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Michael A. Mooney, Joseph Georges, Mohammedhassan Izady Yazdanabadi, Katherine Y. Goehring, William L. White, Andrew S. Little, Mark C. Preul, Stephen W. Coons, Peter Nakaji, and Jennifer M. Eschbacher

OBJECTIVE

The objective of this study was to evaluate the feasibility of using confocal reflectance microscopy (CRM) ex vivo to differentiate adenoma from normal pituitary gland in surgical biopsy specimens. CRM allows for rapid, label-free evaluation of biopsy specimens with cellular resolution while avoiding some limitations of frozen section analysis.

METHODS

Biopsy specimens from 11 patients with suspected pituitary adenomas were transported directly to the pathology department. Samples were immediately positioned and visualized with CRM using a confocal microscope located in the same area of the pathology department where frozen sections are prepared. An H & E–stained slide was subsequently prepared from imaged tissue. A neuropathologist compared the histopathological characteristics of the H & E–stained slide and the matched CRM images. A second neuropathologist reviewed images in a blinded fashion and assigned diagnoses of adenoma or normal gland.

RESULTS

For all specimens, CRM contrasted cellularity, tissue architecture, nuclear pleomorphism, vascularity, and stroma. Pituitary adenomas demonstrated sheets and large lobules of cells, similar to the matched H & E–stained slides. CRM images of normal tissue showed scattered small lobules of pituitary epithelial cells, consistent with matched H & E–stained images of normal gland. Blinded review by a neuropathologist confirmed the diagnosis in 15 (94%) of 16 images of adenoma versus normal gland.

CONCLUSIONS

CRM is a simple, reliable approach for rapidly evaluating pituitary adenoma specimens ex vivo. This technique can be used to accurately differentiate between pituitary adenoma and normal gland while preserving biopsy tissue for future permanent analysis, immunohistochemical studies, and molecular studies.

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M. Yashar S. Kalani, John E. Wanebo, Nikolay L. Martirosyan, Peter Nakaji, Joseph M. Zabramski, and Robert F. Spetzler

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Michael R. Levitt, Randall J. Hlubek, Karam Moon, M. Yashar S. Kalani, Peter Nakaji, Kris A. Smith, Andrew S. Little, Kerry Knievel, Jane W. Chan, Cameron G. McDougall, and Felipe C. Albuquerque

OBJECTIVE

Cerebral venous pressure gradient (CVPG) from dural venous sinus stenosis is implicated in headache syndromes such as idiopathic intracranial hypertension (IIH). The incidence of CVPG in headache patients has not been reported.

METHODS

The authors reviewed all cerebral venograms with manometry performed for headache between January 2008 and May 2015. Patient demographics, headache etiology, intracranial pressure (ICP) measurements, and radiographic and manometric results were recorded. CVPG was defined as a difference ≥ 8 mm Hg by venographic manometry.

RESULTS

One hundred sixty-four venograms were performed in 155 patients. There were no procedural complications. Ninety-six procedures (58.5%) were for patients with IIH. The overall incidence of CVPG was 25.6% (42 of 164 procedures): 35.4% (34 of 96 procedures) in IIH patients and 11.8% (8 of 68 procedures) in non-IIH patients. Sixty procedures (36.6%) were performed in patients with preexisting shunts. Seventy-seven patients (49.7%) had procedures preceded by an ICP measurement within 4 weeks of venography, and in 66 (85.7%) of these patients, the ICP had been found to be elevated. CVPG was seen in 8.3% (n = 5) of the procedures in the 60 patients with a preexisting shunt and in 0% (n = 0) of the 11 procedures in the 77 patients with normal ICP (p < 0.001 for both). Noninvasive imaging (MR venography, CT venography) was assessed prior to venography in 112 (68.3%) of 164 cases, and dural venous sinus abnormalities were demonstrated in 73 (65.2%) of these cases; there was a trend toward CVPG (p = 0.07). Multivariate analysis demonstrated an increased likelihood of CVPG in patients with IIH (OR 4.97, 95% CI 1.71–14.47) and a decreased likelihood in patients with a preexisting shunt (OR 0.09, 95% CI 0.02–0.44).

