Odontology

, Volume 102, Issue 2, pp 249–258 | Cite as

Bone response to immediate loading through titanium implants with different surface roughness in rats

  • Naoko Sato
  • Toshie Kuwana
  • Miou Yamamoto
  • Hanako Suenaga
  • Takahisa Anada
  • Shigeto Koyama
  • Osamu Suzuki
  • Keiichi Sasaki
Original Article

Abstract

Because of its high predictability of success, implant therapy is a reliable treatment for replacement of missing teeth. The concept of immediate implant loading has been widely accepted in terms of early esthetic and functional recovery. However, there is little biological evidence to support this concept. The objective of this study was to examine the interactive effects of mechanical loading and surface roughness of immediately loaded titanium implants on bone formation in rats. Screw-shaped anodized titanium implants were either untreated (smooth) or acid-etched. Two implants were inserted parallel to each other in the tibiae of rats, and a closed coil spring (2.0 N) was immediately applied. Trabecular and cortical bone around both implants was analyzed using microtomographic images, and a removal torque test was performed at weeks 1, 2, and 4. Immediate loading of acid-etched implants resulted in significant decreases in bone mineral density, contact surface area, and cortical bone thickness. These effects were not observed after immediate loading of smooth implants. Conversely, loading did not influence acid-etched implant fixation; however, smooth implant fixation at week 1 was significantly reduced. These results imply that surface roughness regulates bone response to mechanical stress and that immediate loading might not inhibit osseointegration for smooth and rough implants in the late healing stages.

Keywords

Immediate loading Osseointegration Bone reaction Surface roughness Rats 

Notes

Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research (grant no. 21791876) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Conflict of Interest

None of the authors have any conflicts of interest associated with this study.

