A new criterion for the alarm point using a combination of waveform amplitude and onset latency in Br(E)-MsEP monitoring in spine surgery

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  • 1 Department of Orthopaedic Surgery, Nagoya University Graduate School of Medicine, Showa-ku, Nagoya; and
  • | 2 Department of Orthopaedic Surgery, Anjo Kosei Hospital, Anjo, Aichi, Japan
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OBJECTIVE

Monitoring of brain evoked muscle-action potentials (Br[E]-MsEPs) is a sensitive method that provides accurate periodic assessment of neurological status. However, occasionally this method gives a relatively high rate of false-positives, and thus hinders surgery. The alarm point is often defined based on a particular decrease in amplitude of a Br(E)-MsEP waveform, but waveform latency has not been widely examined. The purpose of this study was to evaluate onset latency in Br(E)-MsEP monitoring in spinal surgery and to examine the efficacy of an alarm point using a combination of amplitude and latency.

METHODS

A single-center, retrospective study was performed in 83 patients who underwent spine surgery using intraoperative Br(E)-MsEP monitoring. A total of 1726 muscles in extremities were chosen for monitoring, and acceptable baseline Br(E)-MsEP responses were obtained from 1640 (95%). Onset latency was defined as the period from stimulation until the waveform was detected. Relationships of postoperative motor deficit with onset latency alone and in combination with a decrease in amplitude of ≥ 70% from baseline were examined.

RESULTS

Nine of the 83 patients had postoperative motor deficits. The delay of onset latency compared to the control waveform differed significantly between patients with and without these deficits (1.09% ± 0.06% vs 1.31% ± 0.14%, p < 0.01). In ROC analysis, an intraoperative 15% delay in latency from baseline had a sensitivity of 78% and a specificity of 96% for prediction of postoperative motor deficit. In further ROC analysis, a combination of a decrease in amplitude of ≥ 70% and delay of onset latency of ≥ 10% from baseline had sensitivity of 100%, specificity of 93%, a false positive rate of 7%, a false negative rate of 0%, a positive predictive value of 64%, and a negative predictive value of 100% for this prediction.

CONCLUSIONS

In spinal cord monitoring with intraoperative Br(E)-MsEP, an alarm point using a decrease in amplitude of ≥ 70% and delay in onset latency of ≥ 10% from baseline has high specificity that reduces false positive results.

ABBREVIATIONS

AIS = adolescent idiopathic scoliosis; Br(E)-MsEP = brain evoked muscle-action potential; EMG = electromyography; FNR = false negative rate; FPR = false positive rate; MIOM = multimodal intraoperative monitoring; MMT = manual muscle test; NPV = negative predictive value; OLF = ossification of the ligament flavum; OPLL = ossification of the posterior longitudinal ligament; PPV = positive predictive value; SBP = systolic blood pressure; SCEP = spinal cord evoked potential; SSEP = somatosensory evoked potential.

OBJECTIVE

Monitoring of brain evoked muscle-action potentials (Br[E]-MsEPs) is a sensitive method that provides accurate periodic assessment of neurological status. However, occasionally this method gives a relatively high rate of false-positives, and thus hinders surgery. The alarm point is often defined based on a particular decrease in amplitude of a Br(E)-MsEP waveform, but waveform latency has not been widely examined. The purpose of this study was to evaluate onset latency in Br(E)-MsEP monitoring in spinal surgery and to examine the efficacy of an alarm point using a combination of amplitude and latency.

METHODS

A single-center, retrospective study was performed in 83 patients who underwent spine surgery using intraoperative Br(E)-MsEP monitoring. A total of 1726 muscles in extremities were chosen for monitoring, and acceptable baseline Br(E)-MsEP responses were obtained from 1640 (95%). Onset latency was defined as the period from stimulation until the waveform was detected. Relationships of postoperative motor deficit with onset latency alone and in combination with a decrease in amplitude of ≥ 70% from baseline were examined.

RESULTS

Nine of the 83 patients had postoperative motor deficits. The delay of onset latency compared to the control waveform differed significantly between patients with and without these deficits (1.09% ± 0.06% vs 1.31% ± 0.14%, p < 0.01). In ROC analysis, an intraoperative 15% delay in latency from baseline had a sensitivity of 78% and a specificity of 96% for prediction of postoperative motor deficit. In further ROC analysis, a combination of a decrease in amplitude of ≥ 70% and delay of onset latency of ≥ 10% from baseline had sensitivity of 100%, specificity of 93%, a false positive rate of 7%, a false negative rate of 0%, a positive predictive value of 64%, and a negative predictive value of 100% for this prediction.

CONCLUSIONS

In spinal cord monitoring with intraoperative Br(E)-MsEP, an alarm point using a decrease in amplitude of ≥ 70% and delay in onset latency of ≥ 10% from baseline has high specificity that reduces false positive results.

