Vasa vasorum and atherosclerosis – Quid novi?

Alexander C. Langheinrich; Marian Kampschulte; Thomas Buch; Rainer M. Bohle

doi:10.1160/TH06-12-0742

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2007; 97(06): 873-879
DOI: 10.1160/TH06-12-0742

Review Article

Schattauer GmbH

Vasa vasorum and atherosclerosis – Quid novi?

Authors

Alexander C. Langheinrich

¹University of Giessen, Department of Radiology, Giessen, Germany
Marian Kampschulte

¹University of Giessen, Department of Radiology, Giessen, Germany
Thomas Buch

¹University of Giessen, Department of Radiology, Giessen, Germany
Rainer M. Bohle

²University of Homburg/Saar, Department of Pathology, Homburg/Saar, Germany

Abstract

Summary

The role of vasa vasorum (VV) in atherosclerosis is hotly debated, and new experimental techniques have recently opened an opportunity to take a fresh look at this important topic. Although the proliferation of VV due to atherogenic stimuli is controversial, experimental and clinical evidence strongly suggest the potential of VV in vascular proliferative disorders. In the past, paradigms of atherosclerosis and restenosis have excluded the adventitia and VV in the artery wall due, in part, to a lack of i) appropriate animal models featuring adventitial VV neovascularization, ii) imaging technologies to quantitate adventitial VV and plaque neovascularization and iii) its consequences, concerning information on detectable plaque substrate in vulnerable lesions. VV proliferation is associated with increasing plaque burden and is linked to cellular processes which are critical during the development of atherosclerotic plaques such as inflammation, plaque perfusion and concomitant intraplaque hemorrhage – but the regulation and induction of VV based on pathological settings are poorly understood. This review discusses the current scientific status and its controversies and identifies open research questions.

