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BioMed Research International
Volume 2013 (2013), Article ID 539834, 9 pages
http://dx.doi.org/10.1155/2013/539834
Research Article

Allergy or Tolerance: Reduced Inflammatory Cytokine Response and Concomitant IL-10 Production of Lymphocytes and Monocytes in Symptom-Free Titanium Dental Implant Patients

1Department of Dermatology and Allergology, Ludwig-Maximilians-University of Munich, Frauenlobstraße 9-11, 80337 Munich, Germany
2Department of Dentistry, Georg-August University of Göttingen, Robert-Koch-Str. 40, 37075 Göttingen, Germany
3Dental Surgery, Bahhnhofstraße 20, 87700 Memmingen, Germany
4Clinic of Trauma Surgery, University Hospital of Zürich, Rämistr. 100, 8091 Zürich, Switzerland

Received 30 April 2013; Revised 24 July 2013; Accepted 25 July 2013

Academic Editor: Taiyoun Rhim

Copyright © 2013 Peter Thomas et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Büdinger and M. Hertl, “Immunologic mechanisms in hypersensitivity reactions to metal ions: an overview,” Allergy, vol. 55, no. 2, pp. 108–115, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. D. A. Basketter, E. Whittle, and B. Monk, “Possible allergy to complex titanium salt,” Contact Dermatitis, vol. 42, no. 5, pp. 310–311, 2000. View at Scopus
  3. P. A. Lalor, P. A. Revell, A. B. Gray, S. Wright, G. T. Railton, and M. A. R. Freeman, “Sensitivity to titanium. A cause of implant failure?” Journal of Bone and Joint Surgery B, vol. 73, no. 1, pp. 25–28, 1991. View at Scopus
  4. P. Thomas, W. Bandl, S. Maier, B. Summer, and B. Przybilla, “Hypersensitivity to titanium osteosynthesis with impaired fracture healing, eczema, and T-cell hyperresponsiveness in vitro: case report and review of the literature,” Contact Dermatitis, vol. 55, no. 4, pp. 199–202, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Viraben, S. Boulinguez, and C. Alba, “Granulomatous dermatitis after implantation of a titanium-containing pacemaker,” Contact Dermatitis, vol. 33, no. 6, p. 437, 1995. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Yamauchi, A. Morita, and T. Tsuji, “Pacemaker dermatitis from titanium,” Contact Dermatitis, vol. 42, no. 1, pp. 52–53, 2000. View at Scopus
  7. K. Müller and E. Valentine-Thon, “Hypersensitivity to titanium: clinical and laboratory evidence,” Neuroendocrinology Letters, vol. 27, supplement 1, pp. 31–35, 2006. View at Scopus
  8. F. Javed, K. Al-Hezaimi, K. Almas, and G. E. Romanos, “Is titanium sensitivity associated with allergic reactions in patients with dental implants? A systematic review,” Clinical Implant Dentistry and Related Research, vol. 15, no. 1, pp. 47–52, 2013.
  9. A. Siddiqi, A. G. T. Payne, R. K. De Silva, and W. J. Duncan, “Titanium allergy: could it affect dental implant integration?” Clinical Oral Implants Research, vol. 22, no. 7, pp. 673–680, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Eis and U. Wolf, “Qualitätssicherung beim Lymphozytentransformationstest—Addendum zum LTT-Papier der RKI-Kommission ‘Methoden und Qualitätssicherung in der Umweltmedizin’,” Bundesgesundheitsbl-Gesundheitsforsch-Gesundheitsschutz, vol. 51, pp. 1070–1076, 2008.
  11. H. F. Merk, “Diagnosis of drug hypersensitivity: lymphocyte transformation test and cytokines,” Toxicology, vol. 209, no. 2, pp. 217–220, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. W. J. Pichler and J. Tilch, “The lymphocyte transformation test in the diagnosis of drug hypersensitivity,” Allergy, vol. 59, no. 8, pp. 809–820, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Cadosch, E. Chan, O. P. Gautschi, and L. Filgueira, “Metal is not inert: role of metal ions released by biocorrosion in aseptic loosening-current concepts,” Journal of Biomedical Materials Research A, vol. 91, no. 4, pp. 1252–1262, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Okazaki, E. Gotoh, T. Manabe, and K. Kobayashi, “Comparison of metal concentrations in rat tibia tissues with various metallic implants,” Biomaterials, vol. 25, no. 28, pp. 5913–5920, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. R. M. Urban, J. J. Jacobs, M. J. Tomlinson, J. Gavrilovic, J. Black, and M. Peoc'h, “Dissemination of wear particles to the liver, spleen, and abdominal lymph nodes of patients with hip or knee replacement,” Journal of Bone and Joint Surgery A, vol. 82, no. 4, pp. 457–477, 2000. View at Scopus
