AccScience Publishing / IJB / Volume 7 / Issue 3 / DOI: 10.18063/ijb.v7i3.367
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REVIEW

3D Bioprinting Photo-Crosslinkable Hydrogels for Bone and Cartilage Repair

Quanjing Mei1† Jingdong Rao1† Ho Pan Bei1 Yaxiong Liu2 Xin Zhao1*
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1 Department of Biomedical Engineering, The Hong Kong Polytechnic University, Hung Hom, Hong Kong, China
2 Jihua Laboratory, Foshan, Guangdong, China
© Invalid date by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

Three-dimensional (3D) bioprinting has become a promising strategy for bone manufacturing, with excellent control over geometry and microarchitectures of the scaffolds. The bioprinting ink for bone and cartilage engineering has thus become the key to developing 3D constructs for bone and cartilage defect repair. Maintaining the balance of cellular viability, drugs or cytokines’ function, and mechanical integrity is critical for constructing 3D bone and/or cartilage scaffolds. Photo-crosslinkable hydrogel is one of the most promising materials in tissue engineering; it can respond to light and induce structural or morphological transition. The biocompatibility, easy fabrication, as well as controllable mechanical and degradation properties of photo-crosslinkable hydrogel can meet various requirements of the bone and cartilage scaffolds, which enable it to serve as an effective bio-ink for 3D bioprinting. Here, in this review, we first introduce commonly used photo-crosslinkable hydrogel materials and additives (such as nanomaterials, functional cells, and drugs/cytokine), and then discuss the applications of the 3D bioprinted photo-crosslinkable hydrogel scaffolds for bone and cartilage engineering. Finally, we conclude the review with future perspectives about the development of 3D bioprinting photo-crosslinkable hydrogels in bone and cartilage engineering.

Keywords
Bone and cartilage engineering
Hydrogel
Photo-crosslinking
Three-dimensional printing
References

1. Midha S, Dalela M, Sybil D, et al., 2019, Advances in Three dimensional Bioprinting of Bone: Progress and Challenges. J Tissue Eng Regen Med, 13:925–45. https://doi.org/10.1002/term.2847

2. Liu Y, Luo D, Wang T, 2016, Hierarchical Structures of Bone and Bioinspired Bone Tissue Engineering. Small, 12:4611–32. https://doi.org/10.1002/smll.201600626

3. Bai X, Gao M, Syed S, et al., 2018, Bioactive Hydrogels For Bone Regeneration. Bioact Mater, 3:401–17.

4. Mandrycky C, Wang Z, Kim K, et al., 2016, 3D Bioprinting for Engineering Complex Tissues. Biotechnol Adv, 34:422–34. https://doi.org/10.1016/j.biotechadv.2015.12.011

5. Allen MR, Burr DB, 2014, Bone Modeling and Remodeling. In: Basic and Applied Bone Biology. Amsterdam, Netherlands: Elsevier. p75-90. https://doi.org/10.1016/b978-0-12-416015-6.00004-6

6. Byambaa B, Annabi N, Yue K, et al., 2017, Bioprinted Osteogenic and Vasculogenic Patterns for Engineering 3D Bone Tissue. Adv Healthc Mater, 6:1700015. https://doi.org/10.1002/adhm.201700015

7. Groll J, Boland T, Blunk T, et al., 2016, Biofabrication: Reappraising the Definition of an Evolving Field. Biofabrication, 8:013001. https://doi.org/10.1088/1758-5090/8/1/013001

8. Ashammakhi N, Hasan A, Kaarela O, et al., 2019, Advancing Frontiers in Bone Bioprinting. Adv Healthc Mater, 8:1801048. https://doi.org/10.1002/adhm.201801048

9. Keriquel V, Oliveira H, Rémy M, et al., 2017, In Situ Printing of Mesenchymal Stromal Cells, by Laser-assisted Bioprinting, for In Vivo Bone Regeneration Applications. Sci Rep, 7:1–10. https://doi.org/10.1038/s41598-017-01914-x

