Methods of improving the mechanical properties of hydrogels and their research progress in bone tissue engineering_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LI Yongwei , ZHOU Junpeng , HU Shugang , WANG Jialin , WANG Kunzheng ,  WANG Wei

Department of Bone and Joint Surgery, the Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an Shaanxi, 710004, P.R.China;

Corresponding author：

WANG Wei, Email: dr.wangwei@xjtu.edu.cn

Keywords：

Bone tissue engineering; hydrogels; scaffold material; mechanical property; bone defect repair

DOI：

10.7507/1002-1892.202107053

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To review the methods of improving the mechanical properties of hydrogels and the research progress in bone tissue engineering. Methods The recent domestic and foreign literature on hydrogels in bone tissue engineering was reviewed, and the methods of improving the mechanical properties of hydrogels and the effect of bone repair in vivo and in vitro were summarized. Results Hydrogels are widely used in bone tissue engineering, but their mechanical properties are poor. Improving the mechanical properties of hydrogels can enhance bone repair. The methods of improving the mechanical properties of hydrogels include the construction of dual network structures, inorganic nanoparticle composites, introduction of conductive materials, and fiber network reinforcement. These methods can improve the mechanical properties of hydrogels to various degrees while also demonstrating a significant bone repair impact. Conclusion The mechanical properties of hydrogels can be effectively improved by modifying the system, components, and fiber structure, and bone repair can be effectively promoted.

Citation： LI Yongwei, ZHOU Junpeng, HU Shugang, WANG Jialin, WANG Kunzheng, WANG Wei. Methods of improving the mechanical properties of hydrogels and their research progress in bone tissue engineering. Chinese Journal of Reparative and Reconstructive Surgery, 2021, 35(12): 1615-1622. doi: 10.7507/1002-1892.202107053 Copy

1.	Turnbull G, Clarke J, Picard F, et al. 3D bioactive composite scaffolds for bone tissue engineering. Bioact Mater, 2017, 3(3): 278-314.
2.	McDermott AM, Herberg S, Mason DE, et al. Recapitulating bone development through engineered mesenchymal condensations and mechanical cues for tissue regeneration. Sci Transl Med, 2019, 11(495): eaav7756. doi: 10.1126/scitranslmed.aav7756.
3.	Ashman O, Phillips AM. Treatment of non-unions with bone defects: which option and why? Injury, 2013, 44 Suppl 1: S43-45.
4.	Bhumiratana S, Bernhard JC, Alfi DM, et al. Tissue-engineered autologous grafts for facial bone reconstruction. Sci Transl Med, 2016, 8(343): 343ra83. doi: 10.1126/scitranslmed.aad5904.
5.	García-Gareta E, Coathup MJ, Blunn GW. Osteoinduction of bone grafting materials for bone repair and regeneration. Bone, 2015, 81: 112-121.
6.	Bose S, Sarkar N. Natural medicinal compounds in bone tissue engineering. Trends Biotechnol, 2020, 38(4): 404-417.
7.	吕维加, 李朝阳. 可注射骨修复材料的研发与展望. 骨科临床与研究杂志, 2021, 6(1): 1-6, 19.
8.	Askari M, Afzali Naniz M, Kouhi M, et al. Recent progress in extrusion 3D bioprinting of hydrogel biomaterials for tissue regeneration: a comprehensive review with focus on advanced fabrication techniques. Biomater Sci, 2021, 9(3): 535-573.
9.	Zhang Y, Li Z, Guan J, et al. Hydrogel: A potential therapeutic material for bone tissue engineering. AIP Advances, 2021, 11(1): 010701. doi: 10.1063/5.0035504.
10.	Gong JP, Katsuyama Y, Kurokawa T, et al. Double-network hydrogels with extremely high mechanical strength. Adv Mater, 2003, 15(14): 1155-1158.
11.	Haraguchi K, Takehisa T. Nanocomposite hydrogels: A unique organic-inorganic network structure with extraordinary mechanical, optical, and swelling/de‐swelling properties. Advanced materials, 2002, 14(16): 1120-1124.
12.	Zhang X, Huang P, Jiang G, et al. A novel magnesium ion-incorporating dual-crosslinked hydrogel to improve bone scaffold-mediated osteogenesis and angiogenesis. Mater Sci Eng C Mater Biol Appl, 2021, 121: 111868. doi: 10.1016/j.msec.2021.111868.
13.	Li A, Xu H, Yu P, et al. Injectable hydrogels based on gellan gum promotes in situ mineralization and potential osteogenesis. European Polymer Journal, 2020, 141: 110091. doi: 10.1016/j.eurpolymj.2020.110091.
