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Hemorrhagic stroke
Does treatment modality affect vasospasm distribution in aneurysmal subarachnoid hemorrhage: differential use of intra-arterial interventions for cerebral vasospasm in surgical clipping and endovascular coiling populations
  1. Daniel Cooke1,
  2. Douglas Seiler1,
  3. Danial Hallam1,
  4. Louis Kim2,
  5. Jeffrey G Jarvik1,2,
  6. Laligam Sekhar1,2,
  7. Basavaraj Ghodke1,2
  1. 1Department of Radiology, University of Washington School of Medicine, Seattle, Washington, USA
  2. 2Department of Neurosurgery, University of Washington School of Medicine, Seattle, Washington, USA
  1. Correspondence to Daniel Cooke, Department of Radiology, University of Washington SOM, 1959 NE Pacific St, Seattle, WA 98195, USA; dcooke{at}uw.edu

Abstract

Object Endovascular treatment of cerebral vasospasm consists primarily of transluminal balloon angioplasty (TBA) and intra-arterial (IA) vasodilator administration, the former restricted to use within the distal internal carotid and proximal intracerebral arteries. Our objective was to characterize clinical and angiographic features of those patients undergoing TBA and IA vasodilator treatments, particularly as it related to the aneurysm treatment modality.

Methods Retrospective analysis of consecutive patients admitted for aneurysmal SAH undergoing IA treatment for cerebral vasospasm (n=73) examining clinical and angiographic variables. Continuous and ordinal means were examined with Mann–Whitney and Student t tests while nominal values were examined with χ2/Fisher's exact tests. Multivariate logistic and linear regression included admission Glasgow coma scale, age, number of aneurysms and number of vasospastic vessels.

Results Those patients receiving IA vasodilator in isolation (n=16) were older (45.9 vs 59.1 years, p=0.001) and more frequently had vasospasm involving the anterior cerebral artery alone (0.0% vs 31.3%, p <0.001). The use of an IA vasodilator alone or in combination with TBA more frequently occurred in the coiled population (32.3% vs 50.1%, p=0.021).

Conclusion TBA and IA vasodilators are safe and effective means to treat cerebral vasospasm. Their use for proximal and distal vasospasm, respectively, and in tandem for diffuse disease, suggests regional differences in cerebral vasospasm between surgical clipping and endovascular coiling populations with coiled patients more often having distal vasospasm. Craniotomy and/or hemorrhagic evacuation performed during open surgery may contribute to this difference.

  • Vasospasm
  • subarachnoid hemorrhage
  • aneurysm
  • interventional radiology
  • angioplasty
  • brain
  • subarachnoid
  • aneurysm
  • hemorrhage
  • angioplasty

https://doi.org/10.1136/jnis.2009.000919

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    Introduction

    Cerebral vasospasm remains a major cause of morbidity and mortality among patients following subarachnoid hemorrhage (SAH) from ruptured intracranial aneurysms. With an estimated incidence of 6–16 per 100 000, aneurysm rupture is the etiology in approximately 5%–15% of stroke patients, with high overall mortality ranging from 30%–70%.1 Approximately 35% die before hospital arrival or within the first 24 h following aneurysm rupture.2 3 Those surviving the initial hemorrhage and after undergoing definitive aneurysm treatment, either by surgical clipping or endovascular coiling, experience the greatest morbidity and mortality as a result of cerebral vasospasm. Of patients with aneurysmal SAH, 30%–70% will develop cerebral angiographic vasospasm, with delayed neurologic deficits manifesting in 30%–50%.1 4 Vasospasm causes death or permanent disability in 12%–17% of SAH patients, and remains a central focus in clinical management in the days and weeks following hemorrhage.1 4 5

