Multiple distinct outbreaks of Panton–Valentine leucocidin-positive community-associated meticillin-resistant Staphylococcus aureus in Ireland investigated by whole-genome sequencing

B.A Mcmanus,B.K Aloba,M.R Earls,G.I Brennan,B O'Connell,S Monecke,R Ehricht,A.C Shore,D.C Coleman

doi:10.1016/j.jhin.2020.11.021

Abstract

Panton-Valentine leucocidin (PVL)-positive community-associated meticillin-resistant Staphylococcus aureus (CA-MRSA) is increasingly associated with infection outbreaks. To investigate multiple suspected PVL-positive CA-MRSA outbreaks using whole-genome sequencing (WGS). Forty-six suspected outbreak-associated isolates from 36 individuals at three separate Irish hospitals (H1-H3) and from separate incidents involving separate families associated with H2 were investigated by whole-genome multi-locus sequence typing (wgMLST). Two clusters (CH1 and CH2) consisting of 8/10 and 6/6 PVL-positive t008 ST8-MRSA-IVa isolates from H1 and H2, respectively, were identified. Within each cluster, neighbouring isolates were separated by ≤5 allelic differences; however, ≥73 allelic differences were identified between the clusters, indicating two independent outbreaks. Isolates from the H3 maternity unit formed two clusters (CH3-SCI and CH3-SCII) composed of four PVL-negative t4667 ST5-MRSA-V and 14 PVL-positive t002 ST5-MRSA-IVc isolates, respectively. Within clusters, neighbouring isolates were separated by ≤24 allelic differences, whereas both clusters were separated by 1822 allelic differences, indicating two distinct H3 outbreaks. Eight PVL-positive t127 ST1-MRSA-V+fus and three PVL-negative t267 ST97-MRSA-V+fus isolates from two distinct H2-associated families FC1 (N= 4) and FC2 (N= 7) formed three separate clusters (FC1 (t127), FC2 (t127) and FC2 (t267)). Neighbouring isolates within clusters were closely related and exhibited ≤7 allelic differences. Intrafamilial transmission was apparent, but the detection of ≥48 allelic differences between clusters indicated no interfamilial transmission. The frequent importation of PVL-positive CA-MRSA into healthcare settings, transmission and association with outbreaks is a serious ongoing concern. WGS is a highly discriminatory, informative method for deciphering such outbreaks conclusively.

Highlights

Community-associated methicillin-resistant infections were originally defined as those occurring in otherwise healthy populations without traditional healthcare-associated MRSA (HA-MRSA) risk factors[1]
Twenty MRSA isolates submitted to the NMRSARL were included as comparator reference isolates (CRFs) including Panton-Valentine leukocidin (PVL)-positive MRSA identified as spa types t002, t008 and t127 recovered between 2014 and 2019 from community general practice clinics, regional Irish hospitals, or Dublin-based teaching hospitals other than those included in the present study (Table SI)
Six additional isolates recovered from two separate patients at a separate Dublin hospital (H2) during one week within the same period of the H1 outbreak were identified as arginine catabolic mobile element (ACME)- and PVL-positive ST8-MRSA-IVa

Summary

Introduction

Community-associated methicillin-resistant infections were originally defined as those occurring in otherwise healthy populations without traditional healthcare-associated MRSA (HA-MRSA) risk factors[1]. CA-MRSA lineages typically carry smaller staphylococcal chromosomal cassette elements harbouring mec (SCCmec) such as SCCmec types IV and V, fewer antimicrobial resistance determinants and larger arsenals of virulence factor-encoding genes than HA-MRSA. These are considered contributory factors in the ability of CA-MRSA to infect otherwise healthy individuals. The boundaries between CA-MRSA and HA-MRSA have increasingly blurred as CA-MRSA lineages have diversified and become increasingly prevalent in hospitals and other healthcare settings[1]

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