Application of Bioprinting in Ophthalmology

Authors

  • Yanfang Wang Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of Education, Chongqing, 400045, China;Guangdong Engineering Research Center for Translation of Medical 3D Printing Application, Guangdong Provincial Key Laboratory of Medical Biomechanics, School of Basic Medical Sciences, Southern Medical University, Guangzhou 510515, China;Guangdong Innovation Platform for Translation of 3D Printing Application, The third Affiliated Hospital of Southern Medical University, Guangzhou 510630, China
  • Jiejie Wang Department of Anatomy, School of Basic Medical Sciences, Southern Medical University, Guangzhou 510515, China
  • Ziyu Ji College of Integrated Chinese and Western Medicine, Southwest Medical University, Lu Zhou 646000, China
  • Wei Yan Department of Anatomy, Hebei Medical University, Shijiazhuang 050011, China
  • Hong Zhao School of Basic Medicine, Guangdong Medical University, Dongguan, Guangdong 523000, China
  • Wenhua Huang Guangdong Engineering Research Center for Translation of Medical 3D Printing Application, Guangdong Provincial Key Laboratory of Medical Biomechanics, School of Basic Medical Sciences, Southern Medical University, Guangzhou 510515, China;Guangdong Innovation Platform for Translation of 3D Printing Application, The third Affiliated Hospital of Southern Medical University, Guangzhou 510630, China;Department of Anatomy, School of Basic Medical Sciences, Southern Medical University, Guangzhou 510515, China
  • Huan Liu National Traditional Chinese Medicine Clinical Research Base, The Affiliated Traditional Chinese Medicine Hospital of Southwest Medical University, Luzhou, Sichuan 646000, China

DOI:

https://doi.org/10.18063/ijb.v8i2.552

Keywords:

Bioprinting, Ophthalmology, Bioinks, Biomaterials, Ocular bioprinting

Abstract

Three-dimensional (3D) bioprinting is an emerging technology that is widely used in regenerative medicine. With the continuous development of the technology, it has attracted great attention and demonstrated promising prospects in ophthalmologic applications. In this paper, we review the three main types of 3D bioprinting technologies: Vat polymerizationbased bioprinting, extrusion-based bioprinting, and jetting-based bioprinting. We also present in this review the analysis of the usage of both natural and synthesized hydrogels as well as the types of cells adopted for bioinks. Cornea and retina are the two main types of ocular tissues developed in bioprinting, while other device and implants were also developed for the ocular disease treatment. We also summarize the advantages and limitations as well as the future prospects of the current bioprinting technologies based on systematic reviews.

References

Di Marzio N, Eglin D, Serra T, et al., 2020, Bio-Fabrication: Convergence of 3D Bioprinting and Nano-Biomaterials in Tissue Engineering and Regenerative Medicine. Front Bioeng Biotechnol, 8:326. https://doi.org/10.3389/fbioe.2020.00326

Moroni L, Burdick JA, Highley C, et al., 2018, Biofabrication Strategies for 3D In Vitro Models and Regenerative Medicine. Nature reviews. Materials, 3:21–37. https://doi.org/10.1038/s41578-018-0006-y

Hull CW, Uvp I, 1986, Apparatus for Production of Three dimensional Objects by Stereolithography. Patent US-6027324-A.

Klebe RJ, 1988, Cytoscribing: A Method for Micropositioning Cells and the Construction of Two and Three-dimensional Synthetic Tissues. Exp Cell Res, 179:362–73. https://doi.org/10.1016/0014-4827(88)90275-3

Castilho M, de Ruijter M, Beirne S, et al., 2020, Multitechnology Biofabrication: A New Approach for the Manufacturing of Functional Tissue Structures? Trends Biotechnol, 38:1316–28. https://doi.org/10.1016/j.tibtech.2020.04.014

Maloca PM, Tufail A, Hasler PW, et al., 2019, 3D Printing of the Choroidal Vessels and Tumours Based on Optical Coherence Tomography. Acta Ophthalmol, 97:e313–6. https://doi.org/10.1111/aos.13637

AlQattan B, Yetisen A Kand Butt H, 2018, Direct laser writing of nanophotonic structures on contact lenses. ACS Nano, 12:5130–40. https://doi.org/10.1021/acsnano.8b00222

