Skip to main content
Top
Published in: International Journal of Implant Dentistry 1/2020

Open Access 01-12-2020 | Research

Surface roughness of titanium disks influences the adhesion, proliferation and differentiation of osteogenic properties derived from human

Authors: Maria Alejandra Frias Martinez, Ísis de Fátima Balderrama, Paula Stephania Brandão Hage Karam, Rodrigo Cardoso de Oliveira, Flávia Amadeu de Oliveira, Carlos Roberto Grandini, Fábio Bossoi Vicente, Andreas Stavropoulos, Mariana Schutzer Ragghianti Zangrando, Adriana Campos Passanezi Sant’Ana

Published in: International Journal of Implant Dentistry | Issue 1/2020

Login to get access

Abstract

Purpose

The aim of this study was to investigate the response of osteogenic cell lineage and gingival fibroblastic cells to different surface treatments of grade IV commercially pure Titanium (cpTi) disks.

Material and methods

Grade IV cpTi disks with different surfaces were produced: machined (M), sandblasting (B), sandblasting and acid subtraction (NP), and hydrophilic treatment (ACQ). Surface microtopography characteristics and chemical composition were investigated by scanning electron microscopy (SEM) and energy dispersive x-ray spectrometry (EDS). Adhesion and proliferation of SC-EHAD (human surgically-created early healing alveolar defects) and HGF-1 (human gingival fibroblasts) on Ti disks were investigated at 24 and 48 h, and osteogenic differentiation and mineralization were evaluated by assessing alkaline phosphatase (ALP) activity and alizarin red staining, respectively.

Results

No significant differences were found among the various surface treatments for all surface roughness parameters, except for skewness of the assessed profile (Rsk) favoring M (p = 0.035 ANOVA). M disks showed a slightly higher (p > 0.05; Kruskal-Wallis/Dunn) adhesion of HGF-1 (89.43 ± 9.13%) than SC-EHAD cells (57.11 ± 17.72%). ACQ showed a significantly higher percentage of SC-EHAD (100%) than HGF-1 (69.67 ± 13.97%) cells adhered at 24 h. SC-EHAD cells expressed increased ALP activity in osteogenic medium at M (213%) and NP (235.04%) surfaces, but higher mineralization activity on ACQ (54.94 ± 4.80%) at 14 days.

Conclusion

These findings suggest that surface treatment influences the chemical composition and the adhesion and differentiation of osteogenic cells in vitro.

