Bioactive calcium phosphate foam ceramics modified by biomimetic apatite

By combining the method of replication of polyurethane foam matrices at 1200 °C and modification in model SBF (Simulated Body Fluid) solutions of various compositions, open-pore calcium phosphate foam ceramics with a porosity of 53-60 % was obtained. The architecture and morphology of the calcium phosphate foam ceramics surface was formed by using polyurethane foam matrices («Granufoam», «STR») with different porosity and quantity of open pores. Modification of the calcium phosphate foam ceramics in SBF solutions of various compositions leads to a slight decrease in porosity to 3 %, which indicates the formation of an ultrathin apatite layer. The calcium phosphate-modified foam ceramics consisted of β-tricalcium phosphate, β-calcium pyrophosphate, α-tricalcium phosphate, and biomimetic apatite. In the standard SBF solution, the formation of apatite on calcium phosphate foam ceramics occurs slowly (14-56 days) and the strength increases by a factor of 2 as compared to the initial one. Soaking of calcium phosphate foam ceramics in SBF without HCO₃- leads to the formation of biomimetic apatite with inclusions of calcium chloride dihydrophosphate in spherulites. Modification in a 5-fold concentrated SBF solution for 3-5 days at 37 °C makes it possible to form 6-10 times more biomimetic apatite compared to standard SBF with a 2.5-fold increase in static strength to 0.05 MPa. It has been established that at 800 °C biomimetic apatite crystallizes into β- tricalcium phosphate.

1. Wang J., Wang M., Chen F. Nano-Hydroxyapatite Coating Promotes Porous Calcium Phosphate Ceramic-Induced Osteogenesis Via BMP/Smad Signaling Pathway. International Journal of Nanomedicine, 2019, vol. 14, pp. 7987-8000. https://doi.org/10.2147/IJN.S216182

2. Safronova T. V. Inorganic Materials for Regenerative Medicine. Inorganic Materials, 2021, vol. 57, no. 5, pp. 443-474. https://doi.org/10.1134/S002016852105006X

3. Daculsi G., Baroth S., LeGeros R. Z. 20 years of biphasic calcium phosphate bioceramics development and applications. Advances in Bioceramics and Porous Ceramics II. Wiley, American Ceramic Society, 2010, pp. 45-58. https://doi.org/10.1002/9780470584354.ch5

4. Barinov S. M., Komlev V. S. Approaches to the fabrication of calcium phosphate-based porous materials for bone tissue regeneration. Inorganic Materials, 2016, vol. 52, no. 4, pp. 339-346. https://doi.org/10.1134/S0020168516040026

5. Doremus R. H. Review: Bioceramics. Journal of Materials Science, 1992, vol. 27, pp. 285-297. https://doi.org/10.1007/bf00543915

6. Tavoni M., Tampieri A., Sprio S. Bioactive calcium phosphate-based composites for bone regeneration. Journal of Composites Science, 2021, vol. 5, pp. 227-254. https://doi.org/10.3390/jcs5090227

7. Barinov S. M., Komlev V. S. Bioceramics based on calcium phosphates. Moscow, Nauka Publ., 2005. 204 p. (in Russian).

8. Cai Y., Liu Y., Yan W., Hu Q., Tao J., Zhang M., Shi Zh., Tang R. Role of hydroxyapatite nanoparticle size in bone cell proliferation. Journal of Materials Chemistry, 2007, vol. 17, no. 36, pp. 3780-3787. https://doi.org/10.1039/B705129H

9. Krut'ko V. K., Maslova L. Yu, Musskaya O. N., Safronova T. V., Kulak A. I. Calcium phosphate ceramic foam obtained by firing a hydroxyapatite - monocalcium phosphate monohydrate powder mixture. Glass and ceramics, 2022, vol. 78, no. 11-12, pp. 476-480. https://doi.org/10.1007/s10717-022-00435-y

