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Published in: International Journal of Implant Dentistry 1/2015

Open Access 01-12-2015 | Review

Genomic analyses of early peri-implant bone healing in humans: a systematic review

Authors: Siddharth Shanbhag, Vivek Shanbhag, Andreas Stavropoulos

Published in: International Journal of Implant Dentistry | Issue 1/2015

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Abstract

Objective

The objective of the study was to systematically review the literature for studies reporting gene expression analyses (GEA) of the biological processes involved in early human peri-implant bone healing.

Methods

Electronic databases (MEDLINE, EMBASE) were searched in duplicate. Controlled and uncontrolled studies reporting GEA of human peri-implant tissues - including ≥5 patients and ≥2 time points - during the first 4 weeks of healing were eligible for inclusion. Methodological quality and risk of bias were also assessed.

Results

Four exploratory studies were included in reporting GEA of either tissues attached to SLA or SLActive implants after 4 to 14 days or cells attached to TiOBlast or Osseospeed implants after 3 to 7 days. A total of 111 implants from 43 patients were analyzed using validated array methods; however, considerable heterogeneity and risk of bias were detected. A consistent overall pattern of gene expression was observed; genes representing an immuno-inflammatory response were overexpressed at days 3 to 4, followed by genes representing osteogenic processes at day 7. Genes representing bone remodeling, angiogenesis, and neurogenesis were expressed concomitantly with osteogenesis. Several regulators of these processes, such as cytokines, growth factors, transcription factors, and signaling pathways, were identified. Implant surface properties seemed to influence the healing processes at various stages via differential gene expression.

Conclusion

Limited evidence from gene expression studies in humans indicates that osteogenic processes commence within the first post-operative week and they appear influenced at various stages by implant surface properties.
Literature
1.
go back to reference Setzer FC, Kim S. Comparison of long-term survival of implants and endodontically treated teeth. J Dent Res. 2014;93(1):19–26. doi:10.1177/0022034513504782.CrossRefPubMedCentralPubMed Setzer FC, Kim S. Comparison of long-term survival of implants and endodontically treated teeth. J Dent Res. 2014;93(1):19–26. doi:10.1177/0022034513504782.CrossRefPubMedCentralPubMed
2.
go back to reference Albrektsson T, Brånemark PI, Hansson HA, Lindström J. Osseointegrated titanium implants. Requirements for ensuring a long-lasting, direct bone-to-implant anchorage in man. Acta Orthop Scand. 1981;52(2):155–70.CrossRefPubMed Albrektsson T, Brånemark PI, Hansson HA, Lindström J. Osseointegrated titanium implants. Requirements for ensuring a long-lasting, direct bone-to-implant anchorage in man. Acta Orthop Scand. 1981;52(2):155–70.CrossRefPubMed
3.
go back to reference Berglundh T, Abrahamsson I, Lang NP, Lindhe J. De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res. 2003;14(3):251–62. doi:972.CrossRefPubMed Berglundh T, Abrahamsson I, Lang NP, Lindhe J. De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res. 2003;14(3):251–62. doi:972.CrossRefPubMed
4.
go back to reference Abrahamsson I, Berglundh T, Linder E, Lang NP, Lindhe J. Early bone formation adjacent to rough and turned endosseous implant surfaces. An experimental study in the dog. Clin Oral Implants Res. 2004;15(4):381–92. doi: 10.1111/j.1600-0501.2004.01082.x.CrossRefPubMed Abrahamsson I, Berglundh T, Linder E, Lang NP, Lindhe J. Early bone formation adjacent to rough and turned endosseous implant surfaces. An experimental study in the dog. Clin Oral Implants Res. 2004;15(4):381–92. doi: 10.1111/j.1600-0501.2004.01082.x.CrossRefPubMed
5.
go back to reference Lang NP, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, Bosshardt DD. Early osseointegration to hydrophilic and hydrophobic implant surfaces in humans. Clin Oral Implants Res. 2011;22(4):349–56. doi:10.1111/j.1600-0501.2011.02172.x.CrossRefPubMed Lang NP, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, Bosshardt DD. Early osseointegration to hydrophilic and hydrophobic implant surfaces in humans. Clin Oral Implants Res. 2011;22(4):349–56. doi:10.1111/j.1600-0501.2011.02172.x.CrossRefPubMed
6.
go back to reference Bosshardt DD, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, Lang NP. The role of bone debris in early healing adjacent to hydrophilic and hydrophobic implant surfaces in man. Clin Oral Implants Res. 2011;22(4):357–64. doi:10.1111/j.1600-0501.2010.02107.x.CrossRefPubMed Bosshardt DD, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, Lang NP. The role of bone debris in early healing adjacent to hydrophilic and hydrophobic implant surfaces in man. Clin Oral Implants Res. 2011;22(4):357–64. doi:10.1111/j.1600-0501.2010.02107.x.CrossRefPubMed
7.
go back to reference Terheyden H, Lang NP, Bierbaum S, Stadlinger B. Osseointegration - communication of cells. Clin Oral Implants Res. 2012;23(10):1127–35. doi:10.1111/j.1600-0501.2011.02327.x.CrossRefPubMed Terheyden H, Lang NP, Bierbaum S, Stadlinger B. Osseointegration - communication of cells. Clin Oral Implants Res. 2012;23(10):1127–35. doi:10.1111/j.1600-0501.2011.02327.x.CrossRefPubMed
8.
