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Original article

A review of monopolar motor mapping and a comprehensive guide to


continuous dynamic motor mapping for resection of motor eloquent
brain tumors
P. Schucht 1,∗ , K. Seidel 1 , A. Jilch , J. Beck , A. Raabe
Department of Neurosurgery, Inselspital, Bern University Hospital, 3010 Bern, Switzerland

a r t i c l e i n f o a b s t r a c t

Article history: Monopolar mapping of motor function differs from the most commonly used method of intraoperative
Received 12 May 2016 mapping, i.e. bipolar direct electrical stimulation at 50–60 Hz (Penfield technique mapping). Most impor-
Received in revised form 23 January 2017 tantly, the monopolar probe emits a radial, homogenous electrical field different to the more focused
Accepted 27 January 2017
inter-tip bipolar electrical field. Most users combine monopolar stimulation with the short train tech-
Available online xxx
nique, also called high frequency stimulation, or train-of-five techniques. It consists of trains of four to
nine monopolar rectangular electrical pulses of 200–500 ␮s pulse length with an inter stimulus inter-
Keywords:
val of 2–4 msec. High frequency short train stimulation triggers a time-locked motor-evoked potential
Intraoperative neuromonitoring
Motor-evoked potential
response, which has a defined latency and an easily quantifiable amplitude. In this way, motor thresh-
Monopolar motor mapping olds might be used to evaluate a current-to-distance relation. The homogeneous electrical field and the
Glioma surgery current-to-distance approximation provide the surgeon with an estimate of the remaining distance to
Continuous dynamic mapping the corticospinal tract, enabling the surgeon to adjust the speed of resection as the corticospinal tract
is approached. Furthermore, this stimulation paradigm is associated with a lower incidence of intraop-
erative seizures, allowing continuous stimulation. Hence, monopolar mapping is increasingly used as
part of a strategy of continuous dynamic mapping: ergonomically integrated into the surgeon’s tools, the
monopolar probe reliably provides continuous/uninterrupted feedback on motor function. As part of this
strategy, motor mapping is not any longer a time consuming interruption of resection but rather a radar-
like, real-time information system on the spatial relationship of the current resection site to eloquent
motor structures.
© 2017 Published by Elsevier Masson SAS.

1. Introduction becomes a modifiable risk factor for disease progression and death,
emphasizing the value of [4] intraoperative neurophysiology.
Despite the lack of randomized controlled studies, the prog- Today, the benefit of intraoperative neurophysiology to achieve
nostic impact for radical resections of gliomas according to MRI safe and radical resections of brain tumors is [5] uncontested and
becomes increasingly stronger [1,2]. Removing the last and deep- our attention is increasingly shifting towards the modalities of
est part of the tumor often draws resection near to eloquent intraoperative monitoring (IOM). IOM of motor-evoked potentials
areas, potentially putting neurological functions at risk. Hence, (MEPs) by direct cortical stimulation (DCS) with a strip electrode
the oncological advantage of a more radical resection may be permits continuous, real-time assessment of the primary motor
counterweighted by increasing risks of neurological deficits [3] as system’s functional integrity [6,7]. Intermittent subcortical map-
the surgeon proceeds with tumor removal. Mapping and moni- ping with a handheld probe provides crucial information on the
toring of motor function not only helps to avoid permanent motor function and functionality of a given area during surgery [6,8].
deficits, in fact, these technologies indirectly increase the success Bipolar, 50–60 Hz stimulation mapping has become the standard-
rate of radical resection by clarifying the functional relevance of-care due to its limited current spread and its ability to reliably
of a presumably eloquent area. Presumed eloquence therefore reflect the function of tissue at-sight, i.e. of tissue between the
forceps.
In this review, we explore alternatives to the classical Penfield
∗ Corresponding author. stimulation protocol. We also discuss how presumed shortcomings
E-mail address: Philippe.schucht@insel.ch (P. Schucht). of those alternatives provide unique benefits to the surgeon. Lastly,
1
Prof. Dr. P. Schucht and Dr. K. Seidel share first authorship. we detail the strategy of continuous dynamic mapping, in which

http://dx.doi.org/10.1016/j.neuchi.2017.01.007
0028-3770/© 2017 Published by Elsevier Masson SAS.

