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(Stroke. 2001;32:1567.)
© 2001 American Heart Association, Inc.
Original Contributions |
Cerebral Vasoreactivity and Internal Carotid Artery Flow Help to Identify Patients at Risk for Hyperperfusion After Carotid Endarterectomy
From the Department of Neurosurgery, Hyogo Brain and Heart Center, Himeji (K.H., T.K., Y.S., M.K., K.K., J.K., S.F), and Department of Neurosurgery, Kobe University School of Medicine (N.T.) (Japan).
Correspondence to Kohkichi Hosoda, MD, Department of Neurosurgery, Hyogo Brain and Heart Center, 520 Saisho-ko, Himeji 670-0981, Japan. E-mail khosoda{at}venus.dti.ne.jp
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose—Hyperperfusion syndrome is a rare but potentially devastating complication after carotid endarterectomy (CEA). The aim of this study was to investigate whether preoperative measurement of cerebral vasoreactivity (CVR) and intraoperative measurement of internal carotid artery (ICA) flow could identify patients at risk for hyperperfusion after CEA.
Methods—For 26 patients
with unilateral ICA stenosis 
70%, cerebral blood flow (CBF)
and CVR were investigated before and 1 month after CEA, with resting
and acetazolamide-challenge single-photon emission CT. CBF
on the first postoperative day was also measured. ICA flow was measured
before and after reconstruction by electromagnetic flowmeter during
surgery.
Results—Ipsilateral CBF
on the first postoperative day significantly increased relatively
(56.6±53.2%) as well as absolutely (37.9±8.8 to 57.7±18.0 mL/100 g
per minute) in the reduced CVR group (CVR <12%) but not in the normal
CVR group (CVR 12%) (10.3±15.5% and 40.6±7.9 to 43.9±5.7 mL/100
g per minute, respectively). One month later, this difference almost
disappeared. Two patients showed ipsilateral CBF increase of 100%. A
significant association of intracerebral steal with
hyperperfusion (CBF increase 100%) on the first postoperative day
was also observed. ICA flow increase after reconstruction significantly
correlated with CBF increase on the first postoperative day in the
reduced CVR group but not in the normal CVR group. The threshold of ICA
flow increase for hyperperfusion was estimated to be 330 mL/min in the
reduced CVR group.
Conclusions—Single-photon emission CT with acetazolamide challenge and ICA flow measurement during surgery could identify patients at risk for hyperperfusion after CEA, in whom careful monitoring and control of blood pressure should be initiated even intraoperatively.
Key Words: blood flow • carotid endarterectomy • cerebral blood flow • tomography, emission computed • vasomotor reactivity
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Most postoperative complications of carotid endarterectomy (CEA) are ischemic in nature, caused by embolization or inadequate cerebral protection in patients with poor collateral supply. In a small subset of patients, however, postoperative neurological deficit may also be related to hyperperfusion, which is defined as a major increase in ipsilateral cerebral blood flow (CBF) well above the metabolic demands of the brain tissue after removal of a high-grade carotid stenosis.1 2 The patients with hyperperfusion may develop the classic clinical triad, which includes severe unilateral headache, face and eye pain, seizures, and intracerebral hemorrhage.1 2 3 4 According to the literature, intracerebral hemorrhage is reported to occur in 0.4% to 1.8% of patients after CEA.2 4 5 6 7 8 9 The largest series reported that intracerebral hemorrhage constituted approximately one fifth of perioperative strokes.8 The prognosis for these patients is poor, with mortality rates of 36% to 63%, and survivors have significant morbidity. However, less florid manifestations of hyperperfusion are probably more common.10