ABBREVIATIONS

AIS = adolescent idiopathic scoliosis; Br(E)-MsEP = brain evoked muscle-action potential; EMG = electromyography; FNR = false negative rate; FPR = false positive rate; MIOM = multimodal intraoperative monitoring; MMT = manual muscle test; NPV = negative predictive value; OLF = ossification of the ligament flavum; OPLL = ossification of the posterior longitudinal ligament; PPV = positive predictive value; SBP = systolic blood pressure; SCEP = spinal cord evoked potential; SSEP = somatosensory evoked potential.

Intramedullary tumor resection, ossification of the posterior longitudinal ligament (OPLL) decompression procedures, and scoliosis surgery are often performed in critical situations,1,4,10 and the importance of intraoperative spinal cord monitoring in these spinal surgeries is widely acknowledged.16,20,25,28,32 Somatosensory evoked potentials (SSEPs) have been used to monitor spinal surgery since the 1980s,3,18,26 and spinal cord evoked potentials (SCEPs) after brain stimulation (Br-SCEP, D-wave) have been used for motor pathway monitoring since the 1990s.15,30,31 Other monitoring techniques include free-running electromyography,7,9 monitoring of SCEPs after stimulation of the spinal cord (Sp-SCEPs) or peripheral nerve (Pn-SCEPs), and monitoring of brain evoked muscle-action potentials (Br[E]-MsEPs).2,16,17,19 Br(E)-MsEP monitoring is regarded as the most sensitive method17,30 for accurate periodical assessment of neurological status, but a few reports have shown that Br(E)-MsEP monitoring can produce a relative high rate of false-positives, which can hinder surgery.20,25

Br(E)-MsEP monitoring is mainly used for intraoperative spinal cord monitoring, and previously the alarm point has been defined as a particular decrease in waveform amplitude. However, the utility of waveform latency has not been widely examined. Thus, we examined the characteristics of latency in Br(E)-MsEP monitoring. The purpose of this study is to evaluate onset latency and examine its efficacy for prediction of postoperative motor deficit using a delay in onset latency in combination with an amplitude decrease in Br(E)-MsEPs. The final goal is to define a new alarm point based on a combination of latency and amplitude.

Methods

Patient Selection and Neurological Evaluation

A total of 91 consecutive cervical and thoracic spine surgeries performed under intraoperative neurophysiological monitoring with Br(E)-MsEPs at our hospital were reviewed retrospectively. Eight cases from which no monitorable baseline Br(E)-MsEP from any lower extremity muscle was obtained were excluded from the study. Preoperative motor status itself was not included in the exclusion criteria. Finally, 83 cases with 1726 monitored muscles in the extremities were selected for the study based on acceptable baseline Br(E)-MsEP responses. The patients had a mean age of 45 years (range 10–74 years); 49 were female and 34 were male. The diseases were intradural extramedullary tumor (n = 21), OPLL or ossification of the ligament flavum (OLF) (n = 19), adolescent idiopathic scoliosis (AIS) (n = 18), spinal intramedullary tumor (n = 12), congenital scoliosis (n = 7), and others (n = 6); and 21 patients had preoperative motor deficits. The McCormick grade at admission was I (normal gait) in 62 cases, II (mild gait disturbance not requiring support) in 10 cases, III (able to walk with support) in 5 cases, IV (assistance required for ambulation) in 5 cases, and V (wheelchair needed) in 1 case.22

The onset latency was defined as the period from stimulation to detection of the waveform (Fig. 1), and the % latency delay was calculated from the onset latency at baseline: [(latency − latency at baseline)/latency at baseline] × 100. A decrease in postoperative manual muscle test (MMT) score of ≥ 1 compared with preoperative MMT was defined as a postoperative motor deficit, and relationships with onset latency and with a combination of onset latency and a decrease in amplitude of ≥ 70% from baseline11,17 were examined. This study was approved by the institutional review board of Nagoya University Graduate School of Medicine, and each patient gave informed consent before enrollment.

Fig. 1.
Fig. 1.

Onset latency was defined as the period from stimulation until the waveform was detected. mS = milliseconds.

Anesthetic Management and General Conditions During Surgery

A minimal benzodiazepine dose was used as pre-anesthetic medication to avoid possible suppression of waveform latency and amplitude. Propofol (3–4 mg/kg), vecuronium (0.12–0.16 mg/kg), and fentanyl (2 mg/kg) were administered for induction, and anesthesia was maintained with propofol (50–100 μg/kg/min), fentanyl (1–2.5 μg/kg/hr), and vecuronium (0.01–0.04 mg/kg/hr). Anesthesia was given as appropriate with continuous prostaglandin E1 (PGE1) and a short-acting β1 blocker (landiolol). Patients were maintained in a normothermic state, and the temperature was raised in the event of possible intraoperative spinal damage. Systolic blood pressure (SBP) variations were measured during surgery, and SBPs were determined at the time of waveform deterioration.11

