A qualitative assessment tool for the potential of

infectious disease emergence and spread

V.E. Bridges *, J. Akkina, J. Grannis, C. Johnson,R. Johnson, C. Tuszynski

US Department of Agriculture, Centers for Epidemiology and Animal Health, Center for Emerging Issues,

2150 Centre Avenue, Bldg B, Fort Collins, CO 80526, USA

Abstract

Improved understanding and assessment of the complex factors associated with disease emer-

gence and spread will lead to better management and thus reduction of risk for disease occurrence.

Specific biological, ecologic, environmental, and societal factors have been identified that precede

emerging infections. Based on these factors, a qualitative tool was developed to assess risk for disease

emergence and spread. Within this tool, three separate assessment elements were developed: novel

disease evolution, pathways by which a disease agent could be introduced into a country, and

domestic spread from the location of introduction or evolution. Risk factors identified for each of the

three elements consist of specific descriptions of production practices, consumer demand, trade,

health conditions, and environmental conditions, and are categorized as primary or secondary. Using

this tool, those factors contributing greatest to risk of disease emergence can be identified and

targeted for mitigation. In addition, risk can be monitored over time, focusing on factors that are

primary or that have the greatest potential for increasing disease emergence risk.

Published by Elsevier B.V.

Keywords: Factors for disease emergence; Qualitative risk assessment; Emerging disease; Risk factor

www.elsevier.com/locate/prevetmed

Preventive Veterinary Medicine 81 (2007) 80–91

* Corresponding author at: USDA, Centers for Epidemiology and Animal Health, 2150 Centre Avenue, Bldg B,

Fort Collins, CO 80526, USA. Tel.: +1 970 494 7000.

E-mail address: Victoria.E.Bridges@aphis.usda.gov (V.E. Bridges).

0167-5877/$ – see front matter. Published by Elsevier B.V.

doi:10.1016/j.prevetmed.2007.04.008

1. Introduction

Emerging infectious diseases are those diseases that have newly appeared in a

population or have previously existed but are evolving or increasing in incidence or

geographic range. Emerging infectious diseases have impacted animal and human health in

recent decades, demonstrated by bovine spongiform encephalopathy, variant Creutzfeldt–

Jakob Disease (vCJD), West Nile virus, hendra virus, and nipah virus, among others. New

diseases will continue to emerge and impact animal and public health, along with the

economic well-being of countries throughout the world (Brown, 2004; King et al., 2004).

Disease emergence can occur through evolution of pathogens or introduction of existing

pathogens or hosts to a new location, followed by establishment and spread. Pathogen

evolution is driven by biological, ecological, environmental, and societal factors, such as

those which put adaptive and selective pressure on microbes and hosts. Introduction of

agents, hosts, or vectors into new settings (including intra-country spread as well as

transboundry spread) is promoted through ecological and environmental changes,

migration, trade, and travel (Lederberg et al., 1992; Morse, 1995; Smolinski et al., 2003).

Current methodologies for pathways analysis and risk assessment focus on predicting

the likelihood of movement of known diseases to new locations. However, to be able to

prevent or decrease the frequency of emerging disease occurrence, a method to predict

emergence and movement of novel or evolving diseases is needed. New approaches are

needed to accomplish this. Numerous authors have suggested utilizing the biological,

ecological, environmental, and/or societal factors associated with disease emergence as a

way to improve prediction; however, interactions among these emergence factors can be

complex making modeling difficult (Linthicum et al., 1990; Wilson et al., 1994; Myers

et al., 2000). Attempts to date have focused on predicting the potential movement of known

vector-borne diseases, such as Rift Valley fever, by examining climate and ecological

factors (Linthicum et al., 1990; Myers et al., 2000).

The goal of this project was to develop a method utilizing information on risk factors

which could assess disease emergence potential for an industry. The focus of the project

was, therefore, to assess an industry’s overall likelihood of disease emergence rather than

assessing the likelihood of emergence of a particular disease. Such a tool could be used by

industry and government officials to identify areas of vulnerability and to effectively target

mitigation measures, thus making the industry more resistant to disease emergence. The

tool could also be used to monitor how changes in the dynamics associated with an industry

increase or decrease potential for disease emergence over time.

