Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) strains from different geographic areas have different genetic backgrounds, suggesting independent clonal evolutions. To better understand the virulence of MRSA strains and the relationship to their clonal and geographic origins, we undertook an analysis of epidemiologic, molecular, and virulence characteristics of a large number of MRSA isolates from geographically diverse origins, in a Caenorhabditis elegans infection model. A total of 99 MRSA isolates collected between 1993 and 2010 at the Geneva University Hospitals from diverse global origins were characterized with Panton–Valentine leukocidin (PVL), toxic shock syndrome toxin (TSST), accessory gene regulator (agr) group, staphylococcal cassette chromosome mec (SCCmec), S. aureus protein A (spa), multilocus sequence typing (MLST), and pulsed-field gel electrophoresis (PFGE) typing. Epidemiologic data were provided from clinical records. The bacterial virulence was tested in a C. elegans host model. The inter-relationships of epidemiological/molecular characteristics in association with nematocidal activities were analyzed with univariate and two-factor analysis of variance (ANOVA). Community-associated MRSA (CA-MRSA) strains were more virulent than hospital-associated MRSA (HA-MRSA), with higher nematocidal activities in CA-MRSA strains (0.776 vs. 0.506, p = 0.0005). All molecular characteristics (PVL, TSST, spa, SCCmec, MLST, and PFGE types) showed a significant association with nematocidal activities on univariate analysis (p < 0.005). PVL was not a significant predictor after adjusting for genomic backgrounds using spa, MLST, or PFGE typing. The dominant CA-MRSA strains in North America showed higher nematocidal activities than strains from other regions (p < 0.0001). Strains with global origins containing distinct genetic backgrounds have different virulence in the C. elegans model. Nematocidal activities were most highly correlated with SCCmec, spa, MLST, and PFGE typing, suggesting that genomic background rather than a single exotoxin characteristic was the most discriminating predictor of virulence.
Highlights
Methicillin-resistant Staphylococcus aureus (MRSA) infections have been reported in the hospital and community settings worldwide since the first case was identified in the United Kingdom [1]
We have previously shown that community-associated MRSA (CA-MRSA) is more virulent than hospital-associated MRSA (HA-MRSA) using an invertebrate Caenorhabditis elegans host model, correlating the findings with human clinical data [13]
All isolates were resistant to methicillin, and carried type I, II, III, IV, V, or VI staphylococcal cassette chromosome mec (SCCmec) elements, except for two isolates, both of which contained mecA, but were unable to be typed with the available methodology
Summary
Methicillin-resistant Staphylococcus aureus (MRSA) infections have been reported in the hospital and community settings worldwide since the first case was identified in the United Kingdom [1]. Based on multilocus sequence typing (MLST), there are currently 17 major clonal complexes (CCs) identified from the S. aureus isolates collected worldwide, including methicillinsusceptible S. aureus (MSSA) and MRSA strains [2]. For hospital-associated MRSA (HA-MRSA), the Iberian (ST247), Brazilian (ST239), Paediatric (ST5), EMRSA15 (ST22), EMRSA16 (ST36), and Berlin (ST45) clones are recognized pandemic clones in the world [3]. Community-associated MRSA (CA-MRSA) have different patterns, with the major CA-MRSA clones being ST1, ST8, ST30, ST59, ST80, and ST88, plus other minor clones, circulating around the world [4,5,6]. ST30, ST59, ST80, and ST88 are successful CA-MRSA strains present in Australia, Taiwan, Europe, and Africa, respectively [7, 8]
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