Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 23, Number 10—October 2017

Disease Burden of Clostridium difficile Infections in Adults, Hong Kong, China, 2006–2014

Jeffery Ho1, Rudin Z.W. Dai1, Thomas N.Y. Kwong, Xiansong Wang, Lin Zhang, Margaret Ip, Raphael Chan, Peter M.K. Hawkey, Kelvin L.Y. Lam, Martin C.S. Wong, Gary Tse, Matthew T.V. Chan, Francis K.L. Chan, Jun Yu, Siew C. Ng, Nelson Lee, Justin C.Y. Wu, Joseph J.Y. Sung, William K.K. WuComments to Author , and Sunny H. WongComments to Author 
Author affiliations: Chinese University of Hong Kong, Hong Kong, China (J. Ho, R.Z.W. Dai, T.N.Y. Kwong, X. Wang, L. Zhang, M. Ip, R. Chan, K.L.Y. Lam, M.C.S. Wong, G. Tse, M.T.V. Chan, F.K.L. Chan, J. Yu, S.C. Ng, N. Lee, J.C.Y. Wu, J.J.Y. Sung, W.K.K. Wu, S.H. Wong); Health Protection Agency, Birmingham, UK (P.M.K. Hawkey); University of Birmingham, Birmingham (P.M.K. Hawkey)

Main Article

Table 4

Cox proportional hazard regression analysis of potential independent variables associated with time to recurrence of Clostridium difficile infections, Hong Kong, China, 2006–2014*

Variable Univariate analysis
Multivariate analysis
β Hazard ratio (95% CI) p value β Adjusted hazard ratio (95% CI) p value
Age, y
<44 NA 1.0 NA NA 1.0 NA
45−64 0.14 1.15 (0.86–1.55) 0.34 0.01 1.00 (0.74–1.36) 0.99
65−84 0.29 1.33 (0.01–1.75) 0.04 0.04 1.04 (0.78–1.38) 0.81
>85 0.41 1.50 (1.14–1.98) <0.01 0.16 1.17 (0.87–1.56) 0.29
Male sex −0.02 0.99 (0.88–1.10) 0.79 NA NA NA
Resident of home for elderly persons −0.02 0.98 (0.87–1.11) 0.99 NA NA NA
Severe disease† 0.32 1.38 (1.22–1.55) <0.01 0.35 1.41 (1.26–1.59) <0.01
Antimicrobial drug use‡
High-risk drug 0.49 1.55 (1.36–1.77) <0.01 0.32 1.37 (1.20–1.57) <0.01
Medium-risk drug 0.41 1.51 (1.33–1.72) 0.01 −0.01 0.99 (0.86–1.16) 0.96
Low-risk drug 0.11 1.12 (0.69–1.83) 0.66 NA NA NA
Diagnostic test
Bacterial culture NA 1.0 NA NA 1.0 NA
Toxin detection 0.69 1.89 (1.62–2.21) 0.01 0.57 1.79 (1.53–2.11) <0.01
NAAT 0.27 1.31 (1.12–1.52) 0.01 0.23 1.26 (1.08–1.47) <0.01
Use of proton-pump inhibitor 0.08 1.09 (0.97–1.22) 0.16 NA NA NA
Use of histamine-2 receptor antagonist 0.18 1.19 (1.07–1.34) 0.01 0.09 1.09 (0.97–1.22) 0.15
Healthcare-associated disease 0.49 1.65 (1.15–2.35) 0.01 0.42 1.52 (1.06–2.20) 0.02
Concurrent condition
Myocardial infarction 0.09 1.10 (0.92–1.32) 0.32 NA NA NA
Cerebrovascular disease 0.49 1.63 (1.46–1.82) <0.01 −0.15 0.86 (0.74–0.99) 0.04
Chronic lung disease −0.05 0.95 (0.82–1.12) 0.56 NA NA NA
Diabetes mellitus 0.08 1.08 (0.94–1.24) 0.30 NA NA NA
Renal disease 0.05 1.05 (0.92–1.20) 0.47 NA NA NA
Nonmetastatic tumor −0.24 0.79 (0.69–0.90) 0.01 −0.15 0.86 (0.74–0.99) 0.04
AIDS −0.58 0.56 (0.18–1.74) 0.32 NA NA NA
Inflammatory bowel disease 0.14 1.15 (0.62–2.14) 0.66 NA NA NA

*NA, not applicable; NAAT, nucleic acid amplification test.
†Severe disease was diagnosed according to the according to criteria of Cohen et al (13).
‡Antimicrobial drug use 8 weeks before diagnosis was stratified into high risk (floroquinolones, cephalosporins, and clindamycin); medium risk (penicillins, macrolides, and sulfonamides); and low risk (tetracyclines).

