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Published in: Clinical Neuroradiology 3/2018

Open Access 01-09-2018 | Original Article

Internal Carotid Artery Stenosis and Collateral Recruitment in Stroke Patients

Authors: Jan W. Dankbaar, Kelly G. P. Kerckhoffs, Alexander D. Horsch, Irene C. van der Schaaf, L. Jaap Kappelle, Birgitta K. Velthuis, DUST investigators

Published in: Clinical Neuroradiology | Issue 3/2018

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Abstract

Purpose

Leptomeningeal collaterals improve outcome in stroke patients. There is great individual variability in their extent. Internal carotid artery (ICA) stenosis may lead to more extensive recruitment of leptomeningeal collaterals. The purpose of this study was to evaluate the association of pre-existing ICA stenosis with leptomeningeal collateral filling visualized with computed tomography perfusion (CTP).

Methods

From a prospective acute ischemic stroke cohort, patients were included with an M1 middle cerebral artery (MCA) occlusion and absent ipsilateral, extracranial ICA occlusion. ICA stenosis was determined on admission CT angiography (CTA). Leptomeningeal collaterals were graded as good (>50%) or poor (≤50%) collateral filling in the affected MCA territory on CTP-derived vessel images of the admission scan. The association between ipsilateral ICA stenosis ≥70% and extent of collateral filling was analyzed using logistic regression. In a multivariable analysis the odds ratio (OR) of ICA stenosis ≥70% was adjusted for complete circle of Willis, gender and age.

Results

We included 188 patients in our analyses, 50 (26.6%) patients were classified as having poor collateral filling and 138 (73.4%) as good. Of the patients 4 with poor collateral filling had an ICA stenosis ≥70% and 14 with good collateral filling. Unadjusted and adjusted ORs of ICA stenosis ≥70% for good collateral filling were 1.30 (0.41–4.15) and 2.67 (0.81–8.77), respectively. Patients with poor collateral filling had a significantly worse outcome (90-day modified Rankin scale 3–6; 80% versus 52%, p = 0.001).

