Background Thrombus characteristics, including Hounsfield unit (HU) value to measure density and thrombus volume and length, can predict successful recanalization following IV thrombolysis with recombinant tissue plasminogen activator. Conflicting and limited data exist regarding the value of assessing thrombus properties in acute stroke cases treated with endovascular IA approaches.
Methods We retrospectively reviewed cases of anterior circulation acute ischemic stroke in which a Solitaire stent retriever (ev3-Covidien) was the primary treatment device. We measured the following thrombus characteristics: absolute and corrected HU values; thrombus length and volume; clot burden score; and vessel bifurcation involvement. Fisher's exact test and the t test were used to study the association between these clot characteristics and successful recanalization (Thrombolysis in Cerebral Infarction (TICI) score 2b–3).
Results We identified 41 patients with anterior circulation stroke treated with the Solitaire stent retriever as the primary treatment device. Successful recanalization (TICI score 2b–3) was achieved in 59% of cases. Higher absolute and corrected HU values were strongly predictive of successful recanalization (49.9±7.6 vs 43.8±6.6, p=0.01 for absolute HU values and 1.2±0.2 vs 1.0±0.1, p=0.03 for HU ratio in TICI 2b–3 and TICI 0–2a groups, respectively). There was no significant difference between recanalization and non-recanalization groups in the other thrombus characteristics studied.
Conclusions In acute stroke treated with Solitaire stent retriever thrombectomy, higher thrombus HU values are predictive of successful recanalization. Such information can be used in decision making when estimating recanalization success rate with different endovascular treatment approaches.
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Several studies have demonstrated the prognostic value of thrombus characteristics in predicting revascularization with IV thrombolysis in acute ischemic stroke due to large vessel occlusion.1–3 Low clot density measured with Hounsfield unit (HU) values and longer thrombus length on admission non-contrast CT images indicate thrombi more resistant to IV thrombolysis and a lower chance of successful recanalization.1–3
Conflicting and limited data exist regarding the value of assessing thrombus properties in cases of acute stroke treated with endovascular IA approaches. Moftakhar et al3 demonstrated that thrombi with a lower density were more resistant to local IA thrombolysis with recombinant tissue plasminogen activator or thrombectomy with the Merci (Concentric Medical, Mountain View, California, USA) or Penumbra (Penumbra Inc, Alameda, California, USA) device. The presence of hyperdense thrombi predicted successful recanalization using the Merci device in a study by Froehler et al.4 Yet another study that included stroke cases treated primarily with the Penumbra aspiration system failed to show an association between thrombus density and recanalization.5 The goal of our study was to analyze the prognostic value of thrombus characteristics on the ability of the Solitaire stent retriever (ev3-Covidien, Irvine, California, USA) to achieve successful recanalization in stroke.
The study was approved by our local institutional review board. We retrospectively reviewed cases of patients with acute ischemic stroke treated by endovascular IA therapy between January 1, 2010 and July 30, 2013. We included cases where Solitaire stent retriever thrombectomy was the primary device strategy for the treatment of occlusion of the internal carotid artery terminus or M1 or proximal M2 segment of the middle cerebral artery. We excluded those cases in which the Solitaire stent retriever was used after other endovascular devices were applied first but failed to achieve successful recanalization. In cases where other devices were used following the Solitaire stent retriever, only the part of the angiogram related to Solitaire use was analyzed to assess recanalization results. No patients received IA recombinant tissue plasminogen activator prior to Solitaire thrombectomy.
All patients underwent 5 mm non-contrast head CT imaging performed using the Aquilion ONE scanner (Toshiba Medical Systems, Nasu, Japan) with the following parameters: tube voltage 125 kV; tube current 370 mA; and rotation speed 0.75 s. Cranial and cervical CT angiography was obtained by infusing an 80 mL bolus of 350 mg I/mL of contrast agent at a rate of 4 mL/s. CT angiography images were reconstructed at 0.5 mm thickness. All postprocessing was performed on a multimodality workstation (Vitrea 2; Vital Images, Minnetonka, Minnesota, USA).
