Staphylococcal cassette chromosome mec (SCCmec) and arginine catabolic mobile element (ACME) in Staphylococcus epidermidis isolated from prosthetic joint infections

  • B. Hellmark
  • C. Berglund
  • Å. Nilsdotter-Augustinsson
  • M. Unemo
  • B. Söderquist
Article

Abstract

The aim of the present study was to characterise the staphylococcal cassette chromosome mec (SCCmec) in Staphylococcus epidermidis isolated from prosthetic joint infections (PJIs) and, if possible, assign them to any of the presently known SCCmec types. In addition, the isolates were examined for the presence of the arginine catabolic mobile element (ACME). Sixty-one S. epidermidis isolates obtained from PJIs and 24 commensal S. epidermidis isolates were analysed. The mecA gene was detected in 49 of the 61 (80 %) PJI isolates and in four of the 24 (17 %) commensal isolates, and the composition of the SCCmec was further analysed. SCCmec types I and IV were the most common types among the PJI isolates. However, for over half (57 %) of the isolates, it was not possible to assign an SCCmec type. ACME was detected in eight (13 %) of the PJI isolates and in 14 (58 %) of the commensal isolates. The characterisation of the SCCmec elements revealed a large heterogeneity, with a high frequency of isolates carrying more than one type of the ccr gene complex. ACME was more common among the commensal isolates and may represent a survival benefit for S. epidermidis colonising healthy individuals in the community.

