EPIDEMIOLOGY OF METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS IN ARAB COUNTRIES OF THE MIDDLE EAST AND NORTH AFRICAN REGION

Main Article Content

Hussam Tabaja
Dr. Joya-Rita Hindy
Dr. Souha S. Kanj

Keywords

MRSA, Methicillin Resistant Staphylococcus aureus, Middle East, North African

Abstract

Available data suggests a high burden of methicillin-resistant staphylococcus aureus (MRSA) in Arab countries of the Middle East and North Africa (MENA). To review the MRSA prevalence and molecular epidemiology in this region, we used PubMed search engine to identify relative articles published from January 2005 to December 2019. Great heterogeneity in reported rates was expectedly seen. Nasal MRSA colonization ranged from 0-32% in healthy volunteers but 4-73% in healthcare workers. Infective MRSA rates ranged between 6%-66% in Saudi Arabia, 12%-29% in United Arab of Emirates, 13%-21% in Qatar, 14%-37% in Oman, 20%-72% in Lebanon, 56% in Gaza, 32%-68% in Jordan, 34%-88% in Iraq and Iraqi Kurdistan, 47%-77% in Egypt, 19-86% in Algeria, and 18-40% in Tunisia. In the GCC, [PVL-] ST239-III, [PVL+] ST80-IV, [PVL+] ST30-IV, [PVL-] ST22-IV and its [PVL+] and [tst1+] variants, [PVL-] CC6-IV, [PVL-] CC5-IV, and [PVL-] ST5-II had a significant presence. In the Levant region, [PVL+] ST80-IV, [PVL+] ST30-IV, [PVL-] ST239-III, [PVL-] ST22-IV were prevalent in Lebanon, Jordan, and Gaza; [PVL-] ST22-IVa-t223 (“Gaza strain”) was prevalent in Gaza and Jordan; USA300, and USA800 were prevalent in Iraq. In North Africa, [PVL+] ST80-IV and [PVL-] ST239-III was commonly reported in Egypt, Algeria, and Tunisia. Finally, significant antimicrobial resistance was seen in the region with variation in patterns depending on location and clonal type. For a more accurate assessment of MRSA epidemiology and burden, the Arab countries need to implement national surveillance systems.

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Reference

1. 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(9538):874-85.
2. Borg MA, de Kraker M, Scicluna E, van de Sande-Bruinsma N, Tiemersma E, Monen J, et al. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in invasive isolates from southern and eastern Mediterranean countries. J Antimicrob Chemother. 2007;60(6):1310-5.
3. Yousef SA, Mahmoud SY, MT. E. PREVALENCE OF METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS IN SAUDI ARABIA: SYSTEMIC REVIEW AND META-ANALYSIS. . Afr J Cln Exper Microbiol.2013. p. 146-54.
4. "Middle East & North Africa | Data". Data.Worldbank.Org , 2021, https://data.worldbank.org/country/ZQ.
5. Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect. 2007;13(3):222-35.
6. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One. 2011;6(4):e17936.
7. El-Mahdy TS, El-Ahmady M, Goering RV. Molecular characterization of methicillin-resistant Staphylococcus aureus isolated over a 2-year period in a Qatari hospital from multinational patients. Clin Microbiol Infect. 2014;20(2):169-73.
8. Abou Shady HM, Bakr AEA, Hashad ME, Alzohairy MA. Staphylococcus aureus nasal carriage among outpatients attending primary health care centers: a comparative study of two cities in Saudi Arabia and Egypt. Brazilian Journal of Infectious Diseases. 2015;19(1):68-76.
9. Zakai SA. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among medical students in Jeddah, Saudi Arabia. Saudi Med J. 2015;36(7):807-12.
10. Panhotra BR, Saxena AK, Al Mulhim AS. Prevalence of methicillin-resistant and methicillin-sensitive Staphylococcus aureus nasal colonization among patients at the time of admission to the hospital. Ann Saudi Med. 2005;25(4):304-8.
11. Alhussaini MS. Methicillin-resistant Staphylococcus aureus Nasal Carriage Among Patients Admitted at Shaqra General Hospital in Saudi Arabia. Pak J Biol Sci. 2016;19(5):233-8.
12. Iyer A, Kumosani T, Azhar E, Barbour E, Harakeh S. High incidence rate of methicillin-resistant Staphylococcus aureus (MRSA) among healthcare workers in Saudi Arabia. J Infect Dev Ctries. 2014;8(3):372-8.
13. El-Mahdy, T.S., et al. Complex Clonal Diversity of Staphylococcus aureus Nasal Colonization among Community Personnel, Healthcare Workers, and Clinical Students in the Eastern Province, Saudi Arabia. Biomed Res Int, 2018. 2018: p. 4208762.
