In cerebral infarction, the prognostic value of angiographic
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1 Nonrelevant Cerebral Atherosclerosis is a Strong Prognostic Factor in Acute Cerebral Infarction Jinkwon Kim, MD; Tae-Jin Song, MD; Dongbeom Song, MD; Hye Sun Lee, MS; Chung Mo Nam, PhD; Hyo Suk Nam, MD, PhD; Young Dae Kim, MD, PhD; Ji Hoe Heo, MD, PhD Downloaded from by guest on April 29, 2018 Background and Purpose We investigated whether the presence of nonrelevant cerebral atherosclerosis (NRCA) had prognostic value in patients with acute stroke. Methods We compared prognosis in 780 consecutive patients with first-ever acute cerebral infarction who underwent cerebral angiography and diffusion-weighted MRI. Results NRCA was present in 267 patients (34.2%). Multivariate analysis demonstrated that the presence of NRCA was independently associated with less improvement in National Institute of Health Stroke Scale score during the first 7 days (P=0.004), and a poor functional outcome (modified Rankin Scale score >2) after 3 months (odds ratio, 2.51; 95% confidence interval, ). An increase in burden count of NRCA was also associated with poor outcomes. Conclusions The presence and burden count of NRCA were associated with poor neurological outcomes in patients with acute cerebral infarction. (Stroke. 2013;44: ) Key words: acute stroke angiography atherosclerosis prognosis In cerebral infarction, the prognostic value of angiographic information is mainly focused on the steno-occlusive lesion of the symptomatic cerebral artery (relevant cerebral atherosclerosis [RCA]). 1 Asymptomatic cerebral atherosclerosis (non-rca [NRCA]) is also often found during cerebral angiography. Previous studies showed that the increase of total burden of cerebral atherosclerosis or RCA is associated with poor outcome. 1 3 However, the prognostic value of NRCA is not well known. Therefore, we investigated whether the presence of NRCA also has a prognostic value in patients with acute cerebral infarction. Methods This was a retrospective, observational study on patients with acute cerebral infarction who were admitted to a neurology department within 72 hours of symptom onset between November 2008 and November We excluded patients with (1) high-risk potential cardiac sources of embolism on the basis of Trial of Org in Acute Stroke Treatment classification system because embolic occlusive lesions often cannot be differentiated from atherosclerotic lesions based on angiography, (2) rare causes of stroke, (3) history of previous stroke, (4) in-hospital stroke, (5) history of malignancy, and (6) patients who did not have a cerebral angiography or who had missing laboratory data used as covariates for analyses. All patients underwent digital subtraction angiography, MR angiography, or computed tomography angiography. Cerebral atherosclerosis was defined when the artery showed 50% stenosis or occlusion. We divided the cerebral atherosclerosis into relevant and nonrelevant lesions (RCA and NRCA) on the basis of the arterial territory of acute infarction found on diffusion-weighted MR images. Figure I in the online-only Data Supplement shows examples of patients with NRCA. The burden count of NRCA was calculated in each patient. Primary outcomes of this study were (1) early changes in the National Institute of Health Stroke Scale (NIHSS) scores during 7 days after admission and (2) functional outcome using the modified Rankin Scale (mrs) after 3 months from stroke onset. We collected NIHSS scores at admission (day 0), day 1, day 3, and day 7. If a patient was discharged between days 4 and 6, the NIHSS score at discharge was used as the score for day 7. Statistical analyses were performed using SPSS for Windows (version 18.0, SPSS Inc, Chicago, IL). To evaluate the association between variables and early changes in NIHSS scores, we used a linear mixed model of repeated measures with unstructured covariances within subjects. We performed ordinal logistic regression to evaluate variables associated with mrs (0 6) and binary logistic regression on the basis of a dichotomized mrs (mrs 2 versus mrs>2). Multivariate models were adjusted for sex, age, and those variables with P<0.10 in the univariate analysis. P<0.05 was considered statistically significant. Assessment for cerebral atherosclerosis and detailed statistical methods are shown in the online-only Data Supplement. The Institutional Review Board of Severance Hospital, Yonsei University Health System approved this study and waived the requirement for informed consent because of the retrospective and observational nature of the study. Results There were 1564 candidates who were admitted during the study period. After excluding 784 patients according to the exclusion criteria, 780 patients were included. Among them, RCA was found Received February 7, 2013; accepted March 29, From the Department of Neurology, CHA Bundang Medical Center, CHA University, Seongnam, Republic of Korea (J.K.); and Departments of Neurology (T.-J.S., D.S., H.S.N., Y.D.K., J.H.H.) and Biostatistics (H.S.L., C.M.N.), Yonsei University College of Medicine, Seoul, Republic of Korea. The online-only Data Supplement is available with this article at /-/DC1. Correspondence to Ji Hoe Heo, MD, PhD, Department of Neurology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemoon-gu, Seoul , Republic of Korea. jhheo@yuhs.ac 2013 American Heart Association, Inc. Stroke is available at DOI: /STROKEAHA
