Skip to main content
SpringerLink
Log in

Underestimation of Clostridium difficile infection among clinicians: an international survey

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

An Erratum to this article was published on 29 August 2012

Abstract

The objective of this investigation was to document clinicians’ awareness regarding the incidence and severity of Clostridium difficile-associated diarrhea (CDAD). An international electronic survey was conducted among corresponding authors of articles indexed by PubMed and published during the last 10 years in ‘Core Clinical Journals’. A total of 1,163 clinicians answered (response rate 59%); most of the responses were submitted from North America (54.6%), Europe (32.2%), and Asia/Pacific (11.6%). Only 2.2% of the participants answered correctly all four questions, while 14.1% answered all questions incorrectly. Regarding each question, 10.8% of the participants correctly estimated current CDAD treatment failure or recurrence rates to be around 40%, 33.4% correctly estimated the ratio of antibiotic-associated colitis attributed to C. difficile to be around 60%, 72.7% correctly responded that almost all antibiotics are associated with CDAD, and 41.7% correctly responded that any patient is at risk for CDAD. Almost half (44.4%) of the respondents considered CDAD to be underestimated. Participants from North America scored higher than those from Europe or Asia/Pacific (p < 0.001). Participants considering CDAD to be overestimated (3.4%) had the lowest mean score of correct answers. Among a clinically diverse international sample of physicians with academic expertise, there was an inadequate level of awareness of the magnitude and clinical importance of CDAD.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Centers for Disease Control and Prevention (CDC), Morbidity and Mortality Weekly Report (MMWR) (2011) QuickStats: Rates of Clostridium difficile infection among hospitalized patients aged ≥65 years,* by age group—National Hospital Discharge Survey, United States, 1996–2009; 60(34):1171

  2. Clements AC, Magalhães RJ, Tatem AJ, Paterson DL, Riley TV (2010) Clostridium difficile PCR ribotype 027: assessing the risks of further worldwide spread. Lancet Infect Dis 10:395–404

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. Ricciardi R, Rothenberger DA, Madoff RD, Baxter NN (2007) Increasing prevalence and severity of Clostridium difficile colitis in hospitalized patients in the United States. Arch Surg 142:624–631; discussion 631

    Article  PubMed  Google Scholar 

  6. Vonberg RP, Schwab F, Gastmeier P (2007) Clostridium difficile in discharged inpatients, Germany. Emerg Infect Dis 13:179–180

    PubMed  Google Scholar 

  7. Wilcox MH, Smyth ET (1998) Incidence and impact of Clostridium difficile infection in the UK, 1993–1996. J Hosp Infect 39:181–187

    Article  PubMed  CAS  Google Scholar 

  8. Zilberberg MD, Shorr AF, Kollef MH (2008) Increase in adult Clostridium difficile-related hospitalizations and case–fatality rate, United States, 2000–2005. Emerg Infect Dis 14:929–931

    Article  PubMed  Google Scholar 

  9. Coignard B, Barbut F, Blanckaert K, Thiolet JM, Poujol I, Carbonne A, Petit JC, Desenclos JC (2006) Emergence of Clostridium difficile toxinotype III, PCR-ribotype 027-associated disease, France, 2006. Euro Surveill 11(9):E060914.1

    Google Scholar 

  10. Loo VG, Poirier L, Miller MA, Oughton M, Libman MD, Michaud S, Bourgault AM, Nguyen T, Frenette C, Kelly M, Vibien A, Brassard P, Fenn S, Dewar K, Hudson TJ, Horn R, René P, Monczak Y, Dascal A (2005) A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 353:2442–2449

    Article  PubMed  CAS  Google Scholar 

  11. Muto CA, Pokrywka M, Shutt K, Mendelsohn AB, Nouri K, Posey K, Roberts T, Croyle K, Krystofiak S, Patel-Brown S, Pasculle AW, Paterson DL, Saul M, Harrison LH (2005) A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol 26:273–280

    Article  PubMed  Google Scholar 

  12. Pépin J, Valiquette L, Alary ME, Villemure P, Pelletier A, Forget K, Pépin K, Chouinard D (2004) Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 171:466–472

    Article  PubMed  Google Scholar 

  13. McDonald LC, Killgore GE, Thompson A, Owens RC Jr, Kazakova SV, Sambol SP, Johnson S, Gerding DN (2005) An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 353:2433–2441

    Article  PubMed  CAS  Google Scholar 

  14. Warny M, Pepin J, Fang A, Killgore G, Thompson A, Brazier J, Frost E, McDonald LC (2005) Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 366:1079–1084

    Article  PubMed  CAS  Google Scholar 

  15. Cheng VC, Yam WC, Chan JF, To KK, Ho PL, Yuen KY (2009) Clostridium difficile ribotype 027 arrives in Hong Kong. Int J Antimicrob Agents 34:492–493

    Article  PubMed  CAS  Google Scholar 

  16. Kato H, Ito Y, van den Berg RJ, Kuijper EJ, Arakawa Y (2007) First isolation of Clostridium difficile 027 in Japan. Euro Surveill 12(1):E070111.3

