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Volume 65, Issue 12

Coagulase-negative staphylococci: pathogenesis, occurrence of antibiotic resistance genes and effects of antimicrobial agents on biofilm-growing bacteria Free

Abstract

Coagulase-negative staphylococci (CoNS) are opportunistic pathogens that particularly cause infections in patients with implanted medical devices. The present research was performed to study the virulence potential of 53 clinical isolates of , , , , and All clinical strains were clonally unrelated. Isolates carried genes encoding resistance to β-lactam () (15 %), aminoglycoside [(11 %), (15 %), (19 %)] and macrolide, lincosamide and streptogramin B (MLS) [(A) (4 %), (B) (13 %), (C) (41 %), (A) (11 %)] antibiotics. CoNS isolates (64 %) were able to form biofilms. Confocal laser scanning microscopy revealed that these biofilms formed a threedimensional structure composed mainly of living cells. All biofilm-positive strains carried the operon. studies demonstrated that a combination treatment with tigecycline and rifampicin was more effective against biofilms than one with ciprofloxacin and rifampicin. The minimum biofilm eradication concentration values were 0.062–0.5 µg ml for tigecycline/rifampicin and 0.250–2 µg ml for ciprofloxacin/rifampicin. All CoNS strains adhered to the human epithelial cell line HeLa, and more than half of the isolates were able to invade the HeLa cells, although most invaded relatively poorly. The virulence of CoNS is also attributed to their cytotoxic effects on HeLa cells. Incubation of HeLa cells with culture supernatant of the CoNS isolates resulted in cell death. The results indicate that the pathogenicity of , , , and is multi-factorial, involving the ability of these bacteria to adhere to human epithelial cells, form biofilms and invade and destroy human cells.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): adhesion , antibiotic resistance , biofilm formation , Coagulase-negative staphylococci , Cytotoxicity and invasion
© 2016 The Authors
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2016-12-16
2024-04-19
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References

  1. Allignet J., Aubert S., Dyke K. G., El Solh N. 2001; Staphylococcus caprae strains carry determinants known to be involved in pathogenicity: a gene encoding an autolysin-binding fibronectin and the ica operon involved in biofilm formation. Infect Immun 69:712 – 718 [View Article][PubMed]
     [Google Scholar]
  2. Almeida R. A., Oliver S. P. 2001; Interaction of coagulase-negative Staphylococcus species with bovine mammary epithelial cells. Microb Pathog 31:205 – 212 [View Article][PubMed]
     [Google Scholar]
  3. Anaya-López J. L., Contreras-Guzmán O. E., Cárabez-Trejo A., Baizabal-Aguirre V. M., López-Meza J. E., Valdez-Alarcón J. J., Ochoa-Zarzosa A. 2006; Invasive potential of bacterial isolates associated with subclinical bovine mastitis. Res Vet Sci 81:358 – 361 [View Article][PubMed]
     [Google Scholar]
  4. Ardic N., Sareyyupoglu B., Ozyurt M., Haznedaroglu T., Ilga U. 2006; Investigation of aminoglycoside modifying enzyme genes in methicillin-resistant staphylococci. Microbiol Res 161:49 – 54 [View Article]
     [Google Scholar]
  5. Aybar Y., Ozaras R., Besirli K., Engin E., Karabulut E., Salihoglu T., Mete B., Tabak F., Mert A. et al. 2012; Efficacy of tigecycline and vancomycin in experimental catheter-related Staphylococcus epidermidis infection: microbiological and electron microscopic analysis of biofilm. Int J Antimicrob Agents 39:338 – 342 [View Article][PubMed]
     [Google Scholar]
