Virulence gene profiles, SCCmec types, integrons, and antimicrobial resistance of clinical Staphylococcus aureus isolates from Yasuj, southwest Iran
-
Sahar Milani
,
Hadi Ebrahimi
,
Seyed Sajjad Khoramrooz
,
Leila Manzuri
,
Marjan Salahi
,
Seyed Abdolmajid Khosravani
,
Kasra Sharifi
,
Asghar Sharifi
Abstract
Background and Objectives: Staphylococcus aureus poses clinical challenges through its virulence and antibiotic resistance, including SCCmec-mediated methicillin resistance. Integrated data on virulence profiling, molecular typing, and resistance are limited in Southwest Iran. We characterized virulence genes, SCCmec types, integrons, and antimicrobial resistance in S. aureus from diverse clinical sources in Yasuj, Iran.
Materials and Methods: We analyzed 214 S. aureus isolates recovered from tonsil, wound, sinus, and blood specimens (2020–2023). Species confirmation was by nuc PCR. Antimicrobial susceptibility testing followed CLSI disk diffusion guidelines; MRSA was confirmed by mecA PCR. PCR assays detected hemolysin genes (hla, hlb, hld), toxin genes (tst, pvl, eta, etb, etd), MSCRAMM genes (sdrC, sdrD, sdrE), sak, integrase genes (intI, intII), and SCCmec types I, III, and IVa.
Results: Isolates were from tonsils (59.8%), wounds (29.9%), sinusitis (6.1%), and blood (4.2%). MRSA prevalence was 29.0%. Highest resistance was to penicillin (98.6%), erythromycin (59.3%), and tetracycline (54.7%), with MDR in 32.7%. Prevalent virulence genes were hld (87.9%), hla (68.2%), sak (60.3%), sdrC (44.4%), eta (37.9%), sdrD (36.9%), tst (32.2%), sdrE (29.0%), etd (18.2%), and pvl (3.7%). Among 104 MDR/MRSA isolates, intI and intII were found in 14.4% and 10.6%. SCCmec type III dominated (80.5%), followed by I (14.5%) and IVa (5.0%); types I and III were significantly linked to MDR (P < 0.05). Four isolates co-harbored pvl, tst, and hla.
Conclusion: Considerable virulence gene carriage and SCCmec type III dominance were observed. Gentamicin, ciprofloxacin, cotrimoxazole, and clindamycin remain effective. Coexistence of life-threatening toxin genes and high resistance rates necessitates enhanced infection control.
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2. Moridikia F, Ghaedi M, Khosravania SA, Khoramrooz SS, Mohseni R, Zoladl M, et al. The influence of hydro alcoholic extract of Satureja mutica zinc Oxide nanoparticle and zinc complex against coagulase gene expression on standard and clinical isolated of methicillin resistant Staphylococcus aureus. J Comput Appl Mech 2022; 53: 41-54.
3. John J, George S, Nori SRC, Nelson-Sathi S. Phylogenomic analysis reveals the evolutionary route of resistant genes in Staphylococcus aureus. Genome Biol Evol 2019; 11: 2917-2926.
4. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci 2010; 67: 3057-3071.
5. Sadeghi Moghaddam T, Namaei MH, Afshar D, Yousefi M. High frequency of SCCmec type IV and multidrug-resistant SCCmec type I among hospital acquired methicillin-resistant Staphylococcus aureus isolates in Birjand Imam Reza Hospital, Iran. Iran J Microbiol 2022; 14: 67-75.
6. Dawoud TM, Al-Hajjaj YA, Mubarak A, Elbehiry A, El-Tayeb M, Moussa IM. Prevalence, genotyping, and molecular relatedness of methicillin-resistant Staphylococcus aureus isolated from tertiary care hospitals in Jeddah, Saudi Arabia. Cell Mol Biol (Noisy-le-grand) 2025; 71: 95-103.
