RESEARCH—HUMAN—CLINICAL STUDIES
RESEARCH—HUMAN—CLINICAL STUDIES

Detection of Cerebral Vasospasm Following
Aneurysmal Subarachnoid Hemorrhage Using
Motor Evoked Potentials
Stefan Grossauer, MD, MBA*‡
Katharina Koeck, MD, MBA*‡
Jakob Kraschl, MD‡
Oliver Olipitz, BA§
Klaus A. Hausegger, MD,
PhD¶
Giles H. Vince, MD, PhD‡
‡Department of Neurosurgery, General
Hospital of Klagenfurt, Klagenfurt, Austria;
§Institute of Human Biology, Karl-Franzens
University Graz, Graz, Austria; ¶Department
of Interventional and Diagnostic Radiology,
General Hospital of Klagenfurt, Klagenfurt,
Austria
*These authors contributed equally to
this article.
Correspondence:
Stefan Grossauer, MD, MBA,
Department of Neurological Surgery,
Helen Diller Cancer Research Building,
University of California San Francisco,
1450 Third St,
Box 0520,
Rm HD482 (4th floor),
San Francisco, CA 94158-2197.
E-mail: stefan.grossauer@ucsf.edu
Received, March 21, 2015.
Accepted, August 20, 2015.
Published Online, September 29, 2015.
Copyright © 2015 by the
Congress of Neurological Surgeons.

BACKGROUND: Early detection of vasospasm (VS) following aneurysmal subarachnoid
hemorrhage (aSAH) is vital to trigger therapy and to prevent infarction and subsequent
permanent neurological deficit. Although motor evoked potentials (MEPs) are a wellestablished method for intraoperative detection of cerebral VS and cerebral ischemia
during aneurysm surgery, there are no studies investigating the diagnostic value of
MEPs for detecting delayed VS following aSAH in an intensive care unit.
OBJECTIVE: A prospective study was conceived to assess the diagnostic accuracy of
MEPs in comparison with digital subtraction angiography.
METHODS: MEP threshold changes were determined in patients both with and without angiographic VS following high-grade aSAHs. Sensitivity, specificity, and the positive and negative predictive values of significant MEP threshold increases, which
indicate angiographic VS, were calculated.
RESULTS: In all patients experiencing VS of the arteries supplying cerebral motor areas,
a minimal MEP threshold increase of 50 mA (mean 66.25 mA) was observed, whereas
a maximum MEP threshold increase of 30 mA was observed in patients without VS.
Therefore, an increase from a baseline of $50 mA was considered significant and resulted in a sensitivity of 0.83, a specificity of 0.92, a positive predictive value of 0.83, and
a negative predictive value of 0.92.
CONCLUSION: VS following aSAH can be detected accurately by using MEPs. MEPs are
a feasible bedside tool for online VS detection in an intensive care unit and, therefore,
may complement existing diagnostic tools.
KEY WORDS: Intracranial aneurysm, Motor evoked potentials, Neurophysiological monitoring, Subarachnoid
hemorrhage, Vasospasm
Neurosurgery 78:265–273, 2016

DOI: 10.1227/NEU.0000000000001040

V

asospasm (VS) following aneurysmal subarachnoid hemorrhage (aSAH) is a severe
condition associated with high morbidity
and mortality. Early detection is vital to trigger
therapy and to prevent infarction and subsequent
permanent neurological deficit.1 Many methods,
including neurological examination, digital
subtraction angiography (DSA), perfusion
computed tomography (PCT), and transcranial
Doppler (TCD) sonography,2-7 are used to
ABBREVIATIONS: aSAH, aneurysmal subarachnoid
hemorrhage; DSA, digital subtraction angiography;
ICU, intensive care unit; MEP, motor evoked
potential; PCT, perfusion computed tomography;
TCD, transcranial Doppler; VS, vasospasm

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detect VS. Although neurological examination
has proven to be a simple bedside method with
high diagnostic sensitivity, many patients are
not amenable to this examination because they
require anesthesia.8 Unfortunately, this subgroup often exhibits pronounced aSAH and,
therefore, carries the highest risk for sustaining
delayed cerebral VS.9 Although cerebral angiography is considered the gold standard, TCD
remains the best-established and most widely
used bedside method for anesthetized patients.
Unfortunately, this method offers only comparatively low sensitivity and specificity in detecting
angiographic VS.8
Although electrophysiological methods are
routinely used at intensive care units (ICUs) on
severely brain-injured patients,10-14 no study yet

