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Utilization of Health Services Among Adults With Recurrent Clostridium difficile Infection: A 12-Year Population-Based Study

  • Jennifer L. Kuntz (a1), Jennifer M. Baker (a2), Patricia Kipnis (a2), Sherian Xu Li (a2), Vincent Liu (a2), Yang Xie (a3), Stephen Marcella (a3) and Gabriel J. Escobar (a2)...



Considerable efforts have been dedicated to developing strategies to prevent and treat recurrent Clostridium difficile infection (rCDI); however, evidence of the impact of rCDI on patient healthcare utilization and outcomes is limited.


To compare healthcare utilization and 1-year mortality among adults who had rCDI, nonrecurrent CDI, or no CDI.


We performed a nested case-control study among adult Kaiser Foundation Health Plan members from September 1, 2001, through December 31, 2013. We identified CDI through the presence of a positive laboratory test result and divided patients into 3 groups: patients with rCDI, defined as CDI in the 14–57 days after initial CDI; patients with nonrecurrent CDI; and patients who never had CDI. We conducted 3 matched comparisons: (1) rCDI vs no CDI; (2) rCDI vs nonrecurrent CDI; (3) nonrecurrent CDI vs no CDI. We followed patients for 1 year and compared healthcare utilization between groups, after matching patients on age, sex, and comorbidity.


We found that patients with rCDI consistently have substantially higher levels of healthcare utilization in various settings and greater 1-year mortality risk than both patients who had nonrecurrent CDI and patients who never had CDI.


Patients who develop an initial CDI are generally characterized by excess underlying, severe illness and utilization. However, patients with rCDI experience even greater adverse consequences of their disease than patients who do not experience rCDI. Our results further support the need for continued emphasis on identifying and using novel approaches to prevent and treat rCDI.

Infect Control Hosp Epidemiol. 2016;1–8


Corresponding author

Address correspondence to Gabriel J. Escobar, MD, Kaiser Permanente Division of Research, 2000 Broadway Ave, 032 R01, Oakland, CA 94612 (


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Presented in part: The European Congress of Clinical Microbiology and Infectious Diseases; Barcelona, Spain; May 10–13, 2014; and the Interscience Conference on Antimicrobial Agents and Chemotherapy; Washington, DC; September 5–9, 2014.



