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Kai U. Frerichs, Perttu J. Lindsberg, John M. Hallenbeck and Giora Z. Feuerstein

✓ The effects of a platelet-activating factor (PAF) antagonist on brain edema, cortical microcirculation, blood-brain barrier (BBB) disruption, and neuronal death following focal brain injury are reported. A neodymium:yttrium-aluminum-garnet (Nd:YAG) laser was used to induce highly reproducible focal cortical lesions in anesthetized rats. Secondary brain damage in this model was characterized by progressive cortical hypoperfusion, edema, and BBB disruption in the vicinity of the hemispheroid lesion occurring acutely after injury. The histopathological evolution was followed for up to 4 days. Neuronal damage in the cortex and the hippocampus (CA-1) was assessed quantitatively, revealing secondary and progressive loss of neuronal tissue within the first 24 hours following injury.

Pretreatment with the PAF antagonist BN 50739 ameliorated the severe hypoperfusion in 12 rats (increasing local cerebral blood flow from a mean ± standard error of the mean of 40.5% ± 8.3% to 80.2% ± 7.8%, p < 0.01) and reduced edema by 70% in 10 rats (p < 0.05) acutely after injury. The PAF antagonist also reduced the progression of neuronal damage in the cortex and the CA-1 hippocampal neurons (decrease of neuronal death from 88.0% ± 3.9% to 49.8% ± 4.2% at 24 hours in the cortex and from 40.2 ± 5.0% to 13.2% ± 2.1% in the hippocampus in 30 rats; p < 0.05).

This study provides evidence to support progressive brain damage following focal brain injury, associated with secondary loss of neuronal cells. In this latter process, PAF antagonists may provide significant therapeutic protection in arresting secondary brain damage following cerebral ischemia and neurological trauma.

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Kai U. Frerichs, Philip E. Stieg and Robert M. Friedlander

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Michael A. Silva, Alfred P. See, Hormuzdiyar H. Dasenbrock, Ramsey Ashour, Priyank Khandelwal, Nirav J. Patel, Kai U. Frerichs and Mohammad A. Aziz-Sultan

Successful application of endovascular neurosurgery depends on high-quality imaging to define the pathology and the devices as they are being deployed. This is especially challenging in the treatment of complex cases, particularly in proximity to the skull base or in patients who have undergone prior endovascular treatment. The authors sought to optimize real-time image guidance using a simple algorithm that can be applied to any existing fluoroscopy system. Exposure management (exposure level, pulse management) and image post-processing parameters (edge enhancement) were modified from traditional fluoroscopy to improve visualization of device position and material density during deployment. Examples include the deployment of coils in small aneurysms, coils in giant aneurysms, the Pipeline embolization device (PED), the Woven EndoBridge (WEB) device, and carotid artery stents. The authors report on the development of the protocol and their experience using representative cases.

The stent deployment protocol is an image capture and post-processing algorithm that can be applied to existing fluoroscopy systems to improve real-time visualization of device deployment without hardware modifications. Improved image guidance facilitates aneurysm coil packing and proper positioning and deployment of carotid artery stents, flow diverters, and the WEB device, especially in the context of complex anatomy and an obscured field of view.

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Hormuzdiyar H. Dasenbrock, Robert F. Rudy, Pui Man Rosalind Lai, Timothy R. Smith, Kai U. Frerichs, William B. Gormley, M. Ali Aziz-Sultan and Rose Du

OBJECTIVE

Although cigarette smoking is one of the strongest risk factors for cerebral aneurysm development and rupture, there are limited data evaluating the impact of smoking on outcomes after aneurysmal subarachnoid hemorrhage (SAH). Additionally, two recent studies suggested that nicotine replacement therapy was associated with improved neurological outcomes among smokers who had sustained an SAH compared with smokers who did not receive nicotine.

