Skip to main content

Advertisement

SpringerLink
Log in

Biomaterials, substitutes, and tissue engineering in bone repair: current and future concepts

  • Review Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

Bone is a complex, constantly changing organ comprised of mineralized hard tissue. This important structural component of vertebrate’s body serves a variety of functions. Healthy bone system is essential for lifelong execution of these functions. Millions of people worldwide suffer from bone defects due to various reasons, including trauma, tumor, bone diseases, congenital defects, and aging. These defects are increasingly becoming the majority of the clinical cases in orthopedics. For all the aforementioned cases in which the normal process of bone regeneration is either impaired or simply insufficient, there are currently a number of treatment methods available which can be used either alone or in combination for the enhancement of bone healing and regeneration. Accordingly, bone repair has been the focus of many research activities related to clinical therapies. The traditional bone repair procedure widely used in current era involves the use of bone-grafting methods such as autografts, allografts, and xenografts; however, these methods are associated with number of limitations. Therefore, to overcome these problems, tissue engineering as a new and developing option had been introduced recently. In order to provide ideal bone substitutes, a wide range of biomaterials and synthetic bone substitutes are available depending on the goal, each has advantages and disadvantages. The combined use of different bone substitutes together with healing promotive factors, stem cells, gene therapy, and more recently, three-dimensional printing of tissue-engineered constructs may open new insights in bone regeneration in near future. In this review, we describe developments and recognized properties of some of the most utilized materials in bone regenerative medicine heretofore. It may be concluded that presently strong requirements are still to be met in the repair and regeneration of bone defects.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alsousou J, Thompson M, Hulley P, Noble A, Willett K (2009) The biology of platelet-rich plasma and its application in trauma and orthopaedic surgery: a review of the literature. J Bone Joint Surg Br 91(8):987–996

    Article  CAS  PubMed  Google Scholar 

  • Aurrekoetxea M, Garcia-Gallastegui P, Irastorza I, Luzuriaga J, Uribe-Etxebarria V, Unda F et al (2015) Dental pulp stem cells as a multifaceted tool for bioengineering and the regeneration of craniomaxillofacial tissues. Front Physiol 6:289

    Article  PubMed  PubMed Central  Google Scholar 

  • Balmayor ER, van Griensven M (2015) Gene therapy for bone engineering. Front Bioeng Biotechnol 3:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Barba M, Cicione C, Bernardini C, Michetti F, Lattanzi W (2013) Adipose-derived mesenchymal cells for bone regereneration: state of the art. Biomed Res Int 2013:416391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnes K, Lanz O, Werre S, Clapp K, Gilley R (2015) Comparison of autogenous cancellous bone grafting and extracorporeal shock wave therapy on osteotomy healing in the tibial tuberosity advancement procedure in dogs. Radiographic densitometric evaluation. Vet Comp Orthop Traumatol 28(3):207–214

    Article  CAS  PubMed  Google Scholar 

  • Buckwalter JA, Cooper RR (1987) Bone structure and function. Instr Course Lect 36:2748

    Google Scholar 

  • Cadman J, Zhou S, Chen Y, Li Q (2012) Cuttlebone: characterisation, application and development of biomimetic materials. J Bionic Eng 9(3):367–376

    Article  Google Scholar 

  • Calori GM, D'Avino M, Tagliabue L, Albisetti W, d'Imporzano M, Peretti G (2006) An ongoing research for evaluation of treatment with BMPs or AGFs in long bone non-union: protocol description and preliminary results. Injury 37(Suppl 3):S43–S50

    Article  PubMed  Google Scholar 

  • Campana V, Milano G, Pagano E, Barba M, Cicione C, Salonna G et al (2014) Bone substitutes in orthopaedic surgery: from basic science to clinical practice. J Mater Sci Mater Med 25(10):2445–2461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cha JK, Lee JS, Kim MS, Choi SH, Cho KS, Jung UW (2014) Sinus augmentation using BMP-2 in a bovine hydroxyapatite/collagen carrier in dogs. J Clin Periodontol 41(1):86–93

