(Stroke. 1999;30:2623.)
© 1999 American Heart Association, Inc.
Original Contributions |
Distributions of Local Oxygen Saturation and Its Response to Changes of Mean Arterial Blood Pressure in the Cerebral Cortex Adjacent to Arteriovenous Malformations
Presented in part at the Proceedings of the Second Conference on Cerebral Oxygenation held in Würzburg, Germany, September 1997, and published in abstract form in Neurological Research 1998;20(suppl 1).
From the Departments of Neurosurgery (B.M., C.S., J.S.) and Anesthesiology (C.F., B.E.), University of Bonn (Germany).
Correspondence to Bernhard Meyer, MD, Department of Neurosurgery, University of Bonn, Sigmund Freud Str 25, 53127 Bonn, Germany. E-mail bmey{at}mailer.meb.uni-bonn.de
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Abstract |
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Background and Purpose—To test the hypothesis that neither "steal" as cortical ischemia caused by reduced perfusion pressure nor "breakthrough" on the grounds of loss of pressure autoregulation exist in brain tissue surrounding arteriovenous malformations (AVMs), we established patterns of cortical oxygen saturation (SO2) adjacent to AVMs and its behavior after alterations of mean arterial blood pressure.
Methods—With a microspectrophotometer, SO2 was scanned in the cortex around AVMs of 44 patients before and after resection and in that of a non-AVM group (n=42) before transsylvian dissection. Autoregulation was evaluated by linear regression analysis after elevation of mean arterial blood pressure (5 µg/min IV noradrenaline). SO2 values were calculated as medians, percentage of critical values (<25% SO2), and coefficients of variance (approximate heterogeneity of SO2 distributions). All values are given as mean±SD.
Results—Forty patients with AVM had an uneventful postoperative course (group A). Four hyperemic complications ("breakthrough") occurred (group B). Autoregulation was tested intact in all groups at all times. Preoperative SO2 distributions in groups A and C (non-AVMs) were identical. In group B, significantly (P<0.05) lower medians (group A, 52.9±16.3%; group B, 44.2±17.1%; group C, 51.9±11.5% SO2), more critical values (group A, 6.5±5.1%; group B, 14.7±11.1%; group C, 7.1±4.9%), and heterogeneous SO2 distributions (group A, 20.2±12.7%; group B, 27.9±12.4%; group C, 26.8±10.9%) were seen. Increase of median values was significantly higher in group B (76.3±10.4% SO2) than in group A (65.9±13.4% SO2) after resection.
Conclusions—Severely hypoxic areas are uncommon in the cortex adjacent to AVMs and occur predominantly in patients prone to hyperemic complications. Reduced perfusion pressure is compensated in most cases, and moderate hyperemia prevails after excision. Reperfusion into unprotected capillaries of severely hypoxic cortical areas results in "breakthrough," for which vasoparalysis appears not to be the underlying mechanism.
Key Words: autoregulation • cerebral arteriovenous malformations • cerebrovascular circulation • oxygen
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Introduction |
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It has long been described in a qualitative manner that cerebral arteriovenous malformations (AVMs) induce alterations of cerebral blood flow in the surrounding brain tissue and that these alterations are closely related to pathophysiological events occurring after the exclusion of AVMs from the cerebral circulation,1 some of which still have disastrous consequences for a considerable percentage of patients.2 It seemed plausible that AVMs generate an ischemic environment in the surrounding cortex and that their exclusion causes a hyperemic response.3 Certain labels were attributed to these situations such as preoperative "steal" and postoperative "breakthrough" in the case of edema formation or hemorrhage.1 4
A theory was formulated in 1978 derived from clinical observations and animal experiments (Normal Perfusion Pressure Breakthrough Theory, NPPB).4 It was postulated that AVMs cause a reduction of cerebral perfusion pressure (CPP), which induces a maximum reduction of cerebrovascular resistance (CVR) in the surrounding brain tissue to the point where ischemia occurs and cerebral pressure autoregulation is lost. Closure of the arteriovenous shunt system then normalizes perfusion pressure, but autoregulatory capacity is not restored in certain cases, which is the underlying mechanism for a "breakthrough."
