Virulence Markers in Staphylococcus aureus Strains Isolated from Hemodialysis Catheters of Mexican Patients


Methicillin-resistant Staphylococcus aureus is an increasingly important cause of nosocomial bacterial infections worldwide. S. aureus is responsible for several pathologies, including skin infections, endocarditis, meningitis, deep-tissue ulcers, and sepsis. S. aureus biofilm formation on catheters and other medical devices is a major post-operative concern, because biofilms are often the source of persistent and difficult to treat bacterial infections. While catheter-related S. aureus infections have been reported, the strains responsible for these infections have not been genetically characterized. We genetically characterized S. aureus strains isolated from hemodialysis catheters in Mexican patients. The frequency of 35 genes coding for adhesins, toxins, and other virulence-associated products in the 55 isolated S. aureus strains was determined using PCR, while real-time PCR was used to examine the level of gene expression. Of the 55 S. aureus strains isolated from 109 patients, 45 (81.8%) were determined to be methicillin-resistant. The icaA, rbf, sarA, and agr genes are involved in biofilm formation and bacterial dispersion and were detected in 96.3%, 40.0%, 74.5%, and 100% of S. aureus strains, respectively, and 70.9% of the strains formed a detectable biofilm. Interestingly, 67.2% of the strains contained the icaA, agr, spa, clfA, sdrC, sdrD, sdrE, seg, seh, and sei genes, suggesting that this gene combination is important for successful catheter colonization. The results of this study provide significant insight into the virulence gene make-up of catheter-colonizing S. aureus strains, and will assist in developing a more targeted treatment approach for persistent S. aureus biofilm contamination of medical devices.

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G. Paniagua-Contreras, T. Sáinz-Espuñes, E. Monroy-Pérez, J. Raymundo Rodríguez-Moctezuma, D. Arenas-Aranda, E. Negrete-Abascal and S. Vaca, "Virulence Markers in Staphylococcus aureus Strains Isolated from Hemodialysis Catheters of Mexican Patients," Advances in Microbiology, Vol. 2 No. 4, 2012, pp. 476-487. doi: 10.4236/aim.2012.24061.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] P. Viale and S. Stefani, “Vascular Catheter-Associated Infections: A Microbiological and Therapeutic Update,” Journal of Chemotherapy, Vol. 18, No. 3, 2006, pp. 235-249.
[2] I. M. Gould, “The Clinical Significance of Methicillin-Resistant Staphylococcus aureus,” The Journal of Hospital Infection, Vol. 61, No. 4, 2005, pp. 277-282. doi:10.1016/j.jhin.2005.06.014
[3] Centers for Diseases Control, “Invasive Methicillin-Resistant Staphylococcus aureus Infections among Dialysis Patients—United States, 2005,” Morbidity and Mortality Weekly Report, Vol. 56, No. 9, 2007, pp. 197-199.
[4] F. Gotz, “Staphylococcus and Biofilms,” Molecular Microbiology, Vol. 43, No. 6, 2002, pp. 1367-1378. doi:10.1046/j.1365-2958.2002.02827.x
[5] D. Cue, M. G. Lei, T. T. Luong, L. Kuechenmeister, P. M. Dunman, S. O’Donnell, S. Rowe, J. P. O’Gara and C. Y. Lee, “Rbf Promotes Biofilm Formation by Staphylococcus aureus via Repression of icaR, a Negative Regulator of icaADBC,” Journal of Bacteriology, Vol. 191 No. 20, 2009, pp. 6363-6373. doi:10.1128/JB.00913-09
[6] K. E. Beenken, J. S. Blevins and M. S. Smeltzer, “Mutation of SarA in Staphylococcus aureus Limits Biofilm Formation,” Infection and Immunity, Vol. 71, No. 7, 2003, pp. 4206-4211. doi:10.1128/IAI.71.7.4206-4211.2003
[7] J. Valle, A. Toledo-Arana, C. Berasain, J. M. Ghigo, B. Amorena, J. R. Penadés and I. Lasa, “SarA and Not Sigma-B Is Essential for Biofilm Development by Staphylococcus aureus,” Molecular Microbiology, Vol. 48, No. 4, 2003, pp. 1075-1087. doi:10.1046/j.1365-2958.2003.03493.x
[8] E. Mongodin, O. Bajolet, J. Cutrona, N. Bonnet, F. Dupuit, E. Puchelle and S. de Bentzmann, “Fibronectin-Binding Proteins of Staphylococcus aureus Are Involved in Adherence to Human Airway Epithelium,” Infection and Immunity, Vol. 70, No. 2, 2002, pp. 620-630.
