Download Continuous Monitoring of Cerebrovascular Autoregulation

Continuous Monitoring of Cerebrovascular Autoregulation
After Subarachnoid Hemorrhage by Brain Tissue Oxygen
Pressure Reactivity and Its Relation to Delayed
Cerebral Infarction
Matthias Jaeger, MD; Martin U. Schuhmann, MD, PhD; Martin Soehle, MD;
Christoph Nagel, MD; Jürgen Meixensberger, MD, PhD
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Background and Purpose—Disturbances of cerebrovascular autoregulation are thought to be involved in delayed cerebral
ischemia and infarction after aneurysmal subarachnoid hemorrhage (SAH). We hypothesized that the continuous
monitoring of brain tissue oxygen (PtiO2) pressure reactivity enables the detection of impaired autoregulation after SAH
and that impaired autoregulation is associated with delayed infarction.
Methods—In 67 patients after severe SAH, continuous monitoring of cerebral perfusion pressure (CPP) and PtiO2 was
performed for an average of 7.4 days. For assessment of autoregulation, the index of PtiO2 pressure reactivity (ORx) was
calculated as a moving correlation coefficient between values of CPP and PtiO2. Higher ORx values indicate disturbed
autoregulation, whereas lower ORx values signify intact autoregulation.
Results—Twenty patients developed delayed cerebral infarction, and 47 did not. Mean ORx was significantly higher in the
infarction group compared with the noninfarction group (0.43⫾0.09 vs 0.23⫾0.14, respectively; P⬍0.0001). In a
day-by-day analysis, ORx did not differ between groups from days 1 to 4 after SAH but was significantly higher from
day 5 onward in the infarction group, indicating a deficit of autoregulatory capacity. In a logistic-regression model, ORx
values from days 5 and 6 after SAH carried predictive value for the occurrence of delayed infarction but before this event
ultimately occurred (P⫽0.003).
Conclusions—ORx indicates impaired autoregulation in patients who develop delayed infarction after SAH. Furthermore,
this index may distinguish between patients who finally develop delayed infarction and those who do not. (Stroke. 2007;
38:981-986.)
Key Words: autoregulation 䡲 brain tissue oxygen 䡲 delayed ischemia 䡲 subarachnoid hemorrhage
P
increased risk for delayed ischemia and infarction. The
continuous monitoring of brain tissue oxygen (PtiO2) pressure
reactivity has been shown to allow for an assessment of
autoregulation after head injury.8 In this study, we examine
the hypothesis that the continuous monitoring of PtiO2 pressure reactivity enables the detection of autoregulatory disturbances after SAH and that these disturbances are related to
the occurrence of delayed cerebral infarction.
atients after aneurysmal subarachnoid hemorrhage (SAH)
carry a considerable risk for the development of delayed
cerebral ischemia and subsequent cerebral infarction. These
critical reductions of brain perfusion are typically attributed
to posthemorrhagic vasospasm, but the traditional concept of
progressive vessel narrowing as the sole cause for ischemia
has been challenged.1–3 Other models suggest that disturbances of cerebrovascular autoregulation are involved in the
development of delayed ischemia. After SAH, when autoregulation is frequently impaired,4 – 6 the risk of ischemia may
increase as the disturbed autoregulatory function of the
cerebral vasculature fails to compensate for reductions in
vessel diameter caused by vasospasm. In contrast, patients
with intact autoregulation appear not to experience delayed
ischemia after SAH.1,7
Assessment of the status of cerebrovascular autoregulation
could thus play a role in the identification of patients with an
Patients and Methods
Patients and Management
Sixty-seven patients with the diagnosis of acute SAH were included
in this study. Collected data included age, sex, neurological status
according to the World Federation of Neurosurgical Societies,9 the
amount of blood on computed tomography (CT) scan according to
Fisher et al,10 location of the aneurysm, and choice of treatment
(surgical clipping versus endovascular coiling).
Received June 12, 2006; final revision received September 22, 2006; accepted October 11, 2006.
