(Stroke. 1997;28:701-707.)
© 1997 American Heart Association, Inc.
Articles |
Response to Hypercapnia in Moyamoya Disease
Cerebrovascular Response to Hypercapnia in Pediatric and Adult Patients With Moyamoya Disease
From the Departments of Radiology (Y.K., Y.I., M.S., T.Y., K.M.) and Neurosurgery (T.M., M.F.), Faculty of Medicine, Kyushu University, Fukuoka, Japan.
Correspondence to Yasuo Kuwabara, MD, Department of Radiology, Faculty of Medicine, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-82, Japan.
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Abstract |
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Background and Purpose We have previously reported that cerebral blood flow decreased and oxygen extraction fraction and cerebral blood volume increased in pediatric patients with moyamoya disease, whereas these values did not change significantly in adult patients. In this study, we measured the cerebrovascular response to hypercapnia using 15O H2O positron emission tomography (PET) in each group of patients. These data were also compared with the oxygen extraction fraction and transit time (cerebral blood volume/cerebral blood flow) measured by 15O PET.
Methods The subjects consisted of 20 patients with moyamoya disease (7 pediatric and 13 adult patients). Cerebral blood flow was measured by the 15O H2O bolus injection method at the resting state and during the inhalation of 5% CO2. Cerebrovascular CO2 response was estimated as the percentage change of cerebral blood flow per 1 mm Hg change of PaCO2. Oxygen extraction fraction and transit time were measured by the 15O steady-state method.
Results Cerebrovascular response to hypercapnia severely decreased over the cerebral cortices in both pediatric and adult patients with moyamoya disease when compared with those of normal control subjects, and there was no significant difference between pediatric and adult patients. A significant correlation was observed between the CO2 response and transit time, whereas no significant correlation was seen between the CO2 response and oxygen extraction fraction.
Conclusions Our study revealed that the cerebral hemodynamic reserve capacity decreased to an equal degree in both pediatric and adult patients with moyamoya disease. This finding may thus help to explain the occurrence of transient ischemic attack in adult patients.
Key Words: cerebral blood flow • moyamoya disease • hypercapnia • positron emission tomography
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Introduction |
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Moyamoya disease is a disease entity of unknown origin that is characterized by the bilateral stenosis or occlusion of the internal carotid arteries at the proximal portion.1 2 This disease occurs in both pediatric and adult patients. The major clinical manifestations are TIA in pediatric patients and cerebral hemorrhage in adult patients.3 4 Our previous study using PET5 revealed that CBF decreased and that OEF and CBV increased in pediatric patients with moyamoya disease, whereas these values neither increased nor decreased in adult patients. However, the TT (CBV/CBF) was significantly prolonged in adult patients,5 and TIA occurs as frequently in adult patients as in pediatric patients with moyamoya disease. Thus, to clarify the cerebral hemodynamic reserve capacity in pediatric and adult patients, we measured the cerebrovascular response to hypercapnia using 15O H2O PET and compared the results between these groups of patients. Relationships between the vascular response and clinical manifestations, TT, and OEF were also evaluated.
