J Clin Monit Comput (2015) 29:549–554 DOI 10.1007/s10877-015-9713-8
ORIGINAL RESEARCH
Trans-cranial motor evoked potential detection of femoral nerve injury in trans-psoas lateral lumbar interbody fusion Kshitij Chaudhary1 • Katharine Speights3 • Kevin McGuire1 Andrew P. White1,2
•
Received: 2 November 2014 / Accepted: 5 June 2015 / Published online: 17 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Trans-psoas lateral lumbar interbody fusion (LLIF) is frequently associated with neurological complications, limiting its value as a less invasive procedure. The routine use of EMG neuromonitoring has been inadequate to detect iatrogenic injuries; significant postoperative deficits have gone undetected by EMG. An effective way to monitor for these intraoperative neurological events is not yet well established. To our knowledge, detection of lumbar plexus injury during LLIF by trans-cranial motor evoked potentials (MEP) without corresponding change in EMG has not been reported in the literature. Three cases are presented to illustrate the potential utility of transcranial MEP monitoring during trans-psoas LLIF. We introduce a modified intraoperative neuro-monitoring (IONM) protocol for LLIF surgery, which includes MEP in addition to spontaneous and triggered EMG. Postoperative neurological outcome was correlated with the IONM findings. In each case, loss of quadriceps MEP signals occurred during LLIF at L4/L5, and after prolonged retraction (27, 25 and 61 min respectively). The EMG, however, did not show any abnormal activity. Two patients had post-operative quadriceps weakness, concordant with MEP data. The third patient, in whom the MEP signals & Kshitij Chaudhary [email protected] Andrew P. White [email protected] 1
Beth Israel Deaconess Medical Center, Department of Orthopaedic Surgery, Harvard Medical School, Boston, MA, USA
2
BIDMC Orthopaedics, 330 Brookline Ave, Stoneman 10, Boston, MA 02215, USA
3
Safe Passage Neuromonitoring, Boston, USA
returned to normal after expeditious removal of the retractor, did not exhibit quadriceps weakness, also concordant with MEP data. These cases contribute to the developing perception that stand-alone EMG nerve monitoring is not adequate for trans-psoas surgery. The addition of MEP may improve the sensitivity of IONM during transpsoas surgery. Multimodality IONM may offer the opportunity to intervene on evolving iatrogenic nerve injuries, and may reduce the incidence of adverse postoperative findings. Keywords Motor evoked potentials Electromyography Trans-psoas interbody fusion LLIF XLIF DLIF Lumbar plexus
1 Introduction While trans-psoas lateral lumbar interbody fusion (LLIF) has gained popularity, postoperative neurological complications have dampened enthusiasm for this potentially less invasive surgery. Unfavorable neurological symptoms are commonly observed following LLIF, particularly when operating at L4–L5. Despite normal intraoperative electromyography (EMG) findings, postoperative weakness (including thigh weakness) has been reported to be as frequent as 24 % [1–3]. Specifically, quadriceps weakness has been reported to occur in 1.7–6.7 % cases [1, 2, 4]. As such, stand-alone EMG neuromonitoring (IONM) may not be adequate. We have developed a multimodal method of neuromonitoring for trans-psoas surgery, which includes EMG and trans-cranial motor evoked potentials (MEP). This method was used in 58 patients between January 2009 and September 2011. Here we present our technique and discuss three cases from this series where MEP monitoring
123
550
demonstrated alerts while EMG monitoring was normal. Out of these three patients, two developed quadriceps weakness. The purpose of this report is to expose the inadequacy of using stand-alone EMG to detect iatrogenic nerve injury during LLIF, and to introduce a potentially helpful monitoring technique. The surgical technique has been previously described by the senior author [5]. The neuromonitoring technique requires total intravenous anesthesia (propofol and opioid) without muscle relaxants. A certified neurophysiologist performed the intra-operative neuromonitoring, remotely supervised by a neurologist. Multimodal neuromonitoring, including spontaneous EMG (sEMG), triggered EMG (tEMG), and MEP was used in all patients. Sub-dermal needle electrodes were used in seven muscles on the operative side viz. iliopsoas, adductor longus, vastus medialis, vastus lateralis, anterior tibialis, gastrocnemius, and abductor hallucis. Muscles with potentially redundant innervation were chosen to assure thorough monitoring of the lumbar plexus. Control recordings were obtained on the contralateral side in four muscles viz. vastus medialis, vastus lateralis, anterior tibialis, and gastrocnemius. In male patients, sub-dermal electrode was placed in the cremaster muscle to monitor the genitofemoral nerve. During MEP stimulation, EMG responses were evoked by pulsed train voltage stimulation using the TCS-1 Caldwell stimulator. A train of 7–9 pulses, 50 ms in duration, with an inter-pulse interval of 2–3 ms and a voltage of 250–410 V were used. The parameters, primarily voltage, were varied such that reliable baseline responses could be obtained. Prior to incision, the impedance of all electrodes was calculated to ensure proper contact. A train-of-four (TOF) was stimulated from the posterior tibial nerve and recorded in the abductor hallucis to ensure neuromuscular blockade was not present. TOF was recorded as 4/4 twitches at baseline, and was tested periodically to confirm that no muscle relaxation was present during the surgery. Spontaneous EMG monitoring was continued for the duration of the procedure after confirming that there was no spontaneous activity. tEMG was utilized to navigate through the psoas muscle, to place the retractor, and confirm the absence of nerves within the retractor. For each dilator, we started at 0 mA and progressed up to 10 mA or until we found a threshold. We used a rep rate of 4.7/s at 200lS duration. The retractor was placed only if the threshold was more than 5 mA. A ball-tipped monopolar probe at 2 mA was used to stimulate the retractor blades and the periphery of the operative field within the retractor. This was to check whether any nerves were directly in contact with the blades or within the surgical corridor. Baseline MEP data was obtained pre-incision. MEP data was collected every 5–10 min after the retractor placement.
