Advances in in vitro and in vivo models for studying the staphylococcal factors involved in implant infections

International Journal of Artificial Organs

Volumn 29, Issue 4, 2006, Pages 368-378

  Harraghy, Niamh ^a   Seiler, S ^a   Jacobs, K ^b   Hannig, M ^a   Menger, M D ^a   Herrmann, M ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Adherence; Biofilm; Implant infection; In vitro models; In vivo models; Staphylococcus aureus; Staphylococcus epidermidis

Indexed keywords

ASSAYS; BIOFILMS; REAL TIME SYSTEMS; SCANNING ELECTRON MICROSCOPY;

ADHERENCE; BIOFILM FORMATION; IMPLANT INFECTIONS; IN VIVO MODEL; IN-VITRO; IN-VITRO MODELS; IN-VIVO; STAPHYLOCOCCUS EPIDERMIDIS; VITRO AND IN VIVO; VIVO MODELS;

BACTERIA;

ANTIBIOTIC AGENT;

BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM IDENTIFICATION; BIOFILM; DEVICE INFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VITRO STUDY; IN VIVO STUDY; INFECTION RISK; ISOTOPE LABELING; MOLECULAR GENETICS; NONHUMAN; REVIEW; RISK FACTOR; STANDARDIZATION; STAPHYLOCOCCUS INFECTION;

EID: 33745279569     PISSN: 03913988     EISSN: None     Source Type: Journal    
DOI: 10.1177/039139880602900406     Document Type: Review

References (108)