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TABLE 1. Inclusion and Exclusion Criteriaa
Inclusion Criteria

a

Exclusion Criteria

aSAH Fisher grade III and IV
Intracranial aneurysm verified by cerebral angiography
Clinical condition requires deep anesthesia at the time of
baseline and control MEP recording

Conscious patients
Intracranial pressure $20 mm Hg as verified with ICP probe
Other clinical condition that does not allow MEP recording as decided by the
responsible neurosurgeon (eg, increased arterial blood pressure or increased heart
rate following transcranial electric stimulation)

Absence of vasospasm at the time of baseline MEP
recording as demonstrated on cerebral angiography
Time window #4 h between angiography and start of
MEP recording
Presence or absence of vasospasm verified by cerebral
angiography at the time of control MEP recording
Age $18 y

Contradictory evaluation results of cerebral angiography by the vascular
neurosurgeon and neuroradiologist
Patient requiring barbiturates for anesthesia (eg, sodium pentothal)

aSAH, aneurysmal subarachnoid hemorrhage; ICP, intracranial pressure; MEP, motor evoked potentials.

has evaluated the diagnostic accuracy and feasibility of motor
evoked potentials (MEPs) in detecting cerebral VS. The fact that
the motor cortex is the cerebral structure most sensitive to
cerebral ischemia can be exploited when using MEPs to detect
impending cerebral ischemia when it is still potentially reversible.
Therefore, MEPs represent a well-established method for intraoperative detection of cerebral VS and cerebral ischemia during
aneurysm surgery, and the literature demonstrates that MEPs are
a reliable tool for online, minimally invasive detection of cerebral
ischemia and VS during aneurysm surgery.15-26 Diagnostic
accuracy of transcranial magnetic MEPs was investigated in
a rabbit VS model in which VS following aSAH resulted in
a significant increase of MEP latencies. Therefore, it was
concluded that MEPs might be valuable in VS diagnostics.27
To the authors’ knowledge, there are no studies investigating the
diagnostic accuracy and feasibility of MEPs in detecting delayed
cerebral VS following aSAH in humans. Accordingly, we
designed a prospective study investigating the diagnostic accuracy
of MEPs in detecting angiographic cerebral VS in humans and
evaluating its feasibility in an ICU.

METHODS
Selecting Patients
The study included all patients admitted to the neurosurgical ICU of
the academic hospital of Klagenfurt for aSAH from April 1 to July 30,
2014, whose clinical parameters were consistent with all inclusion
criteria and who had no exclusion criteria. The local institutional review
board approved the study. Table 1 summarizes the inclusion and
exclusion criteria. In brief, those included were adult patients
sustaining high-grade aSAHs as demonstrated by computed tomography (Fisher grade III-IV), whose clinical condition required deep
anesthesia at the time of baseline and control MEP recordings, and who
had undergone DSA at least twice. The study excluded conscious
patients and those exhibiting increased intracranial pressure verified by
an intracranial pressure probe.

