Skip to main content
Top
Published in: BMC Neurology 1/2024

Open Access 01-12-2024 | Stroke | Research

Brain frailty associated with stroke events in anterior circulation large artery occlusion

Authors: Jing Tian, Kun Zhang, Junzhao Cui, Jin Qin, Binbin Wang, Lixia Zhou, Tong Li, Kailin Bu, Zhongzhong Li, Lin Liu, Qisong Wang, Si Yuan, Lina Ma, Ye Wang, Rui Wang, Chaoyue Meng, Biyi Zhou, Li Guo, Xiaoyun Liu

Published in: BMC Neurology | Issue 1/2024

Login to get access

Abstract

Objective

To investigate the factors associated with brain frailty and the effect of brain frailty in patients with anterior circulation large artery occlusion (AC-LAO).

Methods

1100 patients with AC-LVO consecutively admitted to the Second Hospital of Hebei Medical University, North China between June 2016 and April 2018 were retrospectively analyzed. The variables associated with brain frailty and stroke outcome were analyzed by ANOVA analysis, the Mann-Whitney U test and multiple linear regression. Based on previous research. Brain frailty score comprises 1 point each for white matter hyperintensity (WMH), old infarction lesions, and cerebral atrophy among 983 participants with baseline brain magnetic resonance imaging or computed tomography.

Results

Among AC-LAO participants, baseline brain frailty score ≥ 1 was common (750/983, 76.3%). Duration of hypertension > 5 years (mean difference [MD] 0.236, 95% CI 0.077, 0.395, p = 0.004), multiple vessel occlusion (MD 0.339, 95% CI 0.068, 0.611, p = 0.014) and basal ganglia infarction (MD -0.308, 95% CI -0.456, -0.160, p < 0.001) were independently associated with brain frailty score. Brain frailty score was independently associated with stroke events, and higher brain frailty scores were associated with higher rates of stroke events (p < 0.001). However, brain frailty has no independent effect on short-term outcome of ACI in AC-LAO patients.

