Early identification and control of carbapenemase-producing ...

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b University of South Florida, College of Medicine, Tampa General Hospital, ... of Infection Prevention and Control, H. Lee Moffitt Cancer Center, Tampa, FL.
American Journal of Infection Control 41 (2013) 562-4

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American Journal of Infection Control

American Journal of Infection Control

journal homepage: www.ajicjournal.org

Brief report

Early identification and control of carbapenemase-producing Klebsiella pneumoniae, originating from contaminated endoscopic equipment Sally F. Alrabaa MD a, *, Phuong Nguyen MD b, Roger Sanderson MA, BSN c, Aliyah Baluch MD d, Ramon L. Sandin MD, MS, FCAP, ABP-MM e, Danashree Kelker MD b, Chaitanya Karlapalem MBBS e, Peggy Thompson RN, BSN, CIC f, Kay Sams RN, BSN, CIC, CCRN g, Stacy Martin RN, BSN, CIC g, Jose Montero MD a, John N. Greene MD h a

Department of Infectious Diseases and International Medicine, University of South Florida, College of Medicine, Tampa, FL University of South Florida, College of Medicine, Tampa General Hospital, Tampa, FL c Florida Department of Health, Tampa General Hospital, Tampa, FL d Division of Infectious Diseases and Tropical Medicine, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL e Department of Infectious Diseases, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL f Department of Infection Prevention and Control, Tampa General Hospital, Tampa, FL g Department of Infection Prevention and Control, H. Lee Moffitt Cancer Center, Tampa, FL h Division of Infectious Diseases and Tropical Medicine, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL b

Key Words: Iatrogenic transmission Endoscopic retrograde cholangiopancreatography ERCP Source identification Outbreak prevention

Klebsiella producing carbapenemase is an emerging pathogen. We report transmission of this organism by contaminated endoscopic instruments. Quick identification of source, staff education, contact precautions, and emphasis on hand and environmental hygiene led to case control and prevention of outbreak. Copyright Ó 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.

Outbreaks of carbapenem-resistant Klebsiella (CRKP) in the United States and worldwide are increasingly recognized.1-3 Infections with CRKP carry high mortality.4 We describe the first 7 cases of CRKP strains in 2 tertiary hospitals in patients who had endoscopic procedures at a third facility and we identify the cause. METHODS Hospital A is a 206-bed cancer center, and hospital B is a 988-bed tertiary hospital. Between June 2008 and January 2009, the first 3 patients with CRKP were identified in hospital A and the first 4 cases in hospital B. Both hospitals receive patients transferred from other facilities. Carbapenem resistance was not previously seen at either hospital. The regional epidemiologist with Department of Health was notified, and an investigation to determine the source was initiated. Infection control team performed active surveillance by rectal swabs of all patients in units where CRKP was identified. Positive cultures were confirmed with Hodge test. Records of the 7 cases * Address correspondence to Sally F. Alrabaa, MD, Tampa General Hospital, 1 Tampa General Circle, Room G, Tampa, FL 33606. E-mail address: [email protected] (S.F. Alrabaa). Conflicts of interest: None to report.

were reviewed. Data collected included diagnosis, transferring facility, procedures done before and after admission, response to treatment, and final outcomes. Positive cultures in the blood, urine, or sputum for Klebsiella pneumoniae or other gram-negative bacteria with reduced susceptibility to carbapenems was considered a case. Pneumonia, urinary tract infection, and bloodstream infection were defined per Centers for Disease Control and Prevention guidelines. Antibiotic susceptibilities were determined in accordance with the National Committee for Clinical Laboratory Standards (NCCLS) using the Vitek AMS system. RESULTS Seven cases of CRKP were identified. Infection sites included blood, bile, and urine. Admission diagnoses included pancreatic cancer, gallbladder cancer, liver mass, and chronic pancreatitis. All 7 patients had endoscopic retrograde cholangiopancreatography (ERCP) at the same endoscopy center within the prior 60 days (Table 1). All 7 CRKP isolates were resistant to imipenem, 5 were susceptible to tigecyline, and 4 were susceptible to aminoglycosides. Two patients received intravenous colistin, and both developed renal failure requiring hemodialysis. Four patients received

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S.F. Alrabaa et al. / American Journal of Infection Control 41 (2013) 562-4

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Table 1 Data on patients positive for carbapenemase producing Klebsiella isolates at 2 tertiary centers between July 2008 and January 2009

Patient Age/sex 1 2 3 4 5 6 7

73 M 62 F 59 M 78 F 81 M 82 M 83 M

Diagnosis

Procedure within prior 60 days

Pancreatic cancer Pancreatic cancer Gallbladder cancer Panceratitis Gallbladder cancer Liver mass Gallbladder cancer

ERCP ERCP/stent ERCP/cholecystectomy ERCP/EGD ERCP ERCP ERCP

Procedure performed at Endoscopy Endoscopy Endoscopy Endoscopy Endoscopy Endoscopy Endoscopy

facility facility facility facility facility facility facility

Patient transferred to tertiary center C C C C C C C

A A A B B B B

Site of infection

Treatment received

Blood Colistin Blood Colistin Urine Tigecycline Blood Tigecycline þ Biliary fluid Tigecycline þ Blood Tigecycline þ Blood Tigecycline þ

Outcome

Alive to hospice Alive Alive gentamicin Alive to nursing home meropenem Expired amikacin Alive amikacin Alive to hospice