  16. G. M. Keegan, I. D. Learmonth, and C. P. Case, “Orthopaedic metals and their potential toxicity in the arthroplasty patient. A review of current knowledge and future strategies,” Journal of Bone and Joint Surgery B, vol. 89, no. 5, pp. 567–573, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Nuevo-Ordóñez, M. Montes-Bayón, E. Blanco-González et al., “Titanium release in serum of patients with different bone fixation implants and its interaction with serum biomolecules at physiological levels,” Analytical and Bioanalytical Chemistry, vol. 401, no. 9, pp. 2747–2754, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. T. D. Richardson, S. J. Pineda, K. B. Strenge et al., “Serum titanium levels after instrumented spinal arthrodesis,” Spine, vol. 33, no. 7, pp. 792–796, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Chiba, H. E. Rubash, K. J. K. Kang Jung Kim, and Y. Iwaki, “The characterization of cytokines in the interface tissue obtained from failed cementless total hip arthroplasty with and without femoral osteolysis,” Clinical Orthopaedics and Related Research, no. 300, pp. 304–312, 1994. View at Scopus
  20. N. J. Epstein, B. A. Warme, J. Spanogle et al., “Interleukin-1 modulates periprosthetic tissue formation in an intramedullary model of particle-induced inflammation,” Journal of Orthopaedic Research, vol. 23, no. 3, pp. 501–510, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. M. S. Caicedo, R. Desai, K. McAllister, A. Reddy, J. J. Jacobs, and N. J. Hallab, “Soluble and particulate Co-Cr-Mo alloy implant metals activate the inflammasome danger signaling pathway in human macrophages: a novel mechanism for implant debris reactivity,” Journal of Orthopaedic Research, vol. 27, no. 7, pp. 847–854, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. C. A. St Pierre, M. Chan, Y. Iwakura, D. C. Ayers, E. A. Kurt-Jones, and R. W. Finberg, “Periprosthetic osteolysis: characterizing the innate immune response to titanium wear-particles,” Journal of Orthopaedic Research, vol. 28, no. 11, pp. 1418–1424, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Candel-Martí, A. Flichy-Fernández, T. Alegre-Domingo, J. Ata-Ali, and M. A. Peñarrocha-Diago, “Interleukins IL-6, IL-8, IL-10, IL-12 and periimplant disease. An update,” Medicina Oral, Patologia Oral y Cirugia Bucal, vol. 16, no. 4, pp. e518–e521, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Maitra, C. C. Clement, B. Scharf et al., “Endosomal damage and TLR2 mediated inflammasome activation by alkane particles in the generation of aseptic osteolysis,” Molecular Immunology, vol. 47, no. 2-3, pp. 175–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. L. A. J. O'Neill, “Immunology: how frustration leads to inflammation,” Science, vol. 320, no. 5876, pp. 619–620, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Summer, C. A. Sander, B. Przybilla, and P. Thomas, “Molecular analysis of T-cell clonality with concomitant specific T-cell proliferation in vitro in nickel-allergic individuals,” Allergy, vol. 56, no. 8, pp. 767–770, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Merritt and S. A. Brown, “Distribution of cobalt chromium wear and corrosion products and biologic reactions,” Clinical Orthopaedics and Related Research, no. 329, pp. S233–S243, 1996. View at Scopus
  28. K. Onodera, K. Ooya, and H. Kawamura, “Titanium lymph node pigmentation in the reconstruction plate system of a mandibular bone defect,” Oral Surgery Oral Medicine and Oral Pathology, vol. 75, no. 4, pp. 495–497, 1993. View at Scopus
  29. D. Weingart, “Titanium deposition in regional lymph nodes after insertion of titanium screw implants in maxillofacial region,” International Journal of Oral and Maxillofacial Surgery, vol. 23, no. 6, pp. 450–452, 1994. View at Scopus
  30. T. P. Chaturvedi, “An overview of the corrosion aspect of dental implants (titanium and its alloys),” Indian Journal of Dental Research, vol. 20, no. 1, pp. 91–98, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Ingham and J. Fisher, “The role of macrophages in osteolysis of total joint replacement,” Biomaterials, vol. 26, no. 11, pp. 1271–1286, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Stea, M. Visentin, D. Granchi et al., “Cytokines and osteolysis around total hip prostheses,” Cytokine, vol. 12, no. 10, pp. 1575–1579, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. R. S. Tuan, F. Y. Lee, Y. T Konttinen, J. M. Wilkinson, and R. L. Smith, “What are the local and systemic biologic reactions and mediators to wear debris, and what host factors determine or modulate the biologic response to wear particles?” The Journal of the American Academy of Orthopaedic Surgeons, vol. 16, supplement 1, pp. S42–S48, 2008. View at Scopus
  34. E. M. Schwarz, A. P. Lu, J. J. Goater et al., “Tumor necrosis factor-α/nuclear transcription factor-κB signaling in periprosthetic osteolysis,” Journal of Orthopaedic Research, vol. 18, no. 3, pp. 472–480, 2000. View at Scopus
