Abstract
Surface modification techniques have been applied to generate titanium implant surfaces that promote osseointegration for the implants in cementless arthroplasty. However, its effect is not sufficient for osteoporotic bone. Strontium (Sr) promotes osteoblast proliferation and inhibits osteoclast proliferation and positively affects bone regeneration. The aim of this study was to confirm the effects of strontium-substituted hydroxyapatite (Sr-HA) coating via electrochemical deposition on implant’s osseointegration in the osteoporotic condition. Female Sprague Dawley rats were used for this study. Twelve weeks after bilateral ovariectomy, all animals were randomly divided into four groups: group HA; group 5 % Sr-HA; group 10 % Sr-HA; and group 20 % Sr-HA. Afterward, all rats from groups HA, 5 % Sr-HA, 10 % Sr-HA, and 20 % Sr-HA received implants with hydroxyapatite coating containing 0, 5, 10, and 20 % Sr. Implants were inserted bilaterally in all animals until death at 12 weeks. The bilateral femurs of rats were harvested for evaluation. All treatment groups increased new bone formation around the surface of titanium rods and push-out force; group 20 % Sr-HA showed the strongest effects on new bone formation and biomechanical strength. Additionally, these are significant differences in bone formation and push-out force was observed between groups 5 % Sr-HA and 10 % Sr-HA. This finding suggests that Sr-HA coating can improve implant osseointegration, and the 20 % Sr coating exhibited the best properties for implant osseointegration among the tested coatings in osteoporosis rats.
Similar content being viewed by others
References
Alegre DN, Ribeiro C, Sousa C, Correia J, Silva L, de Almeida L (2012) Possible benefits of strontium ranelate in complicated long bone fractures. Rheumatol Int 32(2):439–443. doi:10.1007/s00296-010-1687-8
Ammann P, Badoud I, Barraud S, Dayer R, Rizzoli R (2007) Strontium ranelate treatment improves trabecular and cortical intrinsic bone tissue quality, a determinant of bone strength. J Bone Miner Res 22(9):1419–1425. doi:10.1359/jbmr.070607
Baier M, Staudt P, Klein R, Sommer U, Wenz R, Grafe I, Meeder PJ, Nawroth PP, Kasperk C (2013) Strontium enhances osseointegration of calcium phosphate cement: a histomorphometric pilot study in ovariectomized rats. J Orthop Surg Res 8:16. doi:10.1186/1749-799X-8-16
Barrere F, van Blitterswijk CA, de Groot K (2006) Bone regeneration: molecular and cellular interactions with calcium phosphate ceramics. Int J Nanomed 1(3):317–332
Boanini E, Torricelli P, Fini M, Bigi A (2011) Osteopenic bone cell response to strontium-substituted hydroxyapatite. J Mater Sci Mater Med 22(9):2079–2088. doi:10.1007/s10856-011-4379-3
Bonnelye E, Chabadel A, Saltel F, Jurdic P (2008) Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone 42(1):129–138. doi:10.1016/j.bone.2007.08.043
Bozic KJ, Kurtz SM, Lau E, Ong K, Vail TP, Berry DJ (2009) The epidemiology of revision total hip arthroplasty in the United States. J Bone Joint Surg Am 91(1):128–133. doi:10.2106/JBJS.H.00155
Caverzasio J, Thouverey C (2011) Activation of FGF receptors is a new mechanism by which strontium ranelate induces osteoblastic cell growth. Cell Physiol Biochem 27(3–4):243–250
Choudhary S, Halbout P, Alander C, Raisz L, Pilbeam C (2007) Strontium ranelate promotes osteoblastic differentiation and mineralization of murine bone marrow stromal cells: involvement of prostaglandins. J Bone Miner Res 22(7):1002–1010. doi:10.1359/jbmr.070321
Doublier A, Farlay D, Jaurand X, Vera R, Boivin G (2013) Effects of strontium on the quality of bone apatite crystals: a paired biopsy study in postmenopausal osteoporotic women. Osteoporos Int 24(3):1079–1087. doi:10.1007/s00198-012-2181-9
Duarte PM, Cesar Neto JB, Goncalves PF, Sallum EA, Nociti JF (2003) Estrogen deficiency affects bone healing around titanium implants: a histometric study in rats. Implant Dent 12(4):340–346
