Bone-implant interface in biofilm-associated bone and joint infections

Bone-Implant Interface in Orthopedic Surgery: Basic Science to Clinical Applications

Volumn 9781447154099, Issue , 2014, Pages 239-253

  Malizos, Konstantinos N ^a   Ioannou, Maria ^a  

^a UNIVERSITY OF THESSALY   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; HYDROXYAPATITE; JOINTS (ANATOMY); METAL IMPLANTS; ORTHOPEDICS;

ARTHRITIC JOINTS; BONE-IMPLANT INTERFACES; FUNCTIONAL DISABILITIES; HIP AND KNEES; OVERALL QUALITY; QUALITY OF LIFE; TOTAL HIP ARTHROPLASTY; TOTAL KNEE ARTHROPLASTY; TRAUMATOLOGY; TWENTIETH CENTURY;

BIOCOMPATIBILITY;

EID: 84935895344     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4471-5409-9_17     Document Type: Chapter

References (125)

1. http://marketsandmarkets.wordpress.com/2009/08/29/biomaterials-find-wide-usage-in-the-medical-devicesindustry
2. Williams DF. On the mechanisms of biocompatibility. Biomaterials. 2008;29:2941-53.
3. Athanasou NA. Peri-implant pathology-relation to implant failure and tumor formation. J Long Term Eff Med Implants. 2007;17(3):193-206.
4. Morawietz L, Classen RA, Schroeder JH, Dynybil C, Perka C, Skwara A, Neidel J, Gehrke T, Frommelt L, Hansen T, Otto M, Barden B, Aigner T, Stiehl P, Schubert T, Meyer-Scholten C, Konig A, Strobel P, Rader CP, Kirschner S, Lintner F, Ruther W, Bos I, Hendrich C, Kriegsmann J, Krenn V. Proposal for a histopathological consensus classification of the periprosthetic interface membrane. J Clin Pathol. 2006;59:591-7.
5. Rand JA, Morrey BF, Bryan RS. Management of the infected total joint arthroplasty. J Bone Joint Surg Am. 1983;64A:491-504.
6. Lew DP, Waldvogel FA. Osteomyelitis. N Engl J Med. 1997;363:999-1007.
7. Tsukayama DT. Pathophysiology of posttraumatic osteomyelitis. Clin Orthop. 1999;360:22-9.
8. Ehrlich GD, Hu FZ, Lin Q, Costerton JW, Post JC. Intelligent implants to battle biofilms. ASM News. 2004;70:127-33.
9. Gustillo RB, Anderson JT. Prevention of infection in the treatment of 1025 open fractures of long bones: retrospective and prospective analysis. J Bone Joint Surg Am. 1976;58A:453-8.
10. Schmidt AH, Swiontkowski MF. Pathophysiology of infections after internal fixations of fractures. J Am Acad Orthop Surg. 2000;8:285-91.
11. Fluckiger U, Zimmerli W. Factors influencing antimicrobial therapy of surface adhering microorganisms. Recent Res Devel Antimicrob Agents Chemother. 2000;4:165-75.
12. Gristina AG. Biomaterial-centered infection: microbial adhesion versus tissue integration. Science. 1987;237(4822):1588-95.
13. Campoccia D, Montanaro L, Arciola CR. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials. 2006; 27(11):2331-9.
14. Creech 2nd CB, Kernodle DS, Alsentzer A, Wilson C, Edwards KM. Increasing rates of nasal carriage of methicillin-resistant Staphylococcus aureus in healthy children. Pediatr Infect Dis J. 2005;24:617-21.
15. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5:751-62.
16. Frebourg NB, Cauliez B, Lemeland JF. Evidence for nasal carriage of methicillin-resistant staphylococci colonizing intravascular devices. J Clin Microbiol. 1999;37:1182-5.
17. Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity. 2006; 24:19-28.
18. Stroh P, Günther F, Meyle E, Prior B, Wagner C, Hänsch GM. Host defence against Staphylococcus aureus biofilms by polymorphonuclear neutrophils: oxygen radical production but not phagocytosis depends on opsonisation with immunoglobulin G. Immunobiology. 2011;216(3):351-7.
