Genomic analysis of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) causing infections in children—a Spanish multicenter study

Abstract

Staphylococcus aureus; Community-associated infections; Skin and soft tissue infections

Staphylococcus aureus; Infecciones asociadas a la comunidad; Infecciones de piel y tejidos blandos

Staphylococcus aureus; Infeccions associades a la comunitat; Infeccions de la pell i dels teixits tous

Objectives: Staphylococcus aureus is one of the most common human pathogens causing skin and soft tissue infections (SSTIs) among children. This study investigated the molecular traits of community-associated methicillin-resistant S. aureus (CA-MRSA) isolates causing infections in children in Spain. Methods: Antibiotic susceptibility testing and whole-genome sequencing were performed in 98 CA-MRSA isolates (4.2 median age, 52% males). The phylogenetic relationship, antibiotic resistance, virulence, and plasmid replicon genes content were investigated. Results: Resistance rates were found as follows: Erythromycin, 42.9%, which could be explained due to the presence of erm(C), mph(C), and msr(A) genes; tobramycin, 27.5%, which could be explained due to the presence of aac(6′)-Ie/aph(2″)-Ia and aadD1 genes; tetracycline, 25.5%, which could be explained mainly due to the presence of tet(K) genes; levofloxacin and moxifloxacin, 19.4%, which could be explained primarily due to the mutations in gyrA and parC genes; and gentamicin, 15.3%, which could be explained due to the presence of aac(6′)-Ie/aph(2″)-Ia gene. The most prevalent lineage was ST8-IVc and t008. Most isolates were genetically diverse, except for three groups of isolates from the same hospital and one group of isolates from different hospitals. These had less than or equal to 5 allele differences by core-genome multilocus sequence typing (cgMLST) analysis or 0–6 core single-nucleotide polymorphisms (SNPs) by core-genome SNP-based analysis. Phage-encoded Panton–Valentine leukocidin (PVL) genes were found in 75.5% of the isolates. Other common virulence genes were related to adhesion (capA and capP), lipid degradation (geh), hemolysis (hlb, hld, hlgABC, and hly/hla), and tissue destruction (sspAB). Conclusion: This study observed a high genetic diversity among CA-MRSA isolates causing community-acquired infections in children in Spain, with ST8-IVc as the most prevalent lineage. Nevertheless, genetic relatedness of some isolates from the same as well as different hospitals suggests the dissemination of CA-MRSA among children by contact.

The author(s) declare that financial support was received for the research and/or publication of this article. This study was supported by the Spanish Ministry of Science and Innovation, Instituto de Salud Carlos III (ISCIII) and the European Regional Development Funds (grant number: PI23CIII/00917); the Consorcio Centro de Investigación Biomédica en Red (CIBER); Instituto de Salud Carlos III, Ministerio de Ciencia e Innovación; and Unión Europea-NextGenerationEU (CB21/13/00095, CB21/13/00025, CB21/13/00054, and CB21/13/00099). SG-C was supported by the Dirección General de Investigación e Innovación, Consejería de Educación e Investigación, Comunidad de Madrid (CAM), and the Instituto de Salud Carlos III (ISCIII) (grant numbers: 2018-T1/BMD-11174 and 2022-5A/BMD-24243; Research Talent Attraction Program – Modality 1). BB-Q-d-L was supported by the Instituto de Salud Carlos III and the European Union (grant number: CM23/00057; Río Hortega Program).