Tailoring the Foreign Body Response for In Situ Vascular Tissue Engineering
Publication: Tissue Engineering Part C: Methods
Volume 21, Issue Number 5
Abstract
This study describes a screening platform for a guided in situ vascular tissue engineering approach. Polymer rods were developed that upon 3 weeks of subcutaneous implantation evoke a controlled inflammatory response culminating in encapsulation by a tube-shaped autologous fibrocellular tissue capsule, which can form a basis for a tissue-engineered blood vessel. Rods of co-polymer were produced using different ratios of poly(ethylene oxide terephthalate) and poly(butylene terephthalate) to create a range of physicochemical properties. In addition, a set of different physical, chemical, and biological surface modifications were tested on their ability to actively steer this tissue capsule formation using a rat model as testing platform. Tissue capsules were mainly composed of circumferentially aligned collagen and myofibroblasts. Different implant material resulted in distinct differences in tissue capsule formation. Compared to its unmodified counterparts, all surface modifications resulted in increased wall thickness, collagen, and myofibroblasts. Oxygen plasma-treated rods resulted in loose tissue arrangement, collagen, and collagen/TGF-β-coated rods yielded thick, collagen-rich, densely packed tissue capsules, though with a random distribution of myofibroblasts. In contrast, chloroform-etched rods provided homogenous densely packed tissue capsules, completely populated by myofibroblasts. In conclusion, by varying the implant's surface characteristics, tissue capsule composition, cell distribution, and tissue arrangement could be tailored, enabling controlled guidance of the tissue response for in vivo vascular tissue engineering.
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References
1.
McKee J.A., Banik S.S., Boyer M.J., et al. Human arteries engineered in vitro. EMBO Rep 4, 633, 2003.
2.
Sayers R.D., Raptis S., Berce M., and Miller J.H. Long-term results of femorotibial bypass with vein or polytetrafluoroethylene. Br J Surg 85, 934, 1998.
3.
Kaufman J.L., Garb J.L., Berman J.A., et al. A prospective comparison of two expanded polytetrafluoroethylene grafts for linear forearm hemodialysis access: does the manufacturer matter? J Am Coll Surg 185, 74, 1997.
4.
Tordoir J., Canaud B., Haage P., et al. EBPG on vascular access. Nephrol Dial Transplant 22 Suppl 2, ii88, 2007.
5.
Vascular Access 2006 Work Group. Clinical practice guidelines for vascular access. Am J Kidney Dis 48 Suppl 1, S176, 2006.
6.
Roy-Chaudhury P., El-Khatib M., Campos-Naciff B., et al. Back to the future: how biology and technology could change the role of PTFE grafts in vascular access management. Semin Dial 25, 495, 2012.
7.
Rotmans J.I., Pasterkamp G., Verhagen H.J., et al. Hemodialysis access graft failure: time to revisit an unmet clinical need? J Nephrol 18, 9, 2005.
8.
Roy-Chaudhury P., Kelly B.S., Miller M.A., et al. Venous neointimal hyperplasia in polytetrafluoroethylene dialysis grafts. Kidney Int 59, 2325, 2001.
9.
Friedl R., Li J., Schumacher B., et al. Intimal hyperplasia and expression of transforming growth factor-beta1 in saphenous veins and internal mammary arteries before coronary artery surgery. Ann Thorac Surg 78, 1312, 2004.
10.
Lee T., Chauhan V., Krishnamoorthy M., et al. Severe venous neointimal hyperplasia prior to dialysis access surgery. Nephrol Dial Transplant 26, 2264, 2011.
11.
Weinberg C.B., and Bell E. A blood vessel model constructed from collagen and cultured vascular cells. Science 231, 397, 1986.
12.
Rotmans J.I., Heyligers J.M., Verhagen H.J., et al. In vivo cell seeding with anti-CD34 antibodies successfully accelerates endothelialization but stimulates intimal hyperplasia in porcine arteriovenous expanded polytetrafluoroethylene grafts. Circulation 112, 12, 2005.
