Comparative in vivo study of alloy titanium implants with two different surfaces: biomechanical and SEM analysis

  • Francisley Ávila SouzaEmail author
  • Thayane Silveira Mata Furtado
  • Ulisses Ribeiro Campos Dayube
  • Willian Moraes Melo
  • Renato Sussumu Nishioka
  • Pier Paolo Poli
  • Carlo Maiorana
  • Paulo Sérgio Perri de Carvalho
Original Article



The purpose of this study was to evaluate the biomechanical behavior of the interface formed between bone and implants with machined surfaces (MS) and those modified by Al2O3 sandblasting and acid etching (SBAS).

Materials and methods

Before surgery, topographic characterization was performed by SEM-EDX and by mean roughness measurements. Ten Albinus rabbits received randomly 20 Ti-6Al-4V implants on its right and left tibiae, with one implant placed in each tibia. After implant insertion, the implant stability quotient (ISQ) was measured by means of resonance frequency analysis (RFA). After 3 and 6 weeks, the ISQ was again measured, followed by torque removal measurements. Analysis of variance and Tukey tests were used to analyze the data. The surface of the implants removed was evaluated by SEM-EDX. Immunohistochemical analysis of osteopontin (OPN) and osteocalcin (OC) protein was performed in bone tissue.


The topographic characterization showed differences between the analyzed surfaces, and the mean roughness values of SBAS group were statistically higher than MS. Overall, higher statistically significant ISQ values were observed in the SBAS group compared to the MS group (p = 0.012). The intra-group comparison of ISQ values in the SBAS group showed statistically significant differences between 0 and 3 weeks (p = 0.032) and 0 and 6 weeks (p = 0.003). The torque removal measurements of group SBAS were statistically higher when compared with the torque removal measurements of group MS in the time intervals of 3 weeks (p = 0.002) and 6 weeks (p < 0.001). SEM-EDX of the implant surfaces removed in SBAS group showed greater bone tissue covering and mean values atomic in percentage of Ca, P, and O statistically superior (p < 0.05) than MS group. Immunohistochemical reactions showed intense OC immunolabeling at 6 weeks postoperative for SBAS group.


The topographical modifications made in group SBAS allowed a better mechanical interlocking between the implant and bone tissue.


Biomechanics Dental implant Osseointegration Surface modification 



The authors would like to thank the Laboratory for the Study of Mineralized Tissues (LSMT) of the Araçatuba Dental of School-UNESP (FAPESP, 2012/159122-2; 2015/14688-0) from immunohistochemistry analysis, and would like to thank the Emfils Colosso Company for providing the implants used in this study.

Funding information

This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–CAPES, Universal-422842/2016-8.

Compliance with ethical standards

Conflict of interest

Francisley Ávila Souza declares that he has no conflict of interest. Thayane Silveira Mata Furtado declares that she has no conflict of interest. Ulisses Ribeiro Campos Dayube declares that he has no conflict of interest. Willian Moraes Melo declares that he has no conflict of interest. Renato Sussumu Nishioka declares that he has no conflict of interest. Pier Paolo Poli declares that he has no conflict of interest. Carlo Maiorana declares that he has no conflict of interest. Paulo Sérgio Perri de Carvalhop declares that he has no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Informed consent

For this type of study, formal consent is not required.


