Coral Scaffolds in Bone Tissue Engineering and Bone Regeneration

  • Mathieu ManasseroEmail author
  • Adeline Decambron
  • Nane Guillemin
  • Hervé Petite
  • Rena Bizios
  • Véronique Viateau


Coral exoskeleton, which consists of CaCO3 and has an interconnected-pore structure that resembles that of natural human bone, has been used as scaffold material to fill bone defects in both animal models and humans since the early 1970s. This natural material is biocompatible, osteoconductive, and biodegradable. Most importantly, the possibility of seeding coral scaffolds with either stem cells or loading them with growth factors has provided novel alternatives for bone tissue engineering. In vitro studies have demonstrated that (1) seeded cells adhered and proliferated in a time-dependent manner, and (2) loaded growth factors were absorbed on coral scaffold and subsequently released. Moreover, when coral scaffolds containing either cells and/or growth factors were implanted in vivo, a significantly increased amount of newly-formed bone was observed. Most importantly, timely resorption of the scaffold material in vivo was associated with full bone regeneration in a clinically-relevant sheep model of bone defect. Although sometimes inconsistent, such outcomes provided evidence that bone regeneration, which matches, and even supersedes, the efficacy of autologous bone graft, is achievable with coral scaffolds.

Use of coral scaffolds for bone tissue regeneration purposes is thus an appealing strategy for the following reasons: (1) these materials are biocompatible and bioresorbable; (2) have three-dimensional structure and porosity; (3) have material surface chemistry which promotes stem cell differentiation and function of differentiated cells which are pertinent to new tissue formation; and (4) they can be used as carriers for growth factors.


Coral exoskeleton Bone regeneration Bone resorption Animal models Tissue engineering Bone cells Stem cells Growth factors 


  1. Al-Salihi KA (2009) In vitro evaluation of Malaysian natural coral Porites bone graft substitutes (CORAGRAF) for bone tissue engineering: a preliminary study. Braz J Oral Sci 8(4):210–216Google Scholar
  2. Al-Salihi KA, Samsudin AR (2004) Bone marrow mesenchymal stem cells differentiation and proliferation on the surface of coral implant. Med J Malaysia 59(Suppl B):45–46PubMedGoogle Scholar
  3. Amini AR, Laurencin CT, Nukavarapu SP (2012) Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng 40(5):363–408PubMedPubMedCentralCrossRefGoogle Scholar
  4. Arnaud E, Morieux C, Wybier M, de Vernejoul MC (1994) Potentiation of transforming growth factor (TGF-beta 1) by natural coral and fibrin in a rabbit cranioplasty model. Calcif Tissue Int 54(6):493–498PubMedCrossRefGoogle Scholar
  5. Arnaud E, Molina F, Mendoza M, Fuente del Campo A, Ortiz-Monasterio F (1998) Bone substitute with growth factor. Preliminary clinical cases for cranio– and maxillo-facial indications. Ann Chir Plast Esthet 43(1):40–50PubMedGoogle Scholar
  6. Arnaud E, De Pollak C, Meunier A, Sedel L, Damien C, Petite H (1999) Osteogenesis with coral is increased by BMP and BMC in a rat cranioplasty. Biomaterials 20(20):1909–1918PubMedCrossRefGoogle Scholar
  7. Aryal R, Chen XP, Fang C, Hu YC (2014) Bone morphogenetic protein-2 and vascular endothelial growth factor in bone tissue regeneration: new insight and perspectives. Orthop Surg 6(3):171–178PubMedCrossRefGoogle Scholar
  8. Becquart P, Cambon-Binder A, Monfoulet LE, Bourguignon M, Vandamme K, Bensidhoum M, Petite H, Logeart-Avramoglou D (2012) Ischemia is the prime but not the only cause of human multipotent stromal cell death in tissue-engineered constructs in vivo. Tissue Eng Part A 18(19–20):2084–2094PubMedCrossRefGoogle Scholar
  9. Bensaid W, Oudina K, Viateau V, Potier E, Bousson V, Blanchat C, Sedel L, Guillemin G, Petite H (2005) De novo reconstruction of functional bone by tissue engineering in the metatarsal sheep model. Tissue Eng 11(5–6):814–824PubMedCrossRefGoogle Scholar
  10. Blokhuis TJ, Termaat MF, den Boer FC, Patka P, Bakker FC, Haarman HJ (2000) Properties of calcium phosphate ceramics in relation to their in vivo behavior. J Trauma 48(1):179–186PubMedCrossRefGoogle Scholar
  11. Boden SD, Schimandle JH, Hutton WC (1995a) 1995 Volvo award in basic sciences. The use of an osteoinductive growth factor for lumbar spinal fusion. Part II: study of dose, carrier, and species. Spine (Phila Pa 1976) 20(24):2633–2644CrossRefGoogle Scholar
