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cerned? APPENDIX H FOOD CONTAMINATION William E. Pace1 When considering the effects on human health of subtherapeuti~ use of antibiotics in animal feeds, the food scientist must first consider the order of events that could lead to possible adverse effects. To develop a systematic approach, one must face a number of questions that are ultimately related but do-not lend themselves to a simple sequential consideration. Among these are: With what potential human health effects should we be con Do epidemiological data indicate that real problems exist today or could exist in the future? ~ What diseases may be involved? Might the use of antibiotics in animal feeds play a direct or indirect role in increasing the incidence or in complicating the treatment of diseases? What lines of communication connect animals and humans in the chain of events that might result in manifestation of adverse effects? Do processing and storage significantly decrease antibio- tic residues? Are there beneficial effects from the presence of anti- biotics in.foods? Is the attention given to foods of foreign origin similar to that given to foods originating in the United States? use? What recommendations should be made regarding antibiotic Office of the Surgeon General, Headquarters, U.S. Air Force, Balling Air Force Base, Washington, D.C. 262

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263 CONCERNS There are two general areas of concern: the toxic effect of antibiotic residues and the potentiation of disease by anti- biotic-microorganisms. The former is far simpler to approach than is the latter. TOXIC EFFECTS Manifestation of a toxic effect requires only that a sus- ceptible individual be exposed to the antibiotic residues. Mercer (1975) reported that approximately 7.2X of a test popu- lation was hypersensitive to penicillin and that ingestion of as little as 10 units has produced mild reactions. Furthermore, he stated that neomycin has cross-sensitization properties with streptomycin and that 5.7% of a test population was sensitive to neomycin. These data alone are adequate to indicate that there is a strong and definite potential for toxic effects from anti- biotic residues. However, measures to control or eliminate such effects are relatively simple to define. Although the suscept- ibility of a population cannot be changed easily, steps can be taken to avoid or to minimize exposure. Most if not all of those steps are already in routine use. APPROVAL OF USE The use of antibiotics in animal feeds must be limited to those that are safe, have proven efficacy, and can readily be detected in the tissues or products of the animals receiving them. All of these criteria must be met before the Food and Drug Administration (FDA) will approve a New Animal Drug Application (NADA). After approval has been granted, our concerns must then turn to detecting illicit use (concentrations in feed exceeding those authorized, inadequate or improper mixing procedures, com- bining with unapproved additives, etc.), ensuring adherence to prescribed withdrawal periods, and sampling of market-ready pro- ducts for residue analyses. Responsibility for residue analysis of meats, poultry, and their products is vested in the U.S. De- partment of Agriculture (USDA). The FDA is responsible for analysis of dairy products.

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264 SAMPLING FOR RES IDUE ANALYSES Mussman (1973) stated that two types of sampling programs are used by the USDA. Each is designed to provide a different kind of information. One, an "objective" program, is aimed at determining the nationwide extent of a specific residue and identifying herds or flocks that require detailed examination. The other, a "selec- tive" program, is designed to define problems identified by the objective program. Analysis for specific antibiotics involves the combined use of bioassay and thin-layer or gas chromatographic techniques. EFFECTS OF PROCESSING AND STORAGE ON RES IDUES Morrison and Munro (1969) have commented on the destruction of drug residues in foods by food processing and storage. Liter- ature cited by them indicates that cooking causes significant reductions of tetracyclines in chicken, fish, and beef. Data presented by Mercer (1975) indicate a marked reduction in levels of penicillin in the kidney, liver, and muscle of chickens, swine, and lambs following frozen storage for as short a time as 8 days. In the United States, fresh poultry reaches the market within 1 to 2 days whereas fresh beef and pork require from 1 to 3 weeks. By intention, frozen products reach the market weeks or even months after processing. The changes in levels of antibiotic residues during storage and preparation add an additional margin of safety for the antibiotic-susceptible consumer. Assays must continue to be performed as quickly as possible after slaughter when residue levels are highest and most readily detectable. ANTIBIOTIC-RESISTANT MICROORGANISMS One must decide which organisms pose potential adverse health effects as a first step in considerations of antibiotic-resistant microorganisms. Since transferable antibiotic resistance is known to occur only in Gram-negative organisms (Baldwin, 1970), we can narrow our considerations relatively safely to those Gram-negative organisms found most frequently in meats and meat products. There- fore, the group is narrowed to some species of salmonellae, Shigella, coliforms, Vibrio, Campylobacter, Yersinia, Pasteurella, Brucella, Neisseria, Haemophilus, Pseudomonas, Achromobacter' Proteus, Flavo- bacterium, and Alcaligenes. Since the latter five are not known to include pathogens, we can probably afford to omit them from further consideration. The shigellae are well known as enteric pathogens,

