Acta Microbiologica et Immunologica Hungarica
Volume/Issue:
Volume 69: Issue 3
Molecular epidemiology, virulence and antimicrobial resistance of Bulgarian methicillin resistant Staphylococcus aureus isolates
Authors:
Raina Gergova Department of Medical Microbiology, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

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https://orcid.org/0000-0003-3605-6447
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Virna-Maria Tsitou Department of Medical Microbiology, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

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Svetoslav G. Dimov Department of Genetics, Sofia University “St. Kliment Ohridski”, Sofia, Bulgaria

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Lyudmila Boyanova Department of Medical Microbiology, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

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Kalina Mihova Department of Medical Chemistry and Biochemistry, Molecular Medicine Center, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

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Tanya Strateva Department of Medical Microbiology, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

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Ivanka Gergova Department of Microbiology, Military Epidemiology and Hygiene, Military Medical Academy, Sofia, Bulgaria

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Rumyana Markovska Department of Medical Microbiology, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

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Pages:
193–200
Online Publication Date:
21 Jun 2022
Publication Date:
16 Sep 2022
Article Category:
Research Article
DOI:
https://doi.org/10.1556/030.2022.01766
Keywords:
MRSA; RAPD; MLST; virulence; clonal complexes
Restricted access

Abstract

Background

Severe infections of virulent methicillin-resistant Staphylococcus aureus (MRSA) are a serious health problem. The present study aimed to investigate clonal spread, virulence and antimicrobial resistance rates of Bulgarian MRSA isolates in 2016–2020.

Methods

Molecular identification and mecA gene detection were performed with PCR. Clonal relatedness was evaluated by RAPD PCR and MLST. MRSA epidemiology, virulence and resistance patterns were investigated by PCR.

Results

All 27 isolates were identified as S. aureus and were mecA positive, and all were susceptible to linezolid, tigecycline and vancomycin. The toxin genes hlg (in 92.6% of isolates), seb (77.8%), sei (77.8%), seh (59.3%), sej (55.6%), and seg (48.1%), were frequently found among the isolates. Epidemiological typing by RAPD identified 4 clones (16 isolates) and 11 were with a unique profile. MLST analysis of the same MRSA isolates showed five MLST clonal complexes and 11 ST types, including CC5 (33.3%) (ST5, ST221, ST4776), CC8 (22.2%) (ST8, ST239, ST72), CC15 (ST582), CC22 (14.8%) (ST217, ST5417), CC30 (ST30) CC398 (ST398), and CC59 (ST59). The isolates from CC5 showed higher virulence potential and almost all were macrolide resistant (ermB or ermC positive). CC8 isolates showed higher level of resistance.

Conclusion

To the best of our knowledge, this study is the first describing the clonal spreading of Bulgarian MRSA and the association with their virulence and resistance determinants. Monitoring of MRSA epidemiology, resistance and virulence profile can lead to better prevention and faster therapeutic choice in cases of severe infections.

  • 1.

    Wang X, Liu Q, Zhang H, Li X, Huang W, Fu Q, et al. Molecular characteristics of community-associated Staphylococcus aureus isolates from pediatric patients with bloodstream infections between 2012 and 2017 in Shanghai, China. Front Microbiol 2018 Jun 6; 9: 1211. https://doi.org/10.3389/fmicb.2018.01211.

    • Search Google Scholar
    • Export Citation
  • 2.

    Asgeirsson H, Thalme A, Weiland O. Staphylococcus aureus bacteraemia and endocarditis – epidemiology and outcome: a review. Infect Dis 2018; 50: 3, 175–192, https://doi.org/10.1080/23744235.2017.1392039.

    • Search Google Scholar
    • Export Citation
  • 3.

    Khoshnood SF, Shahi N, Jomehzadeh EA, Montazeri M, Saki SM, Maghsoumi-Norouzabad ML. Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among methicillin-resistant Staphylocoссus aureus strains isolated from burn patients. Acta Microbiol Immunol Hung 2019; 66(3): 387-398. https://doi.org/10.1556/030.66.2019.015.