go back to reference Marco F, Milena F, Gianluca G, Vittoria O. Peri-implant osteogenesis in health and osteoporosis. Micron. 2005;36(7–8):630–44. doi:10.1016/j.micron.2005.07.008.CrossRefPubMed Marco F, Milena F, Gianluca G, Vittoria O. Peri-implant osteogenesis in health and osteoporosis. Micron. 2005;36(7–8):630–44. doi:10.1016/j.micron.2005.07.008.CrossRefPubMed
9.
go back to reference Sela J, Gross UM, Kohavi D, Shani J, Dean DD, Boyan BD, et al. Primary mineralization at the surfaces of implants. Crit Rev Oral Biol Med. 2000;11(4):423–36.CrossRefPubMed Sela J, Gross UM, Kohavi D, Shani J, Dean DD, Boyan BD, et al. Primary mineralization at the surfaces of implants. Crit Rev Oral Biol Med. 2000;11(4):423–36.CrossRefPubMed
10.
go back to reference Raghavendra S, Wood MC, Taylor TD. Early wound healing around endosseous implants: a review of the literature. Int J Oral Maxillofac Implants. 2005;20(3):425–31.PubMed Raghavendra S, Wood MC, Taylor TD. Early wound healing around endosseous implants: a review of the literature. Int J Oral Maxillofac Implants. 2005;20(3):425–31.PubMed
11.
go back to reference Kanczler JM, Oreffo RO. Osteogenesis and angiogenesis: the potential for engineering bone. Eur Cell Mater. 2008;15:100–14.PubMed Kanczler JM, Oreffo RO. Osteogenesis and angiogenesis: the potential for engineering bone. Eur Cell Mater. 2008;15:100–14.PubMed
12.
go back to reference Sağirkaya E, Kucukekenci AS, Karasoy D, Akça K, Eckert SE, Çehreli MC. Comparative assessments, meta-analysis, and recommended guidelines for reporting studies on histomorphometric bone-implant contact in humans. Int J Oral Maxillofac Implants. 2013;28(5):1243–53.CrossRefPubMed Sağirkaya E, Kucukekenci AS, Karasoy D, Akça K, Eckert SE, Çehreli MC. Comparative assessments, meta-analysis, and recommended guidelines for reporting studies on histomorphometric bone-implant contact in humans. Int J Oral Maxillofac Implants. 2013;28(5):1243–53.CrossRefPubMed
13.
go back to reference Kojima N, Ozawa S, Miyata Y, Hasegawa H, Tanaka Y, Ogawa T. High-throughput gene expression analysis in bone healing around titanium implants by DNA microarray. Clin Oral Implants Res. 2008;19(2):173–81. doi:10.1111/j.1600-0501.2007.01432.x.CrossRefPubMed Kojima N, Ozawa S, Miyata Y, Hasegawa H, Tanaka Y, Ogawa T. High-throughput gene expression analysis in bone healing around titanium implants by DNA microarray. Clin Oral Implants Res. 2008;19(2):173–81. doi:10.1111/j.1600-0501.2007.01432.x.CrossRefPubMed
14.
go back to reference Lin Z, Rios HF, Volk SL, Sugai JV, Jin Q, Giannobile WV. Gene expression dynamics during bone healing and osseointegration. J Periodontol. 2011;82(7):1007–17. doi:10.1902/jop.2010.100577.CrossRefPubMedCentralPubMed Lin Z, Rios HF, Volk SL, Sugai JV, Jin Q, Giannobile WV. Gene expression dynamics during bone healing and osseointegration. J Periodontol. 2011;82(7):1007–17. doi:10.1902/jop.2010.100577.CrossRefPubMedCentralPubMed
15.
go back to reference Ai-Aql ZS, Alagl AS, Graves DT, Gerstenfeld LC, Einhorn TA. Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res. 2008;87(2):107–18.CrossRefPubMedCentralPubMed Ai-Aql ZS, Alagl AS, Graves DT, Gerstenfeld LC, Einhorn TA. Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res. 2008;87(2):107–18.CrossRefPubMedCentralPubMed
16.
go back to reference Albrektsson T, Johansson C. Osteoinduction, osteoconduction and osseointegration. Eur Spine J. 2001;10 Suppl 2:S96–101. doi:10.1007/s005860100282.PubMedCentralPubMed Albrektsson T, Johansson C. Osteoinduction, osteoconduction and osseointegration. Eur Spine J. 2001;10 Suppl 2:S96–101. doi:10.1007/s005860100282.PubMedCentralPubMed
17.
go back to reference Miron RJ, Zhang YF. Osteoinduction: a review of old concepts with new standards. J Dent Res. 2012;91(8):736–44. doi:10.1177/0022034511435260.CrossRefPubMed Miron RJ, Zhang YF. Osteoinduction: a review of old concepts with new standards. J Dent Res. 2012;91(8):736–44. doi:10.1177/0022034511435260.CrossRefPubMed
18.
go back to reference Ito H. Chemokines in mesenchymal stem cell therapy for bone repair: a novel concept of recruiting mesenchymal stem cells and the possible cell sources. Mod Rheumatol. 2011;21(2):113–21. doi:10.1007/s10165-010-0357-8.CrossRefPubMed Ito H. Chemokines in mesenchymal stem cell therapy for bone repair: a novel concept of recruiting mesenchymal stem cells and the possible cell sources. Mod Rheumatol. 2011;21(2):113–21. doi:10.1007/s10165-010-0357-8.CrossRefPubMed
19.
