Background: Autopsy studies show a higher prevalence of circle of Willis anomalies in brains with signs of ischemic infarction. Our goal was to examine the collateral function of the circle of Willis in ischemic stroke patients and to assess in a case-control study if a collateral deficient circle of Willis is a risk factor for ischemic stroke in patients with severe internal carotid artery (ICA) occlusive disease. Methods: Our case-control study included 109 patients with an acute ischemic stroke in the anterior circulation and 113 patients with peripheral arterial disease and no known history of cerebral ischemia. The collateral function of the anterior and posterior communicating arteries of the circle of Willis was assessed by means of transcranial color-coded duplex ultrasonography (TCCD) and carotid compression tests. Results: TCCD was successfully performed in 75 case patients (mean age 64 years, range 41–91 years) and in 100 control patients (mean age 61 years, range 35–89 years). In 26 cases and 19 controls, a ≧70% stenosis or occlusion of the ICA was found. A nonfunctional anterior collateral pathway in the circle of Willis was found in 33% of the cases and in 6% of the controls (p < 0.001). The posterior collateral pathway was nonfunctional in 57% of the cases and in 43% of the controls (p = 0.02). In patients with severe ICA occlusive disease, the odds ratios of a nonfunctional anterior and a nonfunctional posterior collateral pathway were 7.33 (95% confidence interval, CI, = 1.19–76.52) and 3.00 (95% CI = 0.77–12.04), respectively. Conclusions: Patients who suffer ischemic stroke in the anterior circulation have a higher incidence of collateral deficient circles of Willis than those with atherosclerotic vascular disease without ischemic cerebrovascular disease. The presence of a nonfunctional anterior collateral pathway in the circle of Willis in patients with severe ICA occlusive disease is strongly associated with ischemic stroke.

Keywords:
Circle of Willis, Collateral circulation, Cerebral ischemia, Transcranial ultrasound
1.
Alpers BJ, Berry RG: Circle of Willis in cerebral vascular disorders. Arch Neurol 1963;8:398–402.
2.
Battacharji SK, Hutchinson EC, McCall AJ: The circle of Willis: The incidence of developmental abnormalities in normal and infarcted brains. Brain 1967;90:747–758.
3.
Ringelstein EB, Weiller C, Weckesser M, Weckesser S: Cerebral vasomotor reactivity is significantly reduced in low-flow as compared to thromboembolic infarctions: The key role of the circle of Willis. J Neurol Sci 1994;121:103–109.
4.
Schomer DF, Marks MP, Steinberg GK, Johnstone IM, Boothroyd DB, Ross MR, Pelc NJ, Enzmann DR: The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. N Engl J Med 1994;330:1565–1570.
5.
Hedera P, Bujdakova J, Traubner P: Effect of collateral flow patterns on outcome of carotid occlusion. Eur Neurol 1995;35:212–216.
6.
Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJM, for the North American Symptomatic Carotid Endarterectomy Trial (NASCET) Group: Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 2000;31:128–132.
7.
Vernieri F, Pasqualetti P, Matteis M, Passarelli F, Troisi E, Rossini PM, Caltagirone C, Silvestrini M: Effect of collateral blood flow and cerebral vasomotor reactivity on the outcome of carotid artery occlusion. Stroke 2001;32:1552–1558.
8.
Caplan LR: Brain embolism, revisited. Neurology 1993;43:1281–1287.
9.
Barnett HJM, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, Rankin RN, Clagett GP, Hachinski VC, Sackett DL, Thorpe KE, Meldrum HE, for the North American Symptomatic Carotid Endarterectomy Trial Collaborators: Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. N Engl J Med 1998;339:1415–1425.
10.
Kleiser B, Widder B: Course of carotid artery occlusions with impaired cerebrovascular reactivity. Stroke 1992;23:171–174.
11.
Klijn CJM, Kappelle J, Tulleken CAF, Van Gijn J: Symptomatic carotid artery occlusion: A reappraisal of hemodynamic factors. Stroke 1997;28:2084–2093.
12.
Grubb RL, Derdeyn CP, Fritsch SM, Carpenter DA, Yundt KD, Videen TO, Spitznagel EL, Powers WJ: Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. JAMA 1998;280:1055–1060.
13.
Caplan LR, Hennerici M: Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism and ischemic stroke. Arch Neurol 1998;55:1475–1482.
14.
Mull M, Schwarz M, Thron A: Cerebral hemispheric low-flow infarcts in arterial occlusive disease: Lesion patterns and angiomorphological conditions. Stroke 1997;28:118–123.
15.
Silvestrini M, Vernieri F, Troisi E, Passarelli F, Matteis M, Pasqualetti P, Rossini PM, Caltagirone C: Cerebrovascular reactivity in carotid artery occlusion: Possible implications for surgical management of selected groups of patients. Acta Neurol Scand 1999;99:187–191.
16.
Bogdahn U, Becker G, Winkler J, Greiner K, Perez J, Meurers B: Transcranial color-coded real-time sonography in adults. Stroke 1990;21:1680–1688.
17.
Hetzel A, von Reutern G-M, Wernz MG, Droste DW, Schumacher M: The carotid compression test for therapeutic occlusion of the internal carotid artery: Comparison of angiography with transcranial Doppler sonography. Cerebrovasc Dis 2000;10:194–199.
18.
Hoksbergen AWJ, Fülesdi B, Legemate DA, Csiba L: The collateral configuration of the circle of Willis: Transcranial color-coded duplex ultrasonography and comparison with postmortem anatomy. Stroke 2000;31:1346–1351.
