Abstract
Background: Despite the many reports attesting to the efficacy of
intraoperative somatosensory evoked potential monitoring in reducing the
prevalence of iatrogenic spinal cord injury during corrective scoliosis
surgery, these afferent neurophysiological signals can provide only indirect
evidence of injury to the motor tracts since they monitor posterior column
function. Early reports on the use of transcranial electric motor evoked
potentials to monitor the corticospinal motor tracts directly suggested that
the method holds great promise for improving detection of emerging spinal cord
injury. We sought to compare the efficacy of these two methods of monitoring
to detect impending iatrogenic neural injury during scoliosis surgery.
Methods: We reviewed the intraoperative neurophysiological
monitoring records of 1121 consecutive patients (834 female and 287 male) with
adolescent idiopathic scoliosis (mean age, 13.9 years) treated between 2000
and 2004 at four pediatric spine centers. The same group of experienced
surgical neurophysiologists monitored spinal cord function in all patients
with use of a standardized multimodality technique with the patient under
total intravenous anesthesia. A relevant neurophysiological change (an alert)
was defined as a reduction in amplitude (unilateral or bilateral) of at least
50% for somatosensory evoked potentials and at least 65% for transcranial
electric motor evoked potentials compared with baseline.
Results: Thirty-eight (3.4%) of the 1121 patients had recordings
that met the criteria for a relevant signal change (i.e., an alert). Of those
thirty-eight patients, seventeen showed suppression of the amplitude of
transcranial electric motor evoked potentials in excess of 65% without any
evidence of changes in somatosensory evoked potentials. In nine of the
thirty-eight patients, the signal change was related to hypotension and was
corrected with augmentation of the blood pressure. The remaining twenty-nine
patients had an alert that was related directly to a surgical maneuver. Three
alerts occurred following segmental vessel clamping, and the remaining
twenty-six were related to posterior instrumentation and correction. Nine
(35%) of these twenty-six patients with an instrumentation-related alert, or
0.8% of the cohort, awoke with a transient motor and/or sensory deficit. Seven
of these nine patients presented solely with a motor deficit, which was
detected by intraoperative monitoring of transcranial electric motor evoked
potentials in all cases, and two patients had only sensory symptoms.
Somatosensory evoked potential monitoring failed to identify a motor deficit
in four of the seven patients with a confirmed motor deficit. Furthermore,
when changes in somatosensory evoked potentials occurred, they lagged behind
the changes in transcranial electric motor evoked potentials by an average of
approximately five minutes. With an appropriate response to the alert, the
motor or sensory deficit resolved in all nine patients within one to ninety
days.
Conclusions: This study underscores the advantage of monitoring the
spinal cord motor tracts directly by recording transcranial electric motor
evoked potentials in addition to somatosensory evoked potentials. Transcranial
electric motor evoked potentials are exquisitely sensitive to altered spinal
cord blood flow due to either hypotension or a vascular insult. Moreover,
changes in transcranial electric motor evoked potentials are detected earlier
than are changes in somatosensory evoked potentials, thereby facilitating more
rapid identification of impending spinal cord injury.
Level of Evidence: Diagnostic Level I. See Instructions
to Authors for a complete description of levels of evidence.
Iatrogenic spinal cord injury remains the most feared complication of
corrective scoliosis
surgery1-4.
It ranges from a minor sensory disturbance to
paraplegia1,2.
The potential for an intraoperative neurologic complication has become a
particular concern in recent years because of the complexity of patients with
pediatric and adult deformity having surgical treatment. As a result, there is
an ever-growing need for improved and more sophisticated spinal cord
monitoring to reduce the risk of intraoperative neurologic complications.
Prior to the mid-1970s, the only method for detecting spinal cord injury
during corrective scoliosis surgery was the Stagnara wake-up test, which
consisted of waking the patient intraoperatively and observing voluntary
lower-extremity
movement5. Although
the wake-up test is still considered by some to be the standard for assessing
global motor function, it is not without substantial
shortcomings1,2.
Salient among these is the assumption that anatomic injury occurs only at a
single point in time—namely, after the implant is placed and corrective
forces are applied (i.e., at the time when the Stagnara test is performed). Of
related importance is the fact that it can take several minutes to awaken the
patient sufficiently from the anesthesia to elicit a voluntary motor response
in all extremities. The long interval from the time of the insult to the
detection of the motor deficit not only may delay timely intervention to
reverse the injury, but also may interfere with accurate identification of the
responsible surgical
maneuver1,2.
Moreover, a spinal cord injury, particularly one related to a vascular insult,
may not present immediately following the correctional maneuvers. As a result
of such a delay in the clinical manifestation of the injury, the patient may
be able to move the lower extremities voluntarily at the time of the wake-up
test, only to demonstrate paralysis on emergence from the
anesthesia6.
