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3 Food Animals as Sentinels Food animals are exposed to infectious agents and to a multitude of environ- mental contaminants that can accumulate in their bodies. Food animals can serve as sentinels of environmental health hazards, because identification of infectious or foreign substances in a food animal is a signal of potential bio- logic or chemical contamination of the animal's environment, of other animals and humans that share the animal's environment, and of humans that ingest the animals and animal products. Many toxic chemicals are taken up in the tissues of food animals. For example, after accumulating in forage plants, a chemical can accumulate further in beef cattle that eat the plants. A propen- sity for bioaccumulation is one of the generally accepted criteria that define a xenobiotic as "potentially hazardous" (Stern and Walker, 1978~. The result of such serial bioaccumulation, particularly of some chlorinated hydrocarbon pesticides, is the potential for greater exposure of animals at the top of the food chainincluding humansthan of animals lower in the food chain. Because food animals are part of the food chain, they are monitored for biologic or chemical contaminants in numerous programs. All the programs are epidemiologic studies~ata usually are collected on animals that are not intentionally exposed to biologic or chemical contaminants. Among the sever- al agencies that monitor foods for purity in the United States are the Food Safety and Inspection Service (FSIS) of the U.S. Department of Agriculture (USDA), the Food and Drug Administration (FDA) of the U.S. Department of Health and Human Services (HHS), and state government agencies. Those agencies conduct tests for contaminants infectious agents, pesticides, and toxic chemicalsin and on plant and animal food products. Food-monitoring programs are designed to monitor hazards to human consumers; they produce data useful for signaling environmental contamina- tion in the geographic area of the food animals' origin and for predicting human risk associated with consumption of the sentinel animals themselves. Food-monitoring programs generate information on contaminants in tissues; for example, they provide information on tissues infected with microorganisms and their toxins and with toxicants from the environment. Many food-moni- 53

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54 ANI~lLS AS SENTINELS taring programs (e.g., FDA's Total Diet Study) provide quantitative data on the extent of human exposure to chemicals in food by reporting concentrations of xenobiotics in animals' tissues. The federal and state programs that monitor food animals for chemical residues do so primarily to determine adherence to environmental regulations aimed at protecting humans from harmful chemicals in their food and at protecting animals from direct and indirect effects of chemical contaminants. The principal federal agencies that operate chemical-residue monitoring pro- grams for protection of the human food supply are FSIS and FDA. FSIS is responsible for monitoring the safety of meat and poultry; FDA is responsible for monitoring pesticide residues and other chemicals of interest in all other foods in interstate commerce, e.g., animal feeds, fruits, vegetables, grains, eggs, milk, processed dairy products, fish, and shellfish. In addition, FDA monitors shellfish for metals, microbial pollution, and algal toxins. Many state agencies conduct parallel monitoring programs on animal products in intra- state commerce. Agencies that conduct chemical-residue monitoring to pro- tect the health of wildlife and human consumers include the U.S. Fish and Wildlife Service (FWS), the National Marine Fisheries Service (NMFS), and many state agencies. EPA registers or approves the use of pesticides and establishes tolerances if use of specific pesticides might lead to the presence of residues in food. The residue and chemical-contamination monitoring programs of FDA, USDA, and various other federal, state, and local agencies can be thought of as animal sentinel programs. In effect, they collect data from animals that are acting as sentinels of environmental hazards. This chapter describes some of the most important food-chain monitoring programs in the United States. DESCRIPI~VE EPIDEMIOLOGIC STUDIES U.S. Departmera of Ag~cul~= Food Safety and Inspection Service The responsibility for ensuring the safety of meat and poultry was given to USDA in the Federal Meat Inspection Act of 1906 and through later acts and amendments. USDA is charged with the inspection of meat and poultry products that enter commerce and are destined for human consumption. FSIS monitors all relevant stages of animal slaughter and of meat and poultry processing. The magnitude of that responsibility is reflected in the large number of animals that are slaughtered each year in the United States for