14.	Xu M, Qin M, Zhang X, et al. Porous PVA/SA/HA hydrogels fabricated by dual-crosslinking method for bone tissue engineering. J Biomater Sci Polym Ed, 2020, 31(6): 816-831.
15.	Bi S, Wang P, Hu S, et al. Construction of physical-crosslink chitosan/PVA double-network hydrogel with surface mineralization for bone repair. Carbohydr Polym, 2019, 224: 115176. doi: 10.1016/j.carbpol.2019.115176.
16.	Dorozhkin SV. A detailed history of calcium orthophosphates from 1770s till 1950. Mater Sci Eng C Mater Biol Appl, 2013, 33(6): 3085-3110.
17.	Wang Y, Cao X, Ma M, et al. A gelMA-PEGDA-nHA composite hydrogel for bone tissue engineering. Materials (Basel), 2020, 13(17): 3735. doi: 10.3390/ma13173735.
18.	Liu C, Wu J, Gan D, et al. The characteristics of mussel-inspired nHA/OSA injectable hydrogel and repaired bone defect in rabbit. J Biomed Mater Res B Appl Biomater, 2020, 108(5): 1814-1825.
19.	Nie L, Wu Q, Long H, et al. Development of chitosan/gelatin hydrogels incorporation of biphasic calcium phosphate nanoparticles for bone tissue engineering. J Biomater Sci Polym Ed, 2019, 30(17): 1636-1657.
20.	Sen KS, Duarte Campos DF, Köpf M, et al. The effect of addition of calcium phosphate particles to hydrogel-based composite materials on stiffness and differentiation of mesenchymal stromal cells toward osteogenesis. Adv Healthc Mater, 2018, 7(18): e1800343. doi: 10.1002/adhm.201800343.
21.	Ye Q, Zhang Y, Dai K, et al. Three dimensional printed bioglass/gelatin/alginate composite scaffolds with promoted mechanical strength, biomineralization, cell responses and osteogenesis. J Mater Sci Mater Med, 2020, 31(9): 77. doi: 10.1007/s10856-020-06413-6.
22.	Killion JA, Kehoe S, Geever LM, et al. Hydrogel/bioactive glass composites for bone regeneration applications: synthesis and characterisation. Mater Sci Eng C Mater Biol Appl, 2013, 33(7): 4203-4212.
23.	Wu J, Zheng K, Huang X, et al. Thermally triggered injectable chitosan/silk fibroin/bioactive glass nanoparticle hydrogels for in-situ bone formation in rat calvarial bone defects. Acta Biomater, 2019, 91: 60-71.
24.	Dawson JI, Oreffo RO. Clay: new opportunities for tissue regeneration and biomaterial design. Adv Mater, 2013, 25(30): 4069-4086.
25.	Mihaila SM, Gaharwar AK, Reis RL, et al. The osteogenic differentiation of SSEA-4 sub-population of human adipose derived stem cells using silicate nanoplatelets. Biomaterials, 2014, 35(33): 9087-9099.
26.	Xavier JR, Thakur T, Desai P, et al. Bioactive nanoengineered hydrogels for bone tissue engineering: a growth-factor-free approach. ACS Nano, 2015, 9(3): 3109-3118.
27.	Guggenheim S, Martin R. Definition of clay and clay mineral: joint report of the AIPEA nomenclature and CMS nomenclature committees. Clays and clay minerals, 1995, 43(2): 255-256.
28.	Han X, Xu H, Che L, et al. Application of inorganic nanocomposite hydrogels in bone tissue engineering. iScience, 2020, 23(12): 101845. doi: 10.1016/j.isci.2020.101845.
29.	Jin Y, Liu C, Chai W, et al. Self-supporting nanoclay as internal scaffold material for direct printing of soft hydrogel composite structures in air. ACS Appl Mater Interfaces, 2017, 9(20): 17456-17465.
30.	Gaharwar AK, Schexnailder PJ, Kline BP, et al. Assessment of using laponite cross-linked poly(ethylene oxide) for controlled cell adhesion and mineralization. Acta Biomater, 2011, 7(2): 568-577.
31.	Liu B, Li J, Lei X, et al. Cell-loaded injectable gelatin/alginate/LAPONITE^® nanocomposite hydrogel promotes bone healing in a critical-size rat calvarial defect model. RSC Advances, 2020, 10(43): 25652-25661.
32.	Ou Q, Huang K, Fu C, et al. Nanosilver-incorporated halloysite nanotubes/gelatin methacrylate hybrid hydrogel with osteoimmunomodulatory and antibacterial activity for bone regeneration. Chemical Engineering Journal, 2020, 382: 123019. doi: 10.1016/j.cej.2019.123019.