References

  1. 1.
    Brånemark PI, Zarb G, Albrektsson T. Tissue-integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence 1985:11–77.Google Scholar
  2. 2.
    Brånemark PI, Hansson B, Adell R, Breine U, Lindström J, Hallén 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.PubMedGoogle Scholar
  3. 3.
    Boyan BD, Lossdorfer S, Wang L, Zhao G, Lohmann CH, Cochran DL, Schwartz Z. Osteoblasts generate an osteogenic microenvironment when grown on surfaces with rough microtopographies. Eur Cell Mater. 2003;6:22–7.PubMedGoogle Scholar
  4. 4.
    Schwartz Z, Lohmann CH, Vocke AK, Sylvia VL, Cochran DL, Dean DD, Boyan BD. Osteoblast response to titanium surface roughness and 1alpha, 25-(OH)(2)D(3) is mediated through the mitogen-activated protein kinase (MAPK) pathway. J Biomed Mater Res. 2001;56:417–26.PubMedGoogle Scholar
  5. 5.
    Takeuchi K, Saruwatari L, Nakamura HK, Yang JM, Ogawa T. Enhanced intrinsic biomechanical properties of osteoblastic mineralized tissue on roughened titanium surface. J Biomed Mater Res A. 2005;72:296–305.PubMedGoogle Scholar
  6. 6.
    Lai HC, Zhuang LF, Zhang ZY, Wieland M, Liu X. Bone apposition around two different sandblasted, large-grit and acid-etched implant surfaces at sites with coronal circumferential defects: an experimental study in dogs. Clin Oral Implants Res. 2009;20:247–53.PubMedGoogle Scholar
  7. 7.
    Butz F, Ogawa T, Nishimura I. Interfacial shear strength of endosseous implants. Int J Oral Maxillofac Implants. 2011;26:746–51.PubMedGoogle Scholar
  8. 8.
    Cooper LF. A role for surface topography in creating and maintaining bone at titanium endosseous implants. J Prosthet Dent. 2000;84:522–34.PubMedGoogle Scholar
  9. 9.
    Ogawa T, Nishimura I. Different bone integration profiles of turned and acid-etched implants associated with modulated expression of extracellular matrix genes. Int J Oral Maxillofac Implants. 2003;18:200–10.PubMedGoogle Scholar
  10. 10.
    Ogawa T, Ozawa S, Shih JH, Ryu KH, Sukotjo C, Yang JM, Nishimura I. Biomechanical evaluation of osseous implants having different surface topographies in rats. J Dent Res. 2000;79:1857–63.PubMedGoogle Scholar
  11. 11.
    Sanuki R, Shionome C, Kuwabara A, Mitsui N, Koyama Y, Suzuki N, Zhang F, Shimizu N, Maeno M. Compressive force induces osteoclast differentiation via prostaglandin E(2) production in MC3T3-E1 cells. Connect Tissue Res. 2010;51:150–8.PubMedGoogle Scholar
  12. 12.
    Balcells M, Fernandez Suarez M, Vazquez M, Edelman ER. Cells in fluidic environments are sensitive to flow frequency. J Cell Physiol. 2005;204:329–35.PubMedGoogle Scholar
  13. 13.
    Zhang X, Naert I, Van Schoonhoven D, Duyck J. Direct high-frequency stimulation of peri-implant rabbit bone: a pilot study. Clin Implant Dent Relat Res. 2010. doi: 10.1111/j.1708-8208.2010.00298x.PubMedGoogle Scholar
  14. 14.
    Ogawa T, Possemiers T, Zhang X, Naert I, Chaudhari A, Sasaki K, Duyck J. Influence of whole-body vibration time on peri-implant bone healing: a histomorphometrical animal study. J Clin Periodontol. 2011;38:180–5.PubMedGoogle Scholar
  15. 15.
    Bannister SR, Lohmann CH, Liu Y, Sylvia VL, Cochran DL, Dean DD, Boyan BD, Schwartz Z. Shear force modulates osteoblast response to surface roughness. J Biomed Mater Res. 2002;60:167–74.PubMedGoogle Scholar
  16. 16.
    Frost HM. A determinant of bone architecture. The minimum effective strain. Clin Orthop Relat Res. 1983:286–92.Google Scholar
  17. 17.
    Hoshaw SJ, Brunski BJ, Cochran GVB. Mechanical loading of Brånemark implants affects interfacial bone modeling and remodeling. Int J Oral Maxillofac Implants. 1994;9:345–60.Google Scholar
  18. 18.
    Vandamme K, Naert I, Geris L, Vander Sloten J, Puers R, Duyck J. The effect of micro-motion on the tissue response around immediately loaded roughened titanium implants in the rabbit. Eur J Oral Sci. 2007;115:21–9.PubMedGoogle Scholar
  19. 19.
    De Smet E, Jaecques SV, Wevers M, Jansen JA, Jacobs R, Sloten JV, Naert IE. Effect of controlled early implant loading on bone healing and bone mass in guinea pigs, as assessed by micro-CT and histology. Eur J Oral Sci. 2006;114:232–42.PubMedGoogle Scholar
  20. 20.
    Isidor F. Histological evaluation of peri-implant bone at implants subjected to occlusal overload or plaque accumulation. Clin Oral Implants Res. 1997;8:1–9.PubMedGoogle Scholar
  21. 21.
    Isidor F. Mobility assessment with the periotest system in relation to histologic findings of oral implants. Int J Oral Maxillofac Implants. 1998;13:377–83.PubMedGoogle Scholar
  22. 22.
    Simmons CA, Meguid SA, Pilliar RM. Differences in osseointegration rate due to implant surface geometry can be explained by local tissue strains. J Orthop Res. 2001;19:187–94.PubMedGoogle Scholar
  23. 23.
    Wiskott HW, Belser UC. Lack of integration of smooth titanium surfaces: a working hypothesis based on strains generated in the surrounding bone. Clin Oral Implants Res. 1999;10:429–44.PubMedGoogle Scholar
  24. 24.
    Boyan BD, Sylvia VL, Liu Y, Sagun R, Cochran DL, Lohmann CH, Dean DD, Schwartz Z. Surface roughness mediates its effects on osteoblasts via protein kinase A and phospholipase A2. Biomaterials. 1999;20:2305–10.PubMedGoogle Scholar
  25. 25.
    Das K, Bose S, Bandyopadhyay A. TiO2 nanotubes on Ti: influence of nanoscale morphology on bone cell-materials interaction. J Biomed Mater Res A. 2009;90:225–37.PubMedGoogle Scholar
  26. 26.
    Vandamme K, Naert I, Vander Sloten J, Puers R, Duyck J. Effect of implant surface roughness and loading on peri-implant bone formation. Eur J Oral Sci. 2008;79:150–7.Google Scholar
  27. 27.
