(Stroke. 1999;30:407-413.)
© 1999 American Heart Association, Inc.
Original Contributions |
An Additional Monitoring of Regional Cerebral Oxygen Saturation to HMPAO SPECT Study During Balloon Test Occlusion
From the Departments of Neurosurgery (M.K., M. Onizuka, H.T., S.S.) and Radiology (M. Ochi), Nagasaki University School of Medicine, Nagasaki, Japan.
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Abstract |
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Background and Purpose—To increase the reliability of 99mTc–hexamethyl propyleneamine oxime (HMPAO) single photon emission computed tomography (SPECT) study in the evaluation of hemodynamic change with balloon test occlusion (BTO) of the internal carotid artery, we attempted to clarify the usefulness of additional monitoring of regional oxygen saturation of the brain (rSO2).
Methods—During BTO, rSO2 monitoring with transcranial near infrared spectroscopy was performed 17 times on 16 patients. Asymmetrical distribution of the tracer was classified visually as follows: group 1, little or no asymmetry, and group 2, moderate or severe asymmetry. Seven regions of interest (ROI) were defined in the middle cerebral artery area of each hemisphere, and the asymmetry index (AI)=200x(Cnon-Coccl)/(Cnon+Coccl)), where Cnon=mean counts on the nonoccluded side, and Coccl=mean counts on the occluded side were also calculated. Then, mean AI (MAI) was obtained from AI of 7 ROIs for each study.
Results—Of the 17 procedures, 10 BTOs were in group 1 and 5 BTOs
were in group 2. Two patients did not undergo SPECT study because of
the immediate appearance of a neurological deficit with BTO; they were
defined as group 3. The MAI in group 1 was 2.6±3.3%, which was
significantly smaller than the MAI in group 2 (25.6±5.0%,
P<0.02). The 
rSO2 (baseline
rSO2-rSO2 during ICA occlusion) with BTO in
group 1 was 1.5±1.4% (n=10), which was statistically smaller than
that in group 2 (5.5±1.3%, n=4, P<0.05). The
rSO2 in group 3 was 9.0±0.0% (n=2). In group 1,
however, rSO2 began to decline when the stump pressure fell
to 45 mm Hg and always declined when the stump pressure fell
below 40 mm Hg. Furthermore, in group 1, a significant
correlation was observed between the rSO2 and stump
pressure (r=0.85, P<0.0001).
Conclusions—This preliminary study reveals that an obvious asymmetrical SPECT pattern always accompanies a profound decrease in rSO2 and that rSO2 parallels a severe reduction in stump pressure in cases exhibiting a symmetrical SPECT pattern. Thus, the cerebral oximetry sensitively reflects the cerebral oxygenation, and simultaneous measurements of rSO2 and stump pressure with 99mTc-HMPAO SPECT study apparently are useful in evaluating hemodynamic integrity with BTO.
Key Words: balloon dilatation • cerebral arteries • oximetry • tomography, emission computed
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Temporary or permanent occlusion of the internal carotid artery (ICA) is often required in the surgical treatment of patients with cerebral aneurysms, skull base tumors, or cervical tumors. Measurement of cerebral blood flow (CBF) during balloon test occlusion (BTO) has been used increasingly to raise the procedure's reliability to predict high-risk patients.1 2 3 4 Among several methods of CBF study, 99mTc–hexamethyl propyleneamine oxime (HMPAO) SPECT is used widely in clinical BTO because it is readily available and simple.5 6 7 8 9 Because 99mTc-HMPAO rapidly distributes in the brain tissue and is kept constant for a long time after intravenous injection,10 11 12 the CBF pattern during transient ICA occlusion can be evaluated by intravenous injection of 99mTc-HMPAO during BTO, followed by SPECT study after the completion of all BTO procedures. 99mTc-HMPAO SPECT provides fair tomographic resolution of CBF and detects focal flow defects or asymmetrical CBF distribution during BTO. However, because 99mTc-HMPAO SPECT reveals only relative CBF distribution, CBF changes with BTO compared with the baseline have not been evaluated using this method.