10. Yang Y, Zhang Q, Xu T, et al., 2020, Photo crosslinkable Nanocomposite Ink for Printing Strong, Biodegradable and Bioactive Bone Graft. Biomaterials, 263:120378. https://doi.org/10.1016/j.biomaterials.2020.120378

11. Nguyen QV, Park JH, Lee DS, 2015, Injectable Polymeric Hydrogels for the Delivery of Therapeutic Agents: A Review. Eur Polym J, 72:602–619. https://doi.org/10.1016/j.eurpolymj.2015.03.016

12. Yue K, Trujillo-de Santiago G, Alvarez MM, et al., 2015, Synthesis, Properties, and Biomedical Applications of Gelatin Methacryloyl (GelMA) Hydrogels. Biomaterials, 73:254–271. https://doi.org/10.1016/j.biomaterials.2015.08.045

13. Vijayavenkataraman S, Yan WC, Lu WF, et al., 2018, 3D Bioprinting of Tissues and Organs for Regenerative Medicine. Adv Drug Deliv Rev, 132:296–332. https://doi.org/10.1016/j.addr.2018.07.004

14. Li X, Chen S, Li J, et al., 2016, 3D Culture of Chondrocytes in Gelatin Hydrogels with Different Stiffness. Polymers (Basel), 8:269. https://doi.org/10.3390/polym8080269

15. Bryant SJ, Chowdhury TT, Lee DA, et al., 2004, Crosslinking Density Influences Chondrocyte Metabolism in Dynamically Loaded Photocrosslinked Poly (Ethylene Glycol) Hydrogels. Ann Biomed Eng, 32:407–17. https://doi.org/10.1023/b: abme.0000017535.00602.ca

16. Marklein RA, Burdick JA, 2010, Spatially Controlled Hydrogel Mechanics to Modulate Stem Cell Interactions. Soft Matter, 6:136–43. https://doi.org/10.1039/b916933d

17. Bian L, Hou C, Tous E, et al., 2013, The Influence of Hyaluronic Acid Hydrogel Crosslinking Density and Macromolecular Diffusivity on Human MSC Chondrogenesis and Hypertrophy. Biomaterials, 34:413–21. https://doi.org/10.1016/j.biomaterials.2012.09.052

18. Nguyen KT, West JL, 2002, Photopolymerizable Hydrogels for Tissue Engineering Applications. Biomaterials, 23: 4307–14. https://doi.org/10.1016/s0142-9612(02)00175-8

19. Annabi N, Tamayol A, Uquillas JA, et al., 2014, 25th Anniversary Article: Rational Design and Applications of Hydrogels in Regenerative Medicine. Adv Mater, 26:85–124. https://doi.org/10.1002/adma.201303233

20. Jiang Y, Chen J, Deng C, et al., 2014, Click Hydrogels, Microgels and Nanogels: Emerging Platforms for Drug Delivery and Tissue Engineering. Biomaterials, 35:4969–85. https://doi.org/10.1016/j.biomaterials.2014.03.001

21. Van Vlierberghe S, Dubruel P, Schacht EJ, 2011, Biopolymer based Hydrogels as Scaffolds for Tissue Engineering Applications: A Review. Biomacromolecules, 12:1387–408. https://doi.org/10.1021/bm200083n

22. Collins MN, Birkinshaw CJ, 2013, Hyaluronic Acid Based Scaffolds for Tissue Engineering a review. Rom J Morphol Embryol, 92:1262–79. https://doi.org/10.1016/j.carbpol.2012.10.028

23. Sherman L, Sleeman J, Herrlich P, et al., 1994, Hyaluronate Receptors: Key Players in Growth, Differentiation, Migration and Tumor Progression. Curr Opin Cell Biol, 6:726–33. https://doi.org/10.1016/0955-0674(94)90100-7

24. Prestwich GD, 2011, Hyaluronic Acid-based Clinical Biomaterials Derived for Cell and Molecule Delivery in Regenerative Medicine. J Control Release, 155:193–9. https://doi.org/10.1016/j.jconrel.2011.04.007

