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.
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Soussy CJ (2006) Recommandations 2008. Comité de l’Antibiogramme de la Société Française de Microbiologie (CA-SFM). pp. 33–35
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
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
Vuong C, Otto M (2002) Staphylococcus epidermidis infections. Microb Infect 4:481–489
Werckenthin C, Schwarz S, Westh H (1999) Structural alteration in the translational attenuator of constitutively expressed ermC genes. Antimicrob Agents Chemother 43:1681–685
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-008-9227-4