Abstract
Staphylococcal cassette chromosome mec (SCCmec) typing is essential for investigating the molecular epidemiology of methicillin-resistant Staphylococcus aureus (MRSA). Published assays were often found to be limited in their ability to characterize isolates that were not collected locally. We aimed to develop, test, and implement a molecular method which would enable the SCCmec classification of a large collection of MRSA isolates in a routine clinical laboratory. A multistep working algorithm consisting of two main steps and four additional supplementary steps was developed, using previously reported primers. A total of 1,008 isolates obtained locally, by both clinical and screening cultures, were tested. The majority of isolates (82.54%) could be classified using two main reactions. Overall, our MRSA SCCmec typing strategy was able to classify 917/1,008 (90.97%) of the MRSA isolates. The most predominant was type II SCCmec (41%); a high prevalence of type V SCCmec (16.37%) was also found. PVL gene carriage was found among two type IV SCCmec isolates only. We present a logistically feasible, multistep, MRSA SCCmec typing algorithm which can be used to type a large collection of MRSA isolates. The distinctly higher prevalence of SCCmec type V might reflect a unique MRSA distribution pattern in Israel.
Similar content being viewed by others
References
Deresinski S (2005) Methicillin-resistant Staphylococcus aureus: an evolutionary, epidemiologic, and therapeutic odyssey. Clin Infect Dis 40(4):562–573
Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, Liassine N, Bes M, Greenland T, Reverdy ME, Etienne J (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton–Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9(8):978–984
Hiramatsu K, Watanabe S, Takeuchi F, Ito T, Baba T (2004) Genetic characterization of methicillin-resistant Staphylococcus aureus. Vaccine 22(Suppl 1):S5–S8
Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K (2007) Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother 51(1):264–274
Berglund C, Mölling P, Sjöberg L, Söderquist B (2005) Predominance of staphylococcal cassette chromosome mec (SCCmec) type IV among methicillin-resistant Staphylococcus aureus (MRSA) in a Swedish county and presence of unknown SCCmec types with Panton–Valentine leukocidin genes. Clin Microbiol Infect 11(6):447–456
Huletsky A, Giroux R, Rossbach V, Gagnon M, Vaillancourt M, Bernier M, Gagnon F, Truchon K, Bastien M, Picard FJ, van Belkum A, Ouellette M, Roy PH, Bergeron MG (2004) New real-time PCR assay for rapid detection of methicillin-resistant Staphylococcus aureus directly from specimens containing a mixture of staphylococci. J Clin Microbiol 42(5):1875–1884
Oliveira DC, de Lencastre H (2002) Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 46(7):2155–2161
Chen L, Mediavilla JR, Oliveira DC, Willey BM, de Lencastre H, Kreiswirth BN (2009) Multiplex real-time PCR for rapid staphylococcal cassette chromosome mec typing. J Clin Microbiol 47(11):3692–3706
Shitrit P, Gottesman BS, Katzir M, Kilman A, Ben-Nissan Y, Chowers M (2006) Active surveillance for methicillin-resistant Staphylococcus aureus (MRSA) decreases the incidence of MRSA bacteremia. Infect Control Hosp Epidemiol 27(10):1004–1008
Chmelnitsky I, Navon-Venezia S, Leavit A, Somekh E, Regev-Yochai G, Chowers M, Shitrit P, Carmeli Y (2008) SCCmec and spa types of methicillin-resistant Staphylococcus aureus strains in Israel. Detection of SCCmec type V. Eur J Clin Microbiol Infect Dis 27(5):385–390
Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH (2003) Manual of clinical microbiology, 8th edn. ASM Press, Washington DC
Reischl U, Youssef MT, Kilwinski J, Lehn N, Zhang WL, Karch H, Strockbine NA (2002) Real-time fluorescence PCR assays for detection and characterization of Shiga toxin, intimin, and enterohemolysin genes from Shiga toxin-producing Escherichia coli. J Clin Microbiol 40(7):2555–2565
Zhang K, McClure JA, Elsayed S, Louie T, Conly JM (2005) Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol 43(10):5026–5033
Ito T, Kuwahara K, Hiramatsu K (2001) Staphylococcal cassette chromosome mec (SCCmec) analysis of MRSA. In: Ji Y (ed) Methods in molecular biology. Humana Press, Totowa, New Jersey, pp 87–102
