Iranian Journal of Microbiology 2018. 10(2):82-89.

Genetic diversity of Staphylococcus aureus strains from a teaching hospital in Isfahan, Iran: The emergence of MRSA ST639- SCCmec III and ST343- SCCmec III
Hossein Sedaghat, Bahram Nasr Esfahani, Mehrdad Halaji, Azhar Sallari Jazi, Sina Mobasherizadeh, Seyed Rohollah Havaei, Mohammad Emaneini, Seyed Asghar Havaei


Background and Objectives: Staphylococcus aureus is an important pathogen that can be colonized in the nose and increase the risk of spreading infections in hospitals. The present study aimed at determining the phenotypic and genotypic characterization of S. aureus strains isolated from patients and healthcare workers (HCWs) from a teaching hospital in Isfahan, Iran.

Materials and Methods: This cross-sectional study was performed on 262 nasal swabs and 23 clinical isolates that were collected from a teaching hospital during February and April 2016. Staphylococcal cassette chromosome mec (SCCmec) and multilocus sequence typing (MLST) were performed for selected isolates.

Results: Overall, 23% and 18% of healthcare workers and patients were carriers, respectively. Methicillin-resistant S. aureus (MRSA) rate was 13%, 33% and 52% in nasal HCWs, nasal patients, and clinical samples, respectively. The molecular typing of MRSA isolates revealed that the most common SCCmec type is SCCmec type III (88%). The highest rate of resistance was observed against tetracycline and erythromycin, with 48.7%. The most frequently detected toxin genes among S. aureus isolates were hla (99%) and sea (44%), moreover, pvl genes were detected in (40%) of MRSA isolates. The results of MLST showed 7 different sequence types (STs): ST859 (2/9), ST6 (2/9), ST639 (1/9), ST343 (1/9), ST239 (1/9), ST291 (1/9) and ST25 (1/9).

Conclusion: Our results revealed that ST clones associated with healthcare-associated MRSA (HA-MRSA) are actively circulating among nasal carriage in our healthcare setting, and thus, effective infection control policies are needed to reduce nasal carriage in healthcare settings.


MRSA; MLST; Nasal carrier; SCCmec typing

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Deurenberg RH, Beisser PS, Visschers MJ, Driessen C, Stobberingh EE. Molecular typing of methicillin-susceptible Staphylococcus aureus isolates collected in the Yogyakarta area in Indonesia, 2006. Clin Microbiol Infect 2010;16:92-94.

Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005;5:751-762.

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;1085:131-148.

Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000;38:1032-1035.

Motallebi M, Jabalameli F, Asadollahi K, Taherikalani M, Emaneini M. Spreading of genes encoding enterotoxins, haemolysins, adhesin and biofilm among methicillin resistant Staphylococcus aureus strains with staphylococcal cassette chromosome mec type IIIA isolated from burn patients. Microb Pathog 2016;97:34-37.

Ghasemian A, Najar Peerayeh S, 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;10:258-264.

Namvar AE, Asghari B, Ezzatifar F, Azizi G, Lari AR. Detection of the intercellular adhesion gene cluster (ica) in clinical Staphylococcus aureus isolates. GMS Hyg Infect Control 2013; 8(1):Doc03.

Khoshkharam-Roodmajani H, Sarvari J, Bazargani A, Kandekar-Ghahraman MR, Nazari-Alam A, Motamedifar M. Molecular typing of methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from Shiraz teaching hospitals by PCR-RFLP of coagulase gene. Iran J Microbiol 2014;6:246-452.

Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 2000;38:1008-1015.

Stranden A, Frei R, Widmer AF. Molecular typing of methicillin-resistant Staphylococcus aureus: can PCR replace pulsed-field gelelectrophoresis? J Clin Microbiol 2003;41:3181-3186.

Mahon CR, Lehman DC, Manuselis G (2014). Textbook of Diagnostic Microbiology. Elsevier Health Sciences, Amsterdam, Netherlands.

CLSI (2015). Performance standards for antimicrobial susceptibility testing t, informational supplement. M100-S25. Wayne PCaLSI.

Vancraeynest D, Hermans K, Haesebrouck F. Genotypic and phenotypic screening of high and low virulence Staphylococcus aureus isolates from rabbits for biofilm formation and MSCRAMMs. Vet Microbiol 2004;103(3-4):241-247.

Johnson WM, Tyler SD, Ewan EP, Ashton FE, Pollard DR, Rozee KR. Detection of genes for enterotoxins, exfoliative toxins, and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reaction. J Clin Microbiol 1991;29:426-430.

Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002;70: 631-641.

Sauer P, Sila J, Stosova T, Vecerova R, Hejnar P, Vagnerova I, et al. Prevalence of genes encoding extracellular virulence factors among meticillin-resistant Staphylococcus aureus isolates from the university hospital, Olomouc, Czech Republic. J Med Microbiol 2008;57(Pt 4):403-410.

Emaneini M, Jabalameli F, Rahdar H, Leeuwen WBV, Beigverdi R. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Iranian healthcare workers: a systematic review and meta-analysis. Rev Soc Bras Med Trop 2017;50:590-597.

