The Korean journal of internal medicine

The Korean Association of Internal Medicine (대한내과학회)
권호 표지
DOI QR코드

DOI QR Code

Hard tissue regeneration using bone substitutes: an update on innovations in materials

  • Sarkar, Swapan Kumar (Institute of Tissue Regeneration, Soonchunhyang University College of Medicine) ;
  • Lee, Byong Taek (Institute of Tissue Regeneration, Soonchunhyang University College of Medicine)
  • Published : 2015.05.01
⟨ Previous Next ⟩

Abstract

Bone is a unique organ composed of mineralized hard tissue, unlike any other body part. The unique manner in which bone can constantly undergo self-remodeling has created interesting clinical approaches to the healing of damaged bone. Healing of large bone defects is achieved using implant materials that gradually integrate with the body after healing is completed. Such strategies require a multidisciplinary approach by material scientists, biological scientists, and clinicians. Development of materials for bone healing and exploration of the interactions thereof with the body are active research areas. In this review, we explore ongoing developments in the creation of materials for regenerating hard tissues.

Keywords

Acknowledgement

Supported by : Ministry of Health and Welfare

References

  1. Urist MR, O'Conner BT, Burwell RG. Bone Graft, Derivatives and Substitutes. Oxford: Butterworth Heinemann, 1994.
  2. Flati G, Di Stanislao C. Chirurgia nella preistoria: parte I. Provincia Med Aquila 2004;2:8-11.
  3. Donati D, Zolezzi C, Tomba P, Vigano A. Bone grafting: historical and conceptual review, starting with an old manuscript by Vittorio Putti. Acta Orthop 2007;78:19-25. https://doi.org/10.1080/17453670610013376
  4. Pryor LS, Gage E, Langevin CJ, et al. Review of bone substitutes. Craniomaxi l lofac Trauma Reconstr 2009;2:151-160. https://doi.org/10.1055/s-0029-1224777
  5. de Boer HH. The history of bone grafts. Clin Orthop Relat Res 1988;226:292-298.
  6. De Long WG Jr, Einhorn TA, Koval K, et al. Bone grafts and bone graft substitutes in orthopaedic trauma surgery: a critical analysis. J Bone Joint Surg Am 2007;89:649-658. https://doi.org/10.2106/JBJS.F.00465
  7. Urist MR. Bone: formation by autoinduction. Science 1965;150:893-899. https://doi.org/10.1126/science.150.3698.893
  8. Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000;21:2529-2543. https://doi.org/10.1016/S0142-9612(00)00121-6
  9. Kellomaki M, Niiranen H, Puumanen K, Ashammakhi N, Waris T, Tormala P. Bioabsorbable scaffolds for guided bone regeneration and generation. Biomaterials 2000;21:2495-2505. https://doi.org/10.1016/S0142-9612(00)00117-4
  10. Torres AL, Gaspar VM, Serra IR, et al. Bioactive polymeric-ceramic hybrid 3D scaffold for application in bone tissue regeneration. Mater Sci Eng C Mater Biol Appl 2013;33:4460-4469. https://doi.org/10.1016/j.msec.2013.07.003
  11. Rezwan K, Chen QZ, Blaker JJ, Boccaccini AR. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 2006;27:3413-3431. https://doi.org/10.1016/j.biomaterials.2006.01.039
  12. Sfeir C, Ho L, Doll BA, Azari K, Hollinger JO. Fracture repair. In: Lieberman JR, Friedlaender GE, eds. Bone Regeneration and Repair: Biology and Clinical Applications. Totowa: Humana Press, 2005.