  12. Boden SD, Schimandle JH, Hutton WC, Chen MI (1995b) 1995 Volvo Award in basic sciences. The use of an osteoinductive growth factor for lumbar spinal fusion. Part I: Biol Spinal Fus Spine (Phila Pa 1976) 20(24):2626–2632Google Scholar
  13. Boden SD, Schimandle JH, Hutton WC, Damien CJ, Benedict JJ, Baranowski C, Collier S (1997) In vivo evaluation of a resorbable osteoinductive composite as a graft substitute for lumbar spinal fusion. J Spinal Disord 10(1):1–11PubMedCrossRefGoogle Scholar
  14. Boden SD, Martin GJ Jr, Morone M, Ugbo JL, Titus L, Hutton WC (1999) The use of coralline hydroxyapatite with bone marrow, autogenous bone graft, or osteoinductive bone protein extract for posterolateral lumbar spine fusion. Spine (Phila Pa 1976) 24(4):320–327CrossRefGoogle Scholar
  15. Boerckel JD, Kolambkar YM, Dupont KM, Uhrig BA, Phelps EA, Stevens HY, Garcia AJ, Guldberg RE (2011) Effects of protein dose and delivery system on BMP-mediated bone regeneration. Biomaterials 32(22):5241–5251PubMedPubMedCentralCrossRefGoogle Scholar
  16. Braye F, Irigaray JL, Jallot E, Oudadesse H, Weber G, Deschamps N, Deschamps C, Frayssinet P, Tourenne P, Tixier H, Terver S, Lefaivre J, Amirabadi A (1996) Resorption kinetics of osseous substitute: natural coral and synthetic hydroxyapatite. Biomaterials 17(13):1345–1350PubMedCrossRefGoogle Scholar
  17. Bruder SP, Kraus KH, Goldberg VM, Kadiyala S (1998) The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am 80(7):985–996PubMedGoogle Scholar
  18. Bucholz RW, Carlton A, Holmes R (1989) Interporous hydroxyapatite as a bone graft substitute in tibial plateau fractures. Clin Orthop Relat Res 240:53–62PubMedGoogle Scholar
  19. Burastero G, Scarfi S, Ferraris C, Fresia C, Sessarego N, Fruscione F, Monetti F, Scarfo F, Schupbach P, Podesta M, Grappiolo G, Zocchi E (2010) The association of human mesenchymal stem cells with BMP-7 improves bone regeneration of critical-size segmental bone defects in athymic rats. Bone 47(1):117–126PubMedCrossRefGoogle Scholar
  20. Chatzinikolaidou M, Rekstyte S, Danilevicius P, Pontikoglou C, Papadaki H, Farsari M, Vamvakaki M (2015) Adhesion and growth of human bone marrow mesenchymal stem cells on precise-geometry 3D organic-inorganic composite scaffolds for bone repair. Mater Sci Eng C Mater Biol Appl 48:301–309PubMedCrossRefGoogle Scholar
  21. Clarke SA, Walsh P, Maggs CA, Buchanan F (2011) Designs from the deep: marine organisms for bone tissue engineering. Biotechnol Adv 29(6):610–617PubMedCrossRefGoogle Scholar
  22. Cook EA, Cook JJ (2009) Bone graft substitutes and allografts for reconstruction of the foot and ankle. Clin Podiatr Med Surg 26(4):589–605PubMedCrossRefGoogle Scholar
  23. Coughlin MJ, Grimes JS, Kennedy MP (2006) Coralline hydroxyapatite bone graft substitute in hindfoot surgery. Foot Ankle Int 27(1):19–22PubMedGoogle Scholar
  24. Cukierman E, Pankov R, Stevens DR, Yamada KM (2001) Taking cell-matrix adhesions to the third dimension. Science 294(5547):1708–1712PubMedCrossRefGoogle Scholar
  25. Cunin G, Boissonnet H, Petite H, Blanchat C, Guillemin G (2000) Experimental vertebroplasty using osteoconductive granular material. Spine (Phila Pa 1976) 25(9):1070–1076CrossRefGoogle Scholar
  26. Damien CJ, Christel PS, Benedict JJ, Patat JL, Guillemin G (1993) A composite of natural coral, collagen, bone protein and basic fibroblast growth factor tested in a rat subcutaneous model. Ann Chir Gynaecol Suppl 207:117–128PubMedGoogle Scholar
  27. Damien CJ, Ricci JL, Christel P, Alexander H, Patat JL (1994) Formation of a calcium phosphate-rich layer on absorbable calcium carbonate bone graft substitutes. Calcif Tissue Int 55(2):151–158PubMedCrossRefGoogle Scholar
  28. David B, Bonnefont-Rousselot D, Oudina K, Degat MC, Deschepper M, Viateau V, Bensidhoum M, Oddou C, Petite H (2011) A perfusion bioreactor for engineering bone constructs: an in vitro and in vivo study. Tissue Eng Part C Methods 17(5):505–516PubMedCrossRefGoogle Scholar
  29. de la Caffiniere JY, Viehweger E, Worcel A (1998) Long-term radiologic evolution of coral implanted in cancellous bone of the lower limb. Madreporic coral versus coral hydroxyapatite. Rev Chir Orthop Reparatrice Appar Mot 84(6):501–507PubMedGoogle Scholar
  30. De Long WG Jr, Einhorn TA, Koval K, McKee M, Smith W, Sanders R, Watson T (2007) Bone grafts and bone graft substitutes in orthopaedic trauma surgery. A critical analysis. J Bone Joint Surg Am 89(3):649–658PubMedCrossRefGoogle Scholar
  31. de Peretti F, Trojani C, Cambas PM, Loubiere R, Argenson C (1996) Coral as support of traumatic articular compression. A prospective study of 23 cases involving the lower limb. Rev Chir Orthop Reparatrice Appar Mot 82(3):234–240PubMedGoogle Scholar
