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Calcified Algae for Tissue Engineering

  • Gina Choi
  • Louise A. EvansEmail author
Chapter
Part of the Springer Series in Biomaterials Science and Engineering book series (SSBSE, volume 14)

Abstract

Extensive research has been conducted on hydroxyapatite as a bone tissue engineering scaffold due to its low toxicity, biocompatibility, bioactivity and chemical similarity to bone. Hard coral species as well as red and green calcified marine algae have naturally porous skeletons that resemble cancellous bone. Under controlled hydrothermal conditions, these materials can be converted to hydroxyapatite with their porosity and interconnectivity preserved. The availability of hard coral species is limited due to the damage caused by harvesting procedures and decline in coral reefs. As an alternative, hydroxyapatite can be produced from red and green algae species. Currently, red algae derived Algipore® grafts are commercially available for maxillary sinus bone augmentation. Long term clinical studies have confirmed the bone regenerating capabilities of Algipore® when mixed with autologous bone debris and blood, but research on the use of Algipore® tissue scaffolds seeded with mesenchymal stem cells is still ongoing. This chapter reviews the synthesis of hydroxyapatite derived from marine algae and gives background to clinical studies as well as the characterisation techniques used to analyse these materials.

Keywords

Hydroxyapatite Aragonite Calcified algae Scanning electron microscopy X-ray diffraction analysis Fourier-transform infrared spectroscopy Bone regeneration Hydrothermal conversion Mesenchymal stem cells Algae-derived hydroxyapatite Bone tissue engineering 

Notes

Acknowledgements

The authors with to thank Professor Besim Ben-Nissan of the University of Technology Sydney and Professor Sophie Cazalbou of the University of Toulouse, France, for their expert advice together with the members of the Microstructural Analysis Unit of the University of Technology Sydney.

References

  1. 1.
    Lowenstam HA, Weiner S (1989) On biomineralization. Oxford University Press on Demand, OxfordGoogle Scholar
  2. 2.
    Weiner S, Dove PM (2003) An overview of biomineralization processes and the problem of the vital effect. In: Dove PM, DeYoreo JJ, Weiner S (eds) Biomineralization. Reviews in Mineralogy and Geochemistry, vol 54. Mineralogical Society America, Virginia, pp 1–29Google Scholar
  3. 3.
    Mann S (2001) Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry. Oxford University Press, New YorkGoogle Scholar
  4. 4.
    Weiner S, Addadi L (1997) Design strategies in mineralized biological materials. J Mater Chem 7:689–702CrossRefGoogle Scholar
  5. 5.
    Addadi L, Raz S, Weiner S (2003) Taking advantage of disorder: Amorphous calcium carbonate and its roles in biomineralization. Adv Mater 15:959–970CrossRefGoogle Scholar
  6. 6.
    Lowenstam HA (1981) Minerals formed by organisms. Science 211:1126–1131CrossRefGoogle Scholar
  7. 7.
    Brandi ML (2009) Microarchitecture, the key to bone quality. Rheumatology 48 Suppl 4: iv3–8CrossRefGoogle Scholar
  8. 8.
    Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3(Suppl 3):S131–S139CrossRefGoogle Scholar
  9. 9.
    Thomson BM (1998) Bone. In: Allen LH, Prentice A (eds) Encyclopedia of Human Nutrition (Second Edition), 2nd edn. Elsevier, Oxford, pp 220–225CrossRefGoogle Scholar
  10. 10.
    De Jong W (1926) La substance minerale dans les os. Recl Trav Chim Pays-Bas 45:445–448CrossRefGoogle Scholar
  11. 11.
    Terra J, Dourado ER, Eon JG et al (2009) The structure of strontium-doped hydroxyapatite: an experimental and theoretical study. Phys Chem Chem Phys 11:568–577CrossRefGoogle Scholar
  12. 12.
    Weiner S, Wagner HD (1998) The material bone: Structure mechanical function relations. Annu Rev Mater Res 28:271–298Google Scholar
  13. 13.