  1. 1.
    Branemark PI, Adell R, Breine U, Hansson BO, Lindstrom J, Ohlsson A (1969) Intra-osseous anchorage of dental prostheses. I. Experimental studies. Scand J Plast Reconstr Surg 3:81–100CrossRefGoogle Scholar
  2. 2.
    Albrektsson T, Branemark PI, Hansson HA, Lindstrom J (1981) Osseointegrated titanium implants. Requirements for ensuring a long-lasting, direct bone-to-implant anchorage in man. Acta Orthop Scand 52:155–170CrossRefGoogle Scholar
  3. 3.
    Adell R, Lekholm U, Rockler B, Branemark PI (1981) A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 10:387–416CrossRefGoogle Scholar
  4. 4.
    Albrektsson T, Zarb G, Worthington P, Eriksson AR (1986) The long-term efficacy of currently used dental implants: a review and proposed criteria of success. Int J Oral Maxillofac Implants 1:11–25Google Scholar
  5. 5.
    Albrektsson T (1988) A multicenter report on osseointegrated oral implants. J Prosthet Dent 60:75–84CrossRefGoogle Scholar
  6. 6.
    Adell R, Eriksson B, Lekholm U, Branemark PI, Jemt T (1990) Long-term follow-up study of osseointegrated implants in the treatment of totally edentulous jaws. Int J Oral Maxillofac Implants 5:347–359Google Scholar
  7. 7.
    Carvalho PSP, Ponzoni D (2002) Aspectos biológicos da osseointegração. In: Gomes LA (ed) Implantes osseointegrados: técnica e arte. Ed. Santos, São Paulo, pp 1–9Google Scholar
  8. 8.
    Mabilleau G, Bourdon S, Joly-Guillou ML, Filmon R, Basle MF, Chappard D (2006) Influence of fluoride, hydrogen peroxide and lactic acid on the corrosion resistance of commercially pure titanium. Acta Biomater 2:121–129CrossRefGoogle Scholar
  9. 9.
    Carvalho PSP, Carvalho MCA, Bassi APF (2016) Fundamentos da Osseointegração. In: Carvalho PSP, Pelizer EP (eds). Fundamentos em Implantodontia: uma visão contemporânea, 2 edn. pp 57–70Google Scholar
  10. 10.
    Davies JE (2003) Understanding peri-implant endosseous healing. J Dent Educ 67:932–949Google Scholar
  11. 11.
    Davies JE, Hosseini MM (2000) Histodynamics of endosseous wound healing. In: Davies JE (ed) Bone engineering. Toronto, pp 1–14Google Scholar
  12. 12.
    Santiago Junior JF, Pellizzer EP, Verri FR, de Carvalho PS (2013) Stress analysis in bone tissue around single implants with different diameters and veneering materials: a 3-D finite element study. Mater Sci Eng C Mater Biol Appl 33:4700–4714CrossRefGoogle Scholar
  13. 13.
    Mathew MT, Barao VA, Yuan JC, Assuncao WG, Sukotjo C, Wimmer MA (2012) What is the role of lipopolysaccharide on the tribocorrosive behavior of titanium? J Mech Behav Biomed Mater 8:71–85CrossRefGoogle Scholar
  14. 14.
    Gittens RA, Olivares-Navarrete R, McLachlan T, Cai Y, Hyzy SL, Schneider JM, Schwartz Z, Sandhage KH, Boyan BD (2012) Differential responses of osteoblast lineage cells to nanotopographically-modified, microroughened titanium-aluminum-vanadium alloy surfaces. Biomaterials 33:8986–8994CrossRefGoogle Scholar
  15. 15.
    Catalani S, Stea S, Beraudi A, Gilberti ME, Bordini B, Toni A, Apostoli P (2013) Vanadium release in whole blood, serum and urine of patients implanted with a titanium alloy hip prosthesis. Clin Toxicol (Phila) 51:550–556CrossRefGoogle Scholar
  16. 16.
    Elias CN, Fernandes DJ, Resende CR, Roestel J (2015) Mechanical properties, surface morphology and stability of a modified commercially pure high strength titanium alloy for dental implants. Dent Mater 31:e1–e13CrossRefGoogle Scholar
  17. 17.
