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Hidetoshi Matsukawa, Rokuya Tanikawa, Hiroyasu Kamiyama, Toshiyuki Tsuboi, Kosumo Noda, Nakao Ota, Shiro Miyata, Jumpei Oda, Rihee Takeda, Sadahisa Tokuda and Kyousuke Kamada

OBJECT

The revascularization technique, including bypass created using the external carotid artery (ECA), radial artery (RA), and M2 portion of middle cerebral artery (MCA), has remained indispensable for treatment of complex aneurysms. To date, it remains unknown whether diameters of the RA, superficial temporal artery (STA), and C2 portion of the internal carotid artery (ICA) and intraoperative MCA blood pressure have influences on the outcome and the symptomatic watershed infarction (WI). The aim of the present study was to evaluate the factors for the symptomatic WI and neurological worsening in patients treated by ECA-RA-M2 bypass for complex ICA aneurysm with therapeutic ICA occlusion.

METHODS

The authors measured the sizes of vessels (RA, C2, M2, and STA) and intraoperative MCA blood pressure (initial, after ICA occlusion, and after releasing the RA graft bypass) in 37 patients. Symptomatic WI was defined as presence of the following: postoperative new neurological deficits, WI on postoperative diffusion-weighted imaging, and ipsilateral cerebral blood flow reduction on SPECT. Neurological worsening was defined as the increase in 1 or more modified Rankin Scale scores. First, the authors performed receiver operating characteristic curve analysis for continuous variables and the binary end point of the symptomatic WI. The clinical, radiological, and physiological characteristics of patients with and without the symptomatic WI were compared using the log-rank test. Then, the authors compared the variables between patients with and without neurological worsening at discharge and at the 12-month follow-up examination or last hospital visit.

RESULTS

Symptomatic WI was observed in 2 (5.4%) patients. The mean MCA pressure after releasing the RA graft (< 55 mm Hg; p = 0.017), mean (MCA pressure after releasing the RA graft)/(initial MCA pressure) (< 0.70 mm Hg; p = 0.032), and mean cross-sectional area ratio ([RA/C2 diameter]2 < 0.40 mm [p < 0.0001] and [STA/C2 diameter]2 < 0.044 mm [p < 0.0001]) were related to the symptomatic WI. All preoperatively independent patients remained independent (modified Rankin Scale score < 3). After adjusting for age and sex, left operative side (p = 0.0090 and 0.038) and perforating artery ischemia (p = 0.0050 and 0.022) were related to neurological worsening at discharge (11 [29%] patients) and at the 12-month follow-up or last hospital visit (8 [22%] patients).

CONCLUSIONS

Results of the present study showed that the vessel diameter and intraoperative MCA pressure had impacts on the symptomatic WI and that operative side and perforating artery ischemia were related to neurological worsening in patients with complex ICA aneurysms treated by ECA-RA-M2 bypass.

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Nakao Ota, Rokuya Tanikawa, Hirotake Eda, Takashi Matsumoto, Takanori Miyazaki, Hidetoshi Matsukawa, Takeshi Yanagisawa, Go Suzuki, Shiro Miyata, Jumpei Oda, Kosumo Noda, Toshiyuki Tsuboi, Rihei Takeda, Hiroyasu Kamiyama and Sadahisa Tokuda

OBJECTIVE

Bilateral vertebral artery dissecting aneurysms (VADAs) have a poor prognosis because progressive enlargement of the aneurysms compresses the brainstem or causes subarachnoid hemorrhage. The trapping of 1 vertebral artery (VA) places increased hemodynamic stress on the contralateral VA and may lead to enlargement and rupture. Therefore, management strategies are controversial. This study describes a radical treatment for bilateral VADAs using bypass surgery.

METHODS

Seven patients with bilateral VADAs were included. Three patients were treated by trapping of 1 VA via coiling or clipping at another hospital; the previously treated VA in 1 patient and the contralateral untreated VA in 2 patients subsequently enlarged. The other 4 patients presented without previous intervention and progressive enlargement of the aneurysms.

RESULTS

The post–coil embolization patients underwent V3–posterior cerebral artery (PCA) bypass and trapping. The other 4 patients underwent VA reconstruction via V3–V4 or V4–V4 bypass, with contralateral trapping on a separate day in 3 patients and observation in 1 patient. Perioperative complications included 1 case of cerebrospinal fluid leakage for which the patient required an additional operation, 1 case of dysphagia and facial palsy due to sigmoid sinus thrombosis, and 1 case of dysphagia. The long-term outcomes of these patients were favorable.