    There is controversy regarding the role aneurysm treatment, be it surgical clipping or endovascular coiling, has in the development and/or exacerbation of cerebral vasospasm. A number of series, primarily retrospective in design, have taken light to this issue with varied results.6 As great an impact as the technical advances in aneurysm treatment have had, the medical and mechanical treatments for cerebral vasospasm need also be considered. Current methods of vasospasm treatment include both medical and interventional techniques. Transluminal balloon angioplasty (TBA) and intra-arterial (IA) infusion of pharmacological vasodilators are now considered standard of care for medically refractory vasospasm.1 4 5 7 The relative performance of TBA and IA vasodilators has also been a subject of extensive study, with TBA considered the more efficacious method of treatment.4 7–16 This reflects the practice at our institution whereby TBA is used primarily save in instances of distal vasospasm or in proximal vessels that cannot be safely accessed with a microcatheter. Given the lack of data describing the complement between aneurysm and cerebral vasospasm treatments our objective was to characterize the angiographic and clinical parameters of those patients undergoing TBA and IA vasodilator treatments, particularly as it related to the aneurysm treatment modality.

    Clinical materials and methods

    Under Institutional Review Board approval we assembled a retrospective case series of all patients admitted for aneurysmal SAH between January 2005 and June 2007 to Harborview medical center (n=301) with a sub-selection of all patients undergoing IA treatment for cerebral vasospasm (n=73). Four patients were lost to follow-up. Demographic, clinical, diagnostic, treatment and complications variables were tabulated. Many patients underwent multiple IA treatments, though only the first intervention was studied and only one per patient. As we were using a clinical endpoint 6–12 months after hospital discharge, using the data from each treatment iteration in those patients receiving multiple treatments would confound our result. We did record whether a patient had single or multiple interventions as a binary variable.

    To minimize the heterogeneity of Glasgow coma scale (GCS) within the clinical records we tabulated the GCS most representative of that patient during the 24 h period 48 h after his/her intervention. We modified the raw admission and all subsequently tabulated GCSs for intubated patients with a conversion factor (((GCS−2)×1.5)+3) to more accurately reflect clinical status.17 Gale et al17 demonstrated that up to 17% of head injury patients arrive at the hospital intubated and it is common to keep patients sedated within the neurological intensive care unit (NICU) during the immediate convalescent period. Assigning a 1 for the verbal portion of the score for these patients artifactually decreases the GCS and serves as a confounder. Major complications were defined as renal failure, vascular injury, stroke or death.

    All patients were admitted by the neurosurgical service and managed within the NICU using standard triple ‘H’ therapy (hypertension, hemodilution and hypervolemia) if vasospasm was suspected clinically or by transcranial Doppler (TCD). The patients underwent daily neurological evaluation and TCD ultrasound. Single photon emission tomography (SPECT) studies were done following aneurysm or IA vasospasm treatment, deterioration in clinical exam and/or increasing evidence of vasospasm by TCD. A patient underwent digital subtraction angiography (DSA) if they met three of the following four criteria: (1) new onset neurological deficit without other known cause; (2) persistent neurological deficit despite triple ‘H’ management; (3) new or worsening vasospasm by TCD; and/or (4) new or worsening vasospasm by SPECT.

    IA intervention was performed on those patients demonstrating angiographic vasospasm and only on those vessels demonstrating vasospasm whether proximal or distal in location. All diagnostic angiograms and interventions were performed by one of three neurointerventional surgeons. Use of vasodilator, TBA or combination thereof was determined by intracranial arterial microwire accessibility and severity of disease, that is, those patients with moderate and severe vasospasm of the terminal internal carotid artery (ICA), basilar artery and first-order intracranial arterial divisions underwent TBA while those with mild vasospasm within the proximal arteries or any degree of vasospasm beyond the second-order intracranial arterial division had administration of a vasodilator. In the setting of proximal and distal vasospasm both methods were used.

    All patients undergoing IA intervention were under general anesthesia and were monitored throughout the procedure by the anesthesia service. Interventions were via femoral approach using a 6 Fr. sheath and 6 Fr. Envoy guiding catheter (Cordis Endovascular Systems, Inc., Miami Lakes, Florida, USA). For TBA patients, heparin was administered with a goal activated clotting time of 250–300s. A 4×10 mm hyperglide balloon was used primarily with occasional use of a Gateway 2 mm balloon and an 0.014 inch wire for more difficult access, often within the A1 segment. Balloons were inflated in serial increments in a distal-to-proximal direction. IA nicardipine was used as a vasodilator with doses titrated relative to blood and intracranial pressures with a maximum dose of 25 mg per ICA or 10 mg within the posterior circulation. Angiographic outcomes were measured of the vessel segment and/or distribution treated as complete (no sign of residual stenosis or attenuated perfusion), partial (decreased, though persistent stenosis or attenuated perfusion) and none (no change prior to intervention).