    Google Scholar 

  17. Kuijper EJ, Barbut F, Brazier JS, Kleinkauf N, Eckmanns T, Lambert ML, Drudy D, Fitzpatrick F, Wiuff C, Brown DJ, Coia JE, Pituch H, Reichert P, Even J, Mossong J, Widmer AF, Olsen KE, Allerberger F, Notermans DW, Delmée M, Coignard B, Wilcox M, Patel B, Frei R, Nagy E, Bouza E, Marin M, Akerlund T, Virolainen-Julkunen A, Lyytikäinen O, Kotila S, Ingebretsen A, Smyth B, Rooney P, Poxton IR, Monnet DL (2008) Update of Clostridium difficile infection due to PCR ribotype 027 in Europe, 2008. Euro Surveill 13(31). pi: 18942

    Google Scholar 

  18. Lim PL, Ling ML, Lee HY, Koh TH, Tan AL, Kuijper EJ, Goh SS, Low BS, Ang LP, Harmanus C, Lin RT, Krishnan P, James L, Lee CE (2011) Isolation of the first three cases of Clostridium difficile polymerase chain reaction ribotype 027 in Singapore. Singapore Med J 52:361–364

    PubMed  CAS  Google Scholar 

  19. Quesada-Gómez C, Rodríguez C, Gamboa-Coronado Mdel M, Rodríguez-Cavallini E, Du T, Mulvey MR, Villalobos-Zúñiga M, Boza-Cordero R (2010) Emergence of Clostridium difficile NAP1 in Latin America. J Clin Microbiol 48:669–670

    Article  PubMed  Google Scholar 

  20. Riley TV, Thean S, Hool G, Golledge CL (2009) First Australian isolation of epidemic Clostridium difficile PCR ribotype 027. Med J Aust 190:706–708

    PubMed  Google Scholar 

  21. Tae CH, Jung SA, Song HJ, Kim SE, Choi HJ, Lee M, Hwang Y, Kim H, Lee K (2009) The first case of antibiotic-associated colitis by Clostridium difficile PCR ribotype 027 in Korea. J Korean Med Sci 24:520–524

    Article  PubMed  CAS  Google Scholar 

  22. Kyne L, Hamel MB, Polavaram R, Kelly CP (2002) Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis 34:346–353

    Article  PubMed  Google Scholar 

  23. Vardakas KZ, Polyzos KA, Patouni K, Rafailidis PI, Samonis G, Falagas ME (2012) Treatment failure and recurrence of Clostridium difficile infection following treatment with vancomycin or metronidazole: a systematic review of the evidence. Int J Antimicrob Agents. doi:10.1016/j.ijantimicag.2012.01.004

  24. Hautmann MG, Hipp M, Kölbl O (2011) Clostridium difficile-associated diarrhea in radiooncology: an underestimated problem for the feasibility of the radiooncological treatment? Radiat Oncol 6:89

    Article  PubMed  Google Scholar 

  25. Navaneethan U, Schauer D, Giannella R (2011) Awareness about Clostridium difficile infection among internal medicine residents in the United States. Minerva Gastroenterol Dietol 57:231–240

    PubMed  CAS  Google Scholar 

  26. Alexiou VG, Ierodiakonou V, Peppas G, Falagas ME (2010) Antimicrobial prophylaxis in surgery: an international survey. Surg Infect (Larchmt) 11:343–348

    Article  Google Scholar 

  27. Falagas ME, Ierodiakonou V, Alexiou VG (2009) Clinical practice of obtaining blood cultures from patients with a central venous catheter in place: an international survey. Clin Microbiol Infect 15:683–686

    Article  PubMed  CAS  Google Scholar 

  28. Falagas ME, Makris GC, Karageorgopoulos DE, Batsiou M, Alexiou VG (2009) How well do clinical researchers understand risk estimates? Epidemiology 20:930–931

    Article  PubMed  Google Scholar 

  29. United States National Library of Medicine (2011) Abridged Index Medicus (AIM or “Core Clinical”) Journal Titles. Available online at: http://www.nlm.nih.gov/bsd/aim.html. Accessed 2 November 2011

  30. Mullane KM, Miller MA, Weiss K, Lentnek A, Golan Y, Sears PS, Shue YK, Louie TJ, Gorbach SL (2011) Efficacy of fidaxomicin versus vancomycin as therapy for Clostridium difficile infection in individuals taking concomitant antibiotics for other concurrent infections. Clin Infect Dis 53:440–477

    Article  PubMed  CAS  Google Scholar 

  31. Louie TJ, Miller MA, Mullane KM, Weiss K, Lentnek A, Golan Y, Gorbach S, Sears P, Shue YK, OPT-80-003 Clinical Study Group (2011) Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med 364:422–431