Conclusion

No association was found between pre-existing ICA stenosis and extent of CTP derived collateral filling in patients with an M1 occlusion.
Literature
1.
go back to reference Souza LC, Yoo AJ, Chaudhry ZA, Payabvash S, Kemmling A, Schaefer PW, Hirsch JA, Furie KL, González RG, Nogueira RG, Lev MH. Malignant CTA collateral profile is highly specific for large admission DWI infarct core and poor outcome in acute stroke. AJNR Am J Neuroradiol. 2012;33:1331–6.CrossRefPubMedPubMedCentral Souza LC, Yoo AJ, Chaudhry ZA, Payabvash S, Kemmling A, Schaefer PW, Hirsch JA, Furie KL, González RG, Nogueira RG, Lev MH. Malignant CTA collateral profile is highly specific for large admission DWI infarct core and poor outcome in acute stroke. AJNR Am J Neuroradiol. 2012;33:1331–6.CrossRefPubMedPubMedCentral
2.
go back to reference Menon BK, Smith EE, Modi J, Patel SK, Bhatia R, Watson TW, Hill MD, Demchuk AM, Goyal M. Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions. AJNR Am J Neuroradiol. 2011;32:1640–5.CrossRefPubMed Menon BK, Smith EE, Modi J, Patel SK, Bhatia R, Watson TW, Hill MD, Demchuk AM, Goyal M. Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions. AJNR Am J Neuroradiol. 2011;32:1640–5.CrossRefPubMed
3.
go back to reference Maas MB, Lev MH, Ay H, Singhal AB, Greer DM, Smith WS, Harris GJ, Halpern E, Kemmling A, Koroshetz WJ, Furie KL. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke. 2009;40:3001–5.CrossRefPubMedPubMedCentral Maas MB, Lev MH, Ay H, Singhal AB, Greer DM, Smith WS, Harris GJ, Halpern E, Kemmling A, Koroshetz WJ, Furie KL. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke. 2009;40:3001–5.CrossRefPubMedPubMedCentral
4.
go back to reference Tan IY1, Demchuk AM, Hopyan J, Zhang L, Gladstone D, Wong K, Martin M, Symons SP, Fox AJ, Aviv RI. CT angiography clot burden score and collateral score: Correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. AJNR Am J Neuroradiol. 2009;30:525–31.CrossRefPubMed Tan IY1, Demchuk AM, Hopyan J, Zhang L, Gladstone D, Wong K, Martin M, Symons SP, Fox AJ, Aviv RI. CT angiography clot burden score and collateral score: Correlation with clinical and radiologic outcomes in acute middle cerebral artery infarct. AJNR Am J Neuroradiol. 2009;30:525–31.CrossRefPubMed
5.
go back to reference Christoforidis GA, Mohammad Y, Kehagias D, Avutu B, Slivka AP. Angiographic assessment of pial collaterals as a prognostic indicator following intra-arterial thrombolysis for acute ischemic stroke. AJNR Am J Neuroradiol. 2005;26:1789–97.PubMed Christoforidis GA, Mohammad Y, Kehagias D, Avutu B, Slivka AP. Angiographic assessment of pial collaterals as a prognostic indicator following intra-arterial thrombolysis for acute ischemic stroke. AJNR Am J Neuroradiol. 2005;26:1789–97.PubMed
6.
go back to reference Calleja AI, Cortijo E, García-Bermejo P, Gómez RD, Pérez-Fernández S, Del Monte JM, Muñoz MF, Fernández-Herranz R, Arenillas JF. Collateral circulation on perfusion-computed tomography-source images predicts the response to stroke intravenous thrombolysis. Eur J Neurol. 2013;20:795–802.CrossRefPubMed Calleja AI, Cortijo E, García-Bermejo P, Gómez RD, Pérez-Fernández S, Del Monte JM, Muñoz MF, Fernández-Herranz R, Arenillas JF. Collateral circulation on perfusion-computed tomography-source images predicts the response to stroke intravenous thrombolysis. Eur J Neurol. 2013;20:795–802.CrossRefPubMed
7.
