Infection of orthopedic implants with emphasis on bacterial adhesion process and techniques used in studying bacterial-material interactions

Marta Ribeiro, Fernando J Monteiro, Maria P Ferraz, Marta Ribeiro, Fernando J Monteiro, Maria P Ferraz

Abstract

Staphylococcus comprises up to two-thirds of all pathogens in orthopedic implant infections and they are the principal causative agents of two major types of infection affecting bone: septic arthritis and osteomyelitis, which involve the inflammatory destruction of joint and bone. Bacterial adhesion is the first and most important step in implant infection. It is a complex process influenced by environmental factors, bacterial properties, material surface properties and by the presence of serum or tissue proteins. Properties of the substrate, such as chemical composition of the material, surface charge, hydrophobicity, surface roughness and the presence of specific proteins at the surface, are all thought to be important in the initial cell attachment process. The biofilm mode of growth of infecting bacteria on an implant surface protects the organisms from the host immune system and antibiotic therapy. The research for novel therapeutic strategies is incited by the emergence of antibiotic-resistant bacteria. This work will provide an overview of the mechanisms and factors involved in bacterial adhesion, the techniques that are currently being used studying bacterial-material interactions as well as provide insight into future directions in the field.

Keywords: Orthopedic implants; Staphylococcus; bacteria-material interactions; bacterial adhesion; bone infections.

References

    1. Navarro M, Michiardi A, Castaño O, Planell JÁ. Biomaterials in orthopaedics. J R Soc Interface. 2008;5:1137–58. doi: 10.1098/rsif.2008.0151.
    1. Smith KR, Hunt TR, Asher MA, Anderson HC, Carson WL, Robinson RG. The effect of a stiff spinal implant on the bone-mineral content of the lumbar spine in dogs. J Bone Joint Surg Am. 1991;73:115–23.
    1. Paital SR, Dahotre NB. Calcium phosphate coatings for bio-implant applications: Materials, performance factors, and methodologies. Mater Sci Eng Rep. 2009;66:1–70. doi: 10.1016/j.mser.2009.05.001.
    1. Long PH. Medical devices in orthopedic applications. Toxicol Pathol. 2008;36:85–91. doi: 10.1177/0192623307310951.
    1. Chevalier J, Gremillard L. Ceramics for medical applications: A picture for the next 20 years. J Eur Ceram Soc. 2009;29:1245–55. doi: 10.1016/j.jeurceramsoc.2008.08.025.
    1. Vallet-Regí M. Evolution of bioceramics within the field of biomaterials. C R Chim. 2010;13:174–85. doi: 10.1016/j.crci.2009.03.004.
    1. Duan K, Wang R. Surface modifications of bone implants through wet chemistry. J Mater Chem. 2006;16:2309–21. doi: 10.1039/b517634d.
    1. Ercan B, Kummer KM, Tarquinio KM, Webster TJ. Decreased Staphylococcus aureus biofilm growth on anodized nanotubular titanium and the effect of electrical stimulation. Acta Biomater. 2011;7:3003–12. doi: 10.1016/j.actbio.2011.04.002.
    1. Zilberman M, Elsner JJ. Antibiotic-eluting medical devices for various applications. J Control Release. 2008;130:202–15. doi: 10.1016/j.jconrel.2008.05.020.
    1. Trampuz A, Osmon DR, Hanssen AD, Steckelberg JM, Patel R. Molecular and antibiofilm approaches to prosthetic joint infection. Clin Orthop Relat Res. 2003;414:69–88. doi: 10.1097/01.blo.0000087324.60612.93.
    1. Turner IG, Pilliar RM, Srichana T, Domb AJ, Lacroix D, Planell JA, et al. Sterility and Infection. In: Narayan R, ed. Biomedical Materials. New York, NY: Springer Science, 2009:239-258.
    1. Davies D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov. 2003;2:114–22. doi: 10.1038/nrd1008.
    1. Gristina AG, Naylor P, Myrvik Q. Infections from biomaterials and implants: a race for the surface. Med Prog Technol. 1988-1989;14:205–24.
    1. Montanaro L, Campoccia D, Arciola CR. Nanostructured materials for inhibition of bacterial adhesion in orthopedic implants: a minireview. Int J Artif Organs. 2008;31:771–6.
    1. Alexander H, Anderson JM, Bianco RW, Brunski JB, Chang TMS, Colas A, et al. Host Reactions to Biomaterials and Their Evaluation. In: Ratner BD, Hoffman AS, Schoen FJ, Lemons JE, eds. Biomaterials Science: An Introduction to Materials in Medicine. 2nd Edition. London, UK: Elsevier Academic Press, 2004:293-345.
    1. Campoccia D, Montanaro L, Arciola CR. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials. 2006;27:2331–9. doi: 10.1016/j.biomaterials.2005.11.044.
    1. Kalita SJ, Verma S. Nanocrystalline hydroxyapatite bioceramic using microwave radiation: Synthesis and characterization. Mater Sci Eng C. 2010;30:295–303. doi: 10.1016/j.msec.2009.11.007.
    1. Harris LG, Richards RG. Staphylococci and implant surfaces: a review. Injury. Int J Care Injured. 2006;37:3–14. doi: 10.1016/j.injury.2006.04.003.
    1. Teterycz D, Ferry T, Lew D, Stern R, Assal M, Hoffmeyer P, et al. Outcome of orthopedic implant infections due to different staphylococci. Int J Infect Dis. 2010;14:e913–8. doi: 10.1016/j.ijid.2010.05.014.
    1. Wright JA, Nair SP. Interaction of staphylococci with bone. Int J Med Microbiol. 2010;300:193–204. doi: 10.1016/j.ijmm.2009.10.003.
    1. Ghasemzadeh-Moghaddam H, Ghaznavi-Rad E, Sekawi Z, Yun-Khoon L, Aziz MN, Hamat RA, et al. Methicillin-susceptible Staphylococcus aureus from clinical and community sources are genetically diverse. Int J Med Microbiol. 2011;301:347–53. doi: 10.1016/j.ijmm.2010.10.004.
    1. Campoccia D, Baldassarri L, Pirini V, Ravaioli S, Montanaro L, Arciola CR. Molecular epidemiology of Staphylococcus aureus from implant orthopaedic infections: ribotypes, agr polymorphism, leukocidal toxins and antibiotic resistance. Biomaterials. 2008;29:4108–16. doi: 10.1016/j.biomaterials.2008.07.006.
    1. François P, Scherl A, Hochstrasser D, Schrenzel J. Proteomic approaches to study Staphylococcus aureus pathogenesis. J Proteomics. 2010;73:701–8. doi: 10.1016/j.jprot.2009.10.007.
    1. Hudson MC, Ramp WK, Frankenburg KP. Staphylococcus aureus adhesion to bone matrix and bone-associated biomaterials. FEMS Microbiol Lett. 1999;173:279–84. doi: 10.1111/j.1574-6968.1999.tb13514.x.
    1. Arciola CR, Campoccia D, Gamberini S, Donati ME, Montanaro L. Presence of fibrinogen-binding adhesin gene in Staphylococcus epidermidis isolates from central venous catheters-associated and orthopaedic implant-associated infections. Biomaterials. 2004;25:4825–9. doi: 10.1016/j.biomaterials.2003.11.056.
