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1
Department of Radiology, Samsung Medial Center, Sungkyunkwan University School
of Medicine, 50 Irwon-Dong, Kangnam-Gu, Seoul 135-230, Koreay.
2
Department of Neurosurgery, Samsung Medial Center, Sungkyunkwan University
School of Medicine, Seoul 135-230 Korea.
3
Department of Pediatrics, Samsung Medial Center, Sungkyunkwan University
School of Medicine, Seoul, 135-230, Korea.
Received May 12, 1999;
accepted after revision June 11, 1999.
Address correspondence to H.-K. Yoon.
Abstract
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SUBJECTS AND METHODS. Twenty-six patients (51 hemispheres) with angiographically confirmed moyamoya disease who underwent encephaloduroarteriosynangiosis were included in the study. Findings on preoperative MR angiography were compared with those on conventional angiography. Postoperative neurologic status was categorized as poor, fair, good, or excellent. Postoperative MR angiography was examined for the appearance of the superficial temporal artery, changes in moyamoya vessels, and transdural collateral vessels into the middle cerebral artery territory.
RESULTS. Preoperative MR angiography revealed moyamoya disease in all patients (diagnostic accuracy, 100%). MR angiography correctly depicted the degree of internal carotid artery stenosis in 37 arteries (73%), moyamoya vessels in 33 hemispheres (65%), and the degree of stenosis in the middle, anterior, and posterior cerebral arteries in 125 (82%) of 153 arteries. After surgery, 39 hemispheres showed an excellent outcome, eight showed a good outcome, two a fair outcome, and two a poor outcome. On postoperative MR angiography, vascular supply to the middle cerebral artery territory via transdural collateral vessels increased in 28 hemispheres (55%) and decreased in four (8%). The size of the superficial temporal artery increased in 41 (80%) of 51 hemispheres. The extent of moyamoya vessels decreased in 27 hemispheres (53%) after surgery.
CONCLUSION. MR angiography can show the changes in the superficial temporal artery and development of transdural collateral vessels after encephaloduroarteriosynangiosis. Because MR angiography is noninvasive, it is valuable for evaluating postoperative changes.
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Classically, conventional angiography is the gold standard for diagnosis of moyamoya disease [3]. Recently, noninvasive MR angiography has been widely used in evaluating cerebrovascular disease in both adults and children. Several reports have described the usefulness of MR angiography for evaluation of moyamoya disease [4, 5, 6, 7, 8, 9]. Accuracy of MR angiography is reported to be comparable with that of conventional angiography in diagnosing moyamoya disease [10]. After bypass surgery, the development of collateral vessels from the external carotid artery into the territory of the middle cerebral artery and the enlargement of the superficial temporal artery are expected to be seen on conventional angiograms [11, 12]. MR angiography can help assess the anastomotic vessels after bypass surgery [13]. Our purpose was to assess the role of MR angiography in evaluating moyamoya disease before and after encephaloduroarteriosynangiosis.
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A total of 51 encephaloduroarteriosynangiosis procedures were performed, bilaterally in 25 patients and unilaterally in one patient. The duration of follow-up after surgery was 3 months to 3 years (mean, 1.5 years). Patients' neurologic status after encephaloduroarteriosynangiosis was evaluated by an experienced pediatric neurosurgeon. It was divided into four categories [14]: poor, indicating neurologic deficit after surgery; fair, indicating unchanged symptoms after surgery; good, indicating improvement of minor neurologic deficits; and excellent, indicating complete recovery of neurologic deficits and disappearance of transient ischemic attacks.
The interval between surgery and postoperative MR angiography ranged from 1 to 12 months (mean, 5.8 months).
Imaging
Three-dimensional time-of-flight MR angiography (55/6.9 [TR/TE], 20°
flip angle) was performed with a 1.5-T imager (Signa; General Electric Medical
Systems, Milwaukee, WI). The orientation of volume slab was chosen to cover
the circle of Willis, posterior cerebral artery, and middle cerebral artery.
Slab thickness was 64 mm with 64 partitions, resulting in section thickness of
1 mm. The acquisition matrix was 512 x 192 and the field of view
measured 22 cm.
A total of 42 postoperative MR angiograms were available: one in 16 patients, two in eight patients, three in two patients, and four in one patient.
