J Clin Neurol.  2014 Apr;10(2):133-139. 10.3988/jcn.2014.10.2.133.

Association between Ischemic Stroke and Vascular Shear Stress in the Carotid Artery

• Jeong SK
• Lee JY
• Rosenson R

• KMID: 2287531
• DOI: http://doi.org/10.3988/jcn.2014.10.2.133

Abstract

BACKGROUND AND PURPOSE
Vascular shear stress is essential for maintaining the morphology and function of endothelial cells. We hypothesized that shear stress in the internal carotid artery (ICA) may differ between patients with ischemic stroke and healthy control subjects.
METHODS
ICA shear stress was calculated in 143 controls and 122 patients with ischemic stroke who had a normal ICA or an ICA with <50% stenosis. The stroke group included patients who presented with a first-ever or recurrent ischemic stroke but excluded cardioembolic stroke and uncertain etiologies. Of the 122 patients, 107 (87.7%) and 15 (12.3%) patients were categorized as first-ever and recurrent stroke, respectively.
RESULTS
Carotid diameters were significantly larger, and both peak-systolic and end-diastolic velocities were significantly lower in patients with ischemic stroke than in controls (all p values <0.05). Mean values of peak-systolic and end-diastolic shear stress in both ICAs were significantly lower in patients with ischemic stroke in models that adjusted for age, sex, and vascular risk factors (p for trend <0.05). The ICA shear stress was lowest in patients with recurrent stroke or the subtype of small-vessel occlusion. Higher peak-systolic and end-diastolic shear stresses in both ICAs were independently and negatively associated with ischemic stroke after adjusting for potential confounders (all p values <0.05).
CONCLUSIONS
ICA shear stresses were significantly lower in patients with ischemic stroke than in control subjects. Future studies should attempt to define the causal relationship between carotid arterial shear stress and ischemic stroke.

Keyword

carotid artery; hemodynamics; ischemic stroke; shear stress

MeSH Terms

Carotid Arteries*
Carotid Artery, Internal
Constriction, Pathologic
Endothelial Cells
Hemodynamics
Humans
Risk Factors
Stroke*

Reference

1. Cunningham KS, Gotlieb AI. The role of shear stress in the pathogenesis of atherosclerosis. Lab Invest. 2005; 85:9–23.

2. Giannoglou GD, Soulis JV, Farmakis TM, Farmakis DM, Louridas GE. Haemodynamic factors and the important role of local low static pressure in coronary wall thickening. Int J Cardiol. 2002; 86:27–40.

3. Nesbitt WS, Westein E, Tovar-Lopez FJ, Tolouei E, Mitchell A, Fu J, et al. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med. 2009; 15:665–673.

4. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA. 1999; 282:2035–2042.

5. Lee SW, Antiga L, Spence JD, Steinman DA. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke. 2008; 39:2341–2347.

6. Groen HC, Gijsen FJ, van der Lugt A, Ferguson MS, Hatsukami TS, van der Steen AF, et al. Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke. 2007; 38:2379–2381.

7. Palm-Meinders IH, Box FM, de Craen AJ, Blauw GJ, van Buchem MA, van der Grond J. Diastolic wall shear stress in the internal carotid artery is associated with different cardiovascular risk factors than systolic wall shear stress. Cerebrovasc Dis. 2009; 28:185–190.

8. Carallo C, Lucca LF, Ciamei M, Tucci S, de Franceschi MS. Wall shear stress is lower in the carotid artery responsible for a unilateral ischemic stroke. Atherosclerosis. 2006; 185:108–113.

9. Rothwell PM, Warlow CP. Low risk of ischemic stroke in patients with reduced internal carotid artery lumen diameter distal to severe symptomatic carotid stenosis: cerebral protection due to low poststenotic flow? On behalf of the European Carotid Surgery Trialists' Collaborative Group. Stroke. 2000; 31:622–630.

10. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993; 24:35–41.

11. Hardie K, Hankey GJ, Jamrozik K, Broadhurst RJ, Anderson C. Ten-year risk of first recurrent stroke and disability after first-ever stroke in the Perth Community Stroke Study. Stroke. 2004; 35:731–735.

