Skip to main content

Advertisement

Log in

Recent developments in strontium-based biocomposites for bone regeneration

  • Review
  • Biomaterials
  • Published:
Journal of Artificial Organs Aims and scope Submit manuscript

Abstract

Recent advances in biomaterial designing techniques offer immense support to tailor biomimetic scaffolds and to engineer the microstructure of biomaterials for triggering bone regeneration in challenging bone defects. The current review presents the different categories of recently explored strontium-integrated biomaterials, including calcium silicate, calcium phosphate, bioglasses and polymer-based synthetic implants along with their in vivo bone formation efficacies and/or in vitro cell responses. The role and significance of controlled drug release scaffold/carrier design in strontium-triggered osteogenesis was also comprehensively described. Furthermore, the effects of stem cells and growth factors on bone remodeling are also elucidated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Sterling JA, Guelcher SA. Biomaterial scaffolds for treating osteoporotic bone. Curr Osteoporos Rep. 2014;12:48–544.

    PubMed  PubMed Central  Google Scholar 

  2. Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng. 2012;40:363–408.

    PubMed  PubMed Central  Google Scholar 

  3. Sarkar K, Kumar V, Devi KB, Ghosh D, Nandi SK, Roy M. Effects of Sr doping on biodegradation and bone regeneration of magnesium phosphate bioceramics. Materialia. 2019;5:100211. https://doi.org/10.1016/j.mtla.2019.100211.

    Article  CAS  Google Scholar 

  4. Campana V, Milano G, Pagano E, Barba M, Cicione C, Salonna G, et al. Bone substitutes in orthopaedic surgery: from basic science to clinical practice. J Mater Sci Mater Med. 2014;25:2445–611.

    PubMed  PubMed Central  CAS  Google Scholar 

  5. Bose S, Fielding G, Tarafder S, Bandyopadhyay A. Understanding of dopant-induced osteogenesis and angiogenesis in calcium phosphate ceramics. Trends Biotechnol. 2013;31:594–605.

    PubMed  CAS  Google Scholar 

  6. Saidak Z, Marie PJ. Strontium signaling: molecular mechanisms and therapeutic implications in osteoporosis. Pharmacol Ther. 2012;136:216–26.

    PubMed  CAS  Google Scholar 

  7. Li D, Chen K, Duan L, Fu T, Li J, Mu Z, et al. Strontium ranelate incorporated enzyme-cross-linked gelatin nanoparticle/silk fibroin aerogel for osteogenesis in OVX-induced osteoporosis. ACS Biomater Sci Eng. 2019;5:1440–511.

    CAS  Google Scholar 

  8. Kong CH, Steffi C, Shi Z, Wang W. Development of mesoporous bioactive glass nanoparticles and its use in bone tissue engineering. J Biomed Mater Res Part B Appl Biomater. 2018;106:2878–87.

    PubMed  CAS  Google Scholar 

  9. Vallet-Regí M, Salinas AJ. Ceramics as bone repair materials. Bone Repair Biomater. 2019;20:141–78.

    Google Scholar 

  10. Perez RA, Altankov G, Jorge-Herrero E, Ginebra MP. Micro- and nanostructured hydroxyapatite–collagen microcarriers for bone tissue-engineering applications. J Tissue Eng Regen Med. 2013;7:353–61. https://doi.org/10.1002/term.530.

    Article  PubMed  CAS  Google Scholar 

  11. Benic GI, Ge Y, Gallucci GO, Jung RE, Schneider D, Hämmerle CHF. Guided bone regeneration and abutment connection augment the buccal soft tissue contour: 3-year results of a prospective comparative clinical study. Clin Oral Implants Res. 2017;28:219–25. https://doi.org/10.1111/clr.12786.

    Article  PubMed  Google Scholar 

  12. Soltani Dehnavi S, Mehdikhani M, Rafienia M, Bonakdar S. Preparation and in vitro evaluation of polycaprolactone/PEG/bioactive glass nanopowders nanocomposite membranes for GTR/GBR applications. Mater Sci Eng C. 2018;90:236–47.

