Published online before print November 6, 2008, doi: 10.1161/STROKEAHA.108.515817
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(Stroke. 2009;40:187.)
© 2009 American Heart Association, Inc.
Original Contributions |
DWI Lesions and TIA Etiology Improve the Prediction of Stroke After TIA
From the Departments of Neurology (D.C., E.T., G.T., J.-L.M.) and Neuroradiology (C.O., J-F.M), Centre Hospitalier Sainte-Anne, Paris Descartes University INSERM U894, Paris, France.
Correspondence and reprint requests to Pr Jean-Louis Mas, Service de Neurologie, Hôpital Sainte-Anne, 1 rue Cabanis, 75014 Paris, France. E-mail jl.mas{at}ch-sainte-anne.fr
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Abstract |
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Background and Purpose— The ABCD2 score has been shown to predict the early risk of stroke after transient ischemic attack (TIA). The additional predictive value of diffusion-weighted imaging (DWI) and TIA etiology is not well known.
Methods— From January 2003 to June 2007, 343 consecutive patients (mean±SD age, 62.4±15.4 years) with TIA were admitted to our stroke unit. Most (339) patients underwent DWI and all had an etiologic work-up and were followed up for 3 months. The predictive value of the ABCD2 score, positive DWI findings, large-artery atherosclerosis (LAA), and atrial fibrillation (AF) with respect to occurrence of ischemic stroke at 1 week and 3 months was assessed.
Results— DWI was positive in 136 (40%) patients. Sixty (17%) patients had LAA and 27 (8%) had AF. Patients with positive DWI findings were more likely to have unilateral weakness (odds ratio [OR]=2.2; 95% CI, 1.3 to 3.7), TIA duration 
60 minutes (OR=2.6; 95% CI, 1.3 to 5.2), ABCD2 >5 (OR=4.7; 95% CI, 2.0 to 11.0), LAA (OR=1.8; 95% CI, 1.0 to 3.1), and AF (OR=3.5; 95% CI, 1.5 to 8.0). During follow-up, 5 patients had a stroke within 7 days (absolute risk=1.5%, 95% CI, 0.3% to 2.7%), and 10 had a stroke within 3 months (absolute risk=2.9%; 95% CI, 1.1% to 4.7%). All early strokes but 1 occurred in patients with positive DWI findings. ABCD2 score and positive DWI findings were associated with an increased 7-day and 3-month risk of stroke. At 3 months, ABCD2 score >5 (hazard ratio=10.1; 95% CI, 1.1 to 93.4), positive DWI result (hazard ratio=8.7; 95% CI, 1.1 to 71.0), and LAA (hazard ratio=3.4; 95% CI, 1.0 to 11.8) were independently associated with an increased risk of stroke. There was no association with AF.
Conclusions— Taking DWI and TIA etiology into account in addition to the ABCD2 score improves the prediction of the early risk of stroke after TIA.
Key Words: atherosclerosis • diffusion-weighted imaging • prognosis • transient ischemic attack
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Introduction |
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The early risk of stroke after transient ischemic attack (TIA) is higher than previously thought and is predictable from simple clinical features.1–3 The ABCD2 clinical score has been shown to accurately predict that risk in population- and emergency department–based studies.1 It has also been suggested that the presence of ischemic lesions on diffusion-weighted imaging (DWI) and TIA etiology, such as large-artery atherosclerosis (LAA)4 and atrial fibrillation (AF), could improve stroke risk prediction after TIA.4–7 However, studies that assessed the prognostic value of positive DWI findings and TIA etiology either were underpowered or used composite outcomes that included cardiac events or recurrent TIA.5–10 Moreover, because positive DWI findings and TIA etiology may be correlated with several components of the ABCD2 score,11,12 it remains uncertain whether those potential factors can predict the early risk of stroke independently of the ABCD2 score. We therefore assessed the additional value of positive DWI findings and TIA etiology to predict the early risk of stroke in a cohort of 343 consecutive TIA patients admitted to a stroke unit.
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Methods |
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Among 2032 consecutive patients admitted to our stroke unit for ischemic stroke or TIA from January 2003 to June 2007, 343 patients with probable or possible TIA according to National Institute of Neurological Disorders and Stroke criteria13 and who were admitted within 48 hours of symptom onset were enrolled. Patients are referred to our stroke unit by emergency departments from different hospitals located in our geographic area, general practitioners, and emergency ambulance services. Patients are admitted as soon as possible after the neurologist is contacted by telephone; no selection criteria were applied for TIA and they were treated as inpatients. Data on management and DWI–magnetic resonance imaging (MRI) findings of the first patients enrolled in this cohort have been previously reported.8,14,15 Demographic data, vascular risk factors, and past medical history were collected at the time of admission on a standardized case report form. The first blood pressure recorded after TIA was collected from general practitioner notes, emergency department notes, or at admission to the stroke unit, depending on where the patient was first examined after the TIA. In patients with several recent TIAs, the most recent event was considered.
