Characteristics of bacterial biofilm associated with implant material in clinical practice

Polymer Journal

Volumn 45, Issue 2, 2013, Pages 137-152

  Nandakumar, Venkatesan ^a   Chittaranjan, Samuel ^b   Kurian, Valikapathalil Mathew ^c   Doble, Mukesh ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

^b CHRISTIAN MEDICAL COLLEGE   (India)

^c INSTITUTE OF CARDIOVASCULAR DISEASES   (India)

Author keywords

antimicrobial resistance; cardiology; computational approach; implants; material design; orthopedics; quorum sensing

Indexed keywords

ANTIMICROBIAL RESISTANCES; BACTERIAL ADHESION; BACTERIAL BIOFILM; BIOFILM FORMATION; CLINICAL PRACTICES; COMPUTATIONAL APPROACH; HOST CELLS; IMPLANT MATERIALS; IN-VIVO; LONG CHAINS; MATERIAL DESIGNS; POLYMERIC IMPLANTS; QUORUM-SENSING; UROLOGICAL IMPLANT; VASCULAR GRAFTS;

BACTERIA; CARDIOLOGY; DENTAL PROSTHESES; GRAFTS; IMAGING TECHNIQUES; MONOCLONAL ANTIBODIES; ORTHOPEDICS; PRODUCT DEVELOPMENT; TISSUE;

BIOFILMS;

EID: 84873592040     PISSN: 00323896     EISSN: 13490540     Source Type: Journal    
DOI: 10.1038/pj.2012.130     Document Type: Review

References (250)

1. Jass, J., Surman, S. & Walker, J. T. Medical Biofilms: Detection, Prevention, and Control Vol. 2 (Wiley, UK, 2003).
2. Richards, M. J., Edwards, J. R., Culver, D. H. & Gaynes, R. P. Nosocomial infections in medical intensive care units in the United States. Crit. Care Med. 27, 887 (1999).
3. O'Toole, G., Kaplan, H. B. & Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54, 49-79 (2000).
4. Zhang, X., Bishop, P. L. & Kupferle, M. J. Measurement of polysaccharides and proteins in biofilm extracellular polymers. Water Sci. Technol. 37, 345-348 (1998).
5. Trampuz, A. & Zimmerli, W. Diagnosis and treatment of infections associated with fracture-fixation devices. Injury 37, S59-S66 (2006).
6. Gustilo, R. B., Gruninger, R. P. & Davis, T. Classification of type III (severe) open fractures relative to treatment and results. Orthopedics 10, 1781 (1987).
7. Willenegger, H. & Roth, B. [Treatment tactics and late results in early infection following osteosynthesis]. Unfallchirurgie 12, 241 (1986).
8. Arens, S., Hansis, M., Schlegel, U., Eijer, H., Printzen, G., Ziegler, W. J. & Perren, S. M. Infection after open reduction and internal fixation with dynamic compression plates-clinical and experimental data. Injury 27(Suppl 3), SC27-SC33 (1996).
9. Arens, S., Kraft, C, Schlegel, U., Printzen, G., Perren, S. M. & Hansis, M. Susceptibility to local infection in biological internal fixation. Experimental study of open vs minimally invasive plate osteosynthesis in rabbits. Arch. Orthop. Trauma Surg. 119, 82-85 (1999).
10. Law, Jr M. D. & Stein, R. E. Late infection in healed fractures after open reduction and internal fixation. Orthopaed. Rev. 22, 545 (1993).
11. Maderazo, E. G., Judson, S. & Pasternak, H. Late infections of total joint prostheses: a review and recommendations for prevention. Clin. Orthop. Relat. Res. 229, 131 (1988).
12. Campoccia, D., Montanaro, L. & Arciola, C. R. Current methods for molecular epidemiology studies of implant infections. Int. J. Artif. Organs 32, 642 (2009).
13. Baldassarri, L., Donnelli, G., Gelosia, A., Voglino, M. C, Simpson, A. W. & Christensen, G. D. Purification and characterization of the staphylococcal slime-associated antigen and its occurrence among Staphylococcus epidermis clinical isolates. Infect. Immun. 64, 3410-3415 (1996).
14. Hussain, M., Wilcox, M. H. & White, P. J. The slime of coagulase-negative staphylococci: biochemistry and relation to adherence. FEMS Microbiol. Lett. 104, 191-207 (1993).
15. Hazan, Z., Zumeris, J., Jacob, H., Raskin, H., Kratysh, G., Vishnia, M., Dror, N., Barliya, T., Mandel, M. & Lavie, G. Effective prevention of microbial biofilm formation on medical devices by Low-Energy Surface Acoustic Waves. Antimicrob. Agents Chemother. 5, 4144-4152 (2006).
16. MacKintosh, E. E., Patel, J. D., Marchant, R. E. & Anderson, J. M. Effects of biomaterial surface chemistry on the adhesion and biofilm formation of Staphylococcus epidermidis in vitro. J. Biomed. Mater. Res. A 78, 836-842 (2006).
17. Korber, D. R., Lawrence, J. R., Sutton, B. & Caldwell, D. E. Effect of laminar flow velocity on the kinetics of surface recolonization by Mot+ and Mot-Pseudomonas fluorescens. Microb. Ecol. 18, 1-19 (1989).
18. Rosenberg, M., Bayer, E. A., Delarea, J. & Rosenberg, E. Role of thin fimbriae in adherence and growth of Acinetobacter calcoaceticus RAG-1 on hexadecane. Appl. Environ. Microbiol. 44, 929 (1982).
19. Donlan, R. M. Biofilms and device-associated infections. Emerg. Infect. Dis. 7, 277 (2001).
20. Donlan, R. M. Biofilm formation: a clinically relevant microbiological process. Clin. Infect. Dis. 33, 1387 (2001).
21. Picioreanu, C, van Loosdrecht, M. C. M. & Heijnen, J. J. Two-dimensional model of biofilm detachment caused by internal stress from liquid flow. Biotechnol. Bioeng. 72, 205-218 (2001).
22. Stoodley, P., Cargo, R., Rupp, C. J., Wilson, S. & Klapper, I. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J. Ind. Microbiol. Biotechnol. 29, 361-367 (2002).
23. Gilbert, P., Das, J. & Foley, I. Biofilms susceptibility to antimicrobials. Adv. Dent. Res. 11, 160-167 (1997).
24. Costerton, J., Stewart, P. & Greenberg, E. Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322 (1999).
25. Daly, B., Betts, W. B., Brown, A. P. & O'Neill, J. G. Bacterial loss from biofilms exposed to free chlorine. Microbios96, 7-21 (1998).
26. Lee, S. F., Li, Y. H. & Bowden, G. H. Detachment of Streptococcus mutans biofilm cells by an endogenous enzymatic activity. Infect. Immun. 64, 1035 (1996).
27. Ji, Y K. & Ling, J. Q. [Spatial distribution of dead and vital bacteria in the native dental biofilm]. Zhonghua Kou Qiang Yi Xue Za Zhi 42, 294 (2007).