Stimulation and Recording Methods

An MS120B system (Nihon Kohden) was used to perform transcranial stimulation, with parameters of 5 stimulations in a row at 2-msec intervals, a constant biphasic current of 200 mA for 500 μsec, a 50–1000-Hz filter, and a 100-msec epoch time with ≤ 20 recorded signal responses. The stimulated point was 2 cm anterior and 6 cm lateral from the Cz location over the cerebral cortex motor area. Using the Neuromaster MEE-1232 version 05.10 (Nihon Kohden), which is expandable to 32 channels, muscle action potentials were recorded from the upper and lower extremities via a pair of needle electrodes 3 to 5 Br(E)-MsEPs apart.11 The target muscles in cervical spine surgery (bilateral trapezius, triceps, deltoid, biceps, brachioradialis, abductor digit minimi, extensor carpi ulnaris, adductor longus, quadriceps femoris, hamstrings, tibialis anterior, gastrocnemius, abductor hallucis, and anal sphincter muscles) were routinely monitored using 28 channels. The target muscles in thoracic spine surgery (bilateral deltoid, extensor carpi ulnaris, adductor longus, quadriceps femoris, hamstrings, tibialis anterior, gastrocnemius, abductor hallucis, and anal sphincter muscles) were routinely monitored using 18 channels.13,14 Br(E)-MsEP data from these muscles were used for analysis. Multimodal monitoring was used in all cases, with a particular combination of D-wave and SSEP. Free-running electromyography (EMG) from all muscles was monitored throughout the operation.12,13

Monitoring and Alert Parameters

The Br(E)-MsEP baseline was determined immediately after documented surgical exposure of the spine. Waiting until this point for baseline measurements reduced the effects on Br(E)-MsEP responses because of body and spinal cord temperature changes occurring with exposure. Signals were rechecked after surgical exposure, screw insertion, decompression, and wound closure. Surgeons were informed of an acute change in the Br(E)-MsEP response.13,14 If a waveform changed during surgery, SBP was raised or hypotensive anesthesia was reversed, the patient was warmed, and irrigation was performed with warm saline. If the waveform did not recover, surgery at the then-current site was suspended. Surgery at a different site continued until the waveform recovered. If there was no improvement, surgery was terminated.12

Results

Of 1726 muscles used for monitoring in the extremities of 83 patients, acceptable baseline Br(E)-MsEP responses were obtained from 1640 (95%). Of the 83 patients, 9 (11%) had postoperative motor deficits, of which 0, 0, 3, 4, and 2 were classified at discharge into McCormick grades I, II, II, IV, and V, respectively. The details of responses to monitoring and changes in amplitude and latency in these 9 cases are shown in Table 1.

TABLE 1.

Details of cases with postoperative neurological deficits (n = 9)

Age (yrs), SexDiseaseTiming of Waveform DeteriorationDeterioration in Latency & AmpProcedures in Response to Monitoring ChangeMcCormick Grade
PreopPostop  
13, FScoliosisAfter rotation maneuverLatency delayed by 23%; amp deter below 70%Maneuver interruption & release of correctionIIII
47, MT-OPLLDuring decomprLatency delayed by 13%; amp deter below 70%Dekyphotic corr fusion w/ instrIIV
33, MT-OPLLDuring decomprLatency delayed by 55%; amp deter below 80%Dekyphotic corr fusion w/ instrIIIIV
52, FT-OPLLDuring decomprLatency delayed by 20%; amp deter below 80%Dekyphotic corr fusion w/ instrIIIII
49, FT-OPLLAfter screw insertionLatency delayed by 11%; amp deter below 70%Alignment maintained using rod & decompr quicklyIIIV
37, MT-OPLLAfter screw insertionLatency delayed by 41%; amp deter below 70%Alignment maintained using rod & decompr quicklyIIIII
42, MIM tumorDuring tumor excisionLatency delayed by 31%; amp deter below 70%Temp susp of proc & IV steroid adminIIIV
54, FIM tumorDuring tumor excisionLatency delayed by 42%; amp deter below 90%Temp susp of proc & IV steroid adminIIIV
48, FIM tumorDuring tumor excisionLatency delayed by 49%; amp deter below 80%Temp susp of proc & IV steroid adminIIIV

Admin = administration; amp = amplitude; corr = corrective; decompr = decompression; deter = deteriorated; IM = intramedullary; instr = instrumentation; IV = intravenous; proc = procedure; susp = suspension; temp = temporary; T-OPLL = thoracic OPLL.

The onset latency compared to the control waveform differed significantly in cases with and without a postoperative motor deficit (1.09% ± 0.06% vs 1.31% ± 0.14%, p < 0.01) (Fig. 2). In receiver operating characteristic (ROC) analysis, an intraoperative Br(E)-MsEP latency delay of 15% from baseline had a sensitivity of 78% and a specificity of 96% for prediction of postoperative motor deficit (Fig. 3).

Fig. 2.
Fig. 2.

Change in onset latency compared to the control waveform (% delay of the baseline latency) in cases with and without postoperative motor deficit. The mean values for the 2 groups were significantly different (p < 0.01).

Fig. 3.
Fig. 3.

