Multi-site implementation of whole genome sequencing for hospital infection control: A prospective genomic epidemiological analysis.

Norelle L Sherry, Claire L Gorrie, Jason C Kwong, Charlie Higgs, Rhonda L Stuart, Caroline Marshall, Susan A Ballard, Michelle Sait, Tony M Korman, Monica A Slavin, Robyn S Lee, Maryza Graham, Marcel Leroi, Leon J Worth, Hiu Tat Chan, Torsten Seemann, M Lindsay Grayson, Benjamin P Howden, Controlling Superbugs Study Group
Author Information
  1. Norelle L Sherry: Microbiological Diagnostic Unit (MDU) Public Health Laboratory, Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  2. Claire L Gorrie: Microbiological Diagnostic Unit (MDU) Public Health Laboratory, Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  3. Jason C Kwong: Department of Infectious Diseases, Austin Health, Heidelberg, Victoria, Australia.
  4. Charlie Higgs: Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  5. Rhonda L Stuart: Monash Infectious Diseases, Monash Health, Clayton, Victoria, Australia.
  6. Caroline Marshall: Infection Prevention & Surveillance, Victorian Infectious Diseases Service, Melbourne Health, Parkville, Victoria, Australia.
  7. Susan A Ballard: Microbiological Diagnostic Unit (MDU) Public Health Laboratory, Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  8. Michelle Sait: Microbiological Diagnostic Unit (MDU) Public Health Laboratory, Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  9. Tony M Korman: Monash Infectious Diseases, Monash Health, Clayton, Victoria, Australia.
  10. Monica A Slavin: Department of Infectious Diseases, Peter MacCallum Cancer Centre, Parkville, Victoria, Australia.
  11. Robyn S Lee: Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  12. Maryza Graham: Monash Infectious Diseases, Monash Health, Clayton, Victoria, Australia.
  13. Marcel Leroi: Department of Infectious Diseases, Austin Health, Heidelberg, Victoria, Australia.
  14. Leon J Worth: Department of Infectious Diseases, Peter MacCallum Cancer Centre, Parkville, Victoria, Australia.
  15. Hiu Tat Chan: Department of Microbiology, Melbourne Health, Parkville, Victoria, Australia.
  16. Torsten Seemann: Microbiological Diagnostic Unit (MDU) Public Health Laboratory, Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.
  17. M Lindsay Grayson: Department of Infectious Diseases, Austin Health, Heidelberg, Victoria, Australia.
  18. Benjamin P Howden: Microbiological Diagnostic Unit (MDU) Public Health Laboratory, Department of Microbiology & Immunology at the Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria, Australia.

Abstract

Background: Current microbiological methods lack the resolution to accurately identify multidrug-resistant organism (MDRO) transmission, however, whole genome sequencing can identify highly-related patient isolates providing opportunities for precision infection control interventions. We investigated the feasibility and potential impact of a prospective multi-centre genomics workflow for hospital infection control.
Methods: We conducted a prospective genomics implementation study across eight Australian hospitals over 15 months (2017,2018), collecting all clinical and screening isolates from inpatients with VRE, MRSA, ESBL (ESBL-Ec), or ESBL (ESBL-Kp). Genomic and epidemiologic data were integrated to assess MDRO transmission.
Findings: In total, 2275 isolates were included from 1970 patients, predominantly ESBL-Ec (40·8%) followed by MRSA (35·6%), VRE (15·2%), and ESBL-Kp (8·3%).Overall, hospital and genomic epidemiology showed 607 patients (30·8%) acquired their MDRO in hospital, including the majority of VRE (266 patients, 86·4%), with lower proportions of ESBL-Ec (186 patients, 23·0%), ESBL-Kp (42 patients, 26·3%), and MRSA (113 patients, 16·3%). Complex patient movements meant the majority of MDRO transmissions would remain undetected without genomic data.The genomics implementation had major impacts, identifying unexpected MDRO transmissions prompting new infection control interventions, and contributing to VRE becoming a notifiable condition. We identified barriers to implementation and recommend strategies for mitigation.
Interpretation: Implementation of a multi-centre genomics-informed infection control workflow is feasible and identifies many unrecognised MDRO transmissions. This provides critical opportunities for interventions to improve patient safety in hospitals.
Funding: Melbourne Genomics Health Alliance (supported by State Government of Victoria, Australia), and National Health and Medical Research Council (Australia).

Keywords

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Word Cloud

Created with Highcharts 10.0.0MDROpatientsinfectioncontrolVREgenomesequencinghospitalimplementationMRSAESBL-EcESBL-Kppatientisolatesinterventionsprospectivegenomicsgenomictransmissionsidentifyorganismtransmissionwholeopportunitiesmulti-centreworkflowhospitalsESBLdataepidemiologymajorityHealthAustraliaExtended-spectrumbeta-lactamaseWholeBackground:Currentmicrobiologicalmethodslackresolutionaccuratelymultidrug-resistanthowevercanhighly-relatedprovidingprecisioninvestigatedfeasibilitypotentialimpactMethods:conductedstudyacrosseightAustralian15months20172018collectingclinicalscreeninginpatientsGenomicepidemiologicintegratedassessFindings:total2275included1970predominantly40·8%followed35·6%15·2%8·3%Overallshowed60730·8%acquiredincluding26686·4%lowerproportions18623·0%4226·3%11316·3%ComplexmovementsmeantremainundetectedwithoutThemajorimpactsidentifyingunexpectedpromptingnewcontributingbecomingnotifiableconditionidentifiedbarriersrecommendstrategiesmitigationInterpretation:Implementationgenomics-informedfeasibleidentifiesmanyunrecognisedprovidescriticalimprovesafetyFunding:MelbourneGenomicsAlliancesupportedStateGovernmentVictoriaNationalMedicalResearchCouncilMulti-sitecontrol:epidemiologicalanalysisAntimicrobialresistanceEscherichiacoliKlebsiellapneumoniaeHospitalInfectionpreventionMultidrug-resistantMethicillin-resistantStaphylococcusaureusVancomycin-resistantEnterococcusWGS

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