28. Lewis, K. Persister cells and the riddle of biofilm survival. Biochemistry (Moscow) 70, 267-274 (2005).
29. Yarwood, J. M., Paquette, K. M., Tikh, I. B., Volper, E. M. & Greenberg, E. P. Generation of virulence factor variants in Staphylococcus aureus biofilms. J. Bacteriol. 189, 7961 (2007).
30. Boles, B. R., Thoendel, M. & Singh, P. K. Self-generated diversity produces 'insurance effects' in biofilm communities. Proc. Natl Acad. Sci. USA 101, 16630 (2004).
31. Allegrucci, M. & Sauer, K. Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J. Bacteriol. 189, 2030 (2007).
32. Handke, L. D., Conlon, K. M., Slater, S. R., Elbaruni, S., Fitzpatrick, F., Humphreys, H., Giles, W. P., Rupp, M. E., Fey, P. D. & O'Gara, J. P. Genetic and phenotypic analysis of biofilm phenotypic variation in multiple Staphylococcus epidermidis isolates. J. Med. Microbiol. 53, 367-374 (2004).
33. Hansen, S. K., Haagensen, J. A. J., Gjermansen, M., Jorgensen, T. M., Tolker-Nielsen, T. & M olin, S. C ha racterization of a Pseudomonas putida rough variant evolved in a mixed-species biofilm with Acinetobacter sp. strain C6. J. Bacteriol. 189, 4932-4943 (2007).
34. Vance, R. E., Zhu, J. & Mekalanos, J. J. A constitutively active variant of the quorum-sensing regulator LuxO affects protease production and biofilm formation in Vibrio cholerae. Infect. Immun. 71, 2571 (2003).
35. Grau, B. L., Henk, M. C. & Pettis, G. S. High-frequency phase variation of Vibrio vulnificus 1003: isolation and characterization of a rugose phenotypic variant. J. Bacteriol. 187, 2519 (2005).
36. Ingavale, S., Van Wamel, W., Luong, T. T., Lee, C. Y. & Cheung, A. L. Rat/MgrA, a regulator of autolysis, is a regulator of virulence genes in Staphylococcus aureus. Infect. Immun. 73, 1423 (2005).
37. Seidl, K., Muller, S., Francois, P., Kriebitzsch, C., Schrenzel, J., Engelmann, S., Bischoff, M. & Berger-Bachi, B. Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol. 9, 95-111 (2009).
38. Vuong, C. & Otto, M. Staphylococcus epidermidis infections. Microbes Infect. 4, 481-489 (2002).
39. Wang, L., Li, M., Dong, D., Bach, T. H., Sturdevant, D. E., Vuong, C., Otto, M. & Gao, Q. SarZ is a key regulator of biofilm formation and virulence in Staphylococcus epidermidis. J. Infect. Dis. 197, 1254-1262 (2008).
40. Rijavec, M., Müller-Premru, M., Zakotnik, B. & Zgur-Bertok, D. Virulence factors and biofilm production among Escherichia coli strains causing bacteraemia of urinary tract origin. J. Med. Microbiol. 57, 1329 (2008).
41. Parkins, M. D., Ceri, H. & Storey, D. G. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol. Microbiol. 40, 1215-1226 (2001).
42. Koo, H., Xiao, J. & Klein, M. I. Extracellular polysaccharides matrix-an often forgotten virulence factor in oral biofilm research. Int. J. Oral Sci. 1, 229-234 (2009).
43. Nield-Gehrig, J. S. Dental plaque biofilms. J. Pract. Hygiene 14, 16 (2005).
44. Pye, A. D., Lockhart, D. E. A., Dawson, M. P., Murray, C. A. & Smith, A. J. A review of dental implants and infection. J. Hosp. Infect. 72, 104-110 (2009).
45. Adell, R., Lekholm, U., Rockler, B. & Brånemark, P. A 15-year study of osseointe-grated previous term implants next term in the treatment of the edentulous jaw. Int. J. Oral Surg. 10, 387-416 (1981).
46. Renvert, S., Samuelsson, E., Lindahl, C. & Persson, G. Mechanical non surgical treatment of peri implantitis: a double blind randomized longitudinal clinical study. I: clinical results. J. Clin. Periodont. 36, 604-609 (2009).
47. Balaji, S. M. Textbook of Oral And Maxillofacial Surgery. 1 edn (Elsevier, India, 2007).
48. Saxton, C. Scanning electron microscopy study of the formation of dental plaque. Caries Res 19, 111-123 (1973).
49. Maximo, M. B., de Mendonca, A. C., Renata Santos, V., Figueiredo, L. C., Feres, M. & Duarte, P. M. Short term clinical and microbiological evaluations of peri implant diseases before and after mechanical anti infective therapies. Clin. Oral Implan. Res. 20, 99-108 (2009).
50. Rams, T. E. & Link, Jr C. C. Microbiology of failing dental implants in humans: electron microscopic observations. J. Oral Implantol. 11, 93 (1983).
51. Heimdahl, A., Köndell, P. A., Nord, C. E. & Nordenram, A. Effect of insertion of osseo-integrated prosthesis on the oral microflora. Swed. Dent. J. 7, 199 (1983).
52. Krekeler, G., Pelz, K. & Nelissen, R. Mikrobielle Besiedlung der Zahnfleischtaschen am künstlichen Titanpfeiler. Dtsch. Zahnarztl. Z 41, 569-572 (1986).
53. Mombelli, A., Oosten, M. A. C., Schürch, Jr E. & Lang, N. P. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Micro-biol. Immun. 2, 145-151 (1987).
54. Sanz, M., Newman, M. G., Nachnani, S., Holt, R., Stewart, R. & Flemmig, T. Characterization of the subgingival microbial flora around endosteal sapphire dental implants in partially edentulous patients. Int. J. Oral. Maxillofac. Implants 5, 247-253 (1990).
55. Becker, W., Becker, B. E., Newman, M. G. & Nyman, S. Clinical and microbiologic findings that may contribute to dental implant failure. Int J Oral Maxillofac Implants 5, 31 (1990).
56. Rams, T. E., Feik, D. & Slots, J. Staphylococci in human periodontal diseases. Oral Microbiol. Immun. 5, 29-32 (1990).
57. Augthun, M. & Conrads, G. Microbial findings of deep peri-implant bone defects. Int. J. Oral Maxillofac. Implants 12, 106 (1997).
58. Leonhardt, Å., Dahlén, G. & Renvert, S. Five-year clinical, microbiological, and radiological outcome following treatment of peri-implantitis in man. J. Periodont. 74, 1415-1422 (2003).
59. Mombelli, A. & Décaillet, F. The characteristics of biofilms in peri implant disease. J. Clin. Periodont. 38, 203-213 (2011).
60. Saginur, R., StDenis, M., Ferris, W., Aaron, S. D., Chan, F., Lee, C. & Ramotar, K. Multiple combination bactericidal testing of staphylococcal biofilms from implant-associated infections. Antimicrob. Agents Chemother. 50, 55-61 (2006).
