Occurrence of zoonotic Clostridia and Yersinia in healthy cattle

Journal of Food Protection

Volumn 76, Issue 10, 2013, Pages 1697-1703

  Schmid, A ^a,b   Messelhausser U ^a   Hormansdorfer S ^a   Sauter Louis, C ^b   Mansfeld, R ^b  

^a Bavarian Health and Food Safety Authority   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL TOXIN;

ANIMAL; ARTICLE; CATTLE; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM DIFFICILE; DUST; FECES; GENETICS; GERMANY; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; RISK FACTOR; YERSINIA ENTEROCOLITICA; ZOONOSIS;

ANIMALS; BACTERIAL TOXINS; CATTLE; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM DIFFICILE; DNA, BACTERIAL; DUST; ENVIRONMENTAL MICROBIOLOGY; FECES; GERMANY; HUMANS; RISK FACTORS; YERSINIA ENTEROCOLITICA; ZOONOSES;

EID: 84885435710     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-13-151     Document Type: Article

References (59)

1. Aureli, P., M. Di Cunto, A. Maffei, G. De Chiara, G. Franciosa, L. Accorinti, A. M. Gambardella, and D. Greco. 2000. An outbreak in Italy of botulism associated with a dessert made with mascarpone cream cheese. Eur. J. Epidemiol. 16: 913-918.
2. Avbersek, J., S. Janezic, M. Pate, M. Rupnik, V. Zidaric, K. Logar, M. Vengust, M. Zemljic, T. Pirs, and M. Ocepek. 2009. Diversity of Clostridium difficile in pigs and other animals in Slovenia. Anaerobe 15: 252-255.
3. Bailey, G. D., B. A. Vanselow, M. A. Hornitzky, S. I. Hum, G. J. Eamens, P. A. Gill, K. H. Walker, and J. P. Cronin. 2003. A study of the foodborne pathogens: Campylobacter, Listeria and Yersinia, in faeces from slaughter-age cattle and sheep in Australia. Commun. Dis. Intell. Q. Rep. 27: 249-257.
4. Bauer, M. P., D. W. Notermans, B. H. van Benthem, J. S. Brazier, M. H. Wilcox, M. Rupnik, D. L. Monnet, J. T. van Dissel, and E. J. Kuijper. 2011. Clostridium difficile infection in Europe: a hospitalbased survey. Lancet 377: 63-73.
5. Baverud, V. 2002. Clostridium difficile infections in animals with special reference to the horse. A review. Vet. Q. 24: 203-219.
6. Bojesen, A. M., K. E. Olsen, and M. F. Bertelsen. 2006. Fatal enterocolitis in Asian elephants (Elephas maximus) caused by Clostridium difficile. Vet. Microbiol. 116: 329-335.
7. Bonardi, S., A. Paris, C. Bacci, M. D'Incau, L. Ferroni, and F. Brindani. 2007. Detection and characterization of Yersinia enterocolitica from pigs and cattle. Vet. Res. Commun. 31(Suppl. 1): 347-350.
8. Bouttier, S., M. C. Barc, B. Felix, S. Lambert, A. Collignon, and F. Barbut. 2010. Clostridium difficile in ground meat, France. Emerg. Infect. Dis. 16: 733-735.
9. Bucher, M., C. Meyer, B. Grotzbach, S. Wacheck, A. Stolle, and M. Fredriksson-Ahomaa. 2008. Epidemiological data on pathogenic Yersinia enterocolitica in southern Germany during 2000-2006. Foodborne Pathog. Dis. 5: 273-280.
10. Centers for Disease Control and Prevention. 2011. Notes from the field: Yersinia enterocolitica infections associated with pasteurized milk - southwestern Pennsylvania, March-August, 2011. Morb. Mortal. Wkly. Rep. 60: 1428.
11. Costa, M. C., R. Reid-Smith, S. Gow, S. J. Hannon, C. Booker, J. Rousseau, K. M. Benedict, P. S. Morley, and J. S. Weese. 2012. Prevalence and molecular characterization of Clostridium difficile isolated from feedlot beef cattle upon arrival and mid-feeding period. BMC Vet. Res. 8: 38.