During skull base surgery and carotid endarterectomy, regional oxygen saturation of the brain (rSO2) monitoring with transcranial near infrared spectroscopy (NIRS) has been used and proven to provide reliable information about changes in cerebral perfusion during these procedures.13 14 Therefore, even with a bilateral symmetrical decrease of CBF, rSO2 monitoring can detect the relative CBF changes with BTO compared with baseline. In this study, we evaluated the feasibility and usefulness of additional rSO2 monitoring during BTO with 99mTc-HMPAO SPECT to estimate the hemodynamic changes with ICA occlusion.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Prior to ICA manipulation or ICA ligation, 16 patients (7 with cervical tumors, 5 with skull base tumors, and 4 with inaccessible aneurysms of the ICA) were examined with BTO of the ICA under rSO2 monitoring with NIRS (Table
). Informed consent was
obtained from the patients or their guardians. In these patients,
99mTc-HMPAO SPECT study was also attempted after
balloon occlusion. However, if any neurological symptoms or signs
developed after inflation, the balloon was immediately deflated to
restore blood flow without SPECT study.
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BTO
All procedures were performed under local anesthesia
with the patients in a fully awake state. After a neurological
examination and 3- or 4-vessel angiogram, cross-filling via the
communicating arteries was examined by contralateral carotid angiogram
or vertebral angiogram under manual compression of the objective
carotid artery. Then, a 7F balloon catheter was introduced into the
carotid artery and placed at the C1 or C2 level. Systemic
heparinization (5000 IU) was routinely used. In principle, a trial BTO
was first performed for 5 minutes to obtain an outline of
symptomatic tolerance or changes in stump pressure and
rSO2 level. The complete occlusion of ICA was
confirmed by a drop in the stump pressure and changes in the
arterial pulse wave. After the trial BTO, patients were
transferred from the angiography suite to radioisotope suite
with the balloon deflated but still in place. In the radioisotope
suite, mean systemic pressure was reduced by approximately 20% with
the continuous intravenous infusion of trimetaphan
camsilate, a ganglion blocking agent.15 The balloon was
inflated after stabilization of the systemic blood pressure.
Neurological status, stump pressure, and rSO2
were evaluated every 30 seconds. Five minutes after inflation, 740 MBq
of 99mTc-HMPAO was injected
intravenously. After the tracer injection, the ICA
occlusion was maintained for an additional 15 minutes. Finally,
protamine sulfate was used to reverse the effect of heparin.
SPECT Studies
SPECT imaging was performed after removal of the catheter and
stabilization of the patients, usually 30 to 60 minutes after
injection. SPECT was performed using a triple-head gamma camera (PRISM
3000; Picker International, Cleveland, OH) equipped with a low-energy
high-resolution fan beam collimator. A 20% window was centered on the
140 keV photopeak of 99mTc. One hundred twenty
30-second frames were acquired using the elliptical contour rotation
mode into a 128x128 image matrix. The images were prefiltered using a
Butterworth filter (cutoff frequency=0.266 to 0.302 cycles/cm,
order=8.1). The attenuation correction was set at 0.09. The
reconstructed slice thicknesses were 3.91 mm for the transaxial
planes and 7.81 mm for coronal and sagittal planes.
The SPECT images were analyzed both visually and
semiquantitatively. For visual analysis, 3 experienced
neurosurgeons (coauthors of this manuscript) ranked the asymmetrical
distribution of the tracer as little or none or moderate or severe
based on the color codes of the computer and the defined group 1
(Figure 1) or group 2 (Figure 2), respectively. Relative quantification
by means of region of interest (ROI) analysis was performed
retrospectively. A total of 7 ROIs were defined on each side of the
middle cerebral artery (MCA) area in 2 transaxial slices parallel to
the orbitomeatal line (Figure 3). The
slices were selected by 2 observers and were at the level of the
temporal and caudoputaminal region, and the mid-parietal region. The
round-shaped ROI consisting of 55 to 60 pixels was used, and the mean
count of tracer from the 7 ROIs in each hemisphere was calculated.
The degree of side-to-side asymmetry (AI) in the MCA territory was
then obtained using the equation
AI=200x(Cnon-Coccl)/(Cnon+Coccl),
where Cnon is the mean tracer count on the
nonoccluded side and Coccl is the mean tracer
count on the occluded side. Then, mean AI (MAI) was calculated from 7
ROIs in each SPECT study.
