Skip to main content

Advertisement

Log in

Coagulase-negative staphylococci: update on the molecular epidemiology and clinical presentation, with a focus on Staphylococcus epidermidis and Staphylococcus saprophyticus

  • Review
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Coagulase-negative staphylococci (CoNS), originally described as ubiquitous commensals of the healthy human skin and mucosa, have emerged as important opportunistic pathogens primarily causing healthcare-associated infections in patients with indwelling medical devices. Recent studies, utilizing new molecular typing methods, particularly on Staphylococcus epidermidis, have increased our understanding of the mechanisms that contribute to the evolutionary success of these extremely versatile microorganisms. In the following mini-review, we summarize recent research in this area focusing on the molecular methods and epidemiology of S. epidermidis and S. saprophyticus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Rogers KL, Fey PD, Rupp ME (2009) Coagulase-negative staphylococcal infections. Infect Dis Clin North Am 23(1):73–98

    Article  PubMed  Google Scholar 

  2. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39(3):309–317

    Article  PubMed  Google Scholar 

  3. Kernodle DS, Barg NL, Kaiser AB (1988) Low-level colonization of hospitalized patients with methicillin-resistant coagulase-negative staphylococci and emergence of the organisms during surgical antimicrobial prophylaxis. Antimicrob Agents Chemother 32(2):202–208

    PubMed  CAS  Google Scholar 

  4. Schoenfelder SM, Lange C, Eckart M, Hennig S, Kozytska S, Ziebuhr W (2010) Success through diversity—how Staphylococcus epidermidis establishes as a nosocomial pathogen. Int J Med Microbiol 300(6):380–386

    Article  PubMed  Google Scholar 

  5. Miragaia M, Thomas JC, Couto I, Enright MC, de Lencastre H (2007) Inferring a population structure for Staphylococcus epidermidis from multilocus sequence typing data. J Bacteriol 189(6):2540–2552

    Article  PubMed  CAS  Google Scholar 

  6. Kozitskaya S, Olson ME, Fey PD, Witte W, Ohlsen K, Ziebuhr W (2005) Clonal analysis of Staphylococcus epidermidis isolates carrying or lacking biofilm-mediating genes by multilocus sequence typing. J Clin Microbiol 43(9):4751–4757

    Article  PubMed  CAS  Google Scholar 

  7. Widerström M, Monsen T, Karlsson C, Edebro H, Johansson A, Wiström J (2009) Clonality among multidrug-resistant hospital-associated Staphylococcus epidermidis in northern Europe. Scand J Infect Dis 41(9):642–649

    Article  PubMed  Google Scholar 

  8. Li M, Wang X, Gao Q, Lu Y (2009) Molecular characterization of Staphylococcus epidermidis strains isolated from a teaching hospital in Shanghai, China. J Med Microbiol 58(Pt 4):456–461

    Article  PubMed  CAS  Google Scholar 

  9. Nováková D, Pantůcek R, Hubálek Z, Falsen E, Busse HJ, Schumann P, Sedlácek I (2010) Staphylococcus microti sp. nov., isolated from the common vole (Microtus arvalis). Int J Syst Evol Microbiol 60(Pt 3):566–573

    Article  PubMed  CAS  Google Scholar 

  10. Kloos WE, Musselwhite MS (1975) Distribution and persistence of Staphylococcus and Micrococcus species and other aerobic bacteria on human skin. Appl Microbiol 30(3):381–385

    PubMed  CAS  Google Scholar 

  11. Raz R, Colodner R, Kunin CM (2005) Who are you—Staphylococcus saprophyticus? Clin Infect Dis 40(6):896–898

    Article  PubMed  Google Scholar 

  12. Hoffman DJ, Brown GD, Lombardo FA (2007) Early-onset sepsis with Staphylococcus auricularis in an extremely low-birth weight infant—an uncommon pathogen. J Perinatol 27(8):519–520

    Article  PubMed  CAS  Google Scholar 

  13. Gras-Le Guen C, Fournier S, Andre-Richet B, Caillon J, Chamoux C, Espaze E, Richet H, Roze JC, Lepelletier D (2007) Almond oil implicated in a Staphylococcus capitis outbreak in a neonatal intensive care unit. J Perinatol 27(11):713–717

    Article  PubMed  CAS  Google Scholar 

  14. Van Der Zwet WC, Debets-Ossenkopp YJ, Reinders E, Kapi M, Savelkoul PH, Van Elburg RM, Hiramatsu K, Vandenbroucke-Grauls CM (2002) Nosocomial spread of a Staphylococcus capitis strain with heteroresistance to vancomycin in a neonatal intensive care unit. J Clin Microbiol 40(7):2520–2525

    Article  CAS  Google Scholar 

  15. Ross TL, Fuss EP, Harrington SM, Cai M, Perl TM, Merz WG (2005) Methicillin-resistant Staphylococcus caprae in a neonatal intensive care unit. J Clin Microbiol 43(1):363–367