    Dorozhkin SV (2007) Calcium orthophosphates. J Mater Sci 42:1061–1095CrossRefGoogle Scholar
  14. 14.
    Felicio-Fernandes G, Laranjeira MCM (2000) Calcium phosphate biomaterials from marine algae. Hydrothermal synthesis and characterisation. Quim Nova 23:441–446CrossRefGoogle Scholar
  15. 15.
    LeGeros RZ, Trautz OR, Klein E et al (1969) Two types of carbonate substitution in the apatite structure. Experientia 25:5–7CrossRefGoogle Scholar
  16. 16.
    Ben-Nissan B, Chai C, Evans L (1995) Crystallographic and spectroscopic characterization and morphology of biogenic and synthetic apatites. In: Wise DL, Trantolo DJ, Altobelli DE et al (eds) Encyclopedic handbook of biomaterials and bioengineering: part B. Applications. Marcel Dekker, New York, pp 191–221Google Scholar
  17. 17.
    Combes C, Cazalbou S, Rey C (2016) Apatite biominerals. Minerals.  https://doi.org/10.3390/min6020034CrossRefGoogle Scholar
  18. 18.
    Launey ME, Buehler MJ, Ritchie RO (2010) On the mechanistic origins of toughness in bone. In: Clarke DR, Ruhle M, Zok F (eds) Annual review of materials research, vol 40. Annual Reviews, California, pp 25–53Google Scholar
  19. 19.
    LeGeros RZ (2008) Calcium phosphate-based osteoinductive materials. Chem Rev 108:4742–4753CrossRefGoogle Scholar
  20. 20.
    Thibodeau GA, Patton KT (2013) Structure and function of the body. Elsevier, New YorkGoogle Scholar
  21. 21.
    Tang D, Tare RS, Yang LY et al (2016) Biofabrication of bone tissue: approaches, challenges and translation for bone regeneration. Biomaterials 83:363–382CrossRefGoogle Scholar
  22. 22.
    Leach JK, Mooney DJ (2004) Bone engineering by controlled delivery of osteoinductive molecules and cells. Expert Opin Biol Ther 4:1015–1027CrossRefGoogle Scholar
  23. 23.
    Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17:1726–1733CrossRefGoogle Scholar
  24. 24.
    Keating JF, McQueen MM (2001) Substitutes for autologous bone graft in orthopaedic trauma. J Bone Joint Surg Br 83:3–8CrossRefGoogle Scholar
  25. 25.
    Williams DF (2008) On the mechanisms of biocompatibility. Biomaterials 29:2941–2953CrossRefGoogle Scholar
  26. 26.
    Finkemeier CG (2002) Bone-grafting and bone-graft substitutes. J Bone Joint Surg Am 84:454–464CrossRefGoogle Scholar
  27. 27.
    Oryan A, Alidadi S, Moshiri A et al (2014) Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res 9:18.  https://doi.org/10.1186/1749-799X-9-18CrossRefGoogle Scholar
  28. 28.
    Williams DF (2009) On the nature of biomaterials. Biomaterials 30:5897–5909CrossRefGoogle Scholar
  29. 29.
    Park J, Lakes RS (2007) Biomaterials: an Introduction. Springer, New YorkGoogle Scholar
  30. 30.
    Sivakumar R (1999) On the relevance and requirements of biomaterials. Bull Mater Sci 22:647–655CrossRefGoogle Scholar
  31. 31.
    Dubok VA (2000) Bioceramics - yesterday, today, tomorrow. Powder Metall Met Ceram 39:381–394CrossRefGoogle Scholar
  32. 32.
    Langer R, Vacanti JP (1993) Tissue Engineering. Science 260:920–926CrossRefGoogle Scholar
  33. 33.
    Nerem RM, Sambanis A (1995) Tissue engineering: from biology to biological substitutes. Tissue Eng 1:3–13CrossRefGoogle Scholar
  34. 34.