Conclusions

In AC-LAO patients, older age, duration of hypertension > 5 years, and multiple vessel occlusion influenced the brain frailty score. Brain frailty score was independently associated with the occurrence of stroke events in AC-LAO patients.
Appendix
Available only for authorised users
Literature
1.
go back to reference Yassi N, Churilov L, Campbell BCV, Sharma G, Bammer R, Desmond PM, et al. The association between lesion location and functional outcome after ischemic stroke. Int J Stroke. 2015;10:1270–6.CrossRefPubMed Yassi N, Churilov L, Campbell BCV, Sharma G, Bammer R, Desmond PM, et al. The association between lesion location and functional outcome after ischemic stroke. Int J Stroke. 2015;10:1270–6.CrossRefPubMed
2.
go back to reference Tziaka E, Christidi F, Tsiptsios D, Sousanidou A, Karatzetzou S, Tsiakiri A, et al. Leukoaraiosis as a predictor of Depression and Cognitive Impairment among Stroke survivors: a systematic review. Neurol Int. 2023;15:238–72.CrossRefPubMedPubMedCentral Tziaka E, Christidi F, Tsiptsios D, Sousanidou A, Karatzetzou S, Tsiakiri A, et al. Leukoaraiosis as a predictor of Depression and Cognitive Impairment among Stroke survivors: a systematic review. Neurol Int. 2023;15:238–72.CrossRefPubMedPubMedCentral
3.
go back to reference Delcourt C, Wang X, Zhou Z, Wardlaw JM, Mair G, Robinson TG, et al. Brain imaging abnormalities and outcome after acute ischaemic stroke: the ENCHANTED trial. J Neurol Neurosurg Psychiatry. 2020;91:1290–6.CrossRefPubMed Delcourt C, Wang X, Zhou Z, Wardlaw JM, Mair G, Robinson TG, et al. Brain imaging abnormalities and outcome after acute ischaemic stroke: the ENCHANTED trial. J Neurol Neurosurg Psychiatry. 2020;91:1290–6.CrossRefPubMed
4.
go back to reference Goyal M, Ospel JM, Kappelhof M, Ganesh A. Challenges of Outcome Prediction for Acute Stroke Treatment decisions. Stroke. 2021;52:1921–8.CrossRefPubMed Goyal M, Ospel JM, Kappelhof M, Ganesh A. Challenges of Outcome Prediction for Acute Stroke Treatment decisions. Stroke. 2021;52:1921–8.CrossRefPubMed
5.
go back to reference Gardener H, Caunca M, Dong C, Cheung YK, Alperin N, Rundek T, et al. Ideal Cardiovascular Health and biomarkers of subclinical brain aging: the Northern Manhattan Study. J Am Heart Assoc. 2018;7:e009544.CrossRefPubMedPubMedCentral Gardener H, Caunca M, Dong C, Cheung YK, Alperin N, Rundek T, et al. Ideal Cardiovascular Health and biomarkers of subclinical brain aging: the Northern Manhattan Study. J Am Heart Assoc. 2018;7:e009544.CrossRefPubMedPubMedCentral
6.
go back to reference Pase MP, Davis-Plourde K, Himali JJ, Satizabal CL, Aparicio H, Seshadri S, et al. Vascular risk at younger ages most strongly associates with current and future brain volume. Neurology. 2018;91:e1479–86.CrossRefPubMedPubMedCentral Pase MP, Davis-Plourde K, Himali JJ, Satizabal CL, Aparicio H, Seshadri S, et al. Vascular risk at younger ages most strongly associates with current and future brain volume. Neurology. 2018;91:e1479–86.CrossRefPubMedPubMedCentral
7.
go back to reference Gómez-Choco M, Mengual JJ, Rodríguez-Antigüedad J, Paré-Curell M, Purroy F, Palomeras E, et al. Pre-existing cerebral small vessel disease limits early recovery in patients with Acute Lacunar Infarct. J Stroke Cerebrovasc Dis. 2019;28:104312.CrossRefPubMed Gómez-Choco M, Mengual JJ, Rodríguez-Antigüedad J, Paré-Curell M, Purroy F, Palomeras E, et al. Pre-existing cerebral small vessel disease limits early recovery in patients with Acute Lacunar Infarct. J Stroke Cerebrovasc Dis. 2019;28:104312.CrossRefPubMed
9.
go back to reference Appleton JP, Woodhouse LJ, Adami A, Becker JL, Berge E, Cala LA, et al. Imaging markers of small vessel disease and brain frailty, and outcomes in acute stroke. Neurology. 2020;94:e439–52.CrossRefPubMedPubMedCentral Appleton JP, Woodhouse LJ, Adami A, Becker JL, Berge E, Cala LA, et al. Imaging markers of small vessel disease and brain frailty, and outcomes in acute stroke. Neurology. 2020;94:e439–52.CrossRefPubMedPubMedCentral
10.
go back to reference Bu N, Khlif MS, Lemmens R, Wouters A, Fiebach JB, Chamorro A, et al. Imaging markers of brain frailty and outcome in patients with Acute ischemic stroke. Stroke. 2021;52:1004–11.CrossRefPubMed Bu N, Khlif MS, Lemmens R, Wouters A, Fiebach JB, Chamorro A, et al. Imaging markers of brain frailty and outcome in patients with Acute ischemic stroke. Stroke. 2021;52:1004–11.CrossRefPubMed