    • Search Google Scholar
    • Export Citation
  • 4.

    Orosz L, Lengyel G, Ánosi N, Lakatos L, Burián K. Changes in resistance pattern of ESKAPE pathogens between 2010 and 2020 in the clinical center of University of Szeged, Hungary. Acta Microbiol Immunol Hung 2022; 69(1): 27–34, https://doi.org/10.1556/030.2022.01640.

    • Search Google Scholar
    • Export Citation
  • 5.

    European Centre for Disease Prevention and Control. Surveillance of antimicrobial resistance in Europe, 2020 Data available at: http:///www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-resistance-europe-2020.

    • Search Google Scholar
    • Export Citation
  • 6.

    Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 2021; 12(1): 547-569, https://doi.org/10.1080/21505594.2021.1878688.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Gergova RT, Tsitou VS, Gergova II, Muhtarova AA, Mitov IG. Correlation of methicillin resistance and virulence genes of Staphylococcus aureus with infection types and mode of acquisition in Sofia, Bulgaria. Afr J Clin Exper Microbiol 2019; 20(4): 280-288. https://dx.doi.org/10.4314/ajcem.v20i4.3.

    • Search Google Scholar
    • Export Citation
  • 8.

    Syed MA, Jamil B, Ramadan H, Rukan M, Ali S, Abbasi SA, et al. Genetic diversity of Staphylococcus aureus strains from a tertiary care hospital in Rawalpindi, Pakistan. Microorg 2021; 9. https://doi.org/10.3390/microorganisms9112301.

    • Search Google Scholar
    • Export Citation
  • 9.

    Wang X, Zhao H, Wang B, Zhou Y, Xu Y, Rao L, et al. Identification of methicillin-resistant Staphylococcus aureus ST8 isolates in China with potential high virulence. Emerg Microbes Infect 2022 Dec; 11(1): 507–518. https://doi.org/10.1080/22221751.2022.2031310.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Silva V, Ribeiro J, Rocha J, Manaia CM, Silva A, Pereira JE, et al. High frequency of the EMRSA-15 clone (ST22-MRSA-IV) in hospital wastewater. Microorganisms 2022; 10: 147. https://doi.org/10.3390/microorganisms10010147.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    European Committee on Antimicrobial Susceptibility Testing. Clinical breakpoint tables – bacteria. Version 11.0 2021; http://www.eucast.org.

    • Search Google Scholar
    • Export Citation
  • 12.

    Cantekin Z, Ergun Y, Solmaz Özmen H, Demir M, Saidi R. PCR assay with host specific internal control for Staphylococcus aureus from bovine milk samples. Mac Vet Rev 2015; 38(1): 97–100. https://doi.org/10.14432/j.macvetrev.2015.01.038.

    • Search Google Scholar
    • Export Citation
  • 13.

    Tsitou V-M, Mitov I, Gergova R. Relationship between MLSB resistance and the prevalent virulence genotypes among Bulgarian Staphylocoссus aureus. Acta Microbiologica et Immunologica Hungarica 2021; 68(1): 55-61. https://doi.org/10.1556/030.2020.01218.

    • Search Google Scholar
    • Export Citation
  • 14.

    Yoon JM. Genetic distances of Paralichthys olivaceus populations investigated by PCR. Dev Reprod 2018; 22(3): 283–288.

  • 17.

    Aung MS, San T, Urushibara N, San N, Hlaing MS, Pan ES, et al. Diversity and molecular characteristics of methicillin-susceptible and resistant Staphylococcus aureus from pediatric patients in Myanmar 2021. Microb Drug Resist 2022; 191-198. https://doi.org/10.1089/mdr.2021.0051.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Gu F, He W, Xiao S, Wang S, Li X, Zeng Q, et al. Antimicrobial resistance and molecular epidemiology of Staphylococcus aureus causing bloodstream infections at Ruijin hospital in Shanghai from 2013 to 2018. Sci Rep 2020; 10(6019). https://doi.org/10.1038/s41598-020-63248-5.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Coombs GW, Pearson JC, O'Brien FG, Murray RJ, Grubb WB, Christiansen KJ, et al. Methicillin-resistant Staphylocoссus aureus clones. Western Australia Emerg Infect Dis 2006; 12(2): 241. www.cdc.gov/eid.

