Conversion of natural marine skeletons as scaffolds for bone tissue engineering

doi:10.1007/s11706-013-0204-x

Front Mater Sci

2013, Vol. 7

Issue (2) : 103-117 https://doi.org/10.1007/s11706-013-0204-x

REVIEW ARTICLE

Conversion of natural marine skeletons as scaffolds for bone tissue engineering

Xing ZHANG¹(

), Kenneth S. VECCHIO²

1. Department of Bioengineering, Rice University, Houston, Texas 77030, USA; 2. Department of NanoEngineering, University of California at San Diego, La Jolla, California 92093, USA

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Abstract

Marine CaCO₃ skeletons have tailored architectures created by nature, which give them structural support and other functions. For example, seashells have dense lamellar structures, while coral, cuttlebone and sea urchin spines have interconnected porous structures. In our experiments, seashells, coral and cuttlebone were hydrothermally converted to hydroxyapatite (HAP), and sea urchin spines were converted to Mg-substituted tricalcium phosphate, while maintaining their original structures. Partially converted shell samples have mechanical strength, which is close to that of compact human bone. After implantation of converted shell and spine samples in rat femoral defects for 6 weeks, there was newly formed bone growth up to and around the implants. Some new bone was found to migrate through the pores of converted spine samples and grow inward. These results show good bioactivity and osteoconductivity of the implants, indicating the converted shell and spine samples can be used as bone defect fillers. The interconnected porous HAP scaffolds from converted coral or cuttlebone that have pore size larger than 100 μm likely support infiltration of bone cells and vessels, and finally encourage new bone ingrowth.

Keywords seashell sea urchin spine coral cuttlebone hydrothermal conversion hydroxyapatite (HAP) β-tricalcium phosphate (β-TCP)

Corresponding Author(s): ZHANG Xing,Email:xingucsd@gmail.com

Issue Date: 05 June 2013

Cite this article:

Xing ZHANG,Kenneth S. VECCHIO. Conversion of natural marine skeletons as scaffolds for bone tissue engineering[J]. Front Mater Sci, 2013, 7(2): 103-117.

URL:

https://academic.hep.com.cn/foms/EN/10.1007/s11706-013-0204-x
https://academic.hep.com.cn/foms/EN/Y2013/V7/I2/103

