- Departments of Clinical Neuroscience, Tokushima University, Tokushima, Japan,
- Neurosurgery, Tokushima University, Tokushima, Japan.
Correspondence Address:
Yuki Yamamoto, Department of Clinical Neuroscience, Tokushima University, Tokushima, Japan.
DOI:10.25259/SNI_1160_2021
Copyright: © 2022 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.How to cite this article: Yuki Yamamoto1, Nobuaki Yamamoto1, Yasuhisa Kanematsu2, Izumi Yamaguchi2, Manabu Ishihara2, Takeshi Miyamoto2, Shu Sogabe2, Kenji Shimada2, Yasushi Takagi2, Yuishin Izumi1. The claw sign predicts first-pass effect in mechanical thrombectomy for cerebral large vessel occlusion in the anterior circulation. 25-Feb-2022;13:72
How to cite this URL: Yuki Yamamoto1, Nobuaki Yamamoto1, Yasuhisa Kanematsu2, Izumi Yamaguchi2, Manabu Ishihara2, Takeshi Miyamoto2, Shu Sogabe2, Kenji Shimada2, Yasushi Takagi2, Yuishin Izumi1. The claw sign predicts first-pass effect in mechanical thrombectomy for cerebral large vessel occlusion in the anterior circulation. 25-Feb-2022;13:72. Available from: https://surgicalneurologyint.com/surgicalint-articles/11409/
Abstract
Background: Mechanical thrombectomy (MT) is an effective treatment for acute cerebral large vessel occlusion (LVO). Complete recanalization of vessels in a single procedure is defined as the first-pass effect (FPE) and is associated with good prognosis. In this study, angiographic clot protruding sign termed the “claw sign,” was examined as candidate preoperative imaging factor for predicting the FPE.
Methods: We retrospectively analyzed data from 91 consecutive patients treated for acute LVO in the anterior circulation by MT between January 2014 and December 2019. The claw sign was defined as a thrombus that protruded proximally by more than half of the diameter of the parent artery. Radiological findings such as claw sign, clinical and etiological features, and outcomes were compared between groups with and without successful FPE. Multivariate analysis was conducted to evaluate perioperative factors associated with FPE.
Results: FPE was achieved in 26 of 91 (28.6%) patients and the claw sign was observed in 34 of 91 (37.4%) patients. The claw sign was significantly more frequent in the successful FPE group than in the failed FPE group (53.8% vs. 30.8%; P = 0.040). After the multivariate analysis, the claw sign was the only pretreatment parameter that could predict FPE (odds ratio, 2.67; 95% confidence interval, 1.01–7.06; P = 0.047).
Conclusion: The claw sign is an angiographic imaging factor that might predict FPE after MT for anterior circulation acute ischemic stroke.
Keywords: Acute ischemic stroke, Angiography, Claw sign, First pass, Mechanical thrombectomy
INTRODUCTION
As a result of recent major clinical trials, mechanical thrombectomy (MT) has been established as the standard treatment in patients with acute intracranial large vessel occlusion (LVO).[
Zaidat et al. reported that FPE was more likely to be obtained in cases with balloon guide catheter use and noninternal carotid artery (ICA) occlusion.[
MATERIALS AND METHODS
Study design and data collection
We retrospectively examined 130 consecutive patients who underwent MT at our hospital from January 2014 to December 2019. During this period, 121 cases were treated for acute intracranial LVO in the ICA or proximal portion of the middle cerebral artery (MCA M1-2). After excluding patients with tandem occlusion and extensive infarction defined as Alberta Stroke Program Early Computed Tomography (CT) Score <6 on diffusion-weighted imaging, 91 patients were finally analyzed [
Diagnosis of acute cerebral LVO was performed using magnetic resonance imaging (MRI). MT was performed either alone or with intravenous recombinant tissue plasminogen activator (IV-TPA), depending on the adaption. According to our institutional protocol, patients with eligibility for IVTPA were administered this at a dose of 0.6 mg/kg within 4.5 h of onset.[
Susceptibility vessel sign (SVS), two-layered SVS (TL-SVS), and claw sign were selected as candidates for perioperative imaging factors that predict FPE. SVS was defined as a hypointense signal exceeding the size of the contralateral arterial diameter on MRI T2*-weighted image in a vessel cistern. TL-SVS was defined as SVS with a low-intensity core and higher intensity signal around the core.[
Figure 2:
Positive case of claw sign. A 91-year-old man with the right internal carotid artery (ICA) occlusion. (a) Angiography reveals proximal protrusion of the thrombus (white arrow) at the terminus of ICA. (b) After lesion passing through a microcatheter, stent retriever (black arrows) (Solitaire 2, Medtronic, Dublin, Ireland) is deployed. (c) After retrieving of stent, angiography shows complete recanalization of ICA.
Figure 3:
Angiograms with the claw sign. (a) A case of proximal middle cerebral artery occlusion. (b) The thrombus protrudes proximally by more than half of the diameter of vessel. (c) A case of middle cerebral artery M2 occlusion. (d) The thrombus protrudes proximally by more than half of the diameter of vessel.
