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Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor
Ceramics International ∎ (∎∎∎∎) ∎∎∎–∎∎∎
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Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor Akari Takeuchi a,n, Tomohito Tsuge a, Masanori Kikuchi b a b
Department of Chemistry, Faculty of Science, Shinshu University, 3-1-1, Asahi, Matsumoto, Nagano 390-8621, Japan National Institute for Materials Science, 1-1, Namiki, Tsukuba, Ibaraki 305-0044, Japan
art ic l e i nf o
a b s t r a c t
Article history: Received 31 May 2016 Accepted 27 June 2016
Porous β-tricalcium phosphate (β-TCP) was successfully prepared from starfish-derived calcium carbonate (sf-bone) under several hydrothermal conditions. The sf-bone, obtained from Patiria Pectinifera by bleaching to remove organic substances, was Mg-containing calcite granules with an interconnected microporous structure of approximately 10 50 mm of pore, and was hydrothermally treated with ammonium phosphate aqueous solutions at various pHs and temperatures. The sf-bone was converted to Mg-containing β-TCP with maintaining its microporous structure by the hydrothermal treatment for 1 day or longer in (NH4)2HPO4 aqueous solution at 200 °C. This conversion was based on dissolutionreprecipitation process of Mg-containing calcite in the phosphate salt aqueous solution. Thus, conditions during the conversion, pH and temperature, affected the morphologies and crystal phases of sf-bone after the treatment depended upon both calcite dissolution and calcium phosphate-formation rates. & 2016 Published by Elsevier Ltd and Techna Group S.r.l.
Keywords: β-tricalcium phosphate Porous calcium phosphate Calcium carbonate Hydrothermal treatment
1. Introduction Although bone is a living tissue and has macropores for cell penetration and micropores for transportation of nutrients and body fluids, micropores in bioactive bone filling porous ceramics, hydroxyapatite (HAp, Ca10(PO4)6(OH)2) and β-tricalcium phosphate (β-TCP, β-Ca3(PO4)2), had not been considered enough. In fact, presence of macropores, more than 100 mm in diameter, in these ceramics has achieved sufficient clinical result in their limited applications with their good cell and bone tissue penetrations. However, in recent situations to expand applications of these bioactive porous ceramics to the cell scaffold in the regenerative medicine, the importance of their micro-pores have been considered to enable cell viability as well as to enable faster bone formation [1,2]. Many fabrication techniques for porous ceramics from synthetic calcium phosphates have been documented, e.g., by using burnable porogens [3–6] or polyurethane foams [7–9], by gelcasting methods [10–12] and by additive manufacturing [13,14], etc. Usage of porognes or polyurethane foams lead insufficient pore wall strength due to microcracks formed by their expansions caused by heating and following their vaporization. Thus, these methods showed drawbacks in mechanical strength and operability if they have sufficient pore interconnectivity. Gelcastings n
Corresponding author. E-mail address: [email protected] (A. Takeuchi).
with a foaming agent and appropriate gelation agent seemed to be the best porous ceramics in the traditional way; however, they can only control very well in a spherical macroporous structure, which is not similar to that of bone. Even additive manufacturing is a promising method to control of multi-scale structure, it still under investigation to control microporous structure for ceramics. Recently, tri-scale porous bioceramics, Apaceram-AXs, HAp, and Superpores, β-TCP, were commercialized by HOYA Technosurgical Co.; however, their macroporous structure is still spherical, and the size of micropores is less than 10 mm, which is generally enough for water penetration but is not optimized for in vivo environment. Further, porous HAp with micro- and macropores by sintering apatite fibers showed good bone formation as described above, but is very weak. In sum, porous ceramics of calcium phosphates with micro- and macropores fabricated from their synthetic powders faced on processing difficulties to control their porous structure. Contrarily, HAp converted from coralline mineral had success with the interconnected macroporous structure similar to cancellous bone [15–18]. Coralline mineral is porous calcium carbonate (aragonite or calcite) with pore sizes in the ranges of 150– 500 mm. Roy and Linnehan were firstly reported the hydrothermal method to convert coral calcium carbonate to HAp with a maintenance of the porous structure [15]. This porous HAp is called coralline apatite and commercially available bone graft in the United States as ProOsteons. Although it shows high affinity to bone and has cancellous bone-like structure, it does not have micropores. The use of coralline minerals has also drawbacks
http://dx.doi.org/10.1016/j.ceramint.2016.06.183 0272-8842/& 2016 Published by Elsevier Ltd and Techna Group S.r.l.
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 1. Morphologies of sf-bone harvested from Patiria pectinifera. (a): Naked-eye image. (b), (c): FE-SEM images at lower and higher magnifications, respectively.
Irregular shapes of the granules would result in macroporous structure due to the inter-granules hollow after packed into bone defect. Therefore, the feasibility of starfish-derived calcite to be a source material to prepare porous calcium phosphate was investigated in the present study. Porous calcium carbonates obtained from the starfish, Patiria Pectinifera harvested from oceans around Japan, were hydrothermally treated with ammonium phosphate aqueous solutions at various pHs and temperatures, and effects of pHs and temperatures on the transformation of starfish derived porous calcium carbonate to calcium phosphate were investigated.
2. Materials and methods
Fig. 2. Powder XRD pattern of sf-bone harvested from Patiria pectinifera.
associated with the harvest of corals from the sea, i.e., high cost due to harvesting corals from sea and most importantly, decreasing of corals strongly affect to global environment including global warming because of carbonate reservoir role of corals. Considering marine environment, utilization of marine wastes could be better than that of marine resources that are important for the environment. Starfishes are generally by-caught in net fisheries and caught by control programs of marine environments, and are a marine waste. Starfish mineral is known as Mg2 þ containing calcite granules [19], and they have interconnected microporous structure of several tens micrometers in pore diameter.
