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Progress and perspectives of metal-ion-substituted hydroxyapatite for bone tissue engineering: comparison with hydroxyapatite

Journal of the Korean Ceramic Society volume 59, pages 271–288 (2022)Cite this article

Abstract

Hydroxyapatite (HA) is one of the most common bioceramics and is abundant in human bones. HA is composed of calcium phosphate, which is prevalent in biomedical processes, particularly bone formation, osteogenesis, and angiogenesis. As HA is one of the core materials that makes up the human body, there has been considerable research on methods of synthesizing HA while changing its properties by substituting various types of metal ions. In particular, previous studies have intensively investigated the size, crystallinities, and morphologies generated using various synthesis methods to change the characteristics of HA by substituting different metal ions. This review summarizes the findings of these studies on HA, including findings on the characteristics of HA in natural bone, methods of synthesizing HA, and findings on metal-ion-substituted HA. Furthermore, the characteristics and applications of HA that were investigated in previous studies are summarized, and the latest trends and perspectives on the future of the field are also presented.

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References

  1. Z. Tang, Y. Tan, Y. Ni, J. Wang, X. Zhu, Y. Fan, X. Chen, X. Yang, X. Zhang, Comparison of ectopic bone formation process induced by four calcium phosphate ceramics in mice. Mater. Sci. Eng. C 70, 1000–1010 (2017). https://doi.org/10.1016/j.msec.2016.06.097

    Article  CAS  Google Scholar 

  2. Y. Deng, Y. Yang, Y. Ma, K. Fan, W. Yang, G. Yin, Nano-hydroxyapatite reinforced polyphenylene sulfide biocomposite with superior cytocompatibility and in vivo osteogenesis as a novel orthopedic implant. RSC Adv. 7, 559–573 (2017). https://doi.org/10.1039/c6ra25526d

    Article  CAS  Google Scholar 

  3. J.H. Lee, G.S. Yi, J.W. Lee, D.J. Kim, Physicochemical characterization of porcine bone-derived grafting material and comparison with bovine xenografts for dental applications. J. Periodontal Implant Sci. 47, 388–401 (2017). https://doi.org/10.5051/jpis.2017.47.6.388

    Article  CAS  Google Scholar 

  4. T.H. Lim, J.R. Choi, D.Y. Lim, S.H. Lee, S.Y. Yeo, Preparation of fiber based binder materials to enhance the gas adsorption efficiency of carbon air filter. J. Nanosci. Nanotechnol. 15, 8034–8041 (2015). https://doi.org/10.1166/jnn.2015.11276

    Article  CAS  Google Scholar 

  5. L.F. Sukhodub, L.B. Sukhodub, A.D. Pogrebnjak, A. Turlybekuly, A. Kistaubayeva, I. Savitskaya, D. Shokatayeva, Effect of magnetic particles adding into nanostructured hydroxyapatite–alginate composites for orthopedics. J. Korean Ceram. Soc. 57, 557–569 (2020). https://doi.org/10.1007/s43207-020-00061-w

    Article  CAS  Google Scholar 

  6. B. Mohapatra, T.R. Rautray, Strontium-substituted biphasic calcium phosphate scaffold for orthopedic applications. J. Korean Ceram. Soc. 57, 392–400 (2020). https://doi.org/10.1007/s43207-020-00028-x

    Article  CAS  Google Scholar 

  7. C. Shuai, S. Li, S. Peng, P. Feng, Y. Lai, C. Gao, Biodegradable metallic bone implants. Mater. Chem. Front. 3, 544–562 (2019). https://doi.org/10.1039/c8qm00507a

    Article  CAS  Google Scholar 

  8. N. Strutynska, A. Malyshenko, N. Tverdokhleb, M. Evstigneev, L. Vovchenko, Y. Prylutskyy, N. Slobodyanik, U. Ritter, Design, characterization and mechanical properties of new Na+, CO32−-apatite/alginate/C60 fullerene hybrid biocomposites. J. Korean Ceram. Soc. 58, 422–429 (2021). https://doi.org/10.1007/s43207-020-00107-z

    Article  CAS  Google Scholar 

  9. J.W. Lee, S. Chae, S. Oh, S.H. Kim, K.H. Choi, M. Meeseepong, J. Chang, N. Kim, Y.H. Kim, N.E. Lee, J.H. Lee, J.Y. Choi, Single-chain atomic crystals as extracellular matrix-mimicking material with exceptional biocompatibility and bioactivity. Nano Lett. 18, 7619–7627 (2018). https://doi.org/10.1021/acs.nanolett.8b03201

    Article  CAS  Google Scholar 

  10. E. Saygili, E. Kaya, E. Ilhan-Ayisigi, P. Saglam-Metiner, E. Alarcin, A. Kazan, E. Girgic, Y.W. Kim, K. Gunes, G.G. Eren-Ozcan, D. Akakin, J.Y. Sun, O. Yesil-Celiktas, An alginate-poly(acrylamide) hydrogel with TGF-β3 loaded nanoparticles for cartilage repair: biodegradability, biocompatibility and protein adsorption. Int. J. Biol. Macromol. 172, 381–393 (2021). https://doi.org/10.1016/j.ijbiomac.2021.01.069

    Article  CAS  Google Scholar 

  11. J.H. Lee, I.H. Ko, S.H. Jeon, J.H. Chae, J.H. Chang, Micro-structured hydroxyapatite microspheres for local delivery of alendronate and BMP-2 carriers. Mater. Lett. 105, 136–139 (2013). https://doi.org/10.1016/j.matlet.2013.04.082

    Article  CAS  Google Scholar 

  12. H.G. Jung, D. Lee, S.W. Lee, I. Kim, Y. Kim, J.W. Jang, J.H. Lee, G. Lee, D.S. Yoon, Nanoindentation for monitoring the time-variant mechanical strength of drug-loaded collagen hydrogel regulated by hydroxyapatite nanoparticles. ACS Omega 6, 9269–9278 (2021). https://doi.org/10.1021/acsomega.1c00824

    Article  CAS  Google Scholar 

  13. M. Park, J.C. Pyun, J. Jose, Orientation and density control of proteins on solid matters by outer membrane coating: analytical and diagnostic applications. J. Pharm. Biomed. Anal. 147, 174–184 (2018). https://doi.org/10.1016/j.jpba.2017.07.043

    Article  CAS  Google Scholar 

  14. J.H. Kim, S.H. Kim, H.K. Kim, T. Akaike, S.C. Kim, Synthesis and characterization of hydroxyapatite crystals: a review study on the analytical methods. J. Biomed. Mater. Res. 62, 600–612 (2002). https://doi.org/10.1002/jbm.10280

    Article  CAS  Google Scholar 

  15. B. Cengiz, Y. Gokce, N. Yildiz, Z. Aktas, A. Calimli, Synthesis and characterization of hydroxyapatite nanoparticles. Colloids Surf. A Physicochem. Eng. Asp. 322, 29–33 (2008). https://doi.org/10.1016/j.colsurfa.2008.02.011

