Preliminary Study of Neurocognitive Dysfunction in Adult Moyamoya Disease and Improvement after Superficial Temporal Artery-Middle Cerebral Artery Bypass

OBJECTIVE: Moyamoya disease (MMD) is a chronic cerebrovascular occlusive disease of unknown etiology. In addition, the neurocognitive impairment of adults with MMD is infrequently reported and, to date, has not been well described. We attempted to determine both the neurocognitive profile of adult moyamoya disease and whether a superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis can improve the neurocognitive impairment in exhibiting hemodynamic disturbance without stroke. METHODS: From September 2010 through November 2012, 12 patients with angiographically diagnosed MMD underwent STA-MCA anastomosis for hemodynamic impairment. Patients with hypoperfusion and impaired cerebrovascular reserve (CVR) capacity but without evidence of ischemic stroke underwent a cognitive function test, the Seoul Neuropsychological Screening Battery (SNSB). Five patients agreed to undergo a follow-up SNSB test. Data from preoperative and postoperative neurocognitive function tests were compared and analyzed. RESULTS: Five of 12 patients were enrolled. The median age was 45 years (range, 24-55 years). A comparison of preoperative to postoperative status of SNSB, memory domain, especially delayed recall showed significant improvement. Although most of the domains showed improvement after surgery, the results were not statistically significant. CONCLUSION: In our preliminary study, large proportions of adult patients with MMD demonstrate disruption of cognitive function. This suggests the possibility of chronic hypoperfusion as a primary cause of the neurocognitive impairment. When preoperative and postoperative status of cognitive function was compared, memory domain showed remarkable improvement. Although further study is needed, neurocognitive impairment may be an indication for earlier intervention with reperfusion procedures that can improve cognitive function.

The Usefulness of the Ivy Sign on Fluid-Attenuated Intensity Recovery Images in Improved Brain Hemodynamic Changes after Superficial Temporal Artery-Middle Cerebral Artery Anastomosis in Adult Patients with Moyamoya Disease

OBJECTIVE: MR perfusion and single photon emission computerized tomography (SPECT) are well known imaging studies to evaluate hemodynamic change between prior to and following superficial temporal artery (STA)-middle cerebral artery (MCA) anastomosis in moyamoya disease. But their side effects and invasiveness make discomfort to patients. We evaluated the ivy sign on MR fluid attenuated inversion recovery (FLAIR) images in adult patients with moyamoya disease and compared it with result of SPECT and MR perfusion images. METHODS: We enrolled twelve patients (thirteen cases) who were diagnosed with moyamoya disease and underwent STA-MCA anastomosis at our medical institution during a period ranging from September of 2010 to December of 2012. The presence of the ivy sign on MR FLAIR images was classified as Negative (0), Minimal (1), and Positive (2). Regions were classified into four territories: the anterior cerebral artery (ACA), the anterior MCA, the posterior MCA and the posterior cerebral artery. RESULTS: Ivy signs on preoperative and postoperative MR FLAIR were improved (8 and 4 in the ACA regions, 13 and 4 in the anterior MCA regions and 19 and 9 in the posterior MCA regions). Like this result, the cerebrovascular reserve (CVR) on SPECT was significantly increased in the sum of CVR in same regions after STA-MCA anastomosis. CONCLUSION: After STA-MCA anastomosis, ivy signs were decreased in the cerebral hemisphere. As compared with conventional diagnostic modalities such as SPECT and MR perfusion images, the ivy sign on MR FLAIR is considered as a useful indicator in detecting brain hemodynamic changes between preoperatively and postoperatively in adult moyamoya patients.

Superficial Temporal Artery-Middle Cerebral Artery Anastomosis for Internal Carotid Artery Occlusion by Subacute In-Stent Thrombosis after Carotid Artery Stenting

Alternative to carotid endarterectomy, carotid artery stenting (CAS) can be performed for symptomatic severe stenosis of internal carotid artery, especially for high-risk patients. Among several complications after CAS, subacute in-stent thrombosis is rare but important, because patient's condition can deteriorate rapidly. Subacute in-stent thrombosis with carotid artery occlusion can be managed by superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis. We report two cases of STA-MCA anastomosis for internal carotid artery occlusion by subacute in-stent thrombosis after CAS.