ROC curve for determination of the cutoff for prediction of postoperative motor deficit using the onset latency of the intraoperative Br(E)-MsEP waveform (expressed as % delay of the baseline latency). AUC = area under the ROC curve.

A decrease in intraoperative amplitude of ≥ 70% from baseline occurred in 30 cases, with a sensitivity of 100%, a specificity of 72%, a false positive rate (FPR) of 28%, a false negative rate (FNR) of 0%, a positive predictive value (PPV) of 30%, and a negative predictive value (NPV) of 100% for prediction of postoperative motor deficit (Table 2). An onset latency delay of ≥ 15% cutoff gave a sensitivity of 78%, a specificity of 96%, FPR of 4%, FNR of 22%, PPV of 70%, and NPV of 97%, and an onset latency delay of ≥ 10% cutoff gave a sensitivity of 100%, a specificity of 84%, FPR of 16%, FNR of 0%, PPV of 43%, and NPV of 100% for prediction of postoperative motor deficit. Combination of a decrease in amplitude of ≥ 70% and an onset latency of ≥ 15% from baseline had a sensitivity of 78%, a specificity of 97%, FPR of 3%, FNR of 22%, PPV of 78%, and NPV of 97%, and a combination of a decrease in amplitude of ≥ 70% and an onset latency of ≥ 10% from baseline had a sensitivity of 100%, a specificity of 93%, FPR of 7%, FNR of 0%, PPV of 64%, and NPV of 100% for prediction of postoperative motor deficit. These results showed that a cutoff of an onset latency delay of ≥ 15% cutoff had decreased sensitivity due to inclusion of 2 false-negative cases. Therefore, we defined a combination of a decrease in amplitude of ≥ 70% and an onset latency delay of ≥ 10% from baseline as the new alarm point (Table 2).

TABLE 2.

Relationship of postoperative motor deficit with waveform deterioration

Waveform DeteriorationAll PtsPostop Motor DeficitSensitivitySpecificityFPRFNRPPVNPV
PresentAbsent  
Decrease in amp of ≥70% from baseline100%72%28%0%30%100%
 Present30921
 Absent53053
 Total83974
Delay in onset latency of ≥15% from baseline78%96%4%22%70%97%
 Present1073
 Absent73271
 Total83974
Delay in onset latency of ≥10% from baseline100%84%16%0%43%100%
 Present21912
 Absent62062
 Total83974
Decrease in amp of ≥70% & delay in onset latency of ≥15% from baseline78%97%3%22%78%97%
 Present972
 Absent74272
 Total83974
Decrease in amp of ≥70% & delay in onset latency of ≥10% from baseline100%93%7%0%64%100%
 Present1495
 Absent69069
 Total83974

FNR = false negative rate; FPR = false positive rate; NPV = negative predictive value; PPV = positive predictive value; pts = patients.

For prediction of postoperative motor deficit, this new alarm point had a sensitivity of 100%, a specificity of 91%, PPV of 50%, and NPV of 100% in scoliosis cases (n = 25); a sensitivity of 100%, a specificity of 67%, PPV of 50%, and NPV of 100% in OPLL cases (n = 16); and a sensitivity of 100%, a specificity of 38%, PPV of 44%, and NPV of 100% in intramedullary tumor cases (n = 12) (Table 3). In subgroup analysis in 62 patients who had no preoperative motor deficits (McCormick grade I), the new alarm point of a combination of a decrease in amplitude of ≥ 70% and an onset latency of ≥ 10% from baseline had a sensitivity of 100%, a specificity of 90%, FPR of 10%, FNR of 0%, PPV of 33%, and NPV of 100% for prediction of postoperative motor deficit (Table 4). There were 5 cases in which the waveform became flat during surgery, including 3 cases of thoracic spinal OPLL and 2 cases of intramedullary tumor. In these cases, “onset” was difficult to determine and we were only able to evaluate amplitude alone.

TABLE 3.

Sensitivity, specificity, PPV, and NPV in scoliosis, OPLL, and intramedullary tumor cases based on a decrease in amplitude of ≥ 70% and delay in onset latency of ≥ 10% from baseline

DiseaseSensitivitySpecificityPPVNPV
Scoliosis (n = 25)100% (2/2)91% (21/23)50% (2/4)100% (21/21)
OPLL (n = 16)100% (4/4)67% (8/12)50% (4/8)100% (8/8)
Intramedullary tumor (n = 12)100% (4/4)38% (3/8)44% (4/9)100% (3/3)
TABLE 4.

Relationship of postoperative motor deficit with waveform amplitude deterioration and delay in onset latency in 62 patients with no motor deficits at baseline

Decrease in Amp of ≥70% & Delay in Onset Latency of ≥10% From BaselinePostop Motor Deficit
PresentAbsentTotal 
Present369
Absent05353
Total35962

Sensitivity = 100%, specificity = 90%, false positive rate = 10%, false negative rate = 0%, positive predictive value = 33%, negative predictive value = 100%.