123
J Clin Monit Comput (2015) 29:549–554
Criteria for alert were 80 % (or greater) reduction in MEP amplitude, or any EMG activity consistent with neurotonic injury.
2 Case 1 This 39-year-old man underwent a left sided L4–L5 LLIF for treatment of recurrent stenosis causing L5 radiculopathy. The preoperative lower extremity strength was normal. MEPs were elicited using 400 V. Baseline MEPs were not present in left adductor or left iliopsoas. Signals were adequate in all other muscles. Direct stimulation of dilators elicited a response in the left anterior tibialis at 9 mA. After placement of the retractor, tEMGs were quiet with ball tip at 2 mA in all areas around retractor. The left vastus medialis and lateralis MEP signals were lost 27 min after retractor placement (Fig. 1). The MEP signals in the other muscles were unaltered. No confounding cause, systemic or positional, was found. The retractor was removed 23 min after the first MEP alert. The EMG was quiet throughout the procedure. The MEP signals had not returned at the final testing after skin closure. Postoperatively, the patient demonstrated left quadriceps weakness, graded 3/5, with anterior thigh numbness. The patient underwent urgent MR imaging, demonstrating no stenosis, no epidural or psoas hematoma, and appropriate placement of the interbody device. The quadriceps strength normalized in 7 days, but anterior thigh numbness persisted for 6 months.
3 Case 2 This 31-year-old woman underwent left sided L4–L5 LLIF for recurrent L5 radiculopathy after previously undergoing two discectomies at the same level. tEMG response was quiet at 10 mA on direct stimulation of the dilators. After placement of the retractor, tEMGs were quiet with ball tip at 2 mA in all areas around the retractor. The stimulating voltage for MEP was 220 V bilaterally. The left vastus medialis, vastus lateralis and adductor MEP signals were lost 32 min after the retractor placement (Fig. 2). The MEP signals in the other monitored muscle groups were unaltered. The retractor was removed 9 min after the initial alert. sEMG was quiet throughout the procedure. The MEP signals had not returned at the final testing after the skin closure (Fig. 2). Postoperatively, the patient had left quadriceps weakness, graded 2/5. This motor deficit recovered to 4/5 in 24 h and to 5/5 in 4 days. Anterior thigh numbness persisted for 6 weeks.
J Clin Monit Comput (2015) 29:549–554 Fig. 1 The timeline of electrophysiological data in Case 1. Twenty-seven minutes after retractor placement, the left vastus medialis and vastus lateralis MEP signals were lost. The EMG was quiet throughout the procedure. The retractor was removed 23 min after the first MEP alert. The MEP did not improve, however, and the patient awoke with 3/5 quadriceps weakness
551
Incision 9:10 am
Retractor in 9:33am
Discectomy 9:46am ALERT 10:00 am Trials 10:01 am Cage in 10:17 am Retractor out 10:23 am
Closure 10:36am Extubated 10:54 am
Fig. 2 The electrophysiological data in Case 2. An MEP alert was observed 32 min following retractor placement, when the vastus medialis, vastus lateralis and adductor MEP signals were lost. sEMG was quiet, however, throughout the entire procedure. The retractor was removed 9 min after the MEP alert, but signals had not returned at the final testing, and the patient awoke with 2/5 quadriceps weakness
50 µV Quad 500 µV TA 100 µV Gas
Incision 9:01 am
Retractor in 9:23am
Discectomy 9:39am
ALERT 9:55 am Trials 9:56 am Cage in 10:03 am Retractor out 10:04 am
Closure 10:23am Extubated 10:34 am 100 µV Add 500 µV VM 2000 µV TA 1000 µV Gas
4 Case 3 This 62-year-old man underwent right-sided L4–L5 LLIF for radiculopathy in the L4 and L5 distributions. He had previously undergone right L4–L5 hemilaminotomy but
developed recurrent symptoms, with progressive disk collapse and recurrent stenosis. His preoperative lower extremity strength was normal. The MEP stimulating voltage was 220 V on the right and 260 V on the left. The direct stimulation (tEMG) of the
123
552
J Clin Monit Comput (2015) 29:549–554
dilator elicited response at 9 mA. After placement of the retractor, tEMGs were quiet with ball tip at 3 mA in all areas around retractor. The first sEMG alert was sounded 47 min after the retractor placement. sEMGs showed tonic activity in bilateral tibialis anterior and gastrocnemius. Anesthetist altered the narcotic dose as the patient was in a lighter plane. This resolved the EMG activity, and sEMG remained quiet throughout the rest of the procedure. Sixtyone minutes after the retractor placement, the MEP signals in the right vastus medialis, vastus lateralis and adductors were lost. In response, the trans-psoas retractor was removed as quickly as possible, 3 min after the MEP alert. The MEP signals returned to baseline amplitude 7 min after retractor removal (Fig. 3). Postoperatively, the patient demonstrated normal and symmetric quadriceps strength. He had anterior thigh numbness, which resolved by the 6-week follow up visit.