Main Article

  1. Lessa  FC, Mu  Y, Bamberg  WM, Beldavs  ZG, Dumyati  GK, Dunn  JR, et al. Burden of Clostridium difficile infection in the United States. N Engl J Med. 2015;372:82534. DOIPubMed
  2. Kotila  SM, Mentula  S, Ollgren  J, Virolainen-Julkunen  A, Lyytikäinen  O. Community- and healthcare-associated Clostridium difficile infections, Finland, 2008–2013. Emerg Infect Dis. 2016;22:174753. DOIPubMed
  3. Levy  AR, Szabo  SM, Lozano-Ortega  G, Lloyd-Smith  E, Leung  V, Lawrence  R, et al. Incidence and costs of Clostridium difficile infections in Canada. Open Forum Infect Dis. 2015;2:ofv076. DOIPubMed
  4. Dingle  KE, Didelot  X, Quan  TP, Eyre  DW, Stoesser  N, Golubchik  T, et al.; Modernising Medical Microbiology Informatics Group. Effects of control interventions on Clostridium difficile infection in England: an observational study. Lancet Infect Dis. 2017;17:41121. DOIPubMed
  5. Kim  YS, Han  DS, Kim  YH, Kim  WH, Kim  JS, Kim  HS, et al. Incidence and clinical features of Clostridium difficile infection in Korea: a nationwide study. Epidemiol Infect. 2013;141:18994. DOIPubMed
  6. Reveles  KR, Lee  GC, Boyd  NK, Frei  CR. The rise in Clostridium difficile infection incidence among hospitalized adults in the United States: 2001-2010. Am J Infect Control. 2014;42:102832. DOIPubMed
  7. Slimings  C, Armstrong  P, Beckingham  WD, Bull  AL, Hall  L, Kennedy  KJ, et al. Increasing incidence of Clostridium difficile infection, Australia, 2011-2012. Med J Aust. 2014;200:2726. DOIPubMed
  8. Lübbert  C, Zimmermann  L, Borchert  J, Hörner  B, Mutters  R, Rodloff  AC. Epidemiology and recurrence rates of Clostridium difficile infections in Germany: a secondary data analysis. Infect Dis Ther. 2016;5:54554. DOIPubMed
  9. Chitnis  AS, Holzbauer  SM, Belflower  RM, Winston  LG, Bamberg  WM, Lyons  C, et al. Epidemiology of community-associated Clostridium difficile infection, 2009 through 2011. JAMA Intern Med. 2013;173:135967. DOIPubMed
  10. Chan  EW, Lau  WC, Leung  WK, Mok  MT, He  Y, Tong  TS, et al. Prevention of dabigatran-related gastrointestinal bleeding with gastroprotective agents: a population-based study. Gastroenterology. 2015;149:58695.e3. DOIPubMed
  11. Ng  SC, Leung  WK, Shi  HY, Li  MK, Leung  CM, Ng  CK, et al. Epidemiology of inflammatory bowel disease from 1981 to 2014: results from a territory-wide population-based registry in Hong Kong. Inflamm Bowel Dis. 2016;22:195460. DOIPubMed
  12. Chiu  SS, Lau  YL, Chan  KH, Wong  WH, Peiris  JS. Influenza-related hospitalizations among children in Hong Kong. N Engl J Med. 2002;347:2097103. DOIPubMed
  13. Cohen  SH, Gerding  DN, Johnson  S, Kelly  CP, Loo  VG, McDonald  LC, et al.; Society for Healthcare Epidemiology of America; Infectious Diseases Society of America. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31:43155. DOIPubMed
  14. Brown  KA, Khanafer  N, Daneman  N, Fisman  DN. Meta-analysis of antibiotics and the risk of community-associated Clostridium difficile infection. Antimicrob Agents Chemother. 2013;57:232632. DOIPubMed
  15. Slimings  C, Riley  TV. Antibiotics and hospital-acquired Clostridium difficile infection: update of systematic review and meta-analysis. J Antimicrob Chemother. 2014;69:88191. DOIPubMed
  16. Tsang  JK, Tsang  OT, Yao  R, Lai  S. The Antimicrobal Stewardship Programme: where have we been...where are we going? World Hosp Health Serv. 2013;49:1821.PubMed
  17. Loo  VG, Bourgault  AM, Poirier  L, Lamothe  F, Michaud  S, Turgeon  N, et al. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med. 2011;365:1693703. DOIPubMed
