Tissue-engineered Vascular Grafts: Balance of the Four Major Requirements

Abstract Tissue-engineered vascular grafts (TEVGs) have emerged as a new choice for substitution of damaged blood vessels. A passage of a new blood vessel can be regenerated through the continuous secretion of extracellular matrix of cells seeded on the TEVGs, which is not possible using conventional vascular grafts. Although great progress has been made in TEVGs technology with advances in scaffold design and cell seeding, none have been applied in clinic hitherto. This review summarized the progress of TEVGs during the recent 7 years on the basis of four major requirements of TEVGs, namely, matched mechanical properties, blood compatibility, endothelium friendliness and biodegradability, in the hope of promoting the development of TEVGs.

[1]  Jeffrey T. Krawiec,et al.  Adult stem cell-based tissue engineered blood vessels: a review. , 2012, Biomaterials.

[2]  Gordon Minru Xiong,et al.  Endothelial cell thrombogenicity is reduced by ATRP-mediated grafting of gelatin onto PCL surfaces. , 2014, Journal of materials chemistry. B.

[3]  Min Zhang,et al.  Toward delivery of multiple growth factors in tissue engineering. , 2010, Biomaterials.

[4]  Jiehua Li,et al.  A novel strategy to graft RGD peptide on biomaterials surfaces for endothelization of small-diamater vascular grafts and tissue engineering blood vessel , 2008, Journal of materials science. Materials in medicine.

[5]  P. Nair,et al.  Tissue engineered vascular grafts--preclinical aspects. , 2013, International journal of cardiology.

[6]  Jun Zhang,et al.  Endothelialization and patency of RGD-functionalized vascular grafts in a rabbit carotid artery model. , 2012, Biomaterials.

[7]  A. G. Guex,et al.  Pericyte Seeded Dual Peptide Scaffold with Improved Endothelialization for Vascular Graft Tissue Engineering , 2016, Advanced healthcare materials.

[8]  E. Fortunati,et al.  Biodegradable polymer matrix nanocomposites for tissue engineering: A review , 2010 .

[9]  M. Radisic,et al.  Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis , 2016, Nature materials.

[10]  G. Ameer,et al.  Mechanocompatible Polymer‐Extracellular‐Matrix Composites for Vascular Tissue Engineering , 2016, Advanced healthcare materials.

[11]  Abdellah Ajji,et al.  Low thrombogenicity coating of nonwoven PET fiber structures for vascular grafts. , 2011, Macromolecular bioscience.

[12]  Hong Chen,et al.  Bioinspired Blood Compatible Surface Having Combined Fibrinolytic and Vascular Endothelium‐Like Properties via a Sequential Coimmobilization Strategy , 2015 .

[13]  A. Seifalian,et al.  Luminal surface engineering, 'micro and nanopatterning': potential for self endothelialising vascular grafts? , 2014, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[14]  Ali Khademhosseini,et al.  Electrospun scaffolds for tissue engineering of vascular grafts. , 2014, Acta biomaterialia.

[15]  Jeffrey A. Hubbell,et al.  Endothelial Cell-Selective Materials for Tissue Engineering in the Vascular Graft Via a New Receptor , 1991, Bio/Technology.

[16]  Jyothi U. Menon,et al.  Electrospun biodegradable elastic polyurethane scaffolds with dipyridamole release for small diameter vascular grafts. , 2014, Acta biomaterialia.

[17]  Changyou Gao,et al.  Complementary density gradient of Poly(hydroxyethyl methacrylate) and YIGSR selectively guides migration of endotheliocytes. , 2014, Biomacromolecules.

[18]  Lei Jiang,et al.  On improving blood compatibility: from bioinspired to synthetic design and fabrication of biointerfacial topography at micro/nano scales. , 2011, Colloids and Surfaces B: Biointerfaces.

[19]  Mathias Wilhelmi,et al.  Bioartificial fabrication of regenerating blood vessel substitutes: requirements and current strategies , 2014, Biomedizinische Technik. Biomedical engineering.