14. Pathare NA, Tejani S, Asogan H, Al Mahruqi G, Al Fakhri S, Zafarulla R, et al. Comparison of Methicillin Resistant Staphylococcus Aureus in Healthy Community Hospital Visitors [CA-MRSA] and Hospital Staff [HA-MRSA]. Mediterr J Hematol Infect Dis. 2015;7(1):e2015053.
15. Pathare NA, Asogan H, Tejani S, Al Mahruqi G, Al Fakhri S, Zafarulla R, et al. Prevalence of methicillin resistant Staphylococcus aureus [MRSA] colonization or carriage among health-care workers. J Infect Public Health. 2016;9(5):571-6.
16. Ghanem HM, Abou-Alia AM, Alsirafy SA. Prevalence of methicillin-resistant Staphylococcus aureus colonization and infection in hospitalized palliative care patients with cancer. Am J Hosp Palliat Care. 2013;30(4):377-9.
17. Al-Humaidan OS, El-Kersh TA, Al-Akeel RA. Risk factors of nasal carriage of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus among health care staff in a teaching hospital in central Saudi Arabia. Saudi Med J. 2015;36(9):1084-90.
18. Aqel AA, Alzoubi HM, Vickers A, Pichon B, Kearns AM. Molecular epidemiology of nasal isolates of methicillin-resistant Staphylococcus aureus from Jordan. J Infect Public Health. 2015;8(1):90-7.
19. Kaibni MH, Farraj MA, Adwan K, Essawi TA. Community-acquired meticillin-resistant Staphylococcus aureus in Palestine. J Med Microbiol. 2009;58(Pt 5):644-7.
20. Hussein NR, Assafi MS, Ijaz T. Methicillin-resistant Staphylococcus aureus nasal colonisation amongst healthcare workers in Kurdistan Region, Iraq. J Glob Antimicrob Resist. 2017;9:78-81.
21. El Aila NA, Al Laham NA, Ayesh BM. Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at Al Shifa hospital in Gaza Strip. Bmc Infect Dis. 2017;17.
22. Halablab MA, Hijazi SM, Fawzi MA, Araj GF. Staphylococcus aureus nasal carriage rate and associated risk factors in individuals in the community. Epidemiol Infect. 2010;138(5):702-6.
23. Sfeir M, Obeid Y, Eid C, Saliby M, Farra A, Farhat H, et al. Prevalence of Staphylococcus aureus methicillin-sensitive and methicillin-resistant nasal and pharyngeal colonization in outpatients in Lebanon. Am J Infect Control. 2014;42(2):160-3.
24. Abaza AF, Mohamed ON, El-Fiky FK, Ahmed KA. Nasal carriage of methicillin-resistant Staphylococcus aureus and the effect of tea extracts on isolates. J Egypt Public Health Assoc. 2016;91(3):135-43.
25. Ben Slama K, Gharsa H, Klibi N, Jouini A, Lozano C, Gómez-Sanz E, et al. Nasal carriage of Staphylococcus aureus in healthy humans with different levels of contact with animals in Tunisia: genetic lineages, methicillin resistance, and virulence factors. Eur J Clin Microbiol Infect Dis. 2011;30(4):499-508.
26. Antri K, Akkou M, Bouchiat C, Bes M, Martins-Simoes P, Dauwalder O, et al. High levels of Staphylococcus aureus and MRSA carriage in healthy population of Algiers revealed by additional enrichment and multisite screening. Eur J Clin Microbiol Infect Dis. 2018;37(8):1521-9.
27. Khairalla AS, Wasfi R, Ashour HM. Carriage frequency, phenotypic, and genotypic characteristics of methicillin-resistant Staphylococcus aureus isolated from dental health-care personnel, patients, and environment. Sci Rep. 2017;7(1):7390.
28. Hefzy EM, Hassan GM, Abd El Reheem F. Detection of Panton-Valentine Leukocidin-Positive Methicillin-Resistant Staphylococcus aureus Nasal Carriage among Egyptian Health Care Workers. Surg Infect (Larchmt). 2016;17(3):369-75.
29. Djoudi F, Benallaoua S, Aleo A, Touati A, Challal M, Bonura C, et al. Descriptive epidemiology of nasal carriage of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus among patients admitted to two healthcare facilities in Algeria. Microb Drug Resist. 2015;21(2):218-23.
30. Al-Bakri AG, Al-Hadithi H, Kasabri V, Othman G, Kriegeskorte A, Becker K. The epidemiology and molecular characterization of methicillin-resistant staphylococci sampled from a healthy Jordanian population. Epidemiol Infect. 2013;141(11):2384-91.
31. Biber A, Abuelaish I, Rahav G, Raz M, Cohen L, Valinsky L, et al. A typical hospital-acquired methicillin-resistant Staphylococcus aureus clone is widespread in the community in the Gaza strip. PLoS One. 2012;7(8):e42864.
32. Alfouzan W, Dhar R, Udo E. Genetic Lineages of Methicillin-Resistant Staphylococcus aureus Acquired during Admission to an Intensive Care Unit of a General Hospital. Med Princ Pract. 2017;26(2):113-7.
