Hostname: page-component-6898cfcb55-kwdml Total loading time: 0 Render date: 2026-11-11T10:24:28.311Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification and control of two outbreaks of unrelated New Delhi metallo-β-lactamase–producing carbapenem-resistant Escherichia coli traced to the same endoscope defect

Published online by Cambridge University Press:  23 February 2023

Halima K. Dabaja-YounisOpen the ORCID record for Halima K. Dabaja-Younis[Opens in a new window],
Vered SchechnerOpen the ORCID record for Vered Schechner[Opens in a new window],
Ibrahim FiranOpen the ORCID record for Ibrahim Firan[Opens in a new window],
Iyad Khamaysi,
Gabrielle D. Levi,
Mor N. Lurie-WeinbergerOpen the ORCID record for Mor N. Lurie-Weinberger[Opens in a new window],
Avi WeissmanOpen the ORCID record for Avi Weissman[Opens in a new window],
Yuri Guriel,
Yuval Geffen and
Khetam HusseinOpen the ORCID record for Khetam Hussein[Opens in a new window]
Halima K. Dabaja-Younis
Affiliation:
Infection Control and Prevention Unit, Rambam Health Care Campus, Haifa, IsraelThe Ruth & Bruce Rappaport Faculty of Medicine, Technion–Israel Institute of Technology, Haifa, Israel
Vered Schechner
Affiliation:
National Institute for Antibiotic Resistance and Infection Control, Ministry of Health, Tel Aviv, IsraelSackler Faculty of Medicine, Tel Aviv University, Israel
Ibrahim Firan
Affiliation:
Infection Control and Prevention Unit, Rambam Health Care Campus, Haifa, Israel
Iyad Khamaysi
Affiliation:
The Ruth & Bruce Rappaport Faculty of Medicine, Technion–Israel Institute of Technology, Haifa, IsraelGastroenterology Unit, Rambam Health Care Campus, Haifa, Israel
Gabrielle D. Levi
Affiliation:
National Institute for Antibiotic Resistance and Infection Control, Ministry of Health, Tel Aviv, Israel
Mor N. Lurie-Weinberger
Affiliation:
National Institute for Antibiotic Resistance and Infection Control, Ministry of Health, Tel Aviv, Israel
Avi Weissman
Affiliation:
The Ruth & Bruce Rappaport Faculty of Medicine, Technion–Israel Institute of Technology, Haifa, IsraelHospital Management, Rambam Health Care Campus, Haifa, Israel
Yuri Guriel
Affiliation:
Gastroenterology Unit, Rambam Health Care Campus, Haifa, Israel
Yuval Geffen
Affiliation:
The Ruth & Bruce Rappaport Faculty of Medicine, Technion–Israel Institute of Technology, Haifa, IsraelMicrobiology Laboratory, Rambam Health Care Campus, Haifa, Israel
Khetam Hussein*
Affiliation:
Infection Control and Prevention Unit, Rambam Health Care Campus, Haifa, IsraelThe Ruth & Bruce Rappaport Faculty of Medicine, Technion–Israel Institute of Technology, Haifa, Israel
*
Author for correspondence: Dr. Khetam Hussein, Infectious Control and Prevention Unit Rambam Health Care Campus, PO Box 9602, Haifa 31096, Israel. E-mail: k_hussein@rambam.health.gov.il
Rights & Permissions [Opens in a new window]

Abstract

We report 2 outbreaks of genetically unrelated carbapenem-resistant New Delhi metallo-β-lactamase–producing Escherichia coli caused by contaminated duodenoscopes. Using endoscopes with disposable end caps, adherence to the manufacturer’s reprocessing instructions, routine audits, and manufacturer evaluation are critical in preventing such outbreaks.