References

  1. 1.
    Huebner J, Goldmann DA (1999) Coagulase-negative staphylococci: role as pathogens. Annu Rev Med 50:223–236PubMedCrossRefGoogle Scholar
  2. 2.
    von Eiff C, Peters G, Heilmann C (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2(11):677–685CrossRefGoogle Scholar
  3. 3.
    Zimmerli W, Trampuz A, Ochsner PE (2004) Prosthetic-joint infections. N Engl J Med 351(16):1645–1654PubMedCrossRefGoogle Scholar
  4. 4.
    Vuong C, Otto M (2002) Staphylococcus epidermidis infections. Microbes Infect 4(4):481–489PubMedCrossRefGoogle Scholar
  5. 5.
    Hellmark B, Unemo M, Nilsdotter-Augustinsson A, Söderquist B (2009) Antibiotic susceptibility among Staphylococcus epidermidis isolated from prosthetic joint infections with special focus on rifampicin and variability of the rpoB gene. Clin Microbiol Infect 15(3):238–244PubMedCrossRefGoogle Scholar
  6. 6.
    Otto M (2009) Staphylococcus epidermidis—the ‘accidental’ pathogen. Nat Rev Microbiol 7(8):555–567PubMedCrossRefGoogle Scholar
  7. 7.
    Uçkay I, Harbarth S, Ferry T, Lübbeke A, Emonet S, Hoffmeyer P, Pittet D (2011) Meticillin resistance in orthopaedic coagulase-negative staphylococcal infections. J Hosp Infect 79(3):248–253PubMedCrossRefGoogle Scholar
  8. 8.
    Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, Hiramatsu K (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45(5):1323–1336PubMedCrossRefGoogle Scholar
  9. 9.
    Berglund C, Söderquist B (2008) The origin of a methicillin-resistant Staphylococcus aureus isolate at a neonatal ward in Sweden-possible horizontal transfer of a staphylococcal cassette chromosome mec between methicillin-resistant Staphylococcus haemolyticus and Staphylococcus aureus. Clin Microbiol Infect 14(11):1048–1056PubMedCrossRefGoogle Scholar
  10. 10.
    Hanssen AM, Sollid JU (2007) Multiple staphylococcal cassette chromosomes and allelic variants of cassette chromosome recombinases in Staphylococcus aureus and coagulase-negative staphylococci from Norway. Antimicrob Agents Chemother 51(5):1671–1677PubMedCrossRefGoogle Scholar
  11. 11.
    Berglund C, Ito T, Ikeda M, Ma XX, Söderquist B, Hiramatsu K (2008) Novel type of staphylococcal cassette chromosome mec in a methicillin-resistant Staphylococcus aureus strain isolated in Sweden. Antimicrob Agents Chemother 52(10):3512–3516PubMedCrossRefGoogle Scholar
  12. 12.
    García-Álvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RL, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA (2011) Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11(8):595–603PubMedCrossRefGoogle Scholar
  13. 13.
    Ito T, Ma XX, Takeuchi F, Okuma K, Yuzawa H, Hiramatsu K (2004) Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrob Agents Chemother 48(7):2637–2651PubMedCrossRefGoogle Scholar
  14. 14.
    Li S, Skov RL, Han X, Larsen AR, Larsen J, Sørum M, Wulf M, Voss A, Hiramatsu K, Ito T (2011) Novel types of staphylococcal cassette chromosome mec elements identified in clonal complex 398 methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 55(6):3046–3050PubMedCrossRefGoogle Scholar
  15. 15.
    Ma XX, Ito T, Tiensasitorn C, Jamklang M, Chongtrakool P, Boyle-Vavra S, Daum RS, Hiramatsu K (2002) Novel type of staphylococcal cassette chromosome mec identified in community-acquired methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 46(4):1147–1152PubMedCrossRefGoogle Scholar
  16. 16.
    Oliveira DC, Milheiriço C, de Lencastre H (2006) Redefining a structural variant of staphylococcal cassette chromosome mec, SCCmec type VI. Antimicrob Agents Chemother 50(10):3457–3459PubMedCrossRefGoogle Scholar
  17. 17.
    Shore AC, Deasy EC, Slickers P, Brennan G, O’Connell B, Monecke S, Ehricht R, Coleman DC (2011) Detection of staphylococcal cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1, blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 55(8):3765–3773PubMedCrossRefGoogle Scholar
  18. 18.
    Zhang K, McClure JA, Elsayed S, Conly JM (2009) Novel staphylococcal cassette chromosome mec type, tentatively designated type VIII, harboring class A mec and type 4 ccr gene complexes in a Canadian epidemic strain of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 53(2):531–540PubMedCrossRefGoogle Scholar
  19. 19.
    International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53(12):4961–4967CrossRefGoogle Scholar
  20. 20.
    Lim TT, Chong FN, O’Brien FG, Grubb WB (2003) Are all community methicillin-resistant Staphylococcus aureus related? A comparison of their mec regions. Pathology 35(4):336–343PubMedCrossRefGoogle Scholar
  21. 21.
    Milheiriço C, Oliveira DC, de Lencastre H (2007) Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: ‘SCCmec IV multiplex’. J Antimicrob Chemother 60(1):42–48PubMedCrossRefGoogle Scholar
  22. 22.
    Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, des Etages SA, Jones A, Palazzolo-Ballance AM, Perdreau-Remington F, Sensabaugh GF, DeLeo FR, Chambers HF (2008) The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197(11):1523–1530PubMedCrossRefGoogle Scholar
  23. 23.
    Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-Remington F (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367(9512):731–739PubMedCrossRefGoogle Scholar
  24. 24.
    Miragaia M, de Lencastre H, Perdreau-Remington F, Chambers HF, Higashi J, Sullam PM, Lin J, Wong KI, King KA, Otto M, Sensabaugh GF, Diep BA (2009) Genetic diversity of arginine catabolic mobile element in Staphylococcus epidermidis. PLoS One 4(11):e7722PubMedCrossRefGoogle Scholar
  25. 25.
    Hellmark B, Söderquist B, Unemo M (2009) Simultaneous species identification and detection of rifampicin resistance in staphylococci by sequencing of the rpoB gene. Eur J Clin Microbiol Infect Dis 28(2):183–190PubMedCrossRefGoogle Scholar
  26. 26.
    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):447–456PubMedCrossRefGoogle Scholar
  27. 27.