    Article  CAS  PubMed  Google Scholar 

  • Chen YC, Chen RN, Jhan HJ, Liu DZ, Ho HO, Mao Y et al (2015) Development and characterization of acellular extracellular matrix scaffolds from porcine menisci for use in cartilage tissue engineering. Tissue Eng Part C Methods 21(9):971–986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen G, Yang L, Lv Y (2016) Cell-free scaffolds with different stiffness but same microstructure promote bone regeneration in rabbit large bone defect model. J Biomed Mater Res A 104(4):833–841

    Article  CAS  PubMed  Google Scholar 

  • Chou CH, Chen YG, Lin CC, Lin SM, Yang KC, Chang SH (2014) Bioabsorbable fish scale for the internal fixation of fracture: a preliminary study. Tissue Eng Part A 20(17–18):2493–2502

    Article  CAS  PubMed  Google Scholar 

  • Civinini R, Macera A, Nistri L, Redl B, Innocenti M (2011) The use of autologous blood-derived growth factors in bone regeneration. Clin Cases Miner Bone Metab 8(1):25–31

    PubMed  PubMed Central  Google Scholar 

  • Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3(Suppl 3):S131–S139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke SA, Walsh P, Maggs CA, Buchanan F (2011) Designs from the deep: marine organisms for bone tissue engineering. Biotechnol Adv 29(6):610–617

    Article  CAS  PubMed  Google Scholar 

  • Cray J Jr, Henderson SE, Smith DM, Kinsella CR Jr, Bykowski M, Cooper GM et al (2014) BMP-2-regenerated calvarial bone: a biomechanical appraisal in a large animal model. Ann Plast Surg 73(5):591–597

    Article  CAS  PubMed  Google Scholar 

  • De Baat P, Heijboer MP, De Baat C (2005) Development, physiology, and cell activity of bone. Ned Tijdschr Tandheelkd 112(7):258–263

    PubMed  Google Scholar 

  • Denny HR, Butterworth SJ (2000) A guide to canine and feline orthopaedic surgery, 4th edn. Blackwell, Australia

    Book  Google Scholar 

  • Dewi AH, Ana ID, Wolke J, Jansen J (2015) Behavior of POP-calcium carbonate hydrogel as bone substitute with controlled release capability: a study in rat. J Biomed Mater Res A 103(10):3273–3283

    Article  CAS  PubMed  Google Scholar 

  • Dhillon RS, Schwarz EM, Maloney MD (2012) Platelet-rich plasma therapy—future or trend? Arthritis Res Ther 14(4):219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimitriou R, Jones E, McGonagle D, Giannoudis PV (2011) Bone regeneration: current concepts and future directions. BMC Med 9:66

    Article  PubMed  PubMed Central  Google Scholar 

  • Dogan E, Okumus Z (2014) Cuttlebone used as a bone xenograft in bone healing. Vet Med (Praha) 59(5):254–260

    Article  Google Scholar 

  • Dong J, Mo X, Li Y, Chen D (2012) Recent research progress of decellularization of native tissues. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 29(5):1007–1013

    CAS  PubMed  Google Scholar 

  • DurmuŞlar MC, Alpaslan C, Alpaslan G, Çakır M (2014) Clinical and radiographic evaluation of the efficacy of plateletrich plasma combined with hydroxyapatite bone graft substitutes in the treatment of intrabony defects in maxillofacial region. Acta Odontol Scand 72(8):948–953

    Article  CAS  PubMed  Google Scholar 

  • EL Backly RM, Zaky SH, Canciani B, Saad MM, Eweida AM, Brun F et al (2014) Platelet rich plasma enhances osteoconductive properties of a hydroxyapatite/β-tricalcium phosphate scaffold (Skelite) for late healing of critical size rabbit calvarial defects. J Craniomaxillofac Surg 42(5):e70–e79