Illustrative Case

This 13-year-old female patient had a preoperative main Cobb angle of 84° due to AIS (Fig. 4A). The results of preoperative motor and sensory examinations were normal. The patient underwent posterior spinal fusion with instrumentation from T4 to L4 with posterior osteotomy around the apex of the deformity (T11, T12, L1) due to the rigidity of the curve and fused segments (Fig. 4B). She had acceptable baseline Br(E)-MsEP values bilaterally (Fig. 4C, open arrow). After a rotation maneuver, the waveform amplitude deteriorate beyond the 70% criterion for the adductor longus bilaterally and for the left quadriceps, hamstrings, and gastrocnemius; and onset latency of the gastrocnemius was delayed by 23% (26 → 32 msec) (Fig. 4C). The maneuver was interrupted and the correction was released. The waveform eventually improved to > 50% of baseline for the left quadriceps, but there was no improvement in the waveforms for the other muscles improved (Fig. 4C). Immediately after surgery, the MMT score in the left quadriceps femoris and hamstrings dropped from the preoperative score of 5/5 to 4/5. The patient’s neurological function had normalized at the 1-month postoperative evaluation. The postoperative Cobb angle was 11°, with a curve correction rate of 87%.

Fig. 4.
Fig. 4.

A: Preoperative posteroanterior radiographs obtained in a 13-year-old female patient with AIS. The curve magnitudes were 84° thoracic, 45° upper thoracic, and 60° lumbar. B: The patient underwent posterior spinal fusion with instrumentation from T4 to L4 with posterior osteotomy around the apex of the deformity (T11, T12, L1) due to the stiffness of the curve and fused segments. The postoperative Cobb angle was 11°, with a curve correction rate of 87%. C: In Br(E)-MsEP monitoring, after a rotation maneuver, the waveform amplitude deteriorated below the 70% criterion for the adductor longus bilaterally and for the left quadriceps, hamstrings, and gastrocnemius, and the onset latency of the gastrocnemius was delayed by 23% (26 → 32 msec) (arrowhead). The maneuver was interrupted and the correction was released. The waveform eventually improved to > 50% of baseline for the left quadriceps, while others were not improved (open arrowhead). AH = abductor hallucis; AL = adductor longus; Gc = gastrocnemius; Ham = hamstrings; TA = tibialis anterior.

Discussion

The alarm point in intraoperative Br(E)-MsEP monitoring has been defined as waveform amplitude disappearance and a ≥ 50% D-wave amplitude decrement,31 a decrease in amplitude of ≥ 50% from baseline,27,32,33 a decrease in amplitude of ≥ 70% from baseline,8,12–14 a decrease in amplitude of ≥ 80% from baseline,16 and multiphase of the waveform.27 In our facility, we usually use the 70% amplitude criterion because the monitoring working group of the Japanese Society for Spine Surgery and Related Research recommends this criterion in Japan.8,14 However, a clear alarm point for Br(E)-MsEP monitoring has yet to be established. Use of an alarm point based only on Br(E)-MsEP amplitude has a concern that the high number of false positives can hamper smooth surgery.8,12–14,23,24 Multimodal intraoperative monitoring (MIOM) has been used to attenuate false positives. Sutter and colleagues examined MIOM in 1017 cases, and found a sensitivity of 89% and a specificity of 99%,32 and Ito et al. reported that the multimodal approach has a sensitivity of 90% and a FPR of 6.1%.8 However, 63% of institutions currently use Br(E)-MsEP monitoring, and only 27.8% use Br(E)-SCEP monitoring; and 33% of facilities use only a single modality.21 Thus, it is likely that the number of institutions performing simultaneous MIOM with Br(E)-MsEP and Br(E)-SCEP is relatively low. Therefore, in this situation, it is still important to define a simple alarm point setting.

There are 2 types of criteria for latency: onset and peak. In our series, latency was defined using onset of Br(E)-MsEP because it is difficult to evaluate the peak at which a waveform change occurs. In contrast, the onset time is easier to determine, and accurate evaluation is possible. Therefore, onset time could be valuable since it is easier to evaluate than peak time. However, when a waveform approaches flatness due to deterioration of the amplitude, it is difficult to determine the onset time point. In these cases, there is no choice but to evaluate amplitude alone, and we included 5 such cases. In our series, according to the ROC analysis, ≥ 15% might have been a better latency cutoff; however, we examined the data using a ≥ 10% cutoff (sensitivity 100%, specificity 84%) in addition to the ≥ 15% cutoff (sensitivity 78%, specificity 97%). This was because 2 cases with postoperative motor deficit were both false negatives. In surgery, detection of postoperative motor deficit is most important, and therefore, sensitivity is more important and higher sensitivity is required. Therefore, to avoid false-negative cases, we defined the new alarm point using a delay in onset latency of ≥ 10% from baseline. We note that the 2 false-negatives cases at an onset latency delay of ≥ 15% cutoff were due to the absolute amplitude being reduced to ≤ 2 μV. It might not be appropriate to evaluate the alarm point using latency only and might be better to evaluate amplitude and use latency as an auxiliary indicator. Thus, the combination of the high sensitivity of amplitude and high specificity of latency may give an ideal alarm point. Based on this consideration, we finally defined the new alarm point as a combination of a decrease in amplitude of ≥ 70% and a delay in onset latency of ≥ 10% from baseline, and this alarm point had 100% sensitivity, 93% specificity, FPR 7%, and FNR 0%, which is suitable for an alarm point using a single modality.