Statistical analyses
Results are expressed as means ± standard deviations or as medians (minimum-maximum) for quantitative variables and as count and percentages for categorical variables. Univariate analyses were performed with the Mann– Whitney U-test for continuous or ordinal variables and the χ2 test for categorical variables. A one-way analysis of variance was used to compare the difference of variables among the three groups (the Bonferroni correction was used as post hoc analysis). All statistical tests were two sided, and the significance (P) level was set at 0.05. Multivariate analysis was performed including non-ICA terminus occlusion as a known FPE predictor and preoperative factors with P < 0.05 obtained by univariate analysis. All statistical analyses were performed with SPSS 26.0 (IBM, Armonk, New York).
RESULTS
Basic characteristics and clinical outcomes
We included and analyzed data from 91 consecutive patients (50 females; mean age: 75.6 ± 11.0 years). The baseline characteristics of patients are summarized in
Procedural outcomes significantly demonstrated a smaller number of passes (median, 1 vs. 2; P < 0.01) and shorter puncture to reperfusion time (33 min vs. 76 min; P < 0.01) in the FPE group. Clinical outcomes showed a lower NIHSS at discharge (median, 0 vs. 8; P < 0.01) and a better mRS score at 90 days after onset (mRS 0–1, 57.7% vs. 29.2%; P = 0.11) in the FPE group [
Predictors of FPE
The multivariate analysis included non-ICA terminus occlusion as a known FPE predictor and the preoperative factors (presence of claw sign, female sex, and not smoking) for which there were significant differences identified in the univariate analysis [
DISCUSSION
In this study, we selected SVS, TL-SVS, and claw sign as imaging candidates to predict FPE after MT for anterior circulation acute ischemic stroke. Univariate analysis showed that female sex, not smoking, and the presence of claw sign were significantly more frequently seen in the successful FPE group. From multivariate analysis in which nonICA occlusion was added to these three factors, claw sign emerged as an independent predictor of FPE with an odds ratio of 2.67.
In recent years, several studies have described the morphological characteristics of clots observed on angiography during MT[
Consoli et al. classified the morphological phenotype of the occlusion site in the M1 segment of the MCA into regular and irregular.[
Yamamoto et al. investigated 73 patients who underwent MT for ICA, MCA M1-2, and VA-BA occlusion and found claw sign in 29 patients (40.0%). It was also reported that infarction with an embolic mechanism was more frequent (93.1% vs. 72.7%) in the claw sign-positive group than in the -negative group.[
SVS is a hypointense signal exceeding the diameter of the contralateral artery on MRI T2*-gradient echo imaging sequences.[
There are some potential limitations of this study. First, this study was performed in a single center and followed a retrospective design. Further investigations are needed with a larger sample size to validate our results. The procedure technique and the devices were not unified in advance and were left to the operator. Finally, in some cases, the proximal end of the thrombus might not be accurately evaluated due to tortuous nature of the vessels or inadequate contrast injection.
CONCLUSION
The claw sign is an angiographic imaging factor that predicts FPE after MT for anterior circulation acute ischemic stroke. Angiographical clot protruding features at the occlusion site can predict treatment outcomes and stroke subtypes and may be useful in the future for procedure and device selection.
Ethics approval and consent to participate
The study protocol was approved by the local research ethics committee and consent for publication was obtained from all participants.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
1. Al Kasab S, Almadidy Z, Spiotta AM, Turk AS, Chaudry MI, Hungerford JP. Endovascular treatment for AIS with underlying ICAD. J Neurointerv Surg. 2017. 9: 948-51
2. Bai X, Zhang X, Yang W, Zhang Y, Wang T, Xu R. Influence of first-pass effect on recanalization outcomes in the era of mechanical thrombectomy: A systemic review and meta-analysis. Neuroradiology. 2021. 63: 795-807
3. Baik SH, Jung C, Kim BM, Han K, Kim DJ. Clot meniscus sign: An angiographic clue for choosing between stent retriever and contact aspiration in acute basilar artery occlusion. AJNR Am J Neuroradiol. 2021. 42: 732-7
4. Baik SH, Kim JW, Kim BM, Kim DJ. Significance of angiographic clot meniscus sign in mechanical thrombectomy of basilar artery stroke. J Neurointerv Surg. 2020. 12: 477-82
5. Bourcier R, Derraz I, Bracard S, Oppenheim C, Naggara O. Two-layered susceptibility vessel sign and high overestimation ratio on MRI are predictive of cardioembolic stroke. AJNR Am J Neuroradiol. 2019. 40: 65-7