  13. Burg KJ, Porter S, Kellam JF. Biomaterial developments for bone tissue engineering. Biomaterials 2000;21:2347-2359. https://doi.org/10.1016/S0142-9612(00)00102-2
  14. Goff T, Kanakaris NK, Giannoudis PV. Use of bone graft substitutes in the management of tibial plateau fractures. Injury 2013;44 Suppl 1:S86-S94. https://doi.org/10.1016/S0020-1383(13)70019-6
  15. Ricciardi BF, Bostrom MP. Bone graft substitutes: claims and credibility. Semin Arthroplasty 2013;24:119-123. https://doi.org/10.1053/j.sart.2013.07.002
  16. Cannilloa V, Chiellinib F, Fabbria P, Sola A. Production of $Bioglass^{(R)}$ 45S5: polycaprolactone composite scaffolds via salt-leaching. Compos Struct 2010;92:1823-1832. https://doi.org/10.1016/j.compstruct.2010.01.017
  17. Wu C, Zhang Y, Zhu Y, Friis T, Xiao Y. Structure-property relationships of silk-modified mesoporous bioglass scaffolds. Biomaterials 2010;31:3429-3438. https://doi.org/10.1016/j.biomaterials.2010.01.061
  18. Wang X, Ruan JM, Chen QY. Effects of surfactants on the microstructure of porous ceramic scaffolds fabricated by foaming for bone tissue engineering. Mater Res Bull 2009;44:1275-1279. https://doi.org/10.1016/j.materresbull.2009.01.004
  19. Wu C, Ramaswamy Y, Zreiqat H. Porous diopside (CaMg-Si(2)O(6)) scaffold: a promising bioactive material forbone tissue engineering. Acta Biomater 2010;6:2237-2245. https://doi.org/10.1016/j.actbio.2009.12.022
  20. Wu ZY, Hill RG, Yue S, Nightingale D, Lee PD, Jones JR. Melt-derived bioactive glass scaffolds produced by a gelcast foaming technique. Acta Biomater 2011;7:1807-1816. https://doi.org/10.1016/j.actbio.2010.11.041
  21. Xu S, Lin K, Wang Z, et al. Reconstruction of calvarial defect of rabbits using porous calcium silicate bioactive ceramics. Biomaterials 2008;29:2588-2596. https://doi.org/10.1016/j.biomaterials.2008.03.013
  22. Wu C, Luo Y, Cuniberti G, Xiao Y, Gelinsky M. Three-dimensional printing of hierarchical and tough mesoporous bioactive glass scaffolds with a controllable pore architecture, excellent mechanical strength and mineralization ability. Acta Biomater 2011;7:2644-2650. https://doi.org/10.1016/j.actbio.2011.03.009
  23. Karageorgiou V, Kaplan D. Porosity of 3D biomaterialscaffolds and osteogenesis. Biomaterials 2005;26:5474-5491. https://doi.org/10.1016/j.biomaterials.2005.02.002
  24. Inzana JA, Olvera D, Fuller SM, et al. 3D printing of composite calcium phosphate and collagen scaffolds for bone regeneration. Biomaterials 2014;35:4026-4034. https://doi.org/10.1016/j.biomaterials.2014.01.064
  25. Brie J, Chartier T, Chaput C, et al. A new custom made bioceramic implant for the repair of large and complex craniofacial bone defects. J Craniomaxillofac Surg 2013;41:403-407. https://doi.org/10.1016/j.jcms.2012.11.005
  26. Peroglio M, Gremillard L, Eglin D, Lezuo P, Alini M, Chevalier J. Evaluation of a new press-fit in situ setting composite porous scaffold for cancellous bone repair: towards a "surgeon-friendly" bone filler? Acta Biomater 2010;6:3808-3812. https://doi.org/10.1016/j.actbio.2010.03.018
  27. Comesana R, Lusquinos F, del Val J, et al. Calcium phosphate grafts produced by rapid prototyping based on laser cladding. J Eur Ceram Soc 2011;31:29-41. https://doi.org/10.1016/j.jeurceramsoc.2010.08.011
  28. Hayakawa S, Kanaya T, Tsuru K, et al. Heterogeneous structure and in vitro degradation behavior of wet-chemically derived nanocrystalline silicon-containing hydroxyapatite particles. Acta Biomater 2013;9:4856-4867. https://doi.org/10.1016/j.actbio.2012.08.024
  29. Baeza A, Izquierdo-Barba I, Vallet-Regi M. Biotinylation of silicon-doped hydroxyapatite: a new approach to protein fixation for bone tissue regeneration. Acta Biomater 2010;6:743-749. https://doi.org/10.1016/j.actbio.2009.09.004
  30. Hing KA, Revell PA, Smith N, Buckland T. Effect of silicon level on rate, quality and progression of bone healing within silicate-substituted porous hydroxyapatite scaffolds. Biomaterials 2006;27:5014-5026. https://doi.org/10.1016/j.biomaterials.2006.05.039
  31. Boanini E, Torricelli P, Gazzano M, Della Bella E, Fini M2, Bigi A. Combined effect of strontium and zoledronate on hydroxyapatite structure and bone cell responses. Biomaterials 2014;35:5619-5626. https://doi.org/10.1016/j.biomaterials.2014.03.053
