Clinical Neurophysiology 126 (2015) 1264–1270
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Role of multimodal intraoperative neurophysiological monitoring during positioning of patient prior to cervical spine surgery Julio Plata Bello a,⇑, Pedro Javier Pérez-Lorensu b, Héctor Roldán-Delgado a, Liberto Brage a, Verónica Rocha a, Vanessa Hernández-Hernández a, Ayoze Dóniz a, Víctor García-Marín a a b
Hospital Universitario de Canarias (Department of Neurosurgery), S/C de Tenerife, Spain Hospital Universitario de Canarias (Intraoperative Neurophysiologic Monitoring Unit), S/C de Tenerife, Spain
a r t i c l e
i n f o
Article history: Accepted 17 September 2014 Available online 2 October 2014 Keywords: Intraoperative neurophysiological monitoring Cervical spine surgery Neck positioning
h i g h l i g h t s Neck positioning during cervical spine surgery may lead to spinal cord injury. Intraoperative neurophysiological monitoring (IONM) helps to prevent spinal cord injury during neck
positioning. Transcranial motor evoked potentials (TcMEP) showed a higher sensitivity than somatosensory
evoked potentials (SEPs) in detecting mechanical injury to the spinal cord during neck/or arm positioning.
a b s t r a c t Objective: To determine the use of multimodal intraoperative neurophysiological monitoring (IONM) during positioning procedures in cervical spine surgery. Methods: IONM data was collected from 75 patients from the onset of positioning to the end of the surgical procedure. These included: transcranial motor evoked potentials (TcMEP), somatosensory evoked potentials (SEP) and free running electromyography (EMG) recordings. Sensitivity, specificity, positive predictive value (PPV) and negative predictive value (PNV) were calculated. Results: IONM warnings were given in 5 cases during neck positioning. These consisted of the disappearance of TcMEP in all the cases, while two cases showed a loss of SEPs as well. Four of these patients presented a complete recovery of TcMEP and SEPs after neck repositioning. The patient in which this recovery was not present, woke up with new postoperative neurological deficits. Sensitivity, specificity, PPV and NPV of TcMEP during cervical positioning were all 100%. Sensitivity of SEPs was 40%; specificity and PPV were 100%; and the NPV of SEPs was 95.9%. Conclusion: Multimodal IONM is a useful method to prevent spinal cord injury during neck positioning in cervical spine surgical procedures. TcMEPs showed the highest sensitivity in detecting injuries to cervical spine related to neck positioning. Significance: Multimodal IONM should not only be considered for detecting intra-operative warnings, but also during positioning. Ó 2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Intraoperative neurophysiological monitoring (IONM) is not used as a routine in spine surgery in many centers, although it is ⇑ Corresponding author at: Hospital Universitario de Canarias (Neuroscience department), Calle Ofra s/n La Cuesta, CP 38320 La Laguna, S/C de Tenerife, Spain. Tel.: +34 922 255 544/646 625 973. E-mail address: [email protected] (J. Plata Bello).
a standard of care in scoliosis procedures (Tomé-Bermejo et al., 2014). Indeed, irreversible changes during IONM are predictive of severe adverse neurological outcomes (level of evidence class A) (Nuwer et al., 2012) which is why it is becoming more popular in cervical spine procedures because it seems to be producing better functional results (Li et al., 2012; Clark et al., 2013). Certain studies point out that the combination of somatosensory evoked potentials (SEPs) and motor evoked potentials (MEPs)
http://dx.doi.org/10.1016/j.clinph.2014.09.020 1388-2457/Ó 2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
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in IONM is more effective than the use of only one of these methods for the detection of neurological injury during the surgical procedure (Pelosi et al., 2002; Costa et al., 2007; Sutter et al., 2007; Clark et al., 2013). However, neurological injury may not only appear during the surgical procedure itself, but can also occur during neck or arm positioning before surgery (Bose et al., 2004; Jahangiri et al., 2011). Therefore, IONM should be considered during this early stage of the surgical approach to prevent neurological injury that may turn out to cause new motor and/or sensory clinical deficits and consequently a worse functional outcome. To the best of our knowledge, apart from some case reports, no research has focused on this issue. The aim of the present study is to evaluate the use of SEPs and MEPs in detecting injury to the nervous system during neck and/or arm positioning for anterior and posterior cervical spine procedures. 2. Materials and methods 2.1. Patients Seventy-five consecutive patients (22 female; mean age of 60.15, SD = 15.1) who were undergoing cervical spine surgery from January to September 2013 were recruited for the study. Table 1 summarizes the diagnoses of this patient cohort and Table 2 indicates the cervical levels that were approached. IONM was performed in all patients and consisted of SEPs, MEPs and EMG recordings during the whole surgical procedure, from positioning to re-positioning in bed after surgery. 2.2. Anesthesia Midazolam was used for sedation and total intravenous anesthesia (TIVA) was used in all patients (Valverde Junguito et al., 2007). Induction was done with propofol 3 mcg/kg, remifentanil 0.15–0.25 mcg/kg. After induction, intravenous rocuronium 30 mg was only administered for intubation purposes. No further doses of neuromuscular blocking agents were used after that. Anesthesia was maintained by infusion with propofol (range, from 2 to 3 mcg/L) and remifentanil (0.5 mcg/kg/min). Before positioning, gamma-cyclodextrin (sugammadexÒ) 4–8 mg/kg was administered to reverse neuromuscular blockade and to prevent any interference in the motor evoked muscle responses (Reid et al., 2011). No inhalational agents were ever used for induction or during the surgical procedure. 2.3. IONM recording All procedures were recorded by the same clinical neurophysiologist and intraoperative neurophysiologic monitoring device (Cadwell Cascade, Cadwell Labs, USA) and followed the standard procedure setup (Valverde Junguito et al., 2007). 2.3.1. Somatosensory evoked potentials (SEPs) A pair of stimulating surface electrodes (AmbuÒ Neuroline 72015-K) was applied on the posterior tibial nerve at the ankle
Table 1 Primary indications for surgery.
Table 2 Cervical levels approached. Level Single level
Multilevel
No. of cases C1–C2 C2–C3 C3–C4 C4–C5 C5–C6 C6–C7
0 1 6 11 17 18 22
and median nerve at the wrist bilaterally. An electrical pulse stimulation of 30 mA, 5.1 Hz frequency, 0.2 ms duration was used. Subdermal corkscrew electrodes (AmbuÒ Subdermal Corkscrew) were used to record SEPs from the scalp. The SEPs were recorded at C3, C4, Cz and Fpz (10–20 International System) with derivations including C3–Cz, C4–Cz, C3–C4, Cz–Fz and peripheral responses, using a bandpass of 1–300 Hz. Warning criteria were defined as a 50% decrease in amplitude or a 10% increase in latency uni- or bilaterally. 2.3.2. Transcranial motor evoked potentials (TcMEPs) Stimulation was performed using a multipulse technique based on a train of 7 pulses with an interstimulus interval (ISI) of 4 ms, pulse width of 50 ls, and an intensity between 240 and 400 V, delivered at C1–C2 by corkscrew electrodes (TCS Stimulator, Cadwell Labs, USA). Muscle MEPs were recorded by paired subdermal needle electrodes from the first dorsal interosseus (FDI) in the upper limbs and tibialis anterior (TA) and abductor hallucis (AH) in the lower limbs. Band pass was 10–1500 Hz. An 80% decrease in amplitude or a 10% increase in latency unilaterally or bilaterally or an increase of 100 V stimulation intensity were used to detect the MEPs over the basal threshold as warning criteria. 2.3.3. Free-running electromyography (EMG) A continuous intraoperative free running EMG was recorded from the upper limbs over both deltoids and biceps to detect C5– C6 radiculopathy using twisted paired stainless-steel subdermal needle electrodes (AmbuÒ 12 0.40 mm). 2.4. Statistical analysis Sensitivity and specificity, as well as positive and negative predictive values were calculated. A true positive was defined as the presence of irreversible SEP and/or TcMEP warnings during positioning or during the surgical procedure followed by neurological deficits in the postoperative period. On the other hand, a true negative was defined as the absence of monitoring alerts or the recovery of the potentials after re-positioning and absence of new neurological deficits after surgery. A false positive was defined as the presence of SEP and/or TcMEP warnings during positioning or during the surgical procedure that was not followed by neurological deficits in the postoperative period. A false negative was defined as the absence of warnings during IONM or recovery of SEPs or MEPs after re-positioning but the presence of new neurological deficits after surgery. All analyses were performed on the data using SPSS 18.0 (SPSS Inc., Chicago). 3. Results
Diagnosis
%
Degenerative myelopathy Disc herniation Fracture/luxation Tumour
50.7 24.0 22.7 2.7
Out of seventy-five patients, thirty-nine patients (52%) underwent cervical spinal surgery using an anterior approach while the rest were operated on using a posterior approach. Twelve patients (16%) presented altered TcMEP and SEP recordings at
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baseline which were clinically compatible to their neurological exam. A warning based on IONM was issued in 5 cases during positioning. All of them presented a sudden complete loss of TcMEP during neck positioning. Additionally, two of those patients also presented a loss of SEPs. In other words, three cases presented only TcMEP warning while the other two had both TcMEP and SEP warning, in spite of increasing the stimulation intensity over 100 V. Secondary causes of potential loss were ruled out (e.g. low blood pressure or any anesthesia interference) in every case. Four of the five patients mentioned above, showed a recovery to their baseline evoked potentials after re-positioning of the neck and none of them presented neurological deficits after the surgical procedure (Table 3; Fig. 1a). This recovery was progressive after repositioning and the time they reached their baseline was variable. In any case, it was always completely recovered before the end of the surgery and the onset of the recovery was clearly related with the change of posture. However, the other patient did not recover to baseline in spite of re-positioning and increasing the patient´s blood pressure. The surgeon rejected making a wake-up test and, eventually, an urgent anterior decompression was performed without any improvement in evoked potentials during the surgery (Table 3; Figs. 1b and 2). The patient suffered postsurgical tetraparesia but finally completely recovered after 2 weeks of rehabilitation. Only three patients had IONM warnings during the surgical procedure, and all three of them presented motor and sensory deficits after the procedure (true positives) (Table 4). The rest of the patients, including those who presented IONM warnings during positioning and recovered basal responses, did not present new postoperative neurological deficits (true negatives). No false negatives or false positives were documented. In such patients, brachial plexus injury was ruled out by demonstrating the presence of variations in TcMEPs and/or SEPs in upper limbs, with normal recordings in lower limbs. The three true positive patients that presented IONM warnings during the surgical procedure had different outcomes to each other. Two of them recovered completely after rehabilitation over 3–6 months. However, the other one presents important disability and mobility restriction. No further discussion of these data is made because it is beyond the scope of the present research. Finally, none of the patients presented warnings on free EMG recording and no cases of postoperative radiculopathy were observed. In the series presented here, the use of TcMEPs during neck positioning presented 100% sensitivity and specificity while SEPs had 40% sensitivity and 100% specificity, with a negative predictive value (NPV) of 95.9%. On the other hand, the use of both TcMEPs and SEPs for monitoring the surgical procedure presented positive and negative predictive values of 100% (Table 4).
4. Discussion The present observational study has focused on the role of IONM during neck positioning in severe cervical myelopathic patients. The main finding was the observation of a complete loss of TcMEPs in 5 cases and its reappearance in four cases after repositioning. In the other case, irreversible TcMEP loss correlated with a new postoperative neurological deficit in accordance with previous studies (Nuwer et al., 2012). One of the most important clinical implications of this study is the potential utility of this technique in predicting and avoiding spinal cord injury provoked by an inadequate surgical position. Mechanical injury to the spinal cord is most likely a result of neck manipulation during patient positioning for the surgical procedure. This stage includes intubation, neck positioning and downward traction of the shoulders. Considering the potential risk of injury that these manoeuvres may imply, perioperative monitoring is still necessary to prevent new life-changing neurological deficits. During the anesthetic procedure, fiberoptic intubation may be requested in selected cases of cervical spinal cord surgeries, especially in cases where radiculopathy or significant instability of the cervical spine is present (Fessler and Sekhar, 2006). Moreover, Malcharek et al. (2012) have proposed the performance of awake fiberoptic intubation and self-positioning to achieve continuous preoperative neurological monitoring (Malcharek et al., 2012). However, this technique may not be suitable for all kinds of patients, in this respect, neurophysiological monitoring could acquire a relevant role during this pre-surgical step. However, intubation is not the most harmful procedure for the cervical spinal cord. The positioning of the neck is probably the most relevant factor that may induce damage at this level. Anterior and posterior cervical approaches require different positions of the neck. A neutral position of the neck is necessary in anterior approaches, although a slight cervical extension is sometimes used. On the other hand, posterior approaches tend to place the cervical spine in a slight flexion, usually aided by a head holder three point skull fixation system (Stevens et al., 1997). Bearing this in mind, the diameters of the cervical canal may be reduced significantly (flexion and extension) and lead to a possible injury to the spinal cord in patients with previous cervical spine pathology. In this sense, Morishita et al. (2013) identified a deterioration of SEPs in cervical spondylotic myelopathy patients during extension of the neck in positioning steps (Morishita et al., 2013) and other authors have also described similar findings (Kraus and Christophis, 1994; Haavik-Taylor and Murphy, 2007; Insola et al., 2010). A prolongation of central motor conduction time by neck extension in compressive cervical myelopathy has also been reported (Heidegger and Ziemann, 2011). Therefore, the dynamics of the cervical spine or the presence of instabilities may lead to spinal cord injury and, consequently, to neurological deficits.
Table 3 Features of the five patients who presented IONM alerts during positioning. Gender
Age
Diagnosis
Approach
Warning
Outcome
Patient 1
Male
50
Degenerative myelopathy
Anterior
Loss of MEPs in both AH and TA. Loss of cortical SEPs
Recovery after neck reposition. No deficit
Patient 2
Male
77
Degenerative myelopathy
Posterior
Loss of right TA and AH MEPs
Recovery after repositioning of the arms. No deficit
Patient 3
Male
50
Disc herniation
Anterior
Loss of both FDI, right TA and right AH. Loss of cortical SEPs
No recovery. Postsurgical deficit
Patient 4
Male
69
Degenerative myelopathy
Posterior
Loss of right FDI and both TA
Recovery after neck reposition. No deficit
Patient 5
Male
47
C5-C6 luxation
Posterior
Loss of MEPs in both AH and TA
Recovery after neck reposition. No deficit
AH: Abducens Hallucis; FDI: First Dorsal Interosseus; TA: Tibial Anterior.
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Fig. 1. Examples of IONM alerts during neck positioning. (A) IONM screenshot showing the loss of MEPs with normal SEPs during neck positioning and their reappearance after posture correction (Patient 4). A loss of right FDI and both TA are present after positioning and they are recovered after a modification in the posture. The signal return to the baseline before the end of the surgery (data not shown); (B) IONM screenshot showing the irreversible loss of MEPs and SEPs during neck positioning (Patient 3). A loss of bilateral FDI, right TA and right AH are presented in the TcMEPs (superior panel). The SEPs are of poor quality (inferior panels), but they show a loss without recovery of left median SEPs. The attempts of repositioning are not indicated because they were multiple and no change in the monitoring with any posture was observed after maintaining each posture for at least 3 min. Abbreviations: AbdH: Abducens Hallucis; FDI: First Dorsal Interosseus; TA: Tibial Anterior.
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Fig. 2. Pre-surgical Magnetic Resonance Imaging (MRI) of the patient who did not recover either TcMEPs or SEPs after neck repositioning. (A) Sagital T2 weighted image of the cervical spine, showing a C5–C6 disc herniation with caudal migration and compression of the spinal cord. (B) Axial T2 weighted image showing the intense spinal cord compression produced by the disc herniation. The patient was rapidly operated on, conducting an anterior decompression. He suffered a post-operative tetraparesis and he eventually recovered after two weeks of rehabilitation.
Table 4 Contingency tabulation of data from the patients presenting IONM warning. Postsurgical outcome
TcMEP warning No
Yes Permanent
Surgical warning Reversible
Deficits present 0 1 0 3 Deficits absent 67 0 4 0 The use of TcMEPs during neck positioning presented 100% sensitivity and specificity. No false positives or false negatives were detected Deficits present 0 1 0 3 Deficits absent 70 0 1 0 The use of SEPs during neck positioning presented 40% sensitivity (two patients did not present changes in SEP recordings while losses of TcMEPs were recorded) and 100% specificity. No false positives were detected
Further, another phase of positioning is arm and shoulder placement. Traction to provide adequate lateral X-ray view of lower levels of cervical spine is necessary in cervical spine procedures. When the shoulders are directed downwards, this could lead to neurological injury secondary to an elongation of the brachial plexus. In this sense, Jahangiri et al. (2011) documented a deterioration of SEPs followed by a loss of TcMEPs during draping with a spontaneous recovery shortly after removing all of the tapes (Jahangiri et al., 2011). Considering that surgical procedures for the cervical spine require specific positioning of the neck, damage to the spinal cord or nerve roots/plexus may occur. A surprising finding of the present work has been the existence of more warnings during cervical positioning than during the surgical procedure itself. This finding might be of great relevance, because positioning is a stage that is not routinely monitored and, as this work shows, it is a risky procedure that may compromise the spinal cord function. Previous works focusing on IONM during cervical spine surgery have not considered the possibility that neck positioning might be a source of postoperative neurological deficits, unrelated to the surgical procedure itself. In this sense, although multimodal IONM has been shown to have the highest sensitivity and specificity rates, some series have reported the existence of some false negatives among their cases (Eggspuehler et al., 2007; Smith et al., 2007; Sutter et al., 2007). This means that no IONM alerts occurred when
post-surgical neurological deficits existed. One of the possible explanations for these false negatives is that positioning was not adequately monitored and baseline potentials were acquired when the patient was already positioned. In these cases, spinal cord or nerve root damage could have developed during this pre-surgical step and, because of that, no objective warning sign was established. Warning signs in neurophysiological monitoring during positioning have been previously described by Bose et al. (2004) in a series of cases of anterior cervical spine surgeries with SEP monitoring. They detected three alerts related to a hyperextension of the neck and one to arm position (Bose et al., 2004). Bearing this in mind, the authors suggested that IONM provides valuable information during patient positioning before anterior cervical fusion. As was previously pointed by Anderson RC et al. in a case report (Anderson et al., 2001), the present work has shown that the IONM is also a useful technique for monitoring the positioning during posterior cervical approaches. Therefore, neck positioning is a dangerous manoeuvre that might lead to more damage to the spinal cord than even the surgery itself in certain cases. Because of this, the use of IONM seems to be suitable in this pre-surgical step. The type of monitoring to be performed during positioning could also be a matter of debate. Monitoring TcMEPs is supposed to provide earlier detection of neurological injury and is associated with greater sensitivity (Hilibrand et al., 2004). Its superiority to
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SEPs has been reported in previous works (Clark et al., 2013), and that is compatible with the findings reported here, where TcMEPs showed greater sensitivity for identifying positioning related injuries. However, certain authors still recommend the use of both modalities (Costa et al., 2007; Sutter et al., 2007). Positioning should be monitored using TcMEPs, considering the higher rates of false negatives that have been described when only using SEPs. Nevertheless, considering that true positive isolated SEP loss and preservation of TcMEP responses have been reported (ToméBermejo et al., 2014), it would seem logical to recommend the use of both modalities in combination. Moreover, something that has to be emphasized is that the changes in the TcMEP monitoring in all of the cases which presented a warning were a complete loss of response. This condition shows the presumable high sensitivity of the TcMEPs in identifying spinal cord compressions secondary to an inadequate positioning. On the other hand, the reversibility that experienced the TcMEPs in four patients after cervical realignment should also be highlighted. This IONM technique might allow not only the identification, but also the prevention of damage to the spinal cord by indicating the best cervical position. The case without reversible TcMEP recording shows the good correlation between this technique with the neurological postsurgical outcome, as has been stated previously (Nuwer et al., 2012). The higher rate of postoperative deficits (4/75 = 5.3%) than previously reported risk (Cramer et al., 2009) should also be mentioned. The possible explanation of this finding might be the severity of the operated cases. As is shown in Table 1, more than 50% of patients showed myeloptahy and more than 20% of patients presented tumors or trauma related injuries where the complexity of the surgical procedure is normally higher. Therefore, the severity of the cases presented here may be higher than other presented series and this might be the explanation of the higher frequency in post-operative deficits. On the other hand, these complex cases could benefit most by this sort of monitoring during positioning, because their positions seem to present a small margin of error. Apart from preventing the possible development of new neurological deficits, IONM has important medico-legal implications. One of the most common causes of litigation involving the cervical spine is postoperative quadriparesis/quadriplegia (Epstein, 2013). Considering that an inadequate position could lead to one of these life-changing complications, neurophysiological monitoring during neck and/or arm positioning would therefore have an important role, particularly in cases with myelopathy.
5. Conclusion Positioning during cervical procedures is a potentially damaging manoeuvre that may require an adequate neurophysiological monitoring technique in order to prevent damage to the spinal cord and consequently, the development of new postoperative neurological deficits. In this sense, the loss of TcMEPs seems to indicate any potential damaging position of the neck. This loss of TcMEPs may not be definitive, because their recovery is described after modifying the position of the neck and no neurological deficits when this occurred. In other words, the present work has shown that TcMEP loss can be reversible after repositioning and this has a good correlation with the final clinical outcome. On the other hand, although it might be biased by the complexity of the cases, more warnings in the IONM during positioning than during the surgical procedure were identified. This might underline the importance of monitoring in pre-surgical manoeuvres, mostly in severe cases.
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Therefore, IONM during cervical positioning allows the immediate identification of spinal cord damage, thereby preventing a potential neurological deficit by correcting neck and/or arm position. Disclosure All authors declare no conflict of interest with respect to the authorship or the publication of this article. References Anderson RC, Emerson RG, Dowling KC, Feldstein NA. Attenuation of somatosensory evoked potentials during positioning in a patient undergoing suboccipital craniectomy for Chiari I malformation with syringomyelia. J Child Neurol 2001;16:936–9. Bose B, Sestokas AK, Schwartz DM. Neurophysiological monitoring of spinal cord function during instrumented anterior cervical fusion. Spine J 2004;4:202–7. Clark AJ, Ziewacz JE, Safaee M, Lau D, Lyon R, Chou D, et al. Intraoperative neuromonitoring with MEPs and prediction of postoperative neurological deficits in patients undergoing surgery for cervical and cervicothoracic myelopathy. Neurosurg Focus 2013;35:E7. Costa P, Bruno A, Bonzanino M, Massaro F, Caruso L, Vincenzo I, et al. Somatosensory- and motor-evoked potential monitoring during spine and spinal cord surgery. Spinal Cord 2007;45:86–91. Cramer DE, Maher PC, Pettigrew DB, Kuntz C. Major neurologic deficit immediately after adult spinal surgery: incidence and etiology over 10 years at a single training institution. J Spinal Disord Tech 2009;22:565–70. Eggspuehler A, Sutter MA, Grob D, Jeszenszky D, Porchet F, Dvorak J. Multimodal intraoperative monitoring (MIOM) during cervical spine surgical procedures in 246 patients. Eur Spine J 2007;16(Suppl 2):S209–15. Epstein NE. The need to add motor evoked potential monitoring to somatosensory and electromyographic monitoring in cervical spine surgery. Surg Neurol Int 2013;4:S383–91. Fessler RG, Sekhar L. Atlas of Neurosurgical Techniques. In: Dille B, editor. Spine and peripheral nerves. 1st ed. New York: Thieme; 2006. Haavik-Taylor H, Murphy B. Cervical spine manipulation alters sensorimotor integration: a somatosensory evoked potential study. Clin Neurophysiol 2007;118:391–402. Heidegger T, Ziemann U. Prolongation of central motor conduction time by neck extension in compressive cervical myelopathy. Clin Neurophysiol 2011;122:1891–3. Hilibrand AS, Schwartz DM, Sethuraman V, Vaccaro AR, Albert TJ. Comparison of transcranial electric motor and somatosensory evoked potential monitoring during cervical spine surgery. J Bone Joint Surg Am 2004;86-A:1248–53. Insola A, Padua L, Mazzone P, Valeriani M. Effect of movement on SEPs generated by dorsal column nuclei. Clin Neurophysiol 2010;121:921–9. Jahangiri FR, Holmberg A, Vega-Bermudez F, Arlet V. Preventing position-related brachial plexus injury with intraoperative somatosensory evoked potentials and transcranial electrical motor evoked potentials during anterior cervical spine surgery. Am J Electroneurodiagnostic Technol 2011;51:198–205. Kraus R, Christophis P. [Functional studies of the spinal cord in chronic stenosing diseases of the cervical spine using somatosensory evoked potentials]. Zentralbl Neurochir 1994;55:96–101. Li F, Gorji R, Allott G, Modes K, Lunn R, Yang Z-J. The usefulness of intraoperative neurophysiological monitoring in cervical spine surgery: a retrospective analysis of 200 consecutive patients. J Neurosurg Anesthesiol 2012;24:185–90. Malcharek MJ, Rogos B, Watzlawek S, Sorge O, Sablotzki A, Gille J, et al. Awake fiberoptic intubation and self-positioning in patients at risk of secondary cervical injury: a pilot study. J Neurosurg Anesthesiol 2012;24:217–21. Morishita Y, Maeda T, Ueta T, Naito M, Shiba K. Dynamic somatosensory evoked potentials to determine electrophysiological effects on the spinal cord during cervical spine extension: clinical article. J Neurosurg Spine 2013;19: 288–92. Nuwer MR, Emerson RG, Galloway G, Legatt AD, Lopez J, Minahan R, et al. Evidencebased guideline update: intraoperative spinal monitoring with somatosensory and transcranial electrical motor evoked potentials: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 2012;78:585–9. Pelosi L, Lamb J, Grevitt M, Mehdian SMH, Webb JK, Blumhardt LD. Combined monitoring of motor and somatosensory evoked potentials in orthopaedic spinal surgery. Clin Neurophysiol 2002;113:1082–91. Reid S, Shields MO, Luney SR. Use of sugammadex for reversal of neuromuscular blockade in 2 patients requiring intraoperative neurophysiological monitoring. J Neurosurg Anesthesiol 2011;23:56–7. Smith PN, Balzer JR, Khan MH, Davis RA, Crammond D, Welch WC, et al. Intraoperative somatosensory evoked potential monitoring during anterior cervical discectomy and fusion in nonmyelopathic patients – a review of 1039 cases. Spine J 2007;7:83–7. Stevens WR, Glazer PA, Kelley SD, Lietman TM, Bradford DS. Ophthalmic
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Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Role of multimodal intraoperative neurophysiological monitoring during positioning of patient prior to cervical spine surgery Julio Plata Bello a,⇑, Pedro Javier Pérez-Lorensu b, Héctor Roldán-Delgado a, Liberto Brage a, Verónica Rocha a, Vanessa Hernández-Hernández a, Ayoze Dóniz a, Víctor García-Marín a a b
Hospital Universitario de Canarias (Department of Neurosurgery), S/C de Tenerife, Spain Hospital Universitario de Canarias (Intraoperative Neurophysiologic Monitoring Unit), S/C de Tenerife, Spain
a r t i c l e
i n f o
Article history: Accepted 17 September 2014 Available online 2 October 2014 Keywords: Intraoperative neurophysiological monitoring Cervical spine surgery Neck positioning
h i g h l i g h t s Neck positioning during cervical spine surgery may lead to spinal cord injury. Intraoperative neurophysiological monitoring (IONM) helps to prevent spinal cord injury during neck
positioning. Transcranial motor evoked potentials (TcMEP) showed a higher sensitivity than somatosensory
evoked potentials (SEPs) in detecting mechanical injury to the spinal cord during neck/or arm positioning.
a b s t r a c t Objective: To determine the use of multimodal intraoperative neurophysiological monitoring (IONM) during positioning procedures in cervical spine surgery. Methods: IONM data was collected from 75 patients from the onset of positioning to the end of the surgical procedure. These included: transcranial motor evoked potentials (TcMEP), somatosensory evoked potentials (SEP) and free running electromyography (EMG) recordings. Sensitivity, specificity, positive predictive value (PPV) and negative predictive value (PNV) were calculated. Results: IONM warnings were given in 5 cases during neck positioning. These consisted of the disappearance of TcMEP in all the cases, while two cases showed a loss of SEPs as well. Four of these patients presented a complete recovery of TcMEP and SEPs after neck repositioning. The patient in which this recovery was not present, woke up with new postoperative neurological deficits. Sensitivity, specificity, PPV and NPV of TcMEP during cervical positioning were all 100%. Sensitivity of SEPs was 40%; specificity and PPV were 100%; and the NPV of SEPs was 95.9%. Conclusion: Multimodal IONM is a useful method to prevent spinal cord injury during neck positioning in cervical spine surgical procedures. TcMEPs showed the highest sensitivity in detecting injuries to cervical spine related to neck positioning. Significance: Multimodal IONM should not only be considered for detecting intra-operative warnings, but also during positioning. Ó 2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Intraoperative neurophysiological monitoring (IONM) is not used as a routine in spine surgery in many centers, although it is ⇑ Corresponding author at: Hospital Universitario de Canarias (Neuroscience department), Calle Ofra s/n La Cuesta, CP 38320 La Laguna, S/C de Tenerife, Spain. Tel.: +34 922 255 544/646 625 973. E-mail address: [email protected] (J. Plata Bello).
a standard of care in scoliosis procedures (Tomé-Bermejo et al., 2014). Indeed, irreversible changes during IONM are predictive of severe adverse neurological outcomes (level of evidence class A) (Nuwer et al., 2012) which is why it is becoming more popular in cervical spine procedures because it seems to be producing better functional results (Li et al., 2012; Clark et al., 2013). Certain studies point out that the combination of somatosensory evoked potentials (SEPs) and motor evoked potentials (MEPs)
http://dx.doi.org/10.1016/j.clinph.2014.09.020 1388-2457/Ó 2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
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in IONM is more effective than the use of only one of these methods for the detection of neurological injury during the surgical procedure (Pelosi et al., 2002; Costa et al., 2007; Sutter et al., 2007; Clark et al., 2013). However, neurological injury may not only appear during the surgical procedure itself, but can also occur during neck or arm positioning before surgery (Bose et al., 2004; Jahangiri et al., 2011). Therefore, IONM should be considered during this early stage of the surgical approach to prevent neurological injury that may turn out to cause new motor and/or sensory clinical deficits and consequently a worse functional outcome. To the best of our knowledge, apart from some case reports, no research has focused on this issue. The aim of the present study is to evaluate the use of SEPs and MEPs in detecting injury to the nervous system during neck and/or arm positioning for anterior and posterior cervical spine procedures. 2. Materials and methods 2.1. Patients Seventy-five consecutive patients (22 female; mean age of 60.15, SD = 15.1) who were undergoing cervical spine surgery from January to September 2013 were recruited for the study. Table 1 summarizes the diagnoses of this patient cohort and Table 2 indicates the cervical levels that were approached. IONM was performed in all patients and consisted of SEPs, MEPs and EMG recordings during the whole surgical procedure, from positioning to re-positioning in bed after surgery. 2.2. Anesthesia Midazolam was used for sedation and total intravenous anesthesia (TIVA) was used in all patients (Valverde Junguito et al., 2007). Induction was done with propofol 3 mcg/kg, remifentanil 0.15–0.25 mcg/kg. After induction, intravenous rocuronium 30 mg was only administered for intubation purposes. No further doses of neuromuscular blocking agents were used after that. Anesthesia was maintained by infusion with propofol (range, from 2 to 3 mcg/L) and remifentanil (0.5 mcg/kg/min). Before positioning, gamma-cyclodextrin (sugammadexÒ) 4–8 mg/kg was administered to reverse neuromuscular blockade and to prevent any interference in the motor evoked muscle responses (Reid et al., 2011). No inhalational agents were ever used for induction or during the surgical procedure. 2.3. IONM recording All procedures were recorded by the same clinical neurophysiologist and intraoperative neurophysiologic monitoring device (Cadwell Cascade, Cadwell Labs, USA) and followed the standard procedure setup (Valverde Junguito et al., 2007). 2.3.1. Somatosensory evoked potentials (SEPs) A pair of stimulating surface electrodes (AmbuÒ Neuroline 72015-K) was applied on the posterior tibial nerve at the ankle
Table 1 Primary indications for surgery.
Table 2 Cervical levels approached. Level Single level
Multilevel
No. of cases C1–C2 C2–C3 C3–C4 C4–C5 C5–C6 C6–C7
0 1 6 11 17 18 22
and median nerve at the wrist bilaterally. An electrical pulse stimulation of 30 mA, 5.1 Hz frequency, 0.2 ms duration was used. Subdermal corkscrew electrodes (AmbuÒ Subdermal Corkscrew) were used to record SEPs from the scalp. The SEPs were recorded at C3, C4, Cz and Fpz (10–20 International System) with derivations including C3–Cz, C4–Cz, C3–C4, Cz–Fz and peripheral responses, using a bandpass of 1–300 Hz. Warning criteria were defined as a 50% decrease in amplitude or a 10% increase in latency uni- or bilaterally. 2.3.2. Transcranial motor evoked potentials (TcMEPs) Stimulation was performed using a multipulse technique based on a train of 7 pulses with an interstimulus interval (ISI) of 4 ms, pulse width of 50 ls, and an intensity between 240 and 400 V, delivered at C1–C2 by corkscrew electrodes (TCS Stimulator, Cadwell Labs, USA). Muscle MEPs were recorded by paired subdermal needle electrodes from the first dorsal interosseus (FDI) in the upper limbs and tibialis anterior (TA) and abductor hallucis (AH) in the lower limbs. Band pass was 10–1500 Hz. An 80% decrease in amplitude or a 10% increase in latency unilaterally or bilaterally or an increase of 100 V stimulation intensity were used to detect the MEPs over the basal threshold as warning criteria. 2.3.3. Free-running electromyography (EMG) A continuous intraoperative free running EMG was recorded from the upper limbs over both deltoids and biceps to detect C5– C6 radiculopathy using twisted paired stainless-steel subdermal needle electrodes (AmbuÒ 12 0.40 mm). 2.4. Statistical analysis Sensitivity and specificity, as well as positive and negative predictive values were calculated. A true positive was defined as the presence of irreversible SEP and/or TcMEP warnings during positioning or during the surgical procedure followed by neurological deficits in the postoperative period. On the other hand, a true negative was defined as the absence of monitoring alerts or the recovery of the potentials after re-positioning and absence of new neurological deficits after surgery. A false positive was defined as the presence of SEP and/or TcMEP warnings during positioning or during the surgical procedure that was not followed by neurological deficits in the postoperative period. A false negative was defined as the absence of warnings during IONM or recovery of SEPs or MEPs after re-positioning but the presence of new neurological deficits after surgery. All analyses were performed on the data using SPSS 18.0 (SPSS Inc., Chicago). 3. Results
Diagnosis
%
Degenerative myelopathy Disc herniation Fracture/luxation Tumour
50.7 24.0 22.7 2.7
Out of seventy-five patients, thirty-nine patients (52%) underwent cervical spinal surgery using an anterior approach while the rest were operated on using a posterior approach. Twelve patients (16%) presented altered TcMEP and SEP recordings at
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baseline which were clinically compatible to their neurological exam. A warning based on IONM was issued in 5 cases during positioning. All of them presented a sudden complete loss of TcMEP during neck positioning. Additionally, two of those patients also presented a loss of SEPs. In other words, three cases presented only TcMEP warning while the other two had both TcMEP and SEP warning, in spite of increasing the stimulation intensity over 100 V. Secondary causes of potential loss were ruled out (e.g. low blood pressure or any anesthesia interference) in every case. Four of the five patients mentioned above, showed a recovery to their baseline evoked potentials after re-positioning of the neck and none of them presented neurological deficits after the surgical procedure (Table 3; Fig. 1a). This recovery was progressive after repositioning and the time they reached their baseline was variable. In any case, it was always completely recovered before the end of the surgery and the onset of the recovery was clearly related with the change of posture. However, the other patient did not recover to baseline in spite of re-positioning and increasing the patient´s blood pressure. The surgeon rejected making a wake-up test and, eventually, an urgent anterior decompression was performed without any improvement in evoked potentials during the surgery (Table 3; Figs. 1b and 2). The patient suffered postsurgical tetraparesia but finally completely recovered after 2 weeks of rehabilitation. Only three patients had IONM warnings during the surgical procedure, and all three of them presented motor and sensory deficits after the procedure (true positives) (Table 4). The rest of the patients, including those who presented IONM warnings during positioning and recovered basal responses, did not present new postoperative neurological deficits (true negatives). No false negatives or false positives were documented. In such patients, brachial plexus injury was ruled out by demonstrating the presence of variations in TcMEPs and/or SEPs in upper limbs, with normal recordings in lower limbs. The three true positive patients that presented IONM warnings during the surgical procedure had different outcomes to each other. Two of them recovered completely after rehabilitation over 3–6 months. However, the other one presents important disability and mobility restriction. No further discussion of these data is made because it is beyond the scope of the present research. Finally, none of the patients presented warnings on free EMG recording and no cases of postoperative radiculopathy were observed. In the series presented here, the use of TcMEPs during neck positioning presented 100% sensitivity and specificity while SEPs had 40% sensitivity and 100% specificity, with a negative predictive value (NPV) of 95.9%. On the other hand, the use of both TcMEPs and SEPs for monitoring the surgical procedure presented positive and negative predictive values of 100% (Table 4).
4. Discussion The present observational study has focused on the role of IONM during neck positioning in severe cervical myelopathic patients. The main finding was the observation of a complete loss of TcMEPs in 5 cases and its reappearance in four cases after repositioning. In the other case, irreversible TcMEP loss correlated with a new postoperative neurological deficit in accordance with previous studies (Nuwer et al., 2012). One of the most important clinical implications of this study is the potential utility of this technique in predicting and avoiding spinal cord injury provoked by an inadequate surgical position. Mechanical injury to the spinal cord is most likely a result of neck manipulation during patient positioning for the surgical procedure. This stage includes intubation, neck positioning and downward traction of the shoulders. Considering the potential risk of injury that these manoeuvres may imply, perioperative monitoring is still necessary to prevent new life-changing neurological deficits. During the anesthetic procedure, fiberoptic intubation may be requested in selected cases of cervical spinal cord surgeries, especially in cases where radiculopathy or significant instability of the cervical spine is present (Fessler and Sekhar, 2006). Moreover, Malcharek et al. (2012) have proposed the performance of awake fiberoptic intubation and self-positioning to achieve continuous preoperative neurological monitoring (Malcharek et al., 2012). However, this technique may not be suitable for all kinds of patients, in this respect, neurophysiological monitoring could acquire a relevant role during this pre-surgical step. However, intubation is not the most harmful procedure for the cervical spinal cord. The positioning of the neck is probably the most relevant factor that may induce damage at this level. Anterior and posterior cervical approaches require different positions of the neck. A neutral position of the neck is necessary in anterior approaches, although a slight cervical extension is sometimes used. On the other hand, posterior approaches tend to place the cervical spine in a slight flexion, usually aided by a head holder three point skull fixation system (Stevens et al., 1997). Bearing this in mind, the diameters of the cervical canal may be reduced significantly (flexion and extension) and lead to a possible injury to the spinal cord in patients with previous cervical spine pathology. In this sense, Morishita et al. (2013) identified a deterioration of SEPs in cervical spondylotic myelopathy patients during extension of the neck in positioning steps (Morishita et al., 2013) and other authors have also described similar findings (Kraus and Christophis, 1994; Haavik-Taylor and Murphy, 2007; Insola et al., 2010). A prolongation of central motor conduction time by neck extension in compressive cervical myelopathy has also been reported (Heidegger and Ziemann, 2011). Therefore, the dynamics of the cervical spine or the presence of instabilities may lead to spinal cord injury and, consequently, to neurological deficits.
Table 3 Features of the five patients who presented IONM alerts during positioning. Gender
Age
Diagnosis
Approach
Warning
Outcome
Patient 1
Male
50
Degenerative myelopathy
Anterior
Loss of MEPs in both AH and TA. Loss of cortical SEPs
Recovery after neck reposition. No deficit
Patient 2
Male
77
Degenerative myelopathy
Posterior
Loss of right TA and AH MEPs
Recovery after repositioning of the arms. No deficit
Patient 3
Male
50
Disc herniation
Anterior
Loss of both FDI, right TA and right AH. Loss of cortical SEPs
No recovery. Postsurgical deficit
Patient 4
Male
69
Degenerative myelopathy
Posterior
Loss of right FDI and both TA
Recovery after neck reposition. No deficit
Patient 5
Male
47
C5-C6 luxation
Posterior
Loss of MEPs in both AH and TA
Recovery after neck reposition. No deficit
AH: Abducens Hallucis; FDI: First Dorsal Interosseus; TA: Tibial Anterior.
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Fig. 1. Examples of IONM alerts during neck positioning. (A) IONM screenshot showing the loss of MEPs with normal SEPs during neck positioning and their reappearance after posture correction (Patient 4). A loss of right FDI and both TA are present after positioning and they are recovered after a modification in the posture. The signal return to the baseline before the end of the surgery (data not shown); (B) IONM screenshot showing the irreversible loss of MEPs and SEPs during neck positioning (Patient 3). A loss of bilateral FDI, right TA and right AH are presented in the TcMEPs (superior panel). The SEPs are of poor quality (inferior panels), but they show a loss without recovery of left median SEPs. The attempts of repositioning are not indicated because they were multiple and no change in the monitoring with any posture was observed after maintaining each posture for at least 3 min. Abbreviations: AbdH: Abducens Hallucis; FDI: First Dorsal Interosseus; TA: Tibial Anterior.
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Fig. 2. Pre-surgical Magnetic Resonance Imaging (MRI) of the patient who did not recover either TcMEPs or SEPs after neck repositioning. (A) Sagital T2 weighted image of the cervical spine, showing a C5–C6 disc herniation with caudal migration and compression of the spinal cord. (B) Axial T2 weighted image showing the intense spinal cord compression produced by the disc herniation. The patient was rapidly operated on, conducting an anterior decompression. He suffered a post-operative tetraparesis and he eventually recovered after two weeks of rehabilitation.
Table 4 Contingency tabulation of data from the patients presenting IONM warning. Postsurgical outcome
TcMEP warning No
Yes Permanent
Surgical warning Reversible
Deficits present 0 1 0 3 Deficits absent 67 0 4 0 The use of TcMEPs during neck positioning presented 100% sensitivity and specificity. No false positives or false negatives were detected Deficits present 0 1 0 3 Deficits absent 70 0 1 0 The use of SEPs during neck positioning presented 40% sensitivity (two patients did not present changes in SEP recordings while losses of TcMEPs were recorded) and 100% specificity. No false positives were detected
Further, another phase of positioning is arm and shoulder placement. Traction to provide adequate lateral X-ray view of lower levels of cervical spine is necessary in cervical spine procedures. When the shoulders are directed downwards, this could lead to neurological injury secondary to an elongation of the brachial plexus. In this sense, Jahangiri et al. (2011) documented a deterioration of SEPs followed by a loss of TcMEPs during draping with a spontaneous recovery shortly after removing all of the tapes (Jahangiri et al., 2011). Considering that surgical procedures for the cervical spine require specific positioning of the neck, damage to the spinal cord or nerve roots/plexus may occur. A surprising finding of the present work has been the existence of more warnings during cervical positioning than during the surgical procedure itself. This finding might be of great relevance, because positioning is a stage that is not routinely monitored and, as this work shows, it is a risky procedure that may compromise the spinal cord function. Previous works focusing on IONM during cervical spine surgery have not considered the possibility that neck positioning might be a source of postoperative neurological deficits, unrelated to the surgical procedure itself. In this sense, although multimodal IONM has been shown to have the highest sensitivity and specificity rates, some series have reported the existence of some false negatives among their cases (Eggspuehler et al., 2007; Smith et al., 2007; Sutter et al., 2007). This means that no IONM alerts occurred when
post-surgical neurological deficits existed. One of the possible explanations for these false negatives is that positioning was not adequately monitored and baseline potentials were acquired when the patient was already positioned. In these cases, spinal cord or nerve root damage could have developed during this pre-surgical step and, because of that, no objective warning sign was established. Warning signs in neurophysiological monitoring during positioning have been previously described by Bose et al. (2004) in a series of cases of anterior cervical spine surgeries with SEP monitoring. They detected three alerts related to a hyperextension of the neck and one to arm position (Bose et al., 2004). Bearing this in mind, the authors suggested that IONM provides valuable information during patient positioning before anterior cervical fusion. As was previously pointed by Anderson RC et al. in a case report (Anderson et al., 2001), the present work has shown that the IONM is also a useful technique for monitoring the positioning during posterior cervical approaches. Therefore, neck positioning is a dangerous manoeuvre that might lead to more damage to the spinal cord than even the surgery itself in certain cases. Because of this, the use of IONM seems to be suitable in this pre-surgical step. The type of monitoring to be performed during positioning could also be a matter of debate. Monitoring TcMEPs is supposed to provide earlier detection of neurological injury and is associated with greater sensitivity (Hilibrand et al., 2004). Its superiority to
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SEPs has been reported in previous works (Clark et al., 2013), and that is compatible with the findings reported here, where TcMEPs showed greater sensitivity for identifying positioning related injuries. However, certain authors still recommend the use of both modalities (Costa et al., 2007; Sutter et al., 2007). Positioning should be monitored using TcMEPs, considering the higher rates of false negatives that have been described when only using SEPs. Nevertheless, considering that true positive isolated SEP loss and preservation of TcMEP responses have been reported (ToméBermejo et al., 2014), it would seem logical to recommend the use of both modalities in combination. Moreover, something that has to be emphasized is that the changes in the TcMEP monitoring in all of the cases which presented a warning were a complete loss of response. This condition shows the presumable high sensitivity of the TcMEPs in identifying spinal cord compressions secondary to an inadequate positioning. On the other hand, the reversibility that experienced the TcMEPs in four patients after cervical realignment should also be highlighted. This IONM technique might allow not only the identification, but also the prevention of damage to the spinal cord by indicating the best cervical position. The case without reversible TcMEP recording shows the good correlation between this technique with the neurological postsurgical outcome, as has been stated previously (Nuwer et al., 2012). The higher rate of postoperative deficits (4/75 = 5.3%) than previously reported risk (Cramer et al., 2009) should also be mentioned. The possible explanation of this finding might be the severity of the operated cases. As is shown in Table 1, more than 50% of patients showed myeloptahy and more than 20% of patients presented tumors or trauma related injuries where the complexity of the surgical procedure is normally higher. Therefore, the severity of the cases presented here may be higher than other presented series and this might be the explanation of the higher frequency in post-operative deficits. On the other hand, these complex cases could benefit most by this sort of monitoring during positioning, because their positions seem to present a small margin of error. Apart from preventing the possible development of new neurological deficits, IONM has important medico-legal implications. One of the most common causes of litigation involving the cervical spine is postoperative quadriparesis/quadriplegia (Epstein, 2013). Considering that an inadequate position could lead to one of these life-changing complications, neurophysiological monitoring during neck and/or arm positioning would therefore have an important role, particularly in cases with myelopathy.
5. Conclusion Positioning during cervical procedures is a potentially damaging manoeuvre that may require an adequate neurophysiological monitoring technique in order to prevent damage to the spinal cord and consequently, the development of new postoperative neurological deficits. In this sense, the loss of TcMEPs seems to indicate any potential damaging position of the neck. This loss of TcMEPs may not be definitive, because their recovery is described after modifying the position of the neck and no neurological deficits when this occurred. In other words, the present work has shown that TcMEP loss can be reversible after repositioning and this has a good correlation with the final clinical outcome. On the other hand, although it might be biased by the complexity of the cases, more warnings in the IONM during positioning than during the surgical procedure were identified. This might underline the importance of monitoring in pre-surgical manoeuvres, mostly in severe cases.
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