Park J, Ahn D B, Kim J, et al., 2019, Printing of Wirelessly Rechargeable Solid-state Supercapacitors for Soft, Smart Contact Lenses with Continuous Operations. Sci Adv, 5:eaay0764. https://doi.org/10.1126/sciadv.aay0764

Sommer AC, Blumenthal EZ, 2019, Implementations of 3D Printing in Ophthalmology. Graefes Arch Clin Exp Ophthalmol, 257:1815–22. https://doi.org/10.1007/s00417-019-04312-3

Xie P, Hu Z, Zhang X, et al., 2014, Application of 3-dimensional Printing Technology to Construct an Eye Model for Fundus Viewing Study. PLoS One, 9:e109373. https://doi.org/10.1371/journal.pone.0109373

Ng WL, Lee JM, Zhou M, et al., 2020, Vat Polymerization based Bioprinting-Process, Materials, Applications and Regulatory Challenges. Biofabrication, 12:022001. https://doi.org/10.1088/1758-5090/ab6034

Zhao W, Qin P, Zhang D, et al., 2019, Long Non-coding RNA PVT1 Encapsulated in Bone Marrow Mesenchymal Stem Cell-derived Exosomes Promotes Osteosarcoma Growth and Metastasis by Stabilizing ERG and Sponging miR-183-5p. Aging (Albany NY), 11:9581–96. https://doi.org/10.18632/aging.102406

Hinczewski C, Corbel S, Chartier T, 1998, Ceramic Suspensions Suitable for Stereolithography. J Eur Ceram Soc, 18:583–90. https://doi.org/10.1016/S0955-2219(97)00186-6

Zhu W, Ma X, Gou M, et al., 2016, 3D Printing of Functional Biomaterials for Tissue Engineering. Curr Opin Biotechnol, 40:103–12. https://doi.org/10.1016/j.copbio.2016.03.014

Xing JF, Zheng ML, Duan XM, 2015, Two-photon Polymerization Microfabrication of Hydrogels: An Advanced 3D Printing Technology For Tissue Engineering and Drug Delivery. Chem Soc Rev, 44:5031–9. https://doi.org/10.1039/c5cs00278h

Nguyen AK, Narayan RJ, 2017, Two-photon Polymerization for Biological Applications. Mater Today, 20:314–22. https://doi.org/10.1016/j.mattod.2017.06.004

Jiang T, Munguia-Lopez JG, Flores-Torres S, et al., 2019, Extrusion Bioprinting of Soft Materials: An Emerging Technique for Biological Model Fabrication. Appl Phys Rev, 6:011310. https://doi.org/10.1063/1.5059393

Li X, Liu B, Pei B, et al., 2020, Inkjet Bioprinting of Biomaterials. Chem Rev, 120:10793–833.

Cui X, Boland T, D’Lima DD, et al., 2012, Thermal Inkjet Printing in Tissue Engineering and Regenerative Medicine. Recent Pat Drug Deliv Formul, 6:149–155. https://doi.org/10.2174/187221112800672949

Nishiyama Y, Nakamura M, Henmi C, et al., 2009, Development of a Three-dimensional Bioprinter: Construction of Cell Supporting Structures Using Hydrogel and State-of the-art Inkjet Technology. J Biomech Eng, 131:035001. https://doi.org/10.1115/1.3002759

Nakamura M, Iwanaga S, Henmi C, et al., 2010, Biomatrices and Biomaterials for Future Developments of Bioprinting and Biofabrication. Biofabrication, 2:0141. https://doi.org/10.1088/1758-5082/2/1/014110

Wijshoff H, 2010, The Dynamics of the Piezo Inkjet Printhead Operation. Phys Rep, 491:77–177. https://doi.org/10.1016/j.physrep.20https://doi.org/10.03.003

Christensen K, Xu C, Chai W, et al., 2015, Freeform Inkjet Printing of Cellular Structures with Bifurcations. Biotechnol Bioeng, 112:1047–55. https://doi.org/10.1002/bit.25501

Park JU, Hardy M, Kang SJ, et al., 2007, High-resolution Electrohydrodynamic Jet Printing. Nat Mater, 6:782–9. https://doi.org/10.1038/nmat1974