CONCLUSIONS

CVPG is uncommon in IIH patients, rare in those with preexisting shunts, and absent in those with normal ICP.

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Christopher D. Wilson, Sam Safavi-Abbasi, Hai Sun, M. Yashar S. Kalani, Yan D. Zhao, Michael R. Levitt, Ricardo A. Hanel, Eric Sauvageau, Timothy B. Mapstone, Felipe C. Albuquerque, Cameron G. McDougall, Peter Nakaji, and Robert F. Spetzler

OBJECTIVE

Aneurysmal subarachnoid hemorrhage (aSAH) may be complicated by hydrocephalus in 6.5%–67% of cases. Some patients with aSAH develop shunt dependency, which is often managed by ventriculoperitoneal shunt placement. The objectives of this study were to review published risk factors for shunt dependency in patients with aSAH, determine the level of evidence for each factor, and calculate the magnitude of each risk factor to better guide patient management.

METHODS

The authors searched PubMed and MEDLINE databases for Level A and Level B articles published through December 31, 2014, that describe factors affecting shunt dependency after aSAH and performed a systematic review and meta-analysis, stratifying the existing data according to level of evidence.

RESULTS

On the basis of the results of the meta-analysis, risk factors for shunt dependency included high Fisher grade (OR 7.74, 95% CI 4.47–13.41), acute hydrocephalus (OR 5.67, 95% CI 3.96–8.12), in-hospital complications (OR 4.91, 95% CI 2.79–8.64), presence of intraventricular blood (OR 3.93, 95% CI 2.80–5.52), high Hunt and Hess Scale score (OR 3.25, 95% CI 2.51–4.21), rehemorrhage (OR 2.21, 95% CI 1.24–3.95), posterior circulation location of the aneurysm (OR 1.85, 95% CI 1.35–2.53), and age ≥ 60 years (OR 1.81, 95% CI 1.50–2.19). The only risk factor included in the meta-analysis that did not reach statistical significance was female sex (OR 1.13, 95% CI 0.77–1.65).

CONCLUSIONS

The authors identified several risk factors for shunt dependency in aSAH patients that help predict which patients are likely to require a permanent shunt. Although some of these risk factors are not independent of each other, this information assists clinicians in identifying at-risk patients and managing their treatment.

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Ali M. Elhadi, Hasan A. Zaidi, Kaan Yagmurlu, Shah Ahmed, Albert L. Rhoton Jr., Peter Nakaji, Mark C. Preul, and Andrew S. Little

OBJECTIVE

Endoscopic transmaxillary approaches (ETMAs) address pathology of the anterolateral skull base, including the cavernous sinus, pterygopalatine fossa, and infratemporal fossa. This anatomically complex region contains branches of the trigeminal nerve and external carotid artery and is in proximity to the internal carotid artery. The authors postulated, on the basis of intraoperative observations, that the infraorbital nerve (ION) is a useful surgical landmark for navigating this region; therefore, they studied the anatomy of the ION and its relationships to critical neurovascular structures and the maxillary nerve (V2) encountered in ETMAs.

METHODS

Endoscopic anatomical dissections were performed bilaterally in 5 silicone-injected, formalin-fixed cadaveric heads (10 sides). Endonasal transmaxillary and direct transmaxillary (Caldwell-Luc) approaches were performed, and anatomical correlations were analyzed and documented. Stereotactic imaging of each specimen was performed to correlate landmarks and enable precise measurement of each segment.

