Approaches to heart valve tissue engineering scaffold design.

Heart valve disease is a significant cause of mortality worldwide. However, to date, a nonthrombogenic, noncalcific prosthetic, which maintains normal valve mechanical properties and hemodynamic flow, and exhibits sufficient fatigue properties has not been designed. Current prosthetic designs have not been optimized and are unsuitable treatment for congenital heart defects. Research is therefore moving towards the development of a tissue engineered heart valve equivalent. Two approaches may be used in the creation of a tissue engineered heart valve, the traditional approach, which involves seeding a scaffold in vitro, in the presence of specific signals prior to implantation, and the guided tissue regeneration approach, which relies on autologous reseeding in vivo. Regardless of the approach taken, the design of a scaffold capable of supporting the growth of cells and extracellular matrix generation and capable of withstanding the unrelenting cardiovascular environment while forming a tight seal during closure, is critical to the success of the tissue engineered construct. This paper focuses on the quest to design, such a scaffold.

[1]  Frederick J. Schoen,et al.  Early In Vivo Experience With Tissue-Engineered Trileaflet Heart Valves , 2000, Circulation.

[2]  K J Halbhuber,et al.  Comparative study of cellular and extracellular matrix composition of native and tissue engineered heart valves. , 2004, Matrix biology : journal of the International Society for Matrix Biology.

[3]  H. Scheld,et al.  Tissue Engineering of Heart Valves: Formation of a Three-Dimensional Tissue Using Porcine Heart Valve Cells , 2002, ASAIO journal.

[4]  A. Gotlieb,et al.  Advances towards understanding heart valve response to injury. , 2002, Cardiovascular pathology : the official journal of the Society for Cardiovascular Pathology.

[5]  E. Minar,et al.  Prospective clinical study with in vitro endothelial cell lining of expanded polytetrafluoroethylene grafts in crural repeat reconstruction. , 1992, Journal of vascular surgery.

[6]  Jeffrey A. Hubbell,et al.  Biomaterials in Tissue Engineering , 1995, Bio/Technology.

[7]  S Jockenhoevel,et al.  Fibrin gel as a three dimensional matrix in cardiovascular tissue engineering. , 2000, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[8]  V. Crescenzi,et al.  New cross-linked and sulfated derivatives of partially deacetylated hyaluronan: synthesis and preliminary characterization. , 2002, Biopolymers.

[9]  P. Wolf,et al.  Heart disease and stroke statistics--2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. , 2006, Circulation.

[10]  Ernst Wolner,et al.  The decellularized porcine heart valve matrix in tissue engineering , 2005, Thrombosis and Haemostasis.

[11]  Robert M Nerem,et al.  Valvular endothelial cells regulate the phenotype of interstitial cells in co-culture: effects of steady shear stress. , 2006, Tissue engineering.

[12]  D C Teller,et al.  Crosslinking kinetics of the human transglutaminase, factor XIII[A2], acting on fibrin gels and gamma-chain peptides. , 1997, Biochemistry.

[13]  Kristi S Anseth,et al.  Synthesis and characterization of photocrosslinkable, degradable poly(vinyl alcohol)-based tissue engineering scaffolds. , 2002, Biomaterials.

[14]  T. Shih,et al.  Development of Intracranial Complications following Transoral Stab Wounds in Children , 2002, Pediatric Neurosurgery.

[15]  U. Stock,et al.  Performance of decellularized xenogeneic tissue in heart valve replacement. , 2006, Biomaterials.

[16]  Simon P Hoerstrup,et al.  Human umbilical cord cells: a new cell source for cardiovascular tissue engineering. , 2002, The Annals of thoracic surgery.

[17]  Artur Lichtenberg,et al.  Flow-dependent re-endothelialization of tissue-engineered heart valves. , 2006, The Journal of heart valve disease.

[18]  D. Herbage,et al.  Collagen-based biomaterials as 3D scaffold for cell cultures: applications for tissue engineering and gene therapy , 2000, Medical and Biological Engineering and Computing.

[19]  J. Ronald,et al.  Dermal fibroblasts cultured on small intestinal submucosa: Conditions for the formation of a neotissue. , 2005, Journal of biomedical materials research. Part A.

[20]  Kristyn S Masters,et al.  Designing scaffolds for valvular interstitial cells: cell adhesion and function on naturally derived materials. , 2004, Journal of biomedical materials research. Part A.

[21]  H. Alexander,et al.  Development and characterization of tissue-engineered aortic valves. , 2001, Tissue engineering.

