Abstract
Objectives This study reported a single-center clinical trial of endovascular treatment for symptomatic nonacute occlusion of the intracranial large artery (NA-ILAO). The aim of this study was to evaluate the safety, feasibility, and clinical effect of simple balloon dilatation and stent implantation.
Methods The patients diagnosed with symptomatic NA-ILAO were enrolled. A total of 40 cases were included in this study. While recanalization failed in 4 patients, it was successful in 36 patients, who were then divided into two groups for further analysis: balloon dilatation group ( n = 24) and stent implantation group ( n = 12). The perioperative complications, clinical outcome, and follow-up results were analyzed.
Results Perioperative complications in the stent implantation group were significantly higher than those in the simple balloon dilatation group ( p < 0.05). There were 21 and 10 cases of 90-day good clinical outcome (modified Rankin scale [mRS] ≤ 2) in the balloon and stent groups, respectively ( p = 0.518). All patients with successful recanalization underwent digital subtraction angiography (DSA) or CT angiography (CTA) during an average follow-up of 14 months. There were two cases of restenosis in the balloon dilatation group and one in the stent implantation group ( p = 1.000). There were two cases of re-occlusion in the stent group and none in the balloon dilatation group ( p < 0.001). Stroke recurred in two cases in the stent group and in one case in the simple balloon dilatation group ( p = 0.013).
Conclusion Endovascular recanalization is safe and feasible for patients with symptomatic NA-ILAO. Compared with stent implantation, simple balloon dilation may be a better recanalization method, but larger randomized controlled trials are needed to confirm it.
Keywords: nonacute intracranial large artery occlusion, endovascular recanalization, balloon dilatation, stent implantation
Introduction
Large artery intracranial occlusive disease poses a major stroke problem worldwide and is associated with high risk of stroke recurrence and poor stroke outcome. 1 To distinguish the time window of treatment for acute intracranial artery occlusion, some studies refer to occlusion for more than 24 hours as nonacute intracranial large artery occlusion (NA-ILAO). 2 Hemodynamics after NA-ILAO is the main mechanism leading to the recurrence of stroke. 3 4 Improving the hemodynamics of the low perfusion area through revascularization can prevent the deterioration and recurrence of stroke. However, how revascularization can be achieved is a hot issue among neurologists at present. Extracranial–intracranial artery bypass surgery is very difficult to perform, and there is not enough evidence-based medical support for its safety and efficacy. In the recent years, intravascular recanalization has become a popular method in clinical practice. At present, the technique of nerve intervention is widely used. Balloon angioplasty and stenting are also necessary for treatment of nonacute intracranial arterial occlusion, but safety and efficacy of these procedures need to be further studied.
Therefore, this study was conducted to evaluate the safety, feasibility, and clinical effect of simple balloon dilatation and stent implantation in patients with symptomatic NA-ILAO for promoting a better treatment option.
Materials and Methods
Study Population
Forty consecutive patients with symptomatic NA-ILAO treated in the Third People's Hospital of Hubei Province from January 2015 to October 2020 were included in this retrospective study. Recanalization failed in 4 patients, and it was successful in 36 patients who were further divided into two groups: the balloon dilatation group and the stent implantation group. Nonacute occlusion was defined as stroke or transient ischemic attack (TIA) for greater than 24 hours, which was diagnosed by computed tomography angiography (CTA)/magnetic resonance angiography (MRA) and confirmed by digital subtraction angiography (DSA) as intracranial artery occlusion, including occlusion of the internal carotid artery (ICA), middle cerebral artery, and basilar artery. 2 The clinical and imaging data were collected and analyzed. Informed consents were obtained from all the patients.
Inclusion and Exclusion Criteria
The inclusion criteria were the following: (1) atherosclerosis was the primary etiology of aterial occlusion; (2) DSA confirmed the occlusion of the large intracranial artery, stroke, or TIA related to the occluded artery; (3) the nervous system was deteriorating despite aggressive medical treatment; (4) the preoperative CT revealed small infarction core and large area of hypoperfusion in the occluded territory; and (5) DSA showed retrograde perfusion of the distal vessels.
The exclusion criteria were the following: (1) nonarteriosclerosis occlusion, including arteritis, dissection, cardiogenic thrombus, moyamoya disease, etc.; (2) any hemorrhagic disorders; (3) large infarction core; (4) contraindications to heparin, aspirin, clopidogrel, metal implants, or narcotic drugs; (5) life expectancy less than 1 year due to other medical conditions; and (6) patients who were unable to tolerate general anesthesia.
