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Michael M. McDowell, Christopher P. Kellner, Sunjay M. Barton, Charles B. Mikell, Eric S. Sussman, Simon G. Heuts and E. Sander Connolly

In this report, the authors sought to summarize existing literature to provide an overview of the currently available techniques and to critically assess the evidence for or against their application in intracerebral hemorrhage (ICH) for management, prognostication, and research. Functional imaging in ICH represents a potential major step forward in the ability of physicians to assess patients suffering from this devastating illness due to the advantages over standing imaging modalities focused on general tissue structure alone, but its use is highly controversial due to the relative paucity of literature and the lack of consolidation of the predominantly small data sets that are currently in existence. Current data support that diffusion tensor imaging and tractography, diffusion-perfusion weighted MRI techniques, and functional MRI all possess major potential in the areas of highlighting motor deficits, motor recovery, and network reorganization. Novel clinical studies designed to objectively assess the value of each of these modalities on a wider scale in conjunction with other methods of investigation and management will allow for their rapid incorporation into standard practice.

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Eric S. Sussman, Christopher P. Kellner, Joanna L. Mergeche, Samuel S. Bruce, Michael M. McDowell, Eric J. Heyer and E. Sander Connolly

Object

Approximately 25% of patients exhibit cognitive dysfunction 24 hours after carotid endarterectomy (CEA). One of the purported mechanisms of early cognitive dysfunction (eCD) is hypoperfusion due to inadequate collateral circulation during cross-clamping of the carotid artery. The authors assessed whether poor collateral circulation within the circle of Willis, as determined by preoperative CT angiography (CTA) or MR angiography (MRA), could predict eCD.

Methods

Patients who underwent CEA after preoperative MRA or CTA imaging and full neuropsychometric evaluation were included in this study (n = 42); 4 patients were excluded due to intraoperative electroencephalographic changes and subsequent shunt placement. Thirty-eight patients were included in the statistical analyses. Patients were stratified according to posterior communicating artery (PCoA) status (radiographic visualization of at least 1 PCoA vs of no PCoAs). Variables with p < 0.20 in univariate analyses were included in a stepwise multivariate logistic regression model to identify predictors of eCD after CEA.

Results

Overall, 23.7% of patients exhibited eCD. In the final multivariate logistic regression model, radiographic absence of both PCoAs was the only independent predictor of eCD (OR 9.64, 95% CI 1.43–64.92, p = 0.02).

Conclusions

The absence of both PCoAs on preoperative radiographic imaging is predictive of eCD after CEA. This finding supports the evidence for an underlying ischemic etiology of eCD. Larger studies are justified to verify the findings of this study. Clinical trial registration no.: NCT00597883 (http://www.clinicaltrials.gov).

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Eric S. Sussman, Christopher P. Kellner, Eric Nelson, Michael M. McDowell, Samuel S. Bruce, Rachel A. Bruce, Zong Zhuang and E. Sander Connolly Jr.

Object

Ventriculostomy—the placement of an external ventricular drain (EVD)—is a common procedure performed in patients with acute neurological injury. Although generally considered a low-risk intervention, recent studies have cited higher rates of hemorrhagic complications than those previously reported. The authors sought to determine the rate of postventriculostomy hemorrhage in a cohort of patients with intracerebral hemorrhage (ICH) and to identify predictors of hemorrhagic complications of EVD placement.

Methods

Patients with ICH who underwent EVD placement and had both pre- and postprocedural imaging available for analysis were included in this study. Relevant data were prospectively collected for each patient who satisfied inclusion criteria. Variables with a p < 0.20 on univariate analyses were included in a stepwise logistic regression model to identify predictors of postventriculostomy hemorrhage.