19.
Baumgartner RW, Baumgartner I, Mattle HP, Schroth G: Transcranial color-coded duplex sonography in the evaluation of collateral flow through the circle of Willis. Am J Neuroradiol 1997;18:127–133.
20.
Van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJA, van Gijn J: Interobserver agreement for the assessment of handicap in stroke patients. Stroke 1988;19:604–607.
21.
Hoksbergen AWJ, Legemate DA, Ubbink, DT, Jacobs MJHM: Collateral variations in the circle of Willis in an atherosclerotic population assessed by means of transcranial color-coded duplex ultrasonography. Stroke 2000;31:1661–1666.
22.
Moneta GL, Edwards JM, Chitwood RW, Taylor LM, Lee RW, Cummings CA, Porter JM: Correlation of North American Symptomatic Carotid Endarterectomy Trial (NASCET) angiographic definition of 70% to 99% internal carotid artery stenosis with duplex scanning. J Vasc Surg 1993;17:152–159.
23.
Aaslid R, Markwalder T, Nornes H: Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982;57:769–774.
24.
Tsuchiya T, Yasaka M, Yamaguchi T, Kimura K, Omae T: Imaging of the basal cerebral arteries and measurement of blood flow velocity in adults by using transcranial real-time color flow Doppler sonography. Am J Neuroradiol 1991;12:497–502.
25.
Chaudhuri R, Padayachee TS, Lewis RR, Gosling RG, Cox TCS: Non-invasive assessment of the circle of Willis using transcranial pulsed Doppler ultrasound with angiographic correlation. Clin Radiol 1992;46:193–197.
26.
Keunen RWM: Transcranial Doppler Sonography of the Cerebral Circulation in Occlusive Cerebrovascular Disease (thesis). Nijmegen, Benda, 1990.
27.
Baumgartner RW, Baumgartner I, Schroth G: Diagnostic criteria for transcranial colour-coded duplex sonography evaluation of cross-flow through the circle of Willis in unilateral obstructive carotid artery disease. J Neurol 1996;243:516–521.
28.
Hoksbergen AWJ, Legemate DA, Ubbink DT, Jacobs MJHM: Success rate of transcranial color-coded duplex ultrasonography in visualizing the basal cerebral arteries in vascular patients over 60 years of age. Stroke 1999;30:1450–1455.
29.
Hofmeijer J, Klijn CJM, Kappelle LJ, van Huffelen AC, van Gijn J: Collateral circulation via the ophthalmic artery or leptomeningeal vessels is associated with impaired cerebral vasoreactivity in patients with symptomatic carotid artery occlusion. Cerebrovasc Dis 2002;14:22–26.
30.
Schneider PA, Rossman ME, Bernstein EF, Ringelstein EB, Otis SM: Noninvasive assessment of cerebral collateral blood supply through the ophthalmic artery. Stroke 1991;22:31–36.
31.
Hennerici M, Daffertshofer M, Jakobs L: Failure to identify cerebral infarct mechanisms from topography of vascular territory lesions. Am J Neuroradiol 1998;19:1067–1074.
32.
Hedera P, Bujdáková J, Traubner P, Pancák J: Stroke risk factors and development of collateral flow in carotid occlusive disease. Acta Neurol Scand 1998;98:182–186.
33.
Lopez-Bresnahan MV, Kearse LA, Yanez P, Young TI: Anterior communicating artery collateral flow protection against ischemic change during carotid endarterectomy. J Neurosurg 1993;79:379–382.
34.
Cassot F, Vergeur V, Bossuet P, Hillen B, Zagzoule M, Marc-Vergnes JP: Effects of anterior communicating artery diameter on cerebral hemodynamics in internal carotid artery disease. Circulation 1995;92:3122–3131.
35.
Doblar DD, Plyushcheva NV, Jordan W, McDowell H: Predicting the effect of carotid artery occlusion during carotid endarterectomy: Comparing transcranial Doppler measurements and cerebral angiography. Stroke 1998;28:2038–2042.
36.
Kluytmans M, van der Grond J, van Everdingen KJ, Klijn CJM, Kappelle LJ, Viergever MA: Cerebral hemodynamics in relation to patterns of collateral flow. Stroke 1999;30:1432–1439.
37.
Hoksbergen AWJ, Legemate DA, Ubbink, DT, de Vos HJ, Jacobs MJHM: Influence of the collateral function of the circle of Willis on hemispherical perfusion during carotid occlusion as assessed by transcranial colour-coded duplex ultrasonography. Eur J Vasc Endovasc Surg 1999;17:486–492.
38.
Droste DW, Jürgens R, Weber S, Tietje R, Ringelstein EB: Benefit of echocontrast-enhanced transcranial color-coded duplex ultrasound in the assessment of intracranial collateral pathways. Stroke 2000;31:920–923.
39.
Gahn G, Hallmeyer-Elgner S, Kunz A, Straube T, Bourquain H, Reichmann H, von Kummer R: Echo-enhanced transcranial color-coded duplex sonography to study collateral blood flow in patients with symptomatic obstructions of the internal carotid artery and limited acoustic bone windows. Cerebrovasc Dis 2001;11:107–112.
40.
Droste DW, Llull JB, Pezzoli C, Bogdahn U, Kaps M: Sonovue® (BR1), a new long-acting echocontrast agent, improves transcranial colour-coded duplex ultrasonic imaging. Cerebrovasc Dis 2002;14:27–32.
© 2003 S. Karger AG, Basel
2003
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.