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Enhancing bone tissue regeneration: a review synergistic hydrogel approach for comprehensive bone repair

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Abstract

A comprehensive approach to utilization of optimal materials derived from hydroxyapatite and chitosan for mending bone fractures has been studied. These materials consist of granules and hydrogel components encompassing essential constituents such as Ca2+ (calcium), PO43− (phosphate), OH− (hydroxyl), and NH2 (amino), which play a pivotal role in absorbing material ions within fractured bones, facilitating osteoconduction. The study demonstrates the efficacy of the freeze-drying method as a versatile technique for creating hydrogels for bone repair. This method encompasses three primary phases: freezing (ensuring sample solidification), primary drying (sublimating frozen water), and secondary drying (eliminating unfrozen water). Concurrently, the article highlights the process of osteoinduction, involving the stimulation of new bone tissue growth facilitated by osteoblasts. These osteoblasts contribute to bone metabolism by synthesizing diverse bone matrix proteins, regulating matrix mineralization, and overseeing osteoclastic activities, angiogenesis, thereby fostering enhanced bone formation within soft tissue. Additionally, this process activates expedited bone growth in stem cells and blood within bone structures.

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References

  1. L Li H Lu Y Zhao 2019 Functionalized cell-free scaffolds for bone defect repair inspired by self-healing of bone fractures: a review and new perspectives Mater Sci Eng C 98 1241 1251

    Article  CAS  Google Scholar 

  2. S Wang W He H Wang 2023 Bioactive materials hematoma-like dynamic hydrogelation through natural glycopeptide molecular recognition for infected bone fracture repair Bioact Mater 30 73 84

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Y Sawatari Y Alshamrani 2019 Concurrent hyoid bone fracture associated with multiple facial fractures secondary to assault: case report and review of literature Oral Maxillofac Surg Cases 5 100119

    Article  Google Scholar 

  4. BH Shares CO Smith TJ Sheu 2020 Inhibition of the mitochondrial permeability transition improves bone fracture repair Bone 137 115391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. NM Ergul S Unal I Kartal 2019 3D printing of chitosan/poly(vinyl alcohol) hydrogel containing synthesized hydroxyapatite scaffolds for hard-tissue engineering Polym Test 79 106006

    Article  CAS  Google Scholar 

  6. B Li L Wang Y Hao 2015 Ultraviolet-crosslinkable and injectable chitosan/hydroxyapatite hybrid hydrogel for critical size calvarial defect repair in vivo J Nanotechnol Eng Med 6 2 7

    Article  Google Scholar 

  7. A Merivaara J Zini E Koivunotko 2021 Preservation of biomaterials and cells by freeze-drying: change of paradigm J Control Release 336 480 498

    Article  CAS  PubMed  Google Scholar 

  8. M Wang X Feng T Wang 2016 Synthesis and characterization of an injectable and self-curing poly(methyl methacrylate) cement functionalized with a biomimetic chitosan-poly(vinyl alcohol)/nano-sized hydroxyapatite/silver hydrogel RSC Adv 6 60609 60619

    Article  CAS  Google Scholar 

  9. Z Zou L Wang Z Zhou 2021 Simultaneous incorporation of PTH (1–34) and nano-hydroxyapatite into chitosan/alginate hydrogels for efficient bone regeneration Bioact Mater 6 1839 1851

    CAS  PubMed  Google Scholar 

  10. X He Z Huang W Liu 2021 Electrospun polycaprolactone/hydroxyapatite/ZnO films as potential biomaterials for application in bone-tendon interface repair Coll Surf B Biointerfaces 204 111825

    Article  CAS  Google Scholar 

  11. C Gao Y Cai X Kong 2013 Development and characterization of injectable chitosan-based hydrogels containing dexamethasone/rhBMP-2 loaded hydroxyapatite nanoparticles Mater Lett 93 312 315

