Awake Volunteer Pain Scores During Neuromuscular Monitoring

Abstract

BACKGROUND: 

There is a need for easy to use, reliable neuromuscular monitors (NMMs). This multicenter, prospective, unblinded study compared the discomfort associated with neurostimulation in unmedicated healthy volunteers when using the new electromyography (EMG)-based TetraGraph and acceleromyography (AMG)-based TOF-Watch NMMs. The secondary aim was to compare the repeatability of the train-of-four (TOF) ratios (TOFRs) obtained with the 2 devices.

METHODS: 

The TOF measurements of 135 volunteers from 3 university hospitals were analyzed (age: 38.3 ± 12 years [mean ± standard deviation [SD]]; male/female ratio = 63:72). The left or right ulnar nerve was stimulated at the wrist in TOF mode with 20, 30, 40, and 50 mA stimulating current intensities with both devices in random order. The TOF-Watch used standard electrocardiography (ECG) electrodes (Red Dot; 3M Health Care) for nerve stimulation. The stimulating surface area of 1 ECG electrode is 113 mm². The piezoelectric probe was attached to the thumb, and a hand adapter was used to ensure consistency of AMG measurements. The TetraGraph uses proprietary surface strip electrodes for nerve stimulation and muscle action potential recording, whose stimulating surface area is roughly twice as big as that of standard ECG electrodes (228.5 mm²). The volunteers were asked to rate the discomfort associated with neurostimulation on a 0–10 verbal numerical rating scale (VNRS) score anchored with 0 (no pain) and 10 (worst pain ever experienced). A linear mixed-effects model was used to evaluate the difference in VNRS scores between devices. P <.05 was accepted as the level of significance.

RESULTS: 

In the linear mixed-effects model, there were no differences in VNRS scores between devices at any of the stimulating current intensities, P = .38. The median (range) VNRS scores obtained with TOF-Watch and TetraGraph devices were 2 (0–7) vs 2 (0–8) at 20 mA, 3 (1–9) vs 3 (1–9) at 30 mA, 5 (1–10) vs 5 (1–10) at 40 mA, and 5 (1–10) vs 6 (1–10) at 50 mA stimulating current intensities. The mean of the 1469 TOFRs obtained with TetraGraph was 100.43% ± 7.74% (standard error = 0.2%). Due to technical difficulties, the repeatability of the TOFRs could not be determined.

CONCLUSIONS: 

Despite the different size and design of the stimulating electrodes, the 2 NMMs caused the same level of discomfort in unmedicated healthy volunteers.

KEY POINTS

• Question: Does increasing the size of stimulating electrodes during neuromuscular monitoring decrease pain intensity in awake unmedicated volunteers?
• Findings: Verbal numerical rating scale (VNRS) scores proved identical at 20–50 mA train-of-four (TOF) stimulation when comparing 2 types of neuromuscular monitors (NMMs) having different electrodes.
• Meaning: Increasing the size of stimulating electrodes did not influence volunteers’ discomfort.

Objective neuromuscular monitoring devices help to guide neuromuscular blockade management during surgery and confirm adequate recovery.^1,2 A recent panel of experts strongly recommend the use of neuromuscular monitors (NMMs) as means of decreasing postoperative residual blockade and improving patient safety.¹ Unfortunately, many clinicians are unfamiliar with objective monitoring techniques and cite a mistrust in their reliability.^3,4 There is also a reluctance to use these monitors in awake patients, as neurostimulation can be uncomfortable.^5–7 In addition, the examination of patients recovering from anesthesia can be challenging and might give doubtful results.⁸ Compounding the problem, there is a paucity of user-friendly, reliable NMMs.³