Poellmann MJ, Barton KL, Mishra S, et al., 2011, Patterned Hydrogel Substrates for Cell Culture with Electrohydrodynamic Jet Printing. Macromol Biosci, 11:1164–8. https://doi.org/10.1002/mabi.201100004

Dorishetty P, Dutta NK, Choudhury NR, 2020, Bioprintable Tough Hydrogels for Tissue Engineering Applications. Adv Colloid Interface Sci, 281:102163. https://doi.org/10.1016/j.cis.2020.102163

Gu Z, Fu J, Lin H, et al., 2019, Development of 3D Bioprinting: From Printing Methods to Biomedical Applications. Asian J Pharm Sci, 15:529–557. https://doi.org/10.1016/j.ajps.2019.11.003

Sorkio A, Koch L, Koivusalo L, et al., 2018, Human Stem Cell Based Corneal Tissue Mimicking Structures Using Laser-assisted 3D Bioprinting and Functional Bioinks. Biomaterials, 171:57–71. https://doi.org/10.1016/j.biomaterials.2018.04.034

Mecham RP, 2012, Overview of Extracellular Matrix. Curr Protoc Cell Biol, Chapter 10:Unit 10 11. https://doi.org/10.1002/0471143030.cb1001s57

Pati F, Jang J, Ha DH, et al., 2014, Printing Three-dimensional Tissue Analogues with Decellularized Extracellular Matrix Bioink. Nat Commun, 5:3935. https://doi.org/10.1038/ncomms4935

Kim H, Park MN, Kim J, et al., 2019, Characterization of Cornea-specific Bioink: High transparency, Improved In Vivo Safety. J Tissue Eng, 10:2041731418823382. https://doi.org/10.1177/2041731418823382

Maqueda M, Mosquera JL, Garcia-Arumi J, et al., 2021, Repopulation of Decellularized Retinas with hiPSC-derived Retinal Pigment Epithelial and Ocular Progenitor Cells Shows Cell Engraftment, Organization and Differentiation. Biomaterials, 276:121049. https://doi.org/10.1016/j.biomaterials.2021.121049

Wang F, Shi W, Li H, et al., 2020, Decellularized Porcine Cornea-derived Hydrogels for the Regeneration of Epithelium and Stroma in Focal Corneal Defects. Ocul Surf, 18:748–60. https://doi.org/10.1016/j.jtos.2020.07.020

Chameettachal S, Prasad D, Parekh Y, et al., 2021, Prevention of Corneal Myofibroblastic Differentiation In Vitro Using a Biomimetic ECM Hydrogel for Corneal Tissue Regeneration. ACS Appl Bio Mater, 4:533–44. https://doi.org/10.1021/acsabm.0c01112

Bektas CK, Hasirci V, 2020, Cell Loaded 3D Bioprinted GelMA Hydrogels for Corneal Stroma Engineering. Biomater Sci, 8:438–49. https://doi.org/10.1039/C9BM01236B

Leijten J, Seo J, Yue K, et al., 2017, Spatially and Temporally Controlled Hydrogels for Tissue Engineering. Mater Sci Eng R Rep, 119:1–35. https://doi.org/10.1016/j.mser.2017.07.001

Lee KY, Mooney DJ, 2001, Hydrogels for Tissue Engineering. Chem Rev, 101:1869–79. https://doi.org/10.1021/cr000108x

Osidak EO, Karalkin PA, Osidak MS, et al., 2019, Viscoll Collagen Solution as a Novel Bioink for Direct 3D Bioprinting. J Mater Sci Mater Med, 30:31. https://doi.org/10.1007/s10856-019-6233-y

Stepanovska J, Otahal M, Hanzalek K, et al., 2021, pH Modification of High-Concentrated Collagen Bioinks as a Factor Affecting Cell Viability, Mechanical Properties, and Printability. Gels, 7:252. https://doi.org/10.3390/gels7040252

Wu Z, Liu J, Lin J, et al., 2022, Novel Digital Light Processing Printing Strategy Using a Collagen-Based Bioink with Prospective Cross-Linker Procyanidins. Biomacromolecules, 23:240–52. https://doi.org/10.1021/acs.biomac.1c01244