12. Costa, M. C., H. R. Stämpfli, L. G. Arroyo, D. L. Pearl, and J. S. Weese. 2011. Epidemiology of Clostridium difficile on a veal farm: prevalence, molecular characterization and tetracycline resistance. Vet. Microbiol. 152: 379-384.
13. Dahlenborg, M., E. Borch, and P. Radstrom. 2003. Prevalence of Clostridium botulinum types B, E and F in faecal samples from Swedish cattle. Int. J. Food Microbiol. 82: 105-110.
14. de Boer, E., A. Zwartkruis-Nahuis, A. E. Heuvelink, C. Harmanus, and E. J. Kuijper. 2011. Prevalence of Clostridium difficile in retailed meat in the Netherlands. Int. J. Food Microbiol. 144: 561-564.
15. European Committee on Antimicrobial Susceptibility Testing. 2012. Antimicrobial susceptibility testing. EUCAST disk diffusion method, version 2.1. European Society of Clinical Microbiology and Infectious Diseases, Basel. Available at: http://www.eucast.org/antimicrobial-susceptibility-testing. Accessed 7 August 2013.
16. European Food Safety Authority and European Centre for Disease Prevention and Control. 2012. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA J. 10: 442.
17. Fantasia, M., M. Grazia Mingrone, D. Crotti, and C. Boscato. 1985. Isolation of Yersinia enterocolitica biotype 4 serotype O3 from canine sources in Italy. J. Clin. Microbiol. 22: 314-315.
18. Fenwick, S. G., P. Madie, and C. R. Wilks. 1994. Duration of carriage and transmission of Yersinia enterocolitica biotype 4, serotype 0: 3 in dogs. Epidemiol. Infect. 113: 471-477.
19. Fredriksson-Ahomaa, M., S. Hielm, and H. Korkeala. 1999. High prevalence of yadA-positive Yersinia enterocolitica in pig tongues and minced meat at the retail level in Finland. J. Food Prot. 62: 123-127.
20. Fredriksson-Ahomaa, M., and H. Korkeala. 2003. Low occurrence of pathogenic Yersinia enterocolitica in clinical, food, and environmental samples: a methodological problem. Clin. Microbiol. Rev. 16: 220-229.
21. Fredriksson-Ahomaa, M., and H. Korkeala. 2003. Molecular epidemiology of Yersinia enterocolitica 4/O: 3. Adv. Exp. Med. Biol. 529: 295-302.
22. Fredriksson-Ahomaa, M., C. Meyer, R. Bonke, E. Stuber, and S. Wacheck. 2010. Characterization of Yersinia enterocolitica 4/O: 3 isolates from tonsils of Bavarian slaughter pigs. Lett. Appl. Microbiol. 50: 412-418.
23. Fredriksson-Ahomaa, M., A. Stolle, A. Siitonen, and H. Korkeala. 2006. Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O: 3 originate mainly from pigs. J. Med. Microbiol. 55: 747-749.
24. Goorhuis, A., D. Bakker, J. Corver, S. B. Debast, C. Harmanus, D. W. Notermans, A. A. Bergwerff, F. W. Dekker, and E. J. Kuijper. 2008. Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin. Infect. Dis. 47: 1162-1170.
25. Houser, B. A., A. L. Hattel, and B. M. Jayarao. 2010. Real-time multiplex polymerase chain reaction assay for rapid detection of Clostridium difficile toxin-encoding strains. Foodborne Pathog. Dis. 7: 719-726.
26. Huss, H. H. 1980. Distribution of Clostridium botulinum. Appl. Environ. Microbiol. 39: 764-769.
