Nerve regeneration and elastin formation within poly(glycerol sebacate)-based synthetic arterial grafts one-year post-implantation in a rat model

Biomaterials

Volumn 35, Issue 1, 2014, Pages 165-173

  Allen, Robert A ^a   Wu, Wei ^a,e   Yao, Mingyi ^b,f   Dutta, Debaditya ^c   Duan, Xinjie ^a   Bachman, Timothy N ^b   Champion, Hunter C ^b,c,d   Stolz, Donna B ^b,d   Robertson, Anne M ^a,b   Kim, Kang ^a,b,c   Isenberg, Jeffrey S ^b,d   Wang, Yadong ^a,b  

^a University of Pittsburgh   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e YALE UNIVERSITY   (United States)

^f MIDWESTERN UNIVERSITY   (United States)

Author keywords

Degradation; Elastin; Elastomer; Nerve; Vascular grafts

Indexed keywords

DYNAMIC MECHANICAL; LONG TERM PERFORMANCE; MATRIX ORGANIZATIONS; NERVE; NERVE REGENERATION; POLIES (GLYCEROLSEBACATE); POLY(GLYCEROL SEBACATE); VASCULAR GRAFTS;

BIOMINERALIZATION; DEGRADATION; ELASTOMERS; GLYCEROL; GLYCOPROTEINS; GRAFTS; POLYCAPROLACTONE; RATS;

ELASTIN;

ACETYLCHOLINE; CD31 ANTIGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; ELASTIN; FIBRILLIN 1; FORSKOLIN; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN 11; NANOFIBER; NITROPRUSSIDE SODIUM; PHENYLEPHRINE; POLYMER; SEROTONIN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ABDOMINAL AORTA; ADVENTITIA; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY GRAFT; ARTICLE; BLOOD VESSEL CALCIFICATION; BLOOD VESSEL OCCLUSION; CELL STRUCTURE; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; GENE PRODUCT; IMPEDANCE; MACROPHAGE; MYOGRAPHY; NEOARTERY; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; VASODILATATION;

RATTUS;

DEGRADATION; ELASTIN; ELASTOMER; NERVE; VASCULAR GRAFTS;

ANIMALS; BLOOD VESSEL PROSTHESIS; DECANOATES; ELASTIN; GLYCEROL; MALE; MICROSCOPY, FLUORESCENCE; MODELS, ANIMAL; NERVE REGENERATION; POLYMERS; RATS; RATS, INBRED LEW; VASOCONSTRICTION; VASODILATION;

EID: 84887026451     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.09.081     Document Type: Article

References (51)

