Abstract

Methicillin-susceptible (MSSA) and methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization predisposes individuals for endogenous infections and is a major threat to children. Recently, oxacillin/cefoxitin-susceptible mecA-positive S. aureus (OS-MRSA) has been reported worldwide. Herein, a prospective, cross-sectional study was conducted across five schools, representing three educational stages, in Guangzhou, China. Nasal swabs from 2,375 students were cultured for S. aureus and all isolates were subjected to antibiotic susceptibility testing phenotypically and confirmed by femB and mecA genetic detection; all the isolates were classified as MSSA, MRSA, or OS-MRSA. All strains were also analyzed by multi-locus sequence typing. Among the 2,375 swabs, S. aureus was detected in 744 children (31.3%, 95% CI: 25.9–36.7%), of whom 72 had MRSA (3.0%, 95% CI: 0.6–5.4%) and 4 had OS-MRSA (0.2%, 95% CI: 0.1–0.3%), of which an oxacillin- and cefoxitin-susceptible MRSA strain was identified. The prevalence of S. aureus and MRSA was higher in younger children. The highest percentage of drug resistance of the S. aureus isolates (n = 744) was to penicillin (85.5%), followed by erythromycin (43.3%) and clidamycin (41.0%). The most prevalent sequence types (STs) were ST30, ST45, and ST188 in MSSA, accounting for 38.7% of the total isolates, whereas ST45, ST59, and ST338 accounted for 74.6% of the MRSA isolates and ST338 accounted for 50.0% of the OS-MRSA isolates. The MRSA and OS-MRSA isolates (n = 76) were grouped into three clades and one singleton, with clonal complex (CC) 45 as the most predominant linkage. The top nine multi-locus sequence typing-based CCs (CC30, CC45, CC5, CC1, CC15, CC944, CC398, CC59, CC7) represented 86.7% of all S. aureus isolates. All CC30 isolates were resistant to erythromycin and clidamycin, and almost all these isolates were also resistant to penicillin (99.2%). The CC45 and CC59 isolates exhibited high resistance rates to oxacillin at 31.5 and 59.0%, respectively. This study provides updated data valuable for designing effective control strategies to mitigate the burden of disease and to improve the adequacy of empirical antimicrobial treatments for potentially harmful infections.

Highlights

  • Community-acquired pneumonia caused by prevalent respiratory pathogens such as Staphylococcus aureus is a major public health concern and leading cause of death [1, 2]

  • The prevalence of S. aureus and methicillin-resistant Staphylococcus aureus (MRSA) nasal carriage was high among students across all educational stages with an average of 31.3% [95% confidence interval (CI): 25.9–36.7%] and 3.0%, respectively, whereas OS-MRSA was relatively low at 0.2%

  • The overall prevalence of MRSA (3.0%, 95% CI: 0.6–5.4%) was in the upper range [34], whereas that of OS-MRSA (0.2%, 95% CI: 0.1–0.3%) was relatively low at ∼0.5% in cases of S. aureus [35]. This finding that nasal carriages of S. aureus, MRSA, were significantly higher among children at earlier educational stages agreed with several other studies [32, 36]

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Summary

Introduction

Community-acquired pneumonia caused by prevalent respiratory pathogens such as Staphylococcus aureus is a major public health concern and leading cause of death [1, 2]. The prevalence of multidrug-resistant isolates, methicillin-resistant S. aureus (MRSA), remains persistently high in China and is recognized as a major cause of nosocomial infections [3]. MRSA acquired drug resistance via incorporation of mecA or its ortholog into the chromosome at a specific site, encoding an alternative penicillin-binding protein that has low affinity for almost the entire class of β-lactam drugs including methicillin, oxacillin, and most cephem agents [12]. MRSA is defined as S. aureus isolates genetically containing mecA or mecC or phenotypically showing resistance to oxacillin conventionally or to cefoxitin [13]. Oxacillin- and cefoxitin-susceptiblemecA-positive S. aureus isolates, known as “stealth” MRSA, have been increasingly reported worldwide; these bacteria can be misinterpreted as methicillin-susceptible S. aureus (MSSA) and convert to oxacillin-resistant when exposed to β-lactam antibiotics [16]

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