61. Lauderdale, K. J., Malone, C. L., Boles, B. R., Morcuende, J. & Horswill, A. R. Biofilm dispersal of community associated methicillin resistant Staphylococcus aureus on orthopedic implant material. J. Orthopaed. Res. 28, 55-61 (2010).
62. Sia, I. G., Berbari, E. F. & Karchmer, A. W. Prosthetic joint infections. Infect. Dis. Clin. North Am. 19, 885-914 (2005).
63. Bengtson, S., Blomgren, G., Knutson, K., Wigren, A. & Lidgren, L. Hematogenous infection after knee arthroplasty. Acta. Orthop. Scand. 58, 529-534 (1987).
64. Geipel, U. Pathogenic organisms in hip joint infections. Int. J. Med. Sci. 6, 234 (2009).
65. Cuckler, J. M. The infected total knee: management options. J. Arthroplasty 20, 33-36 (2005).
66. Gristina, A. G., Jennings, R. A., Naylor, P. T., Myrvik, Q. N. & Webb, L. X. Comparative in vitro antibiotic resistance of surface-colonizing coagulase-negative staphylococci. Antimicrob. Agents Chemother. 33, 813 (1989).
67. Ha, K. Y., Chung, Y. G. & Ryoo, S. J. Adherence and biofilm formation of Staphylococcus epidermidis and Mycobacterium tuberculosis on various spinal implants. Spine 30, 38 (2005).
68. Lynch, A. S. & Robertson, G. T. Bacterial and fungal biofilm infections. Annu. Rev. Med. 59, 415-428 (2008).
69. Donlan, R. M. & Costerton, J. W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167 (2002).
70. Kokare, C. R., Chakraborty, S., Khopade, A. N. & Mahadik, K. R. Biofilm: Importance and applications. Indian J. Biotechnol. 8, 159-168 (2009).
71. Litzler, P. Y., Benard, L., Barbier-Frebourg, N., Vilain, S., Jouenne, T., Beucher, E., Bunel, C., Lemeland, J. F. & Bessou, J. P. Biofilm formation on pyrolytic carbon heart valves: influence of surface free energy, roughness, and bacterial species. J. Thorac. Cardiovas. Surg. 134, 1025-1032 (2007).
72. Calderwood, S. B., Swinski, L. A., Waternaux, C. M., Karchmer, A. W. & Buckley, M. J. Risk factors for the development of prosthetic valve endocarditis. Circulation 72, 31 (1985).
73. Grover, F. L., Cohen, D. J., Oprian, C., Henderson, W. G., Sethi, G. & Hammermeister, K. E. Determinants of the occurrence of and survival from prosthetic valve endocarditis: experience of the Veterans Affairs Cooperative Study on Valvular Heart Disease. J. Thorac. Cardiovas. Surg. 108, 207-214 (1994).
74. Baumgartner, W. A., Miller, D. C., Reitz, B. A., Oyer, P. E., Jamieson, S. W., Stinson, E. B. & Shumway, N. E. Surgical treatment of prosthetic valve endocarditis. Ann.Thorac. Surg. 35, 87-104 (1983).
75. Vongpatanasin, W., Hillis, L. D. & Lange, R. A. Prosthetic heart valves. N. Engl. J. Med. 335, 407-416 (1996).
76. Schmitt, D. D., Bandyk, D. F., Pequet, A. J. & Towne, J. B. Bacterial adherence to vascular prostheses. A determinant of graft infectivity. J. Vasc. Surg. 3, 732 (1986).
77. Bunt, T. J. Synthetic vascular graft infections. I. Graft infections. Surgery 93, 733 (1983).
78. Seeger, J. M. Management of patients with prosthetic vascular graft infection. Am.Surg. 66, 166-177 (2000).
79. Zetrenne, E., McIntosh, B. C., McRae, M. H., Gusberg, R., Evans, G. R. D. & Narayan, D. Prosthetic vascular graft infection: a multi-center review of surgical management. Yale J. Biol. Med. 80, 113-121 (2007).
80. Narasimhan, S., Aslam, S., Lin, P. H., Bechara, C. F., Mansouri, M. D. & Darouiche, R. O. Bacterial translocation across ePTFE vascular graft surfaces. J. Infect. 60, 486-490 (2010).
81. Venkatesan, N., Shroff, S., Jayachandran, K. & Doble, M. Polymers as ureteral stents. J. Endourol. 24, 191-198 (2010).
82. Reid, G., Denstedt, J. D., Kang, Y. S., Lam, D. & Nause, C. Microbial adhesion and biofilm formation on ureteral stents in vitro and in vivo. J. Urol. 148, 1592 (1992).
83. Riedl, C. R., Plas, E., Hubner, W. A., Zimmerl, H., Ulrich, W. & Pfluger, H. Bacterial colonization of ureteral stents. Eur. Urol. 36, 53-59 (2000).
84. Licht, M. R., Montague, D. K., Angermeier, K. W. & Lakin, M. M. Cultures from genitourinary prostheses at reoperation: questioning the role of Staphylococcus epidermidis in periprosthetic infection. J. Urol. 154, 387-390 (1995).
85. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R. & Lappin-Scott, H. M. Microbial biofilms. Annu. Rev. Microbiol. 49, 711-745 (1995).
86. Evans, B., Silverstein, A. D. & Donatucci, C. F. Biofilm formation on clinically noninfected penile prosthetic surfaces. Int. J. Impot. Res. 15, S162 (2003).
87. Garibaldi, R. A., Burke, J. P., Britt, M. R., Miller, W. A. & Smith, C. B. Meatal colonization and catheter-associated bacteriuria. N. Engl. J. Med. 303, 316-318 (1980).
88. Norden, C. W., Green, G. M. & Kass, E. H. Antibacterial mechanisms of the urinary bladder. J. Clin. Invest. 47, 2689 (1968).
89. Kucheria, R., Dasgupta, P., Sacks, S., Khan, M. & Sheerin, N. Urinary tract infections: new insights into a common problem. Postgrad. Med. J. 81, 83 (2005).
90. Maki, D. G. & Tambyah, P. A. Engineering out the risk for infection with urinary catheters. Emerg. Infect. Dis. 7, 342 (2001).
91. Collins, F. S. Cystic fibrosis: molecular biology and therapeutic implications. Science 256, 774-779 (1992).
92. Boyd, A. & Chakrabarty, A. M. Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J. Ind. Microbiol. 15, 162-168 (1995).
93. 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 monochlor-amine. J. Appl. Microbiol. 88, 546-553 (2000).
94. Dingman, J. R., Rayner, M. G., Mishra, S., Zhang, Y., Ehrlich, M. D., Post, J. C. & Ehrlich, G. D. Correlation between presence of viable bacteria and presence of endotoxin in middle-ear effusions. J. Clin. Microbiol. 36, 3417-3419 (1998).
95. Hall-Stoodley, L., Hu, F. Z., Gieseke, A., Nistico, L., Nguyen, D., Hayes, J., Forbes, M., Greenberg, D. P., Dice, B., Burrows, A., Wackym, P. A., Stoodley, P., Post, J. C., Ehrlich, G. D. & Kerschner, J. E. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. J. Am. Med. Assoc. 296, 202-211 (2006).
