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Ovid: Cerebral Hyperemia after Arteriovenous Malformation Resection Is Related to"Breakthrough" Complications but Not to Feeding Artery Pressure.

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Cerebral Hyperemia after Arteriovenous Malformation Resection Is Related to“Breakthrough” Complications but Not to Feeding Artery Pressure

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Author(s):

Young, William L. M.D.; Kader, Abraham M.D.; Ornstein, Eugene Ph.D., M.D.; Baker, Kristy Z. M.D.; Ostapkovich,

Noeleen R.EPT.; Pile-Spellman, John M.D.; Fogarty-Mack, Patricia M.D.; Stein, Bennett M. M.D.; The Columbia

University Arteriovenous Malformation Study Project

Issue: Volume 38(6), June 1996, pp 1085-1095

Publication Type: [Clinical Studies]

Publisher: Copyright © by the Congress of Neurological Surgeons

Institution(s):

Departments of Anesthesiology (WLY, EO, KZB, NO, PF-M), Neurological Surgery (WLY, AK, JP-S, BMS), and

Radiology (WLY, JP-S), College of Physicians and Surgeons, Columbia University, New York, New York

Received, November 27, 1995. Accepted, January 12, 1996.

Reprint requests: William L. Young, M.D., Columbia-Presbyterian Medical Center, 630 W. 168th Street, New York,

NY 10032.

Keywords: Brain swelling, Cerebral autoregulation, Cerebral blood flow, Cerebral hemorrhage, Cerebrovascular CO2 reactivity,

Complications, surgical

Table of Contents:

≪ ANNOUNCEMENT. ≫ Long-term Treatment of Malignant Gliomas with Intramuscularly Administered Polyinosinic-Polycytidylic Acid Stabilized with Polylysine and Carboxymethylcellulose: An Open Pilot Study.

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AbstractComplete ReferenceExternalResolverBasic

Outline

● Abstract ● PATIENTS AND METHODS

�❍ Overview of study �❍ Intraoperative management

and timing of measurements �❍ Arterial CO2 pressure

(PaCO2) management �❍ CBF methodology �❍ Control group �❍ Correction factors for CBF �❍ Definition of breakthrough

complications �❍ Data analysis

● RESULTS �❍ Incidence of NPPB �❍ Relationship of CBF changes

to NPPB �❍ Influence of detector location

on CBF results �❍ Relationship of CBF changes

to other clinical and physiological variables

�❍ Relationship of FMAP to CBF changes

Abstract

TO STUDY THE pathophysiology of idiopathic postoperative brain swelling

or hemorrhage after arteriovenous malformation resection, termed normal

perfusion pressure breakthrough (NPPB), we performed cerebral blood flow

(CBF) studies during 152 operations in 143 patients, using the xenon-133

intravenous injection method. In the first part of the study, CBF was

intraoperatively measured (isoflurane/N20 anesthesia) during relative hypocapnia

in 95 patients before and after resection. The NPPB group had a greater increase (P

< 0.0001) in mean ± standard deviation global CBF (28 ± 6 to 47 ± 16 ml/100 g/min,

n = 5) than did the non-NPPB group (25 ± 7 to 29 ± 10 ml/100 g/min, n = 90);

both arteriovenous malformation groups showed greater increase (P < 0.05) than

did controls undergoing craniotomy for tumor (23 ± 6 to 23± 6 ml/100 g/min, n =

22). Ipsilateral and contralateral CBF changes were similar. In a second cohort

of patients with arteriovenous malformations, CBF was measured at

relative normocapnia and it increased (P < 0.002) from pre- to postresection (40 ±

13 to 49 ± 15 ml/100 g/min, n = 57). There were no NPPB patients in this

latter cohort. The feeding mean arterial pressure was measured

intraoperatively before resection or at the last embolization before surgery (n =

64). The feeding mean arterial pressure (44 ± 16 mm Hg) was 56% of the

systemic arterial pressure (78± 12 mm Hg, P < 0.0001) and was not related to

changes in CBF from pre- to postresection. There was an association

between increases in global CBF from pre- to postresection and NPPB-

type complications, but there was no relationship of these CBF changes

to preoperative regional arterial hypotension. These data do not support a

uniquely hemodynamic mechanism that explains cerebral hyperemia as

a consequence of repressurization in hypotensive vascular beds.