  18. United Nations Department of Economic and Social Affairs/Population Division. World Population Prospects: the 2015 revision, key findings, and advance tables. New York: The Department; 2015.
  19. Census and Statistics Department of Hong Kong Special Administrative Region. Hong Kong population projections, 2012 [cited 2017 Jul 20].
  20. Tsai  CS, Hung  YP, Lee  JC, Lee  NY, Chen  PL, Syue  LS, et al. Community-onset Clostridium difficile infection at a tertiary medical center in southern Taiwan, 2007-2015. J Microbiol Immunol Infect. 2016;•••:S16841182.PubMed
  21. Bloomfield  LE, Riley  TV. Epidemiology and risk factors for community-associated Clostridium difficile infection: a narrative review. Infect Dis Ther. 2016;5:23151. DOIPubMed
  22. Cheng  VCC, Yam  WC, Lam  OTC, Tsang  JL, Tse  EY, Siu  GK, et al. Clostridium difficile isolates with increased sporulation: emergence of PCR ribotype 002 in Hong Kong. Eur J Clin Microbiol Infect Dis. 2011;30:137181. DOIPubMed
  23. Dauby  N, Libois  A, Van Broeck  J, Delmée  M, Vandenberg  O, Martiny  D. Fatal community-acquired ribotype 002 Clostridium difficile bacteremia. Anaerobe. 2017;44:12. DOIPubMed
  24. McGlone  SM, Bailey  RR, Zimmer  SM, Popovich  MJ, Tian  Y, Ufberg  P, et al. The economic burden of Clostridium difficile. Clin Microbiol Infect. 2012;18:2829. DOIPubMed
  25. Gupta  A, Khanna  S. Community-acquired Clostridium difficile infection: an increasing public health threat. Infect Drug Resist. 2014;7:6372.PubMed
  26. Songer  JG, Trinh  HT, Killgore  GE, Thompson  AD, McDonald  LC, Limbago  BM. Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis. 2009;15:81921. DOIPubMed
  27. Weese  JS, Avery  BP, Rousseau  J, Reid-Smith  RJ. Detection and enumeration of Clostridium difficile spores in retail beef and pork. Appl Environ Microbiol. 2009;75:500911. DOIPubMed
  28. Ho  J, O’Donoghue  MM, Boost  MV. Occupational exposure to raw meat: a newly-recognized risk factor for Staphylococcus aureus nasal colonization amongst food handlers. Int J Hyg Environ Health. 2014;217:34753. DOIPubMed
  29. Riggs  MM, Sethi  AK, Zabarsky  TF, Eckstein  EC, Jump  RL, Donskey  CJ. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents. Clin Infect Dis. 2007;45:9928. DOIPubMed
  30. Schlackow  I, Walker  AS, Dingle  K, Griffiths  D, Oakley  S, Finney  J, et al. Surveillance of infection severity: a registry study of laboratory diagnosed Clostridium difficile. PLoS Med. 2012;9:e1001279. DOIPubMed
  31. Abou Chakra  CN, Pepin  J, Sirard  S, Valiquette  L. Risk factors for recurrence, complications and mortality in Clostridium difficile infection: a systematic review. PLoS One. 2014;9:e98400. DOIPubMed
  32. Brown  K, Valenta  K, Fisman  D, Simor  A, Daneman  N. Hospital ward antibiotic prescribing and the risks of Clostridium difficile infection. JAMA Intern Med. 2015;175:62633. DOIPubMed
  33. Zuo  T, Wong  SH, Lam  K, Lui  R, Cheung  K, Tang  W, et al. Bacteriophage transfer during faecal microbiota transplantation in Clostridium difficile infection is associated with treatment outcome. Gut. 2017 May 24;pii: gutjnl 017–313952.
  34. Choi  HY, Park  SY, Kim  YA, Yoon  TY, Choi  JM, Choe  BK, et al. The epidemiology and economic burden of Clostridium difficile infection in Korea. Biomed Res Int. 2015;2015:510386. .DOI
  35. Putsathit  P, Kiratisin  P, Ngamwongsatit  P, Riley  TV. Clostridium difficile infection in Thailand. Int J Antimicrob Agents. 2015;45:17. DOIPubMed

Main Article

1These authors contributed equally to this article.

Page created: September 18, 2017
Page updated: September 18, 2017
Page reviewed: September 18, 2017
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.