Is nasal carriage of Staphylococcus aureus the main acquisition pathway for surgical-site infection in orthopaedic surgery?

  • P. Berthelot
  • F. Grattard
  • C. Cazorla
  • J.-P. Passot
  • J.-P. Fayard
  • R. Meley
  • J. Bejuy
  • F. Farizon
  • B. Pozzetto
  • F. Lucht


The endogenous or exogenous origin of Staphylococcus aureus, responsible for orthopaedic surgical-site infections (SSI), remains debated. We conducted a multicentre prospective cohort study to analyse the respective part of exogenous contamination and endogenous self-inoculation by S. aureus during elective orthopaedic surgery. The nose of each consecutive patient was sampled before surgery. Strains of S. aureus isolated from the nose and the wound, in the case of SSI, were compared by antibiotypes or pulsed-field gel electrophoresis (PFGE). A total of 3,908 consecutive patients undergoing orthopaedic surgery were included. Seventy-seven patients developed an SSI (2%), including 22 related to S. aureus (0.6%). S. aureus was isolated from the nose of 790 patients (20.2%) at the time of surgery. In the multivariate analysis, S. aureus nasal carriage was found to be a risk factor for S. aureus SSI in orthopaedic surgery. However, only nine subjects exhibiting S. aureus SSI had been found to be carriers before surgery: when compared, three pairs of strains were considered to be different and six similar. In most cases of S. aureus SSI, either an endogenous origin could not be demonstrated or pre-operative nasal colonisation retrieved a strain that was different from the one recovered from the surgical site



The authors particularly thank Nicolas Eydoux, Estelle Badel and Fabrice Di Palma for the collection and recording of the data.

Conflict of interest statement

The authors have received funding support from the Ministère de la Santé, France, Programme Hospitalier de Recherche Clinique (PHRC Dépistaph) for this study. No conflict of interest is declared. No financial interest in a pharmaceutical company is declared.


  1. 1.
    Harris WH, Sledge CB (1990) Total hip and total knee replacement. N Engl J Med 323:801–807PubMedGoogle Scholar
  2. 2.
    Sperling JW, Kozak TK, Hanssen AD, Cofield RH (2001) Infection after shoulder arthroplasty. Clin Orthop Relat Res 382:206–216CrossRefPubMedGoogle Scholar
  3. 3.
    Chesney D, Sales J, Elton R, Brenkel IJ (2008) Infection after knee arthroplasty: a prospective study of 1509 cases. J Arthroplasty 23:355–359CrossRefPubMedGoogle Scholar
  4. 4.
    Trampuz A, Zimmerli W (2006) Diagnosis and treatment of infections associated with fracture-fixation devices. Injury 37:S59–S66CrossRefPubMedGoogle Scholar
  5. 5.
    Powers KA, Terpenning MS, Voice RA, Kauffman CA (1990) Prosthetic joint infections in the elderly. Am J Med 88:9N–13NPubMedGoogle Scholar
  6. 6.
    NIH Consensus Development Panel on Total Hip Replacement (1995) NIH consensus conference: total hip replacement. JAMA 273:1950–1956CrossRefGoogle Scholar
  7. 7.
    Darouiche RO (2004) Treatment of infections associated with surgical implants. N Engl J Med 350:1422–1429CrossRefPubMedGoogle Scholar
  8. 8.
    Kalmeijer MD, van Nieuwland-Bollen E, Bogaers-Hofman D, de Baere GA (2000) Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery. Infect Control Hosp Epidemiol 21:319–323CrossRefPubMedGoogle Scholar
  9. 9.
    Perl TM, Cullen JJ, Wenzel RP, Zimmerman MB, Pfaller MA, Sheppard D, Twombley J, French PP, Herwaldt LA (2002) Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med 346:1871–1877CrossRefPubMedGoogle Scholar
  10. 10.
    Kluytmans JA, Mouton JW, Ijzerman EP, Vandenbroucke-Grauls CM, Maat AW, Wagenvoort JH, Verbrugh HA (1995) Nasal carriage of Staphylococcus aureus as a major risk factor for wound infections after cardiac surgery. J Infect Dis 171:216–219PubMedGoogle Scholar
  11. 11.
    Muñoz P, Hortal J, Giannella M, Barrio JM, Rodríguez-Créixems M, Pérez MJ, Rincón C, Bouza E (2008) Nasal carriage of S. aureus increases the risk of surgical site infection after major heart surgery. J Hosp Infect 68:25–31CrossRefPubMedGoogle Scholar
  12. 12.
    Gernaat-van der Sluis AJ, Hoogenboom-Verdegaal AM, Edixhoven PJ, Spies-van Rooijen NH (1998) Prophylactic mupirocin could reduce orthopedic wound infections. 1,044 patients treated with mupirocin compared with 1,260 historical controls. Acta Orthop Scand 69:412–414PubMedCrossRefGoogle Scholar
  13. 13.
    Rao N, Cannella B, Crossett LS, Yates AJ Jr, McGough R 3rd (2008) A preoperative decolonization protocol for Staphylococcus aureus prevents orthopaedic infections. Clin Orthop Relat Res 66:1343–1348CrossRefGoogle Scholar
  14. 14.
    Hacek DM, Robb WJ, Paule SM, Kudrna JC, Stamos VP, Peterson LR (2008) Staphylococcus aureus nasal decolonization in joint replacement surgery reduces infection. Clin Orthop Relat Res 466:1349–1355CrossRefPubMedGoogle Scholar
  15. 15.
    Kalmeijer MD, Coertjens H, van Nieuwland-Bollen PM, Bogaers-Hofman D, de Baere GA, Stuurman A, van Belkum A, Kluytmans JA (2002) Surgical site infections in orthopedic surgery: the effect of mupirocin nasal ointment in a double-blind, randomized, placebo-controlled study. Clin Infect Dis 35:353–358CrossRefPubMedGoogle Scholar
  16. 16.
    Matushek MG, Bonten MJ, Hayden MK (1996) Rapid preparation of bacterial DNA for pulsed-field gel electrophoresis. J Clin Microbiol 34:2598–2600PubMedGoogle Scholar
  17. 17.
    Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG (1992) CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections. Am J Infect Control 20:271–274CrossRefPubMedGoogle Scholar
  18. 18.
    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 33:2233–2239PubMedGoogle Scholar
  19. 19.
    San Juan R, Chaves F, López Gude MJ, Díaz-Pedroche C, Otero J, Cortina Romero JM, Rufilanchas JJ, Aguado JM (2007) Staphylococcus aureus poststernotomy mediastinitis: description of two distinct acquisition pathways with different potential preventive approaches. J Thorac Cardiovasc Surg 134:670–676CrossRefPubMedGoogle Scholar
  20. 20.
    Harbarth S, Huttner B, Gervaz P, Fankhauser C, Chraiti MN, Schrenzel J, Licker M, Pittet D (2008) Risk factors for methicillin-resistant Staphylococcus aureus surgical site infection. Infect Control Hosp Epidemiol 29:890–893CrossRefPubMedGoogle Scholar
  21. 21.
    Kluytmans J, van Belkum A, Verbrugh H (1997) Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10:505–520PubMedGoogle Scholar
  22. 22.
    Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339:520–532CrossRefPubMedGoogle Scholar
  23. 23.
    Mertz D, Frei R, Jaussi B, Tietz A, Stebler C, Flückiger U, Widmer AF (2007) Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin Infect Dis 45:475–477CrossRefPubMedGoogle Scholar
  24. 24.
    Van Belkum A, Verkaik NJ, de Vogel CP, Boelens HA, Verveer J, Nouwen JL, Verbrugh HA, Wertheim HF (2009) Reclassification of Staphylococcus aureus nasal carriage types. J Infect Dis 199:1820–1826CrossRefPubMedGoogle Scholar
  25. 25.
    Nouwen JL, Ott A, Kluytmans-Vandenbergh MF, Boelens HA, Hofman A, van Belkum A, Verbrugh HA (2004) Predicting the Staphylococcus aureus nasal carrier state: derivation and validation of a “culture rule”. Clin Infect Dis 39:806–811CrossRefPubMedGoogle Scholar
  26. 26.
    Schafroth M, Zimmerli W, Brunazzi M, Ochsner PE (2003) Infections. In: Oschner PE (ed) Total hip replacement. Springer, Berlin, pp 65–90Google Scholar
  27. 27.
    Acton DS, Plat-Sinnige MJ, van Wamel W, de Groot N, van Belkum A (2009) Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? Eur J Clin Microbiol Infect Dis 28:115–127CrossRefPubMedGoogle Scholar
  28. 28.
    Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Inf Dis 5:751–762CrossRefGoogle Scholar
  29. 29.
    Murdoch DR, Roberts SA, Fowler VG Jr, Shah MA, Taylor SL, Morris AJ, Corey GR (2001) Infection of orthopedic prostheses after Staphylococcus aureus bacteremia. Clin Infect Dis 32:646–649CrossRefGoogle Scholar
  30. 30.
    Blok HE, Troelstra A, Kamp-Hopmans TE, Gigengack-Baars AC, Vandenbroucke-Grauls CM, Weersink AJ, Verhoef J, Mascini EM (2003) Role of healthcare workers in outbreaks of methicillin-resistant Staphylococcus aureus: a 10-year evaluation from a Dutch university hospital. Infect Control Hosp Epidemiol 24:679–685CrossRefPubMedGoogle Scholar
  31. 31.
    Anderson DJ, Kaye KS, Classen D, Arias KM, Podgorny K, Burstin H, Calfee DP, Coffin SE, Dubberke ER, Fraser V, Gerding DN, Griffin FA, Gross P, Klompas M, Lo E, Marschall J, Mermel LA, Nicolle L, Pegues DA, Perl TM, Saint S, Salgado CD, Weinstein RA, Wise R, Yokoe DS (2008) Strategies to prevent surgical site infections in acute care hospital. Infect Control Hosp Epidemiol 29:S51–S61CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • P. Berthelot
    • 1
    • 2
    • 5
  • F. Grattard
    • 1
    • 2
  • C. Cazorla
    • 1
    • 2
  • J.-P. Passot
    • 3
  • J.-P. Fayard
    • 3
  • R. Meley
    • 3
  • J. Bejuy
    • 4
  • F. Farizon
    • 1
  • B. Pozzetto
    • 1
    • 2
  • F. Lucht
    • 1
    • 2
  1. 1.University Hospital and University Jean MonnetSaint EtienneFrance
  2. 2.Group “Mucosal Immunity and Pathogen Agents”University Jean MonnetSaint EtienneFrance
  3. 3.Clinique MutualisteSaint EtienneFrance
  4. 4.University HospitalLyonFrance
  5. 5.Department of Infectious Diseases and Infection Control UnitCHU Saint EtienneSaint Etienne Cedex 02France

Personalised recommendations