The pathogenesis of idiopathic postoperative brain swelling and

intracranial hemorrhage (ICH) after arteriovenous malformation (AVM)

resection, termed normal perfusion pressure breakthrough (NPPB), is


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�❍ Relationship of CBF changes to general neurological outcome

�❍ Relationship of CBF changes in AVM patients to that in control patients

● DISCUSSION �❍ Relationship of CBF and NPPB �❍ Time effect of volatile

anesthetics �❍ Relationship between

cerebral arterial pressure and CBF changes

�❍ Possible mechanisms for postoperative CBF changes

● CONCLUSION ● ACKNOWLEDGMENTS ● REFERENCES ● APPENDIX ● COMMENTS

Graphics

● Figure 1 ● Figure 2 ● Table 1 ● Table 2 ● Figure 3 ● Table 3 ● Table 4 ● Figure 4 ● Plate 9

unclear. Although most large series describe an incidence


of the sterile field) (Fig. 1). The protocol was modified during the latter part of the study to address the two following

primary criticisms: 1) that relative hypocapnia may blunt any hyperemic responses and 2) that the detector placement was

not sensitive to changes occurring at the margins of the resection. To this end, during the latter third of the study, pre-

and postresection CBF was measured at relative normocapnia; CO2 was added to the inspired gas mixture for the postresection

CBF measurement (n = 57). In addition, ipsilateral CBF monitoring was accomplished by placement of a sterilized

detector immediately adjacent to the margin of the resection (n = 38).

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FIGURE 1. Depiction of CBF detector placement for “near” detectors (those placed in the sterile field directly over the

cortex) and“distant” detectors (those placed adjacent to the sterile field at the margin of the craniotomy). See text

for further explanation.

Intraoperative management and timing of measurements

Anesthetic management was a 0.75 to 0.9% isoflurane/60% N2O/O2 balanced technique, titrated to maintain patient blood

pressure within [approximately equal to]10% below ward values. After placement of spinal drainage, patients were positioned

in rigid pin fixation. An operating microscope was used in all patients. With dural exposure, a baseline CBF measurement

was obtained. The final CBF measurement took place after the AVM was completely removed, during inspection of the surgical

bed for hemostasis.

Expired concentration of anesthetic was adjusted to identical values for the pre- and postresection CBF measurements. After

the postresection CBF measurement, phenylephrine was generally used to increase mean arterial pressure 20 to 30% to

further verify hemostasis. Thereafter, use of the isoflurane was discontinued and, until 1988, propranolol and hydralazine

were used to control emergence and postoperative hypertension. Esmolol and labetalol were used after this time to maintain


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the mean arterial pressure at approximately 10% below baseline preoperative values.

When a suitable artery could be identified, the FMAP was intraoperatively measured with the use of a 26-gauge needle

transduced with a strain gauge. Otherwise, the FMAP was examined from the last embolization before surgery during which

pressure was measured using a 1.5-French superselective catheter immediately before injection of N-butyl cyanoacrylate glue (11).

Arterial CO2 pressure (PaCO2) management

In all patients, after the initial CBF measurement, cerebrovascular reactivity to CO2 was individually established for each

patient before resection by increasing PaCO2 by [approximately equal to]10 mm Hg by adding CO2 to the fresh gas mixture or

by changing minute ventilation. During the first two-thirds of the study, postexcision measurements were made at

relative hypocapnia and compared with the preresection hypocapnic measurements. During the latter third of the

study, postexcision measurements were made at relative normocapnia and compared with the preresection

normocapnic measurements(CO2 was added to the inspired gas mixture before the final CBF measurement). During the

actual microsurgical resection, however, PaCO2 was managed at the hypocapnic level in all patients.