  32. Boyd AR, Rutledge L, Randolph LD, Meenan BJ. Strontium- substituted hydroxyapatite coatings deposited via a co-deposition sputter technique. Mater Sci Eng C Mater Biol Appl 2015;46:290-300. https://doi.org/10.1016/j.msec.2014.10.046
  33. Chung CJ, Long HY. Systematic strontium substitution in hydroxyapatite coatings on titanium via micro-arc treatment and their osteoblast/osteoclast responses. Acta Biomater 2011;7:4081-4087. https://doi.org/10.1016/j.actbio.2011.07.004
  34. Tank KP, Chudasama KS, Thaker VS, Joshi MJ. Pure and zinc doped nano-hydroxyapatite: synthesis, characterization, antimicrobial and hemolytic studies. J Cryst Growth 2014;401:474-479. https://doi.org/10.1016/j.jcrysgro.2014.01.062
  35. Ashuri M, Moztarzadeh F, Nezafati N, Hamedani AA, Tahriri M. Development of a composite based on hydroxyapatite and magnesium and zinc-containing solgel-derived bioactive glass for bone substitute applications. Mater Sci Eng C Mater Biol Appl 2012;32:2330-2339. https://doi.org/10.1016/j.msec.2012.07.004
  36. Fox K, Tran PA, Tran N. Recent advances in research applications of nanophase hydroxyapatite. Chemphyschem 2012;13:2495-2506. https://doi.org/10.1002/cphc.201200080
  37. Zakaria SM, Sharif Zein SH, Othman MR, Yang F, Jansen JA. Nanophase hydroxyapatite as a biomaterial in advanced hard tissue engineering: a review. Tissue Eng Part B Rev 2013;19:431-441. https://doi.org/10.1089/ten.teb.2012.0624
  38. Jokic B, Stamenkovic I, Zrilic M, Obradovic-Djuricic K, Petrovic R, Janackovic D. Silicon-doped biphasic $\alpha$-calcium-phosphate/hydroxyapatite scaffolds obtained by a replica foam method using uniform pre-annealed spherical particles. Mater Lett 2012;74:155-158. https://doi.org/10.1016/j.matlet.2012.01.081
  39. Byun IS, Sarkar SK, Anirban Jyoti M, et al. Initial biocompatibility and enhanced osteoblast response of Si doping in a porous BCP bone graft substitute. J Mater Sci Mater Med 2010;21:1937-1947. https://doi.org/10.1007/s10856-010-4061-1
  40. Carpena NT, Jang DW, Padalhin AR, Sarkar SK, Kim BR, Lee BY, Bae JS, Lee BT. Improved bone regeneration of silicon-doped biphasic calcium phosphate micro- channeled granular bone substitute with collagen and BMP-2 surface modification. ACS Appl Mater Interfaces, Submitted and under review.
  41. Kamitakahara M, Imai R, Ioku K. Preparation and evaluation of spherical Ca-deficient hydroxyapatite granules with controlled surface microstructure as drug carriers. Mater Sci Eng C Mater Biol Appl 2013;33:2446-2450. https://doi.org/10.1016/j.msec.2013.01.017
  42. Eshraghi S, Das S. Micromechanical f inite-element modeling and experimental characterization of the compressive mechanical properties of polycaprolactone-hydroxyapatite composite scaffolds prepared by selective laser sintering for bone tissue engineering. Acta Biomater 2012;8:3138-3143. https://doi.org/10.1016/j.actbio.2012.04.022
  43. Laschke MW, Strohe A, Menger MD, Alini M, Eglin D. In vitro and in vivo evaluation of a novel nanosize hydroxyapatite particles/poly(ester-urethane) composite scaffold for bone tissue engineering. Acta Biomater 2010;6:2020-2027. https://doi.org/10.1016/j.actbio.2009.12.004
  44. Shin YM, Jo SY, Park JS, Gwon HJ, Jeong SI, Lim YM. Synergistic effect of dual-functionalized fibrous scaffold with BCP and RGD containing peptide for improved osteogenic differentiation. Macromol Biosci 2014;14:1190-1198. https://doi.org/10.1002/mabi.201400023
  45. Nie L, Chen D, Yang Q, et al. Hydroxyapatite/poly-l-lactide nanocomposites coating improves the adherence and proliferation of human bone mesenchymal stem cells on porous biphasic calcium phosphate scaffolds. Mater Lett 2013;92:25-28. https://doi.org/10.1016/j.matlet.2012.10.077
  46. Milovac D, Gamboa-Martinez TC, Ivankovic M, Gallego Ferrer G, Ivankovic H. PCL-coated hydroxyapatite scaffold derived from cuttlefish bone: in vitro cell culture studies. Mater Sci Eng C Mater Biol Appl 2014;42:264-272. https://doi.org/10.1016/j.msec.2014.05.034
  47. Gunn JM, Rekola J, Hirvonen J, Aho AJ. Comparison of the osteoconductive properties of three particulate bone fillers in a rabbit model: allograft, calcium carbonate ($Biocoral^{(R)}$) and S53P4 bioactive glass. Acta Odontol Scand 2013;71:1238-1242. https://doi.org/10.3109/00016357.2012.757642
  48. Hench LL, Pantano CG Jr, Buscemi PJ, Greenspan DC. Analysis of bioglass fixation of hip prostheses. J Biomed Mater Res 1977;11:267-282. https://doi.org/10.1002/jbm.820110211