7. Moatti S, Shojaee Sadi B, Ghaznavi-rad E. Genetic analysis of integrons among methicillin-resistant and susceptible Staphylococcus aureus isolated from nosocomial infections. J Arak Univ Med Sci 2017; 20: 98-107.
8. Mohammadi M, Bahrami N, Khajavian M, Faghri J. The occurrence of type I, II, and III integrons in multi-drug resistance and methicillin-resistant Staphylococcus aureus isolates in Iran. Curr Microbiol 2020; 77: 1653-1659.
9. Shettigar K, Murali TS. Virulence factors and clonal diversity of Staphylococcus aureus in colonization and wound infection with emphasis on diabetic foot infection. Eur J Clin Microbiol Infect Dis 2020; 39: 2235-2246.
10. Burnside K, Lembo A, de Los Reyes M, Iliuk A, BinhTran NT, Connelly JE, et al. Regulation of hemolysin expression and virulence of Staphylococcus aureus by a serine/threonine kinase and phosphatase. PLoS One 2010; 5(6): e11071.
11. Sabat A, Melles DC, Martirosian G, Grundmann H, van Belkum A, Hryniewicz W. Distribution of the serine-aspartate repeat protein-encoding sdr genes among nasal-carriage and invasive Staphylococcus aureus strains. J Clin Microbiol 2006; 44: 1135-1138.
12. Kong C, Neoh HM, Nathan S. Targeting Staphylococcus aureus toxins: a potential form of anti-virulence therapy. Toxins (Basel) 2016; 8: 72.
13. Khodabux RMJ, Mariappan S, Sekar U. Spectrum of virulence factors in clinical isolates of Staphylococcus aureus and prevalence of SCCmec types in methicillin-resistant Staphylococcus aureus in a tertiary care center. J Lab Physicians 2023; 15: 450-461.
14. CLSI (2018). Performance Standards for Antimicrobial Susceptibility Testing. 28th ed. CLSI supplement M100. Wayne, PA. Clinical and Laboratory Standards Institute.
15. Mir Z, Farahani NN, Abbasian S, Alinejad F, Sattarzadeh M, Pouriran R, et al. The prevalence of exotoxins, adhesion, and biofilm-related genes in Staphylococcus aureus isolates from the main burn center of Tehran, Iran. Iran J Basic Med Sci 2019; 22: 1267-1274.
16. Eslami G, Taghizadeh Maleki D, Ghalavand Z, Nikmanesh B, Hashemi A, Kadkhoda H. Identification of virulence genes in Staphylococcus aureus isolates segregated from children's wounds. Res Med 2019; 43: 52-57.
17. Adame-Gómez R, Castro-Alarcón N, Vences-Velázquez A, Toribio-Jiménez J, Pérez-Valdespino A, Leyva-Vázquez MA, et al. Genetic diversity and virulence factors of Staphylococcus aureus isolated from food, humans, and animals. Int J Microbiol 2020; 2020: 1048097.
18. Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2005; 43: 5026-5033.
19. Ren C, Zhao Y, Shen Y. Analysis of the effect of integrons on drug-resistant Staphylococcus aureus by multiplex PCR detection. Mol Med Rep 2013; 7: 719-724.
20. Motamedi H, Fard ES, Aria M, Moosavian SM. SCCmec typing and the association of pvl, ACME, sea and seb genes in Staphylococcus aureus isolates from burn wound infections. Avicenna J Clin Microbiol Infect 2018; 5: 91-96.
21. 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: 614.
22. Moosavian M, Shahin M, Navidifar T, Torabipour M. Typing of staphylococcal cassette chromosome mec encoding methicillin resistance in Staphylococcus aureus isolates in Ahvaz, Iran. New Microbes New Infect 2017; 21: 90-94.
23. Tajik S, Najar-Peerayeh S, Bakhshi B, Golmohammadi R. Molecular characterization of community-associated methicillin-resistant Staphylococcus aureus in Iranian burn patients. Iran J Pathol 2019; 14: 284-289.