    Article  PubMed  CAS  Google Scholar 

  16. Cid J, Lozano M, Nomdedeu B, Mazzara R, Vila J, Rives S, Ordinas A (1997) Staphylococcal sepsis associated with platelet transfusion: report of a new case and review of the literature. Sangre (Barc) 42(5):407–409

    CAS  Google Scholar 

  17. Basaglia G, Moras L, Bearz A, Scalone S, Paoli PD (2003) Staphylococcus cohnii septicaemia in a patient with colon cancer. J Med Microbiol 52(Pt 1):101–102

    Article  PubMed  Google Scholar 

  18. Ibrahem S, Salmenlinna S, Lyytikäinen O, Vaara M, Vuopio-Varkila J (2008) Molecular characterization of methicillin-resistant Staphylococcus epidermidis strains from bacteraemic patients. Clin Microbiol Infect 14(11):1020–1027

    Article  PubMed  CAS  Google Scholar 

  19. Klingenberg C, Rønnestad A, Anderson AS, Abrahamsen TG, Zorman J, Villaruz A, Flaegstad T, Otto M, Sollid JE (2007) Persistent strains of coagulase-negative staphylococci in a neonatal intensive care unit: virulence factors and invasiveness. Clin Microbiol Infect 13(11):1100–1111

    Article  PubMed  CAS  Google Scholar 

  20. Krediet TG, Mascini EM, van Rooij E, Vlooswijk J, Paauw A, Gerards LJ, Fleer A (2004) Molecular epidemiology of coagulase-negative staphylococci causing sepsis in a neonatal intensive care unit over an 11-year period. J Clin Microbiol 42(3):992–995

    Article  PubMed  CAS  Google Scholar 

  21. Milisavljevic V, Wu F, Cimmotti J, Haas J, Della-Latta P, Larson E, Saiman L (2005) Genetic relatedness of Staphylococcus epidermidis from infected infants and staff in the neonatal intensive care unit. Am J Infect Control 33(6):341–347

    Article  PubMed  Google Scholar 

  22. Monsen T, Karlsson C, Wiström J (2005) Spread of clones of multidrug-resistant, coagulase-negative staphylococci within a university hospital. Infect Control Hosp Epidemiol 26(1):76–80

    Article  PubMed  Google Scholar 

  23. Rodríguez-Aranda A, Daskalaki M, Villar J, Sanz F, Otero JR, Chaves F (2009) Nosocomial spread of linezolid-resistant Staphylococcus haemolyticus infections in an intensive care unit. Diagn Microbiol Infect Dis 63(4):398–402

    Article  PubMed  CAS  Google Scholar 

  24. Palazzo IC, d’Azevedo PA, Secchi C, Pignatari AC, Darini AL (2008) Staphylococcus hominis subsp. novobiosepticus strains causing nosocomial bloodstream infection in Brazil. J Antimicrob Chemother 62(6):1222–1226

    Article  PubMed  CAS  Google Scholar 

  25. Sorlozano A, Gutierrez J, Martinez T, Yuste ME, Perez-Lopez JA, Vindel A, Guillen J, Boquete T (2010) Detection of new mutations conferring resistance to linezolid in glycopeptide-intermediate susceptibility Staphylococcus hominis subspecies hominis circulating in an intensive care unit. Eur J Clin Microbiol Infect Dis 29(1):73–80

    Article  PubMed  CAS  Google Scholar 

  26. Hellbacher C, Törnqvist E, Söderquist B (2006) Staphylococcus lugdunensis: clinical spectrum, antibiotic susceptibility, and phenotypic and genotypic patterns of 39 isolates. Clin Microbiol Infect 12(1):43–49

    Article  PubMed  CAS  Google Scholar 

  27. Savini V, Catavitello C, Carlino D, Bianco A, Pompilio A, Balbinot A, Piccolomini R, Di Bonaventura G, D’Antonio D (2009) Staphylococcus pasteuri bacteraemia in a patient with leukaemia. J Clin Pathol 62(10):957–958

    Article  PubMed  CAS  Google Scholar 

  28. Song SH, Park JS, Kwon HR, Kim SH, Kim HB, Chang HE, Park KU, Song J, Kim EC (2009) Human bloodstream infection caused by Staphylococcus pettenkoferi. J Med Microbiol 58(Pt 2):270–272

    Article  PubMed  Google Scholar 

  29. Krishnan S, Haglund L, Ashfaq A, Leist P, Roat T (1996) Prosthetic valve endocarditis due to Staphylococcus saccharolyticus. Clin Infect Dis 22(4):722–723

    Article  PubMed  CAS  Google Scholar 

  30. Widerström M, Wiström J, Ferry S, Karlsson C, Monsen T (2007) Molecular epidemiology of Staphylococcus saprophyticus isolated from women with uncomplicated community-acquired urinary tract infection. J Clin Microbiol 45(5):1561–1564

