Characterization of Ocular Methicillin-Resistant Staphylococcus epidermidis Isolates Belonging Predominantly to Clonal Complex 2 Subcluster II

Abstract

Staphylococcus epidermidis is an abundant member of the microbiota of the human skin and wet mucosa, which is commonly associated with sight-threatening infections in eyes with predisposing factors. Ocular S. epidermidis has become notorious because of its capability to form biofilms on different ocular devices and due to the evolving rates of antimicrobial resistance. In this study, the molecular epidemiology of 30 ocular methicillin-resistant S. epidermidis (MRSE) isolates was assessed using multilocus sequence typing (MLST). Antimicrobial resistance, accessory gene-regulator and staphylococcal cassette chromosome mec (SCCmec) types, biofilm formation, and the occurrence of biofilm-associated genes were correlated with MLST clonal complexes. Sequence types (STs) frequently found in the hospital setting were rarely found in our collection. Overall, 12 different STs were detected with a predominance of ST59 (30%), ST5 and ST6 (13.3% each). Most of the isolates (93.3%) belonged to the clonal complex 2 (CC2) and grouped mainly within subcluster CC2-II (92.9%). Isolates grouped within this subcluster were frequently biofilm producers (92.3%) with a higher occurrence of the aap (84.5%) and bhp (46.1%) genes compared to icaA (19.2%). SCCmec type IV (53.8%) was predominant within CC2-II strains, while 38.4% were nontypeable. In addition, CC2-II strains were frequently multidrug resistant (80.7%) and demonstrated to be particularly resistant to ciprofloxacin (80.8%), ofloxacin (77%), azithromycin (61.5%), and gentamicin (57.7%). Our findings demonstrate the predominance of a particular MRSE cluster causing ocular infections, which was associated with high rates of antimicrobial resistance and particularly the carriage of biofilm-related genes coding for proteinaceous factors implicated in biofilm accumulation.

Biofilm formation of ica operon‐positive Staphylococcus epidermidis from different sources

“…The genetic diversity of SCC mec in this study was high, as in previous studies of MRSE isolates from community setting . The presence of the ica operon has been described before among clinical S. epidermidis isolates belonging to the ST2, ST5, ST6, ST7, ST16, ST23, ST35, ST284 lineages . Interestingly four icaRADBC ‐positive animal S. epidermidis belonged to STs related to icaRADBC ‐positive clinical isolates (Fig.…”

“…In our study, the three genes were frequent in nearly all the populations investigated, but aap was more frequent among icaADBCR ‐positive strains from mechanically ventilated patients, and bhp was more frequent among icaADBCR ‐positive animal isolates. The genes embp and aap have been reported at higher frequencies (≥70%) among clinical S. epidermidis obtained from diverse device‐associated infections and ocular infections , as well as among isolates from catheter colonization . However, the prevalence of bhp ranged from 40 to 50% among isolates from prosthetic joints and ocular infections , and it was reported infrequent (8–16%) among S. epidermidis from implanted central venous catheters, and non‐catheter related bacteremia, as well as among catheter colonizing isolates .…”

Molecular epidemiology of Staphylococcus epidermidis in neonatal intensive care units

“…Studies on S. epidermidis clinical isolates from neonates and adults have revealed the occurrence of predominant strains that can persist in one unit for decades , disseminate between hospitals and even countries , and belong to the widespread genetic lineage MLST clonal complex 5 (CC5) . Particularly frequent is sequence type (ST) 2, which is responsible for the majority of infections, including bloodstream, prosthetic joint, and ocular infections . The successful spread of strains causing infections has been attributed, in part, to the high rate of resistance to antibiotics.…”

“…For example, the prevalence of methicillin resistance among clinical isolates exceeds 70%, reaching nearly 100% , most commonly conferred by the staphylococcal cassette chromosome mec (SCC mec ) type IV . In addition, 40–52% of infecting isolates harbor the ica operon, 55–74% carry insertion sequence element IS 256 , and 57–74% are of agr type I . Although the carriage rate of arginine catabolic mobile element (ACME) is commonly reported to be 23–53% in invasive strains , recently, a prevalence of 78% was reported .…”

Synergy between antibiotics and natural agents results in increased antimicrobial activity against Staphylococcus epidermidis

“…Staphylococci, above all Staphylococcus aureus and Staphylococcus epidermidis, are the most frequent causes of biofilm-associated infections on indwelling medical devices, with S. epidermidis representing up to 75% of all clinical isolates in some cases [2][3][4].…”