Hara T, Hayashi K, Nakashima Y, Kanemaru T, Iwamoto Y (1999) The effect of hydroxyapatite coating on the bonding of bone to titanium implants in the femora of ovariectomised rats. J Bone Joint Surg Br 81(4):705–709
Hardy DC, Frayssinet P, Guilhem A, Lafontaine MA, Delince PE (1991) Bonding of hydroxyapatite-coated femoral prostheses. Histopathology of specimens from four cases. J Bone Joint Surg Br 73(5):732–740
Hiligsmann M, Ben Sedrine W, Bruyere O, Reginster JY (2013) Cost-effectiveness of strontium ranelate in the treatment of male osteoporosis. Osteoporos Int 24(8):2291–2300. doi:10.1007/s00198-013-2272-2
Kendler DL (2006) Strontium ranelate—data on vertebral and nonvertebral fracture efficacy and safety: mechanism of action. Curr Osteoporos Rep 4(1):34–39
Lakhkar N, Abou Neel EA, Salih V, Knowles JC (2011) Titanium and strontium-doped phosphate glasses as vehicles for strontium ion delivery to cells. J Biomater Appl 25(8):877–893. doi:10.1177/0885328210362125
Li Y, Feng G, Gao Y, Luo E, Liu X, Hu J (2010) Strontium ranelate treatment enhances hydroxyapatite-coated titanium screws fixation in osteoporotic rats. J Orthop Res 28(5):578–582. doi:10.1002/jor.21050
Li Y, Li Q, Zhu S, Luo E, Li J, Feng G, Liao Y, Hu J (2010) The effect of strontium-substituted hydroxyapatite coating on implant fixation in ovariectomized rats. Biomaterials 31(34):9006–9014
Li Y, Li X, Song G, Chen K, Yin G, Hu J (2012) Effects of strontium ranelate on osseointegration of titanium implant in osteoporotic rats. Clin Oral Implants Res 23(9):1038–1044. doi:10.1111/j.1600-0501.2011.02252.x
Liang Y, Li H, Xu J, Li X, Qi M, Hu M (2014) Morphology, composition, and bioactivity of strontium-doped brushite coatings deposited on titanium implants via electrochemical deposition. Int J Mol Sci 15(6):9952–9962. doi:10.3390/ijms15069952
Maimoun L, Brennan TC, Badoud I, Dubois-Ferriere V, Rizzoli R, Ammann P (2010) Strontium ranelate improves implant osseointegration. Bone 46(5):1436–1441. doi:10.1016/j.bone.2010.01.379
Marie PJ (2006) Strontium ranelate: a dual mode of action rebalancing bone turnover in favour of bone formation. Curr Opin Rheumatol 18(Suppl 1):S11–S15. doi:10.1097/01.bor.0000229522.89546.7b
Nih Consensus Development Panel on Osteoporosis Prevention D, Therapy (2001) Osteoporosis prevention, diagnosis, and therapy. JAMA 285(6):785–795
Pan HB, Zhao XL, Zhang X, Zhang KB, Li LC, Li ZY, Lam WM, Lu WW, Wang DP, Huang WH, Lin KL, Chang J (2010) Strontium borate glass: potential biomaterial for bone regeneration. J R Soc Interface 7(48):1025–1031. doi:10.1098/rsif.2009.0504
Tao ZS, Zhou WS, Tu KK, Huang ZL, Zhou Q, Sun T, Lv YX, Cui W, Yang L (2015) The effects of combined human parathyroid hormone (1-34) and simvastatin treatment on osseous integration of hydroxyapatite-coated titanium implants in the femur of ovariectomized rats. Injury 46(11):2164–2169. doi:10.1016/j.injury.2015.08.034
Tao ZS, Qiang Z, Tu KK, Huang ZL, Xu HM, Sun T, Lv YX, Cui W, Yang L (2015) Treatment study of distal femur for parathyroid hormone (1-34) and beta-tricalcium phosphate on bone formation in critical size defects in rats. J Biomater Appl 30(4):484–491. doi:10.1177/0885328215592854
Tao ZS, Lv YX, Cui W, Huang ZL, Tu KK, Zhou Q, Sun T, Yang L (2015) Effect of teriparatide on repair of femoral metaphyseal defect in ovariectomized rats. Z Gerontol Geriatr. doi:10.1007/s00391-015-0949-1
Tao ZS, Tu KK, Huang ZL, Zhou Q, Sun T, Xu HM, Zhou YL, Lv YX, Cui W, Yang L (2015) Combined treatment with parathyroid hormone (1-34) and beta-tricalcium phosphate had an additive effect on local bone formation in a rat defect model. Med Biol Eng Comput. doi:10.1007/s11517-015-1402-8
Tao ZS, Zhou WS, Tu KK, Huang ZL, Zhou Q, Sun T, Lv YX, Cui W, Yang L (2015) Effect exerted by teriparatide upon repair function of beta-tricalcium phosphate to ovariectomised rat’s femoral metaphysis defect caused by osteoporosis. Injury 46(11):2134–2141. doi:10.1016/j.injury.2015.07.042