The problem for nearly the next 2 decades was that none of these phenomena could be pinpointed without reasonable doubt in patients. Neither "steal" nor "hyperemia" could be reliably quantified in most studies. Ambiguous results obtained after testing of CO2 reactivity were subject to controversial interpretations, and assumptions were made on pressure autoregulation, which was never tested itself. Some misconceptions arose from the neglect of the heterogeneity of cerebral blood flow under physiological conditions and/or the use of methods with insufficient resolution.5 6 7 8 Furthermore, results obtained by measurements of "shunt flow" (within the AVM system) were used to deduce assumptions on "perfusion flow" (within the surrounding tissue).9 10
In some recent studies, however, solid evidence for several aspects of AVM pathophysiology was presented. It was demonstrated that the AVM-induced reduction of CPP11 12 13 did not cause a maximum reduction of CVR in the adjacent cortex of patients with AVM because further arteriolar relaxation was possible in every case. Preoperative CBF levels in patients with AVM were seemingly not lower than in control patients.13 14 Pressure autoregulation-tested for the first time-appeared to be intact before and after resection of AVMs.15 16 These results called into question the classic concepts of "steal" in the sense of cortical ischemia as a consequence of reduced CPP and "breakthrough" on the grounds of loss of pressure autoregulation. It was concluded that if these phenomena occur, the pathophysiological mechanism responsible is obviously not at the arteriolar level and probably multifactorial.13 14 15 Doubts regarding their results and conclusions were expressed by the same authors because of the insufficient temporal and spatial resolution of the method used, which did not allow insights into the microenvironment of the surrounding cortex. Their findings with regard to intact pressure autoregulation so far have not been corroborated in general and in the event of a "breakthrough" in particular.
We therefore initiated a systematic intraoperative study on patients with AVM by using a technique that quantifies cortical capillary oxygen saturation (SO2) with high temporal and spatial resolution. Our aims were primarily to establish patterns of oxygen supply in cortical microcirculatory units adjacent to AVMs before and after their resection and behavior of SO2 after induced alterations of systemic blood pressure. Because cerebral oxygen metabolism was assumed to be constant during the experiments, changes in SO2 were interpreted to reflect primarily changes of regional CBF.
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Subjects and Methods |
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This study was approved by the local ethics review committee. Written consent was obtained from all patients for the experiments at least 24 hours before the operation.
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
1989.17 It was designed for fast, diffuse remission
spectrophotometry by flexible microlight guides in small tissue volumes
of moving organs in situ. Light in the visible domain illuminates
tissue by means of the illuminating fiber, and backscattered light is
transmitted by 6 detecting fibers (Ø 70 µm)-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 thus transmitted to a photomultiplier, an
AD-converter, and finally to a computer, in which 1
SO2 value per spectrum is calculated
by algorithms described elsewhere.17 18 The obtained
SO2 values reliably indicate oxygen
transport to tissue19 and indirectly nutritive capillary
flow20 (see Discussion). The high temporal (100 spectra/s)
and spatial (75x250 µm) resolution permits an easy scanning
procedure of superficial cortical capillaries by moving the light guide
above the brain surface.21
Study Groups and Protocol
Forty-four patients (19 female patients, 25 male patients, mean
age 32 years, range 5 to 66 years) harboring cerebral AVMs of
Spetzler/Martin22 grades I (n=4), II (n=19), III (n=15),
and IV (n=6) were included in the study. All underwent elective
microsurgery for complete resection of the malformations.
SO2 distributions were measured by
scanning an average of 5 small (
5 mm2)
areas (300 to 500 SO2 values per
area and measurement) of the exposed cortex surrounding the AVM before
and after the resection at distances 2 to 4 cm from the nidus
(approximate resection margin). All areas were numbered and
photographically documented under the highest magnification of the
operating microscope for exact postoperative relocation. Areas in which
surgical trauma was suspected by microscopic inspection or otherwise
(eg, to close to resection margin) were excluded from postoperative
measurements.
Preoperative and postoperative behavior of cortical
SO2 after alterations of mean
arterial blood pressure (MABP) was established by
simultaneous, continuous monitoring of MABP (radial artery)
and SO2 (in identical cortical areas
before and after surgery). MABP was elevated 40% above baseline
(30 mm Hg) by continuous intravenous infusion of 5
µg/min noradrenaline. Under the assumption that
alterations of SO2 depend
predominantly on alterations of flow, the observed behavior was
considered a measure of cerebral pressure autoregulation. Nineteen
patients in the AVM group gave their consent to undergo the test.
