Prevalence, enumeration, and antimicrobial agent resistance of Clostridium difficile in cattle at harvest in the United States

Journal of Food Protection

Volumn 74, Issue 10, 2011, Pages 1618-1624

  Rodriguez Palacios, Alexander ^a,b   Koohmaraie, Mohammad ^c   Lejeune, Jeffrey T ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c Institute for Environmental Health Laboratories and Consulting   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT;

ANIMAL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COUNT; BACTERIAL SHEDDING; BACTERIUM IDENTIFICATION; CATTLE; CLASSIFICATION; CLOSTRIDIUM DIFFICILE; DRUG EFFECT; FECES; FOOD CONTAMINATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; MEAT; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PREVALENCE; PRODUCT SAFETY; RIBOTYPING; UNITED STATES;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL SHEDDING; BACTERIAL TYPING TECHNIQUES; CATTLE; CLOSTRIDIUM DIFFICILE; COLONY COUNT, MICROBIAL; CONSUMER PRODUCT SAFETY; DRUG RESISTANCE, BACTERIAL; FECES; FOOD CONTAMINATION; HUMANS; MEAT; MICROBIAL SENSITIVITY TESTS; PREVALENCE; RIBOTYPING; UNITED STATES;

ANIMALIA; BOS; CLOSTRIDIUM DIFFICILE;

EID: 80053909012     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-11-141     Document Type: Article

References (53)

