Predictive Value of Susceptibility Vessel Sign for Arterial Recanalization and Clinical Improvement in Ischemic Stroke
Abstract
Background and Purpose—
Our goal was to evaluate whether the presence of a low signal intensity known as susceptibility vessel sign (SVS) on T2*-gradient echo imaging sequence was predictive of arterial recanalization and the early clinical improvement after mechanical thrombectomy.
Methods—
This observational study was based on a prospective database of acute ischemic strokes treated by mechanical thrombectomy. Inclusion criteria were patients with acute anterior ischemic stroke, diagnosed by magnetic resonance imaging, including a T2*-gradient echo imaging sequence, and treated by mechanical thrombectomy. Two independent readers assessed the presence of an SVS. Successful recanalization was defined as a Thrombolysis in Cerebral Infarction score of 2b-3 after mechanical thrombectomy. Early clinical improvement was estimated by the difference between the baseline National Institutes of Health Stroke Scale and the National Institutes of Health Stroke Scale on day 1 after treatment
Results—
The SVS was detected in 137 (76%) out of 180 patients. The kappa interrater agreement was 0.71 with a 95% CI of 0.59 to 0.82. Successful recanalization was associated with an SVS+ with odds ratio, 2.48; 95% CI, 1.05–5.74; P=0.03. The early clinical improvement was better in patients with an SVS+ (median, −6; interquartile range, −11 to 0) compared with SVS− patients (median, −1; interquartile range, −10 to 3) with P=0.01.
Conclusions—
The visualization of SVS is a reliable and easily accessible predictive factor of recanalization success and early clinical improvement.
The benefit of mechanical thrombectomy (MT) in large vessel occlusion acute ischemic stroke (LVOAIS) of the anterior circulation has been established by several randomized trials.1 However, in these series, thrombectomy failed to obtain a successful recanalization (SR), as defined by Thrombolysis in Cerebral Infarction (TICI) 2B/3, in 11 to 41% of the cases. Clots that were retrieved had various macroscopic aspects and histopathologic compositions.2,3 Thrombi with a high level of red blood cells are spontaneously hyperdense on computed tomography and appear with a low signal intensity known as a susceptibility vessel sign (SVS)+ on magnetic resonance imaging (MRI) T2*-gradient echo imaging sequences (T2*-gradient echo imaging).2,4 The SVS is related to the presence of deoxyhemoglobin, which causes inhomogeneities in local magnetic fields and hence signal loss on T2*sequences. Hyperdense clots are associated with SR.2 Previous studies have had controversial results concerning the relationship between SVS+ and SR.2,4–7 Finally, the association between SVS+ and a good clinical outcome has been reported in only one study.5 Our goal was to evaluate whether the presence of an SVS+ was predictive of arterial recanalization and early clinical improvement assessed by the difference between the baseline National Institutes of Health Stroke Scale (NIHSS) and the NIHSS on day 1.
Methods
Data Collection
A retrospective review of stroke in the Toulouse biobank database (DC2016-2804) was performed (January 2015–January 2017) using an institutional board–approved protocol. All consecutive LVOAIS with an MRI on admission and treated by MT were included.
Clinical Information
The authors declare that all supporting data are available within the article. Demographic data, the NIHSS score before and 24 hours after treatment, use of IV tPA (intravenous tissue-type plasminogen activator), and time metrics were collected. Early clinical improvement on day 1 was calculated as NIHSS pretreatment−NIHSS on day 1.
Imaging Data
SVS Analysis
In our center, 3 different MR scans (3T Skyra; Siemens, Erlangen, Germany; or 3T Achieva; Philips, Andover; or 1.5T Optima MR350; General Electric Medical System, Boston) were used for LVOAIS diagnosis using a routine clinical protocol. In addition, some drip and ship patients did undergo an MRI in a remote hospital. As previously reported, the presence or absence of the SVS was retrospectively assessed on T2*-gradient echo imaging by 2 independent investigators.5,6 Interrater agreements for SVS+ or SVS− were assessed using the kappa coefficient and a CI of 95% (Figure).
Endovascular Data
Endovascular procedures were performed on a biplane system (AlluraClarity 20/10; Philips Healthcare, Best, the Netherlands). SR was assessed with the TICI score and defined as TICI 2b or 3.8
Statistical Analysis
For descriptive analyses, continuous variables were expressed as means±SD or medians and interquartile ranges and categorical variables as frequencies and percentages. Clinical characteristics were compared between SVS groups: Wilcoxon tests were used for quantitative variables and χ2 tests for qualitative ones. To test if SVS was associated with TICI and early clinical improvement (NIHSS pretreatment−NIHSS on day 1), a logistic regression model and a linear regression model were used (respectively). The first model was adjusted on age, IV tPA, clot location and the second on age, IV tPA, baseline NIHSS, and TICI. These adjustments were based on clinical considerations.
