Tissue engineering of vascular vessels: the methods of cells and scaffold combining

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access


Cell seeding is one of the most important stages in tissue engineering. Attempting to achieve fast, efficient and reliable result researchers in vascular tissue engineering use advantages of the tubular geometry of the grafts with conjunction of physical forces, such as pressure difference, centrifugal, electrostatic, magnetic forces and their combinations. This review describes the main trends and challenges in scaffold developing, main cellular types used for vascular tissue engineering and various methods for cell seeding, their advantages and drawbacks.

About the authors

A. S Nasredinov

Federal Almazov Medical Research Center, Saint-Petersburg, Russia

A. V Lavreshin

Federal Almazov Medical Research Center, Saint-Petersburg, Russia


  1. Veith F.J., Gupta S.K., Ascer E. et al. Six-year prospective multicenter randomized comparison of autologous saphenous vein and expanded polytetrafluoroethylene grafts in infrainguinal arterial reconstructions. J. Vasc. Surg. 1986; 3(1): 104-14.
  2. Sapsford R.N., Oakley G.D., Talbot S. Early and late patency of expanded polytetrafluoroethylene vascular grafts in aorta-coronary bypass. J. Thorac. Cardiovasc. Surg. 1981; 81(6): 860-4.
  3. Klinkert P., Post P.N., Breslau P.J. et al. Saphenous vein versus PTFE for above-knee femoropopliteal bypass. A review of the literature. Eur. J. Vasc. Endovasc. Surg. 2004; 27(4): 357-62
  4. Herring M., Gardner A., Glover J. A single-staged technique for seeding vascular grafts with autogenous endothelium. Surgery 1978; 84(4): 498-504.
  5. Herring M.B., Dilley R., Jersild R.A. et al. Seeding arterial prostheses with vascular endothelium. The nature of the lining. Ann. Surg. 1979; 190(1): 84-90.
  6. Thomson G.J.L., Vohra R., Walker M.G. Cell Seeding for Small Diameter ePTFE Vascular Grafts: A Comparison Between Adult Human Endothelial and Mesothelial Cells. Ann. Vasc. Surg. 1989; 3(2): 140-5.
  7. Shin'oka T., Matsumura G., Hibino N. et al. Midterm clinical result of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J. Thorac. Cardiovasc. Surg. 2005; 129(6): 1330-8.
  8. L'Heureux N., Dusserre N., Marini A. et al. Technology insight: the evolution of tissue-engineered vascular grafts--from research to clinical practice. Nat. Clin. Pract. Cardiovasc. Med. 2007; 4(7): 389-95.
  9. Naito Y., Shinoka T., Duncan D. et al. Vascular tissue engineering: Towards the next generation vascular grafts. Adv. Drug Deliv. Rev. 2011; 63(4-5): 312-23.
  10. Campbell G.R., Campbell J.H. Development of tissue engineered vascular grafts. Curr. Pharm. Biotechnol. 2007; 8(1): 43-50.
  11. Chen Q.-Z., Harding S.E., Ali N.N. et al. Biomaterials in cardiac tissue engineering: Ten years of research survey. Mater. Sci. Eng.: R: Rep. 2008; 59(1-6): 1-37.
  12. Kalra M., Miller V.M. Early remodeling of saphenous vein grafts: proliferation, migration and apoptosis of adventitial and medial cells occur simultaneously with changes in graft diameter and blood flow. J. Vasc. Res. 2000; 37(6): 576-84.
  13. Villalona G.A., Udelsman B., Duncan D.R. et al. Cell-seeding techniques in vascular tissue engineering. Tissue Eng., Part B Rev. 2010; 16(3): 341-50.
  14. Mohebbi-Kalhori D., Rukhlova M., Ajji A. et al. A novel automated cell-seeding device for tissue engineering of tubular scaffolds: design and functional validation. J. Tissue Eng. Regen. Med. 2012; 6(9): 710-20.
  15. Nieponice A., Soletti L., Guan J. et al. Development of a tissue-engineered vascular graft combining a biodegradable scaffold, muscle-derived stem cells and a rotational vacuum seeding technique. Biomaterials 2008; 29(7): 825-33.