2. Material and methods

As a first step to building a disease emergence risk assessment tool, the food fish portion

of the U.S. aquaculture industry was chosen to help provide focus and specificity during the

development of the method. It was then necessary to develop an understanding of the

dynamics associated with the industry being assessed and how those dynamics might

impact disease emergence. Within the food fish portion of the aquaculture industry, nine

broad areas were examined: agent/host/vector biology, ecology/environment/climate,

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economics/industry, health management, international trade, politics/regulations, produc-

tion practices, social/cultural, and technology. These broad areas of focus were identified

based on existing literature on forces for disease emergence (Lederberg et al., 1992; Morse,

1995; Smolinski et al., 2003).

Identification of individual risk factors to include in the risk assessment tool was based

on research of the industry, forces for disease emergence, and the interaction of these forces

with the industry. Research was conducted to determine specific risk factors for disease

emergence which might exist within these broad areas of focus. This research included

gathering detailed information in each of the nine areas for the food fish aquaculture

industry in general and for several species-specific sectors within the industry. Sources

used to identify risk factors for disease emergence within the industry included published

literature such as journals, industry publications, and government publications, as well as

discussions with industry experts and site visits to production facilities. Additionally, risk

factors were identified based on standard epidemiologic principles and known risk factors

for transmission and spread of diseases.

Based on the research conducted, general risk factors were made specific to the

aquaculture industry. For example, direct contact with other species is a general risk factor

for disease emergence as it provides opportunity for transfer and mixing of pathogens and

micro-organisms in general. This risk factor was tailored to the aquaculture industry by

focusing on the amount of polyculture practiced. Polyculture is the production of multiple

aquatic species in a single aquaculture environment, including species which may or may

not naturally coexist together in the wild, and provides the opportunity for transfer and

mixing of micro-organisms. Utilization of waste products from fish or other species for

fertilization of aquaculture ponds is another example of a specific risk factor for disease

emergence in the aquaculture industry that falls under the broader economics/industry

category of forces for disease emergence.

Factors ultimately included in the assessment were those which were identifiable and

measurable. In some cases, specific information on an important factor was not found and a

proxy factor had to be used. An example of this use of a proxy factor is the use of import

value rather than volume. This was required since import data do not provide volume data

broken out by species. A more complex example of the use of a proxy factor is one

addressing the issue of changing consumer demand. Increased consumer demand over a

short period of time can result in changes in the supply chain that result in higher disease

emergence risk; however, data quantifying consumer demand of various species of

aquacultured food fish were not available for this assessment. The proxy risk factor

developed measured recent changes in imports of live food fish. An increasing rate of

change in such imports indicates higher demand for the products and may be a signal that

aquaculture production, for those species that can be aquacultured, may be increasing in

the importing country or that new importers with little experience may be entering the

market. These importers may try to increase their import volume quickly without

appropriate expansion of infrastructure and without attention to best management practices

to ensure healthy and fresh product delivery.

Developing this disease emergence risk assessment tool required aligning potential

emergence risk factors identified through industry research into a structured model which

allowed completion of a qualitative risk assessment. Upon the identification of specific risk

V.E. Bridges et al. / Preventive Veterinary Medicine 81 (2007) 80–9182

factors, definitions for level of risk (high, medium, low, no defined risk) were developed for

each factor. These risk levels allow the specific attributes associated with industry sectors to

be captured and applied to each factor. For example, for the risk factor assessing broodstock

source, the low risk level is defined as the industry using domesticated broodstock while high

risk is associated with the use of wild caught fish as broodstock. For this risk factor, no defined

risk is not an applicable risk level. Criteria for the definition of each level of risk for each

factor was based on the previously mentioned research and the epidemiological expertise of

the authors, vetted by consensus expert opinion from industry experts. Each risk factor’s

criteria are documented in full in the risk assessment documentation.

