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Kothbauer 2007
Kothbauer 2007
REVIEW/MISE AU POINT
Division of Neurosurgery, Department of surgery, Kantonsspital Luzern, 6000 Luzern 16, Switzerland
0987-7053/$ — see front matter © 2007 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.neucli.2007.10.003
408 K.F. Kothbauer
the recordings to spontaneously improve again, irrigating with warm saline solution to wash out
blocking potassium. Other measures include the elevation of mean arterial pressure to improve
local perfusion. Even staged resection can be considered if intraoperative measures do not
sufficiently improve the recordings.
© 2007 Elsevier Masson SAS. All rights reserved.
Neurophysiology
Figure 1 Single stimulus and multipulse stimulation to evoke
Motor potentials are evoked with transcranial electrical D-waves and motor potentials.
motor cortex stimulation. The stimulus points are C3, C4,
C1, C2, Cz, and a point 6 cm in front of Cz (International
10/20 EEG electrode system [24]). Cork-screw electrodes all four extremities (thenar, hypothenar, anterior tibialis,
are optimal for fixation to the scalp, but straight needle abductor hallucis). Other muscles, such as the quadriceps,
electrodes as well as surface electrodes are also in use. hamstrings, biceps, even the diaphragm, and the external
Electrical stimulation with rectangular constant current anal sphincter can be used. The signals are amplified 10,000
impulses of 0.5 ms duration and intensities between 15 and times, and recorded on epochs of 100 ms with a filter setting
220 mA is used. from 1.5 to 800 Hz. Muscle MEPs also do not require averag-
D-waves [7] are elicited with single stimuli. This is there- ing and can be repeated at a rate of 0.5—2 Hz. With the focal
fore called the ‘‘single stimulus technique’’ (Fig. 1). The anode as stimulating electrode, a montage of C1/2 (anode at
D-waves are recorded as travelling waves directly from the C1, cathode at C2) will first yield responses in the right-sided
spinal cord with an electrode inserted into the spinal epidu- muscles, and higher intensities in muscles of both sides. Usu-
ral space by the surgeon. The signals are amplified 10,000 ally the lower extremities require higher stimulus intensities
times, the filter bandpass is set from 1.5 to 1700 Hz, record- than the upper extremities. C3/4, C4/3 or Cz/6 are used
ing epochs are 20 ms. Baseline recordings are obtained individually as alternative stimulation points. The stimula-
before dura opening. The signal usually does not require tion parameters have recently been further elucidated to
averaging, although recording quality often improves with
a few averages. The stimulations are repeatable at a rate of
0.5—2 Hz. This provides practically real-time feedback.
The relevant D-wave parameter is its peak-to-peak ampli-
tude (Fig. 2). A decrease of more than 50% of the baseline
amplitude is associated with a long-term motor deficit [25].
Latency changes of the D-wave are much less important and
usually not due to surgery but to circumstances such as tem-
perature [26]. Higher stimulation intensities are followed
by shorter D-wave latencies. This is likely due to the corti-
cospinal tract fiber activation occuring deeper in the white
matter of the brain [14].
Muscle MEPs are elicited with transcranial electrical stim-
ulation over the same electrodes as for the D-wave. A short
train of five to seven stimuli with four milliseconds inter-
stimulus intervals [27,28] is used. The technique is called
‘‘multipulse technique’’ [22] or ‘‘train stimulus technique’’
(Fig. 1) [17,18]. Compound muscle action potentials are Figure 2 D-wave recording and interpretation. The peak-to-
recorded with needle electrodes from target muscles in peak amplitude is the relevant parameter.
410 K.F. Kothbauer
Ninety-two patients could be reliably monitored. None of Changes due to non-surgical influences (intravenous bolus
the eight patients in this study who preoperatively had of anesthetic, temperature or blood pressure changes) can
severe motor deficits had recordable MEPs at the beginning be recognized by following these parameters and efficiently
of surgery. Postoperatively a short-term motor deteriora- communicating with the anesthesiologist.
