Malaria vector control in the Greater Mekong Sub …Greater Mekong Sub-region (GMS). While there has been a steady decline of malaria in the GMS, it is clear that achieving the Sub-regions

Malaria vector control in the Greater Mekong Sub-region:

an independent situation analysis and suggestions for improvement

21 September 2018

Prepared by

Sean Hewitt PhD

VBDC Consulting Ltd.

Upon the request of

World Health Organization

Global Malaria Programme

The author alone is responsible for the content and views expressed in this document and they do not necessarily represent the views, decisions or policies of the World Health Organization.

Malaria vector control in the Greater Mekong Sub-region.

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List of acronyms ACT artemisinin-based combination therapy

ACTMalaria Asian Collaborative Training Network for Malaria

Ae. Aedes

AFRIMS Armed Forces Research Institute of Medical Sciences

AMI Australian Army Malaria Institute

An. Anopheles

ANC ante-natal care

API Annual parasite incidence

APMEN The Asia Pacific Malaria Elimination Network

ASEAN Association of South East Asian Nations

ATSB attractive toxic sugar bait

BCC Behaviour Change Communication

BMGF Bill and Melinda Gates Foundation

BVBD Bureau of Vector-borne Diseases

CDC US Centers for Disease Control and Prevention

CHC Commune Health Centre

CMPE Centre for Malariology, Parasitology and Entomology

CMS Central Medical Supplies

CNM National Center for Malaria Control, Parasitology and Entomology (Cambodia)

COP Chief of Party

Consortium HA Consortium HA

CPMU Central Project Management Unit

CSO Civil Society Organization

DALY Disability Adjusted Life Year

DAMN District Anti-Malaria Nuclei

DCDC Department of Communicable Diseases Control

DDT dichlorodiphenyltrichloroethane

DEET N,N-diethyl-3-methylbenz-amide

DHC District Health Centres

DHIS2 District Health Information System 2

DMC Department for Malaria Control

DMR Department of Medical Research

DOPH Department of Public Health

EHO Ethnic Health Organizations

ELISA enzyme-linked immunosorbent assay

EMG ethnic minority group FHI360 Family Health International

GF Global Fund for AIDS, TB and Malaria

GHG Global Health Group

GMP Global Malaria Programme

GMS Greater Mekong Sub-region

GoC Government of Cambodia


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GoL Government of Lao PDR

GoT Government of Thailand

GoV Government of Viet Nam

GPIRM Global Plan for Insecticide Resistance Management

GPS Global Positioning System

GTS Global Technical Strategy

HC Health Centre

HFCA Health Facility Coverage Area

HIS Health Information System

HIV Human Immuno-deficiency Virus

HPA Health Poverty Action

HR human resources

HSP3 Third Health Strategic Plan

ICC Inter-Country Component

ICEMR International Centers of Excellence for Malaria Research

IDP Internally Displaced People

IEC Information, Communication and Education

IMPE-HCMC Institute of Malariology, Parasitology and Entomology - Ho Chi Minh City

IMPE-QN Institute of Malariology, Parasitology and Entomology - Quy Nhon

IOM International Organization for Migration

IPC Institut Pasteur du Cambodge

IPL Institut Pasteur du Laos

IRD Institut de Recherche pour le Developpement

IRS indoor residual spraying

IT Information technology

ITM Institute of Tropical Medicine (Antwerp)

ITN insecticide treated net

IVCC Innovative Vector Control Consortium

JICA Japan International Cooperation Agency

kdr knockdown resistance

LLHN long-lasting insecticide treated hammock nets

LLIB long-lasting insecticidal blanket

LLIN long-lasting insecticidal net

LSM larval source management

M-HSCC Myanmar Health Sector Coordinating Committee

M&E monitoring and evaluation

MC Malaria Consortium

MCNV Medisch Comite Nederland-Vietnam

MDA Mass drug administration

MEAF Malaria Elimination Action Framework

MHV Migrant Health Volunteer

MIS Malaria Indicator Survey

MMP mobile and migrant populations


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MMW Mobile Malaria Workers

MoA Ministry of Agriculture

MoAFF Ministry of Agriculture, Forests and Fisheries

MoE Ministry of the Environment

MoH Ministry of Health

MoHS Ministry of Health and Sports

MoI-HD Ministry of Interior-Health Department

MoND Ministry of National Defence

MoND Ministry of National Defence

MoPH Ministry of Public Health

MPR Malaria Programme Review

MPW Malaria Post Worker

MPW Malaria Post Workers

NAMRU-2 Naval Medical Research Unit Two

NCC National Coordinating Committee

NGO Non-Governmental Organizations

NHDP National Health Development Plan

NIH National Institutes of Health (United States)

NIMPE National Institute of Malariology, Parasitology and Entomology

NMCP National Malaria Control Programme

NMEC National Malaria Elimination Committee

NSMCE National Strategy for Malaria Control and Elimination

NSP National Strategic Plan

OD Operational District

ODPC Office of Disease Prevention and Control

P. Plasmodium

PAMS Provincial Anti-Malaria Station

PCD passive case detection

PCDC Provincial Centre for Disease Control

PCR polymerase chain reaction

PDR People’s Democratic Republic

PfD Partners for Development

PHD Provincial Health Department

PMC Provincial Malaria Centre

PMI President’s Malaria Initiative

PPHO Provincial Public Health Offices

PPM Public-Private Mix

PPMU Provincial Project Management Unit

PR Principal Recipient

PSI Population Services International

PSK Population Services Kampuchea

PSM procurement and supply management

PTBDU polymer-coated permethrin-impregnated clothing


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QA Quality Assurance

RAI First Regional Artemisinin Initiative grant

RAI2E Second Regional Artemisinin Initiative grant

RCT randomized control trial

RDT rapid diagnostic test

RMT residual malaria transmission

SCF Save the Children Federation, Inc

SEAMEO TROPMED

Secretary General of the Southeast Asian Ministers of Education Tropical Medicine and Public Health

SEARO South East Asia Regional Office

SMRU Shoklo Malaria Research Unit, Mahidol University

SOP Standard Operating Procedures

SR Sub-Recipient

SR Sub-Sub-Recipient

STWG Sub-Technical Working Group

TB tuberculosis

ToR Terms of Reference

TSG Technical Strategy Group

TWGH Technical Working Group for Health

UCSF University of California, San Francisco

UN United Nations

UNOPS United Nations Office for Project Services

URC University Research Company

USAID United States Agency for International Development

VBDC Vector Borne Disease Centre

VBDU Vector Borne Disease Unit

VCPP Vector Control and Personal Protection

VCTWG Vector Control Technical Working Group

VCWG Vector Control Working Group

VHV Village Health Volunteer

VHW Village Health Worker

VMW Village Malaria Worker

VPP Voluntary Pooled Procurement

WCS Wildlife Conservation Society

WHO World Health Organization

WHOPES WHO Pesticide Evaluation Scheme


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Table of contents List of acronyms ..................................................................................................................... 2

Table of contents .................................................................................................................... 6

Executive summary .................................................................................................................. 10

Introduction ............................................................................................................................. 15

Background and rationale .................................................................................................... 15

Objectives ............................................................................................................................. 15

Approach .............................................................................................................................. 16

GMS Context ............................................................................................................................ 17

Epidemiology ........................................................................................................................ 17

Evolving strategies................................................................................................................ 20

Evidence-base for established vector control interventions in the GMS ................................ 20

Insecticide-Treated Nets ................................................................................................... 20

Indoor Residual Spraying .................................................................................................. 23

Cost effectiveness ............................................................................................................. 25

Individual country profiles ....................................................................................................... 27

Cambodia – Country profile ................................................................................................. 27

Policy framework for vector control ................................................................................ 27

Structure of vector control programme ........................................................................... 29

Capacity (manpower, technical capabilities, training, infrastructure and financial resources) ......................................................................................................................... 29

Partners involved in vector control and entomology....................................................... 30

Intra-sectoral and intersectoral collaboration ................................................................. 32

Vector control interventions (LLINs, ITNs and LLHNs; IRS; other).................................... 33

Data systems ..................................................................................................................... 43

Monitoring and evaluation of vector control ................................................................... 43

Vector surveillance ........................................................................................................... 44

Insecticide resistance monitoring..................................................................................... 45

Research and innovation .................................................................................................. 47

Other issues. ..................................................................................................................... 50

Lao PDR – Country profile .................................................................................................... 51






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Data systems ..................................................................................................................... 60





Myanmar – Country profile .................................................................................................. 63







Data systems ..................................................................................................................... 76





Thailand – Country profile .................................................................................................... 78


Structure of vector control programme[80] .................................................................... 81





Data systems ..................................................................................................................... 89





Viet Nam – Country profile .................................................................................................. 93




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Data systems ................................................................................................................... 105

Monitoring and evaluation of vector control ................................................................. 105

Vector surveillance ......................................................................................................... 105

Insecticide resistance monitoring................................................................................... 106

Research and innovation ................................................................................................ 107

Overall findings and recommendations ................................................................................. 109

Challenges to malaria elimination in the GMS ................................................................... 109

Entomology lacks credibility ........................................................................................... 109

Complex and diverse transmission dynamics................................................................. 109

Poor public health entomology capacity ........................................................................ 114

Uneven coverage and poor quality of vector control interventions .............................. 115

Weak surveillance and M&E ........................................................................................... 119

Weaknesses undermining programme management and implementation .................. 119

Extensive knowledge gaps .............................................................................................. 120

Few supplementary vector control options ................................................................... 121

Promising supplementary malaria vector control tools .................................................... 125

Insecticide treated blankets/sheets. .............................................................................. 125

Insecticide treated clothing. ........................................................................................... 125

Topical repellents. .......................................................................................................... 126

Larval source management (LSM). ................................................................................. 127

Ivermectin. ...................................................................................................................... 128

Restricting forest access. ................................................................................................ 129

Insecticidal interventions for the control of zoophilic vectors....................................... 129

Spatial repellents. ........................................................................................................... 129

Push-pull systems. .......................................................................................................... 129

Attractive toxic sugar baits. ............................................................................................ 130

Barrier systems. .............................................................................................................. 130

Improving housing quality. ............................................................................................. 130

Screening forest shelters and swidden farm huts .......................................................... 130

Opportunities for strengthening vector control in the region ........................................... 131

Increase public health entomology capacity .................................................................. 131


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Improve quality and coverage of vector control ............................................................ 132

Strengthen surveillance and M&E .................................................................................. 136

Strengthen programme management and implementation ......................................... 136

Work towards funding equity across countries ............................................................. 138

Close the knowledge gaps relating to residual malaria transmission (RMT) ................. 138

Develop and implement new vector control and personal protection (VCPP) interventions for forest goers......................................................................................... 139

References ............................................................................................................................. 141


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Executive summary All countries in the region have made remarkable progress in terms of malaria burden reduction over the last decade or so, but all are now faced with ‘the law of diminishing returns’, whereby programme inputs yield progressively diminishing impact. Programmes are now in danger of stalling, and most are unlikely to reach their elimination targets without radical change.

Vector control forms an integral part of malaria control and elimination efforts in the Greater Mekong Sub-region (GMS). While there has been a steady decline of malaria in the GMS, it is clear that achieving the Sub-region’s elimination goals will require a strengthening of vector control by more strategic deployment of long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) and by supplementing with additional existing or new tools. The World Health Organization (WHO) commissioned this comprehensive analysis across Cambodia, Lao People’s Democratic Republic (PDR), Myanmar, Thailand and Viet Nam in order to identify the steps required to strengthen vector control in order to accelerate malaria elimination in-line with the WHO Strategy for malaria elimination in the Greater Mekong Sub-region 2015-2030.

The objectives of the situation analyses were to provide a comprehensive overview of the current evidence-base on malaria vector control in each of the five countries, and based on lessons learned, formulate clear actions to ensure more strategic deployment of existing vector control interventions, outline current knowledge gaps in the area of entomology and vector control and ways to close these, and formulate clear actions on where and how improvements to the collection, management and use of data for decision-making could be made. The assessment included a desk-based data and information collation exercise to capture available published and unpublished information on entomology and vector control in the GMS followed by an on-the-ground assessment of practices relating to malaria entomology and vector control. The report provides an overview of malaria related epidemiology, entomology and current vector control and personal protection (VCPP) strategies in the Sub-region and describes the evidence base supporting the use of these strategies. The report then goes on to provide individual country profiles. The final section of the report focuses on overall findings. Challenges to malaria elimination in the GMS are highlighted, promising supplementary malaria vector control tools are described and opportunities for strengthening vector control in the region are discussed.

Overview of malaria related epidemiology, entomology and current vector control and personal protection (VCPP) strategies in the Sub-region. The epidemiology of malaria in the GMS is highly complex. All four species of human plasmodia occur and cases of Plasmodium knowlesi have also been documented in all of the five countries covered by this review. The vast majority of malaria cases are caused by Plasmodium falciparum and Plasmodium vivax. The epidemiology of the disease varies greatly between and within countries and from one population group, or individual, or situation to another. In many cases the different situations and contexts require different malaria control strategies, adapted to suit specific risk groups and vector behaviours, and adjusted to take into consideration local infrastructure and health service coverage.

Malaria elimination efforts in the GMS still face a daunting array of challenges relating to both technical and programmatic issues, to political and economic constraints, to security problems, to environmental changes, to the evolving partner landscape, to the progressive


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disinterest amongst policy makers responsible for allocating funds for malaria elimination and to the lack of engagement by communities in elimination efforts. Multidrug-resistant P. falciparum adds considerably to the frontline difficulties associated with efforts to effectively eliminate the disease.

In the GMS intense malaria transmission is restricted to densely forested areas. The most efficient vectors, members of the Anopheles dirus species complex, cannot survive without dense shade and high humidity. Wherever transmission occurs on a regular basis it tends to be perennial with seasonal peaks associated with rainfall or sometimes linked to internal or cross-border population movements.

There is high biodiversity of vector species in the GMS. Numerous Anopheles species and species complexes are present, and these differ in aquatic habitats, geographic distribution and adult resting, feeding and mating behaviours. Altogether these factors result in extreme entomological complexity in the Sub-region. Much of the information on vector bionomics gathered to-date has been linked to species complexes as single entities, rather than to their constituent sub-species resulting in multiple ambiguities. Vector bionomics vary according to a multitude of factors (sub-species, time, season, moon-phase, climate, weather, land-use, vector control activities, altitude and latitude), and so developing a comprehensive overview of the distribution and role of vectors in the GMS that might be truly useful from a programmatic point of view, would be an impossible task.

Evidence base for established vector control interventions in the GMS. The evidence base supporting the use of insecticide treated nets (ITNs) in the GMS is not as robust as that supporting their use in the majority of African countries. Nevertheless, a number of randomized controlled trials (RCT) conducted in the region have found significant improvements in malaria outcomes as a result of ITNs. Although there is relatively little definitive evidence from RCTs, historical and programmatic documentation has clearly established the impact of IRS, which has been applied effectively to eliminate malaria from parts of Asia, Russia, Europe, and Latin America. A review is currently being undertaken by WHO to consolidate the evidence base beyond RCTs.

Individual country profiles. Country profiles cover policy frameworks for vector control, programme structure, programme capacity, partners, intra- and inter-sectoral collaboration, vector control interventions, data systems, monitoring and evaluation (M&E), vector surveillance, insecticide resistance monitoring, and research and innovation. Summary tables help readers to compare and contrast the various country approaches and situations. There is considerable variability between countries with regard to infrastructure and capacity for entomology and vector control. Some countries are getting stronger and have sound plans for capacity development, while others are getting weaker. LLIN targeting strategies differ considerably between countries (and sometimes within countries) making some inter-country comparisons difficult. Different countries use different models and different assumptions within those models to quantify their LLIN requirements. For example, the LLIN attrition rates used may differ from one country to the next for similar net types and this affects the scale of topping-up operations and therefore the cost effectiveness of the overall approach.

Challenges to malaria elimination in the GMS. Coverage with LLINs has increased dramatically in recent years and according to LLIN quantification models, all of those in settled communities targeted under RAI2E support either already have access or will have


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access to LLINs by the end of 2018. However, recent malaria indicator surveys in the GMS have continued to show very high ownership and use of untreated conventional nets bought from markets. Furthermore, coverage of mobile individuals and mobile groups spending time in forest transmission hot-spots remains poor in many areas.

On occasions, poor quality or inappropriate VCPP tools have likely undermined programmatic impact. The targeting of VCPP interventions is sometimes weak, undermining impact and cost-effectiveness.

All countries in the region are using IRS with synthetic pyrethroids in at least some communities already provided with LLINs despite WHO recommendations that communities be targeted with either LLINs or IRS, but not both.

Persisting civil unrest in southern Thailand and the eastern and northern states in Myanmar and the recent Thai-Cambodia border conflict have all contributed to internal and cross-border population displacements and have hampered the provision of VCPP tools in affected areas.

The really critical gaps in our knowledge in the areas of entomology and vector control relate to residual malaria transmission (RMT). There may be opportunities to accelerate the elimination of RMT if implementers can quickly develop an in-depth understanding of the micro-epidemiology of the disease in persistent transmission foci. This means identifying the likely site of transmission, identifying the vectors, investigating their bionomics and understanding the human behaviour affecting person-vector contact at the transmission site.

While progress has been made in developing the evidence-base for some potential new tools, e.g. repellents, insecticide treated blankets, insecticide treated clothing and ivermectin, this progress has often stopped short of large-scale implementation studies and hence has had limited potential to effect policy change.

The current lack of incentivization of elimination activities in the periphery is undermining programmatic impact.

There appears to be substantial variation in the level of funding from the Global Fund for AIDS, TB and Malaria (GFATM) for malaria control across the GMS.

Promising supplementary malaria vector control tools. There are a number of promising supplementary malaria VCPP tools under investigation in the GMS at present. Insecticide treated blankets and clothing show promise for reducing outdoor transmission. Although topical repellents have been shown not to result in any additional decline in malaria in less endemic communities already protected by LLINs in the GMS, they may still prove valuable for the protection of forest goers visiting high transmission settings, often without alternative VCPP tools. Larval source management (LSM) could also prove useful in specific settings where breeding sites are ‘few, fixed and findable’ and easy to identify, map and treat. Ivermectin also appears to show promise for the control of RMT. Extensive work has been carried out in recent years in Thailand and in Africa and South America, looking at its endectocidal, and transmission blocking sporonticidal and sporozioticidal effects for malaria. Other supplementary tools discussed include restricting forest access, insecticidal/endectocidal interventions targeting livestock for the control of zoophilic vectors, spatial repellents, ‘push-pull systems’, attractive toxic sugar baits (ATSB), barrier systems, house screening and improved housing.


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Opportunities for strengthening vector control in the region. The tools necessary to eliminate malaria transmission in community settings in the GMS are already available: LLINs, ITNs, IRS and early access to diagnosis and appropriate treatment, together with deforestation, urbanization and social development, are more than a match for malaria in these areas. However, poor-quality implementation undermines progress in many places and in settled communities where transmission persists, it is usually poor-quality implementation that is responsible. Implementers need to focus on improving the quality of implementation, while researchers need to focus on developing solutions for RMT in forest settings.

There is an urgent need for entomological capacity development across the region. Efforts should continue to roll-out regional training on mosquito taxonomy, identification and broader aspects of entomology and vector control.

The focus of entomology for malaria needs to be on ‘epidemiology-led problem solving’. It is essential that entomological activities support malaria elimination in a powerful, practical and effective way. Given resource constraints, surveillance must concentrate on ‘focus investigations’ and ‘spot checks’ rather than routine assessments in sentinel sites. Entomologists need to help identify why persistent transmission foci are persistent (e.g. due to insecticide resistance or due to a shift to outdoor biting by vectors) and develop locally appropriate solutions to deal with these persistent foci.

Much more attention should be focused on ensuring that the tools procured by programmes for vector control are locally appropriate in order to maximize utilization and impact. The quantification of VCPP commodities is weak, particularly for forest-goers. There is too much wastage of LLINs in settled communities and insufficient coverage with VCPP commodities for forest-goers.

There must be a far greater sense of urgency and far more action to address the issue of malaria amongst forest-goers. The coverage of VCPP tools amongst formal sector forest-goers is appallingly low in some countries, given their epidemiological importance and the ease with which they can be accessed. This issue needs to be resolved immediately. Much more use should be made of the military and other formal sector forest-goers to support VCPP efforts targeting forest-goers in the informal sector. More use also needs to be made of volunteers drawn from within the different informal sector forest-goer groups.

Focus investigations must place much more emphasis on investigating likely transmission sites and in the case of forest-based transmission, concentrate on finding patient’s co-forest-goers and providing them with appropriate services.

Programmes should place increased emphasis on treating existing conventional nets with quality-assured long-lasting insecticides in preference to distributing additional LLINs to people who are already happily using conventional nets. APLMA and IVCC should work towards ensuring an affordable WHO prequalified long-lasting insecticidal net treatment product is available again as soon as possible. Until a long-lasting formulation is available, countries should use one of the several standard (not long-lasting) prequalified net treatment products available at present.

Funding partners should consider supporting a long-term high-level technical advisor at regional level, supported by a team of long-term mid-level technical advisors at country


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level, plus international volunteers to strengthen capacity in weaker provinces or districts at the forefront of elimination efforts.

In most countries in the GMS vector control infrastructure and human resource capacity need considerable strengthening, both in support of malaria elimination and in order to effectively deal with vector borne diseases other than malaria in future. Most countries are capable of building up their vector control infrastructure and human resource capacity using their domestic budgets. They need to be convinced to do so.

Programmes need to work with malaria stakeholders to develop and implement realistic incentives and allowances for those implementing malaria elimination activities.

Programme guidance at country level needs to be much more explicit and tailored to the individual country in question. It needs to be more practical and locally appropriate, taking human and financial resource constraints into consideration.

There is a critical need for ongoing evaluation of current investments in malaria elimination in the GMS. Programme evaluations should cover all implementers annually. Programmes must set strict targets for utilization of LLHN and other VCPP tools by formal and informal forest-goers.

Large-scale multi-country ‘trials’ with one or more of the most promising new tools should be initiated as soon as possible. WHO and other technical partners should lobby for research funding to focus on tackling RMT as an absolute priority.


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Introduction This situation analysis was conducted for the World Health Organization’s (WHO) Global Malaria Programme (GMP) in 2018.

Background and rationale Vector control forms an integral part of malaria control and elimination efforts, including the WHO Strategy for malaria elimination in the Greater Mekong Sub-region 2015-2030. However, the majority of data on the effectiveness of core interventions has been generated in Sub-Saharan Africa and is not necessarily of relevance to the GMS1 where malaria is transmitted by anopheline vectors that differ considerably in ecology and behaviour from those in Africa. There is some evidence that the core interventions highly effective in controlling African anopheline vectors – LLINs and IRS – may achieve less impact in the GMS due to low usage, propensity of certain populations to stay outside of the primary residence such as in forest farms, and the early evening or outdoor biting behaviour of the major malaria vectors. While there has been a steady decline of malaria in the GMS, it is clear that achieving the Sub-region’s elimination goals will require a strengthening of vector control by more strategic deployment of LLINs and IRS and by potentially supplementing with additional existing or new tools.

Vector control in the GMS will need to be underpinned by a more robust understanding of vector bionomics and of past and present vector control experiences in countries of the Sub-region. At present, there is relatively limited recent data on entomology and vector control available from the GMS, and the available data are generally not accessible in a consolidated format. Comprehensive national assessments of vector distribution are lacking for most countries and, with a few exceptions, insecticide susceptibility data are sparse and insufficient.

To identify the steps required to strengthen vector control in the GMS in order to accelerate malaria elimination in line with the WHO Strategy for malaria elimination in the Greater Mekong Sub-region 2015-2030, WHO commissioned this comprehensive analysis across Cambodia, Lao PDR, Myanmar, Thailand and Viet Nam. Yunnan Province in China, which is also part of the GMS, was excluded due to time constraints and due to the advanced nature of its malaria elimination effort.

Objectives The objectives of the situation analyses were to provide a comprehensive overview of the current evidence-base on malaria vector control in each of the five countries assessed, including existing methods of data collection, collation and management to guide decision-making, and based on the in-depth understanding generated:

a. formulate some clear actions to ensure more strategic deployment of existing vector control interventions

b. outline current knowledge gaps in the area of entomology and vector control and ways to close these

c. formulate clear actions on where and how improvements to the collection, management and use of data for decision-making could be made

1 For the present assessment the GMS is considered to consist of Cambodia, Lao People's Democratic Republic (Lao PDR), Myanmar, Thailand, and Viet Nam.


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Approach The following methodology was applied:

1) A desk-based data and information collation exercise, drawing on expertise in national programmes and their implementing partners (including research and academic institutions) to capture available published and unpublished information on the implementation of vector control interventions, as well as on vector bionomics and insecticide susceptibility of the local vectors.

2) An on-the-ground assessment of routine collection and reporting systems for entomological and vector control data, and how these data are being used to inform decision-making.

3) Preparation of a comprehensive situation analysis document outlining current coverage and usage of vector control interventions, knowledge in the area of malaria entomology and vector control, as well as critical knowledge gaps, and proposing clear actions on where and how improvements could be made based on currently available information to strengthen vector control in the GMS.


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GMS Context Epidemiology The epidemiology of malaria in the GMS is highly complex. All four species of human plasmodia occur and cases of P. knowlesi (a zoonosis associated with macaques but sometimes transmitted to humans in deep forest areas) have also been documented in all of the five countries covered by this review [1–6]. The vast majority of malaria cases are caused by P. falciparum and P. vivax. The epidemiology of the disease varies greatly between and within countries and from one population group, or individual, or situation to another. In many cases the different situations and contexts require different malaria control strategies, adapted to suit specific risk groups and vector behaviours, and adjusted to take into consideration local infrastructure and health service coverage. In addition malaria control strategies must be sufficiently reactive and innovative to deal with the rapidly evolving environmental conditions resulting from the large number of economic development projects currently underway[7,8].

During the last decade there has been an overall improvement in the malaria situation in the GMS. However, the burden of disease remains unacceptably high and in Cambodia and Myanmar the situation is particularly serious (figure 1). Furthermore, the risk of a significant resurgence of malaria remains real in populations residing in areas that have become free of malaria but where primary vectors persist.

Figure 1. Cases of malaria in the Greater Mekong Sub-region during 2015.


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The relative importance of vivax malaria is increasing region-wide especially in areas where control efforts are having a significant impact on falciparum malaria (which is more amenable to control on account of the fact that it does not have difficult to treat liver stages like vivax malaria).

Malaria control and elimination efforts in the Sub-region still face a daunting array of challenges relating to both technical and programmatic issues, to political and economic constraints, to security problems, to environmental changes, to the evolving partner landscape, to the progressive disinterest amongst policy makers responsible for allocating funds for malaria elimination and to the lack of engagement by communities in elimination efforts. Multidrug-resistant P. falciparum adds considerably to the frontline difficulties associated with efforts to effectively eliminate the disease.

In the GMS intense malaria transmission is restricted to densely forested areas. The most efficient vectors, members of the An. dirus species complex, cannot survive without dense shade and high humidity. Deforestation therefore generally leads to substantially reduced malaria transmission. The next most efficient vector, which is probably the most important in terms of transmission, is An. minimus (senso lato). This species is also primarily forest-based but can survive in less densely shaded forest, forest fringes and in the bamboo thickets that commonly persist post-deforestation. Secondary vectors such as Anopheles maculatus and Anopheles aconitus occur in areas of open farmland and in flooded rice fields and sporadic secondary transmission can take place in these areas as a result of imported cases. Wherever transmission occurs on a regular basis it tends to be perennial with seasonal peaks associated with rainfall or sometimes linked to internal or cross-border

Box 1. Main population groups at risk of malaria in the GMS.

Static populations

• Established villages (ethnic minority groups (EMGs) and ethnic majority).

• Refugee camps.

• New settlements.

• Camps associated with large-scale construction projects (dams, bridges, mines, etc.).

Mobile and migrant populations

• Traditional slash-and-burn and paddy field farming communities visiting their forest farms (commonly EMGs).

• Seasonal agricultural labourers (particularly those moving between low-endemic plains areas and high-endemic forested foothill areas).

• Defence and security services (Army, Police, Border Guards).

• Forest workers in the formal sector (Forest Rangers, forest/wildlife conservation Civil Society Organizations).

• Forest workers in the informal sector (hunters, people gathering forest products such as precious timber, orchids, medicinal plants, fungi, amber, resin for the manufacture of varnish, construction timber, charcoal, rattan or bamboo).

• Transient or mobile camps associated with commercial projects (road construction, large-scale logging).

• Formal and informal cross-border migrant workers (legal and illegal workforces).


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population movements.

The main population groups at risk of malaria in the GMS are presented in Box 1. The epidemiology of the disease varies considerably from one group to another. The level of malaria risk for each of these groups is dependent on a number of location-specific factors, including degree of endemicity, accessibility to malaria commodities and services and health system strength. Marginalized mobile and migrant populations (MMPs) and ethnic minority groups (EMGs) working or living in the forest and on the forest-fringes carry the greatest burden of disease.

Mobile populations are proving particularly difficult to target with effective interventions for a number of reasons: Many actively avoid contact with authorities either because they are illegal immigrants, or are breaking national rules relating to internal migration, or are involved in illegal activities of some sort. Added to this, many are driven only by the need to make money and so getting accurate information for health action from them is a sensitive and complex multi-sector task. A team working in Cambodia recently developed a population movement framework to inform strategies for malaria control and elimination and improve the targeting of behaviour change and outreach interventions for MMPs[9].

Outdoor transmission is a key feature of the epidemiology of malaria in the GMS, limiting the effectiveness of key interventions for vector control and personal protection and hampering further progress with malaria control and elimination efforts.

Figure 2. Numbers of ACTs failing in the GMS in 2017[10].

Antimalaria drug resistance in the GMS. In 2006, artemisinin resistant P. falciparum malaria was reported in eastern Cambodia and by 2013, confirmed or suspected artemisinin


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resistance had been identified in another four GMS countries. Resistance to various artemisinin-based combination therapy (ACT) has now been documented in all of the five countries covered by this review and in Cambodia resistance has been documented for five different ACTs (figure 2).

Evolving strategies Vector control strategies, such as use of ITNs or the more recently developed LLINs, as well as IRS, together with case management (prompt access to diagnosis and effective treatment) are critical for reducing malaria morbidity and mortality and reducing malaria transmission. In all areas, especially as programmes approach elimination, it is important to ‘Ensure universal access to malaria prevention, diagnosis and treatment’ for at-risk populations, as emphasised in Pillar 1 of the WHO Global Technical Strategy (GTS) for malaria[11]. WHO’s ‘A framework for malaria elimination’ highlights programme actions along the continuum of malaria transmission, from very high to very low, with emphasis on preparation for successive steps, stressing the importance of iterative planning with anticipation of transitions and evolving approaches. In addition, it reiterates the importance of adapting and tailoring interventions to certain areas within a country[12]. In-line with this WHO guidance, programmes across the GMS are evolving gradually to meet the needs associated with elimination. However, targets are looming2, and most countries need to do more if they are to achieve their elimination goals in a timely manner.

Evidence-base for established vector control interventions in the GMS Vector control remains the most generally effective measure to prevent malaria transmission and therefore is one of the four core interventions of the GTS[11]. The principal objective of vector control is the reduction of malaria morbidity and mortality by reducing levels of transmission.

ITNs, generally in the form of LLINs, form the core of malaria prevention efforts in all of the five countries covered by this review. All five countries also use IRS as an emergency response to outbreaks and confirmed transmission foci and most use it on a very limited scale for routine malaria prevention. Routine application is usually targeted at high transmission areas with low ITN coverage. The quality of implementation is variable. All countries also support communication measures to maximize utilization of malaria prevention services by target populations in order to enhance programme impact.

Insecticide-Treated Nets ITNs have been shown to be highly effective in reducing malaria morbidity and mortality by as much as 50% and 17% respectively among children in areas of stable transmission in sub-Saharan Africa [13]. The evidence base supporting the use of ITNs in the GMS is not as robust as that supporting their use in the majority of African countries. Nevertheless, a number of RCTs conducted in the Sub-region have found significant improvements in malaria outcomes as a result of ITNs. In a study on the Thailand-Myanmar border, children aged 4-15 (n = 350) who were given ITNs had 41% fewer symptomatic episodes and a non-statistically significant 20% relative reduction in prevalence of P. falciparum compared to those with untreated nets[14]. A study in eastern Thailand showed a 41% reduction in the

2 Elimination targets in the five GMS countries covered by this review: Cambodia: P. falciparum by 2020, all species by 2025; Lao PDR: P. falciparum by 2025, all species by 2030; Myanmar: all species by 2030; Thailand: all species by 2025; and Vietnam: P. falciparum by 2025, all species by 2030.


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incidence of mild clinical episodes of P. falciparum and P. vivax in migrant workers (n=261) provided with ITN compared to untreated nets[15]. A Cochrane review conducted in 2004, which included findings from three RCTs in Asia (the two in Thailand cited above plus one in Pakistan) concluded ‘In Asia (areas with low malaria transmission, entomological inoculation rate <1), the use of ITNs significantly reduced the number of clinical episodes due to both P. falciparum and P. vivax’.

A large-scale cluster-RCT conducted in 34 villages in northeast Cambodia (population 10,726) in 2001-2 revealed a non-statistically significant reduction of 28% in P. falciparum incidence overall and a 35% reduction in P. falciparum incidence in children under 5-years old in communities provided with ITNs compared with communities not provided with any nets[16].

Despite important differences in vector behaviour, transmission intensity and malaria burden, these estimates of ITN effectiveness from the GMS are similar to those seen in trials in Africa.

The Malaria Consortium (MC) summarized all published reports found on efficacy of ITNs and LLINs in the GMS countries, and found 11 papers supporting some effectiveness of ITNs and treated hammocks or hammock nets[13,14,16–25] and just one paper from western Myanmar showing no effect due to the local occurrence of Anopheles annularis, a secondary malaria vector [26].

ITNs are primarily a personal protection measure, however, there is some evidence from trials in Africa that high coverage rates (often quoted as a critical threshold of 80%) also provide a ‘community effect’ reducing overall transmission so that people without nets gain some level of protection[27]. WHO-GMP has recently commissioned a review of evidence on this ‘community effect’.

There is a strong culture of mosquito net use in the GMS where they have been used traditionally for many years, mainly for privacy and protection against nuisance mosquitoes. ITNs have been in increasingly widespread use by National Malaria Control Programme (NMCPs) since the 1990s. During the 2010s, conventional ITNs were largely superseded by LLINs everywhere in the GMS, except in Viet Nam[28] where LLINs were only adopted on a large scale in 2014.

LLINs are a specific type of ITNs that are factory-treated to have insecticide either incorporated into or coated onto filaments and designed to gradually release insecticide to the surface of the filament. As a result, they do not require re-treatment and are expected to retain biological activity for a minimum of 3-years of recommended use under field conditions [29].

The need for frequent retreatment with conventional insecticides was a major limitation in getting to scale with ITNs in the early days of this intervention and so the move to LLINs was seen as a very significant advance, and LLINs were heavily promoted through normative guidance.

Nevertheless, private ownership of untreated nets was high in many parts of the Sub-region and so most NMCPs provided retreatment services during bednet distribution campaigns, whereby members of the target population who preferred to use their own conventional nets could have these treated initially with a conventional and then with a long-lasting formulation of insecticide free-of-charge. The long-lasting conventional net treatment


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formulations were however expensive (costing as much as an LLIN but lasting for only one year rather than three) and utilization dwindled as funding diminished and NMCPs were forced to make cuts. The two products for long-lasting treatment of conventional nets that were originally recommended by WHO’s Pesticide Evaluation Scheme (WHOPES) - ‘ICON® Maxx’ and ‘KO-Tab 1-2-3®’ – went out of production. Myanmar, Thailand and Viet Nam continue to provide net retreatment services alongside their LLIN campaigns using various synthetic pyrethroid formulations3.

Delivery approach. Different countries in the region have adopted different approaches to LLIN delivery but all provide their core bednet services free-of-charge for all those residing in target areas. Most strategies are now based on periodic mass distribution campaigns (directed by NMCPs, managed by local health services - with the support of Civil Society Organizations (CSO) where present - and supported by community volunteers), the frequency of which depend on the estimated viable life of the LLINs used. Some countries organize mass distributions of LLINs nationwide every few years while others organise mass distributions in different areas each year on a cyclical basis depending on logistical constraints. These mass distributions are sometimes supplemented by ongoing complementary continuous distribution to maintain coverage. Top-up operations aim to replace lost or damaged nets and provide nets for pregnant women and new settlers, with delivery through health facilities, antenatal services and special campaigns as appropriate. An Africa-focused model developed recently indicates that in high transmission settings, supplementing a universal mass campaign with extra delivery through ante-natal care (ANC) services should achieve a 1.4 times higher mortality reduction than campaign delivery alone[30].

LLIN targeting strategies differ considerably between countries (and sometimes within countries) making some inter-country comparisons difficult. Until recently most NMCPs in the GMS targeted vector control operations based on proxy indicators of endemicity such as proximity to forest or on some more complex stratification of risk, considering ecological and entomological factors as well as epidemiological ones. Now all countries target LLIN operations based on Annual Parasite Incidence (API), but they still use different thresholds and base API on data from different time periods. The units of stratification (village, commune, district, township, health facility catchment area) also differ, potentially having a profound effect on the relative cost-effectiveness and impact of interventions in different countries. In the recent past, targeted coverage (nets per person), netting material, insecticide, insecticide formulation and method of attachment to the netting fibres, and net size also sometimes varied between countries, but with the introduction of the GFATM’s Voluntary Pooled Procurement (VPP) mechanism, these factors are now standardized across the region for the vast majority of LLINs procured4.

With LLINs the timing of the intervention (distribution) is not as critical as it is with IRS (or conventional ITNs using insecticide without ‘binder’5). This is a major advantage as it removes the operational demands associated with rapid deployment.

3 Viet Nam uses lambdacyhalothrin 2.5 CS (WHO pre-qualified as ICON CS-ITN kit3) and Thailand uses ‘deltamethrin 25%

WT’ (a locally produced net treatment tablet which is not WHO prequalified). 4 GFATM procures the vast majority of LLINs used in the region. Some LLINs are however procured separately by PMI when requested by national programmes. 5 The use of a ‘binder’ with insecticide for treating ITNs gives the insecticide long-lasting properties.


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Quantification of requirements. Different countries use different models and different assumptions within those models to quantify their LLIN requirements. For example, the LLIN attrition rates used may differ from one country to the next for similar net types and this affects the scale of topping-up operations and therefore the cost effectiveness of the overall approach. These assumptions have generally not been validated and are not necessarily aligned with WHO recommendations[29].