CBF methodology

The CBF measurements were performed using a Cerebrograph 10a (Novo Diagnostic Systems, Bagsvaerd, Denmark), as

previously described (36, 39, 40). The arterial input function was estimated by a sampling of end-tidal gas from the

endotracheal tube. Because the purpose of this study was to investigate hemispheric flow derangements that may occur

in anatomically normal vascular beds as a result of surgical excision, detectors were placed to interrogate normal tissue in the

same major arterial supply territory as the fistula. One detector was placed 5 to 6 cm from the margin of the resection, and

the other was placed in a contralateral homologous position.

In the last 38 patients, a sterilized detector was mounted in the operative field over the cortex immediately adjacent to the

margin of the AVM in the same arterial supply (Fig. 1). CBF was measured by the intravenous injection of [approximately equal

to]20 mCi xenon-133 in saline, and tracer washout was recorded for 11 minutes. CBF data were analyzed by the M2 model

and expressed as the Initial Slope Index, in units of milliliters per 100 grams per minute, assuming a combined tissue http://ovidsp.tx.ovid.com/spb/ovidweb.cgi (5 of 24) [6/12/2008 5:47:41 PM]


partition coefficient of 1.0 (40).

Control group

A control group of 22 patients undergoing craniotomy for mass lesions(tumors) was also studied. The anesthetic management

and the timing of the CBF measurements were the same. Vascular pressures were not measured.

Correction factors for CBF

There were small changes in PaCO2 between the CBF measurements and unavoidable increases in temperature and decreases

in hematocrit over the course of surgery. Such changes might affect the interpretation of individual data, although group data

can be analyzed by standard statistical techniques. Therefore, to evaluate individual patients, we also examined corrected

CBF data (CBFcorrected). The observed CBF was “corrected” to render the pre-excision CBF value more comparable to

the physiological conditions present at the postresection measurement. The following corrections were used: 1)

individual preresection CO2 reactivity, calculated as the absolute increase in CBF per mm Hg change in PaCO2, expressed as

ml/100 g/min/mm Hg (if missing [n = 7], the group mean was used), 2) 1% increase in CBF for each 0.1°C increase in

core temperature (37), and 3) 3% increase in CBF for each percentage increase in hematocrit (12).

Comparisons were made with both uncorrected and corrected values for absolute and percentage change between preresection

and postresection values. Because no significant difference was found between the four ways of expressing CBF change,

most comparisons are given as only percent change in CBFcorrected from baseline (%[DELTA]CBF), for the sake of clarity. A

histogram of relative and percentage changes was visually inspected to verify that values were normally distributed.

Definition of breakthrough complications

NPPB was defined as intraoperative brain swelling interfering with the course of surgery, postoperative computed tomography

or magnetic resonance imaging evidence of brain swelling that went beyond the immediate proximity of the surgical bed,

or postoperative ICH that could not be explained by other causes. The assignment of NPPB was made by the senior

neurosurgeon (BMS) without knowledge of CBF results. In addition, all cases of postoperative hemorrhage or swelling that


Ovid: Cerebral Hyperemia after Arteriovenous Malformation Resection Is Related to"Breakthrough" Complications but Not to Feeding Artery Pressure.occurred during the time period of the study but were not included in the CBF protocol were reviewed.

Data analysis

Data are reported as mean ± standard deviation (SD) (except in Fig. 2 for clarity, in which the standard error of the mean is

given). Continuous data were analyzed by repeated-measures analysis of variance and linear regression or Spearman

rank correlation. Category data were analyzed by [chi]2 or Fisher's exact test.


FIGURE 2. Mean ± standard error of the mean changes in uncorrected CBF from pre- to postresection in 95 patients

undergoing AVM resection under relative hypocapnia. Patients with NPPB (n = 5) had a greater(P < 0.0001) increase in

CBF from pre- to postresection than did AVM patients without NPPB (n = 90). Both NPPB(P < 0.001) and non-NPPB (P<

0.05) patients had a greater increase in CBF after resection than did control patients (n = 22).