go back to reference Hughes FJ, Turner W, Belibasakis G, Martuscelli G. Effects of growth factors and cytokines on osteoblast differentiation. Periodontol 2000. 2006;41:48–72. doi:10.1111/j.1600-0757.2006.00161.x.CrossRefPubMed Hughes FJ, Turner W, Belibasakis G, Martuscelli G. Effects of growth factors and cytokines on osteoblast differentiation. Periodontol 2000. 2006;41:48–72. doi:10.1111/j.1600-0757.2006.00161.x.CrossRefPubMed
20.
go back to reference Scheller EL, Krebsbach PH. The use of soluble signals to harness the power of the bone microenvironment for implant therapeutics. Int J Oral Maxillofac Implants. 2011;26(Suppl):70–9. discussion 80–4.PubMedCentralPubMed Scheller EL, Krebsbach PH. The use of soluble signals to harness the power of the bone microenvironment for implant therapeutics. Int J Oral Maxillofac Implants. 2011;26(Suppl):70–9. discussion 80–4.PubMedCentralPubMed
21.
go back to reference Marie PJ. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys. 2008;473(2):98–105. doi:10.1016/j.abb.2008.02.030.CrossRefPubMed Marie PJ. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys. 2008;473(2):98–105. doi:10.1016/j.abb.2008.02.030.CrossRefPubMed
22.
go back to reference Fakhry M, Hamade E, Badran B, Buchet R, Magne D. Molecular mechanisms of mesenchymal stem cell differentiation towards osteoblasts. World J Stem Cells. 2013;5(4):136–48. doi: 10.4252/wjsc.v5.i4.136.CrossRefPubMedCentralPubMed Fakhry M, Hamade E, Badran B, Buchet R, Magne D. Molecular mechanisms of mesenchymal stem cell differentiation towards osteoblasts. World J Stem Cells. 2013;5(4):136–48. doi: 10.4252/wjsc.v5.i4.136.CrossRefPubMedCentralPubMed
23.
go back to reference Minkin C, Marinho VC. Role of the osteoclast at the bone-implant interface. Adv Dent Res. 1999;13:49–56.CrossRefPubMed Minkin C, Marinho VC. Role of the osteoclast at the bone-implant interface. Adv Dent Res. 1999;13:49–56.CrossRefPubMed
24.
go back to reference Thalji G, Cooper L. Molecular assessment of osseointegration in vitro: a review of the current literature. Oral & Craniofacial Tissue Engineering. 2012;2(3):221–49. Thalji G, Cooper L. Molecular assessment of osseointegration in vitro: a review of the current literature. Oral & Craniofacial Tissue Engineering. 2012;2(3):221–49.
25.
go back to reference Thalji G, Cooper LF. Molecular assessment of osseointegration in vivo: a review of the current literature. Int J Oral Maxillofac Implants. 2013;28(6):e521–34.CrossRefPubMed Thalji G, Cooper LF. Molecular assessment of osseointegration in vivo: a review of the current literature. Int J Oral Maxillofac Implants. 2013;28(6):e521–34.CrossRefPubMed
26.
go back to reference Cooper LF. Biologic determinants of bone formation for osseointegration: clues for future clinical improvements. J Prosthet Dent. 1998;80(4):439–49.CrossRefPubMed Cooper LF. Biologic determinants of bone formation for osseointegration: clues for future clinical improvements. J Prosthet Dent. 1998;80(4):439–49.CrossRefPubMed
27.
go back to reference Omar OM, Lennerås ME, Suska F, Emanuelsson L, Hall JM, Palmquist A, et al. The correlation between gene expression of proinflammatory markers and bone formation during osseointegration with titanium implants. Biomaterials. 2011;32(2):374–86. doi:10.1016/j.biomaterials.2010.09.011.CrossRefPubMed Omar OM, Lennerås ME, Suska F, Emanuelsson L, Hall JM, Palmquist A, et al. The correlation between gene expression of proinflammatory markers and bone formation during osseointegration with titanium implants. Biomaterials. 2011;32(2):374–86. doi:10.1016/j.biomaterials.2010.09.011.CrossRefPubMed
29.
go back to reference Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org; 2011. Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.​cochrane-handbook.​org; 2011.
30.
go back to reference Tarca AL, Romero R, Draghici S. Analysis of microarray experiments of gene expression profiling. Am J Obstet Gynecol. 2006;195(2):373–88. doi:10.1016/j.ajog.2006.07.001.CrossRefPubMedCentralPubMed Tarca AL, Romero R, Draghici S. Analysis of microarray experiments of gene expression profiling. Am J Obstet Gynecol. 2006;195(2):373–88. doi:10.1016/j.ajog.2006.07.001.CrossRefPubMedCentralPubMed
31.
32.
go back to reference Nibali L. Suggested guidelines for systematic reviews of periodontal genetic association studies. J Clin Periodontol. 2013;40(8):753–6. doi:10.1111/jcpe.12128.CrossRefPubMed Nibali L. Suggested guidelines for systematic reviews of periodontal genetic association studies. J Clin Periodontol. 2013;40(8):753–6. doi:10.1111/jcpe.12128.CrossRefPubMed
33.
go back to reference Little J, Higgins JP, Ioannidis JP, Moher D, Gagnon F, von Elm E, et al. Strengthening the reporting of genetic association studies (STREGA): an extension of the STROBE statement. PLoS Med. 2009;6(2):e22. doi:10.1371/journal.pmed.1000022.CrossRefPubMed Little J, Higgins JP, Ioannidis JP, Moher D, Gagnon F, von Elm E, et al. Strengthening the reporting of genetic association studies (STREGA): an extension of the STROBE statement. PLoS Med. 2009;6(2):e22. doi:10.1371/journal.pmed.1000022.CrossRefPubMed
34.
