Abstract
The molecular fingerprinting of a collection of 94 Staphylococcus aureus isolates from patients with osteomyelitis in Argentina was performed. Twenty-three SmaI pulsed-field gel electrophoresis (PFGE) types and 37 spa types were identified. The isolates were assigned to 23 sequence types (STs). The proportion of methicillin-resistant S. aureus (MRSA) isolates was significantly higher among cap5 S. aureus (35/61) compared with cap8 S. aureus (8/33) isolates (p = 0.0025). Twenty-four of the 94 isolates carried the lukS-PV/lukF-PV genes, which were significantly associated to cap5 [(23/38) compared with cap8 S. aureus isolates (1/32) (p = 0.0001)]. Forty of the 94 isolates carried genes of the egc locus (seg/sei). The distribution of seg/sei genes among isolates was related to certain clones. Isolates of the four agr types were found in the S. aureus collection. Whereas agr I isolates were evenly distributed among cap5 and cap8 S. aureus isolates (32/61 and 14/33, respectively), the agr II group was composed of 29 cap5 S. aureus isolates and agr III was composed of 16 cap8 S. aureus isolates. Two clones originally associated to animals (ST 188, 7 isolates and ST 1796, 5 isolates) were associated with chronic osteomyelitis and lack of capsular polysaccharide (CP) production. Loss of CP production remains the single factor among those investigated that is associated with chronic osteomyelitis.
Similar content being viewed by others
References
Wright JA, Nair SP (2010) Interaction of staphylococci with bone. Int J Med Microbiol 300:193
Shams WE, Rapp RP (2004) Methicillin-resistant staphylococcal infections: an important consideration for orthopedic surgeons. Orthopedics 27:565
Costello ME, Huygens F (2011) Diversity of community acquired MRSA carrying the PVL gene in Queensland and New South Wales, Australia. Eur J Clin Microbiol Infect Dis 30:1163
Schuenck RP, Nouér SA, de Winter CO, Cavalcante FS, Scotti TD, Ferreira AL, Giambiagi-de Marval M, dos Santos KR (2009) Polyclonal presence of non-multiresistant methicillin-resistant Staphylococcus aureus isolates carrying SCCmec IV in health care-associated infections in a hospital in Rio de Janeiro, Brazil. Diagn Microbiol Infect Dis 64:434
Que Y-A, Moreillon P (2010) Staphylococcus aureus (including staphylococcal toxic shock). In: Mandell GL, Bennett JE, Dolin R (eds) Principles and practice of infectious diseases. Churchill Livingstone Elsevier, Philadelphia, electronic version
Lee CY, Lee JC (2006) Staphylococcal capsule. In: Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI (eds) Gram-positive pathogens. ASM Press, Washington DC, p 456
Tuchscherr LPN, Löffler B, Buzzola FR, Sordelli DO (2010) Staphylococcus aureus adaptation to the host and persistence: role of loss of capsular polysaccharide expression. Future Microbiol 5:1823
Lattar SM, Tuchscherr LPN, Caccuri RL, Centrón D, Becker K, Alonso CA, Barberis C, Miranda G, Buzzola FR, von Eiff C, Sordelli DO (2009) Capsule expression and genotypic differences among Staphylococcus aureus isolates from patients with chronic or acute osteomyelitis. Infect Immun 77:1968
Tuchscherr LPN, Buzzola FR, Alvarez LP, Caccuri RL, Lee JC, Sordelli DO (2005) Capsule-negative Staphylococcus aureus induces chronic experimental mastitis in mice. Infect Immun 73:7932
Tuchscherr LPN, Buzzola FR, Alvarez LP, Lee JC, Sordelli DO (2008) Antibodies to capsular polysaccharide and clumping factor a prevent mastitis and the emergence of unencapsulated and small-colony variants of Staphylococcus aureus in mice. Infect Immun 76:5738
Sordelli DO, Buzzola FR, Gómez MI, Steele-Moore L, Berg D, Gentilini E, Catalano M, Reitz AJ, Tollersrud T, Denamiel G, Jeric P, Lee JC (2000) Capsule expression by bovine isolates of Staphylococcus aureus from Argentina: genetic and epidemiologic analyses. J Clin Microbiol 38:846