[9] W. Navarre and O. Schneewind, “Surface Proteins of Gram-Positive Bacteria and Mechanisms of Their Targeting to the Cell Wall Envelope,” Microbiology and Molecular Biology Reviews, Vol. 63, No. 1, 1999, pp. 174-229.
[10] S. J. Peacock, N. P. J. Day, M. G. Thomas, A. R. Berendt and T. J. Foster, “Clinical Isolates of Staphylococcus aureus Exhibit Diversity in fnb Genes and Adhesion to Human Fibronectin,” The Journal of Infection, Vol. 41, No. 1, 2000, pp. 23-31. doi:10.1053/jinf.2000.0657
[11] N. Palmqvist, T. Foster, A. Tarkowski and E. Josefsson, “Protein A Is a Virulence Factor in Staphylococcus aureus Arthritis and Septic Death,” Microbial Pathogenesis, Vol. 33, No. 5, 2003, pp. 239-249. doi:10.1006/mpat.2002.0533
[12] S. A. Hienz, T. Schennings, A. Heimdahl and J. L. Flock, “Collagen Binding of Staphylococcus aureus Is a Virulence Factor in Experimental Endocarditis,” The Journal of Infectious Diseases, Vol. 174, No. 1, 1996, pp. 83-88. doi:10.1093/infdis/174.1.83
[13] M. O. Elasri, J. R. Thomas and R. A. Skinner, “Staphylococcus aureus Collagen Adhesin CONTRIBUTES to the Pathogenesis of Osteomyelitis,” Bone, Vol. 30, No. 1, 2002, pp. 275-280. doi:10.1016/S8756-3282(01)00632-9
[14] M. N. Rhem, E. M. Lech, J. M. Patti, D. McDevitt, M. Hook, D. B. Jones and K. R. Wilhelmus, “The Collagen-Binding Adhesin Is a Virulence Factor in Staphylococcus aureus Keratitis,” Infection and Immunity, Vol. 68, No. 6, 2000, pp. 3776-3779. doi:10.1128/IAI.68.6.3776-3779.2000
[15] P. Moreillon, J. M. Entenza, P. Francioli, D. McDevitt, T. J. Foster, P. Francois and P. Vaudaux, “Role of Staphylococcus aureus Coagulase and Clumping Factor in Pathogenesis of Experimental Endocarditis,” Infection and Immunity, Vol. 63, No. 12, 1995, pp. 4738-4743.
[16] E. Josefsson, O. Hartford, L. O’Brien, J. M. Patti and T. Foster, “Protection against Experimental Staphylococcus aureus Arthritis by Vaccination with Clumping Factor A, a Novel Virulence Determinant,” The Journal of Infectious Diseases, Vol. 184, No. 12, 2001, pp. 1572-1580. doi:10.1086/324430
[17] J. Vernachio, A. S. Bayer, T. Le, Y. L. Chai, B. Prater, A. Schneider, B. Ames, P. Syribeys, J. Robbins and J. M. Patti, “Anti-Clumping Factor A Immunoglobulin Reduces the Duration of Methicillinresistant Staphylococcus aureus Bacteremia in an Experimental Model of Infective Endocarditis,” Antimicrobial Agents and Chemotherapy, Vol. 47, No. 11, 2003, pp. 3400-3406. doi:10.1128/AAC.47.11.3400-3406.2003
[18] J. Higgings, A. Louhhman, K. P. van Kessel, J. A. van Strijp and T. J. Foster, “Clumping Factor A of Staphylococcus aureus Inhibits Phagocytosi by Human Polymor-phonuclear Leucocytes,” FEMS Microbiology Letters, Vol. 258, No. 2, 2006, pp. 290-296.
