Association Between MR‐Based Thrombus Imaging Characteristics and Endovascular Therapy Outcome in Acute Ischemic Stroke: A Systematic Review and Meta‐Analysis

Mohammad Hossein Abbasi; Adrienne N Dula; Steven J Warach; Hamidreza Saber

doi:10.1161/SVIN.123.001142

. 2024 Feb 10;4(2):e001142. doi: 10.1161/SVIN.123.001142

Association Between MR‐Based Thrombus Imaging Characteristics and Endovascular Therapy Outcome in Acute Ischemic Stroke: A Systematic Review and Meta‐Analysis

Mohammad Hossein Abbasi ¹, Adrienne N Dula ¹, Steven J Warach ^1,², Hamidreza Saber ^1,^2,^3,^✉

PMCID: PMC12778482 PMID: 41583600

Abstract

Background

Prediction of successful revascularization and achieving a favorable functional outcome may help determine the optimal treatment strategy and improve the management of stroke. A growing body of literature has implicated a predictive value for thrombus imaging characteristics for stroke outcomes.

Methods

We conducted an electronic search using PubMed, Ovid MEDLINE, and EMBASE, previously published meta‐analyses, and systematic review studies that intervened by endovascular thrombectomy or intravenous thrombolysis following large vessel occlusion stroke from 2000 to 2023 and involved magnetic resonance‐based thrombus imaging, then screened 2007 studies against our eligibility criteria. We extracted the enrollees’ characteristics and the association between clot features and radiological and functional outcome measures.

Results

Thirty‐three studies were found eligible, with a total number of 6902 enrollees. Susceptibility vessel sign was found in 3531 subjects (51.2%). Nine studies involved only the administration of intravenous thrombolysis, whereas 24 studies intervened by endovascular thrombectomy. Seventeen studies found at least an association between thrombus imaging characteristics and successful revascularization, whereas the others reported no association. only 13 studies found at least one thrombus characteristic associated with functional outcome, while the others showed no association between the thrombus characteristics and functional outcome after stroke. Pooled meta‐analysis of studies that involved endovascular thrombectomy with or without intravenous thrombolysis showed a statistically significant association between the presence of susceptibility vessel sign and both successful reperfusion (odds ratio [OR]: 1.57 [1.09–2.27]; P = 0.02) and favorable functional outcome (OR: 1.76 [1.17–2.66]; P = 0.007).

Conclusion

The presence of susceptibility vessel sign on magnetic resonance‐based clot imaging was associated with functional outcome and successful reperfusion following thrombectomy.

Keywords: large vessel occlusion, magnetic resonance imaging (MRI), stroke, susceptibility vessel sign, thrombus characteristics

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Nonstandard Abbreviations and Acronyms

CBS: clot burden score
ELVO: emergent large vessel occlusive strokes
SWI: susceptibility weighted imaging
TICI: Thrombolysis In Cerebral Infarction

Clinical Perspective

In this updated meta‐analysis, susceptibility vessel sign on preinterventional magnetic resonance imaging was associated with significantly higher rates of successful reperfusion and favorable clinical outcomes following thrombectomy in acute ischemic stroke.
Magnetic resonance imaging thrombus characteristics provide important information on radiographic and clinical outcomes in acute large vessel occlusion strokes and may be used to tailor optimal treatment strategies in this population.

Recent trials have employed advanced parenchymal imaging techniques by magnetic resonance imaging (MRI) to patient selection for endovascular thrombectomy (EVT) or intravenous thrombolysis (IVT) to manage emergent large vessel occlusive strokes (ELVO). ¹ , ² , ³ Despite advancements in the treatment of ELVO, a considerable proportion of these patients fail to achieve successful revascularization or functional independence. ⁴ Prediction of successful revascularization using early markers may help to determine the optimal treatment strategy and potentially improve stroke treatment outcomes. ⁵ A growing body of evidence has suggested that imaging characteristics of the occlusive thrombi can provide valuable prognostic information. ⁶ For instance, imaging markers on non‐contrast computed tomography (CT) and CT angiography have been investigated in several studies to predict revascularization success or functional independence after stroke. ⁷ , ⁸ , ⁹ , ¹⁰ , ¹¹ , ¹² , ¹³ , ¹⁴ , ¹⁵ , ¹⁶ , ¹⁷ , ¹⁸ , ¹⁹ Commonly studied markers, including thrombus attenuation, length, burden, and perviousness (i.e., degree of contrast enhancement), have been associated with various outcome measures. ⁵ , ⁶ However, multiple studies have reported conflicting results, thus preventing any firm recommendations regarding the role of thrombus imaging in acute stroke treatment. A noteworthy thrombus imaging feature on MRI is called the susceptibility vessel sign (SVS), defined as a distinct loss of signal within the affected vessel and caused by a paramagnetic property of deoxygenated hemoglobin (deoxyhemoglobin) trapped in the clots. ²⁰ SVS is specifically well visualized on susceptibility weighted imaging (SWI) MRI, a sequence particularly sensitive to very small blood product compounds and calcium. ²⁰ Therefore, a higher component of red blood cells on a clot, termed red thrombi, results in a more hypointensity of SVS on the SWI sequence. ²¹ Thrombi with higher fibrin components are termed white thrombi. However, MRI is an unreliable modality to differentiate between these 2 clot types. ²¹ , ²² , ²³ The SVS sign on MRI has shown a higher sensitivity than the hyperdense vessel sign on CT‐based clot imaging, indicating the possible superiority of MR‐based clot imaging techniques compared with other modalities. ²⁴

This systematic review will focus on studies evaluating thrombus characteristics using MRI gradient‐recalled echo and SWI sequences. We performed a comprehensive systematic review to assess the published studies investigating the relationship between MR imaging characteristics of thrombi and radiological and clinical outcomes in ELVO.