1	Laurencin C T, Attawia M, Borden M D. Advancements in tissue engineered bone substitutes. Current Opinion in Orthopaedics , 1999, 10(6): 445–451
2	Enneking W. Transplanting allografts. Journal of the American College of Surgeons , 2005, 201(1): 5–6
3	LeGeros R Z. Biodegradation and bioresorption of calcium phosphate ceramics. Clinical Materials , 1993, 14(1): 65–88
4	Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials , 2005, 26(27): 5474–5491
5	Hing K A. Bioceramic bone graft substitutes: Influence of porosity and chemistry. International Journal of Applied Ceramic Technology , 2005, 2(3): 184–199
6	LeGeros R Z. Properties of osteoconductive biomaterials: calcium phosphates. Clinical Orthopaedics and Related Research , 2002, 395(395): 81–98
7	Vallet-Regí M, González-Calbet J M. Calcium phosphates as substitution of bone tissues. Progress in Solid State Chemistry , 2004, 32(1-2): 1–31
8	Aoki H, Kato K, Ebihara M, . Studies on the application of apatite to dental materials. (I) Apatite ceramics. Shika Rikogaku Zasshi , 1976, 17(39): 200–205
9	Barney V C, Levin M P, Adams D F. Bioceramic implants in surgical periodontal defects. A comparison study. Journal of Periodontology , 1986, 57(12): 764–770
10	Cranin A N, Tobin G P, Gelbman J. Applications of hydroxylapatite in oral and maxillofacial surgery. Part II: Ridge augmentation and repair of major oral defects. Compendium , 1987, 8(5): 334–335 , 337 -338 , 340
11	Denissen H W, de Groot K. Immediate dental root implants from synthetic dense calcium hydroxylapatite. The Journal of Prosthetic Dentistry , 1979, 42(5): 551–556
12	Ellinger R F, Nery E B, Lynch K L. Histological assessment of periodontal osseous defects following implantation of hydroxyapatite and biphasic calcium phosphate ceramics: a case report. The International Journal of Periodontics & Restorative Dentistry , 1986, 6(3): 22–33
13	Albee F H, Morrison H A R O L D F. Studies in bone growth: triple calcium phosphate as a stimulus to osteogenesis. Annals of Surgery , 1920, 71(1): 32–39
14	Daculsi G, Passuti N, Martin S, . Macroporous calcium phosphate ceramic for long bone surgery in humans and dogs. Clinical and histological study. Journal of Biomedical Materials Research , 1990, 24(3): 379–396
15	Sun L, Berndt C C, Gross K A, . Material fundamentals and clinical performance of plasma-sprayed hydroxyapatite coatings: a review. Journal of Biomedical Materials Research , 2001, 58(5): 570–592
16	Hing K A, Revell P A, Smith N, . Effect of silicon level on rate, quality and progression of bone healing within silicate-substituted porous hydroxyapatite scaffolds. Biomaterials , 2006, 27(29): 5014–5026
17	Kondo N, Ogose A, Tokunaga K, . Bone formation and resorption of highly purified beta-tricalcium phosphate in the rat femoral condyle. Biomaterials , 2005, 26(28): 5600–5608
18	Hasegawa S, Ishii S, Tamura J, . A 5-7 year in vivo study of high-strength hydroxyapatite/poly(l-lactide) composite rods for the internal fixation of bone fractures. Biomaterials , 2006, 27(8): 1327–1332
19	Ohura K, Bohner M, Hardouin P, . Resorption of, and bone formation from, new β-tricalcium phosphate-monocalcium phosphate cements: An in vivo study. Journal of Biomedical Materials Research , 1996, 30(2): 193–200
20	Tanaka T, Kumagae Y, Saito M, . Bone formation and resorption in patients after implantation of β-tricalcium phosphate blocks with 60% and 75% porosity in opening-wedge high tibial osteotomy. Journal of Biomedical Materials Research Part B: Applied Biomaterials , 2008, 86B(2): 453–459
21	Okuda T, Ioku K, Yonezawa I, . The effect of the microstructure of beta-tricalcium phosphate on the metabolism of subsequently formed bone tissue. Biomaterials , 2007, 28(16): 2612–2621
22	Yoshikawa H, Tamai N, Murase T, . Interconnected porous hydroxyapatite ceramics for bone tissue engineering. Journal of the Royal Society Interface , 2009, 6(Suppl 3): S341–S348
23	Bose S, Roy M, Bandyopadhyay A. Recent advances in bone tissue engineering scaffolds. Trends in Biotechnology , 2012, 30(10): 546–554
24	Suchanek W, Yoshimura M. Processing and properties of hydroxyapatite-based biomaterials for use as hard tissue replacement implants. Journal of Materials Research , 1998, 13(01): 94–117
25	Kaplan D L. Mollusc shell structures: novel design strategies for synthetic materials. Current Opinion in Solid State and Materials Science , 1998, 3(3): 232–236
26	Belcher A M, Wu X H, Christensen R J, . Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature , 1996, 381(6577): 56–58
27	Sudo S, Fujikawa T, Nagakura T, . Structures of mollusc shell framework proteins. Nature , 1997, 387(6633): 563–564
28	Vecchio K S, Zhang X, Massie J B, . Conversion of bulk seashells to biocompatible hydroxyapatite for bone implants. Acta Biomaterialia , 2007, 3(6): 910–918
29	Roy D M, Linnehan S K. Hydroxyapatite formed from coral skeletal carbonate by hydrothermal exchange. Nature , 1974, 247(5438): 220–222
30	Birchall J D, Thomas N L. On the architecture and function of cuttlefish bone. Journal of Materials Science , 1983, 18(7): 2081–2086
31	Kim B-S, Kim J S, Sung H-M, . Cellular attachment and osteoblast differentiation of mesenchymal stem cells on natural cuttlefish bone. Journal of Biomedical Materials Research Part A , 2012, 100A(7): 1673–1679
