Background: When an internal carotid artery (ICA) occludes, a patient may develop cerebral infarction (CI). We investigated whether CI caused by ICA occlusion (ICAO) is associated with collateral flow through the anterior and posterior communicating arteries (ACoA and PCoA). Methods: In 100 patients with ICAO, we investigated CI and white matter disease by performing an MRI and the anatomy of the ACoA and PCoA were investigated by performing magnetic resonance angiography. All patients were divided into the symptomatic CI group or the no-CI group. The collateral flow pathway was estimated by the anterior cerebral artery (ACA)-PCoA score and the collateral flow volume after ICAO was estimated by the middle cerebral artery (MCA) flow score, based on how well the MCA was visualized. Results: Of 100 patients with ICAO, the symptomatic CI group included 36 patients. ACA-PCoA score and white matter disease grades were significantly higher in the CI group (indicating poor collateral flow). More than 80% of patients with an ACA-PCoA score of 4 (poor collateral) experienced symptomatic CI. Thirty-one symptomatic CI patients (86%) had an MCA flow score of 1 or 2 (decreased MCA flow). Conclusion: The ACA-PCoA score and white matter disease grade may suggest an increased risk of CI following ICAO.

Keywords:
Circle of Willis, Internal carotid artery, Cerebral infarction, Cerebral blood flow, White matter disease
1.
North American Symptomatic Carotid Endarterectomy Trial Collaborators: Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 1991;325:445-453.
2.
Miralles M, Dolz JL, Cotillas J, Aldoma J, Santiso MA, Gimenez A, Capdevila A, Cairols MA: The role of the circle of Willis in carotid occlusion: assessment with phase contrast MR angiography and transcranial duplex. Eur J Vasc Endovasc Surg 1995;10:424-430.
3.
Bisschops RH, Klijn CJ, Kappelle LJ, van Huffelen AC, van der Grond J: Collateral flow and ischemic brain lesions in patients with unilateral carotid artery occlusion. Neurology 2003;60:1435-1441.
4.
Kim JT, Park MS, Choi KH, Nam TS, Choi SM, Cho KH: Clinical implications of collateral middle cerebral artery flow in acute ischaemic stroke with internal carotid artery occlusion. Eur J Neurol 2011;18:1384-1390.
5.
Kluytmans M, van der Grond J, van Everdingen KJ, Klijn CJ, Kappelle LJ, Viergever MA: Cerebral hemodynamics in relation to patterns of collateral flow. Stroke 1999;30:1432-1439.
6.
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.
7.
Hendrikse J, Hartkamp MJ, Hillen B, Mali WP, van der Grond J: Collateral ability of the Circle of Willis in patients with unilateral internal carotid artery occlusion: border zone infarcts and clinical symptoms. Stroke 2001;32:2768-2773.
8.
Hedera P, Bujdakova J, Traubner P, Pancak J: Stroke risk factors and development of collateral flow in carotid occlusive disease. Acta Neurol Scand 1998;98:182-186.
9.
Bae YJ, Jung C, Kim JH, Choi BS, Kim E: Quantitative magnetic resonance angiography in internal carotid artery occlusion with primary collateral pathway. J Stroke 2015;17:320-326.
10.
Kim DE, Lee KB, Roh H, Ahn MY, Roh JK: Association of internal border zone infarction with middle cerebral artery steno-occlusion. Eur Neurol 2010;64:178-185.
11.
Ay H, Arsava EM, Rosand J, Furie KL, Singhal AB, Schaefer PW, Wu O, Gonzalez RG, Koroshetz WJ, Sorensen AG: Severity of leukoaraiosis and susceptibility to infarct growth in acute stroke. Stroke 2008;39:1409-1413.
12.
Helenius J, Henninger N: Leukoaraiosis burden significantly modulates the association between infarct volume and national institutes of health stroke scale in ischemic stroke. Stroke 2015;46:1857-1863.
13.
Bernbaum M, Menon BK, Fick G, Smith EE, Goyal M, Frayne R, Coutts SB: Reduced blood flow in normal white matter predicts development of leukoaraiosis. J Cereb Blood Flow Metab 2015;35:1610-1615.
14.
Shinohara Y, Tohgi H, Hirai S, Terashi A, Fukuuchi Y, Yamaguchi T, Okudera T: Effect of the Ca antagonist nilvadipine on stroke occurrence or recurrence and extension of asymptomatic cerebral infarction in hypertensive patients with or without history of stroke (PICA Study). 1. Design and results at enrollment. Cerebrovasc Dis 2007;24:202-209.
15.
Liebeskind DS, Kosinski AS, Lynn MJ, Scalzo F, Fong AK, Fariborz P, Chimowitz MI, Feldmann E; SONIA and WASID Investigators: Noninvasive fractional flow on MRA predicts stroke risk of intracranial stenosis. J Neuroimaging 2015;25:87-91.
16.
Ozgur HT, Kent Walsh T, Masaryk A, Seeger JF, Williams W, Krupinski E, Melgar M, Labadie E: Correlation of cerebrovascular reserve as measured by acetazolamide-challenged SPECT with angiographic flow patterns and intra- or extracranial arterial stenosis. AJNR Am J Neuroradiol 2001;22:928-936.
17.
Tomura N, Sasaki K, Kidani H, Nishii T, Yasuda K, Ishiyama K, Otani T, Sakuma I, Takahashi S, Watarai J, Yanagisawa T, Mizoi K: Reduced perfusion reserve in leukoaraiosis demonstrated using acetazolamide challenge 123I-IMP SPECT. J Comput Assist Tomogr 2007;31:884-887.
18.
Giurgiutiu DV, Yoo AJ, Fitzpatrick K, Chaudhry Z, Leslie-Mazwi T, Schwamm LH, Rost NS: Severity of leukoaraiosis, leptomeningeal collaterals, and clinical outcomes after intra-arterial therapy in patients with acute ischemic stroke. J Neurointerv Surg 2015;7:326-330.
19.
Henninger N, Lin E, Baker SP, Wakhloo AK, Takhtani D, Moonis M: Leukoaraiosis predicts poor 90-day outcome after acute large cerebral artery occlusion. Cerebrovasc Dis 2012;33:525-531.
20.
Karadeli HH, Giurgiutiu DV, Cloonan L, Fitzpatrick K, Kanakis A, Ozcan ME, Schwamm LH, Rost NS: FLAIR vascular hyperintensity is a surrogate of collateral flow and leukoaraiosis in patients with acute stroke due to proximal artery occlusion. J Neuroimaging 2016;26:219-223.
21.
Ishikawa M, Saito H, Yamaguro T, Ikoda M, Ebihara A, Kusaka G, Tanaka Y: Cognitive impairment and neurovascular function in patients with severe steno-occlusive disease of a main cerebral artery. J Neurol Sci 2016;361:43-48.
22.
Katano H, Mase M, Sakurai K, Miyachi S, Yamada K: Revaluation of collateral pathways as escape routes from hyperemia/hyperperfusion following surgical treatment for carotid stenosis. Acta Neurochir (Wien) 2012;154:2139-2148; discussion 2148-2149.
23.
Arboix A, Cabeza N, Garcia-Eroles L, Massons J, Oliveres M, Targa C, Balcells M: Relevance of transient ischemic attack to early neurological recovery after nonlacunar ischemic stroke. Cerebrovasc Dis 2004;18:304-311.
24.
Grau-Olivares M, Arboix A: Mild cognitive impairment in stroke patients with ischemic cerebral small-vessel disease: a forerunner of vascular dementia? Expert Rev Neurother 2009;9:1201-1217.
© 2016 S. Karger AG, Basel
2016
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.