Clinical relevance

Hydrophilic surface treatment of grade IV cpTi disks influences osteogenic cell adhesion and differentiation, which might enhance osseointegration.
Literature
1.
go back to reference Albrektsson T, Branemark PI, Hansson HA, Lindstrom J. Osseointegrated titanium implants. Acta Orthop Scand. 1981;52:155–70.PubMed Albrektsson T, Branemark PI, Hansson HA, Lindstrom J. Osseointegrated titanium implants. Acta Orthop Scand. 1981;52:155–70.PubMed
2.
go back to reference Albrektsson T, Wennerberg A. The impact of oral implants – past and future, 1966 – 2042. J Can Dent Assoc. 2005;71(5):327.PubMed Albrektsson T, Wennerberg A. The impact of oral implants – past and future, 1966 – 2042. J Can Dent Assoc. 2005;71(5):327.PubMed
3.
go back to reference Liu R, Lei T, Dusevich V, Yao X, Liu Y, Walker MP, Wang Y, Ye L. Surface characteristics and cell adhesion: a comparative study of four commercial dental implants. J Prosthod. 2013;22:641–51. Liu R, Lei T, Dusevich V, Yao X, Liu Y, Walker MP, Wang Y, Ye L. Surface characteristics and cell adhesion: a comparative study of four commercial dental implants. J Prosthod. 2013;22:641–51.
4.
go back to reference Albrektsson T, Jacobsson M. Bone–metal interface in osseointegration. J Prosthet Dent. 1987;57:597–607.PubMed Albrektsson T, Jacobsson M. Bone–metal interface in osseointegration. J Prosthet Dent. 1987;57:597–607.PubMed
5.
go back to reference Wennerberg A, Albrektsson T. Effects of titanium surface topography on bone. Impl Res. 2009;20(Suppl 4):172–84. Wennerberg A, Albrektsson T. Effects of titanium surface topography on bone. Impl Res. 2009;20(Suppl 4):172–84.
6.
go back to reference Wennerberg A, Albrektsson T. On implants surfaces: a review of current knwoledge and opinions. Int J Oral Maxillofac Implants. 2009;24:63–74. Wennerberg A, Albrektsson T. On implants surfaces: a review of current knwoledge and opinions. Int J Oral Maxillofac Implants. 2009;24:63–74.
7.
go back to reference Mendonça G, Mendonça DBS, Simões LGP, Araújo AL, Leite ER, Duarte WR, Aragão FJL, Cooper LF. The effects of implant surface nanoscale features on osteoblastspecific gene expression. Biomaterials. 2009;30:4053–62.PubMed Mendonça G, Mendonça DBS, Simões LGP, Araújo AL, Leite ER, Duarte WR, Aragão FJL, Cooper LF. The effects of implant surface nanoscale features on osteoblastspecific gene expression. Biomaterials. 2009;30:4053–62.PubMed
8.
go back to reference Anselme K, et al. The relative influence of the topography and chemistry of TiA16V4 surfaces on osteoblastic cell behaviour. Biomaterials. 2000;21:1567–77.PubMed Anselme K, et al. The relative influence of the topography and chemistry of TiA16V4 surfaces on osteoblastic cell behaviour. Biomaterials. 2000;21:1567–77.PubMed
9.
go back to reference Anselme K. Osteoblast adhesion on biomaterials. Biomaterials. 2000;21(7):667–81.PubMed Anselme K. Osteoblast adhesion on biomaterials. Biomaterials. 2000;21(7):667–81.PubMed
10.
go back to reference Lange R, Luthen F, Beck U, Rychly J, Baumann A, Nebe B. Cell–extracellular matrix interactions and physiochemical characteristics of titanium surfaces depend on the roughness of the material. Biomol Eng. 2002;19:255–61.PubMed Lange R, Luthen F, Beck U, Rychly J, Baumann A, Nebe B. Cell–extracellular matrix interactions and physiochemical characteristics of titanium surfaces depend on the roughness of the material. Biomol Eng. 2002;19:255–61.PubMed
11.
go back to reference Magnani A, Priamo A, Pasqui D, Barbucci R. Cell behavior on chemically microstructured surfaces. Mater Sci Eng C. 2003;23:315–28. Magnani A, Priamo A, Pasqui D, Barbucci R. Cell behavior on chemically microstructured surfaces. Mater Sci Eng C. 2003;23:315–28.
12.
