Research Note: Incidence, Number, and Serotypes of Salmonella on Frozen Broiler Chickens at Retail1 A. L. E A T , 2 J. M. KOPEK, and J. D. McGINNIS Department of Animal and Poultry Sciences, University of Arkansas, Fayettevitte, Arkansas 72701 (Received for publication October 15, 1990)
1991 Poultry Science 70:1438-1440
rized according to source, including chickens, turkeys, swine, cattle, and other categories. Numerous surveys have been conducted to Fifty-two percent of over 9,000 isolates came estimate the percentage of various food prodfrom poultry. The top five isolates not adapted ucts contaminated with pathogenic organisms to host from chickens were (in order) 5. during production, through the various phases Heidelberg, Salmonella hadar, Salmonella of processing, and at retail. The organism most typhimurium, Salmonella enteritidis, and Salwidely studied in the area of poultry producmonella berta. These serotypes represent 54% tion and processing is Salmonella. From 1983 of the isolates from chicken. Kvenberg and to 1986, Lammerding et al. (1988) isolated Archer (1987) reported that the top five human Salmonella from 61% of retail broiler carisolates reported to the Centers for Disease casses sampled in Canada. A salmoneUae Control in 1985 were (in order) S. typhimuriincidence rate of 79% has been reported in the um, S. enteriditis, S. heidelberg, Salmonella United Kingdom (Roberts, 1982). In the newport, and Salmonella agona. United States, Silliker (1982) and Engel (1987) The literature contains several estimates on sampled frozen and refrigerated broiler carcasses and found incidence rates ranging from the incidence rates and serotypes of Salmo30 to 50%. Izat et al. (1989) evaluated prechill nella commonly associated with poultry. There broiler carcasses at a commercial processing are also a few studies that include data plant and found that 16 to 100% of the indicating the extent to which broiler carcasses carcasses were positive for salmoneUae de- are contaminated with Salmonella (Surkiewicz et al., 1969; Notermans et al., 1975; Mulder et pending on the particular sampling day. al, 1977). Salmonella Heidelberg, Salmonella saintAnother topic that has not been investigated paul, and Salmonella Johannesburg are sero- or challenged is the claims made by certain types frequently isolated from chickens and "organic" or "natural" poultry producers and turkeys (Jay, 1986). In the 1985 annual survey processors that their broilers are "cleaner". The by the Centers for Disease Control (1987), objective of the foUowing study was to nonhuman salmoneUae isolates were catego- investigate the incidence, number, and serotypes of Salmonella on broUer chickens avaUable at retail, including one brand of product that was produced and processed by natural or i Published with the approval of the director, Arkansas organic means. The information gained from Agricultural Experiment Station, Fayetteville, AR. the present study should provide useful inforZTo whom correspondence should be addressed. INTRODUCTION
1438
Downloaded from http://ps.oxfordjournals.org/ at New York University on June 4, 2015
ABSTRACT Two similar trials were conducted to evaluate broiler carcasses at retail for incidence, number, and serotypes of salmoneUae. Twelve frozen carcasses were purchased from each of three retail outlets on two sampling days. Two of the brands purchased were produced and processed conventionally, but the third brand was produced and processed under organic conditions. The frozen carcasses were tempered to 4.4 C prior to microbiological sampling. All carcasses were sampled using a mechanical shaker and 100 mL of sterile water. Recovered rinse fluid was evaluated for levels of salmoneUae using a three-tube most probable number technique. All recovered Salmonella isolates were serotyped using the Kauffmann-White scheme. Incidence rates across the three brands ranged from 17 to 50%, with most probable number of salmoneUae per 100 mL of recovered rinse fluid ranging from 5 to 34 organisms. Serotypes recovered include Salmonella typhimurium, Salmonella paratyphi, and Salmonella arizonae. (?Cey words: salmoneUae, retail, incidence, levels, serotypes)
1439
RESEARCH NOTE
mation to the poultry processor, health administrator, and consumer. MATERIALS AND METHODS
'All prepared media from Difco, Detroit, MI 48201.
