Hydroxyapatite and Biopolymer Composites with Promising Biomedical Applications

Juanita Daria Flores Valdez; Aidé Sáenz Galindo; Claudia Magdalena López Badillo; Adali Oliva Castañeda Facio; Pablo Acuña Vazquez

doi:10.17488/RMIB.43.2.1

Authors

Juanita Daria Flores Valdez Universidad Autónoma de Coahuila, México https://orcid.org/0000-0002-7068-7480
Aidé Sáenz Galindo Universidad Autónoma de Coahuila, México
Claudia Magdalena López Badillo Universidad Autónoma de Coahuila, México https://orcid.org/0000-0001-6892-1541
Adali Oliva Castañeda Facio Universidad Autónoma de Coahuila, México https://orcid.org/0000-0003-3780-112X
Pablo Acuña Vazquez Centro de Investigación en Química Aplicada, México https://orcid.org/0000-0003-0987-7880

DOI:

https://doi.org/10.17488/RMIB.43.2.1

Keywords:

Composites, Hydroxyapatite, Biopolymers

Abstract

The purpose of tissue engineering (regenerative medicine) is to develop materials that replace human tissue, having as main characteristics' biodegradability, biocompatibility, no toxicity, osteoconductivity, which lead to cell maturation and proliferation. Due to the importance of the development of this type of materials, several researchers have used biopolymers and calcium phosphate salts (hydroxyapatite) as composites to be used in this area as drug releases, scaffolds, implants, among others. Different biopolymers can be suitable for this type of application, in this work we have described the most widely used biopolymers for biomedical purposes, such as alginate, collagen, gellan gum, chitosan, and polylactic acid, in addition to a detailed description of hydroxyapatite, biopolymers, as well as biopolymer/hydroxyapatite composites, to highlight their potential and the most relevant characteristics of these materials.

Downloads

Download data is not yet available.

References

El-Habashy SE, Eltaher HM, Gaballah A, Zaki EI, et al. Hybrid bioactive hydroxyapatite/polycaprolactone nanoparticles for enhanced osteogenesis. Mater Sci Eng C [Internet]. 2021;119:111599. Available from: https://doi.org/10.1016/j.msec.2020.111599

Escobar Sierra D, Mesa Ospina D. Evaluación de recubrimientos de quitosano sobre cuerpos porosos de hidroxiapatita. Sci Tech [Internet]. 2019;24(1):161-172. Available from: https://doi.org/10.22517/23447214.20051

Chen J, Yu Q, Zhang G, Yang S, et al. Preparation and biocompatibility of nanohybrid scaffolds by in situ homogeneous formation of nano hydroxyapatite from biopolymer polyelectrolyte complex for bone repair applications. Colloids Surf B [Internet]. 2012;93:100–107. Available from: http://dx.doi.org/10.1016/j.colsurfb.2011.12.022

Chakravarty J, Rabbi MF, Chalivendra V, Ferreira T, et al. Mechanical and biological properties of chitin/polylactide (PLA)/hydroxyapatite (HAP) composites cast using ionic liquid solutions. Int J Biol Macromol [Internet]. 2020;151:1213–1223. Available from: https://doi.org/10.1016/j.ijbiomac.2019.10.168

Kalisz G, Przekora A, Kazimierczak P, Gieroba B, et al. Physicochemical changes of the chitosan/β-1,3-glucan/hydroxyapatite biocomposite caused by mesenchymal stem cells cultured on its surface in vitro. Spectrochim Acta A Mol Biomol [Internet]. 2021;251:119439. Available from: https://doi.org/10.1016/j.saa.2021.119439

Benedini L, Laiuppa J, Santillán G, Baldini M, et al. Antibacterial alginate/nano-hydroxyapatite composites for bone tissue engineering: Assessment of their bioactivity, biocompatibility, and antibacterial activity. Mater Sci Eng C [Internet]. 2020;115:111101. Available from: https://doi.org/10.1016/j.msec.2020.111101

Sathiyavimal S, Vasantharaj S, LewisOscar F, Selvaraj R, Brindhadevi K, Pugazhendhi A. Natural organic and inorganic–hydroxyapatite biopolymer composite for biomedical applications. Prog Org Coat [Internet]. 2020;147:105858. Available from: https://doi.org/10.1016/j.porgcoat.2020.105858

Lett AJ, Sagadevan S, Fatimah I, Hoque ME, et al. Recent advances in natural polymer-based hydroxyapatite scaffolds: Properties and applications. Eur Polym [Internet]. 2021;148:110360. Available from: https://doi.org/10.1016/j.eurpolymj.2021.110360

Trakoolwannachai V, Kheolamai P, Ummartyotin S. Characterization of hydroxyapatite from eggshell waste and polycaprolactone (PCL) composite for scaffold material. Compos B Eng [Internet]. 2019;173:106974. Available from: https://doi.org/10.1016/j.compositesb.2019.106974

Williams RAD, Elliot JC. Bioquímica dental básica y aplicada. Distrito Federal, México: El Manual Moderno; 1990. 263p. Spanish.

