Neurol Med Chir (Tokyo) 50, 1099¿1104, 2010

Cerebral Hyperperfusion Syndrome Associated With
Non-convulsive Status Epilepticus Following Superficial
Temporal Artery-Middle Cerebral Artery Anastomosis
—Case Report—
Takeshi HAMAMURA, Takato MORIOKA, Tetsuro SAYAMA, Nobutaka MUKAE,
Shuji ARAKAWA*, Hironobu MAEDA**, and Tomio SASAKI***
Departments of Neurosurgery, *Cerebrovascular Disease, and
**Radiology, Kyushu Rosai Hospital, Kitakyushu, Fukuoka;
***Department of Neurosurgery, Graduate School of Medical Sciences,
Kyushu University, Fukuoka

Abstract
A 77-year-old man developed cerebral hyperperfusion syndrome with temporal deterioration of consciousness and worsening of left hemiparesis on the 6th postoperative day following superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis for right M 1 occlusion. Electroencephalography (EEG) revealed frequent ictal discharges in the right hemisphere, although convulsive
seizures were not apparent. Administration of anticonvulsants was performed based on the diagnosis of
non-convulsive status epilepticus (NCSE). Complete recovery from hyperperfusion syndrome was
achieved with rapid improvement of EEG findings. The present case demonstrates the pathophysiological mechanism of hyperperfusion syndrome associated with NCSE after STA-MCA anastomosis.
Key words: cerebral hyperperfusion syndrome, non-convulsive status epilepticus,
superficial temporal artery-middle cerebral artery anastomosis, ictal hyperperfusion,
electroencephalography

Introduction
Carotid reconstruction surgery including carotid endarterectomy (CEA) or carotid stenting (CAS) can cause a
rapid increase in cerebral blood flow (CBF) in the chronic
ischemic brain of patients with atherosclerotic diseases,
resulting in complications such as cerebral hyperperfusion syndrome.3,15,19,22) Patients with poor cerebrovascular
reactivity are known to have higher risk for hyperperfusion syndrome.12,18,23) The severity of intraoperative ischemia is also reported to be one of the predictive factors for
hyperperfusion syndrome after CEA.12) In contrast, hyperperfusion syndrome after superficial temporal arterymiddle cerebral artery (STA-MCA) anastomosis for
atherosclerotic diseases is thought to be rare, since STAMCA anastomosis usually provides low-flow revascularization.23) However, recent evidence suggests that STAMCA anastomosis for moyamoya disease as well as
atherosclerotic disease can also result in symptomatic
hyperperfusion.4,5,7,10,11,13) However, the exact mechanism
of hyperperfusion syndrome following STA-MCA anastomosis is still controversial.7,10)
We report a case of hyperperfusion syndrome associReceived

March 3, 2010;

Accepted

May 19, 2010

1099

ated with non-convulsive status epilepticus (NCSE) following STA-MCA anastomosis for M1 occlusion, which
demonstrates the exact temporal relationship between
clinical findings, CBF measurements, and electroencephalography (EEG) findings in hyperperfusion syndrome.

Case Report
A 77-year-old right-handed man had been treated with 100
mg of aspirin under a diagnosis of multiple cerebral infarctions since age 75 years. He presented with left
hemiparesis due to infarction in the right corona radiata 6
months previously. His hemiparesis gradually improved
over several months of rehabilitation and he was introduced to our hospital to evaluate the capacity of
cerebral perfusion reserve.
On admission, he had mild left hemiparesis, but was independent in activities of daily living. Fluid-attenuated inversion recovery (FLAIR) magnetic resonance (MR) imaging demonstrated a small infarction in the right corona
radiata as well as periventricular hyperintensity on both
sides (Fig. 1A). MR angiography and computed
tomography (CT) angiography revealed occlusion (or severe stenosis) of the right M1 portion (Fig. 1B). All MR im-

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Fig. 1 A: Preoperative fluid-attenuated inversion recovery magnetic resonance (MR) image demonstrating a small infarction in the
right corona radiata with arteriosclerotic change in the bilateral corona radiata. B: Preoperative MR angiogram indicating occlusion (or severe stenosis) of the right M1 portion. C: Diffusion-weighted MR images on the 6th postoperative day demonstrating gyriform cortical hyperintensity in the posterior part of the middle cerebral artery (MCA) territory. D: MR angiogram on the 6th
postoperative day showing patency of the superficial temporal artery-MCA anastomosis and hypervascularity of the peripheral
branches of the right MCA.