Large-scale unforeseen population movements may sometimes undermine quantification of LLIN requirements and well-set plans for distribution campaigns are sometimes thrown off course by funding and procurement bottlenecks.

Indoor Residual Spraying IRS is the application of long-acting insecticides to the walls and ceilings of houses and animal sheds in order to kill adult vector mosquitoes that land and rest on these surfaces. The primary effects of IRS are to reduce the lifespan of vector mosquitoes so that they do not have time to transmit malaria parasites6 from one person to another, and to reduce the population of vector mosquitoes. Some insecticides also repel mosquitoes and so reduce the number of mosquitoes entering the sprayed room thereby reducing human-vector contact. All of these effects result in reduced vectorial capacity.

Although there is relatively little definitive evidence from RCTs, historical and programmatic documentation has clearly established the impact of IRS. It has been applied effectively to eliminate malaria from parts of Asia[31], Russia, Europe, and Latin America[32,33]. A review is currently being undertaken by WHO-GMP to consolidate the evidence base for IRS beyond RCTs. IRS is still used to control malaria on a large scale especially in sub-Saharan Africa and is considered a core malaria vector control intervention. A recent review concluded that the evidence from comparisons of IRS versus no IRS in unstable malaria settings confirmed that IRS reduces malaria incidence and prevalence[34]. One RCT in India demonstrated a protective efficacy of 31% in terms of incidence and 28% in terms of prevalence[35] while another in Pakistan demonstrated a protective efficacy of 88% (95% CI 69 to 96%) in terms of incidence and 76% in terms of prevalence[36]. The review team also found that some limited data suggested that ITNs give better protection than IRS in unstable areas, but concluded that more trials would be needed to compare the effects of ITNs with IRS, as well as to quantify their combined effects[34].

In the final years of the ‘Global Malaria Eradication Program’ (which lasted from 1955 to 1969), IRS activities were stopped in most countries following the development of resistance to DDT7. Recently, IRS has re-commenced across the region, primarily for responsive use in the event of confirmed transmission foci or outbreaks, but also for mass preventive treatment in some settings such as some ethnic minority communities in Viet Nam where LLINs are not popular.

Combining ITNs with IRS. A 2009 review of data from household surveys and studies of non-experimental design concluded that, while it was not possible to draw firm conclusions regarding the benefits of a combined vector control strategy based on ITNs and IRS, their analysis provided remarkably consistent evidence of added protection offered to individuals who sleep under a mosquito net or ITN in an IRS-treated house[37]. Despite several RCTs it

6 From becoming infected it generally takes at least 9 days for a mosquito to become infective to humans (longer at lower temperatures). 7 DDT is dichlorodiphenyltrichloroethane.


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remains unclear whether it would be appropriate to combine large-scale deployment of ITNs with large-scale deployment of IRS[38]. WHO issued guidance on combining IRS with bednet interventions in 2014 based on a review of four studies (three of which were unpublished)[39]. Three of the trials reviewed showed no significant additional protective efficacy from combining IRS and LLINs compared to LLINs alone. One trial (in Tanzania) showed significant added protection of the combination against malaria when a non-pyrethroid insecticide was used for the IRS. Modest LLIN coverage and high levels of pyrethroid resistance in the Tanzania study site may have contributed to the boosting effect of IRS. A more recent cluster RCT conducted in an area of Sudan characterised by pyrethroid-resistant, carbamate-susceptible malaria vectors, which compared the impact of LLINs alone or in combination with deltamethrin-based IRS in the first year and bendiocarb-based IRS in the two subsequent years, showed no added value of pyrethroid IRS, but significant added value for bendiocarb IRS [interaction incidence rate ratio = 0.55 (95% CI: 0.40–0.76; P <0.001)][40]. The incremental cost of using the carbamate insecticide was US $0.65 per person protected per year, which is considered acceptable by international standards.

All of these trials were conducted in African countries and so extrapolation of evidence to GMS countries is of limited value, given the differences in the behaviour and vectorial capacities of local vectors. Even if a significant effect could be demonstrated, budgets for malaria control have been tightening in the GMS and so the cost of combining both approaches seems likely to be prohibitive in most circumstances. The use of combined IRS and LLIN for a limited period, followed by LLIN alone once transmission rates have been reduced could however prove practical in settings that are more endemic.

WHO recommends that ‘All programmes for malaria elimination should establish and maintain their capacity to conduct IRS for rapid clearance of transmission foci and as an adjunct or targeted control measure, even where ITNs/LLINs are the core vector control strategy…’[24]. In order to minimize pressure for the selection of pyrethroid resistant vectors, WHO guidance states that ‘If LLINs and IRS are to be deployed together in the same geographical location, the IRS should use non-pyrethroid insecticides. [39]’.

Delivery mechanisms. IRS in the GMS can be broadly divided into two types: ‘mass preventive’ and ‘focal responsive’. Mass preventive IRS is often a routine response in areas of consistently high annual incidence. Spraying is generally carried out at regular intervals of six or twelve months depending on the length of the transmission season and the residual efficacy of the insecticide used. In contrast, focal responsive IRS is an emergency response to malaria outbreaks in endemic areas or to confirmed transmission foci in areas targeted for elimination. Focal responsive IRS normally relies on a single round of spraying. In the case of malaria outbreaks, all households in the outbreak community are usually targeted, whereas in the case of confirmed transmission foci, spraying is usually restricted to households within a given distance of each confirmed case.

The residual efficacy of IRS varies from around two to twelve months, depending on the insecticide used and the type of surface treated (e.g. mud, brick, thatch or wood)8, so to ensure maximum effect campaigns should be carried-out immediately before the

8 Depending on dosage and substrate the residual efficacy of various public health insecticides can be expected to fall in

the following ranges: DDT – 6 to 12 months; pyrethroids – 4 to 6 months; organophosphates and carbamates – 2 to 6 months.


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transmission season. WHO has prequalified 22 insecticide compounds/formulations for use in IRS (though not all insecticide classes that have a policy recommendation have an associated prequalified product available e.g. DDT)[41]. The choice of insecticide should depend on its registration status in-country, the housing construction, the duration of the malaria transmission season, and susceptibility of local Anopheles mosquitoes to the insecticide.

IRS requires strong management for planning, organization and implementation. For maximum impact it is also heavily dependent on community acceptance. A high degree of cooperation is required from local residents who must permit access to their homes and remove furniture prior to spraying. IRS programs present numerous logistical and operational challenges. Vehicles are required to transport the spray teams, insecticide and equipment to the targeted areas.

IRS programmes need to aim to achieve at least 80% coverage of the at-risk population in the target area for the intervention to have the desired impact

Implementation of IRS in the GMS. According to national strategic plans, Cambodia, Lao PDR, Myanmar, Thailand and Viet Nam all conduct mass preventive IRS once or twice a year (depending on the duration of the transmission season) in endemic areas, generally targeting residents in communities not covered by GFATM supported LLINs. In fact, the coverage of mass preventive IRS is generally very low, with all countries placing much greater emphasis on LLINs. In theory, all five GMS countries assessed conduct responsive focal IRS either in the event of ‘outbreaks’ in more endemic areas or when ‘active transmission foci’ are identified in elimination areas. In fact, the use of focal responsive IRS is also very limited and in most GMS countries technical capacity is sub-optimal, standard operating procedures are either in the process of being field-tested and fine-tuned, or not yet available, and thresholds for implementation are not well defined.

Behavioural changes in vectors in response to control efforts. The evidence that the use of IRS and mosquito nets may select for earlier biting is mounting[42–44]. While early biting could be expected to reduce the effectiveness of ITNs, this has not yet been substantiated[42]. The general consensus amongst vector control specialists is that despite these limitations the protective efficacy of ITNs remains sufficiently high to make them a key tool for malaria prevention in the GMS[45], but only where vectors persist.

Cost effectiveness Given the size of the malaria disease burden and the scarcity of funding, interventions need to be deployed in a manner that is cost effective, equitable and sustainable in order to optimize resource allocation.

ITNs/LLINs. WHO recommends LLINs as one of the most cost-effective interventions against malaria. Either free or highly subsidized distribution is recommended to maximize and maintain high coverage, and also to gain the benefits of community protection [27,46]. In 22 studies of the cost effectiveness of ITN/LLIN programs analysed in a recent review[47], the median financial cost per person protected per annum was $2.31 (range $0.92-$10.00) in 2011$, and the median cost per DALY saved was $28.30 (range $8.54-115.28) which is cost effective relative to other public health interventions. The commodity cost of LLINs has decreased significantly since 2011, so the cost effectiveness has increased significantly since this review of cost effectiveness was conducted.


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WHO also recommends that LLINs be purchased in preference to ITNs, as the costs per death averted and per DALY saved for LLINs were shown to be half of the equivalent costs for conventional ITNs9[48]. However, the ITN costings were based on programmes purchasing conventional nets for target beneficiaries. Where ownership of conventional nets is high, such as in the GMS, the situation would be quite different.

IRS. Only one cost effectiveness study on IRS has been conducted in the GMS[20] but this was in the 1990s and is therefore quite outdated. Based on studies primarily in Sub-Saharan Africa, the median financial cost of protecting one person for one year with IRS is estimated to be $7.11 (range 2.33-13.47) in 2011$ and the cost per DALY saved to be $150 ($141-157)[47]. Yukich et al. estimated that the cost effectiveness of IRS is over three times more expensive than LLINs[48], but nonetheless IRS remains cost effective relative to other public health interventions. It should be noted that the absolute cost of IRS is likely to go up with increasing use of new and non-pyrethroid IRS formulations in response to insecticide resistance.


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Individual country profiles Cambodia – Country profile Over the last decade Cambodia has made significant, although somewhat sporadic progress in malaria control. Malaria deaths have decreased dramatically from 241 in 2007[49] to 1 in 2017[50]. The number of reported malaria cases declined from 221,193 in 2007 to 45,911 in 2017. However, caseload appears to be on the rise. With just 23,627 cases reported in 2016, the number of reported cases rose by 94% in 2017 relative to 2016, and the caseload for February-April 2018 was higher than it has been for the last 5 years, indicating that malaria burden in 2018 could be considerably higher than in 2017. Fortunately, the proportion of cases caused by P. falciparum during this period was very much lower than previously recorded, which may bode well for falciparum malaria specific elimination targets.

The spread of artemisinin resistance and difficulties addressing forest-based transmission remain serious challenges to the achievement of national elimination goals. Implementation of the Malaria Elimination Action Framework (MEAF) in GFATM supported provinces has been severely disrupted over the last several years as a result of issues affecting funding flow.

Malaria is endemic in 21 out of Cambodia’s 25 provinces, with incidence highest in the north-east. Increasingly malaria is becoming an occupational disease predominantly affecting men.

Policy framework for vector control In 2011, the Prime Minister of Cambodia endorsed the ‘National Strategic Plan (NSP) for Elimination of Malaria for 2011–2025’. This strategy is based on the following goals:

• Short-Term (by 2015) - To move towards pre-elimination of malaria across Cambodia with special efforts to contain artemisinin-resistant P. falciparum malaria.

• Medium-Term (by 2020) - To move towards elimination of malaria across Cambodia with an initial focus on P. falciparum malaria and ensure zero deaths from malaria.

• Long-Term (by 2025) - To achieve phased elimination of all forms of malaria in Cambodia.

In 2014 the GMS developed a coordinated strategy for malaria elimination by 2030. As a result, the National Malaria Program developed the MEAF 2016 -2020 to update national strategies within the NSP and align with the GMS Malaria Elimination Strategy.

The MEAF identifies 3 programme phases which are presented in figure 3:

Figure 3: Phased approach to malaria elimination in Cambodia


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The MEAF is fully aligned with ‘The Third Health Strategic Plan (HSP3) 2016-2020’, which is the Government of Cambodia’s (GoC) strategic management tool to guide the Ministry of


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Health (MoH) and all health institutions as well as concerned stakeholders to effectively and efficiently use their available resources to translate health strategies into action.

Structure of vector control programme The National Center for Malaria Control, Parasitology and Entomology (CNM), which is responsible for overseeing the implementation of the MEAF, sits within MoH (figure 4). Although leadership for malaria control and elimination activities in Cambodia rests at the central level, with the decentralization of MoH, Provincial Health Department (PHD) and Operational District (OD) Malaria Supervisors are involved with planning and implementing activities in the periphery. Village Malaria Workers (VMWs), Mobile Malaria Workers (MMWs), and local authorities have been deployed to improve the availability and accessibility of malaria services, including early diagnosis and treatment, LLIN distribution, and malaria health education.

Figure 4. Structure of the National Malaria Program within the Ministry of Health, Cambodia

Capacity (manpower, technical capabilities, training, infrastructure and financial resources) The programme has a number of critical weakness affecting entomology and vector control including manpower constraints (three MSc level entomologists at CNM but only 1 actively involved in entomology and no trained staff in the periphery), financial constraints and burdensome administrative issues (low salaries, lack of incentives and inadequate reimbursement of costs) undermining staff morale. The PMI ‘VectorLink Project’ focusing on capacity development in support of entomological surveillance and monitoring to help


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inform vector control programme decisions shows promise, although initially efforts will focus on just 3 provinces.

Partners involved in vector control and entomology CNM-MoH has established a central level coordination structure – the National Coordinating Committee (NCC) – to oversee the coordination of partners during the planning and implementation of mass LLIN distribution, in an effort to optimize use of relevant in-country skills, personnel and resources. The NCC comprises a broad range of partners including public and private sector, civil society and faith-based organizations and other technical and financial organizations supporting MoH.

The United States Agency for International Development (USAID)/President’s Malaria Initiative (PMI) supports the implementation of malaria elimination efforts in Battambang and Pursat through an annual grant of approximately US$3 million to the University Research Company (URC). This support covers both vector control and related entomology (including the new ‘VectorLink Project’ – see below). PMI has also financed valuable technical assistance delivered through WHO, including that related to the recent development of an entomology surveillance plan (see below). PMI support for malaria elimination efforts may expand to cover 2-3 provinces in 2020, in which case its annual budget could rise to US$10 million.

PMI staff in Cambodia consider that coverage of LLINs delivered through mass distributions is excessive and should be further restricted to cover only communities with indigenous transmission.

At present URC uses GFATM LLINs for mass distribution and procures its own PMI funded LLINs for continuous distribution through routine channels. In future, URC may procure all of the LLINs required to meet the needs of its target population. Distribution is carried out according to national guidelines.

Work in URC areas has progressed well during the last three years, unaffected by the problems undermining efforts in GFATM supported areas.

Malaria control and elimination efforts in the rest of the country are currently funded by GFATM’s second Regional Artemisinin Initiative grant (RAI2E) (approximately US$20 million per year for Cambodia). The GFATM grant is managed by the Principal Recipient (PR), the United Nations Office for Project Services (UNOPS) and implementation is managed by a number of Sub-Recipients (SRs) operating in different provinces or dealing with specific work areas, e.g. the private sector in the case of Population Services International (PSI)/Population Services Kampuchea (PSK). The SRs dealing with specific geographical areas include the CNM and a number of CSOs. Partners for Development (PfD), Health Poverty Action (HPA) (formerly Health Unlimited) and Family Health International (FHI360) all provide management support for malaria control activities in their selected provinces. This support covers LLIN distribution, associated community mobilization and communication efforts, case-based surveillance (which includes entomological assessment) in elimination areas. Another SR, MC, provides technical support for monitoring and evaluation (M&E) including management of periodic large-scale malaria indicator surveys, development of surveillance systems, operational research and behaviour change communication (BCC). Until recently another SR, PSI/PSK, supported the bundling of conventional mosquito nets with a long-lasting insecticide treatment kit. At present, PSI/PSK focus in Cambodia is on


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research relating to LLIN user preferences (see below), since all of its Public-Private Mix (PPM) related work for malaria has been placed on hold by CNM/GoC.

Organizations collaborating on malaria entomology in Cambodia include ‘Institut Pasteur du Cambodge’ (IPC), ‘Institute of Tropical Medicine’ in Antwerp (ITM), ‘Naval Medical Research Unit Two’ (NAMRU-2) and ‘Abt Associates’.

Vector control related and entomological research at IPC is focused on supporting and evaluating the impact of MEAF strategies and transmission of Plasmodia by vector mosquitoes (see ‘Research and innovation’ below).

ITM has provided valuable training in recent years, including to Master’s level. It has also collaborated on research in the past (including MALVEC Asia and a large-scale RCT assessing the effectiveness of topical repellents (picaridin) in community settings[51]) and continues to conduct polymerase chain reaction (PCR)-based screening of samples for the CNM entomology team.

NAMRU-2 is working closely with CNM on insecticide resistance in five provinces. They have also been involved in vector mapping (along with MC and IPC). The data from the various groups has not been consolidated into a single system yet. NAMRU-2 is in the process of building a new insectary at CNM, which will result in improved biosecurity.

WHO provides technical assistance through a number of long-term advisors at country and regional level, as well as through short-term consultants, as required.

Abt Associates, a major American business and government research, technical assistance, and consulting company, manages the USAID-funded ‘Vector Control Task Order 1’, which supports the malaria related work of PMI and USAID. The company is in the process of recruiting a senior international entomologist to support the implementation of the PMI ‘VectorLink Project’ as ‘Chief of Party’ (COP). During its initial stages this project will be supporting entomological surveillance and monitoring to help inform vector control program decisions in three provinces where malaria is characterized by forest-based transmission: Kampong Chnang (close to Pursat), Stung Treng and Mondulkiri. The VectorLink team will work in close collaboration with the entomology team at CNM. The plan is apparently to build capacity during the first two years of the project through the implementation of routine surveillance, before moving on to problem solving. Given the countries’ looming elimination targets, it might be more appropriate to build capacity while problem solving. The Terms of Reference (ToR) for the COP are broad and include a number of activities of limited operational significance. These ToRs should be reviewed in light of this report and revised in-line with the CNM’s plan for ‘Entomological surveillance for malaria elimination in Cambodia 2017-2021’ described below.

The ‘Cambodia Research Consortium’ was established in 2014 to expedite research for malaria elimination as part of the emergency response to artemisinin resistance[52]. It was designed to serve as a framework for partners, stakeholders and researchers to share research projects, information and results, and to promote the goals of CNM. This would appear to offer a good model to streamline research efforts in other countries in the GMS and across the region. However, while the approach makes sense, the consortium has so far failed to gain much traction. As with many initiatives of this kind, success often depends on finding the right character to drive the process.


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Intra-sectoral and intersectoral collaboration The MEAF places heavy emphasis on the importance of adopting a multisectoral approach to achieve success in malaria elimination:

‘The Ministry of Health, CNM, WHO, and partners, including the Asia Pacific Malaria Leaders Alliance (APLMA), will continue to advocate for commitment to malaria elimination at the highest levels to secure effective multi-sectorial engagement

The Prime Minister of the Royal Government of Cambodia has committed to elimination of all forms of malaria by 2025. This support was reiterated at the 2014 East Asia Summit in November 2014, when 18 heads of state from the Asia-Pacific region, including Cambodia’s, committed to the goal of malaria elimination in the entire region by 2030. The Ministry of Health, CNM, WHO, and partners, including the Asia Pacific Malaria Leaders Alliance (APLMA), will continue to advocate for commitment to malaria elimination at the highest levels to secure effective multi-sectorial engagement, address human resources requirements for malaria, ensure effective national leadership and governance, expand health services to provide full access for people in remote areas, and determine appropriate approaches to sustain community-level services beyond malaria specific services.

Elimination goal and objectives will be included and prioritized in national health sector strategy. The CNM will issue official malaria progress reports to senior management of the Ministry of Health as well as publish these updates on the CNM’s website (http://www.cnm.gov.kh/) to maintain visibility of the program.

Partners including governmental sectors, national and international nongovernmental organizations, the private sector, media, bilateral and multilateral agencies, and funding institutions will be harnessed for achievement of the malaria elimination goal. A National Multi-Sectoral Malaria Elimination Committee, consisting of all relevant health and non-health stakeholders, will meet bi-annually to discuss current progress and challenges related to malaria elimination. Provincial elimination committees, consisting of key health staff and other intersectoral partners relevant to malaria, which already exist in some areas of the country, will be expanded and strengthened to support interventions specific to the local context.

CNM will appoint focal person to coordinate all country partnerships. CNM will require all partners and their activities to be aligned with the elimination action framework. The Malaria Elimination Sub-Technical Working Group, made up of government staff and representatives from partner organizations with extensive international and local expertise in malaria, will meet every two months to coordinate activities. Working groups representing each thematic area (Case Management, Vector Control, Surveillance and Monitoring and Evaluation, Procurement and Supply Chain, and IEC/BCC) will meet on an ad hoc basis to advise the STWG and CNM.

At Annual Malaria Review Meeting in quarter one of each calendar year, one day will be dedicated for technical and financial partners to present achievements and indicate future plans for coming year. CNM will utilize current partnerships with the WHO, the Asia Pacific Malaria Elimination Network (APMEN), and other technical partners to develop program capacity and liaise with other regional malaria programs to inform technical strategies.


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Cambodia recently endorsed the Strategy for Malaria Elimination in Greater Mekong Sub-region (2015- 2030), along with neighboring Vietnam, Thailand, and the Lao People’s Democratic Republic (Lao PDR), which will support alignment of national strategies and monitoring and evaluation frameworks. The CNM, in close collaboration with WHO and implementing partners, and in the context of the Greater Mekong Strategy, will strengthen existing cross border activities and establish new ones through conducting biannual planning and review meeting, and harmonization and synchronization of interventions at border areas with neighboring countries. Coordination between border districts of Cambodia and neighboring countries will be strengthened through data sharing agreements and formal action planning sessions. IEC/BCC materials will be developed in relevant languages for each area to ensure that key messages are absorbed by targeted audiences.’

Unfortunately, some of this remains aspirational as progress has been undermined by the administrative issues that have blighted malaria elimination efforts in Cambodia in recent years.

Vector control interventions (LLINs, ITNs and LLHNs; IRS; other) Since the 1990s, Cambodia has relied on conventional ITNs, LLINs and long-lasting insecticide treated hammock nets (LLHNs) for malaria control. Prior to 2005, the NMCP focused on distribution and treatment of conventional nets first using a liquid pyrethroid formulation and later using pyrethroid tablets, targeting high transmission areas. The programme gradually replaced conventional ITNs with LLINs from 2005 onwards.

In 2016, the programme developed detailed implementation guidelines10 in order to ensure that all implementing partners conduct the net distributions in a standardized manner throughout the country. The implementation guidelines provide clear step-by-step instructions on how to plan, implement, monitor and evaluate net distribution activities including mass distribution campaigns. The Annexes contain Standard Operating Procedures (SOP) for net distribution and supporting documents for planning, budgeting, logistics and monitoring and evaluation. These guidelines are designed to be regularly reviewed and updated as required.

Indoor residual spraying (IRS). In addition to nets, CNM plans to conduct IRS in response to outbreaks and active transmission foci in order to quickly reduce vector numbers and minimize transmission. US$2.5 million has been allocated for this IRS under RAI2E for three years. Some experts believe that this is a costly distraction and that it would be better to focus on improving the quality of what is already happening than to add another low-quality intervention.

Topical repellent. Topical repellents are popular in some areas and CNM remains keen to pilot their use in forest settings.

Targeting The targeting of the 2018 LLIN mass campaign was based on 2014 malaria information system data. Due to problems with project implementation between 2015 and 2017, this was the most recent reasonably reliable dataset available. As data quality was somewhat variable the national Vector Control Technical Working Group (VCTWG) developed an

10 Guidelines for Distribution of Long Lasting Insecticidal Mosquito Nets (21/01/2019).


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unusual stratification methodology which involved calculating proxy village-level APIs. All villages with an API >5 were identified and listed (the threshold API was >1 for previous distributions). The resulting village lists were then reviewed and finalized in consultation with health workers and volunteers in the periphery, thereby taking local knowledge of malaria endemicity into consideration. This approach resulted in a final target population of 2.6 million, down from 3.6 million in 2015, and in many villages in elimination areas not being targeted. The surveillance system is just now being revamped after two years with little or no community-based surveillance. The risk of localized resurgence is thus high, particularly in communities that are both receptive and vulnerable. Targeting of earlier campaigns was based primarily on forest proximity where incidence data was weak.

The programme also supports ‘occupation-related distribution channels’ for those whose occupations are considered to place them at high risk of malaria, such as formal and informal forest workers (construction project workers, miners, woodcutters, hunters and foragers) and farm and plantation workers and their families living close to the forest fringe (collectively referred to as ‘mobile and migrant populations’ - MMPs).

The practice of loaning LLINs to farm and plantation managers to cover their seasonal staff, which proved problematic from a management perspective, has now been dropped in favour of free provision of LLINs annually as required.

CNM has recently introduced six-monthly mapping of malaria relevant MMPs identified by Health Centres (HC)/ODs/PHDs/other implementing partners. So far, the flow of information from the periphery has been problematic, but efforts to improve performance are continuing.

Unofficial new settlements in forest/forest fringe settings are not targeted to receive LLINs as it is understood by CNM that distribution to unofficial populations would not be sanctioned by GFATM. This is an example of technical decisions being hampered by misplaced perceptions of the GFATM approach.

Epidemiological data indicates that the emphasis placed on providing malaria control interventions for rubber plantations is unjustified and an expensive distraction from the malaria elimination effort.

The Army. As elsewhere in the region, the army forms a significant at-risk population, but detailed epidemiological information is difficult to access as data relating to the number of cases amongst soldiers and the numbers of soldiers based in forest areas are restricted. The number of malaria cases detected by army medics are aggregated and then shared with CNM and WHO through monthly reports submitted by NAMRU-2. However, these aggregated data cover both soldiers and civilians. Furthermore, while data are broken down by health facility, there is no breakdown by age, gender or specific location. Access to microscopy is limited to camp hospitals and the army does not receive sufficient RDTs, so many of the cases treated and reported are ‘suspected’ rather than ‘confirmed’. The data from the military are therefore not incorporated into routine CNM reports.

Some limited information is available and, unsurprisingly, this points to high incidence amongst soldiers based in the forest. For example, during the conflict with Thailand in Preah Vihear Province in 2015-16, 40% of approximately 140 soldiers tested by quality assured microscopists during passive case detection (PCD) were slide positive for malaria. NAMRU-2 is currently in the process of recruiting an epidemiologist to review available data from the


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Cambodian military and publish findings where possible. NAMRU-2 is also talking to military officials about the possibility of enhanced data sharing in support of malaria elimination.

According to senior officials at CNM, both the Army and the Police are currently provided with LLINs/LLHNs by the programme. But according to other interviewees this is not happening in all endemic areas. Soldiers and police operating in highly endemic areas of Mondulkiri for example apparently remain unprotected. In 2018, forest rangers were added to the CNM’s list of forest-goers to be targeted with LLINs/LLHNs.

Quantification of commodity requirements CNM-MoH leads campaign planning and related guidance for mass LLIN distribution through the CNM’s Sub-Technical Working Group (STWG) of the Technical Working Group for Health (TWGH).

Quantification of all vector control commodity requirements is carried out at Central level by CNM with the assistance of technical partners, based on the stratification described under ‘Targeting’ above. The resulting figures for population-at-risk are fed into an Excel model that takes in to account existing LLINs, factoring-in the expected lifespan of the LLINs in question and yearly attrition rates due to wear and tear, and loss. In-line with normative guidance, one double-size LLIN is calculated for every 1.8 people living in settled communities targeted with mass distribution[29]. In the case of monks in monasteries, one LLIN is allocated for each individual.

In addition, every household is allocated one LLHN (just a hammock net, no hammock included) to protect forest-goers.

Detailed planning including micro-planning: It is not possible to store large quantities of LLINs and LLHNs at HC level due to lack of space, so programme personnel at PHD and OD level work with relevant health facility staff to develop detailed micro-plans that include the following information:

• Ensure that all villages identified as ‘at risk’ by PHD/OD/HC staff are approved by CNM

• Estimate the number of nets required, allowing for buffers at village (3%) and OD (10%)

levels

• Allocate time to conduct census and distribute Household Cards (should be completed

within seven days)

• Establish the timetable for distribution in HC catchment area (seven to 15 days duration)

• Establish the timetable for distribution in each village (at least three days in advance)

In order to ensure the development of realistic and robust micro-plans, CNM organises micro-planning workshops at regional level for PHD, OD and HC staff and implementing partners (both Government Line Ministry Departments and Non-Governmental Organizations (NGOs)) providing detailed guidance as well as specific templates to assist the planning and budgeting process.

The PHD, OD and HC staff then work together to develop and submit detailed provincial micro-plans. These are then reviewed by CNM with technical support from the PR and after the necessary iterations, the plans are finalised and approved for implementation.

The approved micro-plans are shared with the relevant HC staff, programme staff at OD and PHD levels as well as net-distribution monitoring teams from CNM and the PR.


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For the Army, quantification of needs is based on requests from the Ministry of National Defence (MoND) and for Police and Forest Rangers quantification of needs is/will be based on requests from the Ministry of Interior-Health Department (MOIHD).

Procurement of vector control commodities In order to take advantage of economies of scale, all LLINs purchased with funds from the RAI2E grant (for all GMS countries) are being procured through GFATM’s VPP mechanism - a competitive tendering and supplier selection process.

For Cambodia’s procurement of LLINs for 2018, following a plea from the NMCP and its implementing partners, which was based on anecdotal evidence and the findings of a survey conducted by PSI/PSK[53] (see ‘Research findings’ below), GFATM agreed to allow the country to procure polyester LLINs in preference to polyethylene LLINs on condition that the government paid any excess funds required. As it happened, unusually the polyester LLINs were cheaper than the polyethylene LLINs and so the procurement went through without the government having to spend any additional funds.

In the past, imported LLINs/LLHNs were stored at central level either at the Central Medical Supplies (CMS) store or in a rented warehouse if necessary. But the most recent procurement was shipped directly to PHD level by the supplier.

Well in advance of the supply date the CNM prepares an LLINs/LLHNs supply plan and communicates with PHDs, ODs and SRs on quantities to be supplied and planned delivery dates. Agreements are then signed between CNM and PHDs, ODs and SRs. Provincial Malaria Supervisors ensure that there is sufficient storage space in OD stores, identify an appropriate location within the stores, and ensure that the storeroom is tidy before delivery. The CNM arranges transportation (plus unloading services) for LLINs/LLHNs from PHD level to ODs and SRs.

LLINs/LLHNs are generally delivered in bales of 50 nets. Bales are stacked appropriately and on pallets where available to avoid contamination with any liquids that may leak on to the floor. On receipt, the storekeeper and one other local official count the number of LLIN/LLHNs bales and inspect them for damage before signing the delivery note. Any discrepancies/problems are noted. An authorized person from the PHDs/ODs or SRs sign and stamp the delivery note, retain a copy and send the original to CNM for reference.

PHDs/ODs are required to make an entry of the new stock balance of LLINs/LLHNs from the delivery note into the Operational District Drug Inventory Database (ODDID). Stock management is based on the First Expired, First Out (FEFO)/First In, First Out (FIFO) principles.

PHDs/ODs and SRs are responsible for safeguarding LLINs/LLHNs stock balances before, during and after the distribution activity. LLINs/LLHNs stock balances and distribution data are regularly maintained and updated during the distribution process. PHDs/ODs and SRs provide stock balance reports and distribution reports to the PR upon the completion of the distribution process or upon special request.

Figure 5. Workflow for LLIN/LLHN logistics management and storage process.


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It is usually not possible to store large quantities of LLINs and LLHNs at PHD, OD or HC levels due to lack of space, so it is important that the supply system works efficiently and that distribution to end users happens quickly and efficiently. The workflow plan for LLIN/LLHN logistics management and storage process is presented in figure 5.

A similar process is followed for delivery of LLINs/LLHNs from PHD/OD.

Based on the data collected and compiled during a pre-distribution census at village level (see below), PHDs/ODs prepare a LLIN/LLHN transportation plan and communicates with HC staff and village chiefs on the dates of delivery and quantities to be received. Although LLINs are usually individually wrapped and bales robustly packaged, every transport vehicle must be equipped with the minimum of a tarpaulin for the protection of its loads.

HC staff are responsible for identifying a secure space (lockable, with limited access) where stocks of LLINs/LLHNs can be stored and ensuring that the space is ready and tidy before the arrival of the LLINs/LLHNs.

On delivery PHD/OD staff issue an LLINs/LLHNs delivery note as proof of delivery to HC/Village, and on receipt, two HC/village focal persons at each site count the number of bales and inspect them for damage before signing the delivery note. Any discrepancies/problems are noted. Stocks of LLINs/LLHNs meant for mass distribution should not remain at HC/village level for more than three days before distribution to end users.


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Pre-distribution planning PHDs convene team meetings with all personnel involved in malaria programme activities at the provincial level at least one month before distribution campaigns commence, to discuss logistics and finalize planning.

In elimination settings PHDs are required to convene a meeting of the Provincial Special Working Group for Malaria Elimination chaired by the Provincial Governor/Deputy Governor and present the provincial LLIN distribution plan in order to seek support for advocacy associated with distribution efforts, particularly from Line Ministry Departments at provincial level. Minutes should be taken at this meeting and a report on the decisions made should be submitted to the CNM so they may in turn report progress to the MoH.

Pre-distribution census. Household Cards (figure 6) are provided to all householders during the pre-distribution census – an enumeration activity conducted by the HC staff in collaboration with the village level volunteers and Village Chiefs. Approximately 20-30 households are enumerated by each enumerator each day depending upon the distances between households. Each enumerator may have to work for 5-8 hours per day and each household registration may take approximately 15 minutes (introductions, explanation of purpose of visit, asking questions of the beneficiary and recording information, responding to questions from the beneficiary and disseminating key messages about the dates and procedure for the LLIN distribution). The names of all family members are included in the household card, the number of nets to be delivered is calculated and recorded, and the card is then signed by a member of the enumeration team. The household representative is told to retain the card in order to receive LLINs/LLHNs during the mass campaign or to access supplementary nets through continuous channels. A copy of the form in the card is retained at the HC. The information contained is summarised and entered into a ‘Household Summary Form’.

Figure 6. Cambodian ‘Household Card’.


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During the census, households are informed about the timing of the distribution to ensure people are available to receive their nets. Details are reconfirmed at least three days in advance of distribution.

Implementation The most recent mass distribution campaign was due for completion in June 2018.

Mass distribution aims to rapidly scale-up coverage. Distribution is carried-out by HF staff and community volunteers. Distributions are timed to take place immediately prior to the start of the rainy season. The exact location for distribution within each village is decided in consultation with the Village Chief and village volunteers and informed to the community at least three days in advance.

Signatures/thumb prints of all recipients are recorded on Household Cards for each net supplied and these records are verified with the supplier’s signature. Those who miss the campaign can collect their net from their designated HC. Health education relating to proper use of nets including hanging instructions, maintenance and avoidance of excessive washing, is provided to all present.

Members of the distribution team are not permitted to collect any direct or indirect payment from the households for the issue of LLINs/LLHNs.

In case there are insufficient nets to cover all those in need, households without nets are recorded and prioritized for subsequent distributions.

To achieve universal coverage, LLINs should be provided based on the sleeping behaviour of the target beneficiaries. Those who sleep alone should be provided with an LLIN of their own.

Topping-up to maintain coverage. It is estimated based on local expert opinion that 10-20% of nets distributed during mass distribution campaigns will be damaged or lost during the first year of use. There are also some additions to the at-risk population resulting from births and immigration. A community-based top‐up distribution has been in place since 2015, whereby 50 LLINs (1 bale) are kept with the community volunteers in every malaria endemic village to meet such needs on an annual basis. In addition, at least two bales of LLINs are kept in reserve at the HC level to replenish VMW stocks as well as to distribute to malaria inpatients, mothers attending antenatal care sessions and other vulnerable people who have reportedly not received any nets at the household level for some reason or other. Under this continuous distribution approach, LLINs are intended to be always available.

All LLINs provided to people from target villages in this way are recorded on their Household Cards witnessed by the Village Chief. When stocks run out in one village, HC staff are required to replenish stocks either from nearby villages or directly from the HC level.

LLIN/LLHNs for ‘MMPs’. In the case of independent MMPs spending time in high-risk areas, nets are supplied directly by community-based volunteers or OD/HC staff depending on circumstances. In the case of companies employing MMPs in high-risk areas, the nets are given to company managers by PHD/OD/HC representatives to pass on to their staff according to CNM guidance.

Wherever possible during continuous distribution, the programme offers MMP recipients a choice of either LLIN or LLHN. Efforts are made to assess needs, taking into consideration distribution history, established MMP population, MMP immigration, LLIN/LLHN life etc.


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PHDs/ODs are strongly advised to prepare and submit quarterly distribution micro-plans to CNM or the CSO supporting implementation in their area, however this is not functioning well and, as mentioned above, quantification of MMPs remains weak.

Under RAI2E, 950,000 LLHNs have been budgeted for MMPs and these have already been procured. Many experts are critical of the design of these LLINs, which they believe makes them difficult to deploy effectively and thereby undermines utilization. Hammocks are not included, except when LLHNs are supplied as part of the ‘Forest Packs’ being provided to the military by HPA, and this further undermines utilization. In order to improve utilization some

in-country experts are recommending ‘DawaPlus’11 as a costly but much more popular alternative to the current product.

Army and Police. The NMCP supports the distribution of LLINs/LLHNs by MoND, and MOIHD to soldiers and police as well as any family members living or operating in high-risk areas. As in civilian populations, those in family quarters receive nets at a rate of one net per 1.8 people, whereas those in barracks or going on patrol receive one additional LLIN/LLHN each.

In April 2018, the CNM established a collaboration with the forest rangers whereby 200 rangers based in 21 provinces will be provided with LLIN/LLHNs for personal use and trained as MMWs. They will be provided with 30,000 LLHNs (not including hammocks) and 1,500 LLINs to distribute to forest-goers.

For all MMPs, use of household cards is left to the discretion of the implementing agency (PHD/OD/HC/MOND/MOI-HD) but some form of identification must be provided.

Under the RAI2E grant, 1,000 forest packages (a backpack, a limited supply of insect repellent, a flashlight, a hammock and an LLHN at a total value US$20) were provided by HPA to the military in 2017. Another 1,000 forest packs have been budgeted for distribution in 2018 and if uptake is positive, additional resources may be mobilized to expand this intervention.

Forest rangers fall under the Ministry of the Environment (MoE) if they are based in protected forest reserves or under the Ministry of Agriculture, Forests and Fisheries (MoAFF) if they are based in community forests.

All nets are distributed free of charge.

