BMJ Open · 4 El Colegio de la Frontera Sur – ECOSUR, San Cristóbal de Las Casas, Chiapas, México 5 Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Quinindé,

For peer review only

Soil-Transmitted Helminthiasis in indigenous communities of the southern border of Amazonian Ecuador: Is

chemoprophylaxis enough?

Journal: BMJ Open

Manuscript ID bmjopen-2016-013626

Article Type: Research

Date Submitted by the Author: 28-Jul-2016

Complete List of Authors: Romero-Sandoval, Natalia; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida; Grups de Reserca d'Amèrica i Africa LLatines, Ortiz Rico, Claudia; Universidad Autonoma de Barcelona, Unidad de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Sánchez-Pérez, Hector; El Colegio de la Frontera Sur - ECOSUR; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Valdivieso, Daniel; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida Sandoval, Carlos; Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Parasitología Pástor, Jacob; Instituto Geografico Militar Martin Mateo, Miguel; Universidad Autónoma de Barcelona, Departamento de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL

<b>Primary Subject Heading</b>:

Public health

Secondary Subject Heading: Epidemiology, Infectious diseases, General practice / Family practice

Keywords: Epidemiology < TROPICAL MEDICINE, helminths, indigenous population, chemoprophylaxis, Ecuador

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Soil-Transmitted Helminthiasis in indigenous communities of the southern border of

Amazonian Ecuador: Is chemoprophylaxis enough?

Natalia Romero-Sandoval PhD1,2* Claudia Ortiz-Rico MPH2,3 Héctor Javier Sánchez-

Pérez PhD2,4 Daniel Valdivieso1 Carlos Sandoval5 Jacob Pástor6 Miguel Martín PhD2,3

1Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del

Ecuador, Quito, Ecuador

2 Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL, Barcelona, España

3 Unidad de Bioestadística y Epidemiología, Universidad Autónoma de Barcelona,

Barcelona, España

4 El Colegio de la Frontera Sur – ECOSUR, San Cristóbal de Las Casas, Chiapas,

México

5 Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Quinindé, Ecuador

6Instituto Geográfico Militar, Quito, Ecuador

* Corresponding author

Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del


Av. Jorge Fernandez and Simon Bolivar, Quito, Ecuador. Zip Code: EC170113

E-mail: [email protected]

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Telephone number: + 593 2 2 985600

Keywords: helminths, rural population, indigenous population, chemoprophylaxis,

Ecuador

Word count: 2856

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Abstract

Background: Rural communities on the Amazonian southern border of Ecuador have

been the object of governmental social programs during the past nine years, addressing

diseases associated with poverty, such as soil-transmitted helminth infection. The aim of

this study was to explore the prevalence of geo-helminth infection and factors

associated with it –including having received chemoprophylaxis in the last month- in

those communities.

Methods: Cross sectional study, in two indigenous communities of the Amazonian

southern border of Ecuador. The data were analyzed at both household level and

individual level.

Results: At individual level, the prevalence found was 46.9% (95% CI 39.5-54.2), with

no differences in terms of gender, age, temporary migration movements, or previous

chemoprophylaxis. In 72.9% of households, one or more members were infected.

Receiving subsidies and overcrowding were associated to presence of helminths.

Conclusion: The prevalence found of soil-helminth infection remained high in spite of

recent chemoprophylaxis. Our study suggests that it is necessary to conduct studies

focusing on communities, and not simply on captive groups such as school-children,

with the object of proposing more suitable and effective strategies to control this

problem.

Strengths and limitations of this study

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• A cross-sectional study carried out in indigenous communities of extreme

poverty, during a community visit, shows the situation of geo helminths.

• Applied strategy called for 80% of the inhabitants and only one of every three

homes not found helminths.

• This study was conceived as an exercise in community participation, conceived

as a mechanism for more democracy and transformation of the health sector.

• This study is limited by the low participation rate of men of working age.

• This study is limited by the collection of a single stool sample and prevalence

could be underestimated.

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INTRODUCTION

Soil-transmitted helminthiasis is a neglected tropical disease, which particularly

affects low and medium-low income population groups. The social and health

consequences become evident through academic performance, nutritional status,

economic development and chronic infection.[1] Both Ascaris lumbricoides and

whipworm (Trichuris trichiura), are transmitted through food and water contaminated

by feces of infected individuals, while Ancylostoma duodenale (hookworm) is

transmitted by walking barefoot on contaminated soil, or by ingestion of larva. The

situation is particularly serious in populations with high rates of migration and mobility

within and between rural and urban communities, and hence these infections constitute

a serious public health problem in these kinds of communities.[2]

Since the announcement in 2001[3] of a commitment to eradicate soil-

transmitted helminthiasis in low transmission areas, and reduce morbidity in high

transmission areas, reports from various places around the world indicate that these

goals are not being met, despite the established chemoprophylactic models.[4]

Ecuador, a multi-ethnic, medium-low income country, initiated a process of

social and economic reform in 2007, which has been reflected, for example, in a rise of

122% in public health spending and in the proportion of the gross domestic product

during the period 2000-2011.[5]

Among the various social policies, we may cite the antipoverty conditional cash

transfer programs (human development subsidies, subsidies for school books, and for

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school uniforms), aimed to assist people in extreme poverty.[6] On the other hand,

Ecuador has had one of the highest rates of internal and external migration, including

inhabitants of the Amazonian area.[7]

In the Amazonian southern border area, object of the present study, 34% of

homes are considered to be of poor quality (bare earth floor, gaps in house walls, roof of

metal or palm leaves), 55% use water from a well, river or rainwater collection system,

only 22% are connected to a sewage network.[8] These communities, located some 45

km from the nearest urban area and nearest communication center, until five years ago

were only accessible via unpaved road, and residents could only get to health facilities

and administrative municipal offices via narrow tracks through the jungle.

In Ecuador there are no data on soil-transmitted helminthiasis prevalence, nor on

systematic coverage of prophylactic treatment or epidemiological surveillance;

however, according to official figures covering the whole country, all children aged

under five years ought to have received chemoprophylaxis in 2014.[9]

Seeking to increase visibility of health problems in population areas which are

so small that classical studies tend to conceal them, the GRAAL research group (“Grups

de Recerca d’Amèrica i Âfrica Llatines”) conducts studies on infectious/contagious

diseases focusing on vulnerable, and often high-risk, population groups, often invisible

in national level epidemiological analyses. This approach has been termed patchwork

studies.[10]

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In the present study in two indigenous communities of the Amazonian southern

border of Ecuador, we aimed to quantify the prevalence of soil-transmitted

helminthiasis at both household and individual levels, as well as its relationship with

chemotherapy received in the last month, among other variables of interest.

METHODS

In June 2015, a cross-sectional study was performed in two communities, once

agreement and consent of local authorities had been obtained, based on criteria of

convenience in a community assembly where local political and health personnel were

represented. Although no censuses were available for these communities, they are

estimated to have about 240 inhabitants, according to their leaders. Both communities

can be reached by road, and are situated around 10 hours travelling (540 km) from the

capital of Ecuador.

Figure 1 shows the rate of joint distribution of the proportion of households self-

identified as indigenous poverty measured by unsatisfied basic needs index in Ecuador.

The studied communities are located in the Amazon border and one of the two

Ecuadorian areas with more poverty among the indigenous population.[11]

Following the patchwork methodological scheme, which has been applied by

our research team to analyze health problems such as pulmonary tuberculosis and

sylvatic rabies,[12,13] we applied a questionnaire that was administered face-to-face to

identify dwellings and obtain household characteristics, including whether they boiled

the water used, overcrowding, whether they received any unconditional cash transfers

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(subsidy), functionally illiterate person and transportation system to the nearest health

unit. At individual level we recorded self-perceived presence of geohelminths in the last

month, whether they had received preventive chemotherapy (also in the last month,

since the communities had recently been visited by local health teams), and temporary

migratory movements. Age was categorized into three categories (2-5, 6-19, ≥20 years).

For children aged under eight years, the questions were answered by the mother or

guardian.

One fecal sample was collected from each participant. All samples (192) were

examined using direct observation, 178 samples by Kato-Katz technique, and 184 by

formol-ether concentration; in both the latter cases, missing data corresponds to samples

that were insufficient to permit their being assessed. A positive sample was defined by

the presence of at least one egg or larva being detected by any one of the three methods.

