Bioprinting of artificial blood vessels: current approaches towards a demanding goal.

Free-form fabrication techniques, often referred to as '3D printing', are currently tested with regard to the processing of biological and biocompatible materials in general and for fabrication of vessel-like structures in particular. Such computer-controlled methods assemble 3D objects by layer-wise deposition or layer-wise cross-linking of materials. They use, for example, nozzle-based deposition of hydrogels and cells, drop-on-demand inkjet-printing of cell suspensions with subsequent cross-linking, layer-by-layer cross-linking of synthetic or biological polymers by selective irradiation with light and even laser-induced deposition of single cells. The need of vessel-like structures has become increasingly crucial for the supply of encapsulated cells for 3D tissue engineering, or even with regard to future application such as vascular grafts. The anticipated potential of providing tubes with tailored branching geometries made of biocompatible or biological materials pushes future visions of patient-specific vascularized tissue substitutions, tissue-engineered blood vessels and bio-based vascular grafts. We review here the early attempts of bringing together innovative free-form manufacturing processes with bio-based and biodegradable materials. The presented studies provide many important proofs of concepts such as the possibility to integrate viable cells into computer-controlled processes and the feasibility of supplying cells in a hydrogel matrix by generation of a network of perfused channels. Several impressive results in the generation of complex shapes and high-aspect-ratio tubular structures demonstrate the potential of additive assembly methods. Yet, it also becomes obvious that there remain major challenges to simultaneously match all material requirements in terms of biological functions (cell function supporting properties), physicochemical functions (mechanical properties of the printed material) and process-related (viscosity, cross-linkability) functions, towards the demanding goal of biofabricating artificial blood vessels.

[1]  Michael Wegener,et al.  Soft Polymers for Building up Small and Smallest Blood Supplying Systems by Stereolithography , 2012, Journal of functional biomaterials.

[2]  Esther Novosel,et al.  Vascularization is the key challenge in tissue engineering. , 2011, Advanced drug delivery reviews.

[3]  Anja Lode,et al.  Direct Plotting of Three‐Dimensional Hollow Fiber Scaffolds Based on Concentrated Alginate Pastes for Tissue Engineering , 2013, Advanced healthcare materials.

[4]  Zhang Ji,et al.  C57BL/6および129SvEvマウス間の大動脈弓形状,血行動態,プラークパッターンの相異 | 文献情報 | J-GLOBAL 科学技術総合リンクセンター , 2009 .

[5]  S. Bryant,et al.  Cell encapsulation in biodegradable hydrogels for tissue engineering applications. , 2008, Tissue engineering. Part B, Reviews.

[6]  Angela Panoskaltsis-Mortari,et al.  Development of a decellularized lung bioreactor system for bioengineering the lung: the matrix reloaded. , 2010, Tissue engineering. Part A.

[7]  Makoto Nakamura,et al.  Development of a three-dimensional bioprinter: construction of cell supporting structures using hydrogel and state-of-the-art inkjet technology. , 2009, Journal of biomechanical engineering.

[8]  Jos Malda,et al.  Extracellular matrix scaffolds for cartilage and bone regeneration. , 2013, Trends in biotechnology.

[9]  Y. Seo,et al.  Tissue engineered artificial skin composed of dermis and epidermis. , 2000, Artificial organs.

[10]  Karoly Jakab,et al.  Tissue engineering by self-assembly and bio-printing of living cells , 2010, Biofabrication.

[11]  M Nakamura,et al.  Biomatrices and biomaterials for future developments of bioprinting and biofabrication , 2010, Biofabrication.

[12]  Stefan Baudis,et al.  Elastomeric degradable biomaterials by photopolymerization-based CAD-CAM for vascular tissue engineering , 2011, Biomedical materials.

[13]  H. Walles,et al.  Upcyte® microvascular endothelial cells repopulate decellularized scaffold. , 2013, Tissue engineering. Part C, Methods.

[14]  Antonios G. Mikos,et al.  Formation of highly porous biodegradable scaffolds for tissue engineering , 2000 .

[15]  J. Lewis,et al.  Omnidirectional Printing of 3D Microvascular Networks , 2011, Advanced materials.

[16]  Jason R. Thonhoff,et al.  Compatibility of human fetal neural stem cells with hydrogel biomaterials in vitro , 2008, Brain Research.

