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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.

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Shouri Lahiri, Mani Nezhad, Konrad H. Schlick, Brenda Rinsky, Axel Rosengart, Stephan A. Mayer and Patrick D. Lyden

OBJECTIVE

Intravenous nicardipine is commonly used for blood pressure reduction in patients with acute stroke. However, few studies have described its effects on cerebrovascular hemodynamics as measured by transcranial Doppler (TCD) waveform analysis and pulsatility index (PI). In this study, the authors report examples of a consistent but paradoxical finding associated with nicardipine that suggests intracranial vasoconstriction, contrary to what is expected from a vasodilator.

METHODS

The data presented are from a convenience sample of patients who underwent TCD monitoring before, after, or during nicardipine administration. In each case, TCD waveform morphologies and PIs were compared.

RESULTS

The TCD waveforms during nicardipine infusion are characterized by a prominent systolic peak and dicrotic notch. Systolic deceleration was more pronounced and PIs were significantly elevated in patients who were on nicardipine (p < 0.001). This finding was not evident when patients were not on nicardipine.

CONCLUSIONS

This study provides the first evidence of paradoxical intracranial vasoconstriction associated with intravenous nicardipine. In the authors' experience, this finding is consistently encountered in the vast majority of patients who are treated with intravenous nicardipine, and is contradictory to what is expected from a vasodilator. Future studies are needed to confirm this finding in larger populations and diverse clinical settings and to examine mechanisms that explain this phenomenon.

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Charles L. Francoeur, David Roh, J. Michael Schmidt, Stephan A. Mayer, M. Cristina Falo, Sachin Agarwal, E. Sander Connolly, Jan Claassen, Mitchell S. V. Elkind and Soojin Park

OBJECTIVE

Rebleeding remains a frequent and catastrophic event leading to poor outcome after subarachnoid hemorrhage (SAH). Reduced platelet function after the initial bleed is associated with higher risk of early rebleeding. Desmopressin (DDAVP) is a well-known hemostatic agent, and recent guidelines already suggest its use in individuals exposed to antiplatelet drugs. The authors hypothesized that DDAVP administration in patients with SAH at admission would be associated with lower risks of rebleeding.

METHODS

The authors performed an observational cohort study of patients enrolled in the Columbia University SAH Outcome Project between August 1996 and July 2015. The authors compared the rate of rebleeding between patients who were and those who were not treated with DDAVP. After adjustment for known predictors, logistic regression was used to measure the association between treatment with DDAVP and risks of rebleeding.

RESULTS

Among 1639 patients with SAH, 12% were treated with DDAVP. The main indication for treatment was suspected exposure to an antiplatelet agent. The overall incidence of rebleeding was 9% (1% among patients treated with DDAVP compared with 8% among those not treated). After adjustment for antiplatelet use and known predictors, treatment with DDAVP was associated with a 45% reduction in the risks of rebleeding (adjusted OR 0.55, 95% CI 0.27–0.97). DDAVP was associated with a higher incidence of hyponatremia but not with thrombotic events or delayed cerebral ischemia.

CONCLUSIONS

Treatment with DDAVP was associated with a lower risk of rebleeding among patients with SAH. These findings support further study of DDAVP as first-line therapy for medical hemostasis in patients with SAH.

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Neha S. Dangayach, Harpreet Singh Grewal, Gian Marco De Marchis, Roberta K. Sefcik, Rachel Bruce, Aarti Chhatlani, E. Sander Connolly, M. Cristina Falo, Sachin Agarwal, Jan Claassen, J. Michael Schmidt and Stephan A. Mayer

OBJECTIVE

Being overweight or mildly obese has been associated with a decreased risk of death or hospitalization in patients with cardiovascular disease. Similarly, overweight patients admitted to an intensive care unit (ICU) have improved survival up to 1 year after admission. These counterintuitive observations are examples of the “obesity paradox.” Does the obesity paradox exist in patients with intracerebral hemorrhage (ICH)? In this study the authors examined whether there was an association between obesity and functional outcome in patients with ICH.

METHODS

The authors analyzed 202 patients admitted to the neurological ICU (NICU) who were prospectively enrolled in the Columbia University ICH Outcomes Project between September 2009 and December 2012. Patients were categorized into 2 groups: overweight (body mass index [BMI] ≥ 25 kg/m2) and not overweight (BMI < 25 kg/m2). The primary outcome was defined as survival with favorable outcome (modified Rankin Scale [mRS] score 0–3) versus death or severe disability (mRS score 4–6) at 3 months.