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265 while the involvement of V~brio, Campylobacter, and Yersinia in gastrointestinal disturbance is becoming more apparent. Brucella in milk and dairy products must continue to be of concern because of brucellosis. The salmonellae and the coliforms (especially Escherichia coli) deserve our greatest attention, the former because they are known animal and human pathogens that are transferred between the two and the latter because they are almost ubiquitous, are routinely used as indicators of inadequate hygienic practices, are routinely present in the human alimentary tract, can easily transfer drug resistances, and have an increasingly recognized role in outbreaks of gastroin- testinal disorders in humans. Review articles and reports of origi- nal research (Groves et al., 1970; Gustafson, 1975; Howe et al., 1976; Kobland, 1975; Licczardello et al., 1968; Linton et al., 1977, in press; Newell and Williams, 1971; Patterson, 1969; Walton, 1970, 1971; Weissman and Carpenter, 1969) reveal an extremely wide varia- tion in the reported incidence of salmonellae and E. cold on animal carcasses in slaughterhouses or the ma rket. Figures for salmonellae incidence range from 34X for chickens (Licciardello et al., 1968) to 84% for pork carcasses (Kobland, 1975), and to 74% for beef carcasses (Weissman and Carpenter, 1969~. One paper cites a rate of 9X for carcasses of ducks and turkeys (Patterson, 1969~. Figures reported for the incidence of E. cold contamination range from 97X for pig carcasses (Walton, 1971), to 73% for beef carcasses (Walton, 1971), and to 81% for chicken carcasses (Lipton et al., in press). These variations appear to be due to differing levels of sanitation in processing plants, to the use or nonuse of bactericidal preparations in rinse waters and in chill tanks, to variations in sampling proce- dures, and to differences in culture techniques. Several of these authors also reported antibiotic resistance in E. cold in up to 58.57` of the isolates from chickens (Lipton et al., in press), up to 797 of those from pork (Walton, 1970), and up to 39% of those from cattle (Walton, 1970~. Antibiotic resistance was also reported in up to 23% of the salmonellae isolated from pigs (Kobland, 1975~. It is safe to conclude that both resistant_ cold and Salmonella can probably be found frequently in carcasses of all species of meat animals. There is little available data upon which to assess the level of contamination by these organisms. SOURCES OF CONTAMINANTS E. cold is routinely found in the gut of both domestic animals and humans. Even minor transgressions in proper sanitary practices in slaughterhouses readily result in contamination of carcasses,

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266 which most often results from spillage of intestinal contents during removal of the viscera. Salmonellae, while in no way "normal" inhabitants, are found in the intestinal tract of ani- mals very frequently. Most authorities agree that the primary source of salmonellae in domestic animals is contaminated feed or contaminated protein supplements. Groves et al. (1970), in a study of salmonellae contamination of slaughter pigs, reported isolation of the organisms from feed on 33% of the farms surveyed and in pigs from 33.3% of the farms (correlation between the two was not specified). Conversely, work cited by Edel et al. (1974) indicated that pigs gained little or no salmonellae infection from pelletized feed. However, they also cited data showing that the use of pelletized feed alone did not prevent salmonellae in- fections and concluded that environmental influences must also play a major role. Lapses in enforcement of proper hygienic practices rapidly lead from salmonellae and E. cold contamination of the gut to contamination of the carcasses, slaughter equipment, the slaugh- ter environment, and the processing environment to the finished product and on to the kitchens in private homes and institutions. There, unknown to the preparer, cross-contamination to other foods occurs frequently. The hide of cattle and the skin of hogs are routinely contam- inated by intestinal contents. Jensen and Hess (1941) concluded that these constituted the main source of organisms for carcass con- tamination. Intestinal contents also readily contaminate transp- ortation facilities and holding pens where other animals are subse- quently contaminated, many of which are young animals later shipped to farms or to heavily concentrated populations in fattening pens. During transportation animals are subjected to major stress and may become sick. The therapeutic use of certain antibiotics in treating these sick animals could lead to rapid dissemination of resistant strains if the animals are not isolated during therapy. Threlfall _ al. (1978) have proposed that similar circumstances might possibly have been involved in the recent outbreaks of salmonellosis in Britain involving the chloramphenicol-resistant strain of Salmo- nella phage type 204. Datta (1965) stated that some resistance factors carry resistance to as many as seven different drugs. Van Houweling (1967) noted that exposure to an antibiotic could result in transfer of resistance to other antibiotics as well because of the linkage of resistance genes. As early as 1943, Stuart and McNally showed that eggs are not contaminated by the parent bird during egg formation or laying.