Information

Type
Concise Communication
Information
Infection Control & Hospital Epidemiology , Volume 44 , Issue 10 , October 2023, pp. 1673 - 1675
Check for updates
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

Endoscopic retrograde cholangiopancreatography (ERCP) is a widely used procedure. Bacteremia or infection are a known complication of ERCP. Reference Anderson, Shimpi and McDonald1 The rate of ERCP-related infections is 15.2%. Reference Larsen, Russell and Ockert2 Duodenoscopes contain many small functional parts, so proper reprocessing and disinfection is essential to prevent endoscope-related infections. Reference Beilenhoff, Biering and Blum3,Reference Guideline Task Force, Petersen and Cohen4 However, several outbreaks of multidrug-resistant organisms (MDROs) have been reported after ERCP even though the manufacturers’ reprocessing instructions were strictly followed. Reference Epstein, Hunter and Arwady5,Reference Humphries, Yang and Kim6

We describe 2 ERCP-related outbreaks of carbapenem-resistant New Delhi metallo-β-lactamase (NDM)–producing Escherichia coli that occurred 7 months apart at Rambam Health Care Campus (RHCC), a 1,000-bed, university-affiliated hospital in Haifa, northern Israel. Approximately 500 patients undergo ERCP at RHCC each year. At the time of the outbreaks, 2 types of duodenoscopes were in use: TJF-Q190V (with disposable end cap) and TJF-Q180V (with fixed end cap). Carbapenem-resistant Enterobacteriaceae screening guidelines at RHCC are listed in Supplementary Table 1 (online).

First outbreak

On day 1 and day 3, E. coli NDM was detected in 2 patients hospitalized at the surgical department during routine surveillance. Remarkably, E. coli NDM was extremely rare in our hospital, so the infection prevention and control (IPAC) staff initiated an epidemiological investigation, which revealed that both patients had undergone ERCP procedures in our hospital 1 week earlier.

On day 18, a third patient was admitted to the hospital with septic shock secondary to E. coli NDM 3 days after ERCP. The 3 cases raised immediate concern that the infections were related to recent ERCP procedures.

Second outbreak

On day 214, 7 months later, a rectal screening of a 2-year-old patient performed after transfer from the pediatric intensive care unit yielded a positive result for E. coli-NDM. A rapid investigation revealed that he had undergone an ERCP procedure 3 days earlier (day 211). Also, 8 days earlier (day 203), a known carrier of E. coli-NDM (index case 2) had been treated with the same endoscope (endoscope 2-TJF-Q180V, serial no. 2507365) (Table 1).

Table 1.

Patients Positive for Carbapenem-Resistant Enterobacteriaceae, NDM β-Lactamase

Note. NDM, New Delhi metallo; ERCP, endoscopic retrograde cholangiopancreatography; N/A, not available.

Methods

In both investigations, the medical records of all patients who had undergone an ERCP procedure up to 45 days before the mentioned events were reviewed. The IPAC team observed the endoscope’s reprocessing techniques. All involved endoscopes were sampled and returned to the manufacturer for evaluation.

Results

First investigation

The 3 patients underwent procedures with the same endoscopic device (endoscope 1-TJF-Q180V, serial no. 2507371). Another endoscope was used to re-examine one of the patients (endoscope 2-TJF-Q180V, serial no. 2507365). Both endoscopes were immediately taken out of service, and ERCP procedures at the hospital were discontinued.

An investigation revealed that a known E. coli NDM carrier with E. coli NDM detected in his gallbladder aspirate underwent ERCP with the first endoscope 42 days before day 1. This patient was presumably the index case 1 (Table 1).

All patients who had undergone an ERCP procedure with endoscope 1 (16 patients) after the index case or with endoscope 2 (7 patients), which was used to re-examine one of the patients, were invited for rectal screening. All 23 patients were screened at least once; 9 were screened twice at least 1 month apart. All results were negative.

Deficiencies in cleaning and storage of endoscopes were noted. Reprocessing of the duodenoscopes was performed according to manufacturer’s instructions and included immediate manual wiping of the outside of the duodenoscope and leak testing, then soaking with an enzymatic solution and manual reprocessing within an hour of completion of the procedure, followed by automated reprocessing with HLD, and finally vertical hanging for drying in an unventilated cabinet. The process of cleaning and storing clean endoscopes occurred in the same room without separation between clean and contaminated zones.