Fig. 2 A, B: Preoperative N-isopropyl-p-[123I]iodoamphetamine single-photon emission computed tomography (IMP-SPECT) images
at rest (A) and after acetazolamide loading (B) showing cerebral blood flow (CBF) in the right middle cerebral artery (MCA) territory
is slightly decreased (A) and the vascular reserve capacity in the right MCA territory is markedly compromised (B, arrows). C:
[99mTc]-ethyl-cysteinate dimmer SPECT images on the 6th postoperative day showing increased CBF in the MCA territory (arrows), especially in the posterior part of the MCA territory (asterisks). D, E: IMP-SPECT images on the 20th postoperative day showing disappearance of the hyperperfusion of the right MCA territory (D), and improved vascular reserve capacity in the right MCA territory
after acetazolamide loading (E). Upper and lower rows are axial and coronal views, respectively.

aging was performed with a 1.5 T MR unit (Signa Exite
HD, version 12 software; GE Medical Systems, Milwaukee, Wis, U.S.A.). N-isopropyl-p-[123I]iodoamphetamine

single-photon emission computed tomography (IMPSPECT) showed that vascular reserve capacity was markedly compromised in the right MCA territory (Fig. 2A,

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Fig. 3 A: Electroencephalograms (EEGs) on the 6th postoperative day revealing frequent ictal discharges (rhythmic slow waves),
which originate from the right occipital region (O2 of the International 10–20 system, arrow), extending to the right temporo-parietal
region (P4 and C4, black lines) and then to the right frontal region (Fp2, dotted line). B: EEGs on the 9th postoperative day showing
no ictal discharge, although non-rhythmic slow waves were intermittently observed in the right fronto-parietal region. Relatively
well-organized background activity was noted on O2, which is the ictal onset zone, on the 6th postoperative day. C: EEGs on the 20th
postoperative day showing well-organized background activity in the bilateral occipital region, although intermittent slow waves
were noted in the right frontal region (reference; ipsilateral earlobe).

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Fig. 4 A, B: Ultrasonograms of the right superficial temporal artery (STA) on the 8th postoperative day (A) revealing marked increase in flow velocity in the systolic and end-diastolic periods (120.2 and 54.6 cm/sec, respectively) compared with the left STA (B;
57.6 and 4.9 cm/sec, respectively). C: Ultrasonograms of the right STA on the 32nd postoperative day showing decrease in flow velocity in the systolic and end-diastolic periods (62.2 and 22.9 cm/sec, respectively).

B). CBF in the right and left MCA territories was 31.81 and
33.29 ml/100 g/min, respectively (Fig. 2A). Regional
cerebrovascular reactivity (rCVR) after acetazolamide
loading in the right and left MCA territories was －21.69
and ＋11.79%, respectively (Fig. 2B). Therefore, right
STA-MCA anastomosis was scheduled.
Right fronto-temporo-parietal craniotomy was performed, and the parietal and frontal branches of the STA
were anastomosed with the M4 portions on the frontal and
temporal lobes, respectively. Occlusion times during the
STA-MCA double anastomosis were 25 and 14 minutes,
respectively. No cerebral contusion or subarachnoid
hemorrhage was observed at craniotomy. The postoperative course was uneventful and systemic blood pressure
was well controlled. However, the patient experienced deterioration of consciousness with confusion and worsening of left hemiparesis on the 6th postoperative day.
T1- or T2-weighted and FLAIR MR imaging failed to reveal additional abnormalities that could explain his neurological deterioration, but diffusion-weighted imaging
demonstrated gyriform cortical hyperintensity in the
posterior part of the MCA territory (Fig. 1C). The low apparent diffusion coefficients score of the right posterior
temporal lobe was decreased by 33% compared with that
in the contralateral side. MR angiography showed an apparently patent STA-MCA bypass as a thick hyperintense
area compared with the preoperative images (Fig. 1D), as
well as dilated branches of the MCA supplied by the bypass. [99mTc]-ethyl-cysteinate dimmer (ECD)-SPECT observed an increase in CBF in the MCA territory, especially
in the posterior part of the MCA territory (Fig. 2C).
EEG showed frequent ictal discharges on the right
hemisphere, although convulsive seizures were not apparent. Ictal EEG patterns were stereotyped; rhythmic slow
waves, which originated from the right occipital region
(O2 of the International 10–20 system), extended to the