METHODS

Patients who underwent endovascular or microsurgical repair of a ruptured cerebral aneurysm were extracted from the Nationwide Inpatient Sample (NIS, 2009–2011) and stratified by cigarette smoking. Multivariable logistic regression analyzed in-hospital mortality, complications, tracheostomy or gastrostomy placement, and discharge to institutional care (a nursing or an extended care facility). Additionally, the composite NIS-SAH outcome measure (based on mortality, tracheostomy or gastrostomy, and discharge disposition) was evaluated, which has been shown to have excellent agreement with a modified Rankin Scale score greater than 3. Covariates included in regression constructs were patient age, sex, race/ethnicity, insurance status, socioeconomic status, comorbidities (including hypertension, drug and alcohol abuse), the NIS-SAH severity scale (previously validated against the Hunt and Hess grade), treatment modality used for aneurysm repair, and hospital characteristics. A sensitivity analysis was performed matching smokers to nonsmokers on age, sex, number of comorbidities, and NIS-SAH severity scale score.

RESULTS

Among the 5784 admissions evaluated, 37.1% (n = 2148) had a diagnosis of tobacco use, of which 31.1% (n = 1800) were current and 6.0% (n = 348) prior tobacco users. Smokers were significantly younger (mean age 51.4 vs 56.2 years) and had more comorbidities compared with nonsmokers (p < 0.001). There were no significant differences in mortality, total complications, or neurological complications by smoking status. However, compared with nonsmokers, smokers had significantly decreased adjusted odds of tracheostomy or gastrostomy placement (11.9% vs 22.7%, odds ratio [OR] 0.63, 95% confidence interval [CI] 0.51–0.78, p < 0.001), discharge to institutional care (OR 0.71, 95% CI 0.57–0.89, p = 0.002), and a poor outcome (OR 0.65, 95% CI 0.55–0.77, p < 0.001). Similar statistical associations were noted in the matched-pairs sensitivity analysis and in a subgroup of poor-grade patients (the upper quartile of the NIS-SAH severity scale).

CONCLUSIONS

In this nationwide study, smokers experienced SAH at a younger age and had a greater number of comorbidities compared with nonsmokers, highlighting the negative ramifications of cigarette smoking among patients with cerebral aneurysms. However, smoking was also associated with paradoxical superior outcomes on some measures, and future research to confirm and further understand the basis of this relationship is needed.

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Ning Lin, Allen Ho, Bradley A. Gross, Steven Pieper, Kai U. Frerichs, Arthur L. Day and Rose Du

Object

Management of unruptured intracranial aneurysms remains controversial in neurosurgery. The contribution of morphological parameters has not been included in the treatment paradigm in a systematic manner or for any particular aneurysm location. The authors present a large sample of middle cerebral artery (MCA) aneurysms that were assessed using morphological variables to determine the parameters associated with aneurysm rupture.

Methods

Preoperative CT angiography (CTA) studies were evaluated using Slicer software to generate 3D models of the aneurysms and their surrounding vascular architecture. Morphological parameters examined in each model included 5 variables already defined in the literature (aneurysm size, aspect ratio, aneurysm angle, vessel angle, and size ratio) and 3 novel variables (flow angle, distance to the genu, and parent-daughter angle). Univariate and multivariate statistical analyses were performed to determine statistical significance.

Results

Between 2005 and 2008, 132 MCA aneurysms were treated at a single institution, and CTA studies of 79 aneurysms (40 ruptured and 39 unruptured) were analyzed. Fifty-three aneurysms were excluded because of reoperation (4), associated AVM (2), or lack of preoperative CTA studies (47). Ruptured aneurysms were associated with larger size, greater aspect ratio, larger aneurysm and flow angles, and smaller parent-daughter angle. Multivariate logistic regression revealed that aspect ratio, flow angle, and parent-daughter angle were the strongest factors associated with ruptured aneurysms.

Conclusions

Aspect ratio, flow angle, and parent-daughter angle are more strongly associated with ruptured MCA aneurysms than size. The association of parameters independent of aneurysm morphology with ruptured aneurysms suggests that these parameters may be associated with an increased risk of aneurysm rupture. These factors are readily applied in clinical practice and should be considered in addition to aneurysm size when assessing the risk of aneurysm rupture specific to the MCA location.