Br(E)-MsEP monitoring has been performed for various diseases, and detection of root level palsies or brachial plexus compression from positioning has also been reported. Chen et al.5 found that multimodality monitoring with spontaneous and electrically triggered EMG combined with SSEP and MEP may be the best approach. Raynor et al.29 and Duncan et al.6 also reported that, together with SSEP and MEP, EMG is a necessary part of a multimodality protocol for monitoring lumbar spinal nerve roots. In an experimental study, Yang et al.33 evaluated the brachial plexus and vessel compression in a combined central and peripheral electrodiagnostic approach. However, the alarm point for detection of root level palsies or brachial plexus compression from positioning has not been determined. Therefore, further studies are needed to determine whether the same parameters can be used for multiple diseases. Based on our findings, it will be necessary to study whether the same parameters apply equally to detection of root level palsies or brachial plexus compression from positioning and to examine new alarm points using amplitude and latency.

In intraoperative spinal cord monitoring, it is important to increase the sensitivity in detection of waveform deterioration. In our series, muscles were monitored routinely through 28 channels in cervical surgery and 18 in thoracic surgery. This is advantageous because the increased number of detection channels allows easy detection of waveform deterioration, which increases the sensitivity. In addition, the combination of amplitude and latency used in this study will make it possible to evaluate intraoperative changes to the spinal cord acutely.

This study has several limitations, including its retrospective design, the small number of cases reducing the power of the statistical analysis, and the variety of surgical procedures. A prospective study would have shown whether cases with new paralysis could have been prevented using the proposed alarm point, and such a should be performed. Within these limitations, we were able to evaluate numerous waveforms from 1726 muscles in 83 cases in detail at a single institution. This is the first study to examine a combination of waveform amplitude and latency as an alarm point and the first to show the efficacy of latency for this purpose. The combination of a decrease in amplitude of ≥ 70% and a delay in onset latency of ≥ 10% from baseline gives an alarm point with high specificity that could lead to reduction of false-positive results.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: all authors. Acquisition of data: all authors. Analysis and interpretation of data: Kobayashi, Ando. Drafting the article: Kobayashi. Critically revising the article: Kobayashi. Reviewed submitted version of manuscript: Kobayashi. Statistical analysis: Kobayashi. Administrative/technical/material support: Kobayashi. Study supervision: Imagama.

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    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Langeloo DD, Lelivelt A, Louis Journée H, Slappendel R, de Kleuver M: Transcranial electrical motor-evoked potential monitoring during surgery for spinal deformity: a study of 145 patients. Spine (Phila Pa 1976) 28:10431050, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Lesser RP, Raudzens P, Lüders H, Nuwer MR, Goldie WD, Morris HH III, et al.: Postoperative neurological deficits may occur despite unchanged intraoperative somatosensory evoked potentials. Ann Neurol 19:2225, 1986

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Luk KD, Hu Y, Wong YW, Cheung KM: Evaluation of various evoked potential techniques for spinal cord monitoring during scoliosis surgery. Spine (Phila Pa 1976) 26:17721777, 2001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Macdonald DB: Intraoperative motor evoked potential monitoring: overview and update. J Clin Monit Comput 20:347377, 2006

  • 21

    Matsuyama Y, Shinomiya K, Ando M, Kazuhiko S, Toshikazu T, Ishiguro N: [Intraoperative spinal cord monitoring—multi center study of Japanese Society for Spine Surgery and Related Research (JSSR).] Rinsho-Nouha 51:286291, 2009 (Jpn)

    • Search Google Scholar
    • Export Citation
  • 22

    McCormick PC, Michelsen WJ, Post KD, Carmel PW, Stein BM: Cavernous malformations of the spinal cord. Neurosurgery 23:459463, 1988

  • 23

    Muramoto A, Imagama S, Ito Z, Ando K, Tauchi R, Matsumoto T, et al.: The cutoff amplitude of transcranial motor evoked potentials for transient postoperative motor deficits in intramedullary spinal cord tumor surgery. Spine (Phila Pa 1976) 39:E1086E1094, 2014

    • Search Google Scholar
    • Export Citation
  • 24

    Muramoto A, Imagama S, Ito Z, Wakao N, Ando K, Tauchi R, et al.: The cutoff amplitude of transcranial motor-evoked potentials for predicting postoperative motor deficits in thoracic spine surgery. Spine (Phila Pa 1976) 38:E21E27, 2013