RESULTSIncidence of NPPB

During the entire study period, there were 260 operations performed in 235 patients with AVMs. All cases of

postoperative hemorrhage or significant bilateral or holohemispheric brain swelling in this period were reviewed and are listed

in Table 1. There were six cases attributed to NPPB, for a total incidence of 2.3% per surgery (or 2.6% per patient). As shown

in Table 1, two patients had immediate (



TABLE 1. Postoperative Hemorrhage or Hemispheric Swelling in 260 Arteriovenous Malformation Operations in 235

Patientsa

There were also five hemorrhages that were not assigned to the NPPB group. Two were caused by residual AVMs documented

by angiogram, one of which was fatal 3 days postoperatively. There were two hemorrhages into the operative bed without

mass effect seen on routine postoperative computed tomographic scans, which were not clinically significant. Finally, there

was one epidural hematoma.

Relationship of CBF changes to NPPB

CBF studies were performed during 152 operations in 143 patients. There were 125 patients with AVMs who had single-stage

surgery and 18 who had two-stage surgery. Of the 18 patients undergoing two stages, 9 patients underwent CBF monitoring

during both stages, 5 underwent it during the first surgery only, and 4 underwent it during the second surgery only.

There were five patients with NPPB in the group that underwent CBF monitoring (one patient with severe brain swelling in the

NPPB group did not have CBF measured). All NPPB complications occurred during the first phase of the study when

CBF measurements were made at relative hypocapnia; preoperative embolization was performed in 28% of patients in this group.

In the second half of the study, in which CBF was measured at relative normocapnia, 76% had undergone preoperative embolization.


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There was no difference between changes in ipsilateral and contralateral CBF. For the patients studied during relative

hypocapnia, the NPPB group had a greater increase in both global CBF and CBFcorrected (P < 0.0001), as shown in Table 2 and

Figure 2. Figure 3 shows the%[DELTA]CBF from pre- to postresection. CBF and physiological variables for the group studied

during relative normocapnia are shown in Table 3. Other than differences in PaCO2, there was no difference in

physiological variables between the patients studied during relative hypocapnia and relative normocapnia. The relative%[DELTA]

CBF from pre- to postresection was similar for both groups (18 ± 47 versus 16 ± 26%, P = 0.80). Therefore, the PaCO2 level did

not influence the magnitude of pre- to postresection CBF increases. The%[DELTA]CBF in four patients with

postoperative hemorrhages not assigned to the NPPB was not different(P > 0.8) from that of the other non-NPPB patients.


TABLE 2. Cerebral Blood Flow and Associated Physiological Variables Measured Pre- and Postresection at Relative

Hypocapnia (n = 95)a


FIGURE 3. Individual values for%[DELTA]CBF (see text for explanation) from pre- to postresection in 95 patients

undergoing AVM resection under relative hypocapnia. Values for mean ± SD are also shown. Patients with NPPB had a

greater (



TABLE 3. Cerebral Blood Flow and Associated Physiological Variables Measured before and after Resection at

Relative Normocapnia (n = 57)a

In the relative hypocapnic group, global CO2 reactivity tended to be slightly higher in the NPPB (n = 5) than in the non-NPPB (n =

83) group (2.4± 0.9 versus 1.8 ± 0.8 ml/100 g/min/mm Hg, P = 0.12) but there was no difference between ipsilateral

and contralateral values. CO2 reactivity was not different between the hypo- and normocapnic groups (1.8 ± 0.8 versus 2.0 ±

1.4 ml/100 g/min/mm Hg).

In the cohort studied at relative normocapnia, both the percent (14± 35%) and absolute (3 ± 10 ml/100 g/min) changes

in CBFcorrected were used to estimate the sensitivity of CBF monitoring to detect NPPB. For the NPPB group, 60% (three of

five patients) had a >2 SD increase from pre- to postresection for both percent and absolute CBF values. For the non-NPPB

group, this was 4 and 7%, respectively, approximating the expected values >2 SD in a normal distribution.