5 Discussion In each of these L4/L5 LLIF cases, intraoperative lumbar plexus nerve injury was detected by MEP, and not by EMG monitoring. To our knowledge, such an observation has not been reported in the literature. These cases contribute to the developing perception that stand-alone EMG nerve monitoring is not adequate for trans-psoas surgery. The incidence in our series is 3.4 % (2 out of 58), which is well within the range reported in literature [1, 2, 4]. The risk of nerve injuries is highest at L4/L5 [1]. Here, as Fig. 3 The timeline of electrophysiological data in Case 3. The MEP signals in the right vastus medialis, vastus lateralis and adductors were lost 61 min after retractor placement, while sEMG remained quiet. The retractor was removed 3 min after the MEP alert. The signals returned to baseline amplitude 7 min after retractor removal, and the patient awoke with normal quadriceps strength
compared to more cranial levels, there are more nerves within the psoas, and the nerves traverse more anteriorly [6]. As such, retraction is more likely to cause greater nerve displacement and induce more nerve tension. L4/L5 may also be associated with injuries more frequently because the psoas is larger here than it is more cranially: there is a larger volume of tissue compacted between the retractor and the transverse process, inducing more compression (Fig. 4). We believe that there are two distinct mechanisms of lumbar plexus injury during LLIF. The first is a direct mechanism where the nerve is instantaneously injured by inadvertent instrument or retractor placement. The second mechanism, however, is an indirect injury. It is related to prolonged compression of the lumbosacral nerves between the posterior retractor blade and the transverse process (Fig. 4). We attribute the nerve injuries seen in our three cases to this prolonged compression mechanism of injury; the MEP signals were significantly diminished not at the time of retractor placement, but after a period of prolonged retraction. This proposition is supported by studies that have reported higher likelihood of nerve injury with increasing surgical times [7]. Spontaneous or mechanically elicited EMG (sEMG) monitoring is highly sensitive for direct nerve injuries (first mechanism). This is because uninjured nerves will reliably depolarize when mechanically perturbed by a dilator or retractor, resulting in an EMG response. This is well illustrated by the cases reported by Cahill et al. [1]. In contrast, EMG monitoring is less sensitive to the second
Retractor in 9:36 am
Discectomy begins 10:09 am
Cage in 10:31 am
ALERT 10:37 am Retractor out 10:40 am MEPs return 10:47 am Skin Closure 10:51 am
Extubated 11:13 am 1000 µV Add 1000 µV VM 500 µV TA 1000 µV Gas
123
J Clin Monit Comput (2015) 29:549–554
Fig. 4 The lateral perspective of the anatomic structures and a transpsoas retractor, relevant to L4/L5 surgery. A significant volume of psoas muscle and traversing roots is compressed into the space between the posterior aspect of the retractor and the anterior aspect of the transverse process. Prolonged compression of the nerves here may contribute to neurological injury
(progressive compression) mechanism of injury, accounting for the common observation of false negatives with LLIF [8]. This has a neurophysiological basis; gradual and progressive compression of nerve root is unlikely to incite
553
neurotonic firing [9]. In the cases presented in this paper, we did not encounter neurotonic discharges at the time of MEP decrement. This may be the reason many reported cases of clinically significant neurologic injury following LLIF have gone undetected on EMG monitoring [2, 3]. Another potential reason for failure of the current systems to detect nerve injuries using sEMG could be the type of electrode used. Skinner et al. have shown that surface electrodes are clearly inadequate compared to subdermal electrodes. They found intramuscular electrodes superior to subdermal electrodes [10]. We did use subdermal electrodes in our study and acknowledge that this may be a potential reason for the EMG insensitivity. Triggered or electrically stimulated EMG (tEMG) is used to identify nerves within the trans-psoas surgical portal, to reduce the risk of injury by the first (direct) mechanism. Triggered EMG cannot, however, detect injuries incurred by the second (prolonged compression) mechanism. One hypothetical way of using triggered EMG to detect the second mechanism of nerve injury would be to stimulate proximal to the nerve injury and measure the nerve root stimulation threshold (NRT) that elicits a distal response. Experimentally, an increase in NRT is predictive of distal nerve injury [9]. This kind of testing is not clinically feasible in the setting of trans-psoas surgery, however, since the proximal and distal aspects of the nerve roots are not accessible to direct stimulation. Furthermore, the site of nerve stimulation could be distal to the nerve injury. The MEP alerts observed in these cases offered us an opportunity to intervene on a progressive neurological injury. We recommend that the retractor be released or removed following confirmation of an MEP alert, especially if there is a complete loss of amplitude. The opportunity to make this intervention may reduce the severity of the injury. The patient discussed in Case 3, in whom we observed a return of MEP signals after expeditiously removing the retractor may be an example of this; he awoke without a motor deficit. Several factors limit the interpretation of MEP when applied to nerve root monitoring [11]. These include; (1) Radicular overlap: multiple nerve roots innervate individual muscles. Thus, MEP recorded in a particular muscle is a function of signal conduction through multiple nerve roots. Conduction via uninjured nerve roots may mask a single nerve injury, especially if the injured nerve is nondominant. (2) Limited sampling: trans-cranial stimulation activates only a small population of alpha motor neurons. In addition, the electrodes record muscle units fire in close proximity. Due to this double sampling limitation, MEP response that is recorded in a muscle measures only 4–5 % of motor axons [12]. Moreover, each trans-cranial stimulus activates a varying population of alpha motor neurons. If