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Subjects and Methods |
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We previously measured the cerebrovascular response to hypercapnia in 52 patients with moyamoya disease using H2O PET from 1989 to 1995. Among them, 20 patients, including 7 children (mean age, 10.9 years; range, 7 to 15 years) and 13 adults (mean age, 30.4 years; range, 18 to 52 years), were carefully selected for this study. Angiography and MRI were performed on all patients. All patients showed either stenosis or occlusion of the internal carotid artery at the distal portion on both sides. Patients with a recent (within 1 month) episode of either infarct or hemorrhage were excluded because of possible lingering effects on cerebral hemodynamics. Patients with lesions measuring >2 cm showing abnormal signal intensity or multiple lesions on MRI were also excluded. None of the patients showed neurological deficits at the time of the PET study. Patient characteristics, clinical symptoms, and MRI findings are summarized in Table 1
. All 7 pediatric patients were TIA type; 7 of the 13
adult patients were TIA type. The 5 adult patients had episodes of
cerebral or intraventricular hemorrhaging and were
thus classified as hemorrhage type. However, 4 of these 5
hemorrhage-type patients also had episodes of TIA. One patient
showed only headache. Thus, the adult patients were also divided into
two groups: the recent-TIA (TIA occurred within 2 months before PET
study) and the no-recent-TIA groups. The angiographic stage according
to Suzuki and Takaku2 was 1 to 2 in 7 sides, 3 in 23
sides, and 4 to 5 in 10 sides. The control subjects were 7 normal
volunteers (mean age, 28.1 years; range, 21 to 40 years) who were
either medical doctors or students. These PET studies were performed
for the preoperative evaluation of the cerebral
hemodynamics in patients with moyamoya disease and
were approved by the committee for the clinical application of
cyclotron-producing radionuclides in Kyushu University Hospital.
Informed consent was obtained from the patients and/or their families
before patients underwent the PET studies.
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PET was performed with a Headtome-III device, which had a spatial resolution of 8.2 mm in full width at half maximum and simultaneously obtained five contiguous slices 15 mm apart. The subjects were placed in a supine position on a bed in a semidark room. A small cannula was placed in the femoral or ulnar artery for arterial blood sampling. A transmission scan with a Ge-68/Ga-68 ring source was obtained for each patient for attenuation correction. The regional CBF was measured by the 15O H2O bolus injection method6 7 at the resting state and during the inhalation of 5% CO2 at an interval of 15 minutes. In the 15O H2O PET study, 740 MBq of 15O H2O was infused as a bolus, and the scan was started when the radioactivity appeared on the head monitor. The data were collected for 75 seconds in each scan. Arterial blood was continuously drawn at a rate of 15 mL/min for 2 minutes, and radioactivity was recorded by a beta-ray detector system using a plastic scintillator (1.1 cm thick and 5.1 cm in diameter). Arterial blood gases and arterial blood pressure were measured at the start and the end of the scan and then were averaged. The dispersion and time delay of the input function was corrected according to the method of Iida et al.8 The fixed time constant (10 seconds) was used for the dispersion correction. The OEF was measured by the 15O steady-state method9 10 on the same day. The blood volume was measured by a single inhalation of 15O CO11 and used for the correction of the intravascular radioactivity in calculating the OEF. The TT was calculated by dividing the CBV by the CBF.12 The data were collected for 6 to 7 minutes using the 15O steady-state method. Arterial blood was drawn every 2 minutes during the scan. The arterial blood radioactivities were averaged into a single value and then used for the calculation of the OEF.
The regions of interest in dimensions of 18x14 mm or 14x14 mm were established on the PET images referring to MR images as shown in our previous report.5 The regions of interest over the infarcted or hemorrhagic area were excluded. The response to CO2 was expressed as the percent change of CBF per 1 mm Hg change of PaCO2. The values on both sides were averaged into a single value and then compared between the control subjects and patients with moyamoya disease. In adult patients, they were also compared between TIA and hemorrhage types and between the recent-TIA and the no-recent-TIA groups. In the latter case, the data on the affected side (contralateral to the TIA side) were used for comparison. The statistical analysis was performed either by repeated measures ANOVA or one-way ANOVA and by post hoc unpaired t test or Welch's t test with unequal variance. The value of P<.007 was used to indicate significance according to the Bonferroni correction in multiple comparisons.
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Results |
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The levels of arterial blood gases, hemoglobin, and blood pressure at the resting state and during inhalation of 5% CO2 on PET study are shown in Table 2
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arterial hemoglobin levels in the patient groups were
significantly lower than those of the control subjects. However, no
significant difference was observed between the pediatric and adult
patients. PaCO2 increased by 8 mm Hg
(mean) (range, 5 to 11 mm Hg) during inhalation of 5%
CO2. The maximum arterial blood pressure
slightly increased during the inhalation of 5% CO2, but it
did not increase significantly. There were no significant differences
in age, hemoglobin, PaCO2, and
arterial blood pressure between the TIA and
hemorrhage types. There were also no differences between
patients with or without recent TIA.