27. Indra, A., H. Lassnig, N. Baliko, P. Much, A. Fiedler, S. Huhulescu, and F. Allerberger. 2009. Clostridium difficile: a new zoonotic agent? Wien. Klin. Wochenschr. 121: 91-95.
28. International Organization for Standardization. 2003. Microbiology of food and animal feeding stuffs - horizontal method for the detection of presumptive pathogenic Yersinia enterocolitica. International Organization for Standardization, Geneva.
29. Jayarao, B. M., S. C. Donaldson, B. A. Straley, A. A. Sawant, N. V. Hegde, and J. L. Brown. 2006. A survey of foodborne pathogens in bulk tank milk and raw milk consumption among farm families in Pennsylvania. J. Dairy Sci. 89: 2451-2458.
30. 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.
31. Keel, M. K., and J. G. Songer. 2006. The comparative pathology of Clostridium difficile-associated disease. Vet. Pathol. 43: 225-240.
32. Keessen, E. C., W. Gaastra, and L. J. Lipman. 2011. Clostridium difficile infection in humans and animals, differences and similarities. Vet. Microbiol. 153: 205-217.
33. Khanna, S., D. S. Pardi, S. L. Aronson, P. P. Kammer, R. Orenstein, J. L. St. Sauver, W. S. Harmsen, and A. R. Zinsmeister. 2012. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am. J. Gastroenterol. 107: 89-95.
34. Klarmann, D. 1989. The detection of Clostridium botulinum in fecal samples of cattle and swine and in the raw material and animal meal of different animal body rendering plants. Berl. Muench. Tieraerztl. Wochenschr. 102: 84-86.
35. Kuijper, E., F. Barbut, J. S. Brazier, N. Kleinkauf, T. Eckmanns, M. L. Lambert, D. Drudy, F. Fitzpatrick, C. Wiuff, D. J. Brown, J. E. Coia, H. Pituch, P. Reichert, J. Even, J. Mossong, A. F. Widmer, K. E. Olsen, F. Allerberger, D. W. Notermans, M. Delmée, B. Coignard, M. Wilcox, B. Patel, R. Frei, E. Nagy, E. Bouza, M. Marin, T. Å kerlund, A. Virolainen-Julkunen, O. Lyytikäinen, S. Kotila, A. Ingebretsen, B. Smyth, P. Rooney, I. R. Poxton, and D. L. Monnet. 2008. Update of Clostridium difficile infection due to PCR ribotype 027 in Europe, 2008. Euro Surveill. 13(31):pii~18942.
36. Lindstrom, M., J. Myllykoski, S. Sivela, and H. Korkeala. 2010. Clostridium botulinum in cattle and dairy products. Crit. Rev. Food Sci. Nutr. 50: 281-304.
37. McDonald, L. C., G. E. Killgore, A. Thompson, R. C. Owens, Jr., S. V. Kazakova, S. P. Sambol, S. Johnson, and D. N. Gerding. 2005. An epidemic, toxin gene-variant strain of Clostridium difficile. N. Engl. J. Med. 353: 2433-2441.
38. McDonald, L. C., M. Owings, and D. B. Jernigan. 2006. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996-2003. Emerg. Infect. Dis. 12: 409-415.
39. McNally, A., T. Cheasty, C. Fearnley, R. W. Dalziel, G. A. Paiba, G. Manning, and D. G. Newell. 2004. Comparison of the biotypes of Yersinia enterocolitica isolated from pigs, cattle and sheep at slaughter and from humans with yersiniosis in Great Britain during 1999-2000. Lett. Appl. Microbiol. 39: 103-108.
40. Messelhäusser, U., P. Kämpf, J. Colditz, H. Bauer, H. Schreiner, C. Höller, and U. Busch. 2011. Qualitative and quantitative detection of human pathogenic Yersinia enterocolitica in different food matrices at retail level in Bavaria. Foodborne Pathog. Dis. 8: 39-44.
