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Anthony Wan, Blessing N. R. Jaja, Tom A. Schweizer and R. Loch Macdonald

OBJECTIVE

Intracerebral hematoma (ICH) with subarachnoid hemorrhage (SAH) indicates a unique feature of intracranial aneurysm rupture since the aneurysm is in the subarachnoid space and separated from the brain by pia mater. Broad consensus is lacking regarding the concept that ultra-early treatment improves outcome. The aim of this study is to determine the associative factors for ICH, ascertain the prognostic value of ICH, and investigate how the timing of treatment relates to the outcome of SAH with concurrent ICH.

METHODS

The study data were pooled from the SAH International Trialists repository. Logistic regression was applied to study the associations of clinical and aneurysm characteristics with ICH. Proportional odds models and dominance analysis were applied to study the effect of ICH on 3-month outcome (Glasgow Outcome Scale) and investigate the effect of time from ictus to treatment on outcome.

RESULTS

Of the 5362 SAH patients analyzed, 1120 (21%) had concurrent ICH. In order of importance, neurological status, aneurysm location, aneurysm size, and patient ethnicity were significantly associated with ICH. Patients with ICH experienced poorer outcome than those without ICH (OR 1.58; 95% CI 1.37–1.82). Treatment within 6 hours of SAH was associated with poorer outcome than treatment thereafter (adjusted OR 1.67; 95% CI 1.04–2.69). Subgroup analysis with adjustment for ICH volume, location, and midline shift resulted in no association between time from ictus to treatment and outcome (OR 0.99; 95% CI 0.94–1.07).

CONCLUSIONS

The most important associative factor for ICH is neurological status on admission. The finding regarding the value of ultra-early treatment suggests the need to more robustly reevaluate the concept that hematoma evacuation of an ICH and repair of a ruptured aneurysm within 6 hours of ictus is the most optimal treatment path.

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Peter Egeto, R. Loch Macdonald, Tisha J. Ornstein and Tom A. Schweizer

OBJECTIVE

Subarachnoid hemorrhage (SAH) is treated with either surgical clipping or endovascular coiling, though the latter is the preferred treatment method given its more favorable functional outcomes. However, neuropsychological functioning after treatment is rarely taken into account. In this meta-analysis, the authors synthesized relevant data from the literature and compared neuropsychological functioning in patients after coiling and clipping of SAH. They hypothesized that the coiled patients would outperform the clipped patients; that group differences would be greater with higher posterior circulation rupture rates, in older patients, and in more recent publications; that group differences would be smaller with greater rates of middle cerebral artery (MCA) rupture; and that anterior communicating artery (ACoA) rupture rates would not influence effect sizes.

METHODS

The MEDLINE, Embase, and PsycINFO databases were searched for clinical studies that compared neuropsychological functioning after either endovascular coiling or surgical clipping for SAH. Hedge's g and 95% confidence intervals were calculated using random effects models. Patients who had undergone coiling or clipping were compared on test performance in 8 neuropsychological domains: executive functions, language, attention/processing speed, verbal memory, visual memory, spatial memory, visuospatial functions, and intelligence. Patients were also compared with healthy controls, and meta-regressions were used to explore the relation between effect sizes and publication year, delay between treatment and neuropsychological testing, mean patient age, and rates of posterior circulation, ACoA, and MCA ruptures.

RESULTS

Thirteen studies with 396 clipped cases, 314 coiled cases, and 169 healthy controls were included in the study. The coil-treated patients outperformed the clip-treated patients on executive function (g = 0.17, 95% CI 0.08–0.25) and language tests (g = 0.23, 95% CI 0.07–0.39), and all patients were impaired relative to healthy controls (g ranged from −0.93 to −0.29). Coiled patients outperformed clipped patients to a greater degree in more recent publications, over longer posttreatment testing delays, and among older patients. Higher rates of posterior circulation and MCA aneurysms were associated with smaller group differences, while ACoA rupture rates did not influence effect sizes.

CONCLUSIONS

Coiling of SAH may promote superior neuropsychological functioning under certain circumstances and could have applications for the specialized care of SAH patients.

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Alan K. H. Tam, Anish Kapadia, Don Ilodigwe, Zeyu Li, Tom A. Schweizer and R. Loch Macdonald

Object

Atrophy in specific brain areas correlates with poor neuropsychological outcome after subarachnoid hemorrhage (SAH). Few studies have compared global atrophy in SAH with outcome. The authors examined the relationship between global brain atrophy, clinical factors, and outcome after SAH.