    Salgado AJ, Coutinho OP, Reis RL (2004) Bone tissue engineering: state of the art and future trends. Macromol Biosci 4:743–765CrossRefGoogle Scholar
  35. 35.
    Vacanti JP, Langer R (1999) Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet 354:SI32-SI34CrossRefGoogle Scholar
  36. 36.
    Ramay HR, Zhang M (2004) Biphasic calcium phosphate nanocomposite porous scaffolds for load-bearing bone tissue engineering. Biomaterials 25:5171–5180CrossRefGoogle Scholar
  37. 37.
    Ma L, Gao C, Mao Z et al (2003) Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials 24:4833–4841CrossRefGoogle Scholar
  38. 38.
    Mano JF, Vaz CM, Mendes SC et al (1999) Dynamic mechanical properties of hydroxyapatite-reinforced and porous starch-based degradable biomaterials. J Mater Sci Mater Med 10:857–862CrossRefGoogle Scholar
  39. 39.
    Vacanti JP, Morse MA, Saltzman WM et al (1988) Selective cell transplantation using bioabsorbable artificial polymers as matrices. J Pediatr Surg 23:3–9CrossRefGoogle Scholar
  40. 40.
    Crane GM, Ishaug SL, Mikos AG (1995) Bone tissue engineering. Nat Med 1:1322–1324CrossRefGoogle Scholar
  41. 41.
    Hutmacher DW (2000) Scaffolds in tissue engineering bone and cartilage. Biomaterials 21:2529–2543CrossRefGoogle Scholar
  42. 42.
    Gotoh Y, Fujisawa K, Satomura K et al (1995) Osteogenesis by human osteoblastic cells in diffusion chamber in vivo. Calcif Tissue Int 56:246–251CrossRefGoogle Scholar
  43. 43.
    Haynesworth SE, Goshima J, Goldberg VM et al (1992) Characterization of cells with osteogenic potential from human marrow. Bone 13:81–88CrossRefGoogle Scholar
  44. 44.
    Petrakova KV, Tolmacheva AA, Fridenshtein AY (1963) Osteogenesis following transplantation of marrow in diffusion chambers. Bull Exp Biol Med 56:1375–1378CrossRefGoogle Scholar
  45. 45.
    Bruder SP, Kurth AA, Shea M et al (1998) Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells. J Orthop Res 16:155–162CrossRefGoogle Scholar
  46. 46.
    Rose FR, Oreffo RO (2002) Bone tissue engineering: hope vs hype. Biochem Biophys Res Commun 292:1–7CrossRefGoogle Scholar
  47. 47.
    Reddi AH (1992) Regulation of cartilage and bone differentiation by bone morphogenetic proteins. Curr Opin Cell Biol 4:850–855CrossRefGoogle Scholar
  48. 48.
    Kim TH, Browne F, Upton J et al (1997) Enhanced induction of engineered bone with basic fibroblast growth factor. Tissue Eng 3:303–308CrossRefGoogle Scholar
  49. 49.
    Nevins M, Giannobile WV, McGuire MK et al (2005) Platelet-derived growth factor stimulates bone fill and rate of attachment level gain: results of a large multicenter randomized controlled trial. J Periodontol 76:2205–2215CrossRefGoogle Scholar
  50. 50.
    LeGeros RZ, LeGeros JP (2003) Calcium phosphate bioceramics: past, present and future. In: Ben-Nissan B, Sher D, Walsh W (eds) 15th international symposium on ceramics in medicine, Sydney, December 2002. Key engineering materials, vol 240–242. Trans Tech Publications, Zurich-Uetikon, pp 3–10CrossRefGoogle Scholar
  51. 51.
    Dimitriou R, Jones E, McGonagle D et al (2011) Bone regeneration: current concepts and future directions. BMC Med 9:66.  https://doi.org/10.1186/1741-7015-9-66CrossRefGoogle Scholar
  52. 52.
    Van Lieshout EM, Alt V (2016) Bone graft substitutes and bone morphogenetic proteins for osteoporotic fractures: what is the evidence? Injury 47:S43–S46CrossRefGoogle Scholar
  53. 53.