1. Ackermann, G., D. Adler, and A. C. Rodloff. 2003. In vitro activity of linezolid against Clostridium difficile. J. Antimicrob. Chemother. 51:743-745. (Pubitemid 36336177)
2. Arroyo, L. G., J. Rousseau, B. M. Willey, D. E. Low, H. Staempfli, A. McGeer, and J. S. Weese. 2005. Use of a selective enrichment broth to recover Clostridium difficile from stool swabs stored under different conditions. J. Clin. Microbiol. 43:5341-5343. (Pubitemid 41484055)
3. Bidet, P., F. Barbut, V. Lalande, B. Burghoffer, and J. C. Petit. 1999. Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol. Lett. 175:261-266. (Pubitemid 29352246)
4. Biller, P., B. Shank, L. Lind, M. Brennan, L. Tkatch, G. Killgore, A. Thompson, and L. C. McDonald. 2007. Moxifloxacin therapy as a risk factor for Clostridium difficile-associated disease during an outbreak: attempts to control a new epidemic strain. Infect. Control Hosp. Epidemiol. 28:198-201. (Pubitemid 46374161)
5. Chase-Topping, M., D. Gally, C. Low, L. Matthews, and M. Woolhouse. 2008. Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat. Rev. Microbiol. 6:904-912.
6. Clopper, C. J., and E. S. Pearson. 1934. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26:404-413.
7. Cohen, S. H., D. N. Gerding, S. Johnson, C. P. Kelly, V. G. Loo, L. C. McDonald, J. Pepin, and M. H. Wilcox. 2010. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect. Control Hosp. Epidemiol. 31:431-455.
8. Costa, M. C., L. Arroyo, D. L. Pearl, J. S. Weese, and H. Staempfli. 2009. Incidence of Clostridium difficile in feces of male Holstein veal calves. American College of Veterinary Internal Medicine Forum. Available at: http://www.acvim.org/websites/acvim/File/Costa.pdf. Accessed 15 March 2011.
9. Elder, R. O., J. E. Keen, G. R. Siragusa, G. A. Barkocy-Gallagher, M. Koohmaraie, and W. W. Laegreid. 2000. Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc. Natl. Acad. Sci. USA 97:2999-3003. (Pubitemid 30183244)
10. Fedorko, D. P., and E. C. Williams. 1997. Use of cycloserinecefoxitin- fructose agar and L-proline-aminopeptidase (PRO Discs) in the rapid identification of Clostridium difficile. J. Clin. Microbiol. 35:1258-1259. (Pubitemid 27175263)
11. Fluckey, W. M., G. H. Loneragan, R. D. Warner, A. Echeverry, and M. M. Brashears. 2009. Diversity and susceptibility of Enterococcus isolated from cattle before and after harvest. J. Food Prot. 72:766-774.
12. Food Animal Residue Avoidance and Depletion Program. 2011. Prohibited drug list. Available at: http://www.farad.org/eldu/prohibit.html. Accessed 15 March 2011.
13. French, E., A. Rodriguez-Palacios, and J. T. LeJeune. 2010. Enteric bacterial pathogens with zoonotic potential isolated from farm-raised deer. Foodborne Pathog. Dis. 7:1031-1037.
14. Garcia, A., J. Perez, A. Pulido, J. Niubo, P. Perez, and R. Martin. 2000. [Evaluation of four rapid methods for the investigation of the toxigenic capacity of Clostridium difficile strains isolated in a selective medium]. Enferm. Infecc. Microbiol. Clin. 18:109-112.
15. Hammitt, M. C., D. M. Bueschel, M. K. Keel, R. D. Glock, P. Cuneo, D. W. DeYoung, C. Reggiardo, H. T. Trinh, and J. G. Songer. 2008. A possible role for Clostridium difficile in the etiology of calf enteritis. Vet. Microbiol. 127:343-352. (Pubitemid 351173516)
16. Hecht, D. W., and D. Citron. 2007. M11-A7: Methods for antimicrobial susceptibility testing of anaerobic bacteria; approved guideline, 7th ed. Clinical Laboratory Standards Institute, Wayne, PA.
17. Jones, R. N., T. R. Fritsche, H. S. Sader, and J. E. Ross. 2007. LEADER surveillance program results for 2006: an activity and spectrum analysis of linezolid with clinical isolates from the United States (50 medical centers). Diagn. Microbiol. Infect. Dis. 59:309-317. (Pubitemid 350016703)
18. Jones, R. N., S. Kohno, Y. Ono, J. E. Ross, and K. Yanagihara. 2009. ZAAPS International Surveillance Program (2007) for linezolid resistance: results from 5, 591 gram-positive clinical isolates in 23 countries. Diagn. Microbiol. Infect. Dis. 64:191-201.