Rahavi SS, Ghaderi O, Monshi A, Fathi MH. A comparative study on physicochemical properties of hydroxyapatite powders derived from natural and synthetic sources. Russ J Non-Ferrous Metals [Internet]. 2017;58(3):276–286. Available from: https://doi.org/10.3103/S1067821217030178

Giraldo-Betancur A, Espinosa-Arbelaez DG, del Real-López A, Millan-Malo BM, et al. Comparison of physicochemical properties of bio and commercial hydroxyapatite. Curr Appl Phys [Internet]. 2013;13(7):1383–1390. Available from: http://dx.doi.org/10.1016/j.cap.2013.04.019

Alvarez-Barreto J, Márquez K, Gallardo E, Moret J, et al. Mesenchymal Stem Cell Culture on Composite Hydrogels of Hydroxyapatite Nanoparticles and Photo-Crosslinking Chitosan. Rev Mex Ing Biom [Internet]. 2017;38(3):524-536. Available from: http://dx.doi.org/10.17488/RMIB.38.3.2

Rivera JA, Fetter G, Bosch P. Efecto del pH en la síntesis de hidroxiapatita en presencia de microondas. Rev Mater [Internet]. 2011;15(4):488-505. Available from: https://doi.org/10.1590/S1517-70762010000400003

Flores-Valdez JD, Sáenz-Galindo A, Múzquiz-Ramos EM, Soria Aguilar MJ. Biopolymers and applications. CienciAcierta [Internet]. 2021;(66):61–72. Available from: http://www.cienciacierta.uadec.mx/articulos/CC66/biopolimerosyaplicaciones.pdf

Sivakanthan S, Rajendran S, Gamage A, Madhujith T, et al. Antioxidant and antimicrobial applications of biopolymers: A review. Food Res Int [Internet]. 2020;136:109327. Available from: https://doi.org/10.1016/j.foodres.2020.109327

Lizundia E, Kundu D. Advances in Natural Biopolymer‐Based Electrolytes and Separators for Battery Applications. Adv Funct [Internet]. 2021;31(3):2005646. Available from: https://doi.org/10.1002/adfm.202005646

Hochmańska-Kaniewska P, Janiszewska D, Oleszek T. Enhancement of the properties of acrylic wood coatings with the use of biopolymers. Prog Org Coat [Internet]. 2022;162:106522. Available from: https://doi.org/10.1016/j.porgcoat.2021.106522

Tuan Naiwi TSR, Aung MM, Rayung M, Ahmad A, et al. Dielectric and ionic transport properties of bio-based polyurethane acrylate solid polymer electrolyte for application in electrochemical devices. Polym Test [Internet]. 2022;106:107459. Available from: https://doi.org/10.1016/j.polymertesting.2021.107459

Wan Mahari AW, Kee SH, Foong SY, Amelia TSM, et al. Generating alternative fuel and bioplastics from medical plastic waste and waste frying oil using microwave co-pyrolysis combined with microbial fermentation. Renew Sustain Energy Rev [Internet]. 2022;153:111790. Available from: https://doi.org/10.1016/j.rser.2021.111790

Parveen FK. Recent Advances in Biopolymers [Internet]. London: IntechOpen; 2016. 288p. Available from: https://doi.org/10.5772/60630

Narain, R. Polymer Science and Nanotechnology Fundamentals and Applications [Internet]. United Kingdom: Elsevier; 2020. 488p. https://doi.org/10.1016/C2018-0-01134-2

Rebelo R, Fernandes M, Fangueiro R. Biopolymers in Medical Implants: A Brief Review. Procedia Eng [Internet]. 2017;200:236–243. Available from: https://doi.org/10.1016/j.proeng.2017.07.034

Hassan MES, Bai J, Dou D-Q. Biopolymers; Definition, Classification and Applications. Egypt J Chem [Internet]. 2019;62(9):133–145. Available from: https://dx.doi.org/10.21608/ejchem.2019.6967.1580

Ahmed S, Kanchi S, Kumar G. Handbook of Biopolymers: Advances and Multifaceted Applications. California: Jenny Stanford Publishing; 2018. 308p.

Dubinenko GE, Zinoviev AL, Bolbasov EN, Novikov VT, et al. Preparation of Poly(L-lactic acid)/Hydroxyapatite composite scaffolds by fused deposit modeling 3D printing. Mater Today Proc [Internet]. 2020;22:228–234. Available from: https://doi.org/10.1016/j.matpr.2019.08.092

Kumar PPP, Lim D-K. Gold-Polymer Nanocomposites for Future Therapeutic and Tissue Engineering Applications. Pharmaceutics [Internet]. 2021;14(1):70. Available from: https://doi.org/10.3390/pharmaceutics14010070

Biswal T. Biopolymers for tissue engineering applications: A review. Mater Today Proc [Internet]. 2021;41:397–402. Available from: https/doi.org/10.1016/j.matpr.2020.09.628

Villareal Valdiviezo GP, Múzquiz Ramos EM, Farías Cepeda L. Medical applications of biopolymers. CienciAcierta [Internet]. 2020;63:83. Available from: http://www.cienciacierta.uadec.mx/articulos/CC63/83AplicacionesMedicas.pdf

Aboudi J, Arnold SM, Bednarcyk BA. Mechanics of Composite Materials [Internet]. 2nd ed. Butterworth-Heinemann: Elsevier; 2013. 984p. Available from: https://doi.org/10.1016/C2011-0-05224-9

Gay D, Hoa SV, Tsai SW. Composite Materials: Design and Applications. 1st ed. Florida: CRC Press; 2002. 552p.

Gibson RE. Principal of Composite Mechanics. 4th ed. Boca Raton: CRC Press; 2016. 700p.