19. Kubes P, Ward PA. The leukocyte recruitment and the acute inflammatory response. Brain Pathol. 2000; 10:127-35.
20. Rubin RH, Ferraro MJ. Understanding and diagnosing infectious complications in the immunocompromised host. Current issues and trends. Hematol Oncol Clin North Am. 1993;7:795-812.
21. Takagi J, Springer TA. Integrin activation and structural rearrangement. Immunol Rev. 2000;186:141-63.
22. Kaplanski G, Marin V, Montero-Julian F, Mantovani A, Farnarier C. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol. 2003;24:47-52.
23. Savill J. Apoptosis in resolution of inflammation. J Leukoc Biol. 1997;61:375-80.
24. Sendo F, Tsuchida H, Takeda Y. Regulation of neutrophil apoptosis - its biological significance in inflammation and the immune response. Hum Cell. 1999;9:215-22.
25. Kobayashi SD, Voyich JM, Buhl CL, Stahl RM, DeLeo FR. Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression. Proc Natl Acad Sci U S A. 2002;99:6901-6.
26. Savill J, Wyllie AH, Henson JE, Walport MJ, Henson PM, Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest. 1989;83:865-75.
27. Watnik P, Kolter R. Biofilm, City of microbes. J Bacteriol. 2000;182:2675-9.
28. Davey ME, O'Toole GA. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev. 2000;64:847-67.
29. Dunne WM. Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev. 2002;15:155-66.
30. Arciola CR, Campoccia D, Gamberini S, Donati ME, Baldassarri L, Montanaro L. Occurrence of ica genes for slime synthesis in a collection of Staphylococcus epidermis strains from orthopedic prosthesis infections. Acta Orthop Scand. 2003;74:617-21.
31. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. The involvement of cellto-cell signals in the development of a bacterial biofilm. Science. 1998;280:295-8.
32. Rice KC, Firek BA, Nelson JB, Yang SJ, Patton TG, Bayles KW. The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J Bacteriol. 2003;185:2635-43.
33. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135-8.
34. Costerton JW, Montanaro L, Arciola CR. Biofilm in implant infections: its production and regulation. Int J Artif Organs. 2005;28(11):1062-8.
35. Høiby N, Ciofu O, Johansen HK, Song ZJ, Moser C, Jensen PØ, Molin S, Givskov M, Tolker-Nielsen T, Bjarnsholt T. The clinical impact of bacterial biofilms. Int J Oral Sci. 2011;3(2):55-65.
36. Arciola CR, Campoccia D, Gamberini S, Donati ME, Pirini V, Visai L, Speziale P, Montanaro L. Antibiotic resistance in exopolysaccharide-forming Staphylococcus epidermidis clinical isolates from orthopaedic implant infections. Biomaterials. 2005;26(33):6530-5.
37. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318-22.
38. Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol. 2005;13(1):34-40.
39. Montanaro L, Testoni F, Poggi A, Visai L, Speziale P, Arciola CR. Emerging pathogenetic mechanisms of the implant-related osteomyelitis by Staphylococcus aureus. Int J Artif Organs. 2011;34(9):781-8.
40. Petty W, Spanier S, Shuster JJ, Silverthorne C. The influence of skeletal implants on incidence of infection. Experiments in a canine model. J Bone Joint Surg Am. 1985;67:1236-44.
41. Barth E, Myrvik QM, Wagner W, Gristina AG. In vitro and in vivo comparative colonization of Staphylococcus aureus and Staphylococcus epidermidis on orthopaedic implant materials. Biomaterials. 1989;10(5):325-8.
42. Wassall MA, Santin M, Isalberti C, Cannas M, Denyer SP. Adhesion of bacteria to stainless steel and silvercoated orthopedic external fixation pins. J Biomed Mater Res. 1997;36(3):325-30.
43. Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339(8):520-32.
44. http://www.eurekalert.org/pub-releases/2011-01/hu-apb010711.php
45. Donlan RM. Biofilms and device-associated infections. Emerg Infect Dis. 2001;7:277-81.
46. Wagner C, Obst U, Hänsch GM. The implantassociated posttraumatic osteomyelitis: collateral damage by the local host defence? Int J Artif Organs. 2005;28(11):1172-80.