96. Lamont, R. J. & Jenkinson, H. F. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62, 1244 (1998).
97. Anderson, G. G., Palermo, J. J., Schilling, J. D., Roth, R., Heuser, J. & Hultgren, S. J. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301, 105-107 (2003).
98. Bayer, A. S., Bolger, A. F., Taubert, K. A., Wilson, W., Steckelberg, J., Karchmer, A. W., Levison, M., Chambers, H. F., Dajani, A. S., Gewitz, M. H., Newburger, J. W., Gerber, M. A., Shulman, S. T., Pallasch, T. J., Gage, T. W. & Ferrieri, P. Diagnosis and management of infective endocarditis and its complications. Circulation 98, 2936-2948 (1998).
99. Domingue, Sr G. J. & Hellstrom, W. J. G. Prostatitis. Clin. Microbiol. Rev. 11, 604 (1998).
100. Nishimura, S., Tsurumoto, T., Yonekura, A., Adachi, K. & Shindo, H. Antimicrobial susceptibility of Staphylococcus aureus and Staphylococcus epidermidis biofilms isolated from infected total hip arthroplasty cases. J. Orthop. Sci. 11, 46-50 (2006).
101. Ceri, H., Olson, M. E., Stremick, C., Read, R. R., Morck, D. & Buret, A. The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 37, 1771-1776 (1999).
102. Williams, I., Venables, W. A., Lloyd, D., Paul, F. & Critchley, I. The effects of adherence to silicone surfaces on antibiotic susceptibility in Staphylococcus aureus. Microbiology 143, 2407 (1997).
103. Hoyle, B. D., Wong, C. K. W. & Costerton, J. W. Disparate efficacy of tobramycin on Ca2 +-, Mg2+-, and HEPES-treated Pseudomonas aeruginosa biofilms. Can. J. Microbiol. 38, 1214-1218 (1992).
104. Duguid, I. G., Evans, E., Brown, M. R. W. & Gilbert, P. Effect of biofilm culture upon the susceptibility of Staphylococcus epidermidis to tobramycin. J. Antimicrob. Chemother. 30, 803 (1992).
105. Tresse, O., Jouenne, T. & Junter, G. A. The role of oxygen limitation in the resistance of agar-entrapped, sessile-like Escherichia coli to aminoglycoside and-lactam antibiotics. J. Antimicrob. Chemother 36, 521 (1995).
106. Duguid, I. G., Evans, E., Brown, M. R. W. & Gilbert, P. Growth-rate-independent killing by ciprofloxacin of biofilm-derived Staphylococcus epidermidis evidence for cell-cycle dependency. J. Antimicrob. Chemother. 30, 791 (1992).
107. Christensen, B. B., Sternberg, C., Andersen, J. B., Eberl, L., Moller, S., Givskov, M. & Molin, S. Establishment of new genetic traits in a microbial biofilm community. Appl. Environ. Microbiol. 64, 2247-2255 (1998).
108. Sutherland, I. W. The biofilm matrix-an immobilized but dynamic microbial environment. Trends Micorbiol. 9, 222-227 (2001).
109. Ghigo, J. M. Natural conjugative plasmids induce bacterial biofilm development. Nature 412, 442-445 (2001).
110. Ehlers, L. J. & Bouwer, E. J. RP4 plasmid transfer among species of Pseudomonas in a biofilm reactor. Water Sci. Technol. 39, 163-171 (1999).
111. Chen, L. & Wen, Y. The role of bacterial biofilm in persistent infections and control strategies. Int. J. Oral Sci. 3, 66 (2011).
112. Nobbs, A. H., Lamont, R. J. & Jenkinson, H. F. Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 73, 407 (2009).
113. Tojo, M., Yamashita, N., Goldmann, D. A. & Pier, G. B. Isolation and characterization of a capsular polysaccharide adhesin from Staphylococcus epidermidis. J. Infect. Dis. 157, 713 (1988).
114. Zhang, Y. Q., Ren, S. X., Li, H. L., Wang, Y. X., Fu, G., Yang, J., Qin, Z. Q., Miao, Y. G., Wang, W. Y., Chen, R. S., Shen, Y., Chen, Z., Yuan, Z. H., Zhao, G. P., Qu, D., Danchin, A. & Wen, Y. M. Genome based analysis of virulence genes in a non biofilm forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol. 49, 1577-1593 (2003).
115. Russell, M. W., Bergmeier, L. A., Zanders, E. D. & Lehner, T. Protein antigens of Streptococcus mutans: purification and properties of a double antigen and its protease-resistant component. Infect. Immun. 28, 486 (1980).
116. Banas, J. A. & Vickerman, M. M. Glucan-binding proteins of the oral streptococci. Crit. Rev. Oral Biol. Med. 14, 89 (2003).
117. Kolenbrander, P. E., Ganeshkumar, N., Cassels, F. J. & Hughes, C. V. Coaggregation: specific adherence among human oral plaque bacteria. FA S E B J 7, 406-413 (1993).
118. Sanchez, C. J., Shivshankar, P., Stol, K., Trakhtenbroit, S., Sullam, P. M., Sauer, K., Hermans, P. W. M. & Orihuela, C. J. The pneumococcal serine-rich repeat protein is an intra-species bacterial adhesin that promotes bacterial aggregation in vivo and in biofilms. PLoS Pathog. 6, e1001044 (2010).
119. Krämer, R. & Jung, K. in Bacterial Signaling (eds Heilmann, C. & Götz, F.) 7-22 (Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, 2010).
120. Hall-Stoodley, L., Nistico, L., Sambanthamoorthy, K., Dice, B., Nguyen, D., Mershon, W. J., Johnson, C., Hu, F. Z., Stoodley, P., Ehrlich, G. D. & Post, J. C. Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule down regulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol. 8, 173 (2008).
121. Allesen Holm, M., Barken, K. B., Yang, L., Klausen, M., Webb, J. S., Kjelleberg, S., Molin, S., Givskov, M. & Tolker-Nielsen, T. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59, 1114-1128 (2006).
122. Thomas, V. C., Thurlow, L. R., Boyle, D. & Hancock, L. E. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J. Bacteriol. 190, 5690 (2008).
123. Rice, K. C., Mann, E. E., Endres, J. L., Weiss, E. C., Cassat, J. E., Smeltzer, M. S. & Bayles, K. W. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 104, 8113-8118 (2007).
124. Waters, C. M. & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319-346 (2005).
125. Eberi, L. N-acyl homoserinelactone-mediated gene regulation in gram-negative bacteria. Syst. Appl. Microbiol. 22, 493-506 (1999).
126. Miller, M. B. & Bassler, B. L. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165-199 (2001).
127. Chu, F., Kearns, D. B., McLoon, A., Chai, Y., Kolter, R. & Losick, R. A novel regulatory protein governing biofilm formation in Bacillus subtilis. Mol. Microbiol. 68, 1117-1127 (2008).
128. 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. 20, 1083-1091 (1996).
129. Rupp, M. E., Ulphani, J. S., Fey, P. D. & Mack, D. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect. Immun. 67, 2656 (1999).
