Skip to main content
SpringerLink
Log in

Clinical characteristics of Clostridium difficile infection in hospitalized patients with antibiotic-associated diarrhea in a university hospital in China

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

Abstract

The purpose of this study was to identify clinical characteristics of Clostridium difficile infection (CDI) in patients with antibiotic-associated diarrhea (AAD). A prospective study was conducted among patients hospitalized in Fudan University Hospital Huashan from August 1, 2012 to July 31, 2013. Toxigenic C. difficile isolates were characterized by PCR ribotyping and multilocus sequence typing. AAD developed in 1.0 % (206/20437) of the antibiotic-treated hospitalized patients and toxigenic C. difficile was isolated from 30.6 % (63/206) of patients with AAD. The frequency of AAD was highest in the intensive care unit (10.7 %); however the proportion of CDI in AAD was highest in the Geriatric Unit (38 %). AAD ranged in severity from mild to moderate. One case with pseudomembranous colitis was identified. Use of carbapenems was found to significantly increase the risk of CDI (OR, 2.31; 95 % CI, 1.22–4.38; p = 0.011). Patient demographics, presumed risk factors, clinical manifestations and laboratory findings revealed no significant difference between patients with CDI and non-C. difficile AAD. Over 90 % of the patients with CDI or non-C. difficile AAD were cured. Two patients had CDI recurrence. Ribotype H was the dominant (18.8 %) genotype, followed by ribotype 012 and ribotype 017. C. difficile plays a significant role in AAD in our setting in China. Because the severity of diarrhea ranges from mild to moderate, it is difficult for Chinese clinicians to identify CDI from AAD patients, therefore CDI should be included in the routine differential diagnoses for hospitalized patients presenting with AAD.

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. Beaugerie L, Petit JC (2004) Microbial-gut interactions in health and disease. Antibiot Assoc diarrhoea Best Pract Res Clin Gastroenterol 18(2):337–352

    Article  CAS  Google Scholar 

  2. Varughese CA, Vakil NH, Phillips KM (2013) Antibiotic-associated diarrhea: a refresher on causes and possible prevention with probiotics-continuing education article. J Pharm Pract 26(5):476–482

    Article  PubMed  Google Scholar 

  3. McDonald LC, Coignard B, Dubberke E, Song X, Horan T, Kutty PK, Ad Hoc Clostridium difficile Surveillance Working Group (2007) Recommendations for surveillance of Clostridium difficile–associated disease. Infect Control Hosp Epidemiol 28(2):140–145

    Article  PubMed  Google Scholar 

  4. Debast SB, Bauer MP, Kuijper EJ, Committee (2014) European society of clinical microbiology and infectious diseases : update of the treatment guidance document for Clostridium difficile infection. Clin Microbiol Infect 20(2):1–26

    Article  PubMed  CAS  Google Scholar 

  5. Bartlett JG (2002) Antibiotic-associated diarrhea. N Engl J Med 346(5):334–339

    Article  PubMed  Google Scholar 

  6. Asha NJ, Tompkins D, Wilcox MH (2006) Comparative analysis of prevalence, risk factors, and molecular epidemiology of antibiotic-associated diarrhea due to Clostridium difficile, Clostridium perfringens, and Staphylococcus aureus. J Clin Microbiol 44(8):2785–2791

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Bauer MP, Kuijper EJ, van Dissel JT, European Society of Clinical Microbiology and Infectious Diseases (2009) European society of clinical microbiology and infectious diseases (ESCMID): treatment guidance document for clostridium difficile infection (CDI). Clin Microbiol Infect 15(12):1067–1079

    Article  PubMed  CAS  Google Scholar 

  8. Kato H, Kato N, Watanabe K, Iwai N, Nakamura H, Yamamoto T, Suzuki K, Kim SM, Chong Y, Wasito EB (1998) Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol 36(8):2178–2182

    PubMed  CAS  PubMed Central  Google Scholar 

  9. Huang H, Weintraub A, Fang H, Wu S, Zhang Y, Nord CE (2010) Antimicrobial susceptibility and heteroresistance in Chinese Clostridium difficile strains. Anaerobe 16(6):633–635

    Article  PubMed  CAS  Google Scholar 

  10. Stabler RA, Dawson LF, Valiente E, Cairns MD, Martin MJ, Donahue EH, Riley TV, Songer JG, Kuijper EJ, Dingle KE, Wren BW (2012) Macro and micro diversity of Clostridium difficile isolates from diverse sources and geographical locations. PLoS ONE 7(3):e31559

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  11. Loo VG, Bourgault AM, Poirier L, Lamothe F, Michaud S, Turgeon N, Toye B, Beaudoin A, Frost EH, Gilca R, Brassard P, Dendukuri N, Béliveau C, Oughton M, Brukner I, Dascal A (2011) Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med 365(18):1693–1703

    Article  PubMed  CAS  Google Scholar 

  12. Rodríguez-Pardo D, Almirante B, Bartolomé RM, Pomar V, Mirelis B, Navarro F, Soriano A, Sorlí L, Martínez-Montauti J, Molins MT, Lung M, Vila J, Pahissa A, Barcelona Clostridium difficile Study Group (2013) Epidemiology of Clostridium difficile infection and risk factors for unfavorable clinical outcomes: results of a hospital-based study in Barcelona, Spain. J Clin Microbiol 51(5):1465–1473

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bergogne-Bérézin E (2000) Treatment and prevention of antibiotic associated diarrhea. Int J Antimicrob Agents 16(4):521–526

