NEURAL DAMAGE CAUSED BY CEREBRAL
HYPERPERFUSION AFTER ARTERIAL BYPASS SURGERY IN A
PATIENT WITH MOYAMOYA DISEASE: CASE REPORT
Kuniaki Ogasawara, M.D.
Department of Neurosurgery
and Cyclotron Research Center,
Iwate Medical University,
Morioka, Japan

Nobukazu Komoribayashi,
M.D.
Department of Neurosurgery
and Cyclotron Research Center,
Iwate Medical University,
Morioka, Japan

Masakazu Kobayashi, M.D.
Department of Neurosurgery
and Cyclotron Research Center,
Iwate Medical University,
Morioka, Japan

Takeshi Fukuda, M.D.
Department of Neurosurgery
and Cyclotron Research Center,
Iwate Medical University,
Morioka, Japan

OBJECTIVE AND IMPORTANCE: The prognosis of cerebral hyperperfusion syndrome
after vascular reconstructive surgery, including extracranial-intracranial arterial bypass, is not poor unless intracerebral hemorrhage develops secondary to
hyperperfusion.
CLINICAL PRESENTATION: A 48-year-old man with symptomatic moyamoya disease
with misery perfusion in the right cerebral hemisphere underwent double right superficial temporal artery-to-middle cerebral artery bypasses. The postoperative course was
uneventful until the patient developed headache and agitated delirium on the 4th
postoperative day.
INTERVENTION: Perfusion computed tomographic imaging demonstrated hyperperfusion in the right temporal lobe. The symptoms resolved by institution of intensive
blood pressure control. Positron emission tomography performed 2 months after
surgery demonstrated a postoperative reduction of the cerebral metabolic rate of
oxygen in the right temporal lobe, where brain atrophy was observed on magnetic
resonance images 3 months postoperatively. Neuropsychological testing performed 3
months postoperatively showed worsening digit span, which adversely affected the
patient’s quality of life.
CONCLUSION: The current case suggests that cerebral hyperperfusion after vascular
reconstructive surgery can cause irreversible neural damage, which results in cognitive
impairment.

Takashi Inoue, M.D.

KEY WORDS: Arterial bypass, Cerebral hyperperfusion, Moyamoya disease

Department of Neurosurgery
and Cyclotron Research Center,
Iwate Medical University,
Morioka, Japan

Neurosurgery 56:1380-1381, 2005

Keiko Yamadate, M.Sc.
Department of Neurosurgery
and Cyclotron Research Center,
Iwate Medical University,
Morioka, Japan

Akira Ogawa, M.D.
Department of Neurosurgery
and Cyclotron Research Center,
Iwate Medical University,
Morioka, Japan
Reprint requests:
Kuniaki Ogasawara, M.D.,
Department of Neurosurgery,
Iwate Medical University,
19-1 Uchimaru,
Morioka, Japan 020-8505.
Email: kuogasa@iwate-med.ac.jp
Received, July 27, 2004.
Accepted, January 21, 2005.

E

DOI: 10.1227/01.NEU.0000159719.47528.2E

xtracranial-intracranial arterial bypass is
the treatment of choice for patients with
moyamoya disease and symptoms of cerebral ischemia (16, 23). However, cerebral hyperperfusion syndrome may occur after vascular reconstructive surgery, including
extracranial-intracranial arterial bypass and
carotid endarterectomy (4, 6, 8, 10, 12, 14, 18,
21, 34, 35). Cerebral hyperperfusion is defined as
a major increase in ipsilateral cerebral blood
flow (CBF) after surgical repair of arterial stenosis or occlusion, well above the metabolic
demands of the brain tissue (26, 32). A rapid
restoration of normal perfusion pressure after
vascular reconstruction may result in regional
hyperperfusion secondary to impaired autoregulation that occurs in the context of chronic
ischemia (32). Whereas cerebral hyperperfusion syndrome is characterized by unilateral
headache, face and eye pain, seizure, and focal
symptoms, the prognosis of this syndrome is

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not poor unless intracerebral hemorrhage develops secondary to hyperperfusion (4, 6, 11,
12, 18, 21, 26, 31, 32, 34, 35).
In this report, we describe a case of cerebral
hyperperfusion syndrome without intracerebral
hemorrhage after extracranial-intracranial arterial bypass in a patient with moyamoya disease.
The cerebral hyperperfusion resulted in neural
damage characterized by a decrease in cerebral
metabolism, brain atrophy, and cognitive
impairment.

