Issue 23-5, 2024
Review
Osteoplastic Biomaterials from Organic and Mineral Components of the Bone Matrix: a Literature Review
1Pavel A. Markov, 1,*
Petr S. Eremin, 1
Elena S. Berezkina,1
Marina V. Volkova, 1
Irina A. Usova,1
Ilmira R. Gilmutdinova
1National Medical Research Center for Rehabilitation and Balneology, Moscow, Russia
ABSTRACT
INTRODUCTION. The bones of the human and animal have a unique ability to remodel. The ability to constantly renew bone tissue determines the healing of fractures and the adaptation of bones to mechanical loads. However, the process of bone self-healing is effective only for defects of non-critical size. In segmental and critical defects, endogenous stimulation of bone tissue regeneration is required. In this regard, there remains a need to design osteoplastic biomaterials with improved pro-regenerative action. Every year, new data appear that expand our understanding of the methods and mechanisms for stimulating bone tissue restoration using artifi cial osteoplastic materials. AIM. Characteristics of modern methods of constructing biomimetic materials from organic and mineral components of bone matrix.MATERIALS AND METHODS. The literature review was conducted using the PubMed and ScienceDirect databases. Query dates — may–july 2024, query depth — 1965–2024.
MAIN CONTENT OF THE REVIEW. Effective use of bone polymers for the creation of biomimetic osteoplastic materials is possible only with an understanding of the principles of molecular-cellular interaction of biopolymers with bone cells and tissues. By now, it has been established that the ability of collagen to influence the functional activity of cells involved in the reparative regeneration of bone tissue is due to the presence of special patterns in its structure - binding sites with cellular receptors, which are formed by a specific sequence of amino acids in the collagen polypeptide chain. In the case of inorganic bone material, the functionally significant elements are the chemical composition and crystal structure of calcium phosphate salts. A current trend in the design of osteoplastic materials is to impart biomimetic properties to them. At the molecular level, this approach is implemented using as intrafibrillar and extrafibrillar mineralization of collagen fibrils. At the tissue and organ level, biomimicry is achieved through the use of three-dimensional bioprint ing technologies.
CONCLUSION. Thus, thanks to advances in biology, physics, chemistry and engineering sciences, it was possible to develop new tech nologies for designing osteoplastic materials that imitate the structure and function of native bone tissue. The use of biomaterials cre ated using biomimetics principles increases the efficiency of bone tissue damage restoration.
KEYWORDS: collagen, hydroxyapatite, tricalcium phosphates, biocomposite, bioceramics
FUNDING: The authors declare no external funding in the conduct of the study.
CONFLICT OF INTEREST: The authors declare no apparent or potential conflicts of interest related to the publication of this article.
FOR CITATION: Markov P.A., Eremin P.S., Berezkina E.S., Volkova M.V., Usova I.A., Gilmutdinova I.R. Osteoplastic Biomaterials from Organic and Mineral Components of the Bone Matrix: a Literature Review. Bulletin of Rehabilitation Medicine. 2024; 23(5):97-107. https://doi.org/10.38025/2078-1962-2024-23-5-97-107 (In Russ.).