Within the assessment tool, disease emergence is separated into three distinct elements:

disease evolution, pathways, and spread. The identified risk factors within these three

elements were determined to be primary or secondary risk factors, based on defined criteria,

as well as being classified into one of six risk factor categories (agent/host/vector biology,

ecology/environment/climate, economics/industry, health management, politics/regulations,

social/cultural). These six risk factor categories were synthesized from the original nine

broad areas of research for forces of disease emergence into the structured model.

The full process, from the initial researching of forces for disease emergence to the final

output tables developed upon application of the methodology, is summarized in Fig. 1.

3. Results

3.1. Disease emergence elements

Risk factors were organized into three disease emergence elements: disease evolution,

pathways, and spread. Table 1 provides examples of risk factors within each of the three

disease emergence elements, organized by category of force for disease emergence.

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Fig. 1. Process used for methodology development, from initial research of forces for disease emergence to final

output tables.

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Table 1

Examples of risk factors by category and by element

Agent/host/vector biology Ecology/environment/climate Economics/industry Health management Social/cultural Politics/regulations

Disease evolution element

Existing disease burden

in the industry

Latitude at which

production takes

place

Rate of change

in production volume

Use of drugs, chemicals,

and vaccines in industry

Commercial production

of new species

Treatment of

discharge water

Length of lifecycles Occurrence of major

weather disasters

Broodstock source Overall level of health

management

Total imports of live

food fish during most

recent year

–

Pathways element

Presence of OIE listed

diseases in country

from which largest

share of imports of

live fish originate

Ballast water dumping

in assessed country

Imports of fish feed

containing fish products

during most recent year

– Total imports of all live

food finfish during most

recent year

Regulatory

infrastructure

regarding

importations

Presence of OIE listed

diseases in country

from which largest

share of imports

of non-live fish

originate

Migratory and

predatory birds

– – Geographic diversity from

which imports of whole

food fish originate

Imports of used

aquaculture

production

equipment

Spread element

– Level of stocking in

lakes and streams

Movement of fish during

production cycle

Disease management

practices used in the

industry

Types of sales of products

from farms

State regulations

regarding hauling

of fish

– Movements of fish caused

by predation or major

weather events

Content and processing

of feed fed

Handling of mortalities – Treatment of

discharge water

The disease evolution element examines the domestic potential for novel pathogens to

develop or for existing pathogens to evolve. Risk factors associated with disease evolution

include those associated with altering the environment, stressing the host, and bringing the

assessed species in contact with microbes or other species. For disease evolution, trade

related risk factors are included to capture the opportunity importation presents for mixing

of microbes and hosts in new settings, which can lead to pathogen evolution.

Risk factors included in the pathways element address avenues by which a new or

existing pathogen can enter the country being assessed. International trade risk factors

represent the majority of factors in this element, incorporating both overall volume and rate

of change in volume of relevant imports. The overall volume of trade indicates the size of

the ‘‘pipeline’’ of product entering a country, while a rapid rate of change in trade volume

may indicate the potential for new buyers and sellers entering the marketplace or the

potential for the assessed species to be sourced from new countries to meet changing

demand.

The spread element examines the potential for newly emerged, evolved, or introduced

pathogens to spread domestically from that point of emergence, evolution, or introduction.

Risk factors associated with spread are those which specifically relate to the movement of

the host species or of pathogens within the country being assessed.

This methodology did not include an assessment of impact to the industry upon disease

emergence or spread. It should also be noted that not all categories of forces for disease

emergence are represented within each element (Table 1). For example, the category of

health management has no risk factors in the pathways element as factors in this category

do not play a direct role in the movement of pathogens from one country to another, after

that pathogen has emerged in the exporting country. Health management risk factors do

however play roles in both the disease evolution and spread elements.

3.2. Levels of risk

For each factor within each element, definitions were developed to determine the level of

risk attributable to that factor within the industry being assessed. Levels of risk included are

high, medium, low, and no defined risk. These risk rankings allow specific attributes

associated with industry sectors to be captured and taken into account within each risk factor.

