Skip to main content

Attributable Burden of Hospital-Onset Clostridium difficile Infection: A Propensity Score Matching Study

  • Ying P. Tabak (a1), Marya D. Zilberberg (a2), Richard S. Johannes (a1) (a3), Xiaowu Sun (a1) and L. Clifford McDonald (a4)...

To determine the attributable in-hospital mortality, length of stay (LOS), and cost of hospital-onset Clostridium difficile infection (HO-CDI).


Propensity score matching.


Six Pennsylvania hospitals (2 academic centers, 1 community teaching facility, and 3 community nonteaching facilities) contributing data to a clinical research database.


Adult inpatients between 2007 and 2008.


We defined HO-CDI in adult inpatients as a positive C. difficile toxin assay result from a specimen collected more than 48 hours after admission and more than 8 weeks following any previous positive result. We developed an HO-CDI propensity model and matched cases with noncases by propensity score at a 1 : 3 ratio. We further restricted matching within the same hospital, within the same principal disease group, and within a similar length of lead time from admission to onset of HO-CDI.


Among 77,257 discharges, 282 HO-CDI cases were identified. The propensity score-matched rate was 90%. Compared with matched noncases, HO-CDI patients had higher mortality (11.8% vs 7.3%; P<.05), longer LOS (median [interquartile range (IQR)], 12 [9–21] vs 11 [8–17] days; P< .01), and higher cost (median [IQR], $20,804 [$ll,059-$38,429] vs $16,634 [$9,413–$30,319]; P< .01). The attributable effect of HO-CDI was 4.5% (95% confidence interval [CI], 0.2%–8.7%; P<.05) for mortality, 2.3 days (95% CI, 0.9–3.8; P<.01) for LOS, and $6,117 (95% CI, $1,659–$10,574; P<.01) for cost.


Patients with HO-CDI incur additional attributable mortality, LOS, and cost burden compared with patients with similar primary clinical condition, exposure risk, lead time of hospitalization, and baseline characteristics.

