J Neurosurg 83:133–137, 1995

Imaging studies of cerebral hyperperfusion after carotid
endarterectomy
Case report
ANNA A. PENN, A.B, DON F. SCHOMER, M.D., AND GARY K. STEINBERG, M.D., PH.D.
Department of Neurosurgery and Division of Neuroradiology, Stanford University School of
Medicine, Stanford, California
U A case is reported of severe unilateral hemispheric edema and localized hemorrhage associated with seizures following endarterectomy of an ipsilateral high-grade carotid stenosis. Imaging studies including angiography, computerized tomography (CT), magnetic resonance imaging/angiography, and xenon-CT, suggested postoperative ipsilateral cerebral hyperperfusion. Cerebral hyperperfusion syndromes caused by a probable failure of vascular autoregulation
are rare but potentially serious complications after endarterectomy. The literature on this type of complication is briefly
reviewed, and the role of various imaging modalities in identification of the syndrome and in guiding management
decisions is emphasized.

KEY WORDS • carotid endarterectomy • carotid stenosis • cerebral hyperperfusion •
postoperative seizures • imaging studies

M

OST complications following carotid endarterec-

tomy are considered to be ischemic in nature,
caused either by embolization or occlusion.
However, postoperative neurological dysfunction may
also be related to a syndrome of cerebral hyperperfusion.
Hyperperfusion is a major increase (. 100%) in ipsilateral cerebral blood flow (CBF) well above the metabolic demands of the tissue after removal of a high-grade
carotid stenosis.13,28 We report a patient with multiple risk
factors for ipsilateral hyperperfusion who developed
seizures after undergoing carotid endarterectomy. We
have documented this case with the following imaging
studies: angiography, computerized tomography (CT),
magnetic resonance (MR) imaging/angiography, singlephoton emission computerized tomography (SPECT), and
xenon (Xe)-CT. We thus demonstrate both the changes
that may be associated with hyperperfusion and the role of
imaging studies in the diagnosis and management of this
unusual syndrome.

Case Report
This 53-year-old woman had a long history of carotid
disease, including bilateral endarterectomy at 24 years
of age, and subsequent left subclavian to left common
carotid artery (CCA) saphenous vein grafting with a vein
J. Neurosurg. / Volume 83 / July, 1995

patch graft of the left internal carotid artery (ICA) at
25 years of age. She presented to a community hospital
in 1993 with right-sided hemisensory disturbance and expressive aphasia. Her symptoms resolved within 24 hours;
however, despite heparin anticoagulation therapy and continuation of her routine aspirin antiplatelet therapy, she
had a second transient ischemic attack (TIA) consisting
of tingling of her right shoulder. A cerebral angiogram
demonstrated occlusion of the left CCA at its origin. A
saphenous vein graft with end-to-side anastomosis to the
left subclavian artery several centimeters distal to the vertebral artery origin, and end-to-end anastomosis to the left
CCA bifurcation were identified. A severe (. 95%) circumferential stenosis was present near the distal anastomosis site, with poststenotic dilation of the left ICA (vein
patch) (Fig. 1). Occlusion of the right CCA origin with
distal reconstitution via muscular collaterals from the right
vertebral artery was present. Patency of the left vertebral
artery was also demonstrated.
The patient’s medical history was remarkable for the
prior cerebrovascular procedures noted above, with intermittent TIAs since those surgeries, but no permanent neurological deficits. She also had chronic obstructive pulmonary disease, coronary artery disease, hyperlipidemia;
and she smoked heavily.
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A. A. Penn, D. F. Schomer, and G. K. Steinberg

FIG. 1. Left subclavian artery angiogram showing a lateral view
of the saphenous vein graft to the common carotid artery and
revealing a high-grade (≥ 95%) stenosis at the site of the previous
anastomosis (arrow), with poststenotic dilation of the vein patched
internal carotid artery.