FOR CORRESPONDENCE:
Petr S. Eremin, E-mail: ereminps@gmail.com, EreminPS@nmicrk.ru
References:
- Florencio-Silva R., Sasso G.R., Sasso-Cerri E., et al. Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells. Biomedical Research International. 2015; 2015: 421746. https://doi.org/10.1155/2015/421746
- Rossi N., Hadad H., Bejar-Chapa M., et al. Bone Marrow Stem Cells with Tissue-Engineered Scaffolds for Large Bone Segmental Defects: A Systematic Review. Tissue Engineering Part B Rev. 2023; 29(5): 457–472. https://doi.org/10.1089/ten.TEB.2022.0213
- Intravaia J.T., Graham T., Kim H.S., et al. Smart Orthopedic Biomaterials and Implants. Current opinion in biomedical engineering. 2023; 25: 100439. https://doi.org/10.1016/j.cobme.2022.100439
- Cárdenas-Aguazaco W., Lara-Bertrand A. L., Prieto-Abello L., et al. Exploring calcium-free alternatives in endochondral bone repair tested on In vivo trials - A review. Regenerative therapy. 2024; 26: 145–160. https://doi.org/10.1016/j.reth.2024.05.017
- Khan M.U.A., Aslam M.A., Bin Abdullah M.F., et al. Recent perspective of polymeric biomaterial in tissue engineering — a review. Materials Today Chemistry. 2023; 34: 101818. https://doi.org/10.1016/j.mtchem.2023.101818
- Al Mahmud M.Z., Mobarak M.H., Hossain N., et al. Emerging breakthroughs in biomaterials for orthopedic applications: A comprehensive review. Bioprinting. 2023; 36: e00323. https://doi.org/10.1016/j.bprint.2023.e00323
- Battafarano G., Rossi M., De Martino V., et al. Strategies for Bone Regeneration: From Graft to Tissue Engineering. International Journal of Molecular Sciences. 2021; 22(3): 1128. https://doi.org/10.3390/ijms2203112810.3390/ijms22031128
- Senn N. Senn on the Healing of Aseptic Bone Cavities by Implantation of Antiseptic Decalcified Bone. Annals Surgery. 1889; 10(5): 352–368. https://doi.org/10.1097/00000658-188907000-00043
- Urist M.R. Bone: formation by autoinduction. Science. 1965; 150(3698): 893–899. https://doi.org/10.1126/science.150.3698.893
- Katz M.S., Ooms M., Heitzer M., et al. Postoperative Morbidity and Complications in Elderly Patients after Harvesting of Iliac Crest Bone Grafts. Medicina (Kaunas). 2021; 57(8): 759. https://doi.org/10.3390/medicina57080759
- Zhang H., Yang L., Yang X.G., et al. Demineralized Bone Matrix Carriers and their Clinical Applications: An Overview. Orthopaedic Surgery. 2019; 11(5): 725–737. https://doi.org/10.1111/os.12509
- Sorushanova A., Delgado L.M., Wu Z., et al. The Collagen Suprafamily: From Biosynthesis to Advanced Biomaterial Development. Advanced Materials. 2019; 31(1): e1801651. https://doi.org/10.1002/adma.201801651
- Siadat S.M., Ruberti J.W. Mechanochemistry of collagen. Acta Biomaterials. 2023; 163: 50–62. https://doi.org/10.1016/j.actbio.2023.01.025
- Salvatore L., Gallo N., Natali M.L., et al. Mimicking the Hierarchical Organization of Natural Collagen: Toward the Development of Ideal Scaffolding Material for Tissue Regeneration. Frontiers in Bioengineering and Biotechnology. 2021; 9: 644595. https://doi.org/10.3389/fbioe.2021.644595
- Mikhailov O.V. Gelatin as It Is: History and Modernity. International Journal of Molecular Sciences. 2023; 24(4): 3583. https://doi.org/10.3390/ijms24043583
- Lin K., Zhang D., Macedo M.H., et al. Advanced collagen-based biomaterials for regenerative biomedicine. Advanced Functional Materials. 2019; 29: 1804943. https://doi.org/10.1002/adfm.201804943
- Hoop C.L., Zhu J., Nunes A.M., et al. Revealing Accessibility of Cryptic Protein Binding Sites within the Functional Collagen Fibril. Biomolecules. 2017; 7(4): 76. https://doi.org/10.3390/biom7040076
