Venous hypoxia: A poorly studied etiological factor of varicose veins

Journal of Vascular Research

Volumn 48, Issue 3, 2011, Pages 185-194

  Lim, C S ^a,b   Gohel, M S ^a   Shepherd, A C ^a   Paleolog, E ^b   Davies, A H ^a  

^a CHARING CROSS HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Hypoxia; Varicose veins; Vein and oxygen

Indexed keywords

BLOOD OXYGENATION; HUMAN; HYPOXIA; LEUKOCYTE ACTIVATION; MEDIATOR; PRIORITY JOURNAL; REVIEW; TISSUE OXYGENATION; VARICOSIS; VASCULITIS; VEIN WALL;

ANIMALS; ANOXIA; CARDIOVASCULAR AGENTS; EVIDENCE-BASED MEDICINE; HUMANS; OXYGEN; RISK ASSESSMENT; RISK FACTORS; TREATMENT OUTCOME; VARICOSE VEINS; VEINS;

EID: 78449233656     PISSN: 10181172     EISSN: None     Source Type: Journal    
DOI: 10.1159/000320624     Document Type: Review

References (74)

1. Lee AJ, Evans CJ, Allan PL, Ruckley CV, Fowkes FG: Lifestyle factors and the risk of varicose veins: Edinburgh Vein Study. J Clin Epidemiol 2003; 56: 171-179. (Pubitemid 36315944)
2. International task force. The management of chronic venous disorders of the leg: an evidence-based report of an international task force. Epidemiology. Phlebology 1999; 14(suppl 1):23.
3. Nicolaides AN: Investigation of chronic venous insufficiency: a consensus statement (France, March 5-9, 1997). Circulation 2000; 102:E126-E163.
4. Raffetto JD, Khalil RA: Mechanisms of varicose vein formation: valve dysfunction and wall dilation. Phlebolog y 2008; 23: 85-98.
5. Somers P, Knaapen M: The histopathology of varicose vein disease. Angiology 2006; 57: 546-555. (Pubitemid 44564310)
6. Lim CS, Davies AH: Pathogenesis of primary varicose veins. Br J Surg 2009; 96:1231-1242.
7. Lim CS, Shalhoub J, Gohel MS, Shepherd AC, Davies AH: Matrix metalloproteinases in vascular disease -a potential therapeutic target? Curr Vasc Pharmacol 2010; 8: 75-85.
8. Michiels C, Bouaziz N, Remacle J: Role of the endothelium and blood stasis in the development of varicose veins. Int Angiol 2002; 21: 18-25. (Pubitemid 35414734)
9. Taccoen A, Lebard C, Borie H, Poullain JC, Zuccarelli F, Gerentes I, Stern S, Guichard M: Measurement of oxygen tension in normal and varicose vein walls (in French). J Mal Vasc 1996; 21(suppl C):259-265. (Pubitemid 26362698)
10. Kachlik D, Lametschwandtner A, Rejmon-tova J, Stingl J, Vanek I: Vasa vasorum of the human great saphenous vein. Surg Radiol A nat 2003; 24: 377-381.
11. Lefebvre D, Lescalie F: Vascularization of the wall of the superficial veins. Anatomic study of the vasa vasorum (in French). J Mal Vasc 1996; 21(suppl C):245-248.
12. Kachlik D, Baca V, Stingl J, Sosna B, Lametschwandtner A, Minnich B, Setina M: Architectonic arrangement of the vasa vaso-rum of the human great saphenous vein. J Vasc Res 2007; 4 4: 157-166.
13. 2 . Am J Physiol 1986; 250:H434-H442.
14. Bigel P, Taccoen A: Morphology and vascu-larization of the varicose internal saphenous vein. Comparison with the normal structure (in French). J Mal Vasc 1996; 21(su pl C ) : 249-252. (Pubitemid 26362696)
15. Kachlik D, Stingl J, Sosna B, Straka Z, Lametschwandtner A, Minnich B, Fara P: Morphological features of vasa vasorum in pathologically changed human great saphe-nous vein and its tributaries. Vasa 20 08; 37: 127-136. (Pubitemid 351881024)
16. Michiels C, Arnould T, Remacle J: Endothe-lial cell responses to hypoxia: initiation of a cascade of cellular interactions. Biochim Biophys Acta 2000; 1497:1-10. (Pubitemid 30330885)
17. Nicolaides AN: From symptoms to leg edema: Efficacy of Daflon 500 mg. Angiology 2003; 54(suppl 1):S33-S44. (Pubitemid 36935349)
