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APPENDIX G TRANSMIS S ION OF FOOD-BORNE D ISEASE S IMPLICATIONS OF THE SUBT~RAPEUTIC USE OF ANTIMICROBIALS , Jackson S. Risers The major food-borne bacterial diseases in the United States are caused by salmonellae, staphylococci, and Clostridium botulinum (Center for Disease Control, 1977b) (Table 1~. The number of out- breaks of food poisoning by salmonellae and staphylococci is with- out doubt greatly underestimated because many outbreaks are unre- ported and undiagnosed. Because of its acute onset and rapid course, staphylococcal food poisoning, in particular, is not often brought to the attention of any medical authority. The statistics of C. botulinum food poisoning, because it is a much more serious disease in terms of its life-threatening poten- tial, are much more accurate. However, since there is no known or suspected connection between _ botulinum food poisoning and the use of antibiotics at subtherapeutic levels in animal feeds, it will not be discussed further in this paper. Salmonellosis is ubiquitous. It occurs usually as entero- colitis, usually of only a few days duration, and it is frequently caused by food-borne salmonellae. This form of salmonellosis is acutely uncomfortable and may cause humans to be absent from work for one or several days. The disease frequently involves a visit to a physician and, occasionally, hospitalization for a short period. It is generally agreed that antibiotic treatment is con- traindicated since it does not shorten the course of the disease or lessen the severity of the symptoms (Hook and Johnson, 1972~. Moreover, such treatment is likely to prolong the fecal excretion of the organisms (Aserkoff and Bennett, 1969~. SALMONELLOSIS IN FOOD ANIMALS AND HUMANS Salmonellae infect both warm-blooded and cold-blooded ani- mals. In 1977, 5,243 Salmonella isolates from nonhuman sources were reported to the U.S. Department of Agriculture (USDA) and the Center for Disease Control (CDC). Of the total nonhuman iso- lates, 28% (1,474) were obtained from chickens and turkeys, 25% (1,313) were of porcine origin, and 14X (713) were of bovine origin (CDC, 1979~. Five of the 10 serotypes most frequently isolated Consultant, Agricultural Division of American Cyanamid Co., Princeton, N.J. 203
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204 TABLE 1 Confirmed Outbreaks of Food-Borne Disease, by Etiology, 1976 Outbreaks t Cases Organism Number ~ Number %b Salmonella 28 21.2 1,169 32.7 Staphylococcus 26 19. 7 930 26.0 Clostridium botulinum 23 17.440 1.1 Clostridium perfringens 6 4.5509 14.2 Shigella 6 4.5273 7.6 Bacillus cereus 2 1. 563 1.8 Yersinia enterocolitica 1 0.8286 8.0 TOTAL 92 69.63,270 91.4 From Center for Disease Control, 1977b. Percent of all (bacterial, chemical, parasitic, and viral) food-borne disease outbreaks in the United States.
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205 from animals (Table 2) were also among the 10 serotypes most f requently isolated from humans (Table 3 ~ . S. typhimurium, in- cluding var. Copenhagen, comprised 35. 5% of the Herman isolates reported and 19. 7% of the isolates from nonhuman sources. It is by far the most frequently isolated serotype. Although the greatest number of isolates from nonhuman sources was obtained from swine, the inc idence of Salmonella In healthy market-ready swine varies greatly trom place to place. In 1975, a survey was conducted at a slaughterhouse in each of three hog-producing areas (Gustafson et al., 1976~. The purpose of the survey was to determine the incidence of Salmonella in healthy swine at market and to see what percent of them might be harboring salmonellae with resistance to more than one antibiotic. Of 151 hogs sampled in Pennsylvania, 54 (35.77) had salmonellae and none had multiply resistant salmonellae. Of 251 hogs sampled in Iowa, 26 (10.3%) had salmonellae and one had multiply resistant salmonellae. Of 256 hogs sampled in Georgia, 215 had salmonellae (83.9%) and 9 (3.5%) had multiply resistant salmonellae. These data suggest that only a few hogs harbor multiply antibiotic- resistant salmonellae. THE EFFECT OF SUBTHERAPEUTIC TETRACYCLINES ON SALMONELLAE IN _ DOMESTIC ANIMALS In April 1973, the Food and Drug Administration (FDA) issued a statement requiring the manufacturers of tetracyclines and cer- tain other drugs to show, by April 20, 1974, that the use of these drugs in animal feeds did not increase the Salmonella reservoir in animals