- Ghatak S., Niland S., Schulz J.N., et al. Role of Integrins α1β1 and α2β1 in Wound and Tumor Angiogenesis in Mice. American Journal of Pathology. 2016; 86(11): 3011–3027. https://doi.org/10.1016/j.ajpath.2016.06.021
- Zhou L., Hinerman J.M., Blaszczyk M., et al. Structural basis for collagen recognition by the immune receptor OSCAR. Blood. 2016; 127(5): 529–537. https://doi.org/10.1182/blood-2015-08-667055
- Joyce K., Fabra G.T., Bozkurt Y., Pandit A. Bioactive potential of natural biomaterials: identification, retention and assessment of biological properties. Signal Transduction and Targeted Therapy. 2021; 6(1): 122. https://doi.org/10.1038/s41392-021-00512-8
- Kang J.I., Park K.M. Advances in gelatin-based hydrogels for wound management. Journal of Materials Chemistry B. 2021; 9(6): 1503–1520. https://doi.org/10.1039/D0TB02582H
- Feng Y., Qin S., Yang Y., et al. A functional hydrogel of dopamine-modified gelatin with photothermal properties for enhancing infected wound healing. Colloids and surfaces. B, Biointerfaces. 2024; 241: 114058. https://doi.org/10.1016/j.colsurfb.2024.114058
- Cui B., Zhang C., Gan B., et al. Collagen-tussah silk fibroin hybrid scaffolds loaded with bone mesenchymal stem cells promote skin wound repair in rats. Materials science and engineering. C, Materials for biological applications. 2020; 109: 110611. https://doi.org/10.1016/j.msec.2019.110611
- Hong C., Chung H., Lee G., et al. Remendable Cross-Linked Alginate/Gelatin Hydrogels Incorporating Nanofibers for Wound Repair and Regeneration. Biomacromolecules. 2024; 25(7): 4344–4357. https://doi.org/10.1021/acs.biomac.4c00406
- Qin D., Wang N., You X.G., et al. Collagen-based biocomposites inspired by bone hierarchical structures for advanced bone regeneration: ongoing research and perspectives. Biomaterial Science. 2022; 10(2): 318–353. https://doi.org/10.1039/d1bm01294k
- Maternini M., Guttadauro A., Mascagni D., et al. Non cross-linked equine collagen (Salvecoll-E gel) for treatment of complex ano-rectal fistula. Asian Journal of Surgery. 2019; 43: 401–404. https://doi.org/10.1016/j.asjsur.2019.06.009
- Rezvani Ghomi E., Nourbakhsh N., Akbari Kenari M., et al. Collagen-based biomaterials for biomedical applications. Journal of biomedical materials research. Part B, Applied biomaterials. 2021; 109(12): 1986–1999. https://doi.org/10.1002/jbm.b.34881
- Wang Y., Wang Z., Dong Y. Collagen-Based Biomaterials for Tissue Engineering. ACS biomaterials science & engineering. 2023; 9(3): 1132–1150. https://doi.org/10.1021/acsbiomaterials.2c00730
- Dawson E., Bae H.W., Burkus J.K., et al. Recombinant human bone morphogenetic protein-2 on an absorbable collagen sponge with an osteoconductive bulking agent in posterolateral arthrodesis with instrumentation. A prospective randomized trial. Journal of bone and joint surgery. 2009; 91(7): 1604–1613. https://doi.org/10.2106/JBJS.G.01157
- Lu H., Kawazoe N., Kitajima T., et al. Spatial immobilization of bone morphogenetic protein-4 in a collagen-PLGA hybrid scaffold for enhanced osteoinductivity. Biomaterials. 2012; 33(26): 6140–6146. https://doi.org/10.1016/j.biomaterials.2012.05.038
- Oryan A., Alidadi S., Moshiri A., Bigham-Sadegh A. Bone morphogenetic proteins: a powerful osteoinductive compound with non-negligible side effects and limitations. Biofactors. 2014; 40(5): 459–481. https://doi.org/10.1002/biof.1177
