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Mahtab Hadadi *
Hamid Heidari
Hadi Sedigh Ebrahim-Saraie
Mohammad Motamedifar
(*) Corresponding Author:
Mahtab Hadadi |


Background: Staphylococcus aureus is a common cause of nosocomial infections that leads to broad spectrum of diseases. Increasing antibiotic resistance among S. aureus strains, particularly methicillin-resistant S. aureus (MRSA) is a serious concern. In addition, the emergence of antiseptics resistance in MRSA helps organism to easily persist and spread in healthcare environments. The aim of this study was to determine the molecular characteristics of vancomycin, mupirocin and antiseptic resistant S. aureus strains.

Materials and Methods: This cross-sectional study was performed on a total of 120 MRSA isolates collected from two major hospitals in Shiraz, Iran. Minimum inhibitory concentrations (MICs) of vancomycin and mupirocin were determined by E-test method according to CLSI and Eucast guidelines. Presence of resistance genes were investigated by PCR method.

Results: Antibacterial susceptibility tests for MRSA isolates showed that 7 isolates (5.8%) were vancomycin-resistant S. aureus (VRSA) and 15 isolates (12.5%) were high-level mupirocin resistant (MuH). None of the isolate had vancomycin resistance gene (vanA), but the frequency of mupirocin resistance gene was significant and 55 (45.8%) isolates carried mupA gene.

Moreover, norA, smr and qacA/B genes were detected in 110 (91.7%), 55 (45.8%) and 36 (30%) strains, respectively.

Conclusion: This study showed the existence of VISA and VRSA strains in our region, and we also found high frequency of mupirocin and biocide resistance genes among strains.