The overall quantities of LLINs/LLHNs procured are reconciled by CNM at every level after completion of distribution to end-users.

IRS. IRS is being reintroduced in Cambodia and will be used as part of the response to malaria ‘hot spots’ in order to stop transmission quickly. IRS capacity will be established in all malarious ODs.

Community mobilization The programme expects communication activities to be planned early and to engage key partners, organizations and private sector companies that can contribute to mobilizing the community and ensuring participation and ownership. The CNM has a communication sub-committee, which is responsible for pre-testing and approving all communication materials.

At National and Provincial levels journalists are briefed about the campaign ahead of time and provided with a press release at least 2-4 weeks prior to distribution. At the local level

11 http://www.tananetting.com/dawaplus-canopy-hammock/


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radio presenters are briefed about the campaign and informed about the process of household registration. They are given a set of talking points to support the campaign during the week leading up to distribution. Household registration teams are properly identified through the provision of caps and T-shirts. Efforts are made to ensure that community leaders are actively involved from the planning stages through to implementation of the campaign.

The ‘National Malaria BCC Strategy’ provides guidance on key messages and effective communication for behaviour change. In provinces supported by CSOs these CSOs play a major role in supporting the dissemination of information to communities, using messages developed in collaboration with the CNM. Communications emphasize the care that nets require and the importance of repairing them if they get torn.

Quality control Batch testing. The programme implements batch testing of all vector control products procured. A recent batch of LLINs from Singapore failed batch testing due to low insecticide concentrations. The nets were sent back for re-treating and unfortunately arrived back in Cambodia later than required resulting in delayed distribution.

Supervision of net distribution. The programme supports supervision and on-the-job mentoring to facilitate better planning, implementation and problem-solving and at the same time to ensure transparency and accountability. Supervision is carried out in three phases:

1. During household registration to ensure the quality of the activity and the effective management of the data collected. Enumerator performance is assessed, and immediate corrective action is taken where households have been missed.

2. During net distribution, particularly on the first day when the majority of beneficiaries come to receive their nets and overcrowding can sometimes disrupt the smooth running of the distribution process.

3. Following net distribution (especially as part of integrated supervision) to be able to provide corrective action, including follow-on distribution of nets to address stock-outs, or provide enhanced communication when LLIN utilization falls below expected levels (new LLINs deployed in less than eight out of ten households randomly checked).

Supervision teams aim to visit 20-30% of total distribution sites/target villages during one of the three phases. Sites selection is not random, but based on programmatic consideration, with emphasis placed on including sites targeted to receive large numbers of nets, and remote and inaccessible sites. CNM, PHDs, ODs and CSOs conduct coordinated but independent supervisory visits to maximize coverage and cost effectiveness.

In the case of large companies operating in endemic areas, monitoring and follow-up of net provision and utilization is carried out with company owners to ensure that all employees at-risk have access to nets. In all cases, record checks are performed by appropriate supervisory staff.

CNM works with UNOPS and other partners who procure and provide LLINs/LLHNs for the programme to ensure that all are marked ‘NOT FOR SALE’ stitched on to the nets and stamped on the net packaging. Any programme LLINs/LLHNs that are found for sale during site visits are confiscated.


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Coverage The 2013 Cambodia Malaria Survey showed:

▪ Increased LLIN ownership. Mass distributions of LLINs in Cambodia at a one net to one person ratio have resulted in an increased proportion of households (all risk categories) with any LLINs (52% in 2010, 75% in 2013) and with sufficient LLINs to protect all inhabitants (23% in 2010, 51% in 2013).

▪ Increased proportion of the at-risk population sleeping under LLINs. In the targeted at-risk villages (those in risk categories 1-3, located less than two kilometres from the forest), ‘use of LLINs last night’ increased from 32% in 2010 to 57% in 2013. However, the main reason for this increase was a switch in use from ITNs to LLINs.

▪ Increased net use among forest-goers. Of participants included in the household survey who reported sleeping overnight in the forest in the previous six months and who are resident in the targeted at-risk villages, the proportion reporting they used an ITN on their last trip to the forest increased moderately from 37% in 2010 to 43% in 2013. Use of any net on last visit to the forest remained stable (74% in 2010, 72% in 2013), indicating increased use of ITNs/LLINs among those taking nets to the forest.

Preliminary findings from a recent survey by ‘Consortium for Health Action’ (Consortium HA) in forest and forest fringe villages in Mondulkiri Province showed that 64% of LLINs received were not being used (Colin Ohrt, personal communication)). 67% of interviewees said that this was because their existing nets were still in good condition. Only 4% of people reported using an LLHN. 22% of interviewees said that hammock nets were not necessary for owners of zip-type hammock nets.

Key risk groups The Army. The Cambodian Army is a major supplier of forces for UN peacekeeping missions. At any one time around 800 Cambodian soldiers are deployed overseas in this way, often in malaria endemic settings, especially in Africa (this compares with a combined total of around 30 from Thailand, Viet Nam, Myanmar and Lao PDR). Full coverage with effective vector control and personal protection measures it therefore particularly important in this group.

In an effort to prevent the spread of multi-drug resistant (including artemisinin-based combination therapy (ACT) resistant) P. falciparum, Cambodia’s soldiers are screened for malaria prior to overseas deployment, but only with RDTs (which have limited sensitivity) and then they are sent on home leave for two weeks before being mobilized. A significant number of these soldiers presumably spend their home leave in endemic provinces and so the pre-deployment screening is clearly flawed. NAMRU has put forward a proposal to the Center for US Defense Funding to provide PCR facilities at CNM for screening soldiers immediately prior to overseas deployment. However, even if funding is approved, it is unlikely to arrive before March 2019. This is a serious cause for concern.

Conservation agencies. Wildlife Conservation Society (WCS) is one of a number of CSOs with staff working in highly endemic forested areas across the GMS. In Cambodia WCS has approximately 300 staff, comprising of ‘community teams’ that work on social development in villages in the forest and on the forest fringes, enforcement teams of five to seven people based in forest sub-stations and six-person research teams that spend long periods deep in


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the forest. The enforcement and research teams are most affected by malaria and some of WCS’s staff members may have three or four episodes a year. In the forest reserves where they work, WCS estimates that their staff comprise approximately 10% of the forest-going population.

WCS team leaders from the Keo Seima Wildlife Sanctuary in Mondulkiri reported three to five cases of malaria per person per year in their highest risk research teams and one to two cases per person per year for their workforce overall. Staff members use untreated hammock nets and sometimes DEET repellent and mosquito coils. They report that they generally use the same sleeping sites as other forest-goers and that most of these forest sleeping sites can be reached within one hour and very few are more than two hours walk from a road.

As of June 2018, WCS had had no contact with the NMCP or its implementing partners and their staff had not had access to LLINs (the situation has apparently been similar for other conservation groups in Cambodia). In 2018 WCS started treating staff’s conventional bednets and uniforms with insecticide for malaria prevention, under the guidance of the CSO ‘Consortium HA’. In July 2018 WCS staff were provided with LLINs procured by PMI and supplied by MoE.

Conservation NGOs are deeply involved with communities in the forest and on the forest fringes and they know well who goes to the forest and they are very knowledgeable about the behaviour of forest-goers. As well as being an underserved key risk group, they provide a valuable resource for NMCPs trying to address residual malaria transmission amongst informal forest-goers.

A collaboration is currently evolving between the CNM and the Ministry of the Environment which is responsible for forest protection. These collaborative efforts need to be extended to cover all groups of formal sector forest-goers.

Data systems Entomological surveillance data is entered into a Microsoft Access-based database at central level. The CNM entomologist reviews data as it is gathered and submits descriptive analyses to her line manager on an ad hoc basis. Statistical skills within the entomology unit are limited.

HCs (including those supported by CSOs) are responsible for consolidating net distribution lists and submitting consolidated data to ODs. ODs are responsible for entering net distribution data into the MIS (with support from CSOs where present). Copies of primary supporting documents (e.g. net distribution receipts duly thumb-printed and signed) are kept by both HCs and CSOs (or their equivalents in the MoND/MoIH.

PHDs and CSOs are required to submit a copy of signed and dated net distribution reports generated from the Malaria Information System to CNM.

Monitoring and evaluation of vector control Overall program evaluations to assess progress towards program goals and objectives take place every three years. These are used to assess the feasibility, efficiency, effectiveness, impact, relevance and sustainability of specific interventions such as LLINs/LLHNs.

Under RAI2E an ‘Independent Monitoring Panel’ will be established by the Regional Steering Committee to monitor progress across the GMS on a six-monthly basis.


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The Cambodia Malaria Survey, a large-scale household, drug and net outlet and health facility survey, which is generally conducted once every three years, is the key malaria evaluation tool used to assess the performance and impact of malaria control and elimination activities in Cambodia. At the same time, it assists in the monitoring and evaluation of grants funded by the GFATM. The Cambodia Malaria Survey is the primary source of data for outcome indicators under the GFATM’s Grant Performance Frameworks.

A recent BMGF project introduced quick bednet distribution assessments that were carried out one month after mass campaigns. CNM considered these to be very useful, but they have now been dropped due to lack of funding.

Vector surveillance The CNM has recently developed a detailed, high quality plan for ‘Entomological surveillance for malaria elimination in Cambodia 2017-2021’. This provides strategies and workplans designed to improve and expand entomological surveillance and insecticide resistance monitoring and management for the MoH and its implementing partners in Cambodia. Provided separately is an excellent package of SOPs for entomological field techniques, insecticide resistance testing and insectary management. Also provided separately are training curricula and materials for provincial and OD malaria supervisors and for entomology technicians who will be participating in mosquito collection and field processing.

The timeline for roll-out of entomological activities (Annex 1 of the Plan) has slipped somewhat and should now be updated. With the latest support from USAID/PMI for entomological strengthening channelled through Abt Associates (see above), it seems likely that good progress could be made in the coming years.

Four entomological monitoring contexts are defined: Entomological monitoring in burden reduction areas; Focus and outbreak investigation; Vector mapping; and, Operational research. Each context has a set of basic entomological indicators, with accompanying SOPs, the frequency of collections, the staff involved and the daily work schedule. It is noted that staffing and scheduling may be adjusted according to the context, accessibility and the human and systems resources available.

The importance of vector mapping and risk area stratification for supporting efficient use of limited resources and on locating and eliminating remaining transmission foci is perhaps overstated given the role of epidemiological data. It is not necessary for entomological information to complement epidemiological information in order to clearly define where malaria transmission is or is not occurring (so that wasteful investments for LLINs in non-transmission zones can be re-allocated to activities for malaria elimination). This can be done based purely on epidemiological information.

Entomological surveillance has been carried out as part of focus investigations by URC funded teams in Sampov Loun since July 2015. The last indigenous case in this area occurred in March 2016. No vector species were found, and staff concluded that the entomological component of focus investigations was not useful in settings such as theirs.

In GFATM-supported areas the cumbersome administrative procedures associated with authorizing a ‘mission order’ mean that it will not be possible to adhere to the ‘1-3-7’ timeline for case investigation, focus investigation and focus response adopted by the NMCP.


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The CNM is conducting enzyme-linked immune-sorbent assay (ELISA) based screening for sporozoites (using individual rather than pooled mosquitoes) as part of its routine surveillance. In 2011, PCR cross-check results revealed an extremely high false positive rate for P. falciparum ELISA conducted on relatively zoophilic species12 (none of the 104 positives cross-checked were confirmed by PCR)[54]. All ELISA-positive specimens are now sent to ITM-Antwerp for PCR-based confirmation.

Insecticide resistance monitoring As mentioned above, the CNM has recently developed a strategy for insecticide resistance monitoring as part of its detailed plan for ‘Entomological surveillance for malaria elimination in Cambodia 2017-2021’ (the Entomological Surveillance Plan). The strategy for insecticide resistance monitoring and management is based on the WHO’s ‘Global Plan for Insecticide Resistance Management’ (GPIRM) and more recent updates on resistance testing. Full details are provided in the associated SOP. The new Entomological Surveillance Plan includes expanded insecticide resistance testing, but it has not yet been implemented.

The CNM currently has four sentinel sites selected to represent the main vectors of malaria in Cambodia (An. dirus, An. minimus, An. barbirostris, An. maculatus and An. epiroticus13), which it aims to monitor (bionomics and insecticide resistance) three times per year. However, in 2017 only six of the 12 planned missions were possible due to GFATM-related administrative issues affecting funding flow and due to limited human resources (HR) (the CNM has only one trained entomologist14 available to carry-out field work). Furthermore, the team had difficulty catching sufficient specimens for bioassays due to unusually high levels of rainfall. Only 144 An. minimus were tested, 124 for deltamethrin and 20 for permethrin. These tests did not reveal any evidence of resistance.

Data provided by the CNM to WHO for the 2015 World Malaria Report (table 1) did not reveal any indications of reduced susceptibility to pyrethoids in An. dirus. An. minimus and An. maculatus may have been showing some indication of resistance to pyrethoids; An. epiroticus was fully susceptible.

Table 1. Insecticide resistance data provided by the CNM to WHO for the 2015 World Malaria Report. (Note: where more than one species against the same insecticide is listed, this indicates a separate test at a different time or location).

12 An. maculatus (50), An. barbirostris (33), An. minimus s.l. (20) and An. jamesii (1). 13 An. epiroticus has long been rumoured to have some role in malaria transmission in coastal areas of Cambodia, but an

in-depth but unpublished study conducted by CNM in 2001-2, when incidence of malaria was much higher than it is now, failed to incriminate this species as a vector. 14 ITM-Antwerp MSc in Public Health with thesis in entomology.


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It is important to note that results from WHO tube bioassays do not indicate control failure. Even at the high frequencies observed with An. barbirostris in table 1 above, this is no indication that LLINs would not be effective against this species. Ideally, where resistance has been detected in a vector, as here with An. minimus, intensity assays should be conducted, as well as further investigations using other methods (WHO test kits can now be used for intensity assays, as papers with different concentrations of insecticide are now available from Malaysia).

It is difficult to find blood-fed wild caught An. dirus or An. minimus that will subsequently oviposit and produce F1 progeny that can be bioassay tested at three to five days old (WHO’s preferred methodology). As a result, as elsewhere in the region, only wild-caught females are used for WHO bioassays in Cambodia. This could become problematic, as in any given location there could be mixtures of morphologically identical sibling-species. Also, as individuals with metabolic resistance will tend to lose their ability to detoxify insecticides as they age, this approach could underestimate resistance in the population.


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Insecticide resistance surveillance findings are shared with WHO and partners every year through CNMs annual report.

WHO’s GPIRM[55] provides a framework for implementing a national insecticide resistance management strategy. A key first step is to: ‘Establish a strong intersectoral body to decide on insecticide resistance management’ and to ‘Ensure international coordination and data-sharing for effective national decision-making’. In the Cambodia context, this intersectoral body is to be formed, with the Vector Control Working Group (VCWG), chaired by the CNM, at its core. The Terms of Reference for the VCWG were provided as an annex to the detailed Entomological Surveillance Plan but to date action has been limited.

Mitigation options in the event of insecticide resistance detection are limited and will likely rely on ‘next generation’ combination LLINs including pyrethroid-piperonyl butoxide nets and other products once these have been prequalified by WHO.

The Entomological Surveillance Plan supports decentralizing and expanding the responsibility for entomological surveillance, with much greater involvement for malaria supervisors at PHD and OD. An ‘Action Framework for Entomological Surveillance’ is provided. Included are training curricula for PHD and OD staff to provide a basic understanding of mosquito vectors.

Unfortunately, much of what is written seems to be aspirational rather than actual. At present the entomology unit at CNM actually does whatever is funded, rather than what has been prioritized in the Entomological Surveillance Plan. Funding partners often have limited understanding of entomological issues and so understandably tend to fund what they know: ‘vector bionomics and insecticide resistance in sentinel sites’, rather than what would be most useful to the programme in a resource limited environment.

The CNM and its partners have recently developed a ‘Surveillance for Malaria Elimination’ manual, which covers entomological surveillance as part of focus investigation. In the opinion of the reviewer this document is overly complicated. For example, in the section on focus response, interventions are decided based on three grades of vulnerability and three grades of receptivity using a three by three table with nine different intervention package options. Furthermore, the layout of the manual seems overly ‘arty’, detracting from, rather than accentuating the technical content. Countries need simple accessible guidelines that can be used effectively by staff in the periphery who may have limited technical capacity.

Research and innovation The CNM is maintaining a thriving colony of mouse fed An. dirus, which was established by the National Institutes of Health (NIH) in the United States, from specimens collected in Pursat in 2012. The colony is used for assessing the residual efficacy of LLINs using WHO cone bioassays. Biosecurity at the insectary in Phnom Penh is however weak.

In the recent past CNM has been engaged with WHOPES on Phase III evaluations of LLINs seeking WHO approval.

The entomology team is not currently involved in any unilateral hypothesis-driven research. To date, no experimental hut or experimental platform studies have been conducted in Cambodia.

There are several international organizations conducting entomological operational research in Cambodia. Individually, some of these organizations provide significant support


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to entomology capacity and infrastructure development at the CNM, as well as training and mentoring field staff in their areas of operation. However, there is a need to improve overall coordination and information sharing. The Entomological Surveillance Plan logically proposes various ways in which CNM can coordinate partners and develop information repositories and data-bases for entomology work conducted in Cambodia: Participate in the Vector Control Working Group; Create an inventory of Cambodia’s entomology partners, locations of field sites and activities undertaken; Develop a directory of persons trained in entomology and vector control; Keep records of all mosquito collection and vector incrimination work carried out; Keep records of all insecticide resistance testing; and, Support information sharing through research symposia.

The Entomological Surveillance Plan also sets out operational research priorities:

• mapping and entomological surveillance in the forested transmission areas, to

understand the presence, abundance, biting times and if possible the longevity and

sporozoite rates of these vectors that may be transmitting malaria in the deep forest

(this also involves refinement of tools and strategies for improved and more efficient

entomological surveillance in the light of ethical restrictions on man-landing catches).

• personal protection for the control of outdoor and residual transmission beyond the

reach of traditional LLINs and IRS.

The Entomological Surveillance Plan rightly highlights the importance of linking entomological studies to social/behavioural studies to determine when and where most individuals are being infected.

The overarching strategic priority is improved partner collaboration and focus on national program needs. There is a need to more efficiently coordinate and adapt the entomological resources available in Cambodia to build capacity and provide the necessary information to better target and monitor interventions, and not to divert staff time and resources away from program needs.

Two in-service training curricula are provided in the Entomological Surveillance Plan, one for malaria supervisors and one for entomology technicians. Not included is pre-service training and ongoing efforts to improve undergraduate and graduate training in public health entomology through the Royal University of Phnom Penh and the National Institute of Public Heath, with collaboration among the CNM, the Institute Pasteur/Cambodia and other international partners and institutions.

According to their ‘Guidelines for Distribution of LLINs’ CNM also plans to conduct operational research on: acceptability and usage of all net types; changing forest ecology; use of insecticides for IRS; and, repellents for forest goers. Research findings and lessons learnt will be used to further refine the vector control strategies for malaria elimination. However, during interviews with CNM officials, only the following entomological priorities were identified: insecticide resistance monitoring; LLIN distribution; and, vector species distribution.

Recent research findings.

Figure 8. Bar chart displaying average number of P. falciparum cases reported by each VMW, each month, in areas receiving the first phase of interventions (zones 1 and 2, blue) and in zones receiving the second phase of interventions (red).


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A descriptive analysis (figure 8) carried out in Cambodia as part of GFATM’s ‘Prospective Country Evaluations’ provides a compelling illustration of an association between phased mass ITN distribution and malaria burden (data from the passive surveillance system). A large reduction in the number of cases reported in zones 1 and 2 (blue bars) occurred after these areas received ITNs in May 2009, while zone 3 cases (red bars) remained at a similar level to the previous year. Following an ITN distribution in zone 3 in early 2010, the number of cases reported in zone 3 fell significantly compared to the previous two years.

In a study of spatial repellents in Mondolkiri Province metofluthrin emanators (10% w/w metofluthrin) reduced landing rates of outdoor biting secondary vectors of malaria but had no observable effect on malaria prevalence, however, malaria transmission levels were low[56].

Reports from IPC of 17.4% day-biting in A. dirus during 24-hour static landing catches (research funded under France’s ‘Initiative 5%’) have very serious implications for the development of effective tools for personal protection from malaria in forest settings. Results are likely to be published late in 2018 (Amelie Vantaux, personal communication). CNM representatives confirmed similar, as yet unpublished, findings in Cambodia.

IPC is currently investigating forest movements in Mondulkiri with support from NIH through its ‘International Centers of Excellence for Malaria Research (ICEMR)’ grant.

In 2016 Population Services International/Population Services Kampuchea (PSI/PSK) conducted a qualitative study in six villages in each of two provinces in Cambodia to determine mosquito net usage determinants and user preference[53]. The study identified wide-spread antipathy for distributed LLINs because of their small size, low height and, in some cases, polyethylene material. The latter is considered uncomfortable to the touch and associated with large mesh-hole size (allowing insects access) and material deformity (shrinking, wrinkling, inward bowing and hole-size deformation). The study found that LLINs were valued for the additional protection the insecticide treatment provided when


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compared to untreated nets, particularly for use in remote areas with high mosquito densities, but that a lack of knowledge concerning the insecticide undermined LLIN utilization. The team recommended changes in LLIN specifications and procurement practices.

PSI/PSK has just been awarded a grant under the ICC component of the RAI2E grant to conduct a quantitative follow-on study to assess the relationship between LLIN material and LLIN usage in Cambodia.

Researchers from the United States National Institutes of Health (NIH) collaborating with CNM on a range of entomological studies between 2013 and 2014 used PCR to detect malaria parasites in the heads and thoraces of the anopheline mosquitoes they collected. 17 of 35 species examined tested positive for P. falciparum (figure 9). The researchers concluded that all were ‘carrying P. falciparum’[57]. These conclusions have been met with scepticism by many and it has been suggested that PCR may be so sensitive that it is detecting mosquitoes that have fed on people (or monkeys in the case of P. knowlesi) infected with malaria, rather than mosquitoes that have actually gone on to develop sporozoites and become infective. However, to validate the approach other researchers tested the heads and thoraxes of mosquitoes at different intervals after an infected feed and found that if the dissection was clean (no part of the midgut included), there were no parasites in other parts of the mosquitoes until the oocysts burst (Brandy St Laurent, personal communication), and so the conclusion that ‘many species previously thought to be minor vectors may be sustaining transmission’ appears to be robust.

Figure 9. Results of recent PCR-based vector incrimination work in Cambodia[57].

Other issues. GFATM fiduciary controls. GFATM fiduciary controls have been undermining CNM staff morale and adversely affecting implementation of the complete spectrum of GFATM funded


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activities including entomological surveillance. Examples include: Despite the fact that use of mobile phones can be sporadic in remote areas, GFATM requires entomologists to reimburse them for mosquito collectors’ fees if the Local Fund Agent (a GFATM contracted accountancy firm) cannot contact the mosquito collectors by phone to confirm that they were in receipt of GFATM funds; and, although travel requirements can be unpredictable in remote areas, with routes affected by flooding or landslides, any unplanned expenditure relating to fieldwork is not reimbursed by GFATM. The situation is apparently much better now than it was, and staff are almost fully functional once more, but they complain frequently as the work is hard and the benefits are too small.

Lao PDR – Country profile Malaria is still considered an important public health problem in Lao PDR. Although the overall trend is downwards, the country remains epidemic prone. Incidence decreased between 2000 and 2010 by 92%, from 279,903 cases to 23,047 cases, respectively. However, there was a large-scale epidemic in the southern part of the country in 2012 and 46,202 cases were confirmed nationwide. Caseload rose to 50,674 in 2014 before the epidemic ended. In 2017, there were just 9,332 malaria cases reported, 49% of which were P. falciparum infections. Malaria deaths have decreased from 14 reported in 2007[49] to 1 in 2017[58].

The vast majority (95%) of cases are concentrated in the southern five provinces: Savannakhet, Saravane, Sekong, Champasack, and Attapeu. Malaria transmission in the northern provinces is low and sporadic (figure 10).

Figure 10. Screen-shot from GIS showing geographical distribution of malaria cases in Lao PDR in 2017.


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Policy framework for vector control The 8th National Socio-Economic Development Plan (2016-2020) is Lao PDR's guiding strategic document. The plan is regarded as a measure for achieving socio-economic development, industrialization and modernization towards the year 2020. It paves the way towards the graduation from ‘Least Developed Countries’ status and lays a strong foundation for the achievement of the National Strategy on Socio-Economic Development 2025 and the Vision 2030 as well as the Sustainable Development Goals.

The National Strategic Plan for Malaria Control and Elimination (2016-2020) represents the first phase of the 15-year strategy to eliminate malaria in Lao PDR. The first five years of the strategy sets out to reduce the burden of malaria in the southern provinces to below five cases per 1,000 population while eliminating P. falciparum malaria in primarily northern provinces. By 2025, the country aims to eliminate P. falciparum and P. vivax from all northern provinces and to eliminate P. falciparum in the four southern-most provinces. By 2030, Lao PDR aims to have achieved national elimination. The timelines and geographic targets for elimination are depicted in figure 11.


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Figure 11. Timelines and geographic targets for malaria elimination in Lao PDR, 2015-2030

Structure of vector control programme The Centre for Malariology, Parasitology and Entomology (CMPE), part of Department of Communicable Diseases Control (DCDC) of the MoH, provides technical and managerial support for the NMCP as part of a highly decentralized health system that focuses much of the decision-making power at the provincial level. CMPE has no direct authority over the 18 provinces, each of which has a Provincial Anti-Malaria Station (PAMS). CMPE provides the provinces with funds, key commodities, technical advice and support, and limited oversight, especially in the more endemic south of the country.

The DCDC plays an oversight role for the malaria programme at the macro level. Responsibilities include providing advocacy to higher level authorities within government, fund raising, policy formulation, coordination with relevant ministries and departments, and convening high level meetings including with donors.

CMPE has a direct programmatic responsibility for malaria and other vector-borne and parasitic diseases at sub-national levels. It has a Director and two Deputy Directors. There are four technical units (Epidemiology, Vector Control, Laboratory and Treatment, and Training and Health Education) and one administrative unit (figure 12). Of the 49 staff positions existing at present, there are currently 13 vacant technical posts and two vacant administrative posts.

Figure 12. Organigram of CMPE.


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There are 18 PAMS, each with an organizational structure modelled on CMPE. Depending on the size of the province, the number of staff varies from five to 25.

The 147 District Anti-Malaria Nuclei (DAMN) usually have one to three staff; they are divided into two units: the ITN Unit and the Laboratory and Treatment Unit.

There are 879 HCs serving more than 11,000 villages. Each HC is responsible for five to twelve villages in its service area and provides primary health care, basic training and health education, and referrals. There is/are usually one to three staff at each HC but in future this may increase to seven. HC staff supervise VMWs. Currently there are 649 VMWs and 5,176 multi-purpose Village Health Volunteers (VHV) with malaria training, operating in selected malaria endemic areas. They organize distribution of LLINs and provide health education. The head of the DAMN makes regular visits to HCs to monitor and supervise program activities.

Technical aspects of the programme are all centralised at present, but efforts are underway to decentralize insecticide resistance monitoring and vector bionomics to provincial level.

Capacity (manpower, technical capabilities, training, infrastructure and financial resources) Program management for malaria requires strengthening across all levels of the health system in Lao PDR. Health service provision is constrained by serious weaknesses relating to human resources for health. The lack of human resource availability and capacity has been one of the primary challenges faced by CMPE and its implementing partners. Key issues include: limited numbers of qualified health workers; inappropriate distribution of qualified staff among geographic and health system levels; low salaries; lack of incentives (financial, training, personal development); and inadequate reimbursement of costs leading to poor staff morale and low staff productivity.

Furthermore, the Government of Lao PDR (GoL) operates a quota system for staff positions, whereby if a member of staff leaves CMPE it may result in a new staff position being funded in another MoH unit. This results in disruptive competition between units.


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HR issues are exacerbated by the fact that the GoL does not have a mechanism for hiring staff on a short-term, grant-funded basis. Several development partners are currently lobbying for this to change.

Six to ten students are trained at CMPE each year in an effort to increase in-country capacity for medical entomology and vector control. Lack of English (and French) language skills has seriously undermined capacity development, with CMPE staff not eligible for scholarship placements in the West. Fortunately, Thai is widely spoken and so Thai universities offer a good option for training to increase capacity in the immediate future.

Financially, the NMCP in Lao PDR appears to be very under resourced compared with other countries in the Sub-region, and although CMPE’s entomology laboratory is adequately supplied with good quality microscopes that are in good condition, its Vector Control Section is particularly underfunded. Low absorption capacity has apparently been cited as a reason for donors not increasing the funding envelope for Lao’s NMCP, however only a small proportion of the NMCP’s underspending can be attributed to the NMCP itself (approximately 20% during the first 3-year RAI grant. The rest has been due to extrinsic factors beyond CMPE’s control. Assessments of absorption capacity by funding partners should always take the causes of any underspending into consideration, in order to avoid inappropriately penalizing programmes.

Partners involved in vector control and entomology Institut Pasteur du Laos (IPL) is a Lao PDR National Institution, which was created by Prime Ministerial Decree in November 2007. Its mandate includes: Research on vector borne diseases; Training, education and capacity building; and, Provision of technical assistance for investigation of epidemics.

Although a component of the MoH, IPL has a large degree of legal, scientific, management and financial autonomy. It is able to engage freely in collaborative research and investigations with other Lao and international research and public health organisations including CMPE. It is able to receive outside funding (donations, grants, bequeaths, etc.) and it is well financed as a result.

IPL has four laboratories including one that focuses on medical entomology. It also has a dedicated training center for hands-on laboratory training.

University of California, San Francisco (UCSF) is managing a Bill and Melinda Gates Foundation (BMGF) funded Malaria Elimination Initiative in Lao PDR. The project is directed towards: 1) Improving understanding of malaria epidemiology and elimination readiness in northern Lao PDR. 2) Strengthening surveillance and response systems to detect and respond to malaria epidemics. 3) Assisting CMPE and partners to design and iteratively refine multi-sectorial malaria elimination strategies. Specific project activities include: trainings and technical support for data collection and analysis by health staff; field surveys to determine high-risk groups and risk factors; development and implementation of surveillance and rapid response systems to support rapid elimination; and operational research studies to understand local epidemiology and assess targeted case detection strategies.

Globally, UCSF is in the process of working with partners including the ‘ECK Institute for Global Health’ and BMGF to develop an Entomological Surveillance Planning Tool (ESPT) to support problem solving and vector control decision making. Initially the tool is being


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piloted in four countries globally, including Lao PDR. The development of the tool aims to address both the lack of consolidated operational guidance for entomological surveillance and the growing need among programs for a deeper understanding of transmission dynamics and gaps in protection to inform the development of appropriate responses. The approach appears to be sound and broadly in-line with the recommendations presented in this review.

Intra-sectoral and intersectoral collaboration Despite the issues associated with the GoL’s quota system for staff positions described above, there is a good level of cooperation between the CMPE and other departments within the MoH. TB and malaria share microscopy points for example, and staff from various units in the periphery collaborate on implementation of LLINs through mass and continuous channels as necessary.

There is good intersectoral collaboration between CMPE and the military but beyond this intersectoral collaboration requires strengthening.

Vector control interventions (LLINs, ITNs and LLHNs; IRS; other) LLINs are the primary personal protection measure used in Lao PDR. The main distribution channel for LLINs is through mass campaigns every three years targeting the static population. LLINs are also provided to other key risk groups, through several continuous channels.

IRS is being reintroduced for outbreak response (LLINs are also topped up in the event of an outbreak as required). All PAMS in burden reduction areas and some PAMS in transitional or elimination-targeted provinces are being trained and equipped to support IRS operations under RAI2E. The programme is using ‘Damthrin-SP’ (deltamethrin) from Thailand for all of its IRS operations.

Only five out of eight Hudson compression sprayers were functional at central level. The situation regarding IRS equipment at provincial level is under review by CMPE.

Targeting In 2017, CMPE and its technical partners developed a revised approach to stratification of malaria risk to take advantage of recent improvements in the malaria surveillance system. The Health Facility Coverage Area (HFCA) was used as the basic unit for the new stratification. Data from the District Health Information System 2 (DHIS2) was validated by field staff and used to produce a preliminary stratification using four strata plus an unknown category. Modelling using a combination of different epidemiological and ecological measures was then used to provide estimates for categorizing the unknowns and to validate the reported incidence data to produce a final list of HFCAs by strata, a national map (figure 13) and individual provincial maps (HFCAs have not been geographically delineated, and so only the positions of the health facilities, and not the catchment areas themselves, appear on the map).

The strata based on the two methods is summarized as follows:

• Stratum 1 - Malaria Free

• Stratum 2a - Low burden with imported cases only

• Stratum 2b - Low burden but with local transmission

• Stratum 3 - High burden, a mix of local transmission and imported cases.


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Figure 13. Map showing location and strata for health facility catchment areas .

The entire population living in stratum 3 (API>10) HFCAs nationwide and in stratum 2b (at least 1 malaria case, potentially contracted locally) HFCAs in the five highly endemic southern provinces have been targeted to receive LLINs.

The DHIS2 reporting rate is now greater than 90% so this system will provide a robust platform for future stratifications, with less need for modelling at central level and data validation by peripheral staff.

Supply of LLINs to MMPs through continuous channels will supply the same target HFCAs as the mass distribution. 33,000 LLINs per year will be targeted on MMPs.

The NGO ‘HPA’ is implementing forest kits, but these may be more difficult to target since the ban on illegal logging has reduced the number of forest-goers.

A further 25,000 LLINs per year will be provided to the army.


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Quantification of commodity requirements Overall quantification for the country as a whole takes place at central level based on the stratification of malaria risk and on population data from the latest census adjusted for population growth. These figures are fed into a Microsoft Excel model that takes into account existing LLINs, factoring-in the expected lifespan of the LLINs in question and yearly attrition rates due to wear and tear, and loss. In-line with normative guidance, 1 double LLIN is calculated for every 1.8 people living in settled communities targeted for mass distribution. For quantification of needs down to village level, pre-distribution enumeration of the at-risk population is meant to be carried out, but this has not worked very well in the past. Usually, provincial level staff have allocated LLINs to villages based on the population data on file, which was often out of date. In future, CMPE will work with PAMS and DAMN to develop a distribution micro-plan for each area in an effort to ensure LLINs reach all of those in need. Efforts are underway to improve the methodology and strengthen the quality of implementation of the micro-planning process.

At present the quantification of LLIN’s for MMPs is based on 2% of the target population for mass distribution. HPA is working to develop a more robust quantification methodology and additional LLINs are likely to be required during years two and three of the RAI2E, which the Programme plans to accommodate through routine reprogramming of funds. Continuous distribution will be carried out by health facilities, volunteers, HPA and two local CSOs.

Quantification of LLIN requirements for the army are based on requests from the army.

Procurement of vector control commodities In 2018, 888,000 LLINs will be procured for distribution in 2019. 50% of these will be financed by GFATM and 50% by GoL. There are now concerns however that the GoL contribution may be late, which would mean that the procurement would need to be conducted in two tranches.

CMPE, working with WHO and partners, determines product specifications for LLINs nine to twelve months prior to distribution. In order to take advantage of economies of scale, all LLINs purchased with RAI2E funds (for all GMS countries), as well as LLINs financed by GoL, are being procured through GFATM’s VPP mechanism.

CHAI is supporting all in-country aspects of procurement and supply management (PSM) including procurement, distribution direct to province and storage. It has recruited one fulltime professional staff member in each of five southern provinces and trained them to support malaria staff in the use of ‘mSupply’ software.

Implementation Newly procured LLINs will be supplied direct to PAMS by the supplier. CMPE and its technical partners will provide technical assistance to PAMS as required. PAMS will supply LLINs to DAMN and then DAMN will supply LLINs on to HCs under the guidance of PAMS (with the assistance of associated technical partners where necessary and available). HC staff will supply LLINs to target villages and then work with VMWs, VHVs and village leaders to distribute LLINs free of charge. HC and village representatives are together responsible for data recording during distribution.

Community mobilization LLIN distribution will be accompanied by a mass media health education campaign and community mobilization strategies will be employed by LLIN implementation teams.


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Quality control Batch testing. The programme does not currently implement batch testing of vector control products, but relies on product conformity documentation provided by suppliers.

Supervision of net distribution. The programme and its technical and implementing partners support supervision and on-the-job training to facilitate planning, implementation of vector control measures.

Coverage CMPE will evaluate LLIN ownership and utilization following mass distribution campaigns by means of annual small-scale community surveys. Where appropriate, LLIN surveys will be integrated into malaria multi-indicator surveys.

While the NMCP has made notable attempts since 2012 to address coverage of MMPs with LLINs, LLHNs and mosquito repellents, high-risk groups without fixed addresses such as new forest fringe settlers and forest-goers originating from outside of villages targeted for LLIN remain underserved. A recent small-scale survey carried out by HPA in the south of the country, revealed that 82% of MMPs used conventional mosquito nets and untreated hammock-nets purchased from the market, while only 16% used LLINs distributed by the program[59]. In addition, 26% said they preferred using mosquito coils, lotion, or spray repellents.

Key risk groups As elsewhere in the region, the Lao PDR Army forms a significant at-risk population. WHO estimates that army personnel account for over 10% of confirmed malaria cases reported from the southern provinces[60]. Detailed epidemiological data is not available but based on the likely degree of man-vector contact, the malaria burden in this group can certainly be assumed to be high. Forest patrols commonly last for three to six months. There are usually about ten soldiers in each patrol. Many forest-goers choose to overnight with army patrols for security reasons, further elevating transmission risk.

CMPE provides army entomologists and trainers with training on vector control and personal protection. Soldiers are provided with LLINs (supplied by the programme), repellent soap and health education relating to malaria and its prevention. However, supplies are short, and the level of coverage achieved for LLINs and repellents is low (the Military Institute of Disease Prevention estimates approximately 50-60% and 30% respectively for those most at risk on night patrols in the forest). Army representatives estimate that they require approximately 50,000 LLINs every three years to maintain full coverage. They have recently requested 15,000 single camouflaged LLINs from PMI to help address the current shortfall.

The Army does not use IRS, but it has used fogging for malaria control in the past.

Some soldiers buy their own repellent.

There is no use of chemoprophylaxis in the army as this is not recommended by CMPE.

Each patrol is equipped with RDTs and ACT. They test and treat other forest-goers as required, but often they do not have enough RDTs so they provide presumptive treatment for suspected cases. Resupply of RDTs from DAMN is a laborious process and so often patrols manage without. All positive (or suspected) cases are referred either to the nearest health centre or a military hospital, whichever is most convenient.