RESULTS AND DISCUSSION
The number of salmonellae found on each carcass was extremely low; the percentage of salmonellae-positive carcasses across the three brands ranged from 17 to 50% (Table 1), about the United States industry average as shown in previous surveys (Silliker, 1982; Engel, 1987). In both trials there were no significant differences in incidence rates or levels of salmonellae among the three brands. However, there was a significant difference in level of salmonellae between Trials 1 (MPN of .23/ mL) and 2 (MPN of .06/mL) for Brand A. Levels of salmonellae across the three brands ranged from 5 to 34 organisms per 100 mL of recovered rinse fluid (Table 1). The salmonellae incidence rates and levels on the carcasses at retail were the same regardless of rearing and processing conditions (commercial compared with organic). The specific serotypes of salmonellae found on the chickens were S. typhimurium, Salmo-
Downloaded from http://ps.oxfordjournals.org/ at New York University on June 4, 2015
Two brands of commercially grown and processed broiler chickens (Brands A and B) and a third brand of organic broiler chickens (Brand C) were purchased from three retail locations in the Fayetteville, Arkansas area on two sampling days. Sampling days were 2 wk apart, and on each sampling day 12 carcasses of each of the three brands were purchased. A total of 24 broiler chickens of each of the three brands was purchased on the 2 sampling days. Brand C claimed to be raised free of drugs, growth stimulants, antibiotics, or hormones and chickens received a diet that included no animal by-products. This brand of chicken was also raised in a more spacious environment than the typical chicken and was processed entirely by hand, which the manufacturer states "is a lot cleaner" than the conventional automated systems. All of this information was printed on literature distributed with the purchased product. The organic chickens were inspected by the USDA and scalded in a conventional scalder but were chilled in stationary batches of 300 carcasses for 12 to 24 h. The organic brand of chicken was purchased from a wholesale health food store. All carcasses were marketed as whole icepacked product, but all carcasses had actually been subjected to freezing at the retail outlets prior to purchase and were frozen at the time of purchase. Thus, all carcasses were tempered to 4.4 C for 24 h prior to microbiological testing. The retailers of all three brands received the carcasses prepackaged. Each of the chickens was evaluated for the presence or absence of salmonellae, the number of salmonellae recovered in a single whole carcass rinse, and the specific serotypes of Salmonella present. A whole carcassrinseprocedure (Cox et al., 1983) was used to sample each carcass. Carcasses were rinsed with 100 mL of sterile water using a mechanical shaker (Dickens et al, 1985). At least 80 mL of rinse fluid was recovered from all carcasses. Rinse samples were subjected to a three-tube most probable number (MPN) procedure (Oblinger and Koburger, 1984) in selenite cystine.3 Rinse
samples were not preenriched in lactose broth prior to direct enrichment in selenite cystine because there is evidence that preenrichment in lactose broth is not necessary for recovery of salmonellae from frozen broiler carcasses (Cox and Mercuri, 1979). Enriched samples were incubated for 24 h at 37 C. After incubation a loopful of sample was streaked onto xylose lysine desoxycholate and hektoen enteric agar plates that were incubated for 24 h at 37 C. At least two suspect colonies from each plate were streaked and stabbed into triple sugar iron and lysine iron agar slants. Slants were incubated for 24 h at 37 C. Colonies from slants exhibiting typical salmonellae reactions were confirmed serologically and biochemically (Food and Drug Administration, 1984). The lower detection level for salmonellae (MPN) was .03 organisms/mL of carcass rinse fluid. Confirmed isolates were sent to a USDA-approved Salmonella laboratory for identification of serotypes using the Kauffmann-White scheme (Jay, 1986). Incidence data among brands and between trials (sampling days) was analyzed using the chi-square analysis (SAS Institute, 1982). Numbers of salmonellae among brands and between trials was analyzed using die General Linear Model (GLM) procedure and means separated using Least Squares Means (LSMEANS) procedure which uses repeated t tests (SAS Institute, 1982).