18. Colm Malone P, Agutter PS: To what extent might deep venous thrombosis and chronic venous insufficiency share a common etiology? Int Angiol 2009; 28:254-268.
19. McEwan AJ, McArdle CS: Effect of hydroxy-ethylrutosides on blood oxygen levels and venous insufficiency symptoms in varicose veins. Br Med J 1971; 2:138-141.
20. De Takats G, Quint H, Tillotson BI, Critten-den PJ: The impairment of circulation in the varicose ex tremity. Arch Surg 1929; 18: 671.
21. Reikerås O, Sorlie D: The significance of ar-teriovenous shunting for the development of varicose veins. Acta Chir Scand 1983; 149: 479-481. (Pubitemid 13045425)
22. Scott HJ, Cheatle TR, McMullin GM, Coleridge Smith PD, Scurr JH: Reappraisal of the oxygenation of blood in varicose veins. Br J Surg 1990; 77: 934-936. (Pubitemid 20249709)
23. Holling HE, Beecher HK, Linton RR: Study of the tendency to edema formation associated with incompetence of the valves of the communicating veins of the leg. Oxygen tension of the blood contained in varicose veins. J Clin Invest 1938; 17:555-561.
24. Murphy MA, Hands L: Is arteriovenous shu nt i ng i nvolved in the development of var-icosities? A study of the intraluminal pressure and oxygen content in varicose veins. Phlebolog y 2008; 23: 137-141.
25. Schraibman IG: Blood oxygen saturation and dye-dilution studies in the investigation of the aetiology of varicose veins. Aust NZ J Surg 1966; 36: 136-144 .
26. Wali MA: Oxygenation of blood in varicose veins. Afr J Med Med Sci 2002; 31:219-222.
27. Blalock A: Oxygen content of blood in patients with varicose veins. Arch Surg 1929; 19: 298-305.
28. Baron HC, Cassaro S: The role of arteriove-nous shunts in the pathogenesis of varicose veins. J Vasc Surg 1986; 4:124-128. (Pubitemid 16043825)
29. 2 in patients with varicose veins. J Surg Res 1977; 23: 35-36. (Pubitemid 8144488)
30. Jacob MP, Cazaubon M, Scemama A, Prie D, Blanchet F, Guillin MC, Michel JB: Plasma matrix metalloproteinase-9 as a marker of blood stasis in varicose veins. Circulation 2002; 106 : 535-538. (Pubitemid 34827700)
31. Takase S, Lerond L, Bergan JJ, Schmid-Schonbein GW: The inflammatory reaction during venous hypertension in the rat. Mi-crocirculation 2000; 7:41-52.
32. Thomas PR, Nash GB, Dormandy JA: White cell accumulation in dependent legs of patients with venous hypertension: a possible mechanism for trophic changes in the skin. Br Med J (Clin Res Ed) 1988; 296:1693-1695.
33. Smith PD: Neutrophil activation and mediators of inflammation in chronic venous in-suff iciency. J Vasc Res 1999; 36(suppl 1):24-36. (Pubitemid 29411272)
34. Lengyel I, Acsady G: Histomorphological and pathobiochemical changes of varicose veins. A possible explanation of the development of varicosis. Acta Morphol Hung 1990; 38:259-267.
35. Niebes P: Vessel wall modification in venous pathology. Application to the study of phle-botonic drugs. Int Angiol 1996; 15:88-92. (Pubitemid 26182235)
36. Glowinski J, Glowinski S: Generation of reactive oxygen metabolites by the varicose vein wall. Eur J Vasc Endovasc Surg 2002; 23: 550-555. (Pubitemid 41079408)
37. Flore R, Santoliquido A, Antonio DL, Pola E, Flex A, Pola R, Muzi MG, Farinon A, Rulli F, Gaetani E, Tondi P, Gerardino L, Gasbarrini A: Long saphenous vein stripping reduces local level of reactive oxygen metabolites in patients with varicose disease of the lower limbs. World J Surg 2003; 27:473-475. (Pubitemid 36920124)