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The Lao PDR Army does not deploy soldiers on UN peace keeping missions and so there is little risk of soldiers exporting ACT resistant strains of malaria to other endemic countries. At present there is no routine or pre-/post-deployment screening of soldiers for malaria.

Although the Army does have entomologists, they are not involved in any entomological research, but instead focus on vector-borne disease prevention education for soldiers. With the exception of CMPE, the Army does not collaborate with any agencies on malaria related research.

CMPE has recently brokered plans to establish a memorandum of agreement between MoH and MoD to address the problem of malaria among soldiers, including the sharing of information on malaria morbidity and mortality[59].

Data systems HC staff and VMWs/VHVs collect village-level data and routinely report it to the HC where it is compiled (aggregated without village-specific data) with HC data and sent to the DAMN. Hospitals report directly to DAMN.

The DAMN are responsible for compiling paper-based records of all of the malaria information (LLIN, morbidity, mortality, training, ‘Information, Communication and Education’ (IEC) activities, etc.) received from HCs and hospitals and reporting it to PAMS routinely on a monthly basis. The DAMN retain hard copies of the village level LLIN distribution records for data quality audit purposes. Data quality assurance measures are performed through quarterly supervisory missions by the DAMN team to the HC level. Some of the villages are also covered during these missions.

The heads of the different units at PAMS are in charge of collecting, verifying, compiling and reporting the different types of data and submitting reports to their corresponding units in CMPE. CMPE units then enter the data into Microsoft Excel.

Focus investigation data:

The surveillance protocol for elimination areas is currently being field tested and fine-tuned prior to roll-out. At present the arrangements relating to data flow are as follows:

• All case investigation and focus investigation data should be entered into the DHIS2 case tracker database at DAMN or PAM (depending on who was leading the investigation and response) immediately after the investigation, classification and response activities have been completed.

• Monthly elimination reports will be automatically generated within the database and each elimination province will be required to share these reports with the provincial health manager, CMPE and other stakeholders on a monthly basis.

• Changes in focus classification status will be automatically updated in the database throughout the year based on the dates of the case notifications and dates of confirmation of locally acquired cases in each focus. All new foci will also be automatically added to the foci list for tracking and classification.

There are plans to enter all data into DHIS2 at district level in future.


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Monitoring and evaluation of vector control Overall program evaluations to assess progress towards program goals and objectives take place every three years. These are used to assess the feasibility, efficiency, effectiveness, impact, relevance and sustainability of specific interventions such as LLINs/LLHNs.

Under RAI2E and ‘Independent Monitoring Panel’ will be established by the Regional Steering Committee to monitor progress across the GMS on a six-monthly basis.

Vector surveillance Currently very limited entomological surveys are being carried-out due primarily to the lack of funding available. There is no budget for entomological field-work by provincial staff. 80% of entomological efforts are dengue related.

CMPE is in the process of developing an ‘Operational Manual for Entomological Surveillance for malaria vectors in Lao PDR’ with assistance from WHO. Rather than developing this document from scratch, it would make sense to adapt the excellent Cambodia document ‘Entomological surveillance for malaria elimination in Cambodia 2017-2021’, which was also developed with the assistance of WHO.

Implementation of elimination activities only started in 2018. All programme staff should be trained by the end of June. CMPE plans to incorporate entomological assessment and mapping into elimination related focus investigation activities in order to identify the vectors responsible for transmission and assess and address any gaps in vector control at the focus level. ‘Malaria Elimination Surveillance Guidelines’ were finalized in November 2017 and SOPs are now being developed (as part of the ‘Operational Manual for Entomological Surveillance for malaria vectors in Lao PDR’ mentioned above) and field tested with WHO support.

According to the ‘Malaria Elimination Surveillance Guidelines’, if there are potential malaria mosquito breeding sites within a focus area, then larval surveys will be conducted by members of the focus investigation team made up of staff from PAM and DAMN. If Anopheles larvae are detected, then control measures, including the use of larvicides, will be implemented. Results from breeding site assessments will be recorded in the ‘Larval Survey’ form. Adult mosquito surveillance activities will be conducted in foci to determine which vector species are present, and to investigate their biting behaviour. Results from this activity will be recorded in the ‘Adult surveillance forms’) and then summarized in Section 3.2 Part E of the ‘Foci Investigation and Response form’(figure 14). Results from both larval and adult vector assessments will be summarized in sections D and E of the ‘Foci Investigation and Response form’ (figure 14) respectively. Breeding sites will be featured in focus maps developed by investigation teams. Similar activities are conducted by a team from CMPE, PAM and DAMN in the event of outbreaks if entomological man-power permits. These are outlined in the ‘Malaria Burden Reduction Surveillance Guidelines’ (also finalized in November 2017).

Figure 14. Vector control section of ‘Foci Investigation and Response form’.


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LLIN coverage will be assessed in a rapid coverage assessment and findings recorded in the ‘LLIN Rapid Coverage Assessment’ form. Twenty houses will be randomly selected and physically surveyed for the presence and number of LLINs, and an estimated coverage rate calculated. Results will be summarized in part B of the ‘Foci Investigation and Response form’ (figure 14). If LLIN coverage rates are too low (less than one net per two people per household) then additional LLINs will be distributed so that adequate protection is provided. LLIN distribution forms will be completed and the results summarized in part C of the ‘Foci Investigation and Response form’ (figure 14). IRS may also be carried-out, but details appear to be undecided as yet.

Insecticide resistance monitoring A recent collaborative study by IPL, CMPE and Institut de Recherche pour le Developpement (IRD) funded by ‘Initiative 5%’, investigated the susceptibility of Anopheles species, including several confirmed malaria vectors (An. maculatus and An. minimus), to various insecticides in ten provinces of Lao PDR through a north-south transect[61] (Part of the MALVEC Project). Bioassays were performed on field caught female mosquitoes using the standard WHO susceptibility tests with DDT (4%), deltamethrin (0.05%) and permethrin (0.75%). In addition, gene amplification and sequencing was used to identify knockdown resistance


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(kdr) mutations. Resistance to DDT and permethrin was detected in suspected malaria vectors, such as An. nivipes and An. philippinensis in Lao PDR. Resistance to DDT (now banned but formerly in widespread use) was found in a population of An. maculatus s.l. from Luang Prabang province. No resistance to pyrethroids was found in primary vectors, indicating that these insecticides are still adequate for malaria vector control. However, high resistance levels to pyrethroids was found in potential vector species and reduced susceptibility to permethrin in An. minimus and An. maculatus was reported in specific localities raising concerns regarding pyrethroid-based control in the future. No kdr mutation was found in any of the resistant populations tested hence suggesting a probable role of detoxification enzymes in resistance.

Research and innovation Over the last 10 years entomological and vector control related research in Lao PDR has been conducted mainly by or in collaboration with IPL and has focused primarily on vector distribution[62], risk factors[63,64] and insecticide resistance profiling[61].

An IPL team also modelled spatial variation in risk of presence and insecticide resistance for malaria vectors [65]. The authors concluded that use of modelling to estimate the probability of presence of malaria vectors and insecticide resistance could be used to target insecticide resistance surveillance efforts more strategically.

Another collaborative study investigated alternatives to human landing catches for collecting outdoor biting mosquitoes[66] concluded that the human-baited double net trap is a simple and cheap method to estimate the human-biting rate outdoors without exposing collectors to mosquito bites..

An RCT of N,N-diethyl-3-methylbenz-amide (DEET) for malaria control amongst agricultural populations in Attapeu and Sekong provinces in the south of the country was carried out by a team from the United Kingdom in collaboration with CMPE [67]. The trial failed to demonstrate an effect and the authors concluded that topical repellents were not likely to be a suitable intervention for malaria control in settled communities with high LLIN coverage in the GMS. They did however highlight that DEET should not be discounted as an intervention for high risk forest-goers on the basis of these findings.

Myanmar – Country profile There has been a steady reduction in malaria burden in Myanmar since 2010 (figure 15). The caseload fell from approximately 700,000 probable and confirmed cases in 2010 during the later stages of roll-out of rapid diagnostic test (RDT) based diagnosis (Vector Borne Disease Centre (VBDC) estimate) to 110,141 confirmed cases in 2016[58]. Malaria deaths have decreased very dramatically over the last decade, falling from 1,265 in 2007[49] to 21 in 2016[58] (a reduction of over 98%) reflecting major improvements in access to early diagnosis and appropriate treatment (these cases and deaths do not include those who crossed the border and sought treatment in Thailand). The proportion of cases caused by P. falciparum has fallen from 71% in 2010 to 60% in 2016.

Figure 15: Recent trends in reported malaria burden (confirmed and probable cases and deaths) in Myanmar


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Malaria is becoming an increasingly focal disease. In 2015 (figure 16), out of 291 townships which were endemic, 120 townships had API<1 per 1,000 population at risk compared to 45 townships in 2006. In 2015, 5 out of 15 administrative regions together accounted for 71% of confirmed P. falciparum cases (Rakhine, Sagaing, Chin, Kayin and Ayeyarwady). Rakhine and Sagaing accounted for 24% and 18% respectively. Figure 16. Township level malaria micro-stratification map of Myanmar in 2015


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Some segments of the population are hard to reach due to geographical isolation or ongoing security concerns, mainly in border areas (see ‘Key risk groups’ below).

Although very significant progress has been made in Myanmar in recent years the national malaria elimination effort is now facing ‘the law of diminishing returns’ and, as elsewhere in the region, the spread of artemisinin resistance and difficulties addressing forest-based transmission remain serious challenges to the achievement of national elimination goals.

Policy framework for vector control The National Strategic Plan for Intensifying Malaria Control and Accelerating Progress towards Malaria Elimination (2016-2020) represents the first phase of a 15-year strategy to eliminate malaria in Myanmar. The first five years of the strategy sets out to eliminate malaria in less endemic areas, while accelerating control efforts in more endemic areas to reduce cases to a low level. Post 2020, it is expected that the proportion of areas targeted for elimination phase will expand progressively. P. falciparum will be eliminated by 2025 and by 2030 Myanmar will be malaria free.

The NSP will serve as reference for all institutions working on malaria control/elimination in order to ensure that their efforts are aligned with those of the NMCP. The strategy is in-line


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with the Strategy for Malaria Elimination in Greater Mekong Sub-region (2015-2030), the Global Technical Strategy for Malaria 2016-2030, and considers lessons learned from successful implementation of malaria control efforts in Myanmar during the past decade. It is fully aligned with the Myanmar National Health Plan (2017 - 2021).

Structure of vector control programme Under the ‘Ministry of Health and Sports’ (MoHS) the ‘Department of Public Health’ (DOPH) is responsible for providing health care services to the entire population in the country. Under the DOPH the VBDC programme is responsible for implementing the NMCP (with its various partners). At central level, the VBDC programme is mandated to formulate plans, policies, standards and norms related to malaria, provide training, conduct operational research, control outbreaks, and provide consultative and advisory services to implementing agencies. At state/region level, VBDC is responsible for the control of malaria, under the supervision of the State/Regional Health Director. The Medical Officers lead the state and regional level VBDC teams which consist of field, laboratory and entomological sections. These teams have responsibilities for supervision and monitoring of implementation at lower levels.

The ‘Myanmar Health Sector Coordinating Committee’ (M-HSCC) (an expansion of the GFATM specific ‘Myanmar-Country Coordinating Mechanism’) was established in 2013 and takes a leading role in coordination of both governmental and non-governmental sectors. The M-HSCC has a Technical Strategy Group (TSG) for malaria, which is led by the Department of Disease Control, with WHO serving as technical secretariat. The mandate of the TSG-Malaria is to provide technical guidance in the development of national strategies, to provide coordination among partners, and to provide clarity on major technical and policy issues. The TSG meets periodically to discuss, review and endorse certain proposals, reports and other documents and carry out the assignments given to them. It also provides broad oversight of the implementation of grants and projects as required. The TSG-Malaria appoints a working group (the Core Group for TSG-Malaria) to deal with specific tasks as necessary.

Myanmar has established a strong and proactive National Malaria Elimination Committee (NMEC) responsible for monitoring progress and coordination of elimination activities. The NMEC has the Vice President as Patron, Minister for Health as Chairperson. Altogether there are 35 members in the committee. The NMEC has a Working Group and an Executive Working Group. Both have the Deputy Minister of Health and the Advisor of the President’s Office as Patrons and are chaired by the Director General of DOPH.

The NMEC Working Group has 60 members, that includes Deputy DGs of all Ministries, all implementing partners of malaria, WHO as technical partner, all donors and all TSG members. Its role is to collaborate with national and international NGOs for development of elimination planning activities and implementation; assist in securing aid and support; provide assistance and technical support for the implementation of operational research; and provide continuous guidance to achieve malaria elimination targets.

The NMEC Executive Working Group has 25 members, mainly from NMCP and State/Regional Public Health Departments and Health Committees. Its role is to oversee the effective implementation of malaria elimination as laid down in the NSP.

NMCP takes the leading role in malaria elimination providing all the necessary support to general health and specialized programme staff based at state/region, district and township


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levels. The decentralization of implementation to states/regions, districts and townships will be in alignment with the National Health Sector Strategy that ensures NMCP is directly responsible for providing funds and HR for malaria elimination activities in the future.

The Entomology Unit is one of the units under the NMCPs Deputy Director Malaria. The unit is responsible for entomological surveillance and operational research relating to malaria and other vector-borne diseases (figure 17) and for guiding vector control policy and practice.

Figure 17. Organizational structure of Entomology Unit in VBDC Programme.

Capacity (manpower, technical capabilities, training, infrastructure and financial resources) VBDC has suffered severe depletion of its HR over the last 20 years and entomological manpower is now very limited. Only four of the seven sanctioned posts for entomologists and seven of the 19 sanctioned posts of assistant entomologists have been filled. Most of the vacant assistant entomologist posts are located in high malaria burden townships. Senior state/region level staff are overwhelmed by the number of tasks they have to attend to: Japanese encephalitis, dengue, chikungunya etc. all require attendance at central level meetings leaving insufficient time to focus on implementation of activities[68].

A human resource development plan has been developed, but this has not been actioned as it is difficult to recruit staff. Budget for staff is available but VBDC cannot attract candidates as public sector salaries are much lower than those available in the UN, NGO and private sectors. There has been a seven-year gap in entomological recruitment, and some interviewees felt that this issue has not been prioritized by NMCP.

As a result of these HR capacity constraints the programme focuses primarily on routine surveillance.

VBDC has its own entomological laboratory and insectary in Yangon but both need renovation. The fact that these facilities are sited in rented properties means that funding partners are unwilling to invest in an upgrade.


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Remarkably, VBDC has only one vehicle, which understandably is allocated to the Programme Manager. Staff use public transport whenever they need to travel to the field, which they pay for themselves before being reimbursed.

Partners involved in vector control and entomology PMI’s budget for Myanmar in 2018 is $9 million. This supports a broad range of malaria elimination related activities implemented primarily through URC, two of which are particularly relevant to vector control and entomology: Strengthening the entomological monitoring component of focus investigations and strengthening insecticide resistance monitoring and management (with emphasis on capacity development through training); and, procuring approximately 300,000 LLINs to cover at-risk-populations in areas not supported under RAI2E (with emphasis on reaching internally displaced and migrant and mobile populations).

There are numerous SRs under GFATM’s RAI2E grant most of which are involved in supporting the implementation of NMCP’s vector control operations, either technically or in their respective geographical areas. These include: NMCP, Save the Children Federation, Inc (SCF), Myanmar Red Cross Society, Myanmar Health Assistant Association, PSI, Medical Action Myanmar, Malteser International, Myanmar Council of Churches, Myanmar Medical Association, American Refugee Committee, HPA, Shoklo Malaria Research Unit, Mahidol University (SMRU), MC[69], Central Medical Store, Ministry of National Defence (MoND) and WHO.

The Myanmar Department of Medical Research (DMR) is a WHO collaborating centre and it carries-out a significant amount of work in collaboration with VBDC. Although the malaria burden has fallen dramatically in recent years, the disease remains a priority for the DMR (see ‘Research and innovation’ below). DMR has its own laboratories and insectaries in Yangon and in Pyin Oo Lwin near Mandalay. Its entomology staff are well trained and active in a number of research areas (see below).

Intra-sectoral and intersectoral collaboration The NMCP works closely with a number of government departments in order to implement various activities. A key collaboration affecting vector control operations (to some extent at least) is the formal 2017 cost sharing agreement between malaria, HIV, TB and leprosy for Community Malaria Volunteers.

There is a major collaboration with China implementing cross-border malaria control interventions in ‘Special Development Zones’ along the border in the north of the country, as well as through HPA (supported under Myanmar’s component of the RAI2E grant).

Since 2014 there has been a high-profile collaboration between Myanmar and Thailand in Tanintharyi Region, where IRS is carried-out along both sides of the river border to maintain a cordon sanitaire (covering a population of about 6,000 people on the Myanmar side). Here, as elsewhere in the Sub-region, targeting of IRS appears to be influenced by local politics and is only roughly based on API[68].

Vector control interventions (LLINs, ITNs and LLHNs; IRS; other)

The selection of vector control interventions has been guided by an eco-epidemiological assessment informed by malaria case and entomological surveillance data. Two recent documents provide guidance on key vector control interventions: ‘National policy and implementation strategies on appropriate use of ITN/LLIN for malaria elimination in the


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Republic of the Union of Myanmar, 2017’; and, ‘National policy on indoor residual spray in malaria elimination in Myanmar, 2017’. The quality of these documents is variable. Both would benefit from additional fine-tuning.

In theory, the use of insecticidal interventions follows technical recommendations provided in WHO’s ‘Global plan for insecticide resistance management in malaria vectors’[55], but in fact IRS with synthetic pyrethroids often accompanies LLINs. At present there is often complete overlap of LLINs/ITNs with IRS using alphacypermethrin. VBDC considered adopting a carbamate for IRS but concluded that it was too expensive and toxic. It therefore aims to adopt etofenprox, which is a pyrethroid derivative which has a different mode of action to the synthetic pyrethroids used for LLINs/ITNs.

Larval source management (LSM) is being considered for focal response in future if any situations where vector breeding sites are ‘few, fixed and findable’[70].

There is no culture of hammock use in Myanmar so LLHNs are not considered to be locally appropriate. However, LLHNs have been successfully implemented in other GMS countries that did not have a culture of hammock net use, and so VBDC should consider running an LLHN pilot study in Myanmar.

Targeting Multiple delivery strategies are used to maximize coverage of ITNs in target areas nationwide. In theory, urban areas are excluded, but a recent review of implementation quality for the RAI grant highlighted excessive LLIN coverage in some townships, with nets provided to settled communities in urban areas[68].

In 2011, the VBDC, United Nations Children's Fund (UNICEF) and WHO developed an approach to micro-stratification, which reflected practical experiences from the country and other South-East Asian countries with similar transmission characteristics. This approach allowed the use of simple and available ecological, social and epidemiological indicators to classify any area or village as malarious, potentially malarious and non-malarious. Micro-stratification was completed in 180 Townships in 2012. However, the criteria for micro-stratification have since been revised and are now more objective. Wherever data is available, stratification is now based on the mean API over the last three years at Sub-centre level. Proxy indicators for transmission are still used to stratify risk in areas where epidemiological data is absent or incomplete, especially in conflict areas covered by ‘Ethnic Health Organizations’ (EHO). However, this process does not always work well. During the recent review of data quality under RAI[68] it was noted that because data was not available for Kayah at Central level, the entire state was assumed to be in the most endemic stratum. In fact, much of Kayah should have been in stratum one or two. The reviewer felt that this could quickly have been resolved with better communication between key players at central and state level.

Table 2 presents a summary of the results of the most recent stratification used for the development of the funding application for the current RAI2E GFATM grant.

Table 2: Population breakdown by stratum in 2015 (Note: API >5 - high, API 1-5 - moderate, API >0-<1 low, API 0 - potential/free).


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NMCP recognizes that in areas with highly mobile populations, even moderate or high API in a village does not necessarily imply that local transmission is occurring directly in that village, and that improved surveillance methods that distinguish between locally transmitted and imported malaria are needed to guide the choice of interventions. However, at present measuring API in the human population is considered to offer a more reliable indicator of local transmission than ecological risk factors and risk factors that pertain only to the mosquito vector.

According to the NSP, as the quality of surveillance improves, the stratification will evolve to distinguish between endemic villages and villages where all cases are imported. Endemic villages will continue to receive periodic mass distributions, but in villages where all cases are imported, LLINs will be provided only to targeted populations like forest-goers. The programme will thus move further away from blanket LLIN coverage towards increased focus to maximize cost effectiveness and sustainability.

Targeting of IRS. The recent review of implementation quality for the RAI grant highlighted the fact that targeting of IRS appears to be influenced by local politics and only roughly based on API[68].

The current stratification methodology (based on mean API during the last three years) is questionable. Where caseload is falling so fast, this approach results in what might be considered to be an overly cautious appraisal of risk. The approach to malaria risk stratification should be reviewed.

Quantification of commodity requirements Overall quantification of all vector control commodity requirements is carried out at central level by VBDC with the assistance of technical partners, based on the stratification described under ‘Targeting’ above. The resulting figures for population-at-risk are fed into a Microsoft Excel model that takes in to account existing LLINs, factoring-in the expected lifespan of the LLINs in question and yearly attrition rates due to wear and tear, and loss. The target coverage rate used for large sized LLINs was 1.8 people per net (in-line with WHO recommendations15)[29].

Township officials conduct microplanning for LLIN distribution as part of their routine duties. Microplanning takes into consideration which members of a household share a sleeping space in order to ensure 100% population coverage without wastage. As elsewhere in the region, during microplanning surveys the owners of some larger-scale enterprises

15 The ‘1.8’ is WHO’s guiding figure. Countries are free to modify this depending on their needs, if they find that 1.8 does not work for them. A change away from this should be informed by evidence, however.


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were reluctant to tell government health staff exactly how many workers they employed because of issues related to tax and social security payments.

The number of LLINs allocated to migrants and mobile people was based on best guestimates by experts at central level. Given the budgetary constraints, these guestimates were kept conservative, in the knowledge that additional LLINs could be procured through reprogramming of RAI2E funding and through supplementary procurements supported by PMI if necessary.

10,000 LLINs were procured for security services and selected (inactive) ethnic armed groups in 2017.

Procurement of vector control commodities All LLINs are procured using GFATM funds through its VPP mechanism. In the past operations have often been delayed due to issues relating to procurement and supply management. However, it appears that bottlenecks have now been addressed.

Recent GFATM funded LLIN procurements have been delivered direct to each target state/region by the supplier based on the central level quantification. The state/region takes delivery of the LLINs and signs a receipt for the supplier and sends a copy to the VBDC. The state/region then works with the township focal points to confirm village allocations in-line with broad guidelines from the VBDC. Village level line-listings are developed by peripheral health staff in partnership with community leaders and Community Malaria Volunteers. These line listings are signed by each LLIN beneficiary on receipt. The original is kept at township level and a copy is sent to state/region level. The state/region focal point then compiles a report stating the total number of LLINs delivered and sends it to the VBDC at central level.

Records are kept of all transactions throughout the supply chain and stock inspections are carried out as part of routine annual supervision by upper levels.

Implementation LLINs are provided free of charge to cover the entire population residing in established settlements (villages, displaced people’s camps, prisons etc.) in target communities16. These LLINs are delivered through regular mass distributions every three years (all recent procurements in Myanmar have been of polyester LLINs with an estimated effective lifespan of three years). For people who prefer to use their own conventional net rather than the LLINs provided by the programme, the programme aims to provide a conventional net treatment service using a long-lasting insecticide formulation during mass distribution campaigns17, as it has in the past. However, WHO prequalified products that were adopted from the former WHOPES list are no longer commercially available, and this aspect of service delivery has stalled as a result.

16 The ‘within allocation’ request to GFATM under RAI2E for LLINs for settled communities covered only stratum 3a

(API>5), LLINs for strata 3b, 3c and 2 were requested as part of the ‘above allocation’ request but are as yet unfunded. 17 According to the national policy document, the retreatment service is restricted to communities where ownership of conventional nets exceeds 20%, even though all of the evidence seems to suggest that ownership of such nets is much higher than this everywhere.


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Where appropriate, additional LLINs18 are provided for key risk populations and to maintain coverage in targeted Sub-centres:

• LLINs are also given to pregnant women. These nets are delivered through ANC services,

an approach that maximizes LLIN coverage for infants and has a positive impact on ANC

attendance.

• LLINs are provided for use in forest/forest farms (targeting informal-sector forest

workers e.g. small-scale gem/gold miners, people gathering forest products and

traditional swidden farming communities respectively). These nets are delivered in LLIN

target communities during routine mass distribution.

• LLINs are provided to employers to provide to their workers. This intervention targets:

construction project settlements (e.g. dams, bridges and mines); plantations (e.g.

rubber, palm oil, fruit, coffee etc.); forest workers in the formal sector (e.g.

forest/wildlife protection services); and, camps associated with commercial projects

(e.g. road/railway construction, large-scale logging).

• LLINs are also provided to managers of farms to give to their seasonal agricultural

workers when they arrive.

• LLINs are provided to people in new settlements e.g. Internally Displaced People (IDP),

roadside economic migrants, settlements adjacent to construction projects.

• LLINs are supplied through malaria clinics and volunteers at forest entry points, targeting

forest workers in the informal sector e.g. small-scale gem/gold miners and people

gathering forest products.

• Defence service personnel based in or operating in target areas are protected from

malaria by LLINs distributed by the defence services themselves. Oversight and technical

assistance is provided by the NMCP.

• Continuous distribution of LLINs is provided through the VHV network in order to

address any LLIN attrition in-between mass distributions. LLIN stores are held at

township level.

• VHVs monitor and report on unusual population movements to allow programmes to

react in a timely manner to low LLIN coverage levels caused by the arrival of mobile

population groups in risk areas.

• In the event of disasters, outbreaks and confirmed transmission foci in target areas,

LLINs are provided to anyone who has not already been covered.

These continuous delivery approaches were only introduced in GFATM supported areas in 2017 (some continuous channels were introduced by URC in PMI supported areas some years earlier) and so the implementing partners are learning by doing. NMCP interviewees feel that more use could be made of EHOs to supply LLINs to forest farms in areas that are hard for other implementers to access.

18 The ‘within allocation’ request to GFATM under RAI2E for all additional LLINs covered only strata 3a and 3b (API>1), LLINs for strata 3c and 2 were requested as part of the ‘above allocation’ request but are as yet unfunded.


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Community mobilization Distribution of LLINs is coupled with locally appropriate and gender sensitive ‘behaviour change communication’ to ensure community mobilization and high and correct LLIN usage. All of the various RAI2E and PMI implementing partners are supporting the national programme by providing capacity building in behavioural change communication strategies[71] and delivering behavioural change campaigns at the community level.

Quality control VBDC does not carry-out batch testing of LLINs or insecticides for IRS at port of entry, but it does oversee supervision of implementation.

Compression sprayers for IRS are not being calibrated, but nozzles are replaced on a regular basis.

Supervision of IRS includes assessment of acceptance of IRS by target communities, IRS coverage at village (proportion of target households sprayed) but not at household level (percentage of sprayable surfaces sprayed) and there is no routine assessment of residual efficacy.

Cone bioassays conducted by VBDC entomologists did demonstrate a lack of efficacy in the past with ‘type 1’ Permanets and as a result the programme halted procurement of this brand.

Coverage There is a very strong culture of mosquito net use in Myanmar. Results from the PMI funded 2015 MIS conducted by NMCP in association with MC, which covered 4,731 households during the peak transmission season, revealed very high rates of net ownership among households:

• 99.6% of households owned at least one net of any type and 88% of households

owned sufficient nets (one net per two people) of any type.

• Only 19% of households owned at least one ITN and only 11% of households owned

sufficient ITNs.

• Ownership was better for higher risk households, with 48% of households with one

or more ‘forest-goer’ owning at least one ITN.

• Overall usage was very high, with 93% of respondents having used a net of any type

the previous night.

• But overall usage of ITNs was very low due in part at least to their lack of availability:

only 9% of respondents used an ITN the previous night.

• In households with sufficient ITNs to cover all inhabitants this figure rose to 69%.

• Among respondents in hard-to-reach areas, who are considered especially

vulnerable, 65% reported having slept under any net the previous night, and 42%

reported having slept under an ITN.

The NMCP’s recent external review[72], recommended retreating existing conventional nets with a long-lasting insecticide formulation in preference to distributing LLINs to those who already used conventional nets. This approach would have the advantage of ensuring that the nets people were actually using were treated, the annual campaigns required would provide a valuable opportunity for BCC and community mobilization, and depending on the


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cost of the insecticidal formulation, the intervention could be more cost effective than mass distribution of LLINs, particularly given that some of the LLINs distributed are never used. LLINs would still be required for those without conventional nets. The main disadvantage of treating conventional nets is that the approach is relatively labour intensive.

Unfortunately, production of both commercial brands of long-lasting insecticide net treatments has ceased.

A follow-on study in 2016 covering 32,052 people including 1,514 forest-goers in 7,042 households selected from every state/region except Chin State, revealed:

• 98.9% of households had at least one mosquito net and 69.8% had at least one LLIN/ITN; 40.8% had sufficient LLIN/ITN.

• 90.3% of household members slept under any net and 53.7% slept under an LLIN/ITN (age/gender had little effect).

• Of those households with sufficient LLIN/ITN, 84.5% slept under their treated net (for ITNs the date of last treatment was not considered in the analysis).

• 13.7% of all households had members who went to the forest within the last three months and 4.7% of all household members went to the forest within the last three months.

This last finding is probably broadly applicable across endemic communities in the GMS. It suggests that the common practice in the region of providing 1 supplementary LLIN\LLHN per household for forest-goers is an extremely ineffective way of targeting this high-risk group. Furthermore, it suggests that the estimated quantity of LLINs/LLHNs needed to protect forest-goers is seriously underestimated in some countries.

More quantitative data on the use of mosquito nets by MMPs would be useful.

Key risk groups Traditional farming communities. Many ethnic minority groups have large communal villages that are left all but empty for much of the year as families spend months away tending their crops in small farms scattered through the nearby forest. In addition, individuals (usually young men) may spend short periods away from their homes or forest farms, hunting or collecting forest products. Access to healthcare is often made even more difficult as a result.

Forest-goers and seasonal workers. People involved in forest-based activities in both the formal and informal sectors are at high risk of contracting malaria. Key risk groups include defence services (army, police and border guards), forest/wildlife protection services, workers involved in timber extraction (including illegal loggers and sandal wood collectors and groups digging out timber stumps for the production of carved ornaments), workers involved in infrastructure development projects (such as building roads and dams), workers involved in agricultural development projects (establishing rubber, cashew and coffee plantations), gem and gold miners (e.g. in Mandalay), and increasingly tourists.

Seasonal workers harvesting fruit from orchards and rice close to the forest are also at high risk. While the forest-goers described above are mostly men, the seasonal workers include many women. In each case, workers may come from villages near the forest but many also


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come from other regions when seasonal demand for labour in those areas is low. Often, they have little or no immunity to malaria.

Defence services. The defence services form a sizable and particularly mobile high-risk group. They are often deployed in hard to reach areas, based in camps located in the forest or forest fringes. While on night patrol duties they are at particularly high risk of contracting malaria. The fact that they are often redeployed long distances to new malaria endemic areas means that they have the potential to introduce parasite strains that are new to these areas. This is a particular concern given the possibility of multi-ACT resistant P. falciparum being introduced to Myanmar from elsewhere in the region by retuning migrants. Reaching these mobile populations with appropriate prevention and case management services is crucial to the success of malaria control and elimination efforts in Myanmar.

Internally Displaced People. Due to ongoing clashes between the defence services and non-state fighters in Kachin, Rakhine and Northern Shan States, IDPs remain a significant problem in Myanmar. UNHCR reported 514,000 IDPs in December 2015 (of which around 120,000 were in Rakhine and around 100,000 were in Kachin and Northern Shan States). These populations generally have less access to the services and hence are less well protected from malaria than other populations in the same areas. Malaria prevention and management services including LLINs and occasionally IRS are provided by HPA to non-combatants according to NMCP guidance. However, rebel fighters, who constitute one of the main risk-groups in these areas, are not supported by HPA in any way.

Cross-border workers. These are a diverse mobile population who cross the border for work, both legal and illegal. Some are long term or permanent migrants, while others cross the border often or even daily. According to the International Organization for Migration (IOM) there are an estimated two million Myanmar nationals based in Thailand at present and about 200,000 in Bangladesh. While many of these spend their time abroad in urban or other non-endemic areas others, particularly seasonal agricultural workers (see above), are based in areas where transmission does occur. There is a possibility that cross-border workers retuning from parts of the GMS could introduce multi-ACT resistant P. falciparum to receptive areas of Myanmar.

Migrants. Migrants may be found in most of the situations described above, working for large private companies, living in unauthorized housing developments, working as seasonal agricultural labourers or as informal forest workers. Migrants, both national and international, are a particular concern in that they could potentially contribute to the spread of artemisinin resistant malaria parasites.

All of the mobile and migrant populations described above can be considered to have disproportionately low access to prevention services. Key factors contributing to this inequality include: language (often only a small proportion of people from ethnic minority groups speak the national language making communication of health messages problematic); remoteness (malaria transmission tends to be most intense in remote areas, commonly along borders, where access to both public and private sector healthcare services is relatively limited); poverty (the populations living in or passing through these remote areas are generally some of the poorest in the country); marginalization (ethnic minority groups and migrants are amongst the most marginalized groups in the country); and mobility (the high mobility of some individuals means that they may have moved to non-


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endemic areas, where health workers are less likely to be familiar with malaria, when symptoms first appear).

Data systems Reporting relating to LLINs and IRS is generally based on implementation reports. Data flows up from implementation teams to VBDC at central level, via the VBDC focal point at the state/region and township level with data compiled at each stage.

The collection of entomological data is paper-based using standard formats. The data is entered into a database at central level and hard copies are filed. Findings are shared with the NMCP and its implementing partners annually, during six-monthly VBDC review meetings and on an ad hoc basis as required.

Monitoring and evaluation of vector control VBDC has a relatively well-established M&E system described in its ‘Monitoring and Evaluation Plan 2016-2020’. Key programme outcome indicators relating to vector control and entomology include: ‘Percentage of households in target areas with at least one ITN’ and ‘Percentage of people in target villages who slept under an ITN during the previous night’ (disaggregated by age and sex), both measured by means of household surveys in a representative random sample of households in a representative random sample of villages targeted by the vector control programme (MIS - as conducted by NMCP in collaboration with MC in 2016)[73]; ‘Percentage of mobile/migrant population in targeted areas who slept under an insecticide-treated net the last time they slept in a transmission area’ measured by means of special MMP surveys in a representative random sample of people from MMPs in high risk areas; and, ‘Percentage of foci fully investigated and registered within three days of detection (including malaria focus investigation form, entomological investigation form and focus geo-referencing and mapping)’ measured by means of the routine Health Information System (HIS).

MC is supporting the national programme by providing capacity building in monitoring and evaluation methods.

Vector surveillance A recent document developed by NMCP and technical partners provides guidance on key entomological monitoring and surveillance: ‘Guidelines and standard operating procedures for entomological monitoring and surveillance, 2017’. As with the two vector control documents described above, this document would benefit from some fine tuning particularly to simplify and improve the relevance of the guidance presented.

Indoor and outdoor man-landing catches and cow-baited trap-net catches, as well as indoor and outdoor resting catches, are used routinely for vector surveillance in Myanmar. These traditional collection techniques are well described in WHO’s 2013 ‘Training module on malaria control: Entomology and vector control’[74].

Identifications are based primarily of morphological characteristics, but increasingly molecular techniques are being used. VBDC is aiming to establish its own molecular entomology facility, but in the view of some advisers this would not be a good use of funds, given that samples could be processed relatively cheaply if outsourced to facilities in Thailand.

ELISA sporozoite tests are being carried out routinely. Tests on 2,393 Anopheles mosquitoes collected in 2017 revealed just five sporozoite positives (one An. minimus [P. falciparum],


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one An. annularis [P. vivax], two An. aconitus [P. vivax] and one An. philipinensis [P. falciparum]). No confirmatory PCR testing was carried out and so the value of these findings is questionable. The NMCP should consider dropping ELISA testing as a part of routine surveillance and restricting its use to special studies (e.g. investigating the micro-epidemiology of malaria transmission in transmission hotspots in the forest). All positive results should always be cross-checked with PCR to identify false-positives, which are especially common amongst more zoophilic vectors[54,75].

Insecticide resistance monitoring The NMCP and other research groups assess insecticide resistance in selected high disease burden sites on an ad hoc basis (entomological investigations are not conducted as part of focus investigations at present, but this is planned for the future). Seven sites were investigated by NMCP in 2017. The assays used look at phenotypic resistance in wild caught adult females. All anopheles species collected in sufficient numbers are tested. These are collected mainly from cow-baited net-traps and so tend to be blood-fed. Staff were trained recently on the CDC bottle bioassay technique, but they continue to use the WHO bioassays in preference.

Vector bionomics and insecticide susceptibility status are also monitored routinely by DMR at selected sites in Kayah and Mon States and Bago Region.

There is widespread pyrethroid resistance in An. hyrcanus and pyrethroid resistance has also been found in An. vagus in Naypyitaw. There is no evidence of insecticide resistance in important vectors of malaria at present.

Ad hoc surveys may be carried out in additional sites in outbreak areas (where insecticide resistance may have contributed to the outbreak) and in areas at high risk of insecticide resistance (e.g. areas with high agricultural pyrethroid use).

Resulting data is shared with WHO and technical partners. If insecticide resistance is found its operational significance will be assessed and a suitable response will be developed as required.

Myanmar does not have an insecticide resistance management plan in place at present.

Research and innovation The VBDC does not conduct any entomological research of its own, but it does collaborate with other research groups such as the DMR and PSI where funding permits.

The VBDC insectary in Yangon rears An. minimus and Aedes aegypti and at present is conducting bioassays in support of PSI’s assessment of the residual efficacy of LLINs. This study is being run in collaboration with VBDC, which is conducting bioassays on the samples provided by PSI. However, there appeared to be no ownership of the study on the VBDC side, with VBDC staff completely unaware of the protocol being used by PSI for sample collection.

The Japan International Cooperation Agency (JICA) is supporting VBDC to conduct cross-sectional surveys in Myanmar’s central mountains looking at the relationship between topography, land use and vector landscape, with a view to using topography and land use to stratify the country according to receptivity.