  16. Krawiec J.T., Vorp D.A. Adult stem cell-based tissue engineered blood vessels: a review. Biomaterials 2012; 33(12): 3388-400.
  17. Pawlowski K.J., Rittgers S.E., Schmidt S.P. et al. Endothelial cell seeding of polymeric vascular grafts. Front. Biosci. 2004; 9: 1412-21.
  18. Hashi C.K., Zhu Y., Yang G.-Y. et al. Antithrombogenic property of bone marrow mesenchymal stem cells in nanofibrous vascular grafts. PNAS USA 2007; 104(29): 11915-20.
  19. Cho S.-W., Lim S.H., Kim I.-K. et al. Small-diameter blood vessels engineered with bone marrow-derived cells. Ann. Surg. 2005; 241(3): 506-15.
  20. Yow K.-H., Ingram J., Korossis S.A. et al. Tissue engineering of vascular conduits. Br. J. Surg. 2006; 93(6): 652-61.
  21. Parikh S.A., Edelman E.R. Endothelial cell delivery for cardiovascular therapy. Adv. Drug Deliv. Rev. 2000; 42(1-2): 139-61.
  22. Kakisis J.D., Liapis C.D., Breuer C. et al. Artificial blood vessel: the Holy Grail of peripheral vascular surgery. J. Vasc. Surg. 2005; 41(2): 349-54.
  23. Conte M.S. The ideal small arterial substitute: a search for the Holy Grail? FASEB J. 1998; 12(1): 43-5.
  24. Ahsan T., Nerem R.M. Bioengineered tissues: the science, the technology, and the industry. Orthod. Craniofac. Res. 2005; 8(3): 134-40.
  25. Ravi S., Qu Z., Chaikof E.L. Polymeric materials for tissue engineering of arterial substitutes. Vascular 2009; 17(Sup.1): S45-54.
  26. Kim B.S., Putnam A.J., Kulik T.J. et al. Optimizing seeding and culture methods to engineer smooth muscle tissue on biodegradable polymer matrices. Biotechnol. Bioeng. 1998; 57(1): 46-54.
  27. Udelsman B., Hibino N., Villalona G.A. et al. Development of an operator-independent method for seeding tissue-engineered vascular grafts. Tissue Eng. Part C Methods 2011; 17(7): 731-6.
  28. Berglund J.D., Mohseni M.M., Nerem R.M. et al. A biological hybrid model for collagen-based tissue engineered vascular constructs. Biomaterials 2003; 24(7): 1241-54.
  29. Bacakova L., Novotna K., Panzek M. Polysaccharides as cell carriers for tissue engineering: the use of cellulose in vascular wall reconstruction. Physiol. Res. 2014; 63(Sup.1): S29-47.
  30. Seib F.P., Herklotz M., Burke K.A. et al. Multifunctional silk-heparin biomaterials for vascular tissue engineering applications. Biomaterials 2014; 35(1): 83-91.
  31. Wray L.S., Tsioris K., Gi E.S. et al. Slowly degradable porous silk microfabricated scaffolds for vascularized tissue formation. Adv. Funct. Mater. 2013; 23(27): 3404-12.
  32. Schaner P.J., Martin N.D., Tulenko T.N. et al. Decellularized vein as a potential scaffold for vascular tissue engineering. J. Vasc. Surg. 2004; 40(1): 146-53.
  33. Shimizu K., Ito A., Arinobe M. et al. Effective cell-seeding technique using magnetite nanoparticles and magnetic force onto decellularized blood vessels for vascular tissue engineering. J. Biosci. Bioeng. 2007; 103(5): 472-78.
  34. Teebken O.E., Bader A., Steinhoff G. et al. Tissue Engineering of vascular grafts: human cell seeding of decellularised porcine matrix. Eur. J. Vasc. Endovasc. Surg. 2000; 19(4): 381-6.
  35. Kim B.-S., Park I.-K., Hoshiba T. et al. Design of artificial extracellular matrices for tissue engineering. Prog. Polym. Sci. 2011; 36(2): 238-68.