Until its recent withdrawal from market, the acceleromyography (AMG)-based TOF-Watch (Schering-Plough/Merck Inc, Kenilworth, NJ) NMM series has been one of the most widely used NMM in the clinical setting even though AMG has several limitations that kept it from gaining widespread clinical use. These limitations include the need for preload, the fixation of the hand and arm, the lengthy calibration, and need for normalization of obtained train-of-four (TOF) ratios (TOFR).⁹ Most of these limitations can be avoided by the use of electromyography (EMG)-based NMMs.¹ EMG-based devices are easy and fast to set up. Their reliability and ability to obtain useful measurements when the limbs are restricted during surgical positioning have led experts to suggest this modality as a gold standard for quantitative neuromonitoring.¹

The current study investigated the prototype of a new, portable, EMG-based NMM (TetraGraph; Senzime AB, Uppsala, Sweden) and compared it to the AMG-based TOF-Watch NMM. The TetraGraph has recently gained Conformité Européenne (CE) approval but is not approved by the Food and Drug Administration. The TetraGraph utilizes a novel type of surface strip electrodes (TetraSens; Senzime AB). The surface area of each stimulating electrode is roughly twice as large as that of commercially available electrocardiography (ECG) electrodes. They were designed to disperse the potentially painful stimulating current through the skin and subcutaneous tissues. The elongated shape of the stimulating electrodes might increase the likelihood of ulnar nerve depolarization.

The primary aim of the study was to compare the discomfort associated with TOF stimulation by the 2 NMMs, using an 11-point verbal numerical rating scale (VNRS) at 4 different stimulating current intensities in 10 mA increments (20–50 mA). These intensities were chosen as they are the typical intensities advocated for testing of awakening surgical patients. The stimulations were performed in awake, unmedicated volunteers from 3 clinical centers who received no neuromuscular blocking agents. Based on a pilot investigation of 10 volunteers, the authors hypothesized that neurostimulation with the larger stimulating electrodes would be less painful to the volunteers.¹⁰ The secondary aim of the study was to determine the repeatability of the AMG- and EMG-derived TOFRs at individual current intensities.

METHODS

This study was approved by the universities’ institutional review board (IRB) (Mayo Clinic: IRB #16-005022; NorthShore University Health System: IRB #EH16-251; University of Debrecen: DE RKEB/IKEB 494–2018), and written informed consent was obtained from all subjects participating in the trial. The trial was registered before patient enrollment at clinicaltrials.gov (NCT02912039, Principal investigator: J.R.R., Date of registration: September 21, 2016).

The study aimed to enroll 135 volunteers from the 3 centers, 45 volunteers from each. Hospital staff was asked to volunteer in this preclinical investigation. Written informed consent was obtained from all subjects participating in the trial before enrollment. One site enrolled 53 volunteers because of an administrative error. The protocol had prescribed the inclusion of 45 volunteers per center; therefore, measurements from 8 volunteers were ultimately excluded from the final data analysis from this center. There were 2 reasons for excluding these data: 4 volunteers had incomplete datasets because they withdrew from testing at higher (40–50 mA) current intensities; and 4 volunteers participated twice and had duplicate measurements (the second element of the duplicates was excluded). Each volunteer received nerve stimulations with 4 different current amplitudes (20, 30, 40, and 50 mA) in random order with each of the 2 monitors.

Setup of TOF-Watch NMM

Figure 1.: Conventional electrocardiography electrodes (Red Dot; 3M Health Care, St Paul, MN) used for nerve stimulation (red circles indicate the edge of conductive area) and the TetraSens electrodes used by TetraGraph. The stimulating electrodes are positioned under the electrocardiography electrodes.

Figure 2.: Application of the 2 neuromuscular monitors. A, TOF-Watch S neuromuscular monitor with hand adaptor. B, TetraGraph neuromuscular monitor with the TetraSens electrode placed over the course of the ulnar nerve and the adductor pollicis muscle. TOF indicates train of four.