33. Udo EE, Boswihi SS, Al-Sweih N. High prevalence of toxic shock syndrome toxin-producing epidemic methicillin-resistant Staphylococcus aureus 15 (EMRSA-15) strains in Kuwait hospitals. New Microbes New Infect. 2016;12:24-30.
34. Al-Tawfiq JA. Incidence and epidemiology of methicillin-resistant Staphylococcus aureus infection in a Saudi Arabian Hospital, 1999-2003. Infect Control Hosp Epidemiol. 2006;27(10):1137-9.
35. Eed EM, Ghonaim MM, Hussein YM, Al-Shehri SS, Khalifa AS. Molecular characterisation of Panton-Valentine leucocidin-producing methicillin-resistant Staphylococcus aureus clones isolated from the main hospitals in Taif, KSA. Indian J Med Microbiol. 2016;34(4):476-82.
36. Asghar AH. Molecular characterization of methicillin-resistant Staphylococcus aureus isolated from tertiary care hospitals. Pak J Med Sci. 2014;30(4):698-702.
37. Sonnevend Á BI, Alkaabi M, Jumaa P, Al Haj M, Ghazawi A, Akawi N, Jouhar FS, Hamadeh MB, Pál T. Change in meticillin-resistant Staphylococcus aureus clones at a tertiary care hospital in the United Arab Emirates over a 5-year period. J Clin Pathol 2012;65(2):178-82.
38. Al Jalaf M, Fadali H, Alanee R, Najjar F, Al Deesi Z, Seliem RM, et al. Methicillin resistant Staphylococcus Aureus in emergency department patients in the United Arab Emirates. BMC Emerg Med. 2018;18(1):12.
39. Al-Yaqoubi M, Elhag K. Susceptibilities of common bacterial isolates from oman to old and new antibiotics. Oman Med J. 2008;23(3):173-8.
40. Al Rahmany D, Albeloushi A, Alreesi I, Alzaabi A, Alreesi M, Pontiggia L, et al. Exploring bacterial resistance in Northern Oman, a foundation for implementing evidence-based antimicrobial stewardship program. Int J Infect Dis. 2019;83:77-82.
41. Khan FY, Elshafie SS, Almaslamani M, Abu-Khattab M, El Hiday AH, Errayes M, et al. Epidemiology of bacteraemia in Hamad general hospital, Qatar: a one year hospital-based study. Travel Med Infect Dis. 2010;8(6):377-87.
42. Haseeb A, Faidah HS, Bakhsh AR, Malki WH, Elrggal ME, Saleem F, et al. Antimicrobial resistance among pilgrims: a retrospective study from two hospitals in Makkah, Saudi Arabia. Int J Infect Dis. 2016;47:92-4.
43. Abdel-Fattah MM. Surveillance of nosocomial infections at a Saudi Arabian military hospital for a one-year period. Ger Med Sci. 2005;3:Doc06.
44. Bukharie HA. Increasing threat of community-acquired methicillin-resistant Staphylococcus aureus. Am J Med Sci. 2010;340(5):378-81.
45. Khanfar H, Senok A, Anani A, Zinkevich V. Methicillin-resistant Staphylococcus aureus transmission in a low-prevalence healthcare setting. J Infect Public Health. 2012;5(4):311-6.
46. Balkhy HH, Memish ZA, Almuneef MA, Cunningham GC, Francis C, Fong KC, et al. Methicillin-resistant Staphylococcus aureus: a 5-year review of surveillance data in a tertiary care hospital in Saudi Arabia. Infect Control Hosp Epidemiol. 2007;28(8):976-82.
47. Al Laham N, Mediavilla JR, Chen L, Abdelateef N, Elamreen FA, Ginocchio CC, et al. MRSA clonal complex 22 strains harboring toxic shock syndrome toxin (TSST-1) are endemic in the primary hospital in Gaza, Palestine. PLoS One. 2015;10(3):e0120008.
48. Al-Zoubi MS, Al-Tayyar IA, Hussein E, Jabali AA, Khudairat S. Antimicrobial susceptibility pattern of Staphylococcus aureus isolated from clinical specimens in Northern area of Jordan. Iran J Microbiol. 2015;7(5):265-72.
49. Bazzoun DA, Harastani HH, Shehabi AA, Tokajian ST. Molecular typing of Staphylococcus aureus collected from a Major Hospital in Amman, Jordan. J Infect Dev Ctries. 2014;8(4):441-7.
50. Tokajian ST, Khalil PA, Jabbour D, Rizk M, Farah MJ, Hashwa FA, et al. Molecular characterization of Staphylococcus aureus in Lebanon. Epidemiol Infect. 2010;138(5):707-12.
51. Chamoun K, Farah M, Araj G, Daoud Z, Moghnieh R, Salameh P, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective nationwide compiled data. Int J Infect Dis. 2016;46:64-70.