go back to reference Liebeskind DS, Tomsick TA, Foster LD, Yeatts SD, Carrozzella J, Demchuk AM, Jovin TG, Khatri P, von Kummer R, Sugg RM, Zaidat OO, Hussain SI, Goyal M, Menon BK, Al Ali F, Yan B, Palesch YY, Broderick JP; IMS III Investigators. Collaterals at angiography and outcomes in the Interventional Management of Stroke (IMS) III trial. Stroke. 2014;45:759–64.CrossRefPubMedPubMedCentral Liebeskind DS, Tomsick TA, Foster LD, Yeatts SD, Carrozzella J, Demchuk AM, Jovin TG, Khatri P, von Kummer R, Sugg RM, Zaidat OO, Hussain SI, Goyal M, Menon BK, Al Ali F, Yan B, Palesch YY, Broderick JP; IMS III Investigators. Collaterals at angiography and outcomes in the Interventional Management of Stroke (IMS) III trial. Stroke. 2014;45:759–64.CrossRefPubMedPubMedCentral
8.
go back to reference Marks MP, Lansberg MG, Mlynash M, Olivot JM, Straka M, Kemp S, McTaggart R, Inoue M, Zaharchuk G, Bammer R, Albers GW; Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution 2 Investigators. Effect of collateral blood flow on patients undergoing endovascular therapy for acute ischemic stroke. Stroke. 2014;45:1035–9.CrossRefPubMedPubMedCentral Marks MP, Lansberg MG, Mlynash M, Olivot JM, Straka M, Kemp S, McTaggart R, Inoue M, Zaharchuk G, Bammer R, Albers GW; Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution 2 Investigators. Effect of collateral blood flow on patients undergoing endovascular therapy for acute ischemic stroke. Stroke. 2014;45:1035–9.CrossRefPubMedPubMedCentral
10.
11.
go back to reference Malik N, Hou Q, Vagal A, Patrie J, Xin W, Michel P, Eskandari A, Jovin T, Wintermark M. Demographic and clinical predictors of leptomeningeal collaterals in stroke patients. J Stroke Cerebrovasc Dis. 2014;23:2018–22.CrossRefPubMed Malik N, Hou Q, Vagal A, Patrie J, Xin W, Michel P, Eskandari A, Jovin T, Wintermark M. Demographic and clinical predictors of leptomeningeal collaterals in stroke patients. J Stroke Cerebrovasc Dis. 2014;23:2018–22.CrossRefPubMed
12.
go back to reference Koerselman J, van der Graaf Y, de Jaegere PP, Grobbee DE. Coronary collaterals: An important and underexposed aspect of coronary artery disease. Circulation. 2003;107:2507–11.CrossRefPubMed Koerselman J, van der Graaf Y, de Jaegere PP, Grobbee DE. Coronary collaterals: An important and underexposed aspect of coronary artery disease. Circulation. 2003;107:2507–11.CrossRefPubMed
13.
go back to reference Romero JR, Pikula A, Nguyen TN, Nien YL, Norbash A, Babikian VL. Cerebral collateral circulation in carotid artery disease. Curr Cardiol Rev. 2009;5:279–88.CrossRefPubMedPubMedCentral Romero JR, Pikula A, Nguyen TN, Nien YL, Norbash A, Babikian VL. Cerebral collateral circulation in carotid artery disease. Curr Cardiol Rev. 2009;5:279–88.CrossRefPubMedPubMedCentral
14.
go back to reference Lima FO, Furie KL, Silva GS, Lev MH, Camargo EC, Singhal AB, Harris GJ, Halpern EF, Koroshetz WJ, Smith WS, Yoo AJ, Nogueira RG. The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke. 2010;41:2316–22.CrossRefPubMedPubMedCentral Lima FO, Furie KL, Silva GS, Lev MH, Camargo EC, Singhal AB, Harris GJ, Halpern EF, Koroshetz WJ, Smith WS, Yoo AJ, Nogueira RG. The pattern of leptomeningeal collaterals on CT angiography is a strong predictor of long-term functional outcome in stroke patients with large vessel intracranial occlusion. Stroke. 2010;41:2316–22.CrossRefPubMedPubMedCentral
15.
go back to reference Smit EJ, Vonken EJ, van Seeters T, Dankbaar JW, van der Schaaf IC, Kappelle LJ, van Ginneken B, Velthuis BK, Prokop M. Timing-invariant imaging of collateral vessels in acute ischemic stroke. Stroke. 2013;44:2194–9.CrossRefPubMed Smit EJ, Vonken EJ, van Seeters T, Dankbaar JW, van der Schaaf IC, Kappelle LJ, van Ginneken B, Velthuis BK, Prokop M. Timing-invariant imaging of collateral vessels in acute ischemic stroke. Stroke. 2013;44:2194–9.CrossRefPubMed
16.