After the outbreak, cleaning and disinfection processes of duodenoscopes were moved to the main gastroenterology cleaning unit that work according to infection prevention and control standards. Clean endoscopes were stored in standardized lockers in a separate room adjacent to the ERCP unit.

Affected endoscopes were sampled and E. coli-NDM grew in cultures from 3 channels of the first endoscope. Cultures from the second endoscope and the brushes were sterile. Molecular typing revealed that all organisms had carbapenemase gene bla NDM-19. All isolates were E. coli ST167 with the same resistance profile and antibiotic resistance genes. According to the phylogenetic tree, the 5 isolates were very closely related (Supplementary Fig. 1 online). In addition, all samples appeared to contain the same plasmid, IncX3. After laboratory confirmation, all 5 endoscopes used in the ERCP unit were immediately sterilized with ethylene oxide gas.

The endoscopes were revised by the manufacturer and showed numerous cracks and corrosion damage to the insertion tube and protector, the control unit connector, and the distal end cap. The damage was repaired before they were reused.

For devices used in patients known to be MDRO carriers, a cleaning protocol with double reprocessing cycles was implemented. Small brushes that fit on the tip of the elevator portion of the endoscope were procured to clean inaccessible parts of the endoscopes.

Second investigation

E. coli-NDM was detected in cultures from the endoscope 2. However, 5 patients who had undergone ERCP with this endoscope after the index case were screened for CPE and the culture results were negative. Positive samples from the index case, the child, and endoscope 2, were sent to the referral microbiology laboratory for molecular identification.

Molecular typing revealed that all samples had the carbapenemase gene bla NDM-1. All isolates were E. coli ST115 with the same resistance profile, which was different from the isolates of the first outbreak (Supplementary Table 2 online). According to the phylogenetic tree, the 3 isolates were very closely related (Supplementary Fig. 1 online). Similarly, all samples appeared to contain the plasmid ColpVC.

Inspection by the manufacturer revealed numerous cracks and deformations in the distal end cap. The TJF-Q180V endoscopes were not returned to service due to nonusability, and all endoscopes were replaced with PENTAX duodenoscopes. The ED34-i10T2 video duodenoscope from PENTAX Medical (Montvale, NJ) has a sterile disposable elevator cap that is easily replaced and improves the cleanability of the duodenoscope. No additional cases have been reported since the second outbreak (28 months).

Discussion

We report here 2 genetically unrelated outbreaks of E. coli-NDM transmission via ERCP endoscopes. The occurrence of 2 unrelated events within a few months despite improvement in HLD compliance supports our hypothesis of contamination from inaccessible parts of the elevator channels. Contamination rates can be as high as 5.7% despite double HLD or ethylene gas sterilization, Reference Larsen, Russell and Ockert2 underscoring the difficulty of cleaning and supporting our decision to use endoscopes with disposable elevator end caps. This action is supported by the recent US Food and Drug Administration recommendation to switch to disposable end caps, which allows more effective reprocessing of endoscopes. 7

Awareness of violations in the cleaning process needs to be heightened, and audits should be conducted regularly. Reference Cristina, Sartini and Schinca8 Manual bedside cleaning and leak testing should be performed immediately after the procedure. Proper manual cleaning of endoscopes with special brushes compatible with the internal channels and detachable parts of the endoscope is critical to remove debris and to prevent biofilm formation. Reference Valeriani, Agodi and Casini9

Small cracks in the internal canals of duodenoscopes could serve as escape points for organic materials and bacteria and subsequent biofilm formation. Thus, annual compatibility testing by the manufacturer may be warranted.

In addition, microbiologic surveillance of duodenoscopes should be performed at specific intervals, as recommended by the Center for Disease Control and Prevention. 10 In the case of repeated positive cultures, evaluation by the manufacturer is warranted. Reference Cristina, Sartini and Schinca8,10 The investigations of these outbreaks were conducted after the detection of a very rare MDRO infection. Our findings may suggest that other events caused by more common pathogens may go unnoticed.