52. Araj GF, Avedissian AZ, Ayyash NS, Bey HA, El Asmar RG, Hammoud RZ, et al. A reflection on bacterial resistance to antimicrobial agents at a major tertiary care center in Lebanon over a decade. J Med Liban. 2012;60(3):125-35.
53. Co EM, Keen EF, 3rd, Aldous WK. Prevalence of methicillin-resistant staphylococcus aureus in a combat support hospital in Iraq. Mil Med. 2011;176(1):89-93.
54. Roberts SS, Kazragis RJ. Methicillin-resistant Staphylococcus aureus infections in U.S. service members deployed to Iraq. Mil Med. 2009;174(4):408-11.
55. Babakir-Mina M, Othman N, Najmuldeen HH, Noori CK, Fatah CF, Perno CF, et al. Antibiotic susceptibility of vancomyin and nitrofurantoin in Staphylococcus aureus isolated from burnt patients in Sulaimaniyah, Iraqi Kurdistan. New Microbiol. 2012;35(4):439-46.
56. Sobhy N, Aly F, Abd El Kader O, Ghazal A, Elbaradei A. Community-acquired methicillin-resistant Staphylococcus aureus from skin and soft tissue infections (in a sample of Egyptian population): analysis of mec gene and staphylococcal cassette chromosome. Braz J Infect Dis. 2012;16(5):426-31.
57. Abdel-Maksoud M, El-Shokry M, Ismail G, Hafez S, El-Kholy A, Attia E, et al. Methicillin-Resistant Staphylococcus aureus Recovered from Healthcare- and Community-Associated Infections in Egypt. Int J Bacteriol. 2016;2016:5751785.
58. Abd El-Hamid MI, Bendary MM. Comparative phenotypic and genotypic discrimination of methicillin resistant and susceptible Staphylococcus aureus in Egypt. Cell Mol Biol (Noisy-le-grand). 2015;61(4):101-12.
59. Bendary MM, Solyman SM, Azab MM, Mahmoud NF, Hanora AM. Characterization of Methicillin Resistant Staphylococcus aureus isolated from human and animal samples in Egypt. Cell Mol Biol (Noisy-le-grand). 2016;62(2):94-100.
60. Alioua MA, Labid A, Amoura K, Bertine M, Gacemi-Kirane D, Dekhil M. Emergence of the European ST80 clone of community-associated methicillin-resistant Staphylococcus aureus as a cause of healthcare-associated infections in Eastern Algeria. Med Mal Infect. 2014;44(4):180-3.
61. Djoudi F, Bonura C, Benallaoua S, Touati A, Touati D, Aleo A, et al. Panton-Valentine leukocidin positive sequence type 80 methicillin-resistant Staphylococcus aureus carrying a staphylococcal cassette chromosome mec type IVc is dominant in neonates and children in an Algiers hospital. New Microbiol. 2013;36(1):49-55.
62. Antri K, Rouzic N, Dauwalder O, Boubekri I, Bes M, Lina G, et al. High prevalence of methicillin-resistant Staphylococcus aureus clone ST80-IV in hospital and community settings in Algiers. Clin Microbiol Infect. 2011;17(4):526-32.
63. Rebiahi SA, Abdelouahid DE, Rahmoun M, Abdelali S, Azzaoui H. Emergence of vancomycin-resistant Staphylococcus aureus identified in the Tlemcen university hospital (North-West Algeria). Med Mal Infect. 2011;41(12):646-51.
64. Djahmi N, Messad N, Nedjai S, Moussaoui A, Mazouz D, Richard JL, et al. Molecular epidemiology of Staphylococcus aureus strains isolated from inpatients with infected diabetic foot ulcers in an Algerian University Hospital. Clin Microbiol Infect. 2013;19(9):E398-404.
65. Bouchami O, Achour W, Ben Hassen A. Typing of staphylococcal cassette chromosome mec encoding methicillin resistance in Staphylococcus aureus strains isolated at the bone marrow transplant centre of Tunisia. Curr Microbiol. 2009;59(4):380-5.
66. Mesrati I, Saïdani M, Ennigrou S, Zouari B, Ben Redjeb S. Clinical isolates of Pantone-Valentine leucocidin- and gamma-haemolysin-producing Staphylococcus aureus: prevalence and association with clinical infections. J Hosp Infect. 2010;75(4):265-8.
67. Elhani D, Gharsa H, Kalai D, Lozano C, Gomez P, Boutheina J, et al. Clonal lineages detected amongst tetracycline-resistant meticillin-resistant Staphylococcus aureus isolates of a Tunisian hospital, with detection of lineage ST398. J Med Microbiol. 2015;64(6):623-9.
68. Alreshidi MA, Alsalamah AA, Hamat RA, Neela V, Alshrari AS, Atshan SS, et al. Genetic variation among methicillin-resistant Staphylococcus aureus isolates from cancer patients in Saudi Arabia. Eur J Clin Microbiol Infect Dis. 2013;32(6):755-61.