    • Search Google Scholar
    • Export Citation
  • 20.

    Monecke S, Coombs G, Shore AC et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE 2011; 6(4): e17936. https://doi.org/10.1371/journal.pone.0017936.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Christianson S, Golding GR, Campbell J, Mulvey M, Boyd D, Bryce E, et al.(the Canadian nosocomial infection surveillance program). Comparative genomics of canadian epidemic lineages of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2007; 45: 1904–1911.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Monecke S, Syed MA, Khan MA. Genotyping of methicillin-resistant Staphylococcus aureus from sepsis patients in Pakistan and detection of antibodies against staphylococcal virulence factors. Eur J Clin Microbiol Infect Dis 2020; 39: 85–92.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Aires-de-Sousa M, Correia B, de Lencastre H. Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol 2008; 46: 2912–2917.

    • Search Google Scholar
    • Export Citation
  • 24.

    Liu Y, Zhang J, Zhong D, Ji L, Yang J, Phillips J, et al. Characterization of Staphylocoссusaureus isolates from pediatric patients with cystic fibrosis. World J Microbiol Biotechnol 2016; (32): 162.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Aman MJ, Adhikari RP. Staphylococcal bicomponent pore-forming toxins: targets for prophylaxis and immunotherapy. Toxins 2014; 6: 950-972.

  • 26.

    Nashev D. Characterization of methicillin-resistant Staphylococcus aureus isolated in Bulgarian hospitals, 2005–2011. The APUA Newsl 2013; 31(3): 17–19.

    • Search Google Scholar
    • Export Citation
  • 27.

    Drougka E, Foka A, Liakopoulos A, Doudoulakakis A, Jelastopulu E, Chini V, et al. A 12-year survey of methicillin-resistant Staphylococcus aureus infections in Greece: ST80-IV epidemic? Clin Microbiol Infect 2014; 20(11): O796-O803. https://doi.org/10.1111/1469-0691.12624.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Asanin J, Misic D, Aksentijevic K, Tambur Z, Rakonjac B, Kovacevic I, et al. Genetic profiling and comparison of human and animal methicillin-resistant Staphylococcus aureus (MRSA) isolates from Serbia. Antibiotics (Basel) 2019; 16;8(1): 26. https://doi.org/10.3390/antibiotics8010026.

    • Search Google Scholar
    • Export Citation
  • 29.

    Alp E , Klaassen CH, Doganay M , Altoparlak U, Aydin K, Engin A, et al. MRSA genotypes in Turkey: persistence over 10 years of a single clone of ST239. J Infect 2009; 58: 433-438.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Güngör S, Karagöz A, Koçak N, Arslantaş T. Methicillin-resistant Staphylococcus aureus in a Turkish hospital: characterization of clonal types and antibiotic susceptibility. J Infect Dev Ctries 2021; 15(12): 1854-1860. https://doi.org/10.3855/jidc.14963.

    • Search Google Scholar
    • Export Citation
  • 31.

    Sapugahawatte DN, Li C, Yeoh YK, Dharmaratne P, Zhu C, Ip M. Swine methicillin-resistant Staphylococcus aureus carrying toxic-shock syndrome toxin gene in Hong Kong, China. Emerg Microbes Infect 2020; 9(1): 1534–1536. https://doi.org/10.1080/22221751.2020.1785335.

    • Search Google Scholar
    • Export Citation
  • 32.

    Doudoulakakis A, Spiliopoulou I, Giormezis N, Syridou G, Nika A, Bozavoutoglou E, et al. Methicillin-resistant Staphylococcus aureus transmission and hospital-acquired bacteremia in a neonatal intensive care unit in Greece, J Infect Chemother 2022; 28(2): 176–180, https://doi.org/10.1016/j.jiac.2021.07.013.

    • Search Google Scholar
    • Export Citation
  • 33.