130. Kristian, S. A., Golda, T., Ferracin, F., Cramton, S. E., Neumeister, B., Peschel, A., Gotz, F. & Landmann, R. The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microb. Pathogenesis 36, 237-245 (2004).
131. Ziebuhr, W., Heilmann, C., Gotz, F., Meyer, P., Wilms, K., Straube, E. & Hacker, J. Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect. Immun. 65, 890-896 (1997).
132. Vuong, C., Gotz, F. & Otto, M. Construction and characterization of an agr deletion mutant of Staphylococcus epidermidis. Infect. Immun. 68, 1048 (2000).
133. Vuong, C., Saenz, H. L., Götz, F. & Otto, M. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182, 1688 (2000).
134. Vuong, C., Kocianova, S., Yao, Y., Carmody, A. B. & Otto, M. Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermi-dis in vivo. J. Infect. Dis. 190, 1498 (2004).
135. Williams, R. J. & Govan, J. R. W. Pyocine syping of mucoid strains of Pseudomonas aeruginosa isolated from children with cystic fibrosis. J. Med. Microbiol. 6, 409-412 (1973).
136. Ogle, J. W., Janda, J. M., Woods, D. E. & Vasil, M. L. Characterization and use of a DNA probe as an epidemiological marker for Pseudomonas aeruginosa. J. Infect. Dis. 155, 119 (1987).
137. Mack, D. Molecular mechanisms of Staphylococcus epidermidis biofilm formation. J. Hosp. Infect. 43, S113-S125 (1999).
138. McCann, M. T., Gilmore, B. F. & Gorman, S. P. Staphylococcus epidermidis device related infections: pathogenesis and clinical management. J. Pharm. Pharmacol. 60, 1551-1571 (2008).
139. Caiazza, N. C., Merritt, J. H., Brothers, K. M. & O'Toole, G. A. Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189, 3603 (2007).
140. Tabak, M., Scher, K., Hartog, E., Romling, U., Matthews, K. R., Chikindas, M. L. & Yaron, S. Effect of triclosan on Salmonella typhimurium at different growth stages and in biofilms. FEMS Microbiol. Lett. 267, 200-206 (2007).
141. Herrmann, M., Vaudaux, P. E., Pittet, D., Auckenthaler, R., Lew, P. D., Schumacher-Perdreau, F., Peters, G. & Waldvogel, F. A. Fibronectin, fibrinogen, and laminin act as mediators of adherence of clinical Staphylococcal isolates to foreign material. J. Infect. Dis. 158, 693-701 (1988).
142. McGavin, M. H., Krajewska-Pietrasik, D., Ryden, C. & Hook, M. Identification of a Staphylococcus aureus extracellular matrix-binding protein with broad specificity. Infect. Immun. 61, 2479 (1993).
143. Eberhard, J., Menzel, N., Dommisch, H., Winter, J., Jepsen, S. & Mutters, R. The stage of native biofilm formation determines the gene expression of human defensin 2, psoriasin, ribonuclease 7 and inflammatory mediators: a novel approach for stimulation of keratinocytes with in situ formed biofilms. Oral Microbiol. Immun. 23, 21-28 (2008).
144. Cierny Iii, G. & DiPasquale, D. Periprosthetic total joint infections: staging, treatment, and outcomes. Clin. Orthop. Relat. Res. 403, 23 (2002).
145. McPherson, E. J., Woodson, C., Holtom, P., Roidis, N., Shufelt, C. & Patzakis, M. Periprosthetic total hip infection: outcomes using a staging system. Clin. Orthop. Relat. Res. 403, 8-15 (2002).
146. Kehinde, E. O., Rotimi, V. O., Al-Awadi, K. A., Abdul-Halim, H., Boland, F., Al-Hunayan, A. & Pazhoor, A. Factors predisposing to urinary tract infection after J ureteral stent insertion. J. Urol. 167, 1334-1337 (2002).
147. Quirynen, M., Brecx, M. & Steenberghe, V. D. Biofilms in the Oral Cavity: Impact of Surface Characteristics 167-187 (Harwood Academic Publishers, Amsterdam, 2000).
148. Subramani, K., Jung, R. E., Molenberg, A. & Hammerle, C. H. Biofilm on dental implants: a review of the literature. Int. J. Oral. Maxillofac. Implants 24, 616 (2009).
149. Ramage, G., Tunney, M. M., Patrick, S., Gorman, S. P. & Nixon, J. R. Formation of Propionibacterium acnes biofilms on orthopaedic biomaterials and their susceptibility to antimicrobials. Biomaterials 24, 3221-3227 (2003).
150. Teughels, W., Van Assche, N., Sliepen, I. & Quirynen, M. Effect of material characteristics and/or surface topography on biofilm development. Clin. Oral Implan. Res 17, 68-81 (2006).
151. Medilanski, E., Kaufmann, K., Wick, L. Y., Wanner, O. & Harms, H. Influence of the surface topography of stainless steel on bacterial adhesion. Biofouling 18, 193-203 (2002).
152. Carlen, A., Nikdel, K., Wennerberg, A., Holmberg, K. & Olsson, J. Surface characteristics and in vitro biofilm formation on glass ionomer and composite resin. Biomaterials 22, 481-487 (2001).
153. Allion, A., Baron, J. P. & Boulange-Petermann, L. Impact of surface energy and roughness on cell distribution and viability. Biofouling 22, 269-278 (2006).
154. Emery, B. E., Dixit, R., Formby, C. C. & Biedlingmaier, J. F. The resistance of maxillofacial reconstruction plates to biofilm formation in vitro. Laryngoscope 113, 1977-1982 (2003).
155. Absolom, D. R., Lamberti, F. V., Policova, Z., Zingg, W., Van Oss, C. J. & Neumann, A. W. Surface thermodynamics of bacterial adhesion. Appl. Environ. Microbiol. 46, 90-97 (1983).
156. Reid, G., Hawthorn, L. A., Mandatori, R., Cook, R. L. & Beg, H. S. Adhesion of lactobacilli to polymer surfaces in vivo and in vitro. Microb. Ecol. 16, 241-251 (1988).
157. Reid, G., Lam, D., Policova, Z. & Neumann, A. W. Adhesion of two uropathogens to silicone and lubricious catheters: influence of pH, urea and creatinine. J. Mater. Sci. Mater. Med 4, 17-22 (1993).
158. Pasmore, M., Todd, P., Smith, S., Baker, D., Silverstein, J., Coons, D. & Bowman, C. N. Effects of ultrafiltration membrane surface properties on Pseudomonas aeruginosa biofilm initiation for the purpose of reducing biofouling. J. Membr. Sci. 194, 15-32 (2001).
159. Razatos, A., Ong, Y. L., Sharma, M. M. & Georgiou, G. Molecular determinants of bacterial adhesion monitored by atomic force microscopy. Proc. Natl. Acad. Sci. 95, 11059 (1998).
160. Naylor, P. T., Myrvik, Q. N. & Gristina, A. Antibiotic resistance of biomaterial-adherent coagulase-negative and coagulase-positive staphylococci. Clin. Orthop. Relat. Res. 261, 126 (1990).