41. Messelhäusser, U., R. Zucker, H. Ziegler, D. Elmer-Englhard, W. Kleih, C. Höller, and U. Busch. 2007. Detection of Clostridium botulinum type A, B, E and F with real-time PCR. J. Cons. Prot. Food Saf. 2: 198-201.
42. Milnes, A. S., I. Stewart, F. A. Clifton-Hadley, R. H. Davies, D. G. Newell, A. R. Sayers, T. Cheasty, C. Cassar, A. Ridley, A. J. Cook, S. J. Evans, C. J. Teale, R. P. Smith, A. McNally, M. Toszeghy, R. Futter, A. Kay, and G. A. Paiba. 2008. Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol. Infect. 136: 739-751.
43. Notermans, S. H., A. H. Havelaar, J. B. Dufrenne, and J. Oosterom. 1985. [Incidence of Clostridium botulinum on cattle farms]. Tijdschrift. Diergeneeskd. 110: 175-180.
44. O'Mahony, M., E. Mitchell, R. J. Gilbert, D. N. Hutchinson, N. T. Begg, J. C. Rodhouse, and J. E. Morris. 1990. An outbreak of foodborne botulism associated with contaminated hazelnut yoghurt. Epidemiol. Infect. 104: 389-395.
45. Rodriguez, C., B. Taminiau, J. Van Broeck, V. Avesani, M. Delmee, and G. Daube. 2012. Clostridium difficile in young farm animals and slaughter animals in Belgium. Anaerobe 8: 621-625.
46. Rodriguez-Palacios, A., M. Koohmaraie, and J. T. LeJeune. 2011. Prevalence, enumeration, and antimicrobial agent resistance of Clostridium difficile in cattle at harvest in the United States. J. Food Prot. 74: 1618-1624.
47. 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.
48. Rodriguez-Palacios, A., H. R. Stämpfli, 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.
49. Rodriguez-Palacios, A., H. R. Stämpfli, T. Duffield, and J. S. Weese. 2007. Clostridium difficile in retail ground meat, Canada. Emerg. Infect. Dis. 13: 485-487.
50. Romano, V., F. Albanese, S. Dumontet, K. Krovacek, O. Petrini, and V. Pasquale. 2012. Prevalence and genotypic characterization of Clostridium difficile from ruminants in Switzerland. Zoonoses Public Health 59: 545-548.
51. Schneeberg, A., M. Rupnik, H. Neubauer, and C. Seyboldt. 2012. Prevalence and distribution of Clostridium difficile PCR ribotypes in cats and dogs from animal shelters in Thuringia, Germany. Anaerobe 18: 484-488.
52. Smith, G. R., and A. M. Young. 1980. Clostridium botulinum in British soil. J. Hyg. (Lond.) 85: 271-274.
53. Songer, J. G., and M. A. Anderson. 2006. Clostridium difficile: an important pathogen of food animals. Anaerobe 12: 1-4.
54. 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.
55. 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.
56. Von Abercron, S. M., F. Karlsson, G. T. Wigh, M. Wierup, and K. Krovacek. 2009. Low occurrence of Clostridium difficile in retail ground meat in Sweden. J. Food Prot. 72: 1732-1734.
57. Weese, J. S., B. P. Avery, J. Rousseau, and R. J. Reid-Smith. 2009. Detection and enumeration of Clostridium difficile spores in retail beef and pork. Appl. Environ. Microbiol. 75: 5009-5011.
58. Weese, J. S., R. Finley, R. R. Reid-Smith, N. Janecko, and J. Rousseau. 2010. Evaluation of Clostridium difficile in dogs and the household environment. Epidemiol. Infect. 138: 1100-1104.
59. Ziegler, J. 2013. Comparative differentiation of Clostridium spp. with biochemical and molecular methods and MALDI-TOF mass spectrometry. Available at: http://edoc.ub.uni-muenchen.de/15463/1/Ziegler-Julia.pdf. Accessed April 2013.