Cirkovic I, Stepanovic S, Skov R, Trajkovic J, Grgurevic A, Larsen AR. Carriage and genetic diversity of methicillin-resistant Staphylococcus aureus among patients and healthcare workers in a Serbian university hospital. PLoS One 2015:10(5):e0127347.

Cirkovic I, Trajkovic J, Hauschild T, Andersen PS, Shittu A, Larsen AR. Nasal and pharyngeal carriage of methicillin-resistant Staphylococcus sciuri among hospitalised patients and healthcare workers in a Serbian university hospital. PLoS One 2017: 12: e0185181.

Askarian M, Zeinalzadeh A, Japoni A, Alborzi A, Memish ZA. Prevalence of nasal carriage of methicillin-resistant Staphylococcus aureus and its antibiotic susceptibility pattern in healthcare workers at Namazi Hospital, Shiraz, Iran. Int J Infect Dis 2009;13(5):e241-247.

Emaneini M, Jabalameli F, Rahdar H, Leeuwen WB, Beigverdi R. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Iranian healthcare workers: a systematic review and meta-analysis. Rev Soc Bras Med Trop 2017; 50: 590-597.

Ohadian Moghadam S, Pourmand MR, Davoodabadi A. The Detection of mupirocin resistance and nasal carriage of methicillin resistant Staphylococcus aureus among healthcare workers at university hospitals of Tehran, Iran. Iran J Public Health 2015;44:361-368.

Ghasemian R, Najafi N, Makhlough A, Khademloo M. Frequency of nasal carriage of Staphylococcus aureus and its antimicrobial resistance pattern in patients on hemodialysis. Iran J Kidney Dis 2010; 3: 218-222.

Karimi M, Esfahani BN, Halaji M, Mobasherizadeh S, Shahin M, Havaei SR, et al. Molecular characteristics and antibiotic resistance pattern of Staphylococcus aureus nasal carriage in tertiary care hospitals of Isfahan, Iran. Infez Med 2017; 25: 234-240.

Hidron AI, Kourbatova EV, Halvosa JS, Terrell BJ, McDougal LK, Tenover FC, et al. Risk factorsfor colonization with methicillin-resistant Staphylococcus aureus (MRSA) in patients admitted to anurban hospital: emergence of community-associated MRSA nasal carriage. Clin Infect Dis 2005;41:159-66.

Havaei SA, Vidovic S, Tahmineh N, Mohammad K, Mohsen K, Starnino S, et al. Epidemic methicillin-susceptible Staphylococcus aureus lineages are the main cause of infections at an Iranian university hospital. J Clin Microbiol 2011;49:3990-3993.

Goudarzi M, Goudarzi H, Sa 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.

Ohadian Moghadam S, Pourmand MR, Mahmoudi M, Sadighian H. Molecular characterization of methicillin-resistant Staphylococcus aureus: characterization of major clones and emergence of epidemic clones of sequence type (ST) 36 and ST 121 in Tehran, Iran. FEMS Microbiol Lett 2015;362(8):fnv043.

Shekarabi M, HajikhaniB, Salimi Chirani A, Fazeli M, Goudarzi M. Molecular characterization of vancomycin-resistant Staphylococcus aureus strains isolated from clinical samples: A three year study in Tehran, Iran. PLoS One 2017;12:e0183607.

Tabor DE, Yu L, Mok H, Tkaczyk C, Sellman BR, Wu Y, et al. Staphylococcus aureus Alpha-toxin is conserved among diverse hospital respiratory isolates collected from a global surveillance study and is neutralized by monoclonal antibody MEDI4893. Antimicrob Agents Chemother 2016; 60: 5312-5321.

Kateete DP, Namazzi S, Okee M, Okeng A, Baluku H, Musisi NL, et al. High prevalence of methicillin resistant Staphylococcus aureus in the surgical units of Mulago hospital in Kampala, Uganda. BMC Res Notes 2011;4:326.

Sedaghat H, Nasr Esfahani B, Mobasherizadeh S, Sallari JA, Halaji M, Sadeghi P. et al. Phenotypic and genotypic characterization of macrolide resistance among Staphylococcus aureus isolates in Isfahan, Iran. Iran J Microbiol 2017; 9: 264-270.

Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG, Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015;28:603-661.

Bien J, Sokolova O, Bozko P. Characterizationof virulence factors of Staphylococcus aureus: novel function of known virulence factors that are implicated in activation of airway epithelial proinflammatory response. J Pathog 2011;601905.

Chua KY, Monk IR, Lin YH, Seemann T, Tuck KL, Porter JL, et al. Hyperexpression of α-hemolysin explains enhanced virulence of sequence type 93 community-associated methicillin-resistant Staphylococcus aureus. BMC Microbiol 2014; 14:31.

Kamarehei F, Ghaemi EA, Dadgar T. Prevalence of enterotoxin A and B genes in Staphylococcusa Kamarehei F, Ghaemi EA, Dadgar T. Prevalence of enterotoxin A and B genes in Staphylococcus aureus isolated from clinical samples and healthy carriers in Gorgan City, North of Iran. Indian J Pathol Microbiol 2013;56:265-268.

Pourmand RP MM, Hoseini M, Bagherzadeh Yazdchi S. High prevalence of SEA gene among clinical isolates of Staphylococcus aureus in Tehran. Acta Medica Iranica 2009;47:357-361.


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