Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-28T04:17:51.743Z Has data issue: false hasContentIssue false
  • English
  • Français

A Time-Series Analysis of Clostridium difficile and Its Seasonal Association with Influenza

Published online by Cambridge University Press:  02 January 2015

Philip M. Polgreen ,
Ming Yang ,
Lucas C. Bohnett  and
Joseph E. Cavanaugh
Philip M. Polgreen*
Affiliation:
Department of Internal Medicine, University of Iowa Carver College of Medicine, Iowa City, Iowa Department of Epidemiology, University of Iowa College of Public Health, Iowa City, Iowa
Ming Yang
Affiliation:
Department of Biostatistics, University of Iowa College of Public Health, Iowa City, Iowa
Lucas C. Bohnett
Affiliation:
Department of Biostatistics, University of Iowa College of Public Health, Iowa City, Iowa
Joseph E. Cavanaugh
Affiliation:
Department of Biostatistics, University of Iowa College of Public Health, Iowa City, Iowa
*
Division of Infectious Diseases, Department of Internal Medicine, University of Iowa, Carver College of Medicine, 200 Hawkins Drive, Iowa City, IA 52242 (philip-polgreen@uiowa.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective.

To characterize the temporal progression of the monthly incidence of Clostridium difficile infections (CDIs) and to determine whether the incidence of CDI is related to the incidence of seasonal influenza.

Design.

A retrospective study of patients in the Nationwide Inpatient Sample during the period from 1998 through 2005.

Methods.

We identified all hospitalizations with a primary or secondary diagnosis of CDI with use of International Classification of Diseases, 9th Revision, Clinical Modification codes, and we did the same for influenza. The incidence of CDI was modeled as an autoregression about a linear trend. To investigate the association of CDI with influenza, we compared national and regional CDI and influenza series data and calculated cross-correlation functions with data that had been prewhitened (filtered to remove temporal patterns common to both series). To estimate the burden of seasonal CDI, we developed a proportional measure of seasonal CDI.

Results.

Time-series analysis of the monthly number of CDI cases reveals a distinct positive linear trend and a clear pattern of seasonal variation (R2 = 0.98). The cross-correlation functions indicate that influenza activity precedes CDI activity on both a national and regional basis. The average burden of seasonal (ie, winter) CDI is 23%.

Conclusions.

The epidemiologic characteristics of CDI follow a pattern that is seasonal and associated with influenza, which is likely due to antimicrobial use during influenza seasons. Approximately 23% of average monthly CDI during the peak 3 winter months could be eliminated if CDI remained at summer levels.

