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Matthew C. Garrett, Ricardo J. Komotar, Maxwell B. Merkow, Robert M. Starke, Marc L. Otten and E. Sander Connolly

✓The 1985 International Extracranial–Intracranial (EC-IC) Bypass Trial failed to show a surgical benefit of EC-IC bypass in patients with varying degrees of angiographic stenosis. This study was limited by the technology available at the time it was conducted. In the 20 years since, there has been considerable progress in imaging techniques that now enable the identification of a subset of stroke patients with hemodynamic ischemia. In the present study, the authors review the relevant literature and propose a reevaluation of the benefits of the EC-IC bypass procedure using these new imaging techniques.

The authors reviewed the admission criteria for the EC-IC Bypass Trial in the light of more recently discovered neurovascular physiology and showed that the imaging criteria used in that trial are not physiologically adequate. A MED-LINE (1985–2007) database search for EC-IC case studies was conducted, and additional studies were identified manually by scrutinizing references from identified manuscripts, major neurosurgical journals and texts, and personal files.

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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.

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Robert M. Starke, Ricardo J. Komotar and E. Sander Connolly

Moyamoya disease is a chronic cerebrovascular occlusive disorder that results in severe morbidity and death. There is much controversy surrounding the optimal treatment for adult patients with the disorder. There have been no randomized trials to assess the efficacy of any single surgical treatment, and existing case series suffer from inadequate power, selection bias, and inherent differences in patient characteristics. In this article the authors review the literature concerning the optimal surgical treatment of adult patients with moyamoya disease.

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Ricardo J. Komotar, Robert M. Starke, Marc L. Otten, Maxwell B. Merkow, Matthew C. Garrett, Randolph S. Marshall, Mitchell S. V. Elkind and E. Sander Connolly Jr.

Object

The optimal treatment of medically refractory intracranial atheroocclusive disease remains unclear. The EC-IC Bypass Study Investigators found that patients with internal carotid and middle cerebral artery (ICA and MCA) occlusion received no benefit from direct superficial temporal artery to MCA bypass, and that patients with ICA occlusion and MCA stenosis may have actually fared worse after surgery, perhaps in part due to flow reversal in critical perforator-bearing segments. Although the results of recent investigations have suggested that direct bypass may be beneficial in a subgroup of patients with hemodynamic failure secondary to unilateral ICA occlusion, similar data do not exist for patients with hemodynamic failure from other intracranial stenoocclusive diseases. Indirect bypass via encephaloduroarteriosynangiosis offers a surgical alternative that may avoid rapid flow reversal while providing additional flow to at-risk, distal vascular territories.

Methods

Twelve patients with medically resistant hemodynamic failure from intracranial atheroocclusive disease underwent indirect vascular bypass. Eight patients had ICA occlusion and coexistent MCA stenosis, 1 patient had tandem ICA stenoses and MCA stenosis, 1 patient had tandem ICA and MCA occlusion, 1 patient had ICA and posterior cerebral artery occlusion and an ischemic hemisphere supplied via a proximal superficial temporal artery branch, and 1 patient had poor donor arteries and severe medical comorbidities that precluded the use of general anesthesia. Patient evaluation included clinical assessment of neurological status, CT scanning, MR imaging, digital subtraction angiography, and transcranial Doppler ultrasonography with CO2 reactivity, or SPECT with acetazolamide challenge. Patient records were reviewed and patients were interviewed for outcome assessment, including transient ischemic attack (TIA), cerebral infarction, change in cerebral perfusion, graft patency, and functional level according to the modified Rankin scale. Kaplan-Meier cumulative failure curves for the primary end point of cerebral infarction were used to compare these patients to a control group of 81 patients derived from the literature who received medical management for severe symptomatic hemodynamic failure.

Results

Eleven patients underwent encephaloduroarteriosynangiosis and 1 patient received bur holes with dural and arachnoid incisions; the mean length of follow-up was 51.2 ± 40.1 months. Five patients had decreased perfusion on follow-up despite graft patency, and 10 patients suffered new infarctions or TIAs during the follow-up period. Five patients (42%) suffered infarctions within 1 year of surgery. A meta-analysis of 4 studies of patients with symptomatic ICA occlusion and severe hemodynamic failure who underwent medical treatment revealed a new infarction rate of 30% in the first year after entry into the study. There was no significant difference between patients with severe hemodynamic failure who underwent surgery and those in the medically treated control group (log-rank test, p = 0.179).

Conclusions

The authors found that indirect bypass does not promote adequate pial collateral artery development and appears to be of limited utility in patients with symptomatic ICA or MCA stenoocclusive disease and secondary hemodynamic failure. Rates of postoperative TIAs or cerebral infarctions after indirect bypass in this patient population do not differ from previous reports in patients who received medical management only.

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Ricardo J. Komotar, David K. Hahn, Grace H. Kim, Robert M. Starke, Matthew C. Garrett, Maxwell B. Merkow, Marc L. Otten, Robert R. Sciacca and E. Sander Connolly Jr.