    Article  CAS  Google Scholar 

  12. GA Fielding M Roy A Bandyopadhyay 2012 Antibacterial and biological characteristics of silver containing and strontium doped plasma sprayed hydroxyapatite coatings Acta Biomater 8 3144 3152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. X Ding X Li C Li 2019 Chitosan/dextran hydrogel constructs containing strontium-doped hydroxyapatite with enhanced osteogenic potential in rat cranium ACS Biomater Sci Eng 5 4574 4586

    Article  CAS  PubMed  Google Scholar 

  14. DY Ji TF Kuo WuH Da 2012 A novel injectable chitosan/polyglutamate polyelectrolyte complex hydrogel with hydroxyapatite for soft-tissue augmentation Carbohydr Polym 89 1123 1130

    Article  CAS  PubMed  Google Scholar 

  15. A Rogina A Ressler I Matić 2017 Cellular hydrogels based on pH-responsive chitosan-hydroxyapatite system Carbohydr Polym 166 173 182

    Article  CAS  PubMed  Google Scholar 

  16. M Kardan-Halvaei MR Morovvati SN Angili 2023 Fabrication of 3D-printed hydroxyapatite using freeze-drying method for bone regeneration: RVE and finite element simulation analysis J Mater Res Technol 24 8682 8692

    Article  CAS  Google Scholar 

  17. M Sayed EM Mahmoud F Bondioli 2019 Developing porous diopside/hydroxyapatite bio-composite scaffolds via a combination of freeze-drying and coating process Ceram Int 45 9025 9031

    Article  CAS  Google Scholar 

  18. TR Kim TS Goh JS Lee 2023 Experimental and numerical investigations for compressive behavior of porous hydroxyapatite bone scaffold fabricated via freeze-gel casting method Mater Des 231 112080

    Article  CAS  Google Scholar 

  19. F Qiao X Ma X Qiu 2024 Nuclear inst. and methods in physics research, a enhancing stability of microchannel plates (MCPs) through freeze-drying method Nucl Inst Methods Phys Res A 1062 169205

    Article  CAS  Google Scholar 

  20. SA Ledri JM Milani SA Shahidi 2024 Comparative analysis of freeze drying and spray drying methods for encapsulation of chlorophyll with maltodextrin and whey protein isolate Food Chem X 21 101156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. MJ Pikal S Shah ML Roy 1990 The secondary drying stage of freeze drying: drying kinetics as a function of temperature and chamber pressure Int J Pharm 60 203 207

    Article  CAS  Google Scholar 

  22. K Zafeiris D Brasinika A Karatza 2021 Additive manufacturing of hydroxyapatite–chitosan–genipin composite scaffolds for bone tissue engineering applications Mater Sci Eng C 119 111639

    Article  CAS  Google Scholar 

  23. S Deville 2008 Freeze-casting of porous ceramics: a review of current achievements and issues Adv Eng Mater 10 155 169

    Article  CAS  Google Scholar 

  24. K Taecha-apaikun P Pisek J Suwanprateeb 2021 In vitro resorbability and granular characteristics of 3D-printed hydroxyapatite granules versus allograft, xenograft, and alloplast for alveolar cleft surgery applications Proc Inst Mech Eng Part H J Eng Med 235 1288 1296

    Article  Google Scholar 

  25. MF Mohd Yusoff NH Abu Kasim WH Himratul-Aznita 2021 Physicochemical, antibacterial and biocompatibility assessments of silver incorporated nano-hydroxyapatite synthesized using a novel microwave-assisted wet precipitation technique Mater Charact 178 111169

    Article  CAS  Google Scholar 

  26. NA Sajahan WMA Wan Ibrahim 2014 Microwave irradiation of nanohydroxyapatite from chicken eggshells and duck eggshells Sci World J 2014 275984

    Article  Google Scholar 

  27. F Piri A Mollahosseini A Khadir 2020 Synthesis of a novel magnetic zeolite–hydroxyapatite adsorbent via microwave-assisted method for protein adsorption via magnetic solid-phase extraction J Iran Chem Soc 17 1635 1648

    Article  CAS  Google Scholar 

  28. BK Preetha B Vishalakshi 2020 Microwave assisted synthesis of karaya gum based montmorillonite nanocomposite: characterisation, swelling and dye adsorption studies Int J Biol Macromol 154 739 750