Methods

Search Strategy

This systematic review complied with the guidelines of Preferred Reporting Item for Systematic Reviews and Meta‐Analysis, as summarized in the supplementary flow diagram (Figure S1). Data will be available upon reasonable request. We performed a systematic electronic search using PubMed, Ovid MEDLINE, EMBASE, previously published meta‐analyses, and systematic reviews with no language limitations. The search terms were “clot,” “thrombus,” “embolus,” “stroke,” “ischemic stroke,” “large vessel occlusion,” “mechanical thrombectomy,” “CT,” “MRI,” and “imaging,” using both “AND” and “OR” combinations.

Study Selection and Data Extraction

The types of studies included were original articles published in peer‐reviewed scientific journals. The target population was patients with ELVO managed by EVT or IVT therapies. ELVO was defined as acute occlusion of the vertebral, basilar, terminal carotid, middle, and anterior cerebral arteries as determined by MR angiography, CT angiography, or digital subtraction angiography. We excluded review articles, nonhuman studies, and studies with incorrect patient populations. Studies published between January 1, 2000, and March 1, 2023, were found and screened against the eligibility criteria that included studies with ≥10 enrollees with acute ischemic stroke due to ELVO managed by EVT and/or IVT, reported at least 1 imaging characteristic of thrombi using MR‐based techniques, and reported at least 1 of the revascularization outcome or functional outcome measures following stroke treatment. Two reviewers (H.S. and M.H.A.) independently screened titles and abstracts based on inclusion and exclusion criteria, and consensus resolved disagreements. Full‐text reports were reviewed after eliminating articles with target conditions different than stroke or those that do not assess at least a clot characteristic and an outcome measure. Subsequently, we performed a hand search of all included studies until no further relevant studies were identified. The data were independently extracted by H.S. and M.H.A. using a standardized protocol and data extraction form. We extracted study characteristics such as sample size, characteristics of imaging modalities, and patient characteristics such as baseline demographic and clinical characteristics. Among the eligible studies for the meta‐analysis, we selected papers with complete and available statistics regarding the association between SVS and either radiological outcome or functional outcome in subjects for whom mechanical thrombectomy with or without preceding thrombolysis was performed.

The methodological quality of the studies was rated using the Newcastle‐Ottawa quality assessment scale, a tool for quality assessment of nonrandomized studies. This instrument consists of 8 items within 3 domains: selection, comparability, and outcome/exposure. The total maximum score is 9, where 7–9 represents a high‐quality study with a low risk of bias, 4–6, moderate risk, and 0–3 high risk of bias ²⁵ (Supplementary Questionnaire).

Other Clot Features

Studies assessed the imaging characteristics of thrombi on MRI (presence or absence of SVS on gradient‐recalled echo or SWI, thrombus length, and clot burden score [CBS]) associated with the recovery from stroke. Thrombus length was measured on magnetic resonance angiography based on a delayed gadolinium‐enhanced T1‐weighted image, or SWI. Geometrical features of the clot also included the length and width of SVS on the SWI sequence of MRI. The CBS was another predictive parameter reported by the previous studies. The CBS is a 10‐point grading system of thrombus extent on CT angiography imaging for anterior circulation, in which a lower score reflects a more extensive involvement of vasculature by thrombi. A CBS of 10 is a normal score, implying the absence of a thrombus. There will be 2 score deductions from the total of 10 for occlusion of the supraclinoid portion of the internal carotid artery, proximal M1 middle cerebral artery, or distal M1 middle cerebral artery, whereas occlusion of infra clinoid portion of the internal carotid artery and right M2, left M2, or anterior cerebral artery each decline only 1 score from the total of 10. ²⁶

Functional and Radiological Outcomes

The association between radiologic thrombus characteristics and treatment efficacy (revascularization success) and functional outcomes were evaluated in this systematic review. Reperfusion status was classified based on the Thrombolysis In Myocardial Infarction score, Thrombolysis In Cerebral Infarction (TICI) score, or modified TICI (mTICI) score. Successful reperfusion was defined as Thrombolysis in Myocardial Infarction score ≥2 or TICI/mTICI score ≥2b. Functional outcomes included a modified Rankin scale on day 90 after stroke or early neurological deterioration at 24 hours after stroke. Early neurological deterioration was defined by at least an increase of 4 scores on the National Institutes of Health Stroke Scale within the first 24 hours after stroke compared with baseline. Favorable functional outcomes were defined as a modified Rankin scale score of 0–2 on day 90 after stroke.

Statistical Analysis

We reported baseline demographic and clinical characteristics using means, SD, medians, and interquartile ranges for continuous variables, and categorical variables were reported using frequencies.

Systematic review and meta‐analysis were done in compliance with the Cochrane Collaboration and the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses Statement. Meta‐analyses were performed by using the Review Manager (RevMan) Version 5.3. The Chi‐square test of heterogeneity and I² statistic of inconsistency were used to assess the heterogeneity between studies. I² values of 25%, 50%, and 75% were considered as low, moderate, and high heterogeneities, respectively. ²⁷ , ²⁸ A significant heterogeneity was considered if P<0.05 or I² statistics >50%. The pooled effect of the interventions was measured using odds ratio (OR) or standardized mean difference with a 95% CI. The small study effect, including publication bias, was tested using the visual estimation of funnel plot for asymmetry and Egger's regression test. ²⁹

Results

Study and Patient Characteristics

An electronic scientific literature search identified 2007 articles (Figure S1). After screening against the eligibility criteria, 33 studies were identified and reviewed. Characteristics of enrollees in studies that only involved thrombolysis as their intervention are summarized in Tables S1 and S2. The features of studies that involved EVT (with or without thrombolysis) are reported in Tables 1 and 2. The technical features of the MR‐based imaging that were used for thrombus evaluation are summarized in the supplementary Tables S3 and S4.

Table 1.

