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Clinical Oral Investigations

, Volume 23, Issue 10, pp 3731–3738 | Cite as

Changes in proinflammatory gene expression in human whole blood after contact with UV-conditioned implant surfaces

  • Sönke HarderEmail author
  • Elgar Susanne Quabius
  • Fabian Meinke
  • Christian Mehl
  • Matthias Kern
Original Article
  • 122 Downloads

Abstract

Objectives

The aim of this in vitro study was to assess changes in the gene expression of proinflammatory cytokines in human whole blood after contact with titanium implant surfaces conditioned by UV light. To this end, expression levels of proinflammatory cytokines were analyzed in vitro in human whole blood.

Materials and methods

Dental implants made of grade 4 titanium were conditioned by UV light in a UV device and submerged in human whole blood. Unconditioned implants served as controls, and blood samples without implants served as the negative control group. Sampling was performed at 1, 8, and 24 h. Changes in the expression levels of interleukin-1β (IL1B) and tumor necrosis factor alpha (TNF) were assessed using RT-qPCR at the mRNA level.

Results

The gene expression of IL1B was significantly suppressed in the test group over the observation period compared to the control group during the 1–8 h after having contact between the implant surface and the blood. The gene expression of TNF was not significantly altered by UV conditioning after 1 and 8 h of observation, but both cytokine expression levels were increased significantly after 24 h.

Conclusions

Differences in the gene expression of proinflammatory cytokines after insertion of UV-conditioned titanium implants can be assessed using a human whole blood test. UV-conditioned implant surfaces apparently suppress the release of IL1B in vitro.

Clinical relevance

The results of our publication demonstrate that modulation of the early inflammatory response in human whole blood is possible by surface treatment with UV light. In particular, the suppression of IL1B expression, especially after the initial contact of blood cells, may be beneficial in the osseointegration of titanium implants by positively influence the balance between rejection and acceptance of an implant.

Keywords

Implants Gene expression analysis UV Proinflammatory cytokines Osseointegration Photofunctionalization 

Notes

Acknowledgements

The authors gratefully acknowledge the excellent technical assistance of Hilke Clasen (Department of Immunology at the University Hospital Schleswig-Holstein, Campus Kiel).

Funding

The work was supported by a material donation of the Oral Reconstruction Foundation (former Camlog Foundation) (grant CF11602), Baseland, Switzerland, and a grant from the German Society for Prosthetic Dentistry and Biomaterials (DGPro), Hannover, Germany.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

