Cluster analysis of ribotyping profiles of Staphylococcus epidermidis isolates recovered from foreign body-associated orthopedic infections
Davide Campoccia
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Search for more papers by this authorLucio Montanaro
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Experimental Pathology Department, University of Bologna, Italy
Search for more papers by this authorChristof von Eiff
Institute of Medical Microbiology, University of Münster Hospital and Clinics, Münster, Germany
Search for more papers by this authorValter Pirini
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Search for more papers by this authorStefano Ravaioli
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Search for more papers by this authorKarsten Becker
Institute of Medical Microbiology, University of Münster Hospital and Clinics, Münster, Germany
Search for more papers by this authorCorresponding Author
Carla Renata Arciola
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Experimental Pathology Department, University of Bologna, Italy
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, ItalySearch for more papers by this authorDavide Campoccia
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Search for more papers by this authorLucio Montanaro
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Experimental Pathology Department, University of Bologna, Italy
Search for more papers by this authorChristof von Eiff
Institute of Medical Microbiology, University of Münster Hospital and Clinics, Münster, Germany
Search for more papers by this authorValter Pirini
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Search for more papers by this authorStefano Ravaioli
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Search for more papers by this authorKarsten Becker
Institute of Medical Microbiology, University of Münster Hospital and Clinics, Münster, Germany
Search for more papers by this authorCorresponding Author
Carla Renata Arciola
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, Italy
Experimental Pathology Department, University of Bologna, Italy
Research Unit on Implant Infections, Rizzoli Orthopaedic Institute, Bologna, ItalySearch for more papers by this authorAbstract
Staphylococcus epidermidis is an opportunistic pathogen of major clinical interest for its high prevalence in implant-associated infections. However, only little information is available on the phylogeny of its major clonal entities and their virulence and resistance markers. Therefore, purpose of this study was to characterize four clusters identified by automated ribotyping of 70 isolates derived from orthopedic, mostly foreign body-related infections. The ica locus, encoding the polysaccharide intercellular adhesin, the IS256 insertion element as well as the resistance to gentamicin, clindamycin, chloramphenicol, and ciprofloxacin were all traits uniquely observed in two of these clusters. The phylogenetic analysis of the S. epidermidis clusters offered a detailed insight into the clonal origin of exopolysaccharide- producing and multiresistant strains with transposons appearing to be actively involved in genetic exchanges. © 2008 Wiley Periodicals, Inc. J Biomed Mater Res, 2009
References
- 1 Vuong C,Otto M. Staphylococcus epidermidis infections. Microbes Infect 2002; 4: 481–489.
- 2 Ziebuhr W,Hennig S,Eckart M,Kranzler H,Batzilla C,Kozitskaya S. Nosocomial infections by Staphylococcus epidermidis: How a commensal bacterium turns into a pathogen. Int J Antimicrob Agents 2006; 28 ( Suppl 1): S14–S20.
- 3 von Eiff C,Peters G,Heilmann C. Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2002; 2: 677–685.
- 4
von Eiff C,Heilmann C,Peters G.
Staphylococcus epidermidis: Why is it so successful?
Clin Microbiol Infect
1998;
4:
297–300.
10.1111/j.1469-0691.1998.tb00062.x Google Scholar
- 5 Mohanty SS,Kay PR. Infection in total joint replacements. Why we screen MRSA when MRSE is the problem? J Bone Joint Surg Br 2004; 86: 266–268.
- 6 Campoccia D,Montanaro L,Baldassarri L,An YH,Arciola CR. Antibiotic resistance in Staphylococcus aureus and Staphylococcus epidermidis clinical isolates from implant orthopedic infections. Int J Artif Organs 2005; 28: 1186–1191.
- 7 Arciola CR,Campoccia D,Gamberini S,Donati ME,Pirini V,Visai L,Speziale P,Montanaro L. Antibiotic resistance in exopolysaccharide-forming Staphylococcus epidermidis clinical isolates from orthopaedic implant infections. Biomaterials 2005; 26: 6530–6535.
- 8 Gu J,Li H,Li M,Vuong C,Otto M,Wen Y,Gao Q. Bacterial insertion sequence IS256 as a potential molecular marker to discriminate invasive strains from commensal strains of Staphylococcus epidermidis. J Hosp Infect 2005; 61: 342–348.
- 9 Bradford R,Abdul MR,Daley AJ,Pearce C,Ramalingam A,D'Mello D,Mueller Y,Uahwatanasakul W,Qu Y,Grando D,Garland S,Deighton M. Coagulase-negative staphylococci in very-low-birth-weight infants: Inability of genetic markers to distinguish invasive strains from blood culture contaminants. Eur J Clin Microbiol Infect Dis 2006; 25: 283–290.
- 10 Frebourg NB,Lefebvre S,Baert S,Lemeland JF. PCR-Based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains. J Clin Microbiol 2000; 38: 877–880.
- 11 Rohde H,Kalitzky M,Kroger N,Scherpe S,Horstkotte MA,Knobloch JK,Zander AR,Mack D. Detection of virulence-associated genes not useful for discriminating between invasive and commensal Staphylococcus epidermidis strains from a bone marrow transplant unit. J Clin Microbiol 2004; 42: 5614–5619.
