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Advances in the Fabrication of Scaffold and 3D Printing of Biomimetic Bone Graft

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Abstract

The need for bone grafts is tremendous, and that leads to the use of autograft, allograft, and bone graft substitutes. The biology of the bone is quite complex regarding cellular composition and architecture, hence developing a mineralized connective tissue graft is challenging. Traditionally used bone graft substitutes including metals, biomaterial coated metals and biodegradable scaffolds, suffer from persistent limitations. With the advent and rise of additive manufacturing technologies, the future of repairing bone trauma and defects seems to be optimistic. 3D printing has significant advantages, the foremost of all being faster manipulation of various biocompatible materials and live cells or tissues into the complex natural geometries necessary to mimic and stimulate cellular bone growth. The advent of new-generation bioprinters working with high-precision, micro-dispensing and direct digital manufacturing is aiding in ground-breaking organ and tissue printing, including the bone. The future bone replacement for patients holds excellent promise as scientists are moving closer to the generation of better 3D printed bio-bone grafts that will be safer and more effective. This review aims to summarize the advances in scaffold fabrication techniques, emphasizing 3D printing of biomimetic bone grafts.

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References

  1. Abbah, S. A., J. Liu, R. W. M. Lam, J. C. H. Goh, and H. K. Wong. In vivo bioactivity of rhBMP-2 delivered with novel polyelectrolyte complexation shells assembled on an alginate microbead core template. J. Control. Release 162:364–372, 2012.

    CAS  PubMed  Google Scholar 

  2. Aboudzadeh, N., M. Imani, M. A. Shokrgozar, A. Khavandi, J. Javadpour, Y. Shafieyan, and M. Farokhi. Fabrication and characterization of poly(d, l-lactide-co-glycolide)/hydroxyapatite nanocomposite scaffolds for bone tissue regeneration. J. Biomed. Mater. Res. Part A 94:137–145, 2010.

    Google Scholar 

  3. Agarwal, R., and A. J. Garcia. Biomaterial strategies for engineering implants for enhanced osseointegration and bone repair. Adv. Drug Deliv. Rev. 94:53–62, 2015.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Alaribe, F. N., S. L. Manoto, and S. C. K. M. Motaung. Scaffolds from biomaterials: Advantages and limitations in bone and tissue engineering. Biologia 71:353–366, 2016.

    Google Scholar 

  5. Alizadeh-Osgouei, M., Y. Li, and C. Wen. A comprehensive review of biodegradable synthetic polymer-ceramic composites and their manufacture for biomedical applications. Bioactive Mater. 4:22–36, 2019.

    Google Scholar 

  6. Alvarez, K., and H. Nakajima. Metallic Scaffolds for bone regeneration. Materials 2:790–832, 2009.

    CAS  PubMed Central  Google Scholar 

  7. Amosi, N., S. Zarzhitsky, E. Gilsohn, O. Salnikov, E. Monsonego-Ornan, R. Shahar, and H. Rapaport. Acidic peptide hydrogel scaffolds enhance calcium phosphate mineral turnover into bone tissue. Acta Biomater. 8:2466–2475, 2012.

    CAS  PubMed  Google Scholar 

  8. Aranaz, I., M. Mengibar, R. Harris, I. Panos, B. Miralles, N. Acosta, G. Galed, and A. Heras. Functional characterization of chitin and chitosan. Curr. Chem. Biol. 3:203–230, 2009.

    CAS  Google Scholar 

  9. Aszodi, A., J. F. Bateman, E. Gustafsson, R. Boot-Handford, and R. Fassler. Mammalian skeletogenesis and extracellular matrix: What can we learn from knockout mice? Cell Struct. Funct. 25:73–84, 2000.

    CAS  PubMed  Google Scholar 

  10. Baldwin, P., D. J. Li, D. A. Auston, H. S. Mir, R. S. Yoon, and K. J. Koval. Autograft, allograft, and bone graft substitutes. J. Orthop. Trauma 33:203–213, 2019.

    PubMed  Google Scholar 

  11. Barron, J. A., P. Wu, H. D. Ladouceur, and B. R. Ringeisen. Biological laser printing: A novel technique for creating heterogeneous 3-dimensional cell patterns. Biomed. Microdev. 6:139–147, 2004.

    CAS  Google Scholar 

  12. Beederman, M., J. D. Lamplot, G. Nan, J. Wang, X. Liu, L. Yin, R. Li, W. Shui, H. Zhang, S. H. Kim, W. Zhang, J. Zhang, Y. Kong, S. Denduluri, M. R. Rogers, A. Pratt, R. C. Haydon, H. H. Luu, J. Angeles, L. L. Shi, and T. C. He. BMP signaling in mesenchymal stem cell differentiation and bone formation. J. Biomed. Sci. Eng. 6:32–52, 2013.

    PubMed  PubMed Central  Google Scholar 

  13. Beuttel, E., N. Bormann, A.-M. Pobloth, G. Duda, and B. Wildemann. Impact of gentamicin-loaded bone graft on defect healing in a sheep model. Materials 12:1116, 2019.

    CAS  PubMed Central  Google Scholar 

  14. Bhattacharjee, P., B. Kundu, D. Naskar, H. W. Kim, T. K. Maiti, D. Bhattacharya, and S. C. Kundu. Silk scaffolds in bone tissue engineering: An overview. Acta Biomater. 63:1–17, 2017.

    CAS  PubMed  Google Scholar 

  15. Bigham-Sadegh, A., and A. Oryan. Selection of animal models for pre-clinical strategies in evaluating the fracture healing, bone graft substitutes and bone tissue regeneration and engineering. Connect. Tissue Res. 56:175–194, 2015.

    CAS  PubMed  Google Scholar 

  16. Bishop, E. S., S. Mostafa, M. Pakvasa, H. H. Luu, M. J. Lee, J. M. Wolf, G. A. Ameer, T. C. He, and R. R. Reid. 3-D bioprinting technologies in tissue engineering and regenerative medicine: Current and future trends. Genes Dis. 4:185–195, 2017.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Bose, S., M. Roy, and A. Bandyopadhyay. Recent advances in bone tissue engineering scaffolds. Trends Biotechnol. 30:546–554, 2012.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Bose, S., S. Vahabzadeh, and A. Bandyopadhyay. Bone tissue engineering using 3D printing. Mater. Today 16:496–504, 2013.