[19] S. Watanabe, T. Ito, T. Sasaki, S. Li, I. Uchiyama, K. Kishii, K. Kikuchi, R. L. Skov and K. Hiramatsu, “Genetic Diversity of Staphylocoagulase Genes (coa): Insight into the Evolution of Variable Chromosomal Virulence Factors in Staphylococcus aureus,” PLoS One, Vol. 4, No. 5, 2009, Article ID: e5714. doi:10.1371/journal.pone.0005714
[20] G. Ji, R. C. Beavis and R. P. Novick, “Cell Density Control of Staphylococcal Virulence Mediated by an Octapeptide Pheromone,” Proceedings of the National Academy of Science USA, Vol. 92, No. 26, 1995, pp. 12055-12059. doi:10.1073/pnas.92.26.12055
[21] J. J. Ayala-Gaytan, M. C. Aleman-Bocanegra, C. E. Guajardo-Lara, S. B. Valdovinos-Chávez, “Catheter-Associated Bloodstream Infections. Review of Five-Year Surveillance among Hospitalized Patients,” Revista Medica del Instituto Mexicano del Seguro Social, Vol. 48, No. 2, 2010, pp. 145-150.
[22] G. Jean, “Incidence and Risk Factors for Infections from Hemodialysis Catheters,” Néphrologie, Vol. 22, No. 8, 2001, pp. 443-448.
[23] G. Jean, B. Charra, C. Chazot, T. Vanel, J. C. Terrat, J. M. Hurot and G. Laurent, “Risk Factors Analysis for Long-Term Tunneled Dialysis-Catheter Related Bacteremia,” Nephron, Vol. 91, No. 3, 2002, pp. 399-405. doi:10.1159/000064279
[24] M. G. Parker and B. N. Doebbeling, “The Challenge of Methicillin-Resistant Staphylococcus aureus Prevention in Hemodialysis Therapy,” Seminars in Dialysis, Vol. 25, No. 1, 2012, pp. 42-49. doi:10.1111/j.1525-139X.2011.00999.x
[25] K. Plata, A. E. Rosato and G. Wegrzyn, “Staphylococus aureus as an Infectious Agent: Overview of Biochemistry and Molecular Genetics of Its Pathogenicity,” Acta Biochimica Polonica, Vol. 56, No. 4, 2009, pp. 597-612.
[26] T. Moretro, L. Hermansen, A. L. Holck, M. S. Sidhu, K. Rudi and S. Langsrud, “Biofilm Formation and the Presence of the Intercellular Adhesion Locus ica among Staphylococci from Food and Food Processing Environments,” Applied and Environmental Microbiology, Vol. 69, No. 9, 2003, pp. 5648-5655. doi:10.1128/AEM.69.9.5648-5655.2003
[27] K. Toshkova, C. Annemuller, O. Akineden and C. Lammler, “The Significance of Nasal Carriage of Staphylococcus aureus as Risk Factor for Human Skin Infections,” FEMS Microbiology Letters, Vol. 202, No. 1, 2001, pp. 17-24. doi:10.1111/j.1574-6968.2001.tb10774.x
[28] R. Stolic, G. Trajkovic, V. Peric, A. Jovanovic, D. Stolic, S. Sovtic, T. Lazarevic, Z. Zivic and G. Subaric-Gorgieva, “Central Venous Catheters in Hemodialysis: To Accept Recommendations or to Stick to Own Experience,” Vojnosanitetski Pregled, Vol. 65, No. 1, 2008, pp. 21-26. doi:10.2298/VSP0801021S
[29] V. G. Fowler Jr., C. L. Nelson, L. M. McIntyre, B. N. Kreiswirth, A. Monk, G. L. Archer, J. Federspiel, S. Naidich, B. Remortel, T. Rude, P. Brown, L. B. Reller, G. R. Corey and S. R. Gill, “Potential Associations between Hematogenous Complications and Bacterial Genotype in Staphylococcus aureus Infection,” The Journal of Infectious Diseases, Vol. 196, No. 5, 2007, pp. 738-747. doi:10.1086/520088