right temporo-parietal region (P4, C4) and then to the right
frontal region (Fp2) (Fig. 3A). Duration of the seizure activities was 19–63 seconds (42.1 sec average). Fourteen
episodes of ictal activities were recorded during 15
minutes. No paroxysmal activities were noted during the
interictal period.
Ultrasonography examination of the STA demonstrated
marked increases in flow velocities of the right STA in the
systolic and end-diastolic periods (120.2 and 54.6 cm/sec,
respectively) compared with the left STA (57.6 and 4.9
cm/sec, respectively) (Fig. 4A, B). Based on the diagnosis
of hyperperfusion syndrome associated with NCSE,
phenytoin was intravenously administered and a free radical scavenger (edaravone) was given.
The patient became well-orientated on the 9th postoperative day. EEG detected no ictal discharge, although nonrhythmic slow waves were observed in the right frontoparietal region. Relatively well-organized background activities were noted in O2, the location of the ictal onset
zone on the 6th postoperative day (Fig. 3B). The patient's
neurological condition had completely returned to that of
the preoperative period on the 18th postoperative day. EEG
showed well-organized background activity in the bilateral occipital regions (O1 and O2), although intermittent
slow waves were noted in the right frontal region (Fig.
3C). Diffusion-weighted imaging demonstrated disappearance of cortical hyperintensity in the MCA territory on the
postoperative 20th day. MR angiography showed that
hypervascularity of the peripheral branches of the right
MCA had disappeared. IMP-SPECT revealed disappearance of the hyperperfusion of the right MCA territory on
the 20th postoperative day (Fig. 2D). CBF was 55.73 and
55.57 ml/100 g/min in the right and left MCA territories,
respectively (Fig. 2A), and the vascular reserve capacity
after acetazolamide loading in the right MCA territory had
improved compared with that in the preoperative period

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NCSE Following STA-MCA Anastomosis
(Fig. 2E). rCVR was ＋55.73 and ＋55.57% in the right and
left MCA territories, respectively. Ultrasonography of the
right STA revealed decreased flow velocity of the right
STA in the systolic and end-diastolic periods (62.2 and
22.9 cm/sec, respectively) on the 32nd postoperative day
(Fig. 4C). The patient was transferred to another hospital
for further rehabilitation on the 40th postoperative day.