- Salvatore L., Gallo N., Natali M.L. et al. Marine collagen and its derivatives: Versatile and sustainable bio-resources for healthcare. Materials Science & Engineering C-Materials for Biological Applications. 2020; 113: 110963. https://doi.org/10.1016/j.msec.2020.110963
- Song J.E., Thangavelu M., Choi J., et al. Bone Regeneration Using Duck’s Feet-Derived Collagen Scaffold as an Alternative Collagen Source. Advances in Experimental Medicine and Biology. 2020; 1250: 3–13. https://doi.org/10.1007/978-981-15-3262-7_1
- Lim D.J. Bone Mineralization in Electrospun-Based Bone Tissue Engineering. Polymers (Basel). 2022; 14(10): 2123. https://doi.org/10.3390/polym14102123
- Takagi S., Chow L.C., Ishikawa K. Formation of hydroxyapatite in new calcium phosphate cements. Biomaterials. 1998; 19(17): 1593–1599. https://doi.org/10.1016/S0142-9612(97)00119-1
- Jeong J., Kim J.H., Shim J.H., et al. Bioactive calcium phosphate materials and applications in bone regeneration. Biomaterials research. 2019; 23: 4. https://doi.org/10.1186/s40824-018-0149-3
- Hou X., Zhang L., Zhou Z., et al. Calcium Phosphate-Based Biomaterials for Bone Repair. Journal of Functional Biomaterials. 2022; 13(4): 187. https://doi.org/10.3390/jfb13040187
- Ambard A.J., Mueninghoff, L. Calcium Phosphate Cement: Review of Mechanical and Biological Properties. Journal of Prosthodontics. 2006; 15: 321–328. https://doi.org/10.1111/j.1532-849X.2006.00129.x
- Ramesh N., Moratti S.C., Dias G.J. Hydroxyapatite-polymer biocomposites for bone regeneration: A review of current trends. Journal of Biomedical Materials Research Part B: Applied Biomaterials. 2018; 106(5): 2046–2057. https://doi.org/10.1002/jbm.b.33950
- Samavedi S., Whittington A.R., Goldstein A.S. Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior. Acta Biomaterials. 2013; 9(9): 8037–8045. https://doi.org/10.1016/j.actbio.2013.06.014
- Xiao D., Zhang J., Zhang C., et al. The role of calcium phosphate surface structure in osteogenesis and the mechanisms involved. Acta Biomaterialia. 2020; 106: 22–33. https://doi.org/10.1016/j.actbio.2019.12.034
- Katebifar S., Arul M., Abdulmalik S., et al. Novel high-strength polyester composite scaffolds for bone regeneration. Polymers for advanced technologies. 2023; 34(12): 3770–3791. https://doi.org/10.1002/pat.6178
- Terkawi M.A., Matsumae G., Shimizu T., et al. Interplay between Inflammation and Pathological Bone Resorption: Insights into Recent Mechanisms and Pathways in Related Diseases for Future Perspectives. International Journal of Molecular Sciences. 2022; 23(3): 1786. https://doi.org/10.3390/ijms23031786
- Ponzetti M., Rucci N. Updates on Osteoimmunology: What’s New on the Cross-Talk Between Bone and Immune System. Frontiers in Endocrinology 2019; 10: 236. https://doi.org/10.3389/fendo.2019.00236
- Mariani E., Lisignoli G., Borzì R.M., Pulsatelli L. Biomaterials: Foreign Bodies or Tuners for the Immune Response? International journal of molecular sciences. 2019; 20(3): 636. https://doi.org/10.3390/ijms20030636
- Gou M., Wang H., Xie H., Song, H. Macrophages in guided bone regeneration: potential roles and future directions. Frontiers in immunology. 2024; 15: 1396759. https://doi.org/10.3389/fimmu.2024.1396759
- Chen X., Wang M., Chen F., et al. Correlations between macrophage polarization and osteoinduction of porous calcium phosphate ceramics. Acta Biomaterials. 2020; 103: 318–332. https://doi.org/10.1016/j.actbio.2019.12.019
- Li M., Guo X., Qi W., et al. Macrophage polarization plays roles in bone formation instructed by calcium phosphate ceramics. Journal of Materials Chemistry B. 2020; 8(9): 1863–1877. https://doi.org/10.1039/C9TB02932J
