Materials for creating tissue-engineered constructs using 3D bioprinting: cartilaginous and soft tissue restoration

3D Bioprinting is a dynamically developing technology for tissue engineering and regenerative medicine. The main advantage of this technique is its ability to reproduce a given scaffold geometry and structure both in terms of the shape of the tissue-engineered construct and the distribution of its components. The key factor in bioprinting is bio ink, a cell-laden biocompatible material that mimics extracellular matrix. To meet all the requirements, the bio ink must include not only the main material, but also other components ensuring cell proliferation, differentiation and scaffold performance as a whole. The purpose of this review is to describe the most common materials applicable in bioprinting, consider their properties, prospects and limitations in cartilage restoration.

[1]  Dongan Wang,et al.  Effects of permeability and living space on cell fate and neo-tissue development in hydrogel-based scaffolds: a study with cartilaginous model. , 2015, Macromolecular bioscience.

[2]  Anja Lode,et al.  Three‐dimensional plotting of a cell‐laden alginate/methylcellulose blend: towards biofabrication of tissue engineering constructs with clinically relevant dimensions , 2017, Journal of tissue engineering and regenerative medicine.

[3]  Dongan Wang,et al.  Development of size-customized hepatocarcinoma spheroids as a potential drug testing platform using a sacrificial gelatin microsphere system. , 2016, Materials science & engineering. C, Materials for biological applications.

[4]  A. Grumezescu,et al.  Hyaluronic acid-based scaffolds for tissue engineering. , 2018, Romanian journal of morphology and embryology = Revue roumaine de morphologie et embryologie.

[5]  Andreas Kurtz,et al.  Generation of a 3D Liver Model Comprising Human Extracellular Matrix in an Alginate/Gelatin-Based Bioink by Extrusion Bioprinting for Infection and Transduction Studies , 2018, International journal of molecular sciences.

[6]  P. Gatenholm,et al.  Alginate Sulfate–Nanocellulose Bioinks for Cartilage Bioprinting Applications , 2016, Annals of Biomedical Engineering.

[7]  G. Perale,et al.  A Perspective on Polylactic Acid-Based Polymers Use for Nanoparticles Synthesis and Applications , 2019, Front. Bioeng. Biotechnol..

[8]  Eugene Khor,et al.  Implantable applications of chitin and chitosan. , 2003, Biomaterials.

[9]  J. Lewis,et al.  3D Bioprinting of Vascularized, Heterogeneous Cell‐Laden Tissue Constructs , 2014, Advanced materials.

[10]  C. P. Sharma,et al.  Use of chitosan as a biomaterial: studies on its safety and hemostatic potential. , 1997, Journal of biomedical materials research.

[11]  M. Taya,et al.  Differentiation potential of human adipose stem cells bioprinted with hyaluronic acid/gelatin‐based bioink through microextrusion and visible light‐initiated crosslinking , 2018, Biopolymers.

[12]  Nathaniel S. Hwang,et al.  Riboflavin-induced photo-crosslinking of collagen hydrogel and its application in meniscus tissue engineering , 2015, Drug Delivery and Translational Research.

[13]  Zohreh Izadifar,et al.  Analyzing Biological Performance of 3D-Printed, Cell-Impregnated Hybrid Constructs for Cartilage Tissue Engineering. , 2016, Tissue engineering. Part C, Methods.

[14]  G. Vunjak‐Novakovic,et al.  Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. , 2012, Acta biomaterialia.

[15]  K. Tang,et al.  Dissolution of natural polymers in ionic liquids: A review , 2012 .

[16]  Y. Liu,et al.  A Versatile Method for Fabricating Tissue Engineering Scaffolds with a Three-Dimensional Channel for Prevasculature Networks. , 2016, ACS applied materials & interfaces.

[17]  Kai Chen,et al.  Study on the technology and properties of 3D bioprinting SF/GT/n-HA composite scaffolds , 2019, Materials Letters.