    Article  PubMed  Google Scholar 

  14. Wiström J, Norrby SR, Myhre EB, Eriksson S, Granström G, Lagergren L, Englund G, Nord CE, Svenungsson B (2001) Frequency of antibiotic-associated diarrhoea in 2462 antibiotic-treated hospitalized patients: a prospective study. J Antimicrob Chemother 47(1):43–50

    Article  PubMed  Google Scholar 

  15. Chen J, Guo X (2006) Clinical characteristics, control and prevention of antibiotic—associated diarrhea. World Chin J Digestol 14(9):927–929

    Google Scholar 

  16. Wang Y, Lin J (2008) Clinical analysis of antibiotic associated diarrhea. Chin J Health Lab Technol 18(7):1393–1394

    Google Scholar 

  17. Chen YB, Gu SL, Wei ZQ, Shen P, Kong HS, Yang Q, Li LJ (2014) Molecular epidemiology of Clostridium difficile in a tertiary hospital of China. J Med Microbiol 63(Pt 4):562–569

    Article  PubMed  Google Scholar 

  18. Hawkey PM, Marriott C, Liu WE, Jian ZJ, Gao Q, Ling TK, Chow V, So E, Chan R, Hardy K, Xu L, Manzoor S (2013) Molecular epidemiology of Clostridium difficile infection in a major Chinese hospital: an underrecognized problem in Asia? J Clin Microbiol 51(10):3308–3313

    Article  PubMed  PubMed Central  Google Scholar 

  19. Cote GA, Buchman AL (2006) Antibiotic-associated diarrhoea. Expert Opin Drug Saf 5(3):361–372

    Article  PubMed  CAS  Google Scholar 

  20. Hensgens MP, Goorhuis A, van Kinschot CM, Crobach MJ, Harmanus C, Kuijper EJ (2011) Clostridium difficile infection in an endemic setting in the Netherlands. Eur J Clin Microbiol Infect Dis 30(4):587–93

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  21. Vesteinsdottir I, Gudlaugsdottir S, Einarsdottir R, Kalaitzakis E, Sigurdardottir O, Bjornsson ES (2012) Risk factors for Clostridium difficile toxin-positive diarrhea: a population-based prospective case–control study. Eur J Clin Microbiol Infect Dis 31(10):2601–10

    Article  PubMed  CAS  Google Scholar 

  22. Huang H, Wu S, Wang M, Zhang Y, Fang H, Palmgren AC, Weintraub A, Nord CE (2008) Molecular and clinical characteristics of Clostridium difficile infection in a University Hospital in Shanghai, China. Clin Infect Dis 47(12):1606–1608

    Article  PubMed  Google Scholar 

  23. Surawicz CM, Brandt LJ, Binion DG, Ananthakrishnan AN, Curry SR, Gilligan PH, McFarland LV, Mellow M, Zuckerbraun BS (2013) Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 108(4):478–498

    Article  PubMed  CAS  Google Scholar 

  24. Tillhon M, Guaman Ortiz LM, Lombardi P, Scovassi AI (2012) Berberine: new perspectives for old remedies. Biochem Pharmacol 84(10):1260–1267

    Article  PubMed  CAS  Google Scholar 

  25. Zhang Y, Wang X, Liu L, Cai N, Li Q, Wu K (2010) The anti-diarrhea mechanisms of berberine in diarrhea disease. Shaanxi Med J 39(1):6–8

    Google Scholar 

  26. Chen CM, Chang HC (1995) Determination of berberine in plasma, urine and bile by high-performance liquid chromatography. J Chromatogr B Biomed Appl 665(1):117–123

    Article  PubMed  CAS  Google Scholar 

  27. He C, Gao P (2010) Meta-analysis of antibiotic-associated diarrhea treated by traditional Chinese medicine. Chin J TCM WM Crit Care 17(2):69–72

    Google Scholar 

  28. Shu Q, Peng S, Feng Y, Zhang Z, Xie Y, Zhou S (2013) The influences of Chinese herbal compounds on in vitro expression of toxic genes tcdA/tcdB of Clostridium difficile. Chin J Microecol 25(4):373–375, 380

    Google Scholar 

  29. Yan Q, Zhang J, Chen C, Zhou H, Du P, Cui Z, Cen R, Liu L, Li W, Cao B, Lu J, Cheng Y (2013) Multilocus sequence typing (MLST) analysis of 104 Clostridium difficile strains isolated from China. Epidemiol Infect 141(1):195–199

    Article  PubMed  CAS  Google Scholar 

  30. Wang P, Zhou Y, Wang Z, Xie S, Chen Y, Jiang B, Zhang T, Lin M, Li R, Tan J (2014) Identification of Clostridium difficile Ribotype 027 for the first time in mainland China. Infect Control Hosp Epidemiol 35(1):95–98

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the National Natural Science Foundation of China (no. 30973594 and no. 81101292) and Shanghai Pujiang Programme (no. 10PJ1401800). The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

Conflict of interest

None declared.

Author information

Authors and Affiliations

  1. Institute of Antibiotics, Huashan Hospital, Fudan University, Shanghai, 200040, China

    F. F. Zhou, S. Wu & H. H. Huang

  2. Global Disease Detection Branch, Division of Global Health Protection, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, GA, USA

    J. D. Klena

Authors
  1. F. F. Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. D. Klena
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. H. Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. H. Huang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, F.F., Wu, S., Klena, J.D. et al. Clinical characteristics of Clostridium difficile infection in hospitalized patients with antibiotic-associated diarrhea in a university hospital in China. Eur J Clin Microbiol Infect Dis 33, 1773–1779 (2014). https://doi.org/10.1007/s10096-014-2132-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-014-2132-9

Keywords

Search

Navigation