In 2013, the Myanmar Health and Development Consortium (MHDC) carried out mapping of employees in different industries in three malaria endemic districts in Myanmar. The


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resulting reports highlighted the scale of workplace related malaria risk and identified means of increasing understanding of public-private partnerships and increasing corporate social responsibility.

MC is also involved in operational research in Myanmar. Activities include behavioural research to understand consumer preferences and barriers to the use of LLINs[76], rapid coverage monitoring of net distribution, qualitative assessment of personal protection measures and behaviours of at-risk populations. In 2015, a collaborative study between DMR with MC demonstrated a high level of acceptability for insecticide treated clothing amongst rubber tappers in Mon State[77].

SMRU, URC and IOM are conducting studies on the movements of migrants and mobile populations, including through the use of Global Positioning System (GPS) technology.

Recently DMR’s Medical Entomology Research Division has conducted a number of research projects on vectors of malaria. Special areas of interest recently have been: Mobility dynamics of migrant workers[78]; Challenges in universal coverage and utilization of ITNs in migrant plantation workers[79]; and, The efficacy of various natural and synthetic repellents. The DMR’s Medical Entomology Unit in Yangon has an insectary with colonies of An. minimus and An. dirus. The An. dirus colony is maintained through artificial mating.

An advanced molecular laboratory for research on communicable diseases was established at DMR in Yangon with support of the Korea International Cooperation Agency (KOICA) during 2011-2014. This project was implemented with the aim of strengthening laboratory research capacity on malaria as well as viral hepatitis and tuberculosis. The DMR now has state-of-the-art facilities for PCR and ELISA. It is currently collaborating closely with Duke University in North Carolina especially on ultra-sensitive quantitative PCR (qPCR). A current focus of the molecular work at DMR is identifying genes for insecticide resistance.

DMR coordinates a Malaria Scientific Working Group, which is composed of scientists from all backgrounds which meets twice per year. DMR holds a national symposium annually which is well attended by national and international delegates. Senior staff at DMR felt that despite these efforts communication with VBDC and other malaria stakeholders in the country and in the Sub-region could still be improved.

Thailand – Country profile There has been a mostly steady reduction in malaria burden in Thailand during the last decade (figure 18). Caseload fell from an 75,000 in 2007 (Bureau of Vector-borne Diseases (BVBD) estimate) to 17,246 in 2016[58]. Malaria deaths have decreased from 97 in 2007[49] to 27 in 2016[58]. These cases and deaths include those who crossed the border and sought treatment at malaria posts and health facilities in Thailand. The proportion of cases caused by P. falciparum has fallen from 42% in 2010 to 28% in 2016.

Figure 18: Malaria morbidity and mortality in Thailand among Thais and non-Thai migrants (M1 migrants - in Thailand for six months or longer, and M2 migrants - in Thailand for less than six months) during 2000-2016. (Source: BVBD from PMI)


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In Thailand malaria cases mainly occur in provinces bordering Myanmar, Cambodia, and Malaysia (figure 19).

The conflict in southern Thailand has contributed to a recent dramatic malaria resurgence. In Yala, Songkla, and Naratiwat provinces bordering Malaysia malaria caseload (mostly P. vivax) during October to February of FY 2016 and FY 2017 increased from 317 to 4,766 respectively.

In 2013, demand for expensive hard wood resulted in increased illegal logging in the forests in the north-eastern of Thailand and in adjacent provinces in southern Lao PDR and northern Cambodia, leading to a multi-country outbreak and 10% surge in malaria caseload in Thailand.

In the southwest of Thailand, on the border with Cambodia, falling rubber prices have recently forced rubber plantation workers to supplement their income by collecting forest products, which is leading to localised increases in malaria transmission.

As elsewhere in the region, the spread of artemisinin resistance and difficulties addressing forest-based transmission remain serious challenges to the achievement of national elimination goals.

Figure 19. Villages with malaria transmission in Thailand, 2015-2016. (Source: BVBD from PMI)


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Policy framework for vector control The 12th ‘National Health Development Plan’ (NHDP) 2017-2021 falls under the 12th ‘National Economic and Social Development Plan’. It is a five-year plan which serves as a mechanism to facilitate the implementation of the 20-year ‘National Health Strategy’. It sets out to strengthen, support and foster a multi-sectoral participation by the public sector, private sector, academics and civil society, in developing and governing Thailand’s health system to be strong and responsive to the changing landscape.

There are four Health Development Strategies within the NHDP:

1. Health promotion, disease prevention and consumer and environmental protection excellence (P3 excellence);

2. Foster fair treatment and reduce inequality (service excellence);


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3. Develop and create a mechanism to increase the efficiency in managing HR for health (people excellence);

4. Develop and strengthen health governance system (governance excellence).

Efforts towards achieving malaria elimination set-out in the National Malaria Elimination Operational Plan 2017-2021 are aligned to these strategies:

Structure of vector control programme[80] The Thai Malaria Control Programme was a vertical programme from its inception in 1949 until 1996, when it partially merged with other vector-borne disease programs. It is now called the Bureau of Vector-borne Diseases (BVBD) within the Department of Disease Control in the Ministry of Public Health (MoPH). BVBD is the programme manager of the NMCP. Currently, the malaria control programme is undergoing decentralization to the general health service, reducing the number of specialized field malaria officials and funds. The organigram in figure 20 presents both the original (left hand side) and the new (right hand side) structure for the delivery of malaria control services. Programmatic responsibilities including entomology are being progressively transferred to ‘Provincial Public Health Offices’ (PPHO) and ‘Health Promoting Hospitals’ are taking over responsibility for LLIN distributions. However, to date no capacity strengthening has been provided for the staff who are newly responsible for malaria control and PPHOs have no plans to recruit entomologists (see ‘Capacity’ below).

BVBD remains responsible for malaria-related research, generating policy for malaria control, and evaluating the programme.

In addition to malaria clinics, malaria posts (community-based malaria clinics) were introduced under GFATM funding to manage malaria in vulnerable populations and foreign migrants in remote areas along international borders. These posts are operated by villagers called Malaria Post Workers (MPWs) equipped with microscopes or RDTs. Additionally, all endemic communities have Village Health Workers (VHW) who are actively involved in malaria prevention and health promotion activities. Under Global Fund Round 7, Migrant Health Volunteers (MHV) equipped with RDTs and ACT were also introduced to complement the role and function of MPWs.

Figure 20. Reporting, supervision and coordination at each level of implementation of Thailand’s NMCP during transition from vertical (left) to decentralized structure (right).


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Sub-districts are responsible for procuring their own commodities for vector control unless commodities are procured under GFATM support, in which case the process is centralized. Procurement at sub-district level is not necessarily in-line with recommendations from BVBD.

Regional coordinators are the link between BVBD and VBDC at provincial level, however they tend to have limited malaria knowledge and capacity. Senior interviewees explained that regional coordinators are more senior than managers at BVBD and so BVBD does not have authority over what happens at regional level.

‘…in some regions guidance from BVBD is often disregarded’.

Capacity (manpower, technical capabilities, training, infrastructure and financial resources) There are approximately 80 entomologists working with Thailand’s NMCP. In addition to malaria they are responsible for all other endemic vector borne diseases, as well as for the control of nuisance insects. Most are trained in agricultural entomology. Many are on two-year government contracts and so tend to leave VBDC when government agricultural entomology jobs become available. Staff attrition rates are high.


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Every year, training on vector borne diseases is provided by BVBD and university staff. Focus investigation training was conducted for VBDC-level entomologists and insect collectors in 2015 and 2016 and will continue on an annual basis if funds permit.

Senior managers at BVBD felt that it would be very useful if recruits were to attend the six-month ‘Diploma in Applied Parasitology and Entomology’ at the Institute for Medical Research in Malaysia and that this might reduce staff attrition rates.

At central level (BVBD) there is a focal person for each subject area (vector surveillance, taxonomy, chemical control, other vector control etc.) but all work together to address issues as needed. MoPH entomologists spend a lot of their time ‘firefighting’ for other vector borne diseases.

Twenty years ago, the malaria division was very strong, however, the consolidation of communicable and non-communicable diseases under the Department for Disease Control (when the malaria division became BVBD) weakened the system considerably.

The government is no longer recruiting staff for Vector Borne Disease Units (VBDU) to be posted at district level or malaria clinics, so these units will close as staff leave or retire. In theory, the activities conducted by VBDUs and Malaria Clinics will in future be conducted by staff at the new ‘Health Promoting Hospitals’, but no training has been given or is planned for these staff. Thus,

‘…responsibility, but not capacity, has been transferred from VBDCs to Provincial Health Authorities’.

Senior interviewees explained that morale amongst staff at VBDCs and VBDUs is now ‘desperately low’. They felt that BVBD is in need of radical reform.

Partners involved in vector control and entomology Malaria Consortium. MC opened its Asia office in Thailand in 2008 focusing on the containment and elimination of multi-drug resistant falciparum malaria in the GMS. With support from GFATM’s RAI grant, MC is working closely with the Thai NMCP at national and provincial levels, as well as with local NGOs along Thai-Myanmar and Thai-Cambodia border. MC has been leading on M&E, including periodic large-scale surveys, to ensure effective implementation. MC is also providing technical support for the development and revision of a behaviour change communications strategy for Thailand. MC is also responsible for coordinating and facilitating various capacity building activities and undertaking operational research (see ‘Research and innovation’ below).

US President’s Malaria Initiative. PMI works with partner organizations and the NMCP to strengthen malaria surveillance systems, to improve the national programme capacity for quality laboratory diagnosis, and to ensure that all patients have access to critical anti-malarial drugs and other malaria services. During 2018, PMI will support entomological monitoring and insecticide resistance management with emphasis on entomology for focus investigations and resistance monitoring. PMI will also provide support for entomological capacity strengthening, in response to the changing vector ecology including updating malaria entomology curricula used for regional training. PMI procured approximately 200,000 LLINs for migrant and vulnerable populations in 2017 and will procure approximately 300,000 LLINs (for Thailand and Lao PDR) in 2018 to address commodity gaps not covered by GFATM. It will also support LLIN distribution and associated BCC activities.


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The Armed Forces Research Institute of Medical Sciences (AFRIMS). AFRIMS has long been a valuable resource for entomology in Thailand providing entomological training for many groups both at national and at regional levels and supporting operational research (see below).

Mahidol University, Faculty of Tropical Medicine, Dept. of Medical Entomology. Mahidol is supported under the US NIH ICEMR programme as part of the ‘South East Asia Center of Excellence’. The Department of Medical Entomology is actively involved in education, research and public service. Apart from the regular subjects of Medical Entomology for the regionally popular ‘Diploma in Tropical Medicine and Health’ (DTM&H) course, Master’s in Tropical Medicine and Doctorate in Tropical Medicine, the department also provides tailored training on medically important arthropods and vector control both for individuals and groups on request.

Kasetsart University. Kasetsart University’s Department of Medical Entomology works closely with the MoPH and BVBD, providing high level training and conducting joint research.

Institut de Recherche pour le Developpement (IRD)/Institute Pasteur. The IRD works closely with Kasetsart University with the ‘The STOP-VEC’ research project.

The Asian Collaborative Training Network for Malaria (ACTMalaria). ACTMalaria provides training and mentoring for entomology and vector control across the Asia-Pacific Region. Most recently two staff from the BVBD attended a training for entomological monitoring and insecticide resistance testing in Manila. ACTMalaria sponsors a range of courses on many aspects of malaria and dengue control in the region, including a course on Integrated Vector Management and a course on the Management of Malaria Field Operations which includes a module on entomological monitoring.

The Asia Pacific Malaria Elimination Network (APMEN). APMEN’s Vector Control Working Group supports information exchange between vector control experts and national programmes of Asia Pacific countries, and identification of solutions to the challenges faced in the region. High priority challenges include insecticide resistance, larval source management, local vector surveillance, and improving the consistency and targeting of vector control interventions. The working group has supported a range of activities to build vector control capacity in the region, including providing training fellowships to vector control officers in priority areas, supporting community efficacy studies of interventions, and consolidating information on vector management practices in the region.

The working group’s objectives are: • To advocate for the level of vector control capacity at regional and country level

required to attain and maintain malaria elimination. • To stimulate, and where possible coordinate, operational research to support the

implementation of solutions to the unique vector control challenges faced by Asia Pacific countries.

• To review current vector control strategies, interventions and their effectiveness in various operational and epidemiological settings to:

o identify challenges for effective vector control implementation in different country programs; and

o establish what works, where - especially within vulnerable and mobile populations.


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Intra-sectoral and intersectoral collaboration There is a high level of intra-sectoral collaboration at all levels, especially where integration has already occurred. Entomologists and staff involved in vector control at BVBD move freely between workstreams (malaria, dengue, nuisance mosquitoes etc.) as needs arise. A province and district level vehicles and equipment are shared as necessary. Intra-sectoral collaboration is a formal policy of BVBD ordered by the Minister for Health.

There is also a degree of Intra-sectoral collaboration across borders, with BVBD supplying An. minimus to the NMCP in Myanmar for example, and an ongoing assistance program for malaria and other vector-borne diseases in Cambodia initiated by Her Royal Highness Princess Maha Chaki Sirindhorn of Thailand in 2008. Thailand also shares programme data internationally through WHO’s data sharing platforms.

Both a ‘National Steering Committee on Malaria Elimination’ and a ‘National Executive Committee on Malaria Elimination’ chaired by the Deputy Prime Minister have been established to support malaria elimination and promote intersectoral collaboration. The Ministries of Interior, Education, Defence and Environment are represented alongside the Ministry of Public Health. BVBD is working closely with various government agencies within and among the ministries through routine day-to-day coordination and collaboration and through the works of the committees [81], including:

• Ministry of Interior – migrant issues, cross border collaboration

• Ministry of Agriculture – the use of insecticides, deforestation

• Ministry of Defence – malaria treatment in Ministry of Defence hospitals, research

• Ministry of Finance – budget to support malaria programme

• Academia/Universities – research, monitoring and evaluation.

Vector control interventions (LLINs, ITNs and LLHNs; IRS; other) LLINs are distributed through a process of rolling mass distributions amongst Thai and registered Non-Thai (‘M1 migrant’) populations in endemic areas, whereby every village is visited every year and LLINs are supplied according to requirements. LLINs are also provided for unregistered foreign nationals (‘M2 migrants’) attending peripheral public health and NGO-run health facilities.

LLINs are now prioritized over IRS, with BVBD encouraging NMCP implementers only to use IRS where nets are not appropriate (e.g. in populations where utilization is habitually low). As mentioned above, adherence to BVBD advice is variable.

LLHNs are also being distributed in target A1 and A2 areas in order to provide protection from malaria for forest-goers.

The NMCP retreats conventional nets as well as LLINs more than three years old with bifenthrin or locally produced deltamethrin 25% WT.

In A1 and A2 areas, limited quantities of GoT procured topical repellents are distributed to migrants and soldiers spending time in the forest.

LSM is not recommended by BVBD as it is not considered useful for the control of An. dirus or An. minimus as breeding sites are rarely ‘few, fixed and findable’. However, some VBDCs do practice LSM using larvivarous fish despite BVBD guidance.


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Similarly, fogging with deltamethrin is used for the control of malaria vectors in some areas, against the advice of BVBD.

WHO prequalified LLINs are not approved for domestic retail sale in Thailand.

Targeting Thailand’s malaria surveillance data is comprehensive and timely. Malaria risk is stratified annually at the village-level. Until recently the stratification was carried out according to the following criteria:

• A1: Perennial transmission area (transmission reported for at least six months per year)

• A2: Periodic transmission area (transmission reported for less than six months per year)

• B1: High and moderate receptivity (transmission not reported within the last three years but primary and secondary vectors present)

• B2: Low and no receptivity (transmission not reported within the last three years and

primary and secondary vectors absent, suspected vector may be present)

But, recently A1 and A2 strata have been revised based on focus classification and in-line with the requirements of elimination:

• A1: Active focus (Locally acquired case(s) have been detected within the current calendar year);

• A2: Residual non-active (The last locally acquired case was detected in the previous calendar year or up to 3 years earlier);

A1 and A2 villages are targeted to receive LLINs (RAI2E supported) or IRS. Treatment of conventional bednets is supported under the government budget.

M2 migrants attending Malaria Clinics or Malaria Posts in A1 and A2 areas are provided with either an LLINs or an LLHN if they do not already have one.

In addition, LLINs and bed mats are distributed by NGOs to all residents in camps along the Thai-Myanmar border on arrival and on a three-yearly replacement basis.

Quantification of commodity requirements Quantification of all vector control commodity requirements is carried out at central level by BVBD with the assistance of technical partners, based on the stratification described under ‘Targeting’ above and on population data from the latest census adjusted for population growth. These figures are fed into an Microsoft Excel model that takes in to account existing LLINs, factoring-in the expected lifespan of the LLINs in question and yearly attrition rates due to wear and tear, and loss. In-line with normative guidance, 1 double LLIN is calculated for every 1.8 people living in settled communities targeted for mass distribution.

Quantification of requirements for LLHNs by forest-goers has been based on local expert guestimates of need tempered by the desire to keep budgets manageable for funding partners (1% of the total population in A1 and A2 villages is estimated to spend nights in the forest).

Surveys will be conducted prior to distribution in order to accurately quantify the number of LLINs and LLHNs needed per household in each target village.


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Procurement of vector control commodities All LLINs and LLHNs procured using GFATM funds are sourced through the VPP mechanism. Under RAI2E, the programme is procuring high quality LLHNs (hammock with integral net) at a cost of US$14 each, including delivery to end user. Insecticide is procured exclusively with national funds. At present deltamethrin 5% WP is used for IRS and locally produced deltamethrin 25% WT is used for dipping conventional nets.

There are twelve regions, each procures its own insecticide. BVBD procures insecticides for emergency use. Only insecticides approved by BVBD are procured. These include bifenthrin, etofenprox, deltamethrin, alpha-cypermethrin and lambda-cyhalothrin. Selection is based on conformity with product specifications and cost. All procurement follows national guidelines issued by the Food and Drug Administration, which are in full compliance with WHO procurement standards.

Taxes and tariffs for vector control products supported by external funders are waived.

Implementation BVBD provides overall management for the procurement and distribution of LLINs, which are scheduled to be replaced every three years. Macro-distribution to provincial level is through the supplier (LLINs will be delivered in their containers which will serve as storage prior to micro-distribution). Micro-distribution of LLINs and insecticide for treating ITNs for Thai residents and M1 migrants will be managed by the BVBD through the government channels described in the organigram in figure 20, as well as through sub-recipient (SR) NGOs in the case of refugee camps for example.

BVBD also manages continuous distribution of LLINs and LLHNs for M2 migrants through malaria clinics and malaria posts. Further efforts are needed to increase access to LLINs by hard to reach at-risk populations, especially M2 migrants.

Mass preventive IRS is timed to take place immediately prior to the predicted seasonal increase in transmission leading up to the peak transmission period. Focal responsive IRS is carried-out as required. Hudson X-Pert compression sprayers are the application tool of choice. Depending on the formulation and on the situation one or two rounds of IRS may be applied in a year.

Interviews conducted during a field visit to Chanthaburi VBDC showed a variable approach to vector control. Using the new stratification tier definitions (updated in-line with elimination terminology) A1 areas are targeted with IRS, A2 areas are targeted with ITN, and staff at malaria clinics give LLINs to M2 migrants if they are slide positive or have a temperature over 37.5oC. In addition, LLINs are provided to any cases detected during active case finding who do not already have an LLIN. Active case finding is carried out in all A1 and A2 villages. Staff said that they use whichever form of vector control seems best suited to the area in question and do not necessarily follow guidelines from BVBD. They said that generally, people in A1 and A2 areas have at least one vector control measure in place with more than 20% overlap of IRS/LLINs. ‘Olyset’ LLINs were apparently not popular and some people used ITNs in preference. There were also complaints that the LLINs provided were too small and had an unpleasant smell.

Community mobilization BVBD develops BCC materials for the Thai resident population. This includes a school-based programme based on a strategy launched in 2000, which involves the provision of teaching


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manuals, textbooks and teacher training (a study confirmed that as a result of the programme, schoolchildren changed their behaviour positively towards malaria prevention[82]).

IOM and its RAI2E grant Sub-Sub-Recipients (SSRs) are playing leading roles in the development of BCC materials for migrants and mobile populations. One SSR is supporting BVBD’s school-based programme by conducting workshops to develop a curriculum and associated materials. Other SSRs are developing materials for refugee camps along the Thai-Myanmar border. Language specific materials are developed for migrant populations.

A recent GMS-wide assessment of vector control by ‘NetWorks’ identified a number of issues undermining BCC and community mobilization in Thailand[80]. These included:

• a lack of behavioural research relating to bednet preferences, willingness to pay and interest in alternative tools for personal protection.

• a lack of lesson learning from advocacy efforts associated with inter-sectoral collaboration for HIV/AIDS

• a lack of mapping of malaria relevant Special Economic Zones – businesses and their migrant labour force

Quality control There is no routine batch testing for vector control products in Thailand. Batch testing for LLIN and insecticides would only be carried out if no certificate of compliance was supplied by the manufacturer.

Supportive supervision of the implementation of vector control is performed at provincial, district and municipal levels to ensure that the quality of programme implementation is high, but BVBD managers feel that more budget is needed to improve the coverage and frequency of these efforts, especially at municipality and sub-district hospital levels. Capacity building has been planned to help to address this issue.

BVBD conducts testing of LLIN/LLHN samples from the field every year to assess their efficacy over time under local conditions.

Coverage The number of LLINs distributed, number of ITNs treated and number of people protected by IRS are determined annually and details are communicated to WHO for the World Malaria Report. Approximately 362,500, 348,700, 237,400 people were protected with IRS in 2014, 2015 and 2016 respectively. Approximately 528,900, 251,500, 454,700 LLINs were distributed in 2015, 2016 and 2017 giving a modelled coverage of the population at risk in the then target area of 80%, 95% and 100% respectively.

Coverage and utilization rates are also assessed periodically by means of household surveys. A cross-sectional household survey conducted in malaria endemic regions in Thailand in 2016 revealed that ownership of at least one ITN/LLIN was 52.3% and of sufficient ITNs/LLINs was 40.3%, although ownership of ITNs/LLINs among those living in GFATM supported areas was higher[83]. Most nets owned were conventional nets bought from the market. Only 10% of owned nets were ITNs. Usage of an ITN/LLIN the previous night amongst those with access to an ITN/LLIN was just 52%. Usage was higher with larger nets, coloured nets and nets made from nylon or cotton.


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Post distribution surveys will be conducted in a representative random sample of target villages covered by RAI2E, and these will provide a measure of access and utilization.

Key risk groups Thailand draws large numbers of migrant workers from Myanmar, Cambodia, and Lao PDR. Many of these migrant workers live and work in border districts and provinces where malaria is still endemic, while others move back and forth between home communities and various work destinations in Thailand.

Data systems Thailand has an online reporting system called ‘Malaria online’ for programmatic data (developed by ‘Biophics’ using Arc-GIS data), plus a separate entomological database for insecticide resistance and vector distribution and density data.

The Thai vector control reporting forms are electronic, with line listings by household. Unfortunately, it is not possible to identify the level of overlap between LLINs/ITNs and IRS as there is a separate database for each. There are some issues associated with data entry and BVBD is now trying to motivate information technology (IT) staff to enter data in a timely fashion. One problem with the input of vector control data is that there are two separate reporting channels: It is the responsibility of the Provincial Health Officer (PHO) to report GFATM related vector control activities (LLINs), but the VBDU/VBDC/ Office of Disease Prevention and Control’s (ODPC) responsibility to report on vector control activities supported by the domestic budget (ITNs and IRS). Furthermore, an incentive of 15 Bhat is paid with GFATM funds for each LLIN delivered, but no incentive is paid for domestic nets.

Based on discussions with BVBD staff, it seems that the entomology database does not allow automated analysis. Unfortunately, the IT specialist at BVBD responsible for the database (and for mapping entomology data) was in Australia at the time of this review studying for a Master’s degree (for 2 years). This highlights the importance of training more than one person to fulfil each specialized role.

Monitoring and evaluation of vector control M&E associated with LLINs and IRS (coverage, quality and utilization) is systematic. Key outcome indicators relating to vector control are: Proportion of population that slept under an ITN the previous night; Proportion of Mobile and Migrant Population that used an ITN last time they slept in a transmission area; Proportion of households with at least one ITN for every two people; Proportion of existing ITNs used the previous night; Proportion of target households protected by IRS. Data for all of these indicators is collected during periodic household surveys.

As mentioned, unfortunately GFATM supported LLINs are reported separately from Government of Thailand (GoT) supported ITNs and IRS and, as a result, there is no real clarity on the proportion of the population protected by one or the other, or by both interventions.

Vector surveillance Indoor and outdoor man-landing catches and cow-baited trap-net catches, as well as indoor and outdoor resting catches, are used routinely for vector surveillance in Thailand. These traditional collection techniques are well described in WHO’s 2013 ‘Training module on malaria control: Entomology and vector control’[74].


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Entomological collections were carried out in 18 sites in stratum B (no malaria for last three years) under GFATM in 2017 and findings were used to identify B1/B2 stratification status (with [B1] or without vectors present [B2]). Given that there are no differences between the way B1 and B2 areas are treated by the NMCP, the rationale for this work is unclear.

Identifications are based primarily of morphological characteristics, but increasingly molecular techniques are being used.

AFRIMS conducts entomological surveillance in eight sentinel sites in Thailand every other month. This work is funded by the US Armed Forces Health Surveillance Center-Global Emerging Infections Surveillance and Response System (AFHSC-GEIS) and has been ongoing for many years. In one geographical location in Thailand, species identification based on morphology alone resulted in the identification of 21 species by AFRIMS and just six species by the local VBDU. While different capture techniques may have accounted for some variation in species profile, it seems clear that there was a lack of technical capacity at VBDU level. This is likely a widespread problem and it may therefore have significantly undermined the validity of existing vector maps based on VBDU data.

Some senior interviewees questioned the added value of routine surveillance carried out by VBDUs given these quality related issues and felt that staff time might be better spent focusing on problem solving. The alternative would be a major investment in capacity strengthening, perhaps along the lines of the PMI Cambodia model.

Senior interviewees at BVBD felt that the entomology component of focus investigations is not generally done well, if it is done at all, as there is not enough manpower within the NMCPs entomology staff.

Insecticide resistance monitoring Insecticide resistance monitoring is included in the NSP, but there is no detailed plan in place. Training has been supported through PMI, WHO and ACTMalaria and other partners, including Kasetsart, IRD and Mahidol, have been directly supporting insecticide susceptibility monitoring for some years.

BVBD uses standard WHO bioassay tubes. Staff were trained recently on the CDC bottle bioassay technique, but prefer to use WHO bioassays as they are more familiar with them.

There are three GFATM supported sentinel sites plus two domestically supported sites. The types of insecticide tested are rotated each year. Insecticide resistance test mosquitoes are from cow-baited trap-net catches, so Anopheles are primarily blood-fed and so in the event of suspected insecticide resistance, studies would need to be repeated using unfed F1 test mosquitoes.

Thailand has a separate database for insecticide resistance results. Some regions conduct their own insecticide resistance surveillance and some of these enter their data into the insecticide resistance database, but not all.

There were no reported findings of pyrethroid resistance in An. dirus or An. minimus populations in Thailand from 2000 to 2018. The precise reasons for this are unclear but there are a number of plausible explanations:

• While there is extensive use of agricultural pesticides in Thailand (and elsewhere), the

particular larval habitats of An. dirus and An. minimus are not exposed to run off, as are

those of An. barbirostris, An. subpictus and An. epiroticus (and An. gambiae in Africa),


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and so agricultural pesticides do not result in selective pressure for the development of

resistance. Universal coverage of LLINs may however provide enough selective pressure

to result in pyrethroid resistance in these relatively anthropophilic vectors in future.

• A recent publication suggested that behavioural avoidance to insecticides may have

reduced selection pressure and thus occurrence and spread of insecticide

resistance[84][85]. Among anopheline vectors in Africa, where pyrethroid resistance is

wide-spread, it is becoming increasingly apparent that metabolic resistance, rather than

kdr resistance alone, is more closely linked to control failure, and that the ‘intensity’ or

‘strength’ of resistance is more important than the mere frequency as detected by the

traditional WHO tube assay or CDC bottle assay[86].

BVBD does not actively manage insecticide resistance in malaria vectors but plans to do so once resistance has been detected. IRS, LLINs and ITNs are all pyrethroid based and the overlap between IRS and LLINs/ITNs is believed to be high.

Research and innovation Many insecticides have been studied in Thailand, but the findings have not been published in English. Extensive trials conducted by the ODPC in the north of the country 25 years ago have influenced insecticide choice ever since. Studies were carried-out comparing the residual efficacy of deltamethrin versus lambda-cyhalothrin versus DDT, and deltamethrin was selected as it was efficacious, did not cause skin irritation and unlike DDT was not a persistent environmental pollutant.

At that time, it was policy to test insecticides prior to adoption. More recently the requirement for a trial prior to adoption was dropped and instead insecticides were selected by a vector control sub-committee of the ‘National Committee for Vector Control’. This sub-committee ceased to function in 2013, and plans are now being made to re-establish it. Likely members include the Food and Drug Administration, the Department of Medical Science, the Department of Agriculture, and Mahidol and Kasetsart Universities. For the time being, any procurement of insecticide is based on the decisions made by the previous sub-committee.

Interviewees were unable to cite recent examples of research influencing policy and practice even though the ‘Research Sub-Committee’ of the ‘National Malaria Elimination Task Force’ (chaired by the now retired Deputy Prime Minister) and WHO-South East Asia Regional Office’s (SEARO) ‘Advisory Committee on Research and Development’, both chaired by the Secretary General of the Southeast Asian Ministers of Education Tropical Medicine and Public Health (SEAMEO TROPMED) Network, should be well placed to support this progression.

A trial of insecticide treated clothing for malaria control in rubber plantation workers (with epidemiological, entomological and behavioural components) was started in Thailand three years ago but was never published, as the trial did not involve a control group, and the assessment of incidence pre-, mid- and post-intervention proved inconclusive (Boonsern Aumaung, personal communication).

A broad range of research has been conducted by the programme’s technical partners in recent years, much of it in collaboration with BVBD:


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Malaria Consortium. Recent research led by MC, and conducted in partnership with NMCP, has covered: an ‘Evaluation of Spatial Repellents’, supported by S C Johnson & Son, Inc. in 2014; the ‘Innovative Malaria M&E Research and Surveillance towards Elimination (IMMERSE)’ project, funded by CDC; the ‘Partnership for Containment of Artemisinin Resistance and moving towards the Elimination of Plasmodium in Thailand’ supported by GF; and, ‘Residual Malaria Transmission in the GMS - Studies to examine its magnitude and identify its causes’ funded by WHO’s Tropical disease Research (TDR) fund.

The Armed Forces Research Institute of Medical Sciences. Within the medical entomology unit at AFRIMS there is ongoing work for the development and evaluation of mosquito surveillance traps (including CO2 baited CDC light traps). There is also work on the evaluation of novel control or preventive measures including ivermectin as an endectocide, insecticide barrier treatments, insecticide-impregnated bed nets and tents, and personal-use and spatial repellents. Studies are aimed at understanding basic vector biology and behaviour through vector competence and oviposition assays. Taxonomic keys are continually developed and updated for the mosquitoes of Thailand. Research relating to entomological aspects on malaria biology and transmission includes studies on malaria parasite development in mosquitoes and the establishment of an in vitro system to screen antimalarial compounds and vaccines against sporogonic stages of malaria parasites.

Mahidol University, Faculty of Tropical Medicine, Dept. of Medical Entomology. Key areas of interest for Mahidol are basic and applied research relating to the control of mosquito-borne diseases. A recent vector incrimination study confirmed the major vector status of An. minimus s.l. and An. maculatus s.l. and identified An. annularis s.l. and An. barbirostris s.l. as additional vectors, but findings were based on ELISA alone and there was no use of PCR for confirmation [87].

Mahidol’s Insecticide Research Unit provides biological testing and analysis services for a range of insecticidal products.

Kasetsart University. Kasetsart University’s Department of Medical Entomology works closely with the MoPH and BVBD, conducting joint research covering species diversity, biting activity and host preference of malaria vectors[88–92], vector incrimination using ELISA and PCR in combination[92] ( a recent study revealed a 0.97% (9/926) infectivity rate in An. epiroticus[93]), vector mapping[94], insecticide resistance and control of outdoor transmission. The unit has field sites in Tak province along the Myanmar border, in Mae Sot District and Mae Hong Son where there is a rich diversity of malaria vectors among the three major malaria vector complexes19. The group is currently using experimental hut studies to investigate the excito-repellent effects of various insecticides in local vector species. Studies on outdoor transmission focus on spatial and topical repellents including the development of botanical spatial repellents.

Institut de Recherche pour le Developpement (IRD)/Institute Pasteur. The IRD works closely with Kasetsart University with the ‘The STOP-VEC’ project which conducts basic and applied research to better understand the causes of the emergence and resurgence of vector borne diseases in Thailand in order to improve their control. The programme has developed three research components: biology and ecology of vectors; insecticide resistance and

19 One species within the Minimus complex (An. minimus) along with two related species in the Funestus group, (An. aconitus, An. varuna), two species within the Dirus complex (An. dirus, An. baimaii), and four species within the Maculatus group (An. maculatus, An. sawadwongporni, An. pseudowillmori, and An. dravidicus).


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management; and, innovative vector control strategies. The IRD is currently assessing the efficacy and durability of a polypropylene LLIN (Bayer’s ‘LifeNet’) in comparison to polyethylene (Olyset) and polyester (PermaNet 2.0) LLINs in Kanchanaburi province.

Viet Nam – Country profile The burden of malaria is decreasing rapidly in Viet Nam (figure 21) and the disease is becoming increasingly focal[28]. In 2015, just 211 communes had an Annual Parasite Incidence (API) > 1, compared to 488 in 2011. Malaria deaths have decreased from 20 in 2007[49] to 3 in 2016[58].

Figure 21. Monthly confirmed caseload in Viet Nam since January 2010.

Between August 2016 and July 2017 just six out of 63 provinces/municipalities (Gia Lai, Binh Phuoc, Quang Tri, Dak Nong, Khanh Hoa, Ninh Thuan) together accounted for 66% (1,925/2,903) of total confirmed malaria cases and 81% (1,297/1,601) of confirmed P. falciparum. Binh Phuoc alone accounted for 39% of confirmed P. falciparum. As elsewhere in the GMS, increasingly malaria is becoming an occupational disease predominantly affecting men.

The spread of artemisinin resistance and difficulties addressing forest-based transmission remain serious challenges to the achievement of national elimination goals.

Policy framework for vector control The ‘National strategy for malaria control and elimination in the period 2011-20 and orientation to 2030’ (NSMCE) (Issued with Decision No. 1920/QĐ-TTg by the Prime Minister on 27 October 2011) provides a broad overview of planned programme direction during the current decade. The ‘National Strategy for Malaria Control and Elimination Workplan 2015-2020’ provides a more detailed account of the activities that were planned for implementation during 2015-20, but this is understandably somewhat out of step with the latest guidance on elimination from WHO, which was published in 2017. The activities described in the recent (2017) GFATM funding request deviates somewhat from the 2015-20 workplan in order to follow recent WHO guidance. The 2015-20 workplan is being

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updated for the period 2018-20 to take into consideration the GFATM funding request and reflect the recommendations presented in the 2017 Malaria Programme Review (MPR). All of these documents are in-line with the MoH’s broader 'Plan for People's Health Protection, Care and Promotion in the Period of 2016-2020'.

The goal of the NSMCE is to actively control malaria in moderate and high endemic areas and to eliminate malaria in areas where malaria has been reduced to a low level. Targets for 2020 are: morbidity below 0.15 per 1,000 population; mortality below 0.02 per 100,000 population; and, malaria eliminated in at least 40 provinces. With more than 40 provinces now malaria-free, all of these targets at the impact level have already been achieved.

While strategic documents developed at central level are basically sound, there is often a ‘disconnect’ between what is written at central level and what is actually implemented at the periphery. This needs to be addressed through the development of SOPs, job aids and a programme of supportive supervision that reflect and support national strategy documents.

Structure of vector control programme Specialized malaria control services are responsible for technical guidance, overall planning and procurement relating to malaria control nationwide. The National Institute of Malariology, Parasitology and Entomology (NIMPE) is responsible for the 28 northern provinces and provides oversight nationally. The regional Institute of Malariology, Parasitology and Entomology (IMPE) - Quy Nhon is responsible for malaria control activities in the central provinces and IMPE - Ho Chi Minh City (HCMC) is responsible for malaria control activities in the southern provinces and Lam Dong (a central province)(figure 22).

Figure 22. Overview of Viet Nam health services organizational structure.


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Until recently, the most endemic provinces had a separate Provincial Malaria Centre (PMC). In less endemic provinces the Provincial Centre for Preventive Medicine managed malaria control with a smaller Department for Malaria Control (DMC). MoH is currently in the process of integrating all vertically oriented disease programmes within a ‘Provincial Centre for Disease Control’ (PCDC) in each province20. This process should be complete by the end of 2020.

Each commune has a Commune Health Centre (CHC) and in malaria endemic (or recently malaria endemic) communes these have specially trained staff responsible for malaria control (amongst other duties).

At peripheral level the policy is to have one VHW in each village. These VHWs are members of the community who receive training from the provincial health service, often at the district level, to cope with the most common medical needs of the population of the village. VHWs are the backbone of the community-level health response in Viet Nam. They are not full-time employed government officials but do receive an allowance from the government budget for the times they are engaged in outreach activities, mainly focused on health promotion and prevention, including supporting the delivery of LLINs and IRS. They are

20 MOH Circular No: 26/2017/TT-BYT (Guiding functions, tasks, authorities, and organizational structure of Centers for Disease Control and Prevention of provinces and cities under Central Authority).


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unusual in the GMS in that they are not volunteers and they differ from Cambodia’s ‘Village Malaria Workers’ for example, in that they are relatively extensively trained.

In addition, the NMCP works in close association with two key national community groups, the Women’s Union and the Youth Union.

Capacity (manpower, technical capabilities, training, infrastructure and financial resources) The 2017 MPR[28] found that the programme had good overall management, both at Central level and generally at GFATM supported PHDs, District Health Centres (DHCs) and CHCs. HR capacity is generally strong and the programme is well supported by a committed VHW network. The quality of programme management varies considerably between provinces. The degree of autonomy exercised by provinces over NMCP guidance also varies considerably from one province to another.