Results

Sixty-nine patients were eligible for this analysis. Postventriculostomy hemorrhage occurred in 31.9% of patients. Among all patients with intraparenchymal hemorrhage, the mean hemorrhage volume was 0.66 ± 1.06 cm3. Stratified according to ventricular catheter diameter, patients treated with smaller-diameter catheters had a significantly greater mean hemorrhage volume than patients treated with larger-diameter catheters (0.84 ± 1.2 cm3 vs 0.14 ± 0.12 cm3, p = 0.049). Postventriculostomy hemorrhage was clinically significant in only 1 patient (1.4%). Overall, postventriculostomy hemorrhage was not associated with functional outcome or mortality at either discharge or 90 days. In the multivariate model, an age > 75 years was the only independent predictor of EVD-associated hemorrhage.

Conclusions

Advanced age is predictive of EVD-related hemorrhage in patients with ICH. While postventriculostomy hemorrhage is common, it appears to be of minor clinical significance in the majority of patients.

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Michael M. McDowell, Yin Zhao, Christopher P. Kellner, Sunjay M. Barton, Eric Sussman, Jan Claassen, Andrew F. Ducruet and E. Sander Connolly

OBJECTIVE

Pathophysiological differences that underlie the development and subsequent growth of multiple aneurysms may exist. In this study, the authors assessed the factors associated with the occurrence of multiple aneurysms in patients presenting with aneurysmal subarachnoid hemorrhage (SAH).

METHODS

Consecutive patients presenting with aneurysmal SAH between 1996 and 2012 were prospectively enrolled in the Subarachnoid Hemorrhage Outcome Project. Patients harboring 1, 2, or 3 or more aneurysms were stratified into groups, and the clinical and radiological characteristics of each group were compared using multivariate logistic regression.

RESULTS

Of 1277 patients with ruptured intracranial aneurysms, 890 had 1 aneurysm, 267 had 2 aneurysms, and 120 had 3 or more aneurysms. On multinomial regression using the single-aneurysm cohort as base case, risk factors for patients presenting with 2 aneurysms were female sex (relative risk ratio [RRR] 1.80, p < 0.001), higher body mass index (BMI) (RRR 1.02, p = 0.003), more years of smoking (RRR = 1.01, p = 0.004), and black race (RRR 1.83, p = 0.001). The risk factors for patients presenting with 3 or more aneurysms were female sex (RRR 3.10, p < 0.001), higher BMI (RRR 1.03, p < 0.001), aneurysm in the posterior circulation (RRR 2.59, p < 0.001), and black race (RRR 2.15, p = 0.001). Female sex, longer smoking history, aneurysms in the posterior circulation, BMI, and black race were independently associated with the development of multiple aneurysms in our adjusted multivariate multinomial model.

CONCLUSIONS

Significant demographic and clinical differences are found between patients presenting with single and multiple aneurysms in the setting of aneurysmal SAH. These predictors of multiple aneurysms likely reflect a predisposition toward inflammation and endothelial injury.

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Christopher P. Kellner, Michael M. McDowell, Michelle Q. Phan, E. Sander Connolly, Sean D. Lavine, Philip M. Meyers, Daniel Sahlein, Robert A. Solomon, Neil A. Feldstein and Richard C.E. Anderson

Object

The significance of draining vein anatomy is poorly defined in pediatric arteriovenous malformations (AVMs). In adult cohorts, the presence of fewer veins has been shown to lead to an increased rate of hemorrhage, but this phenomenon has not yet been studied in pediatric AVMs. This report analyzes the impact of draining vein anatomy on presentation and outcome in a large series of pediatric AVMs.

Methods

Eighty-five pediatric patients with AVMs were treated at the Columbia University Medical Center between 1991 and 2012. Charts were retrospectively reviewed for patient characteristics, clinical course, neurological outcome, and AVM angioarchitectural features identified on the angiogram performed at presentation. Univariate analyses were performed using chi-square test and ANOVA when appropriate; multivariate analysis was performed using logistic regression.