33.	Pietraszek A, Ledwójcik G, Lewandowska-Łańcucka J, et al. Bioactive hydrogel scaffolds reinforced with alkaline-phosphatase containing halloysite nanotubes for bone repair applications. Int J Biol Macromol, 2020, 163: 1187-1195.
34.	Cui ZK, Kim S, Baljon JJ, et al. Microporous methacrylated glycol chitosan-montmorillonite nanocomposite hydrogel for bone tissue engineering. Nat Commun, 2019, 10(1): 3523. doi: 10.1038/s41467-019-11511-3.
35.	Lim K, Hexiu J, Kim J, et al. Effects of electromagnetic fields on osteogenesis of human alveolar bone-derived mesenchymal stem cells. Biomed Res Int, 2013, 2013: 296019. doi: 10.1155/2013/296019.
36.	McCullen SD, McQuilling JP, Grossfeld RM, et al. Application of low-frequency alternating current electric fields via interdigitated electrodes: effects on cellular viability, cytoplasmic calcium, and osteogenic differentiation of human adipose-derived stem cells. Tissue Eng Part C Methods, 2010, 16(6): 1377-1386.
37.	Min JH, Patel M, Koh WG. Incorporation of conductive materials into hydrogels for tissue engineering applications. Polymers (Basel), 2018, 10(10): 1078. doi: 10.3390/polym10101078.
38.	Guo B, Ma PX. Conducting polymers for tissue engineering. Biomacromolecules, 2018, 19(6): 1764-1782.
39.	Zare M, Ramezani Z, Rahbar N. Development of zirconia nanoparticles-decorated calcium alginate hydrogel fibers for extraction of organophosphorous pesticides from water and juice samples: Facile synthesis and application with elimination of matrix effects. J Chromatogr A, 2016, 1473: 28-37.
40.	Paquet C, de Haan HW, Leek DM, et al. Clusters of superparamagnetic iron oxide nanoparticles encapsulated in a hydrogel: a particle architecture generating a synergistic enhancement of the T2 relaxation. ACS Nano, 2011, 5(4): 3104-3112.
41.	Xu L, Li X, Takemura T, et al. Genotoxicity and molecular response of silver nanoparticle (NP)-based hydrogel. J Nanobiotechnology, 2012, 10: 16. doi: 10.1186/1477-3155-10-16.
42.	Xing R, Liu K, Jiao T, et al. An injectable self-assembling collagen-gold hybrid hydrogel for combinatorial antitumor photothermal/photodynamic therapy. Adv Mater, 2016, 28(19): 3669-3676.
43.	Ribeiro M, Ferraz MP, Monteiro FJ, et al. Antibacterial silk fibroin/nanohydroxyapatite hydrogels with silver and gold nanoparticles for bone regeneration. Nanomedicine, 2017, 13(1): 231-239.
44.	Heo DN, Ko WK, Bae MS, et al. Enhanced bone regeneration with a gold nanoparticle-hydrogel complex. J Mater Chem B, 2014, 2(11): 1584-1593.
45.	Celikkin N, Mastrogiacomo S, Walboomers XF, et al. Enhancing X-ray attenuation of 3D printed gelatin methacrylate (GelMA) hydrogels utilizing gold nanoparticles for bone tissue engineering applications. Polymers (Basel), 2019, 11(2): 367. doi: 10.3390/polym11020367.
46.	Arvizo RR, Bhattacharyya S, Kudgus RA, et al. Intrinsic therapeutic applications of noble metal nanoparticles: past, present and future. Chem Soc Rev, 2012, 41(7): 2943-2970.
47.	Paun IA, Popescu RC, Calin BS, et al. 3D biomimetic magnetic structures for static magnetic field stimulation of osteogenesis. Int J Mol Sci, 2018, 19(2): 495. doi: 10.3390/ijms19020495.
48.	Uskoković V, Graziani V, Wu VM, et al. Gold is for the mistress, silver for the maid: Enhanced mechanical properties, osteoinduction and antibacterial activity due to iron doping of tricalcium phosphate bone cements. Mater Sci Eng C Mater Biol Appl, 2019, 94: 798-810.
49.	Lin HY, Huang HY, Shiue SJ, et al. Osteogenic effects of inductive coupling magnetism from magnetic 3D printed hydrogel scaffold. Journal of Magnetism and Magnetic Materials, 2020, 504: 166680. doi: 10.1016/j.jmmm.2020.166680.