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267 They confirmed that the egg, shell and all, is deposited in the nest in a sterile condition. Sound eggs from normal chickens are contaminated after laying by coming into contact with the external body or feet of birds or with the nest. Therefore, efforts to reduce contamination of shell eggs should be aimed at environmental factors rather than at the physiological processes of egg formation. VALUE OF ANTIBIOTICS IN FOODS Since there is no question regarding the potential dangers of antibiotic residues in foods, one must also ask whether such residues also have beneficial effects. Such effects have been clearly demonstrated. Chlortetracycline and oxytetracycline were formerly approved by the FDA in concentrations of 5 to 7 ppm for delaying microbial spoilage of fresh poultry, scallops, shrimp, and eviscerated fish. Approval for these uses was withdrawn in 1966 because small residues could sometimes be detected in the products after they were cooked. According to the Food, Drug, and Cosmetic Act, residues of any drug in tissues of animals re- ceiving the products are considered as food additives, the same as when they are added directly. Furthermore, the use of any food additive in a manner other than that approved by the FDA is regarded as an adulteration and renders the food ineligible for interstate shipment. An FDA-approved use of antibiotics will not result in the presence of residues (or at least not al ter a specified withdrawal period has been observed). CONTROLLING CONTAMINATION BY PATHOGENS One might ask whether antibiotics might be used in animal feeds to reduce the incidence of pathogens in the gut of live animals, hence reducing the potential for carcass and environ- mental contamination leading ultimately to the consumer. Smith and Tucker (1978) recently commented that the administration of feed containing neomycin to broilers a few days prior to slaugh- ter is being advocated and practiced in Britain as a means of reducing the proportion of birds shedding salmonellae. Their studies using 500 g/long ton (1,016 kg), i.e., 480 g/kg, for 9 days produced only a slight reduction. The use of 225 g/long ton ~ 221 g/kg) for 2 days also produced only a slight reduction in the proportion of birds shedding salmonellae but resulted in the emergence of enormous populations of E. cold that possessed

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268 multiple, transmissible-type antibiotic resistance in the ali- mentary tract of the treated chickens. Childers et al. (1977) suggested very strongly that environmental controls within the slaughterhouse are the most appropriate, and possibly the safest and simplest, means of reducing contamination of car- casses by pathogenic organisms. Transporting and holding swine in sanitized surroundings prior to slaughter did not effectively reduce contamination of carcasses with either salmonellae or E. colt. However, several relatively minor modifications of the evisceration procedures were effective in reducing contamination levels to between 12X and 20% as opposed to between 50% and 63% in control carcasses. The significant changes were the instilla- tion of greater care on the part of workers to avoid spillage of intestinal contents and to wash their hands and disinfect cutt- ing knives in chlorine solutions before handling a new carcass. Studies by Mosley et al. (1976) had indicated that hypochlorites and iodophors were similar in effectiveness and that both were superior to quaternary ammonium compounds in reducing levels of Gram-negative organisms, including salmonellae, on stainless- steel surfaces. INSPECTION OF FOREIGN-ORIGIN MEATS All control activities mentioned so far have concerned pro- ducts of U.S. origin. Since the volume of imported products is rather extensive, we should address this topic also. The respon- sibility for reviewing foreign programs regulating meat produc- tion and for inspecting imported meats, poultry, and products of meat and poultry is vested in the Foreign Programs Branch, Field Operations Division, Meat and Poultry Inspection Program, Food Safety and Quality Service of the USDA (McEnroe, 1971~. Review of foreign programs was initiated in 1966 to assess the effectiveness of meat and poultry inspection programs in those countries that desired to export their products to the United States. The Federal Meat Inspection Act of 1907, amended in 1938 and revised by the Wholesome Meat Act of 1967, requires that countries that export meats or meat products to the United States have facilities, sanitation standards, and inspection practices at least equal to our own. Section 20 of the Act also requires visits by U.S. experts to ensure compliance of foreign plants. In describing the program, Lyons (1971) stated that official certification by the USDA also requires the concurrence of the Department of State. Furthermore, foreign products are