Baseline Characteristics of Studies That Intervened by Mechanical Thrombectomy With or Without Thrombolysis

Studies	Cases	Age, y Mean±SD/M (Q1, Q3)	Female sex (%)	Initial NIHSS Mean±SD/M (Q1, Q3)	Onset to groin puncture time (minute) Mean±SD/M (Q1, Q3)	Artery	Primary treatment modality	tPA patient no.	Device	Successful reperfusion
Weisstanner et al (2014) ⁴¹	88	66.5±16	53	13.5 (3–36)	250	M1, M2	MT or tPA+MT	28 (32%)	Stent retriever, aspiration, IA lysis	62 (70.5%)
Jindal et al (2014) ⁴²	28	58 (36–81)	51	18 (8–26)	NR	M1, ICA	MT or tPA+MT	24 (65%)	Solitaire, Trevo, Penumbra	23 (82%)
Fujimoto et al (2015) ⁴⁴	25	73±14	64	20±6	352 (230–480)	ICA terminus	MT or tPA+MT	NR	Merci, Penumbra, Solitaire	10 (40%)
Soize et al (2015) ³³	153	59±17	53	17.2±6.5	289±173	MCA, ICA, BA	MT or tPA+MT	84 (55%)	Solitaire	86 (56.2%)
Bourcier et al (2015) ³⁴	73	59 (25–85)	51	18 (2–27)	241.5	M1, ICA	MT or tPA+MT	40 (55%)	Stent retriever+manual aspiration	57 (78%)
Kim et al (2015) ³⁵	91	68.6±11.5	42	11.5±3.7	245	M1, M2	MT or tPA+MT	54 (59%)	Solitaire/aspiration	77 (84.6%)
Bourcier et al (2017) ^* , ³⁰	30	70±16	40	16 (2–27)	198 (60–349)	M1, ICA terminus	MT or tPA+MT	17 (57%)	Merci or Penumbra	27 (90%)
Ganeshan et al (2018) ^* , ⁴⁸	34	72 (66–85)	56	11 (4–18)	NR	MCA, ICA, vertebrobasilar	tPA or MT	21 (62%)	NA	NR
Kang et al (2017) ⁴³	89	68±13	47	15 (9–18)	354±198	M1, M2, ICA, ACA	MT or tPA+MT	35 (39%)	Stent retriever, aspiration	70 (78.6%)
Kim et al (2018) ⁶⁵	96	67.9±10.7	44.8	14 (1–24)	241.4±138.6	ICA, MCA	MT or tPA+MT	75(78.1)	Solitaire, Penumbra, Trevo	39 (40.6%)
Seners et al (2018) ³⁹	1107	70	49.3	16	NR	ICA terminus, M1, M2	tPA+MT	1107(100%)	NR	209 (18%)
Zhu et al (2018) ⁴⁶	231	69.3±14.7	46.3	18 (12–20)	219 (180–270)	M1, M2, ICA	MT or tPA+MT	NR	Stent retriever or contact aspiration	197 (85.3%)
Bourcier et al (2019) ³⁶	217	65	48	16	216	M1, M2, ICA	MT or tPA+MT	176 (81%)	Stent retriever, aspiration	175 (80.6%)
Darcourt (2019) ³¹	180	68.2±15.9	NR	17±6.3	NR	M1, M2, ICA terminus	MT or tPA+MT	118 (65.6%)	NR	137 (76.1%)
Derraz et al (2019) ³⁷	281	63	48	18	NR	ICA, M1	MT or tPA+MT	142 (50.5%)	Stent retriever	66 (23.4%)
Guenego et al (2018) ⁶⁶	912	67.5±15.3	48	16 (10–20)	255	M1, M2, ICAT, BA, Tandem	MT or tPA+MT	607 (66.6%)	Stent retriever±aspiration	728 (79.8%)
Seners et al (2020) ⁴⁰	218	72 (61–80)	45	16 (10–20)	160 (130–192)	M1, M2, ICA	tPA+MT	218 (100%)	NR	NR
Semerano et al (2021) ⁶⁷	11	47 (38–50)	55	16 (14–20)	NR	M1, M2, ICA	MT or tPA+MT	7 (64%)	NR	11 (100%)
Jing (2021) ⁴⁷	47	57.3±11.8	21.3	6 (3–11)	NR	M1, M2, ICA	MT or tPA+MT	16 (34%)	NR	31 (66%)
Darcourt et al (2021) ³²	210	71.83	NR	17.26	NR	M1, M2, ICA	MT or tPA+MT	115 (54.8%)	Contact aspiration alone or combined therapy with stent retriever	176 (83.8%)
Belachew et al (2021) ²⁰	577	74.2 (61.9–81.8)	51.3	12 (7–17)	235.0 (165.3–395.8)	M1, M2, M3, intracranial ICA, ACA, posterior circulation	MT or tPA+MT	225 (39%)	NR	479 (83%)
Guenego et al (2021) ⁴⁵	62	70 (57–77)	53	16 (12–21)	419 ^†	M1, M2, ICA, basilar	MT or tPA+MT	40 (65%)	Stent retriever, contact aspiration	55 (89%)
Dillmann et al (2022) ³⁸	221	69.2±16.4	54.3	17	NR	M1, M2, ICA, vertebrobasilar	MT	NR	Stent retriever	172/212 (81.1%)
de la Riva et al (2022) ⁶⁸	118	75.9±11.2	54.2	17 (11.5–21)	257.8±94.2 ^†	M1, ICA	MT or tPA+MT	29 (24.6%)	Stent retriever	111 (94.9%)

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ACA indicates anterior cerebral artery; BA, basilar artery; IA lysis, Intra Arterial Thrombolysis; ICA, internal carotid artery; MCA, middle cerebral artery; MT, mechanical thrombectomy; NIHSS, National Institutes of Health Stroke Scale; NR, not reported; and tPA, tissue plasminogen activator.

Data for patients post tPA and not post MT.

