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Pharyngeal motor evoked potentials elicited by transcranial electrical stimulation for intraoperative monitoring during skull base surgery

Clinical article

Masafumi Fukuda, Makoto Oishi, Tetsuya Hiraishi, Akihiko Saito, and Yukihiko Fujii


The purpose of this study was to determine whether monitoring of pharyngeal motor evoked potentials (PhMEPs) elicited by transcranial electrical stimulation during skull base tumor surgery might be useful for predicting postoperative swallowing deterioration.


The authors analyzed PhMEPs in 21 patients during 22 surgical procedures for the treatment of skull base tumors. Corkscrew electrodes positioned at C3 or C4 and Cz were used to deliver supramaximal stimuli (220–550 V). Pharyngeal MEPs were recorded from the posterior wall of the pharynx through a modified endotracheal tube. The correlation between the final/baseline PhMEP ratio and postoperative swallowing function was examined.


Postoperative swallowing function was significantly (p < 0.05), although not strongly (r = −0.47), correlated with the final/baseline PhMEP ratio. A PhMEP ratio < 50% was recorded during 4 of 22 procedures; in all 4 of these cases, the patients experienced postoperative deterioration of swallowing function. After 18 procedures, the PhMEP ratios remained > 50%; nevertheless, after 4 (22.2%) of these 18 procedures, patients showed deterioration of swallowing function.


Intraoperative PhMEP monitoring can be useful for predicting swallowing deterioration following skull base surgery, especially in patients with swallowing disturbances that are mainly due to reduction in the motor functions of the pharyngeal muscles.

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Three-dimensional anisotropy contrast magnetic resonance axonography to predict the prognosis for motor function in patients suffering from stroke

Toru Watanabe, Yoshiho Honda, Yukihiko Fujii, Miyako Koyama, Hitoshi Matsuzawa, and Ryuichi Tanaka

Object. The purpose of this study was to assess how early wallerian degeneration in the corticospinal tracts of patients who had suffered from stroke was detected using three-dimensional anisotropy contrast (3D-AC) magnetic resonance (MR) axonography and to explore the possibility of predicting the prognosis for motor function in these patients.

Methods. Ten healthy volunteers and 16 stroke patients with hemiparesis were studied using MR images including 3D-AC MR axonography images obtained using a 1.5-tesla MR imaging system. The axonography was performed using an echoplanar imaging method. All patients underwent MR studies 2, 3, and 10 weeks after stroke onset. To detect wallerian degeneration, the diffusion anisotropy in the corticospinal tracts at the level of the upper pons was evaluated on axial images. These MR findings were compared with the patients' motor functions, which were classified according to the Brunnstrom criteria 12 weeks after the onset of stroke.

In all patients with poor recovery (Brunnstrom Stages I–IV), wallerian degeneration, which was demonstrated as a reduction in diffusion anisotropy on axonography images, could be observed in the corticospinal tracts; this degeneration was not found in patients with good recovery (Stages V and VI). Axonography could be used to detect degeneration between 2 and 3 weeks after stroke onset. On conventional T2-weighted MR images, hyperintense areas indicating wallerian degeneration were not detected until 10 weeks after stroke onset.

Conclusions. With the aid of 3D-AC MR axonography, wallerian degeneration can be detected in the corticospinal tracts during the early stage of stroke (2–3 weeks after onset), much earlier than it can be detected using T2-weighted MR imaging. The procedure of 3D-AC MR axonography may be useful in predicting motor function prognosis in stroke patients.

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High-field magnetic resonance imaging in patients with moyamoya disease

Atsuko Harada, Yukihiko Fujii, Yuichiro Yoneoka, Shigekazu Takeuchi, Ryuichi Tanaka, and Tsutomu Nakada

Object. The purpose of this study was to assess the utility of high-field magnetic resonance (MR) imaging as a quantitative tool for estimating cerebral circulation in patients with moyamoya disease.

Methods. Eighteen patients with moyamoya disease who were scheduled to undergo revascularization surgery and 100 healthy volunteers were examined using T2-reversed MR imaging performed using a 3-tesla system. Ten of the 18 patients underwent a second study between 1 year and 3 years after revascularization. Magnetic resonance images obtained in the patients with moyamoya disease were statistically analyzed and compared with those obtained in healthy volunteers. The MR imaging findings were also correlated with results of single-photon emission computerized tomography and conventional cerebral angiography studies.