2.1. Preparation of porous calcium phosphate P. Pectinifera, one of starfish species, was used to obtain porous calcium carbonates for a precursor material of porous calcium phosphate. Organic substances of the starfish was removed by soaking it in a domestic bleach (approximately 6 vol% sodium hypochlorite aqueous solution, Haiters, Kao Co., Tokyo, Japan) overnight. The porous granules of calcium carbonate (sf-bone) obtained were then filtered, rinsed with ion-exchanged water for 5 times and dried at 60 °C for 24 h. One point five grams of sf-bone granules and 20 mL of 0.5 mol/ L (NH4)2HPO4 (pH 8.0) or (NH4)H2PO4 (pH 4.0) aqueous solution were put into a stainless steel autoclave at a filling ratio of 80% in volume and hydrothermally treated at 60, 80, 100 or 200 °C for 1 h,
Table 1 Main crystal phases, Mg contents and lattice parameters of sf-bones before and after hydrothermal treatment. Treatment period
Non treated 1h 1 day 3 days 7 days Calcite* β-TCP** Mg-containing β-TCP[20] * **
Main crystal phase
Calcite Calcite þ β-TCP β-TCP β-TCP β-TCP Calcite β-TCP β-TCP
Mg content /mmol g 1
1.32 7 0.04 – 1.28 7 0.08 1.217 0.09 1.197 0.20 – – –
Mg/(Ca þ Mg) molar ratio
0.1397 0.003 – 0.1417 0.001 0.1427 0.001 0.1427 0.002 – 0 0.29
(Ca þ Mg)/P molar ratio
– – 1.54 7 0.04 1.50 7 0.03 1.497 0.01 – 1.50 1.50
Lattice parameter /Å a
c
4.9331(6)
16.811(5)
10.330(8) 10.331(14) 10.334(3) 4.989 10.429 10.337(1)
37.14(4) 37.14(6) 37.117(7) 17.062 37.38 37.068(4)
ICDD-5-586. ICDD-9-169.
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 3. FE-SEM images of sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h ((a), (e)), 1 day ((b), (f)), 3 days ((c), (g)) and 7 days ((d), (h)). (a)–(d): Images at lower magnification. (e)–(h): Images at higher magnification.
1 day, 3 days and 7 days. The samples obtained were rinsed with ion-exchanged water for 10 times and dried at 60 °C for 24 h. 2.2. Characterization of porous calcium phosphate
Fig. 4. Powder XRD patterns of sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h (a), 1 day (b), 3 days (c) and 7 days (d).
Morphologies of the sf-bone granules before and after hydrothermal treatment were observed with a field emission-scanning electron microscope (FE-SEM, JSM-7600F, JEOL Ltd., Tokyo, Japan) equipped with an energy dispersive X-ray spectroscope (EDX, X– MaxN, Oxford Instruments plc., Oxfordshire, United Kingdom) at an accelerating voltage of 15 kV. Inorganic phases of the sf-bone granules before and after hydrothermal treatment were identified by powder X-ray diffractometry (XRD, Ultima IV, Rigaku Corp., Tokyo, Japan) using counter-monochromatized CuKα radiation generated at 40 kV and 40 mA by a continuous scanning mode at a step size of 0.02° and a scanning rate of 2.00°/min. Lattice parameters of the inorganic phase was calculated with an integrated X-ray powder diffraction software, PDXL (Rigaku Corp., Tokyo, Japan) using diffraction data collected by a fixed-time scanning mode at a step size of 0.02° and a counting time of 25 min/° using Si (NIST 640d) as an internal standard. Chemical composition of the sf-bone granules before and after hydrothermal treatment were measured by the ion chromatography using high-performance liquid chromatograph system (LC10A series, Shimadzu Co., Kyoto, Japan) consisted of a SCL-10A system controller, a LC-10 CE pump, a SIL-10A auto-injector, a CTO 10A column oven, and a CDD-6A conductivity detector linked to a Chromato-PRO data integrator (Run Time Co., Kanagawa, Japan). The sf-bone granules were dissolved into 0.1 mol/L nitric acid and diluted 10 times with ion-exchanged water. Amounts of cations, Ca and Mg, was measured using a
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 5. Powder XRD patterns of sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) ((a)–(d)) and (NH4)H2PO4 (pH 4.0) ((e)–(h)) aqueous solutions at various temperatures for 3 days. Listed pH values indicated those of reaction solutions after 3-day treatment.
Fig. 6. Solubility of calcite in water [22] and transformation rate of calcite to β-TCP after hydrothermal treatment for 3 days as a function of water temperature.
cationic column, Shodexs IC YS-50 (Showa Denko, Tokyo, Japan) with eluting solution of 4.0 mmol/L methanesulfonic acid at a flow rate of 0.65 mL/min, and those of anion, PO4, was measured using an anionic column, Shim-Pack IC-A1 (Shimadzu Co., Kyoto, Japan) with a mixed aqueous solution of 6.0 mmol/L boric acid, 18.0 mmol/L D(-)-mannitol and 7.5 mmol/L tris-(hydroxymethyl)aminomethane at a flow rate of 0.5 mL/min.
3. Results and discussion Fig. 1 shows morphologies of the raw sf-bone granules. Nakedeye observation, Fig. 1-(a), showed that they have irregular shapes
with 1 4 mm in size. Interconnected porous structure with approximately 10 50 mm of pore size and the smooth feature of pore wall were observed with an FE-SEM (Fig. 1-(b), (c)). Calcium, magnesium, carbon and oxygen were detected by the EDX analysis. The Mg content of the raw sf-bone determined by the ion chromatography was 1.32 70.04 mmol/g. All diffraction peaks in the powder XRD pattern of the raw sf-bone shown in Fig. 2 were assigned to those of calcite, ICDD-5-586, and were shifted to higher diffraction angle, which means the lattice is shrunk. In fact, the lattice parameters of the raw sf-bone were a ¼4.9331(6) and c¼16.811(5) as shown in the first row of Table 1, which were smaller than those of calcite in ICDD-5-586. This lattice shrinkage was caused by the exchange of Ca2 þ with Mg2 þ , which has smaller ionic radius than Ca. Fig. 3 shows FE-SEM images of the sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h, 1 day, 3 days and 7 days. Porous structure of sf-bone was maintained even after the hydrothermal treatment for 7 days (Figs. 1-(b) and 3-(a)–(d)). At higher magnification, the aggregations of fine crystals less than 1 mm in size were observed (Fig. 3(e)–(h)). Although the surface of the sf-bone treated for 1 h showed a rough feature with some pores, that treated for more than 3 days showed uniform feature. Fig. 4 shows XRD patterns of the sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h, 1 day, 3 days or 7 days. Main inorganic phase of the 1-hour treated sf-bone was calcite and the other minor phase was β-TCP. Calcite peaks were gradually decreased with the treatment time, and it became a β-TCP single phase by treatment for 1 day or longer. Main crystal phases, Mg contents and lattice parameters of the sf-bone before and after hydrothermal treatment were summarized in Table 1. The Mg contents showed no significant differences between the sf-bone before and after hydrothermal treatment. Lattice parameters of βTCP in the sf-bone after hydrothermal treatment were smaller than those of β-TCP in ICDD-9-169 but very similar to those of Mg-
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 7. FE-SEM images of sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) ((a)–(d)) and (NH4)H2PO4 (pH 4.0) ((e)–(h)) aqueous solutions at various temperatures for 3 days.