  36. Kim B.-S., Nikolovski J., Bonadio J. et al. Engineered smooth muscle tissues: regulating cell phenotype with the scaffold. Exp. Cell Res. 1999; 251(2): 318-28.
  37. Niklason L.E., Gao J., Abbott W.M. et al. Functional arteries grown in vitro. Science 1999; 284(5413): 489-93.
  38. Higgins S.P., Solan A.K., Niklason L.E. Effects of polyglycolic acid on porcine smooth muscle cell growth and differentiation. J. Biomed. Mater. Res. A 2003; 67 A(1): 295-302.
  39. Shum-Tim D., Stock U., Hrkach J. et al. Tissue engineering of autologous aorta using a new biodegradable polymer. Ann. Thorac. Surg. 1999; 68(6): 2298-304.
  40. Hoerstrup S.P., Kadner A., Breymann C. et al. Living, autologous pulmonary artery conduits tissue engineered from human umbilical cord cells. Ann. Thorac. Surg. 2002; 74(1): 46-52.
  41. Gogolewski S., Jovanovic M., Perren S. et al. Tissue response and in vivo degradation of selected polyhydroxyacids: polylactides (PLA), poly(3-hydroxybutyrate) (PHB), and poly(3-hydroxybutyrate-co-3-hydroxyvalerate) (pHb/VA). J. Biomed. Mater. Res. 1993; 27 (9): 1135-48.
  42. Watanabe M., Shin'oka T., Tohyama S. et al. Tissue-engineered vascular autograft: inferior vena cava replacement in a dog model. Tissue Eng. 2001; 7(4): 429-39.
  43. Mooney D.J., Mazzoni C.L., Breuer C. et al. Stabilized polyglycolic acid fibre-based tubes for tissue engineering. Biomaterials 1996; 17(2): 115-24.
  44. Wake M.C., Gupta P.K., Mikos A.G. Fabrication of pliable biodegradable polymer foams to engineer soft tissues. Cell Transplant. 1996; 5(4): 465-73.
  45. Nerem R.M., Seliktar D. Vascular Tissue Engineering. Annu. Rev. Biomed. Eng. 2001; 3(1): 225-43.
  46. Zhang W.J., Liu W., Cui L. Tissue engineering of blood vessel. J. Cell Mol. Med. 2007; 11(5): 945-57.
  47. Sobral J.M., Caridade S.G., Sousa R.A. et al. Threedimensional plotted scaffolds with controlled pore size gradients: Effect of scaffold geometry on mechanical performance and cell seeding efficiency. Acta Biomater. 2011; 7(3): 1009-18.
  48. O'Brien F.J., Harley B.A., Waller M.A. et al. The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol. Health Care 2007; 15(1): 3-17.
  49. Murphy C.M., O'Brien F.J. Understanding the effect of mean pore size on cell activity in collagen-glycosaminoglycan scaffolds. Cell Adhes. Migr. 2010; 4(3): 377-81.
  50. Ma H., Hu J., Ma P.X. Polymer scaffolds for small-diameter vascular tissue engineering. Adv. Funct. Mater. 2010; 20(17): 2833-41.
  51. Sodian R., Lemke T., Fritsche C. et al. Tissue-engineering bioreactors: a new combined cell-seeding and perfusion system for vascular tissue engineering. Tissue Eng. 2002; 8(5): 863-70.
  52. Boccafoschi F., Habermehl J., Vesentini S. et al. Biological performances of collagen-based scaffolds for vascular tissue engineering. Biomaterials 2005; 26(35): 7410-7.
  53. Weinberg C.B., Bell E. A blood vessel model constructed from collagen and cultured vascular cells. Science 1986; 231(4736): 397-400.
  54. Hirai J., Kanda K., Oka T. et al. Highly oriented, tubular hybrid vascular tissue for a low pressure circulatory system. ASAIO J. 1994; 40(3): 383-8.
