Journal of Vascular Surgery
Volume 47, Issue 3 , Pages 616-624 , March 2008

Vein wall re-endothelialization after deep vein thrombosis is improved with low-molecular-weight heparin

Received 15 August 2007 ,Accepted 12 November 2007.

References 

  1. Prandoni P, Lensing AW, Cogo A, Cuppini S, Villalta S, Carta M, et al. The long-term clinical course of acute deep venous thrombosis. Ann Intern Med. 1996;125:1–7
  2. Delis KT, Bountouroglou D, Mansfield AO. Venous claudication in iliofemoral thrombosis: long-term effects on venous hemodynamics, clinical status, and quality of life. Ann Surg. 2004;239:118–126
  3. Bates SM, Ginsberg JS. Clinical practice (Treatment of deep-vein thrombosis). N Engl J Med. 2004;351:268–277
  4. Snow V, Qaseem A, Barry P, Hornbake ER, Rodnick JE, Tobolic T, et al. Management of venous thromboembolism: a clinical practice guideline from the American College of Physicians and the American Academy of Family Physicians. Ann Intern Med. 2007;146:204–210
  5. Hull RD, Pineo GF, Brant RF, Mah AF, Burke N, Dear R, et al. Long-term low-molecular-weight heparin versus usual care in proximal-vein thrombosis patients with cancer. Am J Med. 2006;119:1062–1072
  6. Wakefield TW, Henke PK. The role of inflammation in early and late venous thrombosis: Are there clinical implications?. Semin Vasc Surg. 2005;18:118–129
  7. Gennaro G, Menard C, Michaud SE, Rivard A. Age-dependent impairment of reendothelialization after arterial injury: role of vascular endothelial growth factor. Circulation. 2003;107:230–233
  8. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, et al. Statin therapy accelerates reendothelialization - a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation. 2002;105:3017–3024
  9. Modarai B, Burnand KG, Sawyer B, Smith A. Endothelial progenitor cells are recruited into resolving venous thrombi. Circulation. 2005;111:2645–2653
  10. Aird WC. Phenotypic heterogeneity of the endothelium: I (Structure, function, and mechanisms). Circ Res. 2007;100:158–173
  11. Hedin U, Roy J, Tran PK, Lundmark K, Rahman A. Control of smooth muscle cell proliferation–the role of the basement membrane. Thromb Haemost. 1999;82(suppl 1):23–26
  12. Aguilera CM, George SJ, Johnson JL, Newby AC. Relationship between type IV collagen degradation, metalloproteinase activity and smooth muscle cell migration and proliferation in cultured human saphenous vein. Cardiovasc Res. 2003;58:679–688
  13. Davis GE, Senger DR. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res. 2005;97:1093–1107
  14. Dollery CM, Humphries SE, McClelland A, Latchman DS, McEwan JR. Expression of tissue inhibitor of matrix metalloproteinases 1 by use of an adenoviral vector inhibits smooth muscle cell migration and reduces neointimal hyperplasia in the rat model of vascular balloon injury. Circulation. 1999;99:3199–3205
  15. Thyberg J, Hultgardh-Nilsson A. Fibronectin and the basement membrane components laminin and collagen type IV influence the phenotypic properties of subcultured rat aortic smooth muscle cells differently. Cell Tissue Res. 1994;276:263–271
  16. Henke PK, Varga A, De S, Deatrick CB, Eliason J, Arenberg DA, et al. Deep vein thrombosis resolution is modulated by monocyte CXCR2-mediated activity in a mouse model. Arterioscler Thromb Vasc Biol. 2004;24:1130–1137
  17. Wakefield TW, Strieter RM, Wilke CA, Kadell AM, Wrobleski SK, Burdick MD, et al. Venous thrombosis-associated inflammation and attenuation with neutralizing antibodies to cytokines and adhesion molecules. Arterioscler Thromb Vasc Biol. 1995;15:258–268
  18. Henke PK, Varma MR, Deatrick KB, Drewyer NA, Lynch EM, Moore AJ, et al. Neutrophils modulate post-thrombotic vein wall remodeling but not thrombus neovascularization. Thromb Haemost. 2006;95:272–281
  19. Myers DD, Henke PK, Bedard PW, Wrobleski SK, Kaila N, Shaw G, et al. Treatment with an oral small molecule inhibitor of P selectin (PSI-697) decreases vein wall injury in a rat stenosis model of venous thrombosis. J Vasc Surg. 2006;44:625–632
  20. Thanaporn P, Myers DD, Wrobleski SK, Hawley AE, Farris DM, Wakefield TW, et al. P-selectin inhibition decreases post-thrombotic vein wall fibrosis in a rat model. Surgery. 2003;134:365–371
  21. Varma MR, Moaveni DM, Dewyer NA, Varga AJ, Deatrick KB, Kunkel SL, et al. Deep vein thrombosis resolution is not accelerated with increased neovascularization. J Vasc Surg. 2004;40:536–542