    Souza FA, Queiroz TP, Guastaldi AC, Garcia-Junior IR, Magro-Filho O, Nishioka RS, Sisti KE, Sonoda CK (2013) Comparative in vivo study of commercially pure Ti implants with surfaces modified by laser with and without silicate deposition: biomechanical and scanning electron microscopy analysis. J Biomed Mater Res B Appl Biomater 101:76–84CrossRefGoogle Scholar
  18. 18.
    Klokkevold PR, Johnson P, Dadgostari S, Caputo A, Davies JE, Nishimura RD (2001) Early endosseous integration enhanced by dual acid etching of titanium: a torque removal study in the rabbit. Clin Oral Implants Res 12:350–357CrossRefGoogle Scholar
  19. 19.
    Buser D, Nydegger T, Hirt HP, Cochran DL, Nolte LP (1998) Removal torque values of titanium implants in the maxilla of miniature pigs. Int J Oral Maxillofac Implants 13:611–619Google Scholar
  20. 20.
    Buser D, Schenk RK, Steinemann S, Fiorellini JP, Fox CH, Stich H (1991) Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs. J Biomed Mater Res 25:889–902CrossRefGoogle Scholar
  21. 21.
    Piattelli A, Manzon L, Scarano A, Paolantonio M, Piattelli M (1998) Histologic and histomorphometric analysis of the bone response to machined and sandblasted titanium implants: an experimental study in rabbits. Int J Oral Maxillofac Implants 13:805–810Google Scholar
  22. 22.
    Buser D, Nydegger T, Oxland T, Cochran DL, Schenk RK, Hirt HP, Snetivy D, Nolte LP (1999) Interface shear strength of titanium implants with a sandblasted and acid-etched surface: a biomechanical study in the maxilla of miniature pigs. J Biomed Mater Res 45:75–83CrossRefGoogle Scholar
  23. 23.
    Chen CJ, Ding SJ, Chen CC (2016) Effects of surface conditions of titanium dental implants on bacterial adhesion. Photomed Laser Surg 34:379–388CrossRefGoogle Scholar
  24. 24.
    Mueller WD, Gross U, Fritz T, Voigt C, Fischer P, Berger G, Rogaschewski S, Lange KP (2003) Evaluation of the interface between bone and titanium surfaces being blasted by aluminium oxide or bioceramic particles. Clin Oral Implants Res 14:349–356CrossRefGoogle Scholar
  25. 25.
    Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2012) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Osteoarthr Cartil 20:256–260CrossRefGoogle Scholar
  26. 26.
    Gehrke SA, Ramirez-Fernandez MP, Granero Marin JM, Barbosa Salles M, Del Fabbro M, Calvo Guirado JL (2016) A comparative evaluation between aluminium and titanium dioxide microparticles for blasting the surface titanium dental implants: an experimental study in rabbits. Clin Oral Implants ResGoogle Scholar
  27. 27.
    Queiroz TP, Souza FA, Guastaldi AC, Margonar R, Garcia-Junior IR, Hochuli-Vieira E (2013) Commercially pure titanium implants with surfaces modified by laser beam with and without chemical deposition of apatite. Biomechanical and topographical analysis in rabbits. Clin Oral Implants Res 24:896–903CrossRefGoogle Scholar
  28. 28.
    Manrique N, Pereira CC, Luvizuto ER, Sánchez M d P, Okamoto T, Okamoto R, Sumida DH, Antoniali C (2015) Hypertension modifies OPG, RANK, and RANKL expression during the dental socket bone healing process in spontaneously hypertensive rats. Clin Oral Investig 19:1319–1327CrossRefGoogle Scholar
  29. 29.
    Beier US, Strobl H, Dhima M (2014) Correction of esthetic and biomechanical outcomes after maxillary anterior single dental implant fracture: a case report. Compend Contin Educ Dent 35:e1–e5Google Scholar
  30. 30.
    Marcelo CG, Filie Haddad M, Gennari Filho H, Marcelo Ribeiro Villa L, Dos Santos DM, Aldieris AP (2014) Dental implant fractures - aetiology, treatment and case report. J Clin Diagn Res 8:300–304Google Scholar
