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Thromb Haemost 1997; 78(05): 1392-1398
DOI: 10.1055/s-0038-1665417
Review Article
Schattauer GmbH Stuttgart

Naturally Produced Extracellular Matrix Is an Excellent Substrate for Canine Endothelial Cell Proliferation and Resistance to Shear Stress on PTFE Vascular Grafts

A Schneider
1   The Joseph Lunenfeld Cardiac Surgery Research Center, Oncology Dept. Haifa, Israel
,
M Chandra
1   The Joseph Lunenfeld Cardiac Surgery Research Center, Oncology Dept. Haifa, Israel
,
G Lazarovici
1   The Joseph Lunenfeld Cardiac Surgery Research Center, Oncology Dept. Haifa, Israel
,
I Vlodavsky
2   Hadassah University Hospital, Hebrew University Hadassah Medical School, Jerusalem and Cardiothoracic Surgery Dept. Haifa, Israel
,
G Merin
1   The Joseph Lunenfeld Cardiac Surgery Research Center, Oncology Dept. Haifa, Israel
,
G Uretzky
3   Carmel Medical Center, Technion-lsrael Institute of Technology, Haifa, Israel
,
J B Borman
1   The Joseph Lunenfeld Cardiac Surgery Research Center, Oncology Dept. Haifa, Israel
,
H Schwalb
1   The Joseph Lunenfeld Cardiac Surgery Research Center, Oncology Dept. Haifa, Israel
› Author Affiliations
Further Information

Publication History

Received 07 1997

Accepted after resubmission 07 July 1997

Publication Date:
12 July 2018 (online)

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Summary

Purpose: Successful development of a vascular prosthesis lined with endothelial cells (EC) may depend on the ability of the attached cells to resist shear forces after implantation. The present study was designed to investigate EC detachment from extracellular matrix (ECM) precoated vascular prostheses, caused by shear stress in vitro and to test the performance of these grafts in vivo. Methods: Bovine aortic endothelial cells were seeded inside untreated polytetrafluoro-ethylene (PTFE) vascular graft (10 X 0.6 cm), PTFE graft precoated with fibronectin (FN), or PTFE precoated with FN and a naturally produced ECM (106 cells/graft). Sixteen hours after seeding the medium was replaced and unattached cells counted. The strength of endothelial cell attachment was evaluated by subjecting the grafts to a physiologic shear stress of 15 dynes/cm2 for 1 h. The detached cells were collected and quantitated. PTFE or EC preseeded ECM coated grafts were implanted in the common carotid arteries of dogs. Results: While little or no differences were found in the extent of endothelial cell attachment to the various grafts (79%, 87% and 94% of the cells attached to PTFE, FN precoated PTFE, or FN+ECM precoated PTFE, respectively), the number of cells retained after a shear stress was significanly increased on ECM coated PTFE (20%, 54% and 85% on PTFE, FN coated PTFE, and FN+ECM coated PTFE, respectively, p <0.01). Implantation experiments in dogs revealed a significant increase in EC coverage and a reduced incidence of thrombus formation on ECM coated grafts that were seeded with autologous saphenous vein endothelial cells prior to implantation. Conclusion: ECM coating significantly increased the strength of endothelial cell attachment to vascular prostheses subjected to shear stress. The presence of adhesive macromolecules and potent endothelial cell growth promoting factors may render the ECM a promising substrate for vascular prostheses.

 