  49. Hench LL. Bioceramics. J Am Ceram Soc 1998;81:1705-1728.
  50. Piotrowski G, Hench LL, Allen WC, Miller GJ. Mechanical studies of the bone bioglass interfacial bond. J Biomed Mater Res 1975;9:47-61. https://doi.org/10.1002/jbm.820090408
  51. Erol MM, Mourino V, Newby P, et al. Copper-releasing, boron-containing bioactive glass-based scaffolds coated with alginate for bone tissue engineering. Acta Biomater 2012;8:792-801. https://doi.org/10.1016/j.actbio.2011.10.013
  52. Vrouwenvelder WC, Groot CG, de Groot K. Better histology and biochemistry for osteoblasts cultured on titanium-doped bioactive glass: bioglass 45S5 compared with iron-, titanium-, f luorine- and boron-containing bioactive glasses. Biomaterials 1994;15:97-106. https://doi.org/10.1016/0142-9612(94)90257-7
  53. Khorami M, Hesaraki S, Behnamghader A, Nazarian H, Shahrabi S. In vitro bioactivity and biocompatibility of lithium substituted 45S5 bioglass. Mater Sci Eng C Mater Biol Appl 2011;31:1584-1592. https://doi.org/10.1016/j.msec.2011.07.011
  54. ElBatal HA, Khalil EM, Hamdy YM. In vitro behavior of bioactive phosphate glass-ceramics from the system P2O5-Na2O-CaO containing titania. Ceram Int 2009;35:1195-1204. https://doi.org/10.1016/j.ceramint.2008.06.004
  55. Cannas M, Indemini E, Krajewski A, Ravaglioli A, Contoli S. In vitro observations of iron-doped bioactive glasses. Biomaterials 1990;11:281-285. https://doi.org/10.1016/0142-9612(90)90011-E
  56. Sabareeswaran A, Basu B, Shenoy SJ, Jaffer Z, Saha N, Stamboulis A. Early osseointegration of a strontium containing glass ceramic in a rabbit model. Biomaterials 2013;34:9278-9286. https://doi.org/10.1016/j.biomaterials.2013.08.070
  57. Silva Lazaro G, Santos SC, Resende CX, Santos EA. Individual and combined effects of the elements Zn, Mg and Sr on the surface reactivity of a SiO2.CaO.Na2O.P2O5 bioglass system. J Non Cryst Solids 2014;386:19-28. https://doi.org/10.1016/j.jnoncrysol.2013.11.038
  58. Vedel E, Zhang D, Arstila H, Hupa L, Hupa M. Predicting physical and chemical properties of bioactive glasses from chemical composition: part 4: tailoring compositions with desired properties. Glass Technol Eur J Glass Sci Technol A 2009;50:9-16.
  59. Brink M. The influence of alkali and alkaline earths on the working range for bioactive glasses. J Biomed Mater Res 1997;36:109-117. https://doi.org/10.1002/(SICI)1097-4636(199707)36:1<109::AID-JBM13>3.0.CO;2-D
  60. Elgayar I, Aliev AE, Boccaccini AR, Hill RG. Structural analysis of bioactive glasses. . J Non Cryst Solids 2005;351:173-183. https://doi.org/10.1016/j.jnoncrysol.2004.07.067
  61. Bellucci D, Cannillo V, Sola A. Calcium and potassium addition to facilitate the sintering of bioactive glasses. Mater Lett 2011;65:1825-1827. https://doi.org/10.1016/j.matlet.2011.03.060
  62. Sarkar SK, Sadiasa A, Lee BT. Synthesis of a novel bioactive glass using the ultrasonic energy assisted hydrothermal method and their biocompatibility evaluation. J Mater Res 2014;29:1781-1789. https://doi.org/10.1557/jmr.2014.215
  63. Wu C, Chang J. Multifunctional mesoporous bioactive glasses for effective delivery of therapeutic ions and drug/growth factors. J Control Release 2014;193:282-295. https://doi.org/10.1016/j.jconrel.2014.04.026
  64. Zhang Y, Cheng N, Miron R, Shi B, Cheng X. Delivery of PDGF-B and BMP-7 by mesoporous bioglass/silk fibrin scaffolds for the repair of osteoporotic defects. Biomaterials 2012;33:6698-6708. https://doi.org/10.1016/j.biomaterials.2012.06.021
  65. Wang X, Li X, Ito A, Sogo Y. Synthesis and characterization of hierarchically macroporous and mesoporous CaO-MO-SiO(2)-P(2)O(5) (M=Mg, Zn, Sr) bioactive glass scaffolds. Acta Biomater 2011;7:3638-3644. https://doi.org/10.1016/j.actbio.2011.06.029
  66. Chen QZ, Thouas GA. Fabrication and characterization of sol-gel derived 45S5 $Bioglass^{(R)}$-ceramic scaffolds. Acta Biomater 2011;7:3616-3626. https://doi.org/10.1016/j.actbio.2011.06.005
  67. Sepulveda P, Jones JR, Hench LL. Bioactive sol-gel foams for tissue repair. J Biomed Mater Res 2002;59:340-348. https://doi.org/10.1002/jbm.1250
  68. Niemela T, Niiranen H, Kellomaki M, Tormala P. Self-reinforced composites of bioabsorbable polymer and bioactive glass with different bioactive glass contents. Part I: Initial mechanical properties and bioactivity. Acta Biomater 2005;1:235-242. https://doi.org/10.1016/j.actbio.2004.11.002
  69. Maquet V, Boccaccini AR, Pravata L, Notingher I, Jerome R. Porous poly(alpha-hydroxyacid)/Bioglass composite scaffolds for bone tissue engineering I: Preparation and in vitro characterisation. Biomaterials 2004;25:4185-4194. https://doi.org/10.1016/j.biomaterials.2003.10.082
  70. Cattini A, Bellucci D, Sola A, Pawlowski L, Cannillo V. Suspension plasma spraying of optimised functionally graded coatings of bioactive glass/hydroxyapatite. Surf Coat Technol 2013;236:118-126. https://doi.org/10.1016/j.surfcoat.2013.09.037
