Childs Nerv Syst
DOI 10.1007/s00381-016-3052-z

CASE REPORT

Reversible diffusion weighted imaging hyperintensities
during the acute phase of ischemic stroke in pediatric moyamoya
disease: a case report
Goichiro Tamura 1 & Satoshi Ihara 1 & Nobuhito Morota 1

Received: 19 November 2015 / Accepted: 4 March 2016
# Springer-Verlag Berlin Heidelberg 2016

Abstract
Background Moyamoya disease is one of the primary causes
of pediatric ischemic stroke, especially in East Asia. Areas of
high signal intensity on diffusion weighted imaging (DWI)
with decreased apparent diffusion coefficient (ADC) values
usually point to irreversible ischemic damage. Reversibility
of these DWI hyperintensities during the acute phase of ischemic stroke in pediatric moyamoya disease has not previously
been reported.
Case report A 3-year-old girl was admitted to our emergency
department due to sudden onset speech impairment and right
hemiplegia. Computed tomography (CT) revealed a
multilobal low-density area in the left cerebral hemisphere.
The area was hyperintense on DWI with decreased ADC
values. Magnetic resonance (MR) angiography revealed stenosis of the bilateral internal carotid artery bifurcations and
their branches. Acute cerebral infarction due to moyamoya
disease was diagnosed. MR images taken 4 days later showed
resolution of most of the DWI hyperintensity areas. The initial
decline in the ADC of the reversible DWI hyperintensities was
less severe compared to the irreversible lesion. Within several
days after onset, the patient became ambulatory although the
follow-up MR fluid attenuated inversion recovery (FLAIR)
images taken 2 weeks after onset revealed thinning of the
corresponding cortical gyri.
Conclusion These findings indicate that a wide area of DWI
hyperintensity during the acute phase of ischemic stroke can
be reversed by appropriate treatment in pediatric moyamoya

* Goichiro Tamura
g-tamura@umin.ac.jp

1

Division of Neurosurgery, Tokyo Metropolitan Children’s Medical
Center, 2-8-29 Musashidai, Fuchu, Tokyo 183-8561, Japan

disease. To the best of our knowledge, this is the first report of
reversible DWI hyperintensities over a wide cortical area during the acute phase of ischemic stroke in pediatric moyamoya
disease.
Keywords Moyamoya . Ischemic stroke . Reversible . DWI .
ADC

Abbreviations
ADC
Apparent diffusion coefficient
CT
Computed tomography
DWI
Diffusion weighted imaging
MRI
Magnetic resonance imaging
ROI
Region of interest
TIA
Transient ischemic attack
FLAIR Fluid attenuated inversion recovery

Introduction
Diffusion weighted imaging (DWI), a form of magnetic resonance imaging (MRI), is regarded at present as the most sensitive means of detecting acute ischemic stroke [1, 13].
Hyperintense areas on DWI with decreased apparent diffusion
coefficient (ADC) values usually represent irreversible ischemic damage resulting from a cerebral infarction [2]. Even with
the recent development of thrombolytic agents and advances
in endovascular therapy, these hyperintense areas are very
difficult to reverse during the acute phase of an ischemic
stroke.
Ischemic symptoms of moyamoya disease are often induced by hyperventilation, in which the resulting hemodynamic mechanism is thought to trigger the formation of the
cerebral infarction [7]. The mechanism of ischemia in pediatric moyamoya disease seems to differ greatly from that of

Childs Nerv Syst

cerebral infarctions in adults, most of which are characterized
by atherosclerosis or embolisms. Only a few reports have
described the ischemic patterns of pediatric moyamoya disease [4, 12], and none have yet described the reversibility of
these DWI hyperintensities in this particular disease.
Herein we report a case of pediatric moyamoya disease,
which was remarkable in that the initial DWI hyperintensities
with decreased ADC values and low CT density returned to
the baseline level within 4 days.

