Cerebral Hemodynamic Change in the Child and the Adult With Moyamoya Disease
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1 272 Cerebral Hemodynamic Change in the Child and the Adult With Moyamoya Disease Yasuo Kuwabara, MD, Yuichi Ichiya, MD, Makoto Otsuka, MD, Takashi Tahara, MD, Ranjan Gunasekera, MD, Kanehiro Hasuo, MD, Kouji Masuda, MD, Toshio Matsushima, MD, and Masashi Fukui, MD To clarify the differences in cerebral hemodynamics and metabolism between children and adults with bilateral moyamoya disease, we measured regional cerebral blood flow, regional oxygen extraction fraction, regional metabolic rate for oxygen, regional cerebral blood volume, and regional transit time using positron emission tomography in nine patients (five children and four adults) and compared the values with those in controls (four children with unilateral moyamoya disease and six normal adults). The major differences between pediatric and adult patients were in regional cerebral blood volume and regional oxygen extraction fraction. Regional cerebral blood volume was more markedly increased relative to the control value in the children than in the adults. Also, regional oxygen extraction fraction was greater than control in areas with low blood flow in the children but was never increased in the adults. However, in the adults, only regional transit time was significantly prolonged relative to the control values. The increased regional oxygen extraction fraction relative to the control value observed in children with moyamoya disease may explain why transient ischemic attacks are a common symptom in this group. (Stroke 1990;21: ) Moyamoya disease is well-recognized in Japan and is characterized by stenosis or occlusion of unknown etiology of both internal carotid arteries (ICAs) and of numerous collateral vessels around the circle of Willis. 1 ' 2 Peak incidences are among persons aged 0-10 and years, and the disease is usually divided into two types, pediatric and adult. 23 The types show different clinical courses and features, and the pediatric type is more progressive than the adult type. The common symptoms of moyamoya disease in children are transient ischemic attacks (TTAs) such as hemiparesis or weakness of the limbs, whereas the symptoms in adults are attacks of bleeding such as intracerebral or subarachnoid hemorrhage. 3 Many workers have investigated cerebral hemodynamics in patients with moyamoya disease, 4-7 but there have been no reports on the differences in cerebral hemodynamics and metabolism between pediatric and adult patients. To our knowledge, we are the first to measure cerebral hemodynamics and From the Department of Radiology, Faculty of Medicine (Y.K., Y.I., M.O., T.T., R.G., K.H., K.M.) and the Department of Neurosurgery, Neurological Institute (T.M., M.F.), Kyushu University, Fukuoka, Japan. Address for correspondence: Yasuo Kuwabara, Department of Radiology, Faculty of Medicine, Kyushu University, Maidashi, Higashi-ku, Fukuoka, 812 Japan. Received February 6, 1989; accepted September 20, metabolism and to compare the pediatric with the adult type of moyamoya disease using positron emission tomography (PET). Subjects and Methods We studied 30 patients with moyamoya disease using PET. The disease was diagnosed in all patients by angiography, which showed stenosis or occlusion of the ICAs and moyamoya vessels on both sides. From these 30 patients, we carefully selected nine (five children and four adults) retrospectively for this study. We excluded patients with multiple cerebral infarcts or recent (^2 ) infarction or hemorrhage to avoid their effects on cerebral blood flow and metabolism. We also excluded adult patients with the onset of moyamoya disease during childhood because they had multiple cerebral infarcts and cerebral atrophy. The clinical features of the nine patients are summarized in Table 1. Five had small low-density lesions on computed tomography (CT). had a neurologic deficit when the PET study was performed. The PET device (HEADTOME-III, Shimadzu Corp., Kyoto, Japan, and Akita Noken, Akita, Japan) had a transaxial resolution of 8.2 mm and an axial resolution of 13 mm full-width at halfmaximum. Regional cerebral blood flow (rcbf), regional oxygen extraction fraction (roef), and