ERCP, Endoscopic retrograde cholangiopancreatography; F, female; M, male.

tygecyline and aminogycoside. One patient died during hospitalization (Table 1). Intervention Infection control measures Strict contact precautions and enhanced environmental cleaning were performed. Health care personnel were reminded to practice optimal hand hygiene and required to wear disposable gowns and gloves when caring for these patients. Flags indicating the presence of a multidrug-resistant organism were placed in the electronic medical record and chart. Source identification and control All 7 patients had endoscopic procedures at the same endoscopic center (facility C) within the prior 60 days with a median of 35 days prior to onset of infection. This suggested an epidemiologic link. The endoscopy center frequently receives patients from another local hospital, hospital X. Endoscopy center and hospital X were contacted by Department of Health, and breaches in infection control were investigated. Because all identified patients received ERCP in facility C, ERCP practices and procedures, including reprocessing procedures, were examined. Hospital X did not isolate patients with gram-negative multidrug-resistant organisms. Also, an inadequate ERCP cleaning technique was identified at the endoscopy center. The ERCP scope is particularly hard to clean because the tip of the scope consists of a small tube with a complex design including a small mobile metal piece called the elevator. Adherence with manufacturers’ instruction to clean this piece was not adequately followed. Biodebris remained under the elevator piece of the implicated scope after it was presumably cleaned. Samples obtained from this elevator area cultured carbapenemaseproducing Escherichia coli. Forty-six of 51 patients who underwent ERCP procedures from January 2008 to January 2009 at this facility were invited for screening, and an additional 3 patients colonized with carbapenamse-producing organisms were identified. There was no evidence of other bloodborne pathogen transmission. The facility received instruction on correct cleaning and handling of ERCP scope including manual scrubbing of the elevator part of the scope using a brush, prior to standard processing common to all scopes (Fig 1). They were also instructed to screen and isolate patients with multidrug-resistant organisms as recommended by Centers for Disease Control and Prevention. Postintervention assessment All subsequent transfers from endoscopy facility C and hospital X were placed in contact isolation until screening was done. All gramnegative bacteria testing positive for b-lactamase production were screened for carbapenem resistance, and appropriate infection control was immediately instituted. No outbreaks of carbapenemresistant organisms occurred at tertiary hospitals A and B.

Fig 1. Terminal part of ERCP scope. The small channel under elevator piece needs to be manually cleaned using a brush prior to standard ERCP processing.

DISCUSSION CRKP outbreaks mostly occurred in intensive care units and chronic care facilities.1 Transmission of carbapenem-resistant genes among bacterial species existing in same environment contributes to spread of resistance.5 Infection control and antibiotic stewardship remain our main defenses to limit propagation. Treatment is difficult, and the only therapeutic options currently are colistin and tigecycline. Bratu et al reported in vitro susceptibility of CRKP isolates to tigecycline and polymixin B and synergy between polymixin B and rifampin.6 We report early identification and control of CRKP at 2 tertiary hospitals epidemiologically linked to gastrointestinal procedures at an endoscopy center. Reports of outbreaks of Klebsiella pneumoniae have been associated with various sources including sinks,7 ultrasonography gel,8 intravenous saline solution,9 and bath soap.10 This is the first report of contaminated endoscopic instrument as the source of transmission of CRKP. This resulted from inadequate cleaning of the complex terminal part of the ERCP scope that contains the scope elevator. This part of the scope needs additional manual cleaning using a brush prior to standard scope processing. Overlooking this step result in biodebris remaining under the elevator that can harbor dangerous microorganisms resulting in iatrogenic transmissions between patients. References 1. Nadkarni AS, Schliep T, Khan L. Cluster of bloodstream infections caused by KPC-2 carbapenemase-producing Klebsiella pneumoniae in Manhattan. Am J Infect Control 2009;37:121-6. 2. Bratu S, Mooty M, Nichani S, Landman D, Gullans C, Pettinato B, et al. Emergence of KPC-possessing Klebsiella pneumoniae in Brooklyn, New York: epidemiology and recommendations for detection. Antimicrob Agents Chemother 2005;49:3018-20. 3. Wiener J, Quinn J, Bradford P, Goering R, Nathan C, Bush K, et al. Multiple antibiotic-resistant Klebsiella and Escherichia coli in nursing homes. JAMA 1999; 281:517-23. 4. Patel G, Huprikar S, Factor SH, Jenkins SG, Calfee DP. Outcomes of carbapenemresistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol 2008;29:1099-106. 5. Medeiros AA. Evolution and dissemination of b-lactamases accelerated by generations of b-lactam antibiotics. Clin Infect Dis 1997;24:S19-45.

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b-lactamase, originating from a contaminated ultrasonography coupling gel. J Clin Microbiol 1998;36:1357-60. 9. Goetz AM, Rihs JD, Chow JW, Singh N, Muder R. An outbreak of infusion-related Klebsiella pneumoniae bacteremia in a liver transplantation unit. Clin Infect Dis 1995;21:1501-3. 10. Szabo D, Filetoth Z, Szentandrassy J, Nemedi M, Toth E, Jeney C, et al. Molecular epidemiology of a cluster of cases due to Klebsiella pneumoniae producing SHV-5 extended-spectrum b-lactamase in the premature intensive care unit of a Hungarian hospital. J Clin Microbiol 1999;37:4167-9.