1. Edelman E.R. Vascular tissue engineering: designer arteries. Circ Res 1999, 85:1115-1117.
2. Wang X., Lin P., Yao Q., Chen C. Development of small-diameter vascular grafts. World J Surg 2007, 31:682-689.
3. Kannan R.Y., Salacinski H.J., Butler P.E., Hamilton G., Seifalian A.M. Current status of prosthetic bypass grafts: a review. JBiomed Mater Res B Appl Biomater 2005, 74:570-581.
4. L'Heureux N., Paquet S., Labbe R., Germain L., Auger F.A. Acompletely biological tissue-engineered human blood vessel. FASEB J 1998, 12:47-56.
5. Niklason L.E., Gao J., Abbott W.M., Hirschi K.K., Houser S., Marini R., et al. Functional arteries grown invitro. Science 1999, 284:489-493.
6. He H., Matsuda T. Newly designed compliant hierarchic hybrid vascular graft wrapped with microprocessed elastomeric film-II: Morphogenesis and compliance change upon implantation. Cell Transplant 2002, 11:75-87.
7. Swartz D.D., Russell J.A., Andreadis S.T. Engineering of fibrin-based functional and implantable small-diameter blood vessels. Am J Physiol Heart Circ Physiol 2005, 288:H1451-H1460.
8. Hoerstrup S.P., Cummings Mrcs I., Lachat M., Schoen F.J., Jenni R., Leschka S., et al. Functional growth in tissue-engineered living, vascular grafts: follow-up at 100 weeks in a large animal model. Circulation 2006, 114:I159-I166.
9. L'Heureux N., Dusserre N., Konig G., Victor B., Keire P., Wight T.N., et al. Human tissue-engineered blood vessels for adult arterial revascularization. Nat Med 2006, 12:361-365.
10. Yang D., Guo T., Nie C., Morris S.F. Tissue-engineered blood vessel graft produced by self-derived cells and allogenic acellular matrix: a functional performance and histologic study. Ann Plast Surg 2009, 62:297-303.
11. Koch S., Flanagan T.C., Sachweh J.S., Tanios F., Schnoering H., Deichmann T., et al. Fibrin-polylactide-based tissue-engineered vascular graft in the arterial circulation. Biomaterials 2010, 31:4731-4739.
12. Neff L.P., Tillman B.W., Yazdani S.K., Machingal M.A., Yoo J.J., Soker S., et al. Vascular smooth muscle enhances functionality of tissue-engineered blood vessels invivo. JVasc Surg 2011, 53:426-434.
13. McAllister T.N., Maruszewski M., Garrido S.A., Wystrychowski W., Dusserre N., Marini A., et al. Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study. Lancet 2009, 373:1440-1446.
14. Quint C., Kondo Y., Manson R.J., Lawson J.H., Dardik A., Niklason L.E. Decellularized tissue-engineered blood vessel as an arterial conduit. Proc Natl Acad Sci USA 2011, 108:9214-9219.
15. Dahl S.L., Kypson A.P., Lawson J.H., Blum J.L., Strader J.T., Li Y., et al. Readily available tissue-engineered vascular grafts. Sci Transl Med 2011, 3:68ra9.
16. Wystrychowski W., Cierpka L., Zagalski K., Garrido S., Dusserre N., Radochonski S., et al. Case study: first implantation of a frozen, devitalized tissue-engineered vascular graft for urgent hemodialysis access. JVasc Access 2011, 12:67-70.
17. Shinoka T., Shum-Tim D., Ma P.X., Tanel R.E., Isogai N., Langer R., et al. Creation of viable pulmonary artery autografts through tissue engineering. JThorac Cardiovasc Surg 1998, 115:536-545. [discussion 45-6].
18. Cho S.W., Lim S.H., Kim I.K., Hong Y.S., Kim S.S., Yoo K.J., et al. Small-diameter blood vessels engineered with bone marrow-derived cells. Ann Surg 2005, 241:506-515.
19. Soletti L., Nieponice A., Guan J., Stankus J.J., Wagner W.R., Vorp D.A. Aseeding device for tissue engineered tubular structures. Biomaterials 2006, 27:4863-4870.
20. Hashi C.K., Zhu Y., Yang G.Y., Young W.L., Hsiao B.S., Wang K., et al. Antithrombogenic property of bone marrow mesenchymal stem cells in nanofibrous vascular grafts. Proc Natl Acad Sci USA 2007, 104:11915-11920.
21. Nelson G.N., Mirensky T., Brennan M.P., Roh J.D., Yi T., Wang Y., et al. Functional small-diameter human tissue-engineered arterial grafts in an immunodeficient mouse model: preliminary findings. Arch Surg 2008, 143:488-494.
22. Brennan M.P., Dardik A., Hibino N., Roh J.D., Nelson G.N., Papademitris X., et al. Tissue-engineered vascular grafts demonstrate evidence of growth and development when implanted in a juvenile animal model. Ann Surg 2008, 248:370-377.
23. Mirensky T.L., Nelson G.N., Brennan M.P., Roh J.D., Hibino N., Yi T., et al. Tissue-engineered arterial grafts: long-term results after implantation in a small animal model. JPediatr Surg 2009, 44:1127-1132. [discussion 32-3].
24. Zhao Y., Zhang S., Zhou J., Wang J., Zhen M., Liu Y., et al. The development of a tissue-engineered artery using decellularized scaffold and autologous ovine mesenchymal stem cells. Biomaterials 2010, 31:296-307.
25. Mirensky T.L., Hibino N., Sawh-Martinez R.F., Yi T., Villalona G., Shinoka T., et al. Tissue-engineered vascular grafts: does cell seeding matter?. JPediatr Surg 2010, 45:1299-1305.
26. Roh J.D., Sawh-Martinez R., Brennan M.P., Jay S.M., Devine L., Rao D.A., et al. Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc Natl Acad Sci USA 2010, 107:4669-4674.