1. Wisplinghoff H, Seifert H, Tallent SM, Bischoff T, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in pediatric patients in United States hospitals: Epidemiology, clinical features and susceptibilities. Pediatr Infect Dis J 2003; 22: 686-91.
2. Arciola CR, An YH, Campoccia D, Donati ME, Montanaro L. Etiology of implant orthopaedic infections: A survey on 1027 clinical isolates. Int J Artif Organs 2005; 28: 1091-100
3. Costerton JW, Montanaro L, Arciola CR. Biofilm in implant infections. Int J Artif Organs 2005; 28: 1062-8.
4. von Eiff C, Peters G, Heilmann C. Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2002; 2: 677-85.
5. Meyer HG, Wengler-Becker U, Gatermann SG. The hemagglutinin of Staphylococcus saprophyticus is a major adhesin for uroepithelial cells. Infect Immun 1996; 64: 3893-6.
6. Hell W, Meyer HG, Gatermann SG. Cloning of aas, a gene encoding a Staphylococcus saprophyticus surface protein with adhesive and autolytic properties. Mol Microbiol 1998; 29: 871-81.
7. Mitchell J, Tristan A, Foster TJ. Characterization of the fibrinogen-binding surface protein Fbl of Staphylococcus lugdunensis. Microbiology 2004; 150: 3831-41.
8. Christensen GD, Simpson WA, Bisno AL, Beachey EH. Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect Immun 1982; 37: 318-26.
9. Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM, et al. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: A quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 1985; 22: 996-1006.
10. Cramton SE, Gerke C, Gotz F. In vitro methods to study staphylococcal biofilm formation. Methods Enzymol 2001; 336: 239-55.
11. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40: 175-9.
12. Mack D, Siemssen N, Laufs R. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: Evidence for functional relation to intercellular adhesion. Infect Immun 1992; 60: 2048-57.
13. Mack D, Bartscht K, Fischer C, Rohde H, de Grahl C, Dobinsky S, et al. Genetic and biochemical analysis of Staphylococcus epidermidis biofilm accumulation. Methods Enzymol 2001; 336: 215-39.
14. Beenken KE, Blevins JS, Smeltzer MS. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect Immun 2003; 71: 4206-11.
15. Cerca N, Pier GB, Oliveira R, Azeredo J. Comparative evaluation of coagulase-negative staphylococci (CoNS) adherence to acrylic by a static method and a parallel-plate flow dynamic method. Res Microbiol 2004; 155: 755-60.
16. Knobloch JK, Horstkotte MA, Rohde H, Mack D. Evaluation of different detection methods of biofilm formation in Staphylococcus aureus. Med Microbiol Immunol (Berl) 2002; 191: 101-6.
17. Rohde H, Burdelski C, Bartscht K, Hussain M, Buck F, Horstkotte MA, et al. Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 2005; 55: 1883-95.
18. Arciola CR, Campoccia D, Baldassarri L, Donati ME, Pirini V, Gamberini S, Montanaro L. Detection of biofilm formation in Staphylococcus epidermidis from implant infections. Comparison of a PCR-method that recognizes the presence of ica genes with two classic phenotypic methods. J Biomed Mater Res A 2006; 76: 425-30.
19. Heilmann C, Thumm G, Chhatwal GS, Hartleib J, Uekotter A, Peters G. Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology 2003; 149: 2769-78.
20. Simpson KH, Bowden MG, Peacock SJ, Arya M, Hook M, Anvari B. Adherence of Staphylococcus aureus fibronectin binding protein A mutants: An investigation using optical tweezers. Biomol Eng 2004; 21: 105-11.
21. Peacock SJ, Day NP, Thomas MG, Berendt AR, Foster TJ. Clinical isolates of Staphylococcus aureus exhibit diversity in fnb genes and adhesion to human fibronectin. J Infect 2000; 41: 23-31.
22. Vaudaux P, Suzuki R, Waldvogel FA, Morgenthaler JJ, Nydegger UE. Foreign body infection: Role of fibronectin as a ligand for the adherence of Staphylococcus aureus. J Infect Dis 1984; 150: 546-53.
23. Vaudaux P, Pittet D, Haeberli A, Lerch PG, Morgenthaler JJ, Proctor RA, et al. Fibronectin is more active than fibrin or fibrinogen in promoting Staphylococcus aureus adherence to inserted intravascular catheters. J Infect Dis 1993; 167: 633-41.