    CAS  Google Scholar 

  19. Bouet, G., D. Marchat, M. Cruel, L. Malaval, and L. Vico. In vitro three-dimensional bone tissue models: from cells to controlled and dynamic environment. Tissue Eng. Part B 21:133–156, 2015.

    Google Scholar 

  20. Brunello, G., S. Panda, L. Schiavon, S. Sivolella, L. Biasetto, and M. Del Fabbro. The impact of bioceramic scaffolds on bone regeneration in preclinical in vivo studies: A systematic review. Materials 13:1500, 2020.

    CAS  PubMed Central  Google Scholar 

  21. Campbell, P. G., and L. E. Weiss. Tissue engineering with the aid of inkjet printers. Exp. Opin. Biol. Ther. 7:1123–1127, 2007.

    CAS  Google Scholar 

  22. Capulli, M., R. Paone, and N. Rucci. Osteoblast and osteocyte: Games without frontiers. Arch. Biochem. Biophys. 561:3–12, 2014.

    CAS  PubMed  Google Scholar 

  23. Charles, J. F., and A. O. Aliprantis. Osteoclasts: More than ‘bone eaters’. Trends Mol. Med. 20:449–459, 2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Chen, C. Y., C. J. Ke, K. C. Yen, H. C. Hsieh, J. S. Sun, and F. H. Lin. 3D porous calcium-alginate scaffolds cell culture system improved human osteoblast cell clusters for cell therapy. Theranostics 5:643–655, 2015.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Chen, Q. Z., Y. Li, L. Y. Jin, J. M. Quinn, and P. A. Komesaroff. A new sol-gel process for producing Na(2)O-containing bioactive glass ceramics. Acta Biomater. 6:4143–4153, 2010.

    CAS  PubMed  Google Scholar 

  26. Chen, Q. Z., K. Rezwan, V. Francon, D. Armitage, S. N. Nazhat, F. H. Jones, and A. R. Boccaccini. Surface functionalization of Bioglass-derived porous scaffolds. Acta Biomater. 3:551–562, 2007.

    CAS  PubMed  Google Scholar 

  27. Chen, J., Z.-D. Shi, X. Ji, J. Morales, J. Zhang, N. Kaur, and S. Wang. Enhanced osteogenesis of human mesenchymal stem cells by periodic heat shock in self-assembling peptide hydrogel. Tissue Eng. Part A 19:716–728, 2013.

    CAS  PubMed  Google Scholar 

  28. Chen, Q. Z., I. D. Thompson, and A. R. Boccaccini. 45S5 Bioglass-derived glass-ceramic scaffolds for bone tissue engineering. Biomaterials 27:2414–2425, 2006.

    CAS  PubMed  Google Scholar 

  29. Cheong, V. S., P. Fromme, M. J. Coathup, A. Mumith, and G. W. Blunn. Partial bone formation in additive manufactured porous implants reduces predicted stress and danger of fatigue failure. Ann. Biomed. Eng. 48:502–514, 2020.

    PubMed  Google Scholar 

  30. Chia, H. N., and B. M. Wu. Recent advances in 3D printing of biomaterials. J. Biol. Eng. 9:1–14, 2015.

    CAS  Google Scholar 

  31. Chocholata, P., V. Kulda, and V. Babuska. Fabrication of Scaffolds for bone-tissue regeneration. Materials 12:568, 2019.

    CAS  PubMed Central  Google Scholar 

  32. Chung, C., and J. A. Burdick. Engineering cartilage tissue. Adv. Drug Deliv. Rev. 60:243–262, 2008.

    CAS  PubMed  Google Scholar 

  33. Cipitria, A., J. C. Reichert, D. R. Epari, S. Saifzadeh, A. Berner, H. Schell, M. Mehta, M. A. Schuetz, G. N. Duda, and D. W. Hutmacher. Polycaprolactone scaffold and reduced rhBMP-7 dose for the regeneration of critical-sized defects in sheep tibiae. Biomaterials 34:9960–9968, 2013.

    CAS  PubMed  Google Scholar 

  34. Clarke, B. Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephrol. 3:S131–S139, 2008.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Collins, M. N., and C. Birkinshaw. Hyaluronic acid based scaffolds for tissue engineering-A review. Carbohydr. Polym. 92:1262–1279, 2013.

    CAS  PubMed  Google Scholar 

  36. Collins, A. M., N. J. V. Skaer, T. Gheysens, D. Knight, C. Bertram, H. I. Roach, R. O. C. Oreffo, S. Von-Aulock, T. Baris, J. Skinner, and S. Mann. Bone-like resorbable silk-based scaffolds for load-bearing osteoregenerative applications. Adv. Mater. 21:75–78, 2009.

    CAS  Google Scholar 

  37. Conoscenti, G., V. L. Carrubba, and V. Brucato. A versatile technique to produce porous polymeric Scaffolds: The thermally induced phase separation (TIPS) Method. Arch. Chem. Res. 01:1–3, 2017.

    Google Scholar 

  38. Conoscenti, G., T. Schneider, K. Stoelzel, F. CarfiPavia, V. Brucato, C. Goegele, V. La Carrubba, and G. Schulze-Tanzil. PLLA scaffolds produced by thermally induced phase separation (TIPS) allow human chondrocyte growth and extracellular matrix formation dependent on pore size. Mater. Sci. Eng. C 80:449–459, 2017.

    CAS  Google Scholar 

  39. Cornell, C. N., J. M. Lane, M. Chapman, R. Merkow, D. Seligson, S. Henry, R. Gustilo, and K. Vincent. Multicenter trial of Collagraft as bone graft substitute. J. Orthop. Trauma 5:1–8, 1991.

    CAS  PubMed  Google Scholar 

  40. Costantini, M., and A. Barbetta. Gas foaming technologies for 3D scaffold engineering. Funct. Tissue Eng. Scaffolds 5:127–149, 2018.

    Google Scholar 

  41. Crockett, J. C., D. J. Mellis, D. I. Scott, and M. H. Helfrich. New knowledge on critical osteoclast formation and activation pathways from study of rare genetic diseases of osteoclasts: focus on the RANK/RANKL axis. Osteoporos. Int. 22:1–20, 2011.

    CAS  PubMed  Google Scholar 

  42. Crovace, A. M., A. D. Giancamillo, F. Gervaso, L. Mangiavini, D. Zani, F. Scalera, B. Palazzo, D. Izzo, M. Agnoletto, M. Domenicucci, C. Sosio, A. Sannino, M. D. Giancamillo, and G. M. Peretti. Evaluation of in vivo response of three biphasic scaffolds for osteochondral tissue regeneration in a sheep model. Vet. Sci. 6:90, 2019.