Direct observation and the Kato-Katz method were used to assess samples on the same

day on site, in the communities, with a mobile parasitological analysis laboratory

installed there. Kato-Katz technique was performed with a template of 41.7 mg, as

recommended by the WHO.[14] Samples were preserved in formol-ether and an

analysis of this concentrate was performed at a base laboratory.

In the cases of the Kato-Katz method and formol-ether concentrate analyses, the

result recorded was the highest value obtained after examining two aliquots. Eggs per

gram of feces (epg) were calculated using the helminths eggs counted for each parasite

species obtained from the Kato-Katz technique multiplied by a factor of 24, as

recommended by WHO for the template used. Egg counts as epg were utilized to

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classify the intensity of infection as slight, moderate or high respectively, as follows: for

A. lumbricoides 1-4999 epg, 5000 – 49999 epg, and >= 50000 epg; for T. trichuria 1-

999 epg, 1000 – 9999 epg, and >= 10000 epg.[15] We used frequencies, percentages;

mean, standard desviation, median and percentile for continuous variables. We estimate

global and stratified prevalence and 95% confidence intervals. In the case of cross

tabulations we used prevalence ratio (PR) and 95% confidence intervals, likelihood

ratio (LR) and p value ≤ 0.05. We calculated a linear association between age and

perception of parasites, and having received preventive chemotherapy.

RESULTS

The study included 59 households, and a total of 320 individual members. The

number of members per household ranged from 2 to 13 (average 5.4, median 5). At

least one functionally illiterate person was identified in 33.3% of the households

studied; 15.4% of the households had to travel by walking to get to the nearest health

facility, the remainder used ground-based public transport; 72.4% of households

reported that at least one member had expelled geohelminths in the last month. Fifty

nine households provided fecal samples (average number of members providing a

sample: 3.1; median, 3).

In 16 (27.1%) of the households which provided fecal samples, no geohelminths

were observed; in another 30 (50.8%) one or more members were infected, and in 13

(22.0%; 95% CI 12.1-32.8) all fecal samples were positive.

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Sanitary and/or socioeconomic deficiencies were observed in 49.2% of

households (bare earth floor, windows not covered, no wastewater disposal system, no

electricity, did not have their own supply of drinking water), and in 79.3% (23/29) of

these, at least one member was infected by geohelminths; in contrast, among

households with better conditions, 66.7% (20/30) presented one or more infected

members (PR 1.19; 95% CI 0.86-1.67).

Forty four (74.6%) households reported receiving one or more state subsidies.

Of them, 81.8% had infected members, compared to 46.7% (7/15) among households

not receiving any subsidies (PR 1.75; 95% CI 1.09-3.97).

Twenty nine (49.2%) of the households reported overcrowding (more than three

inhabitants per bedroom), of which 86.2% had infected members (PR 1.44; 95% CI

1.04-1.99) versus 60.0% (18/30). Among the 36 households declaring they did not boil

the water, 28 (77.8%; 95% CI 64.2-91.4) had geohelminths infection, whereas the

corresponding figure among households reporting they do boil water was 63.6% (95%

CI 53.3-73.8) (PR 1.22; 95% CI 0.88-1.88).

Of the 192 participants who provided fecal samples, 106 (55.2%) were females.

The mean age was 22.8 (SD 19.4) years, while P25 corresponded to 8 years, P50 to 14

years, and P75 to 38 years (range 76). The median ages for males and females were 10

and 18 years, respectively (p<0.05).

Positivity to the presence of soil-transmitted helminths was detected in 28.6% of

the 192 samples analyzed by direct observation; 39.9% by the Kato-Katz method, and

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31.5% by the formol-ether concentrate. It was possible to analyze 178 cases by both

direct observation and the Kato-Katz method, of which 105 were negative to both

(59%); 20 were negative according to direct observation but positive to Kato-Katz; two

were positive according to direct observation but negative to Kato-Katz, and 51 were

positive to both (28.9%). Determinations obtained by both direct observation and by

analysis of the formol-ether concentrate coincided in 184 cases: 119 were negative

(64.7%) and 45 (24.5%) positive to both; 13 were negative according to direct

observation but positive according to the formol-ether method, and 7 were positive by

direct observation but negative according to the formol-ether method.

A positive result in at least one of the three tests for soil-transmitted

helminthiasis was observed in 83 of the 177 samples where it was possible to perform

such determinations (46.9%; 95% CI 39.5-54.2). Among females the prevalence was

52.6%; (51/97; 95% CI 42.7-62.5) and among males was 40.0% (32/80; 95%CI 29.3-

50.7); prevalence ratio 1.31 (95% CI 0.9-1.8). In the 60/177 participants who declared

temporarily going away from their communities, geohelminthiasis was found in 51.7%

(95% CI 44.1-59.3), whereas among those who did not go away, the corresponding

figure was 44.4% (95% CI 37.3-52.0).

One hundred and twelve participants (58.3%; 95% CI 51.0-65.1) –without

significant differences by sex– declared the self-perceived presence of geohelminths in

the last month. Table 1 shows the distributions of the presence, both measured and self-

perceived, of soil-transmitted helminthiasis, by age groups. In the case of the measured

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presence of soil-transmitted helminthiasis, no differences were found in terms of age

groups (LR 1.53; p=0.47) (Table 1). In contrast, for the perceived presence of parasites,

differences were significant (LR 9.75; p<0.05), a linear association being found

between perception of parasites and age, with higher ages reporting a lower perception

(80.0% to 48.1%) (p<0.05).

Table 1. Measured and perceived prevalence of geohelminthiasis

Age group (years)

Presence of geohelminthiasis (measured)

Presence of geohelminthiasis in the last month (perceived )

n (%)

95% CI n

(%) 95% CI

2-5 15/29 24/30 51.7 34.5-69.0 80.0 63.3-93.3

6-19 39/80 51/85 48.8 37.5-58.8 60.0 49.4-70.6

≥20 40/68 37/77 58.8 47.1-70.6 48.1 36.4-59.7

In the group aged 2 to 5 years, having received preventive chemotherapy in the

last month was declared by 25/30 participants (83.3%); 56/85 (65.9%) in the group aged

6 to 19 years, and 30/77 (39.0%) in the group aged 20 years and over (LR 22.37

p<0.05). This association was also linear (p<0.05).

Of the 104 participants who declared having received preventive chemotherapy

in the last month and in whom the coproparasite assessment was performed, 46 (49.2%)

were positive to the presence of helminths, while this happened for 37/73 (50.7%) of

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those who had not received it (LR 0.72; p=>0.05); there were no differences by either

sex or age group.

The parasitic load of A. lumbricoides varied from 24 to 18792 epg, 50% having

408 epg or over. In the group aged 2-5 years the median intensity was 600 epg, in those

aged 6-19 it was 348, and in those aged 20 and over it was 384.

The intensity of infection among individuals aged 2-5 years was slight, among

those aged 6-19 years it was slight in 90% and moderate in 10%, while in those aged 20

or over it was slight in 86.4% and moderate in 13.6%. The parasitic load of T. trichuria

ranged from 24 to 1080 epg, with median 72 and levels by age group of 48, 72 and 60,

respectively. The most common level of intensity of infection, in all age groups, was

slight, with moderate levels being found in 2% of those aged 6 to 19 years.

DISCUSSION

Even though members of the two communities analyzed had received preventive

chemoprophylaxis one month before the study, 72.9% of households had at least one

person infected by soil-transmitted helminthiasis, and in 13% all members were

infected. Also we found a higher prevalence among households stating they did not boil

water, or presented overcrowding, as well as families receiving any kind of state

subsidy, thus indicating their worse sanitary conditions. This is an important aspect to

consider because our results show that preventive community health campaigns simply

aiming to reduce or avoid soil-transmitted helminthiasis, are not sufficient, and must be

accompanied by changes in sanitary conditions and poverty. In this sense, the lack of

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good water supplies and the inadequate basic sanitation observed during the fieldwork,

as well as a low participation of the communities themselves in basic sanitation

activities, could both be factors that impede the control of soil-transmitted helminth

infections.[16–18]

Additionally, the fact that receiving any kind of state subsidy or presenting

overcrowding were both associated to prevalence of infection at household level seems

to confirm that it is not enough to treat this problem as merely a medical one, and that it

is necessary improve the socioeconomic and sanitary conditions of population. At

individual level, the high prevalence found was not differentiated by gender, age group,

temporary migratory movement, nor by whether they had received chemoprophylaxis or

not.