1440
EAT ET AL. TABLE 1. Incidence, number, and serotypes of Salmonella on frozen chicken broilers at retail
Trial
Brand A Incidence2 MPN3
Brand B Incidence MPN
Brand C Incidence MPN
2/12 -23 a 3/12 .09 6/12 .34 3/12 .0(P 3/12 £7 4/12 .05 ab ' Indicates a significant difference in levels of salmonellae between Trials 1 and 2 (P£.05). No other differences in levels or incidence rates between trials or among brands were observed. 1 Whole broiler carcasses purchased frozen and tempered to 4.4 C prior to microbiological examination. Brands A and B were commercially grown and processed; Brand C was "organically" grown and processed by hand. ^Designates the number of carcasses from which salmonellae could be recovered out of the total number sampled. 3 Most probable number (MPN) of salmonellae per milliliter of recovered rinse fluid using a whole carcass rinse procedure and a three-tube MPN technique. The lower detection levels was .03 organisms/mL of carcass rinse fluid. 1 2
ACKNOWLEDGMENT
This study was funded under the USDACSRS Special Research Grants Program, Number 8902384. REFERENCES Centers for Disease Control, 1987. Salmonella Surveillance Report-1985. Annual Summary, Centers for Disease Control, U.S. Department of Health and Human Services, Washington, DC. Cox, N. A., and A. J. Mercuri, 1979. Research Note: Recovering low levels of various Salmonella serotypes from deep-frozen broiler carcasses by direct enrichment. J. Food Prot. 42:660-661. Cox, N. A., J. E. Thomson, and J. S. Bailey, 1983. Procedure for isolation and identification of Salmonella from poultry carcasses. Agriculture Handbook No. 603. USDA, Agriculture Research Service, Washington, DC. Dickens, J. A., N. A. Cox, J. S. Bailey, and J. E. Thomson, 1985. Automated microbiological sampling of broiler carcasses. Poultry Sci. 64:1116-1120.
Engel, R. E., 1987. Final report of the 1982-1984 national survey of Salmonella in broilers. Food Safety Inspection Service 2630-5(12.79). USDA, Washington, DC. Food and Drag Administration, 1984. Bacteriological Analytical Manual. 6th ed. Food and Drug Administration, Association of Official Analytical Chemists, Arlington, VA. Izat, A. L., C. D. Driggers, M. Colberg, M. A. Reiber, and M. H. Adams, 1989. Comparison of the DNA probe to culture methods for the detection of Salmonella on poultry carcasses and processing waters. J. Food Prot. 52:564-570. Jay, J. M., 1986. Food-borne gastroenteritis caused by Salmonella and Escherichia. Pages 489-514 in: Modern Food Microbiology. 3rd ed. Van Nostrand Reinhold Co., Inc., New York, NY. Kvenberg, J. E., and D. A. Archer, 1987. Economic impact of colonization control on foodbome disease. Food Technol. 41:79-98. Lammerding, A. M , M. M. Garcia, E. D. Mann, Y. Robinson, W. J. Dorward, R. B. Truscott, and F. Tittiger, 1988. Prevalence of Salmonella and thermophilic Campylobacter in fresh pork, beef, veal and poultry in Canada. J. Food Prot 51:47-52. Mulder, R.W.A.W., S. Notermans, and E. H. Kampelmacher, 1977. Inactivarion of salmonellae on chilled and deep frozen broiler carcasses by irradiation. J. Appl. Bacteriol. 42:179-185. Notermans, S., M. Van Schothorst, F. M. Van Leusden, and E. H. Kampelmacher, 1975. Onderzoekingen over net kwantitatief voorkomen van salmonellae bij diepvrieskuikens. Tijdschr. Diergeneesk 100: 648-653. Oblinger, J. L., and J. A. Koburger, 1984. The most probable number technique. Pages 99-111 in: Compendium of Methods for the Microbiological Examination of Foods. 2nd ed. M. L. Speck, ed. American Public Health Association, Inc., Washington, DC. Roberts, D., 1982. Factors contributing to outbreaks of food poisoning in England and Wales 1970-1979. J. Hyg. 89:491-498. SAS Institute, 1982. SAS® User's Guide: Statistics, Version 5 Edition. SAS Institute, Inc., Cary, NC. Silliker, J. H., 1982. The Salmonella problem: Current status and future direction. J. Food Prot 45:661-666. Surktewicz, B. F., R. W. Johnston, A. B. Moran, and G. W. Kromm, 1969. A bacteriological survey of chicken eviscerating plants. Food Technol. 23:80-85.
Downloaded from http://ps.oxfordjournals.org/ at New York University on June 4, 2015
nella paratyphi, and Salmonella arizonae. Salmonellae arizonae was isolated from at least one carcass from each of the three brands on both of the sampling days. Salmonella typhimurium was isolated from Brand C only on each of the sampling days. Salmonella paratyphi was isolated from Brands A and B on each of the two sampling days. The findings from the study suggest that chicken is sometimes contaminated with salmonellae but that the levels are extremely low. With proper handling and cooking procedures the consumer can eliminate any potential hazard. These findings also suggest that "natural" or "organic" chicken is not contaminated with salmonellae to any lesser degree than conventionally processed products; however serotypes present may differ.