Impact of Collateral Status Evaluated by Dynamic Computed Tomographic Angiography on Clinical Outcome in Patients With Ischemic Stroke
Abstract
Background and Purpose—
Status of collateral circulation is a strong predictor of outcome after acute ischemic stroke. Our aim was to compare the predictive value of strategies for collateral blood flow assessment with dynamic computed tomographic angiography (CTA) and conventional single-phase CT angiography.
Methods—
Patients with a proximal middle cerebral artery occlusion underwent noncontrast CT, single-phase CTA and whole brain CT perfusion/dynamic CTA within 9 hours after stroke onset. We defined poor outcome as a score on the modified Rankin Scale score of ≥3. The association between collateral score and clinical outcome at 3 months was analyzed with Poisson regression. The prognostic value of collateral scoring with dynamic CTA and single-phase CTA in addition to age, stroke severity, and noncontrast CT was assessed with logistic regression and summarized with the area under the curve.
Results—
Seventy patients were included, with a mean age of 68 years. We observed an increased risk of poor outcome in patients with poor collaterals on single-phase CTA (risk ratio, 1.8; 95% confidence interval, 1.0–3.1) and on dynamic CTA (risk ratio, 2.0; 95% confidence interval, 1.5–2.7). The prediction of poor clinical outcome by means of collateral adjustment was better with dynamic CTA (area under the curve, 0.84; likelihood ratio test P<0.01) than by single-phase CTA (area under the curve, 0.80; likelihood ratio test P=0.33).
Conclusions—
Collateral assessment with dynamic CTA better predicts clinical outcome at 3 months than single-phase conventional CTA.
Clinical Trial Registration—
URL: http://www.trialregister.nl/trialreg. Unique identifier: NTR1804. URL: http://www.clinicaltrials.gov. Unique identifier: NCT00880113.
Introduction
In approximately 1 of 3 patients, acute ischemic stroke is caused by a proximal occlusion in one of the major intracranial arteries in the anterior circulation.1,2 Recent multiple randomized clinical trials3–6 have shown clinical benefit of adding intra-arterial treatment (IAT) to standard treatment, which is intravenous thrombolysis in a vast majority of cases. Despite these recent advances in endovascular stroke treatment, the likelihood of functional dependence or death at 3 months follow-up is still 40% to 67%.3–6 Strict time windows limit the use of intravenous and intra-arterial therapies. Improved stratification of patients would be of great value to select those patients who will most likely benefit from treatment and those in whom treatment will probably be futile. Strong predictors of outcome may be of potential value for predicting treatment effect.
Clinical factors predicting stroke outcome include age, baseline National Institute of Health Stroke Scale (NIHSS), systolic blood pressure, and hyperglycemia.7 Numerous radiological parameters relate to clinical outcome, such as the extent of early ischemic changes as assessed by the Alberta Stroke Program Early Computed Tomographic Score (ASPECTS),8 location of the occlusion,9 perfusion parameters indicative of infarct core and penumbra,10 and the extent of arterial occlusion as assessed by the clot burden score.11 A promising feature for patient selection in acute stroke treatment is the status of the collateral circulation.12 Especially in patients with a proximal artery occlusion, collateral status has been shown to relate to clinical outcome.13,14 Collateral status has already been used to select patients for endovascular treatment outside the currently used time windows in clinical trials because collaterals can sustain tissue at risk for a longer time period.4
Digital subtraction angiography (DSA) has been considered the gold standard to assess collateral status because of its high temporal and spatial resolution. However, for collateral assessment in acute stroke, DSA is not feasible as a fast diagnostic tool because it is resource intensive and has a higher rate of complications than noninvasive imaging modalities.15 Proper assessment of the collateral status on DSA would also require catheterization of multiple vessels, which is often not performed even when IAT is indicated. A commonly used noninvasive marker to evaluate collateral status is the single-phase computed tomographic angiography (CTA). This technique provides only a snap shot in time of the cerebral vasculature and has been shown to lead to an underestimation of the collateral status.16,17 Dynamic CTA can be derived from CT perfusion (CTP) data sets, herewith providing time-resolved images of the arterial, parenchymal, and venous phases. On dynamic CTA, contrast flow though the brain vasculature can be studied, enabling evaluation of pial arterial backfilling.16,17 The aim of our study was to investigate the value of the collateral status as assessed by dynamic CTA in predicting clinical outcome at 3 months in patients with stroke because of proximal vessel occlusion in the anterior circulation.