tion was found in roughly one third of the patients (35 During surgery, D-waves and muscle MEPs indicate
out of 92: 38%). Thus, the data obtained with D-wave and some effect of the surgical manipulation on the func-
MEP-monitoring during intramedullary surgery do reflect the tional integrity of the motor pathways at some point
clinical ‘‘reality’’. In only two cases a severe permanent during the procedure in almost 50% of the cases. In
neurological dysfunction occurred as a direct result of the about one third of cases, these changes remain until
operation. Therefore the risk of paraplegia following resec- the end of the operation, and then correlate to a tem-
tion of a spinal-cord tumor is lower than commonly believed. porary motor deficit. In the remainder of cases the
These changes in clinical status are adquately reflected by changes are reversible during surgery and this correlates
the intraoperative MEP information. to intact motor function when the patient awakes from
The second question — whether or not there is a time win- anesthesia.
dow of reversible change of MEP recordings — is addressed
by the concept of ‘‘transient motor deficit’’. This concept
Interpretation of D-wave recordings
comprises correlation of a reversible motor deficit — usu-
ally leg monoparesis or paraparesis — with muscle MEP loss
The relevant parameter in D-wave interpretation is its peak-
and D-wave preservation: As long as the D-wave is pre-
to-peak amplitude.
served with sufficient amplitude, that is, an amplitude of at
The monitorability of the D-wave and the intraop-
least 50% of the baseline value, loss of muscle MEPs during
erative significant decline of its amplitude have been
intramedullary surgery is only correlating with a paraparesis,
shown to be of predictive value for the motor outcome
or, at maximal, paraplegia of finite duration. This concept
after intramedullary surgery [25]. In about two-thirds of
has been practically observed by numerous surgical groups
the patients with non-conus tumors, a D-wave is record-
and provides a ‘‘window of warning’’, during which the
able [6,25]. Since D-waves are generated by corticospinal
surgical manipulation can be adapted before a permanent
tract axons, conus tumors cannot be monitored with this
deficit occurs.
modality.
The third question — whether or not the use of MEP
Patients who have no monitorable D-wave at the begin-
monitoring indeed improves neurological outcome — has
ning of surgery have a higher risk of postoperative motor
recently been answered by a publication from Verona [23].
deficits than those with a recordable D-wave [25]. Whether
A significant number of consecutive intramedullary tumor
this is due to an inherent subclinical damage and vulner-
surgeries performed before introduction of MEP monitor-
ability of the motor tract, or to the fact that there was
ing were compared to a comparable number of consecutive
no monitoring support for the surgery, is not known. The
operations performed with monitoring. The same highly-
explanation for the absence of a recordable D-wave in an
experienced surgeon performed those operations, thereby
individual with intact motor function (and recordable mus-
virtually excluding the surgical learning curve. The result
cle MEPs) is believed to be due to a desynchronization of the
was a neurological outcome advantage for the monitored
wave [43]. This appears to occur more frequently in patients
group. Extent of resection did not differ in both groups,
with prior surgery, very extensive tumors, and particularly
documenting that the use of monitoring does not make the
those with prior radiation therapy to the spinal cord.
surgeon too ‘‘timid’’ to proceed until a tumor resection is,
The intraoperative amplitude decrease of the D-wave
indeed, complete.
correlates with postoperative outcome. If the D-wave is
unchanged, there is no permanent postoperative deficit,
Practical intraoperative neurophysiology for although there may be a transient deficit if muscle MEPs are
spinal-cord surgery lost. If the D-wave amplitude declines more than 50% of the
baseline value or even disappears, permanent paraplegia is
likely to occur [11,25].
Feasibility and practicality of monitoring
The preparation of the electrode setup on the patient is Interpretation of muscle MEPs
completed parallel to the surgical and anesthesia prepa-
ration after intubation. After positioning and during the The presence of muscle MEPs always indicates intact func-
approach, baseline recordings are obtained. Any additional tional integrity of the corticospinal tract. Occasionally, in
time requirement for monitoring preparations is moderate patients with a moderate motor deficit, it may be difficult
at most. The epidural recording electrodes are placed by to obtain recordings from both lower extremities. If that
the surgeon. Occasionally scarring from a prior surgery can occurs, usually responses in the weaker leg require higher
hinder the electrode insertion. Subdural placement can then stimulation intensities. Intraoperative preservation of mus-
be attempted as an alternative. cle MEPs means intact motor function postoperatively in all
Practically all patients without severe preoperative cases. Intraoperative loss of muscle MEPs indicates some
motor deficits can be monitored with either D-wave or mus- postoperative impairment of voluntary motor control with
cle MEPs or both. a specificity of about 90%. For instance, muscle MEP loss
The recordings are usually robust (between 10 and 70 V in one leg during the resection means that the patient will
amplitudes of epidural and up to 2 mV in muscle MEPs). postoperatively be unable to move this particular extremity
412 K.F. Kothbauer
described above and thus an acceptable limit of MEP change ticospinal pathways during scoliosis surgery with a note on
is reached (D-wave decline, loss of muscle MEPs). Although motor conduction velocities. J Neurol Neurosurg Psychiatry
the actual number of cases is low, about 5% in a previously 1986;49:251—7.