go back to reference Ivanovski S, Hamlet S, Salvi GE, Huynh-Ba G, Bosshardt DD, Lang NP, et al. Transcriptional profiling of osseointegration in humans. Clin Oral Implants Res. 2011;22(4):373–81. doi:10.1111/j.1600-0501.2010.02112.x.CrossRefPubMed Ivanovski S, Hamlet S, Salvi GE, Huynh-Ba G, Bosshardt DD, Lang NP, et al. Transcriptional profiling of osseointegration in humans. Clin Oral Implants Res. 2011;22(4):373–81. doi:10.1111/j.1600-0501.2010.02112.x.CrossRefPubMed
35.
go back to reference Donos N, Hamlet S, Lang NP, Salvi GE, Huynh-Ba G, Bosshardt DD, et al. Gene expression profile of osseointegration of a hydrophilic compared with a hydrophobic microrough implant surface. Clin Oral Implants Res. 2011;22(4):365–72. doi:10.1111/j.1600-0501.2010.02113.x.CrossRefPubMed Donos N, Hamlet S, Lang NP, Salvi GE, Huynh-Ba G, Bosshardt DD, et al. Gene expression profile of osseointegration of a hydrophilic compared with a hydrophobic microrough implant surface. Clin Oral Implants Res. 2011;22(4):365–72. doi:10.1111/j.1600-0501.2010.02113.x.CrossRefPubMed
36.
go back to reference Bryington M, Mendonça G, Nares S, Cooper LF. Osteoblastic and cytokine gene expression of implant-adherent cells in humans. Clin Oral Implants Res. 2012; doi:10.1111/clr.12054. Bryington M, Mendonça G, Nares S, Cooper LF. Osteoblastic and cytokine gene expression of implant-adherent cells in humans. Clin Oral Implants Res. 2012; doi:10.1111/clr.12054.
37.
go back to reference Thalji GN, Nares S, Cooper LF. Early molecular assessment of osseointegration in humans. Clin Oral Implants Res. 2013; doi:10.1111/clr.12266. Thalji GN, Nares S, Cooper LF. Early molecular assessment of osseointegration in humans. Clin Oral Implants Res. 2013; doi:10.1111/clr.12266.
38.
go back to reference Morey JS, Ryan JC, Van Dolah FM. Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online. 2006;8:175–93. doi:10.1251/bpo126.CrossRefPubMedCentralPubMed Morey JS, Ryan JC, Van Dolah FM. Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online. 2006;8:175–93. doi:10.1251/bpo126.CrossRefPubMedCentralPubMed
39.
go back to reference Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res. 2001;125(1–2):279–84.CrossRefPubMed Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res. 2001;125(1–2):279–84.CrossRefPubMed
40.
go back to reference Alfarsi MA, Hamlet SM, Ivanovski S. Titanium surface hydrophilicity modulates the human macrophage inflammatory cytokine response. J Biomed Mater Res A. 2013; doi:10.1002/jbm.a.34666. Alfarsi MA, Hamlet SM, Ivanovski S. Titanium surface hydrophilicity modulates the human macrophage inflammatory cytokine response. J Biomed Mater Res A. 2013; doi:10.1002/jbm.a.34666.
41.
go back to reference Pajarinen J, Kouri VP, Jämsen E, Li TF, Mandelin J, Konttinen YT. The response of macrophages to titanium particles is determined by macrophage polarization. Acta Biomater. 2013;9(11):9229–40. doi:10.1016/j.actbio.2013.06.027.CrossRefPubMed Pajarinen J, Kouri VP, Jämsen E, Li TF, Mandelin J, Konttinen YT. The response of macrophages to titanium particles is determined by macrophage polarization. Acta Biomater. 2013;9(11):9229–40. doi:10.1016/j.actbio.2013.06.027.CrossRefPubMed
42.
go back to reference Chehroudi B, Ghrebi S, Murakami H, Waterfield JD, Owen G, Brunette DM. Bone formation on rough, but not polished, subcutaneously implanted Ti surfaces is preceded by macrophage accumulation. J Biomed Mater Res A. 2010;93(2):724–37. doi:10.1002/jbm.a.32587.PubMed Chehroudi B, Ghrebi S, Murakami H, Waterfield JD, Owen G, Brunette DM. Bone formation on rough, but not polished, subcutaneously implanted Ti surfaces is preceded by macrophage accumulation. J Biomed Mater Res A. 2010;93(2):724–37. doi:10.1002/jbm.a.32587.PubMed
43.
go back to reference Heng BC, Cao T, Stanton LW, Robson P, Olsen B. Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro. J Bone Miner Res. 2004;19(9):1379–94. doi:10.1359/JBMR.040714.CrossRefPubMed Heng BC, Cao T, Stanton LW, Robson P, Olsen B. Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro. J Bone Miner Res. 2004;19(9):1379–94. doi:10.1359/JBMR.040714.CrossRefPubMed
44.
go back to reference Dhore CR, Snel SJ, Jacques SV, Naert IE, Walboomers XF, Jansen JA. In vitro osteogenic potential of bone debris resulting from placement of titanium screw-type implants. Clin Oral Implants Res. 2008;19(6):606–11. doi:10.1111/j.1600-0501.2007.01519.x.CrossRefPubMed Dhore CR, Snel SJ, Jacques SV, Naert IE, Walboomers XF, Jansen JA. In vitro osteogenic potential of bone debris resulting from placement of titanium screw-type implants. Clin Oral Implants Res. 2008;19(6):606–11. doi:10.1111/j.1600-0501.2007.01519.x.CrossRefPubMed
45.