An alpha level of 5% was used. Data were analyzed using SAS software.
Results
From January 2015 to January 2017, 392 MT were performed in our center. Two hundred and fifty-nine of these patients were diagnosed with LVOAIS by MRI, and 180 of them met all the inclusion criteria.
Baseline characteristics are described in the Table.
| Total | % | SVS+ | % | SVS− | % | P Value* | |
|---|---|---|---|---|---|---|---|
| N=180 | n=137 | n=43 | |||||
| Age | |||||||
| Mean±SD | 68.2±15.9 | 67.4±15.7 | 70.7±16.5 | 0.12 | |||
| NIHSS | |||||||
| Mean±SD | 17±6.3 | 16.7±6.4 | 16.9±6.0 | 0.72 | |||
| Occlusion | |||||||
| No tandem | 146 | 81.1 | 107 | 78.1 | 39 | 90.7 | 0.07 |
| Tandem | 34 | 18.9 | 30 | 21.9 | 4 | 9.3 | |
| Intracranial clot location (tandem included) | |||||||
| T ICA | 38 | 21.1 | 29 | 21.2 | 9 | 20.9 | 0.46 |
| M1 | 110 | 61.1 | 81 | 59.1 | 29 | 67.4 | |
| M2 | 32 | 17.8 | 27 | 19.7 | 5 | 11.6 | |
| IV tPA | |||||||
| No | 62 | 34.4 | 45 | 32.8 | 17 | 39.5 | 0.42 |
| Yes | 118 | 65.6 | 92 | 67.2 | 26 | 60.5 | |
| Time onset-image | |||||||
| Median | 129 | 129 | 128 | 0.65 | |||
| IQR | 89–172 | 90–171 | 76–178 | ||||
| Time groin-recanalization | |||||||
| Median | 45 | 43 | 61 | 0.3 | |||
| IQR | 29–79 | 30–66 | 29–96 | ||||
| Time onset-recanalization | |||||||
| Median | 273 | 269 | 281 | 0.91 | |||
| IQR | 217–344 | 219–340 | 217–347 | ||||
IQR indicates interquartile range; IV tPA, intravenous tissue-type plasminogen activator; M1, first segment of the middle cerebral artery; M2, second segment of the middle cerebral artery; MRI, magnetic resonance imaging; NIHSS, National Institutes of Health Stroke Scale Score; SVS, susceptibility vessel sign; and T ICA, terminal internal carotid artery.
*
χ2 test for qualitative characteristics and Wilcoxon test for quantitative characteristics.
SVS was present (SVS+) in 137 (76%) out of 180 patients. The kappa interrater agreement for SVS+ or SVS− was calculated as K=0.71 with a 95% CI, 0.59–0.82. IV tPA was used in 118 procedures (66%). SR was achieved in 147 (82%) patients. SVS+ was associated with SR with odds ratio, 2.48; 95% CI, 1.05–5.74; P=0.03.
Patients with SVS+ had a higher level of early clinical improvement (median, −6; IQR, −11 to 0) compared with SVS− patients (median, −1; IQR, −10 to 3) with a linear regression coefficient of −2.84; 95% CI, −5.37 to −0.30; P=0.03.
Discussion
Our study demonstrates that SVS+ is associated with a higher rate of SR and better early clinical improvement after MT.
Although interrater agreement was inferior to published kappa statistics for SVS+, it was nevertheless satisfactory.5,6,9,10 Most of the disparities between the findings of the 2 investigators were observed when the clot was hypointense in T2* but did not exceed the size of the same contralateral vessel. We observed a similar ratio of SVS+ (76%), compared with the 73% of SVS+ reported in the largest cohorts.7,9
Previous studies that investigated the relationships between SVS+ and SR and MT are controversial. One publication reported an association between SVS+ and SR,6 contrary to 3 other studies which reported the opposite.4,5,9,10 A similar study analyzed the volume of SVS and found no association with SR.10 Our results show that SVS+ is associated with a higher rate of SR (85% versus 69%).
To our knowledge, no study has reported the predictive value of SVS+ on early clinical improvement on day 1. Our results suggest that patients with SVS+ experienced a higher level of improvement in NIHSS than patients with SVS−. We decided not to collect 3 months modified Rankin Scale because of the drip and ship patients (19.4 %), for whom the modified Rankin Scale evaluation could not be performed by stroke neurologist.