Object

Chronic hydrocephalus requiring shunt placement is a common complication following aneurysmal subarachnoid hemorrhage (SAH). Controversy exists over whether microsurgical fenestration of the lamina terminalis during aneurysm surgery affords a reduction in the development of shunt-dependent hydrocephalus. To resolve this debate, the authors performed a systematic review and quantitative analysis of the literature to determine the efficacy of lamina terminalis fenestration in reducing aneurysmal SAH–associated shunt-dependent hydrocephalus.

Methods

A MEDLINE (1950–2007) database search was performed using the following keywords, singly and in combination: “ventriculoperitoneal shunt,” “hydrocephalus,” “subarachnoid hemorrhage,” “aneurysm,” “fenestration,” and “lamina terminalis.” Additional studies were manually singled out by scrutinizing references from identified manuscripts, major neurosurgical journals and texts, and personal files. A recent study from the authors' institution was also incorporated into the review. Data from included studies were analyzed using the chi-square analysis and Student t-test. The Cochran-Mantel-Haenszel test was used to compare overall incidence of shunt-dependent hydrocephalus.

Results

The literature search revealed 19 studies, but only 11 were included in this review, involving 1973 patients. The fenestrated and nonfenestrated cohorts (combined from the various studies) differed significantly with regard to patient sex, age, and clinical grade as well as aneurysm location (p = 0.0065, 0.0028, 0.0003, and 0.017, respectively). The overall incidence of shunt-dependent hydrocephalus in the fenestrated cohort was 10%, as compared with 14% in the nonfenestrated cohort (p = 0.089). The relative risk of shunt-dependent hydrocephalus in the fenestrated cohort was 0.88 (95% CI 0.62–1.24).

Conclusions

This systematic review revealed no significant association between lamina terminalis fenestration and a reduced incidence of shunt-dependent hydrocephalus. The interpretation of these results, however, is restricted by unmatched cohort differences as well as other inherent study limitations. Although the overall literature supports lamina terminalis fenestration, a number of authors have questioned the technique's benefits, thus rendering its efficacy in reducing shunt-dependent hydrocephalus unclear. A well-designed, multicenter, randomized controlled trial is needed to definitively address the efficacy of this microsurgical technique.

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Robert M. Starke, Ricardo J. Komotar, Zachary L. Hickman, Yehuda E. Paz, Angela G. Pugliese, Marc L. Otten, Matthew C. Garrett, Mitchell S. V. Elkind, Randolph S. Marshall, Joanne R. Festa, Philip M. Meyers and E. Sander Connolly Jr.

Object

The object of this study was to report the clinical features, surgical treatment, and long-term outcomes in adults with moyamoya phenomenon treated at a single institution in the US.

Methods

Forty-three adult patients with moyamoya disease (mean age 40 ± 11 years [SD], range 18–69 years) were treated with encephaloduroarteriosynangiosis (EDAS). Neurologists examined patients pre- and postoperatively. Follow-up was obtained in person or by structured telephone interview (median 41 months, range 4–126 months). The following outcomes were collected: transient ischemic attack (TIA), infarction, graft collateralization, change in cerebral perfusion, and functional level according to the modified Rankin scale (mRS). Kaplan-Meier estimates of infarction risk were calculated for comparison of surgically treated and contralateral hemispheres.

Results

The majority of patients were women (65%), were Caucasian (65%), presented with ischemic symptoms (98%), and had bilateral disease (86%). Nineteen patients underwent unilateral and 24 patients bilateral EDAS (67 treated hemispheres). Collateral vessels developed in 50 (98%) of 52 hemispheres for which imaging was available and there was evidence of increased perfusion on SPECT scans in 41 (82%) of the 50 hemispheres evaluated. Periprocedural infarction (< 48 hours) occurred in 3% of the hemispheres treated. In the follow-up period patients experienced 10 TIAs, 6 infarctions, and 1 intracranial hemorrhage. Although the hemisphere selected for surgery was based upon patients' symptoms and severity of pathology, the 5-year infarction-free survival rate was 94% in the surgically treated hemispheres versus < 36% in the untreated hemispheres (p = 0.007). After controlling for age and sex, infarction was 89% less likely to occur in the surgically treated hemispheres than in the contralateral hemispheres (hazard ratio 0.11, 95% CI 0.02–0.56). Thirty-eight (88%) of 43 patients had preserved or improved mRS scores, relative to baseline status.

Conclusions

In this mixed-race population of North American patients, indirect bypass promoted adequate pial collateral development and increased perfusion in the majority of adult patients with moyamoya disease. Patients had low rates of postoperative TIAs, infarction, and hemorrhage, and the majority of patients had preserved or improved functional status.