CASE REPORT
A 48-year-old man was in his usual state of
good health when he presented with newonset blurred vision and was admitted to a
local hospital for evaluation and treatment.
The patient displayed left homonymous hemianopsia, and a computed tomographic (CT)
scan of the head revealed a cerebral infarct in

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NEURAL DAMAGE CAUSED BY HYPERPERFUSION

the right temporo-occipital region. Cerebral angiography
demonstrated severe stenosis involving the bilateral distal
internal carotid arteries (ICAs), basal moyamoya vessels, and
poor collateral circulation to the right middle cerebral artery
(MCA) territory via a stenotic right posterior cerebral artery
(Fig. 1, A–C). The diagnosis, according to the angiographic
classification described by Suzuki and Kodama (33), was cerebral infarction owing to Stage 3 moyamoya disease, and
antiplatelet medication was initiated. However, 2 months after
symptom onset, the patient experienced a transient ischemic
attack manifesting as left hemiparesis and was admitted to our
hospital for specialized care and further evaluation.
Upon admission, a neurological examination revealed left
homonymous hemianopsia. Neuropsychological testing, consisting of the Japanese translation of the Wechsler Adult Intelligence Scale Revised (WAIS-R) (28) and the Japanese translation of the Wechsler Memory Scale (WMS) (13),
demonstrated impairment of performance intelligence quotient (Table 1). Magnetic resonance (MR) imaging revealed a
cerebral infarct in the right temporo-occipitoparietal region
(Fig. 2, A–C). A positron emission tomographic (PET) study
using 15O-labeled O2 and CO inhalation and H2O autoradiography (27) revealed a decreased cerebral metabolic rate of
oxygen (CMRO2) and a marked decrease in CBF, resulting in
an increased oxygen extraction fraction (OEF) in the right
temporal, frontal, and parietal lobes (Fig. 3, A and B, top row).
Based on these results, the right cerebral hemisphere was
considered to be in a misery perfusion state, and superficial

FIGURE 1. A and B, preoperative
anteroposterior cerebral angiograms
showing severe stenosis at the terminal portion of the bilateral ICAs (A,
right ICA; B, left ICA) and the presence of moyamoya-type vessels. C,
preoperative left vertebral angiogram showing poor collateral circulation to the right MCA territory via
the stenotic right posterior cerebral
artery.

NEUROSURGERY

FIGURE 2. A, C, E, preoperative T2-weighted MR images showing a
cerebral infarct in the right temporo-occipitoparietal region. An infarct
lesion in the right occipital lobe was more extensive than that in the right
temporal lobe. B, D, F, T2-weighted MR images obtained 3 months after
surgery showing brain atrophy in only the right temporal lobe. The right
frontal, parietal, and occipital lobes did not exhibit brain atrophy.

temporal artery (STA)-MCA anastomosis was performed 1
month after the evaluation with neuropsychological testing,
MR imaging, and PET study. Anesthesia was maintained by
intravenous propofol and fentanyl, and the patient was mechanically ventilated with an air-oxygen mixture (inspired
fraction of oxygen ⵑ0.30). Periodic analysis of arterial blood
gas samples ensured normocapnia (PaCO2, 38–40 mm Hg).
Blood pressure was maintained in a range ⫾15% of the preoperative level throughout the procedure by adjusting the

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OGASAWARA ET AL.

