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Published in: Antimicrobial Resistance & Infection Control 1/2020

01-12-2020 | Research

Molecular analysis of methicillin-resistant Staphylococcus aureus isolates from four teaching hospitals in Iran: the emergence of novel MRSA clones

Authors: Farzaneh Firoozeh, Mitra Omidi, Mahmood Saffari, Hossein Sedaghat, Mohammad Zibaei

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2020

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Abstract

Background

The global spread of methicillin-resistant Staphylococcus aureus (MRSA) infections necessitates the use of validated methods for the identification and typing of this bacterium. This study aimed to determine the distribution of main molecular types of MRSA strain circulating among hospitalized patients in teaching hospitals in Isfahan and Kashan.

Methods

A total of 146 Staphylococcus aureus strains were isolated from patients in four teaching hospitals in Isfahan and Kashan during June 2017 to September 2018. The antimicrobial resistance patterns of Staphylococcus aureus strains were performed by disc diffusion method. The MRSA strains were identified phenotypically and confirmed by PCR assay. The prevalence of microbial surface components recognizing adhesive matrix molecules (MSCRAMMs) genes among MRSA strains was evaluated by multiplex PCR. The genotypes of MRSA strains were determined by multilocus sequence typing and SCCmec typing.

Results

Of 146 Staphylococcus aureus isolates, 24 (16.4%) isolates were identified as MRSA strains. According to antimicrobial susceptibility testing the highest resistance rates were seen for tetracycline, erythromycin, ciprofloxacin and gentamicin. All of Staphylococcus aureus isolates were susceptible to vancomycin whereas 3 (2.1%) isolates were resistant to linezolid. Three different SCCmec types were obtained among MRSA strains including 16 (66.7%) SCCmec type V, 3 (12.5%) SCCmec type III and 5 (20.8%) SCCmec type II. Of 24 MRSA isolates 20 (83.3%) carried MSCRAMMs genes including eno (70.8%), fib (54.1%), cna (25.0%), fnbB (16.6%), ebps 5 (20.8%), and the fnbA, bbp and clfA genes were not detected in any MRSA isolate. MLST analysis revealed 11 sequence types among MRSA isolates as follows: ST239, ST291, ST22, ST861, ST889, ST8, ST59, ST343, ST772, ST6 and ST1465. Also seven MLST-based clonal complexes (CCs) were identified among MRSA strains including: CC8, CC7, CC398, CC59, CC22, CC1 and CC5.