With respect to the results obtained in this community-based study (global

prevalence of 46.9% in samples where it was possible to perform the three

determinations –direct observation, Kato-Katz method and analysis of the formol-ether

concentrate), there are few references with which we can compare, since the majority of

studies are conducted in “captive” populations, such as school-children.[19-21]

The prevalence found in this study is much higher than figures reported by four articles

available in the scientific literature that deal with the Ecuadorian situation –with an

average of 18.9%[22,23] –, which formed part of a meta-analysis based on all

publications related to prevalence of soil-transmitted helminth infection in South

American countries. Nevertheless, our overall prevalence figure is lower than that

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reported by a previous study carried out in groups of Shuar people (prevalence rate of

65%), using Kato-Katz method but without the antecedent of having received

chemoprophylaxis.[24]

We found a large discrepancy between the measured and perceived prevalence

of geohelminthiasis, particularly for children under 5 years of age, since in nearly 8 of

every ten, the mother or guardian who responded perceived the presence of parasites,

whereas our determinations halve this figure. This discrepancy could be explained by

the fact that the national program of preventive chemotherapy acted in these

communities four weeks before this study. On the other hand, the prevalence in those

aged over 19 years, who were also the least treated group, leads us to reflect that in

these communities, the adult population could constitute a reservoir for infection and re-

infection.[24]

In Ecuador, the epidemiological surveillance of soil-transmitted helminth

infections has not been considered either explicitly, nor as part of the group of neglected

infectious diseases, and the estimated prevalence of infection might be high,[25] but

currently the data are scarce or non-existent. However, the Ecuadorian state publishes

reports of its successful health campaigns for the control of neglected diseases such as

brucellosis, Chagas disease, urban rabies, Onchocerciasis, and publicizes the important

increase in the budget for the control of neglected tropical diseases.[26] Nevertheless,

the official figures themselves are indicative of the poor housing conditions, the high

proportion of indigenous population with limited access to health services and poor

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sanitation, all aspects that facilitate the continuance of these parasitic infections,

especially in rural areas.

The transmission rate of soil-helminths remains high in regions such as the

Amazonian southern border of Ecuador, in spite of the fact that in recent years Pan

American Health Organization member countries have celebrated regional conventions

addressing the intensification of control of these poverty-related diseases.[27] On the

other hand, the World Health Organization recommends that school-based deworming

programs include health hygiene education as a complementary measure, although the

sustainability and the long-term impact of such education in hygiene does not appear to

show encouraging results.[28]

These limitations in the control and epidemiological surveillance of helminthic

infections could be solved with a long-term, intersectoral multidisciplinary

program.[29]

Finally, two limitations should be taking into account when interpreting our

results. Given the age distribution of participants, the participation rate among working-

age males was very low, something which could be attributable to two aspects: to their

absence from the community due to work, and a tendency of people in this group to

refuse to provide fecal samples. The other limitation is that the collection of a single

stool sample probably means prevalence has been underestimated. Given the

environmental conditions and geographical isolation, as well as a lack of resources, it

was not possible to obtain more fecal samples.

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CONCLUSIONS

All inhabitants of the two participating communities may consider themselves to be at

risk of soil-transmitted helminth infection, despite their reporting having been

administered preventive chemotherapy during the month prior to the study. For this

reason, it is necessary to conduct holistic studies focusing on communities, and not

simply on captive groups such as school-children, with the object of proposing more

suitable and effective strategies to control such infections.

ACKNOWLEDGMENTS The authors gratefully acknowledge the contributions of

Lino Arisqueta, Lizeth Cifuentes, Nicole Mora-Bowen, Gabriela León and Paola Lecaro

to the field work of the study.

CONTRIBUTORS NRS, COR, MM wrote the statistical analysis plan, cleaned and

analyzed the data, and drafted and revised the paper. NRS, MM, CS JP and HSP

provided guidance on the data handling, contributed to the design of the analysis,

provided interpretation of data and revised the paper. COR, DV, CS, JP contributed to

interpretation of the data and revised the paper. NRS, JP, MM and HSP provided

guidance on the conception of the work, interpretation of the data and revised the paper

for content. All members have approved the final version of the manuscript.

FUNDING This work was supported by Universidad Internacional del Ecuador

Research Programme grant number I-EO-01-2014.

COMPETING INTERESTS None.

ETHICS APPROVAL The study protocol was approved by the Ethical Committee of

the Universidad Central del Ecuador, and by the Ecuador Ministry of Public Health.

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Each study participant gave their written informed consent, and in the case of children,

signed by their parents.

DATA SHARING STATEMENT No additional data available.

REFERENCES

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MM. Pulmonary Tuberculosis in Latin America: Patchwork Studies Reveal

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Inequalities in Its Control–The Cases of Chiapas (Mexico), Chine (Ecuador) and

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(accessed 2 Jun 2016).

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rabies and the perception of vampire bat activity in communities in the

Ecuadorian Amazon. Cad Saúde Pública. 2014;30(3):669–74.

13 Ortiz-Rico C, Aldaz C, Sánchez HJ, Martin M, Romero-Sandoval N.

Conformance contrast testing between rates of pulmonary tuberculosis in

Ecuadorian border areas. Salud Publica de Mexico. 2015;57(6):496-503.

14 WHO Expert Committee. Prevention and control of schistosomiasis and soil-

transmitted helminthiasis. World Health Organization technical report series,

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15 Speich B, Ali SM, Ame SM, Albonico M, Utzinger J, Keiser J. Quality control

in the diagnosis of Trichuris trichiura and Ascaris lumbricoides using the Kato-

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Katz technique: experience from three randomised controlled trials. Parasit

Vectors. 2015;8:82.

16 Bain R, Cronk R, Wright J, Yang H, Slaymaker T, Bartram J. Fecal

contamination of drinking-water in low- and middle-income countries: a

systematic review and meta-analysis. PLoS Med. 2014;11(5):e1001644.

17 Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M. Impact of health

education on soil-transmitted helminth infections in schoolchildren of the

Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis.

2013;7(9):e2397.

18 Lo NC, Bogoch II, Blackburn BG, Raso G, N’Goran EK, Coulibaly JT, et al.

Comparison of community-wide, integrated mass drug administration strategies

for schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness

modelling study. Lancet Glob Health. 2015;3(10):e629–e638.

19 Dana D, Mekonnen Z, Emana D, Ayana M, Getachew M, Workneh N, et al.

Prevalence and intensity of soil-transmitted helminth infections among pre-

school age children in 12 kindergartens in Jimma Town, southwest Ethiopia.

Trans R Soc Trop Med Hyg. 2015;109(3):225–7.

20 Macchioni F, Segundo H, Gabrielli S, Totino V, Gonzales PR, Salazar E, et al.

Dramatic decrease in prevalence of soil-transmitted helminths and new insights

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into intestinal protozoa in children living in the Chaco region, Bolivia. Am J

Trop Med Hyg. 2015;92(4):794–6.

21 Chammartin F, Scholte RGC, Guimarães LH, Tanner M, Utzinger J, Vounatsou

P. Soil-transmitted helminth infection in South America: a systematic review

and geostatistical meta-analysis. Lancet Infect Dis. 2013;13(6):507–18.

22 Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and

disease burden of soil transmitted helminth infections in 2010. Parasit Vectors.

2014;7:37.

23 Cepon-Robins TJ, Liebert MA, Gildner TE, Urlacher SS, Colehour AM,

Snodgrass JJ, et al. Soil-transmitted helminth prevalence and infection intensity

among geographically and economically distinct Shuar communities in the

Ecuadorian Amazon. J Parasitol. 2014;100(5):598–607.

24 Nikolay B, Mwandawiro CS, Kihara JH, Okoyo C, Cano J, Mwanje MT, et al.

Understanding Heterogeneity in the Impact of National Neglected Tropical

Disease Control Programmes: Evidence from School-Based Deworming in

Kenya. PLoS Negl Trop Dis. 2015;9(9):e0004108.

25 Menzies SK, Rodriguez A, Chico M, Sandoval C, Broncano N, Guadalupe I, et

al. Risk factors for soil-transmitted helminth infections during the first 3 years of

life in the tropics; findings from a birth cohort. PLoS Negl Trop Dis.