50.	Farzaneh S, Hosseinzadeh S, Samanipour R, et al. Fabrication and characterization of cobalt ferrite magnetic hydrogel combined with static magnetic field as a potential bio-composite for bone tissue engineering. Journal of Drug Delivery Science and Technology, 2021, 64: 102525. doi: 10.1016/j.jddst.2021.102525.
51.	Lee JH, Shin YC, Lee SM, et al. Enhanced osteogenesis by reduced graphene oxide/hydroxyapatite nanocomposites. Sci Rep, 2015, 5: 18833. doi: 10.1038/srep18833.
52.	Xue D, Chen E, Zhong H, et al. Immunomodulatory properties of graphene oxide for osteogenesis and angiogenesis. Int J Nanomedicine, 2018, 13: 5799-5810.
53.	Mohammadrezaei D, Golzar H, Rezai Rad M, et al. In vitro effect of graphene structures as an osteoinductive factor in bone tissue engineering: A systematic review. J Biomed Mater Res A, 2018, 106(8): 2284-2343.
54.	Kang ES, Kim DS, Suhito IR, et al. Guiding osteogenesis of mesenchymal stem cells using carbon-based nanomaterials. Nano convergence, 2017, 4(1): 1-14.
55.	Pei B, Wang W, Dunne N, et al. Applications of carbon nanotubes in bone tissue regeneration and engineering: superiority, concerns, current advancements, and prospects. Nanomaterials, 2019, 9(10): 1501. doi: 10.3390/nano9101501.
56.	Cha C, Shin SR, Gao X, et al. Controlling mechanical properties of cell-laden hydrogels by covalent incorporation of graphene oxide. Small, 2014, 10(3): 514-523.
57.	Zhou M, Lozano N, Wychowaniec JK, et al. Graphene oxide: A growth factor delivery carrier to enhance chondrogenic differentiation of human mesenchymal stem cells in 3D hydrogels. Acta biomaterialia, 2019, 96: 271-280.
58.	Nosrati H, Sarraf Mamoory R, Svend Le DQ, et al. Fabrication of gelatin/hydroxyapatite/3D-graphene scaffolds by a hydrogel 3D-printing method. Materials Chemistry and Physics, 2020, 239(1): 122305. doi: 10.1016/j.matchemphys.2019.122305.
59.	Jiao D, Zheng A, Liu Y, et al. Bidirectional differentiation of BMSCs induced by a biomimetic procallus based on a gelatin-reduced graphene oxide reinforced hydrogel for rapid bone regeneration. Bioact Mater, 2020, 6(7): 2011-2028.
60.	Li X, Chen J, Xu Z, et al. Osteoblastic differentiation of stem cells induced by graphene oxide-hydroxyapatite-alginate hydrogel composites and construction of tissue-engineered bone. J Mater Sci Mater Med, 2020, 31(12): 125. doi: 10.1007/s10856-020-06467-6.
61.	Cui H, Yu Y, Li X, et al. Direct 3D printing of a tough hydrogel incorporated with carbon nanotubes for bone regeneration. J Mater Chem B, 2019, 7(45): 7207-7217.
62.	Pelto J, Björninen M, Pälli A, et al. Novel polypyrrole-coated polylactide scaffolds enhance adipose stem cell proliferation and early osteogenic differentiation. Tissue Eng Part A, 2013, 19(7-8): 882-892.
63.	Chen J, Yu M, Guo B, et al. Conductive nanofibrous composite scaffolds based on in-situ formed polyaniline nanoparticle and polylactide for bone regeneration. J Colloid Interface Sci, 2018, 514: 517-527.
64.	Yang J, Choe G, Yang S, et al. Polypyrrole-incorporated conductive hyaluronic acid hydrogels. Biomater Res, 2016, 20: 31. doi: 10.1186/s40824-016-0078-y.
65.	Sawyer SW, Dong P, Venn S, et al. Conductive gelatin methacrylate-poly (aniline) hydrogel for cell encapsulation. Biomedical Physics & Engineering Express, 2017, 4(1): 015005. doi: 10.1088/2057-1976/aa91f9.
66.	Liu X, George MN, Li L, et al. Injectable electrical conductive and phosphate releasing gel with two-dimensional black phosphorus and carbon nanotubes for bone tissue engineering. ACS Biomater Sci Eng, 2020, 6(8): 4653-4665.
67.	Gao X, Shi Z, Liu C, et al. Inelastic behaviour of bacterial cellulose hydrogel: in aqua cyclic tests. Polymer Testing, 2015, 44: 82-92.