RESULTS

The ION was readily identified in the roof of the maxillary sinus at the beginning of the surgical procedure in all specimens. Anatomical dissections of the ION and the maxillary branch of the trigeminal nerve (V2) to the cavernous sinus suggested that the ION/V2 complex has 4 distinct segments that may have implications in endoscopic approaches: 1) Segment I, the cutaneous segment of the ION and its terminal branches (5–11 branches) to the face, distal to the infraorbital foramen; 2) Segment II, the orbitomaxillary segment of the ION within the infraorbital canal from the infraorbital foramen along the infraorbital groove (length 12 ± 3.2 mm); 3) Segment III, the pterygopalatine segment within the pterygopalatine fossa, which starts at the infraorbital groove to the foramen rotundum (13 ± 2.5 mm); and 4) Segment IV, the cavernous segment from the foramen rotundum to the trigeminal ganglion (15 ± 4.1 mm), which passes in the lateral wall of the cavernous sinus. The relationship of the ION/V2 complex to the contents of the cavernous sinus, carotid artery, and pterygopalatine fossa is described in the text.

CONCLUSIONS

The ION/V2 complex is an easily identifiable and potentially useful surgical landmark to the foramen rotundum, cavernous sinus, carotid artery, pterygopalatine fossa, and anterolateral skull base during ETMAs.

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Sam Safavi-Abbasi, Felix Moron, Hai Sun, Mark E. Oppenlander, M. Yashar S. Kalani, Celene B. Mulholland, Joseph M. Zabramski, Peter Nakaji, and Robert F. Spetzler

OBJECTIVE

To address the challenges of microsurgically treating broad-based, frail, and otherwise complex aneurysms that are not amenable to direct clipping, alternative techniques have been developed. One such technique is to use cotton to augment clipping (“cotton-clipping” technique), which is also used to manage intraoperative aneurysm neck rupture, and another is to reinforce unclippable segments or remnants of aneurysm necks with cotton (“cotton-augmentation” technique). This study reviews the natural history of patients with aneurysms treated with cotton-clipping and cotton-augmentation techniques.

METHODS

The authors queried a database consisting of all patients with aneurysms treated at Barrow Neurological Institute in Phoenix, Arizona, between January 1, 2004, and December 31, 2014, to identify cases in which cotton-clipping or cotton-augmentation strategies had been used. Management was categorized as the cotton-clipping technique if cotton was used within the blades of the aneurysm clip and as the cotton-clipping technique if cotton was used to reinforce aneurysms or portions of the aneurysm that were unclippable due to the presence of perforators, atherosclerosis, or residual aneurysms. Data were reviewed to assess patient outcomes and annual rates of aneurysm recurrence or hemorrhage after the initial procedures were performed.

RESULTS

The authors identified 60 aneurysms treated with these techniques in 57 patients (18 patients with ruptured aneurysms and 39 patients with unruptured aneurysms) whose mean age was 53.1 years (median 55 years; range 24–72 years). Twenty-three aneurysms (11 cases of subarachnoid hemorrhage) were treated using cotton-clipping and 37 with cotton-augmentation techniques (7 cases of subarachnoid hemorrhage). In total, 18 patients presented with subarachnoid hemorrhage. The mean Glasgow Outcome Scale (GOS) score at the time of discharge was 4.4. At a mean follow-up of 60.9 ± 35.6 months (median 70 months; range 10–126 months), the mean GOS score at last follow-up was 4.8. The total number of patient follow-up years was 289.4. During the follow-up period, none of the cotton-clipped aneurysms increased in size, changed in configuration, or rebled. None of the patients experienced early rebleeding. The annual hemorrhage rate for aneurysms treated with cotton-augmentation was 0.52% and the recurrence rate was 1.03% per year. For all patients in the study, the overall risk of hemorrhage was 0.35% per year and the annual recurrence rate was 0.69%.

CONCLUSIONS

Cotton-clipping is an effective and durable treatment strategy for intraoperative aneurysm rupture and for management of broad-based aneurysms. Cotton-augmentation can be safely used to manage unclippable or partially clipped intracranial aneurysms and affords protection from early aneurysm re-rupture and a relatively low rate of late rehemorrhage.