    Article  PubMed  Google Scholar 

  • Farahani F, Fattahian HR, Kajbafzadeh AM (2015) Experimental study on ostrich dermal acellular matrix in repair of full thickness wounds of guinea pig. Kafkas Univ Vet Fak 21(5):697

    Google Scholar 

  • Farnebo S, Woon CY, Bronstein JA, Schmitt T, Lindsey DP, Pham H et al (2014 Jan) Decellularized tendon-bone composite grafts for extremity reconstruction: an experimental study. Plast Reconstr Surg 133(1):79–89

    Article  CAS  PubMed  Google Scholar 

  • Fatourehchi M, Fattahian HR, Kajbafzadeh AM (2015) The experimental study of bio-engineered free-cell ostrich cornea as xenograft. Comp Pathobiol. Comp pathbiol 12(2)

  • Funamoto S, Nam K, Kimura T, Murakoshi A, Hashimoto Y, Niwaya K et al (2010) The use of high-hydrostatic pressure treatment to decellularize blood vessels. Biomaterials 31(13):3590–3595

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Cui X (2016) Three-dimensional bioprinting in tissue engineering and regenerative medicine. Biotechnol Lett 38(2):203–211

    Article  CAS  PubMed  Google Scholar 

  • Gao Z, Mao TQ, Chen FL, He LS, Hou R, Yang YW et al (2007) The preparation of series of controllable degredation coral-hydroxyapatite (SCHA-200R) and the on its application as the scaffold in bone tissue-engineering. Zhonghua Zheng Xing Wai Ke Za Zhi 23(3):236–240

    PubMed  Google Scholar 

  • Gomez-Barrena E, Rosset P, Muller I, Giordano R, Bunu C, Layrolle P et al (2011) Bone regeneration: stem cell therapies and clinical studies in orthopaedics and traumatology. J Cell Mol Med 15(6):1266–1286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Barrena E, Rosset P, Lozano D, Stanovici J, Ermthaller C, Gerbhard F (2015) Bone fracture healing: cell therapy in delayed unions and nonunions. Bone 70:93–101

    Article  PubMed  Google Scholar 

  • Gong T, Xie J, Liao J, Zhang T, Lin S, Lin Y (2015) Nanomaterials and bone regeneration. Bone Res 3:15029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hakimi M, Jungbluth P, Sager M, Betsch M, Herten M, Becker J et al (2010) Combined use of plateletrich plasma and autologous bone grafts in the treatment of long bone defects in minipigs. Injury 41(7):71723

    Article  Google Scholar 

  • Hannouche D, Petite H, Sedel L (2001) Current trends in the enhancement of fracture healing. J Bone Joint Surg Br 83(2):157–164

    Article  CAS  PubMed  Google Scholar 

  • Harwood PJ, Giannoudis PV (2005) Application of bone morphogenetic proteins in orthopaedic practice: their efficacy and side effects. Expert Opin Drug Saf 4(1):75–89

    Article  CAS  PubMed  Google Scholar 

  • Hayakawa S, Kanaya T, Tsuru K, Shirosaki Y, Osaka A, Fujii E et al (2013) Heterogeneous structure and in vitro degradation behavior of wet-chemically derived nanocrystalline silicon-containing hydroxyapatite particles. Acta Biomater 9(1):4856–4867

    Article  CAS  PubMed  Google Scholar 

  • Heyde M, Partridge KA, Oreffo RO, Howdle SM, Shakesheff KM, Garnett MC (2007) Gene therapy used for tissue engineering applications. J Pharm Pharmacol 59(3):329–350

    Article  CAS  PubMed  Google Scholar 

  • Hongmin L, Wei Z, Xingrong Y, Jing W, Wenxin G, Jihong C et al (2015) Osteoinductive nanohydroxyapatite bone substitute prepared via in situ hydrothermal transformation of cuttlefish bone. J Biomed Mater Res B Appl Biomater 103(4):816–824

