Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-18T16:20:43.770Z Has data issue: false hasContentIssue false

Multihospital Outbreak of Clostridium difficile Ribotype 027 Infection: Epidemiology and Analysis of Control Measures

Published online by Cambridge University Press:  02 January 2015

Mamoon A. Aldeyab*
Affiliation:
Clinical and Practice Research Group, School of Pharmacy, Queen's University Belfast, Belfast, Northern Ireland, United Kingdom
Michael J. Devine
Affiliation:
Northern Health and Social Services Board (currently Public Health Agency), County Hall, Ballymena, Northern Ireland, United Kingdom
Peter Flanagan
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Michael Mannion
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Avril Craig
Affiliation:
Northern Health and Social Services Board (currently Public Health Agency), County Hall, Ballymena, Northern Ireland, United Kingdom
Michael G. Scott
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Stephan Harbarth
Affiliation:
Infection Control Program, University of Geneva Hospitals and Medical School, Geneva, Switzerland
Nathalie Vernaz
Affiliation:
Pharmacy Department, University of Geneva Hospitals and Medical School, Geneva, Switzerland
Elizabeth Davies
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Jon S. Brazier
Affiliation:
Anaerobe Reference Laboratory, Public Health Wales, Microbiology Cardiff, University Hospital of Wales, Cardiff, United Kingdom
Brian Smyth
Affiliation:
Health Protection Agency Communicable Disease Surveillance Centre (Northern Ireland) (currently Public Health Agency), Belfast, Northern Ireland, United Kingdom
James C. McElnay
Affiliation:
Clinical and Practice Research Group, School of Pharmacy, Queen's University Belfast, Belfast, Northern Ireland, United Kingdom
Brendan F. Gilmore
Affiliation:
Biomaterials and Drug Delivery Group, School of Pharmacy, Queen's University Belfast, Belfast, Northern Ireland, United Kingdom
Geraldine Conlon
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Fidelma A. Magee
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Feras W. Darwish Elhajji
Affiliation:
Clinical and Practice Research Group, School of Pharmacy, Queen's University Belfast, Belfast, Northern Ireland, United Kingdom
Shaunagh Small
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Collette Edwards
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Chris Funston
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
Mary P. Kearney
Affiliation:
Northern Health and Social Care Trust, Ballymena, Northern Ireland, United Kingdom
*
Clinical and Practice Research Group, School of Pharmacy, Queen's University Belfast, Belfast BT9 7BL, United Kingdom (maldeyab02@qub.ac.uk)

Abstract

Objective.

To report a large outbreak of Clostridium difficile infection (CDI; ribotype 027) between June 2007 and August 2008, describe infection control measures, and evaluate the impact of restricting the use of fluoroquinolones in controlling the outbreak.

Design.

Outbreak investigation in 3 acute care hospitals of the Northern Health and Social Care Trust in Northern Ireland.

Interventions.

Implementation of a series of CDI control measures that targeted high-risk antibiotic agents (ie, restriction of fluoroquinolones), infection control practices, and environmental hygiene.

Results.

A total of 318 cases of CDI were identified during the outbreak, which was the result of the interaction between C. difficile ribotype 027 being introduced into the affected hospitals for the first time and other predisposing risk factors (ranging from host factors to suboptimal compliance with antibiotic guidelines and infection control policies). The 30-day all-cause mortality rate was 24.5%; however, CDI was the attributable cause of death for only 2.5% of the infected patients. Time series analysis showed that restricting the use of fluoroquinolones was associated with a significant reduction in the incidence of CDI (coefficient, —0.054; lag time, 4 months; P = .003).

Conclusion.

These findings provide additional evidence to support the value of antimicrobial stewardship as an essential element of multifaceted interventions to control CDI outbreaks. The present CDI outbreak was ended following the implementation of an action plan improving communication, antibiotic stewardship, infection control practices, environmental hygiene, and surveillance.

