Abstract
Background: There has been little enthusiasm for somatosensory
evoked potential monitoring in cervical spine surgery as a result, in part, of
the increased risk of motor tract injury at this level, to which somatosensory
monitoring may be insensitive. Transcranial electric motor evoked potential
monitoring allows assessment of the motor tracts; therefore, we compared
transcranial electric motor evoked potential and somatosensory evoked
potential monitoring during cervical spine surgery to determine the temporal
relationship between the changes in the potentials demonstrated by each type
of monitoring and neurological sequelae and to identify patient-related and
surgical factors associated with intraoperative neurophysiological
changes.
Methods: Somatosensory evoked potential and transcranial electric
motor evoked potential data recorded for 427 patients undergoing anterior or
posterior cervical spine surgery between January 1999 and March 2001 were
analyzed. All patients who showed substantial (at least 60%) or complete
unilateral or bilateral amplitude loss, for at least ten minutes, during the
transcranial electric motor evoked potential and/or somatosensory evoked
potential monitoring were identified.
Results: Twelve of the 427 patients demonstrated substantial or
complete loss of amplitude of the transcranial electric motor evoked
potentials. Ten of those patients had complete reversal of the loss following
prompt intraoperative intervention, whereas two awoke with a new motor
deficit. Somatosensory evoked potential monitoring failed to identify any
change in one of the two patients, and the change in the somatosensory evoked
potentials lagged behind the change in the transcranial electric motor evoked
potentials by thirty-three minutes in the other. No patient showed loss of
amplitude of the somatosensory evoked potentials in the absence of changes in
the transcranial electric motor evoked potentials. Transcranial electric motor
evoked potential monitoring was 100% sensitive and 100% specific, whereas
somatosensory evoked potential monitoring was only 25% sensitive; it was,
however, 100% specific.
Conclusions: Transcranial electric motor evoked potential monitoring
appears to be superior to conventional somatosensory evoked potential
monitoring for identifying evolving motor tract injury during cervical spine
surgery. Surgeons should strongly consider using this modality when operating
on patients with cervical spondylotic myelopathy in general and on those with
ossification of the posterior longitudinal ligament in particular.
Level of Evidence: Diagnostic study, Level I-1 (testing
of previously developed diagnostic criteria in series of consecutive patients
[with universally applied reference "gold" standard]). See
Instructions to Authors for a complete description of levels of evidence.
Neurophysiological monitoring is used during spine surgery to assess the
function of the spinal cord and to identify any evolving iatrogenic spinal
cord injury. Studies of patients undergoing surgery for scoliosis and
thoracolumbar injuries have demonstrated that continuous somatosensory evoked
potential (SSEP) monitoring can reduce the risk of iatrogenic
paraplegia1-7.
Despite the success of identification of iatrogenic injury with SSEP
monitoring during operations for the correction of scoliosis and other
corrective operations on the thoracic spine, SSEPs are mediated primarily by
the dorsal sensory spinal cord tracts. As such, the diagnosis of an impending
motor tract injury based on changes in SSEP amplitude and/or latency is
presumptive at best. Hence, there is the risk of a false-negative
result8-13.
Although transcranial electric motor evoked potential (tceMEP) monitoring
has shown great promise with regard to more rapid identification of
corticospinal tract injury during excision of spinal cord tumors or correction
of
scoliosis14-20,
there is a dearth of information related to its use to monitor motor tract
function during cervical spine
surgery21,22.
Hence, this study was designed to determine and compare the sensitivity and
specificity of tceMEP and conventional SSEP monitoring for detection of
impending spinal cord injury during cervical spine surgery; to determine the
temporal relationship between the changes demonstrated by these two monitoring
modalities and subsequent, clinically important neurological sequelae, and to
identify patient-related and surgical risk factors associated with
intraoperative changes in these evoked potentials.
The protocol for this study was reviewed by the institutional review board
of Thomas Jefferson University Hospital and was granted an exempt status
because it was an anonymous retrospective chart review. Outcomes data for all
cervical spine surgical procedures performed with multimodality spinal cord
monitoring between January 1, 1999, and March 31, 2001, at a single
institution were reviewed. A total of 427 procedures were performed in 242
male patients (57%) and 185 female patients (43%) ranging in age from fifteen
to ninety-five years, with an average age of fifty years, at the time of the
index procedure. There were 324 anterior, eighty-three posterior, and twenty
combined anterior and posterior procedures. Of the 427 patients, 216 (51%)
presented with a preoperative diagnosis of cervical spondylotic myelopathy,
and twenty-two (10%) of the 216 had ossification of the posterior longitudinal
ligament. Intraoperative records were examined in an attempt to identify the
operative event that correlated with the neurophysiologic change as well as
the effect of surgical and/or anesthesia-related intervention on the changes
demonstrated by monitoring. Hospital and office charts were also reviewed to
determine the preoperative diagnoses as well as the preoperative, immediate
postoperative, and most recent neurological data. The anesthesia protocol used
during the study period is described in detail in the Appendix.
