1887

Abstract

This study provides data on the distribution and relationship of PCR ribotypes in diarrhoeic calves in Germany. was isolated from 176 of 999 (17.6 %) faecal samples or swabs of diarrhoeic calves from 603 farms collected between January 2010 and August 2012 by eight federal laboratories of six states. Strains were assigned to 17 PCR ribotypes. PCR ribotypes 033 (57 %), 078 (17 %) and 045/FLI01 (closest match to 045 in the WEBRIBO database; 9 %) were found the most frequently. Nine per cent of all culture-positive tested animals shed more than one multiple locus variable number tandem repeat analysis (MLVA) or PCR ribotype. Eight PCR ribotypes with related profiles (including 033, 078 and 045/FLI01) representing 92 % of all isolates were grouped into three clusters. Molecular relatedness was supported by the absence of the MLVA locus A6 only in clustered strains and identical toxin gene profiles for strains within each cluster. Previously reported mulitilocus sequence typing analysis for PCR ribotypes that were also recovered in this study found identical sequence types and a deletion (Δ39 bp) for 033, 045, 078 and 126 (ST-11), confirming this clustering. A different geographical occurrence of PCR ribotypes was shown for cluster 033 (found more frequently in southern Germany) and 045 (found more frequently in northern Germany). This study showed that clusters of PCR ribotypes related to 033, 078 and 045 are predominant in diarrhoeic calves in Germany. The high number of strains belonging to PCR ribotype 078 demonstrated that diarrhoeic calves are also potential reservoirs for human pathogenic strains.

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2013-08-01
2019-10-23
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References

  1. Avbersek J. , Janezic S. , Pate M. , Rupnik M. , Zidaric V. , Logar K. , Vengust M. , Zemljic M. , Pirs T. , Ocepek M. . ( 2009; ). Diversity of Clostridium difficile in pigs and other animals in Slovenia. . Anaerobe 15:, 252–255. [CrossRef] [PubMed]
    [Google Scholar]
  2. Bakker D. , Corver J. , Harmanus C. , Goorhuis A. , Keessen E. C. , Fawley W. N. , Wilcox M. H. , Kuijper E. J. . ( 2010; ). Relatedness of human and animal Clostridium difficile PCR ribotype 078 isolates based on multi locus variable number of tandem repeat analysis and tetracycline resistance. . J Clin Microbiol 48:, 3744–3749.[CrossRef]
    [Google Scholar]
  3. Bauer M. P. , Notermans D. W. , van Benthem B. H. , Brazier J. S. , Wilcox M. H. , Rupnik M. , Monnet D. L. , van Dissel J. T. , Kuijper E. J. . ECDIS Study Group ( 2011; ). Clostridium difficile infection in Europe: a hospital-based survey. . Lancet 377:, 63–73. [CrossRef] [PubMed]
    [Google Scholar]
  4. Clopper C. J. , Pearson E. S. . ( 1934; ). The use of confidence or fiducial limits illustrated in the case of the binomial. . Biometrika 26:, 404–413. [CrossRef]
    [Google Scholar]
  5. Costa M. C. , Stämpfli H. R. , Arroyo L. G. , Pearl D. L. , Weese J. S. . ( 2011; ). Epidemiology of Clostridium difficile on a veal farm: prevalence, molecular characterization and tetracycline resistance. . Vet Microbiol 152:, 379–384. [CrossRef] [PubMed]
    [Google Scholar]
