Patterns of Cortical Oxygen Saturation Changes During
CO2 Reactivity Testing in the Vicinity of Cerebral
Arteriovenous Malformations
Carlo Schaller, MD; Johannes Schramm, MD; Dorothee Haun, PhD; Bernhard Meyer, MD
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Background and Purpose—The aim of this study was to test the hypothesis that patterns of cerebrovascular reactivity
(CVR) in the vicinity of cerebral arteriovenous malformations (AVMs) before and after resection are not specific for
this disease.
Methods—With a microspectrophotometer, cortical oxygen saturation (SO2) was measured under steady-state conditions
(PaCO2, 33 mm Hg) before and after removal of 22 AVMs and in 30 control subjects before and after transsylvian
amygdalohippocampectomy. Intraoperative vasoreactivity tests were performed by induced changes of end-tidal CO2
(25, 45, and 25 mm Hg) with simultaneous recording of local SO2 in all patients. CVR patterns were established by linear
regression analysis (P⬍0.05) to define parallel (positive) versus inverse (negative) behavior, and reactivity indexes were
calculated to define their degree.
Results—Cortical oxygenation under steady-state conditions increased significantly (P⬍0.05) from preoperative to
postoperative levels equally in both groups (preoperative AVM, 54.8⫾10.4%SO2; postoperative AVM, 73.1⫾10.1%SO2;
preoperative control, 52.7⫾9.1%SO2; postoperative control, 73.6⫾8.9%SO2). The rate of inverse CVR patterns increased
significantly (P⬍0.05) from before to after resection without showing statistically significant differences between
groups.
Conclusions—Local CVR patterns on presumably normal human cortex of control subjects are heterogeneous, including
inverse behavior, and are similar to those of AVM patients before surgery. After surgery, cortical hyperemia is present
in both groups, and a significant increase in inverse reactivity patterns interpreted as microvascular steal is noted. An
AVM-specific CVR pattern could not convincingly be proved. (Stroke. 2003;34:938-944.)
Key Words: cerebral arteriovenous malformations 䡲 cerebrovascular circulation 䡲 oxygen
T
he literature on the topic implies that specific patterns for
cerebrovascular reactivity (CVR) exist in the presence of
cerebral arteriovenous malformations (AVMs) and after their
resection. Some authors even speculate that these patterns
might be predictive of the occurrence of neurological deficits
or the so-called postoperative hyperperfusion injury syndrome.1– 6 “CVR overshoot” and impaired reactivity have
been noted and were rather arbitrarily interpreted as being
AVM specific and/or predictive.1,2 The results of other
studies, however, speak for a uniformly preserved vasoreactivity in the brain surrounding AVMs before and after their
obliteration.7–9 Thus, the question remains as to whether CVR
patterns in the presence of AVM are unique to this disease.
Recently, it was shown that spectroscopic techniques are
suitable for measuring the responses of HbO2 during induced
alterations of CO2 for the assessment of CVR in a clinical
setting.10,11 We adopted this algorithm for intraoperative
studies in AVM patients and control subjects by using a
previously described experimental method of high-resolution
remission spectrophotometry to answer the above question.
Subjects and Methods
This study was approved by the local ethics committee (protocol
121/96). All patients gave informed consent for participation.
Measurements of Intracapillary Oxygen Saturation
Values of intracapillary SO2 were measured with the Erlangen
Microlightguide Spectrophotometer (EMPHO II, Bodenseewerk
Gerätetechnik GmbH, BGT), which was introduced in 1989.12 It was
designed for fast, diffuse remission spectrophotometry by flexible
micro light guides in small tissue volumes of moving organs in situ.
Light in the visible domain illuminates tissue via the illuminating
fiber, and backscattered light is transmitted via 6 detecting fibers (Ø,
70 ␮m) arranged in a hexagonal pattern around the illuminating fiber
to a rotating bandpass interference filter disk. This serves as a
monochromating unit in the spectral range of 502 to 628 nm in 2-nm
steps. Spectra of 64 wavelengths per rotation are transmitted to a
photomultiplier, an AD converter, and a computer, in which 1 SO2
value per spectrum (1 single raw data point) is calculated by
algorithms described elsewhere.12 Under unchanged O2 consumption, SO2 changes reflect changes in regional cerebral blood volume.