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Michael A. Silva, Alfred P. See, Priyank Khandelwal, Ashutosh Mahapatra, Kai U. Frerichs, Rose Du, Nirav J. Patel and Mohammad A. Aziz-Sultan

OBJECTIVE

Paraclinoid aneurysms represent approximately 5% of intracranial aneurysms (Drake et al. [1968]). Visual impairment, which occurs in 16%–40% of patients, is among the most common presentations of these aneurysms (Day [1990], Lai and Morgan [2013], Sahlein et al. [2015], and Silva et al. [2017]). Flow-diverting stents, such as the Pipeline Embolization Device (PED), are increasingly used to treat these aneurysms, in part because of their theoretical reduction of mass effect (Fiorella et al. [2009]). Limited data on paraclinoid aneurysms treated with a PED exist, and few studies have compared outcomes of patients after PED placement with those of patients after clipping or coiling.

METHODS

The authors performed a retrospective analysis of 115 patients with an aneurysm of the cavernous to ophthalmic segments of the internal carotid artery treated with clipping, coiling, or PED deployment between January 2011 and March 2017. Postoperative complications were defined as new neurological deficit, aneurysm rupture, recanalization, or other any operative complication that required reintervention.

RESULTS

A total of 125 paraclinoid aneurysms in 115 patients were treated, including 70 with PED placement, 23 with coiling, and 32 with clipping. Eighteen (14%) aneurysms were ruptured. The mean aneurysm size was 8.2 mm, and the mean follow-up duration was 18.4 months. Most aneurysms were discovered incidentally, but visual impairment, which occurred in 21 (18%) patients, was the most common presenting symptom. Among these patients, 15 (71%) experienced improvement in their visual symptoms after treatment, including 14 (93%) of these 15 patients who were treated with PED deployment. Complete angiographic occlusion was achieved in 89% of the patients. Complications were seen in 17 (15%) patients, including 10 (16%) after PED placement, 2 (9%) after coiling, and 5 (17%) after clipping. Patients with incomplete aneurysm occlusion had a higher rate of procedural complications than those with complete occlusion (p = 0.02). The rate of postoperative visual improvement was significantly higher among patients treated with PED deployment than in those treated with coiling (p = 0.01). The significant predictors of procedural complications were incomplete occlusion (p = 0.03), hypertension, (p = 0.04), and diabetes (p = 0.03).

CONCLUSIONS

In a large series in which patient outcomes after treatment of paraclinoid aneurysms were compared, the authors found a high rate of aneurysm occlusion and a comparable rate of procedural complications among patients treated with PED placement compared with the rates among those who underwent clipping or coiling. For patients who presented with visual symptoms, those treated with PED placement had the highest rate of visual improvement. The results of this study suggest that the PED is an effective and safe modality for treating paraclinoid aneurysms, especially for patients who present with visual symptoms.

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Hormuzdiyar H. Dasenbrock, Robert F. Rudy, Timothy R. Smith, William B. Gormley, Nirav J. Patel, Kai U. Frerichs, M. Ali Aziz-Sultan and Rose Du

OBJECTIVE

The complex decision analysis of unruptured intracranial aneurysms entails weighing the benefits of aneurysm repair against operative risk. The goal of the present analysis was to build and validate a predictive scale that identifies patients with the greatest odds of a postsurgical adverse event.

METHODS

Data on patients who underwent surgical clipping of an unruptured aneurysm were extracted from the prospective National Surgical Quality Improvement Program registry (NSQIP; 2007–2014); NSQIP does not systematically collect data on patients undergoing intracranial endovascular intervention. Multivariable logistic regression evaluated predictors of any 30-day adverse event; variables screened included patient demographics, comorbidities, functional status, preoperative laboratory values, aneurysm location/complexity, and operative time. A predictive scale was constructed based on statistically significant independent predictors, which was validated using both NSQIP (2015–2016) and the Nationwide Inpatient Sample (NIS; 2002–2011).

RESULTS

The NSQIP unruptured aneurysm scale was proposed: 1 point was assigned for a bleeding disorder; 2 points for age 51–60 years, cardiac disease, diabetes mellitus, morbid obesity, anemia (hematocrit < 36%), operative time 240–330 minutes; 3 points for leukocytosis (white blood cell count > 12,000/μL) and operative time > 330 minutes; and 4 points for age > 60 years. An increased score was predictive of postoperative stroke or coma (NSQIP: p = 0.002, C-statistic = 0.70; NIS: p < 0.001, C-statistic = 0.61), a medical complication (NSQIP: p = 0.01, C-statistic = 0.71; NIS: p < 0.001, C-statistic = 0.64), and a nonroutine discharge (NSQIP: p < 0.001, C-statistic = 0.75; NIS: p < 0.001, C-statistic = 0.66) in both validation populations. Greater score was also predictive of increased odds of any adverse event, a major complication, and an extended hospitalization in both validation populations (p ≤ 0.03).