Results

Four patients were excluded due to incomplete records. Twenty-seven patients had 2 or 3 draining veins; 12 (44.4%) of these patients suffered from hemorrhage prior to surgery. Fifty-four patients had 1 draining vein; 39 (72.2%) of these 54 suffered from hemorrhage. Independent predictors of hemorrhage included the presence of a single draining vein (p = 0.04) and deep venous drainage (p = 0.02). Good outcome (modified Rankin Scale [mRS] score < 3) on discharge was found to be associated with higher admission Glasgow Coma Scale (GCS) scores (p = 0.0001, OR 0.638, 95% CI 0.40–0.93). Poor outcome (mRS score > 2) on discharge was found to be associated with deep venous drainage (p = 0.04, OR 4.68, 95% CI 1.1–19.98). A higher admission GCS score was associated with a lower discharge mRS score (p = 0.0003, OR 0.6, 95% CI 0.46–0.79), and the presence of a single draining vein was associated with a lower mRS score on long-term follow-up (p = 0.04, OR 0.18, 95% CI 0.032–0.99).

Conclusions

The authors' data suggest that the presence of a single draining vein or deep venous drainage plays a role in hemorrhage risk and ultimate outcome in pediatric AVMs. Small AVMs with a single or deep draining vein may have the highest risk of hemorrhage.

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Eric S. Sussman, Christopher P. Kellner, Michael M. McDowell, Samuel S. Bruce, Simon G. Heuts, Zong Zhuang, Rachel A. Bruce, Jan Claassen and E. Sander Connolly Jr.

Intracerebral hemorrhage (ICH) is the most deadly and least treatable subtype of stroke, and at the present time there are no evidence-based therapeutic interventions for patients with this disease. Secondary injury mechanisms are known to cause substantial rates of morbidity and mortality following ICH, and the inflammatory cascade is a major contributor to this post-ICH secondary injury. The alpha-7 nicotinic acetylcholine receptor (α7-nAChR) agonists have a well-established antiinflammatory effect and have been shown to attenuate perihematomal edema volume and to improve functional outcome in experimental ICH. The authors evaluate the current evidence for the use of an α7-nAChR agonist as a novel therapeutic agent in patients with ICH.

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Simon G. Heuts, Samuel S. Bruce, Brad E. Zacharia, Zachary L. Hickman, Christopher P. Kellner, Eric S. Sussman, Michael M. McDowell, Rachel A. Bruce and E. Sander Connolly Jr.

Object

Large intracerebral hemorrhage (ICH), compounded by perihematomal edema, can produce severe elevations of intracranial pressure (ICP). Decompressive hemicraniectomy (DHC) with or without clot evacuation has been considered a part of the armamentarium of treatment options for these patients. The authors sought to assess the preliminary utility of DHC without evacuation for ICH in patients with supratentorial, dominant-sided lesions.

Methods

From September 2009 to May 2012, patients with ICH who were admitted to the neurological ICU at Columbia University Medical Center were prospectively enrolled in that institution's ICH Outcomes Project (ICHOP). Five patients with spontaneous supratentorial dominant-sided ICH underwent DHC without clot evacuation for recalcitrant elevated ICP. Data pertaining to the patients' characteristics and outcomes of treatment were prospectively collected.

Results

The patients' median age was 43 years (range 30–55 years) and the ICH etiology was hypertension in 4 of 5 patients, and systemic lupus erythematosus vasculitis in 1 patient. On admission, the median Glasgow Coma Scale (GCS) score was 7 (range 5–9). The median ICH volume was 53 cm3 (range 28–79 cm3), and the median midline shift was 7.6 mm (range 3.0–11.3 mm). One day after surgery, the median decrease in midline shift was 2.7 mm (range 1.5–4.6 mm), and the median change in GCS score was +1 (range −3 to +5). At discharge, all patients were still alive, and the median GCS score was 10 (range 9–11), the median modified Rankin Scale (mRS) score was 5 (range 5–5), and the median NIHSS (National Institutes of Health Stroke Scale) score was 22 (range 17–27). Six months after hemorrhage, 1 patient had died, 2 were functionally dependent (mRS Score 4–5), and 2 were functionally independent (mRS Score 0–3). Outcomes for the patients treated with DHC were good compared with 1) outcomes for all patients with spontaneous supratentorial ICH admitted during the same period (n = 144) and 2) outcomes for matched patients (dominant ICH, GCS Score 5–9, ICH volume 28–79 cm3, age < 60 years) whose cases were managed nonoperatively (n = 5).