    Article  CAS  Google Scholar 

  16. G.B.C. Cardoso, A. Tondon, L.R.B. Maia, M.R. Cunha, C.A.C. Zavaglia, R.R. Kaunas, In vivo approach of calcium deficient hydroxyapatite filler as bone induction factor. Mater. Sci. Eng. C 99, 999–1006 (2019). https://doi.org/10.1016/j.msec.2019.02.060

    Article  CAS  Google Scholar 

  17. R.M.G. Rajapakse, W.P.S.L. Wijesinghe, M.M.M.G.P.G. Mantilaka, K.G. Chathuranga Senarathna, H.M.T.U. Herath, T.N. Premachandra, C.S.K. Ranasinghe, R.P.V.J. Rajapakse, M. Edirisinghe, S. Mahalingam, I.M.C.C.D. Bandara, S. Singh, Preparation of bone-implants by coating hydroxyapatite nanoparticles on self-formed titanium dioxide thin-layers on titanium metal surfaces. Mater. Sci. Eng. C 63, 172–184 (2016). https://doi.org/10.1016/j.msec.2016.02.053

    Article  CAS  Google Scholar 

  18. L. Chen, Z. Wu, Y. Zhou, L. Li, Y. Wang, Z. Wang, Y. Chen, P. Zhang, Biomimetic porous collagen/hydroxyapatite scaffold for bone tissue engineering. J. Appl. Polym. Sci. 134, 1–8 (2017). https://doi.org/10.1002/app.45271

    Article  CAS  Google Scholar 

  19. S.M. Lee, H.J. Byeon, B.H. Kim, J. Lee, J.Y. Jeong, J.H. Lee, J.H. Moon, C. Park, H. Choi, S.H. Lee, K.H. Lee, Flexible and implantable capacitive microelectrode for bio-potential acquisition. Biochip J. 11, 153–163 (2017). https://doi.org/10.1007/s13206-017-1304-y

    Article  CAS  Google Scholar 

  20. E. Boanini, M. Gazzano, A. Bigi, Ionic substitutions in calcium phosphates synthesized at low temperature. Acta Biomater. 6, 1882–1894 (2010). https://doi.org/10.1016/j.actbio.2009.12.041

    Article  CAS  Google Scholar 

  21. K. Sato, Mechanism of hydroxyapatite mineralization in biological systems. J. Ceram. Soc. Japan 115, 124–130 (2007). https://doi.org/10.2109/jcersj.115.124

    Article  CAS  Google Scholar 

  22. S.H. Han, J.U. Lee, K.M. Lee, Y.Z. Jin, H. Yun, G.H. Kim, J.H. Lee, Enhanced healing of rat calvarial defects with 3D printed calcium-deficient hydroxyapatite/collagen/bone morphogenetic protein 2 scaffolds. J. Mech. Behav. Biomed. Mater. 108, 103782 (2020). https://doi.org/10.1016/j.jmbbm.2020.103782

    Article  CAS  Google Scholar 

  23. M. Vallet-Regí, J.M. González-Calbet, Calcium phosphates as substitution of bone tissues. Prog. Solid State Chem. 32, 1–31 (2004). https://doi.org/10.1016/j.progsolidstchem.2004.07.001

    Article  CAS  Google Scholar 

  24. M. Sadat-Shojai, M.T. Khorasani, E. Dinpanah-Khoshdargi, A. Jamshidi, Synthesis methods for nanosized hydroxyapatite with diverse structures. Acta Biomater. 9, 7591–7621 (2013). https://doi.org/10.1016/j.actbio.2013.04.012

    Article  CAS  Google Scholar 

  25. A. Szcześ, L. Hołysz, E. Chibowski, Synthesis of hydroxyapatite for biomedical applications. Adv. Colloid Interface Sci. 249, 321–330 (2017). https://doi.org/10.1016/j.cis.2017.04.007

    Article  CAS  Google Scholar 

  26. J. Vecstaudza, M. Gasik, J. Locs, Amorphous calcium phosphate materials: formation, structure and thermal behaviour. J. Eur. Ceram. Soc. 39, 1642–1649 (2019). https://doi.org/10.1016/j.jeurceramsoc.2018.11.003

    Article  CAS  Google Scholar 

  27. J.M. Thomann, J.C. Voegel, P. Gramain, Kinetics of dissolution of calcium hydroxyapatite powder. III: pH and sample conditioning effects. Calcif Tissue Int. 46, 121–129 (1990). https://doi.org/10.1007/BF02556096

    Article  CAS  Google Scholar 

  28. L. Pighinelli, M. Kucharska, Chitosan-hydroxyapatite composites. Carbohydr. Polym. 93, 256–262 (2013). https://doi.org/10.1016/j.carbpol.2012.06.004

    Article  CAS  Google Scholar 

  29. D.W. Hutmacher, Scaffolds in tissue engineering bone and cartilage. Biomater. Silver Jubil. Compend. 21, 175–189 (2000). https://doi.org/10.1016/B978-008045154-1.50021-6

    Article  Google Scholar 

  30. K. Rezwan, Q.Z. Chen, J.J. Blaker, A.R. Boccaccini, Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27, 3413–3431 (2006). https://doi.org/10.1016/j.biomaterials.2006.01.039

    Article  CAS  Google Scholar 

  31. S.V. Dorozhkin, Calcium orthophosphates in nature, biology and medicine. Materials (Basel) 2, 399–498 (2009). https://doi.org/10.3390/ma2020399

    Article  CAS  Google Scholar 

  32. S.V. Dorozhkin, Calcium orthophosphates. J. Mater. Sci. 42, 1061–1095 (2007). https://doi.org/10.1007/s10853-006-1467-8

    Article  CAS  Google Scholar 

  33. L.C. Chow, Solubility of calcium phosphates. Monogr. Oral Sci. 18, 94–111 (2001). https://doi.org/10.1159/000061650

    Article  CAS  Google Scholar 

  34. R.I. Martin, P.W. Brown, Mechanical properties of hydroxyapatite formed at physiological temperature. J. Mater. Sci. Mater. Med. 6, 138–143 (1995). https://doi.org/10.1007/BF00120289

    Article  CAS  Google Scholar 

  35. A. Gortemaker, J.A. Jansen, NHJC, Critical reviews in oral biology & medicine: aging and bone. J. Dent. Res. 89, 1333–1348 (2010). https://doi.org/10.1177/0022034510377791

    Article  CAS  Google Scholar 

  36. C.H. Turner, Bone strength: current concepts. Ann. N. Y. Acad. Sci. 1068, 429–446 (2006). https://doi.org/10.1196/annals.1346.039

    Article  Google Scholar 

  37. S.H. Ralston, Bone structure and metabolism. Medicine (United Kingdom) 45, 560–564 (2017). https://doi.org/10.1016/j.mpmed.2017.06.008

    Article  Google Scholar 

  38. K.A. Hing, S.M. Best, W. Bonfield, Characterization of porous hydroxyapatite. J. Mater. Sci. Mater. Med. 10, 135–145 (1999). https://doi.org/10.1023/A:1008929305897

