Epidemiology of mecA-Methicillin Resistant Staphylococcus aureus in Iran: A Systematic Review and Meta-analysis

Document Type : Review Article

Authors

1 Mashhad Medical Microbiology Student Research Group, Mashhad University of Medical Sciences, Mashhad, Iran

2 Department of Biostatistics, Mashhad University of Medical Sciences, Mashhad, Iran

3 Department of Microbiology, Central Laboratory, Imam Reza Teaching Hospital, Mashhad, Iran

Abstract

Objective(s)
Staphylococcus aureus is a prevalent pathogen worldwide. Methicillin resistant S. aureus (MRSA), which is usually multi-resistant in hospitals, has been a daunting challenge for clinicians for more than half a century. The aim of this systematic review and meta-analysis is to determine the relative frequency (RF) of MRSA in different regions of Iran.
Materials and Methods
Search terms “Staphylococcus aureus”, “Methicillin”, “mecA” and “Iran” were used in PubMed, Scirus and Google Scholar. Two Persian scientific search engines and ten recent national congresses were also explored. Articles/abstracts, which used clinical specimens and had done PCR to detect the mecA gene, were included in this review. Comprehensive Meta-Analysis and Meta-Analyst software were used for statistical analysis.
Results
Out of 2690 results found in the mentioned databases, 48 articles were included in the final analysis. These studies were done in Ahvaz, Falavarjan, Fasa, Gorgan, Hamedan, Isfahan, Kashan, Mashhad, Sanandaj, Shahrekord, Shiraz, Tabriz, Tehran and Tonekabon. Pooled estimation of 7464 S. aureus samples showed that 52.7%±4.7 (95% confidence interval [CI]) of strains were mecA positive. MRSA RF in different studies varied from 20.48% to 90% in Isfahan and Tehran, respectively. We found a moderate heterogeneity (I2= 48.5%) of MRSA RF among studies conducted in Tehran (ranging from 28.88% to 90%, mean 52.7% [95% CI: 46.6%±58.8%]).
Conclusion
According to the results of this study, MRSA RF in Iran is in the high range. Thus, measures should be taken to keep the emergence and transmission of these strains to a minimum.

