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Coating with artificial matrices from collagen and sulfated hyaluronan influences the osseointegration of dental implants

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Abstract

Dental implants are an established therapy for oral rehabilitation. High success rates are achieved in healthy bone, however, these rates decrease in compromised host bone. Coating of dental implants with components of the extracellular matrix is a promising approach to enhance osseointegration in compromised peri-implant bone. Dental titanium implants were coated with an artificial extracellular matrix (aECM) consisting of collagen type I and either one of two regioselectively low sulfated hyaluronan (sHA) derivatives (coll/sHA1Δ6s and coll/sHA1) and compared to commercial pure titanium implants (control). After extraction of the premolar teeth, 36 implants were inserted into the maxilla of 6 miniature pigs (6 implants per maxilla). The healing periods were 4 and 8 weeks, respectively. After animal sacrifice, the samples were evaluated histomorphologically and histomorphometrically. All surface states led to a sufficient implant osseointegration after 4 and 8 weeks. Inflammatory or foreign body reactions could not be observed. After 4 weeks of healing, implants coated with coll/sHA1Δ6s showed the highest bone implant contact (BIC; coll/sHA1Δ6s: 45.4 %; coll/sHA1: 42.2 %; control: 42.3 %). After 8 weeks, a decrease of BIC could be observed for coll/sHA1Δ6s and controls (coll/sHA1Δ6s: 37.3 %; control: 31.7 %). For implants coated with coll/sHA1, the bone implant contact increased (coll/sHA1: 50.8 %). Statistically significant differences could not be observed. Within the limits of the current study, aECM coatings containing low sHA increase peri-implant bone formation around dental implants in maxillary bone compared to controls in the early healing period.

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References

  1. Buser D, Janner SFM, Wittneben J, Bragger U, Ramseier CA, Salvi GE. 10-year survival and success rates of 511 titanium implants with a sandblasted and acid-etched surface: a retrospective study in 303 partially edentulous patients. Clin Implant Dent Relat Res. 2012. doi:10.1111/j.1708-8208.2012.00456.x.

    Google Scholar 

  2. Alsaadi G, Quirynen M, Komarek A, van Steenberghe D. Impact of local and systemic factors on the incidence of oral implant failures, up to abutment connection. J Clin Periodontol. 2007. doi:10.1111/j.1600-051X.2007.01077.x.

    Google Scholar 

  3. Branemark PI, Hansson BO, Adell R, Breine U, Lindstrom J, Hallen O, Ohman A. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl. 1977;16:1–132.

    Google Scholar 

  4. Prince CW, Navia JM. Glycosaminoglycan alterations in rat bone due to growth and fluorosis. J Nutr. 1983;113(8):1576–82.

    Google Scholar 

  5. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 2006. doi:10.1096/fj.05-4682rev.

    Google Scholar 

  6. Almond A. Hyaluronan. Cell Mol Life Sci. 2007. doi:10.1007/s00018-007-7032-z.

    Google Scholar 

  7. Takahashi K, Goomer RS, Harwood F, Kubo T, Hirasawa Y, Amiel D. The effects of hyaluronan on matrix metalloproteinase-3 (MMP-3), interleukin-1β(IL-1β), and tissue inhibitor of metalloproteinase-1 (TIMP-1) gene expression during the development of osteoarthritis. Osteoarthr Cartil. 1999. doi:10.1053/joca.1998.0207.

    Google Scholar 

  8. Toole BP. Hyaluronan in morphogenesis. Semin Cell Dev Biol. 2001. doi:10.1006/scdb.2000.0244.

    Google Scholar 

  9. Sasaki T, Watanabe C. Stimulation of osteoinduction in bone wound healing by high-molecular hyaluronic acid. Bone. 1995;16(1):9–15.

    Google Scholar 

  10. Nagahata M, Tsuchiya T, Ishiguro T, Matsuda N, Nakatsuchi Y, Teramoto A, Hachimori A, Abe K. A novel function of N-cadherin and Connexin43: marked enhancement of alkaline phosphatase activity in rat calvarial osteoblast exposed to sulfated hyaluronan. Biochem Biophys Res Commun. 2004. doi:10.1016/j.bbrc.2004.01.098.