    Article  CAS  PubMed  Google Scholar 

  • Hoyer B, Bernhardt A, Heinemann S, Stachel A, Meyer M, Gelinsky M (2012) Biomimetically mineralized salmon collagen scaffolds for application in bone tissue engineering. Biomacromolecules 13(4):1059–1066

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Yang Z, Zhou Y, Liu Y, Li K, Lu H (2015) Porous biphasic calcium phosphate ceramics coated with nano-hydroxyapatite and seeded with mesenchymal stem cells for reconstruction of radius segmental defects in rabbits. J Mater Sci Mater Med 26(11):257

    Article  CAS  PubMed  Google Scholar 

  • Ivankovic H, Gallego Ferrer G, Tkalcec E, Orlic S, Ivankovic M (2009) Preparation of highly porous hydroxyapatite from cuttlefish bone. J Mater Sci Mater Med 20(5):1039–1046

    Article  CAS  PubMed  Google Scholar 

  • Ivankovic H, Tkalcec E, Orlic S, Ferrer GG, Schauperl Z (2010) Hydroxyapatite formation from cuttlefish bones: kinetics. J Mater Sci Mater Med 21(10):2711–2722

    Article  CAS  PubMed  Google Scholar 

  • Jeong CG, Atala A (2015) 3D printing and biofabrication for load bearing tissue engineering. Adv Exp Med Biol 881:3–14

    Article  CAS  PubMed  Google Scholar 

  • Kim SJ, Shin YW, Yang KH, Kim SB, Yoo MJ, Han SK et al (2009) A multi-center, randomized, clinical study to compare the effect and safety of autologous cultured osteoblast (Ossron) injection to treat fractures. BMC Musculoskelet Disord 10:20

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim BS, Kim JS, Sung HM, You HK, Lee J (2012) Cellular attachment and osteoblast differentiation of mesenchymal stem cells on natural cuttlefish bone. J Biomed Mater Res A 100(7):1673–1679

    Article  CAS  PubMed  Google Scholar 

  • Kim BS, Kang HJ, Lee J (2013) Improvement of the compressive strength of a cuttlefish bone-derived porous hydroxyapatite scaffold via polycaprolactone coating. J Biomed Mater Res B Appl Biomater 101(7):1302–1309

    Article  CAS  PubMed  Google Scholar 

  • Kim BS, Yang SS, Lee J (2014) A polycaprolactone/cuttlefish bone-derived hydroxyapatite composite porous scaffold for bone tissue engineering. J Biomed Mater Res B Appl Biomater 102(5):943–951

    Article  CAS  PubMed  Google Scholar 

  • Kisiel AH, McDuffee LA, Masaoud E, Bailey TR, Esparza Gonzalez BP, Nino-Fong R (2012) Isolation, characterization, and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow, adipose tissue, muscle, and periosteum. Am J Vet Res 73(8):1305–1317

    Article  CAS  PubMed  Google Scholar 

  • Knight MN, Hankenson KD (2013) Mesenchymal stem cells in bone regeneration. Adv Wound Care (New Rochelle) 2(6):306–316

    Article  Google Scholar 

  • Kovach TK, Dighe AS, Lobo PI, Cui Q (2015) Interactions between MSCs and immune cells: implications for bone healing. J Immunol Res 2015:752510

    Article  PubMed  PubMed Central  Google Scholar 

  • Kraus KH (2012) Bone grafts and substitutes. In: Tobias KM, Johnston SA (eds) Veterinary surgery: small animal. Saunders, Canada, pp 676–684

    Google Scholar 

  • Levi B, Longaker MT (2011) Concise review: adipose-derived stromal cells for skeletal regenerative medicine. Stem Cells 29(4):576–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao X, Lu S, Zhou Y, Winter C, Xu W, Li B et al (2011) Bone physiology, biomaterial and the effect of mechanical/physical microenvironment on MSC osteogenesis. Cell Mol Bioeng 4(4):579–590