Risk factors of this syndrome include long-standing hypertension, a high-grade stenosis, poor collateral blood flow, and contralateral carotid occlusion that often impairs cerebral hemodynamic reserve.11 A rapid restoration of normal perfusion pressure after removal of a tight stenosis by CEA could cause a large increase of blood flow through the internal carotid artery (ICA) and hyperperfusion in a region of brain that had been chronically ischemic with autoregulatory vasoparalysis. In other words, hyperperfusion after CEA may be equivalent to normal perfusion pressure breakthrough to describe the cerebral edema and hemorrhage that sometimes occur after the resection of an arteriovenous malformation.3 12 If this hypothesis is correct, the preoperative assessment of cerebral hemodynamic reserve and intraoperative measurement of ICA flow seem to be important in predicting this rare but potentially devastating complication. Many studies have reported the usefulness of single-photon emission CT (SPECT) with acetazolamide challenge for evaluation of cerebral hemodynamic reserve.13 14 15 16 17 In addition, SPECT has been reported to show increased radionucleotide tracer uptake in patients with hyperperfusion after CEA,18 19 20 even in the absence of CT findings.21
The purpose of this study was to investigate whether preoperative SPECT with acetazolamide challenge and intraoperative measurement of ICA flow could identify patients at risk for hyperperfusion after CEA.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Between December 1998 and April 2000, 34 consecutive patients underwent CEA, 26 of whom fulfilled the following criteria and entered the present study. Inclusion criterion was unilateral ICA stenosis
70%. Exclusion criteria were bilateral carotid
lesions, intracranial artery stenosis or occlusion, and/or
major disabling stroke. Twenty-two of the 26 patients were male, and 4 were female. Mean age was 69.5±6.8 years (mean±SD), ranging from 57 to 84 years. Twenty-one patients were hypertensive, and 8 had diabetes mellitus. Seventeen patients showed ipsilateral carotid territory symptoms. Transient ischemic attacks (TIAs) referring to the relevant carotid artery were the only symptoms for 5 patients. Three patients had suffered TIAs with subsequent strokes, and 9 patients had suffered strokes only. All stroke patients had made good functional recoveries. Nine patients exhibited asymptomatic ICA stenosis.
Preoperative CT and MRI demonstrated no signs of infarction in 11 patients. Infarctions were seen in the hemisphere ipsilateral to the side of ICA stenosis in 15 patients. Fourteen of them represented symptomatic infarctions correlating with clinical presentation of TIA or stroke. The final patient represented asymptomatic infarctions. Two patients had asymptomatic infarction in the contralateral hemisphere.
All patients underwent preoperative angiography. Overall
average of the degree of ICA stenosis was 85.0±10.1%, with a
range of 70% to 99%, according to the method of the North American
Symptomatic Carotid Endarterectomy
Trial.22 There was no
patient with 30% stenosis of contralateral ICA.
All patients underwent surgery under general anesthesia. Thirteen patients underwent surgery on the left side and 13 on the right side. An indwelling shunt (high-flow shunt) was routinely used.23 We obtained informed consent from all patients or their next of kin.
Blood flow through the ICA was measured before and after reconstruction by a cuff probe of an electromagnetic flowmeter (Nihon Koden MFV-3200 FG) during CEA.
CBF Studies
The resting CBF was assessed by means of SPECT, with
a rotating dual-headed gamma camera (GAMA View SPECT 2000 H-20,
Hitachi) before CEA, 1 day after CEA, and 1 month after CEA. We
also measured cerebral vasoreactivity (CVR) to the
acetazolamide challenge for evaluation of cerebral
hemodynamic reserve before and 1 month after CEA. Five
to 7 days after resting SPECT, 1 g of acetazolamide
was given intravenously; 20 minutes later, SPECT was
repeated to investigate regional CVR (rCVR). The median time between
the latest ipsilateral neurological event and preoperative SPECT study
was 47.5 days (range, 18 to 178 days) for strokes and 30 days (range,
10 to 56 days) for TIAs. The median time between the preoperative SPECT
studies and CEA was 15 days (range, 2 to 73 days).
