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Ischemic stroke
Original research
Lesion location, stability, and pretreatment management: factors affecting outcomes of endovascular treatment for vertebrobasilar atherosclerosis
  1. Matthew D Alexander1,
  2. Jeffrey M Rebhun2,
  3. Steven W Hetts3,
  4. Anthony S Kim4,
  5. Jeffrey Nelson5,
  6. Helen Kim5,
  7. Matthew R Amans3,
  8. Fabio Settecase3,
  9. Christopher F Dowd3,
  10. Van V Halbach3,
  11. Randall T Higashida3,
  12. Daniel L Cooke3
  1. 1Department of Radiology, University of Washington, Seattle, Washington, USA
  2. 2University of California, Berkeley, California, USA
  3. 3Department of Neurointerventional Radiology, University of California San Francisco, San Francisco, California, USA
  4. 4Department of Neurology, University of California San Francisco, San Francisco, California, USA
  5. 5Department of Anesthesia and Perioperative Care, University of California San Francisco, San Francisco, California, USA
  1. Correspondence to Dr D L Cooke, Department of Radiology and Biomedical Imaging, University of California San Francisco, 505 Parnassus Avenue, San Francisco, CA 94143-0628, USA; daniel.cooke{at}ucsf.edu

Abstract

Background and purpose The proper role of endovascular treatment of cervicocerebral atherosclerosis is unclear. Posterior circulation disease has not been investigated as extensively as disease in the anterior circulation. In this study, we characterized the rates of technical success, transient ischemic attack, stroke, and death or disability, for both acute and elective endovascular treatment of atherosclerosis in the vertebrobasilar system.

Methods We identified patients with atherosclerosis of the vertebrobasilar circulation who underwent endovascular intervention at our hospital through retrospective medical record review, and evaluated the association between lesion and treatment features and subsequent stroke, death, or disability at 30 days and 1 year.

Results We identified 136 lesions in 122 patients, including 13 interventions for acute strokes. Technical success was achieved in 123 of 136 cases (90.4%). Elective procedures had higher rates of technical success (6.5% vs 15.4%, p=0.21) and better clinical outcomes. In multivariate analysis, intracranial lesions were associated with more disability (modified Rankin Scale score >2) at 30 days (OR 7.1, p=0.01) and 1 year (OR 10, p=0.03). Patients with non-hypoperfusion related symptoms had fewer strokes at follow-up at 1 year when treated after an asymptomatic interval of >10 days compared with those treated within 10 days of the presenting symptoms (OR 0.2, p=0.03). Statin treatment prior to intervention was associated with favorable outcomes across several examined endpoints. Preoperative antiplatelet treatment was associated with lower rates of disability at 30 days and 1 year (OR 0.1, p<0.01 and OR 0.07, p=0.01, respectively), and preoperative anticoagulation treatment was associated with higher rates of death at 30 days, particularly when prescribed for reasons other than atrial fibrillation (OR 6.4, p=0.01).

Conclusions Endovascular treatment of symptomatic vertebrobasilar atherosclerosis can be performed safely and with good outcomes. Technical results were better for those with extracranial disease while clinical outcomes were more favorable in those patients with non-progressive symptoms in the subacute period and those receiving statin therapy.

  • Atherosclerosis
  • Stent
  • Angioplasty
  • Stroke

https://doi.org/10.1136/neurintsurg-2014-011633

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    Introduction

    Atherosclerotic disease (AD) of both the intracranial and extracranial cervicocerebral arteries is a significant contributor to ischemic stroke. The proper role of endovascular treatment of such AD is controversial, given the disparate findings of recent studies, and the precise role for endovascular treatment of certain medically refractory symptomatic lesions remains to be defined (figure 1).1 ,2

    Figure 1
    Figure 1

    (A) Frontal projection demonstrating focal atherosclerotic plaque (arrow) causing 80% stenosis in the V4 segment of the right vertebral artery. (B) Working view projection following deployment of a stent. (C) No residual stenosis visualized on post-treatment angiography in the frontal projection.