    1. Cerca N, Martins S, Pier GB, Oliveira R, Azeredo J. The relationship between inhibition of bacterial adhesion to a solid surface by sub-MICs of antibiotics and subsequent development of a biofilm. Res Microbiol. 2005;156:650–5. doi: 10.1016/j.resmic.2005.02.004.
    1. Vuong C, Otto M. Staphylococcus epidermidis infections. Microbes Infect. 2002;4:481–9. doi: 10.1016/S1286-4579(02)01563-0.
    1. Montanaro L, Campoccia D, Arciola CR. Advancements in molecular epidemiology of implant infections and future perspectives. Biomaterials. 2007;28:5155–68. doi: 10.1016/j.biomaterials.2007.08.003.
    1. Arciola CR, Campoccia D, Gamberini S, Donati ME, Pirini V, Visai L, et al. Antibiotic resistance in exopolysaccharide-forming Staphylococcus epidermidis clinical isolates from orthopaedic implant infections. Biomaterials. 2005;26:6530–5. doi: 10.1016/j.biomaterials.2005.04.031.
    1. Brady RA, Leid JG, Costerton JW, Shirtliff ME. Osteomyelitis: Clinical Overview and Mechanisms of Infection Persistence. Clin Microbiol Newsl. 2006;28:65–72. doi: 10.1016/j.clinmicnews.2006.04.001.
    1. Cai XY, Yang C, Zhang ZY, Qiu WL, Chen MJ, Zhang SY. Septic arthritis of the temporomandibular joint: a retrospective review of 40 cases. J Oral Maxillofac Surg. 2010;68:731–8. doi: 10.1016/j.joms.2009.07.060.
    1. Aaskov JG, Abdel-Rahman SM, Aebi C, Ament ME, Anderson MS, Arnon SS, et al. Infections Related to prosthetic or artificial devices. In: Feigin RD, Cherry JD, Demmler-Harrison GJ, Kaplan SL, eds. Textbook of Pediatric Infectious Diseases. 6th Edition. Philadelphia, PA: Elsevier Inc., 2009.
    1. Lidgren L, Knutson K, Stefánsdóttir A. Infection and arthritis. Infection of prosthetic joints. Best Pract Res Clin Rheumatol. 2003;17:209–18. doi: 10.1016/S1521-6942(03)00002-0.
    1. Sawan SP, Manivannan G. In: Sawan SP, Manivannan G, eds. Antimicrobial/Anti-Infective Materials: Principles, Applications and Devices. Lancaster, LA: Technomic Publishing Company, Inc., 2000.
    1. Lew DP, Waldvogel FA. Osteomyelitis. Lancet. 2004;364:369–79. doi: 10.1016/S0140-6736(04)16727-5.
    1. Weichert S, Sharland M, Clarke NM, Faust SN. Acute haematogenous osteomyelitis in children: is there any evidence for how long we should treat? Curr Opin Infect Dis. 2008;21:258–62. doi: 10.1097/QCO.0b013e3283005441.
    1. Blyth MJ, Kincaid R, Craigen MA, Bennet GC. The changing epidemiology of acute and subacute haematogenous osteomyelitis in children. J Bone Joint Surg Br. 2001;83:99–102. doi: 10.1302/0301-620X.83B1.10699.
    1. Lazzarini L, Mader JT, Calhoun JH. Osteomyelitis in long bones. J Bone Joint Surg Am. 2004;86-A:2305–18.
    1. Gillespie WJ. Epidemiology in bone and joint infection. Infect Dis Clin North Am. 1990;4:361–76.
    1. Dubost JJ, Soubrier M, De Champs C, Ristori JM, Bussiére JL, Sauvezie B. No changes in the distribution of organisms responsible for septic arthritis over a 20 year period. Ann Rheum Dis. 2002;61:267–9. doi: 10.1136/ard.61.3.267.
    1. Mathews CJ, Weston VC, Jones A, Field M, Coakley G. Bacterial septic arthritis in adults. Lancet. 2010;375:846–55. doi: 10.1016/S0140-6736(09)61595-6.
    1. Goldenberg DL. Septic arthritis. Lancet. 1998;351:197–202. doi: 10.1016/S0140-6736(97)09522-6.
    1. Nade S. Septic arthritis. Best Pract Res Clin Rheumatol. 2003;17:183–200. doi: 10.1016/S1521-6942(02)00106-7.
    1. Stot NS. Paediatric bone and joint infection. J Orthop Surg. 2001;9:83–90.
    1. Levine M, Siegel LB. A swollen joint: why all the fuss? Am J Ther. 2003;10:219–24. doi: 10.1097/00045391-200305000-00009.
    1. Geirsson AJ, Statkevicius S, Víkingsson A. Septic arthritis in Iceland 1990-2002: increasing incidence due to iatrogenic infections. Ann Rheum Dis. 2008;67:638–43. doi: 10.1136/ard.2007.077131.
    1. Coakley G, Mathews C, Field M, Jones A, Kingsley G, Walker D, et al. British Society for Rheumatology Standards, Guidelines and Audit Working Group BSR & BHPR, BOA, RCGP and BSAC guidelines for management of the hot swollen joint in adults. Rheumatology (Oxford) 2006;45:1039–41. doi: 10.1093/rheumatology/kel163a.
    1. Esposito S, Leone S. Prosthetic joint infections: microbiology, diagnosis, management and prevention. Int J Antimicrob Agents. 2008;32:287–93. doi: 10.1016/j.ijantimicag.2008.03.010.
    1. Rohde H, Burandt EC, Siemssen N, Frommelt L, Burdelski C, Wurster S, et al. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials. 2007;28:1711–20. doi: 10.1016/j.biomaterials.2006.11.046.
    1. Trampuz A, Zimmerli W. Prosthetic joint infections: update in diagnosis and treatment. Swiss Med Wkly. 2005;135:243–51.
    1. Hanssen AD, Rand JA. Evaluation and treatment of infection at the site of a total hip or knee arthroplasty. Instr Course Lect. 1999;48:111–22.
    1. Sculco TP. The economic impact of infected joint arthroplasty. Orthopedics. 1995;18:871–3.
    1. Berbari EF, Hanssen AD, Duffy MC, Steckelberg JM, Ilstrup DM, Harmsen WS, et al. Risk factors for prosthetic joint infection: case-control study. Clin Infect Dis. 1998;27:1247–54. doi: 10.1086/514991.
    1. Fisman DN, Reilly DT, Karchmer AW, Goldie SJ. Clinical effectiveness and cost-effectiveness of 2 management strategies for infected total hip arthroplasty in the elderly. Clin Infect Dis. 2001;32:419–30. doi: 10.1086/318502.
    1. Lentino JR. Prosthetic joint infections: bane of orthopedists, challenge for infectious disease specialists. Clin Infect Dis. 2003;36:1157–61. doi: 10.1086/374554.
    1. Zimmerli W, Trampuz A, Ochsner PE. Prosthetic-joint infections. N Engl J Med. 2004;351:1645–54. doi: 10.1056/NEJMra040181.