These are linearly correlated with regional cerebral blood flow
(rCBF) changes, and the obtained SO2 values indicate tissue oxygen-
Received March 20, 2002; final revision received September 14, 2002; accepted October 16, 2002.
From the Department of Neurosurgery, University of Bonn, Bonn, Germany.
Reprint requests to Bernhard Meyer, MD, Department of Neurosurgery, University of Bonn, Sigmund-Freud-Str 25, 53127 Bonn, Germany. E-mail
[email protected]
© 2003 American Heart Association, Inc.
Stroke is available at http://www.strokeaha.org
DOI: 10.1161/01.STR.0000060880.59712.14
938
Schaller et al
Cerebrovascular Reactivity Patterns and Cerebral AVMs
ation and nutritive capillary flow.13,14 The high temporal (100
spectra/s) and spatial (75⫻75⫻250 ␮m) resolution permits a scanning procedure of superficial cortical capillaries by moving the light
guide above the brain.14
Study Groups and Protocol
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Twenty-two patients [9 female, 13 male; mean age, 35 years; range,
11 to 64 years; median clinical assessment according to the American Society of Anesthesiologists (ASA score), 2; range, 1 to 3] who
underwent elective removal of a supratentorial AVM (Spetzler/
Martin grades: I, n⫽5; II, n⫽7; III, n⫽7; IV, n⫽3) were included in
the study.
SO2 distributions were measured by scanning 31 cortical areas
(⬇5⫻5 mm2) located ⱖ2 cm from the AVM nidus before and after
resection. All areas were numbered and photographed for postoperative probe relocation. Approximately 700 SO2 values per area and
measurement were obtained to assess cortical oxygenation under
steady-state moderate hypocapnia (PaCO2, 33 mm Hg).
After each steady-state assessment before and after AVM resection, behavior of SO2 after induced changes in CO2 was tested by
modification of ventilation parameters within a range of 25 to
45 mm Hg end-tidal CO2 (etCO2) and vice versa with the light guide
probe held steady on the cortical areas. The observed behavior was
interpreted as a measure of local CVR.
939
Thirty patients (15 female, 15 male; mean age, 35.5 years; range,
16 to 67 years; median ASA score, 2; range, 1 to 3) with chronic
seizure disorder resulting from Ammon’s horn sclerosis were included as control subjects. None had evidence of intracranial
cerebrovascular or neoplastic disease. All underwent microsurgical
transsylvian selective amygdalohippocampectomy (AH) in which
self-retracting spatula are applied on the frontal and temporal
opercula to gain access to the inferior temporal horn.
With a protocol identical to that used for the AVM group,
steady-state cortical oxygenation was assessed on frontal and temporal opercula ⬇2 cm distant from the sylvian fissure before and
after dissection (after spatula release). Preoperative and postoperative vasoreactivity was tested on 30 areas as described above.
All patients were operated on under total intravenous anesthesia:
1.5 mg/kg propofol (maintenance dosage, 5 to 10 mg · kg⫺1 · h⫺1), 15
␮g/kg alfentanil (maintenance dosage, 0.1 to 0.2 mg · kg⫺1 · h⫺1), and
0.1 mg/kg vecuronium (maintenance dosage, 30 to 60 ␮g · kg⫺1 · h⫺1)
under inhalation of O2 and N2O at a ratio of 40:60. Mean arterial
blood pressure was monitored continuously via the radial artery.
Arterial (PaO2, PaCO2, pH) and venous blood (hematocrit) were taken
at the times of SO2 measurements.
Data Analysis
SO2 values obtained under steady-state hypocapnic conditions were
calculated as means (%SO2) per patient and pooled according to
Figure 1. Example of inverse CVR interpreted as microvascular steal in 1 patient in the control group (top). Illustrated is the inverse
behavior of SO2 on etCO2 during vasodilatation and vasoconstriction. Linear regression analysis was performed for these 2 parts of the
test separately (bottom). From the sign of the slopes, the behavior was categorized as parallel (⫹) or inverse (⫺). Slope of the linear
regressions (⫺1.451 and ⫺0.544 in this case) was then considered a measure for the RI.
