Bridging the Gap Between In Vitro and In Vivo Evaluation of Biomaterial-Associated Infections

  • Guruprakash Subbiahdoss
  • Joana F. da Silva Domingues
  • Roel Kuijer
  • Henny C. van der Mei
  • Henk J. Busscher
Chapter

Abstract

Biomaterial-associated infections constitute a major clinical problem that is difficult to treat and often necessitates implant replacement. Pathogens can be introduced on an implant surface during surgery or postoperative and compete with host cells attempting to integrate the implant. The fate of a biomaterial implant has been depicted as a race between bacterial adhesion and biofilm growth on an implant surface versus tissue integration. Until today, in vitro studies on infection risks of biomaterials or functional coatings for orthopedic and dental implants were performed either for their ability to resist bacterial adhesion or for their ability to support mammalian cell adhesion and proliferation. Even though the concept of the race for the surface in biomaterial-associated infections has been intensively studied before in vivo, until recently no in vitro methodology existed for this purpose. Just very recently various groups have proposed coculture experiments to evaluate the simultaneous response of bacteria and mammalian cells on a surface. As an initial step towards bridging the gap between in vitro and in vivo evaluations of biomaterials, we here describe bi- and tri-culture experiments that allow better evaluation of multifunctional coatings in vitro and therewith bridge the gap between in vitro and in vivo studies.