25. Gramlich WM, Kim IL, Burdick JA, 2013, Synthesis and Orthogonal Photopatterning of Hyaluronic Acid Hydrogels with Thiol-Norbornene Chemistry. Biomaterials, 34:9803–11. https://doi.org/10.1016/j.biomaterials.2013.08.089

26. Oudshoorn MH, Rissmann R, Bouwstra JA, et al., 2007, Synthesis of Methacrylated Hyaluronic Acid with Tailored Degree of Substitution. Polymer, 48:1915–20. https://doi.org/10.1016/j.polymer.2007.01.068

27. Poldervaart MT, Goversen B, De Ruijter M, et al., 2017, 3D Bioprinting of Methacrylated Hyaluronic Acid (MeHA) Hydrogel with Intrinsic Osteogenicity. PLoS One, 12:e0177628. https://doi.org/10.1371/journal.pone.0177628

28. Liu Y, Chan-Park MB, 2010, A Biomimetic Hydrogel Based on Methacrylated Dextran-graft-lysine and Gelatin for 3D Smooth Muscle Cell Culture. Biomaterials, 31:1158–70. https://doi.org/10.1016/j.biomaterials.2009.10.040

29. Lai JY, Li YT, 2010, Functional Assessment of Cross-linked Porous Gelatin Hydrogels for Bioengineered Cell Sheet Carriers. Biomacromolecules, 11:1387–97. https://doi.org/10.1021/bm100213f

30. Schuurman W, Levett PA, Pot MW, et al., 2013, Gelatin methacrylamide Hydrogels as Potential Biomaterials for Fabrication of Tissue-engineered Cartilage Constructs. Macromol Biosci, 13:551–61. https://doi.org/10.1002/mabi.201200471

31. Mũnoz Z, Shih H, Lin CC, 2014, Gelatin Hydrogels Formed by Orthogonal Thiol-Norbornene Photochemistry for Cell Encapsulation. Biomater Sci, 2:1063–72. https://doi.org/10.1039/c4bm00070f

32. Chen YC, Lin RZ, Qi H, et al., 2012, Functional Human Vascular Network Generated in Photocrosslinkable Gelatin Methacrylate Hydrogels. Adv Funct Mater, 22:2027–39. https://doi.org/10.1002/adfm.201101662

33. Sun X, Lang Q, Zhang H, et al., 2017, Electrospun Photocrosslinkable Hydrogel Fibrous Scaffolds for Rapid In Vivo Vascularized Skin Flap Regeneration. Adv Funct Mater, 27:1604617. https://doi.org/10.1002/adfm.201604617

34. Zhao X, Lang Q, Yildirimer L, et al., 2016, Photocrosslinkable Gelatin Hydrogel for Epidermal Tissue Engineering. PLoS One, 5:108–18.

35. Zhao X, Sun X, Yildirimer L, et al., 2017, Cell Infiltrative Hydrogel Fibrous Scaffolds for Accelerated Wound Healing. Acta Biomater, 49:66–77. https://doi.org/10.1016/j.actbio.2016.11.017

36. Pellá MC, Lima-Tenório MK, Tenório-Neto ET, et al., 2018, Chitosan-based Hydrogels: From Preparation to Biomedical Applications. Carbohydr Polym, 196:233–45. https://doi.org/10.1016/j.carbpol.2018.05.033

37. He M, Han B, Jiang Z, et al., 2017, Synthesis of a Chitosan based Photo-Sensitive Hydrogel and its Biocompatibility and Biodegradability. Carbohydr Polym, 166:228–35. https://doi.org/10.1016/j.carbpol.2017.02.072

38. Pei M, Mao J, Xu W, et al., 2019, Photocrosslinkable Chitosan Hydrogels and their Biomedical Applications. J Polym Sci, 57:1862–71.