    Google Scholar 

  11. Hintze V, Moeller S, Schnabelrauch M, Bierbaum S, Viola M, Worch H, Scharnweber D. Modifications of hyaluronan influence the interaction with human bone morphogenetic protein-4 (hBMP-4). Biomacromolecules. 2009. doi:10.1021/bm9008827.

    Google Scholar 

  12. Hintze V, Miron A, Moeller S, Schnabelrauch M, Wiesmann H, Worch H, Scharnweber D. Sulfated hyaluronan and chondroitin sulfate derivatives interact differently with human transforming growth factor-β1 (TGF-β1). Acta Biomater. 2012. doi:10.1016/j.actbio.2012.03.021.

    Google Scholar 

  13. Hempel U, Moller S, Noack C, Hintze V, Scharnweber D, Schnabelrauch M, Dieter P. Sulfated hyaluronan/collagen I matrices enhance the osteogenic differentiation of human mesenchymal stromal cells in vitro even in the absence of dexamethasone. Acta Biomater. 2012. doi:10.1016/j.actbio.2012.06.039.

    Google Scholar 

  14. Hess R, Jaeschke A, Neubert H, Hintze V, Moeller S, Schnabelrauch M, Wiesmann H, Hart DA, Scharnweber D. Synergistic effect of defined artificial extracellular matrices and pulsed electric fields on osteogenic differentiation of human MSCs. Biomaterials. 2012. doi:10.1016/j.biomaterials.2012.08.056.

    Google Scholar 

  15. Hintze V, Miron A, Moller S, Schnabelrauch M, Heinemann S, Worch H, Scharnweber D. Artificial extracellular matrices of collagen and sulphated hyaluronan enhance the differentiation of human mesenchymal stem cells in the presence of dexamethasone. J Tissue Eng Regen Med. 2012. doi:10.1002/term.1528.

    Google Scholar 

  16. Kliemt S, Lange C, Otto W, Hintze V, Moller S, von Bergen M, Hempel U, Kalkhof S. Sulfated hyaluronan containing collagen matrices enhance cell-matrix-interaction, endocytosis, and osteogenic differentiation of human mesenchymal stromal cells. J Proteome Res. 2013. doi:10.1021/pr300640h.

    Google Scholar 

  17. Salbach J, Kliemt S, Rauner M, Rachner TD, Goettsch C, Kalkhof S, von Bergen M, Moller S, Schnabelrauch M, Hintze V, Scharnweber D, Hofbauer LC. The effect of the degree of sulfation of glycosaminoglycans on osteoclast function and signaling pathways. Biomaterials. 2012. doi:10.1016/j.biomaterials.2012.08.028.

    Google Scholar 

  18. Franz S, Allenstein F, Kajahn J, Forstreuter I, Hintze V, Moller S, Simon JC. Artificial extracellular matrices composed of collagen I and high-sulfated hyaluronan promote phenotypic and functional modulation of human pro-inflammatory M1 macrophages. Acta Biomater. 2013. doi:10.1016/j.actbio.2012.11.016.

    Google Scholar 

  19. Kunze R, Rosler M, Moller S, Schnabelrauch M, Riemer T, Hempel U, Dieter P. Sulfated hyaluronan derivatives reduce the proliferation rate of primary rat calvarial osteoblasts. Glycoconj J. 2010. doi:10.1007/s10719-009-9270-9.

    Google Scholar 

  20. Becher J, Möller S, Weiss D, Schiller J, Schnabelrauch M. Synthesis of new regioselectively sulfated hyaluronans for biomedical application. Macromol Symp. 2010;269:446–52.

    Article  Google Scholar 

  21. Bierbaum S, Douglas T, Hanke T, Scharnweber D, Tippelt S, Monsees TK, Funk RHW, Worch H. Collageneous matrix coatings on titanium implants modified with decorin and chondroitin sulfate: characterization and influence on osteoblastic cells. J Biomed Mater Res A. 2006. doi:10.1002/jbm.a.30572.

    Google Scholar 

  22. Junqueira LC, Bignolas G, Mourao PA, Bonetti SS. Quantitation of collagen-proteoglycan interaction in tissue sections. Connect Tissue Res. 1980;7(2):91–6.