    CAS  Google Scholar 

  13. Wang G, Roohani-Esfahani SI, Zhang W, Lv K, Yang G, Ding X, et al. Effects of Sr–HT–Gahnite on osteogenesis and angiogenesis by adipose derived stem cells for critical-sized calvarial defect repair. Sci Rep. 2017;7:1–11.

    PubMed  PubMed Central  Google Scholar 

  14. Zhang L, Yang G, Johnson BN, Jia X. Three-dimensional (3D) printed scaffold and material selection for bone repair. Acta Biomater. 2019;84:16–33. https://doi.org/10.1016/j.actbio.2018.11.039.

    Article  PubMed  CAS  Google Scholar 

  15. Li JJ, Dunstan CR, Entezari A, Li Q, Steck R, Saifzadeh S, et al. A novel bone substitute with high bioactivity, strength, and porosity for repairing large and load-bearing bone defects. Adv Healthc Mater. 2019;8:1–14.

    Google Scholar 

  16. Entezari A, Roohani I, Li G, Dunstan CR, Rognon P, Li Q, et al. Architectural design of 3D printed scaffolds controls the volume and functionality of newly formed bone. Adv Healthc Mater. 2019;8:1–12.

    Google Scholar 

  17. Li JJ, Roohani-Esfahani S-I, Kim K, Kaplan DL, Zreiqat H. Silk coating on a bioactive ceramic scaffold for bone regeneration: effective enhancement of mechanical and in vitro osteogenic properties towards load-bearing applications. J Tissue Eng Regen Med. 2017;11:1741–53. https://doi.org/10.1002/term.2070.

    Article  PubMed  CAS  Google Scholar 

  18. Shie M-Y, Ding S-J, Chang H-C. The role of silicon in osteoblast-like cell proliferation and apoptosis. Acta Biomater. 2011;7:2604–14.

    PubMed  CAS  Google Scholar 

  19. Xu Z, Long J, Zhang N, Cao H, Tang W, Shi K, et al. Strong mineralization ability of strontium zinc silicate: formation of a continuous biomorphic mineralized layer with enhanced osteogenic activity. Colloids Surf B Biointerfaces. 2019;176:420–30. https://doi.org/10.1016/j.colsurfb.2019.01.026.

    Article  PubMed  CAS  Google Scholar 

  20. Xing M, Wang X, Wang E, Gao L, Chang J. Bone tissue engineering strategy based on the synergistic effects of silicon and strontium ions. Acta Biomater. 2018;72:381–95. https://doi.org/10.1016/j.actbio.2018.03.051.

    Article  PubMed  CAS  Google Scholar 

  21. Chiu Y-C, Shie M-Y, Lin Y-H, Lee AK-X, Chen Y-W. Effect of strontium substitution on the physicochemical properties and bone regeneration potential of 3D printed calcium silicate scaffolds. Int J Mol Sci. 2019;20. https://www.mdpi.com/1422-0067/20/11/2729.

  22. No YJ, Roohaniesfahani S, Lu Z, Shi J, Zreiqat H. Strontium-doped calcium silicate bioceramic with name enhanced in vitro osteogenic properties. Biomed Mater. 2017;12:35003. https://doi.org/10.1088/1748-605X/aa6987.

    Article  Google Scholar 

  23. Wang C, Chen B, Wang W, Zhang X, Hu T, He Y, et al. Strontium released bi-lineage scaffolds with immunomodulatory properties induce a pro-regenerative environment for osteochondral regeneration. Mater Sci Eng C. 2019;20:103.

    Google Scholar 

  24. Yu D, Ding H, Mao Y, Liu M, Yu B, Zhao X, et al. Strontium ranelate reduces cartilage degeneration and subchondral bone remodeling in rat osteoarthritis model. Acta Pharmacol Sin. 2013;34:393–402.