    Kawahara H, Aoki H, Koike H, Soeda Y, Kawahara D, Matsuda S. No evidence to indicate topographic dependency on bone formation around cp titanium implants under masticatory loading. J Mater Sci Mater Med. 2006;17:727–34.PubMedGoogle Scholar
  28. 28.
    Schneider GB, Zaharias R, Seabold D, Keller J, Stanford C. Differentiation of preosteoblasts is affected by implant surface microtopographies. J Biomed Mater Res A. 2004;69:462–8.PubMedGoogle Scholar
  29. 29.
    Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. 1998;23:399–407.PubMedGoogle Scholar
  30. 30.
    Sato N, Kubo K, Yamada M, Hori N, Suzuki T, Maeda H, Ogawa T. Osteoblast mechanoresponses on Ti with different surface topographies. J Dent Res. 2009;88:812–6.PubMedGoogle Scholar
  31. 31.
    Ingber DE, Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci. 2003;116:1397–408.PubMedGoogle Scholar
  32. 32.
    Pavalko FM, Norvell SM, Burr DB, Turner CH, Duncan RL, Bidwell JP. A model for mechanotransduction in bone cells: the load-bearing mechanosomes. J Cell Biochem. 2003;88:104–12.PubMedGoogle Scholar
  33. 33.
    Weinbaum S, Guo P, You L. A new view of mechanotransduction and strain amplification in cells with microvilli and cell processes. Biorheology. 2001;38:119–42.PubMedGoogle Scholar
  34. 34.
    Lange R, Luthen F, Beck U, Rychly J, Baumann A, Nebe B. Cell-extracellular matrix interaction and physico-chemical characteristics of titanium surfaces depend on the roughness of the material. Biomol Eng. 2002;19:255–61.PubMedGoogle Scholar
  35. 35.
    Anselme K, Bigerelle M, Noel B, Dufresne E, Judas D, Iost A, Hardouin P. Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. J Biomed Mater Res. 2000;49:155–66.PubMedGoogle Scholar
  36. 36.
    Sela MN, Badihi L, Rosen G, Steinberg D, Kohavi D. Adsorption of human plasma proteins to modified titanium surfaces. Clin Oral Implants Res. 2007;18:630–8.PubMedGoogle Scholar
  37. 37.
    Lanyon LE. Control of bone architecture by functional load bearing. J Bone Miner Res. 1992;7(Suppl 2):S369–75.PubMedGoogle Scholar
  38. 38.
    Medard C, Ribaux C, Chavrier C. A histological investigation on early tissue response to titanium implants in a rat intramedullary model. J Oral Implantol. 2000;26:238–43.PubMedGoogle Scholar
  39. 39.
    Guglielmotti MB, Renou S, Cabrini RL. Evaluation of bone tissue on metallic implants by energy-dispersive X-ray analysis: an experimental study. Implant Dent. 1999;8:303–9.PubMedGoogle Scholar
  40. 40.
    Kajiwara H, Yamaza T, Yoshinari M, Goto T, Iyama S, Atsuta I, Kido MA, Tanaka T. The bisphosphonate pamidronate on the surface of titanium stimulates bone formation around tibial implants in rats. Biomaterials. 2005;26:581–7.PubMedGoogle Scholar
  41. 41.
    Clokie CM, Warshawsky H. Morphologic and radioautographic studies of bone formation in relation to titanium implants using the rat tibia as a model. Int J Oral Maxillofac Implants. 1995;10:155–65.PubMedGoogle Scholar
  42. 42.
    Clokie CM, Warshawsky H. Development of a rat tibia model for morphological studies of the interface between bone and a titanium implant. Compendium 1995;16:56, 58, 60 passim (quiz 8).Google Scholar
  43. 43.
    Duyck J, Cooman MD, Puers R, Van Oosterwyck H, Sloten JV, Naert I. A repeated sampling bone chamber methodology for the evaluation of tissue differentiation and bone adaptation around titanium implants under controlled mechanical conditions. J Biomech. 2004;37:1819–22.PubMedGoogle Scholar
  44. 44.
    Duyck J, Slaets E, Sasaguri K, Vandamme K, Naert I. Effect of intermittent loading and surface roughness on peri-implant bone formation in a bone chamber model. J Clin Periodontol. 2007;34:998–1006.PubMedGoogle Scholar
  45. 45.
    Melsen B, Lang NP. Biological reactions of alveolar bone to orthodontic loading of oral implants. Clin Oral Implants Res. 2001;12:144–52.PubMedGoogle Scholar
  46. 46.
    Gotfredsen K, Berglundh T, Lindhe J. Bone reactions adjacent to titanium implants subjected to static load. A study in the dog (I). Clin Oral Implants Res. 2001;12:1–8.PubMedGoogle Scholar
  47. 47.
    Gotfredsen K, Berglundh T, Lindhe J. Bone reactions adjacent to titanium implants with different surface characteristics subjected to static load. A study in the dog (II). Clin Oral Implants Res. 2001;12:196–201.PubMedGoogle Scholar
  48. 48.
    Gotfredsen K, Berglundh T, Lindhe J. Bone reactions adjacent to titanium implants subjected to static load of different duration. A study in the dog (III). Clin Oral Implants Res. 2001;12:552–8.PubMedGoogle Scholar
  49. 49.
    Shigemitsu R, Ogawa T, Matsumoto T, Yoda N, Gunji Y, Yamakawa Y, Ikeda K, Sasaki K. Stress distribution in the peri-implant bone with splinted and non-splinted implants by in vivo loading data-based finite element analysis. Odontology. 2012. doi: 10.1007/s10266-012-0077-y.PubMedGoogle Scholar
  50. 50.
    Chatzigianni A, Keilig L, Duschner H, Götz H, Eliades T, Bourauel C. Comparative analysis of numerical and experimental data of orthodontic mini-implants. Eur J Orthod. 2011;33:468–75.PubMedGoogle Scholar

Copyright information

© The Society of The Nippon Dental University 2013

Authors and Affiliations

  • Naoko Sato
    • 1
  • Toshie Kuwana
    • 2
  • Miou Yamamoto
    • 2
  • Hanako Suenaga
    • 2
  • Takahisa Anada
    • 3
  • Shigeto Koyama
    • 1
  • Osamu Suzuki
    • 3
  • Keiichi Sasaki
    • 2
  1. 1.Tohoku University HospitalMaxillofacial Prosthetics ClinicSendaiJapan
  2. 2.Division of Advanced ProsthodonticsTohoku University Graduate School of DentistrySendaiJapan
  3. 3.Division of Craniofacial Function EngineeringTohoku University Graduate School of DentistrySendaiJapan

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