[18]  C. Henke,et al.  Extracellular matrix as a driver of progressive fibrosis. , 2018, The Journal of clinical investigation.

[19]  Geunhyung Kim,et al.  Three-Dimensional Hierarchical Nanofibrous Collagen Scaffold Fabricated Using Fibrillated Collagen and Pluronic F-127 for Regenerating Bone Tissue. , 2018, ACS applied materials & interfaces.

[20]  Andrew D. Doyle.  Generation of 3D Collagen Gels with Controlled Diverse Architectures , 2016, Current protocols in cell biology.

[21]  Anders Lindahl,et al.  In Vivo Chondrogenesis in 3D Bioprinted Human Cell-laden Hydrogel Constructs , 2017, Plastic and reconstructive surgery. Global open.

[22]  Ghassem Amoabediny,et al.  The Role of Biodegradable Engineered Scaffold in Tissue Engineering , 2011 .

[23]  Dong-Woo Cho,et al.  Bioprintable, cell-laden silk fibroin-gelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs. , 2015, Acta biomaterialia.

[24]  Hyeongjin Lee,et al.  Strategy to Achieve Highly Porous/Biocompatible Macroscale Cell Blocks, Using a Collagen/Genipin-bioink and an Optimal 3D Printing Process. , 2016, ACS applied materials & interfaces.

[25]  L. Roshangar,et al.  Mechanical and biological performance of printed alginate/methylcellulose/halloysite nanotube/polyvinylidene fluoride bio-scaffolds. , 2018, Materials science & engineering. C, Materials for biological applications.

[26]  M. Keshavarz Moraveji,et al.  Microfluidic assisted synthesis of PLGA drug delivery systems , 2019, RSC advances.

[27]  M. Rinaudo,et al.  Chitin and Chitosan Preparation from Marine Sources. Structure, Properties and Applications , 2015, Marine drugs.

[28]  Yogendra Pratap Singh,et al.  3D Bioprinting using Cross-Linker Free Silk-Gelatin Bioink for Cartilage Tissue Engineering. , 2019, ACS applied materials & interfaces.

[29]  William G Whitford,et al.  A bioink by any other name: terms, concepts and constructions related to 3D bioprinting , 2016, Future science OA.

[30]  Dong-Woo Cho,et al.  Three-dimensional bioprinting of multilayered constructs containing human mesenchymal stromal cells for osteochondral tissue regeneration in the rabbit knee joint , 2016, Biofabrication.

[31]  Yun-yu Hu,et al.  Effects of different cross-linking conditions on the properties of genipin-cross-linked chitosan/collagen scaffolds for cartilage tissue engineering , 2011, Journal of materials science. Materials in medicine.

[32]  Carlos Osuna,et al.  Agarose-Based Hydrogels as Suitable Bioprinting Materials for Tissue Engineering. , 2018, ACS biomaterials science & engineering.

[33]  G. Wallace,et al.  3D printable conducting hydrogels containing chemically converted graphene. , 2017, Nanoscale.

[34]  V. Hasırcı,et al.  PCL and PCL-based materials in biomedical applications , 2018, Journal of biomaterials science. Polymer edition.

[35]  Bochu Wang,et al.  Biodegradation of Silk Biomaterials , 2009, International journal of molecular sciences.

[36]  Fereidoon Shahidi,et al.  Chitin, chitosan, and co-products: chemistry, production, applications, and health effects. , 2005, Advances in food and nutrition research.

[37]  Seung-Schik Yoo,et al.  Generation of Multi-scale Vascular Network System Within 3D Hydrogel Using 3D Bio-printing Technology , 2014, Cellular and molecular bioengineering.

[38]  D. Kaplan,et al.  Hybrid and Composite Scaffolds Based on Extracellular Matrices for Cartilage Tissue Engineering. , 2019, Tissue engineering. Part B, Reviews.