  6. Berdal J. E., Skråmm I., Mowinckel P., Gulbrandsen P., Bjørnholt J. 2005; Use of rifampicin and ciprofloxacin combination therapy after surgical debridement in the treatment of early manifestation prosthetic joint infections. Clin Microbiol Infect 11:843 – 845 [View Article][PubMed]
     [Google Scholar]
  7. Cerca F., França A., Pérez-Cabezas B., Carvalhais V., Ribeiro A., Azeredo J., Pier G., Cerca N., Vilanova M. 2014; Dormant bacteria within Staphylococcus epidermidis biofilms have low inflammatory properties and maintain tolerance to vancomycin and penicillin after entering planktonic growth. J Med Microbiol 63:1274 – 1283 [View Article][PubMed]
     [Google Scholar]
  8. Chokr A., Watier D., Eleaume H., Pangon B., Ghnassia J. C., Mack D., Jabbouri S. 2006; Correlation between biofilm formation and production of polysaccharide intercellular adhesin in clinical isolates of coagulase-negative staphylococci. Int J Med Microbiol 296:381 – 388 [View Article][PubMed]
     [Google Scholar]
  9. Coiffier G., Albert J. D., Arvieux C., Guggenbuhl P. 2013; Optimizing combination rifampin therapy for staphylococcal osteoarticular infections. Joint Bone Spine 80:11 – 17 [View Article][PubMed]
     [Google Scholar]
  10. Cui B., Smooker P. M., Rouch D. A., Daley A. J., Deighton M. A. 2013; Differences between two clinical Staphylococcus capitis subspecies as revealed by biofilm, antibiotic resistance, and pulsed-field gel electrophoresis profiling. J Clin Microbiol 51:9 – 14 [View Article][PubMed]
     [Google Scholar]
  11. Donvito B., Etienne J., Greenland T., Mouren C., Delorme V., Vandenesch F. 1997; Distribution of the synergistic haemolysin genes hld and slush with respect to agr in human staphylococci. FEMS Microbiol Lett 151:139 – 144 [View Article]
     [Google Scholar]
  12. Edwards A. M., Potts J. R., Josefsson E., Massey R. C. 2010; Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathog 6:e1000964 [View Article][PubMed]
     [Google Scholar]
  13. Fey P. D. 2010; Modality of bacterial growth presents unique targets: how do we treat biofilm-mediated infections?. Curr Opin Microbiol 13:610 – 615 [View Article][PubMed]
     [Google Scholar]
  14. Frank K. L., Del Pozo J. L., Patel R. 2008; From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis . Clin Microbiol Rev 21:111 – 133 [View Article][PubMed]
     [Google Scholar]
  15. Fredheim E. G., Klingenberg C., Rohde H., Frankenberger S., Gaustad P., Flaegstad T., Sollid J. E. 2009; Biofilm formation by Staphylococcus haemolyticus . J Clin Microbiol 47:1172 – 1180 [View Article][PubMed]
     [Google Scholar]
  16. Garzoni C., Kelley W. L. 2009; Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol 17:59 – 65 [View Article][PubMed]
     [Google Scholar]
  17. Geha D. J., Uhl J. R., Gustaferro C. A., Persing D. H. 1994; Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. J Clin Microbiol 32:1768 – 1772[PubMed]
     [Google Scholar]
  18. Greco-Stewart V. S., Ali H., Kumaran D., Kalab M., Rood I. G., de Korte D., Ramírez-Arcos S. 2013; Biofilm formation by Staphylococcus capitis strains isolated from contaminated platelet concentrates. J Med Microbiol 62:1051 – 1059 [View Article][PubMed]
     [Google Scholar]
  19. Heldman A. W., Hartert T. V., Ray S. C., Daoud E. G., Kowalski T. E., Pompili V. J., Sisson S. D., Tidmore W. C., vom Eigen K. A. et al. 1996; Oral antibiotic treatment of right-sided staphylococcal endocarditis in injection drug users: prospective randomized comparison with parenteral therapy. Am J Med 101:68 – 76 [View Article][PubMed]
     [Google Scholar]
  20. Heydorn A., Givskov M., Hentzer M., Ersbøll B. K., Sternberg C., Nielsen A. T., Molin S. 2000; Quantification of biofilm structures by the novel computer program comstat. Microbiology 146:2395 – 2407 [View Article]
     [Google Scholar]