  6. Costa M. C. , Reid-Smith R. , Gow S. , Hannon S. J. , Booker C. , Rousseau J. , Benedict K. M. , Morley P. S. , Weese J. S. . ( 2012; ). Prevalence and molecular characterization of Clostridium difficile isolated from feedlot beef cattle upon arrival and mid-feeding period. . BMC Vet Res 8:, 38. [CrossRef] [PubMed]
    [Google Scholar]
  7. Debast S. B. , van Leengoed L. A. , Goorhuis A. , Harmanus C. , Kuijper E. J. , Bergwerff A. A. . ( 2009; ). Clostridium difficile PCR ribotype 078 toxinotype V found in diarrhoeal pigs identical to isolates from affected humans. . Environ Microbiol 11:, 505–511. [CrossRef] [PubMed]
    [Google Scholar]
  8. Goorhuis A. , Bakker D. , Corver J. , Debast S. B. , Harmanus C. , Notermans D. W. , Bergwerff A. A. , Dekker F. W. , Kuijper E. J. . ( 2008; ). Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. . Clin Infect Dis 47:, 1162–1170. [CrossRef] [PubMed]
    [Google Scholar]
  9. Hammitt M. C. , Bueschel D. M. , Keel M. K. , Glock R. D. , Cuneo P. , DeYoung D. W. , Reggiardo C. , Trinh H. T. , Songer J. G. . ( 2008; ). A possible role for Clostridium difficile in the etiology of calf enteritis. . Vet Microbiol 127:, 343–352. [CrossRef] [PubMed]
    [Google Scholar]
  10. Hensgens M. P. , Keessen E. C. , Squire M. M. , Riley T. V. , Koene M. G. , de Boer E. , Lipman L. J. , Kuijper E. J. . on behalf of European Society of Clinical Microbiology and Infectious Diseases Study Group for Clostridium difficile (ESGCD) ( 2012; ). Clostridium difficile infection in the community: a zoonotic disease?. Clin Microbiol Infect 18:, 635–645. [CrossRef] [PubMed]
    [Google Scholar]
  11. Hoffer E. , Haechler H. , Frei R. , Stephan R. . ( 2010; ). Low occurrence of Clostridium difficile in fecal samples of healthy calves and pigs at slaughter and in minced meat in Switzerland. . J Food Prot 73:, 973–975.[PubMed]
    [Google Scholar]
  12. Indra A. , Huhulescu S. , Schneeweis M. , Hasenberger P. , Kernbichler S. , Fiedler A. , Wewalka G. , Allerberger F. , Kuijper E. J. . ( 2008; ). Characterization of Clostridium difficile isolates using capillary gel electrophoresis-based PCR ribotyping. . J Med Microbiol 57:, 1377–1382. [CrossRef] [PubMed]
    [Google Scholar]
  13. Indra A. , Lassnig H. , Baliko N. , Much P. , Fiedler A. , Huhulescu S. , Allerberger F. . ( 2009; ). [ Clostridium difficile: a new zoonotic agent?]. Wien Klin Wochenschr 121:, 91–95 (in German). [CrossRef] [PubMed]
    [Google Scholar]
  14. Jamal W. , Rotimi V. O. , Brazier J. , Duerden B. I. . ( 2010; ). Analysis of prevalence, risk factors and molecular epidemiology of Clostridium difficile infection in Kuwait over a 3-year period. . Anaerobe 16:, 560–565. [CrossRef] [PubMed]
    [Google Scholar]
  15. Jank T. , Giesemann T. , Aktories K. . ( 2007; ). Rho-glucosylating Clostridium difficile toxins A and B: new insights into structure and function. . Glycobiology 17:, 15R–22R. [CrossRef] [PubMed]
    [Google Scholar]
  16. Jhung M. A. , Thompson A. D. , Killgore G. E. , Zukowski W. E. , Songer G. , Warny M. , Johnson S. , Gerding D. N. , McDonald L. C. , Limbago B. M. . ( 2008; ). Toxinotype V Clostridium difficile in humans and food animals. . Emerg Infect Dis 14:, 1039–1045. [CrossRef] [PubMed]
    [Google Scholar]
  17. Kato H. , Kato N. , Watanabe K. , Iwai N. , Nakamura H. , Yamamoto T. , Suzuki K. , Kim S. M. , Chong Y. , Wasito E. B. . ( 1998; ). Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. . J Clin Microbiol 36:, 2178–2182.[PubMed]