68.	Lin S, Cao C, Wang Q, et al. Design of stiff, tough and stretchy hydrogel composites via nanoscale hybrid crosslinking and macroscale fiber reinforcement. Soft Matter, 2014, 10(38): 7519-7527.
69.	Illeperuma WRK, Sun JY, Suo Z, et al. Fiber-reinforced tough hydrogels. Extreme Mechanics Letters, 2014, 1: 90-96.
70.	Agrawal A, Rahbar N, Calvert PD. Strong fiber-reinforced hydrogel. Acta Biomater, 2013, 9(2): 5313-5318.
71.	Xu W, Ma J, Jabbari E. Material properties and osteogenic differentiation of marrow stromal cells on fiber-reinforced laminated hydrogel nanocomposites. Acta Biomater, 2010, 6(6): 1992-2002.
72.	Dubey N, Ferreira JA, Daghrery A, et al. Highly tunable bioactive fiber-reinforced hydrogel for guided bone regeneration. Acta Biomater, 2020, 113: 164-176.

1. Turnbull G, Clarke J, Picard F, et al. 3D bioactive composite scaffolds for bone tissue engineering. Bioact Mater, 2017, 3(3): 278-314.
2. McDermott AM, Herberg S, Mason DE, et al. Recapitulating bone development through engineered mesenchymal condensations and mechanical cues for tissue regeneration. Sci Transl Med, 2019, 11(495): eaav7756. doi: 10.1126/scitranslmed.aav7756.
3. Ashman O, Phillips AM. Treatment of non-unions with bone defects: which option and why? Injury, 2013, 44 Suppl 1: S43-45.
4. Bhumiratana S, Bernhard JC, Alfi DM, et al. Tissue-engineered autologous grafts for facial bone reconstruction. Sci Transl Med, 2016, 8(343): 343ra83. doi: 10.1126/scitranslmed.aad5904.
5. García-Gareta E, Coathup MJ, Blunn GW. Osteoinduction of bone grafting materials for bone repair and regeneration. Bone, 2015, 81: 112-121.
6. Bose S, Sarkar N. Natural medicinal compounds in bone tissue engineering. Trends Biotechnol, 2020, 38(4): 404-417.
7. 吕维加, 李朝阳. 可注射骨修复材料的研发与展望. 骨科临床与研究杂志, 2021, 6(1): 1-6, 19.
8. Askari M, Afzali Naniz M, Kouhi M, et al. Recent progress in extrusion 3D bioprinting of hydrogel biomaterials for tissue regeneration: a comprehensive review with focus on advanced fabrication techniques. Biomater Sci, 2021, 9(3): 535-573.
9. Zhang Y, Li Z, Guan J, et al. Hydrogel: A potential therapeutic material for bone tissue engineering. AIP Advances, 2021, 11(1): 010701. doi: 10.1063/5.0035504.
10. Gong JP, Katsuyama Y, Kurokawa T, et al. Double-network hydrogels with extremely high mechanical strength. Adv Mater, 2003, 15(14): 1155-1158.
11. Haraguchi K, Takehisa T. Nanocomposite hydrogels: A unique organic-inorganic network structure with extraordinary mechanical, optical, and swelling/de‐swelling properties. Advanced materials, 2002, 14(16): 1120-1124.
12. Zhang X, Huang P, Jiang G, et al. A novel magnesium ion-incorporating dual-crosslinked hydrogel to improve bone scaffold-mediated osteogenesis and angiogenesis. Mater Sci Eng C Mater Biol Appl, 2021, 121: 111868. doi: 10.1016/j.msec.2021.111868.
13. Li A, Xu H, Yu P, et al. Injectable hydrogels based on gellan gum promotes in situ mineralization and potential osteogenesis. European Polymer Journal, 2020, 141: 110091. doi: 10.1016/j.eurpolymj.2020.110091.
14. Xu M, Qin M, Zhang X, et al. Porous PVA/SA/HA hydrogels fabricated by dual-crosslinking method for bone tissue engineering. J Biomater Sci Polym Ed, 2020, 31(6): 816-831.
15. Bi S, Wang P, Hu S, et al. Construction of physical-crosslink chitosan/PVA double-network hydrogel with surface mineralization for bone repair. Carbohydr Polym, 2019, 224: 115176. doi: 10.1016/j.carbpol.2019.115176.
16. Dorozhkin SV. A detailed history of calcium orthophosphates from 1770s till 1950. Mater Sci Eng C Mater Biol Appl, 2013, 33(6): 3085-3110.
17. Wang Y, Cao X, Ma M, et al. A gelMA-PEGDA-nHA composite hydrogel for bone tissue engineering. Materials (Basel), 2020, 13(17): 3735. doi: 10.3390/ma13173735.