Lee JM, Suen SK, Ng WL, et al., 2021, Bioprinting of Collagen: Considerations, Potentials, and Applications. Macromol Biosci, 21:e2000280. https://doi.org/10.1002/mabi.202000280

Roth EA, Xu T, Das M, et al., 2004, Inkjet printing for high throughput cell patterning. Biomaterials, 25:3707–15. https://doi.org/10.1016/j.biomaterials.2003.10.052

Ng WL, Lee JM, Yeong WY, et al., 2017, Microvalve-based Bioprinting process, Bio-inks and Applications. Biomater Sci, 5:632–47. https://doi.org/10.1039/c6bm00861e

Wang P, Li X, Zhu W, et al., 2018, 3D Bioprinting of Hydrogels for Retina Cell Culturing. Bioprinting (Amsterdam, Netherlands), 11:e00029. https://doi.org/10.1016/j.bprint.2018.e00029

Khalili M, Asadi M, Kahroba H, et al., 2020, Corneal Endothelium Tissue Engineering: An Evolution of Signaling Molecules, Cells, and Scaffolds toward 3D Bioprinting and Cell Sheets. J Cell Physiol, 236:3275–303. https://doi.org/10.1002/jcp.30085

Ashammakhi N, Ahadian S, Xu C, et al., 2019, Bioinks and Bioprinting Technologies to Make Heterogeneous and Biomimetic Tissue Constructs. Materials Today Bio, 1:100008. https://doi.org/10.1016/j.mtbio.2019.100008

West-Mays JA, Dwivedi DJ, 2006, The Keratocyte: Corneal Stromal Cell with Variable Repair Phenotypes. Int J Biochem Cell Biol, 38:1625–31. https://doi.org/10.1016/j.biocel.2006.03.010

Gouveia RM, Connon CJ, 2013, The Effects of Retinoic Acid on Human Corneal Stromal Keratocytes Cultured In Vitro Under Serum-Free Conditions. Investig Ophthalmol Visual Sci, 54:7483–91. https://doi.org/10.1167/iovs.13-13092

Isaacson A, Swioklo S, Connon CJ, 2018, 3D Bioprinting of a Corneal Stroma Equivalent. Exp Eye Res, 173:188–93. https://doi.org/10.1016/j.exer.2018.05.010

Jin K, Wang S, Zhang Y, et al., 2019, Long Non-coding RNA PVT1 Interacts with MYC and its Downstream Molecules to Synergistically Promote Tumorigenesis. Cell Mol Life Sci, 76:4275–89. https://doi.org/10.1007/s00018-019-03222-1

Kim KW, Lee SJ, Park SH, et al., 2018, Ex Vivo Functionality of 3D Bioprinted Corneal Endothelium Engineered with Ribonuclease 5-Overexpressing Human Corneal Endothelial Cells. Adv Healthc Mater, 7:1800398. https://doi.org/10.1002/adhm.201800398

Masland RH, 2011, Cell Populations of the Retina: The Proctor Lecture. Investig Ophthalmol Visual Sci, 52:4581–91. https://doi.org/10.1167/iovs.10-7083

Lorber B, Hsiao WK, Martin KR, 2016, Three-dimensional Printing of the Retina. Curr Opin Ophthalmol, 27:262–7. https://doi.org/10.1097/ICU.0000000000000252

Kador KE, Grogan SP, Dorthé EW, et al., 2016, Control of Retinal Ganglion Cell Positioning and Neurite Growth: Combining 3D Printing with Radial Electrospun Scaffolds. Tissue Eng Part A, 22:286–94. https://doi.org/10.1089/ten.TEA.2015.0373

Yong HE, Qing GA, Liu A, et al., 2019, 3D Bioprinting: From Structure to Function. J Zhejiang Univ, 53:407–19. https://doi.org/10.3785/j.issn.1008-973X.2019.03.001

Farandos NM, Yetisen AK, Monteiro MJ, et al., 2015, Contact Lens Sensors in Ocular Diagnostics. Adv Healthc Mater, 4:792–8. https://doi.org/10.1002/adhm.201400504

Tang H, Alqattan B, Jackson T, et al., 2020, Cost-Efficient Printing of Graphene Nanostructures on Smart Contact Lenses. ACS Applied Materials & Interfaces, 12(9): 10820-10828. https://doi.org/10.1021/acsami.9b21300