The NMCP has the benefit of adequate office, laboratory and storage space at all levels of the health system, and these facilities are generally maintained to a good standard. Computers are up-to-date and there is Wi-Fi Internet access down to CHC level nationwide. There is a shortage of vehicles, but motorcycles can generally be hired as required.

Partners involved in vector control and entomology NIMPE has a number of valuable long-established partnerships with national and international institutes supporting various malaria related operational research projects. In 2015 it developed a new partnership with PSI in order to ensure effective engagement with private sector malaria case management providers - a key component of the national strategy. In 2018, it will form a number of new partnerships with NGOs supporting the implementation of the 2018-20 RAI2E grant.

PSI is involved in targeted marketing of LLHNs and Vector Control and Personal Protection (VCPP) related research on targeting (see below).

The CSO, HPA is supporting malaria control efforts including vector control in some central provinces with support under the Inter-Country Component (ICC) of RAI2E.

Intra-sectoral and intersectoral collaboration NIMPE and both IMPEs collaborate closely with their respective PCDCs/PMCs/DHCs. NIMPE also collaborates closely with the Army Institute for Preventive Medicine. NIMPE, IMPEs, PCDCs/PMCs/DHCs and CHCs also all actively collaborate with the People's Committee, the Women's Union and the Youth Union who support implementation of bednet campaigns and IRS operations and support community mobilization.

All communicable disease programmes are now integrated at DHC and CHC levels and there is some sharing of transportation for monitoring trips etc. at DHC level, however this could be improved.

There is collaboration between the MoH and the MoA, with annual and sometimes quarterly meetings of the 'One Health Project' to review various issues relating to health and agriculture including insecticides.

There is currently no collaboration between the various elements of the NMCP and the Forest Rangers (a critically important risk group) and the level of collaboration with commercial enterprises operating in endemic forest areas is low. Forest Rangers, hydro-electric power companies, and rubber and sugar cane businesses have all been invited by IMPE-QN to join intersectoral meetings on malaria, but none have attended.


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There is also, inter-country collaboration across the GMS and across ASEAN, with Ministerial level agreement on elimination targets. In 2018 APMEN’s Vector Control Working Group will be supporting the development of a ‘Resource Exchange Network’ to improve communication and strengthen collaboration between its members.

Inter country collaboration with immediate neighbours includes cross-border collaboration in the event of outbreaks (including cross-border missions by spray teams in special cases). There is also free access to malaria diagnosis and treatment at health facilities for all border crossers moving in either direction. Control efforts (IRS campaigns) are, however, not synchronized across borders.

Vector control interventions (LLINs, ITNs and LLHNs; IRS; other) Vector control is a major component of the NMCP in terms of financial and human resources as well as in terms of logistics and monitoring. Vector control is based on a combination of ITNs (including LLINs, conventional nets treated annually with insecticide [ITNs], and LLHNs) and IRS. To date, delivery of LLHNs has been managed directly by NIMPE (rather than IMPEs) and only as part of pilot projects investigating utilization. The strategy has now been adopted and larger-scale distribution is foreseen with support under the GFATM’s current RAI2E grant.

Additional personal protection measures, such as repellents and bush clearing around households, are also being used or promoted in some settings. IEC/BCC materials provided by the NMCP and used by healthcare workers and VHWs indicate that these techniques impact on malaria.

Larval source management is not used against malaria vectors in Viet Nam.

Targeting Until recently targeting of LLINs was based on a combined five-zone commune-level stratification21 based on mean API for the most recent four-year period, and three-tier stratification based on drug-resistance profile (figure 23).

Figure 23. Schematic showing recent targeting approach whereby populations were prioritized to receive LLIN according to ‘Tier’ and ‘Zone’.

Tiers are no longer used to differentiate between drug-resistance levels and the NMCP has now adopted a new simpler stratification based on the previous year’s API, which groups communes into three zones as presented in table 3 GFATM support for LLINs during 2018-

21 Zone 1 - Areas without malaria transmission; Zone 2 - Areas with vectors but free from malaria; Zone 3: low malaria

endemic area (incidence of confirmed malaria <1/1,000 population); Zone 4: moderate malaria endemic area (incidence of confirmed malaria 1 - <5/1,000 population); and Zone 5: high malaria endemic area (incidence of confirmed malaria 5+/1,000 population),


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2020 will target the population in zone III (communes with an API>/=1 implementing control measures).

Table 3. Risk stratification for 2018-20 GFATM funding request.

Until recently re-stratification was a laborious task performed every four to five years. As the health information system improves, stratification should become a simple process conducted annually.

Improved methods for targeting forest-goers are under development with the assistance of one of NMCP’s CSO partners. PSI is in the process of mapping rural stores, blacksmiths and motorbike repair shops near forest entry points and border crossings in its five BMGF supported ‘GMS Elimination of Malaria through Surveillance’ (GEMS) programme provinces in order to inform the creation of an LLHN distribution channel for this hard to reach group. Consumption data will be used to inform future quantification of needs.

Quantification of commodity requirements Quantification of all vector control commodity requirements at central level is carried out by NIMPE with the assistance of technical partners, based on the stratification described under ‘Targeting’ above. Population at risk figures are fed into an Microsoft Excel model that takes into account existing LLINs, factoring-in the expected lifespan of the LLINs in question and yearly attrition rates due to wear and tear, and loss. In-line with normative guidance, one double LLIN is calculated for every 1.8 people living in settled communities targeted for mass distribution. The quantification of LLIN requirements has been problematic in recent years. While a ‘bottom-up’ planning approach is recognized at central level as being ideal, the request from central level to provincial level for a bottom-up LLIN gap assessment to inform the development of ~3-yearly GFATM funding requests has consistently been late. As a result, data from the periphery has not been collated systematically and net quantifications presented to GFATM have sometimes lacked accuracy. In some provinces where LLIN requirements have been underestimated, the number of nets requested at each level is adjusted down according to allocation provided by the administrative level above[28]. There has thus been a suboptimal mix of top-down and bottom-up planning for vector control.

The number of forest-goers in Viet Nam is not well understood. So far, the quantification of LLHN (and supplementary single LLIN) requirements has been deliberately conservative (most recently largely to ensure that the funding request to GFATM did not exceed the allocated amount). To date LLHNs have been supplied at a rate of one per household in areas targeted to receive LLINs and as far as stocks have allowed. Under RAI2E, and with the assistance of CSO partners, they will be targeted more specifically on forest-goers.

Only people registered with the People's Committee can be issued LLINs/LLHNs. Migrant workers are required to register with the People's Committee representative at village-level or with the police at commune-level on arrival. However, many do not. A recent study in Binh Phuoc found that commune-level quantification of LLHN requirements for migrants


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was based on registered migrants alone and suggested that only 50% of migrants in the province were registered[95].

The job of quantification of LLIN requirements for mobile workers has been undermined by the fact that big companies involved in construction, forestry etc. operating in endemic areas often underestimate the number of employees they have in order to minimize their tax and social security obligations. With these companies reluctant to deal with government representatives, CSOs may be better placed to more realistically quantify their commodity needs.

During 2018-20 GFATM is expected to procure 1,235,000 LLINs and approximately 84,000 LLHNs (an additional 54,000 LLINs are available for distribution in 2018 from procurement in 2017.). The LLIN quantification fails to consider the continuous channels of distribution described in the funding request. The quantity of LLINs thus appears to be inadequate.

Procurement and supply of vector control commodities All LLINs and LLHNs are procured using GFATM funds through its VPP mechanism. Under RAI2E the programme is procuring high quality LLHNs (hammock with integral net) at a cost of US$14 each, including delivery to end user. Insecticide is procured exclusively with national funds. At present only ‘Icon 2.5CS’ and ‘Icon 10SC’ (the synthetic pyrethroid, lambda-cyhalothrin) are used for IRS and for dipping conventional nets.

Insecticides are selected based on the results of in-country trials. Regulations require that each new prospective insecticide be field tested in-country to assess residual efficacy.

Recent GFATM funded LLIN procurements have been delivered direct to each target province by the supplier based on the Central Project Management Unit’s (CPMU) quantification. The Provincial Project Management Unit (PPMU) takes delivery of the LLINs and signs a receipt for the supplier and sends a copy to the CPMU. The PPMU then works with the district focal points to confirm village allocations in-line with broad guidelines from the CPMU. Village level line-listings are developed by CHC staff in partnership with People’s Committee officials and VHWs. These line listings are signed by each LLIN beneficiary on receipt. The original is kept at District level and a photocopy is sent to province level. The PPMU then compiles a report stating the total number of LLINs delivered and sends it to the CPMU at NIMPE.

Training is provided on the proper management of vector control pesticide stocks at district and commune levels every year prior to interventions. Stock planning is carried out at central and provincial level annually. Records are kept of all transactions and stock inspections are carried out as part of routine annual supervision by upper levels.

There is adequate storage for LLINs/LLHNs and pesticides at NIMPE/IMPEs, as well as at province and generally at district level.

Implementation Mass distribution of LLINs. Until recently, conventional ITNs have been used to a much greater extent in Viet Nam than LLINs. However, since 2009 ITNs have been progressively replaced by LLINs as funds have become available through GFATM funding. Free LLINs are delivered primarily through nationwide three-yearly mass distributions covering the entire population residing in established settlements in target communes in zone 3. The Government of Viet Nam (GoV) continues to support retreatment of conventional nets for those who prefer to use their own nets in zone 3 and in some less-endemic areas not


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targeted with LLINs. In order to maximize impact, dipping is timed to take place just before malaria transmission normally starts to peak. Training on LLIN distribution, ITN treatment and associated communication for behavioural change is conducted at the district level prior to each distribution.

Continuous distributions. For some years there have been plans to top-up LLINs in-between mass distributions and to provide supplementary LLINs or LLHNs to forest-goers through continuous distribution channels. The Concept Note for the 2016-17 GFATM funding application lists eight mechanisms for delivery. However, no evidence of continuous delivery was found during the recent MPR[28]. Continuous channels for top-up of LLINs in target communities are also described in the Funding Request for the current RAI2E grant22 but no LLINs have been allocated for this in the quantification of requirements (see above). Implementation is due to begin in September 2018, but it would seem that this could only happen if LLINs destined for settled communities are reassigned.

The MPR[28] noted over-allocation of LLINs, net retreatment and IRS in some areas, and significant gaps in other areas. In some situations, allocations at commune and village levels seemed to be more for the sake of ‘fairness’ than based on any clear scientific rationale. The team recommended that the targeting of LLINs and ITNs should be tightened-up to focus on achieving total coverage for people in transmission sites.

Indoor residual spraying with insecticide (IRS). IRS has been an important tool for vector control in Viet Nam since the eradication era. Currently IRS is carried out as a routine mass preventive measure in more endemic areas. It would also be used as a focal responsive measure in the event of an outbreak. The NMCP plans to use IRS in response to confirmed transmission foci in elimination settings, but detailed plans have not yet been developed. Training of spray teams is conducted annually at district level.

To be fully effective, IRS must be applied immediately prior to any seasonal increase in transmission, the timing of which varies from one region to another primarily according to latitude. The MPR[28] noted that the criteria for targeting IRS is vague and that the timing of IRS is often sub-optimal, with some communities spayed not because they are at particular risk, but to prevent the expiry of insecticides and thereby avoid the bureaucracy associated with the disposal of expired stock.

Targeted additional personal protection. Repellents have been used on a number of occasions for personal protection for forest-goers in high transmission areas but funding for this is inconsistent.

Community mobilization Information, education and communication activities are implemented (primarily through interpersonal communication by health staff and volunteers) to educate high-risk individuals about malaria prevention and cure, and to mobilize communities to engage in and support malaria elimination efforts.

22 Referring to the supplementary LLINs foreseen in an early version of the quantification model the funding request states: ’Approximately one third of these LLINs will be given as supplementary LLINs for forest-goers during routine mass distribution and for topping-up in established settlements in non-mass distribution years. Another third will be given to employers to give to their workers and to farmers to give to their seasonal workers. The rest will be used for ad hoc mass distribution in new settlement sites and for supplementary LLIN provision in outbreak areas and in transmission foci.’. However, in the final version of the quantification model the supplementary nets are missing, and they were not included in the budget submitted to GFATM.


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Multi-lingual billboards have been produced in some provinces targeting both the majority Kinh population and the main ethnic minority population in the province in question. All VHWs are involved in providing IEC for their communities.

Under RAI2E the NMCP will develop its IEC/BCC plan for control and elimination. It will conduct an in-depth assessment of current IEC/BCC channels and materials and develop a communication and advocacy strategy. IEC/BCC materials will be developed. The programme will broadcast malaria messages through television, radio and newspapers. The programme will also utilize mass SMS via mobile phone networks to broadcast malaria messages to people entering malaria endemic areas to inform them of the risk of malaria and the need for prevention, and to encourage appropriate treatment seeking. More billboards will be placed at strategic sites in highly endemic areas. Communities will be mobilized to support malaria elimination efforts. Provincial and district health staff will receive additional training on malaria IEC and BCC and ways of engaging the community. Provincial and district health staff will in turn train commune health staff and village health workers, who will act as the frontline for community mobilization. Community meetings and village message campaigns will be carried out during mass LLINs distribution. Religious, civil-social, charitable organizations, NGOs and village leaders will be engaged and trained on malaria messaging and health education. RAI2E will also support 'World Malaria Day' events at selected provinces/districts.

The government’s ‘Sedentarization Policy’[96] has resulted in a significant reduction in malaria transmission in Viet Nam by moving people away from forests to large roadside settlements.

Quality control Bioassay-based batch testing is carried out by NIMPE on all imported LLINs, LLHNs and insecticides. Biochemical testing is carried out either at ‘Vinacontrol’23 (a government controlled semi-privatized agency responsible for certification of public health pesticides and application equipment), or at the ‘Viet Nam Certification Centre’24, under the Ministry of Science and Technology.

The quality assurance (QA) of LLINs/ITNs involves direct observations of distribution/dipping campaigns covering site preparation, quantity and condition of equipment and supplies, dipping technique, number of nets dipped, BCC efforts and health and safety (including protection of impregnation teams, management of insecticides, processing of containers and disposal of redundant insecticides). The coverage of IRS within targeted households is determined using WHO cone bioassays in selected sites at some stage during the six months post-spray period (using either wild caught vector mosquitoes or susceptible insectary-reared mosquitoes brought from NIMPE, IMPE or the PHD).

Similarly, QA for IRS involves direct observations of spray campaigns covering site preparation, quantity and condition of equipment and supplies, spray technique, number of structures sprayed, BCC efforts and health and safety (including protection of spray teams, management of insecticides, processing of containers and disposal of redundant insecticides). The residual efficacy of IRS is determined using WHO cone bioassays in selected sites at some stage during the six months post-spray period (using either wild

23 http://www.vinacontrol.com.vn 24 http://www.quacert.gov.vn/en/home.h6.html


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caught vector mosquitoes or susceptible insectary-reared mosquitoes brought from NIMPE, IMPE or the PHD).

In the past, programme efforts have been undermined by the poor quality of LLINs and LLHNs procured. The polyethylene LLINs procured under the RAI grant were too small, with users complaining that they were unable to tuck their nets under their sleeping mats. During a review of implementation quality under the RAI grant the size and/or relative stiffness of polyethylene LLINs were considered by some interviewees to be likely to limit utilization and thereby undermine impact[68]. Some interviewees said that utilization rates with polyethylene nets fall to as low as 30%. Evidence from Viet Nam, however, remains anecdotal. RAI2E is procuring polyester LLINs in 2018.

Hammock nets procured under RAI were poorly designed. The ‘envelope’ of the net was not deep enough for the hammock to hang down into, and the cover flap was unnecessarily long. As a result, they were uncomfortable, and utilization seems likely to have been suboptimal[68].

The formulations of lambda-cyhalothrin used for retreatment of ITNs in Viet Nam has a relatively short residual life. In an effort to address this issue, a study on a long-lasting formulation of deltamethrin was conducted by (N)IMPEs. Results however indicated this was not efficacious (although studies elsewhere had confirmed that this formulation remained efficacious after 30 washes). Other factors, like high price and concerns that the quality of self-dipping might be poor and could result in harm to people or the environment, also influenced the decision by the NMCP not to adopt the ‘long-lasting’ formulation of deltamethrin for ITN re-treatment.

Coverage The number of LLINs distributed, the number of ITNs treated and the number of people protected by IRS are determined annually and details are communicated to WHO for the World Malaria Report. Approximately 617,000, 620,000, 417,000, people were protected with IRS in 2014, 2015 and 2016 respectively. Approximately 841,000, 213,000, 217,000 LLINs were distributed in 2015, 2016 and 2017, giving a modelled coverage of the population at risk in the then target area of 80%, 95% and 100% respectively.

Coverage and utilization rates are assessed periodically by means of household surveys. The last survey was several years ago and so is no longer relevant.

Both pyrethroid-based IRS and pyrethroid-treated nets were delivered to target communities in many areas visited by the MPR teams[28]. This goes against WHO guidance[39]. It is inefficient use of resources and could potentially accelerate the development of insecticide resistance.

Key risk groups Military. The Viet Nam military has good communications and regular contact with civilian institutes (e.g. NIMPE) and other international partners including the US NAMRU-2, and the Australian Army Malaria Institute (AMI). The Army also collaborates informally with WHO through NIMPE.

The Army Medical Department covers all malaria related work for the military in Viet Nam. Soldiers are obliged to use single green conventional nets wherever they are based/deployed. For those deployed in endemic areas these nets are treated twice a year


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by military clinic staff responsible for vector control with either alphacypermethrin or lambda-cyhalothrin, which is supplied by NIMPE.

Soldiers on patrol in the forest are issued with sleeping mats, which they can tuck the sides of their ITNs under. In larger forest camps, bamboo/wooden platforms are erected, and mats and nets are used on top of these. Some soldiers are issued with hammock-nets, but these are not treated. Most sleeping in hammocks use their ITNs, but they cannot close them well.

IRS using alpha-cypermethrin or lambda-cyhalothrin supplied by NIMPE is carried-out routinely in all permanent military camps.

Repellents are not routinely supplied, but their use is recommended in forest hotspots. Occasionally limited supplies are provided, and quite often soldiers buy repellents for themselves to minimize biting. A study on the entomological efficacy of DEET is being planned with NIMPE, AMI and NAMRU-2. An epidemiological study should be considered.

Soldiers are issued with doxycycline for prophylaxis in endemic areas, but the level of adherence to the regimen is thought to be low.

According to protocol, soldiers should be tested for malaria using microscopy before and after deployment to endemic areas, but actually they are only generally tested after deployment as PCD services in camps are sufficient to ensure that all fever cases are quickly tested for malaria. In addition, all soldiers, irrespective of location, are screened annually for malaria and a wide range of other diseases. The Army Chief of Malariology does not have access to data relating to malaria prevalence but estimates it at less than 1% in all units.

There has not been any large-scale deployment of Vietnamese soldiers for peace-keeping missions in endemic areas (or elsewhere) in recent years, however around 75 soldiers will be deployed to South Sudan in 2018 to establish a secondary hospital.

There were 4,548 confirmed cases (2,858 falciparum) reported amongst civilians in 2017. Caseload in the military is confidential, but well-informed sources suggest that there were just over 300 confirmed malaria cases in the Army and border guards together during 2017.

Border Guards. Border guards are based in all endemic border areas. They are based in permanent camps of approximately 100 soldiers. There has been a lot of deforestation and urbanization in recent years, so the camps are no longer surrounded by forest and vector density has fallen to near zero in most. The border guards carry out foot-patrols at night in forested border areas. They do not camp out, but rest briefly in purpose-built huts. Both the camps and the huts receive IRS on a three to six monthly basis depending on endemicity. The insecticides are procured from GoV funds and are supplied officially by NMCP.

Border guards have the same regulations as the army regarding malaria prevention and personal protection, but they are not subjected to screening (either annual or post deployment), but they do have access to PCD provided by the one or two assistant doctors in each camp. Compliance with ITN use is almost universal.

As in the army, border guards are issued with doxycycline for prophylaxis, however, compliance may be low.

Border guard health teams commonly support healthcare for three communes. They are supplied with adequate quantities of government procured antimalarials through NMCP from central level through their own networks. RDTs, which are procured using GFATM


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funds, are supplied to border guards by peripheral health facilities through unofficial channels depending on availability, and stock-outs occur. Microscopy is now used very little. An estimated 60-70% of treated cases are treated based on clinical symptoms alone. The vast majority of these are likely malaria negative.

Border guards used to collaborate with commune officials to facilitate the delivery and distribution of ITNs to inaccessible communities, but this does not happen any longer as accessibility has improved greatly.

In 2015/16, border guards participated in a trial with repellents produced by an army pharmaceutical manufacturer. They felt that the repellents were effective, but funding shortages mean that repellents are not routinely supplied.

An estimated 90% of confirmed cases in the military occur amongst the border guards.

Border guards do not have any relations with counterparts in neighbouring countries, but relations with civilians living close to the border are good and for these groups borders are porous.

Border guards do not have any links with international research groups.

Forest Rangers. Forest rangers are an armed force (armed for self-defence only) under the MoA responsible for protecting forests and wildlife. Their offices are at provincial level, but rangers are based in ranger stations at district level in districts with Forests, National Parks and Nature Reserves. There are normally 20-30 rangers in each station, but they can be moved around within their respective provinces as required. They operate close to, but not in border areas and so their activities do not overlap with those of border guards. The two agencies do hold regular meetings (not health specific) and there is an informal agreement that border guards report forest incursions to forest rangers. They patrol the forest on rotation for 7-10 days at a time.

In 2016, approximately 11% of forest rangers working in Bu Gia Map National Park, Vietnam screened positive for P. falciparum by PCR[97], and appear to be doing nothing for malaria prevention. This suggests that they may be one of the main transmission reservoirs in the area.

More than a decade ago corruption was widespread amongst forest rangers in Viet Nam and many would take bribes to ignore illegal forest activities. Since the government strengthened its anti-corruption measures, the situation has improved markedly, and the Forest Rangers are now a dedicated and conscientious workforce.

Conservation CSOs. There are a number of CSOs involved in conservation in highly endemic forested areas of Viet Nam. Some have been contacted by the NMCP and are well provided for in terms of personal protection. The quasi NGO, the ‘Center for Environmental and Rural Development’ at Vinh University for example has 15 staff working with rural communities in the forest or on the forest fringe and 15 staff involved in deep forest transects, sometimes camping in the forest for long periods. They are supplied with LLINs, LLHNs and standby treatment by the PPMU in Vinh. They are also supplied with repellent by the university on the advice of the PPMU.

In contrast ‘Fauna and Flora International’ (FFI), which has been working in Vietnam for over 20 years has not had any support from the NMCP. It has approximately 100 staff stationed in the North-West and Central Highlands, including in the malaria endemic provinces of


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Nghe An and Kon Tum. Staff spend up to four months a year in the forest, either camping out or staying in forest huts. They do not use any vector control or personal protection and regularly contract malaria.

Data systems For intervention and entomological data (entomological surveys, insecticide resistance assays, ITN bioassays, IRS bioassays etc.), paper records based on standard templates are completed in the field and fed back to NIMPE/IMPEs for entry into Microsoft Excel or Access. Data are stored on computers at central level and backed-up using an external hard-drive. NIMPE/IMPEs do not use cloud storage. Data is reviewed on an ongoing basis by those responsible at each level. Feedback on data to collection teams is provided where appropriate. Any issues are immediately brought to the attention of the programme management team. Findings are also presented at monthly, quarterly and annual review meetings and at NIMPE’s annual conference (to which multiple stakeholders are invited). Data is formally shared with WHO annually for the WMR and on an ad hoc basis including during meetings. There is no immediate linking of entomological and epidemiological surveillance and intervention data as these are in separate systems. Links are however made during analysis by programme managers and external MPR team members.

PCDCs/PMCs/DMCs surveys are carried out periodically to review numbers of staff, their qualifications, any recent training on entomology and vector control, duration of appointment, vector maps, population protected by ITN treatment/IRS, insecticide (type, formulation and quantity), and availability of key tools including bioassay kits and light traps. This information is collected from more endemic provinces on an annual basis and from less endemic provinces every three years. The form is filled by PPMU staff and entered in to Microsoft Access at central level.

Monitoring and evaluation of vector control M&E associated with LLINs and IRS (coverage, quality and utilization) is not systematic. GFATM-supported LLINs are reported separately from GoV supported ITNs and IRS and as a result there is no real clarity on the proportion of the population protected by one or the other, or by both interventions. The only means of quantifying overlap between LLINs and IRS at present is through household surveys. These surveys are conducted in a representative sample of about 10-15 communities nationwide that have been targeted to receive LLINs and ITN treatment. A team of four entomologists from NIMPE carry-out interviews in 60 households at each site. Data are double-entered into an Microsoft Access database and a household index is generated by an automated template. Each team reviews its findings and generates a report with recommendations for follow-up as required at various levels. These surveys are conducted on an ad hoc basis when funds allow. None have been conducted recently.

Vector surveillance NIMPE and IMPEs are well equipped for surveillance and research with top quality equipment. Laboratory space in HCMC is limited, but elsewhere it is more than adequate. NIMPE and IMPE-Quy Nhon both have state-of-the-art molecular biology facilities (ELISA and PCR).

Longitudinal surveys are conducted annually by NIMPE and the two IMPEs in three sentinel sites (one each) representing northern, central and southern provinces where the main vectors are An. dirus, An. minimus and An. epiroticus respectively. The tests are carried out


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on wild caught adult female mosquitoes collected from man-landing, cow-biting and resting collections (those collected from the latter are frequently blood fed). Species identification is based on morphology. Genotyping is only conducted for specific studies. Selected specimens are screened for sporozoites using ELISAs. IMPE-HCMC performed 1,000 sporozoite dissections on An. dirus, An. minimus, and An. epiroticus in 2017. All were negative. The last sporozoite positive An. epiroticus identified by IMPE-HCMC was found in 1986 when the positivity rate was 0.02%. The team are still conducting sporozoite ELISAs in Ca Mau Province in 2018 even though up until May only one malaria case had been detected there. NIMPE restricts its sporozoite rate analysis work to its most endemic provinces, Binh Phuoc and Phu Yen.

Vector control interventions are withheld in all three sentinel sites in order to ensure that there are enough mosquitoes to study. This undermines the role of the sentinel sites as a means of monitoring the development of insecticide resistance.

Responsive entomology, where there is high endemicity and/or an increase in cases, is normally only carried out by provincial level staff as funds at NIMPE/IMPE level are more focused on routine surveillance and specific operational research projects, often funded through research partners.

In provinces where funds permit, entomological investigations are also conducted as part of focus investigations. NIMPE and IMPEs provide entomological support for this where their funds allow. Assessments include the evaluation of the vector bio-landscape, including the rate of open/closed houses as an indication of likely mosquito entry and appropriateness for IRS spraying; and, the number of people who travel into the forest (such as for farming), how often they go, and how long they stay as an indication of the need for additional personal protection measures. The presence of vectors in a suspected focus confirms the need for vector control interventions, and the assessment of housing structure and ITN utilization determines whether vector control efforts should focus on LLINs or IRS. Funds for this are particularly limited in less endemic provinces that are not supported by GFATM.

Insecticide resistance monitoring Susceptibility to DDT and four synthetic pyrethroid insecticides is assessed using standard WHO bioassay tubes. As well as insecticide susceptibility, data collected covers Anopheles species composition, density and distribution and parasite infectivity rates. Supplies for routine surveillance and insecticide resistance monitoring are adequate.

Since 2014, pyrethroid25 susceptibility tests have been conducted using field-collected mosquitoes (F0 unfed adults collected by human landing catch or indoor resting collections in homes or cattle enclosures). Between 2010 and 2017 pyrethroid-resistance (up to 50% mortality) has been detected in the secondary vector An. epiroticus in the Mekong delta (where transmission is now close to zero), and in An. minimus s.l. (up to 21% mortality) in northern Vietnam. Studies in 2003-5 found An. epiroticus was highly pyrethroid-resistant in the Mekong delta, whereas An. minimus s.l. was pyrethroid-resistant in northern Vietnam. An. dirus s.s. showed possible resistance to type II pyrethroids in central Vietnam. An. subpictus was DDT and pyrethroid resistant in the Mekong Delta[98]. An. maculatus, An. sinensis and An. vagus have been shown to be resistant in many areas.

25 Alphacypermethrin, lambda-cyhalothrin, alpha-cypermethrin and deltamethrin.


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A study in 2009 using molecular and biochemical assays to assess the presence of kdr and metabolic resistance did not detect any kdr alleles in any of the vectors studied in Viet Nam (or in Thailand, Lao PDR or Cambodia) but detected an esterase mediated pyrethroid detoxification mechanism in An. epiroticus and An. subpictus from the Mekong delta. The study’s findings also suggested that DDT resistance in An. subpictus from the Mekong delta might be the result of a high glutathione S-transferase activity and that pyrethroid resistance in An. minimus s.l. in northern Viet Nam may be associated with increased detoxification by esterases and P450 monooxygenases [99].

The Army entomological unit conducts its own insecticide resistance monitoring (see below). Some of the more endemic provinces with PMCs also conduct their own entomological surveillance in sites selected based on endemicity, high vector density and accessibility. The quality of this work varies. The data collected is not used at central level.

There is no insecticide resistance management plan at present.

Research and innovation Entomological research focuses on assessments of the ecology of malaria vectors as it relates to human behaviour[100–103], the transmission role of vectors[100,104], and on new vector control tools, technologies and approaches including LLHNs [24,105,106] and topical repellent creams, mosquito coils, repellent candles, and insecticide-treated barrier fencing (all unpublished studies).

NIMPE has colonies of An. dirus (established 2005), An. epiroticus (established 2005), An. minimus (established 1997) as well as Culex quinquefasciatus (resistant strain), Ae. aegypti and Ae. albopictus. IMPE-QN and IMPE-HCMC have insectaries, with strains of An. dirus (from specimens collected in Hainan in China 20 years ago), An. epiroticus and Ae. aegypti.

Experimental huts have been used in the past during collaborative studies both with ITM (Antwerp) and ‘Medisch Comite Nederland-Vietnam’ (MCNV), but these are no longer functioning. Experimental platforms have not been used.

There is some limited collaboration between NIMPE and the two IMPEs. NIMPE and IMPEs share their research findings during regular symposia, but they do not share their data.

There is a good level of collaboration with other research groups including the Hospital for Tropical Diseases (Hanoi and HCMC - Welcome Trust), PSI, MC, NAMRU-2, ITM-Antwerp, Nagasaki University, Fujita University School of Medicine, Juntendo University and UCSF-Global Health Group (GHG), particularly at NIMPE and IMPE-Quy Nhon.

In a large scale cluster RCT by NIMPE/ITM, LLHNs were shown reduce both the incidence and prevalence of malaria especially in more endemic settings[24], despite evidence that LLHN utilization patterns in the study communities were far from ideal[105]. A follow-on study suggested that, at a cost to the NMCP of US$3.40 (netting only) per person covered per year, LLHNs could represent good value for money for malaria prevention in more remote areas[106].

An unpublished study by NIMPE, IMPE and the MCNV demonstrated that properly placed deltamethrin treated netting barriers could significantly reduce biting by An. dirus and An. maculatus by 50-70% (Vu Duc Chinh, personal communication). The researchers however concluded that the netting would need to be protected by a much more sturdy barrier to prevent damage by people or animals, which could make the approach prohibitively


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expensive. Subsequent studies by the same team have focused on the use of ‘ZeroFly’ stitched to tarpaulins to provide protection around resting sites and washing areas in forested transmission hot-spots.

WHO-TDR recently supported the MC and NIMPE to conduct an ‘Investigation of the magnitude and causes of residual malaria parasite transmission in selected settings’. GPS tracking devices were used to monitor the movements of volunteers (including individuals recently diagnosed with malaria) from high-risk mobile groups in order to identify likely transmission spots away from the village [e.g. overnight rest sites/gathering places].

UCSF-GHG is currently collaborating with IMPE-Quy Nhon on an assessment of the efficacy of ivermectin in cattle for the control of zoophilic vectors in community settings.

Entomological findings have influenced policy quite markedly in Vietnam. Examples cited by senior entomologists at NIMPE/IMPEs include:

• Entomological evidence suggests that there is added value of using LLINs and IRS together in more endemic areas (forest farms), and as a result this has been adopted as policy.

• Entomological findings revealed that major vectors are no longer present in many villages[107], so IRS has been reduced in villages in preference to LLINs, as LLINs can be taken to the forest for protection in transmission sites.

• Entomological studies revealed that LLHNs are effective in reducing man-vector contact, so distribution of LLHNs to forest-goers was adopted as policy.

• WHO recommended 200-500 µg of permethrin per square metre for treatment of ITNs. NIMPE research confirmed 200 µg per square metre was adequate for the control of An. dirus and An. minimus and this was adopted as policy.

• Retreating ITNs once a year was found to be as effective as retreating twice per year, so this was adopted as policy.

• A recent assessment of conical LLINs indicate that they are highly effective and popular. They are likely to be adopted as an optional alternative to standard rectangular LLINs for vector control in future if the budget permits (conical nets generally cost a lot more than rectangular ones).

Vector studies are carried out by the Army entomology unit in two sites in each of the Central Highlands provinces every year. NAMRU-2 supports these vector studies, including PCR for identification of sibling species and parasites (no results yet). Findings are published in Viet Nam’s ‘Journal of Military Medicine’26 (and sometimes in international peer reviewed journals) and presented to stakeholders from other sectors during the Army’s annual malaria conference. Findings also influence the province specific IEC provided to soldiers. The Army has an insectary in Hanoi where they rear mosquito larvae collected from the field for insecticide resistance testing. They do not have vector colonies.

26 Abstracts in English.


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Overall findings and recommendations All countries in the region have made remarkable progress in terms of malaria burden reduction over the last decade or so, but all are now faced with ‘the law of diminishing returns’, whereby programme inputs yield progressively diminishing impact. Programmes are now in danger of stalling, and most are unlikely to reach their elimination targets without radical change.

Challenges to malaria elimination in the GMS An overview of the challenges to malaria elimination in the GMS are presented in table 6 by country.

Entomology lacks credibility Entomology has lost credibility by focusing too much on routine surveillance, which generally has not had any influence on policy or practice for decades. There has been a reluctance to move away from the entomological methodologies developed following the end of the global malaria eradication effort. Furthermore, entomological activities often appear to be driven more by budget availability and the desire to maintain the workforce than by programmatic relevance.

Many staff involved in malaria control consider entomology to be no longer programmatically useful. They feel that the fact that there is still no insecticide resistance amongst primary malaria vectors in the GMS means that it is unlikely to develop, and that even if insecticide resistance were to emerge, it may not have any operational significance. Moreover, given the early outdoor biting habits of the region’s primary vectors, many are not convinced that the principal interventions for vector control in the region are effective. There is a feeling amongst some malariologists that entomologists are more interested in saving entomologists, than in eliminating malaria.

Complex and diverse transmission dynamics There is high biodiversity of vector species in the GMS. Numerous Anopheles species and species complexes are present, and these differ in aquatic habitats, geographic distribution and adult resting, feeding and mating behaviours. Altogether these factors result in extreme entomological complexity in the Sub-region [108][109].

In 2013 WHO’s ‘Mekong Malaria Programme’ commissioned a comprehensive review of malaria vectors in the GMS by Hii and Rueda[110]. 150 publications and reports from 2003 were collated for the review. The findings are summarized under ‘Vector landscape’ and ‘Vector bionomics’ below.

The review identified the need to develop a better understanding of the various causal relations and interactions between physiology, environment and vector bionomics in the GMS and highlighted the need for well-designed trials to assess the effectiveness of innovative strategies to address the issue of ‘residual malaria transmission’ (RMT).

Vector landscape Table 4[110] shows a list of Anopheles vector groups in the GMS and summarizes their geographical distribution. This list clearly illustrates the extreme complexity of the entomological situation with regard to malaria transmission in the Sub-region.


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Table 4. Partial list of species and geographical distribution of common Anopheles vector groups in the GMS. From Hii and Rueda (2013)[110].

Subgenus/ Series/ Group

Subgroup Complex Species1 Vector Status

in GMS/ (other)2

GMS distribution Non-GMS distribution

Anopheles/ Myzorhynchus/ Barbirostris

Barbirostris Barbirostris An. barbirostris Van der Wulp s.l.

U Cambodia, China, Laos, Myammar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Pakistan, Sri Lanka

- An. campestris Reid

C (D, F) Cambodia, China, Thailand, Viet Nam

Malaysia

- An. donaldi Reid (D, F) Laos, Thailand Indonesia, Malaysia

- An. hodgkini Reid C Thailand Australia

- An. pollicaris Reid U Thailand Malaysia

Anopheles/ Myzorhynchus/ Hyrcanus

Lesteri Crawfordi An. crawfordi Reid s.l.

U Cambodia, China, Thailand, Viet Nam

India, Indonesia, Malaysia

- An. belenrae Rueda

(D) China North Korea, South Korea, Japan

- An. lesteri Baisas and Hu (= anthropohagus)

(A) China, Viet Nam Guam, Japan, Philippines, South Korea

- An. paraliae Sandosham

U Thailand, Viet Nam Brunei, Malaysia, Singapore

- An. peditaeniatus (Leicester)

(E) Cambodia, China, Myanmar, Thailand, Viet Nam

Afghanistan, Bangladesh, India, Indonesia, Iran, Malaysia, Nepal, Pakistan,

Philippines, Sri Lanka


Nigerrimus - An. nigerrimus Giles s.l.

U Cambodia, China, Myanmar, Thailand, Viet Nam

Bangladesh, Brunei, India, Indonesia, Malaysia, Nepal, Pakistan, Sri Lanka

- An. nitidus Harrison, Scanlon

and Reid

U Cambodia, China, Myanmar, Thailand,

Viet Nam


- An. pursati Laveran

U Cambodia, Thailand, Viet Nam

Malaysia


Sinensis (new subgroup)

Sinensis An. sinensis Wiedemann s.l.

A (A, E) Cambodia, China, Myammar, Thailand, Viet Nam

India, Indonesia, Japan, Malaysia, Nepal, North Korea, Russia, Singapore, South Korea

- An. argyropus (Swellengrebel) s.l.