Endovascular Recanalization Procedure
A combination of aspirin (100 mg/d, Bayer Corporation) and clopidogrel (75 mg/d, Sanofi Pharma Bristol-Myers Squibb SNC) was taken for patients at least 3 to 5 days before surgery. All procedures were performed under general anesthesia. The right femoral artery was punctured, then an 8-Fr arterial sheath was placed. Heparin was injected intravenously with 50 IU/kg to systemic heparinization, and 1,000 IU heparin was added every 1 hour. An 8-Fr guiding catheter (Envoy, Cordis, United States) was advanced into the proximal ICA or vertebral artery (VA), then a middle catheter (Navien, EV3, United States) accessed through the distal intracranial artery. The microwire (Synchro, Stryker, United States) was used in a combination with a microcatheter (Echelon-10, Stryker) to carefully pass through the occluded segment. If the microwire and microcatheter could not pass the occluded segment or enter the distal true lumen after repeated attempts, the procedure was stopped. If the microwire was successfully steered through the occluded segment, then microcatheter injection confirmed the position distal to occlusion in the distal true lumen. Subsequently, an exchange-length microwire (Transend 014/300, Stryker) was placed in the appropriate position, and the microcatheter was removed. A 2- to 2.5-mm angioplasty balloon catheter (Gateway, Stryker) was centered across the lesion and inflated slowly distal to proximal. The surgeon decided whether or not to implant stent according to the condition of the vessel observed after dilation: (1) the stent should not be implanted when no elastic retraction was observed within 15 to 30 minutes postdilation and (2) the stent was considered when a rough vessel wall or dissection was observed postdilation and when residual stenosis postdilation was greater than 50% and could not be corrected by re-dilation. Based on the measurement of the proximal and distal diameters of the target vessel as well as the length of the occluded segment, a self-expandable stent (Neuroform EZ, Stryker or Enterprise, Codman & Shurtleff, United States) was introduced and deployed according to the operator's preference. Postoperative angiography was performed to confirm the patency. Successful revascularization was defined as a modified thrombolysis in cerebral infarction (TICI) grade 2b or 3 and residual stenosis ≤50%. Brain CT was performed immediately after the operation to rule out intracranial hemorrhage. Blood pressure was maintained at approximately 80% of basal blood pressure to prevent hypertransfusion cerebral hemorrhage. After successful recanalization, double antiplatelet therapy was performed for at least 6 months, followed by lifelong aspirin or clopidogrel monotherapy.
Data Collection and Follow-Up
We collected the following baseline and treatment variables: demographic, clinical, procedural, imaging, and follow-up data. Clinical outcomes were evaluated using the modified Rankin scale (mRS) and the National Institutes of Health Stroke Scale (NIHSS). Complications included dissection, perforator occlusion, hypertransfusion cerebral hemorrhage, and acute thrombosis. Good clinical outcome was defined as mRS ≥2. 5 Restenosis and re-occlusion were defined as a stenosis diameter greater than 50% or complete occlusion of the target artery, respectively. 6
Statistical Analysis
All normally distributed continuous quantitative variables were expressed as mean ± standard deviation (SD), non-normally distributed continuous variables as median and interquartile range, and categoric variables as proportions. Comparisons between groups were performed using Student's t -test or the approximate Fisher's precision probability test when the variances of comparison between groups were quite different and n < 40. Differences were considered significant as p < 0.05. All statistical analyses were performed via SPSS 23.0 (IBM).
Results
Baseline Characteristics
All 40 patients who underwent endovascular treatment were symptomatic nonacute large intracranial artery occlusion. Successful recanalization was performed in 36 patients, including 19 males and 17 females with an average age of 61.65 ± 8.03 years (45–73 years). Recanalization failed in four patients. One was a case of occlusion of the C6 segment of the right ICA with a long interval (>12 months) to recanalization, no stub was observed in this. There was occlusion of the M1 segment in two patients and the micro-guidewire failed to pass through due to a V3 segment occlusion in 1 patient. There were no significant differences in demographic characteristics, risk factors, or clinical characteristics between the two groups ( Table 1 ).