Mohanty AK, Misra M, Drzal LT, Selke S, Harte B, Hinrichsen G. Natural Fibers, Biopolymers, and Biocomposites [Internet]. 1st ed. Boca Raton: CRC Press; 2005. 896p. Available from: https://doi.org/10.1201/9780203508206

Sankaran S, Ravishankar BN, Ravi Sekhar K, Dasgupta S, et al. Syntactic Foams for Multifunctional Applications. In: Kar, K (eds.). Composite Materials [Internet]. Berlin: Springer Berlin Heidelberg; 2017. 281–314p. Available from: https://doi.org/10.1007/978-3-662-49514-8_9

Holban AM, Grumezescu A (eds.). Materials for Biomedical Engineering: Hydrogels and Polymer-based Scaffolds [Internet]. Amsterdam, Oxford, Cambridge: Elsevier; 2019. 562p. Available from: https://doi.org/10.1016/C2017-0-04477-4

Moraes MA, Silva CF, Vieira RS (eds.). Biopolymers Membranes and Films Health, Food, Environment, and Energy Applications. Amsterdam, Oxford, Cambridge: Elsevier; 2020. 633p. Available from: https://doi.org/10.1016/C2018-0-02693-6

Benedini L, Laiuppa J, Santillán G, Baldini M, et al. Antibacterial alginate/nano-hydroxyapatite composites for bone tissue engineering: Assessment of their bioactivity, biocompatibility, and antibacterial activity. Mater Sci Eng C [Internet]. 2020;115:111101. Available from: https://doi.org/10.1016/j.msec.2020.111101

Wang L, Li Y, Li C. In situ processing and properties of nanostructured hydroxyapatite/alginate composite. J Nanopart Res [Internet]. 2009;11(3):691–699. Available from: https://doi.org/10.1007/s11051-008-9431-y

Chae T, Yang H, Leung V, Ko F, et al. Novel biomimetic hydroxyapatite/alginate nanocomposite fibrous scaffolds for bone tissue regeneration. J Mater Sci: Mater Med [Internet]. 2013;24(8):1885–1894. Available from: https://doi.org/10.1007/s10856-013-4957-7

Sukhodub LF, Sukhodub LB, Litsis O, Prylutskyy Y. Synthesis and characterization of hydroxyapatite-alginate nanostructured composites for the controlled drug release. Mater Chem Phys [Internet]. 2018;217:228–34. Available from: https://doi.org/10.1016/j.matchemphys.2018.06.071

Mahmoud EM, Sayed M, El-Kady AM, Elsayed H, et al. In vitro and in vivo study of naturally derived alginate/hydroxyapatite bio composite scaffolds. Int J Biol Macromol [Internet]. 2020;165:1346–1360. Available from: https://doi.org/10.1016/j.ijbiomac.2020.10.014

You F, Chen X, Cooper DML, Chang T, et al. Homogeneous hydroxyapatite/alginate composite hydrogel promotes calcified cartilage matrix deposition with potential for three-dimensional bioprinting. Biofabricación [Internet]. 2018;11:015015. Available from: https://doi.org/10.1088/1758-5090/aaf44a

Ocando C, Dinescu S, Samoila I, Ghitulica CD, et al. Fabrication and properties of alginate-hydroxyapatite biocomposites as efficient biomaterials for bone regeneration. Eur Polym [Internet]. 2021;151:110444. Available from: https://doi.org/10.1016/j.eurpolymj.2021.110444

Sukhodub LF, Sukhodub LB, Pogrebnjak AD, Turlybekuly A, et al. Effect of magnetic particles adding into nanostructured hydroxyapatite–alginate composites for orthopedics. J Korean Ceram Soc [Internet]. 2020;57(5):557–569. Available from: https://doi.org/10.1007/s43207-020-00061-w

De Paula FL, Barreto IC, Rocha-Leão MH, Borojevic R, et al. Hydroxyapatite-alginate biocomposite promotes bone mineralization in different length scales in vivo. Front Mater Sci China. 2009;3(2):145–153. Available from: https://doi.org/10.1007/s11706-009-0029-9

González Paz R, Grillo A, Feijoo JL, Noris-Suárez K, et al. Estudio de Mezclas de Polietileno de Alta Densidad (PEAD) con colágeno/acetato de sodio e Hidroxiapatita (HA). In: Müller-Karger C, Wong S, La Cruz A. (eds). IV Latin American Congress on Biomedical Engineering 2007 [Internet]. Berlin: IFMBE Proceedings; 2008;18:676–680. Available from: https://doi.org/10.1007/978-3-540-74471-9_157

Yoruc ABH, Aydınoglu AK. Synthesis of Hydroxyapatite/Collagen (HA/COL) Composite Powder Using a Novel Precipitation Technique. Acta Phys Pol [Internet]. 2015;127(4):1264–1267. Available from: http://dx.doi.org/10.12693/APhysPolA.127.1264

Sukul M, Min Y-L, Lee B-T. Collagen-hydroxyapatite coated unprocessed cuttlefish bone as a bone substitute. Mater [Internet]. 2016;181:156–560. Available from: http://dx.doi.org/10.1016/j.matlet.2016.05.170

Lara-Rico R, Claudio-Rizo JA, Múzquiz-Ramos E, Lopez-Badillo CM. Hidrogeles de colágeno acoplados con hidroxiapatita para aplicaciones en ingeniería tisular. TIP Rev Espec Cienc Quim-Biol [Internet]. 2020;23:1–12. Available from: https://doi.org/10.22201/fesz.23958723e.2020.0.224

