Abstract
Background
Mechanical thrombectomy has become the standard care for acute ischemic stroke caused by large vessel occlusion. However, complete reperfusion cannot be achieved in all cases, and several factors influencing the results of mechanical thrombectomy have been investigated. Among others, a tortuous anatomy is associated with lower rates of complete reperfusion. We aimed to investigate whether an early division of the middle cerebral artery has an impact on reperfusion results in mechanical thrombectomy.
Methods
Retrospective review of consecutive patients with M1 occlusion treated endovascularly between January 2016 and December 2019 at three tertiary care centers. The study group was dichotomized based on the length of the M1 segment. Early division of the middle cerebral artery was defined as a maximum length of 10 mm of the M1 segment. Primary endpoints were first-pass mTICI scores of 3, ≥2c, and ≥2b. Secondary endpoints contained final reperfusion, number of device-passes, time interval from groin puncture to reperfusion, rate of postinterventional symptomatic intracranial hemorrhage, and frequency of emboli of new territory.
Results
Among 284 included patients, 70 presented with an early division of the M1 segment (25%). Reperfusion results did not differ significantly between early and late division of M1. A higher rate of symptomatic intracranial hemorrhage was found in the group with an early M1 division treated with aspiration only (14.3% vs. 0%; p = 0.013). Patients with late M1 division had a significantly higher rate of large artery sclerosis (19.2% vs. 8.6%, p = 0.039).
Conclusion
The anatomic variant of an early division of the middle cerebral artery was not a predictor for incomplete reperfusion.
Keywords: Acute ischemic stroke, early bifurcation, mechanical thrombectomy, middle cerebral artery, m1 occlusion
Background
Mechanical thrombectomy (MT) is the standard treatment for patients suffering from acute ischemic stroke (AIS) due to intracranial large vessel occlusion in the anterior circulation since large randomized controlled trials showed high recanalization rates and substantially improved clinical outcome compared to standard medical care.1
Previous studies have revealed several risk factors for incomplete reperfusion including thrombus length and volume and histopathologic characteristics such as a fibrin-rich clot and pre-existing atherosclerotic stenosis.2,3 Moreover, few studies indicated that successful recanalization is less likely in patients with tortuous vessels in the anterior circulation.4,5 In addition, recent studies evaluated the value of the dominancy of middle cerebral artery (MCA) branches. M2 occlusions seemed most likely to be located in the dominant branch, and successful reperfusion in distal M1 occlusions was associated with placement within the dominant M2 trunk.6,7 However, the association of vessel geometry and recanalization rates has not yet been fully elucidated.5,8 This study aims to analyze whether an early division of MCA has an impact on angiographic results in MT.
Methods
We conducted a retrospective analysis of patients, who were treated with MT for AIS caused by occlusion of the MCA (M1 segment) at three tertiary care centers in Germany between January 2016 and December 2019. Baseline parameters, anatomic specifics of the MCA, angiographic features, technical, and clinical outcome were retrieved from patient charts and angiographic images. There were no specific exclusion criteria. In particular, there were no limitations regarding the technical approach, which includes the use of different thrombectomy techniques and intra-arterial thrombolysis, which were left to the attending neuroradiologist’s discretion. Endovascular treatment was performed with approved MT devices, using either stent-retrievers or large-bore aspiration catheters.
The length of the M1 segment was evaluated by experienced neuroradiologists based on standard anteroposterior view images on the final angiograms (Figure 1). The study group was dichotomized based on the length of the M1 segment into early and late division of the MCA, whereby a maximum length of the M1 segment of 10 mm was defined as early division.9 Division of the M1 segment in superior/inferior trunk and the anatomic variant of an MCA trifurcation (trifurcate into superior, middle, and inferior divisions) were analyzed. In case of final mTICI 0 or 1, the pre-interventional non-enhanced cranial computed tomography (NECT) images were reviewed instead. Primary study endpoints were first pass complete, near complete, and successful reperfusion, defined as mTICI scale scores of 3, 2c, and 2b.10 Secondary endpoints contained final reperfusion (mTICI ≥ 2b, mTICI ≥ 2c, and mTICI 3), number of device-passes, time interval from groin puncture to reperfusion, rate of postinterventional symptomatic intracranial hemorrhage (sICH), and frequency of emboli in new territory (ENT).