  32. Demers C, Hamdy CR, Corsi K, Chellat F, Tabrizian M, Yahia L (2002a) Natural coral exoskeleton as a bone graft substitute: a review. Biomed Mater Eng 12(1):15–35PubMedGoogle Scholar
  33. Demers CN, Tabrizian M, Petit A, Hamdy RC, Yahia L (2002b) Effect of experimental parameters on the in vitro release kinetics of transforming growth factor beta1 from coral particles. J Biomed Mater Res 59(3):403–410PubMedCrossRefGoogle Scholar
  34. Fricain JC, Roudier M, Rouais F, Basse-Cathalinat B, Dupuy B (1996) Influence of the structure of three corals on their resorption kinetics. J Periodontal Res 31(7):463–469PubMedCrossRefGoogle Scholar
  35. Fricain JC, Bareille R, Rouais F, Basse-Cathalinat B, Dupuy B (1998) “In vitro” dissolution of coral in peritoneal or fibroblast cell cultures. J Dent Res 77(2):406–411PubMedCrossRefGoogle Scholar
  36. Fu K, Xu Q, Czernuszka J, Triffitt JT, Xia Z (2013) Characterization of a biodegradable coralline hydroxyapatite/calcium carbonate composite and its clinical implementation. Biomed Mater 8(6):065007PubMedCrossRefGoogle Scholar
  37. Fuller DA, Stevenson S, Emery SE (1996) The effects of internal fixation on calcium carbonate. Ceramic anterior spinal fusion in dogs. Spine (Phila Pa 1976) 21(18):2131–2136CrossRefGoogle Scholar
  38. Gao TJ, Lindholm TS, Kommonen B, Ragni P, Paronzini A, Lindholm TC, Jalovaara P, Urist MR (1997) The use of a coral composite implant containing bone morphogenetic protein to repair a segmental tibial defect in sheep. Int Orthop 21(3):194–200PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gardiner A, Weitzel PP (2007) Bone graft substitutes in sports medicine. Sports Med Arthrosc Rev 15(3):158–166CrossRefGoogle Scholar
  40. Garrido CA, Lobo SE, Turibio FM, Legeros RZ (2011) Biphasic calcium phosphate bioceramics for orthopaedic reconstructions: clinical outcomes. Int J Biomater 2011:129727PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gay CV, Mueller WJ (1974) Carbonic anhydrase and osteoclasts: localization by labeled inhibitor autoradiography. Science 183(4123):432–434PubMedCrossRefGoogle Scholar
  42. Geiger F, Lorenz H, Xu W, Szalay K, Kasten P, Claes L, Augat P, Richter W (2007) VEGF producing bone marrow stromal cells (BMSC) enhance vascularization and resorption of a natural coral bone substitute. Bone 41(4):516–522PubMedCrossRefGoogle Scholar
  43. Giannoudis PV, Dinopoulos H, Tsiridis E (2005) Bone substitutes: an update. Injury 36(Suppl 3):S20–S27PubMedCrossRefGoogle Scholar
  44. Green DW, Padula MP, Santos J, Chou J, Milthorpe B, Ben-Nissan B (2013) A therapeutic potential for marine skeletal proteins in bone regeneration. Mar Drugs 11(4):1203–1220PubMedPubMedCentralCrossRefGoogle Scholar
  45. Guillemin G, Patat JL, Fournie J, Chetail M (1987) The use of coral as a bone graft substitute. J Biomed Mater Res 21(5):557–567PubMedCrossRefGoogle Scholar
  46. Guillemin G, Meunier A, Dallant P, Christel P, Pouliquen JC, Sedel L (1989) Comparison of coral resorption and bone apposition with two natural corals of different porosities. J Biomed Mater Res 23(7):765–779PubMedCrossRefGoogle Scholar
  47. Guillemin G, Hunter SJ, Gay CV (1995) Resorption of natural calcium carbonate by avian osteoclast in vitro. Cells Mater 5(2):157–165Google Scholar
  48. Hemond EM, Kaluziak ST, Vollmer SV (2014) The genetics of colony form and function in Caribbean Acropora corals. BMC Genomics 15:1133PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hing KA, Wilson LF, Buckland T (2007) Comparative performance of three ceramic bone graft substitutes. Spine J 7(4):475–490PubMedCrossRefGoogle Scholar
  50. Hoppe A, Guldal NS, Boccaccini AR (2011) A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32(11):2757–2774PubMedCrossRefGoogle Scholar
  51. Hou R, Chen F, Yang Y, Cheng X, Gao Z, Yang HO, Wu W, Mao T (2007) Comparative study between coral-mesenchymal stem cells-rhBMP-2 composite and auto-bone-graft in rabbit critical-sized cranial defect model. J Biomed Mater Res A 80(1):85–93PubMedCrossRefGoogle Scholar
  52. Huang RL, Yuan Y, Tu J, Zou GM, Li Q (2014) Exaggerated inflammatory environment decreases BMP-2/ACS-induced ectopic bone mass in a rat model: implications for clinical use of BMP-2. Osteoarthr Cartil/OARS Osteoarthr Res Soc 22(8):1186–1196CrossRefGoogle Scholar
  53. Irigaray JL, Oudadesse H, Blondiaux G, Collangettes D (1993a) Kinetics of the diffusion of some elements evaluated by neutron activation in a coral implanted in vivo. J Radioanal Nucl Chem 169:339–346CrossRefGoogle Scholar