    Data were compiled in a spreadsheet and descriptive and analytical statistics performed with consultation of radiology and neurosurgery department statisticians using SPSS 15.0 software. To simplify comparison between diagnostic modalities, segmental arterial anatomy was reclassified into vascular distributions: anterior (ACA), middle (MCA), posterior (basilar artery and PCA), anterior and middle, anterior and posterior, middle and posterior, and all. Vasospasm affecting the ICA was classified as ‘anterior and middle’. Clinical outcomes were assessed from follow-up notes created 6–12 months after hospital discharge and measured using the modified Rankin score (mRS). Continuous and ordinal means were examined with Mann–Whitney and Student t tests while nominal values were examined with χ2/Fisher's exact tests. Multivariate logistic and linear regression included admission GCS, age, number of aneurysms and number of vasospastic vessels.

    Results

    The patient population (table 1) demonstrated slight female preponderance with most patients affected within the fifth and sixth decades of life.

    View this table:
    Table 1

    General descriptive statistics of retrospective cohort

    SAH hemorrhage was severe in most patients, reflected by mean admission GCS (11.3), Fisher grades (3.5) and Hunt and Hess scores (2.9). Nine deaths occurred during initial hospitalization, though none as result of complication from studied IA interventions. Univariate and multivariate predictors of mRS (table 2) demonstrated significant Pearson correlation between admission GCS, Hunt and Hess, and Fisher scores with admission GCS demonstrating the most statistically significant association as a predictor among the three.

    View this table:
    Table 2

    Predictors of modified Rankin score at 6–12 months after hospitalization

    A relatively greater number of aneurysms also proved a statistically significant predictor of mRS. Trends were noted with predicting worse mRSs in patients >60 years of age and those undergoing multiple IA interventions. Those patients undergoing surgical clipping had better outcomes (p=0.012), though this effect disappeared with multivariate regression analysis. The coiled population (n=27) presented with more severe disease (admission GCS of 9.4±4.0 vs 12.5±3.3, p=0.001) and worse clinical outcomes (mRS of 2.8±2.1 vs 1.9±1.6, p=0.056) relative to their clipped (n=33) counterparts (table 3).

    View this table:
    Table 3

    Aneurysm treatment

    Those within the clipped population more often underwent TBA as their sole modality of IA therapy (p=0.021) an affect that was unchanged in logistic regression analysis controlling for age, the lone additional variable that proved a statistically significant predictor of TBA or IA vasodilator use (p=0.025, p=0.002). Reciprocally, the use of an IA vasodilator alone or in combination with TBA more frequently occurred in the coiled population (p=0.021) while the overall use of TBA was not significantly different between the groups (p=0.365). Admission GCS, Fisher scale, and Hunt and Hess score were not significant predictors of the use of TBA or IA vasodilator use. The combined group (n=5) had more aneurysms (p<0.001), worse outcomes (p=0.006), shorter length of the hospital stay (p=0.043) and greater mortality (p=0.025). The majority of patients underwent TBA (n=53) whether as the solitary modality (n=31) or combined with vasodilator therapy (n=22) (table 4).

    View this table:
    Table 4

    Intra-arterial interventions

    Patients in the vasodilator group (n=16) were older (p=0.001), had fewer vasospastic vessels (p<0.001) and more frequently had vasospasm involving the anterior cerebral artery alone (p<0.001). They also manifested higher mRSs (2.6±2.3) vs the TBA group (2.1±1.7) despite similar admission GCSs, though no method of IA intervention or degree of response as measured by DSA proved a statistically significant predictor of mRS. Those patients in the combined group had more vasospasm (p<0.001) and tended to have lower admission GCSs (10.6±4.1) and higher mRS (2.9±2.1). Multivariate analysis, controlling for admission GCS, age, aneurysm number and number of vasospastic vessels, demonstrated a higher mRS for those patients undergoing combined TBA and IA vasodilator treatments relative to IA treatment (p=0.082) or TBA (p=0.045) alone.

