Advertisement

Regional differences in temporal incidence of Clostridium difficile infection: a systematic review and meta-analysis

Published:August 03, 2019DOI:https://doi.org/10.1016/j.ajic.2019.07.005

      Highlights

      • The global incidence of Clostridium difficile infection increased before 2004.
      • A downward trend was observed after 2004.
      • The incidences have stabilized in North America.
      • The incidences have increased significantly in Asia.

      Background

      Previous decades have witnessed a change in the epidemiology of Clostridium difficile infections. This study aimed to determine temporal trends in the incidence of C difficile infection across geographic regions.

      Methods

      An initial search of the relevant literature was conducted from date inception to October 2018 without language restriction. We estimated the pooled incidences using logit transformation, weighted by inverse variance. The Joinpoint Regression Analysis Program was used to explore its temporal trend.

      Results

      Globally, the estimated incidence of C difficile infection increased from 6.60 per 10,000 patient-days in 1997 to 13.8 per 10,000 patient-days in 2004. Thereafter, a significant downward trend was observed, at –8.75% annually until 2015. From 2005 to 2015, the incidences in most European countries decreased at a rate between 1.97% and 4.11% per annum, except in France, where an increasing incidence was observed (β = 0.16; P < .001). The incidences have stabilized in North America over the same period; however, in Asia, the incidence increased significantly from 2006 to 2014 (annualized percentage change = 14.4%; P < .001). The increase was greatest in Western Asian countries, including Turkey and Israel (β > 0.10; P < .004).

      Conclusions

      This study revealed rapid changes in the incidence of C difficile infection. This meta-analysis should inform the allocation of resources for controlling C difficile infection and future surveillance efforts in countries where epidemiologic information on C difficile infection remains sparse.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Infection Control
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Khanna S
        • Pardi DS
        • Aronson SL
        • Kammer PP
        • Baddour LM
        Outcomes in community-acquired Clostridium difficile infection.
        Alimentary Pharmacol Ther. 2012; 35: 613-618
        • van Kleef E
        • Green N
        • Goldenberg SD
        • Robotham JV
        • Cookson B
        • Jit M
        • et al.
        Excess length of say and mortality due to Clostridium difficile infection: a multi-state modelling approach.
        J Hosp Infect. 2014; 88: 213-217
        • Alfa MJ
        • Du T
        • Beda G
        Survey of incidence of Clostridium difficile infection in Canadian hospitals and diagnostic approaches.
        J Clin Microbiol. 1998; 36: 2076-2080
        • Hyland M
        • Ofner-Agostini M
        • Miller M
        • Paton S
        • Gourdeau M
        • Ishak M
        • et al.
        N-CDAD in Canada: results of the Canadian nosocomial infection surveillance program 1997 N-CDAD prevalence surveillance project.
        Can J Infect Dis. 2001; 12: 81-88
        • Laffan AM
        • Bellatoni MF
        • Greenough WB
        • Zenilman JM
        Burden of Clostridium difficile associated diarrhea in a long-term care facility.
        J Am Geriatr Soc. 2006; 54: 1063-1073
        • McDonald LC
        • Owings M
        • Jernigan DB
        Clostridium difficile infection in patients discharges from US short-stay hospitals, 1996-2003.
        Emerg Infect Dis. 2006; 12: 40915
        • Price MF
        • Dao-Tran T
        • Garey KW
        • Graham G
        • Gentry LO
        • Dhungana L
        • et al.
        Epidemiology and incidence of Clostridium difficile associated diarrhea diagnosed upon admission to a university hospital.
        J Hosp Infect. 2007; 65: 42-46
        • Lawrence SJ
        • Puzniak LA
        • Shadel BN
        • Gillespie KN
        • Kollef MH
        • Mundy LM
        • et al.
        Clostridium difficile in the intensive care unit: epidemiology, costs, and colonization pressure.
        Infect Control Hosp Epidemiol. 2007; 28: 123-130
        • Koh TH
        • Tan AL
        • Tan ML
        • Wang G
        • Song KP
        Epidemiology of Clostridium difficile infection in a large teaching hospital in Singapore.
        Pathology. 2007; 39: 438-442
        • 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: 825-834
        • Ma GK
        • Brensinger CM
        • Wu Q
        • Lewis JD
        Increasing incidence of multiply recurrent Clostridium difficile infection in the United States: a cohort study.
        Ann Intern Med. 2017; 167: 152-158
        • Gilca R
        • Hubert B
        • Fortin E
        • Gaulin C
        • Dionne M
        Epidemiological patterns and hospital characteristics associated with increased incidence of Clostridium difficile infection in Quebec, Canada, 1998-2006.
        Infect Control Hosp Epidemiol. 2010; 31: 939-947
        • Gupta A
        • Tariq R
        • Frank RD
        • Jean GW
        • Beg MS
        • Pardi DS
        • et al.
        Trends in the incidence and outcomes of hospitalized cancer patients with Clostridium difficile infection: a nationwide analysis.
        J Natl Compr Canc Netw. 2017; 15: 466-472
        • Kotila SM
        • Mentula S
        • Ollgren J
        • Virolainen-Julkunen A
        • Lyytikainen O
        Community- and healthcare-associated Clostridium difficile infections, Finland, 2008-2013.
        Emerg Infect Dis. 2016; 22: 1747-1753
        • Davies KA
        • Longshaw CM
        • Davis GL
        • Bouza E
        • Barbut F
        • Barna Z
        • et al.
        Underdiagnosis of Clostridium difficile across Europe: the European, multicentre, prospective, biannual, point-prevalence study of Clostridium difficile infection in hospitalized patients with diarrhea (EUCLID).
        Lancet Infect Dis. 2014; 14120819
        • Ho J
        • Dai RZW
        • Kwong TNY
        • Wang X
        • Zhang L
        • Ip M
        • et al.
        Disease burden of Clostridium difficile infections in adults, Hong Kong, China, 2006-2014.
        Emerg Infect Dis. 2017; 23: 1671-1679
        • Chung CH
        • Wu CJ
        • Lee HC
        • Yan JJ
        • Chang CM
        • Lee NY
        • et al.
        Clostridium difficile infection at a medical center in Southern Taiwan: incidence, clinical features, and prognosis.
        J Microbiol Immunol Infect. 2010; 43: 119-125
        • Han SH
        • Kim H
        • Lee K
        • Jeong SJ
        • Park KH
        • Song JY
        • et al.
        Epidemiology and clinical features of toxigenic culture-confirmed hospital-onset Clostridium difficile infection: a multicentre prospective study in tertiary hospitals of South Korea.
        J Med Microbiol. 2014; 63: 1542-1551
        • Dubberke ER
        • Butler AM
        • Yokoe DS
        • Mayer J
        • Hota B
        • Mangino JE
        • et al.
        Multicenter study of Clostridium difficile infection rates from 2000 to 2006.
        Infect Control Hosp Epidemiol. 2010; 31: 1030-1037
        • Moher D
        • Liberati A
        • Tetzlaff J
        • Altman DG
        • PRISMA Group
        Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
        PLoS Med. 2009; 6e10000097
      1. Wells GA, Shea B, O'Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of non-randomized studies in meta-analyses 2014. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed November 16, 2017.