Forty-two patients (24 female patients, 18 male patients, mean age 36 years, range 14 to 72 years) underwent transsylvian microsurgery for deep-seated nonvascular lesions. Deep-seated lesions were selected to obtain baseline values of SO2 distributions in normal frontal and temporal cortex uncompromised by any space-occupying process. This group was matched to the AVM group with respect to ASA classification. SO2 distributions (n=42) and pressure autoregulation (n=20) were established with the protocol described above before the start of the transsylvian dissection.
For all operations, total intravenous anesthesia was induced with 1.5 mg/kg propofol (maintained with 5 to 10 mg/kg per hour), 15 µg/kg alfentanil (maintained with 0.1 to 0.2 mg/kg per hour), and 0.1 mg/kg vecuronium (maintained with 30 to 60 µg/kg per hour) under inhalation of 40% O2 and 60% N2. MABP and heart rate were monitored continuously with a radial artery line. Arterial blood samples (PaO2, PaCO2, pH) and venous blood samples (hematocrit) were taken at times of SO2 measurements.
Data Analysis
SO2 values were pooled
according to groups and times of measurements and displayed as
frequency histograms. They were calculated as medians [%
SO2] and ratios of critical values
[%] defined as percentage of SO2
values <25% SO2, which
approximately corresponds to a cerebral venous
PO2 of 12 mm Hg. Coefficients
of variance [%] (SD/meanx100%) were calculated to approximate
heterogeneity of SO2
distributions depending (under conditions of constant
arterial oxygen supply and consumption) primarily on
erythrocytic capillary flow. Coefficients of variance (CV) were thus
interpreted as a the numerical expression of
heterogeneity of nutritive capillary flow velocities as
described elsewhere.23 24
ANOVA, Wilcoxon (dependent, nonparametric variables), and Kolmogorov-Smirov (independent, cumulative variables) tests were used for statistical analysis, with a level of significance set at P<0.05. All values are given as mean±SD.
Adopting an algorithm described previously (ie, Reference 2525 ), pressure autoregulation was evaluated by linear regression analysis of SO2 on MABP, with MABP used as the independent variable. Time intervals with continuous rise of MABP from baseline to peak level were used for calculations. Two criteria were applied to define intact autoregulation (ie, absence of vasoparalysis): (1) the calculated regression slope was not greater than the critical slope of 0.4% SO2/mm Hg. The value of 0.4% SO2/mm Hg was selected after evaluation of "normative" autoregulatory data in patients without AVM (mean slope±2 SD). (2) Regressions not reaching statistical significance (P<0.05) were classified as intact pressure autoregulation.
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Results |
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Patients with AVM were subdivided according to their postoperative clinical course into group A (n=40) if uneventful or group B (n=4) if breakthrough (in the following referred to as hyperemic complication) occurred. Hyperemic complications were defined as clinical deteriorations caused by the occurrence of otherwise unexplainable postoperative edema and/or hemorrhage on computed tomography scans. Incomplete AVM resection or other causes were ruled out on postoperative angiograms. Definition of hyperemic complications was performed according to clinical and radiological criteria by the senior author (J.S.) and neuroradiologists, both blinded to SO2 data. Patients without AVM constituted group C.
Physiological variables showed no significant
differences among groups and times of measurements for blood gases and
hematocrit. Only MABP values in group A before resection were
significantly lower (Table 1
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Comparison of pooled data as histograms and calculated
parameters of cortical capillary
SO2 showed no significant difference
in median values and ratio of critical values between patients with AVM
without postoperative hyperemic complications (group A: median
52.9±16.3% SO2, ratio of critical
values 6.5±16.3%) and control subjects (group C: median 51.9±11.5%
SO2, ratio of critical values
7.1±9.9%). Only an insignificant increase of very low
SO2 values in group A was noticed.
Significantly less heterogeneous
SO2 distribution in group A (CV
20.2±12.7%) than in group C (CV 26.8±10.9%) was observed. Median
SO2 values (44.2±17.1%
SO2) in patients with AVM with
postoperative hyperemic complications (group B) were
significantly lower and the ratio of critical values (14.7±30.1%)
significantly higher than in groups A and C.
SO2 distributions in group B (CV
27.9±22.4%) were more heterogeneous than in group A
(Table 2 and Figure 1).