123
554
the injured nerve root has limited axons that contribute to the MEP response, then the injury can be missed. The response to a partial nerve injury also could vary depending on which axons are damaged. (3) Confounding factors: Anesthetic factors, hemodynamic factors, positional problems and many other unknown factors affect the MEP response. Contralateral and rostral control measurements may help to differentiate these from true MEP deteriorations. (4) Variability: MEP responses have an inherent measure of variability due to fluctuating excitability of alpha motor neurons. The extent of this variability differs between patients and muscles. These neurophysiological variables make it difficult to accurately define MEP alert criteria for nerve root monitoring. If the loss of amplitude criterion is increased then the specificity to detect injury increases. Disappearance or 100 % amplitude loss is an ominous sign, as was the case in all our patients. 100 % amplitude loss may indicate multiple nerve root injuries. The 80 % amplitude loss criterion, used in our cases, maximizes specificity but has potential to miss some nerve injuries. Some authors have suggested a 67 % amplitude loss criteria, to reduce the false negatives [13]. Since we do not have the neurophysiologic data on all 58 cases, it is difficult to draw conclusions regarding the efficacy of MEP over EMG in detecting nerve root injury. A larger prospective study with predetermined alert criteria can provide us with a contingency table to determine the relative efficacy of MEP over EMG. However, our case report brings to attention the potential inadequacy of standalone EMG monitoring in LLIF. Similarly, MEP monitoring in isolation is an imperfect technique for monitoring nerve roots. One should not develop a false sense of security with normal MEPs, as this does not entirely preclude a nerve root injury. However, when used together multi-modality monitoring may have the potential to improve the safety of trans-psoas surgery, particularly when operating at L4/L5. Acknowledgments We thank Katiri Wagner for her help in preparing the manuscript. No funds were received in support of this work. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Approval by the authors’ institutional review board (IRB) was obtained (Protocol#: 2012-P-000317/3;BIDMC).
123
J Clin Monit Comput (2015) 29:549–554 Conflict of interest of interest.
The authors declare that they have no conflict
References 1. Cahill KS, Martinez JL, Wang MY, Vanni S, Levi AD. Motor nerve injuries following the minimally invasive lateral transpsoas approach. J Neurosurg Spine. 2012;17:227–31. 2. Cummock MD, Vanni S, Levi AD, Yu Y, Wang MY. An analysis of postoperative thigh symptoms after minimally invasive transpsoas lumbar interbody fusion. J Neurosurg Spine. 2011; 15:11–8. 3. Sofianos DA, Brisen˜o MR, Abrams J, Patel A. Complications of the lateral transpsoas approach for lumbar interbody arthrodesis: a case series and literature review. Clin Orthop Relat Res. 2012;470:1621–32. 4. Tohmeh AG, Rodgers WB, Peterson MD. Dynamically evoked, discrete-threshold electromyography in the extreme lateral interbody fusion approach. J Neurosurg Spine. 2011;14:31–7. 5. Simpson AK, Harrod C, White AP. Lateral lumbar trans-psoas interbody fusion. Tech Orthop. 2011;26:156. 6. Moro T, Kikuchi S-I, Konno S-I, Yaginuma H. An anatomic study of the lumbar plexus with respect to retroperitoneal endoscopic surgery. Spine. 2003;28:423–8 (discussion 427–8). 7. Wang MY, Mummaneni PV. Minimally invasive surgery for thoracolumbar spinal deformity: initial clinical experience with clinical and radiographic outcomes. Neurosurg Focus. 2010;28:E9. 8. Houten JK, Alexandre LC, Nasser R, Wollowick AL. Nerve injury during the transpsoas approach for lumbar fusion. J Neurosurg Spine. 2011;15:280–4. 9. Lyon R, Lieberman JA, Feiner J, Burch S. Relative efficacy of transcranial motor evoked potentials, mechanically-elicited electromyography, and evoked EMG to assess nerve root function during sustained retraction in a porcine model. Spine. 2009;34: E558–64. 10. Skinner SA, Transfeldt EE, Savik K. Surface electrodes are not sufficient to detect neurotonic discharges: observations in a porcine model and clinical review of deltoid electromyographic monitoring using multiple electrodes. J Clin Monit Comput. 2008;22:131–9. 11. Macdonald DB, Stigsby B, Al Homoud I, Abalkhail T, Mokeem A. Utility of motor evoked potentials for intraoperative nerve root monitoring. J Clin Neurophysiol. 2012;29:118–25. 12. Leppanen RE. Intraoperative monitoring of segmental spinal nerve root function with free-run and electrically-triggered electromyography and spinal cord function with reflexes and F-responses. A position statement by the American Society of Neurophysiological Monitoring. J Clin Monit Comput. 2005; 19:437–61. 13. Lieberman JA, Lyon R, Feiner J, Hu SS, Berven SH. The efficacy of motor evoked potentials in fixed sagittal imbalance deformity correction surgery. Spine. 2008;33:E414–24.