^{^†}

Onset to reperfusion was reported.

Table 2.

Outcome Summary for Studies That Intervened by Mechanical Thrombectomy With or Without Thrombolysis

Author (year)	Successful reperfusion	Reperfusion measure	Favorable functional outcome	Functional outcome measure	SVS+
Weisstanner (2014) ⁴¹	62 (70.5)	Final angio TICI 2b/3	40 (47.1)	mRS 0–2/90 d	84 (95.5%)
Jindal (2014) ⁴²	23(82%)	Final angio TICI 2b/3	14 (50%)	mRS 0–2/90 d	NR
Fujimoto (2015) ⁴⁴	10 (40%)	Final angio TICI 2b/3	NR	NR	NR
Soize (2015) ³³	86 (56.2%)	Final angio TICI 2b/3	82 (53%)	mRS 0–2/90 d	113 (74%)
Bourcier (2015) ³⁴	57 (78%)	Final angio TICI 2b/3	38/70 (54%)	mRS 0—2/90 d	53 (73%)
Kim (2015) ³⁵	77 (84.6%)	Final mTICI	49 (53.8%)	mRS 0–2/90 d	49 (54%)
Bourcier (2017) ³⁰ , ^*	27 (90%)	Early successful reperfusion as a TICI 2b/3 obtained with 2 or less attempts with NR stent retriever	NR	NR	17 (57%)
Ganeshan (2018) ⁴⁸ , ^*	NR	NR	36%	mRS 0—2/90 d	23 (68%)
Kang (2017) ⁴³	70 (78.6%)	Final angio TICI 2b/3	NR	NR	69 (78%)
Kim (2018) ⁶⁵	39 (40.6)	TICI 3	40 (100%)	mRS 0–1/90 d	NR
Seners (2018) ³⁹ , ^*	209 (18%)	mTICI 2b/3	NR	NR	851 (76%)
Zhu (2018) ⁴⁶	197 (85.3%)	mTICI 2b/3	116/223 (52%)	mRS 0–2/90 d	NR
Bourcier (2019) ³⁶	175 (80.6%)	mTICI 2b/3	121 (69%)	mRS 0–2/90 d	165 (76%)
Darcourt (2019) ³¹	147 (82%)	TICI 2b/3	NR	NIHSS at day 1	137 (76%)
Derraz (2019) ³⁷	66 (23.4%)	TICI 2b/3	144 (51%)	mRS 0–2/90 d	234 (83%)
Guenego (2018) ⁶⁶	728 (79.8%)	TICI 2b/3	496 (54.4)	mRS 0–2/90 d	NR
Seners (2020) ⁴⁰	34 (15.6%)	Early reperfusion ^†	NR	NR	198 (90.8%)
Semerano (2021) ⁶⁷	11 (100%)	mTICI 2b/3	10 (91%)	mRS 0–2/90 d	4/8 (50%) ^‡ , ^¶
Jing (2021) ⁴⁷	31 (66%)	ICA/MCA TIMI 2–3	23/46 (50%)	mRS 0–2/90 d	28 (59.6%)
Darcourt (2021) ³²	176 (83.8%)	mTICI 2b/3	NR	NR	175 (83.4%)
Belachew (2021) ²⁰	479 (83%)	TICI 2b/3	308 (53.4%)	mRS 0–2/90 d	505 (87.5%)
Guenego (2021) ⁴⁵	55 (89%)	TICI 2b/2c/3	28 (51%)	mRS 0–2/90 d	NR^¶
Dillmann (2022) ³⁸	172/212 (81.1%)	TICI 2b/3	74/182 (41%)	mRS 0–2/90 d	173 (78%)
de la Riva (2022) ⁶⁸	111 (94.9%)	mTICI 2b/3	50 (43.1%)	mRS 0–2/90 d	NR

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TIMI 0: complete occlusion, TIMI 1: severe stenosis, TIMI 2: mild or moderate stenosis, and TIMI 3: normal. TICI 0: no perfusion, TICI 1: minimal perfusion, TICI 2A: only partial filling, TICI 2B: complete filling but slower than normal, and TICI 3: complete perfusion. ICA indicates internal carotid artery; MCA, middle cerebral artery; mRS, modified Rankin scale; MT, mechanical thrombectomy; mTICI, modified Thrombolysis in Cerebral Infarction; NR, not reported; SVS, susceptibility vessel sign; TICI, Thrombolysis in Cerebral Infarction; TIMI, Thrombolysis in Myocardial Infarction; and tPA: tissue plasminogen activator.

Data for patients post‐tPA and not post‐MT.

^{^†}

Early reperfusion was defined as reperfusion within 3 hours after initiation of intravascular thrombolysis.

^{^‡}

Magnetic resonance imaging was not evaluable in 1 patient due to motion artifacts and in 2 patients due to a computed tomography scan performed in stroke acute phase; percentage refers to available data (n = 8).The study reported SVS, but it was not compared in respect to favorable outcome or reperfusion efficacy.

^{^¶}

SVS shape was reported, and only cases with positive SVS were included.

Thrombus Characteristics and Outcomes Following Treatment With EVT With or Without IVT

A total of 24 studies reported thrombus characteristics of 5267 participants, and 20 studies assessed the association between the MRI‐derived thrombus characteristics (SVS and other clot features) and reperfusion success or clinical outcome (Table 2). Eleven studies used stent retrievers, and 8 used aspiration techniques for thrombectomy (Table 1). Seventeen studies reported the presence of SVS in 2997 patients out of their total 3792 participants (79%) (Table 2). The association between the presence of SVS and reperfusion success or functional outcome measures is summarized in Tables 3 and 4.

Table 3.