Methods

This study was a post hoc exploratory analysis of the Clazosentan to Overcome Neurological Ischemia and Infarction Occurring After Subarachnoid Hemorrhage (CONSCIOUS-1) trial, a randomized, double-blind, placebo-controlled trial of 413 patients with aneurysmal SAH. Patients with infarctions or areas of encephalomalacia on CT, and those with large clip/coil artifacts, were excluded. The 97 remaining patients underwent CT at baseline and 6 weeks, which was analyzed using voxel-based volumetric measurements. The percentage difference in volume between time points was compared against clinical variables. The relationship with clinical outcome was modeled using univariate and multivariate analysis.

Results

Older age, male sex, and systemic inflammatory response syndrome (SIRS) during intensive care stay were significantly associated with brain atrophy. Greater brain atrophy was significantly associated with poor outcome on the modified Rankin scale (mRS), severity of deficits on the National Institutes of Health Stroke Scale (NIHSS), worse executive functioning, and lower EuroQol Group–5D (EQ-5D) score. Adjusted for confounders, brain atrophy was not significantly associated with Mini-Mental State Examination and Functional Status Examination scores. Brain atrophy was not associated with angiographic vasospasm or delayed ischemic neurological deficit.

Conclusions

Worse mRS score, NIHSS score, executive functioning, and EQ-5D scores were associated with greater brain atrophy and older age, male sex, and SIRS burden. These data suggest outcome is associated with factors that cause global brain injury independent of focal brain injury.

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Michael J. Bonares, Peter Egeto, Airton Leonardo de Oliveira Manoel, Kristin A. Vesely, R. Loch Macdonald and Tom A. Schweizer

OBJECT

The treatment of an unruptured intracranial aneurysm (UIA) is not free of morbidity and mortality, and the decision is made by weighing the risks of treatment complications against the risk of aneurysm rupture. This meta-analysis quantitatively analyzed the literature on the effects of UIA treatment on cognition.

METHODS

MEDLINE, Embase, and PsycInfo were systematically searched for studies that reported on the cognitive status of UIA patients before and after aneurysm treatment. The search was restricted to prospective cohort and case-control studies published between January 1, 1998, and January 1, 2013. The analyses focused on the effect of treatment on general cognitive functioning, with an emphasis on 4 specific cognitive domains: executive functions, verbal and visual memory, and visuospatial functions.

RESULTS

Eight studies, with a total of 281 patients, were included in the meta-analysis. Treatment did not affect general cognitive functioning (effect size [ES] −0.22 [95% CI −0.78 to 0.34]). Executive functions and verbal memory domains trended toward posttreatment impairment (ES −0.46 [95% CI −0.93 to 0.01] and ES −0.31 [95% CI −1.24 to 0.61]), and performance of visual memory tasks trended toward posttreatment improvement (ES 1.48 [95% CI −0.36 to 3.31]). Lastly, treatment did not significantly affect visuospatial functions (ES −0.08 [95% CI −0.30 to 0.45]).

CONCLUSIONS

The treatment of an UIA does not seem to affect long-term cognitive function. However, definitive conclusions were not possible due to the paucity of studies addressing this issue.

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Blessing N. R. Jaja, Hester Lingsma, Ewout W. Steyerberg, Tom A. Schweizer, Kevin E. Thorpe and R. Loch Macdonald

OBJECT

Neuroimaging characteristics of ruptured aneurysms are important to guide treatment selection, and they have been studied for their value as outcome predictors following aneurysmal subarachnoid hemorrhage (SAH). Despite multiple studies, the prognostic value of aneurysm diameter, location, and extravasated SAH clot on computed tomography scan remains debatable. The authors aimed to more precisely ascertain the relation of these factors to outcome.

METHODS

The data sets of studies included in the Subarachnoid Hemorrhage International Trialists (SAHIT) repository were analyzed including data on ruptured aneurysm location and diameter (7 studies, n = 9125) and on subarachnoid clot graded on the Fisher scale (8 studies; n = 9452) for the relation to outcome on the Glasgow Outcome Scale (GOS) at 3 months. Prognostic strength was quantified by fitting proportional odds logistic regression models. Univariable odds ratios (ORs) were pooled across studies using random effects models. Multivariable analyses were adjusted for fixed effect of study, age, neurological status on admission, other neuroimaging factors, and treatment modality. The neuroimaging predictors were assessed for their added incremental predictive value measured as partial R2.

RESULTS

Spline plots indicated outcomes were worse at extremes of aneurysm size, i.e., less than 4 or greater than 9 mm. In between, aneurysm size had no effect on outcome (OR 1.03, 95% CI 0.98–1.09 for 9 mm vs 4 mm, i.e., 75th vs 25th percentile), except in those who were treated conservatively (OR 1.17, 95% CI 1.02–1.35). Compared with anterior cerebral artery aneurysms, posterior circulation aneurysms tended to result in slightly poorer outcome in patients who underwent endovascular coil embolization (OR 1.13, 95% CI 0.82–1.57) or surgical clipping (OR 1.32, 95% CI 1.10–1.57); the relation was statistically significant only in the latter. Fisher CT subarachnoid clot burden was related to outcome in a gradient manner. Each of the studied predictors accounted for less than 1% of the explained variance in outcome.