Type
Original Article
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2011

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.Thompson, I. Clostridium difficile-associated disease: update and focus on non-antibiotic strategies. Age Ageing 2008;37:1418.Google Scholar
2.Kuijper, EJ, Barbut, F, Brazier, JS, et al.Update of Clostridium difficile infection due to PCR ribotype 027 in Europe, 2008. Eurosurveillance 2008;13(31)pii: 18942.Google Scholar
3.McFarland, LV. Update on the changing epidemiology of Clostridium difficile-associated disease. Nat Clin Pract Gastroenterol Hepatol 2008;5:4048.Google Scholar
4.Labbé, A-C, Poirier, L, MacCannell, D, et al.Clostridium difficile infections in a Canadian tertiary care hospital before and during a regional epidemic associated with the BI/NAP1/027 strain. Antimicrob Agents Chemother 2008;52:31803187.Google Scholar
5.Warny, M, Pepin, J, Fang, A, et al.Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 2005;366:10791084.Google Scholar
6.Debast, SB, Vaessen, N, Choudry, A, Wiegers-Ligtvoet, EA, van den Berg, RJ, Kuijper, EJ. Successful combat of an outbreak due to Clostridium difficile PCR ribotype 027 and recognition of specific risk factors. Clin Microbiol Infect 2009;15:427434.Google Scholar
7.MacCannell, DR, Louie, TJ, Gregson, DB, et al.Molecular analysis of Clostridium difficile PCR ribotype 027 isolates from eastern and western Canada. J Clin Microbiol 2006;44:21472152.Google Scholar
8.Long, S, Fenelon, L, Fitzgerald, S, et al.First isolation and report of clusters of Clostridium difficile PCR 027 cases in Ireland. Eurosurveillance 2007;12(17):pii = 3183.Google Scholar
9.Aldeyab, MA, Monnet, DL, López-Lozano, JM, et al.Modelling the impact of antibiotic use and infection control practices on the incidence of hospital-acquired methicillin-resistant Staphylococcus aureus: a time-series analysis. J Antimicrob Chemother 2008;62:593600.CrossRefGoogle ScholarPubMed
10.Harris, AD, Shardell, M, El-Kamary, SS, Furano, JP, Miller, RR, Perencevich, EN. Statistical analysis and application of quasi experiments to antimicrobial resistance intervention studies. Clin Infect Dis 2007;45:901907.Google Scholar
11.Aldeyab, MA, Harbarth, S, Vernaz, N, et al.Quasiexperimental study of the effects of antibiotic use, gastric acid-suppressive agents, and infection control practices on the incidence of Clostridium difficile-associated diarrhea in hospitalized patients. Antimicrob Agents Chemother 2009;53:20822088.Google Scholar
12.O'Neill, GL, Ogunsola, FT, Brazier, JS, Duerden, BI. Modification of a PCR ribotyping method for application as a routine typing scheme for Clostridium difficile. Anaerobe 1996;2:205209.Google Scholar
13.Stubbs, SLJ, Brazier, JS, O'Neill, GL, Duerden, BI. PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J Clin Microbiol 1999;37:461463.Google Scholar
14.Lewis, SJ, Heaton, KW. Stool form scale as a useful guide to intestinal transit time. Scand J Gastroenterol 1997;32:920924.Google Scholar
15.McDonald, LC, Coignard, B, Dubberke, E, et al., and the Ad Hoc Clostridium difficile Surveillance Working Group. Recommendations for surveillance of Clostridium difficile-associated disease. Infect Control Hosp Epidemiol 2007;28:140145.Google Scholar
16.WHO Collaborating Center for Drug Statistics Methodology. Guidelines for ATC classifications and DDD assignment. Oslo: WHO Collaborating Center; 2002.Google Scholar
17.Department of Health (United Kingdom). 2007. High Impact Intervention No 7: care bundle to reduce the risk from Clostridium difficile. http://www.dh.gov.uk/prod_consum_dh/groups/dh_digitalassets/@dh/@en/documents/digitalasset/dh_078126.pdf. Accessed January 30, 2010.Google Scholar
18.Department of Health Social Services and Public Safety (United Kingdom). Guidance on Death, Stillbirth and Cremation Certification. http://www.dhsspsni.gov.uk/show_publications?txtid = 32940. Accessed January 30, 2010.Google Scholar
19.Helfenstein, U. Box-Jenkins modelling in medical research. Stat Methods Med Res 1996;5:322.Google Scholar
20.Tobacman, JK. Assessment of comorbidity: a review. Clin Perform Quoi Health Care 1994;2:2332.Google Scholar
21.Stone, SP, Cooper, BS, Kibbler, CC, et al.The ORION statement: guidelines for transparent reporting of outbreak reports and intervention studies of nosocomial infection. Lancet Infect Dis 2007;7:282288.Google Scholar
22.Schwaber, MJ, Simhon, A, Block, C, Rovai, V, Ferderber, N, Shapiro, M. Factors associated with nosocomial diarrhea and Clostridium difficile-associated disease on the adult wards of an urban tertiary care hospital. Eur J Clin Microbiol Infect Dis 2000;19:915.Google Scholar