and poultry raised for meat (FDA, 1973~. low. The FDA Bureau of Veterinary Medicine (BVM) then issued a set of human health safety criteria for the drug manufacturers to meet in order to demonstrate that the Salmonella reservoir in meat ani- mals was not increased by the subtherapeutic levels of the drugs in feed. BVM and the manufacturers designed protocols for experiments to determine the effect of the drug on the quantity, prevalence, and duration of shedding and the resistance characteristics of the Salmonella in animals consuming subEherapeutic levels of antibiotics in their feed. By April 20, 1974, these experiments had been con- ducted and the manufacturers had reported the results to the BVM. The experiments that were published are described briefly be
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206 TABLE 2 10 Someone Z Ma Serotypes Most Frequently Isolated from Nonhuman Sources, 1977 Serotype Number of isolates reported, by source b Feed Chickens Turkeys Swine Cattle TOTAL typhimurium ~10 67 17 194 310 1,033 anatum derby25 514 264 1 378 cholerae-suisd1 00 332 4 345 11 11107 69 24 314 agona3 2535 28 85 271 Heidelberg1 75113 3 1 236 saint-paul3 2182 7 1 219 san-die~o Panama 9 012 147 1 188 infantis 3 818 18 7 165 0 1104 1 0 112 . TOTAL 66 267 5921,063 4343,261 PERCENT OF TOTAL OF ALL SEROTYPE S ISOLATED 39 44 6881 6162 TOTAL OF ALL SEROTYPES ISOLATED 168 608 8661,313 7135,243 oFrom CDC, 1979. Also includes isolates from other animals and environmental samples. CIncludes var. Copenhagen. War. kunzendorf. . _
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207 TABLE 3 10 Sa~oneZZa Serotypes Most Frequently Isolated from Human Sources, 1977 1 i SerotypeNumber Percent Rank in 1976 typhimurium9,690 35.3 1 newport2,187 8.0 4 Heidelberg1,741 6.3 2 enteritidis1,472 5.4 5 infantis1,304 4.7 6 agona1,229 4.5 3 saint-paul580 2.1 7 typhi549 2.0 8 montevideo470 1.7 12 oranienburg440 1.6 9 TOTAL19,662 71.6 TOTAL OF ALL SEROTYPES27,462 a From CDC, 1979. bIncludes var. Copenhagen. 100
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208 EXPERIMENTS IN SWINE Gutzmann _ al. (1976) divided 30 5- to 6-week-old pigs, each weighing approximately 7 kg, into three groups of 10. One group was given chlortetracycline at 220 g/metric ton of feed. A second group was given AUREO S.P 250, at a level that supplied 110 g of chlortetracycline, 110 g of sulfamethazine, and 55 g of penicillin G per metric ton of feed. The third group was given the nonmedicated basal ration. On the sixth day of medication, all three groups were given in their feed 100 billion cfu (colony-forming units) per pig of a nalidixic- acid-resistant, tetracycline-sensitive strain of Salmonella typhi- murium of swine origin. A fourth group of 10 pigs from the same breeding was kept as an unmedicated, uninfected control. Fecal samples were taken at 1, 2, 6, 9, 15, 22, and 26 days after admin- istration to detect and enumerate salmonellae. As shown in Figure 1, chlortetracycline at 220 g/metric ton of feed substantially reduced the number of salmonellae shed. The effect of AUREO SeP 250 was somewhat less, but calculation of the total area under each curve, equivalent to the total number of sal- monellae shed by each group, showed a 22.5% reduction in the number of salmonellae shed by the group on chlortetracycline and a 9.6Z reduction in salmonellae shed by the group on AUREO S.P 250. The duration of shedding and number of animals shedding salmonellae was no different in the medicated than in the unmedicated groups. By plating the fecal samples on agar containing nalidixic acid and chlortetracycline, it was possible to learn whether the infecting salmonellae had acquired tetracycline resistance from the tetracy- cline-resistant E. cold which the pigs were known to have. Only a - few tetracycline-resistant Salmonella were found in six of 172 fecal samples, and these occurred in unmedicated as well as medi- cated pigs. Thus, it could be concluded that the drug had not selected for resistance. An experiment by another manufacturer (Evangelist) et al., 1975; Girard _ al., 1976) was conducted in a manner very similar to that described above except that oxytetracycline at 150 g/ton of feed or oxytetracycline at 150 g plus neomycin atj150 g/ton of feed was given to medicated groups. Figure 2 shows the quantity of Salmonella tYPhimurium shed. As in the previously described experiment the medicated groups shed substantially fewer salmonellae than did the unmedicated group.