69. Monecke S, Skakni L, Hasan R, Ruppelt A, Ghazal SS, Hakawi A, et al. Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia. BMC Microbiol. 2012;12:146.
70. Senok A, Ehricht R, Monecke S, Al-Saedan R, Somily A. Molecular characterization of methicillin-resistant Staphylococcus aureus in nosocomial infections in a tertiary-care facility: emergence of new clonal complexes in Saudi Arabia. New Microbes New Infect. 2016;14:13-8.
71. Eed EM, Ghonaim MM, Hussein YM, Saber TM, Khalifa AS. Phenotypic and molecular characterization of HA-MRSA in Taif hospitals, Saudi Arabia. J Infect Dev Ctries. 2015;9(3):298-303.
72. Boswihi SS, Udo EE, Al-Sweih N. Shifts in the Clonal Distribution of Methicillin-Resistant Staphylococcus aureus in Kuwait Hospitals: 1992-2010. PLoS One. 2016;11(9):e0162744.
73. Udo EE, O'Brien FG, Al-Sweih N, Noronha B, Matthew B, Grubb WB. Genetic lineages of community-associated methicillin-resistant Staphylococcus aureus in Kuwait hospitals. J Clin Microbiol. 2008;46(10):3514-6.
74. Moussa I, Kabli SA, Hemeg HA, Al-Garni SM, Shibl AM. A novel multiplex PCR for molecular characterization of methicillin resistant Staphylococcus aureus recovered from Jeddah, Kingdom of Saudi Arabia. Indian J Med Microbiol. 2012;30(3):296-301.
75. Boswihi SS, Udo EE, Monecke S, Mathew B, Noronha B, Verghese T, et al. Emerging variants of methicillin-resistant Staphylococcus aureus genotypes in Kuwait hospitals. PLoS One. 2018;13(4):e0195933.
76. Alfouzan W, Udo EE, Modhaffer A, Alosaimi A. Molecular Characterization of Methicillin- Resistant Staphylococcus aureus in a Tertiary Care hospital in Kuwait. Sci Rep. 2019;9(1):18527.
77. Udo EE, Boswihi SS. Antibiotic Resistance Trends in Methicillin-Resistant Staphylococcus aureus Isolated in Kuwait Hospitals: 2011-2015. Med Princ Pract. 2017;26(5):485-90.
78. Udo EE, Sarkhoo E. The dissemination of ST80-SCCmec-IV community-associated methicillin resistant Staphylococcus aureus clone in Kuwait hospitals. Ann Clin Microbiol Antimicrob. 2010;9:31.
79. Dash N, Panigrahi D, Al Zarouni M, Yassin F, Al-Shamsi M. Incidence of community-acquired methicillin-resistant Staphylococcus aureus carrying Pantone-Valentine leucocidin gene at a referral hospital in United Arab Emirates. APMIS. 2014;122(4):341-6.
80. Huang XZ, Cash DM, Chahine MA, Van Horn GT, Erwin DP, McKay JT, et al. Methicillin-resistant Staphylococcus aureus infection in combat support hospitals in three regions of Iraq. Epidemiol Infect. 2011;139(7):994-7.
81. Harastani HH, Araj GF, Tokajian ST. Molecular characteristics of Staphylococcus aureus isolated from a major hospital in Lebanon. Int J Infect Dis. 2014;19:33-8.
82. Basset P, Amhis W, Blanc DS. Changing molecular epidemiology of methicillin-resistant Staphylococcus aureus in an Algerian hospital. J Infect Dev Ctries. 2015;9(2):206-9.
83. Ouchenane Z, Smati F, Rolain JM, Raoult D. Molecular characterization of methicillin-resistant Staphylococcus aureus isolates in Algeria. Pathol Biol (Paris). 2011;59(6):e129-32.
84. Mariem BJ, Ito T, Zhang M, Jin J, Li S, Ilhem BB, et al. Molecular characterization of methicillin-resistant Panton-valentine leukocidin positive staphylococcus aureus clones disseminating in Tunisian hospitals and in the community. BMC Microbiol. 2013;13:2.
85. Moussa I, Shibl AM. Molecular characterization of methicillin-resistant Staphylococcus aureus recovered from outpatient clinics in Riyadh, Saudi Arabia. Saudi Med J. 2009;30(5):611-7.
86. Baddour MM, Abuelkheir MM, Fatani AJ. Trends in antibiotic susceptibility patterns and epidemiology of MRSA isolates from several hospitals in Riyadh, Saudi Arabia. Ann Clin Microbiol Antimicrob. 2006;5:30.
87. Udo EE, Panigrahi D, Jamsheer AE. Molecular typing of methicillin-resistant Staphylococcus aureus isolated in a Bahrain hospital. Med Princ Pract. 2008;17(4):308-14.