Table 1. Comparison of baseline characteristics between balloon dilatation group and stent group.
| Variable | Balloon dilatation group ( n = 24) | Stent group ( n = 12) | p value |
|---|---|---|---|
| Age, mean (standard deviation [SD]), y | 61.63 (7.67) | 62.00 (9.07) | 0.575 |
| Male, N (%) | 13 (54.2%) | 6 (50.0%) | 0.780 |
| Hypertension | 16 (66.7%) | 8 (66.7%) | >0.999 |
| Diabetes mellitus | 9 (37.5%) | 4 (33.3%) | 0.622 |
| Hyperlipidemia | 6 (25.0%) | 4 (33.3%) | 0.343 |
| Smoke | 12 (50.0%) | 6 (50.0%) | >0.999 |
| Coronary artery disease | 5 (20.8%) | 2 (16.7%) | 0.556 |
| Stroke history | 11 (45.8%) | 6 (50.0%) | 0.780 |
| Last symptom onset to treatment (d), median (IQR) | 11.00 (6.00–25.50) | 13.50 (13.00–25.00) | 0.055 |
| Preoperative NIHSS, median (IQR) | 8.00 (6.00–12.00) | 9.00 (6.50–11.50) | 0.967 |
| Preoperative mRS, median (IQR) | 3.0 (2.0–3.0) | 3.0 (2.0–3.5) | 0.863 |
| Occlusion location, N (%) | |||
| ICA | 6 (25.0%) | 4 (33.3%) | 0.635 |
| MCA | 8 (33.3%) | 5 (41.7%) | |
| BA | 10 (41.7%) | 3 (25.0%) | |
Abbreviations: BA, basilar artery; ICA, intracranial internal carotid artery; IQR, interquartile range; MCA, middle cerebral artery; mRS, modified Rankin scale; NIHSS, National Institutes of Health Stroke Scale.
Perioperative Outcome
There was perioperative complication in 5/36 (13.9%) cases and total stroke or death within 30 days in 3/36 (8.3%) patients. Perioperative complications included two cases in the balloon dilatation group (one case of dissection with good forward blood flow and no stent implantation, and one case of asymptomatic cerebral hemorrhage) and three cases in the stent group (one case of symptomatic cerebral hemorrhage, one case of acute intrastent thrombosis, one case of branch embolization, and all three complications in worsening of symptoms). The perioperative complications in the stent group were significantly higher than those in the simple balloon dilatation group ( p < 0.05).
Follow-Up Outcome
The median follow-up time was 13 months (interquartile range [IQR] = 7.25–22.50). Recanalization was successful in 32 patients with good clinical outcome (mRS ≤ 2) at 90 days (31/36, 86.11%). During the clinical follow-up, DSA or CTA was performed in all successful recanalization patients ( Figs. 1 and 2 ), and three cases of restenosis occurred (two in the balloon dilatation group and one in the stent implantation group). Re-occlusion was found in two cases (all in the stent group), and the rate of re-occlusion in the stent group was significantly higher than that in the simple balloon dilatation group ( p < 0.05). There was recurrence of stroke in three cases (two in the stent group and one in the simple balloon dilatation group); the stroke recurrence rate in the stent group was significantly higher than that in the balloon dilatation group ( p < 0.05; Table 2 ).
Fig. 1.
A man with right limb weakness for 7 days. ( A ) Diffusion-weighted imaging showed acute cerebral infarction in the center of the left semicircle. ( B ) Computed tomography (CT) perfusion revealed that there were large areas of hypoperfusion in the left middle cerebral artery territory. ( C ) Preoperative angiography confirmed the occlusion of C6 segment of left internal carotid artery (ICA), ( D ) with anterior communicating artery collateral. ( E ) Under right roadmap guidance, the microwire, in combination with a microcatheter, passes through the occluded segment. ( F ) After balloon dilatation angioplasty, the left ICA was successfully recanalized with thrombolysis in cerebral ischemia grade 3. ( G ) There was no stenosis at 6 months postoperatively by angiography. ( H ) Perfusion improved significantly after 6 months.
Fig. 2.
A man with right limb weakness, vertigo, slurred speech for 30 days. ( A ) Diffusion-weighted imaging showed multiple infarcts in the pons. ( B ) Computed tomography (CT) angiography showed the V4 segment of the bilateral vertebral artery and basilar artery occlusion. ( C ) CT perfusion revealed that there were large areas of hypoperfusion in the bilateral cerebellum and brainstem territory. ( D ) Preoperative angiography confirmed the occlusion of the V4 segment of the bilateral vertebral artery and basilar artery. ( E ) The lesion was traversed with a microwire, in combination with a microcatheter. ( F ) The residual stenosis after dilation by a small balloon (1.0 mm) was more than 50%, then used a lager balloon (2.5 mm) dilate again. ( G ) The basilar artery was successfully recanalized with Thrombolysis in Cerebral Ischemia grade 3. ( H ) There was no stenosis at 6 months postoperatively by angiography.
