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~ Introduction OVERVIEW An animal sentinel system is a system in which data on animals exposed to contaminants in the environment are regularly and systematically collected and analyzed to identify potential health hazards to other animals or humans. Sentinel systems may be classified according to what they are designed to monitor (e.g., exposure or effect), the types of animals used, the environment in question, or whether the animals are in their natural habitat (observational systems) or are purposely placed in an environment in question (experimental or in situ systems). Sentinel systems may be designed to reveal environmental contamination, to monitor contamination of the food chain, or to investigate the bioavaila- bility of contaminants from environmental media; these types of systems can be designed to facilitate assessment of human exposure to environmental contaminants. Other sentinel systems may be designed to facilitate assessment of health hazards resulting from such exposure; e.g., systems can be designed to provide early warning of human health risks or can involve deliberate place- ment of sentinel animals at a selected site to permit measurement of environ- mental health hazards. Some sentinel systems can be used to indicate both exposure and ha7~.rd~. Companion animals, domestic livestock, laboratory rodents, and free-rang- ing or captive wild animals and fish are all potentially useful for sentinel systems. Animals can be used to monitor any type of environment, including homes, work places, farms, and natural aquatic or terrestrial ecosystems. They can be observed in their natural habitats or placed in work places or sites of suspected contamination. PURPOSE OF THE STUDY As part of its health-related responsibilities pertaining to hazardous waste 19

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20 ANIMALS AS SENTINELS sites and releases of chemicals, the Agency for Toxic Substances and Disease Registry (ATSDR) asked the National Academy of Sciences to review and evaluate the usefulness of animal epidemiologic studies for human risk assess- ment and to recommend types of additional data that should be collected to perform risk assessments for human populations. The National Research Council established the Committee on Animals as Monitors of Environmental Hazards in the Board on Environmental Studies and Toxicology of the Com- mission on Life Sciences. The committee was to address specifically the following: Veterinary epidemiologic studies that characterize animal morbidity and studies of wild populations that characterize reproductive physiology, toxicant body burden, and functional changes or changes in gross pathology. Evidence of correlations between exposure and chemical or physical environmental hazards and between animal and human morbidity. Analytic methods of discerning such correlations. The committee reviewed observational epidemiologic studies, including descriptive and analytic investigations in animal populations. It also reviewed experimental studies in which animals had been purposely placed in an envi- ronment to evaluate exposure or health effects. It included efforts to correlate exposures with clinical disease and other physiologic and pathologic end points, emphasizing sentinel systems that yielded data that could be correlated with exposures of human populations. The committee considered animal sentinels used to monitor exposure and systems used to measure health ef- fects. The committee also held a 2-day workshop in May 1988 to obtain information on programs that collect animal sentinel data from a panel of exerts (see Appendix). The committee was asked to compile a directory of national, state, and local monitoring and surveillance programs and to evaluate them and present recommendations for their use, coordination, and augmentation. However, the committee found that it could not deal with all programs that monitor animal populations, in part because the large number of programs that might have been included in such a directory would exceed its resources. With the concurrence of ATSDR, the committee selected and reviewed only programs that have the potential to improve understanding of human risk. The committee considered the gaps in existing data that need to be ad- dressed if animal sentinel data are to be used in human risk assessment. It discussed issues of coordination between programs and standardization of data collection, analysis, and reporting, and it developed recommendations thereon. The studies reviewed included investigations of outbreaks of disease in food

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INTRODUCTION 21 animals, companion animals, and fish and wildlife; monitoring of wild animals; descriptive and analytic epidemiologic studies; and In situ studies of laboratory and nonlaboratory animals. The committee explored the potential use of animal sentinels in determining risks to human populations posed by environ- mental contaminants, with special care to determine whether in situ and natu- ral-exposure studies could supplement traditional laboratory studies or help to remove difficulties in risk assessment, such as problems in exposure assess- ment, and could be helpful in evaluating exposures to and effects of complex mixtures that are difficult to assess in the laboratory. HISTORICAL USE OF ANIMAL SENTINELS Animals have long sewed as monitors of environmental hazards. The classic example of an animal sentinel system is the use of canaries in mines. Canaries are more sensitive than humans to the effects of carbon monoxide and often were taken into mines (placed in situ) to warn of imminent hazard. No attempt was made to measure the exposure of the birds, but they were effective sentinels. The simplicity of the system exemplifies the ease with which some animal sentinel systems can be developed and used (Schwabe, 1984a). A second historical example exemplifies the use of observational epidemio- logic studies in providing an early warning of human risk related to environ- mental conditions. The death of cattle at an 1873 stock show in Smithfield, England, was associated with a dense fog and preceded the increased morbidi- ty and mortality later observed among humans during air-pollution episodes. (`Vetennarian, 1874a,b). A list of environmental to~ncants first identified in animals is found in Table 1-1. Observation of animals that live in the same environment as humans can yield information for human hazard identification and risk assessment. Like humans, animals are exposed to contaminants in air, soil, water, and food, and they can suffer acute and chronic health effects from those exposures. In some circumstances, animal sentinel systems can provide data more quickly and less expensively than laboratory-based animal experiments. CURRENT USE OFANl~lAL SENTINELS IN RISK ASSESSMENT Animal sentinel systems can provide data to clarify the human health risks posed by environmental contaminants. For example, livestock have been used