    Article  CAS  Google Scholar 

  39. A.E. Jakus, A.L. Rutz, R.N. Shah, Advancing the field of 3D biomaterial printing. Biomed. Mater. (2016). https://doi.org/10.1088/1748-6041/11/1/014102

    Article  Google Scholar 

  40. A. Liu, G.H. Xue, M. Sun, H.F. Shao, C.Y. Ma, Q. Gao, Z.R. Gou, S.G. Yan, Y.M. Liu, Y. He, 3D printing surgical implants at the clinic: a experimental study on anterior cruciate ligament reconstruction. Sci. Rep. 6, 1–13 (2016). https://doi.org/10.1038/srep21704

    Article  CAS  Google Scholar 

  41. K.A. Hing, B. Annaz, S. Saeed, P.A. Revell, T. Buckland, Microporosity enhances bioactivity of synthetic bone graft substitutes. J. Mater. Sci. Mater. Med. 16, 467–475 (2005). https://doi.org/10.1007/s10856-005-6988-1

    Article  CAS  Google Scholar 

  42. C. Kim, J.W. Lee, J.H. Heo, C. Park, D.H. Kim, G.S. Yi, H.C. Kang, H.S. Jung, H. Shin, Lee JH Natural bone-mimicking nanopore-incorporated hydroxyapatite scaffolds for enhanced bone tissue regeneration. Biomater Res. 26, 7 (2022). https://doi.org/10.1186/s40824-022-00253-x

    Article  CAS  Google Scholar 

  43. G. Tripathi, B. Basu, A porous hydroxyapatite scaffold for bone tissue engineering: physico-mechanical and biological evaluations. Ceram. Int. 38, 341–349 (2012). https://doi.org/10.1016/j.ceramint.2011.07.012

    Article  CAS  Google Scholar 

  44. J. Chen, Z. Wang, Z. Wen, S. Yang, J. Wang, Q. Zhang, Controllable self-assembly of mesoporous hydroxyapatite. Colloids Surf. B Biointerfaces 127, 47–53 (2015). https://doi.org/10.1016/j.colsurfb.2014.12.055

    Article  CAS  Google Scholar 

  45. F. He, Y. Yang, J. Ye, Tailoring the pore structure and property of porous biphasic calcium phosphate ceramics by NaCl additive. Ceram. Int. 42, 14679–14684 (2016). https://doi.org/10.1016/j.ceramint.2016.06.092

    Article  CAS  Google Scholar 

  46. S. Yunoki, T. Ikoma, A. Monkawa, K. Ohta, M. Kikuchi, S. Sotome, K. Shinomiya, J. Tanaka, Control of pore structure and mechanical property in hydroxyapatite/collagen composite using unidirectional ice growth. Mater. Lett. 60, 999–1002 (2006). https://doi.org/10.1016/j.matlet.2005.10.064

    Article  CAS  Google Scholar 

  47. P. Habibovic, M.C. Kruyt, M.V. Juhl, S. Clyens, R. Martinetti, L. Dolcini, N. Theilgaard, C.A. Van Blitterswijk, Comparative in vivo study of six hydroxyapatite-based bone graft substitutes. J. Orthop. Res. 26, 1363–1370 (2008). https://doi.org/10.1002/jor.20648

    Article  CAS  Google Scholar 

  48. J.R. Woodard, A.J. Hilldore, S.K. Lan, C.J. Park, A.W. Morgan, J.A.C. Eurell, S.G. Clark, M.B. Wheeler, R.D. Jamison, A.J. Wagoner Johnson, The mechanical properties and osteoconductivity of hydroxyapatite bone scaffolds with multi-scale porosity. Biomaterials 28, 45–54 (2007). https://doi.org/10.1016/j.biomaterials.2006.08.021

    Article  CAS  Google Scholar 

  49. J.A. Juhasz, S.M. Best, W. Bonfield, Preparation of novel bioactive nano-calcium phosphate-hydrogel composites. Sci. Technol. Adv. Mater. (2010). https://doi.org/10.1088/1468-6996/11/1/014103

    Article  Google Scholar 

  50. C.S. Ciobanu, S.L. Iconaru, I. Pasuk, B.S. Vasile, A.R. Lupu, A. Hermenean, A. Dinischiotu, D. Predoi, Structural properties of silver doped hydroxyapatite and their biocompatibility. Mater. Sci. Eng. C 33, 1395–1402 (2013). https://doi.org/10.1016/j.msec.2012.12.042

    Article  CAS  Google Scholar 

  51. F.J. O’Brien, Biomaterials & scaffolds for tissue engineering. Mater. Today 14, 88–95 (2011). https://doi.org/10.1016/S1369-7021(11)70058-X

    Article  CAS  Google Scholar 

  52. J. Biggemann, P. Müller, D. Köllner, S. Simon, P. Hoffmann, P. Heik, J.H. Lee, T. Fey, Hierarchical surface texturing of hydroxyapatite ceramics: influence on the adhesive bonding strength of polymeric polycaprolactone. J. Funct. Biomater. (2020). https://doi.org/10.3390/JFB11040073

    Article  Google Scholar 

  53. A. Jaafar, C. Hecker, P. Árki, Y. Joseph, Sol-gel derived hydroxyapatite coatings for titanium implants: a review. Bioengineering 7, 1–23 (2020). https://doi.org/10.3390/bioengineering7040127

    Article  CAS  Google Scholar 

  54. L. Gritsch, M. Maqbool, V. Mouriño, F.E. Ciraldo, M. Cresswell, P.R. Jackson, C. Lovell, A.R. Boccaccini, Chitosan/hydroxyapatite composite bone tissue engineering scaffolds with dual and decoupled therapeutic ion delivery: copper and strontium. J. Mater. Chem. B 7, 6109–6124 (2019). https://doi.org/10.1039/c9tb00897g

    Article  CAS  Google Scholar 

  55. L.L. Hench, Bioceramics. J. Am. Ceram. Soc. 81, 1705–1728 (1998)

    Article  CAS  Google Scholar 

  56. A.F. Ali, Z.A. Alrowaili, E.M. El-Giar, M.M. Ahmed, A.M. El-Kady, Novel green synthesis of hydroxyapatite uniform nanorods via microwave-hydrothermal route using licorice root extract as template. Ceram. Int. 47, 3928–3937 (2021). https://doi.org/10.1016/j.ceramint.2020.09.256

    Article  CAS  Google Scholar 

  57. J. Indira, K.S. Malathi, Comparison of template mediated ultrasonic and microwave irradiation method on the synthesis of hydroxyapatite nanoparticles for biomedical applications. Mater. Today Proc. (2021). https://doi.org/10.1016/j.matpr.2021.03.028

    Article  Google Scholar 

  58. J.S. Earl, D.J. Wood, S.J. Milne, Hydrothermal synthesis of hydroxyapatite. J. Phys. Conf. Ser. 26, 268–271 (2006). https://doi.org/10.1088/1742-6596/26/1/064