Single-use ECG electrodes (Red Dot; 3M Health Care, St Paul, MN; Figure 1) were placed along the ulnar nerve at the wrist 3 cm apart from each other, with the distal electrode 1 cm proximal to the wrist crease. The stimulating surface area of 1 electrode is 113 mm². The piezoelectric probe of the device was attached to the thumb. A hand adapter (Organon BV, Boxtel, the Netherlands) was used to provide a preload to the thumb muscles. Two centers (Debrecen and NorthShore) used model SX of the TOF-Watch series, and Mayo Clinic used model S (Figure 2A).

Setup of TetraGraph NMM

The TetraGraph is not currently approved in the United States. It has recently gained CE approval. The design and electronics of the investigational device used for the study are identical to the production device marketed outside the United States. The TetraGraph (Figure 2B) uses proprietary, single-use surface electrodes (Figure 1) for nerve stimulation and recording of compound muscle action potentials (CMAPs). The peak-to-peak amplitudes of CMAPs are used to calculate the TOFR. The amplitude of the CMAP is directly proportional to the number of activated muscle fibers and the force of muscle contraction.¹¹ The surface area of the stimulating electrodes is roughly twice as large (228.5 mm²) as that of commercially available adult ECG electrodes. These electrodes also have an elongated shape and are applied perpendicularly to the course of the ulnar nerve to increase the likelihood of nerve stimulation (Figure 2B). The stimulating electrodes are placed in similar position and with the same polarity as the AMG ECG electrodes (negative electrode placed distally). Similarly, the TetraSens uses silver chloride gel to reduce the impedance and improve electrical conductivity of the skin. The active sensing electrode was attached to the thenar eminence (muscle belly), while the referential electrode was attached to the interphalangeal joint of the thumb (tendon insertion site; Figure 2B).

Neurostimulation

The order of the neuromuscular devices and the applied current intensities were random, at the recorder’s discretion, except for the first 20 volunteers in Debrecen, where an increasing current intensity order was used.

At first, 1 moderate intensity (30 mA) single twitch stimulation was delivered to prepare the volunteers for forthcoming stimulations and obtain an anchor (baseline) VNRS score. Afterward, TOF stimulations were delivered with 20 to 30 to 40 to 50 mA current intensity and 0.2 ms pulse width in random order with both devices. Three stimulations were delivered at each current intensity for 1 device. After these TOF stimulations at each current, the other device was utilized in a similar fashion. The order of each device utilized was random. The time interval between the individual stimulations was 15 s with the TOF-Watch and 20 s with the TetraGraph. The volunteers were asked to rate the discomfort associated to TOF stimulation at each current intensity with both devices on a 0–10 VNRS, anchored by 0 (representing no discomfort) and 10 (representing the worst imaginable discomfort). If the given VNRS scores reached 6, the volunteers were asked if they consented to continue the stimulations. The volunteers had been informed that they could stop the stimulation whenever they felt it intolerable. In addition to the VNRS scores, the TOFRs (or TOF counts [TOFCs]) measured by the 2 devices were recorded. Any adverse events relating to the study were also recorded in the clinical research form.

Statistical Methods

Age and pain scores were reported as mean ± standard deviation (SD) and median (range), while sex was reported as frequency. Mean + SD and median (range) of all pain scores were first calculated by device and current level for descriptive purpose without taking into consideration within-subject correlation.

We evaluated the difference in pain scores between devices using a linear mixed-effects model with unstructured correlation matrix, which accounted for the within-subject correlation across repeated measurements from the 3 stimulations per patients for each device at each current level. Baseline pain scores, current intensity level, age, gender, current level, and center were adjusted in the model.

All tests were 2-sided with α level set at .05 for statistical significance. SAS 9.4 (SAS Institute Inc, Cary, NC) was used for statistical analysis.

After an initial pilot study was completed on 10 volunteers, we determined that a mean VNRS score difference of 0.5 was clinically meaningful.¹⁰ We needed a total of 128 volunteers to have 80% power at the 0.05 significance level to detect a mean difference of ≥0.5 on VNRS, assuming an SD of 2 for the difference between methods, based on paired t test. We recruited a total of 135 volunteers to account for the expected dropouts and technical failures.

