et al.

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‡Health of Animals Laboratory, Health Canada, 110 Stone Road West, Guelph, Ontario, Canada, N1G ... obtained from other surveys of Canadian broiler flocks.
ENVIRONMENT AND HEALTH

Salmonella Prevalence in Crops of Ontario and Quebec Broiler Chickens at Slaughter1 J. R. CHAMBERS,*,2 J.-R. BISAILLON,† Y. LABBE´,† C. POPPE,‡ and C. F. LANGFORD*,§ *Southern Crop Protection and Food Research Centre, Research Branch, Agriculture and Agri-Food Canada, Box 3650, 95 Stone Road West, Guelph, Ontario, Canada, N1H 8J7; †Food Inspection Directorate, Canadian Food Inspection Agency, 59 Camelot Court, Nepean, Ontario, Canada, K1A 0Y9; ‡Health of Animals Laboratory, Health Canada, 110 Stone Road West, Guelph, Ontario, Canada, N1G 3W4; and §P.O. Box 68, Campbell’s Bay, Quebec, Canada, J0X 1K0 ABSTRACT Swabs of crop contents of 635 broiler chickens were obtained from 9 Ontario and 12 Quebec processing plants and cultured for Salmonella to determine prevalence in broiler crops. Serotypes of positive cultures were determined to evaluate the serotype profile. The overall prevalence of contamination was low (4.3%). Prevalence was higher in broilers sampled in Quebec (5.8%) than in those sampled in Ontario (2.2%). In Quebec, there were differences in prevalence among the groups of broilers sampled at the various plants. These differences were believed to be attributable to differences in Salmonella prevalence among groups of flocks delivered to the plants due to the limited exposure of the chickens to the plant. The serotype profile of Salmonella isolated from the crops of broilers in this study was similar in several respects to profiles

obtained from other surveys of Canadian broiler flocks using either environmental samples or cloacal swabs. Similarities included: predominance of Salmonella hadar and Salmonella heidelberg; several other common serotypes at a low prevalence; little Salmonella enteritidis isolated in other studies, and no S. enteritidis isolated in this study. Results of this field survey of Salmonella in crops of broilers are similar to those of Canadian studies of other internal and environmental sites of broilers. The similarity indicates that monitoring of Salmonella environments of flocks of live broiler chickens should define profiles of Salmonella contamination of the carcasses and would also aid in determination of Salmonella contamination status of broiler flocks. Such information would assist efforts to reduce Salmonella contamination in broiler chickens.

(Key words: Salmonella, prevalence, carcass contamination, broiler, crop) 1998 Poultry Science 77:1497–1501

INTRODUCTION Salmonella isolations from humans in the U.S. have risen steadily since 1955 and a fourfold increase had accrued by the 1990s (Centers for Disease Control, 1992). Globally, salmonellosis has remained one of the three most common meat-associated diseases in humans (Cooper, 1994). Infected chickens represent the greatest potential Salmonella hazard to public health (Suphabphant et al., 1983). Salmonella is often present in the intestinal tracts of mammals and birds, is readily acquired from feed and environmental sources, and contaminates body

Received for publication April 8, 1997. Accepted for publication May 7, 1998. 1Contribution number 2426 of the Centre for Food and Animal Research, Agriculture and Agri-Food Canada. 2To whom correspondence should be addressed: chambersj@em. agr.ca

parts of fowl on the farm (Bryan and Doyle, 1995). Canada is not exempt from this problem. Surveys of registered Canadian broiler flocks between December 1989 to May 1990 revealed that 226 of 300 (76.9%) randomly sampled flocks were contaminated with at least one of 50 different Salmonella serovars (Poppe et al., 1991a). Poultry carcasses sampled from federally inspected abattoirs across Canada between 1983 and 1986 revealed Salmonella contamination for 60.9% of broiler and 69.1% of turkey carcasses (Lammerding et al., 1988). In the live chicken, the ceca have been reported to be the primary predilection site of Salmonella colonization by several research teams (Brownell et al., 1969; Fanelli et al., 1971; Barrow et al., 1988; Xu et al., 1988). The cloaca (Snoeyenbos et al., 1982; Xu et al., 1988) and the crop

Abbreviation Key: BPW = Buffered Peptone Water; HACCP = Hazard Analysis Critical Control Points.