[39]  Geun Hyung Kim,et al.  Development of a tannic acid cross-linking process for obtaining 3D porous cell-laden collagen structure. , 2017, International journal of biological macromolecules.

[40]  Robert Langer,et al.  Physical and mechanical properties of PLA, and their functions in widespread applications - A comprehensive review. , 2016, Advanced drug delivery reviews.

[41]  D. Kelly,et al.  Meniscus ECM‐functionalised hydrogels containing infrapatellar fat pad‐derived stem cells for bioprinting of regionally defined meniscal tissue , 2018, Journal of tissue engineering and regenerative medicine.

[42]  Todd A. Goldstein,et al.  A 3-dimensional bioprinted tracheal segment implant pilot study: Rabbit tracheal resection with graft implantation. , 2019, International journal of pediatric otorhinolaryngology.

[43]  M. Thanou,et al.  Biodegradation, biodistribution and toxicity of chitosan. , 2010, Advanced drug delivery reviews.

[44]  C. K. Chong,et al.  Fabrication of biodegradable synthetic perfusable vascular networks via a combination of electrospinning and robocasting. , 2015, Biomaterials science.

[45]  G. Wallace,et al.  Biofabrication of human articular cartilage: a path towards the development of a clinical treatment , 2018, Biofabrication.

[46]  Zohaib Khurshid,et al.  Biodegradable Materials for Bone Repair and Tissue Engineering Applications , 2015, Materials.

[47]  D. Cho,et al.  Biomimetic 3D tissue printing for soft tissue regeneration. , 2015, Biomaterials.

[48]  M Gelinsky,et al.  A definition of bioinks and their distinction from biomaterial inks , 2018, Biofabrication.

[49]  Priyamvada Pradeep,et al.  Functionalizing bioinks for 3D bioprinting applications. , 2019, Drug discovery today.

[50]  Barry J Doyle,et al.  Mechanical behaviour of alginate-gelatin hydrogels for 3D bioprinting. , 2018, Journal of the mechanical behavior of biomedical materials.

[51]  J. Brownlie,et al.  Biotechnological production of hyaluronic acid: a mini review , 2016, 3 Biotech.

[52]  Kevin J Edgar,et al.  Alginate derivatization: a review of chemistry, properties and applications. , 2012, Biomaterials.

[53]  D. Mooney,et al.  Alginate: properties and biomedical applications. , 2012, Progress in polymer science.

[54]  Ali Khademhosseini,et al.  Extrusion Bioprinting of Shear‐Thinning Gelatin Methacryloyl Bioinks , 2017, Advanced healthcare materials.

[55]  Ye Been Seo,et al.  Publisher Correction: Precisely printable and biocompatible silk fibroin bioink for digital light processing 3D printing , 2018, Nature Communications.

[56]  Jos Malda,et al.  Double printing of hyaluronic acid/poly(glycidol) hybrid hydrogels with poly(ε-caprolactone) for MSC chondrogenesis , 2017, Biofabrication.

[57]  Vipuil Kishore,et al.  Dual crosslinking strategy to generate mechanically viable cell-laden printable constructs using methacrylated collagen bioinks. , 2020, Materials science & engineering. C, Materials for biological applications.

[58]  L. Bonassar,et al.  High density cell seeding affects the rheology and printability of collagen bioinks , 2019, Biofabrication.

[59]  Kedong Song,et al.  3D Bio-Printing of CS/Gel/HA/Gr Hybrid Osteochondral Scaffolds , 2019, Polymers.

[60]  M. Másson,et al.  Antimicrobial Chitosan and Chitosan Derivatives: A Review of the Structure-Activity Relationship. , 2017, Biomacromolecules.

[61]  Keita Ito,et al.  Silk fibroin as biomaterial for bone tissue engineering. , 2016, Acta biomaterialia.