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269 accepted only when the country's inspection program and the stan- dards in the processing plant have been certified as meeting U.S. standards. Most plants are visited at least annually. Those with minor problems are visited more frequently. Products originating from authorized plants in recognized countries must still be accompanied by a certificate signed by a qualified representative stating that the meat or meat product comes from animals that passed veterinary ante-mortem and post-mortem inspection, that it is wholesome and free of preservatives, and that it is otherwise in compliance with U.S. requirements. Meat products (but not fresh carcass meats) are then sampled at the port of entry by USDA officials and are sub- jected to incubation and to laboratory analyses for pesticides, antibiotics, and other chemical residues. Basically, the program relies on evaluation of the inspection program of the foreign coun- try, inspection of the plants of origin, reliance on the validity of certification, and dependence on the quality control programs of the importing U.S. firms. Microbial analyses would be performed only as part of the sampling programs discussed above. USDA officials do maintain close contact with their counter- parts in foreign countries and are well aware of the animal hus- bandry and food preservation practices in these countries. In case there are significant variances from our own practices, the inspec- tion program can be adjusted to focus on any specific problems that might be anticipated. The status of these programs was confirmed via personal communication (C. S. Johnson, Veterinary Staff Officer, Meat and Poultry Inspection Training Program, FSQS/USDA, Dinton, Texas, personal communication, 1979~. SUMMARY There is no question that the use of subtherapeutic levels of antibiotics in animal feeds has resulted in increasing the amount of animal protein available to the world's consumers. This increase is due to increased growth rates and to the control of low grade infections which often reduce the efficiency of feed utiliza- tion. On the other hand, it becomes more and more apparent that sanitation is the ultimate key to controlling initial levels of carcass and product contamination and that proper refrigeration is the key to controlling multiplication of those few unavoidable mi- crobial contaminants that will still continue to slip through. The use of antibiotics or other agents as preservatives or shelf-life extenders can be used too easily to cover up poor quality control

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270 or to compensate for inadequate or improper animal husbandry prac- tices. This may not hold entirely true in some developing nations where refrigeration and rapid transportation are less than adequate. In those cases, benefits to be gained would have to be balanced against the degree of risk involved. It appears that the primary need today is a vastly stepped-up educational program aimed at producers, processors, service person- nel, and consumers. Such a program must stress the importance of sanitation and personal hygiene at every step, the essentiality of avoiding cross-contamination, and the fact that products of animal- origin are not (and are not intended to be) sterile and must be handled accordingly. The effectiveness of public health programs in the United States has contributed greatly to a healthier popu- lation with an enhanced nutritional status, but they have also produced a nation of consumers who take for granted the safety of the products they consume and who know little about what precau- tionary measures they should take or why. Because the government has helped to create this problem, it has a responsibility to con- tinue to protect the consumers from themselves. RECOMMENDATIONS Frog the view of the food scientist, several recommendations are in order: 1. FDA's criteria for approval of NADA's should remain as they are. 2. Sampling for antibiotic residues in meats, poultry, and their products should be increased. 3. Sampling for pathogens and determination of their anti- biotic resistance should be significantly increased, especially for items of foreign origin. 4. USDA's Meat and Poultry Inspection Programs should place increased emphasis on in-plant sanitation, especially on measures that might reduce carcass contamination. 5. The Center for Disease Control should determine the anti- biotic resistance of cultures of all Gr~m-negative organisms involved in outbreaks of human illness (especially when food-borne transmis- sion is known or suspected). When unusual resistance patterns are recognized, follow-up epidemiological studies should be initiated to

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271 conf irm or to rule out involvement of subtherapeutic use of ant biotics in animal feeds. - 6. Intergovernmental exchange progran~s should be established to exchange data from studies recommended in 5. This is especially significant for countries that export or Sport foods for human consumption to or from the United States. 7 . FDA and state animal regulatory officials should strongly encourage isolation of animals that are on antibiotic therapy. 8. Extensive educational programs such as those descry bed in the summary should be initiated.

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272 REFERENCES Baldwin, R. A. 1970. The development of transferable drug re- sistance in Salmonella and its public health implications. J. Am. Vet. Med. Assoc. 157:1841-1853. Childers, A. B., E. E. Keahey, and A. W. Kotula. 1977. Reduc- tion of Salmonella and fecal contamination of pork during swine slaughter. J. Am. Vet. Med. Assoc. 171:1161-1164. Datta, N. 1965. Infectious drug resistance. Br. Med. Bull. 21: 254-259. Edel, W., M. van Schothorst, P. A. M. Guine, and E. H. Kampelmacher. 1974. Preventive measures to obtain Salmonella-free slaughter pigs. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg., I. Abt. Orig. Reihe B 158:568-577. Groves, B. I., N. A. Fish, and D. A. Barnum. 1970. An epidemiolog- ical study of Salmonella infection in swine in Ontario. Can. J. Public Health 61:396-401. Gustafson, R. H. 1975. Antibiotic sensitivity in Salmonella iso- lated from swine in a Pennsylvania slaughter house. Pp. 193-211 in Animal Industry Research Progress Report, AIR, Vol. 3. Pro- ject No. 3-721. American Cyanamid Company, Princeton, N.J. Howe, K., A. H. Linton, and A. D. Osborne. 1976. An investigation of calf carcass contamination by Escherichia cold from the gut contents at slaughter. J. Appl. Bacterial. 41:37-45. Jensen, L. B., and W. R. Hess. 1941. A study of ham souring. Food Res. 6:273-326. Kobland, J. D. 1975. Antibiotic sensitivity of salmonellae isolated from swine in an Iowa slaughter house. Pp. 291-321 in Animal Industry Research Progress Report, AIR, Vol. 3, Project No. 3-733. American Cyanamid Company, Princeton, N.J. Licciardello, J. J., J. T. R. Nickerson, and S. A. Goldblith. 1968. The Effect of Repeated Treatment with Gamma Rays on the Radio-Resistance, Virulence, and Culture Characteristics of Certain Pathogenic Bacteria. Final Report. Prepared by the Massachusetts Institute of Technology for the U.S. Atomic