Keywords

Migration Catheter Hydrated Pneumonia Chitosan 

References

  1. 1.
    Hebert CK, Williams RE, Levy RS, Barrack RL. Cost of treating an infected total knee replacement. Clin Orthop Relat Res. 1996;331:140–5.CrossRefGoogle Scholar
  2. 2.
    Campoccia D, Montanaro L, Arciola CR. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials. 2006;27:2331–9.CrossRefGoogle Scholar
  3. 3.
    Trampuz A, Zimmerli W. New strategies for the treatment of infections associated with prosthetic joints. Curr Opin Investig Drugs. 2005;6:185–90.Google Scholar
  4. 4.
    Calhoun JH, Klemm K, Anger DM, Mader JT. Use of antibiotic-PMMA beads in the ischemic foot. Orthopedics. 1994;17:453–7.Google Scholar
  5. 5.
    Darouiche RO. Treatment of infections associated with surgical implants. N Engl J Med. 2004;350:1422–9.CrossRefGoogle Scholar
  6. 6.
    Mohr VD, Eickhoff U, Haaker R, Klammer HL. External fixation of open femoral shaft fractures. J Trauma. 1995;38:648–52.CrossRefGoogle Scholar
  7. 7.
    Costerton JW. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–22.CrossRefGoogle Scholar
  8. 8.
    Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15:167–93.CrossRefGoogle Scholar
  9. 9.
    Gristina AG, Naylor PT, Myrvik QN. Musculoskeletal infection, microbial adhesion, and antibiotic resistance. Infect Dis Clin North Am. 1990;4:391–408.Google Scholar
  10. 10.
    Gristina AG. Biomaterial-centered infection: microbial adhesion versus tissue integration. Science. 1987;237:1588–95.CrossRefGoogle Scholar
  11. 11.
    Ahlberg A, Carlsson AS, Lindberg L. Hematogenous infection in total joint replacement. Clin Orthop Relat Res. 1978;137:69–75.Google Scholar
  12. 12.
    Lidwell OM, Lowbury EJ, Whyte W, Blowers R, Stanley SJ, Lowe D. Airborne contamination of wounds in joint replacement operations: the relationship to sepsis rates. J Hosp Infect. 1983;4:111–31.CrossRefGoogle Scholar
  13. 13.
    Fitzgerald RH. Microbiologic environment of the conventional operating-room. Arch Surg. 1979;114:772–5.CrossRefGoogle Scholar
  14. 14.
    Verkkala K, Eklund A, Ojajarvi J, Tiittanen L, Hoborn J, Makela P. The conventionally ventilated operating theatre and air contamination control during cardiac surgery—bacteriological and particulate matter control garment options for low level contamination. Eur J Cardiothorac Surg. 1998;14:206–10.CrossRefGoogle Scholar
  15. 15.
    Wells CL, Maddaus MA, Simmons RL. Role of the macrophage in the translocation of intestinal bacteria. Arch Surg. 1987;122:48–53.CrossRefGoogle Scholar
  16. 16.
    Guo W, Andersson R, Ljungh A, Wang XD, Bengmark S. Enteric bacterial translocation after intraperitoneal implantation of rubber drain pieces. Scand J Gastroenterol. 1993;28:393–400.CrossRefGoogle Scholar
  17. 17.
    Okell CC, Elliott CD. Bacteriaemia and oral sepsis with special reference to the etiology of subacute endocarditis. Lancet. 1935;2:869–75.CrossRefGoogle Scholar
  18. 18.
    Ohara-Nemoto Y, Haraga H, Kimura S, Nemoto TK. Occurrence of staphylococci in the oral cavities of healthy adults and nasal-oral trafficking of the bacteria. J Med Microbiol. 2008;57:95–9.CrossRefGoogle Scholar
  19. 19.
    Gristina AG. Implant failure and the immune-incompetent fibro-inflammatory zone. Clin Orthop Relat Res. 1994;298:106–18.Google Scholar
  20. 20.
    Khalil H, Williams RJ, Stenbeck G, Henderson B, Meghji S, Nair SP. Invasion of bone cells by Staphylococcus epidermidis. Microbes Infect. 2007;9:460–5.CrossRefGoogle Scholar
  21. 21.
    Van Delden C, Iglewski BH. Cell-to-cell signalling and Pseudomonas aeruginosa infections. Emerg Infect Dis. 1998;4:551–60.CrossRefGoogle Scholar
  22. 22.
    Robinson DA, Enright MC. Multilocus sequence typing and the evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect. 2004;10:92–7.CrossRefGoogle Scholar
  23. 23.
    Zimmerli W, Trampuz A, Ochsner PE. Current concepts: prosthetic-joint infections. N Engl J Med. 2004;351:1645–54.CrossRefGoogle Scholar
  24. 24.
    Massey RC, Horsburgh MJ, Lina G, Hook M, Recker M. Opinion - the evolution and maintenance of virulence in Staphylococcus aureus: a role for host-to-host transmission? Nat Rev Microbiol. 2006;4:953–8.CrossRefGoogle Scholar
  25. 25.