38. Whiston RJ, Hallett MB, Davies EV, Harding KG, Lane IF: Inappropriate neutrophil activation in venous disease. Br J Surg 1994; 81: 695-698. (Pubitemid 24192097)
39. Stvrtinova V, Ferencikova J: Lysosomal enzymes and superoxide production in polymorphonuclear leucocytes of patients with primary varicose veins. Cor Vasa 1992; 34: 255-264. (Pubitemid 23153441)
40. Ciuffetti G, Mannarino E, Paltriccia R, Malagigi V, Sergi F, Paulisch P, Pasqualini L, Lupattelli G: Leucocyte activity in chronic venous insufficiency. Int Angiol 1994; 13: 312-316.
41. Bougelet C, Roland IH, Ninane N, Arnould T, Remacle J, Michiels C: Effect of aescine on hypoxia-induced neutrophil adherence to umbilical vein endothelium. Eur J Pharmacol 1998; 345:89-95. (Pubitemid 28179475)
42. Michiels C, Arnould T, Remacle J: Hypoxia-induced activation of endothelial cells as a possible cause of venous diseases: hypothesis. Angiology 1993; 44: 639-646. (Pubitemid 23227951)
43. Arnould T, Michiels C, Alexandre I, Remacle J: Effect of hypoxia upon intracellular calcium concentration of human endothelial cells. J Cell Physiol 1992; 152:215-221.
44. Janssens D, Michiels C, Delaive E, Eliaers F, Drieu K, Remacle J: Protection of hypoxia-induced ATP decrease in endothelial cells by Ginkgo biloba extract and bilobalide. Bio-chem Pharmacol 1995; 50: 991-999.
45. Michiels C, Arnould T, Knott I, Dieu M, Remacle J: Stimulation of prostaglandin synthesis by human endothelial cells exposed to hypoxia. Am J Physiol 1993; 264:C866-C874. (Pubitemid 23118106)
46. Michiels C, De Leener F, Arnould T, Dieu M, Remacle J: Hypoxia stimulates human endothelial cells to release smooth muscle cell mitogens: role of prostaglandins and bFGF. Exp Cell Res 1994; 213:43-54. (Pubitemid 24227381)
47. Michiels C, Bouaziz N, Remacle J: Role of the endothelium and blood stasis in the appearance of varicose veins. Int Angiol 2002; 21: 1-8. (Pubitemid 34413648)
48. Calvani M, Rapisarda A, Uranchimeg B, Shoemaker RH, Melillo G: Hypoxic induction of an HIF-1a-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells. Blood 2006; 107:2705-2712.
49. Zhu XY, Daghini E, Chade AR, Lavi R, Na-poli C, Lerman A, Lerman LO: Disparate effects of simvastatin on angiogenesis during hypoxia and inflammation. Life Sci 2008; 83: 801-809.
50. Jiang J, Xia XB, Xu HZ, Xiong Y, Song WT, Xiong SQ, Li Y: Inhibition of retinal neovascularization by gene transfer of small interfering RNA targeting HIF-1a and VEGF. J Cell Physiol 2009; 218:66-74.
51. Haider DG, Bucek RA, Giurgea AG, Maurer G, Glogar H, Minar E, Wolzt M, Mehrabi MR, Baghestanian M: PGE 1 analog alprosta-dil induces VEGF and ENOS expression in endothelial cells. Am J Physiol Heart Circ Physiol 2005; 289:H2066-H2072. (Pubitemid 41507358)
52. Coulet F, Nadaud S, Agrapart M, Soubrier F: Identification of hypoxia-response element in the human endothelial nitric-oxide synthase gene promoter. J Biol Chem 2003; 278: 46230-46240. (Pubitemid 37452193)
53. Semenza GL: Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda) 2009; 24:97-106.
54. Cook-Johnson RJ, Demasi M, Cleland LG, Gamble JR Saint DA, James MJ: Endothelial cell COX-2 expression and activity in hypoxia. Biochim Biophys Acta 2006; 1761:1443-1449. (Pubitemid 44821907)
55. Matagne D, Gilles R: Effect of O-(|3-hydroxyethyl)-rutoside on the glucose metabolism of cultured human varicose saphenous veins. Arch Int Physiol Biochim 1977; 85: 133-138. (Pubitemid 8069230)
56. Aunapuu M, Arend A: Histopathological changes and expression of adhesion molecules and laminin in varicose veins. Vasa 2005; 34: 170-175. (Pubitemid 41248254)