Comparison of the Complications Arising After Superficial Temporal Artery-Middle Cerebral Artery Anastomosis in Adult Moyamoya Disease and Atherosclerotic Disease / 대한뇌혈관외과학회지

OBJECTIVE: To assess the results of superficial temporal artery-middle cerebral artery anastomosis (SMA) in atherosclerotic disease (ASD) and in adult moyamoya disease (MMD) by comparing the complications that arise. METHODS: We retrospectively reviewed patients with ASD or adult MMD treated by means of SMA, between December 2004 and December 2006, at our neurovascular center. During this period, we performed 115 SMAs on 108 patients: 61 on ASD patients (61 SMAs; the ASD group) and 47 on adult MMD patients (54 SMAs; the MMD group). RESULTS: We found a higher incidence of permanent neurological deficits (PNDs) and a lower incidence of transient neurological deficits (TNDs) in the MMD group than in the ASD group (p-value=0.047). Patients with a preoperative stroke (cerebral infarction/hemorrhage) history were more likely to develop postoperative PND than were the patients with a preoperative history of transient ischemic attack (TIA), in both the ASD (p-values=0.012 and 0.033, respectively) and MMD groups (p-values=0.000 and 0.015, respectively), regardless of overall patients (n=108) and single SMA group (n=62). Delayed seizure (seizure occurring > 1 month after SMA) occurred only in 8 MMD patients (8/47, 17.0%; p-value=0.003) out of all 108 patients and in 2 patients (2/10, 20%, p-value=0.014) out of the single SMA group. CONCLUSION: Regardless of whether the diagnosis is ASD or MMD, patients with TIA preoperatively seem more prone to develop postoperative TND, and patients with a stroke history seem more prone to develop PND in both ASD and MMD groups. However, MMD patients appear more likely to experience a delayed seizure attack after SMA than ASD patients are.

Changes in Bypass Flow during Temporary Occlusion of Unused Branch of Superficial Temporal Artery

OBJECTIVE: Some neurosurgeons intentionally ligate the branches of the superficial temporal artery (STA) that are not used in standard STA-to-middle cerebral artery (MCA) anastomosis for the purpose of improving the flow rate in the bypass graft. We investigated changes in bypass flow during temporary occlusion of such unused branches of the STA. METHODS: Bypass blood flow was measured by a quantitative microvascular ultrasonic flow probe before and after temporary occlusion of branches of the STA that were not used for anastomosis. We performed measurements on twelve subjects and statistically assessed changes in flow. We also examined all the patients with digital subtraction angiography in order to observe any post-operative changes in STA diameter. RESULTS: Initial STA flow ranged from 15 mL/min to 85 mL/min, and the flow did not change significantly during occlusion as compared with pre-occlusion flow. The occlusion time was extended by 30 minutes in all cases, but this did not contribute to any significant flow change. CONCLUSION: The amount of bypass flow in the STA seems to be influenced not by donor vessel status but by recipient vessel demand. Ligation of the unused STA branch after completion of anastomosis does not contribute to improvement in bypass flow immediately after surgery, and furthermore, carries some risk of skin necrosis. It is better to leave the unused branch of the STA intact for use in secondary operation and to prevent donor vessel occlusion.

Assessment of Hyperperfusion by Brain Perfusion SPECT in Transient Neurological Deterioration after Superficial Temporal Artery-Middle Cerebral Artery Anastomosis Surgery / 핵의학분자영상