CONCLUSIONS

Patients with bilateral VADAs require treatment on both sides. If VA trapping is performed first, the treatment options for the other side are limited to V3-PCA bypass and trapping. This procedure is effective; however, it is also invasive and technically difficult. In cases of bilateral VADAs in which it is feasible to reconstruct 1 side, the best approach is to begin by reconstructing the VA that appears technically easiest, followed by trapping of the contralateral VADA. This strategy allows enough time to suture vessels because contralateral reverse flow is maintained.

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Akshay Sharma, Gabrielle E. Rieth, Joseph E. Tanenbaum, James S. Williams, Nakao Ota, Srikant Chakravarthi, Sunil Manjila, Amin Kassam and Bulent Yapicilar

OBJECTIVE

The middle clinoid process (MCP) is a bony projection that extends from the sphenoid bone near the lateral margin of the sella turcica. The varied prevalence and morphological features of the MCP in populations stratified by age, race, and sex are unknown; however, the knowledge of its anatomy and preoperative recognition on CT scans can aid greatly in complication avoidance and management. The aim of this study was to further illustrate the surgical anatomy of the parasellar region and to quantify the incidence of MCP and caroticoclinoid rings (CCRs) in dried preserved human anatomical specimens.

METHODS

The presence, dimensions, morphological classification (incomplete, contact, and CCR), and intracranial relations of the MCP were measured in 2726 dried skull specimens at the Hamann-Todd Osteological Collection at the Cleveland Museum of Natural History. Specific morphometric data points were recorded from each of these hemiskulls, and categorized based on age, sex, and ethnicity. Linear and logistic regressions were used to determine associations between explanatory variables and MCP morphology. Computed tomography scans of the skull specimens were obtained to explore radiological landmarks for different types of MCPs. Illustrative intraoperative videos were also analyzed in the light of these crucial surgical landmarks.

RESULTS

The sample included 2250 specimens from males and 476 from females. Specimens were classified as either “white” (60.5%) or “black” (39.2%). An MCP was found in 42% of specimens, with 60% of those specimens presenting bilaterally. Fully ossified CCR comprised 27% of all MCPs, and contact (defined as contact without ossification between MCP and anterior clinoid process) comprised 4% of all MCPs. White race (relative to black race) and increasing age were significant predictors of MCP presence (p < 0.001). White race was significantly associated with greater average MCP height (p < 0.001). Among skulls with CCR, both male sex and older age (> 70 years relative to < 50 years) were associated with increased CCR diameter (p < 0.001). No other significant predictors or associations were observed. The CT scans of skulls replicated and validated the authors’ morphometric observations on incomplete, contact, and CCR patterns adequately. The surgical strategies of clinoid bone removal are validated, with appropriate video illustrations.

CONCLUSIONS

Variations in the patterns of bony MCPs can pose a significant risk for injury to the internal carotid artery during parasellar procedures, especially those involving clinoidectomy and optic strut drilling. Understanding parasellar anatomy, especially on skull-base CT imaging, may be integral to surgical planning and preoperative risk counseling in both transcranial and extended endonasal procedures, as well as to preparing for complications management perioperatively.

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Hidetoshi Matsukawa, Hiroyasu Kamiyama, Toshiyuki Tsuboi, Kosumo Noda, Nakao Ota, Shiro Miyata, Takanori Miyazaki, Yu Kinoshita, Norihiro Saito, Osamu Takahashi, Rihee Takeda, Sadahisa Tokuda and Rokuya Tanikawa

OBJECTIVE

Only a few previous studies have investigated subarachnoid hemorrhage (SAH) after surgical treatment in patients with unruptured intracranial aneurysms (UIAs). Given the improvement in long-term outcomes of embolization, more extensive data are needed concerning the true rupture rates after microsurgery in order to provide reliable information for treatment decisions. The purpose of this study was to investigate the incidence of and risk factors for postoperative SAH in patients with surgically treated UIAs.

METHODS

Data from 702 consecutive patients harboring 852 surgically treated UIAs were evaluated. Surgical treatments included neck clipping (complete or incomplete), coating/wrapping, trapping, proximal occlusion, and bypass surgery. Clippable UIAs were defined as UIAs treated by complete neck clipping. The annual incidence of postoperative SAH and risk factors for SAH were studied using Kaplan-Meier survival analysis and Cox proportional hazards regression models.

