Whole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in Tanzania

Abstract Background The emergence of multidrug-resistant termed Methicillin-resistant Staphylococcus aureus (MRSA) strain, driven by the acquisition of resistance gene mecA imposes a substantial challenge in the treatment and control of their related infections. Although quinolones have historically...

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Main Authors: Masoud A. Juma, Happiness Kumburu, Boaz Wadugu, Davis Kuchaka, Mariana Shayo, Patrick Kimu, Livin E. Kanje, Melkiory Beti, Marco van Zwetselaar, Blandina Mmbaga, Tolbert Sonda
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Language:English
Published: BMC 2024-11-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-024-11045-z
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author Masoud A. Juma
Happiness Kumburu
Boaz Wadugu
Davis Kuchaka
Mariana Shayo
Patrick Kimu
Livin E. Kanje
Melkiory Beti
Marco van Zwetselaar
Blandina Mmbaga
Tolbert Sonda
author_facet Masoud A. Juma
Happiness Kumburu
Boaz Wadugu
Davis Kuchaka
Mariana Shayo
Patrick Kimu
Livin E. Kanje
Melkiory Beti
Marco van Zwetselaar
Blandina Mmbaga
Tolbert Sonda
author_sort Masoud A. Juma
collection DOAJ
description Abstract Background The emergence of multidrug-resistant termed Methicillin-resistant Staphylococcus aureus (MRSA) strain, driven by the acquisition of resistance gene mecA imposes a substantial challenge in the treatment and control of their related infections. Although quinolones have historically been effective against both MRSA and methicillin-susceptible S. aureus (MSSA) strains, the rising resistance to quinolones among S. aureus isolates, particularly in MRSA, has severely curtailed their potency and further narrowed down the therapeutic options. This study aimed to determine the burden of MRSA among isolates, as well as their resistance profile, genotypic characterization, and molecular relatedness through the construction of a phylogenetic tree. Materials and methods Archived clinical S. aureus isolates from a descriptive, cross-sectional study involving six regional referral hospitals in Dodoma, Songea, Kigoma, Kitete, and Morogoro in the mainland Tanzania and Mnazi Mmoja in Zanzibar were analyzed. Bacterial identification was performed using both classical microbiology and whole genome sequencing on Illumina Nextseq 550 Sequencer. Species identification was done using KmerFinder 3.2, Multilocus Sequence Typing using MLST 2.0, SCCmec typing using SCCmecFinder 1.2, resistance genes using ResFinder 4.1, and phylogenetic relatedness using CSI Phylogeny 1.4. Results Out of the 140 isolates analyzed, 69 (49.3%) were identified as MRSA, with 57 (82.6%) exhibiting quinolone resistance. Conversely, 71 isolates were identified as MSSA, and none of them exhibited resistance to quinolones. Spa-typing revealed six spa types, with t355, t1476, and t498 being the most common. Moreover, all (69) MRSA were found to carry SCCmec type IV. The isolates exhibited 14 different sequence types (STs). Notably, ST152 was prevalent among MSSA (50 isolates, 70%), while ST8 was the predominant sequence type among MRSA (58 isolates, 84%). The antimicrobial resistance profile revealed at least three horizontally acquired resistance genes, with blaZ, dfrG, tet(K), and aac (6’)-aph (2’’) genes being highly prevalent. Conclusion There is a high genetic diversity among the S. aureus isolates existing in Tanzania regional hospitals, with a concerning burden of quinolone resistance among MRSA isolates. The diversity in resistance genes among MRSA lineages emphasizes the necessity for the development of sustainable antimicrobial stewardship and surveillance to support evidence-based guidelines for managing and controlling MRSA infections in both community and hospital settings.
