Multilaboratory Survey To Evaluate Salmonella Prevalence in Diarrheic and Nondiarrheic Dogs and Cats in the United States between 2012 and 2014

Renate Reimschuessel¹, Michael Grabenstein², Jake Guag², Sarah M Nemser², Kyunghee Song³, Junshan Qiu⁴, Kristin A Clothier⁵, Barbara A Byrne⁶, Stanley L Marks⁶, Kyran Cadmus⁷, Kristy Pabilonia⁷, Susan Sanchez⁸, Sreekumari Rajeev⁹, Steve Ensley¹⁰, Timothy S Frana¹⁰, Albert E Jergens¹⁰, Kimberly H Chappell¹¹, Siddhartha Thakur¹¹, Beverly Byrum¹², Jing Cui¹², Yan Zhang¹², Matthew M Erdman¹³, Shelley C Rankin¹⁴, Russell Daly¹⁵, Seema Das¹⁵, Laura Ruesch¹⁵, Sara D Lawhon¹⁶, Shuping Zhang¹⁶, Timothy Baszler¹⁷, Dubraska Diaz-Campos¹⁷, Faye Hartmann¹⁸, Ogi Okwumabua¹⁸

Affiliations

¹ U.S. Food and Drug Administration, Center for Veterinary Medicine, Office of Research, Laurel, Maryland, USA renate.reimschuessel@fda.hhs.gov.
² U.S. Food and Drug Administration, Center for Veterinary Medicine, Office of Research, Laurel, Maryland, USA.
³ U.S. Food and Drug Administration, Center for Veterinary Medicine, Office of New Animal Drug Evaluation, Rockville, Maryland, USA.
⁴ U.S. Food and Drug Administration, Center for Drug Evaluation and Research, Silver Spring, Maryland, USA.
⁵ California Animal Health and Food Safety Laboratory, University of California, Davis, Davis, California, USA.
⁶ School of Veterinary Medicine, University of California, Davis, Davis, California, USA.
⁷ College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
⁸ College of Veterinary Medicine, Department of Infectious Disease, Athens Veterinary Diagnostic Laboratory, The University of Georgia, Athens, Georgia, USA.
⁹ Veterinary Diagnostic and Investigational Laboratory, College of Veterinary Medicine, The University of Georgia, Tifton, Georgia, USA.
¹⁰ College of Veterinary Medicine, Veterinary Diagnostic Laboratory, Iowa State University, Ames, Iowa, USA.
¹¹ College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, USA.
¹² Ohio Animal Disease Diagnostic Laboratory, Ohio Department of Agriculture, Reynoldsburg, Ohio, USA.
¹³ U.S. Department of Agriculture, National Veterinary Services Laboratories, Ames, Iowa, USA.
¹⁴ University of Pennsylvania, Matthew J. Ryan Veterinary Hospital, Philadelphia, Pennsylvania, USA.
¹⁵ Veterinary and Biomedical Sciences Department, Animal Disease Research and Diagnostic Laboratory, South Dakota State University, Brookings, South Dakota, USA.
¹⁶ College of Veterinary Medicine, Texas A&M University, College Station, Texas, USA.
¹⁷ Washington Animal Disease Diagnostic Laboratory, College of Veterinary Medicine, Washington State University, Pullman, Washington, USA.
¹⁸ Department of Pathobiological Sciences/WVDL, University of Wisconsin-Madison, Madison, Wisconsin, USA.

PMID: 28202802
PMCID: PMC5405253
DOI: 10.1128/JCM.02137-16

Multilaboratory Survey To Evaluate Salmonella Prevalence in Diarrheic and Nondiarrheic Dogs and Cats in the United States between 2012 and 2014

Renate Reimschuessel et al. J Clin Microbiol. 2017 May.

. 2017 May;55(5):1350-1368.

doi: 10.1128/JCM.02137-16. Epub 2017 Feb 15.