RESULTS

One hundred thirty-five subjects (age: 38.3 ± 11.7 years; 62 women and 73 men) were analyzed; each received nerve stimulations with 4 different current amplitudes (20, 30, 40, and 50 mA) in random order with each of the 2 monitors. After completion, 1620 VNRS measurements were obtained among all subjects and currents, and utilizing both devices. The median (range) VNRS scores obtained with TOF-Watch and TetraGraph devices were 2 (0–7) vs 2 (0–8) at 20 mA stimulating current intensity; 3 (1–9) vs 3 (1–9) at 30 mA stimulating current intensity; 5 (1–10) vs 5 (1–10) at 40 mA stimulating current intensity; and 5 (1–10) vs 6 (1–10) at 50 mA stimulating current intensity (Table 1). In the linear mixed-effects model, there were no statistically significant differences in VNRS scores between devices at any of the stimulating current intensities, P = .38 (Table 2). The VNRS scores at individual current intensities (20 vs 30, 20 vs 40, 20 vs 50, 30 vs 40, 30 vs 50, and 40 vs 50 mA) showed significantly higher VNRS scores at higher intensity stimulation (P < .001). Higher anchor VNRS scores were associated with higher pain scores on both devices (P < .001). However, no device effect was observed after adjusting for volunteer age (P = .46) and sex (P = .427). Volunteers at Mayo Clinic had lower VNRS scores than volunteers of the 2 other centers, though clinically this was not significant (P = .0126; Table 2).

Table 1. - Summary of VNRS Scores on Each Device and the Difference in Pain Scores Between Devices

Current Intensity
	20 mA	30 mA	40 mA	50 mA	Total
TOF-Watch VNRS scores
N	405	405	405	405	1620
Mean ± SD	2.2 ± 1.4	3.8 ± 1.9	4.9 ± 2.2	5.7 ± 2.3	4.2 ± 2.4
Median (IQR)	2.0 (1.0 to 3.0)	3.0 (2.0 to 5.0)	5.0 (3.0 to 6.0)	5.0 (4.0 to 7.0)	4.0 (2.0 to 6.0)
Range	(0.0 to 7.0)	(1.0 to 9.0)	(1.0 to 10.0)	(1.0 to 10.0)	(0.0 to 10.0)
TetraGraph VNRS scores
N	405	405	405	405	1620
Mean ± SD	2.3 ± 1.4	3.7 ± 1.9	4.7 ± 2.2	5.7 ± 2.4	4.1 ± 2.3
Median (IQR)	2.0 (1.0 to 3.0)	3.0 (2.0 to 5.0)	5.0 (3.0 to 6.0)	6.0 (4.0 to 8.0)	4.0 (2.0 to 6.0)
Range	(0.0 to 8.0)	(1.0 to 9.0)	(1.0 to 10.0)	(1.0 to 10.0)	(0.0 to 10.0)
VNRS score differences (TetraGraph VNRS-TOF-Watch VNRS)
N	405	405	405	405	1620
Mean ± SD	0.1 ± 1.2	−0.1 ± 1.4	−0.2 ± 1.5	0.0 ± 1.5	−0.1 ± 1.4
Median (IQR)	0.0 (0.0 to 1.0)	0.0 (−1.0 to 1.0)	0.0 (−1.0 to 1.0)	0.0 (−1.0 to 1.0)	0.0 (−1.0 to 1.0)
Range	(−4.0 to 5.0)	(−4.0 to 4.0)	(−5.0 to 6.0)	(−5.0 to 8.0)	(−5.0 to 8.0)

Abbreviations: IQR, interquartile range; SD, standard deviation; VNRS, verbal numerical rating scale.