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spelling doaj-art-d0f6945aa3ff4e83918647477da91ec92025-08-20T02:22:33ZengBMCBMC Genomics1471-21642024-11-0125111010.1186/s12864-024-11045-zWhole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in TanzaniaMasoud A. Juma0Happiness Kumburu1Boaz Wadugu2Davis Kuchaka3Mariana Shayo4Patrick Kimu5Livin E. Kanje6Melkiory Beti7Marco van Zwetselaar8Blandina Mmbaga9Tolbert Sonda10Kilimanjaro Christian Medical University College (KCMUCo)Kilimanjaro Christian Medical University College (KCMUCo)Kilimanjaro Christian Medical University College (KCMUCo)Kilimanjaro Clinical Research InstituteKilimanjaro Christian Medical University College (KCMUCo)Kilimanjaro Clinical Research InstituteKilimanjaro Christian Medical University College (KCMUCo)Kilimanjaro Clinical Research InstituteKilimanjaro Clinical Research InstituteKilimanjaro Christian Medical University College (KCMUCo)Kilimanjaro Christian Medical University College (KCMUCo)Abstract Background The emergence of multidrug-resistant termed Methicillin-resistant Staphylococcus aureus (MRSA) strain, driven by the acquisition of resistance gene mecA imposes a substantial challenge in the treatment and control of their related infections. Although quinolones have historically been effective against both MRSA and methicillin-susceptible S. aureus (MSSA) strains, the rising resistance to quinolones among S. aureus isolates, particularly in MRSA, has severely curtailed their potency and further narrowed down the therapeutic options. This study aimed to determine the burden of MRSA among isolates, as well as their resistance profile, genotypic characterization, and molecular relatedness through the construction of a phylogenetic tree. Materials and methods Archived clinical S. aureus isolates from a descriptive, cross-sectional study involving six regional referral hospitals in Dodoma, Songea, Kigoma, Kitete, and Morogoro in the mainland Tanzania and Mnazi Mmoja in Zanzibar were analyzed. Bacterial identification was performed using both classical microbiology and whole genome sequencing on Illumina Nextseq 550 Sequencer. Species identification was done using KmerFinder 3.2, Multilocus Sequence Typing using MLST 2.0, SCCmec typing using SCCmecFinder 1.2, resistance genes using ResFinder 4.1, and phylogenetic relatedness using CSI Phylogeny 1.4. Results Out of the 140 isolates analyzed, 69 (49.3%) were identified as MRSA, with 57 (82.6%) exhibiting quinolone resistance. Conversely, 71 isolates were identified as MSSA, and none of them exhibited resistance to quinolones. Spa-typing revealed six spa types, with t355, t1476, and t498 being the most common. Moreover, all (69) MRSA were found to carry SCCmec type IV. The isolates exhibited 14 different sequence types (STs). Notably, ST152 was prevalent among MSSA (50 isolates, 70%), while ST8 was the predominant sequence type among MRSA (58 isolates, 84%). The antimicrobial resistance profile revealed at least three horizontally acquired resistance genes, with blaZ, dfrG, tet(K), and aac (6’)-aph (2’’) genes being highly prevalent. Conclusion There is a high genetic diversity among the S. aureus isolates existing in Tanzania regional hospitals, with a concerning burden of quinolone resistance among MRSA isolates. The diversity in resistance genes among MRSA lineages emphasizes the necessity for the development of sustainable antimicrobial stewardship and surveillance to support evidence-based guidelines for managing and controlling MRSA infections in both community and hospital settings.https://doi.org/10.1186/s12864-024-11045-zStaphylococcus Cassette chromosome mec (SCCmec)Sequence type (ST)Staphylococcal protein A (spa)Methicillin-resistant S. Aureus (MRSA)
spellingShingle Masoud A. Juma
Happiness Kumburu
Boaz Wadugu
Davis Kuchaka
Mariana Shayo
Patrick Kimu
Livin E. Kanje
Melkiory Beti
Marco van Zwetselaar
Blandina Mmbaga
Tolbert Sonda
Whole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in Tanzania
BMC Genomics
Staphylococcus Cassette chromosome mec (SCCmec)
Sequence type (ST)
Staphylococcal protein A (spa)
Methicillin-resistant S. Aureus (MRSA)
title Whole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in Tanzania
title_full Whole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in Tanzania
title_fullStr Whole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in Tanzania
title_full_unstemmed Whole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in Tanzania
title_short Whole genome sequencing-based characterization and determination of quinolone resistance among methicillin-resistant and methicillin-susceptible S. Aureus isolates from patients attending regional referral hospitals in Tanzania
title_sort whole genome sequencing based characterization and determination of quinolone resistance among methicillin resistant and methicillin susceptible s aureus isolates from patients attending regional referral hospitals in tanzania
topic Staphylococcus Cassette chromosome mec (SCCmec)
Sequence type (ST)
Staphylococcal protein A (spa)
Methicillin-resistant S. Aureus (MRSA)
url https://doi.org/10.1186/s12864-024-11045-z
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