13.
McAllister T.N., Maruszewski M., Garrido S.A., et al. Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study. Lancet 373, 1440, 2009.
14.
Dahl S.L., Kypson A.P., Lawson J.H., et al. Readily available tissue-engineered vascular grafts. Sci Transl Med 3, 68ra9, 2011.
15.
Wu W., Allen R.A., and Wang Y. Fast-degrading elastomer enables rapid remodeling of a cell-free synthetic graft into a neoartery. Nat Med 18, 1148, 2012.
16.
Campbell J.H., Efendy J.L., and Campbell G.R. Novel vascular graft grown within recipient's own peritoneal cavity. Circ Res 85, 1173, 1999.
17.
Sparks C.H. Autogenous grafts made to order. Ann Thorac Surg 8, 104, 1969.
18.
Yamanami M., Ishibashi-Ueda H., Yamamoto A., et al. Implantation study of small-caliber “biotube” vascular grafts in a rat model. J Artif Organs 16, 59, 2013.
19.
Chen S., Jones J.A., Xu Y., et al. Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 31, 3479, 2010.
20.
Brodbeck W.G., Voskerician G., Ziats N.P., et al. In vivo leukocyte cytokine mRNA responses to biomaterials are dependent on surface chemistry. J Biomed Mater Res A 64, 320, 2003.
21.
Thevenot P., Hu W., and Tang L. Surface chemistry influences implant biocompatibility. Curr Top Med Chem 8, 270, 2008.
22.
Bota P.C., Collie A.M., Puolakkainen P., et al. Biomaterial topography alters healing in vivo and monocyte/macrophage activation in vitro. J Biomed Mater Res A 95, 649, 2010.
23.
Lee J.H., Khang G., Lee J.W., and Lee H.B. Interaction of different types of cells on polymer surfaces with wettability gradient. J Colloid Interface Sci 205, 323, 1998.
24.
Deschamps A.A., Claase M.B., Sleijster W.J., et al. Design of segmented poly(ether ester) materials and structures for the tissue engineering of bone. J Control Release 78, 175, 2002.
25.
Mahmood T.A., de Jong R., Riesle J., et al. Adhesion-mediated signal transduction in human articular chondrocytes: the influence of biomaterial chemistry and tenascin-C. Exp Cell Res 301, 179, 2004.
26.
Kumar G., Waters M.S., Farooque T.M., et al. Freeform fabricated scaffolds with roughened struts that enhance both stem cell proliferation and differentiation by controlling cell shape. Biomaterials 33, 4022, 2012.
27.
Gao J., Niklason L., and Langer R. Surface hydrolysis of poly(glycolic acid) meshes increases the seeding density of vascular smooth muscle cells. J Biomed Mater Res 42, 417, 1998.
28.
Liu W., Zhan J., Su Y., et al. Effects of plasma treatment to nanofibers on initial cell adhesion and cell morphology. Colloids Surf B Biointerfaces 113C, 101, 2013.
29.
Ramires P.A., Mirenghi L., Romano A.R., et al. Plasma-treated PET surfaces improve the biocompatibility of human endothelial cells. J Biomed Mater Res 51, 535, 2000.
30.
Olde Riekerink M.B., Claase M.B., Engbers G.H., et al. Gas plasma etching of PEO/PBT segmented block copolymer films. J Biomed Mater Res A 65, 417, 2003.
31.
Li A.G., Quinn M.J., Siddiqui Y., et al. Elevation of transforming growth factor beta (TGFbeta) and its downstream mediators in subcutaneous foreign body capsule tissue. J Biomed Mater Res A 82, 498, 2007.
32.
Tomasek J.J., Gabbiani G., Hinz B., et al. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3, 349, 2002.
33.