Transverse lines in the white matter (medullary streaks) were observed in almost all persons. In healthy volunteers, the diameter sizes of the medullary streaks increased significantly with age (p < 0.001). Multiple logistic regression analysis revealed that age-adjusted medullary streak diameters were significantly larger in patients with moyamoya disease (p < 0.001). Diameter sizes also increased significantly with the increased severity of cerebral hypoperfusion (p < 0.001) and a higher angiographically determined stage of the disease (p < 0.001). Diameter sizes decreased significantly after surgery (p < 0.001).

Conclusions. The increases in medullary streak diameters observed in patients with moyamoya disease appear to represent vessels dilated due to cerebral hypoperfusion. High-field T2-reversed MR imaging is useful in estimating cerebral circulation in patients with moyamoya disease.

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Ultra-early rebleeding in spontaneous subarachnoid hemorrhage

Yukihiko Fujii, Shigekazu Takeuchi, Osamu Sasaki, Takashi Minakawa, Tetsuo Koike, and Ryuichi Tanaka

✓ To determine the incidence of, and risk factors for, the occurrence of rebleeding between admission and early operation (ultra-early rebleeding) in patients with spontaneous subarachnoid hemorrhage (SAH), the authors reviewed the cases of 179 patients admitted within 24 hours after their last attack of SAH. Thirty-one (17.3%) of these patients had ultra-early rebleeding despite scheduling of early operation (within 24 hours after admission). The incidence of rebleeding significantly decreased as the time interval between the last attack and admission increased. Patients with rebleeding before admission, high systolic blood pressure, intracerebral or intraventricular hematoma, those in poor neurological condition on admission, and those who underwent angiography within 6 hours of the last SAH were significantly more likely to have ultra-early rebleeding than those without these factors. The incidence of rebleeding also significantly increased as levels of enhancement of platelet sensitivity and thrombin—antithrombin complex increased. Multivariate analysis revealed that the following three factors were independently associated with ultra-early rebleeding: the level of enhancement of platelet sensitivity; the time interval between the last attack and admission; and the level of thrombin—antithrombin complex. On the basis of these findings, the authors suggest that many of the risk factors for ultra-early rebleeding are interrelated. A particularly high risk of ultra-early rebleeding was observed in those patients 1) who had platelet hypoaggregability; 2) who were admitted shortly after their last SAH; and 3) whose thrombin—antithrombin complex levels were extremely high and were thus in severe clinical condition.

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Hematoma enlargement in spontaneous intracerebral hemorrhage

Yukihiko Fujii, Ryuichi Tanaka, Shigekazu Takeuchi, Tetsuo Koike, Takashi Minakawa, and Osamu Sasaki

✓ In order to evaluate the incidence and risk factors of hematoma enlargement in spontaneous intracerebral hemorrhage (ICH), 419 cases of ICH were reviewed. The first computerized tomography (CT) scan was performed within 24 hours of onset and the second within 24 hours of admission; a blood sample was taken for laboratory examination within 1 hour of admission. In 60 patients (14.3%) the second CT scan showed an enlarged hematoma. The incidence of enlargement significantly decreased with time (p < 0.05) and significantly increased with the severity of liver dysfunction and the volume of the hematoma on the first CT scan. Patients with an irregularly shaped hematoma had a higher risk of hematoma growth than those with a round hematoma. In addition, patients with hematoma enlargement were more likely to have coagulation abnormalities (low platelet counts and low levels of fibrinogen, α2-antiplasmin activity and platelet aggregation). Moreover, hematoma growth was associated with a poor clinical outcome.

It is concluded that patients admitted to a hospital within 6 hours of onset of ICH, especially those admitted within 2 hours, and patients with liver dysfunction or irregularly shaped large hematomas should be closely observed for at least 6 hours after onset in preparation for emergency surgery, since the risk of hematoma growth in these circumstances is high.