    Data on endovascular therapies for AD of the intracranial and extracranial vertebrobasilar circulation are limited. Vertebrobasilar disease may be considered pathophysiologically distinct from anterior circulation disease and often leads to worse clinical outcomes.3–5 Given this grave potential, more aggressive treatment approaches may be warranted. To better understand the outcomes of endovascular interventions performed on vertebrobasilar AD, we reviewed a cohort of patients with intracranial or extracranial AD undergoing either elective interventions or emergency treatment for acute ischemic stroke.

    Materials and methods

    Under institutional review board approved protocols, we searched procedure registries at three hospitals with comprehensive neurointerventional services to identify patients for whom angioplasty or stent deployment for vertebral or basilar artery stenosis was initiated either on an elective basis or during endovascular treatment of acute ischemic stroke. Patients with arterial luminal narrowing due to disease processes other than AD, such as vasculitis, trauma, or dissection, were excluded.

    We abstracted information from the medical records of each of these patients according to the guidelines of the Standards Committee of the Society for NeuroInterventional Surgery for investigations of endovascular treatment of intracranial AD.1 Ischemic symptoms were classified as transient ischemic attack (TIA) or stroke. To identify surrogates of lesion stability in keeping with our previously published analysis, symptoms were further subclassified as due to hypoperfusion, if there was clear evidence that reduced perfusion elicited the ischemic symptoms.6 ,7 Examples of hypoperfusion symptoms included reduced flow on perfusion imaging and symptom exacerbation during known hypotension. Symptoms that were likely due to mixed subtypes or symptoms that could not be clearly classified as due to hypoperfusion were classified as indeterminate. To test the hypothesis that less stable lesions caused recent non-hypoperfusion symptoms, non-hypoperfusion lesions were further classified according to the duration of the symptom free interval prior to treatment. Previous treatment with antiplatelet therapy (excluding preprocedural loading doses) or warfarin therapy was noted, as was previous treatment with statins. Functional status was evaluated using the modified Rankin Scale (mRS), as assigned by the data abstractors, based on descriptions of functional performance in the medical record if a score was not formally noted.

    Lesion features and technical success were abstracted from clinical reports from the primary interventionalist, if available, or imputed by investigators by reviewing available clinical data. The degree of arterial stenosis was determined using the Warfarin–Aspirin Symptomatic Intracranial Disease Trial (WASID) technique.1 ,8 ,9

    Technical success was defined as residual stenosis <50% in the treated artery without any procedural complications.1 To blind the measurements, one author performed image review and another assessed clinical outcomes by reviewing medical records. Any procedural complications were noted, as well as whether or not such complications were symptomatic.

    The primary operator determined the timing and type of clinical and imaging follow-up for each patient in an individualized manner based on severity of symptoms, comorbidities, and the experience of the interventionalist.

    Endpoints evaluated were ischemic stroke, death, and disability (mRS >2) at 30 days and at 1 year, as assessed based on any available clinical documentation. Patients without data at these time points were excluded from analysis. Statistical analysis was performed with χ2 tests and logistic regression analysis. Multivariate models were then constructed with variables with p values <0.2 in univariate analysis, excluding any additional variables with near colinearity to enhance model stability. All statistical tests were performed using IBM SPSS V.20 (IBM, Armonk, New York, USA).

    Results

    We identified 136 lesions among 122 patients treated between August 1998 and August 2013 that met the inclusion criteria. Patient demographics, symptoms, lesion characteristics, and treatment features are summarized in table 1. Expanded findings by symptom subtypes are provided in the online supplementary table S1. The use of periprocedural antiplatelet agents changed over time. Most patients (116 lesions, 85.6%) were treated with at least single antiplatelet therapy prior to endovascular procedures, while 53 (39.0%) lesions were treated with dual antiplatelet therapy, which became our standard practice in 2005. We also favored treatment with stents rather than angioplasty alone. One hundred and two (82.9%) of 123 elective treatments were performed with stent deployment while the remainder received angioplasty alone. Concomitant angioplasty was performed in all interventions performed with stent deployment.

    View this table:
    Table 1

    Demographics, and lesion and treatment characteristics

    Technical success was achieved in 123 (90.4%) procedures overall, with success in 47 of 51 (92.2%) extracranial lesions and in 76 of 85 (89.4%) intracranial lesions. Vertebral artery origin lesions resulted in higher rates of technical success compared with all other locations (98.0% vs 85.1%, OR 9.1, p=0.02). There were 10 (7.4%) procedural complications, all for intracranial lesions, with 4 of these complications (2.9%) being symptomatic. Complications are summarized in the online supplementary table S2. Median follow-up time was 413 days (IQR 9–1257). Thirty day and 1 year follow-up data were available for 41 (33.6%) and 72 (59.0%) patients, respectively. The follow-up data are summarized in table 2.