    Article  PubMed  CAS  Google Scholar 

  31. Hernández JL, Calvo J, Sota R, Agüero J, García-Palomo JD, Fariñas MC (2001) Clinical and microbiological characteristics of 28 patients with Staphylococcus schleiferi infection. Eur J Clin Microbiol Infect Dis 20(3):153–158

    Article  PubMed  Google Scholar 

  32. Hedin G, Widerström M (1998) Endocarditis due to Staphylococcus sciuri. Eur J Clin Microbiol Infect Dis 17(9):673–675

    PubMed  CAS  Google Scholar 

  33. Tammelin A, Hambraeus A, Ståhle E (2002) Mediastinitis after cardiac surgery: improvement of bacteriological diagnosis by use of multiple tissue samples and strain typing. J Clin Microbiol 40(8):2936–2941

    Article  PubMed  Google Scholar 

  34. Center KJ, Reboli AC, Hubler R, Rodgers GL, Long SS (2003) Decreased vancomycin susceptibility of coagulase-negative staphylococci in a neonatal intensive care unit: evidence of spread of Staphylococcus warneri. J Clin Microbiol 41(10):4660–4665

    Article  PubMed  CAS  Google Scholar 

  35. Mastroianni A, Coronado O, Nanetti A, Chiodo F (1994) Staphylococcus xylosus isolated from a pancreatic pseudocyst in a patient infected with the human immunodeficiency virus. Clin Infect Dis 19(6):1173–1174

    Article  PubMed  CAS  Google Scholar 

  36. Sloos JH, Dijkshoorn L, Vogel L, van Boven CP (2000) Performance of phenotypic and genotypic methods to determine the clinical relevance of serial blood isolates of Staphylococcus epidermidis in patients with septicemia. J Clin Microbiol 38(7):2488–2493

    PubMed  CAS  Google Scholar 

  37. Miragaia M, Carriço JA, Thomas JC, Couto I, Enright MC, de Lencastre H (2008) Comparison of molecular typing methods for characterization of Staphylococcus epidermidis: proposal for clone definition. J Clin Microbiol 46(1):118–129

    Article  PubMed  CAS  Google Scholar 

  38. Willemse-Erix HF, Jachtenberg J, Barutçi H, Puppels GJ, van Belkum A, Vos MC, Maquelin K (2010) Proof of principle for successful characterization of methicillin-resistant coagulase-negative staphylococci isolated from skin by use of Raman spectroscopy and pulsed-field gel electrophoresis. J Clin Microbiol 48(3):736–740

    Article  PubMed  CAS  Google Scholar 

  39. Dubois D, Leyssene D, Chacornac JP, Kostrzewa M, Schmit PO, Talon R, Bonnet R, Delmas J (2010) Identification of a variety of Staphylococcus species by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol 48(3):941–945. doi:10.1128/JCM.00413-09

    Article  PubMed  CAS  Google Scholar 

  40. Szabados F, Woloszyn J, Richter C, Kaase M, Gatermann S (2010) Identification of molecularly defined Staphylococcus aureus strains using matrix-assisted laser desorption/ionization time of flight mass spectrometry and the Biotyper 2.0 database. J Med Microbiol 59(Pt 7):787–790. doi:10.1099/jmm.0.016733-0

    Article  PubMed  CAS  Google Scholar 

  41. van Belkum A, Tassios PT, Dijkshoorn L, Haeggman S, Cookson B, Fry NK, Fussing V, Green J, Feil E, Gerner-Smidt P, Brisse S, Struelens M (2007) Guidelines for the validation and application of typing methods for use in bacterial epidemiology. Clin Microbiol Infect 13(Supp 3):1–46. doi:10.1111/j.1469-0691.2007.01786.x

    Article  PubMed  Google Scholar 

  42. Kluytmans J, Berg H, Steegh P, Vandenesch F, Etienne J, van Belkum A (1998) Outbreak of Staphylococcus schleiferi wound infections: strain characterization by randomly amplified polymorphic DNA analysis, PCR ribotyping, conventional ribotyping, and pulsed-field gel electrophoresis. J Clin Microbiol 36(8):2214–2219

    PubMed  CAS  Google Scholar 

  43. Carretto E, Barbarini D, Couto I, De Vitis D, Marone P, Verhoef J, De Lencastre H, Brisse S (2005) Identification of coagulase-negative staphylococci other than Staphylococcus epidermidis by automated ribotyping. Clin Microbiol Infect 11(3):177–184

    Article  PubMed  CAS  Google Scholar 

  44. Casey AL, Worthington T, Caddick JM, Hilton AC, Lambert PA, Elliott TS (2006) RAPD for the typing of coagulase-negative staphylococci implicated in catheter-related bloodstream infection. J Infect 52(4):282–289

    Article  PubMed  CAS  Google Scholar 

  45. Deplano A, Schuermans A, Van Eldere J, Witte W, Meugnier H, Etienne J, Grundmann H, Jonas D, Noordhoek GT, Dijkstra J, van Belkum A, van Leeuwen W, Tassios PT, Legakis NJ, van der Zee A, Bergmans A, Blanc DS, Tenover FC, Cookson BC, O’Neil G, Struelens MJ (2000) Multicenter evaluation of epidemiological typing of methicillin-resistant Staphylococcus aureus strains by repetitive-element PCR analysis. The European Study Group on Epidemiological Markers of the ESCMID. J Clin Microbiol 38(10):3527–3533

