Distribution of Biocide Resistance Genes and Association with Clonal Complex Genotypes in Staphylococcus aureus Isolated from School-Age Children in Guangzhou

Background: Disinfectant and antibiotics such as chlorhexidine and mupirocin are often prescribed to children in affected communities to prevent colonization and transmission of Staphylococcus aureus, but this has led to an increasing rate of biocide resistance. In this study, we aimed to determine the distribution of biocide resistance genes among S. aureus isolates from school-age children in Guangzhou, investigate chlorhexidine gluconate and mupirocin susceptibility and clonal complex (CC) genotypes in strains carrying biocide-resistance genes, and further explore the role of biofilms in this resistance.Methods: Antibiotic resistance and multilocus sequence genotyping were performed on 722 S. aureus isolates from 2375 nasal swabs from school-aged children in Guangzhou. The distribution of nine biocide genes (qacA/B, mupA, mepA, sepA, norA, lmrS, smr, mupB, qacG) was determined by PCR. Isolates carrying qacA/B or mupA genes were further tested for susceptibility to chlorhexidine gluconate (CHG) and mupirocin using broth microdilution and their biofilm formation abilities were evaluated by a microtiter plate test.Results: The most prevalent of the nine biocide resistance genes were mepA (95.57%), followed by norA (78.81%), lmrS (77.01%), and sepA (58.17%). The qacG gene was not detected. We found that junior school students possessed a significantly higher distribution of qacA/B and mupA and a lower distribution of mepA, norA and lmrS genes; distribution of sepA was significantly decreased in CC30 and CC45 genotypes, and presence of sepA was associated with resistance to antibiotics such as CLI, ERY, TCY, SXT, CIP, and LVX. In addition, 64 (94.1%, n=68) qacA/B+ isolates showed CHG resistance, 12 (100.0%, n=12) mupA+ isolates were mupirocin resistant, and 4 (80%, n=5) and 5 (100%, n=5) qacA/B+mupA+ isolates were CHG and mupirocin resistant, respectively. Of these 85 isolates, 98.8 % (n=84) had different degrees of biofilm-forming abilities, which were positively associated with CHG and mupirocin resistance.Conclusion: The distribution of biocide resistance genes was associated with special CCs. The qacA/B and mupA genes are associated with resistance to CHG and mupirocin, and biofilm formation was found to contribute to this biocide resistance.