Prevalence of resistance and toxin genes in community-acquired and hospital-acquired methicillin-resistant Staphylococcus aureus clinical isolates

Document Type: Original Article

Authors

1 Microbiology Department, Faculty of Science, Ain Shams University, Cairo, Egypt

2 Microbiology Department, Faculty of Pharmacy, Misr International University, Cairo, Egypt

10.22038/ijbms.2020.40260.9534

Abstract

Objective(s): Methicillin-resistant Staphylococcus aureus (MRSA) is one of the major health hazards and became of greater public health concern since the emergence of community-acquired MRSA. This work aimed to study the prevalence of mecA, femA, femB, lukS-PV, lukF-PV (PVL), intI, and intII genes among community-acquired (CA) hospital-acquired (HA) MRSA to increase vigilance in the diagnosis and management of suspected infections.
Materials and Methods: S. aureus isolates recovered from clinical samples were classified into community or hospital-acquired and tested for their antibiotic susceptibility against 19 antibiotics. All isolates were screened for mecA, femA, femB, lukS-PV, lukF-PV, intI, and intII genes. Statistical correlations were carried out.
Results: Out of 338 S. aureus isolates, only 105 were MRSA and classified as 77 CA-MRSA and 28 HA-MRSA. mecA and femA genes were present in all HA-MRSA and CA-MRSA isolates. femB was found in all HA-MRSA and 93.5% of CA-MRSA isolates. PVL genes were detected in 28.6% HA-MRSA isolates and 92.2% CA-MRSA. intI gene was recovered from 60.7% HA-MRSA isolates and 37.7% CA-MRSA isolates while the intII gene recovered from only 10.7% HA-MRSA isolates and 6.5% CA-MRSA.
Conclusion: The high prevalence of MRSA colonizing the groin, axilla, and nose may play a significant role in endogenous infection, re-infection, and also acts as a route for MRSA transmission. mecA and femA genes could be used as a sole and fast step for identification of MRSA, while PVL genes cannot be used as a sole stable marker for CA-MRSA identification.

Keywords


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Simor AE, Goodfellow J, Louie L, Louie M. Evaluation of a new medium; oxacillin resistance screening agar base, for detection of methicillin resistant Staphylococcus aureus from clin specimens. J Clin Microbiol 2001; 39:3422-3422.
Cherkaoui A, Renzi G, François P, Schrenzel J. Comparison of four chromogenic media for culture-based screening of meticillin-resistant Staphylococcus aureus. J Med Microbiol 2007; 56(4): 500-503.
Xie X, Bao Y, Ouyang N, Dai X, Pan K, Chen B, Deng Y, Wu X, Xu F, Li H, Huang S. Molecular epidemiology and characteristic of virulence gene of community-acquired and hospital-acquired methicillin-resistant Staphylococcus aureus isolates in Sun Yat-sen Memorial hospital, Guangzhou, Southern China. BMC Inf Dis 2006;16:339
Nahimana I, Francioli P, Blanc DS. Evaluation of three chromogenic media (MRSA‐ID, MRSA‐Select and CHROMagar MRSA) and ORSAB for surveillance cultures of methicillin‐resistant Staphylococcus aureus. Clin Microbiol Inf 2006;12:1168-1174
Domann E, Hossain H, Füssle R, Chakraborty T. Rapid and reliable detection of multiresistent Staphylococcus aureus (MRSA) by multiplex PCR. Dtsche Med Wochenschr 200; 125:613-618
Farr BM, Jarvis WR. Would active surveillance cultures help control healthcare-related methicillin-resistant Staphylococcus aureus infections?. Inf Cont Hosp Epidemiol 2002;23:65-68
Badawi H, Omar M, Helmi, H. Evaluation of screening method for detection and typing of MRSA strains involved in noscomial spread. Eg J Med Microbiol 2001;10:679-89
Cetinkol Y, Altindiş M, Cetinkaya Z, Aktepe OC. Short communication: Determination of methicillin resistance in Staphylococci with different methods and detection of multiple antibiotic resistance. Mikrobiyol bulteni 2008;42:119-124
Naqao M, Okamto A, Yamada K, Haseqawa T, Haseqawa Y, and Ohta M,. Variations in amount of TSST-1 produced by clinical methicillin resistant Staphylococcus aureus (MRSA) isolates and allelic variation in accessory gene regulator (agr) locus. J. Clin. Microbiol 2009; 10:9-52.