    Article  CAS  PubMed  Google Scholar 

  29. L Zhang GJ Zheng YT Guo 2014 Preparation of novel biodegradable pHEMA hydrogel for a tissue engineering scaffold by microwave-assisted polymerization Asian Pac J Trop Med 7 136 140

    Article  CAS  PubMed  Google Scholar 

  30. RC Silva da SB Aguiar de PLR Cunha da 2020 Effect of microwave on the synthesis of polyacrylamide-g-chitosan gel for azo dye removal React Funct Polym 148 104491

    Article  Google Scholar 

  31. D Shi H Tong M Lv 2021 Optimization of hydrothermal synthesis of hydroxyapatite from chicken eggshell waste for effective adsorption of aqueous Pb(II) Environ Sci Pollut Res 28 58189 58205

    Article  CAS  Google Scholar 

  32. E Vieira M Silva A Maia-Filho 2021 Effect of cerium-containing hydroxyapatite in bone repair in female rats with osteoporosis induced by ovariectomy Minerals 11 2075

    Article  Google Scholar 

  33. DV Abere SA Ojo GM Oyatogun 2022 Mechanical and morphological characterization of nano-hydroxyapatite (nHA) for bone regeneration: a mini review Biomed Eng Adv 4 100056

    Article  Google Scholar 

  34. YW Ge M Chu ZY Zhu 2022 Nacre-inspired magnetically oriented micro-cellulose fibres/nano-hydroxyapatite/chitosan layered scaffold enhances pro-osteogenesis and angiogenesis Mater Today Bio 16 100439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. CM Tang FY Fan YC Ke 2021 Effects of electrode plate annealing treatment and the addition of hydrogen peroxide on improving the degradation of cobalt hydroxyapatite for bone repair Mater Chem Phys 259 123962

    Article  CAS  Google Scholar 

  36. F Xing Z Chi R Yang 2021 Chitin-hydroxyapatite-collagen composite scaffolds for bone regeneration Int J Biol Macromol 184 170 180

    Article  CAS  PubMed  Google Scholar 

  37. K Lavanya SV Chandran K Balagangadharan 2020 Temperature- and pH-responsive chitosan-based injectable hydrogels for bone tissue engineering Mater Sci Eng C 111 110862

    Article  CAS  Google Scholar 

  38. V Jahed E Vasheghani-Farahani F Bagheri 2020 Quantum dots-βcyclodextrin-histidine labeled human adipose stem cells-laden chitosan hydrogel for bone tissue engineering Nanomed Nanotechnol Biol Med 27 102217

    Article  CAS  Google Scholar 

  39. MH Malik L Shahzadi R Batool 2020 Thyroxine-loaded chitosan/carboxymethyl cellulose/hydroxyapatite hydrogels enhance angiogenesis in in-ovo experiments Int J Biol Macromol 145 1162 1170

    Article  CAS  PubMed  Google Scholar 

  40. L Ma W Su Y Ran 2020 Synthesis and characterization of injectable self-healing hydrogels based on oxidized alginate-hybrid-hydroxyapatite nanoparticles and carboxymethyl chitosan Int J Biol Macromol 165 1164 1174

    Article  CAS  PubMed  Google Scholar 

  41. N Tamai A Myoui T Tomita 2009 Interconnected porous hydroxyapatite ceramics for bone tissue engineering J R Soc Interface 6 341 348

    Google Scholar 

  42. AK Gosain PA Riordan L Song 2004 A 1-year study of osteoinduction in hydroxyapatite-derived biomaterials in an adult sheep model: part II. Bioengineering implants to optimize bone replacement in reconstruction of cranial defects Plast Reconstr Surg 114 1155 1163

    Article  PubMed  Google Scholar 

  43. M Murata J Hino MA Kabir 2021 Osteoinduction in novel micropores of partially dissolved and precipitated hydroxyapatite block in scalp of young rats Materials (Basel) 14 1 9