6. Bourcier R, Hassen WB, Soize S, Roux P, Labreuche J, Kyheng M. Susceptibility vessel sign on MRI predicts better clinical outcome in patients with anterior circulation acute stroke treated with stent retriever as first-line strategy. J Neurointerv Surg. 2019. 11: 328-33
7. Consoli A, Rosi A, Coskun O, Nappini S, di Maria F, Renieri L. Thrombectomy for M1-middle cerebral artery occlusion: Angiographic aspect of the arterial occlusion and recanalization: A preliminary observation. Stroke. 2018. 49: 1286-9
8. Darcourt J, Withayasuk P, Vukasinovic I, Michelozzi C, Bellanger G, Guenego A. Predictive value of susceptibility vessel sign for arterial recanalization and clinical improvement in ischemic stroke. Stroke. 2019. 50: 512-5
9. Dargazanli C, Fahed R, Blanc R, Gory B, Labreuche J, Duhamel A. Modified thrombolysis in cerebral infarction 2C/thrombolysis in cerebral infarction 3 reperfusion should be the aim of mechanical thrombectomy: Insights from the ASTER trial (contact aspiration versus stent retriever for successful revascularization). Stroke. 2018. 49: 1189-96
10. Di Maria F, Kyheng M, Consoli A, Desilles JP, Gory B, Richard S. Identifying the predictors of first-pass effect and its influence on clinical outcome in the setting of endovascular thrombectomy for acute ischemic stroke: Results from a multicentric prospective registry. Int J Stroke. 2021. 16: 20-8
11. Garcia-Bermejo P, Patro SN, Ahmed AZ, Al Rumaihi G, Akhtar N, Kamran S. Baseline occlusion angiographic appearance on mechanical thrombectomy suggests underlying etiology and outcome. Front Neurol. 2019. 10: 499
12. Goyal M, Menon BK, van Zwam WH, Dippel DW, Mitchell PJ, Demchuk AM. Endovascular thrombectomy after large-vessel ischaemic stroke: A meta-analysis of individual patient data from five randomised trials. Lancet. 2016. 387: 1723-31
13. Hacke W, Kaste M, Fieschi C, von Kummer R, Davalos A, Meier D. Randomised double-blind placebo-controlled trial of thrombolytic therapy with intravenous alteplase in acute ischaemic stroke (ECASS II). Second European-Australasian acute stroke study investigators. Lancet. 1998. 352: 1245-51
14. Kang DH, Kim YW, Hwang YH, Park SP, Kim YS, Baik SK. Instant reocclusion following mechanical thrombectomy of in situ thromboocclusion and the role of low-dose intra-arterial tirofiban. Cerebrovasc Dis. 2014. 37: 350-5
15. Kang DW, Jeong HG, Kim DY, Yang W, Lee SH. Prediction of stroke subtype and recanalization using susceptibility vessel sign on susceptibility-weighted magnetic resonance imaging. Stroke. 2017. 48: 1554-9
16. Liang W, Wang Y, Du Z, Mang J, Wang J. Intraprocedural angiographic signs observed during endovascular thrombectomy in patients with acute ischemic stroke: A systematic review. Neurology. 2021. 96: 1080-90
17. Liebeskind DS, Sanossian N, Yong WH, Starkman S, Tsang MP, Moya AL. CT and MRI early vessel signs reflect clot composition in acute stroke. Stroke. 2011. 42: 1237-43
18. Maus V, Behme D, Kabbasch C, Borggrefe J, Tsogkas I, Nikoubashman O. Maximizing first-pass complete reperfusion with SAVE. Clin Neuroradiol. 2018. 28: 327-38
19. Mönch S, Boeckh-Behrens T, Berndt M, Maegerlein C, Wunderlich S, Zimmer C. Angiographic baseline proximal thrombus appearance of M1/M2 occlusions in mechanical thrombectomy. Clin Neuroradiol. 2021. 31: 189-96
20. Soize S, Batista AL, Regent CR, Trystram D, Tisserand M, Turc G. Susceptibility vessel sign on T2* magnetic resonance imaging and recanalization results of mechanical thrombectomy with stent retrievers: A multicentre cohort study. Eur J Neurol. 2015. 22: 967-72
21. Tomasello A, Ribò M, Gramegna LL, Melendez F, Rosati S, Moreu M. Procedural approaches and angiographic signs predicting first-pass recanalization in patients treated with mechanical thrombectomy for acute ischaemic stroke. Int Neuroradiol. 2019. 25: 491-6
22. Yamaguchi T, Mori E, Minematsu K, Nakagawara J, Hashi K, Saito I. Alteplase at 0.6 mg/kg for acute ischemic stroke within 3 hours of onset: Japan alteplase clinical trial (J-ACT). Stroke. 2006. 37: 1810-5
23. Yamamoto N, Satomi J, Tada Y, Harada M, Izumi Y, Nagahiro S. Two-layered susceptibility vessel sign on 3-tesla T2*-weighted imaging is a predictive biomarker of stroke subtype. Stroke. 2015. 46: 269-71
24. Yamamoto Y, Yamamoto N, Kanematsu Y, Korai M, Shimada K, Izumi Y. The claw sign: An angiographic predictor of recanalization after mechanical thrombectomy for cerebral large vessel occlusion. J Stroke Cerebrovasc Dis. 2019. 28: 1555-60
25. Zaidat OO, Castonguay AC, Linfante I, Gupta R, Martin CO, Holloway WE. First pass effect: A new measure for stroke thrombectomy devices. Stroke. 2018. 49: 660-6