Tissue-Engineered Blood Vessels: Alternative to Autologous Grafts?

Although vascular bypass grafting remains the mainstay for revascularization for ischemic heart disease and peripheral vascular disease, many patients do not have healthy vessels suitable for harvest. Thus, prosthetic grafts made of synthetic polymers were developed, but their use is limited to high-flow/low-resistance conditions because of poor elasticity, low compliance, and thrombogenicity of their synthetic surfaces. To fill this need, several laboratories have produced in vivo or in vitro tissue-engineered blood vessels using molds or prosthetic or biodegradable scaffolds, but each artificial graft has significant problems. Recently, conduits have been grown in the peritoneal cavity of the same animals in which they will be grafted, ensuring no rejection, in the short time of 2 to 3 weeks. Remodeling occurs after grafting such that the tissue is almost indistinguishable from native vessels. This conduit is derived from cells of bone marrow origin, opening new possibilities in vascular modeling and remodeling.

[1]  F. Crawford,et al.  Human internal mammary artery produces more prostacyclin than saphenous vein. , 1986, The Journal of thoracic and cardiovascular surgery.

[2]  A. Seifalian,et al.  Performance of a polyurethane vascular prosthesis carrying a dipyridamole (Persantin) coating on its lumenal surface , 2001 .

[3]  P. Hagen,et al.  Remodeling of an acellular collagen graft into a physiologically responsive neovessel , 1999, Nature Biotechnology.

[4]  Alexander M Seifalian,et al.  In vivo biostability of a poly(carbonate-urea)urethane graft. , 2003, Biomaterials.

[5]  T. Matsuda,et al.  Canine endothelial progenitor cell-lined hybrid vascular graft with nonthrombogenic potential. , 2003, The Journal of thoracic and cardiovascular surgery.

[6]  Frederick J Schoen,et al.  Cardiovascular tissue engineering. , 2002, Cardiovascular pathology : the official journal of the Society for Cardiovascular Pathology.

[7]  B. Sumpio,et al.  Effects of cyclic strain on vascular cells. , 2004, Endothelium : journal of endothelial cell research.

[8]  W. Schaper,et al.  Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. , 1998, The Journal of clinical investigation.

[9]  G. Hamilton,et al.  Engineering of bypass conduits to improve patency , 2004, Cell proliferation.

[10]  A Haverich,et al.  Engineering of human vascular aortic tissue based on a xenogeneic starter matrix. , 2000, Transplantation.

[11]  R Langer,et al.  Morphologic and mechanical characteristics of engineered bovine arteries. , 2001, Journal of vascular surgery.

[12]  G. Spangrude,et al.  Chimerism of the transplanted heart. , 2002, The New England journal of medicine.

[13]  Athanassios Sambanis,et al.  A biological hybrid model for collagen-based tissue engineered vascular constructs. , 2003, Biomaterials.

[14]  S. Verma,et al.  Should radial arteries be used routinely for coronary artery bypass grafting? , 2004, Circulation.

[15]  R. C. Thomson,et al.  Improvements in GORE-TEX 1 Vascular Graft Performance by Carmeda 1 BioActive Surface Heparin Immobilization , 2012 .

[16]  A. Remuzzi,et al.  Vascular smooth muscle cells on hyaluronic acid: culture and mechanical characterization of an engineered vascular construct. , 2004, Tissue engineering.

[17]  G. Abatangelo,et al.  Functions of hyaluronan in wound repair , 1999, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[18]  J. Campbell,et al.  Culture techniques and their applications to studies of vascular smooth muscle. , 1993, Clinical science.

[19]  A Haverich,et al.  Improved endothelial cell attachment on ePTFE vascular grafts pretreated with synthetic RGD-containing peptides. , 1996, European Journal of Vascular and Endovascular Surgery.

[20]  Laura E Niklason,et al.  Human arteries engineered in vitro , 2003, EMBO reports.

[21]  David J. Mooney,et al.  Cyclic mechanical strain regulates the development of engineered smooth muscle tissue , 1999, Nature Biotechnology.

[22]  A. Carpentier,et al.  The aorta-to-coronary radial artery bypass graft. A technique avoiding pathological changes in grafts. , 1973, The Annals of thoracic surgery.

[23]  T. Matsuda,et al.  Self-organized, tubular hybrid vascular tissue composed of vascular cells and collagen for low-pressure-loaded venous system. , 1995, Cell transplantation.

[24]  R. Tranquillo,et al.  Mechanisms of stiffening and strengthening in media-equivalents fabricated using glycation. , 2000, Journal of biomechanical engineering.