  31. 31.
    Shalabi MM, Wolke JG, Jansen JA (2006) The effects of implant surface roughness and surgical technique on implant fixation in an in vitro model. Clin Oral Implants Res 17:172–178CrossRefGoogle Scholar
  32. 32.
    Martinez-Gonzalez JM, Garcia-Saban F, Ferrandiz-Bernal J, Gonzalo-Lafuente JC, Cano-Sanchez J, Barona-Dorado C (2006) Removal torque and physico-chemical characteristics of dental implants etched with hydrofluoric and nitric acid. An experimental study in beagle dogs. Med Oral Patol Oral Cir Bucal 11:E281–E285Google Scholar
  33. 33.
    Zechner W, Tangl S, Furst G, Tepper G, Thams U, Mailath G, Watzek G (2003) Osseous healing characteristics of three different implant types. Clin Oral Implants Res 14:150–157CrossRefGoogle Scholar
  34. 34.
    Marinho VC, Celletti R, Bracchetti G, Petrone G, Minkin C, Piattelli A (2003) Sandblasted and acid-etched dental implants: a histologic study in rats. Int J Oral Maxillofac Implants 18:75–81Google Scholar
  35. 35.
    Souza FA, Queiroz TP, Sonoda CK, Okamoto R, Margonar R, Guastaldi AC, Nishioka RS, Garcia Junior IR (2014) Histometric analysis and topographic characterization of cp Ti implants with surfaces modified by laser with and without silica deposition. J Biomed Mater Res B Appl Biomater 102:1677–1688CrossRefGoogle Scholar
  36. 36.
    Carlsson L, Rostlund T, Albrektsson B, Albrektsson T (1988) Removal torques for polished and rough titanium implants. Int J Oral Maxillofac Implants 3:21–24Google Scholar
  37. 37.
    Cordioli G, Majzoub Z, Piattelli A, Scarano A (2000) Removal torque and histomorphometric investigation of 4 different titanium surfaces: an experimental study in the rabbit tibia. Int J Oral Maxillofac Implants 15:668–674Google Scholar
  38. 38.
    Cho SA, Jung SK (2003) A removal torque of the laser-treated titanium implants in rabbit tibia. Biomaterials 24:4859–4863CrossRefGoogle Scholar
  39. 39.
    Sennerby L, Thomsen P, Ericson LE (1992) A morphometric and biomechanic comparison of titanium implants inserted in rabbit cortical and cancellous bone. Int J Oral Maxillofac Implants 7:62–71Google Scholar
  40. 40.
    Lindgren C, Hallman M, Sennerby L, Sammons R (2010) Back-scattered electron imaging and elemental analysis of retrieved bone tissue following sinus augmentation with deproteinized bovine bone or biphasic calcium phosphate. Clin Oral Implants Res 21:924–930Google Scholar
  41. 41.
    Lozano-Carrascal N, Satorres-Nieto M, Delgado-Ruiz R, Maté-Sánchez de Val JE, Gehrke SA, Gargallo-Albiol J, Calvo-Guirado JL (2017) Scanning electron microscopy study of new bone formation following small and large defects preserved with xenografts supplemented with pamidronate-a pilot study in Fox-hound dogs at 4 and 8 weeks. Ann Anat 209:61–68CrossRefGoogle Scholar
  42. 42.
    Han CH, Johansson CB, Wennerberg A, Albrektsson T (1998) Quantitative and qualitative investigations of surface enlarged titanium and titanium alloy implants. Clin Oral Implants Res 9:1–10CrossRefGoogle Scholar
  43. 43.
    Stenport VF, Johansson CB (2008) Evaluations of bone tissue integration to pure and alloyed titanium implants. Clin Implant Dent Relat Res 10:191–199CrossRefGoogle Scholar
  44. 44.
    Niinomi M, Nakai M, Hieda J (2012) Development of new metallic alloys for biomedical applications. Acta Biomater 8:3888–3903CrossRefGoogle Scholar
  45. 45.
    Li Y, Jiao Y, Li X, Guo Z (2015) Improving the osteointegration of Ti6Al4V by zeolite MFI coating. Biochem Biophys Res Commun 460:151–156CrossRefGoogle Scholar