Cholas R, Padmanabhan SK, Gervaso F, Udayan G, et al. Scaffolds for bone regeneration made of hydroxyapatite microspheres in a collagen matrix. Mater Sci Eng C [Internet]. 2016;63:499–505. Available from: http://dx.doi.org/10.1016/j.msec.2016.03.022

Bhuiyan D, Jablonsky MJ, Kolesov I, Middleton J, et al. Novel synthesis and characterization of a collagen-based biopolymer initiated by hydroxyapatite nanoparticles. Acta Biomater [Internet]. 2015;15:181–190. Available from: http://dx.doi.org/10.1016/j.actbio.2014.11.044

Sun R-X, Lv Y, Niu Y-R, Zhao X-H, et al. Physicochemical and biological properties of bovine-derived porous hydroxyapatite/collagen composite and its hydroxyapatite powders. Ceram Int [Internet]. 2017;43(18):16792–16798. Available from: http://dx.doi.org/10.1016/j.ceramint.2017.09.075

Becerra J, Rodriguez M, Leal D, Noris-Suarez K, et al. Chitosan-collagen-hydroxyapatite membranes for tissue engineering. J Mater Sci: Mater Med [Internet]. 2022;33(2):18. Available from: https://doi.org/10.1007/s10856-022-06643-w

Zhao X, Li H, Xu Z, Li K, et al. Selective preparation and characterization of nano-hydroxyapatite/collagen coatings with three-dimensional network structure. Surf Coat Technol [Internet]. 2017;322:227–237. Available from: http://dx.doi.org/10.1016/j.surfcoat.2017.05.042

Kaczmarek B, Sionkowska A, Osyczka AM. Physicochemical properties of scaffolds based on mixtures of chitosan, collagen and glycosaminoglycans with nano-hydroxyapatite addition. Int J Biol Macromol [Internet]. 2018;118:1880–1883. Available from: https://doi.org/10.1016/j.ijbiomac.2018.07.035

Kaczmarek B, Sionkowska A, Gołyńska M, Polkowska I, et al. In vivo study on scaffolds based on chitosan, collagen, and hyaluronic acid with hydroxyapatite. Int J Biol Macromol [Internet]. 2018;118:938–944. Available from: https://doi.org/10.1016/j.ijbiomac.2018.06.175

Kikuchi M, Itoh S, Ichinose S, Shinomiya K, et al. Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials [Internet]. 2001;22(13):1705–1711. Available from: https://doi.org/10.1016/S0142-9612(00)00305-7

Dou DD, Zhou G, Liu HW, Zhang J, et al. Sequential releasing of VEGF and BMP-2 in hydroxyapatite collagen scaffolds for bone tissue engineering: Design and characterization. Int J Biol Macromol [Internet]. 2019;123:622–628. Available from: https://doi.org/10.1016/j.ijbiomac.2018.11.099

Taniyama T, Masaoka T, Yamada T, Wei X, et al. Repair of Osteochondral Defects in a Rabbit Model Using a Porous Hydroxyapatite Collagen Composite Impregnated With Bone Morphogenetic Protein-2. Artif Organs [Internet]. 2015;39(6):529–535. Available from: https://doi.org/10.1111/aor.12409

Osmałek T, Froelich A, Tasarek S. Application of gellan gum in pharmacy and medicine. Int J Pharm. 2014;466(1–2):328–340. Available from: https://doi.org/10.1016/j.ijpharm.2014.03.038

Zare EN, Makvandi P, Borzacchiello A, Tay FR, et al. Antimicrobial gum bio-based nanocomposites and their industrial and biomedical applications. Chem Commun [Internet]. 2019;55(99):14871–14885. Available from: https://doi.org/10.1039/C9CC08207G

Santos MVB, Oliveira AL, Osajima JA, Silva-Filho EC. Development of composites scaffolds with calcium and cerium-hydroxyapatite and gellan gum. Ceram Int [Internet]. 2020;46(3):3811–3817. Available from: https://doi.org/10.1016/j.ceramint.2019.10.104

Rajesh R, Ravichandran YD, Reddy MJK, Ryu SH, et al. Development of functionalized multi-walled carbon nanotube-based polysaccharide–hydroxyapatite scaffolds for bone tissue engineering. RSC Adv [Internet]. 2016;6(85):82385–82393. Available from: http://dx.doi.org/10.1039/C6RA16709H

Manda MG, da Silva LP, Cerqueira MT, Pereira DR, et al. Gellan gum-hydroxyapatite composite spongy-like hydrogels for bone tissue engineering. J Biomed Mater Res A [Internet]. 2018;106(2):479–490. Available from: https://doi.org/10.1002/jbm.a.36248

Vieira S, da Silva Morais A, Garet E, Silva-Correia J, et al. Self-mineralizing Ca-enriched methacrylated gellan gum beads for bone tissue engineering. Acta Biomater [Internet]. 2019;93:74–85. Available from: https://doi.org/10.1016/j.actbio.2019.01.053

Shin H, Olsen BD, Khademhosseini A. Gellan gum microgel-reinforced cell-laden gelatin hydrogels. J Mater Chem B [Internet]. 2014;2(17):2508–2516. Available from: https://doi.org/10.1039/C3TB20984A