  54. Irigaray JL, Oudadesse H, El Fadl H, Sauvage T, Thomas G, Vernay AM (1993b) Effet de la température sur la structure cristalline d’un biocorail. J Therm Anal 39:3–14CrossRefGoogle Scholar
  55. Irigaray JL, Sauvage T, Oudadesse H, El Fadl H, Deschamps C, Lefaivre J, Barlet JP, Terver S, Tixier H (1993c) Study of the mineralization of coral implanted in vivo by radioactive tracers. J Radioanal Nucl Chem 174:93–102CrossRefGoogle Scholar
  56. Jammet P, Souyris F, Baldet P, Bonnel F, Huguet M (1994) The effect of different porosities in coral implants: an experimental study. J Craniomaxillofac Surg 22(2):103–108PubMedCrossRefGoogle Scholar
  57. Karageorgiou V, Kaplan D (2005) Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26(27):5474–5491PubMedCrossRefGoogle Scholar
  58. Kim RY, Oh JH, Lee BS, Seo YK, Hwang SJ, Kim IS (2014) The effect of dose on rhBMP-2 signaling, delivered via collagen sponge, on osteoclast activation and in vivo bone resorption. Biomaterials 35(6):1869–1881PubMedCrossRefGoogle Scholar
  59. Kon E, Muraglia A, Corsi A, Bianco P, Marcacci M, Martin I, Boyde A, Ruspantini I, Chistolini P, Rocca M, Giardino R, Cancedda R, Quarto R (2000) Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. J Biomed Mater Res 49(3):328–337PubMedCrossRefGoogle Scholar
  60. Kuboki Y, Takita H, Kobayashi D, Tsuruga E, Inoue M, Murata M, Nagai N, Dohi Y, Ohgushi H (1998) BMP-induced osteogenesis on the surface of hydroxyapatite with geometrically feasible and nonfeasible structures: topology of osteogenesis. J Biomed Mater Res 39(2):190–199PubMedCrossRefGoogle Scholar
  61. Kuhne JH, Bartl R, Frisch B, Hammer C, Jansson V, Zimmer M (1994) Bone formation in coralline hydroxyapatite. Effects of pore size studied in rabbits. Acta Orthop Scand 65(3):246–252PubMedCrossRefGoogle Scholar
  62. Kujala S, Raatikainen T, Ryhanen J, Kaarela O, Jalovaara P (2002) Composite implant of native bovine bone morphogenetic protein (BMP) and biocoral in the treatment of scaphoid nonunions – a preliminary study. Scand J Surg 91(2):186–190PubMedGoogle Scholar
  63. Kujala S, Raatikainen T, Ryhanen J, Kaarela O, Jalovaara P (2004) Composite implant of native bovine bone morphogenetic protein (BMP), collagen carrier and biocoral in the treatment of resistant ulnar nonunions: report of five preliminary cases. Arch Orthop Trauma Surg 124(1):26–30PubMedCrossRefGoogle Scholar
  64. Le Nihouannen D, Daculsi G, Saffarzadeh A, Gauthier O, Delplace S, Pilet P, Layrolle P (2005) Ectopic bone formation by microporous calcium phosphate ceramic particles in sheep muscles. Bone 36(6):1086–1093PubMedCrossRefGoogle Scholar
  65. LeGeros RZ (2008) Calcium phosphate-based osteoinductive materials. Chem Rev 108(11):4742–4753PubMedCrossRefGoogle Scholar
  66. LeGeros RZ, Orly I, Gregoire M, Kazimiroff J (1991) Comparative properties and in vitro reactions of HA ceramic and coralline HA. Apatite 1:229–233Google Scholar
  67. LeGeros RZ, Daculsi G, LeGeros JP (2008) Bioactive bioceramics. In: Pietrzak WS (ed) Muskuloskeletal tissue regenration: biological materials and methods. Humana Press Inc, New Jersey, pp 153–181CrossRefGoogle Scholar
  68. Li S, De Wijn JR, Li J, Layrolle P, De Groot K (2003) Macroporous biphasic calcium phosphate scaffold with high permeability/porosity ratio. Tissue Eng 9(3):535–548PubMedCrossRefGoogle Scholar
  69. Lieberman JR, Daluiski A, Einhorn TA (2002) The role of growth factors in the repair of bone. Biology and clinical applications. J Bone Joint Surg Am 84-A(6):1032–1044PubMedGoogle Scholar
  70. Logeart-Avramoglou D, Bourguignon M, Oudina K, Ten Dijke P, Petite H (2006) An assay for the determination of biologically active bone morphogenetic proteins using cells transfected with an inhibitor of differentiation promoter-luciferase construct. Anal Biochem 349(1):78–86PubMedCrossRefGoogle Scholar
  71. Loty B, Roux FX, George B, Courpied JP, Postel M (1990) Utilisation du corail en chirurgie osseuse - Résultats après 4 ans d’utilisation. Int Orthop 14:255–259PubMedGoogle Scholar
  72. Louisia S, Stromboni M, Meunier A, Sedel L, Petite H (1999) Coral grafting supplemented with bone marrow. J Bone Joint Surg Br 81(4):719–724PubMedCrossRefGoogle Scholar
  73. Lowery GL, Kulkarni S, Pennisi AE (1999) Use of autologous growth factors in lumbar spinal fusion. Bone 25(2 Suppl):47S–50SPubMedCrossRefGoogle Scholar
  74. Ma Q, Mao T, Liu B (2000a) The experimental study on the activity of rhBMP-2, coral and collagen composites inducing intramuscle bone. Hua xi kou qiang yi xue za zhi: Huaxi kouqiang yixue zazhi: West China J Stomatology 18(2):94–97Google Scholar