24. Motallebi M, Jabalameli F, Beigverdi R, Emaneini M. High prevalence of direct repeat unit types of 10di, 8h and 8i among methicillin resistant Staphylococcus aureus strains with staphylococcal cassette chromosome mec type IIIA isolated in Tehran, Iran. Antimicrob Resist Infect Control 2019; 8: 50.
25. Yu F, Liu Y, Lv J, Qi X, Lu C, Ding Y, et al. Antimicrobial susceptibility, virulence determinant carriage and molecular characteristics of Staphylococcus aureus isolates associated with skin and soft tissue infections. Braz J Infect Dis 2015; 19: 614-622.
26. Alfeky AE, Tawfick MM, Ashour MS, El-Moghazy AA. High prevalence of multi-drug resistant methicillin-resistant Staphylococcus aureus in tertiary Egyptian hospitals. J Infect Dev Ctries 2022; 16: 795-806.
27. Raut S, Bajracharya K, Adhikari J, Pant SS, Adhikari B. Prevalence of methicillin resistant Staphylococcus aureus in Lumbini Medical College and Teaching Hospital, Palpa, Western Nepal. BMC Res Notes 2017; 10: 187.
28. Hosseini SM, Hadi N, Bazargani A, Emami A, Pirbonyeh N. The first report of prevalence of class 1-3 integrons in clinical isolates of Staphylococcus aureus in southwestern Iran: a multicenter study. Jundishapur J Microbiol 2019; 12(11): e90902.
29. Navidinia M, Goudarzi H, Pouriran R, Azimi H, Goudarzi M. Molecular analysis and integron carriage of mupirocin-resistant Staphylococcus aureus strains isolated from burn wound infections, Tehran, Iran. Arch Clin Infect Dis 2019; 14(1): e84764.
30. Goudarzi M, Mohammadi A, Goudarzi H, Fazeli M, Sabzehali F. Genetic variability and integron occurrence in methicillin resistant Staphylococcus aureus strains recovered from patients with urinary tract infection. Arch Pediatr Infect Dis 2019; 7)2): e86189.
31. Li L, Zhao X. Characterization of the resistance class 1 integrons in Staphylococcus aureus isolates from milk of lactating dairy cattle in Northwestern China. BMC Vet Res 2018; 14: 59.
32. Amirkhiz MF, Rezaee MA, Hasani A, Aghazadeh M, Naghili B. SCCmec typing of methicillin-resistant Staphylococcus aureus: an eight year experience. Arch Pediatr Infect Dis 2015; 3(4): e30632.
33. Dhawan B, Rao C, Udo E, Gadepalli R, Vishnubhatla S, Kapil A. Dissemination of methicillin-resistant Staphylococcus aureus SCCmec type IV and SCCmec type V epidemic clones in a tertiary hospital: challenge to infection control. Epidemiol Infect 2015; 143: 343-353.
34. Bhowmik D, Chetri S, Das BJ, Dhar Chanda D, Bhattacharjee A. Distribution of virulence genes and SCCmec types among methicillin-resistant Staphylococcus aureus of clinical and environmental origin: a study from community of Assam, India. BMC Res Notes 2021; 14: 58.
35. Tahbaz SV, Fallah F, Nowroozi J, Armin S, Azimi L. Molecular characterization of exotoxin genes in Staphylococcus aureus recovered from hospitalized patients. J Med Bacteriol 2019; 8: 21-29.
36. Vaez H, Ghalehnoo ZR. Molecular characteristics of Staphylococcus aureus nasal carriage among health care workers at a referral hospital in Zabol, Iran. Pan Afr Med J 2019; 34: 196.
37. Shahini Shams-Abadi M, Halaji M, Hoseini-Alfatemi S, Gholipour A, Mojtahedi A, Ebrahim-Saraie HS. Epidemiology of toxic shock syndrome toxin-1 harboring Staphylococcus aureus obtained from clinical samples in Iran: a systematic review and meta-analysis. Ann Ig 2018; 30: 391-400.