Chung M, Dickinson G, De Lencastre H, Tomasz A (2004) International clones of methicillin-resistant Staphylococcus aureus in two hospitals in Miami, Florida. J Clin Microbiol 42(2):542–547
Cookson BD, Robinson DA, Monk AB, Murchan S, Deplano A, de Ryck R, Struelens MJ, Scheel C, Fussing V, Salmenlinna S, Vuopio-Varkila J, Cuny C, Witte W, Tassios PT, Legakis NJ, van Leeuwen W, van Belkum A, Vindel A, Garaizar J, Haeggman S, Olsson-Liljequist B, Ransjo U, Muller-Premru M, Hryniewicz W, Rossney A, O’Connell B, Short BD, Thomas J, O’Hanlon S, Enright MC (2007) Evaluation of molecular typing methods in characterizing a European collection of epidemic methicillin-resistant Staphylococcus aureus strains: the HARMONY collection. J Clin Microbiol 45(6):1830–1837
Kilic A, Guclu AU, Senses Z, Bedir O, Aydogan H, Basustaoglu AC (2008) Staphylococcal cassette chromosome mec (SCCmec) characterization and Panton–Valentine leukocidin gene occurrence for methicillin-resistant Staphylococcus aureus in Turkey, from 2003 to 2006. Antonie Van Leeuwenhoek 94(4):607–614
Pérez-Roth E, Lorenzo-Díaz F, Batista N, Moreno A, Méndez-Alvarez S (2004) Tracking methicillin-resistant Staphylococcus aureus clones during a 5-year period (1998 to 2002) in a Spanish hospital. J Clin Microbiol 42(10):4649–4656
Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, Tiensasitorn C, Jamklang M, Chavalit T, Song JH, Hiramatsu K (2006) 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 50(3):1001–1012
Amorim ML, Faria NA, Oliveira DC, Vasconcelos C, Cabeda JC, Mendes AC, Calado E, Castro AP, Ramos MH, Amorim JM, de Lencastre H (2007) Changes in the clonal nature and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus isolates associated with spread of the EMRSA-15 clone in a tertiary care Portuguese hospital. J Clin Microbiol 45(9):2881–2888
Hallin M, Denis O, Deplano A, De Ryck R, Crèvecoeur S, Rottiers S, de Mendonça R, Struelens MJ (2008) Evolutionary relationships between sporadic and epidemic strains of healthcare-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 14(7):659–669
Lina G, Durand G, Berchich C, Short B, Meugnier H, Vandenesch F, Etienne J, Enright MC (2006) Staphylococcal chromosome cassette evolution in Staphylococcus aureus inferred from ccr gene complex sequence typing analysis. Clin Microbiol Infect 12(12):1175–1184
Monecke S, Jatzwauk L, Weber S, Slickers P, Ehricht R (2008) DNA microarray-based genotyping of methicillin-resistant Staphylococcus aureus strains from Eastern Saxony. Clin Microbiol Infect 14(6):534–545
Vainio A, Kardén-Lilja M, Ibrahem S, Kerttula AM, Salmenlinna S, Virolainen A, Vuopio-Varkila J (2008) Clonality of epidemic methicillin-resistant Staphylococcus aureus strains in Finland as defined by several molecular methods. Eur J Clin Microbiol Infect Dis 27(7):545–555
Budimir A, Deurenberg RH, Plecko V, Vink C, Kalenic S, Stobberingh EE (2006) Molecular characterization of methicillin-resistant Staphylococcus aureus bloodstream isolates from Croatia. J Antimicrob Chemother 57(2):331–334
Laplana LM, Cepero MA, Ruiz J, Zolezzi PC, Calvo MA, Erazo MC, Gómez-Lus R (2007) Molecular typing of Staphylococcus aureus clinical isolates by pulsed-field gel electrophoresis, staphylococcal cassette chromosome mec type determination and dissemination of antibiotic resistance genes. Int J Antimicrob Agents 30(6):505–513
Blanc DS, Petignat C, Wenger A, Kuhn G, Vallet Y, Fracheboud D, Trachsel S, Reymond M, Troillet N, Siegrist HH, Oeuvray S, Bes M, Etienne J, Bille J, Francioli P, Zanetti G (2007) Changing molecular epidemiology of methicillin-resistant Staphylococcus aureus in a small geographic area over an eight-year period. J Clin Microbiol 45(11):3729–3736
Acknowledgments
We would like to thank Dr. S. Navon-Venezia from the Tel Aviv Sourasky Medical Center, Israel, and Dr. Michele Bes from the National Reference Laboratory for Staphylococci, INSERM E0230, IFR62, Faculté de Médecine Laennec, Lyon, France, for kindly providing the control strains.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Alon, D., Abd-Elkadir, F., Chowers, M. et al. MRSA SCCmec epidemiology in Israel: development and implementation of an MRSA SCCmec typing strategy. Eur J Clin Microbiol Infect Dis 30, 1443–1452 (2011). https://doi.org/10.1007/s10096-011-1243-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-011-1243-9