We performed CBF measurement with N-isopropyl-p-[123I]iodoamphetamine (IMP) combined with a modification of arterial input sampling.17 24 25 26 The patient’s head was immobilized with a holder, and bandages were placed across the forehead and fastened to the holder. An arterial line was placed in the radial artery and connected to an infusion pump. A dose of 111 MBq (3 mCi) of [123I]IMP was injected into an arm vein. At the same time, the time-activity curve of the entire brain was monitored with a gamma camera in the anterior view until 15 minutes after injection. Arterial blood was withdrawn at a constant speed of 1.7 mL/min for 5 minutes immediately after injection. These arterial whole-blood samples were analyzed for true tracer activity with the use of octanol extraction. SPECT acquisition was started from 15 minutes after IMP injection and lasted for 35 minutes. Data were accumulated in 64 steps, and each step collected counts for 30 seconds. Data were collected in 64x64 matrices and were reconstructed in transaxial sections parallel to the orbitomeatal line with 8 mm thickness to allow the same area to be quantified between the preoperative and postoperative SPECT studies. After SPECT acquisition, the entire brain activity was obtained in the anterior view for 30 seconds. The attenuation correction technique was not used.
The equation for determining regional CBF (rCBF) is as follows:
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A cross-calibration factor between the rotating camera system and well counter was obtained with the use of a 20-cm-diameter cylindrical phantom filled with standard activity (0.35 µCi/mL). The factor was calculated by dividing the activity measured by well counter by reconstructed counts per pixel.
Reconstructed counts of tomographic images 30 minutes after injection, when the brain activity reached a plateau, were corrected to represent 5-minute reference values with the use of the monitored time-activity curve of the entire brain.
Cb values were calculated as follows:
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We measured rCBF by placing 6 to 10 regions of interest (each 16x16 mm) in bilaterally symmetrical regions of the middle cerebral artery territory on a SPECT image plane where the asymmetry of radioisotope uptake distribution was most prominent. The pairs that showed the largest difference in values were used. A region where infarction was seen on CT and/or MRI was carefully excluded from the evaluation.
The rCVR was calculated as follows:
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100% on the
first postoperative day, according to Piepgras et
al.2
Statistical Analysis
Descriptive statistics are presented as
mean±SD. For comparison study, we used ANOVA in a repeated-measures
design (independent variable: CVR status; within factors: side and
time point; dependent variables: CBF or CBF increase [%]) and
Student’s t test. Fisher’s
exact test was used for proportion analysis. Values of
P<0.05 are reported to be
significant. A commercially available software package was used
(Statview 5.0; Abacus Concepts and Statistica 4.1;
StatSoft).
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The patients were divided into 2 groups on the basis of the preoperative status of cerebral vasoreactivity, ie, normal CVR (rCVR
12%; n=17) or reduced CVR (rCVR <12%; n=9). Six patients in
the reduced CVR group demonstrated CBF decrease (-4.7±2.5%, ranging
from -2.1% to -9.5%) after acetazolamide challenge,
representing intracerebral steal
(Figure 1
, top row).
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All patients recovered without new major neurological
deficits after surgery. No patient exhibited postoperative
intracerebral hemorrhage. In 2 patients,
however, postoperative ipsilateral hyperperfusion (CBF increase of
100%) was clearly observed on SPECT on the first postoperative day
(Figure 1
, middle row), although postoperative CT scans were
normal. Incidence of postoperative hyperperfusion was higher in the
reduced CVR group (2/9; 22%) than in the normal CVR group (0/17; 0%),
but there was no significant difference
(Table). However, the incidence was significantly
higher in the intracerebral steal group (2/6; 33%)
than in the nonsteal group (0/20; 0%)
(P=0.046)
(Table).
There was no significant association between hyperperfusion and
clinical (age, hypertension, diabetes mellitus, and symptoms) or
physiological (degree of stenosis)
variables.
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Changes of CBF Before and After CEA
Ipsilateral CBF significantly increased on the first
postoperative day in the reduced CVR group (37.9±8.8 to 57.7±18.0
mL/100 g per minute; P=0.00003)
but not in the normal CVR group (40.6±7.9 to 43.9±5.7 mL/100 g per
minute)
(Figure 2). As described above, ipsilateral
hyperperfusion (CBF increase of 100%) on the first postoperative day
was observed in 2 patients who had demonstrated
intracerebral steal on the preoperative SPECT study
(Figure 2, right panel, black arrows). The preoperative
asymmetry of perfusion on both resting and
acetazolamide-challenge SPECT was more severe and diffuse
in the 2 patients than in other 4 patients with
intracerebral steal
(Figure 1, top row). These 2 patients suffered a unilateral
headache and mild confusion for a couple of days after CEA but
eventually fully recovered after strict control of blood pressure.
