Fredric B. Meyer
Roberto C. Heros
Tomohito Hishikawa, Koji Iihara, Naoaki Yamada, Hatsue Ishibashi-Ueda and Susumu Miyamoto
The aim of this study was to assess the histopathological differences between advanced atherosclerotic carotid artery (CA) plaques with signal hyperintensity on T1-weighted MR images and those without, focusing on necrotic core size and intraplaque hemorrhage (IPH).
Thirty-five patients scheduled for carotid endarterectomy underwent preoperative CA MR imaging using 3D inversion-recovery-based T1-weighted imaging (magnetization-prepared rapid acquisition gradient-echo [MPRAGE]). The signal intensity of the CA plaque on MPRAGE sequences was classified as “high” when the intensity was more than 200% that of adjacent muscle. A total of 96 axial MR images obtained in 35 patients were compared with corresponding histological sections from 36 excised specimens. The area of the necrotic core in histological sections was compared between specimens with and without high signal intensity on MPRAGE sequences. The IPH was histopathologically graded according to the size of the area positive for glycophorin A as revealed by immunohistochemical staining. The difference between plaques with and without high signal intensity was investigated with respect to the degree of IPH. The relationship of the severity of IPH to size of the necrotic core was also evaluated.
The area of the necrotic core in plaques with high signal intensity on MPRAGE sequences was significantly larger than that in plaques without high signal intensity (median 51.2% [interquartile range 43.3–66.8%] vs 49.0% [33.2–57.6%], p = 0.029). Carotid artery plaques with high signal intensity had significantly more severe IPH than plaques with lower signal intensity (p < 0.0001). The severity of IPH was significantly associated with the size of the necrotic core (p < 0.0001).
Atherosclerotic CA plaques with high signal intensity on MPRAGE sequences had large necrotic cores with IPH in patients with high-grade stenosis; MPRAGE is useful for the evaluation of CA plaque progression.
Susumu Miyamoto, Takeshi Funaki, Koji Iihara and Jun C. Takahashi
The authors evaluated the efficacy of a new flow reduction strategy for giant partially thrombosed upper basilar artery (BA) aneurysms, for which proximal parent artery occlusion is not always effective.
Eight consecutive patients with severely symptomatic, partially thrombosed, giant upper BA aneurysms were treated with a tailored flow reduction strategy, or received conservative therapies. The flow reduction strategy comprised isolation of several branches from the upper BA at their origins with bypasses in addition to parent artery occlusion.
The median follow-up period of all 8 patients was 15.0 months (range 4–31 months). In 6 patients treated with flow reduction, the mean decrease in residual blood lumen was −10.7 mm (95% CI −19.7 to −1.7 mm; p = 0.029) and the mean decrease in diameter of the aneurysms was −11.5 mm (95% CI −25.1 to 2.1 mm; p = 0.082). Complete or virtually complete thrombosis was achieved in all but 1 aneurysm (83%) and shrinkage was observed in 4 (67%). In those in whom complete or virtually complete thrombosis was achieved, significant shrinkage of the aneurysm was observed (mean decrease in diameter −14.8 mm; 95% CI −28.8 to −0.8 mm; p = 0.043). Improvement or stabilization of symptoms occurred in 67% of the patients who received flow reduction treatment. Both patients who received conservative treatment had unfavorable outcomes.
The flow reduction strategy is effective at promoting complete thrombosis of the aneurysm. This strategy can also induce shrinkage of the aneurysm if successful thrombosis is achieved. Although the neurological outcome of the treatment appears favorable considering its intractable nature, further study of the treatment is necessary to confirm its clinical efficacy and safety.
Eika Hamano, Hiroharu Kataoka, Naomi Morita, Daisuke Maruyama, Tetsu Satow, Koji Iihara and Jun C. Takahashi
Transient neurological symptoms are frequently observed during the early postoperative period after direct bypass surgery for moyamoya disease. Abnormal signal changes in the cerebral cortex can be seen in postoperative MR images. The purpose of this study was to reveal the radiological features of the “cortical hyperintensity belt (CHB) sign” in postoperative FLAIR images and to verify its relationship to transient neurological events (TNEs) and regional cerebral blood flow (rCBF).