18. Liu C, Wu J, Gan D, et al. The characteristics of mussel-inspired nHA/OSA injectable hydrogel and repaired bone defect in rabbit. J Biomed Mater Res B Appl Biomater, 2020, 108(5): 1814-1825.
19. Nie L, Wu Q, Long H, et al. Development of chitosan/gelatin hydrogels incorporation of biphasic calcium phosphate nanoparticles for bone tissue engineering. J Biomater Sci Polym Ed, 2019, 30(17): 1636-1657.
20. Sen KS, Duarte Campos DF, Köpf M, et al. The effect of addition of calcium phosphate particles to hydrogel-based composite materials on stiffness and differentiation of mesenchymal stromal cells toward osteogenesis. Adv Healthc Mater, 2018, 7(18): e1800343. doi: 10.1002/adhm.201800343.
21. Ye Q, Zhang Y, Dai K, et al. Three dimensional printed bioglass/gelatin/alginate composite scaffolds with promoted mechanical strength, biomineralization, cell responses and osteogenesis. J Mater Sci Mater Med, 2020, 31(9): 77. doi: 10.1007/s10856-020-06413-6.
22. Killion JA, Kehoe S, Geever LM, et al. Hydrogel/bioactive glass composites for bone regeneration applications: synthesis and characterisation. Mater Sci Eng C Mater Biol Appl, 2013, 33(7): 4203-4212.
23. Wu J, Zheng K, Huang X, et al. Thermally triggered injectable chitosan/silk fibroin/bioactive glass nanoparticle hydrogels for in-situ bone formation in rat calvarial bone defects. Acta Biomater, 2019, 91: 60-71.
24. Dawson JI, Oreffo RO. Clay: new opportunities for tissue regeneration and biomaterial design. Adv Mater, 2013, 25(30): 4069-4086.
25. Mihaila SM, Gaharwar AK, Reis RL, et al. The osteogenic differentiation of SSEA-4 sub-population of human adipose derived stem cells using silicate nanoplatelets. Biomaterials, 2014, 35(33): 9087-9099.
26. Xavier JR, Thakur T, Desai P, et al. Bioactive nanoengineered hydrogels for bone tissue engineering: a growth-factor-free approach. ACS Nano, 2015, 9(3): 3109-3118.
27. Guggenheim S, Martin R. Definition of clay and clay mineral: joint report of the AIPEA nomenclature and CMS nomenclature committees. Clays and clay minerals, 1995, 43(2): 255-256.
28. Han X, Xu H, Che L, et al. Application of inorganic nanocomposite hydrogels in bone tissue engineering. iScience, 2020, 23(12): 101845. doi: 10.1016/j.isci.2020.101845.
29. Jin Y, Liu C, Chai W, et al. Self-supporting nanoclay as internal scaffold material for direct printing of soft hydrogel composite structures in air. ACS Appl Mater Interfaces, 2017, 9(20): 17456-17465.
30. Gaharwar AK, Schexnailder PJ, Kline BP, et al. Assessment of using laponite cross-linked poly(ethylene oxide) for controlled cell adhesion and mineralization. Acta Biomater, 2011, 7(2): 568-577.
31. Liu B, Li J, Lei X, et al. Cell-loaded injectable gelatin/alginate/LAPONITE^® nanocomposite hydrogel promotes bone healing in a critical-size rat calvarial defect model. RSC Advances, 2020, 10(43): 25652-25661.
32. Ou Q, Huang K, Fu C, et al. Nanosilver-incorporated halloysite nanotubes/gelatin methacrylate hybrid hydrogel with osteoimmunomodulatory and antibacterial activity for bone regeneration. Chemical Engineering Journal, 2020, 382: 123019. doi: 10.1016/j.cej.2019.123019.
33. Pietraszek A, Ledwójcik G, Lewandowska-Łańcucka J, et al. Bioactive hydrogel scaffolds reinforced with alkaline-phosphatase containing halloysite nanotubes for bone repair applications. Int J Biol Macromol, 2020, 163: 1187-1195.
34. Cui ZK, Kim S, Baljon JJ, et al. Microporous methacrylated glycol chitosan-montmorillonite nanocomposite hydrogel for bone tissue engineering. Nat Commun, 2019, 10(1): 3523. doi: 10.1038/s41467-019-11511-3.
35. Lim K, Hexiu J, Kim J, et al. Effects of electromagnetic fields on osteogenesis of human alveolar bone-derived mesenchymal stem cells. Biomed Res Int, 2013, 2013: 296019. doi: 10.1155/2013/296019.