2 Kuwabara el al Cerebral Hemodynamics and Metabolism in Moyamoya Disease 273 TABLE 1. Clinical Features of Nine and Four Pediatric With Moyamoya Disease Iviajor symptoms Case/ Interval Low-density lesions on CT age/sex Type Description onset-pet Location Size (cm 2 ) Pediatric 1/9/F 2/9/M 3/9/F 4/11/F 5/15/F +IVM Weakness of R hand Choreic movement Weakness of L hand Weakness of limbs Weakness of L foot 5 2 years 10 4 years 11 1 year 4 R frontal subcortical R temporal subcortical lxl 1x2 Angiographic findings Occlusion of B ACAs and MCAs Occlusion of B ACAs and MCAs 6/33/M 7/35/M 8/40/F 9/59/F Pediatric controls 10/8/M 11/9/F 12/9/M 13/11/M - Hemorrhage RIND Weakness of L hand Weakness of L limbs Headache Headache Weakenss of L hand Paresthesia of R hand Weakness of L limbs L hemiparesis 6 years 6 4 years 8 years 3 years 1 year years 8 R frontal cortical L frontal subcortical R parietal cortical R temporal cortical 3x3 1x2 2x4 2x2 Stenosis of B ACAs and MCAs Stenosis of B ICAs Occlusion of R ICA Occlusion of L ICA Stenosis of R ICA Occlusion of R ICA PET, positron emission tomography; CT, computed tomography; F, female; M, male;, transient ischemic attack; IVM, involuntary movement; RIND, reversible ischemic neurologic deficit; R, right; L, left; B, bilateral; ICA, internal carotid artery; ACA, anterior cerebral artery; MCA, middle cerebral artery. regional cerebral metabolic rate for oxygen (rcmro 2 ) were measured using the oxygen-15 steady-state method 8-9 with continuous infusion of H 2 15 O or inhalation of C^Oz and 15 O 2. Regional cerebral blood volume (rcbv) was measured using a single inhalation of "CO or C 15 O. roef and rcmro 2 were corrected for rcbv. 9 Regional transit time (rtt) was calculated as rcbv+rcbf. 10 A small cannula was placed in the femoral artery for blood sampling. A PET transmission scan with a germanium- 68-gallium- 68 ring source was obtained from each patient for attenuation correction. 11 For the oxygen-15 steady-state method, five crosssectional planes 20, 35, 50, 65, and 80 mm above the orbitomeatal line were scanned simultaneously for 6 minutes. Arterial radioactivities were measured every 2 minutes. PaOj, PacOj, and arterial ph were measured at the start and end of each scan and averaged. The values are expressed as mean±sd. The values of rcbf, roef, rcmro 2, rcbv, and rtt were obtained using rectangular regions of interest 18x14 or 14x14 mm in the cerebellum, in the frontal, temporal, parietal, and occipital cortices, and in the striatum on both sides (Figure 1) and averaged. The regions of interest were selected from the blood flow images and the CT scan to avoid the low-density lesions shown on CT. The values are expressed as mean±sd. Age, arterial blood gases, hemoglobin content, rcbf, roef, rcmro 2, rcbv, and rtt in the nine patients were compared with those in respective controls (four children with unilateral moyamoya disease [Table 1] and six normal volunteers aged years old) using Student's t test and Welch's t test with unequal variance. rcbf, roef, rcmro 2, rcbv, and rtt in the angiographically normal hemisphere were used in the pediatric controls. Results Age, arterial blood gases, and hemoglobin content in the pediatric and adult patients with moyamoya disease are compared with values in their respective controls in Table 2. There was no significant difference between the patients and their respective controls. rcbf, roef, rcmro 2, rcbv, and rtt in various anatomic regions in the pediatric and adult patients with moyamoya disease are compared with values in their respective controls in Table 3. In the pediatric patients, rcbf was not significantly decreased, although it was approximately 20% lower than control in the frontal and parietal regions; the occipital region and the cerebellum were spared. Adult patients also showed no significant reduction in rcbf, although it was slightly decreased in the entire brain. rcmro 2 was not decreased in the pediatric
3 274 Stroke Vol 21, No 2, February 1990 TABLE 2. Age, Arterial Blood Gases, and Hemoglobin Content in Pediatric and Adult With Moyamoya Disease and Respective Pediatric Adult Age (yr) PacO} (mm Hg) PaOs (mm Hg) Hemoglobin (g/dl) Values are mean±sd. ("=5) («=4) 93± ± ± ±0.7 («=4) 41.8± ± ±1.9 («=6) 29.7± ± ± ±0.8 TABLE 3. rcbf, roef, rcmroj, rcbv, and rtt in Brain Regions of Pediatric and Adult With Moyamoya Disease and Respective Pediatric Adult Region rcbf roef rcmro 2 rcbv rtt («=5) 49.0± ± ± ± ± ± ± ±9.4* 50.2±8.5t 51.7±6.0t ± ± ± ± ± ± ±1.94f 5.88±1.28* 6.33±1.74t 6.98±2.34f 6.46±2.97f 3.87± ± ± ±4.25t 11.6±3.84t 9.91±4.73f (»=4) ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±0.% 6.45± ±OJ0 («=4) 44.4± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± t 7.30±1.14t 7.62 ± ("=6) 51.0± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±1.01 rcbf, regional cerebral blood flow as ml/min/100 ml brain; roef, regional oxygen extraction fraction as %; rcmroj, regional cerebral metabolic rate for oxygen as ml/min/100 ml brain; rcbv, regional cerebral blood volume as ml/100 ml brain; rtt, regional transit time as seconds. Values are mean±sd. 't p<0.02, <0.05, <0.01, respectively, different from control by Student's / test or Welch's / test.