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209 7 6 in 8 a, 5 - c' lo- 4 _ o 3 ; _ 2 _ 1 < Unmedicated in\ I\ AUREO S' P 250 (to supply 110 9 \ \ chlortetracycline, 1109 sulfametha zine and 55 9 penicillin G/metric If feed) \ ~ hi, Chlortetracycline, ZO g/metric ton of feed \ _N in, in_ -_ 1 1 1 1 1 1 1 1 2 6 9 15 22 26 DAYS (Postinoculation with 1 X 1 o1 1 cfu S. typhimurium) FIGl~RF 1. Summary of Salmonella typhimurium isolations from swine. From Gutzmann_ al., 1976, with permis- sion from the authors and the American Journal of Veterinary Research.
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210 J m - - 7r Unmedicated 6 4 \~ 1 lo Oxytetracycline _ 150 g/ton \ \ Neomycin + Oxytetracycline, ~50 9 each/ton - - - I I I 7 10 14 21 28 1 1 , DAYS (Postinoculation with 1.4 X 1 o1 1 salmonellae) FIGURE 2. Number of salmonellae recovered from swine feces. From Evangelisti et al., 1975, and Girard et al., 1976.
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211 There was no difference in duration of shedding between the medi- cated and unmedicated groups. Only two resistant isolates were de- tected in the medicated groups. None was seen in the unmedicated group. EXPERIMENTS IN CALVES . Layton et al. (1975) divided 24 4-week-old calves into three groups of eight calves each. One group was given 350 mg of chlortetracycline per head per day in feed, and the other group was given 350 mg of chlortetracycline plus 350 mg of sulfamethazine per head per day in feed. These levels were supplied by a weighed amount of a concentrate containing the desired amount of the anti- microbial. The third group was not medicated. After 5 days of medication, each calf 9as infected orally via stomach tube with approximately 6.5 x 10 cfu of a nalidixic-acid-resistant, anti- biotic-sensitive strain of Salmonella typhimurium of bovine ori gin. Fecal samples were obtained at 1, 2, 6, 9, 15, 22, and 26 days after infection and examined for the number of salmonellae. Figure 3 shows that the number of salmonellae from the medicated groups was lower than that from the unmedicated group at each sampling. The group on chlortetracycline shed 38.0Z fewer salmo- nellae. The group on the combination shed 28.6% fewer salmonel- lae. The duration and prevalence of shedding was slightly greater in the unmedicated than in the medicated group. Salmonellae that were resistant to chlortetracycline were recovered from five calves in the unmedicated group, three calves in the chlortetracycline- medicated group, and one calf in the group on the combination. Only a very small fraction of the salmonellae In any of these sam- ples was resistant, and in only two instances were resistant orga- nisms isolated more than once from the same calf. In no instance did the resistant organisms become established in a calf. In another experiment (Evangelist) et al., 1975; Girard et ale 1976), run in much the same way, three groups of 10 calves each, averaging approximately 85 kg per calf, were given feed containing oxytetracycline at 350 mg per head per day or oxytetracycline and neomycin in an amount calculated to give each calf 350 mg of each drug per head per day. One group was not medicated. The results of this experiment were very similar to the previously described experiment in calves. The number of salmonellae shed is shown in Figure 4. The duration and prevalence of shedding in the medicated groups were considerably less than in the unmedicated group. No tetracycline-resistant salmonellae were detected.
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212 .~ / J l 105 104 in LU c' 1 03 1o2 lo1 _ ~\ ~ \` \Nonmedicated \ ~ \ Chlortetracycline + Sulfamethazine \~350 mg each/head/day ~ \ Chlortetracycline, 350 mg/head/da~', 1 1 1 1 1 1 1 1 2 6 9 15 22 26 DAYS (Postinoculation with 6.5 X 109 cfu S. typhimurium) FIGURE 3. Salmonella typhimurium isolated from feces of infected . calves (expressed as geometric means). From Layton et al., 1975, with permission from the authors and Zentral- blatt fuer Veterinaermedizin Reibe B.
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213 6 . ~ 2 ~ 2 LL J m 4 o /\lonmedicated Oxytetracycl ins, 350 mg/head/day r~~l ~~ I ---r~~~'~l~~ 2 4 7 10 14 21 28 Neomycin + \ Oxytetracycline, 350 mg each/head/day ~' \/ ~-~ DAYS (Postinoculation with 1.10 X 1 o1 ] salmonellae) FIGURE 4. Number of salTnonellae recovered from calves feces. From Evangelisti et al., 1975, and Girard et al., 1976.