    View this table:
    Table 2

    Endpoints at 30 days and 1 year

    Disability at 30 days and death at 1 year were higher for intracranial lesions (28.6 vs 0.0%, p=0.049; 35.5% vs 11.8%, p=0.01) compared with extracranial lesions. This was particularly true with ostial lesions compared with intracranial and extracranial lesions distal to the ostium, with lower 1 year mortality (1.9% vs 14.1%, OR 0.14, p=0.03). Treatment with a statin was associated with lower rates of stroke, death, and disability at 1 year (3.1% vs 66.7%, p<0.01; 12.1% vs 83.3%, p<0.01; 19.7% vs 83.3%, p=0.02). Previous treatment with anticoagulation therapy was associated with higher rates of stroke and death at 1 year (16.1% vs 2.4%, p=0.049; 29.0% vs 9.8%, p=0.04). When the indication for anticoagulation was not for atrial fibrillation, associations were stronger with stroke and death at 1 year (16.7% vs 2.4%, p=0.04; 30.0% vs 9.5%, p=0.03). Lesions causing non-hypoperfusion symptoms with more than 10 days since most recent symptoms at the time of treatment had lower rates of stroke at 1 year (3.3% vs 25.0%, p=0.04).

    In multivariate analysis, intracranial lesion location was more likely to be associated with disability at 30 days and death at 1 year (OR 7.1, 95% CI 1.2 to 148, p=0.01; OR 10, 95% CI 1.2 to 83, p=0.03, respectively) than extracranial lesion location. Patients with non-hypoperfusion symptoms and more than 10 days without additional symptoms prior to treatment were less likely to have stroke at 1 year (OR 0.2, 95% CI 0.01 to 0.7, p=0.03). Preoperative statin treatment was associated with lower odds of stroke, death, or disability at 1 year (OR 0.02, 95% CI <0.01 to 0.14, p<0.01; OR 0.05, 95% CI <0.01 to 0.5, p<0.01; OR 0.06, 95% CI <0.01 to 0.6, p=0.02, respectively). Preoperative antiplatelet treatment was associated with lower rates of disability at 30 days and 1 year (OR 0.1, 95% CI <0.01 to 0.2, p<0.01; OR 0.07, 95% CI <0.01 to 0.7, p=0.01). Preoperative anticoagulation treatment was associated with death at 30 days, and this association was stronger when warfarin therapy was prescribed for reasons other than atrial fibrillation, which was included in the multivariate model for this reason (OR 6.4, 95% CI 1.9 to 150, p=0.01). Univariate and multivariate analyses are summarized in the online supplementary table S3.

    Discussion

    The role of endovascular treatment for cervicocerebral AD is controversial. This is true for both anterior and posterior circulation disease, although previous investigations have more often focused on anterior circulation lesions. This retrospective study reviewed the technical and clinical outcomes for a large series of patients who received endovascular treatments of arteries in the intracranial and extracranial vertebrobasilar circulation, both in the setting of acute stroke treatment and on an elective basis.

    Ischemic stroke causes substantial morbidity and mortality worldwide. Intracranial AD accounts for 10–15% of ischemic strokes in the USA and has been reported to account for up to half of ischemic strokes in people of Chinese or African ancestry.1 ,10–13 Among all ischemic strokes, 25–40% are referable to the posterior circulation.14–16 The vertebral artery origin is the most common site of stenosis in these cases, and approximately 20% of posterior circulation strokes occur in the setting of such lesions.16–18 One in four patients with posterior circulation TIA or stroke have atherosclerotic lesions somewhere in the vertebrobasilar system, and these lesions are frequently symptomatic, often in a progressive fashion.3 Patients experiencing TIAs with extracranial vertebral artery disease carry a 30% risk of stroke within 5 years,19–21 and in those with a posterior circulation stroke, recurrence is more than three times as likely if underlying stenosis is present. Strokes in this territory carry a 10–15% annual recurrence risk,18 ,22–24 and recurrence tends to occur soon in the days and weeks following the primary event.22