onset of these symptoms
demonstrated a hyperintensity in the right temporal lobe
3rd postoperative
6th postoperative
b
Test
Preoperative
SD
(Fig. 4). MR angiography remonth
month
vealed patent double STAWAIS-R
MCA anastomoses (Fig. 5).
Full-scale IQ
83
86
88
13.4
Subsequent perfusion CT imVerbal IQ
97
91
93
13.6
aging (19) demonstrated inInformation
11
12
12
4.2
creased CBF and cerebral
Digit span
9
5
5
3.8
blood volume in the right
Vocabulary
10
7
8
3.5
temporal lobe (Fig. 6, top
Arithmetic
11
10
11
4.2
row). CBF was twice as high
Comprehension
3
5
4
4.3
in the right temporal lobe as
Similarities
13
12
13
5.1
it was in the left temporal
Performance IQ
68
70
71
13.3
lobe. Based on these findings,
Picture completion
5
5
5
3.7
a diagnosis of cerebral hyperPicture arrangement
6
4
6
4.8
perfusion syndrome was
Block design
7
8
8
3.9
made, and intensive control
Digit symbol
4
3
4
4.6
of systolic blood pressure to a
Object assembly
5
8
8
3.5
goal range between 90 and
120 mm Hg was instituted
WMS
using 0.45 mg per day of an
MQ
110
99
104
19.8
orally administered, centrally
Information
5
6
6
2.6
acting ␣2-agonist, clonidine
Orientation
5
5
5
2.1
(Catapres; Boehringer InMental control
9
4
6
5.1
gelheim, Gaithersburg, MD),
Count back
3
2
3
2.1
and 3 ␮g/kg/min of an intraAlphabet
3
2
3
1.8
venously
administered calSerial counting by 3
3
0
2
3.1
cium
antagonist,
nicardipine
Logical memory
9
9
9
5.8
(Perdipine;
Yamanouchi
Digit span
8
3
3
4.7
Pharmaceutical, Tokyo, JaDigits forward
5
0
0
3.5
pan). The patient’s sympD~igits backward
3
3
3
2.8
toms resolved 5 days after
Visual reproduction
11
13
12
4.9
the onset of the hyperperfuAssociate learning
15.5
15
15
5.2
sion syndrome. Repeated T2Easy pairs
17
18
18
4.8
weighted MR and perfusion
Hard pairs
7
6
7
3.1
CT imaging performed 15
a
SD, standard deviation; WAIS-R, Wechsler Adult Intelligence Scale-Revised; IQ, intelligence quotient; WMS, Wechsler
days after the onset of the hyMemory Scale; MQ, memory quotient.
perperfusion syndrome demb
~These values were obtained from a population of 81 patients with carotid stenosis that was described previously (20).
onstrated resolution of both
hyperintensity and hyperperfusion in the right temporal lobe (Fig. 6, bottom row), and pharmacological control of
depth of anesthesia. During the operation, the frontal and
blood pressure was discontinued.
parietal branches of the STA were anastomosed to a cortical
The PET study performed in the same manner 2 months
artery in the temporal and frontal lobes, respectively. The
after surgery revealed increased CBF and unchanged CMRO2,
operation was accomplished without difficulty, and the duration of the temporary occlusion of each recipient artery was 25
resulting in normalization of OEF in the right frontal and
and 23 minutes, respectively. The patient recovered from anparietal lobes (Fig. 3B, bottom row). In contrast, in the right
esthesia without new neurological deficits and did not exhibit
temporal lobe, whereas CBF was slightly increased, CMRO2
additional ischemic lesions on a CT scan performed on the 1st
was lower than the preoperative value, and OEF was lower
postoperative day.
than the contralateral value (Fig. 3A, bottom row). MR imaging
The patient had an uneventful course until the 4th postopperformed 3 months after surgery showed brain atrophy only
erative day, when he experienced severe headache and agiin the right temporal lobe (Fig. 2, D–F). In contrast, the right
tated delirium characterized by vivid hallucinations, delufrontal, parietal, and occipital lobes did not exhibit brain atsions, and extreme agitation and irritability (15). T2- and
rophy. Neuropsychological testing was repeated 3 months
diffusion-weighted MR imaging performed 6 hours after the
after surgery, and a conventional definition of postoperative
TABLE 1. Neuropsychologic test scores before and after bypass surgerya

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NEURAL DAMAGE CAUSED BY HYPERPERFUSION

the tests revealed postoperative improvement. Neuropsychological testing performed 6 months after
surgery showed persistence
of impaired digit span in
both the WAIS-R and the
WMS (Table 1). The patient’s quality of life, including work ability, was
adversely affected by this
cognitive impairment.