Keywords


1. Deleo FR, Otto M, Kreiswirth BN, Chambers HF. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 2010; 375:1557-1568.
2. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 2006; 368:874-885.
3. Cookson B. Five decades of MRSA: controversy and uncertainty continues. Lancet 2011; 378:1291-1292.
4. Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, et al. Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill 2010; 15:1-9.
5. Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003; 36:53-59.
6. Moellering RC. Why has methicillin-resistant Staphylococcus aureus become such a successful pathogen in adults? Infect Dis Clin Pract 2010;18:286-291.
7. Stefani S, Chung DR, Lindsay JA, Friedrich AW, Kearns AM, Westh H, et al. Meticillin-resistant Staphylococcus aureus (MRSA): global epidemiology and harmonisation of typing methods. Int J Antimicrob Agents 2012; 39:273-282.
8. Graveland H, Duim B, van Duijkeren E, Heederik D, Wagenaar JA. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int J Med Microbiol 2011; 301:630-634.
9. Forbes BA. Issues in the identification and susceptibility testing of Staphylococci. In: Crossley KB, Jefferson KK, Archer GL, Fowler VG, editors. Staphylococci in Human Disease. 2nd ed. Oxford, UK: Wiley-Blackwell; 2009. p. 235-252.
10. Karami S, Rahbar M, Vand Yousefi J. Evaluation of five phenotypic methods for detection of methicillin resistant Staphylococcus aureus (MRSA). Iran J Pathol 2011; 6:27-31.
11. Radlberger P, Zechmeister I. Innovative framework for evidence-based decision making in healthcare – standardised working in HTA (WP1.2): HTA- Projektbericht. 2011. Available at: http://eprints.hta.lbg.ac.at/932/1/HTA-Projektbericht_Nr.44a.pdf.
12. Clinical and Laboratory Standards Institute/NCCLS. 2007. Performance standards for antimicrobial susceptibility testing; 17th informational supplement. CLSI document M100-S17. Clinical and Laboratory Standards Institute, Wayne, PA.
13. Clinical and Laboratory Standards Institute/NCCLS. 2008. Performance standards for antimicrobial susceptibility testing; 18th informational supplement. CLSI document M100-S18. Clinical and Laboratory Standards Institute, Wayne, PA.
14. Ekrami A, Samarbafzadeh A, Alavi M, Kalantar E, Hamzeloi F. Prevalence of methicillin resistant Staphylococcus species isolated from burn patients in a burn center, Ahvaz, Iran. Jundishapur J Microbiol 2010; 3:84-91.
15. Moosavian M, Torabipour M. Identification of mecA gene in phenotypic methicillin-resistant Staphylococcus aureus strains isolated from clinical specimens.The First Iranian International Congress of Medical Bacteriology; 4-7 sep; Tabriz, Iran2011. p. 255.
16. Khosravi AD, Hoveizavi H, Farshadzadeh Z. The prevalence of genes encoding leukocidins in Staphylococcus aureus strains resistant and sensitive to methicillin isolated from burn patients in Taleghani hospital, Ahvaz, Iran. Burns 2012; 38:247-251.
17. Heidari M, Momtaz H, Madani M. Detection of the antibiotic resistance genes in Staphylococcus aureus isolated from human infections and bovine mastitis. Afr J Microbiol Res 2011; 5:5132-5136.
18. Abdollahi A, Koohpayeh A, Najafipour S, Mansouri Y, Abdollahi S, Jafari S. Evaluation of drug esistance and SCCmec genotype in MRSA strains. Behdad 2012; 1:47-52.
19. Vaez H, Tabaraei A, Moradi A,Ghaemi EA. Evaluation of methicillin resistance Staphylococcus aureus isolated from patients in Golestan province-north of Iran. Afr J Microbiol Res 2011; 5:432-436.
20. Zamani A, Sadeghian S, Ghaderkhani J, Alikhani MY, Najafimosleh M, Taghi Goodarzi M, et al. Detection of methicillin-resistance (mec-A) gene in Staphylococcus aureus strains by PCR and determination of antibiotic susceptibility. Ann Microbiol 2007; 57:273-276.