266 | VOLUME 78 | NUMBER 2 | FEBRUARY 2016

Recording MEPs
All MEP recordings were performed by 2 neurosurgeons with extensive
experience and training in electroneurophysiology (S.G., J.K.). Baseline
MEPs were recorded on the day of admission and aneurysm rupture. On
the same day, a baseline DSA was performed to rule out VS at the time of
recording baseline MEPs. According to DSA results, all patients
underwent occlusion of the ruptured aneurysm by endovascular coiling
or microsurgical clipping within 48 hours after admission. In addition,
control MEPs were recorded within 4 hours before a second DSA was
performed, 1 to 17 days after baseline DSA. Reasons for cerebral control
angiography included suspected VS as indicated by TCD and postclipping
or postcoiling routine angiography. Throughout the MEP recording
procedure, the analog-sedation required by patients’ clinical condition
was maintained with a customized combination of propofol, remifentanyl, midazolam, piritramide, and esketamine hydrochloride. Needle
electrodes were inserted subdermally into the target muscles and
connected to the amplifiers of the head box unit of the intraoperative
electrophysiology device. Corkscrew electrodes were placed subcutaneously on the scalp over the stimulating sites according to the
international 10-20 system and connected to the stimulation unit.
Table 2 lists stimulation and recording parameters.
Then, the biosignal window was checked for artifacts. If artifacts were
encountered, recording conditions were improved by ensuring proper
needle placement or, in the case of electrical interference, relocating
electrical devices. For tracheal tube safety, an oropharyngeal tube was
placed in each patient. Transcranial stimulation began at an intensity of
30 mA and increased in 5-mA steps until stable MEPs could be elicited
in all recording muscles of the upper and lower extremities bilaterally, or
until the maximum stimulus intensity of 220 mA was reached. Initially,
the stimulation sites were 1 electrode placed at C3 as the anode and 1 at
C4 as the cathode. The threshold required for each muscle was noted in
a prepared case report form. Threshold was defined as the lowest
stimulus intensity required for each target muscle to elicit clearly
identifiable, repeatable MEP signals on the device screen at a display
sensitivity of 200 mV. Then, the polarity of the stimulation electrodes
was switched and the procedure repeated with anodal stimulation over
C4 and cathodal stimulation over C3. If MEPs could not be elicited
with stimulation electrodes placed in either of these arrangements,

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TABLE 2. Summary of Stimulation and Recording Parametersa
Parameter
Stimulation sites
Number and form
of stimuli
Stimulus lengths
Stimulus intensity
Interstimulus
interval
Recording muscles
Stimulus frequency
Display sensitivity
Number of
averaged signals
Low pass filter
High pass filter

Value
C3/4; C4/3; Cz/Fz
Train of five
500 ms
30-220 mA
4 ms
ABP bilateral, forearm extensors bilateral,
TA bilateral, ABH bilateral
0.5 Hz
200 mV
2
50 Hz
3000 Hz

a

ABH, abductor hallucis muscle; ABP, abductor pollicis brevis muscle; TA, tibialis
anterior muscle.

electrode placement was changed to provide anodal stimulation at Cz
and cathodal stimulation at Fz and the recording procedure repeated as
described above.

Defining Vasospasm and Evaluating
Cerebral Angiography
All patients included in the study underwent DSA at least twice: once
on the day of baseline MEP recording and again on the day of control
MEP recording. Reasons to forward patients to DSA included initial
diagnostic evaluation, flow velocity of TCD that indicated cerebral VS,
and postclipping or postcoiling control. Angiographic VS was defined as
more than 30% narrowing of the diameter of a vessel trunk on 2dimensional DSA and a significant subsequent delay of contrast flow distal
to the spastic segment. DSA images were stored digitally for post hoc
analysis and were reviewed and evaluated for the presence or absence of
cerebral VS independently by a neuroradiologist and a vascular neurosurgeon unaware of MEP recording results. If VS could be demonstrated
on DSA, the spastic artery or arteries were named in the case report form.
In the case of contradictory DSA evaluation results by the neuroradiologist
and neurosurgeon, the patient was excluded from analysis.

Evaluating MEP Results and Proposing
Diagnostic Criteria
As shown by intraoperative MEP studies, either the MEP threshold
increases significantly or MEPs cannot be elicited at all in muscles
innervated by vasospastic and/or ischemic motor cortex.22,24 Therefore, it
is to be expected that VS of the medial cerebral artery results in an
increased MEP threshold of the contralateral upper extremity muscles,
whereas VS of the anterior cerebral artery results in a MEP threshold
increase in the contralateral lower extremity muscles. VS of the vertebral
arteries or of the basilar artery may result in a threshold increase of lower
and/or upper extremity muscles, owing to their vascular supply of the
brainstem, whereas VS of the posterior cerebral artery may result in no
threshold increase at all, owing to supplying nonmotor areas of the brain.