    Article  CAS  PubMed  Google Scholar 

  • Liao HT, Lee MY, Tsai WW, Wang HC, Lu WC (2013) Osteogenesis of adipose-derived stem cells on polycaprolactone-beta-tricalcium phosphate scaffold fabricated via selective laser sintering and surface coating with collagen type I. J Tissue Eng Regen Med. doi:10.1002/term.1811

  • Liu Y, Yu J, Bai J, Gu JS, Cai B, Zhou X (2013) Effects of cuttlefish bone-bone morphogenetic protein composite material on osteogenesis and revascularization of bone defect in rats. Zhonghua Shao Shang Za Zhi 29(6):54853

    Google Scholar 

  • Ma C, Jing Y, Sun H, Liu X (2015) Hierarchical nanofibrous microspheres with controlled growth factor delivery for bone regeneration. Adv Healthc Mater 4(17):2699–2708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcucio RS, Nauth A, Giannoudis PV, Bahney C, Piuzzi NS, Muschler G et al (2015) Stem cell therapies in orthopaedic trauma. J Orthop Trauma 29(Suppl 12):S24–S27

    Article  PubMed  PubMed Central  Google Scholar 

  • Marsell R, Einhorn TA (2011) The biology of fracture healing. Injury 42(6):551–555

    Article  PubMed  PubMed Central  Google Scholar 

  • McMahon RE, Wang L, Skoracki R, Mathur AB (2013) Development of nanomaterials for bone repair and regeneration. J Biomed Mater Res B Appl Biomater 101(2):387–397

    Article  CAS  PubMed  Google Scholar 

  • Michel J, Penna M, Kochen J, Cheung H (2015) Recent advances in hydroxyapatite scaffolds containing mesenchymal stem cells. Stem Cells Int 2015:305217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Millis DL, Martinez SA (2003) Bone Grafts. In: Douglas S (ed) Textbook of small animal surgery, 3th edn. Saunders, United States of America, pp 1875–1891

    Google Scholar 

  • Miyazaki M, Tsumura H, Wang JC, Alanay A (2009) An update on bone substitutes for spinal fusion. Eur Spine J 18(6):783–799

    Article  PubMed  PubMed Central  Google Scholar 

  • Moeinzadeh S, Jabbari E (2015) Morphogenic peptides in regeneration of load bearing tissues. Adv Exp Med Biol 881:95–110

    Article  CAS  PubMed  Google Scholar 

  • Navarro M, Michiardi M, Castaño O, Planell A (2008) Biomaterials in orthopaedics. J R Soc Interface 5(27):1137–1158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neves PC, Abib Sde C, Neves RF, Pircchio O, Saad KR, Saad PF et al (2013) Effect of hyperbaric oxygen therapy combined with autologous platelet concentrate applied in rabbit fibula fraction healing. Clinics (Sao Paulo) 68(9):1239–1246

    Article  Google Scholar 

  • Ni M, Ratner BD (2003) Nacre surface transformation to hydroxyapatite in a phosphate buffer solution. Biomaterials 24(23):4323–4331

    Article  CAS  PubMed  Google Scholar 

  • Oryan A, Alidadi S, Moshiri A, Maffulli N (2014a) Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res 9:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Oryan A, Alidadi S, Moshiri A, Maffulli N (2014b) Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res 9(1):18

    Article  PubMed  PubMed Central  Google Scholar 

  • Parrilla C, Saulnier N, Bernardini C, Patti R, Tartaglione T, Fetoni AR et al (2011) Undifferentiated human adipose tissue-derived stromal cells induce mandibular bone healing in rats. Arch Otolaryngol Head Neck Surg 137(5):463–470

    Article  PubMed  Google Scholar 

  • Parsons P, Butcher A, Hesselden K, Ellis K, Maughan J, Milner R et al (2008) Platelet-rich concentrate supports human mesenchymal stem cell proliferation, bone morphogenetic protein-2 messenger RNA expression, alkaline phosphatase activity, and bone formation in vitro: a mode of action to enhance bone repair. J Orthop Trauma 22(9):595–604