  75. Ma Q, Mao T, Liu B, Zhao J, Chen F, Wang H, Zhao M (2000b) Vascular osteomuscular autograft prefabrication using coral, type I collagen and recombinant human bone morphogenetic protein-2. Br J Oral Maxillofac Surg 38(5):561–564PubMedCrossRefGoogle Scholar
  76. Maeno S, Niki Y, Matsumoto H, Morioka H, Yatabe T, Funayama A, Toyama Y, Taguchi T, Tanaka J (2005) The effect of calcium ion concentration on osteoblast viability, proliferation and differentiation in monolayer and 3D culture. Biomaterials 26(23):4847–4855PubMedCrossRefGoogle Scholar
  77. Mainard D, Gouin F, Chauveaux D, Rosset P, Schwartz C (2011) Les substituts de l’os, du cartilage et du ménisque. Romillat, ParisGoogle Scholar
  78. Manassero M, Viateau V, Retortillo J, Deschepper M, Bensidhoum M, Logeart-Avramoglou D, Petite H (2012) In vivo evaluation of human mesenchymal stem cells survival in a large segmental bone defect in mice. In: Orthopaedic Research Society Meeting, San Francisco, 4–7 February 2012Google Scholar
  79. Manassero M, Viateau V, Deschepper M, Oudina K, Logeart-Avramoglou D, Petite H, Bensidhoum M (2013) Bone regeneration in sheep using acropora coral, a natural resorbable scaffold, and autologous mesenchymal stem cells. Tissue Eng Part A 19(13–14):1554–1563PubMedCrossRefGoogle Scholar
  80. Mangano C, Paino F, D’Aquino R, De Rosa A, Iezzi G, Piattelli A, Laino L, Mitsiadis T, Desiderio V, Mangano F, Papaccio G, Tirino V et al (2011) Human dental pulp stem cells hook into biocoral scaffold forming an engineered biocomplex. PLoS One 6(4):e18721PubMedPubMedCentralCrossRefGoogle Scholar
  81. Marcacci M, Kon E, Zaffagnini S, Giardino R, Rocca M, Corsi A, Benvenuti A, Bianco P, Quarto R, Martin I, Muraglia A, Cancedda R (1999) Reconstruction of extensive long-bone defects in sheep using porous hydroxyapatite sponges. Calcif Tissue Int 64(1):83–90PubMedCrossRefGoogle Scholar
  82. Marchac D, Sandor G (1994) Use of coral granules in the craniofacial skeleton. J Craniofac Surg 5(4):213–217PubMedCrossRefGoogle Scholar
  83. Marie PJ (2010) The calcium-sensing receptor in bone cells: a potential therapeutic target in osteoporosis. Bone 46(3):571–576PubMedCrossRefGoogle Scholar
  84. Molly L, Vandromme H, Quirynen M, Schepers E, Adams JL, van Steenberghe D (2008) Bone formation following implantation of bone biomaterials into extraction sites. J Periodontol 79(6):1108–1115PubMedCrossRefGoogle Scholar
  85. Murugan R, Ramakrishna S (2004) Coupling of therapeutic molecules onto surface modified coralline hydroxyapatite. Biomaterials 25(15):3073–3080PubMedCrossRefGoogle Scholar
  86. Mygind T, Stiehler M, Baatrup A, Li H, Zou X, Flyvbjerg A, Kassem M, Bunger C (2007) Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials 28(6):1036–1047PubMedCrossRefGoogle Scholar
  87. Nandi SK, Kundu B, Mukherjee J, Mahato A, Datta S, Balla VK (2015) Converted marine coral hydroxyapatite implants with growth factors: in vivo bone regeneration. Mater Sci Eng C Mater Biol Appl 49:816–823PubMedCrossRefGoogle Scholar
  88. Papa F, Cortese A, Sagliocco R, Farella M, Banzi C, Maltarello MC, Pellegrini C, D’Agostino E, Aimola P, Claudio PP (2009) Outcome of 47 consecutive sinus lift operations using aragonitic calcium carbonate associated with autologous platelet-rich plasma: clinical, histologic, and histomorphometrical evaluations. J Craniofac Surg 20(6):2067–2074PubMedCrossRefGoogle Scholar
  89. Papacharalambous SK, Anastasoff KI (1993) Natural coral skeleton used as onlay graft for contour augmentation of the face. A preliminary report. Int J Oral Maxillofac Surg 22(5):260–264PubMedCrossRefGoogle Scholar
  90. Parizi AM, Oryan A, Shafiei-Sarvestani Z, Bigham AS (2012) Human platelet rich plasma plus Persian Gulf coral effects on experimental bone healing in rabbit model: radiological, histological, macroscopical and biomechanical evaluation. J Mater Sci Mater Med 23(2):473–483PubMedCrossRefGoogle Scholar
  91. Patat JL, Pouliquen JC, Guillemin G (1992) Natural coral used as a substitute for bone graft. Its role in the economics of blood in spinal surgery. Acta Orthop Belg 58(Suppl 1):115–121PubMedGoogle Scholar
  92. Patel A, Honnart F, Guillemin G, Patat JL (1980) Use of madreporaria coral skeletal fragments in orthopedic and reconstructive surgery: experimental studies and human clinical application (author’s transl). Chirurgie 106(3):199–205PubMedGoogle Scholar
  93. Perry CR (1999) Bone repair techniques, bone graft, and bone graft substitutes. Clin Orthop Relat Res 360:71–86PubMedCrossRefGoogle Scholar
