Electroencephalographic Findings in Children With Moyamoya Disease Namio Kodama, MD; Yasunori Aoki, MD; Hatao

\s=b\ The EEG findings in 25 children with moyamoya disease were studied. Characteristic findings such as posterior slow, centrotemporal slow (CT slow), "rebuildup" after the end of hyperventilation, and sleep spindle depression were observed. Posterior slow activity was mainly observed in the EEGs examined within a short period (mean, 10 months) after onset, CT slow activity after a longer period (mean, 28 months), and a diffuse low-voltage pattern after these periods (mean, 56 months). Buildup after the end of hyperventilation, which we refer to as "rebuildup," was discovered in more than half of the cases. (Arch Neurol 36:16-19, 1979)

IX/T oyamoya disease':'

was

described

by Suzuki and colleagues as a disorder showing abnormal netlike vessels (hereafter referred to as "moyamoya" vessels) at the base of the brain on the carotid angiogram. The pathogenesis of the disorder has "·*

Hiraga, MD; Tokuo Wada, MD; Jiro Suzuki,

changes in children whereas in adults they show less prominent changes. It has been believed that the electroen¬ cephalogram (EEG) has little or no value in the diagnosis of this disease even though slight abnormalities have been reported.' However, we believe that the EEG can play an important role as a means of screening, since we have found characteristic features in children with moyamoya disease. PATIENTS AND METHODS

study

included 25 children under 13 years of age (Table). The EEG records were made from three days to 72 months following the onset of symptoms. The international 10-20 electrode system was applied. Waking records as well as activa¬ tion records produced by photic stimula¬

Our

tion, hyperventilation, and sleep were analyzed. The following characteristics were evalu¬ ated: (1) slow wave activity, which was classified into two types according to the location of its appearance: posterior slow (P slow) and centrotemporal slow (CT

MD

slow); (2) diffuse low-voltage pattern, by

which is indicated diffuse low-amplitude activity of variable frequencies from theta to beta activity with or without laterality; (3) changes with hyperventilation; (4) sleep spindles; (5) degree of EEG abnormality, which was classified into five grades: normal (N), borderline (B), slightly abnor¬ mal (A,), moderately abnormal (A2), and severely abnormal (A;l); (6) relation be¬ tween the degree of EEG abnormality and the phase of angiographie findings (The angiographie findings of moyamoya cases were classified into six phases, I through VI, according to Suzuki and Takaku.2 Correlation between degree of EEG abnor¬ mality and angiographie phases was evalu¬ ated. All the angiograms were performed within two weeks before or after the EEG recordings.); and (7) correlation between the more involved side on EEG and neuro¬

logical symptoms. RESULTS Slow Wave Activity

Seventeen

cases

showed

slow

activity, which was characterized by high-amplitude, monorhythmic waves

not yet been clarified, and the symp¬ toms and angiographie studies differ

in children and adults. The main symptoms in children are transient hémiplégie attacks, mental retarda¬ tion, and fine involuntary movements of the extremities, while in adults, there may be intracranial hemorrhage with severe headache and loss of consciousness. On sequential angio¬ graphie studies, moyamoya vessels show remarkable and progressive Accepted for publication

March 2, 1978. From the Division of Neurosurgery, Institute of Brain Diseases (Drs Kodama and Suzuki), and the Department of Central Laboratory (Dr Hiraga), Tohoku University School of Medicine, Sendai, Japan, and the Clinics of CNS Diseases (Dr Aoki) and Neurosurgery (Dr Wada), National Sendai Hospital. Read in part before the Ninth International Congress of Electroencephalography and Clinical Neurophysiology, Amsterdam, 1977. Reprint requests to Division of Neurosurgery, Institute of Brain Diseases, Tohoku University School of Medicine, 5-13-1 Nagamachi, Sendai 982

Japan (Dr Kodama).

slow and anterior dominant Fig 1.—Electroencephalogram of patient 9, showing high-voltage slow activity. Calibration: 50 jtV and one second. Same calibration is used in all figures. EMV indicates eye movement vertical.

