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Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China

Mupirocin, a topical antimicrobial agent, is an important component in the eradication of methicillin-resistant Staphylococcus aureus (MRSA) colonization. The molecular characteristics of 46 mupirocin-resistant MRSA (MR-MRSA) clinical isolates were analyzed by multilocus sequence typing (MLST), stap...

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Autores principales: Guo, Yinjuan, Xu, Linling, Wang, Bingjie, Rao, Lulin, Xu, Yanlei, Wang, Xinyi, Zhao, Huilin, Yu, Jingyi, Zhou, Ying, Yu, Fangyou
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927232/
https://www.ncbi.nlm.nih.gov/pubmed/36622214
http://dx.doi.org/10.1128/spectrum.03794-22
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author Guo, Yinjuan
Xu, Linling
Wang, Bingjie
Rao, Lulin
Xu, Yanlei
Wang, Xinyi
Zhao, Huilin
Yu, Jingyi
Zhou, Ying
Yu, Fangyou
author_facet Guo, Yinjuan
Xu, Linling
Wang, Bingjie
Rao, Lulin
Xu, Yanlei
Wang, Xinyi
Zhao, Huilin
Yu, Jingyi
Zhou, Ying
Yu, Fangyou
author_sort Guo, Yinjuan
collection PubMed
description Mupirocin, a topical antimicrobial agent, is an important component in the eradication of methicillin-resistant Staphylococcus aureus (MRSA) colonization. The molecular characteristics of 46 mupirocin-resistant MRSA (MR-MRSA) clinical isolates were analyzed by multilocus sequence typing (MLST), staphylococcal cassette chromosome mec element (SCCmec) typing, spa typing, and analysis of virulence genes. All 26 MRSA isolates with low-level mupirocin resistance possessed a V588F mutation in ileS. Among 20 MRSA isolates with high-level resistance to mupirocin, all carried mupA; 2 isolates also possessed the V588F mutation in ileS, and 1 possessed the V631F mutation in ileS (isoleucyl-tRNA synthetase). The majority of MR-MRSA isolates were resistant to erythromycin, clindamycin, tetracycline, ciprofloxacin, and gentamicin, but the rates of resistance to rifampin and fusidic acid were 8.7% and 6.5%, respectively. Eight sequence types (STs) were found among the 46 MR-MRSA isolates, of which ST764 was the most prevalent (76.1%). The most frequent spa type identified was t1084 (52.2%). The SCCmec type most frequently found was type II (80.4%). The most common clone among low-level MR-MRSA isolates was ST764-MRSA-SCCmec type II-t1084 (23 isolates), while ST764-MRSA-SCCmec type II-t002 (9 isolates) was the most common clone among high-level MR-MRSA isolates. Additionally, all toxin genes except the seb gene were not identified among ST764 isolates. Among clonal complex 5 (CC5) isolates, immune evasion cluster (IEC)-associated genes (chp, sak, and scn) and seb were present in ST764 but absent in ST5, while sec, sel1, tsst-1, and hlb genes were identified in ST5 but absent in ST764. In conclusion, the spread of CC5 clones, especially a novel ST764-MRSA-SCCmec type II-t1084 clone with high-level resistance to mupirocin, was responsible for the increase in mupirocin resistance. These findings indicated that the emergence of the ST764 MR-MRSA clone involves a therapeutic challenge for treating serious MRSA infections. IMPORTANCE Mupirocin, a topical antibiotic that is commonly used for the nasal decolonization of MRSA and methicillin-sensitive Staphylococcus aureus in hospital settings and nursing homes, was introduced as a highly effective antibiotic against MRSA. Mupirocin acts by competitively binding isoleucyl-tRNA synthetase, thereby disrupting protein synthesis. This drug shows bacteriostatic and bactericidal activity at low and high concentrations, respectively. However, with the increase in mupirocin use, low-level and high-level resistance during nasal mupirocin treatment has been reported. In a previous study, the proportion of MRSA strains with high-level mupirocin resistance in a Canadian hospital increased from 1.6% in the first 5 years of surveillance (1995 to 1999) to 7.0% (2000 to 2004).