References

  1. 1.
    Trindade R, Albrektsson T, Galli S, Prgomet Z, Tengvall P, Wennerberg A (2018) Osseointegration and foreign body reaction: titanium implants activate the immune system and suppress bone resorption during the first 4 weeks after implantation. Clin Implant Dent Relat Res 20:82–91.  https://doi.org/10.1111/cid.12578 CrossRefPubMedGoogle Scholar
  2. 2.
    Trindade R, Albrektsson T, Tengvall P, Wennerberg A (2016) Foreign body reaction to biomaterials: on mechanisms for buildup and breakdown of osseointegration. Clin Implant Dent Relat Res 18:192–203.  https://doi.org/10.1111/cid.12274 CrossRefPubMedGoogle Scholar
  3. 3.
    Franz S, Rammelt S, Scharnweber D, Simon JC (2011) Immune responses to implants - a review of the implications for the design of immunomodulatory biomaterials. Biomaterials 32:6692–6709.  https://doi.org/10.1016/j.biomaterials.2011.05.078 CrossRefPubMedGoogle Scholar
  4. 4.
    Junker R, Dimakis A, Thoneick M, Jansen JA (2009) Effects of implant surface coatings and composition on bone integration: a systematic review. Clin Oral Implants Res 20(Suppl 4):185–206.  https://doi.org/10.1111/j.1600-0501.2009.01777.x CrossRefPubMedGoogle Scholar
  5. 5.
    Henningsen A, Smeets R, Heuberger R, Jung OT, Hanken H, Heiland M, Cacaci C, Precht C (2018) Changes in surface characteristics of titanium and zirconia after surface treatment with ultraviolet light or non-thermal plasma. Eur J Oral Sci 126:126–134.  https://doi.org/10.1111/eos.12400 CrossRefPubMedGoogle Scholar
  6. 6.
    Aita H, Hori N, Takeuchi M, Suzuki T, Yamada M, Anpo M, Ogawa T (2009) The effect of ultraviolet functionalization of titanium on integration with bone. Biomaterials 30:1015–1025.  https://doi.org/10.1016/j.biomaterials.2008.11.004 CrossRefPubMedGoogle Scholar
  7. 7.
    Ogawa T (2014) Ultraviolet photofunctionalization of titanium implants. Int J Oral Maxillofac Implants 29:e95–e102.  https://doi.org/10.11607/jomi.te47
  8. 8.
    Bielemann AM, Marcello-Machado RM, Del Bel Cury AA, Faot F (2018) Systematic review of wound healing biomarkers in peri-implant crevicular fluid during osseointegration. Arch Oral Biol 89:107–128.  https://doi.org/10.1016/j.archoralbio.2018.02.013 CrossRefPubMedGoogle Scholar
  9. 9.
    Feller L, Jadwat Y, Khammissa RA, Meyerov R, Schechter I, Lemmer J (2015) Cellular responses evoked by different surface characteristics of intraosseous titanium implants. Biomed Res Int 2015:171945–171948.  https://doi.org/10.1155/2015/171945 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Alfarsi MA, Hamlet SM, Ivanovski S (2014) Titanium surface hydrophilicity modulates the human macrophage inflammatory cytokine response. J Biomed Mater Res A 102:60–67.  https://doi.org/10.1002/jbm.a.34666 CrossRefPubMedGoogle Scholar
  11. 11.
    Williams DF (2008) On the mechanisms of biocompatibility. Biomaterials 29:2941–2953.  https://doi.org/10.1016/j.biomaterials.2008.04.023 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Bielemann AM, Marcello-Machado RM, Leite FRM, Martinho FC, Chagas-Junior OL, Antoninha Del Bel Cury A, Faot F (2018) Comparison between inflammation-related markers in peri-implant crevicular fluid and clinical parameters during osseointegration in edentulous jaws. Clin Oral Investig 22:531–543.  https://doi.org/10.1007/s00784-017-2169-0 CrossRefPubMedGoogle Scholar
  13. 13.
    Urbanski W, Marycz K, Krzak J, Pezowicz C, Dragan SF (2017) Cytokine induction of sol-gel-derived TiO2 and SiO2 coatings on metallic substrates after implantation to rat femur. Int J Nanomedicine 12:1639–1645.  https://doi.org/10.2147/ijn.S114885 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Harmankaya N, Igawa K, Stenlund P, Palmquist A, Tengvall P (2012) Healing of complement activating Ti implants compared with non-activating Ti in rat tibia. Acta Biomater 8:3532–3540.  https://doi.org/10.1016/j.actbio.2012.05.017 CrossRefPubMedGoogle Scholar
  15. 15.
    Linderback P, Harmankaya N, Askendal A, Areva S, Lausmaa J, Tengvall P (2010) The effect of heat- or ultra violet ozone-treatment of titanium on complement deposition from human blood plasma. Biomaterials 31:4795–4801.  https://doi.org/10.1016/j.biomaterials.2010.02.060 CrossRefPubMedGoogle Scholar