  94. Petite H, Viateau V, Bensaid W, Meunier A, de Pollak C, Bourguignon M, Oudina K, Sedel L, Guillemin G (2000) Tissue-engineered bone regeneration. Nat Biotechnol 18(9):959–963PubMedCrossRefGoogle Scholar
  95. Polo-Corrales L, Latorre-Esteves M, Ramirez-Vick JE (2014) Scaffold design for bone regeneration. J Nanosci Nanotechnol 14(1):15–56PubMedPubMedCentralCrossRefGoogle Scholar
  96. Pouliquen JC, Noat M, Verneret C, Guillemin G, Patat JL (1989) Coral substituted for bone grafting in posterior vertebral arthrodesis in children. Initial results. Rev Chir Orthop Reparatrice Appar Mot 75(6):360–369PubMedGoogle Scholar
  97. Preaemer A, Furnes S, Rice D (1992) Musculoskeletal conditions in the United States. American Academy of Orthopedic Surgeons, RosemontGoogle Scholar
  98. Puvaneswary S, Balaji Raghavendran HR, Ibrahim NS, Murali MR, Merican AM, Kamarul T (2013) A comparative study on morphochemical properties and osteogenic cell differentiation within bone graft and coral graft culture systems. Int J Med Sci 10(12):1608–1614PubMedPubMedCentralCrossRefGoogle Scholar
  99. Ramos-Silva P, Kaandorp J, Herbst F, Plasseraud L, Alcaraz G, Stern C, Corneillat M, Guichard N, Durlet C, Luquet G, Marin F (2014) The skeleton of the staghorn coral Acropora millepora: molecular and structural characterization. PLoS One 9(6):e97454PubMedPubMedCentralCrossRefGoogle Scholar
  100. Ramzi N, Ribeiro-Vaz G, Fomekong E, Lecouvet FE, Raftopoulos C (2008) Long term outcome of anterior cervical discectomy and fusion using coral grafts. Acta Neurochir 150(12):1249–1256; discussion 1256PubMedCrossRefGoogle Scholar
  101. Rey C, Combes C, Drouet C, Glimcher MJ (2009) Bone mineral: update on chemical composition and structure. Osteoporos Int 20(6):1013–1021PubMedPubMedCentralCrossRefGoogle Scholar
  102. Richard M, Aguado E, Cottrel M, Daculsi G (1998) Ultrastructural and electron diffraction of the bone-ceramic interfacial zone in coral and biphasic CaP implants. Calcif Tissue Int 62(5):437–442PubMedCrossRefGoogle Scholar
  103. Roudier M, Bouchon C, Rouvillain JL, Amedee J, Bareille R, Rouais F, Fricain JC, Dupuy B, Kien P, Jeandot R et al (1995) The resorption of bone-implanted corals varies with porosity but also with the host reaction. J Biomed Mater Res 29(8):909–915PubMedCrossRefGoogle Scholar
  104. Roux FX, Brasnu D, Loty B, George B, Guillemin G (1988a) Madreporic coral: a new bone graft substitute for cranial surgery. J Neurosurg 69(4):510–513PubMedCrossRefGoogle Scholar
  105. Roux FX, Loty B, Brasnu D, Guillemin G (1988b) Reconstruction of the anterior face of the base of the skull using coral grafts. Neurochirurgie 34(2):110–112PubMedGoogle Scholar
  106. Roux FX, Brasnu D, Menard M, Devaux B, Nohra G, Loty B (1995) Madreporic coral for cranial base reconstruction. 8 years experience. Acta Neurochir 133(3–4):201–205PubMedCrossRefGoogle Scholar
  107. Roy DM, Linnehan SK (1974) Hydroxyapatite formed from coral skeletal carbonate by hydrothermal exchange. Nature 247(5438):220–222PubMedCrossRefGoogle Scholar
  108. Schliephake H, Kage T (2001) Enhancement of bone regeneration using resorbable ceramics and a polymer-ceramic composite material. J Biomed Mater Res 56(1):128–136PubMedCrossRefGoogle Scholar
  109. Sciadini MF, Johnson KD (2000) Evaluation of recombinant human bone morphogenetic protein-2 as a bone-graft substitute in a canine segmental defect model. J Orthop Res 18(2):289–302PubMedCrossRefGoogle Scholar
  110. Sciadini MF, Dawson JM, Johnson KD (1997a) Bovine-derived bone protein as a bone graft substitute in a canine segmental defect model. J Orthop Trauma 11(7):496–508PubMedCrossRefGoogle Scholar
  111. Sciadini MF, Dawson JM, Johnson KD (1997b) Evaluation of bovine-derived bone protein with a natural coral carrier as a bone-graft substitute in a canine segmental defect model. J Orthop Res 15(6):844–857PubMedCrossRefGoogle Scholar
  112. Sen MK, Miclau T (2007) Autologous iliac crest bone graft: should it still be the gold standard for treating nonunions? Injury 38(Suppl 1):S75–S80PubMedCrossRefGoogle Scholar
  113. Shafiei-Sarvestani Z, Oryan A, Bigham AS, Meimandi-Parizi A (2012) The effect of hydroxyapatite-hPRP, and coral-hPRP on bone healing in rabbits: radiological, biomechanical, macroscopic and histopathologic evaluation. Int J Surg 10(2):96–101PubMedCrossRefGoogle Scholar
  114. Shahgaldi BF (1998) Coral graft restoration of osteochondral defects. Biomaterials 19(1–3):205–213PubMedCrossRefGoogle Scholar