Figure 1.
Schematics of the vessel anatomy of the middle cerebral artery are shown with an early (a) and late (b) division of the M1 segment.
Embolization in new territory was defined as emboli observed on postthrombectomy angiography within previously unaffected territories. Clinical outcome was determined by the rate of favorable outcome measured by the modified Rankin Scale (mRS) and defined as 0–2 at discharge and 90 days. NECT was performed within 24 h after MT or in case of clinical deterioration. sICH was graded after the ECASS criteria.11 The etiology of the occlusion was based on the TOAST classification.12 All National Institutes of Health stroke scale (NIHSS) and mRS grades were assessed by a consultant neurologist. According to the guidelines of the respective local ethics committees, ethical approval was given when necessary for this anonymous retrospective study, which was conducted in accordance to the Declaration of Helsinki. A patient’s consent for treatment was obtained according to the individual institutional guidelines. Due to the retrospective nature of the study, additional informed consent was waived.
Statistical analysis
Qualitative variables are presented as numbers and percentages, and groups were compared using the Chi-Square or the Fisher exact test. Quantitative variables are presented as mean ± standard deviation, and normal distribution was assessed by the Shapiro–Wilk test. Groups were compared with the Mann–Whitney U test or the unpaired Student’s t-test, as appropriate. All computations were performed using SPSS software (IBM SPSS Statistics for Windows, Version 25.0, Armonk, NY, USA). A p-value < 0.05 was regarded as statistically significant. To adjust for potential confounders, a multiple logistic regression analysis was performed that included variables which were significantly different (p < 0.1) between the two study groups.
Results
In total, 284 patients from three tertiary stroke centers were included in the study. Median age was 78 years (interquartile range (IQR) 67–84 years) and 38% (107/284) patients were male. Median NIHSS at baseline was 15 (IQR 9–18). Median baseline ASPECTS was 9 (IQR 7–10) and 26% (73/284) patients were presented as wake-up strokes. Out of 284 patients, 198 (70%) were treated with a combined technical approach (stent-retriever and aspiration MT) and 86 (30%) patients were treated with aspiration only (“A Direct Aspiration first Pass Technique,” ADAPT). Concomitant intravenous thrombolysis was administered to 52% (149/284) of patients according to the national neurological guidelines by the attending neurologist. Early division of the M1 segment was found in 25% (70/284) of patients (Figure 2), and the proportion of patients with a trifurcation of the MCA was 4% (12/284). The mean length of the M1 segment with an early division was 8.4 mm compared to 16.7 mm with a late division.
Figure 2.
Anteroposterior angiograms pre- (a + c) and postprocedural (b + d) of patients with a proximal M1 occlusion. In patient 1 late bifurcation of the M1 segment (b) is shown with complete reperfusion (mTICI 3). Patient 2 was presented with early bifurcation of the M1 segment (d), and near complete reperfusion (mTICI 2c) was achieved.
Baseline data showed no significant differences between the early and late MCA division besides stroke etiology, as detailed in Table 1. The group with late MCA division had a significantly higher rate of large artery sclerosis (19.2% vs. 8.6%, p = 0.039).
Table 1.
Baseline characteristics.