Our study has several limitations. In the first instance, an MRI is needed to evaluate the SVS. Even if a 10-minute expedited protocol is used, MRI takes longer than computed tomography in LVOAIS and is not available for a large proportion of stroke patients. Clot analysis was done on routine T2*-gradient echo imaging brain images. Sequences dedicated to clot visualization such as T2* mapping would improve the analysis and might enable quantitative analysis of the clot structure. Finally, the current study is limited by the absence of long-term clinical outcome follow-up that should be evaluated in a further study.
Conclusions
Our results suggest that in our cohort of patients, SVS is an accessible clinical biomarker associated with SR after thrombectomy and early clinical improvement after MT. Multicentric studies with specially dedicated sequences that focus on basal arteries are required to confirm those results.
References
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Brinjikji W, Duffy S, Burrows A, Hacke W, Liebeskind D, Majoie CBLM, et al. Correlation of imaging and histopathology of thrombi in acute ischemic stroke with etiology and outcome: a systematic review. J Neurointerv Surg. 2017;9:529–534. doi: 10.1136/neurintsurg-2016-012391
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Bourcier R, Brecheteau N, Costalat V, Daumas-Duport B, Guyomarch-Delasalle B, Desal H, et al. MRI quantitative T2* mapping on thrombus to predict recanalization after endovascular treatment for acute anterior ischemic stroke. J Neuroradiol. 2017;44:241–246. doi: 10.1016/j.neurad.2017.03.006
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Bourcier R, Mazighi M, Labreuche J, Fahed R, Blanc R, Gory B, et al; ASTER Trial Investigators. Susceptibility vessel sign in the ASTER trial: higher recanalization rate and more favourable clinical outcome after first line stent retriever compared to contact aspiration. J Stroke. 2018;20:268–276. doi: 10.5853/jos.2018.00192
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© 2019 American Heart Association, Inc.
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History
Received: 22 April 2018
Revision received: 13 November 2018
Accepted: 30 November 2018
Published online: 3 January 2019
Published in print: February 2019
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Disclosures
Dr Cognard is a consultant in Stryker, Microvention, Medtronic, and Cerenovus. Dr Olivot is a consultant in Servier, Astra Zeneca, and Medtronic and receives speaker fee from Bristol-Myers Squibb and Pfizer. The other authors report no conflicts.
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- Susceptibility vessel sign, Radiopaedia.org, (2024).https://doi.org/10.53347/rID-184107
- Association Between MR‐Based Thrombus Imaging Characteristics and Endovascular Therapy Outcome in Acute Ischemic Stroke: A Systematic Review and Meta‐Analysis, Stroke: Vascular and Interventional Neurology, 4, 2, (2024)./doi/10.1161/SVIN.123.001142
- Safety and efficacy of stent retrievers plus contact aspiration in patients with acute ischaemic anterior circulation stroke and positive susceptibility vessel sign in France (VECTOR): a randomised, single-blind trial, The Lancet Neurology, 23, 7, (700-711), (2024).https://doi.org/10.1016/S1474-4422(24)00165-0
- Current Approaches and Methods to Understand Acute Ischemic Stroke Treatment Using Aspiration Thrombectomy, Cardiovascular Engineering and Technology, 15, 4, (481-502), (2024).https://doi.org/10.1007/s13239-024-00735-0
- Identifying ex vivo acute ischemic stroke thrombus composition using electrochemical impedance spectroscopy, Interventional Neuroradiology, (2023).https://doi.org/10.1177/15910199231175377
- Push and Fluff technique for optimization of clot integration with stent-retriever: An in vitro model, Interventional Neuroradiology, (2023).https://doi.org/10.1177/15910199231175348
- Clot composition and recanalization outcomes in mechanical thrombectomy, Journal of NeuroInterventional Surgery, 16, 5, (466-470), (2023).https://doi.org/10.1136/jnis-2023-020117
- Predictive value of clot imaging in acute ischemic stroke: A systematic review of artificial intelligence and conventional studies, Neuroscience Informatics, 3, 1, (100114), (2023).https://doi.org/10.1016/j.neuri.2022.100114
- Impact of width of susceptibility vessel sign on recanalization following endovascular therapy, Journal of the Neurological Sciences, 446, (120583), (2023).https://doi.org/10.1016/j.jns.2023.120583
- Clot Morphology in Acute Ischemic Stroke Decision Making, International Journal of Molecular Sciences, 23, 20, (12373), (2022).https://doi.org/10.3390/ijms232012373
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