Nayak AK, Alkahtani S, Hasnain MS. Jackfruit Seed Starch-Based Composite Beads for Controlled Drug Release. In: Nayak AK, Alkahtani S, Hasnain MS (eds). Polymeric and Natural Composites. Advances in Material Research and Technology [Internet]. Springer Cham ;2022. 213-240p. Available from: https://doi.org/10.1007/978-3-030-70266-3_7

Xu L, Bai X, Yang J, Li J, et al. Preparation and characterisation of a gellan gum-based hydrogel enabling osteogenesis and inhibiting Enterococcus faecalis. Int J Biol Macromol [Internet]. 2020;165:2964–2973. Available from: https://doi.org/10.1016/j.ijbiomac.2020.10.083

Pereira DR, Canadas RF, Silva-Correia J, da Silva Morais A, et al. Injectable gellan-gum/hydroxyapatite-based bilayered hydrogel composites for osteochondral tissue regeneration. Appl Mater Today [Internet]. 2018;12:309–321. Available from: https://doi.org/10.1016/j.apmt.2018.06.005

Altieri MA, Nicholls CI. Agroecology Scaling Up for Food Sovereignty and Resiliency. Lichtfouse E (eds). Sustainable Agriculture Reviews [Internet]. Dordrecht: Springer Dordrecht; 2012. 1–29 p. Available from: https://doi.org/10.1007/978-94-007-5449-2

Ahmed S, Ikram S. Chitosan: Derivatives, Composites and Applications. Hoboken: Wiley; 2017. 516p.

Thomas MS, Koshy RR, Mary SK, Thomas S, et al. Starch, Chitin and Chitosan Based Composites and Nanocomposites [Internet]. Springer Cham; 2019. 57p. Available from: https://doi.org/10.1007/978-3-030-03158-9

Shakir M, Jolly R, Khan AA, Ahmed SS, et al. Resol based chitosan/nano-hydroxyapatite nanoensemble for effective bone tissue engineering. Carbohydr Polym [Internet]. 2018;179:317–327. Available from: http://dx.doi.org/10.1016/j.carbpol.2017.09.103

Shen J, Jin B, Qi Y-C, Jiang Q, et al. Carboxylated chitosan/silver-hydroxyapatite hybrid microspheres with improved antibacterial activity and cytocompatibility. Mater Sci Eng C [Internet]. 2017;78:589–597. Available from: http://dx.doi.org/10.1016/j.msec.2017.03.100

Costa-Pinto AR, Lemos AL, Tavaria FK, Pintado M. Chitosan and Hydroxyapatite Based Biomaterials to Circumvent Periprosthetic Joint Infections. Materials [Internet]. 2021;14(4):804. Available from: https://doi.org/10.3390/ma14040804

Li L, Iqbal J, Zhu Y, Zhang P, et al. Chitosan/Ag-hydroxyapatite nanocomposite beads as a potential adsorbent for the efficient removal of toxic aquatic pollutants. Int J Biol Macromol [Internet]. 2018;120:1752–1759. Available from: https://doi.org/10.1016/j.ijbiomac.2018.09.190

Nabipour H, Wang X, Song L, Hu Y. A fully bio-based coating made from alginate, chitosan and hydroxyapatite for protecting flexible polyurethane foam from fire. Carbohydr Polym [Internet]. 2020;246:116641. Available from: https://doi.org/10.1016/j.carbpol.2020.116641

Alvarez-Barreto J, Máquez K, Gallardo E, Moret J, et al. Mesenchymal Stem Cell Culture on Composite Hydrogels of Hydroxyapatite Nanoparticles and Photo-Crosslinking Chitosan. Rev Mex Ing Biom [Internet]. 2017;38(3):524-536. Available from: https://doi.org/10.17488/RMIB.38.3.2

Trakoolwannachai V, Kheolamai P, Ummartyotin S. Development of hydroxyapatite from eggshell waste and a chitosan-based composite: In vitro behavior of human osteoblast-like cell (Saos-2) cultures. Int J Biol Macromol [Internet]. 2019;134:557–564. Available from: https://doi.org/10.1016/j.ijbiomac.2019.05.004

Tripathi A, Saravanan S, Pattnaik S, Moorthi A, et al. Bio-composite scaffolds containing chitosan/nano-hydroxyapatite/nano-copper–zinc for bone tissue engineering. Int J Biol Macromol [Internet]. 2012;50(1):294–299. Available from: http://dx.doi.org/10.1016/j.ijbiomac.2011.11.013

Soriente A, Fasolino I, Gomez-Sánchez A, Prokhorov E, et al. Chitosan/hydroxyapatite nanocomposite scaffolds to modulate osteogenic and inflammatory response. J Biomed Mater Res Part A [Internet]. 2022;110(2):266–272. Available from: https://doi.org/10.1002/jbm.a.37283

Kaczmarek B, Sionkowska A, Skopinska-Wisniewska J. Influence of glycosaminoglycans on the properties of thin films based on chitosan/collagen blends. J Mech Behav Biomed Mater [Internet]. 2018;80:189–193. Available from: https://doi.org/10.1016/j.jmbbm.2018.02.006

Okada T, Nobunaga Y, Konishi T, Yoshioka T, et al. Preparation of chitosan-hydroxyapatite composite mono-fiber using coagulation method and their mechanical properties. Carbohydr Polym [Internet]. 2017;175:355–360. Available from: http://dx.doi.org/10.1016/j.carbpol.2017.07.072