ORIGINAL RESEARCH
Trans-cranial motor evoked potential detection of femoral nerve injury in trans-psoas lateral lumbar interbody fusion Kshitij Chaudhary1 • Katharine Speights3 • Kevin McGuire1 Andrew P. White1,2
•
Received: 2 November 2014 / Accepted: 5 June 2015 / Published online: 17 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Trans-psoas lateral lumbar interbody fusion (LLIF) is frequently associated with neurological complications, limiting its value as a less invasive procedure. The routine use of EMG neuromonitoring has been inadequate to detect iatrogenic injuries; significant postoperative deficits have gone undetected by EMG. An effective way to monitor for these intraoperative neurological events is not yet well established. To our knowledge, detection of lumbar plexus injury during LLIF by trans-cranial motor evoked potentials (MEP) without corresponding change in EMG has not been reported in the literature. Three cases are presented to illustrate the potential utility of transcranial MEP monitoring during trans-psoas LLIF. We introduce a modified intraoperative neuro-monitoring (IONM) protocol for LLIF surgery, which includes MEP in addition to spontaneous and triggered EMG. Postoperative neurological outcome was correlated with the IONM findings. In each case, loss of quadriceps MEP signals occurred during LLIF at L4/L5, and after prolonged retraction (27, 25 and 61 min respectively). The EMG, however, did not show any abnormal activity. Two patients had post-operative quadriceps weakness, concordant with MEP data. The third patient, in whom the MEP signals & Kshitij Chaudhary [email protected] Andrew P. White [email protected] 1
Beth Israel Deaconess Medical Center, Department of Orthopaedic Surgery, Harvard Medical School, Boston, MA, USA
2
BIDMC Orthopaedics, 330 Brookline Ave, Stoneman 10, Boston, MA 02215, USA
3
Safe Passage Neuromonitoring, Boston, USA
returned to normal after expeditious removal of the retractor, did not exhibit quadriceps weakness, also concordant with MEP data. These cases contribute to the developing perception that stand-alone EMG nerve monitoring is not adequate for trans-psoas surgery. The addition of MEP may improve the sensitivity of IONM during transpsoas surgery. Multimodality IONM may offer the opportunity to intervene on evolving iatrogenic nerve injuries, and may reduce the incidence of adverse postoperative findings. Keywords Motor evoked potentials Electromyography Trans-psoas interbody fusion LLIF XLIF DLIF Lumbar plexus
1 Introduction While trans-psoas lateral lumbar interbody fusion (LLIF) has gained popularity, postoperative neurological complications have dampened enthusiasm for this potentially less invasive surgery. Unfavorable neurological symptoms are commonly observed following LLIF, particularly when operating at L4–L5. Despite normal intraoperative electromyography (EMG) findings, postoperative weakness (including thigh weakness) has been reported to be as frequent as 24 % [1–3]. Specifically, quadriceps weakness has been reported to occur in 1.7–6.7 % cases [1, 2, 4]. As such, stand-alone EMG neuromonitoring (IONM) may not be adequate. We have developed a multimodal method of neuromonitoring for trans-psoas surgery, which includes EMG and trans-cranial motor evoked potentials (MEP). This method was used in 58 patients between January 2009 and September 2011. Here we present our technique and discuss three cases from this series where MEP monitoring
123
550
demonstrated alerts while EMG monitoring was normal. Out of these three patients, two developed quadriceps weakness. The purpose of this report is to expose the inadequacy of using stand-alone EMG to detect iatrogenic nerve injury during LLIF, and to introduce a potentially helpful monitoring technique. The surgical technique has been previously described by the senior author [5]. The neuromonitoring technique requires total intravenous anesthesia (propofol and opioid) without muscle relaxants. A certified neurophysiologist performed the intra-operative neuromonitoring, remotely supervised by a neurologist. Multimodal neuromonitoring, including spontaneous EMG (sEMG), triggered EMG (tEMG), and MEP was used in all patients. Sub-dermal needle electrodes were used in seven muscles on the operative side viz. iliopsoas, adductor longus, vastus medialis, vastus lateralis, anterior tibialis, gastrocnemius, and abductor hallucis. Muscles with potentially redundant innervation were chosen to assure thorough monitoring of the lumbar plexus. Control recordings were obtained on the contralateral side in four muscles viz. vastus medialis, vastus lateralis, anterior tibialis, and gastrocnemius. In male patients, sub-dermal electrode was placed in the cremaster muscle to monitor the genitofemoral nerve. During MEP stimulation, EMG responses were evoked by pulsed train voltage stimulation using the TCS-1 Caldwell stimulator. A train of 7–9 pulses, 50 ms in duration, with an inter-pulse interval of 2–3 ms and a voltage of 250–410 V were used. The parameters, primarily voltage, were varied such that reliable baseline responses could be obtained. Prior to incision, the impedance of all electrodes was calculated to ensure proper contact. A train-of-four (TOF) was stimulated from the posterior tibial nerve and recorded in the abductor hallucis to ensure neuromuscular blockade was not present. TOF was recorded as 4/4 twitches at baseline, and was tested periodically to confirm that no muscle relaxation was present during the surgery. Spontaneous EMG monitoring was continued for the duration of the procedure after confirming that there was no spontaneous activity. tEMG was utilized to navigate through the psoas muscle, to place the retractor, and confirm the absence of nerves within the retractor. For each dilator, we started at 0 mA and progressed up to 10 mA or until we found a threshold. We used a rep rate of 4.7/s at 200lS duration. The retractor was placed only if the threshold was more than 5 mA. A ball-tipped monopolar probe at 2 mA was used to stimulate the retractor blades and the periphery of the operative field within the retractor. This was to check whether any nerves were directly in contact with the blades or within the surgical corridor. Baseline MEP data was obtained pre-incision. MEP data was collected every 5–10 min after the retractor placement.
