Skip to main content
Top
Published in: Neurological Sciences 6/2019

01-06-2019 | Computed Tomography | Original Article

Small vessel disease and clinical outcomes after endovascular treatment in acute ischemic stroke

Authors: Francesco Arba, Giuseppe Dario Testa, Nicola Limbucci, Sergio Nappini, Leonardo Renieri, Giovanni Pracucci, Patrizia Nencini, Domenico Inzitari

Published in: Neurological Sciences | Issue 6/2019

Login to get access

Abstract

Background

Pre-existing small vessel disease (SVD) has been associated with poor functional outcomes in patients with acute ischemic stroke treated with intravenous thrombolysis; however, there are scarce data in patients treated with endovascular therapy. We aimed to investigate the associations between SVD and clinical outcomes in patients treated with endovascular therapy.

Methods

We retrospectivel y evaluated patients with acute ischemic stroke in the anterior circulation receiving endovascular treatment. We assessed SVD markers with visual scales using non-contrast computed tomography. Early outcomes included intracerebral hemorrhage and 7-day/discharge stroke severity, and late outcomes included modified Rankin scale (mRS) 90 days after stroke. We used logistic and ordinal regression models adjusted for age, sex, stroke severity, and time-to-groin puncture time.

Results

A total of 175 patients were included in the study, mean (±SD) age 72.3 (± 12.4) years, 90 (51%) males. Among SVD features, only brain atrophy was associated with 7-day stroke severity (OR = 2.28; 95% CI = 1.11–4.68) and with worse mRS at 90 days (OR = 2.72; 95% CI = 1.25–5.91). Global SVD burden was associated with worse mRS at 90 days (OR = 1.63; 95% CI = 1.01–2.62) but not with 7-day stroke severity (OR = 1.71; 95% CI = 0.97–3.01).