Conclusions

Decompressive hemicraniectomy without clot evacuation appears feasible in patients with large ICH and deserves further investigation, preferably in a randomized controlled setting.

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Brian Y. Hwang, Samuel S. Bruce, Geoffrey Appelboom, Matthew A. Piazza, Amanda M. Carpenter, Paul R. Gigante, Christopher P. Kellner, Andrew F. Ducruet, Michael A. Kellner, Rajeev Deb-Sen, Kerry A. Vaughan, Philip M. Meyers and E. Sander Connolly Jr.

Object

Intraventricular hemorrhage (IVH) associated with intracerebral hemorrhage (ICH) is an independent predictor of poor outcome. Clinical methods for evaluating IVH, however, are not well established. This study sought to determine the best IVH grading scale by evaluating the predictive accuracies of IVH, Graeb, and LeRoux scores in an independent cohort of ICH patients with IVH. Subacute IVH dynamics as well as the impact of external ventricular drain (EVD) placement on IVH and outcome were also investigated.

Methods

A consecutive cohort of 142 primary ICH patients with IVH was admitted to Columbia University Medical Center between February 2009 and February 2011. Baseline demographics, clinical presentation, and hospital course were prospectively recorded. Admission CT scans performed within 24 hours of onset were reviewed for ICH location, hematoma volume, and presence of IVH. Intraventricular hemorrhage was categorized according to IVH, Graeb, and LeRoux scores. For each patient, the last scan performed within 6 days of ictus was similarly evaluated. Outcomes at discharge were assessed using the modified Rankin Scale (mRS). Receiver operating characteristic analysis was used to determine the predictive accuracies of the grading scales for poor outcome (mRS score ≥ 3).

Results

Seventy-three primary ICH patients (51%) had IVH. Median admission IVH, Graeb, and LeRoux scores were 13, 6, and 8, respectively. Median IVH, Graeb and LeRoux scores decreased to 9 (p = 0.005), 4 (p = 0.002), and 4 (p = 0.003), respectively, within 6 days of ictus. Poor outcome was noted in 55 patients (75%). Areas under the receiver operating characteristic curve were similar among the IVH, Graeb, and LeRoux scores (0.745, 0.743, and 0.744, respectively) and within 6 days postictus (0.765, 0.722, 0.723, respectively). Moreover, the IVH, Graeb, and LeRoux scores had similar maximum Youden Indices both at admission (0.515 vs 0.477 vs 0.440, respectively) and within 6 days postictus (0.515 vs 0.339 vs 0.365, respectively). Patients who received EVDs had higher mean IVH volumes (23 ± 26 ml vs 9 ± 11 ml, p = 0.003) and increased incidence of Glasgow Coma Scale scores < 8 (67% vs 38%, p = 0.015) and hydrocephalus (82% vs 50%, p = 0.004) at admission but had similar outcome as those who did not receive an EVD.

Conclusions

The IVH, Graeb, and LeRoux scores predict outcome well with similarly good accuracy in ICH patients with IVH when assessed at admission and within 6 days after hemorrhage. Therefore, any of one of the scores would be equally useful for assessing IVH severity and risk-stratifying ICH patients with regard to outcome. These results suggest that EVD placement may be beneficial for patients with severe IVH, who have particularly poor prognosis at admission, but a randomized clinical trial is needed to conclusively demonstrate its therapeutic value.