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252 1975 outbreaks of disease from Staphylococcus exceeded those from Salmonella, although Salmonella ranked first in 1976. Because staphylococcal enterotoxin is heat-stable, it is not destroyed by cooking. While meat products are frequently implicated in outbreaks of staphylococcal food-poisoning, investigation frequently reveals that the food has been contaminated by a food handler who is a carrier of an enterotoxin-producing strain of staphylococcus or who has a staphylococcus-infected wound (Bryan, 1978; CDC, 1977b). This contamination of meat by staphylococci of human origin was confirmed in a study by Sinell et al. (1975) in the Federal Republic of Germany. These investigators examined 3,065 cultures of staphylococci from slaughtered pigs, meat plant equipment, and other sources including human beings. Strains originating from swine produced significantly less (21%) enterotoxin than did strains from clinical specimens obtained in hospitals (approximately 40%~. Enterotoxin was not produced by any of 39 phage group II strains, a group that is considered to be specific to animals. The strains from animals were more frequently resistant to antibiotics than were the strains from the hospital. In 1973, before the German govern- ment banned the use of tetracycline in animal feed, there was a high incidence of resistance to tetracycline. In 1974, after the ban, a survey showed that the incidence of resistance to tetracycline in cultures from pigs had dropped but that the incidence of resistance to bacitracin had become very high. Strains of staphylococci iso- lated in a meat plant in 1974 continued to have a high incidence of resistance to both tetracycline and bacitracin. Domestic animals and pets can become carriers of strains of staphylococci of phage types that are frequently associated with human disease (Pagano et al., 1960~. During the school year 1956- 1957 an unusual number of senior students at the University of Pennsylvania School of Veterinary Medicine were afflicted with furuncles, deep cutaneous abscesses, cellulitis, and paronychia. The epidemic continued through the following 2 years. Staphylo- coccus aureus phage type 80/81 was repeatedly isolated from these . lesions. This strain was resistant to penicillin, streptomycin, the tetracyclines, and, occasionally, to erythromycin but was sensitive to chloramphenicol and novobiocin. A survey of students, faculty, and other employees of the school revealed that only the senior students who spent much of their time in the clinic and the faculty of the clinic had a high incidence of this strain in their external Hares. They frequently became carriers after contact with a student with an active lesion.
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253 Sporadic culturing of swabs from lesions of animals in the clinic revealed the existence of type 80/81 strain on only three occa- sions, whereas random swabbing of the nostrils of the animals failed to show it. In 1959 a systematic swabbing of the nostrils of the animals showed the strain to be present in cows, horses, goats, and, most frequently, in dogs. There was no proof that the organism was transmitted from an animal to a human. The animal-to-person transfer of antibiotic-resistant S. aureus of human type 80/81 was suggested by Wallace et al. (1962~. Eight of 287 cows tested yielded staphylococci type 80/81 with resistance to streptomycin, tetracycline, and penicillin, and sensitivity to chloramphenicol, neomycin, novobiocin, oleandomycin, and carbomycin. The cows all had mastitis. Some cases were so severe that the ani- mals had to be destroyed. Three people in the family that operated the dairy studied by Wallace _ al. also yielded type 80/81 with the same resistance pattern when swabs were taken from their nares and from two boils on the father at different times and from one boil and the sore throat of an 18-month-old child. Here again the spread from animal to per- son is putative. The organism could have spread from the humans to the animals. Antibiotic resistance in staphylococci from mastitic cows is common because large amounts of antibiotics are used in intramammary infusions to treat the mastitis, which may clear up but frequently recurs. Another study on antibiotic-resistant S. aureus from dairy herds was reported by Devriese and H~mmez (1975~. In 1971 and from July 1972 to June 1973 they isolated 68 methicillin-resistant strains of _ aureus from milk samples from mastitic cows in 20 Belgian dairy herds. In the 1972-1973 survey 52 methicillin-resistant strains were isolated on nine farms, representing 50% of all S. aureus iso- lated on those farms. A determination of the biological and phage- types of the methicillin-resistant strains suggested that they were actually strains from humans and might have had a common human source, but that seems highly speculative. In summary, food poisoning due to Staphylococcus aureus entero- toxin is frequently reported in the United States, England, and Wales. It often involves meat products, but upon investigation it is fre- quently found that the food was contaminated by a human carrier or one with a staphylococcal lesion. There is no evidence that the use of antibiotics in animal feed is in any way involved.