CONCLUSIONS

This study, which is based on the largest cohort of patients so far analyzed, has more precisely determined the prognostic value of the studied neuroimaging factors. Treatment choice has strong influence on the prognostic effect of aneurysm size and location. These findings should guide the development of reliable prognostic models and inform the design and analysis of future prospective studies, including clinical trials.

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Blessing N. R. Jaja, Hester Lingsma, Tom A. Schweizer, Kevin E. Thorpe, Ewout W. Steyerberg and R. Loch Macdonald

OBJECT

The literature has conflicting reports about the prognostic value of premorbid hypertension and neurological status in aneurysmal subarachnoid hemorrhage (SAH). The aim of this study was to investigate the prognostic value of premorbid hypertension and neurological status in the SAH International Trialists repository.

METHODS

Patient-level meta-analyses were conducted to investigate univariate associations between premorbid hypertension (6 studies; n = 7249), admission neurological status measured on the World Federation of Neurosurgical Societies (WFNS) scale (10 studies; n = 10,869), and 3-month Glasgow Outcome Scale (GOS) score. Multivariable analyses were performed to sequentially adjust for the effects of age, CT clot burden, aneurysm location, aneurysm size, and modality of aneurysm repair. Prognostic associations were estimated across the ordered categories of the GOS using proportional odds models. Nagelkerke's R2 statistic was used to quantify the added prognostic value of hypertension and neurological status beyond those of the adjustment factors.

RESULTS

Premorbid hypertension was independently associated with poor outcome, with an unadjusted pooled odds ratio (OR) of 1.73 (95% confidence interval [CI] 1.50–2.00) and an adjusted OR of 1.38 (95% CI 1.25–1.53). Patients with a premorbid history of hypertension had higher rates of cardiovascular and renal comorbidities, poorer neurological status (p ≤ 0.001), and higher odds of neurological complications including cerebral infarctions, hydrocephalus, rebleeding, and delayed ischemic neurological deficits. Worsening neurological status was strongly independently associated with poor outcome, including WFNS Grades II (OR 1.85, 95% CI 1.68–2.03), III (OR 3.85, 95% CI 3.32–4.47), IV (OR 5.58, 95% CI 4.91–6.35), and V (OR 14.18, 95% CI 12.20–16.49). Neurological status had substantial added predictive value greater than the combined value of other prognostic factors (R2 increase > 10%), while the added predictive value of hypertension was marginal (R2 increase < 0.5%).

CONCLUSIONS

This study confirmed the strong prognostic effect of neurological status as measured on the WFNS scale and the independent but weak prognostic effect of premorbid hypertension. The effect of premorbid hypertension could involve multifactorial mechanisms, including an increase in the severity of initial bleeding, the rate of comorbid events, and neurological complications.

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Melanie A. Morrison, Fred Tam, Marco M. Garavaglia, Laleh Golestanirad, Gregory M. T. Hare, Michael D. Cusimano, Tom A. Schweizer, Sunit Das and Simon J. Graham

A computerized platform has been developed to enhance behavioral testing during intraoperative language mapping in awake craniotomy procedures. The system is uniquely compatible with the environmental demands of both the operating room and preoperative functional MRI (fMRI), thus providing standardized testing toward improving spatial agreement between the 2 brain mapping techniques. Details of the platform architecture, its advantages over traditional testing methods, and its use for language mapping are described. Four illustrative cases demonstrate the efficacy of using the testing platform to administer sophisticated language paradigms, and the spatial agreement between intraoperative mapping and preoperative fMRI results. The testing platform substantially improved the ability of the surgeon to detect and characterize language deficits. Use of a written word generation task to assess language production helped confirm areas of speech apraxia and speech arrest that were inadequately characterized or missed with the use of traditional paradigms, respectively. Preoperative fMRI of the analogous writing task was also assistive, displaying excellent spatial agreement with intraoperative mapping in all 4 cases. Sole use of traditional testing paradigms can be limiting during awake craniotomy procedures. Comprehensive assessment of language function will require additional use of more sophisticated and ecologically valid testing paradigms. The platform presented here provides a means to do so.