940
Stroke
April 2003
TABLE 1. Data From Arterial Blood Gas Analyses, Venous Hematocrits, and Mean Arterial
Blood Pressure Obtained at Times of Measurements of Cortical SO2
AVM Group Before
Surgery (n⫽22)
AVM After Surgery
(n⫽22)
Control Group Before
Surgery (n⫽30)
Control Group After
Surgery (n⫽30)
Hb, g/dL
12.3⫾1.5*
11.2⫾1.8
11.5⫾1.3
11.2⫾2.9
Hct, vol%
36.6⫾4.3†
33.1⫾5.5
32.6⫾3.5
30.8⫾4.0
pH
7.45⫾0.03
7.48⫾0.04
7.46⫾0.04
7.48⫾0.04
PaO2, mm Hg
201.1⫾44.5
192.8⫾51.1
215.6⫾57.1
222.6⫾41.4
PaCO2, mm Hg
33.6⫾2.6
32.3⫾3.9
34.6⫾2.9
33.6⫾3.3
Heart rate, bpm
70.1⫾10.5
76.1⫾19.7
67.8⫾13.8
67.4⫾11.7
MABP, mm Hg
86.5⫾8.6
86.9⫾8.5
81.5⫾11.1
78.2⫾18.2
Temperature, °C
35.9⫾0.7
36.5⫾0.6
36.0⫾0.6
37.0⫾0.6‡
Hct indicates hematocrit; MABP, mean arterial blood pressure. Measurements were performed before and after
resection of cerebral AVMs and before and after transsylvian AH. Values are mean⫾SD.
*Different from AVM after surgery and control before surgery (P⬍0.05).
†Different from AVM after, control before, and control after surgery (P⬍0.05).
‡Different from AVM before, AVM after, and control before surgery (P⬍0.05).
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
and hematocrit, which were higher in the AVM group before
surgery, and postoperative temperature, which was higher in
control subjects than in all other groups (Table 1).
Comparison of SO2 data from measurements under steadystate conditions of moderate hypocapnia (PaCO2, 33 mm Hg)
showed that baseline values before AVM resection or transsylvian dissection were identical (AVM, 54.8⫾10.4%SO2;
control subjects, 52.7⫾9.1%SO2). In both groups, a significant increase in cortical oxygenation occurred after surgery
(AVM, 73.1⫾10.1%SO2; control subjects, 73.6⫾8.9%SO2),
without showing a significant intergroup difference among
the postresective values (Table 2).
The ratio of parallel to inverse behavior of CVR in groups
and times is displayed separately for the vasodilatory and
vasoconstrictive parts of the tests in Figure 2. In both groups,
after the vasodilating and vasoconstricting stimuli, a comparable percentage of patients with inverse behavior exists
before surgery. After surgery, the proportions of parallel
versus inverse CVR patterns are practically reversed, becoming significantly different from the preoperative situation.
The mean⫾SD group values of the RIs derived from the
slopes of the regression lines are displayed in Table 3 and
Figure 3. No statistically significant intergroup differences
were seen, except for the lower postoperative RI for parallel
behavior under induced vasodilation in AVMs, which was
significantly lower than preoperatively in the AVM group
groups (AVM versus control subjects) and times of measurements
(before versus after). Physiological variables and SO2 data were
compared via analysis of variance (ANOVA) with a level of
significance set at P⬍0.05. All values are given as mean⫾SD.
For analysis of SO2 reactivity as a measure of CVR, linear
regression analysis of SO2 on etCO2 was performed for increasing
and decreasing etCO2, with etCO2 as an independent variable.
Regressions not reaching statistical significance were excluded from
further analysis. If the slope of the regression line was positive, the
behavior of SO2 was categorized as parallel; in cases of a negative
slope, the behavior was categorized as inverse (see Figure 1). The
ratios in which these CVR patterns occurred within groups and/or
times of measurements were calculated and compared via ␹2 and
Fisher’s exact test (P⬍0.05).
To further quantify the degree of positive or negative CVR, a
reactivity index (RI) was introduced. For each test, the slope of the
linear regression of SO2 on etCO2 within exactly corresponding time
intervals was considered an appropriate measure for this reactivity
(Figure 1) because the dynamic component of the response was
included, as opposed to previously described end-point calculations
for RIs.10,11
ANOVA was used for comparison of RIs among groups and times
of measurements (eg, AVM before versus AVM after or AVM
before versus control subjects before) separately for inverse and
parallel CVR. In 9 AVM patients in whom ⬎1 area was assessed, the
mean RI was calculated.