go back to reference Boyan BD, Lossdorfer S, Wang L, Zhao G. Osteoblasts generate an osteogenic microenvironment when grown on surfaces with rough microtopographies. Eur Cells Mat. 2003;5(2):11–2. Boyan BD, Lossdorfer S, Wang L, Zhao G. Osteoblasts generate an osteogenic microenvironment when grown on surfaces with rough microtopographies. Eur Cells Mat. 2003;5(2):11–2.
13.
go back to reference Rupp F, Scheideler L, Rehbein D, Axmann D, Geis-Gerstorfer J. Roughness induced dynamic changes of wettability of acid etched titanium implant modification. Biomaterials. 2004;25:1429–38.PubMed Rupp F, Scheideler L, Rehbein D, Axmann D, Geis-Gerstorfer J. Roughness induced dynamic changes of wettability of acid etched titanium implant modification. Biomaterials. 2004;25:1429–38.PubMed
14.
go back to reference Le Guehennec L, Lopez-Heredia MA, Enkel B, Weiss P, Amouriq Y, Layrolle P. Osteoblastic cell behaviour on different titanium implant surfaces. Acta Biomater. 2008;4(3):535–43.PubMed Le Guehennec L, Lopez-Heredia MA, Enkel B, Weiss P, Amouriq Y, Layrolle P. Osteoblastic cell behaviour on different titanium implant surfaces. Acta Biomater. 2008;4(3):535–43.PubMed
15.
go back to reference Elias CN, Meirelles L. Improving osseointegration of dental implants. Exp Rev Med Dev. 2010;7(2):241–56. Elias CN, Meirelles L. Improving osseointegration of dental implants. Exp Rev Med Dev. 2010;7(2):241–56.
16.
go back to reference Boyan BD, Schwartz Z, Lohmann CH, Sylvia VL, Cochran DL, Dean DD, Puzas JE. Pretreatment of bone with osteoclasts affects phenotypic expression of osteoblast-like cells. J Orthop Res. 2003;21:638–47.PubMed Boyan BD, Schwartz Z, Lohmann CH, Sylvia VL, Cochran DL, Dean DD, Puzas JE. Pretreatment of bone with osteoclasts affects phenotypic expression of osteoblast-like cells. J Orthop Res. 2003;21:638–47.PubMed
17.
go back to reference Lüthen F, Lange R, Becker P, et al. The influence of surface roughness of titanium on b1 and b3-integrin adhesion and the organization of fibronectin in human osteoblastic cells. Biomaterials. 2005;26:2423–40.PubMed Lüthen F, Lange R, Becker P, et al. The influence of surface roughness of titanium on b1 and b3-integrin adhesion and the organization of fibronectin in human osteoblastic cells. Biomaterials. 2005;26:2423–40.PubMed
18.
go back to reference Vallés G, Gil-Garay E, Munuera L, et al. Modulation of the cross-talk between macrophages and osteoblasts by titanium based particles. Biomaterials. 2008;29:2326–35.PubMed Vallés G, Gil-Garay E, Munuera L, et al. Modulation of the cross-talk between macrophages and osteoblasts by titanium based particles. Biomaterials. 2008;29:2326–35.PubMed
19.
go back to reference Nebe B, Lüthen F, Lange R, et al. Topography-induced alterations in adhesion structures affect mineralization in human osteoblasts on titanium. Mater Sci Eng. 2004;24:619–24. Nebe B, Lüthen F, Lange R, et al. Topography-induced alterations in adhesion structures affect mineralization in human osteoblasts on titanium. Mater Sci Eng. 2004;24:619–24.
20.
go back to reference Bagno A, Di Bello C. Surface treatments and roughness properties of Ti based biomaterials. J Mater Sci Mater Med. 2004;15:935–49.PubMed Bagno A, Di Bello C. Surface treatments and roughness properties of Ti based biomaterials. J Mater Sci Mater Med. 2004;15:935–49.PubMed
21.
go back to reference Hazan R, Brener R, Oron U. Bone growth to metal implants is regulated by their surface chemical properties. Biomaterials. 1993;14:570–4.PubMed Hazan R, Brener R, Oron U. Bone growth to metal implants is regulated by their surface chemical properties. Biomaterials. 1993;14:570–4.PubMed
22.
go back to reference Larsson C, et al. Bone response to surface-modified titanium implants: studies on the early tissue response to machined and electropolished implants with different oxide thicknesses. Biomaterials. 1996;17:605–16.PubMed Larsson C, et al. Bone response to surface-modified titanium implants: studies on the early tissue response to machined and electropolished implants with different oxide thicknesses. Biomaterials. 1996;17:605–16.PubMed