    PubMed  PubMed Central  CAS  Google Scholar 

  25. Okita N, Honda Y, Kishimoto N, Liao W, Azumi E, Hashimoto Y, et al. Supplementation of strontium to a chondrogenic medium promotes chondrogenic differentiation of human dedifferentiated fat cells. Tissue Eng Part A. 2015;21:1695–704.

    PubMed  CAS  Google Scholar 

  26. Liu Y-D, Yang H-X, Liao L-F, Jiao K, Zhang H-Y, Lu L, et al. Systemic administration of strontium or NBD peptide ameliorates early stage cartilage degradation of mouse mandibular condyles. Osteoarthr Cartil Engl. 2016;24:178–87.

    Google Scholar 

  27. Deng C, Zhu H, Li J, Feng C, Yao Q, Wang L, et al. Bioactive scaffolds for regeneration of cartilage and subchondral bone interface. Theranostics. 2018;8:1940–55.

    PubMed  PubMed Central  CAS  Google Scholar 

  28. Vilamitjana JA. Strontium-doped hydroxyapatite polysaccharide materials effect on ectopic bone formation. PLoS ONE. 2017;12:1–21.

    Google Scholar 

  29. Han X, Zhou X, Qiu K, Feng W, Mo H, Wang M, et al. Strontium-incorporated mineralized PLLA nanofibrous membranes for promoting bone defect repair. Colloids Surf B Biointerfaces. 2019;179:363–73. https://doi.org/10.1016/j.colsurfb.2019.04.011.

    Article  PubMed  CAS  Google Scholar 

  30. Yan S, Xia P, Xu S, Zhang K, Li G, Cui L, et al. Nanocomposite porous microcarriers based on strontium-substituted HA-g-poly(γ-benzyl-l-glutamate) for bone tissue engineering. ACS Appl Mater Interfaces. 2018;10:16270–81.

    PubMed  CAS  Google Scholar 

  31. Liu D, Nie W, Li D, Wang W, Zheng L, Zhang J, et al. 3D printed PCL/SrHA scaffold for enhanced bone regeneration. Chem Eng J. 2019;362:269–79. https://doi.org/10.1016/j.cej.2019.01.015.

    Article  CAS  Google Scholar 

  32. Chandran S, Shenoy SJ, Babu SS, Nair PR, Varma HK, John A. Strontium hydroxyapatite scaffolds engineered with stem cells aid osteointegration and osteogenesis in osteoporotic sheep model. Colloids Surf B Biointerfaces. 2018;163:346–54. https://doi.org/10.1016/j.colsurfb.2017.12.048.

    Article  PubMed  CAS  Google Scholar 

  33. Boivin G, Deloffre P, Perrat B, Panczer G, Boudeulle M, Mauras Y, et al. Strontium distribution and interactions with bone mineral in monkey iliac bone after strontium salt (S 12911) administration. J Bone Miner Res. 1996;11:1302–11. https://doi.org/10.1002/jbmr.5650110915.

    Article  PubMed  CAS  Google Scholar 

  34. Reitmaier S, Kovtun A, Schuelke J, Kanter B, Lemm M, Hoess A, et al. Strontium(II) and mechanical loading additively augment bone formation in calcium phosphate scaffolds. J Orthop Res. 2018;36:106–17. https://doi.org/10.1002/jor.23623.

    Article  PubMed  CAS  Google Scholar 

  35. Xie H, Gu Z, He Y, Xu J, Xu C, Li L, et al. Microenvironment construction of strontium–calcium-based biomaterials for bone tissue regeneration: the equilibrium effect of calcium to strontium. J Mater Chem B. 2018;6:2332–9. https://doi.org/10.1039/C8TB00306H.

    Article  PubMed  CAS  Google Scholar 

  36. Morohashi T, Sano T, Yamada S. Effects of strontium on calcium metabolism in rats. I. A distinction between the pharmacological and toxic doses. Jpn J Pharmacol. 1994;64:155–62.