Balagangadharan K, Chandran SV, Arumugam B, Saravanan S, et al. Chitosan/nano-hydroxyapatite/nano-zirconium dioxide scaffolds with miR-590-5p for bone regeneration. Int J Biol Macromol [Internet]. 2018;111:953–958. Available from: https://doi.org/10.1016/j.ijbiomac.2018.01.122

Chakravarty J, Rabbi MF, Chalivendra V, Ferreira T, et al. Mechanical and biological properties of chitin/polylactide (PLA)/hydroxyapatite (HAP) composites cast using ionic liquid solutions. Int J Biol Macromol [Internet]. 2020;151:1213–1223. Available from: https://doi.org/10.1016/j.ijbiomac.2019.10.168

Akindoyo JO, Beg MDH, Ghazali S, Heim HP, et al. Effects of surface modification on dispersion, mechanical, thermal and dynamic mechanical properties of injection molded PLA-hydroxyapatite composites. Compos Part A Appl Sci Manuf [Internet]. 2017;103:96–105. Available from: http://dx.doi.org/10.1016/j.compositesa.2017.09.013

Grémare A, Guduric V, Bareille R, Heroguez V, et al. Characterization of printed PLA scaffolds for bone tissue engineering. J Biomed Mater Res Part A [Internet]. 2018;106(4):887–894. Available from: https://doi.org/10.1002/jbm.a.36289

Akindoyo JO, Beg MDH, Ghazali S, Heim HP, et al. Impact modified PLA-hydroxyapatite composites – Thermo-mechanical properties. Compos Part A Appl Sci Manuf [Internet]. 2018;107:326–333. Available from: https://doi.org/10.1016/j.compositesa.2018.01.017

Armentano I, Bitinis N, Fortunati E, Mattioli S, et al. Multifunctional nanostructured PLA materials for packaging and tissue engineering. Prog Polym Sci [Internet]. 2013;38(10-11):1720–1747. Available from: http://dx.doi.org/10.1016/j.progpolymsci.2013.05.010

Mohammadi MS, Bureau MN, Nazhat SN. Polylactic acid (PLA) biomedical foams for tissue engineering. In: Netti PA (eds). Biomedical Foams for Tissue Engineering Applications [Internet]. United Kingdom: Elsevier; 2014. 313–334. Available from: https://doi.org/10.1533/9780857097033.2.313

Esposito Corcione C, Gervaso F, Scalera F, Padmanabhan SK, et al. Highly loaded hydroxyapatite microsphere/ PLA porous scaffolds obtained by fused deposition modelling. Ceram Int [Internet]. 2019;45(2):2803–2810. Available from: https://doi.org/10.1016/j.ceramint.2018.07.297

Mondal S, Nguyen TP, Hiệp PV, Hoang G, et al. Hydroxyapatite nano bioceramics optimized 3D printed poly lactic acid scaffold for bone tissue engineering application. Ceram Int [Internet]. 2020;46(3):3443–3455. Available from: https://doi.org/10.1016/j.ceramint.2019.10.057

Talal A, Waheed N, Al-Masri M, McKay IJ, et al. Absorption and release of protein from hydroxyapatite-polylactic acid (HA-PLA) membranes. J Dent [Internet]. 2009;37(11):820–826. Available from: https://doi.org/10.1016/j.jdent.2009.06.014

Thanh DTM, Trang PTT, Thom NT, Phuong NT, et al. Effects of Porogen on Structure and Properties of Poly Lactic Acid/Hydroxyapatite Nanocomposites (PLA/HAp). J Nanosci Nanotechnol [Internet]. 2016;16(9):9450–9459. Available from: https://doi.org/10.1166/jnn.2016.12032

Zhang H, Fu Q-W, Sun T-W, Chen F, et al. Amorphous calcium phosphate, hydroxyapatite and poly(D,L-lactic acid) composite nanofibers: Electrospinning preparation, mineralization and in vivo bone defect repair. Colloids Surf B [Internet]. 2015;136:27–36. Available from: http://dx.doi.org/10.1016/j.colsurfb.2015.08.015

Moura NKd, Siqueira IAWB, Machado JPdB, Kido HW, et al. Production and Characterization of Porous Polymeric Membranes of PLA/PCL Blends with the Addition of Hydroxyapatite. J Compos Sci [Internet]. 2019;3(2):45. Available from: https://doi.org/10.3390/jcs3020045

Zhang J, Wang Q, Wang A. In situ generation of sodium alginate/hydroxyapatite nanocomposite beads as drug-controlled release matrices. Acta Biomater [Internet]. 2010;6(2):445–454. Available from: http://dx.doi.org/10.1016/j.actbio.2009.07.001

Sukhodub LF, Sukhodub LB, Litsis O, Prylutskyy Y. Synthesis and characterization of hydroxyapatite-alginate nanostructured composites for the controlled drug release. Mater Chem Phys [Internet]. 2018;217:228–234. Available from: https://doi.org/10.1016/j.matchemphys.2018.06.071

Rossi AL, Barreto IC, Maciel WQ, Rosa FP, et al. Ultrastructure of regenerated bone mineral surrounding hydroxyapatite–alginate composite and sintered hydroxyapatite. Bone [Internet]. 2012;50(1):301–310. Available from: http://dx.doi.org/10.1016/j.bone.2011.10.022