    Article  CAS  Google Scholar 

  59. D.M. Liu, T. Troczynski, W.J. Tseng, Water-based sol-gel synthesis of hydroxyapatite: process development. Biomaterials 22, 1721–1730 (2001). https://doi.org/10.1016/S0142-9612(00)00332-X

    Article  CAS  Google Scholar 

  60. S.H. Rhee, Synthesis of hydroxyapatite via mechanochemical treatment. Biomaterials 23, 1147–1152 (2002). https://doi.org/10.1016/S0142-9612(01)00229-0

    Article  CAS  Google Scholar 

  61. Y.J. Wang, C.J. Di, K. Wei, S.H. Zhang, X.D. Wang, Surfactant-assisted synthesis of hydroxyapatite particles. Mater. Lett. 60, 3227–3231 (2006). https://doi.org/10.1016/j.matlet.2006.02.077

    Article  CAS  Google Scholar 

  62. A. Yelten-Yilmaz, S. Yilmaz, Wet chemical precipitation synthesis of hydroxyapatite (HA) powders. Ceram. Int. 44, 9703–9710 (2018). https://doi.org/10.1016/j.ceramint.2018.02.201

    Article  CAS  Google Scholar 

  63. S.J. Lee, Y.S. Yoon, M.H. Lee, N.S. Oh, Nanosized hydroxyapatite powder synthesized from eggshell and phosphoric acid. J. Nanosci. Nanotechnol. 7, 4061–4064 (2007). https://doi.org/10.1166/jnn.2007.067

    Article  CAS  Google Scholar 

  64. A. Buekenhoudt, A. Kovalevsky, J. Luyten, F. Snijkers, in 1.11 - basic aspects in inorganic membrane preparation, ed. by Drioli E, (Elsevier, Oxford, 2010), pp. 217–252. https://doi.org/10.1016/B978-0-08-093250-7.00011-6

    Chapter  Google Scholar 

  65. S. Pramanik, A.K. Agarwal, K.N. Rai, A. Garg, Development of high strength hydroxyapatite by solid-state-sintering process. Ceram. Int. 33, 419–426 (2007). https://doi.org/10.1016/j.ceramint.2005.10.025

    Article  CAS  Google Scholar 

  66. M.H. Santos, M. de Oliveira, L.P.F. de Souza, H.S. Mansur, W.L. Vasconcelos, Synthesis control and characterization of hydroxyapatite prepared by wet precipitation process. Mater. Res. 7, 625–630 (2004). https://doi.org/10.1590/s1516-14392004000400017

    Article  CAS  Google Scholar 

  67. D. Moreno, F. Vargas, J. Ruiz, M.E. López, Solid-state synthesis of alpha tricalcium phosphate for cements used in biomedical applications. Bol. la Soc. Esp. Ceram. y Vidr. 59, 193–200 (2020). https://doi.org/10.1016/j.bsecv.2019.11.004

    Article  CAS  Google Scholar 

  68. K. Teshima, S.H. Lee, M. Sakurai, Y. Kameno, K. Yubuta, T. Suzuki, T. Shishido, M. Endo, S. Oishi, Well-formed one-dimensional hydroxyapatite crystals grown by an environmentally friendly flux method. Cryst. Growth Des. 9, 2937–2940 (2009). https://doi.org/10.1021/cg900159j

    Article  CAS  Google Scholar 

  69. H.R. Javadinejad, R. Ebrahimi-Kahrizsangi, Thermal and kinetic study of hydroxyapatite formation by solid-state reaction. Int. J. Chem. Kinet. 53, 583–595 (2021). https://doi.org/10.1002/kin.21467

    Article  CAS  Google Scholar 

  70. T. Rojac, M. Kosec, Mechanochemical synthesis of complex ceramic oxides. High-Energy Ball Milling (2010). https://doi.org/10.1533/9781845699444.2.113

    Article  Google Scholar 

  71. R. Dorey, Routes to thick films. Ceram. Thick Film MEMS Microdevices (2012). https://doi.org/10.1016/b978-1-4377-7817-5.00002-x

    Article  Google Scholar 

  72. F.C. Gennari, J.J. Andrade-Gamboa, A systematic approach to the synthesis, thermal stability and hydrogen storage properties of rare-earth borohydrides, Emerging materials for energy conversion and storage (Elsevier, Amsterdam, Netherlands, 2018), pp. 429–459. https://doi.org/10.1016/B978-0-12-813794-9.00013-2

    Chapter  Google Scholar 

  73. N. Llorca-Isern, C. Artieda-Guzmán, Metal-based composite powders, Advances in powder metallurgy: Properties, processing and applications (Elsevier Inc, Sawston, Cambridge, United Kingdom, 2013), pp. 241–72. https://doi.org/10.1533/9780857098900.2.241

    Chapter  Google Scholar 

  74. R.B. Schwarz, Introduction to the viewpoint set on: mechanical alloying. Scr. Mater. 34, 1–4 (1996). https://doi.org/10.1016/1359-6462(95)00463-7

    Article  CAS  Google Scholar 

  75. T.D. Shen, C.C. Koch, T.L. McCormick, R.J. Nemanich, J.Y. Huang, J.G. Huang, The structure and property characteristics of amorphous/nanocrystalline silicon produced by ball milling. J. Mater. Res. 10, 139–148 (1995). https://doi.org/10.1557/JMR.1995.0139

    Article  CAS  Google Scholar 

  76. K.C.B. Yeong, J. Wang, S.C. Ng, Mechanochemical synthesis of nanocrystalline hydroxyapatite from CaO and CaHPO4. Biomaterials 22, 2705–2712 (2001). https://doi.org/10.1016/S0142-9612(00)00257-X

    Article  CAS  Google Scholar 

  77. M.H. Fathi, E.M. Zahrani, Fabrication and characterization of fluoridated hydroxyapatite nanopowders via mechanical alloying. J. Alloys Compd. 475, 408–414 (2009). https://doi.org/10.1016/j.jallcom.2008.07.058

    Article  CAS  Google Scholar 

  78. T.K. Achar, A. Bose, P. Mal, Mechanochemical synthesis of small organic molecules. Beilstein J. Org. Chem. 13, 1907–1931 (2017). https://doi.org/10.3762/bjoc.13.186

    Article  CAS  Google Scholar 

  79. C. Shu, W. Yanwei, L. Hong, P. Zhengzheng, Y. Kangde, Synthesis of carbonated hydroxyapatite nanofibers by mechanochemical methods. Ceram. Int. 31, 135–138 (2005). https://doi.org/10.1016/j.ceramint.2004.04.012

    Article  CAS  Google Scholar 

  80. S. Dinda, A. Bhagavatam, H. Alrehaili, G.P. Dinda, Mechanochemical synthesis of nanocrystalline hydroxyapatite from Ca(H2PO4)2·H2O, CaO, Ca(OH)2, and P2O5 mixtures. Nanomaterials 10, 1–10 (2020). https://doi.org/10.3390/nano10112232