U Cambodia, China, Laos, Myanmar, Thailand, Viet Nam


An. kweiyangensis Yao and Wu

U China

- An. kunmingensis Dong and Wang

U China

- An. liangshanensis Kang, Tan and Cao

U China

An. nimpe Nguyen, Tran and Harbach

U Viet Nam

An. pullus Yamada F (A, F) China North and South Korea

An. vietnamensis Nguyen, Tran and Nguyen

U Vietnam

Celia/ Neomyzomyia/ Leucosphyrus

Leuco-sphyrus

Leuco-sphyrus

An. introlatus Colless

U Thailand Indonesia, Malaysia

An. latens Sallum and Peyton (= leucophyrus A)

(D, F) Thailand Indonesia, Malaysia

Dirus An. baimai Sallum and Peyton (= dirus D)

A China, Myanmar, Thailand

Bangladesh, India

An. cracens Sallum and Peyton (= dirus B)

D Thailand Indonesia, Malaysia

An. dirus Peyton and Harrison (= dirus A)

A (A) Cambodia, China, Laos, Thailand, Viet Nam

An. nemophilous Peyton (= dirus F)

U Thailand Malaysia

An. scanloni Sallum and Peyton (= dirus C)

U Thailand


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Hackeri - An. hackeri Edwards

U Thailand Malaysia, Philippines

- An. pujutensis Colless

U Thailand Indonesia, Malaysia


Riparis - An. macarthuri Colless

U Thailand Malaysia

Celia/ Neomyzomyia/ Kochi

- - An. kochi Doenitz C (A) Cambodia, China, Laos, Myammar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Malaysia, Nepal, Philippines

Celia/ Neomyzomyia/ Tessellatus

- - An. tessellatus Theobald

B (A, E, F)

Cambodia, China, Laos, Myanmar, Thailand, Viet Nam

Bangladesh Guam, India, Indonesia, Malaysia, Maldives, Nepal, Philippines, Sri Lanka, Taiwan

Celia/ Myzomyia/ Funestus

Un-associated subgroup

Jeyporiensis An. jeyporiensis James s.l.

(D, E) Cambodia, China, Laos, Myanmar, Thailand, Viet Nam

Bangladesh, India, Nepal, Taiwan


Minimus Minimus An. minimus Theobald (= minimus A)

A (A) Cambodia, China, Laos, Myanmar, Thailand,Viet Nam

Bangladesh, India, Indonesia, Japan, Malaysia, Nepal, Pakistan, Sri Lanka, China (Taiwan)

An. harrisoni Harbach and Manguin (= minimus C)

China, Myanmar, Viet Nam

Fluviatilis An. fluviatilis James s.l.

China, Myanmar, Viet Nam

Afghanistan, Bahrain, Bangladesh, India, Iran, Iraq, Kazakhstan, Nepal, Oman, Pakistan, Saudi Arabia, Sri Lanka


Aconitus - An. aconitus Doenitz s.l.

A Thailand Indonesia

- An. pampanai Buttiker and Beales

U Cambodia, Laos, Thailand, Viet Nam

- An. varuna Iyengar

(F) China, Laos, Myammar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Nepal, Sri Lanka


Culicifacies Culicifacies An. culicifacies Giles

(D) Cambodia, China, Laos, Myanmar (Burma), Thailand, Viet Nam

Afghanistan, Bahrain, Bangladesh, Eritrea, Ethiopia, India, Iran, Iraq, Nepal, Oman, Pakistan, Sri Lanka, Yemen

Celia/ Pyretophorus/ Ludlowae

- Sundaicus An. epiroticus Linton and Harbach (= sundaicus A)

B (A) Cambodia, Thailand, Viet Nam

Malaysia, Singapore

An. sundaicus

(Rodenwaldt) s.l.

B (A) China, Myanmar Bangladesh, India, Indonesia

Celia/ Pyretophorus/ Subpictus

- Subpictus An. subpictus Grassi s.l.

(A, E, F) Cambodia, China, Myanmar, Thailand, Viet Nam

Afghanistan, Bangladesh, India, Indonesia, Iran, Malaysia, Maldives, Mariana Islands, Nepal, Pakistan, Papua New Guinea, Philippines, Sri Lanka

- - An. indefinitus (Ludlow)

U Cambodia, China, Laos, Thailand, Viet Nam

Indonesia, Malaysia, Marianas Islands, Nepal, Philippines

- - An. vagus Doenitz C (A, E) Cambodia, China, Laos, Myammar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Malaysia, Mariana Islands, Nepal, Philippines, Sri Lanka

Cellia/ Neocellia/ Annularis

- - An. annularis Van der Wulp

C (A, E, F)

Cambodia, China, Myanmar, Thailand, Viet Nam

India, Indonesia, Malaysia, Philippines

- - An. philippinensis Ludlow

B (A) Cambodia, China, Laos, Myanmar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Laos, Malaysia, Nepal, Philippines

- Nivipes An. nivipes (Theobald) s.l.

C China, Laos, Thailand, Viet Nam

India, Malaysia, Nepal

Cellia/ Neocellia/ Jamesii

- - An. jamesi Theobald s.l.

U Cambodia, China, Laos, Myanmar, Thailand, Viet Nam

Bangladesh, India, Malaysia, Nepal, Sri Lanka

- - An. pseudojamesi Strickland and Choudhury

U China, Myanmar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Nepal

- - An. splendidus Koidzumi

U China, Myanmar, Thailand, Viet Nam

Afghanistan, India, Nepal, Pakistan


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Cellia/ Neocellia/ Maculatus

Maculatus - An. dravidicus Christophers (= maculatus C)

U China, Laos, Myanmar, Thailand

India, Nepal

Maculatus An. maculatus Theobald (= maculatus B)

B (A, F) Cambodia, China, Laos, Myanmar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Malaysia, Nepal, Pakistan, Philippines

An. maculatus Theobald s.l.

U Thailand Malaysia

Cellia/ Neocellia/ Maculatus

Sawad-wongporni

- An. notanandai Rattanarithikul and Green (= maculatus G)

U Laos, Thailand

- An. sawadwongporni Rattanarithikul and Green (= maculatus A)

C China, Laos, Myanmar, Thailand, Viet Nam

Un-associated subgroup

- An. pseudowillmori (Theobald) (= maculatus I)

A China, Laos, Thailand, Viet Nam

India, Nepal

- An. willmori (James) (= maculatus H)

(A) China, Myanmar, Thailand

Bangladesh, India, Nepal, Pakistan

Cellia/ Neocellia/un-associated group

- Karwari An. karwari James s.l.

B (D) Cambodia, China, Laos, Myanmar, Thailand, Viet Nam

Bangladesh, India, Indonesia, Malaysia, Nepal, Philippines, Sri Lanka

- An. stephensi

Liston

(A) China, Myanmar,

Thailand

Afghanistan, Bahrain,

Bangladesh, Egypt, India, Iran, Iraq, Nepal, Oman, Pakistan, Saudi Arabia

1Sensu lato (s.l.) means ‘in the broad sense’, i.e. any or all members of the species complex. 2Vector status for malaria, A-C (A = sporozoites in the salivary glands, B = oocysts, C = ELISA, D = noted as vector, but unspecified sprozoites or oocysts); Japanese encephalites, E; Filariasis, F ; non-vector, U.

Vector mapping. Thailand’s 2015 MPR[81] highlights gaps in vector mapping and makes recommendations for the expansion of vector mapping using networks of villagers trained in ‘cost-effective trapping methods’. However, there is little evidence that detailed vector maps could be used to influence intervention type or targeting, beyond ‘broad brushstrokes’. Some gaps in knowledge are simply unavoidable, and many of these gaps are not critical. Programme planners should be able to rely on less specific ecological indicators to determine interventions of choice (e.g. in coastal areas An. epiroticus may be the main vector and larval source reduction may therefore be an appropriate intervention). Comprehensive national assessments of vector distribution and bionomics are simply not feasible given the complexity of vector behaviour (exacerbated by the extensive presence of sympatric sibling species), manpower shortages and lack of technical capacity. It would be more appropriate to focus on transects looking at vector profiles in relation to topography and land-use (as JICA is doing with VBDC in Myanmar), and then use topography and land-use as a proxy for vector presence and receptivity. A non-entomological alternative would be to simply rely on robust epidemiological surveillance to immediately identify and address transmission foci as and when they emerge . Entomological assistance could be brought in in the event that initial measures fail to address the situation effectively.

Vector bionomics Once again the review by Hii and Rueda[110] demonstrates the extreme complexity of vector bionomics in the Sub-region, and highlights the ambiguities associated with the fact that much of the information gathered to-date has been linked to species complexes as single entities, rather than to their constituent sub-species.

The behaviour of Anopheles species largely determines their vector status, and insights into their behaviour help to evaluate the appropriateness of various vector control


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measures[111]. Anopheles mosquitoes are mainly nocturnal, but precise biting periodicity can vary according to a wide range of extrinsic factors (see below). Some species prefer to feed indoors (endophagic) while others prefer to feed outdoors (exophagic). Some prefer to rest indoors after taking a blood meal (endophilic) while others prefer to rest outdoors (exophilic). Malaria transmission caused by late-biting endophagic vectors can be markedly reduced through the use of ITNs/LLINs or through improved housing construction to prevent mosquito entry (e.g. window screens). Indoor spraying with residual insecticides readily controls endophilic mosquitoes. In contrast, exophagic and exophilic vectors may be best controlled through source reduction (destruction of aquatic habitats) if aquatic habitiats are accessible and limited in size and number – ‘few, fixed and findable’ and easy to identify, map and treat[70].

An. dirus and An. minimus are the main vectors of malaria in the GMS. Both are species complexes made up of several closely related species. An. dirus is generally long-lived, highly anthropophagic and exophagic making it a particularly efficient vector even at low population densities[31]. The open construction of most houses in the forest present little barrier to biting even for exophagic mosquitoes[112]. An. dirus has been by far the most efficient vector of malaria in the GMS; however, with a distribution closely linked to dense forest cover, its relative importance as a vector is diminishing as deforestation continues. Overall, An. minimus has been reported as more zoophilic, exophilic, and exophagic than An. dirus, making it a less efficient vector [29]. However, An. minimus requires less shade than An. dirus and so is less vulnerable to the effects of deforestation. As deforestation continues in the Sub-region the relative importance of An. minimus as a malaria vector can be expected to grow.

An. maculatus (also a species complex) has been implicated as an important secondary vector of malaria in the GMS[31]. It is often present at the margins of hilly forest zones. Studies in the Sub-region have shown that An. maculatus is relatively zoophilic and exophagic when compared with An. dirus and An. minimus, which accounts for its lower vectorial capacity[88].

For all of these species complexes the behaviour and vectorial capacity can vary considerably between and within sibling species. Major differences may also occur from one place to another according to a multifarious range of interactions between host and vector. A recent review of published studies on the biting periodicity of An. dirus failed to classify this species as either a late or an early biter due to the remarkable variation in findings[112]. The phase of the moon, the season and the weather were each identified as key influencing factors. This is likely to hold true for both An. minimus and An. maculatus.

With vector bionomics varying according to this multitude of factors, developing a comprehensive overview of the distribution and role of vectors in the GMS that might be truly useful from a programmatic point of view, would be an impossible task.

Day biting forest vectors. Reports from IPC of 17.4% day-biting in A. dirus during 24-hour static landing catches have very serious implications for the development of effective tools for personal protection from malaria in forest settings. It can be assumed that the proportion of An. dirus bites received during the day would rise much higher than 17.4% amongst those moving from place to place foraging for forest products between dawn and dusk. IPC’s findings are likely to be published in late 2018 (Amelie Vantaux, personal communication). CNM representatives confirmed similar, as yet unpublished, findings. In-


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line with these findings, reports from Lao PDR suggest that a recent outbreak in Nong District in Savannakhet Province, which affected males and females from all age groups, was the result of entire families foraging in the forest during the day time for scarce but high value medicinal leaves to sell to Vietnamese buyers (Bouasy Hongvanthong, personal communication).

Changing ecology of malaria transmission. The ecology of malaria transmission in the region is changing rapidly, with deforestation on the one side and reforestation and development of orchards and plantations on the other. As indicated under ‘Vector bionomics’ above, changing forest cover has a profound influence on the local presence of the major malaria vectors[113]. While shade-loving An. dirus s.l. populations may be drastically reduced, the less efficient sun-loving vector An. maculatus s.l. may increase with deforestation. In the case of An. minimus s.l., for which preferred larval habitats are slow moving streams in the forest fringe, deforestation, reforestation and plantation development can each sometimes result in population decreases or population increases[114]. With the changing ecology, members of the An. maculatus, An. hyrcanus and An. barbirostris species groups are increasingly being implicated as vectors in specific local contexts[57,88,92,93,104].

For a long time the consensus has been that mature rubber plantations, especially those next to the forest, provided a suitable habitat for An. dirus[115]. Unpublished parasite prevalence surveys conducted sporadically over the last 20 years in Cambodia, however, suggest that there is very little transmission in most plantations. Anecdotal evidence from Thailand and Viet Nam indicates that the vast majority of cases amongst plantation workers are contracted in nearby forests where the workers go to collect forest products to supplement their income. There has actually been an increase in the number of cases amongst some rubber plantation workers in recent years, but this has coincided with a global reduction in rubber prices, which has impacted on wages, forcing workers to find additional sources of income – forest products.

Reforestation may become an increasingly important issue for malaria control and elimination in the GMS during the coming years. Within one year of ‘planting out’, teak saplings reach a height of two metres and within a few years of that they provide a dense canopy suitable for forest vectors. The potential role of reforestation should therefore be considered during focus investigations.

Poor public health entomology capacity Quality issues undermining the value of entomological surveillance. The quality of entomological surveillance is very variable across the region. Technical capacity is generally higher at research institutes than within national programmes. Research institutes with multiple international collaborations are generally the strongest. Poor quality entomology (e.g. sporozoite ELISA studies that are not backed-up by confirmatory PCR testing, or incorrectly identified specimens) is not useful and involves a significant waste of time, effort and resources. More emphasis needs to be placed on capacity development. Centres of excellence across the Sub-region need to do more in this regard.

National programmes and partners currently use a variety of keys developed in the Sub-region over the past three or four decades. One commonly in use now is the 2006 illustrated key for the Anopheles of Thailand[116]. Vietnam has another key by Nguyen et al. 2008 and Myanmar often uses a pictorial key developed by JICA 2009. These various keys need to be reviewed, revised and consolidated.


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Uneven coverage and poor quality of vector control interventions Provision of vector control and personal protection services. Providing malaria related services to high-risk static populations is relatively straightforward, at least theoretically. The location of settlements, construction sites and development projects can be mapped, populations can be quantified and plans for delivering interventions can be formulated. Furthermore, post-delivery checks can be made to validate coverage. However, in reality so far it has only generally been the ‘established villages’ that have been well served by routine prevention operations. According to LLIN quantification models all of those in settled communities targeted under RAI2E support either already have access or will have access to LLINs by the end of 2018.

Treating existing conventional nets. Despite mass distributions of free LLINs, recent Malaria Indicator Surveys in the GMS have continued to show very high ownership and use of untreated conventional nets bought from markets. This is clearly a lost opportunity given the higher protective efficacy of treated versus untreated nets (a 2004 Cochrane review showed that ITNs reduced the incidence of uncomplicated malarial episodes in areas of unstable malaria: by 43% compared to untreated nets for P. falciparum, and by 11% compared to untreated nets for P. vivax)[13].

The strong culture of net use in the GMS means that treating existing conventional nets with long-lasting insecticide formulations in preference to distributing LLINs to those who already own and use conventional nets would appear to make sense in many areas. Unfortunately, the two brands of long-lasting insecticide net treatment formerly WHOPES approved are no longer commercially available. Treating existing conventional nets with long-lasting insecticides in preference to distributing LLINs to those who already own conventional nets could reduce costs significantly and improve utilization of ITNs, making this a much more cost-effective approach. LLINs would still be required for those without privately owned conventional nets.

Services for forest goers. The challenges to service delivery among mobile populations are more complex. Mapping is often not possible, there may not be any actual houses or other structures in which to suspend an LLIN, the population size may vary from day to day making quantification of needs difficult, and in the case of illegal migrants and individuals involved in illegal activities, fear of punishment often prevents attempts to access malaria services from official groups or groups that are perceived to be official. Added to this, many people in these groups are driven only by the need to make money, and so getting accurate information for health action from them is a sensitive and complex multi-sector task[1].

While some forest-goers in the formal sector, such as the army and police, may receive some level of protection in the form of ITNs and early access to treatment, other formal sector forest-goers, such as border guards, forest rangers and CSO staff involved in forest and wildlife protection services, as well as informal forest workers, are commonly completely unprotected.

‘Mobile and migrant populations’. As highlighted in the 2015 RAI review[119], the term ‘mobile and migrant populations’ (typically abbreviated to MMPs) unhelpfully lumps together disparate groups of people.

Recent Malaria Indicator Surveys in the GMS have continued to show that coverage of mobile individuals and mobile groups spending time in forest transmission hot-spots remains poor in many areas. There are many operational challenges in defining and


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mapping high-risk mobile people and migrant populations due to lack of established methodologies, their high mobility, differences in each of the countries, and seasonal and year-to-year dynamics. Similarly, there are operational challenges in reaching and providing services to them. Although a significant portion of the commodities funded under RAI and RAI2E (particularly LLHNs) are destined for distribution to these populations, channels for distribution and strategies for targeting these populations are still not well established in many areas.

Development projects. Recent rapid growth in the hydroelectric, mining and plantation sectors and road construction associated with the development of new economic corridors are all resulting in increased population movements locally in the Sub-region. In some cases population movements have occurred as a result of forced resettlement[120]. Economic migration is also placing people, who often have no immunity, in malaria endemic areas with poor health service coverage[120].

Conflict and civil unrest. Persisting civil unrest in southern Thailand and the eastern and northern states in Myanmar and the recent Thai-Cambodia border conflict have all contributed to internal and cross-border population displacements and have hampered the provision of health services in affected areas. Although the GFATM supported CSO HPA is working in conflict areas in northern Myanmar, it is not in a position to supply LLINs or provide other malaria related services to rebel fighters and as a result, the conflict there is exacerbating the malaria situation.

Hammock-nets. LLHNs have proved popular in some groups such as forest-goers for whom bednets are unsuitable. However, their popularity appears to vary from country to country without obvious reason. Research is needed to see if the geographical coverage of this intervention could be expanded (it should be noted that no LLHNs have yet been prequalified by WHO).

Poor quality LLINs/LLHNs. During a recent review of the RAI grant in Viet Nam, the size and/or relative stiffness of polyethylene LLINs were raised at all levels - from CCM to village malaria post - as issues that can limit LLIN effectiveness[68]. Both the polyester and the polyethylene LLINs procured under RAI in Viet Nam (and presumably elsewhere as LLINs were procured through VPP) were too small, with users complaining that they were unable to tuck their nets under their sleeping mats. For many years there has been contention over people’s preference for polyester rather than polyethylene nets, with some officials believing that utilization rates with polyethylene nets fall to as low as 30%[68].

A recent review of literature and data from Sub-Saharan Africa indicated that preferences for certain net attributes exist, but do not impede high rates of net use[121]. However, in the GMS there is a very strong culture of net use27 and so the situation may be quite different. A qualitative non-observational study by PSI/PSK in Cambodia in 2016 to determine net usage determinants and user preferences identified wide-spread antipathy for distributed LLINs resulting from their small interior size, low height and, in some cases, polyethylene material[53]. In 2018 PSI/PSK will conduct a quantitative follow-on study funded by RAI2E to assess the relationship between LLIN material and LLIN usage. The protocol is under development and not yet available for review. There are concerns among some regional experts that the details included in the call for ‘Expressions of Interest’ issued

27 The 2015 Myanmar Malaria Indicator Surveys revealed 99.6% of households with a net of any type, 88% with sufficient nets of any type but only 19% with an ITN and 11% with sufficient ITNs.


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by the RAI2E Regional Steering Committee did not allow sufficient time or budget for a definitive observational cross-over study.

The hammock nets procured under the last RAI grant were also perceived to be inappropriate. The ‘envelope’ of the nets was not deep enough for the hammock to hang down into, and the cover flap was unnecessarily long. As a result, they were uncomfortable, and utilization seems likely to be low.

Targeting of vector control operations. There is little doubt that the current core vector control interventions have contributed significantly to the recent decrease in malaria across the GMS, and universal coverage with LLINs or IRS remains a priority in communities situated in or close to the forest which are endemic, or where receptivity and vulnerability are high. But there are now many non-endemic communities in the GMS that are neither receptive nor vulnerable where universal coverage is being maintained at unnecessary expense. A recent RAI grant review identified excessive use of LLINs in some of the sites visited in both Myanmar and Viet Nam, with programmes targeting some urban areas as well as some rural areas that had not seen transmission for many years. Targeting thresholds for mass distribution of LLIN vary across the region (table 5).

Given the recent rapid reduction in malaria burden in many areas, the current API-based stratification approach adopted by Myanmar, which is based on incidence data from the previous 3 years, may be overestimating the level of risk and resulting in unnecessary provision of LLINs[28].

A suboptimal mix of top-down and bottom-up planning for the various vector control interventions is the norm across the region at present. Planning at central level is commonly a rushed affair associated with funding application development. Models quantifying commodity requirements are often based on best guestimates (particularly in the case of mobile populations) rather than on robust data from the field. The unit cost per LLHN is relatively high compared with LLINs and so the quantification of LLHNs has been tempered by the desire to keep budgets within the country-specific funding envelopes set by GFATM. The resulting numbers seem to be serious underestimates in some countries.

The common practice across the GMS of providing one supplementary LLIN or LLHN per household for forest-goers is an extremely ineffective way of targeting this high-risk group. Workers and volunteers in the periphery generally have a good understanding of the numbers and activities of mobile people in endemic areas nearby. Staff at Central level need to start their planning exercises early in order to allow workers and volunteers in the periphery to guide the quantification of commodity requirements more accurately.

In Viet Nam LLINs/LLHNs are only distributed to named individuals authorized by Commune People’s Committees. This effectively excludes people who have not registered with the People’s Committee.

Overlap of LLIN and IRS. All countries in the region are using IRS with synthetic pyrethroids in at least some communities already provided with LLINs, despite WHO recommendations that communities should not be targeted with both pyrethroid-based interventions.

Cross-border projects. The ICC of RAI2E is currently supporting cross-border projects (including support for VCPP) focusing on narrow strips of land along borders. The approach so far has been problematic and has placed additional workload on peripheral health staff[28]. The recent MPR in Viet Nam found the targeting to be inefficient and


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recommended an alternative approach proposed by the CSO ‘Consortium HA’ based on eliminating malaria in each of the ‘forest islands’ where transmission persists (which may or may not cross provincial and international borders).

Table 5. Stratification of risk and targeting of LLINs and LLHNs across the GMS.

Cambodia Lao PDR Myanmar Thailand Viet Nam

Unit village Health Facility Coverage Area

Sub-centre Village Commune

Data source for risk stratification.

Incidence data for 2014.

Incidence data for last 18 months.

Incidence data for last 3 years.

Incidence data for last 3 years.

Incidence data for last year.

Threshold for LLIN targeting.

API>5 Nationwide: API>10.

5 most endemic provinces: ‘At least 1 malaria case potentially contracted locally’.

API>5 Any locally acquired case detected.

API>1

Standard modelling appproach1.

Yes Yes Yes Yes Yes

Corroboration with peripheral health workers/volunteers.

Yes Yes Not in conflict areas

No No

Pre-distribution enumeration for village level microplanning.

Yes Yes, but weak Yes Yes Yes

Supplementary LLINs for top-up and for other risk populations.

Yes Yes Yes Yes No2

LLIN's for unregistered people.

No Yes Yes (not for non-govt combatants)

Yes (not for non-govt combatants)

No

ITNs. No No Yes Yes Yes

LLHN. 1 LLHN for each household in LLIN target villages.

1 LLHN per person for 2% of the LLIN target pop.

None 1 LLHN per person for 1% of the LLIN target pop.

1 LLHN per person for 6% of the LLIN target pop.

1Modelling at central level based on population extrapolated from census. 1.8. people per LLIN. Existing LLINs, expected lifespan of LLINs and yearly attrition rates all considered

2LLIN quantification fails to consider continuous channels of distribution described in GFATM funding request.


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Weak surveillance and M&E In many countries entomological efforts need more technical direction to be worthwhile from a programmatic perspective. Given the limited resources available in the Sub-region, the emphasis should be on problem solving through ‘spot checks’ and ‘focus investigations’ rather than ‘routine sentinel surveys’ (box 2).

Targeting of focus investigations. Across the GMS, focus investigations (which in theory at least include an entomological component) are almost invariably conducted in the village where the case originated from, rather than at the site where the case most likely became infected, which in the vast majority of instances would be in forests or forest farms. Focus investigation teams are reluctant to travel to these sites as they are usually hard to access and the associated allowances provided are small. This failure of investigation teams to reach transmission sites is illustrated by data from active case investigations in Chanthaburi in Thailand, where the ‘1:3:7’ approach to case-based reporting and follow-up appears to be going particularly well (reporting rate 92%, case investigation rate within 3 days ~99% and focus investigation rate within seven days 98% in 2018). In this province, 9,591 people were screened in suspected foci during 2017-18, but not a single secondary case was found. This clearly demonstrates that the focus investigations were being carried-out in the wrong place.

Weaknesses undermining programme management and implementation Programme guidance by technical partners. Guidance provided to countries by technical partners sometimes needs to be more explicit, more practical and more locally appropriate, taking human and financial resource constraints into consideration.

Management capacity. Quality of programme implementation often varies considerably between different administrative areas depending on management capacity. In some countries CSOs are already mandated to strengthen capacity while managing implementation in different geographical locations, but often they are short-staffed and struggle to implement planned activities.

Box 2. Spot checks and focus investigations[1]

Spot checks: Ad-hoc assessments are carried out in selected locations as a supplement to routine observations and when more information is required to inform programme adjustment or response. Spot checks may include investigations in areas where there are suspected problems in the quality of implementation of an intervention; an expected increase in receptivity and/or vulnerability, perhaps due to reintroduction or proliferation of a vector species as a result of environmental changes; the presence of vulnerable populations due, e.g. to resettlement, migration or mining; and heightened risks for importation due to increased human movement in border areas or transport routes linked to endemic countries.

Focus investigations: These investigations are undertaken in areas of new, persistent or resurgent malaria transmission to determine why the interventions being used are no longer reducing transmission. They are short-term, reactive epidemiological investigations in settings of elimination or prevention of re-establishment. The trigger for a focus investigation could be an increase in the prevalence of parasite infections or clinical malaria cases.


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Administrative issues. In some GFATM supported countries the administrative procedures associated with authorizing a ‘mission order’ mean that it will not be possible to adhere to the ‘1-3-7’ timeline for case investigation, focus investigation and focus response adopted by NMCPs. This means that a timely vector control response may not always be possible.

Intersectoral collaboration. Despite recent efforts, in many places the level of collaboration between NMCPs and commercial enterprises operating in endemic forest areas is low. Businesses across the Sub-region have been invited to join intersectoral meetings on malaria, but attendance has been poor. It seems likely that there is simply not enough malaria and therefore not enough financial incentive for businesses in the GMS to engage in malaria control efforts.

Incentives for arduous field work. The economic realities for staff on the ground need to be realistically considered in light of low public sector salaries, especially for non-clinical staff who may be unable to develop supplementary sources of income[122]. Incentives, whether financial or non-financial, have produced results in many countries[123,124]. Incentives need to be realistic and tailored to the nature of the work involved. At present, attendance at meetings at Central level is incentivised through the provision of adequate allowances, but arduous missions to the forest to conduct focus investigations for example are not. As a result, managerial staff in the periphery are drawn away from their frontline duties and workers and volunteers in the periphery are reluctant to do the extra work needed to achieve elimination. In some places inadequate reimbursement of costs is leading to poor staff morale and low staff productivity.

More equitable funding across the region. There appears to be substantial inconsistencies in the level of funding for malaria control across the GMS under RAI2E. VBDC in Myanmar for example has just one vehicle for the entire national programme and entomologists are forced to use public transport to get to their field sites.

Extensive knowledge gaps While there has been some progress towards developing the evidence-base for some potential new tools, many gaps in our knowledge remain. The really critical gaps in the areas of entomology and vector control relate to RMT (which is now defined as ‘Persistence of malaria transmission following the implementation in time and space of a widely effective antimalaria programme’28).

There may be opportunities to accelerate the elimination of RMT if implementers can quickly develop an in-depth understanding of the micro-epidemiology of the disease in persistent transmission foci. This means identifying the likely site of transmission, identifying the vectors, investigating their bionomics and understanding the human behaviour affecting person-vector contact at the transmission site.

Despite recent efforts including the publication of WHO guidance on RMT[125], and RMT related research funding from the BMGF (Grand Challenges) and WHO-TDR, the evidence-base for informed deployment of improved or novel tools, technologies and approaches or combined usage with existing interventions, remains limited. There is heavy reliance on small-scale studies or theoretical analyses with mathematical models.

28 Note: The sources of and risks for “residual transmission” may vary by location, time and the existing components of the current “effective antimalarial programme”.


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The WHO guidance note on RMT [125] proposed a number of approaches to accelerate the availability and uptake of new tools:

‘The development, optimization, validation and evidence-based deployment of vector control tools to address residual transmission will require the concerted effort of NMCPs and their partners, including industry, research and academia, and WHO. Whilst new tools are under development and in the process of validation, NMCPs should ensure that the core interventions are implemented optimally’.

Some progress has been made. APMEN has established the 'Mekong Outdoor Malaria Transmission Network' to collectively explore the challenges of addressing this issue. Collaborations between academic institutions and industry have generated useful local evidence on the magnitude of the RMT problem, and information on human and vector behaviour, and intervention effectiveness. However, only a small proportion of this research has focused on developing a clear understanding of human behaviour relating to the time and place of exposure to mosquito bites, and this is key. Much more needs to be done in this regard.

Unfortunately, for security reasons there is a widespread reluctance on the part of the militaries to share data relating to malaria amongst their personnel. Such data could help to elucidate the epidemiology of forest-based transmission and help to develop strategies for the control of RMT.

Effectiveness and cost-effectiveness of vector control strategies to guide policy. There is a gap in evidence on the effectiveness and cost-effectiveness of key interventions in the GMS, including ITNs/LLINs and IRS. A study on the impact and cost-effectiveness of combining LLINs with IRS in the GMS is also overdue. Findings would vary according to endemicity, vector behaviour, insecticide susceptibility and product used and so, in addition to collecting field data, mathematical modelling would need to be a key component of any comprehensive study. However, large-scale malaria intervention studies tend to be problematic in most parts of the GMS due to falling incidence and the focal, seasonal and sporadic nature of the disease in many places. Sample sizes required to generate statistically significant results in community-based studies would generally need to be unfeasibly large.

There is also a lack of evidence to guide the development of locally appropriate methods of applying residual insecticides. It has been suggested by experts that spraying in the GMS should not just target indoor surfaces but also the outer walls of houses and animal sheds29 in order to take into account the resting behaviour of local vectors before and after feeding[111], but no research has been conducted yet to validate this approach.

Few supplementary vector control options There is a critical need to develop new vector control and personal protection methods to address outdoor transmission[126] especially in the GMS where it now accounts for the vast majority of cases and threatens to stall programmatic progress towards elimination targets.

While progress has been made in developing the evidence-base for some potential new tools, e.g. with repellents, insecticide treated blankets and clothing, and ivermectin, this

29 An environmental impact assessment may be required prior to any large-scale implementation of applying residual insecticides to the outer walls of houses and animal sheds.


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progress has generally stopped short of large-scale implementation studies and hence has limited potential to effect policy change.

The steps, procedures and evidence required to validate new forms of vector control tools, technologies and approaches and to introduce them to market are outlined in WHO’s ‘The evaluation process for vector control products’[127]. Unfortunately, national regulatory systems tend to be cumbersome and hinder the timely deployment of new tools. One researcher complained:

‘The default setting of the Review Board is to block applications, irrespective of what has already been approved in previous applications.’

APLMA’s Access Team and its regulatory partners and the Innovative Vector Control Consortium (IVCC) are currently working to identify and develop options to improve rapid access to new and current quality-assured commodities for vector control and personal protection. These efforts should help to speed programmatic progress and at the same time contribute to the global evidence base for the elimination of RMT.

The problem of getting a VCPP product into use often does not end as soon as that product has been prequalified. Some countries will not simply adopt WHO prequalified products, but instead insist on a completely separate evaluation, in some cases including national trials.

Relevance of research and influence on policy and practice. There is currently a big gap between researchers and implementers. Scientific publications on vector bionomics often conclude that findings should serve to improve programmatic targeting, but it seems that this is seldom the case. Programme staff need to read and understand relevant published literature. With a large volume of information released regularly, most do not have time, and some may struggle with the highly technical language that is often used by researchers. Furthermore, many publications are not relevant to informing programmatic decision-making. Linkage mechanisms between research institutes and programmes are often weak.

Some interviewees felt that there is a lack of real interest in capacity development amongst some international research partners:

‘These partners recruit the best staff from the public sector and build their capacity, but the staff never return’;

‘They have zero interest in capacity development or malaria elimination… It’s only about the number of publications‘.

Some interviewees felt that research themes are too often imposed by funding agencies and not well aligned with NMCP priorities.

‘…high quality, high cost research but largely academic and unlikely to influence policy, while forest malaria goes largely unaddressed’;

‘…international research partners inject money and some training but divert attention from the basic work that needs to be done’.

The MALVEC Asia project was cited as an example of this. The MALVEC project, which is funded through the French ‘Initiative 5%’, ends in 2018. A new call for research applications is expected in 2018. One interviewee felt that the malaria elimination community should lobby for the ‘new call’ to focus on clarifying our understanding of the microepidemiology of malaria in forests and developing new tools for the protection of forest-goers.


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Similarly, some interviewees felt that the scope of the RAI2E research funding is too broad and that RMT should be prioritized.

The ‘Cambodia Research Consortium’ was established in 2014 to expedite research for malaria elimination as part of the emergency response to artemisinin resistance[1], and, although it is not fully functional at present, it appears to offer a good model for streamlining research efforts in other countries in the GMS and across the region. However, success would likely depend on finding the right character to drive the process. SEAMO TROPMED might be best placed to take on this role at the regional level.

WHO’s prequalification requirements. WHO’s requirement for gold standard RCTs as part of the validation process are considered by some to be unduly demanding in the context of elimination in the GMS, where sample sizes often need to be unfeasibly large to demonstrate impact. As one senior entomologist said:

Don’t let the perfect be the enemy of the good. We know the treated blanket, the shelter or the topical repellent will not, on its own, be the answer. But allow us to procure product, deploy it, measure as best we can, tweak the ‘Target Product Profile’ and see, if in combination with other measures, it can help. Now, without the pre-qual recommendation, UN and US funded procurements cannot procure these items. (Michael Macdonald, personal communication).

Table 6. An overview of the challenges to malaria elimination in the GMS by country.


Transmission dynamics Complex Complex Complex Complex Complex

Public health entomology capacity

Within national programmes Intermediate Weak Weak Strong Strong

Within instiutes/universities Strong Strong Intermediate Strong Not applicable

Entomology/vector control in-country TA Strong Strong Weak Weak Weak

Coverage of vector control interventions

Settled populations High High High High High

Formal sector forest goers

Security forces Variable Variable Variable No information High

Forest protection services Variable Very low Very low No information Variable

Informal sector forest goers Very low Very low Very low Very low Very low

Quality of vector control interventions Variable Variable Variable Variable Variable

Surveillance and M&E

Emphasis of surveillance Sentinel sites Sentinel sites Sentinel sites Sentinel sites Sentinel sites

Targeting of focus investigations Weak Weak Weak Weak Weak

Evaluation of implementing partners Weak Weak Weak Weak Weak

Programme management

Guidance documents Generally strong Improving Variable Variable Variable

Incentives Weak Weak Weak Weak Weak

Reimbursement Weak Adequate Adequate Adequate Adequate

Funding challenges Significant Very significant Very significant Significant Significant

Knowledge gaps Significant Significant Significant Significant Significant

Few supplementary vector control measures Critical issue Critical issue Critical issue Critical issue Critical issue

NMCP entomology/vector control 'overall strength' Weak Weak Weak Intermediate Strong

NMCP entomology/vector control 'trajectory' Improving Steady Steady Deteriorating Steady

Table 7. Recent studies and implementation of promising supplementary malaria vector control tools by country.

Promising supplementary malaria vector

control tools


Insecticide treated blankets No No 2006 feasibility study showed all forest goers

took a traditional blanket and man-landing rates

on people with treated blankets were ~80% lower

than on people with untreated blankets.

(Masatoshi Nakamura, personal communication).

No No

Insecticide treated clothing An unpublished 2017 RCT amongst soldiers in

Cambodia demonstrated permethrin treated

uniforms had a 56% protective efficacy (Colin

Ohrt, personal communication).

No 2017 study demonstrated that insecticide treated

clothing for personal protection was well

accepted by migrant rubber tappers [Malar J.

2017;16:92.].

No No

Topical repellents for settled communities 2016 study showed that picaridin failed to control

malaria in settled communities with high LLIN

coverage[Lancet Infect Dis. 2016;16:1169–77. ]

2013 study showed DEET failed to control malaria

in settled communities with high LLIN coverage

[PLoS ONE. 2013;8:e70664. ].

No No No

Topical repellents for forest goers Topical repellent provided to forest goers in

GFATM supported forest kits.Topical repellent

sometimes provided to soldiers.

Topical repellent provided to forest goers in

GFATM supported forest kits. Repellent soap


Topical repellent provided to forest goers in PMI

supported forest kits in URC areas. Topical

repellent sometimes provided to soldiers.

GoT procured topical repellents are distributed to

migrants and soldiers spending time in the forest.

Topical repellent sometimes provided to soldiers.

Repellents have been provided on occasions for

forest-goers in high transmission areas when

domestic funds allowed. Topical repellent


Larval source management Researchers from the University of South Florida

are currently using drone technology to search for

the ‘spectral signatures’ of malaria vectors’ larval

habitats

No LSM being considered for focal response in

future.

LSM not recommended by BVBD but some

VBDCs do practice LSM using larvivarous fish.

No

Ivermectin as a prophylactic/endectocide

for forest goers

No No No Mahidol/AFRIMS planning RCT with ivermectin

MDA in rubber plantations in 2018.

No

Restricting forest access Restrictions associated with forest reserves. Restrictions associated with forest reserves. Restrictions associated with forest reserves. Restrictions associated with forest reserves. Restrictions associated with forest reserves. The

government’s ‘Sedentarization Policy’ has

resulted in a significant reduction in malaria

transmission by moving people away from forests

to large roadside settlements.

Treating livestock with

insecticide/endectocide

No No No No 2018 assessment of the efficacy of ivermectin

treated cattle for control of zoophilic vectors in

community settings.