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Sam Safavi-Abbasi, Noritaka Komune, Jacob B. Archer, Hai Sun, Nicholas Theodore, Jeffrey James, Andrew S. Little, Peter Nakaji, Michael E. Sughrue, Albert L. Rhoton, and Robert F. Spetzler

OBJECT

The objective of this study was to describe the surgical anatomy and technical nuances of various vascularized tissue flaps.

METHODS

The surgical anatomy of various tissue flaps and their vascular pedicles was studied in 5 colored silicone-injected anatomical specimens. Medical records were reviewed of 11 consecutive patients who underwent repair of extensive skull base defects with a combination of various vascularized flaps.

RESULTS

The supraorbital, supratrochlear, superficial temporal, greater auricular, and occipital arteries contribute to the vascular supply of the pericranium. The pericranial flap can be designed based on an axial blood supply. Laterally, various flaps are supplied by the deep or superficial temporal arteries. The nasoseptal flap is a vascular pedicled flap based on the nasoseptal artery. Patients with extensive skull base defects can undergo effective repair with dual flaps or triple flaps using these pedicled vascularized flaps.

CONCLUSIONS

Multiple pedicled flaps are available for reconstitution of the skull base. Knowledge of the surgical anatomy of these flaps is crucial for the skull base surgeon. These vascularized tissue flaps can be used effectively as single or combination flaps. Multilayered closure of cranial base defects with vascularized tissue can be used safely and may lead to excellent repair outcomes.

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Tim E. Darsaut and Jean Raymond

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Robert F. Spetzler, Cameron G. McDougall, Joseph M. Zabramski, Felipe C. Albuquerque, Nancy K. Hills, Jonathan J. Russin, Shahram Partovi, Peter Nakaji, and Robert C. Wallace

OBJECT

The authors report the 6-year results of the Barrow Ruptured Aneurysm Trial (BRAT). This ongoing randomized trial, with the final goal of a 10-year follow-up, compares the safety and efficacy of surgical clip occlusion and endovascular coil embolization in patients presenting with subarachnoid hemorrhage (SAH) from a ruptured aneurysm. The 1- and 3-year results of this trial have been previously reported.

METHODS

In total, 500 patients with an SAH met the entry criteria and were enrolled in the study. Of these patients, 471 were randomly assigned to the treatments: 238 to surgical clipping and 233 to endovascular coiling. Six patients who died before treatment and 57 patients with nonaneurysmal SAHs were excluded, leaving a total of 408 patients who underwent clipping (209 assigned) or coiling (199 assigned). Whether to treat patients within the assigned group or to cross over patients to the other group was at the discretion of the treating physician; 38% (75/199) of the patients assigned to coiling were crossed over to clipping and 1.9% (4/209) assigned to clipping were crossed over to coiling. The outcome data were collected by a dedicated nurse practitioner. The primary outcome analysis was based on the assigned treatment group; poor outcome was defined as a modified Rankin Scale (mRS) score > 2 and was independently adjudicated. Six years after randomization, 336 (82%) of 408 patients who had been treated were available for examination.

RESULTS

On the basis of an mRS score of > 2, and similar to the results at the 3-year follow-up, no significant difference in outcomes (p = 0.24) was detected between the 2 treatment groups. Complete aneurysm obliteration at 6 years was achieved in 96% (111/116) of the clipping group and in 48% (23/48) of the coiling group (p < 0.0001). In the period between the 3- and 6-year follow-ups, 3 additional patients assigned to coiling and none assigned to clipping received retreatment, for overall retreatment rates of 4.6% (13/280) for clipping and 16.4% (21/128) for coiling (p < 0.0001).

When aneurysm location was considered, the 6-year results continued to match the previously reported results, with no difference in outcome for anterior circulation aneurysms at most time points. Of the anterior circulation aneurysms assigned to coiling treatment, 42% (70/168) were crossed over to clipping treatment. The outcomes for posterior circulation aneurysms continued to favor coiling. The randomization process was unexpectedly skewed, with 18 of 21 treated aneurysms of the posterior inferior cerebellar artery (PICA) being assigned to clipping, but even when PICA aneurysms were removed from the analysis, outcomes for the posterior circulation aneurysms still favored coiling.