2014;8(2):e2718.

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26 Cartelle Gestal M, Holban AM, Escalante S, Cevallos M. Epidemiology of

Tropical Neglected Diseases in Ecuador in the Last 20 Years. PloS One.

2015;10(9):e0138311.

27 Holveck JC, Ehrenberg JP, Ault SK, Rojas R, Vasquez J, Cerqueira MT, et al.

Prevention, control, and elimination of neglected diseases in the Americas:

pathways to integrated, inter-programmatic, inter-sectoral action for health and

development. BMC Public Health. 2007;7(1):6.

28 Thériault FL, Blouin B, Casapía M, Gyorkos TW. Sustaining a hygiene

education intervention to prevent and control geohelminth infections at schools

in the Peruvian Amazon. Revista Panamericana de Salud Pública.

2015;38(4):344-6.

29 Panic G, Duthaler U, Speich B, Keiser J. Repurposing drugs for the treatment

and control of helminth infections. Int J Parasitol Drugs Drug Resist.

2014;4(3):185–200.

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Figure 1. Poverty, indigenus and study area

297x210mm (299 x 299 DPI)

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STROBE Statement—checklist of items that should be included in reports of observational studies

Item

No

Recommendation Pg

Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the

abstract

3

(b) Provide in the abstract an informative and balanced summary of what was

done and what was found

3

Introduction

Background/rationale 2 Explain the scientific background and rationale for the investigation being

reported

5

Objectives 3 State specific objectives, including any prespecified hypotheses 7

Methods

Study design 4 Present key elements of study design early in the paper 7

Setting 5 Describe the setting, locations, and relevant dates, including periods of

recruitment, exposure, follow-up, and data collection

7

Participants 6 (a) Cohort study—Give the eligibility criteria, and the sources and methods of

selection of participants. Describe methods of follow-up

Case-control study—Give the eligibility criteria, and the sources and methods

of case ascertainment and control selection. Give the rationale for the choice

of cases and controls

Cross-sectional study—Give the eligibility criteria, and the sources and

methods of selection of participants

7

(b) Cohort study—For matched studies, give matching criteria and number of

exposed and unexposed

Case-control study—For matched studies, give matching criteria and the

number of controls per case

-

Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and

effect modifiers. Give diagnostic criteria, if applicable

8

Data sources/

measurement

8* For each variable of interest, give sources of data and details of methods of

assessment (measurement). Describe comparability of assessment methods if

there is more than one group

8

Bias 9 Describe any efforts to address potential sources of bias 7

Study size 10 Explain how the study size was arrived at 7

Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable,

describe which groupings were chosen and why

7-8

Statistical methods 12 (a) Describe all statistical methods, including those used to control for

confounding

9

(b) Describe any methods used to examine subgroups and interactions 9

(c) Explain how missing data were addressed 9-

10

(d) Cohort study—If applicable, explain how loss to follow-up was addressed

Case-control study—If applicable, explain how matching of cases and

controls was addressed

Cross-sectional study—If applicable, describe analytical methods taking

account of sampling strategy

-

(e) Describe any sensitivity analyses -

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Results Pg

Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially

eligible, examined for eligibility, confirmed eligible, included in the study, completing

follow-up, and analysed

-

(b) Give reasons for non-participation at each stage -

(c) Consider use of a flow diagram -

Descriptive

data

14* (a) Give characteristics of study participants (eg demographic, clinical, social) and

information on exposures and potential confounders

9-10

(b) Indicate number of participants with missing data for each variable of interest 9-10

(c) Cohort study—Summarise follow-up time (eg, average and total amount) -

Outcome data 15* Cohort study—Report numbers of outcome events or summary measures over time -

Case-control study—Report numbers in each exposure category, or summary

measures of exposure

-

Cross-sectional study—Report numbers of outcome events or summary measures 9-10

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and

their precision (eg, 95% confidence interval). Make clear which confounders were

adjusted for and why they were included

9-12

(b) Report category boundaries when continuous variables were categorized 8

(c) If relevant, consider translating estimates of relative risk into absolute risk for a

meaningful time period

-

Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and

sensitivity analyses

-

Discussion

Key results 18 Summarise key results with reference to study objectives 13

Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or

imprecision. Discuss both direction and magnitude of any potential bias

14,16

Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,

multiplicity of analyses, results from similar studies, and other relevant evidence

13-

16

Generalisability 21 Discuss the generalisability (external validity) of the study results 15

Other information

Funding 22 Give the source of funding and the role of the funders for the present study and, if

applicable, for the original study on which the present article is based

17

*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and

unexposed groups in cohort and cross-sectional studies.

Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and

published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely

available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at

http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is

available at www.strobe-statement.org.

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Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional study in the southern border of

Amazonian Ecuador

Journal: BMJ Open

Manuscript ID bmjopen-2016-013626.R1


Date Submitted by the Author: 03-Nov-2016

Complete List of Authors: Romero-Sandoval, Natalia; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida; Grups de Reserca d'Amèrica i Africa LLatines, Ortiz Rico, Claudia; Universidad Autonoma de Barcelona, Unidad de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Sánchez-Pérez, Hector; El Colegio de la Frontera Sur - ECOSUR; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Valdivieso, Daniel; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida Sandoval, Carlos; Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Parasitología Pástor, Jacob; Instituto Geografico Militar Martin Mateo, Miguel; Universidad Autónoma de Barcelona, Departamento de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL


Public health




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1

Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional

study in the southern border of Amazonian Ecuador.







Barcelona, España


México








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Ecuador

Word count: 2935

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Abstract

Background: Rural communities in the Amazonian southern border of Ecuador have

benefited from governmental social programs during the past nine years, which have

been addressing diseases associated with poverty, such as soil-transmitted helminth

infection. The aim of this study was to explore the prevalence of geo-helminth infection

and several factors associated with it in those communities.

Methods: Cross sectional study in two indigenous communities of the Amazonian

southern border of Ecuador. The data were analyzed at both household and individual

level.

Results: At individual level, the prevalence of geo-helminthes reached a 46.9% (95% CI

39.5-54.2), with no differences in terms of gender, age, temporary migration

movements, or previous chemoprophylaxis. In 72.9% of the households, one or more

members were infected. Receiving subsidies and overcrowding were associated to

presence of helminths.

Conclusion: The prevalence found of soil-helminth infection remained high. Our study

suggests that it is necessary to conduct studies focusing on communities, and not simply

on captive groups such as school-children, with the object of proposing more suitable

and effective strategies to control this problem.


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poverty, shows the situation of geo helminths.

• Applied strategy called for 80% of the inhabitants and only one of every three

homes not found helminths.

• This study constituted an exercise in community participation, conceived as a

mechanism for achieving greater democracy.


• This study is constrained by the collection of a single stool sample and

prevalence could be underestimated.

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INTRODUCTION







transmitted by walking barefoot on contaminated soil, or by ingestion of larva.[2]

The situation is particularly serious in populations with high rates of migration

and mobility within and between rural and urban communities, and hence these

infections and hence these infections continue transmitting and spreading.[3]

Since the announcement in 2001[4] of a commitment to eliminate soil-









transfer programs (“human development subsidies”, for instance, subsidies for school

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books, and for school uniforms), aimed to assist people in extreme poverty.[7] On the

other hand, Ecuador has had one of the highest rates of internal and external migration,

including inhabitants of the Amazonian region.[8]


dwellings are considered to be of poor quality (bare earth floor, gaps in house walls,

roof of metal or palm leaves), 55% use water from a well, river or rainwater collection

system, only 22% are connected to a sewage network.[9] These communities, located

approximately 45 km from the nearest urban area and nearest communication center,

until five years ago were only accessible via unpaved roads, and residents could only

get to health facilities and administrative municipal offices via narrow tracks through

the jungle.




from two to five years ought to have received chemoprophylaxis in 2014.[10]

In an effort seeking to increase visibility of health problems in population areas

which are so small that classical studies tend to conceal them, the GRAAL research

group (“Grups de Recerca d’Amèrica i Âfrica Llatines”) conducts studies on

infectious/contagious diseases focusing on vulnerable, and often high-risk, population

groups, often invisible in national level epidemiological analyses. This approach has

been termed patchwork studies.[11]

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8




several variables of interest.

METHODS






can be reached by road, and are situated around 10 hours journey (540 km) from the

capital of Ecuador, Quito.