    • Search Google Scholar
    • Export Citation
  • 25

    Paradiso G, Lee GY, Sarjeant R, Hoang L, Massicotte EM, Fehlings MG: Multimodality intraoperative neurophysiologic monitoring findings during surgery for adult tethered cord syndrome: analysis of a series of 44 patients with long-term follow-up. Spine (Phila Pa 1976) 31:20952102, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Park P, Wang AC, Sangala JR, Kim SM, Hervey-Jumper S, Than KD, et al.: Impact of multimodal intraoperative monitoring during correction of symptomatic cervical or cervicothoracic kyphosis. J Neurosurg Spine 14:99105, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Pelosi L, Lamb J, Grevitt M, Mehdian SM, Webb JK, Blumhardt LD: Combined monitoring of motor and somatosensory evoked potentials in orthopaedic spinal surgery. Clin Neurophysiol 113:10821091, 2002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Quiñones-Hinojosa A, Lyon R, Zada G, Lamborn KR, Gupta N, Parsa AT, et al.: Changes in transcranial motor evoked potentials during intramedullary spinal cord tumor resection correlate with postoperative motor function. Neurosurgery 56:982993, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Raynor BL, Lenke LG, Bridwell KH, Taylor BA, Padberg AM: Correlation between low triggered electromyographic thresholds and lumbar pedicle screw malposition: analysis of 4857 screws. Spine (Phila Pa 1976) 32:26732678, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sala F, Bricolo A, Faccioli F, Lanteri P, Gerosa M: Surgery for intramedullary spinal cord tumors: the role of intraoperative (neurophysiological) monitoring. Eur Spine J 16 (Suppl 2):S130S139, 2007

    • Search Google Scholar
    • Export Citation
  • 31

    Sala F, Palandri G, Basso E, Lanteri P, Deletis V, Faccioli F, et al.: Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery 58:11291143, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Sutter M, Eggspuehler A, Grob D, Jeszenszky D, Benini A, Porchet F, et al.: The diagnostic value of multimodal intraoperative monitoring (MIOM) during spine surgery: a prospective study of 1,017 patients. Eur Spine J 16 (Suppl 2):S162S170, 2007

    • Search Google Scholar
    • Export Citation
  • 33

    Yang C, Xu J, Chen J, Li S, Cao Y, Zhu Y, et al.: Experimental study of brachial plexus and vessel compression: evaluation of combined central and peripheral electrodiagnostic approach. Oncotarget 8:5061850628, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
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    Onset latency was defined as the period from stimulation until the waveform was detected. mS = milliseconds.

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    Change in onset latency compared to the control waveform (% delay of the baseline latency) in cases with and without postoperative motor deficit. The mean values for the 2 groups were significantly different (p < 0.01).

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    ROC curve for determination of the cutoff for prediction of postoperative motor deficit using the onset latency of the intraoperative Br(E)-MsEP waveform (expressed as % delay of the baseline latency). AUC = area under the ROC curve.

  • View in gallery

    A: Preoperative posteroanterior radiographs obtained in a 13-year-old female patient with AIS. The curve magnitudes were 84° thoracic, 45° upper thoracic, and 60° lumbar. B: The patient underwent posterior spinal fusion with instrumentation from T4 to L4 with posterior osteotomy around the apex of the deformity (T11, T12, L1) due to the stiffness of the curve and fused segments. The postoperative Cobb angle was 11°, with a curve correction rate of 87%. C: In Br(E)-MsEP monitoring, after a rotation maneuver, the waveform amplitude deteriorated below the 70% criterion for the adductor longus bilaterally and for the left quadriceps, hamstrings, and gastrocnemius, and the onset latency of the gastrocnemius was delayed by 23% (26 → 32 msec) (arrowhead). The maneuver was interrupted and the correction was released. The waveform eventually improved to > 50% of baseline for the left quadriceps, while others were not improved (open arrowhead). AH = abductor hallucis; AL = adductor longus; Gc = gastrocnemius; Ham = hamstrings; TA = tibialis anterior.

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    Ito Z, Imagama S, Sakai Y, Katayama Y, Wakao N, Ando K, et al.: A new criterion for the alarm point for compound muscle action potentials. J Neurosurg Spine 17:348356, 2012

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    Kobayashi K, Ando K, Yagi H, Ito K, Tsushima M, Morozumi M, et al.: Prevention and prediction of postoperative bowel bladder disorder using an anal plug electrode with Tc-MsEP monitoring during spine surgery. Nagoya J Med Sci 79:459466, 2017

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    Kobayashi K, Imagama S, Ito Z, Ando K, Hida T, Ishiguro N: Prevention of spinal cord injury using brain-evoked muscle-action potential (Br(E)-MsEP) monitoring in cervical spinal screw fixation. Eur Spine J 26:11541161, 2017

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    Kobayashi K, Imagama S, Ito Z, Ando K, Hida T, Ito K, et al.: Transcranial motor evoked potential waveform changes in corrective fusion for adolescent idiopathic scoliosis. J Neurosurg Pediatr 19:108115, 2017