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Summary

of

Electroencephalographic EEG

Case/Age, yr/Sex 1/2/M 2/10/F 3/9/F 4/1.7/F 5/5.7/F 6/6/M

Duration Between Onset and Electroen¬

cephalogram 3 days 20 days 2

mo

4 4

mo

4

mo

7/6.7/M

4

mo

8/8.6/M

4

mo

9/9/M

4 mo

Findings

and Clinical

Findings

Slow-Wave

Activity Inactive

Rebulldup by Hyper-

Pattern

ventilation

Diffuse

Slow

CT Slow

Sleep Spindle Depression

Degree of

Abnormality A, A, A, A, A,

mo

CAG Phase

Symptoms hemiparesis Left hemiparesis Transient motor aphasia Right hemiplegia Left

lll(lll)

lll(lll) lll(lll) H(lll) IV(III) lll(ll)

Weakness of left

V(lll) A,

arm

Right hemiparesis phasia

and

dys-

Weakness of four extremi¬ ties (severe at left arm), severe headache Weakness of right arm, headache Weakness of four extremi¬ ties (left more than right),

IV(III) lll(l)

_laughing attack_ 10/5/F

6

mo

A,

11/7.6/F

6

mo

.,

12/4/M

8

mo

l(ll) Ill(ll) lll(lll)

Weakness of

13/10/F

11

mo

A2

lll(lll)

Left hemiparesis, vomiting Transient right hemiparesis, convulsion Weakness of left hand and

14/5.11/M

13

mo

A,

IV(III)

Right hemiparesis, dyspha-

15/6.7/F

16

mo

Aa

V(none)

Right hemiparesis,

right

arm

fingers_ sla

16/6/F 17/6/M 18/8.6/M 19/7/F 20/8.5/F 21/8/F 22/13.7/M

46 42

mo

A,

mo

A,

14 mo

20

mo

30

mo

48 42

mo

23/9/F

48

mo

24/9/M

60

25/10/F

72

mo

'

mental

retardation Mental retardation

iv(iv) IV(IV) ll(ll) H(IH) IV(V) lll(lll) V(IV)

Mental retardation Mental retardation Left hemiparesis Mental retardation

Right hemiparesis Right hemiparesis, mental retardation gait, mental retarda¬ tion

lll(lll)

Ataxlc

mo

IV(IV)

Right hemiparesis, dyspha-

mo

V(V)

Mental retardation

+

sia

"Degree of abnormality on carotid angiography by Suzuki and Takaku." First figure indicates angiographical phase of more involved hemisphere on EEG; figure in parenthesis indicates less involved hemisphere on EEG.

appearing with a paroxysmal or nonparoxysmal pattern, more dominant in the posterior area of one hemi¬ sphere. This activity was suppressed by opening the eyes and was remark¬ ably decreased during sleep. In five cases, similar anterior slow activity was

found to accompany

slow activity, the EEGs were per¬ formed from three days to 42 months after the onset. The mean duration was ten months. In four cases that showed CT slow activity, the duration was from 14 to 48 months. The mean duration was 28 months.

slow activ¬

ity (Fig 1).

Four cases showed CT slow activity, which was characterized by moderate¬

ly

high-amplitude, polyrhythmic appearing continuously in centrotemporal areas, more dominant in one hemisphere. This was not sup¬ pressed by opening the eyes and continued during sleep (Fig 2).

waves

The time between the onset of symptoms and the EEG recording tended to be related to the location of slow waves. In 17 cases that showed

Diffuse

Low-Voltage

Pattern

This was found in four cases in which the EEGs were taken from 42 to 72 months following the onset (Fig 3). The mean duration was 56 months.

Changes

With

Hyperventilation

Hyperventilation was done in 20 Buildup of slow waves by hyper¬

cases.

ventilation

as

well

as

return to the

prehyperventilation pattern within 20

to 60 seconds after the termination of

hyperventilation was observed in each

14 cases, buildup of slow began to appear soon after the original buildup had returned to the prehyperventilation pattern. This phenomenon, designated as "rebuildup," continued for more than one minute, and in some cases confusion was recognized (Fig 4). case. In waves

Sleep Spindles

Sleep spindle depression was found in 21 cases. A sleep record was not

taken in one case. It was observed on the same side of slow and CT slow activity and also on the involved side as suggested by neurologic symp¬ toms.

Degree

of EEG

Of 25 cases, 20 and five as A3.