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FIGURE 1. Graph showing the mean motor evoked potential (MEP) thresholds
and its standard deviations for extremity muscles in patients with aneurysmal
subarachnoid hemorrhage. Black dots represent the mean MEP thresholds in
absence of angiographic vasospasm. Black squares represent the mean MEP
thresholds during angiographic vasospasm. Black triangles represent MEPs that
could not be elicited during angiographic vasospasm with a maximum intensity of
220 mA. ABH, abductor hallucis muscle; APB, abductor pollicis muscle; Ext.,
extensor; N/E, MEPs could not be elicited at all with maximum intensity of
220 mA; Tib., tibialis anterior muscle; VS, vasospasm.

To establish suitable diagnostic criteria to indicate VS, the study
calculated and compared mean MEP thresholds and their standard
deviations of muscles innervated by vasospastic and nonvasospastic
cerebral motor areas. These results defined a significant threshold increase
and tested it for its diagnostic accuracy by calculating sensitivity,
specificity, and positive and negative predictive values.

RESULTS
Baseline and control MEP recordings were performed on 17
patients. One patient was excluded from further analysis because
of pronounced movement artifacts at the time of the control MEP
recording. In the remaining 16 patients, MEP recordings were
uneventful and took between 16 and 31 minutes. Five of 16
patients exhibited angiographic VS on days 6 to 17 following
aSAH, whereas, 1 to 17 days following aSAH, VS was ruled out by
DSA in 11 patients. At baseline recording, mean thresholds for
left-sided extremity muscles were 67.6 mA for extensor digitorum
muscle, 69.2 mA for abductor pollicis brevis muscle, 103.0 mA for
tibialis anterior muscle, and 110.8 mA for abductor hallucis
muscle. Mean threshold values for right-sided muscles were 70.2
mA for extensor digitorum muscle, 68.5 mA for abductor pollicis
brevis muscle, 100.4 mA for tibialis anterior muscle, and 105.9
mA for abductor hallucis muscle. Figure 1 lists these results.
Table 3 shows MEP thresholds for 5 patients before and during
angiographically verified VS. In all patients exhibiting VS of
arteries that supply cerebral motor areas (cases 1-4), a minimum
threshold increase of 50 mA and a mean increase of 66.25 mA
were observed. In cases 2 and 3, MEPs could not be elicited in
some contralateral muscles at the time of VS. Case 5, with VS

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GROSSAUER ET AL

TABLE 3. Motor Evoked Potential Thresholds of 5 Patients in Absence and During Angiographically Verified Vasospasma
Case
Number
1

Vasospastic Artery

Maximum
Narrowing of
Vessel Diameter (%)

Muscle

ACM right

60

Ext. left
ABP left

2

ACA right

40

TA left

ABH left

3

ICA left

70

Ext. right
ABP right
TA right

ABH right

4

ACM left

80

Ext. right
ABP right

5

PCA right

60

Ext. left
ABP left
TA left

ABH left

Ext. right
ABP right
TA right

ABH right

Stim. Site

MEP Threshold
at Baseline (mA)

MEP Threshold
During
Vasospasm (mA)

C3/4
C4/3
C3/4
C4/3
C3/4
C4/3
Cz/Fz
C3/4
C4/3
Cz/Fz
C3/4
C4/3
C3/4
C4/3
C3/4
C4/3
Cz/Fz
C3/4
C4/3
Cz/Fz
C3/4
C4/3
C3/4
C4/3
C3/4
C4/3
C3/4
C4/3
C3/4
C4/3
Cz/Fz
C3/4
C4/3
Cz/Fz
C3/4
C4/3
C3/4
C4/3
C3/4
C4/3
Cz/Fz
C3/4
C4/3
Cz/Fz

50
80
50
75
170
140
N/A
140
150
N/A
60
70
60
70
110
100
N/A
100
100
N/A
60
65
50
50
60
65
60
65
90
100
N/A
130
130
N/A
70
65
60
65
90
100
N/A
130
120
N/A

130
130
130
130
N/E
N/E
N/E
N/E
N/E
N/E
140
140
120
150
N/E
N/E
N/E
N/E
N/E
N/E
120
115
110
120
90
95
90
95
125
135
N/A
120
120
N/A
80
80
80
85
110
110
N/A
110
125
N/A

a

ABP, abductor pollicis muscle; ABH, abductor hallucis muscle; ACA, anterior cerebral artery; ACM, medial cerebral artery; Ext., forearm extensor muscle; ICA, internal carotid artery;
N/A, not applicable; N/E, MEPs could not be elicited with a maximum intensity of 220 mA; PCA, posterior cerebral artery; Stim., Site Stimulation site; TA, tibialis anterior muscle.