21. Alizargar J, Moravveji A. Prevalence of methicillin resistant Staphylococcus in Kashan. First International and 12th Iranian Congress of Microbiology; 23-26 May; Kermanshah, Iran:2011. p. 1328.
22. 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.
23. Zeinali E, Moniri R, Safari M, Mousavi GA. Molecular characterization and SCCmec typing in meticillin-resistant Staphylococcus aureus isolated from clinical samples. Feyz, J Kashan Univ Med Sci 2011; 14:439-446.
24. Naderi Nasab M, Tavakolafshar J, Nazem M, Fatehnasab P, Faramarzi P, Khodadoost M. Detection of methicillin-resistant Staphylococcus aureus by phenotypic methods. Med J Mashhad Univ Med Sci 2005; 48:7-16.
25. Vaiseh P, Ramezanzadeh R, Deilami Z. Identification of class I integron and mecA in Staphylococcus strains typed by REP-PCR method. The Congress of Infections and Antibiotic Resistance; 2-3 May; Gilan, Iran: 2012.p.101.
26. Shariati L, Validi M, Tabatabaiefar MA, Karimi A, Nafisi MR. Comparison of real-time PCR with disk diffusion, agar screen and E-test methods for detection of methicillin-resistant Staphylococcus aureus. Curr Microbiol 2010; 61:520-524.
27. Japoni A, Alborzi A, Orafa F, Rasouli M, Farshad S. Distribution patterns of methicillin resistance genes (mecA) in Staphylococcus aureusisolated from clinical specimens. Iran Biomed J 2004; 8:173-178.
28. Nikbakht M, Nahaei MR, Akhi MT, Asgharzadeh M, Nikvash S. Molecular fingerprinting of meticillin-resistant Staphylococcus aureus strains isolated from patients and staff of two Iranian hospitals. J Hosp Infect 2008; 69:46-55.
29. Zarrini G, Aein F, Bahari Delgosha Z. Study of nosocomial methicillin resistant Staphylococcus aureus (MRSA) using disc diffusion, MASTAScreen MRSA + kit and PCR methods.The Second Iranian Congress of Clinical Microbiology; 7-9 October; Shiraz, Iran:2008. p. 149.
30. Esfandyari Kalajahi A, Hasani A, Riyazi A, Abbasian S, Pourmohammad A, Hasani A. Detection of virulence genes of Staphylococcus aureus isolated from nasal specimens of patients admitted in high risk wards of University teaching hospital, Tabriz. 4th Congress of Laboratory and Clinic; 21-23 December; Tehran, Iran: 2011. p. 491.
31. Kiani nia M. Development of Multiplex PCR for the detection of aph(3)-IIIa and aac(6′)/aph(2′′) genes in methicillin-resistant Staphylococcus aureus (MRSA) isolates from Northwest, Iran. 4th Congress of Laboratory and Clinic; 21-23 December; Tehran, Iran: 2011. p. 996.
32. Kiani nia M, Hasani A, Hasani A, Mirza Ahmadi S, Sadeghifard M, Deghani L. Nasal colonization of high risk group patients of northwest Iran by MRSA Predictability of resistance and concern about prevention. 4th Congress of Laboratory and Clinic; 21-23 December; Tehran, Iran: 2011. p. 853.
33. Mirsalehian A, Jebelameli F, Kazemi B, Alizadeh SA. Comparison of disc diffusion method withpolymerase chain reaction for detectingmethicillin resistancein clinical isolates of Staphylococci. Tehran Univ Med J 2003; 61:420-425.
34. Aligholi M, Emaneini M, Hashemi FB, Shahsavan S, Jabalameli F, Kazemi B. Determination of antimicrobial resistance pattern of Staphylococcus aureus isolated from clinical specimens. Tehran Univ Med J 2006; 64:26-32.
35. Mostafaee M, Behzadian-Nejad G, Najar-peerayeh S, Rezaei Yazdi H, Tohidpoor A. Prevalence of mecA gene in Staphylococcus aureus strains isolated from Tehran hospitals, 1385.The First Iranian Congress of Clinical Microbiology; 8-10 May; Shiraz, Iran:2007.p.16.
36. 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; 17:432-434.
37. Fatholahzadeh B, Emaneini M, Gilbert G, Udo E, Aligholi M, Modarressi MH, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis and antimicrobial susceptibility patterns of methicillin-resistant Staphylococcus aureus (MRSA) isolates in Tehran, Iran. Microb Drug Resist 2008; 14:217-220.