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1. Vardakas, KZ, Polyzos, KA, Patouni, K, Rafailidis, PI, Samonis, G, Falagas, ME. Treatment failure and recurrence of Clostridium difficile infection following treatment with vancomycin or metronidazole: a systematic review of the evidence. Int J Antimicrob Agents 2012;40:18.
2. Garey, KW, Sethi, S, Yadav, Y, DuPont, HL. Meta-analysis to assess risk factors for recurrent Clostridium difficile infection. Journal Hosp Infect 2008;70:298304.
3. Johnson, S. Recurrent Clostridium difficile infection: a review of risk factors, treatments, and outcomes. J Infect 2009;58:403410.
4. McFarland, LV, Surawicz, CM, Rubin, M, Fekety, R, Elmer, GW, Greenberg, RN. Recurrent Clostridium difficile disease: epidemiology and clinical characteristics. Infect Control Hospl Epidemiol 1999;20:4350.
5. Kelly, CP. Can we identify patients at high risk of recurrent Clostridium difficile infection? Clin Microbiol Infect 2012;18:2127.
6. Shields, K, Araujo-Castillo, RV, Theethira, TG, Alonso, CD, Kelly, CP. Recurrent Clostridium difficile infection: from colonization to cure. Anaerobe 2015;34:5973.
7. Youngster, I, Russell, GH, Pindar, C, Ziv-Baran, T, Sauk, J, Hohmann, EL. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA 2014:7.
8. Lowy, I, Molrine, DC, Leav, BA, et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N Engl J Med 2010;362:197205.
9. Bagdasarian, N, Rao, K, Malani, PN. Diagnosis and treatment of Clostridium difficile in adults: a systematic review. JAMA 2015;313:10.
10. Selby, JV. Linking automated databases for research in managed care settings. Ann Intern Med 1997;127:719724.
11. Escobar, G, Greene, J, Scheirer, P, Gardner, M, Draper, D, Kipnis, P. Risk adjusting hospital inpatient mortality using automated inpatient, outpatient, and laboratory databases. Med Care 2008;46:232239.
12. Liu, V, Kipnis, P, Gould, MK, Escobar, GJ. Length of stay predictions: improvements through the use of automated laboratory and comorbidity variables. Med Care 2010;48:739744.
13. Escobar, GJ, Greene, JD, Gardner, MN, Marelich, GP, Quick, B, Kipnis, P. Intra-hospital transfers to a higher level of care: contribution to total hospital and intensive care unit (ICU) mortality and length of stay (LOS). J Hosp Med 2011;6:7480.
14. Liu, V, Kipnis, P, Rizk, NW, Escobar, GJ. Adverse outcomes associated with delayed intensive care unit transfers in an integrated healthcare system. J Hosp Med 2012;7:224230.
15. McDonald, LC, Coignard, B, Dubberke, E, Song, X, Horan, T, Kutty, PK. Recommendations for surveillance of Clostridium difficile-associated disease. Infect Control Hosp Epidemiol 2007;28:140145.
16. Musher, DM, Aslam, S, Logan, N, et al. Relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clin Infect Dis 2005;40:15861590.
17. Ellis, RP, Ash, A. Refinements to the diagnostic cost group (DCG) model. Inquiry 1995;32:418429.
18. Ash, AS, Ellis, RP, Pope, GC, et al. Using diagnoses to describe populations and predict costs. HCF Review 2000;21:728.
19. Diagnostic Cost Groups. Models and methodologies guide. Published 2002. Accessed November 16, 2006.
20. Diagnostic Cost Groups. Published 2006. Accessed November 17, 2006.
21. van Walraven, C, Escobar, GJ, Greene, JD, Forster, AJ. The Kaiser Permanente inpatient risk adjustment methodology was valid in an external patient population. J Clin Epidemiol 2010;63:798803.
22. Rosenbaum, PR. Observational Studies. 2nd ed. New York: Springer-Verlag; 2002.
23. Kosanke, J, Bergstralh, EJ. vmatch: Match cases to controls using variable optimal matching. Replaces OPTIMAL matching option from %MATCH macro. In: Mayo Clinic Division of Biomedical Statistics and Informatics, ed: Mayo Clinic; 2004.
24. Ziegler, A. Generalized Estimating Equations. Vol. 204. New York: Springer Science & Business Media; 2011.
25. Zou, G. A modified Poisson regression approach to prospective studies with binary data. Am J Epidemiol 2004;159:702706.
26. Zimlichman, E, Henderson, D, Tamir, O, et al. Health care-associated infections: a meta-analysis of costs and financial impact on the US health care system. JAMA Intern Med 2013;173:20392046.
27. Kuntz, JL, Johnson, ES, Raebel, MA, et al. Epidemiology and healthcare costs of incident Clostridium difficile infections identified in the outpatient healthcare setting. Infect Control Hospl Epidemiol 2012;33:10311038.
28. Ghantoji, SS, Sail, K, Lairson, DR, DuPont, HL, Garey, KW. Economic healthcare costs of Clostridium difficile infection: a systematic review. J Hosp Infect 2010;74:309318.
29. Gabriel, L, Beriot-Mathiot, A. Hospitalization stay and costs attributable to Clostridium difficile infection: a critical review. J Hosp Infect 2014;88:1221.
30. Shah, DN, Aitken, SL, Barragan, LF, et al. Economic burden of primary compared with recurrent Clostridium difficile infection in hospitalized patients: a prospective cohort study. J Hosp Infect 2016;93:286289.
31. Aitken, SL, Joseph, TB, Shah, DN, et al. Healthcare resource utilization for recurrent Clostridium difficile infection in a large university hospital in Houston, Texas. PLOS ONE 2014;9:e102848.
32. Olsen, MA, Yan, Y, Reske, KA, Zilberberg, MD, Dubberke, ER. Recurrent Clostridium difficile infection is associated with increased mortality. Clin Microbiol Infect 2015;21:164170.
33. Olsen, MA, Yan, Y, Reske, KA, Zilberberg, M, Dubberke, ER. Impact of Clostridium difficile recurrence on hospital readmissions. Am J Infect Control 2015;43:318322.
34. Barbut, F, Richard, A, Hamadi, K, Chomette, V, Burghoffer, B, Petit, JC. Epidemiology of recurrences or reinfections of Clostridium difficile-associated diarrhea. J Clin Microbiol 2000;38:23862388.
35. McFarland, LV, Elmer, GW, Surawicz, CM. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol 2002;97:17691775.
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Utilization of Health Services Among Adults With Recurrent Clostridium difficile Infection: A 12-Year Population-Based Study

  • Jennifer L. Kuntz (a1), Jennifer M. Baker (a2), Patricia Kipnis (a2), Sherian Xu Li (a2), Vincent Liu (a2), Yang Xie (a3), Stephen Marcella (a3) and Gabriel J. Escobar (a2)...


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