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254 Frequently, staphylococci of phase types usually considered to be of human origin have been found in pets and dairy cows. It is likely that these organisms were transferred from humans and were resistant when they were acquired by the cows, but they may have become resistant during treatment for mastitis by antibiotic intra- mammary infusion. It is highly unlikely that the resistance arose due to the use of antibiotics in the feed of the cows since that is a rather uncommon practice in the dairy industry in the United States. CONCLUSIONS Salmonellosis is the most important of the food-borne diseases that may be transmitted from animals to humans. There is a large pool of Salmonella in domestic animals, carcasses are contaminated with Salmonella at the slaughterhouse, and outbreaks of food-borne salmonellosis due to contaminated food of animal origin are a seri- ous threat to human health and an economic problem. It is not clear that the Salmonella on the food originated in the animals. Moreover, when antibiotic resistance has occurred, it does not seem to have been due to the use of antibiotics in animal feed. It seems likely that antibiotic-resistant E. cold in animals does not play a significant role in colonizing the human intestine. If these organisms do colonize temporarily, it is unlikely that they transfer their R factor to the human flora. Carcasses are contami- nated at the slaughterhouse with E. coli--some of which is resistant to antibiotics, but it is doubtful that more than a few of these organisms reach the consumer. The organisms on the meat are probably of human or environmental origin. Plasmids for antibiotic resistance and enterotoxin production can coexist in an _ cold cell and can be transferred together ex- perimentally. Cells containing both genes would have no survival advantage over cells containing the R factor alone in animals receiving antibiotics in feed since a high percentage of the cells would already be resistant. Food poisoning in the United States due to Staphylococcus enterotoxin is second only to salmonellosis as a food-borne disease. It often involves meat products, but upon investigation, it is fre- quently found that the food was contaminated by a human carrier or one with a Staphylococcus-infected lesion. Staphylococci of phase types usually considered to be of human origin have been found in pets and dairy cows. There is no evidence that the use of antibio- tics in animal feed is in any way involved.
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255 REFERENCES Anderson, E. S. 1968a. Drug resistance in Salmonella typhimurium and its implications. Br. Med. J. 3:333-339. Anderson, E. S. 1968b. Transferable drug resistance. Sci. J. 4: 71-76. Anderson, J. D., W. A. Gillespie, and M. H. Richmond. 1973. Chemo- therapy and antibiotic-resistance transfer between enterobac- teria in the human gastro-intestinal tract. J. Med. Microbiol. 6:461-473. Aserkoff, B., and J. V. Bennett. 1969. Effect of antibiotic therapy in acute salmonellosis on the fecal excretion of salmonellae. N. Engl. J. Med. 281:636-640. Bryan, F. L. 1978. Factors that contribute to outbreaks of food- borne disease. J. Food Protection 41:816-827. Center for Disease Control. 1975. Current trends. Microbiologic standards for raw ground beef, cold cuts and frankfurters. Reported by the U. S. Department of Agriculture and the Center for Disease Control. Morbid. Mortal. Weekly Rep. 24:229-230. Center for Disease Control. 1976a. Salmonella bovis-morbificans in precooked roasts of beef. Reported by P. J. Checko, J. N. Lewis, R. Altman, K. Black, H. Rosenfeld, W. Parkin, the U.S. Department of Agriculture, and the Center for Disease Control. Morbid. Mortal. Weekly Rep. 25:333-334. Center for Disease Control. 197 6b. Salmonella Surveillance Annual Summary 1975. Center for Disease Control, Atlanta, Ga. 51 pp. Center for Disease Control. 1977a. Follow-up on salmonellae in precooked roasts of beef. Reported by J. N. Lewis, R. Altman, D. O. Lyman, W. E. Parkin, the U. S. Department of Agriculture, the Food and Drug Administration, and the Center for Disease Control. Morbid. Mortal. Weekly Rep. 26:394-399. Center for Disease Control. 1977b. Food Borne and Water Borne Disease Outbreaks. Annual Summary 1976. Center for Disease Control, Atlanta, Ga. 82 pp.