A total of 141 hemispheres in 107 consecutive patients with moyamoya disease who had undergone direct bypass surgery were analyzed. In all cases, FLAIR images were obtained during postoperative days (PODs) 1–3 and during the chronic period (3.2 ± 1.13 months after surgery). The CHB sign was defined as an intraparenchymal high-intensity signal within the cortex of the surgically treated hemisphere with no infarction or hemorrhage present. The territory of the middle cerebral artery was divided into anterior and posterior parts, with the extent of the CHB sign in each part scored as 0 for none; 1 for presence in less than half of the part; and 2 for presence in more than half of the part. The sum of these scores provided the CHB score (0–4). TNEs were defined as reversible neurological deficits detected both objectively and subjectively. The rCBF was measured with SPECT using N-isopropyl-p-[123I]iodoamphetamine before surgery and during PODs 1–3. The rCBF increase ratio was calculated by comparing the pre- and postoperative count activity.
Cortical hyperintensity belt signs were detected in 112 cases (79.4%) and all disappeared during the chronic period. Although all bypass grafts were anastomosed to the anterior part of the middle cerebral artery territory, CHB signs were much more pronounced in the posterior part (p < 0.0001). TNEs were observed in 86 cases (61.0%). Patients with TNEs showed significantly higher CHB scores than those without (2.31 ± 0.13 vs 1.24 ± 0.16, p < 0.0001). The CHB score, on the other hand, showed no relationship with the rCBF increase ratio (p = 0.775). In addition, the rCBF increase ratio did not differ between those patients with TNEs and those without (1.15 ± 0.033 vs 1.16 ± 0.037, p = 0.978).
The findings strongly suggest that the presence of the CHB sign during PODs 1–3 can be a predictor of TNEs after bypass surgery for moyamoya disease. On the other hand, presence of this sign appears to have no direct relationship with the postoperative local hyperperfusion phenomenon. Vasogenic edema can be hypothesized as the pathophysiology of the CHB sign, because the sign was transient and never accompanied by infarction in the present series.
Hiroyuki Hao, Koji Iihara, Hatsue Ishibashi-Ueda, Fumio Saito and Seiichi Hirota
Preoperative clinical risk classification of carotid artery (CA) stenosis anticipates the outcome of CA intervention. A higher incidence of neurological morbidity was noted after CA stenting (CAS) in patients with medical risks than in those without risks. However, little is known about the correlation between clinical risks and plaque composition. The purpose of this study was to characterize the CA plaque histology in 3 groups of patients who were classified based on clinical risks for carotid endarterectomy (CEA). Furthermore, the authors examined whether the plaque with high embolic potential after CA intervention, particularly CAS, could be predicted based on clinical risks for CEA.
Patients were divided into 4 groups, according to the CEA risk classification system, and 3 groups with more than 10 cases were enrolled in this study as follows: absence of all angiographic, medical, and neurological risks (Grade I, 27 cases); presence of medical risk, but no neurological risk (Grade III, 31 cases); and presence of neurological risk (Grade IV, 17 cases). Histopathological characteristics of CA plaques, including fibrous cap thickness, plaque disruption, thrombus formation, intraplaque hemorrhage (IPH), and adipophilin expression were examined without information regarding clinical status.
Plaques in patients in Grades III and IV demonstrated a thin fibrous cap and enhanced IPH, compared with those in Grade I. Plaques in patients in Grade IV showed more adipophilin-expressing macrophages in the fibrous cap than in those of the other groups.
