Journal of Clinical Monitoring and Computing

https://doi.org/10.1007/s10877-020-00621-9

ORIGINAL RESEARCH

Anaesthesia and multimodality intraoperative neuromonitoring

in carotid endarterectomy. Chronological evolution and effects
on intraoperative neurophysiology
Ana Mirallave Pescador1   · Pedro Javier Pérez Lorensu2 · Ángel Saponaro González2 · Beneharo Darias Delbey3 ·
José Luis Pérez Burkhardt4 · Roberto Ucelay Gómez4 · Enrique Francisco González Tabares4 · Zeina Ibrahim Achi4 ·
Christian Salvador Guerrero Ramírez4 · Carol Elizabeth Padrón Encalada4 · Alejandro Jiménez Sosa5 ·
Julio Plata Bello6

Received: 20 August 2020 / Accepted: 18 November 2020

© Springer Nature B.V. 2021

Abstract
Contingency data was retrospectively collected to evaluate the historical and current ability to provide multimodality intra‑
operative neurophysiological monitoring during carotid endarterectomy under two conditions: total intravenous anaesthesia
(TIVA) and low dose halogenated anaesthesia (SEVO). 229 patients were monitored during carotid endarterectomy proce‑
dures under general anaesthesia between 2012 and 2020. 121 Patients were monitored with SEVO at a minimum alveolar
concentration less than 0.7 and 108 were monitored using TIVA, according to common anaesthetic practice standards in
our hospital across the years. Multimodality IONM was established with electroencephalography, somatosensory evoked
potentials and motor evoked potentials. As compared to TIVA, patients monitored with SEVO showed significantly higher
motor evoked potential thresholds (313.52 ± 77.74 SEVO and 218.93 V ± 103.2 V TIVA p < 0.05) and lower reproducibility.
Electroencephalography and somatosensory evoked potentials showed no significant differences among the groups. When
using SEVO, multimodality intraoperative neurophysiological monitoring during carotid endarterectomy could mask or miss
a motor isolated change in patients in spite of low dose minimum alveolar concentration and of apparently adequate electro‑
encephalography and somatosensory evoked potentials for monitoring. Given these difficulties, we believe the chronological
transfer to TIVA could have improved our ability to establish multimodality intraoperative neurophysiological monitoring
during carotid endarterectomy in recent times.

Keywords  Carotid endarterectomy · Intraoperative neurophysiological monitoring · Sevoflurane · TIVA · Anaesthesia

1 Introduction
* Ana Mirallave Pescador
A.mirallave‑pescador@nhs.net Carotid endarterectomy (CEA) has proven to be a satisfac‑
1 tory method of prevention of stroke especially in patients
Queen´S Hospital, Barking, Havering and Redbridge
University Trust NHS, Romford, UK presenting with a recent cerebrovascular event and stenosis
2 above 70% [1, 2]. Around the globe, stroke is the second
Unidad de Monitorización Neurofisiológica Intraoperatoria,
Hospital Universitario de Canarias, Santa Cruz de Tenerife, most common cause of mortality and third most common
España cause of disability [3].
3
Servicio de Anestesia, Hospital Universitario de Canarias, While there are several methods of performing CEA
Santa Cruz de Tenerife, España which have shown to equally minimize the risks of stroke
4
Servicio de Cirugía Vascular, Hospital Universitario de including awake procedures [4], there are significant advan‑
Canarias, Santa Cruz de Tenerife, España tages of general anaesthesia (GA) over local anaesthesia
5
Unidad de Investigación, Hospital Universitario de Canarias, with sedation such as better hemodynamic and respiratory
Santa Cruz de Tenerife, España management and better surgical convenience [5]. For this
6
Servicio de Neurocirugía, Hospital Universitario de Canarias, reason, there is a tendency to perform these procedures
Santa Cruz de Tenerife, España under GA.