    1. Giulieri SG, Graber P, Ochsner PE, Zimmerli W. Management of infection associated with total hip arthroplasty according to a treatment algorithm. Infection. 2004;32:222–8. doi: 10.1007/s15010-004-4020-1.
    1. Laffer R, Graber P, Ochsner P, Zimmerli W. The case for differentiated orthopedic management of prosthetic knee-associated infection. 44th ICAAC, American Society for Microbiology, 2004, Washington, DC 2004; Abstract K-113.
    1. Zimmerli W. Infection and musculoskeletal conditions: Prosthetic-joint-associated infections. Best Pract Res Clin Rheumatol. 2006;20:1045–63. doi: 10.1016/j.berh.2006.08.003.
    1. Vacheethasanee K, Temenoff JS, Higashi JM, Gary A, Anderson JM, Bayston R, et al. Bacterial surface properties of clinically isolated Staphylococcus epidermidis strains determine adhesion on polyethylene. J Biomed Mater Res. 1998;42:425–32. doi: 10.1002/(SICI)1097-4636(19981205)42:3<425::AID-JBM12>;2-F.
    1. An YH, Friedman RJ. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J Biomed Mater Res. 1998;43:338–48. doi: 10.1002/(SICI)1097-4636(199823)43:3<338::AID-JBM16>;2-B.
    1. An YH, Friedman RJ, Draughn RA, Smith EA, Nicholson JH, John JF. Rapid quantification of staphylococci adhered to titanium surfaces using image analyzed epifluorescence microscopy. J Microbiol Methods. 1995;24:29–40. doi: 10.1016/0167-7012(95)00051-8.
    1. Costa F, Carvalho IF, Montelaro RC, Gomes P, Martins MCL. Covalent immobilization of antimicrobial peptides (AMPs) onto biomaterial surfaces. Acta Biomater. 2011;7:1431–40. doi: 10.1016/j.actbio.2010.11.005.
    1. Extremina CI, Granja PL, da Fonseca AF, Fonseca AP. Adhesion of staphylococcus epidermidis to a modified cellulose triacetate membrane. Int J Antimicrob Agents. 2007;29:S143–S144. doi: 10.1016/S0924-8579(07)70458-2.
    1. Fonseca AP, Granja PL, Nogueira JA, Oliveira DR, Barbosa MA. Staphylococcus epidermidis RP62A adhesion to chemically modified cellulose derivatives. J Mater Sci Mater Med. 2001;12:543–8. doi: 10.1023/A:1011227915575.
    1. Fonseca AP, Extremina C, Fonseca AF, Sousa JC. Effect of subinhibitory concentration of piperacillin/tazobactam on Pseudomonas aeruginosa. J Med Microbiol. 2004;53:903–10. doi: 10.1099/jmm.0.45637-0.
    1. Ueshima M, Tanaka S, Nakamura S, Yamashita K. Manipulation of bacterial adhesion and proliferation by surface charges of electrically polarized hydroxyapatite. J Biomed Mater Res. 2002;60:578–84. doi: 10.1002/jbm.10113.
    1. Popat KC, Eltgroth M, Latempa TJ, Grimes CA, Desai TA. Decreased Staphylococcus epidermis adhesion and increased osteoblast functionality on antibiotic-loaded titania nanotubes. Biomaterials. 2007;28:4880–8. doi: 10.1016/j.biomaterials.2007.07.037.
    1. Katsikogianni M, Missirlis YF. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur Cell Mater. 2004;8:37–57.
    1. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358:135–8. doi: 10.1016/S0140-6736(01)05321-1.
    1. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167–93. doi: 10.1128/CMR.15.2.167-193.2002. [were added.]
    1. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science. 1998;280:295–8. doi: 10.1126/science.280.5361.295.
    1. Harris LG, Tosatti S, Wieland M, Textor M, Richards RG. Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(L-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials. 2004;25:4135–48. doi: 10.1016/j.biomaterials.2003.11.033.
    1. Katsikogianni M, Spiliopoulou I, Dowling DP, Missirlis YF. Adhesion of slime producing Staphylococcus epidermidis strains to PVC and diamond-like carbon/silver/fluorinated coatings. J Mater Sci Mater Med. 2006;17:679–89. doi: 10.1007/s10856-006-9678-8.
    1. Hetrick EM, Schoenfisch MH. Reducing implant-related infections: active release strategies. Chem Soc Rev. 2006;35:780–9. doi: 10.1039/b515219b.
    1. Martins MC, Wang D, Ji J, Feng L, Barbosa MA. Albumin and fibrinogen adsorption on cibacron blue F3G-A immobilised onto PU-PHEMA (polyurethane-poly(hydroxyethylmethacrylate)) surfaces. J Biomater Sci Polym Ed. 2003;14:439–55. doi: 10.1163/156856203766652057.
    1. Grenho L, Manso MC, Monteiro FJ, Ferraz MP. Adhesion of Staphylococcus aureus, Staphylococcus epidermidis, and Pseudomonas aeruginosa onto nanohydroxyapatite as a bone regeneration material. J Biomed Mater Res A. 2012;100:1823–30. doi: 10.1002/jbm.a.34139.
    1. Extremina CI, Fonseca AF, Granja PL, Fonseca AP. Anti-adhesion and antiproliferative cellulose triacetate membrane for prevention of biomaterial-centred infections associated with Staphylococcus epidermidis. Int J Antimicrob Agents. 2010;35:164–8. doi: 10.1016/j.ijantimicag.2009.09.017.
    1. Parreira P, Magalhães A, Gonçalves IC, Gomes J, Vidal R, Reis CA, et al. Effect of surface chemistry on bacterial adhesion, viability, and morphology. J Biomed Mater Res A. 2011;99:344–53. doi: 10.1002/jbm.a.33178.
    1. Isberg RR, Barnes P. Dancing with the host; flow-dependent bacterial adhesion. Cell. 2002;110:1–4. doi: 10.1016/S0092-8674(02)00821-8.
    1. Klapper I, Rupp CJ, Cargo R, Purvedorj B, Stoodley P. Viscoelastic fluid description of bacterial biofilm material properties. Biotechnol Bioeng. 2002;80:289–96. doi: 10.1002/bit.10376.
    1. Katsikogianni MG, Missirlis YF. Interactions of bacteria with specific biomaterial surface chemistries under flow conditions. Acta Biomater. 2010;6:1107–18. doi: 10.1016/j.actbio.2009.08.006.
    1. Liu Y, Tay J-H. The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Res. 2002;36:1653–65. doi: 10.1016/S0043-1354(01)00379-7.
    1. Mohamed N, Rainier TR, Jr., Ross JM. Novel experimental study of receptor-mediated bacterial adhesion under the influence of fluid shear. Biotechnol Bioeng. 2000;68:628–36. doi: 10.1002/(SICI)1097-0290(20000620)68:6<628::AID-BIT5>;2-D.
    1. Rowland BM. Bacterial contamination of dental unit waterlines: what is your dentist spraying into your mouth? Clin Microbiol Newsl. 2003;25:73–7. doi: 10.1016/S0196-4399(03)80016-8.