Case report
Patient history and management
A 3-year-old girl was referred to our emergency department
due to sudden onset speech impairment and right hemiplegia.
She experienced no seizures. The initial brain CT revealed
multilobal (temporal, parietal, and occipital lobes) lowdensity areas in the left hemisphere (Fig. 1). The area appeared

Fig. 1 Initial brain CT images taken 12 h after the onset of stroke: axial
views. The left hemisphere, predominantly the temporal and parietal
lobes, shows low density, indicating the area of cerebral ischemia

hyperintense on the DWI with decreased signal intensity on
the ADC map (Fig. 2). MR angiography revealed the stenosis
of the bilateral internal carotid artery bifurcations and the
proximal segments of the anterior and middle cerebral arteries
(Fig. 3). Abnormal collateral vessels, the so-called moyamoya
vessels, were observed around the circle of Willis. Based on
these findings, the diagnosis of acute cerebral infarction due to
moyamoya disease was made.
Neurologically, the patient was unable to lift her right arm
or stand at the time of admission. She had been mildly sedated
for 4 days to prevent crying and was well-infused to prevent
hypovolemia. An MRI taken 4 days after admission showed a
significantly diminished area of hyperintensity on DWI only
in the left premotor cortex (Fig. 4). Within a week after onset,
her symptoms resolved dramatically except for a very subtle
disturbance in the fine movement of her right fingers. Once
she became ambulatory, she was discharged and later
underwent bilateral direct revascularization surgery.

Fig. 2 Initial MRI taken 13 h after the onset of stroke: axial
views. The left hemisphere shows high signal intensity on DWI
(a). The corresponding lesion shows decreased signal intensity on
the ADC map (b)

Childs Nerv Syst

Fig. 3 MR angiography: anteroposterior (upper panel) and lateral
views (lower panel). Stenosis of the bilateral internal carotid
artery bifurcations and the proximal segments of anterior and
middle cerebral arteries are evident. Abnormal collateral vessels
are observed around the circle of Willis

A follow-up pre-surgical MRI was taken 2 weeks after
onset (Fig. 5). Fluid attenuated inversion recovery (FLAIR)
images revealed thinning and mildly increased intensity of the
cortical gyri indicating the presence of ischemic damage. The
affected area of the cortical gyri coincided with the hyperintense area on initial DWI at the time of onset.
MR imaging and assessment
All MR images were obtained with a 1.5 Tesla scanner
(Philips Electronics, Amsterdam, Netherlands) while the patient was under intravenous sedation. Absolute ADC values
were calculated using the following formula:
ADC = −ln(Sb1000/Sb0)/(1000 − 0), where S denoted DWI
signal intensities of b = 0 and b = 1000 s/mm2. Six regions
of interest (ROIs) were manually drawn within the reversible
and irreversible lesions on the initial DWI. The mean absolute
ADC values (and their standard deviation) of the reversible
and irreversible lesions were 579.5 (±216.6) × 10−6 and
313.2(±117.5) × 10−6 mm2/s, respectively. As recommended
by previous researchers [10, 17], the ADC ratios were also
obtained to minimize the influence of the cerebrospinal fluid.
They were calculated by dividing each ADC value of the
lesion by the ADC value of the corresponding normal area
in the contralateral hemisphere. The mean ADC ratios (and
their standard deviation) of the reversible and irreversible

Fig. 4 MRI taken 4 days after the onset of stroke: axial views. The DWI
hyperintensity becomes significantly smaller and remains only in the left
premotor cortex (a). The signal intensity of the corresponding lesion
remained low on the ADC map (b)

areas of hyperintensity were 50.8 (±15.5) % and 28.9
(±10.2) %, respectively. The unpaired t test revealed a significant difference between the two groups: p = 0.0286 for absolute ADC values and p = 0.0279 for ADC ratios (Table 1). The
p values <0.05 were considered statistically significant.
The area of reversible hyperintensities on initial DWI was
delineated manually in a slice-by-slice fashion. The volume of
the reversible lesion was determined by calculating each area
and multiplying it by the slice thickness. The volume of the
reversible DWI hyperintensities was 55.1 mL.

Discussion
There are very little data regarding spatial and temporal imaging patterns of cerebral infarctions in moyamoya disease [4,
12]. Cho et al. reported that childhood-onset moyamoya disease was characterized by gyral or atypical territorial patterns
[4]. The finding was very different from that of adult