go back to reference Frölich AM, Wolff SL, Psychogios MN, Klotz E, Schramm R, Wasser K, Knauth M, Schramm P. Time-resolved assessment of collateral flow using 4D CT angiography in large-vessel occlusion stroke. Eur Radiol. 2014;24:390–6.CrossRefPubMed Frölich AM, Wolff SL, Psychogios MN, Klotz E, Schramm R, Wasser K, Knauth M, Schramm P. Time-resolved assessment of collateral flow using 4D CT angiography in large-vessel occlusion stroke. Eur Radiol. 2014;24:390–6.CrossRefPubMed
17.
go back to reference Menon BK, O’Brien B, Bivard A, Spratt NJ, Demchuk AM, Miteff F, Lu X, Levi C, Parsons MW. Assessment of leptomeningeal collaterals using dynamic CT angiography in patients with acute ischemic stroke. J Cereb Blood Flow Metab. 2013;33:365–71.CrossRefPubMed Menon BK, O’Brien B, Bivard A, Spratt NJ, Demchuk AM, Miteff F, Lu X, Levi C, Parsons MW. Assessment of leptomeningeal collaterals using dynamic CT angiography in patients with acute ischemic stroke. J Cereb Blood Flow Metab. 2013;33:365–71.CrossRefPubMed
18.
go back to reference van Seeters T, Biessels GJ, van der Schaaf IC, Dankbaar JW, Horsch AD, Luitse MJ, Niesten JM, Mali WP, Kappelle LJ, van der Graaf Y, Velthuis BK; DUST investigators. Prediction of outcome in patients with suspected acute ischaemic stroke with CT perfusion and CT angiography: The dutch acute stroke trial (dust) study protocol. BMC Neurol. 2014;14:37.CrossRefPubMedPubMedCentral van Seeters T, Biessels GJ, van der Schaaf IC, Dankbaar JW, Horsch AD, Luitse MJ, Niesten JM, Mali WP, Kappelle LJ, van der Graaf Y, Velthuis BK; DUST investigators. Prediction of outcome in patients with suspected acute ischaemic stroke with CT perfusion and CT angiography: The dutch acute stroke trial (dust) study protocol. BMC Neurol. 2014;14:37.CrossRefPubMedPubMedCentral
19.
go back to reference Adams HP Jr1, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd. 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(1):35–41.CrossRefPubMed Adams HP Jr1, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd. 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(1):35–41.CrossRefPubMed
20.
go back to reference van Seeters T, Biessels GJ, Kappelle LJ, van der Schaaf IC, Dankbaar JW, Horsch AD, Niesten JM, Luitse MJ, Majoie CB, Vos JA, Schonewille WJ, van Walderveen MA, Wermer MJ, Duijm LE, Keizer K, Bot JC, Visser MC, van der Lugt A, Dippel DW, Kesselring FO, Hofmeijer J, Lycklama À Nijeholt GJ, Boiten J, van Rooij WJ, de Kort PL, Roos YB, van Dijk EJ, Pleiter CC, Mali WP, van der Graaf Y, Velthuis BK; Dutch acute stroke study (DUST) investigators. The prognostic value of CT angiography and CT perfusion in acute ischemic stroke. Cerebrovasc Dis. 2015;40:258–69.CrossRefPubMed van Seeters T, Biessels GJ, Kappelle LJ, van der Schaaf IC, Dankbaar JW, Horsch AD, Niesten JM, Luitse MJ, Majoie CB, Vos JA, Schonewille WJ, van Walderveen MA, Wermer MJ, Duijm LE, Keizer K, Bot JC, Visser MC, van der Lugt A, Dippel DW, Kesselring FO, Hofmeijer J, Lycklama À Nijeholt GJ, Boiten J, van Rooij WJ, de Kort PL, Roos YB, van Dijk EJ, Pleiter CC, Mali WP, van der Graaf Y, Velthuis BK; Dutch acute stroke study (DUST) investigators. The prognostic value of CT angiography and CT perfusion in acute ischemic stroke. Cerebrovasc Dis. 2015;40:258–69.CrossRefPubMed
21.
go back to reference 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;325:445–53.CrossRef 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;325:445–53.CrossRef
22.
go back to reference Silvennoinen HM, Ikonen S, Soinne L, Railo M, Valanne L. CT angiographic analysis of carotid artery stenosis: Comparison of manual assessment, semiautomatic vessel analysis, and digital subtraction angiography. AJNR Am J Neuroradiol. 2007;28:97–103.CrossRefPubMed Silvennoinen HM, Ikonen S, Soinne L, Railo M, Valanne L. CT angiographic analysis of carotid artery stenosis: Comparison of manual assessment, semiautomatic vessel analysis, and digital subtraction angiography. AJNR Am J Neuroradiol. 2007;28:97–103.CrossRefPubMed