    Article  PubMed  CAS  Google Scholar 

  32. Bartlett JG (2002) Clinical practice. Antibiotic-associated diarrhea. N Engl J Med 346:334–349

    Article  PubMed  Google Scholar 

  33. Kelly CP, Pothoulakis C, LaMont JT (1994) Clostridium difficile colitis. N Engl J Med 330:257–262

    Article  PubMed  CAS  Google Scholar 

  34. Asha NJ, Wilcox MH (2002) Laboratory diagnosis of Clostridium perfringens antibiotic-associated diarrhoea. J Med Microbiol 51:891–894

    PubMed  CAS  Google Scholar 

  35. Olsen SJ, DeBess EE, McGivern TE, Marano N, Eby T, Mauvais S, Balan VK, Zirnstein G, Cieslak PR, Angulo FJ (2001) A nosocomial outbreak of fluoroquinolone-resistant salmonella infection. N Engl J Med 344:1572–1579

    Article  PubMed  CAS  Google Scholar 

  36. Levine J, Dykoski RK, Janoff EN (1995) Candida-associated diarrhea: a syndrome in search of credibility. Clin Infect Dis 21:881–886

    Article  PubMed  CAS  Google Scholar 

  37. Neal KR, Briji SO, Slack RC, Hawkey CJ, Logan RF (1994) Recent treatment with H2 antagonists and antibiotics and gastric surgery as risk factors for salmonella infection. BMJ 308:176

    Article  PubMed  CAS  Google Scholar 

  38. Kuntz JL, Chrischilles EA, Pendergast JF, Herwaldt LA, Polgreen PM (2011) Incidence of and risk factors for community-associated Clostridium difficile infection: a nested case–control study. BMC Infect Dis 11:194

    Article  PubMed  Google Scholar 

  39. Pepin J, Saheb N, Coulombe MA, Alary ME, Corriveau MP, Authier S, Leblanc M, Rivard G, Bettez M, Primeau V, Nguyen M, Jacob CE, Lanthier L (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  CAS  Google Scholar 

  40. Allard R, Dascal A, Camara B, Létourneau J, Valiquette L (2011) Community-acquired Clostridium difficile-associated diarrhea, Montréal, 2005–2006: frequency estimates and their validity. Infect Control Hosp Epidemiol 32:1032–1034

    Article  PubMed  Google Scholar 

  41. Garey KW, Jiang ZD, Yadav Y, Mullins B, Wong K, Dupont HL (2008) Peripartum Clostridium difficile infection: case series and review of the literature. Am J Obstet Gynecol 199:332–337

    Article  PubMed  Google Scholar 

  42. 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 

  43. Kelly CP, LaMont JT (2008) Clostridium difficile—more difficult than ever. N Engl J Med 359:1932–1940

    Article  PubMed  CAS  Google Scholar 

  44. RML Specialty Hospital—Hinsdale, Illinois. Reducing hospital-acquired Clostridium difficile transmission rates. Available online at: http://www.aha.org/content/00-10/10postacutecase-rmlspec.pdf. Accessed 2 November 2011

  45. Centers for Diseases Control and Prevention (CDC) (2011) Clostridium difficile infection (CDI) baseline prevention practices assessment tool for states establishing HAI prevention collaboratives using ARRA funds. Available online at: http://www.cdc.gov/HAI/recoveryact/PDF/CDI_EvalQuestions_Final_Clearedversion32910.pdf. Accessed 2 November 2011

  46. Schmidt WC (1997) World-Wide Web survey research: benefits, potential problems, and solutions. Behav Res Methods 29:274–279

    Article  Google Scholar 

  47. Wright KB (2005) Researching Internet-based populations: advantages and disadvantages of online survey research, online questionnaire authoring software packages, and Web survey services. J Comput Med Commun 10(3), article 11

    Google Scholar 

Download references

Funding

Astellas Pharma Europe.

Author information

Authors and Affiliations

  1. Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23, Marousi, Athens, Greece

    M. N. Mavros, V. G. Alexiou, K. Z. Vardakas, K. Tsokali, T. A. Sardi & M. E. Falagas

  2. Department of Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    M. N. Mavros

  3. Department of Surgery, University Hospitals of Leicester, Leicester, UK

    V. G. Alexiou

  4. Department of Applied Mathematics and Physics, National Technical University of Athens, Athens, Greece

    K. Tsokali

  5. Department of Medicine, Henry Dunant Hospital, Athens, Greece

    K. Z. Vardakas & M. E. Falagas

  6. Department of Medicine, Tufts University School of Medicine, Boston, MA, USA

    M. E. Falagas

Authors
  1. M. N. Mavros
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. G. Alexiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Z. Vardakas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Tsokali
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. A. Sardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. E. Falagas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. E. Falagas.

About this article

Cite this article

Mavros, M.N., Alexiou, V.G., Vardakas, K.Z. et al. Underestimation of Clostridium difficile infection among clinicians: an international survey. Eur J Clin Microbiol Infect Dis 31, 2439–2444 (2012). https://doi.org/10.1007/s10096-012-1587-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-012-1587-9

Keywords

Search

Navigation