Rajkumar M, Meenakshisundaram N, Rajendran V. Development of nanocomposites based on hydroxyapatite/sodium alginate: Synthesis and characterisation. Mater Charact [Internet]. 2011;62(5):469–479. Available from: http://dx.doi.org/10.1016/j.matchar.2011.02.008

Rajesh R, Ravichandran YD. Development of a new carbon nanotube–alginate–hydroxyapatite tricomponent composite scaffold for application in bone tissue engineering. Int J Nanomedicine [Internet]. 2015;10:7-15. Available from: https://doi.org/10.2147/IJN.S79971

Mahmoud EM, Sayed M, El-Kady AM, Elsayed H, et al. In vitro and in vivo study of naturally derived alginate / hydroxyapatite bio composite scaffolds. Int J Biol Macromol [Internet]. 2020;165:1346–1360. Available from: https://doi.org/10.1016/j.ijbiomac.2020.10.014

Gholizadeh BS, Buazar F, Hosseini SM, Mousavi SM. Enhanced antibacterial activity, mechanical and physical properties of alginate/hydroxyapatite bionanocomposite film. Int J Biol Macromol [Internet]. 2018;116:786–792. Available from: https://doi.org/10.1016/j.ijbiomac.2018.05.104

Bian T, Xing H. A collagen (Col)/nano-hydroxyapatite (nHA) biological composite bone scaffold with double multi-level interface reinforcement. Arab J Chem [Internet]. 2022;15(5):103733. Available from: https://doi.org/10.1016/j.arabjc.2022.103733

Bian T, Zhao K, Meng Q, Tang Y, et al. The construction and performance of multi-level hierarchical hydroxyapatite (HA)/ collagen composite implant based on biomimetic bone Haversian motif. Mater Des [Internet]. 2019;162:60–69. Available from: https://doi.org/10.1016/j.matdes.2018.11.040

Yilmaz E, Çakıroğlu B, Gökçe A, Findik F, et al. Novel hydroxyapatite/graphene oxide/collagen bioactive composite coating on Ti16Nb alloys by electrodeposition. Mater Sci Eng C [Internet]. 2019;101:292–305. Available from: https://doi.org/10.1016/j.msec.2019.03.078

Sun R-X, Lv Y, Niu Y-R, Zhao X-H, et al. Physicochemical and biological properties of bovine-derived porous hydroxyapatite/collagen composite and its hydroxyapatite powders. Ceram Int [Internet]. 2017;43(18):16792–16798. Available from: http://dx.doi.org/10.1016/j.ceramint.2017.09.075

Li H, Sun X, Li Y, Wang H, et al. Carbon nanotube-collagen@hydroxyapatite composites with improved mechanical and biological properties fabricated by a multi in situ synthesis process. Biomed Microdevices [Internet]. 2020;22:64. Available from: https://doi.org/10.1007/s10544-020-00520-5

Siswanto S, Hikmawati D, Kulsum U, Rudyardjo DI, et al. Biocompatibility and osteoconductivity of scaffold porous composite collagen–hydroxyapatite based coral for bone regeneration. Open Chem [Internet]. 2020;18(1):584–590. Available from: https://doi.org/10.1515/chem-2020-0080

Kane RJ, Weiss-Bilka HE, Meagher MJ, Liu Y, et al. Hydroxyapatite reinforced collagen scaffolds with improved architecture and mechanical properties. Acta Biomater [Internet]. 2015;17:16–25. Available from: http://dx.doi.org/10.1016/j.actbio.2015.01.031

Sionkowska A, Kozłowska J. Properties and modification of porous 3-D collagen/hydroxyapatite composites. Int J Biol Macromol [Internet]. 2013;52(1):250–259. Available from: http://dx.doi.org/10.1016/j.ijbiomac.2012.10.002

Zvicer J, Medic A, Veljovic D, Jevtic S, et al. Biomimetic characterization reveals enhancement of hydroxyapatite formation by fluid flow in gellan gum and bioactive glass composite scaffolds. Polym Test [Internet]. 2019;76:464–472. Available from: https://doi.org/10.1016/j.polymertesting.2019.04.004

Bastos AR, Raquel Maia F, Miguel Oliveira J, Reis RL, et al. Influence of gellan gum-hydroxyapatite spongy-like hydrogels on human osteoblasts under long-term osteogenic differentiation conditions. Mater Sci Eng C [Internet]. 2021;129:112413. Available from: https://doi.org/10.1016/j.msec.2021.112413

Anandan D, Madhumathi G, Nambiraj NA, Jaiswal AK. Gum based 3D composite scaffolds for bone tissue engineering applications. Carbohydr Polym [Internet]. 2019;214:62–70. Available from: https://doi.org/10.1016/j.carbpol.2019.03.020

Jamshidi P, Chouhan G, Williams RL, Cox SC, et al. Modification of gellan gum with nanocrystalline hydroxyapatite facilitates cell expansion and spontaneous osteogenesis. Biotechnol Bioeng [Internet]. 2016;113(7):1568–1576. Available from: https://doi.org/10.1002/bit.25915

Manda MG, da Silva LP, Cerqueira MT, Pereira DR, et al. Gellan gum-hydroxyapatite composite spongy-like hydrogels for bone tissue engineering. J Biomed Mater Res Part A [Internet]. 2018;106(2):479–490. Available from: https://doi.org/10.1002/jbm.a.36248

dos Santos MVB, Bastos Nogueira Rocha L, Gomes Vieira E, Leite Oliveira A, et al. Development of Composite Scaffolds Based on Cerium Doped-Hydroxyapatite and Natural Gums—Biological and Mechanical Properties. Materials [Internet]. 2019;12(15):2389. Available from: https://doi.org/10.3390/ma12152389