  16. 16.
    Kanagaraja S, Lundstrom I, Nygren H, Tengvall P (1996) Platelet binding and protein adsorption to titanium and gold after short time exposure to heparinized plasma and whole blood. Biomaterials 17:2225–2232CrossRefGoogle Scholar
  17. 17.
    Arvidsson S, Askendal A, Tengvall P (2007) Blood plasma contact activation on silicon, titanium and aluminium. Biomaterials 28:1346–1354.  https://doi.org/10.1016/j.biomaterials.2006.11.005 CrossRefPubMedGoogle Scholar
  18. 18.
    Thor A, Rasmusson L, Wennerberg A, Thomsen P, Hirsch JM, Nilsson B, Hong J (2007) The role of whole blood in thrombin generation in contact with various titanium surfaces. Biomaterials 28:966–974.  https://doi.org/10.1016/j.biomaterials.2006.10.020 CrossRefPubMedGoogle Scholar
  19. 19.
    Clark R (1996) The molecular and cellular biology of wound repair. Springer US, New YorkGoogle Scholar
  20. 20.
    Dirschnabel AJ, Alvim-Pereira F, Alvim-Pereira CC, Bernardino JF, Rosa EA, Trevilatto PC (2011) Analysis of the association of IL1B(C-511T) polymorphism with dental implant loss and the clusterization phenomenon. Clin Oral Implants Res 22:1235–1241.  https://doi.org/10.1111/j.1600-0501.2010.02080.x CrossRefPubMedGoogle Scholar
  21. 21.
    Slotte C, Lenneras M, Gothberg C, Suska F, Zoric N, Thomsen P, Nannmark U (2012) Gene expression of inflammation and bone healing in peri-implant crevicular fluid after placement and loading of dental implants. A kinetic clinical pilot study using quantitative real-time PCR. Clin Implant Dent Relat Res 14:723–736.  https://doi.org/10.1111/j.1708-8208.2010.00309.x CrossRefPubMedGoogle Scholar
  22. 22.
    Thurm CW, Halsey JF (2005) Measurement of cytokine production using whole blood. Curr Protoc Immunol Chapter 7:Unit 7.18B.  https://doi.org/10.1002/0471142735.im0718bs66
  23. 23.
    Harder S, Quabius ES, Ossenkop L, Mehl C, Kern M (2012) Surface contamination of dental implants assessed by gene expression analysis in a whole-blood in vitro assay: a preliminary study. J Clin Periodontol 39:987–994.  https://doi.org/10.1111/j.1600-051X.2012.01929.x CrossRefPubMedGoogle Scholar
  24. 24.
    Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1:581–585.  https://doi.org/10.1038/nprot.2006.83 CrossRefPubMedGoogle Scholar
  25. 25.
    Sambrook J, Green MR (2012) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, Cold Spring HarbourGoogle Scholar
  26. 26.
    Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45–e445Google Scholar
  27. 27.
    Monasterio G, Guevara J, Ibarra JP, Castillo F, Diaz-Zuniga J, Alvarez C, Cafferata EA, Vernal R (2018) Immunostimulatory activity of low-molecular-weight hyaluronan on dendritic cells stimulated with Aggregatibacter actinomycetemcomitans or Porphyromonas gingivalis. Clin Oral Investig.  https://doi.org/10.1007/s00784-018-2641-5
  28. 28.
    Lopez-Castejon G, Brough D (2011) Understanding the mechanism of IL-1beta secretion. Cytokine Growth Factor Rev 22:189–195.  https://doi.org/10.1016/j.cytogfr.2011.10.001 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    T A, C J (2001) Osteoinduction, osteoconduction and osseointegration. Eur Spine J 10(Suppl 2):S96–S101.  https://doi.org/10.1007/s005860100282
  30. 30.
    Raghavendra S, Wood MC, Taylor TD (2005) Early wound healing around endosseous implants: a review of the literature. Int J Oral Maxillofac Implants 20:425–431PubMedGoogle Scholar
  31. 31.
    Nilsson B, Larsson R, Hong J, Elgue G, Ekdahl KN, Sahu A, Lambris JD (1998) Compstatin inhibits complement and cellular activation in whole blood in two models of extracorporeal circulation. Blood 92:1661–1667CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Prosthodontics, Propaedeutics and Dental Materials, School of DentistryChristian-Albrechts University KielKielGermany
  2. 2.Institute of ImmunologyChristian-Albrechts University KielKielGermany
  3. 3.Department of Otorhinolaryngology, Head and Neck SurgeryChristian-Albrechts University KielKielGermany

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