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Serial changes of hemostasis in aneurysmal subarachnoid hemorrhage with special reference to delayed ischemic neurological deficits

Yukihiko Fujii, Shigekazu Takeuchi, Osamu Sasaki, Takashi Minakawa, Tetsuo Koike, and Ryuichi Tanaka

✓ This study was undertaken to elucidate comprehensively the serial changes occurring in hemostatic systems after aneurysmal subarachnoid hemorrhage (SAH) and thereby to ascertain whether the examination of the integrity of these systems is helpful in predicting delayed ischemic neurological deficits (DINDs). The authors examined 117 patients admitted to the hospital within 24 hours after onset of SAH. Blood samples were collected from each patient on Days 0 (at admission), 3, 6, 14, and 30. A number of hemostatic parameters were examined in these samples, and the relationships between their changes and DINDs were assessed. Eighteen (15.4%) of the patients exhibited DINDs, and their frequency increased as the severity of subarachnoid clotting increased. Also, the frequency of DINDs was significantly higher in the patients with hydrocephalus on initial computerized tomography (CT) scans than in those without hydrocephalus. Regarding the hemostatic parameters at admission, there was no significant difference between the patients with and without DINDs. On Day 3, however, the fibrinogen and D-dimer levels were higher in the patients with than in those without DINDs. The fibrinogen and thrombin—antithrombin complex levels on Day 6 and the D-dimer level on Day 14 in the patients with DINDs were higher than the corresponding levels in those without DINDs. Multivariate analyses revealed that the following variables (in order of importance) were independent predictors of DINDs: the levels of D-dimer on Day 3, fibrinogen on Day 6, and the presence of hydrocephalus on admission. These data indicate that the levels of hemostatic parameters in concert with the CT findings may enable us to predict the appearance of DINDs.

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Diffusion tensor analysis of peritumoral edema using lambda chart analysis indicative of the heterogeneity of the microstructure within edema

Ken-ichi Morita, Hitoshi Matsuzawa, Yukihiko Fujii, Ryuichi Tanaka, Ingrid L. Kwee, and Tsutomu Nakada

Object. Histopathological studies indicate that cerebral edema associated with tumors (peritumoral edema) does not represent a single pathophysiological or clinical entity. In this study the authors investigated peritumoral edema by performing lambda chart analysis (LCA), a noninvasive technique that can be used to make visible and analyze apparent water diffusivity in tissues in vivo, and assessed the utility of LCA in differentiating high-grade gliomas from nonglial tumors.

Methods. The water diffusivity characteristics of peritumoral edema associated with four tumor groups—12 high-grade gliomas, five low-grade gliomas, 11 metastatic tumors, and 15 meningiomas—were assessed in 43 patients by performing magnetic resonance imaging with the aid of a 3-tesla magnetic resonance imaging system. In all tumor groups, peritumoral edema exhibited greater trace values and reduced anisotropy compared with normal white matter. Edema associated with high-grade gliomas had significantly higher trace values than edema associated with the other three tumor groups, although the anisotropic angles of those groups were comparable.

Conclusions. Lambda chart analysis identified two distinct types of peritumoral edema: edema associated with high-grade gliomas and edema associated with low-grade gliomas or nonglial tumors. The apparent water diffusivity was significantly greater in high-grade gliomas, whereas the anisotropy in these lesions was comparable to that of edema in other tumors. These findings indicated that water movement in areas of edema, predominantly in the extracellular spaces, was less restricted in high-grade gliomas, a phenomenon that likely reflected the destruction of the extracellular matrix ultrastructure by malignant cell infiltration and consequently greater water diffusion. Although preliminary, this study indicates that LCA could be used as a clinical tool for differentiating high-grade gliomas and for evaluating the extent of cellular infiltration.

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Blood pressure in the artery distal to an intraarterial embolus during thrombolytic therapy for occlusion of a major artery: a predictor of cerebral infarction following good recanalization

Takatoshi Sorimachi, Yukihiko Fujii, Naoto Tsuchiya, Takeo Nashimoto, Masatsune Saito, Kenichi Morita, Yasushi Ito, and Ryuichi Tanaka

Object. The aim in this study was the investigation of back pressure in arteries distal to the occlusion site during intraarterial thrombolysis as well as the usefulness of back pressure measurement in combination with diffusion-weighted (DW) magnetic resonance (MR) imaging to predict the occurrence of ischemic lesions following good recanalization.