    In light of the above information, posterior circulation atherosclerosis can be considered fundamentally different than carotid atherosclerosis. However, enrollment in recent clinical trials has been skewed toward the more common anterior circulation lesions. In the Stenting and Aggressive Medical Management for Preventing Recurrent stroke in Intracranial Stenosis (SAMMPRIS) trial, which compared medical management and stenting with medical management alone, patients with posterior circulation lesions represented just 32% of patients in the medical management arm and 39% of the medical management plus stenting arm.25 Unfortunately, early closure of this trial limited subgroup analysis that could have more directly compared anterior and posterior AD. A recent meta analysis contradicts the SAMMPRIS results with respect to vertebrobasilar lesions, indicating that lesions in this territory treated with medical management alone had similar rates of stroke and death compared with patients undergoing endovascular treatment.5 Prior to SAMMPRIS, posterior circulation lesions accounted for 34% and 41% of lesions in the two largest registries investigating the Wingspan stent device,26 ,27 while in the more recent Interventional Management of Stroke (IMS)-III trial investigating interventions for acute ischemic stroke, only 2% of patients undergoing intra-arterial intervention for acute stroke presented with posterior circulation stroke.28 Additionally, the recently published Multicenter Randomized Clinical Trial of Endovascular Treatment for Acute Ischemic Stroke in the Netherlands (MR CLEAN), which demonstrated superior results following endovascular treatment of acute ischemic stroke, did not enroll patients with posterior circulation strokes.29

    There are few direct comparisons of outcomes of endovascular treatment of anterior circulation AD and posterior circulation AD, although in a previously reported analysis of our intracranial AD cohort there was no difference in outcomes for anterior and posterior circulation lesions.7 Perhaps the most relevant comparison of our outcomes with existing outcome data is for patients treated for acute ischemic stroke. Given the exceedingly small number of posterior circulation lesions treated in IMS-III, the reported outcomes of this study may roughly be considered representative of anterior circulation disease only. In the IMS-III intra-arterial intervention group, 39% of patients had a good outcome (mRS ≤2) at 90 days compared with 31% of the acute stroke patients in our cohort.28 At 1 year, we found 3.0% and 12.2% of patients within our treatment cohort had a documented secondary stroke or had died. This contrasts with the results of the Carotid Revascularization Endarterectomy versus Stenting Trial (CREST), that compared carotid artery stenting and endarterectomy, in which long term stroke and death rates were 10.2% and 11.3%, respectively.2 In the SAMMPRIS trial, the 30 day stroke rate was 10.3%, and the rate of death at 1 year was 3.4%.25 Despite the seemingly worse natural history for posterior circulation lesions compared with those in the anterior circulation, technical outcomes do not appear to be appreciably different, although further direct comparison is necessary.7

    Endovascular treatment of intracranial lesions is often more difficult and carries a higher risk of adverse events than treatment of extracranial lesions, especially when comparing the relative safety of treating the vertebral origin compared with downstream lesions.1 ,16 ,20 ,21 ,30–37 In this study, we found higher rates of technical success and no procedural complications with ostial lesions. Risks of symptomatic complication were low (2.9%), particularly for ostial lesions, although the type of symptomatic presentation proved as predicative of future stroke as the lesion location itself. In addition to technical complications, intracranial lesions had significantly higher rates of disability at 30 days and death at 1 year. This result may reflect the perforators arising from intracranial vertebrobasilar arteries that may become symptomatically occluded in the setting of intracranial balloon angioplasty or stent deployment.

    While the treatment success rates in our series include technology and techniques from up to 16 years ago, our outcomes were comparable with some of the largest case series from recent years.1 ,25–27 Our series included patients with AD treated in the context of endovascular treatment of acute stroke. For direct comparison, 1 year death or disability among patients undergoing elective treatment was 6.1% (0.0% extracranial vs 7.7% intracranial) in our study, compared with 20.0% in the intervention group of SAMMPRIS.25 Our rate of death or disability at 1 year was nearly half that of the aggressive medical management arm of SAMMPRIS (7.7% vs 12.2%).25