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Detailed analysis of SO2 distribution in group B revealed median values as low as 20% SO2, a ratio of critical values as high as 60%, and CVs up to 70% in individual areas. Nongaussian distributions prevailed in single areas of group B as opposed to groups A and C. Gaussian SO2 distributions were predominant in individual areas of the latter groups, and calculated SO2 parameters were preferentially similar to the pooled data.
A significant shift to the right of the distributions (toward higher
SO2 values) in the frequency
histograms of groups A and B was observed after the resection of the
AVMs. Pooled group data correspondingly revealed a significant decrease
of the ratio of critical values (group A 0.8±4.4%, group B
0.7±2.7%) and of CV (group A 11.5±6.6%, group B 11.1±8.3%).
However, the increase of median SO2
in patients with AVM with hyperemic complications (group B
76.3±10.4% SO2) was significantly
higher than in patients with an uneventful postoperative course (group
A 65.9±13.4% SO2) (Table 2
and Figure 2).
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Detailed analysis of the SO2 distributions in group B after the resection of the AVMs showed the highest SO2 levels, preferentially within those areas with the lowest preoperative oxygen supply.
During the tests of pressure autoregulation in the control group (group
C), 18 of 20 linear regressions reached statistical significance
(P<0.05). Mean elevation of MABP above baseline was
+42±16%, with an average velocity of induced blood pressure change of
+0.20±0.09 mm Hg/s. Mean slope of all significant regressions
was +0.02±0.18% SO2/mm Hg
(range +0.26% to 0.40%
SO2/mm Hg) (Table 3 and Figure 3).
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In the AVM group a total of 19 pressure autoregulation tests were
performed (group B: n=3, group A: n=16) before the resection and 18
(group B: n=3, group A: n=15) after the resection of the AVMs. The
cortical area in 1 patient of group A, in which the
SO2 had been continuously monitored
during the induced MABP changes, was excluded from the postoperative
measurements for suspected surgical trauma. All preoperative and
postoperative regressions in group B reached statistical significance
(P<0.05) as well as 15 preoperative and 13 postoperative
regressions in group A. Mean elevation of MABP above baseline in the
AVM group before excision was +39±13%, with an average velocity of
induced blood pressure change of +0.14±0.07 mm Hg/s (+37±12%,
respectively, +0.13±0.08 mm Hg/s after excision). Mean slope of
all significant regression lines was +0.02±0.20%
SO2/mm Hg (range +0.32% to
0.41% SO2/mm Hg) before
surgery and +0.02±0.17%
SO2/mm Hg (range +0.28 to
0.37% SO2/mm Hg) after
surgery. None of the slopes exceeded the critical slope of +0.4%
SO2/mm Hg. Thus autoregulation
was considered intact in all patients tested in the AVM group before
and after the resection of the malformations regardless of the
occurrence of hyperemic complications (Table 3 and
Figure 3).
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Discussion |
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Methodology
The potential drawback of the microspectrophotometric technique (ie, the EMPHO II) applied in this study, has been discussed previously.20 It lies in the lack of an exact validation for brain tissue, through which assumptions in the algorithm might eventually be violated. This is, however, only of interest with respect to exact assessment of truly absolute SO2 values in the brain. The absolute data gathered by the EMPHO II are identical to those obtained by other systems used for intravital microreflectometry under comparable conditions.26 This shows that even the error for absolute readings of cortical SO2 is probably minor.
Moreover, it has now been demonstrated reliably that the obtained SO2 values reflect tissue oxygenation very accurately because simultaneous recordings of SO2 with the EMPHO II and tissue oxygen partial pressure (PtO2) with multiwire surface electrodes have shown an excellent correlation over a wide range (20% to 80% SO2) of arterial oxygenation levels.19 Under constant arterial oxygen supply and oxygen consumption, the SO2 readings obtained by this technique reflect changes of nutritive capillary flow with a very high sensitivity, as evidenced by simultaneous measurements of SO2 (EMPHO II) and CBF (laser Doppler flowmetry).20 Furthermore, it could be demonstrated under conditions of hypoxic or anemic hypoxia26 as well as ischemia20 that capillary saturation levels may fall below venous SO2, a situation similar to the one observed in group B. Although exact validation of very low SO2 values does not exist, we consider it therefore a true assumption that such a configuration of SO2 distributions indicates severe tissue hypoxia or ischemia.