11.
go back to reference Arba F, Inzitari D, Ali M, Warach SJ, Luby M, Lees KR, et al. Small vessel disease and clinical outcomes after IV rt-PA treatment. Acta Neurol Scand. 2017;136:72–7.CrossRefPubMed Arba F, Inzitari D, Ali M, Warach SJ, Luby M, Lees KR, et al. Small vessel disease and clinical outcomes after IV rt-PA treatment. Acta Neurol Scand. 2017;136:72–7.CrossRefPubMed
12.
go back to reference Tschirret O, Moreno Legast G, Mansuy A, Mewton N, Buisson M, Hannoun S, et al. Impact of brain atrophy on early neurological deterioration and outcome in severe ischemic stroke treated by intravenous thrombolysis. Eur Neurol. 2018;79:240–6.CrossRefPubMed Tschirret O, Moreno Legast G, Mansuy A, Mewton N, Buisson M, Hannoun S, et al. Impact of brain atrophy on early neurological deterioration and outcome in severe ischemic stroke treated by intravenous thrombolysis. Eur Neurol. 2018;79:240–6.CrossRefPubMed
13.
go back to reference Barnett K, Mercer SW, Norbury M, Watt G, Wyke S, Guthrie B. Epidemiology of multimorbidity and implications for health care, research, and medical education: a cross-sectional study. Lancet. 2012;380:37–43.CrossRefPubMed Barnett K, Mercer SW, Norbury M, Watt G, Wyke S, Guthrie B. Epidemiology of multimorbidity and implications for health care, research, and medical education: a cross-sectional study. Lancet. 2012;380:37–43.CrossRefPubMed
14.
go back to reference Flint AC, Bhandari SG, Cullen SP, Reddy AV, Hsu DP, Rao VA, et al. Detection of anterior circulation large artery occlusion in ischemic stroke using Noninvasive Cerebral Oximetry. Stroke. 2018;49:458–60.CrossRefPubMed Flint AC, Bhandari SG, Cullen SP, Reddy AV, Hsu DP, Rao VA, et al. Detection of anterior circulation large artery occlusion in ischemic stroke using Noninvasive Cerebral Oximetry. Stroke. 2018;49:458–60.CrossRefPubMed
15.
go back to reference Kwon H-M, Lynn MJ, Turan TN, Derdeyn CP, Fiorella D, Lane BF, et al. Frequency, risk factors, and outcome of Coexistent Small Vessel Disease and Intracranial arterial stenosis: results from the stenting and Aggressive Medical Management for preventing recurrent stroke in intracranial stenosis (SAMMPRIS) trial. JAMA Neurol. 2016;73:36–42.CrossRefPubMedPubMedCentral Kwon H-M, Lynn MJ, Turan TN, Derdeyn CP, Fiorella D, Lane BF, et al. Frequency, risk factors, and outcome of Coexistent Small Vessel Disease and Intracranial arterial stenosis: results from the stenting and Aggressive Medical Management for preventing recurrent stroke in intracranial stenosis (SAMMPRIS) trial. JAMA Neurol. 2016;73:36–42.CrossRefPubMedPubMedCentral
16.
go back to reference Song J, Kim K-H, Jeon P, Kim Y-W, Kim D-I, Park Y-J, et al. White matter hyperintensity determines ischemic stroke severity in symptomatic carotid artery stenosis. Neurol Sci. 2021;42:3367–74.CrossRefPubMed Song J, Kim K-H, Jeon P, Kim Y-W, Kim D-I, Park Y-J, et al. White matter hyperintensity determines ischemic stroke severity in symptomatic carotid artery stenosis. Neurol Sci. 2021;42:3367–74.CrossRefPubMed
17.
go back to reference Zerna C, Yu AYX, Modi J, Patel SK, Coulter JI, Smith EE, et al. Association of White Matter Hyperintensities with short-term outcomes in patients with minor cerebrovascular events. Stroke. 2018;49:919–23.CrossRefPubMed Zerna C, Yu AYX, Modi J, Patel SK, Coulter JI, Smith EE, et al. Association of White Matter Hyperintensities with short-term outcomes in patients with minor cerebrovascular events. Stroke. 2018;49:919–23.CrossRefPubMed
18.
go back to reference de Havenon A, Wong K-H, Elkhetali A, McNally JS, Majersik JJ, Rost NS. Carotid artery stiffness accurately predicts White Matter Hyperintensity 20 years later: a secondary analysis of the atherosclerosis risk in the Community Study. AJNR Am J Neuroradiol. 2019;40:1369–73.CrossRefPubMedPubMedCentral de Havenon A, Wong K-H, Elkhetali A, McNally JS, Majersik JJ, Rost NS. Carotid artery stiffness accurately predicts White Matter Hyperintensity 20 years later: a secondary analysis of the atherosclerosis risk in the Community Study. AJNR Am J Neuroradiol. 2019;40:1369–73.CrossRefPubMedPubMedCentral
19.