Twenty-six patients underwent conventional cerebral angiography before surgery, including bilateral internal and external carotid arteriography and unilateral vertebral arteriography. Conventional angiograms were obtained with digital subtraction techniques. Conventional angiography was performed within 2 months of preoperative MR angiography.
Image Analysis
Preoperative cerebral angiography and preoperative MR angiography were
evaluated by two radiologists, who made diagnoses by consensus. Findings on
conventional angiography were used as the gold standard. Findings evaluated on
preoperative MR angiography included degree of distal internal carotid artery
stenosis, extent of moyamoya vessels, and involvement of the middle, anterior,
and posterior cerebral arteries. The degree of distal internal carotid artery
involvement was classified as normal, mild stenosis, severe stenosis, or
occlusion. The extent of moyamoya vessels was classified as absent, mild, and
marked. Middle, anterior, and posterior cerebral artery involvement was
classified as normal, stenosis, or occlusion.
Postoperative MR angiography was compared with the preoperative studies for evaluation of transdural collateral vessels and changes in the superficial temporal artery and moyamoya vessels. Formation of transdural collateral vessels in the middle cerebral artery territory was categorized into good, fair, and poor, adopted from conventional angiography criteria described by Matsushima and Inaha [15]. Collateral vessels at the synangiosis site were classified as grade A if they supplied more than two thirds of the middle cerebral artery territory, grade B if they supplied between one third and two thirds, and grade C if they supplied less than one third.
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Internal Carotid Artery Stenosis
In 37 (73%) of 51 internal carotid arteries, the degree of stenoocclusive
lesions was correctly depicted on MR angiography
(Table 1). In 14 hemispheres
(27%), stenoocclusive lesions were overestimated compared with those on
conventional angiography
(Fig. 1A,
Fig. 1B,
Fig. 1C).
In no patient was the
degree of the stenoocclusive lesion of the internal carotid artery
underestimated.
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Middle, Anterior, and Posterior Cerebral Artery Stenosis
A total of 153 arteries were evaluated and MR angiography correctly
depicted the degree of the stenoocclusive lesions of the middle, anterior, and
posterior cerebral arteries in 125 arteries (82%)
(Table 2)
(Fig. 1). In 26 patients the
degree of the stenoocclusive lesions was overestimated and in two cases it was
underestimated.
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Moyamoya Vessels
Moyamoya vessels were absent in two hemispheres, mild in 20 hemispheres,
and marked in 29 hemispheres on conventional angiography
(Table 3). In 33 hemispheres
(65%), the degree of moyamoya vessels was correctly depicted on MR angiography
(Fig. 1A,
Fig. 1B,
Fig. 1C).
The extent of the
moyamoya vessels was underestimated in 16 hemispheres (31%) and overestimated
in two hemispheres (4%) with mild moyamoya vessels.
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Postoperative Outcome and Transdural Collateral Vessels
In terms of postoperative status, results were excellent in 39 hemispheres,
good in eight, fair in two (both sides in one patient), and poor in two (both
sides in one patient) (Table
4). Postoperative MR angiography showed good development of the
transdural collateral vessels with increased vascular supply to the middle
cerebral artery territory in 28 hemispheres (55%) and no change in 19 (37%)
(Figs. 1A,
1B,
1C and
Figs. 2A, 2B).
In four hemispheres (8%), transdural collateral vessels were poorly formed
with decrease in vascular supply to the middle cerebral artery territory;
clinical status was excellent in two of these patients, good in one, and poor
in one
(Table 4,
Figs. 3A
3B).
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Changes in Superficial Temporal Artery and Moyamoya Vessels
Compared with preoperative MR angiography, postoperative MR angiography
showed interval increase in the size of the superficial temporal artery in 41
hemispheres (80%) and no change in 10 hemispheres (20%)
(Fig. 4A,
4B).
Postoperative MR angiography showed interval decrease in the extent of
moyamoya vessels in 27 hemispheres (53%), no change in 17 (33%), and interval
increase in seven (14%)
(Figs. 2A
2B
and
Figs. 3A
3B).
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The goal of surgical treatment in moyamoya disease is to improve blood flow to hypoperfused regions. Several direct and indirect bypass procedures have been attempted [2]. Direct superficial temporal artery-middle cerebral artery anastomosis is not easy to perform in children because both the donor scalp artery and the recipient cortical artery are small. Indirect surgical procedures for moyamoya disease include encephalomyosynangiosis and encephaloduroarteriosynangiosis. At present, encephaloduroarteriosynangiosis is generally accepted as the treatment of choice in children with moyamoya disease.