Examination. The patient was transferred to Stanford
Medical Center, where examination revealed a loud left
carotid bruit. She was neurologically normal except for
poor recent memory and a mild right pronator drift. Collateral flow to the left hemisphere was poor, with the fetal
origin of the left posterior cerebral artery limiting important collateral contribution from the posterior circulation
(Fig. 2A). Right carotid occlusive disease was also
demonstrated, with filling of the middle cerebral artery
(MCA) territory via collateralization primarily from a
large right posterior communicating artery. Also in evidence were reverse flow through the right ophthalmic
artery, as well as reconstitution of the right ICA via collateral vessels (Fig. 2A). An MR image/angiogram obtained just prior to surgery showed a small left hemisphere
watershed infarction in the centrum semiovale (Fig. 2B,
arrow).
Operative and Postoperative Course. The patient
received intravenously administered heparin until surgery
(partial thromboplastin time, 50–70 seconds). A left
carotid endarterectomy was performed and revealed a
high-grade stenosis (. 95%) of the left CCA at the anastomosis site between the saphenous vein graft and the
CCA, but minimal plaque elsewhere. A shunt was used,
and total cross-clamp time was 2 minutes for shunt placement and 4.5 minutes for shunt removal. Heparin antico134

FIG. 2. Magnetic resonance (MR) angiograms/images. A: A
direction-sensitive three-dimensional phase-contrast MR angiogram through the circle of Willis revealing relatively poor flow to
the left hemisphere with development of leptomeningeal collateralization. Velocity encoding during image acquisition allows for
flow direction analysis. High signal (white) depicts anteroposterior
flow. Retrograde (anteroposterior) flow seen in the right ophthalmic artery (OA) (arrow) suggests that this vessel serves as a
collateral from the right external to the internal carotid artery
(ICA). Flow in the right posterior communicating artery is also
reversed (posteroanterior), suggesting that it serves as a collateral
from the posterior circulation (noncomposite data not shown). The
left hemisphere cannot develop these additional collateral sources
because the left posterior cerebral artery has a fetal origin from the
ICA and the external carotid artery is occluded preventing recruitment of the OA. Flow to the left hemisphere is therefore greatly
impaired. B: Selected T2-weighted (TR 2000 msec, TE 80 msec)
conventional spin-echo MR image of the brain demonstrating a
focal area of signal hyperintensity (arrow) in the deep white matter of the left hemisphere, compatible with a watershed infarct.

agulation therapy was continued throughout surgery and
an additional 5000 U was administered prior to crossclamping. Heparin was not reversed. Blood pressure was
tightly controlled postoperatively, keeping the mean arterial pressure between 70 and 90 mm Hg for the 1st day,
then keeping systolic blood pressure less than 120 mm Hg
and less than 140 mm Hg for the 2nd and 3rd days, respectively. Her immediate postoperative recovery was uneventful and her right pronator drift resolved.
After discharge on the 4th postoperative day, she had
a witnessed focal motor seizure with secondary generalization. She presented to the community hospital in an
unresponsive condition and was treated with dilantin and
decadron. A CT scan revealed severe left hemisphere
white matter hypodensity with vasogenic edema and a
small hemorrhage in the left temporal region (Fig. 3A and
B). Emergency carotid ultrasound and a carotid angiogram revealed a widely patent endarterectomy site and excellent flow through her left CCA and ICA graft (Fig. 4).
A SPECT study indicated delayed filling and hypoperfusion of the right cerebral hemisphere relative to the left
and a region of increased radionucleotide uptake in the left
temporal region (Fig. 5). Her neurological status returned
to baseline the following day and no further seizures were
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Hyperperfusion after endarterectomy

FIG. 3. Postoperative computerized tomography (CT). Axial
CT scan of the brain at the level of the ventricles (A), and centrum
semiovale (B) obtained to investigate postoperative seizures
revealing extensive vasogenic edema in the left hemisphere and
a small focal hemorrhage in the left posterior temporal region
(arrow). Similar views obtained 2 months later (C and D), revealing complete resolution of these findings.

noted. An episode of hypertension was noted during this
hospitalization, and when she was discharged she was
receiving antihypertensive medications as well as dilantin
and aspirin. She was well until 2 months later when she
had another TIA causing right upper-extremity weakness.
A CT scan revealed resolution of the earlier edema with
no acute infarction or hemorrhage (Fig. 3C and D).
Coumadin therapy was initiated and she has since
remained stable. A Xe-CT scan obtained 3 months after
the seizures showed asymmetrical blood flow to the two
hemispheres, with normal blood flow to the left hemisphere, low normal flow to the right hemisphere, and good
flow reserves bilaterally.
Discussion
The incidence of hyperperfusion syndromes after
carotid endarterectomy is reported to be between 0.3%
and 1.2%.6,15,21,23,28 The symptoms cover a wide spectrum
from benign to fatal, and include ipsilateral headaches,
seizures, and intracerebral hemorrhage. Risk factors include: a high-grade stenosis (. 70%); a large pressure
J. Neurosurg. / Volume 83 / July, 1995