Moroni L., de Wijn J.R., and van Blitterswijk C.A. 3D fiber-deposited scaffolds for tissue engineering: influence of pores geometry and architecture on dynamic mechanical properties. Biomaterials 27, 974, 2006.
34.
Roy-Chaudhury P, Arend L., Zhang J., et al. Neointimal hyperplasia in early arteriovenous fistula failure. Am J Kidney Dis 50, 782, 2007.
35.
Anderson J.M., Rodriguez A., and Chang D.T. Foreign body reaction to biomaterials. Semin Immunol 20, 86, 2008.
36.
Onuki Y., Bhardwaj U., Papadimitrakopoulos F., and Burgess D.J. A review of the biocompatibility of implantable devices: current challenges to overcome foreign body response. J Diabetes Sci Technol 2, 1003, 2008.
37.
Ratner B.D. Reducing capsular thickness and enhancing angiogenesis around implant drug release systems. J Control Release 78, 211, 2002.
38.
Le S.J., Gongora M., Zhang B., et al. Gene expression profile of the fibrotic response in the peritoneal cavity. Differentiation 79, 232, 2010.
39.
Claase M.B., Olde Riekerink M.B., de Bruijn J.D., et al. Enhanced bone marrow stromal cell adhesion and growth on segmented poly(ether ester)s based on poly(ethylene oxide) and poly(butylene terephthalate). Biomacromolecules 4, 57, 2003.
40.
Barth K.A., Waterfield J.D., and Brunette D.M. The effect of surface roughness on RAW 264.7 macrophage phenotype. J Biomed Mater Res A 101, 2679, 2013.
41.
Refai A.K., Textor M., Brunette D.M., and Waterfield J.D. Effect of titanium surface topography on macrophage activation and secretion of proinflammatory cytokines and chemokines. J Biomed Mater Res A 70, 194, 2004.
42.
Nandakumar A., Tahmasebi B.Z., Santos D., et al. Surface modification of electrospun fibre meshes by oxygen plasma for bone regeneration. Biofabrication 5, 015006, 2013.
43.
Waser-Althaus J., Salamon A., Waser M., et al. Differentiation of human mesenchymal stem cells on plasma-treated polyetheretherketone. J Mater Sci Mater Med 25, 515, 2014.
44.
Buitinga M., Truckenmuller R., Engelse M.A., et al. Microwell scaffolds for the extrahepatic transplantation of islets of langerhans. PLoS One 8, e64772, 2013.
45.
Papenburg B.J., Vogelaar L., Bolhuis-Versteeg L.A., et al. One-step fabrication of porous micropatterned scaffolds to control cell behavior. Biomaterials 28, 1998, 2007.
46.
Berry C.C., Campbell G., Spadiccino A., et al. The influence of microscale topography on fibroblast attachment and motility. Biomaterials 25, 5781, 2004.
47.
Biela S.A., Su Y., Spatz J.P., and Kemkemer R. Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. Acta Biomater 5, 2460, 2009.
48.
Eckes B., Zigrino P., Kessler D., et al. Fibroblast-matrix interactions in wound healing and fibrosis. Matrix Biol 19, 325, 2000.
49.
Siniscalchi R.T., Melo M., Palma P.C., et al. Highly purified collagen coating enhances tissue adherence and integration properties of monofilament polypropylene meshes. Int Urogynecol J 24, 1747, 2013.
50.
Nagai M., Hayakawa T., Fukatsu A., et al. In vitro study of collagen coating of titanium implants for initial cell attachment. Dent Mater J 21, 250, 2002.
51.
Barrientos S., Stojadinovic O., Golinko M.S., et al. Growth factors and cytokines in wound healing. Wound Repair Regen 16, 585, 2008.
52.
Zioncheck T.F., Chen S.A., Richardson L., et al. Pharmacokinetics and tissue distribution of recombinant human transforming growth factor beta 1 after topical and intravenous administration in male rats. Pharm Res 11, 213, 1994.
53.