  71. Rojaee R, Fathi M, Raeissi K. Electrophoretic deposition of nano structured hydroxyapatite coating on AZ91 magnesium alloy implants with different surface treatments. Appl Surf Sci 2013;285:664-673. https://doi.org/10.1016/j.apsusc.2013.08.108
  72. Dorozhkin SV. Biocomposites and hybrid biomaterials based on calcium orthophosphates. Biomatter 2011;1:3-56. https://doi.org/10.4161/biom.1.1.16782
  73. Okamoto M, John B. Synthetic biopolymer nanocomposites for tissue engineering scaffolds. Prog Polym Sci 2013;38:1487-1503. https://doi.org/10.1016/j.progpolymsci.2013.06.001
  74. Liu Y, Lim J, Teoh SH. Review: development of clinically relevant scaffolds for vascularised bone tissue engineering. Biotechnol Adv 2013;31:688-705. https://doi.org/10.1016/j.biotechadv.2012.10.003
  75. Swetha M, Sahithi K, Moorthi A, Srinivasan N, Ramasamy K, Selvamurugan N. Biocomposites containing natural polymers and hydroxyapatite for bone tissue engineering. Int J Biol Macromol 2010;47:1-4. https://doi.org/10.1016/j.ijbiomac.2010.03.015
  76. Sokolsky-Papkov M, Agashi K, Olaye A, Shakesheff K, Domb AJ. Polymer carriers for drug delivery in tissue engineering. Adv Drug Deliv Rev 2007;59:187-206. https://doi.org/10.1016/j.addr.2007.04.001
  77. Sahoo S, Ang LT, Goh JC, Toh SL. Growth factor delivery through electrospun nanofibers in scaffolds for tissue engineering applications. J Biomed Mater Res A 2010;93:1539-1550.
  78. Bao M, Lou X, Zhou Q, Dong W, Yuan H, Zhang Y. Electrospun biomimetic fibrous scaffold from shape memory polymer of PDLLA-co-TMC for bone tissue engineering. ACS Appl Mater Interfaces 2014;6:2611-2621. https://doi.org/10.1021/am405101k
  79. Ribeiro N, Sousa SR, van Blitterswijk CA, Moroni L, Monteiro FJ. A biocomposite of collagen nanofibers and nanohydroxyapatite for bone regeneration. Biofabrication 2014;6:035015. https://doi.org/10.1088/1758-5082/6/3/035015
  80. Kim YH, Lee BT. Novel approach to the fabrication of an artificial small bone using a combination of sponge replica and electrospinning methods. Sci Technol Adv Mater 2011;12:035002. https://doi.org/10.1088/1468-6996/12/3/035002
  81. Kim BR, Nguyen TB, Min YK, Lee BT. In vitro and in vivo studies of BMP-2-loaded PCL-gelatin-BCP electrospun scaffolds. Tissue Eng Part A 2014;20:3279-3289. https://doi.org/10.1089/ten.tea.2014.0081
  82. Park JB. The use of hydrogels in bone-tissue engineering. Med Oral Patol Oral Cir Bucal 2011;16:e115-e118.
  83. Slaughter BV, Khurshid SS, Fisher OZ, Khademhosseini A, Peppas NA. Hydrogels in regenerative medicine. Adv Mater 2009;21:3307-3329. https://doi.org/10.1002/adma.200802106
  84. Amirian J, Thuy Ba Linh N, Min YK, Lee BT. The effect of BMP-2 and VEGF loading of gelatin-pectin-BCP scaffolds to enhance osteoblast proliferation. J Appl Polym Sci 2014 Aug 11 [Epub]. http://dx.doi.org/10.1002/app.41241.
  85. Nguyen MK, Alsberg E. Bioactive factor delivery strategies from engineered polymer hydrogels for therapeutic medicine. Prog Polym Sci 2014;39:1236-1265.
  86. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147. https://doi.org/10.1126/science.284.5411.143
  87. Montjovent MO, Burri N, Mark S, et al. Fetal bone cells for tissue engineering. Bone 2004;35:1323-1333. https://doi.org/10.1016/j.bone.2004.07.001
  88. Dee KC, Anderson TT, Bizios R. Osteoblast population migration characteristics on substrates modified with immobilized adhesive peptides. Biomaterials 1999;20:221-227. https://doi.org/10.1016/S0142-9612(98)00161-6
  89. Rezania A, Healy KE. Biomimetic peptide surfaces that regulate adhesion, spreading, cytoskeletal organization, and mineralization of the matrix deposited by osteoblast-like cells. Biotechnol Prog 1999;15:19-32. https://doi.org/10.1021/bp980083b
  90. Burdick JA, Anseth KS. Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering. Biomaterials 2002;23:4315-4323. https://doi.org/10.1016/S0142-9612(02)00176-X
  91. Weinand C, Pomerantseva I, Neville CM, et al. Hydrogel-beta-TCP scaffolds and stem cells for tissue engineering bone. Bone 2006;38:555-563. https://doi.org/10.1016/j.bone.2005.10.016
  92. Lawson MA, Barralet JE, Wang L, Shelton RM, Triffitt JT. Adhesion and growth of bone marrow stromal cells on modified alginate hydrogels. Tissue Eng 2004;10:1480-1491. https://doi.org/10.1089/ten.2004.10.1480
  93. Simmons CA, Alsberg E, Hsiong S, Kim WJ, Mooney DJ. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 2004;35:562-569. https://doi.org/10.1016/j.bone.2004.02.027
  94. Schantz JT, Hutmacher DW, Lam CX, et al. Repair of calvarial defects with customised tissue-engineered bone grafts II: evaluation of cellular efficiency and efficacy in vivo. Tissue Eng 2003;9 Suppl 1:S127-S139.