Table 2. Periprocedural complications, outcomes and following-up outcomes.
| Variable | Balloon dilatation group ( n = 24) | Stent group ( n = 12) | p value |
|---|---|---|---|
| Periprocedural complications, N (%) | 2 (8.3%) | 3 (25.0%) | 0.011 |
| Dissection ( N ) | 1 | 0 | |
| Acute thrombosis ( N ) | 0 | 1 | |
| Reperfusion hemorrhage ( N ) | 1 | 1 | |
| Branch occlusion ( N ) | 0 | 1 | |
| Stroke within 30 d, N (%) | 0 | 3 | <0.001 |
| Death within 30 d, N (%) | 0 | 0 | >0.999 |
| 90 d mRS ≤ 2 | 21 (87.5%) | 10 (83.3) | 0.518 |
| Follow-up time (mo), median (IQR) | 13.00 (8.50–13.50) | 15.00 (12.00–20.00) | 0.877 |
| Restenosis, N (%) | 2 (8.3%) | 1 (8.3%) | >0.999 |
| Re-occlusion | 0 | 2 (16.7%) | <0.001 |
| Stroke recurrence (beyond 30 d) | 1 (4.2%) | 2 (16.7%) | 0.013 |
Abbreviations: IQR, interquartile range; mRS, modified Rankin scale.
Discussion
Although a growing number of studies have reported that intravascular recanalization appeared to be safe and efficient for symptomatic NA-ILAO. 7 8 9 10 11 12 However, there was heterogeneity of outcomes and perioperative complications for endovascular recanalization, 13 and it was believed that there were differences in the difficulty and risk at different locations of occlusion. 2 14 The high perioperative complication rate and high postoperative restenosis/re-occlusion rate 15 greatly limit its wide application.
In our study, the total perioperative complication rate was 13.9%, the restenosis/re-occlusion rate was 13.9%, and the total stroke recurrence rate was 8.4%. We searched the PubMed database for more than 10 published literatures 2 7 8 13 14 15 16 17 18 19 20 21 ( Table 3 ) of symptomatic NA-ILAC with an overall success rate of 83.9%, perioperative complication rate of 20.1%, restenosis/re-occlusion rate of 12.4%, and postoperative adverse events rate of 6.9%. The results of the previous studies were not significantly different with this study. In contrast to this study, nearly 90% of the endovascular patients in the retrieved study received stenting. In our study, for the first time, we compared the clinical outcomes of patients with NA-ILAO treated with simple balloon dilatation and stenting. However, the high rate of recanalization and good clinical prognosis suggested that balloon dilation alone was not inferior to stenting. It should be highlighted that since this is a retrospective study, not enough attention was paid to shower emboli and any potential cognitive impairment brought on by numerous minor postprocedural emboli, and the necessary data were also lacking. More research has been done on the effects of tiny emboli on cognition following orthopaedic surgery and cardiopulmonary bypass, although the links between the two are still unclear. 22 23 There are two primary techniques for examining postoperative shower emboli: magnetic resonance imaging and transcranial Doppler. 24 25 Both of these approaches have benefits and drawbacks, and prior researches have not consistently found encouraging results when shower emboli are examined. Additionally, there have been inconsistent follow-up periods for postoperative cognitive dysfunction in earlier research, which makes it challenging to determine the cause and degree of postoperative cognitive impairment. These restrictions mean that we can concentrate on comparing the postoperative shower emboli assessment techniques and their association with long-term cognitive impairment in the future.
Table 3. Documentation.