13
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Monitoring cerebral perfusion becomes a challenge in
an uncooperative patient and the fact that the permeability
of the circle of Willis is deeply variable in the population
[6] further adds potential risks of strokes during temporal
clamping of the internal carotid. Shunt placement to prevent
cerebral ischemia during CEA can be done selectively or
routinely [7] but also carries significant risks such as throm‑
bosis or carotid dissection [8].
Intraoperative neurophysiological monitoring (IONM)
during carotid surgery has been used since the 70 s, starting
with electroencephalography (EEG) [9–11] and somatosen‑
sory evoked potentials (SSEPs) [12, 13], and more recently
motor evoked potentials (MEPs) [14, 15] to detect cerebral
ischemia. Multimodality IONM requires an anesthetic regi‑
men that allows for the recording of neurophysiological
signals reliably, which usually is based on total intravenous
anaesthesia (TIVA) with no muscle relaxants after intuba‑
tion [16–19]. Halogenated agents like sevoflurane (SEVO)
were however more commonly used in the past as TIVA was
not always available and there was a belief that these had
some advantages over TIVA on cardioprotection especially
in patients who already presented with cardiovascular risks
preoperatively [20]. Recently, there have been trials assess‑
ing the reliability of IONM under halogenated agents at a
low minimal alveolar concentration (MAC) of 0.5–0.7 [21].
Our main aim in the present study is to assess the effects
of TIVA versus halogenated agents at a low MAC on neu‑
rophysiological signals during IONM of CEA to evaluate
the reliability of monitoring with both techniques as well as
what differences are expected amongst them.
2 Methods
This study was approved by the ethics committee at Hospital
Universitario de Canarias with the code 2017_76 as a retro‑
spective study. All participants signed an informed consent.
2.1 Inclusion criteria
229 patients were included in this study from January 1st
2012 to January 31st 2020 who underwent CEA procedures
by an experienced vascular surgical team performing a lon‑
gitudinal arteriotomy for carotid stenosis of 70% or above
as confirmed by duplex and/or angiography regardless of
whether this was a symptomatic (141) or asymptomatic (88)
stenosis.
2.1.1 Anesthetic regime
All patients underwent CEA under GA. The use of TIVA
or halogenated agents was not randomized in any manner
and was left to the election of the anesthesiologist in charge
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Journal of Clinical Monitoring and Computing
based on patient’s cardiovascular risks. TIVA was induced
with a standardized protocol of Propofol and Remifentanil
which was maintained at 4–7 mg/kg/h and 0.05–0.5 mcg/
kg/min respectively. Halogenated anaesthesia was estab‑
lished using Sevoflurane at a MAC of 0.7–1 and remifentanil
(0.05–0.5 mcg/kg/min). Rocuronium was given for intuba‑
tion purposes only (0.5–0.6 mg/kg) and was reversed with
sugammadex (2–4 mg/kg) when needed. Oxygen saturation
was kept above 95% and CO2 was maintained stable [22].
Mean arterial pressure was kept 20% above baseline during
clamping if a warning was identified [23], temperature was
maintained above 35 °C [24].
2.1.2 Intraoperative neurophysiological monitoring
Multimodality IONM was performed with a Cadwell Elite
32 channel system (Kennewick, WA, USA). using EEG,
SSEPs and MEPs as follows:
– EEG: was recorded using corkscrew electrodes in posi‑
tions Fp1, F7, C3, P3, T3, O1, Fp2, F8, C4, P4, T4, O2,
Fz y Cz in a double banana montage with filters 0.5–
70 Hz.
– SSEPs: were recorded scalp and peripheral SSEPs after
stimulation of the bilateral median nerve at the wrist
with a varying intensity of 15–45 mA, 5.1 Hz stimu‑
lation frequency and pulse width of 0.2 ms. Peripheral
SSEPs were recorded at the axillary point and at Cv–Fz.
Cortical SSEPs were recorded at C3′–C4′/Cz’–Fz.
– TcMEPs: were evoked using anodal transcranial pulses at
position C3–Cz/C4–Cz using corkscrew electrodes (train
of 5–7 pulses, 0.05 ms, ISI 4 ms). Thresholds to elicit
MEPs were calculated such as the minimal intensity to
evoke a reliable response and minimize cephalic move‑
ment that could disrupt the surgery. We used twisted
bipolar needle electrodes bilaterally on the extensor dig‑
itorum comunis, abductor pollicis brevis and abductor
hallucis muscles to record the MEPs.
2.1.3 Surgical approach and alarm criteria
Before the permanent clamp and arteriotomy, a 2  min
sequential test clamp of the internal, external and common
carotid arteries was performed in order to assess perme‑
ability of the cerebral perfusion and compensation across
the circle of Willis after ipsilateral arterial blood restric‑
tion. Neurophysiological signals were constantly checked
for warnings and if these were averted, we first increased the
mean arterial blood pressure by 20%. If the neurophysiologi‑
cal signals returned to normal, we continued the surgery at
this blood pressure level. If they did not recover, we released
the clamp until they did and then re-clamped placing a shunt.
Journal of Clinical Monitoring and Computing
Alarm criteria were assessed all throughout the surgery.
However, in attempts to narrow these to surgical action and
for analytic purposes, this study only accounts for signal
changes that happened after the test clamp and until the end
of the surgery. Significant signal changes were: a drop in
amplitude of the EEG of 50% or marked change (delta) in
the background frequency ipsi or bilateral to the surgery, a
drop of 50% or more of the amplitude of SSEPs or a 90%
drop of amplitude of the MEPs.
3 Results
For calculations of predictive values, sensitivity, specificity
and likelihood ratio (LR) Within these alarm criteria we
defined 3 conditions:
1. Permanent signal change (PSC): a significant signal
change that was not reverted at the end of the surgery.
2. Reversible signal change (RSC): a significant signal
change that was reverted during surgery.
3. No signal change (NSC): cases where no significant sig‑
nal changes were identified.
Within the reversible signal changes, we applied Hill’s
guidelines for temporality, strength and biological plausi‑
bility [25] to determine the likelihood of these changes to
have been reverted by surgical action [26]. In this regard,
we thought that surgical action that was more likely to have
caused a meaningful return to normal of the neurophysi‑
ological signals after the 2 min test clamp was that of a
shunt placement after failure to achieve this by increasing
mean arterial pressure by 20%. On the contrary, we believe
that mean arterial pressure increase in isolation would be
a less likely cause to have reverted the neurophysiological
warning and therefore RSCs could also be false positives or
the causality of the RSC could not be precisely determined
(i.e. neurophysiological traces could have been returned to
baseline spontaneously in spite of an increased BP).
3.1 General demographics
A total of 229 patients underwent CEA with full multimo‑
dality IONM. 183 men and 46 women. 121 patients were
monitored with halogenated agents during the years and 108
were monitored using TIVA. As seen in Fig. 1, the tendency
towards TIVA has increased in recent years (2018–2020)
while in the first years of the study, there was a tendency to
use SEVO.
The mean age of the patients in the SEVO group was
of 68.47 ± 9.26 years and 68.29 ± 9.19 years in the TIVA
group. There were 141 patients in total which presented
symptoms of cerebrovascular events preoperatively and 88
Fig. 1  Anaesthesia time evolution in CEA
Table 1  Demographics and TcMEP threshold
SEVO n = 121 TIVA n = 108 p < 0.05
Age (years) 68.47 ± 9.26 68.29 ± 9.19 –
% Stenosis Intervened 82.84 ± 8.35 83.65 ± 8.78 –
carotid
% Stenosis contralateral 60.09 ± 21.53 56.48 ± 23.29 –
carotid
TcMEP threshold (V) 313.52 ± 77.74 218.93 ± 21.53  + 
which did not. However, symptomatic (p = 0.48) or asymp‑
tomatic (p = 0.26) artery stenosis did not differ significantly
between the groups. In asymptomatic patients however,
half of the warnings were given in those whose contralat‑
eral carotid artery showed a stenosis of 100% or had previ‑
ously undergone CEA in the past regardless of anesthesia.
The mean % stenosis of the intervened carotid artery was of
82.84 ± 8.35% and of 60.09 ± 21.53 of the contralateral in
the SEVO group and of 83.65 ± 8.78% and 56.48 ± 23.29%
respectively in the TIVA group (Table 1).
3.2 Monitorability
In both groups, we managed to achieve a continuous raw
EEG that would allow to monitor changes reliably after
clamping. SSEPs could be recorded in 100% of cases but
MEPs could not be recorded in 7 patients with SEVO. MEP
threshold moreover with SEVO was 313.52 ± 77.74 and it
was 218.93 V ± 103.2 V with TIVA. These values were sig‑
nificantly lower with TIVA than SEVO (p < 0.05) Fig. 2.
3.3 Warnings
3.3.1 TIVA
17 patients presented with EEG warnings (9 unilateral and
8 bilateral to the carotid stenosis) of which 8 also presented
SSEP warnings and 4 TcMEP warnings. None of the cases
in which the SSEP or MEPs changed significantly showed a
stable EEG while in 3 patients, SSEP changes were detected
13