  95. Fowler EB, Cuenin MF, Hokett SD, et al. Evaluation of pluronic polyols as carriers for grafting materials: study in rat calvaria defects. J Periodontol 2002;73:191-197. https://doi.org/10.1902/jop.2002.73.2.191
  96. Nath SD, Abueva C, Kim B, Lee BT. Chitosan-hyaluronic acid polyelectrolyte complex scaffold crosslinked with genipin for immobilization and controlled release of BMP-2. Carbohydr Polym 2015;115:160-169. https://doi.org/10.1016/j.carbpol.2014.08.077
  97. Barbetta A, Rizzitelli G, Bedini R, Peccib R, Dentini M. Porous gelatin hydrogels by gas-in-liquid foam templating. Soft Matter 2010;6:1785-1792. https://doi.org/10.1039/b920049e
  98. Nam YS, Park TG. Biodegradable polymeric microcellular foams by modified thermally induced phase separation method. Biomaterials 1999;20:1783-1790. https://doi.org/10.1016/S0142-9612(99)00073-3
  99. Wen Y, Grondahl L, Gallego MR, Jorgensen L, Moller EH, Nielsen HM. Delivery of dermatan sulfate from polyelectrolyte complex-containing alginate composite microspheres for tissue regeneration. Biomacromolecules 2012;13:905-917. https://doi.org/10.1021/bm201821x
  100. Wan AC, Tai BC, Schumacher KM, Schumacher A, Chin SY, Ying JY. Polyelectrolyte complex membranes for specific cell adhesion. Langmuir 2008;24:2611-2617. https://doi.org/10.1021/la7025768
  101. Boddohi S, Moore N, Johnson PA, Kipper MJ. Polysaccharide-based polyelectrolyte complex nanoparticles from chitosan, heparin, and hyaluronan. Biomacromolecules 2009;10:1402-1409. https://doi.org/10.1021/bm801513e
  102. Wan AC, Yim EK, Liao IC, Le Visage C, Leong KW. Encapsulation of biologics in self-assembled fibers as biostructural units for tissue engineering. J Biomed Mater Res A 2004;71:586-595.
  103. Shovsky A, Varga I, Makuska R, Claesson PM. Formation and stability of water-soluble, molecular polyelectrolyte complexes: effects of charge density, mixing ratio, and polyelectrolyte concentration. Langmuir 2009;25:6113-6121. https://doi.org/10.1021/la804189w
  104. Shovsky A, Bijelic G, Varga I, Makuska R, Claesson PM. Adsorption characteristics of stoichiometric and nonstoichiometric molecular polyelectrolyte complexes on silicon oxynitride surfaces. Langmuir 2011;27:1044-1050. https://doi.org/10.1021/la103957v
  105. Abbah SA, Liu J, Lam RW, Goh JC, Wong HK. In vivo bioactivity of rhBMP-2 delivered with novel polyelectrolyte complexation shells assembled on an alginate microbead core template. J Control Release 2012;162:364-372. https://doi.org/10.1016/j.jconrel.2012.07.027
  106. Chu H, Johnson NR, Mason NS, Wang Y. A [polycation: heparin] complex releases growth factors with enhanced bioactivity. J Control Release 2011;150:157-163. https://doi.org/10.1016/j.jconrel.2010.11.025
  107. Czichocki G, Dautzenberg H, Capan E, Vorlop KD. New and effective entrapment of polyelectrolyte-enzyme-complexes in Lent iKats. Biotechnol Lett 2001;23:1303-1307. https://doi.org/10.1023/A:1010569322537
  108. Trubetskoy VS, Loomis A, Hagstrom JE, Budker VG, Wolff JA. Layer-by-layer deposition of oppositely charged polyelectrolytes on the surface of condensed DNA particles. Nucleic Acids Res 1999;27:3090-3095. https://doi.org/10.1093/nar/27.15.3090
  109. Liu W, Sun S, Cao Z, et al. An investigation on the physicochemical properties of chitosan/DNA polyelectrolyte complexes. Biomaterials 2005;26:2705-2711. https://doi.org/10.1016/j.biomaterials.2004.07.038
  110. Nguyen TB, Lee BT. A combination of biphasic calcium phosphate scaffold with hyaluronic acid-gelatin hydrogel as a new tool for bone regeneration. Tissue Eng Part A 2014;20:1993-2004. https://doi.org/10.1089/ten.tea.2013.0352
  111. Hench LL. Bioceramics: from concept to clinic. J Am Ceram Soc 1991;74:1487-1510. https://doi.org/10.1111/j.1151-2916.1991.tb07132.x
  112. Tancred DC, Carr AJ, McCormack BA. The sintering and mechanical behavior of hydroxyapatite with bioglass additions. J Mater Sci Mater Med 2001;12:81-93.