    Article  CAS  Google Scholar 

  81. S. Eiden-Aßmann, M. Viertelhaus, A. Heiß, K.A. Hoetzer, J. Felsche, The influence of amino acids on the biomineralization of hydroxyapatite in gelatin. J. Inorg. Biochem. 91, 481–486 (2002). https://doi.org/10.1016/S0162-0134(02)00481-6

    Article  Google Scholar 

  82. J. Zhan, Y.H. Tseng, J.C.C. Chan, C.Y. Mou, Biomimetic formation of hydroxyapatite nanorods by a single-crystal-to- single-crystal transformation. Adv. Funct. Mater. 15, 2005–2010 (2005). https://doi.org/10.1002/adfm.200500274

    Article  CAS  Google Scholar 

  83. D.W. Kim, I.S. Cho, J.Y. Kim, H.L. Jang, G.S. Han, H.S. Ryu, H. Shin, H.S. Jung, H. Kim, K.S. Hong, Simple large-scale synthesis of hydroxyapatite nanoparticles: In situ observation of crystallization process. Langmuir 26, 384–388 (2010). https://doi.org/10.1021/la902157z

    Article  CAS  Google Scholar 

  84. S. Catros, F. Guillemot, E. Lebraud, C. Chanseau, S. Perez, R. Bareille, J. Amédée, J.C. Fricain, Physico-chemical and biological properties of a nano-hydroxyapatite powder synthesized at room temperature. Irbm 31, 226–233 (2010). https://doi.org/10.1016/j.irbm.2010.04.002

    Article  Google Scholar 

  85. Y.H. Huang, Y.J. Shih, F.J. Cheng, Novel KMnO 4-modified iron oxide for effective arsenite removal. J. Hazard Mater. 198, 1–6 (2011). https://doi.org/10.1016/j.jhazmat.2011.10.010

    Article  CAS  Google Scholar 

  86. E. Bouyer, F. Gitzhofer, M.I. Boulos, Morphological study of hydroxyapatite nanocrystal suspension. J. Mater. Sci. Mater. Med. 11, 523–531 (2000). https://doi.org/10.1023/A:1008918110156

    Article  CAS  Google Scholar 

  87. A. Afshar, M. Ghorbani, N. Ehsani, M.R. Saeri, C.C. Sorrell, Some important factors in the wet precipitation process of hydroxyapatite. Mater. Des. 24, 197–202 (2003). https://doi.org/10.1016/S0261-3069(03)00003-7

    Article  CAS  Google Scholar 

  88. T. Matsumoto, K.I. Tamine, R. Kagawa, Y. Hamada, M. Okazaki, J. Takahashi, Different behavior of implanted hydroxyapatite depending on morphology, size and crystallinity. J. Ceram. Soc. Japan 114, 760–762 (2006). https://doi.org/10.2109/jcersj.114.760

    Article  CAS  Google Scholar 

  89. I. Mobasherpour, M.S. Heshajin, A. Kazemzadeh, M. Zakeri, Synthesis of nanocrystalline hydroxyapatite by using precipitation method. J. Alloys Compd. 430, 330–333 (2007). https://doi.org/10.1016/j.jallcom.2006.05.018

    Article  CAS  Google Scholar 

  90. G. Gecim, S. Dönmez, E. Erkoc, Calcium deficient hydroxyapatite by precipitation: continuous process by vortex reactor and semi-batch synthesis. Ceram. Int. 47, 1917–1928 (2021). https://doi.org/10.1016/j.ceramint.2020.09.020

    Article  CAS  Google Scholar 

  91. Y. Wang, X. Ren, X. Ma, W. Su, Y. Zhang, X. Sun, X. Li, Alginate-intervened hydrothermal synthesis of hydroxyapatite nanocrystals with nanopores. Cryst. Growth Des. 15, 1949–1956 (2015). https://doi.org/10.1021/acs.cgd.5b00113

    Article  CAS  Google Scholar 

  92. Y. Qi, J. Shen, Q. Jiang, B. Jin, J. Chen, X. Zhang, The morphology control of hydroxyapatite microsphere at high pH values by hydrothermal method. Adv. Powder Technol. 26, 1041–1046 (2015). https://doi.org/10.1016/j.apt.2015.04.008

    Article  CAS  Google Scholar 

  93. G. Zhang, J. Chen, S. Yang, Q. Yu, Z. Wang, Q. Zhang, Preparation of amino-acid-regulated hydroxyapatite particles by hydrothermal method. Mater. Lett. 65, 572–574 (2011). https://doi.org/10.1016/j.matlet.2010.10.078

    Article  CAS  Google Scholar 

  94. F. Nagata, Y. Yamauchi, M. Tomita, K. Kato, Hydrothermal synthesis of hydroxyapatite nanoparticles and their protein adsorption behavior. J. Ceram. Soc. Japan 121, 797–801 (2013). https://doi.org/10.2109/jcersj2.121.797

    Article  CAS  Google Scholar 

  95. N.A.S. Mohd Pu’ad, R.H. Abdul Haq, H. Mohd Noh, H.Z. Abdullah, M.I. Idris, T.C. Lee, Synthesis method of hydroxyapatite: a review. Mater. Today Proc. 29, 233–239 (2019). https://doi.org/10.1016/j.matpr.2020.05.536

    Article  CAS  Google Scholar 

  96. W.J. Shih, M.C. Wang, M.H. Hon, Morphology and crystallinity of the nanosized hydroxyapatite synthesized by hydrolysis using cetyltrimethylammonium bromide (CTAB) as a surfactant. J. Cryst. Growth 275, 2339–2344 (2005). https://doi.org/10.1016/j.jcrysgro.2004.11.330

    Article  CAS  Google Scholar 

  97. A. Almirall, G. Larrecq, J.A. Delgado, S. Martínez, J.A. Planell, M.P. Ginebra, Fabrication of low temperature macroporous hydroxyapatite scaffolds by foaming and hydrolysis of an α-TCP paste. Biomaterials 25, 3671–3680 (2004). https://doi.org/10.1016/j.biomaterials.2003.10.066

    Article  CAS  Google Scholar 

  98. M. Kavitha, R. Subramanian, K.S. Vinoth, R. Narayanan, G. Venkatesh, N. Esakkiraja, Optimization of process parameters for solution combustion synthesis of strontium substituted hydroxyapatite nanocrystals using design of experiments approach. Powder Technol. 271, 167–181 (2015). https://doi.org/10.1016/j.powtec.2014.10.046

    Article  CAS  Google Scholar 

  99. J.S. Cho, J.C. Lee, S.H. Rhee, Effect of precursor concentration and spray pyrolysis temperature upon hydroxyapatite particle size and density. J. Biomed. Mater. Res. Part B Appl. Biomater. 104, 422–430 (2016). https://doi.org/10.1002/jbm.b.33406