containing β-TCP, Ca2.71Mg0.29(PO4)2 [20]. These results indicated that Mg-containing calcite, sf-bone, was converted to Mg-containing β-TCP with maintaining its microporous structure by 1 day or longer hydrothermal treatment with (NH4)2HPO4 aqueous
solution at 200 °C. Fig. 5 shows XRD patterns of the sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) or (NH4)H2PO4 (pH 4.0) aqueous solutions at various temperatures for 3 days. Main inorganic phase of the sf-bone after treated at 60 °C and pH
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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8.0 was calcite which is attributed to the raw sf-bone, and the other phase was apatite as shown in Fig. 5-(a). The main phase was still calcite for the sf-bone treated at 80 and 100 °C and the other phase was β-TCP (Fig. 5-(b), (c)). According to previous report, calcite was converted to HAp based on dissolution–reprecipitation process by a hydrothermal treatment in the aqueous solutions of phosphate salt at neutral or weak basic condition [21], i.e., release of Ca2 þ , Mg2 þ and CO32– by dissolution of calcite increased supersaturation for most stable calcium phosphate in neutral and weak basic condition, HAp. Thus, first step of the process could be dissolution of Mg-containing calcite and formation of HAp in neutral and weak basic condition; however, presence of Mg2 þ inhibited crystal growth of HAp and stabilized β-TCP even in aqueous solution. Accordingly, low temperature treatment, which could not promote crystal growth of HAp, allowed forming low crystalline HAp as the following reaction. 10CaCO3 þ 6(NH4)2HPO4 þ 2H2 -Ca10(PO4)6(OH)2 þ6(NH4)2CO3 þ4H2CO3 With increasing in the treatment temperature, under the condition that inhibit crystal growth of HAp, conversion of Mg-containing calcite to β-TCP occurred preferentially as the following reaction, even the solution pH after treatment became more basic, i.e., much preferable condition for HAp formation in comparison to β-TCP formation, than the initial pH (Fig. 5-(a)–(c)). 3(Ca, Mg)CO3 þ2(NH4)2HPO4 -2(Ca, Mg)3(PO4)2 þ2(NH4)2CO3 þ 2H2CO3 In addition, a fast dissolution-reprecipitation process at 200 °C could form rough surface due to differences of density between calcite, 2.71, and β-TCP, 3.07, as shown in Fig. 2-(e). Pores in the rough surface were gradually filled with newly formed β-TCP to be homogeneous surface with increasing in treatment time. The transformation of the sf-bone to calcium phosphate had not been completed by the treatment for 3 days at a treatment temperature lower than 100 °C. Remaining phosphate ion in the solution was precipitated as magnesium ammonium phosphates, NH4Mg(PO4) 6H2O and NH4Mg(PO4) H2O. Same tendency for β-TCP formation was observed in treatment under acidic conditions (Fig. 5-(f)-(h)) whereas dicalcium phosphate dihydrate (DCPD) and octacalcium phosphate (OCP) were detected in the sf-bone after treated at 60 °C (Fig. 5-(e)) instead of low crystalline HAp, because DCPD and OCP are more stable than HAp in acidic pH. Fig. 6 shows solubility of calcite [22] and transformation rate of calcite to β-TCP, determined from the peak intensity ratio of 02 10 diffraction of β-TCP and 104 diffraction of calcite, at 3 days as a function of treatment temperature. The transformation rates for the samples treated in (NH4)H2PO4 aq (pH 4.0) were higher than those in (NH4)2HPO4 aq (pH 8.0) at 80, 100 and 160 °C. As mentioned above, transformation reaction of calcite to β-TCP is the dissolution-reprecipitation process; therefore, it was dominated by both calcite–dissolution and calcium phosphate–formation rates in aqueous solution, that depend upon their solubilities. Influence of pH in reaction rate could be explained by solubility of calcite in different pH, higher in acidic and lower in basic pHs. The lower transformation rates at 100 °C in both solutions than those at 80 °C could be explained from a negative temperature gradient in solubility of calcite (Fig. 6). Higher concentrations of PO43 and Ca2 þ due to calcite dissolution at 80 °C resulted in faster calcium phosphates precipitates due to higher supersaturation even a negative temperature gradient in calcium phosphate solubility. Thus, the lower transformation rate at 100 °C than that at 80 °C was attributed to the lower solubility of at 100 °C than that at 80 °C.
Although the solubility of calcite at 200 °C was expected to be significantly low, calcite was completely converted to β-TCP due to higher reaction rate because higher formation rate of calcium phosphate and activity of phosphate ions could become ratecontrolling factors at higher temperature. Fig. 7 shows FE-SEM images of sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) and (NH4)H2PO4 (pH 4.0) aqueous solutions at various temperatures for 3 days. Scale-like crystals, estimated as low crystalline apatite from powder XRD, were deposited to plug micropores of the sf-bone, on the sf-bone treated at 60 °C in (NH4)2HPO4 aq (Fig. 7-(a)) for 3 days. However, microporous structure of the sf-bone granule was maintained for the sf-bone after treatment at 80 °C or higher (Fig. 7-(b)–(d)). Spherical aggregates of spindle-shaped β-TCP crystals less than 1 mm in size were observed for the sf-bones treated at 80 and 100 °C (Fig. 7-(b), (c)) and uniform deposition of small crystals was observed at 200 °C (Fig. 7-(d)). The similar morphological change was observed for the sf-bones treated under acidic condition in (NH4)H2PO4 aq except for that treated at 60 °C. It revealed small pores on the surface of sf-bone that might be formed by dissolution of calcite.