  22. Henke PK, Pearce CG, Moaveni DM, Moore AJ, Lynch EM, Longo C, et al. Targeted deletion of CCR2 impairs deep vein thrombosis resolution in a mouse model. J Immunol. 2006;177:3388–3397
  23. Sullivan VV, Hawley AE, Farris DM, Knipp BS, Varga AJ, Wrobleski SK, et al. Decrease in fibrin content of venous thrombi in selectin-deficient mice. J Surg Res. 2003;109:1–7
  24. Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA. Interleukin-1 activation of vascular endothelium (Effects on procoagulant activity and leukocyte adhesion). Am J Pathol. 1985;121:394–403
  25. Kaplanski G, Fabrigoule M, Boulay V, Dinarello CA, Bongrand P, Kaplanski S, et al. Thrombin induces endothelial type II activation in vitro: IL-1 and TNF-alpha-independent IL-8 secretion and E-selectin expression. J Immunol. 1997;158:5435–5441
  26. Maier JA, Hla T, Maciag T. Cyclooxygenase is an immediate-early gene induced by interleukin-1 in human endothelial cells. J Biol Chem. 1990;265:10805–10808
  27. Ginzinger DG. Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp Hematol. 2002;30:503–512
  28. Varma MR, Varga AJ, Knipp BS, Sukheepod P, Upchurch GR, Kunkel SL, et al. Neutropenia impairs venous thrombosis resolution in the rat. J Vasc Surg. 2003;38:1090–1098
  29. Deatrick KB, Eliason JL, Lynch EM, Moore AJ, Dewyer NA, Varma MR, et al. Vein wall remodeling after deep vein thrombosis involves matrix metalloproteinases and late fibrosis in a mouse model. J Vasc Surg. 2005;42:140–148
  30. Wang L, Brown JR, Varki A, Esko JD. Heparin’s anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins. J Clin Invest. 2002;110:127–136
  31. Ranjbaran H, Wang Y, Manes TD, Yakimov AO, Akhtar S, Kluger MS, et al. Heparin displaces interferon-gamma-inducible chemokines (IP-10, I-TAC, and Mig) sequestered in the vasculature and inhibits the transendothelial migration and arterial recruitment of T cells. Circulation. 2006;114:1293–1300
  32. Downing LJ, Strieter RM, Kadell AM, Wilke CA, Greenfield LJ, Wakefield TW. Low-dose low-molecular-weight heparin is anti-inflammatory during venous thrombosis. J Vasc Surg. 1998;28:848–854
  33. Carr JA, Cho JS. Low molecular weight heparin suppresses tumor necrosis factor expression from deep vein thrombosis. Ann Vasc Surg. 2007;21:50–55
  34. Trabucchi E, Foschi D, Marazzi M, Abelli P, Andriuoli G, Lami F, et al. Heparin prevents stasis-induced thrombosis through protection of the venous endothelial cells: an electron microscopic study in rabbits. Haemostasis. 1991;21:37–44
  35. Henke PK, Varma MR, Moaveni DK, Dewyer NA, Moore AJ, Lynch EM, et al. Fibrotic injury after experimental deep vein thrombosis is determined by the mechanism of thrombogenesis. Thromb Haemost. 2007;98:1045–1055
  36. Stenberg B, Bylock A, Risberg B. Effect of venous stasis on vessel wall fibrinolysis. Thromb Haemost. 1984;51:240–242
  37. Rabelink TJ, Luscher TF. Endothelial nitric oxide synthase: host defense enzyme of the endothelium?. Arterioscler Thromb Vasc Biol. 2006;26:267–271
  38. Blackman DJ, Morris-Thurgood JA, Atherton JJ, Ellis GR, Anderson RA, Cockcroft JR, et al. Endothelium-derived nitric oxide contributes to the regulation of venous tone in humans. Circulation. 2000;101:165–170
  39. Waugh JM, Yuksel E, Li J, Kuo MD, Kattash M, Saxena R, et al. Local overexpression of thrombomodulin for in vivo prevention of arterial thrombosis in a rabbit model. Circ Res. 1999;84:84–92
  40. Kim AY, Walinsky PL, Kolodgie FD, Bian C, Sperry JL, Deming CB, et al. Early loss of thrombomodulin expression impairs vein graft thromboresistance: implications for vein graft failure. Circ Res. 2002;90:205–212
  41. Rudic RD, Brinster D, Cheng Y, Fries S, Song WL, Austin S, et al. COX-2-derived prostacyclin modulates vascular remodeling. Circ Res. 2005;96:1240–1247
  42. Henke PK, Ferguson E, Varma M, Deatrick KB, Wakefield GT, Woodrum DT. Proximate versus nonproximate risk factor associated primary deep venous thrombosis: clinical spectrum and outcomes. J Vasc Surg. 2007;45:998–1003discussion 1003-4; quiz 1005-7

 Competition of interest: none.Supported in part by the McKay Cardiovascular Research Grant and National Institutes of Health (NIH) R-01 HL083918 to Dr Henke.

PII: S0741-5214(07)01784-3

doi: 10.1016/j.jvs.2007.11.040

Journal of Vascular Surgery
Volume 47, Issue 3 , Pages 616-624 , March 2008

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