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The cerebrovascular responses to hypercapnia in the brain regions of
the normal control subjects and pediatric and adult patients are shown
in Table 3. The F values, probability values, and
interaction for the data of the cerebrovascular response to hypercapnia
by repeated measures ANOVA are presented in Table 4. A significant difference in the cerebrovascular
response to hypercapnia between the brain regions was thus observed.
There was also a significant difference between the normal control and
the patient groups. A significant interaction was observed between
region and group in recent TIA versus no recent TIA. A significant
decrease in the cerebrovascular response to hypercapnia was observed in
the frontal, temporal, parietal, and occipital cortices and in striatum
in both pediatric and adult patients in comparison with those of the
normal control subjects, whereas the cerebrovascular response to
hypercapnia was relatively preserved in the thalamus and cerebellum. In
addition, there was no difference in the cerebrovascular response to
hypercapnia between adult and pediatric patients. No significant
difference in the cerebrovascular response to hypercapnia was found
between the TIA and hemorrhage types in adult patients. The
patients with recent TIA (within 2 months before PET study) showed a
lower response to hypercapnia in the occipital cortex and thalamus in
comparison with the patients without recent TIA, although no
significant difference was observed between them. The averaged values
in CBF, OEF, and TT are presented with the cerebrovascular
response to hypercapnia in Table 5. The OEFs in the
pediatric patients were higher than those of control subjects. However,
no significant difference was observed between them. The TTs in
moyamoya patients were significantly higher than those of control
subjects in both pediatric and adult patients.
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The relationship between the cerebrovascular response to hypercapnia in the cerebral hemisphere and age was evaluated. The cerebrovascular response to hypercapnia in the patients with moyamoya disease did not show any apparent decline with age (r=-.20, y=2.66-0.02x), and a wide variation was observed in the response in each patient. The relationship between the cerebrovascular response to hypercapnia and the angiographic stage of Suzuki and Takaku2 was also evaluated. The mean values of the cerebrovascular response to hypercapnia were 2.78±0.88, 2.34±1.18, and 1.70±0.85 in stages 1 to 2, stage 3, and stages 4 to 5, respectively. This value declined as the stage advanced; however, no significant difference was observed between the stages (F=2.33, P=.1115, by one-way ANOVA).
Fig 1 shows the relationship between the cerebrovascular
response to hypercapnia and TT in the brain regions. A significant
correlation was observed between them, and the cerebrovascular response
to hypercapnia decreased with the elongation of the TT
(r=-.36 and -.41, F=14.5 and 35.5 in pediatric and adult
patients, respectively; 1% significant). The correlation coefficient
was slightly higher in adult patients than in pediatric patients. A
steal phenomenon (decrease in CBF) was observed in four regions of 3
pediatric patients (patients 1, 2, and 4) and 20 regions of 6 adult
patients (patients 8, 11, 14, 17, and 18). In 7 of these 9 patients,
this phenomenon was observed in the frontal or parietal regions
contralateral to the TIA sides. There was no significant correlation
between the cerebrovascular response to hypercapnia and OEF in either
pediatric or adult patients (r=-.11 and -.10, F=1.24 and
1.82 in pediatric and adult patients, respectively). The correlation
coefficients between the absolute CBF change during inhalation of 5%
CO2 and TT were -.45 and -.35 in pediatric and adult
patients, respectively (F=23.9 and 24.9, 1% significant). We also
correlated the CBF values with the cerebrovascular response to
hypercapnia and thus obtained correlation coefficients of .26 (5%
significant) and .37 (1% significant) in the pediatric and the adult
patients, respectively.