Influence of detector location on CBF results

There was no influence of detector location on CBF results. The increase in CBF (P < 0.0001) from pre- to postresection was

similar whether the detector was adjacent to the AVM nidus or mounted 5 to 6 cm distant. Values for ipsilateral and

contralateral CBF in both groups of patients are shown in Table 4.


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TABLE 4. Comparison of Detector Location on Cerebral Blood Flow Changes in 57 Patients Studied During

Normocapniaa

Relationship of CBF changes to other clinical and physiological variables

There was no relationship between CBF changes and size, feeding artery, or number of embolizations. Patient age was 35 ±

11 years. There was, as might be expected, a weak inverse correlation between age and preresection CBF(r = 0.24, P =

0.003). However, changes in CBF were not related to age. The largest AVM diameter was 4.3 ± 1.8 cm, with no difference

between NPPB and non-NPPB groups. Primary location was in the cerebral hemispheres in 139 (91%) patients, the basal

ganglia/diencephalon in 7 (5%), and the posterior fossa in 6 (4%). There was no influence of location on CBF changes.

Central venous and pulmonary artery pressures were measured in 83 patients. There was no relationship between CBF and

central filling pressures. There was a small increase (P < 0.0001) from pre- to postresection for both pulmonary artery

diastolic pressure (11 ± 4 to 12 ± 5 mm Hg) and central venous pressure (7 ± 4 to 9 ± 4 mm Hg). Cardiac output was measured in

69 patients and tended to increase (P = 0.064) from pre- to postresection (6.7 ± 1.7 to 7.1 ± 2.2 L/min). There was no

relationship to changes in CBF.

The change in CBF from pre- to postresection was not related to the time elapsed from induction of anesthesia to the final

CBF measurement. Isoflurane-expired concentration did not change (0.83 ± 0.20 versus 0.84 ± 0.17%), and small individual

changes had no relationship to changes in CBF.

Relationship of FMAP to CBF changes

The FMAP (44 ± 16 mm Hg) was 56% of the systemic arterial pressure(78 ± 12 mm Hg, P < 0.0001) and was not related to%

[DELTA]CBF from pre- to postresection (y = 0.2x + 13, r = 0.07, P= 0.57, n = 64), as shown in Figure 4. There was no

apparent influence of prior embolization on this relationship; patients who had undergone prior embolization are indicated in http://ovidsp.tx.ovid.com/spb/ovidweb.cgi (11 of 24) [6/12/2008 5:47:41 PM]

http://ovidsp.tx.ovid.com/spb/ovidweb.cgi?View+Image=00006123-199606000-00005|TT4&S=EAJDFPODPEDDOKFDMCHLGBOKNPPPAA00&WebLinkReturn=Full+Text%3dL%7cS.sh.15.16.42.46%7c0%7c00006123-199606000-00005http://www.ovid.com/site/help/documentation/ovidsp/en/imview.htmhttp://ovidsp.tx.ovid.com/spb/ovidweb.cgi?S=EAJDFPODPEDDOKFDMCHLGBOKNPPPAA00&Save+As+Jumpstart=Image%7c%26PAGE%3dimage%26IMAGE%3d00006123-199606000-00005%7cTT4%26D%3dovft


Figure 4. When limited to the 20 FMAP measurements taken intraoperatively immediately before the preresection CBF

measurement (at the same time under similar physiological conditions), there was still no evidence for larger increases in CBF to

be associated with low FMAP. Only one patient who developed NPPB had FMAP measured.


FIGURE 4. Individual values for%[DELTA]CBF from pre- to post-resection in 64 patients who had FMAP measured during

craniotomy or during the last embolization session before surgery. There was no relationship(y = 0.2x + 13, r = 0.07, P =

0.57). The findings were similar when patients were restricted to only those who had FMAP measured during craniotomy.