CONCLUSIONS

Although BRAT was statistically underpowered to detect small differences, these results suggest little difference in outcome between the 2 treatments for anterior circulation aneurysms. This was not the case for the posterior circulation aneurysms, where coil embolization appeared to provide a sustained advantage over clipping. Aneurysm obliteration rates in BRAT were significantly lower and retreatment rates significantly higher in the patients undergoing coiling than in those undergoing clipping. However, despite the fact that retreatment rates were higher after coiling, no recurrent hemorrhages were known to have occurred in patients undergoing coiling in BRAT who were followed up for 6 years. Sufficient questions remain about the relative benefits of the 2 treatment modalities to warrant further well-designed randomized trials.

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Richard W. Williamson, David A. Wilson, Adib A. Abla, Cameron G. McDougall, Peter Nakaji, Felipe C. Albuquerque, and Robert F. Spetzler

OBJECT

Subarachnoid hemorrhage (SAH) from ruptured posterior inferior cerebellar artery (PICA) aneurysms is uncommon, and long-term outcome data for patients who have suffered such hemorrhages is lacking. This study investigated in-hospital and long-term clinical data from a prospective cohort of patients with SAH from ruptured PICA aneurysms enrolled in a randomized trial; their outcomes were compared with those of SAH patients who were treated for other types of ruptured intracranial aneurysms. The authors hypothesize that PICA patients fare worse than those with aneurysms in other locations and this difference is related to the high rate of lower cranial nerve dysfunction in PICA patients.

METHODS

The authors analyzed data for 472 patients enrolled in the Barrow Ruptured Aneurysm Trial (BRAT) and retrospectively reviewed vasospasm data not collected prospectively. In the initial cohort, 57 patients were considered angiographically negative for aneurysmal SAH source and did not receive treatment for aneurysms, leaving 415 patients with aneurysmal SAH.

RESULTS

Of 415 patients with aneurysmal SAH, 22 (5.3%) harbored a ruptured PICA aneurysm. Eight of them had dissecting/fusiform-type aneurysms while 14 had saccular-type aneurysms. Nineteen PICA patients were treated with clipping (1 crossover from coiling), 2 were treated with coiling, and 1 died before treatment. When comparing PICA patients to all other aneurysm patients in the study cohort, there were no statistically significant differences in age (mean 57.6 ± 11.8 vs 53.9 ± 11.8 years, p = 0.17), Hunt and Hess grade median III [IQR II–IV] vs III [IQR II–III], p = 0.15), Fisher grade median 3 [IQR 3–3] vs 3 [IQR 3–3], p = 0.53), aneurysm size (mean 6.2 ± 3.0 vs 6.7 ± 4.0 mm, p = 0.55), radiographic vasospasm (53% vs 50%, p = 0.88), or clinical vasospasm (12% vs 23%, p = 0.38). PICA patients were more likely to have a fusiform aneurysm (36% vs 12%, p = 0.004) and had a higher incidence of lower cranial nerve dysfunction and higher rate of tracheostomy/percutaneous endoscopic gastrostomy placement compared with non-PICA patients (50% vs 16%, p < 0.001). PICA patients had a significantly higher incidence of poor outcome at discharge (91% vs 67%, p = 0.017), 1-year follow-up (63% vs 29%, p = 0.002), and 3-year follow-up (63% vs 32%, p = 0.006).

CONCLUSIONS

Patients with ruptured PICA aneurysms had a similar rate of radiographic vasospasm, equivalent admission Fisher grade and Hunt and Hess scores, but poorer clinical outcomes at discharge and at 1- and 3-year follow-up when compared with the rest of the BRAT SAH patients with ruptured aneurysms. The PICA's location at the medulla and the resultant high rate of lower cranial nerve dysfunction may play a role in the poor outcome for these patients. Furthermore, PICA aneurysms were more likely to be fusiform than saccular, compared with non-PICA aneurysms; the complex nature of these aneurysms may also contribute to their poorer outcome.