  113. Suchanek W, Yashima M, Kakihana M, Yoshimura M. Processing and mechanical properties of hydroxyapatite reinforced with hydroxyapatite whiskers. Biomaterials 1996;17:1715-1723. https://doi.org/10.1016/0142-9612(96)87652-6
  114. Jun YK, Kim WH, Kweon OK, Hong SH. The fabrication and biochemical evaluation of alumina reinforced calcium phosphate porous implants. Biomaterials 2003;24:3731-3739. https://doi.org/10.1016/S0142-9612(03)00248-5
  115. Hu H, Xu G, Zan Q, et al. In situ formation of nano-hydroxyapatite whisker reinfoced porous $\beta$-TCP scaffolds. Microelectron Eng 2012;98:566-569. https://doi.org/10.1016/j.mee.2012.07.001
  116. Kang Y, Scully A, Young DA, et al. Enhanced mechanical performance and biological evaluation of a PLGA coated $\beta$-TCP composite scaffold for load-bearing applications. Eur Polym J 2011;47:1569-1577. https://doi.org/10.1016/j.eurpolymj.2011.05.004
  117. Lee BT, Sarkar SK, Song HY. Novel bamboo-like f ibrous, micro-channeled and functional gradient microstructure control of ceramics. Mater Trans 2008;49:339-344. https://doi.org/10.2320/matertrans.MRA2007148
  118. Feng P, Wei P, Li P, Gao C, Shuai C, Peng S. Calcium silicate ceramic scaffolds toughened with hydroxyapatite whiskers for bone tissue engineering. Mater Charact 2014;97:47-56. https://doi.org/10.1016/j.matchar.2014.08.017
  119. McNamara SL, Rnjak-Kovacina J, Schmidt DF, Lo TJ, Kaplan DL. Silk as a biocohesive sacrificial binder in the fabrication of hydroxyapatite load bearing scaffolds. Biomaterials 2014;35:6941-6953. https://doi.org/10.1016/j.biomaterials.2014.05.013
  120. Giannitelli SM, Accoto D, Trombetta M, Rainer A. Current trends in the design of scaffolds for computer-aided tissue engineering. Acta Biomater 2014;10:580-594. https://doi.org/10.1016/j.actbio.2013.10.024
  121. Melchels FP, Domingos MA, Klein TJ, Malda J, Bartolo PJ, Hutmacher DW. Additive manufacturing of tissues and organs. Prog Polym Sci 2012;37:1079-1104. https://doi.org/10.1016/j.progpolymsci.2011.11.007
  122. Bartolo PJ, Almeida H, Laoui T. Rapid prototyping and manufacturing for tissue engineering scaffolds. Int J Comput Appl Technol 2009;36:1-9. https://doi.org/10.1504/IJCAT.2009.026664
  123. Peltola SM, Melchels FP, Grijpma DW, Kellomaki M. A review of rapid prototyping techniques for tissue engineering purposes. Ann Med 2008;40:268-280. https://doi.org/10.1080/07853890701881788
  124. Liu X, Rahaman MN, Fu Q. Bone regeneration in strong porous bioactive glass (13-93) scaffolds with an oriented microstructure implanted in rat calvarial defects. Acta Biomater 2013;9:4889-4898. https://doi.org/10.1016/j.actbio.2012.08.029
  125. Rubshtein AP, Trakhtenberg ISh, Makarova EB, et al. Porous material based on spongy titanium granules: structure, mechanical properties, and osseointegration. Mater Sci Eng C Mater Biol Appl 2014;35:363-369. https://doi.org/10.1016/j.msec.2013.11.020
  126. Kim YH, Jyoti MA, Youn MH, et al. In vitro and in vivo evaluation of a macro porous beta-TCP granule-shaped bone substitute fabricated by the fibrous monolithic process. Biomed Mater 2010;5:035007. https://doi.org/10.1088/1748-6041/5/3/035007
  127. Gomez-Barrena E, Rosset P, Lozano D, Stanovici J, Ermthaller C, Gerbhard F. Bone fracture healing: cell therapy in delayed unions and nonunions. Bone 2015;70:93-101. https://doi.org/10.1016/j.bone.2014.07.033
  128. Langer R, Vacanti JP. Tissue engineering. Science 1993;260:920-926. https://doi.org/10.1126/science.8493529
  129. Kaigler D, Pagni G, Park CH, et al. Stem cell therapy for craniofacial bone regeneration: a randomized, controlled feasibility trial. Cell Transplant 2013;22:767-777. https://doi.org/10.3727/096368912X652968
  130. Jager M, Hernigou P, Zilkens C, et al. Cell therapy in bone healing disorders. Orthop Rev 2010;2:e20. https://doi.org/10.4081/or.2010.e20
  131. Hernigou P, Mathieu G, Poignard A, Manicom O, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions: surgical technique. J Bone Joint Surg Am 2006;88 Suppl 1:322-327. https://doi.org/10.2106/00004623-200609001-00015