Methods. Twenty-five consecutive patients with severe hemiparesis caused by embolism of the internal carotid artery (10 patients) and the proximal middle cerebral artery (15 patients) were treated using intraarterial thrombolysis. Systolic back pressure, measured through a microcatheter in the artery just distal to the emboli, ranged from 22 to 78 mm Hg. According to an angiographic inclusion criterion for good recanalization—that is, recanalization of the M2 or more distal arteries at the end of thrombolysis—21 of 25 patients underwent evaluation in this study. In 14 patients volumes of low-density areas on computerized tomography (CT) scans obtained 2 months postthrombolysis were smaller in comparison with volumes of hyperintense areas on DW MR images acquired before treatment, whereas these low-density areas were larger in seven patients. Compared with those on initial DW MR images, the volume of abnormalities on CT scans obtained 2 months posttreatment were significantly reduced in patients with a systolic back pressure greater than 30 mm Hg (16 patients) than in those with a back pressure of 30 mm Hg or less (five patients) (p < 0.05). Systolic back pressures greater than 30 mm Hg were associated with significantly better modified Rankin Scale scores than those 30 mm Hg or less (p < 0.05).

Conclusions. Back pressure measurement in combination with DW MR imaging can be used to predict the occurrence of infarction as demonstrated on CT scans following thrombolysis.

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Serial evaluation of axonal function in patients with brain death by using anisotropic diffusion-weighted magnetic resonance imaging

Toru Watanabe, Yoshiho Honda, Yukihiko Fujii, Miyako Koyama, and Ryuichi Tanaka

Object. The purposes of this study were to evaluate the serial changes in diffusion anisotropy of the brain, probably reflecting axonal function in brain-dead patients, and thus to explore the possibility of quantitatively estimating the risk of brain death.

Methods. Ten patients suffering from stroke with or without impending brain death and 10 healthy volunteers were studied using three-dimensional anisotropy contrast (3DAC) magnetic resonance (MR) axonography with the aid of a 1.5-tesla MR imaging system. To detect changes in the diffusion anisotropy of neural bundles, the corticospinal tract was evaluated.

Diffusion anisotropy of short axonal fibers decreased immediately after apparent brain death. Whereas the trichromatic coefficients of the corticospinal tract greatly diminished between 6 and 12 hours after apparent brain death, the coefficients of the corpus callosum and the optic radiation decreased in less time, that is, between 1 and 6 hours. The coefficients of these three bundles turned isotropic between 24 and 44 hours after apparent brain death.

Conclusions. Results of 3DAC MR axonography revealed that diffusion anisotropy of neural bundles diminished between 1 and 12 hours after the onset of apparent brain death, probably depending on the length of the bundles, and disappeared between 24 and 44 hours after the onset of brain death, which might reflect dynamic changes of axonal structure and indirectly herald axonal dysfunction. These findings seem to be greatly helpful in establishing an appropriate method to estimate the risk of brain death quantitatively and in forming the basis of future definitions of brain death.

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Interactive presurgical simulation applying advanced 3D imaging and modeling techniques for skull base and deep tumors

Clinical article

Makoto Oishi, Masafumi Fukuda, Naoki Yajima, Kenzo Yoshida, Machiko Takahashi, Tetsuya Hiraishi, Tetsuro Takao, Akihiko Saito, and Yukihiko Fujii


In this paper, the authors' goal was to report their novel presurgical simulation method applying interactive virtual simulation (IVS) using 3D computer graphics (CG) data and microscopic observation of color-printed plaster models based on these CG data in surgery for skull base and deep tumors.


For 25 operations in 23 patients with skull base or deep intracranial tumors (meningiomas, schwannomas, epidermoid tumors, chordomas, and others), the authors carried out presurgical simulation based on 3D CG data created by image analysis for radiological data. Interactive virtual simulation was performed by modifying the 3D CG data to imitate various surgical procedures, such as bone drilling, brain retraction, and tumor removal, with manipulation of a haptic device. The authors also produced color-printed plaster models of modified 3D CG data by a selective laser sintering method and observed them under the operative microscope.


In all patients, IVS provided detailed and realistic surgical perspectives of sufficient quality, thereby allowing surgeons to determine an appropriate and feasible surgical approach. Surgeons agreed that in 44% of the 25 operations IVS showed high utility (as indicated by a rating of “prominent”) in comprehending 3D microsurgical anatomies for which reconstruction using only 2D images was complicated. Microscopic observation of color-printed plaster models in 12 patients provided further utility in confirming realistic surgical anatomies.


The authors' presurgical simulation method applying advanced 3D imaging and modeling techniques provided a realistic environment for practicing microsurgical procedures virtually and enabled the authors to ascertain complex microsurgical anatomy, to determine the optimal surgical strategies, and also to efficiently educate neurosurgical trainees, especially during surgery for skull base and deep tumors.