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Fig 2 shows CBF images of a 9-year-old boy with
moyamoya disease at the resting state and during inhalation of 5%
CO2, as well as a response map. He complained of weakness
in the left limbs after crying at 2 months before the PET study. After
that, however, no further TIA occurred. The CBF image at the resting
state did not show any abnormality. The CBF images during the
inhalation of 5% CO2 revealed a decrease in
cerebrovascular response to hypercapnia over the brain. The
PaCO2 increased by 5.5 mm Hg during the
inhalation of 5% CO2. The response to hypercapnia was most
severely impaired in the frontal cortices on both sides, while it was
relatively preserved in the thalamus, cerebellum, and medial part of
the occipital cortices.
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Fig 3 shows the CBF images of an 18-year-old woman with
moyamoya disease at the resting state and during the inhalation of
5% CO2, as well as a response map. She had one or two TIAs
per month before the PET study. The CBF slightly decreased in the right
fronto-temporo-occipital region. The cerebrovascular response to
hypercapnia was also severely impaired, and a steal phenomenon
(decrease in the CBF) was observed in the same regions, while it was
relatively preserved in the cerebellum, thalamus, and left
frontotemporal region. The PaCO2 increased by
7.9 mm Hg during the inhalation of 5% CO2.
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Discussion |
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There have been many studies on the cerebrovascular response to hypercapnia in moyamoya disease. Uemura et al,13 using the 133Xe clearance method, reported that the cerebrovascular CO2 response in hypercapnia decreased in all 3 pediatric patients with moyamoya disease, whereas it decreased partially in 1 of 2 adult patients. Wada14 also reported a decrease in the vascular response to hypercapnia in moyamoya disease using the 15O steady-state method with a continuous infusion of 15O H2O, although 7 of 8 patients were postoperative cases. Takeuchi et al15 and Tomura et al16 studied the cerebrovascular response to both hypercapnia and hypocapnia using the 133Xe inhalation method and 15O H2O PET, respectively, and also reported that the vasodilative response was impaired in pediatric patients with moyamoya disease, while the vasocontractive response was maintained. However, there have been few reports on the difference between pediatric and adult patients, and no precise description of the regional cerebrovascular response to hypercapnia has yet been made because these studies included patients with a large infarct or hemorrhage.
In the present study, the patients were carefully selected on the
basis of clinical and MRI findings to avoid the effects of organic
brain lesions on cerebral hemodynamics. As shown in
Table 3
, the cerebrovascular response to hypercapnia was severely
impaired in both pediatric and adult patients with moyamoya
disease, and no difference was found between pediatric and adult
patients. As described above, TIA is the most frequent clinical
manifestation in pediatric patients, and hemorrhage is the most
frequent in adult patients.3 4 We thus compared the
cerebrovascular response to hypercapnia between TIA and
hemorrhage types of adult patients. However, we could not find
any difference in the cerebrovascular response to hypercapnia between
the TIA and hemorrhage types of adult patients except for
arterial blood pressure. As shown in Table 1, 4 of 5 adult
patients of the hemorrhage type also had episodes of TIA before
or after hemorrhagic attack, and there may be no essential difference
in the cerebral hemodynamics between TIA and
hemorrhage types. In addition, TIA was frequently observed on
the side contralateral to the brain region with a very severely
impaired cerebrovascular response to hypercapnia (decrease in CBF).
These findings suggest that the occurrence of TIA in the adult
patients, as well as in pediatric patients, is caused by a decrease in
hemodynamic reserve capacity or by
hemodynamic ischemia.