  132. Hernigou P, Poignard A, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Influence of the number and concentration of progenitor cells. J Bone Joint Surg Am 2005;87:1430-1437. https://doi.org/10.2106/JBJS.D.02215

Cited by

  1. A comparative study of the areas of osteochondral defects produced in femoral condyles of rabbits treated with sugar cane biopolymer gel vol.30, pp.11, 2015, https://doi.org/10.1590/s0102-865020150110000008
  2. Evaluation of BMMSCs-EPCs sheets for repairing alveolar bone defects in ovariectomized rats vol.7, pp.None, 2017, https://doi.org/10.1038/s41598-017-16404-3
  3. Synthesis and Characterization of Akermanite by Mechanical Milling and Subsequent Heat Treatment vol.1082, pp.None, 2018, https://doi.org/10.1088/1742-6596/1082/1/012021
  4. Advanced Therapy Medicinal Products: A Guide for Bone Marrow-derived MSC Application in Bone and Cartilage Tissue Engineering vol.24, pp.2, 2015, https://doi.org/10.1089/ten.teb.2017.0305
  5. Bone regeneration strategy by different sized multichanneled biphasic calcium phosphate granules: In vivo evaluation in rabbit model vol.32, pp.10, 2015, https://doi.org/10.1177/0885328218768605
  6. The role of fish scale derived scaffold and platelet rich plasma in healing of rabbit tibial defect: an experimental study vol.87, pp.4, 2015, https://doi.org/10.2754/avb201887040363
  7. Isolation and characterization of minipig perivascular stem cells for bone tissue engineering vol.18, pp.4, 2015, https://doi.org/10.3892/mmr.2018.9410
  8. Laser Cladding of Ti-6Al-4V Alloy with Ti-Al2O3 Coating for Biomedical Applications vol.350, pp.None, 2015, https://doi.org/10.1088/1757-899x/350/1/012005
  9. Bioactive Glasses: From Parent 45S5 Composition to Scaffold-Assisted Tissue-Healing Therapies vol.9, pp.1, 2015, https://doi.org/10.3390/jfb9010024
  10. 3D Printing and Electrospinning of Composite Hydrogels for Cartilage and Bone Tissue Engineering vol.10, pp.3, 2015, https://doi.org/10.3390/polym10030285
  11. Effect of Polymethylmethacrylate-Hydroxyapatite Composites on Callus Formation and Compressive Strength in Goat Vertebral Body vol.12, pp.3, 2015, https://doi.org/10.5704/moj.1811.002
  12. A Radiological Approach to Evaluate Bone Graft Integration in Reconstructive Surgeries vol.9, pp.7, 2015, https://doi.org/10.3390/app9071469
  13. Metal-Based Nanostructures/PLGA Nanocomposites: Antimicrobial Activity, Cytotoxicity, and Their Biomedical Applications vol.12, pp.3, 2020, https://doi.org/10.1021/acsami.9b19435
  14. Scaffolds and coatings for bone regeneration vol.31, pp.3, 2015, https://doi.org/10.1007/s10856-020-06364-y
  15. A biphasic calcium phosphate ceramic scaffold loaded with oxidized cellulose nanofiber–gelatin hydrogel with immobilized simvastatin drug for osteogenic differentiation vol.108, pp.4, 2020, https://doi.org/10.1002/jbm.b.34471
  16. Evaluation of the In Vivo Biological Effects of Marine Collagen and Hydroxyapatite Composite in a Tibial Bone Defect Model in Rats vol.22, pp.3, 2020, https://doi.org/10.1007/s10126-020-09955-6
  17. Antibacterial graphene‐based hydroxyapatite/chitosan coating with gentamicin for potential applications in bone tissue engineering vol.108, pp.11, 2015, https://doi.org/10.1002/jbm.a.36974
  18. Sintering Behavior of a Six-Oxide Silicate Bioactive Glass for Scaffold Manufacturing vol.10, pp.22, 2020, https://doi.org/10.3390/app10228279
  19. Long-Term Effect of Honeycomb β-Tricalcium Phosphate on Zygomatic Bone Regeneration in Rats vol.13, pp.23, 2015, https://doi.org/10.3390/ma13235374
  20. Rabbit umbilical cord mesenchymal stem cells: A new option for tissue engineering vol.23, pp.1, 2021, https://doi.org/10.1002/jgm.3282
  21. Synthesis and characterization of poly(vinyl alcohol)/chondroitin sulfate composite hydrogels containing strontium‐doped hydroxyapatite as promising biomaterials vol.109, pp.7, 2015, https://doi.org/10.1002/jbm.a.37108