Hsueh PR, Teng LJ, Chen WH, Pan HJ, Chen ML, Chang SC, Lin FY. Increasing prevalence of methicillin-resistant Staphylococcus aureus causing nosocomial infections at a university hospital in Taiwan from 1986 to 2001. Antimicrob Agents Chemother 2004; 48:1361-1364
Francois P, Pittet D, Bento M, Pepey B, Vaudaux P, Lew D, Schrenzel J. Rapid detection of methicillin-resistant Staphylococcus aureus directly from sterile or nonsterile clinical samples by a new molecular assay. J Clin Microbiol 2003; 41:254-260
Nozaki C, Masaki T, Kim SJ, Cruz RS, Bermido CM, Kim KY,  Park C. Comparative prevalence of community-acquired-methicillin-resistant Staphyloccocus aureus (CA-MRSA) among students of Centro Escolar University (Philippines), Kumamoto Health Science University (Japan) and Daegu Health College (Korea). Biomed Res 2015; 26:259-265
Paniagua-Contreras G, Sáinz-Espuñes T, Monroy-Pérez E, Rodríguez-Moctezuma JR, Arenas-Aranda D, Negrete-Abascal E, Vaca S. Virulence markers in Staphylococcus aureus strains isolated from hemodialysis catheters of Mexican patients. Adv Microbiol 2012; 2: 476-487
Li X, Xiong Y, Fan X, Zhong Z, Feng P, Tang H, Zhou T. A study of the regulating gene of femA from methicillin-resistant Staphylococcus aureus clin isolates. J Int Med Res 2008; 36:420-433
Ishihara K, Shimokubo N, Sakagami A, Ueno H, Muramatsu Y, Kadosawa TY, anagisawa C, Hanaki H, Nakajima C, Suzuki Y, Tamura Y. Occurrence and molecular characteristics of methicillin-resistant Staphylococcus aureus and methicillin-resistant Staphylococcus pseudintermedius in an academic veterinary hospital. Appl Env Microbiol 2010; 76:5165-5174
Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infec Dis 2003; 9:978-984
Genestier AL, Michallet MC, Prévost G, Bellot G, Chalabreysse L, Peyrol S,  Vandenesch F. Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils.  J Clin Invest 2005; 115:3117-3127
Li M, Cheung GY, Hu J, Wang D, Joo HS, DeLeo FR, Otto M. Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J Inf Dis 2010; (202):1866-1876
Nield BS, Holmes AJ, Gillings MR, Recchia GD, Mabbutt BC, Nevalainen KH, Stokes, H W. Recovery of new integron classes from environmental DNA. FEMS Microbiol Lett 2001; 195:59-65
Deng Y, Liu J, Peters BM, Chen L, Miao J, Li B, Shirtliff ME. Antimicrobial resistance investigation on Staphylococcus strains in a local hospital in Guangzhou, China, 2001–2010. Microbial Drug Resist 2015; 21:102-104
Xu Z, Li L, Alam MJ, Zhang L, Yamasaki S, Shi L. First confirmation of integron-bearing methicillin-resistant Staphylococcus aureus. Current Microbiol 2008; 57:264-268
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
Collee JG, Miles RS, Watt B. Tests for identification of bacteria. Mackie and McCartney Practical Medical Microbiology 1996; 14:131-49
Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH. American Society for Microbiol, Manual of Clin Microbiol 7th edition ASM Press, Washington, DC, USA 1999
Cappuccino JG, Sherman N. Microbiol, Laboratory manual Person education. INC New Delhi 2004; 282-283
Koneman EW, Allen SD, Janda WM, Schreckenberger PC, Winn-Jr WC.  The gram-positive cocci part II: Streptococci and Streptococcus-like bacteria. Color atlas and textbook of diagnostic Microbiol 4th ed Philadelphia, USA: JB Lippincott 1992; 431-466
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing of Anaerobic Bacteria: Informational Supplement. (CLSI); 2012
Siegel JD, Rhinehart E, Jackson M, Chiarello L, and the Healthcare Infection Control Practices Advisory Committee (CDC). Guideline for isolation precautions: Preventing transmission of infectious agents in healthcare settings 2007. http://wwwcdcgov/ncidod/dhqp/pdf/isolation2007pdf.