    1. Garret TR, Bhakoo M, Zhang Z. Bacterial adhesion and biofilms on surfaces. Prog Nat Sci. 2008;18:1049–56. doi: 10.1016/j.pnsc.2008.04.001.
    1. Li Y, Hanna MN, Svensäter G, Ellen RP, Cvitkovitch DG. Cell density modulates acid adaption in Streptococcus mutans. J Bacteriol. 2001;183:6875–84. doi: 10.1128/JB.183.23.6875-6884.2001.
    1. Oliveira R, Melo L, Oliveira A, Salgueiro R. Polysaccharide production and biofilm formation by Pseudomonas fluorescens: effects of pH and surface material. Col Surf B: Biointerf. 1994;2:41–6. doi: 10.1016/0927-7765(94)80016-2.
    1. Hamadi F, Latrache H, Mabrrouki M, Elghmari A, Outzourhit A, Ellouali M, et al. Effect of pH on distribution and adhesion of Staphylococcus aureus to glass. J Adhes Sci Technol. 2005;19:73–85. doi: 10.1163/1568561053066891.
    1. Kinnari TJ, Esteban J, Martin-de-Hijas NZ, Sánchez-Muñoz O, Sánchez-Salcedo S, Colilla M, et al. Influence of surface porosity and pH on bacterial adherence to hydroxyapatite and biphasic calcium phosphate bioceramics. J Med Microbiol. 2009;58:132–7. doi: 10.1099/jmm.0.002758-0.
    1. Konttinen YT, Takagi M, Mandelin J, Lassus J, Salo J, Ainola M, et al. Acid attack and cathepsin K in bone resorption around total hip replacement prosthesis. J Bone Miner Res. 2001;16:1780–6. doi: 10.1359/jbmr.2001.16.10.1780.
    1. Ferraz MP, Mateus AY, Sousa JC, Monteiro FJ. Nanohydroxyapatite microspheres as delivery system for antibiotics: release kinetics, antimicrobial activity, and interaction with osteoblasts. J Biomed Mater Res A. 2007;81:994–1004. doi: 10.1002/jbm.a.31151.
    1. Kohnen W, Kolbenschlag C, Teske-Keiser S, Jansen B. Development of a long-lasting ventricular catheter impregnated with a combination of antibiotics. Biomaterials. 2003;24:4865–9. doi: 10.1016/S0142-9612(03)00379-X.
    1. Stigter M, de Groot K, Layrolle P. Incorporation of tobramycin into biomimetic hydroxyapatite coating on titanium. Biomaterials. 2002;23:4143–53. doi: 10.1016/S0142-9612(02)00157-6.
    1. Galanakos SP, Papadakis SA, Kateros K, Papakostas I, Macheras G. Biofilm and orthopaedic practice: the world of microbes in a world of implants. Orthop Trauma. 2009;23:175–9.
    1. Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis. 2002;8:881–90. doi: 10.3201/eid0809.020063.
    1. Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Annu Rev Microbiol. 2002;56:187–209. doi: 10.1146/annurev.micro.56.012302.160705.
    1. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358:135–8. doi: 10.1016/S0140-6736(01)05321-1.
    1. Costerton JW, Stewart PS. Battling biofilms. Sci Am. 2001;285:74–81. doi: 10.1038/scientificamerican0701-74.
    1. Furneri PM, Garozzo A, Musumarra MP, Scuderi AC, Russo A, Bonfiglio G. Effects on adhesiveness and hydrophobicity of sub-inhibitory concentrations of netilmicin. Int J Antimicrob Agents. 2003;22:164–7. doi: 10.1016/S0924-8579(03)00149-3.
    1. Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun. 1999;67:5427–33.
    1. Galdbart JO, Allignet J, Tung HS, Rydèn C, El Solh N. Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses. J Infect Dis. 2000;182:351–5. doi: 10.1086/315660.
    1. del Prado G, Ruiz V, Naves P, Rodríguez-Cerrato V, Soriano F, del Carmen Ponte M. Biofilm formation by Streptococcus pneumoniae strains and effects of human serum albumin, ibuprofen, N-acetyl-l-cysteine, amoxicillin, erythromycin, and levofloxacin. Diagn Microbiol Infect Dis. 2010;67:311–8. doi: 10.1016/j.diagmicrobio.2010.03.016.
    1. Poelstra KA, Barekzi NA, Rediske AM, Felts AG, Slunt JB, Grainger DW. Prophylactic treatment of gram-positive and gram-negative abdominal implant infections using locally delivered polyclonal antibodies. J Biomed Mater Res. 2002;60:206–15. doi: 10.1002/jbm.10069.
    1. Pagano PJ, Buchanan LV, Dailey CF, Haas JV, Van Enk RA, Gibson JK. Effects of linezolid on staphylococcal adherence versus time of treatment. Int J Antimicrob Agents. 2004;23:226–34. doi: 10.1016/j.ijantimicag.2003.07.012.
    1. Scheuerman TR, Camper AK, Hamilton MA. Effects of substratum topography on bacterial adhesion. J Colloid Interface Sci. 1998;208:23–33. doi: 10.1006/jcis.1998.5717.
    1. Oztürk O, Sudagidan M, Türkan U. Biofilm formation by Staphylococcus epidermidis on nitrogen ion implanted CoCrMo alloy material. J Biomed Mater Res A. 2007;81:663–8. doi: 10.1002/jbm.a.31037.
    1. Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res. 2006;17(Suppl 2):68–81. doi: 10.1111/j.1600-0501.2006.01353.x.
    1. Katainen J, Paajanen M, Ahtola E, Pore V, Lahtinen J. Adhesion as an interplay between particle size and surface roughness. J Colloid Interface Sci. 2006;304:524–9. doi: 10.1016/j.jcis.2006.09.015.
    1. Mitik-Dineva N, Wang J, Mocanasu RC, Stoddart PR, Crawford RJ, Ivanova EP. Impact of nano-topography on bacterial attachment. Biotechnol J. 2008;3:536–44. doi: 10.1002/biot.200700244.
    1. Truong VK, Lapovok R, Estrin YS, Rundell S, Wang JY, Fluke CJ, et al. The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials. 2010;31:3674–83. doi: 10.1016/j.biomaterials.2010.01.071.
    1. Whitehead KA, Colligon J, Verran J. Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloids Surf B Biointerfaces. 2005;41:129–38. doi: 10.1016/j.colsurfb.2004.11.010.
    1. Webster TJ, Tong Z, Liu J, Katherine Banks M. Adhesion of Pseudomonas fluorescens onto nanophase materials. Nanotechnology. 2005;16:S449–57. doi: 10.1088/0957-4484/16/7/021.
    1. Colon G, Ward BC, Webster TJ. Increased osteoblast and decreased Staphylococcus epidermidis functions on nanophase ZnO and TiO2. J Biomed Mater Res A. 2006;78:595–604. doi: 10.1002/jbm.a.30789.
    1. Merritt K, Shafer JW, Brown SA. Implant site infection rates with porous and dense materials. J Biomed Mater Res. 1979;13:101–8. doi: 10.1002/jbm.820130111.
    1. Harris JM, Martin LF. An in vitro study of the properties influencing Staphylococcus epidermidis adhesion to prosthetic vascular graft materials. Ann Surg. 1987;206:612–20. doi: 10.1097/00000658-198711000-00010.