Given the limitations of the wake-up test, intraoperative
neurophysiological monitoring of somatosensory evoked potentials became
commonplace in most leading pediatric and adult spine centers after
publication of the paper by Nash et al. three decades
ago7. Despite its
overwhelming historical success, however, there has been heightened concern
and debate about the adequacy of somatosensory evoked potential monitoring
alone4,8,9,
partly as a result of the broadening of surgical indications to include
patients with difficult and extensive deformities, who have an increased risk
of surgical insult to the spinal cord and its vascular
supply1. Such cases
create challenges for neurophysiological monitoring that seem to be beyond the
capability of somatosensory evoked potentials, which are mediated by the
posterior sensory columns of the spinal cord and provide no direct information
about the descending spinal cord motor tracts or the spinal cord gray
matter10.
During the last two decades, there have been a number of attempts to extend
neurophysiological monitoring to include surveillance of the dorsolateral and
ventral motor tracts of the spinal cord. Some initially promising techniques
for monitoring motor evoked potentials, such as recording of the neurogenic
descending evoked
potential11, proved
to be unreliable because it is mediated by antidromic conduction along sensory
instead of motor spinal cord
pathways12-16.
Conversely, motor evoked potentials, triggered by multipulse transcranial
electric stimulation, reflect neural transmission through corticospinal motor
tracts. Recording of transcranial electric motor evoked potentials has
recently emerged as an effective and clinically practical way to monitor
spinal cord motor function in nearly real time during corrective spine
surgery, thereby complementing somatosensory evoked potential monitoring and
taking on a primary role in the effort to prevent intraoperative neurologic
sequelae8,9,17-21.
Despite the apparent benefits of monitoring of transcranial electric motor
evoked potentials compared with somatosensory evoked potentials, many adult
and pediatric spine centers have been reluctant to incorporate that method
into their intraoperative neurophysiological monitoring regimen, in the belief
that its advantages, either alone or in addition to somatosensory evoked
potential monitoring, remain unproven in the absence of a large-scale
investigation. Presented here is our combined multicenter experience with use
of standardized multimodality spinal cord monitoring and associated uniform
anesthesia protocols. A primary goal of the study was to calculate and compare
the receiver operating characteristics (i.e., sensitivity and specificity) of
somatosensory evoked potential and transcranial electric motor evoked
potential monitoring for detection of an emerging neurologic deficit during
surgery for adolescent idiopathic scoliosis.
The study protocol was reviewed by the institutional review boards of the
Children's Hospital of Philadelphia, Alfred I. duPont Hospital for Children,
Robert Wood Johnson University Hospital, and St. Christopher's Hospital for
Children and an exempt status for anonymous retrospective chart review was
granted at all four participating institutions. The intraoperative monitoring
records, operative narratives, anesthesia records, and outpatient clinical
notes were reviewed for 1121 consecutive patients who had undergone surgical
correction of adolescent idiopathic scoliosis at the four pediatric spine
centers between January 1, 2000, and June 30, 2004. There were 834 female
patients (74%) and 287 male patients (26%) ranging in age from ten to eighteen
years old (average, 13.9 years old) at the time of surgery. The operative
reports, anesthesia records, and spinal cord monitoring records were analyzed
to determine temporal relationships between specific intraoperative events and
consequent loss in the amplitude of transcranial electric motor evoked
potentials and/or somatosensory evoked potentials and to ascertain the effect
of surgical and/or anesthesia-associated interventions initiated to reverse
those changes. Important demographic and clinical data, including age, gender,
height, weight, body-mass index, preoperative neurologic status, and
preoperative curve type and degree, were obtained from the outpatient clinical
notes. Patients with a preexisting neurologic deficit, Scheuermann disease, or
other kyphotic deformities and those with an age of less than ten or more than
eighteen years were excluded from the cohort.
Serial neurophysiological monitoring of spinal cord motor and sensory tract
function was performed, from the time that the patient was positioned to the
time that he or she was awakened from the anesthesia, by repeatedly recording
both lower and upper-extremity efferent transcranial electric motor potentials
and afferent lower-extremity (posterior tibial nerve) and upper-extremity
(ulnar nerve) somatosensory evoked potentials. The upper-extremity
transcranial electric motor and somatosensory evoked potential modalities
served both as neurophysiological monitoring controls and as techniques to
identify impending positional brachial
plexopathy22,23.