    Fernández E, Gil FJ, Ginebra MP et al (1999) Calcium phosphate bone cements for clinical applications. Part II: precipitate formation during setting reactions. J Mater Sci Mater Med 10:177–183CrossRefGoogle Scholar
  54. 54.
    Dorozhkin SV (2010) Bioceramics of calcium orthophosphates. Biomaterials 31:1465–1485CrossRefGoogle Scholar
  55. 55.
    Yuan H, Yang Z, Li Y et al (1998) Osteoinduction by calcium phosphate biomaterials. J Mater Sci Mater Med 9:723–726CrossRefGoogle Scholar
  56. 56.
    Liu JB, Ye XY, Wang H et al (2003) The influence of pH and temperature on the morphology of hydroxyapatite synthesized by hydrothermal method. Ceram Int 29:629–633CrossRefGoogle Scholar
  57. 57.
    Mekmene O, Quillard S, Rouillon T et al (2009) Effects of pH and Ca/P molar ratio on the quantity and crystalline structure of calcium phosphates obtained from aqueous solutions. Dairy Sci Technol 89:301–316CrossRefGoogle Scholar
  58. 58.
    Jillavenkatesa A, Condrate RA (1998) Sol-gel processing of hydroxyapatite. J Mater Sci 33:4111–4119CrossRefGoogle Scholar
  59. 59.
    Santos MH, de Oliveira M, Souza LPdF et al (2004) Synthesis control and characterization of hydroxyapatite prepared by wet precipitation process. Mater Res 7:625–630CrossRefGoogle Scholar
  60. 60.
    Earl JS, Wood DJ, Milne SJ (2006) Hydrothermal synthesis of hydroxyapatite. In: Brown PD, Baker R, Hamilton B (eds) EMAG/NANO conference on imaging, analysis and fabrication on the nanoscale, Leeds, August 2005. journal of physics conference series, vol 26. IOP Publishing Ltd., Bristol, p 268Google Scholar
  61. 61.
    Ramay HR, Zhang M (2003) Preparation of porous hydroxyapatite scaffolds by combination of the gel-casting and polymer sponge methods. Biomaterials 24:3293–3302CrossRefGoogle Scholar
  62. 62.
    Flatley TJ, Lynch KL, Benson M (1983) Tissue response to implants of calcium phosphate ceramic in the rabbit spine. Clin Orthop Relat Res 179:246–252CrossRefGoogle Scholar
  63. 63.
    Hing KA, Annaz B, Saeed S et al (2005) Microporosity enhances bioactivity of synthetic bone graft substitutes. J Mater Sci Mater Med 16:467–475CrossRefGoogle Scholar
  64. 64.
    Mobasherpour I, Heshajin MS, Kazemzadeh A et al (2007) Synthesis of nanocrystalline hydroxyapatite by using precipitation method. J Alloys Compd 430:330–333CrossRefGoogle Scholar
  65. 65.
    Shih WJ, Chen YF, Wang MC et al (2004) Crystal growth and morphology of the nano-sized hydroxyapatite powders synthesized from CaHPO4·2H2O and CaCO3 by hydrolysis method. J Cryst Growth 270:211–218CrossRefGoogle Scholar
  66. 66.
    Rao RR, Roopa HN, Kannan TS (1997) Solid state synthesis and thermal stability of HAp and HAp - β-TCP composite ceramic powders. J Mater Sci Mater Med 8:511–518CrossRefGoogle Scholar
  67. 67.
    Yeon KC, Wang J, Ng SC (2001) Mechanochemical synthesis of nanocrystalline hydroxyapatite from CaO and CaHPO4. Biomaterials 22:2705–2712CrossRefGoogle Scholar
  68. 68.
    Ghosh SK, Roy SK, Kundu B et al (2011) Synthesis of nano-sized hydroxyapatite powders through solution combustion route under different reaction conditions. Mater Sci Eng B-Adv 176:14–21CrossRefGoogle Scholar
  69. 69.