Among the 343 enrolled patients, all but 4 (pacemaker in 2 and prosthetic valve in 2) underwent brain MRI (1.5-T MRI unit equipped with echoplanar capability; Signa, General Electric Medical Systems, Milwaukee, Wis) within the day after admission. Our routine MRI stroke protocol included the following sequences acquired in the axial plane: spin-echo DWI (b=0 to 1000 s/mm2), fast fluid-attenuated inversion recovery, gradient-echo T2-weighted and 3D time-of-flight angiography of the circle of Willis. The presence of acute ischemic lesions was defined by areas of high signal intensity on DWI. All films and reports were retrospectively reviewed without knowledge of baseline clinical and follow-up data.
All patients underwent a standardized etiologic work-up, including standard blood tests, 12-lead ECG, prolonged 3-lead cardiac monitoring, and Doppler ultrasound. All Doppler ultrasound scans were performed with a Phillips ATL 5000 echograph, and standardized diagnostic criteria were used for artery stenosis.16 Cervical gadolinium-enhanced MR angiography was performed in 307 (90%) patients. Those who did not undergo MR angiography had either normal Doppler results or contraindications to MRI. Most patients (340, 99%) underwent transthoracic echocardiography, and 269 (78%) underwent transesophageal echocardiography. LAA was defined, according to TOAST classification, as the presence of a 50% stenosis (degree of stenosis measured by the NASCET method for lesions at the carotid artery bifurcation or by using the ratio of the luminal diameter at the site of maximal narrowing to the diameter of normal artery for other arteries) or occlusion presumably due to atherosclerosis in the clinically relevant extracranial or intracranial artery.17 AF was considered present if it was previously known or diagnosed at admission or during hospitalization. Patients were routinely reassessed at 3 months by a neurologist from our department, and the occurrence of stroke, TIA, myocardial infarction, or death was recorded. Two patients were lost to follow-up at 7 and 8 days. Two hundred fifty-eight (76%) patients had a face-to-face follow-up visit at 3-months, and 60 had a telephone interview. In 23 patients who could not be assessed in person or by telephone, follow-up data were obtained from their general practitioners.
Statistical Analysis
We calculated individual ABCD2 scores.1 Data were expressed as mean±SD, median with interquartile range (IQR), or percentage, where appropriate. Kaplan-Meier survival analysis was used to assess the cumulative risk of ischemic stroke. The predictive value of the ABCD2 score, positive DWI result, LAA, and AF with respect to the occurrence of ischemic stroke at 1 week and 3 months was assessed with the use of log-rank tests and Cox proportional-hazards models. Prespecified cutoffs were used for the ABCD2 score as previously proposed1: <4=low risk, 4 to 5=moderate risk, and >5=high risk. To quantify the predictive value of the ABCD2 score, we calculated areas under the receiver operating characteristic curve (c statistics) and their 95% CIs. The c statistic integrates measures of sensitivity and specificity of the range of a variable. Ideal prediction produces a c statistic of 1.00, whereas prediction no better than chance is associated with a statistic of 0.50. Statistical analyses were performed with the SPSS statistical package, version 15.0. To quantify the predictive value of the ABCD2 score alone and with positive DWI and TIA etiology, we used the predicted probabilities calculated from regression logistic models to calculate c statistics.
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Results |
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Among the 343 patients enrolled in the study, 301 (88%) had a probable TIA (including 21 patients with amaurosis fugax) and 42 had a possible TIA. The median (IQR) time from TIA onset to admission to the stroke unit was 11.0 (5.0 to 22.5) hours. The characteristics of the patients are shown in Table 1. The carotid territory was involved in 198 (58%) patients, the vertebrobasilar territory in 85 (25%), and undetermined territory in 59 (17%). Sixty patients had LAA (extracranial carotid artery, n=38; basilar artery, n=7; other extra- or intracranial arteries, n=15) and 27 had AF (previously known, n=19; diagnosed at admission, n=5; diagnosed during hospitalization, n=3). Among the 38 patients with LAA carotid artery TIA, endarterectomy was performed in 12 patients and angioplasty/stenting in 3 between 4 and 22 days after TIA, with no complications. The 23 remaining patients had either 50% to 69% nonsurgical carotid artery stenosis (n=11) or carotid artery occlusion (n=12). Regarding patients with AF, anticoagulation was started or adjusted at admission in 24 patients and started at the time of diagnosis in 3.
