Recombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settings

Abstract Background Methicillin-resistant Staphylococcus aureus (MRSA) is a rapidly evolving pathogen that is frequently associated with outbreaks and sustained epidemics. This study investigated the population structure, resistome, virulome, and the correlation between antimicrobial resistance dete...

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Main Authors: Salma W. Elsayed, Reem A. Elghaish, Eman Badr, Shaimaa F. Mouftah, Nehal A. Saif, Iman S. Naga, Ahmed H. Shata, Ben Pascoe, Samuel K. Sheppard, Mohamed Elhadidy
Format: Article
Language:English
Published: BMC 2023-12-01
Series:Annals of Clinical Microbiology and Antimicrobials
Subjects:
Online Access:https://doi.org/10.1186/s12941-023-00659-y
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author Salma W. Elsayed
Reem A. Elghaish
Eman Badr
Shaimaa F. Mouftah
Nehal A. Saif
Iman S. Naga
Ahmed H. Shata
Ben Pascoe
Samuel K. Sheppard
Mohamed Elhadidy
author_facet Salma W. Elsayed
Reem A. Elghaish
Eman Badr
Shaimaa F. Mouftah
Nehal A. Saif
Iman S. Naga
Ahmed H. Shata
Ben Pascoe
Samuel K. Sheppard
Mohamed Elhadidy
author_sort Salma W. Elsayed
collection DOAJ
description Abstract Background Methicillin-resistant Staphylococcus aureus (MRSA) is a rapidly evolving pathogen that is frequently associated with outbreaks and sustained epidemics. This study investigated the population structure, resistome, virulome, and the correlation between antimicrobial resistance determinants with phenotypic resistance profiles of 36 representative hospital-acquired MRSA isolates recovered from hospital settings in Egypt. Results The community-acquired MRSA lineage, clonal complex 1 (CC1) was the most frequently detected clone, followed by three other globally disseminated clones, CC121, CC8, and CC22. Most isolates carried SCCmec type V and more than half of isolates demonstrated multi-drug resistant phenotypes. Resistance to linezolid, a last resort antibiotic for treating multidrug resistant MRSA, was observed in 11.11% of the isolates belonging to different genetic backgrounds. Virulome analysis indicated that most isolates harboured a large pool of virulence factors and toxins. Genes encoding aureolysin, gamma hemolysins, and serine proteases were the most frequently detected virulence encoding genes. CC1 was observed to have a high pool of AMR resistance determinants including cfr, qacA, and qacB genes, which are involved in linezolid and quaternary ammonium compounds resistance, as well as high content of virulence-related genes, including both of the PVL toxin genes. Molecular clock analysis revealed that CC1 had the greatest frequency of recombination (compared to mutation) among the four major clones, supporting the role of horizontal gene transfer in modulating AMR and hypervirulence in this clone. Conclusions This pilot study provided evidence on the dissemination success of CA-MRSA clone CC1 among Egyptian hospitals. Co-detection of multiple AMR and virulence genes in this lineage pose a broad public health risk, with implications for successful treatment. The results of this study, together with other surveillance studies in Egypt, should be used to develop strategies for controlling MRSA infections in Egyptian health-care settings.
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spelling doaj.art-45f663a8e8a84454bc4aa1b4c0b3f54d2023-12-17T12:09:30ZengBMCAnnals of Clinical Microbiology and Antimicrobials1476-07112023-12-0122111410.1186/s12941-023-00659-yRecombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settingsSalma W. Elsayed0Reem A. Elghaish1Eman Badr2Shaimaa F. Mouftah3Nehal A. Saif4Iman S. Naga5Ahmed H. Shata6Ben Pascoe7Samuel K. Sheppard8Mohamed Elhadidy9Center for Genomics, Helmy Institute for Medical Sciences, Zewail City of Science and TechnologyCenter for Genomics, Helmy Institute for Medical Sciences, Zewail City of Science and TechnologyBiomedical Sciences Program, University of Science and Technology, Zewail City of Science and TechnologyBiomedical Sciences Program, University of Science and Technology, Zewail City of Science and TechnologyCenter for Genomics, Helmy Institute for Medical Sciences, Zewail City of Science and TechnologyDepartment of Microbiology, Medical Research Institute, Alexandria UniversityCenter for Genomics, Helmy Institute for Medical Sciences, Zewail City of Science and TechnologyCentre for Genomic Pathogen Surveillance, Big Data Institute, University of OxfordIneos Oxford Institute, Department of Biology, University of OxfordCenter for Genomics, Helmy Institute for Medical Sciences, Zewail City of Science and TechnologyAbstract Background Methicillin-resistant Staphylococcus aureus (MRSA) is a rapidly evolving pathogen that is frequently associated with outbreaks and sustained epidemics. This study investigated the population structure, resistome, virulome, and the correlation between antimicrobial resistance determinants with phenotypic resistance profiles of 36 representative hospital-acquired MRSA isolates recovered from hospital settings in Egypt. Results The community-acquired MRSA lineage, clonal complex 1 (CC1) was the most frequently detected clone, followed by three other globally disseminated clones, CC121, CC8, and CC22. Most isolates carried SCCmec type V and more than half of isolates demonstrated multi-drug resistant phenotypes. Resistance to linezolid, a last resort antibiotic for treating multidrug resistant MRSA, was observed in 11.11% of the isolates belonging to different genetic backgrounds. Virulome analysis indicated that most isolates harboured a large pool of virulence factors and toxins. Genes encoding aureolysin, gamma hemolysins, and serine proteases were the most frequently detected virulence encoding genes. CC1 was observed to have a high pool of AMR resistance determinants including cfr, qacA, and qacB genes, which are involved in linezolid and quaternary ammonium compounds resistance, as well as high content of virulence-related genes, including both of the PVL toxin genes. Molecular clock analysis revealed that CC1 had the greatest frequency of recombination (compared to mutation) among the four major clones, supporting the role of horizontal gene transfer in modulating AMR and hypervirulence in this clone. Conclusions This pilot study provided evidence on the dissemination success of CA-MRSA clone CC1 among Egyptian hospitals. Co-detection of multiple AMR and virulence genes in this lineage pose a broad public health risk, with implications for successful treatment. The results of this study, together with other surveillance studies in Egypt, should be used to develop strategies for controlling MRSA infections in Egyptian health-care settings.https://doi.org/10.1186/s12941-023-00659-yMethicillin-resistant Staphylococcus aureus (MRSA)Hospital settingsAntimicrobial resistanceVirulenceRecombinationLinezolid resistance
spellingShingle Salma W. Elsayed
Reem A. Elghaish
Eman Badr
Shaimaa F. Mouftah
Nehal A. Saif
Iman S. Naga
Ahmed H. Shata
Ben Pascoe
Samuel K. Sheppard
Mohamed Elhadidy
Recombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settings
Annals of Clinical Microbiology and Antimicrobials
Methicillin-resistant Staphylococcus aureus (MRSA)
Hospital settings
Antimicrobial resistance
Virulence
Recombination
Linezolid resistance
title Recombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settings
title_full Recombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settings
title_fullStr Recombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settings
title_full_unstemmed Recombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settings
title_short Recombination-mediated dissemination of Methicillin-resistant S. aureus clonal complex 1 in the Egyptian health care settings
title_sort recombination mediated dissemination of methicillin resistant s aureus clonal complex 1 in the egyptian health care settings
topic Methicillin-resistant Staphylococcus aureus (MRSA)
Hospital settings
Antimicrobial resistance
Virulence
Recombination
Linezolid resistance
url https://doi.org/10.1186/s12941-023-00659-y
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