2 2014 Stroke July 2013 Figure. Clinical outcomes according to the presence of nonrelevant cerebral atherosclerosis (NRCA). A, Boxplot for early changes in National Institutes of Health Stroke Scale (NIHSS) score. Probability values from Mann Whitney test. *P<0.01; NS, P>0.05. B, modified Rankin Scale (mrs) after 3 months from stroke onset. P<0.001 from χ 2 test for trend. Downloaded from by guest on April 29, 2018 in 285 patients (36.5%), and NRCA was present in 267 patients (34.2%). NRCA was most frequent in extracranial vertebral artery, followed by posterior and middle cerebral arteries (Table I in the online-only Data Supplement). Patients with NRCA were older, had higher high-sensitive C-reactive protein and glucose levels at admission than those without NRCA. The prevalence of RCA was not different between patients with NRCA and those without (Table II in the online-only Data Supplement). The NIHSS score was assessed in all patients (100%) at day 0, 742 patients (95.1%) at day 1, 764 patients (97.9%) at day 3, and 696 patients (89.2%) at day 7. The NIHSS score at admission did not differ in patients with NRCA and those without NRCA. However, the NIHSS scores at day 1, day 3, and day 7 were higher in patients with NRCA than those without (Figure [A]). In multivariate linear mixed model, the presence and burden count of NRCA were positively associated with repeatedly measured NIHSS scores (Table). This finding means that there was less improvement in neurological deficits for 7 days in patients with NRCA than in those without NRCA. An mrs score at 3 months after stroke onset was available in 749 patients (96.0%). An increase in burden count of NRCA was significantly associated with a worse functional outcome after 3 months (Figure [B]). In multivariate ordinal and binary Table. logistic regression model, the presence and burden count of NRCA were independently associated with a worse functional outcome (Table). There was no significant interaction between the presence of RCA and NRCA in the multivariate models. We performed further analysis by dividing patients into 4 groups according to the location of NRCA (no NRCA, only extracranial NRCA, only intracranial NRCA, and both intracranial and extracranial NRCA). Compared with the no NRCA group, patients with only intracranial NRCA showed less early improvement in neurological deficits and worse functional outcome. However, the presence of only extracranial NRCA was not a significant predictor in multivariate linear mixed model and ordinal logistic regression model (Table III in the online-only Data Supplement). Discussion We demonstrated that the presence and burden count of NRCA are independent prognostic factors for short- and long-term neurological outcomes in patients with acute stroke. Our findings, together with previous evidence, 3 indicate that advanced cerebral atherosclerosis, even though it is asymptomatic, may result in poor clinical outcomes. The presence of NRCA might affect the development and efficiency of the collateral vessels, 2 Nonrelevant Cerebral Atherosclerosis in Multivariate Models for Short- and Long-Term Prognosis NIHSS Score For 7 Days Linear Mixed Model* Ordinal Logistic Regression mrs After 3 Mo Binary Logistic Regression (mrs 2 vs mrs>2) Estimate SE P Value OR 95% CI P Value OR 95% CI P Value Presence of nonrelevant cerebral <0.001 atherosclerosis Burden of nonrelevant cerebral < <0.001 atherosclerosis, per 1 count CI indicates confidence interval; hs-crp, high-sensitive C-reactive protein; mrs, modified Rankin Scale; NIHSS indicates National Institutes of Health Stroke Scale; OR, odds ratio; RCA, relevant cerebral atherosclerosis; and SE, standard error. *Adjusted for time of NIHSS score measurement, NIHSS score at admission, sex, age, thrombolysis at admission, and white blood cell count. Adjusted for sex, age, NIHSS score at admission, diabetes mellitus, peripheral artery occlusive disease, thrombolysis at admission, white blood cell count, platelet count, hs-crp, albumin, glucose, and RCA. Adjusted for sex, age, NIHSS score at admission, current smoking, peripheral artery occlusive disease, white blood cell count, platelet count, hemoglobin, hs-crp, triglyceride, albumin, blood urea nitrogen, and RCA. The estimate indicates the mean change in measured NIHSS score conferred by nonrelevant cerebral atherosclerosis (the dependent variables were repeatedly measured NIHSS scores at day 1, day 3, and day 7). The OR indicates the common odds of shifting to a worse mrs category at each cut-off. The OR indicates the risk of obtaining a poor functional outcome (mrs>2).