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256 Center for Disease Control. 1977c. Multi-state outbreak of Sal- monella newport transmitted by precooked roasts of beef. Reported by P. J. Checko, J. N. Lewis, R. Altman, G. Halpin, R. Inglis, M. Pierce, K. Pilot, J. Prince, W. Rednor, M. Fleissner, D. O. Lyman, W. E. Parkin, the U. S. Department of Agriculture, and the Center for Disease Control. Morbid. Mor- tal. Weekly Rep. 26:277-278. Center for Disease Control. 1977d. Salmonella Surveillance Annual Summary 1976. Center for Disease Control, Atlanta, Ga.  pp. Center for Disease Control. 1977e. Salmonellosis associated with home-made ice cream--Michigan. Reported by R. Locey, P. Owens, G. Markakis, R. P. Daniels, D. F. Fuller, Jr., D. Muentener, N. S. Hayner, K. S. Read, and the Center for Disease Control. Morbid. Mortal. Weekly Rep. 26:94-99. Center for Disease Control. 197 7f. Salmonellosis--Kentucky. Re- ported by R. N. McLeod, W. L. Adams, L. M. Mullins, M. A. Shepherd, R. K. Bonner, B. F. Brown, N. J. Cambron, C. Hernandez, G. E. Killgore, J. W. Skaggs, [Kentucky] Epidemio- logical Notes and Reports 12~4~: 1, and the Center for Disease Control. Morbid. Mortal. Weekly Rep. 26:239. Center for Disease Control. 1979. Salmonella Surveillance Annual Summary 1977. Center for Disease Control, Atlanta, Ga.  PP Cherubin, C. E., M. Szmuness, and J. Winter. 1972. Antibiotic resistance of Salmonella. Northeastern United States--1970. N. Y. State J. Med. 72:369-372. Cherubin, C. E., J. F. Timoney, M. F. Sierra, P. Ma, J. Marr, and S. Shin. 1980. A sudden decline in ampicillin resistance in Salmonella typhimurium. J. Am. Med. Assoc. 243:439-442. Cooke, E. M., A. L. Breaden, R. A. Shooter, and S. M. O' Farrell. 1971. Antibiotic sensitivity of Escherichia cold isolated from animals, food, hospital patients, and normal people. Lance t 2:8-lO. Devriese, L. A., and J. Hommez. 1975. Epidemiology of methi- cillin-resistant Staphylococcus aureus in dairy herds. Res. Vet. Sci. 19:23-27.
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257 DuPont, H. L., H. West, D. G. Evans, J. Olarte, and D. J. Evans, Jr. 1978. Antimicrobial susceptibility of enterotoxigenic Escherichia colt. J. Antimicrob. Chemother. 4:100-102. Edel, W., M. van Schothorst, P. A. M. Guin£e, 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. Evangelisti, D. G., A. R. English, A. E. Girard, J. E. Lynch, and I. A. Solomons. 1975. Influence of subtherapeutic levels of oxytetracycline on Salmonella typhimurium in swine, calves, and chickens. Antimicrob. Agents Chemother. 8:664-672. Falkow, S., and C. Gyles. 1973. Studies on In viva transfer of the Ent plasmid. Progress Report. FDA contract number 73-210 M #1. Food and Drug Administration, Rockville, Md. Falkow, S., L. P. Williams, Jr., S. L. Seaman, and L. D. Rollins. 1976. Increased survival in calves of Escherichia cold K-12 carrying an Ent plasmid. Infect. Immun. 13:1005-1007. Finlayson, M. 1977. Salmonella in Alberta poultry products and their significance in human infections. Pp. 156-180 in Proceedings of the International Symposium on Salmonella and Prospects for Control, June 8-11, 1977, University of Guelph, Guelph, Ontario, Canada. Food and Drug Administration. 1973. Antibiotic and sulfonamide drugs in the feed of animals. Fed. Reg. 38:9811-9814. Galton, M. M., M. V. Smith, H. B. McElrath, and A. B. Hardy. 1954. Salmonella in swine, cattle and the environment of abattoirs. J. Infect. Dis. 95:236-245. Garside, J. S., R. F. Gordon, and J. F. Tucker. 1960. The emer- gence of resistant strains of Salmonella typhimurium in the tissues and alimentary tracts of chickens following the feeding of an antibiotic. Res. Vet. Sci. 1:184-199. Girard, A. E., A. R. English, D. G. Evangelisti, J. E. Lynch, and I. A. Solomons. 1976. Influence of subtherapeutic levels of a combination of neomycin and oxytetracycline on Salmonella typhimurium in swine, calves, and chickens. Antimicrob. Agents Chemother. 10:89-95.
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Representative terms from entire chapter: