Preventive Veterinary Medicine 48 (2001) 261271

International trade, animal health and veterinary

epidemiology: challenges and opportunities
C. Zepedaa,*, M. Salmana, R. Ruppannerb
a
Center for Veterinary Epidemiology and Disease Surveillance Systems, College of Veterinary Medicine and
Biomedical Sciences, Colorado State University, Fort Collins, CO 80523, USA
b
INRS-Institut Armand-Frappier, Universite du Quebec, Laval, QC, Canada H7V 1B7
Accepted 20 September 2000

Abstract

The link between international trade, animal health and epidemiology has been recognized for a
long time and has taken an additional importance in the aftermath of the Uruguay Round of
Multilateral Trade Negotiations of the General Agreement on Tariffs and Trade (GATT) and of the
inception of the World Trade Organization. The Agreement on the Application of Sanitary and
Phytosanitary Measures of the World Trade Organization demands that sanitary and phytosanitary
measures be scientifically based, placing epidemiology at the center of decisions related animal
health and trade. This paper analyses the interactions between international trade of animals (and
animal products) and epidemiology with discussion on the inputs of epidemiology in surveillance,
risk analysis and regionalization. # 2001 Elsevier Science B.V. All rights reserved.

Keywords: International trade; SPS Agreement; Epidemiology; Risk analysis; Regionalization; Surveillance

1. Introduction

International trade in live animals and animal products occasionally has led to the
spread of disease between countries resulting in severe consequences for the
agricultural economy of a country. Several examples of trans-boundary spread of diseases
have been documented. The spread of rinderpest to Belgium from cattle originating in
India destined for Brazil and transiting in the port of Antwerp in 1920 reintroduced the
cattle plague to Europe (OIE, 1999a). Foot-and-mouth disease (FMD) was introduced to
Mexico from Brazil in the 1950s and led to the destruction of one million cattle, sheep

*
Corresponding author. Present address: 555 S. Howes Street, Fort Collins, CO 80526, USA.
Tel.: 1-970-490-7975; fax: 1-970-490-7999.
E-mail address: cristobal.zepeda@aphis.usda.gov (C. Zepeda).

0167-5877/01/$ see front matter # 2001 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 7 - 5 8 7 7 ( 0 0 ) 0 0 2 0 0 - 2
262 C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271

and goats and to a severe socio-economic crisis (Machado, 1968). In 1978, an African
swine fever epidemic broke out in the island of Hispaniola and could be controlled only
by the destruction of the entire swine population on the island. In Haiti, in particular, this
had a dramatic effect in the already precarious livelihood of the rural population (Zepeda,
1989). More recently, in 1997, classical swine fever was introduced to the Netherlands
and forced the destruction of roughly 11 million pigs (Dijkhuizen, 1999). The same year
FMD caused the destruction of Taiwan's swine industry (OIE, 1999b) and currently
affects several Asian countries1 (OIE, 2000a).
The introduction of rinderpest to Belgium in 1920 highlighted the need to have an
international body to help coordinate disease control efforts and in particular, to
regulate international trade in animals and animal products. In 1924, the Office
International des Epizooties (OIE) was established by an international agreement signed
by 28 countries. Its main purpose has been to inform Governments of the occurrence and
course of animal diseases throughout the world and of ways to control these diseases; to
coordinate (at the international level) studies devoted to the surveillance and control of
animal diseases; and to harmonize regulations for trade in animals and animal products
among member countries (OIE, 2000b).
In April 1994, the Final Act of the Uruguay Round of Multilateral Trade Negotiations
of the General Agreement on Tariffs and Trade (GATT) was signed; this led to the
creation of the World Trade Organization (WTO) in January 1995. Among the
agreements that were included in the treaty that established the WTO is the Agreement on
the Application of Sanitary and Phytosanitary Measures (SPS Agreement) which sets out
the basic rules for food safety, and animal and plant health standards (WTO, 1995).
The SPS Agreement specifically empowers the OIE as the organization responsible to
draft international standards for animal health. The renewed importance conferred by the
SPS Agreement on the OIE has spurred the interest of countries across the globe; in 1989,
114 countries were members and by December 1999 membership had reached 155
countries (OIE, 2000b).
The main goal of the SPS Agreement is to allow increased trade of agricultural
products while recognizing the right of countries to protect human, animal and plant
health.

2. Risk, trust and trade

Over the years, one of the most important means to prevent the introduction of disease
through trade has been a policy of risk avoidance (i.e. a ``zero-risk'' approach to trade).
The driving philosophy behind this approach is captured in a phrase widely used in past
decades by animal health officials: ``if in doubt, keep it out''. Although the ``zero-risk''
approach has prevented disease introductions, it is widely understood that it often led to
unnecessarily stringent measures that frequently had no scientific basis and were in fact
used as barriers to trade.

1
Promed-mail: 05-APR-00 South Korea, 06-APR-00 Japan, 10-MAY-00 Mongolia, 26-MAY-00 Kyrgyzia
(Bishkek), 19-MAY-00 Georgia, 19-MAY-00 Kazakhstan.
 C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271 263

Zero-risk is not attainable. The validity of the zero-risk approach to trade issues can be
questioned with the following points:

 In all areas of safety, risk can be reduced to an unimportant level but scientifically it
is impossible to reduce it to zero. Scientific evidence cannot prove the absence of risk;
rather, it gives some certainty of the potential for the absence of risk.
 Nature does not respect political boundaries. Thus, a disease can pass a political
boundary without notice, with or without international trade.
 Unnecessary restrictive technical barriers to trade can lead to smuggling as a means of
getting around such barriers. This can threaten agricultural security seriously the
opposite effect to that intended. They also can lead to a country finding itself isolated
from overseas market opportunities.
 International travel and trade is a fact of our current global community and risk always
will be present (no matter how small).

In short, trade implies risk; however, the lack of officially regulated trade also implies
risk because it stimulates informal, unregulated trade.

3. The SPS agreement and epidemiology

Some of the key notions contained in the SPS Agreement are risk analysis,
regionalization, harmonization, equivalence and transparency. Both, risk analysis and
regionalization depend on the data generated by a comprehensive surveillance system
with a sound epidemiological design. Thus, epidemiology is a key element in providing
the scientific basis to satisfy international trade requirements. Harmonization,
equivalence and transparency are the basis for mutual trust between veterinary services
essential to ensure safe trade.
The SPS Agreement defines harmonization as the establishment, recognition and
application of common sanitary and phytosanitary measures and encourages countries to
participate actively in the development of international standards through the relevant
international organizations. However, embedded within the concept of equivalence, the
agreement also recognizes that different measures may achieve the appropriate level of
protection deemed by the importing country and allows the establishment of bilateral and
multilateral agreements on recognition of equivalence of specified measures. All changes
in the application of SPS measures should be published and made available to WTO and
trading partners, ensuring thus transparency (WTO, 1995).

4. International animal health standards

SPS measures should be science-based and should follow international standards laid
out in OIE's International Animal Health Code (OIE, 1999c). The OIE Code covers the
most important diseases and provides guidelines on issues like surveillance, risk analysis
and regionalization. If a country chooses to adopt a higher standard of protection, it must
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provide a scientific justification and base its decision on a risk analysis. Article 3 of the
SPS Agreement provides the basis upon which valid SPS measures can be applied:
``Members shall ensure that their sanitary and phytosanitary measures do not
arbitrarily or unjustiably discriminate between members where identical or similar
conditions prevail, including between their own territory and that of other members.
Sanitary and phytosanitary measures shall not be applied in a manner which would
constitute a disguised restriction on international trade'' (WTO, 1995).
In other words, a country may impose sanitary measures only if the disease of concern
is exotic or if it is under an official control program. Furthermore, measures can be
applied to trading countries only if they are also required internally within the importing
country. The flow to establish valid SPS measures is presented in Fig. 1.

5. Epidemiology and risk analysis

As mentioned above, the relationship between epidemiology and international trade

revolves around risk analysis and regionalization. Animal-health risk analysis relies on
epidemiological input; without such input, the process could become a mere probabilistic
exercise that is not biologically coherent. In the following paragraphs, we will describe

Fig. 1. Validity criteria for sanitary and phytosanitary measures in international trade.
 C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271 265

the epidemiological components linked to the risk analysis process. Table 1 summarizes
these interactions.
Animal-health risk analysis is a process composed of hazard identification, risk
assessment, risk management and risk communication. Its objectives are to identify the
potential hazards associated with a commodity, to assess the probability of introduction,
establishment and spread within the importing country; and to estimate the potential
consequences related to its introduction (OIE, 1999c). Although, risk analysis as a formal,
documented, methodological approach is relatively new for veterinary services, the
concept has been applied informally for many years.

5.1. Hazard identification

The risk analysis process is initiated by identifying the hazards. The first step is to
prepare a complete list of pathogenic agents that could be associated with the
commodity.2 To do this, a thorough knowledge of the infectious diseases affecting the
species and the commodity of concern is required. Once this list is established, it needs to
be contrasted with the diseases existing (or potentially existing) in the export country.
Epidemiological information will then help to determine whether diseases may be present
in the exporting country but do not affect the species of interest, or whether the diseases
may affect the species but the agents are not present in the export product.
Hazard identification may be initiated by a request from the exporting country to be
recognized as free from a specific disease. In this situation, the methods used to
demonstrate the absence of disease and the measures taken to avoid its introduction or
reintroduction need to be reviewed.
Importing countries need to determine for which diseases valid SPS measures can be
established; this is done by defining which diseases are exotic and which diseases are
under an official control program. The pathogens identified during hazard identification
are arranged by importance of the disease(s) usually according to OIE criteria for the
categorization of diseases: List A and B (OIE, 1999c). However, diseases (hazards) other
than those listed by the OIE may be included in the list.

5.2. Risk assessment

In theory, a risk assessment should be conducted for each hazard; in practice, however,
a risk assessment is conducted initially for the most important hazard; if the risk is
deemed to be acceptable, then the remaining hazards are assessed. Alternatively, all
hazards can be assessed qualitatively; and, a more thorough, quantitative assessment is
performed only on those hazards for which the risk (i.e. likelihood and consequences) is
perceived to be high.
Risk assessment consists of three interrelated steps: release assessment, exposure
assessment and consequence assessment (OIE, 1999c). Each of these steps requires a
thorough epidemiological knowledge of the disease in question. In the case of

2
According to the OIE Code (OIE, 1999c), the term commodity is used to include live animals, animal
products, semen, embryos and pathological material.
 266
Table 1
Epidemiological components within risk assessment

C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271

Risk assessment steps Epidemiological components Data/knowledge requirements

Hazard identification List of pathogenic agents that could be associated with the commodity Existing control programs
Exotic diseases
Emerging diseases
Epidemiology of each disease in relation to the commodity
Knowledge on the presence or absence of disease in a country or zone Methods to demonstrate absence of disease
Release assessment Prevalence of disease in the importing country/risk of introduction of Survey and surveillance results
disease from neighboring countries or zones or from trade with other countries Survey methodology
Confidence level, precision, expected prevalence
True prevalence
Herd-level sensitivity and specificity
Animal-level sensitivity and specificity
Role of commercial and backyard operations
Regionalization
Epidemiological characteristics of the disease and the agent Incubation period
Carriers
Role of wildlife
Morbidity
Mortality
Method of spread
Pathogenesis
Target organs
Susceptible species
Agent inactivation procedures
Diagnostic tests Test Se and Sp
Cut-off values
Testing strategies
Exposure assessment Characteristics of the susceptible populations and environmental factors Pathways for exposure
in the importing country Herd and animal densities
Immune status
Vectors
Seasonality
Cultural practices
Volume

C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271

Intended use of the commodity
Consequence assess-Biologic and economic consequences Susceptible species
ment
Method of spread
Contact rates
Morbidity
Mortality
Number of affected herds/animals
Direct economic impact (mortality, impact on production)
Cost of control and eradication
Indirect economic impact: interrupted trade,
loss of international markets

267
268 C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271

quantitative risk assessments, an understanding of probabilistic and statistical methods

also is needed.
Release assessment describes the biological pathways leading to the introduction
(``release'') of the hazard into the importing country and estimates the associated
probabilities. One asks, whether the disease is present (or potentially present) in the
country of origin. To answer this question, one must analyze available survey and
surveillance findings, the survey methods, characteristics of the diagnostic systems used
and the relationship between different production systems. Most importantly, the
epidemiological characteristics of the disease and the agent must be taken into account
(e.g. the length of the incubation period, the range of susceptible species, transmission
mechanisms and agent inactivation procedures).
The next step in the process is the exposure assessment; it describes the pathways that
could lead to infection of human or animal populations in the importing country and
estimates the associated probabilities. This requires information on the demographics of the
susceptible populations, immune status, geographic distribution of herds, types of production
systems, presence and distribution of vectors and seasonality. Exposure pathways often are
shaped by economic forces that regulate the volume of trade and the potential for distribution
of the commodity within an importing country. It is important to understand the factors
influencing trade to analyze the potential consequences of disease introduction.
Risk is the combination of the likelihood of occurrence of an adverse event and the
magnitude of the consequences (Ahl et al., 1993). Once the probability of occurrence has
been determined, the last step in the risk assessment is the consequence assessment,
which deals with both the biologic and economic impacts following a disease
introduction. The expected number of affected herds, mortality and morbidity rates,
contact rates and wildlife susceptibility as well as direct and indirect economic costs
must be assessed to estimate the magnitude of the impact of the adverse event. Thus,
epidemiological information about the disease and agent under investigation is of prime
importance at each of the three steps of the risk assessment process.