RESULTS

The mean age of the patients in the study was 61 years. The mean BMI was 28 ± 6 kg/m2. The mean Glasgow Coma Scale score was 10 ± 4 and the mean ICH score was 1.9 ± 1.3. The overall 90-day mortality rate was 41%. Among patients with a BMI < 25 kg/m2, 24% (17/70) had a good outcome, compared with 39% (52/132) among those with a BMI ≥ 25 kg/m2 (p = 0.03). After adjusting for ICH score, sex, do-not-resuscitate code status, and history of hypertension, being overweight or obese (BMI ≥ 25 kg/m2) was associated with twice the odds of having a good outcome compared with patients with BMI < 25 kg/m2 (adjusted odds ratio 2.05, 95% confidence interval 1.03–4.06, p = 0.04).

CONCLUSIONS

In patients with ICH admitted to the NICU, being overweight or obese (BMI ≥ 25 kg/m2) was associated with favorable outcome after adjustment for established predictors. The reason for this finding requires further study.

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Alexander G. Chartrain, Ahmed J. Awad, Christopher A. Sarkiss, Rui Feng, Yangbo Liu, J Mocco, Joshua B. Bederson, Stephan A. Mayer, Neha S. Dangayach and Errol Gordon

OBJECTIVE

Patients who have experienced subarachnoid hemorrhage (SAH) often receive care in the setting of the ICU. However, SAH patients may not all require extended ICU admission. The authors established a protocol on January 1, 2015, to transfer select, low-risk patients to a step-down unit (SDU) to streamline care for SAH patients. This study describes the results of the implemented protocol.

METHODS

In this retrospective chart review, patients presenting with SAH between January 2011 and September 2016 were reviewed for inclusion. The control group consisted of patients admitted prior to establishment of the SDU transfer protocol, while the intervention group consisted of patients admitted afterward.

RESULTS

Of the patients in the intervention group, 79.2% (57/72) were transferred to the SDU during their admission. Of these transferred patients, 29.8% (17/57) required return to the neurosurgical ICU (NSICU). There were no instances of morbidity or mortality directly related to care in the SDU. Patients in the intervention group had a mean reduced NSICU length of stay, by 1.95 days, which trended toward significance, and a longer average hospitalization, by 2.7 days, which also trended toward significance. In-hospital mortality and 90-day readmission rate were not statistically different between the groups. In addition, early transfer timing prior to 7 days was associated with neither a higher return rate to the NSICU nor higher 90-day readmission rate.

CONCLUSIONS

In this retrospective study, the authors demonstrated that the transfer protocol was safe, feasible, and effective in reducing the ICU length of stay and was independent of transfer timing. Confirmation of these results is needed in a large, multicenter study.

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Fawaz Al-Mufti, David Roh, Shouri Lahiri, Emma Meyers, Jens Witsch, Hans-Peter Frey, Neha Dangayach, Cristina Falo, Stephan A. Mayer, Sachin Agarwal, Soojin Park, Philip M. Meyers, E. Sander Connolly, Jan Claassen and J. Michael Schmidt

OBJECTIVE

The clinical significance of cerebral ultra-early angiographic vasospasm (UEAV), defined as cerebral arterial narrowing within the first 48 hours of aneurysmal subarachnoid hemorrhage (aSAH), remains poorly characterized. The authors sought to determine its frequency, predictors, and impact on functional outcome.

METHODS

The authors prospectively studied UEAV in a cohort of 1286 consecutively admitted patients with aSAH between August 1996 and June 2013. Admission clinical, radiographic, and acute clinical course information was documented during patient hospitalization. Functional outcome was assessed at 3 months using the modified Rankin Scale. Logistic regression and Cox proportional hazards models were generated to assess predictors of UEAV and its relationship to delayed cerebral ischemia (DCI) and outcome. Multiple imputation methods were used to address data lost to follow-up.

RESULTS

The cohort incidence rate of UEAV was 4.6%. Multivariable logistic regression analysis revealed that younger age, sentinel bleed, and poor admission clinical grade were significantly associated with UEAV. Patients with UEAV had a 2-fold increased risk of DCI (odds ratio [OR] 2.3, 95% confidence interval [CI] 1.4–3.9, p = 0.002) and cerebral infarction (OR 2.0, 95% CI 1.0–3.9, p = 0.04), after adjusting for known predictors. Excluding patients who experienced sentinel bleeding did not change this effect. Patients with UEAV also had a significantly higher hazard for DCI in a multivariable model. UEAV was not found to be significantly associated with poor functional outcome (OR 0.8, 95% CI 0.4–1.6, p = 0.5).

