Skip to main content
SpringerLink
Log in

Clostridium difficile: a new zoonotic agent?

Clostridium difficile: ein neuer Zoonoseerreger?

  • Review article
  • Published:
Wiener klinische Wochenschrift Aims and scope Submit manuscript

Zusammenfassung

Clostridium difficile wird meist als nosokomialer Erreger, der mit Diarrhö oder pseudomembranöser Colitis einhergeht, angesehen. Im Jahr 2007 wurden von Spitälern in Österreich 2.761 Clostridium-difficile-Infektionen (277 davon mit tödlichem Ausgang) gemeldet, im Vergleich dazu waren im Jahr 2003 nur 777 Fälle (53 davon mit tödlichem Ausgang) registriert worden. Neben diesem Anstieg der nosokomialen Erkrankungen wird auch über ein vermehrtes Auftreten von ambulant erworbenen C. difficile-Infektionen berichtet. Aktuelle Publikationen belegen das Vorkommen von C. difficile bei Tieren und in Lebensmitteln. Ziel der vorliegenden Studie war der Nachweis von C. difficile in Tieren und Lebensmitteln in Österreich. Zwischen März 2008 und Juli 2008 wurden Stuhl- und Kotproben von 67 Rindern, 61 Schweinen und 59 Broilern in österreichischen Schlachthöfen gesammelt. Zudem wurden Fleischproben (51 Rind [25 davon faschiert], 27 Schwein [17 faschiert] und 6 Hühnerfleischproben) zwischen Februar 2008 und April 2008 in Supermärkten gekauft und untersucht. Von den 187 getesteten Proben konnten in 8 C. difficile nachgewiesen werden: dabei waren 3/67 (4,5%) Kuhproben, 2/61 (3,3%) Schweineproben und 3/59 (5%) Hühnerproben positiv. Sechs der acht Isolate (2/67 [3%] Kuhproben, 2/61 [3,3%] Schweineproben und 2/59 [3,4%] Hühnerproben) waren toxinbildende C. difficile. In einem der zwei Toxin-positiven C. difficile Schweineproben war auch der Nachweis eines binären Toxin-Bildners des PCR-Ribotyps 126 möglich. In keiner der untersuchten Fleischproben konnte C. difficile nachgewiesen werden. Die Ergebnisse dieser Studie bestätigen, dass Tiere als Reservoir dienen können und eine Übertragung von C. difficile über Lebensmittel möglich ist.

Summary

Clostridium difficile is mainly considered a nosocomial pathogen associated with diarrhea and pseudomembranous colitis in hospitalized patients. Austrian hospitals reported 2761 cases of C. difficile infection (including 277 lethal outcomes) in 2007, compared with 777 cases (including 54 lethal outcomes) in 2003. The occurrence of community-acquired C. difficile infection is also increasingly reported. Recent studies have shown the occurrence of C. difficile in food and animals. The aim of the present study was to determine the occurrence of C. difficile in food and animals in Austria. Between March and July 2008, gut or fecal samples from 67 cows, 61 pigs and 59 broiler chickens were collected at Austrian abattoirs. Between February and April 2008 meat samples (51 beef [25 ground], 27 pork [17 ground] and 6 samples of chicken meat) were purchased at retail outlets. Of the 187 samples tested, eight yielded C. difficile: in cows 3/67 samples (4.5%) were positive, in pigs 2/61 (3.3%), in broiler chickens 3/59 (5%). Six of the eight isolates yielded toxigenic C. difficile (toxins A and B): 2/67 (3%) cow samples, 2/61 (3.3%) pig samples, 2/59 (3.4%) chicken samples. Genes for the binary toxin were detected in one of the two pig isolates, a PCR ribotype 126 strain. None of the 84 meat samples yielded C. difficile. The results of this Austrian study suggest that animal reservoirs are possible sources, via food, of human C. difficile infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

References

  • Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS (2007) Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis 13: 485–487

    PubMed  CAS  Google Scholar 

  • Kuijper EJ, Barbut F, Brazier JS, Kleinkauf N, Eckmanns T, Lambert ML, et al (2008) Update of Clostridium difficile infection due to PCR ribotype 027 in Europe, 2008. Euro Surveill 13 (31) pii: 18942