Plaques in Grades III and IV patients were characterized by thin fibrous cap atheroma with IPH. Adipophilin-positive macrophage infiltration in the fibrous cap might be correlated with instability in neurological status. The plaque morphology in patients with medical and neurological risks needs to be examined carefully with the aid of imaging modalities. In plaques demonstrating a thin fibrous cap and IPH, the CAS procedure should be avoided and CEA should be performed instead.
Satoshi Matsuo, Serhat Baydin, Abuzer Güngör, Erik H. Middlebrooks, Noritaka Komune, Koji Iihara and Albert L. Rhoton Jr.
A postoperative visual field defect resulting from damage to the occipital lobe during surgery is a unique complication of the occipital transtentorial approach. Though the association between patient position and this complication is well investigated, preventing the complication remains a challenge. To define the area of the occipital lobe in which retraction is least harmful, the surface anatomy of the brain, course of the optic radiations, and microsurgical anatomy of the occipital transtentorial approach were examined.
Twelve formalin-fixed cadaveric adult heads were examined with the aid of a surgical microscope and 0° and 45° endoscopes. The optic radiations were examined by fiber dissection and MR tractography techniques.
The arterial and venous relationships of the lateral, medial, and inferior surfaces of the occipital lobe were defined anatomically. The full course of the optic radiations was displayed via both fiber dissection and MR tractography. Although the stems of the optic radiations as exposed by both techniques are similar, the terminations of the fibers are slightly different. The occipital transtentorial approach provides access for the removal of lesions involving the splenium, pineal gland, collicular plate, cerebellomesencephalic fissure, and anterosuperior part of the cerebellum. An angled endoscope can aid in exposing the superior medullary velum and superior cerebellar peduncles.
Anatomical findings suggest that retracting the inferior surface of the occipital lobe may avoid direct damage and perfusion deficiency around the calcarine cortex and optic radiations near their termination. An accurate understanding of the course of the optic radiations and vascular relationships around the occipital lobe and careful retraction of the inferior surface of the occipital lobe may reduce the incidence of postoperative visual field defect.
Koji Iihara, Masakazu Okawa, Tomohito Hishikawa, Naoaki Yamada, Kazuhito Fukushima, Hidehiro Iida and Susumu Miyamoto
The authors report a rare case of slowly progressive neuronal death associated with postischemic hyperperfusion in cortical laminar necrosis after radial artery/external carotid artery–middle cerebral artery bypass graft surgery for an intracavernous carotid artery aneurysm. Under barbiturate protection, a 69-year-old man underwent high-flow bypass surgery combined with carotid artery sacrifice for a symptomatic intracavernous aneurysm. The patient became restless postoperatively, and this restlessness peaked on postoperative Day (POD) 7. Diffusion-weighted and FLAIR MR images obtained on PODs 1 and 7 revealed subtle cortical hyperintensity in the temporal cortex subjected to temporary occlusion. On POD 13, 123I-iomazenil (123I-IMZ) SPECT clearly showed increased distribution on the early image and mildly decreased binding on the delayed image with count ratios of the affected–unaffected corresponding regions of interest of 1.23 and 0.84, respectively, suggesting postischemic hyperperfusion. This was consistent with the finding on 123I-iodoamphetamine SPECT. Of note, neuronal density in the affected cortex on the delayed 123I-IMZ image further decreased to the affected/unaffected ratio of 0.44 on POD 55 during the subacute stage when characteristic cortical hyperintensity on T1-weighted MR imaging, typical of cortical laminar necrosis, was emerging. The affected cortex showed marked atrophy 8 months after the operation despite complete neurological recovery. This report illustrates, for the first time, dynamic neuroradiological correlations between slowly progressive neuronal death shown by 123I-IMZ SPECT and cortical laminar necrosis on MR imaging in human stroke.
Koji Iihara, Nobuyuki Sakai, Kenichi Murao, Hideki Sakai, Toshio Higashi, Shuji Kogure, Jun C. Takahashi and Izumi Nagata
Object. The authors present a retrospective analysis of their experience in the treatment of vertebral artery (VA) dissecting aneurysms and propose a management strategy for such aneurysms, with special emphasis on the most formidable VA dissecting aneurysms, which involve the origin of the posterior inferior cerebellar artery (PICA).