    PubMed Central  Google Scholar 

  43. Cui, X., T. Boland, D. D. D’Lima, and M. K. Lotz. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat. Drug Deliv. Formul. 6:149–155, 2012.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Dababneh, A. B., and I. T. Ozbolat. Bioprinting technology: A current state-of-the-art review. J. Manufactur. Sci. Eng. Trans. ASME 136:6, 2014.

    Google Scholar 

  45. Dallas, S. L., and L. F. Bonewald. Dynamics of the transition from osteoblast to osteocyte. Skeletal Biol. Med. 1192:437–443, 2010.

    CAS  Google Scholar 

  46. Damsky, C. H. Extracellular matrix–integrin interactions in osteoblast function and tissue remodeling. Bone 25:95–96, 1999.

    CAS  PubMed  Google Scholar 

  47. Darus, F., and M. Jaafar. Enhancement of carbonate apatite scaffold properties with surface treatment and alginate and gelatine coating. J. Porous Mater. 27:831–842, 2020.

    CAS  Google Scholar 

  48. Di Martino, A., M. Sittinger, and M. V. Risbud. Chitosan: A versatile biopolymer for orthopaedic tissue-engineering. Biomaterials 26:5983–5990, 2005.

    PubMed  Google Scholar 

  49. Donnaloja, F., E. Jacchetti, M. Soncini, and M. T. Raimondi. Natural and synthetic polymers for bone scaffolds optimization. Polymers 12:905, 2020.

    CAS  PubMed Central  Google Scholar 

  50. dos Santos, D. M., D. S. Correa, E. S. Medeiros, J. E. Oliveira, and L. H. C. Mattoso. Advances in functional polymer nanofibers: From spinning fabrication techniques to recent biomedical applications. ACS Appl. Mater. Interfaces 12:45673–45701, 2020.

    PubMed  Google Scholar 

  51. Drzewiecki, K. E., A. S. Parmar, I. D. Gaudet, J. R. Branch, D. H. Pike, V. Nanda, and D. I. Shreiber. Methacrylation induces rapid, temperature-dependent, reversible self-assembly of type-I collagen. Langmuir 30:11204–11211, 2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Duan, B., E. Kapetanovic, L. A. Hockaday, and J. T. Butcher. Three-dimensional printed trileaflet valve conduits using biological hydrogels and human valve interstitial cells. Acta Biomater. 10:1836–1846, 2014.

    CAS  PubMed  Google Scholar 

  53. Dzobo, K., N. E. Thomford, D. A. Senthebane, H. Shipanga, A. Rowe, C. Dandara, M. Pillay, and K. S. C. M. Motaung. Advances in regenerative medicine and tissue engineering: Innovation and transformation of medicine. Stem Cells Int. 2018. https://doi.org/10.1155/2018/2495848.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Einhorn, T. A., and L. C. Gerstenfeld. Fracture healing: mechanisms and interventions. Nat. Rev. Rheumatol. 11:45–54, 2015.

    PubMed  Google Scholar 

  55. Elbadawi, M., J. Meredith, L. Hopkins, and I. Reaney. Progress in bioactive metal and ceramic implants for load-bearing application. Adv. Tech. Bone Regener. 2016. https://doi.org/10.5772/62598.

    Article  Google Scholar 

  56. Eltom, A., G. Zhong, and A. Muhammad. Scaffold techniques and designs in tissue engineering functions and purposes: A review. Adv. Mater. Sci. Eng. 2019:1–13, 2019.

    Google Scholar 

  57. Everts, V., J. M. Delaisse, W. Korper, D. C. Jansen, W. Tigchelaar-Gutter, P. Saftig, and W. Beertsen. The bone lining cell: Its role in cleaning Howship’s lacunae and initiating bone formation. J. Bone Miner. Res. 17:77–90, 2002.

    CAS  PubMed  Google Scholar 

  58. Fernandez de Grado, G., L. Keller, Y. Idoux-Gillet, Q. Wagner, A.-M. Musset, N. Benkirane-Jessel, F. Bornert, and D. Offner. Bone substitutes: A review of their characteristics, clinical use, and perspectives for large bone defects management. J. Tissue Eng. 9:2041731418776819, 2018.

    PubMed  PubMed Central  Google Scholar 

  59. Florencio-Silva, R., G. R. D. Sasso, E. Sasso-Cerri, M. J. Simoes, and P. S. Cerri. Biology of bone tissue: structure, function, and factors that influence bone cells. Biomed Res. Int. 2015. https://doi.org/10.1155/2015/421746.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Gan, D. L., M. Liu, T. Xu, K. F. Wang, H. Tan, and X. Lu. Chitosan/biphasic calcium phosphate scaffolds functionalized with BMP-2-encapsulated nanoparticles and RGD for bone regeneration. J. Biomed. Mater. Res. Part A 106:2613–2624, 2018.

    CAS  Google Scholar 

  61. Gao, C. D., Y. W. Deng, P. Feng, Z. Z. Mao, P. J. Li, B. Yang, J. J. Deng, Y. Y. Cao, C. J. Shuai, and S. P. Peng. Current progress in bioactive ceramic scaffolds for bone repair and regeneration. Int. J. Mol. Sci. 15:4714–4732, 2014.

    PubMed  PubMed Central  Google Scholar 

  62. Gay, S., G. Lefebvre, M. Bonnin, B. Nottelet, F. Boury, A. Gibaud, and B. Calvignac. PLA scaffolds production from Thermally Induced Phase Separation: Effect of process parameters and development of an environmentally improved route assisted by supercritical carbon dioxide. J. Supercrit. Fluids 136:123–135, 2018.

    CAS  Google Scholar 

  63. Ghassemi, T., A. Shahroodi, M. H. Ebrahimzadeh, A. Mousavian, J. Movaffagh, and A. Moradi. Current concepts in scaffolding for bone tissue engineering. Arch. Bone Jt. Surg. 6:90–99, 2018.

    PubMed  PubMed Central  Google Scholar 

  64. Glass, D. A., P. Bialek, J. D. Ahn, M. Starbuck, M. S. Patel, H. Clevers, M. M. Taketo, F. X. Long, A. P. McMahon, R. A. Lang, and G. Karsenty. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev. Cell 8:751–764, 2005.