47. Gristina AG, Costerton JW. Bacterial adherence and the glycocalyx and their role in musculoskeletal infection. Orthop Clin North Am. 1984;15(3):517-35.
48. Marrie TJ, Costerton JW. Mode of growth of bacterial pathogens in chronic polymicrobial human osteomyelitis. J Clin Microbiol. 1985;22(6):924-33.
49. Gristina AG, Costerton JW. Bacterial adherence to biomaterials and tissue. The significance of its role in clinical sepsis. J Bone Joint Surg Am. 1985;67A:264-73.
50. Wagner C, Kondella K, Bernschneider T, Heppert V, Wentzensen A, Hänsch GM. Post traumatic osteitis: analysis of inflammatory cells recruited into the site of infection. Shock. 2003;20(6):503-10.
51. Wagner C, Kaksa A, Müller W, Denefleh B, Heppert V, Wentzensen A, Hänsch GM. Polymorphonuclear neutrophils in posttraumatic osteomyelitis: cells recovered from the inflamed site lack chemotactic activity but generate superoxides. Shock. 2004;22:108-15.
52. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature. 2007;449(7164):819-26.
53. Janeway Jr CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002;20:197-216.
54. Verbrugh HA. Phagocytosis and destruction of Staphylococcus aureus. Vet Q. 1981;3(2):91-7.
55. Arciola CR. Host defense against implant infection: the ambivalent role of phagocytosis. Int J Artif Organs. 2010;33(9):565-77.
56. Meyle E, Stroh P, Günther F, Hoppy-Tichy T, Wagner C, Hänsch GM. Destruction of bacterial biofilms by polymorphonuclear neutrophils: relative contribution of phagocytosis, DNA release, and degranulation. Int J Artif Organs. 2010;33(9):608-20.
57. Guenther F, Stroh P, Wagner C, Obst U, Hänsch GM. Phagocytosis of staphylococci biofilms by polymorphonuclear neutrophils: S. aureus and S. epidermidis differ with regard to their susceptibility towards the host defense. Int J Artif Organs. 2009; 32(9):565-73.
58. Bettin D, Härle A. Die diagnostische Wertigkeit der Labor- und Wundsekretanalyse zur Erkennung einer latenten Frühinfektion in der Endoprothetik. Das infizierte Implantat Kongressband 7. Berlin: Steglitzer Unfalltagung; 1988.p. 50-6.
59. Bettin D, Härle A. The diagnostic value of wound secretion analysis. Z Orthop Ihre Grenzgeb. 1989;127(4):518-21.
60. Verschoor CP, Puchta A, Bowdish DM. The macrophage. Methods Mol Biol. 2012;844:139-56.
61. Gordon S. The macrophage: past, present and future. Eur J Immunol. 2007;37(S1):9-17.
62. Haynes DR, Crotti TN, Potter AE, Loric M, Atkins GJ, Howie DW, Findlay DM. The osteoclastogenic molecules RANKL and RANK are associated with periprosthetic osteolysis. J Bone Joint Surg Br. 2001;38B:902-11.
63. Del Fattore A, Teti A. The tight relationship between osteoclasts and the immune system. Inflamm Allergy Drug Targets. 2012;11(3):181-7.
64. Otto M. Molecular basis of Staphylococcus epidermidis infections. Semin Immunopathol. 2012;34(2):201-14.
65. Horowitz MC, Lorenzo JA. The origins of osteoclasts. Curr Opin Rheumatol. 2004;16:456-64.
66. Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature. 2003;423:337-42.
67. Kudo O, Fujikawa Y, Itonaga I, Sabokbar A, Torisu T, Athanasou NA. Proinflammatory cytokine (TNFalpha/IL-1 alpha) induction of human osteoclast formation. J Pathol. 2002;198:220-7.
68. Theill LE, Boyle WJ, Penninger JM. RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu Rev Immunol. 2002;20:795-823.
69. Nair SP, Meghji S, Wilson M, Krisanavane R, White P, Henderson B. Bacterially induced bone destruction: mechanisms and misconceptions. Infect Immun. 1996;64:2371-80.