Relationship of CBF changes to general neurological outcome

Excluding the cases of hemorrhage, there was no relationship between changes in CBF and other neurological deficits.

Relationship of CBF changes in AVM patients to that in control patients

CBF changes for the control group are shown in Table 2 and Figure 2. Unlike the AVM group, there was no significant change

from pre- to postresection. Preresection CO2 reactivity in the control group (1.6 ± 1.0 ml/100 g/min/mm Hg) was not different

from that in the AVM group. Compared with that in the AVM group, the postresection CBF measurement was performed sooner (P

< 0.05) after the induction of anesthesia (6.0 ± 1.8 versus 7.4 ± 1.7 h). Systemic mean arterial pressure at the postresection

CBF was higher(P < 0.05) in the control group (83 ± 12 versus 79± 11 mm Hg).

DISCUSSION

The primary focus of this study was to systemically delineate the relationship of altered cerebral hemodynamics as a result

of arteriovenous shunt ablation on the pathophysiology of certain postoperative complications. There are three main findings.

First, patients who have complications, such as swelling or hemorrhage attributable to NPPB, have greater increases in CBF


http://ovidsp.tx.ovid.com/spb/ovidweb.cgi?View+Image=00006123-199606000-00005|FF6D&S=EAJDFPODPEDDOKFDMCHLGBOKNPPPAA00&WebLinkReturn=Full+Text%3dL%7cS.sh.15.16.42.46%7c0%7c00006123-199606000-00005http://www.ovid.com/site/help/documentation/ovidsp/en/imview.htmhttp://ovidsp.tx.ovid.com/spb/ovidweb.cgi?S=EAJDFPODPEDDOKFDMCHLGBOKNPPPAA00&Save+As+Jumpstart=Image%7c%26PAGE%3dimage%26IMAGE%3d00006123-199606000-00005%7cFF6D%26D%3dovft


after resection than those who do not display NPPB. These changes, however, are global. Second, these CBF changes are not

related to the degree of hypotension caused by the shunt; that is, there was no relationship to increases in CBF and

preresection FMAP. Third, the placement of CBF detectors, whether immediately adjacent to or removed from the margin of

the nidus, influences neither the detection nor the degree of hyperemia after resection.

Relationship of CBF and NPPB

This investigation confirms previous reports that NPPB is a relatively rare occurrence, and studies to investigate its

pathophysiology are inherently limited by statistical power issues. This study is the largest series to date to

investigate cerebrovascular phenomena related to NPPB.

There is a wide range of definitions given for NPPB or“hyperemic” complications in the literature (2, 3, 4, 9, 15, 23, 25, 30,

35). This is an inherent problem in any study in which an attempt is made to determine the pathophysiological conditions that

are associated with NPPB. There is no universally acceptable way to independently verify the existence of NPPB. We

have attempted to constrain our assignment of this syndrome to patients in whom swelling and hemorrhage did not have

another proximate cause. As a practical matter, we emphasize that the diagnosis of“hyperemic complications” should be

a diagnosis of exclusion only after all possible causes of swelling or hemorrhage have been carefully considered. In our series,

it may be that, for example, our patient with postoperative ICH, without an angiogram or an autopsy, may have had a residual

AVM that was not identified during surgical re-exploration. Therefore, our reported incidence of NPPB (2.3% per surgery)

may actually overestimate the true incidence.

Compared with control patients, patients with AVMs had a larger increase in global CBF after resection, but the difference

was small. We used a series of correction factors for our CBF values to ascertain whether decreases in hematocrit and increases

in temperature introduced systematic error into our data. It does not seem that increases seen after resection are

entirely attributable to these physiological factors.