  21. Hirschhausen N., Schlesier T., Schmidt M. A., Götz F., Peters G., Heilmann C. 2010; A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol 12:1746 – 1764 [View Article][PubMed]
     [Google Scholar]
  22. Kim J. H., Kim C. H., Hacker J., Ziebuhr W., Lee B. K., Cho S. H. 2008; Molecular characterization of regulatory genes associated with biofilm variation in a Staphylococcus aureus strain. J Microbiol Biotechnol 18:28 – 34[PubMed]
     [Google Scholar]
  23. Koksal F., Yasar H., Samasti M. 2009; Antibiotic resistance patterns of coagulase-negative staphylococcus strains isolated from blood cultures of septicemic patients in Turkey. Microbiol Res 164:404 – 410 [View Article][PubMed]
     [Google Scholar]
  24. Krzymińska S., Szczuka E., Kaznowski A. 2012; Staphylococcus haemolyticus strains target mitochondria and induce caspase-dependent apoptosis of macrophages. Antonie Van Leeuwenhoek 102:611 – 620 [View Article][PubMed]
     [Google Scholar]
  25. Krzymińska S., Szczuka E., Dudzińska K., Kaznowski A. 2015; Virulence and the presence of aminoglycoside resistance genes of Staphylococcus haemolyticus strains isolated from clinical specimens. Antonie Van Leeuwenhoek 107:857 – 868 [View Article][PubMed]
     [Google Scholar]
  26. Le K. Y., Dastgheyb S., Ho T. V., Otto M. 2014; Molecular determinants of staphylococcal biofilm dispersal and structuring. Front Cell Infect Microbiol 4:167 [View Article][PubMed]
     [Google Scholar]
  27. Le Bouter A., Leclercq R., Cattoir V. 2011; Molecular basis of resistance to macrolides, lincosamides and streptogramins in Staphylococcus saprophyticus clinical isolates. Int J Antimicrob Agents 37:118 – 123 [View Article][PubMed]
     [Google Scholar]
  28. Mack D., Rohde H., Harris L. G., Davies A. P., Horstkotte M. A., Knobloch J. K.-M. 2006; Biofilm formation in medical device-related infection. Inter J Art Organs 29:343 – 359
     [Google Scholar]
  29. Moskowitz S. M., Foster J. M., Emerson J., Burns J. L. 2004; Clinically feasible biofilm susceptibility assay for isolates of Pseudomonas aeruginosa from patients with cystic fibrosis. J Clin Microbiol 42:1915 – 1922 [View Article][PubMed]
     [Google Scholar]
  30. Osman K. M., Abd El-Razik K. A., Marie H. S., Arafa A. 2015; Relevance of biofilm formation and virulence of different species of coagulase-negative staphylococci to public health. Eur J Clin Microbiol Infect Dis 34:2009 – 2016 [View Article][PubMed]
     [Google Scholar]
  31. Otto M. 2004; Virulence factors of the coagulase-negative staphylococci. Front Biosci 9:841 – 863 [View Article][PubMed]
     [Google Scholar]
  32. Otto M. 2012; Molecular basis of Staphylococcus epidermidis infections. Semin Immunopathol 34:201 – 214 [View Article][PubMed]
     [Google Scholar]
  33. Pereira E. M., Teixeira C. A., Alvarenga A. L., Schuenck R. P., Giambiagi-Demarval M., Holandino C., Mattos-Guaraldi A. L., dos Santos K. R. 2012; A brazilian lineage of Staphylococcus lugdunensis presenting rough colony morphology may adhere to and invade lung epithelial cells. J Med Microbiol 61:463 – 469 [View Article][PubMed]
     [Google Scholar]
  34. Piette A., Verschraegen G. 2009; Role of coagulase-negative staphylococci in human disease. Vet Microbiol 134:45 – 54 [View Article][PubMed]
     [Google Scholar]
  35. Qin Z., Yang X., Yang L., Jiang J., Ou Y., Molin S., Qu D. 2007; Formation and properties of in vitro biofilms of ica-negative Staphylococcus epidermidis clinical isolates. J Med Microbiol 56:83 – 93 [View Article][PubMed]
     [Google Scholar]
  36. Qu Y., Daley A. J., Istivan T. S., Garland S. M., Deighton M. A. 2010; Antibiotic susceptibility of coagulase-negative staphylococci isolated from very low birth weight babies: comprehensive comparisons of bacteria at different stages of biofilm formation. Ann Clin Microbiol Antimicrob 9:16 [View Article]