CONCLUSIONS

UEAV may be less frequent than has been reported previously. Patients who exhibit UEAV are at higher risk for refractory DCI that results in cerebral infarction. These patients may benefit from earlier monitoring for signs of DCI and more aggressive treatment. Further study is needed to determine the long-term functional significance of UEAV.

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Bartosz T. Grobelny, Andrew F. Ducruet, Peter A. DeRosa, Ivan S. Kotchetkov, Brad E. Zacharia, Zachary L. Hickman, Luis Fernandez, Reshma Narula, Jan Claassen, Kiwon Lee, Neeraj Badjatia, Stephan A. Mayer and E. Sander Connolly Jr.

Object

Cystathionine β-synthase (CBS) is an enzyme that metabolizes homocysteine to form H2S in the brain. Hydrogen sulfide functions as a vasodilator as well as a regulator of neuronal ion channels and multiple intracellular signaling pathways. Given the myriad effects of H2S, the authors hypothesized that patients possessing gain-of-function polymorphisms of the CBS gene will experience a decreased incidence of delayed cerebral ischemia (DCI) following aneurysmal subarachnoid hemorrhage (aSAH).

Methods

Patients were enrolled in a prospective observational database of aSAH outcomes. DNA was extracted from buccal swabs and sequenced for 3 functional polymorphisms of the CBS gene (699C→T, 844ins68, and 1080C→T) by polymerase chain reaction. Serum homocysteine levels (μmol/L) were assayed. Multivariate analysis was used to determine the relationship between CBS genotype and occurrence of both angiographic vasospasm and DCI.

Results

There were 87 patients included in the study. None of the polymorphisms investigated were significantly associated with the incidence of angiographic vasospasm. However, after controlling for admission hypertension, patients with the gain-of-function 844 WT/ins genotypes were less likely to experience DCI relative to those with the 844 WT/WT genotype (86 patients, p = 0.050), while the decrease-in-function genotype 1080 TT was more likely to experience DCI relative to those with 1080 CC and CT genotypes (84 patients, p = 0.042). Serum homocysteine levels did not correlate with the extent of either angiographic vasospasm or DCI in this analysis.

Conclusions

Polymorphisms of the CBS gene that impart gain-of-function may be associated with a reduced risk of DCI after aSAH, independent of serum homocysteine. Signaling through H2S may mediate protection from DCI following aSAH through a mechanism that does not involve macrovascular vasodilation.

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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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Grace H. Kim, David K. Hahn, Christopher P. Kellner, Ricardo J. Komotar, Robert Starke, Matthew C. Garrett, Jiang Yao, Justin Cleveland, Stephan A. Mayer and E. Sander Connolly Jr.

Object

Heparin-induced thrombocytopenia Type II (HIT II) is a serious complication that occurs in 0.2–3% of patients treated with heparin and is associated with a high risk of thrombotic events. One center recently reported an incidence of HIT II of 15% in a population of patients with aneurysmal subarachnoid hemorrhage (aSAH). Because these patients are typically exposed to heparin during angiography, controversy exists regarding whether prophylaxis with enoxaparin rather than heparin affords any reduction in the risk of developing HIT II. In this study, the authors investigated the effect of heparin compared with enoxaparin on the incidence of HIT II in patients with aSAH.

Methods

The authors reviewed the medical records of 300 patients treated for aSAH who received thromboprophylaxis with either heparin or enoxaparin, and identified patients who developed HIT II. The incidences of HIT II in the 2 treatment groups were then compared.

Results

One hundred sixty-six patients with aSAH were treated with heparin, and 134 patients were treated with enoxaparin. Sixteen (5.3%) of 300 patients met the diagnostic criteria for HIT II. Of those treated with heparin, 8 (4.8%) of 166 developed HIT II, compared with 8 (6%) of 134 treated with enoxaparin (difference not significant).

Conclusions

The authors report a lower incidence of HIT II in patients with aSAH than has previously been reported. The data also suggest that patients with aSAH who receive heparin are at no greater risk of developing HIT II than those who receive enoxaparin. This finding challenges the merit of choosing enoxaparin rather than heparin for thromboprophylaxis in patients with a SAH.