  55. Hirai J., Matsuda T. Venous reconstruction using hybrid vascular tissue composed of vascular cells and collagen: Tissue regeneration process. Cell Transplant. 1996; 5(1): 93-105.
  56. Crapo P.M., Gilbert T.W., Badylak S.F. An overview of tissue and whole organ decellularization processes. Biomaterials 2011; 32(12): 3233-43.
  57. Dahl S.L.M., Koh J., Prabhakar V. et al. Decellularized native and engineered arterial scaffolds for transplantation. Cell Transplant. 2003; 12(6): 659-66.
  58. Murase Y., Narita Y., Kagami H. et al. Evaluation of compliance and stiffness of decellularized tissues as scaffolds for tissue-engineered small caliber vascular grafts using intravascular ultrasound. ASAIO J. 2006; 52(4): 450-5.
  59. Zhao Y., Zhang S., Zhou J. et al. The development of a tissue-engineered artery using decellularized scaffold and autologous ovine mesenchymal stem cells. Biomaterials 2010; 31(2): 296-307.
  60. Fitzpatrick J.C., Clark P.M., Capaldi F.M. Effect of decellularization protocol on the mechanical behavior of porcine descending aorta. Int. J. Biomater. 2010; 2010: 1-11.
  61. McFetridge P.S., Daniel J.W., Bodamyali T. et al. Preparation of porcine carotid arteries for vascular tissue engineering applications. J. Biomed. Mater. Res. A. 2004; 70A(2): 224-34.
  62. Soletti L., Hong Y., Guan J. et al. A bi-layered elastomeric scaffold for tissue engineering of small-diameter vascular grafts. Acta Biomater. 2010; 6(1): 110-22.
  63. Mathews A., Colombus S., Krishnan V.K. et al. Vascular tissue construction on poly(e-caprolactone) scaffolds by dynamic endothelial cell seeding: effect of pore size. J. Tissue Eng. Regen. Med. 2012; 6(6): 451-61.
  64. Nemeno-Guanzon J.G., Lee S., Berg J.R. et al. Trends in tissue engineering for blood vessels. J. Biomed. Biotechnol. 2012; 2012: 1-14.
  65. Bajpai V.K., Andreadis S.T. Stem cell sources for vascular tissue engineering and regeneration. Tissue Eng. Part B Rev. 2012; 18(5): 405-25.
  66. Stegemann J.P., Kaszuba S.N., Rowe S.L. Review: advances in vascular tissue engineering using protein-based biomaterials. Tissue Eng. 2007; 13(11): 2601-13.
  67. Peck M., Gebhart D., Dusserre N. et al. The evolution of vascular tissue engineering and current state of the art. Cells Tissues Organs 2011; 195(1-2): 144-58.
  68. Howard D., Buttery L.D., Shakesheff K.M. et al. Tissue engineering: strategies, stem cells and scaffolds. J. Anat. 2008; 213(1): 66-72.
  69. Hass R., Kasper C., Bohm S. et al. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun. Signal. 2011; 9: 1-14
  70. Roh J.D., Nelson G.N., Udelsman B.V. et al. Centrifugal seeding increases seeding efficiency and cellular distribution of bone marrow stromal cells in porous biodegradable scaffolds. Tissue Eng. 2007; 13(11): 2743-9.
  71. Ma P.X. Biomimetic materials for tissue engineering. Adv. Drug Deliv. Rev. 2008; 60(2): 184-98.
  72. West J.L. Modification of materials with bioactive peptides. In: Hollander A.P., Hatton P.V., еditors. Biopolymer methods in tissue engineering. Clifton New Jersey: Humana Press; 2004. p. 113-22.
  73. Schmidt C.E., Baier J.M. Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. Biomaterials 2000; 21(22): 2215-31.
  74. Salacinski H.J., Tiwari A., Hamilton G. et al. Cellular engineering of vascular bypass grafts: role of chemical coatings for enhancing endothelial cell attachment. Med. Biol. Eng. Comput. 2001; 39(6): 609-18.
  75. Sagnella S., Anderson E., Sanabria N. et al. Human endothelial cell interaction with biomimetic surfactant polymers containing Peptide ligands from the heparin binding domain of fibronectin. Tissue Eng. 2005; 11(1-2): 226-36.