    Goudarzi M, Razeghi M, SalimiChirani A, Fazeli M, Tayebi Z, Pouriran R. Characteristics of methicillin-resistant Staphylococcus aureus carrying the toxic shock syndrome toxin gene: high prevalence of clonal complex 22 strains and the emergence of new spa types t223 and t605 in Iran. New Microbes and New Infections 2020; 36: 100695. https://doi.org/10.1016/j.nmni.2020.100695.

    • PubMed
    • Search Google Scholar
    • Export Citation
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Cover Acta Microbiologica et Immunologica Hungarica
Acta Microbiologica et Immunologica Hungarica A Quarterly of the Hungarian Academy of Sciences
Print ISSN:
1217-8950
Online ISSN:
1588-2640

Senior editors

Editor-in-Chief: Prof. Dóra Szabó (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Managing Editor: Dr. Béla Kocsis (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Co-editor: Dr. Andrea Horváth (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Editorial Board

  • Prof. Éva ÁDÁM (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Sebastian AMYES (Department of Medical Microbiology, University of Edinburgh, Edinburgh, UK.)
  • Dr. Katalin BURIÁN (Institute of Clinical Microbiology University of Szeged, Szeged, Hungary; Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary.)
  • Dr. Orsolya DOBAY (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Ildikó Rita DUNAY (Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-von-Guericke University, Magdeburg, Germany; Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany)
  • Prof. Levente EMŐDY(Department of Medical Microbiology and Immunology, University of Pécs, Pécs, Hungary.)
  • Prof. Anna ERDEI (Department of Immunology, Eötvös Loránd University, Budapest, Hungary, MTA-ELTE Immunology Research Group, Eötvös Loránd University, Budapest, Hungary.)
  • Prof. Éva Mária FENYŐ (Division of Medical Microbiology, University of Lund, Lund, Sweden)
  • Prof. László FODOR (Department of Microbiology and Infectious Diseases, University of Veterinary Medicine, Budapest, Hungary)
  • Prof. József KÓNYA (Department of Medical Microbiology, University of Debrecen, Debrecen, Hungary)
  • Prof. Yvette MÁNDI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Károly MÁRIALIGETI (Department of Microbiology, Eötvös Loránd University, Budapest, Hungary)
  • Prof. János MINÁROVITS (Department of Oral Biology and Experimental Dental Research, University of Szeged, Szeged, Hungary)
  • Prof. Béla NAGY (Centre for Agricultural Research, Institute for Veterinary Medical Research, Budapest, Hungary.)
  • Prof. István NÁSZ (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Kristóf NÉKÁM (Hospital of the Hospitaller Brothers in Buda, Budapest, Hungary.)
  • Dr. Eszter OSTORHÁZI (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Rozália PUSZTAI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Peter L. RÁDY (Department of Dermatology, University of Texas, Houston, Texas, USA)
  • Prof. Éva RAJNAVÖLGYI (Department of Immunology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary)
  • Prof. Ferenc ROZGONYI (Institute of Laboratory Medicine, Semmelweis University, Budapest, Hungary)
  • Prof. Joseph G. SINKOVICS (The Cancer Institute, St. Joseph’s Hospital, Tampa, Florida, USA)
  • Prof. Júlia SZEKERES (Department of Medical Biology, University of Pécs, Pécs, Hungary.)
  • Prof. Mária TAKÁCS (National Reference Laboratory for Viral Zoonoses, National Public Health Center, Budapest, Hungary.)
  • Prof. Edit URBÁN (Department of Medical Microbiology and Immunology University of Pécs, Pécs, Hungary; Institute of Translational Medicine, University of Pécs, Pécs, Hungary.)

 

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Acta Microbiologica et Immunologica Hungarica
Language English
Size A4
Year of
Foundation		 1954
Volumes
per Year		 1
Issues
per Year		 4
Founder Magyar Tudományos Akadémia
Founder's
Address		 H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address		 H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher		 Chief Executive Officer, Akadémiai Kiadó
ISSN 1217-8950 (Print)
ISSN 1588-2640 (Online)

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