DISCUSSION
FIGURE 4. Diffusion-weighted MR

FIGURE 3. PET images at the level of the basal cistern (A) and the body
of the lateral ventricle (B) before (top row) and 2 months after (bottom
row) surgery. Preoperative CMRO2 was decreased, and CBF was markedly decreased, which resulted in increased OEF in the right temporal,
frontal, and parietal lobes. Preoperative OEF was not elevated in the left
cerebral hemisphere. Whereas CBF in the right temporal lobe was slightly
increased postoperatively, CMRO2 was lower than the preoperative value,
and OEF was lower than the contralateral value. In contrast, in the right
frontal and parietal lobes, CBF was increased and CMRO2 was unchanged
postoperatively, which resulted in normalization of OEF.

neuropsychological deficit (20, 30) was applied. This system
uses the standard deviation (SD) unit for each test obtained
from the preoperative scores in the patient population and
defines a deficit for each test in each patient as a decrease in
the postoperative score by ⱖ 1 SD unit from the preoperative
score. Furthermore, an improvement was defined as ⱖ 1 SD
unit elevation above the preoperative score. In the current
study, the SD obtained from 81 patients undergoing carotid
endarterectomy was used (20), and neuropsychological testing
demonstrated a postoperative decline only in digit span in
both the WAIS-R and the WMS (Table 1). Furthermore, none of

NEUROSURGERY

Investigators have pro- image obtained 6 hours after the onset of
posed mechanisms for devel- headache and agitated delirium showing
opment of hyperperfusion af- hyperintense lesions in the right tempoter vascular reconstructive ral lobe.
surgery (1). In cases with severe ICA stenosis and deficient collateral circulation,
hemispheric perfusion pressure is severely reduced distal
to the ICA stenosis. This may
result in a reduction of perfusion pressure below the compensatory capacity of autoregulatory mechanisms, thus
leading to maximal dilation of
resistance vessels and misery FIGURE 5. MR angiogram performed
perfusion. After restoration of 6 hours after the onset of headache and
normal perfusion pressure af- agitated delirium showing patent double
ter vascular reconstructive STA-MCA anastomoses. The signal insurgery, chronically impaired tensity was higher in the right MCA
autoregulatory mechanisms branches than in the left MCA branches.
may require several days to
adjust to the new steady state, resulting in hyperperfusion in the
interim. The current case, in which the patient experienced hyperperfusion after bypass surgery for the right temporal lobe with a
misery perfusion, is consistent with this theory.
In the current case, PET performed 2 months after surgery
demonstrated a postoperative reduction of CMRO2 in the
right temporal lobe, where brain atrophy was observed on MR
images 3 months postoperatively. These findings indicate
postoperative development of irreversible neural damage in
the right temporal lobe. In addition, transient hyperperfusion
after surgery was observed in that region, and diffusionweighted MR imaging demonstrated transient hyperintense
lesions, which may reflect cytotoxic edema (29). Thus, cytotoxic edema owing to hyperperfusion may result in irreversible neural damage in the right temporal lobe.
We previously demonstrated that cognitive improvement
after STA-MCA bypass in patients with symptomatic atherosclerotic ICA or MCA occlusion was dependent on preoperative OEF and was associated with improvement in OEF (27).

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OGASAWARA ET AL.

FIGURE 6. Perfusion CT images 7 hours after the onset of headache and
agitated delirium showing increased CBF and cerebral blood volume in the
right temporal lobe (top row). The CBF was twice as high in the right
temporal lobe (76 ml/100 g/min) as in the left temporal lobe (34 ml/100
g/min). Repeated perfusion CT images 15 days after the onset of the symptoms show resolution of hyperperfusion in the right temporal lobe (bottom
row).

