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Examination of the inflammatory response following implantation of titanium plates coated with phospholipids in rats

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Abstract

Implantation of biomaterials like titanium (Ti) causes inflammatory reactions possibly affecting implant functionality. Surface modifications could improve biocompatibility and functionality of implants. Biomembrane-derived phospholipids might be useful as implant coating due to their biomimetic properties. In vitro studies demonstrated beneficial effects for 2-oleoyl-1-palmitoyl-sn-glycero-3-phosphoethanolamin (POPE) as coating regarding interactions with cells and bacteria. Therefore, this in vivo study aimed at examining local inflammatory reactions after implantation of POPE-coated Ti plates. Ti implants with POPE attached non-covalently or covalent via octadecylphosphonic acid (OPA), with OPA alone and uncoated controls were simultaneously implanted intramuscularly in rats for 7, 14 and 56 days. The peri-implant tissue was quantitatively analyzed by immunohistochemistry for total macrophages, tissue macrophages, T cells, antigen-presenting cells and proliferating cells. Overall, both POPE-coated series were comparable to the controls. Furthermore, no differences were found between POPE coating on a covalently linked OPA monolayer and POPE coating dried from solution. Together with earlier in vitro results, this demonstrates the potential of phospholipids for implant surface modification.

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References

  1. Williams DF. On the nature of biomaterials. Biomaterials. 2009;30:5897–909.

    Article  CAS  Google Scholar 

  2. Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol. 2008;20:86–100.

    Article  CAS  Google Scholar 

  3. Williams DF. On the mechanisms of biocompatibility. Biomaterials. 2008;29:2941–53.

    Article  CAS  Google Scholar 

  4. Zreiqat H, Kumar RK, Markovic B, Zicat B, Howlett CR. Macrophages at the skeletal tissue-device interface of loosened prosthetic devices express bone-related genes and their products. J Biomed Mater Res A. 2003;65:109–17.

    Article  CAS  Google Scholar 

  5. Allemann F, Mizuno S, Eid K, Yates KE, Zaleske D, Glowacki J. Effects of hyaluronan on engineered articular cartilage extracellular matrix gene expression in 3-dimensional collagen scaffolds. J Biomed Mater Res. 2001;55:13–9.

    Article  CAS  Google Scholar 

  6. Briggs EP, Walpole AR, Wilshaw PR, Karlsson M, Pålsgård E. Formation of highly adherent nano-porous alumina on Ti-based substrates: a novel bone implant coating. J Mater Sci Mater Med. 2004;15:1021–9.

    Article  CAS  Google Scholar 

  7. Roy RK, Lee KR. Biomedical applications of diamond-like carbon coatings: a review. J Biomed Mater Res B Appl Biomater. 2007;83:72–84.

    Google Scholar 

  8. Moritz N, Vedel E, Ylänen H, Jokinen M, Hupa M, Yli-Urpo A. Characterisation of bioactive glass coatings on titanium substrates produced using a CO2 laser. J Mater Sci Mater Med. 2004;15:787–94.

    Article  CAS  Google Scholar 

  9. Chen JS, Juang HY, Hon MH. Calcium phosphate coating on titanium substrate by a modified electrocrystallization process. J Mater Sci Mater Med. 1998;9:297–300.

    Article  CAS  Google Scholar 

  10. Osborn JF. Biological behavior of the hydroxyapatite ceramic coating on the femur shaft of a titanium endoprosthesis—initial histologic evaluation of a human explant. Biomed Technol (Berl). 1987;32:177–83.

    Article  CAS  Google Scholar 

  11. Trojanowicz M. Miniaturized biochemical sensing devices based on planar bilayer lipid membranes. Fresenius J Anal Chem. 2001;371:246–60.

    Article  CAS  Google Scholar 

  12. Ishihara K, Oshida H, Endo Y, Ueda T, Watanabe A, Nakabayashi N. Hemocompatibility of human whole blood on polymers with a phospholipid polar group and its mechanism. J Biomed Mater Res. 1992;26:1543–52.

    Article  CAS  Google Scholar 

  13. Choi J, Konno T, Matsuno R, Takai M, Ishihara K. Surface immobilization of biocompatible phospholipid polymer multilayered hydrogel on titanium alloy. Colloids Surf B Biointerfaces. 2008;67:216–23.

    Article  CAS  Google Scholar 

  14. Rudolph AS. Biomaterial biotechnology using self-assembled lipid microstructures. J Cell Biochem. 1994;56:183–7.

    Article  CAS  Google Scholar 

  15. Murphy EF, Keddie JL, Lu JR, Brewer J, Russell J. The reduced adsorption of lysozyme at the phosphorylcholine incorporated polymer/aqueous solution interface studied by spectroscopic ellipsometry. Biomaterials. 1999;20:1501–11.