Results
Physiological variables showed no significant differences
among groups (AVM versus control subjects) and times
(before versus after) in measurements, except for hemoglobin
TABLE 2. Cortical Oxygenation Under Steady-State Conditions of Moderate
Arterial Hypocapnia in Patients With AVM Before and After Resection and in
Control Patients Before and After Dissection of the Sylvian Fissure
Before Surgery
Mean, % SO2
After Surgery
AVM
(n⫽22)
Control
(n⫽30)
Total
(n⫽52)
AVM
(n⫽22)
Control
(n⫽30)
Total
(n⫽52)
54.8⫾10.4
52.7⫾9.1
53.6⫾9.7
73.1⫾10.1*
73.6⫾8.9*
73.4⫾9.4*
Measurements were performed under steady-state conditions of moderate hypocapnia (PaCO2,
33 mm Hg). SO2 values per patient were calculated and pooled according to groups and times and
are provided as mean⫾SD.
*Different from before surgery (P⬍0.05). There were no intergroup differences before and after
surgery.
Schaller et al
Cerebrovascular Reactivity Patterns and Cerebral AVMs
941
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Figure 2. Distributions of CVR patterns illustrated as ratios of parallel to inverse reactivity within the AVM and control groups before
(pre) and after (post) surgery analyzed separately for increasing and decreasing etCO2. Testing of vasodilatory capacity (increasing
etCO2) revealed that in a similar percentage of patients, CVR shows an inverse behavior in both groups before and after surgery. Ratio
of parallel to inverse patterns was uniformly reversed after surgery in both groups. Under vasoconstriction, preoperative CVR patterns
are also distributed similarly in both groups. The graph suggests, however, a difference in the postoperative situation in which a smaller
percentage of patients in the control group than in the AVM group exhibits inverse behavior. Although this difference did not reach statistical significance, it could suggest a somewhat-reduced global capacity for vasoconstriction after AVM resection.
and in control subjects but not significantly lower than for
postoperative control subjects.
Discussion
Our study provides evidence for similarly heterogenous CVR
patterns on supposedly normal frontal and temporal cortex in
patients with Ammon’s horn sclerosis and cortex in the
vicinity of cerebral AVM.
Methodology
One problem arises from the fact that CVR is traditionally
defined as changes in CBF to vasodilating or vasoconstricting
stimuli. The inability to measure CBF quantitatively with
sufficient temporal and spatial resolution in a clinical setting
has resulted in the use of substitutes such as blood flow
velocity3,8 or HbO2 with nearly infrared spectroscopy
(NIRS).10,11 We have adopted the latter approach because
Smielewski et al10,11 have shown that HbO2 changes after
induced alterations in CO2 allow valid assessment of CVR.
This algorithm is based on the assumption that SO2 changes
under constant conditions of O2 consumption reflect changes
in regional cerebral blood volume, which are linearly correlated with rCBF changes. This linearity is eventually violated
under ischemic conditions,15 which was ruled out in our
patients by the rSO2 measurements under steady-state hypocapnia. Our apparatus differs from NIRS systems with respect
to the catchment volume. Unlike NIRS, ours measures SO2 in
smaller supply units, which explains some counterintuitive
results in our control group (see below).
The second concern is whether our control patients were
normal with regard to cerebrovascular status. We thought the
best approach to control for potential confounders was to
select a homogeneous cohort of patients with isolated Ammon’s horn sclerosis. They are best matched regarding age,
comorbidities, etc, to the AVM group and harbor a non–
space-occupying lesion remote from the measuring site.
Workup and operative procedures are standardized, enabling
us to isolate the influence of a uniform surgical trauma.
Patients with chronic seizures may have altered vasoreactivity because abnormalities in rCBF/metabolism and morphological capillary alterations in resected tissue may occur.16,17
These findings, however, are confined to the epileptogenic
focus. Highly sensitive MRI sequences, PET or single photon
emission CT, and EEG define those patients with structural,
metabolic, and electrophysiological abnormalities extending
into the lateral cortex, which will then undergo a temporal
lobe resection instead of selective AH. The assumption of
normality in our control subjects seems more reasonable than
in patients with unruptured aneurysms, which harbor a local
phenomenon of a mostly generalized vascular disorder.
