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Salmonella 4:12:b: still have a relatively high prevalence. Prevention of ... Beetles observed during production or cleaning of the house (yes/no) . . . . . . Appearance of the ... chickens or the intestines from 50 weak or dead in shell chickens from ...
ENVIRONMENT AND HEALTH Risk Factors Associated with Salmonella enterica Serovar typhimurium Infection in Danish Broiler Flocks M. N. SKOV,*,1 Ø. ANGEN,*,2 M. CHRIE´L,† J. E. OLSEN,* and M. BISGAARD* *Department of Veterinary Microbiology, and †Department of Animal Science and Animal Health, Division of Ethology and Health, The Royal Veterinary and Agricultural University, Bu¨lowsvej 13, DK-1870 Frederiksberg C, Denmark ABSTRACT A retrospective longitudinal study was conducted to identify risk factors associated with Salmonella enterica serovar typhimurium (S. typhimurium) infection in Danish broiler flocks. The data included all broiler flocks slaughtered in 1995, and the epidemiological unit was the individual broiler flock. The S. typhimurium status was determined by microbiological examination of 60 fresh fecal samples. This procedure should detect an infected flock with a probability above 95%, if the prevalence is above 5%, and given that the sensitivity of the test is 100%. Nineteen variables were selected for analysis. Five factors and an interaction term were found significant by multivariate logistic regression analysis. An increased risk for S. typhimurium infection was associated with two parent flocks, one confirmed infected and one suspected of being infected with S. typhimurium, with two of the

hatcheries, and with five houses on the farm. An interaction between season and the previously mentioned hatcheries, and a random effect at farm level was also found to be statistically significant. Twelve variables were not found to be associated with S. typhimurium infection: medication, growth promoters, breed of the laying flock, animal density, size of the flock, area of the house, age of the house, geographical location of the farm, observation of beetles, number of days between disinfection and replacement, visual appearance of the bedding, and age of the chickens when they were tested for Salmonella. Three variables (feed mill, slaughterhouse, and Salmonella status of the preceding flock) were not evaluated in the multivariate analysis due to collinearity with other included variables.

(Key words: Salmonella, broiler, epidemiology, risk factors, Salmonella typhimurium) 1999 Poultry Science 78:848–854

Salmonella berta (Olsen et al., 1992), Salmonella enteritidis (Brown et al., 1994), Salmonella tennessee (Christensen et al., 1997), and Salmonella virchow (D. J. Brown et al., The Royal Veterinary and Agricultural University, Denmark, unpublished results) are examples of serotypes that have been successfully eliminated, whereas others, predominantly S. typhimurium, Salmonella infantis, and Salmonella 4:12:b: still have a relatively high prevalence. Prevention of Salmonella contamination of broilers requires detailed knowledge of the most important risk factors associated with its presence in the production system. A previous investigation has identified certain hatcheries and feed mills, size of farms in terms of number of houses, a positive Salmonella status of the preceding flock, and rearing of flocks in the autumn as important risk factors for S. enterica in broilers in Denmark (Angen et al., 1996). Data available at that time, however, did not allow serotype specific risk analysis. By the end of 1994, the detection procedure used to monitor the Salmonella status of the Danish broiler flocks

INTRODUCTION In Denmark, the incidence rate of human Salmonella enterica serovar typhimurium (S. typhimurium) infections has been increasing during the last decade. Next to S. enteritidis, S. typhimurium was the most frequently isolated serotype of S. enterica in 1995 (Anonymous, 1995a). Pork and poultry products are considered to be major sources of human infections with S. typhimurium (Baggesen and Wegener, 1994; Wegener et al., 1994). In order to reduce the level of S. enterica infection in broilers, a national eradication program has been implemented (Bisgaard, 1992). The program has been continuously upgraded, and although relapses have occurred, the program has resulted in decreasing prevalence of S. enterica in broilers (Anonymous, 1995a).

Received for publication August 13, 1998. Accepted for publication February 2, 1999. 1Present address: Danish Veterinary Laboratory, Hangøvej 2, DK˚ rhus N, Denmark. To whom correspondence should be 8200 A addressed: [email protected] 2Present address: Danish Veterinary Laboratory, Bu ¨ lowsvej 27, DK1790 København V, Denmark.

Abbreviation Key: AM = antemortem.