4. Conclusion Starfish mineral was calcite form calcium carbonate, in which Mg2 þ was incorporated, and was irregular shaped granules with micropores of 10 50 mm in size. The granules converted to Mgcontaining β-TCP with maintaining its microporous structure by 1 day or longer hydrothermal treatment with (NH4)2HPO4 aqueous solution at 200 °C. The morphologies and crystal phases of the granules after hydrothermal treatment depended on pHs and temperatures during the conversion and they were explained by both reaction rate of calcium phosphate formation from solution and dissolution rate of calcite. The β-TCP with interconnected micropores was prepared using starfish derived calcium carbonate as a precursor and would be porous bone graft with both microand macropores due to the inter-granules hollow.
Acknowledgements A part of this study was financially supported by Japanese association for marine biology and revitalizing a local community by the development of new materials with sea urchin shells, the program for a proportion of practical uses with fish industry waste’s resources, Shakotan-cho, Hokkaido, Japan.
References [1] M. Sakamoto, T. Matsumoto, Development and evaluation of superporous ceramics bone tissue scaffold materials with triple pore structure a) hydroxyapatite, b) beta-tricalcium phosphate, in: H. Tal (Ed.), Bone Regeneration, InTech, Rijeka, Croatia, 2012, pp. 301–320. [2] H. Morisue, M. Matsumoto, K. Chiba, H. Matsumoto, Y. Toyama, M. Aizawa, N. Kanzawa, T.J. Fujimi, H. Uchida, I. Okada, Novel apatite fiber scaffolds can promote three-dimensional proliferation of osteoblasts in rodent bone regeneration models, J. Biomed. Mater. Res. 90A (2009) 811–818. [3] A. Uchida, S. Nade, E. McCartney, W. Ching, Bone ingrowth into three different porous ceramics implanted into the tibia of rats and rabbits, J. Orthop. Res. 3 (1985) 65–77. [4] D.M. Liu, Fabrication of hydroxyapatite ceramic with controlled porosity, J. Mater. Sci. Mater. Med. 8 (1997) 227–232. [5] N.O. Engin, A.C. Tas, Manufacture of macroporous calcium hydroxyapatite bioceramics, J. Eur. Ceram. Soc. 19 (1999) 2569–2572. [6] A.M. Le Ray, H. Gautier, J.M. Bouler, P. Weiss, C. Merle, A new technological procedure using sucrose as porogen compound to manufacture porous biphasic calcium phosphate ceramics of appropriate micro- and macrostructure, Ceram. Int. 36 (2010) 93–101.
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
A. Takeuchi et al. / Ceramics International ∎ (∎∎∎∎) ∎∎∎–∎∎∎ [7] J. Tian, J. Tian, Preparation of porous hydroxyapatite, J. Mater. Sci. 36 (2001) 3061–3066. [8] X. Miao, Y. Hu, J. Liu, A.P. Wong, Porous calcium phosphate ceramics prepared by coating polyurethane foams with calcium phosphate cements, Mater. Lett. 58 (2004) 397–402. [9] M.L. Munar, K. Udoh, K. Ishikawa, S. Matsuya, M. Nakagawa, Effects of sintering temperature over 1300 °C on the physical and compositional properties of porous hydroxyapatite foam, Dent. Mater. J. 25 (2006) 51–58. [10] P. Sepulveda, J.G.P. Binner, S.O. Rogero, O.Z. Higa, J.C. Bressiani, Production of porous hydroxyapatite by the gel-casting of foams and cytotoxic evaluation, J. Biomed. Mater. Res. 50 (2000) 27–34. [11] N.O. Engin, A.C. Tas, Preparation of porous Ca10(PO4)6(OH)2 and β-Ca3(PO4)2 bioceramics, J. Am. Ceram. Soc. 83 (2000) 1581–1584. [12] H.R. Ramay, M. Zhang, Preparation of porous hydroxyapatite scaffolds by combination of the gel-casting and polymer sponge methods, Biomaterials 24 (2003) 3293–3302. [13] E. Saiz, L. Gremillard, G. Menendez, P. Miranda, K. Gryn, A.P. Tomsia, Preparation of porous hydroxyapatite scaffolds, Mat. Sci. Eng. C 27 (2007) 546–550. [14] S. Tarafder, V.K. Balla, N.M. Davies, A. Bandyopadhyay, S. Bose, Microwavesintered 3D printed tricalcium phosphate scaffolds for bone tissue engineering, J. Tissue Eng. Regen. Med. 7 (2013) 631–641.
7
[15] D.M. Roy, S.K. Linnehan, Hydroxyapatite formed from coral skeletal carbonate by hydrothermal exchange, Nature 247 (1974) 220–222. [16] J. Hu, J.J. Russell, B. Ben-Nissan, Production and analysis of hydroxyapatite from Australian corals via hydrothermal process, J. Mater. Sci. Lett. 20 (2001) 85–87. [17] Y. Xu, D. Wang, L. Yang, H. Tang, Hydrothermal conversion of coral into hydroxyapatite, Mater. Charact. 47 (2001) 83–87. [18] S. Jinawath, D. Polchai, M. Yoshimura, Low-temperature, hydrothermal transformation of aragonite to hydroxyapatite, Mat. Sci. Eng. C 22 (2002) 35–39. [19] R.B. Emlet, Echinoderm calcite: a mechanical analysis from larval spicules, Biol. Bull. 163 (1982) 264–275. [20] L.W. Schroeder, B. Dickens, W.E. Brown, Crystallographic studies of the role of Mg as a stabilizing impurity in β-Ca3(PO4)2. II. Refinement of Mg-containing βCa3(PO4)2, J. Solid State Chem. 22 (1977) 253–262. [21] M. Yoshimura, P. Sujaridworakun, F. Koh, T. Fujiwara, D. Pongkao, A. Ahniyaz, Hydrothermal conversion of calcite crystals to hydroxyapatite, Mater. Sci. Eng. C 24 (2004) 521–525. [22] L.N. Plummer, E. Busenberg, The solubilities of calcite, aragonite and vaterite in CO2-H2O solutions between 0 and 90 °C, and an evaluation of the aqueous model for the system CaCO3-CO2-H2O, Geochim. Cosmochim. Acta 46 (1982) 1011–1040.