70. Hendersen B, Nair SP. Hard labour: bacterial infection of the skeleton. Trends Microbiol. 2003;11:570-7.
71. Goldring SR. Inflammatory mediators as essential elements in bone remodeling. Calcif Tissue Int. 2003;73:97-100.
72. Walsh NC, Gravellese EM. Bone loss in inflammatory arthritis: mechanisms and treatment strategies. Curr Opin Rheumatol. 2004;16:419-27.
73. McCarthy EF, Frassica FJ. The pathology of failed total joint arthroplasty. In: Pathology of bone and joint disorders with clinical and radiographic correlation. Philadelphia: WB Saunders; 1998. p. 353-63.
74. Colliers JP, Bauer TW, Bloebaum RD, Bobyn JD, Cook SD, Galante JO, Harris WH, Head WC, Jasty MJ, Mayer MB, Sumner DR, Whiteside LA. Results of implant retrieval from postmortem specimens in patients with well-functioning, long-term total hip replacement. Clin Orthop. 1992;274:97-112.
75. Wright TM, Goodman SB, editors. Implant wear in total joint replacement. Rosemont: AAOS; 2001.
76. Krohmer G, Koleganova N, Hadjicostas PT, Fink B, Berger I. Degenerative changes in the interface membrane as a possible reason for prosthesis loosening. Histol Histopathol. 2008;23:925-33.
77. Müller M, Morawietz L, Hasart O, Strube P, Perka C, Tohtz S. Diagnosis of periprosthetic infection following total hip arthroplasty - evaluation of the diagnostic values of pre- and intraoperative parameters and the associated strategy to preoperatively select patients with a high probability of joint infection. J Orthop Surg Res. 2008;3:31-8.
78. Bori G, Munoz-Mahamud E, Garcia S, Mallofre C, Gallart X, Bosch J, Garcia E, Riba J, Mensa J, Soriano A. Interface membrane is the best sample for histological study to diagnose prosthetic joint infection. Mod Pathol. 2011;24:579-894.
79. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol. 1995;49:711-45.
80. Marion K, Pasmore M, Freney J, Delawari E, Renaud F, Costerton JW, Traeger J. A new procedure allowing the complete removal and prevention of hemodialysis biofilms. Blood Purif. 2005;23(5):339-48.
81. Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell densityresponsive transcriptional regulators. J Bacteriol. 1994;76(2):269-75.
82. Balaban N, Goldkorn T, Nhan RT, Dang LB, Scott S, Ridgley RM, Rasooly A, Wright SC, Larrick JW, Rasooly R, Carlsonet JR. Autoinducer of virulence as a target for vaccine and therapy against Staphylococcus aureus. Science. 1998;280(5362):438-40.
83. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, Manefield M, Costerton JW, Molin S, Eber L, Steinberg P, Kjelleberg S, Høiby N, Givskov M. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 2003;22(15):3803-15.
84. De Nys R, Givskov M, Kumar N, Kjelleberg S, Steinberg PD. Furanones. Prog Mol Subcell Biol. 2006;42:55-86.
85. Balaban N, Giacometti A, Cirioni O, Gov Y, Ghiselli R, Mocchegiani F, Viticchi C, Del Prete MS, Saba V, Scalise G, Dell'Acqua G. Use of the quorumsensing inhibitor RNAIII inhibiting peptide to prevent biofilm formation in vivo by drug-resistant Staphylococcus epidermidis. J Infect Dis. 2003; 187(4):625-30.
86. Balaban N, Stoodley P, Fux CA, Wilson S, Costerton JW, Dell'Acqua G. Prevention of staphylococcal biofilm-associated infections by the quorum sensing inhibitor RIP. Clin Orthop. 2005;437:48-54.
87. Balaban N, Gov Y, Bitler A, Boelaert JR. Prevention of Staphylococcus aureus biofilm on dialysis catheters and adherence to human cells. Kidney Int. 2003; 63(1):340-5.
88. Giacometti A, Cirioni O, Ghiselli R, Dell'Acqua G, Orlando F, D'Amato G, Mocchegiani F, Silvestri C, Del Prete MS, Rocchi M, Balaban N, Saba V, Scalise G. RNAIII-inhibiting peptide improves efficacy of clinically used antibiotics in a murine model of staphylococcal sepsis. Peptides. 2005; 26(2):169-75.