23.
go back to reference Giavaresi G, Fini M, Cigada A, Chiesa R, Rondelli G, Rimondini L, Vicoli Aldini N, Martini L, Giardino R. Histomorphometric and microhardness assessments of sheep cortical bone surrounding titanium implants with different surface treatments. J Biomed Mater Res. 2003;67A:112–20. Giavaresi G, Fini M, Cigada A, Chiesa R, Rondelli G, Rimondini L, Vicoli Aldini N, Martini L, Giardino R. Histomorphometric and microhardness assessments of sheep cortical bone surrounding titanium implants with different surface treatments. J Biomed Mater Res. 2003;67A:112–20.
24.
go back to reference Kim MJ, Choi MU, Kim CW. Activation of phospholipase D1 by surface roughness of titanium in MG63 osteoblast-like cell. Biomaterials. 2006;27:5502–11.PubMed Kim MJ, Choi MU, Kim CW. Activation of phospholipase D1 by surface roughness of titanium in MG63 osteoblast-like cell. Biomaterials. 2006;27:5502–11.PubMed
25.
go back to reference Albrektsson T, Sennerdy L, Wennerberg A. State of the art of oral implants. Periodontology 2000. 2008;47:15–26.PubMed Albrektsson T, Sennerdy L, Wennerberg A. State of the art of oral implants. Periodontology 2000. 2008;47:15–26.PubMed
26.
go back to reference Albrektsson T, Buser D, Sennerdy L. On crestal/marginal bone loss around dental implants. Int J Periodont Rest Dent. 2013;33(1):9–11. Albrektsson T, Buser D, Sennerdy L. On crestal/marginal bone loss around dental implants. Int J Periodont Rest Dent. 2013;33(1):9–11.
27.
go back to reference Schwarz F, Wieland M, Schwartz Z, Zhao G, Rupp F, Geis-Gerstorfer J, Schedle A, Broggini N, Bornstein M, Buser D, Ferguson SJ, Becker J, Boyan BD, Cochran DL. Potential of chemically modified hydrophilic surface characteristics to support tissue integration of titanium dental implants. J Biomed Mater Res Part B: Appl Biomater. 2009;88B:544–57. Schwarz F, Wieland M, Schwartz Z, Zhao G, Rupp F, Geis-Gerstorfer J, Schedle A, Broggini N, Bornstein M, Buser D, Ferguson SJ, Becker J, Boyan BD, Cochran DL. Potential of chemically modified hydrophilic surface characteristics to support tissue integration of titanium dental implants. J Biomed Mater Res Part B: Appl Biomater. 2009;88B:544–57.
28.
go back to reference Bang S-M, Moon H-J, Kwon Y-D, Yoo J-Y, Pae A, Kwon IK. Osteoblastic and osteoclastic differentiation on SLA and hydrophilic modified SLA titanium surfaces. Clin Oral Impl Res. 2014;25:831–7. Bang S-M, Moon H-J, Kwon Y-D, Yoo J-Y, Pae A, Kwon IK. Osteoblastic and osteoclastic differentiation on SLA and hydrophilic modified SLA titanium surfaces. Clin Oral Impl Res. 2014;25:831–7.
29.
go back to reference Zhao GZO, Schwartz Z, Wieland M, Landolt D, Boyan BD. Osteoblastlike cells are sensitive to submicron-scale surface structure. Clin Oral Implants Res. 2006;17:258–64.PubMed Zhao GZO, Schwartz Z, Wieland M, Landolt D, Boyan BD. Osteoblastlike cells are sensitive to submicron-scale surface structure. Clin Oral Implants Res. 2006;17:258–64.PubMed
30.
go back to reference Mendonça G, Mendonça DBS, Aragão FJL, Cooper LF. The combination of micron and nanotopography by H2SO4/H2O2 treatment and its effects on osteoblast-specific gene expression of hMSCs. J Biomed Mater Res. 2010;94A:169–79. Mendonça G, Mendonça DBS, Aragão FJL, Cooper LF. The combination of micron and nanotopography by H2SO4/H2O2 treatment and its effects on osteoblast-specific gene expression of hMSCs. J Biomed Mater Res. 2010;94A:169–79.
31.
go back to reference Sant’Ana ACP, Damante CA, Frias Martinez MA, Valdivia MAM, Karam PSBH, de Oliveira FA, et al. Isolation and characterization of progenitor cells from surgically created early healing alveolar defects in humans: a preliminary study. J Periodontol. 2018;89(11):1326–33.PubMed Sant’Ana ACP, Damante CA, Frias Martinez MA, Valdivia MAM, Karam PSBH, de Oliveira FA, et al. Isolation and characterization of progenitor cells from surgically created early healing alveolar defects in humans: a preliminary study. J Periodontol. 2018;89(11):1326–33.PubMed