    There were no major complications, as defined by renal failure, vascular injury, stroke or death, in the studied interventions. Minor complications, such as groin hematoma or contrast nephropathy not necessitating dialysis were not tabulated.

    Discussion

    We demonstrated a significant difference in the use of IA vasodilators as either the solitary mode of treatment or in combination with TBA between surgical clipping and endovascular coiling populations with vasodilator administration being associated more frequently with the latter despite no significant difference in the number or distribution of vasospastic vessels between treatment groups (table 3). Given our practice of using TBA within the terminal ICA, basilar and proximal segments of the intracranial arteries, and IA vasodilators for more distal vasospasm, our data suggest that coiled patients may have more distal disease. The IA treatment methods serve as indirect indicators of vasospasm distribution within an arterial division, with the TBA group reflecting proximal disease, the IA vasodilator group distal disease and the combination therapy group diffuse disease (table 4). Overall, 70% of coiled and 82% of clipped patients underwent TBA, be it as the sole modality or in combination with an IA vasodilator. A higher percentage (41% vs 21%) of those patients receiving both IA vasodilator and TBA therapies, however, had undergone coil embolization rather than surgical clipping. Given the historical association between the degree of SAH and the incidence of vasospasm we performed regression analysis controlling for Fisher score relative to the absolute use of either TBA or IA vasodilator between clipping and coiling groups and found no difference in the statistically significant increased frequency of IA vasodilator use in coiled patients. We did similar regression analyses controlling for age, Hunt and Hess score and admission GCS and again found no change in this result. This difference in vasospastic distribution may be secondary to an additional, unknown cofounder, though may be secondary to the aneurysm treatment modality. Surgical clipping may reduce distal vasospasm as a result of direct evacuation of hemorrhage or indirectly via fenestration of the lamina terminalis.18–21 The decompressive effects of craniotomy certainly contribute to reductions in intracranial pressure and in turn may also reduce distal vasospasm.18 Furthermore, the comparable use of TBA in clipped and coiled patients suggests a similar incidence of proximal vasospasm between the populations. Prior studies have demonstrated mixed effects of vessel manipulation incurred with clipping as well as with open surgery during the peak vasospasm interval, that is, 4–10 days post-initial SAH.22–27 As is the practice at our institution, the majority of patients underwent aneurysm treatment within 3 days of inciting rupture limiting the applicability of our results to the aforementioned 4–10-day interval. Additionally, our data do not suggest that vessel manipulation does not contribute to vasospasm, only that TBA use in clipped and coiled populations is similar. The etiology of that proximal vasospasm is indeterminate and may stem from physiological vasospasm and/or from an iatrogenic cause. The ability, however, to more effectively diagnose and treat the stenosis cannot be overlooked.

    The long-term sequela of a relatively greater burden of distal vasospasm is difficult to discern given the fundamental differences in the patient populations. As is the practice at many institutions, endovascular coiling is used more frequently in those patients with more severe clinical and/or hemorrhagic presentation which our data reflect.28 We found the clinical presentation the greatest determinant of a patient's eventual outcome, a variable that when controlled for accounts for the disparity between the outcomes between surgical and endovascular treatment groups (table 2).19 29 Previous work implicates hemorrhage and its degradation products in the manifestations of cerebral vasospasm and while we did not find Fisher score a statistically significant predictor of outcome it likely reflects the higher degree of hemorrhage (table 1) within the entire cohort.20 21 Furthermore, we are limited in that our retrospective cohort sampled only those patients undergoing IA treatment of some sort and cannot make comparison with a population with untreated vasospasm.