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Ceramics International journal homepage: www.elsevier.com/locate/ceramint
Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor Akari Takeuchi a,n, Tomohito Tsuge a, Masanori Kikuchi b a b
Department of Chemistry, Faculty of Science, Shinshu University, 3-1-1, Asahi, Matsumoto, Nagano 390-8621, Japan National Institute for Materials Science, 1-1, Namiki, Tsukuba, Ibaraki 305-0044, Japan
art ic l e i nf o
a b s t r a c t
Article history: Received 31 May 2016 Accepted 27 June 2016
Porous β-tricalcium phosphate (β-TCP) was successfully prepared from starfish-derived calcium carbonate (sf-bone) under several hydrothermal conditions. The sf-bone, obtained from Patiria Pectinifera by bleaching to remove organic substances, was Mg-containing calcite granules with an interconnected microporous structure of approximately 10 50 mm of pore, and was hydrothermally treated with ammonium phosphate aqueous solutions at various pHs and temperatures. The sf-bone was converted to Mg-containing β-TCP with maintaining its microporous structure by the hydrothermal treatment for 1 day or longer in (NH4)2HPO4 aqueous solution at 200 °C. This conversion was based on dissolutionreprecipitation process of Mg-containing calcite in the phosphate salt aqueous solution. Thus, conditions during the conversion, pH and temperature, affected the morphologies and crystal phases of sf-bone after the treatment depended upon both calcite dissolution and calcium phosphate-formation rates. & 2016 Published by Elsevier Ltd and Techna Group S.r.l.
Keywords: β-tricalcium phosphate Porous calcium phosphate Calcium carbonate Hydrothermal treatment
1. Introduction Although bone is a living tissue and has macropores for cell penetration and micropores for transportation of nutrients and body fluids, micropores in bioactive bone filling porous ceramics, hydroxyapatite (HAp, Ca10(PO4)6(OH)2) and β-tricalcium phosphate (β-TCP, β-Ca3(PO4)2), had not been considered enough. In fact, presence of macropores, more than 100 mm in diameter, in these ceramics has achieved sufficient clinical result in their limited applications with their good cell and bone tissue penetrations. However, in recent situations to expand applications of these bioactive porous ceramics to the cell scaffold in the regenerative medicine, the importance of their micro-pores have been considered to enable cell viability as well as to enable faster bone formation [1,2]. Many fabrication techniques for porous ceramics from synthetic calcium phosphates have been documented, e.g., by using burnable porogens [3–6] or polyurethane foams [7–9], by gelcasting methods [10–12] and by additive manufacturing [13,14], etc. Usage of porognes or polyurethane foams lead insufficient pore wall strength due to microcracks formed by their expansions caused by heating and following their vaporization. Thus, these methods showed drawbacks in mechanical strength and operability if they have sufficient pore interconnectivity. Gelcastings n
Corresponding author. E-mail address: [email protected] (A. Takeuchi).
with a foaming agent and appropriate gelation agent seemed to be the best porous ceramics in the traditional way; however, they can only control very well in a spherical macroporous structure, which is not similar to that of bone. Even additive manufacturing is a promising method to control of multi-scale structure, it still under investigation to control microporous structure for ceramics. Recently, tri-scale porous bioceramics, Apaceram-AXs, HAp, and Superpores, β-TCP, were commercialized by HOYA Technosurgical Co.; however, their macroporous structure is still spherical, and the size of micropores is less than 10 mm, which is generally enough for water penetration but is not optimized for in vivo environment. Further, porous HAp with micro- and macropores by sintering apatite fibers showed good bone formation as described above, but is very weak. In sum, porous ceramics of calcium phosphates with micro- and macropores fabricated from their synthetic powders faced on processing difficulties to control their porous structure. Contrarily, HAp converted from coralline mineral had success with the interconnected macroporous structure similar to cancellous bone [15–18]. Coralline mineral is porous calcium carbonate (aragonite or calcite) with pore sizes in the ranges of 150– 500 mm. Roy and Linnehan were firstly reported the hydrothermal method to convert coral calcium carbonate to HAp with a maintenance of the porous structure [15]. This porous HAp is called coralline apatite and commercially available bone graft in the United States as ProOsteons. Although it shows high affinity to bone and has cancellous bone-like structure, it does not have micropores. The use of coralline minerals has also drawbacks
http://dx.doi.org/10.1016/j.ceramint.2016.06.183 0272-8842/& 2016 Published by Elsevier Ltd and Techna Group S.r.l.
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 1. Morphologies of sf-bone harvested from Patiria pectinifera. (a): Naked-eye image. (b), (c): FE-SEM images at lower and higher magnifications, respectively.
Irregular shapes of the granules would result in macroporous structure due to the inter-granules hollow after packed into bone defect. Therefore, the feasibility of starfish-derived calcite to be a source material to prepare porous calcium phosphate was investigated in the present study. Porous calcium carbonates obtained from the starfish, Patiria Pectinifera harvested from oceans around Japan, were hydrothermally treated with ammonium phosphate aqueous solutions at various pHs and temperatures, and effects of pHs and temperatures on the transformation of starfish derived porous calcium carbonate to calcium phosphate were investigated.
2. Materials and methods
Fig. 2. Powder XRD pattern of sf-bone harvested from Patiria pectinifera.
associated with the harvest of corals from the sea, i.e., high cost due to harvesting corals from sea and most importantly, decreasing of corals strongly affect to global environment including global warming because of carbonate reservoir role of corals. Considering marine environment, utilization of marine wastes could be better than that of marine resources that are important for the environment. Starfishes are generally by-caught in net fisheries and caught by control programs of marine environments, and are a marine waste. Starfish mineral is known as Mg2 þ containing calcite granules [19], and they have interconnected microporous structure of several tens micrometers in pore diameter.