go back to reference Kim DH, Yoo KH, Choi KS, Choi J, Choi SY, Yang SE, et al. Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine. 2005;31(2):119–26. doi:10.1016/j.cyto.2005.04.004.CrossRefPubMed Kim DH, Yoo KH, Choi KS, Choi J, Choi SY, Yang SE, et al. Gene expression profile of cytokine and growth factor during differentiation of bone marrow-derived mesenchymal stem cell. Cytokine. 2005;31(2):119–26. doi:10.1016/j.cyto.2005.04.004.CrossRefPubMed
46.
go back to reference Omar O, Svensson S, Zoric N, Lenneras M, Suska F, Wigren S, et al. In vivo gene expression in response to anodically oxidized versus machined titanium implants. J Biomed Mater Res A. 2010;92(4):1552–66. doi:10.1002/jbm.a.32475.PubMed Omar O, Svensson S, Zoric N, Lenneras M, Suska F, Wigren S, et al. In vivo gene expression in response to anodically oxidized versus machined titanium implants. J Biomed Mater Res A. 2010;92(4):1552–66. doi:10.1002/jbm.a.32475.PubMed
47.
go back to reference Marcellini S, Henriquez JP, Bertin A. Control of osteogenesis by the canonical Wnt and BMP pathways in vivo: cooperation and antagonism between the canonical Wnt and BMP pathways as cells differentiate from osteochondroprogenitors to osteoblasts and osteocytes. Bioessays. 2012;34(11):953–62. doi:10.1002/bies.201200061.CrossRefPubMed Marcellini S, Henriquez JP, Bertin A. Control of osteogenesis by the canonical Wnt and BMP pathways in vivo: cooperation and antagonism between the canonical Wnt and BMP pathways as cells differentiate from osteochondroprogenitors to osteoblasts and osteocytes. Bioessays. 2012;34(11):953–62. doi:10.1002/bies.201200061.CrossRefPubMed
48.
go back to reference Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002;108(1):17–29.CrossRefPubMed Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002;108(1):17–29.CrossRefPubMed
49.
go back to reference Komori T. Regulation of osteoblast differentiation by Runx2. Adv Exp Med Biol. 2010;658:43–9. doi:10.1007/978-1-4419-1050-9_5.CrossRefPubMed Komori T. Regulation of osteoblast differentiation by Runx2. Adv Exp Med Biol. 2010;658:43–9. doi:10.1007/978-1-4419-1050-9_5.CrossRefPubMed
50.
go back to reference Guo J, Padilla RJ, Ambrose W, De Kok IJ, Cooper LF. The effect of hydrofluoric acid treatment of TiO2 grit blasted titanium implants on adherent osteoblast gene expression in vitro and in vivo. Biomaterials. 2007;28(36):5418–25. doi:10.1016/j.biomaterials.2007.08.032.CrossRefPubMed Guo J, Padilla RJ, Ambrose W, De Kok IJ, Cooper LF. The effect of hydrofluoric acid treatment of TiO2 grit blasted titanium implants on adherent osteoblast gene expression in vitro and in vivo. Biomaterials. 2007;28(36):5418–25. doi:10.1016/j.biomaterials.2007.08.032.CrossRefPubMed
51.
go back to reference Mendonça G, Mendonça DB, Simões LG, Araújo AL, Leite ER, Duarte WR, et al. Nanostructured alumina-coated implant surface: effect on osteoblast-related gene expression and bone-to-implant contact in vivo. Int J Oral Maxillofac Implants. 2009;24(2):205–15.PubMed Mendonça G, Mendonça DB, Simões LG, Araújo AL, Leite ER, Duarte WR, et al. Nanostructured alumina-coated implant surface: effect on osteoblast-related gene expression and bone-to-implant contact in vivo. Int J Oral Maxillofac Implants. 2009;24(2):205–15.PubMed
52.
go back to reference Rocci M, Rocci A, Martignoni M, Albrektsson T, Barlattani A, Gargari M. Comparing the TiOblast and Osseospeed surfaces. Histomorphometric and histological analysis in humans. Oral Implantol (Rome). 2008;1(1):34–42. Rocci M, Rocci A, Martignoni M, Albrektsson T, Barlattani A, Gargari M. Comparing the TiOblast and Osseospeed surfaces. Histomorphometric and histological analysis in humans. Oral Implantol (Rome). 2008;1(1):34–42.
53.
go back to reference Qin C, Baba O, Butler WT. Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med. 2004;15(3):126–36.CrossRefPubMed Qin C, Baba O, Butler WT. Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med. 2004;15(3):126–36.CrossRefPubMed
54.
go back to reference Vlacic-Zischke J, Hamlet SM, Friis T, Tonetti MS, Ivanovski S. The influence of surface microroughness and hydrophilicity of titanium on the up-regulation of TGFβ/BMP signalling in osteoblasts. Biomaterials. 2011;32(3):665–71. doi:10.1016/j.biomaterials.2010.09.025.CrossRefPubMed Vlacic-Zischke J, Hamlet SM, Friis T, Tonetti MS, Ivanovski S. The influence of surface microroughness and hydrophilicity of titanium on the up-regulation of TGFβ/BMP signalling in osteoblasts. Biomaterials. 2011;32(3):665–71. doi:10.1016/j.biomaterials.2010.09.025.CrossRefPubMed
55.