RESULTS

The patients’ median age was 64 years (interquartile range [IQR] 56–71 years). Of 852 UIAs, 767 were clippable and 85 were not. The mean duration of follow-up was 731 days (SD 380 days). During 1708 aneurysm years, there were 4 episodes of SAH, giving an overall average annual incidence rate of 0.23% (95% CI 0.12%–0.59%) and an average annual incidence rate of 0.065% (95% CI 0.0017%–0.37%) for clippable UIAs (1 episode of SAH, 1552 aneurysm-years). Basilar artery location (adjusted hazard ratio [HR] 23, 95% CI 2.0–255, p = 0.0012) and unclippable UIA status (adjusted HR 15, 95% CI 1.1–215, p = 0.046) were significantly related to postoperative SAH. An excellent outcome (modified Rankin Scale score of 0 or 1) was achieved in 816 (95.7%) of 852 cases overall and in 748 (98%) of 767 clippable UIAs at 12 months.

CONCLUSIONS

In this large case series, microsurgical treatment of UIAs was found to be safe and effective. Aneurysm location and unclippable morphologies were related to postoperative SAH in patients with surgically treated UIAs.

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Hidetoshi Matsukawa, Shiro Miyata, Toshiyuki Tsuboi, Kosumo Noda, Nakao Ota, Osamu Takahashi, Rihee Takeda, Sadahisa Tokuda, Hiroyasu Kamiyama and Rokuya Tanikawa

OBJECTIVE

After internal carotid artery (ICA) sacrifice without revascularization for complex aneurysms, ischemic complications can occur. In addition, hemodynamic alterations in the circle of Willis create conditions conducive to the formation of de novo aneurysms or the enlargement of existing untreated aneurysms. Therefore, the revascularization technique remains indispensable. Because vessel sizes and the development of collateral circulation are different in each patient, the ideal graft size to prevent low flow–related ischemic complications (LRICs) in external carotid artery (ECA)–middle cerebral artery (MCA) bypass with therapeutic ICA occlusion (ICAO) has not been well established. Authors of this study hypothesized that the adequate graft size could be calculated from the size of the sacrificed ICA and the values of MCA pressure (MCAP) and undertook an investigation in patients with complex ICA aneurysms treated with ECA-graft-MCA bypass and therapeutic ICAO.

METHODS

In the period between July 2006 and January 2016, 80 patients with complex ICA aneurysms were treated with ECA-MCA bypass and therapeutic ICAO. Preoperative balloon test occlusion (BTO) was performed, and the BTO pressure ratio was defined as the mean stump pressure/mean preocclusion pressure. Low flow–related ischemic complications were defined as new postoperative neurological deficits and ipsilateral cerebral blood flow reduction. Initial MCAP (iMCAP), MCAP after clamping the ICA (cMCAP), and MCAP after releasing the graft (gMCAP) were intraoperatively monitored. The MCAP ratio was defined as gMCAP/iMCAP. Based on the Hagen-Poiseuille law, the expected MCAP ratio ([expected gMCAP]/iMCAP) was hypothesized as follows: (1 – cMCAP/iMCAP)(graft radius/ICA radius)2 + (cMCAP/iMCAP). Correlations between the BTO pressure ratio and cMCAP/iMCAP, and between the actual and expected MCAP ratios, were evaluated. Risk factors for LRICs were also evaluated.

RESULTS

The mean BTO pressure ratio was significantly correlated with the mean cMCAP/iMCAP (r = 0.68, p < 0.0001). The actual MCAP ratio correlated with the expected MCAP ratio (r = 0.43, p < 0.0001). If the expected MCAP ratio was set up using the BTO pressure ratio instead of cMCAP/iMCAP (BTO-expected MCAP ratio), the mean BTO-expected MCAP ratio significantly correlated with the expected MCAP ratio (r = 0.95, p < 0.0001). During a median follow-up period of 26.1 months, LRICs were observed in 9 patients (11%). An actual MCAP ratio < 0.80 (p = 0.003), expected MCAP ratio < 0.80 (p = 0.001), and (M2 radius/graft radius)2 < 0.49 (p = 0.002) were related to LRICs according to the Cox proportional-hazards model.

CONCLUSIONS

Data in the present study indicated that it was important to use an adequate graft to achieve a sufficient MCAP ratio in order to avoid LRICs and that the adequate graft size could be evaluated based on a formula in patients with complex ICA aneurysms treated with ICAO.

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Hidetoshi Matsukawa, Hiroyasu Kamiyama, Takanori Miyazaki, Yu Kinoshita, Nakao Ota, Kosumo Noda, Takaharu Shonai, Osamu Takahashi, Sadahisa Tokuda and Rokuya Tanikawa

OBJECTIVE

Perforator territory infarction (PTI) is still a major problem needing to be solved to achieve good outcomes in aneurysm surgery. However, details and risk factors of PTI diagnosed on postoperative MRI remain unknown. The authors aimed to investigate the details of PTI on postoperative diffusion-weighted imaging (DWI) in patients with surgically treated unruptured intracranial saccular aneurysms (UISAs).

