Authors:
Zahra Rahmani Infectious Diseases and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Department of Otorhinolaryngology, Loghman Hospital, Shahid-Beheshti University of Medical Sciences, Tehran, Iran

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Sareh Sadat Hosseini Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

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Parmida Bagheri Department of Biotechnology, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, Tehran, Iran

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Mehdi Goudarzi Infectious Diseases and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

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https://orcid.org/0000-0001-6720-9341
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Abstract

Increase in antibiotic resistance in Staphylococcus aureus isolated from ear infection is a serious public health problem. The objective of this investigation was to determine the antibacterial resistance profile and genetic variability of the S. aureus isolated from adult patients with otitis externa (OE) and otitis media (OM) infections, Tehran- Iran. The disk diffusion was employed to detect the susceptibility of 45 S. aureus strains. Biofilm production was evaluated by microtiter plate assay. Genetic diversity of the isolates was determined by staphylococcal cassette SCCmec, spa, and MLST techniques. Resistance to mupirocin and vancomycin were identified in 40 and 2.2% of isolates. Out of the 45 S. aureus isolates, 41 (91.2%) strains were considered as positive biofilm strains at different levels. According to our results, S. aureus isolated from OM (44.4%, 20/45) were including CC8/ST239-SCCmecIII corresponded to spa types t860, t030, t037, t234, t421 (70%, 14/20) and CC/ST30-SCCmecIV corresponded to spa types t605 and t019 (30%, 6/20) while S. aureus isolated from OE (55.6%, 25/45) were including CC/ST30-SCCmecIV corresponded to spa types t605, t345 and t1130 (52%, 13/25), CC/ST22-SCCmecIV corresponded to spa type t790 (20%, 5/25), CC8/ST8-SCCmecIV corresponded to spa type t008 (16%, 4/25), and CC/ST45-SCCmecIV corresponded to spa types t004 and t038 (12%, 3/25). This study highlighted genetic variability and strong biofilm formation ability among our isolates revealing its crucial role in enhancing the resistance of this bacteria to drugs. Thus, it is necessary to continue the epidemiological analysis to improve the control of ear infections related to S. aureus.

  • 1.

    Cheung GY, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 2021; 12: 547569. https://doi.org/10.1080/21505594.2021.1878688.

    • Search Google Scholar
    • Export Citation
  • 2.

    Duarte MJ, Kozin ED, Bispo PJ, Mitchell AH, Gilmore MS, Remenschneider AK. Methicillin-resistant Staphylococcus aureus in acute otitis externa. World J Otorhinolaryngol Head Neck Surg 2017; 4: 246252. https://doi.org/10.1016/j.wjorl.2017.09.003.

    • Search Google Scholar
    • Export Citation
  • 3.

    Kiakojuri K, Armaki MT, Rajabnia R, Pournajaf A, Karami M, Khademian A, et al. Outer ear infections in Iran: a review. Open Access Maced J Med Sci 2019; 7: 1233. https://doi.org/10.3889/oamjms.2019.176.

    • Search Google Scholar
    • Export Citation
  • 4.

    Chen Q, Xie S, Lou X, Cheng S, Liu X, Zheng W, et al. Biofilm formation and prevalence of adhesion genes among Staphylococcus aureus isolates from different food sources. Microbiologyopen 2020; 9: e00946. https://doi.org/10.1002/mbo3.946.

    • Search Google Scholar
    • Export Citation
  • 5.

    Goudarzi M, Bahramian M, Tabrizi MS, Udo EE, Figueiredo AMS, Fazeli M, et al. Genetic diversity of methicillin resistant Staphylococcus aureus strains isolated from burn patients in Iran: ST239-SCCmec III/t037 emerges as the major clone. Microb Pathog 2017; 105: 17. https://doi.org/10.1016/j.micpath.2017.02.004.

    • Search Google Scholar
    • Export Citation
  • 6.

