Authors:
Suna KızılyıldırımDepartment of Pharmaceutical Microbiology, Faculty of Pharmacy, University of Süleyman Demirel, 32260, Isparta, Turkey

Search for other papers by Suna Kızılyıldırım in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-1039-8556
,
Fatih KöksalDepartment of Medical Microbiology, Faculty of Medical, University of Çukurova, 01380, Adana, Turkey

Search for other papers by Fatih Köksal in
Current site
Google Scholar
PubMed
Close
, and
Cansu Önlen GüneriDepartment of Medical Microbiology, Gulhane Vocational School of Health Services, University of Sağlık Bilimleri, 06010, Ankara, Turkey

Search for other papers by Cansu Önlen Güneri in
Current site
Google Scholar
PubMed
Close
Restricted access

Abstract

Group A streptococci are important pathogens with various virulence factors, such as M protein, superantigens, hemolysins, deoxyribonuclease, and proteases. The aims of this study are to investigate the detection of emm genotypes and other virulence genes, such as SAgs, DNase, protease, antibiotic resistance, and phylogenetic relationships in GAS strains isolated from clinical samples.

Test strains were obtained from Çukurova University Balcalı Hospital and regional hospitals in Adana province. The M proteins were detected by sequence analysis of emm genes. SAgs and other virulence gene profiles were determined using the Multiplex-PCR method. The antibiotic susceptibility of the isolates was performed by the disc diffusion method and evaluated according to CLSI criteria. The PFGE method was used to determine the clonal relationship between the strains.

The emm gene was positive in 86 isolates. The most common emm genotypes were emm28 (22%), emm1 (18.6%), emm12 (13.9%), and emm3 (11.6%). Also, the most common virulence genes were speG (58.1%), speC (56.9%), sdaB (53.4%), and mac (53.4%). The rates of resistance to erythromycin, clindamycin, levofloxacin, ciprofloxacin and telithromycin were 19.8%, 16.3%, 4.7%, 3.5%, and 3.5%, respectively.

As a result, additional regional studies on the detection and prevalence of GAS virulence factors in Turkey are required. We believe that this study will provide valuable information for epidemiological studies on emm sequences, Sags, and other virulence factors of Streptococcus pyogenes in Turkey.

  • 1.

    Steer AC, Lamagni T, Curtis N, Carapetis JR. Invasive group a streptococcal disease: epidemiology, pathogenesis and management. Drugs 2012; 72(9): 12131227.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Cunningham MW. Pathogenesis of group a streptococcal infection. Clin Microbiol Rev 2000; 13(3): 470511.

  • 3.

    Hasegawa T, Torii K, Hashikawa S, Iinuma Y, Ohta M. Cloning and characterization of two novel DNases from Streptococcus pyogenes. Arch Microbiol 2002; 177: 451456.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Athey TB, Teatero S, Li A, Marchand-Austin A, Beall BW, Fittipaldi N. Deriving group a streptococcus typing ınformation from short-read whole-genome sequencing data. J Clin Microbiol 2014; 52(6): 18711876.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Pato C, Melo JC, Ramirez M. Friães A and the Portuguese Group for the Study of Streptococcal Infections. Streptococcus pyogenes causing skin and soft tissue ınfections are enriched in the recently emerged emm89 clade 3 and are not associated with abrogation of CovRS. Front Microbiol 2018; 9: 2372.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Ekelund K, Darenberg J, Teglund AN, Hoffmann S, Bang D, Skinhø P, et al. Variations in emm type among group a streptococcal isolates causing invasive or noninvasive infections in a nationwide study. J Clin Microbiol 2005; 43(7): 31013109.

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

    CDC (Centers for Disease and Prevention). Available from: https://www.cdc.gov/streplab/groupa-strep/emm-background.html.

  • 8.

    Khosravi AD, Ebrahimifard N, Shamsizadeh A, Shoja S. Isolation of Streptococcus pyogenes from children with pharyngitis and emm type analysis. J Chin Med Assoc 2016; 79: 276280.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Friães A, Pinto FR, Silva-Costa C, Ramirez M, Melo-Cristino J. Portuguese Group for the Study of Streptococcal Infections. Group a streptococci clones associated with invasive infections and pharyngitis in Portugal present differences in emm types, superantigen gene content and antimicrobial resistance. BMC Microbiol 2012; 12: 280.

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

    Imohl M, Fitzner C, Perniciaro S, Linden M. Epidemiologyand distribution of 10 superantigens among invasive Streptococcus pyogenes disease in Germany from 2009 to 2014. PLoS One 2017; 12(7): e0180757.