[20]  W Flameng,et al.  Improved endothelialization and reduced thrombosis by coating a synthetic vascular graft with fibronectin and stem cell homing factor SDF-1α. , 2012, Acta biomaterialia.

[21]  G. Njus,et al.  Material and structural characterization of human saphenous vein. , 1990, Journal of vascular surgery.

[22]  S. Kitamura,et al.  Study on the physical properties of tissue-engineered blood vessels made by chemical cross-linking and polymer-tissue cross-linking , 2009, Journal of Artificial Organs.

[23]  James J. Yoo,et al.  Bilayered scaffold for engineering cellularized blood vessels. , 2010, Biomaterials.

[24]  Marissa Nichole Rylander,et al.  The influence of electrospun scaffold topography on endothelial cell morphology, alignment, and adhesion in response to fluid flow , 2014, Biotechnology and bioengineering.

[25]  T. Ciach,et al.  Surface modification and endothelialization of polyurethane for vascular tissue engineering applications: a review. , 2016, Biomaterials science.

[26]  Xuejun Wen,et al.  Fabrication and characterization of permeable degradable poly(DL-lactide-co-glycolide) (PLGA) hollow fiber phase inversion membranes for use as nerve tract guidance channels. , 2006, Biomaterials.

[27]  Heungsoo Shin,et al.  Polydopamine-mediated immobilization of multiple bioactive molecules for the development of functional vascular graft materials. , 2012, Biomaterials.

[28]  C. Breuer,et al.  Vascular tissue engineering: the next generation. , 2012, Trends in molecular medicine.

[29]  David G Simpson,et al.  Suture-reinforced electrospun polydioxanone-elastin small-diameter tubes for use in vascular tissue engineering: a feasibility study. , 2008, Acta biomaterialia.

[30]  X. Mo,et al.  Fabrication of small-diameter vascular scaffolds by heparin-bonded P(LLA-CL) composite nanofibers to improve graft patency , 2013, International journal of nanomedicine.

[31]  J. Feijen,et al.  Tissue engineering of small-diameter vascular grafts: a literature review. , 2011, Clinical hemorheology and microcirculation.

[32]  Song Li,et al.  Antithrombogenic Modification of Small-Diameter Microfibrous Vascular Grafts , 2010, Arteriosclerosis, thrombosis, and vascular biology.

[33]  H. Bergmeister,et al.  Healing characteristics of electrospun polyurethane grafts with various porosities. , 2013, Acta biomaterialia.

[34]  David A. Vorp,et al.  A small diameter, fibrous vascular conduit generated from a poly(ester urethane)urea and phospholipid polymer blend. , 2009, Biomaterials.

[35]  M. Mozafari,et al.  Fabrication and characterization of electrospun poly-L-lactide/gelatin graded tubular scaffolds: Toward a new design for performance enhancement in vascular tissue engineering , 2015 .

[36]  A. Boccaccini,et al.  Vascular Tissue Engineering: Effects of Integrating Collagen into a PCL Based Nanofiber Material , 2017, BioMed research international.

[37]  Peter X Ma,et al.  Polymer Scaffolds for Small‐Diameter Vascular Tissue Engineering , 2010, Advanced functional materials.

[38]  Xuhui Huang,et al.  Controlling the Integration of Polyvinylpyrrolidone onto Substrate by Quartz Crystal Microbalance with Dissipation To Achieve Excellent Protein Resistance and Detoxification. , 2016, ACS applied materials & interfaces.

[39]  A. Seifalian,et al.  Small calibre polyhedral oligomeric silsesquioxane nanocomposite cardiovascular grafts: influence of porosity on the structure, haemocompatibility and mechanical properties. , 2011, Acta biomaterialia.

[40]  Y U Lee,et al.  3D‐Printed Biodegradable Polymeric Vascular Grafts , 2016, Advanced healthcare materials.