    Article  CAS  Google Scholar 

  100. S. Sasikumar, R. Vijayaraghavan, Synthesis and characterization of bioceramic calcium phosphates by rapid combustion synthesis. J. Mater. Sci. Technol. 26, 1114–1118 (2010). https://doi.org/10.1016/S1005-0302(11)60010-8

    Article  CAS  Google Scholar 

  101. R. Ayers, N. Hannigan, N. Vollmer, C. Unuvar, Combustion synthesis of heterogeneous calcium phosphate bioceramics from calcium oxide and phosphate precursors. Int. J. Self Propag. High Temp. Synth. 20, 6–14 (2011). https://doi.org/10.3103/S1061386211010031

    Article  CAS  Google Scholar 

  102. R. Ramakrishnan, P. Wilson, T. Sivakumar, I. Jemina, A comparative study of hydroxyapatites synthesized using various fuels through aqueous and alcohol mediated combustion routes. Ceram. Int. 39, 3519–3532 (2013). https://doi.org/10.1016/j.ceramint.2012.10.176

    Article  CAS  Google Scholar 

  103. N. Wakiya, M. Yamasaki, T. Adachi, A. Inukai, N. Sakamoto, D. Fu, O. Sakurai, K. Shinozaki, H. Suzuki, Preparation of hydroxyapatite-ferrite composite particles by ultrasonic spray pyrolysis. Mater. Sci. Eng. B Solid State Mater. Adv. Technol. 173, 195–198 (2010). https://doi.org/10.1016/j.mseb.2009.12.013

    Article  CAS  Google Scholar 

  104. W. Widiyastuti, A. Setiawan, S. Winardi, T. Nurtono, H. Setyawan, Particle formation of hydroxyapatite precursor containing two components in a spray pyrolysis process. Front. Chem. Sci. Eng. 8, 104–113 (2014). https://doi.org/10.1007/s11705-014-1406-1

    Article  CAS  Google Scholar 

  105. G.H. An, H.J. Wang, B.H. Kim, Y.G. Jeong, Y.H. Choa, Fabrication and characterization of a hydroxyapatite nanopowder by ultrasonic spray pyrolysis with salt-assisted decomposition. Mater. Sci. Eng. A 449–451, 821–824 (2007). https://doi.org/10.1016/j.msea.2006.02.436

    Article  CAS  Google Scholar 

  106. J.S. Cho, Y.C. Kang, Nano-sized hydroxyapatite powders prepared by flame spray pyrolysis. J. Alloys Compd. 464, 282–287 (2008). https://doi.org/10.1016/j.jallcom.2007.09.092

    Article  CAS  Google Scholar 

  107. M.E. Zilm, L. Chen, V. Sharma, A. McDannald, M. Jain, R. Ramprasad, M. Wei, Hydroxyapatite substituted by transition metals: experiment and theory. Phys. Chem. Chem. Phys. 18, 16457–16465 (2016). https://doi.org/10.1039/c6cp00474a

    Article  CAS  Google Scholar 

  108. M. Frasnelli, F. Cristofaro, V.M. Sglavo, S. Dirè, E. Callone, R. Ceccato, G. Bruni, A.I. Cornaglia, L. Visai, Synthesis and characterization of strontium-substituted hydroxyapatite nanoparticles for bone regeneration. Mater. Sci. Eng. C 71, 653–662 (2017). https://doi.org/10.1016/j.msec.2016.10.047

    Article  CAS  Google Scholar 

  109. S.Y. Park, K.-I. Kim, S.P. Park, J.H. Lee, H.S. Jung, Aspartic acid-assisted synthesis of multifunctional strontium-substituted hydroxyapatite microspheres. Cryst. Growth Des. 16, 4318–4326 (2016). https://doi.org/10.1021/acs.cgd.6b00420

    Article  CAS  Google Scholar 

  110. J. Li, L. Yang, X. Guo, W. Cui, S. Yang, J. Wang, Y. Qu, Z. Shao, S. Xu, Osteogenesis effects of strontium-substituted hydroxyapatite coatings on true bone ceramic surfaces in vitro and in vivo. Biomed. Mater. (2018). https://doi.org/10.1088/1748-605X/aa89af

    Article  Google Scholar 

  111. J. Li, X. Liu, S. Park, A.L. Miller, A. Terzic, L. Lu, Strontium-substituted hydroxyapatite stimulates osteogenesis on poly(propylene fumarate) nanocomposite scaffolds. J. Biomed. Mater. Res. Part A 107, 631–642 (2019). https://doi.org/10.1002/jbm.a.36579

    Article  CAS  Google Scholar 

  112. Z. Geng, X. Wang, J. Zhao, Z. Li, L. Ma, S. Zhu, Y. Liang, Z. Cui, H. He, X. Yang, The synergistic effect of strontium-substituted hydroxyapatite and microRNA-21 on improving bone remodeling and osseointegration. Biomater. Sci. 6, 2694–2703 (2018). https://doi.org/10.1039/c8bm00716k

    Article  CAS  Google Scholar 

  113. F. Tamimi, N.D. Le, D.C. Bassett, S. Ibasco, U. Gbureck, J. Knowles, A. Wright, A. Flynn, S.V. Komarova, J.E. Barralet, Biocompatibility of magnesium phosphate minerals and their stability under physiological conditions. Acta Biomater. 7, 2678–2685 (2011). https://doi.org/10.1016/j.actbio.2011.02.007

    Article  CAS  Google Scholar 

  114. A. Ewald, K. Helmschrott, G. Knebl, N. Mehrban, L.M. Grover, U. Gbureck, Effect of cold-setting calcium- and magnesium phosphate matrices on protein expression in osteoblastic cells. J Biomed Mater Res Part B Appl Biomater 96 B, 326–332 (2011). https://doi.org/10.1002/jbm.b.31771

    Article  CAS  Google Scholar 

  115. N.C. Andrés, N.L. D’Elía, J.M. Ruso, A.E. Campelo, V.L. Massheimer, P.V. Messina, Manipulation of Mg2+-Ca2+ switch on the development of bone mimetic hydroxyapatite. ACS Appl. Mater. Interfaces 9, 15698–15710 (2017). https://doi.org/10.1021/acsami.7b02241

    Article  CAS  Google Scholar 

  116. I. Uysal, F. Severcan, A. Tezcaner, Z. Evis, Co-doping of hydroxyapatite with zinc and fluoride improves mechanical and biological properties of hydroxyapatite. Prog. Nat. Sci. Mater. Int. 24, 340–349 (2014). https://doi.org/10.1016/j.pnsc.2014.06.004

    Article  CAS  Google Scholar 

  117. M. Irfan, S.N. Sultana, B. Venkateswarlu, M. Jagannatham, R. Dumpala, B.R. Sunil, Zinc-substituted hydroxyapatite: synthesis, structural analysis, and antimicrobial behavior. Trans. Indian Inst. Met. 74, 2335–2344 (2021). https://doi.org/10.1007/s12666-021-02290-x