go back to reference Zhang K, Li T, Tian J, Li P, Fu B, Yang X, et al. Subtypes of anterior circulation large artery occlusions with acute brain ischemic stroke. Sci Rep. 2020;10:3442.ADSCrossRefPubMedPubMedCentral Zhang K, Li T, Tian J, Li P, Fu B, Yang X, et al. Subtypes of anterior circulation large artery occlusions with acute brain ischemic stroke. Sci Rep. 2020;10:3442.ADSCrossRefPubMedPubMedCentral
20.
go back to reference Cui J, Yang J, Zhang K, Xu G, Zhao R, Li X, et al. Machine learning-based Model for Predicting incidence and severity of Acute ischemic stroke in anterior circulation large vessel occlusion. Front Neurol. 2021;12:749599.CrossRefPubMedPubMedCentral Cui J, Yang J, Zhang K, Xu G, Zhao R, Li X, et al. Machine learning-based Model for Predicting incidence and severity of Acute ischemic stroke in anterior circulation large vessel occlusion. Front Neurol. 2021;12:749599.CrossRefPubMedPubMedCentral
21.
go back to reference Farrell C, Chappell F, Armitage PA, Keston P, Maclullich A, Shenkin S, et al. Development and initial testing of normal reference MR images for the brain at ages 65–70 and 75–80 years. Eur Radiol. 2009;19:177–83.CrossRefPubMed Farrell C, Chappell F, Armitage PA, Keston P, Maclullich A, Shenkin S, et al. Development and initial testing of normal reference MR images for the brain at ages 65–70 and 75–80 years. Eur Radiol. 2009;19:177–83.CrossRefPubMed
22.
go back to reference IST-3 collaborative group. 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. 2015;14:485–96.CrossRef IST-3 collaborative group. 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. 2015;14:485–96.CrossRef
23.
go back to reference Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149:351–6.CrossRefPubMed Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149:351–6.CrossRefPubMed
24.
go back to reference Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9:689–701.CrossRefPubMed Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9:689–701.CrossRefPubMed
25.
go back to reference Scharf EL, Graff-Radford J, Przybelski SA, Lesnick TG, Mielke MM, Knopman DS, et al. Cardiometabolic Health and Longitudinal Progression of White Matter Hyperintensity: the Mayo Clinic Study of Aging. Stroke. 2019;50:3037–44.CrossRefPubMedPubMedCentral Scharf EL, Graff-Radford J, Przybelski SA, Lesnick TG, Mielke MM, Knopman DS, et al. Cardiometabolic Health and Longitudinal Progression of White Matter Hyperintensity: the Mayo Clinic Study of Aging. Stroke. 2019;50:3037–44.CrossRefPubMedPubMedCentral
26.
go back to reference Tariq S, Barber PA. Dementia risk and prevention by targeting modifiable vascular risk factors. J Neurochem. 2018;144:565–81.CrossRefPubMed Tariq S, Barber PA. Dementia risk and prevention by targeting modifiable vascular risk factors. J Neurochem. 2018;144:565–81.CrossRefPubMed
27.
go back to reference Pathak GA, Barber RC, Phillips NR. Multiomics Investigation of Hypertension and White Matter Hyperintensity as a source of vascular dementia or a comorbidity to Alzheimer’s Disease. Curr Alzheimer Res. 2021;18:171–7.CrossRefPubMed Pathak GA, Barber RC, Phillips NR. Multiomics Investigation of Hypertension and White Matter Hyperintensity as a source of vascular dementia or a comorbidity to Alzheimer’s Disease. Curr Alzheimer Res. 2021;18:171–7.CrossRefPubMed
28.
go back to reference Shi Y, Guo L, Chen Y, Xie Q, Yan Z, Liu Y, et al. Risk factors for ischemic stroke: differences between cerebral small vessel and large artery atherosclerosis aetiologies. Folia Neuropathol. 2021;59:378–85.CrossRefPubMed Shi Y, Guo L, Chen Y, Xie Q, Yan Z, Liu Y, et al. Risk factors for ischemic stroke: differences between cerebral small vessel and large artery atherosclerosis aetiologies. Folia Neuropathol. 2021;59:378–85.CrossRefPubMed
29.
go back to reference Yoshida J, Yamashita F, Sasaki M, Yoshioka K, Fujiwara S, Kobayashi M, et al. Adverse effects of pre-existing cerebral small vessel disease on cognitive improvement after carotid endarterectomy. Int J Stroke. 2020;15:657–65.CrossRefPubMed Yoshida J, Yamashita F, Sasaki M, Yoshioka K, Fujiwara S, Kobayashi M, et al. Adverse effects of pre-existing cerebral small vessel disease on cognitive improvement after carotid endarterectomy. Int J Stroke. 2020;15:657–65.CrossRefPubMed