  76. Stephan S., Ball S.G., Williamson M. et al. Cell-matrix biology in vascular tissue engineering. J. Anat. 2006; 209(4): 495-502.
  77. Mann B.K., Schmedlen R.H., West J.L. Tethered-TGF-p increases extracellular matrix production of vascular smooth muscle cells. Biomaterials 2001; 22(5): 439-44.
  78. Drumheller P.D., Hubbell J.A. Polymer networks with grafted cell adhesion peptides for highly biospecific cell adhesive substrates. Anal. Biochem. 1994; 222(2): 380-8.
  79. Blum J.S., Temenoff J.S., Park H. et al. Development and characterization of enhanced green fluorescent protein and luciferase expressing cell line for non-destructive evaluation of tissue engineering constructs. Biomaterials 2004; 25(27): 5809-19.
  80. Godbey W.T., Hindy S.B.S, Sherman M.E. et al. A novel use of centrifugal force for cell seeding into porous scaffolds. Biomaterials 2004; 25(14): 2799-805.
  81. Yasuda K., Inoue S., Tabata Y. Influence of culture method on the proliferation and osteogenic differentiation of human adipo-stromal cells in nonwoven fabrics. Tissue Eng. 2004; 10(9-10): 1587-96.
  82. Vunjak-Novakovic G., Obradovic B., Martin I. et al. Dynamic cell seeding of polymer scaffolds for cartilage tissue engineering. Biotechnol. Prog. 1998; 14(2): 193-202.
  83. Hsu S., Tsai I., Lin D. et al. The effect of dynamic culture conditions on endothelial cell seeding and retention on small diameter polyurethane vascular grafts. Med. Eng. Phys. 2005; 27(3): 267-72.
  84. Wang S., Mo X.M., Jiang B.J. et al. Fabrication of small-diameter vascular scaffolds by heparin-bonded P(LLA-CL) composite nanofibers to improve graft patency. Int. J. Nanomedicine 2013; 8): 2131-9.
  85. Nasseri B.A., Pomerantseva I., Kaazempur-Mofrad M.R. et al. Dynamic rotational seeding and cell culture system for vascular tube formation. Tissue Eng. 2003; 9(2): 291-9.
  86. Ng R., Gurm J.S., Yang S.-T. Centrifugal seeding of mammalian cells in nonwoven fibrous matrices. Biotechnol. Prog. 2010; 26(1): 239-45.
  87. Way L., Scutt N., Scutt A. Cytocentrifugation: a convenient and efficient method for seeding tendon-derived cells into monolayer cultures or 3-D tissue engineering scaffolds. Cytotechnology 2011; 63(6): 567-79.
  88. Wolf M., Yunker L., Trescony P. Seeding implantable medical devices with cells. US patent WO/2006/094146. 2006.
  89. Bowlin G.L., Meyer A., Fields C. et al. The persistence of electrostatically seeded endothelial cells lining a small diameter expanded polytetrafluoroethylene vascular graft. J. Biomater. Appl. 2001; 16(2): 157-73.
  90. Fields C., Cassano A., Allen C. et al. Endothelial cell seeding of a 4-mm I.D. polyurethane vascular graft. J. Biomater. Appl. 2002; 17(1): 45-70.
  91. Fields C., Cassano A., Makhoul R.G. et al. Evaluation of electrostatically endothelial cell seeded expanded polytetrafluoroethylene grafts in a canine femoral artery model. J. Biomater. Appl. 2002; 17(2): 135-52.
  92. Kempczinski R.F., Rosenman J.E., Pearce W.H. et al. Endothelial cell seeding of a new PTFE vascular prosthesis. J. Vasc. Surg. 1985; 2(3): 424-9.
  93. Williams C., Wick T.M. Perfusion bioreactor for small diameter tissue-engineered arteries. Tissue Eng. 2004; 10(5-6): 930-41.