    1. Doyle RJ. Contribution of the hydrophobic effect to microbial infection. Microbes Infect. 2000;2:391–400. doi: 10.1016/S1286-4579(00)00328-2.
    1. Meyer HGW, Gatermann S. Surface properties of Staphylococcus saprophyticus: hydrophobicity, haemagglutination and Staphylococcus saprophyticus surface-associated protein (Ssp) represent distinct entities. APMIS. 1994;102:538–44. doi: 10.1111/j.1699-0463.1994.tb05203.x.
    1. Charville GW, Hetrick EM, Geer CB, Schoenfisch MH. Reduced bacterial adhesion to fibrinogen-coated substrates via nitric oxide release. Biomaterials. 2008;29:4039–44. doi: 10.1016/j.biomaterials.2008.07.005.
    1. Walker SL, Hill JE, Redman JA, Elimelech M. Influence of growth phase on adhesion kinetics of Escherichia coli D21g. Appl Environ Microbiol. 2005;71:3093–9. doi: 10.1128/AEM.71.6.3093-3099.2005.
    1. Kuntiya A, Nicolella C, Pyle L, Poosaran N. Effect of sodium chloride on cell surface hydrophobicity and formation of biofilm in membrane bioreactor. Songklanakarin J Sci Technol. 2005;27:1073–82.
    1. Hussain M, Wilcox MH, White PJ, Faulkner MK, Spencer RC. Importance of medium and atmosphere type to both slime production and adherence by coagulase-negative staphylococci. J Hosp Infect. 1992;20:173–84. doi: 10.1016/0195-6701(92)90085-Z.
    1. Xu LC, Siedlecki CA. Effects of surface wettability and contact time on protein adhesion to biomaterial surfaces. Biomaterials. 2007;28:3273–83. doi: 10.1016/j.biomaterials.2007.03.032.
    1. Luensmann D, Jones L. Albumin adsorption to contact lens materials: a review. Cont Lens Anterior Eye. 2008;31:179–87. doi: 10.1016/j.clae.2008.05.004.
    1. Khoo X, O’Toole GA, Nair SA, Snyder BD, Kenan DJ, Grinstaff MW. Staphylococcus aureus resistance on titanium coated with multivalent PEGylated-peptides. Biomaterials. 2010;31:9285–92. doi: 10.1016/j.biomaterials.2010.08.031.
    1. Tang H, Wang A, Liang X, Cao T, Salley SO, McAllister JP, 3rd, et al. Effect of surface proteins on Staphylococcus epidermidis adhesion and colonization on silicone. Colloids Surf B Biointerfaces. 2006;51:16–24. doi: 10.1016/j.colsurfb.2006.04.011.
    1. Arciola CR, Bustanji Y, Conti M, Campoccia D, Baldassarri L, Samorì B, et al. Staphylococcus epidermidis-fibronectin binding and its inhibition by heparin. Biomaterials. 2003;24:3013–9. doi: 10.1016/S0142-9612(03)00133-9.
    1. Holmes SD, May K. Johanss on V, Markey F, Critchley IA. Studies on the interaction of Staphylococcus aureus and Staphylococcus epidermidis with fibronectin using surface Plasmon resonance (BIAcore) J Microbiol Methods. 1997;28:77–84. doi: 10.1016/S0167-7012(96)00967-0.
    1. Henderson B, Nair S, Pallas J, Williams MA. Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol Rev. 2011;35:147–200. doi: 10.1111/j.1574-6976.2010.00243.x.
    1. Williams RJ, Henderson B, Nair SP. Staphylococcus aureus fibronectin binding proteins A and B possess a second fibronectin binding region that may have biological relevance to bone tissues. Calcif Tissue Int. 2002;70:416–21. doi: 10.1007/s00223-001-2073-z.
    1. Williams RJ, Henderson B, Sharp LJ, Nair SP. Identification of a fibronectin-binding protein from Staphylococcus epidermidis. Infect Immun. 2002;70:6805–10. doi: 10.1128/IAI.70.12.6805-6810.2002.
    1. Buck AW, Fowler VG, Jr., Yongsunthon R, Liu J, DiBartola AC, Que YA, et al. Bonds between fibronectin and fibronectin-binding proteins on Staphylococcus aureus and Lactococcus lactis. Langmuir. 2010;26:10764–70. doi: 10.1021/la100549u.
    1. Fowler T, Wann ER, Joh D, Johansson S, Foster TJ, Höök M. Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell β1 integrins. Eur J Cell Biol. 2000;79:672–9. doi: 10.1078/0171-9335-00104.
    1. 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. doi: 10.1053/jinf.2000.0657.
    1. Schwarz-Linek U, Höök M, Potts JR. Fibronectin-binding proteins of gram-positive cocci. Microbes Infect. 2006;8:2291–8. doi: 10.1016/j.micinf.2006.03.011.
    1. Rohde H, Frankenberger S, Zähringer U, Mack D. Structure, function and contribution of polysaccharide intercellular adhesin (PIA) to Staphylococcus epidermidis biofilm formation and pathogenesis of biomaterial-associated infections. Eur J Cell Biol. 2010;89:103–11. doi: 10.1016/j.ejcb.2009.10.005.
    1. Christner M, Franke GC, Schommer NN, Wendt U, Wegert K, Pehle P, et al. The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol Microbiol. 2010;75:187–207. doi: 10.1111/j.1365-2958.2009.06981.x.
    1. Kinnari TJ, Peltonen LI, Kuusela P, Kivilahti J, Könönen M, Jero J. Bacterial adherence to titanium surface coated with human serum albumin. Otol Neurotol. 2005;26:380–4. doi: 10.1097/01.mao.0000169767.85549.87.
    1. Brokke P, Dankert J, Carballo J, Feijen J. Adherence of coagulase-negative staphylococci onto polyethylene catheters in vitro and in vivo: a study on the influence of various plasma proteins. J Biomater Appl. 1991;5:204–26. doi: 10.1177/088532829100500305.
    1. Reynolds EC, Wong A. Effect of adsorbed protein on hydroxyapatite zeta potential and Streptococcus mutans adherence. Infect Immun. 1983;39:1285–90.
    1. An YH, Bradley J, Powers DL, Friedman RJ. The prevention of prosthetic infection using a cross-linked albumin coating in a rabbit model. J Bone Joint Surg Br. 1997;79:816–9. doi: 10.1302/0301-620X.79B5.7228.
    1. del Prado G, Ruiz V, Naves P, Rodríguez-Cerrato V, Soriano F, del Carmen Ponte M. Biofilm formation by Streptococcus pneumoniae strains and effects of human serum albumin, ibuprofen, N-acetyl-l-cysteine, amoxicillin, erythromycin, and levofloxacin. Diagn Microbiol Infect Dis. 2010;67:311–8. doi: 10.1016/j.diagmicrobio.2010.03.016.
    1. Naves P, del Prado G, Huelves L, Rodríguez-Cerrato V, Ruiz V, Ponte MC, et al. Effects of human serum albumin, ibuprofen and N-acetyl-L-cysteine against biofilm formation by pathogenic Escherichia coli strains. J Hosp Infect. 2010;76:165–70. doi: 10.1016/j.jhin.2010.05.011.