    Article  CAS  Google Scholar 

  16. Andersson AS, Glasmästar K, Sutherland D, Lidberg U, Kasemo B. Cell adhesion on supported lipid bilayers. J Biomed Mater Res A. 2003;64:622–9.

    Article  Google Scholar 

  17. Chapman D. Biocompatible surfaces based upon the phospholipid asymmetry of biomembranes. Biochem Soc Trans. 1993;21:258–62.

    CAS  Google Scholar 

  18. Hayward JA, Chapman D. Biomembrane surfaces as models for polymer design: the potential for haemocompatibility. Biomaterials. 1984;5:135–42.

    Article  CAS  Google Scholar 

  19. Hayward JA, Johnston DS, Chapman D. Polymeric phospholipids as new biomaterials. Ann N Y Acad Sci. 1985;446:267–81.

    Article  CAS  Google Scholar 

  20. Willumeit R, Schuster A, Iliev P, Linser S, Feyerabend F. Phospholipids as implant coatings. J Mater Sci Mater Med. 2007;18:367–80.

    Article  CAS  Google Scholar 

  21. Willumeit R, Schossig M, Clemens H, Feyerabend F. In vitro interactions of human chondrocytes and mesenchymal stem cells, and of mouse macrophages with phospholipid-covered metallic implant materials. Eur Cell Mater. 2007;13:11–25.

    CAS  Google Scholar 

  22. Willumeit R, Kamusewitz H, Schossig M, Schröder J, Clemens H. Implant surface modification by biological multi-layer systems. Mater Res Soc Symp Proc. 2003;734:B8.6.1–6.

    Google Scholar 

  23. Adden N, Gamble LJ, Castner DG, Hoffmann A, Gross G, Menzel H. Phosphonic acid monolayers for binding of bioactive molecules to titanium surfaces. Langmuir. 2006;22:8197–204.

    Article  CAS  Google Scholar 

  24. Silverman BM, Wieghaus KA, Schwartz J. Comparative properties of siloxane vs phosphonate monolayers on a key titanium alloy. Langmuir. 2005;21:225–8.

    Article  CAS  Google Scholar 

  25. Finke B, Luethen F, Schroeder K, Mueller PD, Bergemann C, Frant M, Ohl A, Nebe BJ. The effect of positively charged plasma polymerization on initial osteoblastic focal adhesion on titanium surfaces. Biomaterials. 2007;28:4521–34.

    Article  CAS  Google Scholar 

  26. Gallagher JA. Human osteoblast culture. Methods Mol Med. 2003;80:3–18.

    CAS  Google Scholar 

  27. Walschus U, Hoene A, Neumann HG, Wilhelm L, Lucke S, Lüthen F, Rychly J, Schlosser M. Morphometric immunohistochemical examination of the inflammatory tissue reaction after implantation of calcium phosphate-coated titanium plates in rats. Acta Biomater. 2009;5:776–84.

    Article  CAS  Google Scholar 

  28. Tang L, Eaton J. Inflammatory responses to biomaterials. Am J Clin Pathol. 1995;103:466–71.

    CAS  Google Scholar 

  29. Brett T. The laboratory assessment of biocompatibility: the role of complement activation testing. Med Dev Technol. 1992;3:326–30.

    Google Scholar 

  30. Mollnes T. Complement and biocompatibility. Vox Sang. 1998;74:303–7.

    CAS  Google Scholar 

  31. Ward RA. Phagocytic cell function as an index of biocompatibility. Nephrol Dial Transplant. 1994;9:46–56.

    Google Scholar 

  32. Pereira BJ, Dinarello CA. Production of cytokines and inhibitory proteins in patients on dialysis. Nephrol Dial Transplant. 1994;9:60–71.

    Google Scholar 

  33. Grammer LC, Patterson R. IgE against ethylene-oxide-altered human serum albumin (ETO-HSA) as an etiologic agent in allergic reactions of hemodialysis patients. Artif Organs. 1987;11:97–9.

    Article  CAS  Google Scholar 

  34. Tang L, Jennings TA, Eaton JW. Mast cells mediate acute inflammatory responses to implanted biomaterials. Proc Natl Acad Sci USA. 1998;95:8841–6.