PURPOSE: Transient neurological deterioration (TND) is one of the complications after extracranial-intracranial bypass surgery, and it has been assumed to be caused by postoperative transient hyperperfusion. This study was performed to evaluate the relationship between TND and preoperative and postoperative cerebral perfusion status on brain perfusion SPECT following superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis surgery. Materials and METHODS: A total of 60 STA-MCA anastomosis surgeries of 56 patients (mean age: 50+/-16 yrs; M:F=29:27; atherosclerotic disease: 33, moyamoya disease: 27) which were done between September 2003 and July 2006 were enrolled. The resting cerebral perfusion and cerebral vascular reserve (CVR) after acetazolamide challenge were measured before and 10 days after surgery using (99m)Tc-ethylcysteinate dimer (ECD) SPECT. Moreover, the cerebral perfusion was measured on the third postoperative day. With the use of the statistical parametric mapping and probabilistic brain atlas, the counts for the middle cerebral artery (MCA) territory were calculated for each image, and statistical analyses were performed. RESULTS: In 6 of 60 cases (10%), TND occurred after surgery. In all patients, the preoperative cerebral perfusion of affected MCA territory was significantly lower than that of contralateral side (p=0.002). The cerebral perfusion on the third and tenth day after surgery was significantly higher than preoperative cerebral perfusion (p=0.001, p=0.02). In TND patients, basal cerebral perfusion and CVR on preoperative SPECT were significantly lower than those of non-TND patients (p=0.01, p=0.05). Further, the increases in cerebral perfusion on the third day after surgery were significant higher than those in other patients (p=0.008). In patients with TND, the cerebral perfusion ratio of affected side to contralateral side on third postoperative day was significantly higher than that of other patients (p=0.002). However, there was no significant difference of the cerebral perfusion ratio on preoperative and tenth postoperative day between patients with TND and other patients. CONCLUSION: In patients with TND, relative and moderate hyperperfusion was observed in affected side after bypass surgery. These finding may help to understand the pathophysiology of TND.

Hemodynamic Outcome of Successful Bypass Surgery in Patients with Atherosclerotic Cerebrovascular Disease: A study with Acetazolamide and (99m)Tc-ECD SPECT / 핵의학분자영상

PURPOSE: The aim of the study was to evaluate the hemodynamic changes after successful bypass surgery in patients with atherosclerotic stenosis in ICA using (99m)Tc-ECD SPECT. MATERIALS AND METHODS: Fourteen patients (M:F=8:6, mean age; 60+/-9 years) who underwent STA-MCA anastomosis for unilateral atherosclerotic cerebrovascular disease were enrolled. (99m)Tc-ECD basal/acetazolamide perfusion SPECT studies were performed before, 10 days and 6 months after bypass surgery. Perfusion reserve was defined as the % changes after acetazolamide over rest image. Regional cerebral blood flow and perfusion reserve were compared preoperative, early-postoperative and late-postoperative scans. RESULTS: The mean resting perfusion and decrease in perfusion reserve in affected ICA territory on preoperative scan was 52.4+/-3.5 and -7.9+/-4.7%, respectively. The resting perfusion was significantly improved after surgery on early-postoperative scan (mean 53.7+/-2.7) and late-postoperative scan (mean 53.3+/-2.5) compared with preoperative images (p<0.05, respectively). Resting perfusion did not showed further improvement on late-postoperative scan compared with early-postoperative scan. The perfusion reserve was -3.7+/-2.6% on early-postoperative scan, and -1.6+/-2.3% on late-postoperative scan, which was significantly improved after surgery. Additionally, further improvement of perfusion reserved as observed on late-postoperative scan (p<0.05). While, in the unaffected ICA territory, no significant changes in the resting perfusion and perfusion reserve was observed. CONCLUSION: The improvement of resting perfusion and perfusion reserve in early-postoperative scan reflects the immediate restoration of the cerebral blood flow by bypass surgery. In contrasts, further improvement of perfusion reserve showing on late-postoperative scan may indicate a good collateral development after surgery, which may indicate good surgical outcome after surgery.