[30] E. Josefsson, K. W. McCrea, D. Ni Eidhin, D. O’Connell, J. Cox, M. Hook and T. J. Foster, “Three New Members of the Serine-Aspartate Repeat Protein Multigene Family of Staphylococcus aureus,” Microbiology, Vol. 144, No. 12, 1998, pp. 3387-3395. doi:10.1099/00221287-144-12-3387
[31] S. J. Peacock, C. E. Moore, A. Justice, M. Kantzanou, L. Story, K. Mackie, G. O’Neill and N. P. Day, “Virulent Combinations of Adhesin and Toxin Genes in Natural Populations of Staphylococcus aureus,” Infection and Immunity, Vol. 70, No. 9, 2002, pp. 4987-4996. doi:10.1128/IAI.70.9.4987-4996.2002
[32] A. Sabath, D. C. Melles, G. Martirosian, H. Grundmann, A. van Belkum and W. Hryniewicz, “Distribution of the Serine-Aspartate Repeat Protein-Encoding sdr Genes among Nasal and Invasive Staphylococcus aureus Strains,” Journal of Clinical Microbiology, Vol. 44, No. 3, 2006, pp. 1135-1138. doi:10.1128/JCM.44.3.1135-1138.2006
[33] S. Trad, J. Allignet, L. Frangeul, M. Davi, M. Vergassola, E. Couve, A. Morvan, A. Kechrid, C. Buchrieser, P. Glaser and N. El-Solh, “DNA Macroarray for Identification and Typing of Staphylococcus aureus Isolates,” Journal of Clinical Microbiology, Vol. 42, No. 5, 2004, pp. 2054-2064. doi:10.1128/JCM.42.5.2054-2064.2004
[34] P. Sauer, J. Síla, T. Stosova, R. Vecerova, P. Hejnar, I. Vagnerova, M. Kolar, V. Raclavsky, J. Petrzelova, Y. Loveckova and D. Koukalova, “Prevalence of Genes Encoding Extracellular Virulence Factors among Meticillin-Resistant Staphylococcus aureus Isolates from the University Hospital, Olomouc, Czech Republic,” Journal of Medical Microbiology, Vol. 57, No. 4, 2008, pp. 403-410. doi:10.1099/jmm.0.47413-0
[35] S. J. Campbell, H. S. Deshmukh, C. L. Nelson, I. G. Bae, M. E. Stryjewski, J. J. Federspiel, G. T. Tonthat, T. H. Rude, S. L. Barriere, R. Corey and V. G. Fowler Jr., “Genotypic Characteristics of Staphylococcus aureus Isolates from a Multinational Trial of Complicated Skin and Skin Structure Infections,” Journal of Clinical Microbiology, Vol. 46, No. 2, 2008, pp. 678-684. doi:10.1128/JCM.01822-07
[36] J. S. Groeger, A. B. Lucas, H. T. Thaler, H. Friedlander- Klar, A. E. Brown, T. E. Kiehn and D. Armstrong, “Infectious Morbidity Associated with Long-Term Use of Venous Access Devices in Patients with Cancer,” Annals of Internal Medicine, Vol. 119, No. 12, 1993, pp. 1168-1174.
[37] R. Fluck, J. Wilson and C. R. Tomson, “UK Renal Registry 12th Annual Report (December 2009): Chapter 12: Epidemiology of Methicillin Resistant Staphylococcus aureus Bacteraemia amongst Patients Receiving Dialysis for Established Renal Failure in England in 2008: A Joint Report from the UK Renal Registry and the Health Protection Agency,” Nephron Clinical Practice, Vol. 115, No. 1, 2010, pp. 261-270. doi:10.1159/000301235

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