  • References

  • 1 Schneider A, Melmed RN, Schwalb H, Karck M, Vlodavsky I, Uretzky G. An improved method for endothelial cell seeding on PTFE small caliber vascular grafts. J Vase Sug 1992; 15: 649-656
    PubMedGoogle Scholar
  • 2 Schneider A, Schwalb H, Vlodavsky I, Uretzky G. An improved method of endothelial seeding on small caliber prosthetic vascular grafts coated with natural extracellular matrix. Clinical Materials 1993; 13: 51-55
    CrossrefPubMedGoogle Scholar
  • 3 Schneider PA, Kotze HF, Du PHeynsA, Hanson SR. Thromboembolic potential of synthetic vascular grafts in baboons. J Vase Surg 1989; 10: 75-82
    CrossrefPubMedGoogle Scholar
  • 4 Szilagyi DE. Vascular substitutes 1981. Achievements, disappointment, prospects. J Cardiovasc Surg (Torino) 1982; 23: 183-193
    PubMedGoogle Scholar
  • 5 Stanley JC, Burkel WE, Ford JW, Vinter DW, Kahn RH, Whitehouse Jr WM, Graham LM. Enhanced patency of small-diameter, externally supported Dacron iliofemoral grafts seeded with endothelial cells. Surgery 1982; 92: 994-1005
    PubMedGoogle Scholar
  • 6 Allen BT, Long JA, Clark RE, Sicard GA, Hopkins KT, Welch MJ. Influence of endothelial cell seeding on platelet deposition and patency in small diameter Dacron arterial grafts. J Vase Surg 1984; 1: 224-233
    CrossrefPubMedGoogle Scholar
  • 7 Belden T, Schmidt S, Falkow L, Sharp W. Endothelial cell seeding of small diameter vascular grafts. Trans Am Soc Artif Intern Organs 1982; 28: 173-177
    PubMedGoogle Scholar
  • 8 Schmidt SP, Hunter TJ, Sharp WV, Malindzak GS, Evancho MM. Endothelial cell-seeded four-millimeter Dacron vascular grafts: Effects of blood flow manipulation through the grafts. J Vase Surg 1984; 01: 434-441
    PubMedGoogle Scholar
  • 9 Rosenman JE, Kempczinski RF, Pearce WH, Silberstein EB. Kinetics of endothelial cell seeding. J Vase Surg 1985; 2: 778-784
    CrossrefPubMedGoogle Scholar
  • 10 Zilla P, Fasol R, Deutsch M, Fischlein T, Minar E, Hammerle A, Krupicka O, Kadletz M. Endothelial cell seeding of polytetrafluoroethylene vascular grafts in humans: preliminary report. J Vase Surg 1987; 6: 535-541
    CrossrefPubMedGoogle Scholar
  • 11 Walker MG, Thomson GJL, Shaw JW. Endothelial cell seeded versus nonseeded ePTFE grafts in patients with severe peripheral vascular disease. In: Endothelialization of Vascular Grafts. Zilla P, Fasol R, Deutsch M. (eds) Karger: 1987: 245-248
    Google Scholar
  • 12 Fasol R, Zilla P, Deutsch M, Grimm M, Fischlein T, Lautle G. Human endothelial cell seeding: evaluation of its effectiveness by platelet parameters after one year. J Vase Surg 1989; 9: 432-436
    CrossrefPubMedGoogle Scholar
  • 13 Herring MB, Gardner A, Glover J. Seeding human arterial prostheses with mechanically derived endothelium: the detrimental effect of smoking. J Vase Surg 1984; 1: 279-289
    CrossrefPubMedGoogle Scholar
  • 14 Herring MB, Compton RS, Gardner AL, LeGrand DR. Clinical experience with endothelial seeding in Indianapolis. In: Endothelialization of Vascular Grafts. Zilla P, Fasol R, Deutsch M. (eds) Karger: 1987: 218-224
    Google Scholar
  • 15 Herring MB, Baughman MS, Glover J. Endothelium develops on seeded human arterial prostheses: a brief clinical note. J Vase Surg 1985; 02: 727-730
    CrossrefPubMedGoogle Scholar
  • 16 Ortenwal P, Wadenvik II, Kutti J, Risberg B. Reduction in deposition of Indium-111 labeled platelets after autologous endothelial seeding of Dacron aortic bifurcation grafts in humans: a preliminary report. J Vase Surg 1987; 6: 17-25
    CrossrefPubMedGoogle Scholar
  • 17 Ortenwal P, Wadenvik II, Risberg B. Reduced platelet deposition on seeded versus unseeded segments of expanded polytetrafluoroethylene grafts: clinical observations after a 6 month follow-up. J Vase Surg 1989; 10: 374-380
    CrossrefPubMedGoogle Scholar