With a primarily negative finding reported in this paper (no
proof of AVM-specific CVR patterns), the question remains
as to whether this lack of significant intergroup differences
indicates equivalence. For group sizes ⱖ20, a statistical
power of 80% was reached. This was not always the case in
subgroup comparisons of RIs for parallel and inverse behavior under different etCO2 curves. We are well aware that
statistical nonsignificance does not necessarily imply equivalence and therefore discuss suggestive but insignificant
findings below.
942
Stroke
April 2003
TABLE 3. Reactivity Indexes for Parallel and Inverse CVR Patterns as Calculated
From Local SO2 Changes After Alterations in etCO2 in the Cortex of Patients With
AVM and Control Patients With Ammon’s Horn Sclerosis Before and After Surgery
AVM
Before
(n⫽22)
AVM
After
(n⫽22)
Control
Before
(n⫽30)
Control
After
(n⫽30)
RI, %SO2/mm Hg
(etCO2 increase)
1.0⫾0.5
0.3⫾0.1*
0.9⫾0.6
0.8⫾0.6
RI, %SO2/mm Hg
(etCO2 decrease)
0.8⫾0.5
0.6⫾0.4
0.8⫾0.7
0.5⫾0.5
RI, %SO2/mm Hg
(etCO2 increase)
⫺0.6⫾0.5
⫺0.5⫾0.3
⫺1.0⫾0.4
⫺0.9⫾0.6
RI, %SO2/mm Hg
(etCO2 decrease)
⫺0.3⫾0.4
⫺0.7⫾0.5
⫺0.8⫾0.4
⫺0.8⫾0.6
Parallel CVR
Inverse CVR
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Reactivity tests were performed before and after surgery in both groups. RIs were derived from the
slopes of the regression lines of SO2 on etCO2. Positive values indicate parallel behavior of SO2 and
etCO2; negative values indicate inverse behavior. Values are mean⫾SD. Statistical tests (ANOVA,
P⬍0.05) were performed separately for inverse and parallel CVR patterns and for vasoconstriction
(etCO2 decrease) and vasodilatation (etCO2 increase).
*Different from AVM before and control before surgery (P⬍0.05).
CVR in AVM Patients and Control Subjects
Preoperative Situation
Results of CVR testing in AVM patients reported in the
literature are inconclusive. This may be explained by the
variety of methods applied and by arbitrary interpretations of
results. For example, in studies using transcranial Doppler,
one has to take into account which vessels were insonated. In
one study, the results were considered indicative of pathological vasoreactivity without clearly stating whether these
arteries were involved in AVM supply,3 whereas other
authors found evidence for intact CVR in nonfeeding arteries
with transcranial Doppler sonography8 or intraoperative
micro-Doppler.7
Other authors found impaired CVR and hyperresponsiveness
to vasodilative stimuli and thought that they were predictive of
the occurrence of postoperative hyperemic complications.1,2,6
The results of xenon CT studies after acetazolamide challenges
were found to indicate a compromised vascular reserve capacity
in up to one third of the regions.4,5 Arteriolar exhaustion
resulting from a shunt-induced, chronically reduced cerebral
perfusion pressure was thought to be the underlying cause.
In contrast, Young et al,9 applying intraoperative xenon CBF
measurements, described regional CVR intact in all AVM
cases.9 They could further demonstrate that arteriolar dilation
compensates for reduced cerebral perfusion pressure but never to
a maximum extent.18,19 In conjunction with the results of studies
showing intact pressure autoregulation in all cases,20 –22 we
thought it unlikely that the myogenic response to vasodilatation
or vasoconstriction is disturbed in an AVM-specific manner. To
test this hypothesis, we compared the distribution of parallel
versus inverse CVR patterns between AVM and control patients
and also tested whether the degree of vasoreactivity is different.