Table 2. - Main Effects of Device, Current Intensity, and Demographic Parameters on Outcome Variable

Effect	Coefficient Estimate (95% CI)	P Value	Overall P Value
Device: TOF-Watch	Reference	Reference	.3842
Device: TetraGraph	−0.11 (−0.35 to 0.14)	.3842
Current intensity	1.07 (1.00 to 1013)		<.001
Sex: Male	Reference	Reference	.427
Sex: Female	0.10 (−0.15 to 0.36)	.427
Age (y)/1 unit increase	−0.00 (−0.02 to 0.01)	.46	.46
VNRS Anchor/1 unit increase	0.59 (0.51 to 0.66)	<.0001	<.0001
Center: Debrecen	Reference	Reference	.041
Center: NorthShore	−0.16 (−0.49 to 0.16)	.3181
Center: Mayo	−0.39 (−0.70 to −0.09)	.0126

Abbreviations: CI, confidence interval; VNRS, verbal numerical rating scale.

TOFRs were also collected with the TetraGraph and TOF-Watch devices at the 3 sites. However, there were difficulties with 1 site’s ability to consistently obtain TOFRs with the TOF-Watch SX (74% of all readings were TOFCs instead of TOFRs), and the data were excluded from analysis.

There were successful TOFR measurements with the TetraGraph in 91% of the 1620 stimulations. The number of false TOFC readings (when the device gave only a TOFC instead of a TOFR approximating 100%) with TetraGraph was 73 of 405 stimulations (18.0%) at 20 mA stimulating current intensity, 36 (8.9%) at 30 mA stimulating current intensity, and 21 (5.2%) at both 40 and 50 mA stimulating current intensity (P < .001).

The mean ± SD of the 1469 TOFRs obtained with TetraGraph was 100.43% ± 7.74% (95% confidence interval [CI], 100.04–100.83). A total of 64.7% of measurements were in the range of TOFRs 95%–105%, and 87.1% of the measurements fell within the range of TOF ratios 90%–110%. The means ± SDs and 95% CIs of the TOFRs obtained at the individual current intensities are presented in Table 3.

Table 3. - Train-of-Four Ratios Obtained With TetraGraph at Different Stimulating Current Intensities

	Mean ± SD	SE	95% CI
20 mA (n = 332)	100.66 ± 8.55	0.47	99.74–101.58
30 mA (n = 369)	100.81 ± 7.31	0.38	100.07–101.56
40 mA (n = 384)	100.04 ± 7.26	0.37	99.31–100.76
50 mA (n = 384)	100.26 ± 7.85	0.4	99.48–101.05
All (n = 1469)	100.43 ± 7.74	0.2	100.04–100.83

Abbreviations: CI, confidence interval; SD, standard deviation; SE, standard error.

None of the volunteers reported any adverse events related to the study.

DISCUSSION

Based on a pilot investigation, the authors had expected that stimulation with TetraSens electrodes would be less painful compared to the standard ECG electrodes.¹⁰ However, results obtained from this large cohort of 135 volunteers did not support this hypothesis. The TetraSens electrodes and the standard ECG electrodes induced identical discomfort to the volunteers at each current intensity. The VNRS scores increased as a function of stimulating current intensities, which is in agreement with previous reports.^5–7 The age or sex did not influence the level of pain perception. Higher anchor VNRS scores at 30 mA single twitch stimulation yielded higher VNRS scores for all current intensities of TOF stimulation.