6. Risk analysis and regionalization

Previously, when a country declared the presence of a disease, its entire territory was
considered affected. The SPS Agreement recognizes that either a zone within an infected
country or a region (comprised of several countries or parts thereof within an infected
sub-continent) could be declared disease-free based on factors such as geography,
ecosystems, veterinary infrastructure and in particular, animal-movement control and
disease-surveillance systems (WTO, 1995). This has opened the possibility to concentrate
disease-control efforts on areas with greater export potential, without the need to
eradicate disease on a countrywide basis.
Risk analysis and regionalization are closely linked. When conducting a risk analysis
to assess a commodity originating from a disease-free region or a zone, two perspectives
should be considered: (1) the probability of disease reintroduction into the zone or region
and the potential for spread of the disease; and (2) the probability of introducing a
pathogen through the importation of animals or animal products from that zone or region
 C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271 269

(given the probability of reintroduction). In this context, the evaluation of the veterinary
services in the country is of utmost importance. The veterinary services should have the
ability to provide appropriate services within their country and to provide reliable
epidemiological data and information to other countries. In 1993, the OIE published
guidelines for the evaluation of veterinary services, including a model questionnaire used for
self-evaluation of a national veterinary service (OIE, 1993). The rationale behind this
evaluation is twofold, to assist the national authorities in the decision making process
regarding priorities to be given to its own veterinary services; and to assist the process of risk
assessment related to international trade in animals and animal products. In both cases, the
evaluation is to demonstrate the veterinary service's ability to effectively control the health
status of the national herd and the sanitary status of animal products marketed.
Although the process includes evaluation of the resources, of the management
capability, of legislative and administrative support, and of performance history (among
other items), the main issue is one of trust the confidence of trading partners in each
other's competence and integrity.
These zones and regions have to respond to internationally accepted criteria to be
recognized as disease-free. Epidemiology has an important role to play in proposing such
criteria based on scientific reasoning and which eventually can be adopted by
international organizations such as OIE and WTO. Efforts now are being made by some
of our fellow epidemiologists to assess the validity of survey and surveillance systems
critically, in view of declaring a zone, country or region ``disease-free'' (taking into
account that tests are not perfect, that diseases are not necessarily randomly distributed
within a national herd, and that surveys and surveillance systems must be specifically
designed and statistically represented to yield valid results) (Salman and Ruppanner,
1999; Dufour, 1997).

6.1. Risk management

One of the objectives of risk analysis is to determine the most appropriate methods to
achieve the desired level of protection. Risk assessment identifies the points along the
pathway of introduction that have the greatest effect on risk (an appropriate selection of
mitigating measures applied to the most sensitive points in the process, usually allows for
substantial reductions in risk). Decision analysis is a method applied to several
epidemiological health problems (Dargatz and Salman, 1990; Carpenter and Norman,
1983) and has a direct application to international trade. This method integrates economic or
biological consequences and the probability of an event occurring so that the selection of
options in decision making process can be optimized. Evaluating the efficacy of the options
selected is an iterative process that involves their incorporation into the risk assessment and
the comparison of the resulting level of risk to that considered acceptable (OIE, 1999c).

7. Acceptable risk

The notion of ``acceptable risk'' has been debated for a long time. The SPS Agreement
does not indicate how to determine the acceptable level of risk (also termed the
270 C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271

appropriate level of protection (ALOP)). A current line of thought is to include

economics in the determination of the appropriate level of protection by taking into
consideration the benefits of trade and the potential costs of disease introduction and its
associated probability of occurrence. However, this is an idea that has not yet gained wide
acceptance particularly at political levels. Regardless of the method used to determine
the ALOP, a country must be consistent in its application and should try to minimize the
negative effects on international trade (WTO, 1995).