161. Webb, L. X., Holman, J., de Araujo, B., Zaccaro, D. J. & Gordon, E. S. Antibiotic resistance in staphylococci adherent to cortical bone. J. Orthop. Trauma 8, 28 (1994).
162. Hallab, N., Bundy, K., O'Coonor, K., Clark, R. & Moses, R. Surface charge, biofilm composition and cellular morphology as related to cellular adhesion to biomaterials. Proceedings of the 1995 Fourteenth Southern Biomedical Engineering Conference, pp 81-84.
163. Subbiahdoss, G., Kuijer, R., Busscher, H. J. & van der Mei, H. C. Mammalian cell growth versus biofilm formation on biomaterial surfaces in an in vitro post-operative contamination model. Microbiology 156, 3073 (2010).
164. Gottenbos, B., Grijpma, D. W., Van Der Mei, H. C., Feijen, J. & Busscher, H. J. Antimicrobial effects of positively charged surfaces on adhering Gram-positive and Gram-negative bacteria. J. Antimicrob. Chemother. 48, 7 (2001).
165. Nguyen, L. L., Nelson, C. L., Saccente, M., Smeltzer, M. S., Wassell, D. L. & McLaren, S. G. Detecting bacterial colonization of implanted orthopaedic devices by ultrasonication. Clin. Orthop. Relat. Res 403, 29-37 (2002).
166. Ince, A., Rupp, J., Frommelt, L., Katzer, A., Gille, J. & Lohr, J. F. Is 'Aseptic' Loosening of the Prosthetic Cup after Total Hip Replacement Due to Nonculturable Bacterial Pathogens in Patients with Low-Grade Infection? Clin. Infect. Dis 39, 1599-1603 (2004).
167. Stoodley, P., Kathju, S., Hu, F. Z., Erdos, G., Levenson, J. E., Mehta, N., Dice, B., Johnson, S., Hall-Stoodley, L., Nistico, L., Sotereanos, N., Sewecke, J., Post, J. C. & Ehrlich, G. D. Molecular and imaging techniques for bacterial biofilms in joint arthroplasty infections. Clin. Orthop. Relat. Res 437, 31-40 (2005).
168. Sampedro, M. F., Huddleston, P. M., Piper, K. E., Karau, M. J., Dekutoski, M. B., Yaszemski, M. J., Currier, B. L., Mandrekar, J. N., Osmon, D. R., McDowell, A, Patrick, S, Steckelberg, J. M. & Patel, R A biofilm approach to detect bacteria on removed spinal implants. Spine 35, 1218-1224 (2010).
169. Piper, K. E., Sampedro, M. F., Steckelberg, K. E., Mandrekar, J. N., Karau, M. J, Steckelberg, J. M., Berbari, E. F., Osmon, D. R., Hanssen, A. D., Lewallen, D. G., Cofield, R. H., Sperling, J. W., Sotelo, J. S., Huddleston, P. M., Dekutoski, M. B., Yaszemski, M., Currier, B. & Patel, R. C-reactive protein, erythrocyte sedimentation rate and orthopedic implant infection. PLoS One 5, e9358 (2010).
170. Panda, R. K., Malaviya, A. N., Sampathkumar, A., Iyer, K. S., Das, B., Sharma, M. L. & Venugopal, P. Serial estimation of C-reactive protein following cardiac surgery. Indian J. Thorac. Cardiovas. Surg. 5, 18-23 (1987).
171. Bottner, F., Wegner, A., Winkelmann, W., Becker, K., Erren, M. & Gotze, C. Interleukin-6, procalcitonin and TNF-{alpha}: markers of peri-prosthetic infection following total joint replacement. J. Bone Joint Surg. Br 89, 94-99 (2007).
172. Schiesser, M., Stumpe, K. D. M., Trentz, O., Kossmann, T. & von Schulthess, G. K. Detection of Metallic Implant-associated Infections with FDG PET in Patients with Trauma: Correlation with Microbiologic Results1. Radiology 226, 391 (2003).
173. Meffert, R. M. Maintenance and treatment of the ailing and failing implant. J. Indiana Dent. Assoc. 73, 22 (1994).
174. Jovanovic, S. A. The management of peri-implant breakdown around functioning osseointegrated dental implants. J. Periodont. 64, 1176 (1993).
175. Shirtliff, M. & Leid, J. in Biofilm Formation on Natural Teeth and Dental Implants: What is the Difference? Vol. 3 (eds. Armellini, D., Reynolds, M. A., Harro, J. M. & Molly, L.) 109-122 (Springer, Maryland, 2009).
176. Falahee, M. H., Matthews, L. S. & Kaufer, H. Resection arthroplasty as a salvage procedure for a knee with infection after a total arthroplasty. J. Bone Joint Surg. Am 69, 1013 (1987).
177. Tsukayama, D. T., Estrada, R. & Gustilo, R. B. Infection after total hip arthroplasty: a study of the treatment of one hundred and six infections. J. Bone Joint Surg. Am. 78, 512-523 (1996).
178. Hanssen, A. D., Rand, J. A. & Osmon, D. R. Treatment of the infected total knee arthroplasty with insertion of another prosthesis: the effect of antibiotic-impregnated bone cement. Clin. Orthop. Relat. Res. 309, 44 (1994).
179. Duncan, C. P. & Beauchamp, C. A temporary antibiotic-loaded joint replacement system for management of complex infections involving the hip. Orthop. Clin. North. Am. 24, 751 (1993).
180. Masri, B. A., Duncan, C. P. & Beauchamp, C.P. Long-term elution of antibiotics from bone-cement: an in vivo study using the prosthesis of antibiotic-loaded acrylic cement (PROSTALAC) system. J. Arthroplasty 13, 331-338 (1998).
181. Trebse, R., Pisot, V. & Trampuz, A. Treatment of infected retained implants. J. Bone Joint Surg. Br. 87, 249 (2005).
182. Bergamini, T. M., Peyton, J. C. & Cheadle, W. G. Prophylactic antibiotics prevent bacterial biofilm graft infection. J. Surg. Res. 52, 101-105 (1992).
183. Kwaan, J. H. M. & Connolly, J. E. Successful management of prosthetic graft infection with continuous povidone-iodine irrigation. Arch. Surg. 116, 716 (1981).
184. Kehinde, E. O., Rotimi, V. O., Al-Hunayan, A., Abdul-Halim, H., Boland, F. & Al-Awadi, K. A. Bacteriology of urinary tract infection associated with indwelling J ureteral stents. J. Endourol. 18, 891-896 (2004).
185. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L. & Leibler, S. Bacterial persistence as a phenotypic switch. Science 305, 1622 (2004).
186. Brackman, G., Hillaert, U., Van Calenbergh, S., Nelis, H. J. & Coenye, T. Use of quorum sensing inhibitors to interfere with biofilm formation and development in Burkholderia multivorans and Burkholderia cenocepacia. Res. Microbiol. 160, 144-151 (2009).