    Article  Google Scholar 

  44. A Pistone D Iannazzo C Celesti 2020 Chitosan/PAMAM/Hydroxyapatite engineered drug release hydrogels with tunable rheological properties Polymers (Basel) 12 3390

    Article  Google Scholar 

  45. Y Huang X Zhang A Wu 2016 An injectable nano-hydroxyapatite (n-HA)/glycol chitosan (G-CS)/hyaluronic acid (HyA) composite hydrogel for bone tissue engineering RSC Adv 6 33529 33536

    Article  CAS  Google Scholar 

  46. A Kaviani SM Zebarjad S Javadpour 2019 Fabrication and characterization of low-cost freeze-gelated chitosan/collagen/hydroxyapatite hydrogel nanocomposite scaffold Int J Polym Anal Charact 24 191 203

    Article  CAS  Google Scholar 

  47. GF Zuo YZ Wan ZJ Liu 2014 Preparation and characterisation of laminated hydroxyapatite/chitosan composite hydrogels Plast Rubber Compos 43 71 75

    Article  CAS  Google Scholar 

  48. Y Chen F Zhang Q Fu 2016 In vitro proliferation and osteogenic differentiation of human dental pulp stem cells in injectable thermo-sensitive chitosan/β-glycerophosphate/hydroxyapatite hydrogel J Biomater Appl 31 317 327

    Article  CAS  PubMed  Google Scholar 

  49. Y Sa M Wang H Deng 2015 Beneficial effects of biomimetic nano-sized hydroxyapatite/antibiotic gentamicin enriched chitosan-glycerophosphate hydrogel on the performance of injectable polymethylmethacrylate RSC Adv 5 91082 91092

    Article  CAS  Google Scholar 

  50. X Liu Y Chen Q Huang 2014 A novel thermo-sensitive hydrogel based on thiolated chitosan/hydroxyapatite/beta-glycerophosphate Carbohydr Polym 110 62 69

    Article  CAS  PubMed  Google Scholar 

  51. K Madhumathi KT Shalumon VVD Rani 2009 Wet chemical synthesis of chitosan hydrogel-hydroxyapatite composite membranes for tissue engineering applications Int J Biol Macromol 45 12 15

    Article  CAS  PubMed  Google Scholar 

  52. GR Mahdavinia MH Karimi M Soltaniniya 2019 In vitro evaluation of sustained ciprofloxacin release from κ-carrageenan-crosslinked chitosan/hydroxyapatite hydrogel nanocomposites Int J Biol Macromol 126 443 453

    Article  CAS  PubMed  Google Scholar 

  53. M Wang Y Sa P Li 2018 A versatile and injectable poly(methyl methacrylate) cement functionalized with quaternized chitosan-glycerophosphate/nanosized hydroxyapatite hydrogels Mater Sci Eng C 90 264 272

    Article  CAS  Google Scholar 

  54. Y Tang Y Du Y Li 2009 A thermosensitive chitosan/poly(vinyl alcohol) hydrogel containing hydroxyapatite for protein delivery J Biomed Mater Res Part A 91 953 963

    Article  Google Scholar 

  55. X Li B Ma J Li 2020 A method to visually observe the degradation-diffusion-reconstruction behavior of hydroxyapatite in the bone repair process Acta Biomater 101 554 564

    Article  CAS  PubMed  Google Scholar 

  56. J Han B Ma H Liu 2018 Hydroxyapatite nanowires modified polylactic acid membrane plays barrier/osteoinduction dual roles and promotes bone regeneration in a rat mandible defect model J Biomed Mater Res Part A 106 3099 3110

    Article  CAS  Google Scholar 

  57. L Xiong J Zeng A Yao 2015 BMP2-loaded hollow hydroxyapatite microspheres exhibit enhanced osteoinduction and osteogenicity in large bone defects Int J Nanomedicine 10 517 526

    Article  PubMed  PubMed Central  Google Scholar 

  58. T Xu X He Z Chen 2019 Effect of magnesium particle fraction on osteoinduction of hydroxyapatite sphere-based scaffolds J Mater Chem B 7 5648 5660