Spatial repellents 2016, Mondolkiri Province metofluthrin

emanators reduced landing rates of outdoor

biting secondary vectors of malaria but had no

observable effect on malaria prevalence,

however, malaria transmission levels were low

No No 2018 Kasetsart University, MC and AFRIMS all

conducting studies on spatiial repellents.

No

Push-pull systems’ No No No 2018 AFRIMS conducting study on push-pull

systems.

No

Attractive toxic sugar baits No No No 2017 AFRIMS conducted study on ATSB. No

Barrier systems No No No No 2010 unpublished NIMPE/IMPE/MCNV study

demonstrated properly placed deltamethrin

treated netting barriers could reduce biting by An.

dirus and An. maculatus by 50-70%[Vu Duc Chinh,

personal communication].

Improved housing/screening No No No No No

Promising supplementary malaria vector control tools A recent systematic review of the availability and quality of evidence for 21 supplementary malaria vector control tools (excluding ITNs and IRS) found considerable variability in the volume and quality of evidence[128]. The quality of evidence was greatest for LSM and topical repellents. LSM appeared likely to provide effective protection against malaria at the population-level while topical repellents generally did not. The reviewers concluded that strengthening operational capacity and research to implement underutilized vector control tools, such as LSM and mosquito-proofed housing, using an adaptive, learning-by-doing approach, while expanding the evidence base for promising supplementary vector control tools that are locally tailored, should be considered central to global malaria elimination efforts.

Insecticide treated blankets/sheets. A randomized controlled trial amongst Afghan refugee communities in Pakistan demonstrated that permethrin-treated chaddars and top-sheets reduced the odds of having a falciparum or vivax malaria episode by 64% in children aged 0-10 years and by 38% in refugees aged <20 years (incidence in refugees over 20 years old was not significantly reduced)[129]. A parallel entomological study simulating real-life conditions indicated that host-seeking mosquitoes were up to 70% less successful at feeding on men sleeping under treated chaddars and some were killed by the insecticide. An experimental hut study in Tanzania demonstrated the potential of long-lasting insecticidal blankets (LLIBs) to provide substantial personal protection against mosquitoes[130]. A feasibility study on insecticide treated blankets for malaria prevention in Myanmar was conducted by VBDC in 2006 with technical and financial support from JICA (Masatoshi Nakamura, personal communication). The assessment revealed that, except for Tangya people, most forest workers did not take mosquito nets with them when they went to the forest30, but that everybody took a traditional blanket. Man-landing rates on people with treated blankets were approximately 80% lower than on people with untreated blankets. A randomized controlled trial of treated blankets for malaria control amongst forest-goers in Myanmar should be considered. The approach might be similarly useful in Cambodia where traditional scarves (‘kramas’) are widely used as bed-sheets at night. Apparently, blankets are rarely used in Thailand (Boonsern Aumaung, personal communication) and so this intervention may not be locally appropriate across the entire GMS. Where blankets are used, however, the LLIB intervention would have the major advantage of not requiring any behaviour change, and where still present, the existing ITN retreatment channels could be used for implementation.

MC won a BMGF grant to investigate the use of permethrin-treated kramas among mobile populations in Western Cambodia in 2010, but unfortunately the study was never implemented due to issues relating to ethical clearance.

Insecticide treated clothing. Insecticide-treated clothing has been used for many years by the military and in recreational activities as personal protection against bites from a variety of arthropods including mosquitoes. Permethrin is the most commonly used active ingredient, but others, including bifenthrin, deltamethrin, cyfluthrin, DEET, Icaridin, IR3535 and KBR3023, have also been trialled[131,132]. Microencapsulation technologies prolong the activity of insecticides

30 This study was conducted before high levels of ITN coverage were achieved in Myanmar.


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on clothing helping to overcome the reduction in efficacy over time that occurs as a result of washing, ultraviolet light exposure, and the normal wear and tear of the fabric. These ‘controlled release systems’ also decrease permeation and consequently, systemic toxicity[132]. A 2014 review of the evidence base for the use of insecticide-treated clothing revealed that although some studies have demonstrated protection against the transmission of pathogens, there were surprisingly few, and the level of protection provided varied according to the type of study conducted (from 0-75% in the case of malaria)[131]. Overall, there was substantial evidence that insecticide-treated clothing can provide protection against mosquito bites, and this bite protection evidence suggested that insecticide-treated clothing could be useful in the prevention of malaria transmission. The review concluded that further investigations were needed to accurately demonstrate transmission reduction.

A 2018 Cochrane review of trials conducted in refugee camps in Pakistan and amongst military based in the Colombian Amazon concluded that, in the absence of ITNs, insecticide-treated clothing may reduce risk of clinical malaria caused by P. falciparum infection by approximately 50%[133].

A study in French Guiana published in 2017 demonstrated that long-lasting polymer-coated permethrin-impregnated clothing (PTBDU) provided a good level of protection against malaria in hyperendemic foci[134]. 25 personnel wearing PTBDUs and exposed for 9.5 person-months contracted no cases of malaria, whereas 125 persons wearing untreated uniforms, exposed for 30.5 person-months, contracted 11 cases of malaria, indicating that PTBDU use significantly (p=0.0139) protected against malaria infection. The PTBDUs also showed good residual efficacy despite washing.

A study in Myanmar in 2017 demonstrated that insecticide treated clothing for personal protection was well accepted by migrant rubber tappers [77]. An unpublished RCT amongst soldiers in Cambodia demonstrated permethrin treated uniforms had a 56% protective efficacy (Colin Ohrt, personal communication). A large-scale intervention study of the protective efficacy of PTBDUs in the GMS is therefore now warranted.

1990’s-type US Army uniforms are available for purchase on the market in Cambodia for $15 and the cost for retreatment with the US Army insecticide kit equivalent should be <$1 every 3-6 months (Colin Ohrt, personal communication). AFRIMS and the Armed Forces Pest Management Board’s “Deployed War Fighter Protection Program” can provide the latest information on treated materials and topical and spatial repellents[86].

There is a perceived security risk in some armies in the GMS associated with the potential purchase of insecticide treated uniforms from overseas. This could clearly undermine the adoption of this approach for these groups.

Topical repellents. Effective topical repellents have been shown to provide good levels of personal protection against mosquitoes[135], and in Afghanistan a repellent soap containing DEET was shown to provide valuable protection against falciparum malaria [136]. Use of topical repellents clearly has the potential to provide personal protection from vector mosquitoes if properly used. However, randomized controlled trials in low endemic settings with high LLIN coverage in Tanzania[137], Lao PDR[67] and Cambodia[138] demonstrated that mass distribution of topical repellents did not result in any additional decline in malaria endemicity. In Cambodia, weak daily compliance and inappropriate use of the repellents


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were considered the main obstacles. In Tanzania, a lack of statistical power was considered a key factor affecting the outcome of the trial.

A 2018 Cochrane review of mosquito repellents for malaria prevention concluded that ‘it is questionable if topical repellents can be used for malaria prevention in the general population as daily compliance and poor standardization (amount of repellent used, surface area applied, time of application, and period between repeated applications) are major limitations of this intervention’[133].

Given that topical repellents are actively promoted or even supported by several vector borne disease control programmes in the Sub-region (e.g. for the military, for plantation workers and for forest-goers), evidence for effectiveness in these more specific settings needs to be strengthened. Further investigation of topical repellents specifically for personal protection for forest-goers is justified, particularly given that compliance may be higher amongst those for whom repellents may be perceived to offer the only solution for personal protection. Furthermore, the fact that malaria burden is considerably higher amongst forest-goers than amongst the settled populations from which they come and given that LLIN/LLHN use is usually low in these settings, so the impact of repellent should be easier to discern, it should be possible to achieve the statistical power required for a trial without the need for an unfeasibly large study population.

Larval source management (LSM). LSM consists of four sub-interventions: habitat modification, which is a permanent alteration of the environment, e.g. land reclamation and deforestation (LSM has been one of the positive side effects of the widespread deforestation across the region); habitat manipulation, which is a recurrent activity, e.g. flushing of streams; larviciding, which is the regular application of biological or chemical insecticides to water bodies; and biological control, which consists of the introduction of natural predators into water bodies.

Until the 1950s, LSM was the primary method of malaria control worldwide. After the introduction of IRS with DDT in the 1950s, and then ITNs in the 1990s, LSM was used less commonly[70]. With the prospect of elimination in the GMS and the difficulties associated with adequately addressing RMT, the potential benefits of LSM are becoming more interesting once again. While the opportunities may be limited, in some specific circumstances it seems likely that LSM could have a significant impact. A Cochrane review of mosquito LSM for controlling malaria conducted in 2013 concluded that, as long as a sufficient proportion of larval habitats can be targeted, the intervention is another policy option, alongside LLINs and IRS, for reducing malaria morbidity[139]. In the GMS, in areas where An. dirus breeding is restricted to gem pits[140] or wells[141], LSM could clearly be effective. Unfortunately, in the vast majority of cases An. dirus breeding sites are widely disseminated in dense forest.

Habitat modification may offer more promise than source reduction as a sustainable means of reducing malaria transmission in highly endemic hotspots. Anecdotal evidence from northeast Cambodia suggests that until recent improvements in access to healthcare came into effect, a vicious-cycle of malaria related to episodic environmental changes existed amongst some ethnic minority groups[108]: Traditionally, swidden farming Jarai and Tampoun communities would relocate their main village periodically to avoid evil spirits whenever the burden of disease and mortality reached intolerable levels. The new settlements were generally established within a few hundred metres of the original village.


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Trees were cleared, stilt houses made of timber, bamboo and thatch were constructed and fruit trees (including coconut and mango trees) were planted within the confines of the new settlement. Immediately after the move, the health of the villagers would improve. However, as the trees grew they provided increasing levels of shade and humidity, increasing the risk of various communicable diseases including malaria. When morbidity and mortality reached intolerable levels, the communities would once again relocate. During informal discussions, community leaders indicated that relocation occurred infrequently, once or twice in their lifetimes. All felt that moving resulted in a definite improvement in the health of their people. Surveys conducted during 2001[16] corroborated these perceptions revealing that prevalence of malaria was generally lower in newly-established un-shaded settlements, than in long-established well-shaded settlements. Convincing villagers to plant fruit trees in orchards outside their villages, rather than within the boundaries of their villages, may be difficult but could have a profound impact on transmission in these settings.

Researchers from the University of South Florida are currently using drone technology in Cambodia to search for the ‘spectral signatures’ of malaria vectors’ larval habitats in an effort to effectively target LSM interventions. Given the dense forest cover in An. dirus habitats this seems likely to be better suited to targeting An. minimus and other secondary vectors.

Ivermectin. Ivermectin appears to show promise for the control of residual malaria transmission[142]. Extensive work has been carried out in recent years in Thailand and in Africa and South America, looking at the endectocidal, and transmission blocking sporonticidal and sporozioticidal effects of ivermectin for malaria. This work has included entomological studies (both laboratory and field based)[143,144], laboratory-based parasitological studies (including the use of mouse models)[145] and clinical studies and large-scale epidemiological field trials[146–148].

MDA trials incorporating ivermectin in West Africa have demonstrated a reduction in survival[146,149], parity[146] and sporozoite rates[146,147] in An. gambiae. MDA incorporating ivermectin targets the vector with mosquito-lethal endectocides which immediately suppresses mosquito-to-human transmission[147,149,150] thus reducing the number of new infections in treated and untreated people. The direct personal benefits associated with ivermectin[151], mean that incorporating it into antimalarial MDAs may enhance overall compliance with the intervention.

Mahidol University and AFRIMS are planning to conduct a large-scale clinical study looking at the impact of ivermectin MDA in rubber plantations in Thailand in 2018 (Jetsumon Sattabongkot Prachumsri - Principal Investigator). The entomological component of the study will measure changes in the population age structure, vector composition and density, and sporozoite rate, while the epidemiological component will measure changes in malaria prevalence and incidence, gametocytemia, drug-resistant parasite ratio, and anaemia.

Ivermectin is a completely different class of insecticide to any used for LLINs, ITNs or IRS and thus its use will not exert any pressure for the selection of insecticide resistance that could undermine the effectiveness of existing vector control efforts.

A request for the evaluation of the use ivermectin as an endectocide was recently submitted to WHO and is under review. At present, no WHO policy recommendation for the use of this tool has been issued.


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Restricting forest access. As so much of RMT is forest-based in the GMS, restricting forest access is one of the most obvious means of breaking the transmission cycle, yet it is not generally discussed in malaria elimination circles. Reduced forest access commonly occurs as a result of socio-economic development, which can make community members less dependent on forest products or can allow them to purchase motorcycles so that they no longer need to overnight at forest farms. In some circumstances, socio-economic development can however increase forest access by allowing forest-goers to purchase vehicles - commonly two-wheel tractors - that enable them to spend more time deeper in the forest[119], but this example is probably the exception rather than the rule.

Reduced forest access also occurs as a result of forest and wildlife protection efforts. Governments across the GMS have established forest reserves where public access is forbidden or restricted. Policing these reserves is difficult and incursions are frequent, as evidenced by the relatively high malaria burden seen amongst adult males in the surrounding communities. In fact, malaria data, which is increasingly being generated on a real-time basis in elimination settings, could act as a good proxy indicator for forest incursions. If NMCPs were to anonymize and then share their GIS malaria data with forest and wildlife protection agencies, then these agencies might be able to target their operations more effectively, and thereby reduce the number of forest incursions and help to reduce RMT.

The Government of Viet Nam’s ‘Sedentarization Policy’[96] has resulted in a significant reduction in malaria transmission by moving people away from forests to large roadside settlements.

Insecticidal interventions for the control of zoophilic vectors. Barrier spraying around the places where livestock are kept has been suggested as a means of malaria vector control in endemic villages in Viet Nam , but sponging livestock directly with insecticide may be more effective and offers additional veterinary benefits, which is likely to strengthen compliance[152,153]. Treating livestock with ivermectin would work in a similar manner and could be expected to benefit from similarly high compliance, while not exerting any pressure for the selection of insecticide resistance. An assessment of the efficacy of ivermectin treated cattle for the control of zoophilic vectors in community settings has already been carried out with promising results in Tanzania[154] and a study is currently underway in Viet Nam.

Spatial repellents. A study in Cambodia demonstrated that spatial repellents significantly reduce landing rates of outdoor biting anophelines in some settings[155]. Unsurprisingly, a study in low endemic communities with high LLIN coverage in Mondulkiri Province, where most cases were amongst adult male forest-goers, demonstrated that spatial repellents did not result in any additional decline in malaria endemicity[56].

Push-pull systems. Village-based push-pull systems, which combine the use of spatial repellents (push) with the use of baited traps (pull), have shown promise in some settings[156]. The approach seems unlikely to have an application away from the village setting, and so seems unlikely to be useful in the GMS, where the vast majority of malaria transmission is now forest-based. A 2018 Cochrane review of mosquito repellents for malaria control concluded that there is


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insufficient evidence to conclude spatial repellents can prevent malaria[133]. Cluster randomized trials on a transfluthrin passive emanator are ongoing as part of a formal evaluation of this intervention under the WHO evaluation process for vector control tools.

Attractive toxic sugar baits. ATSBs have shown promising results in some settings where nectar sources are limited and where easy access allows for regular replenishment[157]. In some cases, acceptability has been hampered by the unpleasant odour of the formulations used (Alongkot Ponlawat, personal communication). It is not clear whether the technology could have a role in the control of forest-based malaria transmission in the GMS, where nectar sources are relatively abundant. An ATSB intervention is presently under formal WHO review, which will include cluster randomized trials.

Barrier systems.

Insecticide treated barriers (e.g.’ZeroFly’) or large outdoor treated nets could prove an effective means of vector control or personal protection in certain circumstances in places where groups gather outside in the evening (e.g. bathing areas and cafes/restaurants/bars).

Improving housing quality. A recent review and meta-analysis of the evidence for improving housing to reduce malaria concluded that, despite low quality evidence, the direction and consistency of effects indicate that traditional housing is an important risk factor for malaria[158].

Screening forest shelters and swidden farm huts Screening forest shelters and swidden farm huts with long-lasting insecticide treated netting seems to be a very obvious way in which a key risk group could be better protected against malaria, but apparently no research has been conducted on this approach to date.

A summary of recent studies and implementation of promising supplementary malaria vector control tools in the GMS by country is presented in table 7.


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Opportunities for strengthening vector control in the region The tools necessary to eliminate malaria transmission in community settings in the GMS are already available: LLINs, ITNs, IRS and early access to diagnosis and appropriate treatment, together with deforestation, urbanization and social development, are more than a match for malaria in these areas. However, poor-quality implementation undermines progress in many places and in settled communities where transmission persists, it is usually poor-quality implementation that is responsible. Implementers need to focus on improving the quality of implementation, while researchers need to focus on developing solutions for RMT in forest settings.

Increase public health entomology capacity Strengthen entomological capacity. Entomology has lost credibility by focusing too much on routine surveillance, which generally has not had any influence on policy or practice for decades. There is a feeling amongst some malariologists that entomologists are more interested in saving entomologists, than in eliminating malaria. In order to counter these obstructive views, entomologists now need to focus on ‘spelling out’ exactly what they can do to help accelerate progress towards elimination. This should probably be a key focus of the APMEN Vector Control Working Group’s ‘Resource Exchange Network’.

Entomological capacity is currently low across much of the GMS. Investment in national capacity for public health entomology and vector control is urgently required across the region, especially in Lao PDR, Myanmar and Thailand, both in support of malaria elimination and in order to effectively deal with vector borne diseases other than malaria in future. WHO’s recent intensive training course on mosquito taxonomy and identification at IPC in Cambodia was a good first step and efforts should continue to roll-out regional training on mosquito taxonomy, identification and broader aspects of entomology and vector control. Centres of excellence across the Sub-region need to do more to build capacity.

Capacity building for malaria entomology needs to be linked to the requirements of Aedes control programs.

Countries need to be convinced to build up their vector control infrastructure and human resource capacity using their domestic budgets, both in support of malaria elimination and in order to effectively deal with vector borne diseases other than malaria in future. WHO should support national programmes in the development of national strategic plans for vector control (covering all indigenous vector borne diseases), to better target existing resources and to help mobilize funds.

Adjust the focus of entomology. Given that resistance to synthetic pyrethroids in primary vectors of malaria is not yet widespread in the Sub-region and does not seem to have increased significantly over the past seven years[159], and given that the vast majority of cases are now contracted in the forest where insecticidal pressure on primary vectors is minimal, and given that the aim of the GMS malaria effort is to eliminate malaria by 2030 (and much earlier in several countries), the risks of operationally significant insecticide resistance developing in the GMS before elimination is achieved have probably been overstated. Nevertheless, monitoring the insecticide resistance status of primary vectors remains important, but the routine sentinel site approach to monitoring used in most countries is labour intensive and likely to be of limited use (except in terms of maintaining entomological capacity, which can be achieved in other ways). Insecticide resistance can be very focal and so could easily go undetected by susceptibility assessments in a small number


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of sentinel sites. Surveys should instead be targeted in areas where epidemiological findings give cause to suspect insecticide resistance. Persistent transmission foci for example could potentially indicate the presence of insecticide resistant vectors.

The focus of entomology for malaria needs to be on ‘epidemiology-led problem solving’. It is essential that entomological activities support malaria elimination in a powerful, practical and effective way. Entomologists need to help identify why persistent transmission foci are persistent and develop locally appropriate solutions. Programmes need to make urgent changes:

• Vector bionomics and insecticide resistance monitoring in sentinel sites should be

dropped in favour of responsive monitoring in the event of outbreaks and in persistent

transmission foci (‘focus investigations’), and on problem solving through ‘spot checks’.

• Wherever capacity exists, entomologists should be used strategically to investigate new

interventions for RMT.

• Sporozoite rate assessments should be dropped except in specific research contexts and

should always be conducted in conjunction with confirmatory PCR-testing.

• Insecticide resistance should only be assessed for insecticides that are in use or likely to

be brought into use (there is for example no point in assessing resistance to DDT in

countries that have banned its use).

Given that most countries either already have, or are rolling-out, mandatory day-0 reporting for malaria plus associated case and focus investigation and response measures, entomological mapping of receptivity should no longer be a priority. Programmes should be able to use epidemiological data as a direct indicator of risk, so should not need to collect entomological data as a proxy indicator. This will be a topic for a WHO Evidence Review Group in October 2018. In circumstances where it is necessary to map receptivity, for example in order to target epidemiological surveillance measures where they are not already present, NMCPs could use forest cover and topography as a proxy for the presence of vector species and potential transmission.

Improve quality and coverage of vector control Ensure that all VCPP products procured are locally appropriate and high quality. Much more attention should be focused on ensuring that the tools procured by programmes for VCPP are locally appropriate in order to maximize utilization and impact. People’s LLIN and LLHN preferences relating particularly to hole size, material (polyester or polyethylene) and LLHN design are likely to be important determinants of use[160] and should be taken into consideration prior to procurement. Whether LLHNs are provided with or without hammocks is likely to be particularly critical for forest goers. Once appropriate LLIN and LLHNs have been identified their details should be clearly specified during the initial stages of the procurement process.

Strengthen the quantification of commodity requirements. Bottom-up planning, particularly for the quantification of commodity requirements for forest-goers should be promoted. Quantification of LLHN needs for example must be based on the number of people going to the forest, rather than simply on a rate of one hammock net per household as happens in some GMS countries, or on a fixed percentage of the nets required for settled populations as happens in others. In order to accurately quantify the number of forest-goers, data needs


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to be collected by peripheral health workers and volunteers on the nature and number of people spending nights in the forest or at forest farms (taking into consideration seasonal fluctuations in forest activities) and their various preferences regarding VCPP tools. The different target groups should be involved wherever possible, with participation incentivized as necessary. Based on the information collected from the periphery, best guesses need to be developed at central level regarding the nature and scale of commodity requirements. A coordinated approach to collecting the necessary data region-wide would strengthen the evidence-base supporting VCPP requirements for forest goers.

NGO partners may be best placed to support the quantification of needs, particularly those needs associated with larger private companies operating in high-risk areas, which are often reluctant to provide authorities with accurate information regarding employee numbers.

The requirement for more robust quantification should not prevent immediate implementation. It is clear that LLHN requirements have been significantly underestimated in most settings. Realistic guestimates should be made based on local opinion and some rapid expert appraisals of need, and procurement and distribution should take place urgently while estimates of need are updated based on more detailed and comprehensive feedback from the periphery.

WHO has recently produced a series of useful toolkits designed to help address some of the issues associated with malaria amongst mobile populations and migrants (box 3).

Strengthen the targeting of interventions. The targeting of vector control interventions should always be evidence-based and never influenced by political pressures, as IRS in particular often is.

Box 3. WHO toolkits related to malaria amongst mobile populations and migrants.

1. Mobile and migrant populations and malaria information systems. This document provides current country experiences gained to improve access by mobile and migrant populations to malaria services and how to connect those services with basic information needed to improve surveillance and response mechanisms to mitigate epidemics, to detect new active malaria foci or to quickly monitor and respond to multidrug resistant parasite strains.

2. Decision-tree framework for selecting study methods for malaria interventions in mobile and migrant populations. The objective of this toolkit is to help managers decide on the kind of study that would be most useful for them, based on grant applications to be made or reported, and decisions to be made or problems to be solved.

3. Vector control and personal protection of migrant and mobile populations in the GMS: A matrix guidance on the best options and methodologies. Migrant and mobile populations require vector control and personal protection because their labour or other practices may increase their exposure to malaria mosquitos. The objective of this toolkit is to help managers to target interventions according to the specific requirements of the population in need.


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The targeting of LLINs should be tightened-up to minimize wastage and maximize cost-effectiveness without compromising impact. LLINs need to be targeted more effectively to avoiding excessively costly blanket coverage in areas that are no longer endemic. Any scale-back of vector control such as this should be based on a detailed analysis that includes assessment of receptivity and vulnerability, the strength of the active disease surveillance system, and the capacity for case management and vector control response[161].

Programmes could, for example, restrict mass distribution of LLINs to communities with recent local transmission (as in Thailand). Case-based surveillance, which is being rolled-out as a key component of the elimination strategy in the GMS, will yield the necessary information on whether or not transmission is likely to be local. Roll-out of case-based surveillance will however be a gradual process, so in the meantime programmes could use cases amongst women and children as a proxy indicator for local transmission. As a restricted approach to LLIN distribution such as this would carry some limited risks of small-scale focal malaria resurgence, provision would need to be made for increased responsive distribution of LLINs in confirmed transmission foci.

At present the approach to stratification of risk and associated targeting of LLINs varies very considerably from country to country (table 5) with profound implications for cost effectiveness. As GFATM is funding the majority of LLINs in the region, it should consider pushing for a standardised approach to targeting this high cost intervention (country funding allocations would need to be adjusted to support such a standardized approach).

NMCPs should consider halting the use of mass preventive IRS in areas adequately protected by LLINs/ITNs. Where both IRS and LLINs/ITNs are used, for example in the event of an outbreak, an alternative non-pyrethroid insecticide such as a carbamate should be used for IRS to minimize the risk of development of insecticide resistance in vector populations.

Other targeting-specific suggestions include:

• In the absence of evidence of malaria transmission in rubber plantations, programmes

should drop rubber plantation related initiatives and focus on addressing forest-based

transmission.

• Given the recent rapid reduction in malaria burden in many areas, the current API-based

stratification approach used in Myanmar may be overestimating the level of risk and

should therefore be reviewed and adjusted if appropriate[28].

• Health officials in Viet Nam need to convince People’s Committee officials that providing

VCPP to all of those in endemic areas, including unregistered mobile people, is in the

best interests of their communities.

• WCS and other conservation groups have access to forest cover maps which they use to

assess their impact and target operations. These maps are updated every two months.

The maps identify deforestation hotspots and could be used by NMCPs to target VCPP

interventions for wood-cutters more effectively.

• Research should be carried out to see if the geographical coverage of LLHNs could be

expanded to Myanmar despite the lack of habitual hammock use there.


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Adjust the focus of cross border initiatives under RAI2E ICC. Regional programmes should move away from cross-border projects focusing on narrow strips of land along borders and instead adopt a coordinated approach to eliminating malaria in each of the large forested ‘islands’ where intense transmission continues to persist. These ‘transmission islands’ often stretch well beyond border regions and cover parts of several districts, provinces or countries. This approach could likely be supported through the ICC of the RAI2E grant or through PMI. Rather than taking already overstretched peripheral health staff away from their work, each ‘forest project’ should provide the additional short-term manpower required to eliminate malaria in these inaccessible high transmission areas. More use needs to be made of volunteers drawn from within the different informal sector forest-goer groups. Programmes need to harness this human resource. These people want to stay healthy, they know how to link in to their networks, and they understand the special environments that they face in the forest.

Instigate a much greater sense of urgency surrounding the issue of forest goers. There must be a far greater sense of urgency and far more action to address the issue of malaria amongst forest goers. Increasing the coverage of personal protection measures for mobile individuals and mobile groups spending time in forest transmission hot-spots should be a primary objective of vector control staff. Each of the individual risk-groups that make up ‘MMPs’ should receive malaria prevention and case management services tailored to suit their specific needs and delivered through appropriate channels.

There should be more effort to target informal sector forest-goers at gathering points and at points of entry into risk areas. There are very few completely independent workers in the forest. Almost all are either hired by ‘managers’ or sell their products to local buyers. These managers and buyers are generally well known within the local communities. Programmes and CSO partners should work with these individuals to access informal sector forest-goers and provide them with the necessary VCPP interventions. ‘Operations research’ should take the place of ‘operational research’, with programs ‘learning by doing’ rather than ‘learning then doing’.

Take immediate action to boost the coverage of VCPP tools amongst formal sector forest-goers. The evidence collected during this review indicates that the coverage of VCPP tools amongst formal sector forest-goers is abysmally low, given their epidemiological importance and the ease with which they can be accessed. Special emphasis should be placed on ensuring state-of-the-art vector control and personal protection measures (and case management services) in the military, a highly mobile and particularly critical risk group. Military partners such as AFRIMS and NAMRU may be best placed to support this although they do not operate in all of the GMS countries. Special emphasis should also be placed on providing these services to border guards, police and forest rangers operating in the forest.

Make much more use of military and other formal sector forest-goers to support elimination efforts. Much more use should be made of the military and other formal sector forest-goers to support VCPP efforts targeting informal sector forest-goers. NMCPs must interact on a number of levels with CSOs involved in conservation in order to:

• ensure that these very high-risk groups are adequately protected (LLINs, LLHNs, repellent, treated uniforms, prophylaxis perhaps including ivermectin, and regular screening);


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• engage the CSOs in the provision of services for other forest-goers (provide them with RDT/ACT and additional LLHNs and repellent to distribute either as part of their routine community development work or from sub-stations);

• share anonymized malaria data as a proxy indicator of forest incursions to help the CSOs better target their forest protection measures (and thereby reduce malaria transmission).

Increase emphasis on treating existing conventional nets. Programmes should place increased emphasis on treating existing conventional nets with quality-assured long-lasting insecticides in preference to distributing additional LLINs to people who are already happily using conventional nets. APLMA and IVCC should work towards ensuring an affordable WHO prequalified long-lasting insecticidal net treatment product is available again as soon as possible. Using GFATM’s VPP system it should be possible to maximize demand and thereby minimize costs. Until a long-lasting formulation is available, countries should use one of the several standard (not long-lasting) prequalified net treatment products available at present.

Strengthen surveillance and M&E Strengthen targeting of focus investigations in elimination settings. Focus investigations must place much more emphasis on investigating likely transmission sites and in the case of forest-based transmission, concentrate on finding patient’s co-forest-goers and providing them with appropriate services.

Introduce additional targets for utilization of VCPP tools amongst different categories of forest goers. Programmes should set strict targets for utilization of LLHN and other VCPP tools by both formal and informal sector forest goers in the forest (for example >90% by formal and >70% for informal sector).

Introduce regular and comprehensive programme evaluation. There is a critical need for ongoing evaluation of current investments in the GMS. Either the scope of the RAI2E’s Independent Monitoring Panel should be expanded to cover the work of all sub-recipients of GFATM on at least an annual basis, or some alternative mechanism for this should be put in place.

Strengthen programme management and implementation Strengthen programme guidance. WHO guidance at global and regional levels is necessarily broad and ambitious. For example, WHO’s ‘A framework for malaria elimination’[12] states that:

‘The suitability, effectiveness and quality of vector control activities should be determined from an entomological surveillance system that operates throughout the country to monitor populations of adult Anopheles mosquitoes and changes in transmission risks’

and that,

‘Vector larval sites should also be monitored, with estimates of the abundance of larval habitats and the density of larvae and adult mosquitoes (both indoors and outdoors), insecticide resistance and meteorological indicators such as the average daily temperature and rainfall’.


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Guidance at country level, however, needs to be much more explicit and tailored to the individual country in question. It needs to be more practical and locally appropriate, taking human and financial resource constraints into consideration. With some minor amendments31 Cambodia’s plan for ‘Entomological surveillance for malaria elimination in Cambodia 2017-2021’ (see ‘Cambodia country profile’ above) for example provides a valuable template for country specific guidance. Unfortunately, this plan relies on recruiting (internationally) a suitable entomologist to lead capacity development. This has already proven difficult and so if the model were replicated to other countries across the region it would likely be impossible to recruit suitable candidates to lead. An option may be a long-term high-level technical advisor at regional level, importantly, supported by a team of long-term mid-level technical advisors at country level. Programmes should consider placements for international volunteers to strengthen capacity in weaker areas in the periphery at the forefront of malaria elimination efforts.

Much of what is written in strategy documents (often developed with technical assistance) seems to be aspirational rather than actual. There is often a ‘disconnect’ between what is written at central level and what is actually implemented in the periphery. Most entomology units do whatever is funded, rather than what has been prioritized in their plans. Planning, resource mobilization and implementation for vector control needs to be more closely linked. Senior entomologists must be more involved, particularly during resource mobilization processes.

Funding partners often have limited knowledge of entomological and vector control issues and so understandably tend to fund what they know: ‘vector bionomics’ and ‘insecticide resistance in sentinel sites’, rather than what would be most useful to the programme in a resource limited environment. Senior entomologists need to be more forthright when presenting their needs to funding partners and should call on the support of technical partners to back their requests when necessary.

Some of the guidance documents developed with the assistance of technical partners are overly complicated. Countries need simple accessible guidelines that can be used effectively by staff in the periphery who may have limited technical capacity. There needs to be more robust technical oversight and quality assurance of all technical documentation produced, including that developed with RAI2E funding.

The current WHO guidance on vector control will need to be updated to reflect lessons learned as programmes in the region progress towards elimination and prevention of reestablishment. The GTS states that:

‘A shift from universal coverage to targeting of vector control to specific populations or areas may be justified in circumstances where the inherent transmission potential is low, surveillance systems are strong, there is a high level of preparedness and the ability exists to respond quickly in the event of a resurgence’ [11].

However, WHO’s Elimination Framework states:

31 The plan is apparently to build capacity during the first 2 years of the project through the implementation of routine

surveillance, before moving on to problem solving. Given the countries looming elimination targets, it might be more appropriate to build capacity while problem solving.


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‘Optimal coverage of ITNs/LLINs or IRS should be ensured and maintained in strata that are both receptive and vulnerable to malaria transmission’.

The second statement is more cautious than the first and the two are somewhat contradictory. A number of malaria specialists in the GMS believe that the move away from blanket coverage of communities with LLINs, in favour of a focal responsive approach to LLIN distribution is overdue in many areas and that future mass distributions should be on a much smaller scale, prioritising universal coverage only in communities with local transmission.

Incentivise arduous field work. Local solutions need to be developed urgently to incentivize elimination efforts at all levels to ensure staff and volunteers make the extra efforts required to achieve elimination, despite knowing that these efforts will likely transition their jobs, and even their programmes, out of existence[162]. While there are clearly concerns regarding the sustainability of incentivizing malaria elimination, it should be noted that sustainability is less of an issue as the intensified effort needed to achieve malaria elimination will be time limited.

Address administrative issues. The GFATM needs to address administrative issues, such as the requirement for mission orders even for time-critical activities such as focus investigations and the inflexible approach towards reimbursement of unexpected costs associated with fieldwork, that are undermining programme implementation in some countries.

Strengthen and adjust the focus of intersectoral collaboration efforts. If efforts, to foster collaboration between NMCPs and commercial enterprises operating in endemic forest areas are to succeed, programmes will need to take a much more proactive approach. Rather than simply inviting potential partners to attend meetings, meetings probably need to be taken to the stakeholders’ own offices, or perhaps incentivised in some way, initially at least. Special efforts should be made to ensure that formal sector forest goers are both fully protected and fully involved in supporting implementation of malaria elimination efforts targeting informal sector forest goers. This work with formal sector forest goers should be the primary focus of efforts to boost intersectoral collaboration.

Work towards funding equity across countries Funding partners should assess funding resources by country, taking in to account any modifications to risk stratification and targeting of VCPP tools described above, and consider adjusting allocations where necessary.

Assessments of absorption capacity by funding partners should always take the causes of any underspending into consideration, in order to avoid inappropriately penalizing programmes.

Close the knowledge gaps relating to residual malaria transmission (RMT) Empirical observations are now required on a large-scale to elucidate the epidemiology of forest-based malaria transmission. Standardized protocols should be developed and incorporated into the entomological component of standard operating procedures for focus investigations across the GMS. Reports of day biting An. dirus should be taken very seriously and research associated with RMT should be adjusted accordingly.


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Develop and implement new vector control and personal protection (VCPP) interventions for forest goers Initiate large-scale trials with multiple interventions. There is an immediate need to develop new VCPP methods to address outdoor transmission[126] especially for deployment in the GMS where it now accounts for a major proportion of malaria burden and threatens to stall programmatic progress towards elimination. If GMS elimination targets are to be met, then large-scale implementation trials will need to be prioritized for the most promising tools and approaches for addressing forest-based transmission. That is, those that are likely to be cost-effective, locally appropriate and scalable. As discussed above, some of the most promising of these are:

• Locally appropriate LLHNs

• Screening forest huts with long-lasting insecticidal netting

• Insecticide treated clothing for formal sector forest-goers

• Insecticide treated blankets/sheets for informal sector forest-goers (where these are in common use)

• Topical repellents for forest-goers

• Ivermectin as an endectocide for forest-goers

• Barriers treated with long-lasting insecticides.

These trials will likely need to be coordinated between research consortia and national programmes, with both contributing to resource mobilization efforts (likely the former for funds for the research component and the latter for funds for the actual intervention(s)). Where sample size is likely to be an issue, researchers should consider trialling groups of interventions in order to increase impact and lower sample size requirements.

It may be useful in some circumstances to establish experimental entomological field-study facilities (huts and ‘biospheres’) in order to assess the entomological efficacy of new vector control/personal protection interventions. Entomological studies of this kind can be useful in helping to guide the development of larger-scale epidemiological trials. Local academic and research institutions would likely be best placed to conduct these technically advanced assessments.

Once the supporting evidence base is available, policy setting mechanisms within WHO will make appropriate recommendations for implementation by national programmes[125].

Work around product registration where possible. While every effort should be made to improve coordination between national regulatory authorities, NMCPs and vector control product manufacturers to accelerate in-country product registration, it may also be possible to accelerate elimination by working around some of the obstacles associated with regulation. For example, if products are funded by an external donor some aspects of regulation may not apply. Similarly, if products are being trialled, they may not be subject to the same regulatory requirements as products that are to be sold through the retail sector. Given the fact that RMT is becoming increasingly focal, it may be necessary to enrol a significant proportion of persistent transmission foci in a study of the effectiveness of an intervention designed to address RMT. In this case the trial itself could have a major impact in terms of burden reduction and moving the GMS closer to elimination.

Promote two-way communication between researchers and implementers. Communication needs to be two-way, with programme staff influencing research priorities and researchers


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influencing policy and practice. WHO-SEARO’s ‘Advisory Committee on Research and Development’, chaired by the Secretary General of SEAMEO TROPMED Network, should be well placed to support this. Research findings need to be reviewed and any with operational significance need to be distilled into a form in which they are accessible to programme staff. In some countries, programme leaders may need support to advocate effectively for appropriate operations research to be conducted, and researchers may need support to advocate for policy change where indicated.

Soften prequalification requirements. WHO should consider softening its requirement for gold standard RCTs as part of its prequalification process in the context of elimination in the GMS, where sample sizes sometimes need to be unfeasibly large to demonstrate impact.

Tighten the focus of research funding. WHO and other technical partners should lobby for research funding to focus on tackling RMT as an absolute priority.


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Malaria vector control in the Greater Mekong Sub …Greater Mekong Sub-region (GMS). While there has been a steady decline of malaria in the GMS, it is clear that achieving the Sub-regions