[22]  B J Messmer,et al.  Tissue engineering: complete autologous valve conduit--a new moulding technique. , 2001, The Thoracic and cardiovascular surgeon.

[23]  F J Schoen,et al.  Functional Living Trileaflet Heart Valves Grown In Vitro , 2000, Circulation.

[24]  F J Schoen,et al.  Tissue engineering of heart valves: in vitro experiences. , 2000, The Annals of thoracic surgery.

[25]  A Haverich,et al.  Acellularized porcine heart valve scaffolds for heart valve tissue engineering and the risk of cross-species transmission of porcine endogenous retrovirus. , 2003, The Journal of thoracic and cardiovascular surgery.

[26]  Dusan Pavcnik,et al.  Transcatheter placement of a low-profile biodegradable pulmonary valve made of small intestinal submucosa: a long-term study in a swine model. , 2005, The Journal of thoracic and cardiovascular surgery.

[27]  Gino Gerosa,et al.  Cell characterization of porcine aortic valve and decellularized leaflets repopulated with aortic valve interstitial cells: the VESALIO Project (Vitalitate Exornatum Succedaneum Aorticum Labore Ingenioso Obtenibitur). , 2003, The Annals of thoracic surgery.

[28]  C. Stamm,et al.  Mechanical and structural properties of a novel hybrid heart valve scaffold for tissue engineering. , 2004, Artificial organs.

[29]  P J Kilner,et al.  The aortic outflow and root: a tale of dynamism and crosstalk. , 1999, The Annals of thoracic surgery.

[30]  L. Leinwand,et al.  Serum deprivation improves seeding and repopulation of acellular matrices with valvular interstitial cells. , 2005, Journal of biomedical materials research. Part A.

[31]  C K Breuer,et al.  Tissue engineering heart valves: valve leaflet replacement study in a lamb model. , 1995, The Annals of thoracic surgery.

[32]  W G Kim,et al.  Tissue-Engineered Heart Valve Leaflets: An Animal Study , 2001, The International journal of artificial organs.

[33]  M. DeRuiter,et al.  Histological evaluation of decellularised porcine aortic valves: matrix changes due to different decellularisation methods. , 2005, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[34]  Michael S Sacks,et al.  The independent role of cyclic flexure in the early in vitro development of an engineered heart valve tissue. , 2005, Biomaterials.

[35]  Michael Sacks,et al.  Thoracic Surgery Directors Association Award. Bone marrow as a cell source for tissue engineering heart valves. , 2003, The Annals of thoracic surgery.

[36]  I. C. Howard,et al.  On the opening mechanism of the aortic valve: some observations from simulations , 2003, Journal of medical engineering & technology.

[37]  D E Pegg,et al.  Freeze drying of cardiac valves in preparation for cellular repopulation. , 1997, Cryobiology.

[38]  David P. Martin,et al.  Quantitative evaluation of endothelial progenitors and cardiac valve endothelial cells: proliferation and differentiation on poly-glycolic acid/poly-4-hydroxybutyrate scaffold in response to vascular endothelial growth factor and transforming growth factor beta1. , 2003, Tissue engineering.

[39]  H. Gulbins,et al.  Preseeding with autologous fibroblasts improves endothelialization of glutaraldehyde-fixed porcine aortic valves. , 2003, The Journal of thoracic and cardiovascular surgery.

[40]  U. Galili,et al.  The α-Gal epitope (Galα1-3Galβ1-4GlcNAc-R) in xenotransplantation. , 2001, Biochimie.

[41]  A Haverich,et al.  Tissue Engineering of Pulmonary Heart Valves on Allogenic Acellular Matrix Conduits: In Vivo Restoration of Valve Tissue , 2000, Circulation.

[42]  A. Hoffman,et al.  Adhesive protein interactions with chitosan: consequences for valve endothelial cell growth on tissue-engineering materials. , 2003, Journal of biomedical materials research. Part A.

[43]  Ivan Vesely,et al.  Heart Valve Tissue Engineering , 2005 .

[44]  H. Yeger,et al.  Acellular matrix: a biomaterials approach for coronary artery bypass and heart valve replacement. , 1995, The Annals of thoracic surgery.

[45]  U A Stock,et al.  Tissue engineering of cardiac valves on the basis of PGA/PLA Co-polymers. , 2001, Journal of long-term effects of medical implants.

[46]  KAREN MENDELSON,et al.  Heart Valve Tissue Engineering: Concepts, Approaches, Progress, and Challenges , 2006, Annals of Biomedical Engineering.