METHODS

The data of 848 patients with 1047 UISAs were retrospectively evaluated. PTI was diagnosed on DWI, which was performed the day after aneurysm surgery. Clinical and radiological characteristics were compared between UISAs with and without PTI. Poor outcome was defined as an increase in 1 or more modified Rankin Scale scores at 12 months after aneurysm surgery.

RESULTS

Postoperative DWI was performed in all cases, and it revealed PTI in 56 UISA cases (5.3%). Forty-three PTIs occurred without direct injury and occlusion of perforators (43 of 56, 77%). Poor outcome was more frequently observed in the PTI group (17 of 56, 30%) than the non-PTI group (57 of 1047, 5.4%) (p < 0.0001). Thalamotuberal arteries (p < 0.01), lateral striate arteries (p < 0.01), Heubner’s artery (p < 0.01), anterior median commissural artery (p < 0.05), terminal internal carotid artery perforators (p < 0 0.01), and basilar artery perforator (p < 0 0.01) infarctions were related to poor outcome by adjusted residual analysis. On multivariate analysis, statin use (OR 10, 95% CI, 3.3–31; p < 0.0001), specific aneurysm locations (posterior communicating artery [OR 4.1, 95% CI 2.1–8.1; p < 0.0001] and basilar artery [OR 3.1, 95% CI 1.1–8.9; p = 0.031]), larger aneurysm size (OR 1.1, 95% CI 1.1–1.2; p = 0.043), and permanent decrease of motor evoked potential (OR 38, 95% CI 3.1–468; p = 0.0045) were related to PTI.

CONCLUSIONS

Despite efforts to avoid PTI, it occurred even without direct injury, occlusion of perforators, or evoked potential abnormality. Therefore, surgical treatment of UISAs, especially with the aforementioned risk factors of PTI, should be more carefully considered. The evaluation of PTI in the territory of the above-mentioned perforators could be useful in helping predict the clinical course in patients after aneurysm surgery.

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Hidetoshi Matsukawa, Hiroyasu Kamiyama, Yu Kinoshita, Norihiro Saito, Yuto Hatano, Takanori Miyazaki, Nakao Ota, Kosumo Noda, Takaharu Shonai, Osamu Takahashi, Sadahisa Tokuda and Rokuya Tanikawa

OBJECTIVE

It is well known that larger aneurysm size is a risk factor for poor outcome after surgical treatment of unruptured saccular intracranial aneurysms (USIAs). However, the authors have occasionally observed poor outcome in the surgical treatment of small USIAs and hypothesized that size ratio has a negative impact on outcome. The aim of this paper was to investigate the influence of size ratio on outcome in the surgical treatment of USIAs.

METHODS

Prospectively collected clinical and radiological data of 683 consecutive patients harboring 683 surgically treated USIAs were evaluated. Dome-to-neck ratio was defined as the ratio of the maximum width of the aneurysm to the average neck diameter. The aspect ratio was defined as the ratio of the maximum perpendicular height of the aneurysm to the average neck diameter of the aneurysm. The size ratio was calculated by dividing the maximum aneurysm diameter (height or width, mm) by the average parent artery diameter (mm). Neurological worsening was defined as an increase in modified Rankin Scale score of 1 or more points at 12 months. Clinical and radiological variables were compared between patients with and without neurological worsening.

RESULTS

The median patient age was 64 years (IQR 56–71 years), and 528 (77%) patients were female. The median maximum size, dome-to-neck ratio, aspect ratio, and size ratio were 4.7 mm (IQR 3.6–6.7 mm), 1.2 (IQR 1.0–1.4), 1.0 (IQR 0.76–1.3), and 1.9 (IQR 1.4–2.8), respectively. The size ratio was significantly correlated with maximum size (r = 0.83, p < 0.0001), dome-to-neck ratio (r = 0.69, p < 0.0001), and aspect ratio (r = 0.74, p < 0.0001). Multivariate logistic regression analysis showed that the specific USIA location (paraclinoid segment of the internal carotid artery: OR 6.2, 95% CI 2.6–15, p < 0.0001; and basilar artery: OR 8.4, 95% CI 2.8–25, p < 0.0001), size ratio (OR 1.3, 95% CI 1.1–1.6, p = 0.021), and postoperative ischemic lesion (OR 9.4, 95% CI 4.4–19, p < 0.0001) were associated with neurological worsening (n = 52, 7.6%), and other characteristics showed no significant differences.

CONCLUSIONS

The present study showed that size ratio, and not other morphological parameters, was a risk factor for 12-month neurological worsening in surgically treated patients with USIAs. The size ratio should be further studied in a large, prospective observational cohort to predict neurological worsening in the surgical treatment of USIAs.