Methods
Study Design
Patients were retrospectively selected in a single center from the Dutch Acute Stroke Trial (DUST), a prospective multicentre cohort study18 and the Multicenter Randomized Clinical trial of Endovascular treatment for Acute ischemic stroke in the Netherlands (MR CLEAN).3 We included only ischemic stroke patients with a proximal middle cerebral artery occlusion who underwent a noncontrast CT, single-phase CTA and whole brain CTP/dynamic CTA in our stroke center at presentation. Proximal middle cerebral artery occlusion was defined as occlusion of the M1 or M2 segments, with or without occlusion of the internal carotid artery. Adult patients were included ≤9 hours after symptom onset in the DUST. For the MR CLEAN trial, initiation of IAT had to be possible within 6 hours after symptom onset. For both studies, a score of ≥2 on the National Institutes of Health Stroke Scale was required for inclusion (NIHSS: range, 0–42, with higher scores indicating more severe neurological deficits). Collateral status was not used to select patients into the trials.3,18 Clinical data of patients were collected from previously composed databases provided by the DUST and the MR CLEAN investigators. The primary outcome measure was a poor clinical outcome defined as a modified Rankin Scale score of ≥3 at 90 days, indicating functional dependence or death.
CT Image Acquisition and Image Analysis
Patients were evaluated using a standard protocol, including noncontrast CT, single-phase CTA from aortic arch to vertex, and whole brain CTP/dynamic CTA. Images were obtained with a 320-slice multidetector CT (Aquilion-One Toshiba Medical Systems, Tokyo, Japan), where the 320 detector arrays of 0.5-mm lead to 16-cm whole brain coverage. Infarct volumes at follow-up were provided to us by the DUST and the MR CLEAN investigators.19 Poor radiological outcome was defined as an infarct volume of ≥70 mL at follow-up. Radiological data were assessed independently by a trained neuroradiologist and a trained neurologist who were given information about the clinical symptoms only. Interobserver agreement was evaluated after the 2 raters independently assessed all dynamic CTAs (see Methods section in the online-only Data Supplement for more information about acquisition and image analysis).
Collateral Scores
Collateral Score on Single-Phase CTA
On single-phase CTA, we used the Tan Collateral grading system20 Tan Collateral grading system uses a 4 scale grading system: 0=absent collaterals, 1=collaterals filling ≤50% of the occluded territory, 2=collaterals filling >50% but <100% of the occluded territory, and 3=collaterals filling 100% of the occluded territory. For single-phase CTA, a pial arterial filling score of 0 to 1 was considered poor.
Collateral Score on Dynamic CTA
Individual volumes of the whole brain CTP acquisition (19 volumes) were evaluated to fully appreciate the extent and speed of filling. To assess the extent of filling, we divided the anterior circulation into 4 regions. First, the brain was divided into a superior and inferior part, with regard to the level of the body of the caudate nucleus. Second, left and right hemispheres were evaluated separately. Subsequently, we scored the extent of vessel filling for each volume in the 4 different brain regions in a similar way as the collateral score described by Tan et al.20 The extent of filling for each hemisphere was calculated by adding the collateral score of the lower level to that of the upper level. This resulted in a score ranging from 0 (no vessel filling) to 6 (complete vessel filling) for each hemisphere (Figure 1). For dynamic CTA, a pial arterial filling score of 0 to 3 was considered poor.
To assess the speed of collateral filling, we analyzed all dynamic volumes, covering the arterial, capillary, and venous phases. Because the time points of all dynamic volumes were known, we were able to calculate duration of contrast filling of vessels from contrast arrival at the internal carotid artery, as recorded by the appearance of contrast at the level of the skull base, until maximal filling of cerebral vessels for each hemisphere was reached. We compared duration of filling of the cerebral vessels in the symptomatic hemisphere to the nonaffected hemisphere and calculated the median difference for all patients. On the basis of this median difference, fast versus slow collateral filling was defined (see Table I and Figure I for more details in the online-only Data Supplement).