57. Arnould T, Janssens D, Michiels C, Remacle J: Effect of aescine on hypoxia-induced activation of human endothelial cells. Eur J Pharmacol 1996; 315:227-233. (Pubitemid 26390942)
58. Arnould T, Michiels C, Janssens D, Delaive E, Remacle J: Hypoxia induces pmn adherence to umbilical vein endothelium. Cardio-vasc Res 1995; 30:1009-1016.
59. Arnould T, Michiels C, Remacle J: Increased PMN adherence on endothelial cells after hypoxia: Involvement of PAF, CD18/CD11b, and ICAM-1. Am J Physiol 1993; 264:C1102-C1110. (Pubitemid 23158815)
60. Arnould T, Michiels C, Remacle J: Hypoxic human umbilical vein endothelial cells induce activation of adherent polymorphonuclear leukocytes. Blood 1994; 83:3705-3716. (Pubitemid 24175562)
61. Michiels C, Arnould T, Thibaut-Vercruyssen R, Bouaziz N, Janssens D, Remacle J: Perfused human saphenous veins for the study of the origin of varicose veins: role of the endothelium and of hypoxia. Int Angiol 1997; 16:134-141. (Pubitemid 27353146)
62. Michiels C, Remacle J, Bouaziz N: Endothelium and venotropic drugs in chronic venous insufficiency: a review. Phlebology 2002; 17: 145-150. (Pubitemid 36133096)
63. Martinez MJ, Bonfill X, Moreno RM, Vargas E, Capella D: Phlebotonics for venous insufficiency. Cochrane Database Syst Rev 2005;CD003229.
64. Janssens D, Delaive E, Houbion A, Eliaers F, Remacle J, Michiels C: Effect of venotropic drugs on the respiratory activity of isolated mitochondria and in endothelial cells. Br J Pharmacol 2000; 130: 1513-1524. (Pubitemid 30611926)
65. Guilhou JJ, Dereure O, Marzin L, Ouvry P, Zuccarelli F, Debure C, Van Landuyt H, Gil-let-Terver MN, Guillot B, Levesque H, Mignot J, Pillion G, Fevrier B, Dubeaux D: Efficacy of Daflon 500 mg in venouslegulcer healing: a double-blind, randomized, controlled versus placebo trial in 107 patients. Angiology 1997; 48:77-85. (Pubitemid 27026897)
66. Struckmann JR: Clinical efficacy of micron-ized purified flavonoid fraction: an overview. J Vasc Res 1999; 36(suppl 1):37-41. (Pubitemid 29411273)
67. Gohel MS, Davies AH: Pharmacological agents in the treatment of venous disease: An update of the available evidence. Curr Vasc Pharmacol 2009; 7: 303-308.
68. MacKay D: Hemorrhoids and varicose veins: a review of treatment options. Altern Med Rev 2001; 6:126-140. (Pubitemid 32323367)
69. Taccoen A, Belcaro G, Lebard C, Zuccarelli F: Pathogenesis and underlying mechanisms of varicose veins: review and future prospects. Sang Thrombose Vaisseaux 1997; 9: 354-363. (Pubitemid 27382122)
70. Michiels C, Arnould T, Janssens D, Bajou K, Geron I, Remacle J: Interactions between endothelial cells and smooth muscle cells after their activation by hypoxia. A possible etiology for venous disease. Int Angiol 1996; 15: 124-130.
71. Boyce JA, Mellor EA, Perkins B, Lim YC, Luscinskas FW: Human mast cell progenitors use a4-integrin, VCAM-1, and PSGL-1 E-selectin for adhesive interactions with human vascular endothelium under flow conditions. Blood 2002; 99: 2890-2896. (Pubitemid 34525378)
72. Birukov KG: Cyclic stretch, reactive oxygen species, and vascular remodeling. Antioxid Redox Signal 2009; 11:1651-1667.
73. Koskinas KC, Chatzizisis YS, Baker AB, Edelman ER, Stone PH, Feldman CL: The role of low endothelial shear stress in the conversion of atherosclerotic lesions from stable to unstable plaque. Curr Opin Cardiol 2009; 24:580-590.
74. Lim CS, Gohel MS, Davies AH: Is there still a role for basic science research in venous disease? Phlebology 2008; 23: 147-148.