From the Department of Neurosurgery, University of Leipzig (M.J., M.U.S., C.N., J.M.), Leipzig, Germany; and the Department of Anaesthesiology
and Intensive Care Medicine, Rheinische-Friedrich-Wilhelms University (M.S.), Bonn, Germany.
Correspondence to Matthias Jaeger, Department of Neurosurgery, University of Leipzig, Liebigstrasse 20, D-04103 Leipzig, Germany. E-mail
[email protected]
© 2007 American Heart Association, Inc.
Stroke is available at http://www.strokeaha.org
DOI: 10.1161/01.STR.0000257964.65743.99
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After admission, early cerebral angiography was done to identify
the source of bleeding. The decision to treat the aneurysm by either
craniotomy and surgical clipping or interventional endovascular coil
occlusion was based on an interdisciplinary consensus of the treating
neurosurgeon and the interventional neuroradiologist after an analysis of the individual risks and chances of each therapeutic modality.
After aneurysm occlusion, therapy aimed at avoiding secondary
hypotensive episodes by maintaining euvolemia (central venous
pressure at 6 to 10 cm H2O) and mean arterial pressure (MAP) of 80
to 90 mm Hg. When necessary, MAP was elevated by moderate
volume expansion and individually titrated vasopressors (noradrenaline, dobutamine, and/or dopamine).
The clinical condition of all patients included in this study was
considered poor due to their neurological impairment or SAHassociated cardiac or pulmonary failure; therefore, they required
continuous sedation and artificial ventilation. Midazolam (6 to 18
mg/h) and fentanyl (0.1 to 0.5 mg/h) were used for analgesia and
sedation. Patients were ventilated to keep the partial pressure of
arterial carbon dioxide (PaCO2) at 35 to 40 mm Hg and the partial
pressure of arterial oxygen (PaO2) at 100 to 120 mm Hg. Arterial
blood gas samples were obtained every 8 hours or as clinically
indicated to adjust ventilation parameters (ABL 700, Radiometer
A/S). In all patients, an external ventricular drain was placed for
treatment of acute hydrocephalus. As a general policy in our
department, external ventricular drains are inserted in SAH patients
admitted with a Glasgow Coma Scale score ⬍14 to rule out
hydrocephalus as the underlying cause for the depressed consciousness. Nimodipine 6⫻60 mg was administered via nasogastric tube.
None of the patients underwent postoperative/postinterventional
angiography, endovascular angioplasty, or intra-arterial papaverine
infusion. Treatment was performed according to previously published recommendations.11,12
Outcome was assessed at 6 months after the hemorrhage according
to the Glasgow Outcome Scale (GOS) either by personal follow-up
examination or by telephone interview with the patient, next relative,
or caregiver.13
Neuromonitoring
All patients were included in our routine multimodal neuromonitoring protocol for patients with acute severe cerebral insults, comprising measurement of MAP, intracranial pressure (ICP), cerebral
perfusion pressure (CPP), and PtiO2. MAP was monitored by a
catheter inserted into the radial or femoral artery with the transducer
referenced to the foramen of Monro (DTXPlus, Becton Dickinson
Infusion Therapy Systems Inc). CPP was calculated as the difference
between MAP and ICP. Data for ICP (Codman Microsensors ICP
Transducer, Codman & Shurtleff Inc) and PtiO2 (Licox CC1.SB,
Integra NeuroSciences Inc) were monitored with flexible catheters
inserted via a double-lumen skull bolt kit (Licox IM2, Integra
NeuroSciences Inc) into the frontal white matter of the hemisphere
supplied by the aneurysm-carrying artery. In case of anterior communicating artery aneurysms or posterior circulation aneurysms, the
right frontal region was chosen. Probes were inserted in the intensive
care unit after occlusion of the aneurysm and a CT scan obtained
within 24 hours after aneurysm occlusion to rule out interventionrelated infarction. Correct positioning of the PtiO2 probe in CTnormal tissue at a depth of ⬇25 mm subdurally was confirmed by
routine CT. Neuromonitoring was carried out as long as
clinically indicated.