| Study | Country | Sample size ( n ) | Successful recanalization ( n ) | Occlusion location | Procedure | Follow-up time | Complications a | Restenosis/re-occlusion | Adverse event b |
|---|---|---|---|---|---|---|---|---|---|
| He et al 7 | China | 27 | 26 | PCI | Stent 26 | 10.5 | 5 | 3 | 5 |
| Aghaebrahim et al 8 | United States | 24 | 24 | ACI 6 PCI 18 |
Balloon 1 Stent 23 |
3 | 6 | 2/16 | 2 |
| Chen et al 16 | China | 16 | 12 | ACI 4 PCI 12 |
Balloon 1 Stent 11 |
3–64 | 1 | – | 1 |
| Gao et al 17 | China | 14 | 12 | PCI | Stent 12 | 8–94 | 1 | 1/4 | 1 |
| Ma et al 13 | China | 13 | 11 | ACI | Balloon 2 Stent 9 |
3–12 | 5 | 2/11 | 1 |
| Zheng et al 14 | China | 22 | 21 | ACI | Balloon 14 Stent 7 |
5 | 7 | 1/10 | 0 |
| Yao et al 2 | China | 32 | 17 | ACI 20 PCI 12 |
Stent 17 | 39.4 | 3 | 3/10 | 1 |
| Yu Jia et al 15 | Korea | 38 | 29 | ACI | Stent 29 | 36.5 | 4 | 5 | 2 |
| Gao et al 21 | China | 36 | 29 | ACI | Stent 29 | 12 | 14 | 4 | 2 |
| Zhao et al 18 | China | 31 | 27 | PCI | Balloon 11 Stent 16 |
11 | 6 | 2/20 | 2 |
| Mo et al 19 | China | 42 | 35 | ACI | Balloon 4 Stent 31 |
9 | 5 | – | 0 |
| Gao et al 20 | China | 52 | 48 | ACI 43 PCI 9 |
Stent 48 | 19 | 4 | 5/38 | 3 |
| Total | 347 | 291 (83.9%) | Balloon 33/291 (11.3%) | 61/291 (20.1%) | 26/210 (12.4%) | 20/291 (6.9%) |
Abbreviations: ACI, anterior circulation infarction; PCI, posterior circulation infarction.
Perioperative complications including cerebral hemorrhage, dissection, stent thrombosis, perforation, perforator occlusion, etc.
Adverse events during follow-up including death, stroke recurrence, etc.
Stenting may be more effective in preventing elastic retraction and negative remodeling than balloon angioplasty, 26 but early studies have shown no significant difference in reducing the risk of stroke recurrence and death. 27 Whether stenting is superior to angioplasty is still a matter of debate. Our results showed that the stroke recurrence rate and the re-occlusion rate of balloon dilatation alone were significantly lower than stenting, which may be related to the improvement of doctors' experience and the progress and simplification of the balloon dilatation procedure. More importantly, the safety of the procedure has been greatly improved by simple balloon dilatation, and increase of the operation procedure will undoubtedly increase the risk of surgery. Second, balloon angioplasty alone reduced the incidence of acute or subacute thrombosis caused by metallic foreign body stimulation. 28 29 30 The re-occlusion rate during balloon dilatation was lower than that of stent implantation, which may be related to the reduction of inflammatory vascular endothelial stimulation caused by metallic foreign body implantation. It must, however, be understood that comparing angioplasty to stents can be unfair and might have a selection bias. When balloon angioplasty alone was deemed insufficient or impractical, a stent was sometimes employed. Further study would be required to contrast the benefits and drawbacks of angioplasty and stent therapy because these patients would normally be more serious; the risk of re-occlusion after stent placement may naturally be higher and the issues they face may naturally be bigger.
Our study has some limitations. First, our study was a single-center retrospective study with a small sample size with limited reliability. Second, due to the lack of clinical research experience in endovascular treatment of NA-ILAO, more experience is needed to master the indications and recanalization techniques. In addition, we had a short follow-up time, and long-term research is needed to verify the operation outcome in the future.
Conclusion
Recanalization of symptomatic NA-ILAO is technically feasible for some patients and has a definite therapeutic effect. Therefore, recanalization therapy can be used as a safe and effective treatment for symptomatic NA-ILAO. However, recanalization requires a high level of neurosurgical intervention, clinical experience, and perioperative management, and has certain perioperative risks. As far as the mode of recanalization is concerned, balloon dilation alone may be superior to stent implantation. Our study suggested that adverse vascular events increased significantly when the onset to treatment time exceeded 12.5 days, which might provide a reference for the selection of reasonable treatment timing. Larger randomized controlled trials are warranted to provide more reliable results, given the small sample size and retrospective nature of the current study. Due to the limitations of the quantity and quality of the studies included, these findings need to be validated by more high-quality prospective, multicenter studies.
Funding Statement
Funding This work was supported by the Hubei Provincial Health Commission Guidance Project (WJ2019F177).
Conflict of Interest None declared.
Ethical Approval and Consent to Participate
The study protocol was approved by the Ethics Committee of The Third People's Hospital of Hubei Province, Jianghan University. Informed consent was obtained from all the study subjects before enrollment.
Availability of Data and Material
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
Author Contributions
B.D. contributed to the conception, design, and manuscript revision. B.Z. and T.P. collected the data and drafted the manuscript. W.Z. performed the data analysis and edited the manuscript. X.L. and J.L. collected all the data and revised the manuscript.
Both the authors contributed equally to this study.
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