23.Muto, CA, Pokrywka, M, Shutt, K, et al.A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol 2005;26:273280.CrossRefGoogle Scholar
24.Baxter, R, Ray, GT, Fireman, BH. Case-control study of antibiotic use and subsequent Clostridium difficile-associated diarrhea in hospitalized patients. Infect Control Hosp Epidemiol 2008;29:4450.Google Scholar
25.Owens, RC Jr, Donskey, CJ, Gaynes, RP, Loo, VG, Muto, CA. Antimicrobial-associated risk factors for Clostridium difficile infection. Clin Infect Dis 2008;46(suppl 1):S19S31.Google Scholar
26.Akhtar, AJ, Shaheen, M. Increasing incidence of Clostridium difficile-associated diarrhea in African-American and Hispanic patients: association with the use of proton pump inhibitor therapy. J Natl Med Assoc 2007;99:500504.Google ScholarPubMed
27.Cadle, RM, Mansouri, MD, Logan, N, Kudva, DR, Musher, DM. Association of proton-pump inhibitors with outcomes in Clostridium difficile colitis. Am J Health Syst Pharm 2007;64:23592363.Google Scholar
28.Dial, S, Delaney, JA, Barkun, AN, Suissa, S. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA 2005;294:29892995.Google Scholar
29.Apisarnthanarak, A, Zack, JE, Mayfield, JL, et al.Effectiveness of environmental and infection control programs to reduce transmission of Clostridium difficile. Clin Infect Dis 2004;39:601602.Google Scholar
30.Regulation and Quality Improvement Authority (United Kingdom). Clostridium difficile—RQIA Independent Review. Review of the Outbreak of Clostridium difficile in the Northern Health and Social Care Trust, http://www.dhsspsni.gov.uk/assemblydocumentcdiffl4108.pdf. Accessed July 1, 2010.Google Scholar
31.Aldeyab, MA, Elshibly, SM, McElnay, JC, et al.An evaluation of compliance with an antibiotic policy in surgical wards at a general teaching hospital in Northern Ireland. Infect Control Hosp Epidemiol 2009;30:921922.Google Scholar
32.Kuijper, EJ, Coignard, B, Tüll, P, ESCMID Study Group for Clostridium difficile, EU Member States, European Centre for Disease Prevention and Control. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 2006;12(suppl 6):218.Google Scholar
33.Morgan, OW, Rodrigues, B, Elston, T, et al.Clinical severity of Clostridium difficile PCR ribotype 027: a case-case study. PLoS one 2008;3(3):e1812.Google Scholar
34.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;353:24422449.Google Scholar
35.Hubert, B, Loo, VG, Bourgault, A-M, et al.A portrait of the geographic dissemination of the Clostridium difficile North American pulsed-field type 1 strain and the epidemiology of C. difficile-associated disease in Quebec. Clin Infect Dis 2007;44:238244.Google Scholar
36.Barbut, F, Gariazzo, B, Bonné, L, et al.Clinical features of Clostridium difficile-associated infections and molecular characterization of strains: results of a retrospective study, 2000-2004. Infect Control Hosp Epidemiol 2007;28:131139.Google Scholar
37.Goorhuis, A, Van der Kooi, T, Vaessen, N, et al.Spread and epidemiology of Clostridium difficile polymerase chain reaction ribotype 027/toxinotype III in The Netherlands. Clin Infect Dis 2007;45:695703.Google Scholar
38.Miller, M, Gravel, D, Mulvey, M, et al.Health care-associated Clostridium diffidi infection in Canada: patient age and infecting strain type are highly predictive of severe outcome and mortality. Clin Infect Dis 2010;50:194201.Google Scholar
39.Kallen, AJ, Thompson, A, Ristaino, P, et al.Complete restriction of fluoroquinolone use to control an outbreak of Clostridium difficile infection at a community hospital. Infect Control Hosp Epidemiol 2009;30:264272.CrossRefGoogle Scholar
40.McElnay, JC, Scott, MG, Sidara, JY, Kearney, P. Audit of antibiotic usage in medium-sized general hospital over an 11-year period: the impact of antibiotic policies. Pharm World Sci 1995;17:207213.Google Scholar
41.Al-Eidan, FA, McElnay, JC, Scott, MG, Kearney, MP. Clostridium difficile-associated diarrhoea in hospitalised patients. J Clin Pharm Ther 2000;25:101109.Google Scholar
42.Valiquette, L, Cossette, B, Garant M-P, Diab, H, Pépin, J. Impact of a reduction in the use of high-risk antibiotics on the course of an epidemic of Clostridium difficile-associated disease caused by the hypervirulent NAP1/027 strain. Clin Infect Dis 2007;45(suppl 2):S112S121.Google Scholar
43.Vonberg, RP, Kuijper, EJ, Wilcox, MH, et al.Infection control measures to limit the spread of Clostridium difficile. Clin Microbiol Infect 2008;14(suppl 5):220.Google Scholar