Spinal Cord Monitoring
Spinal cord monitoring was performed continuously, from the time of
induction of anesthesia until the patient emerged from the anesthesia, by
recording both upper and lower-extremity efferent transcranial electric motor
(tceMEPs) and afferent somatosensory evoked potentials (SSEPs). Cortical and
subcortical SSEPs were elicited to a 300-µS square-wave electrical pulse
presented sequentially to the posterior tibial and ulnar nerves at a rate of
4.7/sec. Stimulation intensity levels ranged between 35 and 50 mA. These
levels were selected as being well within the asymptotic portion of the SSEP
intensity versus amplitude plot for each patient. Cortical potentials were
recorded from gold-plated cup electrodes (Grass Instruments, Quincy,
Massachusetts) affixed to Cpz, Cp3, and Cp4 and referenced to Fpz
(international 10-20 system). Subcortical cervical/brainstem responses were
recorded over the surface of the C2 or C3 vertebra and also referenced to Fpz.
Commercially available neurophysiology instrumentation (Nicolet Endeavor;
Nicolet Biomedical, Madison, Wisconsin, or Cadwell Sierra; Cadwell
Laboratories, Kennewick, Washington) was used for all SSEP stimulation and
recording.
Transcranial electric motor evoked potentials were recorded over the first
dorsal interosseous muscle in the upper extremities and both tibialis anterior
and abductor hallucis muscles in the lower extremities following a
brief-duration, high-voltage (400 to 1000-V) anodal electrical stimulus train
(pulse width = 50 µS, N = 3 to 7, interpulse interval = 1 to 5 msec). The
multipulse stimulus was delivered between two corkscrew-type electrodes
(A-Gram, Glenn Rock, New Jersey) inserted over motor cortex regions at C1 and
C2 (international 10-20 system). Stimuli were delivered through a commercially
available transcortical stimulator (D185; Digitimer, Welwyn Garden City,
United Kingdom) with responses recorded on the same system used for monitoring
SSEPs.
Response Interpretation
A clinically relevant neurophysiological change was defined as an
intraoperative unilateral or bilateral amplitude loss of at least 60% with
persistence over at least a ten-minute duration. This cutoff value, equating
to a greater than 2.0 standard deviation criterion for a major change, was
selected to reduce the possibility of false-positive interpretation due to
response variability, as reported by York et
al.23. If such a
change in evoked potentials was detected, anesthesia personnel were directed
to increase the patient's mean arterial pressure to at least 90 mm Hg. A
failure of the response amplitude to improve over the course of five to ten
minutes led to the administration of so-called spinal-cord-injury steroids
consisting of high-dose methylprednisolone (NASCIS-2 [National Acute Spinal
Cord Injury Study-2] protocol: 30 mg/kg bolus followed by 5.4 mg/kg/hr for 23
hr)24,25.
If the change in the evoked potentials was temporally associated with
placement of a bone graft or internal fixation, surgical intervention included
removal of the graft or fixation as well.
Statistical Methods
The accuracy of the monitoring with regard to detecting impending
iatrogenic spinal cord injury was expressed by calculating sensitivity and
specificity. We defined an impending injury as any important
neurophysiological change that prompted some type of intervention (for
example, increasing the mean arterial pressure, administering steroids, or
removing bone graft). A true-positive result was defined as any case in which
the changes in the evoked potentials were reversed immediately by the
intervention or in which the changes persisted and the patient awoke with a
new neurological deficit. A false-positive result was defined as any case in
which the changes in the evoked potentials did not respond to intervention and
the patient awoke neurologically intact. A true-negative result was defined as
a case in which monitoring revealed no changes and there was no new
postoperative deficit. A false-negative result was defined as the new onset of
a neurological deficit in a patient who had had no change in the
neurophysiological monitoring data or in whom the change had resolved to a
value within 2.0 standard deviations of the original baseline value following
an intervention or by the end of the surgical procedure.
In addition, the Fisher exact probability test was used to assess whether
the presence of cervical spondylotic myelopathy with or without ossification
of the posterior longitudinal ligament was associated with changes
demonstrated by spinal cord monitoring.
Twelve (2.8%) of the 427 procedures met the criteria for a persistent
neurophysiological change. The changes occurred in eight men and four women
who ranged in age from thirty-nine to sixty-five years (mean, fifty-four
years) at the time of the index procedure. Two of the twelve patients, one man
and one woman, emerged from the anesthesia with a new neurological deficit.