    [Google Scholar]
  18. Keel M. K. , Songer J. G. . ( 2006; ). The comparative pathology of Clostridium difficile-associated disease. . Vet Pathol 43:, 225–240. [CrossRef] [PubMed]
    [Google Scholar]
  19. Keel K. , Brazier J. S. , Post K. W. , Weese S. , Songer J. G. . ( 2007; ). Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species. . J Clin Microbiol 45:, 1963–1964. [CrossRef] [PubMed]
    [Google Scholar]
  20. Khanna S. , Pardi D. S. , Aronson S. L. , Kammer P. P. , Orenstein R. , St Sauver J. L. , Harmsen W. S. , Zinsmeister A. R. . ( 2012; ). The epidemiology of community-acquired Clostridium difficile infection: a population-based study. . Am J Gastroenterol 107:, 89–95. [CrossRef] [PubMed]
    [Google Scholar]
  21. Knetsch C. W. , Hensgens M. P. , Harmanus C. , van der Bijl M. W. , Savelkoul P. H. , Kuijper E. J. , Corver J. , van Leeuwen H. C. . ( 2011; ). Genetic markers for Clostridium difficile lineages linked to hypervirulence. . Microbiology 157:, 3113–3123. [CrossRef] [PubMed]
    [Google Scholar]
  22. Knetsch C. W. , Terveer E. M. , Lauber C. , Gorbalenya A. E. , Harmanus C. , Kuijper E. J. , Corver J. , van Leeuwen H. C. . ( 2012; ). Comparative analysis of an expanded Clostridium difficile reference strain collection reveals genetic diversity and evolution through six lineages. . Infect Genet Evol 12:, 1577–1585. [CrossRef] [PubMed]
    [Google Scholar]
  23. Koene M. G. , Mevius D. , Wagenaar J. A. , Harmanus C. , Hensgens M. P. , Meetsma A. M. , Putirulan F. F. , van Bergen M. A. , Kuijper E. J. . ( 2012; ). Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. . Clin Microbiol Infect 218:, 778–784.[PubMed] [CrossRef]
    [Google Scholar]
  24. Kuehne S. A. , Cartman S. T. , Minton N. P. . ( 2011; ). Both, toxin A and toxin B, are important in Clostridium difficile infection. . Gut Microbes 2:, 252–255. [CrossRef] [PubMed]
    [Google Scholar]
  25. Lentz H. H. , Konschake M. , Teske K. , Kasper M. , Rother B. , Carmanns R. , Petersen B. , Conraths F. J. , Selhorst T. . ( 2011; ). Trade communities and their spatial patterns in the German pork production network. . Prev Vet Med 98:, 176–181. [CrossRef] [PubMed]
    [Google Scholar]
  26. Limbago B. , Thompson A. D. , Greene S. A. , MacCannell D. , MacGowan C. E. , Jolbitado B. , Hardin H. D. , Estes S. R. , Weese J. S. . & other authors ( 2012; ). Development of a consensus method for culture of Clostridium difficile from meat and its use in a survey of U.S. retail meats. . Food Microbiol 32:, 448–451. [CrossRef] [PubMed]
    [Google Scholar]
  27. Metcalf D. S. , Costa M. C. , Dew W. M. , Weese J. S. . ( 2010; ). Clostridium difficile in vegetables, Canada. . Lett Appl Microbiol 51:, 600–602. [CrossRef] [PubMed]
    [Google Scholar]
  28. Metcalf D. , Avery B. P. , Janecko N. , Matic N. , Reid-Smith R. , Weese J. S. . ( 2011; ). Clostridium difficile in seafood and fish. . Anaerobe 17:, 85–86. [CrossRef] [PubMed]
    [Google Scholar]
  29. Papatheodorou P. , Carette J. E. , Bell G. W. , Schwan C. , Guttenberg G. , Brummelkamp T. R. , Aktories K. . ( 2011; ). Lipolysis-stimulated lipoprotein receptor (LSR) is the host receptor for the binary toxin Clostridium difficile transferase (CDT). . Proc Natl Acad Sci U S A 108:, 16422–16427.[CrossRef]
    [Google Scholar]