  • 18 Kesler KA, Herring MB, Arnold MP, Glover JI, Park HM, Helmus MN, Bendick PJ. Enhanced strength of endothelial attachment on polyester elastomer and PTFE graft surfaces with fibronectin substrate. J Vase Surg 1986; 3: 58-64
    CrossrefPubMedGoogle Scholar
  • 19 Dalsing MC, Kevorkian M, Raper B, Nixon C. et al An experimental collagen-impregnated Dacron graft: potential for endothelial seeding. Ann Vase Surg 1989; 3: 127-133
    CrossrefPubMedGoogle Scholar
  • 20 Vohra RK, Thomson GJL, Shamara H, Carr HMH, Walker M. Effect of shear stress on endothelial cell monolayers on expanded polytetrafluoroethylene (ePTFE) grafts using preclot and fibronectin matrices. Eur J Vase Surg 1990; 04: 33-41
    CrossrefPubMedGoogle Scholar
  • 21 Prendiville EJ, Coleman JE, Callow AD, Gould KE, Laliberte-Verdon S, Ramberg K, Conolly RJ. Increased in-vitro incubation time of endothelial cells on fibronectin-treated ePTFE increases cell retention in blood flow. Eur J Vase Surg 1991; 05: 311-319
    CrossrefPubMedGoogle Scholar
  • 22 Gospodarowicz D, Moran J, Braun D, Birdwell C. Clonal growth of bovine vascular endothelial cells, fibroblast growth factor as a survival agent. Proc Nat Acad Sci USA 1976; 73: 4120-4124
    CrossrefPubMedGoogle Scholar
  • 23 Gospodarowicz D, Mescher Al, Birdwell CR. Stimulation of corneal endothelial cell proliferation in vitro by fibroblast and epidermal growth factors. Exp Eye Res 1977; 25: 75-87
    CrossrefPubMedGoogle Scholar
  • 24 Dewey CF. Fluid mechanics of arterial flow. In: Advances in experimental medicine and biology. Wolf S, Werthesse N. (eds.) New York: Plenum Press; 1979: 55-103
    Google Scholar
  • 25 Bar-Shavit R, Benezra M, Eldor A, Hy-Am E, Fenton JW, Wilner G, Vlodavsky I. Thrombin immobilized to extracellular matrix is a mitogen for vascular smooth muscle cells: Non-enzymatic mode of action. Cell Reg 1990; 1: 453-463
    PubMedGoogle Scholar
  • 26 Vlodavsky I, Greenburg G, Johnson LK, Gospodarowicz D. Vascular endothelial cells maintained in the absence of fibroblast growth factor undergo structural and functional alterations that are incompatible with their in vivo differentiated properties. J Cell Biol 1979; 83: 468-486
    CrossrefPubMedGoogle Scholar
  • 27 Vlodavsky I, Folkman J, Sullivan R, Fridman R, Ishai-Michaelli R, Sasse J, Klagsbrun M. Endothelial cell-derived basic fibroblast growth factor: Synthesis and deposition into subendothelial extracellular matrix. Proc Natl Acad Sci USA 1987; 84: 2292-2296
    CrossrefPubMedGoogle Scholar
  • 28 Vlodavsky I, Bar-Shavit R, Komer G, Fuks Z. Extracellular matrix-bound growth factors, enzymes and plasma proteins. In: Basement membranes: Cellular and molecular aspects. Rohrbach DH, Timpl R. (eds). Orlando: Academic Press Inc; 1993: 327-343
    Google Scholar
  • 29 Franke RP, Grafe M, Schnittler H, Seiffge D, Drenckhahn D. Induction of human vascular endothelial stress fibers by fluid shear stress. Nature 1984; 307: 648-649
    CrossrefPubMedGoogle Scholar
  • 30 Reutelingsperger CPM, Van Gool RGJ, Heijnen V, Frederik P, Lindhout T. The rotating disc as a device to study the adhesive properties of endothelial cells under differential shear stresses. J Mat Sci: Mat in Med 1994; 5: 361-367
    CrossrefPubMedGoogle Scholar
  • 31 Lavee J, Martinowitz U, Mohr R, Goor D, Golan M, Langsam J, Malik Z, Savion N. The effect of transfusion of fresh whole blood versus platelet concentrates after cardiac operations. J Thor Cardiovasc Surg 1989; 97: 204-212
    PubMedGoogle Scholar
  • 32 Golan M, Modan M, Lavee J, Martinowitz U, Savion N, Goor D, Mohr R. Transfusion of fresh whole blood stored (4° C) for short period fails to improve platelet aggregation on extracellular matrix and clinical hemostasis after cardiopulmonary bypass. J Thor Cardiovasc Surg 1990; 99: 354-360
    PubMedGoogle Scholar