32.
go back to reference Passanezi E, Janson WA, Nahás D, Campos A Jr. Newly forming bone autografts to treat periodontal infrabony pockets: clinical and histological events. Int J Periodontics Rest Dent. 1989;9(2):140–51. Passanezi E, Janson WA, Nahás D, Campos A Jr. Newly forming bone autografts to treat periodontal infrabony pockets: clinical and histological events. Int J Periodontics Rest Dent. 1989;9(2):140–51.
33.
go back to reference Sant'ana AC, Ferraz BF, de Rezende ML, Greghi SL, Damante CA, Passanezi E. Newly forming bone graft: a novel surgical approach to the treatment of denuded roots. J Appl Oral Sci. 2012;20(3):392–8.PubMedPubMedCentral Sant'ana AC, Ferraz BF, de Rezende ML, Greghi SL, Damante CA, Passanezi E. Newly forming bone graft: a novel surgical approach to the treatment of denuded roots. J Appl Oral Sci. 2012;20(3):392–8.PubMedPubMedCentral
34.
go back to reference Mendonça G, Mendonça DBS, Oliveira LS, Arújo CA. Effects of human mesenchymal stem cells on hydrophilic surfaces. ImplantNews 2013. 10(6 Part A):111–6 [In Portuguese]. Mendonça G, Mendonça DBS, Oliveira LS, Arújo CA. Effects of human mesenchymal stem cells on hydrophilic surfaces. ImplantNews 2013. 10(6 Part A):111–6 [In Portuguese].
35.
go back to reference Martin JY, Schwartz Z, Hummert TW, Schraub DM, Simpson J, Lankford J, Dean DD, Cochran DL, Boyan BD. Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). J Biomed Mater Res. 1995;29:389–401.PubMed Martin JY, Schwartz Z, Hummert TW, Schraub DM, Simpson J, Lankford J, Dean DD, Cochran DL, Boyan BD. Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). J Biomed Mater Res. 1995;29:389–401.PubMed
37.
go back to reference Bryington M, Mendonc AG, Nares S, Cooper LF. Osteoblastic and cytokine gene expression of implant-adherent cells in humans. Clin Oral Impl Res. 2014;25:52–8. Bryington M, Mendonc AG, Nares S, Cooper LF. Osteoblastic and cytokine gene expression of implant-adherent cells in humans. Clin Oral Impl Res. 2014;25:52–8.
38.
go back to reference Lincks J, Boyan BD, Blanchard CR, Lohmann CH, Liu Y, Cochran DL, Dean DD, Schwartz Z. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependente on surface roughness and composition. Biomaterials. 1998;19:2219–32.PubMed Lincks J, Boyan BD, Blanchard CR, Lohmann CH, Liu Y, Cochran DL, Dean DD, Schwartz Z. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependente on surface roughness and composition. Biomaterials. 1998;19:2219–32.PubMed
39.
go back to reference Cooper LF, Zhou Y, Takebe J, Guo J, Abron A, Holmen A, et al. Fluoride modification effects on osteoblast behavior and bone formation at TiO2 grit-blasted c.p. titanium endosseous implants. Biomaterials. 2006;27:926–36.PubMed Cooper LF, Zhou Y, Takebe J, Guo J, Abron A, Holmen A, et al. Fluoride modification effects on osteoblast behavior and bone formation at TiO2 grit-blasted c.p. titanium endosseous implants. Biomaterials. 2006;27:926–36.PubMed
40.
go back to reference Olivares-Navarrete R, Hyzy SL, Hutton DL, Erdman CP, Wieland M, Boyan BD, Schwartz Z. Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage. Biomaterials. 2010;31:2728–35.PubMedPubMedCentral Olivares-Navarrete R, Hyzy SL, Hutton DL, Erdman CP, Wieland M, Boyan BD, Schwartz Z. Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage. Biomaterials. 2010;31:2728–35.PubMedPubMedCentral
41.
go back to reference Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54.
42.
go back to reference Evian CI, Rosenberg ES, Coslet JG, Corn H. The osteogenic activity of bone removed from healing extraction sockets in humans. J Periodontol. 1982;53:81–5.PubMed Evian CI, Rosenberg ES, Coslet JG, Corn H. The osteogenic activity of bone removed from healing extraction sockets in humans. J Periodontol. 1982;53:81–5.PubMed