38. Besharati R, Ghafouri M, Safamanesh S, Khosrojerdi M, Ghazvini K, Nojumi S, et al. Molecular epidemiology of Panton-Valentine leukocidin harboring hospital-associated methicillin-resistant Staphylococcus aureus in septicemic children, Northeastern Iran, Bojnurd. Jundishapur J Microbiol 2019; 12(2): e68183.
39. Khalili H, Najar-Peerayeh S, Mahrooghi M, Mansouri P, Bakhshi B. Methicillin-resistant Staphylococcus aureus colonization of infectious and non-infectious skin and soft tissue lesions in patients in Tehran. BMC Microbiol 2021; 21: 282.
40. Memariani M, Memariani H, Shahidi-Dadras M, Tehranchinia Z, Ghalamkarpour F, Moravvej H. Contemporary systematic review and meta-analysis of exfoliative toxin-producing Staphylococcus aureus strains isolated from patients in Iran. Rev Res Med Microbiol 2020; 31: 1-10.
2. Moridikia F, Ghaedi M, Khosravania SA, Khoramrooz SS, Mohseni R, Zoladl M, et al. The influence of hydro alcoholic extract of Satureja mutica zinc Oxide nanoparticle and zinc complex against coagulase gene expression on standard and clinical isolated of methicillin resistant Staphylococcus aureus. J Comput Appl Mech 2022; 53: 41-54.
3. John J, George S, Nori SRC, Nelson-Sathi S. Phylogenomic analysis reveals the evolutionary route of resistant genes in Staphylococcus aureus. Genome Biol Evol 2019; 11: 2917-2926.
4. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci 2010; 67: 3057-3071.
5. Sadeghi Moghaddam T, Namaei MH, Afshar D, Yousefi M. High frequency of SCCmec type IV and multidrug-resistant SCCmec type I among hospital acquired methicillin-resistant Staphylococcus aureus isolates in Birjand Imam Reza Hospital, Iran. Iran J Microbiol 2022; 14: 67-75.
6. Dawoud TM, Al-Hajjaj YA, Mubarak A, Elbehiry A, El-Tayeb M, Moussa IM. Prevalence, genotyping, and molecular relatedness of methicillin-resistant Staphylococcus aureus isolated from tertiary care hospitals in Jeddah, Saudi Arabia. Cell Mol Biol (Noisy-le-grand) 2025; 71: 95-103.
7. Moatti S, Shojaee Sadi B, Ghaznavi-rad E. Genetic analysis of integrons among methicillin-resistant and susceptible Staphylococcus aureus isolated from nosocomial infections. J Arak Univ Med Sci 2017; 20: 98-107.
8. Mohammadi M, Bahrami N, Khajavian M, Faghri J. The occurrence of type I, II, and III integrons in multi-drug resistance and methicillin-resistant Staphylococcus aureus isolates in Iran. Curr Microbiol 2020; 77: 1653-1659.
9. Shettigar K, Murali TS. Virulence factors and clonal diversity of Staphylococcus aureus in colonization and wound infection with emphasis on diabetic foot infection. Eur J Clin Microbiol Infect Dis 2020; 39: 2235-2246.
10. Burnside K, Lembo A, de Los Reyes M, Iliuk A, BinhTran NT, Connelly JE, et al. Regulation of hemolysin expression and virulence of Staphylococcus aureus by a serine/threonine kinase and phosphatase. PLoS One 2010; 5(6): e11071.
11. Sabat A, Melles DC, Martirosian G, Grundmann H, van Belkum A, Hryniewicz W. Distribution of the serine-aspartate repeat protein-encoding sdr genes among nasal-carriage and invasive Staphylococcus aureus strains. J Clin Microbiol 2006; 44: 1135-1138.
12. Kong C, Neoh HM, Nathan S. Targeting Staphylococcus aureus toxins: a potential form of anti-virulence therapy. Toxins (Basel) 2016; 8: 72.
