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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
OCR for page 20
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
OCR for page 21
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
OCR for page 22
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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:
OCR for page 30
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
OCR for page 31
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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Representative terms from entire chapter:
epidemiologic studies