43.
go back to reference Cardaropoli G, Araújo M, Hayacibara R, Sukekava F, Lindhe J. Healing of extraction sockets and surgically produced – augmented and non-augmented – defects in alveolar ridge. An experimental study in dogs. J Clin Periodontol. 2005;32:435–40.PubMed Cardaropoli G, Araújo M, Hayacibara R, Sukekava F, Lindhe J. Healing of extraction sockets and surgically produced – augmented and non-augmented – defects in alveolar ridge. An experimental study in dogs. J Clin Periodontol. 2005;32:435–40.PubMed
44.
go back to reference Cardaropoli G, Araújo M, Lindhe J. Dynamics of bone tissue formation in tooth extraction sites. J ClinPeriodontol. 2003;30:809–18. Cardaropoli G, Araújo M, Lindhe J. Dynamics of bone tissue formation in tooth extraction sites. J ClinPeriodontol. 2003;30:809–18.
45.
go back to reference Penteado R, Romito GA, Pustiglioni FE, Marques MM. Morphological and proliferative analysis of the healing tissue in human alveolar sockets covered or not by an e-PTFE membrane: a preliminary immunohistochemical and ultrastructural study. Braz J Oral Sci. 2005;4:664–9. Penteado R, Romito GA, Pustiglioni FE, Marques MM. Morphological and proliferative analysis of the healing tissue in human alveolar sockets covered or not by an e-PTFE membrane: a preliminary immunohistochemical and ultrastructural study. Braz J Oral Sci. 2005;4:664–9.
46.
go back to reference Pivodova F, Frankova J, Dolezel P, Ulrichova J. The response of osteoblast-like Saos-2 cells to modified titanium surfaces. Int J Oral Maxillofac Implants. 2013;28:1386–94.PubMed Pivodova F, Frankova J, Dolezel P, Ulrichova J. The response of osteoblast-like Saos-2 cells to modified titanium surfaces. Int J Oral Maxillofac Implants. 2013;28:1386–94.PubMed
47.
go back to reference Wennerberg A. On surface roughness and implant incorporation. Tese (Doutorado). Departmant of Biomaterial/Handicap Research, University of Götenborg. Götenborg, Sweden, 1996. Wennerberg A. On surface roughness and implant incorporation. Tese (Doutorado). Departmant of Biomaterial/Handicap Research, University of Götenborg. Götenborg, Sweden, 1996.
48.
go back to reference Wennerberg A, Hallgren C, Johansson C, Danelli S. A histomorphometric evaluation of screw-shaped implants each prepared with two surface roughnesses. Clin Oral Implants Res. 1998;9:11–9.PubMed Wennerberg A, Hallgren C, Johansson C, Danelli S. A histomorphometric evaluation of screw-shaped implants each prepared with two surface roughnesses. Clin Oral Implants Res. 1998;9:11–9.PubMed
49.
go back to reference Mustafa K, Wennerberg A, Wroblewski J, Hultenby K, Lopez BS, Arvidson K. Determining optimal surface roughness of TiO(2) blasted titanium implant material for attachment, proliferation and differentiation of cells derived from human mandibular alveolar bone. Clin Oral Implants Res. 2001;12:515–25.PubMed Mustafa K, Wennerberg A, Wroblewski J, Hultenby K, Lopez BS, Arvidson K. Determining optimal surface roughness of TiO(2) blasted titanium implant material for attachment, proliferation and differentiation of cells derived from human mandibular alveolar bone. Clin Oral Implants Res. 2001;12:515–25.PubMed
50.
go back to reference Calvo-Guirado JL, Satorres-Nieto M, Aguilar-Salvatierra A, Delgado-Ruiz RA, de Val JEM-S, Gargallo-Albiol J, Gómez-Moreno G, Romanos GE. Influence of surface treatment on osseointegration of dental implants: histological, histomorphometric and radiological analysis in vivo. Clin Oral Invest. 2015;19:509–17. Calvo-Guirado JL, Satorres-Nieto M, Aguilar-Salvatierra A, Delgado-Ruiz RA, de Val JEM-S, Gargallo-Albiol J, Gómez-Moreno G, Romanos GE. Influence of surface treatment on osseointegration of dental implants: histological, histomorphometric and radiological analysis in vivo. Clin Oral Invest. 2015;19:509–17.