Type
Original Articles
Information
Infection Control & Hospital Epidemiology , Volume 31 , Issue 4 , April 2010 , pp. 382 - 387
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Archibald, LK, Banerjee, SN, Jarvis, WR. Secular trends in hospital-acquired Clostridium difficile disease in the United States, 1987-2001. J Infect Dis 2004;189:1585–1589.Google Scholar
2. Pepin, J, Valiquette, L, Alary, ME, et al. Clostridium difficile-associated diarrhea in a region of Quebec from 1991-2003: a changing pattern of disease severity. CMAJ 2004;171:466–472.Google Scholar
3. McDonald, LC, Owings, M, Jernigan, DB. Clostridium difficile infections in patients discharged from US short-stay hospitals, 1996-2003. Emerg Infect Dis 2006;12:409–415.Google Scholar
4. Chandler, RE, Hedberg, K, Cieslak, PR. Clostridium difficile-associated disease in Oregon: increasing incidence and hospital-level risk factors. Infect Control Hosp Epidemiol 2007;28:116–122.Google Scholar
5. Elixhauser, A, Jhung, M. Clostridium difficile-associated disease in U.S. hospitals, 1993-2005. HCUP Statistical Brief 50, April 2008. Rockville, MD: Agency of Healthcare Research and Quality. http://www.hcup-us.ahrq.gov/reports/statbriefs/sb50.pdf. Accessed January 30, 2009.Google Scholar
6. McDonald, LC, Killgore, GE, Thompson, A, et al. An epidemic, toxin gene-variant strain of Clostridium difficile . N Engl J Med 2005;353:2433–2441.Google Scholar
7. McEllistrem, MC, Carman, RJ, Gerding, DN, Genheimer, CW, Zheng, L. A hospital outbreak of Clostridium difficile disease associated with isolates carrying binary toxin genes. Clin Infect Dis 2005;40:265–272.Google Scholar
8. Clabots, CR, Johnson, S, Olson, MM, Peterson, LR, Gerding, DN. Acquisition of Clostridium difficile by hospitalized Patients. J Infect Dis 1992;166:561–567.Google Scholar
9. Kaatz, GW, Gitlin, SD, Schaberg, DR, et al. Acquisition of Clostridium difficile from the hospital environment. Am J Epidemiol 1988;127:1289–1294.Google Scholar
10. Mayfield, JL, Leet, T, Miller, J, Mundy, LM. Environmental control to reduce transmission of Clostridium difficile . Clin Infect Dis 2000;31:995–1000.Google Scholar
11. McFarland, LV, Mulligan, MME, Kwok, RY, Stamm, WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320:204–210.Google Scholar
12. Dubberke, ER, Reske, KA, Yan, Y, Olsen, MA, McDonald, LC, Fraser, VJ. Clostridium difficile-associated disease in a setting of endemicity: identification of novel risk factors. Clin Infect Dis 2007;45:1543–1549.Google Scholar
13. Settle, CD, Wilcox, MH, Fawley, WN, Corrado, OJ, Hawley, PM. Prospective study of the risk of Clostridium difficile diarrhoea in elderly patients following treatment with cefotaxime or piperacillin-tazobactam. Aliment Pharmacol Ther 1998;12:1217–1223.Google Scholar
14. Kyne, L, Sougioultzis, S, McFarland, LV, Kelly, CP. Underlying disease severity as a major risk factor for nosocomial Clostridium difficile diarrhea. Infect Control Hosp Epidemiol 2002;23:653–659.Google Scholar
15. Gaynes, R, Rimland, D, Killum, E, et al. Outbreak of Clostridium difficile infection in a long-term care facility: association with gatifloxacin use. Clin Infect Dis 2004;38:640–645.Google Scholar
16. Pépin, J, Saheb, N, Coulombe, MA, et al. Emergence of fluoroquinolones as the predominant risk factor for Clostridium difficile-associated diarrhea: a cohort study during an epidemic in Quebec. Clin Infect Dis 2005;41:1254–1260.Google Scholar
17. Loo, VG, Poirier, L, Miller, MA, et al. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality (published correction appears in N Engl J Med 2006;354:2200). N Engl J Med 2005;353:2442-2449.Google Scholar
18. Elseviers, MM, Ferech, M, Vander Stichele, RH, Goossens, H; ESAC project group. Antibiotic use in ambulatory care in Europe (ESAC data 19972002): trends, regional differences and seasonal fluctuations. Pharma-coepidemiol Drug Saf 2007;16:115–123.Google Scholar
19. Goossens, H, Ferech, M, Vander Stichele, R, Elseviers, M; ESAC Project Group. Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet 2005;365:579–587.Google Scholar
20. Low, D. Reducing antibiotic use in influenza: challenges and rewards. Clin Microbiol Infect 2008;14:298–306.Google Scholar
21. Agency for Healthcare Research and Quality. HCUP NIS database documentation healthcare cost and utilization project (HCUP). Rockville, MD: Agency for Healthcare Research and Quality; October 2009. http://www.hcup-us.ahrq.gov/db/nation/nis/nisdbdocumentation.jsp. Accessed January 30, 2009.Google Scholar