Ipsilateral CBF significantly decreased 1 month after CEA compared with
the values on the first postoperative day in the reduced CVR group,
returning to the normal range (57.7±18.0 to 41.9±5.9 mL/100 g per
minute; P=0.0004), but not in
the normal CVR group (43.9±5.7 to 43.4±6.4 mL/100 g per minute)
(Figure 2). No significant difference was observed between
preoperative CBF and CBF 1 month after CEA in both groups
(Figure 2). In some patients, however, preoperative
hypoperfusion was remarkably improved
(Figure 1, bottom row).
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significant difference between
normal and reduced CVR group; 
significant difference between
ipsilateral and contralateral CBF (all
P<0.008). See text for details.
Contralateral CBF increase was smaller but statistically
significant on the first postoperative day in the reduced CVR group
(43.5±9.1 to 51.0±14.7 mL/100 g per minute;
P=0.01) but not in the normal
CVR group (42.9±7.4 to 44.6±4.7 mL/100 g per minute)
(Figure 3). Interestingly, a large increase of
contralateral CBF on the first postoperative day was observed in the
same 2 patients who demonstrated ipsilateral hyperperfusion
(Figure 3, right panel, black arrows). Contralateral CBF
significantly decreased 1 month after CEA compared with the values on
the first postoperative day in the reduced CVR group, returning to the
normal range (51.0±14.7 to 44.2±6.7 mL/100 g per minute;
P=0.02), but not in the normal
CVR group (44.6±4.7 to 43.3±6.2 mL/100 g per minute)
(Figure 3). No significant difference was observed between
preoperative CBF and CBF 1 month after CEA in both groups
(Figure 3).
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Further analysis clearly demonstrated asymmetrical
changes of CBF after CEA in the reduced CVR group but not in the normal
CVR group. The ipsilateral CBF on the first postoperative day was
significantly higher than the contralateral CBF in the reduced CVR
group (P=0.00022), but it was
not significantly higher in the normal CVR group
(Figures 2 and 3). The ipsilateral CBF increase on the first
postoperative day as a percentage of the preoperative CBF was
significantly more pronounced compared with contralateral CBF increase
in the reduced CVR group (56.6±53.2% and 16.9±23.2%, respectively;
P=0.0000081)
(Figure 4) but not in the normal CVR group
(10.3±15.5% and 5.8±14.1%, respectively). In addition, CBF and its
percent increase on the first postoperative day were significantly
higher in the reduced CVR group than in the normal CVR group on the
ipsilateral side (P=0.0073 and
P=0.0025, respectively) but not
on the contralateral side
(Figures 2, 3, and 4). These results indicated a relative as
well as absolute ipsilateral CBF increase only in the reduced CVR
group. One month later this difference almost disappeared. However, a
small but significant difference was still observed between percent
increase of ipsilateral and contralateral CBF in the reduced CVR group
(P=0.015)
(Figure 4).
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Relationship Among CVR, ICA Flow, and CBF Increase
After CEA
The overall mean of ICA flow before and after
reconstruction was 79.8±48.6 mL/min (range, 15 to 194 mL/min) and
192.2±80.7 mL/min (range, 75 to 400 mL/min), respectively. The average
increase was 112.4±98.2 mL/min (range, -20 to 380 mL/min). The
increase of ICA flow after CEA was significantly larger in the reduced
CVR group than in the normal CVR group (204.7±102.5 and 63.5±50.0
mL/min, respectively;
P=0.00008).