    Article  Google Scholar 

  23. Walsh BJ, Thornton SC, Penny R, Breit SN. Microplate reader-based quantitation of collagens. Anal Biochem. 1992;203(2):187–90.

    Article  Google Scholar 

  24. Farndale RW, Buttle DJ, Barrett AJ. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta. 1986;883(2):173–7.

    Article  Google Scholar 

  25. Donath K, Breuner G. A method for the study of undecalcified bones and teeth with attached soft tissues. The Sage-Schliff (sawing and grinding) technique. J Oral Pathol. 1982;11(4):318–26.

    Article  Google Scholar 

  26. Friberg B, Jemt T, Lekholm U. Early failures in 4,641 consecutively placed Brånemark dental implants: a study from stage 1 surgery to the connection of completed prostheses. Int J Oral Maxillofac Implants. 1991;6(2):142–6.

    Google Scholar 

  27. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. J Periodontol. 1991. doi:10.1902/jop.1991.62.1.2.

    Google Scholar 

  28. Schliephake H, Aref A, Scharnweber D, Bierbaum S, Sewing A. Effect of modifications of dual acid-etched implant surfaces on peri-implant bone formation. Part I: organic coatings. Clin Oral Implants Res. 2009. doi:10.1111/j.1600-0501.2008.01603.x.

    Google Scholar 

  29. Stadlinger B, Pilling E, Huhle M, Mai R, Bierbaum S, Bernhardt R, Scharnweber D, Kuhlisch E, Hempel U, Eckelt U. Influence of extracellular matrix coatings on implant stability and osseointegration: an animal study. J Biomed Mater Res Part B Appl Biomater. 2007. doi:10.1002/jbm.b.30787.

    Google Scholar 

  30. Stadlinger B, Hintze V, Bierbaum S, Moller S, Schulz MC, Mai R, Kuhlisch E, Heinemann S, Scharnweber D, Schnabelrauch M, Eckelt U. Biological functionalization of dental implants with collagen and glycosaminoglycans-a comparative study. J Biomed Mater Res A. 2011. doi:10.1002/jbm.b.31953.

    Google Scholar 

  31. Wang S, Liu Y, Fang D, Shi S. The miniature pig: a useful large animal model for dental and orofacial research. Oral Dis. 2007. doi:10.1111/j.1601-0825.2006.01337.x.

    Google Scholar 

  32. Weaver ME, Sorenson FM, Jump EB. The miniature pig as an experimental animal in dental research. Arch Oral Biol. 1962;7:17–23.

    Article  Google Scholar 

  33. Misch CE. Density of bone: effect on treatment plans, surgical approach, healing, and progressive boen loading. Int J Oral Implantol. 1990;6(2):23–31.

    Google Scholar 

  34. Germanier Y, Tosatti S, Broggini N, Textor M, Buser D. Enhanced bone apposition around biofunctionalized sandblasted and acid-etched titanium implant surfaces. A histomorphometric study in miniature pigs. Clin Oral Implants Res. 2006. doi:10.1111/j.1600-0501.2005.01222.x.

    Google Scholar 

  35. Hermann JS, Jones AA, Bakaeen LG, Buser D, Schoolfield JD, Cochran DL. Influence of a machined collar on crestal bone changes around titanium implants: a histometric study in the canine mandible. J Periodontol. 2011. doi:10.1902/jop.2011.090728.

    Google Scholar 

  36. Bernhardt R, Kuhlisch E, Schulz MC, Eckelt U, Stadlinger B. Comparison of bone-implant contact and bone-implant volume between 2D-histological sections and 3D-SRmicroCT slices. Eur Cell Mater. 2012;23:237–47 discussion 247–8.

    Google Scholar 

  37. Rammelt S, Illert T, Bierbaum S, Scharnweber D, Zwipp H, Schneiders W. Coating of titanium implants with collagen. RGD peptide and chondroitin sulfate. Biomaterials. 2006. doi:10.1016/j.biomaterials.2006.06.034.

    Google Scholar 

  38. Kajahn J, Franz S, Rueckert E, Forstreuter I, Hintze V, Moeller S, Simon JC. Artificial extracellular matrices composed of collagen I and high sulfated hyaluronan modulate monocyte to macrophage differentiation under conditions of sterile inflammation. Biomatter. 2012. doi:10.4161/biom.22855.

