View More View Less
  • 1 Department of Medical Microbiology, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria
  • | 2 Department of Genetics, Sofia University “St. Kliment Ohridski”, Sofia, Bulgaria
  • | 3 Department of Medical Chemistry and Biochemistry, Molecular Medicine Center, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria
  • | 4 Department of Microbiology, Military Epidemiology and Hygiene, Military Medical Academy, Sofia, Bulgaria
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, 175192, 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): 2734, 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): 507518. https://doi.org/10.1080/22221751.2022.2031310.

    • 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): 97100. 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): 283288.

  • 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: 19041911.

    • 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: 8592.

    • 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: 29122917.

    • 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.

    • 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): 1719.

    • 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): 15341536. 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): 176180, 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

 

The author instruction is available in PDF.
Please, download the file from HERE

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. Zsuzsanna SCHAFF (2nd Department of Pathology, 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.)

 

Editorial Office:
Akadémiai Kiadó Zrt.
Budafoki út 187-187, A/3, H-1117 Budapest, Hungary

Editorial Correspondence:
Acta Microbiologica et Immunologica Hungarica
Institute of Medical Microbiology
Semmelweis University
P.O. Box 370
H-1445 Budapest, Hungary
Phone: + 36 1 459 1500 ext. 56101
Fax: (36 1) 210 2959
E-mail: amih@med.semmelweis-univ.hu

 Indexing and Abstracting Services:

  • Biological Abstracts
  • BIOSIS Previews
  • CAB Abstracts
  • Chemical Abstracts
  • Global Health
  • Index Medicus
  • Index Veterinarius
  • Medline
  • Referativnyi Zhurnal
  • SCOPUS
  • Science Citation Index Expanded

2021  
Web of Science  
Total Cites
WoS
696
Journal Impact Factor 2,298
Rank by Impact Factor Immunology 141/161
Microbiology 118/136
Impact Factor
without
Journal Self Cites
2,143
5 Year
Impact Factor
1,925
Journal Citation Indicator 0,39
Rank by Journal Citation Indicator Immunology 146/177
Microbiology 129/157
Scimago  
Scimago
H-index
29
Scimago
Journal Rank
0,362
Scimago Quartile Score Immunology and Microbiology (miscellaneous) (Q3)
Medicine (miscellaneous) (Q3)
Scopus  
Scopus
Cite Score
3,6
Scopus
CIte Score Rank
General Immunology and Microbiology 26/56 (Q2)
Infectious Diseases 149/295 (Q3)
Microbiology (medical) 66/118 (Q3)
Scopus
SNIP
0,598

2020  
Total Cites 662
WoS
Journal
Impact Factor
2,048
Rank by Immunology 145/162(Q4)
Impact Factor Microbiology 118/137 (Q4)
Impact Factor 1,904
without
Journal Self Cites
5 Year 0,671
Impact Factor
Journal  0,38
Citation Indicator  
Rank by Journal  Immunology 146/174 (Q4)
Citation Indicator  Microbiology 120/142 (Q4)
Citable 42
Items
Total 40
Articles
Total 2
Reviews
Scimago 28
H-index
Scimago 0,439
Journal Rank
Scimago Immunology and Microbiology (miscellaneous) Q4
Quartile Score Medicine (miscellaneous) Q3
Scopus 438/167=2,6
Scite Score  
Scopus General Immunology and Microbiology 31/45 (Q3)
Scite Score Rank  
Scopus 0,760
SNIP
Days from  225
submission
to acceptance
Days from  118
acceptance
to publication
Acceptance 19%
Rate

2019  
Total Cites
WoS
485
Impact Factor 1,086
Impact Factor
without
Journal Self Cites
0,864
5 Year
Impact Factor
1,233
Immediacy
Index
0,286
Citable
Items
42
Total
Articles
40
Total
Reviews
2
Cited
Half-Life
5,8
Citing
Half-Life
7,7
Eigenfactor
Score
0,00059
Article Influence
Score
0,246
% Articles
in
Citable Items
95,24
Normalized
Eigenfactor
0,07317
Average
IF
Percentile
7,690
Scimago
H-index
27
Scimago
Journal Rank
0,352
Scopus
Scite Score
320/161=2
Scopus
Scite Score Rank
General Immunology and Microbiology 35/45 (Q4)
Scopus
SNIP
0,492
Acceptance
Rate
16%

 

Acta Microbiologica et Immunologica Hungarica
Publication Model Online only Hybrid
Submission Fee none
Article Processing Charge 1100 EUR/article
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription fee 2022 Online subsscription: 662 EUR / 832 USD
Print + online subscription: 740 EUR / 930 USD
Subscription fee 2023 Online subsscription: 680 EUR / 832 USD
Print + online subscription: 760 EUR / 930 USD
Subscription Information Online subscribers are entitled access to all back issues published by Akadémiai Kiadó for each title for the duration of the subscription, as well as Online First content for the subscribed content.
Purchase per Title Individual articles are sold on the displayed price.

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)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Jan 2022 0 0 0
Feb 2022 0 0 0
Mar 2022 0 0 0
Apr 2022 0 0 0
May 2022 0 0 0
Jun 2022 101 6 6
Jul 2022 14 1 2