    Article  CAS  PubMed  Google Scholar 

  59. SC Heo BR Keum EJ Seo 2023 Lysophosphatidic acid induces proliferation and osteogenic differentiation of human dental pulp stem cell through lysophosphatidic acid receptor 3/extracellular signal-regulated kinase signaling axis J Dent Sci 18 1219 1226

    Article  PubMed  PubMed Central  Google Scholar 

  60. W Zhi X Wang D Sun 2022 Optimal regenerative repair of large segmental bone defect in a goat model with osteoinductive calcium phosphate bioceramic implants Bioact Mater 11 240 253

    CAS  PubMed  Google Scholar 

  61. W Jing M Zhang L Jin 2015 Assessment of osteoinduction using a porous hydroxyapatite coating prepared by micro-arc oxidation on a new titanium alloy Int J Surg 24 51 56

    Article  PubMed  Google Scholar 

  62. B Ma J Han S Zhang 2018 Hydroxyapatite nanobelt/polylactic acid Janus membrane with osteoinduction/barrier dual functions for precise bone defect repair Acta Biomater 71 108 117

    Article  CAS  PubMed  Google Scholar 

  63. L Cheng F Ye R Yang 2010 Osteoinduction of hydroxyapatite/β-tricalcium phosphate bioceramics in mice with a fractured fibula Acta Biomater 6 1569 1574

    Article  CAS  PubMed  Google Scholar 

  64. Y Tan Z Qiu H Zeng 2023 Microcystin-leucine-arginine impairs bone microstructure and biomechanics by activating osteoimmune response and inhibiting osteoblasts maturation in developing rats Toxicology 494 153595

    Article  CAS  PubMed  Google Scholar 

  65. N Akiyama M Takemoto S Fujibayashi 2011 Difference between dogs and rats with regard to osteoclast-like cells in calcium-deficient hydroxyapatite-induced osteoinduction J Biomed Mater Res Part A 96A 402 412

    Article  CAS  Google Scholar 

  66. JD Bruijn De 2004 A 1-year study of osteoinduction in hydroxyapatite-derived biomaterials in an adult sheep model: part II. Bioengineering implants to optimize bone replacement in reconstruction of cranial defects: discussion Plast Reconstr Surg 114 1164 1165

    Article  Google Scholar 

  67. L Ho Khanh Hy D Viet Ha P Xuan Ky 2021 Preparation of nano-hydroxyapatite obtained from lates calcarifer fish bone by alkaline hydrolysis method Am J Chem Biochem Eng 5 32

    Article  Google Scholar 

  68. M Lu H Chen B Yuan 2020 The morphological effect of nanostructured hydroxyapatite coatings on the osteoinduction and osteogenic capacity of porous titanium Nanoscale 12 24085 24099

    Article  CAS  PubMed  Google Scholar 

  69. F Liu X Wang T Chen 2020 Hydroxyapatite/silver electrospun fibers for anti-infection and osteoinduction J Adv Res 21 91 102

    Article  CAS  PubMed  Google Scholar 

  70. M Li MJ Mondrinos X Chen 2006 Elastin blends for tissue engineering scaffolds J Biomed Mater Res Part A 79 963 973

    Article  Google Scholar 

  71. C Wu G Wang Q Yan 2019 Silk fibroin regulates osteoconduction of hydroxyapatite in rat spine fusion model J Hard Tissue Biol 28 341 348

    Article  CAS  Google Scholar 

  72. R Kiyama T Nonoyama S Wada 2018 Micro patterning of hydroxyapatite by soft lithography on hydrogels for selective osteoconduction Acta Biomater 81 60 69

    Article  CAS  PubMed  Google Scholar 

  73. H Denissen R Martinetti LA Van 2005 Calcium phosphate drug delivery system: influence of local zoledronate release on bone implant osteointegration Bone 36 52 60

    Article  Google Scholar 

  74. X Li Q Zhou Y Wu 2022 Enhanced bone regenerative properties of calcium phosphate ceramic granules in rabbit posterolateral spinal fusion through a reduction of grain size Bioact Mater 11 90 106