    Neopane P, Nepal HP, Shrestha R, Uehara O, Abiko Y. In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance. Int J Gen Med 2018; 11: 2532. https://doi: 10.2147/IJGM.S153268. eCollection 2018.

    • Search Google Scholar
    • Export Citation
  • 7.

    Wurster JI, Bispo PJ, Van Tyne D, Cadorette JJ, Boody R, Gilmore MS. Staphylococcus aureus from ocular and otolaryngology infections are frequently resistant to clinically important antibiotics and are associated with lineages of community and hospital origins. PLoS One 2018; 13: e0208518. https://doi.org/10.1371/journal.pone.0208518.

    • Search Google Scholar
    • Export Citation
  • 8.

    Goudarzi M, Kobayashi N, Dadashi M, Pantůček R, Nasiri MJ, Fazeli M, et al. Prevalence, genetic diversity, and temporary shifts of inducible clindamycin resistance Staphylococcus aureus clones in Tehran, Iran: a molecular–epidemiological analysis from 2013 to 2018. Front Microbiol 2020; 11: 663. https://doi.org/10.3389/fmicb.2020.00663.

    • Search Google Scholar
    • Export Citation
  • 9.

    Yousefi M, Pourmand MR, Fallah F, Hashemi A, Mashhadi R, Nazari-Alam A. Characterization of Staphylococcus aureus biofilm formation in urinary tract infection. Iran J Public Health 2016; 45: 485.

    • Search Google Scholar
    • Export Citation
  • 10.

    Goudarzi M, Goudarzi H, Sá Figueiredo AM, Udo EE, Fazeli M, Asadzadeh M, et al. Molecular characterization of methicillin resistant Staphylococcus aureus strains isolated from intensive care units in Iran: ST22-SCC mec IV/t790 emerges as the major clone. PlosOne 2016; 11: e0155529. https://doi.org/10.1371/journal.pone.0155529.

    • Search Google Scholar
    • Export Citation
  • 11.

    Shekarabi M, Hajikhani B, Salimi Chirani A, Fazeli M, Goudarzi MJPo. Molecular characterization of vancomycin-resistant Staphylococcus aureus strains isolated from clinical samples: a three year study in Tehran, Iran. PlosOne 2017; 12: e0183607. https://doi.org/10.1371/journal.pone.0183607.

    • Search Google Scholar
    • Export Citation
  • 12.

    Boye K, Bartels M, Andersen I, Møller J, Westh H. A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I–V. Clin Microbiol Infect 2007; 13: 725727. https://doi.org/10.1111/j.1469-0691.2007.01720.x.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ding YL, Fu J, Chen J, Mo SF, Xu S, Lin N, et al. Molecular characterization and antimicrobial susceptibility of Staphylococcus aureus isolated from children with acute otitis media in Liuzhou, China. BMC Pediatr 2018; 18: 18. https://doi.org/10.1186/s12887-018-1366-6.

    • Search Google Scholar
    • Export Citation
  • 14.

    Marchisio P, Esposito S, Picca M, Baggi E, Terranova L, Orenti A, et al. Prospective evaluation of the aetiology of acute otitis media with spontaneous tympanic membrane perforation. Clin Microbiol Infect 2017; 23: 486 e1–e6. https://doi.org/10.1016/j.cmi.2017.01.010.

    • Search Google Scholar
    • Export Citation
  • 15.

    Hajikhani B, Goudarzi M, Kakavandi S, Amini S, Zamani S, van Belkum A, et al. The global prevalence of fusidic acid resistance in clinical isolates of Staphylococcus aureus: a systematic review and meta-analysis. Antimicrob Resist Infect Control 2021; 10: 75. https://doi.org/10.1186/s13756-021-00943-6.

    • Search Google Scholar
    • Export Citation
  • 16.

    Castanheira M, Watters AA, Mendes RE, Farrell DJ, Jones RN. Occurrence and molecular characterization of fusidic acid resistance mechanisms among Staphylococcus spp. from European countries (2008). J Antimicrob Chemother 2010; 65: 13531358. https://doi.org/10.1093/jac/dkq094.