CONCLUSIONS

The NSQIP unruptured aneurysm scale may augment the risk stratification of patients undergoing microsurgical clipping of unruptured cerebral aneurysms.

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Hormuzdiyar H. Dasenbrock, Michael O. Nguyen, Kai U. Frerichs, Donovan Guttieres, William B. Gormley, M. Ali Aziz-Sultan and Rose Du

OBJECTIVE

Although the prevalence of obesity is increasing rapidly both nationally and internationally, few studies have analyzed outcomes among obese patients undergoing cranial neurosurgery. The goal of this study, which used a nationwide data set, was to evaluate the association of both obesity and morbid obesity with treatment outcomes among patients with aneurysmal subarachnoid hemorrhage (SAH); in addition, the authors sought to analyze how postoperative complications for obese patients with SAH differ by the treatment modality used for aneurysm repair.

METHODS

Clinical data for adult patients with SAH who underwent microsurgical or endovascular aneurysm repair were extracted from the Nationwide Inpatient Sample (NIS). The body habitus of patients was classified as nonobese (body mass index [BMI] < 30 kg/m2), obese (BMI ≥ 30 kg/m2 and ≤ 40 kg/m2), or morbidly obese (BMI > 40 kg/m2). Multivariable logistic regression analyzed the association of body habitus with in-hospital mortality rate, complications, discharge disposition, and poor outcome as defined by the composite NIS-SAH outcome measure. Covariates included patient demographics, comorbidities (including hypertension and diabetes), health insurance status, the NIS-SAH severity scale, treatment modality used for aneurysm repair, and hospital characteristics.

RESULTS

In total, data from 18,281 patients were included in this study; the prevalence of morbid obesity increased from 0.8% in 2002 to 3.5% in 2011. Obese and morbidly obese patients were significantly younger and had a greater number of comorbidities than nonobese patients (p < 0.001). Mortality rates for obese (11.5%) and morbidly obese patients (10.5%) did not significantly differ from those for nonobese patients (13.5%); likewise, no differences in neurological complications or poor outcome were observed among these 3 groups. Morbid obesity was associated with significantly increased odds of several medical complications, including venous thromboembolic (OR 1.52, 95% CI 1.01–2.30, p = 0.046) and renal (OR 1.64, 95% CI: 1.11–2.43, p = 0.01) complications and infections (OR 1.34, 95% CI 1.08–1.67, p = 0.009, attributable to greater odds of urinary tract and surgical site infections). Moreover, morbidly obese patients had higher odds of a nonroutine hospital discharge (OR 1.33, 95% CI 1.03–1.71, p = 0.03). Patients with milder obesity had decreased odds of some medical complications, including cardiac, pulmonary, and infectious complications, primarily among patients who had undergone coil embolization.

CONCLUSIONS

In this study involving a nationwide administrative database, milder obesity was not significantly associated with increased mortality rates, neurological complications, or poor outcomes after SAH. Morbid obesity, however, was associated with increased odds of venous thromboembolic, renal, and infectious complications, as well as of a nonroutine hospital discharge. Notably, milder obesity was associated with decreased odds of some medical complications, primarily in patients treated with coiling.

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Hormuzdiyar H. Dasenbrock, Sandra C. Yan, Bradley A. Gross, Donovan Guttieres, William B. Gormley, Kai U. Frerichs, M. Ali Aziz-Sultan and Rose Du

OBJECTIVE

Although aspirin usage may be associated with a decreased risk of rupture of cerebral aneurysms, any potential therapeutic benefit from aspirin must be weighed against the theoretical risk of greater hemorrhage volume if subarachnoid hemorrhage (SAH) occurs. However, few studies have evaluated the association between prehemorrhage aspirin use and outcomes. This is the first nationwide analysis to evaluate the impact of long-term aspirin and anticoagulant use on outcomes after SAH.