3 Kim et al Nonrelevant Cerebral Atherosclerosis in Stroke 2015 Downloaded from by guest on April 29, 2018 and increase the risk of recurrent strokes, which could contribute to the poor outcome seen in these patients. Patients with asymptomatic cerebral atherosclerosis frequently have elevated inflammatory biomarkers, 4 which are associated with recurrent stroke and further ischemic damage. The different prognostic effects of extracranial/intracranial NRCA might be because of relatively small number of patients with only extracranial NRCA in this study. This study has limitations. Because of the retrospective design, we could not present the data for stroke recurrence and the degree of collateral circulation according to the presence of NRCA. Some potential bias might be introduced by different diagnostic accuracy for cerebral atherosclerosis among digital subtraction angiography, computed tomography angiography and MR angiography, and interobserver variability in measuring cerebral atherosclerosis, NIHSS and mrs. Summary The presence and burden count of NRCA were associated with poor neurological outcomes in patients with acute cerebral infarction. Our findings suggest that further investigation is needed to the role of NRCA in stroke prognosis. Sources of Funding This work was supported by a grant from the Korea Healthcare Technology Research and Development Project, Ministry for Health, Welfare, and Family Affairs, Republic of Korea (A102065). None. Disclosures References 1. Derex L, Nighoghossian N, Hermier M, Adeleine P, Froment JC, Trouillas P. Early detection of cerebral arterial occlusion on magnetic resonance angiography: predictive value of the baseline NIHSS score and impact on neurological outcome. Cerebrovasc Dis. 2002;13: Fu JH, Chen YK, Chen XY, Mok V, Wong KS. Coexisting small vessel disease predicts poor long-term outcome in stroke patients with intracranial large artery atherosclerosis. Cerebrovasc Dis. 2010;30: Wong KS, Li H, Chan YL, Ahuja A, Lam WW, Wong A,. Use of transcranial Doppler ultrasound to predict outcome in patients with intracranial large-artery occlusive disease. Stroke. 2000;31: López-Cancio E, Galán A, Dorado L, Jiménez M, Hernández M, Millán M, et al. Biological signatures of asymptomatic extra- and intracranial atherosclerosis: the Barcelona-AsIA (Asymptomatic Intracranial Atherosclerosis) study. Stroke. 2012;43:
4 Nonrelevant Cerebral Atherosclerosis is a Strong Prognostic Factor in Acute Cerebral Infarction Jinkwon Kim, Tae-Jin Song, Dongbeom Song, Hye Sun Lee, Chung Mo Nam, Hyo Suk Nam, Young Dae Kim and Ji Hoe Heo Downloaded from by guest on April 29, 2018 Stroke. 2013;44: ; originally published online May 16, 2013; doi: /STROKEAHA Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX Copyright 2013 American Heart Association, Inc. All rights reserved. Print ISSN: Online ISSN: The online version of this article, along with updated information and services, is located on the World Wide Web at: Data Supplement (unedited) at: Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Once the online version of the published article for which permission is being requested is located, click Request Permissions in the middle column of the Web page under Services. Further information about this process is available in the Permissions and Rights Question and Answer document. Reprints: Information about reprints can be found online at: Subscriptions: Information about subscribing to Stroke is online at:
5 ONLINE ONLY SUPPLEMENT Title: Non-relevant cerebral atherosclerosis is a strong prognostic factor in acute cerebral infarction Authors: Jinkwon Kim, MD; Tae-Jin Song, MD; Dongbeom Song, MD; Hye Sun Lee, MS; Chung Mo Nam, PhD; Hyo Suk Nam, MD, PhD; Young Dae Kim, MD, PhD; Ji Hoe Heo, MD, PhD Supplemental method Supplemental table S1. Distribution of non-relevant cerebral atherosclerosis Supplemental table S2. Clinical characteristics and comparisons of study patients with and without non-relevant cerebral atherosclerosis Supplemental table S3. Prognostic value of NRCA according to the location Supplemental figure S1. Examples of patients with non-relevant cerebral atherosclerosis Supplemental reference 1