    Article  PubMed  Google Scholar 

  • Pati F, Datta P, Adhikari B, Dhara S, Ghosh K, Das Mohapatra PK (2012) Collagen scaffolds derived from fresh water fish origin and their biocompatibility. J Biomed Mater Res A 100(4):1068–1079

    Article  CAS  PubMed  Google Scholar 

  • Piermattei DL, Flo G, Decamp CH (2006) Handbook of small animal orthopaedics and fracture repair. 4th ed. United States of America: Saunders. Chapter 3. Bone grafting; p.160

  • Poth N, Seiffart V, Gross G, Menzel H, Dempwolf W (2015) Biodegradable chitosan nanoparticle coatings on titanium for the delivery of BMP-2. Biomol Ther 5(1):3–19

    CAS  Google Scholar 

  • Quan TM, Vu DN, Ha TLB (2014) Decellularization of xenogenic bone grafts for potential use as tissue engineering scaffolds. JJLSR 4(4):38–46

    Google Scholar 

  • Rai R, Raval R, Khandeparker RV, Chidrawar SK, Khan AA, Ganpat MS (2015) Tissue engineering: step ahead in maxillofacial reconstruction. J Int Oral Health 7(9):138–142

    PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Vazquez M, Vega-Ruiz B, Ramos-Zuniga R, Saldana-Koppel DA, Quinones-Olvera LF (2015) Chitosan and its potential use as a scaffold for tissue engineering in regenerative medicine. Biomed Res Int 2015:821279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roffi A, Filardo G, Kon E, Marcacci M (2013) Does PRP enhance bone integration with grafts, graft substitutes, or implants? A systematic review. BMC Musculoskelet Disord 14:330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saadinam F, Fattahian HR, Kajbafzadeh AM (2014) Meniscal lesions and their healing: new aspects. Comp clin pathol

  • Salamanna F, Veronesi F, Maglio M, Della Bella E, Sartori M, Fini M (2015) New and emerging strategies in platelet rich plasma application in musculoskeletal regenerative procedures: general overview on still open questions and outlook. Biomed Res Int 2015:846045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santo VE, Duarte AR, Popa EG, Gomes ME, Mano JF, Reis RL (2012) Enhancement of osteogenic differentiation of human adipose derived stem cells by the controlled release of platelet lysates from hybrid scaffolds produced by supercritical fluid foaming. J Control Release 162(1):19–27

    Article  CAS  PubMed  Google Scholar 

  • Sarkar SK, Lee BT (2015) Hard tissue regeneration using bone substitutes: an update on innovations in materials. Korean J Intern Med 30(3):279–293

    Article  PubMed  PubMed Central  Google Scholar 

  • Shafiei Z, Bigham AS, Dehghani SN, Nezhad ST (2009) Fresh cortical autograft versus fresh cortical allograft effects on experimental bone healing in rabbits: radiological, histopathological and biomechanical evaluation. Cell Tissue Bank 10(1):19–26

    Article  CAS  PubMed  Google Scholar 

  • Silva TH, Silva JM, Marques ALP, Domingues A, Bayon Y, Reis RL (2014) Marine origin collagens and its potential applications. Mar Drugs 12(12):5881–5901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subbiah R, Hwang MP, Van SY, Do SH, Park H, Lee K et al (2015) Osteogenic/angiogenic dual growth factor delivery microcapsules for regeneration of vascularized bone tissue. Adv Healthc Mater 4(13):1982–1992

    Article  CAS  PubMed  Google Scholar 

  • Taniyama T, Masaoka T, Yamada T, Wei X, Yasuda H, Yoshii T et al (2015) Repair of osteochondral defects in a rabbit model using a porous hydroxyapatite collagen composite impregnated with bone morphogenetic protein-2. Artif Organs 39(6):529–535