Defined levels of risk for several risk factors are shown in Table 2 as examples. This table also

shows the category of force for disease emergence for each example factor. In general, if a risk

factor is used in multiple elements, e.g. in both the disease evolution element and the spread

element, the level of risk is assessed using the same definition across elements.

In addition to each factor being given a risk ranking, factors were determined to be

primary or secondary, indicating level of contribution to overall risk, independent of the

outcome of the risk ranking (Table 3). Specific criteria were developed to make this

determination of primary or secondary for each of the three elements. Within the evolution

element, at least one of three criteria had to be present for the factor to be classified as

primary. These three criteria are that the risk factor provides evidence that: pathogens are

present in the farmed host; definite interaction or mixing of pathogens/microbes and hosts

takes place; or definite interaction or mixing of multiple host species takes place. Of the 30

evolution element risk factors, six were classified as primary.

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Table 2

Examples of risk factors by element and by category, with definitions of risk level

Factor Risk factor category Definition of risk level

High Medium Low No defined risk

Disease evolution element

Brood stock source Economics/industry Wild caught Mixed source Domesticated breeding N/A

Pathways element

Total imports of all live

food finfish during

most recent year

Social/cultural Import value 50%

or greater of world

imports

Import value 5% or more

of world imports, but less

than 50%

Import value less than

5% of world imports

No imports

Spread element

Movement of fish due to

predation and major

weather events

Ecology/environment/

climate

Greater than 75% of industry

uses open production

systems, e.g. mariculture,

raceways, uncovered ponds

The industry uses open and

closed production systems

and does not meet the

criteria for a high or low

risk level

Greater than 75% of

industry uses closed

production systems,

e.g. RAS

N/A

One or both of the following criteria had to be present for a factor within the pathways

element to be classified as primary: demonstrates movement of live fish from one country

to another; or direct evidence of presence of pathogens in exporting country. Eight of the 14

pathways element risk factors were determined to be primary. Within the spread element,

unregulated movement of live fish takes place and direct contact between host and

pathogen/microbe are the two criteria, at least one of which must be present for a risk factor

to be classified as primary. Six of the 15 risk factors were identified as primary within the

spread element.

This table also shows the category of force for disease emergence for each example

factor.

The analyst is provided with a predefined structure to the output table, with the risk

factors already classified as primary or secondary, and organized by element. Upon

application of this qualitative assessment process, the analyst then has a completed table of

approximately 60 risk factors which have been ranked from high risk to no defined risk,

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Table 3

Examples of risk factors, primary and secondary, by element

Primary risk factors Secondary risk factors

Disease evolution element

Reported aquaculture disease burden Length of lifecycle

Brood stock source Geographic concentration of production

Content/processing of feed fed Recent change in production volume

Polyculture Level of health management

Waste fertilization Treatment of discharge water

Quality of source water Commercial production of a new species

Pathways element

Presence of OIE listed diseases in country

from which the largest share of live fish

imports originate

Presence of OIE listed diseases in country

from which largest share of non-live

imports originate

Ballast water dumping in assessed country Migratory and predatory birds

Total import value of live food fish during

most recent year

Recent imports of fish feed containing fish products

Rate of change in imports of live food fish Imports of used aquaculture production equipment

Imports of live ornamental fish during

most recent year

Geographic diversity of origination of imports of

whole food finfish and shellfish

Geographic diversity of imports of live fish

(including ornamentals)

Total imports of non-live food finfish and shellfish

during most recent year

Regulatory infrastructure regarding importations

Spread element

Unintentional movement of fish due to predation

and major weather events

Geographic concentration of production

Intentional movement of fish within and

between farms

Production system used

Types of sales of products from farm Treatment of discharge water

Content/processing of feed fed Rate of change in production volume

Quality of source water Disease management practices

State regulations regarding live hauling Handling of mortalities

along with the justification for each factor’s ranking. From these results, the analyst can

produce a summary report, assessing the industry’s susceptibility to disease emergence, as

well as identifying specific areas of highest or lowest risk within that industry.