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The median (IQR) time from TIA onset to DWI was 19.5 (8.0 to 28.3) hours. Acute ischemic lesions were demonstrated by DWI in 136 patients (40%). As shown in Table 1, patients with positive DWI findings were more likely to have unilateral weakness as a symptom of TIA (OR=2.2; 95% CI, 1.3 to 3.7), TIA duration 60 minutes (OR=2.6; 95% CI, 1.3 to 5.2), ABCD2 >5 (OR=4.7; 95% CI, 2.0 to 11.0), LAA (OR=1.8; 95% CI, 1.0 to 3.1), and AF (OR=3.5; 95% CI, 1.5 to 8.). Conversely, they were less likely to have a history of diabetes mellitus (OR=0.4; 95% CI, 0.2 to 1.0), although the difference was not statistically significant (P=0.06). There was an association between ABCD2 score and AF (ABCD2 4 to 5, OR=1.5; 95% CI, 0.6 to 4.0; ABCD2 >5, OR=5.5; 95% CI, 1.8 to 17.1) but no significant association with LAA (ABCD2 4 to 5, OR=1.4; 95% CI, 0.8 to 2.6; ABCD2 >5, OR=1.7; 95% CI, 0.7 to 4.6).
During follow-up, 10 patients had ischemic stroke, 14 had recurrent TIA, and 2 died of cancer. Five ischemic strokes occurred within the first week after the qualifying event, of which 4 were within 48 hours. All strokes but 1 occurred in the same arterial territory as that of the TIA, and we did not identify any new etiology (Table 2). The absolute risk of ischemic stroke was 1.2% (95% CI, 0.0% to 2.4%) at 48 hours, 1.5% (95% CI, 0.3% to %2.7) at 7 days, and 2.9% (95% CI, 1.1% to 4.7%) at 3 months.
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As shown in Table 3, the 5 strokes that occurred within 7 days and 9 of the 10 strokes that occurred within 3 months were in patients with baseline ABCD2 scores 4. In patients with ABCD2 scores >5, all strokes occurred in patients with positive DWI findings (n=21, 70%). LAA accounted for 2 of the 3 strokes that occurred within 7 days and 2 of the 4 strokes that occurred within 3 months. In patients with ABCD2 scores of 4 or 5, all strokes occurred in those with positive DWI findings (n=69, 40%). LAA accounted for none of the 2 strokes that occurred within 7 days and 2 of the 5 strokes that occurred within 3 months. One stroke that occurred within 3 months was in a patient with an ABCD2 score <4 and normal DWI results. That patient had LAA.
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In univariate analysis, ABCD2 score and positive DWI were significantly associated with an increased risk of stroke at 7 days and 3 months (Table 4). LAA was associated with an increased risk of stroke at 3 months. By contrast, there was no significant association with AF. At 3 months, in multivariate Cox analysis including positive DWI (hazard ratio [HR]=8.7; 95% CI, 1.1 to 71.0), ABCD2 score (score >5, HR=10.2; 95% CI, 1.1 to 93.4; score 4 to 5, HR=3.3; 95% CI, 0.4 to 28.7) and LAA (HR=3.4; 95% CI, 1.0 to 11.8) remained associated with an increased risk of stroke, although the result was not statistically significant for an ABCD2 score of 4 or 5.
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The absolute risk of stroke in patients with ABCD2 scores 4 was 2.5% (95% CI, 0.4% to 4.7%) at 7 days and 4.4% (95% CI, 1.7% to 7.1%) at 3 months. The absolute risk in patients with ABCD2 scores 4 and positive DWI findings was 5.4% (95% CI, 0.9% to 9.9%) at 7 days and 9.7% (95% CI, 3.6% to 15.8%) at 3 months. The absolute risk in patients with an ABCD2 score 
4, positive DWI, and LAA was 9.3% (95% CI, 0% to 21.6%) at 7 days and 18.2% (95% CI, 2.1% to 34.1%) at 3 months. The 3-month prognostic value of ABCD2 score, assessed by c statistics, was 0.75 (95% CI, 0.61 to 0.89). The c statistic rose to 0.84 (95% CI, 0.70 to 0.97) when DWI was added and to 0.87 (95% CI, 0.78 to 0.96) when LAA was added.
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Discussion |
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This study, which enrolled a large number of TIA patients who systematically underwent DWI-MRI and etiologic investigations, shows that in addition to the ABCD2 score, positive DWI and, to a lesser extent, LAA are independently associated with an increased early risk of stroke after TIA.