    • Search Google Scholar
    • Export Citation
  • 17.

    Udo EE, Al-Sweih N, Mokaddas E, Johny M, Dhar R, Gomaa HH, et al. Antibacterial resistance and their genetic location in MRSA isolated in Kuwait hospitals, 1994–2004. BMC Infect Dis 2006; 6: 18. https://doi.org/10.1186/1471-2334-6-168.

    • Search Google Scholar
    • Export Citation
  • 18.

    Shariati A, Dadashi M, Moghadam MT, van Belkum A, Yaslianifard S, Darban-Sarokhalil D. Global prevalence and distribution of vancomycin resistant, vancomycin intermediate and heterogeneously vancomycin intermediate Staphylococcus aureus clinical isolates: a systematic review and meta-analysis. Sci Rep 2020; 10: 116. https://doi.org/10.1038/s41598-020-69058-z.

    • Search Google Scholar
    • Export Citation
  • 19.

    Dadashi M, Hajikhani B, Darban-Sarokhalil D, van Belkum A, Goudarzi M. Mupirocin resistance in Staphylococcus aureus: a systematic review and meta-analysis. J Glob Antimicrob Resist 2020; 20: 238247. https://doi.org/10.1016/j.jgar.2019.07.032.

    • Search Google Scholar
    • Export Citation
  • 20.

    Aqel A, Ibrahim A, Shehabi A. Rare occurrence of mupirocin resistance among clinical Staphylococcus isolates in Jordan. Acta Microbiol Immunol Hung 2012; 59: 239247. https://doi.org/10.1556/amicr.59.2012.2.8.

    • Search Google Scholar
    • Export Citation
  • 21.

    Adhikari R, Shrestha S, Barakoti A, Amatya R. Inducible clindamycin and methicillin resistant Staphylococcus aureus in a tertiary care hospital, Kathmandu, Nepal. BMC Infect Dis 2017; 17: 15. https://doi.org/10.1186/s12879-017-2584-5.

    • Search Google Scholar
    • Export Citation
  • 22.

    Bottega A, Rodrigues MdA, Carvalho FA, Wagner TF, Leal IAS, Santos SOd, et al. Evaluation of constitutive and inducible resistance to clindamycin in clinical samples of Staphylococcus aureus from a tertiary hospital. Rev Soc Bras Med Trop 2014; 47: 589592. https://doi.org/10.1590/0037-8682-0140-2014.

    • Search Google Scholar
    • Export Citation
  • 23.

    Senobar Tahaei SA, Stájer A, Barrak I, Ostorházi E, Szabó D, Gajdács M. Correlation between biofilm-formation and the antibiotic resistant phenotype in Staphylococcus aureus isolates: a laboratory-based study in Hungary and a review of the literature. Infect Drug Resist 2021: 11551168. https://doi.org/10.2147/idr.s303992.

    • Search Google Scholar
    • Export Citation
  • 24.

    Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PloS one 2011; 6: e17936. https://doi.org/10.1371/journal.pone.0017936.

    • Search Google Scholar
    • Export Citation
  • 25.

    Boswihi SS, Udo EE, Al-Sweih N. Shifts in the clonal distribution of methicillin-resistant Staphylococcus aureus in Kuwait hospitals: 1992–2010. PloS one 2016; 11: e0162744. https://doi.org/10.1371/journal.pone.0162744.

    • Search Google Scholar
    • Export Citation
  • 26.

    Chamon RC, Iorio NL, da Silva Ribeiro S, Cavalcante FS, Dos Santos KR. Molecular characterization of Staphylococcus aureus isolates carrying the Panton-Valentine leukocidin genes from Rio de Janeiro hospitals. Diagn Microbiol Infect Dis 2015; 83: 331334. https://doi.org/10.1016/j.diagmicrobio.2015.09.004.