A significant linear correlation was observed between ICA
flow increase after reconstruction and ipsilateral CBF increase on the
first postoperative day as a percentage of the preoperative CBF, with
the line defined by CBF increase (%)=-25.1+0.4xICA flow increase
(correlation coefficient
r=0.77,
P=0.015), in the reduced CVR
group
(Figure 5, right panel) but not in the normal CVR group
(Figure 5, left panel). If the formula is reversed, the 95%
CI associated with a predicted mean ICA flow increase for 100% CBF
increase on the first postoperative day is 207 to 332 mL/min.
Therefore, the threshold of ICA flow increase for hyperperfusion was
estimated to be approximately 330 mL/min. In fact, CBF increase >100%
was observed only in 2 patients with ICA flow increase >330 mL/min,
who had demonstrated intracerebral steal on
preoperative SPECT
(Figure 5, right panel).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The incidence of hyperperfusion, which is defined to be CBF increase of
100% after CEA, was reported to be 11.6%, according
to Piepgras et al.2 Of those
with hyperperfusion, intracerebral hemorrhage
developed in 3.3%. In contrast, only 0.24% of those with CBF increase
<100% developed intracerebral hemorrhage.
Taken together, the risk of intracerebral
hemorrhage in patients with hyperperfusion was >10 times that
of patients without hyperperfusion. Therefore, detection of
hyperperfusion after CEA is important in identifying patients at risk
of intracerebral hemorrhage after CEA. Some
previous studies suggested that patients with preoperative
hemodynamic failure run a definite risk for
hyperperfusion
syndrome.1 2 4 29
From these points of view, SPECT is very useful because it can
quantitatively measure both CBF and hemodynamic reserve
as cerebral vasoreactivity to acetazolamide challenge. The
cerebral vasoreactivity to CO2 or
acetazolamide has been proposed as a test for cerebral
hemodynamic
reserve.13 14 15 16 17
Acetazolamide is a carbonic anhydrase inhibitor
that causes a disequilibrium of the CO2 buffer
system and results in vasodilation at least as effective as inhalation
of 5%
CO2.30
Administration of acetazolamide induces a rapid and marked
increase in CBF, ranging from 20% to
80%,14 27 31 32
which corresponds to the vasoreactivity of the controls in the
present study. Recently, it has been demonstrated that
transcranial Doppler ultrasonography (TCD) with
acetazolamide challenge is also able to assess cerebral
vasoreactivity.33 34
However, TCD cannot measure CBF itself, in contrast to
SPECT.
The present study demonstrated that a significant
CBF increase on the first postoperative day was seen only in the
reduced CVR group but not in the normal CVR group. Furthermore, CBF and
its increase 1 day after CEA on the ipsilateral side were significantly
higher than those on the contralateral side in the reduced CVR group
but not in the normal CVR group. One month later this difference almost
disappeared. This relative as well as absolute ipsilateral CBF increase
is in accord with the previous
study.29 However, our
results more clearly demonstrated a significant association of reduced
CVR, which is directly measured on acetazolamide-challenge
SPECT, with postoperative hyperperfusion. It is noteworthy that the CBF
increase of >100% on the first postoperative day was only seen in 2
patients with intracerebral steal. Severe and diffuse
asymmetry on preoperative SPECT of the 2 patients seems to be
characteristic. A significant association of
intracerebral steal with the hyperperfusion (CBF
increase 100%) on the first postoperative day was also observed.
These results suggest that the basic mechanism responsible for the
hyperperfusion is massive vasodilatation due to loss of
vasoconstriction because of chronic cerebral ischemia distal to
the high-grade carotid stenosis. In this situation, the abrupt
restoration of perfusion pressure after surgical correction of a tight
ICA stenosis cannot be compensated for by vasoconstriction and
may result in cerebral edema and even cerebral hemorrhage, as a
consequence of a leaky capillary
bed.1 2 3 11
This is considered to be equivalent to the normal perfusion pressure
breakthrough seen after the resection of some arteriovenous
malformation.3 12
In addition, autopsy studies of patients who died of
intracerebral hemorrhage after CEA have
demonstrated intracerebral arterial
histological change resembling malignant hypertension,
including swelling and hyperplasia of endothelial
cells, extravasation of erythrocytes, and fibrinoid
necrosis.3 35
These findings are consistent with the cerebral
hemodynamics hypothesis described above.