Discussion
Seizures or epilepsy are one of the major symptoms in
patients with hyperperfusion syndrome,17,22) but surprisingly few reports describe the EEG findings. EEG obtained during hyperperfusion syndrome revealed periodic
lateralizing epileptiform discharges (PLEDs) on the side of
the brain ipsilateral to the CEA, even in the absence of seizures or during the postictal state.19) NCSE is defined as a
change in behavior and/or mental process from the baseline associated with ongoing seizure activity or continuous epileptiform discharges on EEG in the absence of convulsive symptoms.2,16,20) Epileptic activity causes increased metabolic demand in the involved cortex, which is
accompanied by temporarily increased regional cerebral
perfusion.6,8) Since PLEDs are one of the EEG patterns in
patients with NCSE,2,9) the pathophysiology of ``ictal''
hyperperfusion could be similar to that observed in our
case.
In the present case, EEG demonstrated frequent ictal
discharges that originated from the right occipital region
or temporo-occipital junction and extended to the central
and parietal region. During NCSE, diffusion-weighted imaging demonstrated marked gyriform cortical hyperintensity of the fronto-temporo-parietal lobe. Furthermore, this
hyperintensity did not completely match the vascular distribution of the MCA but almost coincided with the ictal
onset and spreading zone. This cortical hyperintensity is
one of the typical findings of partial status epilepticus and
is thought to represent cytotoxic and vasogenic edema of
the cortical lamina.14,21) During NCSE, the hyperperfusion
area on ECD-SPECT matched the vascular distribution of
MCA, but the most prominent area was not the anastomosis site but the posterior temporal lobe, which corresponded to the findings of EEG and diffusion-weighted imaging.
Diagnosis of hyperperfusion syndrome is usually based
on CBF findings obtained with SPECT or perfusion
CT.3,5,10,15,22) In this case, ECD-SPECT on the postoperative
6th day clearly showed increased CBF, especially in the
posterior part of the MCA territory, which disappeared on
IMP-SPECT on the 20th postoperative day. However, the
procedures of SPECT and perfusion CT are expensive and
not available at the bedside. Instead, measurement of flow
velocity of M1 with transcranial ultrasonography is useful
for evaluating the hyperperfusion state after CEA or
CAS,22) since ultrasonography is noninvasive and easily
repeatable. Similarly, in our case, measurement of flow velocity of the STA with ultrasonography showed the
hemodynamic state of the MCA territory through the STAMCA anastomosis as previously described.1)
Mortality is reported to be mainly dependent on underlying etiology and age, but NCSE carries a poor prognosis

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so prompt diagnosis and subsequent treatment is important.2,16,20) SPECT and ultrasonography can clearly
demonstrate the hyperperfusion state, but cannot detect
neuronal function, especially neuronal excitability. In
contrast to hyperperfusion after CEA, hyperperfusion is
delayed after STA-MCA anastomosis.10) A possible explanation is that the lower-flow bypass may take time to mature and so could affect the dysautoregulated brain.10)
Another explanation is the delayed occurrence of seizure
activity, as in our case, although whether seizures or
hyperperfusion are the first phenomenon cannot be determined.
After the diagnosis of hyperperfusion syndrome is made
based on measurement of CBF, EEG is recommended even
in the absence of seizures. With the diagnosis of status
epilepticus, the first recommended treatment is rapid administration of antiepileptic drugs such as diazepam,
phenobarbital, and phenytoin.16,20) If prolonged seizure activity is noted, anesthesia with barbiturate or propofol
may be indicated.16,20) If increased CBF cannot overcome
the increased metabolic demand during status epilepticus,
neuronal ischemia can occur and free radicals are produced. Edaravone inhibits lipid peroxidation and vascular
endothelial cell injury, and ameliorates brain edema and
tissue injury. Antioxidants are beneficial in the treatment
of acute stroke. Recently, pretreatment with edaravone
decreased the incidence of post CEA hyperperfusion as
measured by SPECT.18)
The present case suggests that ictal hyperperfusion
should be excluded by EEG, even in the absence of seizures, after the diagnosis of hyperperfusion syndrome following STA-MCA anastomosis based on CBF measurement.

Acknowledgments
We thank Mses. Kuniko Yamamoto and Tomomi Kido, in
the Department of Clinical Laboratory, and Mr. Kohji
Miyazoe, in the Department of Radiology, Kyushu Rosai
Hospital for supporting our study.

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Address reprint requests to: Takato Morioka, M.D., Ph.D., Department of Neurosurgery, Kyushu Rosai Hospital, 1–3–1 Kuzuharatakamatsu, Kokuraminami–ku, Kitakyushu, Fukuoka
800–0296, Japan.
e-mail: takato＠ns.med.kyushu-u.ac.jp

Neurol Med Chir (Tokyo) 50, December, 2010