    PubMed  CAS  Google Scholar 

  46. Kelly S, Collins J, Maguire M, Gowing C, Flanagan M, Donnelly M, Murphy PG (2008) An outbreak of colonization with linezolid-resistant Staphylococcus epidermidis in an intensive therapy unit. J Antimicrob Chemother 61(4):901–907

    Article  PubMed  CAS  Google Scholar 

  47. Savelkoul PH, Melles DC, Buffing N, Gorkink R, Simons G, van Belkum A (2007) High density whole genome fingerprinting of methicillin-resistant and -susceptible strains of Staphylococcus aureus in search of phenotype-specific molecular determinants. J Microbiol Methods 71(1):44–54

    Article  PubMed  CAS  Google Scholar 

  48. Natoli S, Fontana C, Favaro M, Bergamini A, Testore GP, Minelli S, Bossa MC, Casapulla M, Broglio G, Beltrame A, Cudillo L, Cerretti R, Leonardis F (2009) Characterization of coagulase-negative staphylococcal isolates from blood with reduced susceptibility to glycopeptides and therapeutic options. BMC Infect Dis 9:83

    Article  PubMed  CAS  Google Scholar 

  49. Malachowa N, Sabat A, Gniadkowski M, Krzyszton-Russjan J, Empel J, Miedzobrodzki J, Kosowska-Shick K, Appelbaum PC, Hryniewicz W (2005) Comparison of multiple-locus variable-number tandem-repeat analysis with pulsed-field gel electrophoresis, spa typing, and multilocus sequence typing for clonal characterization of Staphylococcus aureus isolates. J Clin Microbiol 43(7):3095–3100

    Article  PubMed  CAS  Google Scholar 

  50. Li W, Raoult D, Fournier PE (2009) Bacterial strain typing in the genomic era. FEMS Microbiol Rev 33(5):892–916

    Article  PubMed  CAS  Google Scholar 

  51. Schouls LM, Spalburg EC, van Luit M, Huijsdens XW, Pluister GN, van Santen-Verheuvel MG, van der Heide HG, Grundmann H, Heck ME, de Neeling AJ (2009) Multiple-locus variable number tandem repeat analysis of Staphylococcus aureus: comparison with pulsed-field gel electrophoresis and spa-typing. PLoS ONE 4(4):e5082

    Article  PubMed  CAS  Google Scholar 

  52. Moser SA, Box MJ, Patel M, Amaya M, Schelonka R, Waites KB (2009) Multiple-locus variable-number tandem-repeat analysis of meticillin-resistant Staphylococcus aureus discriminates within USA pulsed-field gel electrophoresis types. J Hosp Infect 71(4):333–339

    Article  PubMed  CAS  Google Scholar 

  53. Francois P, Hochmann A, Huyghe A, Bonetti EJ, Renzi G, Harbarth S, Klingenberg C, Pittet D, Schrenzel J (2008) Rapid and high-throughput genotyping of Staphylococcus epidermidis isolates by automated multilocus variable-number of tandem repeats: a tool for real-time epidemiology. J Microbiol Methods 72(3):296–305

    Article  PubMed  CAS  Google Scholar 

  54. Johansson A, Koskiniemi S, Gottfridsson P, Wiström J, Monsen T (2006) Multiple-locus variable-number tandem repeat analysis for typing of Staphylococcus epidermidis. J Clin Microbiol 44(1):260–265

    Article  PubMed  CAS  Google Scholar 

  55. Gerner-Smidt P, Hise K, Kincaid J, Hunter S, Rolando S, Hyytiä-Trees E, Ribot EM, Swaminathan B (2006) PulseNet USA: a five-year update. Foodborne Pathog Dis 3(1):9–19

    Article  PubMed  CAS  Google Scholar 

  56. Herschleb J, Ananiev G, Schwartz DC (2007) Pulsed-field gel electrophoresis. Nat Protoc 2(3):677–684

    Article  PubMed  CAS  Google Scholar 

  57. Murchan S, Kaufmann ME, Deplano A, de Ryck R, Struelens M, Zinn CE, Fussing V, Salmenlinna S, Vuopio-Varkila J, El Solh N, Cuny C, Witte W, Tassios PT, Legakis N, van Leeuwen W, van Belkum A, Vindel A, Laconcha I, Garaizar J, Haeggman S, Olsson-Liljequist B, Ransjo U, Coombes G, Cookson B (2003) Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J Clin Microbiol 41(4):1574–1585

    Article  PubMed  CAS  Google Scholar 

  58. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33(9):2233–2239

    PubMed  CAS  Google Scholar 

  59. Blanc DS (2004) The use of molecular typing for epidemiological surveillance and investigation of endemic nosocomial infections. Infect Genet Evol 4(3):193–197