12. Touboul PJ, Hennerici MG, Meairs S, Adams H, Amarenco P, Bornstein N, et al. Mannheim carotid intima-media thickness consensus (2004-2006). An update on behalf of the Advisory Board of the 3rd and 4th Watching the Risk Symposium, 13th and 15th European Stroke Conferences, Mannheim, Germany, 2004, and Brussels, Belgium, 2006. Cerebrovasc Dis. 2007; 23:75–80.

13. Petersen C, Peçanha PB, Venneri L, Pasanisi E, Pratali L, Picano E. The impact of carotid plaque presence and morphology on mortality outcome in cardiological patients. Cardiovasc Ultrasound. 2006; 4:16.

14. Grant EG, Benson CB, Moneta GL, Alexandrov AV, Baker JD, Bluth EI, et al. Carotid artery stenosis: gray-scale and Doppler US diagnosis--Society of Radiologists in Ultrasound Consensus Conference. Radiology. 2003; 229:340–346.

15. Jiang Y, Kohara K, Hiwada K. Association between risk factors for atherosclerosis and mechanical forces in carotid artery. Stroke. 2000; 31:2319–2324.

16. Guyton AC, Hall JE. Textbook of Medical Physiology. 10th ed. Philadelphia, PA: W.B. Saunders;2000.

17. Cho YI, Kensey KR. Effects of the non-Newtonian viscosity of blood on flows in a diseased arterial vessel. Part 1: Steady flows. Biorheology. 1991; 28:241–262.

18. Schulz UG, Rothwell PM. Major variation in carotid bifurcation anatomy: a possible risk factor for plaque development? Stroke. 2001; 32:2522–2529.

19. Kim JT, Lee SH, Hur N, Jeong SK. Blood flow velocities of cerebral arteries in lacunar infarction and other ischemic strokes. J Neurol Sci. 2011; 308:57–61.

20. Irace C, Cortese C, Fiaschi E, Carallo C, Farinaro E, Gnasso A. Wall shear stress is associated with intima-media thickness and carotid atherosclerosis in subjects at low coronary heart disease risk. Stroke. 2004; 35:464–468.

21. Levesque MJ, Liepsch D, Moravec S, Nerem RM. Correlation of endothelial cell shape and wall shear stress in a stenosed dog aorta. Arteriosclerosis. 1986; 6:220–229.

22. Wilcox JN, Subramanian RR, Sundell CL, Tracey WR, Pollock JS, Harrison DG, et al. Expression of multiple isoforms of nitric oxide synthase in normal and atherosclerotic vessels. Arterioscler Thromb Vasc Biol. 1997; 17:2479–2488.

23. Sheikh S, Rainger GE, Gale Z, Rahman M, Nash GB. Exposure to fluid shear stress modulates the ability of endothelial cells to recruit neutrophils in response to tumor necrosis factor-alpha: a basis for local variations in vascular sensitivity to inflammation. Blood. 2003; 102:2828–2834.

24. Zhu CH, Ying DJ, Mi JH, Zhu XH, Sun JS, Cui XP. Low shear stress regulates monocyte adhesion to oxidized lipid-induced endothelial cells via an IkappaBalpha dependent pathway. Biorheology. 2004; 41:127–137.

25. Khatri JJ, Johnson C, Magid R, Lessner SM, Laude KM, Dikalov SI, et al. Vascular oxidant stress enhances progression and angiogenesis of experimental atheroma. Circulation. 2004; 109:520–525.

26. Lee SH, Hur N, Jeong SK. Geometric analysis and blood flow simulation of basilar artery. J Atheroscler Thromb. 2012; 19:397–401.

27. del Zoppo GJ. Virchow's triad: the vascular basis of cerebral injury. Rev Neurol Dis. 2008; 5:Suppl 1. S12–S21.

28. Zhang Y, He X, Liu D, Wu G, Chen X, Ma H, et al. Enhanced external counterpulsation attenuates atherosclerosis progression through modulation of proinflammatory signal pathway. Arterioscler Thromb Vasc Biol. 2010; 30:773–780.

29. Jeong SK, Cho YI, Duey M, Rosenson RS. Cardiovascular risks of anemia correction with erythrocyte stimulating agents: should blood viscosity be monitored for risk assessment? Cardiovasc Drugs Ther. 2010; 24:151–160.