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The role of animal movement, including off-farm rearing of heifers, in the interherd transmission of multidrug-resistant Salmonella

B. Adhikari^*, T. E. Besser, J. M. Gay^*, L. K. Fox^*, M. A. Davis, R. N. Cobbold, A. C. B. Berge^* and D. D. Hancock^*,1

^* AAHP, Field Disease Investigation Unit, Department of Veterinary Clinical Sciences, Washington State University, Pullman 99164
Department of Veterinary Microbiology and Pathology, Washington State University, Pullman 99164
School of Veterinary Science, The University of Queensland, Brisbane, Queensland 4072, Australia

¹ Corresponding author: hancock{at}wsu.edu

	ABSTRACT

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Fifty-nine commercial dairy farms were sampled 7 times over 15 to 21 mo to determine the role of animal movement, including off-farm rearing of heifers, in the interherd transmission of multidrug-resistant (MDR) Salmonella spp. Farm management data were collected by on-site inspections and questionnaires on herd management practices before and after the study. Forty-four percent (26/59) of herds did not acquire any new MDR Salmonella strains. The number of newly introduced MDR Salmonella strains acquired by the remaining 56% (33/59) of herds ranged from 1 to 8. Logistic regression models indicated that off-farm heifer raising, including contract heifer raising where heifers commingle with cattle from other farms [commingled heifers, odds ratio (OR) = 8.9, 95% confidence interval (CI): 2.4, 32.80], and herd size per 100-animal increment (herd size, OR = 1.04, 95% CI, 1.01, 1.05) were significantly associated with the introduction of new MDR Salmonella strains. The negative binomial regression similarly revealed that commingled heifers [relative risk (RR) = 2.3, 95% CI: 1.1, 4.7], herd size per 100 animals (RR = 1.02, 95% CI, 1.01, 1.03), and a history of clinical salmonellosis diagnosed before the study (RR = 2.5, 95% CI, 1.3, 5.0) were significantly associated with the number of new MDR Salmonella strains that were introduced. Factors not associated with the introduction of new MDR Salmonella strains were housing of heifers and cows in the same close-up pen, a common hospital-maternity pen, and the number of purchased cattle. This study highlights the role of animal movement in the interherd transmission of MDR Salmonella spp.

Key Words: multidrug-resistant Salmonella • dairy farm • herd-level risk factor

	INTRODUCTION

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An estimated 1.4 million human salmonellosis cases and over 500 associated deaths occur annually in the United States (Mead et al., 1999; ERS/USDA, 2001). Salmonella enterica is often found in livestock and poultry, including dairy cattle. Nontyphoidal salmonellosis can result from infection by numerous Salmonella serovars, which are often transmitted via contaminated meat and milk (Mazurek et al., 2004; CDC, 2006; Van Kessel et al., 2007) or through direct contact with infected dairy cattle (Wall et al., 1994; Besser et al., 1997; Calvert et al., 1998). Because most infections result in asymptomatic or self-limiting diarrhea, antibiotics should be used only in immunocompromised patients and cases of systemic salmonellosis (Ruiz et al., 2004). Multidrug-resistant (MDR) Salmonella strains can further complicate the treatment of human cases of salmonellosis (Butaye et al., 2006).

Increasing travel and global trade may facilitate the introduction of new Salmonella serovars into importing countries. Reports of emerging MDR Salmonella strains and global spread have been documented (Hancock et al., 2000; Davis et al., 2007). In particular, inter-farm transmission may be a key element in the epidemiology of MDR Salmonella. Some investigators have suggested that the spread of emerging MDR Salmonella between regions is due to international travel and trade (Davis et al., 1999) and is facilitated by the use of antimicrobials. Transmission of non-foodborne Salmonella infection may be attributed to contact with animals, contaminated water, or the environment (Wall et al., 1995; Besser et al., 2000; Fey et al., 2000; Rice et al., 2003; Hendriksen et al., 2004). Previous studies indicated that wild birds and hedgehogs can play a role in the transmission of salmonellosis (Søbstad et al., 2000; Handeland et al., 2002; Boqvist and Vågsholm, 2005) but little is known about the extent of their influence on Washington State dairies. Risk factors have been identified in the transmission of MDR Salmonella between farms. Introduction of newly purchased cattle to the farm has been reported as one of the primary routes of Salmonella transmission (Evans, 1996; Zansky et al., 2002; Vanselow et al., 2007). Some evidence suggests that off-farm raising of heifer calves presents a similar risk of introduction (Hegde et al., 2005). Approximately 12.5% of US dairy farms send their heifer calves off-farm to be reared at dedicated contracted calf ranches where the heifers are commingled with other animals from source facilities (Wolf, 2003; USDA, 2007).