go back to reference Viguet-Carrin S, Garnero P, Delmas PD. The role of collagen in bone strength. Osteoporos Int. 2006;17(3):319–36. doi:10.1007/s00198-005-2035-9.CrossRefPubMed Viguet-Carrin S, Garnero P, Delmas PD. The role of collagen in bone strength. Osteoporos Int. 2006;17(3):319–36. doi:10.1007/s00198-005-2035-9.CrossRefPubMed
56.
go back to reference Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2):195–214. doi:10.1007/s00198-009-1066-z.CrossRefPubMed Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2):195–214. doi:10.1007/s00198-009-1066-z.CrossRefPubMed
57.
go back to reference Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M. Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J Bone Miner Res. 2004;19(8):1349–55. doi:10.1359/JBMR.040323.CrossRefPubMed Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M. Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J Bone Miner Res. 2004;19(8):1349–55. doi:10.1359/JBMR.040323.CrossRefPubMed
58.
go back to reference Kaku M, Mochida Y, Atsawasuwan P, Parisuthiman D, Yamauchi M. Post-translational modifications of collagen upon BMP-induced osteoblast differentiation. Biochem Biophys Res Commun. 2007;359(3):463–8. doi:10.1016/j.bbrc.2007.05.109.CrossRefPubMedCentralPubMed Kaku M, Mochida Y, Atsawasuwan P, Parisuthiman D, Yamauchi M. Post-translational modifications of collagen upon BMP-induced osteoblast differentiation. Biochem Biophys Res Commun. 2007;359(3):463–8. doi:10.1016/j.bbrc.2007.05.109.CrossRefPubMedCentralPubMed
59.
60.
go back to reference Mamalis AA, Markopoulou C, Vrotsos I, Koutsilirieris M. Chemical modification of an implant surface increases osteogenesis and simultaneously reduces osteoclastogenesis: an in vitro study. Clin Oral Implants Res. 2011;22(6):619–26. doi:10.1111/j.1600-0501.2010.02027.x.CrossRefPubMed Mamalis AA, Markopoulou C, Vrotsos I, Koutsilirieris M. Chemical modification of an implant surface increases osteogenesis and simultaneously reduces osteoclastogenesis: an in vitro study. Clin Oral Implants Res. 2011;22(6):619–26. doi:10.1111/j.1600-0501.2010.02027.x.CrossRefPubMed
61.
go back to reference Heppenstall RB, Grislis G, Hunt TK. Tissue gas tensions and oxygen consumption in healing bone defects. Clin Orthop Relat Res. 1975;106:357–65.CrossRefPubMed Heppenstall RB, Grislis G, Hunt TK. Tissue gas tensions and oxygen consumption in healing bone defects. Clin Orthop Relat Res. 1975;106:357–65.CrossRefPubMed
62.
go back to reference Potier E, Ferreira E, Andriamanalijaona R, Pujol JP, Oudina K, Logeart-Avramoglou D, et al. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone. 2007;40(4):1078–87. doi:10.1016/j.bone.2006.11.024.CrossRefPubMed Potier E, Ferreira E, Andriamanalijaona R, Pujol JP, Oudina K, Logeart-Avramoglou D, et al. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone. 2007;40(4):1078–87. doi:10.1016/j.bone.2006.11.024.CrossRefPubMed
63.
go back to reference Mamalis AA, Cochran DL. The role of hypoxia in the regulation of osteogenesis and angiogenesis coupling in intraoral regenerative procedures: a review of the literature. Int J Periodontics Restorative Dent. 2013. doi:10.11607/prd.0868. Mamalis AA, Cochran DL. The role of hypoxia in the regulation of osteogenesis and angiogenesis coupling in intraoral regenerative procedures: a review of the literature. Int J Periodontics Restorative Dent. 2013. doi:10.11607/prd.0868.
64.
go back to reference Nucera S, Biziato D, De Palma M. The interplay between macrophages and angiogenesis in development, tissue injury and regeneration. Int J Dev Biol. 2011;55(4–5):495–503. doi:10.1387/ijdb.103227sn.CrossRefPubMed Nucera S, Biziato D, De Palma M. The interplay between macrophages and angiogenesis in development, tissue injury and regeneration. Int J Dev Biol. 2011;55(4–5):495–503. doi:10.1387/ijdb.103227sn.CrossRefPubMed
65.
go back to reference Ziebart T, Schnell A, Walter C, Kämmerer PW, Pabst A, Lehmann KM, et al. Interactions between endothelial progenitor cells (EPC) and titanium implant surfaces. Clin Oral Investig. 2013;17(1):301–9. doi:10.1007/s00784-012-0691-7.CrossRefPubMed Ziebart T, Schnell A, Walter C, Kämmerer PW, Pabst A, Lehmann KM, et al. Interactions between endothelial progenitor cells (EPC) and titanium implant surfaces. Clin Oral Investig. 2013;17(1):301–9. doi:10.1007/s00784-012-0691-7.CrossRefPubMed
66.
go back to reference Clarkin CE, Gerstenfeld LC. VEGF and bone cell signalling: an essential vessel for communication? Cell Biochem Funct. 2013;31(1):1–11. doi:10.1002/cbf.2911.CrossRefPubMed Clarkin CE, Gerstenfeld LC. VEGF and bone cell signalling: an essential vessel for communication? Cell Biochem Funct. 2013;31(1):1–11. doi:10.1002/cbf.2911.CrossRefPubMed
67.