Keywords

Vasa vasorum - inflammation - atherosclerosis - intraplaque hemorrhage

Full Text

References

References
1 Clarke JA. An x-ray microscopic study of the postnatal development of the vasa vasorum of normal human coronary arteries. Acta Anat (Basel) 1966; 64: 506-516.
2 Clarke JA. An x-ray microscopic study of the development of the vasa vasorum in the human foetal aorta and pulmonary trunk. Acta Anat (Basel) 1966; 63: 55-70.
3 Gossl M, Zamir M, Ritman EL. Vasa vasorum growth in the coronary arteries of newborn pigs. Anat Embryol (Berl) 2004; 208: 351-357.
4 Wolinsky H, Glagov S. Nature of species differences in the medial distribution of aortic vasa vasorum in mammals. Circ Res 1967; 20: 409-421.
5 Schoenenberger F, Mueller A. On the vascularization of the bovine aortic wall. Helv Physiol Pharmacol Acta 1960; 18: 136-150.
6 Gossl M, Rosol M, Malyar NM. et al. Functional anatomy and hemodynamic characteristics of vasa vasorum in the walls of porcine coronary arteries. Anat Rec A Discov Mol Cell Evol Biol 2003; 272: 526-537.
7 Kwon HM, Sangiorgi G, Ritman EL. et al. Enhanced coronary vasa vasorum neovascularization in experimental hypercholesterolemia. J Clin Invest 1998; 101: 1551-1556.
8 Mann FD. Vasa vasorum and coronary atherosclerosis. Perspect Biol Med 1985; 28: 367-369.
9 McGeachie J, Campbell P, Simpson S. et al. Arterial vasa vasorum: a quantitative study in the rat. J Anat 1982; 134: 193-197.
10 Schutte HE. Plaque localization and distribution of vasa vasorum. A micro-angiological study of the human abdominal aorta. Angiologica 1966; 3: 21-39.
11 Werber AH, Heistad DD. Diffusional support of arteries. Am J Physiol 1985; 248: H901-H906.
12 Gossl M, Malyar NM, Rosol M. et al. Impact of coronary vasa vasorum functional structure on coronary vessel wall perfusion distribution. Am J Physiol Heart Circ Physiol 2003; 285: H2019-H2026.
13 Bayer IM, Caniggia I, Adamson SL. et al. Experimental angiogenesis of arterial vasa vasorum. Cell Tissue Res 2002; 307: 303-313.
14 Celletti FL, Hilfiker PR, Ghafouri P. et al. Effect of human recombinant vascular endothelial growth factor165 on progression of atherosclerotic plaque. J Am Coll Cardiol 2001; 37: 2126-2130.
15 Celletti FL, Waugh JM, Amabile PG. et al. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 2001; 7: 425-429.
16 Neufeld G, Cohen T, Gengrinovitch S. et al. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 1999; 13: 9-2.
17 Heistad DD, Armstrong ML, Amundsen S. Blood flow through vasa vasorum in arteries and veins: effects of luminal PO2. Am J Physiol 1986; 250: H434-H442.
18 Davie NJ, Crossno JT, Frid MG. et al. Hypoxia-induced pulmonary artery adventitial remodeling and neovascularization: contribution of progenitor cells. Am J Physiol Lung Cell Mol Physiol 2004; 286: L668-L678.
19 Kai H, Kuwahara F, Tokuda K. et al. Coexistence of hypercholesterolemia and hypertension impairs adventitial vascularization. Hypertension 2002; 39: 455-459.
20 Gossl M, Beighley PE, Malyar NM. et al. Role of vasa vasorum in transendothelial solute transport in the coronary vessel wall: a study with cryostatic micro-CT. Am J Physiol Heart Circ Physiol 2004; 2870: H2346-H2351.
21 Herrmann J, Lerman LO, Rodriguez-Porcel M. et al. Coronary vasa vasorum neovascularization precedes epicardial endothelial dysfunction in experimental hypercholesterolemia. Cardiovasc Res 2001; 51: 762-766.
22 Santilli SM, Kronson J, Payne WD. The effect of hypercholesterolemia on the rabbit transarterial wall oxygen gradient. Ann Vasc Surg 1998; 12: 418-423.
23 Galili O, Herrmann J, Woodrum J. et al. Adventitial vasa vasorum heterogeneity among different vascular beds. J Vasc Surg 2004; 40: 529-535.
24 Rodriguez-Porcel M, Lerman A, Ritman EL. et al. Altered myocardial microvascular 3D architecture in experimental hypercholesterolemia. Circulation 2000; 102: 2028-2030.
25 Zhu XY, Rodriguez-Porcel M, Bentley MD. et al. Antioxidant intervention attenuates myocardial neovascularization in hypercholesterolemia. Circulation 2004; 109: 2109-2115.