8. Challenges and opportunities

The SPS Agreement has opened vast opportunities for veterinary epidemiologists. Still,
the solutions required to facilitate safe trade call for an integrated multidisciplinary
approach including other disciplines such as economics, statistics, geography and
geographic information systems, ecology, sociology and politics.
Epidemiologists have always dealt with the concept of health and disease in
populations; however, the promotion of international trade presents an additional
challenge, it requires a shift from herd-level epidemiology to a much larger scale that
encompasses zones, countries and regions.
There is a need to develop new methods to determine the disease status of countries
and zones as prevalence approaches zero methods to be applied when an area (zone,
country or region) is to be declared free from disease. These methods need to be
statistically valid and at the same time economically viable and sufficiently practical to be
applicable under different field conditions (particularly in developing countries where
different production systems might co-exist).
An additional challenge is the quantitative integration of the results for the evaluation
of veterinary services into the risk analysis process. Although, there is a widespread
recognition that the quality of the veterinary services is linked to the level of risk, at
present, there is lack of methods to assess this relationship in a quantitative way.
Today, perhaps more than ever before, training in veterinary epidemiology is essential
for veterinary services staff at every level. Formal postgraduate training programs
currently offered need to be expanded to include risk analysis and economics in the broad
context of international trade.
The OIE, through several of its collaborating centers, offers training in these fields.
However, the role of collaborating centers is to complement formal epidemiological
training not be a surrogate for it.

9. Conclusions

The SPS Agreement has had a strong impact on the organizational structures of
veterinary services, internationally. Veterinary epidemiology has been always closely
linked with international trade of animals and animal products; nonetheless, the
Agreement on the Application of Sanitary and Phytosanitary Measures of the World
Trade Organization has ratified epidemiology's role, placing it at the center of animal
 C. Zepeda et al. / Preventive Veterinary Medicine 48 (2001) 261271 271

health trade-related decisions. Today, veterinary services worldwide acknowledge this,

and are strengthening their disease surveillance systems and are integrating specialized
multidisciplinary groups to deal with risk analysis and regionalization. Unfortunately,
several countries particularly in the developing world are facing considerable
difficulties in the implementation of the SPS Agreement (WTO, 1999).
Disease surveillance systems play a central role in providing the science-based
information needed to conduct risk assessments and regionalization appraisals.
In the past, SPS measures often were applied in a defensive, reactive mode. Today,
there is the opportunity to shift to a proactive approach that truly promotes agricultural
production and enhances international trade. The common threads supporting this effort
are the scientific basis in the application of SPS measures, transparency and trust.

References

Ahl, A., Acree, J., Gipson, P., McDowell, R., Miller, L., McElvaine, M., 1993. Standardization of nomenclature
for animal health risk analysis. Rev. Sci. Tech. Off. Int. Epiz. 12, 10451053.
Carpenter, T., Norman, B., 1983. An economic evaluation of metabolic and cellular profile testing in calves to be
raised in a feedlot. J. Am. Vet. Med. Assoc. 183, 7275.
Dargatz, D., Salman, M., 1990. Decision tree analysis and its value to herd health. The Compendium 12, 433
439.
Dijkhuizen, A., 1999. The 19971998 outbreak of classical swine fever in the Netherlands. Prev. Vet. Med. 42,
135137.
Dufour, B., 1997. Creation by the Delphi method of an evaluation scale on the quality of animal surveillance
networks. In: Proceedings of ISVEE 8, Paris, pp. 07.01.107.01.3.
Machado, M., 1968. An Industry in Crisis. MexicanUnited States Cooperation in the Control of Foot-and-
Mouth Disease. University of California Press, Berkeley, CA.
OIE, 1993. Guidelines for the evaluation of veterinary services. Rev. Sci. Tech. Off. Int. Epiz. 12, 12911313.
OIE, 1999a. 75 years 19241999. Office International des Epizooties, Paris.
OIE, 1999b. World Animal Health in 1998. Office International des Epizooties, Paris.
OIE, 1999c. International Animal Health Code. Office International des Epizooties, Paris. www.oie.int.
OIE, 2000a. Disease Information. Office International des Epizooties, Paris. www.oie.int.
OIE, 2000b. Ten year report 19901999. Office International des Epizooties, Paris.
Salman, M., Ruppanner, R., 1999. Risk management and decision analysis in animal health. In: Proceedings of
Society for Veterinary Epidemiology and Preventive Medicine, Bristol, pp. 16.
WTO, 1995. Agreement on the Application of Sanitary and Phytosanitary Measures. World Trade Organization.
www.wto.org.
WTO, 1999. Review of the Operation and Implementation of the Agreement on the Application of Sanitary and
Phytosanitary Issues. World Trade Organization. www.wto.org.
Zepeda, C., 1989. Perspectivas de la repoblacion porcina en Hait. Vet. Mex. 20, 6570.