A large, refractory nosocomial outbreak of klebsiella pneumoniae carbapenemase-producing Escherichia coli demonstrates carbapenemase gene outbreaks involving sink sites require novel approaches to infection control

the TRACE Investigators’ Group

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Abstract

Carbapenem-resistant Enterobacteriaceae (CRE) represent a health threat, but effective control interventions remain unclear. Hospital wastewater sites are increasingly being highlighted as important potential reservoirs. We investigated a large Klebsiella pneumoniae carbapenemase (KPC)-producing Escherichia coli outbreak and wider CRE incidence trends in the Central Manchester University Hospital NHS Foundation Trust (CMFT) (United Kingdom) over 8 years, to determine the impact of infection prevention and control measures. Bacteriology and patient administration data (2009 to 2017) were linked, and a subset of CMFT or regional hospital KPC-producing E. coli isolates (n 268) were sequenced. Control interventions followed international guidelines and included cohorting, rectal screening (n 184,539 screens), environmental sampling, enhanced cleaning, and ward closure and plumbing replacement. Segmented regression of time trends for CRE detections was used to evaluate the impact of interventions on CRE incidence. Genomic analysis (n 268 isolates) identified the spread of a KPC-producing E. coli outbreak clone (strain A, sequence type 216 [ST216]; n 125) among patients and in the environment, particularly on 2 cardiac wards (wards 3 and 4), despite control measures. ST216 strain A had caused an antecedent outbreak and shared its KPC plasmids with other E. coli lineages and Enterobacteriaceae species. CRE acquisition incidence declined after closure of wards 3 and 4 and plumbing replacement, suggesting an environmental contribution. However, ward 3/ward 4 wastewater sites were rapidly recolonized with CRE and patient CRE acquisitions recurred, albeit at lower rates. Patient relocation and plumbing replacement were associated with control of a clonal KPC-producing E. coli outbreak; however, environmental contamination with CRE and patient CRE acquisitions recurred rapidly following this intervention. The large numbers of cases and the persistence of blaKPC in E. coli, including pathogenic lineages, are of concern.

Original languageEnglish
Article numbere01689-18
JournalAntimicrobial Agents and Chemotherapy
Volume62
Issue number12
DOIs
Publication statusPublished - Dec 2018

Bibliographical note

Funding Information:
We are grateful for and acknowledge the contributions of the clinical and support staff working in the MHC, CMFT; the microbiology laboratory staff and infection control teams at CMFT; the staff of the Manchester Medical Microbiology Partnership; and the research laboratory (in particular, Ali Vaughan) and informatics and project management teams working as part of the Modernising Medical Microbiology consortium (Oxford). We thank Jeff Scott, Ashley Sharp, and Theresa Shryane (Public Health England [PHE] North West) and Suzan Trienekens (Field Epidemiology Service, PHE) for data collection and Karen Mathieson (CMFT), Jane Turton, and Claire Perry (PHE) for outbreak investigation and support. We thank the Health Protection Research Unit Steering Group for review of the draft manuscript. This work was supported by the National Institute for Health Research, Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Oxford University, in partnership with PHE (grant HPRU-2012-10041). The report presents independent research funded by the National Institute for Health Research. The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research, the Department of Health, or PHE. N.S. is funded by a PHE-University of Oxford Clinical Lectureship. Contemporaneous outbreak investigation by CMFT and PHE was undertaken as part of routine activity.

Funding Information:
We are grateful for and acknowledge the contributions of the clinical and support staff working in the MHC, CMFT; the microbiology laboratory staff and infection control teams at CMFT; the staff of the Manchester Medical Microbiology Partnership; and the research laboratory (in particular, Ali Vaughan) and informatics and project management teams working as part of the Modernising Medical Microbiology consortium (Oxford). We thank Jeff Scott, Ashley Sharp, and Theresa Shryane (Public Health England [PHE] North West) and Suzan Trienekens (Field Epidemiology Service, PHE) for data collection and Karen Mathieson (CMFT), Jane Turton, and Claire Perry (PHE) for outbreak investigation and support. We thank the Health Protection Research Unit Steering Group for review of the draft manuscript. The Transmission of Carbapenemase-producing Enterobacteriaceae (TRACE) study investigators are listed alphabetically, with those also included as named individuals in the author list in parentheses: (Zoie Aiken), (Oluwafemi Akinremi), (Julie Cawthorne), (Paul Cleary), (Derrick W. Crook), (Valerie Decraene), (Andrew Dodgson), Michel Doumith, Matthew Ellington, David W. Eyre, (Ryan George), (Malcolm Guiver), Robert Hill, Katie Hopkins, Rachel Jones, (Cheryl Lenney), (Amy J. Mathers), (Ashley McEwan), Ginny Moore, Sarah Neilson, Tim E. A. Peto, (Hang T. T. Phan), Mark Regan, (Anna C. Seale), (Nicole Stoesser), Jay Turner-Gardner, (Vicky Watts), Jimmy Walker, (A. Sarah Walker), (David H. Wyllie), (William Welfare), and (Neil Woodford). This work was supported by the National Institute for Health Research, Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Oxford University, in partnership with PHE (grant HPRU-2012-10041). The report presents independent research funded by the National Institute for Health Research. The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research, the Department of Health, or PHE. N.S. is funded by a PHE-University of Oxford Clinical Lectureship. Contemporaneous outbreak investigation by CMFT and PHE was undertaken as part of routine activity. We have no conflicts of interest to declare.

Publisher Copyright:
© 2018 American Society for Microbiology. All Rights Reserved.

Keywords

  • Antimicrobial resistance
  • Carbapenemase-producing Enterobacteriaceae
  • Genome sequencing
  • Infection control
  • Molecular epidemiology

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