2.1. Preparation of porous calcium phosphate P. Pectinifera, one of starfish species, was used to obtain porous calcium carbonates for a precursor material of porous calcium phosphate. Organic substances of the starfish was removed by soaking it in a domestic bleach (approximately 6 vol% sodium hypochlorite aqueous solution, Haiters, Kao Co., Tokyo, Japan) overnight. The porous granules of calcium carbonate (sf-bone) obtained were then filtered, rinsed with ion-exchanged water for 5 times and dried at 60 °C for 24 h. One point five grams of sf-bone granules and 20 mL of 0.5 mol/ L (NH4)2HPO4 (pH 8.0) or (NH4)H2PO4 (pH 4.0) aqueous solution were put into a stainless steel autoclave at a filling ratio of 80% in volume and hydrothermally treated at 60, 80, 100 or 200 °C for 1 h,
Table 1 Main crystal phases, Mg contents and lattice parameters of sf-bones before and after hydrothermal treatment. Treatment period
Non treated 1h 1 day 3 days 7 days Calcite* β-TCP** Mg-containing β-TCP[20] * **
Main crystal phase
Calcite Calcite þ β-TCP β-TCP β-TCP β-TCP Calcite β-TCP β-TCP
Mg content /mmol g 1
1.32 7 0.04 – 1.28 7 0.08 1.217 0.09 1.197 0.20 – – –
Mg/(Ca þ Mg) molar ratio
0.1397 0.003 – 0.1417 0.001 0.1427 0.001 0.1427 0.002 – 0 0.29
(Ca þ Mg)/P molar ratio
– – 1.54 7 0.04 1.50 7 0.03 1.497 0.01 – 1.50 1.50
Lattice parameter /Å a
c
4.9331(6)
16.811(5)
10.330(8) 10.331(14) 10.334(3) 4.989 10.429 10.337(1)
37.14(4) 37.14(6) 37.117(7) 17.062 37.38 37.068(4)
ICDD-5-586. ICDD-9-169.
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 3. FE-SEM images of sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h ((a), (e)), 1 day ((b), (f)), 3 days ((c), (g)) and 7 days ((d), (h)). (a)–(d): Images at lower magnification. (e)–(h): Images at higher magnification.
1 day, 3 days and 7 days. The samples obtained were rinsed with ion-exchanged water for 10 times and dried at 60 °C for 24 h. 2.2. Characterization of porous calcium phosphate
Fig. 4. Powder XRD patterns of sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h (a), 1 day (b), 3 days (c) and 7 days (d).
Morphologies of the sf-bone granules before and after hydrothermal treatment were observed with a field emission-scanning electron microscope (FE-SEM, JSM-7600F, JEOL Ltd., Tokyo, Japan) equipped with an energy dispersive X-ray spectroscope (EDX, X– MaxN, Oxford Instruments plc., Oxfordshire, United Kingdom) at an accelerating voltage of 15 kV. Inorganic phases of the sf-bone granules before and after hydrothermal treatment were identified by powder X-ray diffractometry (XRD, Ultima IV, Rigaku Corp., Tokyo, Japan) using counter-monochromatized CuKα radiation generated at 40 kV and 40 mA by a continuous scanning mode at a step size of 0.02° and a scanning rate of 2.00°/min. Lattice parameters of the inorganic phase was calculated with an integrated X-ray powder diffraction software, PDXL (Rigaku Corp., Tokyo, Japan) using diffraction data collected by a fixed-time scanning mode at a step size of 0.02° and a counting time of 25 min/° using Si (NIST 640d) as an internal standard. Chemical composition of the sf-bone granules before and after hydrothermal treatment were measured by the ion chromatography using high-performance liquid chromatograph system (LC10A series, Shimadzu Co., Kyoto, Japan) consisted of a SCL-10A system controller, a LC-10 CE pump, a SIL-10A auto-injector, a CTO 10A column oven, and a CDD-6A conductivity detector linked to a Chromato-PRO data integrator (Run Time Co., Kanagawa, Japan). The sf-bone granules were dissolved into 0.1 mol/L nitric acid and diluted 10 times with ion-exchanged water. Amounts of cations, Ca and Mg, was measured using a
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 5. Powder XRD patterns of sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) ((a)–(d)) and (NH4)H2PO4 (pH 4.0) ((e)–(h)) aqueous solutions at various temperatures for 3 days. Listed pH values indicated those of reaction solutions after 3-day treatment.
Fig. 6. Solubility of calcite in water [22] and transformation rate of calcite to β-TCP after hydrothermal treatment for 3 days as a function of water temperature.
cationic column, Shodexs IC YS-50 (Showa Denko, Tokyo, Japan) with eluting solution of 4.0 mmol/L methanesulfonic acid at a flow rate of 0.65 mL/min, and those of anion, PO4, was measured using an anionic column, Shim-Pack IC-A1 (Shimadzu Co., Kyoto, Japan) with a mixed aqueous solution of 6.0 mmol/L boric acid, 18.0 mmol/L D(-)-mannitol and 7.5 mmol/L tris-(hydroxymethyl)aminomethane at a flow rate of 0.5 mL/min.
3. Results and discussion Fig. 1 shows morphologies of the raw sf-bone granules. Nakedeye observation, Fig. 1-(a), showed that they have irregular shapes
with 1 4 mm in size. Interconnected porous structure with approximately 10 50 mm of pore size and the smooth feature of pore wall were observed with an FE-SEM (Fig. 1-(b), (c)). Calcium, magnesium, carbon and oxygen were detected by the EDX analysis. The Mg content of the raw sf-bone determined by the ion chromatography was 1.32 70.04 mmol/g. All diffraction peaks in the powder XRD pattern of the raw sf-bone shown in Fig. 2 were assigned to those of calcite, ICDD-5-586, and were shifted to higher diffraction angle, which means the lattice is shrunk. In fact, the lattice parameters of the raw sf-bone were a ¼4.9331(6) and c¼16.811(5) as shown in the first row of Table 1, which were smaller than those of calcite in ICDD-5-586. This lattice shrinkage was caused by the exchange of Ca2 þ with Mg2 þ , which has smaller ionic radius than Ca. Fig. 3 shows FE-SEM images of the sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h, 1 day, 3 days and 7 days. Porous structure of sf-bone was maintained even after the hydrothermal treatment for 7 days (Figs. 1-(b) and 3-(a)–(d)). At higher magnification, the aggregations of fine crystals less than 1 mm in size were observed (Fig. 3(e)–(h)). Although the surface of the sf-bone treated for 1 h showed a rough feature with some pores, that treated for more than 3 days showed uniform feature. Fig. 4 shows XRD patterns of the sf-bone after hydrothermal treatment in (NH4)2HPO4 aqueous solution (pH 8.0) at 200 °C for 1 h, 1 day, 3 days or 7 days. Main inorganic phase of the 1-hour treated sf-bone was calcite and the other minor phase was β-TCP. Calcite peaks were gradually decreased with the treatment time, and it became a β-TCP single phase by treatment for 1 day or longer. Main crystal phases, Mg contents and lattice parameters of the sf-bone before and after hydrothermal treatment were summarized in Table 1. The Mg contents showed no significant differences between the sf-bone before and after hydrothermal treatment. Lattice parameters of βTCP in the sf-bone after hydrothermal treatment were smaller than those of β-TCP in ICDD-9-169 but very similar to those of Mg-
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
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Fig. 7. FE-SEM images of sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) ((a)–(d)) and (NH4)H2PO4 (pH 4.0) ((e)–(h)) aqueous solutions at various temperatures for 3 days.