    Article  CAS  PubMed  Google Scholar 

  • Tkalčec E, Popović J, Orlić S, Milardović S, Ivanković H (2014) Hydrothermal synthesis and thermal evolution of carbonate-fluorhydroxyapatite scaffold from cuttlefish bones. Mater Sci Eng C Mater Biol Appl 42:578–586

    Article  CAS  PubMed  Google Scholar 

  • Venkatesan J, Vinodhini PA, Sudha PN, Kim SK (2014) Chitin and chitosan composites for bone tissue regeneration. Adv Food Nutr Res 73:59–81

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Gu Z, Jamal S, Detamore MS, Berkland C (2013) Hybrid hydroxyapatite nanoparticle colloidal gels are injectable fillers for bone tissue engineering. Tissue Eng A 19(23–24):2586–2593

    Article  CAS  Google Scholar 

  • Xu FT, Li HM, Yin QS, Liang ZJ, Huang MH, Chi GY et al (2015) Effect of activated autologous platelet-rich plasma on proliferation and osteogenic differentiation of human adipose-derived stem cells in vitro. Am J Transl Res 7(2):257–270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xuan Y, Tang H, Wu B, Ding X, Lu Z, Li W et al (2014) A specific groove design for individualized healing in a canine partial sternal defect model by a polycaprolactone/hydroxyapatite scaffold coated with bone marrow stromal cells. J Biomed Mater Res A 102(10):3401–3408

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto K, Igawa K, Sugimoto K, Yoshizawa Y, Yanagiguchi K, Ikeda T et al (2014) Biological safety of fish (tilapia) collagen. Biomed Res Int 2014:630757

    PubMed  PubMed Central  Google Scholar 

  • Yi HC, Tang LH, Zhang XP (2011) Experimental study on bone defect treated by combined autologous bone marrow transplantation, cuttlebone, and sodium hyaluronate. Zhongguo Zhong Xi Yi Jie He Za Zhi 31(8):11226

    Google Scholar 

  • Zeng C, Xiao J, Wu Z, Huang W (2015) Evaluation of three-dimensional printing for internal fixation of unstable pelvic fracture from minimal invasive para-rectus abdominis approach: a preliminary report. Int J Clin Exp Med 8(8):13039–13044

    PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhang Y (2015) Tissue engineering applications of three-dimensional bioprinting. Cell Biochem Biophys

  • Zhao SF, Jiang QH, Peel S, Wang XX, He FM (2013) Effects of magnesium-substituted nanohydroxyapatite coating on implant osseointegration. Clin Oral Implants Res 24(Suppl A100):34–41

    Article  PubMed  Google Scholar 

  • Zhao HY, Wu J, Zhu JJ, Xiao ZC, He CC, Shi HX et al (2015) Research advances in tissue engineering materials for sustained release of growth factors. Biomed Res Int 2015:808202

    PubMed  PubMed Central  Google Scholar 

  • Zigdon-Giladi H, Rudich U, Michaeli Geller G, Evron A (2015) Recent advances in bone regeneration using adult stem cells. World J Stem Cells 7(3):630–640

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Specialized Veterinary Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran

    Hamidreza Fattahian, Kimia Mansouri & Nikta Mansouri

  2. Department of Surgery, Faculty of Specialized Veterinary Sciences, Islamic Azad University Science and Research Branch, Number 5, Attar Street, Vanak Square, Tehran, Iran

    Hamidreza Fattahian

Authors
  1. Hamidreza Fattahian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kimia Mansouri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nikta Mansouri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hamidreza Fattahian.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fattahian, H., Mansouri, K. & Mansouri, N. Biomaterials, substitutes, and tissue engineering in bone repair: current and future concepts. Comp Clin Pathol 28, 879–891 (2019). https://doi.org/10.1007/s00580-017-2507-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-017-2507-2

Keywords

Search

Navigation