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Abnormality classified

were

as

A2

children with moyamoya disease shows characteristic findings such as slow and CT slow activity, rebuildup, and sleep spindle depression. Yoshii and Kudo4 reported an exces¬ sive response to hyperventilation but placed no emphasis on slow or CT slow activity. In moyamoya disease of children, slow activity is different from the nonspecific posterior slow waves5 in normal children. This slow activity stands out clearly from the back¬

ground activity, appearing paroxysmally or continuously. Most slow activity is unilateral, corresponding to the side of major involvement, and appears in the same proportion of

01

P3 —

between age of 1 year and 7 months and age 10 years. Consequent¬ ly, slow activity is easily discrimi¬ nated from nonspecific slow waves. Abnormal posterior slow activity is seen in various disorders, such as head injury," brain tumor,7 or petit mal absence."' This posterior slow wave activity is generally divided into two categories: one is monorhythmic slow, projected from deep portions of the brain, and the other is polyrhythmic slow, demonstrating a localized super¬ ficial focus in the occipital areas. Most of the cases of head injury in children show posterior slow waves that are presumably projected from the centrencephalon." Slow waves seen in petit mal absence also seem related to this mechanism. Martinus et al7 reported two types of posterior slow activity associated with cerebellar cases

Fig 2.—Electroencephalogram of patient 20, showing CT slow activity (C, continues

even

after eye

and

T6),

which

opening.

tumor.

essi..·

Fig 3.—Electroencephalogram

amplitude and inactive.

variable

patient 24, showing diffuse inactive pattern frequencies from alpha to beta activity. Left hemisphere of

Relations Between Degree of EEG Abnormalities and Phase of Angiographie Findings

Twenty cases with moderate abnor¬ malities (A.,) in the EEG were distrib¬ uted among the five angiographie phases of moyamoya disease. No important relationship was found be¬ tween EEG findings and angiograph¬ ie phases. The cases showing slow activity were also evenly distributed among the phases. Correlation Between More Involved Side on EEG and Neurological Symptoms

Unilateral

neurological symptoms

of lowis more

found in 19 of 25 cases. The involved side, where slow and CT slow activity and sleep spindle depres¬ sion were observed on EEG, corre¬ sponded to the side suggested by neurological symptoms in all 19

were

cases.

COMMENT

The electroencephalographic find¬ ings in moyamoya disease have been regarded as of no diagnostic value on the grounds that even when abnormal findings are present, they show no characteristic features.' Our study has clearly demonstrated that the EEG in

They are monorhythmic poste¬

rior slow activity, presumably pro¬ jected from the deep portion of the brain due to high intracranial pres¬ sure and enlargement of the third ventricle, and polyrhythmic slow ac¬ tivity, presumably produced by local¬ ized circulatory disturbance of the occipital lobe due to vascular compres¬ sion by the cerebellar tumor. Since the slow waves are monorhythmic, are suppressed by opening the eyes, and disappear or decrease during sleep, slow activity might be interpreted as the result of disturbances involving the deep structures in the brain. The similar wave pattern of anterior slow activity, which often appears in cases with slow activity, may also be projected from the same portion of the brain. On the other hand, CT slow activity is considered to indicate a disturbance of the cortex because it is

polyrhythmic, not suppressed by open¬ ing the eyes, and continues during sleep. According to Suzuki and Takaku,angiographic features of moyamoya

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of the precise mechanisms involved in the production of slow and CT slow activity precludes advantageous dis¬ cussion beyond the points already mentioned, we emphasize from our data the fact that the EEGs in chil¬ dren with moyamoya disease change from slow to CT slow activity and diffuse low-voltage pattern as time

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passes. It was also observed that buildup after hyperventilation in this disease showed characteristic patterns. After the end of hyperventilation, the build¬ up of activity decreased or disap¬

peared

as

the EEG returned to the

pattern prior to hyperventilation. Then, after intervals of 20 to 60

seconds, slow waves started to build up again and some patients seemed

02

2. Rebuildup is shown after end of hyperventi¬ lation. Left, two minutes and 30 seconds later. Center, 20 seconds later. Right, 50 seconds later.