    Roy DM, Linnehan SK (1974) Hydroxyapatite formed from coral skeletal carbonate by hydrothermal exchange. Nature 247:220–222CrossRefGoogle Scholar
  70. 70.
    Hu J, Russell JJ, Ben-Nissan B et al (2001) Production and analysis of hydroxyapatite from Australian corals via hydrothermal process. J Mater Sci Lett 20:85–87CrossRefGoogle Scholar
  71. 71.
    Vecchio KS, Zhang X, Massie JB et al (2007) Conversion of bulk seashells to biocompatible hydroxyapatite for bone implants. Acta Biomater 3:910–918CrossRefGoogle Scholar
  72. 72.
    Raihana MF, Sopyan I, Hamdi M et al (2008) Novel chemical conversion of eggshell to hydroxyapatite powder. In: Abu Osman NA, Ibrahim F, Wan Abas WAB et al (eds) 4th Kuala Lumpur international conference on biomedical engineering, Vols 1 and 2, Kuala Lumpur, Jun 2008. IFMBE Proceedings, vol 21. Springer, New York, p 333Google Scholar
  73. 73.
    Liu DM (1996) Fabrication and characterization of porous hydroxyapatite granules. Biomaterials 17:1955–1957CrossRefGoogle Scholar
  74. 74.
    Sepulveda P, Binner JG, Rogero SO et al (2000) Production of porous hydroxyapatite by the gel-casting of foams and cytotoxic evaluation. J Biomed Mater Res 50:27–34CrossRefGoogle Scholar
  75. 75.
    Sopyan I, Kaur J (2009) Preparation and characterization of porous hydroxyapatite through polymeric sponge method. Ceram Int 35:3161–3168CrossRefGoogle Scholar
  76. 76.
    Leukers B, Gülkan H, Irsen SH et al (2005) Hydroxyapatite scaffolds for bone tissue engineering made by 3D printing. J Mater Sci Mater Med 16:1121–1124CrossRefGoogle Scholar
  77. 77.
    Fierz FC, Beckmann F, Huser M et al (2008) The morphology of anisotropic 3D-printed hydroxyapatite scaffolds. Biomaterials 29:3799–3806CrossRefGoogle Scholar
  78. 78.
    Cox SC, Thornby JA, Gibbons GJ et al (2015) 3D printing of porous hydroxyapatite scaffolds intended for use in bone tissue engineering applications. Mater Sci Eng C Mater Biol Appl 47:237–247CrossRefGoogle Scholar
  79. 79.
    Sadat-Shojai M, Khorasani MT, Dinpanah-Khoshdargi E et al (2013) Synthesis methods for nanosized hydroxyapatite with diverse structures. Acta Biomater 9:7591–7621CrossRefGoogle Scholar
  80. 80.
    Ivankovic H, Gallego Ferrer G, Tkalcec E et al (2009) Preparation of highly porous hydroxyapatite from cuttlefish bone. J Mater Sci Mater Med 20:1039–1046CrossRefGoogle Scholar
  81. 81.
    Rodríguez-Lugo V, Hernández JS, Arellano-Jimenez MJ et al (2005) Characterization of hydroxyapatite by electron microscopy. Microsc Microanal 11:516–523CrossRefGoogle Scholar
  82. 82.
    Sivakumar M, Kumar TS, Shantha KL et al (1996) Development of hydroxyapatite derived from Indian coral. Biomaterials 17:1709–1714CrossRefGoogle Scholar
  83. 83.
    Kasperk C, Ewers R (1986) Tierexperimentelle untersuchungen zur einheilungstendenz synthetischer, koralliner und aus Algen gewonnener (phykogener) Hydroxylapatitmaterialien. Z Zahnärztl Implantol 2:242–248Google Scholar
  84. 84.
    Walsh PJ, Buchanan FJ, Dring M et al (2008) Low-pressure synthesis and characterisation of hydroxyapatite derived from mineralise red algae. Chem Eng J 137:173–179CrossRefGoogle Scholar
  85. 85.