Statistical Analysis
We analyzed the association between clinical or radiological characteristics and poor clinical outcome (modified Rankin Scale score, ≥3) after 3 months with Poisson regression analysis. The additional prognostic value of collateral score as assessed on dynamic CTA when compared with single-phase CTA over clinical and radiological parameters on clinical outcome was analyzed with logistic regression models. In a first basic model (model 1), the variables age, admission NIHSS score, and treatment were used. These variables were previously identified to predict clinical outcome.3,21 In a second model, based on model 1, the ASPECT score at presentation was added. For the final models, we added the collateral score with single-phase CTA to model 2 in model 3a, and the collateral score as assessed with dynamic CTA in model 3b. Subsequently, the area under the curve of the receiver-operating characteristic curves (AUC–ROC) was calculated for all models and potential improvements between the final models and the initial models were determined. Comparison of AUC–ROCs between hierarchical models was done with the likelihood ratio test. The association between collateral status and radiological outcome was analyzed with Poisson regression.
Results
Patients
Between July 2010 and July 2014, a total of 70 patients were eligible for evaluating the collateral status on dynamic CTA. Thirty-seven patients were selected from the DUST and 33 patients from the MR CLEAN trial. The mean age of the study participants was 68 years (range, 26–98); median NIHSS was 14, and 34 participants (49%) were women. Median time from symptom onset to multimodel CT imaging was 67 minutes. Most patients were treated with intravenous thrombolysis (64%) alone, whereas IAT was performed in 17 patients (24%; Table 1). Follow-up imaging with noncontrast CT was performed in 61 patients (87%). At 3 months follow-up, 42 patients (60%) had a poor clinical outcome (modified Rankin Scale score, 3–6) and eighteen patients (26%) were dead.
| Clinical Characteristics | No. (%)* |
|---|---|
| Baseline | |
| Age, y, mean (SD) | 68 (14) |
| Female sex | 34 (49%) |
| NIHSS, median (IQR) | 14 (11–19) |
| Premorbid modified Rankin Scale score, 0–2 | 67 (96%) |
| History of stroke/TIA | 11 (16%) |
| History of hypertension | 31 (44%) |
| History of diabetes mellitus | 10 (14%) |
| History of hyperlipidemia | 13 (19%) |
| History of myocardial infarction | 9 (13%) |
| History of atrial fibrillation | 16 (23%) |
| Systolic blood pressure in mmHg, mean (SD) | 144 (22) |
| Diastolic blood pressure in mmHg, mean (SD) | 81 (15) |
| Serum glucose at arrival, mean (SD) | 7.3 (2) |
| INR at arrival >1.7 | 3 (4%) |
| Treatment | |
| No intravenous thrombolysis, no endovascular treatment | 8 (11%) |
| Only intravenous thrombolysis | 45 (64%) |
| Only mechanical thrombectomy | 3 (4%) |
| Intravenous thrombolysis and mechanical thrombectomy | 14 (20%) |
| Process times (min) | |
| Stroke onset to study CT (n=70), median (IQR) | 67 (44–114) |
| Stroke onset to start of IV alteplase (n=59), median (IQR) | 94 (73–135) |
| Stroke onset to groin puncture (n=17), median (IQR) | 226 (200–249) |
CT indicates computed tomography; INR, international normalized ratio; IQR, interquartile range; IV, intravenous; NIHSS, National Institute of Health Stroke Scale; and TIA, transient ischemic attack.
*
All values are given as number (%), unless otherwise indicated.
Univariable Analyses
Clinical predictors of poor clinical outcome at 3 months follow-up were age ≥60 years (risk ratio [RR], 2.1; 95% confidence interval [CI], 1.1–4.1), history of stroke or transient ischemic attack (RR, 1.7; 95% CI, 1.2–2.3), and involvement of the internal carotid artery (RR, 1.6; 95% CI, 1.2–2.3). About treatment effect, no significant differences between the different modalities could be demonstrated. A trend was observed for later onset to treatment times and poor clinical outcome (Table II in the online-only Data Supplement). A low ASPECT score, a low clot burden score and poor cerebral blood flow at presentation were associated with poor clinical outcome at follow-up. Infarct volume on follow-up noncontrast CT (ie, ≥70-mL infarct volume) was most strongly related to poor clinical outcome at 3 months (RR, 5.3; 95% CI, 2.4–11.7; Table III in the online-only Data Supplement).