[25]  L A Geddes,et al.  Small intestinal submucosa as a vascular graft: a review. , 1993, Journal of investigative surgery : the official journal of the Academy of Surgical Research.

[26]  H. Mertsching,et al.  Influence of scaffold thickness and scaffold composition on bioartificial graft survival. , 2003, Biomaterials.

[27]  P. E. McHugh,et al.  Bioreactors for Cardiovascular Cell and Tissue Growth: A Review , 2003, Annals of Biomedical Engineering.

[28]  W. Konertz,et al.  Clinical experience with autologous endothelial cell-seeded polytetrafluoroethylene coronary artery bypass grafts. , 2000, The Journal of thoracic and cardiovascular surgery.

[29]  M. Makuuchi,et al.  Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis , 2002, Nature Medicine.

[30]  H. Greisler,et al.  Biomaterial pretreatment with ECGF to augment endothelial cell proliferation. , 1987, Journal of vascular surgery.

[31]  K. Kent,et al.  Optimal seeding conditions for human endothelial cells , 1992, Annals of vascular surgery.

[32]  T. Matsuda,et al.  Arterial replacement with compliant hierarchic hybrid vascular graft: biomechanical adaptation and failure. , 2002, Tissue engineering.

[33]  S. Badylak,et al.  Healing comparison of small intestine submucosa and ePTFE grafts in the canine carotid artery. , 1995, The Journal of surgical research.

[34]  R. Ross.  The pathogenesis of atherosclerosis: a perspective for the 1990s , 1993, Nature.

[35]  T. Fabian,et al.  Small Intestinal Submucosa for Vascular Reconstruction in the Presence of Gastrointestinal Contamination , 2004, Annals of surgery.

[36]  F A Auger,et al.  A completely biological tissue‐engineered human blood vessel , 1998, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[37]  N. Woolf,et al.  Effects of autologous mesothelial cell seeding on prostacyclin production within Dacron® arterial prostheses , 1988, The British journal of surgery.

[38]  M. Dake,et al.  In vivo vascular engineering: directed migration of smooth muscle cells to limit neointima. , 2002, Tissue engineering.

[39]  E. Huberman,et al.  A human peripheral blood monocyte-derived subset acts as pluripotent stem cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  K Schindhelm,et al.  A novel textured surface for blood-contact. , 1999, Biomaterials.

[41]  M. Yenidunya,et al.  Experimental vascular graft using small-caliber fascia-wrapped fibrocollagenous tube: short-term evaluation. , 1999, Journal of reconstructive microsurgery.

[42]  V I Kolessov,et al.  Mammary artery-coronary artery anastomosis as method of treatment for angina pectoris. , 1967, The Journal of thoracic and cardiovascular surgery.

[43]  L A Geddes,et al.  Mechanical remodeling of small-intestine submucosa small-diameter vascular grafts--a preliminary report. , 2001, Biomedical instrumentation & technology.

[44]  Alexander M Seifalian,et al.  Shear‐stress preconditioning and tissue‐engineering‐based paradigms for generating arterial substitutes , 2004, Biotechnology and applied biochemistry.

[45]  Julie H. Campbell,et al.  Dog peritoneal and pleural cavities as bioreactors to grow autologous vascular grafts. , 2004, Journal of vascular surgery.

[46]  J. Collin,et al.  Prosthetic vascular graft infection , 1992, The British journal of surgery.

[47]  Christie M. Orschell,et al.  Peripheral Blood “Endothelial Progenitor Cells” Are Derived From Monocyte/Macrophages and Secrete Angiogenic Growth Factors , 2003, Circulation.

[48]  R. Nerem,et al.  Endothelial cell monolayer formation: effect of substrate and fluid shear stress. , 2004, Endothelium : journal of endothelial cell research.

[49]  J. Glover,et al.  Endothelial seeding of polytetrafluoroethylene femoral popliteal bypasses: the failure of low-density seeding to improve patency. , 1994, Journal of vascular surgery.

[50]  T. Matsuda,et al.  Fabrication of Compliant Hybrid Grafts Supported with Elastomeric Meshes , 1999, Cell transplantation.

[51]  K. Kent,et al.  What is the proper role of polytetrafluoroethylene grafts in infrainguinal reconstruction? , 1989, Journal of vascular surgery.

[52]  W. Schaper,et al.  Blood monocyte concentration is critical for enhancement of collateral artery growth. , 2002, American journal of physiology. Heart and circulatory physiology.

[53]  K. Ishihara,et al.  Small diameter vascular prosthesis with a nonthrombogenic phospholipid polymer surface: preliminary study of a new concept for functioning in the absence of pseudo- or neointima formation. , 2000, Artificial organs.