cited series [6], this is an important factor in subsequent [12] Katayama Y, Tsubokawa T, Maemjima S, Hirayama T, Yamamoto
decision making. Depending upon the actual extent of resec- T. Corticospinal direct response in humans: identification of the
motor cortex during intracranial surgery under general anes-
tion on the postoperative MRI scan and the histology of the
thesia. J Neurol Neurosurg Psychiatry 1988;51:50—9.
lesion a second stage of the resection may be attempted [13] Katayama Y, Tsubokawa T, Yamamoto T, Maejima S. Spinal cord
once the patient has recovered motor control. This is of big potentials to direct stimulation of the exposed motor cortex
importance for spinal-cord ependymomas where complete in humans: comparison with data from transcranial motor cor-
resection is the main predictor for long-term progression tex stimulation, in Rossini PM, Marsden CD (eds): Non-invasive
free survival [48]. It has been claimed that MEP monitoring stimulation of brain and spinal cord. New York: Alan R. Liss,
may be too sensitive, actually stopping resection too early Inc.; 1988. p. 305-11.
[49]. There may always be a trade-off between extent of [14] Burke D, Hicks RG, Stephen JPH. Corticospinal volleys evoked
resection and preservation of motor function in some cases. by anodal and cathodal stimulation of the human motor cortex.
But the recent study from Verona [23] clearly shows no dif- J Physiol (Lond) 1990;425:283—99.
[15] Edmonds HL, Paloheimo MPJ, Backman MH, Johnson JR, Holt
ference in the extent of resection between the monitored
RT, Shields CB. Transcranial magnetic motor evoked potentials
and the non-monitored patient groups. Therefore the con- (tcMMEP) for functional monitoring of motor pathways during
clusion can be made that spinal-cord tumors are resected at scoliosis surgery. Spine 1989;14:683—6.
least as radical and safer with than without monitoring. [16] Zentner J. Noninvasive motor evoked potential monitoring dur-
Furthermore, stable MEP recordings are encouraging the ing neurosurgical operations in the spinal cord. Neurosurgery
surgeon to proceed with tumor resection even though the 1989;24:709—12.
anatomical situation suggested otherwise. [17] Taniguchi M, Schramm J, Cedzich C. Recording of myo-
In doubt, it is still wise to err on the safe conserva- genic motor evoked potentials under general anesthesia. In:
tive side, thus to leave residual tumor behind, which may Schramm J, Møller ÅR, editors. Intraoperative neurophysiologic
be accessible to a second surgical attempt than to risk a monitoring in neurosurgery. Berlin: Springer; 1991. p. 72—87.
[18] Taniguchi M, Cedzich C, Schramm J. Modification of cortical
significant and possibly permanent neurological deficit.
stimulation for motor evoked potentials under general anes-
thesia: Technical description. Neurosurgery 1993;32:219—26.
[19] Jones SJ, Harrison R, Koh KF, Mendoza N, Crockard HA.
References Motor evoked potential monitoring during spinal surgery:
responses of distal limb muscles to transcranial cortical stim-
[1] Nash CL, Lorig RA, Schatzinger L, Brown RH. Spinal cord mon- ulation with pulse trains. Electroenceph Clin Neurophysiol
itoring during operative treatment of the spine. Clin Orthop 1996;100:375—83.
1977;126:100—5. [20] Pechstein U, Cedzich C, Nadstawek J, Schramm J. Transcranial
[2] Engler GL, Spielholz NI, Bernhard WN, Danziger F, Merkin H, high-frequency repetitive electrical stimulation for recording
Wolff T. Somatosensory evoked potentials during Harrington myogenic motor evoked potentials with the patient under gen-
instrumentation for scoliosis. J Bone Joint Surg Am 1978;60 eral anesthesia. Neurosurgery 1996;39:335—44.