Fig. 2  Shows a comparison of traces between a case monitored with
Sevoflurane and a case monitored with TIVA. (a) Comparison of
baseline EEG traces using both anaesthetic modalities shows that
a continuous EEG could be obtained. (b) Comparison of baseline
in spite of unchanged MEPs and one patient showed MEP
changes with stable SSEPs (Table 2).
3 patients had a postoperative stroke. 1 patient had no
warnings intraoperatively and the stroke developed postoper‑
atively as a result of an embolus 2 h after surgery (Table 3).
All other 15 cases in which warnings were given had end
surgical traces that returned to opening baseline values at the
end. However, under these RSCs, just 13 were associated to
shunt placement while the other 2 reversed only by increas‑
ing mean arterial pressure. Under these circumstances and
considering the former as possible true positives and the
latter as possible false positives, sensitivity is of 100%,
13
Journal of Clinical Monitoring and Computing
SSEPs with both modalities showing no significant differences. (c)
Comparison of MEPs obtained with both modalities showing a sig‑
nificant threshold difference between the groups in favour of a lower
threshold for the case monitored with TIVA
specificity of 97.84%, positive predictive value (PPV) of
88.23%, likelihood ratio (LR) of 45.45 and negative predic‑
tive value (NPV) of 100%. On the contrary, if we assume
that all RSCs reverted to opening baselines by chance (i.e.
not related to surgical action taken), sensitivity would come
to 100%, specificity to 85.84%, PPV of 11.76%, LR of 7.07
and NPV of 100%. We could also assume that all RSCs are
true positives. These values would then come to sensitiv‑
ity of 100%, specificity of 100%, PPV of 100% and NPV
of 100%. We however believe this last scenario to be less
likely, the first the most likely and reality in a range of all
3 (Table 4).
Journal of Clinical Monitoring and Computing