    Mckevitt AI, Bjornson GL, Mauracher CA, Scheifele DW. Amino-acid-sequence of a deltalike toxin from Staphylococcus epidermidis. Infect Immun. 1990;58:1473–5.Google Scholar
  26. 26.
    Raad I, Alrahwan A, Rolston K. Staphylococcus epidermidis: emerging resistance and need for alternative agents. Clin Infect Dis. 1998;26:1182–7.CrossRefGoogle Scholar
  27. 27.
    Vuong C, Otto M. Staphylococcus epidermidis infections. Microbes Infect. 2002;4:481–9.CrossRefGoogle Scholar
  28. 28.
    Ratner BD, Bryant SJ. Biomaterials: where we have been and where we are going. Annu Rev Biomed Eng. 2004;6:41–75.CrossRefGoogle Scholar
  29. 29.
    Lebaron RG, Athanasiou KA. Extracellular matrix cell adhesion peptides: functional applications in orthopedic materials. Tissue Eng. 2000;6:85–103.CrossRefGoogle Scholar
  30. 30.
    Schuler M, Owen GR, Hamilton DW, De Wilde M, Textor M, Brunette DM, Tosatti SGP. Biomimetic modification of titanium dental implant model surfaces using the RGDSP-peptide sequence: a cell morphology study. Biomaterials. 2006;27:4003–15.CrossRefGoogle Scholar
  31. 31.
    VandeVondele S, Voros J, Hubbell JA. RGD-Grafted poly-l-lysine-graft-(polyethylene glycol) copolymers block non-specific protein adsorption while promoting cell adhesion. Biotechnol Bioeng. 2003;82:784–90.CrossRefGoogle Scholar
  32. 32.
    Shi ZL, Neoh KG, Kang ET, Poh C, Wang W. Bacterial adhesion and osteoblast function on titanium with surface-grafted chitosan and immobilized RGD peptide. J Biomed Mater Res A. 2008;86A:865–72.CrossRefGoogle Scholar
  33. 33.
    Shi Z, Neoh KG, Kang ET, Poh C, Wang W. Titanium with surface-grafted dextran and immobilized bone morphogenetic protein-2 for inhibition of bacterial adhesion and enhancement of osteoblast functions. Tissue Eng Part A. 2009;15:417–26.CrossRefGoogle Scholar
  34. 34.
    Dexter SJ, Pearson RG, Davies MC, Camara M, Shakesheff KM. A comparison of the adhesion of mammalian cells and Staphylococcus epidermidis on fibronectin-modified polymer surfaces. J Biomed Mater Res. 2001;56:222–7.CrossRefGoogle Scholar
  35. 35.
    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.CrossRefGoogle Scholar
  36. 36.
    Maddikeri RR, Tosatti S, Schuler M, Chessari S, Textor M, Richards RG, Harris LG. Reduced medical infection related bacterial strains adhesion on bioactive RGD modified titanium surfaces: a first step toward cell selective surfaces. J Biomed Mater Res A. 2008;84A:425–35.CrossRefGoogle Scholar
  37. 37.
    Ploux L, Anselme K, Dirani A, Ponche A, Soppera O, Roucoules V. Opposite responses of cells and bacteria to micro/nanopatterned surfaces prepared by pulsed plasma polymerization and UV-irradiation. Langmuir. 2009;25:8161–9.CrossRefGoogle Scholar
  38. 38.
    Subbiahdoss G, Kuijer R, Grijpma DW, Van der Mei HC, Busscher HJ. Microbial biofilm growth vs. tissue integration: “the race for the surface” experimentally studied. Acta Biomater. 2009;5:1399–404.CrossRefGoogle Scholar
  39. 39.
    Subbiahdoss G, Grijpma DW, Van der Mei HC, Busscher HJ, Kuijer R. Microbial biofilm growth vs. tissue integration on biomaterials with different wettabilities and a polymer-brush coating. J Biomed Mater Res A. 2010;94A:533–8.Google Scholar
  40. 40.
    Subbiahdoss G, Saldarriaga Fernández IC, Da Silva Domingues JF, Kuijer R, Van der Mei HC, Busscher HJ. In vitro interactions between bacteria, osteoblast-like cells and macrophages in the pathogenesis of biomaterial-associated infections. PLoS ONE. 2011;6:e0024827.CrossRefGoogle Scholar
  41. 41.
    Buchholz HW, Elson RA, Engelbrecht E, Lodenkamper H, Rottger J, Siegel A. Management of deep infection of total hip replacement. J Bone Joint Surg Br. 1981;63B:342–53.Google Scholar
  42. 42.
    Bennion RS, Williams RA, Wilson SE. Comparison of infectibility of vascular prosthetic materials by quantitation of median infective dose. Surgery. 1984;95:22–6.Google Scholar
  43. 43.
    Fleer A, Verhoef J. New aspects of staphylococcal infections: emergence of coagulase-negative staphylococci as pathogens. Antonie Van Leeuwenhoek. 1984;50:729–44.CrossRefGoogle Scholar
  44. 44.
    Subbiahdoss G, Kuijer R, Busscher HJ, Van der Mei HC. Mammalian cell growth versus biofilm formation on biomaterial surfaces in an in vitro post-operative contamination model. Microbiology. 2010;156:3073–8.CrossRefGoogle Scholar