- Shang L., Shao J., Ge S. Immunomodulatory Properties: The Accelerant of Hydroxyapatite-Based Materials for Bone Regeneration. Tissue Engineering Methods (Part C). 2022; 28(8): 377–392. https://doi.org/10.1089/ten.tec.2022.00111112
- Nie Z., Hu Z., Guo X., et al. Genesis of osteoclasts on calcium phosphate ceramics and their role in material-induced bone formation. Acta Biomaterials. 2023; 157: 625–638. https://doi.org/10.1016/j.actbio.2022.11.005
- Pearson J.J., Gerken N., Bae C., et al. In vivo hydroxyapatite scaffold performance in infected bone defects. Journal of Biomedical Materials Research Part B: Applied Biomaterials. 2020; 108(3): 1157–1166. https://doi.org/10.1002/jbm.b.34466
- Hu C., Zilm M., Wei M. et al. Fabrication of intrafibrillar and extrafibrillar mineralized collagen/apatite scaffolds with a hierarchical structure. Journal of Biomedical Materials Research Part A. 2016; 104(5): 1153–1161. https://doi.org/10.1002/jbm.a.35649
- Zou L., Zhang Y., Liu X., et al. Biomimetic mineralization on natural and synthetic polymers to prepare hybrid scaffolds for bone tissue engineering. Colloids and Surfaces B: Biointerfaces. 2019; 178: 222–229. https://doi.org/10.1016/j.colsurfb.2019.03.004
- Hu C., Zhang L., Wei M. Development of biomimetic scaffold woth both intrafibrilar and extrafibrillar mineralization. ACS Biomaterials Science & Engineering. 2015; 1(8): 669–676. https://doi.org/10.1021/acsbiomaterials.5b00088
- Ciocca L., Lesci I.G., Mezini O., et al. Customized hybrid biomimetic hydroxyapatite scaffold for bone tissue regeneration. Journal of Biomedical Materials Research Part B: Applied Biomaterials. 2017; 105(4): 723–734. https://doi.org/10.1002/jbm.b.33597
- Xu S.J., Qiu Z.Y., Wu J.J., et al. Osteogenic differentiation gene expression profiling of hMSCs on hydroxyapatite and mineralized collagen. Tissue Engineering Part A. 2016; 22(2): 170–181. https://doi.org/10.1089/ten.tea.2015.0237
- Qiu Z.Y., Cui Y., Tao C.S., et al. Mineralized collagen: rationale, current status, and clinical applications. Materials (Basel). 2015; 8(8): 4733–4750. https://doi.org/10.3390/ma8084733
- Khalaf A.T., Wei Y., Wan J., et al. Bone Tissue Engineering through 3D Bioprinting of Bioceramic Scaffolds: A Review and Update. Life (Basel). 2022; 12(6): 903. https://doi.org/10.3390/life12060903
- Abbadessa A., Ronca A., Salerno, A. Integrating bioprinting, cell therapies and drug delivery towards in vivo regeneration of cartilage, bone and osteochondral tissue. Drug delivery and translational research. 2024; 14(4): 858–894. https://doi.org/10.1007/s13346-023-01437-1
- Saberi A., Kouhjani M., Mohammadi M., Hosta-Rigau L. Novel scaffold platforms for simultaneous induction osteogenesis and angiogenesis in bone tissue engineering: a cutting-edge approach. Journal of nanobiotechnology. 2023; 21(1): 351. https://doi.org/10.1186/s12951-023-02115-7
- Yuan X., Zhu W., Yang Z., et al. Recent Advances in 3D Printing of Smart Scaffolds for Bone Tissue Engineering and Regeneration. Advanced Materials. 2024; e2403641. https://doi.org/10.1002/adma.202403641
- van der Heide D., Cidonio G., Stoddart M.J., D’Este M. 3D printing of inorganic-biopolymer composites for bone regeneration. Biofabrication. 2022; 14(4): 10.1088/1758-5090/ac8cb2. https://doi.org/10.1088/1758-5090/ac8cb2

The content is available under the Creative Commons Attribution 4.0 License.
©
This is an open article under the CC BY 4.0 license. Published by the National Medical Research Center for Rehabilitation and Balneology.