Table 2  Warnings Of the patients that presented RSCs (14), just 11 could

SEVO n = 16 TIVA n = 17 be associated with the surgical action of a shunt placement
while 3 reverted after the increase in mean arterial pressure.
EEG warning Under these circumstances (11 RCSs as true positives, 3
 Unilateral 8 9 RSCs as false positives), we obtain a sensitivity of 100%,
 Biltera 8 8 specificity of 97.2%, PPV of 81.13%, LR of 35.71 and NPV
SSEP warning 5 (+ EEG) 8 (+ EEG) of 100%. On a different scenario, if we consider that all
TcMEP warning 1 (+ EEG + SSEP) 4 (3 + EEG + SSEP) RSCs reverted to baseline by chance (independent of surgi‑
(1 + EEG) cal action and therefore false positives) this would make for
Warning reverted 3 2 a sensitivity of 100% specificity of 88.23%, PPV of 12.5,
increasing blood
LR of 8.47 and NPV of 100%. If all RSCs as true positives,
pressure
sensitivity would remain, specificity would be 100%, PPV
Shunt effective 11 13
would be 100%. However, we consider this last scenario as
Shunt not effective 2 2
the least likely of the three, with the first case being the most
likely and a possible range existing between all of the three
cases (Table 4).
Table 3  Strokes
SEVO n = 6 TIVA n = 3
3.3.3 Additional statistics