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(Snoeyenbos et al., 1982; Barrow et al., 1988; Impey and Mead, 1989) are also often commonly colonized; however, colonization of the crop is “highly transient” (Snoeyenbos et al., 1982) or less persistent (Barrow et al., 1988). On the other hand, rates of Salmonella contamination were either equal or much greater for crop vs cecal samples of 150 to 200 broilers from each of three commercial broiler flocks (Hargis et al., 1995). After contents of the intestines are voided, these enteric bacteria contribute to the surface contamination of carcasses. Carcass rinses prior to scalding indicate that Salmonella are firmly attached to contaminated chickens on arrival at the processing plant (Lillard, 1989). Rupture of contaminated crops during carcass evisceration also contributes to carcass contamination. Salmonella cross-contamination occurs among birds during transit to market (Bryan and Doyle, 1995). Transportation of broilers from the farm to the processing plant has been associated with increases in frequency and level of broiler crop contamination by Salmonella (Hargis et al., 1995) and levels of carcass surface contamination by Campylobacter (Stern et al., 1995). This increase in Salmonella frequency may be attributed to preslaughter feed restriction. Humphrey et al. (1993) reported increased frequency of recovery of Salmonella enteritidis from crops of chickens that had been deprived of feed for 24 h. Moreover, crops were reported to be 80 times more likely than ceca to rupture during evisceration (Hargis et al., 1995). The crop appears to be an important Critical Control Point in the prevention of Salmonella contamination of carcasses. From a Hazard Analysis Critical Control Point (HACCP) approach, elimination of Salmonella from chickens prior to their arrival at the plant would prevent much of the subsequent carcass contamination with Salmonella due either to surface contamination of the live chicken or to crop colonization. In situations in which only some flocks of chickens are contaminated, scheduling the slaughter of negative flocks ahead of positive flocks on a daily basis would reduce Salmonella contamination of carcasses. To achieve this status, a means of evaluating Salmonella contamination status of the live chicken is required. Cecal contents sampling of chickens is feasible during slaughter; however, there is no convenient method for sampling cecal contents of live chickens. Therefore, the crop of live chickens appears to be a choice site for monitoring Salmonella contamination through swab sampling. A Canadian survey was carried out to determine: 1) the average rate of crop contamination by Salmonella in broiler flocks at processing plants in Ontario and in Quebec, and 2) whether differences in rate of crop contamination of flocks existed between provinces and among broiler groups sampled at processing plants

3Starswab No. S131, Starplex Scientific, Etobicoke, ON, Canada, M9W 6Y3.

within provinces. In addition, positive samples were serotyped to assess the diversity of the Salmonella serotypes involved in broiler crop contaminations.

MATERIALS AND METHODS

Sampling Crop swabs were obtained from 635 broilers being processed at 9 Ontario and 12 Quebec processing plants. Plants contributed from 5 to 8 swabs per sample day with one plant providing 11 swabs on one date. Dates of sampling included 3 consecutive d in March and 12 d between May 1 and June 1. Crops were sampled from most of the processing plants on four of these dates; however, crops were sampled at two plants on three dates, two on five dates, and three on six dates.

Swab Procedure At the processing plant, swabs were collected after slaughter and plucking but prior to evisceration. At 1-h intervals, the 10th carcass subsequent to a carcass noted on the processing line was selected for crop swabbing. This carcass was removed from the line and had the crop removed manually. The esophagus at either end of the crop was tied closed to avoid escape of and carcass contamination by the contents. The crop was cut open using a sterile scalpel and the sterile swab (Microorganism Collection and Transport System, Starplex Scientific)3 was inserted into the contents of the crop and stirred to pick up material. Following removal from the crop, the swab was returned to the sterile test tube with “protective medium” and the stopper was replaced. The charcoal base of the “protective medium” (Microorganism Collection and Transport System) was expected to neutralize acidity of the crop contents and enhance the survival of enteric bacteria during shipment of the samples to the laboratory.

Swab Storage and Transport Following collection, tubes with swabs for a specific day were placed in refrigerated storage containers for shipment to a central laboratory for culturing to detect and isolate Salmonella.

Culturing Culture of samples commenced within 2 d of collection with the exception of collections from three processing plants on 1 d. The latter samples had culture initiated within 3 d of collection. On arrival at the laboratory, each swab was transferred to a tube containing 10 mL 1.0% Buffered Peptone Water (BPW) and the swab stem was cut with flamed scissors before vortexing the swab in the BPW. The swab in the tube was then incubated for 24 h at 35 C (pre-enrichment) before 0.1 mL of the incubated BPW was transferred to a

SALMONELLA PREVALENCE IN CROPS OF BROILERS TABLE 1. Presence of Salmonella in crops of broilers at processing plants in Ontario and Quebec1 Salmonella

Ontario

Quebec

Total

Positive Negative Total Percentage positive

6 267 273 2.2

21 341 362 5.8

27 608 635 4.3

1Chi-square

test of difference between provinces = x21 = 4.1178; (P