Childs Nerv Syst

Fig. 5 MRI taken 2 weeks after onset of stroke: axial views. Fluid
attenuated inversion recovery (FLAIR) images show thinning and
mildly increased intensity of the cortical gyri of the left frontal,
temporal, and parietal lobes

atherosclerotic infarctions, which in most cases followed a
typical vascular territorial pattern. Our case also showed the
characteristic gyral pattern of the cerebral infarction, which
might occur partly because gray matter in children is more
vulnerable to ischemia when the blood supply is markedly
reduced [3, 6]. These data can indicate hypoperfusion rather
than thrombotic vaso-occlusion as being the major mechanism of acute cerebral ischemia in moyamoya disease.
It is widely accepted that high signal intensity on DWI and
decreased ADC values indicate the presence of cytotoxic edema [2, 5]. Vasogenic edema on the contrary is characterized by
iso- or moderately increased diffusion and elevated ADC
values, partly due to the T2 shine-through effect [5].
Cytotoxic edema is caused by acute ischemia and infarctions,
with a consequent decrease in ADC values through a

Table 1 The ADC values and
ratios of reversible and
irreversible DWI hyperintensities

reduction in the diffusibility of protons. Only a small number
of previous reports described the early reversal of such DWI
hyperintensities with decreased ADC values in adult ischemic
stroke patients [1, 8, 9, 11, 15, 16]. Reversibility of DWI
hyperintensities in pediatric moyamoya disease has not yet
been reported.
The previous reports indicated that the reversible lesions
showed a milder ADC decline compared with irreversible
lesions [1, 8, 16]. The finding could be explained by milder
ischemic damage and cell edema leading to early recovery.
They also showed that early reversal of DWI hyperintensities
is limited to small lesions in adult ischemic stroke patients [1,
8]. Our case also showed milder ADC decline in reversible
lesions; however, the multilobal involvement observed in this
particular case is very unique.
Interestingly, a follow-up MRI taken 2 weeks after onset
revealed evidence of an ischemic event. Even the area of the
reversible DWI hyperintensities showed thinning of the cortical gyri and mildly increased intensity in the latest FLAIR
images. Our case is also noteworthy in that the patient’s neurological symptoms dramatically improved within a short period of time. This finding strongly suggested that the area of
reversible DWI hyperintensities was successfully, even if only
partially, restored by timely treatment.
The resolution of DWI hyperintensities and the improvement in the neurological symptoms could be explained by the
existence of collateral vessels. It is widely believed that slowly
progressing steno-occlusive changes in the terminal internal
carotid artery induces the development of pathognomonic collateral pathways [14]. Eloquent areas would have more blood
supply from collateral vessels to meet the higher metabolic
demand and thus would develop greater resistance to ischemia. Moreover, the location of eloquent areas or watershed
border zones would shift in pediatric moyamoya patients because their developing brains are under ischemic conditions
for a long period. In moyamoya patients, it sometimes seems
difficult to predict the prognosis based only on the initial MRI
at the time of onset. The surprising neurological recovery and
resolution of a wide area of initial DWI hyperintensities in our
case can be explained by existence of these collateral vessels.

Reversible lesion

Irreversible lesion

p value

Mean ADC value (±SD)

579.5(±216.6) × 10−6 mm2/s

Mean ADC ratio (±SD)

50.8(±15.5)%

313.2(±117.5) × 10−6 mm2/s
28.9(±10.2)%

0.0286
0.0279

ADC apparent diffusion coefficient, DWI diffusion weighted imaging, SD standard deviation

Childs Nerv Syst

In summary, we report the first case of reversible DWI
hyperintensities in pediatric moyamoya disease during the
acute phase of ischemic stroke. Our findings indicate that
severe symptoms of ischemic stroke at the time of onset, even
with a wide area of DWI hyperintensities, ADC declines, or
CT hypodensities, do not always indicate irreversible cerebral
damage at least where pediatric moyamoya disease is
concerned.

4.

5.

6.

7.
Acknowledgments We thank Mr. James Robert Valera for his editorial
assistance with the manuscript. We also thank Dr. Takeshi Funaki of the
University of Kyoto for providing the follow-up MR images.
Author contributions Author contribution to the study and manuscript
preparation include the following—conception and design: all authors;
acquisition of data: Tamura and Ihara; analysis and interpretation of data:
all authors; drafting of the article: Tamura; critical revision of the article:
Tamura and Morota; review of the submitted version of the manuscript:
Tamura; approval of the final version of the paper on behalf of all authors:
Tamura; statistical analysis: Tamura; and study supervision: Ihara and
Morota.
Compliance with ethical standards Our case report was approved by
our institutional review board/ethics committee.
Conflict of interest The authors declare that they have no conflict of
interest.
Funding The authors received no financial support for the publication
of this article.

8.

9.

10.

11.

12.

13.

14.

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