In conclusion, regular review of duodenoscope reprocessing procedures by IPAC teams is essential, even in the absence of visible deficiencies. However, strict adherence to manufacturers’ reprocessing guidelines is probably not sufficient to prevent all ERCP-related infections. Endoscopes should be inspected regularly for the presence of internal cracks or damage that could promote biofilm formation and that duodenoscopes be used with disposable end caps to ensure optimal cleaning. 10

Supplementary material

To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2023.21

Acknowledgments

Financial support

No financial support was provided relevant to this article.

Conflicts of interest

All authors report no conflicts of interest relevant to this article.

References

Anderson, DJ, Shimpi, RA, McDonald, JR, et al. Infectious complications following endoscopic retrograde cholangiopancreatography: an automated surveillance system for detecting postprocedure bacteremia. Am J Infect Control 2008;36:592–594.10.1016/j.ajic.2007.10.023CrossRefGoogle Scholar
Larsen, S, Russell, R, Ockert, L, et al. Rate and impact of duodenoscope contamination: a systematic review and meta-analysis. EClinicalMedicine 2020;25:100451.10.1016/j.eclinm.2020.100451CrossRefGoogle Scholar
Beilenhoff, U, Biering, H, Blum, R, et al. Reprocessing of flexible endoscopes and endoscopic accessories used in gastrointestinal endoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE) and European Society of Gastroenterology Nurses and Associates (ESGENA)—update 2018. Endoscopy 2018;50:1205–1235.Google Scholar
Guideline Task Force, Reprocessing, Petersen, BT, Cohen, J, et al. Multisociety guideline on reprocessing flexible GI endoscopes: 2016 update. Gastrointest Endosc 2017;85:282–294.e1.Google Scholar
Epstein, L, Hunter, JC, Arwady, MA, et al. New Delhi metallo-β-lactamase–producing carbapenem-resistant Escherichia coli associated with exposure to duodenoscopes. JAMA 2014;312:1447–1455.10.1001/jama.2014.12720CrossRefGoogle Scholar
Humphries, RM, Yang, S, Kim, S, et al. Duodenoscope-related outbreak of a carbapenem-resistant Klebsiella pneumoniae identified using advanced molecular diagnostics. Clin Infect Dis 2017; 65:1159–1166.CrossRefGoogle ScholarPubMed
Use duodenoscopes with innovative designs to enhance safety: FDA safety communication. US Food and Drug Administration website. https://www.fda.gov/medical-devices/safety-communications/use-duodenoscopes-innovative-designs-enhance-safety-fda-safety-communication. Published 2022. Accessed February 3, 2023.Google Scholar
Cristina, ML, Sartini, M, Schinca, E, et al. Is post-reprocessing microbiological surveillance of duodenoscopes effective in reducing the potential risk in transmitting pathogens? Int J Environ Res Public Health 2019;17:140.10.3390/ijerph17010140CrossRefGoogle Scholar
Valeriani, F, Agodi, A, Casini, B, et al. Potential testing of reprocessing procedures by real-time polymerase chain reaction: a multicenter study of colonoscopy devices. Am J Infect Control 2018; 46:159–164.10.1016/j.ajic.2017.08.008CrossRefGoogle Scholar
Interim protocol for healthcare facilities regarding surveillance for bacterial contamination of duodenoscopes after reprocessing. Centers for Disease Control and Prevention website. https://www.cdc.gov/hai/organisms/cre/cre-duodenoscope-surveillance-protocol.html. Published 2015. Accessed February 3, 2023.Google Scholar
Figure 0

Table 1.Patients Positive for Carbapenem-Resistant Enterobacteriaceae, NDM β-Lactamase

Supplementary material: File

Dabaja-Younis et al. supplementary material

Tables S1-S2 and Figure S1

Download Dabaja-Younis et al. supplementary material(File)
File 45.3 KB