FIG. 4. Postoperative and postseizure cerebral angiogram.
Postoperative angiography in the frontal plane demonstrating wide
patency of the endarterectomy site and high flow in the supraclinoid portion of the left internal carotid artery and its branches. The
middle cerebral artery and anterior cerebral artery territories fill
briskly.

gradient across the stenosis; poor collateral flow; contralateral carotid occlusion; evidence of chronic ipsilateral hypoperfusion; pre- and postoperative hypertension;
and perioperative anticoagulation or antiplatelet therapy.2,6,15,21–23,28 Our patient’s preoperative risk factors and
her postoperative imaging studies support the hypothesis
that a mechanism of hyperperfusion led to her seizures.
The angiographic studies indicate an elevated risk due to
the high-grade stenosis and contralateral carotid occlusion. Evidence obtained by MR imaging/angiography of
poor hemispheric collateral flow and the fetal origin of the
posterior communicating artery, in association with a
watershed infarct, suggest chronic hypoperfusion (lack of
collateralization from the posterior circulation has recently been identified as strongly correlated with evidence of
hypoperfusion).18 Postoperatively, the extensive left hemisphere vasogenic edema seen after the seizure, and the
SPECT study, which shows an increased level of technetium 99m-Ceretec uptake in the left hemisphere, support the mechanism of hyperperfusion.
The incidence of seizures following all carotid endarterectomy is 0.4% to 1.0%.15,28,30 Sundt27 initially
reported five patients with seizures early in the postoperative period following carotid endarterectomy, and, in
large-scale reviews, documented that patients with post135

A. A. Penn, D. F. Schomer, and G. K. Steinberg

FIG. 5. Single-photon emission computerized tomography
(SPECT). Rotational SPECT was performed 5 days after the
episode of postoperative seizure using intravenous 99mTc-Ceretec
contrast. A large focus of increased radionucleotide uptake is seen
in the left temporal lobe (arrow). A relative hyperperfusion of the
left hemisphere over the right hemisphere was observed in the
SPECT series. A 99mTc-glucoheptonate cerebral blood flow study
also demonstrated left hemisphere hyperperfusion with a 3 to 4
second delay in filling of the right hemisphere (data not shown).

operative seizures had preoperative ipsilateral CBFs that
were 75% of normal, with a postoperative increase to
approximately 170%.28 In 1.3% of postcarotid endarterectomy patients, an electroencephalogram demonstrated
periodic lateral epileptiform discharges, and 30% of these
patients had clinical seizures associated with an ipsilateral increase in CBF of up to four times baseline.15 The
hyperperfusion-related seizures usually occur within
the first 10 postoperative days.1,9,11,15,28 They are often preceded by severe, ipsilateral frontotemporal or periorbital
headaches: the most common symptom of hyperperfusion.5,15,26,28–30 Most often, they are focal motor seizures
with secondary generalization, frequently followed by a
postictal Todd’s paralysis.5,15,28–30 Whereas the seizures
may initially be very difficult to control, patients generally make a full recovery. However, progression to hemorrhage occurs in more than 40% of such patients9,15,26
and carries a mortality rate of greater than 50%.6,7,13,21–23
Overall, the risk of postendarterectomy hemorrhage is
elevated 10-fold in patients with hyperperfusion.13 Postoperative hypertension and pre- and postoperative anticoagulation or antiplatelet therapy have been identified
as significant risk factors for progression to hemorrhage,6,13,22,23,26 and postcarotid endarterectomy seizures
have been considered a significant contraindication for
anticoagulation therapy.13,26
Hyperperfusion is thought to result from an impairment
of autoregulation. Long-standing decreased flow across a
stenosis leads to inappropriate vasodilation, development
of cerebral edema, breakdown of the blood-brain barrier,
and possible hemorrhage when normal perfusion is re136