Bauer AW, Kirby WM, Sherris JC, Turck, M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966; 45:493-496
National Committee for Clinical Laboratory Standards.  Antimicrobial susceptibility testing. National Committee for Clinical Laboratory Standards (NCCLS) 2017
Zhang K, Sparling J, Chow BL, Elsayed S, Hussain Z, Church DL, Gregson DB, Louie T and Conly JM. New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol. 2004; 42:4947-4955
Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Inf Dis 1999; 29:1128-1132
Udo EE, Al-Sweih N, Dhar R, Dimitrov TS, Mokaddas EM, Johny M, Al-Obaid IA, Gomaa HH, Mobasher LA, Rotimi VO, Al-Asar A. Surveillance of antibacterial resistance in Staphylococcus aureus isolated in Kuwaiti hospitals. Med Principles Practice 2008; 17:71-75
Festus T, Mukesi M, Moyo SR. The distribution of methicillin resistant Staphylococcus aureus isolated at the Namibia Institute of Pathology in WindHoek Namibia. Ind J Med Res Pharm Sci 2016; 3:1-8
Haznedaroğlu T, Öncül O, Hoşbul T, Çavuşlu Ş, Baylan O, Özyurt M. Yatan hastalardan soyutlanan Staphylococcus aureus suşlarında metisilin direnci: Üç Yıllık Trend, TAF. Prev Med Bull 2010; 9:585-590
Becker A, Forster DH, Kniehl E. Oxacillin resistance screening agar base for detection of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2002; 40:4400-4401
Zeeshan M, Jabeen K, Khan E, Irfan S, Ibrahim S, Parween Z, Zafar A. Comparison of different phenotypic methods of detection of methicillin resistance in Staphylococcus aureus with the molecular detection of mecA gene. J Coll Phys Surg Pak 2007; 17:666-670
Stoakes L, Reyes R, Daniel J, Lennox G, John MA, Lannigan R, Hussain Z. Prospective comparison of a new chromogenic medium, MRSA Select, to CHROM agar MRSA and mannitol-salt medium supplemented with oxacillin or cefoxitin for detection of MRSA. J Clin Microbiol 2006; 44:637-639
Ngoyen V, Kitzis J, Chalfine A, Carlet A, Ben A, and Goldstein F. Detection of nasal colonization MRSA: a prospective study comparing real-time genetic amplification assay vs selective chromogenic media. Path. Biologie 2006; 4:285-92.
Nsira SB, Dupuis M, Leclercq R. Evaluation of MRSA Select, a new chromogenic medium for the detection of nasal carriage of methicillin-resistant Staphylococcus aureus. Int J Antimicrob Agents 2006; 27: 561-564
Tiwari HK, Sapkota D, Sen MR. High prevalence of multidrug-resistant MRSA in a tertiary care hospital of northern India. Inf Drug Resist 2008; 1: 57-61.