22. Agency for Healthcare Research and Quality. Nationwide Inpatient Sample Trends Supplemental (NIS-Trends) Files. Rockville, MD: Agency for Healthcare Research and Quality; May 2008. http://www.hcup-us.ahrq.gov/db/nation/nis/nistrends.jsp. Accessed January 30, 2009.Google Scholar
23. Jagai, J, Naumova, E. Clostridium difficile-associated disease in the elderly, United States. Emerg Infect Dis 2009;15(2:343–344.Google Scholar
24. Thompson, WW, Shay, DK, Weintraub, E, et al. Influenza-associated hospitalizations in the United States. JAMA 2004;292(11:1333–1340.CrossRefGoogle ScholarPubMed
25. Collins, SD. Excess mortality from causes other than influenza and pneumonia during influenza epidemics. Public Health Rep 1932;47:2159–2179.Google Scholar
26. Reichert, TA, Simonsen, L, Sharma, A, Pardo, SA, Fedson, DS, Miller, MA. Influenza and the winter increase in mortality in the United States, 19591999. Am J Epidemiol 2004;160(5:492–502.Google Scholar
27. Nichol, KL, Nordin, J, Mullooly, J, Lask, R, Fillbrandt, K, Iwane, M. Influenza vaccination and reduction in hospitalizations for cardiac disease and stroke among the elderly. N Engl J Med 2003;348:1322–1332.Google Scholar
28. Spodick, DH, Flessas, AP, Johnson, MM. Association of acute respiratory symptoms with onset of acute myocardial infarction: prospective investigation of 150 consecutive patients and matched control Patients. Am J Cardiol 1984;53:481–482.Google Scholar
29. Mattila, KJ. Viral and bacterial infections in patients with acute myocardial infarction. J Intern Med 1989;225:293–296.CrossRefGoogle ScholarPubMed
30. Meier, CR, Jick, SS, Derby, LE, Vasilakis, C, Jick, H. Acute respiratory-tract infections and risk of first-time acute myocardial infarction. Lancet 1998;351:1467–1471.Google Scholar
31. Neuzil, KM, Mellen, BG, Wright, PF, Mitchel, EF Jr, Griffin, MR. The effect of influenza on hospitalizations, outpatient visits, and courses of antibiotics in children. N Engl J Med 2000;342:225–231.Google Scholar
32. Falsey, AR, Murata, Y, Walsh, EE. Impact of rapid diagnosis on management of adults hospitalized with influenza. Arch Intern Med 2007;167: 354–360.Google Scholar
33. Dubberke, ER, Reske, KA, McDonald, LC, Fraser, VJ. ICD-9 codes and surveillance for Clostridium difficile-associated disease. Emerg Infect Dis 2006;12:1576–1579.Google Scholar
34. Marsden-Haug, N, Foster, VB, Gould, PL, Elbert, E, Wang, H, Pavlin, JA. Code-based syndromic surveillance for influenzalike illness by International Classification of Diseases, Ninth Revision. Erne rglnfect Dis 2007;13:207–216.Google Scholar
35. Ansari, SA, Springthorpe, VS, Sattar, SA. Survival and vehicular spread of human rotaviruses: possible relation to seasonality of outbreaks. Rev Infect Dis 1991;13(3:448–461.CrossRefGoogle ScholarPubMed
36. Levy, K, Hubbard, AE, Eisenberg, JN. Seasonality of rotavirus disease in the tropics: a systematic review and meta-analysis. Int J Epidemiol 2009;38:1487.CrossRefGoogle ScholarPubMed
37. Shaman, J, Kohn, M. Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad SciUSA 2009;106(9:3243–3248.Google Scholar
38. Rodriguez-Palacios, A, Reid-Smith, RJ, Staempfli, HR, et al. Possible seasonality of Clostridium difficile in retail meat, Canada. Emerg Infect Dis 2009;15(5:802–805.Google Scholar
39. 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;34:346–353.Google Scholar
40. Dubberke, ER, Reske, KA, Olsen, MA, McDonald, LC, Fraser, VJ. Short-and long-term attributable costs of Clostridium difficile-associated disease in nonsurgical in Patients. Clin Infect Dis 2008;46:497–504.Google Scholar
41. O'Brien, JA, 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;28:1219–1227.Google Scholar
42. Abell, S, Chapman, S, Nadin, L, Warren, R. Seasonal variation in fluoroquinolone prescribing. J Antimicrob Chemother 1999;43:315–316.Google Scholar
43. Starr, JM, Rogers, TR, Impallomeni, M. Hospital-acquired Clostridium difficile diarrhoea and herd immunity. Lancet 1997;349:426–428.Google Scholar
44. Dubberke, ER, Reske, KA, Olsen, MA, et al. Evaluation of Clostridium difficile-associated disease pressure as a risk factor for C difficile-associated disease. Arch Intern Med 2007;167(10:1092–1097.CrossRefGoogle ScholarPubMed
45. Musher, DM, Aslam, S, Logan, N, et al. Relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clin Infect Dis 2005;40:1586–1590.Google Scholar
46. Pepin, J, Alary, ME, Valiquette, L, et al. Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Clin Infect Dis 2005;40:1591–1597.Google Scholar