Although TOF stimulation poses less discomfort than tetanic or double burst stimulation,⁵ this discomfort is still considerable.^5–7,12 In this investigation, 8 volunteers reported VNRS score ≥6 at 20 mA stimulating current intensity with either device. A VNRS score of 6 was the predetermined upper limit of discomfort at which the volunteers were asked if they agreed to continue the stimulations. Although these volunteers agreed to continue the measurements, 4 volunteers could not tolerate the stimulations at higher intensities and they were ultimately excluded from final analysis. These data imply that there is a need to optimize nerve stimulation conditions to decrease patient discomfort, as neuromuscular monitoring is performed not exclusively in anesthetized patients. One way could be the development of specially designed stimulating electrodes. Kopman¹³ was the first to advocate the application of single-use ECG electrodes for neuromuscular monitoring in 1976 after burn injuries had been reported in association with NM monitoring when bare metal electrodes were used.¹⁴ The electrode gel reduces the resistance and improves the electrical conductivity of the skin. Since then, most currently available NMMs utilize ECG electrodes for neurostimulation and for signal recording by EMG devices. However, the optimal electrode size for diagnostic nerve stimulation has not been extensively investigated¹⁵; rather the polarity and optimal positioning of electrodes have been studied.^16–18 In the field of electrotherapy, numerous investigations have been conducted to explore the effect of electrode size on pain intensity induced by muscle stimulation.^19–21 Though several studies indicated that larger stimulating surfaces are more comfortable, as they decrease the current density,^15,19 the results are not consistent.^20,21 At the same time, the temporal and spatial characteristics of repetitive stimuli used for muscle stimulation are not directly corresponding to currents used for diagnostic nerve stimulation.

The TetraGraph NMM utilizes a silver/silver chloride surface electrode strip for both neurostimulation and CMAP recording (Figure 1). The surface area of the stimulating electrodes is roughly twice as large as that of commercially available adult ECG electrodes, which was designed to disperse the potentially painful electrical stimulus through the skin and the subcutaneous tissues. These electrodes also have an elongated shape and are applied perpendicularly to the course of the ulnar nerve, which could reduce the chance for suboptimal electrode placement (Figure 2B). However, this investigation did not support the hypothesis that a larger conductive area would decrease pain perception.

To reduce patient discomfort, several investigations have advocated the use of lower stimulating intensities (20–30 mA) in the postoperative setting, finding that decreasing the stimulating current did not influence the reliability of measurements.^5–7,12 Currently, there are no guidelines describing the ideal stimulating parameters for postoperative patients. Previous investigations that reported that TOFRs can be obtained reliably at lower stimulating intensities used mechanomyography and AMG.^6,7,12 In the current investigation, the EMG-based device had a significantly lower success rate in obtaining TOFRs at 20 and 30 mA stimulating current intensities (18% and 8.9% vs 5.2%), likely due to the fact that lower current intensities were not able to reliably activate a sufficient number of nerve fibers. In addition, the short duration of individual investigations (approximately 10 minutes) could have been insufficient for optimal curing of the silver–silver chloride gel of the electrodes. This could adversely affect both stimulating and sensing conditions, especially at low current intensities. Yet, once the stimulating intensity was sufficient to evoke detectable CMAPs, the detection of peak-to-peak amplitudes was equally effective at all current intensities, as the stimulating current intensity did not influence the distribution of the measurements (Table 3). Of note, the mean of the 1469 TOFRs obtained with TetraGraph was 100.43% ± 7.74% (standard error = 0.2%), which is nearly identical to the 100% expected in unmedicated volunteers.

The secondary aim of the study, to compare the repeatability of the AMG- and EMG-derived TOFRs, could not be achieved, as 1 center was unable to consistently obtain TOFRs using the TOF-Watch SX. This resulted in the authors being unable to perform a detailed comparison and draw conclusions on the repeatability in obtaining TOFR with the TOF-Watch and TetraGraph. Faulty or damaged piezoelectric transducer has been implicated in the past as a source of error with AMG devices and could have contributed to the failures experienced by one of the sites.