The fact that 40% (with increasing etCO2), respectively 17%
(with decreasing etCO2) of patients in the AVM group, showed
a propensity for inverse behavior after both stimuli could be
interpreted as being AVM specific.4,5 But a similar distribution
of CVR patterns in control subjects before surgery prohibits this
interpretation and contradicts the notion of uniqueness. The
identical degree of “responsiveness” to either stimulus underlines this point. To accept that CVR in AVM patients is normal,
one would have to be positive that the results in the control group
are representative of normal cerebrovascular behavior. This
poses a problem at first glance, because a ratio of 23% (with
increasing etCO2), respectively 18% (with decreasing etCO2) of
impaired CVR, appears counterintuitive for “healthy” patients.
One may still consider our control group as harboring some form
of vascular compromise, but we would rather propose a different
explanation.
This discussion resembles the one that has taken place with
regard to resting CBF and AVM. Here, a so-called patchy
hypoperfusion has been considered AVM specific23 until proved
otherwise20,24,25 and now is well explained by theories regarding
regulation of capillary circulation.26 Compared with other modalities, the spatial resolution of our methods is higher. Because
it measures erythrocytic capillary flow, the inverse CVR behavior corresponds to a predominantly plasmatic capillary flow26 in
the assessed area during a challenge. As such, it represents a
physiological rather than a pathophysiological phenomenon and
makes its interpretation as “disturbed” at least questionable. It is
probably better defined as a form of microvascular steal.
One result may be considered suggestive for being AVM
dependent: Despite occurring in an equal proportion in both groups,
the inverse response after a vasoconstrictive stimulus (the relative
increase in nutritive capillary flow at the measuring site with
decreasing CO2) seems to occur to a lesser degree in AVM patients
(Figure 3 and Table 3). Yet, more likely, it is a difference by chance
because, according to the data on parallel behavior to decreasing
CO2, this cannot be caused by a hyperresponsiveness for vasoconstriction in other areas surrounding AVM.
Postoperative Situation
After the treatment of AVM, the CVR findings in various
studies were interpreted as “impaired” vasoreactivity,2,4,6
Schaller et al
Cerebrovascular Reactivity Patterns and Cerebral AVMs
943
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
nisms— eg, metabolic coupling— override this stimulus to protect the brain from further CBF increases, it could rather be
regarded a physiologically intact global vasoregulatory response.
The capacity for vasoconstriction is altered to the same extent
after resection of AVM. In this study, 63.2% of patients showed
inverse behavior to decreasing CO2, which is higher than in
control subjects. Although not reaching significance, this result
implies that the cortex after AVM resection is affected by a
reduced vasoconstrictive response. It seems plausible that reactive hyperemia after the release of localized spatula pressure is
regionally better confined than after reversal of chronically
reduced cerebral perfusion pressure in AVM patients.
In conclusion, CVR patterns on supposedly normal frontal
and temporal cortexes in patients with Ammon’s horn sclerosis
and cortex in the vicinity of cerebral AVM before surgery are
similarly heterogeneous and include inverse behavior of SO2 to
changes in CO2 in approximately one third of the examined
patients. After surgery, inverse CVR patterns indicative of
microvascular steal increase significantly because of the presence of reactive hyperemia in both groups. Apart from postoperatively lowered reactivity under induced vasodilation in the
AVM group, no AVM-specific pathological CVR pattern could
be proved. Yet, after surgery, the reduced capacity for vasoconstriction seems to be better confined regionally in control
subjects than in AVM patients.
Acknowledgment
We thank Rudolf Auen and Michael Bothe, medical students, for
their help during intraoperative data acquisition.
References
Figure 3. RIs for parallel (top) and inverse (bottom) CVR patterns in the AVM vs control group before and after surgery with
increasing and decreasing etCO2 (see also Table 3). Degree of
vasoreactivity is thus illustrated. Values are given as means;
bars indicate SD. *Different (P⬍0.05) from AVM before surgery
and control group.
whereas others thought it to be “preserved.”7,9 The postoperative increase in oxygenation under steady-state conditions
confirms that AVM resection leads to reactive hyperemia and
tissue hyperoxia in the surrounding brain.20,25,27 Therefore, it
is not surprising that two thirds of patients showed an inverse
CVR pattern after an increase in CO2 in the AVM group. The
degree of responsiveness was lower after surgery, reaching
statistical significance for parallel behavior under induced
vasodilation in AVM patients but not compared with postoperative controls. Thus, distributions of CVR patterns and
degrees of responsiveness were almost identical to those of
the control group after surgery (Figure 3 and Table 3).