[17]  Makoto Nakamura,et al.  Ink Jet Three-Dimensional Digital Fabrication for Biological Tissue Manufacturing: Analysis of Alginate Microgel Beads Produced by Ink Jet Droplets for Three Dimensional Tissue Fabrication , 2008 .

[18]  Laxminarayanan Krishnan,et al.  Integrative Physiology/Experimental Medicine Determinants of Microvascular Network Topologies in Implanted Neovasculatures , 2011 .

[19]  T. Boland,et al.  Human microvasculature fabrication using thermal inkjet printing technology. , 2009, Biomaterials.

[20]  J. Izquierdo,et al.  Plant biotechnology and food security in Latin America and the Caribbean , 2000 .

[21]  J. Vacanti,et al.  Tissue engineering : Frontiers in biotechnology , 1993 .

[22]  Joe Tien,et al.  Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. , 2007, Lab on a chip.

[23]  Lorna J. Gibson,et al.  Cellular materials as porous scaffolds for tissue engineering , 2001 .

[24]  Wan-Ju Li,et al.  Cartilage tissue engineering: its potential and uses , 2006, Current opinion in rheumatology.

[25]  John G. Collard,et al.  Temporal and Spatial Modulation of Rho GTPases during in Vitro Formation of Capillary Vascular Network , 2003, Journal of Biological Chemistry.

[26]  Arnold Gillner,et al.  Fabrication of 2D protein microstructures and 3D polymer–protein hybrid microstructures by two-photon polymerization , 2011, Biofabrication.

[27]  Jason P. Gleghorn,et al.  Microfluidic scaffolds for tissue engineering. , 2007, Nature materials.

[28]  Ibrahim T. Ozbolat,et al.  Characterization of printable cellular micro-fluidic channels for tissue engineering , 2013, Biofabrication.

[29]  Alexander M Seifalian,et al.  The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review. , 2005, Biomaterials.

[30]  F. Guillemot,et al.  Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. , 2010, Biomaterials.

[31]  Yongnian Yan,et al.  Direct Fabrication of a Hybrid Cell/Hydrogel Construct by a Double-nozzle Assembling Technology: , 2009 .

[32]  E. Piek,et al.  Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. , 2003, Developmental biology.

[33]  H. Fischer,et al.  Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid , 2012, Biofabrication.

[34]  L. Grover,et al.  Cell encapsulation using biopolymer gels for regenerative medicine , 2010, Biotechnology Letters.

[35]  Thomas Hirth,et al.  Evaluation of Cell‐Material Interactions on Newly Designed, Printable Polymers for Tissue Engineering Applications , 2011 .

[36]  Stuart K Williams,et al.  Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. , 2011, Journal of biomedical materials research. Part B, Applied biomaterials.

[37]  A. Mikos,et al.  Review: tissue engineering for regeneration of articular cartilage. , 2000, Biomaterials.

[38]  Tao Xu,et al.  Layer-by-layer printing of cells and its application to tissue engineering , 2004 .

[39]  P. Olinga,et al.  Organ slices as an in vitro test system for drug metabolism in human liver, lung and kidney. , 1999, Toxicology in vitro : an international journal published in association with BIBRA.

[40]  Yu-Hsiang Hsu,et al.  In vitro perfused human capillary networks. , 2013, Tissue engineering. Part C, Methods.

[41]  G. Prestwich,et al.  Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting. , 2010, Tissue engineering. Part A.

[42]  Sangeeta N Bhatia,et al.  Three-dimensional tissue fabrication. , 2004, Advanced drug delivery reviews.

[43]  T Togawa,et al.  Optimal branching structure of the vascular tree. , 1972, The Bulletin of mathematical biophysics.

[44]  G. Prestwich,et al.  Dynamically Crosslinked Gold Nanoparticle – Hyaluronan Hydrogels , 2010, Advanced materials.

[45]  R. Schulz,et al.  Cartilage tissue engineering and bioreactor systems for the cultivation and stimulation of chondrocytes , 2007, European Biophysics Journal.

[46]  J. Hoying,et al.  Angiogenic Potential of Microvessel Fragments is Independent of the Tissue of Origin and can be Influenced by the Cellular Composition of the Implants , 2010, Microcirculation.

[47]  Vladimir Mironov,et al.  Bioprinting is coming of age: report from the International Conference on Bioprinting and Biofabrication in Bordeaux (3B'09) , 2010, Biofabrication.