Yang ES, Tan J, Eells S, Rieg G, Tagudar G, Miller LG. Body site colonization in patients with community‐associated methicillin‐resistant Staphylococcus aureus and other types of S. aureus skin infections. Clin Microbiol and Inf 2010; 16:425-431
Bhatta DR, Cavaco LM, Nath G, Kumar K, Gaur A, Gokhale S. Association of Panton Valentine Leukocidin (PVL) genes with methicillin resistant Staphylococcus aureus (MRSA) in Western Nepal: a matter of concern for community infections (a hospital based prospective study). BMC. Inf Dis 2016; 16:199.
Abdallah, SA, Al-Asfoor KK, Salama, MF, Al-Awadi BM. Prospective analysis methicillin-resistant Staphylococcus aureus and its risk factors. J Global Inf Dis 2013; 5:19-25
Abbas A, Nirwan PS, Srivastava P. Prevalence and antibiogram of hospital acquired-methicillin resistant Staphylococcus aureus and community acquired-methicillin resistant Staphylococcus aureus at a tertiary care hospital National Institute of Medical Sciences. Community Acquir Inf 2015; 2:13-15
Stevenson KB, Searle K, Stoddard G, Samore MH. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci in rural communities, western United States. Emerg Infec Dis 2005; 11:895-903
Huang H, Flynn NM, King JH, Monchaud C, Morita M, Cohen SH. Comparisons of community-associated methicillin-resistant Staphylococcus aureus (MRSA) and hospital-associated MSRA infections in Sacramento, California. J Clin Microbiol 2006; 44:2423-2427
Vysakh PR, Jeya M. A comparative analysis of community acquired and hospital acquired methicillin resistant Staphylococcus aureus. J Clin Diag Res 2013; 7:1339-1342
Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 1991; 29:2240-2244
Sharma VK, Hackbarth CJ, Dickinson TM, Archer GL. Interaction of native and mutant mecI repressors with sequences that regulate mecA, the gene encoding penicillin-binding protein 2a in methicillin-resistant staphylococci. J Bacteriol 1998; 180:2160-2166
Cloney L, Marlowe C, Wong A, Chow R, Bryan R. Rapid detection of mecA in methicillin resistant Staphylococcus aureus using Cycling Probe Technology. Molec Cell Probes 1999; 13:191-197
Wongwanich S, Tishyadhigama P, Paisomboon S, Ohta T, Hayashi H. Epidemiological analysis of methicillin resistant Staphylococcus aureus in Thailand. Southeast Asian J Trop Med Public Health 2000; 31:72-76
Hafez EE, Al-Sohaimy SA, El-Saadani MA. The effect of the mecA gene and its mutant form on the response of S. aureus to the most common antibiotics. Int J Immunol Stud 2009; 1:106-122
Chambers HF, Archer G, Matsuhashi M. Low-level methicillin resistance in strains of Staphylococcus aureus. Antimicrob Agents Chemother 1989; 33:424-428
Ba X, Harrison EM, Edwards GF, Holden MT, Larsen, AR, Petersen A, Holmes MA. Novel mutations in penicillin-binding protein genes in clin Staphylococcus aureus isolates that are methicillin resistant on susceptibility testing but lack the mec gene. J Antimicrob Chemother 2013; 69:594-597
Aziz HW, Al-Dulaimi TH, Al-Marzoqi AH, Ahmed NK. Phenotypic detection of resistance in Staphylococcus aureus isolates: Detection of (mecA and femA) gene in methicillin resistant Staphylococcus aureus (MRSA) by Polymerase Chain Reaction. J Nat Sci Res 2014; 4:112-118
Elhassan MM, Ozbak HA, Hemeg HA, Elmekki MA, Ahmed LM. Absence of the mecA gene in methicillin resistant Staphylococcus aureus isolated from different clinical specimens in Shendi city, Sudan. BioMed Res Int 2015
Ligozzi M, Rossolini GM, Tonin EA, Fontana R. Nonradioactive DNA probe for detection of gene for methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1991; 35:575-578
Hiramatsu K, Kihara H, Yokota T. Analysis of borderline-resistant strains of methicillin-resistant Staphylococcus aureus using polymerase chain reaction. Microbiol Immunol 1992; 36:445-453
Li M, Du X, Villaruz AE, Diep BA, Wang D, Song Y, Tian Y, Hu J, Yu F, Lu Y, Otto M, Otto M. MRSA epidemic linked to a quickly spreading colonization and virulence determinant. Nat Med 2012; 18:816-819
Pournajaf A, Ardebili A, Allah-Ghaemi E, Omidi S, Borhani K, Khodabandeh M, Davarpanah M. Identification of clinical methicillin and mupirocin-resistant Staphylococcus aureus by multiplex-PCR. J Med Bacteriol 2015; 3:52-59.