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FOOD ANIMALS AS SENTINELS 55 human consumption and in the large number condemned (rejected for food or feed consumption) because of chemical contamination or disease (Table 3- 1~. The ultimate goal of the federal inspection program is to ensure that meat, poultry, and meat and poultry products are wholesome, unadulterated, and properly labeled and do not constitute a health hazard to consumers. In 1983, FSIS asked the Food and Nutrition Board of the NRC to evaluate the scientific basis of the current system for inspecting meat, poultry, and meat and poultry products. The NRC committee found that "the meat and poultry inspection program of the FSIS has in general been effective in ensur- ing that apparently healthy animals are slaughtered in clean and sanitary environments" (NRC, 1985~. However, the committee noted deficiencies in the inspection system regarding public-health risks related to chemical agents, including deficiencies in the sample sizes and procedures for measuring chemi- cal residues and in the setting of priorities for testing chemicals. The com- mittee concluded that "the most effective way to prevent or to minimize haz- ards presented by certain infectious agents and chemical residues in meat and poultry is to control these agents at their point of entry into the food chain, i.e., during the production phase on the farm and in feed lots." The Food and Nutrition Board committee noted the absence of an effective national surveillance system for monitoring the disease status of food animals, as well as the absence of an adequate mechanism for tracing infected or contaminated animals to their source. For example, the probability of success- fully tracing diseased or contaminated animals to their producers was approx- imately 10% for cattle and 30% for swine. The committee felt that "the ability to institute action at the first critical point of production (on the farm) places a heavy responsibility on antemortem and postmortem inspections to identify potential health hazards, although such inspections by themselves cannot solve the problem." It recommended development of a mechanism whereby FSIS could coordinate the monitoring and control of hazardous agents during pro- duction, where those agents enter the food supply. To that end, it proposed that a national center be established to monitor and store information on animal diseases and that all USDA animal-disease surveillance programs be designed to make full use of animal-disease prevalence data obtained from meat and poultry inspection programs. USDA has since improved its methods for identifying individual animals and can now trace about 90% of slaughtered animals to their points of origin (and thus to a potential source of contami- nants). However, FSIS has no regulatory authority or responsibility at the producer level.

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AS ANIMALS AS SENTINELS TABLE 3-1 November 1987 Livestock Slaughter Report for the USDA Food Safes and Inspection Service Category of Livestock Number Number Slaughtered Condemned Bulls and stags 41,238 90 Steers 987,866 812 Cows 409,044 6,452 Heifers 665,466 569 Bob veal 84,939 1,532 Formula-fed veal 57,716 75 Non-formula-fed veal 10,048 35 Calves 20,625 37 Mature sheep 19,129 1,345 Lambs and yearlings 332,612 1,206 Goats 15,486 51 Barrows and gilts 4,455,923 4,989 Stags and boars 38,061 220 Sows 183,411 740 Horses 23,159 91 Young chickens 375,150,905 4,196,327 Light fowl 11,406,615 408,323 Fryer-roaster turkeys 366,595 4,705 Young turkeys 21,746,540 243,020 Old breeder turkeys 119,274 3,267 Ducks 1,799,462 22,457 Geese 59,114 891 Rabbits 43,215 156 Capons 100,904 3,183 Heavy fowl 2,605,871 67,162 Young breeder turkeys 103,751 2,082 Others (guineas, squabs, pigeons) 234,935 1,255 Source: USDA, 1987 National Animal Health Monitoring System USDA recognizes the need to quantify diseases in food-producing areas

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FOOD ANIMALS AS SENTINELS 57 and associated production losses. The Animal and Plant Health and Inspec- tion Service (APHIS) of USDA has taken the lead in developing, coordinat- ing, and implementing the National Animal Health Monitoring System (NAHMS) (King, 1987~. The objective of the NAHMS is to develop methods for estimating the incidence, prevalence, trends, and economic impact of important disease and contamination problems in food-producing animals at the local, state, and national levels. The program often entails the systematic collection of animal~feed products" in addition to blood and serum, other tissues, and milk- and the data necessary for tracing specimens to producers, animals, or geographic areas. Samples can be analyzed, not only for disease, but for environmental contaminants of interest to the general public or health officials. The NAHMS collects data from producers on all health-related events and health-care costs for 12 months and uses these data in its estimates. Herds and flocks are randomly selected within production type and by probability in proportion to size, so that results can be extrapolated to larger populations at risk. Each month, veterinary medical officers interview the producers, consoli- date the data, and compile reports that serve as the foundation of the NAHMS data base. A subsample is selected for more intensive diagnostic workups, including bacteriologic, virologic, serologic, and necropsy procedures. The FDA Center for Veterinary Medicine recommended that the NAHMS data base be expanded to consider drug-use patterns and adverse reactions in food animals (Teske and Paige, 1988~. Such an expansion would be useful in alerting USDA, FDA, and consumers to potential hazards associated with drugs used in food animals. Reported events might be used to identify inap- propriate use of drugs in food animals and might be linked to residue data to identify trends. Measurement of environmental contaminants is not part of the current NAHMS program, but its utility could be greatly enhanced if it expanded its program to monitor for the appearance of environmental contaminants, as signaled by adverse health or behavioral effects. The resulting data could be used to relate exposures directly to production, reproductive performance, and other health effects. The benefits to farmers and producers would be greatly increased with the addition of this information, because specific exposures correlated with adverse effects could be eliminated or minimized. Similarly, it would benefit federal, state, and local health officials by signaling contami- nation in the environment, signaling potential risk to humans in the area, and providing data that could be correlated with risk associated with consumption of exposed animals. Although the usefulness of diethylstilbestrol (DES) in food animals was questioned years ago, the NAHMS would not have been particularly useful for