    Article  PubMed  CAS  Google Scholar 

  60. Cookson BD, Robinson DA, Monk AB, Murchan S, Deplano A, de Ryck R, Struelens MJ, Scheel C, Fussing V, Salmenlinna S, Vuopio-Varkila J, Cuny C, Witte W, Tassios PT, Legakis NJ, van Leeuwen W, van Belkum A, Vindel A, Garaizar J, Haeggman S, Olsson-Liljequist B, Ransjo U, Muller-Premru M, Hryniewicz W, Rossney A, O’Connell B, Short BD, Thomas J, O’Hanlon S, Enright MC (2007) Evaluation of molecular typing methods in characterizing a European collection of epidemic methicillin-resistant Staphylococcus aureus strains: the HARMONY collection. J Clin Microbiol 45(6):1830–1837

    Article  PubMed  CAS  Google Scholar 

  61. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38(3):1008–1015

    PubMed  CAS  Google Scholar 

  62. Turner KM, Feil EJ (2007) The secret life of the multilocus sequence type. Int J Antimicrob Agents 29(2):129–135

    Article  PubMed  CAS  Google Scholar 

  63. Thomas JC, Vargas MR, Miragaia M, Peacock SJ, Archer GL, Enright MC (2007) Improved multilocus sequence typing scheme for Staphylococcus epidermidis. J Clin Microbiol 45(2):616–619

    Article  PubMed  Google Scholar 

  64. Monk AB, Archer GL (2007) Use of outer surface protein repeat regions for improved genotyping of Staphylococcus epidermidis. J Clin Microbiol 45(3):730–735

    Article  PubMed  CAS  Google Scholar 

  65. Clarridge JE 3rd (2004) Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 17(4):840–862, table of contents

    Article  PubMed  CAS  Google Scholar 

  66. Ghebremedhin B, Layer F, König W, König B (2008) Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J Clin Microbiol 46(3):1019–1025

    Article  PubMed  CAS  Google Scholar 

  67. Mellmann A, Becker K, von Eiff C, Keckevoet U, Schumann P, Harmsen D (2006) Sequencing and staphylococci identification. Emerg Infect Dis 12(2):333–336

    PubMed  CAS  Google Scholar 

  68. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC) (2009) Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 53(12):4961–4967

    Article  CAS  Google Scholar 

  69. Jamaluddin TZ, Kuwahara-Arai K, Hisata K, Terasawa M, Cui L, Baba T, Sotozono C, Kinoshita S, Ito T, Hiramatsu K (2008) Extreme genetic diversity of methicillin-resistant Staphylococcus epidermidis strains disseminated among healthy Japanese children. J Clin Microbiol 46(11):3778–3783

    Article  PubMed  Google Scholar 

  70. Zhang YQ, Ren SX, Li HL, Wang YX, Fu G, Yang J, Qin ZQ, Miao YG, Wang WY, Chen RS, Shen Y, Chen Z, Yuan ZH, Zhao GP, Qu D, Danchin A, Wen YM (2003) Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 49(6):1577–1593

    Article  PubMed  CAS  Google Scholar 

  71. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, Paulsen IT, Kolonay JF, Brinkac L, Beanan M, Dodson RJ, Daugherty SC, Madupu R, Angiuoli SV, Durkin AS, Haft DH, Vamathevan J, Khouri H, Utterback T, Lee C, Dimitrov G, Jiang L, Qin H, Weidman J, Tran K, Kang K, Hance IR, Nelson KE, Fraser CM (2005) Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 187(7):2426–2438

    Article  PubMed  CAS  Google Scholar 

  72. 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 (2005) Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol 187(21):7292–7308

    Article  PubMed  CAS  Google Scholar 

  73. Kuroda M, Yamashita A, Hirakawa H, Kumano M, Morikawa K, Higashide M, Maruyama A, Inose Y, Matoba K, Toh H, Kuhara S, Hattori M, Ohta T (2005) Whole genome sequence of Staphylococcus saprophyticus reveals the pathogenesis of uncomplicated urinary tract infection. Proc Natl Acad Sci USA 102(37):13272–13277

    Article  PubMed  CAS  Google Scholar 

  74. Ben Zakour NL, Guinane CM, Fitzgerald JR (2008) Pathogenomics of the staphylococci: insights into niche adaptation and the emergence of new virulent strains. FEMS Microbiol Lett 289(1):1–12

    Article  PubMed  CAS  Google Scholar 

  75. Wolters M, Rohde H, Maier T, Belmar-Campos C, Franke G, Scherpe S, Aepfelbacher M, Christner M (2011) MALDI-TOF MS fingerprinting allows for discrimination of major methicillin-resistant Staphylococcus aureus lineages. Int J Med Microbiol 301(1):64–68. doi:10.1016/j.ijmm.2010.06.002