    CAS  PubMed  Google Scholar 

  65. Grottkau, B. E., Z. Hui, Y. Yao, and Y. Pang. Rapid fabrication of anatomically-shaped bone scaffolds using indirect 3D printing and perfusion techniques. Int. J. Mol. Sci. 21:315, 2020.

    CAS  PubMed Central  Google Scholar 

  66. Guillemot, F., A. Souquet, S. Catros, B. Guillotin, J. Lopez, M. Faucon, B. Pippenger, R. Bareille, M. Remy, S. Bellance, P. Chabassier, J. C. Fricain, and J. Amedee. High-throughput laser printing of cells and biomaterials for tissue engineering. Acta Biomater. 6:2494–2500, 2010.

    CAS  PubMed  Google Scholar 

  67. Guillotin, B., A. Souquet, S. Catros, M. Duocastella, B. Pippenger, S. Bellance, R. Bareille, M. Remy, L. Bordenave, J. Amedee, and F. Guillemot. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials 31:7250–7256, 2010.

    CAS  PubMed  Google Scholar 

  68. Hench, L. L., and J. M. Polak. Third-generation biomedical materials. Science 295:1014, 2002.

    CAS  PubMed  Google Scholar 

  69. Huang, W., X. Li, X. Shi, and C. Lai. Microsphere based scaffolds for bone regenerative applications. Biomater. Sci. 2:1145, 2014.

    CAS  PubMed  Google Scholar 

  70. C.W. Hull, Apparatus for production of three-dimensional objects by stereolithography, https://patents.google.com/patent/US4575330A/en, 3D Systems Inc, USA, 1984.

  71. Jakus, A. E., A. L. Rutz, S. W. Jordan, A. Kannan, S. M. Mitchell, C. Yun, K. D. Koube, S. C. Yoo, H. E. Whiteley, C.-P. Richter, R. D. Galiano, W. K. Hsu, S. R. Stock, E. L. Hsu, and R. N. Shah. Hyperelastic “bone”: A highly versatile, growth factor–free, osteoregenerative, scalable, and surgically friendly biomaterial. Sci. Transl. Med. 8:358, 2016.

    Google Scholar 

  72. Ji, C. D., N. Annabi, M. Hosseinkhani, S. Sivaloganathan, and F. Dehghani. Fabrication of poly-(dl)-lactide/polyethylene glycol scaffolds using the gas foaming technique. Acta Biomater. 8:570–578, 2012.

    CAS  PubMed  Google Scholar 

  73. Jimi, E., S. Hirata, K. Osawa, M. Terashita, C. Kitamura, and H. Fukushima. The current and future therapies of bone regeneration to repair bone defects. Int. J. Dent. 2012:148261, 2012.

    PubMed  PubMed Central  Google Scholar 

  74. Jose, G., K. T. Shalumon, H.-T. Liao, C.-Y. Kuo, and J.-P. Chen. Preparation and characterization of surface heat sintered nanohydroxyapatite and nanowhitlockite embedded poly (lactic-co-glycolic acid) microsphere bone graft scaffolds. Vitro and in vivo studies. Int. J. Mol. Sci. 21:528, 2020.

    CAS  PubMed Central  Google Scholar 

  75. Jun, I., H.-S. Han, J. Edwards, and H. Jeon. Electrospun fibrous scaffolds for tissue engineering: Viewpoints on architecture and fabrication. Int. J. Mol. Sci. 19:745, 2018.

    PubMed Central  Google Scholar 

  76. Kaliva, M., A. Georgopoulou, D. A. Dragatogiannis, C. A. Charitidis, M. Chatzinikolaidou, and M. Vamvakaki. Biodegradable chitosan-graft-poly(l-lactide) copolymers for bone tissue engineering. Polymers 12:316, 2020.

    CAS  PubMed Central  Google Scholar 

  77. Kim, S., Z.-K. Cui, J. Fan, A. Fartash, T. L. Aghaloo, and M. Lee. Photocrosslinkable chitosan hydrogels functionalized with the RGD peptide and phosphoserine to enhance osteogenesis. J. Mater. Chem. B 4:5289–5298, 2016.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Kim, M. S., and G. Kim. Three-dimensional electrospun polycaprolactone (PCL)/alginate hybrid composite scaffolds. Carbohydr. Polym. 114:213–221, 2014.

    CAS  PubMed  Google Scholar 

  79. Kokubo, T., H. M. Kim, M. Kawashita, and T. Nakamura. REVIEW Bioactive metals: Preparation and properties. J. Mater. Sci. Mater. Med. 15:99–107, 2004.

    CAS  PubMed  Google Scholar 

  80. Kundu, B., N. E. Kurland, S. Bano, C. Patra, F. B. Engel, V. K. Yadavalli, and S. C. Kundu. Silk proteins for biomedical applications: Bioengineering perspectives. Prog. Polym. Sci. 39:251–267, 2014.

    CAS  Google Scholar 

  81. Kundu, J., F. Pati, J. H. Shim, and D. W. Cho. Rapid prototyping technology for bone regeneration. Rapid Prototyp. Biomater. 70:254–284, 2014.

    CAS  Google Scholar 

  82. Lee, D. J., S. Diachina, Y. T. Lee, L. Zhao, R. Zou, N. Tang, H. Han, X. Chen, and C.-C. Ko. Decellularized bone matrix grafts for calvaria regeneration. J. Tissue Eng. 7:2041731416680306, 2016.

    PubMed  PubMed Central  Google Scholar 

  83. Li, J. P., M. J. Chen, X. Q. Fan, and H. F. Zhou. Recent advances in bioprinting techniques: approaches, applications and future prospects. J. Transl. Med. 14:1–15, 2016.

    Google Scholar 

  84. Li, Y., S.-K. Chen, L. Li, L. Qin, X.-L. Wang, and Y.-X. Lai. Bone defect animal models for testing efficacy of bone substitute biomaterials. J. Orthop. Transl. 3:95–104, 2015.

    Google Scholar 

  85. Li, J. J., K. Kim, S. I. Roohani-Esfahani, J. Guo, D. L. Kaplan, and H. Zreiqat. A biphasic scaffold based on silk and bioactive ceramic with stratified properties for osteochondral tissue regeneration. J. Mater. Chem. B 3:5361–5376, 2015.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Li, Q., T. Wang, G.-F. Zhang, X. Yu, J. Zhang, G. Zhou, and Z.-H. Tang. A Comparative evaluation of the mechanical properties of two calcium phosphate/collagen composite materials and their osteogenic effects on adipose-derived stem cells. Stem Cells Int. 2016:1–12, 2016.