    1. Tegoulia VA, Cooper SL. Staphylococcus aureus adhesion to self-assembled monolayers: effect of surface chemistry and fibrinogen presence. Col Surf B: Biointerf. 2002;24:217–28. doi: 10.1016/S0927-7765(01)00240-5.
    1. Herrmann M, Vaudaux PE, Pittet D, Auckenthaler R, Lew PD, Schumacher-Perdreau F, et al. Fibronectin, fibrinogen, and laminin act as mediators of adherence of clinical staphylococcal isolates to foreign material. J Infect Dis. 1988;158:693–701. doi: 10.1093/infdis/158.4.693.
    1. Arciola CR, Campoccia D, Gamberini S, Donati ME, Montanaro L. Presence of fibrinogen-binding adhesin gene in Staphylococcus epidermidis isolates from central venous catheters-associated and orthopaedic implant-associated infections. Biomaterials. 2004;25:4825–9. doi: 10.1016/j.biomaterials.2003.11.056.
    1. Baumgartner JN, Cooper SL. Influence of thrombus components in mediating Staphylococcus aureus adhesion to polyurethane surfaces. J Biomed Mater Res. 1998;40:660–70. doi: 10.1002/(SICI)1097-4636(19980615)40:4<660::AID-JBM18>;2-J.
    1. Pei L, Flock JI. Functional study of antibodies against a fibrogenin-binding protein in Staphylococcus epidermidis adherence to polyethylene catheters. J Infect Dis. 2001;184:52–5. doi: 10.1086/321003.
    1. Patti JM, Allen BL, McGavin MJ, Höök M. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol. 1994;48:585–617. doi: 10.1146/annurev.mi.48.100194.003101.
    1. Elgalai I, Foster HA. Comparison of adhesion of wound isolates of Staphylococcus aureus to immobilized proteins. J Appl Microbiol. 2003;94:413–20. doi: 10.1046/j.1365-2672.2003.01858.x.
    1. Pei L, Arvholm IL, Lonnies L, Flock JI. GST-Fbe can recognize B-chains of fibrin(ogen) on explanted materials. J Chromatogr B Analyt Technol Biomed Life Sci. 2003;86:319–25. doi: 10.1016/S1570-0232(02)00744-4.
    1. Taylor FB, Jr., Wada H, Kinasewitz G. Description of compensated and uncompensated disseminated intravascular coagulation (DIC) responses (non-overt and overt DIC) in baboon models of intravenous and intraperitoneal Escherichia coli sepsis and in the human model of endotoxemia: toward a better definition of DIC. Crit Care Med. 2000;28(Suppl):S12–9. doi: 10.1097/00003246-200009001-00004.
    1. Tedjo C, Neoh KG, Kang ET, Fang N, Chan V. Bacteria-surface interaction in the presence of proteins and surface attached poly(ethylene glycol) methacrylate chains. J Biomed Mater Res A. 2007;82:479–91. doi: 10.1002/jbm.a.31172.
    1. Lopes JD, dos Reis M, Brentani RR. Presence of laminin receptors in Staphylococcus aureus. Science. 1985;229:275–7. doi: 10.1126/science.3160113.
    1. Wang IW, Anderson JM, Marchant RE. Staphylococcus epidermidis adhesion to hydrophobic biomedical polymer is mediated by platelets. J Infect Dis. 1993;167:329–36. doi: 10.1093/infdis/167.2.329.
    1. Benson DE, Burns GL, Mohammad SF. Effect of plasma on adhesion of biofilm forming Pseudomonas aeruginosa and Staphylococcus epidermidis to fibrin substrate. Trans Am Soc Artif Intern Organs. 1996;42:M655–60. doi: 10.1097/00002480-199609000-00069.
    1. Ardehali R, Shi L, Janatova J, Mohammad SF, Burns GL. The inhibitory activity of serum to prevent bacterial adhesion is mainly due to apo-transferrin. J Biomed Mater Res A. 2003;66:21–8. doi: 10.1002/jbm.a.10493.
    1. Ubbink J, Schär-Zammaretti P. Probing bacterial interactions: integrated approaches combining atomic force microscopy, electron microscopy and biophysical techniques. Micron. 2005;36:293–320. doi: 10.1016/j.micron.2004.11.005.
    1. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Götz F. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol. 1996;20:1083–91. doi: 10.1111/j.1365-2958.1996.tb02548.x.
    1. O’Gara JP, Humphreys H. Staphylococcus epidermidis biofilms: importance and implications. J Med Microbiol. 2001;50:582–7.
    1. Götz F. Staphylococcus and biofilms. Mol Microbiol. 2002;43:1367–78. doi: 10.1046/j.1365-2958.2002.02827.x.
    1. Perrin C, Briandet R, Jubelin G, Lejeune P, Mandrand-Berthelot M-A, Rodrigue A, et al. Nickel promotes biofilm formation by Escherichia coli K-12 strains that produce curli. Appl Environ Microbiol. 2009;75:1723–33. doi: 10.1128/AEM.02171-08.
    1. Bagge N, Ciofu O, Skovgaard LT, Høiby N. Rapid development in vitro and in vivo of resistance to ceftazidime in biofilm-growing Pseudomonas aeruginosa due to chromosomal beta-lactamase. APMIS. 2000;108:589–600. doi: 10.1034/j.1600-0463.2000.d01-102.x.
    1. Xu KD, McFeters GA, Stewart PS. Biofilm resistance to antimicrobial agents. Microbiology. 2000;146:547–9.
    1. Chandra J, Mukherjee PK, Leidich SD, Faddoul FF, Hoyer LL, Douglas LJ, et al. Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J Dent Res. 2001;80:903–8. doi: 10.1177/00220345010800031101.
    1. Beech IB, Smith JR, Steele AA, Penegar I, Campbell SA. The use of atomic force microscopy for studying interactions of bacterial biofilms with surfaces. Col Surf B: Biointerf. 2002;23:231–47. doi: 10.1016/S0927-7765(01)00233-8.
    1. Otto K. Biophysical approaches to study the dynamic process of bacterial adhesion. Res Microbiol. 2008;159:415–22. doi: 10.1016/j.resmic.2008.04.007.
    1. Welch K, Cai Y, Strømme M. A Method for Quantitative Determination of Biofilm Viability. J Funct Biomater. 2012;3:418–31. doi: 10.3390/jfb3020418.
    1. Peeters E, Nelis HJ, Coenye T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods. 2008;72:157–65. doi: 10.1016/j.mimet.2007.11.010.
    1. Extremina CI, Costa L, Aguiar AI, Peixe L, Fonseca AP. Optimization of processing conditions for the quantification of enterococci biofilms using microtitre-plates. J Microbiol Methods. 2011;84:167–73. doi: 10.1016/j.mimet.2010.11.007.
    1. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Cirković I, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 2007;115:891–9. doi: 10.1111/j.1600-0463.2007.apm_630.x.
    1. Heikens E, Bonten MJM, Willems RJL. Enterococcal surface protein Esp is important for biofilm formation of Enterococcus faecium E1162. J Bacteriol. 2007;189:8233–40. doi: 10.1128/JB.01205-07.