    PubMed  CAS  Google Scholar 

  37. Qiu K, Zhao XJ, Wan CX, Zhao CS, Chen YW. Effect of strontium ions on the growth of ROS17/2.8 cells on porous calcium polyphosphate scaffolds. Biomaterials. 2006;27:1277–86.

    PubMed  CAS  Google Scholar 

  38. Tian M, Chen F, Song W, Song Y, Chen Y, Wan C, et al. In vivo study of porous strontium-doped calcium polyphosphate scaffolds for bone substitute applications. J Mater Sci Mater Med. 2009;20:1505–12.

    PubMed  CAS  Google Scholar 

  39. Yang S, Feng S, Tu M, Wang L, Yang Q, Yu B. Enhanced bone formation by strontium modified calcium sulfate hemihydrate in ovariectomized rat critical-size calvarial defects. Biomed Mater. 2017;20:12.

    Google Scholar 

  40. O’Neill R, McCarthy HO, Montufar EB, Ginebra M-P, Wilson DI, Lennon A, et al. Critical review: injectability of calcium phosphate pastes and cements. Acta Biomater. 2017;50:1–19.

    PubMed  Google Scholar 

  41. Henriques Lourenço A, Neves N, Ribeiro-Machado C, Sousa SR, Lamghari M, Barrias CC, et al. Injectable hybrid system for strontium local delivery promotes bone regeneration in a rat critical-sized defect model. Sci Rep. 2017;20:7.

    Google Scholar 

  42. Yuan B, Raucci MG, Fan Y, Zhu X, Yang X, Zhang X, et al. Injectable strontium-doped hydroxyapatite integrated with phosphoserine-tethered poly(epsilon-lysine) dendrons for osteoporotic bone defect repair. J Mater Chem B. 2018;6:7974–84.

    PubMed  CAS  Google Scholar 

  43. No YJ, Xin X, Ramaswamy Y, Li Y, Roohaniesfahani S, Mustaffa S, et al. Novel injectable strontium–hardystonite phosphate cement for cancellous bone filling applications. Mater Sci Eng C. 2019;97:103–15.

    CAS  Google Scholar 

  44. Yan S, Feng L, Zhu Q, Yang W, Lan Y, Li D, et al. Controlled release of BMP-2 from a heparin-conjugated strontium-substituted nanohydroxyapatite/silk fibroin scaffold for bone regeneration. ACS Biomater Sci Eng. 2018;4:3291–303.

    CAS  Google Scholar 

  45. Tao Z, Zhou W, Jiang Y, Wu X, Xu Z, Yang M, et al. Effects of strontium-modified calcium phosphate cement combined with bone morphogenetic protein-2 on osteoporotic bone defects healing in rats. J Biomater Appl. 2018;33:3–10.

    PubMed  CAS  Google Scholar 

  46. Salamanna F, Giavaresi G, Contartese D, Bigi A, Boanini E, Parrilli A, et al. Effect of strontium substituted ß-TCP associated to mesenchymal stem cells from bone marrow and adipose tissue on spinal fusion in healthy and ovariectomized rat. J Cell Physiol. 2019;20:1–11.

    Google Scholar 

  47. Ananjevs V, Ananjeva A, Vetra J, Skagers A, Salma I, Neimane L, et al. General influence of biphasic calcium phosphate on osteoporotic bone density. Proc Latv Acad Sci Sect B Nat Exact Appl Sci. 2019;73:185–8.

    CAS  Google Scholar 

  48. Zarins J, Pilmane M, Sidhoma E, Salma I, Locs J. The role of Strontium enriched hydroxyapatite and tricalcium phosphate biomaterials in osteoporotic bone regeneration. Symmetry (Basel). 2019;20:11.

    Google Scholar 

  49. He F, Lu T, Fang X, Qiu C, Tian Y, Li Y, et al. Study on MgxSr3-x (PO4) 2 bioceramics as potential bone grafts. Colloids Surf B Biointerfaces. 2019;175:158–65. https://doi.org/10.1016/j.colsurfb.2018.11.085.