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Fred Rincon, Errol Gordon, Robert M. Starke, Manuel M. Buitrago, Andres Fernandez, J. Michael Schmidt, Jan Claassen, Katja E. Wartenberg, Jennifer Frontera, David B. Seder, David Palestrant, E. Sander Connolly, Kiwon Lee, Stephan A. Mayer and Neeraj Badjatia

Object

The purpose of this study was to identify predictors of shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage (SAH).

Methods

The authors evaluated the incidence of shunt-dependent hydrocephalus in a consecutive cohort of 580 patients with SAH who were admitted to the Neurological Intensive Care Unit of Columbia University Medical Center between July 1996 and September 2002. Patient demographics, 24-hour admission variables, initial CT scan characteristics, daily transcranial Doppler variables, and development of in-hospital complications were analyzed. Odds ratios and 95% CIs for candidate predictors were calculated using multivariate nominal logistic regression.

Results

Admission glucose of at least 126 mg/dl (adjusted OR 1.6; 95% CI 1.0–2.6), admission brain CT scan with a bicaudate index of at least 0.20 (adjusted OR 1.43; 95% CI 1.0–2.0), Fisher Grade 4 (adjusted OR 2.71; 95% CI 1.2–5.7), fourth ventricle hemorrhage (adjusted OR 1.78; 95% CI 1.1–2.7), and development of nosocomial meningitis (adjusted OR 2.2; 95% CI 1.4–3.7) were independently associated with shunt dependency.

Conclusions

These data suggest that permanent CSF diversion after aneurysmal SAH may be independently predicted by hyperglycemia at admission, findings on the admission CT scan (Fisher Grade 4, fourth ventricle intraventricular hemorrhage, and bicaudate index ≥ 0.20), and development of nosocomial meningitis. Future research is needed to assess if tight glycemic control, reduction of fourth ventricle clot burden, and prevention of nosocomial meningitis may reduce the need for permanent CSF diversion after aneurysmal SAH.

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Scott D. Wait, Adib A. Abla, Brendan D. Killory, Robert M. Starke, Robert F. Spetzler and Peter Nakaji

Object

Many patients undergoing carotid endarterectomy (CEA) regularly take clopidogrel, a permanent platelet inhibitor. The authors sought to determine whether taking clopidogrel in the period before CEA leads to more bleeding or other complications.

Methods

The authors performed a retrospective, institutional review board–approved review of 182 consecutive patients who underwent CEA. Clinical, radiographic, and surgical data were gleaned from hospital and clinic records. Analysis was based on the presence or absence of clopidogrel in patients undergoing CEA and was performed twice by considering clopidogrel use within 8 days and within 5 days of surgery to define the groups.

Results

Taking clopidogrel within 8 days before surgery resulted in no statistical increase in any measure of morbidity or death. Taking clopidogrel within 5 days was associated with a small but significant increase in operative blood loss and conservatively managed postoperative neck swelling. No measure of permanent morbidity or death was increased in either clopidogrel group.

Conclusions

Findings in this study support the safety of preoperative clopidogrel in patients undergoing CEA.

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Roberto C. Heros

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Erin N. Kiehna, Robert M. Starke, Nader Pouratian and Aaron S. Dumont

Object

The Consolidated Standards for Reporting of Trials (CONSORT) criteria were published in 1996 to standardize the reporting and improve the quality of clinical trials. Despite having been endorsed by major medical journals and shown to improve the quality of reported trials, neurosurgical journals have yet to formally adopt these reporting criteria. The purpose of this study is to evaluate the quality and reporting of randomized controlled trials (RCTs) in neurosurgery and the factors that may affect the quality of reported trials.

Methods

The authors evaluated all neurosurgical RCTs published in 2006 and 2007 in the principal neurosurgical journals (Journal of Neurosurgery; Neurosurgery; Surgical Neurology; Journal of Neurology, Neurosurgery, and Psychiatry; and Acta Neurochirurgica) and in 3 leading general medical journals (Journal of the American Medical Association, Lancet, and the New England Journal of Medicine). Randomized controlled trials that addressed operative decision making or the treatment of neurosurgical patients were included in this analysis. The RCT quality was evaluated using the Jadad score and the CONSORT checklist.

Results

In 2006 and 2007, 27 RCTs relevant to intracranial neurosurgery were reported. Of these trials, only 59% had a Jadad score ≥ 3. The 3 major medical journals all endorsed the CONSORT guidelines, while none of the neurosurgical journals have adopted these guidelines. Randomized controlled trials published in the 3 major medical journals had a significantly higher mean CONSORT score (mean 41, range 39–44) compared with those published in neurosurgical journals (mean 26.4, range 17–38; p < 0.0001). Jadad scores were also significantly higher for the major medical journals (mean 3.42, range 2–5) than neurosurgical journals (mean 2.45, range 1–5; p = 0.05).

Conclusions

Despite the growing volume of RCTs in neurosurgery, the quality of reporting of these trials remains suboptimal, especially in the neurosurgical journals. Improved awareness of the CONSORT guidelines by journal editors, reviewers, and authors of these papers could improve the methodology and reporting of RCTs in neurosurgery.