19. Keel, K., J. S. Brazier, K. W. Post, S. Weese, and J. G. Songer. 2007. Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species. J. Clin. Microbiol. 45:1963-1964. (Pubitemid 46933933)
20. Lawley, T. D., S. Clare, A. W. Walker, D. Goulding, R. A. Stabler, N. Croucher, P. Mastroeni, P. Scott, C. Raisen, L. Mottram, N. F. Fairweather, B. W. Wren, J. Parkhill, and G. Dougan. 2009. Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect. Immun. 77:3661-3669.
21. Lemee, L., A. Dhalluin, S. Testelin, M. A. Mattrat, K. Maillard, J. F. Lemeland, and J. L. Pons. 2004. Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (toxin A), and tcdB (toxin B) genes for toxigenic culture of Clostridium difficile. J. Clin. Microbiol. 42:5710-5714. (Pubitemid 39664357)
22. Nagy, E., and M. J. Dowzicky. 2010. In vitro activity of tigecycline and comparators against a European compilation of anaerobes collected as part of the Tigecycline Evaluation and Surveillance Trial (TEST). Scand. J. Infect. Dis. 42:33-38.
23. National Cattlemen's Beef Association. 2002. Increased export of U. S. trimmings could benefit McDonald's, help improve value for U. S. producers [press release]. Available at: http://www.beefusa.org/ NEWSIncreasedExportofUSTrimmingsCouldBenefitMcDonaldsHelp ImproveValueforUSProducers4927.aspx.
24. Norman, K. N., R. B. Harvey, H. M. Scott, M. E. Hume, K. Andrews, and A. D. Brawley. 2009. Varied prevalence of Clostridium difficile in an integrated swine operation. Anaerobe 15:256-260.
25. Pearce, M. C., D. Fenlon, J. C. Low, A. W. Smith, H. I. Knight, J. Evans, G. Foster, B. A. Synge, and G. J. Gunn. 2004. Distribution of Escherichia coli O157 in bovine fecal pats and its impact on estimates of the prevalence of fecal shedding. Appl. Environ. Microbiol. 70:5737-5743. (Pubitemid 39471811)
26. Persson, S., M. Torpdahl, and K. E. Olsen. 2008. New multiplex PCR method for the detection of Clostridium difficile toxin A (tcdA) and toxin B (tcdB) and the binary toxin (cdtA/cdtB) genes applied to a Danish strain collection. Clin. Microbiol. Infect. 14:1057-1064. (Pubitemid 352748847)
27. Petrie, A., and P. Watson. 1999. Statistics for veterinary and animal sciences. Blackwell Science, Oxford.
28. Pirs, T., M. Ocepek, and M. Rupnik. 2008. Isolation of Clostridium difficile from food animals in Slovenia. J. Med. Microbiol. 57:790-792. (Pubitemid 351842074)
29. Rello, J. 2005. Pharmacokinetics, pharmacodynamics, safety and tolerability of tigecycline. J. Chemother. 17(Suppl.):12-22. (Pubitemid 41686777)
30. Rodriguez-Palacios, A., and J. T. LeJeune. 2011. Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Appl. Environ. Microbiol. 77:3085-3091.
31. Rodriguez-Palacios, A., C. Pickworth, S. Loerch, and J. T. Lejeune. 2011. Transient fecal shedding and limited animal-to-animal transmission of Clostridium difficile by naturally infected finishing feedlot cattle. Appl. Environ. Microbiol. 77:3391-3397.
32. Rodriguez-Palacios, A., R. J. Reid-Smith, H. R. Staempfli, D. Daignault, N. Janecko, B. P. Avery, H. Martin, A. D. Thompson, L. C. McDonald, B. Limbago, and J. S. Weese. 2009. Possible seasonality of Clostridium difficile in retail meat, Canada. Emerg. Infect. Dis. 15:802-805.
33. Rodriguez-Palacios, A., R. J. Reid-Smith, H. R. Staempfli, and J. S. Weese. 2010. Clostridium difficile survives minimal temperature recommended for cooking ground meats. Anaerobe 16:540-542.
34. Rodriguez-Palacios, A., H. R. Staempfli, T. Duffield, A. S. Peregrine, L. A. Trotz-Williams, L. G. Arroyo, J. S. Brazier, and J. S. Weese. 2006. Clostridium difficile PCR ribotypes in calves, Canada. Emerg. Infect. Dis. 12:1730-1736. (Pubitemid 44674250)
35. Rodriguez-Palacios, A., H. R. Staempfli, T. Duffield, and J. S. Weese. 2007. Clostridium difficile in retail ground meat, Canada. Emerg. Infect. Dis. 13:485-487. (Pubitemid 46348139)
36. Rodriguez-Palacios, A., H. R. Stampfli, M. Stalker, T. Duffield, and J. S. Weese. 2007. Natural and experimental infection of neonatal calves with Clostridium difficile. Vet. Microbiol. 124:166-172. (Pubitemid 47211679)