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spelling pubmed-99272322023-02-15 Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China Guo, Yinjuan Xu, Linling Wang, Bingjie Rao, Lulin Xu, Yanlei Wang, Xinyi Zhao, Huilin Yu, Jingyi Zhou, Ying Yu, Fangyou Microbiol Spectr Research Article Mupirocin, a topical antimicrobial agent, is an important component in the eradication of methicillin-resistant Staphylococcus aureus (MRSA) colonization. The molecular characteristics of 46 mupirocin-resistant MRSA (MR-MRSA) clinical isolates were analyzed by multilocus sequence typing (MLST), staphylococcal cassette chromosome mec element (SCCmec) typing, spa typing, and analysis of virulence genes. All 26 MRSA isolates with low-level mupirocin resistance possessed a V588F mutation in ileS. Among 20 MRSA isolates with high-level resistance to mupirocin, all carried mupA; 2 isolates also possessed the V588F mutation in ileS, and 1 possessed the V631F mutation in ileS (isoleucyl-tRNA synthetase). The majority of MR-MRSA isolates were resistant to erythromycin, clindamycin, tetracycline, ciprofloxacin, and gentamicin, but the rates of resistance to rifampin and fusidic acid were 8.7% and 6.5%, respectively. Eight sequence types (STs) were found among the 46 MR-MRSA isolates, of which ST764 was the most prevalent (76.1%). The most frequent spa type identified was t1084 (52.2%). The SCCmec type most frequently found was type II (80.4%). The most common clone among low-level MR-MRSA isolates was ST764-MRSA-SCCmec type II-t1084 (23 isolates), while ST764-MRSA-SCCmec type II-t002 (9 isolates) was the most common clone among high-level MR-MRSA isolates. Additionally, all toxin genes except the seb gene were not identified among ST764 isolates. Among clonal complex 5 (CC5) isolates, immune evasion cluster (IEC)-associated genes (chp, sak, and scn) and seb were present in ST764 but absent in ST5, while sec, sel1, tsst-1, and hlb genes were identified in ST5 but absent in ST764. In conclusion, the spread of CC5 clones, especially a novel ST764-MRSA-SCCmec type II-t1084 clone with high-level resistance to mupirocin, was responsible for the increase in mupirocin resistance. These findings indicated that the emergence of the ST764 MR-MRSA clone involves a therapeutic challenge for treating serious MRSA infections. IMPORTANCE Mupirocin, a topical antibiotic that is commonly used for the nasal decolonization of MRSA and methicillin-sensitive Staphylococcus aureus in hospital settings and nursing homes, was introduced as a highly effective antibiotic against MRSA. Mupirocin acts by competitively binding isoleucyl-tRNA synthetase, thereby disrupting protein synthesis. This drug shows bacteriostatic and bactericidal activity at low and high concentrations, respectively. However, with the increase in mupirocin use, low-level and high-level resistance during nasal mupirocin treatment has been reported. In a previous study, the proportion of MRSA strains with high-level mupirocin resistance in a Canadian hospital increased from 1.6% in the first 5 years of surveillance (1995 to 1999) to 7.0% (2000 to 2004). American Society for Microbiology 2023-01-09 /pmc/articles/PMC9927232/ /pubmed/36622214 http://dx.doi.org/10.1128/spectrum.03794-22 Text en Copyright © 2023 Guo et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Guo, Yinjuan
Xu, Linling
Wang, Bingjie
Rao, Lulin
Xu, Yanlei
Wang, Xinyi
Zhao, Huilin
Yu, Jingyi
Zhou, Ying
Yu, Fangyou
Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China
title Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China
title_full Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China
title_fullStr Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China
title_full_unstemmed Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China
title_short Dissemination of Methicillin-Resistant Staphylococcus aureus Sequence Type 764 Isolates with Mupirocin Resistance in China
title_sort dissemination of methicillin-resistant staphylococcus aureus sequence type 764 isolates with mupirocin resistance in china
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927232/
https://www.ncbi.nlm.nih.gov/pubmed/36622214
http://dx.doi.org/10.1128/spectrum.03794-22
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