restricted to the right posterior cerebral artery, exhibited
a maximum threshold increase of 35 mA and a mean increase
of 15.63 mA. A mean threshold increase of 14.47 mA (range 0‒
30 mA) from baseline to control was calculated for 11 patients
without VS. Therefore, an increase in MEP threshold of $50 mA
(“50 or more rule”) from baseline to control was defined as

268 | VOLUME 78 | NUMBER 2 | FEBRUARY 2016

suggestive of VS and, accordingly, tested for diagnostic accuracy
by comparing maximum threshold increase from baseline to
control in each patient. There were 5 true-positive, 11 truenegative, 1 false-positive, and 1 false-negative results. Sensitivity,
specificity, and positive and negative predictive values of the “50 or
more rule” were calculated and are summarized in Tables 4 and 5.

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MEPS AND VASOSPASM DETECTION

a

TABLE 4. Contingency Table Illustrating the MEP Test Results of
the Applied “50 or More Rule”a

TABLE 5. The Diagnostic Accuracy of MEPs in Detection of VS
Following aSAH Compared With DSAa

Test Result

True: Vasospasm

False: No Vasospasm

Total

Parameter

Positive
Negative
Total

4
1
5

1
10
11

5
11
16

Sensitivity
Specificity
Positive predictive value
Negative predictive value

MEP, motor evoked potentials.

Value (in %)
83.0
92.0
83.0
92.0

a

aSAH, aneurysmal subarachnoid hemorrhage; DSA, digital subtraction
angiography; MEP, motor evoked potential; VS, vasospasm.

One false-positive result was obtained in a patient whose
posterior communicating artery aneurysm was clipped and in
whom an inadvertent occlusion of the anterior choroidal artery
led to an infarction in the early postoperative period. In this
patient, significant threshold increases were encountered for all
contralateral upper and lower extremity muscles. Because an
inadvertent operative occlusion rather than VS led to significant
threshold increases in this patient, the test result was considered
to be a false positive. One false-negative result was obtained in
a patient with VS restricted to the right posterior cerebral artery.
In this case, a maximum increase in threshold of only 35 mA
was observed and, therefore, considered to be a false negative.

ILLUSTRATIVE CASE
A 53-year-old woman was admitted to our service after the
sudden onset of severe headaches, nuchal rigidity, and confusion
3 hours earlier. A cranial computed tomography revealed a basal
subarachnoid hemorrhage and intraventricular blood with mild
hydrocephalus. Computed tomography angiography (CTA)
revealed a large saccular aneurysm originating from the anterior
communicating artery. The patient was transferred to the ICU,
anesthesia was induced, and external ventricular drainage
placed. Then, the patient was forwarded to the angiography
operating room to obtain a DSA (Figure 2B). An interventional
radiologist and a vascular neurosurgeon reviewed the DSA
images and decided to obliterate the aneurysm by endovascular
coiling, which was done on the same day without complications
(Figure 2D). During the entire angiography and coiling
procedure, no VS was encountered at any time, so the patient
underwent baseline MEP recording, as described above,
immediately after returning to the ICU. Table 6 lists baseline
MEP thresholds.
On day 9 after aSAH, TCD flow velocities for the right-sided
anterior and medial cerebral arteries showed a considerable
increase of 55 cm/s over values on the day before. MEP
thresholds were obtained, as shown in Table 6, and the patient
was forwarded to DSA, which revealed a significant spasm of
the right-sided M1 (Figure 2B) compared with the initial DSA
(Figure 2A) and no spasm of any other artery. Chemical
spasmolysis was performed immediately by using intra-arterial
administration of nimodipine, which led to a complete
normalization of the diameter and blood flow in the M1.