  45. 45.
    Anderson JM. Inflammation, wound healing, and the foreign-body response. In: Ratner BD, Hoffman AS, Schoen FJ, Lemons JE, editors. Biomaterials science: an Introduction to materials in medicine. San Diego, CA: Elsevier; 2004. p. 296–304.Google Scholar
  46. 46.
    Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol. 1999;17:593–623.CrossRefGoogle Scholar
  47. 47.
    Underhill DM, Ozinsky A. Phagocytosis of microbes: complexity in action. Annu Rev Immunol. 2002;20:825–52.CrossRefGoogle Scholar
  48. 48.
    Stuart LM, Ezekowitz RAB. Phagocytosis: elegant complexity. Immunity. 2005;22:539–50.CrossRefGoogle Scholar
  49. 49.
    Boelens JJ, Dankert J, Murk JL, Weening JJ, Van der Poll T, Dingemans KP, Koole L, Laman JD, Zaat SAJ. Biomaterial-associated persistence of Staphylococcus epidermidis in pericatheter macrophages. J Infect Dis. 2000;181:1337–49.CrossRefGoogle Scholar
  50. 50.
    Babior BM. Oxidants from phagocytes: agents of defense and destruction. Blood. 1984;64: 959–66.Google Scholar
  51. 51.
    Guenther F, Wabnitz GH, Stroh P, Prior B, Obst U, Samstag Y, Wagner C, Haensch GM. Host defence against Staphylococcus aureus biofilms infection: phagocytosis of biofilms by polymorphonuclear neutrophils (PMN). Mol Immunol. 2009;46:1805–13.CrossRefGoogle Scholar
  52. 52.
    Kaplan SS, Heine RP, Simmons RL. Defensins impair phagocytic killing by neutrophils in biomaterial-related infection. Infect Immun. 1999;67:1640–5.Google Scholar
  53. 53.
    Saldarriaga Fernández IC, Da Silva Domingues JF, Van Kooten TG, Metzger S, Grainger DW, Busscher HJ, Van der Mei HC. Macrophage response to staphylococcal biofilm on cross-linked poly(ethylene) glycol polymer coatings in vitro. Eur Cell Mater. 2011;21:73–9.Google Scholar
  54. 54.
    Kubica M, Guzik K, Koziel J, Zarebski M, Richter W, Gajkowska B, Golda A, Maciag-Gudowska A, Brix K, Shaw L, Foster T, Potempa J. A potential new pathway for Staphylococcus aureus dissemination: the silent survival of S. aureus phagocytosed by human monocyte-derived macrophages. PLoS ONE. 2008;3(1):e1409.CrossRefGoogle Scholar
  55. 55.
    Garzoni C, Kelley WL. Staphylococcus aureus: new evidence for intracellular persistence. Trends Microbiol. 2009;17:59–65.CrossRefGoogle Scholar
  56. 56.
    Bonventre PF, Imhoff JG. Uptake of 3H-dihydrostreptomycin by macrophages in culture. Infect Immun. 1970;2:89–95.Google Scholar
  57. 57.
    Tofte RW, Petersoson PK, Kim Y, Quie PG. Influence of serum concentration on opsonization by the classical and alternative complement pathways. Infect Immun. 1980;27:693–6.Google Scholar
  58. 58.
    Watanabe I, Ichiki M, Shiratsuchi A, Nakanishi Y. TLR2-mediated survival of Staphylococcus aureus in macrophages: a novel bacterial strategy against host innate immunity. J Immunol. 2007;178:4917–25.Google Scholar
  59. 59.
    Leid JG, Shirtliff HG, Costerton JW, Stoodley P. Human leukocytes adhere to, penetrate, and to respond to Staphylococcus aureus biofilms. Infect Immun. 2002;70:6339–45.CrossRefGoogle Scholar
  60. 60.
    Johnson GM, Lee DA, Regelmann WE. Interference with granulocyte function by Staphylococcus epidermidis slime. Infect Immun. 1986;54:13–20.Google Scholar
  61. 61.
    Myrvit QN, Wagner W, Barth E, Wood P, Gristina AG. Effects of extracellular slime produced by Staphylococcus epidermidis on oxidative responses of rabbit alveolar macrophages. J Invest Surg. 1989;2:381–9.CrossRefGoogle Scholar
  62. 62.
    Shanbhag A, Yang J, Lilien J, Black J. Decreased neutrophil respiratory burst on exposure to cobaltchrome alloy and polystyrene in vitro. J Biomed Mater Res. 1992;26:185–95.CrossRefGoogle Scholar
  63. 63.
    Zimmerli W, Waldvogel F. Pathogenesis of foreign body infection. J Clin Invest. 1984;73: 1191–200.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Guruprakash Subbiahdoss
    • 1
  • Joana F. da Silva Domingues
    • 1
  • Roel Kuijer
    • 1
  • Henny C. van der Mei
    • 1
  • Henk J. Busscher
    • 1
  1. 1.Department of Biomedical EngineeringUniversity Medical Center Groningen and University of GroningenGroningenThe Netherlands

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