Rostamzad A, Rostamneia N. Prevalence of the Panton-Valentine Leukocidin Gene in Clin Isolates of Staphylococcus aureus isolated from hospitals the Ilam Province of Iran. Avicenna. J Clin Microbiol Inf 2016; 3: e32691.
Özekinci T, Dal T, Yanık K, Özcan N, Can Ş, Tekin A, Yıldırım HI, Kandemir I. Panton-Valentine leukocidin in community and hospital-acquired Staphylococcus aureus strains. Biotechnol Biotechnol Equip. 2014; 28:1089-1094
Nichol KA, Adam HJ, Roscoe DL, Golding GR, Lagacé-Wiens PR, Hoban DJ, et al. Antimicrobial Resistance Alliance (CARA), Zhanel GG, Hoban DJ, Adam HJ. Changing epidemiology of methicillin-resistant Staphylococcus aureus in Canada. J Antimicrob Chemother 2013; 68:47-55
Collignon P, Gosbell I, Vickery A, Nimmo G, Stylianopoulos T, Gottlieb T. Community-acquired meticillin-resistant Staphylococcus aureus in Australia. Lancet 1989; 352(9122): 145-146
Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, Boyle-Vavra S, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 1998; 279:593-598
Naimi TS, LeDell KH, Boxrud DJ, Groom AV, Steward CD, Johnson SK, Osterholm MT. Epidemiology and clonality of community-acquired methicillin-resistant Staphylococcus aureus in Minnesota, 1996–1998. Clin Inf Dis 2001; 33:990-996
Dufour P, Gillet Y, Bes M, Lina G, Vandenesch F, Floret D, Richet H. Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton-Valentine leukocidin. Clin Inf Dis 2002; 35:819-824
Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, Etienne J. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients.  Lancet 2002; 359:753-759
Boyle-Vavra S, Daum RS. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton–Valentine leukocidin. Lab Investig 2007; 87: 3-9
Shashindran N, Nagasundaram N, Thappa DM, Sistla S. Can Panton Valentine Leukocidin gene and clindamycin susceptibility serve as predictors of community origin of MRSA from skin and soft tissue infections?. J Clin Diagn Res JCDR 2016; 10:DC01
Shallcross LJ, Williams K, Hopkins S, Aldridge RW, Johnson AM, Hayward AC. Panton–Valentine leukocidin associated staphylococcal disease: a cross‐sectional study at a London hospital, England. Clin Microbiol Inf 2010; 16:1644-1648
Cupane L, Pugacova N, Berzina D, Cauce V, Gardovska D, Miklaševics E. Patients with Panton-Valentine leukocidin positive Staphylococcus aureus infections run an increased risk of longer hospitalization. Int J Molec Epidemiol and Genet 2012; 3:48-55.