Analog data of MAP, ICP, CPP, and PtiO2 were sampled at 50 Hz
and processed through an analog-to-digital converter (Licox MMM,
Integra NeuroSciences Inc), and average values were stored on a
portable computer at the patient’s bedside every half minute.
Transcranial Doppler (TCD) examinations of mean blood flow
velocity in both middle cerebral arteries were done with a
hand-held 2-MHz probe (DWL Multidop X, DWL Elektronische
Systeme GmbH) during intensive care treatment. This was performed as part of the diagnostic routine every second to every
fourth day, and the maximum flow velocities obtained were
recorded for further analysis.
Index of PtiO2 Pressure Reactivity for
Determining Autoregulation
The index of PtiO2 pressure reactivity (ORx) was calculated as the
moving linear (Pearson’s) correlation coefficient between values of
CPP and PtiO2 from the previous 60 minutes of monitoring. Hence,
every 30 seconds, a new ORx value was calculated from 120 data
points. ORx has been demonstrated to allow for a continuous
assessment of cerebrovascular autoregulation at the patient’s bedside
after head injury and is described in detail elsewhere.8 In brief, the
physiological basis for determining autoregulation with PtiO2 monitoring is that PtiO2 is a surrogate marker of cerebral blood flow.14,15
Quantifying the relation between spontaneous fluctuations of CPP
and PtiO2 thus enables an assessment of autoregulation. ORx, which
may theoretically vary between ⫺1 and ⫹1, displays impaired
autoregulation when PtiO2 passively follows CPP. In this situation, a
good correlation between the 2 parameters exists and ORx is high.
When autoregulation is intact, PtiO2 is relatively unaffected by
changes in CPP, so that no correlation between CPP and PtiO2 can be
observed, and ORx is thus near zero.
This study was approved by the local ethics committee. Because
the invasive monitoring of MAP, ICP, CPP, and PtiO2 is standard
clinical practice in our department in patients with severe SAH
requiring continuous sedation and mechanical ventilation and the
calculation of ORx did not require additional patient manipulation,
the need for informed consent was waived.
Definition of Delayed Cerebral Infarction
Delayed cerebral infarction was defined as radiologically confirmed
new hypodensities on the CT scan that were attributable only to
posthemorrhagic cerebral vasospasm. New hypodensities due to
factors such as brain retraction during surgery, edema around an
intracerebral hematoma, and ischemic complications related to
aneurysm treatment were noted but not considered for analysis.
Statistical Analysis
Artifacts caused by temporary disconnection of catheters or nursing
interventions were manually eliminated from the data sets, and ORx
was calculated after artifact elimination. In cases of progressive
vasospastic cerebral infarction, data collection was terminated when
PtiO2 readings reached 2 mm Hg.
Individual mean values of all neuromonitoring parameters during
the whole monitoring period as well as for each single day after SAH
were calculated. Patients were divided into 2 groups depending on
the occurrence of delayed cerebral infarction as defined earlier.
Comparison of clinical and neuromonitoring parameters between
these 2 groups was done with the univariate Mann–Whitney U test
and ␹2 test (SPSS 11.0.1, SPSS Inc). Independent predictors of
delayed cerebral infarction were evaluated by fitting a step-down
logistic-regression model after identification of candidate variables
in the univariate analysis. A value of P⬍0.05 was considered
statistically significant.
Results
Patient Characteristics
Of the 67 patients in this study, 20 developed delayed
infarction. Table 1 shows the characteristics of both groups.
No differences between the groups were seen with respect to
clinical variables, except that in the infarction group, neuromonitoring ended significantly earlier, and the time of valid
monitoring during which artifact-free data were obtained was
significantly shorter.