Tao ZS, Zhou WS, Tu KK, Huang ZL, Zhou Q, Sun T, Lv YX, Cui W, Yang L (2015) Treatment study of distal femur for parathyroid hormone (1-34) and beta-tricalcium phosphate on bone formation in critical-sized defects in osteopenic rats. J Craniomaxillofac Surg 43(10):2136–2143. doi:10.1016/j.jcms.2015.09.004
Tao ZS, Zhou WS, Qiang Z, Tu KK, Huang ZL, Xu HM, Sun T, Lv YX, Cui W, Yang L (2016) Intermittent administration of human parathyroid hormone (1-34) increases fixation of strontium-doped hydroxyapatite coating titanium implants via electrochemical deposition in ovariectomized rat femur. J Biomater Appl 30(7):952–960. doi:10.1177/0885328215610898
Tao ZS, Zhou WS, Bai BL, Cui W, Lv YX, Yu XB, Huang ZL, Tu KK, Zhou Q, Sun T, Li H, Yang L (2016) The effects of combined human parathyroid hormone (1-34) and simvastatin treatment on the interface of hydroxyapatite-coated titanium rods implanted into osteopenic rats femurs. J Mater Sci Mater Med 27(3):43. doi:10.1007/s10856-015-5650-9
Tao ZS, Zhou WS, He XW, Liu W, Bai BL, Zhou Q, Huang ZL, Tu KK, Li H, Sun T, Lv YX, Cui W, Yang L (2016) A comparative study of zinc, magnesium, strontium-incorporated hydroxyapatite-coated titanium implants for osseointegration of osteopenic rats. Mater Sci Eng C Mater Biol Appl 62:226–232. doi:10.1016/j.msec.2016.01.034
Wei L, Ke J, Prasadam I, Miron RJ, Lin S, Xiao Y, Chang J, Wu C, Zhang Y (2014) A comparative study of Sr-incorporated mesoporous bioactive glass scaffolds for regeneration of osteopenic bone defects. Osteoporos Int 25(8):2089–2096. doi:10.1007/s00198-014-2735-0
Wu CT, Ramaswamy Y, Kwik D, Zreiqat H (2007) The effect of strontium incorporation into CaSiO3 ceramics on their physical and biological properties. Biomaterials 28(21):3171–3181. doi:10.1016/j.biomaterials.2007.04.002
Yu J, Li K, Zheng X, He D, Ye X, Wang M (2013) In vitro and in vivo evaluation of zinc-modified ca-si-based ceramic coating for bone implants. PLoS ONE 8(3):e57564. doi:10.1371/journal.pone.0057564
Zhu LL, Zaidi S, Peng Y, Zhou H, Moonga BS, Blesius A, Dupin-Roger I, Zaidi M, Sun L (2007) Induction of a program gene expression during osteoblast differentiation with strontium ranelate. Biochem Biophys Res Commun 355(2):307–311. doi:10.1016/j.bbrc.2007.01.120
Acknowledgments
This work was funded by a research Grant to Zhejiang Provincial Natural Science Foundation (Grant No: LY16H250002) and Zhejiang Provincial Health Department public projects (Grant No: LY16H250002).
Author contributions
Zhou-Shan Tao, Bing-Li Bai, Xing-Wen, and Wei Liu implemented the tool, performed the experiments for the evaluation, analyzed the datasets and wrote the manuscript; Hang Li, Kai-kai Tu, and Zheng-Liang Huang helped with the implementation regarding experiments; Qiang Zhou and Tao Sun helped with the experiments data acquisition; Yang-Xun Lv and Wei Cui collaborated in the evaluation, analyzed the datasets, and wrote the manuscript; and Lei Yang collaborated in the design, coordinated all the workflow and helped to draft, write and review the manuscript. All authors read and approved the final manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have declared that they have no conflict of interest.
Ethical approval
Statement of ethical approval Animals were handled with the approval of the Animal Experimentation Ethics Committee of Second Affiliated Hospital of Wenzhou Medical University.
Additional information
Zhou-Shan Tao and Bing-Li Bai contributed equally to this work.
Rights and permissions
About this article
Cite this article
Tao, ZS., Bai, BL., He, XW. et al. A comparative study of strontium-substituted hydroxyapatite coating on implant’s osseointegration for osteopenic rats. Med Biol Eng Comput 54, 1959–1968 (2016). https://doi.org/10.1007/s11517-016-1494-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11517-016-1494-9