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Macrolide-Lincosamide Resistance and Virulence Genes in Staphylococcus aureus Isolated from Clinical Specimens in Ardabil, Iran

Document Type : Original Research

Authors

1 Department of Microbiology, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran

2 Department of Infectious Diseases, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran

Abstract

Background & Objective: Staphylococcus aureus causes various hospital- and community-acquired infections. This study aimed to investigate the phenotypic and genotypic characteristics of erythromycin and inducible clindamycin resistance, virulence gene profiles, and spa types of S. aureus isolates collected from patients in Ardabil Province, Iran.
Methods: A total of 118 clinical S. aureus isolates, including 50 (42.4%) methicillin-resistant S. aureus (MRSA) and 68 (57.6%) methicillin-susceptible S. aureus (MSSA) strains, were investigated. Resistance patterns were determined by the disk diffusion method and minimum inhibitory concentration (MIC) test. Inducible macrolide-lincosamide-streptogramin B (iMLSB) resistance was detected using D-test method. The polymerase chain reaction (PCR) was used to identify the virulence and resistance-encoding genes. Additionally, the spa types of the isolates were determined using the PCR, followed by sequencing.
Results: In total, 49.1% (58/118) and 44% (52/118) of the isolates were resistant to erythromycin and clindamycin, respectively. Overall, 13.5% (16/118) of the isolates showed the iMLSB resistance phenotype. The ermC gene (72.4% [42]) was the most frequent erythromycin resistance-encoding gene, followed by ermA (60.3% [35]), ermB (60.3% [35]), ermTR (51.7% [30]), and msrA (15.5% [9]) genes among erythromycin-resistant isolates. The virulence genes hla, hld, sea, LukS PV, tst, seb, sed, eta, sec, and etb were detected in 93.2%, 74.5%, 70.3%, 32.2%, 29.6%, 17%, 8.5%, 8.5%, 5.9%, and 4.2% of the isolates, respectively. Ten different spa types were identified for 58 erythromycin-resistant S. aureus strains, of which t030 and t078 types were the most common types.
Conclusion: A high frequency of macrolide- and lincosamide-resistant S. aureus isolates with different genetic backgrounds of resistance and virulence may be  found  in patients in Ardabil Province, Iran.