    Google Scholar 

  39. Astachov L, Vago R, Aviv M, Nevo Z. Hyaluronan and mesenchymal stem cells: from germ layer to cartilage and bone. Front Biosci. 2011;16:261–76.

    Article  Google Scholar 

  40. Bastow ER, Byers S, Golub SB, Clarkin CE, Pitsillides AA, Fosang AJ. Hyaluronan synthesis and degradation in cartilage and bone. Cell Mol Life Sci. 2008. doi:10.1007/s00018-007-7360-z.

    Google Scholar 

  41. Itoh S, Matubara M, Kawauchi T, Nakamura H, Yukitake S, Ichinose S, Shinomiya K. Enhancement of bone ingrowth in a titanium fiber mesh implant by rhBMP-2 and hyaluronic acid. J Mater Sci Mater Med. 2001;12(7):575–81.

    Article  Google Scholar 

  42. Morra M, Cassinelli C, Cascardo G, Fini M, Giavaresi G, Giardino R. Covalently-linked hyaluronan promotes bone formation around Ti implants in a rabbit model. J Orthop Res. 2009. doi:10.1002/jor.20797.

    Google Scholar 

  43. Stadlinger B, Bierbaum S, Grimmer S, Schulz MC, Kuhlisch E, Scharnweber D, Eckelt U, Mai R. Increased bone formation around coated implants. J Clin Periodontol. 2009. doi:10.1111/j.1600-051X.2009.01435.x.

    Google Scholar 

  44. Rutten S, Nolte PA, Korstjens CM, van Duin MA, Klein-Nulend J. Low-intensity pulsed ultrasound increases bone volume, osteoid thickness and mineral apposition rate in the area of fracture healing in patients with a delayed union of the osteotomized fibula. Bone. 2008. doi:10.1016/j.bone.2008.04.010.

    Google Scholar 

  45. Terheyden H, Lang NP, Bierbaum S, Stadlinger B. Osseointegration–communication of cells. Clin Oral Implants Res. 2012. doi:10.1111/j.1600-0501.2011.02327.x.

    Google Scholar 

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Acknowledgments

The study was supported by the Transregio 67 grant of the German Research Foundation DFG (A2, A3, B6). The implants were donated by Thommen Medical AG, Waldenburg, Switzerland. The authors are grateful to Dr. Roland Jung and Dr. Kathrin Spekl for their support during the animal experiments. Furthermore, the authors wish to thank Diana Jünger, Heike Zimmermann and Sarah Beckmann for their excellent technical assistance.

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Authors and Affiliations

  1. Department of Oral and Maxillofacial Surgery, Medical Faculty “Carl Gustav Carus”, Technische Universität Dresden, Fetscherstraße 74, 01307, Dresden, Germany

    Matthias C. Schulz, Paula Korn, Ronald Mai & Uwe Eckelt

  2. Clinic of Cranio-Maxillofacial and Oral Surgery, University of Zurich, Plattenstr. 11, 8032, Zurich, Switzerland

    Bernd Stadlinger

  3. Institute for Medical Informatics and Biometry, Medical Faculty “Carl Gustav Carus” Technische Universität Dresden, Blasewitzer Str. 86, 01309, Dresden, Germany

    Ursula Range

  4. Biomaterials Department, INNOVENT e.V., Prüssingstrasse 27 B, 07745, Jena, Germany

    Stephanie Möller, Jana Becher & Matthias Schnabelrauch

  5. Institute of Materials Science, Max-Bergmann-Center of Biomaterials, Technische Universität Dresden, Budapester Str. 27, 01062, Dresden, Germany

    Dieter Scharnweber & Vera Hintze

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  1. Matthias C. Schulz
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  2. Paula Korn
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Correspondence to Matthias C. Schulz.

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Schulz, M.C., Korn, P., Stadlinger, B. et al. Coating with artificial matrices from collagen and sulfated hyaluronan influences the osseointegration of dental implants. J Mater Sci: Mater Med 25, 247–258 (2014). https://doi.org/10.1007/s10856-013-5066-3

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