  30. Pirs T. , Ocepek M. , Rupnik M. . ( 2008; ). Isolation of Clostridium difficile from food animals in Slovenia. . J Med Microbiol 57:, 790–792. [CrossRef] [PubMed]
    [Google Scholar]
  31. Pituch H. , Brazier J. S. , Obuch-Woszczatynski P. , Wultanska D. , Meisel-Mikolajczyk F. , Luczak M. . ( 2006; ). Prevalence and association of PCR ribotypes of Clostridium difficile isolated from symptomatic patients from Warsaw with macrolide-lincosamide-streptogramin B (MLSB) type resistance. . J Med Microbiol 55:, 207–213. [CrossRef] [PubMed]
    [Google Scholar]
  32. Princewell T. J. , Agba M. I. . ( 1982; ). Examination of bovine faeces for the isolation and identification of Clostridium species. . J Appl Bacteriol 52:, 97–102. [CrossRef] [PubMed]
    [Google Scholar]
  33. Reil M. , Hensgens M. P. , Kuijper E. J. , Jakobiak T. , Gruber H. , Kist M. , Borgmann S. . ( 2012; ). Seasonality of Clostridium difficile infections in Southern Germany. . Epidemiol Infect 140:, 1787–1793. [CrossRef] [PubMed]
    [Google Scholar]
  34. Rodriguez C. , Taminiau B. , Van Broeck J. , Avesani V. , Delmée M. , Daube G. . ( 2012; ). Clostridium difficile in young farm animals and slaughter animals in Belgium. . Anaerobe 18:, 621–625. [CrossRef] [PubMed]
    [Google Scholar]
  35. Rodriguez-Palacios A. , Stämpfli H. R. , Duffield T. , Peregrine A. S. , Trotz-Williams L. A. , Arroyo L. G. , Brazier J. S. , Weese J. S. . ( 2006; ). Clostridium difficile PCR ribotypes in calves, Canada. . Emerg Infect Dis 12:, 1730–1736. [CrossRef] [PubMed]
    [Google Scholar]
  36. Rodriguez-Palacios A. , Stämpfli H. R. , Stalker M. , Duffield T. , Weese J. S. . ( 2007; ). Natural and experimental infection of neonatal calves with Clostridium difficile. . Vet Microbiol 124:, 166–172. [CrossRef] [PubMed]
    [Google Scholar]
  37. Rodriguez-Palacios A. , Reid-Smith R. J. , Staempfli H. R. , Daignault D. , Janecko N. , Avery B. P. , Martin H. , Thomspon A. D. , McDonald L. C. . & other authors ( 2009; ). Possible seasonality of Clostridium difficile in retail meat, Canada. . Emerg Infect Dis 15:, 802–805. [CrossRef] [PubMed]
    [Google Scholar]
  38. Rodriguez-Palacios A. , Koohmaraie M. , LeJeune J. T. . ( 2011a; ). Prevalence, enumeration, and antimicrobial agent resistance of Clostridium difficile in cattle at harvest in the United States. . J Food Prot 74:, 1618–1624. [CrossRef] [PubMed]
    [Google Scholar]
  39. Rodriguez-Palacios A. , Pickworth C. , Loerch S. , LeJeune J. T. . ( 2011b; ). Transient fecal shedding and limited animal-to-animal transmission of Clostridium difficile by naturally infected finishing feedlot cattle. . Appl Environ Microbiol 77:, 3391–3397. [CrossRef] [PubMed]
    [Google Scholar]
  40. Romano V. , Albanese F. , Dumontet S. , Krovacek K. , Petrini O. , Pasquale V. . ( 2012; ). Prevalence and genotypic characterization of Clostridium difficile from ruminants in Switzerland. . Zoonoses Public Health 59:, 545–548. [CrossRef] [PubMed]
    [Google Scholar]
  41. Rupnik M. . ( 2007; ). Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease?. Clin Microbiol Infect 13:, 457–459. [CrossRef] [PubMed]
    [Google Scholar]
  42. Rupnik M. , Just I. . ( 2006; ). Large clostridial cytotoxins modifying small GTPases. . In The Comprehensive Sourcebook of Bacterial Protein Toxins, , 3rd edn., pp. 409–429. Edited by Joseph E. A. , Michel R. P. . . London:: Academic Press;. [CrossRef]