AMG is particularly sensitive to external movements and also exhibits to the so-called “reverse fade phenomenon,” in which the baseline TOFRs, obtained before neuromuscular blockade, often exceed the ideal 100% value²² and have been reported as high as 147%.²³ The imprecision of the technique can be higher when examining unanesthetized volunteers or awake patients, due to the involuntary withdrawal movements in response to nerve stimulation. Baillard et al⁸ drew the attention to this problem in 2004 when they examined 253 patients recovering from anesthesia. Due to the discordance of the measurements, in 24% of the cases the investigators could not tell from 2 sequential AMG TOF stimulations if the patients had residual neuromuscular blockade. To ensure the uniform movement of the thumb and minimize the inherent imprecision of the AMG devices, the use of a hand adapter (Organon BV, Boxtel, the Netherlands) and the fixation of the arm and fingers are advocated.²⁴ Although these measures can effectively improve the precision of the technique,²⁴ they increase the setup time required and may discourage clinicians from the routine use of neuromuscular monitoring. EMG has a fixed recording electrode position. While some authors reported that EMG can also be subject to reverse fade phenomenon and advocated the use of preload devices,^11,25 the extent of this is much smaller compared to AMG²⁵ and the use of a hand adapter is not required.²⁶

Besides the use of the hand adapter, there is another way to decrease the incidence of reverse fade phenomenon and improve clinical application. Model S of the TOF-Watch series (used at Mayo Clinic) uses a modified algorithm to determine the TOFR. When the second signal amplitude (T2) of the TOF is greater than the first amplitude (T1) of the TOF sequence, T2 is used for the calculating the TOFR (TOFR = T4/T2).²⁷ This modified algorithm was shown to reduce the occurrence of reverse fade phenomenon and makes the interpretation of TOFRs easier without significantly reducing the reliability of TOF measurements.²⁷ However, this modification implies that TOF-Watch S cannot be used for scientific purposes.

There were several limitations to this study. One center enrolled 8 more cases than originally prescribed; therefore, 4 incomplete measurements and 4 duplicate measurements were subsequently excluded from analysis. Although the study was underpowered to compare the repeatability of TOFRs, the authors intended to give a descriptive analysis of the TOFRs obtained with EMG and the 2 types of AMG devices. However, the technical problem made this impossible. Also, the study design is unable to account for the carryover effect on VNRS scores from previous stimulations on different devices. As such, the order of devices and currents was kept random in an effort to minimize this confounder.

In conclusion, neurostimulation with the 2 monitors proved to cause the same level of discomfort in this large cohort of unmedicated volunteers from 3 different centers. Increasing the stimulating surface area did not reduce the discomfort of neurostimulation in this setting. The EMG-based TetraGraph NMM had a higher success rate of obtaining TOFRs than the AMG-based TOF-Watch devices in unmedicated individuals, yet the number of false TOFRs was still considerable. The success rate of the TetraGraph was acceptable at lower stimulating current intensities; however, the reliability of low-intensity EMG monitoring in the postoperative setting has not yet been investigated, and this concept needs further investigation to prove its feasibility.

ACKNOWLEDGMENTS

The authors would like to express their gratitude to Dr Franklin Dexter, MD, PhD (University of Iowa, IA) and Zhuo Li, MS (Mayo Clinic, FL) for their guidance with statistical analysis.

DISCLOSURES

Name: Réka Nemes, MD.

Contribution: This author helped write the protocol of the study, collect and analyze the data, and write the manuscript.

Name: György Nagy, MD.

Contribution: This author helped with data collection and writing of the manuscript.

Name: Glenn S. Murphy, MD.

Contribution: This author helped with data collection, data analysis, and writing the manuscript.

Name: Ilana I. Logvinov, DNP, RN.

Contribution: This author helped to write the protocol of the study, collect and analyze data, and write the manuscript.

Name: Béla Fülesdi, MD, PhD, DSci.

Contribution: This author helped to write the protocol of the study, collect and analyze data, and write the manuscript.

Name: J. Ross Renew, MD.

Contribution: This author helped to write the protocol of the study, collect and analyze data, and write the manuscript.

This manuscript was handled by: Ken B. Johnson, MD.