123
J Clin Monit Comput (2015) 29:549–554
Criteria for alert were 80 % (or greater) reduction in MEP amplitude, or any EMG activity consistent with neurotonic injury.
2 Case 1 This 39-year-old man underwent a left sided L4–L5 LLIF for treatment of recurrent stenosis causing L5 radiculopathy. The preoperative lower extremity strength was normal. MEPs were elicited using 400 V. Baseline MEPs were not present in left adductor or left iliopsoas. Signals were adequate in all other muscles. Direct stimulation of dilators elicited a response in the left anterior tibialis at 9 mA. After placement of the retractor, tEMGs were quiet with ball tip at 2 mA in all areas around retractor. The left vastus medialis and lateralis MEP signals were lost 27 min after retractor placement (Fig. 1). The MEP signals in the other muscles were unaltered. No confounding cause, systemic or positional, was found. The retractor was removed 23 min after the first MEP alert. The EMG was quiet throughout the procedure. The MEP signals had not returned at the final testing after skin closure. Postoperatively, the patient demonstrated left quadriceps weakness, graded 3/5, with anterior thigh numbness. The patient underwent urgent MR imaging, demonstrating no stenosis, no epidural or psoas hematoma, and appropriate placement of the interbody device. The quadriceps strength normalized in 7 days, but anterior thigh numbness persisted for 6 months.
3 Case 2 This 31-year-old woman underwent left sided L4–L5 LLIF for recurrent L5 radiculopathy after previously undergoing two discectomies at the same level. tEMG response was quiet at 10 mA on direct stimulation of the dilators. After placement of the retractor, tEMGs were quiet with ball tip at 2 mA in all areas around the retractor. The stimulating voltage for MEP was 220 V bilaterally. The left vastus medialis, vastus lateralis and adductor MEP signals were lost 32 min after the retractor placement (Fig. 2). The MEP signals in the other monitored muscle groups were unaltered. The retractor was removed 9 min after the initial alert. sEMG was quiet throughout the procedure. The MEP signals had not returned at the final testing after the skin closure (Fig. 2). Postoperatively, the patient had left quadriceps weakness, graded 2/5. This motor deficit recovered to 4/5 in 24 h and to 5/5 in 4 days. Anterior thigh numbness persisted for 6 weeks.
J Clin Monit Comput (2015) 29:549–554 Fig. 1 The timeline of electrophysiological data in Case 1. Twenty-seven minutes after retractor placement, the left vastus medialis and vastus lateralis MEP signals were lost. The EMG was quiet throughout the procedure. The retractor was removed 23 min after the first MEP alert. The MEP did not improve, however, and the patient awoke with 3/5 quadriceps weakness
551
Incision 9:10 am
Retractor in 9:33am
Discectomy 9:46am ALERT 10:00 am Trials 10:01 am Cage in 10:17 am Retractor out 10:23 am
Closure 10:36am Extubated 10:54 am
Fig. 2 The electrophysiological data in Case 2. An MEP alert was observed 32 min following retractor placement, when the vastus medialis, vastus lateralis and adductor MEP signals were lost. sEMG was quiet, however, throughout the entire procedure. The retractor was removed 9 min after the MEP alert, but signals had not returned at the final testing, and the patient awoke with 2/5 quadriceps weakness
50 µV Quad 500 µV TA 100 µV Gas
Incision 9:01 am
Retractor in 9:23am
Discectomy 9:39am
ALERT 9:55 am Trials 9:56 am Cage in 10:03 am Retractor out 10:04 am
Closure 10:23am Extubated 10:34 am 100 µV Add 500 µV VM 2000 µV TA 1000 µV Gas
4 Case 3 This 62-year-old man underwent right-sided L4–L5 LLIF for radiculopathy in the L4 and L5 distributions. He had previously undergone right L4–L5 hemilaminotomy but
developed recurrent symptoms, with progressive disk collapse and recurrent stenosis. His preoperative lower extremity strength was normal. The MEP stimulating voltage was 220 V on the right and 260 V on the left. The direct stimulation (tEMG) of the
123
552
J Clin Monit Comput (2015) 29:549–554
dilator elicited response at 9 mA. After placement of the retractor, tEMGs were quiet with ball tip at 3 mA in all areas around retractor. The first sEMG alert was sounded 47 min after the retractor placement. sEMGs showed tonic activity in bilateral tibialis anterior and gastrocnemius. Anesthetist altered the narcotic dose as the patient was in a lighter plane. This resolved the EMG activity, and sEMG remained quiet throughout the rest of the procedure. Sixtyone minutes after the retractor placement, the MEP signals in the right vastus medialis, vastus lateralis and adductors were lost. In response, the trans-psoas retractor was removed as quickly as possible, 3 min after the MEP alert. The MEP signals returned to baseline amplitude 7 min after retractor removal (Fig. 3). Postoperatively, the patient demonstrated normal and symmetric quadriceps strength. He had anterior thigh numbness, which resolved by the 6-week follow up visit.
