Genomic characterization of MRSA recovered from people with cystic fibrosis during two Spanish multicentre studies (2013 and 2021)

Abstract

Background: Chronic bronchopulmonary infection due to MRSA in people with cystic fibrosis (pwCF) has been associated with accelerated decline in lung function, increased hospitalizations and increased mortality.

Material and methods: We studied microbiological and genomic characteristics of MRSA isolates recovered from pwCF in two Spanish multicentre studies (2013, 2021). Antimicrobial susceptibility was performed. WGS was carried out to determine population structure [MLST, spa-typing, staphylococcal cassette chromosome mec (SCCmec)], resistome and virulome. Clinical charts of MRSA-infected and MRSA-non-infected pwCF were also reviewed.

Results: MRSA infection prevalence decreased between 2013 (29/341, 8.5%) and 2021 (21/326, 6.4%) (P = 0.378). Differences in lung function were observed between infected and non-infected patients (P < 0.005). A higher prevalence of hospital-acquired (HA) clones was found compared with community-acquired (CA) clones (2013: 67% versus 33%; and 2021: 71% versus 29%). Overall, we noted clustering of isolates based on year of sampling, type of acquisition and clonal complex (CC). HA-MRSA population was dominated by CC5, with ST125-MRSA-IVc-t067 the most prevalent lineage (37%). A higher clonal diversity was detected among CA-MRSA. One Panton-Valentine leucocidin (PVL)-positive strain (ST8-MRSA-IV) and three strains of porcine origin (two ST398-MRSA-V-t011, one ST398-MRSA-V-t8567) were found. Additionally, acquired resistance genes (n = 24) were detected, including the cfr gene conferring linezolid resistance. A higher gentamicin resistance was found in 2021 (42%) compared with 2013 (7%) (P = 0.046), associated with the aac(6')-aph(2″) gene.

Conclusions: Despite a decrease in MRSA prevalence, we showed its potential impact on CF severity and progression. Moreover, we observed great genotypic and phenotypic diversity in MRSA isolates from pwCF as well as an MDR trait.

Figure 1.

Percentage of resistant strains in HA-MRSA and CA-MRSA. CLI, clindamycin; ERY, erythromycin; GEN, gentamicin; LVX, levofloxacin; LZD, linezolid; RIF, rifampicin; SXT, trimethoprim/sulfamethoxazole.

Figure 2.

Core genome maximum-likelihood phylogenetic tree of all MRSA isolates and S. aureus reference genome (NC_007795.1) analysed by WGS.

Figure 3.

Minimum spanning trees constructed using the algorithm goeBURST (http://www.phyloviz.net/) and annotated by: (a) clonal complex multilocus sequence type (CCMLST); (b) sequence type (ST); (c) staphylococcal cassette chromosome mec (SCCmec); and (d) spa type.