Transcranial electric motor and somatosensory evoked potential monitoring were
principal components of a broader neuromonitoring protocol, which included
spontaneous and stimulated electromyography whenever thoracic or lumbar
pedicle screw fixation was involved, electroencephalography for assessing the
depth of the anesthesia, and train-of-four peripheral nerve stimulation to
test for clearance of muscle relaxant from the neuromuscular junction. All
neuromonitoring for this study was performed by one experienced
neurophysiological monitoring group using a common, algorithmically based
standard both for consistency and improved detection
accuracy20,24.
Somatosensory Evoked Potentials
Both cortical and subcortical somatosensory evoked potentials were elicited
by a 300-µsec square-wave electrical pulse presented, in turn, to the
posterior tibial and ulnar nerves at a rate of 4.7/sec. Stimulation intensity
levels ranged from 25 to 45 mA, with intensity selected to achieve a response
amplitude within the asymptotic portion of the somatosensory evoked potential
intensity versus amplitude curve for each individual patient. Cortical
potentials were recorded from eithe gold-plated cup (Grass Instruments,
Quincy, Massachusetts) or subdermal needle (Rochester Electro-Medical, Tampa,
Florida, or Axon Systems, Hauppauge, New York) electrodes affixed to Cpz, Cp3,
and Cp4 and referenced to Fpz (International 10-20 System). Subcortical
responses were recorded similarly with electrodes placed over the surface of
the second or third cervical vertebra and also referenced to Fpz. All
stimulation and recording of somatosensory evoked potentials was performed
with use of commercially available neurophysiological monitoring workstations
(Axon EpochXP; Axon Systems; Sierra, Cadwell Laboratories, Kennewick,
Washington; or Nicolet Endeavor, Viasys Healthcare, Madison, Wisconsin).
Transcranial Electric Motor Evoked Potentials
Transcranial electric motor evoked potentials were recorded bilaterally
from the first dorsal interosseous muscles in the upper extremities (control)
and bilaterally from, at a minimum, the anterior tibialis and abductor
hallucis muscles in the lower extremities. Other sites included the rectus
abdominis, iliopsoas, adductor, quadriceps, and gastrocnemius muscles,
depending on the complexity of the curve and the incorporation and levels of
pedicle screw fixation. These myogenic responses were elicited with use of a
commercially available transcranial electrical stimulator (Digitimer D185;
Digitimer, Welwyn Garden City, United Kingdom) that delivered a brief
(50-µsec), high-voltage (250 to 500-V) anodal pulse train (two to seven
pulses with a 1 to 5-msec interstimulus interval) between two corkscrew
electrodes (A-Gram, Glenn Rock, New Jersey) inserted subcutaneously over motor
cortex regions C1-C2 (International 10-20 System). The stimulation parameter
values (i.e., the number of pulses, interstimulus interval, and voltage) were
optimized to elicit maximal response amplitudes for each patient with use of a
modified psychophysical "stair-step" paradigm; that is, stimulus
parameters were varied to achieve the maximum baseline amplitude possible for
that particular patient. Transcranial electric motor evoked potentials were
recorded with the same neurophysiology workstations used for somatosensory
evoked potential monitoring.
Anesthesia
A uniform total intravenous anesthesia maintenance routine was implemented
across all four institutions. There were slight differences only in the
initial induction; however, this had no effect on the neurophysiological
monitoring data once the spine was exposed since the anesthesia maintenance
protocol was the same across all four
institutions25.
Some, but not all, children were premedicated with oral benzodiazepine
(Versed, 0.5 mg/kg). Peripheral venous access often was accomplished with the
assistance of nitrous oxide (60% to 70%) and a low-concentration potent agent
(e.g., sevoflurane). Once peripheral venous access was established, anesthesia
was induced either through potent mask anesthesia or with an intravenous
agent. Mask induction was performed with use of sevoflurane (6.0% to 8.0%) and
nitrous oxide (60% to 70%) along with an opioid bolus (fentanyl, 2.0 to 3.0
mg/kg) and either a short-acting depolarizing (succinylcholine) or
non-depolarizing (mivacurium) muscle relaxant. Following induction and
intubation, all inhalational agents were turned off and no additional muscle
relaxant was administered for the remainder of the surgery. Alternatively,
intravenous induction was carried out with propofol (2.0 to 3.0 mg/kg)
augmented with an opioid bolus and short-acting depolarizing or
non-depolarizing neuromuscular blockade. An arterial line was placed along
with stimulating and recording electrodes for neurophysiological monitoring
following intubation. From this time forward, general anesthesia was
maintained, at all institutions, with pump-controlled intravenous infusions of
propofol (125 to 200 µg/kg/min) and remifentanil (0.1 to 0.5 µg/kg/min)
with particular effort made to achieve a stable, target mean arterial blood
pressure of at least 65 mm Hg. A small (1.0-mg) dose of Versed was sometimes
added as an adjunct for amnesia. No muscle relaxant was used following
intubation so as not to compromise transcranial electric motor evoked
potential amplitudes. Monitoring of the neuromuscular junction with use of
train-of-four stimulation of the posterior tibial nerve and recording compound
muscle action potentials from the abductor hallucis muscle ensured adequate
clearance of the relaxing agent.