    Google Scholar 

  87. Lin, Y. X., Z. Y. Ding, X. B. Zhou, S. T. Li, M. Xie, Z. Z. Li, and G. D. Sun. In vitro and in vivo evaluation of the developed PLGA/HAp/Zein scaffolds for bone-cartilage interface regeneration. Biomed. Environ. Sci. 28:1–12, 2015.

    PubMed  Google Scholar 

  88. Lin, Y., M. Umebayashi, M.-N. Abdallah, G. Dong, M. G. Roskies, Y. F. Zhao, M. Murshed, Z. Zhang, and S. D. Tran. Combination of polyetherketoneketone scaffold and human mesenchymal stem cells from temporomandibular joint synovial fluid enhances bone regeneration. Sci. Rep. 2019. https://doi.org/10.1038/s41598-018-36778-2.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Liu, M., and Y. Lv. Reconstructing bone with natural bone graft: A review of in vivo studies in bone defect animal model. Nanomaterials 8:999, 2018.

    PubMed Central  Google Scholar 

  90. Loordhuswamy, A., S. Thinakaran, and G. D. Venkateshwapuram Rangaswamy. Centrifugal spun osteoconductive ultrafine fibrous mat as a scaffold for bone regeneration. J. Drug Deliv. Sci. Technol. 60:101978, 2020.

    CAS  Google Scholar 

  91. Lu, J., and X. Wang. Biomimetic self-assembling peptide hydrogels for tissue engineering applications. Biomimetic Med. Mater. 1064:297–312, 2018.

    CAS  Google Scholar 

  92. Manassero, M., A. Decambron, N. Guillemin, H. Petite, R. Bizios, and V. Viateau. Coral scaffolds in bone tissue engineering and bone regeneration. Cnidaria: Past Present Future, pp. 691–714, 2016.

    Google Scholar 

  93. Mandrycky, C., Z. J. Wang, K. Kim, and D. H. Kim. 3D bioprinting for engineering complex tissues. Biotechnol. Adv. 34:422–434, 2016.

    CAS  PubMed  Google Scholar 

  94. Marelli, B., C. E. Ghezzi, A. Alessandrino, J. E. Barralet, G. Freddi, and S. N. Nazhat. Silk fibroin derived polypeptide-induced biomineralization of collagen. Biomaterials 33:102–108, 2012.

    CAS  PubMed  Google Scholar 

  95. Martin, R. B., D. B. Burr, N. A. Sharkey, and D. P. Fyhrie. Mechanical Properties of Bone. Skeletal Tissue Mech. 12:355–422, 2015.

    Google Scholar 

  96. Maude, S., E. Ingham, and A. Aggeli. Biomimetic self-assembling peptides as scaffolds for soft tissue engineering. Nanomedicine 8:823–847, 2013.

    CAS  PubMed  Google Scholar 

  97. McGovern, J. A., M. Griffin, and D. W. Hutmacher. Animal models for bone tissue engineering and modelling disease. Dis. Models Mech. 11:4, 2018.

    Google Scholar 

  98. Meinel, L., S. Hofmann, V. Karageorgiou, C. Kirker-Head, J. McCool, G. Gronowicz, L. Zichner, R. Langer, G. Vunjak-Novakovic, and D. L. Kaplan. The inflammatory responses to silk films in vitro and in vivo. Biomaterials 26:147–155, 2005.

    CAS  PubMed  Google Scholar 

  99. Moest, T., K. A. Schlegel, M. Kesting, M. Fenner, R. Lutz, D. M. Beck, E. Nkenke, and C. von Wilmowsky. A new standardized critical size bone defect model in the pig forehead for comparative testing of bone regeneration materials. Clin. Oral Investig. 1:1–11, 2019.

    Google Scholar 

  100. Montero, F. E., R. A. Rezende, J. V. L. da Silva, and M. A. Sabino. Development of a smart bioink for bioprinting applications. Front. Mech. Eng. 5:56, 2019.

    Google Scholar 

  101. Morgan, E. F., G. U. Unnikrisnan, and A. I. Hussein. Bone mechanical properties in healthy and diseased states. Annu. Rev. Biomed. Eng. 20:119–143, 2018.

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Motamedian, S. R., S. Hosseinpour, M. G. Ahsaie, and A. Khojasteh. Smart scaffolds in bone tissue engineering: A systematic review of literature. World J. Stem Cells 7:657–668, 2015.

    PubMed  PubMed Central  Google Scholar 

  103. Murata, M., F. Maki, D. Sato, T. Shibata, and M. Arisue. Bone augmentation by onlay implant using recombinant human BMP-2 and collagen on adult rat skull without periosteum. Clin. Oral Implant Res. 11:289–295, 2000.

    CAS  Google Scholar 

  104. Muzzarelli, R. A. A., M. Mattioli-Belmonte, C. Tietz, R. Biagini, G. Ferioli, M. A. Brunelli, M. Fini, R. Giardino, P. Ilari, and G. Biagini. Stimulatory effect on bone formation exerted by a modified chitosan. Biomaterials 15:1075–1081, 1994.

    CAS  PubMed  Google Scholar 

  105. Navarro, M., A. Michiardi, O. Castano, and J. A. Planell. Biomaterials in orthopaedics. J. R. Soc. Interface 5:1137–1158, 2008.

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Nguyen, L. H., N. Annabi, M. Nikkhah, H. Bae, L. Binan, S. Park, Y. Q. Kang, Y. Z. Yang, and A. Khademhosseini. Vascularized bone tissue engineering: Approaches for potential improvement. Tissue Eng. Part B 18:363–382, 2012.

    CAS  Google Scholar 

  107. Nguyen, T. B. L., and B. T. Lee. A combination of biphasic calcium phosphate scaffold with hyaluronic acid-gelatin hydrogel as a new tool for bone regeneration. Tissue Eng. Part A 20:1993–2004, 2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  108. O’Brien, F. J. Biomaterials & scaffolds for tissue engineering. Mater. Today 14:88–95, 2011.

    Google Scholar 

  109. Orwoll, E. S. Clinical practice guidelines for osteoporosis: Translating data to patients? Ann. Intern. Med. 166:852–853, 2017.