Figure 1 shows the participating communities and its geographical location, as

well as the joint distribution of the proportion of households self-identified as

indigenous and categorized as poor based on a measured called unsatisfied basic needs

index. These communities are located in the Amazon border and one of the two

Ecuadorian areas with more poverty among the indigenous population.[12]



sylvatic rabies,[13,14] we applied a questionnaire that was administered face-to-face to

identify dwellings and obtain household characteristics, including presence or absence

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9

of water supply and sanitary toilets, whether households boil water for consumption,

overcrowding, whether they received any subsidy. At individual level we recorded

temporary migratory movements, self-perceived presence of geohelminths in the last

month and whether they had received preventive chemotherapy – something which

could only be ascertained for the last month, due to problems in the register of the

information about administration of chemoprophylaxis in the studied communities. The

medication (Albendazol 400 mg one dose) was provided by Ecuador Ministry of Public

Health. For children aged under eight years, the questions were answered by the mother

or guardian.

One direct fecal sample was collected from each participant. All samples (192)

were examined using direct observation, 178 samples by Kato-Katz technique, and 184

by formol-ether concentration; in both the latter cases, missing data corresponds to

samples that were insufficient to permit their being assessed. A positive sample was

defined by the presence of at least one egg or larva being detected by any one of the

three methods. Direct observation and the Kato-Katz method were used to assess

samples on the same day on site, in the communities, with a mobile parasitological

analysis laboratory installed there. Kato-Katz technique was performed with a template

of 41.7 mg, as recommended by the WHO.[15] Samples were preserved in formol-ether

and an analysis of this concentrate was performed at a base laboratory. All three

techniques have been used by other studies in Ecuador.[16,17]



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999 epg, 1000 – 9999 epg, and >= 10000 epg.[18]

RESULTS












All inhabitants use natural spring-water, which is piped to community tanks

without any type of treatment; nobody had toilets. Other sanitary and/or socioeconomic

deficiencies were observed in 49.2% of households (bare earth floor, windows not

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covered, no wastewater disposal system, no electricity, absence of own drinking water

supply), and in 79.3% (23/29) of these, at least one member was infected by

geohelminths; in a similar fashion, among households with better conditions, 66.7%

(20/30) presented one or more infected members (PR 1.19; 95% CI 0.86-1.67).









CI 53.3-73.8) (PR 1.22; 95% CI 0.88-1.88).


The mean age was 22.8 (SD 19.4) years, while percentile 25 corresponded to 8 years,

percentile 50 to 14 years, and percentile 75 to 38 years (range 76). The median ages for

males and females were 10 and 18 years, respectively (p<0.05); 37% of working-age

men reported having to migrate for work-related reasons (hunting, agriculture, mine-

work), tending to be away for 8 to 15 days, or even more.



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temporarily going away from their communities, geohelmintiasis was found in 51.7%


figure was 44.4% (95% CI 37.3-52.0).






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between perception of parasites and age, with higher ages reporting a lower perception

(80.0% to 48.1%) (p<0.05).


Age group (years)



n (%)

95% CI n (%)

95% CI

2-5 15/29 24/30 51.7 34.5-69.0 80.0 63.3-93.3

6-19 39/80 51/85 48.8 37.5-58.8 60.0 49.4-70.6

≥20 40/68 37/77 58.8 47.1-70.6 48.1 36.4-59.7

In the last month 57.8% reported having received preventive chemotherapy; in

the group aged 2 to 5 years, having received preventive chemotherapy in the last month

was declared by 25/30 participants (83.3%); 56/85 (65.9%) in the group aged 6 to 19

years, and 30/77 (39.0%) in the group aged 20 years and over (LR 22.37 p<0.05). This

association was also linear (p<0.05).




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sex or age group.










DISCUSSION

In this study we found that 72.9% of households had at least one person infected

by soil-transmitted helminthiasis, and in 13% all members were infected. Also we found

a higher prevalence among households stating they did not boil water; or presented

overcrowding, as well as families receiving any kind of state subsidy, thus suggesting

their worse sanitary conditions and greater poverty.

In marginalized populations, lacking sanitary conditions, one form of treating

water for human consumption, in the home, is by boiling it, thus preventing its

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contamination through contact with unwashed hands, dust rising from the bare earth

floor, etc., even though the effectiveness of boiling may be questionable.[19]

This is an important aspect to consider because our results show that community

de-worming campaigns (57.8% received chemoprophylaxis in the last month) aiming to

reduce or avoid soil-transmitted helminthiasis, without health education, are not

sufficient, and must be accompanied by changes in sanitary conditions and poverty

reduction policies and actions. In this sense, the lack of good water supplies and the

inadequate basic sanitation observed during the fieldwork, as well as a low participation

of the communities themselves in basic sanitation activities, could both be factors that

impede the control of soil-transmitted helminth infections.[20–22]



to confirm that it is not enough to treat this problem merely as a medical, and that it is

necessary to improve the socioeconomic and sanitary conditions of the population. At

individual level, the high prevalence found was not differentiated by gender, age group,

temporary migratory movement, nor by whether they had received chemoprophylaxis or

not, this latter aspect being seen as a reflection of the community's situation, and not

necessarily as an assessment of the efficacy of the chemoprophylaxis program of Public

Health Ministry.



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concentrate), there are few references with which we can compare against, since the

majority of studies are conducted in “captive” populations, such as school-children.[23-

25]

The prevalence found in this study is much higher than figures reported by several

articles available in the scientific literature that deal with the Ecuadorian situation –with

an average prevalence of 18.9%[26,27], which formed part of a meta-analysis based on

all publications related to prevalence of soil-transmitted helminth infection in South






of geohelminthiasis, particularly for children under 5 years of age, since nearly 8 of

every ten, the mother or guardian who responded perceived the presence of parasites,

whereas our findings halve this figure. This discrepancy could be explained by the fact

that the national program of preventive chemotherapy acted in these communities four

weeks before this study. On the other hand, the prevalence in those aged over 19 years,

who were also the least treated group, leads us to reflect that in these communities, the

adult population could constitute a reservoir for infection and re-infection.

In Ecuador, the epidemiological surveillance of soil-transmitted helminth

infections has not been considered either explicitly, nor as part of the group of neglected

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infectious diseases, and the estimated prevalence of infection might be high,[16] but

currently the data are scarce. On the other hand, the Ecuadorian state publishes reports

of its successful health campaigns for the control of neglected diseases such as

brucellosis, Chagas disease, urban rabies, Onchocerciasis, and publicizes the important

increase in the budget for the control of neglected tropical diseases.[29]


Amazonian southern border of Ecuador, in spite of the fact that in recent years member

countries of the Pan American Health Organization have celebrated regional

conventions to address the intensification of control of these poverty-related

diseases.[30]

As a part of intensification of control, the World Health Organization

recommends that school-based deworming programs include health hygiene education

as a complementary measure, although the sustainability and the long-term impact of

such education in hygiene does not appear to show encouraging results. These

limitations in the control and epidemiological surveillance of helminthic infections

could be solved with a long-term, intersectoral multidisciplinary program.[31-32]

Finally, two limitations should be taken into account when interpreting our





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CONCLUSIONS


risk of soil-transmitted helminth infection, despite having reported being subjected to

the administration of preventive chemotherapy during the month prior to the study. For

this reason, it is necessary to conduct holistic studies focusing on communities, and not

simply on captive groups such as school-children, with the object of proposing more

suitable and effective strategies to control such infections.



to the field work of the study.


analyzed the data, and drafted and revised the paper. NRS, MM, CS JP and HSP


provided interpretation of data and revised the paper. COR, DV, CS, JP contributed to

interpretation of the data and revised the paper. NRS, JP, MM and HSP provided

guidance on the conception of the work, interpretation of the data and revised the paper

for content. All members have approved the final version of the manuscript.


Research Programme (I-EO-01-2014).

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REFERENCES

1. Addiss DG. Soil-transmitted helminthiasis: back to the original point. Lancet Infect Dis. 2015 Aug;15(8):871–2.

2. Ojha SC, Jaide C, Jinawath N, Rotjanapan P, Baral P. Geohelminths: public health significance. J Infect Dev Ctries. 2014 Jan;8(1):5–16.

