Abstract
The prevalence of Staphylococcus aureus as an aggressive pathogen resistant to multiple antibiotics causing nosocomial and community-acquired infections is increasing with limited therapeutic options. Macrolide-lincosamide streptogramin B (MLSB) family of antibiotics represents an important alternative therapy for staphylococcal infections. This study was conducted over a period of five years from August 2013 to July 2018 to investigate the prevalence and molecular epidemiology in Iran of inducible resistance in S. aureus. In the current study, 126 inducible methicillin-resistant S. aureus (MRSA) (n = 106) and methicillin-sensitive S. aureus (MSSA) (n = 20) isolates were characterized by in vitro susceptibility analysis, resistance and virulence encoding gene distribution, phenotypic and genotypic analysis of biofilm formation, prophage typing, S. aureus protein A locus (spa) typing, staphylocoagulase (SC) typing, staphylococcal cassette chromosome mec (SCCmec) typing, and multilocus sequence typing. Of the 126 isolates, 76 (60.3%) were classified as hospital onset, and 50 (39.7%) were classified as community onset (CO). Biofilm formation was observed in 97 strains (77%). A total of 14 sequence types (STs), 26 spa types, 7 coagulase types, 9 prophage types, 3 agr types (no agr IV), and 9 clonal complexes (CCs) were identified in this study. The prevalence of the inducible MLSB (iMLSB) S. aureus increased from 7.5% (25/335) to 21.7% (38/175) during the study period. The iMLSB MRSA isolates were distributed in nine CCs, whereas the MSSA isolates were less diverse, which mainly belonged to CC22 (7.95%) and CC30 (7.95%). High-level mupirocin-resistant strains belonged to ST85-SCCmec IV/t008 (n = 4), ST5-SCCmec IV/t002 (n = 4), ST239-SCCmec III/t631 (n = 2), and ST8-SCCmec IV/t064 (n = 2) clones, whereas low-level mupirocin-resistant strains belonged to ST15-SCCmec IV/t084 (n = 5), ST239-SCCmec III/t860 (n = 3), and ST22-SCCmec IV/t790 (n = 3) clones. All the fusidic acid–resistant iMLSB isolates were MRSA and belonged to ST15-SCCmec IV/t084 (n = 2), ST239-SCCmec III/t030 (n = 2), ST1-SCCmec V/t6811 (n = 1), ST80-SCCmec IV/t044 (n = 1), and ST59-SCCmec IV/t437 (n = 1). The CC22 that was predominant in 2013–2014 (36% of the isolates) had almost disappeared in 2017–2018, being replaced by the CC8, which represented 39.5% of the 2017–2018 isolates. This is the first description of temporal shifts of iMLSB S. aureus isolates in Iran that identifies predominant clones and treatment options for iMLSB S. aureus–related infections.
Highlights
Staphylococcus aureus is one of the most common aggressive pathogen that causes many diseases in humans and animals such as skin and soft tissue infections, osteomyelitis, bacteremia, and endocarditis (Gordon and Lowy, 2008)
Of 126 iMLSB S. aureus isolates, 41 were collected from female patients (32.6%), and the rest were collected from male patients (85, 67.4%)
Regarding the occurrence of inducible resistance in S. aureus strains, data exhibited that most cases belonged to the age groups of 21 to years between 2013 and 2017, whereas in 2018, more than half of the cases were found to be in the age group between and 65 years
Summary
Staphylococcus aureus is one of the most common aggressive pathogen that causes many diseases in humans and animals such as skin and soft tissue infections, osteomyelitis, bacteremia, and endocarditis (Gordon and Lowy, 2008). The rate of infections due to S. aureus, especially the antibiotic-resistant strains, has dramatically increased recently, which is becoming a serious problem all over the world (Gould et al, 2012). Emerging simultaneous resistance to multiple antibacterial agents underscores the necessity for therapeutic alternatives for the treatment of bacterium-related infections (Pantosti et al, 2007; Dadashi et al, 2018). The use of macrolide–lincosamide– streptogramin group B (MLSB) antibiotics has been favored, which is regarded as an alternative approach to treating such infections (Patel et al, 2006). Clindamycin, a member of MLSB family, serves as one such effective therapeutic alternative for treating S. aureus infections, because of its proven efficacy, safety, convenience of administration (parenteral and oral), and excellent pharmacokinetic properties. One important issue in clindamycin administration is the potential emergence of inducible clindamycin resistance, which may increase the risk of clinical failure (Chavez-Bueno et al, 2005; Adhikari et al, 2017)
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