established.3,12,13,23,24 Eighty percent carotid stenosis21 has
been associated with postoperative hyperperfusion, and a
stenosis of 95% to 99% carries the highest risk.6,13,15,23
Severe stenosis may induce maximum dilation of cerebral
arterioles, with cerebral autoregulation being reset to a
low CBF.12,13,15,22,23,28 Episodes of acute ischemia may also
impair vascular reactivity. After endarterectomy, the vasculature is unable to respond immediately to increased
perfusion pressures, and edema or hemorrhage may result.
Autopsy studies of postcarotid endarterectomy hemorrhage patients have demonstrated changes resembling
malignant hypertension, including fibrinoid necrosis of
arterioles, and red blood cell extravasation into cerebral
parenchyma associated with severe edema.3 These histological changes may occur specifically in the presence of
perioperative hypertension or acute ischemic insult.16 The
mechanism of postendarterectomy hyperperfusion parallels Spetzler’s normoperfusion pressure breakthrough theory,24 and cases such as ours suggest that this mechanism
may produce seizures and hemorrhage.
Imaging studies are crucial in identifying hyperperfusion in postendarterectomy patients with seizures.
Magnetic resonance imaging/angiography may provide a
method for identifying those at high risk for hyperperfusion due to poor collateral vessels and chronic preoperative hypoperfusion, and, although it cannot be recommended in the assessment of all carotid endarterectomy
patients, it is warranted in selected patients with highgrade stenoses. Once hyperperfusion syndrome is suspected, there are a variety of studies that may aid in
its diagnosis. The subcortical hypodensity seen on our
patient’s postseizure CT scan is characteristic of vasogenic edema and is unlikely to be due directly to the
seizures or to acute infarct, as neither has been reported to
cause this striking generalized pattern of edema. Although
emboli could contribute to this picture, progression to
hemorrhage, seen focally in our patient, is extremely rare
in seizure patients without evidence of hyperperfusion.
The literature reports a number of different radiological
findings in hyperperfusion cases: no radiological changes,
patchy edema, and two cases similar to ours in which
an ipsilateral region of subcortical hypodensity was seen
after an episode of seizures.5,7,15,29,30 Severe ipsilateral
hypodensity after carotid endarterectomy has also been
reported in a case of temporary neurological deterioration
unaccompanied by seizures.2
Because the symptoms and radiological signs of hyperperfusion are variable, it may be beneficial to assess CBF
using SPECT/radionucleotide or other methods. XenonCT flow studies have the advantage of assessing the CBF
reserve capacity and indicating quantitative increases in
flow. It is the best method for demonstrating hyperperfusion; however, it is costly and often unavailable. The use
of the simple, inexpensive method of transcranial Doppler
(TCD) to evaluate postoperative MCA velocities is also
under investigation.4,8,14,17 Elevated ipsilateral CBF in at
least the 1st postoperative week has been shown by bedside 133Xe monitoring22 and TCD measurements of MCA
velocity.4 Furthermore, patients who have little increase in
MCA velocity with preoperative vasodilator challenges,
as shown by TCD, have abnormally elevated MCA velocities postoperatively8,17 and may have symptoms of hyperperfusion, including seizures.8
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Hyperperfusion after endarterectomy
Management to reduce the threat of hyperperfusion is
essential in high-risk patients. It is prudent to diligently
control blood pressure not only in patients with symptoms
of hyperperfusion, but in patients at increased risk of such
syndromes. It has been suggested that equalization of ipsiand contralateral TCDs could be used to optimize blood
pressure control.8 It has also been suggested that antihypertensive medications that increase CBF, such as
hydralazine, may be inappropriate in these patients.19,20 To
reduce the risk of catastrophic hemorrhage, anticoagulation therapy must be carefully considered and may be best
avoided. The use of prophylactic anticonvulsant drugs
in high-risk patients has been recommended,11 but remains controversial. Future interventions may be aimed
at pharmacological prevention of reperfusion hyperemia,
by agents that attenuate this phenomenon,10,25 and such
interventions may be particularly valuable in high-risk
patients.
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Manuscript received June 24, 1994.
Accepted in final form September 13, 1994.
Address reprint requests to: Gary K. Steinberg, M.D., Ph.D.,
Department of Neurosurgery S006, Stanford University Medical
Center, Stanford, California 94305.

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