5 Discussion In each of these L4/L5 LLIF cases, intraoperative lumbar plexus nerve injury was detected by MEP, and not by EMG monitoring. To our knowledge, such an observation has not been reported in the literature. These cases contribute to the developing perception that stand-alone EMG nerve monitoring is not adequate for trans-psoas surgery. The incidence in our series is 3.4 % (2 out of 58), which is well within the range reported in literature [1, 2, 4]. The risk of nerve injuries is highest at L4/L5 [1]. Here, as Fig. 3 The timeline of electrophysiological data in Case 3. The MEP signals in the right vastus medialis, vastus lateralis and adductors were lost 61 min after retractor placement, while sEMG remained quiet. The retractor was removed 3 min after the MEP alert. The signals returned to baseline amplitude 7 min after retractor removal, and the patient awoke with normal quadriceps strength
compared to more cranial levels, there are more nerves within the psoas, and the nerves traverse more anteriorly [6]. As such, retraction is more likely to cause greater nerve displacement and induce more nerve tension. L4/L5 may also be associated with injuries more frequently because the psoas is larger here than it is more cranially: there is a larger volume of tissue compacted between the retractor and the transverse process, inducing more compression (Fig. 4). We believe that there are two distinct mechanisms of lumbar plexus injury during LLIF. The first is a direct mechanism where the nerve is instantaneously injured by inadvertent instrument or retractor placement. The second mechanism, however, is an indirect injury. It is related to prolonged compression of the lumbosacral nerves between the posterior retractor blade and the transverse process (Fig. 4). We attribute the nerve injuries seen in our three cases to this prolonged compression mechanism of injury; the MEP signals were significantly diminished not at the time of retractor placement, but after a period of prolonged retraction. This proposition is supported by studies that have reported higher likelihood of nerve injury with increasing surgical times [7]. Spontaneous or mechanically elicited EMG (sEMG) monitoring is highly sensitive for direct nerve injuries (first mechanism). This is because uninjured nerves will reliably depolarize when mechanically perturbed by a dilator or retractor, resulting in an EMG response. This is well illustrated by the cases reported by Cahill et al. [1]. In contrast, EMG monitoring is less sensitive to the second
Retractor in 9:36 am
Discectomy begins 10:09 am
Cage in 10:31 am
ALERT 10:37 am Retractor out 10:40 am MEPs return 10:47 am Skin Closure 10:51 am
Extubated 11:13 am 1000 µV Add 1000 µV VM 500 µV TA 1000 µV Gas
123
J Clin Monit Comput (2015) 29:549–554
Fig. 4 The lateral perspective of the anatomic structures and a transpsoas retractor, relevant to L4/L5 surgery. A significant volume of psoas muscle and traversing roots is compressed into the space between the posterior aspect of the retractor and the anterior aspect of the transverse process. Prolonged compression of the nerves here may contribute to neurological injury
(progressive compression) mechanism of injury, accounting for the common observation of false negatives with LLIF [8]. This has a neurophysiological basis; gradual and progressive compression of nerve root is unlikely to incite
553
neurotonic firing [9]. In the cases presented in this paper, we did not encounter neurotonic discharges at the time of MEP decrement. This may be the reason many reported cases of clinically significant neurologic injury following LLIF have gone undetected on EMG monitoring [2, 3]. Another potential reason for failure of the current systems to detect nerve injuries using sEMG could be the type of electrode used. Skinner et al. have shown that surface electrodes are clearly inadequate compared to subdermal electrodes. They found intramuscular electrodes superior to subdermal electrodes [10]. We did use subdermal electrodes in our study and acknowledge that this may be a potential reason for the EMG insensitivity. Triggered or electrically stimulated EMG (tEMG) is used to identify nerves within the trans-psoas surgical portal, to reduce the risk of injury by the first (direct) mechanism. Triggered EMG cannot, however, detect injuries incurred by the second (prolonged compression) mechanism. One hypothetical way of using triggered EMG to detect the second mechanism of nerve injury would be to stimulate proximal to the nerve injury and measure the nerve root stimulation threshold (NRT) that elicits a distal response. Experimentally, an increase in NRT is predictive of distal nerve injury [9]. This kind of testing is not clinically feasible in the setting of trans-psoas surgery, however, since the proximal and distal aspects of the nerve roots are not accessible to direct stimulation. Furthermore, the site of nerve stimulation could be distal to the nerve injury. The MEP alerts observed in these cases offered us an opportunity to intervene on a progressive neurological injury. We recommend that the retractor be released or removed following confirmation of an MEP alert, especially if there is a complete loss of amplitude. The opportunity to make this intervention may reduce the severity of the injury. The patient discussed in Case 3, in whom we observed a return of MEP signals after expeditiously removing the retractor may be an example of this; he awoke without a motor deficit. Several factors limit the interpretation of MEP when applied to nerve root monitoring [11]. These include; (1) Radicular overlap: multiple nerve roots innervate individual muscles. Thus, MEP recorded in a particular muscle is a function of signal conduction through multiple nerve roots. Conduction via uninjured nerve roots may mask a single nerve injury, especially if the injured nerve is nondominant. (2) Limited sampling: trans-cranial stimulation activates only a small population of alpha motor neurons. In addition, the electrodes record muscle units fire in close proximity. Due to this double sampling limitation, MEP response that is recorded in a muscle measures only 4–5 % of motor axons [12]. Moreover, each trans-cranial stimulus activates a varying population of alpha motor neurons. If