32	Vecchio K S, Zhang X, Massie J B, . Conversion of sea urchin spines to Mg-substituted tricalcium phosphate for bone implants. Acta Biomaterialia , 2007, 3(5): 785–793
33	Lin A Y M, Meyers M A, Vecchio K S. Mechanical properties and structure of Strombus gigas, Tridacna gigas, and Haliotis rufescens sea shells: A comparative study. Materials Science and Engineering C , 2006, 26(8): 1380–1389
34	Camprasse S, Camprasse G, Pouzol M, . Artificial dental root made of natural calcium carbonate (bioracine). Clinical Materials , 1990, 5(2-4): 235–250
35	Lamghari M, Almeida M J, Berland S, . Stimulation of bone marrow cells and bone formation by nacre: in vivo and in vitro studies. Bone , 1999, 25(2 Supplement 1): 91S–94S
36	Lopez E, Vidal B, Berland S, . Demonstration of the capacity of nacre to induce bone formation by human osteoblasts maintained in vitro. Tissue and Cell , 1992, 24(5): 667–679
37	Atlan G, Delattre O, Berland S, . Interface between bone and nacre implants in sheep. Biomaterials , 1999, 20(11): 1017–1022
38	Zhang X, Vecchio K S. Creation of dense hydroxyapatite (synthetic bone) by hydrothermal conversion of seashells. Materials Science and Engineering C , 2006, 26(8): 1445–1450
39	Menig R, Meyers M H, Meyers M A, . Quasi-static and dynamic mechanical response of Strombus gigas (conch) shells. Materials Science and Engineering A , 2001, 297(1-2): 203–211
40	Hou D F, Zhou G S, Zheng M. Conch shell structure and its effect on mechanical behaviors. Biomaterials , 2004, 25(4): 751–756
41	Kamat S, Su X, Ballarini R, . Structural basis for the fracture toughness of the shell of the conch Strombus gigas. Nature , 2000, 405(6790): 1036–1040
42	Weber J N, White E W, Lebiedzik J. New porous biomaterials by replication of echinoderm skeletal microstructures. Nature , 1971, 233(5318): 337–339
43	Rocha J H, Lemos A F, Agathopoulos S, . Hydrothermal growth of hydroxyapatite scaffolds from aragonitic cuttlefish bones. Journal of Biomedical Materials Research Part A , 2006, 77A(1): 160–168
44	LeGeros R Z, Gatti A M, Kijkowska R, . Mg-substituted tricalcium phosphates: formation and properties. Key Engineering Materials , 2004, 254-256: 127–130
45	Zhang X, Takahashi T, Vecchio K S. Development of bioresorbable Mg-substituted tricalcium phosphate scaffolds for bone tissue engineering. Materials Science and Engineering C , 2009, 29(6): 2003–2010
46	Zhang X, Jiang F, Groth T, . Preparation, characterization and mechanical performance of dense β-TCP ceramics with/without magnesium substitution. Journal of Materials Science: Materials in Medicine , 2008, 19(9): 3063–3070
47	Rezwan K, Chen Q Z, Blaker J J, . Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials , 2006, 27(18): 3413–3431
48	Wasielewski R C, Sheridan K C, Lubbers M A. Coralline hydroxyapatite in complex acetabular reconstruction. Orthopedics , 2008, 31(4): 367
49	Knackstedt M A, Arns C H, Senden T J, . Structure and properties of clinical coralline implants measured via 3D imaging and analysis. Biomaterials , 2006, 27(13): 2776–2786
50	Hsu C-J, Chou W-Y, Teng H-P, . Coralline hydroxyapatite and laminectomy-derived bone as adjuvant graft material for lumbar posterolateral fusion. Journal of Neurosurgery: Spine , 2005, 3(4): 271–275
51	Ivankovic H, Gallego Ferrer G, Tkalcec E, . Preparation of highly porous hydroxyapatite ceramics from cuttlefish bone. Advances in Science and Technology , 2006, 49: 142–147
52	Zhang X. Preparation and characterization of calcium phosphate ceramics and composites as bone substitutes. Dissertation for the Doctoral Degree . San Diego, USA: University of California, 2007
53	Klawitter J J, Bagwell J G, Weinstein A M, . An evaluation of bone growth into porous high density polyethylene. Journal of Biomedical Materials Research , 1976, 10(2): 311–323
54	Klawitter J J, Hulbert S F. Application of porous ceramics for the attachment of load bearing internal orthopedic applications. Journal of Biomedical Materials Research Part A , 1971, 5(6): 161–229
55	Sherrard K M. Cuttlebone morphology limits habitat depth in eleven species of Sepia (Cephalopoda: Sepiidae). The Biological Bulletin , 2000, 198(3): 404–414
56	Denton E J, Gilpin-Brown J B. The buoyancy of the cuttlefish, Sepia officinalis (L.). Journal of the Marine Biological Association of the United Kingdom , 1961, 41(2): 319–342
57	Walsh P J, Buchanan F J, Dring M, . Low-pressure synthesis and characterisation of hydroxyapatite derived from mineralise red algae. Chemical Engineering Journal , 2008, 137(1): 173–179
58	Felicio-Fernandes G, Laranjeira M C M. Calcium phosphate biomaterials from marine algae. Hydrothermal synthesis and characterisation. Quimica Nova , 2000, 23(4): 441–446
59	dePaula S M, Huila M F, Araki K, . Confocal Raman and electronic microscopy studies on the topotactic conversion of calcium carbonate from Pomacea lineate shells into hydroxyapatite bioceramic materials in phosphate media. Micron , 2010, 41(8): 983–989
60	Cunningham E, Dunne N, Walker G, . Hydroxyapatite bone substitutes developed via replication of natural marine sponges. Journal of Materials Science: Materials in Medicine , 2010, 21(8): 2255–2261

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