For these reasons, we thought this technique to be ideal for the questions to be answered in this study, that is, the supply situation in microcirculatory units of the cortex surrounding cerebral AVMs. Besides its sufficient spatial resolution, the apparatus permits an easy and fast scanning procedure in a "no-touch" technique because of its high temporal resolution.
Another methodological problem to be discussed is the evaluation of pressure autoregulation. We consider it a valid assumption that the behavior of SO2 after alterations of MABP under constant conditions is almost exclusively a function of local CBF.20 21 This has also been shown in recent studies, which measured cerebrovascular reactivity reliably by means of near-infrared spectroscopy (eg, see Reference 2727 ), although the relation of SO2 and CBF is theoretically nonlinear.28 This is consistent with the trend to use estimates such as CBF velocity for dynamic testing of cerebral autoregulation.25 29 30
In our opinion, the problem lies within the algorithm and even more the definition of pressure autoregulation. Although we performed a dynamic measurement as opposed to static testing,31 which has also been applied in the aforementioned AVM studies,15 16 linear regression analysis allows only for definition of intact versus lost autoregulation by an arbitrary cutoff line. The problem that no "gold standard for quantification of autoregulation" exists has been acknowledged in all previous publications.25 Very recently developed, more complex algorithms will probably enhance sensitivity29 30 32 and allow for a better quantification and grading of cerebral pressure autoregulation.32 Yet even with the application of these algorithms, the decision that calculated value indicates an disturbance remains arbitrary. We think that our method enabled us to achieve our primary goal, that is, to rule out major disturbances of autoregulation such as complete vasoparalysis, postulated to be the underlying mechanism of "breakthrough." This assumption is corroborated by the fact that the patterns of SO2 behavior after induced alterations of MABP within the brain tissue surrounding AVMs are strikingly similar to those measured in normal cortex.
Preoperative Steal Syndrome
In contrast to previous studies,7 we have shown that
the proven reduction of CPP in brain-nutrifying branches of
arterial feeding arteries does not cause lowered tissue
oxygenation in the vast majority of patients with AVMs.
This is in accordance with recent publications14 giving no
evidence for "cerebral hypoperfusion" in patients with AVM. The
distributions of oxygen supply and thus nutritive capillary flow to the
cortex surrounding AVMs is almost identical to that in normal cortex.
The previously observed "patchy hypoperfusion" in brain tissue
surrounding these malformations5 6 7 may therefore
correspond overwhelmingly to the "natural"
heterogeneity of CBF and is not evidence for steal.
Even in unaffected human cortex, 7% of the areas have capillary
oxygen saturation levels <25% SO2
(ie, below the so-called "lethal threshold" for cerebral venous
PO2 of 12 mm Hg), a fact
already appreciated previously (eg, see Reference 2121 ). This per se does
not indicate tissue hypoxia and is now well explained by recent
theories regarding regulation of capillary circulation in the brain,
according to which plasmatic capillary flow prevails in this local
areas. For further discussion of this phenomenon, we refer to the
literature.23 24 26 33 34
Compensating mechanisms, therefore, must counteract the reduced perfusion pressure. Arteriolar dilatation has been proven to be one of them but seemingly never to the extent of a maximum CVR reduction.12 By having shown that SO2 in the cortex adjacent to AVM never follows alterations of MABP passively, we were able to corroborate these findings. We thus reproduced the results of Young et al,16 demonstrating that chronic hypotension does not result in "vasomotor paralysis" regardless of whether or not a hyperemic complication subsequently occurs. Their hypothesis of an adaptive autoregulatory displacement (ie, a shift of the autoregulatory curve to the left) seems correct.