13. Khodabux RMJ, Mariappan S, Sekar U. Spectrum of virulence factors in clinical isolates of Staphylococcus aureus and prevalence of SCCmec types in methicillin-resistant Staphylococcus aureus in a tertiary care center. J Lab Physicians 2023; 15: 450-461.
14. CLSI (2018). Performance Standards for Antimicrobial Susceptibility Testing. 28th ed. CLSI supplement M100. Wayne, PA. Clinical and Laboratory Standards Institute.
15. Mir Z, Farahani NN, Abbasian S, Alinejad F, Sattarzadeh M, Pouriran R, et al. The prevalence of exotoxins, adhesion, and biofilm-related genes in Staphylococcus aureus isolates from the main burn center of Tehran, Iran. Iran J Basic Med Sci 2019; 22: 1267-1274.
16. Eslami G, Taghizadeh Maleki D, Ghalavand Z, Nikmanesh B, Hashemi A, Kadkhoda H. Identification of virulence genes in Staphylococcus aureus isolates segregated from children's wounds. Res Med 2019; 43: 52-57.
17. Adame-Gómez R, Castro-Alarcón N, Vences-Velázquez A, Toribio-Jiménez J, Pérez-Valdespino A, Leyva-Vázquez MA, et al. Genetic diversity and virulence factors of Staphylococcus aureus isolated from food, humans, and animals. Int J Microbiol 2020; 2020: 1048097.
18. Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2005; 43: 5026-5033.
19. Ren C, Zhao Y, Shen Y. Analysis of the effect of integrons on drug-resistant Staphylococcus aureus by multiplex PCR detection. Mol Med Rep 2013; 7: 719-724.
20. Motamedi H, Fard ES, Aria M, Moosavian SM. SCCmec typing and the association of pvl, ACME, sea and seb genes in Staphylococcus aureus isolates from burn wound infections. Avicenna J Clin Microbiol Infect 2018; 5: 91-96.
21. 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: 614.
22. Moosavian M, Shahin M, Navidifar T, Torabipour M. Typing of staphylococcal cassette chromosome mec encoding methicillin resistance in Staphylococcus aureus isolates in Ahvaz, Iran. New Microbes New Infect 2017; 21: 90-94.
23. Tajik S, Najar-Peerayeh S, Bakhshi B, Golmohammadi R. Molecular characterization of community-associated methicillin-resistant Staphylococcus aureus in Iranian burn patients. Iran J Pathol 2019; 14: 284-289.
24. Motallebi M, Jabalameli F, Beigverdi R, Emaneini M. High prevalence of direct repeat unit types of 10di, 8h and 8i among methicillin resistant Staphylococcus aureus strains with staphylococcal cassette chromosome mec type IIIA isolated in Tehran, Iran. Antimicrob Resist Infect Control 2019; 8: 50.
25. Yu F, Liu Y, Lv J, Qi X, Lu C, Ding Y, et al. Antimicrobial susceptibility, virulence determinant carriage and molecular characteristics of Staphylococcus aureus isolates associated with skin and soft tissue infections. Braz J Infect Dis 2015; 19: 614-622.
26. Alfeky AE, Tawfick MM, Ashour MS, El-Moghazy AA. High prevalence of multi-drug resistant methicillin-resistant Staphylococcus aureus in tertiary Egyptian hospitals. J Infect Dev Ctries 2022; 16: 795-806.
27. Raut S, Bajracharya K, Adhikari J, Pant SS, Adhikari B. Prevalence of methicillin resistant Staphylococcus aureus in Lumbini Medical College and Teaching Hospital, Palpa, Western Nepal. BMC Res Notes 2017; 10: 187.
28. Hosseini SM, Hadi N, Bazargani A, Emami A, Pirbonyeh N. The first report of prevalence of class 1-3 integrons in clinical isolates of Staphylococcus aureus in southwestern Iran: a multicenter study. Jundishapur J Microbiol 2019; 12(11): e90902.