3. Norman FF, Monge-Maillo B, Martínez-Pérez Á, Perez-Molina JA, López-Vélez R. Parasitic infections in travelers and immigrants: part II helminths and ectoparasites. Future Microbiol. 2015;10(1):87–99.

4. Prichard RK, Basáñez M-G, Boatin BA, McCarthy JS, García HH, Yang G-J, et al. A Research Agenda for Helminth Diseases of Humans: Intervention for Control and Elimination. Brooker S, editor. PLoS Negl Trop Dis. 2012 Apr 24;6(4):e1549.

5. Mehta RS, Rodriguez A, Chico M, Guadalupe I, Broncano N, Sandoval C, et al. Maternal geohelminth infections are associated with an increased susceptibility to geohelminth infection in children: a case-control study. PLoS Negl Trop Dis. 2012;6(7):e1753.

6. Malo-Serrano M, Malo-Corral N. Reforma de salud en Ecuador: nunca más el derecho a la salud como un privilegio. Rev Peru Med Exp Salud Publica. 2014 Oct;31(4):754–61.

7. García B, Junior V. Conditional cash transfer a mechanism for social inclusion in Ecuador: An Assessment of Bono de Desarrollo Humano / Programas de transferencias monetarias condicionadas, un mecanismo para la inclusión social en Ecuador: una evaluación del Bono de Desarrollo Humano. 2014 Sep 1 [cited 2016

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Jun 8]; Available from: http://repositorio.educacionsuperior.gob.ec/handle/28000/1408

8. Mosquera GH. Repensar el cuidado a través de la migración internacional: mercado laboral, Estado y familias transnacionales en Ecuador*/Rethinking care through international migration: labour market, State and transnational families in Ecuador. Cuad Relac Laborales. 2012;30(1):139.

9. Instituto Nacional de Estadísticas y Censo. Censo de Población y Vivienda 2010 [Internet]. Available from: http://www.inec.gob.ec/cpv/

10. WHO | PCT databank [Internet]. [cited 2015 Nov 6]. Available from: http://www.who.int/neglected_diseases/preventive_chemotherapy/sth/en/

11. Sánchez-Pérez HJ, Horna–Campos O, Romero-Sandoval N, Consiglio E, Mateo MM. Pulmonary Tuberculosis in Latin America: Patchwork Studies Reveal Inequalities in Its Control–The Cases of Chiapas (Mexico), Chine (Ecuador) and Lima (Peru). 2013 [cited 2013 Sep 6]; Available from: http://cdn.intechopen.com/pdfs/43737/InTech-Pulmonary_tuberculosis_in_latin_america_patchwork_studies_reveal_inequalities_in_its_control_the_cases_of_chiapas_mexico_chine_ecuador_and_lima_peru_.pdf

12. Encuesta de Condiciones de Vida, Ecuador, 2014. Instituto Nacional de Estadísticas y Censo, Ecuador. [cited 2016 Jun 2]. Available from: http://www.ecuadorencifras.gob.ec/documentos/web-inec/ECV/ECV_2015/

13. Romero-Sandoval N, Escobar N, Utzet M, Feijoo-Cid M, Martin M. Sylvatic rabies and the perception of vampire bat activity in communities in the Ecuadorian Amazon. Cad Saúde Pública. 2014 Mar;30(3):669–74.

14. Ortiz-Rico C, Aldaz C, Sánchez HJ, Martin M, Romero-Sandoval N. Conformance contrast testing between rates of pulmonary tuberculosis in Ecuadorian border areas. Salud Publica Mex. 57(6).

15. Committee WE, others. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser. 2002;912:i.

16. Menzies SK, Rodriguez A, Chico M, Sandoval C, Broncano N, Guadalupe I, et al. Risk factors for soil-transmitted helminth infections during the first 3 years of life in the tropics; findings from a birth cohort. PLoS Negl Trop Dis. 2014 Feb;8(2):e2718.

17. Moncayo A-L, Vaca M, Oviedo G, Workman LJ, Chico ME, Platts-Mills T a. E, et al. Effects of geohelminth infection and age on the associations between allergen-

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specific IgE, skin test reactivity and wheeze: a case-control study. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2013 Jan;43(1):60–72.

18. Speich B, Ali SM, Ame SM, Albonico M, Utzinger J, Keiser J. Quality control in the diagnosis of Trichuris trichiura and Ascaris lumbricoides using the Kato-Katz technique: experience from three randomised controlled trials. Parasit Vectors. 2015;8:82.

19. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014 Mar;11(3):e1001620.

20. Bain R, Cronk R, Wright J, Yang H, Slaymaker T, Bartram J. Fecal contamination of drinking-water in low- and middle-income countries: a systematic review and meta-analysis. PLoS Med. 2014 May;11(5):e1001644.

21. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M. Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis. 2013;7(9):e2397.

22. Lo NC, Bogoch II, Blackburn BG, Raso G, N’Goran EK, Coulibaly JT, et al. Comparison of community-wide, integrated mass drug administration strategies for schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness modelling study. Lancet Glob Health. 2015;3(10):e629–e638.

23. Dana D, Mekonnen Z, Emana D, Ayana M, Getachew M, Workneh N, et al. Prevalence and intensity of soil-transmitted helminth infections among pre-school age children in 12 kindergartens in Jimma Town, southwest Ethiopia. Trans R Soc Trop Med Hyg. 2015 Mar;109(3):225–7.

24. Macchioni F, Segundo H, Gabrielli S, Totino V, Gonzales PR, Salazar E, et al. Dramatic decrease in prevalence of soil-transmitted helminths and new insights into intestinal protozoa in children living in the Chaco region, Bolivia. Am J Trop Med Hyg. 2015 Apr;92(4):794–6.

25. Chammartin F, Scholte RGC, Guimarães LH, Tanner M, Utzinger J, Vounatsou P. Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 2013 Jun;13(6):507–18.

26. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.

27. Cepon-Robins TJ, Liebert MA, Gildner TE, Urlacher SS, Colehour AM, Snodgrass JJ, et al. Soil-transmitted helminth prevalence and infection intensity

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among geographically and economically distinct Shuar communities in the Ecuadorian Amazon. J Parasitol. 2014 Oct;100(5):598–607.

28. Nikolay B, Mwandawiro CS, Kihara JH, Okoyo C, Cano J, Mwanje MT, et al. Understanding Heterogeneity in the Impact of National Neglected Tropical Disease Control Programmes: Evidence from School-Based Deworming in Kenya. PLoS Negl Trop Dis. 2015 Sep;9(9):e0004108.

29. Cartelle Gestal M, Holban AM, Escalante S, Cevallos M. Epidemiology of Tropical Neglected Diseases in Ecuador in the Last 20 Years. PloS One. 2015;10(9):e0138311.

30. Thériault FL, Blouin B, Casapía M, Gyorkos TW. Sustaining a hygiene education intervention to prevent and control geohelminth infections at schools in the Peruvian Amazon. 2015 [cited 2016 Jun 15]; Available from: http://iris.paho.org/xmlui/handle/123456789/18385

31. Panic G, Duthaler U, Speich B, Keiser J. Repurposing drugs for the treatment and control of helminth infections. Int J Parasitol Drugs Drug Resist. 2014 Dec;4(3):185–200.

32. Gabrie, J. A., Rueda, M. M., Canales, M., Gyorkos, T. W., & Sanchez, A. L. School hygiene and deworming are key protective factors for reduced transmission of soil-transmitted helminths among schoolchildren in Honduras. Parasites & vectors. 2014;7(1):354.

Figure 1 Distribution of the proportion of households self-identified as indigenous and categorized as poor based on unsatisfied basic needs index* and communities participants.

*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include quality of dwelling materials, access to electricity, kids attendance to school, among others.

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Figure 1 Distribution of the proportion of households self-identified as indigenous and categorized as poor based on unsatisfied basic needs* index and communities participants.

*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include

quality of dwelling materials, access to electricity, kids attendance to school, among others.

297x210mm (299 x 299 DPI)

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confounding

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Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional study in the Amazonian southern

border region of Ecuador

Journal: BMJ Open

Manuscript ID bmjopen-2016-013626.R2


Date Submitted by the Author: 30-Jan-2017

Complete List of Authors: Romero-Sandoval, Natalia; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida; Grups de Reserca d'Amèrica i Africa LLatines, GRAAL Ortiz Rico, Claudia; Universidad Autonoma de Barcelona, Unidad de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Sánchez-Pérez, Hector; El Colegio de la Frontera Sur - ECOSUR; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Valdivieso, Daniel; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida Sandoval, Carlos; Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Parasitología Pástor, Jacob; Instituto Geografico Militar Martin Mateo, Miguel; Universidad Autónoma de Barcelona, Departamento de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL


Public health




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Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional

study in the Amazonian southern border region of Ecuador.