    Allemand D, Tambutté É, Zoccola D et al (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 119–150CrossRefGoogle Scholar
  86. 86.
    Bilan MI, Usov AI (2001) Polysaccharides of calcareous algae and their effect on the calcification process. Russ J Bioorgan Chem 27:2–16CrossRefGoogle Scholar
  87. 87.
    Green DW, Ben-Nissan B, Yoon KS et al (2017) Natural and synthetic coral biomineralization for human bone revitalization. Trends Biotechnol 35:43–54CrossRefGoogle Scholar
  88. 88.
    Pena J, LeGeros RZ, Rohanizadeh R et al (2000) CaCO3/Ca-P biphasic materials prepared by microwave processing of natural aragonite and calcite. In: Giannini S, Moroni A (eds) 13th international symposium on ceramic in medicine/symposium on ceramic materials in orthopaedic surgery: clinical results in the Year 2000, Bologna, November 2000. Key Engineering Materials, vol 192–1. Trans Tech Publications, Zurich-Uetikon, pp 267–270Google Scholar
  89. 89.
    Cegla RNR, Macha IJ, Ben-Nissan B et al (2014) Comparative study of conversion of coral with ammonium dihydrogen phosphate and orthophosphoric acid to produce calcium phosphates. J Aust Ceram Soc 50:154–161Google Scholar
  90. 90.
    Macha IJ, Boonyang U, Cazalbou S et al (2015) Comparative study of coral conversion, Part 2: microstructural evolution of calcium phosphate. J Aust Ceram Soc 51:149–159Google Scholar
  91. 91.
    Guillemin G, Patat JL, Fournie J et al (1987) The use of coral as a bone graft substitute. J Biomed Mater Res 21:557–567CrossRefGoogle Scholar
  92. 92.
    Lough JM (2008) 10th Anniversary Review: a changing climate for coral reefs. J Environ Monit 10:21–29CrossRefGoogle Scholar
  93. 93.
    Wray JL (1977) Calcareous algae. Elsevier Science, New YorkGoogle Scholar
  94. 94.
    Kasperk C, Ewers R, Simons B et al (1988) Algae-derived (phycogene) hydroxylapatite. A comparative histological study. Int J Oral Maxillofac Surg 17:319–324CrossRefGoogle Scholar
  95. 95.
    Ewers R (2005) Maxilla sinus grafting with marine algae derived bone forming material: a clinical report of long-term results. J Oral Maxillofac Surg 63:1712–1723CrossRefGoogle Scholar
  96. 96.
    Choi G, Karacan I, Cazalbou S et al (2017) Conversion of calcified algae (Halimeda sp) and hard coral (Porites sp) to hydroxyapatite. In: Rey C, Combes C, Drouet C (eds), 29th international symposium on ceramics in medicine, Toulouse, October 2017. Key engineering materials, vol 758. Trans Tech Publications, Zurich-Uetikon, pp 157–161Google Scholar
  97. 97.
    Denny MW, Gaines SD (eds) (2007) Encyclopedia of Tidepools and Rocky Shores. University of California Press, CaliforniaGoogle Scholar
  98. 98.
    Borowitzka MA, Larkum AW (1977) Calcification in the green alga Halimeda. I. An ultrastructure study of thallus development. J Phycol 13:6–16Google Scholar
  99. 99.
    Tatum H Jr (1986) Maxillary and sinus implant reconstructions. Dent Clin North Am 30:207–229Google Scholar
  100. 100.
    Schopper C, Moser D, Wanschitz F et al (1999) Histomorphologic findings on human bone samples six months after bone augmentation of the maxillary sinus with Algipore. J Long Term Eff Med Implants 9:203–213Google Scholar
  101. 101.
    Ewers R, Goriwoda W, Schopper C et al (2004) Histologic findings at augmented bone areas supplied with two different bone substitute materials combined with sinus floor lifting. Report of one case. Clin Oral Implants Res 15:96–100CrossRefGoogle Scholar
  102. 102.