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Monitoring of rSO2, Systemic Blood Pressure, and
Stump Pressure
Using a cerebral oximeter (INVOS 3100; Somanetics Corp),
rSO2 was continuously monitored on the forehead
of the occluded side. Continuous monitoring of the arterial
pressure was performed with the sheath introducer placed in the femoral
artery and the balloon catheter placed in the ICA. In principle, the
rSO2, systemic blood pressure and stump pressure
at 5 minutes of ICA occlusion when the tracer was injected were used
for analysis.
Statistical Analysis
Values are expressed as mean±SD. The statistical differences of
MAI, stump pressure, and rSO2 (baseline
rSO2-rSO2 during ICA
occlusion) between the groups were evaluated using the Mann-Whitney
test. Correlation between the stump pressure and
rSO2 was evaluated by a simple regression
analysis. A significant difference in the statistical results
was defined as P<0.05.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Asymmetry in SPECT Images
Two patients exhibited right hemiparesis and aphasia immediately after left ICA occlusion; SPECT study could not be performed in these patients, and they were classified as group 3. Therefore, for those patients, the rSO2 and blood pressure just before the deflation of the balloon were used in the following studies. In the remaining 14 patients, 15 BTOs were performed without the appearance of focal neurological deficits and the occlusions examined with SPECT study. These 15 SPECT studies during BTO consisted of 10 from group 1 and 5 from group 2. An AI could not be obtained from 2 of the BTOs in group 1 because raw data were not recorded for these 2 patients. The mean MAI in group 1 was 2.6±3.3% (n=8), which was significantly lower than that in group 2 (25.6±5.0%, n=5, P<0.02). No patient in group 1 had a MAI exceeding 10%, whereas all MAIs in group 2 reached above 19%. A resting SPECT study was performed in 7 patients. The MAI in the resting SPECT ranged from -3.1% to 4.2%. The mean absolute value of the resting MAI was 2.3±1.5%, which was not statistically different from the MAI in group 1 but was statistically smaller than the MAI in group 2 (P<0.01).
Stump Pressure and Asymmetry Index
The mean stump pressures in group 1, group 2, and group 3 were
41.4±9.8, 31.2±15.3, and 29.0±9.9 mm Hg, respectively.
However, there was no statistical difference between them. The mean
stump pressure and MAI did not have a significant correlation
(r=0.497, P=0.0844, Figure 4).
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Monitoring of rSO2
Although the rSO2 was monitored in all 17
BTO procedures, the rSO2 level was unstable
during BTO in only 1 patient from group 2, which was then excluded from
the subsequent studies. The rSO2 in group 1
was 1.5±1.4% (n=10), in group 2 5.5±1.3% (n=4); this difference was
statistically significant (P<0.05). The
rSO2 in group 3 (9.0±0.0%, n=2) was also
greater than that in group 1 or group 2. Group 3, however, was too
small to evaluate statistical significance. In 8 of 10 patients in
group 1, the SPECT study with rSO2 monitoring was
performed under induced hypotension. In these patients, the preceding
5-minute test occlusion of the ICA with rSO2
monitoring was also performed under no hypotensive provocation in the
angiography suite. The rSO2 monitoring in the 18
BTO procedures indicated that even in group 1, the
rSO2 started to decrease if the stump pressure
fell to 45 mm Hg, and the rSO2 always
decreased when the stump pressure fell below 40 mm Hg (Figure 5). Furthermore, a significant linear
correlation existed in group 1 between the
rSO2 and the stump pressure during BTO
(r=0.85, P<0.0001).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Among several methods used to determine CBF distribution in BTO, 99mTc-HMPAO SPECT is used most frequently because of its wide availability. Reportedly, 99mTc-HMPAO SPECT is very useful in detecting unilateral asymmetrical distribution of CBF with BTO.5 6 7 8 9 It is generally accepted that areas of diminished perfusion are abnormal when the interhemispheric differential activity is greater than 10%.5 16 In the present study, visual classification of CBF distribution corresponded well with relative quantitative analysis; no MAI in group 1 exceeded 10%, and all MAIs in group 2 were higher than 19%. The present study also supports the feasibility and usefulness of 99mTc-HMPAO SPECT in high-risk patients because in the present study 5 of 15 BTOs showed significant asymmetry (group 2) without the appearance of neurological symptoms. Furthermore, significant asymmetry on 99mTc-HMPAO distribution was also observed in 1 patient, despite a fairly high level of stump pressure (Figure 2