    PubMed  Google Scholar 

  110. Pamula, E., J. Kokoszka, K. Cholewa-Kowalska, M. Laczka, L. Kantor, L. Niedzwiedzki, G. C. Reilly, J. Filipowska, W. Madej, M. Kolodziejczyk, G. Tylko, and A. M. Osyczka. Degradation, bioactivity, and osteogenic potential of composites made of PLGA and two different sol–gel bioactive glasses. Ann. Biomed. Eng. 39:2114–2129, 2011.

    PubMed  PubMed Central  Google Scholar 

  111. Pati, F., J. Jang, J. W. Lee, and D.-W. Cho. Extrusion Bioprinting, Essentials of 3D Biofabrication and Translation. Boca Raton: Academic Press, pp. 123–152, 2015.

    Google Scholar 

  112. Phipps, M. C., W. C. Clem, J. M. Grunda, G. A. Dines, and S. L. Bellis. Increasing the pore sizes of bone-mimetic electrospun scaffolds comprised of polycaprolactone, collagen I and hydroxyapatite to enhance cell infiltration. Biomaterials 33:524–534, 2012.

    CAS  PubMed  Google Scholar 

  113. Policastro, G. M., F. Lin, L. A. SmithCallahan, A. Esterle, M. Graham, K. SloanStakleff, and M. L. Becker. OGP functionalized phenylalanine-based poly(ester urea) for enhancing osteoinductive potential of human mesenchymal stem cells. Biomacromolecules 16:1358–1371, 2015.

    CAS  PubMed  Google Scholar 

  114. Polo-Corrales, L., M. Latorre-Esteves, and J. E. Ramirez-Vick. Scaffold design for bone regeneration. J. Nanosci. Nanotechnol. 14:15–56, 2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Prakash, D., and D. Learmonth. Natural progression of osteo-chondral defect in the femoral condyle. Knee 9:7–10, 2002.

    PubMed  Google Scholar 

  116. Qaseem, A., M. A. Forciea, R. M. McLean, T. D. Denberg, and C. G. C. A. Coll. Treatment of low bone density or osteoporosis to prevent fractures in men and women: A clinical practice guideline update from the American College of Physicians. Ann. Internal Med. 166:818, 2017.

    Google Scholar 

  117. Qu, H., H. Fu, Z. Han, and Y. Sun. Biomaterials for bone tissue engineering scaffolds: a review. RSC Adv. 9:26252–26262, 2019.

    CAS  Google Scholar 

  118. Randall, I. Liquid-in-liquid printing method could put 3D-printed organs in reach. Science 2019. https://doi.org/10.1126/science.aba0750.

    Article  PubMed  Google Scholar 

  119. Ratnayake, J. T. B., M. Mucalo, and G. J. Dias. Substituted hydroxyapatites for bone regeneration: A review of current trends. J. Biomed. Mater. Res. Part B 105:1285–1299, 2017.

    CAS  Google Scholar 

  120. Rezwan, K., Q. Z. Chen, J. J. Blaker, and A. R. Boccaccini. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27:3413–3431, 2006.

    CAS  PubMed  Google Scholar 

  121. Rhee, S., J. L. Puetzer, B. N. Mason, C. A. Reinhart-King, and L. J. Bonassar. 3D bioprinting of spatially heterogeneous collagen constructs for cartilage tissue engineering. ACS Biomater. Sci. Eng. 2:1800–1805, 2016.

    CAS  PubMed  Google Scholar 

  122. Ripamonti, U. The morphogenesis of bone in replicas of porous hydroxyapatite obtained from conversion of calcium-carbonate exoskeletons of coral. J. Bone Joint Surg. Am. 73:692–703, 1991.

    CAS  PubMed  Google Scholar 

  123. Rodel, M., K. Baumann, J. Groll, and U. Gbureck. Simultaneous structuring and mineralization of silk fibroin scaffolds. J. Tissue Eng. 9:2041731418788509, 2018.

    PubMed  PubMed Central  Google Scholar 

  124. Rodriguez-Salvador, M., R. M. Rio-Belver, and G. Garechana-Anacabe. Scientometric and patentometric analyses to determine the knowledge landscape in innovative technologies: The case of 3D bioprinting. PLoS ONE 12:e0180375, 2017.

    PubMed  PubMed Central  Google Scholar 

  125. Roseti, L., V. Parisi, M. Petretta, C. Cavallo, G. Desando, I. Bartolotti, and B. Grigolo. Scaffolds for bone tissue engineering: State of the art and new perspectives. Mater. Sci. Eng. C 78:1246–1262, 2017.

    CAS  Google Scholar 

  126. Ruehe, B., S. Niehues, S. Heberer, and K. Nelson. Miniature pigs as an animal model for implant research: bone regeneration in critical-size defects. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endodontol. 108:699–706, 2009.

    Google Scholar 

  127. Saleem, M., S. Rasheed, and C. Yougen. Silk fibroin/hydroxyapatite scaffold: A highly compatible material for bone regeneration. Sci. Technol. Adv. Mater. 21:242–266, 2020.

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Saravanan, S., R. S. Leena, and N. Selvamurugan. Chitosan based biocomposite scaffolds for bone tissue engineering. Int. J. Biol. Macromol. 93:1354–1365, 2016.

    CAS  PubMed  Google Scholar 

  129. Scaglione, S., P. Giannoni, P. Bianchini, M. Sandri, R. Marotta, G. Firpo, U. Valbusa, A. Tampieri, A. Diaspro, P. Bianco, and R. Quarto. Order versus Disorder: In vivo bone formation within osteoconductive scaffolds. Sci. Rep. 2:274, 2012.

    PubMed  PubMed Central  Google Scholar 

  130. Schaffler, M. B., W. Y. Cheung, R. Majeska, and O. Kennedy. Osteocytes: Master orchestrators of bone. Calcif. Tissue Int. 94:5–24, 2014.

    CAS  PubMed  Google Scholar 

  131. Seol, Y. J., J. Y. Lee, Y. J. Park, Y. M. Lee, K. Young, I. C. Rhyu, S. J. Lee, S. B. Han, and C. P. Chung. Chitosan sponges as tissue engineering scaffolds for bone formation. Biotechnol. Lett. 26:1037–1041, 2004.