123
554
the injured nerve root has limited axons that contribute to the MEP response, then the injury can be missed. The response to a partial nerve injury also could vary depending on which axons are damaged. (3) Confounding factors: Anesthetic factors, hemodynamic factors, positional problems and many other unknown factors affect the MEP response. Contralateral and rostral control measurements may help to differentiate these from true MEP deteriorations. (4) Variability: MEP responses have an inherent measure of variability due to fluctuating excitability of alpha motor neurons. The extent of this variability differs between patients and muscles. These neurophysiological variables make it difficult to accurately define MEP alert criteria for nerve root monitoring. If the loss of amplitude criterion is increased then the specificity to detect injury increases. Disappearance or 100 % amplitude loss is an ominous sign, as was the case in all our patients. 100 % amplitude loss may indicate multiple nerve root injuries. The 80 % amplitude loss criterion, used in our cases, maximizes specificity but has potential to miss some nerve injuries. Some authors have suggested a 67 % amplitude loss criteria, to reduce the false negatives [13]. Since we do not have the neurophysiologic data on all 58 cases, it is difficult to draw conclusions regarding the efficacy of MEP over EMG in detecting nerve root injury. A larger prospective study with predetermined alert criteria can provide us with a contingency table to determine the relative efficacy of MEP over EMG. However, our case report brings to attention the potential inadequacy of standalone EMG monitoring in LLIF. Similarly, MEP monitoring in isolation is an imperfect technique for monitoring nerve roots. One should not develop a false sense of security with normal MEPs, as this does not entirely preclude a nerve root injury. However, when used together multi-modality monitoring may have the potential to improve the safety of trans-psoas surgery, particularly when operating at L4/L5. Acknowledgments We thank Katiri Wagner for her help in preparing the manuscript. No funds were received in support of this work. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Approval by the authors’ institutional review board (IRB) was obtained (Protocol#: 2012-P-000317/3;BIDMC).
123
J Clin Monit Comput (2015) 29:549–554 Conflict of interest of interest.
The authors declare that they have no conflict
References 1. Cahill KS, Martinez JL, Wang MY, Vanni S, Levi AD. Motor nerve injuries following the minimally invasive lateral transpsoas approach. J Neurosurg Spine. 2012;17:227–31. 2. Cummock MD, Vanni S, Levi AD, Yu Y, Wang MY. An analysis of postoperative thigh symptoms after minimally invasive transpsoas lumbar interbody fusion. J Neurosurg Spine. 2011; 15:11–8. 3. Sofianos DA, Brisen˜o MR, Abrams J, Patel A. Complications of the lateral transpsoas approach for lumbar interbody arthrodesis: a case series and literature review. Clin Orthop Relat Res. 2012;470:1621–32. 4. Tohmeh AG, Rodgers WB, Peterson MD. Dynamically evoked, discrete-threshold electromyography in the extreme lateral interbody fusion approach. J Neurosurg Spine. 2011;14:31–7. 5. Simpson AK, Harrod C, White AP. Lateral lumbar trans-psoas interbody fusion. Tech Orthop. 2011;26:156. 6. Moro T, Kikuchi S-I, Konno S-I, Yaginuma H. An anatomic study of the lumbar plexus with respect to retroperitoneal endoscopic surgery. Spine. 2003;28:423–8 (discussion 427–8). 7. Wang MY, Mummaneni PV. Minimally invasive surgery for thoracolumbar spinal deformity: initial clinical experience with clinical and radiographic outcomes. Neurosurg Focus. 2010;28:E9. 8. Houten JK, Alexandre LC, Nasser R, Wollowick AL. Nerve injury during the transpsoas approach for lumbar fusion. J Neurosurg Spine. 2011;15:280–4. 9. Lyon R, Lieberman JA, Feiner J, Burch S. Relative efficacy of transcranial motor evoked potentials, mechanically-elicited electromyography, and evoked EMG to assess nerve root function during sustained retraction in a porcine model. Spine. 2009;34: E558–64. 10. Skinner SA, Transfeldt EE, Savik K. Surface electrodes are not sufficient to detect neurotonic discharges: observations in a porcine model and clinical review of deltoid electromyographic monitoring using multiple electrodes. J Clin Monit Comput. 2008;22:131–9. 11. Macdonald DB, Stigsby B, Al Homoud I, Abalkhail T, Mokeem A. Utility of motor evoked potentials for intraoperative nerve root monitoring. J Clin Neurophysiol. 2012;29:118–25. 12. Leppanen RE. Intraoperative monitoring of segmental spinal nerve root function with free-run and electrically-triggered electromyography and spinal cord function with reflexes and F-responses. A position statement by the American Society of Neurophysiological Monitoring. J Clin Monit Comput. 2005; 19:437–61. 13. Lieberman JA, Lyon R, Feiner J, Hu SS, Berven SH. The efficacy of motor evoked potentials in fixed sagittal imbalance deformity correction surgery. Spine. 2008;33:E414–24.