Interobserver agreement for assessment of collateral extent with dynamic CTA was excellent (k=0.86; n=70). Table 2 shows that poor clinical outcome at follow-up was more strongly related to our predefined poor arterial filling score on dynamic CTA (RR, 2.0; 95% CI, 1.5–2.7) compared with a poor arterial filling score on single-phase CTA (RR, 1.8; 95% CI, 1.0–3.1). Moreover, risk of poor clinical outcome decreased with increasing dynamic CTA collateral scores (Table 2). Poor collateral status as assessed with dynamic CTA was also more strongly associated with poor radiological outcome at follow-up (n=61, RR, 1.9; 95% CI, 1.3–2.9) than with single-phase CTA (RR, 1.4; 95% CI, 0.8–2.5). For the entire study population (n=70), dynamic CTA analysis showed that the median time difference between optimal filling of the healthy hemisphere when compared with the affected hemisphere was 4.5 s. Fast filling was defined as optimal filling within 4.5 s after optimal filling in the nonaffected hemisphere. Combining the extent and speed of filling, poor outcome was seen in 11 of 26 patients (42%) with good collaterals and fast arterial filling in the affected middle cerebral artery territory. Almost similar results (poor outcome in 14 of 26 patients; 54%) were observed in patients with good collaterals but slow filling of the affected hemisphere. In contrast, 11 of 12 patients (92%) with poor collaterals and fast filling, and all 6 patients with poor collaterals and slow filling, had poor clinical outcome at follow-up.
| Risk of Poor Clinical Outcome at Follow-Up (n/N %) | |||
|---|---|---|---|
| Poor Outcome (n)/Characteristic Present (N) | Poor Outcome (n)/Characteristic Absent (N) | Risk Ratio (95% CI) | |
| Single-Phase CTA | |||
| Poor extent of collateral filling* | 33/47 (70%) | 9/23 (39%) | 1.8 (1.0–3.1) |
| Dynamic CTA and extent of filling | |||
| CS 0–1 | … | … | … |
| CS 2 | 5/5 (100%) | 10/25 (40%)† | 2.5 (1.5–4.0) |
| CS 3 | 12/13 (92%) | 10/25 (40%)† | 2.3 (1.4–3.8) |
| CS 4 | 10/14 (71%) | 10/25 (40%)† | 1.8 (1.0–3.2) |
| CS 5 | 5/13 (39%) | 10/25 (40%)† | 1.0 (0.4–2.2) |
| Dynamic CTA | |||
| Poor extent of collateral filling* | 17/18 (94%) | 25/52 (48%) | 2.0 (1.5–2.7) |
| Dynamic CTA, extent, and timing of filling | |||
| Poor collaterals and slow filling | 6/6 (100%) | 11/26 (42%)‡ | 2.4 (1.5–3.7) |
| Poor collaterals and fast filling | 11/12 (92%) | 11/26 (42%)‡ | 2.2 (1.3–3.5) |
| Good collaterals and slow filling | 14/26 (54%) | 11/26 (42%)‡ | 1.3 (0.7–2.3) |
CI indicates confidence interval; CS, collateral grading system; CTA, computed tomographic angiography; and mRS, modified Rankin scale.
*
Poor extent of collateral filling was defined as collateral filling in ≤50% of the occluded middle cerebral artery territory in the affected hemisphere.
†
Collateral score 6 (maximum collateral score) was taken as a reference.
‡
Group with good and fast collateral filling was taken as a reference.
Multivariable Analyses
At ROC analysis (Figure 2), the AUC was 0.77 for model 1, which included the clinical variables age, NIHSS at admission, and treatment to predict clinical outcome at 3 months follow-up. Adding the baseline ASPECT score to model 1 resulted in model 2 with an AUC of 0.78. Adding collateral status as assessed with single-phase CTA to model 2 resulted in model 3a with an AUC of 0.80. The likelihood ratio test showed no significant increase in predictive value between model 2 and 3a (P=0.33). Adding collateral status as assessed with dynamic CTA to model 2 resulted in model 3b (AUC, 0.84). The prediction of clinical outcome was better with model 3b compared with model 2 (P<0.01).