  35. S. D. Ferreira, G. L. M. Silva, J. R. Cortelli, J. E. Costa, and F. O. Costa, “Prevalence and risk variables for peri-implant disease in Brazilian subjects,” Journal of Clinical Periodontology, vol. 33, no. 12, pp. 929–935, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. N. P. Lang and T. Berglundh, “Periimplant diseases: where are we now?—consensus of the seventh European workshop on periodontology,” Journal of Clinical Periodontology, vol. 38, no. 11, pp. 178–181, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Mombelli and F. Décaillet, “The characteristics of biofilms in peri-implant disease,” Journal of Clinical Periodontology, vol. 38, no. 11, pp. 203–213, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. F. P. Strietzel, P. A. Reichart, A. Kale, M. Kulkarni, B. Wegner, and I. Küchler, “Smoking interferes with the prognosis of dental implant treatment: a systematic review and meta-analysis,” Journal of Clinical Periodontology, vol. 34, no. 6, pp. 523–544, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Bernard, M. Baeck, D. Tennstedt, V. Haufroid, and V. Dekeuleneer, “Chromate or titanium allergy—the role of impurities?” Contact Dermatitis, vol. 68, pp. 191–192, 2013.
  40. P. Thomas, C. von der Helm, C. Schopf et al., “Periimplant histology and cytokine pattern in metal-allergic knee arthroplasty patients with improvement after revision with hypoallergenic materials,” Seminars in Arthroplasty, vol. 23, no. 4, pp. 268–272, 2012.
  41. Y. H. Park, S. H. Jeong, S. M. Yi et al., “Analysis for the potential of polystyrene and TiO2 nanoparticles to induce skin irritation, phototoxicity, and sensitization,” Toxicology In Vitro, vol. 25, no. 8, pp. 1863–1869, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. V. Hornung, F. Bauernfeind, A. Halle et al., “Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization,” Nature Immunology, vol. 9, no. 8, pp. 847–856, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. J. M. Cavaillon, M. Adib-Conquy, C. Fitting, C. Adrie, and D. Payen, “Cytokine cascade in sepsis,” Scandinavian Journal of Infectious Diseases, vol. 35, no. 9, pp. 535–544, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Kawamura, R. Wakusawa, and K. Inada, “Interleukin-10 and interleukin-1 receptor antagonists increase during cardiac surgery,” Canadian Journal of Anaesthesia, vol. 44, no. 1, pp. 38–42, 1997. View at Scopus
  45. E. M. O. Nuallain, P. Puri, K. Mealy, and D. J. Reen, “Induction of interleukin-1 receptor antagonist (IL-1ra) following surgery is associated with major trauma,” Clinical Immunology and Immunopathology, vol. 76, no. 1, pp. 96–101, 1995. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Martire-Greco, N. Rodriguez-Rodrigues, V. I. Landoni, B. Rearte, M. A. Isturiz, and G. C. Fernandez, “Interleukin-10 controls human peripheral PMN activation triggered by lipopolysaccharide,” Cytokine, vol. 62, no. 3, pp. 426–432, 2013.
  47. K. H. Pinke, B. Calzavara, P. F. Faria, M. P. do Nascimento, J. Venturini, and V. S. Lara, “Proinflammatory profile of in vitro monocytes in the ageing is affected by lymphocytes presence,” Immunity & Ageing, vol. 10, p. 22, 2013. View at Publisher · View at Google Scholar
  48. R. Medzhitov, E. M. Shevach, G. Trinchieri et al., “Highlights of 10 years of immunology in Nature Reviews Immunology,” Nature Reviews Immunology, vol. 11, no. 10, pp. 693–702, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Meisel, K. Vogt, C. Platzer, F. Randow, C. Liebenthal, and H. Volk, “Differential regulation of monocytic tumor necrosis factor-α and interleukin-10 expression,” European Journal of Immunology, vol. 26, no. 7, pp. 1580–1586, 1996. View at Publisher · View at Google Scholar · View at Scopus
  50. K. W. Moore, R. De Waal Malefyt, R. L. Coffman, and A. O'Garra, “Interleukin-10 and the interleukin-10 receptor,” Annual Review of Immunology, vol. 19, pp. 683–765, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. A. C. Zenclussen, “CD4+CD25+ T regulatory cells in murine pregnancy,” Journal of Reproductive Immunology, vol. 65, no. 2, pp. 101–110, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Santner-Nanan, K. Straubinger, P. Hsu, et al., “Fetal-maternal alignment of regulatory T cells correlates with IL-10 and bcl-2 upregulation in pregnancy,” Journal of Immunology, vol. 191, no. 1, pp. 145–153, 2013.
  53. M. Jutel and C. A. Akdis, “Immunological mechanisms of allergen-specific immunotherapy,” Allergy, vol. 66, no. 6, pp. 725–732, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Saraiva and A. O'Garra, “The regulation of IL-10 production by immune cells,” Nature Reviews Immunology, vol. 10, no. 3, pp. 170–181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Nowzari, J. E. Botero, M. DeGiacomo, M. C. Villacres, and S. K. Rich, “Microbiology and cytokine levels around healthy dental implants and teeth,” Clinical Implant Dentistry and Related Research, vol. 10, no. 3, pp. 166–173, 2008. View at Publisher · View at Google Scholar · View at Scopus