Hence, the point prevalence of iatrogenic neurological injury in this series
of patients treated with cervical spine surgery was 0.47%.
Operating Characteristics
The 2 × 2 contingency tables used to calculate the sensitivity and
specificity of the tceMEP and SSEP monitoring are presented in Tables
I and
II. Both the sensitivity and
the specificity of tceMEP monitoring were 100%. The sensitivity of the SSEP
monitoring, however, was only 25%, although the specificity was 100%. Of the
twelve patients with substantial tceMEP amplitude change, two emerged from
anesthesia with a motor deficit. One presented with a dense lower-extremity
paraplegia, which did not improve subsequently, and the other had transient
but clinically evident upper-extremity weakness. Both patients had complete
acute bilateral or unilateral loss of the tceMEPs that never recovered,
despite intraoperative intervention. Only one of these patients, however, had
a concomitant SSEP amplitude loss, and that change lagged behind the onset of
the tceMEP changes by thirty-three minutes.
Four additional patients had acute tceMEP amplitude loss of 80% or greater
that necessitated surgical intervention. The precipitating etiology was
attributed to spinal distraction immediately following insertion of a strut
graft. In all four procedures, the tceMEP amplitudes reverted to near-baseline
values only after the graft was removed. During three of the four procedures,
there was a delay of three to seventeen minutes between the detection of
changes by the tceMEP monitoring and the detection of changes by the SSEP
monitoring. One patient, who had a complete loss of tceMEPs following
insertion of a strut graft, had stable SSEP amplitudes, which were classified
as a false-negative SSEP finding. In the remaining six patients, tceMEP
amplitude changes responded to an increase of the mean arterial pressure to 90
mm Hg or more and the administration of a methylprednisolone bolus. All six
patients had completely stable, unchanged SSEP amplitudes. In the four
patients in whom major changes were detected by both modalities, the SSEP
changes lagged behind the tceMEP changes by three to thirty-three minutes.
Hence, although the specificity of the SSEP monitoring was equivalent to that
of the tceMEP monitoring, the temporal differences were clinically
important.
Exemplary Case
A patient with cervical spondylotic myelopathy and ossification of the
posterior longitudinal ligament underwent C4-C6 corpectomy with anterior
strut-grafting from C3 to C7 (Figs.
1-A and
1-B). He had stable ulnar and
posterior tibial nerve SSEPs throughout the multilevel decompression and
placement of the strut graft, with no changes relative to the baseline
(Fig. 1-A). On the basis of the
SSEP recordings alone, this would have been considered an uneventful surgical
procedure, with no untoward neurological consequences predicted. The tceMEP
data (Fig. 1-B), however,
demonstrated that, on placement of the strut graft, there was an acute loss of
upper and lower-extremity motor potentials on the right side, accompanied by
decreases in amplitude on the left side. This time-locked neurophysiological
event prompted an immediate response to try to prevent the evolving spinal
cord injury. Intervention included raising the mean arterial pressure to 93 mm
Hg, removing the strut graft, and administering spinal-cord-injury steroids.
Shortly thereafter, the tceMEPs reappeared, and there was a continuous
increase in amplitude toward baseline values over the course of the next ten
minutes. A shortened graft was reinserted, with no more events. The patient
awoke without any new neurological deficits.
Diagnostic Risk Factors
Because of its frequency of occurrence, cervical spondylotic myelopathy
with or without ossification of the posterior longitudinal ligament emerged as
a prominent risk factor for iatrogenic injury during cervical spine surgery.
The 2 × 2 contingency tables used to perform the Fisher exact
probability test comparing patients with and without cervical spondylotic
myelopathy and comparing those with and without ossification of the posterior
longitudinal ligament are presented in Tables
III and
IV. The results of that
analysis indicated a significantly greater likelihood (p = 0.0057) that
patients with myelopathy would have intraoperative monitoring events than
would patients without myelopathy. Similarly, the presence of ossification of
the posterior longitudinal ligament was an additional risk factor, although
the significance was weaker (p = 0.02). Thus, among patients with myelopathy,
those with ossification of the posterior longitudinal ligament were at a
higher risk for emerging intraoperative spinal cord injury than were those
without ossification of the posterior longitudinal ligament.
Many spine surgeons who use anterior cervical approaches have been
reluctant to use SSEP monitoring, fearing a false-negative result because the
SSEP response is mediated primarily from the dorsal sensory rather than the
ventral motor tracts of the spinal cord. Selective injury to the anterior
portion of the spinal cord may be a greater risk during anterior cervical
spine surgery than it is during posterior scoliosis surgery. Monitoring the
corticospinal tracts following transcranial electrical stimulation has shown
great promise for the real-time identification of iatrogenic intraoperative
injury to the descending spinal-motor pathway. To our knowledge, however,
there has been no large-scale investigation to determine the sensitivity and
specificity of tceMEPs compared with SSEPs for monitoring the function of the
spinal cord during cervical spine surgery.