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was changed from analysis of cecal tonsils from 16 broilers per flock to analysis of 60 fresh fecal samples per flock. Results obtained by the improved sampling procedure are also recorded in the antemortem (AM) data base, described by Angen et al. (1996). Using the AM data base, the aim of the present investigation was to identify risk factors specifically associated with S. typhimurium infections in broiler flocks in Denmark.

MATERIALS AND METHODS

The AM Data Base The AM data base consists of flock data collected by veterinarians during their AM inspections, data from the slaughterhouses, and results from Salmonella examination of 60 fecal samples per flock collected at the age of approximately 3 weeks as previously described (Angen et al., 1996). In addition, 60% of the farms (representing 60% of the flocks) participated in the Flock Economy Control Program, in which different parameters related to the production are recorded. These data were also used in the present study.

sensitivity of the test is 100% (Martin et al., 1987). The flock was regarded as S. typhimurium-positive if one or more of a maximum of 60 Salmonella suspect colonies investigated per flock were identified as S. typhimurium. Detection and serotyping of S. enterica were performed according to the procedures recommended by the Nordic Committee on Food Analysis (1991).

Salmonella Status of the Parent Flocks During the production period, the parent flocks were screened for Salmonella. Meconium samples from 250 chickens or the intestines from 50 weak or dead in shell chickens from each parent flock were examined every 2nd wk. If one of these samples tested Salmonella positive, the parent flock was suspected of being infected with Salmonella. Sixty hens per subunit (section or house) of the parent flock were subsequently killed and submitted for bacteriological confirmation. If S. enterica was isolated from one or more killed birds, the chickens in the Salmonella-positive sections or houses were confirmed as infected and subsequently killed.

Selection of Variables Salmonella Status of Broiler Flocks The Salmonella status of the flocks was based upon examination of 12 pools each consisting of five fresh fecal samples taken by the farmer at the flock age of approximately 3 wk (2.7 wk in average, SE = 6 d). This sample size will detect an infected flock with a probability > 95%, if the prevalence is above 5%, and given that the

The selection of variables was based on previous studies (Angen et al., 1996). Nineteen variables were initially selected for use in a multivariate analysis (Table 1). In addition to the variables used in the study of Angen et al. (1996), the following new variables were included: breed of the parent flock, medication (yes/no), growth promoters used, identification number of the parent flocks

TABLE 1. Variables selected for initial analysis, including distribution of the continuous variables for 3,839 Danish broiler flocks Variables

Mean (range)

SD

Hatchery Feed mill Season (date of the AM2 inspection) Slaughterhouse of the preceding flock ST3 status of the preceding flock AM district (geographical location of the farm) ID4 number of the parent flock from which the broiler flock was derived (No. 1-127) Breed of the parent flock Medication (yes/no) Name of growth promoters used Beetles observed during production or cleaning of the house (yes/no) Appearance of the bedding (hard/wet/dry or dry and hard) Number of houses on the farm Animal density, broilers/m2 Flock size, number of chickens placed Area of the house, m2 Age of the house, yr of construction Days between disinfection and replacement The age of the broilers when Salmonella tested, d

. . .1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 (1 to 9) 27.4 (4.6 to 49.5) 28,753 (1,1100 to 72,213) 1,202 (151 to 2,800) 1979 (1935 to 1995) 11.7 (1 to 95) 18.7 (1 to 52)

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25 3.3 13,708 509 10.4 6.7 6.1

1Not

applicable. = antemortem. 3ST = Salmonella typhimurium. 4ID = identification number of the parent flock. 5Rounded figures. 2AM

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from which the respective broiler flocks originated, and a random effect at the farm level.

Descriptive statistics of the continuous variables not included in the final model are shown in Tables 1 and 2. The prevalence of S. typhimurium in relation to the

Definition of the Data Sets The data base, provided by the Danish Poultry Council, initially contained information on 4,221 flocks, all of which had been visited by the AM veterinarians in 1995. The uni- and bivariate analyses were based on 3,839 flock observations for which the Salmonella status of the individual flocks was known. The multivariate analysis was based on 2,776 flock observations, excluding flocks with missing values.

TABLE 2. Descriptive statistics for variables which were significant (P < 0.20) in the bivariate analysis, but not included in the final logistic regression model; 3,839 Danish broiler flocks, 1995

Variable1

Level

Percentage of flocks

Density