    Beyond the differences between the aneurysm treatment populations, we found that patients undergoing IA vasodilator or TBA treatment tended to have or had significantly better outcomes than those undergoing a combination of those treatments, respectively. Given the relatively lower admission GCS of those patients undergoing combined therapy this result is not surprising. We noted that despite many demographic and clinical similarities, the IA vasodilator treatment group differed from the TBA group in variables such as age and vascular distribution of cerebral vasospasm. IA vasodilators, in isolation, were used more frequently in more elderly patients and those with vasospasm affecting the ACA. The more advanced age suggests a population with greater atherosclerosis and in turn more tortuous and irregular vessels while the ACA predilection speaks to the greater technical difficulty in accessing the A1 segment. This reflects our clinical practice whereby TBA is reserved for intracranial vessels accessible with a microcatheter while vasodilators are used for more distal vasospasm making it difficult to draw firm conclusions as to the relative long-term clinical efficacy of these treatments as they are not being used interchangeably. The use of TBA, however, did demonstrate a trend toward better outcomes relative to IA vasodilator therapy, despite having similar clinical presentations and more vasospastic vessels (table 4). This may reflect the efficacy of TBA, the neurophysiological differences between ACA vs middle cerebral artery vasospasm, and/or other confounders such as age.30

    The pathophysiology of cerebral vasospasm is complex and incompletely understood. To our knowledge no data exist on how the changes initiated by SAH affect the regional course of a vessel, particularly in regard to its proximal-to-distal tapering diameter. It may be the case that vessels are affected in proportion to the duration of contact and surface area surrounded by hemorrhage, which would support the role of hemorrhagic evacuation associated with surgical clipping. It may, however, be that the ischemia and inflammation incurred with SAH affect smaller vessels differently than larger ones. How this influences clinical outcome is difficult to discern as the diagnosis of vasospasm is inextricably linked to its treatment. Certainly there are instances where proximal vasospasm cannot undergo TBA, for example, within a tortuous A1 segment, with data to support that this population does not fare as well.30 How the method of aneurysm treatment contributes to eventual long-term clinical outcomes is also unclear. As with many other studies, our data did not find a significant difference in clinical outcome between clipping and coiling populations after controlling for differences in clinical presentation.31–36 It remains uncertain what clinical significance a greater burden of distal vasospasm has on outcome. It may be that IA vasodilators successfully alleviate disease, that there are deleterious effects of surgery that offset the benefit of reduced distal vasospasm, or some other yet undefined confounding pathophysiological process. An oversimplification no doubt, but one that would be better answered with a prospective trial. Our study is certainly limited by its retrospective design and composition of only those patients undergoing IA treatment for vasospasm, reflecting a greater severity of disease. We cannot extrapolate these findings to the more general coiling and clipping populations, though our results meaningfully contribute to this controversial area and should guide subsequent inquiry.

    Conclusion

    Aneurysmal SAH-related cerebral vasospasm is complex and incompletely understood. TBA and IA vasodilators are safe and effective means in its treatment and de facto standards of care. As reflects our practice, they are used for proximal and distal vasospasm, respectively, and in tandem for diffuse disease. This specific usage profile, suggests regional differences in cerebral vasospasm between surgical clipping and endovascular coiling populations with coiled patients more often having distal vasospasm. Craniotomy and/or hemorrhagic evacuation performed during open surgery may contribute to this difference.

    Key messages

    • Vasospasm is incompletely understood and remains a major source of morbidity and mortality during the management of cerebral aneurysms.

    • Given the limited amount of data detailing the long-term clinical outcomes of patients undergoing endovascular therapy for vasospasm we aimed to describe those clinical, angiographic and treatment variables of a retrospective cohort with particular attention to the differences between clipped and coiled patients.

    • IA administration and TBA are safe methods of treatment and while they are not used interchangeably, their specific usage suggests that coiled patients incur a greater degree of vasospasm than clipped patients.

    • The etiology in differences of regional vasospasm between clipped and coiled patients is unknown, though may stem from effects of craniotomy, hemorrhagic evacuation and/or some other yet undefined surgical component.

    Acknowledgments

    The authors would like to recognize Nancy Temkin and Jason Barber for their efforts assisting with data organization and statistical analysis.

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    Footnotes

    • Portions of this work were presented in abstract form at the 5th annual meeting of the Society of Neurointerventional Surgery, Lake Tahoe, California, July 29, 2008.

    • Competing interests None.

    • Ethics approval This study was conducted with the approval of the Cerebrovascular outcomes registry. University of Washington Institutional Review Board #31833 FWA 00006878.

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