Delayed cerebral infarction was diagnosed at an average of
9.0 days after SAH (range, 7 to 14 days) and was clinically
detected by routine CT scan (n⫽9) or worsening neuromonitoring trends (n⫽11). Outcome was significantly worse in the
infarction group, with all 20 patients having a poor outcome
(GOS 1 to 3), compared with the noninfarction group,
Jaeger et al
TABLE 1. Characteristics of the Noninfarction and
Infarction Groups
Variable
Noninfarction
Group
(n⫽47)
Infarction
Group
(n⫽20)
Age, y
53.0⫾13.2
50.8⫾11.2
0.50*
29/18
16/4
0.13†
Sex, female/male
P
WFNS grade
4 (4, 5)
4 (4, 4)
0.47*
Fisher grade
4 (3, 4)
3.5 (3, 4)
0.88*
0.25†
Aneurysm location
ACoA
18 (38%)
5 (25%)
ACA
2 (4%)
0 (0%)
Pericallosal artery
2 (4%)
2 (10%)
ICA
11 (23%)
9 (45%)
MCA
11 (23%)
2 (10%)
3 (6%)
2 (10%)
VB
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Clipping/coiling
31/16
Hypodensities not attributable
to delayed infarction
16 (34%)
11/9
0.50†
6 (30%)
0.75†
Start of monitoring after SAH, h
55.1⫾51.1
60.1⫾40.2
0.25*
End of monitoring after SAH, h
247.9⫾55.2
205.1⫾64.8
0.01*
Time of valid monitoring, h
165.3⫾56.6
129.6⫾53.3
0.02*
3 (2.25, 4)
1 (1, 2)
GOS score
0.000001*
Values are given as mean⫾SD, median (25th and 75th percentiles), or
absolute numbers (%). WFNS indicates World Federation of Neurological
Surgeons; ACoA, anterior communicating artery; ACA, anterior cerebral artery;
ICA, internal carotid artery; MCA, middle cerebral artery; VB, vertebrobasilar
system.
*P for Mann–Whitney U test; †P for ␹2 likelihood ratio.
wherein 29 patients had a poor outcome and 17 patients
achieved a favorable outcome (GOS 4 to 5). One patient was
lost to follow-up.
Neuromonitoring and
Autoregulation Characteristics
Values of CPP, ICP, PtiO2, and ORx for the entire period of
monitoring are given in Table 2. No significant differences
between groups were observed for the standard neuromonitoring parameters CPP, ICP, and PtiO2. In contrast, ORx was
significantly higher in the infarction group compared with the
noninfarction group. Mean daily values of ORx, CPP, ICP,
and PtiO2 from days 1 to 12 after SAH are presented in the
Figure. ORx did not differ between groups from days 1 to 4,
TABLE 2. CPP, ICP, PtiO2, and ORx Obtained During the Entire
Monitoring Period
Noninfarction
Group
(n⫽47)
Infarction
Group
(n⫽20)
CPP, mm Hg
81.1⫾12.1
82.8⫾11.4
0.43
ICP, mm Hg
12.2⫾3.9
14.4⫾5.2
0.10
PtiO2, mm Hg
23.9⫾5.8
20.8⫾5.0
0.06
ORx
0.23⫾0.14
0.43⫾0.09
0.0000002
Variable
Values are mean⫾SD.
P for Mann–Whitney U test.
P
Autoregulation and Delayed Infarction After SAH
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but from day 5 onward, it was significantly lower in the
noninfarction group than in the infarction group. Whereas
mean ORx gradually decreased to values ⬍0.2 in the noninfarction group, it remained ⬎0.4 in patients who developed
delayed infarction, indicating a persistent deficit in cerebrovascular autoregulatory capacity. Regarding the standard
neuromonitoring parameters, CPP showed significantly
higher values on days 4 and 5 in the infarction group, ICP
showed significantly higher values in the infarction group on
days 9 and 10, and PtiO2 showed significantly lower values in
the infarction group on day 8. These higher ICP and lower
PtiO2 readings at the beginning of the second week of
monitoring appear to be related to the occurrence of cerebral
infarctions with the associated elevations in ICP and deficits
in cerebral perfusion. Owing to the heterogeneous start and
end of monitoring, patient numbers per day varied in both
groups.
Maximum mean blood flow velocity in the middle cerebral
artery was 160⫾46 cm/s in the noninfarction group and
172⫾46 cm/s in the infarction group (P⫽0.32). In 2 patients
of the infarction group and 2 patients of the noninfarction
group, however, no reliable TCD data could be obtained
through the trans-temporal window during intensive care unit
treatment.