4 Kuwabara et al Cerebral Hemodynamics and Metabolism in Moyamoya Disease 275 :n 35 FIGURE 1. Location of regions of interest (ROIs). OEF FIGURE 2. Case 7, 9-year-old girt Computed tomogram (left panel) 50 mm above orbitomeatal line shows no abnormality. Positron emission tomograms (right panel) reveal decrease in regional cerebral blood flow bilaterally in frontal regions. However, regional cerebral metabolic rate for oxygen was relatively preserved and regional oxygen extraction fraction was increased in these regions. Regional cerebral blood volume was markedly increased in basal ganglia.
5 276 Stroke Vol 21, No 2, February 1990 OEF CMPOi FIGURE 3. Case 7, 35-year-old man. Computed tomogram (left panel) 50 mm above orbitomeatal line shows low-density lesion in left frontal subcortical region. Positron emission tomograms (right panel) show slight decrease in regional cerebral blood flow and regional cerebral metabolic rate for oxygen in left basal striatum. Regional oxygen extraction fraction and regional cerebral blood volume were not increased patients, but roef was significantly increased in the regions with low rcbf, especially the frontal and parietal regions. In the adult patients, rcmro2 was not significantly reduced and roef was not increased. rcbv was significantly increased in the cerebral cortices and striatum in the pediatric patients, but it was not increased in the adult patients. rtt was significantly prolonged in the cerebral hemisphere in both groups of patients, especially the pediatric group, but not in the cerebellum. Case 7, adult type. This 35-year-old man developed weakness of his left arm and leg 6 before the PET study. A small low-density lesion was seen in the left frontal subcortical region on CT (Figure 3, left panel). The diagnosis of moyamoya disease was confirmed by angiography, which demonstrated severe bilateral stenosis of the ICAs and their branches. PET showed slightly decreased rcbf and rcmro2 in the right striatum. roef and rcbv were not increased (Figure 3, right panel). Case Reports We selected two typical cases of the pediatric and the adult types of moyamoya disease for illustration. Case 1, pediatric type. At the age of 8 years, transient weakness of the right hand had occurred in this 9-year-old girl. Thereafter, similar attacks occurred every month. CT of her brain showed no abnormalities (Figure 2, left panel), but angiography revealed bilateral stenosis of the ICAs with marked leptomeningeal anastomosis, and the diagnosis of moyamoya disease was confirmed. PET showed decreased rcbf bilaterally in the frontal regions. However, rcmro2 was relatively preserved and roef was increased. rcbv was increased in the cerebral cortices and the basal ganglia (Figure 2, right panel). Discussion Both children and adults with moyamoya disease have occlusions or stenoses of both ICAs. However, it is well known that the types show different clinical courses and features.3 Namely, moyamoya disease in children is more progressive than in adults, clinically and angiographically, and s are more common in children. Therefore, we compared cerebral hemodynamics and metabolism relative to controls between these two groups of patients with moyamoya disease using PET. The most conspicuous difference between pediatric and adult patients was in rcbv, which was increased relative to the control value much more in the former than in the latter. The increase in rcbv in patients with moyamoya disease can be explained by compensatory vasodilatation following the decrease
6 Kuwabara et al Cerebral Hemodynamics and Metabolism in Moyamoya Disease 277 in perfusion pressure and by the development of numerous collateral vessels, the so-called moyamoya vessels, which were most prominent in the basal ganglia. The higher rcbv observed among pediatric patients may be due partly to the presence of dilated vessels on the surface of the brain, which could not be differentiated due to the limited resolution of PET. The reason for this difference between the pediatric and adult patients is not clear, but it can best be explained by the prolonged rtt (low perfusion pressure) observed in the children. In addition, children may develop abundant collateral vessels more easily than adults, thus resulting in increased rcbv. Another major difference in the pediatric and adult patients was in roef. The former had increased roef relative to their controls, whereas the latter did not. Increased roef indicates blood flow insufficient for the oxygen demand, or misery perfusion. 