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DISCUSSION
VS Diagnostics
A variety of methods are well established in daily neurosurgical
practice, including TCD, CTA, DSA, and PCT.2,4-6,8,28-30
Neurological assessment at frequent intervals has been found
to be the most sensitive, specific parameter for cerebral VS
detection,8 but patients requiring anesthesia or those with
impaired conscious states may not be amenable to detailed
neurological assessment. Unfortunately, this subgroup often
harbors pronounced aSAH and, therefore, carries the highest
risk of sustaining VS.9 TCD is a commonly used, noninvasive,
inexpensive bedside method in daily ICU practice that yields high
specificity but comparatively low sensitivity in detecting VS. In
addition, TCD results are highly operator dependent and have
been shown to predict secondary infarction poorly compared
with DSA. Furthermore, measurement of TCD is limited by the
presence of an appropriate “ultrasound window,” which must be
permeable to ultrasound waves. In TCD, a variety of factors not
attributable to vessel diameter can contribute to elevating flow
velocities, and only large-vessel spasms, not peripheral VSs, can
be detected.3,4 CTA and PCT have been proven to detect VS
with high sensitivity and specificity and, therefore, can be used as
monitoring tools by performing scans regularly in addition to
daily TCD.8 The significance of CTAs is limited by beamhardening artifacts from clips and coils and in evaluating posterior
fossa arteries. As with nearly all imaging methods, CTA and PCT
require the patient to be transferred to the imaging unit, which is
costly and has been shown to put patients at increased medical
risk.31 Because of these limitations and the exposure of patients to
radiation, CTA and PCT are unlikely to be used daily, therefore,
increasing the chance that VS is missed or detected too late to
prevent delayed ischemic neurological deficit. DSA is considered
the gold standard for VS detection because of its ability to
demonstrate cerebral VS anatomically with high accuracy and
because it offers the opportunity to perform balloon angioplasty
and chemical spasmolysis immediately. Often, DSA is performed
when clinical VS is suspected. Studies have reported nearly 100%
sensitivity and specificity for 2-dimensional DSA in VS
detection.6 Nevertheless, DSA carries considerable risk of
neurological complications32,33 and exposes patients to comparatively high doses of radiation and contrast medium.29,30

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GROSSAUER ET AL

FIGURE 2. DSA of the left and right ICA of a patient harboring a large ruptured Acom aneurysm before (B) and after (D)
endovascular embolization. DSA of the right ICA at the day of aneurysm rupture (A), and on day 9 following rupture, exhibiting
severe vasospasm (C, white arrow) of the M1 segment. Acom, anterior communicating artery; DSA, digital subtraction angiography; ICA, internal carotid artery.

MEP and Detecting Cerebral Ischemia
The present study was inspired by the idea that the ideal method
for detecting VS would be a minimally invasive, bedside,
inexpensive method providing high diagnostic accuracy, repeatable anytime, and yielding information early enough to provide
adequate therapy and prevent cerebral infarction. Many studies
have proven that this is the case when using MEPs to detect
impending cerebral ischemia during aneurysm surgery.15,16,19,20,22-26,34,35 Because various surgical maneuvers,
including VS, temporary clipping, retraction, dissection, and
vessel occlusion, may disturb focal circulation, a sensitive, specific
method is needed to alert surgeons in a timely way during
surgery. Therefore, transcranial or direct cortical stimulation of
the primary motor cortex is used to produce depolarized action
potentials that can be recorded at short intervals from muscles
during aneurysm surgery.15 Given that, it seemed worthwhile to

270 | VOLUME 78 | NUMBER 2 | FEBRUARY 2016

adopt this approach and evaluate MEPs for their diagnostic
accuracy in detecting delayed VS following aSAH. For their use
in an ICU, we slightly modified MEP recording parameters
compared with parameters used to monitor intraoperatively
during aneurysm surgery. To minimize movement artifacts, we
used the threshold technique, gradually increasing stimulus
intensity in 5-mA steps, starting as low as 30 mA. With that
technique, we were able to determine the minimal stimulus
intensity needed to elicit MEPs for each target muscle separately,
which is defined as its threshold. Conversely, for intraoperative
monitoring, a stimulus intensity strong enough to elicit MEPs in
all target muscles is selected, and, therefore, MEP amplitudes
and, to a lesser extent, MEP latencies are evaluated for significant
changes. Clearly, this is a less time-consuming approach
compared with the threshold method described above, and time
is of paramount importance in intraoperative monitoring, which