Conclusions

Pre-existing SVD burden, mainly driven by brain atrophy, negatively affects early and late clinical outcomes in anterior circulation ischemic stroke treated with endovascular therapy. Our results may help prognostic stratification of stroke patients treated with endovascular therapy.
Literature
1.
go back to reference Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge Rv, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M, STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1) (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838CrossRefPubMedPubMedCentral Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge Rv, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M, STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1) (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838CrossRefPubMedPubMedCentral
2.
go back to reference IST-3 collaborative group (2015) Association between brain imaging signs, early and late outcomes, and response to intravenous alteplase after acute ischaemic stroke in the third International Stroke Trial (IST-3): secondary analysis of a randomised controlled trial. Lancet Neurol 14:485–496CrossRef IST-3 collaborative group (2015) Association between brain imaging signs, early and late outcomes, and response to intravenous alteplase after acute ischaemic stroke in the third International Stroke Trial (IST-3): secondary analysis of a randomised controlled trial. Lancet Neurol 14:485–496CrossRef
3.
go back to reference Shi ZS, Loh Y, Liebeskind DS, Saer JL, Gonzalez NR, Tateshima S, Jahan R, Feng L, Vespa PM, Starkman S, Salamon N, Villablance JP, Ali LK, Ovbiagele B, Kim D, Viñuela F, Duckwiler GR (2012) Leukoaraiosis predicts parenchymal hematoma after mechanical thrombectomy in acute ischemic stroke. Stroke 43:1806–1811CrossRefPubMedPubMedCentral Shi ZS, Loh Y, Liebeskind DS, Saer JL, Gonzalez NR, Tateshima S, Jahan R, Feng L, Vespa PM, Starkman S, Salamon N, Villablance JP, Ali LK, Ovbiagele B, Kim D, Viñuela F, Duckwiler GR (2012) Leukoaraiosis predicts parenchymal hematoma after mechanical thrombectomy in acute ischemic stroke. Stroke 43:1806–1811CrossRefPubMedPubMedCentral
4.
go back to reference Henninger N, Lin E, Baker SP, Wakhloo AK, Takhtani D, Moonis M (2012) Leukoaraiosis predicts poor 90-day outcome after acute large cerebral artery occlusion. Cerebrovasc Dis 33:525–531CrossRefPubMed Henninger N, Lin E, Baker SP, Wakhloo AK, Takhtani D, Moonis M (2012) Leukoaraiosis predicts poor 90-day outcome after acute large cerebral artery occlusion. Cerebrovasc Dis 33:525–531CrossRefPubMed
5.
go back to reference Arba F, Leigh R, Inzitari D, Warach S, Luby M, Lees KR (2017a) On behalf of STIR/VISTA imaging collaboration. Blood-brain barrier leakage increases with small vessel disease in acute ischemic stroke. Neurology 89:2143–2150CrossRefPubMedPubMedCentral Arba F, Leigh R, Inzitari D, Warach S, Luby M, Lees KR (2017a) On behalf of STIR/VISTA imaging collaboration. Blood-brain barrier leakage increases with small vessel disease in acute ischemic stroke. Neurology 89:2143–2150CrossRefPubMedPubMedCentral
6.
go back to reference Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J (2013) Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke 44:2995–2999CrossRefPubMed Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J (2013) Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke 44:2995–2999CrossRefPubMed
7.
go back to reference Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM (2014) Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology. 83:1228–1234CrossRefPubMedPubMedCentral Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM (2014) Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology. 83:1228–1234CrossRefPubMedPubMedCentral
8.
go back to reference Barber PA, Demchuk AM, Zhang J, Buchan AM (2000) Lancet. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS Study Group Alberta Stroke Programme Early CT Score. Lancet 355:1670–1674CrossRefPubMed Barber PA, Demchuk AM, Zhang J, Buchan AM (2000) Lancet. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS Study Group Alberta Stroke Programme Early CT Score. Lancet 355:1670–1674CrossRefPubMed
9.