    Google Scholar 

  • Jhung MA, Thompson AD, Killgore GE, Zukowski WE, Songer G, Warny M, et al (2008) Toxinotype V Clostridium difficile in humans and food animals. Emerg Infect Dis 14: 1039–1045

    Article  PubMed  CAS  Google Scholar 

  • Kuijper EJ, Coignard B, Tüll P (2006) Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 12: 62–68

    Article  Google Scholar 

  • Indra A, Schmid D, Huhulescu S, Hell M, Gattringer R, Hasenberger P, et al (2008) Characterization of clinical Clostridium difficile isolates by PCR ribotyping and detection of toxin genes in Austria, 2006–2007. J Med Microbiol 57: 702–708

    Article  PubMed  CAS  Google Scholar 

  • Indra A, Huhulescu S, Kernbichler S, Kuo HW, Feierl G, Holler A, et al (2008) First cases of Clostridium difficile PCR ribotype 027 acquired in Austria. Euro Surveill 13 (20) pii: 18875

    Google Scholar 

  • McDonald LC, Owings M, Jernigan DB (2006) Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996–2003. Emerg Infect Dis 12: 409–415

    PubMed  Google Scholar 

  • Kuijper EJ, van den Berg RJ, Debast S, Visser CE, Veenendaal D, Troelstra A, et al (2006) Clostridium difficile ribotype 027, toxinotype III, the Netherlands. Emerg Infect Dis 12: 827–830

    PubMed  Google Scholar 

  • Lefebvre SL, Arroyo LG, Weese JS (2006) Epidemic Clostridium difficile strain in hospital visitation dog. Emerg Infect Dis 12: 1036–1037

    PubMed  Google Scholar 

  • 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 (Epub 2008 Apr 16)

    Article  PubMed  Google Scholar 

  • Borriello SP, Honour P (1981) Simplified procedure for the routine isolation of Clostridium difficile from faeces. J Clin Pathol 34: 1124–1127

    Article  PubMed  CAS  Google Scholar 

  • Clinical and Laboratory Standards Institute (2007) Methods for antimicrobial susceptibility testing of anaerobic bacteria, 7th edn. Approved standard M11–A7

  • Bidet P, Barbut F, Lalande V, Burghoffer B, Petit JC (1999) Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett 175: 261–266

    Article  PubMed  CAS  Google Scholar 

  • van den Berg RJ, Claas ECJ, Oyib DH, Klaassen CHW, Dijkshoorn L, Brazier JS, et al (2004) Characterization of toxin A-negative, toxin B-positive Clostridium difficile isolates from outbreaks in different countries by amplified fragment length polymorphism and PCR ribotyping. J Clin Microbiol 42: 1035–1041

    Article  PubMed  CAS  Google Scholar 

  • Kato H, Kato N, Watanabe K, Yamamoto T, Suzuki K, Ishigo S, et al (2001) Analysis of Clostridium difficile isolates from nosocomial outbreaks at three hospitals in diverse areas of Japan. J Clin Microbiol 39: 1391–1395

    Article  PubMed  CAS  Google Scholar 

  • Stubbs SL, Brazier JS, O'Neill GL, Duerden BI (1999) PCR targeted to the 16S–23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J Clin Microbiol 37: 461–463

    PubMed  CAS  Google Scholar 

  • Pépin J, Saheb N, Coulombe M, Alary M, Corriveau M, Authier S, et al (2005) Emergence of fluoroquinolones as the predominant risk factor for Clostridium difficile-associated diarrhea: a cohort study during an epidemic in Quebec. Clin Infect Dis 41: 1254–1260

    Article  PubMed  Google Scholar 

  • al Saif N, Brazier JS (1996) The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 45: 133–137

    PubMed  CAS  Google Scholar 

  • Songer JG, Post KW, Larson DJ, Jost H, Glock RD (2000) Infection of neonatal swine with Clostridium difficile. Swine Health and Production 8: 185–189