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IN7~RODUCTION 29 since the 1950s to monitor lead- and fluoride-containing effluents near indus- trial facilities. The uncertainty of prediction of human risk related to expo- sure to a chemical can be greatly decreased by evidence of toxic effects in animal sentinels at environmentally relevant concentrations. When clinical and epidemiologic information derived from human patients is available, it obviously should be used for human risk assessments; but such information is lacking in the case of most environmental chemicals, so laboratory-animal data usually constitute the primary basis for risk assessments. Even when an~mal- based human risk assessments are expressed in quantitative terms, uncertainty exists, because it is difficult to extrapolate results from inbred laboratory animals (particularly rodents) to humans. In addition, results of exposures at the high doses generally used in the laboratory must be extrapolated to predict results of exposure at low, environmentally relevant doses. Animals outside the laboratory can yield information at each step in risk assessment- risk characterization hazard identification, dose-response assess- ment, and exposure assessment. Under appropriate conditions, the use of domestic and wild animals can help to reveal the presence of unknown chemi- cal contaminants in the environment before they cause human harm or to clarify the extent of risk posed by known chemical contaminants. Domestic and wild animals share the human environment and are in the human food chain (Figure 1-1) and so permit their study to uncover the acute and chronic health hazards caused by contaminants in air, soil, water, and food. Their potential for use as early warnings or sentinels of chemical exposures depends on their responding more rapidly than would humans who are similarly ex- posed (i.e., decreased latency) and their responding at a lower dose (increased susceptibility) (Davidson et al., 1986). An ideal animal sentinel species for risk assessment is one that is exposed to chemical contaminants in habitats shared with humans or comparable with human habitats and at similar concentrations. Furthermore, it should be capable of responding to chemical insults that are manifested by a broad spectrum of pathologic conditions, including behavioral and reproductive dysfunctions, immunologic and biochemical perturbations, and anatomic changes as varied as birth defects and cancer. No animal species used for risk assessment can be expected to respond in exactly the same ways as humans, so those whose primary interest is the assessment of chemical hazards to humans must be able to judge the rele- vance of the animal data. That necessitates an understanding of the toxic properties of the chemicals in question, of the physiology of the animal species tested and of humans, and of the potential for human exposures (Kendall, 19~). The animal sentinel programs and studies described in this report use one or more methodologic approaches:

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30 ANIMALS AS SENTINELS Environmental contamination levels (air, soil, water, food, or feed) Human Animal body burdens _ Food chain levels ~ body burdens 1 Effects in people Effects in animals FIGURE 1-1 The relationship of the environment and the food chain to human and animal health effects. Descriptive epidemiologic studies of animal populations estimate the fre- quency and pattern of disease and evaluate associations with environmental exposures by such techniques as spatial mapping. Clusters of unusual health events such as a new disease or an epidemic, might suggest environmental exposures. Animals serve as monitors for environmental chemicals; the dis- eases and incidence of disease provide data to describe the prevalence of exposure in populations and to evaluate cumulative doses of persistent com- pounds. Analytic epidemiologic studies test hypotheses regarding environmental exposures and estimate risks using controlled-observation study designs. In an in situ study, animals are taken to a site where contamination is suspected (e.g., a hn~ardous-waste site), and then, under controlled conditions in the natural environment, monitored for bioaccumulation and health effects. The relationship among epidemiological studies, in situ studies, and laboratory studies is shown in Figure 1-2. STRUCTURE OF THE REPORT Chapter 2 explains and illustrates the definitions and concepts used in the report. The characteristics of animal sentinel systems species, exposure media, temporal and spatial considerations, and measures of effect are dis- cussed. The objectives of animal sentinel systems for identification of environ- mental contamination, food-chain contamination, and adverse human and

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INTRODUCTION 31 - ( Observationa/ 2- /:ea (native ILL Lab Popu- FIGURE 1-2 Interrelationships of epidemiologic studies. Ex perimenta/ animal health effects are outlined. The uses of animal sentinel systems in epidemiologic and in situ studies are characterized. The chapter also discuss- es the advantages and limitations of such systems, e.g., with respect to prob- lems in extrapolation to humans, suitability for evaluating chemical mixtures, and multifactorial exposures. Chapters 3, 4, and 5 describe applications of sentinel studies in food ani- mals, companion animals, and fish and wildlife. The programs that use animal systems for environmental monitoring and hazard identification are described, as well as programs with potential applicability. Observational studies includ- ing outbreak investigations, analytic epidemiologic investigations, and in situ studies are reviewed and illustrated for each population of food animals, companion animals, and fish and wildlife. The use of animal sentinel systems specifically in risk assessment is consid- ered in Chapters 6 and 7. They focus on selection and application of animal sentinels for components of qualitative and quantitative risk assessment. As requested in the committee's task, some discussion of application of animal sentinel data to geographic information systems methods is included. The committee's conclusions and recommendations for the use of animal sentinel systems are presented in Chapter 8.

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