    Katayama Y, Ito T, Hiramatsu K (2001) Genetic organization of the chromosome region surrounding mecA in clinical staphylococcal strains: role of IS431-mediated mecI deletion in expression of resistance in mecA-carrying, low-level methicillin-resistant Staphylococcus haemolyticus. Antimicrob Agents Chemother 45(7):1955–1963PubMedCrossRefGoogle Scholar
  28. 28.
    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):264–274PubMedCrossRefGoogle Scholar
  29. 29.
    Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM, O’Brien FG, Coombs GW, Pearman JW, Tenover FC, Kapi M, Tiensasitorn C, Ito T, Hiramatsu K (2002) Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 40(11):4289–4294PubMedCrossRefGoogle Scholar
  30. 30.
    Bloemendaal AL, Brouwer EC, Fluit AC (2010) Methicillin resistance transfer from Staphylocccus epidermidis to methicillin-susceptible Staphylococcus aureus in a patient during antibiotic therapy. PLoS One 5(7):e11841PubMedCrossRefGoogle Scholar
  31. 31.
    Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG (2002) The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 99(11):7687–7692PubMedCrossRefGoogle Scholar
  32. 32.
    Hiramatsu K, Cui L, Kuroda M, Ito T (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9(10):486–493PubMedCrossRefGoogle Scholar
  33. 33.
    Nübel U, Roumagnac P, Feldkamp M, Song JH, Ko KS, Huang YC, Coombs G, Ip M, Westh H, Skov R, Struelens MJ, Goering RV, Strommenger B, Weller A, Witte W, Achtman M (2008) Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 105(37):14130–14135PubMedCrossRefGoogle Scholar
  34. 34.
    Robinson DA, Enright MC (2003) Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 47(12):3926–3934PubMedCrossRefGoogle Scholar
  35. 35.
    Miragaia M, Carriço JA, Thomas JC, Couto I, Enright MC, de Lencastre H (2008) Comparison of molecular typing methods for characterization of Staphylococcus epidermidis: proposal for clone definition. J Clin Microbiol 46(1):118–129PubMedCrossRefGoogle Scholar
  36. 36.
    Sivadon V, Rottman M, Quincampoix JC, Prunier E, Le Moal M, de Mazancourt P, Hoffmeyer P, Lortat-Jacob A, Piriou P, Judet T, Bernard L, Gaillard JL (2009) Partial atlE sequencing of Staphylococcus epidermidis strains from prosthetic joint infections. J Clin Microbiol 47(7):2321–2324PubMedCrossRefGoogle Scholar
  37. 37.
    Ibrahem S, Salmenlinna S, Lyytikäinen O, Vaara M, Vuopio-Varkila J (2008) Molecular characterization of methicillin-resistant Staphylococcus epidermidis strains from bacteraemic patients. Clin Microbiol Infect 14(11):1020–1027PubMedCrossRefGoogle Scholar
  38. 38.
    Ruppé E, Barbier F, Mesli Y, Maiga A, Cojocaru R, Benkhalfat M, Benchouk S, Hassaine H, Maiga I, Diallo A, Koumaré AK, Ouattara K, Soumaré S, Dufourcq JB, Nareth C, Sarthou JL, Andremont A, Ruimy R (2009) Diversity of staphylococcal cassette chromosome mec structures in methicillin-resistant Staphylococcus epidermidis and Staphylococcus haemolyticus strains among outpatients from four countries. Antimicrob Agents Chemother 53(2):442–449PubMedCrossRefGoogle Scholar
  39. 39.
    Descloux S, Rossano A, Perreten V (2008) Characterization of new staphylococcal cassette chromosome mec (SCCmec) and topoisomerase genes in fluoroquinolone- and methicillin-resistant Staphylococcus pseudintermedius. J Clin Microbiol 46(5):1818–1823PubMedCrossRefGoogle Scholar
  40. 40.
    Higashide M, Kuroda M, Omura CT, Kumano M, Ohkawa S, Ichimura S, Ohta T (2008) Methicillin-resistant Staphylococcus saprophyticus isolates carrying staphylococcal cassette chromosome mec have emerged in urogenital tract infections. Antimicrob Agents Chemother 52(6):2061–2068PubMedCrossRefGoogle Scholar
  41. 41.
    Ibrahem S, Salmenlinna S, Virolainen A, Kerttula AM, Lyytikäinen O, Jägerroos H, Broas M, Vuopio-Varkila J (2009) Carriage of methicillin-resistant Staphylococci and their SCCmec types in a long-term-care facility. J Clin Microbiol 47(1):32–37PubMedCrossRefGoogle Scholar
  42. 42.
    Miragaia M, Thomas JC, Couto I, Enright MC, de Lencastre H (2007) Inferring a population structure for Staphylococcus epidermidis from multilocus sequence typing data. J Bacteriol 189(6):2540–2552PubMedCrossRefGoogle Scholar
  43. 43.
    Wisplinghoff H, Rosato AE, Enright MC, Noto M, Craig W, Archer GL (2003) Related clones containing SCCmec type IV predominate among clinically significant Staphylococcus epidermidis isolates. Antimicrob Agents Chemother 47(11):3574–3579PubMedCrossRefGoogle Scholar
  44. 44.
    Hellmark B, Söderquist B, Unemo M, Nilsdotter-Augustinsson Å (2012) Comparison of Staphylococcus epidermidis isolated from prosthetic joint infections and commensal isolates in regards to antibiotic susceptibility, agr type, biofilm production, and epidemiology. Int J Med MicrobiolGoogle Scholar
  45. 45.
    Ito T, Okuma K, Ma XX, Yuzawa H, Hiramatsu K (2003) Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist Updat 6(1):41–52PubMedCrossRefGoogle Scholar
  46. 46.
    Barbier F, Lebeaux D, Hernandez D, Delannoy AS, Caro V, François P, Schrenzel J, Ruppé E, Gaillard K, Wolff M, Brisse S, Andremont A, Ruimy R (2011) High prevalence of the arginine catabolic mobile element in carriage isolates of methicillin-resistant Staphylococcus epidermidis. J Antimicrob Chemother 66(1):29–36PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • B. Hellmark
    • 1
  • C. Berglund
    • 2
  • Å. Nilsdotter-Augustinsson
    • 3
  • M. Unemo
    • 1
  • B. Söderquist
    • 1
    • 4
    • 5
  1. 1.Department of Laboratory Medicine, Clinical MicrobiologyÖrebro University HospitalÖrebroSweden
  2. 2.Department of Clinical Microbiology and ChemistryAleris MEDILABTäbySweden
  3. 3.Division of Infectious Diseases, Department of Clinical and Experimental Medicine, Faculty of Health SciencesUniversity of LinköpingLinköpingSweden
  4. 4.Department of Infectious DiseasesÖrebro University HospitalÖrebroSweden
  5. 5.Faculty of Medicine and HealthÖrebro UniversityÖrebroSweden

Personalised recommendations