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    Kobayashi S, Matsuyama Y, Shinomiya K, Kawabata S, Ando M, Kanchiku T, et al.: A new alarm point of transcranial electrical stimulation motor evoked potentials for intraoperative spinal cord monitoring: a prospective multicenter study from the Spinal Cord Monitoring Working Group of the Japanese Society for Spine Surgery and Related Research. J Neurosurg Spine 20:102107, 2014

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  • 16

    Langeloo DD, Journée HL, de Kleuver M, Grotenhuis JA: Criteria for transcranial electrical motor evoked potential monitoring during spinal deformity surgery: a review and discussion of the literature. Neurophysiol Clin 37:431439, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Langeloo DD, Lelivelt A, Louis Journée H, Slappendel R, de Kleuver M: Transcranial electrical motor-evoked potential monitoring during surgery for spinal deformity: a study of 145 patients. Spine (Phila Pa 1976) 28:10431050, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Lesser RP, Raudzens P, Lüders H, Nuwer MR, Goldie WD, Morris HH III, et al.: Postoperative neurological deficits may occur despite unchanged intraoperative somatosensory evoked potentials. Ann Neurol 19:2225, 1986

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Luk KD, Hu Y, Wong YW, Cheung KM: Evaluation of various evoked potential techniques for spinal cord monitoring during scoliosis surgery. Spine (Phila Pa 1976) 26:17721777, 2001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Macdonald DB: Intraoperative motor evoked potential monitoring: overview and update. J Clin Monit Comput 20:347377, 2006

  • 21

    Matsuyama Y, Shinomiya K, Ando M, Kazuhiko S, Toshikazu T, Ishiguro N: [Intraoperative spinal cord monitoring—multi center study of Japanese Society for Spine Surgery and Related Research (JSSR).] Rinsho-Nouha 51:286291, 2009 (Jpn)

    • Search Google Scholar
    • Export Citation
  • 22

    McCormick PC, Michelsen WJ, Post KD, Carmel PW, Stein BM: Cavernous malformations of the spinal cord. Neurosurgery 23:459463, 1988

  • 23

    Muramoto A, Imagama S, Ito Z, Ando K, Tauchi R, Matsumoto T, et al.: The cutoff amplitude of transcranial motor evoked potentials for transient postoperative motor deficits in intramedullary spinal cord tumor surgery. Spine (Phila Pa 1976) 39:E1086E1094, 2014

    • Search Google Scholar
    • Export Citation
  • 24

    Muramoto A, Imagama S, Ito Z, Wakao N, Ando K, Tauchi R, et al.: The cutoff amplitude of transcranial motor-evoked potentials for predicting postoperative motor deficits in thoracic spine surgery. Spine (Phila Pa 1976) 38:E21E27, 2013

    • Search Google Scholar
    • Export Citation
  • 25

    Paradiso G, Lee GY, Sarjeant R, Hoang L, Massicotte EM, Fehlings MG: Multimodality intraoperative neurophysiologic monitoring findings during surgery for adult tethered cord syndrome: analysis of a series of 44 patients with long-term follow-up. Spine (Phila Pa 1976) 31:20952102, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Park P, Wang AC, Sangala JR, Kim SM, Hervey-Jumper S, Than KD, et al.: Impact of multimodal intraoperative monitoring during correction of symptomatic cervical or cervicothoracic kyphosis. J Neurosurg Spine 14:99105, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Pelosi L, Lamb J, Grevitt M, Mehdian SM, Webb JK, Blumhardt LD: Combined monitoring of motor and somatosensory evoked potentials in orthopaedic spinal surgery. Clin Neurophysiol 113:10821091, 2002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Quiñones-Hinojosa A, Lyon R, Zada G, Lamborn KR, Gupta N, Parsa AT, et al.: Changes in transcranial motor evoked potentials during intramedullary spinal cord tumor resection correlate with postoperative motor function. Neurosurgery 56:982993, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Raynor BL, Lenke LG, Bridwell KH, Taylor BA, Padberg AM: Correlation between low triggered electromyographic thresholds and lumbar pedicle screw malposition: analysis of 4857 screws. Spine (Phila Pa 1976) 32:26732678, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sala F, Bricolo A, Faccioli F, Lanteri P, Gerosa M: Surgery for intramedullary spinal cord tumors: the role of intraoperative (neurophysiological) monitoring. Eur Spine J 16 (Suppl 2):S130S139, 2007

    • Search Google Scholar
    • Export Citation
  • 31

    Sala F, Palandri G, Basso E, Lanteri P, Deletis V, Faccioli F, et al.: Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery 58:11291143, 2006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Sutter M, Eggspuehler A, Grob D, Jeszenszky D, Benini A, Porchet F, et al.: The diagnostic value of multimodal intraoperative monitoring (MIOM) during spine surgery: a prospective study of 1,017 patients. Eur Spine J 16 (Suppl 2):S162S170, 2007

    • Search Google Scholar
    • Export Citation
  • 33

    Yang C, Xu J, Chen J, Li S, Cao Y, Zhu Y, et al.: Experimental study of brachial plexus and vessel compression: evaluation of combined central and peripheral electrodiagnostic approach. Oncotarget 8:5061850628, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation

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