    The type of symptoms caused by posterior circulatory disease appears to play a role in clinical outcomes. Vertebrobasilar lesions, whether by reducing perfusion or producing more discrete thrombotic or embolic occlusion of large and small vessels, are both exacerbated by the more limited pial collateralization characteristic of the posterior circulation vessels compared with the anterior circulation.38 As such, injury to the vertebrobasilar watershed carries disproportionately severe clinical outcomes relative to the parenchymal volume it represents.3 ,24 ,38 We previously reported the effect of lesion stability features, as indicated by symptom types, on outcomes after stenting of intracranial lesions in general.6 ,7 The current analysis is consistent with the view that the same features may predict prognosis following treatment of both intracranial and extracranial vertebrobasilar AD. Patients with hypoperfusion symptoms potentially have plaques less likely to rupture, thrombose, or shed emboli. Consequently, these lesions may be less likely to respond adversely to mechanical manipulation. Our analysis showed improved outcomes for patients who had a 10 day symptom free interval prior to treatment, which is consistent with prior reports suggesting that lesions treated closer to most recent symptom occurrence respond less favorably.4 ,6 ,7 ,39 ,40 These findings presumably relate to the degree of thrombotic instability of atheromatous lesions, which may be more likely to have been recently symptomatic.6 ,7 SAMMPRIS made no distinction in the types of symptoms caused by lesions or most recent symptoms in the inclusion criteria,25 and further research is needed to identify reliable markers for plaque instability and the means to stabilize such lesions prior to intervention.

    Our data are consistent with previous data highlighting the importance of pretreatment antiplatelet therapy8 and statin treatment, which was demonstrated in the Stroke Prevention by Aggressive Reduction in Cholesterol Levels (SPARCL) trial and subsequently confirmed in SAMMPRIS.25 ,41 We noted higher rates of stroke and death in those patients taking anticoagulants, particularly when prescribed for the treatment of intracranial cerebral artery disease itself or other clinical reasons apart from atrial fibrillation. Those patients on anticoagulation may have had more severe or repeated clinical events that necessitated such treatment. We did not resolve the nature of the subsequent stroke and death, and implicating the anticoagulants themselves is premature, although it is consistent with the results of WASID.8

    The current study adds to our understanding of vertebrobasilar circulation AD, but it has several limitations, most of which result from its retrospective design. Lack of prospectively developed protocols to assess symptoms limited the analysis. This is particularly true with respect to determination of symptom subtype. Limited data capture within early postprocedure periods resulted from lack of standardized follow-up and the potential for informative loss to follow-up. This occurred because much of the clinical follow-up occurred at referring centers instead of at our hospital. This limits direct comparison with other investigations in some regards. As previously mentioned, the long study period of 16 years included patients treated with methods previously considered appropriate but not currently the standard of care. Low procedural complication rates may reflect a consistent application of meticulous techniques by experienced operators. Additionally, selection bias exists due to the broad criteria used to determine which lesions merit treatment in clinical practice. Such methodological shortcomings can be mitigated with future prospective investigations.

    Conclusion

    Atherosclerosis of the vertebrobasilar system can cause substantial morbidity related to both the territory it supplies and unique anatomic and physiologic features compared with anterior circulation disease. Despite the intrinsic morbidity of lesions in this location, this study demonstrated the technical feasibility and favorable outcomes following endovascular interventions that are comparable with interventions in the anterior circulation. Endovascular treatment of symptomatic lesions of the vertebral origin appears to be very safe, with no complications for treatment at this location in the current study. Among lesions refractory to medical management, those lesions with the most stable features, as indicated by hypoperfusion symptoms or non-hypoperfusion lesions with at least 10 days since last symptoms, appear to respond most favorably to treatment. Further research to identify lesions most suitable for endovascular treatment and technical factors to optimize outcomes is warranted.

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    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

      Files in this Data Supplement:

    Footnotes

    • Contributors MDA performed the data collection, data analysis, and authored the manuscript. DLC, JMR, MRA, FS, ASK, CFD, VVH, RTH, and SWH participated in patient care, participated in data analysis, and edited the manuscript. JN and HK participated in data analysis and edited the manuscript.

    • Competing interests None.

    • Ethics approval The study was approved by the institutional review boards of each of the medical centers.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Meeting presentation The study was presented at the WNRS 2014 Annual Meeting.