187. Kociolek, M. G. Quorum-sensing inhibitors and biofilms. Curr. Med. Chem.: AntiInfect. Agents 8, 315-326 (2009).
188. Givskov, M., de Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P. D. & Kjelleberg, S. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178, 6618-6622 (1996).
189. Eberl, L., Christiansen, G., Molin, S. & Givskov, M. Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon. J. Bacteriol. 178, 554 (1996).
190. Rasmussen, T. B., Manefield, M., Andersen, J. B., Eberl, L., Anthoni, U., Christo-phersen, C., Steinberg, P., Kjelleberg, S. & Givskov, M. How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 146, 3237-3244 (2000).
191. Persson, T., Hansen, T. H., Rasmussen, T. B., Skinderso, M. E., Givskov, M. & Nielsen, J. Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org. Biomol. Chem. 3, 253-262 (2004).
192. Reverchon, S., Chantegrel, B., Deshayes, C., Doutheau, A. & Cotte-Pattat, N. New synthetic analogues of N-acyl homoserine lactones as agonists or antagonists of transcriptional regulators involved in bacterial quorum sensing. Bioorg. Medicinal Chem. Lett. 12, 1153-1157 (2002).
193. Darouiche, R. O. Device-associated infections: a macroproblem that starts with microadherence. Clin. Infect. Dis. 33, 1567-1572 (2001).
194. Reid, G. Applications from bacterial adhesion and biofilm studies in relation to urogenital tissues and biomaterials: a review. J. Ind. Microbiol. Biotechnol. 13, 90-96 (1994).
195. Wizemann, T. M., Adamou, J. E. & Langermann, S. Adhesins as targets for vaccine development. Emerg. Infect. Dis. 5, 395 (1999).
196. Palaszynski, S., Pinkner, J., Leath, S., Barren, P, Auguste, C. G., Burlein, J., Hultgren, S. & Langermann, S. Systemic immunization with conserved pilus-associated adhesins protects against mucosal infections. Dev. Biol. Stand. 92, 117-122 (1998).
197. Chung, K. K., Schumacher, J. F., Sampson, E. M., Burne, R. A., Antonelli, P.J. & Brennan, A. B. Impact of engineered surface microtopography on biofilm formation of Staphylococcus aureus. Biointerphases 2, 89-94 (2007).
198. Hetrick, E. M. & Schoenfisch, M. H. Reducing implant-related infections: active release strategies. Chem. Soc. Rev. 35, 780-789 (2006).
199. Charville, G. W., Hetrick, E. M., Geer, C. B. & Schoenfisch, M. H. Reduced bacterial adhesion to fibrinogen-coated substrates via nitric oxide release. Biomaterials 29, 4039-4044 (2008).
200. Ovaska, M., Lindahl, J., Makinen, T., Madanat, R., Pulliainen, L., Kiljunen, V., Hirvensalo, E. & Tukiainen, E. [Postoperative infection-removal of screws and plates?]. Suomen Ortopedia ja Traumatologia 4, 34-36 (2011).
201. Hawthorn, L. A. & Reid, G Exclusion of uropathogen adhesion to polymer surfaces by Lactobacillus acidophilus. J. Biomed. Mater. Res. 24, 39-46 (1990).
202. Darouiche, R. O., Donovan, W. H., Del Terzo, M., Thornby, J. I., Rudy, D. C. & Hull, R. A. Pilot trial of bacterial interference for preventing urinary tract infection. Urology 58, 339-344 (2001).
203. Yoshinari, M., Kato, T., Matsuzaka, K., Hayakawa, T. & Shiba, K. Prevention of biofilm formation on titanium surfaces modified with conjugated molecules comprised of antimicrobial and titanium-binding peptides. Biofouling 26, 103-110 (2009).
204. Curtin, J. J. & Donlan, R. M. Using bacteriophages to reduce formation of catheter-associated biofilms by Staphylococcus epidermidis. Antimicrob. Agents Chemother. 50, 1268 (2006).
205. DiTizio, V., Ferguson, G. W., Mittelman, M. W., Khoury, A. E., Bruce, A. W. & DiCosmo, F. A liposomal hydrogel for the prevention of bacterial adhesion to catheters. Biomaterials 19, 1877-1884 (1998).
206. Taylor, E. N. & Webster, T. J. The use of superparamagnetic nanoparticles for prosthetic biofilm prevention. Int. J. Nanomed 4, 145 (2009).
207. Rittmann, B. E. & McCarty, P. L. Model of steady state biofilm kinetics. Biotechnol. Bioeng. 22, 2343-2357 (1980).
208. Wanner, O. & Gujer, W. A multispecies biofilm model. Biotechnol. Bioeng. 28, 314-328 (1986).
209. Cogan, N. G. & Keener, J. P. The role of the biofilm matrix in structural development. Math. Med. Biol. 21, 147 (2004).
210. Eberl, H. J. & Collinson, S. Theoretical biology and medical modelling. Theor. Biol. Med. Model 6, 30 (2009).
211. Kreft, J. U. & Wimpenny, J. W. T. Effect of EPS on biofilm structure and function as revealed by an individual-based model of biofilm growth. Water Sci. Technol 43, 135-142 (2001).
212. Eberl, H. J., Khassehkhan, H. & Demaret, L. A mixed-culture model of a probiotic biofilm control system. Comput. Math. Met. Med. 11, 99-118 (2010).
213. Klapper, I., Rupp, C. J., Cargo, R., Purvedorj, B. & Stoodley, P. Viscoelastic fluid description of bacterial biofilm material properties. Biotechnol. Bioeng. 80, 289-296 (2002).
214. Elliott, T. S. J., Moss, H. A., Tebbs, S. E., Wilson, I. C., Bonser, R. S., Graham, T. R., Burke, L. P. & Faroqui, M. H. Novel approach to investigate a source of microbial contamination of central venous catheters. Eur. J. Clin. Microbiol. Infect. Dis. 16, 210-213 (1997).
215. Guo, B., Zhao, X., Shi, Y., Zhu, D. & Zhang, Y. Pathogenic implication of a fibrinogen-binding protein of Staphylococcus epidermidis in a rat model of intravascular-catheter-associated infection. Infect. Immun. 75, 2991 (2007).
216. Schwab, S. J. & Beathard, G. The hemodialysis catheter conundrum: Hate living with them, but can't live without them. Kidney Int. 56, 1-17 (1999).
217. Rello, J., Coll, P., Net, A. & Prats, G. Infection of pulmonary artery catheters. Epidemiologic characteristics and multivariate analysis of risk factors. Chest 103, 132 (1993).
218. Bonner, M. C., Tunney, M. M., Jones, D. S. & Gorman, S. P. Factors affecting in vitro adherence of ureteral stent biofilm isolates to polyurethane. Int. J. Pharm. 151, 201-207 (1997).
219. Read, R. R., Eberwein, P., Dasgupta, M. K., Grant, S. K., Lam, K., Nickel, J. C. & Costerton, J. W. Peritonitis in peritoneal dialysis: bacterial colonization by biofilm spread along the catheter surface. Kidney Int. 35, 614-621 (1989).