[41]  Hong Chen,et al.  A multifunctional surface for blood contact with fibrinolytic activity, ability to promote endothelial cell adhesion and inhibit smooth muscle cell adhesion. , 2017, Journal of materials chemistry. B.

[42]  V. Thomas,et al.  In vitro degradation and cell attachment studies of a new electrospun polymeric tubular graft , 2015, Progress in Biomaterials.

[43]  Lih-Sheng Turng,et al.  Approaches to Fabricating Multiple-Layered Vascular Scaffolds Using Hybrid Electrospinning and Thermally Induced Phase Separation Methods , 2016 .

[44]  Zhikai Tan,et al.  Composite vascular grafts with high cell infiltration by co-electrospinning. , 2016, Materials science & engineering. C, Materials for biological applications.

[45]  Wei Liu,et al.  Tissue engineering of blood vessel , 2007, Journal of cellular and molecular medicine.

[46]  D. Grijpma,et al.  Hollow fibers of poly(lactide-co-glycolide) and poly(ε-caprolactone) blends for vascular tissue engineering applications. , 2013, Acta biomaterialia.

[47]  Marcel C M Rutten,et al.  Dynamic straining combined with fibrin gel cell seeding improves strength of tissue-engineered small-diameter vascular grafts. , 2009, Tissue engineering. Part A.

[48]  J. Zhong,et al.  Electrospun vein grafts with high cell infiltration for vascular tissue engineering. , 2017, Materials science & engineering. C, Materials for biological applications.

[49]  D. Grijpma,et al.  Development and characterization of poly(ε-caprolactone) hollow fiber membranes for vascular tissue engineering , 2013 .

[50]  Shaobing Zhou,et al.  A Dynamically Tunable, Bioinspired Micropatterned Surface Regulates Vascular Endothelial and Smooth Muscle Cells Growth at Vascularization. , 2016, Small.

[51]  Wenjie Yuan,et al.  Co-electrospun blends of PU and PEG as potential biocompatible scaffolds for small-diameter vascular tissue engineering , 2012 .

[52]  Anthony Callanan,et al.  Fibrin: A Natural Biodegradable Scaffold in Vascular Tissue Engineering , 2008, Cells Tissues Organs.

[53]  Jingjing Huang,et al.  Zwitterionic monomer graft copolymerization onto polyurethane surface through a PEG spacer , 2010 .

[54]  Hong Chen,et al.  A hemocompatible polyurethane surface having dual fibrinolytic and nitric oxide generating functions. , 2017, Journal of materials chemistry. B.

[55]  Yubo Fan,et al.  Dual-delivery of VEGF and PDGF by double-layered electrospun membranes for blood vessel regeneration. , 2013, Biomaterials.

[56]  X. Mo,et al.  Heparin loading and pre-endothelialization in enhancing the patency rate of electrospun small-diameter vascular grafts in a canine model. , 2013, ACS applied materials & interfaces.

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

[58]  S. Soker,et al.  The use of thermal treatments to enhance the mechanical properties of electrospun poly(ɛ-caprolactone) scaffolds , 2008 .

[59]  Nan Ma,et al.  Surface modification and endothelialization of biomaterials as potential scaffolds for vascular tissue engineering applications. , 2015, Chemical Society reviews.

[60]  S. Burchielli,et al.  Long term performance of small-diameter vascular grafts made of a poly(ether)urethane-polydimethylsiloxane semi-interpenetrating polymeric network. , 2010, Biomaterials.

[61]  Guanglei Xiong,et al.  Current progress in 3D printing for cardiovascular tissue engineering , 2015, Biomedical materials.

[62]  Xiaohong Li,et al.  Engineering blood vessels through micropatterned co-culture of vascular endothelial and smooth muscle cells on bilayered electrospun fibrous mats with pDNA inoculation. , 2015, Acta biomaterialia.