Early Surgery-Related Complications after STA-MCA Anastomoses: Clinical Article / 대한뇌혈관외과학회지

OBJECTIVES: Extracranial-intracranial bypass has remained option of augmenting the cerebral circulation in patient with occlusive cerebrovascular disease, especially hemodynamic cerebral ischemia. The purpose of this article is to investigate early surgery-related complications and its prognosis after superficial temporal artery (STA)-middle cerebral artery (MCA) anastomoses. METHODS: The study consists of a retrospective review of 47 patients who underwent 50 STA-MCA anastomoses performed by one surgeon for symptomatic occlusive cerebrovascular disease between 1996 and 2004. A surgical complication was determined on the basis of intraoperative findings, transcranial doppler examination, and radiological study. RESULTS: A procedure-related surgical complication was diagnosed in 7 cases (14%). Complications included marked reduction of blood flow due to stretching of STA in 2, injury of STA in 1, obstruction of MCA angular branch due to incomplete suture in 2, thrombotic obstruction at the site of anastomosis in 1, and embolic obstruction at the site of anastomosis in 2 cases. Functional outcome was evaluated by Glasgow outcome scale. CONCLUSIONS: To improve surgical performance, it is imperative to recognize all procedure-related complications, regardless of how minimal they may seem. We hope this will allow the patient to benefit the most from a procedure that has been proven effective in selected patients with hemodynamic cerebral ischemia.

Limb-Shaking Transient Ischemic Attack due to Stenosis of the Middle Cerebral Artery: Case Report

We present a case of a 51-year-old man with frequent left limb-shaking transient ischemic attacks due to severe stenosis of the right proximal middle cerebral artery(MCA). The involuntary movement was provoked by walking and it was relieved by adopting a squatting posture. Initially, we tried antiepileptic medication, but it did not eliminate the involuntary movement. Cerebral angiography and single photon emission computed tomography demonstrated decreased perfusion and reserve capacity of the right cerebral hemisphere which correspond to stenotic proximal MCA territory. After superficial temporal artery to MCA anastomosis, the decreased reserve capacity was restored and his limb-shaking attack completely disappeared. His history of radiotherapy for craniopharyngioma, in addition to hypercholesterolemia and diabetes mellitus, seems to have contributed to gradual stenosis of right MCA.

Restoration of Vasoreactivity in Patients with Symptomatic ICA Occlusion after Extracranial-Intracranial Bypass Surgery / 대한뇌혈관학회지

OBJECTIVE: The purpose of this study is to investigate changes of vasoreactivity after STA-MCA anastomosis in patients who develop hemodynamic cerebral ischemia associated with ICA or MCA occlusion. METHODS: Twenty-five patients with hemodyamic infarction due to symptomatic ICA or MCA occlusion were treated with extracranial-intracranial bypass surgery (EIAB). Of these, we enrolled 17 patients who underwent follow-up SPECT and follow-up angiogram. To test vasomotor reactivity, we measured relative regional cerebral blood flow (rrCBF) with SPECT both at rest and after diamox infusion. rrCBF were calculated using the following equation: (lesional radioactivity/contralateral radioactivity) x100. We performed EIAB in patients with impaired vasomotor reactivity. To evaluate changes in vasomotor reactivity after surgery, follow-up brain SPECT was performed 1-6 months after surgery and compared rrCBF before and after surgery. RESULTS: Base line radioactivity ratios did not change after surgery. These ratios after diamox challenge were 59.8+/-4.2%, however, 1-6 months after surgery, ratios increased to 77.7+/-.6% (p<0.05, Paired T-test). Preoperative degree of angiographic collateral circulation did not influence the restoration of vasoreactivity. All but two patients showed good collateral circulation through the bypass. There were no cerebral accidents in any these patients at 6 months to 2 years follow-up. CONCLUSION: These results demonstrate the restoration of vasomotor reactivity distal to the occluded ICA or MCA after EIAB, and also show that measurement of rrCBF using SPECT are useful indicators of the clinical and hemodynamic improvement.