Tuchscherr LPN, Gómez MI, Buzzola FR, Calvinho LF, Lee JC, Sordelli DO (2007) Characterization of a new variant of IS257 prevalent among bovine isolates of Staphylococcus aureus in Argentina. Infect Immun 75:5483
Cocchiaro JL, Gómez MI, Risley A, Solinga R, Sordelli DO, Lee JC (2006) Molecular characterization of the capsule locus from non-typeable Staphylococcus aureus. Mol Microbiol 59:948
Cockfield JD, Pathak S, Edgeworth JD, Lindsay JA (2007) Rapid determination of hospital-acquired meticillin-resistant Staphylococcus aureus lineages. J Med Microbiol 56:614
Cierny G, Mader JT (1984) Adult chronic osteomyelitis. Orthopedics 7:1557
Bannerman TL (2003) Staphylococcus, Micrococcus, and other catalase-positive cocci that grow aerobically. In: Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH (eds) Manual of clinical microbiology, 8th edn. ASM Press, Washington DC, p 384
Martineau F, Picard FJ, Roy PH, Ouellette M, Bergeron MG (1998) Species-specific and ubiquitous-DNA-based assays for rapid identification of Staphylococcus aureus. J Clin Microbiol 36:618
Quelle LS, Corso A, Galas M, Sordelli DO (2003) STAR gene restriction profile analysis in epidemiological typing of methicillin-resistant Staphylococcus aureus: description of the new method and comparison with other polymerase chain reaction (PCR)-based methods. Diagn Microbiol Infect Dis 47:455
Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38:1008
Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, Vogel U (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41:5442
Lee JC, Liu MJ, Parsonnet J, Arbeit RD (1990) Expression of type 8 capsular polysaccharide and production of toxic shock syndrome toxin 1 are associated among vaginal isolates of Staphylococcus aureus. J Clin Microbiol 28:2612
Clinical and Laboratory Standards Institute (CLSI) (2006) Performance standards for antimicrobial susceptibility testing, 16th informational supplement, M100-S16. CLSI, Wayne
Clinical and Laboratory Standards Institute (CLSI) (2006) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M7-A7, 7th edn. CLSI, Wayne
Hartman BJ, Tomasz A (1986) Expression of methicillin resistance in heterogeneous strains of Staphylococcus aureus. Antimicrob Agents Chemother 29:85
Milheiriço C, Oliveira DC, de Lencastre H (2007) Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrob Agents Chemother 51:3374
Otsuka T, Saito K, Dohmae S, Takano T, Higuchi W, Takizawa Y, Okubo T, Iwakura N, Yamamoto T (2006) Key adhesin gene in community-acquired methicillin-resistant Staphylococcus aureus. Biochem Biophys Res Commun 346:1234
Gilot P, Lina G, Cochard T, Poutrel B (2002) Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol 40:4060
Fischer A, von Eiff C, Kuczius T, Omoe K, Peters G, Becker K (2007) A quantitative real-time immuno-PCR approach for detection of staphylococcal enterotoxins. J Mol Med (Berl) 85:461
Deurenberg RH, Stobberingh EE (2009) The molecular evolution of hospital- and community-associated methicillin-resistant Staphylococcus aureus. Curr Mol Med 9:100
Luedicke C, Slickers P, Ehricht R, Monecke S (2010) Molecular fingerprinting of Staphylococcus aureus from bone and joint infections. Eur J Clin Microbiol Infect Dis 29:457
Varshney AK, Mediavilla JR, Robiou N, Guh A, Wang X, Gialanella P, Levi MH, Kreiswirth BN, Fries BC (2009) Diverse enterotoxin gene profiles among clonal complexes of Staphylococcus aureus isolates from the Bronx, New York. Appl Environ Microbiol 75:6839
Sola C, Saka HA; Cordoba MRSA Collaborative Study Group, Vindel A, Bocco JL (2008) Emergence and dissemination of a community-associated methicillin-resistant Panton–Valentine leucocidin-positive Staphylococcus aureus clone sharing the sequence type 5 lineage with the most prevalent nosocomial clone in the same region of Argentina. J Clin Microbiol 46:1826
Gardella N, Murzicato S, Di Gregorio S, Cuirolo A, Desse J, Crudo F, Gutkind G, Mollerach M (2011) Prevalence and characterization of methicillin-resistant Staphylococcus aureus among healthy children in a city of Argentina. Infect Genet Evol 11:1066