In control subjects, reactive hyperemia is present after spatula
release to the same extent (Table 2) after transient pressureinduced ischemia.28,29 If this reduced capacity for vasodilatation
was due to exhaustion of the myogenic response, it could be
labeled disturbed. If it occurs because intact feedback mecha-
1. Barnett GH, Little JR, Ebrahim ZY, Jones SC, Friel HT. Cerebral circulation during arteriovenous malformation operation. Neurosurgery. 1987;
20:836 – 842.
2. Batjer HH, Devous MD Sr, Meyer YJ, Purdy PD, Samson DS. Cerebrovascular hemodynamics in arteriovenous malformation complicated by
normal perfusion pressure breakthrough. Neurosurgery. 1988;22:503–509.
3. Diehl RR, Henkes H, Nahser HC, Kuhne D, Berlit P. Blood flow velocity and
vasomotor reactivity in patients with arteriovenous malformations: a transcranial Doppler study. Stroke. 1994;25:1574–1580.
4. Tarr RW, Johnson DW, Horton JA, Yonas H, Pentheny S, Durham S,
Jungreis CA, Hecht ST. Impaired cerebral vasoreactivity after embolization
of arteriovenous malformations: assessment with serial acetazolamide
challenge xenon CT. AJNR Am J Neuroradiol. 1991;12:417–423.
5. Tarr RW, Johnson DW, Rutigliano M, Hecht ST, Pentheny S, Jungreis CA,
Horton JA, Yonas H. Use of acetazolamide-challenge xenon CT in the
assessment of cerebral blood flow dynamics in patients with arteriovenous
malformations. AJNR Am J Neuroradiol. 1990;11:441–448.
6. Van Roost D, Schramm J. What factors are related to impairment of cerebrovascular reserve before and after arteriovenous malformation resection? A
cerebral blood flow study using xenon-enhanced computed tomography.
Neurosurgery. 2001;48:709–716.
7. Hassler W, Steinmetz H. Cerebral hemodynamics in angioma patients: an
intraoperative study. J Neurosurg. 1987;67:822–831.
8. De Salles AA, Manchola I. CO2 reactivity in arteriovenous malformations of
the brain: a transcranial Doppler ultrasound study. J Neurosurg. 1994;80:
624–30.
9. Young WL, Prohovnik I, Ornstein E, Ostapkovich N, Sisti MB, Solomon
RA, Stein BM. The effect of arteriovenous malformation resection on cerebrovascular reactivity to carbon dioxide. Neurosurgery. 1990;27:257–266.
10. Smielewski P, Czosnyka M, Pickard JD, Kirkpatrick P. Clinical evaluation of
near-infrared spectroscopy for testing cerebrovascular reactivity in patients
with carotid artery disease. Stroke. 1997;28:331–338.
11. Smielewski P, Kirkpatrick P, Minhas P, Pickard JD, Czosnyka M. Can
cerebrovascular reactivity be measured with near-infrared spectroscopy?
Stroke. 1995;26:2285–2292.
944
Stroke
April 2003
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
12. Frank KH, Kessler M, Appelbaum K, Dummler W. The Erlangen micro-light
guide spectrophotometer EMPHO I. Phys Med Biol. 1989;34:1883–1900.
13. Meyer B, Schultheiss R, Schramm J. Capillary oxygen saturation and tissue
oxygen pressure in the rat cortex at different stages of hypoxic hypoxia.
Neurol Res. 2000;22:721–726.
14. Nakase H, Sakaki T, Kempski O. A scanning technique to measure regional
cerebral blood flow and oxyhemoglobin level. Neurosurgery. 2001;48:
1335–1342.
15. Sakoh M, Rohl L, Gyldensted C, Gjedde A, Ostergaard L. Cerebral blood
flow and blood volume measured by magnetic resonance imaging bolus
tracking after acute stroke in pigs: comparison with [(15)O]H(2)O positron
emission tomography. Stroke. 2000;31:1958 –1964.
16. Weinand ME, Carter LP, el-Saadany WF, Sioutos PJ, Labiner DM, Oommen
KJ. Cerebral blood flow and temporal lobe epileptogenicity. J Neurosurg.
1997;86:226–232.