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TABLE 6. MEP Thresholds of a Patient at Day of Aneurysm Rupture
and on the Day of Exhibiting Angiographic VS of the Right M1a

Muscle
Ext. left
ABP left
TA left
ABH
Ext. right
ABP right
TA right
ABH right

Stimulation
Site

MEP
Threshold at
Baseline

MEP Threshold during
Right MCA Vasospasm

C3/C4
C4/C3
C3/C4
C4/C3
C3/C4
C4/C3
C3/C4
C4/C3
C3/C4
C4/C3
C3/C4
C4/C3
C3/C4
C4/C3
C3/C4
C4/C3

50
80
50
75
55
65
50
130
50
65
50
50
50
130
50
70

130
130
130
130
75
80
70
130
60
75
80
80
60
160
75
75

CONCLUSION

a

ABH, abductor hallucis muscle; ABP, abductor pollicis muscle; Ext., forearm
extensor muscle; MCA, medial cerebral artery; MEP, Motor evoked potentials; TA,
tibialis anterior muscle; VS, Vasospasm.

must interfere as little as possible with surgery. We demonstrated
that MEP recording with the threshold technique could be
completed bedside in 16 to 31 minutes in an ICU, which
compares favorably to all methods requiring intrahospital patient
transport.
Limitations
This method and the present study have several limitations.
From the methodological perspective, MEPs have limited diagnostic value because they enable detection of VS only in vascular
territories that supply the motor cortex or the corticospinal tracts,
missing any VS restricted to nonmotor areas. Although the most
important cerebrovascular territories may be covered by MEP
monitoring, 1 patient in the study exhibited VS limited to the

TABLE 7. Diagnostic Accuracy of Different Methods Compared
With Digital Subtraction Angiographya,b
Method
Neurological assessment
TCD
Perfusion CT
MEPs
a

Sensitivity

Specificity

PPV

NPV

1.00
0.77
0.93
0.80

0.33
0.44
0.27
0.91

0.69
0.73
0.71
0.80

1.00
0.62
0.67
0.91

MEP, motor evoked potentials; NPV, negative predictive value; Perfusion CT,
perfusion computed tomography; PPV, positive predictive value; TCD, transcranial
Doppler sonography.
b
Adapted from Kunze et al.8

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posterior cerebral artery, which insignificantly affected MEP
thresholds. Accordingly, relying on MEPs alone would have
missed VS in this patient. Another limitation is that MEP
recordings as presented here can be used only in anesthetized
patients, because conscious patients could not tolerate the needle
electrodes and high stimulus intensities. In contrast, it is likely that
conscious patients are amenable to neurological assessment, which
has been proven to detect VS with supreme sensitivity.8 Given
that, these patients do not require another, more invasive bedside
method. Table 7 summarizes the results of a study by Kunze et al8
in which the authors prospectively evaluated the diagnostic
accuracy of neurological assessment, TCD, and PCT in VS
detection compared with DSA. As Table 7 shows, when MEPs
were compared with TCD, it provided at least comparable
sensitivity and superior specificity. Because of the limitations of
both MEPs and TCD, they may complement each other to
reduce the overall rate of false-negative results.

MEPs can detect VS following aSAH with high accuracy, are
a feasible bedside tool for online VS detection in an ICU, and,
therefore, may complement existing diagnostic tools. MEPs may
contribute to a decreased rate of cerebral ischemia following VS.
Future technical refinement may include increasing the practicality of MEP recording for this indication. Further studies seem
warranted to address the input of this technique on clinical
outcomes in patients sustaining aSAH.
Disclosure
The authors have no personal, financial, or institutional interest in any of the
drugs, materials, or devices described in this article.