containing β-TCP, Ca2.71Mg0.29(PO4)2 [20]. These results indicated that Mg-containing calcite, sf-bone, was converted to Mg-containing β-TCP with maintaining its microporous structure by 1 day or longer hydrothermal treatment with (NH4)2HPO4 aqueous
solution at 200 °C. Fig. 5 shows XRD patterns of the sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) or (NH4)H2PO4 (pH 4.0) aqueous solutions at various temperatures for 3 days. Main inorganic phase of the sf-bone after treated at 60 °C and pH
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8.0 was calcite which is attributed to the raw sf-bone, and the other phase was apatite as shown in Fig. 5-(a). The main phase was still calcite for the sf-bone treated at 80 and 100 °C and the other phase was β-TCP (Fig. 5-(b), (c)). According to previous report, calcite was converted to HAp based on dissolution–reprecipitation process by a hydrothermal treatment in the aqueous solutions of phosphate salt at neutral or weak basic condition [21], i.e., release of Ca2 þ , Mg2 þ and CO32– by dissolution of calcite increased supersaturation for most stable calcium phosphate in neutral and weak basic condition, HAp. Thus, first step of the process could be dissolution of Mg-containing calcite and formation of HAp in neutral and weak basic condition; however, presence of Mg2 þ inhibited crystal growth of HAp and stabilized β-TCP even in aqueous solution. Accordingly, low temperature treatment, which could not promote crystal growth of HAp, allowed forming low crystalline HAp as the following reaction. 10CaCO3 þ 6(NH4)2HPO4 þ 2H2 -Ca10(PO4)6(OH)2 þ6(NH4)2CO3 þ4H2CO3 With increasing in the treatment temperature, under the condition that inhibit crystal growth of HAp, conversion of Mg-containing calcite to β-TCP occurred preferentially as the following reaction, even the solution pH after treatment became more basic, i.e., much preferable condition for HAp formation in comparison to β-TCP formation, than the initial pH (Fig. 5-(a)–(c)). 3(Ca, Mg)CO3 þ2(NH4)2HPO4 -2(Ca, Mg)3(PO4)2 þ2(NH4)2CO3 þ 2H2CO3 In addition, a fast dissolution-reprecipitation process at 200 °C could form rough surface due to differences of density between calcite, 2.71, and β-TCP, 3.07, as shown in Fig. 2-(e). Pores in the rough surface were gradually filled with newly formed β-TCP to be homogeneous surface with increasing in treatment time. The transformation of the sf-bone to calcium phosphate had not been completed by the treatment for 3 days at a treatment temperature lower than 100 °C. Remaining phosphate ion in the solution was precipitated as magnesium ammonium phosphates, NH4Mg(PO4) 6H2O and NH4Mg(PO4) H2O. Same tendency for β-TCP formation was observed in treatment under acidic conditions (Fig. 5-(f)-(h)) whereas dicalcium phosphate dihydrate (DCPD) and octacalcium phosphate (OCP) were detected in the sf-bone after treated at 60 °C (Fig. 5-(e)) instead of low crystalline HAp, because DCPD and OCP are more stable than HAp in acidic pH. Fig. 6 shows solubility of calcite [22] and transformation rate of calcite to β-TCP, determined from the peak intensity ratio of 02 10 diffraction of β-TCP and 104 diffraction of calcite, at 3 days as a function of treatment temperature. The transformation rates for the samples treated in (NH4)H2PO4 aq (pH 4.0) were higher than those in (NH4)2HPO4 aq (pH 8.0) at 80, 100 and 160 °C. As mentioned above, transformation reaction of calcite to β-TCP is the dissolution-reprecipitation process; therefore, it was dominated by both calcite–dissolution and calcium phosphate–formation rates in aqueous solution, that depend upon their solubilities. Influence of pH in reaction rate could be explained by solubility of calcite in different pH, higher in acidic and lower in basic pHs. The lower transformation rates at 100 °C in both solutions than those at 80 °C could be explained from a negative temperature gradient in solubility of calcite (Fig. 6). Higher concentrations of PO43 and Ca2 þ due to calcite dissolution at 80 °C resulted in faster calcium phosphates precipitates due to higher supersaturation even a negative temperature gradient in calcium phosphate solubility. Thus, the lower transformation rate at 100 °C than that at 80 °C was attributed to the lower solubility of at 100 °C than that at 80 °C.
Although the solubility of calcite at 200 °C was expected to be significantly low, calcite was completely converted to β-TCP due to higher reaction rate because higher formation rate of calcium phosphate and activity of phosphate ions could become ratecontrolling factors at higher temperature. Fig. 7 shows FE-SEM images of sf-bone after hydrothermal treatment in (NH4)2HPO4 (pH 8.0) and (NH4)H2PO4 (pH 4.0) aqueous solutions at various temperatures for 3 days. Scale-like crystals, estimated as low crystalline apatite from powder XRD, were deposited to plug micropores of the sf-bone, on the sf-bone treated at 60 °C in (NH4)2HPO4 aq (Fig. 7-(a)) for 3 days. However, microporous structure of the sf-bone granule was maintained for the sf-bone after treatment at 80 °C or higher (Fig. 7-(b)–(d)). Spherical aggregates of spindle-shaped β-TCP crystals less than 1 mm in size were observed for the sf-bones treated at 80 and 100 °C (Fig. 7-(b), (c)) and uniform deposition of small crystals was observed at 200 °C (Fig. 7-(d)). The similar morphological change was observed for the sf-bones treated under acidic condition in (NH4)H2PO4 aq except for that treated at 60 °C. It revealed small pores on the surface of sf-bone that might be formed by dissolution of calcite.
