10.1007/s40204-019-00124-0

Effect of anodized zirconium implants on early osseointegration process in adult rats: a histological and histomorphometric study

  1. INTEMA, Applied Electrochemistry Division, National University of Mar del Plata-CONICET, Mar del Plata, B7608FDQ, AR
  2. Biology Department, FCEyN, National University of Mar del Plata, Mar del Plata, B7602AYJ, AR
  3. CIT Villa María–CONICET, Villa María, 5900, AR UTN-FRVM, Villa María, 5900, AR
  4. Marine and Coastal Research Institute (IIMyC), Biology Department, FCEyN, National University of Mar del Plata-CONICET, Mar del Plata, B7602AYJ, AR
Cover Image

Published in Issue 2019-11-22

How to Cite

Tano de la Hoz, M. F., Katunar, M. R., González, A., Gomez Sanchez, A., Díaz, A. O., & Ceré, S. (2019). Effect of anodized zirconium implants on early osseointegration process in adult rats: a histological and histomorphometric study. Progress in Biomaterials, 8(4 (December 2019). https://doi.org/10.1007/s40204-019-00124-0

Abstract

Abstract Since surface plays a key role in bioactivity, the response of the host to the biomaterial will determine the success or failure of the prosthesis. The purpose of this study is to make an exhaustive analysis of the histological and histochemical characteristics of new bone tissue around Zr implants anodized at 60 V (Zr60) supported by histomorphometric methods in a rat model. Fibrous tissue was observed around the control implants (Zr0) and osteoblasts were identified on the trabeculae close to the implantation site that showed typical cytological characteristics of active secretory cells, regardless of the surface condition. The histomorphometrical analysis revealed a significant increase in cancellous bone volume, trabecular thickness and in trabecular number together with a decrease in trabecular separation facing Zr60. TRAP staining showed that there was a relative increase in the number of osteoclasts for Zr60. In addition, a larger number of osteoclast with a greater number of nuclei were detected in the tibiae for Zr60. This research demonstrated that the new bone microarchitecture in contact with Zr60 is able to improve the early stages of the osseointegration process and consequently the primary stability of implants which is a crucial factor to reduce recovery time for patients.

Keywords

  • Osseointegration,
  • Zirconium implants,
  • Anodization,
  • Histology,
  • Histomorphometry