38. Habibi M, Saderi H, Owlia P, Asadi Karam M. Detection of methicillin resistance in Staphylococcus aureus by disk diffusion and PCR methods. Iran J Pathol 2008; 3:11-14.
39. Azimian A, Najar-peerayeh S, Farshchian M, Naderi M, Salehipoor Z, Mostafaee M. Occurrence of the methicillin-resistant Staphylococcus aureus (MRSA) among clinical samples in Tehran and its correlation with the site of infection.The Second Iranian Congress of Clinical Microbiology; 7-9 October; Shiraz, Iran:2008.p.1101.
40. Bagherzadeh Yazdchi S, Pourmand MR, Zaeimi Yazdi J. Anbiotic susceptibility patterns and detection of coa and mecA genes in the Iranian isolates of Staphylococcus aureus.13th International Congress on Infectious Diseases;19-22 June; Kuala Lumpur, Malaysia 2008. p. e271.
41. Dadaei T, Eftekhar F. Correlation of biofilm formation in clinical isolates of Staphylococcus aureus by colony morphology and microplate measurement of biofilm formation.The Second Iranian Congress of Clinical Microbiology; 7-9 October; Shiraz, Iran:2008. p.107.
42. Salehipour Z, Azimian A, Ghazvini K. Phenotypic and genotypic study of drug resistance in Staphylococcus aureus strains isolated from blood culture of septicemia pateints in selected hospitals of Tehran.The Second Iranian Congress of Clinical Microbiology; 7-9 October; Shiraz, Iran:2008. p.172.
43. Aligholi M, Emaneini M, Jabalameli F, Shahsavan S, Abdolmaleki Z, Sedaghat H, et al. Antibiotic susceptibility pattern of gram-positive cocci cultured from patients in three university hospitals in Tehran, Iran during 2001-2005. Acta Med Iran 2009;47:329-334.
44. Emaneini M, Taherikalani M, Eslampour MA, Sedaghat H, Aligholi M, Jabalameli F, et al. Phenotypic and genotypic evaluation of aminoglycoside resistance in clinical isolates of Staphylococci in Tehran, Iran. Microb Drug Resist 2009; 15:129-132.
45. Najar-Peerayeh S, Azimian A, Mostafaee M, Siadat SD. Identification of methicillin-resistant Staphylococcus aureus by disk diffusion method, determination of MIC, and PCR for mecA Gene. Modares Med Sci J: Pathobiol 2009; 12:61-69.
46. Rahimi F, Bouzari M, Maleki Z, Rahimi F. Antibiotic susceptibility pattern among Staphylococcus spp. with emphasis on detection of mecA gene in methicillin resistant Staphylococcus aureus isolates. Iran J Clin Infect Dis 2009; 4:143-150.
47. Yadegar A, Sattari M, Mozafari NA, Goudarzi GR. Prevalence of the genes encoding aminoglycoside-modifying enzymes and methicillin resistance among clinical isolates of Staphylococcus aureus in Tehran, Iran. Microb Drug Resist 2009; 15:109-113.
48. Farhadian A, Behzadian Nejad, Najar-peerayeh S, Farhadian A, Vaziri. Determination of vancomycin and methicillin resistant in isolates of S.aureus in hospitals in the Iran.Third Iranian Congress of Clinical Microbiology; 6-8 October; Shiraz, Iran:2009.p.21.
49. Javan E, Falahati H, Seifi M, Talebi M, Ebrahimpoor G, Poorshafi M. Detection of mecA gene in oxacillin resistant Staphylococcus aureus strains isolated from Tehran hospitals. Iran J Infect Dis Trop Med 2010; 49:17-22.
50. Faghri J, Azimian A, Sadighian H, Khosrojerdi M. Occurrence of the methicillin-resistant Staphylococcus aureus (MRSA)among respiratory tract samples in patients of selected Tehran hospitals.4th Iranian Congress of Clinical Microbiology; 9-11 November; Isfahan, Iran:2010.p.75.
51. Aligholi M, Mirsalehian A, Halimi S, Imaneini H, Taherikalani M, Jabalameli F, et al. Phenotypic and genotypic evaluation of fluoroquinolone resistance in clinical isolates of Staphylococcus aureus in Tehran. Med Sci Monit 2011; 17:PH71-74.
52. 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. Pejouhandeh 2011; 16:83-91.
53. Saderi H, Emadi B, Owlia P. Phenotypic and genotypic study of macrolide, lincosamide and streptogramin B (MLSB) resistance in clinical isolates of Staphylococcus aureus in Tehran, Iran. Med Sci Monit 2011; 17:BR48-53.