Early Predictors of Delayed Cerebral Infarction
Because ORx displayed significant differences between the
noninfarction and infarction group from day 5 onward but
delayed cerebral infarction was detected at the earliest on day
7 after SAH, this suggested a “diagnostic window” at days 5
and 6 that might allow for the early identification of patients
with an increased risk for delayed infarction but before this
event ultimately occurs.
In the univariate analysis, mean values at days 5 and 6 of
ORx, PtiO2, and CPP were identified as candidate variables
for a logistic-regression model, because they displayed significant differences between the noninfarction and infarction
group (ORx, 0.25⫾0.16 vs 0.41⫾0.15, P⫽0.0007; PtiO2,
26.3⫾7.6 vs 19.9⫾8.7 mm Hg, P⫽0.02; CPP, 78.1⫾12.7 vs
85.8⫾13.2 mm Hg, P⫽0.04, for the noninfarction and infarction groups, respectively). Thus, ORx and PtiO2 values from
days 5 and 6 were entered into the analysis; however, CPP
was not considered, because higher CPP levels are not related
to symptomatic vasospasm according to our current understanding of the pathophysiological mechanisms of the disease. In the final model, ORx carried a predictive value on the
occurrence of delayed cerebral infarction after SAH
(P⫽0.003), whereas PtiO2 did not (P⫽0.08). Table 3 displays
the probability of infarction for ORx thresholds of ⬍0.25 and
⬎0.4. These values were chosen after data analysis, with the
intention to provide thresholds for easy clinical interpretation.
Only 42 patients from the noninfarction group and 19 patients
from the infarction group could be entered into the logisticregression analysis, as they were monitored during the time
interval of days 5 and 6.
Relation Between Location of PtiO2 Probe and
Territory of Delayed Infarction
The position of the PtiO2 probe in relation to the location of
delayed cerebral infarction is shown in Table 4. No signifi-
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Time course of ORx, CPP, ICP, and PtiO2 after
SAH. The black line indicates the noninfarction
group, and the gray line represents the infarction
group. Given values are the mean; error bars represent 95% CIs of the mean. P values from the
Mann–Whitney U test for each day of monitoring
are given at the bottom of each graph.
cant differences in ORx were seen between probes located in
a later-infarcted area and probes not so located.
Discussion
This study demonstrated differences in cerebrovascular autoregulation, as measured by the index of PtiO2 pressure
reactivity ORx between patients who developed delayed
cerebral infarction after SAH and those who did not. The
intrinsic capacity of the brain to control cerebral blood flow
relatively independently of CPP was significantly diminished
in infarcted patients. This finding confirms the pathophysiological model that impairment of autoregulation plays a role
in the development of critical ischemia after SAH. ORx was
equally high, ⬇0.4, during the first days after the ictus,
Jaeger et al
Autoregulation and Delayed Infarction After SAH
TABLE 3. Likelihood of Delayed Infarction Among Suggested
Thresholds of ORx From Days 5 and 6
Noninfarction
Group
(n⫽42)
Infarction
Group
(n⫽19)
ORx ⬍0.25
21
2
9
0.25 ⬍ORx ⬍0.40
14
6
30
7
11
61
Variable
ORx ⬎0.40
Percentage With
Delayed
Infarction
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irrespective of future infarction, indicating the immediate
impact of the bleeding on the cerebral vasculature. In the
further course of the disease, patients with improving
autoregulation rarely experienced delayed infarction,
whereas a continuing loss of autoregulation was closely
associated with this devastating event.