39. Elizalde-Peña E, Flores-Ramirez N, Luna-Barcenas G, et al., 2007, Synthesis and Characterization of Chitosan-g-glycidyl Methacrylate with Methyl Methacrylate. Eur Polym J, 43:3963–9. https://doi.org/10.1016/j.eurpolymj.2007.06.004

40. Lin CC, Raza A, Shih HJ, 2011, PEG Hydrogels Formed by Thiol-ene Photo-Click Chemistry and their Effect on the Formation and Recovery of Insulin-Secreting Cell Spheroids. Biomaterials, 32:9685–95. https://doi.org/10.1016/j.biomaterials.2011.08.083

41. Hockaday L, Kang K, Colangelo N, et al., 2012, Rapid 3D Printing of Anatomically Accurate and Mechanically Heterogeneous Aortic Valve Hydrogel Scaffolds. Biofabricatio, 4:035005. https://doi.org/10.1088/1758-5082/4/3/035005

42. Lim WS, Chen K, Chong TW, et al., 2018, A Bilayer Swellable Drug-eluting Ureteric Stent: Localized Drug Delivery to Treat Urothelial Diseases. Biomaterials, 165:25–38. https://doi.org/10.1016/j.biomaterials.2018.02.035

43. Shin H, Olsen BD, Khademhosseini A, 2012, The Mechanical Properties and Cytotoxicity of Cell-laden Double-network Hydrogels Based on Photocrosslinkable Gelatin and Gellan Gum Biomacromolecules. Biomaterials, 33:3143–52. https://doi.org/10.1016/j.biomaterials.2011.12.050

44. Kaur M, Srivastava A, 2002, Photopolymerization: A review. J Macromol Sci Part C Polym Rev, 42:481–512.

45. Yan Q, Dong H, Su J, et al., 2018, A Review of 3D Printing Technology for Medical Applications. Engineering, 4:729–42.

46. Colosi C, Shin SR, Manoharan V, et al., 2016, Microfluidic Bioprinting of Heterogeneous 3D Tissue Constructs Using Low-viscosity Bioink. Adv Mater, 28:677–84. https://doi.org/10.1002/adma.201503310

47. Wadnap S, Krishnamoorthy S, Zhang Z, et al., 2019, Biofabrication of 3D Cell-encapsulated Tubular Constructs Using Dynamic Optical Projection Stereolithography. J Mater Sci Mater Med, 30:1–10. https://doi.org/10.1007/s10856-019-6239-5

48. Xu H, Liu Q, Casillas J, et al., 2020, Prediction of Cell Viability in Dynamic Optical Projection Stereolithography based Bioprinting Using Machine Learning. J Intell Manuf, 2020:1–11. https://doi.org/10.1007/s10845-020-01708-5

49. Zhang K, Feng Q, Xu J, et al., 2017, Self-assembled Injectable Nanocomposite Hydrogels Stabilized by Bisphosphonate-magnesium (Mg2+) Coordination Regulates the Differentiation of Encapsulated Stem Cells Via Dual Crosslinking. Adv Funct Mater, 27:1701642. https://doi.org/10.1002/adfm.201701642

50. Zuo Y, Liu X, Wei D, et al., 2015, Photo-cross-linkable Methacrylated Gelatin and Hydroxyapatite Hybrid Hydrogel for Modularly Engineering Biomimetic Osteon. 7:10386–94. https://doi.org/10.1021/acsami.5b01433

51. Shi D, Xu X, Ye Y, et al., 2016, Photo-cross-linked Scaffold with Kartogenin-encapsulated Nanoparticles for Cartilage Regeneration. ACS Nano, 10:1292–9. https://doi.org/10.1021/acsnano.5b06663.s001

52. de Windt TS, Vonk LA, Slaper-Cortenbach IC, et al., 2017, Allogeneic Mesenchymal Stem Cells Stimulate Cartilage Regeneration and are Safe for Single-stage Cartilage Repair in Humans Upon Mixture with Recycled Autologous Chondrons. Stem Cells, 35:256–64. https://doi.org/10.1002/stem.2475