89. Arciola CR, Radin L, Alvergna P, Cenni E, Pizzoferrato A. Heparin surface treatment of poly(methylmethacrylate) alters adhesion of a Staphylococcus aureus strain: utility of bacterial fatty acid analysis. Biomaterials. 1993; 14(15):1161-4.
90. Arciola CR, Caramazza R, Pizzoferrato A. In vitro adhesion of Staphylococcus epidermidis on heparinsurface-modified intraocular lenses. J Cataract Refract Surg. 1994;20(2):58-61.
91. Arciola CR, Bustanji Y, Conti M, Campoccia D, Baldassarri L, Samorì B, Montanaro L. Staphylococcus epidermidis-fibronectin binding and its inhibition by heparin. Biomaterials. 2003;24(18):3013-9.
92. Schildhauer TA, Peter E, Muhr G, Köller M. Activation of human leukocytes on tantalum trabecular metal in comparison to commonly used orthopedic metal implant materials. J Biomed Mater Res A. 1999;88(2):332-41.
93. Rozalska B, Sadowska B, Ljungh A, Rudnicka W. Granulocyte-macrophage colony-stimulating factor (GM-CSF)-coated implants and their potential for reducing biomaterial-associated infection in neutropenic hosts. Zentralbl Bakteriol. 1998;288(2):237-51.
94. Bai X, Zhang C, Ruan D, He Q, Hou L, Li H. Recombinant human granulocyte colony-stimulating factor (rhG-CSF) could be an effective adjuvant therapy for orthopedic implant-related infections (OIRI). Med Hypotheses. 2011;76(5):703-5.
95. Simbirtsev A, Variouchina E, Konusova V, Kotov A, Ketlinsky S, Salamatov A, Bisenkov L. Local administration of interleukin-1beta for the treatment of lung abscesses induces neutrophil activation and changes in proinflammation cytokine production. Eur Cytokine Netw. 2001;12(3):420-9.
96. Kaplan SS, Simmons RL. Effect of plasma and matrix proteins on defensin-induced impairment of phagocytic killing by adherent neutrophils. J Biomed Mater Res. 2001;57(1):1-7.
97. Kreyden OP, Hafner J, Burg G, Nestle FO. Case report on therapy with granulocyte stimulating factor in diabetic foot. Hautarzt. 2001;52(4):327-30.
98. Zalavras CG, Patzakis MJ, Holtom P. Local antibiotic therapy in the treatment of open fractures and osteomyelitis. Clin Orthop. 2004;427:86-93.
99. Norris P, Noble M, Francolini I, Vinogradov AM, Stewart PS, Ratner BD, Costerton JW, Stoodley P. Ultrasonically controlled release of ciprofloxacin from self-assembled coatings on poly(2-hydroxyethyl methacrylate) hydrogels for Pseudomonas aeruginosa biofilm prevention. Antimicrob Agents Chemother. 2005;49(10):4272-9.
100. Neoh KG, Kang ET. Combating bacterial colonization on metals via polymer coatings: relevance to marine and medical applications. ACS Appl Mater Interfaces. 2011;3(8):2808-19.
101. Tan H, Peng Z, Li Q, Xu X, Guo S, Tang T. The use of quaternised chitosan-loaded PMMA to inhibit biofilm formation and downregulate the virulenceassociated gene expression of antibiotic-resistant Staphylococcus. Biomaterials. 2012;33:365-77.
102. Schwandt LQ, van Weissenbruch R, Stokroos I, Van der Mei HC, Busscher HJ, Albers FW. Prevention of biofilm formation by dairy products and N-acetylcysteine on voice prostheses in an artificial throat. Acta Otolaryngol. 2004;124:726-31.
103. Aslam S, Darouiche RO. Role of antibiofilm-antimicrobial agents in controlling device-related infections. Int J Artif Organs. 2011;34(9):752-8.
104. Fu J, Ji J, Yuan W, Shen J. Construction of anti-adhesive and antibacterial multilayer films via layer-by-layer assembly of heparin and chitosan. Biomaterials. 2005;26(33):6684-92.