    Article  PubMed  CAS  Google Scholar 

  76. Spanu T, De Carolis E, Fiori B, Sanguinetti M, D’Inzeo T, Fadda G, Posteraro B (2010) Evaluation of matrix-assisted laser desorption ionization-time-of-flight mass spectrometry in comparison to rpoB gene sequencing for species identification of bloodstream infection staphylococcal isolates. Clin Microbiol Infect 17(1):44–49. doi:10.1111/j.1469-0691.2010.03181.x

    Article  Google Scholar 

  77. Murray PR (2010) Matrix-assisted laser desorption ionization time-of-flight mass spectrometry: usefulness for taxonomy and epidemiology. Clin Microbiol Infect 16(11):1626–1630. doi:10.1111/j.1469-0691.2010.03364.x

    Article  PubMed  CAS  Google Scholar 

  78. Harris LG, El-Bouri K, Johnston S, Rees E, Frommelt L, Siemssen N, Christner M, Davies AP, Rohde H, Mack D (2010) Rapid identification of staphylococci from prosthetic joint infections using MALDI-TOF mass-spectrometry. Int J Artif Organs 33(9):568–574

    PubMed  CAS  Google Scholar 

  79. Moussaoui W, Jaulhac B, Hoffmann AM, Ludes B, Kostrzewa M, Riegel P, Prévost G (2010) Matrix-assisted laser desorption ionization time-of-flight mass spectrometry identifies 90% of bacteria directly from blood culture vials. Clin Microbiol Infect 16(11):1631–1638. doi:10.1111/j.1469-0691.2010.03356.x

    Article  PubMed  CAS  Google Scholar 

  80. Jarvis RM, Goodacre R (2004) Discrimination of bacteria using surface-enhanced Raman spectroscopy. Anal Chem 76(1):40–47

    Article  PubMed  CAS  Google Scholar 

  81. Maquelin K, Dijkshoorn L, van der Reijden TJ, Puppels GJ (2006) Rapid epidemiological analysis of Acinetobacter strains by Raman spectroscopy. J Microbiol Methods 64(1):126–131

    Article  PubMed  CAS  Google Scholar 

  82. Otto M (2009) Staphylococcus epidermidis—the ‘accidental’ pathogen. Nat Rev Microbiol 7(8):555–567

    Article  PubMed  CAS  Google Scholar 

  83. Miragaia M, de Lencastre H, Perdreau-Remington F, Chambers HF, Higashi J, Sullam PM, Lin J, Wong KI, King KA, Otto M, Sensabaugh GF, Diep BA (2009) Genetic diversity of arginine catabolic mobile element in Staphylococcus epidermidis. PLoS ONE 4(11):e7722

    Article  PubMed  CAS  Google Scholar 

  84. Granslo HN, Klingenberg C, Fredheim EG, Rønnestad A, Mollnes TE, Flaegstad T (2010) Arginine catabolic mobile element is associated with low antibiotic resistance and low pathogenicity in Staphylococcus epidermidis from neonates. Pediatr Res 68(3):237–241

    Article  PubMed  CAS  Google Scholar 

  85. Denton C, Pappas EG, Uricchio JF, Goldberg H, Likoff W (1957) Bacterial endocarditis following cardiac surgery. Circulation 15(4):525–531

    PubMed  CAS  Google Scholar 

  86. Torres Pereira A (1962) Coagulase-negative strains of Staphylococcus possessing antigen 51 as agents of urinary infection. J Clin Pathol 15:252–253

    Article  PubMed  CAS  Google Scholar 

  87. Hovelius B, Mårdh PA (1984) Staphylococcus saprophyticus as a common cause of urinary tract infections. Rev Infect Dis 6(3):328–337

    Article  PubMed  CAS  Google Scholar 

  88. von Eiff C, Peters G, Heilmann C (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2(11):677–685

    Article  Google Scholar 

  89. Mermel LA, Allon M, Bouza E, Craven DE, Flynn P, O’Grady NP, Raad II, Rijnders BJ, Sherertz RJ, Warren DK (2009) Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 Update by the Infectious Diseases Society of America. Clin Infect Dis 49(1):1–45

    Article  PubMed  CAS  Google Scholar 

  90. Tokars JI (2004) Predictive value of blood cultures positive for coagulase-negative staphylococci: implications for patient care and health care quality assurance. Clin Infect Dis 39(3):333–341

    Article  PubMed  Google Scholar 

  91. Kassis C, Rangaraj G, Jiang Y, Hachem RY, Raad I (2009) Differentiating culture samples representing coagulase-negative staphylococcal bacteremia from those representing contamination by use of time-to-positivity and quantitative blood culture methods. J Clin Microbiol 47(10):3255–3260

    Article  PubMed  Google Scholar 

  92. Saleem BR, Meerwaldt R, Tielliu IF, Verhoeven EL, van den Dungen JJ, Zeebregts CJ (2010) Conservative treatment of vascular prosthetic graft infection is associated with high mortality. Am J Surg 200(1):47–52

    Article  PubMed  Google Scholar 

  93. Prusseit J, Simon M, von der Brelie C, Heep A, Molitor E, Volz S, Simon A (2009) Epidemiology, prevention and management of ventriculoperitoneal shunt infections in children. Pediatr Neurosurg 45(5):325–336

    Article  PubMed  Google Scholar 

  94. Ratilal B, Costa J, Sampaio C (2008) Antibiotic prophylaxis for surgical introduction of intracranial ventricular shunts: a systematic review. J Neurosurg Pediatr 1(1):48–56

    Article  PubMed  Google Scholar 

  95. Schreffler RT, Schreffler AJ, Wittler RR (2002) Treatment of cerebrospinal fluid shunt infections: a decision analysis. Pediatr Infect Dis J 21(7):632–636

    Article  PubMed  Google Scholar 

  96. Chu VH, Woods CW, Miro JM, Hoen B, Cabell CH, Pappas PA, Federspiel J, Athan E, Stryjewski ME, Nacinovich F, Marco F, Levine DP, Elliott TS, Fortes CQ, Tornos P, Gordon DL, Utili R, Delahaye F, Corey GR, Fowler VG Jr (2008) Emergence of coagulase-negative staphylococci as a cause of native valve endocarditis. Clin Infect Dis 46(2):232–242

    Article  PubMed  Google Scholar 

  97. Chu VH, Miro JM, Hoen B, Cabell CH, Pappas PA, Jones P, Stryjewski ME, Anguera I, Braun S, Muñoz P, Commerford P, Tornos P, Francis J, Oyonarte M, Selton-Suty C, Morris AJ, Habib G, Almirante B, Sexton DJ, Corey GR, Fowler VG Jr (2009) Coagulase-negative staphylococcal prosthetic valve endocarditis—a contemporary update based on the International Collaboration on Endocarditis: prospective cohort study. Heart (British Cardiac Society) 95(7):570–576

    Article  CAS  Google Scholar 

  98. Gandelman G, Frishman WH, Wiese C, Green-Gastwirth V, Hong S, Aronow WS, Horowitz HW (2007) Intravascular device infections: epidemiology, diagnosis, and management. Cardiol Rev 15(1):13–23

    Article  PubMed  Google Scholar 

  99. Rundström H, Kennergren C, Andersson R, Alestig K, Hogevik H (2004) Pacemaker endocarditis during 18 years in Göteborg. Scand J Infect Dis 36(9):674–679

    Article  PubMed  Google Scholar 

  100. Matthews PC, Berendt AR, McNally MA, Byren I (2009) Diagnosis and management of prosthetic joint infection. BMJ 338:b1773

    Article  PubMed  Google Scholar 

  101. Del Pozo JL, Patel R (2009) Clinical practice. Infection associated with prosthetic joints. N Engl J Med 361(8):787–794

    Article  PubMed  Google Scholar 

  102. Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, Fridkin SK (2008) NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol 29(11):996–1011

    Article  PubMed  Google Scholar 

  103. Söderquist B (2007) Surgical site infections in cardiac surgery: microbiology. APMIS 115(9):1008–1011

    Article  PubMed  Google Scholar 

  104. Lalwani GA, Flynn HW Jr, Scott IU, Quinn CM, Berrocal AM, Davis JL, Murray TG, Smiddy WE, Miller D (2008) Acute-onset endophthalmitis after clear corneal cataract surgery (1996–2005). Clinical features, causative organisms, and visual acuity outcomes. Ophthalmology 115(3):473–476

    Article  PubMed  Google Scholar 

  105. Hovelius B, Colleen S, Mårdh PA (1984) Urinary tract infections in men caused by Staphylococcus saprophyticus. Scand J Infect Dis 16(1):37–41

    Article  PubMed  CAS  Google Scholar 

  106. Ishihara S, Yokoi S, Ito M, Kobayashi S, Deguchi T (2001) Pathologic significance of Staphylococcus saprophyticus in complicated urinary tract infections. Urology 57(1):17–20

    Article  PubMed  CAS  Google Scholar 

  107. Ferry SA, Holm SE, Stenlund H, Lundholm R, Monsen TJ (2004) The natural course of uncomplicated lower urinary tract infection in women illustrated by a randomized placebo controlled study. Scand J Infect Dis 36(4):296–301

    Article  PubMed  Google Scholar 

  108. Coton E, Desmonts MH, Leroy S, Coton M, Jamet E, Christieans S, Donnio PY, Lebert I, Talon R (2010) Biodiversity of coagulase-negative Staphylococci in French cheeses, dry fermented sausages, processing environments and clinical samples. Int J Food Microbiol 137(2–3):221–229

    Article  PubMed  CAS  Google Scholar 

  109. Gillespie BE, Headrick SI, Boonyayatra S, Oliver SP (2009) Prevalence and persistence of coagulase-negative Staphylococcus species in three dairy research herds. Vet Microbiol 134(1–2):65–72