Sanchez-Tena MA, Alvarez-Peregrina C, Santos-Arias F, et al., 2019, Application of 3D Printing Technology in Scleral Cover Shell Prosthesis. J Med Syst, 43:149. https://doi.org/10.1007/s10916-019-1280-y

Debellemanière G, Flores M, Montard M, et al., 2016, Three dimensional Printing of Optical Lenses and Ophthalmic Surgery: Challenges and Perspectives. J Refract Surg (Thorofare NJ: 1995), 32:201–4. https://doi.org/10.3928/1081597X-20160121-05

John G, Michal EP, Tomasz ST, 2017, Quantitative Evaluation of Performance of Three-dimensional Printed Lenses. Opt Eng, 56:1–13. https://doi.org/10.1117/1.OE.56.8.084110

Park SH, Su R, Jeong J, et al., 2018, 3D Printed Polymer Photodetectors. Adv Mater (Deerfield Beach, Fla.), 30:e1803980. https://doi.org/10.1002/adma.201803980

Callahan AB, Campbell AA, Petris C, et al., 2017, Low-Cost 3D Printing Orbital Implant Templates in Secondary Orbital Reconstructions. Ophthalmic Plastic Reconstr Surg, 33:376–80. https://doi.org/10.1097/IOP.0000000000000884

Dave TV, Gaur G, Chowdary N, et al., 2018, Customized 3D Printing: A Novel Approach to Migrated Orbital Implant. Saudi J Ophthalmol, 32:330–3. https://doi.org/10.1016/j.sjopt.2018.03.003

Fan B, Chen H, Sun YJ, et al., 2017, Clinical Effects of 3-D Printing-assisted Personalized Reconstructive Surgery for Blowout Orbital Fractures. Graefes Arch Clin Exp Ophthalmol, 255:2051–7. https://doi.org/10.1007/s00417-017-3766-y

Kang S, Kwon J, Ahn CJ, et al., 2018, Generation of Customized Orbital Implant Templates Using 3-dimensional Printing for Orbital Wall Reconstruction. Eye (London, England), 32:1864–70. https://doi.org/10.1038/s41433-018-0193-1

Zamboulis A, Nanaki S, Michailidou G, et al., 2020, Chitosan and its Derivatives for Ocular Delivery Formulations: Recent Advances and Developments. Polymers, 12:1519. https://doi.org/10.3390/polym12071519

Silva MM, Calado R, Marto J, et al., 2017, Chitosan Nanoparticles as a Mucoadhesive Drug Delivery System for Ocular Administration. Mar Drugs, 15:370. https://doi.org/10.3390/md15120370

Başaran E, Yazan Y, 2012, Ocular Application of Chitosan. Exp Opin Drug Deliv, 9:701–12. https://doi.org/10.1517/17425247.2012.681775

Lynch C, Kondiah PP, Choonara YE, et al., 2019, Advances in Biodegradable Nano-Sized Polymer-Based Ocular Drug Delivery. Polymers, 11:1371. https://doi.org/10.3390/polym11081371

Cho H, Jammalamadaka U, Tappa K, 2018, Nanogels for Pharmaceutical and Biomedical Applications and Their Fabrication Using 3D Printing Technologies. Materials (Basel, Switzerland), 11:302. https://doi.org/10.3390/ma11020302

Flaxman SR, Bourne RR, Resnikoff S, et al., 2017, Global Causes of Blindness and Distance Vision Impairment 1990–2020: A Systematic Review and meta analysis. Lancet Global Health, 5:e1221–34. https://doi.org/10.1016/S2214-109X(17)30393-5

Mathews PM, Lindsley K, Aldave AJ, et al., 2018, Etiology of Global Corneal Blindness and Current Practices of Corneal Transplantation: A Focused Review. Cornea, 37:1198–203. https://doi.org/10.1097/ICO.0000000000001666

Gain P, Jullienne R, He Z, et al., 2016, Global Survey of Corneal Transplantation and Eye Banking. JAMA Ophthalmol, 134:167–73. https://doi.org/10.1001/jamaophthalmol.2015.4776