In the current case, although the preoperative increase in OEF
in the frontal and parietal lobes normalized after STA-MCA
bypass, digit span, which is used to evaluate memory and
attention (13, 28), worsened postoperatively. Several investigators hypothesize that the temporal lobe plays an important
role in memory (7, 25). For example, Burton et al. (2) recently
demonstrated significant associations between memory and
white matter hyperintensity volumes in the left or right temporal lobe on MR imaging. In addition, agitated delirium,
which developed as a symptom of cerebral hyperperfusion in
the current case, may be caused by dysfunction of the right
temporal lobe and can be associated with impairment of attention (15). Thus, the postoperative decline in digit span in
our patient may result from neural damage in the right temporal lobe.
Postoperative cognitive impairment, as revealed by neuropsychological testing, occurs in 20 to 30% of patients undergoing carotid endarterectomy (3, 9) and is associated with
cerebral hyperperfusion after surgery, even when asymptomatic (20). Furthermore, the development of hyperperfusion
syndrome is associated with persistence (e.g., at least 6 mo) of
postoperative cognitive impairment (20). Results from the current case are consistent with these findings and suggest that
cerebral hyperperfusion after vascular reconstructive surgery
can also cause irreversible neural damage and lead to cognitive impairment.
Interpretation of data from the current case poses several
problems that require discussion. First, cognitive impairment
or brain atrophy may also occur secondary to the chronic
ischemia associated with moyamoya disease. However, this

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patient developed brain atrophy and impairment in digit span
between the 1-month preoperative evaluation and the
3-month postoperative evaluation. Furthermore, postoperative MR angiography revealed patent double STA-MCA bypasses, and postoperative PET imaging showed an increase in
CBF and a reduction of OEF in the entire right cerebral hemisphere. Thus, it is not likely that the chronic cerebral ischemia
of moyamoya disease explains the subacute development of
brain atrophy and impaired digit span in the current case.
Secondly, brain atrophy may also occur secondary to brain
infarction (5, 24). Indeed, preoperative MR images of our
patient showed an area of infarction that was much more
prominent in the right occipital lobe than in the right temporal
lobe. However, if the brain atrophy in this patient resulted
from the initial infarction, then the right occipital lobe should
become more atrophic than the right temporal lobe. Instead,
MR images obtained 3 months after surgery showed brain
atrophy in only the right temporal lobe. In addition, the right
frontal, parietal, and occipital lobes did not exhibit brain atrophy. Thus, brain atrophy in our patient is likely not related
to initial infarction. Lastly, postoperative cognitive impairment may also result from craniotomy or from the bypass
surgery itself. However, at our institution, surgical treatment
of unruptured intracranial aneurysms by means of craniotomy
did not impair cognitive function (22), and patients with preoperative WAIS-R full-scale intelligence quotient greater than
80 did not display cognitive decline after bypass surgery (27).
Thus, the postoperative cognitive impairment in this patient
may not be related to the craniotomy or to the bypass surgery
itself.
The patient’s quality of life, including work ability, was adversely affected by his cognitive impairment. Although strict
control of blood pressure in the postoperative period is effective
in preventing intracerebral hemorrhage owing to hyperperfusion, it cannot prevent the development of cerebral hyperperfusion itself (4, 18, 21, 35). We have recently reported that pretreatment with a novel free radical scavenger, such as edaravone,
could prevent the occurrence of cerebral hyperperfusion after
carotid endarterectomy (17). Thus, further research regarding
strategies to decrease the incidence of cerebral hyperperfusion
after bypass surgery in moyamoya disease, which may include
the use of edaravone, would be of benefit.

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COMMENTS

T

he authors report a case of a 48-year-old man with symptomatic moyamoya disease that was treated with a double
superficial temporal artery (STA)-middle cerebral artery
(MCA) bypass, which subsequently caused a cerebral hyperperfusion syndrome similar to that observed after carotid
endarterectomy. The patient was managed by lowering his
systolic blood pressure to between 90 and 120 mmHg, but he
suffered neural damage, cognitive impairment, and disability
that were irreversible. Hyperperfusion syndrome is rare, is
seen mostly after over exuberant revascularization after saphenous vein bypass, and can result in intracerebral hemorrhage with more devastating consequences. The authors serve
us well by documenting this syndrome after a routine STAMCA bypass in a moyamoya patient, and by investigating free
radical scavengers as an additional therapy. Still, it is important to emphasize that most moyamoya patients require normal or slightly higher than normal blood pressures in the
perioperative period during and after bypass surgery to prevent ischemic complications, rather than efforts to lower blood
pressure and prevent this unlikely hyperperfusion syndrome.
Michael T. Lawton
San Francisco, California

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OGASAWARA ET AL.