The results of the study showed that continuous monitoring
of ORx provides early information on the patient’s individual
risk for delayed infarction. This is of major interest, because
in our cohort of predominantly poor-grade SAH patients, this
information was unavailable from other methods, either
clinically or from monitoring. Also, TCD did not differentiate
between the groups, but the limited frequency of TCD
examinations (only every 2 to 4 days) might have attenuated
the significance of this finding. However, especially in
ventilated and sedated patients, the diagnosis of symptomatic
delayed ischemia remains challenging, because a reliable
neurological assessment is impossible and appropriate timing
of invasive therapeutic measures that are not risk-free, such as
aggressive hypertensive/hypervolemic/hemodilutional therapy or angioplasty, cannot be made. Monitoring of ORx at
the bedside of ventilated and sedated patients may thus
allow clinicians to identify those with a high probability of
infarction, for whom such invasive therapeutic measures
may appear justified. On the other hand, when ORx is low,
therapy can be maintained at a more restrained level.
Despite the promising results of the logistic-regression
analysis in predicting the occurrence of delayed infarction,
we have been unable to establish a certain threshold for ORx
above which infarction definitely occurred or below which
infarction could be ruled out. It appeared that with deteriorating ORx, the risk of infarction greatly increased, but high
ORx values did not fully explain all of the observed new
hypodensities. As demonstrated in Table 3, a subset of
patients still experienced new infarctions, although their ORx
values at days 5 and 6 were ⬍0.25, indicating relatively intact
autoregulation. In these patients, vasospasm at that time may
not have been fully developed, and later progression of
vasospasm may have then led to a further loss of autoreguTABLE 4. ORx Obtained From PtiO2 Probes Not Located in the
Territory of Delayed Cerebral Infarction vs PtiO2 Probes Located
in the Territory of Delayed Cerebral Infarction
Variable
ORx
Probe Not in
Infarction (n⫽11)
Probe in
Infarction (n⫽9)
P
0.42⫾0.06
0.45⫾0.12
0.79
Values are mean⫾SD.
P for Mann–Whitney U test.
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lation.5 Also, disturbances of autoregulation in the cortical
gray matter, which might play a dominant role in perfusion
impairment after SAH, might have been overlooked and not
appropriately displayed by our PtiO2 monitoring technique,
which assesses for this surrogate of cerebral blood flow in the
white matter.
PtiO2 probes were usually placed in tissue considered to
be at risk for delayed ischemia, but the distribution of
infarcts did vary. Interestingly, our results suggest that the
PtiO2 probes do not necessarily need to be in an area of
future infarction to detect a critical impairment of autoregulation. This finding supports the concept that autoregulation is globally impaired after SAH, in which case a
local monitoring technique may be sufficient. However,
interhemispheric differences in autoregulation have been
demonstrated after SAH.5 Therefore, the potential influence of probe location on our results should be kept in
mind, and the important issue of where to place the probe
needs to be evaluated in further studies with larger patient
numbers.
Monitoring of PtiO2 alone did not reveal obvious differences between the noninfarction group and infarction group.
This physiological variable showed a trend toward lower
values in infarcted patients, indicating reduced levels of
cerebral blood flow, but a clear statistical conclusion could
not be drawn and PtiO2 did not carry an early predictive value
for delayed infarction. Although previous studies have questioned the value of PtiO2 in predicting survival after
SAH,16 we think that this variable also deserves further
evaluation in larger patients groups regarding its relation
to delayed infarction.
In summary, continuous monitoring of ORx allows detection of impaired autoregulation after SAH. Persistent autoregulatory failure is independently associated with the
occurrence of delayed cerebral infarction and seems to be
an important cofactor in addition to vasospasm itself.
Acknowledgments
The authors thankfully acknowledge the statistical assistance of Dr
Dirk Hasenclever, Institute for Medical Informatics, Statistics and
Epidemiology, University of Leipzig, Germany.
Disclosures
None.
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Continuous Monitoring of Cerebrovascular Autoregulation After Subarachnoid
Hemorrhage by Brain Tissue Oxygen Pressure Reactivity and Its Relation to Delayed
Cerebral Infarction
Matthias Jaeger, Martin U. Schuhmann, Martin Soehle, Christoph Nagel and Jürgen
Meixensberger
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Stroke. 2007;38:981-986; originally published online February 1, 2007;
doi: 10.1161/01.STR.0000257964.65743.99
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 2007 American Heart Association, Inc. All rights reserved.
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