36. McCullen SD, McQuilling JP, Grossfeld RM, et al. Application of low-frequency alternating current electric fields via interdigitated electrodes: effects on cellular viability, cytoplasmic calcium, and osteogenic differentiation of human adipose-derived stem cells. Tissue Eng Part C Methods, 2010, 16(6): 1377-1386.
37. Min JH, Patel M, Koh WG. Incorporation of conductive materials into hydrogels for tissue engineering applications. Polymers (Basel), 2018, 10(10): 1078. doi: 10.3390/polym10101078.
38. Guo B, Ma PX. Conducting polymers for tissue engineering. Biomacromolecules, 2018, 19(6): 1764-1782.
39. Zare M, Ramezani Z, Rahbar N. Development of zirconia nanoparticles-decorated calcium alginate hydrogel fibers for extraction of organophosphorous pesticides from water and juice samples: Facile synthesis and application with elimination of matrix effects. J Chromatogr A, 2016, 1473: 28-37.
40. Paquet C, de Haan HW, Leek DM, et al. Clusters of superparamagnetic iron oxide nanoparticles encapsulated in a hydrogel: a particle architecture generating a synergistic enhancement of the T2 relaxation. ACS Nano, 2011, 5(4): 3104-3112.
41. Xu L, Li X, Takemura T, et al. Genotoxicity and molecular response of silver nanoparticle (NP)-based hydrogel. J Nanobiotechnology, 2012, 10: 16. doi: 10.1186/1477-3155-10-16.
42. Xing R, Liu K, Jiao T, et al. An injectable self-assembling collagen-gold hybrid hydrogel for combinatorial antitumor photothermal/photodynamic therapy. Adv Mater, 2016, 28(19): 3669-3676.
43. Ribeiro M, Ferraz MP, Monteiro FJ, et al. Antibacterial silk fibroin/nanohydroxyapatite hydrogels with silver and gold nanoparticles for bone regeneration. Nanomedicine, 2017, 13(1): 231-239.
44. Heo DN, Ko WK, Bae MS, et al. Enhanced bone regeneration with a gold nanoparticle-hydrogel complex. J Mater Chem B, 2014, 2(11): 1584-1593.
45. Celikkin N, Mastrogiacomo S, Walboomers XF, et al. Enhancing X-ray attenuation of 3D printed gelatin methacrylate (GelMA) hydrogels utilizing gold nanoparticles for bone tissue engineering applications. Polymers (Basel), 2019, 11(2): 367. doi: 10.3390/polym11020367.
46. Arvizo RR, Bhattacharyya S, Kudgus RA, et al. Intrinsic therapeutic applications of noble metal nanoparticles: past, present and future. Chem Soc Rev, 2012, 41(7): 2943-2970.
47. Paun IA, Popescu RC, Calin BS, et al. 3D biomimetic magnetic structures for static magnetic field stimulation of osteogenesis. Int J Mol Sci, 2018, 19(2): 495. doi: 10.3390/ijms19020495.
48. Uskoković V, Graziani V, Wu VM, et al. Gold is for the mistress, silver for the maid: Enhanced mechanical properties, osteoinduction and antibacterial activity due to iron doping of tricalcium phosphate bone cements. Mater Sci Eng C Mater Biol Appl, 2019, 94: 798-810.
49. Lin HY, Huang HY, Shiue SJ, et al. Osteogenic effects of inductive coupling magnetism from magnetic 3D printed hydrogel scaffold. Journal of Magnetism and Magnetic Materials, 2020, 504: 166680. doi: 10.1016/j.jmmm.2020.166680.
50. Farzaneh S, Hosseinzadeh S, Samanipour R, et al. Fabrication and characterization of cobalt ferrite magnetic hydrogel combined with static magnetic field as a potential bio-composite for bone tissue engineering. Journal of Drug Delivery Science and Technology, 2021, 64: 102525. doi: 10.1016/j.jddst.2021.102525.
51. Lee JH, Shin YC, Lee SM, et al. Enhanced osteogenesis by reduced graphene oxide/hydroxyapatite nanocomposites. Sci Rep, 2015, 5: 18833. doi: 10.1038/srep18833.
52. Xue D, Chen E, Zhong H, et al. Immunomodulatory properties of graphene oxide for osteogenesis and angiogenesis. Int J Nanomedicine, 2018, 13: 5799-5810.
53. Mohammadrezaei D, Golzar H, Rezai Rad M, et al. In vitro effect of graphene structures as an osteoinductive factor in bone tissue engineering: A systematic review. J Biomed Mater Res A, 2018, 106(8): 2284-2343.