10. Dorozhkin S. V. Calcium orthophosphate bioceramics. Ceramics International B, 2015, vol. 41, pp. 13913-13966. https://doi.org/10.1016/j.ceramint.2015.08.004

11. Krut'ko V. K., Kulak A. I., Musskaya O. N. Thermal transformations of composites based on hydroxyapatite and zirconia. Inorganic Materials, 2017, vol. 53, no. 4. pp. 429-436. https://doi.org/10.1134/S0020168517040094

12. Kim H.-W. Noh Y.-J., Koh Y.-H., Kim H.-E., Kim H.-M. Effect of CaF2 on Densification and Properties of Hydroxyapatite- Zirconia Composites for Biomedical Applications. Biomaterials, 2002, vol. 23, pp. 4113-4121. https://doi.org/10.1016/s0142-9612(02)00150-3

13. Montufar E. B., Vojtova L., Celko L., Ginebra M.-P. Calcium Phosphate Foams: Potential Scaffolds for Bone Tissue Modeling in Three Dimension. Koledova Z. (ed.) 3D Cell Culture. Methods and Protocols. New York, Humana Press, 2017, pp. 79-94. https://doi.org/10.1007/978-1-4939-7021-6_6

14. Cancedda R., Mastrogiacomo M., Bianchi G., Derubeis A., Muraglia A., Quarto R. Bone marrow stromal cells and their use in regenerating bone. Tissue Engineering of Cartilage and Bone: Novartis Foundation Symposium. Vol. 249. Chichester, UK: John Wiley & Sons, 2003, pp. 133-147. https://doi.org/10.1002/0470867973.ch10

15. Launay F., Jouve J.-L., Guillaume J.-M., Viehweger E., Jacquemier M., Bollini G. Les allongements progressifs de l'avant-bras chez l'enfant. A propos d'une serie de 14 cas. Revue de Chirurgie Orthopedique et Reparatriee de I’Appareil Moteur, 2001, vol. 87, pp. 786-795 (in French). https://doi.org/RCO-12-2001-87-8-0035-1040-101019-ART5

16. Dee P., You H. Y., Teoh S. H., Le Ferrand H. Bioinspired approaches to toughen calcium phosphate-based ceramics for bone repair. Journal of the Meehanieal Behavior of Biomedieal Materials, 2020, no. 112. Article ID 104078. https://doi.org/10.1016/j.jmbbm.2020.104078

17. Hench L. L. Bioceramics. Journal of the Ameriean Ceramie Soeiety, 1998, vol. 81, no. 7, pp. 1705-1728. https://doi.org/10.1111/j.1151-2916.1998.tb02540.x

18. Kokubo T., Kushitani H., Sakka S., Kitsugi T., Yamamuro T. Solutions able to reproduce in vivo surface-structure change in bioactive glass-ceramic A-W. Journal of Biomedieal Materials Researeh, 1990, no. 24, pp. 721-734. https://doi.org/10.1002/jbm.820240607

19. Krut'ko V. K., Musskaya O. N., Kulak A. I., Safronova T. V. Thermal evolution of calcium phosphate foam ceramics obtained on the basis of hydroxyapatite and monocalcium phosphate of monohydrate. Fiziko-khimieheskie aspekty izueheniya klasterov, nanostruktur i nanomaterialov = Physieal and ehemieal aspeets of the study of elusters, nanostruetures and nanomaterials, 2019, no. 11, pp. 615-623 (in Russian). https://doi.org/10.26456/pcascnn/2019.11.615

20. Krut'ko V. K., Kulak A. I., Musskaya O. N., Lesnikovich Yu. A. Synthetic hydroxyapatite - the basis of bone-replacing biomaterials. Sofiya, 2017, no. 1, pp. 50-57 (in Russian).