[54]  Katja Schenke-Layland,et al.  Tissue engineering of aortic tissue: dire consequence of suboptimal elastic fiber synthesis in vivo. , 2004, Cardiovascular research.

[55]  O. Ohta,et al.  Development of vasa vasorum in the arterially implanted autovein bypass graft and its anastomosis in the dog. , 1997, International angiology : a journal of the International Union of Angiology.

[56]  R. Bucala,et al.  Peripheral Blood Fibrocytes: Differentiation Pathway and Migration to Wound Sites1 , 2001, The Journal of Immunology.

[57]  M Komeda,et al.  A new acellular vascular prosthesis as a scaffold for host tissue regeneration. , 2003, The International journal of artificial organs.

[58]  S. Sparks,et al.  Small-caliber Mesothelial Cell–layered Polytetraflouroethylene Vascular Grafts in New Zealand White Rabbits , 2002, Annals of vascular surgery.

[59]  U. Losert,et al.  Organisation of experimental thrombosis by blood cells , 1985, Virchows Archiv A.

[60]  Yasuko Tomizawa,et al.  Autocrine angiogenic vascular prosthesis with bone marrow transplantation , 1996, Nature Medicine.

[61]  N. Delépine,et al.  Possible monocytic origin of chondrosarcoma: in vitro transdifferentiation of HLA-DR blood monocyte-like cells from a patient with chondrosarcoma, into neo-fibroblasts and chondrocyte-like cells. , 1997, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[62]  D. J. Dempsey,et al.  Covalent linkage of recombinant hirudin to a novel ionic poly(carbonate) urethane polymer with protein binding sites: determination of surface antithrombin activity. , 1998, Artificial organs.

[63]  P. Zilla,et al.  Clinical autologous in vitro endothelialization of infrainguinal ePTFE grafts in 100 patients: a 9-year experience. , 1999, Surgery.

[64]  R. Mulligan,et al.  Genetic interventions for vein bypass graft disease: a review. , 2002, Journal of vascular surgery.

[65]  S Glagov,et al.  Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. , 2003, Science.

[66]  S. Hanson,et al.  In vitro endothelialization of small-caliber vascular grafts. , 1987, Surgery.

[67]  H. Schaff,et al.  Frequency of early occlusion and stenosis in a left internal mammary artery to left anterior descending artery bypass graft after surgery through a median sternotomy on conventional bypass: benchmark for minimally invasive direct coronary artery bypass. , 1999, Circulation.

[68]  T. Matsuda,et al.  A hybrid vascular model biomimicking the hierarchic structure of arterial wall: neointimal stability and neoarterial regeneration process under arterial circulation. , 1995, The Journal of thoracic and cardiovascular surgery.

[69]  H. Greisler,et al.  Kinetics of cell proliferation as a function of vascular graft material. , 1993, Journal of biomedical materials research.

[70]  H. Greisler.  Interactions at the blood/material interface , 1990, Annals of vascular surgery.

[71]  Julie H. Campbell,et al.  Haemopoietic Origin of Myofibroblasts Formed in the Peritoneal Cavity in Response to a Foreign Body , 2000, Journal of Vascular Research.

[72]  A. Seifalian,et al.  Effect of prolonged pulsatile shear stress in vitro on endothelial cell seeded PTFE and compliant polyurethane vascular grafts. , 1998, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[73]  M A Moses,et al.  Tissue engineering of autologous aorta using a new biodegradable polymer. , 1999, The Annals of thoracic surgery.

[74]  G. Campbell,et al.  ORIGIN OF MYOFIBROBLASTS IN THE AVASCULAR CAPSULE AROUND FREE‐FLOATING INTRAPERITONEAL BLOOD CLOTS , 1983, Pathology.

[75]  N. Caplice,et al.  Smooth Muscle Progenitor Cells in Human Blood , 2002, Circulation.

[76]  J C Stanley,et al.  Small-caliber polyurethane and polytetrafluoroethylene grafts: a comparative study in a canine aortoiliac model. , 1990, Journal of biomedical materials research.

[77]  Julie H. Campbell,et al.  Macrophages, myofibroblasts and neointimal hyperplasia after coronary artery injury and repair. , 2002, Atherosclerosis.

[78]  S. Schmidt,et al.  Endothelial cell--seeded four-millimeter Dacron vascular grafts: effects of blood flow manipulation through the grafts. , 1984, Journal of vascular surgery.

[79]  Julie H. Campbell,et al.  Neointimal Formation by Circulating Bone Marrow Cells , 2001, Annals of the New York Academy of Sciences.