220. Hurrell, E., Kucerova, E., Loughlin, M., Caubilla-Barron, J. & Forsythe, S. J. Biofilm formation on enteral feeding tubes by Cronobacter sakazakii, Salmonella serovars and other Enterobacteriaceae. Int. J. Food Microbiol. 136, 227-231 (2009).
221. DeLegge, R. L. & DeLegge, M. H. Percutaneous endoscopic gastrostomy evaluation of device materials: are we 'Failsafe'? Nutr. Clin. Pract. 20, 613 (2005).
222. O'May, G. A., Reynolds, N., Smith, A. R., Kennedy, A. & Macfarlane, G. T. Effect of pH and antibiotics on microbial overgrowth in the stomachs and duodena of patients undergoing percutaneous endoscopic gastrostomy feeding. J. Clin. Microbiol. 43, 3059 (2005).
223. Lai, H. C., Juang, S. E., Liu, T. J. & Ho, W. M. Fires of endotracheal tubes of three different materials during carbon dioxide laser surgery. Acta. Anaesthesiol. Sin. 40, 47 (2002).
224. Perkins, S. D., Woeltje, K. F. & Angenent, L. T. Endotracheal tube biofilm inoculation of oral flora and subsequent colonization of opportunistic pathogens. Int. J. Med. Microbiol. 300, 503-511 (2010).
225. Bjorling, G., Axelsson, S., Johansson, U. B., Lysdahl, M., Markstrom, A., Schedin, U., Aune, R. E., Frostell, C. & Karlsson, S. Clinical use and material wear of polymeric tracheostomy tubes. Laryngoscope 117, 1552-1559 (2007).
226. Meslemani, D., Yaremchuk, K. & Rontal, M. Presence of biofilm on adult tracheost-omy tubes. Ear Nose Throat J. 89, 496 (2010).
227. Barker-Davies, R. M., Freeman, B. J. C., Bayston, R. & Ashraf, W. Spinal implant materials: attachment and biofilm production by propionibacterium acnes and subsequent effect of exposure to antibiotics. J. Bone Joint Surg. Br. Proc. 88, 391 (2006).
228. Rajpurkar, A., Shah, R., Starkman, J. & Dhabuwala, C. B. Tissue ingrowth in penile implants and its effect on repeat penile surgery. Int. J. Impot. Res. 16, 203-206 (2004).
229. Silverstein, A. D., Henry, G. D., Evans, B., Pasmore, M., Simmons, C. J. & Donatucci, C. F. Biofilm formation on clinically non infected penile prostheses. J. Urol. 176, 1008-1011 (2006).
230. Dunn, K. W., Hall, P. N. & Khoo, C. T. K. Breast implant materials: sense and safety. Brit. J. Plast. Surg. 45, 315-321 (1992).
231. Netscher, D. T., Weizer, G., Wigoda, P., Walker, L. E., Thornby, J. & Bowen, D. Clinical relevance of positive breast periprosthetic cultures without overt infection. Plast. Reconstr. Surg. 96, 1125-1129 (1995).
232. Bono, J. V. & Scott, R. D. Revision Total Knee Arthroplasty (Springer Verlag, New York, 2005).
233. Sokoloff, L. The Joints and Synovial Fluid (Academic Press, New York, 1978).
234. Al-Maiyah, M., Hill, D., Bajwa, A., Slater, S., Patil, P., Port, A. & Gregg, P. J. Bacterial contaminants and antibiotic prophylaxis in total hip arthroplasty. J. Bone Joint Surg. Br 87, 1256-1258 (2005).
235. Zembic, A., Sailer, I., Jung, R. E. & Hämmerle, C. H. F. Randomized controlled clinical trial of customized zirconia and titanium implant abutments for single tooth implants in canine and posterior regions: 3 year results. Clin. Oral Implan. Res 20, 802-808 (2009).
236. Elter, C., Heuer, W., Demling, A., Hannig, M., Heidenblut, T. & Stiesch, M. Comparative analysis of biofilm formation on dental implant abutments with respect to supra-and subgingival areas: polytetrafluoroethylene versus titanium. Int. J. Prosthodont. 24, 373-375 (2011).
237. Gil, F. J., Aparicio, C., Manero, J. M. & Padrós, A. Influence of the height of the external hexagon and surface treatment on fatigue life of commercially pure titanium dental implants. Int J Oral Maxillofac Implants 24, 583 (2009).
238. Agostinho, A., James, G., Wazni, O., Citron, M. & Wilkoff, B. D. Inhibition of Staphylococcus aureus biofilms by a novel antibacterial envelope for use with implantable cardiac devices. Clin. Transl. Sci. 2, 193-198 (2009).
239. Yu, J. L., Andersson, R. & Ljungh, A. Protein adsorption and bacterial adhesion to biliary stent materials. J. Surg. Res. 62, 69-73 (1996).
240. Pruthi, V., Al-Janabi, A. & Pereira, B. J. Characterization of biofilm formed on intrauterine devices. Indian J. Med. Microbiol. 21, 161 (2003).
241. Nair, K., Muraleedharan, C. V. & Bhuvaneshwar, G. S. Developments in mechanical heart valve prosthesis. Sadhana 28, 575-587 (2003).
242. Park, J. B. & Bronzino, J. D. in Metallic Biomaterials (eds Park, J. B. & Kim, Y. K.) (CRC Press, Boca Raton, 2003).
243. Ratner, B. D., Hoffman, A. S., Schoen, F. J. & Lemons, J. E in Metals (ed. Brunski, J. B.) 137-153 (Elsevier Academic Press, San Diego, 2004).
244. Mani, G., Feldman, M. D., Patel, D. & Agrawal, C. Coronary stents: a materials perspective. Biomaterials 28, 1689-1710 (2007).
245. Shimizu, K., Kobayakawa, S., Tsuji, A. & Tochikubo, T. Biofilm formation on hydrophilic intraocular lens material. Curr. Eye Res. 31, 989-997 (2006).
246. Okajima, Y., Kobayakawa, S., Tsuji, A. & Tochikubo, T. Biofilm formation by Staphylococcus epidermidis on intraocular lens material. Invest. Ophthalmol. Vis. Sci. 47, 2971 (2006).
247. Bayston, R., Vera, L. & Ashraf, W. Activity of an Antimicrobial Hydrocephalus Shunt Catheter against Propionibacterium acnes. Antimicrob. Agents Chemother. 54, 5082 (2010).
248. Kettle, C. & Johanson, R. B. Absorbable synthetic versus catgut suture material for perineal repair. Cochrane Database Syst. Rev. 2, CD000006 (2000).
249. Henry-Stanley, M. J., Hess, D. J., Barnes, A. M. T., Dunny, G. M. & Wells, C. L. Bacterial Contamination of Surgical Suture Resembles a Biofilm. Surg. Infect. 11, 433-439 (2010).
250. Kathju, S., Nistico, L., Hall-Stoodley, L., Post, J. C., Ehrlich, G. D. & Stoodley, P. Chronic surgical site infection due to suture-associated polymicrobial biofilm. Surg. Infect. 10, 457-461 (2009).