An increased capillary density as a structural mechanism of adaption has recently been appreciated.35 A third mechanism to compensate for a low CPP is a reduced glucose and oxygen metabolism without increased oxygen extraction in the perilesional brain tissue, which has been found in studies with either positron emission tomography36 37 or PtO2 electrodes.38 Accordingly, our results did not point to a higher than normal oxygen consumption. A fourth mechanism speculated by Hoffman et al38 and us lies at the level of capillary regulation itself. Because of the less heterogeneous SO2 distribution in group A of patients with AVM in contrast to those without AVM, we also hypothesize that erythrocytic capillary recruitment as defined by Kuschinsky and Paulson33 plays an independent role. Very few scattered hypoxic areas around AVMs not prone to postoperative hyperemic complications might trigger this mechanism, as known from animal experiments.39 40
We therefore agree with Mast et al41 that steal should not be defined as cortical ischemia as a consequence of arterial hypotension. Frequent clinical steal phenomena such as progressive focal neurological deficits or impairment of higher cognitive functions are rather a consequence of neuronal deafferentation and diaschitic phenomena in distant or even contralateral regions of the brain.36 37 41
However, severely hypoxic situations in the cortex adjacent to AVMs exist. They are very rare and predominantly encountered in patients prone to postoperative hyperemic complications. We were able to substantiate the existence of such local areas with SO2 patterns resembling that of "low-flow anoxia" in all patients with a breakthrough, consistent with a previous report.42 Because we could not demonstrate vasoparalysis in these patients, exhausted arteriolar regulation is most probably not the single underlying mechanism that leads to drastically reduced oxygen supply in those cortical areas. This is in agreement with other authors12 13 14 15 36 37 who argue that persistent hemodynamic effects are not primarily responsible. It remains speculative as to which of the above-mentioned other compensating mechanisms are disturbed,13 leading to local supply situations indicative for morphological damage.
Postoperative Breakthrough
Immediately after the resection of AVMs, a significant increase in
cortical capillary SO2 (ie, a shift
of the distributions to the right) takes place in virtually all
patients. This can certainly be regarded as flow-related because a
hyperemic environment in the surrounding brain tissue-as
opposed to the formerly postulated "normalization" of CBF-has
already been demonstrated.14 The observed patterns in
cortical areas of patients without breakthrough correspond to that of
reactive hyperemia in the sense that supply exceeds demand. We
encountered the highest postoperative
SO2 values in patients with
subsequent neurological deteriorations caused by brain swelling and
hemorrhage. The same observation was communicated by Young et
al.14 In further accordance with the results of this
group,15 we could not find evidence for abolished pressure
autoregulation regardless of the occurrence of breakthrough
complications.
We conclude that normalized perfusion pressure after AVM resection leads to moderate reactive hyperemia in all patients with uneventful postoperative course because intact feedback mechanisms beyond the myogenic response (ie, metabolic feedback) limit the reperfusion. Because the highest increase in capillary oxygen saturation values measured in the surrounding cortex immediately after resection takes place in cortical areas with evidence for a prior state of severe hypoxia, we confirm the notion of Spetzler et al4 that "breakthrough of normal perfusion pressure occurs in an ischemic cortex." However, vasomotor paralysis is not responsible for this phenomenon. It is much more likely that uncoupling of CBF and metabolism has taken place in those local areas. As a consequence of the lacking metabolic feedback, insufficiently limited hyperperfusion results in a reperfusion injury as described for various other ischemic conditions of the brain. In contrast to Hoffman et al,38 who assume that capillary recruitment itself renders the capillary bed vulnerable to normalized perfusion pressure, we are therefore convinced that obviously the lack of recruitment in these areas promotes breakthrough. Structural deficiencies of the capillaries that occur in the process of neovascularization have been observed in an animal model for AVMs and may contribute to the breakdown of the blood-brain barrier.35
All in all, we think that the underlying mechanism for the occurrence of brain swelling and hemorrhage after AVM resection is not as unique to this disease, as it might be inferred from the NPPB theory.
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Acknowledgments |
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The authors sincerely thank Horst Urbach, MD, Neuroradiologist, Department of Radiology, University of Bonn, for his assistance in interpretation of angiograms and Thomas Gampe and Stefan Hirschelmann, medical students, for meticulous collection of data.
Received January 15, 1999; revision received September 17, 1999; accepted September 17, 1999.