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COMMENT

V

asospasm (VS) and its deleterious effects following aneurysmal subarachnoid hemorrhage (SAH) have been extensively documented.1
Given the delayed onset of vasospasm and the perception that it is
a secondary event following SAH, immense effort has been made into
studying the risk factors and predictors of VS. The majority of these
studies continue to reinforce the observation that (a) the occurrence and
(b) the severity of cerebral vasospasm relate to the quantum of blood in
the subarachnoid spaces.2-4 The gold standard for diagnosis of cerebral
vasospasm has been digital subtraction angiography. The burden of clot
is most evident on CT imaging and traditionally has been sufficient to
raise the alarm as to which patients tend to have the potential for
vasospasm.
The issue however gets more complicated from there on. Not all
patients with angiographic vasospasm are clinically symptomatic from
it, while at the same time clinical symptoms that reverse with the
increase in cerebral perfusion from raising systemic blood pressure is
sufficient to diagnose vasospasm without imaging (other causes being
ruled out). Therefore, a prudent management strategy would incorporate a stance between aggressive angiography “for all” and reliance on
clinical examination only, to effectively predict and diagnose vasospasm and decide further on treatment. At a practical level, present
modalities are either directed toward imaging definition of spasm
(transcranial Doppler [TCD], CT angiography [CTA], digital subtraction angiography [DSA]) or the pathological effects of spasm on
brain function (electroencephalogram [EEG], somatosensory evoked
potential [SSEP], brain tissue oxygen tension, cerebrospinal fluid
[CSF] markers of inflammation).
In the present study, the authors describe an interesting prospectively
designed study in patients with high-grade SAH in which they noted the
extent of correlation of changes in motor evoked potentials (MEPs) with
angiographic vasospasm. They mention that MEP variations in the form
of increase in threshold values and/or decrease in amplitudes correlate with
angiographic spasm with very high sensitivity, specificity, and predictive
values. The pathophysiology behind the observation is intuitive and the
authors are successful in corroborating a downstream physiological effect
of cortical ischemia to the causative factor, namely cerebral vasospasm.
However, the exclusion of conscious patients (irrespective of the burden of
subarachnoid blood on the admission CT scan) is a missed opportunity of
studying how these individuals are different from patients with similar clot
burden. Indeed, there is the obvious difficulty of subjecting a conscious
patient to this rather painful procedure, especially in the context of a study.
The other drawback of the study is the lack of demonstration of consistent
improvement of MEPs with vasodilator therapy. The inability to detect
distal small-vessel spasm is a significant limitation, too. The data are
ultimately not robust enough to convince vascular neurosurgeons to
supplant or supplement established diagnostic modalities that most
commonly involve vascular imaging.

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MEPS AND VASOSPASM DETECTION

Changes in MEP parameters may indeed be correlated with VS, but
this technique still needs substantial investment in terms of time and
personnel. In addition, very much like TCD, recording MEPs is an
intentionally triggered event in contrast to detecting seizure activity by
continuous EEG monitoring, for example. The practical day-to-day
utility of MEP monitoring for physicians who manage patients with
SAH is uncertain. An apt analogy of a reliable and proven monitoring
technique in acute vascular care is the combination of electrocardiographic telemetry monitoring and repeated cardiac enzyme levels in
patients with acute coronary syndromes.5 The neurovascular community is in desperate need of a similar protocol for managing vasospasm
in SAH.
Mithun G. Sattur
Tariq K. Halasa
Bernard R. Bendok
Phoenix, Arizona

NEUROSURGERY

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presenting with aneurysmal subarachnoid hemorrhage: a review. Neurosurgery.
2005;56(4):633–654.
3. Abla AA, Wilson DA, Williamson RW, et al. The relationship between ruptured
aneurysm location, subarachnoid hemorrhage clot thickness, and incidence of
radiographic or symptomatic vasospasm in patients enrolled in a prospective
randomized controlled trial. J Neurosurg. 2014;120(2):391–397.
4. Yin L, Ma CY, Li ZK, Wang DD, Bai CM. Predictors analysis of symptomatic
cerebral vasospasm after subarachnoid hemorrhage. Acta Neurochir Suppl. 2011;110
(pt 2):175–178.
5. Antman EM, Anbe DT, Armstrong PW, et al; American College of Cardiology;
American Heart Association; Canadian Cardiovascular Society. ACC/AHA guidelines for the management of patients with ST-elevation myocardial infarction—
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the 1999 guidelines for the management of patients with acute myocardial
infarction). J Am Coll Cardiol. 2004;44(3):671–719.

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