Please cite this article in press as: Schucht P, et al. A review of monopolar motor mapping and a comprehen-
sive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Neurochirurgie (2017),
http://dx.doi.org/10.1016/j.neuchi.2017.01.007
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2 P. Schucht et al. / Neurochirurgie xxx (2017) xxx–xxx

combinations of MEP triggering and continuous monopolar map- optimal orientation between the probe and the expected fiber ori-
ping improve safety and speed of resection. entation during cortical and subcortical stimulation, has recently
been recognized by the neurosurgical community [17]. Finally, this
technique was applied to evaluate the distance of the CST to the
2. Selection of the stimulation paradigm
stimulation probe [29–34].
Two stimulation paradigms are available for cortical and sub-
cortical mapping. The most established paradigm is the classical 4. Estimating the remaining distance to the CST
Penfield technique with a pulse stimulation frequency of 50 or
60 Hz, a 1 msec pulse duration and a stimulus duration of 1 to 4 sec Whether or not a motor response is provoked depends on the
depending on the particular tissue of interest [8–11]. Stimulating charge applied to the tissue, which in turn depends on stimulation
the motor system under general anesthesia in the described man- intensity and pulse duration [17]. Moreover, the current density
ner will induce a tonic muscle twitch which starts with a certain decreases with distance. The higher the stimulation intensity, the
amplitude and increases in amplitude while stimulation is going on larger the areas where motor-evoked potentials can be generated,
[12,13], but does not permit a precise measurement of the motor and vice versa [20]. This also implies that with higher stimulation
threshold [14]. intensity a positive answer can be found at a greater distance from
Another more recently introduced concept is the short train the CST. Several groups investigated the “stimulation-intensity-to-
technique also called high frequency stimulation, or train-of-five CST-distance” relationship: they correlated stimulation intensity
technique. It typically consists of trains of four to nine monopolar (in mA) needed to elicit motor-evoked potentials with distance
rectangular electrical pulses of 200–500 ␮s pulse length with an (in mm) to the CST [29–34]. Although a definite statement on this
inter-stimulus interval of 2–4 msec (corresponding to 250–500 Hz) current-to-distance relationship is yet missing, a rule of thumb
[6,15–18]. The temporal summation of multiple descending volleys of “1 mA corresponds to 1 mm” is increasingly being used as a
in high frequency short train stimulation finally triggers a time- reliable approximation during subcortical short train monopolar
locked MEP response [15,19], which has a defined latency and an stimulation.
easily quantifiable amplitude [13,14,20].
The lower charge applied during stimulation using those
paradigms might explain why the incidence of intraoperative 5. Acoustic feedback system
seizures is lower in the short train technique than in classical Pen-
field stimulation [21]. The reported incidence of seizures during As the surgeon focuses on the resection, he cannot simulta-
intraoperative electrical brain stimulation ranges from 1–4% using neously monitor MEPs himself. Here, an acoustic feedback system
short train of electrical stimuli, and 5–20% in Penfield method of has proven to be of great help. A high-pitch negative control sound
electrical stimulation [6,7,9,16,21–25]. is heard as long as the probe touches the brain and current flows
but no MEP is elicited. This control sound immediately switches to
a low-pitch warning sound the very moment the dynamic probe
3. Selection of the stimulation probe triggers an MEP, thereby informing the surgeon that the resection
has come within a certain range of the CST according to the
Different stimulation probes are available for mapping. The most stimulation-intensity-to-CST relationship [3,35].
commonly applied probes are bipolar probes with two spherical
electrodes with an inter-tip distance of 5 mm [9,11] (Fig. 1C). This
probe is very selective, as it activates the tissue located between 6. The warning sign hierarchy: combining MEP monitoring
the two tips. The electric field is inhomogeneous beyond the space and mapping
between the tips and activation of distant tissue is less likely
[14,17,20]. Therefore, bipolar probes provide reliable information Both MEP monitoring and motor mapping are known for their
of the function if the region of interest is between the tips, but ability to provide warning signs for motor system damage during
are of limited use if the region of interest is further away from the surgery, with each method having its own strengths and weak-
stimulation site. nesses. Even though DCS-MEP is a useful predictor of later motor
Another way of mapping is performed by applying a monopolar deficits, its actual value during surgery is limited because signal
finger stick probe [26] (Fig. 1A–B). In this setting, the probe is the alterations may happen abrupt and irreversible: by the time MEP
active part spreading the current to a reference electrode lying fur- changes become apparent the damage may already be done. In a
ther away in the skin [27]. The radial and homogeneous spreading recent publication on surgeries for motor eloquent tumors, the rate
of the electrical field from the monopolar probe allows the elec- of permanent motor deficits was 25% for patients with irreversible
trical current to enter perpendicularly into the axon, resulting in MEP changes and 75% for patients with MEP loss during surgery
a more effective stimulation [17]. Monopolar mapping permits the [20]. Motor mapping on the other hand, is a formidable guide as it
use of reliable quantitative thresholds and allows predictions on the provides reliable information on the functional relevance of an area
distance from the probe to the corticospinal tract (CST) by abso- at risk. However, classical mapping is punctiform in time and space
lute stimulation current values [20,27]. Therefore, the presumed and cannot detect whether a proximal damage to the motor sys-
shortcoming of monopolar mapping, namely that its current is not tem has already occurred [20]. Therefore, mapping should be used
focused on the surface area but instead spreads in a radial fash- as the primary source of functional information during surgery in
ion, may be used to provide crucial information on the proximity proximity to the CST, complemented by DCS-MEP monitoring at
of eloquent areas at any given stage of resection. a low mapping motor threshold for uninterrupted examination of
Monopolar cathodal stimulation is more effective compared to the functional integrity of the primary motor system. A safe map-
bipolar stimulation in terms of eliciting MEPs [17]. This was first ping corridor for mechanical injury of the CST using subcortical
described in peripheral motor nerve stimulation with monopo- short train monopolar stimulation has been established between
lar versus bipolar stimulation [28]. Later monopolar (referential) high and low motor thresholds. Neither significant signal changes
stimulation was introduced for mapping during tumor resection in MEP monitoring nor permanent motor deficits occur as long as
[26]. The advantage of the radial spreading of the electric field the resection is stopped at motor thresholds of 1–2 mA at the very
of a monopolar probe, which in fact eases the finding of the latest [20].