53. Levato R, Webb WR, Otto IA, et al., 2017, The Bio in the Ink: Cartilage Regeneration with Bioprintable Hydrogels and Articular Cartilage-derived Progenitor Cells. Acta Biomater, 61:41–53. https://doi.org/10.1016/j.actbio.2017.08.005

54. Yan S, Wang T, Feng L, et al., 2014, Injectable In Situ Self-cross-linking Hydrogels Based on Poly (L-glutamic Acid) and Alginate for Cartilage Tissue Engineering. Biomacromolecules, 15:4495–508. https://doi.org/10.1021/bm501313t

55. Gao G, Schilling AF, Hubbell K, et al., 2015, Improved Properties of Bone and Cartilage Tissue from 3D Inkjet bioprinted Human Mesenchymal Stem Cells by Simultaneous Deposition and Photocrosslinking in PEG-GelMA. 37:2349–55. https://doi.org/10.1007/s10529-015-1921-2

56. Rao RR, Stegemann JP, 2013, Cell-based Approaches to the Engineering of Vascularized Bone Tissue. Cytotherapy, 15:1309–22. https://doi.org/10.1016/j.jcyt.2013.06.005

57. Peters EB, 2018, Endothelial Progenitor Cells for the Vascularization of Engineered Tissues. Tissue Eng Part B Rev, 24:1–24.

58. Zhai X, Ruan C, Ma Y, et al., 2018, 3D-bioprinted Osteoblast laden Nanocomposite Hydrogel Constructs with Induced Microenvironments Promote Cell Viability, Differentiation, and Osteogenesis Both In Vitro and In Vivo. Adv Sci (Weinh), 5:1700550. https://doi.org/10.1002/advs.201700550

59. Wenz A, Tjoeng I, Schneider I, et al., 2018, Improved Vasculogenesis and Bone Matrix Formation through Coculture of Endothelial Cells and Stem Cells in Tissue specific Methacryloyl Gelatin-Based Hydrogels. Biotechnol Bioeng, 115:2643–53. https://doi.org/10.1002/bit.26792

60. Doschak MR, Kucharski CM, Wright JE, et al., 2009, Improved Bone Delivery of Osteoprotegerin by Bisphosphonate Conjugation in a Rat Model of Osteoarthritis. Mol Pharm, 6:634–40. https://doi.org/10.1021/mp8002368

61. Park D, Park CW, Choi Y, et al., 2016, A Novel Small molecule PPI Inhibitor Targeting Integrin αvβ3-osteopontin Interface Blocks Bone Resorption In Vitro and Prevents Bone Loss in Mice. Biomaterials, 98:131–42. https://doi.org/10.1016/j.biomaterials.2016.05.007

62. Teno N, Masuya K, Ehara T, et al., 2008, Effect of Cathepsin K Inhibitors on Bone Resorption. J Med Chem, 51:5459–62.

63. Arrighi I, Mark S, Alvisi M, et al., 2009, Bone Healing Induced by Local Delivery of an Engineered Parathyroid Hormone Prodrug. Biomaterials, 30:1763–71. https://doi.org/10.1016/j.biomaterials.2008.12.023

64. Rodan GA, Martin TJ, 2000, Therapeutic Approaches to Bone Diseases. Science, 289:1508–14.

65. Zhang Gand Suggs L J J A d d r, 2007, Matrices and scaffolds for drug delivery in vascular tissue engineering. Adv Drug Deliv Rev, 59:360–73. https://doi.org/10.1016/j.addr.2009.08.002

66. Nomi M, Atala A, De Coppi P, et al., 2002, Principals of Neovascularization for Tissue Engineering. Mol Aspects Med, 23:463–83. https://doi.org/10.1016/s0098-2997(02)00008-0

67. An Y, Hubbell JA, 2000, Intraarterial Protein Delivery Via Intimally-adherent Bilayer Hydrogels. J Control Release, 64:205–15. https://doi.org/10.1016/s0168-3659(99)00143-1

