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Clonality and Occurrence of Genes Encoding Antibiotic Resistance and Biofilm in Methicillin-Resistant Staphylococcus epidermidis Strains Isolated from Catheters and Bacteremia in Neutropenic Patients

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Abstract

Thirty methicillin-resistant Staphylococcus epidermidis strains isolated from catheters and blood cultures from neutropenic patients were studied. They were classified into 17 multidrug-resistance patterns. Polymerase cahin reaction analysis revealed that methicillin resistance was encoded by the mecA gene in all strains, and aminoglycosides resistance was due to aac(6′)-Ie-aph(2″)-Ia (23 strains), ant(4′)-Ia (13), and aph(3′)-IIIa (1) genes. The aac(6′)-Ie-aph(2″)-Ia gene was detected concomitantly with aph(3′)-IIIa, and ant(4′)-Ia genes in one and nine strains, respectively. Erythromycin resistance was encoded by the ermC (11 strains), ermA (6), and msrA (2) genes. The ermC gene was inducibly expressed in five strains, whereas the ermA was exclusively constitutively expressed. The icaA and icaC genes were detected in 19 strains; however, biofilm production was observed in only 16 strains. Most strains harbored multiple plasmids of variable sizes ranging from 2.2 to 70 kb, and two strains were plasmid-free. PFGE identified 15 distinct PFGE types, and five predominant genotypes were found. Our study showed the occurrence of complex genetic phenomenons. In unrelated strains, evidence of horizontal transfer of antibiotic-encoding genes and/or ica operon, and in indistinguishable strains, there is a quite good likelihood of independent steps of loss and/or gain of these genes. This genome dynamicity might have enhanced the invasiveness power of these methicillin-resistant S epidermidis strains.

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References

  1. Ben Hassen A, Gréco A, Jouaihia W, Leclercq R (2001) Profil épidémiologique des souches de Staphylococcus epidermidis méticilline résistant de sensibilité diminuée à la teicoplanine et isolées chez des patients neutropéniques au Centre National de Greffe de Moelle Osseuse à Tunis. Pathol Biol 49:634–640

    Article  PubMed  CAS  Google Scholar 

  2. Bouchami O, Achour W, Ben Hassen A (2007) Prevalence and mechanisms of macrolide resistance among Staphylococcus epidermidis isolates from neutropenic patients in Tunisia. Clin Microbiol Infect 13:103–106

    Article  PubMed  CAS  Google Scholar 

  3. Butt T, Afzal RK, Ahmad RN, Salman M, Mahmood A, Anwar M (2004) Bloodstream infections in febrile neutropenic patients: bacterial spectrum and antimicrobial susceptibility pattern. J Ayub Med Coll Abbottabad 16:18–22

    PubMed  Google Scholar 

  4. Cafiso V, Bertuccio T, Santagati M et al (2004) Presence of the ica operon in clinical isolates of Staphylococcus epidermidis and its role in biofilm production. Clin Microbiol Infect 10:1081–1088

    Article  PubMed  CAS  Google Scholar 

  5. Chaieb K, Mahdouania K, Bakhrouf A (2005) Detection of icaA and icaD loci by polymerase chain reaction and biofilm formation by Staphylococcus epidermidis isolated from dialysate and needles in a dialysis unit. J Hosp Infect 61:225–230

    Article  PubMed  CAS  Google Scholar 

  6. Chaieb K, Touati A, Abbassi MS, Ben Hassen A, Mahdouani K, Bakhrouf A (2006) DNA fingerprinting of a multi-resistant coagulase-negative staphylococci isolated from biomaterials in dialysis services. Arch Med Res 37:953–960

    Article  PubMed  CAS  Google Scholar 

  7. Choi SM, Kim SH, Kim HJ et al (2003) Multiplex PCR for the detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among Staphylococcus species. J Korean Med Sci 18:631–636

    PubMed  CAS  Google Scholar 

  8. Chokr A, Leterme D, Watier D, Jabbouri S (2007) Neither the presence of ica locus, nor in vitro-biofilm formation ability is a crucial parameter for some Staphylococcus epidermidis strains to maintain an infection in a guinea pig tissue cage model. Microb Pathogen 42:94–97

    Article  CAS  Google Scholar 

  9. Cui L, Ma X, Sato K, Okuma K et al (2003) Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J Clin Microbiol 41:5–14

    Article  PubMed  CAS  Google Scholar 

  10. Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE (2007) The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 13:222–235

    Article  PubMed  CAS  Google Scholar 

  11. Klingenberg C, Sundsfjord A, Rønnestad A, Mikalsen J, Gaustad P, Flægstad T (2004) Phenotypic and genotypic aminoglycoside resistance in blood culture isolates of coagulase-negative staphylococci from a single neonatal intensive care unit, 1989–2000. J Antimicrobiol Chemother 54:889–896

    Article  CAS  Google Scholar 

  12. Klingenberg C, Ronnestad A, Anderson AS et al (2007) Persistent strains of coagulase-negative staphylococci in neonatal intensive care unit: virulence factors and invasiveness. Clin Microbiol Infect 13:1100–1111