Ambrozova, H, Maresova V, Fajt M, Pavlicek P, Rohacova H, Machova I, Petras P. The first case of fatal pneumonia caused by Panton–Valentine leukocidin-producing Staphylococcus aureus in an infant in the Czech Republic. Folia Microbiol 2013; 58:225-228
Madiyarov RS, Bektemirov AM, Ibadova GA, Abdukhalilova GK, Khodiev AV, Bodhidatta L, et al. Antimicrobial resistance patterns and prevalence of class 1 and 2 integrons in Shigella flexneri and Shigella sonnei isolated in Uzbekistan. Gut Pathogens 2010; 2:18
Marathe NP, Nagarkar SS, Vaishampayan AA, Rasane MH, Samant SA, Dohe V, et al. High prevalence of class 1 integrons in clin isolates of methicillin-resistant Staphylococcus aureus from India. Ind J Med Microbiol 2015; 33:231-236
Xu Z, Li L, Shi L, Shirtliff ME. Class 1 integron in staphylococci. Molec Biol Rep 2011a; 38: 5261-5279
Xu Z, Li L, Shirtliff ME, Peters BM, Li B, Peng Y, et al. Resistance class 1 integron in clin methicillin resistant Staphylococcus aureus strains in southern China, 2001–2006. Clin Microbiol Inf 2011b; 17:714-718
Goudarzi M, Seyedjavadi SS, Azad M, Goudarzi H, Azimi H. Distribution of spa types, integrons and associated gene cassettes in Staphylococcus aureus strains isolated from intensive care units of hospitals in Tehran, Iran. Arch Clin Inf Dis 2016; 11:e38813
Goudarzi M, Seyedjavadi SS, Nasiri MJ, Goudarzi H, Nia RS, Dabiri H. Molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) strains isolated from patients with bacteremia based on MLST, SCCmec, spa, and agr locus types analysis. Microbial Path 2017; 104:328-335


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Haznedaroğlu T, Öncül O, Hoşbul T, Çavuşlu Ş, Baylan O, Özyurt M. Yatan hastalardan soyutlanan Staphylococcus aureus suşlarında metisilin direnci: Üç Yıllık Trend, TAF. Prev Med Bull 2010; 9:585-590
Becker A, Forster DH, Kniehl E. Oxacillin resistance screening agar base for detection of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2002; 40:4400-4401
Zeeshan M, Jabeen K, Khan E, Irfan S, Ibrahim S, Parween Z, Zafar A. Comparison of different phenotypic methods of detection of methicillin resistance in Staphylococcus aureus with the molecular detection of mecA gene. J Coll Phys Surg Pak 2007; 17:666-670
Stoakes L, Reyes R, Daniel J, Lennox G, John MA, Lannigan R, Hussain Z. Prospective comparison of a new chromogenic medium, MRSA Select, to CHROM agar MRSA and mannitol-salt medium supplemented with oxacillin or cefoxitin for detection of MRSA. J Clin Microbiol 2006; 44:637-639
Ngoyen V, Kitzis J, Chalfine A, Carlet A, Ben A, and Goldstein F. Detection of nasal colonization MRSA: a prospective study comparing real-time genetic amplification assay vs selective chromogenic media. Path. Biologie 2006; 4:285-92.
Nsira SB, Dupuis M, Leclercq R. Evaluation of MRSA Select, a new chromogenic medium for the detection of nasal carriage of methicillin-resistant Staphylococcus aureus. Int J Antimicrob Agents 2006; 27: 561-564
Tiwari HK, Sapkota D, Sen MR. High prevalence of multidrug-resistant MRSA in a tertiary care hospital of northern India. Inf Drug Resist 2008; 1: 57-61.
Yang ES, Tan J, Eells S, Rieg G, Tagudar G, Miller LG. Body site colonization in patients with community‐associated methicillin‐resistant Staphylococcus aureus and other types of S. aureus skin infections. Clin Microbiol and Inf 2010; 16:425-431
Bhatta DR, Cavaco LM, Nath G, Kumar K, Gaur A, Gokhale S. Association of Panton Valentine Leukocidin (PVL) genes with methicillin resistant Staphylococcus aureus (MRSA) in Western Nepal: a matter of concern for community infections (a hospital based prospective study). BMC. Inf Dis 2016; 16:199.