During the last decade there has been an alarming increase in the appearance of antibiotic-resistant Salmonella that may be a consequence of selective pressure associated with the use of antimicrobial agents in food animals (Varma et al., 2005). Increased morbidity and mortality may result in an inability to treat salmonellosis due to antimicrobial resistance. Investigators have also reported that antimicrobial-resistant strains may be more virulent and cause more prolonged or more severe illness than antimicrobial-susceptible strains (Travers and Barza, 2002). The purpose of this study was to determine the role of animal movement, including off-farm rearing of heifers, in the interherd transmission of MDR Salmonella spp.

	MATERIALS AND METHODS

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Study Farms
Sixty commercial dairy farms in Washington State were enrolled into the study using the following selection criteria: farm located within Washington State and operated as a commercial dairy farm. According to the Dairy Farmers of Washington (2007; http://www.havemilk.com), there were 496 dairy farms and 238,000 milk cows in Washington. Sample size calculation was performed as described previously (Christensen and Gardner, 2000) with consideration of the herd-level sensitivity (0.95), expected disease prevalence (8% or more), and expected test sensitivity (0.5). These farms represented 173,253 dairy cattle in Washington State. Dairy farms were selected across the 3 major dairy areas (western, central, and south-central) of the state, proportional to the total dairy farms in that region. Sixty-six farms were randomly selected alphabetically from a list of dairies, and contact was made through telephone and herd veterinarian to explain the project. Sixty farms were enrolled and 1 farm went out of business during the study, leaving us with 59 farms for study; 6 declined participation. Management-related information was collected via a standardized questionnaire and by on-site inspections (Table 1).

Sampling Plan
Each farm was visited 7 times at intervals of 2 to 4 mo over a period of 15 to 21 mo to collect samples. All samplings occurred between August 2005 and December 2007. A total of 7,009 pooled fecal samples were collected from the participating herds. Each fecal pool consisted of approximately 5 g of feces randomly collected from 10 individual, undisturbed fresh fecal pats from the ground in the pen using sterile tongue depressors. An average of 16 fecal pools was collected per farm visit from different groups of cattle. These fecal samples were collected from lactating cows (3–9 pools), 2 to 3 dry cows (2–3 pools), close-up dry cows (2–3 pools), heifers (1–2 pools), cows in the maternity/hospital area (1–2 pools), and calves (1 pool). The number of fecal pools was adjusted according to the number of strings per group of animals. The more strings per group of target animals (e.g., lactating cows), the greater the number of fecal pools were collected. This sampling method was estimated to provide at least 95% probability of detecting a positive herd if the within-herd prevalence was 8% or more (Jordan, 2005). The sensitivity was likely to be higher than the computed number because more samples were collected from target populations (calves, lactating cows, maternity/hospital cows) reported to be at increased risk of infection (Hancock, 1996; Warnick et al., 2003a). A slurry sample of 50 mL from slurry pond was collected from each dairy farm.

Salmonella Culture and Identification
For isolation of Salmonella spp. from the feces, 12.5 g of each fecal sample was enriched in 112.5 mL of tetrathionate broth (Hardy Diagnostics, Santa Maria, CA) and 112.5 mL of Rappaport-Vassiliadis broth (Hardy Diagnostics). The cultures were incubated for 48 h at 42°C. Each enriched sample was plated onto xylose lysine tergitol-4 (XLT-4, Hardy Diagnostics) agar and MacConkey (Mac, Hardy Diagnostics) agar supplemented with ampicillin (256 µg/mL), chloramphenicol (8 µg/mL), and streptomycin (32 µg/mL; Sigma-Aldrich, Dallas, TX). The plates were incubated for 24 h at 37°C. In this method, 2 XLT-4 and 2 Mac plates per sample were used. All the Mac plates contained antibiotics as described above, whereas XLT-4 plates did not contain any antibiotics. For isolation of Salmonella spp. from the slurry, 25 mL of slurry sample was pre-enriched in 225 mL of buffered peptone water (BPW; Hardy Diagnostics) and incubated for 24 h at 37°C. Pre-enrichment steps were followed by enrichment steps by transferring 1 mL of BPW to 9 mL of tetrathionate broth and 100 µL of BPW to 10 mL of Rappaport-Vassiliadis broth and incubating for 48 h at 42°C. The enriched sample was plated onto XLT-4 and Mac agar plates and incubated for 24 h at 37°C. For confirmation of suspected Salmonella, 3 colonies from XLT-4 and Mac plates were inoculated onto lysine iron agar slants and incubated for 24 h at 37°C. Salmonella suspects from lysine iron agar were transferred to triple sugar iron agar slants and subsequently to urea agar slants and were incubated for 18 to 24 h at 37°C. One isolate per sample was further screened with agglutination tests for serogroup identification using commercial polyvalent A-I and Vi antisera (Difco Laboratory, Detroit, MI). Isolates were then banked in brain-heart infusion broth containing 25 to 30% buffered glycerol and stored at –80°C. One isolate per sample (except when different serogroups were detected for the same sample on 2 different culture media) was selected for further characterization by antimicrobial susceptibility testing. Isolates showing antimicrobial resistance to 2 or more antimicrobials belonging to distinct classes of antimicrobial agents were designated as MDR isolates. One MDR isolate (except for isolate with multiple serogroups) per sample per visit was serotyped at the National Veterinary Service Laboratory (Ames, IA).