  • 33 Vlodavsky I, Eldor A, Hyam E, Atzmon R, Fuks Z. Platelet interaction with the extracellular matrix produced by cultured endothelial cells: A model to study the thrombogenicity of isolated subendothelial basal lamina. Thromb Res 1982; 28: 179-191
    CrossrefPubMedGoogle Scholar
  • 34 Bellon JM, Bujan J, Honduvilla NG, Hernando A, Navlet J. Endothelial cell seeding of polytetrafluoroethylene vascular prostheses coated with a fibroblastic matrix. Ann Vase Surg 1993; 7: 549-555
    CrossrefPubMedGoogle Scholar
  • 35 Lalka SG, Oelker LM, Malone JM, Duhamel RC. et al A cellular vascular matrix: a natural endothelial cell substrate. Ann Vase Surg 1989; 3: 108-117
    CrossrefPubMedGoogle Scholar
  • 36 Ingber DE. Fibronectin controls capillary endothelial cell growth by modulating cell shape. Proc Natl Acad Sci USA 1990; 87: 3579-3583
    CrossrefPubMedGoogle Scholar
  • 37 Zilla P, Fasol R, Dudeck U, Siedler S, Preiss P, Fischlein T, Muller-Glauser W, Battelia-Eberle G, Sanan D, Odell J, Reichart B. In situ cannulation, microgrid follow-up and low density plating provide first passage endothelial cell mass cultures for in vitro lining. J Vase Surg 1990; 12: 180-189
    CrossrefPubMedGoogle Scholar
  • 38 Fischlein T, Zilla P, Eberl T, Puschmann R, Meinhart J, Minar E, Deutsch M. Initial clinical data on human in vitro endothelialization of vascular prostheses. In: Applied Cardiovascular Biology 1990-1991. Zilla P, Fasol R, Callow A. (eds.) Karger; 1991
    Google Scholar
  • 39 Zilla P, Deutsch M, Meinhart J, Puschmann R, Eberl T, Minar E, Dudczak R, Lugmaier H, Schmidt P, Noszian I, Fischleim T. Clinical in vitro endothelialization of femoropopliteal grafts: An actuarial follow-up over three years. J Vase Surg 1994; 19: 540-548
    CrossrefPubMedGoogle Scholar
  • 40 Schoen FJ. Interventional and surgical pathology: clinical correlations and basic principles. Philadelphia: Saunders; 1989. 241. 279
    Google Scholar
  • 41 Clowes AW, Reidy MA. Prevention of stenosis after vascular reconstruction: pharmacologic control of intimal hyperplasia – a review. J Vase Surg 1991; 13: 885-891
    PubMedGoogle Scholar
  • 42 Anderson JM, Hering TH, Abbuhl MF. Human vascular grafts: cellular and extracellular matrix components. In: Arterial surgery: new diagnostic and operative techniques. Bergen JJ, Yao JST. (eds.) New York: Grune & Stratton; 1988: 21-29
    Google Scholar
  • 43 Ziats NP, Anderson JM. Atherosclerosis and healing aberrations in clinical and experimental vascular grafts. In: Atherosclerosis and arteriosclerosis: human pathology and experimental animal methods and models. White RA. (ed.) Boca Raton: CRC Press; 1989: 289-302
    Google Scholar
  • 44 Hering TH, Suzuki Y, Anderson JM. Collagen type distribution distributing in healing of synthetic arterial prostheses. Conn Tiss Res 1986; 15: 141-154
    CrossrefPubMedGoogle Scholar
  • 45 Anderson JM, Hering TH, Suzuki Y. Studies on the healing of human vascular grafts: quantitative analysis of collagen and collagen types. In: Vascular grafts: safety and performance, ASTM STP 898. Hambic HE, Kantro-witz A, Sung P. (eds.) Philadelphia: American Society for Testing and Materials; 1986: 180-188
    Google Scholar
  • 46 Trelsted RL, Carvalho ACA. Type IV and type A-B collagens do not elicit platelet aggregation or the serotonin release reaction. J Lab Clin Med 1979; 93: 499-505
    PubMedGoogle Scholar
  • 47 Parson TJ, Haycraft DL, Hoak JC, Sage H. Diminished platelet adherence to type V collagen. Arteriosclerosis 1983; 3: 589-598
    CrossrefPubMedGoogle Scholar
  • 48 Koenig JM, Chahine A, Ratnoff OD. Inhibition of the activation of Hage- man factor (factor XII) by soluble human placental collagens types III, IV and V. J Lab Clin Med 1991; 117: 523-527
    PubMedGoogle Scholar
  • 49 Ziats NP, Anderson JM. Human vascular endothelial cell attachment and growth inhibition by type V collagen. J Vase Surg 1993; 17: 710-718
    CrossrefPubMedGoogle Scholar