In the regional estimation of the cerebrovascular response to hypercapnia, the cerebral cortices were more severely impaired than the cerebellum or thalamus in both pediatric and adult patients. This finding was also observed by Takeuchi et al15 using the 133Xe inhalation method and Fukuuchi et al17 using stable Xe CT. Hoshi et al,18 using N-isopropyl-p-(123I)iodoamphetamine–labeled single-photon emission computed tomography (IMP-SPECT), reported that the count rate ratios (cerebral cortices/cerebellum) decreased in the frontal, temporal, and parietal regions after intravenous acetazolamide. In moyamoya disease, abundant collateral circulations develop around the Willis ring, or so-called moyamoya vessels, while the leptomeningeal anastomosis develops from the basilar and posterior cerebral arteries. Thus, the anterior circulation is severely impaired in moyamoya disease, while the posterior circulation is relatively preserved by the development of the leptomeningeal anastomosis from the posterior cerebral arteries. Our results support these findings from the viewpoint of hemodynamic reserve capacity.
It is well known that the cerebrovascular CO2 response
normally decreases with age when expressed as
CBF/PaCO2, but
%CBF/PaCO2 does not change with
age.19 20 In this study, we used
%CBF/PaCO2 as an index of vasoreactivity
and could not find apparent decline in the cerebrovascular response to
hypercapnia with age. Thus, we did not consider the aging effect when
comparing the vascular response to hypercapnia between pediatric and
adult patients. Suzuki and Takaku2 classified the
angiographic findings of moyamoya disease into six stages. Fukuuchi
et al17 evaluated the relationship between the
cerebrovascular response to hypercapnia and angiographic stage of
Suzuki and Takaku and reported that the response decreased as the stage
advanced. In our study, the cerebrovascular response to hypercapnia
declined with the stage, although no significant difference was
observed between stages 1 to 2, stage 3, and stages 4 to 5. These
results indicate that the hemodynamic reserve capacity
decreases with the advance of the occlusive lesions in the cerebral
arteries.
OEF is an indicator of the uncoupling of the blood flow to energy metabolism and can provide important information that can help in selecting the appropriate surgical treatment.21 We have reported that OEF increased in the pediatric patients with moyamoya disease, although it did not do so in adult patients.5 This suggests that pediatric patients suffer more severe ischemia than adult patients. In this study, we studied the relationship between CO2 response and OEF. However, contrary to our prediction, no significant correlation was observed between them, even in the pediatric patients. Theoretically, the vasodilatory capacity can decrease without an increase in OEF,22 while OEF can increase in other situations such as hyperventilation or anemia.23 In addition, a wide variation was observed in the cerebrovascular response to hypercapnia in each patient. These may be reasons for the poor correlation between the CO2 response and OEF.
Gibbs et al24 reported that CBF/CBV had potential value as an index of perfusion reserve (or pressure) and related to OEF. Taki et al25 studied CBF/CBV using PET and reported that it decreased in adult patients with moyamoya disease. The inverse equation (regional CBV/regional CBF) equals TT.12 As described above, we have reported that the TT was prolonged in both pediatric and adult patients with moyamoya disease.5 Thus, the decrease in the cerebrovascular response to hypercapnia in moyamoya disease was thought to be caused by vasodilatation associated with the decrease in perfusion pressure due to either stenosis or occlusion of the internal carotid arteries. In this study, cerebrovascular response to hypercapnia and TT were significantly correlated with each other in both pediatric and adult patients. However, the correlation coefficients were not high. In patients with moyamoya disease, abundant collateral vessels developed over the brain, and the superficial veins were also dilated. These vascular components cannot be differentiated from the dilatation of the small resistant vessels because of the limited resolution of the PET scanner. This may be one of the reasons for the low correlation coefficients between TT and response to hypercapnia.
In conclusion, our present study revealed that the cerebral hemodynamic reserve capacity decreased equally in both pediatric and adult patients with moyamoya disease. This finding may thus help to explain the occurrence of TIA in adult patients, in whom CBF did not decrease in our previous study.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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We would like to express our thanks to Toshimitsu Fukumura for the production of 15O H2O, Dr Kanehiro Hasuo for the interpretation of neuroradiological examinations, and Naoko Kinukawa for assistance in performing the statistical analysis of the PET data.
Received September 9, 1996; revision received January 20, 1997; accepted January 20, 1997.
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