    Article  PubMed  CAS  Google Scholar 

  13. Kobayashi N, Alam MM, Nishimoto Y, Urasawa S, Uehara N, Watanabe N (2001) Distribution of aminoglycoside resistance genes in recent clinical isolates of Enterococcus faecalis, Enterococcus faecium and Enterococcus avium. Epidemiol Infect 126:197–204

    Article  PubMed  CAS  Google Scholar 

  14. Leclercq R (2002) Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications. Clin Infect Dis 34:482–492

    Article  PubMed  CAS  Google Scholar 

  15. Lodder G, Werckenthin C, Schwarz S, Dyke K (1997) Molecular analysis of naturally occurring ermC-encoding plasmids in staphylococci isolated from animals with and without previous contact with macrolides/lincosamides antibiotics. FEMS Immunol Med Microbiol 18:7–15

    Article  PubMed  CAS  Google Scholar 

  16. Mack D, Becker P, Chatterjee I et al (2004) Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 294:203–212

    Article  PubMed  CAS  Google Scholar 

  17. Maniati M, Petinaki E, Spiliopoulou I et al (2005) Rapid increase in numbers of Staphylococcus epidermidis strains with reduced susceptibility to teicoplanin in Greece. Int J Antimicrob Agents 25:346–348

    Article  PubMed  CAS  Google Scholar 

  18. Martineau F, Picard FJ, Lansac N et al (2000) Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis. Antimicrob Agents Chemother 44:231–238

    Article  PubMed  CAS  Google Scholar 

  19. Miragaia M, Couto I, Pereira SFF et al (2002) Molecular characterization of methicillin-resistant Staphylococcus epidermidis clones: evidence of geographic dissemination. J Clin Microbiol 40:430–438

    Article  PubMed  CAS  Google Scholar 

  20. Ninin E, Caroff N, Espaze E et al (2006) Assessment of ica operon carriage and biofilm production in Staphylococcus epidermidis isolates causing bacteraemia in bone marrow transplant recipients. Clin Microbiol Infect 12:446–452

    Article  PubMed  CAS  Google Scholar 

  21. Nouwen JL, van Belkum A, DE Marie S et al (1998) Clonal expansion of Staphylococcus epidermidis strains causing Hickman catheter-related infections in a hemato-oncologic department. J Clin Microbiol 36:2696–2702

    PubMed  CAS  Google Scholar 

  22. Ounissi H, Derlot E, Carlier C, Courvalin P (1990) Gene homogeneity for aminoglycoside-modifying enzymes in gram-positive cocci. Antimicrob Agents Chemother 34:2164–2168

    PubMed  CAS  Google Scholar 

  23. Schmitz F-J, Fluit AC, Gondolf M et al (1999) The prevalence of aminoglycoside resistance and corresponding resistance genes in clinical isolates of staphylococci from 19 European hospitals. J Antimicrobiol Chemother 43:253–259

    Article  CAS  Google Scholar 

  24. Shaw KJ, Rather PN, Hare RS, Miller GH (1993) Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol Res 57:138–163

    CAS  Google Scholar 

  25. Soussy CJ (2006) Recommandations 2008. Comité de l’Antibiogramme de la Société Française de Microbiologie (CA-SFM). pp. 33–35

  26. Tenover FC, Arbeit RD, Goering RV et al (1995) Interpreting chromosomal DNA restriction patterns produced by PFGE: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239

    PubMed  CAS  Google Scholar 

  27. van Pelt C, Nouwen J, Lugtenburg E et al (2003) Strict infection control measures do not prevent clonal spread of coagulase negative staphylococci colonizing central venous catheters in neutropenic hemato-oncologic patients. FEMS Immunol Med Microbiol 38:153–158

    Article  PubMed  Google Scholar 

  28. Vuong C, Otto M (2002) Staphylococcus epidermidis infections. Microb Infect 4:481–489

    Article  Google Scholar 

  29. Werckenthin C, Schwarz S, Westh H (1999) Structural alteration in the translational attenuator of constitutively expressed ermC genes. Antimicrob Agents Chemother 43:1681–685

    PubMed  CAS  Google Scholar 

  30. Woodford N, Morrison D, Cookson B, Gorge RC (1993) Comparison of high level gentamicin-resistant Enterococcus faecium isolates from different continents. Antimicrob Agents Chemother 37:681–684

    PubMed  CAS  Google Scholar 

  31. Ziebuher W, Krimmer V, Rachid S, Lößner I, Götz F, Jörg H (1999) A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesions synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 32:345–356

    Article  Google Scholar 

Download references

Acknowledgments

We are very grateful to Professor Miragaia Maria and Professor De Lencastre Herminia (Universidade Nova de Liesboa, Oeiras, Portugal) for helpful discussions of the manuscript.

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Correspondence to Assia Ben Hassen.

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Abbassi, M.S., Bouchami, O., Touati, A. et al. Clonality and Occurrence of Genes Encoding Antibiotic Resistance and Biofilm in Methicillin-Resistant Staphylococcus epidermidis Strains Isolated from Catheters and Bacteremia in Neutropenic Patients. Curr Microbiol 57, 442–448 (2008). https://doi.org/10.1007/s00284-008-9227-4

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