The clinical goal of any diagnostic modality is both high sensitivity (a
low false-negative rate) and high specificity (a low false-positive rate);
however, it is often difficult to achieve one without sacrificing the other.
For example, May et
al.26 reported a
sensitivity of 99% at the cost of only 27% specificity with the use of SSEP
monitoring in 191 patients undergoing cervical spine surgery. This suggests
that defining a major change too liberally so that it encompasses the wide
range of normal variability will result in a high false-positive rate in a
population of patients with a low likelihood of neurological compromise. A
high sensitivity (a low threshold for a remarkable change) can be disruptive
to the surgical procedure if it produces too many false-positive results.
Alternatively, too strict a cutoff criterion might decrease the likelihood of
false-positive results but increase the possibility of false-negative
findings.
Because of the statistical variability surrounding SSEP recordings and the
influence of anesthesia on both SSEPs and
tceMEPs23,27-31,
we used a cutoff criterion of 60% or greater loss of amplitude (more than 2.0
standard deviations) and we carefully controlled the anesthesia, eliminating
all inhalational agents. We found that tceMEP monitoring was both 100%
sensitive and 100% specific. It is important to note that, in all procedures
during which a major neurophysiological change resulted in a surgical alert,
the tceMEP amplitude change was 80% or greater. Moreover, of the twelve
patients considered to have had a tceMEP change, ten responded favorably to
intervention, with prompt neurophysiological improvement, and all ten awoke
with no untoward deficit. Conversely, the two patients who had postoperative
paralysis had not had such improvement after intraoperative intervention. The
sensitivity of SSEP monitoring, with use of a cutoff criterion that accounted
for inherent variability, was unacceptably low (25%), although the specificity
was 100%. This high false-negative rate for injury detection justifies the
lack of enthusiasm that most surgeons have for monitoring cervical spine
surgery with SSEPs. Indeed, Jones et
al.32 recently
reported two cases of quadriparesis following anterior cervical discectomy
despite normal, unchanged SSEPs.
Another important finding was the temporal relationship between tceMEP and
SSEP amplitude changes. During the four procedures in which SSEP amplitude
changed in concordance with the changes in the tceMEPs, the SSEP signal
alterations lagged behind those of the tceMEPs by an average of sixteen
minutes. In fact, one of the two patients who awoke with new-onset paralysis
had a thirty-three-minute delay between the tceMEP alert and the SSEP
detection. Such a delay between injury evolution and monitoring alert reduces
the window of opportunity for intervention and may prevent or compromise
reversal of spinal cord injury.
An additional factor that appeared to play a critical role was the mean
arterial blood pressure and its effect on spinal cord perfusion pressure. In
six of the twelve patients with a major tceMEP change, the monitoring
amplitudes reverted to baseline within five minutes of raising the mean
arterial pressure to 90 mm Hg or more. Another four of the twelve cases of
tceMEP changes occurred during strut-grafting, suggesting that an oversized
graft may have caused excessive distraction with stretching of the vascular
supply of the spinal cord. Clearly, maintenance of adequate spinal cord
perfusion is important during cervical spine surgery, particularly at times
when stress is placed on the spinal cord, such as during decompression and
strut-grafting. When a loss of tceMEP amplitude is noted during a procedure,
we recommend raising the mean arterial pressure to at least 90 mm Hg prior to
strut-graft revision and reinsertion.
In this study, we also identified preoperative patient-related risk factors
associated with changes demonstrated by intraoperative monitoring. All but one
of the twelve patients who had tceMEP changes had a preoperative diagnosis of
cervical spondylotic myelopathy, and four of them also presented with
ossification of the posterior longitudinal ligament. Statistical analysis
demonstrated that the likelihood of intraoperative monitoring detecting
changes was greater in patients with myelopathy in general, and in those with
ossification of the posterior longitudinal ligament in particular, than it was
in patients who did not have myelopathy. It would appear, therefore, that
special attention must be given to ensuring adequate spinal cord perfusion in
these patients.
A table showing the anesthesia protocol used during the study period is
available with the electronic versions of this article, on our web site at
(go to the article citation and click on "Supplementary Material")
and on our quarterly CD-ROM (call our subscription department, at
781-449-9780, to order the CD-ROM).
Note: The authors thank Evelyn Redtree, MS, CCC-A, for her data
collection and analysis and for her editorial expertise in preparing this
manuscript for publication.
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