6 Supplemental method Assessment for cerebral atherosclerosis The presence of cerebral atherosclerosis was assessed in the anterior cerebral, middle cerebral, posterior cerebral, basilar, intracranial internal carotid, intracranial vertebral, extracranial internal carotid, extracranial vertebral arteries. The degree of stenosis in the extracranial cerebral artery was measured using the method described in the North American Symptomatic Carotid Endarterectomy Trial, 1 and that in the intracranial cerebral artery was measured using the method reported in Warfarin vs. Aspirin for Symptomatic Intracranial Disease. 2 If one arterial segment had multiple stenotic lesions, the most severe degree was selected. If the degree of stenosis is inaccessible due to occlusion of more proximal cerebral artery in the angiographic study, the inaccessible distal cerebral artery was not counted (i.e. invisible middle cerebral artery with occlusion of ipsilateral internal carotid artery. In the case, the internal carotid artery was counted as cerebral atherosclerosis, but the middle cerebral artery was not). If a patient had relevant tandem stenotic lesions (i.e. stenosis in the middle cerebral artery and internal carotid artery in a patient with acute infarction on the territory of the ipsilateral middle cerebral artery), the both arterial lesions were considered as being relevant. All angiographic findings and relevant artery lesions were determined during the weekly stroke conference based on the consensus of stroke specialists and the radiologist s report, which were prospectively registered in the Yonsei stroke registry. 3 Statistical analyses Continuous variables were expressed as mean standard deviation. Continuous variables were compared with the independent t-test or Mann-Whitney test, and categorical variables were compared with Fisher s exact test or chi-square test for trend. NIHSS score was considered a continuous variable. The dependent variables in linear mixed model were repeatedly measured NIHSS scores at day 1, day 3, and day 7. All analyses in the linear mixed model were adjusted for time of NIHSS score measurement (day 1, day 3 and day 7 as categorical variables) and NIHSS score at admission (day 0) as fixed effects. To determine the independent influence of NRCA on NIHSS score, additional adjustment were performed for sex, age, and variables which had a P<0.10 as fixed effects. In ordinal logistic regression, we calculated proportional odds ratio (OR) for shifts in outcomes across all seven categories of mrs (0 to 6). OR in the ordinal regressions expressed the common odds for worsened outcomes at each mrs category. All statistical tests were two-tailed. 2
7 Supplemental table S1. Distribution of non-relevant cerebral atherosclerosis No of patients with NRCA Burden count No of ACA MCA PCA BA In ICA In VA Ex ICA Ex VA of NRCA patients Patients with 267* NRCA *Patients number who had at least one NRCA. Among them, 31 patients had 75~99% stenosis and 65 patients had occlusion. NRCA indicates non-relevant cerebral atherosclerosis; ACA, anterior cerebral artery; MCA, middle cerebral artery; PCA, posterior cerebral artery; BA, basilar artery; In ICA, intracranial internal carotid artery; In VA, intracranial vertebral artery; Ex ICA, extracranial internal carotid artery; Ex VA, extracranial vertebral artery. 3