  94. Van Wachem P.B., Stronck J.W., Koers-Zuideveld R. et al. Vacuum cell seeding: a new method for the fast application of an evenly distributed cell layer on porous vascular grafts. Biomaterials 1990; 11(8): 602-6.
  95. Solchaga L.A., Tognana E., Penick K. et al. A rapid seeding technique for the assembly of large cell/scaffold composite constructs. Tissue Eng. 2006; 12(7): 1851-63.
  96. Perea H., Aigner J., Hopfner U. et al. Direct magnetic tubular cell seeding: a novel approach for vascular tissue engineering. Cells Tissues Organs 2006; 183(3): 156-65.
  97. Tiwari A., Punshon G., Kidane A. et al. Magnetic beads tDynabead) toxicity to endothelial cells at high bead concentration: implication for tissue engineering of vascular prosthesis. Cell Biol. Toxicol. 2003; 19(5): 265-72.
  98. Gonzalez-Molina J., Riegler J., Southern P. et al. Rapid magnetic cell delivery for large tubular bioengineered constructs. J. R. Soc. Interface 2012; 9(76): 3008-16.
  99. Ito A., Ino K., Hayashida M. et al. Novel methodology for fabrication of tissue-engineered tubular constructs using magnetite nanoparticles and magnetic force. Tissue Eng. 2005; 11(9-10): 1553-61.
  100. Soletti L., Nieponice A., Guan J. et al. A seeding device for tissue engineered tubular structures. Biomaterials 2006; 27(28): 4863-70.
  101. Nieponice A., Vorp D.A., Soletti L. Vacuum rotational seeding and loading device and method for same. US patent 20060075963. 2006.
  102. Nguyen K.T., West J.L. Photopolymerizable hydrogels for tissue engineering applications. Biomaterials 2002; 23(22): 4307-14.
  103. Mann B.K., Gobin A.S., Tsai A.T. et al. Smooth muscle cell growth in photopolymerized hydrogels with cell adhesive and proteolytically degradable domains: synthetic ECM analogs for tissue engineering. Biomaterials 2001; 22(22): 3045-51.
  104. Schmedlen R.H., Elbjeirami W.M., Gobin A.S. et al. Tissue engineered small-diameter vascular grafts. Clin. Plast. Surg. 2003; 30(4): 507-17.
  105. L'Heureux N., Paquet S., Labbe R. et al. A completely biological tissue-engineered human blood vessel. FASEB J. 1998; 12(1): 47-56.
  106. L'Heureux N., McAllister T.N., de la Fuente L.M. Tissue-engineered blood vessel for adult arterial revascularization. N. Engl. J. Med. 2007; 357(14): 1451-3.
  107. L'Heureux N., Germain L., Labbe R. et al. In vitro construction of a human blood vessel from cultured vascular cells: a morphologic study. J. Vasc. Surg. 1993; 17(3): 499-509.
  108. Topper J.N., Gimbrone M.A. Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol. Med. Today. 1999; 5(1): 40-6.
  109. Resnick N., Yahav H., Shay-Salit A. et al. Fluid shear stress and the vascular endothelium: for better and for worse. Prog. Biophys. Mol. Biol. 2003; 81(3): 177-99.
  110. Kalmykova N.V., Cherepanova O.A., Gorelik I.V.et al. Various effects of laminin-1 and laminin-2/4 on adhesion and migration of cultured human keratinocytes. Tsitologiia 2002;44(8):792-8.
  111. Iudintseva N.M., Blinova M.I., Pinaev G.P.Characteristics of cytoskeleton organization of human normal postnatal, scar and embryonic skin fibroblasts spreading on different proteins of extracellular matrix. Tsitologiia2008;50(10):861-7.
  112. Sedov V.M., Andreev D.I., Semenova E.G. et al. Endothelialvascular grafts (experimental research). Angiol. Sosud. Khir.2004;10(2):111-7.
  113. Шевченко Ю.Л., Матвеев С.А. Клеточные технологии в сердечно-сосудистой хирургии. М.: Наука; 2005.

Copyright (c) 2014 Eco-Vector

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: ПИ № ФС 77 - 57156 от 11.03.2014.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies