J Clin Monit Comput DOI 10.1007/s10877-014-9565-7

ORIGINAL RESEARCH

Augmentation of motor evoked potentials using multi-train transcranial electrical stimulation in intraoperative neurophysiologic monitoring during spinal surgery Shunji Tsutsui • Hiroshi Iwasaki • Hiroshi Yamada • Hiroshi Hashizume • Akihito Minamide • Yukihiro Nakagawa • Hideto Nishi • Munehito Yoshida

Received: 21 December 2013 / Accepted: 12 February 2014 Ó Springer Science+Business Media New York 2014

Abstract Transcranial motor evoked potentials (TcMEPs) are widely used to monitor motor function during spinal surgery. Improvements in transcranial stimulation techniques and general anesthesia have made it possible to record reliable and reproducible potentials. However, TcMEPs are much smaller in amplitude compared with compound muscle action potentials (CMAPs) evoked by maximal peripheral nerve stimulation. In this study, multi-train transcranial electrical stimulation (mtTES) was introduced to enhance TcMEPs, and the optimal setting of mt-TES was investigated. In 30 patients undergoing surgical correction of spinal deformities (4 males and 26 females with normal motor status; age range 11–75 years), TcMEPs from the abductor hallucis (AH) and quadriceps femoris (QF) were analyzed. A multipulse (train) stimulus with an individual pulse width of 0.5 ms and an inter-pulse interval of 2 ms was delivered repeatedly (2–7 times) at different rates (2, 5, and 10 Hz). TcMEP amplitudes increased with the number of train stimuli for AH, with the strongest facilitation observed at 5 Hz. The response amplitude increased 6.1 times on average compared with single-train transcranial electrical stimulation (st-TES). This trend was also observed in the QF. No adverse events (e.g., seizures, cardiac arrhythmias, scalp burns, accidental injury resulting from patient movement) were observed in any patients. Although several facilitative techniques using central or peripheral stimuli, preceding transcranial electrical stimulation, have been recently employed to augment TcMEPs during

S. Tsutsui (&)  H. Iwasaki  H. Yamada  H. Hashizume  A. Minamide  Y. Nakagawa  H. Nishi  M. Yoshida Department of Orthopaedic Surgery, Wakayama Medical University, 811-1 Kimiidera, Wakayama 641-8510, Japan e-mail: [email protected]

surgery, responses are still much smaller than CMAPs. Changing from conventional st-TES to mt-TES has potential to greatly enhance TcMEP responses. Keywords Intraoperative neurophysiologic monitoring  Motor evoked potential  Multi-train transcranial electrical stimulation  Spinal surgery

1 Introduction It is essential to monitor motor function during spinal surgery that may damage the spinal cord or the spinal nerve roots. Transcranial motor evoked potentials (TcMEPs), which are muscle action potentials elicited by transcranial brain stimulation, have been widely used for multisegment motor pathway monitoring during surgery. Improvements in transcranial stimulation techniques and general anesthesia have made it possible to record reliable and reproducible potentials [1–5]. However, TcMEPs are much smaller in amplitude compared with compound muscle action potentials (CMAPs) evoked by maximal peripheral nerve stimulation, and vary in clinical practice, suggesting that only a limited number of spinal motor neurons innervating the target muscle are excited by the currently used transcranial stimulation techniques [6, 7]. Therefore, reliable interpretation of the critical changes in TcMEPs remains controversial [8–16]. Additionally, in our clinical experience, we have occasionally encountered false negative cases in which patients have suffered from focal postoperative segmental motor weakness mostly due to single nerve root injury, despite no significant change in TcMEP activity during surgery [17]. In such cases, TcMEPs may not have been reliable monitors of activity in motor units damaged intraoperatively, because of radicular

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overlap and different dominancy of each nerve root innervating the recorded muscle [18, 19]. Recently, several facilitative techniques using central or peripheral stimuli, preceding transcranial electrical stimulation, have been employed to achieve sufficient depolarization of motor neurons and augment TcMEP responses during surgery [20–24]. In addition, it was previously reported that recurrent pulse trains at low frequency built up TcMEP responses [25–29]. In this study, the optimal setting of multiple transcranial electrical pulse trains, socalled multi-train transcranial electrical stimulation (mtTES), was systematically investigated to enhance TcMEP responses.

2 Materials and methods Thirty patients undergoing surgical correction of spinal deformities (4 males and 26 females with normal motor status; aged 11–75 years) gave written informed consent to participate in this study, which was approved by the ethical committee of Wakayama Medical University. A total intravenous anesthetic technique was employed. Anesthesia was induced with a bolus of propofol (1.5 mg/ kg), remifentanil (0.5–1.0 lg/kg), and the short-acting muscle relaxant rocuronium (0.6–0.8 mg/kg), and maintained with propofol (6–10 mg/kg/h) and remifentanil (0.25 lg/kg/min). A muscle relaxant was given only at anesthetic induction to facilitate tracheal intubation. A constant-current stimulator (MS-120B, Nihon Koden, Tokyo, Japan) was used for transcranial brain stimulation. A train of five biphasic stimuli, 0.5-ms in duration (two phases of 0.25 ms in each stimulus), was delivered with an intensity of 200 mA (maximal intensity of the stimulator used) and an inter-pulse interval of 2 ms via a pair of corkscrew electrodes (001–220; Agram, NJ, USA) symmetrically inserted into the scalp, 5 cm lateral and 2 cm forward of Cz (International 10-20 System of electrode placement), based on the method of Matsuda and Shimazu [30]. TcMEPs were recorded from a pair of needle electrodes (NE-220B; Technomed Europe, Amerikalaan, The Netherlands) inserted in the muscle belly of the abductor hallucis (AH) and quadriceps femoris (QF). All measurements were taken before any corrective manipulation of the spine was performed after complete recovery from the effect of the muscle relaxant, which was monitored using the ‘‘Train of Four’’ technique. A multipulse (train) stimulus was delivered repeatedly (2–7 times) at different rates (2, 5, and 10 Hz), and was defined as mt-TES. The amplitudes of TcMEP responses after mt-TES were compared with those elicited by conventional single-train transcranial electrical stimulation (stTES).

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Fig. 1 Augmentation of motor evoked potentials recorded from the AH muscle by mt-TES at different repetitive rates (2, 5, and 10 Hz). Each individual train consists of five biphasic pulses 0.5-ms in duration (two phases of 0.25 ms in each pulse) and a 2.0-ms interpulse interval. The number of train stimuli was changed from two to seven. st-TES single-train transcranial electrical stimulation

3 Results The mean amplitudes of the TcMEPs recorded by st-TES immediately before the measurement using mt-TES were 0.616 mV (range 0.01–2.49 mV) for AH and 0.186 mV (range 0.01–0.78 mV) for QF. TcMEP amplitudes increased with the number of train stimuli for AH, and the strongest facilitation was observed at a repetition rate of 5 Hz (Fig. 1). The response amplitude increased up to 6.1 times on average compared to st-TES (Fig. 2). This trend was also observed in the QF (Fig. 3). The response amplitude increased up to 8.0 times on average compared with st-TES (Fig. 4). No adverse events (e.g., seizures, cardiac arrhythmias, scalp burns, accidental injury resulting from patient movement) were observed in any patients.

4 Discussion The present investigation demonstrated that mt-TES is a simple and effective method to augment TcMEPs in intraoperative neurophysiologic monitoring during spinal surgery. Conditioning stimulation techniques have been used for enhancement of transcranially evoked motor responses [31]. Conditioning stimuli are applied prior to a test stimulus and increase the excitability of cortical and/or spinal motor neurons. According to Journe´e et al. [31], conditioning stimulation can be classified into two categories: (1) heteronymous stimulation in which conditioning stimuli are applied at a different site from a test stimulus,

J Clin Monit Comput

Fig. 2 The proportion of augmentation of motor evoked potentials by mt-TES recorded from the AH muscle at different repetitive rates (2, 5, and 10 Hz) compared to those elicited by single-train stimulation. Each individual train consists of five biphasic pulses 0.5-ms in duration (two phases of 0.25 ms in each pulse) and a 2.0-ms inter-

Fig. 3 Augmentation of motor evoked potentials recorded from the QF muscle by mt-TES at different repetitive rates (2, 5, and 10 Hz). Each individual train consists of five biphasic pulses 0.5-ms in duration (two phases of 0.25 ms in each pulse) and a 2.0-ms interpulse interval. The number of train stimuli was changed from two to seven. st-TES single-train transcranial electrical stimulation

and (2) homonymous stimulation in which both conditioning and test stimuli are applied at the same site. One homonymous conditioning stimulation technique is repetitive multipulse (train) TES, as described by Deletis [25], Deletis and Sala [28]. He applied train TES repeatedly with an intertrain interval (ITI) of 0.5 or 1 s, and reported that each consecutive muscle response had increasing amplitude. In addition, MacDonald et al. [26,

pulse interval. The amplitude of potentials increased with the number of train stimuli. The strongest facilitation was observed at 5 Hz and the response amplitude increased up to 6.1 times on average. st-TES single-train transcranial electrical stimulation, mt-TES multi-train transcranial electrical stimulation

27] demonstrated progressive facilitation after the repetition of four pulse trains at 2–5 Hz during scoliosis surgery. Another homonymous conditioning is double-train TES (dt-TES) developed by Journe´e et al [21]. They demonstrated that dt-TES elicited a marked facilitation of TcMEPs when the ITI was short (10 ms B ITI B 40 ms) or long (ITI C 0.1 s). Taking these previous conditioning techniques into account, train TES was delivered repeatedly at repetitive rates of 2, 5, and 10 Hz (ITI; 0.5, 0.2 and 0.1 s, respectively) in this study. The amplitudes of TcMEPs increased with the number of train stimuli in both the AH and QF, consistent with the finding of Deletis [25]. The strongest augmentation of TcMEPs was observed at a repetition rate of 5 Hz (ITI; 0.2 s) in both muscles. The mechanism of augmentation of TcMEPs by mt-TES is unclear. However, central mechanisms at the level of the brain and spinal cord may be involved as previously reported in studies of conditioning stimulation techniques. Journe´e et al. [31] observed a cortical silent period after TES of about 0.1 s in anesthetized patients, which could be a possible explanation for the greater augmentation at 5 compared with 10 Hz. The disadvantage of homonymous facilitation using high intensity stimuli is the vigorous contractions and twitches of proximal muscle groups that interfere with surgery and put patients at risk of spinal cord injury, and spinal nerve root, eye, tongue, and lip injuries [22]. However, accidental injury resulting from patient movement was not experienced in this study, and was avoided by brief surgical pauses (a few seconds) for monitoring of TcMEPs, coordinated between surgical and electrophysiological teams [32]. In addition, no adverse events such as seizures, cardiac arrhythmias, and scalp burns, were observed in any of the patients.

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Fig. 4 The proportion of augmentation of motor evoked potentials by mt-TES recorded from the QF muscle at different repetitive rates (2, 5, and 10 Hz) compared to those elicited by single-train stimulation. Each individual train consists of five biphasic pulses 0.5-ms in duration (two phases of 0.25 ms in each pulse) and a 2.0-ms inter-

pulse interval. The amplitude of potentials increased with the number of train stimuli. The strongest facilitation was observed at 5 Hz and the response amplitude increased up to 8.0 times on average. st-TES single-train transcranial electrical stimulation, mt-TES multi-train transcranial electrical stimulation

To our knowledge, this is the first report to demonstrate an appropriate clinical setting for mt-TES systematically. However, there are a number of limitations to this study. First, train TES was applied up to 7 times because of the limitation of the equipment. More stimuli may result in greater augmentation of TcMEPs. Second, only patients without motor dysfunction were enrolled. Journe´e et al. [21] reported that facilitation with dt-TES appeared to be most effective when the TcMEPs elicited by st-TES were small or absent. TcMEPs are usually poor or absent in patients with preoperative neurological deficits. Third, only repetitive rates equal to or less than 10 Hz were assessed because of safety issues of repeated TES. As described above, the ITI of 10–40 ms (repetitive rate; 25–100 Hz) is optimal for augmentations of TcMEP responses when using dt-TES [21]. However, continuous brain stimulation over a period of a few seconds with a frequency of 50–60 Hz was reported to easily induce seizures [33]. Finally, there was no ‘‘true positive’’ case in which postoperative neurological deterioration was related to intraoperative critical changes of TcMEPs elicited by mt-TES. Thus, it is unclear how precisely TcMEPs elicited by mtTES can reflect intraoperative damage to the spinal cord and spinal nerve root compared with those elicited by stTES. Further clinical and basic investigation is required to assess the usefulness of mt-TES as a routine method in neurophysiologic monitoring during spinal surgery.

Ethical standards of Japan.

5 Conclusion Changing from conventional st-TES to mt-TES has potential to greatly enhance TcMEP responses.

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Conflict of interest

The experiments comply with the current laws

None.

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Augmentation of motor evoked potentials using multi-train transcranial electrical stimulation in intraoperative neurophysiologic monitoring during spinal surgery.

Transcranial motor evoked potentials (TcMEPs) are widely used to monitor motor function during spinal surgery. Improvements in transcranial stimulatio...
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