Zhang B, Xue Q, Li J, et al., 2019, 3D bioprinting for Artificial Cornea: Challenges and Perspectives. Med Eng Phys, 71:68–78. https://doi.org/10.1016/j.medengphy.2019.05.002

Fuest M, Yam GH, Mehta JS, et al., 2020, Prospects and Challenges of Translational Corneal Bioprinting. Bioengineering, 7:71. https://doi.org/10.3390/bioengineering7030071

Faye PA, Poumeaud F, Chazelas P, et al., 2021, Focus on Cell Therapy to Treat Corneal Endothelial Diseases. Exp Eye Res, 204:108462. https://doi.org/10.1016/j.exer.2021.108462

Campos DF, Rohde M, Ross M, et al., 2019, Corneal Bioprinting Utilizing Collagen-based Bioinks and Primary Human Keratocytes. J Biomed Mater Res Part A, 107:1945–53. https://doi.org/10.1002/jbm.a.36702

Kong B, Chen Y, Liu R, et al., 2020, Fiber Reinforced GelMA Hydrogel to Induce the Regeneration of Corneal Stroma. Nat Commun, 11:1435–5. https://doi.org/10.1038/s41467-020-14887-9

Kim H, Jang J, Park J, et al., 2019, Shear-induced Alignment of Collagen Fibrils Using 3D Cell Printing for Corneal Stroma Tissue Engineering. Biofabrication, 11:035017. https://doi.org/10.1088/1758-5090/ab1a8b

Holland G, Pandit A, Sanchez-Abella L, et al., 2021, Artificial Cornea: Past, Current, and Future Directions. Front Med (Lausanne), 8:770780. https://doi.org/10.3389/fmed.2021.770780

Hoon M, Okawa H, Santina LD, et al., 2014, Functional Architecture of the Retina: Development and Disease. Prog Retin Eye Res, 42:44–84. https://doi.org/10.1016/j.preteyeres.2014.06.003

Ruiz-Alonso S, Villate-Beitia I, Gallego I, et al., 2021, Current Insights Into 3D Bioprinting: An Advanced Approach for Eye Tissue Regeneration. Pharmaceutics, 13:308. https://doi.org/10.3390/pharmaceutics13030308

Lorber B, Hsiao WK, Hutchings IM, et al., 2014, Adult Rat Retinal Ganglion Cells and Glia can be Printed by Piezoelectric Inkjet Printing. Biofabrication, 6:015001. https://doi.org/10.1088/1758-5082/6/1/015001

Masaeli E, Forster V, Picaud S, et al., 2020, Tissue Engineering of Retina Through High Resolution 3-Dimensional Inkjet Bioprinting. Biofabrication, 12:025006. https://doi.org/10.1088/1758-5090/ab4a20

Masaeli E, Marquette C, 2020, Direct-Write Bioprinting Approach to Construct Multilayer Cellular Tissues. Front Bioeng Biotechnol, 7:478. https://doi.org/10.3389/fbioe.2019.00478

Meek KM, Knupp C, 2015, Corneal Structure and Transparency. Prog Retin Eye Res, 49:1–16. https://doi.org/10.1016/j.preteyeres.2015.07.001

Kutlehria S, Dinh TC, Bagde A, et al., 2020, High-throughput 3D Bioprinting of Corneal Stromal Equivalents. J Biomed Mater Res B Appl Biomater, 108:2981–94. https://doi.org/10.1002/jbm.b.34628

Mahdavi SS, Abdekhodaie MJ, Kumar H, et al., 2020, Stereolithography 3D Bioprinting Method for Fabrication of Human Corneal Stroma Equivalent. Ann Biomed Eng, 48:1955–70. https://doi.org/10.1007/s10439-020-02537-6

Shi P, Edgar TY, Yeong WY, et al., 2017, Hybrid Three dimensional (3D) Bioprinting of Retina Equivalent for Ocular Research. Int J Bioprint, 3:8. https://doi.org/10.18063/IJB.2017.02.008

Worthington KS, Wiley LA, Kaalberg EE, et al., 2017, Two-photon Polymerization for Production of Human iPSC derived Retinal Cell Grafts. Acta Biomater, 55:385–95. https://doi.org/10.1016/j.actbio.2017.03.039

Downloads

Published

2022-02-22