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References |
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1. Feindel W, Yamamoto YL, Hodge CP. Red cerebral veins and the cerebral steal syndrome. J Neurosurg. 1971;35:167–179.[Medline] [Order article via Infotrieve]
2. Morgan MK, Johnston IH, Hallinan JM, Weber NC. Complications of surgery for arteriovenous malformations of the brain. J Neurosurg. 1993;78:176–182.[Medline] [Order article via Infotrieve]
3. Mullan S, Brown FB, Patronas NJ. Hyperemic and ischemic problems of surgical treatment of arteriovenous malformations. J Neurosurg. 1979;51:757–764.[Medline] [Order article via Infotrieve]
4. Spetzler RF, Wilson CB, Weinstein P, Mehdorn M, Townsend J, Telles D. Normal perfusion pressure breakthrough theory. Clin Neurosurg. 1978;25:651–672.[Medline] [Order article via Infotrieve]
5. Marks MP, O’Donahue J, Fabricant JI, Frankel KA, Phillips MH, DeLaPaz RL, Enzmann DR. Cerebral blood flow evaluation of arteriovenous malformations with stable xenon CT. AJNR Am J Neuroradiol. 1988;9:1169–1175.[Abstract]
6. Batjer HH, Devous, Seibert GB Purdy PD, Ajmani AK, Delarosa M, Bonte FJ. Intracranial arteriovenous malformation: relationships between clinical and radiographic factors and ipsilateral steal severity. Neurosurgery. 1988;23:322–328.[Medline] [Order article via Infotrieve]
7. Okabe T, Meyer JS, Okayasu H, Harper R, Rose J, Grossmann RG, Centeno R, Tachibana H, Lee YY. Xenon-enhanced CT CBF measurements in cerebral AVMs before and after excision. J Neurosurg. 1983;59:21–31.[Medline] [Order article via Infotrieve]
8. Hassler W, Steinmetz H. Cerebral hemodynamics in angioma patients: an intraoperative study. J Neurosurg. 1987;67:822–831.[Medline] [Order article via Infotrieve]
9. Marks MP, Lane B, Steinberg G, Chang P. Vascular characteristics of intracerebral arteriovenous malformations in patients with clinical steal. AJNR Am J Neuroradiol. 1991;12:489–496.[Abstract]
10. Al-Rodhan NRF, Sundt TM, Piepgras DG, Nichols DA, Rüfenacht D, Stevens LNR. Occlusive hyperemia: a theory for the hemodynamic complications following resection of intracerebral arteriovenous malformations. J Neurosurg. 1993;78:167–175.[Medline] [Order article via Infotrieve]
11. Fogarty-Mack P, Pile-Spellman J, Hacein-Bey L, Osipov A, DeMeritt J, Jackson EC, Young WL. The effect of arteriovenous malformations on the distribution of intracerebral arterial pressures. AJNR Am J Neuroradiol. 1996;17:1443–1449.[Abstract]
12. 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.[Medline] [Order article via Infotrieve]
13.
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.
14. 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. Neurosurgery. 1996;38:1085–1095.[Medline] [Order article via Infotrieve]
15. Young WL, Kader A, Prohovnik I, Ornstein E, Fleischer LH, Ostapkovich N, Jackson LS, Stein BM. Pressure autoregulation is intact after arteriovenous malformation resection. Neurosurgery. 1993;32:491–497.[Medline] [Order article via Infotrieve]
16. Young WL, Pile-Spellman J, Prohovnik I, Kader A, Stein BM. Evidence for adaptive autoregulatory displacement in hypotensive cortical territories adjacent to arteriovenous malformations. Neurosurgery. 1994;34:601–611.[Medline] [Order article via Infotrieve]
17. Frank KH, Kessler M, Appelbaum K, Dümmler W. The Erlangen micro-lightguide spectrophotometer EMPHO I. Phys Med Biol. 1989;34:1883–1900.[Medline] [Order article via Infotrieve]
18. Kubelka P, Munk F. Ein Beitrag zur Optik der Farbanstriche. Z Technische Physik. 1931;11:76–77.
19.
Hasibeder W, Germann R, Sparr H, Haisacki M,
Friesenecker B, Luz G, Pernthaler H, Pfaller K, Maurer H, Ennemoser O.
Vasomotion induces regular major oscillations in jejunal
mucosal tissue oxygenation. Am J
Physiol. 1994;266:G978–G985.
20.
Nakase H, Heimann A, Kempski O. Alterations of regional
cerebral blood flow and oxygen saturation in a rat sinus-vein
thrombosis model. Stroke. 1996;27:720–728.
21. Höper J, Gaab MR. Effect of arterial PaCO2 on local HbO2 and relative Hb concentration in the human brain: a study with the Erlangen micro-lightguide spectrophotometer (EMPHO). Physiol Meas. 1994;15:107–113.[Medline] [Order article via Infotrieve]
22. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–483.[Medline] [Order article via Infotrieve]
23. Vogel J, Kuschinsky W. Decreased heterogeneity of capillary plasma flow in the rat whisker-barrel cortex during functional hyperemia. J Cereb Blood Flow Metab. 1996;16:1300–1306.[Medline] [Order article via Infotrieve]
24.