go back to reference Menon BK, d’Esterre CD, Qazi EM, Almekhlafi M, Hahn L, Demchuk AM, Goyal M (2015) Radiology. Multiphase CT angiography: a new tool for the imaging triage of patients with acute ischemic stroke. Radiology. 275:510–520CrossRefPubMed Menon BK, d’Esterre CD, Qazi EM, Almekhlafi M, Hahn L, Demchuk AM, Goyal M (2015) Radiology. Multiphase CT angiography: a new tool for the imaging triage of patients with acute ischemic stroke. Radiology. 275:510–520CrossRefPubMed
10.
go back to reference Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, Roy D, Jovin TG, Willinsky RA, Sapkota BL, Dowlatshahi D, Frei DF, Kamal NR, Montanera WJ, Poppe AY, Ryckborst KJ, Silver FL, Shuaib A, Tampieri D, Williams D, Bang OY, Baxter BW, Burns PA, Choe H, Heo JH, Holmstedt CA, Jankowitz B, Kelly M, Linares G, Mandzia JL, Shankar J, Sohn SI, Swartz RH, Barber PA, Coutts SB, Smith EE, Morrish WF, Weill A, Subramaniam S, Mitha AP, Wong JH, Lowerison MW, Sajobi TT, Hill MD, ESCAPE Trial Investigators (2015) Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med 372:1019–1030CrossRef Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, Roy D, Jovin TG, Willinsky RA, Sapkota BL, Dowlatshahi D, Frei DF, Kamal NR, Montanera WJ, Poppe AY, Ryckborst KJ, Silver FL, Shuaib A, Tampieri D, Williams D, Bang OY, Baxter BW, Burns PA, Choe H, Heo JH, Holmstedt CA, Jankowitz B, Kelly M, Linares G, Mandzia JL, Shankar J, Sohn SI, Swartz RH, Barber PA, Coutts SB, Smith EE, Morrish WF, Weill A, Subramaniam S, Mitha AP, Wong JH, Lowerison MW, Sajobi TT, Hill MD, ESCAPE Trial Investigators (2015) Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med 372:1019–1030CrossRef
11.
go back to reference Wintermark M, Flanders AE, Velthuis B et al (2006) Perfusion-CT assessment of infarct core and penumbra: receiver operating characteristic curve analysis in 130 patients suspected of acute hemispheric stroke. Stroke. 37:979–985CrossRefPubMed Wintermark M, Flanders AE, Velthuis B et al (2006) Perfusion-CT assessment of infarct core and penumbra: receiver operating characteristic curve analysis in 130 patients suspected of acute hemispheric stroke. Stroke. 37:979–985CrossRefPubMed
12.
go back to reference Van Swieten JC, Hijdra A, Koudstaal PJ, Van Gijn J (1990) Grading white matter lesions on CT and MRI: a simple scale. J Neurol Neurosurg Psychiatry 53:1080–1083CrossRefPubMedPubMedCentral Van Swieten JC, Hijdra A, Koudstaal PJ, Van Gijn J (1990) Grading white matter lesions on CT and MRI: a simple scale. J Neurol Neurosurg Psychiatry 53:1080–1083CrossRefPubMedPubMedCentral
13.
go back to reference Arba F, Inzitari D, Ali M, Warach SJ, Luby M, Lees KR (2017b) Small vessel disease and clinical outcomes after IV rt-PA treatment. Acta Neurol Scand 136:72–77CrossRefPubMed Arba F, Inzitari D, Ali M, Warach SJ, Luby M, Lees KR (2017b) Small vessel disease and clinical outcomes after IV rt-PA treatment. Acta Neurol Scand 136:72–77CrossRefPubMed
14.
go back to reference Arba F, Mair G, Carpenter T, Sakka E, Sandercock PA, Lindley RI, Inzitari D, Wardlaw JM, IST-3 Trial Collaborators (2017c) Cerebral white matter hypoperfusion increases with small vessel disease burden. Data from the third international stroke trial. J Stroke Cerebrovasc Dis 26:1506–1513CrossRefPubMed Arba F, Mair G, Carpenter T, Sakka E, Sandercock PA, Lindley RI, Inzitari D, Wardlaw JM, IST-3 Trial Collaborators (2017c) Cerebral white matter hypoperfusion increases with small vessel disease burden. Data from the third international stroke trial. J Stroke Cerebrovasc Dis 26:1506–1513CrossRefPubMed
15.
go back to reference Fugate JE, Klunder AM, Kallmes DF (2013) What is meant by “TICI”? AJNR Am J Neuroradiol 34:1792–1797CrossRefPubMed Fugate JE, Klunder AM, Kallmes DF (2013) What is meant by “TICI”? AJNR Am J Neuroradiol 34:1792–1797CrossRefPubMed
16.
go back to reference Berger C, Fiorelli M, Steiner T, Schäbitz WR̈, Bozzao L, Bluhmki E, Hacke W, von Kummer R̈ (2001) Hemorrhagic transformation of ischemic brain tissue: asymptomatic or symptomatic? Stroke. 32:1330–1335CrossRefPubMed Berger C, Fiorelli M, Steiner T, Schäbitz WR̈, Bozzao L, Bluhmki E, Hacke W, von Kummer R̈ (2001) Hemorrhagic transformation of ischemic brain tissue: asymptomatic or symptomatic? Stroke. 32:1330–1335CrossRefPubMed
17.