37. Rupnik, M., B. Dupuy, N. F. Fairweather, D. N. Gerding, S. Johnson, I. Just, D. M. Lyerly, M. R. Popoff, J. I. Rood, A. L. Sonenshein, M. Thelestam, B. W. Wren, T. D. Wilkins, and C. von Eichel-Streiber. 2005. Revised nomenclature of Clostridium difficile toxins and associated genes. J. Med. Microbiol. 54:113-117. (Pubitemid 40867994)
38. Rupnik, M., A. Widmer, O. Zimmermann, C. Eckert, and F. Barbut. 2008. Clostridium difficile toxinotype V, ribotype 078, in animals and humans. J. Clin. Microbiol. 46:2146. (Pubitemid 351831867)
39. Shim, J. K., S. Johnson, M. H. Samore, D. Z. Bliss, and D. N. Gerding. 1998. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet 351:633-636. (Pubitemid 28098446)
40. Songer, J. G., R. Jones, M. A. Anderson, A. J. Barbara, K. W. Post, and H. T. Trinh. 2007. Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms. Vet. Microbiol. 124:358-361. (Pubitemid 47268670)
41. Songer, J. G., H. T. Trinh, G. E. Killgore, A. D. Thompson, L. C. McDonald, and B. M. Limbago. 2009. Clostridium difficile in retail meat products, USA, 2007. Emerg. Infect. Dis. 15:819-821.
42. Spigaglia, P., and P. Mastrantonio. 2002. Molecular analysis of the pathogenicity locus and polymorphism in the putative negative regulator of toxin production (TcdC) among Clostridium difficile clinical isolates. J. Clin. Microbiol. 40:3470-3475. (Pubitemid 34977470)
43. Sullivan, N. M., S. Pellett, and T. D. Wilkins. 1982. Purification and characterization of toxins A and B of Clostridium difficile. Infect. Immun. 35:1032-1040.
44. Thitaram, S. N., J. F. Frank, S. A. Lyon, G. R. Siragusa, J. S. Bailey, J. E. Lombard, C. A. Haley, B. A. Wagner, D. A. Dargatz, and P. J. Fedorka-Cray. 2011. Clostridium difficile from healthy food animals: optimized isolation and prevalence. J. Food Prot 74:130-133.
45. Thonnard, J., F. Carreer, V. Avesani, and M. Delmee. 1996. Toxin A detection on Clostridium difficile colonies from 24-h cultures. Clin. Microbiol. Infect. 2:50-54. (Pubitemid 126682078)
46. U. S. Department of Agriculture. 2010. Estimated red meat production. CattleFax and U. S. Department of Agriculture reports: Livestock slaughter and meat production. Available at: http://www.cattlefax.com/quicklinks-data/usda- reports/. Accessed 14 May 2010.
47. U. S. Food and Drug Administration. 2002. Reminder: extra-label use of fluoroquinolones prohibited. Available at: http://www.fda.gov/AnimalVeterinary/ NewsEvents/CVMUpdates/ucm129354.htm. Accessed 31 August 2010.
48. U. S. Food and Drug Administration. 2007. Clindamycin hydrochloride oral drops (for use in dogs and cats). ANADA 200-398 original approval. Available at: http://www.fda.gov/downloads/AnimalVeterinary/Products/ ApprovedAnimalDrugProducts/FOIADrugSummaries/ucm061348.pdf. Accessed 20 May 2011.
49. U. S. Food and Drug Administration. 18 November 2009. FDA takes action against dairy farm and owner-farm selling animals with illegal drug residues in violation of federal law. Available at: http://www.fda.gov/NewsEvents/Newsroom/ PressAnnouncements/2009/ucm 191232.htm. Accessed 20 May 2011.
50. U. S. Food and Drug Administration. 19 November 2009. FDA takes action against Maryland veal calf dealer: man allegedly sold animals for human consumption that contained illegal drug residues. Available at: http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/2009/ucm191446.htm. Accessed 20 May 2011.
51. Wilcox, M. H., W. Fawley, J. Freeman, and J. Brayson. 2000. In vitro activity of new generation fluoroquinolones against genotypically distinct and indistinguishable Clostridium difficile isolates. J. Antimicrob. Chemother. 46:551-556.
52. Wise, R., J. M. Andrews, F. J. Boswell, and J. P. Ashby. 1998. The in vitro activity of linezolid (U-100766) and tentative breakpoints. J. Antimicrob. Chemother. 42:721-728. (Pubitemid 29008072)
53. Zhang, J., S. K. Wall, L. Xu, and P. D. Ebner. 2010. Contamination rates and antimicrobial resistance in bacteria isolated from grass-fed labeled beef products. Foodborne Pathog. Dis. 7:1331-1336.