23.
go back to reference Liebeskind DS, Cotsonis GA, Saver JL, Lynn MJ, Cloft HJ, Chimowitz MI; Warfarin–Aspirin Symptomatic Intracranial Disease (WASID) Investigators. Collateral circulation in symptomatic intracranial atherosclerosis. J Cereb Blood Flow Metab. 2011;31:1293–301.CrossRefPubMed Liebeskind DS, Cotsonis GA, Saver JL, Lynn MJ, Cloft HJ, Chimowitz MI; Warfarin–Aspirin Symptomatic Intracranial Disease (WASID) Investigators. Collateral circulation in symptomatic intracranial atherosclerosis. J Cereb Blood Flow Metab. 2011;31:1293–301.CrossRefPubMed
24.
go back to reference Hofmeijer J, Klijn CJ, 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;14:22–6.CrossRefPubMed Hofmeijer J, Klijn CJ, 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;14:22–6.CrossRefPubMed
25.
go back to reference Wintermark M, Luby M, Bornstein NM, Demchuk A, Fiehler J, Kudo K, Lees KR, Liebeskind DS, Michel P, Nogueira RG, Parsons MW, Sasaki M, Wardlaw JM, Wu O, Zhang W, Zhu G, Warach SJ. International survey of acute stroke imaging used to make revascularization treatment decisions. Int J Stroke. 2015;10:759–62.CrossRefPubMedPubMedCentral Wintermark M, Luby M, Bornstein NM, Demchuk A, Fiehler J, Kudo K, Lees KR, Liebeskind DS, Michel P, Nogueira RG, Parsons MW, Sasaki M, Wardlaw JM, Wu O, Zhang W, Zhu G, Warach SJ. International survey of acute stroke imaging used to make revascularization treatment decisions. Int J Stroke. 2015;10:759–62.CrossRefPubMedPubMedCentral
26.
go back to reference Smit EJ, Vonken EJ, Meijer FJ, Dankbaar JW, Horsch AD, van Ginneken B, Velthuis B, van der Schaaf I, Prokop M. Timing-invariant CT angiography derived from CT perfusion imaging in acute stroke: A diagnostic performance study. AJNR Am J Neuroradiol. 2015;36:1834-8.CrossRefPubMed Smit EJ, Vonken EJ, Meijer FJ, Dankbaar JW, Horsch AD, van Ginneken B, Velthuis B, van der Schaaf I, Prokop M. Timing-invariant CT angiography derived from CT perfusion imaging in acute stroke: A diagnostic performance study. AJNR Am J Neuroradiol. 2015;36:1834-8.CrossRefPubMed
27.
go back to reference McVerry F, Liebeskind DS, Muir KW. Systematic review of methods for assessing leptomeningeal collateral flow. AJNR Am J Neuroradiol. 2012;33:576–82.CrossRefPubMed McVerry F, Liebeskind DS, Muir KW. Systematic review of methods for assessing leptomeningeal collateral flow. AJNR Am J Neuroradiol. 2012;33:576–82.CrossRefPubMed
28.
go back to reference Qureshi AI, El-Gengaihi A, Hussein HM, Suri MF, Liebeskind DS. Occurence and variability in acute formation of leptomeningeal collaterals in proximal middle cerebral artery occlusion. J Vasc Interv Neurol. 2008;1:70–2.PubMedPubMedCentral Qureshi AI, El-Gengaihi A, Hussein HM, Suri MF, Liebeskind DS. Occurence and variability in acute formation of leptomeningeal collaterals in proximal middle cerebral artery occlusion. J Vasc Interv Neurol. 2008;1:70–2.PubMedPubMedCentral
Metadata
Title
Internal Carotid Artery Stenosis and Collateral Recruitment in Stroke Patients
Authors
Jan W. Dankbaar
Kelly G. P. Kerckhoffs
Alexander D. Horsch
Irene C. van der Schaaf
L. Jaap Kappelle
Birgitta K. Velthuis
DUST investigators
Publication date
01-09-2018
Publisher
Springer Berlin Heidelberg
Published in
Clinical Neuroradiology / Issue 3/2018
Print ISSN: 1869-1439
Electronic ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-017-0568-x

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