105. Campoccia D, Montanaro L, Speziale P, Arciola CR. Antibiotic-loaded biomaterials and the risks for the spread of antibiotic resistance following their prophylactic and therapeutic clinical use. Biomaterials. 2010;31:6363-77.
106. Kang SJ, Kim DH, Mishig-Ochir T, Lee BJ. Antimicrobial peptides: their physicochemical properties and therapeutic application. Arch Pharm Res. 2012;35(3):409-13.
107. Gruenheid S, Le Moual H. Resistance to antimicrobial peptides in Gram negative bacteria. FEMS Microbiol Lett. 2012;330:81-9.
108. Bagheri M, Beyermann M, Dathe M. Immobilization reduces the activity of surface-bound cationic antimicrobial peptides with no influence upon the activity spectrum. Antimicrob Agents Chemother. 2009;53(3):1132-41.
109. Arciola CR, Montanaro L, Moroni A, Giordano M, Pizzoferrato A, Donati ME. Hydroxyapatite-coated orthopaedic screws as infection resistant materials: in vitro study. Biomaterials. 1999;20(4):323-7.
110. Campoccia D, Arciola CR, Cervellati M, Maltarello MC, Montanaro L. In vitro behaviour of bone marrow-derived mesenchymal cells cultured on fluorohydroxyapatite-coated substrata with different roughness. Biomaterials. 2003;24:587-96.
111. Schaer TP, Stewart S, Hsu BB, Klibanov AM. Hydrophobic polycationic coatings that inhibit biofilms and support bone healing during infection. Biomaterials. 2012;33:1245-54.
112. Grandi S, Cassinelli V, Bini M, Saino E, Mustarelli P, Arciola CR, Imbriani M, Visai L. Bone reconstruction: Au nanocomposite bioglasses with antibacterial properties. Int J Artif Organs. 2011; 34(9):920-8.
113. Kurek A, Grudniak AM, Kraczkiewicz-Dowjat A, Wolska KI. New antibacterial therapeutics and strategies. Pol J Microbiol. 2011;60:3-12.
114. Wu P, Xie R, Imlay K, Shang JK. Visible-lightinduced bactericidal activity of titanium dioxide codoped with nitrogen and silver. Environ Sci Technol. 2010;44:6992-7.
115. Visai L, De Nardo L, Punta C, Melone L, Cigada A, Imbriani M, Arciola CR. Titanium oxide antibacterial surfaces in biomedical devices. Int J Artif Organs. 2011;34(9):929-46.
116. Montanaro L, Campoccia D, Arciola CR. Advancements in molecular epidemiology of implant infections and future perspectives. Biomaterials. 2007;28(34):5155-68.
117. Rupp ME, Ulphani JS, Fey PD, Mack D. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheterassociated infection in a rat model. Infect Immun. 1999;67(5):2656-9.
118. Rupp ME, Fey PD, Heilmann C, Götz F. Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J Infect Dis. 2001;183(7):1038-42.
119. An YH, Kang QK, Arciola CR. Animal models of osteomyelitis. Int J Artif Organs. 2006;29(4):407-20.
120. Costerton JW. Biofilm theory can guide the treatment of device-related orthopaedic infections. Clin Orthop. 2005;437:7-11.
121. Costerton JW, Post JC, Ehrlich GD, Hu FZ, Kreft R, Nistico L, Kathju S, Stoodley P, Hall-Stoodley L, Maale G, James G, Sotereanos N, DeMeo P. New methods for the detection of orthopedic and other biofilm infections. FEMS Immunol Med Microbiol. 2011;61(2):133-40.
122. Mack D, Becker P, Chatterjee I, Dobinsky S, Knobloch JK, Peters G, Rohde H, Herrmann M. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol. 2004; 294(2-3):203-12.
123. 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.
124. Arciola CR, Montanaro L, Costerton JW. New trends in diagnosis and control strategies for implant infections. Int J Artif Organs. 2011;34(9):727-36.
125. Brady RA, O'May GA, Leid JG, Prior ML, Costerton JW, Shirtliff ME. Resolution of Staphylococcus aureus biofilm infection using vaccination and antibiotic treatment. Infect Immun. 2011; 79:1797-803.