Conclusions

A relatively high diversity was found in MRSA genotypes in Kashan and Isfahan hospitals, and seven clonal complexes were identified. Pandemic MRSA clones including CC8 and CC22 were the most prevalent clones and the novel ST types including ST1465, ST861, ST 889 and ST772 are reported for the first time in Iran in the present study. In addition the high prevalence of MSCRAMMs genes in MRSA isolates demonstrates the high potential of these strains for pathogenicity.
Literature
1.
go back to reference Omidi M, Firoozeh F, Saffari M, Sedaghat H, Zibaei M, Khaledi A. Ability of biofilm production and molecular analysis of spa and ica genes among clinical isolates of methicillin-resistant Staphylococcus aureus. BMC Res Notes. 2020;13:19.CrossRef Omidi M, Firoozeh F, Saffari M, Sedaghat H, Zibaei M, Khaledi A. Ability of biofilm production and molecular analysis of spa and ica genes among clinical isolates of methicillin-resistant Staphylococcus aureus. BMC Res Notes. 2020;13:19.CrossRef
2.
go back to reference Walsh EJ, Miajlovic H, Gorkun OV, Foster TJ. Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the αC-domain of human fibrinogen. Microbiology. 2008;154:550–8.CrossRef Walsh EJ, Miajlovic H, Gorkun OV, Foster TJ. Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the αC-domain of human fibrinogen. Microbiology. 2008;154:550–8.CrossRef
3.
go back to reference Ghasemian A, Peerayeh SN, Bakhshi B, Mirzaee M. The microbial surface components recognizing adhesive matrix molecules (MSCRAMMs) genes among clinical isolates of Staphylococcus aureus from hospitalized children. Iran J Pathol. 2015;10:258–64.PubMedPubMedCentral Ghasemian A, Peerayeh SN, Bakhshi B, Mirzaee M. The microbial surface components recognizing adhesive matrix molecules (MSCRAMMs) genes among clinical isolates of Staphylococcus aureus from hospitalized children. Iran J Pathol. 2015;10:258–64.PubMedPubMedCentral
4.
go back to reference Kot B, Sytykiewicz H, Sprawka I. Expression of the biofilm-associated genes in methicillin-resistant Staphylococcus aureus in biofilm and planktonic conditions. Int J Mol Sci. 2018;19:E3487.CrossRef Kot B, Sytykiewicz H, Sprawka I. Expression of the biofilm-associated genes in methicillin-resistant Staphylococcus aureus in biofilm and planktonic conditions. Int J Mol Sci. 2018;19:E3487.CrossRef
5.
go back to reference Joh D, Wann ER, Kreikemeyer B, Speziale P, Höök M. Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol. 1999;18:211–23.CrossRef Joh D, Wann ER, Kreikemeyer B, Speziale P, Höök M. Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol. 1999;18:211–23.CrossRef
6.
go back to reference Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol. 2003;41:4465–7.CrossRef Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol. 2003;41:4465–7.CrossRef
7.
go back to reference Francois P, Pittet D, Bento M, Pepey B, Vaudaux P, Lew D, et al. Rapid detection of methicillin-resistant Staphylococcus aureus directly from sterile or nonsterile clinical samples by a new molecular assay. J Clin Microbiol. 2003;41:254–60.CrossRef Francois P, Pittet D, Bento M, Pepey B, Vaudaux P, Lew D, et al. Rapid detection of methicillin-resistant Staphylococcus aureus directly from sterile or nonsterile clinical samples by a new molecular assay. J Clin Microbiol. 2003;41:254–60.CrossRef
8.
go back to reference Kwon NH, Park KT, Moon JS, Jung WK, Kim SH, Kim JM, et al. Staphylococcal cassette chromosome mec (SCCmec) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCmec subtype IVg isolated from bovine milk in Korea. J Antimicrob Chemother. 2005;56:624–32.CrossRef Kwon NH, Park KT, Moon JS, Jung WK, Kim SH, Kim JM, et al. Staphylococcal cassette chromosome mec (SCCmec) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCmec subtype IVg isolated from bovine milk in Korea. J Antimicrob Chemother. 2005;56:624–32.CrossRef
9.