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Richard C. E. Anderson, Michael M. McDowell, Christopher P. Kellner, Geoffrey Appelboom, Samuel S. Bruce, Ivan S. Kotchetkov, Raqeeb Haque, Neil A. Feldstein, E. Sander Connolly Jr., Robert A. Solomon, Philip M. Meyers and Sean D. Lavine

Object

Conventional cerebral angiography and treatment for ruptured arteriovenous malformations (AVMs) in children are often performed in a delayed fashion. In adults, current literature suggests that AVM-associated aneurysms may be more likely to hemorrhage than isolated AVMs, which often leads to earlier angiography and endovascular treatment of associated aneurysms. The nature of AVM-associated aneurysms in the pediatric population is virtually unknown. In this report, the authors investigate the relationship of associated aneurysms in a large group of children with AVMs.

Methods

Seventy-seven pediatric patients (≤ 21 years old) with AVMs were treated at the Columbia University Medical Center between 1991 and 2010. Medical records and imaging studies were retrospectively reviewed, and associated aneurysms were classified as arterial, intranidal, or venous in location. Clinical presentation and outcome variables were compared between children with and without AVM-associated aneurysms.

Results

A total of 30 AVM-associated aneurysms were found in 22 children (29% incidence). Eleven were arterial, 9 intranidal, and 10 were venous in location. There was no significant difference in the rate of hemorrhage (p = 0.91) between children with isolated AVMs (35 of 55 [64%]) and children with AVM-associated aneurysms (13 of 22 [59%]). However, of the 11 children with AVM-associated aneurysms in an arterial location, 10 presented with hemorrhage (91%). An association with hemorrhage was significant in univariate analysis (p = 0.045) but not in multivariate analysis (p = 0.37).

Conclusions

Associated aneurysms are present in nearly a third of children with AVMs, and when arterially located, are more likely to present with hemorrhage. These data suggest that early angiography with endovascular treatment of arterial-based aneurysms in children with AVMs may be indicated.

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Grace H. Kim, Christopher P. Kellner, David K. Hahn, Brianna M. Desantis, Muhith Musabbir, Robert M. Starke, Michal Rynkowski, Ricardo J. Komotar, Marc L. Otten, Robert Sciacca, J. Michael Schmidt, Stephan A. Mayer and E. Sander Connolly Jr.

Object

Despite efforts to elucidate both the molecular mechanism and the clinical predictors of vasospasm after aneurysmal subarachnoid hemorrhage (ASAH), its pathogenesis remains unclear. Monocyte chemoattractant protein–1 (MCP-1) is a chemokine that has been firmly implicated in the pathophysiology of vasospasm and in neural tissue injury following focal ischemia in both animal models and human studies. The authors hypothesized that MCP-1 would be found in increased concentrations in the blood and cerebrospinal fluid (CSF) of patients with ASAH and would correlate with both outcome and the occurrence of vasospasm.

Methods

Seventy-seven patients who presented with ASAH were prospectively enrolled in this study between July 2001 and May 2002. Using an enzyme-linked immunosorbent assay, MCP-1 levels were measured in serum daily and in CSF when available. The mean serum and CSF MCP-1 concentrations were calculated for each patient throughout the entire hospital stay. Neurological outcome was evaluated at discharge or 14 days posthemorrhage using the modified Rankin Scale. Vasospasm was evaluated on angiography.

Results

The serum MCP-1 concentrations correlated with negative outcome such that a 10% increase in concentration predicted a 25% increase in the probability of a poor outcome, whereas the serum MCP-1 levels did not correlate with vasospasm. Concentrations of MCP-1 in the CSF, however, proved to be significantly higher in patients with angiographically demonstrated vasospasm.

Conclusions

These findings suggest a role for MCP-1 in neurological injury and imply that it may act as a biomarker of poor outcome in the serum and of vasospasm in the CSF.