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58 ANIMALS AS SENTINELS predicting adverse health effects of DES in humans, because no adverse out- comes were observed in food animals at the low doses used to promote growth. Nor would the NAHMS have been notably useful for monitoring drug use and adverse reactions to drugs in food animals, because they are not included in the NAHMS data base, although this type of monitoring is a potential use of the NAHMS program. Nonetheless, the unique strengths of the NAHMS surveillance system including its size, design, and food-animal information- - make it potentially useful for monitoring human health hazards. The National Institute for Env'- ronmental Health Sciences and the Centers for Disease Control have consid- ered using the NAHMS data to monitor humans for exposure to environmen- tal contaminants. For example, if NAHMS data indicated potential human exposure to a toxicant, an epidemiologic survey, including blood sampling, of human populations could be carried out (Teske and Paige, 1988~. Market Cattle Identification Program The Market Cattle Identification (MCI) program, one of the most wide- spread surveillance programs in any species for any purpose (Schwabe, 1984b), is a nationwide cooperative federal-state program established in 1959 for the continuous serologic sampling of the U.S. beef-cattle population. The pro- gram is a key element of bovine-brucellosis eradication efforts in the United States; brucellosis, a bacterial infection, affects swine, cattle, sheep, and goats and is transmissible to humans. Blood samples are collected at slaughter from cattle marked at their ranches of origin or at sale yards with official identifying ~backtags.~ The tags are transferred from the animals to the blood specimens In the slaughterhouse, and the specimens are shipped to designated state veterinary diagnostic laboratories. There, the clotted red cells are discarded, an agglutination test for brucellosis is performed on an aliquot of each serum sample, and the remainder of each sample is discarded. Results are recorded, and the data can be traced to the premises of origin of the animals (Schwabe, 1984b). Salman et al. recently used the MCI program as a source of serum samples for the analysis of chemical contaminants (Salman et al., in press). After the bovine serum samples were screened for brucellosis, they were analyzed for chlorinated hydrocarbon insecticides. A total of 241 samples from 53 Colora- do ranches were analyzed. The pesticides were detected in 51% of the sam- ples. The most commonly found contaminant was heptachlor epoxide (28%~.