24. Greene C, McDevitt D, Francois P, Vaudaux PE, Lew DP, Foster TJ. Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol Microbiol 1995; 17: 1143-52.
25. Schröder AC, Herrmann M, Schmidbauer J, Ruprecht KW. Influence of fibronectin on the bacterial adherence to coated and uncoated intraocular lenses. Proceedings of the 22nd Congress of the European Society of Cataract and Refractive Surgery; 2004 Sept 18-22; Paris, France.
26. Kerdudou S, Laschke MW, Sinha B, Menger MD, Herrmann M. Growth phase dependency of Staphylococcus aureus interaction with the microvascular endothelium; Major role of the staphylococcal surface protein, fibronectin binding protein A. Abstract MPP041. Presented at the 57th Congress of the German Society for Microbiology and Hygiene; 2005 Sept 25-28; Göttingen, Germany. Biospektrum 2005; p 119.
27. Heilmann C, Gerke C, Perdreau-Remington F, Gotz F. Characterization of Tn917 insertio mutants of Staphylococcus epidermidis affected in biofilm formation. Infect Immun 1996; 64: 277-82.
28. Donlan RM, Costerton JW. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-93.
29. Yarwood JM, Bartels DJ, Volper EM, Greenberg EP. Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 2004; 186: 1838-50.
30. Beyenal H, Yakymyshyn C, Hyungnak J, Davis CC, Lewandowski Z. An optical microsensor to measure fluorescent light intensity in biofilms. J Microbiol Methods 2004; 58: 367-74.
31. Yang X, Beyenal H, Harkin G, Lewandowski Z. Quantifying biofilm structure using image analysis. J Microbiol Methods 2000; 39: 109-19.
32. Laschke MW, Kerdudou S, Herrmann M, Menger MD. Intravital fluorescence microscopy: A novel tool for the study of the interaction of Staphylococcus aureus with the microvascular endothelium in vivo. J Infect Dis 2005; 191: 435-43.
33. Pratten J, Foster SJ, Chan PF, Wilson M, Nair SP. Staphylococcus aureus accessory regulators: Expression within biofilms and effect on adhesion. Microbes Infect 2001; 3: 633-7.
34. Leid JG, Shirtliff ME, Costerton JW, Stoodley AP. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun 2002; 70: 6339-45.
35. Rupp CJ, Fux CA, Stoodley P. Viscoelasticity of Staphylococcus aureus biofilms in response to fluid shear allows resistance to detachment and facilitates rolling migration. Appl Environ Microbiol 2005; 71: 2175-8.
36. Dickinson RB, Nagel JA, McDevitt D, Foster TJ, Proctor RA, Cooper SL. Quantitative comparison of clumping factor- and coagulase-mediated Staphylococcus aureus adhesion to surface-bound fibrinogen under flow. Infect Immun 1995; 63: 3143-50.
37. McCoy WF, Bryers JD, Robbins J, Costerton JW. Observations of fouling biofilm formation. Can J Microbiol 1981; 27: 910-7.
38. Evans RC, Holmes CJ. Effect of vancomycin hydrochloride on Staphylococcus epidermidis biofilm associated with silicone elastomer. Antimicrob Agents Chemother 1987; 31: 889-94.
39. Schultz CL, Pezzutti MR, Silor D, White R. Bacterial adhesion measurements on soft contact lenses using a Modified Vortex Device and a Modified Robbins Device. J Ind Microbiol 1995; 15: 243-7.
40. Linton CJ, Sherriff A, Millar MR. Use of a modified Robbins device to directly compare the adhesion of Staphylococcus epidermidis RP62A to surfaces. J Appl Microbiol 1999; 86: 194-202.
41. Kharazmi A, Giwercman B, Hoiby N. Robbins device in biofilm research. Methods Enzymol 1999; 310: 207-15.
42. Millar MR, Linton CJ, Sherriff A. Use of a continuous culture system linked to a modified Robbins device or flow cell to study attachment of bacteria to surfaces. Methods Enzymol 2001; 337: 43-62.
43. Becker P, Hufnagle W, Peters G, Herrmann M. Detection of differential gene expression in biofilm-forming versus planktonic populations of Staphylococcus aureus using micro-representational-difference analysis. Appl Environ Microbiol 2001; 67: 2958-65.
44. Chatterjee I, Becker P, Grundmeier M, Bischoff M, Somerville GA, Peters G, et al. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J Bacteriol 2005; 187: 4488-96.