Thrombus HU values were quantified as previously described.2 Briefly, using non-contrast CT scans, each section where the thrombus was seen was manually outlined to obtain the HU value; then the sum of the HU values was divided by the total number of sections. In each case, the contralateral HU values were collected to correct for variability in hematocrit levels. The HU ratio (rHU) was calculated by dividing the HU value of the affected side by the HU value of the contralateral side. We excluded regions with HU values >100, which represented calcifications.3 Thrombus volume was calculated based on the previously described formula.3 The clot burden score was calculated based on a previously described method.6 This score defines the extent of intracranial thrombus on CT angiography found in proximal anterior circulation strokes, using a scale of 0–10. Points are assigned for the presence of contrast opacification and are subtracted for the absence of contrast opacification. The Thrombolysis in Cerebral Infarction (TICI) grading scale7 was used to measure intracranial recanalization. Successful recanalization was defined as a TICI score of 2b–3. Times from stroke symptom onset to non-contrast CT scan and to recanalization were collected (for patients who did not achieve recanalization, it was the time of last attempted stent retriever thrombectomy).
Statistical analysis for each outcome variable was performed with SPSS software (V.19, IBM Software, Chicago, Illinois, USA). Analysis of variables was performed using Fisher's exact test for categorical data and a two tailed t test for continuous data. For all statistical analyses, p<0.05 was considered statistically significant.
Fifty-two patients with anterior circulation strokes were treated with the Solitaire stent retriever during the study period. Three cases were excluded because of the presence of severe calcification at the thrombus site, and eight cases were excluded because the Solitaire stent retriever approach was used as secondline or rescue therapy after other IA approaches had failed to achieve revascularization. Thus Solitaire stent retriever thrombectomy was used as a primary IA treatment in 41 cases, and these cases were used for the final analysis (some of these cases were included in a multicenter retrospective analysis8).
Of those 41 cases, successful recanalization, defined as a TICI score of 2b–3, was achieved with the stent retriever in 24 patients (59%). Demographic and clinical characteristics of the two recanalization outcome groups (final TICI 0–2a and TICI 2b–3) are shown in table 1. The two groups had no significant differences in terms of distribution of cerebrovascular risk factors, demographic data, or baseline National Institutes of Health Stroke Scale score.
The mean absolute thrombus HU values and rHU were significantly higher in patients in whom successful recanalization was achieved with the Solitaire stent retriever than in patients in whom successful recanalization was not achieved (49.9±7.6 vs 43.8±6.6, p=0.01, for absolute HU values and 1.2±0.2 vs 1.0±0.1, p=0.03, for rHU, respectively) (table 1). There was no significant difference between the two groups in other thrombus characteristics, such as thrombus volume, length, involvement of arterial bifurcations, or the clot burden score (table 1).
In our study, thrombus density, measured with HU values, was strongly predictive of successful recanalization with Solitaire stent retriever thrombectomy. To our knowledge, this is the first study that has examined the predictive value of thrombus characteristics for recanalization, specifically in patients treated with a stent retriever as a primary endovascular approach.
In contrast with our findings, in the study conducted by Spiotta et al,5 no association was found between thrombus density and likelihood of recanalization. However, in that study, the majority of cases were treated with the Penumbra aspiration system. The authors included some cases treated with first generation stent retrievers but did not specify the exact number of such cases.
The contradictory results might be explained by a difference in treatment approaches—maceration and aspiration of the thrombus with the Penumbra aspiration system versus entrapment and retrieval of the thrombus with a stent retriever. Froehler et al4 found that mechanical thrombectomy with the Merci device, which works by capturing and retrieving thrombus, is more successful in patients with hyperdense thrombi. Moftakhar et al3 reported an association between clot density and success with mechanical thrombectomy using the Merci and Penumbra devices but did not provide results for each device.
We did not find an association between recanalization and other thrombus characteristics, such as volume and length. A similar lack of association between the extent of thrombus and recanalization was seen in stroke cases treated with the Merci device and the Penumbra aspiration system.4 ,5 The clot burden score is calculated based on the length and location of thrombus in the anterior circulation stroke, and its value is predictive of successful recanalization in patients receiving IV thrombolysis.9 ,10 We found that the efficacy of the Solitaire stent retriever in achieving recanalization was not affected by the value of the clot burden score. Our study suggests that thrombus composition, rather than thrombus volume and extent, is a key determinant of successful recanalization. The proportion of fibrin, erythrocyte, and white blood cell content has been shown to affect thrombus density detected with non-contrast CT.11
Cases of calcifications within the target artery that were overlapping the thrombus (n=3, defined as HU value >100) were excluded from the main analysis because these lesions produce very bright artifact that interferes with accurate interpretation of clot density.3 ,5 In two of those cases, multiple stent retriever attempts were unsuccessful, and adjunct treatment with intracranial balloon angioplasty was required. In the third case, the Solitaire FR became entrapped inside the dense calcification after its deployment and had to be recaptured with a microcatheter.