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FOOD ANIMALS AS SENTINELS 59 Food and Drug Al Current surveillance programs for monitoring food animals have different objectives, according to their mandates and goals. For example, the FDA chemical-contaminants monitoring programs are designed to determine wheth- er contaminant residues exceed tolerances by monitoring domestic and im- ported food and feed commodities for pesticide residues and to take regulato- ry action when impermissible concentrations of residues are found. FDA also determines the occurrence and concentrations of pesticides in the food supply to provide a check on the effectiveness of pesticide regulation, to identify emerging food-contamination problems, and to provide dietary-exposure data to support EPA regulatory decisions on pesticide use; FDA informs the gener- al public and others about pesticide residues in the food supply. Analytes- including radionuclides, industrial chemicals, and other toxic elementscan be analyzed according to the needs and concerns of FDA (Pennington and Gun- derson, 1987~. The Total Diet Study (sometimes known as the Market Basket Study) was designed in the l950s to monitor dietary exposure to radionuclides and was extended to pesticides and metals in the mid-1960s. The program reports the concentrations of contaminants in cooked "table-ready" foods. Its main objec- tives are to enforce tolerances established by EPA for pesticide residues on and in foods and feeds and to determine the incidence and concentrations of pesticide residues in the food supply (Reed et al., 1987~. Unlike the programs described above, the Total Diet Study analyzes dietary composites, not individ- ual animals. A notable example of the usefulness of this study involved the detection of a residue of the preservative and fungicide pentachlorophenol in unflavored gelatin in a 1975 study. Pentachlorophenol had been used to treat hides in slaughterhouses, and many of the treated hides were shipped to gela- tin manufacturers. Pentachlorophenol use on hides had been discontinued In the United States several years before the finding; investigations during the study revealed that the gelatin samples were mixtures of domestic and Mexi- can gelatin. Continued investigation determined that the Mexican gelatin contained the pentachlorophenol, and it was diverted from food use (Pen- nington and Gunderson, 1987~. The Total Diet Study continues to provide evidence of the persistence of DOT in the environment. DDT, although no longer approved for use in the United States, is still found in very low concen- trations in a great many foods, primarily those of animal origin (Lombardo, 1989~. Food animals are deliberately exposed to many chemicals to promote their growth, control their reproductive cycles, control pests, and prevent or treat disease. Although food animals biodegrade most chemicals and toxins in their

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60 ANIMALS AS SENTINELS diets, drug and other residues sometimes remain in the tissues of animals at the time of slaughter. Drug residues in food-animal tissues can be harmful to humans that consume the animals; for example, a relationship between the use of DES to promote weight gain in cattle was questioned more than 20 years ago, even before it was demonstrated that DES administered to humans in high doses is carcinogenic and is associated with reproductive disorders. Although FDA establishes permissible limits for residue concentrations in animals at slaughter, some drugs and chemical residues continue to be worri- some, e.g., chloramphenicol and gentamicin sulfate in milk and culled dairy cows and sulfonamides in milk and pork. The emphasis on continuous residue testing in FDA provides an opportuni- ty to use monitoring and surveillance data from slaughtered animals of various classes to identify residue trends in the animals. Trend data then can be used to determine the frequency of occurrence of residues according to specified attributes, geographic patterns, and seasonal patterns. Such information can help in determining the magnitude of a residue problem (not only for the animals, but for humans consuming them) and planning solutions to that problem. FDA is implementing a computerized data-handling systemthe Tissue Residue Information Management System (TRIMS)through its Center for Veterinary Medicine (CVM). Of the more than 5,000 residue violations reported in 1988, CVM was involved in active followup of more than 600. The Animal Feed Safety Branch of CVM, which is responsible for ensuring the safety of the nation's feed supply, is developing the FDA Animal-Feed Contaminant-Data System (FACS). That data base ultimately will contain toxicologic and contaminant information that can be used in followup investi- gations when residues are encountered in the tissues of food animals (beef, swine, and poultry) at slaughter (Teske and Paige, 1988~. When residues exceed acceptable limits, FDA can notify or investigate feed producers and alert the public to the potential dangers of ingesting contaminated food prod- uctse Sheath log Shellfish monitoring programs have historical and contemporary value and show well how food-chain monitoring aids in protecting human health. The programs monitor for fecal coliform organisms or paralytic shellfish toxin. One such program is the National Shellfish Sanitation Program (NSSP), a cooperative federal-state-industry program that sets guidelines and recommen- dations for production of safe shellfish. Strict adherence to NSSP standards generally will ensure safety of shellfish intended for consumption.