| Early MCA division (n = 70) | Late MCA division (n = 214) | p-Value | |
|---|---|---|---|
| Age (years), mean ± SD | 74.8 ± 13.9 | 74.8 ± 13.3 | 0.990 |
| Sex (male) | 26 (37.1%) | 81 (37.9%) | 0.916 |
| Baseline NIHSS, mean ± SD | 13.9 ± 6.7 | 13.9 ± 5.9 | 0.944 |
| Baseline ASPECTS, mean ± SD | 8.2 ± 1.6 | 8.4 ± 1.5 | 0.545 |
| mRS pre-treatment ≤2 | 63 (90%) | 187 (87.4%) | 0.558 |
| Wake-up stroke | 23 (32.9%) | 50 (23.4%) | 0.115 |
| Onset to groin (min), mean ± SD | 143.7 ± 147.2 | 145.9 ± 153.4 | 0.917 |
| Length of M1 segment (mm) | 8.4 ± 1.6 | 16.7 ± 4.7 | <0.001 |
| IVT | 35 (50%) | 114 (53.3%) | 0.634 |
| Tandem occlusion or stenosis | 4 (5.7%) | 32 (15%) | 0.060 |
| General anesthesia | 44 (62.9%) | 124 (57.9%) | 0.468 |
| Arterial hypertension | 53 (75.7%) | 171 (79.9%) | 0.456 |
| Atrial fibrillation | 36 (51.4%) | 100 (46.7%) | 0.494 |
| Diabetes | 21 (30%) | 62 (29%) | 0.870 |
| TOAST classification | |||
| Large artery sclerosis | 6 (8.6%) | 41 (19.2%) | 0.039 |
| Cardioembolic | 38 (54.3%) | 96 (44.9%) | 0.170 |
| Small-vessel occlusion | 1 (1.4%) | 2 (0.9%) | 0.726 |
| Other | 14 (20%) | 38 (17.8%) | 0.674 |
| Undetermined | 11 (15.7%) | 37 (17.3%) | 0.760 |
| Mechanical thrombectomy | |||
| Combined approach | 49 (70%) | 149 (69.6%) | 0.953 |
| Aspiration only | 21 (30%) | 65 (30.4%) | 0.953 |
| Balloon guide use | 3 (4.3%) | 9 (4.2%) | 0.99 |
ASPECTS: Alberta stroke program early CT score; IVT: intravenous thrombolysis; MCA: middle cerebral artery; mRS: modified Rankin Scale; NIHSS: National Institutes of Health stroke scale; SD: standard deviation.Bold values are regarded as statistically significant.
Angiographic results with early versus late M1 division
First-pass and final reperfusion results did not differ significantly between the two groups (Table 2). First-pass complete reperfusion was reached in 25/70 (35.7%) patients with an early M1 division and in 77/214 (36%) patients with a late M1 division (p = 0.968). The rate of first-pass near-complete reperfusion was 37/70 (52.9%) in the early division group vs. 99/214 (46.3%) in the late division group (p = 0.338). First-pass successful reperfusion was achieved in 50/70 (71.4%) in the early division group vs. 156/214 (72.9%) in the late division group (p = 0.811). Overall rates of reperfusion were as follows: mTICI 3 was achieved in 34/70 (48.6%) in the early division group vs. 106/214 (49.5%) in the late division group (p = 0.889); mTICI ≥ 2c was achieved in 50/70 (71.4%) in the early division group vs. 146/214 (68.2%) in the late division group (p = 0.615). Successful reperfusion (mTICI ≥ 2b) was reached in 65/70 (92.9%) in the early division group vs. 195/214 (91.1%) in the late division group (p = 0.650). Mean number of attempts and mean groin to reperfusion time were equivalent between the two groups (p = 0.747 and p = 0.171, respectively). A higher rate of sICH was confirmed in the group with an early M1 division, but without statistical significance (p = 0.102). Out of 70 patients with an early M1 division, 5 (7.1%) suffered from sICH compared to 6/214 (2.8%) patients with late M1 division. The rate of ENT was 1/70 (1.4%) in the early M1 division group and 3/214 (1.4%) in the late M1 division group (p = 1.0). There was a trend for a favorable outcome at discharge in the group with a late M1 division (50% vs. 37.1%; p = 0.061). Favorable outcome at 90 days did not differ significantly between the two groups (p = 0.766).
Table 2.
Angiographic and clinical outcomes.