go back to reference Zhang F, Qiu T, Wu X, Wan C, Shi W, Wang Y, et al. Sustained BMP signaling in osteoblasts stimulates bone formation by promoting angiogenesis and osteoblast differentiation. J Bone Miner Res. 2009;24(7):1224–33. doi:10.1359/jbmr.090204.CrossRefPubMedCentralPubMed Zhang F, Qiu T, Wu X, Wan C, Shi W, Wang Y, et al. Sustained BMP signaling in osteoblasts stimulates bone formation by promoting angiogenesis and osteoblast differentiation. J Bone Miner Res. 2009;24(7):1224–33. doi:10.1359/jbmr.090204.CrossRefPubMedCentralPubMed
68.
go back to reference Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res. 2002;90(12):1243–50.CrossRefPubMed Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res. 2002;90(12):1243–50.CrossRefPubMed
69.
go back to reference Raines AL, Olivares-Navarrete R, Wieland M, Cochran DL, Schwartz Z, Boyan BD. Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy. Biomaterials. 2010;31(18):4909–17. doi:10.1016/j.biomaterials.2010.02.071.CrossRefPubMedCentralPubMed Raines AL, Olivares-Navarrete R, Wieland M, Cochran DL, Schwartz Z, Boyan BD. Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy. Biomaterials. 2010;31(18):4909–17. doi:10.1016/j.biomaterials.2010.02.071.CrossRefPubMedCentralPubMed
70.
go back to reference Schwarz F, Ferrari D, Herten M, Mihatovic I, Wieland M, Sager M, et al. Effects of surface hydrophilicity and microtopography on early stages of soft and hard tissue integration at non-submerged titanium implants: an immunohistochemical study in dogs. J Periodontol. 2007;78(11):2171–84. doi:10.1902/jop.2007.070157.CrossRefPubMed Schwarz F, Ferrari D, Herten M, Mihatovic I, Wieland M, Sager M, et al. Effects of surface hydrophilicity and microtopography on early stages of soft and hard tissue integration at non-submerged titanium implants: an immunohistochemical study in dogs. J Periodontol. 2007;78(11):2171–84. doi:10.1902/jop.2007.070157.CrossRefPubMed
71.
go back to reference Schwarz F, Herten M, Sager M, Wieland M, Dard M, Becker J. Histological and immunohistochemical analysis of initial and early osseous integration at chemically modified and conventional SLA titanium implants: preliminary results of a pilot study in dogs. Clin Oral Implants Res. 2007;18(4):481–8. doi:10.1111/j.1600-0501.2007.01341.x.CrossRefPubMed Schwarz F, Herten M, Sager M, Wieland M, Dard M, Becker J. Histological and immunohistochemical analysis of initial and early osseous integration at chemically modified and conventional SLA titanium implants: preliminary results of a pilot study in dogs. Clin Oral Implants Res. 2007;18(4):481–8. doi:10.1111/j.1600-0501.2007.01341.x.CrossRefPubMed
72.
go back to reference Lambrichts I. Histological and ultrastructural aspects of bone innervation. In: Jacobs R, editor. Osseoperception. Leuven, Belgium: UZ Leuven; 1998. p. 13–20. Lambrichts I. Histological and ultrastructural aspects of bone innervation. In: Jacobs R, editor. Osseoperception. Leuven, Belgium: UZ Leuven; 1998. p. 13–20.
73.
go back to reference Bais M, McLean J, Sebastiani P, Young M, Wigner N, Smith T, et al. Transcriptional analysis of fracture healing and the induction of embryonic stem cell-related genes. PLoS One. 2009;4(5):e5393. doi:10.1371/journal.pone.0005393.CrossRefPubMedCentralPubMed Bais M, McLean J, Sebastiani P, Young M, Wigner N, Smith T, et al. Transcriptional analysis of fracture healing and the induction of embryonic stem cell-related genes. PLoS One. 2009;4(5):e5393. doi:10.1371/journal.pone.0005393.CrossRefPubMedCentralPubMed
74.
go back to reference Ivanovski S, Hamlet S, Retzepi M, Wall I, Donos N. Transcriptional profiling of “guided bone regeneration” in a critical-size calvarial defect. Clin Oral Implants Res. 2011;22(4):382–9. doi:10.1111/j.1600-0501.2010.02104.x.CrossRefPubMed Ivanovski S, Hamlet S, Retzepi M, Wall I, Donos N. Transcriptional profiling of “guided bone regeneration” in a critical-size calvarial defect. Clin Oral Implants Res. 2011;22(4):382–9. doi:10.1111/j.1600-0501.2010.02104.x.CrossRefPubMed
75.
go back to reference Donos N, Retzepi M, Wall I, Hamlet S, Ivanovski S. In vivo gene expression profile of guided bone regeneration associated with a microrough titanium surface. Clin Oral Implants Res. 2011;22(4):390–8. doi:10.1111/j.1600-0501.2010.02105.x.CrossRefPubMed Donos N, Retzepi M, Wall I, Hamlet S, Ivanovski S. In vivo gene expression profile of guided bone regeneration associated with a microrough titanium surface. Clin Oral Implants Res. 2011;22(4):390–8. doi:10.1111/j.1600-0501.2010.02105.x.CrossRefPubMed
76.
go back to reference Skaper SD. The neurotrophin family of neurotrophic factors: an overview. Methods Mol Biol. 2012;846:1–12. doi:10.1007/978-1-61779-536-7_1.CrossRefPubMed Skaper SD. The neurotrophin family of neurotrophic factors: an overview. Methods Mol Biol. 2012;846:1–12. doi:10.1007/978-1-61779-536-7_1.CrossRefPubMed
77.