Definition of Relevant Change
An intraoperative "alert," or clinically relevant
neurophysiological change, was defined as a persistent (i.e., over at least
three test trials) unilateral or bilateral loss of =65% of the amplitude of
the transcranial electric motor evoked potentials or =50% of the amplitude
of the somatosensory evoked potentials relative to a stable baseline. Defining
an alert in this manner helped to minimize the effects of response variability
on interpretation and reduced the potential for a false-positive
result26,27.
Response latency was not used to define an alert suggestive of emerging spinal
cord injury, in keeping with our experience of never having observed a
relevant latency shift as a principal sign of neurologic injury during spine
surgery24.
Intervention
A relevant amplitude change triggered a sequence of interventional steps
based on a predetermined algorithm published
elsewhere1,2,24.
If the neurophysiological change was time-related to a specific surgical
maneuver, the precipitating maneuver was promptly reversed. Regardless of
whether the change was related to a particular surgical action, the
anesthesiologist was always directed to raise the mean arterial blood pressure
to at least 90 mm Hg in order to promote better spinal cord perfusion. If,
after temporary cessation of the surgery and institution of hemodynamic
management, the response amplitude failed to show signs of recovery over the
course of ten minutes, corrective forces were reversed and a
methylprednisolone bolus of 30 mg/kg was administered, according to the
National Acute Spinal Cord Injury Study (NASCIS-2) protocol, to restrict the
effect of cord
edema28. If the
amplitude still did not improve, even after reversal of correction and implant
removal, cessation of the procedure was considered.
Statistical Analysis
Initially, all patients were divided into two broad groups: those who had
no neurophysiological changes and those who had relevant amplitude changes
warranting a surgical and/or anesthesia-related intervention. The latter group
was then divided into three subgroups: those with changes in transcranial
electric motor evoked potential amplitudes only, those with changes in
somatosensory evoked potential amplitudes only, and those with changes in both
transcranial electric motor and somatosensory evoked potential amplitudes.
An impending neurologic injury was defined a priori as a relevant
neurophysiological amplitude change, as detected by one or both of the
neuromonitoring modalities, necessitating some form of intervention, as
described previously. For the purposes of this study, calculation of test
operating characteristics (sensitivity and specificity) of the somatosensory
and transcranial electric motor evoked potentials was based on operational
definitions of evolving and new-onset injury as posited previously by
Hilibrand et al.9.
Accordingly, a true-positive alert was defined as any relevant or complete
loss of the amplitude of transcranial electric motor evoked potentials and/or
somatosensory evoked potentials indicative of an "evolving" injury
that (1) was irreversible despite all interventional measures and was followed
by a postoperative neurologic deficit or (2) responded favorably to
intervention (improved to within 25% of the initial stable baseline
value)—that is, showed neurophysiological evidence of a cause-effect
relationship. A false-positive alert was defined as any case in which the
decrease in signal amplitude could not be reversed to within 25% of the stable
baseline value, regardless of intervention, but the patient awoke without any
postoperative sensory and/or motor deficit. The result was classified as
true-negative when no critical changes were demonstrated by neuromonitoring
and the patient awoke neurologically intact. Finally, the result was
considered to be false-negative when a patient awoke with a new neurologic
deficit even though (1) the transcranial electric and/or somatosensory evoked
potentials had not changed during the operation or (2) a relevant signal
change had resolved to within 25% of baseline following intervention, thereby
suggesting a good prognosis for complete recovery.
Multimodality spinal cord monitoring was achieved successfully in 1121
consecutive patients during surgical correction of adolescent idiopathic
scoliosis. Review of medical records and nursing incidence reports revealed no
complications (e.g., seizures, cardiac arrhythmias, scalp burns, headache, or
tongue lacerations) related to transcranial electrical stimulation for
monitoring of transcranial electric motor evoked potentials. (Since this study
was completed, two self-limiting, spontaneously healing tongue lacerations
occurred in a similar population of patients treated for adolescent idiopathic
scoliosis across the same four institutions.)
Of the 1121 patients, 964 (86%) had a posterior surgical approach, 101 (9%)
had an anterior approach, and fifty-six (5%) had a combined anterior and
posterior approach.