68. Kim HD, Lee EA, An YH, et al., 2017, Chondroitin Sulfate based Biomineralizing Surface Hydrogels for Bone Tissue Engineering. ACS Appl Mater Interfaces, 9:21639–50. https://doi.org/10.1021/acsami.7b04114

69. Xin T, Mao J, Liu L, et al., 2020, Programmed Sustained Release of Recombinant Human Bone Morphogenetic Protein-2 and Inorganic ion Composite Hydrogel as Artificial Periosteum. ACS Appl Mater Interfaces, 12:6840–51. https://doi.org/10.1021/acsami.9b18496

70. Cui H, Zhu W, Nowicki M, et al., 2016, Hierarchical Fabrication of Engineered Vascularized Bone Biphasic Constructs Via Dual 3D Bioprinting: Integrating Regional Bioactive Factors into Architectural Design. Adv Healthc Mater, 5:2174–81. https://doi.org/10.1002/adhm.201600505

71. Boere KW, Visser J, Seyednejad H, et al., 2014, Covalent Attachment of a Three-dimensionally Printed Thermoplast to a Gelatin Hydrogel for Mechanically Enhanced Cartilage Constructs. Acta Biomater, 10:2602–11. https://doi.org/10.1016/j.actbio.2014.02.041

72. Dhawan A, Kennedy PM, Rizk EB, et al., 2019, Three dimensional Bioprinting for Bone and Cartilage Restoration in Orthopaedic Surgery. J Am Acad Orthop Surg, 27:e215–26. https://doi.org/10.5435/jaaos-d-17-00632

73. Duchi S, Onofrillo C, O’Connell CD, et al., 2017, Handheld Co-axial Bioprinting: Application to In Situ Surgical Cartilage Repair. Scientific Reports, 7:1–12. https://doi.org/10.1038/s41598-017-05699-x

74. Galarraga JH, Kwon MY, Burdick JA, 2019, 3D Bioprinting Via an In Situ Crosslinking Technique towards Engineering Cartilage Tissue. Sci Rep, 9:1–12. https://doi.org/10.1038/s41598-019-56117-3

75. Lam T, Dehne T, Krüger JP, et al., 2019, Photopolymerizable Gelatin and Hyaluronic Acid for Stereolithographic 3D Bioprinting of Tissue-engineered Cartilage. J Biomed Mater Res, 107:2649–57. https://doi.org/10.1002/jbm.b.34354

76. Abdollahiyan P, Oroojalian F, Mokhtarzadeh A, et al., 2020, Hydrogel-Based 3D Bioprinting for Bone and Cartilage Tissue Engineering. 15:2000095. https://doi.org/10.1002/biot.202000095

77. Askari M, Naniz MA, Kouhi M, et al., 2021, Recent Progress in Extrusion 3D Bioprinting of Hydrogel Biomaterials for Tissue Regeneration: A Comprehensive Review with Focus on Advanced Fabrication Techniques. Biomater Sci, 9:535–73. https://doi.org/10.1039/d0bm00973c

78. Cui X, Breitenkamp K, Finn M, et al., 2012, Direct Human Cartilage Repair Using Three-dimensional Bioprinting Technology. Tissue Eng Part A, 18:1304–12. https://doi.org/10.1089/ten.tea.2011.0543

79. Gao F, Xu Z, Liang Q, et al., 2019, Osteochondral Regeneration with 3D-Printed Biodegradable High-strength Supramolecular Polymer Reinforced-gelatin Hydrogel Scaffolds. Adv Sci., 6:1900867. https://doi.org/10.1002/advs.201900867

80. Genova T, Roato I, Carossa M, et al., 2020, Advances on Bone Substitutes Through 3D Bioprinting. Int J Mol Sci, 21:7012. https://doi.org/10.3390/ijms21197012

81. Qiao H., Tang TJ, 2018, Engineering 3D Approaches to Model the Dynamic Microenvironments of Cancer Bone Metastasis. Bone Res, 6:1–12. https://doi.org/10.1038/s41413-018-0008-9