go back to reference Vaillant AR, Mazzoni I, Tudan C, Boudreau M, Kaplan DR, Miller FD. Depolarization and neurotrophins converge on the phosphatidylinositol 3-kinase-Akt pathway to synergistically regulate neuronal survival. J Cell Biol. 1999;146(5):955–66.CrossRefPubMedCentralPubMed Vaillant AR, Mazzoni I, Tudan C, Boudreau M, Kaplan DR, Miller FD. Depolarization and neurotrophins converge on the phosphatidylinositol 3-kinase-Akt pathway to synergistically regulate neuronal survival. J Cell Biol. 1999;146(5):955–66.CrossRefPubMedCentralPubMed
78.
go back to reference Wilkins A, Kemp K, Ginty M, Hares K, Mallam E, Scolding N. Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res. 2009;3(1):63–70. doi:10.1016/j.scr.2009.02.006.CrossRefPubMed Wilkins A, Kemp K, Ginty M, Hares K, Mallam E, Scolding N. Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res. 2009;3(1):63–70. doi:10.1016/j.scr.2009.02.006.CrossRefPubMed
79.
go back to reference Buma P, Elmans L, Oestreicher AB. Changes in innervation of long bones after insertion of an implant: immunocytochemical study in goats with antibodies to calcitonin gene-related peptide and B-50/GAP-43. J Orthop Res. 1995;13(4):570–7. doi:10.1002/jor.1100130412.CrossRefPubMed Buma P, Elmans L, Oestreicher AB. Changes in innervation of long bones after insertion of an implant: immunocytochemical study in goats with antibodies to calcitonin gene-related peptide and B-50/GAP-43. J Orthop Res. 1995;13(4):570–7. doi:10.1002/jor.1100130412.CrossRefPubMed
80.
go back to reference Corpas Dos Santos L, Lambrichts I, Quirynen M, Collaert B, Politis C, Vrielinck L, et al. Peri-implant bone innervation: histological findings in humans. Eur J Oral Implantol. 2014;7(3):283–92. Corpas Dos Santos L, Lambrichts I, Quirynen M, Collaert B, Politis C, Vrielinck L, et al. Peri-implant bone innervation: histological findings in humans. Eur J Oral Implantol. 2014;7(3):283–92.
81.
go back to reference Huang Y, Jacobs R, Van Dessel J, Bornstein MM, Lambrichts I, Politis C. A systematic review on the innervation of peri-implant tissues with special emphasis on the influence of implant placement and loading protocols. Clin Oral Implants Res. 2014; doi:10.1111/clr.12344. Huang Y, Jacobs R, Van Dessel J, Bornstein MM, Lambrichts I, Politis C. A systematic review on the innervation of peri-implant tissues with special emphasis on the influence of implant placement and loading protocols. Clin Oral Implants Res. 2014; doi:10.1111/clr.12344.
82.
go back to reference Abarca M, Van Steenberghe D, Malevez C, Jacobs R. The neurophysiology of osseointegrated oral implants. A clinically underestimated aspect. J Oral Rehabil. 2006;33(3):161–9. doi:10.1111/j.1365-2842.2005.01556.x.CrossRefPubMed Abarca M, Van Steenberghe D, Malevez C, Jacobs R. The neurophysiology of osseointegrated oral implants. A clinically underestimated aspect. J Oral Rehabil. 2006;33(3):161–9. doi:10.1111/j.1365-2842.2005.01556.x.CrossRefPubMed
83.
go back to reference Klineberg I, Calford MB, Dreher B, Henry P, Macefield V, Miles T, et al. A consensus statement on osseoperception. Clin Exp Pharmacol Physiol. 2005;32(1–2):145–6. doi:10.1111/j.1440-1681.2005.04144.x.CrossRefPubMed Klineberg I, Calford MB, Dreher B, Henry P, Macefield V, Miles T, et al. A consensus statement on osseoperception. Clin Exp Pharmacol Physiol. 2005;32(1–2):145–6. doi:10.1111/j.1440-1681.2005.04144.x.CrossRefPubMed
84.
go back to reference Enkling N, Utz KH, Bayer S, Stern RM. Osseoperception: active tactile sensibility of osseointegrated dental implants. Int J Oral Maxillofac Implants. 2010;25(6):1159–67.PubMed Enkling N, Utz KH, Bayer S, Stern RM. Osseoperception: active tactile sensibility of osseointegrated dental implants. Int J Oral Maxillofac Implants. 2010;25(6):1159–67.PubMed
85.
go back to reference Canuto RA, Pol R, Martinasso G, Muzio G, Gallesio G, Mozzati M. Hydroxyapatite paste Ostim, without elevation of full-thickness flaps, improves alveolar healing stimulating BMP- and VEGF-mediated signal pathways: an experimental study in humans. Clin Oral Implants Res. 2013;24 Suppl A100:42–8. doi:10.1111/j.1600-0501.2011.02363.x. Canuto RA, Pol R, Martinasso G, Muzio G, Gallesio G, Mozzati M. Hydroxyapatite paste Ostim, without elevation of full-thickness flaps, improves alveolar healing stimulating BMP- and VEGF-mediated signal pathways: an experimental study in humans. Clin Oral Implants Res. 2013;24 Suppl A100:42–8. doi:10.1111/j.1600-0501.2011.02363.x.
Metadata
Title
Genomic analyses of early peri-implant bone healing in humans: a systematic review
Authors
Siddharth Shanbhag
Vivek Shanbhag
Andreas Stavropoulos
Publication date
01-12-2015
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Implant Dentistry / Issue 1/2015
Electronic ISSN: 2198-4034
DOI
https://doi.org/10.1186/s40729-015-0006-2

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