    Article  CAS  Google Scholar 

  35. Anderson JM. Biomaterial biocompatibility and the macrophage. Biomaterials. 1984;5:5–10.

    Article  CAS  Google Scholar 

  36. Bosetti M, Santin M, Lloyd AW, Denyer SP, Sabbatini M, Cannas M. Cell behaviour on phospholipids-coated surfaces. J Mater Sci Mater Med. 2007;18:611–7.

    Article  CAS  Google Scholar 

  37. Santin M, Rhys-Williams W, O’Reilly J, Davies MC, Shakesheff K, Love WG, Lloyd AW, Denyer SP. Calcium-binding phospholipids as a coating material for implant osteointegration. J R Soc Interface. 2006;3:277–81.

    Article  CAS  Google Scholar 

  38. Wilson JT, Cui W, Sun XL, Tucker-Burden C, Weber CJ, Chaikof EL. In vivo biocompatibility and stability of a substrate-supported polymerizable membrane-mimetic film. Biomaterials. 2007;28:609–17.

    Article  CAS  Google Scholar 

  39. De Souza R, Zahedi P, Allen CJ, Piquette-Miller M. Biocompatibility of injectable chitosan-phospholipid implant systems. Biomaterials. 2009;30:3818–24.

    Article  Google Scholar 

  40. Hoene A, Walschus U, Patrzyk M, Finke B, Lucke S, Nebe B, Schröder K, Ohl A, Schlosser M. In vivo investigation of the inflammatory response against allylamine plasma coated titanium implants in a rat model. Acta Biomater. 2010;6:676–83.

    Article  CAS  Google Scholar 

  41. Willumeit R, Feyerabend F, Kamusewitz H, Schossig M, Clemens H. Biological multi-layer systems as implant surface modification. Matwiss Werkst. 2003;34:1084–93.

    Article  CAS  Google Scholar 

  42. Pressl D, Teichert C, Hlawacek G, Clemens H, Iliev PP, Schuster A, Feyerabend F, Willumeit R. Characterization of phospholipid bilayers on Ti-6Al-4V and Ti-6Al-7Nb. Adv Eng Mater. 2008;10:B47–52.

    Article  CAS  Google Scholar 

  43. Pressl D. Surface modification of titanium alloys by phosphlipid membrane systems. Diploma Thesis, Institute of Physics, University of Leoben, 2004.

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Acknowledgments

We would like to thank Kirsten Tornow for excellent technical assistance. In addition we acknowledge the valuable contribution of Dr. Anna Schuster and Jessica Rutz. The study was supported by the Federal State of Mecklenburg-Vorpommern and the Helmholtz Association of German Research Centers (Grant No. VH-MV1).

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Authors and Affiliations

  1. Department of Medical Biochemistry and Molecular Biology, Research Group of Predictive Diagnostics, Ernst Moritz Arndt University of Greifswald, Greifswalder Str. 11c, 17495, Karlsburg, Germany

    Alexandra Kochanowski, Uwe Walschus, Silke Lucke & Michael Schlosser

  2. Institute of Pathophysiology, Ernst Moritz Arndt University of Greifswald, Karlsburg, Germany

    Alexandra Kochanowski, Uwe Walschus, Silke Lucke & Michael Schlosser

  3. Department of Surgery, Ernst Moritz Arndt University of Greifswald, Greifswald, Germany

    Andreas Hoene & Maciej Patrzyk

  4. Institute for Plasma Science and Technology (INP), Felix-Hausdorff-Straße 2, 17489, Greifswald, Germany

    Birgit Finke

  5. Helmholtz-Zentrum Geesthacht, Institute for Materials Research, Geesthacht, Germany

    Bérengère Luthringer, Frank Feyerabend & Regine Willumeit

Authors
  1. Alexandra Kochanowski
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  2. Andreas Hoene
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  3. Maciej Patrzyk
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  4. Uwe Walschus
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  5. Birgit Finke
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  6. Bérengère Luthringer
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  7. Frank Feyerabend
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  8. Regine Willumeit
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  9. Silke Lucke
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  10. Michael Schlosser
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Corresponding author

Correspondence to Michael Schlosser.

Additional information

Paper selected for publication from the 23rd European Conference on Biomaterials, Tampere, Finland, September 2010.

Alexandra Kochanowski and Andreas Hoene have contributed equally to this work.

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Kochanowski, A., Hoene, A., Patrzyk, M. et al. Examination of the inflammatory response following implantation of titanium plates coated with phospholipids in rats. J Mater Sci: Mater Med 22, 1015–1026 (2011). https://doi.org/10.1007/s10856-011-4287-6

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  • DOI: https://doi.org/10.1007/s10856-011-4287-6

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