Intraoperative stroke 2 2 With the above data on both TIVA and SEVO, we were not
Delayed stroke able to calculate the Chi–Square tests given that the contin‑
Stroke <24 h after CEA  2 1 gency 3 × 2 table contains null values. We therefore wanted
 TIA 2 0 to present a different way of approaching the above results.
We attempted to build a contingency 2 × 2 table for each
modality. We further hypothesized that warnings that were
Table 4  Signal changes and correlation with the development of a only reverted by a shunt (and not after increased mean arte‑
stroke rial blood pressure), could mean that the patients may likely
IONM warning No stroke Stroke have developed a stroke if this warning was not reverted.
On the contrary, we cannot say this to the same certainty if
TIVA SEVO TIVA SEVO
the warning was reverted by increasing mean arterial blood
NONE 91 105 0 0 pressure in isolation. Under these circumstances, for both
Reversible 15 14 0 0 modalities the value of P using an exact Fisher test came to
Irreversible 0 0 2 2 be less than 0.001 and therefore significant.
Backbleeding, as a parallel method, failed to recognize
poor vascular compensation in 8 patients (4 in the TIVA,
3.3.2 Sevoflurane 4 in the SEVO), who ended up needing a shunt in spite of
normal values.
Figure 3 shows an exemplary case of the warnings we could
detect with SEVO. 16 patients presented with EEG warn‑
ings (8 were unilateral and 8 were bilateral to the carotid 4 Discussion
stenosis) of which 5 also presented SSEP warnings and 1
TcMEP warnings. None of the 7 patients in which TcMEPs The main finding of our study is that, in line with previ‑
were not recordable showed warnings intraoperatively on ous literature [21, 27], IONM is affected by halogenated
EEG or SSEPs (Table 2). anaesthesia in CEA in spite of low MAC doses. Patients
6 patients presented a postoperative stroke of which 2, monitored with SEVO showed significantly higher thresh‑
had intraoperative warnings not reverted at the end of the olds and lower reproducibility to elicit MEPs (as seen by the
surgery, related to a non-functioning shunt and a carotid dis‑ inability to elicit TcMEPs in 7 patients, compared to TIVA).
section, while 4 did not. Of these, two patients developed This poses a significant pitfall in detecting motor exclusive
only transitory clinical signs of stroke (TIA) due to low deficits in this population [15, 28]. In spite of this, although
blood pressure postoperatively while 2 patients developed a possible, we did not find exclusive MEP warnings and in all
postoperative embolic stroke. All initially woke up with no our patients, and MEP warning was always accompanied by
new neurological deficits (Table 3). an EEG or an SSEP warning.