    CAS  PubMed  Google Scholar 

  75. B Zheng OP Leary DD Liu 2022 Radiographic analysis of neuroforaminal and central canal decompression following lateral lumbar interbody fusion North Am Spine Soc J 10 100110

    Google Scholar 

  76. X Shang yan, Zhou Z guan, Yan K, 2023 Interfacial fracture performance of engineered cementitious composites and fire-damaged concrete Case Stud Constr Mater 19 e02167

    Google Scholar 

  77. W Cai X Xu Y Jiang 2023 Programmed release of hydrogel microspheres via regulating the immune microenvironment to promotes bone repair Mater Today Adv 18 100381

    Article  CAS  Google Scholar 

  78. J Gao M Wang C Shi 2017 A facile green synthesis of trace Si, Sr and F multi-doped hydroxyapatite with enhanced biocompatibility and osteoconduction Mater Lett 196 406 409

    Article  CAS  Google Scholar 

  79. H Zhao J Tang D Zhou 2020 Electrospun icariin-loaded core-shell collagen, polycaprolactone, hydroxyapatite composite scaffolds for the repair of rabbit tibia bone defects Int J Nanomedicine 15 3039 3056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. G Spence S Phillips C Campion 2008 Bone formation in a carbonate-substituted hydroxyapatite implant is inhibited by zoledronate: The importance of bioresorption to osteoconduction J Bone Jt Surg - Ser B 90 1635 1640

    Article  CAS  Google Scholar 

  81. LCA Pires de RC Silva da PP Poli 2020 Evaluation of osteoconduction of a synthetic hydroxyapatite/β-tricalcium phosphate block fixed in rabbit mandibles Materials (Basel) 13 1 16

    Article  Google Scholar 

  82. BS Chang CK Lee KS Hong 2000 Osteoconduction at porous hydroxyapatite with various pore configurations Biomaterials 21 1291 1298

    Article  CAS  PubMed  Google Scholar 

  83. R Chakraborty VS Seesala M Sen 2017 MWCNT reinforced bone like calcium phosphate—hydroxyapatite composite coating developed through pulsed electrodeposition with varying amount of apatite phase and crystallinity to promote superior osteoconduction, cytocompatibility and corrosion protection Surf Coatings Technol 325 496 514

    Article  CAS  Google Scholar 

  84. R Chakraborty VS Seesala S Sengupta 2018 Comparison of Osteoconduction, cytocompatibility and corrosion protection performance of hydroxyapatite-calcium hydrogen phosphate composite coating synthesized in-situ through pulsed electro-deposition with varying amount of phase and crystallinity Surf Interfaces 10 1 10

    Article  CAS  Google Scholar 

  85. ECC Reis APB Borges CC Fonseca 2010 Biodegradation of a hydroxyapatite-polyhydroxybutyrate composite Brazilian Arch Biol Technol 53 817 826

    Article  Google Scholar 

  86. M Azevedo e Sousa Munhoz de KT Pomini AM Guzzi Plepis de 2020 Elastin-derived scaffolding associated or not with bone morphogenetic protein (BMP) or hydroxyapatite (HA) in the repair process of metaphyseal bone defects PLoS One 15 1 21

    Google Scholar 

  87. M Du J Chen K Liu 2021 Recent advances in biomedical engineering of nano-hydroxyapatite including dentistry, cancer treatment and bone repair Compos Part B Eng 215 108790

    Article  CAS  Google Scholar 

  88. A Luca De I Vitrano V Costa 2020 Improvement of osteogenic differentiation of human mesenchymal stem cells on composite poly L-lactic acid/nano-hydroxyapatite scaffolds for bone defect repair J Biosci Bioeng 129 250 257

    Article  PubMed  Google Scholar 

  89. H Yan Z Wang L Li 2021 DOPA-derived electroactive copolymer and IGF-1 immobilized poly(lactic-co-glycolic acid)/hydroxyapatite biodegradable microspheres for synergistic bone repair Chem Eng J. 416 129129

    Article  CAS  Google Scholar 

  90. YM Chen CE Kuo GR Chen 2014 Functional analysis of an orange-spotted grouper (Epinephelus coioides) interferon gene and characterisation of its expression in response to nodavirus infection Dev Comp Immunol 46 117 128