Sparks C.H. Die-grown reinforced arterial grafts: observations on long-term animal grafts and clinical experience. Ann Surg 172, 787, 1970.
54.
Sparks C.H. Silicone mandril method for growing reinforced autogenous femoro-popliteal artery grafts in situ. Ann Surg 177, 293, 1973.
55.
Hallin R.W. Complications with the mandril-grown (Sparks) dacron arterial graft. Am Surg 41, 550, 1975.
56.
Hallin R.W., and Sweetman W.R. The Sparks' mandril graft. A seven year follow-up of mandril grafts placed by Charles H. Sparks and his associates. Am J Surg 132, 221, 1976.
57.
Roberts P.N., and Hopkinson B.R. The Sparks mandril in femoropopliteal bypass. Br Med J 2, 1190, 1977.
58.
Guidoin R., Thevenet A., Noel H.P., et al. [The Sparks-Mandril arterial prosthesis. An ingenious concept, a total failure. What can we learn from it?]. J Mal Vasc 9, 277, 1984.
59.
Chue W.L., Campbell G.R., Caplice N., et al. Dog peritoneal and pleural cavities as bioreactors to grow autologous vascular grafts. J Vasc Surg 39, 859, 2004.
60.
Watanabe T., Kanda K., Yamanami M., et al. Long-term animal implantation study of biotube-autologous small-caliber vascular graft fabricated by in-body tissue architecture. J Biomed Mater Res B Appl Biomater 98, 120, 2011.
61.
Almine J.F., Wise S.G., and Weiss A.S. Elastin signaling in wound repair. Birth Defects Res C Embryo Today 96, 248, 2012.
62.
Leung D.Y., Glagov S., and Mathews M.B. Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. Science 191, 475, 1976.
63.
Ben D.A., Benessiano J., Poitevin P., et al. Arterial expansive remodeling induced by high flow rates. Am J Physiol 272, H851, 1997.
64.
Efendy J.L., Campbell G.R., and Campbell J.H. The effect of environmental cues on the differentiation of myofibroblasts in peritoneal granulation tissue. J Pathol 192, 257, 2000.
65.
Roubos N., Rosenfeldt F.L., Richards S.M., et al. Improved preservation of saphenous vein grafts by the use of glyceryl trinitrate-verapamil solution during harvesting. Circulation 92, II31, 1995.
66.
Pektok E., Nottelet B., Tille J.C., et al. Degradation and healing characteristics of small-diameter poly(epsilon-caprolactone) vascular grafts in the rat systemic arterial circulation. Circulation 118, 2563, 2008.
67.
de V.S., Tille J.C., Mugnai D., et al. Long term performance of polycaprolactone vascular grafts in a rat abdominal aorta replacement model. Biomaterials 33, 38, 2012.
68.
Koschwanez H.E., Yap F.Y., Klitzman B., and Reichert W.M. In vitro and in vivo characterization of porous poly-L-lactic acid coatings for subcutaneously implanted glucose sensors. J Biomed Mater Res A 87, 792, 2008.
69.
Browning M.B., Cereceres S.N., Luong P.T., and Cosgriff-Hernandez E.M. Determination of the in vivo degradation mechanism of PEGDA hydrogels. J Biomed Mater Res A 102, 4244, 2014.
70.
Mang A., Pill J., Gretz N., et al. Biocompatibility of an electrochemical sensor for continuous glucose monitoring in subcutaneous tissue. Diabetes Technol Ther 7, 163, 2005.
Information & Authors
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Published In

Tissue Engineering Part C: Methods
Volume 21 • Issue Number 5 • May 2015
Pages: 436 - 446
PubMed: 25336286
Copyright
Copyright 2015, Mary Ann Liebert, Inc.
History
Published in print: May 2015
Published ahead of print: 1 December 2014
Published online: 25 November 2014
Published ahead of production: 22 October 2014
Accepted: 25 September 2014
Received: 7 May 2014
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All the authors declare no competing financial interests.
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