A:528—32. [21] Rodi Z, Deletis V, Morota N, Vodusek DB. Motor evoked poten-
[3] Ginsburg HH, Shetter AG, Raudzens PA. Postoperative para- tials during brain surgery. Pfluger’s Archiv - European Journal
plegia with preserved intraoperative somatosensory evoked of Physiology 1996;431:R291—2.
potentials. J Neurosurg 1985;63:296—300. [22] Calancie B, Harris W, Broton JG, Alexeeva N, Green BA.
[4] Lesser RP, Raudzens P, Lüders H, Nuwer MR, Goldie WD, Threshold-level’’ multipulse transcranial electrical stimulation
Morris HH, et al. Postoperative neurological deficits may of motor cortex for intraoperative monitoring of spinal motor
occur despite unchanged intraoperative somatosensory evoked tracts: description of method and comparison to somatosensory
potentials. Ann Neurol 1986;19:22—5. evoked potential monitoring. J Neurosurg 1998;88:457—70.
[5] Epstein FJ, Farmer J-P. Pediatric spinal cord tumor surgery. [23] Sala F, Palandri G, Basso E, Lanteri P, Deletis V, Faccioli F, et
Neurosurg Clin North Am 1990;1:569—90. al. Motor evoked potential monitoring improves outcome dur-
[6] Kothbauer KF, Deletis V, Epstein FJ. Motor evoked potential ing surgery for intramedullary spinal cord tumor: A historical
monitoring for intramedullary spinal cord tumor surgery: cor- control study in 50 patients. Neurosurgery 2006;58:1129—43.
relation of clinical and neurophysiological data in a series of [24] Jasper HH. The ten twenty electrode system of the
100 consecutive procedures. Neurosurg Focus 1998;4. Article 1 international federation. Electroenceph Clin Neurophysiol
(http://www.aans.org/journals/online j/may98/4-5-1). 1957;10:371—5.
[7] Patton HD, Amassian VE. Single-and multiple unit analysis of [25] Morota N, Deletis V, Constantini S, Kofler M, Cohen H,
cortical stage of pyramidal tract activation. J Neurophysiol Epstein FJ. The role of motor evoked potentials during
1954;17:345—63. surgery for intramedullary spinal cord tumors. Neurosurgery
[8] Philips CG, Porter R. The pyramidal projection to motoneurones 1997;41:1327—36.
of some muscle groups of the baboon’s forelimb. In: Eccles JC, [26] Deletis V. Intraoperative monitoring of the functional integrity
Schadé JP, editors. Progress in Brain Research. Amsterdam: of the motor pathways. In: Devinsky O, Beric A, Dogali M, edi-
Elsevier; 1964. p. 222—43. tors. Electrical and Magnetic Stimulation of the Brain and Spinal
[9] Merton PA, Morton HB. Stimulation of the cerebral cortex in Cord. New York: Raven Press; 1993. p. 201—14.
the intact human subject. Nature 1980;285:227. [27] Deletis V, Rodi Z, Amassian VE. Neurophysiological mechanisms
[10] Levy WJ, York DH, McCaffrey M, Tanzer F. Motor evoked poten- underlying motor evoked potentials in anesthetized humans.
tials from transcranial stimulation of the motor cortex in Part 2. Relationship between epidurally and muscle recorded
humans. Neurosurgery 1984;15:287—302. MEPs in man. Clin Neurophysiol 2001;112:445—52.
[11] Boyd SG, Rothwell JC, Cowan JMA, Webb PJ, Morley T, [28] Deletis V, Isgum V, Amassian VE. Neurophysiological mech-
Asselman P, et al. A method of monitoring function in cor- anisms underlying motor evoked potentials in anesthetized
414 K.F. Kothbauer
humans. Part 1. Recovery time of corticospinal tract direct [38] Taniguchi M, Nadstawek J, Langenbach U, Bremer F,
waves elicited by pairs of transcranial electrical stimuli. Clin Schramm J. Effects of four intravenous anesthetic agents on
Neurophysiol 2001;112:438—44. motor evoked potentials elicited by magnetic transcranial
[29] Szelenyi A, Kothbauer KF, Deletis V. Transcranial electric stim- stimulation. Neurosurgery 1993;33:407—15.