[48]  M. Nakamura,et al.  3D Micro-fabrication by Inkjet 3D biofabrication for 3D tissue engineering , 2008, 2008 International Symposium on Micro-NanoMechatronics and Human Science.

[49]  J. Lannutti,et al.  Electrospinning for tissue engineering scaffolds , 2007 .

[50]  Allan S Hoffman,et al.  Hydrogels for biomedical applications. , 2002, Advanced drug delivery reviews.

[51]  Lucie Germain,et al.  Inosculation of Tissue‐Engineered Capillaries with the Host's Vasculature in a Reconstructed Skin Transplanted on Mice , 2005, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[52]  R. Markwald,et al.  Scaffold‐free inkjet printing of three‐dimensional zigzag cellular tubes , 2012, Biotechnology and bioengineering.

[53]  Bahattin Koc,et al.  3D Hybrid Bioprinting of Macrovascular Structures , 2013 .

[54]  Glenn D Prestwich,et al.  Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. , 2010, Biomaterials.

[55]  J. Malda,et al.  Biofabrication of multi-material anatomically shaped tissue constructs , 2013, Biofabrication.

[56]  A. Khademhosseini,et al.  A cell-laden microfluidic hydrogel. , 2007, Lab on a chip.

[57]  Ibrahim T. Ozbolat,et al.  Direct Bioprinting of Vessel-Like Tubular Microfluidic Channels , 2013 .

[58]  Brendon M. Baker,et al.  Rapid casting of patterned vascular networks for perfusable engineered 3D tissues , 2012, Nature materials.

[59]  Ibrahim T. Ozbolat,et al.  Evaluation of cell viability and functionality in vessel-like bioprintable cell-laden tubular channels. , 2013, Journal of biomechanical engineering.

[60]  S. Yoo,et al.  On‐demand three‐dimensional freeform fabrication of multi‐layered hydrogel scaffold with fluidic channels , 2010, Biotechnology and bioengineering.

[61]  L. Niklason,et al.  Scaffold-free vascular tissue engineering using bioprinting. , 2009, Biomaterials.

[62]  Doris A Taylor,et al.  Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart , 2008, Nature Medicine.

[63]  Makarand V Risbud,et al.  Tissue engineering: advances in in vitro cartilage generation. , 2002, Trends in biotechnology.

[64]  Y. Sakai,et al.  Soluble Factor–DependentIn VitroGrowth and Maturation of Rat Fetal Liver Cells in a Three-Dimensional Culture System , 2008 .

[65]  Susan C. Roberts,et al.  Pluronic F127 as a cell encapsulation material: utilization of membrane-stabilizing agents. , 2005, Tissue engineering.

[66]  Robert Langer,et al.  A 3D Interconnected Microchannel Network Formed in Gelatin by Sacrificial Shellac Microfibers , 2012, Advanced materials.

[67]  S. Hofmann,et al.  Controlled Positioning of Cells in Biomaterials—Approaches Towards 3D Tissue Printing , 2011, Journal of functional biomaterials.

[68]  Karl R Edminster,et al.  Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. , 2009, Biomaterials.

[69]  E. Sachlos,et al.  Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. , 2003, European cells & materials.

[70]  Robert Liska,et al.  Evaluation of Biocompatible Photopolymers I: Photoreactivity and Mechanical Properties of Reactive Diluents , 2007 .

[71]  In Vivo study of a blended hydrogel composed of pluronic F-127-alginate-hyaluronic acid for its cell injection application , 2012, Tissue Engineering and Regenerative Medicine.

[72]  H. Augustin,et al.  Blood vessel maturation in a 3‐dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[73]  B R Ringeisen,et al.  Development of human umbilical vein endothelial cell (HUVEC) and human umbilical vein smooth muscle cell (HUVSMC) branch/stem structures on hydrogel layers via biological laser printing (BioLP) , 2010, Biofabrication.

[74]  P. Bártolo,et al.  Additive manufacturing of tissues and organs , 2012 .

[75]  Hiroshi Yagi,et al.  Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix , 2010, Nature Medicine.

[76]  F. Prósper,et al.  Strategies of human corneal endothelial tissue regeneration. , 2013, Regenerative medicine.

[77]  T. Hirth,et al.  Chemical tailoring of gelatin to adjust its chemical and physical properties for functional bioprinting. , 2013, Journal of materials chemistry. B.