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

    Commons RJ, Smeesters PR, Proft T, Fraser JD, Robins-Browne R, Curtis N. Streptococcal superantigens: categorization and clinical associations. Trends Mol Med 2014; 20 (1): 4862.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Barnett TC, Cole JN, Hernandez TR, Henningham A, Paton JC, Nizet V, et al. Streptococcal toxins: role in pathogenesis and disease. Cell Microbiol 2015; 17(12): 17211741.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Dağı HT, Yüksekkaya Ş, Seyhan T, Fındık D, Tuncer İ, Arslan U. Investigation of Streptococcus pyogenes virulence factors and typing by multiple locus variable number tandem repeat fingerprinting (MLVF) method. Mikrobiyol Bul 2018; 52(3): 233246.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Otlu B, Karakur C, Bayındır Y, Kayabaş Ü, Yakupoğulları Y, Bağ HG. Carriage of Streptococcus pyogenes in primary school children: M-protein types, pyrogenic toxin genes, and ınvestigation of the clonal relationships between the ısolates. Mikrobiyol Bul 2015; 49(3): 301313.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    CDC (Centers for Disease and Prevention). Available from: https://www.cdc.gov/streplab/groupa-strep/emm-typing-protocol.html.

  • 16.

    Borek AL, Obszańska K, Hryniewicz W, Sitkiewicz I. Detection of Streptococcus pyogenes virulence factors by multiplex PCR. Virulence, Landes Biosci 2012; 3(6): 529533.

    • Search Google Scholar
    • Export Citation
  • 17.

    CDC (Centers for Disease and Prevention). Available from: https://www.cdc.gov/pulsenet/pdf/listeria-pfge-protocol-508c.pdf.

  • 18.

    Graves, LM, Swaminathan B. PulseNet standardized protocol for subtyping Listeria monocytogenes by macrorestriction and pulsed-field gel electrophoresis. Int J Food Microbiol 2001; 65(1–2): 5562.

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

    Karaky NM. Characterization of Streptococcus pyogenes ısolates from Lebanon: pathogenesis, epidemiology and resistance. Lebanese Amerıcan Unıversıty. A thesis Submitted in partial fulfillment of the requirements for the degree of Master of Science in Molecular Biology. Lebanon 2011. https://laur.lau.edu.lb:8443/xmlui/bitstream/handle/10725/5067/Nathalie_Mahmoud_Karaky_Thesis_Redacted.pdf?sequence=3.

    • Search Google Scholar
    • Export Citation
  • 20.

    Smit PW, Lindholm L, Lyytikainen O, Jalava J, Pätäri-Sampo A, Vuopio J. Epidemiology and emm types of invasive group a streptococcal infections in Finland, 2008-2013. Eur J Clin Microbiol Infect Dis 2015; 34(10): 21312136.

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

    Meisal R, Andreasson IKG, Hooiby EA, Aaberge IS, Michaelsen TE, Caugant DA. Streptococcus pyogenes ısolates causing severe ınfections in Norway in 2006 to 2007: emm types, multilocus sequence types, and superantigen profiles. J Clin Microbiol 2010; 48(3): 842851.

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

    Akça G. Determination of M types of group a beta hemolytic streptococci by 'emm' sequencing analyse. PhD thesis. Ankara, 2006. Available from: https://tez.yok.gov.tr/UlusalTezMerkezi/giris.jsp.

    • Search Google Scholar
    • Export Citation
  • 23.

    Çakmak AE. M protein (emm) gene typing of group a beta-hemolytic streptococci isolated from pharyngeal cultures of children with acute tonsillopharyngitis in Istanbul. Child Health and Diseases Specialization Thesis. Istanbul, 2009. Available from: http://nek.istanbul.edu.tr:4444/ekos/TEZ/45289.pdf.

    • Search Google Scholar
    • Export Citation
  • 24.

    Dundar D, Sayan M, Tamer GS. Macrolide and tetracycline resistance and emm type distribution of Streptococcus pyogenes isolates recovered from Turkish patients. Microb Drug Resist 2010; 16(4): 279284.

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

    Arslan U, Oryaşın E, Eskin Z, Dağı HT, Fındık D, Tuncer İ, et al. Distribution of emm genotypes and antibiotic susceptibility of Streptococcus pyogenes strains: analogy with the vaccine in development. Mikrobiyol Bul 2013; 47(2): 318323.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Strus M, Heczko PB, Golinska E, Tomusiak A, Chmielarczyk A, Dorycka M, et al. The virulence factors of group a streptococcus strains isolated from invasive and non-invasive infections in Polish and German centres, 2009–2011. Eur J Clin Microbiol Infect Dis 2017; 36(9): 16431649.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Friães A, Pinto FR, Silva-Costa C, Ramirez M, Melo-Cristino J. Superantigen gene complement of Streptococcus pyogenes relationship with other typing methods and short-term stability. Eur J Clin Microbiol Infect Dis 2013; 32(1): 115125.

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

    Mengeloğlu ZF. Evaluation of emm gene types, toxin gene profiles and clonal relatedness of group a streptococci obtained from patients and carriers. PhD thesis. Zonguldak, 2010. Available from: https://tez.yok.gov.tr/UlusalTezMerkezi/giris.jsp.

    • Search Google Scholar
    • Export Citation
  • 29.

    Karaky NM, Araj GF, Tokajian ST. Molecular characterization of Streptococcus pyogenes group a isolate from a tertiary hospital in Lebanon. J Med Microbiol 2014; 63(9): 11971204.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

 

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
Jun 2022 0 0 0
Jul 2022 0 0 0
Aug 2022 0 0 0
Sep 2022 0 0 0
Oct 2022 0 0 0
Nov 2022 379 2 2
Dec 2022 0 0 0