The criteria for a relevant change in the amplitude of the transcranial
electric motor evoked potentials and/or the somatosensory evoked potentials
were met during thirty-eight (3.4%) of the 1121 procedures. Twenty-nine (76%)
of the thirty-eight patients were female and nine (24%) were male, and their
ages ranged from ten to eighteen years (mean age, 13.9 years). Nine of the
thirty-eight patients, representing 0.8% of the total series, had an alert
that was the consequence of hypotension alone. In each of these cases, there
was a >75% decrease in the amplitude of the transcranial electric motor
evoked potentials with no associated change in the somatosensory evoked
potentials. The average mean arterial blood pressure at the time of the alerts
was 59 mm Hg, which was below the target mean of at least 65 mm Hg. The
amplitudes of the transcranial electric motor evoked potentials returned to
nearly baseline values over a period of no more than five minutes following
augmentation of the blood pressure in all nine of these patients.
The remaining twenty-nine patients (2.6% of the total series) demonstrated
signal amplitude changes attributed to specific surgical maneuvers, as
depicted in Figure 1. Most
(sixteen) of the neuromonitoring alerts were associated with application of
corrective forces. In ten cases, the alert occurred during or following
placement of specific instrumentation components (e.g., sublaminar cables,
sublaminar hooks, or thoracic pedicle screws). For three patients, the
offending action was test clamping of a segmental vessel prior to ligation
during an anterior release. Of all of the vessels that underwent provocative
testing prior to ligation, it was the left T12 segmental vessel that was
associated with relevant or complete loss of the amplitude of transcranial
electric motor evoked potentials after clamping in all three patients.
All patients in whom the neurophysiological signal amplitudes decreased
relevantly as a result of either hypotension (nine) or provocative segmental
vessel testing (three) showed complete resolution of the signal changes, as
summarized in Figure 2. In the
vast majority of patients (88%) in whom the relevant amplitude loss was
associated with the application of corrective forces that can cause stretching
of the vascular supply of the spinal cord, augmentation of the blood pressure,
reduction of correction, steroid therapy, and, when necessary, removal of
instrumentation led to a return of the response. Conversely, patients who had
a sudden loss of amplitude secondary to more direct injury responded less
favorably to intervention, with resolution occurring in three of the five
cases in which the alert followed tightening of a sublaminar cable and none of
the five cases in which it followed insertion of a mid-high thoracic laminar
hook or pedicle screw.
Neurologic Deficits
An instrumentation-related alert was detected in twenty-six patients. Nine
(35%) of them awoke from the surgery with a new postoperative neurologic
deficit despite all interventional efforts. Hence, the overall prevalence of
iatrogenic neurologic sequelae in this consecutive series of 1121 patients
treated for adolescent idiopathic scoliosis was 0.8%. Events leading to loss
in the amplitude of the neurophysiological response included deep hook
penetration (four), passing or tensioning of a sublaminar cable (two), and
spinal distraction and/or derotation (three). The type of deficit was
unilateral motor in four of these nine patients, bilateral motor in two,
unilateral sensory in one, bilateral sensory in one, and bilateral combined
sensory and motor in one. The prevalence of motor or sensorimotor impairment
was 0.62%, and the prevalence of pure sensory impairment was 0.18%. All
neurologic deficits resolved between twenty-four hours and ninety days
postoperatively.
The amplitude of lower-extremity transcranial electric motor evoked
potentials decreased by >80% in the absence of any signal changes in the
upper-extremity controls in all seven patients who presented with a motor
deficit alone or combined sensorimotor impairment. The average magnitude of
improvement in the amplitude of the transcranial electric motor evoked
potentials in those patients, even after release of correction or complete
removal of instrumentation, was marginal. At best, responses remained reduced
by 75% compared with the baseline value. The sensitivity and specificity of
monitoring of transcranial electric motor evoked potentials for identification
of motor loss were each 100%. The mean duration between the detection of the
change in the transcranial electric motor evoked potential amplitudes and the
completion of the surgery was forty-one minutes (range, twenty-five to more
than sixty minutes).
In contrast to the transcranial electric motor evoked potentials, the
amplitude of the posterior tibial nerve somatosensory evoked potentials had
decreased relevantly in only three of the seven patients who had postoperative
motor weakness. When changes were detected by both modalities, the changes in
the somatosensory evoked potentials lagged behind those in the transcranial
electric motor evoked potentials by approximately five minutes (range, zero to
ten minutes). Following intervention, somatosensory evoked potential
amplitudes eventually improved to within 35% of the baseline values, although
the changes persisted for an average of twenty-five minutes (range, four to
thirty-seven minutes). The sensitivity and specificity of the somatosensory
evoked potentials for identification of motor loss, therefore, were 43% and
100%, respectively.