[62]  Ruggero Bettini,et al.  Highly defined 3D printed chitosan scaffolds featuring improved cell growth , 2017, Biomedical materials.

[63]  Liu Yang,et al.  Engineering zonal cartilage through bioprinting collagen type II hydrogel constructs with biomimetic chondrocyte density gradient , 2016, BMC Musculoskeletal Disorders.

[64]  Kevin W Eliceiri,et al.  Control of 3-dimensional collagen matrix polymerization for reproducible human mammary fibroblast cell culture in microfluidic devices. , 2009, Biomaterials.

[65]  Dong-Woo Cho,et al.  3D Cell Printed Tissue Analogues: A New Platform for Theranostics , 2017, Theranostics.

[66]  Wouter J A Dhert,et al.  3D bioprinting of methacrylated hyaluronic acid (MeHA) hydrogel with intrinsic osteogenicity , 2017, PloS one.

[67]  Dongxu Ke,et al.  Bioprinted trachea constructs with patient-matched design, mechanical and biological properties , 2019, Biofabrication.

[68]  Anders Lindahl,et al.  Chondrocytes and stem cells in 3D-bioprinted structures create human cartilage in vivo , 2017, PloS one.

[69]  Luca Gasperini,et al.  Natural polymers for the microencapsulation of cells , 2014, Journal of The Royal Society Interface.

[70]  Ali Khademhosseini,et al.  A perspective on the physical, mechanical and biological specifications of bioinks and the development of functional tissues in 3D bioprinting , 2018 .

[71]  Fumio Watari,et al.  3D-Printed Biopolymers for Tissue Engineering Application , 2014 .

[72]  Eneko Axpe,et al.  Applications of Alginate-Based Bioinks in 3D Bioprinting , 2016, International journal of molecular sciences.

[73]  Shay Soker,et al.  Optimization of collagen type I-hyaluronan hybrid bioink for 3D bioprinted liver microenvironments , 2018, Biofabrication.

[74]  Meng Yin,et al.  Tissue-engineered trachea from a 3D-printed scaffold enhances whole-segment tracheal repair , 2017, Scientific Reports.

[75]  Horst Kessler,et al.  RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. , 2003, Biomaterials.

[76]  Manish K Jaiswal,et al.  Bioactive nanoengineered hydrogels for bone tissue engineering: a growth-factor-free approach. , 2015, ACS nano.

[77]  Li Ren,et al.  Genipin-cross-linked collagen/chitosan biomimetic scaffolds for articular cartilage tissue engineering applications. , 2010, Journal of biomedical materials research. Part A.

[78]  L. Sherman,et al.  Emerging roles of hyaluronic acid bioscaffolds in tissue engineering and regenerative medicine. , 2016, International journal of biological macromolecules.

[79]  P. Gatenholm,et al.  3D Bioprinting of Human Chondrocyte-laden Nanocellulose Hydrogels for Patient-specific Auricular Cartilage Regeneration , 2016 .

[80]  Ruggero Bettini,et al.  3D-printed chitosan-based scaffolds: An in vitro study of human skin cell growth and an in-vivo wound healing evaluation in experimental diabetes in rats. , 2018, Carbohydrate polymers.

[81]  Xiaohong Wang,et al.  Advanced Polymers for Three-Dimensional (3D) Organ Bioprinting , 2019, Micromachines.

[82]  Rhiannon Batchelor,et al.  (−)-Riboflavin (vitamin B2) and flavin mononucleotide as visible light photo initiators in the thiol–ene polymerisation of PEG-based hydrogels , 2017 .

[83]  N. Ahmed,et al.  Recent applications of PLGA based nanostructures in drug delivery. , 2017, Colloids and surfaces. B, Biointerfaces.

[84]  Anthony Atala,et al.  A hydrogel bioink toolkit for mimicking native tissue biochemical and mechanical properties in bioprinted tissue constructs. , 2015, Acta biomaterialia.