45. Vuong C, Kidder JB, Jacobson ER, Otto M, Proctor RA, Somerville GA. Staphylococcus epidermidis polysaccharide intercellular adhesin production significantly increases during tricarboxylic acid cycle stress. J Bacteriol 2005; 187: 2967-73.
46. Beenken KE, Dunman PM, McAleese F, Macapagal D, Murphy E, Projan SJ, et al. Global gene expression in Staphylococcus aureus biofilms. J Bacteriol 2004; 186: 4665-84.
47. B is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate. J Bacteriol 2000; 182: 6824-6.
48. B is essential or biofilm development by Staphylococcus aureus. Mol Microbiol 2003; 48: 1075-87.
49. Que YA, Francois P, Haefliger JA, Entenza JM, Vaudaux P, Moreillon P. Reassessing the role of Staphylococcus aureus clumping factor and fibronectin-binding protein by expression in Lactococcus lactis. Infect Immun 2001; 69: 6296-302.
50. Que YA, Haefliger JA, Piroth L, Francois P, Widmer E, Entenza JM, et al. Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med 2005; 201: 1627-35.
51. Cerca N, Pier GB, Vilanova M, Oliveira R, Azeredo J. Influence of batch or fed-batch growth on Staphylococcus epidermidis biofilm formation. Lett Appl Microbiol 2004; 39: 420-4.
52. Denyer SP, Davies MC, Evans JA, Finch RG, Smith DG, Wilcox MH, et al. Influence of carbon dioxide on the surface characteristics and adherence potential of coagulase-negative staphylococci. J Clin Microbiol 1990; 28: 1813-7.
53. Gorman SP, Jones DS, Mawhinney WM, McGovern JG, Adair CG. Conditioning fluid influences on the surface properties of silicone and polyurethane peritoneal catheters: Implications for infection. J Mater Sci Mater Med 1997; 8: 631-5.
54. Sadovskaya I, Vinogradov E, Flahaut S, Kogan G, Jabbouri S. Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A. Infect Immun 2005; 73: 3007-17.
55. Livni G, Yuhas Y, Ashkenazi S, Michowiz S. In vitro bacterial adherence to ventriculoperitoneal shunts. Pediatr Neurosurg 2004; 40: 64-9.
56. Maira-Litran T, Kropec A, Goldmann D, Pier GB. Biologic properties and vaccine potential of the staphylococcal poly-N-acetyl glucosamine surface polysaccharide. Vaccine 2004; 22: 872-9.
57. Mack D, Becker P, Chatterjee I, Dobinsky S, Knobloch JK, Peters G, et al. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: Functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 2004; 294: 203-12.
58. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 1996; 20: 1083-91.
59. McKenney D, Hubner J, Muller E, Wang Y, Goldmann DA, Pier GB. The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect Immun 1998; 66: 4711-20.
60. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 1999; 67: 5427-33.
61. Dobinsky S, Kiel K, Rohde H, Bartscht K, Knobloch JK, Horstkotte MA, et al. Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: Evidence for an additional factor required for polysaccharide intercellular adhesin synthesis. J Bacteriol 2003; 185: 2879-86.
62. Heilmann C, Gotz F. Further characterization of Staphylococcus epidermidis transposon mutants deficient in primary attachment or intercellular adhesion. Zentralbl Bakteriol 1998; 287: 69-83.
63. Cerca N, Pier GB, Vilanova M, Oliveira R, Azeredo J. Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Res Microbiol 2005; 156: 506-14.
64. Zimmerli W, Waldvogel FA, Vaudaux P, Nydegger UE. Pathogenesis of foreign body infection: Description and characteristics of an animal model. J Infect Dis 1982; 146: 487-97.
65. Vaudaux P, Grau GE, Huggler E, Schumacher-Perdreau F, Fiedler F, Waldvogel FA, et al. Contribution of tumor necrosis factor to host defense against staphylococci in a guinea pig model of foreign body infections. J Infect Dis 1992; 166: 58-64.
66. Goerke C, Fluckiger U, Steinhuber A, Zimmerli W, Wolz C. Impact of the regulatory loci agr, sarA and sae of Staphylococcus aureus on the induction of alpha-toxin during device-related infection resolved by direct quantitative transcript analysis. Mol Microbiol 2001; 40: 1439-47.
67. B in virulence gene expression during device-related infection. Infect Immun 2005; 73: 3415-21.
68. Rupp ME, Ulphani JS, Fey PD, Mack D. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect Immun 1999; 67: 2656-9.