    • Search Google Scholar
    • Export Citation
  • 27.

    Hashemizadeh Z, Hadi N, Mohebi S, Kalantar-Neyestanaki D, Bazargani A. Characterization of SCCmec, spa types and Multi Drug Resistant of methicillin-resistant Staphylococcus aureus isolates among inpatients and outpatients in a referral hospital in Shiraz, Iran. BMC Res Notes 2019; 12: 16. https://doi.org/10.1186/s13104-019-4627-z.

    • Search Google Scholar
    • Export Citation
  • 28.

    Aggarwal S, Jena S, Panda S, Sharma S, Dhawan B, Nath G, et al. Antibiotic susceptibility, virulence pattern, and typing of Staphylococcus aureus strains isolated from variety of infections in India. Front Microbiol 2019; 10: 2763. https://doi.org/10.3389/fmicb.2019.02763.

    • Search Google Scholar
    • Export Citation
  • 29.

    Boswihi SS, Udo EE, AlFouzan W. Antibiotic resistance and typing of the methicillin-resistant Staphylococcus aureus clones in Kuwait hospitals, 2016–2017. BMC Microbiol 2020; 20: 19. https://doi.org/10.1186/s12866-020-02009-w.

    • Search Google Scholar
    • Export Citation
  • 30.

    Yu F, Liu Y, Lu C, Lv J, Qi X, Ding Y, et al. Dissemination of fusidic acid resistance among Staphylococcus aureus clinical isolates. BMC Microbiol 2015; 15: 16. https://doi.org/10.1186/s12866-015-0552-z.

    • Search Google Scholar
    • Export Citation
  • 31.

    Chen H-J, Hung W-C, Tseng S-P, Tsai J-C, Hsueh P-R, Teng L-J. Fusidic acid resistance determinants in Staphylococcus aureus clinical isolates. Antimicrob Agents Chemother 2010; 54: 49854991. https://doi.org/10.1128/aac.00523-10.

    • Search Google Scholar
    • Export Citation
  • 32.

    Havaei SA, Azimian A, Fazeli H, Naderi M, Ghazvini K, Samiee SM, et al. Genetic characterization of methicillin resistant and sensitive, vancomycin intermediate Staphylococcus aureus strains isolated from different Iranian Hospitals. ISRN Microbiol2012; 2012: 215275. https://doi.org/10.5402/2012/215275.

    • Search Google Scholar
    • Export Citation
  • 33.

    Shore AC, Tecklenborg SC, Brennan GI, Ehricht R, Monecke S, Coleman DC. Panton-Valentine leukocidin-positive Staphylococcus aureus in Ireland from 2002 to 2011: 21 clones, frequent importation of clones, temporal shifts of predominant methicillin-resistant S. aureus clones, and increasing multiresistance. J Clin Microbiol 2014; 52: 859870. https://doi.org/10.1128/JCM.02799-13.

    • Search Google Scholar
    • Export Citation
  • 34.

    Liang B, Mai J, Liu Y, Huang Y, Zhong H, Xie Y, et al. Prevalence and characterization of Staphylococcus aureus isolated from women and children in Guangzhou, China. Front Microbiol 2018; 9: 2790. https://doi.org/10.3389/fmicb.2018.02790.

    • Search Google Scholar
    • Export Citation
  • 35.

    Ilczyszyn WM, Sabat AJ, Akkerboom V, Szkarlat A, Klepacka J, Sowa-Sierant I, et al. Clonal structure and characterization of Staphylococcus aureus strains from invasive infections in paediatric patients from South Poland: association between age, spa types, clonal complexes, and genetic markers. PloS One 2016; 11: e0151937. https://doi.org/10.1371/journal.pone.0151937.

    • Search Google Scholar
    • Export Citation
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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
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Foundation
1954
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per Year
1
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per Year
4
Founder Magyar Tudományos Akadémia
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ISSN 1217-8950 (Print)
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