  46. 46.
    Williams D (2001) The golden anniversary of titanium biomaterials. Med Device Technol 12:8–11Google Scholar
  47. 47.
    Piattelli A, Degidi M, Paolantonio M, Mangano C, Scarano A (2003) Residual aluminum oxide on the surface of titanium implants has no effect on osseointegration. Biomaterials 24:4081–4089CrossRefGoogle Scholar
  48. 48.
    Ruger M, Gensior TJ, Herren C, von Walter M, Ocklenburg C, Marx R, Erli HJ (2010) The removal of Al2O3 particles from grit-blasted titanium implant surfaces: effects on biocompatibility, osseointegration and interface strength in vivo. Acta Biomater 6:2852–2861CrossRefGoogle Scholar
  49. 49.
    Faverani LP, Assunção WG, de Carvalho PSP, Yuan JC-C, Sukotjo C, Mathew MT, Barão VA (2014) Effects of dextrose and lipopolysaccharide on the corrosion behavior of a Ti-6Al-4V alloy with a smooth surface or treated with double-acid-etching. PLoS ONE 9:e93377CrossRefGoogle Scholar
  50. 50.
    Kim SJ, Kim MR, Rim JS, Chung SM, Shin SW (2010) Comparison of implant stability after different implant surface treatments in dog bone. J Appl Oral Sci 18:415–420CrossRefGoogle Scholar
  51. 51.
    Sartori IAM, Thomé E, Bernardes SR, Tiossi R, Vieira RA, Souza RCM (2013) Clinical evaluation for immediate implant loading: final insertion torque versus resonance frequency analysis. ImplantNews 10:99–104Google Scholar
  52. 52.
    Avila Souza F, Pereira Queiroz T, Rodrigues Luvizuto E, Nishioka RS, Garcia IR Jr, de Carvalho PS, Okamoto R (2010) Rank protein Immunolabeling during bone-implant Interface healing process. Int J DentGoogle Scholar
  53. 53.
    McKee MD, Nanci A (1996) Osteopontin at mineralized tissue interfaces in bone, teeth and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microsc Res Tech 33:141–164CrossRefGoogle Scholar
  54. 54.
    Dos Santos PR, Boos FB, Gorla LF, Garcia IR Jr, Okamoto R, Hochuli-Vieira E (2017) Maxillary sinus elevation surgery with ChronOS and autogenous bone graft: Immunohistochemical assessment of RUNX2, VEGF, TRAP, and Osteocalcin. Int J Periodontics Restorative Dent 37:e321–e327CrossRefGoogle Scholar
  55. 55.
    Nagata M, Messora M, Okamoto R, Campos N, Pola N, Esper L, Sbrana M, Fucini S, Garcia V, Bosco A (2009) Influence of the proportion of particulate autogenous bone graft/platelet-rich plasma on bone healing in critical-size defects: an immunohistochemical analysis in rat calvaria. Bone 45:339–345CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Francisley Ávila Souza
    • 1
    Email author
  • Thayane Silveira Mata Furtado
    • 2
  • Ulisses Ribeiro Campos Dayube
    • 2
  • Willian Moraes Melo
    • 1
  • Renato Sussumu Nishioka
    • 3
  • Pier Paolo Poli
    • 4
  • Carlo Maiorana
    • 4
  • Paulo Sérgio Perri de Carvalho
    • 1
    • 2
  1. 1.Department of Surgery and Integrated Clinic, Araçatuba Dental SchoolSão Paulo State University Júlio de Mesquita FilhoSão PauloBrazil
  2. 2.Implant Dentistry Postgraduate ProgramSão Leopoldo Mandic School of Dentistry and Research CenterCampinasBrazil
  3. 3.Department of Materials Dental and Prosthesis, São José dos Campos Dental of SchoolSão Paulo State University Júlio de Mesquita FilhoSão PauloBrazil
  4. 4.Implant Center for Edentulism and Jawbone Atrophies, Maxillofacial Surgery and Odontostomatology Unit, Fondazione IRCCS Cà Granda Maggiore Policlinico HospitalUniversity of MilanMilanItaly

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