    1. LaPlante KL, Mermel LA. In vitro activities of telavancin and vancomycin against biofilm-producing Staphylococcus aureus, S. epidermidis, and Enterococcus faecalis strains. Antimicrob Agents Chemother. 2009;53:3166–9. doi: 10.1128/AAC.01642-08.
    1. Kreander K, Vuorela P, Tammela P. A rapid screening method for detecting active compounds against erythromycin-resistant bacterial strains of Finnish origin. Folia Microbiol (Praha) 2005;50:487–93. doi: 10.1007/BF02931435.
    1. Sandberg M, Määttänen A, Peltonen J, Vuorela PM, Fallarero A. Automating a 96-well microtitre plate model for Staphylococcus aureus biofilms: an approach to screening of natural antimicrobial compounds. Int J Antimicrob Agents. 2008;32:233–40. doi: 10.1016/j.ijantimicag.2008.04.022.
    1. An YH, Friedman RJ. Laboratory methods for studies of bacterial adhesion. J Microbiol Methods. 1997;30:141–52. doi: 10.1016/S0167-7012(97)00058-4.
    1. An YH, Friedman RJ, Draughn RA, Smith EA, John JF, Ambrosio L, et al. Biomaterials and Biocompatibility Studies. In: Wise DL, Trantolo DJ, Altobelli DE, Yaszemski MJ, Gresser JD, eds. Human Biomaterials Applications. Totowa, NJ: Humana Press Inc., 1996:1-59.
    1. Whitehead KA, Smith LA, Verran J. The detection and influence of food soils on microorganisms on stainless steel using scanning electron microscopy and epifluorescence microscopy. Int J Food Microbiol. 2010;141(Suppl 1):S125–33. doi: 10.1016/j.ijfoodmicro.2010.01.012.
    1. Weir E, Lawlor A, Whelan A, Regan F. The use of nanoparticles in antimicrobial materials and their characterization. Analyst (Lond) 2008;133:835–45. doi: 10.1039/b715532h.
    1. Wirtanen G, Salo S, Helander IM, Mattila-Sandholm T. Microbiological methods for testing disinfectant efficiency on Pseudomonas biofilm. Colloids Surf B Biointerfaces. 2001;20:37–50. doi: 10.1016/S0927-7765(00)00173-9.
    1. Bogner A, Jouneau PH, Thollet G, Basset D, Gauthier C. A history of scanning electron microscopy developments: towards “wet-STEM” imaging. Micron. 2007;38:390–401. doi: 10.1016/j.micron.2006.06.008.
    1. Kodjikian L, Burillon C, Lina G, Roques C, Pellon G, Freney J, et al. Biofilm formation on intraocular lenses by a clinical strain encoding the ica locus: a scanning electron microscopy study. Invest Ophthalmol Vis Sci. 2003;44:4382–7. doi: 10.1167/iovs.03-0185.
    1. Pajkos A, Vickery K, Cossart Y. Is biofilm accumulation on endoscope tubing a contributor to the failure of cleaning and decontamination? J Hosp Infect. 2004;58:224–9. doi: 10.1016/j.jhin.2004.06.023.
    1. Camargo GMPA, Pizzolitto AC, Pizzolitto EL. Biofilm formation on catheters used after cesarean section as observed by scanning electron microscopy. Int J Gynaecol Obstet. 2005;90:148–9. doi: 10.1016/j.ijgo.2005.04.006.
    1. Lindsay D, von Holy A. Bacterial biofilms within the clinical setting: what healthcare professionals should know. J Hosp Infect. 2006;64:313–25. doi: 10.1016/j.jhin.2006.06.028.
    1. Cook G, Costerton JW, Darouiche RO. Direct confocal microscopy studies of the bacterial colonization in vitro of a silver-coated heart valve sewing cuff. Int J Antimicrob Agents. 2000;13:169–73. doi: 10.1016/S0924-8579(99)00120-X.
    1. Kazama JJ, Gejyo F, Ejiri S, Okada M, Ei I, Arakawa M, et al. Application of confocal laser scanning microscopy to the observation of bone biopsy specimens. Bone. 1993;14:885–9. doi: 10.1016/8756-3282(93)90319-6.
    1. Lemon KP, Earl AM, Vlamakis HC, Aguilar C, Kolter R, Spormann AM, et al. Biofilm Development with an Emphasis on Bacillus subtilis In: Romeo T, ed. Bacterial Biofilms. Clifton Rd., NE: Springer, 2008:1-14.
    1. Fett WF, Cooke PH. A survey of native microbial aggregates on alfalfa, clover and mung bean sprout cotyledons for thickness as determined by confocal scanning laser microscopy. Food Microbiol. 2005;22:253–9. doi: 10.1016/j.fm.2004.03.004.
    1. Burnett SL, Chen J, Beuchat LR. Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Appl Environ Microbiol. 2000;66:4679–87. doi: 10.1128/AEM.66.11.4679-4687.2000.
    1. Lindsay D, Brözel VS, Mostert JF, von Holy A. Differential efficacy of a chlorine dioxide-containing sanitizer against single species and binary biofilms of a dairy-associated Bacillus cereus and a Pseudomonas fluorescens isolate. J Appl Microbiol. 2002;92:352–61. doi: 10.1046/j.1365-2672.2002.01538.x.
    1. Hug T, Gujer W, Siegrist H. Rapid quantification of bacteria in activated sludge using fluorescence in situ hybridization and epifluorescence microscopy. Water Res. 2005;39:3837–48. doi: 10.1016/j.watres.2005.07.013.
    1. Robichon D, Girard J-C, Cenatiempo Y, Cavallier J-F. Atomic force microscopy imaging of dried or living bacteria. C R Acad Sci Paris. Life Sci. 1999;322:687–93.
    1. Willing GA, Ibrahim TH, Etzler FM, Neuman RD. New approach to the study of particle-surface adhesion using atomic force microscopy. J Colloid Interface Sci. 2000;226:185–8. doi: 10.1006/jcis.2000.6801.
    1. Fang HHP, Chan K-Y, Xu LC. Quantification of bacterial adhesion forces using atomic force microscopy (AFM) J Microbiol Methods. 2000;40:89–97. doi: 10.1016/S0167-7012(99)00137-2.
    1. Beech IB, Smith JR, Steele AA, Penegar I, Campbell SA. The use of atomic force microscopy for studying interactions of bacterial biofilms with surfaces. Coll Surf B: Biointerf. 2002;23:231–47. doi: 10.1016/S0927-7765(01)00233-8.
    1. Boyd RD, Verran J, Jones MV, Bhakoo M. Use of Atomic Force Microscope to determine the effect of substratum surface topography on bacterial adhesion. Langmuir. 2002;18:2343–6. doi: 10.1021/la011142p.
    1. Alonso JL, Goldmann WH. Feeling the forces: atomic force microscopy in cell biology. Life Sci. 2003;72:2553–60. doi: 10.1016/S0024-3205(03)00165-6.
    1. Dufrêne YF. Recent progress in the application of atomic force microscopy imaging and force spectroscopy to microbiology. Curr Opin Microbiol. 2003;6:317–23. doi: 10.1016/S1369-5274(03)00058-4.