27. Nieponice A., Soletti L., Guan J., Hong Y., Gharaibeh B., Maul T.M., et al. Invivo assessment of a tissue-engineered vascular graft combining a biodegradable elastomeric scaffold and muscle-derived stem cells in a rat model. Tissue Eng Part A 2010, 16:1215-1223.
28. He W., Nieponice A., Soletti L., Hong Y., Gharaibeh B., Crisan M., et al. Pericyte-based human tissue engineered vascular grafts. Biomaterials 2010, 31:8235-8244.
29. Watanabe M., Shin'oka T., Tohyama S., Hibino N., Konuma T., Matsumura G., et al. Tissue-engineered vascular autograft: inferior vena cava replacement in a dog model. Tissue Eng 2001, 7:429-439.
30. Zhou M., Liu Z., Liu C., Jiang X., Wei Z., Qiao W., et al. Tissue engineering of small-diameter vascular grafts by endothelial progenitor cells seeding heparin-coated decellularized scaffolds. JBiomed Mater Res B Appl Biomater 2012, 100:111-120.
31. Shin'oka T., Imai Y., Ikada Y. Transplantation of a tissue-engineered pulmonary artery. NEngl J Med 2001, 344:532-533.
32. Hibino N., McGillicuddy E., Matsumura G., Ichihara Y., Naito Y., Breuer C., et al. Late-term results of tissue-engineered vascular grafts in humans. JThorac Cardiovasc Surg 2010, 139:431-436. 6 e1-2.
33. Wu W., Allen R.A., Wang Y. Fast-degrading elastomer enables rapid remodeling of a cell-free synthetic graft into a neoartery. Nat Med 2012, 18:1148-1153.
34. Sandusky G.E., Badylak S.F., Morff R.J., Johnson W.D., Lantz G. Histologic findings after invivo placement of small intestine submucosal vascular grafts and saphenous vein grafts in the carotid artery in dogs. Am J Pathol 1992, 140:317-324.
35. Lepidi S., Abatangelo G., Vindigni V., Deriu G.P., Zavan B., Tonello C., et al. Invivo regeneration of small-diameter (2 mm) arteries using a polymer scaffold. FASEB J 2006, 20:103-105.
36. Yokota T., Ichikawa H., Matsumiya G., Kuratani T., Sakaguchi T., Iwai S., et al. In situ tissue regeneration using a novel tissue-engineered, small-caliber vascular graft without cell seeding. JThorac Cardiovasc Surg 2008, 136:900-907.
37. Zavan B., Vindigni V., Lepidi S., Iacopetti I., Avruscio G., Abatangelo G., et al. Neoarteries grown invivo using a tissue-engineered hyaluronan-based scaffold. FASEB J 2008, 22:2853-2861.
38. Enomoto S., Sumi M., Kajimoto K., Nakazawa Y., Takahashi R., Takabayashi C., et al. Long-term patency of small-diameter vascular graft made from fibroin, a silk-based biodegradable material. JVasc Surg 2010, 51:155-164.
39. Hashi C.K., Derugin N., Janairo R.R., Lee R., Schultz D., Lotz J., et al. Antithrombogenic modification of small-diameter microfibrous vascular grafts. Arterioscler Thromb Vasc Biol 2010, 30:1621-1627.
40. Soletti L., Nieponice A., Hong Y., Ye S.H., Stankus J.J., Wagner W.R., et al. Invivo performance of a phospholipid-coated bioerodable elastomeric graft for small-diameter vascular applications. JBiomed Mater Res A 2011, 96:436-448.
41. de Valence S., Tille J.C., Mugnai D., Mrowczynski W., Gurny R., Moller M., et al. Long term performance of polycaprolactone vascular grafts in a rat abdominal aorta replacement model. Biomaterials 2012, 33:38-47.
42. Gao J., Crapo P.M., Wang Y. Macroporous elastomeric scaffolds with extensive micropores for soft tissue engineering. Tissue Eng 2006, 12:917-925.
43. Bauer E.M., Qin Y., Miller T.W., Bandle R.W., Csanyi G., Pagano P.J., et al. Thrombospondin-1 supports blood pressure by limiting eNOS activation and endothelial-dependent vasorelaxation. Cardiovasc Res 2010, 88:471-481.
44. Hill M.R., Duan X., Gibson G.A., Watkins S., Robertson A.M. Atheoretical and non-destructive experimental approach for direct inclusion of measured collagen orientation and recruitment into mechanical models of the artery wall. JBiomech 2012, 45:762-771.
45. Li L., Terry C.M., Shiu Y.T., Cheung A.K. Neointimal hyperplasia associated with synthetic hemodialysis grafts. Kidney Int 2008, 74:1247-1261.
46. Mendelson K., Schoen F. Heart valve tissue engineering: concepts, approaches, progress, and challenges. Ann Biomed Eng 2006, 34:1799-1819.
47. Huynh T., Abraham G., Murray J., Brockbank K., Hagen P.O., Sullivan S. Remodeling of an acellular collagen graft into a physiologically responsive neovessel. Nat Biotechnol 1999, 17:1083-1086.
48. Torikai K., Ichikawa H., Hirakawa K., Matsumiya G., Kuratani T., Iwai S., et al. Aself-renewing, tissue-engineered vascular graft for arterial reconstruction. JThorac Cardiovasc Surg 2008, 136:37-45. e1.
49. Jones E.A., le Noble F., Eichmann A. What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology 2006, 21:388-395.
50. Bull D.A., Hunter G.C., Holubec H., Aguirre M.L., Rappaport W.D., Putnam C.W. Cellular origin and rate of endothelial cell coverage of PTFE grafts. JSurg Res 1995, 58:58-68.
51. Zilla P., Bezuidenhout D., Human P. Prosthetic vascular grafts: wrong models, wrong questions and no healing. Biomaterials 2007, 28:5009-5027.