Advanced search
Publication Cover
Acta Orthopaedica Volume 78, 2007 - Issue 3
Journal homepage
2,873
Views
93
CrossRef citations to date
0
Altmetric
Review

The role of small-colony variants in failure to diagnose and treat biofilm infections in orthopedics

Daniëlle Neut Department of Biomedical Engineering, University Medical Center Groningen, and University of Groningen, Groningen, the Netherlands; Department of Orthopaedic Surgery, University Medical Center Groningen, and University of Groningen, Groningen, he NetherlandsCorrespondence[email protected]
,
Henny C Van Der Mei Department of Biomedical Engineering, University Medical Center Groningen, and University of Groningen, Groningen, the Netherlands
,
Sjoerd K Bulstra Department of Orthopaedic Surgery, University Medical Center Groningen, and University of Groningen, Groningen, he Netherlands
&
Henk J Busscher Department of Biomedical Engineering, University Medical Center Groningen, and University of Groningen, Groningen, the Netherlands
Pages 299-308 | Received 19 Jul 2006, Accepted 30 Oct 2006, Published online: 08 Jul 2009

  • Arciola C R, Campoccia D, Gamberini S, Donati M E, Pirini V, Visai L, Speziale P, Montanaro L. Antibiotic resistance in exopolysaccharide-forming Staphylococcus epidermidis clinical isolates from orthopaedic implant infections. Biomaterials 2005; 26: 6530–5
  • Ashby M J, Neale J E, Knott S J, Critchley I A. Effect of antibiotics on non–growing planktonic cells and biofilms of Escherichia coli. J Antimicrob Chemother 1994; 33: 443–52
  • Atkins B L, Bowler I C. The diagnosis of large joint sepsis. J Hosp Infect 1998; 40: 263–74
  • Balwit J M, Van Langevelde P, Vann J M, Proctor R A. Gentamicin–resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J Infect Dis 1994; 170: 1033–7
  • Barrack R L, Jennings R W, Wolfe M W, Bertot A J. The value of preoperative aspiration before total knee revision. Clin Orthop 1997, 345: 8–16
  • Baumert N, Von Eiff C, Schaaff F, Peters G, Proctor R A, Sahl H G. Physiology and antibiotic susceptibility of Staphylococcus aureus small colony variants. Microb Drug Resist 2002; 8: 253–60
  • Bayer A S, Norman D C, Kim K S. Characterization of impermeability variants of Pseudomonas aeruginosa isolated during unsuccessful therapy of experimental endocarditis. Antimicrob Agents Chemother 1987; 31: 70–5
  • Bayston R. Biofilms and prosthetic devices. Community structure and co–operation in biofilms, D G Allison, P Gilbert, H M Lappin–Scott, M Wilson. Cambridge university press. 2000: 295–308
  • Bergoge–Berezin E. Resistance and new antibiotic strategies The problem with staphylococcus. Presse Med 2000; 29: 2018–21
  • Bos R, Van der Mei H C, Busscher H J. Physico–chemistry of initial microbial adhesive interactions––its mechanisms and methods for study. FEMS Microbiol Rev 1999; 23: 179–230
  • Cochran W L, Suh S J, McFeters G A, Stewart P S. Role of RpoS and AlgT in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide and monochloramine. J Appl Microbiol 2000; 88: 546–53
  • Cogan N G. Effects of persister formation on bacterial response to dosing. J Theor Biol 2006; 238: 694–703
  • Costerton J W, Cheng K J, Geesey G G, Ladd T I, Nickel J C, Dasgupta M, Marrie T J. Bacterial biofilms in nature and disease. Annu Rev Microbiol 1987; 41: 435–64
  • Costerton J W, Stewart P S, Greenberg E P. Bacterial biofilms: a common cause of persistent infections. Science 1999; 284: 1318–22
  • Darouiche R O, Dhir A, Miller A J, Landon G C, Raad I I, Musher D M. Vancomycin penetration into biofilm covering infected prostheses and effect on bacteria. J Infect Dis 1994; 170: 720–3
  • Davenport D S, Massanari R M, Pfaller M A, Bale M J, Streed S A, Hierholzer W J, Jr. Usefulness of a test for slime production as a marker for clinically significant infections with coagulase–negative staphylococci. J Infect Dis 1986; 153: 332–9
  • Drenkard E, Ausubel F M. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 2002; 416: 740–3
  • Fux C A, Costerton J W, Stewart P S, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol 2005; 13: 34–40
  • Gracia E, Fernandez A, Conchello P, Lacleriga A, Paniagua L, Seral F, Amorena B. Adherence of Staphylococcus aureus slime–producing strain variants to biomaterials used in orthopaedic surgery. Int Orthop 1997; 21: 46–51
  • Gristina A G. Biomaterial–centered infection; microbial adhesion versus tissue integration. Science 1987; 237: 1588–95
  • Gristina A G, Costerton J W. Bacterial adherence to biomaterials and tissue: The significance of its role in clinical sepsis. J Bone Joint Surg (Am) 1985; 67: 264–73
  • Haussler S, Tummler B, Weissbrodt H, Rohde M, Steinmetz I. Small–colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 1999; 29: 621–5
  • Hudson M C, Ramp W K, Nicholson N C, Williams A S, Nousiainen M T. Internalization of Staphylococcus aureus by cultured osteoblasts. Microb Pathog 1995; 19: 409–19
  • Jefferson K K, Goldmann D A, Pier G B. Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms. Antimicrob Agents Chemother 2005; 49: 2467–73
  • Josefsson G, Kolmert L. Prophylaxis with systematic antibiotics versus gentamicin bone cement in total hip arthroplasty. A ten–year survey of 1,688 hips. Clin Orthop 1993, 292: 210–4
  • Kahl B, Herrmann M, Everding A S, Koch H G, Becker K, Harms E, Proctor R A, Peters G. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J Infect Dis 1998; 177: 1023–9
  • Kahl B C, Belling G, Reichelt R, Herrmann M, Proctor R A, Peters G. Thymidine–dependent small–colony variants of Staphylococcus aureus exhibit gross morphological and ultrastructural changes consistent with impaired cell separation. J Clin Microbiol 2003a; 41: 410–3
  • Kahl B C, Duebbers A, Lubritz G, Haeberle J, Koch H G, Ritzerfeld B, Reilly M, Harms E, Proctor R A, Herrmann M, Peters G. Population dynamics of persistent Staphylococcus aureus isolated from the airways of cystic fibrosis patients during a 6–year prospective study. J Clin Microbiol 2003b; 41: 4424–7
  • Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K. Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 2004; 230: 13–8
  • Kirisits M J, Prost L, Starkey M, Parsek M R. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2005; 71: 4809–21
  • Kragsbjerg P, Holmberg H. Serum concentrations of inter–leukin–6, tumour necrosis factor–a, and C–reactive protein in patients undergoing major operations. Eur J Surg 1995; 161: 17–22
  • Kurtz S, Mowat F, Ong K, Chan N, Lau E, Halpern M. Prevalence of primary and revision total hip and knee arthroplasty in the United States from 1990 through 2002. J Bone Joint Surg (Am) 2005; 87: 1487–97
  • Langford P R, Anwar H, Gonda I, Brown M R. Outer membrane proteins of gentamicin induced small colony variants of Pseudomonas aeruginosa. FEMS Microbiol Lett 1989; 61: 33–6
  • Lewis K. Persister cells and the riddle of biofilm survival. Biochemistry (Mosc) 2005; 70: 267–74
  • Lewis L A, Li K B, Gousse A, Pereira F, Pacheco N, Pierre S, Kodaman P, Lawson S. Genetic and molecular analysis of spontaneous respiratory deficient (res) mutants of Escherichia coli K–12. Microbiol Immunol 1991; 35: 289–301
  • Lidwell O M, Lowbury E J, Whyte W, Blowers R, Stanley S J, Lowe D. Airborne contamination of wounds in joint replacement operations: the relationship to sepsis rates. J Hosp Infect 1983; 4: 111–31
  • Looney W J. Small–colony variants of Staphylococcus aureus. Br J Biomed Sci 2000; 57: 317–22
  • Mah T F, Pitts B, Pellock B, Walker G C, Stewart P S, O'Toole G A. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 2003; 426: 306–10
  • McDonald D J, Fitzgerald R H, Jr, Ilstrup D M. Two–stage reconstruction of a total hip arthroplasty because of infection. J Bone Joint Surg (Am) 1989; 71: 828–34
  • Muli F W, Struthers J K. The growth of Gardnerella vaginalis and Lactobacillus acidophilus in Sorbarod biofilms. J Med Microbiol 1998; 47: 401–5
  • Musher D M, Baughn R E, Templeton G B, Minuth J N. Emergence of variant forms of Staphylococcus aureus after exposure to gentamicin and infectivity of the variants in experimental animals. J Infect Dis 1977; 136: 360–9
  • Neut D, Van de Belt H, Stokroos I, Van Horn J R, Van der Mei H C, Busscher H J. Biomaterials–associated infection of gentamicin–loaded PMMA beads in orthopaedic revision surgery. J Antimicro Chemo 2001; 47: 885–91
  • Neut D, Van Horn J R, Van Kooten T G, Van der Mei H C, Busscher H J. Detection of biomaterial–associated infections in orthopaedic joint implants. Clin Orthop 2003, 413: 261–8
  • Ng T. Erythrocyte sedimentation rate, plasma viscosity and C–reactive protein in clinical practice. Br J Hosp Med 1998; 58: 521–3
  • Philips J E, Crane T P. The incidence of deep prosthetic infections. J Bone Joint Surg (Br) 2006; 88(7)943–8
  • Philips W C, Kattapuram S V. Efficiacy of preoperative hip aspiration performed in the radiology department. Clin Orthop 1983, 179: 141–6
  • Pittet D, Ducel G. Infectious risk factors related to operating rooms. Infect Control Hosp Epidemiol 1994; 15: 456–62
  • Proctor R A. Microbial pathogenic factors: small colony. Infections associated with indwelling medical devices variants, A L Bisno, F A Waldvogel. American Society for Microbiology, Washington, DC 1994; 79–90
  • Proctor R A, Peters G. Small colony variants in staphylococcal infections: diagnostic and therapeutic implications. Clin Infect Dis 1998; 27: 419–23
  • Proctor R A, Van Langevelde P, Kristjansson M, Maslow J N, Arbeit R D. Persistent and relapsing infections associated with small–colony variants of Staphylococcus aureus. Clin Infect Dis 1995; 20: 95–102
  • Proctor R A, Kahl B, von Eiff C, Vaudaux P E, Lew D P, Peters G. Staphylococcal small colony variants have novel mechanisms for antibiotic resistance. Clin Infect Dis 1998; 27: S68–S74
  • Proctor R A, von Eiff C, Kahl B C, Becker K, McNamara P, Herrmann M, Peters G. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 2006; 4: 295–305
  • Roberts M E, Stewart P S. Modelling protection from antimicrobial agents in biofilms through the formation of persister cells. Microbiology 2005; 151: 75–80
  • Roggenkamp A, Sing A, Hornef M, Brunner U, Autenrieth I B, Heesemann J. Chronic prosthetic hip infection caused by a small–colony variant of Escherichia coli. J Clin Microb 1998; 36: 2530–4
  • Rusthoven J J, Davies T A, Lerner S A. Clinical isolation and characterization of aminoglycoside–resistant small colony variants of Enterobacter aerogenes. Am J Med 1979; 67: 702–6
  • Sanzén L, Carlsson A S. The diagnostic valuen of C–reactive protein in infected total hip arhtroplasties. J Bone Joint Surg (Br) 1989; 71: 638–41
  • Seifert H, Von Eiff C, Fätkenheuer G. Fatal case due to methicillin–resistant Staphylococcus aureus small colony variants in an AIDS patient. Emerg Infect Dis 1999; 5: 450–3
  • Seifert H, Wisplinghoff H, Schnabel P, von Eiff C. Small colony variants of Staphylococcus aureus and pacemakerrelated infection. Emerg Infect Dis 2003; 9: 1316–8
  • Sendi P, Rohrbach M, Graber P, Frei R, Ochsner P E, Zimmerli W. Staphylococcus aureus small colony variants in prosthetic joint infection. Clin Infect Dis 2006; 43: 961–7
  • Sheldon A T, Jr. Antibiotic resistance: a survival strategy. Clin Lab Sci 2005; 18: 170–80
  • Shih L Y, Wu J J, Yang D J. Erythrocyte sedimentation rate and C–reactive protein values in patients with total hip arthroplasty. Clin Orthop 1987; 225: 238–46
  • Spanu T, Romano L, D'Inzeo T, Masucci L, Albanese A, Papacci F, Marchese E, Sanguinetti M, Fadda G. Recurrent ventriculoperitoneal shunt infection caused by smallcolony variants of Staphylococcus aureus. Clin Infect Dis 2005; 41: 48–52
  • Stewart P S. Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 2002; 292: 107–13
  • Tattevin P, Cremieux A C, Pottier P, Huten D, Carbon C. Prosthetic joint infection: when can prosthesis salvage be considered. Clin Infect Dis 1999; 29: 292–5
  • Tunney M M, Patrick S, Gorman S P, Nixon J R, Anderson N, Davis R I, Hanna D, Ramage G. Improved detection of infection in hip replacements A currently underestimated problem. J Bone Joint Surg (Br) 1998; 80: 568–72
  • Vaudaux P, Francois P, Bisognano C, Kelley W L, Lew D P, Schrenzel J, Proctor R A, McNamara P J, Peters G, Von Eiff C. Increased expression of clumping factor and fibro–nectin–binding proteins by hemB mutants of Staphylococacus aureus expressing small colony variant phenotypes. Infect Immun 2002; 70: 5428–37
  • Vaudaux P, Kelley W L, Lew D P. Staphylococcus aureus small colony variants: difficult to diagnose and difficult to treat. Clin Infect Dis 2006; 43: 968–70
  • Von Eiff C, Bettin D, Proctor R A, Rolauffs B, Lindner N, Winkelmann W, Peters G. Recovery of small colony variants of Staphylococcus aureus following gentamicin bead placement for osteomyelitis. Clin Infect Dis 1997; 25: 1250–1
  • Von Eiff C, Vaudaux P, Kahl B C, Lew D, Emler S, Schmidt A, Peters G, Proctor R A. Bloodstream infections caused by small–colony variants of coagulase–negative staphylococci following pacemaker implantation. Clin Infect Dis 1999; 29: 932–4
  • Von Eiff C, Proctor R A, Peters G. Staphylococcus aureus small colony variants: formation and clinical impact. Int J Clin Pract 2000; 115: S44–9
  • Von Eiff C, Becker K, Metze D, Lubritz G, Hockmann J, Schwarz T, Peters G. Intracellular persistence of Staphylococcus aureus small–colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with Darier's disease. Clin Infect Dis 2001; 32: 1643–7
  • Walenkamp G H I M. Chronic osteomyelitis. Acta Orthop Scand 1997; 68: 497–506
  • Widmer A F. New developments in diagnosis and treatment of infection in orthopedic implants. Clin Infect Dis 2001; 33: S94–106
  • Widmer A F, Frei R, Rajacic Z, Zimmerli W. Correlation between in vivo and in vitro efficacy of antimicrobial agents against foreign body infections. J Infect Dis 1990; 162: 96–102
  • Wise R I. Small colonies (G variants) of staphylococci: isolation from cultures and infection. Ann NY Acad Sci 1998; 65: 169–74
  • Zheng Z, Stewart P S. Penetration of rifampin through Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 2002; 46: 900–3

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.