    CAS  PubMed  Google Scholar 

  132. Shi, C., Z. Yuan, F. Han, C. Zhu, and B. Li. Polymeric biomaterials for bone regeneration. Ann. Jt. 1:27–27, 2016.

    Google Scholar 

  133. Singh, M. R., S. Patel, and D. Singh. Natural polymer-based hydrogels as scaffolds for tissue engineering. Nanobiomater. Soft Tissue Eng. 5:231–260, 2016.

    CAS  Google Scholar 

  134. Sohn, H. S., and J. K. Oh. Review of bone graft and bone substitutes with an emphasis on fracture surgeries. Biomater. Res. 23:9, 2019.

    PubMed  PubMed Central  Google Scholar 

  135. Sokolova, V., K. Kostka, K. T. Shalumon, O. Prymak, J.-P. Chen, and M. Epple. Synthesis and characterization of PLGA/HAP scaffolds with DNA-functionalised calcium phosphate nanoparticles for bone tissue engineering. J. Mater. Sci. 31:1–12, 2020.

    Google Scholar 

  136. Song, J.-L., X.-Y. Fu, A. Raza, N.-A. Shen, Y.-Q. Xue, H.-J. Wang, and J.-Y. Wang. Enhancement of mechanical strength of TCP-alginate based bioprinted constructs. J. Mech. Behav. Biomed. Mater. 103:103533, 2020.

    CAS  PubMed  Google Scholar 

  137. Soysa, N. S., N. Alles, K. Aoki, and K. Ohya. Osteoclast formation and differentiation: An overview. J Med Dent Sci 59:65–74, 2012.

    PubMed  Google Scholar 

  138. Su, A., and S. J. Al’Aref. History of 3D Printing, 3D Printing Applications in Cardiovascular Medicine. Boca Raton: Academic Press, pp. 1–10, 2018.

    Google Scholar 

  139. Subramaniam, S., Y. H. Fang, S. Sivasubramanian, F. H. Lin, and C. P. Lin. Hydroxyapatite-calcium sulfate-hyaluronic acid composite encapsulated with collagenase as bone substitute for alveolar bone regeneration. Biomaterials 74:99–108, 2016.

    CAS  PubMed  Google Scholar 

  140. Tamay, D. G., T. DursunUsal, A. S. Alagoz, D. Yucel, N. Hasirci, and V. Hasirci. 3D and 4D printing of polymers for tissue engineering applications. Front. Bioeng. Biotechnol. 7:164, 2019.

    PubMed  PubMed Central  Google Scholar 

  141. Tamay, D. G., T. D. Usal, A. S. Alagoz, D. Yucel, N. Hasirci, and V. Hasirci. 3D and 4D printing of polymers for tissue engineering applications. Front. Bioeng. Biotechnol. 7:164, 2019.

    PubMed  PubMed Central  Google Scholar 

  142. Tan, Z., C. Parisi, L. Di Silvio, D. Dini, and A. E. Forte. Cryogenic 3D printing of super soft hydrogels. Sci. Rep. 7:16293, 2017.

    PubMed  PubMed Central  Google Scholar 

  143. Tarafder, S., and S. Bose. Polycaprolactone-coated 3D printed tricalcium phosphate scaffolds for bone tissue engineering, vitro alendronate release behavior and local delivery effect on in vivo osteogenesis. ACS Appl. Mater. Interfaces 6:9955–9965, 2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Teixeira, S., H. Fernandes, A. Leusink, C. van Blitterswijk, M. P. Ferraz, F. J. Monteiro, and J. de Boer. In vivo evaluation of highly macroporous ceramic scaffolds for bone tissue engineering. J. Biomed. Mater. Res. Part A 93:567–575, 2010.

    CAS  Google Scholar 

  145. Thadavirul, N., P. Pavasant, and P. Supaphol. Development of polycaprolactone porous scaffolds by combining solvent casting, particulate leaching, and polymer leaching techniques for bone tissue engineering. J. Biomed. Mater. Res. Part A 102(10):3379–3392, 2013.

    Google Scholar 

  146. Thanh, D. T. M., P. T. T. Trang, N. T. Thom, N. T. Phuong, P. T. Nam, N. T. T. Trang, J. Seo-Park, and T. Hoang. Effects of porogen on structure and properties of poly lactic acid/hydroxyapatite nanocomposites (PLA/HAp). J. Nanosci. Nanotechnol. 16:9450–9459, 2016.

    CAS  Google Scholar 

  147. Turco, G., E. Marsich, F. Bellomo, S. Semeraro, I. Donati, F. Brun, M. Grandolfo, A. Accardo, and S. Paoletti. Alginate/hydroxyapatite biocomposite for bone ingrowth: A trabecular structure with high and isotropic connectivity. Biomacromolecules 10:1575–1583, 2009.

    CAS  PubMed  Google Scholar 

  148. Turnbull, G., J. Clarke, F. Picard, P. Riches, L. Jia, F. Han, B. Li, and W. Shu. 3D bioactive composite scaffolds for bone tissue engineering. Bioactive Mater. 3:278–314, 2018.

    Google Scholar 

  149. Valot, L., J. Martinez, A. Mehdi, and G. Subra. Chemical insights into bioinks for 3D printing. Chem. Soc. Rev. 48:4049–4086, 2019.

    CAS  PubMed  Google Scholar 

  150. Velasco, M. A., C. A. Narváez-Tovar, and D. A. Garzón-Alvarado. Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering. Biomed. Res. Int. 2015:1–21, 2015.

    Google Scholar 

  151. Venkatesan, J., and S. K. Kim. Chitosan composites for bone tissue engineering-an overview. Marine Drugs 8:2252–2266, 2010.

    CAS  PubMed  PubMed Central  Google Scholar 

  152. Wang, M. M., R. L. Flores, L. Witek, A. Torroni, A. Ibrahim, Z. Wang, H. A. Liss, B. N. Cronstein, C. D. Lopez, S. G. Maliha, and P. G. Coelho. Dipyridamole-loaded 3D-printed bioceramic scaffolds stimulate pediatric bone regeneration in vivo without disruption of craniofacial growth through facial maturity. Sci. Rep. 9:1–15, 2019.

    Google Scholar 

  153. Wang, C., J. Tanjaya, J. Shen, S. Lee, B. Bisht, H. C. Pan, S. Pang, Y. Zhang, E. A. Berthiaume, E. Chen, A. L. Da Lio, X. Zhang, K. Ting, S. Guo, and C. Soo. Peroxisome proliferator-activated receptor-γ knockdown impairs bone morphogenetic protein-2-induced critical-size bone defect repair. Am. J. Pathol. 189:648–664, 2019.