54. Shahsavan S, Emaneini M, Noorazar Khoshgnab B, Khoramian B, Asadollahi P, Aligholi M, et al. A high prevalence of mupirocin and macrolide resistance determinant among Staphylococcus aureus strains isolated from burnt patients. Burns 2012; 38:378-382.
55. Ghorbani S, Imani Fooladi AA, Nourani MR. Prevalence of methicillin-resistance (mec-A) gene in Staphylococcus aureus strains from scar by PCR and determination of antibiotic susceptibility. 4th Congress of Laboratory and Clinic; 21-23 December; Tehran, Iran:2011.p.540.
56. Mobaiyen H, Molaabaszadeh H, Modirrousta S, Reza Soltani S. Surveying of Staphylococcus aureus methicillin resistant (mec-A) and determine its antibiotic susceptibility with PCR method in Tehran in 2010.International Union of Microbiological Societies 2011 Congress;Sapporo, Japan:2011. P-BA25-11.
57. Sahebnasagh R, Saderi H, Owlia P. Detection of methicillin-resistant Staphylococcus aureus strains from clinical samples in Tehran by detection of the mecA and nuc genes. The First Iranian International Congress of Medical Bacteriology; 4-7 September; Tabriz, Iran; 2011. p. 195.
58. Sepehriseresht S, Boroumand MA, Pourgholi L, Sotoudeh Anvari M, Habibi E, Sattarzadeh Tabrizi M, et al. Emergence of mupirocin-resistant MRSA among Iranian clinical isolates.Comp Clin Pathol 2012. doi: 10.1007/s00580-012-1472-z.
59. Razavi Davoodi N, Vand Yousefi A, Harzandi N, Hahrafi A, Rajaei B, Gerayeshnejad S, et al.Molecular detection of methicillin resistantStaphylococcus aureus (MRSA) and methicillinresistant coagulase-negative Staphylococcus (CoNS) inIran. Afr J Microbiol Res 2012; 6:3716-3721.
60. Azizi Barjini K, Mousazadeh M, Amani J, Asadi A, Khalili S. Detection of MRSA by Disk diffusion and PCR method and detection of resistance pattern. The Congress of Rational Usage of Antibiotics; 27-28 February; Sari, Iran :2012. p. 38.
61. Forghani F, Alipourfard I, Ghayyomi M, Mahmudi S, Heydari N. Comparative study of methicillin resistant Staphylococcus aureus (MRSA) molecular detection by PCR, with bacteriological methods. First International and 12th Iranian Congress of Microbiology; 23-26 May; Kermanshah, Iran:2011. p. 1194.
62. Dezfulian A, Aslani MM, Oskoui M, Farrokh P, Azimirad M, Dabiri H, et al. Identification and characterization of a high vancomycin-resistant Staphylococcus aureusharboring vanAgene cluster isolated from diabetic foot ulcer. Iran J Basic Med Sci 2012; 15:803-806.
63. Song JH, Hsueh PR, Chung DR, Ko KS, Kang CI, Peck KR, et al. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study. J Antimicrob Chemother 2011; 66:1061-1069.
64. Guzmán-Blanco M, Hsueh PR, Isturiz R, Alvarez C, Bavestrello L, Gotuzzo E, et al. Epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) in Latin America. Int J Antimicrob Agents 2009; 34:304-308.
65. Nimmo GR, Pearson JC, Collignon PJ, Christiansen KJ, Coombs GW, Bell JM, et al. Antimicrobial susceptibility of Staphylococcus aureus isolated from hospital inpatients, 2009: Report from the Australian Group on Antimicrobial Resistance. Commun Dis Intell 2011; 35:237–243.
66. Styers D, Sheehan DJ, Hogan P, Sahm DF. Laboratory-based surveillance of current antimicrobial resistance patterns and trends among Staphylococcus aureus: 2005 status in the United States. Ann Clin Microbiol Antimicrob 2006; 5:1-9.
67. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 2007; 298:1763-1771.
68. Ray GT, Morrison MA, Baxter R. Trends and characteristics of culture-confirmed Staphylococcus aureusinfections in a large U.S. integrated health care organization. J Clin Microbiol 2012; 50:1950-1957.
69. Simor AE, Loeb M. Epidemiology of healthcare-associated Staphylococcus aureus infections. In: Crossley KB, Jefferson KK, Archer GL, Fowler VG, editors. Staphylococci in Human Disease. 2nded. Oxford, UK: Wiley-Blackwell; 2009. p. 290-309.