Summary of Proportions of Favorable Treatment and Functional Outcomes Based on SVS Positivity Between Thrombus Characteristics and Outcome in Studies That Intervened by Mechanical Thrombectomy With or Without Thrombolysis

Study	Outcomes reported	SVS−	SVS+
Bourcier (2015) ³⁴	TICI 2B‐3	14/20 (70%)	43/53 (81%)
	mRS≤2 at 3 mo	5/20 (26%)	33/53 (65%)
Soize (2015) ³³	TICI 2B‐3	23/39 (58.9%)	63/114 (55.2%)
Kang (2017) ⁴³	TICI 2B‐3	14/20 (70%)	56/69 (81%)
Bourcier (2019) ³⁶	TICI 2B‐3	42/52 (80.8)	133/165 (80.6)
	mRS≤2 at 90 d	23/52 (44.2)	98/165 (59.4)
Darcourt (2019) ³¹	TICI 2B‐3	30/43 (69%)	117/137 (85%)
Jing (2021) ⁴⁷	mRS≤2 at 3 mo	10/19 (52.63%)	13/27 (48.1%)
Darcourt (2021) ³²	TICI 2B‐3	24/35 (68.6%)	152/175 (86.9%)
Belachew (2021) ²⁰	TICI 2B‐3	52/72	427/505 (84.5%)
	mRS≤2 at 3 mo	28/72 (38.9%)	280/505 (55.4%)
Dillmann (2022) ³⁸	TICI 2B‐3	36/43 (83.7%)	136/169 (80.4%)
	mRS≤2 at 3 mo	13/35 (37.1%)	61/147 (41.5%)

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mRS indicates modified Rankin scale; SVS, susceptibility vessel sign; and TICI, Thrombolysis in Cerebral Infarction.

Table 4.

The Association of Thrombus Characteristics With Reperfusion Efficacy and Outcome in Studies That Intervened by Mechanical Thrombectomy With or Without Thrombolysis