A

lthough there have been previous reports of hyperperfusion syndrome following STA-MCA bypass in moyamoya
patients, including temporary neurologic deficits and imaging
evidence of hyperperfusion, this is the first report to document
persistent cerebral injury reflected by positron emission tomographic scanning 2 months after surgery and cognitive impairment potentially related to the hyperperfusion syndrome. In
our series of 182 direct bypasses for moyamoya patients, we
have observed two instances of temporary neurologic deficits
(partial aphasia) unassociated with hemorrhage or acute ischemia or infarct on diffusion-weighted magnetic resonance imaging, which we attributed to hyperperfusion syndrome. Both
these patients showed resolution of their deficits on neurological examination, but we did not perform neuropsychological
testing. We currently measure intraoperative M4 middle cerebral artery blood flows before and after STA-MCA bypass, as
well as pre- and postoperative transcranial Doppler MCA
velocities in our moyamoya patients. If there is evidence of
significant hyperperfusion after the bypass, we rigorously
control the patients’ blood pressure for several days postoperatively, with the hope of minimizing the detrimental consequences of hyperperfusion syndrome.
The authors draw attention to the benefits of performing
neuropsychological testing before and after revascularization
in their moyamoya patients, because less obvious, but functionally important, deficits or improvements can be detected
compared with neurological examination alone. We too have
recently initiated such neuropsychological testing in our
moyamoya patients.
Gary K. Steinberg
Stanford, California

C

erebral hyperperfusion after revascularization of the brain
has been well documented. The current study documents
a case of cerebral hyperperfusion after extracranial to intracranial bypass surgery using modern imaging techniques to
more elegantly and convincingly demonstrate the hyperperfusion and the long-term ill effects of that complication on the
brain. The authors use perfusion computed tomography to
illustrate the hyperperfusion in the right temporal lobe and
positron emission tomography to demonstrate a postoperative
reduction of the cerebral metabolic rate of oxygen consump-

E1380 | VOLUME 56 | NUMBER 6 | JUNE 2005

tion in the ipsilateral temporal lobe. Perfusion computed tomography measurements of oxygen extraction fraction improved in the frontal and parietal lobes after the bypass, but
worsened in the temporal lobe, which seemed to experience
the consequences of postoperative hyperperfusion. Finally,
the authors used both pre- and postoperative neuropsychological testing to document the deterioration of cognitive function in this patient.
Hyperperfusion after extracranial to intracranial bypass is
rare, and is most likely caused by the relatively low blood flow
provided by the STA initially after the operation. This report
documents this risk and should serve as a caution to surgeons
to be diligent in the postoperative management of patients
undergoing revascularization procedures. In particular, strict
control of blood pressure in the perioperative period is of
paramount importance.
Daniel L. Barrow
Atlanta, Georgia

T

he authors reported an interesting case of moyamoya disease that developed delayed hyperperfusion syndrome
after bypass surgery resulting in the disturbance of higher
cognitive function. Although cases of hyperperfusion syndrome after bypass surgery in moyamoya disease has already
been reported, it is of practical value because the authors
mentioned the anesthesiological and medical management to
avoid hyperperfusion syndrome in the surgical treatment of
moyamoya disease. Additionally, they showed that higher
cognitive function cannot always be improved by bypass surgery in moyamoya disease, even when misery perfusion is
revealed by preoperative positron emission tomographic
study, although it can usually be improved in the treatment of
atherosclerotic cerebroocclusive disease. This paper provided
significant information practically available for the treatment
of moyamoya disease. We hope that this concept will be
verified by many neurosurgeons to add further information
for the understanding and improvement of the surgical treatment of moyamoya disease.
Ken-ichiro Kikuta
Nobuo Hashimoto
Kyoto, Japan

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