  115. Shor L, Guceri S, Wen X, Gandhi M, Sun W (2007) Fabrication of three-dimensional polycaprolactone/hydroxyapatite tissue scaffolds and osteoblast-scaffold interactions in vitro. Biomaterials 28(35):5291–5297PubMedCrossRefGoogle Scholar
  116. Shors EC (1999) Coralline bone graft substitutes. Orthop Clin North Am 30(4):599–613PubMedCrossRefGoogle Scholar
  117. Sivakumar M, Kumar TS, Shantha KL, Rao KP (1996) Development of hydroxyapatite derived from Indian coral. Biomaterials 17(17):1709–1714PubMedCrossRefGoogle Scholar
  118. Soffer E, Ouhayoun JP, Meunier A, Anagnostou F (2006) Effects of autologous platelet lysates on ceramic particle resorption and new bone formation in critical size defects: the role of anatomical sites. J Biomed Mater Res B Appl Biomater 79(1):86–94PubMedCrossRefGoogle Scholar
  119. Soost F, Reisshauer B, Herrmann A, Neumann HJ (1998) Natural coral calcium carbonate as alternative substitute in bone defects of the skull. Mund-, Kiefer– und Gesichtschirurgie: MKG 2(2):96–100PubMedCrossRefGoogle Scholar
  120. Thalgott JS, Giuffre JM, Fritts K, Timlin M, Klezl Z (2001) Instrumented posterolateral lumbar fusion using coralline hydroxyapatite with or without demineralized bone matrix, as an adjunct to autologous bone. Spine J 1(2):131–137PubMedCrossRefGoogle Scholar
  121. Tho KS, Krishnamoorthy S (1996) Use of coral grafts in anterior interbody fusion of the rabbit spine. Ann Acad Med Singapore 25(6):824–827PubMedGoogle Scholar
  122. Toombs JP, Wallace LJ, Bjorling DE, Rowland GN (1985) Evaluation of Key’s hypothesis in the feline tibia: an experimental model for augmented bone healing studies. Am J Vet Res 46(2):513–518PubMedGoogle Scholar
  123. Tran CT, Gargiulo C, Thao HD, Tuan HM, Filgueira L, Michael Strong D (2011) Culture and differentiation of osteoblasts on coral scaffold from human bone marrow mesenchymal stem cells. Cell Tissue Bank 12(4):247–261PubMedCrossRefGoogle Scholar
  124. Tuominen T, Jamsa T, Tuukkanen J, Nieminen P, Lindholm TC, Lindholm TS, Jalovaara P (2000) Native bovine bone morphogenetic protein improves the potential of biocoral to heal segmental canine ulnar defects. Int Orthop 24(5):289–294PubMedPubMedCentralCrossRefGoogle Scholar
  125. Valerio P, Pereira MM, Goes AM, Leite MF (2009) Effects of extracellular calcium concentration on the glutamate release by bioactive glass (BG60S) preincubated osteoblasts. Biomed Mater 4(4):045011PubMedCrossRefGoogle Scholar
  126. Vecchio KS, Zhang X, Massie JB, Wang M, Kim CW (2007) Conversion of sea urchin spines to Mg-substituted tricalcium phosphate for bone implants. Acta Biomater 3(5):785–793PubMedCrossRefGoogle Scholar
  127. Velich N, Nemeth Z, Toth C, Szabo G (2004) Long-term results with different bone substitutes used for sinus floor elevation. J Craniofac Surg 15(1):38–41PubMedCrossRefGoogle Scholar
  128. Viateau V, Guillemin G, Yang YC, Bensaid W, Reviron T, Oudina K, Meunier A, Sedel L, Petite H (2004) A technique for creating critical-size defects in the metatarsus of sheep for use in investigation of healing of long-bone defects. Am J Vet Res 65(12):1653–1657PubMedCrossRefGoogle Scholar
  129. Viateau V, Guillemin G, Calando Y, Logeart D, Oudina K, Sedel L, Hannouche D, Bousson V, Petite H (2006) Induction of a barrier membrane to facilitate reconstruction of massive segmental diaphyseal bone defects: an ovine model. Vet Surg 35(5):445–452PubMedCrossRefGoogle Scholar
  130. Viateau V, Guillemin G, Bousson V, Oudina K, Hannouche D, Sedel L, Logeart-Avramoglou D, Petite H (2007) Long-bone critical-size defects treated with tissue-engineered grafts: a study on sheep. J Orthop Res 25(6):741–749PubMedCrossRefGoogle Scholar
  131. Viateau V, Bensidhoum M, Guillemin G, Petite H, Hannouche D, Anagnostou F, Pelissier P (2010) Use of the induced membrane technique for bone tissue engineering purposes: animal studies. Orthop Clin North Am 41(1):49–56PubMedCrossRefGoogle Scholar
  132. Viateau V, Manassero M, Sensebe L, Langonne A, Marchat D, Logeart-Avramoglou D, Petite H, Bensidhoum M (2016) Comparative study of the osteogenic ability of four different ceramic constructs in an ectopic large animal model. J Tissue Eng Regen Med 10(3):E177–187Google Scholar
  133. Volpi N (1999) Adsorption of glycosaminoglycans onto coral – a new possible implant biomaterials for regeneration therapy. Biomaterials 20(15):1359–1363PubMedCrossRefGoogle Scholar
  134. Volpi N (2002) Influence of charge density, sulfate group position and molecular mass on adsorption of chondroitin sulfate onto coral. Biomaterials 23(14):3015–3022PubMedCrossRefGoogle Scholar