    [Google Scholar]
  43. Rupnik M. , Widmer A. , Zimmermann O. , Eckert C. , Barbut F. . ( 2008; ). Clostridium difficile toxinotype V, ribotype 078, in animals and humans. . J Clin Microbiol 46:, 2146. [CrossRef] [PubMed]
    [Google Scholar]
  44. Rupnik M. , Wilcox M. H. , Gerding D. N. . ( 2009; ). Clostridium difficile infection: new developments in epidemiology and pathogenesis. . Nat Rev Microbiol 7:, 526–536. [CrossRef] [PubMed]
    [Google Scholar]
  45. Sakurai J. , Nagahama M. , Oda M. , Tsuge H. , Kobayashi K. . ( 2009; ). Clostridium perfringens iota-toxin: structure and function. . Toxins (Basel) 1:, 208–228. [CrossRef] [PubMed]
    [Google Scholar]
  46. Songer J. G. , Anderson M. A. . ( 2006; ). Clostridium difficile: an important pathogen of food animals. . Anaerobe 12:, 1–4. [CrossRef] [PubMed]
    [Google Scholar]
  47. Stabler R. A. , Dawson L. F. , Valiente E. , Cairns M. D. , Martin M. J. , Donahue E. H. , Riley T. V. , Songer J. G. , Kuijper E. J. . & other authors ( 2012; ). Macro and micro diversity of Clostridium difficile isolates from diverse sources and geographical locations. . PLoS ONE 7:, e31559. [CrossRef] [PubMed]
    [Google Scholar]
  48. Stubbs S. , Rupnik M. , Gibert M. , Brazier J. , Duerden B. , Popoff M. . ( 2000; ). Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. . FEMS Microbiol Lett 186:, 307–312. [CrossRef] [PubMed]
    [Google Scholar]
  49. Thelestam M. , Chaves-Olarte E. . ( 2000; ). Cytotoxic effects of the Clostridium difficile toxins. . Curr Top Microbiol Immunol 250:, 85–96. [CrossRef] [PubMed]
    [Google Scholar]
  50. van den Berg R. J. , Schaap I. , Templeton K. E. , Klaassen C. H. , Kuijper E. J. . ( 2007; ). Typing and subtyping of Clostridium difficile isolates by using multiple-locus variable-number tandem-repeat analysis. . J Clin Microbiol 45:, 1024–1028. [CrossRef] [PubMed]
    [Google Scholar]
  51. Weese J. S. , Finley R. , Reid-Smith R. R. , Janecko N. , Rousseau J. . ( 2010; ). Evaluation of Clostridium difficile in dogs and the household environment. . Epidemiol Infect 138:, 1100–1104. [CrossRef] [PubMed]
    [Google Scholar]
  52. Wilcox M. H. , Mooney L. , Bendall R. , Settle C. D. , Fawley W. N. . ( 2008; ). A case–control study of community-associated Clostridium difficile infection. . J Antimicrob Chemother 62:, 388–396. [CrossRef] [PubMed]
    [Google Scholar]
  53. Zaiss N. H. , Witte W. , Nübel U. . ( 2010; ). Fluoroquinolone resistance and Clostridium difficile, Germany. . Emerg Infect Dis 16:, 675–677. [CrossRef] [PubMed]
    [Google Scholar]
  54. Zidaric V. , Zemljic M. , Janezic S. , Kocuvan A. , Rupnik M. . ( 2008; ). High diversity of Clostridium difficile genotypes isolated from a single poultry farm producing replacement laying hens. . Anaerobe 14:, 325–327. [CrossRef] [PubMed]
    [Google Scholar]
  55. Zidaric V. , Pardon B. , Dos Vultos T. , Deprez P. , Brouwer M. S. , Roberts A. P. , Henriques A. O. , Rupnik M. . ( 2012; ). Multiclonal presence of Clostridium difficile PCR ribotypes 078, 126 and 033 within a single calf farm is associated with differences in antibiotic resistance and sporulation properties. . Appl Environ Microbiol 21:, 21.
    [Google Scholar]
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