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1. Samanta D, Elasri MO. The msaABCR operon regulates resistance in vancomycin-intermediate Staphylococcus aureus strains. Antimicrob Agents Chemother. 2014;58:6685-95.
2. Périchon B, Courvalin P. VanA-type vancomycin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2009;53:4580-87.
3. Seah C, Alexander DC, Louie L, Simor A, Low DE, Longtin J, Melano RG. MupB, a new high-level mupirocin resistance mechanism in Staphylococcus aureus. Antimicrob Agents Chemother. 2012;56:1916-20.
4. Schmitz FJ, Lindenlauf E, Hofmann B, Fluit AD, Verhoef J, Heinz HP, Jones ME. The prevalence of low-and high-level mupirocin resistance in staphylococci from 19 European hospitals. J Antimicrob Chemother. 1998;42:489-95.
5. Oommen SK, Appalaraju B, Jinsha K. Mupirocin resistance in clinical isolates of staphylococci in a tertiary care centre in south India. Indian J Med Microbiol. 2010;28:372-5.
6. Taheri N, Ardebili A, Amouzandeh-Nobaveh A, Ghaznavi-Rad E. Frequency of Antiseptic resistance among Staphylococcus aureus and Coagulase-Negative Staphylococci isolated from a university hospital in central Iran. Oman Med J. 2016;31:426.
7. Vali L, Davies SE, Lai LL, Dave J, Amyes SG. Frequency of biocide resistance genes, antibiotic resistance and the effect of chlorhexidine exposure on clinical methicillin-resistant Staphylococcus aureus isolates. J Antimicrob Chemother. 2008;61:524-32.
8. Noguchi N, Suwa J, Narui K, Sasatsu M, Ito T, Hiramatsu K, Song JH. Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J Med Microbiol. 2005:54:557-65.
9. W. Winn Jr., S. Allen, W. Janda. Koneman's Color Atlas and Textbook of
Diagnostic Microbiology, sixth ed., Lippincott Williams & Wilkins, 2006.
10. Kobayashi N, Wu H, Kojima K, Taniguchi K, Urasawa S, Uehara N, Omizu Y, Kishi Y, Yagihashi A, Kurokawa I. Detection of mecA, femA, and femB genes in clinical strains of staphylococci using polymerase chain reaction. Epidemiol Infect. 1994;113:259-66.
11. Clinical and Laboratory Standards Institute, Performance Standards for Antimicrobial.Susceptibility Testing; Twenty-sixth Informational Supplemen, 2016 (m100-s26).
12. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters [Internet]. Breakpoint tables for interpretation of MICs and zone diameters; 2016.
13. Sambrook J, Russell DW. Purification of nucleic acids by extraction with phenol: chloroform. Cold Spring Harb Protoc. 2006;2006:4455.
14. Liu Q, Zhao H, Han L, Shu W, Wu Q, Ni Y. Frequency of biocide-resistant genes and susceptibility to chlorhexidine in high-level mupirocin-resistant, methicillin-resistant Staphylococcus aureus (MuH MRSA). Diagn Microbiol Infect Dis. 2015;82:278-83.
15. Clark NC, Cooksey RC, Hill BC, Swenson JM, Tenover FC. Characterization of glycopeptide-resistant enterococci from US hospitals. Antimicrob Agents Chemother. 1993;37:2311-17.
16. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, Hori S, Fukuchi Y, Kobayashi I. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet. 1997;350:1670-73.
17. McGuinness WA, Malachowa N, DeLeo FR. Focus: Infectious Diseases: Vancomycin Resistance in Staphylococcus aureus. Yale J Biol Med. 2017;90:269-81.
18. Aligholi M, Emaneini M, Jabalameli F, Shahsavan S, Dabiri H, Sedaght H. Emergence of high-level vancomycin-resistant Staphylococcus aureus in the Imam Khomeini Hospital in Tehran Med Princ Pract. 2008;17:432-4.
19. Shekarabi M, Hajikhani B, Chirani AS, 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;12:183607.
20. Thati V, Shivannavar CT, Gaddad SM. Vancomycin resistance among methicillin resistant Staphylococcus aureus isolates from intensive care units of tertiary care hospitals in Hyderabad. Indian J Med Res. 2011;134:704.
21. Tiwari HK, Sen MR. Emergence of vancomycin resistant Staphylococcus aureus (VRSA) from a tertiary care hospital from northern part of India. BMC Infect Dis. 2006;6:156.
22. Oliveira GA, Dell'Aquila AM, Masiero RL, Levy CE, Gomes MS, Cui L, Hiramatsu K, Mamizuka EM. Isolation in Brazil of nosocomial Staphylococcus aureus with reduced susceptibility to vancomycin. Infect Control Hosp Epidemiol. 2001;22:443-48.
23. Dezfulian A, Aslani MM, Oskoui M, Farrokh P, Azimirad M, Dabiri H, Salehian MT, Zali MR. Identification and characterization of a high vancomycin-resistant Staphylococcus aureus harboring vanA gene cluster isolated from diabetic foot ulcer. Iran J Basic Med Sci. 2012;15:803-6.
24. Azimian A, Havaei SA, Fazeli H, Naderi M, Ghazvini K, Samiee SM, Soleimani M, Peerayeh SN. Genetic characterization of a vancomycin-resistant Staphylococcus aureus isolate from the respiratory tract of a patient in a university hospital in northeastern Iran. J Clin Microbiol. 2012; 50:3581-5.
25. Hasani A, Sheikhalizadeh V, Hasani A, Naghili B, Valizadeh V, Nikoonijad AR. Methicillin resistant and susceptible Staphylococcus aureus: Appraising therapeutic approaches in the northwest of Iran. Iran J Microbiol. 2013;5:56-62.
26. 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):241-47.
27. Saderi H, Oulia P, Habibi M. Detection of resistance to mupirocin in Staphylococcus aureus strains isolated from patients in four university hospitals of Tehran by polymerase chain reaction (pcr) method. Daneshvar Med. 2009;16:29 -36.
28. Hesami S, Hosseini SD, Amouzandeh-Nobaveh A, Eskandari S, Ghaznavi-Rad E. Phenotypic and genotypic determination of mupirocin resistance among methicillin susceptibility and resistance in Staphylococci isolated from nosocomial infections. J Mazandaran Uni Med Sci. 2014;23:30-39.
29. Joshi PR, Acharya M, Aryal R, Thapa K, Kakshapati T, Seng R, Singh A, Sitthisak S. Emergence of staphylococcal cassette chromosome mec type I with high-level mupirocin resistance among methicillin-resistant Staphylococcus aureus. Asian Pac J Trop Biomed. 2017;7:193-97.
30. Ebrahim-Saraie HS, Motamedifar M, Sarvari J, Alfatemi SM. Emergence of SCCmec type I obtained from clinical samples in Shiraz teaching hospitals, southwest of Iran. Jundishapur J of microbiol. 2015;8.
31. Fritz SA, Hogan PG, Camins BC, Ainsworth AJ, Patrick C, Martin MS, Krauss MJ, Rodriguez M, Burnham CA. Mupirocin and chlorhexidine resistance in Staphylococcus aureus in patients with community-onset skin and soft tissue infections. Antimicrob Agents Chemother. 2013;57 : 559-68.
32. McDonnell G, Russell AD. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev. 1999;12:147-79.
33. Jaglic Z, Cervinkova D. Genetic basis of resistance to quaternary ammonium compounds -the qac genes and their role: a reviewVet Med. 2012;57.
34. Nowroozi J, Pakzad P, Ebrahimi E, Razavipour R. Detection of biocide resistance genes, qac A/B and smr, among isolated Staphylococcus aureus from clinical and non-clinical sources. Pajoohandeh J. 2011;16:83-91.
35. Mayer S, Boos M, Beyer A, Fluit AC, Schmitz FJ. Distribution of the antiseptic resistance genes qacA, qacB and qacC in 497 methicillin-resistant and -susceptible European isolates of Staphylococcus aureus. J Antimicrob Chemother. 2001;47:896-7.
36. Noguchi N, Suwa J, Narui K, Sasatsu M, Ito T, Hiramatsu K, Song JH. Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J Med Microbiol. 2005; 54:557-65.