    Google Scholar 

  • Songer JG, Anderson MA (2006) Clostridium difficile: an important pathogen of food animals. Anaerobe 12: 1–4

    Article  PubMed  CAS  Google Scholar 

  • Simango C (2006) Prevalence of Clostridium difficile in the environment in a rural community in Zimbabwe. Trans R Soc Trop Med Hyg 100: 1146–1150

    Article  PubMed  Google Scholar 

  • Rodriguez-Palacios A, Stämpfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, et al (2006) Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis 12: 1730–1736

    PubMed  CAS  Google Scholar 

  • Goorhuis A, Bakker D, Corver J, Debast SB, Harmanus C, Notermans DW, et al (2008) Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin Infect Dis 47 (9): 1162–1170

    Article  PubMed  CAS  Google Scholar 

  • Stabler RA, Gerding DN, Songer JG, Drudy D, Brazier JS, Trinh HT, et al (2006) Comparative phylogenomics of Clostridium difficile reveals clade specificity and microevolution of hypervirulent strains. J Bacteriol 188: 7297–7305

    Article  PubMed  CAS  Google Scholar 

  • Indra A, Huhulescu S, Schneeweis M, Hasenberger P, Kernbichler S, Fiedler A, et al (2008) Characterization of Clostridium difficile isolates by capillary gel electrophoresis-based PCR ribotyping. J Med Microbiol 57: 1377–1382

    Article  PubMed  CAS  Google Scholar 

  • Weese JS, Rousseau J, Arroyo L (2005) Bacteriological evaluation of commercial canine and feline raw diets. Can Vet J 46: 513–516

    PubMed  Google Scholar 

  • Lefebvre SL, Waltner-Toews D, Peregrine AS, Reid-Smith R, Hodge L, Arroyo LG, et al (2006) Prevalence of zoonotic agents in dogs visiting hospitalized people in Ontario: implications for infection control. J Hosp Infect 62: 458–466

    Article  PubMed  CAS  Google Scholar 

  • Indra A, Huhulescu S, Hasenberger P, Schmid D, Alfery C, Wuerzner R, et al (2006) First isolation of Clostridium difficile PCR ribotype 027 in Austria. Euro Surveill 11: E060 914.3

    Google Scholar 

  • Rupnik M, Grabnar M, Geric B (2003) Binary toxin producing Clostridium difficile strains. Anaerobe 9: 289–294

    Article  PubMed  CAS  Google Scholar 

  • Bignardi GE, Settle C (2008) Different ribotypes in community-acquired Clostridium difficile. J Hosp Infect 70: 96–98

    Article  PubMed  CAS  Google Scholar 

  • Arroyo LG, Kruth SA, Willey BM, Staempfli HR, Low DE, Weese JS (2005) PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. J Med Microbiol 54: 163–166

    Article  PubMed  CAS  Google Scholar 

  • Goorhuis A, Debast SB, van Leengoed LAMG, Harmanus C, Notermans DW, Bergwerff AA, et al (2008) Clostridium difficile PCR ribotype 078: an emerging strain in humans and in pigs? J Clin Microbiol 46: 1157–1158

    Article  PubMed  Google Scholar 

  • Keel K, Brazier JS, Post KW, Weese S, Songer JG (2007) Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species. J Clin Microbiol 45: 1963–1964

    Article  PubMed  CAS  Google Scholar 

  • Pirs T, Ocepek M, Rupnik M (2008) Isolation of Clostridium difficile from food animals in Slovenia. J Med Microbiol 57: 790–792

    Article  PubMed  CAS  Google Scholar 

  • Songer JG (2004) The emergence of Clostridium difficile as a pathogen of food animals. Anim Health Res Rev 5: 321–326

    Article  PubMed  Google Scholar 

  • Songer JG, Uzal FA (2005) Clostridial enteric infections in pigs. J Vet Diagn Invest 17: 528–536

    PubMed  Google Scholar 

  • Kuijper EJ, Coignard B, Tull P (2006) Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 12 [Suppl 6]: 2–18