4. Discussion

This project explored the potential for assessing ‘‘riskiness’’ of an industry for disease

emergence via a structured qualitative risk assessment tool. The approach sought to model

disease emergence potential based on risk factors in the six broad categories of agent/host/

vector biology, ecology/environment/climate, economics/industry, health management,

politics/regulations, and social/cultural. There is limited previous work in this area of

disease emergence assessment on which to draw and scientific studies outlining the

contribution of individual factors to disease emergence are few. This necessitated

significant development of methodology.

4.1. Risk factors

Rather than trying to be all-inclusive, risk factors included in the assessment were those

which were identifiable, measurable, and significant. A number of potentially important

risk factors could not be assessed due to data limitations. Factors related to ecology/

environment/climate posed particular challenges and the impacts of ecology/environment/

climate changes are likely not fully captured in the current risk assessment tool. In some

cases, specific information on an important factor was not found; however, a proxy factor

was identified and/or proxy data were found that were deemed to be usable. In other cases,

important risk factors could not be included in the assessment tool at all because they were

not measurable and an appropriate proxy could not be determined. Smuggling or theft of

fish and producers changing to new species production within an existing farm are two

examples of such risk factors. These difficulties are not unique to the aquaculture industry

and it is anticipated that such difficulties and lack of data would be encountered when

assessing other animal industries. Such immeasurable factors were documented, even

though they were not considered usable at this point in time. In the future, data may become

available allowing for some of these important risk factors to be included and for less use of

proxy measurement.

Several challenges arose in utilizing trade data. For important products such as live fish

imports, only data on value, not volume, were available. The absence of volume data likely

results from live fish being imported in water, with the fish themselves often being difficult

to count. From a risk perspective, volume is more important than value as changes in value

can be related to price changes with or without simultaneous volume changes. Another

challenge with trade data is that species-specific data were unavailable for some species,

which resulted in a greater amount of assessment taking place at the country level rather

than at the species level. For example, in the U.S. trade data, specific information is

available at the species level for salmon. Catfish, however, fall into a generic category such

as ‘‘freshwater fish’’, though imports into the U.S. of various species of catfish are known to

take place. The lack of species-specific import data and the necessity of using value rather

V.E. Bridges et al. / Preventive Veterinary Medicine 81 (2007) 80–9188

than volume results in less precision in the assessment tool. Quality and specificity of trade

data varies by species. Data for livestock species such as cattle and swine are more detailed

and species-specific than those for fish, therefore these issues would likely be less

significant when assessing other species. Additionally, the issue of lack of volume based

import data would be less of an issue when assessing terrestrial animal species.

As previously discussed, the focus of this project was at the industry level to assess an

industry’s overall likelihood of disease emergence, rather than assessing the likelihood of

disease emergence at the individual farm level. Therefore, most of the factors included in

the disease evolution element and spread element are measured at the industry sector level

(specific to the species being assessed). They are not measured at the individual farm level.

A few factors within these two elements are measured at the country level. Measurement at

the country level denotes the shared risk faced by all aquacultured species associated with

these particular risk factors. For example, production of a new species within a country

poses a level of risk which is shared by all species aquacultured in that country. Conversely,

all of the risk factors included in the pathways element are measured at the country level.

This is due primarily to lack of specificity in trade data as discussed above. It is also a

reflection of disease susceptibility across closely related aquacultured species and that

most of the identified risk factors in the pathways element apply across species.

4.2. Utilization of results

There are a number of ways in which the results gained from application of this disease

emergence risk assessment tool can be utilized. The tool can be used to monitor risk for

each emergence element for each industry sector over time through periodically repeating

the assessment. In this way, changes in the disease emergence elements can be monitored to

determine if the industry’s level of susceptibility to disease emergence is increasing or

decreasing. Alternatively, a subset of risk factors could be selected for monitoring. For

example, only those risk factors which contribute the greatest to overall risk (i.e. primary

risk factors) could be monitored. Monitoring systems could also be established for those

primary risk factors which currently received a rank of low risk, thus watching for changes

which could result in greater risk of disease emergence. These types of monitoring

activities could be part of an emerging disease early warning system which would alert

industry and government officials of rising risk for disease emergence. Upon such alerts,

actions could be taken to decrease that rising level of risk. An example of such action might

be to target educational campaigns to producers regarding identified risky behavior such as

improper handling of mortalities, lack of use of veterinary care, or improper movement of

animals.

