Search and Contain: Impact of an Integrated Genomic and Epidemiological Surveillance and Response Program for Control of Carbapenemase-producing Enterobacterales.

antimicrobial resistance carbapenemase-producing Enterobacterales genomics infection control public health surveillance

Journal

Clinical infectious diseases : an official publication of the Infectious Diseases Society of America
ISSN: 1537-6591
Titre abrégé: Clin Infect Dis
Pays: United States
ID NLM: 9203213

Informations de publication

Date de publication:
06 12 2021
Historique:
received: 10 03 2020
accepted: 08 07 2020
pubmed: 15 7 2020
medline: 15 3 2022
entrez: 15 7 2020
Statut: ppublish

Résumé

Multiresistant organisms (MROs) pose a critical threat to public health. Population-based programs for control of MROs such as carbapenemase-producing Enterobacterales (CPE) have emerged and evaluation is needed. We assessed the feasibility and impact of a statewide CPE surveillance and response program deployed across Victoria, Australia (population 6.5 million). A prospective multimodal intervention including active screening, carrier isolation, centralized case investigation, and comparative pathogen genomics was implemented. We analyzed trends in CPE incidence and clinical presentation, risk factors, and local transmission over the program's first 3 years (2016-2018). CPE case ascertainment increased over the study period to 1.42 cases/100 000 population, linked to increased screening without a concomitant rise in active clinical infections (0.45-0.60 infections/100 000 population, P = .640). KPC-2 infection decreased from 0.29 infections/100 000 population prior to intervention to 0.03 infections/100 000 population in 2018 (P = .003). Comprehensive case investigation identified instances of overseas community acquisition. Median time between isolate referral and genomic and epidemiological assessment for local transmission was 11 days (IQR, 9-14). Prospective surveillance identified numerous small transmission networks (median, 2; range, 1-19 cases), predominantly IMP and KPC, with median pairwise distance of 8 (IQR, 4-13) single nucleotide polymorphisms; low diversity between clusters of the same sequence type suggested genomic cluster definitions alone are insufficient for targeted response. We demonstrate the value of centralized CPE control programs to increase case ascertainment, resolve risk factors, and identify local transmission through prospective genomic and epidemiological surveillance; methodologies are transferable to low-prevalence settings and MROs globally.

Sections du résumé

BACKGROUND
Multiresistant organisms (MROs) pose a critical threat to public health. Population-based programs for control of MROs such as carbapenemase-producing Enterobacterales (CPE) have emerged and evaluation is needed. We assessed the feasibility and impact of a statewide CPE surveillance and response program deployed across Victoria, Australia (population 6.5 million).
METHODS
A prospective multimodal intervention including active screening, carrier isolation, centralized case investigation, and comparative pathogen genomics was implemented. We analyzed trends in CPE incidence and clinical presentation, risk factors, and local transmission over the program's first 3 years (2016-2018).
RESULTS
CPE case ascertainment increased over the study period to 1.42 cases/100 000 population, linked to increased screening without a concomitant rise in active clinical infections (0.45-0.60 infections/100 000 population, P = .640). KPC-2 infection decreased from 0.29 infections/100 000 population prior to intervention to 0.03 infections/100 000 population in 2018 (P = .003). Comprehensive case investigation identified instances of overseas community acquisition. Median time between isolate referral and genomic and epidemiological assessment for local transmission was 11 days (IQR, 9-14). Prospective surveillance identified numerous small transmission networks (median, 2; range, 1-19 cases), predominantly IMP and KPC, with median pairwise distance of 8 (IQR, 4-13) single nucleotide polymorphisms; low diversity between clusters of the same sequence type suggested genomic cluster definitions alone are insufficient for targeted response.
CONCLUSIONS
We demonstrate the value of centralized CPE control programs to increase case ascertainment, resolve risk factors, and identify local transmission through prospective genomic and epidemiological surveillance; methodologies are transferable to low-prevalence settings and MROs globally.

Identifiants

pubmed: 32663248
pii: 5871379
doi: 10.1093/cid/ciaa972
pmc: PMC8662772
doi:

Substances chimiques

Bacterial Proteins 0
beta-Lactamases EC 3.5.2.6
carbapenemase EC 3.5.2.6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3912-e3920

Subventions

Organisme : National Health and Medical Research Council
ID : GNT1149991
Organisme : Australian Government Research Training Program scholarships
Organisme : Microbiological Diagnostic Unit Public Health Laboratory
Organisme : Victorian Government

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America.

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Auteurs

Courtney R Lane (CR)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Judith Brett (J)

VICNISS Healthcare Associated Infection Surveillance Coordinating Centre, at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Mark Schultz (M)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Claire L Gorrie (CL)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Kerrie Stevens (K)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Donna R M Cameron (DRM)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Health and Human Services, Victorian Government, Melbourne, Victoria, Australia.

Siobhan St George (S)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Annaliese van Diemen (A)

Department of Health and Human Services, Victorian Government, Melbourne, Victoria, Australia.

Marion Easton (M)

Department of Health and Human Services, Victorian Government, Melbourne, Victoria, Australia.

Rhonda L Stuart (RL)

Monash Infectious Diseases, Monash Health, Monash Medical Centre, Clayton, Victoria, Australia.

Michelle Sait (M)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Anton Y Peleg (AY)

Department of Infectious Diseases, Alfred Hospital, and Central Clinical School, Monash University, Melbourne, Victoria, Australia.
Infection and Immunity Program, Monash Biomedicine Discovery Institute, Department of Microbiology, Monash University, Clayton, Victoria, Australia.

Andrew J Stewardson (AJ)

Department of Infectious Diseases, Alfred Hospital, and Central Clinical School, Monash University, Melbourne, Victoria, Australia.

Allen C Cheng (AC)

Department of Infectious Diseases, Alfred Hospital, and Central Clinical School, Monash University, Melbourne, Victoria, Australia.
School of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia.

Denis W Spelman (DW)

Department of Infectious Diseases, Alfred Hospital, and Central Clinical School, Monash University, Melbourne, Victoria, Australia.
Department of Microbiology, The Alfred Hospital, Melbourne, Victoria, Australia.

Mary Jo Waters (MJ)

Department of Microbiology, St Vincent's Hospital Melbourne, Fitzroy, Victoria, Australia.

Susan A Ballard (SA)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Norelle L Sherry (NL)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Infectious Diseases, Austin Health, Heidelberg, Victoria, Australia.

Deborah A Williamson (DA)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Finn Romanes (F)

Department of Health and Human Services, Victorian Government, Melbourne, Victoria, Australia.

Brett Sutton (B)

Department of Health and Human Services, Victorian Government, Melbourne, Victoria, Australia.

Jason C Kwong (JC)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Infectious Diseases, Austin Health, Heidelberg, Victoria, Australia.

Torsten Seemann (T)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Anders Goncalves da Silva (A)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.

Nicola Stephens (N)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Health and Human Services, Victorian Government, Melbourne, Victoria, Australia.
University of Tasmania, Hobart, Tasmania, Australia.

Benjamin P Howden (BP)

Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
Department of Infectious Diseases, Austin Health, Heidelberg, Victoria, Australia.

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