NPPB-type complications are associated with a greater increase in CBF than that which occurs in those patients who do not

have evidence of“hyperemic” complications. However, these changes are not restricted to the brain sharing the same


Ovid: Cerebral Hyperemia after Arteriovenous Malformation Resection Is Related to"Breakthrough" Complications but Not to Feeding Artery Pressure.circulatory bed as the AVM and are global in nature. Despite the consistent presence of hyperemia after AVM resection,

monitoring of xenon-133 CBF does not seem to have great sensitivity(60%) to discriminate potential cases of NPPB.

All of our complications attributable to NPPB occurred in patients in the first part of the series. PaCO2 management was

identical except for the brief period of CBF measurement. Possible influences may have been the difference in agents used

for emergence and postoperative blood pressure control (hydrazine and propranolol early, labetalol and esmolol later)

or improvements in techniques of preoperative endovascular embolization.

Time effect of volatile anesthetics

Anesthetic agents influence CBF; some authors have described a time effect of the volatile agents, such as isoflurane. In

several nonprimate animal models, volatile anesthetics induced cerebral hyperemia, which resolved over time (1, 7, 8, 33, 34).

The mechanism was not related to O2 consumption (8) or pH changes (34). In primates, an opposite effect was observed;

CBF progressively increased over time during isoflurane anesthesia, and the increases were blocked by arginine analogs

(21), suggesting involvement of a nitric oxide pathway.

Such effects are controversial, however, because they could not be demonstrated in at least one canine model (27) or in one of

our previous studies in humans undergoing craniotomy for tumor resection (24). A time effect does not seem likely in the

present study. First, there was no increase in CBF over time in the control group. In addition, the increase in CBF in AVM

patients from pre- to postresection was not related to the time elapsed between induction of anesthesia to the final

postresection CBF measurement. Therefore, it is unlikely that our observations in patients with AVMs were simply an artifact of

the anesthetic technique.

Relationship between cerebral arterial pressure and CBF changes

One of the main reasons for the current approach to staged treatment of patients with AVMS (either by embolization or

staged surgery) is to prevent complications resulting from too rapidly changing local cerebral hemodynamics after interruption

of the AVM shunt. This notion is largely based on the assumption that restoration of normal perfusion pressure to

previously hypotensive brain regions will overwhelm local autoregulatory capacity and result in hyperperfusion injury (31).

There are two observations in the present series that argue against such a mechanism. First, there was no relationship between http://ovidsp.tx.ovid.com/spb/ovidweb.cgi (14 of 24) [6/12/2008 5:47:41 PM]


CBF changes after resection and preresection FMAP. If CBF changes were uniquely caused by reperfusion in a paralyzed

vascular bed, the beds with the greatest CBF changes would be expected to have the lowest pretreatment perfusion pressure;

this was not the case. Second, the CBF changes were global, even in patients who developed NPPB. We have recently

presented further arguments against loss or autoregulatory capacity in regions adjacent to AVMs; even severe hypotension

in apparently eloquent brain regions does not necessarily result in loss of autoregulatory vasoconstriction (38).

Our data do not exclude, however, the possibility that there is some“microenvironment” immediately adjacent to the nidus

that may be affected by local hemodynamic changes after treatment. Cortical areas adjacent to AVMs may be unable to dilate

to reductions in local perfusion pressure, as assessed in a previous study using acetazolamide-enhanced single photon

emission tomography (13) (these adjacent regions generally retained intact autoregulatory vasoconstriction to blood

pressure increases with phenylephrine). In the present study, however, the possibility of severe local CBF changes in our

cohort studied with a detector 5 to 6 cm distant from the edge of the nidus cannot be absolutely ruled out. The cohort in which

a detector was placed immediately adjacent to the AVM displayed global hyperemia after resection, but none of this

group developed NPPB. We emphasize that the highly localized hyperemia that our detectors may have missed cannot

explain hemispheric swelling.

Possible mechanisms for postoperative CBF changes

Besides the NPPB theory, other alternative mechanisms for swelling or hemorrhage after treatment include reversal of

decreased pulsatility (10, 16, 17), venous hypertension (2), and technical complications of surgery (14, 26, 32). Another

mechanism is related to autonomic perivascular innervation, which can profoundly influence CBF in various

pathophysiological states (18, 19). A derangement in autonomic perivascular innervation to normal circulatory beds in AVM

patients in compatible with certain paradoxical CBF responses in AVM patients to pharmacological challenges (6, 36, 39).