Please cite this article in press as: Schucht P, et al. A review of monopolar motor mapping and a comprehen-
sive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Neurochirurgie (2017),
http://dx.doi.org/10.1016/j.neuchi.2017.01.007
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Fig. 1. Schematic illustration of stimulation probes. Monopolar stimulation probes are spreading the current to a far reference (so called referential stimulation). This could
be achieved by a conventional fingerstick type probe (A) or a modified surgical instrument like the surgical suction aspirator (B). The resulting electrical field spreads radial
and homogeneous and may enable quantitative statements to the remaining distance of the structure being stimulated. This stimulation type is more sensitive. Bipolar
stimulation probes (C) have a very focal field between the two tips. The electric field is inhomogeneous beyond the space between the tips and activation of distant tissue is
less likely. This stimulation type is more selective/ specific.

7. Overcoming temporal and spatial limitations of mapping

The interruptive and punctiform technique of classical stimula-


tion protocol provides insufficient spatial and temporal coverage
of the surgical site which may lead to motor deficits despite higher
and apparently safe motor thresholds (for example 3–6 mA) [20]. In
order to overcome the temporal and spatial limitations the stimu-
lation probe may be integrated into the surgeons working tools.
A device is needed that allows continuous subcortical stimula-
tion without interrupting the surgical workflow of tumor removal
[35]. This can be achieved by integrating the monopolar stimula-
tion probe in the surgical suction device, which continuously clears
the resection site of blood and debris [35]. The positive stimula-
tion response should further be coupled to an acoustic system to
facilitate real-time feedback [35]. Fig. 2. Continuous dynamic mapping device. The suction device is electrically iso-
lated up to its tip. Owing to a connection beneath the handle, the suction device can
be used as a monopolar stimulation probe.
8. How to use the strategy of continuous dynamic mapping
during surgery

The continuous dynamic mapping device is used when the sur-


geon believes to be approaching the CST, based on the anatomical
orientation of the surgeon and neuronavigation (Figs. 2 and 3).
An initial stimulation intensity of 10–15 mA is recommended,
corresponding to about 10–15 mm distance to the CST [29]. The
high-pitch negative control sound informs the surgeon that the
current flows correctly and that no MEPs were evoked. Hence, he
can proceed swiftly as he knows the operation site to be at a safe
distance from the CST (Fig. 4). The instant an MEP is triggered,
the surgeon is immediately alerted by the change of the control
sound to a low-pitch alert sound, giving the surgeon an estimate
for the remaining distance to the CST. The stimulation intensity
is then reduced in 2-mA steps, allowing the surgeon to continue
tumor removal at decreased and more cautious speed of resection.
The surgeon removes tumor at all sites where no MEPs are trig-
gered with the current stimulation settings. Stimulation intensity
is only lowered once the low-pitch alert sound indicates that Fig. 3. The dynamic suction device clears the surgical site of blood and debris just
the threshold has been reached throughout the resection front. like the standard suction device. Working in parallel to the ultrasonic aspirator, it
Lowering of the stimulation intensity corresponds to a reduction also acts as a monopolar probe, continuously stimulating the tissue that is currently
of the remaining distance to the CST and is reflected in the term under resection.