References

  1. Albrektsson and Johansson (2001) Osseointegration (pp. 96-101) https://doi.org/10.1007/s005860100282
  2. Anselme et al. (2010) Relative influence of surface topography and surface chemistry on cell response to bone implant materials. Part 2: biological aspects (pp. 1487-1507) https://doi.org/10.1243/09544119JEIM901
  3. Arlot et al. (2008) Histomorphometric and μCT analysis of bone biopsies from postmenopausal osteoporotic women treated with strontium ranelate (pp. 215-222) https://doi.org/10.1359/jbmr.071012
  4. Biggs et al. (2007) The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading (pp. 399-404) https://doi.org/10.1007/s10856-006-0705-6
  5. Branzoi et al. (2008) Electrochemical studies on the stability and corrosion resistance of new zirconium-based alloys for biomedical applications (pp. 167-173) https://doi.org/10.1002/sia.2750
  6. Cheng et al. (2016) Strontium (Sr) and silver (Ag) loaded nanotubular structures with combined osteoinductive and antimicrobial activities (pp. 388-400) https://doi.org/10.1016/j.actbio.2015.11.046
  7. Civantos et al. (2017) Titanium coatings and surface modifications: toward clinically useful bioactive implants (pp. 1245-1261) https://doi.org/10.1021/acsbiomaterials.6b00604
  8. Compston et al. (2018) Bone Histomorphometry (pp. 959-973) Academic Press https://doi.org/10.1016/B978-0-12-809965-0.00053-7
  9. Cooper (1998) Biologic determinants of bone formation for osseointegration: clues for future clinical improvements (pp. 439-449) https://doi.org/10.1016/S0022-3913(98)70009-5
  10. Cooper (2000) Endosseous implants https://doi.org/10.14219/jada.archive.2001.0062
  11. Das et al. (2009) TiO2 nanotubes on Ti: influence of nanoscale morphology on bone cell-materials interaction (pp. 225-237) https://doi.org/10.1002/jbm.a.32088
  12. Deligianni et al. (2001) Effect of surface roughness of the titanium alloy Ti–6Al–4 V on human bone marrow cell response and on protein adsorption (pp. 1241-1251) https://doi.org/10.1016/S0142-9612(00)00274-X
  13. Dos Santos et al. (2009) Chemical and topographical influence of hydroxyapatite and β-tricalcium phosphate surfaces on human osteoblastic cell behavior (pp. 510-520) https://doi.org/10.1002/jbm.a.31991
  14. Eliaz et al. (2009) The effect of surface treatment on the surface texture and contact angle of electrochemically deposited hydroxyapatite coating and on its interaction with bone-forming cells (pp. 3178-3191) https://doi.org/10.1016/j.actbio.2009.04.005
  15. Farina et al. (2015) Effect of surface modification on the corrosion resistance of Zr-2.5Nb as material for permanent implants (pp. 1166-1173) https://doi.org/10.1016/j.mspro.2015.04.181
  16. Furuya et al. (2018) Direct cell-cell contact between mature osteoblasts and osteoclasts dynamically controls their functions in vivo (pp. 1-12) https://doi.org/10.1038/s41467-017-02541-w
  17. Gamblin et al. (2014) Bone tissue formation with human mesenchymal stem cells and biphasic calcium phosphate ceramics: the local implication of osteoclasts and macrophages (pp. 9660-9667) https://doi.org/10.1016/j.biomaterials.2014.08.018
  18. Gomez Sanchez et al. (2011) Surface characterization of anodized zirconium for biomedical applications (pp. 6397-6405) https://doi.org/10.1016/j.apsusc.2011.02.005
  19. Gomez Sanchez et al. (2013) Surface modification of zirconium by anodisation as material for permanent implants: in vitro and in vivo study (pp. 161-169) https://doi.org/10.1007/s10856-012-4770-8
  20. Goriainov et al. (2014) Bone and metal: an orthopaedic perspective on osseointegration of metals (pp. 4043-4057) https://doi.org/10.1016/j.actbio.2014.06.004
  21. Bello et al. (2017) A nanoporous titanium surface promotes the maturation of focal adhesions and formation of filopodia with distinctive nanoscale protrusions by osteogenic cells (pp. 339-349) https://doi.org/10.1016/j.actbio.2017.07.022
  22. He et al. (2017) A comparison of micro-CT and histomorphometry for evaluation of osseointegration of PEO-coated titanium implants in a rat model (pp. 1-11) https://doi.org/10.1038/s41598-017-16465-4
  23. Iaquinta et al. (2019) Innovative biomaterials for bone regrowth (pp. 1-17) https://doi.org/10.3390/ijms20030618
  24. Isa et al. (2006) Effects of fluoride-modified titanium surfaces on osteoblast proliferation and gene expression (pp. 203-211)
  25. Jetten et al. (2014) Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo (pp. 109-118) https://doi.org/10.1007/s10456-013-9381-6
  26. Katunar et al. (2014) Can anodised zirconium implants stimulate bone formation? Preliminary study in rat model https://doi.org/10.1007/s40204-014-0024-9
  27. Katunar et al. (2017) In vitro and in vivo characterization of anodised zirconium as a potential material for biomedical applications (pp. 957-968) https://doi.org/10.1016/j.msec.2017.02.139