    Article  PubMed  CAS  Google Scholar 

  50. He J, Ye H, Li Y, Fang J, Mei Q, Lu X, et al. Cancellous-bone-like porous iron scaffold coated with strontium incorporated octacalcium phosphate nanowhiskers for bone regeneration. ACS Biomater Sci Eng. 2019;5:509–18. https://doi.org/10.1021/acsbiomaterials.8b01188.

    Article  CAS  Google Scholar 

  51. Ding Z, Yuan Q, Huang K, Gu Z, Xuan M, Xu Q, et al. Double-layer microsphere incorporated with strontium doped calcium polyphosphate scaffold for bone regeneration. J Biomed Nanotechnol. 2019;15:1223–311.

    PubMed  CAS  Google Scholar 

  52. Fu J, Zhuang C, Qiu J, Ke X, Yang X, Jin Z, et al. Core-shell biphasic microspheres with tunable density of shell micropores providing tailorable bone regeneration. Tissue Eng Part A. 2018;25:588–602.

    PubMed  Google Scholar 

  53. Dziadek M, Stodolak-Zych E, Cholewa-Kowalska K. Biodegradable ceramic-polymer composites for biomedical applications: a review. Mater Sci Eng C. 2017;71:1175–91. https://doi.org/10.1016/j.msec.2016.10.014.

    Article  CAS  Google Scholar 

  54. Chen Y, Zheng Z, Zhou R, Zhang H, Chen C, Xiong Z, et al. Developing a strontium-releasing graphene oxide-/collagen-based organic–inorganic nanobiocomposite for large bone defect regeneration via MAPK signaling pathway. ACS Appl Mater Interfaces. 2019;11:15986–97.

    PubMed  CAS  Google Scholar 

  55. Quade M, Vater C, Schlootz S, Bolte J, Langanke R, Bretschneider H, et al. Strontium enhances BMP-2 mediated bone regeneration in a femoral murine bone defect model. J Biomed Mater Res Part B Appl Biomater. 2019;20:1–9.

    Google Scholar 

  56. Aroni MAT, de Oliveira GJPL, Spolidório LC, Andersen OZ, Foss M, Marcantonio RAC, et al. Loading deproteinized bovine bone with strontium enhances bone regeneration in rat calvarial critical size defects. Clin Oral Investig Clin Oral Investig. 2019;23:1605–14.

    PubMed  Google Scholar 

  57. Fenbo M, Xingyu X, Bin T. Strontium chondroitin sulfate/silk fibroin blend membrane containing microporous structure modulates macrophage responses for guided bone regeneration. Carbohydr Polym. 2019;213:266–75. https://doi.org/10.1016/j.carbpol.2019.02.068.

    Article  PubMed  CAS  Google Scholar 

  58. Elgali I, Turri A, Xia W, Norlindh B, Johansson A, Dahlin C, et al. Guided bone regeneration using resorbable membrane and different bone substitutes: early histological and molecular events. Acta Biomater. 2016;29:409–23.

    PubMed  CAS  Google Scholar 

  59. Lu S, Shen M, Zhang F, Wang P, Zuo B, Zhou X, et al. A novel strontium-loaded silk fibroin nanofibrous membrane for guided bone regeneration: in vitro and in vivo studies. Int J Clin Exp Med. 2016;9:7046–59.

    CAS  Google Scholar 

  60. Luz EPCG, de Borges MF, Andrade FK, de Rosa MF, Infantes-Molina A, Rodríguez-Castellón E, et al. Strontium delivery systems based on bacterial cellulose and hydroxyapatite for guided bone regeneration. Cellulose. 2018;25:6661–79.

    CAS  Google Scholar 

  61. Lei B, Guo B, Rambhia KJ, Ma PX. Hybrid polymer biomaterials for bone tissue regeneration. Front Med. 2019;13:189–201.