[85]  D. Kelly,et al.  A comparison of different bioinks for 3D bioprinting of fibrocartilage and hyaline cartilage , 2016, Biofabrication.

[86]  Binil Starly,et al.  3D-Bioprinting of Polylactic Acid (PLA) Nanofiber-Alginate Hydrogel Bioink Containing Human Adipose-Derived Stem Cells. , 2016, ACS biomaterials science & engineering.

[87]  Ishita Matai,et al.  Progress in 3D bioprinting technology for tissue/organ regenerative engineering. , 2020, Biomaterials.

[88]  Juan de Vicente,et al.  Bio-inspired hydrogel composed of hyaluronic acid and alginate as a potential bioink for 3D bioprinting of articular cartilage engineering constructs. , 2020, Acta biomaterialia.

[89]  Yonggang Lv,et al.  Application of Collagen Scaffold in Tissue Engineering: Recent Advances and New Perspectives , 2016, Polymers.

[90]  D. Shreiber,et al.  A thermoreversible, photocrosslinkable collagen bio-ink for free-form fabrication of scaffolds for regenerative medicine. , 2017, Technology.

[91]  M. Raucci,et al.  Effects of Genipin Concentration on Cross-Linked Chitosan Scaffolds for Bone Tissue Engineering: Structural Characterization and Evidence of Biocompatibility Features , 2017 .

[92]  A. Khademhosseini,et al.  Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. , 2014, Lab on a chip.

[93]  M. Gong,et al.  Biodegradable shape-memory polymers using polycaprolactone and isosorbide based polyurethane blends. , 2018, Materials science & engineering. C, Materials for biological applications.

[94]  MyungGu Yeo,et al.  A cell-printing approach for obtaining hASC-laden scaffolds by using a collagen/polyphenol bioink , 2017, Biofabrication.

[95]  M. Taya,et al.  Gelatin/Hyaluronic Acid Content in Hydrogels Obtained through Blue Light-Induced Gelation Affects Hydrogel Properties and Adipose Stem Cell Behaviors , 2019, Biomolecules.

[96]  Lawrence J Bonassar,et al.  Correlating rheological properties and printability of collagen bioinks: the effects of riboflavin photocrosslinking and pH , 2017, Biofabrication.

[97]  Mohamed Al-Rubeai,et al.  Monitoring pH and dissolved oxygen in mammalian cell culture using optical sensors , 2008, Cytotechnology.

[98]  C. V. van Blitterswijk,et al.  Chitosan scaffolds containing hyaluronic acid for cartilage tissue engineering. , 2011, Tissue engineering. Part C, Methods.

[99]  Craig A. Simmons,et al.  Generating vascular channels within hydrogel constructs using an economical open-source 3D bioprinter and thermoreversible gels , 2018 .

[100]  Xiaohong Tian,et al.  Chitosans for Tissue Repair and Organ Three-Dimensional (3D) Bioprinting , 2019, Micromachines.

[101]  Xin Fu,et al.  Structurally and Functionally Optimized Silk‐Fibroin–Gelatin Scaffold Using 3D Printing to Repair Cartilage Injury In Vitro and In Vivo , 2017, Advanced materials.

[102]  Barry J Doyle,et al.  Characterisation of hyaluronic acid methylcellulose hydrogels for 3D bioprinting. , 2018, Journal of the mechanical behavior of biomedical materials.

[103]  Cynthia A. Reinhart-King,et al.  3D Bioprinting of Spatially Heterogeneous Collagen Constructs for Cartilage Tissue Engineering. , 2016, ACS biomaterials science & engineering.

[104]  A. Theocharis,et al.  Extracellular matrix structure. , 2016, Advanced drug delivery reviews.

[105]  A. Pohar,et al.  A reaction–diffusion kinetic model for the heterogeneous N-deacetylation step in chitin material conversion to chitosan in catalytic alkaline solutions , 2018 .