Abdallah, SA, Al-Asfoor KK, Salama, MF, Al-Awadi BM. Prospective analysis methicillin-resistant Staphylococcus aureus and its risk factors. J Global Inf Dis 2013; 5:19-25
Abbas A, Nirwan PS, Srivastava P. Prevalence and antibiogram of hospital acquired-methicillin resistant Staphylococcus aureus and community acquired-methicillin resistant Staphylococcus aureus at a tertiary care hospital National Institute of Medical Sciences. Community Acquir Inf 2015; 2:13-15
Stevenson KB, Searle K, Stoddard G, Samore MH. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci in rural communities, western United States. Emerg Infec Dis 2005; 11:895-903
Huang H, Flynn NM, King JH, Monchaud C, Morita M, Cohen SH. Comparisons of community-associated methicillin-resistant Staphylococcus aureus (MRSA) and hospital-associated MSRA infections in Sacramento, California. J Clin Microbiol 2006; 44:2423-2427
Vysakh PR, Jeya M. A comparative analysis of community acquired and hospital acquired methicillin resistant Staphylococcus aureus. J Clin Diag Res 2013; 7:1339-1342
Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 1991; 29:2240-2244
Sharma VK, Hackbarth CJ, Dickinson TM, Archer GL. Interaction of native and mutant mecI repressors with sequences that regulate mecA, the gene encoding penicillin-binding protein 2a in methicillin-resistant staphylococci. J Bacteriol 1998; 180:2160-2166
Cloney L, Marlowe C, Wong A, Chow R, Bryan R. Rapid detection of mecA in methicillin resistant Staphylococcus aureus using Cycling Probe Technology. Molec Cell Probes 1999; 13:191-197
Wongwanich S, Tishyadhigama P, Paisomboon S, Ohta T, Hayashi H. Epidemiological analysis of methicillin resistant Staphylococcus aureus in Thailand. Southeast Asian J Trop Med Public Health 2000; 31:72-76
Hafez EE, Al-Sohaimy SA, El-Saadani MA. The effect of the mecA gene and its mutant form on the response of S. aureus to the most common antibiotics. Int J Immunol Stud 2009; 1:106-122
Chambers HF, Archer G, Matsuhashi M. Low-level methicillin resistance in strains of Staphylococcus aureus. Antimicrob Agents Chemother 1989; 33:424-428
Ba X, Harrison EM, Edwards GF, Holden MT, Larsen, AR, Petersen A, Holmes MA. Novel mutations in penicillin-binding protein genes in clin Staphylococcus aureus isolates that are methicillin resistant on susceptibility testing but lack the mec gene. J Antimicrob Chemother 2013; 69:594-597
Aziz HW, Al-Dulaimi TH, Al-Marzoqi AH, Ahmed NK. Phenotypic detection of resistance in Staphylococcus aureus isolates: Detection of (mecA and femA) gene in methicillin resistant Staphylococcus aureus (MRSA) by Polymerase Chain Reaction. J Nat Sci Res 2014; 4:112-118
Elhassan MM, Ozbak HA, Hemeg HA, Elmekki MA, Ahmed LM. Absence of the mecA gene in methicillin resistant Staphylococcus aureus isolated from different clinical specimens in Shendi city, Sudan. BioMed Res Int 2015
Ligozzi M, Rossolini GM, Tonin EA, Fontana R. Nonradioactive DNA probe for detection of gene for methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1991; 35:575-578
Hiramatsu K, Kihara H, Yokota T. Analysis of borderline-resistant strains of methicillin-resistant Staphylococcus aureus using polymerase chain reaction. Microbiol Immunol 1992; 36:445-453
Li M, Du X, Villaruz AE, Diep BA, Wang D, Song Y, Tian Y, Hu J, Yu F, Lu Y, Otto M, Otto M. MRSA epidemic linked to a quickly spreading colonization and virulence determinant. Nat Med 2012; 18:816-819
Pournajaf A, Ardebili A, Allah-Ghaemi E, Omidi S, Borhani K, Khodabandeh M, Davarpanah M. Identification of clinical methicillin and mupirocin-resistant Staphylococcus aureus by multiplex-PCR. J Med Bacteriol 2015; 3:52-59.