Villringer A, Them A, Lindauer U, Einhäupl K,
Dirnagl U. Capillary perfusion of the rat brain cortex: an in vivo
confocal microscopy study. Circ Res. 1994;75:55–62.
25.
Panerai RB, Kelsall WR, Rennie JM. Evans DH: Cerebral
autoregulation dynamics in premature newborns. Stroke.. 1995;26:74–80.
26. Watanabe M, Harada N, Kosaka H, Shiga T. Intravital microreflectometry of individual pial vessels and capillary region of rat. J Cereb Blood Flow Metab. 1994;14:75–84.[Medline] [Order article via Infotrieve]
27.
Smielewski P, Kirkpatrick P, Minhas P, Pickard JD,
Czosnyka M. Can cerebrovascular reactivity be measured with
near-infrared spectroscopy? Stroke.. 1995;26:2285–2292.
28.
Kaminogo M, Ichikura A, Shibata S, Toba T, Yonekura M.
Effect of acetazolamide on regional cerebral oxygen
saturation and regional cerebral blood flow. Stroke. 1995;26:2358–2360.
29. Larsen FS, Olsen KS, Hansen BA, Paulson OB, Knudsen GM. Transcranial doppler is valid for determination of the lower limit of cerebral blood flow autoregulation. Stroke. 1994;25:1985–1988.[Abstract]
30. Newell DW, Aaslid R, Lam A, Mayberg TS, Winn R. Comparison of flow and velocity during dynamic autoregulation testing in humans. Stroke. 1994;25:793–797.[Abstract]
31. Paulson OB, Strandgaard S, Edvinsson L. Cerebral autoregulation. Cerebrovasc Brain Metabol Rev. 1990;2:161–192.[Medline] [Order article via Infotrieve]
32.
Panerai RB, White RP, Markus HS, Evans DH. Grading of
cerebral dynamic autoregulation from spontaneous fluctuations in
arterial blood pressure. Stroke. 1998;29:2341–2346.
33. Kuschinksy W, Paulson OB. Capillary circulation in the brain. Cerebrovasc Brain Metabol Rev. 1992;4:261–286.[Medline] [Order article via Infotrieve]
34.
Theilen H, Schröck H, Kuschinsky W. Capillary
perfusion during incomplete forebrain ischemia and reperfusion
in rat brain. Am J Physiol. 1993;265:H642–H648.
35. Sekhon LHS, Morgan MK, Spence I. Normal perfusion pressure breakthrough: the role of capillaries. J Neurosurg. 1997;86:519–524.[Medline] [Order article via Infotrieve]
36.
Fink GR. Effects of cerebral angiomas on perifocal and
remote tissue: a multivariate positron emission
tomography study. Stroke. 1992;23:1099–1105.
37.
Tyler JL, Leblanc R, Meyer E, Dagher A, Yamamoto YL,
Diksic M, Hakim A. Hemodynamic and
metabolic effects of cerebral arteriovenous malformations
studied by positron emission tomography. Stroke. 1989;20:890–898.
38. Hoffman WE, Charbel FT, Edelman G, Abood C. Brain tissue response to CO2 in patients with arteriovenous malformation. J Cereb Blood Flow Metab. 1996;16:1383–1386.[Medline] [Order article via Infotrieve]
39. Kozniewska E, Weller L, Höper J, Harrison DK, Kessler M. Cerebrocortical microcirculation in different stages of hypoxic hypoxia. J Cereb Blood Flow Metab. 1987;7:464–470.[Medline] [Order article via Infotrieve]
40. Bereczki D, Wei L, Otsuka T, Acuff V, Pettigrew K, Patlak C, Fenstermacher J. Hypoxia increases velocity of blood flow through parenchymal microvascular systems in rat brain. J Cereb Blood Flow Metab. 1993;13:475–486.[Medline] [Order article via Infotrieve]
41.
Mast H, Mohr JP, Osipov A, Pile-Spellman J, Marshall
RS, Lazar RM, Stein BM, Young WL. "Steal" is an
unestablished mechanism for the clinical presentation of
cerebral arteriovenous malformations. Stroke. 1995;26:1215–1220.
42. Barnett GH, Little JR, Ebrahi ZV, Jones SC, Friel HT. Cerebral circulation during arteriovenous malformation operation. Neurosurgery. 1987;20:836–842.[Medline] [Order article via Infotrieve]
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