Conventional cerebral angiography is still considered necessary for a definite diagnosis although it has a risk of complication [3, 4, 8]. Suzuki and Kodama [1] classified the evolution of moyamoya disease using angiographic findings to define six phases of the disease: stage 1, narrowing of carotid fork; stage 2, initiation of basal moyamoya; stage 3, intensification of moyamoya; stage 4, minimization of moyamoya; stage 5, reduction of moyamoya; and stage 6, disappearance of moyamoya. The three major collateral pathways include parenchymal (basal moyamoya), leptomeningeal, and transdural anastomosis. Collateral circulation from the extracranial arteries to the intracranial arteries includes ethmoidal moyamoya from the ophthalmic artery and transdural anastomoses derived from the middle meningeal and superficial temporal arteries. The diagnostic criteria for moyamoya disease were proposed by the research committee on spontaneous occlusion of the circle of Willis [9]: occlusion or stenosis of the terminal portion of the internal carotid artery and proximal portion of the anterior and middle cerebral arteries, abnormal vascular network at the base of the brain, and no underlying disease. If these criteria are seen bilaterally, the diagnosis is definite moyamoya disease. Otherwise, the diagnosis is probable moyamoya disease.
MR imaging is superior to CT in the visualization of infarction in moyamoya disease, particularly for detection of small cortical or periventricular ischemic lesions [7, 9]. MR imaging is a good technique for screening for moyamoya disease; it can reveal stenosis or occlusion of the supraclinoid internal carotid artery and basal moyamoya vessels by signal voids as well as ischemia, infarction, atrophy, and ventricular dilatation. Because the characteristic MR findings of moyamoya disease are well known, our study did not address MR findings.
MR angiography is safer and easier to perform than conventional angiography. Previous reports have shown good results with MR angiography in diagnosing moyamoya disease [3, 4, 5]. The problem is that MR angiography tends to overestimate the degree of stenosis in the internal carotid artery and other arteries. MR angiography often fails to show fine collateral vessels and, as a result, tends to underestimate moyamoya vessels.
Although MR angiography has a limitation in accurate preoperative staging, it may have a promising role for evaluating postoperative outcome [9, 10]. In our patients, MR angiography after encephaloduroarteriosynangiosis showed an increase in the size of superficial temporal arteries and improvement in vascular supply into the middle cerebral artery territory via transdural collateral vessels in 41 and 28 hemispheres, respectively.
For assessment of postoperative effects, findings on conventional angiography after encephaloduroarteriosynangiosis have been described [11, 15]. According to the reports, direct external carotid angiography revealed development of collateral vessels, dilatation of the superficial temporal artery and the adjacent middle meningeal artery, decrease of moyamoya collateral vessels, and progression of stenoocclusive lesions. Because the goal of encephaloduroarteriosynangiosis is to improve blood flow into the hypoperfused middle cerebral artery territory, changes in vascular supply at the synangiosis site and the size of the superficial temporal artery appear to be the most important findings. In our results, MR angiography revealed postoperative changes well, so it may be useful in predicting clinical outcome.
Unlike conventional angiography, MR angiography might have a limitation in evaluating vascular supply into the middle cerebral artery territory. We focused on the changes in visualized vessels at the synangiosis site; whether MR angiography can predict actual middle cerebral artery perfusion was not considered a problem. Blood flow imaging using radionuclide or perfusion MR imaging will be needed for more accurate evaluation of the perfusion. Gadolinium-enhanced MR angiography may also be helpful because it depicts a greater number of fine collateral vessels, although it has a potential limitation in vein visualization.
We found some discrepancies between postoperative clinical outcome and findings on MR angiography. In four hemispheres with interval decrease of vascular supply in the middle cerebral artery territory, postoperative clinical outcome was excellent in two, good in one, and poor in one. However, perfusion worsening does not always mean ischemia or infarction. Radionuclide or perfusion MR imaging may correlate well with clinical status.
CT angiography has been reported to be valuable in evaluating surgical bypass patency in a small number of patients with moyamoya disease [16]. In our patients, unenhanced CT was only performed to evaluate immediate postoperative complications.
MR angiography has a limitation for preoperative staging: it tends to overestimate the degree of the stenosis of arteries and underestimate collateral vessels. MR angiography may be useful in evaluating surgical bypass patency with improved vascular supply at the synangiosis site.
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