      2. United Nations Statistics Division. Standard country or area codes for statistical use 2016.Available at: https://unstats.un.org/unsd/methodology/m49. Accessed November 16, 2017.

        • Wilson E
        Probable inference, the law of succession, and statistical inference.
        J Am Stat Assoc. 1927; 22: 209-212
        • Hunter JP
        • Saratzis A
        • Sutton AJ
        • Boucher RH
        • Sayers RD
        • Bown MJ
        In meta-analyses of proportion studies, funnel plots were found to be an inaccurate method of assessing publication bias.
        J Clin Epidemiol. 2014; 67: 897-903
        • Dingle KE
        • Didelot X
        • Quan TP
        • Eyre DW
        • Stoesser N
        • Golubchik T
        • et al.
        Effect of control inventions on Clostridium difficile infection in England: an observational study.
        Lancet Infect Dis. 2017; 17: 411-421
        • Hogberg LD
        • Muller A
        • Zorzet A
        • Monet DL
        • Cars O
        Antibiotic use worldwide.
        Lancet Infect Dis. 2014; 14: 1179-1180
        • Morgan DJ
        • Okeke IN
        • Laximarayan R
        • Perencevich EN
        • Scott W
        Non-prescription antimicrobial use worldwide: a systematic review.
        Lancet Infect Dis. 2011; 11: 692-701
        • Na'amnih W
        • Adler A
        • Miller-Roll T
        • Cohen D
        • Carmeli Y
        Incidence and risk factors for community and hospital acquisition of Clostridium difficile infection in the Tel Aviv Sourasky medical center.
        Infect Control Hosp Epidmiol. 2017; 38: 912-920
        • Low M
        • Nitzan O
        • Bitterman H
        • Cohen C
        • Hammerman A
        • Lieberman N
        • et al.
        Trends in outpatient antibiotic use in Israel during the years 2000-2010: setting targets for an intervention.
        Infection. 2013; 41: 401-407
        • ECDC
        Summary of the latest data on antibiotic consumption in the European Union. May 2018.
        European Centre for Disease Prevention and Control, Stockholm, Sweden2018
        • Wilcox MH
        • Chalmers JD
        • Nord CE
        • Freeman J
        • Bouza E
        Role of cephalosporins in the era of Clostridium difficile infection.
        J Antimicrob Chemother. 2017; 72: 118
        • Baur D
        • Galdstone BP
        • Burkert F
        • Carrara E
        • Foschi F
        • Dobele S
        • et al.
        Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis.
        Lancet Infect Dis. 2017; 179901001
        • Klein EY
        • van Boeckel TP
        • Martinez EM
        • Pant S
        • Gandra S
        • Levin SA
        • et al.
        Global increase and geographic convergence in antibiotic consumption between 2000 and 2015.
        Proc Natl Acad Sci USA. 2018; 115: E3463-E3470
        • You E
        • Song H
        • Cho J
        • Lee J
        Reduction in the incidence of hospital-acquired Clostridium difficile infection through infection control interventions other than the restriction of antimicrobial use.
        Int J Infect Dis. 2014; 22: 910
        • Barbut F
        • Richard A
        • Hamadi K
        • Chomette V
        • Burghoffer B
        • Pettit JC
        Epidemiology of recurrences or reinfections of Clostridium difficile associated diarrhea.
        J Clin Microbiol. 2000; 38: 2386-2388