Sola C, Paganini H, Egea AL, Moyano AJ, Garnero A, Kevric I, Culasso C, Vindel A; Study Group of CA-MRSA in Children, Argentina-2007, Lopardo H, Bocco JL (2012) Spread of epidemic MRSA-ST5-IV clone encoding PVL as a major cause of community onset staphylococcal infections in Argentinean children. PLoS One 7:e30487, Epub 2012 Jan 23
Eady EA, Cove JH (2003) Staphylococcal resistance revisited: community-acquired methicillin resistant Staphylococcus aureus—an emerging problem for the management of skin and soft tissue infections. Curr Opin Infect Dis 16:103
Sung JM, Lloyd DH, Lindsay JA (2008) Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology 154:1949
Köck R, Harlizius J, Bressan N, Laerberg R, Wieler LH, Witte W, Deurenberg RH, Voss A, Becker K, Friedrich AW (2009) Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur J Clin Microbiol Infect Dis 28:1375
Rabello RF, Moreira BM, Lopes RM, Teixeira LM, Riley LW, Castro AC (2007) Multilocus sequence typing of Staphylococcus aureus isolates recovered from cows with mastitis in Brazilian dairy herds. J Med Microbiol 56:1505
Sompolinsky D, Samra Z, Karakawa WW, Vann WF, Schneerson R, Malik Z (1985) Encapsulation and capsular types in isolates of Staphylococcus aureus from different sources and relationship to phage types. J Clin Microbiol 22:828
Hochkeppel HK, Braun DG, Vischer W, Imm A, Sutter S, Staeubli U, Guggenheim R, Kaplan EL, Boutonnier A, Fournier JM (1987) Serotyping and electron microscopy studies of Staphylococcus aureus clinical isolates with monoclonal antibodies to capsular polysaccharide types 5 and 8. J Clin Microbiol 25:526
Na’was T, Hawwari A, Hendrix E, Hebden J, Edelman R, Martin M, Campbell W, Naso R, Schwalbe R, Fattom AI (1998) Phenotypic and genotypic characterization of nosocomial Staphylococcus aureus isolates from trauma patients. J Clin Microbiol 36:414
Verdier I, Durand G, Bes M, Taylor KL, Lina G, Vandenesch F, Fattom AI, Etienne J (2007) Identification of the capsular polysaccharides in Staphylococcus aureus clinical isolates by PCR and agglutination tests. J Clin Microbiol 45:725
Gardella N, Picasso R, Predari SC, Lasala M, Foccoli M, Benchetrit G, Famiglietti A, Catalano M, Mollerach M, Gutkind G (2005) Methicillin-resistant Staphylococcus aureus strains in Buenos Aires teaching hospitals: replacement of the multidrug resistant South American clone by another susceptible to rifampin, minocycline and trimethoprim–sulfamethoxazole. Rev Argent Microbiol 37:156
Robinson DA, Enright MC (2004) Multilocus sequence typing and the evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 10:92
Holden MT, Lindsay JA, Corton C, Quail MA, Cockfield JD, Pathak S, Batra R, Parkhill J, Bentley SD, Edgeworth JD (2010) Genome sequence of a recently emerged, highly transmissible, multi-antibiotic- and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). J Bacteriol 192:888
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 50:1001
Acknowledgments
This study was partially supported by grants from the ANPCyT (Argentina) PICT 10-01039 to D.O.S. and UBACyT (Universidad de Buenos Aires, Argentina) #20020100100347 to D.O.S.; by the BMBF, Germany, 01KI0700 “SkInStaph” to K.B.; and by NIH grant GM080602 to D.A.R. The authors thank Lorena Medina and Brande Beddingfield for their dedicated technical assistance and Claudia Barberis for providing the strains. We declare that none of the authors have any commercial relationships to other associations that might pose a conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lattar, S.M., Tuchscherr, L.P.N., Centrón, D. et al. Molecular fingerprinting of Staphylococcus aureus isolated from patients with osteomyelitis in Argentina and clonal distribution of the cap5(8) genes and of other selected virulence genes. Eur J Clin Microbiol Infect Dis 31, 2559–2566 (2012). https://doi.org/10.1007/s10096-012-1596-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-012-1596-8