Antimicrobial Susceptibility Testing
Antimicrobial susceptibility testing was performed using the Kirby-Bauer disk diffusion method (Bauer et al., 1966). Each isolate was classified as resistant or susceptible to each antimicrobial drug tested by the threshold zone size for resistance, as recommended by Clinical and Laboratory Standards Institute (formerly NCCLS) guidelines (NCCLS, 2003a,b), using the following antimicrobial drugs (BD Diagnostics, Sparks, MD): ampicillin (10 µg), ceftazidime (30 µg), chloramphenicol (30 µg), gentamicin (10 µg), amoxicillin-clavulanic acid (20/10 µg), kanamycin (30 µg), streptomycin (10 µg), tetracycline (30 µg), triple-sulfa (a combination of sulfadiazine, sulfamethazine, and sulfamerazine; 250 µg), and trimethoprim-sulfamethoxazole (1.25/23.75 µg). These antimicrobial agents are the most relevant to both human and veterinary medicine. All Salmonella isolates were screened for antimicrobial susceptibility phenotypes using 10 different antimicrobial agents. Isolates classified as being MDR were further examined by serotyping and pulsed-field gel electrophoresis (PFGE).

PFGE
All 411 MDR Salmonella isolates from fecal samples were analyzed by PFGE following XbaI restriction digestion based on the PulseNet protocol for Salmonella using Salmonella Braenderup H9812 as a size standard (Hunter et al., 2005). The PFGE images were analyzed using BioNumerics v. 3.5 software (Applied Maths, Sint-Martens-Latem, Belgium). Independent strains were defined by PFGE profiles that differed in at least 2 bands with a position tolerance of 1.5%.

New MDR Salmonella Strain Introduction
Isolates from the first farm sampling or from prestudy diagnostic samples submitted to WADDL during the previous 3 yr were considered pre-existing strains. For the purpose of this article, a strain found on the farm was considered a newly introduced strain (based on 2 or more PFGE band differences) if the strain was isolated at the second or later sampling visit and had not been observed on that farm in the first sampling visit or in diagnostic samples from suspected clinical cases for at least 3 or more years before the commencement of the study.

Data Analysis
Univariate analysis was performed to evaluate the unadjusted association between individual variables and the introduction of any new MDR Salmonella strains. Variables with P-values < 0.25 were entered into multivariable models in a stepwise manner. This was a preselection of variables to enter into the multivariable model. Logistic regression analysis was used to evaluate the association between potential herd-level factors and the probability of whether any new MDR strain had been introduced during the study period. Negative binomial regression was used to test the same factors for association with the number of new MDR Salmonella strains introduced during the study period. The main effects as well as interaction terms were retained in the final multivariate model if they were significant at a P-value < 0.05. The number of months during which a herd was sampled was forced in the model to examine its potential confounding effect. All analyses were performed with SAS v.9.1 software (SAS Institute Inc., Cary, NC) and Excel (Microsoft, Redmond, WA).

	RESULTS

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A total of 1,113 Salmonella spp. were isolated from 59 farms. One farm that had an incomplete data set (the farm went out of business) was excluded in this analysis. Of the 1,113 isolates, 385 were multidrug-resistant. Multidrug-resistant Salmonella spp. were isolated from 66% (39/59) of dairy herds (Table 2). Forty-six percent (27/59) of herds did not acquire any new MDR Salmonella strains, whereas the number of new MDR Salmonella strains acquired by the remaining 54% (32/59) of herds ranged from 1 to 8 (Table 3). Seventeen herds were positive for a single newly acquired strain, whereas 2 of the 33 herds each acquired 8 MDR Salmonella strains.

	DISCUSSION

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We found that 27 (46%) of the herds did not acquire any new MDR Salmonella strains, whereas 32 (54%) of herds acquired one or more new MDR Salmonella strains during the study period. The presence of heifers raised off-farm on ranches where heifers commingle with cattle from several sources was found to be a significant risk factor for introduction of new MDR Salmonella strains into commercial dairy herds. This finding indicates that off-farm heifer raising operations where calves commingled with cattle from other sources was significantly associated with an increased risk of negative dairy herds becoming positive for Salmonella. The results of this study corroborate a finding of a previous study (Hegde et al., 2005), in which the authors reported that the heifer-raising operation could serve as a clearinghouse for Salmonella spp. A recent study, however, reported that the risk of Salmonella transmission from the heifer feedlot back to the dairy was low (Edrington et al., 2008). The latter study, however, used only a limited number of dairy herds and no statistical analysis was performed.