88. Harastani HH, Tokajian ST. Community-associated methicillin-resistant Staphylococcus aureus clonal complex 80 type IV (CC80-MRSA-IV) isolated from the Middle East: a heterogeneous expanding clonal lineage. PLoS One. 2014;9(7):e103715.
89. Tiemersma EW, Bronzwaer SL, Lyytikainen O, Degener JE, Schrijnemakers P, Bruinsma N, et al. Methicillin-resistant Staphylococcus aureus in Europe, 1999-2002. Emerg Infect Dis. 2004;10(9):1627-34.
90. Cirlan M, Saad M, Coman G, Bilal NE, Elbashier AM, Kreft D, et al. International spread of major clones of methicillin resistant Staphylococcus aureus: nosocomial endemicity of multi locus sequence type 239 in Saudi Arabia and Romania. Infect Genet Evol. 2005;5(4):335-9.
91. Weber S, Ehricht R, Slickers P et al. Genetic fingerprinting of MRSA from Abu Dhabi. ECCMID: 2010, Vienna; 2010.
92. Teixeira LA, Resende CA, Ormonde LR, Rosenbaum R, Figueiredo AM, de Lencastre H, et al. Geographic spread of epidemic multiresistant Staphylococcus aureus clone in Brazil. J Clin Microbiol. 1995;33(9):2400-4.
93. Aires De Sousa M, Miragaia M, Sanches IS, Avila S, Adamson I, Casagrande ST, et al. Three-year assessment of methicillin-resistant Staphylococcus aureus clones in Latin America from 1996 to 1998. J Clin Microbiol. 2001;39(6):2197-205.
94. Corso A, Santos Sanches I, Aires de Sousa M, Rossi A, de Lencastre H. Spread of a methicillin-resistant and multiresistant epidemic clone of Staphylococcus aureus in Argentina. Microb Drug Resist. 1998;4(4):277-88.
95. Fatholahzadeh B, Emaneini M, Aligholi M, Gilbert G, Taherikalani M, Jonaidi N, et al. Molecular characterization of methicillin-resistant Staphylococcus aureus clones from a teaching hospital in Tehran. Jpn J Infect Dis. 2009;62(4):309-11.
96. Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, Tiensasitorn C, et al. Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother. 2006;50(3):1001-12.
97. Chen H, Liu Y, Jiang X, Chen M, Wang H. Rapid change of methicillin-resistant Staphylococcus aureus clones in a Chinese tertiary care hospital over a 15-year period. Antimicrob Agents Chemother. 2010;54(5):1842-7.
98. D'Souza N, Rodrigues C, Mehta A. Molecular characterization of methicillin-resistant Staphylococcus aureus with emergence of epidemic clones of sequence type (ST) 22 and ST 772 in Mumbai, India. J Clin Microbiol. 2010;48(5):1806-11.
99. Peck KR, Baek JY, Song JH, Ko KS. Comparison of genotypes and enterotoxin genes between Staphylococcus aureus isolates from blood and nasal colonizers in a Korean hospital. J Korean Med Sci. 2009;24(4):585-91.
100. Ip M, Yung RW, Ng TK, Luk WK, Tse C, Hung P, et al. Contemporary methicillin-resistant Staphylococcus aureus clones in Hong Kong. J Clin Microbiol. 2005;43(10):5069-73.
101. Coombs GW, Nimmo GR, Bell JM, Huygens F, O'Brien FG, Malkowski MJ, et al. Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia. J Clin Microbiol. 2004;42(10):4735-43.
102. Howden BP, Seemann T, Harrison PF, McEvoy CR, Stanton JA, Rand CJ, et al. Complete genome sequence of Staphylococcus aureus strain JKD6008, an ST239 clone of methicillin-resistant Staphylococcus aureus with intermediate-level vancomycin resistance. J Bacteriol. 2010;192(21):5848-9.
103. Baranovich T, Zaraket H, Shabana, II, Nevzorova V, Turcutyuicov V, Suzuki H. Molecular characterization and susceptibility of methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from hospitals and the community in Vladivostok, Russia. Clin Microbiol Infect. 2010;16(6):575-82.
104. de Lencastre H, Severina EP, Milch H, Thege MK, Tomasz A. Wide geographic distribution of a unique methicillin-resistant Staphylococcus aureus clone in Hungarian hospitals. Clin Microbiol Infect. 1997;3(3):289-96.
105. Alp E, Klaassen CH, Doganay M, Altoparlak U, Aydin K, Engin A, et al. MRSA genotypes in Turkey: persistence over 10 years of a single clone of ST239. J Infect. 2009;58(6):433-8.
106. Melter O, Aires de Sousa M, Urbaskova P, Jakubu V, Zemlickova H, de Lencastre H. Update on the major clonal types of methicillin-resistant Staphylococcus aureus in the Czech Republic. J Clin Microbiol. 2003;41(11):4998-5005.