Discussion
Our study showed that collateral status assessed by dynamic CTA better predicts clinical outcome at 3 months than single-phase conventional CTA in patients with acute ischemic stroke caused by a proximal occlusion in the anterior circulation. Also, follow-up infarct volume was more accurately predicted by dynamic CTA, as was previously demonstrated by others.16 In our study, a higher percentage of poor collateral status (ie, filling of <50% of the affected middle cerebral artery territory) was seen with single-phase CTA when compared with dynamic CTA. This probably reflects the earlier reported underestimation of collateral circulation by single-phase CTA.16,17 Dynamic CTA allows for reliable differentiation between antegrade and retrograde vessel filling and, therefore, provides more information than single-phase CTA. Interestingly, the extent of collateral vessel filling was more strongly associated with clinical outcome than the speed of filling. Optimization of the conventional CTA scanning with ≥3 strategic time points (ie, multiphase CTA) could, therefore, probably be sufficient for the assessment of the complete collateral circulation.22 A comparison between the predictive value of dynamic versus multiphase CTA is warranted, especially because multiphase CTA requires less radiation dose and has been reported to be less sensitive to patient motion.22 However, in our study only 2 patients were excluded because of poor imaging quality as a result of motion artifacts. An advantage of dynamic CTA over multiphase CTA is the fact that information from CTP could be used for patient selection in acute stroke management.23 Interestingly, in our dynamic CTA study 36% of patients had a maximum collateral score, which is almost identical to the 35% of patients who had complete collateral flow on DSA in the Interventional Management of Stroke (IMS) III trial.13 Similarly, this trial showed a strong association between collateral status on DSA and clinical outcome. Unfortunately, in our study we were not able to directly compare dynamic CTA to DSA. DSA was performed in <25% of our patients. Moreover, in our IAT patients the diagnostic value of DSA was further limited because only the carotid artery ipsilateral to the occluded target vessel was injected. A proper assessment of the extent and speed of collateral filling taking into account the entire collateral circulation could, therefore, not be performed with our DSA data. This reflects a commonly encountered issue in clinical practice with collateral assessment by DSA in the acute stroke setting.
The main limitation of this study is the relatively low number of patients. Our study was not powered to study collateral status and the interaction with different treatment types, mostly because of the small IAT group. Conclusions about patient selection for endovascular therapy cannot be derived from this study. Future studies should include follow-up dynamic CTA/CTP studies to study the interaction between collaterals, recanalization, reperfusion, and clinical outcome. Another limitation is that patients were selected from 2 different studies. IAT was performed in some patients who were included in the DUST study in which patients were not randomized for endovascular treatment. However, all patients from the DUST study included in our study fulfilled the additional inclusion criteria from the MR CLEAN trial. More specifically, all IAT patients from the DUST study were treated within the 6-hour time-window and intravenous thrombolysis was given within 4.5 hours after symptom onset. All clinical data, including modified Rankin Scale score at follow-up, were collected prospectively in both studies.
In conclusion, the use of dynamic CTA looks promising for implementation in future studies and clinical practice. Unlike DSA, standard implementation of dynamic CTA is possible in the acute phase of ischemic stroke. Images can be acquired noninvasively and rapidly, with the entire scan protocol completed within 5 minutes. Postprocessing can construct an angiography-like movie displaying all intracranial vessels simultaneously, facilitating interpretation of the collateral status of patients with stroke in the acute stage. Although collateral assessment by dynamic CTA requires validation by future research, it could speed up the routine and has the potential to improve decision making in acute stroke treatment.
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The image is taken from an article in this issue, “Time-Dependent Computed Tomographic Perfusion Thresholds for Patients With Acute Ischemic Stroke” by d’Esterre et al (Stroke. 2015;46:3390–3397).
The image is from Figure 3.
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© 2015 American Heart Association, Inc.
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History
Received: 9 June 2015
Revision received: 16 September 2015
Accepted: 6 October 2015
Published online: 5 November 2015
Published in print: December 2015
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Disclosures
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Sources of Funding
Dr Wermer is supported by a personal grant from the Netherlands Organisation for Scientific Research (NWO/ZonMw-VENI grant) and the Dutch Heart Foundation. The Dutch Acute Stroke Trial study was supported by the Dutch Heart Foundation and the NutsOhra Foundation. Dr Velthuis is a regular presenter for Philips Healthcare. The Multicenter Randomized Clinical trial of Endovascular treatment for Acute ischemic stroke in the Netherlands trial was supported by the Dutch Heart Foundation and by unrestricted grants from AngioCare Covidien/EV3, Medac/Lamepro, and Penumbra.
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