    PubMed  Google Scholar 

  62. Cheng D, Liang Q, Li Y, Fan J, Wang G, Pan H, et al. Strontium incorporation improves the bone-forming ability of scaffolds derived from porcine bone. Colloids Surf B Biointerfaces. 2018;162:279–87. https://doi.org/10.1016/j.colsurfb.2017.11.070.

    Article  PubMed  CAS  Google Scholar 

  63. Lino AB, McCarthy AD, Fernández JM. Evaluation of strontium-containing PCL-PDIPF scaffolds for bone tissue engineering: in vitro and in vivo studies. Ann Biomed Eng. 2019;47:902–12.

    PubMed  Google Scholar 

  64. Rodríguez-Méndez I, Fernández-Gutiérrez M, Rodríguez-Navarrete A, Rosales-Ibáñez R, Benito-Garzón L, Vázquez-Lasa B, et al. Bioactive Sr(II)/chitosan/poly(ε-caprolactone) scaffolds for craniofacial tissue regeneration In vitro and in vivo behavior. Polymers (Basel). 2018;10:1–26.

    Google Scholar 

  65. Prabha RD, Nair BP, Ditzel N, Kjems J, Nair PD, Kassem M. Strontium functionalized scaffold for bone tissue engineering. Mater Sci Eng C. 2019;94:509–15. https://doi.org/10.1016/j.msec.2018.09.054.

    Article  CAS  Google Scholar 

  66. Masalskas BF, Martins Júnior W, Leoni GB, de Faloni APS, Marcaccini AM, Silva Sousa YTC, et al. Local delivery of strontium ranelate promotes regeneration of critical size bone defects filled with collagen sponge. J Biomed Mater Res Part A. 2018;106:333–41.

    CAS  Google Scholar 

  67. Roohaniesfahani I, Wang J, No YJ, de Candia C, Miao X, Lu Z, et al. Modulatory effect of simultaneously released magnesium, strontium, and silicon ions on injectable silk hydrogels for bone regeneration. Mater Sci Eng C. 2019;94:976–87.

    CAS  Google Scholar 

  68. Wang X, Shao J, Abd El Raouf M, Xie H, Huang H, Wang H, et al. Near-infrared light-triggered drug delivery system based on black phosphorus for in vivo bone regeneration. Biomaterials. 2018;179:164–74.

    PubMed  CAS  Google Scholar 

  69. Wu J, Luo C, Liu X, Qu X, Cao Y, Li M, et al. In vitro and in vivo characterization of strontium-containing calcium sulfate/poly(amino acid) composite as a novel bioactive graft for bone regeneration. RSC Adv R Soc Chem. 2017;7:54306–12.

    Google Scholar 

  70. Autefage H, Allen F, Tang HM, Kallepitis C, Gentleman E, Reznikov N, et al. Multiscale analyses reveal native-like lamellar bone repair and near perfect bone-contact with porous strontium-loaded bioactive glass. Biomaterials. 2019;209:152–62. https://doi.org/10.1016/j.biomaterials.2019.03.035.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Bellucci D, Cannillo V, Anesi A, Salvatori R, Chiarini L, Manfredini T, et al. Bone regeneration by novel bioactive glasses containing strontium and/or magnesium: a preliminary in-vivo study. Materials (Basel). 2018;11:1–13.

    Google Scholar 

  72. Boyd D, Carroll G, Towler MR, Freeman C, Farthing P, Brook IM. Preliminary investigation of novel bone graft substitutes based on strontium–calcium–zinc–silicate glasses. J Mater Sci Mater Med [Internet]. 2009;20:413–20. https://doi.org/10.1007/s10856-008-3569-0.

    Article  CAS  Google Scholar 

  73. Dahl SG, Allain P, Marie PJ, Mauras Y, Boivin G, Ammann P, et al. Incorporation and distribution of strontium in bone. Bone. 2001;28:446–53.