  28. Kini and Nandeesh (2012) Radionuclide and hybrid bone imaging (pp. 1-1046) https://doi.org/10.1007/978-3-642-02400-9
  29. Kohli et al. (2018) Bone remodelling in vitro: where are we headed? (pp. 38-46) https://doi.org/10.1016/j.bone.2018.01.015
  30. Kreja et al. (2010) Non-resorbing osteoclasts induce migration and osteogenic differentiation of mesenchymal stem cells (pp. 347-355) https://doi.org/10.1002/jcb.22406
  31. Krmpotic et al. (2015) Comparative histology and ontogenetic change in the carapace of armadillos (Mammalia: Dasypodidae) (pp. 601-616) https://doi.org/10.1007/s00435-015-0281-8
  32. Kusumbe and Adams (2014) Osteoclast progenitors promote bone vascularization and osteogenesis (pp. 1238-1240) https://doi.org/10.1038/nm.3747
  33. Lampin et al. (1997) Correlation between substratum roughness and wettability, cell adhesion, and cell migration (pp. 99-108) https://doi.org/10.1002/(SICI)1097-4636(199707)36:1<99::AID-JBM12>3.0.CO;2-E
  34. Le Guéhennec et al. (2007) Surface treatments of titanium dental implants for rapid osseointegration (pp. 844-854) https://doi.org/10.1016/j.dental.2006.06.025
  35. Meirelles et al. (2008) The effect of chemical and nanotopographical modifications on the early stages of osseointegration (pp. 641-647)
  36. Mendonça et al. (2008) Advancing dental implant surface technology from micron- to nanotopography (pp. 3822-3835) https://doi.org/10.1016/j.biomaterials.2008.05.012
  37. Milošev (2010) Metallic materials for biomedical applications: laboratory and clinical studies (pp. 309-324) https://doi.org/10.1351/pac-con-10-07-09
  38. Misra et al. (2009) Cellular response of preosteoblasts to nanograined/ultrafine-grained structures (pp. 1455-1467) https://doi.org/10.1016/j.actbio.2008.12.017
  39. Nanci et al. (1998) Chemical modification of titanium surfaces for covalent attachment of biological molecules (pp. 324-335) https://doi.org/10.1002/(SICI)1097-4636(199805)40:2<324::AID-JBM18>3.0.CO;2-L
  40. Novaes et al. (2010) Influence of implant surfaces on osseointegration (pp. 471-481) https://doi.org/10.1590/S0103-64402010000600001
  41. Pederson et al. (2008) Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate (pp. 20764-20769) https://doi.org/10.1073/pnas.0805133106
  42. Pellegrini et al. (2018) Novel surfaces and osseointegration in implant dentistry 9(4) https://doi.org/10.1111/jicd.12349
  43. Reyes et al. (2007) Biomolecular surface coating to enhance orthopaedic tissue healing and integration (pp. 3228-3235) https://doi.org/10.1016/j.biomaterials.2007.04.003
  44. Rouahi et al. (2006) Quantitative kinetic analysis of gene expression during human osteoblastic adhesion on orthopaedic materials (pp. 2829-2844) https://doi.org/10.1016/j.biomaterials.2006.01.001
  45. Rupp et al. (2006) Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces (pp. 323-334) https://doi.org/10.1002/jbm.a.30518
  46. Sanchez et al. (2013) Surface modification of titanium by anodic oxidation in phosphoric acid at low potentials. Part 2. in vitro and in vivo study (pp. 1395-1401) https://doi.org/10.1002/sia.5298
  47. Sollazzo et al. (2008) Zirconium oxide coating improves implant osseointegration in vivo (pp. 357-361) https://doi.org/10.1016/j.dental.2007.06.003
  48. Steiner et al. (2015) Computational analysis of primary implant stability in trabecular bone (pp. 807-815) https://doi.org/10.1016/j.jbiomech.2014.12.008
  49. Sul (2003) The significance of the surface properties of oxidized titanium to the bone response: special emphasis on potential biochemical bonding of oxidized titanium implant (pp. 3893-3907) https://doi.org/10.1016/S0142-9612(03)00261-8
  50. Sul et al. (2002) Resonance frequency and removal torque analysis of implants with turned and anodized surface oxides (pp. 252-259) https://doi.org/10.1034/j.1600-0501.2002.130304.x
  51. Totea et al. (2014) Elaboration and characterization of the electrodeposited phosphates masses doped with various ions on stainless steel (pp. 575-584)
  52. Vandamme et al. (2010) Establishment of an in vivo model for molecular assessment of titanium implant osseointegration in compromised bone (pp. 311-318) https://doi.org/10.1089/ten.tec.2010.0402
  53. Woodruff et al. (2007) Human osteoblast cell spreading and vinculin expression upon biomaterial surfaces (pp. 491-499) https://doi.org/10.1007/s10735-007-9142-1
  54. Yang et al. (2004) Preparation of bioactive titanium metal via anodic oxidation treatment (pp. 1003-1010) https://doi.org/10.1016/S0142-9612(03)00626-4
  55. Zander and Köster (2004) Corrosion of amorphous and nanocrystalline Zr-based alloys (pp. 53-59) https://doi.org/10.1016/j.msea.2003.10.230