The amplitude of the posterior tibial nerve somatosensory evoked potentials
decreased relevantly in both patients who presented with a pure sensory
deficit and the one patient with sensorimotor impairment. The sensitivity and
specificity of somatosensory evoked potentials for the identification of
sensory loss, therefore, were each 100%.
Of the seventeen remaining patients with an instrumentation-related alert,
all had signal improvement to within 25% of the baseline amplitude following
intervention. Ten of these seventeen patients had changes in the transcranial
electric motor evoked potentials only, without concomitant attenuation of
somatosensory evoked potentials. In the remaining seven patients, the changes
in the somatosensory evoked potentials again tended to lag behind those in the
transcranial electric motor evoked potentials. None of these seventeen
patients awoke with a neurologic deficit, which was consistent with the
magnitude of the signal improvements.
Table I summarizes the
various demographic and clinical characteristics of the patients who did not
have a neuromonitoring alert and those who did. In general, there were no
clinically remarkable differences between the groups with regard to any of the
parameters. Although there were minor differences in body weight, body mass,
and curve magnitude between the groups, none appeared to represent significant
(p < 0.05) predisposing factors for changes identified by
neurophysiological monitoring or for spinal cord injury.
Team Response to Neuromonitoring Alerts
The interventional efforts on the part of surgical and anesthesia personnel
to the thirty-eight intraoperative alerts most commonly included a surgical
pause (mean, 8.7 minutes) and correction of
hypotension24. The
average mean arterial blood pressure at the time of the intraoperative alert
identifying the changes in the transcranial electric motor evoked potentials
and/or somatosensory evoked potentials was 55 mm Hg, well below the desired
target pressure of 65 mm Hg. On the average, the mean arterial blood pressure
was elevated to 91 mm Hg to facilitate an increase in spinal cord blood flow.
If neurophysiological signals failed to improve following elevation of the
mean arterial blood pressure, applied correction was reduced or anchoring
hardware was removed. If there still was no indication of adequate signal
improvement, a steroid bolus was
administered24.
Finally, if there was no noticeable neurophysiological improvement in response
to all other forms of intervention, the spinal implant was removed.
In 1992, the Scoliosis Research Society published a position paper stating
that spinal cord monitoring of somatosensory evoked potentials should be
considered the standard of care for scoliosis
surgery29. Despite
the overall success of somatosensory evoked potential monitoring in reducing
the incidence of iatrogenic spinal cord injury, there have been a number of
noteworthy reports of false-negative findings with this
modality4,9,16,30-36.
While many of these were single case presentations, others were large,
multicenter
surveys35.
Because contemporary scoliosis surgery involves the use of more
sophisticated instrumentation constructs for complex deformities, the
possibility of a false-negative result of somatosensory evoked potential
monitoring is a concern. Over the course of the last decade, advances in
intraoperative monitoring have demonstrated the feasibility of real-time
intraoperative monitoring of the corticospinal tract by recording transcranial
electric motor evoked potentials. The results of the present study provide
convincing evidence that transcranial electric motor evoked potentials are
more sensitive than somatosensory evoked potentials to evolving spinal cord
injury during scoliosis surgery. Monitoring of transcranial electric motor
evoked potentials was 100% sensitive in identifying the seven patients who
subsequently awoke with a transient or short-term neurologic deficit, whereas
the sensitivity of somatosensory evoked potential monitoring was only 43%.
This finding is entirely consistent with those of other
studies8,9,37.
To our knowledge, this is the largest reported series of patients in whom
both transcranial electric motor evoked potentials and somatosensory evoked
potential were monitored. Pelosi et al. reported that three (2.4%) of 126
patients who had undergone corrective spinal surgery awoke with a new-onset
motor deficit that had not been detected by somatosensory evoked potential
monitoring37. In
contrast, all of the deficits were identified correctly with monitoring of
transcranial electric motor evoked potentials. Similarly, in their study of
427 monitored anterior cervical spine procedures, Hilibrand et
al.9 described
patients who awoke with a transient motor deficit despite unaltered
somatosensory evoked potential amplitudes, whereas all of the deficits were
identified with monitoring of transcranial electric motor evoked potentials.
With a few notable exceptions, wide variations in monitoring technique and a
lack of a consistent, optimized total intravenous anesthetic regimen have
previously confounded results of, or precluded careful comparison of, these
two monitoring modalities. These same confounding factors also make it
difficult to compare the results of previous studies with those in the present
series8,17,37-39.