Recent studies have demonstrated that intraoperative TCD monitoring can also identify patients at risk for hyperperfusion.7 36 The TCD criteria for hyperperfusion is >100% increase of ipsilateral peak blood flow velocity or pulsatility index of the middle cerebral artery, which seems to be analogous to hyperperfusion criteria in CBF measurement. Furthermore, repeated observations are more practical with TCD than SPECT. Results from the previous TCD study correlate well with results from the present study but also provide more information about the time course of recovery from hyperperfusion.37 It has been reported, however, that symmetrically elevated velocities in both middle cerebral arteries were seen in a patient with ipsilateral hyperperfusion identified on SPECT.21 In addition, TCD monitoring is not always possible for all patients because of a thick skull, resulting in a poor signal to noise ratio or no signal at all.7 36 When the limitations of TCD are considered, SPECT may be the better method for identifying hyperperfusion after CEA, although it is more expensive. TCD is more suitable for repeated monitoring.
Previous studies with direct intraoperative measurements of ICA flow before and after reconstruction demonstrated results comparable to those reported here, with means of 80 to 130 and 160 to 210 mL/min, respectively.29 38 39 40 In the present study ICA flow increase after reconstruction was significantly larger in the reduced CVR group than in the normal CVR group. In addition, ICA flow increase after reconstruction was significantly correlated with CBF increase on the first postoperative day in the reduced CVR group despite the 1-day interval between the measurement of ICA flow and CBF. This correlation was not observed in the normal CVR group. These results suggest that an extremely large increase of ICA flow after reconstruction occurs only in patients with severely impaired cerebral autoregulation. The 95% CI associated with a predicted mean ICA flow increase for 100% CBF increase on the first postoperative day suggests that the threshold of ICA flow increase for hyperperfusion is 330 mL/min in the reduced CVR group. Such a large increase of ICA flow was observed only in 2 patients with intracerebral steal and resulted in hyperperfusion. During surgery, therefore, an ICA flow increase after reconstruction may be a good indicator of hyperperfusion after CEA.
Once hyperperfusion syndrome is established, it is difficult
to control and
treat.9 34 Review
of the literature suggests that the first few postoperative days are
the high-risk period for intracerebral
hemorrhage after
CEA.35 Therefore, it is
important to diagnose patients as soon as possible to determine when to
start preventative measures. The present results imply that
severely reduced vasoreactivity (intracerebral steal)
and an excessive increase in ICA flow after reconstruction (>330
mL/min) may help to identify patients at risk for developing cerebral
hyperperfusion after CEA. Most authors recommend strict control of
blood pressure in the postoperative period to prevent hyperperfusion
syndrome.1 4 11 35 36
According to the present results, it is possible to start strict
control of blood pressure intraoperatively to prevent postoperative
cerebral hyperperfusion if the patients demonstrate ICA flow increase
of 330 mL/min. Because of the small number of cases in the
present study, however, a larger number of cases would be required
to establish the sensitivity and specificity of this value.
Conclusions
In the present study preoperative SPECT with
acetazolamide challenge and ICA flow measurement during
surgery seem to be sensitive methods to identify patients who are at
risk for hyperperfusion after CEA. Intracerebral steal
on SPECT enables us to select a small subset of patients among those
clinically suspected to be at risk for hyperperfusion. ICA flow
measurement may provide the opportunity to further distinguish patients
at risk and to start careful monitoring and control of blood pressure
intraoperatively to prevent postoperative hyperperfusion
syndrome.
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Acknowledgments |
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We want to express our gratitude to all members of the SPECT technical staff: Osamu Ueda, Yukihiro Otani, Toshiaki Yamaguchi, Masaru Ishihara, and Kenzo Sawada.
Received August 14, 2001; revision received October 27, 2001; accepted February 21, 2001.
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