Corresponding author
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, 1600 Clifton Road, MS A07, Atlanta, GA 30333 (
Hide All
1.Klevens RM, Edwards IR, Richards CL Jret al.Estimating health care–associated infections and deaths in U.S. hospitals, 2002. Public Health Rep 2007;122(2):160166.
2.Roberts RR, Scott RD IIHota B, et al.Costs attributable to healthcare-acquired infection in hospitalized adults and a comparison of economic methods. Med Care 2010;48(11):10261035.
3.Lucado J, Gould C, Elixhauser A. Clostridium difficile infections (CDI) in hospital stays, 2009. Statistical brief 124. Rockville, MD: Healthcare Cost and Utilization Project Statistical Briefs, 2012.
4.Dubberke ER, Wertheimer AI. Review of current literature on the economic burden of Clostridium difficile infection. Infect Control Hosp Epidemiol 2009;30(1):5766.
5.Kyne L, Hamel MB, Polavaram R, Kelly CP. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis 2002;34(3):346353.
6.Dubberke ER, Butler AM, Reske KA, et al.Attributable outcomes of endemic Clostridium difficile–associated disease in nonsurgical patients. Emerg Infect Dis 2008;14(7):10311038.
7.Dubberke ER, Reske KA, Olsen MA, McDonald LC, Fraser VJ. Short- and long-term attributable costs of Clostridium difficile–associated disease in nonsurgical inpatients. Clin Infect Dis 2008;46(4):497504.
8.O'Brien IA, Lahue BJ, Caro JJ, Davidson DM. The emerging infectious challenge of Clostridium difficile–associated disease in Massachusetts hospitals: clinical and economic consequences. Infect Control Hosp Epidemiol 2007;28(11):12191227.
9.Miller M, Gravel D, Mulvey M, et al.Health care–associated Clostridium difficile infection in Canada: patient age and infecting strain type are highly predictive of severe outcome and mortality. Clin Infect Dis 2010;50(2):194201.
10.Lawrence SJ, Puzniak LA, Shadel BN, Gillespie KN, Kollef MH, Mundy LM. Clostridium difficile in the intensive care unit: epidemiology, costs, and colonization pressure. Infect Control Hosp Epidemiol 2007;28(2):123130.
11.Kilgore ML, Ghosh K, Beavers CM, Wong DY, Hymel PA JrBrossette SE. The costs of nosocomial infections. Med Care 2008;46(1):101104.
12.Zilberberg MD, Tabak YP, Sievert DM, et al.Using electronic health information to risk-stratify rates of Clostridium difficile infection in US hospitals. Infect Control Hosp Epidemiol 2011;32(7):649655.
13.Tabak YP, Johannes RS, Silber JH. Using automated clinical data for risk adjustment: development and validation of six disease-specific mortality predictive models for pay-for-performance. Med Care 2007;45(8):789805.
14.Tabak YP, Sun X, Derby KG, Kurtz SG, Johannes RS. Development and validation of a disease-specific risk adjustment system using automated clinical data. Health Serv Res 2010;45:18151835.
15. Acute inpatient PPS. Centers for Medicare and Medicaid Services website. Accessed November 7, 2011.
16.Parsons LS, ed. Reducing bias in a propensity score matched-pair sample using greedy matching techniques. In: Proceedings of the 26th Annual SAS Users Group International Conference. Long Beach, CA: SAS Institute, 2001.
17.Austin PC. Comparing paired vs non-paired statistical methods of analyses when making inferences about absolute risk reductions in propensity-score matched samples. Stat Med 2011;30(11):12921301.
18.Rothman KJ, Greenland S, Lash TL. Modern Epidemiology. 3rd ed. Philadelphia: Lippincott-Wolters-Kluwer, 2008.
19.Sato T. On the variance estimator for the Mantel-Haenszel risk difference. Biometrics 1989;45:13231324.
20.Sullivan LM, Dukes KA, Losina E. Tutorial in biostatistics: an introduction to hierarchical linear modelling. Stat Med 1999;18(7):855888.
21.Efron B, Tibshirani R. An Introduction to the Bootstrap. London: Chapman & Hall, 1993.
22.Dubberke ER, Butler AM, Yokoe DS, et al.Multicenter study of surveillance for hospital-onset Clostridium difficile infection by the use of ICD-9-CM diagnosis codes. Infect Control Hosp Epidemiol 2010;31(3):262268.
23.Dallal RM, Harbrecht BG, Boujoukas AJ, et al.Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg 2002;235(3):363372.
24.Miller MA, Hyland M, Ofner-Agostini M, Gourdeau M, Ishak M. Morbidity, mortality, and healthcare burden of nosocomial Clostridium difficile–associated diarrhea in Canadian hospitals. Infect Control Hosp Epidemiol 2002;23(3):137140.
25.Loo VG, Poirier L, Miller MA, et al.A predominantly clonal multi-institutional outbreak of Clostridium difficile–associated diarrhea with high morbidity and mortality. N Engl J Med 2005;353(23):24422449.
26.Pepin J, Valiquette L, Cossette B. Mortality attributable to nosocomial Clostridium difficile–associated disease during an epidemic caused by a hypervirulent strain in Quebec. CMAJ 2005;173(9):10371042.
27.Forster AJ, Taljaard M, Oake N, Wilson K, Roth V, van Walraven C. The effect of hospital-acquired infection with Clostridium difficile on length of stay in hospital. CMAJ 2012;184(1):3742.
28.Cohen SH, Gerding DN, Johnson S, et al.Clinical practice guide-lines 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(5):431455.
29.Centers for Disease Control and Prevention. Vital signs: preventing Clostridium difficile infections. MMWR Morb Mortal Wkly Rep 2012;61(9):157162.
30.Centers for Medicare and Medicaid Services. Medicare program; hospital inpatient prospective payment systems for acute care hospitals and the long-term care hospital prospective payment system and FY 2012 rates; hospitals' FTE resident caps for graduate medical education payment. Final rules. Fed Regist 2011;76(160):5147651843.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Infection Control & Hospital Epidemiology
  • ISSN: 0899-823X
  • EISSN: 1559-6834
  • URL: /core/journals/infection-control-and-hospital-epidemiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 53 *
Loading metrics...

Abstract views

Total abstract views: 269 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 17th January 2018. This data will be updated every 24 hours.