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273 Energy Commission, Contract No. AT(30-1~-3325. NTIS No. MIT- 3325-40. National Technical Information Service, Springfield, Va. 152 pp. Linton, A. H., B. Handley, A. D. Osborne, B. G. Shaw, T. A. Roberts, and W. R. Hudson. 1977. Contamination of pig carcasses at two abattoirs by Escherichia cold with special reference to O-serotypes and antibiotic resistance. J. Appl. Bacteriol. 42:89-110. Linton, A. H., K. Howe, C. L. Hartley, M. Clements, and A. D. Osborne. In press. Antibiotic resistance and sensitive Escherichia cold O-serotypes in the gut and on the carcass of _ commercially slaughtered broiler chickens and the potential public health implications. Dept. of Bacteriology, University of Bristol, and Dept. of Veterinary Medicine, Langford House, Langford, Bristol. 35 pp. Lyons, J. P. 1971. U.S. Department of Agriculture controls over imported meats. J. Am. Vet. Med. Assoc. 159:1551-1555. McEnroe, K. M. 1971. A changing meat and poultry inspection pro- gram. J. Am. Vet. Med. Assoc. 159:1546-1550. Mercer, H. D. 1975. Antimicrobial drugs in food-producing animals. Control mechanisms of governmental agencies. Vet. Clin. N. Am. 5:3-34. Morrison, A. B., and I. C. Munro. 1969. Appraisal of the signifi- cance to man of drug residues in edible animal products. Pp. 255-269 in The Use of Drugs in Animal Feeds. Proceedings of a Symposium. Publication No. 1679, National Academy of Sciences, Washington, D.C. Mosley, E. B., P. R. Elliker, and H. Hays. 1976. Destruction of food spoilage, indicator and pathogenic organisms by various germicides in solution and on a stainless steel surface. J. Milk Food Technol. 39:830-836. Mussman, H. C. 1973. The changing face of meat and poultry inspection. J. Am. Vet. Med. Assoc. 163:1061-1064. Newell, K. W., and L. P. Williams, Jr. 1971. The control of salmonellae affecting swine and man. J. Am. Vet. Med. Assoc 158:89-98.

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274 Patterson, J. T. 1969. Salmonellae in meat and poultry, poultry plant cooling waters and effluents, and animal feedingstuffs. J. Appl. Bacteriol. 32:329-337. Smith, H. W., and J. F. Tucker. 1978. Oral administration of neo- mycin to chickens experimentally infected with Salmonella typhimurium. Vet. Rec. 102:354-356. Stuart, L. S., and E. H. McNally. 1943. Bacteriological studies on the egg shell. U.S. Egg Poult. Mag. 49:28-31, 45-47. Threlfall, E. J., L. R. Ward, and B. Rowe. 1978. Epidemic spread of a chloramphenicol-resistant strain of Salmonella typhimurium phage type 204 in bovine animals in Britain. Vet. Rec. 103: 438-440. Van Houweling, C. D. 1967. Drugs in animal feeds? A question without an answer. Food and Drug Administration Papers (Sep- tember):11-15. Walton, J. R. 1970. Contamination of meat carcasses by antibiotic- resistant colifor~ bacteria. Lance t 2:561-563. Walton, J. R. 1971. Part VI. Antibiotics and drug resistance in animals. The public health implications of drug-resistant bacteria in farm animals. Ann. N. Y. Acad. Sci. 132:358- 361. Weissman, M. A., and J. A. Carpenter. nellae in meat and meat products. 1969. Incidence of salmo Appl. Microbiol. 17:899-902.