Unique to this investigation was the use of a standardized monitoring
protocol across a large, relatively homogeneous patient population. Given the
low prevalence of neurologic sequelae, a large patient sample was needed to
permit calculation of the sensitivity and specificity of the two monitoring
modalities of interest. A special effort was made to manage anesthesia
consistently at the four pediatric spine surgery centers, which allowed
meaningful comparison of results across institutions. Transcranial electric
motor and somatosensory evoked potentials were recorded in patients treated
with a total intravenous anesthesia regimen tailored to optimize response
amplitudes and reduce response variability. Specifically, a strictly regulated
anesthesia maintenance protocol removed the uncertainty that is often
associated with clinical decision-making based on neuromonitoring done in the
presence of nitrous oxide, potent inhalational agents, and partial muscle
relaxation. While it may be possible to record neurophysiological signals in
the presence of these agents, there is a cost in the form of smaller and more
variable responses, which adds to interpretive ambiguity. The use of these
anesthetic agents is perhaps the biggest reason why many surgeons and
neurophysiologists complain of difficulty in establishing stable and
acceptable transcranial electric motor evoked potential (minimum, 100 µV)
and somatosensory evoked potential (minimum, 1 µV) amplitudes.
All spinal cord monitoring for this study was performed by one group of
surgical neurophysiologists with graduate degree and an average of fourteen
years (range, ten to twenty-seven years) of experience, which may have
improved interpretation
accuracy35,40.
This opinion is supported by the study by Nuwer et
al.35 as well as a
recent study of factors affecting the reliability of interpretations of
intraoperative somatosensory evoked potentials by Stecker and
Robertshaw40. The
authors of both of those investigations concluded that the accuracy of the
interpretation of data derived with somatosensory evoked potential monitoring
correlates highly with the level of education and years of monitoring
experience. Clinical experience, educational level, and the level of clinical
decision-making skills may be even more important factors affecting recording
and interpretation of transcranial electric motor evoked potentials, which
appear to require more advanced academic knowledge and more sophisticated
clinical skills than are necessary for somatosensory evoked potential
monitoring alone.
Of the 1121 patients in this investigation, nine presented with a new-onset
neurologic deficit postoperatively, for a prevalence of 0.8%. While the
percentage of postoperative neurologic sequelae is in keeping with previously
reported estimates, the neurologic injuries may have been less severe in this
series41,42.
All patients recovered within one to ninety days, in contrast to reports of
permanent motor and/or sensory loss in these other studies. One possible
explanation for this finding is that the greater sensitivity of transcranial
electric motor evoked potentials to ischemic change may have facilitated a
more rapid reaction to, and reversal of, an evolving injury. In addition to
having better sensitivity, monitoring of transcranial electric motor evoked
potentials also demonstrated emerging spinal cord motor injury an average of
five minutes earlier than did monitoring of somatosensory evoked potentials in
cases in which both modalities showed changes.
The differential sensitivities of transcranial electric motor evoked
potentials and somatosensory evoked potentials to evolving spinal cord injury
may be related to differences in the neural pathways that mediate these
responses and to the mechanism of spinal cord injury. In contrast to
somatosensory evoked potentials, transcranial electric motor evoked potentials
are mediated by pathways that have critical synaptic junctures within the
spinal cord. Anterior horn motor neurons within the spinal cord and spinal
motor interneurons, in particular, have a high metabolic rate, making the
anterior horn gray matter and spinal motor system highly vulnerable to
ischemic injury43.
The vascular supply to the motor pathways is also less redundant than is the
supply to the posterior sensory columns, adding to this vulnerability. Since
most neurologic injuries during scoliosis surgery appear to be related to
ischemia, transcranial electric motor evoked potentials are more likely to
change under these conditions than are somatosensory evoked potentials.
Transcranial electric motor evoked potentials have been shown to be
exquisitely sensitive to spinal cord ischemia during both aortic and spinal
operations, making them ideal markers of an impending neurologic
deficit2,3,9,10,44.
Timely recognition of a vascular injury affords the opportunity to augment
blood pressure systemically or to reverse the offending surgical
maneuver1-3,10,24,25.
Failure or delay in detection of an intraoperative neurophysiological event,
and the missed opportunity for rapid intervention, can lead to a permanent
neurologic deficit.
One of the major limitations of this study was that delayed postoperative
neurologic deficits were not evaluated to determine whether there were any
subtle neurophysiological monitoring markers that might be used to identify
patients at higher risk for such deficits. These delayed injuries can occur
for a variety of reasons. One mechanism is postoperative spinal cord swelling,
which compromises the vascular supply. In these patients, data derived with
intraoperative monitoring of transcranial electric motor evoked potentials
correlate well with the neurologic status immediately following emergence from
anesthesia, in that a lack of change in transcranial electric motor evoked
potentials at the time of wound closure is consistent with uncompromised motor
function and the patient's ability to move the lower extremities voluntarily.
Later in the postoperative period, however, motor strength may deteriorate
acutely. If the patient is returned to the operating room, transcranial
electric motor evoked potentials show either a partial or a complete loss in
amplitude consistent with the clinically observed neurologic deficit. To
minimize the potential for a delayed-onset motor deficit, special care is
taken to ensure normotension or slightly elevated mean blood pressures (80 to
90 mm Hg) during the immediate recovery period.
In some cases, delayed postoperative neurologic deficits may be related to
periods of prolonged intraoperative hypotension, particularly during spinal
instrumentation and correction. Experience suggests that all too often,
adolescents undergoing scoliosis correction may have volume depletion prior to
as well as during surgery, thereby making the achievement and maintenance of a
target mean arterial blood pressure of =65 mm Hg during anesthesia more
challenging. Treatment of hypotension with an alpha-agonist such as
Neo-Synephrine (phenylephrine) usually offers only a temporary solution and
may have the undesirable effect of encouraging a repeating pattern of
hypotension followed by loss in the amplitude of transcranial electric motor
evoked potentials followed by temporary elevation of the mean arterial blood
pressure leading to resolution of the response. It is usually more productive
to address issues related to volume depletion, blood loss, and the associated
hematocrit proactively in order to ensure adequate blood pressure and
hemodynamic stability. Finally, given the sensitivity of the spinal cord to
ischemic injury, avoidance of prolonged, aggressive, controlled hypotension to
minimize blood loss is recommended. The anesthesia team routinely is advised
to maintain a mean arterial blood pressure of =65 mm Hg once the spine is
exposed and the instrumentation phase begins.
Despite successful spinal cord monitoring of transcranial electric motor
evoked potentials in many large spine centers, this modality has not yet
achieved widespread popularity. In fact, there continues to be opposition to
its routine use based on concerns about inadequate safety, particularly in
children. There is now ample experience and evidence to suggest that
transcranial electric stimulation for triggering of motor evoked potentials is
safe across all age
groups45-47.
In conclusion, the results of this study show that transcranial electric
motor evoked potentials are more sensitive than somatosensory evoked
potentials in detecting evolving spinal cord injury during corrective
scoliosis surgery and support the use of the technique as the primary
monitoring modality during these procedures. These data should not be
interpreted as suggesting that recording of somatosensory evoked potentials no
longer has a place in spinal cord monitoring. Somatosensory evoked potential
monitoring complements transcranial electric motor evoked potential monitoring
by being sensitive to injury limited to the posterior sensory columns, as was
illustrated by two of the nine cases in which there was a sensory deficit in
our study. Moreover, somatosensory evoked potentials can provide confirmation
of global spinal cord injury that is suggested by changes in transcranial
electric motor evoked potentials. Given the 100% specificity of monitoring of
somatosensory evoked potentials, interventional measures are warranted when
there is a >50% loss of the amplitude. These data also led us to the
conclusion that somatosensory evoked potential monitoring alone can no longer
be viewed as the neurophysiological standard for intraoperative detection of
emerging spinal cord injury during corrective spine surgery.
In addition to providing rapid detection of emerging spinal cord injury,
transcranial electric motor evoked potential monitoring has also fostered a
better understanding of the mechanisms of spinal cord injury and the vascular
physiology of the spinal cord. Early detection affords the surgical team an
opportunity to perform rapid intervention to prevent injury progression or
possibly to reverse impending neurologic sequelae. Continued research should
further clarify the pathophysiology of instrumentation-related contusive or
ischemic insults. Retrospective analysis of data derived with multimodality
intraoperative neurophysiological monitoring may lead to a better
understanding of nonoperative factors, such as hypovolemia, that may
predispose some children to hypotension and increase the risk of ischemic
myelopathy. ?
Note: The authors thank Yaser El-Gazzar, BA, Drexel University
College of Medicine, Philadelphia, Pennsylvania, and Thomas McPartland, MD,
Division of Orthopaedic Surgery, Robert Wood Johnson Medical School,
University of Medicine and Dentistry of New Jersey, New Brunswick, New Jersey,
who were responsible for retrieving, reviewing, and collating the surgical,
medical, and demographic data used in this investigation. They also recognize
the editorial contributions of Anthony K. Sestokas, PhD, whose critique of an
earlier draft strengthened this manuscript. Lastly, they thank the
anesthesiologists and orthopaedic operating room staff at the four pediatric
hospitals and the surgical neurophysiologists at Surgical Monitoring
Associates for their professional excellence and team approach to patient
care.
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