| Early MCA division (n = 70) | Late MCA division (n = 214) | p-Value | |
|---|---|---|---|
| Primary outcome | |||
| First-pass reperfusion | |||
| mTICI 3 | 25 (35.7%) | 77 (36%) | 0.968 |
| mTICI ≥2c | 37 (52.9%) | 99 (46.3%) | 0.338 |
| mTICI ≥2b | 50 (71.4%) | 156 (72.9%) | 0.811 |
| Secondary outcome | |||
| Final reperfusion | |||
| mTICI 3 | 34 (48.6%) | 106 (49.5%) | 0.889 |
| mTICI ≥2c | 50 (71.4%) | 146 (68.2%) | 0.615 |
| mTICI ≥2b | 65 (92.9%) | 195 (91.1%) | 0.650 |
| Number of passes, mean ± SD | 1.8 ± 1.3 | 1.7 ± 1.1 | 0.747 |
| Groin puncture – reperfusion (min), mean ± SD | 43.1 ± 32.5 | 49.3 ± 33.2 | 0.171 |
| sICH | 5 (7.1%) | 6 (2.8%) | 0.102 |
| ENT | 1 (1.4%) | 3 (1.4%) | 1.0 |
| Clinical outcome | |||
| mRS score ≤ 2 at discharge | 26 (37.1%) | 107 (50%) | 0.061 |
| mRS score ≤ 2 at 90 days | 17/42 (40.5%) | 59/137 (43.1%) | 0.766 |
ENT: emboli to new territory; MCA: middle cerebral artery; mRS: modified Rankin Scale; mTICI: modified thrombolysis in cerebral infarction; SD: standard deviation; sICH: symptomatic intracranial hemorrhage.
Subgroup analysis
Subgroup analyses were performed in order to evaluate the effects of an early/late MCA division on thrombectomy techniques. In patients with aspiration-only technique, the early M1 division group showed a significantly higher rate of sICH (14.3% vs. 0%, p = 0.013) compared to the late M1 division group (Table 3). Out of three cases with sICH in the early M1 division group, in two patients, postinterventional parenchymal hemorrhage (ECASS PH 1) within the infarct was observed. In one patient, periinterventional subarachnoid hemorrhage due to perforation of the distal M1 was confirmed. Favorable outcome at discharge was significantly higher in the late M1 division group with 37/65 (56.9%) vs. 6/21 (28.6%) in the early M1 division group (p = 0.024). There was no difference between the groups regarding favorable outcome at 90 days (p = 0.926). In patients with combined thrombectomy approach, angiographic and clinical outcome did not differ significantly between the two groups (Supplement online Table 4).
Table 3.
Angiographic and clinical outcomes with aspiration technique.
| Early MCA division (n = 21) | Late MCA division (n = 65) | p-Value | |
|---|---|---|---|
| First-pass reperfusion | |||
| mTICI 3 | 7 (33.3%) | 24 (36.9%) | 0.766 |
| mTICI ≥ 2c | 11 (52.4%) | 33 (50.8%) | 0.898 |
| mTICI ≥ 2b | 12 (57.1%) | 42 (64.6%) | 0.538 |
| ICH | 3 (14.3%) | 0 (0%) | 0.013 |
| NT | 0 (0%) | 1 (1.5%) | 1.0 |
| Clinical outcome | |||
| mRS score ≤2 at discharge | 6 (28.6%) | 37 (56.9%) | 0.024 |
| mRS score ≤2 at 90 days | 5/11 (45.5%) | 16/34 (47.1%) | 0.926 |
ENT: emboli to new territory; MCA: middle cerebral artery; mRS: modified Rankin Scale; mTICI: modified thrombolysis in cerebral infarction; sICH: symptomatic intracranial hemorrhage.Bold values are regarded as statistically significant.
After adjusting for large artery sclerosis and tandem occlusion, there was still a significant difference between the two groups treated with aspiration technique regarding good outcome at discharge (mRS ≤ 2: early M1 division: 6/21 (28.6%) vs. late M1 division: 37/65 (56.9%), p = 0.036, OR 0.3; 95% CI 0.1–0.9). In the adjusted analysis, there were no significant differences between the two groups regarding sICH.
