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

Courtney R Lane; Judith Brett; Mark Schultz; Claire L Gorrie; Kerrie Stevens; Donna R M Cameron; Siobhan St George; Annaliese van Diemen; Marion Easton; Rhonda L Stuart; Michelle Sait; Anton Y Peleg; Andrew J Stewardson; Allen C Cheng; Denis W Spelman; Mary Jo Waters; Susan A Ballard; Norelle L Sherry; Deborah A Williamson; Finn Romanes; Brett Sutton; Jason C Kwong; Torsten Seemann; Anders Goncalves da Silva; Nicola Stephens; Benjamin P Howden

doi:10.1093/cid/ciaa972

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

Clin Infect Dis. 2021 Dec 6;73(11):e3912-e3920. doi: 10.1093/cid/ciaa972.

Authors

Courtney R Lane^{1

2}, Judith Brett³, Mark Schultz^{1

2}, Claire L Gorrie^{1

2}, Kerrie Stevens¹, Donna R M Cameron^{1

4}, Siobhan St George¹, Annaliese van Diemen⁴, Marion Easton⁴, Rhonda L Stuart⁵, Michelle Sait¹, Anton Y Peleg^{6

7}, Andrew J Stewardson⁶, Allen C Cheng^{6

8}, Denis W Spelman^{6

9}, Mary Jo Waters¹⁰, Susan A Ballard¹, Norelle L Sherry^{1

2

11}, Deborah A Williamson¹, Finn Romanes⁴, Brett Sutton⁴, Jason C Kwong^{2

11}, Torsten Seemann², Anders Goncalves da Silva^{1

2}, Nicola Stephens^{2

4

12}, Benjamin P Howden^{1

2

11}

Affiliations

¹ Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
² Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
³ VICNISS Healthcare Associated Infection Surveillance Coordinating Centre, at the Peter Doherty Institute for Infection & Immunity, Melbourne, Victoria, Australia.
⁴ Department of Health and Human Services, Victorian Government, Melbourne, Victoria, Australia.
⁵ Monash Infectious Diseases, Monash Health, Monash Medical Centre, Clayton, Victoria, Australia.
⁶ Department of Infectious Diseases, Alfred Hospital, and Central Clinical School, Monash University, Melbourne, Victoria, Australia.
⁷ Infection and Immunity Program, Monash Biomedicine Discovery Institute, Department of Microbiology, Monash University, Clayton, Victoria, Australia.
⁸ School of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia.
⁹ Department of Microbiology, The Alfred Hospital, Melbourne, Victoria, Australia.
¹⁰ Department of Microbiology, St Vincent's Hospital Melbourne, Fitzroy, Victoria, Australia.
¹¹ Department of Infectious Diseases, Austin Health, Heidelberg, Victoria, Australia.
¹² University of Tasmania, Hobart, Tasmania, Australia.

Abstract

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.

Keywords: antimicrobial resistance; carbapenemase-producing Enterobacterales; genomics; infection control; public health surveillance.

Publication types

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

MeSH terms

Bacterial Proteins / genetics
Enterobacteriaceae Infections* / epidemiology
Enterobacteriaceae Infections* / prevention & control
Genomics
Humans
Prospective Studies
Victoria
beta-Lactamases / genetics

Substances

Bacterial Proteins
beta-Lactamases
carbapenemase

Abstract

Publication types

MeSH terms

Substances

Grants and funding