26 Walker G, Langheinrich AC, Dennhauser E. et al. 3-deazaadenosine prevents adhesion molecule expression and atherosclerotic lesion formation in the aortas of C57BL/6J mice. Arterioscler Thromb Vasc Biol 1999; 19: 2673-2679.
27 Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-874.
28 Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999; 340: 115-126.
29 Moos MP, John N, Grabner R. et al. The lamina adventitia is the major site of immune cell accumulation in standard chow-fed apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25: 2386-2391.
30 Numano F, Okawara M, Inomata H. et al. Takayasu's arteritis. Lancet 2000; 356: 1023-1025.
31 Numano F. Vasa vasoritis, vasculitis and atherosclerosis. Int J Cardiol 2000; 75 (Suppl. 01) S1-S9.
32 Harper L, Savage CO. Pathogenesis of ANCA-associated systemic vasculitis. J Pathol 2000; 190: 349-359.
33 Lentsch AB, Ward PA. Regulation of inflammatory vascular damage. J Pathol 2000; 190: 343-348.
34 Gross PL, Aird WC. The endothelium and thrombosis. Semin Thromb Hemost 2000; 26: 463-478.
35 Moulton KS, Vakili K, Zurakowski D. et al. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci USA 2003; 100: 4736-4741.
36 Moulton KS, Olsen BR, Sonn S. et al. Loss of collagen XVIII enhances neovascularization and vascular permeability in atherosclerosis. Circulation 2004; 110: 1330-1336.
37 Fleiner M, Kummer M, Mirlacher M. et al. Arterial neovascularization and inflammation in vulnerable patients: early and late signs of symptomatic atherosclerosis. Circulation 2004; 110: 2843-2850.
38 Herron GS, Unemori E, Wong M. et al. Connective tissue proteinases and inhibitors in abdominal aortic aneurysms. Involvement of the vasa vasorum in the pathogenesis of aortic aneurysms. Arterioscler Thromb 1991; 11: 1667-1677.
39 Aydin F. Do human intracranial arteries lack vasa vasorum? A comparative immunohistochemical study of intracranial and systemic arteries. Acta Neuropathol (Berl) 1998; 96: 22-28.
40 Connolly ES, Huang J, Goldman JE. et al. Immunohistochemical detection of intracranial vasa vasorum: a human autopsy study. Neurosurgery 1996; 38: 789-793.
41 Atkinson JL, Okazaki H, Sundt TM. et al. Intracranial cerebrovascular vasa vasorum associated with atherosclerosis and large thick-walled aneurysms. Surg Neurol 1991; 36: 365-369.
42 Krings T, Piske RL, Lasjaunias PL. Intracranial arterial aneurysm vasculopathies: targeting the outer vessel wall. Neuroradiology 2005; 47: 931-937.
43 Duvall WL, Vorchheimer DA. Multi-bed vascular disease and atherothrombosis: scope of the problem. J Thromb Thrombolysis 2004; 17: 51-61.
44 Espinola-Klein C, Rupprecht HJ, Blankenberg S. et al. Manifestations of atherosclerosis in various vascular regions. Similarities and differences regarding epidemiology, etiology and prognosis. Med Klin (Munich) 2002; 97: 221-228.
45 Sutton-Tyrrell K, Kuller LH, Matthews KA. et al. Subclinical atherosclerosis in multiple vascular beds: an index of atherosclerotic burden evaluated in postmenopausal women. Atherosclerosis 2002; 160: 407-416.
46 Pasterkamp G, Schoneveld AH, Hillen B. et al. Is plaque formation in the common carotid artery representative for plaque formation and luminal stenosis in other atherosclerotic peripheral arteries? A post mortem study. Atherosclerosis 1998; 137: 205-210.
47 Weber G, Bianciardi G, Bussani R. et al. Atherosclerosis and aging. A morphometric study on arterial lesions of elderly and very elderly necropsy subjects. Arch Pathol Lab Med 1988; 112: 1066-1070.
48 Galili O, Sattler KJ, Herrmann J. et al. Experimental hypercholesterolemia differentially affects adventitial vasa vasorum and vessel structure of the left internal thoracic and coronary arteries. J Thorac Cardiovasc Surg 2005; 129: 767-772.
49 Gray WG, Miller CT. Examination of Darcys law for flow in porous media with variable porosity. Environ Sci Technol 2004; 38: 5895-5901.
50 Hu W, Polinsky P, Sadoun E. et al. Atherosclerotic lesions in the common coronary arteries of ApoE knockout mice. Cardiovasc Pathol 2005; 14: 120-125.