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FOOD ANIMALS AS SENTINELS 61 Fish, mollusks, and crustaceans can acquire pathogenic microorganisms or toxins from the environment. Controls on shellfish became of interest in the United States in the late nineteenth and early twentieth centuries, when pub- lic-health authorities observed a large number of illnesses associated with the consumption of raw oysters, clams, and mussels. In the winter of 1924, wide- spread typhoid fever outbreaks were traced to sewage-polluted oysters. A1- though the typhoid outbreaks were caused by SaImonellae, fecal coliform organisms were easier to measure and were used as the vindicators organism for the potential presence of the typhoid-inducing organisms. Thus, increased concentrations of fecal coliform bacteria in raw shellfish might indicate sewage contamination and the presence of bacteria pathogenic to humans. Fecal coliform-bacteria counts are used as part of the microbiologic standards to monitor the wholesomeness of shellfish and the quality of shellfish-growing waters. Paralytic shellfish poisoning (PSP) is one of the most severe forms of hu- man food poisoning. Some species of dinoflagellates (sometimes called "red tides") are ingested by shellfish and become concentrated enough for human consumption of the shellfish (which can contain heat-stable toxins) to be fatal. Shellfish most often involved include clams, mussels, and scallops. Affected states in the nation regularly assay representative samples of shellfish from growing areas; if the toxin content is found to be at or above 80 ~g/100 g of edible meat, the harvesting area will be legally closed. Paralytic shellfish toxin usually is measured against a saxitoxin standard with a mouse bioassay, in accordance with NSSP guidelines. National Animal Poison Ir~formudon Netwo~c The National Animal Poison Information Network (NAPINet) and the Illinois Animal Poison Information Center (IAPIC) are examples of successful national information-collection programs. As part of NAPINet, the National Animal Poison Control Center was established at the University of Illinois College of Veterinary Medicine in 1978. The center was renamed IAPIC in 1987 to emphasize Illinois's regional role as a hub of NAPINet. IAPIC is a 24-hours/day toxicology consultation service for veterinarians, pet owners, and others. Some network clients raise livestock for human consumption; others handle companion animals. NAPINet has a second regional center at the University of Georgia College of Veterinary Medicine. The latter center and others will submit case data in the same form as the L\PIC for computer- assisted animal epidemiologic assessment. The NAPINet data base contains more than 150,000 cases dating from 1983, and more than 30,000 calls were received in 1988 (Trammel and Buck, 1990~.

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62 ANIMALS AS SENTINELS Methyl Mercury in Fish NAPINet data are limited, because they represent only reported cases of arimals exposed to chemicals or toxins or those with unusual signs of illness. Reports of acute toxicoses outnumber case reports of chronic effects. In addition, after veterinarians call about difficult cases and become familiar with how to deal with a given toxicosis, they are unlikely to consult the network when similar incidents are encountered. Oud~~~eak Inves~ga~ In the l950s, Japanese veterinarians recognized a new disease in cats in the fishing village of Minimata. They called it Dancing cat fever, because the necrologic signs included twitching and involuntary jumping movements. The outbreak was not investigated promptly, and its cause remained a mystery for several years. Then a similar disease afflicted the people of Minimata, partic- ularly fishermen and their families. The similarities between the disease in humans and the disease in cats were recognized, and research was begun in cats to characterize its pathogenesis. Humans and animals that developed the disease had very high mercury concentrations in their brains, livers, and kid- neys. The disease was produced in various laboratory animals that were fed fish and shellfish from Minimata Bay. Environmental studies found high concentrations of organic mercury com- pounds in sediment from Minimata Bay, in the effluent from a nearby factory where mercuric chloride was used in the catalytic process of vinyl chloride production, and in fish taken from this area. A ban on fishing in Minimata Bay eliminated the disease in cats and people. The Minimata experience raised awareness of the possibility of organic mercury poisoning elsewhere and facilitated recognition of outbreaks in swine (Likosky et al., 1970) and people (NRC, 1979~. Canadian and Swedish veteri- narians documented unusually high mercury concentrations in fish from partic- ular lakes and rivers and recognized the potential human dangers as a result of the appearance of toxicoses in animal populations. Polychlorinated Biphenyls in Chickens In 1968, a disease outbreak in chickens in Japan was characterized by labored breathing, ruffled feathers, and decreased egg production; more than 400,000 chickens died. Lesions identified post mortem included subcutaneous