, left). However, symmetrical distribution of
99mTc-HMPAO does not always indicate negative
hemodynamic changes during BTO. Well-developed
collateral circulation through the anterior communicating artery or
posterior communicating artery possibly leads to a bilateral reduction
of CBF with the occlusion of 1 carotid artery. A qualitative CBF study
with a stable xenon CT scan indicated that a symmetrical decrease in
CBF was frequently observed.17 18 Indeed, a stable xenon
CT scan is very useful for the quantitative evaluation of CBF; however,
balloon inflation must be performed on the CT table, and inhalation of
xenon-mixed gas for several minutes affects the neurological
observation during BTO. Furthermore, the stump pressure is not always
stable during BTO, especially under provocative
hypotension, and the duration of several minutes for a xenon CBF study
possibly affects the evaluation of CBF values. Yet,
99mTc-HMPAO is taken up rapidly by the brain with
little redistribution, allowing a snapshot of the brain perfusion at
the time of injection.10 11 12 CBF imaging during the
balloon inflation, thus, can be obtained simply by venous injection of
99mTc-HMPAO during ICA occlusion and scanning,
after all the BTO procedures have been completed. Furthermore, it
provides a fairly good spatial resolution of CBF compared with a xenon
CT study. The timing of the tracer injection may significantly affect
the development of perfusion abnormalities. A previous experimental
study, in which changes in CBF and tissue oxygen tension with
transorbital MCA occlusion were continuously monitored in the MCA area
of rabbits, indicated that collateral circulation developed promptly
within 5 minutes after the start of ischemia19 ;
the tracer was thus injected at 5 minutes after the start of BTO in the
present study. As a simple yet reliable technique for monitoring altered CBF or oxygenation of the brain, rSO2 monitoring by measurement of NIRS with the INVOS 310013 14 20 or other instruments21 has been used during skull base surgery, removal of a cervical tumor involving the carotid artery, and carotid endarterectomy. The sensor for the INVOS 3100 consists of a flexible pad (8.8x4.4 cm) with 1 light source and 2 photodetectors. The distances between the light source and 2 photodetectors were set at 30 and 40 mm to eliminate the interference of blood oxygen saturation from all extracerebral components. The cerebral oximetry used in this experiment reflects the change of cerebral oxygen saturation between the light source and the 40-mm distant photodetector.22 The rSO2 recording became stable within a few minutes except in 1 case, and it could be monitored continuously in 16 of 17 BTOs. Repeated carotid occlusion during a series of tests to verify the reproducibility was not performed in this study. However, 2 sets of BTOs were carried out within a 7-month period in patient 13. The rSO2 decreased by 6% in the first BTO and 7% in the second BTO. The mean stump pressure and MAI were 15 mm Hg and 23.5% in the first BTO and 22 mm Hg and 32.4% in the second BTO. These results might support the good reproducibility in the rSO2 monitoring in the present study.
A critical rSO2 level or
rSO2 to induce neurological deficit has not
been well established. In the present study, we monitored
rSO2 in addition to performing
99mTc-HMPAO SPECT to evaluate the change of
cerebral perfusion on the occluded hemisphere with BTO. Carlin et
al13 reported cases of awake carotid
endarterectomy in which the mean
rSO2 by carotid cross-clamp in patients
without the appearance of neurological deficit was 7.2%. Dujovny et al
reported14 on 2 patients who exhibited neurological
deteriorations with a fall in rSO2 of more than
10% after BTO. Our present results indicate that
rSO2 dropped by 9% immediately after balloon
occlusion of the left ICA in 2 patients who experienced right
hemiparesis and aphasia, whereas rSO2 decreased
by 4% to 7% without the appearance of a neurological deficit in
patients in group 2. Our previous study on the simultaneous
measurement of rSO2 and CBF indicated that 1000
mg acetazolamide increased CBF by 44.4% and
rSO2 from 64.2% to 69.6%.23
Holzschuh et al24 also demonstrated similar results. In
the present study, rSO2 was 5.5±2.1%
(n=4) in group 2, which was significantly higher than the
rSO2 in group 1 (1.5±1.4%, n=10).