Fig 4.—Electroencephalogram of patient

disease in children can be classified into six phases. Initially, the stenotic change occurs at the carotid bifurca¬ tion. Subsequently, the middle cere¬ bral artery, the anterior cerebral artery, and the posterior cerebral artery disappear in that order as the stenotic change advances. Therefore, it can be suggested from these sequential angiographie studies that the areas supplied by these arteries are likely to be damaged in the same order as the disease progresses. The analysis of our data indicated that slow activity appeared within a relatively short time after onset (mean, ten months), CT slow activity at midstage (mean, 28 months), and the diffuse low-voltage pattern at a later time (mean, 56 months). The described EEG changes with time may reflect the degree of slowly progressive circulatory disturbance. Posterior slow activity, which appears at an early stage in the posterior area, is considered electroencephalographically to originate from the centrencephalon, as mentioned previously. There may be two possible explana¬ tions why slow waves appear domi-

in the posterior areas: one is the greater likelihood of posterior slow waves in children whether of nonspecific or pathological origin, and the other is the absence of a mecha¬ nism interfering with slow-wave pro¬ jection from the centrencephalon to the posterior area because the circula¬ tion of this area is still kept intact at the early stage. We would like to think that the latter is more likely, because slow activity accompanied similar waves in the anterior areas in five cases. At the next stage, when CT slow activity appears on the EEG, the cerebral circulation decreases in the centrencephalon as well as in cortical slow areas. The disappearance of activity may be due to either an inca¬ pability of producing slow waves by the damaged centrencephalic regions or interference with projection of this slow wave because of cortical dam¬

nantly

age. At

a late stage, the appearance of the diffuse low-voltage pattern is interpreted as due to far-advanced ischemia in both centrencephalic and cortical portions of the brain. Al¬ though our present lack of knowledge

confused. This "rebuildup" was not found in any of our adult patients but was found in most of the children showing slow or CT slow activity. The mech¬ anism of buildup during hyperventila¬ tion has not been completely clarified. One report suggests that the lowering of C02 concentration in blood due to hyperventilation causes vasoconstric¬ tion of the small arteries in the brain, which disturbs blood flow." However, this will not explain the rebuildup seen in this disease, which has not, to our knowledge, been previously re¬ ported. This rebuildup may be consid¬ ered a typical phenomenon related to moyamoya vessels at the base of the brain, since it appears frequently in childhood cases with abundant moya¬ moya vessels while it seldom appears in children or in most of the adult cases with scanty moyamoya vessels. It is generally believed that moya¬ moya disease in children is rarely accompanied by convulsions. Howev¬ er, Nishimoto and Mizukawa" report convulsive seizures in 12% of children. Moyamoya disease may in these cases be mistaken for idiopathic epilepsy. Some of our patients were treated as epileptic because of repeated tran¬ sient ischemie attacks or a drowsy state due to hyperventilation. In another case, slow activity itself was mistaken for an epileptic discharge.

References 1. Nishimoto A, Takeuchi S:

Moyamoya

dis-

cerebrovascular network in the cerebral basal region, in Vinken PJ, Bruyn GW (eds): Handbook of Clinical Neurology 12. Amsterdam, North-Holland Publishing Co, 1972, ease, abnormal

pp 352-383.

2. Suzuki J, Takaku A: Cerebrovascular Neurol 20:288-299, 1969. 3. Suzuki J, Kodama N: Cerebrovascular "Moyamoya" disease\p=m-\secondreport: Collateral routes to forebrain via ethmoid sinus and

"Moyamoya" disease. Arch

meatus. Angiology 22:223-236, 1971. 4. Yoshii N, Kudo T: EEG findings of occlusion of the circle of Willis, in Kudo T (ed): A Disease With Abnormal Intracranial Vascular Networks. Tokyo, Igakushoin, 1967, p 72. 5. Aird RB, Gastaut Y: Occipital and posterior

superior nasal

electroencephalographic rhythms. Electroencephalogr Clin Neurophysiol 11:637-656, 1959. D: 6. Silverman Electroencephalographic study of acute head injury in children. Neurology 12:273-281, 1962.

7. Martinus J, Matthes A, Lonbroso CT: Elecfeatures in posterior fossa tumors in children. Electroencephalogr Clin Neurophysiol 25:128-139, 1968. 8. Kety SS, Schmidt CF: The effect of active and passive hyperventilation on cerebral blood flow, cerebral oxygen consumption, cardiac output and blood pressure of normal young men. J Clin Invest 25:107-119, 1946. 9. Nishimoto A, Mizukawa N: So-called "Moyamoya disease" from the neurosurgical standpoints. Neurol Med 3:37-45, 1975.

troencephalographic

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Electroencephalographic findings in children with moyamoya disease.

Electroencephalographic Findings in Children With Moyamoya Disease Namio Kodama, MD; Yasunori Aoki, MD; Hatao \s=b\ The EEG findings in 25 children w...
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