8 Supplemental table S2. Clinical characteristics and comparisons of study patients with and without non-relevant cerebral atherosclerosis All patients (n=780) Without NRCA (n=513) With NRCA (n=267) P value* Sex, male 501 (64.23) 335 (65.30) 166 (62.17) Age, year ± ± ± <0.001 SBP, mmhg ± ± ± Body temperature, C ± ± ± Cardiovascular risk factors Hypertension 559 (71.67) 364 (70.96) 195 (73.03) Diabetes mellitus 235 (30.13) 145 (28.27) 90 (33.71) Hypercholesterolemia 206 (26.41) 125 (24.37) 81 (30.34) Current smoking 229 (29.36) 157 (30.60) 72 (26.97) Coronary heart disease 162 (20.77) 107 (20.86) 55 (20.60) >0.999 Congestive heart failure 103 (13.21) 63 (12.28) 40 (14.98) Peripheral artery occlusive disease 55 (7.05) 30 (5.85) 25 (9.36) Thrombolysis at admission 57 (7.31) 43 (8.38) 14 (5.24) Premorbid medication Antiplatelet 198 (25.38) 134 (26.12) 64 (23.97) Statin 112 (14.36) 77 (15.01) 35 (13.11) Laboratory findings at admission White blood cell count, x10 9 /L 8.49 ± ± ± Platelet count, x10 9 /L ± ± ± Hemoglobin, g/dl ± ± ± hs-crp, nmol/l ± ± ± Total cholesterol, mmol/l 5.01 ± ± ± Triglyceride, mmol/l 1.45 ± ± ± Albumin, g/dl 4.31 ± ± ± Glucose, mmol/l 8.07 ± ± ± BUN, mmol/l 6.04 ± ± ± Creatinine, μmol/l ± ± ± Presence of relevant cerebral atherosclerosis 285 (36.54) 181 (35.28) 104 (38.95) Data are shown as number (%) or mean ± standard deviation. NRCA indicates non-relevant cerebral atherosclerosis; SBP, systolic blood pressure; hs-crp, high sensitive C-reactive protein; BUN, blood urea nitrogen. *Comparison between patients with NRCA and those without. 4
9 Supplemental table S3. Prognostic value of NRCA according to the location NIHSS score during 7 days Linear mixed model* mrs after 3 months Ordinal logistic regression Binary logistic regression (mrs 2 vs. mrs>2) N Estimate SE P value N OR 95% CI P value OR# 95% CI P value No NRCA 513 Ref 493 Ref Ref Only extracranial NRCA Only intracranial NRCA Both intracranial and <0.001 extracranial NRCA NIHSS indicates National Institutes of Health Stroke Scale; mrs, modified Rankin Scale; N, number of patient; SE, standard error; OR, odds ratio; CI, confidence interval; hs-crp, high sensitive C-reactive protein; RCA, relevant cerebral atherosclerosis. *adjusted for time of NIHSS score measurement, NIHSS score at admission, sex, age, thrombolysis at admission, and white blood cell count. adjusted for sex, age, NIHSS score at admission, diabetes mellitus, peripheral artery occlusive disease, thrombolysis at admission, white blood cell count, platelet count, hs-crp, albumin, glucose, and RCA. adjusted for sex, age, NIHSS score at admission, current smoking, peripheral artery occlusive disease, white blood cell count, platelet count, hemoglobin, hs-crp, triglyceride, albumin, blood urea nitrogen, and RCA. The estimate indicates the mean change in measured NIHSS score conferred by non-relevant cerebral atherosclerosis (the dependent variables were repeatedly measured NIHSS scores at day 1, day 3 and day 7). The OR indicates the common odds of shifting to a worse mrs category at each cut-off. #The OR indicates the risk of obtaining a poor functional outcome (mrs>2). 5
10 Supplemental figure S1. Examples of patients with non-relevant cerebral atherosclerosis. Diffusion weighted imaging and magnetic resonance angiography are shown. Extracranial cerebral arteries were normal in these patients. A, Relevant cerebral atherosclerosis on right intracranial internal carotid artery, non-relevant cerebral atherosclerosis on left intracranial internal carotid artery and left anterior cerebral artery. B, Relevant cerebral atherosclerosis on left middle cerebral artery, non-relevant cerebral atherosclerosis on right middle cerebral artery. 6
11 Supplemental reference 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: Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, Hertzberg VS, Frankel MR, et al. Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med. 2005;352: Lee BI, Nam HS, Heo JH, Kim DI, Yonsei Stroke T. Yonsei stroke registry. Analysis of 1,000 patients with acute cerebral infarctions. Cerebrovasc Dis. 2001;12:
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