    Article  CAS  Google Scholar 

  118. E.S. Thian, J. Huang, S.M. Best, Z.H. Barber, W. Bonfield, Silicon-substituted hydroxyapatite: the next generation of bioactive coatings. Mater. Sci. Eng. C 27, 251–256 (2007). https://doi.org/10.1016/j.msec.2006.05.016

    Article  CAS  Google Scholar 

  119. Y.O. Nikitina, N.V. Petrakova, A.A. Ashmarin, D.D. Titov, S.V. Shevtsov, T.N. Penkina, E.A. Kuvshinova, S.M. Barinov, V.S. Komlev, N.S. Sergeeva, Preparation and properties of copper-substituted hydroxyapatite powders and ceramics. Inorg. Mater. 55, 1061–1067 (2019). https://doi.org/10.1134/S002016851910011X

    Article  CAS  Google Scholar 

  120. A. Elrayah, W. Zhi, S. Feng, S. Al-Ezzi, H. Lei, J. Weng, Preparation of micro/nano-structure copper-substituted hydroxyapatite scaffolds with improved angiogenesis capacity for bone regeneration. Materials (Basel) (2018). https://doi.org/10.3390/ma11091516

    Article  Google Scholar 

  121. J. Sang Cho, S.H. Um, D. Su Yoo, Y.C. Chung, S. Hye Chung, J.C. Lee, S.H. Rhee, Enhanced osteoconductivity of sodium-substituted hydroxyapatite by system instability. J. Biomed. Mater. Res. Part B Appl. Biomater. 102, 1046–1062 (2014). https://doi.org/10.1002/jbm.b.33087

    Article  CAS  Google Scholar 

  122. W.E. Cabrera, I. Schrooten, M.E. De Broe, P.C. D’Haese, Strontium and bone. J. Bone Miner. Res. 14, 661–668 (1999). https://doi.org/10.1359/jbmr.1999.14.5.661

    Article  CAS  Google Scholar 

  123. C. Li, O. Paris, S. Siegel, P. Roschger, E.P. Paschalis, K. Klaushofer, P. Fratzl, Strontium is incorporated into mineral crystals only in newly formed bone during strontium ranelate treatment. J. Bone Miner. Res. 25, 968–975 (2010). https://doi.org/10.1359/jbmr.091038

    Article  CAS  Google Scholar 

  124. G. Boivin, D. Farlay, M.T. Khebbab, X. Jaurand, P.D. Delmas, P.J. Meunier, In osteoporotic women treated with strontium ranelate, strontium is located in bone formed during treatment with a maintained degree of mineralization. Osteoporos. Int. 21, 667–677 (2010). https://doi.org/10.1007/s00198-009-1005-z

    Article  CAS  Google Scholar 

  125. P. Roschger, I. Manjubala, N. Zoeger, F. Meirer, R. Simon, C. Li, N. Fratzl-Zelman, B.M. Misof, E.P. Paschalis, C. Streli, P. Fratzl, K. Klaushofer, Bone material quality in transiliac bone biopsies of postmenopausal osteoporotic women after 3 years of strontium ranelate treatment. J. Bone Miner. Res. 25, 891–900 (2010). https://doi.org/10.1359/jbmr.091028

    Article  Google Scholar 

  126. J. Christoffersen, M.R. Christoffersen, N. Kolthoff, O. Bärenholdt, Effects of strontium ions on growth and dissolution of hydroxyapatite and on bone mineral detection. Bone 20, 47–54 (1997). https://doi.org/10.1016/S8756-3282(96)00316-X

    Article  CAS  Google Scholar 

  127. H. Zhu, D. Guo, L. Sun, H. Li, D.A.H. Hanaor, F. Schmidt, K. Xu, Nanostructural insights into the dissolution behavior of Sr-doped hydroxyapatite. J. Eur. Ceram. Soc. 38, 5554–5562 (2018). https://doi.org/10.1016/j.jeurceramsoc.2018.07.056

    Article  Google Scholar 

  128. K. Zhu, K. Yanagisawa, R. Shimanouchi, A. Onda, K. Kajiyoshi, Preferential occupancy of metal ions in the hydroxyapatite solid solutions synthesized by hydrothermal method. J. Eur. Ceram. Soc. 26, 509–513 (2006). https://doi.org/10.1016/j.jeurceramsoc.2005.07.019

    Article  CAS  Google Scholar 

  129. K. Kandori, M. Saito, H. Saito, A. Yasukawa, T. Ishikawa, Adsorption of protein on non-stoichiometric calcium-strontium hydroxyapatite. Colloids Surf. A Physicochem. Eng. Asp. 94, 225–230 (1995). https://doi.org/10.1016/0927-7757(94)02969-5

    Article  CAS  Google Scholar 

  130. E. Landi, G. Logroscino, L. Proietti, A. Tampieri, M. Sandri, S. Sprio, Biomimetic Mg-substituted hydroxyapatite: From synthesis to in vivo behaviour. J. Mater. Sci. Mater. Med. 19, 239–247 (2008). https://doi.org/10.1007/s10856-006-0032-y

    Article  CAS  Google Scholar 

  131. S. Gomes, G. Renaudin, E. Jallot, J.M. Nedelec, Structural characterization and biological fluid interaction of sol-gel-derived Mg-substituted biphasic calcium phosphate ceramics. ACS Appl. Mater. Interfaces 1, 505–513 (2009). https://doi.org/10.1021/am800162a

    Article  CAS  Google Scholar 

  132. E. Landi, A. Tampieri, M. Mattioli-Belmonte, G. Celotti, M. Sandri, A. Gigante, P. Fava, G. Biagini, Biomimetic Mg- and Mg, CO3-substituted hydroxyapatites: synthesis characterization and in vitro behaviour. J. Eur. Ceram. Soc. 26, 2593–2601 (2006). https://doi.org/10.1016/j.jeurceramsoc.2005.06.040

    Article  CAS  Google Scholar 

  133. S. Lala, M. Ghosh, P.K. Das, D. Das, T. Kar, S.K. Pradhan, Magnesium substitution in carbonated hydroxyapatite: structural and microstructural characterization by Rietveld’s refinement. Mater. Chem. Phys. 170, 319–329 (2016). https://doi.org/10.1016/j.matchemphys.2015.12.058

    Article  CAS  Google Scholar 

  134. A.A. Chaudhry, J. Goodall, M. Vickers, J.K. Cockcroft, I. Rehman, J.C. Knowles, J.A. Darr, Synthesis and characterisation of magnesium substituted calcium phosphate bioceramic nanoparticles made via continuous hydrothermal flow synthesis. J. Mater. Chem. 18, 5900–5908 (2008). https://doi.org/10.1039/b807920j

    Article  CAS  Google Scholar 

  135. A. Farzadi, F. Bakhshi, M. Solati-Hashjin, M. Asadi-Eydivand, N.A.A. Osman, Magnesium incorporated hydroxyapatite: synthesis and structural properties characterization. Ceram. Int. 40, 6021–6029 (2014). https://doi.org/10.1016/j.ceramint.2013.11.051