21. Kokubo T., Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials, 2006, vol. 27, pp. 2907-2915. https://doi.org/10.1016/j.biomaterials.2006.01.017

22. Krut'ko V. K., Maslova L. Yu, Musskaya O. N., Safronova T. V., Kulak A. I. Modification of calcium phosphate foam ceramics with bioapatite in SBF solution. Fiziko-khimieheskie aspekty izueheniya klasterov, nanostruktur i nanomateria-lov = Physieal and ehemieal aspeets of the study of elusters, nanostruetures and nanomaterials, 2021, no. 13, pp. 870-880 (in Russian). https://doi.org/10.26456/pcascnn/2021.13.870

23. Krut'ko V. K., Kulak A. I., Musskaya O. N., Safronova T. V., Budeiko N. L. Calcium phosphate foam ceramics with regulated bioactivity. Fiziko-khimieheskie aspekty izueheniya klasterov, nanostruktur i nanomaterialov = Physieal and ehemieal aspeets of the study of elusters, nanostruetures and nanomaterials, 2018, no. 10, pp. 374-382 (in Russian). https://doi.org/10.26456/pcascnn/2018.10.374

24. Oyane A., Onuma K., Ito A., Kokubo T. Clustering of calcium phosphate in SBF and in the system CaCl2-H3PO4-KCl-H2O. Bioeeramies, 1999, no. 12, pp. 157-160. https://doi.org/10.1142/9789814291064_0038

25. Glazov I. E., Krut'ko V. K., Musskaya O. N., Kulak A. I. Calcium Phosphate Apatites: Wet Formation, Thermal Transformations, Terminology, and Identification. Russian Journal of Inorganie Chemistry, 2022, vol. 67, no. 2, pp. 173-182. https://doi.org/10.1134/s0036023622020048

26. Glazov I. E., Krut'ko V. K., Kulak A. I., Musskaya O. N., Vlasov R. A., Malakhovsky P. O., Dileep Kumar V. G., Surya P. S., Mysore Sridhar S., Reddy N. Effect of platelet-poor plasma additive on the formation of biocompatible calcium phosphates. Materials Today Communieations, 2021, vol. 77, pp. 102224. https://doi.org/10.1016/j.mtcomm.2021.102224

27. Gernaey K. V., Huusom J. K., Gani R. 12th International Symposium on Proeess Systems Engineering and 25th European Symposium on Computer Aided Proeess Engineering: Parts A, B and C. Elsevier, 2015, pp. 1571-1575.

28. Piga G., Amarante A., Makhoul C., Cunha E., Malgosa A., Enzo S., Goncalves D. в-Tricalcium phosphate interferes with the assessment of crystallinity in burned skeletal remains. Journal of Speetroseopy, 2018, article 5954146. https://doi.org/10.1155/2018/5954146

29. Krut'ko V. K., Kulak A. I., Musskaya O. N., Safronova T. V., Putlyaev V. I. Calcium phosphate foam ceramic based on hydroxyapatite-brushite powder mixture. Glass and eeramies, 2019, vol. 76, no. 3-4, pp. 113-118. https://doi.org/10.1007/s10717-019-00145-y

30. Ryu H.-S., Youn H.-J., Hong K. S., Chang B.-S., Lee Ch.-K., Chung S.-S. An improvement in sintering property of в-tricalcium phosphate by addition of calcium pyrophosphate. Biomaterials, 2002, no. 23, pp. 909-914. https://doi.org/10.1016/s0142-9612(01)00201-0

31. Bucur A. I., Bucur R., Vlase T., Doca N. Thermal analysis and high-temperature X-ray diffraction of nano-tricalcium phosphate crystallization. Journal of Thermal Analysis and Calorimetry, 2012, vol. 107, no. 1, pp. 249-255. https://doi.org/10.1007/s10973-011-1753-9

32. Gajjeraman S., Narayanan K., Hao J., Qin Ch., George A. Matrix macromolecules in hard tissues control the nucleation and hierarchical assembly of hydroxyapatite. Journal of Biological Chemistry, 2007, vol. 282, pp. 1193-1204. https://doi.org/10.1074/jbc.M604732200