Studies	Radiological outcome (TICI>2b/mTICI>2b)	Functional outcome
Weisstanner (2014) ⁴¹ , ^*
SVS sign (+ versus −)	Successful reperfusion was achieved independent of thrombus length on SWI (OR: 0.92 [0.830–1.030]; P = 0.15)	NR
Jindal (2014) ⁴² , ^†
SVS sign (+ versus −)	NR	NR
Length	There was not a statistically significant association between thrombus length and final TICI score (P=0.48)	No statistically significant association between thrombus length and favorable mRS scores at 90 d was observed (P=0.41)
Fujimoto (2015) ⁴⁴ , ^‡
SVS sign (+ versus −)	NR	NR
Thrombus intensity	High FLAIR clot intensity (>0.7952) was associated with successful reperfusion (OR 16.79 [1.29–218.92]; P=0.031)	NR
Soize (2015) ³³ , ^†
SVS sign (+ versus −)	No statistically significant association was observed between the presence of SVS and reperfusion success (OR 1.24 [0.53–2.92]; P=0.84)	NR
Length	Nonrecanalizers demonstrated longer SVS length (20.1±9.0 mm) than recanalizers (15.±8.4 mm; P=0.0003)	NR
Bourcier (2015) ³⁴ , ^*
SVS sign (+ versus −)	No association between positivity of SVS on MRI and successful reperfusion was reported	Presence of SVS is associated with functional independence (OR: 8.7 [1.1–69.4])
Kim (2015) ³⁵ , ^*
SVS sign (+ versus −)	Presence of SVS was not associated with successful reperfusion	Presence of SVS was associated with higher rates of functional independence
Bourcier (2017) ³⁰ , ^*
SVS sign (+ versus −)	Presence of SVS was associated with successful early reperfusion versus late or no reperfusion (P=0.01)	NR
Other	T2 relaxation time was significantly shorter in early reperfusion	NR
Ganeshan (2018) ⁴⁸ , ^†
SVS sign (+ versus −)	NR	NR
Length	All patients with a thrombus length >5 mm on PC‐MRA presented a SVS on T2 ^* ‐weighted images	Thrombus length was associated with favorable functional outcome (mRS 0–2) (P=0.011)
Kang (2017) ⁴³ , ^¶
SVS sign (+ versus −) SVS length SVS diameter	Presence of SVS was associated with cardioembolic strokes, in particular SVS length (P = 0.01) and diameter (P<0.01). A larger SVS diameter was associated with reperfusion success (P=0.04), but they did not find an association between SVS volume and reperfusion success (P>0.05)	NR
Kim (2018) ⁶⁵ , ^*
SVS sign (+ versus −)	NR	NR
Other	DWI lesion volume was statistically significant associated with complete reperfusion (P<0.01) and shorter time interval from onset to reperfusion (P<0.01). In multivariate analysis, smaller initial DWI volume (OR: 1.78 [1.23–2.57]; P<0.01) and faster reperfusion time (OR: 1.07 [1.01–1.14]; P = 0.015) had an independent significance for complete reperfusion after mechanical thrombectomy	Complete reperfusion (mTICI 3) was associated with better functional outcomes (31 for mRS 0–1 vs 8 for mRS 2–6)
Seners (2018) ³⁹ , ^‡
SVS sign (+ versus −)	Early reperfusion was independent from presence of SVS (P = 0.90)	NR
Length	Longer SVS Length (>10 mm) was statistically significant associated with NO early reperfusion	NR
Zhu (2018) ⁴⁶ , ^*
CBS	A higher CBS more than 7 was not statistically significant associated with successful reperfusion following thrombectomy defined as mTICI 2b/3 (RR: 0.93, [0.73–1.18]; P: 0.54)	A higher CBS than 7 was statistically significant associated with both favorable outcome (mRS 0–2 at 90 day) (RR: 1.19 [1.02–1.40]; P = 0.028) and excellent outcome (mRS 0–1 at 90 day) (RR: 1.48 [1.24–1.77); P<0.001). CBS was not statistically significant associated with early recovery (NIHSS change at 24 h) (RR: 1.1 [−1.4 to 3.6]; P = 0.38)
Bourcier (2019) ³⁶ , ^*
SVS sign (+ versus −)	Presence of SVS was not associated with successful reperfusion	Presence of SVS was statistically significant associated with 90‐d mRS improvement (OR: 2.75 [1.44–5.26]) and favorable outcome (OR: 2.76 [1.18–6.45]). Early reduction in NIHSS within 24 h was not associated with presence of SVS (OR: −2.59 [−5.66 to 0.48]; P = 0.09)
Darcourt (2019) ³¹ , ^*
SVS sign (+ versus −)	Presence of SVS was associated with achievement of successful reperfusion (OR, 2.48 [1.05–5.74]; P=0.03)	Patients with presence of SVS had a higher level of early clinical improvement (NIHSS at day1) (median, −6; IQR, −11 to 0) compared with SVS‐negative patients (median, −1; IQR, −10 to 3)
Derraz (2019) ³⁷ , ^†
SVS sign (+ versus −)	There was no association between the presence of SVS and reperfusion result (P=0.45)	Primary outcome was not influenced by the presence of a SVS (P=0.98)
Length	NA	SVS length was associated with functional outcome
Other	CBS did not affect reperfusion result, considered as a continuous variable (P=0.75) or dichotomized (P=0.57)	A higher CBS was not statistically significant in whole population and for IVT+MT group whereas it was significantly associated for IVT group with achievement of a favorable outcome
Guenego (2018) ⁶⁶ , ^*
SVS sign (+ versus −)	NR	NR
Other	No difference in reperfusion in patients with or without extracranial GAD‐enhanced MRA (77% versus 81% for with GAD and without GAD). Multivariate analysis showed no significant difference between groups in groin puncture to clot contact time (RR=0.93 [0.85–1.02]; P=0.14), to reperfusion time (RR=0.92 [0.83–1.03]; P=0.15), or rates of successful reperfusion (defined as a mTICI 2b or 3 (OR=0.93 [0.62–1.42]; P = 0.74)	After adjustment, performing GAD‐enhanced extracranial MRA was not associated with good clinical outcome (OR=1.05 [0.73–1.52]; P=0.79)
Seners (2020) ⁴⁰ , ^†
SVS sign (+ versus −)	NR	NR
Length	Thrombus length was statistically significant smaller in those who had early reperfusion (P<0.01)	NR
Semerano (2021) ⁶⁷ , ^*
SVS sign (+ versus −)	NR	NR
Jing (2021) ⁴⁷ , ^*
SVS sign (+ versus −)	NR	Presence of SVS was not statistically significant correlated with the 90‐d mRS score of 0–2 (P = 0.76). Also, the clot SVS length was not statistically significant associated with the favorable outcome of 90‐d mRS 0–2
Darcourt (2021) ³² , ^*
SVS sign (+ versus −)	Presence of SVS was statistically significant associated with higher rates of successful reperfusion defined as mTICI 2B/3 (P = 0.007). Presence of SVS was not statistically significant associated with first pass reperfusion (P = 0.12)	NR
Belachew (2021) ²⁰ , ^*
SVS sign (+ versus −)	Successful reperfusion was defined as TICI 2B or 3 was statistically significant more frequently achieved in those with positive SVS (P = 0.009). First pass successful reperfusion was not statistically significant correlated with the presence of SVS (P =‐ 0.38)	Presence of SVS was statistically significant associated with a better functional outcome defined as 90‐d mRS 0–2 (P = 0.004)
Guenego (2021) ⁴⁵ , ^*
SVS sign (S‐shaped versus A‐shaped)	Successful reperfusion defined as 2b/2c/3 was not statistically significant correlated with the shape of SVS. S‐shaped: 26/27 (96%), A‐shaped: 29/35 (83%)	Favorable outcome of mRS 0–2 was not statistically significant different between patients with different SVS shapes (P = 0.49). S: shaped:14/25 (56%), A‐shaped: 4/30 (47%)
Dillmann (2022) ³⁸ , ^*
SVS sign (+ versus −)	Presence of SVS was not statistically significant associated with rate of achieving successful reperfusion following thrombectomy	90‐d mRS score of 0–2 as the favorable functional outcome was not statistically significant associated with presence of SVS (P = 0.64). Symptomatic intracranial hemorrhage at 24 h was not associated with presence of SVS (P = 0.69)
de la Riva (2022) ⁶⁸ , ^†
SVS sign (+ versus −)	NR	NR
CBS	NR	CBS was not found statistically significant associated with the risk of hemorrhagic transformation following endovascular thrombectomy (P = 0.77)
Length	NR	Thrombus size was not statistically significant correlated with hemorrhagic transformation (P = 0.67)

Open in a new tab

CBS indicates clot burden score; DWI, diffusion‐weighted imaging; FLAIR, fluid‐attenuated inversion recovery; GAD, gadolinium; IQR, interquartile range; IVT, intravascular thrombolysis; MRA, magnetic resonance angiography MRI, magnetic resonance imaging; MT, mechanical thrombectomy; mTICI, modified thrombolysis in cerebral infarction; NIHSS, National Institutes of Health Stroke Scale; NR, not reported; OR, odds ratio; PC, phase contrast; SVS, susceptibility vessel sign; SWI, susceptibility weighted imaging; and TICI, thrombolysis in cerebral infarction.

Length, thrombus intensity, and diameter characteristics were missed regarding their association with both radiologic and functional outcomes.

^{^†}

Thrombus intensity and diameter characteristics were missed regarding their association with both radiologic and functional outcomes.

^{^‡}

Length and diameter characteristics were missed regarding their association with both radiologic and functional outcomes.

^{^¶}

Thrombus intensity characteristics was missed regarding their association with both radiologic and functional outcomes.