rSO2 in group 3 was 9.0±0.0% (n=2), which
was also higher than the rSO2 in group 1;
however, no statistical difference could be found because group 3 was
too small. Although the relationship between rSO2
and CBF is not simply linear but is determined by Fick's equation, the
prominent fall of rSO2 in groups 2 and 3 suggests
that a fairly profound reduction in CBF develops with BTO in these
cases. Furthermore, even in group 1, if stump pressure fell to 45
mm Hg, then rSO2 started to decline, and
rSO2 always decreased when stump pressure fell
below 40 mm Hg. These results indicate that deterioration of
cerebral perfusion develops even in the case of group 1 when the stump
pressure falls below 40 mm Hg. The relation between asymmetrical
CBF distribution and stump pressure during BTO is still
controversial,25 26 and the present study did not
determine a significant correlation between them. In our study, stump
pressure fell below 40 mm Hg in 9 BTOs. Of these 9 BTOs, a focal
neurological deficit appeared immediately in 2 BTOs, and asymmetrical
distribution of CBF was observed in 3 BTOs, whereas
99mTc-HMPAO SPECT in the remaining 4 BTOs
exhibited symmetrical rather than asymmetrical CBF distribution. Our
results concerning the relation between rSO2,
stump pressure, and asymmetrical CBF distribution in SPECT study
indicate that a lower stump pressure does not always signify
asymmetrical CBF distribution; however, a stump pressure less than
40 mm Hg always accompanies a perfusion disturbance to
affect the rSO2 level. Furthermore, in group 1,
which exhibited little or no asymmetry with BTO, a significant linear
correlation between rSO2 and stump pressure
was demonstrated (r=0.85, P<0.0001). Lorberboym
et al16 reported that 4 of 18 patients in whom
99mTc-HMPAO SPECT study during BTO revealed
symmetrical distribution subsequently suffered from cerebral
ischemia after the permanent sacrifice of the carotid artery.
Although the etiology of their ischemic event was not clearly
identified and stump pressure during BTO was not evaluated in these
patients, the possible involvement of hemodynamic
factors is suggested in their report.
Among the patients in the present study, the following surgical procedures were performed: common carotid ligation in 2, permanent occlusion of the ICA in 1, transient occlusion of the ICA in 1, and resection followed by reconstruction of the common carotid artery in 1. Thromboembolic complications were observed in 1 patient in group 1 after permanent ICA occlusion. Although in the present study we were not able to reveal definitive criteria to predict hemodynamic complication with permanent ICA occlusion, our preliminary study indicates that obvious asymmetrical CBF distribution without the appearance of a neurological deficit always accompanies a profound decrease in rSO2, suggesting the development of a prominent reduction of CBF. Furthermore, even in patients with symmetrical CBF distribution during BTO, a decrease in mean stump pressure below 40 mm Hg always accompanies a decrease in rSO2, and rSO2 parallels a severe reduction in stump pressure in cases in which a symmetrical SPECT pattern is exhibited.
Thus, we verified in this study that rSO2
monitoring is a simple and easily applicable but very sensitive
indicator of the cerebral oxygenation, and we deduce
that the simultaneous measurement of
rSO2 and stump pressure with SPECT study is
useful in the evaluation of hemodynamic integrity after
BTO. Furthermore, rSO2 monitoring is now applied
for intraoperative monitoring in skull base surgery, carotid
endarterectomy, and neck surgery involving the
carotid artery. It provides useful information for the operative
manipulation of carotid artery under rSO2
monitoring to correlate rSO2 following BTO
with stump pressure and SPECT imaging preoperatively.
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Acknowledgments |
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The authors thank Hidenori Matsuo for his technical expertise for SPECT study.
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Footnotes |
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Department of Neurosurgery, Nagasaki University School of Medicine, 1-7-1, Sakamoto, Nagasaki, 852-8501, Japan.
Received September 4, 1998; revision received November 2, 1998; accepted November 2, 1998.
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