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References
  1. DeLeo FR, Chambers HF. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J Clin Invest. 2009; 119(9): 2464-74. [DOI:10.1172/JCI38226] [PMID]
  2. Turlej AG, Hryniewicz WA, Empel J. Staphylococcal cassette chromosome mec (Sccmec) classification and typing methods: an overview. Pol J Microbiol. 2011; 60(2): 95-103. [DOI:10.33073/pjm-2011-013] [PMID]
  3. Maina EK, Kiiyukia C, Wamaea CN, Waiyaki PG, Kariuki S. Characterization of methicillin-resistant Staphylococcus aureus from skin and soft tissue infections in patients in Nairobi, Kenya. Int J Infect Dis. 2013; 17(2): 115-9. [DOI:10.1016/j.ijid.2012.09.006] [PMID]
  4. Yilmaz G, Aydin K, Iskender S, Caylan R, Koksal I. Detection and prevalence of inducible clindamycin resistance in staphylococci. J Med Microbiol. 2007; 56: 342-5. [DOI:10.1099/jmm.0.46761-0] [PMID]
  5. Delialioglu N, Aslan G, Ozturk C, Baki V, Sen S, Emekdas G. Inducible clindamycin resistance in Staphylococci isolated from clinical samples. Jpn J Infect Dis. 2005; 58: 104-6.
  6. Adeyemo O, Okunye O, Nwaokorie F, Kamet O. Isolation and Characterization of Coagulase Positive, Methicillin and Multi-Drug Resistant Staphylococcus and Mammaliicoccus species Isolated from Wound of Patients Attending Federal Medical Centre, Yola, Adamawa State, Nigeria. Iran J Med Microbiol. 2023; 17 (4) :414-422. [DOI: 30699/ijmm.17.4.414]
  7. Mohanasoundaram KM. The prevalence of Inducible clindamycin resistance among gram positive cocci from various clinical specimens. J Clin Diagn Res. 2011; 5(1): 38- 40.
  8. Shrestha B, Pokhrel BM, Mohapatra TM. Phenotypic characterization of nosocomial isolates of Staphylococcus aureus with reference to MRSA. J Infect Dev Ctries. 2009; 3(7): 554-60. [DOI:10.3855/jidc.474] [PMID]
  9. Eady EA, Ross JI, Tipper JL, Walters CE, Cove JH, Noble WC. Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci. J Antimicrob Chemother. 1993; 31(2): 211-7. [DOI:10.1093/jac/31.2.211] [PMID]
  10. Mittal V, Kishore S, Siddique M. Prevalence of inducible clindamycin resistance among clinical isolates of Staphylococcus aureus detected by phenotypic method: A preliminary report. J Infect Dis Immun. 2013; 5(1): 10-2. [DOI:10.5897/JIDI12.005]
  11. Aktas Z, Aridogan A, Kayacan CB, Aydin D. Resistance to macrolide, lincosamide and streptogramin antibiotics in staphylococci isolated in Istanbul, Turkey. J Microbiol. 2007; 45(4): 286-90.
  12. Schwalbe, R, Steele-Moore, L, Goodwin, AC. (Eds.). Antimicrobial susceptibility testing protocols (1st ed). CRC Press, New York. 2007. [DOI:10.1201/9781420014495]
  13. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard-tenth edition, CLSI document M07-A10. Wayne, PA: Clinical and Laboratory Standard Institute; 2023.
  14. Arabestani MR, Rastiyani S, Alikhani MY, Mousavi SF. The relationship between prevalence of antibiotics resistance and virulence factors genes of MRSA and MSSA strains isolated from clinical samples, West Iran. Oman Med J. 2018; 33(2): 134.‏ [DOI:10.5001/omj.2018.25] [PMID]
  15. Abdollahi S, Ramazanzadeh R, Delami Khiabani Z, Kalantar E, Menbari S. Molecular detection of inducible clindamycin resistance among Staphylococcal strains isolated from hospital patients. J Ardabil Uni Med Sci. 2013 10; 13(1): 59-68.
  16. Sedaghat H, Esfahani, BN, Mobasherizadeh, S, Jazi AS, Halaji, Sadeghi P, et al. Phenotypic and genotypic characterization of macrolide resistance among Staphylococcus aureus isolates in Isfahan. Iran. Iran J Microbiol. 2017; 9(5): 264.‏
  17. Patel M., Waites KB, Moser SA, Cloud GA, Hoesley CJ. Prevalence of inducible clindamycin resistance among community- and hospital- associated Staphylococcus aureus isolates. J Clin Microbiol. 2006; 44(7): 2481-4. [DOI:10.1128/JCM.02582-05] [PMID]
  18. Zelazny AM, Ferraro MJ, Glennen A, Hindler JF, Mann LM, Munro S. et al. Selection of strains for quality assessment of the disk induction method for detection of inducible clindamycin resistance in staphylococci: a CLSI collaborative study. J Clin Microbiol. 2005; 43(6): 2613-5. [DOI:10.1128/JCM.43.6.2613-2615.2005] [PMID]
  19. Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003; 41(12): 5442-8. [DOI:10.1128/JCM.41.12.5442-5448.2003] [PMID]
  20. Malachowa N, DeLeo FR. Mobile genetic elements of Staphylococcus aureus. Cell Mol Life Sci. 2010; 67(18): 3057-71. [DOI:10.1007/s00018-010-0389-4] [PMID]
  21. Fiebelkorn KR, Crawford SA, Mc Elmeel ML, Jorgensen JH. Practical disk diffusion method for detection of inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci. J Clin Microbiol. 2003; 41(10): 4740-4. [DOI:10.1128/JCM.41.10.4740-4744.2003] [PMID]
  22. Fokas S, Tsironi M, Kalkani M, Dionysopouloy M. Prevalence of inducible clindamycin resistance in macrolide-resistant Staphylococcus. Clin Microbiol Infect. 2005; 11(4): 337-40. [DOI:10.1111/j.1469-0691.2005.01101.x] [PMID]
  23. Firouzi F, Akhtari J, Nasrolahei M. Prevalence of MRSA and VRSA Strains of Staphylococcus aureus in healthcare staff and inpatients. J Mazandaran Univ Med Sci. 2016 10; 26(142): 96-107.