[63]  M. Chan-Park,et al.  Biomaterials patterned with discontinuous microwalls for vascular smooth muscle cell culture: biodegradable small diameter vascular grafts and stable cell culture substrates , 2016, Journal of biomaterials science. Polymer edition.

[64]  Robert J Levy,et al.  Micropatterning of three-dimensional electrospun polyurethane vascular grafts. , 2010, Acta biomaterialia.

[65]  Heinrich Schima,et al.  Biodegradable, thermoplastic polyurethane grafts for small diameter vascular replacements. , 2015, Acta biomaterialia.

[66]  Gerhard Ziemer,et al.  Induction of EPC homing on biofunctionalized vascular grafts for rapid in vivo self-endothelialization--a review of current strategies. , 2010, Biotechnology advances.

[67]  Changyou Gao,et al.  Preparation of an Arg-Glu-Asp-Val Peptide Density Gradient on Hyaluronic Acid-Coated Poly(ε-caprolactone) Film and Its Influence on the Selective Adhesion and Directional Migration of Endothelial Cells. , 2016, ACS applied materials & interfaces.

[68]  Su A Park,et al.  Characterization and preparation of bio-tubular scaffolds for fabricating artificial vascular grafts by combining electrospinning and a 3D printing system. , 2015, Physical chemistry chemical physics : PCCP.

[69]  A. Melchiorri,et al.  Development and assessment of a biodegradable solvent cast polyester fabric small-diameter vascular graft. , 2014, Journal of biomedical materials research. Part A.

[70]  Jian Yu,et al.  The effect of stromal cell-derived factor-1α/heparin coating of biodegradable vascular grafts on the recruitment of both endothelial and smooth muscle progenitor cells for accelerated regeneration. , 2012, Biomaterials.

[71]  M. Ashkezari,et al.  Coating of Polyurethane Scaffold With Arabinogalactan Leads to Increase of Adhesion to Fibroblast Cells by Integrin Molecules Pathway , 2018 .

[72]  Jan P Stegemann,et al.  Review: advances in vascular tissue engineering using protein-based biomaterials. , 2007, Tissue engineering.

[73]  Ángel E. Mercado-Pagán,et al.  Development and evaluation of elastomeric hollow fiber membranes as small diameter vascular graft substitutes. , 2015, Materials science & engineering. C, Materials for biological applications.

[74]  Hadi Hajiali,et al.  Electrospun PGA/gelatin nanofibrous scaffolds and their potential application in vascular tissue engineering , 2011, International journal of nanomedicine.

[75]  Gavriil Tsechpenakis,et al.  bFGF-containing electrospun gelatin scaffolds with controlled nano-architectural features for directed angiogenesis. , 2012, Acta biomaterialia.

[76]  Wei Zhao,et al.  Gradient nanofibrous chitosan/poly ɛ-caprolactone scaffolds as extracellular microenvironments for vascular tissue engineering. , 2012, Biomaterials.

[77]  Ryan A. Hoshi,et al.  The blood and vascular cell compatibility of heparin-modified ePTFE vascular grafts. , 2013, Biomaterials.

[78]  T. Leichtweiss,et al.  Development of thrombus-resistant and cell compatible crimped polyethylene terephthalate cardiovascular grafts using surface co-immobilized heparin and collagen. , 2014, Materials science & engineering. C, Materials for biological applications.

[79]  D. Stamatialis,et al.  Polymeric hollow fiber membranes for bioartificial organs and tissue engineering applications , 2014 .

[80]  Yi Hong,et al.  A bilayered elastomeric scaffold for tissue engineering of small diameter vascular grafts. , 2010, Acta biomaterialia.

[81]  Qiang Zhao,et al.  The effect of thick fibers and large pores of electrospun poly(ε-caprolactone) vascular grafts on macrophage polarization and arterial regeneration. , 2014, Biomaterials.

[82]  E. Benrashid,et al.  Tissue engineered vascular grafts: Origins, development, and current strategies for clinical application. , 2016, Methods.