    Article  CAS  Google Scholar 

  136. J.P. O’Connor, D. Kanjilal, M. Teitelbaum, S.S. Lin, J.A. Cottrell, Zinc as a therapeutic agent in bone regeneration. Materials (Basel) 13, 1–22 (2020). https://doi.org/10.3390/ma13102211

    Article  CAS  Google Scholar 

  137. M. Yamaguchi, R. Yamaguchi, Action of zinc on bone metabolism in rats. Increases in alkaline phosphatase activity and DNA content. Biochem. Pharmacol. 35, 773–777 (1986). https://doi.org/10.1016/0006-2952(86)90245-5

    Article  CAS  Google Scholar 

  138. C. Ergun, T.J. Webster, R. Bizios, R.H. Doremus, Hydroxylapatite with substituted magnesium, zinc, cadmium, and yttrium. I. Structure and microstructure. J. Biomed. Mater. Res. 59, 305–311 (2002). https://doi.org/10.1002/jbm.1246

    Article  CAS  Google Scholar 

  139. F. Miyaji, Y. Kono, Y. Suyama, Formation and structure of zinc-substituted calcium hydroxyapatite. Mater. Res. Bull. 40, 209–220 (2005). https://doi.org/10.1016/j.materresbull.2004.10.020

    Article  CAS  Google Scholar 

  140. M. Li, X. Xiao, R. Liu, C. Chen, L. Huang, Structural characterization of zinc-substituted hydroxyapatite prepared by hydrothermal method. J. Mater. Sci. Mater. Med. 19, 797–803 (2008). https://doi.org/10.1007/s10856-007-3213-4

    Article  CAS  Google Scholar 

  141. Z. Zhong, J. Qin, J. Ma, Rapid synthesis of citrate-zinc substituted hydroxyapatite using the ultrasonication-microwave method. Ceram. Int. 43, 13308–13313 (2017). https://doi.org/10.1016/j.ceramint.2017.07.029

    Article  CAS  Google Scholar 

  142. E.S. Thian, T. Konishi, Y. Kawanobe, P.N. Lim, C. Choong, B. Ho, M. Aizawa, Zinc-substituted hydroxyapatite: a biomaterial with enhanced bioactivity and antibacterial properties. J. Mater. Sci. Mater. Med. 24, 437–445 (2013). https://doi.org/10.1007/s10856-012-4817-x

    Article  CAS  Google Scholar 

  143. E.M. Carlisle, Silicon: a requirement in bone formation independent of vitamin D1. Calcif. Tissue Int. 33, 27–34 (1981). https://doi.org/10.1007/BF02409409

    Article  CAS  Google Scholar 

  144. W. Götz, E. Tobiasch, S. Witzleben, M. Schulze, Effects of silicon compounds on biomineralization, osteogenesis, and hard tissue formation. Pharmaceutics 11, 1–27 (2019). https://doi.org/10.3390/pharmaceutics11030117

    Article  CAS  Google Scholar 

  145. E.M. Carlisle, Silicon: a possible factor in bone calcification. Science 167(3916), 279–280 (1970). https://doi.org/10.1126/science.167.3916.279

    Article  CAS  Google Scholar 

  146. L.T. Bang, B.D. Long, R. Othman, Carbonate hydroxyapatite and silicon-substituted carbonate hydroxyapatite: synthesis, mechanical properties, and solubility evaluations. Sci. World J. (2014). https://doi.org/10.1155/2014/969876

    Article  Google Scholar 

  147. A. Tsalsabila, Y.W. Sari, A. Maddu, Synthesis of silicon substituted hydroxyapatite using microwave irradiation, in: Proc—2018 1st Int Conf Bioinformatics, Biotechnol Biomed Eng BioMIC 2018, vol. 1, pp. 1–5 (2019). https://doi.org/10.1109/BIOMIC.2018.8610598

  148. C. Palacios, The role of nutrients in bone health, from A to Z. Crit. Rev. Food Sci. Nutr. 46, 621–628 (2006). https://doi.org/10.1080/10408390500466174

    Article  CAS  Google Scholar 

  149. S. Shanmugam, B. Gopal, Copper substituted hydroxyapatite and fluorapatite: synthesis, characterization and antimicrobial properties. Ceram. Int. 40, 15655–15662 (2014). https://doi.org/10.1016/j.ceramint.2014.07.086

    Article  CAS  Google Scholar 

  150. H.J. Kronzucker, D. Coskun, L.M. Schulze, J.R. Wong, D.T. Britto, Sodium as nutrient and toxicant. Plant Soil 369, 1–23 (2013). https://doi.org/10.1007/s11104-013-1801-2

    Article  CAS  Google Scholar 

  151. R. Mangili, J.J. Bending, G. Scott, L.K. Li, A. Gupta, G. Viberti, Increased sodium-lithium countertransport activity in red cells of patients with insulin-dependent diabetes and nephropathy. N. Engl. J. Med. 318, 146–150 (1988)

    Article  CAS  Google Scholar 

  152. K. Hu, B.R. Olsen, The roles of vascular endothelial growth factor in bone repair and regeneration. Bone 91, 30–38 (2016). https://doi.org/10.1016/j.bone.2016.06.013

    Article  CAS  Google Scholar 

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Funding

This research was supported by grants from the National Research Foundation of Korea funded by the Ministry of Science and ICT for Bio-inspired Innovation Technology Development Project (NRF-2018M3C1B7021997) and Basic Science Research Program (NRF-2020R1A2C2006100). Dr. Jun Hyuk Heo and Mr. Si Hyun Kim appreciate the support of the National Research Foundation of Korea funded by the Ministry of Education (NRF-2022R1C1C2002823 (JHH) and NRF-2020R1A6A3A13070482 (SHK)).

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  1. Si Hyun Kim and Cheol Hyun Park have contributed equally to this work.

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  1. School of Advanced Materials Science and Engineering, Sungkyunkwan University (SKKU), Suwon, 16419, Republic of Korea

    Cheol Hyun Park, Jun Hyuk Heo & Jung Heon Lee

  2. Advanced Materials Technology Research Center, Sungkyunkwan University (SKKU), Suwon, 16419, Republic of Korea

    Jun Hyuk Heo & Jung Heon Lee

  3. SKKU Advanced Institute of Nanotechnology (SAINT), Sungkyunkwan University (SKKU), Suwon, 16419, Republic of Korea

    Si Hyun Kim & Jung Heon Lee

  4. Biomedical Institute for Convergence at SKKU (BICS), Sungkyunkwan University (SKKU), Suwon, 16419, Republic of Korea

    Jung Heon Lee

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Kim, S.H., Park, C.H., Heo, J.H. et al. Progress and perspectives of metal-ion-substituted hydroxyapatite for bone tissue engineering: comparison with hydroxyapatite. J. Korean Ceram. Soc. 59, 271–288 (2022). https://doi.org/10.1007/s43207-022-00198-w

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Keywords

  • Hydroxyapatite (HA)
  • Metal ions
  • Substitution
  • Bone tissue engineering
  • Osteogenesis