go back to reference Singh SK, Anwar S, Sharma HK, Chaudhary U, Verma SK. FemA gene in Indian isolates of methicillin resistant Staphylococcus aureus–isolation and amplification through real time PCR. Eur J Exp Biol. 2014;4:90–4. Singh SK, Anwar S, Sharma HK, Chaudhary U, Verma SK. FemA gene in Indian isolates of methicillin resistant Staphylococcus aureus–isolation and amplification through real time PCR. Eur J Exp Biol. 2014;4:90–4.
10.
go back to reference Huang CC, Ho CM, Chen HC, Li CY, Tien N, Fan HM, et al. Evaluation of double locus (clfB and spa) sequence typing for studying molecular epidemiology of methicillin-resistant Staphylococcus aureus in Taiwan. J Microbiol Immunol Infect. 2017;50:604–12.CrossRef Huang CC, Ho CM, Chen HC, Li CY, Tien N, Fan HM, et al. Evaluation of double locus (clfB and spa) sequence typing for studying molecular epidemiology of methicillin-resistant Staphylococcus aureus in Taiwan. J Microbiol Immunol Infect. 2017;50:604–12.CrossRef
11.
go back to reference Green SM, Marsh P, Ahmad N, Jefferies JM, Clarke SC. Characterization of community and hospital Staphylococcus aureus isolates in Southampton, UK. J Med Microbiol. 2010;59:1084–8.CrossRef Green SM, Marsh P, Ahmad N, Jefferies JM, Clarke SC. Characterization of community and hospital Staphylococcus aureus isolates in Southampton, UK. J Med Microbiol. 2010;59:1084–8.CrossRef
12.
go back to reference Lee CY, Fang YP, Chang YF, Wu TH, Yang YY, Huang YC. Comparison of molecular epidemiology of bloodstream methicillin-resistant Staphylococcus aureus isolates between a new and an old hospital in Central Taiwan. Int J Infect Dis. 2019;79:162–8.CrossRef Lee CY, Fang YP, Chang YF, Wu TH, Yang YY, Huang YC. Comparison of molecular epidemiology of bloodstream methicillin-resistant Staphylococcus aureus isolates between a new and an old hospital in Central Taiwan. Int J Infect Dis. 2019;79:162–8.CrossRef
13.
go back to reference Mkrtchyan HV, Xu Z, Yacoub M, Ter-Stepanyan MM, Karapetyan HD, Kearns AM, et al. Detection of diverse genotypes of methicillin-resistant Staphylococcus aureus from hospital personnel and the environment in Armenia. Antimicrob Resist Infect Control. 2017;6:19.CrossRef Mkrtchyan HV, Xu Z, Yacoub M, Ter-Stepanyan MM, Karapetyan HD, Kearns AM, et al. Detection of diverse genotypes of methicillin-resistant Staphylococcus aureus from hospital personnel and the environment in Armenia. Antimicrob Resist Infect Control. 2017;6:19.CrossRef
14.
go back to reference Mahon CR, Lehman DC, Manuselis G. Textbook of diagnostic microbiology.5th ed. Washington DC: Saunders; 2015. Mahon CR, Lehman DC, Manuselis G. Textbook of diagnostic microbiology.5th ed. Washington DC: Saunders; 2015.
15.
go back to reference Amiri A, Firoozeh F, Moniri R, Zibaei M. Prevalence of CTX-M-Type and PER extended-spectrum β-lactamases among Klebsiella spp. isolated from clinical specimens in the teaching hospital of Kashan, Iran. Iran Red Crescent Med J. 2016;18:e22260.CrossRef Amiri A, Firoozeh F, Moniri R, Zibaei M. Prevalence of CTX-M-Type and PER extended-spectrum β-lactamases among Klebsiella spp. isolated from clinical specimens in the teaching hospital of Kashan, Iran. Iran Red Crescent Med J. 2016;18:e22260.CrossRef
16.
go back to reference Clinical and Laboratory Standards Institute. erformance Standards for Antimicrobial Susceptibility Testing. 29th information supplement. Wayne PA: M100-S27; 2019. Clinical and Laboratory Standards Institute. erformance Standards for Antimicrobial Susceptibility Testing. 29th information supplement. Wayne PA: M100-S27; 2019.
17.
go back to reference Jukes L, Mikhail J, Bome-Mannathoko N, Hadfield SJ, Harris LG, El-Bouri K, Davies AP, Mack D. Rapid differentiation of Staphylococcus aureus, Staphylococcus epidermidis and other coagulase-negative staphylococci and meticillin susceptibility testing directly from growth-positive blood cultures by multiplex real-time PCR. J Med Microbiol. 2010;59:1456–61.CrossRef Jukes L, Mikhail J, Bome-Mannathoko N, Hadfield SJ, Harris LG, El-Bouri K, Davies AP, Mack D. Rapid differentiation of Staphylococcus aureus, Staphylococcus epidermidis and other coagulase-negative staphylococci and meticillin susceptibility testing directly from growth-positive blood cultures by multiplex real-time PCR. J Med Microbiol. 2010;59:1456–61.CrossRef