[80]  Ling-Bo Sun,et al.  Pretreatment of a Dacron Graft with Tissue Factor Pathway Inhibitor Decreases Thrombogenicity and Neointimal Thickness: A Preliminary Animal Study , 2001, ASAIO journal.

[81]  R. James,et al.  Attachment of indium‐111 labelled endothelial cells to pretreated polytetrafluoroethylene vascular grafts , 1989, The British journal of surgery.

[82]  R. Favaloro,et al.  Saphenous vein graft in the surgical treatment of coronary artery disease. Operative technique. , 1969, The Journal of thoracic and cardiovascular surgery.

[83]  J. Feijen,et al.  Current Techniques to Improve the Blood Compatibility of Biomaterial Surfaces , 1991, The International journal of artificial organs.

[84]  S. Dimmeler,et al.  Endothelial Progenitor Cells: Characterization and Role in Vascular Biology , 2004, Circulation research.

[85]  E Bell,et al.  A blood vessel model constructed from collagen and cultured vascular cells. , 1986, Science.

[86]  M S Conte,et al.  The ideal small arterial substitute: a search for the Holy Grail? , 1998, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[87]  T. Matsuda,et al.  Reconstruction of a hybrid vascular graft hierarchically layered with three cell types. , 1994, ASAIO journal.

[88]  Robert M. Nerem,et al.  The Role of Matrix Metalloproteinase-2 in the Remodeling of Cell-Seeded Vascular Constructs Subjected to Cyclic Strain , 2001, Annals of Biomedical Engineering.

[89]  J. Sixma,et al.  Thrombomodulin activity on mesothelial cells: perspectives for mesothelial cells as an alternative for endothelial cells for cell seeding on vascular grafts , 1996, British journal of haematology.

[90]  F. C. Lucibello,et al.  Endothelial-like cells derived from human CD14 positive monocytes. , 2000, Differentiation; research in biological diversity.

[91]  D. Mooradian,et al.  Manipulation of remodeling pathways to enhance the mechanical properties of a tissue engineered blood vessel. , 2002, Journal of biomechanical engineering.

[92]  C H Sparks,et al.  Autogenous grafts made to order. , 1969, The Annals of thoracic surgery.

[93]  J. Thyberg,et al.  Smooth-muscle progenitor cells of bone marrow origin contribute to the development of neointimal thickenings in rat aortic allografts and injured rat carotid arteries1 , 2002, Transplantation.

[94]  W. F. Mason,et al.  Necessity for elastic properties in synthetic arterial grafts. , 1974, Canadian journal of surgery. Journal canadien de chirurgie.

[95]  P. Nickerson,et al.  Neointimal and tubulointerstitial infiltration by recipient mesenchymal cells in chronic renal-allograft rejection. , 2001, The New England journal of medicine.

[96]  R Langer,et al.  Functional arteries grown in vitro. , 1999, Science.

[97]  J. Campbell,et al.  Novel vascular graft grown within recipient's own peritoneal cavity. , 1999, Circulation research.

[98]  Julie H. Campbell,et al.  The effect of environmental cues on the differentiation of myofibroblasts in peritoneal granulation tissue , 2000, The Journal of pathology.

[99]  D. Vorp,et al.  ePTFE coating with fibrin glue, FGF-1, and heparin: effect on retention of seeded endothelial cells. , 1996, The Journal of surgical research.

[100]  P. Libby,et al.  Host bone-marrow cells are a source of donor intimal smooth- muscle–like cells in murine aortic transplant arteriopathy , 2001, Nature Medicine.

[101]  K. Ley,et al.  Arterial Injury Increases Expression of Inflammatory Adhesion Molecules in the Carotid Arteries of Apolipoprotein-E-Deficient Mice1 , 1999, Journal of Vascular Research.

[102]  R. Nerem,et al.  Cyclic strain induces an oxidative stress in endothelial cells. , 1997, The American journal of physiology.

[103]  Anthony Atala,et al.  Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo , 2001, Nature Medicine.

[104]  K. Black,et al.  Transformation of nonvascular acellular tissue matrices into durable vascular conduits. , 2001, The Annals of thoracic surgery.

[105]  T. Matsuda,et al.  Venous reconstruction using hybrid vascular tissue composed of vascular cells and collagen: tissue regeneration process. , 1996, Cell transplantation.

[106]  F. Logerfo,et al.  A comparative study of alternative conduits for lower extremity revascularization: all-autogenous conduit versus prosthetic grafts. , 2000, Journal of vascular surgery.

[107]  H. Mertsching,et al.  Guided tissue regeneration of vascular grafts in the peritoneal cavity. , 2002, Circulation research.