go back to reference Kerr DM, Fulton RL, Lees KR, VISTA Collaborators (2012) Seven-day NIHSS is a sensitive outcome measure for exploratory clinical trials in acute stroke: evidence from the Virtual International Stroke Trials Archive. Stroke 43:1401–1403CrossRefPubMed Kerr DM, Fulton RL, Lees KR, VISTA Collaborators (2012) Seven-day NIHSS is a sensitive outcome measure for exploratory clinical trials in acute stroke: evidence from the Virtual International Stroke Trials Archive. Stroke 43:1401–1403CrossRefPubMed
18.
go back to reference Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701CrossRef Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701CrossRef
19.
go back to reference Palumbo V, Boulanger JM, Hill MD, Inzitari D, Buchan AM (2007) Leukoaraiosis and intracerebral hemorrhage after thrombolysis in acute stroke. Neurology. 68:1020–1024CrossRefPubMed Palumbo V, Boulanger JM, Hill MD, Inzitari D, Buchan AM (2007) Leukoaraiosis and intracerebral hemorrhage after thrombolysis in acute stroke. Neurology. 68:1020–1024CrossRefPubMed
20.
go back to reference Zhang J, Puri AS, Khan MA, Goddeau MA Jr, Henninger N (2014) Leukoaraiosis predicts a poor 90-day outcome after endovascular stroke therapy. AJNR. 35:2070–2075CrossRefPubMed Zhang J, Puri AS, Khan MA, Goddeau MA Jr, Henninger N (2014) Leukoaraiosis predicts a poor 90-day outcome after endovascular stroke therapy. AJNR. 35:2070–2075CrossRefPubMed
21.
go back to reference Atchaneeyasakul K, Leslie-Mazwi T, Donahue K, Giese AK, Rost NS (2017) White matter hyperintensity volume and outcome of mechanical thrombectomy with stentriever in acute ischemic stroke. Stroke. 48:2892–2894CrossRefPubMedPubMedCentral Atchaneeyasakul K, Leslie-Mazwi T, Donahue K, Giese AK, Rost NS (2017) White matter hyperintensity volume and outcome of mechanical thrombectomy with stentriever in acute ischemic stroke. Stroke. 48:2892–2894CrossRefPubMedPubMedCentral
22.
go back to reference Dichgans M, Wardlaw J, Smith E, Zietemann V, Seshadri S, Sachdev P, Biessels GJ, Fazekas F, Benavente O, Pantoni L, de Leeuw FE, Norrving B, Matthews P, Chen C, Mok V, Düring M, Whiteley W, Shuler K, Alonso A, Black SE, Brayne C, Chabriat H, Cordonnier C, Doubal F, Duzel E, Ewers M, Frayne R, Hachinski V, Ikram MA, Jessen F, Jouvent E, Linn J, O'Brien J, van Oostenbrugge R, Malik R, Mazoyer B, Schmidt R, Sposato LA, Stephan B, Swartz RH, Vernooij M, Viswanathan A, Werring D, Abe K, Allan L, Arba F, Bae HJ, Bath PMW, Bordet R, Breteler M, Choi S, Deary I, DeCarli C, Ebmeier K, Feng L, Greenberg SM, Ihara M, Kalaria R, Kim SY, Lim JS, Lindley RI, Mead G, Murray A, Quinn T, Ritchie C, Sacco R, al-Shahi Salman R, Sprigg N, Sudlow C, Thomas A, van Boxtel M, van der Grond J, van der Lugt A, Yang YH, ETACOHORTS Consortium (2016) MMETACOHORTS for the study of vascular disease and its contribution to cognitive decline and neurodegeneration: an initiative of the joint programme for neurodegenerative disease research. Alzheimers Dement 12:1235–1249CrossRef Dichgans M, Wardlaw J, Smith E, Zietemann V, Seshadri S, Sachdev P, Biessels GJ, Fazekas F, Benavente O, Pantoni L, de Leeuw FE, Norrving B, Matthews P, Chen C, Mok V, Düring M, Whiteley W, Shuler K, Alonso A, Black SE, Brayne C, Chabriat H, Cordonnier C, Doubal F, Duzel E, Ewers M, Frayne R, Hachinski V, Ikram MA, Jessen F, Jouvent E, Linn J, O'Brien J, van Oostenbrugge R, Malik R, Mazoyer B, Schmidt R, Sposato LA, Stephan B, Swartz RH, Vernooij M, Viswanathan A, Werring D, Abe K, Allan L, Arba F, Bae HJ, Bath PMW, Bordet R, Breteler M, Choi S, Deary I, DeCarli C, Ebmeier K, Feng L, Greenberg SM, Ihara M, Kalaria R, Kim SY, Lim JS, Lindley RI, Mead G, Murray A, Quinn T, Ritchie C, Sacco R, al-Shahi Salman R, Sprigg N, Sudlow C, Thomas A, van Boxtel M, van der Grond J, van der Lugt A, Yang YH, ETACOHORTS Consortium (2016) MMETACOHORTS for the study of vascular disease and its contribution to cognitive decline and neurodegeneration: an initiative of the joint programme for neurodegenerative disease research. Alzheimers Dement 12:1235–1249CrossRef
23.
go back to reference Pini L, Pievani M, Bocchetta M, Altomare D, Bosco P, Cavedo E, Galluzzi S, Marizzoni M, Frisoni GB (2016) Brain atrophy in Alzheimer’s disease and aging. Ageing Res Rev 30:25–48CrossRefPubMed Pini L, Pievani M, Bocchetta M, Altomare D, Bosco P, Cavedo E, Galluzzi S, Marizzoni M, Frisoni GB (2016) Brain atrophy in Alzheimer’s disease and aging. Ageing Res Rev 30:25–48CrossRefPubMed