[47]  E Wolner,et al.  Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients. , 2003, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[48]  A. Ramamurthi,et al.  Smooth muscle cell adhesion on crosslinked hyaluronan gels. , 2002, Journal of biomedical materials research.

[49]  E. Wolner,et al.  Decellularization does not eliminate thrombogenicity and inflammatory stimulation in tissue-engineered porcine heart valves. , 2006, The Journal of heart valve disease.

[50]  C K Breuer,et al.  The in vitro construction of a tissue engineered bioprosthetic heart valve. , 1997, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[51]  Jian Yang,et al.  Biodegradable polyester elastomers in tissue engineering , 2004, Expert opinion on biological therapy.

[52]  J. Suh,et al.  Application of chitosan-based polysaccharide biomaterials in cartilage tissue engineering: a review. , 2000, Biomaterials.

[53]  B Glasmacher,et al.  In vitro modelling of tissue using isolated vascular cells on a synthetic collagen matrix as a substitute for heart valves. , 2001, The Thoracic and cardiovascular surgeon.

[54]  D. Mulholland,et al.  Cardiac valve interstitial cells: regulator of valve structure and function. , 1997 .

[55]  D E Pegg,et al.  Repopulation of freeze-dried porcine valves with human fibroblasts and endothelial cells. , 1997, The Journal of heart valve disease.

[56]  Timothy M. Rose,et al.  Type C Retrovirus Released from Porcine Primary Peripheral Blood Mononuclear Cells Infects Human Cells , 1998, Journal of Virology.

[57]  M. Grinstaff,et al.  Photocrosslinkable polysaccharides for in situ hydrogel formation. , 2001, Journal of biomedical materials research.

[58]  Klaus-Peter Schmitz,et al.  Biomatrix/polymer composite material for heart valve tissue engineering. , 2004, The Annals of thoracic surgery.

[59]  Christine E Schmidt,et al.  Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. , 2003, Biotechnology and bioengineering.

[60]  Birgit Glasmacher,et al.  Ultrastructure of proteoglycans in tissue-engineered cardiovascular structures. , 2002, Tissue engineering.

[61]  Robert T Tranquillo,et al.  Tissue-engineered valves with commissural alignment. , 2004, Tissue engineering.

[62]  Yasuhiro Takeuchi,et al.  Infection of human cells by an endogenous retrovirus of pigs , 1997, Nature Medicine.

[63]  Michael S Sacks,et al.  From Stem Cells to Viable Autologous Semilunar Heart Valve , 2005, Circulation.

[64]  D. Sierra,et al.  Fibrin Sealant Adhesive Systems: A Review of Their Chemistry, Material Properties and Clinical Applications , 1993, Journal of biomaterials applications.

[65]  M. Simionescu,et al.  Interstitial Cells of the Heart Valves Possess Characteristics Similar to Smooth Muscle Cells , 1986, Circulation research.

[66]  Lars Lind,et al.  Different Metabolic Predictors of White-Coat and Sustained Hypertension Over a 20-Year Follow-Up Period: A Population-Based Study of Elderly Men , 2002, Circulation.

[67]  W. Lougheed,et al.  Homologous Aortic-Valve-Segment Transplants as Surgical Treatment for Aortic and Mitral Insufficiency , 1956, Angiology.

[68]  G. Gerosa,et al.  Isolation of intact aortic valve scaffolds for heart-valve bioprostheses: extracellular matrix structure, prevention from calcification, and cell repopulation features. , 2003, Journal of biomedical materials research. Part A.

[69]  Joseph P. Vacanti,et al.  Evaluation of biodegradable, three-dimensional matrices for tissue engineering of heart valves. , 1999, ASAIO journal.

[70]  Christopher K Breuer,et al.  Application of tissue-engineering principles toward the development of a semilunar heart valve substitute. , 2004, Tissue engineering.

[71]  Y. Takeuchi,et al.  Productive infection of primary human endothelial cells by pig endogenous retrovirus (PERV) , 2000, Xenotransplantation.

[72]  A Haverich,et al.  Tissue engineering of heart valves--human endothelial cell seeding of detergent acellularized porcine valves. , 1998, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[73]  S. Badylak Regenerative medicine approach to heart valve replacement. , 2005, Circulation.

[74]  A. Ramamurthi,et al.  Ultraviolet light-induced modification of crosslinked hyaluronan gels. , 2003, Journal of biomedical materials research. Part A.

[75]  C. Schmidt,et al.  Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. , 2000, Biomaterials.

[76]  Ernst Wolner,et al.  Decellularization protocols of porcine heart valves differ importantly in efficiency of cell removal and susceptibility of the matrix to recellularization with human vascular cells. , 2004, The Journal of thoracic and cardiovascular surgery.