    Poeschl PW, Ziya-Ghazvini F, Schicho K et al (2012) Application of platelet-rich plasma for enhanced bone regeneration in grafted sinus. J Oral Maxillofac Surg 70:657–664CrossRefGoogle Scholar
  103. 103.
    Marx RE, Carlson ER, Eichstaedt RM et al (1998) Platelet-rich plasma: Growth factor enhancement for bone grafts. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 85:638–646CrossRefGoogle Scholar
  104. 104.
    Marx RE (2004) Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg 62:489–496CrossRefGoogle Scholar
  105. 105.
    Klongnoi B, Rupprecht S, Kessler P et al (2006) Lack of beneficial effects of platelet-rich plasma on sinus augmentation using a fluorohydroxyapatite or autogenous bone: an explorative study. J Clin Periodontol 33:500–509CrossRefGoogle Scholar
  106. 106.
    Turhani D, Cvikl B, Watzinger E et al (2005) In vitro growth and differentiation of osteoblast-like cells on hydroxyapatite ceramic granule calcified from red algae. J Oral Maxillofac Surg 63:793–799CrossRefGoogle Scholar
  107. 107.
    Malicev E, Marolt D, Kregar Velikonja N et al (2008) Growth and differentiation of alveolar bone cells in tissue-engineered constructs and monolayer cultures. Biotechnol Bioeng 100:773–781CrossRefGoogle Scholar
  108. 108.
    Turhani D, Watzinger E, Weissenböck M et al (2005) Three-dimensional composites manufactured with human mesenchymal cambial layer precursor cells as an alternative for sinus floor augmentation: an in vitro study. Clin Oral Implants Res 16:417–424CrossRefGoogle Scholar
  109. 109.
    Weissenboeck M, Stein E, Undt G et al (2006) Particle size of hydroxyapatite granules calcified from red algae affects the osteogenic potential of human mesenchymal stem cells in vitro. Cells Tissues Organs 182:79–88CrossRefGoogle Scholar
  110. 110.
    Sollazzo V, Palmieri A, Scapoli L et al (2009) Algipore effects on stem cells derived from peripheral blood. J Osseointegration 1:78–85Google Scholar
  111. 111.
    Girardi A, Palmieri A, Cura F et al (2012) Effect of Algipore® on bone marrow stem cells: an in vitro study. Eur J Inflamm 10:59–64Google Scholar
  112. 112.
    Pieri F, Lucarelli E, Corinaldesi G et al (2008) Mesenchymal stem cells and platelet-rich plasma enhance bone formation in sinus grafting: a histomorphometric study in minipigs. J Clin Periodontol 35:539–546CrossRefGoogle Scholar
  113. 113.
    Pieri F, Lucarelli E, Corinaldesi G et al (2009) Effect of mesenchymal stem cells and platelet-rich plasma on the healing of standardized bone defects in the alveolar ridge: a comparative histomorphometric study in minipigs. J Oral Maxillofac Surg 67:265–272CrossRefGoogle Scholar
  114. 114.
    Stuart B (2000) Infrared Spectroscopy. Kirk-Othmer Encyclopedia of Chemical Technology. Wiley, New JerseyGoogle Scholar
  115. 115.
    Berzina-Cimdina L, Borodajenko N (2012) Research of calcium phosphates using fourier transform infrared spectroscopy. In: Theophile T (ed) Infrared spectroscopy. IntechOpen, London.  https://doi.org/10.5772/36942Google Scholar
  116. 116.
    Lee M (2016) X-Ray diffraction for materials research: from fundamentals to applications. Apple Academic Press, New JerseyGoogle Scholar
  117. 117.
    Sigel A, Sigel H, Sigel RKO (eds) (2008) Biomineralization: from nature to application. Wiley, ChichesterGoogle Scholar
  118. 118.
    O’Brien P, Imai H, Green M et al (eds) (2012) Nanoscience: nanostructures through chemistry. Royal Society of Chemistry, LondonGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.School of Mathematical and Physical SciencesUniversity of Technology SydneyBroadwayAustralia

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