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Weiss, L. E., C. H. Amon, S. Finger, E. D. Miller, D. Romero, I. Verdinelli, L. M. Walker, and P. G. Campbell. Bayesian computer-aided experimental design of heterogeneous scaffolds for tissue engineering. Comput. Aided Des. 37:1127–1139, 2005.

    Google Scholar 

  155. Wijshoff, H. The dynamics of the piezo inkjet printhead operation. Phys. Rep. 491:77–177, 2010.

    CAS  Google Scholar 

  156. Wilkinson, D. C., J. A. Alva-Ornelas, J. M. S. Sucre, P. Vijayaraj, A. Durra, W. Richardson, S. J. Jonas, M. K. Paul, S. Karumbayaram, B. Dunn, and B. N. Gomperts. Development of a three-dimensional bioengineering technology to generate lung tissue for personalized disease modeling. Stem Cells Transl. Med. 6:622–633, 2017.

    PubMed  Google Scholar 

  157. Woodruff, M. A., C. Lange, J. Reichert, A. Berner, F. L. Chen, P. Fratzl, J. T. Schantz, and D. W. Hutmacher. Bone tissue engineering: from bench to bedside. Mater. Today 15:430–435, 2012.

    CAS  Google Scholar 

  158. Xu, T., J. Jin, C. Gregory, J. J. Hickman, and T. Boland. Inkjet printing of viable mammalian cells. Biomaterials 26:93–99, 2005.

    PubMed  Google Scholar 

  159. Xu, C. X., P. Q. Su, X. F. Chen, Y. C. Meng, W. H. Yu, A. P. Xiang, and Y. J. Wang. Biocompatibility and osteogenesis of biomimetic bioglass–collagen–phosphatidylserine composite scaffolds for bone tissue engineering. Biomaterials 32:1051–1058, 2011.

    CAS  PubMed  Google Scholar 

  160. Xu, H. H. K., L. Zhao, and M. D. Weir. Stem cell-calcium phosphate constructs for bone engineering. J. Dent. Res. 89:1482–1488, 2010.

    CAS  PubMed  PubMed Central  Google Scholar 

  161. Xu, T., W. X. Zhao, J. M. Zhu, M. Z. Albanna, J. J. Yoo, and A. Atala. Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials 34:130–139, 2013.

    PubMed  Google Scholar 

  162. Yang, H., N. Hong, H. Liu, J. Wang, Y. Li, and S. Wu. Differentiated adipose-derived stem cell cocultures for bone regeneration in RADA16-I in vitro. J. Cell. Physiol. 233:9458–9472, 2018.

    CAS  PubMed  Google Scholar 

  163. Yuan, N., K. S. Rezzadeh, and J. C. Lee. Biomimetic scaffolds for osteogenesis. Receptors Clin. Investig. 2:3, 2015.

    CAS  Google Scholar 

  164. Zaky, S. H., and R. Cancedda. Engineering craniofacial structures: Facing the challenge. J. Dent. Res. 88:1077–1091, 2009.

    CAS  PubMed  Google Scholar 

  165. Zhai, P., X. Peng, B. Li, Y. Liu, H. Sun, and X. Li. The application of hyaluronic acid in bone regeneration. Int. J. Biol. Macromol. 151:1224–1239, 2020.

    CAS  PubMed  Google Scholar 

  166. Zhang, D., X. Wu, J. Chen, and K. Lin. The development of collagen based composite scaffolds for bone regeneration. Bioact. Mater. 3:129–138, 2018.

    PubMed  Google Scholar 

  167. Zhao, F., C. Fu, H. Bai, J. Zhu, Z. Niu, Y. Wang, J. Li, X. Yang, and Y. Bai. Enhanced cell proliferation and osteogenic differentiation in electrospun PLGA/hydroxyapatite nanofibre scaffolds incorporated with graphene oxide. PLoS ONE 12:e0188352, 2017.

    Google Scholar 

  168. Zhu, N., and X. Che. Biofabrication of tissue scaffolds. Adv. Biomater. Sci. Biomed. Appl. 1:11, 2013. https://doi.org/10.5772/54125.

    Article  CAS  Google Scholar 

  169. Zhu, M. L., S. Lin, Y. X. Sun, Q. Feng, G. Li, and L. M. Bian. Hydrogels functionalized with N-cadherin mimetic peptide enhance osteogenesis of hMSCs by emulating the osteogenic niche. Biomaterials 77:44–52, 2016.

    CAS  PubMed  Google Scholar 

  170. Zilberman, M. Active implants and scaffolds for tissue regeneration. Active Implants Scaffolds Tissue Regener. 8:1–514, 2011.

    Google Scholar 

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Acknowledgments

M.P. acknowledges Prof. Steven Dubinett, Prof. Brigitte Gomperts and Prof. Volker Hartenstein, from UCLA for providing constant support and mentoring. A.M. takes this opportunity to acknowledge Raktim Chattopadhyay of Esperer Onco Nutrition Pvt. Ltd. for his constant support. B.B. would like to acknowledge Prof. Jay M. Lee, Prof. Steven Dubinett, and Prof. Brigitte Gomperts, from UCLA for providing constant support and mentoring.

Author Contributions

Conceptualization, MP; writing - original draft preparation, BB, AH, AM, and MP, review and editing, MP.

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Authors and Affiliations

  1. School of Thoracic Surgery, David Geffen School of Medicine, University of California Los Angeles (UCLA), Los Angeles, CA, 90095, USA

    Bharti Bisht

  2. Molecular, Cell, and Developmental Biology, UCLA, Los Angeles, CA, 90095, USA

    Ashley Hope

  3. Esperer Onco Nutrition Pvt. Ltd., Plot No. 247, Pearl Town, Aliabad Village, Shameerpet Mandal, Ranga Reddy District, Hyderabad, Telangana, 500078, India

    Anubhab Mukherjee

  4. Pulmonary Medicine, David Geffen School of Medicine, UCLA, Los Angeles, CA, 90095, USA

    Manash K. Paul

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Bisht, B., Hope, A., Mukherjee, A. et al. Advances in the Fabrication of Scaffold and 3D Printing of Biomimetic Bone Graft. Ann Biomed Eng 49, 1128–1150 (2021). https://doi.org/10.1007/s10439-021-02752-9

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