There are some limitations in our study. First, due to the relatively small size of the ‘no recanalization’ group, a possibility of type II error should be considered when interpreting the results. Because our goal was to investigate the predictive value of clot characteristics specifically for Solitaire stent retriever thrombectomy, we excluded cases where the stent retriever was used as secondline or rescue IA therapy. Second, HU values were obtained from 5 mm thickness slices of non-contrast CT images. Thin slice reconstructions, which were not available for our retrospective study, have been shown to be more reliable in detecting thrombi of the proximal middle cerebral artery.12
Our study shows that thrombus density, measured on admission non-contrast CT images, can be used for predicting successful recanalization in anterior circulation stroke treated with the stent retriever thrombectomy approach. Such information can be used in decision making when estimating outcomes with different endovascular treatment approaches and might prove to be helpful as part of the selection criteria in future clinical trials of endovascular stroke therapies.
The authors thank Debra J Zimmer for editorial assistance.
Contributors Conception and design: MM, SM, KVS, and EIL. Analysis and interpretation of the data: MM, SM, and SKN. Drafting of the manuscript: MM. Acquisition of the data, critically revising the manuscript, and final approval of the manuscript: all authors.
Competing interests LNH receives grant/research support from Toshiba; serves as a consultant to Abbott, Boston Scientific, Cordis, Micrus, and Silk Road; holds financial interests in AccessClosure, Augmenix, Boston Scientific, Claret Medical, Endomation, Micrus, and Valor Medical; holds a board/trustee/officer position with Access Closure and Claret Medical; serves on Abbott Vascular's speakers’ bureau; and has received honoraria from Bard, Boston Scientific, Cleveland Clinic, Complete Conference Management, Cordis, Memorial Health Care System, and the Society for Cardiovascular Angiography and Interventions (SCAI). EIL receives research grant support, other research support (devices), and honoraria from Boston Scientific, and research support from Codman and Shurtleff Inc and ev3-Covidien Vascular Therapies; has ownership interests in Intratech Medical Ltd and Mynx/Access Closure; serves as a consultant on the board of Scientific Advisors to Codman and Shurtleff Inc; serves as a consultant per project and/or per hour for Codman and Shurtleff Inc, ev3-Covidien Vascular Therapies, and TheraSyn Sensors Inc; and receives fees for carotid stent training from Abbott Vascular and ev3-Covidien Vascular Therapies. EIL receives no consulting salary arrangements. All consulting is per project and/or per hour. MM has received an educational grant from Toshiba. AHS has received research grants from the National Institutes of Health (co-investigator: NINDS 1R01NS064592-01A1) and the University at Buffalo (Research Development Award) (neither is related to the present submission); holds financial interests in Hotspur, Intratech Medical, StimSox, Valor Medical, and Blockade Medical; serves as a consultant to Codman and Shurtleff Inc, Concentric Medical, Covidien Vascular Therapies, GuidePoint Global Consulting, Penumbra Inc, Stryker Neurovascular, and Pulsar Vascular; belongs to the speakers’ bureaus of Codman and Shurtleff Inc and Genentech; serves on National Steering Committees for Penumbra Inc 3D Separator Trial and Covidien SWIFT PRIME trial; serves on an advisory board for Codman and Shurtleff and Covidien Vascular Therapies; and has received honoraria from American Association of Neurological Surgeons’ courses, Annual Peripheral Angioplasty, and All That Jazz Course, Penumbra Inc, and from Abbott Vascular and Codman and Shurtleff Inc for training other neurointerventionists in carotid stenting and for training physicians in endovascular stenting for aneurysms. AHS receives no consulting salary arrangements. All consulting is per project and/or per hour. KVS serves as a consultant and a member of the speakers’ bureau for Toshiba and has received honoraria from Toshiba. He serves as a member of the speakers’ bureau for and has received honoraria from ev3 and the Stroke Group.
Ethics approval Ethics approval was obtained from the University at Buffalo Health Sciences institutional review board, project No 403427-3.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement Unpublished anonymized/de-identified data may be available. This would be on a per request basis.