  135. von Doernberg MC, von Rechenberg B, Bohner M, Grunenfelder S, van Lenthe GH, Muller R, Gasser B, Mathys R, Baroud G, Auer J (2006) In vivo behavior of calcium phosphate scaffolds with four different pore sizes. Biomaterials 27(30):5186–5198CrossRefGoogle Scholar
  136. Vuola J, Taurio R, Goransson H, Asko-Seljavaara S (1998) Compressive strength of calcium carbonate and hydroxyapatite implants after bone-marrow-induced osteogenesis. Biomaterials 19(1–3):223–227PubMedCrossRefGoogle Scholar
  137. Vuola J, Bohling T, Kinnunen J, Hirvensalo E, Asko-Seljavaara S (2000) Natural coral as bone-defect-filling material. J Biomed Mater Res 51(1):117–122PubMedCrossRefGoogle Scholar
  138. Ward WG, Goldner RD, Nunley JA (1990) Reconstruction of tibial bone defects in tibial nonunion. Microsurgery 11(1):63–73PubMedCrossRefGoogle Scholar
  139. White E, Shors EC (1986) Biomaterial aspects of Interpore-200 porous hydroxyapatite. Dent Clin N Am 30(1):49–67PubMedGoogle Scholar
  140. White RA, Weber JN, White EW (1972) Replamineform: a new process for preparing porous ceramic, metal, and polymer prosthetic materials. Science 176(4037):922–924PubMedCrossRefGoogle Scholar
  141. Wu YC, Lee TM, Chiu KH, Shaw SY, Yang CY (2009) A comparative study of the physical and mechanical properties of three natural corals based on the criteria for bone-tissue engineering scaffolds. J Mater Sci Mater Med 20(6):1273–1280PubMedCrossRefGoogle Scholar
  142. Yu X, Suarez-Gonzalez D, Khalil AS, Murphy WL (2015) How does the pathophysiological context influence delivery of bone growth factors? Adv Drug Del Rev 84:68–84Google Scholar
  143. Yuan H, Fernandes H, Habibovic P, de Boer J, Barradas AM, de Ruiter A, Walsh WR, van Blitterswijk CA, de Bruijn JD (2010) Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci U S A 107(31):13614–13619PubMedPubMedCentralCrossRefGoogle Scholar
  144. Zaidi M, Moonga BS, Huang CL (2004) Calcium sensing and cell signaling processes in the local regulation of osteoclastic bone resorption. Biol Rev Camb Philos Soc 79(1):79–100PubMedCrossRefGoogle Scholar
  145. Zara JN, Siu RK, Zhang X, Shen J, Ngo R, Lee M, Li W, Chiang M, Chung J, Kwak J, Wu BM, Ting K, Soo C (2011) High doses of bone morphogenetic protein 2 induce structurally abnormal bone and inflammation in vivo. Tissue Eng Part A 17(9–10):1389–1399PubMedPubMedCentralCrossRefGoogle Scholar
  146. Zeng R, Ren C, Li C (1997) Experimental study on bone formation in a denser coral used for repairing cortical defects in dogs. Zhonghua kou qiang yi xue za zhi = Zhonghua kouqiang yixue zazhi = Chinese J Stomatology 32(1):16–18Google Scholar
  147. Zhang S, Mao T, Wang H (1998) An experimental study on the bone repairing ability of recombinant human bone morphogenetic protein-2-coral composited artificial bone. Zhonghua kou qiang yi xue za zhi = Zhonghua kouqiang yixue zazhi = Chinese J Stomatology 33(1):13–14Google Scholar
  148. Zhang Y, Wang Y, Shi B, Cheng X (2007) A platelet-derived growth factor releasing chitosan/coral composite scaffold for periodontal tissue engineering. Biomaterials 28(8):1515–1522PubMedCrossRefGoogle Scholar
  149. Zhang S, Mao T, Chen F (2011) Influence of platelet-rich plasma on ectopic bone formation of bone marrow stromal cells in porous coral. Int J Oral Maxillofac Surg 40(9):961–965PubMedCrossRefGoogle Scholar
  150. Zhang Q, Zhang Y, Chen W, Zhang B, Wang S (2013) Long-term controlled release of I-tagged BMP-2 by mesoporous bioactive glass with ordered nanopores. Exp Ther Med 6(6):1443–1448PubMedPubMedCentralGoogle Scholar
  151. Zhu H, Schulz J, Schliephake H (2010a) Human bone marrow stroma stem cell distribution in calcium carbonate scaffolds using two different seeding methods. Clin Oral Implants Res 21(2):182–188PubMedCrossRefGoogle Scholar
  152. Zhu L, Chuanchang D, Wei L, Yilin C, Jiasheng D (2010b) Enhanced healing of goat femur-defect using BMP7 gene-modified BMSCs and load-bearing tissue-engineered bone. J Orthop Res 28(3):412–418PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Mathieu Manassero
    • 1
    • 2
    Email author
  • Adeline Decambron
    • 1
    • 2
  • Nane Guillemin
    • 1
  • Hervé Petite
    • 1
  • Rena Bizios
    • 3
  • Véronique Viateau
    • 1
    • 2
  1. 1.Laboratoire de Bioingénierie et Bioimagerie Ostéo-Articulaires (B2OA – UMR CNRS 7052), Faculté de medicine de Paris LariboisièreUniversité Paris DiderotParisFrance
  2. 2.Service de chirurgieUniversité Paris-Est, Ecole Nationale Vétérinaire d’AlfortMaisons-AlfortFrance
  3. 3.Department of Biomedical EngineeringThe University of Texas at San AntonioSan AntonioUSA

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