    1. Sénéchal A, Carrigan SD, Tabrizian M. Probing surface adhesion forces of Enterococcus faecalis to medical-grade polymers using atomic force microscopy. Langmuir. 2004;20:4172–7. doi: 10.1021/la035847y.
    1. Krishna OD, Kim K, Byun Y. Covalently grafted phospholipid monolayer on silicone catheter surface for reduction in platelet adhesion. Biomaterials. 2005;26:7115–23. doi: 10.1016/j.biomaterials.2005.05.023.
    1. Churnside AB, King GM, Perkins TT. Label-free optical imaging of membrane patches for atomic force microscopy. Opt Express. 2010;18:23924–32. doi: 10.1364/OE.18.023924.
    1. Erukhimovitch V, Pavlov V, Talyshinsky M, Souprun Y, Huleihel M. FTIR microscopy as a method for identification of bacterial and fungal infections. J Pharm Biomed Anal. 2005;37:1105–8. doi: 10.1016/j.jpba.2004.08.010.
    1. Schmitt J, Flemming H. FTIR-spectroscopy in microbial and material analysis. Int Biodeterior Biodegradation. 1998;41:1–11. doi: 10.1016/S0964-8305(98)80002-4.
    1. Huang WE, Hopper D, Goodacre R, Beckmann M, Singer A, Draper J. Rapid characterization of microbial biodegradation pathways by FT-IR spectroscopy. J Microbiol Methods. 2006;67:273–80. doi: 10.1016/j.mimet.2006.04.009.
    1. Amiali NM, Mulvey MR, Sedman J, Louie M, Simor AE, Ismail AA. Rapid identification of coagulase-negative staphylococci by Fourier transform infrared spectroscopy. J Microbiol Methods. 2007;68:236–42. doi: 10.1016/j.mimet.2006.08.010.
    1. Amiali NM, Mulvey MR, Sedman J, Simor AE, Ismail AA. Epidemiological typing of methicillin-resistant Staphylococcus aureus strains by Fourier transform infrared spectroscopy. J Microbiol Methods. 2007;69:146–53. doi: 10.1016/j.mimet.2006.12.022.
    1. Lin M, Al-Holy M, Chang SS, Huang Y, Cavinato AG, Kang DH, et al. Rapid discrimination of Alicyclobacillus strains in apple juice by Fourier transform infrared spectroscopy. Int J Food Microbiol. 2005;105:369–76. doi: 10.1016/j.ijfoodmicro.2005.04.018.
    1. Goodacre R, Shann B, Gilbert RJ, Timmins EM, McGovern AC, Alsberg BK, et al. Detection of the dipicolinic acid biomarker in Bacillus spores using Curie-point pyrolysis mass spectrometry and Fourier transform infrared spectroscopy. Anal Chem. 2000;72:119–27. doi: 10.1021/ac990661i.
    1. Helm D, Labischinski H, Schallehn G, Naumann D. Classification and identification of bacteria by Fourier-transform infrared spectroscopy. J Gen Microbiol. 1991;137:69–79. doi: 10.1099/00221287-137-1-69.
    1. Maquelin K, Kirschner C, Choo-Smith LP, Ngo-Thi NA, van Vreeswijk T, Stämmler M, et al. Prospective study of the performance of vibrational spectroscopies for rapid identification of bacterial and fungal pathogens recovered from blood cultures. J Clin Microbiol. 2003;41:324–9. doi: 10.1128/JCM.41.1.324-329.2003.
    1. Ofek I, Hasty DL, Doyle RJ. Methodological Approaches to Analysis of Adhesins and Adhesion. In: Ofek I, Hasty DL, Doyle RJ, eds. Bacterial Adhesion to Animal Cells and Tissues. Washington, DC: ASM Press, 2003:19-40.
    1. Timmerman CP, Fleer A, Besnier JM, De Graaf L, Cremers F, Verhoef J. Characterization of a proteinaceous adhesin of Staphylococcus epidermidis which mediates attachment to polystyrene. Infect Immun. 1991;59:4187–92.
    1. Ahimou F, Paquot M, Jacques P, Thonart P, Rouxhet PG. Influence of electrical properties on the evaluation of the surface hydrophobicity of Bacillus subtilis. J Microbiol Methods. 2001;45:119–26. doi: 10.1016/S0167-7012(01)00240-8.
    1. Castonguay MH, van der Schaaf S, Koester W, Krooneman J, van der Meer W, Harmsen H, et al. Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Res Microbiol. 2006;157:471–8. doi: 10.1016/j.resmic.2005.10.003.
    1. Li X, Yan Z, Xu J. Quantitative variation of biofilms among strains in natural populations of Candida albicans. Microbiology. 2003;149:353–62. doi: 10.1099/mic.0.25932-0.
    1. Pitts B, Hamilton MA, Zelver N, Stewart PS. A microtiter-plate screening method for biofilm disinfection and removal. J Microbiol Methods. 2003;54:269–76. doi: 10.1016/S0167-7012(03)00034-4.
    1. Boulos L, Prévost M, Barbeau B, Coallier J, Desjardins R. LIVE/DEAD BacLight : application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J Microbiol Methods. 1999;37:77–86. doi: 10.1016/S0167-7012(99)00048-2.
    1. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science. 2002;295:1487. doi: 10.1126/science.295.5559.1487.
    1. Strathmann M, Wingender J, Flemming HC. Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa. J Microbiol Methods. 2002;50:237–48. doi: 10.1016/S0167-7012(02)00032-5.
    1. Honraet K, Goetghebeur E, Nelis HJ. Comparison of three assays for the quantification of Candida biomass in suspension and CDC reactor grown biofilms. J Microbiol Methods. 2005;63:287–95. doi: 10.1016/j.mimet.2005.03.014.
    1. Honraet K, Nelis HJ. Use of the modified robbins device and fluorescent staining to screen plant extracts for the inhibition of S. mutans biofilm formation. J Microbiol Methods. 2006;64:217–24. doi: 10.1016/j.mimet.2005.05.005.
    1. Sarker SD, Nahar L, Kumarasamy Y. Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods. 2007;42:321–4. doi: 10.1016/j.ymeth.2007.01.006.
    1. O’Brien J, Wilson I, Orton T, Pognan F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem. 2000;267:5421–6. doi: 10.1046/j.1432-1327.2000.01606.x.
    1. Pettit RK, Weber CA, Kean MJ, Hoffmann H, Pettit GR, Tan R, et al. Microplate Alamar blue assay for Staphylococcus epidermidis biofilm susceptibility testing. Antimicrob Agents Chemother. 2005;49:2612–7. doi: 10.1128/AAC.49.7.2612-2617.2005.
    1. Unosson E, Cai Y, Jiang X, Lööf J, Welch K, Engqvist H. Antibacterial properties of dental luting agents: potential to hinder the development of secondary caries. Int J Dent. 2012;2012:529495. doi: 10.1155/2012/529495.
    1. Prieto B, Silva B, Lantes O. Biofilm quantification on stone surfaces: comparison of various methods. Sci Total Environ. 2004;333:1–7. doi: 10.1016/j.scitotenv.2004.05.003.

Source: PubMed

3
Iratkozz fel