METHODS

Data from the Nationwide Inpatient Sample (NIS; 2006–2011) were extracted. Patients with a primary diagnosis of SAH who underwent microsurgical or endovascular aneurysm repair were included; those with a diagnosis of an arteriovenous malformation were excluded. Multivariable logistic regression was performed to calculate the adjusted odds of in-hospital mortality, a nonroutine discharge (any discharge other than to home), or a poor outcome (death, discharge to institutional care, tracheostomy, or gastrostomy) for patients with long-term aspirin or anticoagulant use. Multivariable linear regression was used to evaluate length of hospital stay. Covariates included patient age, sex, comorbidities, primary payer, NIS-SAH severity scale, intracerebral hemorrhage, cerebral edema, herniation, modality of aneurysm repair, hospital bed size, and whether the hospital was a teaching hospital. Subgroup analyses exclusively evaluated patients treated surgically or endovascularly.

RESULTS

The study examined 11,549 hospital admissions. Both aspirin (2.1%, n = 245) and anticoagulant users (0.9%, n = 108) were significantly older and had a greater burden of comorbid disease (p < 0.001); severity of SAH was slightly lower in those with long-term aspirin use (p = 0.03). Neither in-hospital mortality (13.5% vs 12.6%) nor total complication rates (79.6% vs 80.0%) differed significantly by long-term aspirin use. Additionally, aspirin use was associated with decreased odds of a cardiac complication (OR 0.57, 95% CI 0.36%–0.91%, p = 0.02) or of venous thromboembolic events (OR 0.53, 95% CI 0.30%–0.94%, p = 0.03). Length of stay was significantly shorter (15 days vs 17 days [12.73%], 95% CI 5.22%–20.24%, p = 0.001), and the odds of a nonroutine discharge were lower (OR 0.63, 95% CI 0.48%–0.83%, p = 0.001) for aspirin users. In subgroup analyses, the benefits of aspirin were primarily noted in patients who underwent coil embolization; likewise, among patients treated endovascularly, the adjusted odds of a poor outcome were lower among long-term aspirin users (31.8% vs 37.4%, OR 0.63, 95% CI 0.42%–0.94%, p = 0.03). Although the crude rates of in-hospital mortality (19.4% vs 12.6%) and poor outcome (53.6% vs 37.6%) were higher for long-term anticoagulant users, in multivariable logistic regression models these variations were not significantly different (mortality: OR 1.36, 95% CI 0.89%–2.07%, p = 0.16; poor outcome: OR 1.09, 95% CI 0.69%–1.73%, p = 0.72).

CONCLUSIONS

In this nationwide study, neither long-term aspirin nor anticoagulant use were associated with differential mortality or complication rates after SAH. Aspirin use was associated with a shorter hospital stay and lower rates of nonroutine discharge, with these benefits primarily observed in patients treated endovascularly.

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Alexander E. Ropper, Ning Lin, Bradley A. Gross, Hekmat K. Zarzour, Ruth Thiex, John H. Chi, Rose Du and Kai U. Frerichs

Object

The management of spinal vascular malformations has undergone significant evolution with the advent of advanced endovascular and angiographic technology. Three-dimensional rotational spinal angiography is an advanced tool that allows the surgeon to gain a better appreciation of the anatomy of these spinal vascular lesions and their relation to surrounding structures. This article describes the use of rotational angiography and 3D reconstructions in the diagnosis and management of spinal vascular malformations.

Methods

The authors present representative cases involving surgical treatment planning for spinal vascular malformations with focus on the utility and technique of rotational spinal angiography. They report the use of rotational spinal angiography for a heterogeneous collection of vascular pathological conditions.

Results

Eight patients underwent rotational spinal angiography in addition to digital subtraction angiography (DSA) for the diagnosis and characterization of various spinal vascular lesions. Postprocessed images were used to characterize the lesion in relation to surrounding bone and to enhance the surgeon's ability to precisely localize and obliterate the abnormality. The reconstructions provided superior anatomical detail compared with traditional DSA. No associated complications from the rotational angiography were noted, and there was no statistically significant difference in the amount of radiation exposure to patients undergoing rotational angiography relative to traditional angiography.

Conclusions

The use of rotational spinal angiography provides a rapid and powerful diagnostic tool, superior to conventional DSA in the diagnosis and preoperative planning of a variety of spinal vascular pathology. A more detailed understanding of the anatomy of such lesions provided by this technique may improve the safety of the surgical approach.