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FOOD ANIMALS AS SENTINELS 63 and pulmonary edema, hydropericardium, muscle ecchymoses, and a yellow mottling of the liver (Kohanawa et al., 1969a). Epidemiologic and laboratory studies found the cause to be animal feed to which had been added a brand of rice oil that contained high concentrations of PCBs (Kohanawa et al., 1969b). Shortly after the epidemic in chickens, an outbreak of skin disease similar to chIoracne was reported in 1,057 people in western Japan. Symptoms of the disease, known as ~yusho," included ocular discharges and swelling of the upper eyelid, which were followed by acneiform eruptions and pigmentation of the skin. The disease was chronically debilitating; by 1970, many patients had made no improvement. Several had serious complaints, such as persistent headaches, general fatigue and weakness, numbness of limbs, and weight loss (Kuratsune et al., 1972~. Extensive epidemiologic investigations revealed the cause to be the same source of rice oil that had been implicated in the out- break in chickens 6 months earlier. The PCBs were traced to leaking coils in a heating system that was used to deodorize the rice oil. Later studies have shown that the PCBs themselves were contaminated with polychlorinated dibenzofurans (PCDFs), which were probably the primary toxic agents (Masu- da, 1985~. PCDFs are structurally similar to polychlorinated dibenzo-p-dio~nns, which were responsible for similar outbreaks of poisoning among domestic chickens in the l950s (Firestone, 1973~. Correct identification of the toxic agents in- volved was delayed by difficulties in chemical analysis for the incidents in the l950s and in 1968. Polybrominated Biphenyls in Cattle In 1973, a Michigan dairy farmer purchased 65 tons of a protein supple- ment and fed it to his 400 cows. The cows had a marked decrease in milk production, appetite, and weight. Two months after the onset of signs, many animals were losing hair and had abnormal growth of their hooves. Pregnant animals had prolonged gestation and abnormal labor. Many calves were stillborn or died soon after birth (Sanborn et al., 1977~. Epidemiologic studies revealed that the protein supplement fed to the cows was contaminated with a fire retardant that contained polybrominated bi- phenyls (PBBs). The contamination occurred when the fire retardant was shipped inadvertently to the feed manufacturer instead of magnesium oxide, a feed constituent. By the time the mistake was discovered, however, contam- ~nated feed had been distributed to more than 1,000 operations in Michigan; eventually nearly 25,000 cattle, 3,500 swine, and 1,500,000 chickens had to be destroyed.

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64 ANIMALS AS SENTINELS The outbreak of PBB toxicosis in animals caused public-health officials to become concerned about PBB exposures of people via the food chain (Wolff et al., 1982~. The Michigan Department of Health continues to conduct long- term followup studies in human populations that were at risk of exposure. AM4LYTIC EPIDEMIOLOGIC STUDIES Sheep and Hem Metals A recent study of sheep living around a zinc smelter in Peru demonstrated the feasibility of establishing animal sentinels around point sources of pollu- tion (Reif et al., 1989~. Heavy-metal exposures were documented in sheep pastured up to 27 km downwind from the smelter. A mortality data base for the population of 177,000 sheep was used in an attempt to relate heavy-metal burdens to health effects, including cancer. No relationship between hepatic arsenic concentrations or other heavy metals was found for pulmonary adeno- carcinoma, a neoplasm hypothesized a priori to be related to arsenic exposure. Gem and Heavy Metals Animals and people on farms where sludge from sewage-treatment facilities is applied are exposed to a wide range of microrganisms and chemical agents. Furthermore, animals that are exposed to fields where sludge is applied for extended periods and that will be used to grow food might pass on sludge contaminants to consumers. Dorn et al. (1985) conducted a study to measure health effects of sludge applied to farmland. Dairy farms were assigned randomly, with 47 receiving sludge and 47 serving as controls. Sludge was spread at the rate of 2-10 dry metric tons/hectare; this application was repeated approximately once a year. On the basis of information gathered on monthly questionnaires, no differ- ences in human and animal health were observed between the sludge and control farms. But, as judged by regularly collected blood and fecal samples, cattle were more-sensitive indicators than humans of exposure to sludge-borne heavy metals (Ready and Dorn, 1985~. For example, no difference in cadmi- um intake was found between persons at sludge and control farms, but cattle grazing on sludge-treated pastures consumed 3 times more cadmium than cattle grazing on control pastures. Significantly higher cadmium and lead accumulations were found in the kidneys of calves grazing on sludge-treated pastures than in control calves. The investigators concluded that "higher appli-