[77]  I Vesely,et al.  The role of elastin in aortic valve mechanics. , 1997, Journal of biomechanics.

[78]  B J Messmer,et al.  Fibrin gel -- advantages of a new scaffold in cardiovascular tissue engineering. , 2001, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[79]  M. Sacks,et al.  Biaxial mechanical properties of the natural and glutaraldehyde treated aortic valve cusp--Part I: Experimental results. , 2000, Journal of biomechanical engineering.

[80]  R. Bareille,et al.  Clinical performance of vascular grafts lined with endothelial cells. , 1999, Endothelium : journal of endothelial cell research.

[81]  Robert M Nerem,et al.  Unique Morphology and Focal Adhesion Development of Valvular Endothelial Cells in Static and Fluid Flow Environments , 2004, Arteriosclerosis, thrombosis, and vascular biology.

[82]  T. Shinoka Tissue engineered heart valves: autologous cell seeding on biodegradable polymer scaffold. , 2002, Artificial organs.

[83]  David P. Martin,et al.  Fabrication of a trileaflet heart valve scaffold from a polyhydroxyalkanoate biopolyester for use in tissue engineering. , 2000, Tissue engineering.

[84]  Thomas N Robinson,et al.  Cardiovascular Health in Childhood: A Statement for Health Professionals From the Committee on Atherosclerosis, Hypertension, and Obesity in the Young (AHOY) of the Council on Cardiovascular Disease in the Young, American Heart Association , 2002, Circulation.

[85]  S. Hanson,et al.  Confluent durable endothelialization of endarterectomized baboon aorta by early attachment of cultured endothelial cells. , 1990, Journal of vascular surgery.

[86]  Xin Chen,et al.  Biocompatibility of Poly(ε-caprolactone) Scaffold Modified by Chitosan—The Fibroblasts Proliferation in vitro , 2005 .

[87]  Y. M. Elçin,et al.  Hepatocyte attachment on biodegradable modified chitosan membranes: in vitro evaluation for the development of liver organoids. , 1998, Artificial organs.

[88]  Eleftherios Sachlos,et al.  Interaction of human valve interstitial cells with collagen matrices manufactured using rapid prototyping. , 2006, Biomaterials.

[89]  I Vesely,et al.  Evaluation of the matrix-synthesis potential of crosslinked hyaluronan gels for tissue engineering of aortic heart valves. , 2005, Biomaterials.

[90]  A Haverich,et al.  Heart valves from pigs and the porcine endogenous retrovirus: experimental and clinical data to assess the probability of porcine endogenous retrovirus infection in human subjects. , 2001, The Journal of thoracic and cardiovascular surgery.

[91]  Magdi H Yacoub,et al.  Human cardiac valve interstitial cells in collagen sponge: a biological three-dimensional matrix for tissue engineering. , 2002, The Journal of heart valve disease.

[92]  Stefan Jockenhoevel,et al.  A collagen-glycosaminoglycan co-culture model for heart valve tissue engineering applications. , 2006, Biomaterials.

[93]  Artur Lichtenberg,et al.  In vitro re-endothelialization of detergent decellularized heart valves under simulated physiological dynamic conditions. , 2006, Biomaterials.

[94]  Robert M Nerem,et al.  Porcine aortic valve interstitial cells in three-dimensional culture: comparison of phenotype with aortic smooth muscle cells. , 2004, The Journal of heart valve disease.

[95]  Frederick J Schoen,et al.  Evolution of cell phenotype and extracellular matrix in tissue-engineered heart valves during in-vitro maturation and in-vivo remodeling. , 2002, The Journal of heart valve disease.

[96]  G. Christie,et al.  Mechanical properties of porcine pulmonary valve leaflets: how do they differ from aortic leaflets? , 1995, The Annals of thoracic surgery.

[97]  Kristyn S Masters,et al.  Crosslinked hyaluronan scaffolds as a biologically active carrier for valvular interstitial cells. , 2005, Biomaterials.

[98]  Shen‐guo Wang,et al.  Fabrication and biocompatibility of cell scaffolds of poly(L-lactic acid) and poly(L-lactic-co-glycolic acid) , 2002 .

[99]  D. Adams,et al.  Mechanisms of Galα1-3Galβ1-4GlcNAc-R (αGal) expression on porcine valve endothelial cells , 2003 .

[100]  Y. Ikada,et al.  Tissue-Engineered Grafts Matured in the Right Ventricular Outflow Tract , 2004, Cell transplantation.