The absolute risks of ischemic stroke after TIA were 1.5% at 7 days18 and 2.9% at 3 months,19 which is consistent with the rates reported in previous specialist stroke service–based studies.20,21 Interestingly, despite a low early risk of stroke in our population, the ABCD2 score remained useful to predict the risk of stroke, with 90% (n=9) of strokes occurring in 59% of patients (n=201) with an ABCD2 score 4. The c statistic (0.75) was similar to that found in the populations used to validate the ABCD2 score.1
We found that 40% of TIA patients had positive DWI results. This prevalence is in keeping with those observed in previous studies, ranging from 21% to 67%.9,22–25 A positive DWI result was associated with some components of the ABCD2 score but remained significantly associated with an increased early risk of stroke after adjustment for ABCD2 score. Interestingly, all strokes in patients with ABCD2 scores 4 (n=201) occurred in those with DWI lesions (n=90, 45%; Table 2), which emphasizes the ability of DWI to further identify patients at high early risk of stroke after TIA. The predictive value of ischemic lesions on computed tomography and DWI in TIA patients has been reported in previous studies, but none of them took both DWI and ABCD2 score into account in prognostic models.5–7,10,26 In the largest of those studies,7 TIA patients with a positive DWI result were 
10 times more likely to have a TIA or stroke than those with negative DWI results, a relative risk very close to that observed in our study. The fact that some TIA patients with normal DWI findings had nonischemic events such as epileptic, migrainous, or somatoform disease might explain our finding that DWI is a predictor of early stroke in TIA patients. However, this proportion is likely to be small in specialized settings and would probably not entirely explain the finding.
We found that LAA was also an independent predictor of early risk of stroke, which is consistent with a recent study showing that TIA patients with LAA had the highest risk of stroke at 3 months (20% vs 5.7% in other etiologies)4 and with previous studies conducted in population-based cohorts showing an increased risk of recurrent stroke in patients with LAA.27,28 In our population, LAA (n=60 patients, 17%) accounted for 50% of strokes occurring within 3 months. Patients with an ABCD2 score 4, DWI lesions, and LAA had the highest early risk of stroke (18% at 3 months), although they represented only 6.5% (n=22) of our population. By contrast, we did not find a significant association between AF and risk of stroke. This finding could be explained by a beneficial effect of early anticoagulation in those patients.29 However, the lack of association needs to be interpreted cautiously because of the small number of patients with AF, which might partly result from the relatively young age of our population.
Several potential limitations need to be addressed. First, our study was conducted in a specialist stroke service, and although we did not apply any criteria for admission of TIA patients, selection biases may have occurred. The mean age of our population was lower than that of population-based studies,1 but the prevalences of risk factors and of DWI lesions were comparable to those found in previous hospital-based studies. Very similar low risks of stroke were reported in large population- and hospital-based studies with urgent assessment and immediate treatment of TIA patients.20,21 Therefore, the low risks observed in our study are likely to be related to early management8,20,21 rather than to selection biases. Second, it is unlikely that the relative effects of DWI and LAA in predicting early risk of stroke would have been very different in a higher-risk population. Third, because we used a single-center study design, our findings would need to be confirmed in other settings to be generalized. However, all of the predictors that we found have been suggested in previous studies. Finally, the small number of outcome events in our study may have affected the accuracy and precision of regression coefficients in multivariate analysis.30 However, considering the strength of the associations in univariate analysis (HR >3 for each predictive factor)31 and the absence of effect of adjustment in multivariate models, we think that the predictors that we have identified are likely to be independent.
This study has several practical implications. First, the ABCD2 score has the same predictive ability in a specialist stroke service, characterized by a low early risk of stroke, as in large population- or emergency department–based cohorts of patients with TIA.1 Second, MRI improves the prediction of stroke after TIA, which underlines the need to perform DWI-MR quickly after TIA. The predictive value of positive DWI findings may be of particular interest in patients with a moderate risk according to the ABCD2 score to select the subset of patients at highest risk of stroke. Third, considering the high risk in patients with LAA and the increased benefit resulting from early endarterectomy in patients with symptomatic carotid stenosis,32 our study reinforces the need for an urgent arterial work-up to look for LAA in TIA patients. Although we were unable to prevent all recurrent events in patients with LAA, the rate of stroke recurrence was lower than that observed in previous studies in the subgroup of patients with TIA and/or minor stroke related to LAA.4,28 Taken together, all of these factors could help to organize emergency triage of TIA patients and identify those who require admission to specialist stroke services.
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Acknowledgments |
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Disclosures
None.
Received January 29, 2008; revision received May 7, 2008; accepted May 30, 2008.
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