24.
go back to reference Dickie DA, Valdés Hernández MDC, Makin SD et al (2018) The brain health index: towards a combined measure of neurovascular and neurodegenerative structural brain injury. Int J Stroke 13:849–856CrossRefPubMed Dickie DA, Valdés Hernández MDC, Makin SD et al (2018) The brain health index: towards a combined measure of neurovascular and neurodegenerative structural brain injury. Int J Stroke 13:849–856CrossRefPubMed
25.
go back to reference Gilberti N, Gamba M, Premi E, Costa A, Vergani V, Delrio I, Spezi R, Dikran M, Frigerio M, Gasparotti R, Pezzini A, Padovani A, Magoni M (2017) Leukoaraiosis is a predictor of futile recanalization in acute ischemic stroke. J Neurol 264:448–452CrossRefPubMed Gilberti N, Gamba M, Premi E, Costa A, Vergani V, Delrio I, Spezi R, Dikran M, Frigerio M, Gasparotti R, Pezzini A, Padovani A, Magoni M (2017) Leukoaraiosis is a predictor of futile recanalization in acute ischemic stroke. J Neurol 264:448–452CrossRefPubMed
26.
go back to reference Shi ZS, Liebeskind DS, Xiang B, Ge SG, Feng L, Albers GW, Budzik R, Devlin T, Gupta R, Jansen O, Jovin TG, Killer-Oberpfalzer M, Lutsep HL, Macho J, Nogueira RG, Rymer M, Smith WS, Wahlgren N, Duckwiler GR, Multi MERCI, TREVO, and TREVO 2 Investigators (2014) Predictors of functional dependence despite successful revascularization in large-vessel occlusion strokes. Stroke. 45:1977–1984CrossRefPubMedPubMedCentral Shi ZS, Liebeskind DS, Xiang B, Ge SG, Feng L, Albers GW, Budzik R, Devlin T, Gupta R, Jansen O, Jovin TG, Killer-Oberpfalzer M, Lutsep HL, Macho J, Nogueira RG, Rymer M, Smith WS, Wahlgren N, Duckwiler GR, Multi MERCI, TREVO, and TREVO 2 Investigators (2014) Predictors of functional dependence despite successful revascularization in large-vessel occlusion strokes. Stroke. 45:1977–1984CrossRefPubMedPubMedCentral
27.
go back to reference Østergaard L, Jespersen SN, Mouridsen K, Mikkelsen IK, Jonsdottír KÝ, Tietze A, Blicher JU, Aamand R, Hjort N, Iversen NK, Cai C, Hougaard KD, Simonsen CZ, von Weitzel-Mudersbach P, Modrau B, Nagenthiraja K, Ribe LR, Hansen MB, Bekke SL, Dahlman MG, Puig J, Pedraza S, Serena J, Cho TH, Siemonsen S, Thomalla G, Fiehler J, Nighoghossian N, Andersen G (2013) The role of the cerebral capillaries in acute ischemic stroke: the extended penumbra model. J Cereb Blood Flow Metab 33:635–648CrossRefPubMedPubMedCentral Østergaard L, Jespersen SN, Mouridsen K, Mikkelsen IK, Jonsdottír KÝ, Tietze A, Blicher JU, Aamand R, Hjort N, Iversen NK, Cai C, Hougaard KD, Simonsen CZ, von Weitzel-Mudersbach P, Modrau B, Nagenthiraja K, Ribe LR, Hansen MB, Bekke SL, Dahlman MG, Puig J, Pedraza S, Serena J, Cho TH, Siemonsen S, Thomalla G, Fiehler J, Nighoghossian N, Andersen G (2013) The role of the cerebral capillaries in acute ischemic stroke: the extended penumbra model. J Cereb Blood Flow Metab 33:635–648CrossRefPubMedPubMedCentral
28.
go back to reference Ter Telgte A, van Leijsen EMC, Wiegertjes K, Klijn CJM, Tuladhar AM, de Leeuw FE (2018) Cerebral small vessel disease: from a focal to a global perspective. Nat Rev Neurol 14:387–398CrossRefPubMed Ter Telgte A, van Leijsen EMC, Wiegertjes K, Klijn CJM, Tuladhar AM, de Leeuw FE (2018) Cerebral small vessel disease: from a focal to a global perspective. Nat Rev Neurol 14:387–398CrossRefPubMed
29.
go back to reference Eilaghi A, Brooks J, d’Esterre C, Zhang L, Swartz RH, Lee TY, Aviv RI (2013) Reperfusion is a stronger predictor of good clinical outcome than recanalization in ischemic stroke. Radiology. 269:240–248CrossRefPubMed Eilaghi A, Brooks J, d’Esterre C, Zhang L, Swartz RH, Lee TY, Aviv RI (2013) Reperfusion is a stronger predictor of good clinical outcome than recanalization in ischemic stroke. Radiology. 269:240–248CrossRefPubMed
Metadata
Title
Small vessel disease and clinical outcomes after endovascular treatment in acute ischemic stroke
Authors
Francesco Arba
Giuseppe Dario Testa
Nicola Limbucci
Sergio Nappini
Leonardo Renieri
Giovanni Pracucci
Patrizia Nencini
Domenico Inzitari
Publication date
01-06-2019
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 6/2019
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-019-03824-4

Other articles of this Issue 6/2019

Neurological Sciences 6/2019 Go to the issue