    Article  CAS  PubMed  Google Scholar 

  91. MM Alwani MZ Saltagi ME MacPhail 2021 Middle cranial fossa repair of temporal bone spontaneous csf leaks with hydroxyapatite bone cement Laryngoscope 131 624 632

    Article  CAS  PubMed  Google Scholar 

  92. T Liu M Jin Y Zhang 2021 K+/Sr2+/Na+ triple-doped hydroxyapatites/GelMA composite hydrogel scaffold for the repair of bone defects Ceram Int 47 30929 30937

    Article  CAS  Google Scholar 

  93. T Levingstone B Ali C Kearney 2021 Hydroxyapatite sonosensitization of ultrasound-triggered, thermally responsive hydrogels: an on-demand delivery system for bone repair applications J Biomed Mater Res Part B Appl Biomater 109 1622 1633

    Article  CAS  Google Scholar 

  94. N Ramesh JTB Ratnayake SC Moratti 2020 Effect of chitosan infiltration on hydroxyapatite scaffolds derived from New Zealand bovine cancellous bones for bone regeneration Int J Biol Macromol 160 1009 1020

    Article  CAS  PubMed  Google Scholar 

  95. M Shakir R Jolly AA Khan 2018 Resol based chitosan/nano-hydroxyapatite nanoensemble for effective bone tissue engineering Carbohydr Polym 179 317 327

    Article  CAS  PubMed  Google Scholar 

  96. J Venkatesan B Lowe P Manivasagan 2015 Isolation and characterization of nano-hydroxyapatite from salmon fish bone Materials (Basel) 8 5426 5439

    Article  CAS  PubMed  Google Scholar 

  97. JB Feng DR Huang M Zhong 2016 Pharmacokinetics of florfenicol and behaviour of its metabolite florfenicol amine in orange-spotted grouper (Epinephelus coioides) after oral administration J Fish Dis 39 833 843

    Article  CAS  PubMed  Google Scholar 

  98. YJ Hsu CY Hou SJ Lin 2013 The biofunction of orange-spotted grouper (Epinephelus coioides) CC chemokine ligand 4 (CCL4) in innate and adaptive immunity Fish Shellfish Immunol 35 1891 1898

    Article  CAS  PubMed  Google Scholar 

  99. C Houng-Yung C Yu-Chun H Li-Chi 2014 Dietary zinc requirements of juvenile grouper Epinephelus malabaricus Aquac 432 360 364

    Article  Google Scholar 

  100. P Ma W Wu Y Wei 2021 Biomimetic gelatin/chitosan/polyvinyl alcohol/nano-hydroxyapatite scaffolds for bone tissue engineering Mater Des 207 109865

    Article  CAS  Google Scholar 

  101. M Aghazadeh M Samiei VR Hokmabad 2018 The effect of melanocyte stimulating hormone and hydroxyapatite on osteogenesis in pulp stem cells of human teeth transferred into polyester scaffolds Fibers Polym 19 2245 2253

    Article  CAS  Google Scholar 

  102. K Okada N Kawao K Tatsumi 2018 Roles of plasminogen in the alterations in bone marrow hematopoietic stem cells during bone repair Bone Reports 8 195 203

    Article  PubMed  PubMed Central  Google Scholar 

  103. V Alonso-Goulart LB Ferreira CA Duarte 2018 Mesenchymal stem cells from human adipose tissue and bone repair: a literature review Biotechnol Res Innov 2 74 80

    Article  Google Scholar 

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  1. Department of Physics, Hasanudin University, Makassar, 90245, Indonesia

    Febrianti Mahrani Kolly, Nurlaela Rauf & Dahlang Tahir

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  1. Febrianti Mahrani Kolly
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Kolly, F.M., Rauf, N. & Tahir, D. Enhancing bone tissue regeneration: a review synergistic hydrogel approach for comprehensive bone repair. Polym. Bull. (2024). https://doi.org/10.1007/s00289-024-05236-7

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