- 12 Becker K,Haverkämper G,von Eiff C,Roth R,Peters G. Survey of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene in non-Staphylococcus aureus species. Eur J Clin Microbiol Infect Dis 2001; 20: 407–409.
- 13 von Eiff C,Arciola CR,Montanaro L,Becker K,Campoccia D. Emerging Staphylococcus species as new pathogens in implant infections. Int J Artif Organs 2006; 29: 360–367.
- 14 Kozitskaya S,Cho SH,Dietrich K,Marre R,Naber K,Ziebuhr W. The bacterial insertion sequence element IS256 occurs preferentially in nosocomial Staphylococcus epidermidis isolates: Association with biofilm formation and resistance to aminoglycosides. Infect Immun 2004; 72: 1210–1215.
- 15 Arciola CR,Campoccia D,Gamberini S,Rizzi S,Donati ME,Baldassarri L,Montanaro L. Search for the insertion element IS256 within the ica locus of Staphylococcus epidermidis clinical isolates collected from biomaterial-associated infections. Biomaterials 2004; 25: 4117–4125.
- 16 Rohde H,Burandt EC,Siemssen N,Frommelt L,Burdelski C,Wurster S,Scherpe S,Davies AP,Harris LG,Horstkotte MA,Knobloch JK,Ragunath C,Kaplan JB,Mack D. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 2007; 28: 1711–20.
- 17 Takeuchi F,Watanabe S,Baba T,Yuzawa H,Ito T,Morimoto Y,Kuroda M,Cui L,Takahashi M,Ankai A,Baba S,Fukui S,Lee JC,Hiramatsu K. Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol 2005; 187: 7292–7308.
- 18 Morschhäuser J,Kohler G,Ziebuhr W,Blum-Oehler G,Dobrindt U,Hacker J. Evolution of microbial pathogens. Philos Trans R Soc Lond B Biol Sci 2000; 355: 695–704.
- 19 Ziebuhr W,Ohlsen K,Karch H,Korhonen T,Hacker J. Evolution of bacterial pathogenesis. Cell Mol Life Sci 1999; 56: 719–728.
- 20 Montanaro L,Campoccia D,Pirini V,Ravaioli S,Otto M,Arciola CR. Antibiotic multiresistance strictly associated with IS256 and ica genes in Staphylococcus epidermidis strains from implant orthopedic infections. J Biomed Mater Res A. 2007; 83: 813–818
- 21 NCCLS 2002. Analysis and presentation of cumulative susceptibility test data; approved guideline NCCLS document M39-A NCCLS. Wayne, PA: NCCLS.
- 22 NCCLS 2002. Performance standards for antimicrobial susceptibility testing: Twelfth informational supplement NCCLS document M100-S12 NCCLS. Wayne, PA: NCCLS.
- 23 Campoccia D,Montanaro L,Pirini V,Ravaioli S,Arciola CR. Prevalence of genes for aminoglycoside-modifying enzymes in Staphylococcus epidermidis isolates from orthopedic postsurgical and implant-related infections. J Biomed Mater Res A 2008 Mar 11; [Epub ahead of print].
- 24 Arciola CR,An YH,Campoccia D,Donati ME,Montanaro L. Etiology of implant orthopedic infections: A survey on 1027 clinical isolates. Int J Artif Organs 2005; 28: 1091–1100.
- 25 von Eiff C,Jansen B,Kohnen W,Becker K. Infections associated with medical devices: Pathogenesis, management and prophylaxis. Drugs 2005; 65: 179–214.
- 26 von Eiff C,Kohnen W,Becker K,Jansen B. Modern strategies in the prevention of implant-associated infections. Int J Artif Organs 2005; 28: 1146–1156.
- 27 Campoccia D,Montanaro L,Arciola CR. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 2006; 27: 2331–2339.
- 28 Kozitskaya S,Olson ME,Fey PD,Witte W,Ohlsen K,Ziebuhr W. Clonal analysis of Staphylococcus epidermidis isolates carrying or lacking biofilm-mediating genes by multilocus sequence typing. J Clin Microbiol 2005; 43: 4751–4757.
- 29 Johansson A,Koskiniemi S,Gottfridsson P,Wistrom J,Monsen T. Multiple-locus variable-number tandem repeat analysis for typing of Staphylococcus epidermidis. J Clin Microbiol 2006; 44: 260–265.
- 30 Kenchappa P,Duggirala A,Ahmed N,Pathengay A,Das T,Hasnain SE,Sharma S. Fluorescent amplified fragment length polymorphism (FAFLP) genotyping demonstrates the role of biofilm-producing methicillin-resistant periocular Staphylococcus epidermidis strains in postoperative endophthalmitis. BMC Ophthalmol 2006; 6: 1.
- 31 Lina B,Vandenesch F,Etienne J,Kreiswirth B,Fleurette J. Comparison of coagulase-negative staphylococci by pulsed-field electrophoresis. FEMS Microbiol Lett 1992; 71: 133–138.
- 32 Montanaro L,Campoccia D,Arciola CR. Advancements in molecular epidemiology of implant infections and future perspectives. Biomaterials 2007; 28: 5155–5168.
- 33 Moretro T,Hermansen L,Holck AL,Sidhu MS,Rudi K,Langsrud S. Biofilm formation and the presence of the intercellular adhesion locus ica among staphylococci from food and food processing environments. Appl Environ Microbiol 2003; 69: 5648–5655.
Citing Literature