30.
go back to reference Wang X-Y, Lyu J-H, Zhang S-H, Duan C-H, Duan Q, Ma X-X, et al. Severity of Intracranial large artery Disease correlates with cerebral small Vessel Disease. J Magn Reson Imaging. 2022;56:264–72.CrossRefPubMed Wang X-Y, Lyu J-H, Zhang S-H, Duan C-H, Duan Q, Ma X-X, et al. Severity of Intracranial large artery Disease correlates with cerebral small Vessel Disease. J Magn Reson Imaging. 2022;56:264–72.CrossRefPubMed
31.
go back to reference Shu M-J, Zhai F-F, Zhang D-D, Han F, Zhou L, Ni J, et al. Metabolic syndrome, intracranial arterial stenosis and cerebral small vessel disease in community-dwelling populations. Stroke Vasc Neurol. 2021;6:589–94.CrossRefPubMedPubMedCentral Shu M-J, Zhai F-F, Zhang D-D, Han F, Zhou L, Ni J, et al. Metabolic syndrome, intracranial arterial stenosis and cerebral small vessel disease in community-dwelling populations. Stroke Vasc Neurol. 2021;6:589–94.CrossRefPubMedPubMedCentral
32.
go back to reference Liu M, Nie Z-Y, Li R-R, Zhang W, Wang H, He Y-S, et al. Correlation of Brain Perfusion with White Matter Hyperintensity, Brain Atrophy, and Cognition in patients with posterior cerebral artery stenosis and subjective cognitive decline. Med Sci Monit. 2018;24:5729–38.CrossRefPubMedPubMedCentral Liu M, Nie Z-Y, Li R-R, Zhang W, Wang H, He Y-S, et al. Correlation of Brain Perfusion with White Matter Hyperintensity, Brain Atrophy, and Cognition in patients with posterior cerebral artery stenosis and subjective cognitive decline. Med Sci Monit. 2018;24:5729–38.CrossRefPubMedPubMedCentral
33.
go back to reference Fischer U, Hsieh-Meister K, Kellner-Weldon F, Galimanis A, Yan X, Kaesmacher J, et al. Symptomatic and asymptomatic intracranial atherosclerotic stenosis: 3 years’ prospective study. J Neurol. 2020;267:1687–98.CrossRefPubMed Fischer U, Hsieh-Meister K, Kellner-Weldon F, Galimanis A, Yan X, Kaesmacher J, et al. Symptomatic and asymptomatic intracranial atherosclerotic stenosis: 3 years’ prospective study. J Neurol. 2020;267:1687–98.CrossRefPubMed
34.
go back to reference Hurford R, Wolters FJ, Li L, Lau KK, Küker W, Rothwell PM, et al. Prevalence, predictors, and prognosis of symptomatic intracranial stenosis in patients with transient ischaemic attack or minor stroke: a population-based cohort study. Lancet Neurol. 2020;19:413–21.CrossRefPubMedPubMedCentral Hurford R, Wolters FJ, Li L, Lau KK, Küker W, Rothwell PM, et al. Prevalence, predictors, and prognosis of symptomatic intracranial stenosis in patients with transient ischaemic attack or minor stroke: a population-based cohort study. Lancet Neurol. 2020;19:413–21.CrossRefPubMedPubMedCentral
35.
go back to reference Zhou J-Y, Shi Y-B, Xia C, Lu C-Q, Tang T-Y, Lu T, et al. Beyond collaterals: brain frailty additionally improves prediction of clinical outcome in acute ischemic stroke. Eur Radiol. 2022;32:6943–52.CrossRefPubMed Zhou J-Y, Shi Y-B, Xia C, Lu C-Q, Tang T-Y, Lu T, et al. Beyond collaterals: brain frailty additionally improves prediction of clinical outcome in acute ischemic stroke. Eur Radiol. 2022;32:6943–52.CrossRefPubMed
36.
go back to reference Campbell BCV, Mitchell PJ, Churilov L, Yassi N, Kleinig TJ, Dowling RJ, et al. Effect of intravenous tenecteplase dose on cerebral reperfusion before thrombectomy in patients with large vessel occlusion ischemic stroke: the EXTEND-IA TNK Part 2 Randomized Clinical Trial. JAMA. 2020;323:1257–65.CrossRefPubMedPubMedCentral Campbell BCV, Mitchell PJ, Churilov L, Yassi N, Kleinig TJ, Dowling RJ, et al. Effect of intravenous tenecteplase dose on cerebral reperfusion before thrombectomy in patients with large vessel occlusion ischemic stroke: the EXTEND-IA TNK Part 2 Randomized Clinical Trial. JAMA. 2020;323:1257–65.CrossRefPubMedPubMedCentral
Metadata
Title
Brain frailty associated with stroke events in anterior circulation large artery occlusion
Authors
Jing Tian
Kun Zhang
Junzhao Cui
Jin Qin
Binbin Wang
Lixia Zhou
Tong Li
Kailin Bu
Zhongzhong Li
Lin Liu
Qisong Wang
Si Yuan
Lina Ma
Ye Wang
Rui Wang
Chaoyue Meng
Biyi Zhou
Li Guo
Xiaoyun Liu
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2024
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-024-03566-7

Other articles of this Issue 1/2024

BMC Neurology 1/2024 Go to the issue