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Naif M. Alotaibi, Justin Z. Wang, Christopher R. Pasarikovski, Daipayan Guha, Fawaz Al-Mufti, Muhammad Mamdani, Gustavo Saposnik, Tom A. Schweizer and R. Loch Macdonald

Elevated intracranial pressure (ICP) is a well-recognized phenomenon in aneurysmal subarachnoid hemorrhage (aSAH) that has been demonstrated to lead to poor outcomes. Despite significant advances in clinical research into aSAH, there are no consensus guidelines devoted specifically to the management of elevated ICP in the setting of aSAH. To treat high ICP in aSAH, most centers extrapolate their treatment algorithms from studies and published guidelines for traumatic brain injury. Herein, the authors review the current management strategies for treating raised ICP within the aSAH population, emphasize key differences from the traumatic brain injury population, and highlight potential directions for future research in this controversial topic.

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Blessing N. R. Jaja, Gustavo Saposnik, Rosane Nisenbaum, Benjamin W. Y. Lo, Tom A. Schweizer, Kevin E. Thorpe and R. Loch Macdonald

Object

The goal of this study was to determine racial/ethnic differences in inpatient mortality rates and the use of institutional postacute care following subarachnoid hemorrhage (SAH) in the US.

Methods

A cross-sectional study of hospital discharges for SAH was conducted using the Nationwide Inpatient Sample for the years 2005–2010. Discharges with a principal diagnosis of SAH were identified and abstracted using the appropriate ICD-9-CM diagnostic code. Racial/ethnic groups were defined as white, black, Hispanic, Asian/Pacific Islander (API), and American Indian. Multinomial logistic regression analyses were performed comparing racial/ethnic groups with respect to the primary outcome of risk of in-hospital mortality and the secondary outcome of likelihood of discharge to institutional care.

Results

During the study period, 31,631 discharges were related to SAH. Race/ethnicity was a significant predictor of death (p = 0.003) and discharge to institutional care (p ≤ 0.001). In the adjusted analysis, compared with white patients, API patients were at higher risk of death (OR 1.34, 95% CI 1.13–1.59) and Hispanic patients were at lower risk of death (OR 0.84, 95% CI 0.72–0.97). The likelihood of discharge to institutional care was statistically similar between white, Hispanic, API, and Native American patients. Black patients were more likely to be discharged to institutional care compared with white patients (OR 1.27, 95% CI 1.14–1.40), but were similar to white patients in the risk of death.

Conclusions

Significant racial/ethnic differences are present in the risk of inpatient mortality and discharge to institutional care among patients with SAH in the US. Outcome is likely to be poor among API patients and best among Hispanic patients compared with other groups.

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Simone A. Dijkland, Blessing N. R. Jaja, Mathieu van der Jagt, Bob Roozenbeek, Mervyn D. I. Vergouwen, Jose I. Suarez, James C. Torner, Michael M. Todd, Walter M. van den Bergh, Gustavo Saposnik, Daniel W. Zumofen, Michael D. Cusimano, Stephan A. Mayer, Benjamin W. Y. Lo, Ewout W. Steyerberg, Diederik W. J. Dippel, Tom A. Schweizer, R. Loch Macdonald and Hester F. Lingsma

OBJECTIVE

Differences in clinical outcomes between centers and countries may reflect variation in patient characteristics, diagnostic and therapeutic policies, or quality of care. The purpose of this study was to investigate the presence and magnitude of between-center and between-country differences in outcome after aneurysmal subarachnoid hemorrhage (aSAH).

METHODS

The authors analyzed data from 5972 aSAH patients enrolled in randomized clinical trials of 3 different treatments from the Subarachnoid Hemorrhage International Trialists (SAHIT) repository, including data from 179 centers and 20 countries. They used random effects logistic regression adjusted for patient characteristics and timing of aneurysm treatment to estimate between-center and between-country differences in unfavorable outcome, defined as a Glasgow Outcome Scale score of 1–3 (severe disability, vegetative state, or death) or modified Rankin Scale score of 4–6 (moderately severe disability, severe disability, or death) at 3 months. Between-center and between-country differences were quantified with the median odds ratio (MOR), which can be interpreted as the ratio of odds of unfavorable outcome between a typical high-risk and a typical low-risk center or country.

RESULTS

The proportion of patients with unfavorable outcome was 27% (n = 1599). The authors found substantial between-center differences (MOR 1.26, 95% CI 1.16–1.52), which could not be explained by patient characteristics and timing of aneurysm treatment (adjusted MOR 1.21, 95% CI 1.11–1.44). They observed no between-country differences (adjusted MOR 1.13, 95% CI 1.00–1.40).

CONCLUSIONS

Clinical outcomes after aSAH differ between centers. These differences could not be explained by patient characteristics or timing of aneurysm treatment. Further research is needed to confirm the presence of differences in outcome after aSAH between hospitals in more recent data and to investigate potential causes.