Barcelona, España


México








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Ecuador

Word count: 2935

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Abstract

Background: Rural communities in the Amazonian southern border of Ecuador have

benefited from governmental social programs during the past nine years, which have

addressed, among others, diseases associated with poverty, such as soil-transmitted

helminth infection. The aim of this study was to explore the prevalence of geo-helminth

infection and several factors associated with it in those communities.

Methods: Cross sectional study in two indigenous communities of the Amazonian

southern border of Ecuador. The data were analyzed at both household and individual

levels.

Results: At individual level, the prevalence of geo-helminth infection reached 46.9%

(95% CI 39.5-54.2), with no differences in terms of gender, age, temporary migration

movements, or previous chemoprophylaxis. In 72.9% of the households, one or more

members were infected. Receiving subsidies and overcrowding were associated to

presence of helminths.

Conclusion: The prevalence found of geo-helminth infection was high. Our study

suggests that it is necessary to conduct studies focusing on communities, and not simply

on captive groups such as school-children, with the object of proposing more suitable

and effective strategies to control this problem.


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poverty, shows the situation of geo-helminth infection

• The strategy used involved 80% of the inhabitants and only one of every three

homes were free of geo-helminth infection.

• This study constituted an exercise in community participation, conceived as a

mechanism for achieving greater democracy.


• Collection of a single stool sample may mean that prevalence was

underestimated.

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5

INTRODUCTION







transmitted by walking barefoot on contaminated soil, or by ingestion of larva. [2]

The situation is particularly serious in populations with high rates of migration

and mobility within and between rural and urban communities, and hence these

infections continue to spread.[3]

Since the announcement in 2001[4] of a commitment to eliminate soil-









transfer programs (“human development subsidies”, for instance, subsidies for school

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books, and for school uniforms), aimed to assist people in extreme poverty.[7] On the

other hand, Ecuador has had one of the highest rates of internal and external migration,

including inhabitants of the Amazonian region.[8]


dwellings are considered to be of poor quality (bare earth floor, gaps in house walls,

roof of metal or palm leaves), 55% use water from a well, river or rainwater collection

system, only 22% are connected to a sewage network.[9] These communities, located

approximately 45 km from the nearest urban area and nearest communication center,

until five years ago were only accessible via unpaved roads, and residents could only

get to health facilities and administrative municipal offices via narrow tracks through

the jungle.




from two to five years ought to have received chemoprophylaxis in 2014.[10]

In an effort to increase visibility of health problems in population areas which

are so small that classical studies tend to conceal them, the GRAAL research group

(“Grups de Recerca d’Amèrica i Âfrica Llatines”) conducts studies on

infectious/contagious diseases focusing on vulnerable, and often high-risk, population

groups, often invisible in national level epidemiological analyses. This approach has

been termed patchwork studies.[11]

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several variables of interest.

METHODS






can be reached by road, and are situated around 540 km (10 hours travelling time) from

the capital of Ecuador, Quito.

Figure 1 shows the participating communities and their geographical location, as

well as the joint distribution of the proportion of households self-identified as

indigenous and categorized as poor based on a measure known as the unsatisfied basic

needs index. These communities are located in the Amazon border which is one of the

two Ecuadorian areas with more poverty among the indigenous population.[12]



sylvatic rabies,[13,14] we administered a questionnaire (face-to-face) to identify

dwellings and obtain household characteristics, including presence or absence of water

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supply and sanitary toilets, whether households boil water for consumption,

overcrowding, whether they received any subsidy. At individual level we recorded

temporary migratory movements, self-perceived presence of geohelminths in the last

month and whether they had received preventive chemotherapy – something which

could only be ascertained for the last month, due to problems in the recording of

information about administration of chemoprophylaxis in the studied communities. The

medication (Albendazol 400 mg one dose) was provided by the Ecuador Ministry of

Public Health. For children aged under eight years, the questions were answered by the

mother or guardian.

One direct fecal sample was collected from each participant. All samples (192)

were examined using direct observation, 178 samples by Kato-Katz technique, and 184

by formol-ether concentration; in both the latter cases, missing data corresponds to

samples that were insufficient to permit their being assessed. A positive sample was

defined by the presence of at least one egg or larva being detected by any one of the

three methods. Direct observation and the Kato-Katz method were used to assess

samples on the same day on site, in the communities, with a mobile parasitological

analysis laboratory installed there. Kato-Katz technique was performed with a template

of 41.7 mg, as recommended by the WHO.[15] Samples were preserved in formol-ether

and an analysis of this concentrate was performed at a base laboratory. All three

techniques have been used by other studies in Ecuador.[16,17]



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999 epg, 1000 – 9999 epg, and >= 10000 epg.[18]

RESULTS












All inhabitants use natural spring-water, which is piped to community tanks

without any type of treatment; nobody had toilets. Other sanitary and/or socioeconomic

deficiencies were observed in 49.2% of households (bare earth floor, windows not

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covered, no wastewater disposal system, no electricity, absence of own drinking water

supply), and in 79.3% (23/29) of these, at least one member was infected by

geohelminths; in a similar fashion, among households with better conditions, 66.7%

(20/30) presented one or more infected members (PR 1.19; 95% CI 0.86-1.67).









CI 53.3-73.8) (PR 1.22; 95% CI 0.88-1.88).


The mean age was 22.8 (SD 19.4) years, while percentile 25 corresponded to 8 years,

percentile 50 to 14 years, and percentile 75 to 38 years (range 76). The median ages for

males and females were 10 and 18 years, respectively (p<0.05); 37% of working-age

men reported having to migrate for work-related reasons (hunting, agriculture, mine-

work), tending to be away for 8 to 15 days, or even more.



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temporarily going away from their communities, geohelminthiasis was found in 51.7%


figure was 44.4% (95% CI 37.3-52.0).






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between perception of parasites and age, with older ages reporting a lower perception

(80.0% to 48.1%) (p<0.05).


Age group (years)



N (%)

95% CI n (%)

95% CI

2-5 15/29 24/30 51.7 34.5-69.0 80.0 63.3-93.3 6-19 39/80 51/85 48.8 37.5-58.8 60.0 49.4-70.6 ≥20 40/68 37/77 58.8 47.1-70.6 48.1 36.4-59.7

In the last month 57.8% of the participants reported having received preventive

chemotherapy; in the group aged 2 to 5 years, having received preventive chemotherapy

in the last month was declared by 25/30 participants (83.3%); 56/85 (65.9%) in the

group aged 6 to 19 years, and 30/77 (39.0%) in the group aged 20 years and over (LR

22.37 p<0.05). This association was also linear (p<0.05).




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sex or age group.










DISCUSSION

In this study we found that 72.9% of households had at least one person infected

by soil-transmitted helminthiasis, and in 13% all members were infected. Also we found

a higher prevalence among households stating they did not boil water; or presented

overcrowding, as well as families receiving any kind of state subsidy, thus suggesting

their worse sanitary conditions and greater poverty.

In marginalized populations, lacking sanitary conditions, one form of treating

water for human consumption, in the home, is by boiling it, thus preventing its

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contamination through contact with unwashed hands, dust rising from the bare earth

floor, etc., even though the effectiveness of boiling may be questionable.[19]

This is an important aspect to consider because our results show that community

de-worming campaigns (57.8% received chemoprophylaxis in the last month) aiming to

reduce or avoid soil-transmitted helminthiasis, without health education, are not

sufficient, and must be accompanied by changes in sanitary conditions and poverty

reduction policies and actions. In this sense, the lack of good water supplies and the

inadequate basic sanitation observed during the fieldwork, as well as a low participation

of the communities themselves in basic sanitation activities, could both be factors that

impede the control of soil-transmitted helminth infections.[20–22]



to confirm that it is not enough to treat this problem merely as a medical condition, and

that it is necessary to improve the socioeconomic and sanitary conditions of the

population. At individual level, the high prevalence found was not differentiated by

gender, age group, temporary migratory movement, nor by whether they had received

chemoprophylaxis or not, this latter aspect being seen as a reflection of the community's

situation, and not necessarily as an assessment of the efficacy of the chemoprophylaxis

program of the Public Health Ministry.