Discussion
Our study aimed to evaluate whether an early division of the MCA has an impact on angiographic and clinical outcome. In the primary analysis, no significant difference in first pass or final reperfusion between patients with early and late M1 division was shown. The accurate interpretation of MCA anatomy and identification of the occlusion is imperative for thrombectomy selection. True anomalies of the MCA include accessory MCA arising from the anterior cerebral artery, an MCA duplication arising from the internal carotid artery (ICA), and a fenestrated MCA.13 There is a high variability in MCA branching patterns.14 A prominent anterior temporal artery which arises from the proximal M1 segment may be confused with an accessory or duplicated MCA. Whereas accessory MCAs have reported prevalence of 2% and are prone to aneurysm formation, the normal variant of an early division (bifurcation) of the M1 segment close to its origin at ICA is a common finding and not associated with an increased risk of aneurysm formation.13 Based on our own experiences, we hypothesized that MT in patients with an early M1 division would be associated with lower reperfusion rates. In M1 occlusions, the choice of the inferior trunk for distal stent retriever placement is associated with a high rate first pass near-complete/complete reperfusion.6 However, with an early MCA division present, the placement of the distal stent retriever in the inferior trunk can be technically challenging. Still, patients with an early M1 division showed high rates of complete and near-complete reperfusion consistent to comparable studies.15,16
A recent retrospective study by Schwaiger et al.4 showed that tortious vessels significantly influence the results of MT with stent-retrievers for the treatment of AIS. Patients without successful substantial recanalization (TICI 0–2a) showed significantly larger ICA/M1 angles (mean, 110 °± 23.8° versus 69° ± 28.7°, p < .001) and significantly larger M1/M1 angles (56° ± 29.2° versus 29° ± 26.6°, p = .001) compared to patients with successful recanalization (TICI 2b/3). However, further studies evaluating the association between vessel anatomy and recanalization success are lacking; in particular, there are no studies available that analyze the impact on M1 length an angiographic outcome after MT for AIS.
In patients with an early M1 division treated with aspiration-only technique, a higher rate of sICH was observed (p = 0.013). The hemorrhage was confirmed postinterventionally in the infarct core in two of three cases and might be explained by the spatial relationship between the MCA division and lenticulostriate arteries, as these supply the internal capsule and basal ganglia, which are vulnerable and develop readily secondary infarction and hemorrhagic transformation despite successful recanalization.17 In one patient, a perforation of the M1 segment was confirmed, and the early division of the MCA might have contributed to the pathogenesis. In those cases, predicting the length of the M1 segment in the pre-interventional NECT might be useful.
Another interesting finding was the effect of M1 length on clinical outcome. Patients with an early M1 division showed a trend for lower rates of favorable outcome at discharge (37% vs. 50%; p = 0.061). The result was significant in the subgroup analysis with patients treated with aspiration only (28.6% vs. 56.9%; p = 0.024). The occlusion site within the M1 segment (proximal vs. distal) has shown not to be associated with recanalization success.18 Proximal occlusions of the M1 segment incorporating the lenticulostriate perforators are associated with a poorer clinical outcome than distal M1 occlusions that spare these perforators. On the contrary, the baseline ASPECTS between the two groups in our study were comparable (p = 0.545), suggesting that there might be additional factors which should be considered: clot burden, thrombus length/composition, and presence of collaterals.19,20
A late M1 division was associated with atherosclerotic disease as the main cause of AIS with a higher rate of tandem occlusion or stenosis (15% vs. 5.7%, p = 0.060). As such, no impact on angiographic or clinical outcome was found. We postulate that the late division group might have had a robust collateral flow and therefore achieved a similar functional outcome.
A limitation of our study is the retrospective and multicenter design including attendant selection bias and the usage of different equipment and techniques. Clinical outcome after 90 days was missing in 105 patients, introducing a potentially confounding bias. Although angiographic data were regraded in a blinded fashion, results could still be less favorable after core-laboratory adjudication. Notably, there was no difference regarding the endovascular approach between the two groups.
Conclusions
The presence of an early division of the MCA is a common finding. Our results suggest that this normal variant seems to have no impact on angiographic outcome following MT.
Authors’ contribution
Conception and design: DB
Acquisition of data: HS, VM, ACH
Analysis and interpretation of data: VM, LG, SF, CR, MF, AR, DB, HS
Drafting the article: HS, LG
All authors have read and approved the manuscript.
Availability of data and material
All data generated or analyzed during this study are included in this published article.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Ethics approval and consent to participate
According to the guidelines of the respective local ethics committees, ethical approval was given when necessary for this anonymous retrospective study, which was conducted in accordance to the Declaration of Helsinki. A patient’s consent for treatment was obtained according to the individual institutional guidelines. Due to the retrospective nature of the study additional informed consent was deemed unnecessary.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
ORCID iD
Hanna Styczen https://orcid.org/0000-0002-9623-4156
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
All data generated or analyzed during this study are included in this published article.