For example, Batjer (5) argues that post-treatment hyperemia is caused by a deranged vascular bed that actively participates

in swelling and not simply by passive behavior of a paralyzed vascular bed. Although feeding vessels themselves seem to be

devoid of all autonomic or peptidergic innervation (20, 22), local changes in peptidergic activity in adjacent circulatory regions

may somehow affect distant beds by collateral innervation. Such a mechanism might explain why there seem to be global



increases in CBF after many cases of AVM resection, which cannot be explained by local changes in perfusion pressure.

Global changes are also seen after carotid endarterectomy (28, 29), another instance in which repressurization of a

previously hypotensive vascular territory should, intuitively, lead to regional rather than global changes in perfusion.

CONCLUSION

This study does not support a uniquely hemodynamic mechanism that explains cerebral hyperemia as a consequence

of repressurization in hypotensive vascular beds. Further efforts should be aimed at elucidating a mechanism that can

explain global changes in CBF after treatment.

ACKNOWLEDGMENTS

This work was supported by National Institutes of Health Grant RO1-NS27713. We thank Joyce Ouchi and Steven Marshall, B.S.,

for assistance in preparation of the manuscript and Dennis Lu, M.S., and the Neuroradiology technologist staff for expert

technical assistance. We gratefully acknowledge the support and contributions of the other members of the Columbia

University AVM Study Project.

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adaptive autoregulatory displacement in hypotensive cortical territories adjacent to arteriovenous malformations.


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Neurosurgery 34:601-611, 1994. Ovid Full Text ExternalResolverBasic Bibliographic Links [Context Link]

39. 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 27:257-267, 1990.


40. Young WL, Prohovnik I, Schroeder T, Correll JW, Ostapkovich N: Intraoperative 133Xe cerebral blood flow measurements

by intravenous versus intracarotid methods. Anesthesiology 73:637-643, 1990. Ovid Full Text ExternalResolverBasic

Bibliographic Links [Context Link]

1. Takayasu M, Dacey RG Jr: Spontaneous tone of cerebral parenchymal arterioles: A role in cerebral hyperemic phenomena.

J Neurosurg 71:711-717, 1989. ExternalResolverBasic Bibliographic Links [Context Link]

APPENDIX

The following members of the Columbia University Arteriovenous Malformation Study Project also contributed to this work:

Andrei Osipov, M.D.; Tara Jackson, B.S.; LaSandra Jackson, B.S.; Lofti Hacein-Bey, M.D.; Robert R. Sciacca, Eng.Sc.D.; J.P. Mohr,

M.D.; Isak Prohovnik, Ph.D.; Lauren H. Fleischer, M.D.; Michael B. Sisti, M.D.; Robert A. Solomon, M.D.

COMMENTS

In this article, Young et al. make another very significant contribution to our understanding of the hemodynamics of

cerebral arteriovenous malformations(AVMs) as part of their large experience in the Columbia University AVM Study Project.

They have measured cerebral blood flows (CBFs) and feeding cerebral artery pressures in 152 operative procedures for patients

with cerebral AVMs. They have demonstrated a significant increase in global CBF in the small number of patients who go on

to develop normal perfusion pressure breakthrough(NPPB). The CBF changes were similar both ipsilateral and contralateral to

the AVM resection. The authors were unable to correlate feeding mean arterial pressure, however, with the propensity of

patients to develop NPPB. These findings call into question the hypothesis that chronic low perfusion pressures in the

feeding arteries of cerebral AVMs are the sole explanation for this type of cerebral hyperemic phenomenon (1). The authors do

not propose a significant alternative hypothesis.

As the authors indicate, they have made some significant changes in their experimental paradigm since the initiation of


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