54. Kang ES, Kim DS, Suhito IR, et al. Guiding osteogenesis of mesenchymal stem cells using carbon-based nanomaterials. Nano convergence, 2017, 4(1): 1-14.
55. Pei B, Wang W, Dunne N, et al. Applications of carbon nanotubes in bone tissue regeneration and engineering: superiority, concerns, current advancements, and prospects. Nanomaterials, 2019, 9(10): 1501. doi: 10.3390/nano9101501.
56. Cha C, Shin SR, Gao X, et al. Controlling mechanical properties of cell-laden hydrogels by covalent incorporation of graphene oxide. Small, 2014, 10(3): 514-523.
57. Zhou M, Lozano N, Wychowaniec JK, et al. Graphene oxide: A growth factor delivery carrier to enhance chondrogenic differentiation of human mesenchymal stem cells in 3D hydrogels. Acta biomaterialia, 2019, 96: 271-280.
58. Nosrati H, Sarraf Mamoory R, Svend Le DQ, et al. Fabrication of gelatin/hydroxyapatite/3D-graphene scaffolds by a hydrogel 3D-printing method. Materials Chemistry and Physics, 2020, 239(1): 122305. doi: 10.1016/j.matchemphys.2019.122305.
59. Jiao D, Zheng A, Liu Y, et al. Bidirectional differentiation of BMSCs induced by a biomimetic procallus based on a gelatin-reduced graphene oxide reinforced hydrogel for rapid bone regeneration. Bioact Mater, 2020, 6(7): 2011-2028.
60. Li X, Chen J, Xu Z, et al. Osteoblastic differentiation of stem cells induced by graphene oxide-hydroxyapatite-alginate hydrogel composites and construction of tissue-engineered bone. J Mater Sci Mater Med, 2020, 31(12): 125. doi: 10.1007/s10856-020-06467-6.
61. Cui H, Yu Y, Li X, et al. Direct 3D printing of a tough hydrogel incorporated with carbon nanotubes for bone regeneration. J Mater Chem B, 2019, 7(45): 7207-7217.
62. Pelto J, Björninen M, Pälli A, et al. Novel polypyrrole-coated polylactide scaffolds enhance adipose stem cell proliferation and early osteogenic differentiation. Tissue Eng Part A, 2013, 19(7-8): 882-892.
63. Chen J, Yu M, Guo B, et al. Conductive nanofibrous composite scaffolds based on in-situ formed polyaniline nanoparticle and polylactide for bone regeneration. J Colloid Interface Sci, 2018, 514: 517-527.
64. Yang J, Choe G, Yang S, et al. Polypyrrole-incorporated conductive hyaluronic acid hydrogels. Biomater Res, 2016, 20: 31. doi: 10.1186/s40824-016-0078-y.
65. Sawyer SW, Dong P, Venn S, et al. Conductive gelatin methacrylate-poly (aniline) hydrogel for cell encapsulation. Biomedical Physics & Engineering Express, 2017, 4(1): 015005. doi: 10.1088/2057-1976/aa91f9.
66. Liu X, George MN, Li L, et al. Injectable electrical conductive and phosphate releasing gel with two-dimensional black phosphorus and carbon nanotubes for bone tissue engineering. ACS Biomater Sci Eng, 2020, 6(8): 4653-4665.
67. Gao X, Shi Z, Liu C, et al. Inelastic behaviour of bacterial cellulose hydrogel: in aqua cyclic tests. Polymer Testing, 2015, 44: 82-92.
68. Lin S, Cao C, Wang Q, et al. Design of stiff, tough and stretchy hydrogel composites via nanoscale hybrid crosslinking and macroscale fiber reinforcement. Soft Matter, 2014, 10(38): 7519-7527.
69. Illeperuma WRK, Sun JY, Suo Z, et al. Fiber-reinforced tough hydrogels. Extreme Mechanics Letters, 2014, 1: 90-96.
70. Agrawal A, Rahbar N, Calvert PD. Strong fiber-reinforced hydrogel. Acta Biomater, 2013, 9(2): 5313-5318.
71. Xu W, Ma J, Jabbari E. Material properties and osteogenic differentiation of marrow stromal cells on fiber-reinforced laminated hydrogel nanocomposites. Acta Biomater, 2010, 6(6): 1992-2002.
72. Dubey N, Ferreira JA, Daghrery A, et al. Highly tunable bioactive fiber-reinforced hydrogel for guided bone regeneration. Acta Biomater, 2020, 113: 164-176.

Chinese Journal of Reparative and Reconstructive Surgery

Methods of improving the mechanical properties of hydrogels and their research progress in bone tissue engineering

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content