18.
go back to reference Boye K, Bartels MD, Andersen IS, Møller JA, Westh H. A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I–V. Clin Microbiol Infect. 2007;13:725–7.CrossRef Boye K, Bartels MD, Andersen IS, Møller JA, Westh H. A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I–V. Clin Microbiol Infect. 2007;13:725–7.CrossRef
19.
go back to reference Ito T, Kuwahara-Arai K, Katayama Y, Uehara Y, Han X, Kondo Y, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis of MRSA. Methods Mol Biol. 2014;1085:131–48.CrossRef Ito T, Kuwahara-Arai K, Katayama Y, Uehara Y, Han X, Kondo Y, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis of MRSA. Methods Mol Biol. 2014;1085:131–48.CrossRef
20.
go back to reference Pourmand MR, Hassanzadeh S, Mashhadi R, Askari E. Comparison of four diagnostic methods for detection of methicillin resistant Staphylococcus aureus. Iran J Microbiol. 2014;6:341–4.PubMedPubMedCentral Pourmand MR, Hassanzadeh S, Mashhadi R, Askari E. Comparison of four diagnostic methods for detection of methicillin resistant Staphylococcus aureus. Iran J Microbiol. 2014;6:341–4.PubMedPubMedCentral
21.
go back to reference 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-SCCmec IV/t790 emerges as the major clone. PLoS One. 2016;11:e0155529.CrossRef 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-SCCmec IV/t790 emerges as the major clone. PLoS One. 2016;11:e0155529.CrossRef
22.
go back to reference D’Souza N, Rodrigues C, Mehta A. Molecular characterization of methicillin-resistant Staphylococcus aureus with emergence of epidemic clones of sequence type (ST) 22 and ST 772 in Mumbai, India. J Clin Microbiol. 2010;48:1806–11.CrossRef D’Souza N, Rodrigues C, Mehta A. Molecular characterization of methicillin-resistant Staphylococcus aureus with emergence of epidemic clones of sequence type (ST) 22 and ST 772 in Mumbai, India. J Clin Microbiol. 2010;48:1806–11.CrossRef
23.
go back to reference Ghanbari F, Saberianpour S, Zarkesh-Esfahani F, Ghanbari N, Taraghian A, Khademi F. Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated from community- and hospital-acquired infections. Avicenna J Clin Microb Infec. 2017;4:e42244. Ghanbari F, Saberianpour S, Zarkesh-Esfahani F, Ghanbari N, Taraghian A, Khademi F. Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated from community- and hospital-acquired infections. Avicenna J Clin Microb Infec. 2017;4:e42244.
24.
go back to reference Goudarzi M, Eslami G, Rezaee R, Heidary M, Khoshnood S, Sajadi NR. Clonal dissemination of Staphylococcus aureus isolates causing nosocomial infections, Tehran, Iran. Iran J Basic Med Sci. 2019;22:238–45.PubMedPubMedCentral Goudarzi M, Eslami G, Rezaee R, Heidary M, Khoshnood S, Sajadi NR. Clonal dissemination of Staphylococcus aureus isolates causing nosocomial infections, Tehran, Iran. Iran J Basic Med Sci. 2019;22:238–45.PubMedPubMedCentral
25.
go back to reference Havaei SA, Halaji M, Vidovic S, Dillon JR, Karbalaei M, Ghanbari F, et al. Prevalence and genotyping of methicillin-resistant and – susceptible Staphylococcus aureus strains isolated from patients in a university hospital, Isfahan, Iran. Jundishapur J Microbiol. 2017;10:e13571.CrossRef Havaei SA, Halaji M, Vidovic S, Dillon JR, Karbalaei M, Ghanbari F, et al. Prevalence and genotyping of methicillin-resistant and – susceptible Staphylococcus aureus strains isolated from patients in a university hospital, Isfahan, Iran. Jundishapur J Microbiol. 2017;10:e13571.CrossRef
26.