     [Google Scholar]
  37. Rasigade J. P., Raulin O., Picaud J. C., Tellini C., Bes M., Grando J., Ben Saïd M., Claris O., Etienne J. et al. 2007; Methicillin-resistant Staphylococcus capitis with reduced vancomycin susceptibility causes late-onset sepsis in intensive care Neonates. PLoS One 7:e31548 [View Article]
     [Google Scholar]
  38. Rodhe H., Mack D., Christner M., Burdelski C., Franke G., Knobloch J. K.-M. 2006; Pathogenesis of staphylococcal device-related infections: from basic science to new diagnostic, therapeutic and prophylactic approaches. Rev Med Microbiol 17:45 – 54
     [Google Scholar]
  39. Ross T. L., Fuss E. P., Harrington S. M., Cai M., Perl T. M., Merz W. G. 2005; Methicillin-resistant Staphylococcus caprae in a neonatal intensive care unit. J Clin Microbiol 43:363 – 367 [View Article][PubMed]
     [Google Scholar]
  40. Różalska M., Szewczyk E. M. 2008; Staphylococcus cohnii hemolysins – isolation, purification and properties. Folia Microbiol 53:521 – 526
     [Google Scholar]
  41. Rumi M. V., Huguet M. J., Bentancor A. B., Gentilini E. R. 2013; The icaA gene in staphylococci from bovine mastitis. J Infect Dev Ctries 7:556 – 560 [View Article][PubMed]
     [Google Scholar]
  42. Shi S., Zhang X. 2012; Interaction of Staphylococcus aureus with osteoblasts. Exp Ther Med 3:367 – 370 [View Article][PubMed]
     [Google Scholar]
  43. Simojoki H., Hyvönen P., Plumed Ferrer C., Taponen S., Pyörälä S. 2012; Is the biofilm formation and slime producing ability of coagulase-negative staphylococci associated with the persistence and severity of intramammary infection?. Vet Microbiol 158:344 – 352 [View Article][PubMed]
     [Google Scholar]
  44. Szabados F., Marlinghaus L., Korte M., Neumann S., Kaase M., Gatermann S. G. 2011; Fbl is not involved in the invasion of eukaryotic epithelial and endothelial cells by Staphylococcus lugdunensis . FEMS Microbiol Lett 324:48 – 55 [View Article][PubMed]
     [Google Scholar]
  45. Szczuka E., Kaznowski A. 2014; Antimicrobial activity of tigecycline alone or in combination with rifampin against Staphylococcus epidermidis in biofilm. Folia Microbiol 59:283 – 288 [View Article]
     [Google Scholar]
  46. Szczuka E., Grabska K., Kaznowski A. 2015; In vitro activity of Rifampicin combined with Daptomycin or Tigecycline on Staphylococcus haemolyticus biofilms. Curr Microbiol 71:184 – 189 [View Article][PubMed]
     [Google Scholar]
  47. Valour F., Trouillet-Assant S., Rasigade J. P., Lustig S., Chanard E., Meugnier H., Tigaud S., Vandenesch F., Etienne J. et al. 2013; Staphylococcus epidermidis in orthopedic device infections: the role of bacterial internalization in human osteoblasts and biofilm formation. PLoS One 8:e67240 [View Article][PubMed]
     [Google Scholar]
  48. Versalovic J., Koeuth T., Lupski J. R. 1991; Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823 – 6831 [View Article][PubMed]
     [Google Scholar]
  49. Yin L. Y., Lazzarini L., Li F., Stevens C. M., Calhoun J. H. 2005; Comparative evaluation of tigecycline and vancomycin, with and without rifampicin, in the treatment of methicillin-resistant Staphylococcus aureus experimental osteomyelitis in a rabbit model. J Antimicrob Chemother 55:995 – 1002 [View Article][PubMed]
     [Google Scholar]
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Coagulase-negative staphylococci: pathogenesis, occurrence of antibiotic resistance genes and in vitro effects of antimicrobial agents on biofilm-growing bacteria
J. Med. Microbiol. 65, 1405 (2016); https://doi.org/10.1099/jmm.0.000372
/content/journal/jmm/10.1099/jmm.0.000372
/content/journal/jmm/10.1099/jmm.0.000372
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