Please cite this article in press as: Schucht P, et al. A review of monopolar motor mapping and a comprehen-
sive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Neurochirurgie (2017),
http://dx.doi.org/10.1016/j.neuchi.2017.01.007
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Fig. 4. Strategy of continuous dynamic mapping. The device is used as a suctiondevice parallel to the resection tool. Once an estimated distance of 10–15 mm to the
corticospinal tract (CST) is reached the device is activated (a). An initial stimulation intensity of 10–15 Ma is used, corresponding to an estimated distance of 10–15 mm.The
instant a motor-evoked potential (MEP) is triggered the surgeon is warned bya switch from the high-pitch negative control sound to a low-pitch alert sound (b).The stimulation
intensity is then reduced by 2 mA, and the resection is continued at sites negative for the set current (c and d), until again the change from the negative control to the alert
sound warns the surgeon that the next motor threshold has been reached (e). This stepwise approach is continued until a minimal threshold is reached(f, g and h). Purple
indicates tumor tissue, blue indicates CST fibers and green indicates the electrical field that elicits an MEP and triggers the alert sound if it reaches the CST (red star).

Please cite this article in press as: Schucht P, et al. A review of monopolar motor mapping and a comprehen-
sive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Neurochirurgie (2017),
http://dx.doi.org/10.1016/j.neuchi.2017.01.007
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“quantitative mapping” [35]. Resection is usually continued until 12. Conclusion


a motor threshold of 3 mA is reached. Surgery beyond a motor
threshold of 3 mA should only be performed in exclusive cases The radial field of monopolar mapping opens up new possibil-
when the surgeon believes that a complete resection can be ities of intraoperative neurophysiology during surgery for motor
achieved, and provided that DCS-MEPs remain stable. Resection eloquent brain lesions. Combined with short train mapping it offers
should be immediately paused in cases of DCS-MEP alterations, the additional benefit of providing the neurosurgeon with an esti-
and stopped if the alterations persist after a 15-minute pause. mate on the remaining distance to motor eloquent structures,
helping him to adjust the speed of resection as he approaches the
CST. Integrating the monopolar probe into the existing surgical
9. Applying the strategy of continuous dynamic mapping to
instruments and using it continuously throughout all crucial stages
motor eloquent lesions
of resection leads to an uninterrupted workflow with real-time,
dynamic feedback. Moreover, this stimulation paradigm is associ-
In a proof-of-concept analysis, the safety of continuous dynamic
ated with a lower incidence of intraoperative seizures and enables
mapping as a surgical and electrophysiological strategy was estab-
continuous stimulation. Altogether, continuous dynamic monopo-
lished in a cohort of 69 patients undergoing surgery for motor
lar mapping is a compelling and safe strategy for resection of motor
eloquent tumors. No patient had a permanent motor deficit caused
eloquent brain lesions. Integrating monopolar stimulation into a
by a mechanical injury of the CST but 2 patients (3%) sustained
surgical instrument increases reliability and promotes acceptance
permanent motor deficits due to vascular injuries [35].
as well as the clinical handling of subcortical mapping.
The strategy of continuous dynamic mapping was recently
investigated in a cohort of 67 consecutive patients undergoing
surgery for glioblastomas adjacent to the CST (estimated < 10 mm). Disclosure of interest
Transient neurological deficits were observed in 30% and 10% of
the patients on the day after surgery and at discharge, respec- 2014 in Neurosurg Focus zum selben Thema schreiben wir: Dr.
tively, emphasizing the proximity of the resection to the CST. The Schucht is a member of the MSD advisory board and the Integra
lowest motor threshold reached during surgery was 1–3 mA in 23 advisory board, and Dr. Raabe is a patent holder with Inomed. The
patients, 4–5 mA in 13 patients and 6–10 mA in 10 patients, as well other authors declare that they have no competing interest.
as > 10 mA in 21 patients. Three patients suffered from permanent
motor deficits, 2 of which were caused by vascular injuries and 1
was due to mechanical injury. The goal of complete resection of References
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Please cite this article in press as: Schucht P, et al. A review of monopolar motor mapping and a comprehen-
sive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Neurochirurgie (2017),
http://dx.doi.org/10.1016/j.neuchi.2017.01.007
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Please cite this article in press as: Schucht P, et al. A review of monopolar motor mapping and a comprehen-
sive guide to continuous dynamic motor mapping for resection of motor eloquent brain tumors. Neurochirurgie (2017),
http://dx.doi.org/10.1016/j.neuchi.2017.01.007