Another use of the results of this qualitative assessment tool could be to determine

potential foci for risk mitigation efforts. By examining those risk factors which contribute

significantly to risk, industry and government officials can explore potential mitigations

that would have the greatest impact. Those risk factors which are both primary factors and

received a high risk ranking could be evaluated for appropriateness of implementing

mitigation efforts. As an example, lack of regulations regarding live hauling of fish is a risk

factor which is feasible to take action on and such action would decrease risk. In

comparison, length of lifecycle and occurrence of major weather disasters are risk factors

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for which little can be done to mitigate the risk they bring to the industry. In considering

potential mitigations, economics, logistical feasibility, and other considerations have to be

taken into account. By applying the tool in this way, an industry can focus mitigation

efforts to maximize risk reduction potential in a practical and realistic manner.

A final use of the results gained from applying the disease emergence tool is to identify

information and data gaps within an industry. Knowledge of where these gaps lie, and the

impact they have on risk, can be used to direct research funding and data collection efforts.

As an example, one such information gap identified during this project was lack of data

regarding consumer demand for specific species of fish. Such information would be

valuable as it indicates demand drivers impacting production behaviors and thus risk of

disease emergence. Information and data gaps regarding risk factors that have significant

impact to the industry should receive highest priority.

4.3. Application to other industries

The food fish portion of the aquaculture industry in the U.S. was chosen to be used in the

development of this risk assessment tool. In applying the tool to several aquaculture

species, it became evident that while many of the identified risk factors are non-species

specific and would be relevant when assessing the potential for disease emergence in any

animal industry, including terrestrial species, some of the identified risk factors are specific

to the aquaculture industry. Therefore, while this assessment tool provides the basic

framework and would be a good starting place to assess other animal industries, the

individual risk factors would have to be altered to make it applicable. However, it is

believed that the overall process developed, from the beginning research of forces for

disease emergence for the species being assessed to the final ranking and classification of

risk factors, is a sound one and one which is not specific to aquaculture species.

5. Conclusion

The disease emergence risk assessment tool developed in this project was able to rank

risk across three emergence elements for multiple aquaculture sectors. The usefulness of

the results to industry and government officials for understanding the level of risk

associated with different aquaculture sectors and potential risk mitigations needs to be

evaluated. The tool’s predictive capabilities will need to be assessed over time, as well as

the tool’s ability to identify changes in risk based on changes in industry dynamics. As this

is done, and as the tool is utilized to a greater extent, it is expected that additions, deletions,

and clarifications to the risk factors will be made over time, as is the natural maturation of

any new methodology.

In developing this disease emergence assessment tool, several challenges to defining

and assessing risk factors were encountered. Data availability was the primary such

challenge and expert opinion was relied on heavily, especially for the smaller aquaculture

industry sectors where published statistics were difficult to obtain. Another challenge was

in the development of the risk factors themselves. Were all the relevant risk factors

identified and included? Were risk factors included that should not have been? Further

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review by industry experts and application of the tool over time will answer these questions

and allow further refinements in the identified risk factors.

Understanding the risks associated with industry sectors can allow mitigation measures

to be considered and enacted, reducing risk for disease emergence. While further

refinement and evaluation is needed, this qualitative risk assessment method shows

promise of being a helpful tool for government and industry use to monitor potential for

disease emergence and to target mitigation efforts in an efficient and effective manner, thus

decreasing risk of disease emergence.

Acknowledgements

The authors would like to thank the following people for providing their industry

expertise to the development of this project: Stephen K. Ellis (USDA), Kevin M.

Fitzsimmons (University of Arizona), Donald V. Lightner (University of Arizona), Jill B.

Rolland (USDA), Bruce A. Wagner (USDA). We would also like to thank the U.S. Animal

Health Association’s Aquaculture Committee which was used as a sounding board

throughout the methods development process and Kamina Johnson for her research

assistance and development of visuals.

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