Methods. Since 1998, 18 patients with VA dissecting aneurysms, 11 of whom presented with subarachnoid hemorrhage (SAH), have been treated by endovascular surgery at the authors' institution. Obliteration of the entire segment of the dissected site with coils (internal trapping) was performed for aneurysms without involvement of the origin of the PICA (12 cases; among these the treatment-related morbidity rate was 16.7%). The treatment strategy applied to PICA-involved VA dissecting aneurysms presenting with SAH (three cases) included proximal occlusion of the parent artery followed by internal trapping of the aneurysm (one case), proximal occlusion of the parent artery followed by occipital artery (OA)—PICA bypass (one case), and two-staged internal trapping of the aneurysm involving double PICAs (one case). For PICA-involved VA dissecting aneurysms that were not associated with SAH at presentation (three cases), OA—PICA bypass was performed and followed by internal trapping of the aneurysm (two cases). In the remaining case in which a fetal-type posterior communicating artery was present, internal trapping was performed following successful balloon test occlusion (BTO). Overall, there was no sign of infarction in the PICA territory, despite complete occlusion of aneurysms involving the PICA. There was no recurrent bleeding or ischemic symptoms during the follow-up periods. The overall treatment-related morbidity rate for the VA dissecting aneurysms involving the PICA was 16.7%.
Conclusions. Dissecting VA aneurysms that do not involve the PICA can be safely treated by internal trapping. For those lesions that do involve the PICA, a decision-making algorithm is advocated to maximize the efficacy of the treatment as well as to minimize the risks of treatment-related morbidity based on BTO.
Tao Yang, Yoshifumi Higashino, Hiroharu Kataoka, Eika Hamano, Daisuke Maruyama, Koji Iihara and Jun C. Takahashi
Hyperperfusion syndrome (HPS) is a notable complication that causes various neurological symptoms after superficial temporal artery (STA)–middle cerebral artery (MCA) bypass surgery for moyamoya disease (MMD). The authors used intraoperative indocyanine green (ICG) videoangiography to measure the change in microvascular transit time (MVTT) after bypass surgery. An analysis was then conducted to identify the correlation between change in MVTT and presence of postoperative HPS.
This study included 105 hemispheres of 81 patients with MMD who underwent STA-MCA single bypass surgery between January 2010 and January 2015. Intraoperative ICG videoangiography was performed before and after bypass surgery. The MVTT was calculated from the ICG time intensity curve recorded in the pial arterioles and venules. Multivariate logistic regression analysis was conducted to test the effect of multiple variables, including the change in MVTT after bypass surgery, on postoperative HPS.
Postoperative HPS developed in 28 (26.7%) of the 105 hemispheres operated on. MVTT was reduced significantly after bypass surgery (prebypass 5.34 ± 2.00 sec vs postbypass 4.12 ± 1.60 sec; p < 0.001). The difference between prebypass and postbypass MVTT values, defined as ΔMVTT, was significantly greater in the HPS group than in the non-HPS group (2.55 ± 2.66 sec vs 0.75 ± 1.78 sec; p < 0.001). Receiver operating characteristic curve analysis revealed that the optimal cutoff point of ΔMVTT was 2.6 seconds (sensitivity 46.4% and specificity 85.7% as a predictor of postoperative HPS). A ΔMVTT > 2.6 seconds was an independent predictor of HPS in multivariate analysis (hazard ratio 4.88, 95% CI 1.76–13.57; p = 0.002).
MVTT in patients with MMD was reduced significantly after bypass surgery. Patients with a ΔMVTT > 2.6 seconds tended to develop postoperative HPS. Because ΔMVTT can be easily measured during surgery, it is a useful diagnostic tool for identifying patients at high risk for HPS after STA-MCA bypass surgery for MMD.