Long-Term Follow-up Study after Superficial Temporal Artery-Middle Cerebral Artery Anastomosis plus Encephalomyosynangiosis for Moyamoya Disease

During the period from March 1990, through September 1993, 11 patients with moyamoya disease underwent superficial temporal artery(STA)-to-middle cerebral artery(MCA) anastomosis and encephalomyosynangiosis(EMS) bilaterally. The mean follow-up period was 30.6 months(range 17 to 42 months). The most frequent computed tomographic findings were intraventricular hemorrhage in adult patients and cortical infarction in pediatric patients. In all of the patients, confirmatory diagnosis could be made by angiography, and all had typical angiographic finding of moyamoya disease. According to angiographic classification by Suzuki, the most frequent phase was stage three. A modified continuous suture technique was used during anastomosis. The advantages of this microvascular suture technique are saving time for the surgical procedure, lessening bleeding from the anastomotic site and the ease and safety with which anastomosis can be achieved in the deep cranial cavity. Postoperatively, follow-up angiography was taken between 1 year and 2 years after operation. The angiography revascularization rate was 100%, excellent in 6, and good in 5. The typical postoperative angiography findings are as follows : 1) reduction of moyamoya vessels, 2) normalization or improvement of abnormal posterior circulation, 3) visualization of MCA territory through MCA-STA bypass, and 4) dilatation of STA. There were no major complication in patients with surgery, and no poor outcomes. These results indicate that the STA-MCA anastomosis and EMS in moyamoya disease can normalize cerebral circulation and reduce repeat ischemic attack and repeated bleeding.

Cerebral Blood Flow(CBF) Study on Moyamoya Disease

The author analyzed the r-CBF data of 19 patients who admitted to the Kyung Hee University Medical Center under the diagnosis of definite "Moyamoya" disease from 1983 to 1992. Seven of them were followed-up from 1 to 18 months. The results were as fllow : 1) In moyamoya disease patients, the mean hemispheric r-CBF has a tendency to be lower than that of healthy persons. 2) In moyamoya disease patients, the ipsilateral r-CBF also shows a tendency to be lower than that of contralateral side. 3) The 133Xe-inhalation method is one of useful methods to evaluate CBF in Moyamoya disease, especially for follow-up. 4) The results of follow-up study for Moyamoya disease by 133Xe-inhalation method corelate very well with the change in clinical status of the patients. 5) In Moyamoya disease patients, the follow-up by means of 133Xe-inhalation method is one of useful methods to select a good candidate for surgical treatment such as STA-MAC anastomosis.

Clinical Analysis of Surgical Results in Moyamoya Disease Associated with Intraventricular Hemorrhage

Moyamoya disease is an unusual vascular disorder highlighted by progressive bilateral internal carotid artery occlusion and collateralization of intracranial blood flow. The purposes of the bypass procedures : 1) reduce or arrest of the chance of repeated ischemic attack by making the additional collateral blood flow, 2) decrease the chance of repeated bleeding by reducing the number of moyamoya vessels. During the period from June 1989 through February 1991, 8 moyamoya diseases associated with intraventricular hemorrhage were operated by STA-MCA anastomosis plus EMS. Results are as follows : 1) Slightly female dominancy in incidence(5 : 3), and all of the patients were middle aged(range 32 to 55 years). 2) All of the patients had sudden onset of headache, and most patients whad neck stiffness and vomiting. 3) In all of the patients, confirmatory diagnosis could be done by angiography, and all of the patients had gypical angiographic findings of moyamoya disease. 4) All of the patients had IVH in brain CT scan. 5) All of the patients were surgically treated : STA-MCA anastomosis plus EMS. 6) The postoperative revascularization rate was 89%(8 sides in 9 sides). 7) The postoperative results were excellent in 5, good in 1, and death in 2. The rarity of such lesions in KOrea and their surgical results are reviewed briefly.

STA-MCA Anastomosis: 9 Cases

Since 1967 the STA-MCA anastomosis has been popular procedure in neurosurgical operation. The meurosurgical teams at St. Paul's Hospital, Catholic Medical College, recently operated on 8 patients employing 9 times of this technique. The patients were diagnosed as four patients with complete stroke, one with traumatic middle cerebral stenosis, two with moyamoya disease, and one with huge aneurysm at intracavernous portion of ICA. The results were very encouraging of the 8 patients, 7 had favorably improved clinically, and proved by follow-up cerebral angiographies, CT Scanning, EEG or MEP recordings. The remaining one patient had intracerebral and intracerebellar hematoma, two months later after discharge, thus the result was poor. The authors would like to share with you their experiences employing the STA-MCA anastomosis technique, indications the results and the prognosis.