51.
go back to reference Elias CN, Fernandes DJ, Resende CRS, Roestelb J. Mechanical properties, surface morphology and stability of a modified commercially pure high strength titanium alloy for dental implants. Dental Mat. 2015;31:e1–e13. Elias CN, Fernandes DJ, Resende CRS, Roestelb J. Mechanical properties, surface morphology and stability of a modified commercially pure high strength titanium alloy for dental implants. Dental Mat. 2015;31:e1–e13.
52.
go back to reference Gasik M, Braem A, Chaudhari A, Duyck J, Vleugels J. Titanium implants with modified surfaces: meta-analysis of in vivo osteointegration. Mat Sci Engin C. 2015;49:152–258. Gasik M, Braem A, Chaudhari A, Duyck J, Vleugels J. Titanium implants with modified surfaces: meta-analysis of in vivo osteointegration. Mat Sci Engin C. 2015;49:152–258.
53.
go back to reference Hallgren C, Sawase T, Ortengren U, Wennerberg A. Histomorphometric and mechanical evaluation of the bone-tissue response to implants prepared with different orientation of surface topography. Clin Impl Dent Rel Res. 2001;3:194–203. Hallgren C, Sawase T, Ortengren U, Wennerberg A. Histomorphometric and mechanical evaluation of the bone-tissue response to implants prepared with different orientation of surface topography. Clin Impl Dent Rel Res. 2001;3:194–203.
54.
go back to reference Chinga G, Johnsen PO, Dougherty R, Berli EL, Walter J. Quantification of the 3D microstructure of SC surfaces. J Microscopy. 2007;227(Part 3):254–65. Chinga G, Johnsen PO, Dougherty R, Berli EL, Walter J. Quantification of the 3D microstructure of SC surfaces. J Microscopy. 2007;227(Part 3):254–65.
55.
go back to reference Safdar A. Microstructures and surface roughness of EBM produced Ti-6Al-4 V. Dissertation.Material Science, Malmö University, Malmö, Sweden, 2010. Safdar A. Microstructures and surface roughness of EBM produced Ti-6Al-4 V. Dissertation.Material Science, Malmö University, Malmö, Sweden, 2010.
56.
go back to reference Sartoretto SC, Alves ATNN, Resende RFB, Calasans-Maia J, Granjeiro JM, Calasans-Maia MD. Early osseointegration driven by the surface chemistry and wettability of dental implants. J Appl Oral Sci. 2015;23:279–87.PubMedPubMedCentral Sartoretto SC, Alves ATNN, Resende RFB, Calasans-Maia J, Granjeiro JM, Calasans-Maia MD. Early osseointegration driven by the surface chemistry and wettability of dental implants. J Appl Oral Sci. 2015;23:279–87.PubMedPubMedCentral
57.
go back to reference Inoue T, Cox JE, Pilliar RM, Melcher AH. Effect of the surface geometry of smooth and porous-coated titanium alloy on the orientation of fibroblasts in vitro. J Biomed Mater Res. 1987;21:107–26.PubMed Inoue T, Cox JE, Pilliar RM, Melcher AH. Effect of the surface geometry of smooth and porous-coated titanium alloy on the orientation of fibroblasts in vitro. J Biomed Mater Res. 1987;21:107–26.PubMed
58.
go back to reference Dunn GA, Heath JP. A new hypothesis of contact guidance in tissue cells. Exp Cell Res. 1976;101:1–14.PubMed Dunn GA, Heath JP. A new hypothesis of contact guidance in tissue cells. Exp Cell Res. 1976;101:1–14.PubMed
Metadata
Title
Surface roughness of titanium disks influences the adhesion, proliferation and differentiation of osteogenic properties derived from human
Authors
Maria Alejandra Frias Martinez
Ísis de Fátima Balderrama
Paula Stephania Brandão Hage Karam
Rodrigo Cardoso de Oliveira
Flávia Amadeu de Oliveira
Carlos Roberto Grandini
Fábio Bossoi Vicente
Andreas Stavropoulos
Mariana Schutzer Ragghianti Zangrando
Adriana Campos Passanezi Sant’Ana
Publication date
01-12-2020
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Implant Dentistry / Issue 1/2020
Electronic ISSN: 2198-4034
DOI
https://doi.org/10.1186/s40729-020-00243-5

Other articles of this Issue 1/2020

International Journal of Implant Dentistry 1/2020 Go to the issue