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FOOD ANIMALS AS SENTINELS 65 cation rates of sludge than those used in this study would be expected to increase the amount of cadmium and lead translocation through the food chain and possibly cause a significant increase in human and animal illness.. ~ and Fly A disease in cattle resembling osteomalacia was observed by Bartolucci in 1912 (Shupe et al., 1979~. He noted that the affected animals were adjacent to a superphosphate factory; superphosphates often are highly contaminated with fluoride. Blakemore et al. (1948) noted an association between some industries, such as brick manufacturing, and fluorosis in British farm animals. Other industries have been associated with fluoride toxicosis, including alumi- num, steel, and copper smelting; chemical manufacture; ceramic production; and coal-based electricity generation (Shupe et al., 1979~. Dairy and beef cattle in the vicinity of such facilities have been severely affected by fluorosis as a result of airborne contamination of forages. These animals have been suitable sentinels of fluoride emissions and have been used by industry and regulatory agencies to assess the effectiveness of emission control measures. SU~AL4RY Some programs are generating data on chemical-contaminant concentra- tions in monitored foods, and these data can be used for human risk assess- ment (Roberts, 1989~. It is important to note that data on concentrations, as reported by monitoring programs and in several of the studies discussed in this chapter, are being used to assess the risks entailed in human consumption of potentially contaminated products. For example, fish in Lake Michigan (brown trout, lake trout, salmon, yellow perch, and walleye pike) provide data on pesticides (DDT, dieldrin, and chlordane) and PCBs in the lake. In addi- tion to providing information useful in determining the impact of contaminants on the food supply, those fish sentinels provide data that can be useful in determining the potential for human exposure and health risks. A study by the National Wildlife Federation (1989) calculated human exposure to contam- inants in fish from the Great Lakes; the calculations of exposure were used to derive estimates of risks of cancer and noncancer health effects. Some critics regard this approach as premature, although identification of hazards to human health was the primary purpose of conducting the monitoring pro- grams, which were initiated in the 1960s. Monitoring of food animals also yields invaluable data on environmental

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66 ANIMALS AS SENTINELS chemical accidents and other hazards. For example, reindeer in the Arctic and other foraging animals have been sentinels of radioactivity resulting from the April 1986 nuclear-reactor accident in Chernobyl, Ukraine, USSR, by virtue of the radioactivity in their flesh and milk. Those animals provide continuous data on radioactivity in northern Sweden; the data have been used to regulate human exposure. In many food-monitoring programs, the propor- tion of shipments sampled is very small. Moreover, the turnaround time is long, contaminated batches are shipped before the laboratories finish and report their analyses, and the analyses generally do not provide early warning of the presence of contaminants. In short, by the time the contamination problem is well recognized, the food is on the plate. Furthermore, in some programs, dietary composites, rather than individual animals, are analyzed, so it is difficult to trace a contamination problem to its source. The meaning of given amounts of contaminants in a food animal's body is difficult to deter- mine, other than that the animal has been exposed. The data do not provide information about the original dose received by the animal or the route by which the exposure occurred, nor can they usually reveal whether the animal was exposed recently. The animal-sentinel function of herds and flocks could and should be devel- oped further by including data related to environmental contaminants and animal exposures in the NAHMS. For example, an earlier NRC committee examined case histories regarding environmental chemicals in meat and poul- try. The case histories included PCB contamination through the addition of fatty animal byproducts to feed in the western United States in 1979 (USDA, 1980), the contamination of turkey products with chemical residues in the state of Washington during 1979 (USDA, 1980), and PBB contamination in Michi- gan (Sleight, 1979~. It was apparent in each instance that contamination occurred on the farm and that quicker measures than were possible in the traditional food-safety inspection system were needed to detect the contamina- tion. Given that those contaminants are likely to harm animal productivity and health, the NAHMS could be used to alert public-health officials to their presence. A one-state pilot study has shown that the MCI program could be coupled with a chemical-residue monitoring program. Existing samples of the MCI program provide a surplus of serum and unused red cells. The sizes of the samples could be increased, and samples of other tissues of slaughtered ani- mals could be collected and related to the same identifying backtags for other environmental monitoring purposes. The MCI program would continue to be an effective device for brucellosis detection and could become an effective mechanism for additional environmental monitoring purposes. Furthermore, its use would probably be less expensive than developing a program de nova;

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FOOD ANIMALS AS SENTINELS 67 although the program would need to be expanded, the tissues already are collected and tested, and unused portions of blood could all be used to test for pesticide and herbicide residues, heavy metals, and various other environ- mental contaminants. Such an expanded system would provide health officials with a widespread mechanism for monitoring pollutants and ultimately for protecting public health from environmental hazards.

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