Authors

Affiliations

¹ U.S. Food and Drug Administration, Center for Veterinary Medicine, Office of Research, Laurel, Maryland, USA renate.reimschuessel@fda.hhs.gov.
² U.S. Food and Drug Administration, Center for Veterinary Medicine, Office of Research, Laurel, Maryland, USA.
³ U.S. Food and Drug Administration, Center for Veterinary Medicine, Office of New Animal Drug Evaluation, Rockville, Maryland, USA.
⁴ U.S. Food and Drug Administration, Center for Drug Evaluation and Research, Silver Spring, Maryland, USA.
⁵ California Animal Health and Food Safety Laboratory, University of California, Davis, Davis, California, USA.
⁶ School of Veterinary Medicine, University of California, Davis, Davis, California, USA.
⁷ College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
⁸ College of Veterinary Medicine, Department of Infectious Disease, Athens Veterinary Diagnostic Laboratory, The University of Georgia, Athens, Georgia, USA.
⁹ Veterinary Diagnostic and Investigational Laboratory, College of Veterinary Medicine, The University of Georgia, Tifton, Georgia, USA.
¹⁰ College of Veterinary Medicine, Veterinary Diagnostic Laboratory, Iowa State University, Ames, Iowa, USA.
¹¹ College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, USA.
¹² Ohio Animal Disease Diagnostic Laboratory, Ohio Department of Agriculture, Reynoldsburg, Ohio, USA.
¹³ U.S. Department of Agriculture, National Veterinary Services Laboratories, Ames, Iowa, USA.
¹⁴ University of Pennsylvania, Matthew J. Ryan Veterinary Hospital, Philadelphia, Pennsylvania, USA.
¹⁵ Veterinary and Biomedical Sciences Department, Animal Disease Research and Diagnostic Laboratory, South Dakota State University, Brookings, South Dakota, USA.
¹⁶ College of Veterinary Medicine, Texas A&M University, College Station, Texas, USA.
¹⁷ Washington Animal Disease Diagnostic Laboratory, College of Veterinary Medicine, Washington State University, Pullman, Washington, USA.
¹⁸ Department of Pathobiological Sciences/WVDL, University of Wisconsin-Madison, Madison, Wisconsin, USA.

PMID: 28202802
PMCID: PMC5405253
DOI: 10.1128/JCM.02137-16

Abstract

Eleven laboratories collaborated to determine the periodic prevalence of Salmonella in a population of dogs and cats in the United States visiting veterinary clinics. Fecal samples (2,965) solicited from 11 geographically dispersed veterinary testing laboratories were collected in 36 states between January 2012 and April 2014 and tested using a harmonized method. The overall study prevalence of Salmonella in cats (3 of 542) was <1%. The prevalence in dogs (60 of 2,422) was 2.5%. Diarrhea was present in only 55% of positive dogs; however, 3.8% of the all diarrheic dogs were positive, compared with 1.8% of the nondiarrheic dogs. Salmonella-positive dogs were significantly more likely to have consumed raw food (P = 0.01), to have consumed probiotics (P = 0.002), or to have been given antibiotics (P = 0.01). Rural dogs were also more likely to be Salmonella positive than urban (P = 0.002) or suburban (P = 0.001) dogs. In the 67 isolates, 27 unique serovars were identified, with three dogs having two serovars present. Antimicrobial susceptibility testing of 66 isolates revealed that only four of the isolates were resistant to one or more antibiotics. Additional characterization of the 66 isolates was done using pulsed-field gel electrophoresis and whole-genome sequencing (WGS). Sequence data compared well to resistance phenotypic data and were submitted to the National Center for Biotechnology Information (NCBI). This study suggests an overall decline in prevalence of Salmonella-positive dogs and cats over the last decades and identifies consumption of raw food as a major risk factor for Salmonella infection. Of note is that almost half of the Salmonella-positive animals were clinically nondiarrheic.

Keywords: Salmonella; WGS; diarrhea; fecal organisms; pets.

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Figures

**FIG 1**
Percentage of Salmonella-positive isolates versus average monthly outside temperature of the state at the time each fecal sample was collected.

**FIG 2**
Dendrogram of Salmonella PFGE pulsotypes from dog and cat fecal samples collected by 11 laboratories in the United States from January 2012 through April 2014. Serovars determined by the National Veterinary Services Laboratories (NVSL) are compared with those predicted by PFGE.

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Multilaboratory Survey To Evaluate Salmonella Prevalence in Diarrheic and Nondiarrheic Dogs and Cats in the United States between 2012 and 2014

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Multilaboratory Survey To Evaluate Salmonella Prevalence in Diarrheic and Nondiarrheic Dogs and Cats in the United States between 2012 and 2014

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