107. Monecke S, Jatzwauk L, Weber S, Slickers P, Ehricht R. DNA microarray-based genotyping of methicillin-resistant Staphylococcus aureus strains from Eastern Saxony. Clin Microbiol Infect. 2008;14(6):534-45.
108. Campanile F, Bongiorno D, Borbone S, Stefani S. Hospital-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) in Italy. Ann Clin Microbiol Antimicrob. 2009;8:22.
109. Aires de Sousa M, Bartzavali C, Spiliopoulou I, Sanches IS, Crisostomo MI, de Lencastre H. Two international methicillin-resistant Staphylococcus aureus clones endemic in a university hospital in Patras, Greece. J Clin Microbiol. 2003;41(5):2027-32.
110. Aires de Sousa M, Sanches IS, Ferro ML, Vaz MJ, Saraiva Z, Tendeiro T, et al. Intercontinental spread of a multidrug-resistant methicillin-resistant Staphylococcus aureus clone. J Clin Microbiol. 1998;36(9):2590-6.
111. Scicluna EA, Shore AC, Thurmer A, Ehricht R, Slickers P, Borg MA, et al. Characterisation of MRSA from Malta and the description of a Maltese epidemic MRSA strain. Eur J Clin Microbiol Infect Dis. 2010;29(2):163-70.
112. Cuevas O, Cercenado E, Bouza E, Castellares C, Trincado P, Cabrera R, et al. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Spain: a multicentre prevalence study (2002). Clin Microbiol Infect. 2007;13(3):250-6.
113. Conceicao T, Aires-de-Sousa M, Fuzi M, Toth A, Paszti J, Ungvari E, et al. Replacement of methicillin-resistant Staphylococcus aureus clones in Hungary over time: a 10-year surveillance study. Clin Microbiol Infect. 2007;13(10):971-9.
114. Shore A, Rossney AS, Keane CT, Enright MC, Coleman DC. Seven novel variants of the staphylococcal chromosomal cassette mec in methicillin-resistant Staphylococcus aureus isolates from Ireland. Antimicrob Agents Chemother. 2005;49(5):2070-83.
115. Ben Nejma M, Mastouri M, Bel Hadj Jrad B, Nour M. Characterization of ST80 Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus clone in Tunisia. Diagn Microbiol Infect Dis. 2013;77(1):20-4.
116. Harbarth S, Francois P, Shrenzel J, Fankhauser-Rodriguez C, Hugonnet S, Koessler T, et al. Community-associated methicillin-resistant Staphylococcus aureus, Switzerland. Emerg Infect Dis. 2005;11(6):962-5.
117. Enany S, Yaoita E, Yoshida Y, Enany M, Yamamoto T. Molecular characterization of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus isolates in Egypt. Microbiol Res. 2010;165(2):152-62.
118. Bekkhoucha SN, Cady A, Gautier P, Itim F, Donnio PY. A portrait of Staphylococcus aureus from the other side of the Mediterranean Sea: molecular characteristics of isolates from Western Algeria. Eur J Clin Microbiol Infect Dis. 2009;28(5):553-5.
119. Fossum AE, Bukholm G. Increased incidence of methicillin-resistant Staphylococcus aureus ST80, novel ST125 and SCCmecIV in the south-eastern part of Norway during a 12-year period. Clin Microbiol Infect. 2006;12(7):627-33.
120. Witte W, Braulke C, Cuny C, Strommenger B, Werner G, Heuck D, et al. Emergence of methicillin-resistant Staphylococcus aureus with Panton-Valentine leukocidin genes in central Europe. Eur J Clin Microbiol Infect Dis. 2005;24(1):1-5.
121. Tristan A, Bes M, Meugnier H, Lina G, Bozdogan B, Courvalin P, et al. Global distribution of Panton-Valentine leukocidin--positive methicillin-resistant Staphylococcus aureus, 2006. Emerg Infect Dis. 2007;13(4):594-600.
122. Krziwanek K, Luger C, Sammer B, Stumvoll S, Stammler M, Metz-Gercek S, et al. PVL-positive MRSA in Austria. Eur J Clin Microbiol Infect Dis. 2007;26(12):931-5.
123. Faria NA, Oliveira DC, Westh H, Monnet DL, Larsen AR, Skov R, et al. Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide study in a country with low prevalence of MRSA infection. J Clin Microbiol. 2005;43(4):1836-42.
124. Dauwalder O, Lina G, Durand G, Bes M, Meugnier H, Jarlier V, et al. Epidemiology of invasive methicillin-resistant Staphylococcus aureus clones collected in France in 2006 and 2007. J Clin Microbiol. 2008;46(10):3454-8.
125. Monecke S, Slickers P, Hotzel H, Richter-Huhn G, Pohle M, Weber S, et al. Microarray-based characterisation of a Panton-Valentine leukocidin-positive community-acquired strain of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect. 2006;12(8):718-28.