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concentrate), there are few references with which we can compare our findings, since

the majority of studies are conducted in “captive” populations, such as school-

children.[23-25]

The prevalence found in this study is much higher than figures reported by several

articles available in the scientific literature that deal with the Ecuadorian situation –with

an average prevalence of 18.9%[26,27], which formed part of a meta-analysis based on

all publications related to prevalence of soil-transmitted helminth infection in South






of geohelminthiasis, particularly for children under 5 years of age, since in nearly 8 of

every ten cases, the mother or guardian who responded perceived the presence of

parasites, whereas our findings halve this figure. This discrepancy could be explained

by the fact that the national program of preventive chemotherapy acted in these

communities four weeks before this study. On the other hand, the prevalence in those

aged over 19 years, who were also the least treated group, leads us to reflect that in

these communities, the adult population could constitute a reservoir for infection and re-

infection.

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In Ecuador, epidemiological surveillance of soil-transmitted helminth infections

has not been considered either explicitly, nor as part of the group of neglected infectious

diseases, and although the estimated prevalence of infection is high,[16] currently the

data are scarce. On the other hand, the Ecuadorian state publishes reports of its

successful health campaigns for the control of neglected diseases such as brucellosis,

Chagas disease, urban rabies, Onchocerciasis, and publicizes the important increase in

the budget for the control of neglected tropical diseases.[29]


Amazonian southern border of Ecuador, in spite of the fact that in recent years member

countries of the Pan American Health Organization have celebrated regional

conventions to address the intensification of control of these poverty-related

diseases.[30]

As part of this intensification of control, the World Health Organization

recommends that school-based deworming programs include health hygiene education

as a complementary measure, although the sustainability and the long-term impact of

such education in hygiene does not appear to show encouraging results. These

limitations in the control and epidemiological surveillance of helminthic infections

could be solved with a long-term, intersectoral multidisciplinary program.[31-32]

Finally, two limitations should be taken into account when interpreting our



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CONCLUSIONS


risk of soil-transmitted helminth infection, despite having reported receiving preventive

chemotherapy during the month prior to the study. For this reason, it is necessary to

conduct holistic studies focusing on communities, and not simply on captive groups

such as school-children, with the object of proposing more suitable and effective

strategies to control such infections.



to the field work of the study. Our thanks to Dave Macfarlane for help in developing the

english language version of this article.


analyzed the data, and drafted and revised the paper. NRS, MM, CS, JP and HSP


provided interpretation of data and reviewed the paper. COR, DV, CS, and JP

contributed to interpretation of the data and reviewed the paper. NRS, JP, MM and HSP

provided guidance on the conception of the work, interpretation of the data and

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reviewed the paper for content. All members have approved the final version of the

manuscript.


Research Programme (I-EO-01-2014).







REFERENCES

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8. Mosquera GH. Repensar el cuidado a través de la migración internacional: mercado laboral, Estado y familias transnacionales en Ecuador*/Rethinking care through international migration: labour market, State and transnational families in Ecuador. Cuad Relac Laborales. 2012;30(1):139.

9. Instituto Nacional de Estadísticas y Censo. Censo de Población y Vivienda 2010 [Internet]. Available from: http://www.inec.gob.ec/cpv/

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12. Encuesta de Condiciones de Vida, Ecuador, 2014. Instituto Nacional de Estadísticas y Censo, Ecuador. http://www.ecuadorencifras.gob.ec/documentos/web-inec/ECV/ECV_2015/ (accessed 2 jun 2016).

13. Romero-Sandoval N, Escobar N, Utzet M, Feijoo-Cid M, Martin M. Sylvatic rabies and the perception of vampire bat activity in communities in the Ecuadorian Amazon. Cad Saúde Pública. 2014 Mar;30(3):669–74.

14. Ortiz-Rico C, Aldaz C, Sánchez HJ, Martin M, Romero-Sandoval N. Conformance contrast testing between rates of pulmonary tuberculosis in Ecuadorian border areas. Salud Publica Mex. 57(6).

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17. Moncayo A-L, Vaca M, Oviedo G, Workman LJ, Chico ME, Platts-Mills T a. E, et al. Effects of geohelminth infection and age on the associations between allergen-specific IgE, skin test reactivity and wheeze: a case-control study. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2013 Jan;43(1):60–72.

18. Speich B, Ali SM, Ame SM, Albonico M, Utzinger J, Keiser J. Quality control in the diagnosis of Trichuris trichiura and Ascaris lumbricoides using the Kato-Katz technique: experience from three randomised controlled trials. Parasit Vectors. 2015;8:82.

19. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014 Mar;11(3):e1001620.

20. Bain R, Cronk R, Wright J, Yang H, Slaymaker T, Bartram J. Fecal contamination of drinking-water in low- and middle-income countries: a systematic review and meta-analysis. PLoS Med. 2014 May;11(5):e1001644.

21. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M. Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis. 2013;7(9):e2397.

22. Lo NC, Bogoch II, Blackburn BG, Raso G, N’Goran EK, Coulibaly JT, et al. Comparison of community-wide, integrated mass drug administration strategies for schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness modelling study. Lancet Glob Health. 2015;3(10):e629–e638.

23. Dana D, Mekonnen Z, Emana D, Ayana M, Getachew M, Workneh N, et al. Prevalence and intensity of soil-transmitted helminth infections among pre-school age children in 12 kindergartens in Jimma Town, southwest Ethiopia. Trans R Soc Trop Med Hyg. 2015 Mar;109(3):225–7.

24. Macchioni F, Segundo H, Gabrielli S, Totino V, Gonzales PR, Salazar E, et al. Dramatic decrease in prevalence of soil-transmitted helminths and new insights into intestinal protozoa in children living in the Chaco region, Bolivia. Am J Trop Med Hyg. 2015 Apr;92(4):794–6.

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25. Chammartin F, Scholte RGC, Guimarães LH, Tanner M, Utzinger J, Vounatsou P. Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 2013 Jun;13(6):507–18.

26. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.

27. Cepon-Robins TJ, Liebert MA, Gildner TE, Urlacher SS, Colehour AM, Snodgrass JJ, et al. Soil-transmitted helminth prevalence and infection intensity among geographically and economically distinct Shuar communities in the Ecuadorian Amazon. J Parasitol. 2014 Oct;100(5):598–607.

28. Nikolay B, Mwandawiro CS, Kihara JH, Okoyo C, Cano J, Mwanje MT, et al. Understanding Heterogeneity in the Impact of National Neglected Tropical Disease Control Programmes: Evidence from School-Based Deworming in Kenya. PLoS Negl Trop Dis. 2015 Sep;9(9):e0004108.

29. Cartelle Gestal M, Holban AM, Escalante S, Cevallos M. Epidemiology of Tropical Neglected Diseases in Ecuador in the Last 20 Years. PloS One. 2015;10(9):e0138311.

30. Thériault FL, Blouin B, Casapía M, Gyorkos TW. Sustaining a hygiene education intervention to prevent and control geohelminth infections at schools in the Peruvian Amazon. 2015 [cited 2016 Jun 15]; Available from: http://iris.paho.org/xmlui/handle/123456789/18385

31. Panic G, Duthaler U, Speich B, Keiser J. Repurposing drugs for the treatment and control of helminth infections. Int J Parasitol Drugs Drug Resist. 2014 Dec;4(3):185–200.

32. Gabrie, J. A., Rueda, M. M., Canales, M., Gyorkos, T. W., & Sanchez, A. L. School hygiene and deworming are key protective factors for reduced transmission of soil-transmitted helminths among schoolchildren in Honduras. Parasites & vectors. 2014;7(1):354.

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*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include quality of dwelling materials, access to electricity, kids attendance to school, among others.

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*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include

quality of dwelling materials, access to electricity, kids attendance to school, among others.

210x148mm (300 x 300 DPI)

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1


Item

No

Recommendation Pg


abstract

3



3

Introduction


reported

5


Methods




7








7





-



8

Data sources/

measurement




8





7-8


confounding

9



10






-


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Results Pg




-



Descriptive

data



9-10






-





9-12




-



-

Discussion




14,16



13-

16


Other information



17








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