Ten studies (2201 patients) assessed the association between the presence of SVS and successful reperfusion. Four studies (997 patients) found the presence of SVS associated with achieving successful reperfusion by EVT, ²⁰ , ³⁰ , ³¹ , ³² whereas 6 studies (1204 patients) found no association ³³ , ³⁴ , ³⁵ , ³⁶ , ³⁷ , ³⁸ (Table 4). Thrombus length was associated with reperfusion success in 3 studies (1476 patients), with a longer thrombus SVS associated with unsuccessful reperfusion. ³³ , ³⁹ , ⁴⁰ However, 2 studies (117 patients) found no association between reperfusion success and the thrombus length. ⁴¹ , ⁴² A larger SVS diameter and higher clot intensity were also reported in association with successful reperfusion by thrombectomy. ⁴³ , ⁴⁴ However, the shape of SVS, either an S‐shape or A‐shape, ⁴⁵ and the CBS were not associated with achieving successful reperfusion following thrombectomy ³⁷ , ⁴⁶ (Tables 2 and 4).

There were conflicting reports regarding the association between SVS positivity on MRI and functional recovery from stroke. Eight studies reported an association between SVS and favorable functional outcome or early neurological deterioration following EVT with or without preceding IVT. In 5 studies (1138 patients), the presence of SVS was associated with achieving a favorable outcome following EVT, ²⁰ , ³¹ , ³⁴ , ³⁵ , ³⁶ and 3 studies (717 patients) found no association between the presence of SVS and functional outcome after stroke. ³⁷ , ³⁸ , ⁴⁷ Two studies found a statistically significant association of functional outcome with SVS and thrombus length after thrombectomy, ³⁷ , ⁴⁸ whereas 2 others reported no association. ⁴² , ⁴⁷ The shape of SVS did not affect functional outcome at 90 days. ⁴⁵ Moreover, a higher CBS was associated with a favorable outcome ⁴⁶ (Tables 2 and 4).

Two studies with conflicting results assessed the association between SVS and early reperfusion (at <3 attempts). Another study found no association between SVS and first‐pass reperfusion.

Thrombus Characteristics and Outcomes in ELVO Strokes Treated With IVT Only

Of the 9 studies (1635 patients) that administered only IVT, 7 reported the presence of SVS in 534 patients out of their total 832 participants (64.2%). Six studies assessed the association between SVS and revascularization success or functional outcome (Table S5).

Five studies assessed the association between the presence of SVS and successful revascularization. Three studies (252 patients) found the presence of SVS associated with unsuccessful revascularization by IVT. ⁴⁹ , ⁵⁰ , ⁵¹ In comparison, 2 other studies (240 patients) reported no statistically significant difference in the revascularization rates based on the presence of SVS on MRI. ⁵² , ⁵³ The presence of SVS and characteristics of SVS, including SVS length and irregular SVS shape, were associated with unsuccessful revascularization following administration of tissue plasminogen activator. ⁵¹ , ⁵⁴ In contrast, SVS width was not associated with radiological and functional outcome. ⁵⁴ Thrombus length was reported in association with successful revascularization, ⁵⁵ while thrombus width was associated with unsuccessful revascularization. ⁵⁴ A higher CBS (ie, a smaller clot) was reported to be associated with successful revascularization and a more favorable outcome following thrombolysis ⁵² (Table S5).

SVS was associated with a worse functional outcome in 2 studies. ⁴⁹ , ⁵⁶ In contrast, another study (56 patients) reported no significant difference in outcome based on the presence of SVS. ⁵³ Three studies reported a significantly higher rate of poor functional outcome associated with a higher thrombus length ⁵⁵ , ⁵⁶ , ⁵⁷ (Table S5).

Meta‐Analysis

Pooled data from 8 studies, with a total number of 1711 subjects, showed a statistically significant overall association between presence of SVS and successful reperfusion after mechanical thrombectomy for ELVO stroke (OR: 1.57 [1.09–2.27]; P = 0.02; I² = 36%) (Figure A). No significant heterogeneity or evidence of publication bias were seen among studies (Supplemental Funnel Plot 1).

There was a statistically significant overall association between presence of SVS and achieving a favorable functional outcome after thrombectomy for ELVO strokes based on the pooled data from 5 studies consisting of 1095 subjects (OR: 1.76 [1.17–2.66]; P = 0.007; I² = 31%) (Figure B). No significant heterogeneity or evidence of publication bias were seen among studies (Supplemental Funnel Plot 2).

The risk of bias for the included studies in the meta‐analysis were determined to be low based on the Newcastle‐Ottawa quality assessment scale (Table S6).

Discussion

The SVS is an important clot feature on MRI associated with outcomes after stroke. In this comprehensive systematic review and meta‐analysis, we examined 33 studies that assessed MR‐based thrombus imaging characteristics associated with treatment response and functional outcome in patients with ELVO stroke treated by EVT or IVT. Of 8 studies (1711 patients), 3 (967 patients) favored a significant association between a positive SVS and successful reperfusion following EVT. Out of 5 studies that involved patients with stroke treated with EVT with or without IVT, 2 found a significant association between the presence of SVS on MRI and a favorable functional outcome. Our meta‐analysis showed a positive association between the presence of SVS on preintervention MRI and successful reperfusion and achieving a favorable functional outcome after EVT for ELVO strokes.