4. Conclusion Starfish mineral was calcite form calcium carbonate, in which Mg2 þ was incorporated, and was irregular shaped granules with micropores of 10 50 mm in size. The granules converted to Mgcontaining β-TCP with maintaining its microporous structure by 1 day or longer hydrothermal treatment with (NH4)2HPO4 aqueous solution at 200 °C. The morphologies and crystal phases of the granules after hydrothermal treatment depended on pHs and temperatures during the conversion and they were explained by both reaction rate of calcium phosphate formation from solution and dissolution rate of calcite. The β-TCP with interconnected micropores was prepared using starfish derived calcium carbonate as a precursor and would be porous bone graft with both microand macropores due to the inter-granules hollow.
Acknowledgements A part of this study was financially supported by Japanese association for marine biology and revitalizing a local community by the development of new materials with sea urchin shells, the program for a proportion of practical uses with fish industry waste’s resources, Shakotan-cho, Hokkaido, Japan.
References [1] M. Sakamoto, T. Matsumoto, Development and evaluation of superporous ceramics bone tissue scaffold materials with triple pore structure a) hydroxyapatite, b) beta-tricalcium phosphate, in: H. Tal (Ed.), Bone Regeneration, InTech, Rijeka, Croatia, 2012, pp. 301–320. [2] H. Morisue, M. Matsumoto, K. Chiba, H. Matsumoto, Y. Toyama, M. Aizawa, N. Kanzawa, T.J. Fujimi, H. Uchida, I. Okada, Novel apatite fiber scaffolds can promote three-dimensional proliferation of osteoblasts in rodent bone regeneration models, J. Biomed. Mater. Res. 90A (2009) 811–818. [3] A. Uchida, S. Nade, E. McCartney, W. Ching, Bone ingrowth into three different porous ceramics implanted into the tibia of rats and rabbits, J. Orthop. Res. 3 (1985) 65–77. [4] D.M. Liu, Fabrication of hydroxyapatite ceramic with controlled porosity, J. Mater. Sci. Mater. Med. 8 (1997) 227–232. [5] N.O. Engin, A.C. Tas, Manufacture of macroporous calcium hydroxyapatite bioceramics, J. Eur. Ceram. Soc. 19 (1999) 2569–2572. [6] A.M. Le Ray, H. Gautier, J.M. Bouler, P. Weiss, C. Merle, A new technological procedure using sucrose as porogen compound to manufacture porous biphasic calcium phosphate ceramics of appropriate micro- and macrostructure, Ceram. Int. 36 (2010) 93–101.
Please cite this article as: A. Takeuchi, et al., Preparation of porous β-tricalcium phosphate using starfish-derived calcium carbonate as a precursor, Ceramics International (2016), http://dx.doi.org/10.1016/j.ceramint.2016.06.183i
A. Takeuchi et al. / Ceramics International ∎ (∎∎∎∎) ∎∎∎–∎∎∎ [7] J. Tian, J. Tian, Preparation of porous hydroxyapatite, J. Mater. Sci. 36 (2001) 3061–3066. [8] X. Miao, Y. Hu, J. Liu, A.P. Wong, Porous calcium phosphate ceramics prepared by coating polyurethane foams with calcium phosphate cements, Mater. Lett. 58 (2004) 397–402. [9] M.L. Munar, K. Udoh, K. Ishikawa, S. Matsuya, M. Nakagawa, Effects of sintering temperature over 1300 °C on the physical and compositional properties of porous hydroxyapatite foam, Dent. Mater. J. 25 (2006) 51–58. [10] P. Sepulveda, J.G.P. Binner, S.O. Rogero, O.Z. Higa, J.C. Bressiani, Production of porous hydroxyapatite by the gel-casting of foams and cytotoxic evaluation, J. Biomed. Mater. Res. 50 (2000) 27–34. [11] N.O. Engin, A.C. Tas, Preparation of porous Ca10(PO4)6(OH)2 and β-Ca3(PO4)2 bioceramics, J. Am. Ceram. Soc. 83 (2000) 1581–1584. [12] H.R. Ramay, M. Zhang, Preparation of porous hydroxyapatite scaffolds by combination of the gel-casting and polymer sponge methods, Biomaterials 24 (2003) 3293–3302. [13] E. Saiz, L. Gremillard, G. Menendez, P. Miranda, K. Gryn, A.P. Tomsia, Preparation of porous hydroxyapatite scaffolds, Mat. Sci. Eng. C 27 (2007) 546–550. [14] S. Tarafder, V.K. Balla, N.M. Davies, A. Bandyopadhyay, S. Bose, Microwavesintered 3D printed tricalcium phosphate scaffolds for bone tissue engineering, J. Tissue Eng. Regen. Med. 7 (2013) 631–641.
7
[15] D.M. Roy, S.K. Linnehan, Hydroxyapatite formed from coral skeletal carbonate by hydrothermal exchange, Nature 247 (1974) 220–222. [16] J. Hu, J.J. Russell, B. Ben-Nissan, Production and analysis of hydroxyapatite from Australian corals via hydrothermal process, J. Mater. Sci. Lett. 20 (2001) 85–87. [17] Y. Xu, D. Wang, L. Yang, H. Tang, Hydrothermal conversion of coral into hydroxyapatite, Mater. Charact. 47 (2001) 83–87. [18] S. Jinawath, D. Polchai, M. Yoshimura, Low-temperature, hydrothermal transformation of aragonite to hydroxyapatite, Mat. Sci. Eng. C 22 (2002) 35–39. [19] R.B. Emlet, Echinoderm calcite: a mechanical analysis from larval spicules, Biol. Bull. 163 (1982) 264–275. [20] L.W. Schroeder, B. Dickens, W.E. Brown, Crystallographic studies of the role of Mg as a stabilizing impurity in β-Ca3(PO4)2. II. Refinement of Mg-containing βCa3(PO4)2, J. Solid State Chem. 22 (1977) 253–262. [21] M. Yoshimura, P. Sujaridworakun, F. Koh, T. Fujiwara, D. Pongkao, A. Ahniyaz, Hydrothermal conversion of calcite crystals to hydroxyapatite, Mater. Sci. Eng. C 24 (2004) 521–525. [22] L.N. Plummer, E. Busenberg, The solubilities of calcite, aragonite and vaterite in CO2-H2O solutions between 0 and 90 °C, and an evaluation of the aqueous model for the system CaCO3-CO2-H2O, Geochim. Cosmochim. Acta 46 (1982) 1011–1040.
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