82. Ozbolat IT, Peng W, Ozbolat VJ, 2016, Application Areas of 3D Bioprinting. Drug Discov Today, 21:1257–71. https://doi.org/10.1016/j.drudis.2016.04.006

83. Ozbolat IT, Hospodiuk MJ, 2016, Current Advances and Future Perspectives in Extrusion-based Bioprinting. Biomaterials, 76:321–43. https://doi.org/10.1016/j.biomaterials.2015.10.076

84. Miri AK, Nieto D, Iglesias L, et al., 2018, Microfluidics-Enabled Multimaterial Maskless Stereolithographic Bioprinting. Adv Mater, 30:e1800242. https://doi.org/10.1002/adma.201870201

85. Zhu W, Holmes B, Glazer RI, et al., 2016, 3D Printed Nanocomposite Matrix for the Study of Breast Cancer Bone Metastasis. Nanomedicine, 12:69–79. https://doi.org/10.1016/j.nano.2015.09.010

86. Zhou X, Zhu W, Nowicki M, et al., 2016, 3D Bioprinting a Cell-laden Bone Matrix for Breast Cancer Metastasis Study. ACS Appl Mater Interfaces, 8:30017–26. https://doi.org/10.1021/acsami.6b10673

87. Stichler S, Jungst T, Schamel M, et al., 2017, Thiol-ene Clickable Poly(glycidol) Hydrogels for Biofabrication. Ann Biomed Eng, 45:273–85. https://doi.org/10.1007/s10439-016-1633-3

88. Murphy SV, Atala A, 2014, 3D Bioprinting of Tissues and Organs. Nat Biotechnol, 32:773–85. https://doi.org/10.1038/nbt.2958

89. Baxter FR, Bowen CR, Turner IG, et al., 2010, Electrically Active Bioceramics: A Review of Interfacial Responses. Ann Biomed Eng, 38:2079–92. https://doi.org/10.1007/s10439-010-9977-6

90. Jiang L, Wang Y, Liu Z, et al., 2019, Three-dimensional Printing and Injectable Conductive Hydrogels for Tissue Engineering Application. Tissue Eng Part B Rev, 25:398–411. https://doi.org/10.1089/ten.teb.2019.0100

91. Wei K, Zhu M, Sun Y, et al., 2016, Robust Biopolymeric Supramolecular “Host Guest Macromer” Hydrogels Reinforced by In Situ Formed Multivalent Nanoclusters for Cartilage Regeneration. Macromolecules, 49:866–75. https://doi.org/10.1021/acs.macromol.5b02527.s001

92. Salzlechner C, Haghighi T, Huebscher I, et al., 2020, Adhesive Hydrogels for Maxillofacial Tissue Regeneration Using Minimally Invasive Procedures. Adv Healthc Mater, 9:1901134. https://doi.org/10.1002/adhm.201901134

93. Khare D, Basu B, Dubey AK, 2002, Electrical Stimulation and Piezoelectric Biomaterials for Bone Tissue Engineering Applications. Biomaterials, 258:120280.

94. Wang Q, Chen X, Zhu J, et al., 2008, Porous Li-Na-K Niobate Bone-substitute Ceramics: Microstructure and Piezoelectric Properties. Mater Lettt, 62:3506–8. https://doi.org/10.1016/j.matlet.2008.03.024

95. Zhang X, Zhang C, Lin Y, et al., 2016, Nanocomposite Membranes Enhance Bone Regeneration Through Restoring Physiological Electric Microenvironment. ACS Nano, 10:7279–86. https://doi.org/10.1021/acsnano.6b02247.s001

96. Mestres G, Perez RA, D’Elía NL, et al., 2019, Advantages of Microfluidic Systems for Studying Cell-biomaterial Interactions Focus on Bone Regeneration Applications. Biomed Phys Eng Express, 5:032001. https://doi.org/10.1088/2057-1976/ab1033

97. Kirillova A, Maxson R, Stoychev G, et al., 2017, 4D Biofabrication Using Shape-morphing Hydrogels. Adv Mater, 29:1703443. https://doi.org/10.1002/adma.201703443

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