17. Cornford EM, Hyman S, Cornford ME, Landaw EM, Delgado-Escueta AV.
Interictal seizure resections show two configurations of endothelial Glut1
glucose transporter in the human blood-brain barrier. J Cereb Blood Flow
Metab. 1998;18:26–42.
18. Fogarty-Mack P, Pile-Spellman J, Hacein-Bey L, Ostapkovich N, Joshi S,
Vulliemoz Y, Young WL. Superselective intraarterial papaverine administration: effect on regional cerebral blood flow in patients with arteriovenous
malformations. J Neurosurg. 1996;85:395– 402.
19. Joshi S, Young WL, Pile-Spellman J, Fogarty-Mack P, Sciacca RR,
Hacein-Bey L, Duong H, Vulliemoz Y, Ostapkovich N, Jackson T. Intra-arterial nitrovasodilators do not increase cerebral blood flow in angiographically normal territories of arteriovenous malformation patients. Stroke.
1997;28:1115–1122.
20. Meyer B, Schaller C, Frenkel C, Ebeling B, Schramm J. Distributions of local
oxygen saturation and its response to changes of mean arterial blood pressure
21.
22.
23.
24.
25.
26.
27.
28.
29.
in the cerebral cortex adjacent to arteriovenous malformations. Stroke. 1999;
30:2623–2630.
Young WL, Kader A, Prohovnik I, Ornstein E, Fleischer LH, Ostapkovich N,
Jackson LD, Stein BM. Pressure autoregulation is intact after arteriovenous
malformation resection. Neurosurgery. 1993;32:491–496.
Young WL, Pile-Spellman J, Prohovnik I, Kader A, Stein BM. Evidence for
adaptive autoregulatory displacement in hypotensive cortical territories
adjacent to arteriovenous malformations: Columbia University AVM Study
Project. Neurosurgery. 1994;34:601–610.
Okabe T, Meyer JS, Okayasu H, Harper R, Rose J, Grossman RG, Centeno
R, Tachibana H, Lee YY. Xenon-enhanced CT CBF measurements in
cerebral AVM’s before and after excision: contribution to pathogenesis and
treatment. J Neurosurg. 1983;59:21–31.
Taylor CL, Selman WR, Ratcheson RA. Steal affecting the central nervous
system. Neurosurgery. 2002;50:679–688.
Young WL, Kader A, Ornstein E, Baker KZ, Ostapkovich N, Pile-Spellman
J, Fogarty-Mack P, Stein BM. Cerebral hyperemia after arteriovenous malformation resection is related to “breakthrough” complications but not to
feeding artery pressure: the Columbia University Arteriovenous Malformation Study Project. Neurosurgery. 1996;38:1085–1093.
Kuschinsky W, Paulson OB. Capillary circulation in the brain. Cerebrovasc
Brain Metab Rev. 1992;4:261–286.
Hoffman WE, Charbel FT, Edelman G, Ausman JI. Brain tissue gases and pH
during arteriovenous malformation resection. Neurosurgery. 1997;40:
294–300.
Andrews RJ, Bringas JR. A review of brain retraction and recommendations
for minimizing intraoperative brain injury. Neurosurgery. 1993;33:
1052–1063.
Yundt KD, Grubb RL, Jr, Diringer MN, Powers WJ. Cerebral hemodynamic
and metabolic changes caused by brain retraction after aneurysmal subarachnoid hemorrhage. Neurosurgery. 1997;40:442–450.
Patterns of Cortical Oxygen Saturation Changes During CO2 Reactivity Testing in the
Vicinity of Cerebral Arteriovenous Malformations
Carlo Schaller, Johannes Schramm, Dorothee Haun and Bernhard Meyer
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
Stroke. 2003;34:938-944; originally published online March 20, 2003;
doi: 10.1161/01.STR.0000060880.59712.14
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 2003 American Heart Association, Inc. All rights reserved.
Print ISSN: 0039-2499. Online ISSN: 1524-4628
The online version of this article, along with updated information and services, is located on the
World Wide Web at:
http://stroke.ahajournals.org/content/34/4/938
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published
in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office.
Once the online version of the published article for which permission is being requested is located, click
Request Permissions in the middle column of the Web page under Services. Further information about this
process is available in the Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Stroke is online at:
http://stroke.ahajournals.org//subscriptions/