14 In the pediatric patients, rcmro 2 was preserved and roef was increased in brain regions with low rcbf. However, in the adult patients, rcmro 2 and rcbf were preserved and roef was normal. According to previous reports using xenon- 133, children with moyamoya disease had significantly reduced rcbf, 56 but adults did not. 4 Our results support these findings. The increased roef in our pediatric patients was also compatible with their longer rtt and is in good accord with the clinical findings that is the most common symptom in children with moyamoya disease. Two of our four adult patients experienced s. We could not compare cerebral hemodynamics and metabolism in adult patients with and without because there were so few, but there seems to be no difference between the two adult patients with and the two without. In the adult patients rtt was also significantly prolonged, but this was more remarkable in the pediatric patients with a higher incidence of. This indicates that decreased perfusion reserve prevails even in adult patients with moyamoya disease and may explain the occurrence of in them. Increased roef in the pediatric patients indicated that they suffer more severe ischemia than the adult patients. The difference in roef relative to control values between the pediatric and adult patients is probably related to the severity or the rapidity of progression of the occlusive lesions, which were much more progressive in the children than in the adults. 3 Increased roef is also an important finding in considering the management of patients with moyamoya disease, as it may be a good indicator for early surgical intervention According to our preliminary experience, 16 surgical treatment using extracranial-intracranial bypass surgery was more effective in pediatric patients. This is under investigation at present. As described above, rcbv and roef were remarkably different compared with control values between children and adults with moyamoya disease. Increased roef may explain why is a common symptom in the pediatric type of moyamoya disease; in the adults only rtt was significantly prolonged relative to control values. These differences in cerebral hemodynamics and metabolism should be considered primarily in the management and early surgical intervention in patients with moyamoya disease. References 1. Nishimoto A, Takeuchi S: Abnormal cerebral vascular network related to the internal carotid arteries. J Neurosurg 1968;29: Suzuki J, Takaku A: Cerebral vascular "moyamoya" disease. A disease showing abnormal net-like vessels in base of brain. Arch Neurol 1969;20: Suzuki J, Kodama N: Moyamoya disease A review. Stroke 1983;14: Uemura K, Yamaguchi K, Kojima S, Sakurai Y, Ito Z, Kawakami H: Regional cerebral blood flow in cerebrovascular "moyamoya" disease. Study by 133 Xe clearance method and cerebral angiography. No To Shinkei 1974;27: Takeuchi S, Tanaka R, Ishii R, Tsuchida T, Kobayashi K, Arai H: Cerebral hemodynamics in patients with moyamoya disease: A study of regional cerebral blood flow by the U3 Xe inhalation method. Surg Neurol 1985;23: Ogawa A, Nakamura N, Sakurai Y, Kayama T, Wada T, Suzuki J: Cerebral blood flow in moyamoya disease. No To Shinkei 1987;39: Tagawa T, Naritomi H, Mimaki T, Yabuuchi H, Sawada T: Regional cerebral blood flow, clinical manifestations, and age in children with moyamoya disease. Stroke 1987;18: Frackowiack RS, Lenzi GL, Jones T, Heather JD: Quantitative measurement of regional cerebral blood flow and oxygen metabolism in man using 15 O and positron emission tomography: Theory, procedure and normal values. J Comput Assist Tomogr 1980;4: Lammertsma AA, Jones T, Frackowiack RS, Lenzi GL: Correction for the presence of intravascular oxygen extraction ratio in the brain. / Cereb Blood Flow Metab 1983;3: Meier P, Zierler KL: On the theory of the indicator-dilution method for measurement of blood flow and volume. J Appl Physiol 1954;6: Kanno I, Miura S, Yamamoto S, Murakami M, Takahashi K, Uemura K: Design and evaluation of a positron emission tomograph: Headtome III. / Comput Assist Tomogr 1985; 9: Gibbs LM, Wise RJS, Leenders KL: Evaluation of cerebral perfusion reserve in patients with carotid artery occlusion. Lancet 1984;l: Powers W, Grubb RL, Raichle ME: Physiological responses to focal ischemia in humans. Ann Neurol 1984;16: Baron JC: Reversal of focal "misery-perfusion syndrome" by extra-intracranial arterial bypass in hemodynamic cerebral ischemia. A case study with 15 O positron emission tomography. Stroke 1981;12: Powers WJ, Martin WRW, Herscovitch P, Raichle ME, Grubb RL: Extracranial-intracranial bypass surgery: Hemodynamic and metabolic effects. Neurology 1984;34: Fukui M, Matsushima T, Kuwabara Y: Hemodynamic evaluation of moyamoya disease in children by positron emission computed tomography before and after neurosurgical procedures (EDAS, EMS, EMAS), in Handa H (ed): Annual Report of 1986 on the Cooperative Study of Occlusion of the Circle of Willis to the Ministry of Health and Welfare. 1987, pp KEY WORDS tomography, emission computed moyamoya disease metabolism
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