ulation for intraoperative motor evoked potential monitoring: [39] Fennelly ME, Taylor BA, Hetreed M. Anaesthesia and the motor
Stimulation parameters and electrode montages. Clin Neuro- evoked potential, in: Jones SJ, Boyd S, Hetreed M, Smith NJ.,
physiol 2007;118:1586—95. (Eds.), Handbook of Spinal Cord Monitoring Proceedings of
[30] Woodforth IJ, Hicks RG, Crawford MR, Stephen JP, Burke DJ. the Fifth International Symposium on Spinal Cord Monitoring,
Variability of motor-evoked potentials recorded during nitrous London, UK, June 2-5, 1992. Dordrecht: Kluwer Academic Pub-
oxide anesthesia from the tibialis anterior muscle after lishers; 1993. p. 272-76.
transcranial electrical stimulation. Anesth Analg 1996;82: [40] Ubags LH, Kalkman CJ, Been HD. Influence of isoflurane on
744—9. myogenic motor evoked potentials to single and multiple
[31] Lang EW, Beutler AS, Chesnut FM, Patel PM, Kennelly NA, Kalk- transcranial stimuli during nitrous oxide/opioid anesthesia.
man CJ, et al. Myogenic motor-evoked potential monitoring Neurosurgery 1998;43:90—4.
using partial neuromuscular blockade in surgery of the spine. [41] McCormick PC, Torres R, Post KD, Stein BM. Intramedullary
Spine 1996;21:1676—86. ependymoma of the spinal cord. J Neurosurg 1990;72:
[32] Agnew WF, McCreery DB. Considerations for safety in the use 523—32.
of extracranial stimulation for motor evoked potentials. Neu- [42] Constantini S, Miller DC, Allen JC, Rorke LB, Freed D,
rosurgery 1987;20:143—7. Epstein FJ. Radical excision of intramedullary spinal cord
[33] MacDonald DB. Safety of intraoperative transcranial electrical tumors: surgical morbidity and long-term follow-up evalua-
stimulation motor evoked potential monitoring. J Clin Neuro- tion in 164 children and young adults. J Neurosurg (Spine)
physiol 2002;19:416—29. 2000;93:183—93.
[34] Sloan TB. Intraoperative neurophysiology and anesthesia man- [43] Deletis V, Kothbauer K. Intraoperative neurophysiology of the
agement. In: Deletis V, Shils J, editors. Neurophysiology in corticospinal tract. In: Stålberg E, Sharma HS, Olsson Y, editors.
Neurosurgery. Amsterdam: Academic Press, Elsevier Science; Spinal cord monitoring. Vienna: Springer; 1998. p. 421—44.
2002. p. 451—74. [44] Nathan PW, Smith MC. Effects of two unilateral cordotomies on
[35] Jellinek D, Jewkes D, Symon L. Noninvasive intraopera- the motility of the lower limbs. Brain 1973;96:471—94.
tive monitoring of motor evoked potentials under propofol [45] Kothbauer K, Deletis V, Epstein FJ. Motor evoked poten-
anesthesia: effect of spinal surgery on the amplitude and tial monitoring for spinal cord tumor surgery. J Neurosurg
latency of motor evoked potentials. Neurosurgery 1991;29: 1998;88:403A (abstract).
551—7. [46] Greenwood J. Surgical removal of intramedullary tumors. J
[36] Kalkman CJ, Drummond JC, Ribberink AA, Patel PM, Sano T, Neurosurg 1967;26:276—82.
Bickford RG. Effects of propofol, etomidate, midazolam and [47] Jallo GI, Kothbauer KF, Epstein FJ. Contact laser microsurgery.
fentanyl on motor evoked responses to transcranial elec- Child’s Nerv Syst 2002;18:333—6.
trical or magnetic stimulation in humans. Anesthesiology [48] Epstein FJ, Farmer J-P, Freed D. Adult intramedullary spinal
1992;76:502—9. cord ependymoma: the result of surgery in 38 patients. J Neu-
[37] Schmid UD, Boll J, Liechti S, Schmid J, Hess CW. Influence of rosurg 1993;79:204—9.
some anesthetic agents on muscle responses to transcranial [49] Albright AL. Intraoperative spinal cord monitoring for
magnetic cortex stimulation: A pilot study in man. Neuro- intramedullary surgery: an essential adjunct ? Pediatr Neuro-
surgery 1992;30:85—92. surg 1998;29:112.