[83]  Yafei Luan,et al.  An antithrombotic hydrogel with thrombin-responsive fibrinolytic activity: breaking down the clot as it forms , 2016 .

[84]  R. Gurny,et al.  Advantages of bilayered vascular grafts for surgical applicability and tissue regeneration. , 2012, Acta biomaterialia.

[85]  Anthony S Weiss,et al.  Elastomers in vascular tissue engineering. , 2016, Current opinion in biotechnology.

[86]  H. Bergmeister,et al.  Hard‐block degradable thermoplastic urethane‐elastomers for electrospun vascular prostheses , 2012 .

[87]  Y. Tabata,et al.  Enhanced angiogenesis by multiple release of platelet-rich plasma contents and basic fibroblast growth factor from gelatin hydrogels. , 2012, Acta biomaterialia.

[88]  B. C. Ng,et al.  Hemocompatibility evaluation of poly(1,8-octanediol citrate) blend polyethersulfone membranes. , 2017, Journal of biomedical materials research. Part A.

[89]  Abdalla Abdal-hay,et al.  Electrospun biphasic tubular scaffold with enhanced mechanical properties for vascular tissue engineering. , 2018, Materials science & engineering. C, Materials for biological applications.

[90]  Alexander M. Seifalian,et al.  Surface Modification of Biomaterials: A Quest for Blood Compatibility , 2012, International journal of biomaterials.

[91]  Chong Cheng,et al.  Progress in heparin and heparin-like/mimicking polymer-functionalized biomedical membranes. , 2014, Journal of materials chemistry. B.

[92]  Enrica Briganti,et al.  A composite fibrin-based scaffold for controlled delivery of bioactive pro-angiogenetic growth factors. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[93]  Heungsoo Shin,et al.  Mussel-inspired immobilization of vascular endothelial growth factor (VEGF) for enhanced endothelialization of vascular grafts. , 2012, Biomacromolecules.

[94]  Hong Chen,et al.  Blood compatible materials: state of the art. , 2014, Journal of materials chemistry. B.

[95]  Alina Sionkowska,et al.  Current research on the blends of natural and synthetic polymers as new biomaterials: Review , 2011 .

[96]  M. Tabrizian,et al.  Characterization and biocompatibility studies of new degradable poly(urea)urethanes prepared with arginine, glycine or aspartic acid as chain extenders , 2013, Journal of Materials Science: Materials in Medicine.

[97]  Steven G Wise,et al.  A multilayered synthetic human elastin/polycaprolactone hybrid vascular graft with tailored mechanical properties. , 2011, Acta biomaterialia.

[98]  D. Stamatialis,et al.  Development of poly(l-lactic acid) hollow fiber membranes for artificial vasculature in tissue engineering scaffolds , 2011 .

[99]  Kai Wang,et al.  Effect of sustained heparin release from PCL/chitosan hybrid small-diameter vascular grafts on anti-thrombogenic property and endothelialization. , 2014, Acta biomaterialia.

[100]  Doris Klee,et al.  Polymers for Biomedical Applications: Improvement of the Interface Compatibility , 2000 .

[101]  Robert Langer,et al.  A decade of progress in tissue engineering , 2016, Nature Protocols.

[102]  Xiabin Jing,et al.  Biodegradable synthetic polymers: Preparation, functionalization and biomedical application , 2012 .

[103]  Narutoshi Hibino,et al.  Vascular tissue engineering: towards the next generation vascular grafts. , 2011, Advanced drug delivery reviews.

[104]  Aijun Wang,et al.  Engineering the mechanical and biological properties of nanofibrous vascular grafts for in situ vascular tissue engineering , 2017, Biofabrication.

[105]  M. Abedalwafa,et al.  BIODEGRADABLE POLY-EPSILON-CAPROLACTONE (PCL) FOR TISSUE ENGINEERING APPLICATIONS: A REVIEW , 2012 .