69. Rupp ME, Ulphani JS, Fey PD, Bartscht K, Mack D. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect Immun 1999; 67: 2627-32.
70. Fluckiger U, Ulrich M, Steinhuber A, Doring G, Mack D, Landmann R, et al. Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect Immun 2005; 73: 1811-9.
71. Kristian SA, Golda T, Ferracin F, Cramton SE, Neumeister B, Peschel A, et al. The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microb Pathog 2004; 36: 237-45.
72. Francois P, Tu Quoc PH, Bisognano C, Kelley WL, Lew DP, Schrenzel J, et al. Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis. FEMS Immunol Med Microbiol 2003; 35: 135-40.
73. Galliani S, Viot M, Cremieux A, van der Auwera AP. Early adhesion of bacteremic strains of Staphylococcus epidermidis to polystyrene: Influence of hydrophobicity, slime production, plasma, albumin, fibrinogen, and fibronectin. J Lab Clin Med 1994; 123: 685-92.
74. Galliani S, Cremieux A, van der Auwera AP, Viot M. Influence of strain, biomaterial, proteins, and oncostatic chemotherapy on Staphylococcus epidermidis adhesion to intravascular catheters in vitro. J Lab Clin Med 1996; 127: 71-80.
75. Kadurugamuwa JL, Sin L, Albert E, Yu J, Francis K, DeBoer M, et al. Direct continuous method for monitoring biofilm infection in a mouse model. Infect Immun 2003; 71: 882-90.
76. Kadurugamuwa JL, Sin LV, Yu J, Francis KP, Purchio TF, Contag PR. Noninvasive optical imaging method to evaluate postantibiotic effects on biofilm infection in viva. Antimicrob Agents Chemother 2004; 48: 2283-7.
77. Xiong YQ, Willard J, Kadurugamuwa JL, Yu J, Francis KP, Bayer AS. Real-time in vivo bioluminescent imaging for evaluating the efficacy of antibiotics in a rat Staphylococcus aureus endocarditis model. Antimicrob Agents Chemother 2005; 49: 380-7.
78. Fischer B, Vaudaux P, Magnin M, el Mestikawy Y, Proctor RA, Lew DP, et al. Novel animal model for studying the molecular mechanisms of bacterial adhesion to one-implanted metallic devices: Role of fibronectin in Staphylococcus aureus adhesion. J Orthop Res 1996; 14: 914-20.
79. Arens S, Schlegel U, Printzen G, Ziegler WJ, Perren SM, Hansis M. Influence of materials for fixation implants on local infection. An experimental study of steel versus titanium DCP in rabbits. J Bone Joint Surg Br 1996; 78: 647-51.
80. Sheehan E, McKenna J, Mulhall KJ, Marks P, McCormack D. Adhesion of Staphylococcus to orthopaedic metals, an in vivo study. J Orthop Res 2004; 22: 39-43.
81. Menger MD, Hammersen F, Messmer K. In vivo assessment of neovascularization and incorporation of prosthetic vascular biografts. Thorac Cardiovasc Surg 1992; 40: 19-25.
82. Menger MD, Hammersen F, Walter P, Messmer K. Neovascularization of prosthetic vascular grafts. Quantitative analysis of angiogenesis and microhemodynamics by means of intravital microscopy. Thorac Cardiovasc Surg 1990; 38: 139-45.
83. Menger MD, Walter P, Hammersen F, Messmer K. Quantitative analysis of neovascularization of different PTFE-implants. Eur J Cardiothorac Surg 1990; 4: 191-6.
84. Laschke MW, Haufel JM, Thorlacius H, Menger MD. New experimental approach to study host tissue response to surgical mesh materials in viva. J Biomed Mater Res A 2005; 74: 696-704.
85. Kraft CN, Hansis M, Arens S, Menger MD, Vollmar B. Striated muscle microvascular response to silver implants: A comparative in vivo study with titanium and stainless steel. J Biomed Mater Res 2000; 49: 192-9.
86. Kraft CN, Hansis M, Menger MD, Sahl HG, Vollmar B. Control of local bacterial soft tissue contamination by adequate microvascular response is critically dependent on the extent of bacterial challenge. European Journal of Trauma 2001; 27: 199-209.
87. Bowen WR, Lovitt RW, Wright CJ. Atomic force microscopy study of the adhesion of Saccharomyces cerevisiae. J Colloid Interface Sci 2001; 237: 54-61.
88. Emerson RJ, Camesano TA. Nanoscale investigation of pathogenic microbial adhesion to a biomaterial. Appl Environ Microbiol 2004; 70: 6012-22.