Previous studies reported that purchase of cattle from other sources presents important risks of Salmonella transmission between herds (Wray et al., 1990; Evans and Davies, 1996; Zansky et al., 2002).The present study failed to find a significant effect of cattle purchases (cow, bulls, calves, and heifers) on introduction of new MDR Salmonella strains into commercial dairy herds. A recent study found that introduction of new cattle was not associated with Salmonella status dairy herds (Huston et al., 2002). It is not known why the present study did not find cattle purchase as a risk factor for interherd transmission of Salmonella; however, it is possible that the high rate of off-farm heifer raising (nearly 50% of the farms in the present study raised heifers off-farm, where they commingled with cattle from other sources, or replaced stock through contract heifer raising) mitigated the effects of cattle purchases in the present study. As a farm introduced more heifers as replacement stock through contract heifer-raising, they purchased fewer heifers directly from other farms.

Farms with a history of clinical salmonellosis were at increased risk of acquiring new Salmonella enterica strains. Although a previous study identified a significant association between recent clinical salmonellosis and detection of Salmonella in fecal samples from the same herd for up to 8 mo (Warnick et al., 2001), we did not find the same serovar in herds that had a history of clinical salmonellosis. It is unclear why background strains of Salmonella spp. did not persist in the present study herds, but this may be due to intermittent shedding patterns of Salmonella in cattle, environmental conditions, and other unknown factors. The discrepancy between our result and that of the Warnick et al. (2001) study could be related to the observations that clinical salmonellosis occurred in some of the participating herds in the present study more than a year before the start of the study, and herds with clinical salmonellosis were likely managed differently than noninfected herds. Given that the association was still significant after adjustment for other variables, this finding suggests the existence of important risk factors for the introduction of new strains that were not found in the present study. Previous studies suggest that recent antimicrobial treatment can increase the probability of isolating Salmonella in calves, heifers, and cows (Warnick et al., 2003b; Berge et al., 2006). It is possible that antimicrobial use at the farm level increases the susceptibility of dairy herds to acquire new strains.

Culture-dependent isolation of Salmonella spp. is naturally less than 100% sensitive. However, methods such as pooling of samples, targeted sampling, and sample pre-enrichment were used to improve the recovery of damaged cells and subsequent isolation rates. Initial assessment of Salmonella strains present in the dairy farms was based on more intensive sampling around dairy farms. Certain sample types were targeted (e.g., pooled sampling, milk filters, slurry) that increase the chances of determining herd-wide status. Cattle sampling was divided between different groups of cattle on the farm (e.g., heifers, lactating, dry), as Salmonella and MDR Salmonella prevalences have been demonstrated to vary significantly between these groups (Warnick et al., 2003a; Cobbold et al., 2006). It is possible that a pre-existing strain was missed, but the chance of this occurring was minimized through the sampling and microbiological methods employed.

The results of our study indicate that increased herd size was significantly and positively associated with increased risk of introduction of new MDR Salmonella strains and with increased numbers of new MDR Salmonella introductions. This finding corroborates that of another study, which found that increases in herd size and the number of cattle purchased from test-positive herds in the previous year-quarter were significantly and positively associated with an increased risk of negative herds becoming positive for Salmonella (Nielsen et al., 2007). Several previous studies also found an association between herd size and Salmonella prevalence, which might be affected by the Salmonella introduction rate (Kabagambe et al., 2000; Huston et al., 2002; Warnick et al., 2003b).

In conclusion, the findings of the present study strongly implicate off-farm rearing of heifers in the transmission of MDR Salmonella strains between farms. Other factors, including increased herd size and a history of clinical salmonellosis, were also associated with the introduction of MDR Salmonella into dairy herds. For future studies, other important risk factors associated with interherd transmission of Salmonella should be investigated. Studies are needed to clarify whether and how off-farm rearing of heifers can be done without increasing the risk of Salmonella introduction.

	ACKNOWLEDGMENTS

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This project was supported in part by the National Institute of Health, Department of Health and Human Services under the contract number NO1-AI-30055 and by the Agricultural Animal Health Program, College of Veterinary Medicine, Washington State University. The skillful technical assistance of Katherine Kaya Baker [Field Disease Investigation Unit (FDIU), College of Veterinary Medicine, Washington State University] is gratefully acknowledged. We also thank Lindsay Tippett, Lisa Jones, and other staff of the FDIU for their technical assistance.

Received for publication June 27, 2008. Accepted for publication February 3, 2009.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 


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