    PubMed  CAS  Google Scholar 

  74. Gorustovich AA, Roether JA, Boccaccini AR. Effect of bioactive**e glasses on angiogenesis: a review of in vitro and in vivo evidences. Tissue Eng Part B Rev. 2009;16:199–207. https://doi.org/10.1089/ten.teb.2009.0416.

    Article  Google Scholar 

  75. Lao J, Jallot E, Nedelec J-M. Strontium-delivering glasses with enhanced bioactivity: a new biomaterial for antiosteoporotic applications? Chem Mater. 2008;20:4969–73. https://doi.org/10.1021/cm800993s.

    Article  CAS  Google Scholar 

  76. Cui X, Huang C, Zhang M, Ruan C, Peng S, Li L, et al. Enhanced osteointegration of poly(methylmethacrylate) bone cements by incorporating strontium-containing borate bioactive glass. J R Soc Interface. 2017;20:14.

    Google Scholar 

  77. Patel U, Macri-Pellizzeri L, Zakir Hossain KM, Scammell BE, Grant DM, Scotchford CA, et al. In vitro cellular testing of strontium/calcium substituted phosphate glass discs and microspheres shows potential for bone regeneration. J Tissue Eng Regen Med. 2019;13:396–405.

    PubMed  PubMed Central  CAS  Google Scholar 

  78. Li J, Liu X, Park S, Miller AL, Terzic A, Lu L. Strontium-substituted hydroxyapatite stimulates osteogenesis on poly(propylene fumarate) nanocomposite scaffolds. J Biomed Mater Res Part A. 2019;107:631–42.

    CAS  Google Scholar 

  79. Naruphontjirakul P, Tsigkou O, Li S, Porter AE, Jones JR. Human mesenchymal stem cells differentiate into an osteogenic lineage in presence of strontium containing bioactive glass nanoparticles. Acta Biomater. 2019;90:373–92.

    PubMed  CAS  Google Scholar 

  80. Huang TH, Kao CT, Shen YF, Lin YT, Liu YT, Yen SY, et al. Substitutions of strontium in bioactive calcium silicate bone cements stimulate osteogenic differentiation in human mesenchymal stem cells. J Mater Sci Mater Med. 2019. https://doi.org/10.1007/s10856-019-6274-2.

    Article  PubMed  Google Scholar 

  81. Oryan A, Baghaban Eslaminejad M, Kamali A, Hosseini S, Sayahpour FA, Baharvand H. Synergistic effect of strontium, bioactive glass and nano-hydroxyapatite promotes bone regeneration of critical-sized radial bone defects. J Biomed Mater Res Part B Appl Biomater. 2019;107:50–64.

    PubMed  CAS  Google Scholar 

  82. Ferreira MM, Brito AF, Brazete D, Pereira IC, Carrilho E, Abrantes AM, et al. Doping β-TCP as a strategy for enhancing the regenerative potential of composite β-TCP-alkali-free bioactive glass bone grafts. Experimental study in rats. Materials (Basel). 2018;20:12.

    Google Scholar 

  83. Wang W, Nune KC, Tan L, Zhang N, Dong J, Yan J, et al. Bone regeneration of hollow tubular magnesium–strontium scaffolds in critical-size segmental defects: effect of surface coatings. Mater Sci Eng C. 2019;100:297–307.

    CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by Zhejiang Provincial Natural Science Foundation of China (LY18H060013), Medical and Health Research Project of Zhejiang, Province (2019KY225), Science and Technology Project of Shaoxing (2018C30077, 2018C30082, 2018C30165).

Author information

Authors and Affiliations

Authors

Contributions

All authors have participated equally in drafting and revising this paper.

Corresponding author

Correspondence to Wenqing Liang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, S., Dong, Y., Chen, M. et al. Recent developments in strontium-based biocomposites for bone regeneration. J Artif Organs 23, 191–202 (2020). https://doi.org/10.1007/s10047-020-01159-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10047-020-01159-y

Keywords

Navigation