Rostamzad A, Rostamneia N. Prevalence of the Panton-Valentine Leukocidin Gene in Clin Isolates of Staphylococcus aureus isolated from hospitals the Ilam Province of Iran. Avicenna. J Clin Microbiol Inf 2016; 3: e32691.
Özekinci T, Dal T, Yanık K, Özcan N, Can Ş, Tekin A, Yıldırım HI, Kandemir I. Panton-Valentine leukocidin in community and hospital-acquired Staphylococcus aureus strains. Biotechnol Biotechnol Equip. 2014; 28:1089-1094
Nichol KA, Adam HJ, Roscoe DL, Golding GR, Lagacé-Wiens PR, Hoban DJ, et al. Antimicrobial Resistance Alliance (CARA), Zhanel GG, Hoban DJ, Adam HJ. Changing epidemiology of methicillin-resistant Staphylococcus aureus in Canada. J Antimicrob Chemother 2013; 68:47-55
Collignon P, Gosbell I, Vickery A, Nimmo G, Stylianopoulos T, Gottlieb T. Community-acquired meticillin-resistant Staphylococcus aureus in Australia. Lancet 1989; 352(9122): 145-146
Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, Boyle-Vavra S, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 1998; 279:593-598
Naimi TS, LeDell KH, Boxrud DJ, Groom AV, Steward CD, Johnson SK, Osterholm MT. Epidemiology and clonality of community-acquired methicillin-resistant Staphylococcus aureus in Minnesota, 1996–1998. Clin Inf Dis 2001; 33:990-996
Dufour P, Gillet Y, Bes M, Lina G, Vandenesch F, Floret D, Richet H. Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton-Valentine leukocidin. Clin Inf Dis 2002; 35:819-824
Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, Etienne J. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients.  Lancet 2002; 359:753-759
Boyle-Vavra S, Daum RS. Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton–Valentine leukocidin. Lab Investig 2007; 87: 3-9
Shashindran N, Nagasundaram N, Thappa DM, Sistla S. Can Panton Valentine Leukocidin gene and clindamycin susceptibility serve as predictors of community origin of MRSA from skin and soft tissue infections?. J Clin Diagn Res JCDR 2016; 10:DC01
Shallcross LJ, Williams K, Hopkins S, Aldridge RW, Johnson AM, Hayward AC. Panton–Valentine leukocidin associated staphylococcal disease: a cross‐sectional study at a London hospital, England. Clin Microbiol Inf 2010; 16:1644-1648
Cupane L, Pugacova N, Berzina D, Cauce V, Gardovska D, Miklaševics E. Patients with Panton-Valentine leukocidin positive Staphylococcus aureus infections run an increased risk of longer hospitalization. Int J Molec Epidemiol and Genet 2012; 3:48-55.
Ambrozova, H, Maresova V, Fajt M, Pavlicek P, Rohacova H, Machova I, Petras P. The first case of fatal pneumonia caused by Panton–Valentine leukocidin-producing Staphylococcus aureus in an infant in the Czech Republic. Folia Microbiol 2013; 58:225-228
Madiyarov RS, Bektemirov AM, Ibadova GA, Abdukhalilova GK, Khodiev AV, Bodhidatta L, et al. Antimicrobial resistance patterns and prevalence of class 1 and 2 integrons in Shigella flexneri and Shigella sonnei isolated in Uzbekistan. Gut Pathogens 2010; 2:18
Marathe NP, Nagarkar SS, Vaishampayan AA, Rasane MH, Samant SA, Dohe V, et al. High prevalence of class 1 integrons in clin isolates of methicillin-resistant Staphylococcus aureus from India. Ind J Med Microbiol 2015; 33:231-236
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