go back to reference Hallin M, Denis O, Deplano A, De Mendonça R, De Ryck R, Rottiers S, et al. Genetic relatedness between methicillin-susceptible and methicillin-resistant Staphylococcus aureus: results of a national survey. J Antimicrob Chemother. 2007;59:465–72.CrossRef Hallin M, Denis O, Deplano A, De Mendonça R, De Ryck R, Rottiers S, et al. Genetic relatedness between methicillin-susceptible and methicillin-resistant Staphylococcus aureus: results of a national survey. J Antimicrob Chemother. 2007;59:465–72.CrossRef
27.
go back to reference Zafar A, Stone M, Ibrahim S, Parveen Z, Hasan Z, Khan E, et al. Prevalent genotypes of meticillin-resistant Staphylococcus aureus: report from Pakistan. J Med Microbiol. 2011;60:56–62.CrossRef Zafar A, Stone M, Ibrahim S, Parveen Z, Hasan Z, Khan E, et al. Prevalent genotypes of meticillin-resistant Staphylococcus aureus: report from Pakistan. J Med Microbiol. 2011;60:56–62.CrossRef
28.
go back to reference Sedaghat H, Esfahani BN, Halaji M, Jazi AS, Mobasherizadeh S, Havaei SR, et al. Genetic diversity of Staphylococcus aureus strains from a teaching hospital in Isfahan, Iran: the emergence of MRSA ST639- SCCmec III and ST343- SCCmec III. Iran J Microbiol. 2018;10:82–9.PubMedPubMedCentral Sedaghat H, Esfahani BN, Halaji M, Jazi AS, Mobasherizadeh S, Havaei SR, et al. Genetic diversity of Staphylococcus aureus strains from a teaching hospital in Isfahan, Iran: the emergence of MRSA ST639- SCCmec III and ST343- SCCmec III. Iran J Microbiol. 2018;10:82–9.PubMedPubMedCentral
29.
go back to reference Peng H, Liu D, Ma Y, Gao W. Comparison of community- and healthcare-associated methicillin-resistant Staphylococcus aureus isolates at a Chinese tertiary hospital, 2012–2017. Sci Rep. 2018;8:17916.CrossRef Peng H, Liu D, Ma Y, Gao W. Comparison of community- and healthcare-associated methicillin-resistant Staphylococcus aureus isolates at a Chinese tertiary hospital, 2012–2017. Sci Rep. 2018;8:17916.CrossRef
30.
go back to reference Noguchi N, Nakaminami H, Nishijima S, Kurokawa I, So H, Sasatsu M. Antimicrobial agent of susceptibilities and antiseptic resistance gene distribution among methicillin-resistant Staphylococcus aureus isolates from patients with impetigo and staphylococcal scalded skin syndrome. J Clin Microbiol. 2006;44:2119–25.CrossRef Noguchi N, Nakaminami H, Nishijima S, Kurokawa I, So H, Sasatsu M. Antimicrobial agent of susceptibilities and antiseptic resistance gene distribution among methicillin-resistant Staphylococcus aureus isolates from patients with impetigo and staphylococcal scalded skin syndrome. J Clin Microbiol. 2006;44:2119–25.CrossRef
31.
go back to reference Japoni-Nejad A, Rezazadeh M, Kazemian H, Fardmousavi N, van Belkum A, Ghaznavi-Rad E. Molecular characterization of the first community-acquired methicillin-resistant Staphylococcus aureus strains from Central Iran. Int J Infect Dis. 2013;17:e949–54.CrossRef Japoni-Nejad A, Rezazadeh M, Kazemian H, Fardmousavi N, van Belkum A, Ghaznavi-Rad E. Molecular characterization of the first community-acquired methicillin-resistant Staphylococcus aureus strains from Central Iran. Int J Infect Dis. 2013;17:e949–54.CrossRef
32.
go back to reference Linde H, Wagenlehner F, Strommenger B, Drubel I, Tanzer J, Reischl U, et al. Healthcare-associated outbreaks and community-acquired infections due to MRSA carrying the Panton-valentine leucocidin gene in southeastern Germany. Eur J Clin Microbiol Infect Dis. 2005;24:419–22.CrossRef Linde H, Wagenlehner F, Strommenger B, Drubel I, Tanzer J, Reischl U, et al. Healthcare-associated outbreaks and community-acquired infections due to MRSA carrying the Panton-valentine leucocidin gene in southeastern Germany. Eur J Clin Microbiol Infect Dis. 2005;24:419–22.CrossRef
Metadata
Title
Molecular analysis of methicillin-resistant Staphylococcus aureus isolates from four teaching hospitals in Iran: the emergence of novel MRSA clones
Authors
Farzaneh Firoozeh
Mitra Omidi
Mahmood Saffari
Hossein Sedaghat
Mohammad Zibaei
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2020
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-020-00777-8

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