    Article  PubMed  CAS  Google Scholar 

  110. Hedman P, Ringertz O, Eriksson B, Kvarnfors P, Andersson M, Bengtsson L, Olsson K (1990) Staphylococcus saprophyticus found to be a common contaminant of food. J Infect 21(1):11–19

    Article  PubMed  CAS  Google Scholar 

  111. Leroy S, Giammarinaro P, Chacornac JP, Lebert I, Talon R (2010) Biodiversity of indigenous staphylococci of naturally fermented dry sausages and manufacturing environments of small-scale processing units. Food Microbiol 27(2):294–301

    Article  PubMed  CAS  Google Scholar 

  112. Hedman P, Ringertz O (1991) Urinary tract infections caused by Staphylococcus saprophyticus. A matched case control study. J Infect 23(2):145–153

    Article  PubMed  CAS  Google Scholar 

  113. Soge OO, Meschke JS, No DB, Roberts MC (2009) Characterization of methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative Staphylococcus spp. isolated from US West Coast public marine beaches. J Antimicrob Chemother 64(6):1148–1155

    Article  PubMed  CAS  Google Scholar 

  114. Miragaia M, Couto I, de Lencastre H (2005) Genetic diversity among methicillin-resistant Staphylococcus epidermidis (MRSE). Microb Drug Resist 11(2):83–93

    Article  PubMed  CAS  Google Scholar 

  115. Monsen T, Olofsson C, Rönnmark M, Wiström J (2000) Clonal spread of staphylococci among patients with peritonitis associated with continuous ambulatory peritoneal dialysis. Kidney Int 57(2):613–618

    Article  PubMed  CAS  Google Scholar 

  116. Potoski BA, Adams J, Clarke L, Shutt K, Linden PK, Baxter C, Pasculle AW, Capitano B, Peleg AY, Szabo D, Paterson DL (2006) Epidemiological profile of linezolid-resistant coagulase-negative staphylococci. Clin Infect Dis 43(2):165–171

    Article  PubMed  CAS  Google Scholar 

  117. Mulanovich VE, Huband MD, McCurdy SP, Lemmon MM, Lescoe M, Jiang Y, Rolston KV, LaSala PR (2010) Emergence of linezolid-resistant coagulase-negative Staphylococcus in a cancer centre linked to increased linezolid utilization. J Antimicrob Chemother 65(9):2001–2004

    Article  PubMed  CAS  Google Scholar 

  118. Widerström M, Monsen T, Karlsson C, Wiström J (2006) Molecular epidemiology of meticillin-resistant coagulase-negative staphylococci in a Swedish county hospital: evidence of intra- and interhospital clonal spread. J Hosp Infect 64(2):177–183

    Article  PubMed  Google Scholar 

  119. Bonilla H, Huband MD, Seidel J, Schmidt H, Lescoe M, McCurdy SP, Lemmon MM, Brennan LA, Tait-Kamradt A, Puzniak L, Quinn JP (2010) Multicity outbreak of linezolid-resistant Staphylococcus epidermidis associated with clonal spread of a cfr-containing strain. Clin Infect Dis 51(7):796–800

    Article  PubMed  Google Scholar 

  120. Mendes RE, Deshpande LM, Farrell DJ, Spanu T, Fadda G, Jones RN (2010) Assessment of linezolid resistance mechanisms among Staphylococcus epidermidis causing bacteraemia in Rome, Italy. J Antimicrob Chemother 65(11):2329–2335

    Article  PubMed  CAS  Google Scholar 

  121. Milisavljevic V, Tran LP, Batmalle C, Bootsma HJ (2008) Benzyl alcohol and ethanol can enhance the pathogenic potential of clinical Staphylococcus epidermidis strains. Am J Infect Control 36(8):552–558

    Article  PubMed  Google Scholar 

  122. Hira V, Sluijter M, Goessens WH, Ott A, de Groot R, Hermans PW, Kornelisse RF (2010) Coagulase-negative staphylococcal skin carriage among neonatal intensive care unit personnel: from population to infection. J Clin Microbiol 48(11):3876–3881

    Article  PubMed  Google Scholar 

  123. Silva FR, Mattos EM, Coimbra MV, Ferreira-Carvalho BT, Figueiredo AM (2001) Isolation and molecular characterization of methicillin-resistant coagulase-negative staphylococci from nasal flora of healthy humans at three community institutions in Rio de Janeiro City. Epidemiol Infect 127(1):57–62

    Article  PubMed  CAS  Google Scholar 

  124. Widerström M (2010) Molecular epidemiology of coagulase-negative staphylococci in hospitals and in the community. Dissertation, Umeå University, Umeå, Sweden

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Widerström.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Widerström, M., Wiström, J., Sjöstedt, A. et al. Coagulase-negative staphylococci: update on the molecular epidemiology and clinical presentation, with a focus on Staphylococcus epidermidis and Staphylococcus saprophyticus . Eur J Clin Microbiol Infect Dis 31, 7–20 (2012). https://doi.org/10.1007/s10096-011-1270-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-011-1270-6

Keywords

Navigation