    Article  PubMed  CAS  Google Scholar 

  • Joebstl M, Heuberger S, Nepf R, Koefer J, Wagner M (2008) Clostridium difficile in Rohprodukten tierischer Herkunft. In: Proceedings of the 31st OEGHMP Meeting, Bad Ischl, 2008, pp 37–38

  • Olson MM, Shanholtzer CJ, Lee JT, Gerding DN (1994) Ten years of prospective Clostridium difficile-associated disease surveillance and treatment at the Minneapolis VA Medical Center, 1982–1991. Infect Control Hosp Epidemiol 15: 371–381

    Article  PubMed  CAS  Google Scholar 

  • Simango C, Mwakurudza S (2008) Clostridium difficile in broiler chickens sold at market places in Zimbabwe and their antimicrobial susceptibility. Int J Food Microbiol 124: 268–270

    Article  PubMed  CAS  Google Scholar 

  • Barbut F, Petit JC (2001) Epidemiology of Clostridium difficile-associated infections. Clin Microbiol Infect 7: 405–410

    Article  PubMed  CAS  Google Scholar 

  • Brazier J, Patel B, Pearson A (2007) Distribution of Clostridium difficile PCR ribotype 027 in British hospitals. Euro Surveill 12E070426.2 www.eurosurveillance.org/ew/2007/070426.asp#2

  • Bauer MP, Goorhuis A, Koster T, Numan-Ruberg SC, Hagen EC, Debast SB, et al (2008) Community-onset Clostridium difficile-associated diarrhoea not associated with antibiotic usage – two case reports with review of the changing epidemiology of Clostridium difficile-associated diarrhoea. Neth J Med 66: 207–211

    PubMed  CAS  Google Scholar 

  • Benson L, Song X, Campos J, Singh N (2007) Changing epidemiology of Clostridium difficile-associated disease in children. Infect Control Hosp Epidemiol 28: 1233–1235

    Article  PubMed  Google Scholar 

  • DuPont HL, Garey K, Caeiro J, Jiang Z (2008) New advances in Clostridium difficile infection: changing epidemiology, diagnosis, treatment and control. Curr Opin Infect Dis 21: 500–507

    Article  PubMed  Google Scholar 

  • Leal J, Gregson DB, Ross T, Church DL, Laupland KB (2008) Epidemiology of Clostridium species bacteremia in Calgary, Canada, 2000–2006. J Infect 57: 198–203

    Article  PubMed  CAS  Google Scholar 

  • Wilcox MH, Mooney L, Bendall R, Settle CD, Fawley WN (2008) A case-control study of community-associated Clostridium difficile infection. J Antimicrob Chemother 62: 388–396

    Article  PubMed  CAS  Google Scholar 

  • Anonymous (2005) Severe Clostridium difficile-associated disease in populations previously at low risk – four states, 2005. MMWR Morb Mortal Wkly Rep 54: 1201–1205

    Google Scholar 

  • Huhulescu S, Kiss R, Brettlecker M, Cerney R, Hess C, Wewalka G, et al (2008) Etiology of acute gastroenteritis in three sentinel general practices, Austria 2007. Infection (in press)

  • Rupnik M (2007) Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease? Clin Microbiol Infect 13: 457–459

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Austrian Agency for Health and Food Safety, Institute of Medical Microbiology and Hygiene, National Reference Center for Clostridium difficile, Wien, Austria

    Alexander Indra, Nina Baliko, Anita Fiedler, Steliana Huhulescu & Franz Allerberger

  2. Austrian Agency for Health and Food Safety, Institute of Veterinary Medicine, Graz, Austria

    Heimo Lassnig

  3. Austrian Agency for Health and Food Safety, Center for Infectious Diseases Epidemiology, Wien, Austria

    Peter Much

Authors
  1. Alexander Indra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heimo Lassnig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nina Baliko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter Much
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anita Fiedler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Steliana Huhulescu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Franz Allerberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander Indra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Indra, A., Lassnig, H., Baliko, N. et al. Clostridium difficile: a new zoonotic agent?. Wien Klin Wochenschr 121, 91–95 (2009). https://doi.org/10.1007/s00508-008-1127-x

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00508-008-1127-x

Keywords

Search

Navigation