51 Cheng TO. Why is atherosclerosis non-existent in human intramyocardial coronary arteries?. Atherosclerosis 2000; 153: 259.
52 Barger AC, Beeuwkes R, Lainey LL. et al. Hypothesis: vasa vasorum and neovascularization of human coronary arteries. A possible role in the pathophysiology of atherosclerosis. N Engl J Med 1984; 310: 175-177.
53 Inoue M, Itoh H, Ueda M. et al. Vascular endothelial growth factor (VEGF) expression in human coronary atherosclerotic lesions: possible pathophysiological significance of VEGF in progression of atherosclerosis. Circulation 1998; 98: 2108-2116.
54 Zhang Y, Cliff WJ, Schoefl GI. et al. Immunohistochemical study of intimal microvessels in coronary atherosclerosis. Am J Pathol 1993; 143: 164-172.
55 Scher AM. Absence of atherosclerosis in human intramyocardial coronary arteries: a neglected phenomenon. Atherosclerosis 2000; 149: 1-3.
56 Langheinrich AC, Michniewicz A, Bohle RM. et al. Vasa vasorum neovascularization and lesion distribution among different vascular beds in ApoE(-/-)/ LDL(-/-) double knockout mice. Atherosclerosis 2007; 191: 73-81.
57 Moghadasian MH, McManus BM, Nguyen LB. et al. Pathophysiology of apolipoprotein E deficiency in mice: relevance to apo E-related disorders in humans. FASEB J 2001; 15: 2623-2630.
58 Okuyama S, Okuyama J, Okuyama J. et al. The arterial circle of Willis of the mouse helps to decipher secrets of cerebral vascular accidents in the human. Med Hypotheses 2004; 63: 997-1009.
59 Sollberg LA, McGarry PA, Moossy J. et al. Severity of atherosclerosis in cerebral arteries, coronary arteries, and aortas. Ann NY Acad Sci 1968; 149: 956-973.
60 Vink A, Schoneveld AH, Poppen M. et al. Morphometric and immunohistochemical characterization of the intimal layer throughout the arterial system of elderly humans. J Anat 2002; 200: 97-103.
61 Heistad DD. Unstable coronary-artery plaques. N Engl J Med 2003; 349: 2285-2287.
62 Kolodgie FD, Gold HK, Burke AP. et al. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 2003; 349: 2316-2325.
63 Yuan XM, Anders WL, Olsson AG. et al. Iron in human atheroma and LDL oxidation by macrophages following erythrophagocytosis. Atherosclerosis 1996; 124: 61-73.
64 Lee TS, Lee FY, Pang JH. et al. Erythrophagocytosis and iron deposition in atherosclerotic lesions. Chin J Physiol (China) 1999; 42: 17-23.
65 de Nooijer R, Verkleij CJ, von der Thusen JH. et al. Lesional overexpression of matrix metalloproteinase-9 promotes intraplaque hemorrhage in advanced lesions but not at earlier stages of atherogenesis. Arterioscler Thromb Vasc Biol 2006; 26: 340-346.
66 Jeziorska M, Woolley DE. Neovascularization in early atherosclerotic lesions of human carotid arteries: its potential contribution to plaque development. Hum Pathol 1999; 30: 919-925.
67 Jeziorska M, Woolley DE. Local neovascularization and cellular composition within vulnerable regions of atherosclerotic plaques of human carotid arteries. J Pathol 1999; 188: 189-196.
68 Virmani R, Kolodgie FD, Burke AP. et al. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol 2005; 25: 2054-2061.
69 Moreno PR, Purushothaman KR, Fuster V. et al. Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation 2004; 110: 2032-2038.
70 Mazurek T, Zhang L, Zalewski A. et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 2003; 108: 2460-2466.
71 Zhang L, Zalewski A, Liu Y. et al Diabetes-induced oxidative stress and low-grade inflammation in porcine coronary arteries. Circulation 2003; 108: 472-478.
72 Langheinrich AC, Michniewicz A, Sedding DG. et al. Correlation of vasa vasorum neovascularization and plaque progression in aortas of apolipoprotein E(-/-)/ low-density lipoprotein(-/-) double knockout mice. Arterioscler Thromb Vasc Biol 2006; 26: 347-352.
73 Langheinrich AC, Michniewicz A, Sedding DG. et al. Quantitative X-ray imaging of intraplaque hemorrhage in aortas of ApoE-/-/LDL-/- double knockout mice. Invest Radiol 2007; 42: 263-273.