Our results were consistent with a previous systematic review and meta‐analysis that found a significant association between the presence of SVS and favorable functional outcome after stroke managed by thrombectomy, reported by 11 studies and a total number of 1619 participants. They also observed a higher rate of successful reperfusion by thrombectomy in the presence of SVS, even though that was not a statistically significant association. ⁵⁸ In another prior meta‐analysis of 1832 patients, they found significantly lower rates of revascularization and favorable functional outcome in association with the presence of SVS on preintervention MRI in IVT‐only treated studies. In contrast, SVS had a null association with radiological and functional outcomes in patients with stroke treated by EVT. ⁵⁹ However, our review found controversial arguments between different studies about the association between SVS and stroke outcomes where an IVT‐only strategy managed stroke. They also found an association between a smaller SVS length on MRI and successful revascularization. However, SVS width showed no association with revascularization success. ⁵⁹ The current study found the same associations of SVS length and width with revascularization success. In another analysis of 15 studies (896 patients) that used pretreatment MR‐based thrombus imaging, there was no association between SVS and successful revascularization after EVT or IVT. ⁶⁰ Compared with the aforementioned systematic reviews and meta‐analyses, the current review involved more studies and a larger population of patients. Also, our larger number of reviewed studies made it possible for us to evaluate a broader range of clot characteristics associated with stroke outcome, besides discussing the association between SVS and stroke outcome based on the treatment strategy.

The association between SVS positivity on MRI and successful revascularization by an IVT‐only strategy has been controversial among previous studies, where 3 reported a significant negative association. Two other studies found a null association between SVS and successful revascularization by an IVT‐only treatment strategy. Conflicting studies had a similar number of patients (252 versus 240) and baseline characteristics. This observation may represent that in the presence of SVS, associated with a red thrombus and a higher clot burden, an IVT‐only treatment strategy has a lower efficacy in successfully recanalizing the occluded vessels. Evidence is scarce on the association between SVS and functional recovery after stroke, managed by an IVT‐only strategy. Although 2 studies reported a significant association, another study reported no statistically significant difference in stroke outcome after thrombolysis based on the presence of SVS.

Prior literature suggests that a higher clot burden on initial stroke imaging is associated with a lower rate of favorable functional outcome after thrombectomy. Several studies reported a smaller SVS length (thrombus length) in association with a higher rate of successful reperfusion following EVT, whereas SVS shape was not associated with either reperfusion success or functional recovery. Also, a higher clot intensity on fluid‐attenuated inversion recovery and the diameter of the thrombus were associated with successful reperfusion following EVT. ⁴³ , ⁴⁴ On the other hand, previous CT‐based thrombus imaging studies had also found a higher CBS in association with higher rates of favorable functional outcome as well as successful revascularization following EVT with or without IVT ⁷ , ⁸ , ¹¹ , ¹³ or only IVT. ¹⁷ A longer thrombus length on CT images was significantly associated with a worse outcome and higher rates of complications after stroke. ¹⁹ Despite a large body of evidence on clot characteristics based on CT images, the association between MR‐based thrombus characteristics and stroke outcome is generally less well established. This can be explained by the lower general availability of MR imaging in practice before the treatment of ELVO strokes. However, MR imaging provides a higher resolution and accuracy in defining thrombus characteristics and vascular lesions besides a time‐critical identification of infarct lesions.

Major heterogeneity existed in prior MR‐based observational reports with respect to patients’ age, baseline stroke severity, rate of successful revascularization, bridging therapy by IVT, onset to treatment time, MR imaging sequences, and magnet strength used to evaluate the clot characteristics. The low sample size in most of the reviewed studies could have made the observed heterogeneity among them in terms of baselines. Therefore, future studies with larger sample sizes and a homogeneous collection of thrombus imaging features are suggested. Future studies should also consider other MR‐based clot imaging features like hyperintensity vessel sign, other clot radiomics features, and more accurate MR imaging techniques for assessing the clot characteristics (e.g., phase‐sequenced MRI). The other limitation of the current review is that some studies on the association between SVS and successful revascularization did not include a multivariate analysis. Another possible limitation of the conclusions we made regarding the predictive value of SVS for a favorable functional outcome is that such a correlation could be confounded by the fact that MRI is more sensitive to capture SVS in the absence of baseline comorbidities to stroke (e.g., cancer‐related stroke), that could have partially promoted a more favorable functional recovery to be achieved. ⁶¹ The presence of diabetes might also be associated with the absence of SVS, given its correlation with an atherosclerotic thrombi formation that appears as a negative SVS on MRI. ²⁰ , ⁶² , ⁶³ However, all studies in the current meta‐analysis that assess the association between SVS and favorable functional recovery had conclusions based on adjusted analyses for baseline characteristics. Moreover, artificial intelligence is revolutionizing research in different fields of medicine; previous studies implemented artificial intelligence to interpret thrombus characteristics in patients with ischemic stroke. ⁶⁴ Future studies with the aid of artificial intelligence to find the predictive combination of thrombus imaging features for successful revascularization and favorable functional outcome are suggested.

Source of Funding

None.

Disclosures

The authors of this study have no conflicting or competing interest in the subject matter of this manuscript.

Supporting information

Table S1‐S10

Figure S1

Funnel plot 1‐2

SVI2-4-e001142-s001.pdf^{(691KB, pdf)}

Acknowledgments

None.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Table S1‐S10

Figure S1

Funnel plot 1‐2

SVI2-4-e001142-s001.pdf^{(691KB, pdf)}

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PERMALINK

Association Between MR‐Based Thrombus Imaging Characteristics and Endovascular Therapy Outcome in Acute Ischemic Stroke: A Systematic Review and Meta‐Analysis

Mohammad Hossein Abbasi, MD, MPH

Adrienne N Dula, PhD

Steven J Warach, MD, PhD

Hamidreza Saber, MD, MPH

Abstract

Background

Methods

Results

Conclusion

Nonstandard Abbreviations and Acronyms

Clinical Perspective

Methods

Search Strategy

Study Selection and Data Extraction

Other Clot Features

Functional and Radiological Outcomes

Statistical Analysis

Results

Study and Patient Characteristics

Table 1.

Table 2.

Thrombus Characteristics and Outcomes Following Treatment With EVT With or Without IVT

Table 3.

Table 4.

Thrombus Characteristics and Outcomes in ELVO Strokes Treated With IVT Only

Meta‐Analysis

Figure .

Discussion

Source of Funding

Disclosures

Supporting information

Acknowledgments

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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