13

Fig. 3  Shows exemplary cases of the neurophysiological traces
before, during and after clamping of the internal carotid artery. The
black arrows show the moment of the clamp and the red arrows show
In our series, most warnings regarded only an EEG sig‑
nificant change. Moreover, in all patients who had a signifi‑
cant signal change in other modalities, this always included
an EEG change so there were no SSEP or MEP changes in
isolation. It is however known that EEG as a standalone pro‑
cedure has only modest sensitivity in spite of a high speci‑
ficity and can be affected by multiple factors such as the
number of channels used or experience of the neurophysi‑
ologist interpreting the changes amongst others. However,
if these factors are accounted for, Chang et al. [29] found
that patients with an EEG change intraoperatively are 5.79
times more likely to have a stroke in the 30 days following
surgery even if the changes are reverted and if these changes
are irreversible, the likelihood of a stroke is up to 71 times
higher. Moreover, raw EEG in the experienced eye has been
13
Journal of Clinical Monitoring and Computing
the moment when the shunt was placed after detecting a significant
signal change in the IOM. (a) shows the EEG changes, (b) the SSEPs
and (c) the MEPs
proven in multiple occasions to be effective in predicting
selective shunt placement in CEA even in times when TIVA
was not in use [11, 30]. We believe these results to be in
line with our current study where EEG was always the first
significant change patients experienced after clamping. We
would therefore conclude from this that attention should
be paid on EEG changes, both ipsi and contralateral to the
clamped side and that efforts should be made to establish a
level of anaesthesia that permit optimal recordings of EEG
to be able to detect such changes.
Our study could imply that SEVO should not be used if
MEPs are the only IONM modality applied. However, in
terms of MEPs as a standalone procedure for monitoring
CEAs the literature suggests that using MEPs only can in
fact be challenging. Firstly, MEPs are unstable and one of
Journal of Clinical Monitoring and Computing
the major reasons for this is the high sensitivity to anesthetic
agents [31]. In this regard, our study is in agreement. Also,
In a previous study using TIVA, Malcharek et al. [32] Fur‑
ther assessed the correctedness of using MEP non classical
changes such as amplitude drop < 50%, area under the curve
drop or morphological changes to the MEPs during carotid
endarterectomies or the combination of these as warning
criteria in CEA or whether they produced an unaccepta‑
ble number of false positives as compared MEP loss. They
reached the conclusion that non-classical MEP changes, pre‑
sented an inappropriate number of false positive warnings
in CEAs. This suggests for the reader that multimodality
IONM with SEPs an EEG would be more appropriate than
MEPs alone and interpretation of MEP changes during CEA
should be taken with care. MEPs could nonetheless inform
the neurophysiologist about motor isolated changes [15, 21]
and in this respect, we would recommend TIVA to be used
to detect such changes.
Another finding in our series is that shunt placement
percentages were similar in the SEVO (13.22%) and in
the TIVA group (13.08%). While symptomatic (p = 0.48)
or asymptomatic (p = 0.26) artery stenosis did not differ
significantly between the groups, more of our patients pre‑
sented with symptoms of a cerebrovascular event than not,
as also reported as a risk by Thirumala et al. [33] and in
asymptomatic patients, half of the warnings were given in
those whose contralateral carotid artery showed a stenosis of
100% or had previously undergone CEA in the past regard‑
less of anesthesia. These have been identified [34] as factors
which may affect IONM. Backbleeding on the contrary did
not fully predict the presence of warnings or postoperative
strokes and failed to recognize these in 8 patients who did
not meet classical criteria for shunt placement. This is in
our opinion is a near miss situation which was effectively
avoided by IONM.
Postoperative neurological outcome was well predicted
with both modalities of anesthesia. Only 1 patient in the
TIVA and 4 in the SEVO group had a postoperative stroke
with no changes in intraoperative recordings but a postop‑
erative cause for this was always identified and was mostly
related to postoperative embolic phenomena [28]. We
therefore report no false negative results in our series. We
have however made emphasis in determining the meaning
of a reversible signal change and what this would mean to
the neuromonitorist in the operating room. Skinner et al.
[26] and Holdefer et al. [35] highlighted the importance of
these changes and the interpretation implications that these
englobed to potentially prevent irreversible neurological
damage. In our groups, we made a distinction between
signals that reverted after the placement of a shunt and
increased mean arterial pressure and those that reverted only
by increasing the mean arterial pressure as well as signals
reverting only by chance. Although we can never confirm
causality of the normalization of the signal or assess the
clinical status of the patient when a warning that reverts is
given, we believe the former (shunt placement and increase
in mean arterial pressure) more likely to be true as also sup‑
ported by significant results of the Fisher exact test. Reality
would remain in a range between all possibilities. However,
in both the SEVO and TIVA groups we found a similar and
strong association between an IONM warning and postop‑
erative outcome.
Anesthetic protocols in CEA have changed throughout
the years. While in the past it was believed that SEVO had
some grade of cardioprotection [20] and was therefore pre‑
ferred, as was in our series, for patients undergoing vascular
surgery, this is now controversial [36, 37] and in our center,
there has been a gradual shift towards TIVA, which is now
preferred over volatiles. We believe therefore that this shift
further improves our ability to reliably provide full multi‑
modality IONM.
5 Conclusion
Based on the above results, we can conclude that selec‑
tive shunting during CEA guided by IONM is possible for
only some modalities (EEG and SSEPs) for both anesthetic
regimes used, always however if kept in a concentration that
allows for stable baselines. This for us has meant SEVO no
higher than a MAC of 0.7. However, contrary to this, MEP
monitoring in spite of low MAC concentrations was signifi‑
cantly affected by halogenated agents and we do not recom‑
mend it is used in isolation when performing CEA under
neurophysiological guidance. We believe that the gradual
tendency change throughout the years in the use of TIVA
during CEA is therefore improving our ability to monitor
reliably with multimodality IONM including MEPs. We
also would like to highlight the importance of a stable EEG
while monitoring CEAs and recommend this to be a priority,
regardless of the anesthetic regime used.
Author contributions  AMP, PPL and ASG prepared the manuscript,
elaborated statistical analysis and prepared figures and tables. They also
carried out the monitoring. BDD is the attending anesthesiologist and
also prepared the manuscript. JPB, RUG, EGT, ZIA, CGR, CPE are
the vascular surgeons and prepared the manuscript. AJS, JPB helped
with statistical analysis and prepared the manuscript.
Compliance with ethical standards 
Conflict of interest  None of the authors have any conflict of interest.
Ethical approval  This study was approved by the ethics committee at
Hospital Universitario de Canarias with the code 2017_76 as a retro‑
spective study.
13

Informed consent  All participants signed an informed consent.
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