89. Arciola CR, Bustanji Y, Conti M, Campoccia D, Baldassarri L, Samori B, Montanaro L. Staphylococcus epidermidis-fibronectin binding and its inhibition by heparin. Biomaterials 2003; 24: 3013-9.
90. Bustanji Y, Arciola CR, Conti M, Mandello E, Montanaro L, Samori B. Dynamics of the interaction between a fibronectin molecule and a living bacterium under mechanical force. Proc Natl Acad Sci USA 2003; 100: 13292-7.
91. Sanford BA, de Feijter AW, Wade MH, Thomas VL. A dual fluorescence technique for visualization of Staphylococcus epidermidis biofilm using scanning confocal laser microscopy. J Ind Microbiol 1996; 16: 48-56.
92. Strathmann M, Wingender J. Use of an oxonol dye in combination with confocal laser scanning microscopy to monitor damage to Staphylococcus aureus cells during colonisation of silver-coated vascular grafts. Int J Antimicrob Agents 2004; 24: 234-40.
93. Parsek MR, Greenberg EP. Quorum sensing signals in development of Pseudomonas aeruginosa biofilms. Methods Enzymol 1999; 310: 43-55.
94. Gottenbos B, van der Mei HG, Busscher HJ. Models for studying initial adhesion and surface growth in biofilm formation on surfaces. Biofilms 1999; 310: 523-34.
95. Christensen GD, Simpson WA, Bisno AL, Beachey EH. Experimental foreign body infections in mice challenged with slime-producing Staphylococcus epidermidis. Infect Immun 1983; 40: 407-10.
96. Gallimore B, Gagnon RF, Subang R, Richards GK. Natural history of chronic Staphylococcus epidermidis foreign body infection in a mouse model. J Infect Dis 1991; 164: 1220-3.
97. Rupp ME, Fey PD. In vivo models to evaluate adhesion and biofilm formation by Staphylococcus epidermidis. Methods Enzymol 2001; 336: 206-15.
98. Kadurugamuwa JL, Sin LV, Yu J, Francis KP, Kimura R, Purchio T, et al. Rapid direct method for monitoring antibiotics in a mouse model of bacterial biofilm infection. Antimicrob Agents Chemother 2003; 47: 3130-7.
99. Vaudaux P, Grau GE, Huggler E, Schumacher-Perdreau F, Fiedler F, Waldvogel FA, et al. Contribution of tumor necrosis factor to host defense against staphylococci in a guinea pig model of foreign body infections. J Infect Dis 1992; 166: 58-64.
100. Mayberry-Carson KJ, Tober-Meyer B, Smith JK, Lambe DW Jr, Costerton JW. Bacterial adherence and glycocalyx formation in osteomyelitis experimentally induced with Staphylococcus aureus. Infect Immun 1984; 43: 825-33.
101. Cheung AL, Bayer AS, Zhang G, Gresham H, Xiong YQ. Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol Med Microbiol 2004; 40: 1-9.
102. Baddour LM, Tayidi MM, Walker E, McDevitt D, Foster TJ. Virulence of coagulase-deficient mutants of Staphylococcus aureus in experimental endocarditis. J Med Microbiol 1994; 41: 259-63.
103. Cheung AL, Eberhardt KJ, Chung E, Yeaman MR, Sullam PM, Ramos M, et al. Diminished virulence of a sar-/agr-mutant of Staphylococcus aureus in the rabbit model of endocarditis. J Clin Invest 1994; 94: 1815-22.
104. Shiro H, Muller E, Gutierrez N, Boisot S, Grout M, Tosteson TD, et al. Transposon mutants of Staphylococcus epidermidis deficient in elaboration of capsular polysaccharide/adhesin and slime are avirulent in a rabbit model of endocarditis. J Infect Dis 1994; 169: 1042-9.
105. Perdreau-Remington F, Sande MA, Peters G, Chambers HF. The abilities of a Staphylococcus epidermidis wild-type strain and its slime-negative mutant to induce endocarditis in rabbits are comparable. Infect Immun 1998; 66: 2778-81.
106. Xiong YQ, Van Wamel W, Nast CC, Yeaman MR, Cheung AL, Bayer AS. Activation and transcriptional interaction between agr RNAII and RNAIII in Staphylococcus aureus in vitro and in an experimental endocarditis model. J Infect Dis 2002; 186: 668-77.
107. Vaudaux PE, Francois P, Proctor RA, McDevitt D, Foster TJ, Albrecht RM, et al. Use of adhesion-defective mutants of Staphylococcus aureus to define the role of specific plasma proteins in promoting bacterial adhesion to canine arteriovenous shunts. Infect Immun 1995; 63: 585-90.
108. Francois P, Vaudaux P, Lew PD. Role of plasma and extracellular matrix proteins in the physiopathology of foreign body infections. Ann Vasc Surg 1998; 12: 34-40.