Heidari F, Razavi M, E.Bahrololoom M, Bazargan-Lari R, et al. Mechanical properties of natural chitosan/hydroxyapatite/magnetite nanocomposites for tissue engineering applications. Mater Sci Eng C [Internet]. 2016;65:338–344. Available from: http://dx.doi.org/10.1016/j.msec.2016.04.039

Shavandi A, Bekhit AE-DA, Ali MA, Sun Z, et al. Development and characterization of hydroxyapatite/β-TCP/chitosan composites for tissue engineering applications. Mater Sci Eng C [Internet]. 2015;56:481–493. Available from: http://dx.doi.org/10.1016/j.msec.2015.07.004

Ghosh S, Ghosh S, Pramanik N. Bio-evaluation of doxorubicin (DOX)-incorporated hydroxyapatite (HAp)-chitosan (CS) nanocomposite triggered on osteosarcoma cells. Adv Compos Hybrid Mater [Internet]. 2020;3(3):303–314. Available from: https://doi.org/10.1007/s42114-020-00154-4

Gritsch L, Maqbool M, Mouriño V, Ciraldo FE, et al. Chitosan/hydroxyapatite composite bone tissue engineering scaffolds with dual and decoupled therapeutic ion delivery: copper and strontium. J Mater Chem B [Internet]. 2019;7(40):6109–6124. Available from: https://doi.org/10.1039/C9TB00897G

Chen L, Hu J, Shen X, Tong H. Synthesis and characterization of chitosan–multiwalled carbon nanotubes/hydroxyapatite nanocomposites for bone tissue engineering. J Mater Sci: Mater Med [Internet]. 2013;24(8):1843–1851. Available from: https://doi.org/10.1007/s10856-013-4954-x

Li X, Nan K, Shi S, Chen H. Preparation and characterization of nano-hydroxyapatite/chitosan cross-linking composite membrane intended for tissue engineering. Int J Biol Macromol [Internet]. 2012;50(1):43–49. Available from: http://dx.doi.org/10.1016/j.ijbiomac.2011.09.021

Saravanan S, Nethala S, Pattnaik S, Tripathi A, et al. Preparation, characterization and antimicrobial activity of a bio-composite scaffold containing chitosan/nano-hydroxyapatite/nano-silver for bone tissue engineering. Int J Biol Macromol [Internet]. 2011;49(2):188–193. Available from: http://dx.doi.org/10.1016/j.ijbiomac.2011.04.010

Zhang J, Nie J, Zhang Q, Li Y, et al. Preparation and characterization of bionic bone structure chitosan/hydroxyapatite scaffold for bone tissue engineering. J Biomater Sci Polym Ed [Internet]. 2014;25(1):61–74. Available from: https://doi.org/10.1080/09205063.2013.836950

Carfì Pavia F, Conoscenti G, Greco S, La Carrubba V, et al. Preparation, characterization and in vitro test of composites poly-lactic acid/hydroxyapatite scaffolds for bone tissue engineering. Int J Biol Macromol [Internet]. 2018;119:945–953. Available from: https://doi.org/10.1016/j.ijbiomac.2018.08.007

Ma B, Han J, Zhang S, Liu F, et al. Hydroxyapatite nanobelt/polylactic acid Janus membrane with osteoinduction/barrier dual functions for precise bone defect repair. Acta Biomater [Internet]. 2018;71:108–117. Available from: https://doi.org/10.1016/j.actbio.2018.02.033

Anita Lett J, Sagadevan S, Paiman S, Mohammad F, et al. Exploring the thumbprints of Ag-hydroxyapatite composite as a surface coating bone material for the implants. J Mater Res Technol [Internet]. 2020;9(6):12824–12833. Available from: https://doi.org/10.1016/j.jmrt.2020.09.037

Chuan D, Fan R, Wang Y, Ren Y, et al. Stereocomplex poly(lactic acid)-based composite nanofiber membranes with highly dispersed hydroxyapatite for potential bone tissue engineering. Compos Sci Technol [Internet]. 2020;192:108107. Available from: https://doi.org/10.1016/j.compscitech.2020.108107

Zare RN, Doustkhah E, Assadi MHN. Three-dimensional bone printing using hydroxyapatite-PLA composite. Mater Today Proc [Internet]. 2021;42(3):1531–1533. Available from: https://doi.org/10.1016/j.matpr.2019.12.046

Alksne M, Kalvaityte M, Simoliunas E, Rinkunaite I, et al. In vitro comparison of 3D printed polylactic acid/hydroxyapatite and polylactic acid/bioglass composite scaffolds: Insights into materials for bone regeneration. J Mech Behav Biomed Mater [Internet]. 2020;104:103641. Available from: https://doi.org/10.1016/j.jmbbm.2020.103641

Zhang H, Mao X, Zhao D, Jiang W, et al. Three dimensional printed polylactic acid-hydroxyapatite composite scaffolds for prefabricating vascularized tissue engineered bone: An in vivo bioreactor model. Sci Rep [Internet]. 2017;7(1):15255. Available from: http://dx.doi.org/10.1038/s41598-017-14923-7