126. Vourli S, Perimeni D, Makri A, Polemis M, Voyiatzi A, Vatopoulos A. Community acquired MRSA infections in a paediatric population in Greece. Euro Surveill. 2005;10(5):78-9.
127. Rossney AS, Lawrence MJ, Morgan PM, Fitzgibbon MM, Shore A, Coleman DC, et al. Epidemiological typing of MRSA isolates from blood cultures taken in Irish hospitals participating in the European Antimicrobial Resistance Surveillance System (1999-2003). Eur J Clin Microbiol Infect Dis. 2006;25(2):79-89.
128. Stam-Bolink EM, Mithoe D, Baas WH, Arends JP, Moller AV. Spread of a methicillin-resistant Staphylococcus aureus ST80 strain in the community of the northern Netherlands. Eur J Clin Microbiol Infect Dis. 2007;26(10):723-7.
129. Hanssen AM, Fossum A, Mikalsen J, Halvorsen DS, Bukholm G, Sollid JU. Dissemination of community-acquired methicillin-resistant Staphylococcus aureus clones in northern Norway: sequence types 8 and 80 predominate. J Clin Microbiol. 2005;43(5):2118-24.
130. Conceicao T, Aires-de-Sousa M, Pona N, Brito MJ, Barradas C, Coelho R, et al. High prevalence of ST121 in community-associated methicillin-susceptible Staphylococcus aureus lineages responsible for skin and soft tissue infections in Portuguese children. Eur J Clin Microbiol Infect Dis. 2011;30(2):293-7.
131. Fang H, Hedin G, Li G, Nord CE. Genetic diversity of community-associated methicillin-resistant Staphylococcus aureus in southern Stockholm, 2000-2005. Clin Microbiol Infect. 2008;14(4):370-6.
132. Otter JA, French GL. The emergence of community-associated methicillin-resistant Staphylococcus aureus at a London teaching hospital, 2000-2006. Clin Microbiol Infect. 2008;14(7):670-6.
133. Holmes A, Ganner M, McGuane S, Pitt TL, Cookson BD, Kearns AM. Staphylococcus aureus isolates carrying Panton-Valentine leucocidin genes in England and Wales: frequency, characterization, and association with clinical disease. J Clin Microbiol. 2005;43(5):2384-90.
134. Aires-de-Sousa M, Correia B, de Lencastre H, Multilaboratory Project C. Changing patterns in frequency of recovery of five methicillin-resistant Staphylococcus aureus clones in Portuguese hospitals: surveillance over a 16-year period. J Clin Microbiol. 2008;46(9):2912-7.
135. Shore AC, Rossney AS, Kinnevey PM, Brennan OM, Creamer E, Sherlock O, et al. Enhanced discrimination of highly clonal ST22-methicillin-resistant Staphylococcus aureus IV isolates achieved by combining spa, dru, and pulsed-field gel electrophoresis typing data. J Clin Microbiol. 2010;48(5):1839-52.
136. Conceicao T, Tavares A, Miragaia M, Hyde K, Aires-de-Sousa M, de Lencastre H. Prevalence and clonality of methicillin-resistant Staphylococcus aureus (MRSA) in the Atlantic Azores islands: predominance of SCCmec types IV, V and VI. Eur J Clin Microbiol Infect Dis. 2010;29(5):543-50.
137. Ellington MJ, Hope R, Livermore DM, Kearns AM, Henderson K, Cookson BD, et al. Decline of EMRSA-16 amongst methicillin-resistant Staphylococcus aureus causing bacteraemias in the UK between 2001 and 2007. J Antimicrob Chemother. 2010;65(3):446-8.
138. Linde H, Wagenlehner F, Strommenger B, Drubel I, Tanzer J, Reischl U, et al. Healthcare-associated outbreaks and community-acquired infections due to MRSA carrying the Panton-Valentine leucocidin gene in southeastern Germany. Eur J Clin Microbiol Infect Dis. 2005;24(6):419-22.
139. Ellington MJ, Ganner M, Warner M, Cookson BD, Kearns AM. Polyclonal multiply antibiotic-resistant methicillin-resistant Staphylococcus aureus with Panton-Valentine leucocidin in England. J Antimicrob Chemother. 2010;65(1):46-50.
140. Rossney AS, Shore AC, Morgan PM, Fitzgibbon MM, O'Connell B, Coleman DC. The emergence and importation of diverse genotypes of methicillin-resistant Staphylococcus aureus (MRSA) harboring the Panton-Valentine leukocidin gene (pvl) reveal that pvl is a poor marker for community-acquired MRSA strains in Ireland. J Clin Microbiol. 2007;45(8):2554-63.
141. Senok A, Somily A, Raji A, Gawlik D, Al-Shahrani F, Baqi S, et al. Diversity of methicillin-resistant Staphylococcus aureus CC22-MRSA-IV from Saudi Arabia and the Gulf region. Int J Infect Dis. 2016;51:31-5.