  24. Aslanimehr M, Yaghobfar R, Peymani A. Detection of MLSB phenotypes and inducible clindamycin resistance in staphylococcus aureus isolates in-patients of Qazvin and Tehran teaching hospitals. J Qazvin Univ Med Sci. 2014; 18: 30-6.
  25. Fathali Z, Mirzaee M, Najarpeerayeh S. Identification sec, hla, pvl and tsst-1 toxins genes profile in of Methicillin-Resistant Staphylococcus aureus clinical isolates. J Ilam Univ Med Sci. 2016, 24(4): 32-40. [DOI:10.18869/acadpub.sjimu.24.4.32]
  26. Turng B, Sinha J, Deal M, Pollitt J, Callihan D, Brasso B, et al. Detection and interpretation of Macrolide-Lincosamide-Streptogramin resistance among Staphylococcus with Phoenix Automated Microbiology System and BDXpert™ System. As presented at the 15th European Congress of Clinical Microbiology and Infectious Disease (ECCMID), Copenhagen, 2005; LR875.
  27. Watkins RR, Holubar M, and David MZ. Antimicrobial resistance in methicillin-resistant Staphylococcus aureus to newer antimicrobial agents. Antimicrob Agents Chemother. 2019: 63(12): e01216-19.‏ [DOI:10.1128/AAC.01216-19] [PMID]
  28. Spilopoulou I, Petinaki E, Papandreou P, Dimitracopoulos G. erm(C) is the predominant genetic determinant for the expression of resistance to macrolides among methicillin-resistance Staphylococcus aureus clinical isolates in Greece. J Antimicrob Chemother. 2004; 53: 814-817. [DOI:10.1093/jac/dkh197] [PMID]
  29. Omid MR, Jamali H, Kafilzadeh F, Borjian A, Arzanlou M. Molecular epidemiology, virulence factors, antibiotic resistance and risk factors for nasal carriage of Staphylococcus aureus in a teenage student population: High prevalence of oxacillin susceptible MRSA isolates. Jundishapur J Microbio. 2021 30:14(9). [DOI:10.5812/jjm.118240]
  30. Hosseini SS, Niakan M, Saderi H, Motallebi M, Taherikalani M, Asadollahi K, et al. Frequency of genes encoding erythromycin ribosomal methylases among Staphylococcus aureus clinical isolates with different D-phenotypes in Tehran, Iran. Iran J Microbiol. 2016; 8(3): 161.
  31. Gul HC, Kilic A, Guclu AU, Bedir O, Orhon M, Basustaoglu AC. Macrolide-lincosamide-streptogramin B resistant phenotypes and genotypes for methicillin-resistant Staphylococcus aureus in Turkey, from 2003 to 2006. Pol J Microbiol. 2008; 57: 307-312.
  32. ‏32. Arzanlou M, Chai WC, Venter H. Intrinsic, adaptive and acquired antimicrobial resistance in Gram-negative bacteria. Essays Biochem. 2017; 61(1): 49-59.‏ [DOI:10.1042/EBC20160063] [PMID]
  33. Otto M. Staphylococcus aureus toxins. Curr Opin Microbiol. 2014; 7: 32-7. [DOI:10.1016/j.mib.2013.11.004] [PMID]
  34. Evenson ML, Hinds MW, Bernstein RS, Bergdoll MS. Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk. Int J Food Microbiol. 1988; 7(4): 311-6. [DOI:10.1016/0168-1605(88)90057-8] [PMID]
  35. Fries BC, Varshney AK. Bacterial toxins-Staphylococcal enterotoxin B. Microbiol Spectr. 2013; 1(2): 10.1128. [PMID] [DOI:10.1128/microbiolspec.AID-0002-2012]
  36. Pinchuk IV, Beswick EJ, Reyes VE. Staphylococcal enterotoxins. Toxins. 2010; 2(8): 2177-97. [DOI:10.3390/toxins2082177] [PMID]
  37. Krüll M, Dold C, Hippenstiel S, Rosseau S, Lohmeyer J, Suttorp N. Escherichia coli hemolysin and Staphylococcus aureas alpha-toxin potently induce neutrophil adhesion to cultured human endothelial cells. J Immunol. 1996; 157(9): 4133-40. [DOI:10.4049/jimmunol.157.9.4133] [PMID]
  38. Horváth A, Dobay O, Sahin-Tóth J, Juhász E, Pongrácz J, Iván M, et al. Characterisation of antibiotic resistance, virulence, clonality and mortality in MRSA and MSSA bloodstream infections at a tertiary-level hospital in Hungary: a 6-year retrospective study. Ann Clin Microbiol Antimicrob. 2020; 19(1):17. [DOI:10.1186/s12941-020-00357-z] [PMID]
  39. Shukla SK, Karow ME, Brady JM, Stemper ME, Kislow J, Moore N, et al. Virulence genes and genotypic associations in nasal carriage, community-associated methicillin-susceptible and methicillin-resistant USA400 Staphylococcus aureus isolates. J Clin Microbiol. 2010; 48(10): 3582-92. ‏ [DOI:10.1128/JCM.00657-10] [PMID]
  40. Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, et al. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol. 1999; 37(11): 3556-63.‏ [DOI:10.1128/JCM.37.11.3556-3563.1999] [PMID]
  41. Asadollahi P, Farahani NN, Mirzaii M, Khoramrooz SS, Van Belkum A, Asadollahi K. Distribution of the most prevalent spa types among clinical isolates of Methicillin-Resistant and-Susceptible Staphylococcus aureus around the world: A review. Front Microbiol. 2018; 9: 163. [DOI:10.3389/fmicb.2018.00163] [PMID]
  42. Ranjbar Omida M, Jamali H, Kafilzadeh F, Borjian A, Arzanlou M. Occurrence of Staphylococcus spp. in the wastewaters from Iran: Diversity, antimicrobial resistance, and virulence potential. J Water Health. 2023; 21(2): 178-91 [DOI:10.2166/wh.2023.199]
Iranian Journal of Pathology
Volume 18, Issue 4
October 2023
Pages 415-424
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History
  • Receive Date: 10 January 2023
  • Revise Date: 23 July 2023
  • Accept Date: 27 August 2023
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