29. Navidinia M, Goudarzi H, Pouriran R, Azimi H, Goudarzi M. Molecular analysis and integron carriage of mupirocin-resistant Staphylococcus aureus strains isolated from burn wound infections, Tehran, Iran. Arch Clin Infect Dis 2019; 14(1): e84764.
30. Goudarzi M, Mohammadi A, Goudarzi H, Fazeli M, Sabzehali F. Genetic variability and integron occurrence in methicillin resistant Staphylococcus aureus strains recovered from patients with urinary tract infection. Arch Pediatr Infect Dis 2019; 7)2): e86189.
31. Li L, Zhao X. Characterization of the resistance class 1 integrons in Staphylococcus aureus isolates from milk of lactating dairy cattle in Northwestern China. BMC Vet Res 2018; 14: 59.
32. Amirkhiz MF, Rezaee MA, Hasani A, Aghazadeh M, Naghili B. SCCmec typing of methicillin-resistant Staphylococcus aureus: an eight year experience. Arch Pediatr Infect Dis 2015; 3(4): e30632.
33. Dhawan B, Rao C, Udo E, Gadepalli R, Vishnubhatla S, Kapil A. Dissemination of methicillin-resistant Staphylococcus aureus SCCmec type IV and SCCmec type V epidemic clones in a tertiary hospital: challenge to infection control. Epidemiol Infect 2015; 143: 343-353.
34. Bhowmik D, Chetri S, Das BJ, Dhar Chanda D, Bhattacharjee A. Distribution of virulence genes and SCCmec types among methicillin-resistant Staphylococcus aureus of clinical and environmental origin: a study from community of Assam, India. BMC Res Notes 2021; 14: 58.
35. Tahbaz SV, Fallah F, Nowroozi J, Armin S, Azimi L. Molecular characterization of exotoxin genes in Staphylococcus aureus recovered from hospitalized patients. J Med Bacteriol 2019; 8: 21-29.
36. Vaez H, Ghalehnoo ZR. Molecular characteristics of Staphylococcus aureus nasal carriage among health care workers at a referral hospital in Zabol, Iran. Pan Afr Med J 2019; 34: 196.
37. Shahini Shams-Abadi M, Halaji M, Hoseini-Alfatemi S, Gholipour A, Mojtahedi A, Ebrahim-Saraie HS. Epidemiology of toxic shock syndrome toxin-1 harboring Staphylococcus aureus obtained from clinical samples in Iran: a systematic review and meta-analysis. Ann Ig 2018; 30: 391-400.
38. Besharati R, Ghafouri M, Safamanesh S, Khosrojerdi M, Ghazvini K, Nojumi S, et al. Molecular epidemiology of Panton-Valentine leukocidin harboring hospital-associated methicillin-resistant Staphylococcus aureus in septicemic children, Northeastern Iran, Bojnurd. Jundishapur J Microbiol 2019; 12(2): e68183.
39. Khalili H, Najar-Peerayeh S, Mahrooghi M, Mansouri P, Bakhshi B. Methicillin-resistant Staphylococcus aureus colonization of infectious and non-infectious skin and soft tissue lesions in patients in Tehran. BMC Microbiol 2021; 21: 282.
40. Memariani M, Memariani H, Shahidi-Dadras M, Tehranchinia Z, Ghalamkarpour F, Moravvej H. Contemporary systematic review and meta-analysis of exfoliative toxin-producing Staphylococcus aureus strains isolated from patients in Iran. Rev Res Med Microbiol 2020; 31: 1-10.
| Files | ||
| Issue | Vol 18 No 5 (2026) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v18i5.22864 | |
| Keywords | ||
| Staphylococcus aureus Virulence factors Antibiotic resistance Public health Iran | ||
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How to Cite
1.
Milani S, Ebrahimi H, Khoramrooz SS, Manzuri L, Salahi M, Khosravani SA, Sharifi K, Sharifi A. Virulence gene profiles, SCCmec types, integrons, and antimicrobial resistance of clinical Staphylococcus aureus isolates from Yasuj, southwest Iran. Iran J Microbiol. 2026;18(5):729-740.
