The foundation of the evaluation of a patient who. Heuristic map of myotomal innervation in humans using direct intraoperative nerve root stimulation

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1 J Neurosurg Spine 15:64 70, 2011 Heuristic map of myotomal innervation in humans using direct intraoperative nerve root stimulation Clinical article Clemens M. Schirmer, M.D., 1,2 Jay L. Shils, Ph.D., 3 Jeffrey E. Arle, M.D., 3 Ph.D., G. Rees Cosgrove, M.D., 3 Peter K. Dempsey, M.D., 3 Edward Tarlov, M.D., 3 Stephan Kim, M.D., 3 Christopher J. Martin, B.S., 4 Carl Feltz, Au.D., 4 Marina Moul, B.S., 4 and Subu Magge, M.D. 3 1 Division of Neurosurgery, Baystate Medical Center, Springfield; 2 Tufts University School of Medicine, Boston; 3 Department of Neurosurgery, Lahey Clinic, Burlington, Massachusetts; and 4 Impulse Monitoring, Columbia, Maryland Object. Considerable overlap exists in nerve root innervation of various muscles. Knowledge of myotomal innervation is essential for the interpretation of neurological examination findings and neurosurgical decision-making. Previous studies relied on cadaveric dissections, animal studies, and cases with anomalous anatomy. This study investigates the myotomal innervation patterns of cervical and lumbar nerve roots through in vivo stimulation during surgeries for spinal decompression. Methods. Patients undergoing cervical and lumbar surgeries in which nerve roots were exposed in the normal course of surgery were included in the study. Electromyography electrodes were placed in the muscle groups that are generally accepted to be innervated by the roots under study. These locations included levels above and below the spinal levels undergoing decompression. After decompression, a unipolar neural stimulator probe was placed directly on the nerve root sleeve and constant current stimulation in increments of 0.1 ma was performed. Current was raised until at least a 100 mv amplitude triggered electromyographic response was noted in 1 or more muscles. All muscles that responded were recorded. Results. A total of 2295 nerve root locations in 129 patients (mean age 57 ± 15 years, 47 female [36%]) were stimulated, and 1589 stimulations met quality criteria and were analyzed. Four hundred ninety-five stimulations were performed on roots contributing to the cervical and brachial plexus from C-3 to T-1 (31.2%), and 1094 (68.8%) were roots in the lumbosacral plexus between L-1 and S-2. The authors were able to construct a statistical map of the contributions of each cervical and lumbosacral nerve root for the set of muscle groups monitored in the protocol. In many cases the range of muscles innervated by a specific root was broader than previously described in textbooks. Conclusions. This is the largest data set of direct intraoperative nerve root stimulations during decompressive surgery, demonstrating the relative contribution of root-level motor input to various muscle groups. Compared with classic neuroanatomy, a significant number of roots innervate a broader range of muscles than expected, which may account for the variability of presentation between patients with identical number and location of compressed roots. (DOI: / SPINE1068) Key Words innervation nerve root myotome neuroanatomy peripheral nerve Abbreviation used in this paper: EMG = electromyography. The foundation of the evaluation of a patient who presents with radicular pain, sensory symptoms, or weakness is the correlation of the clinical findings with the pathological findings that may be observed on imaging studies. The clinician commonly uses knowledge of dermatomal and myotomal innervation patterns to assess whether an intervention is warranted. Imaging and intraoperative findings do not always correlate with the abnormalities noted on clinical examination. 5,8,10,12,17 Sensory and motor abnormalities are localized to specific spinal nerve roots based on historical data from observational studies and animal studies. 64 J Neurosurg: Spine / Volume 15 / July 2011

2 Human myotomal maps from direct root stimulation The currently accepted and established segmental innervation patterns of spinal nerve roots and the resulting dermatomal and myotomal maps are largely based on historical studies from human clinical observations and experimental animal studies. 1 3,11,14 16,18 Data presented by Dykes and Terzis 2 demonstrated significant overlap of myotomal innervation using root stimulation and muscle EMG. Others also demonstrated significant overlap in human innervations during EMG studies. 9,16 In 1892, Sherrington 14 described a dermatomal pattern of segmental innervation based on experimental data derived from selective dorsal root sections performed on Rhesus monkeys. The information from these experiments led to the creation of a map that is used to this day by clinicians to link peripheral pain with a corresponding spinal cord and root level. The map features a significant amount of overlap of the individual dermatomes. The first human map of segmental dermatomal innervation was created by Head and Campbell 4 in 1900 based on indirect information derived from an analysis of the pattern of pain and the cutaneous lesions of patients suffering from herpes zoster; they found little overlap of the dermatomes. Foerster 3 completed the map of dermatomes in the lower extremities of human patients using Sherrington s method. Sharrard 13 studied 142 patients with poliomyelitis to deduce a similar map of motor innervation. However, to date no study of significant size has examined direct root-to-muscle stimulation in humans. The feasibility of such a study in humans has been difficult due to the need to expose the specified spinal roots to conduct the mapping. This study takes advantage of spinal roots exposed during decompressive spinal surgery to study the myotomal innervation patterns of cervical and lumbar nerve roots through in vivo stimulation. Methods Study Population All patients undergoing cervical and lumbar surgeries at our institution, in whom nerve roots were exposed in the normal course of surgery and intraoperative monitoring was requested by the surgeon, were potentially included in the study. Table 1 lists the inclusion and exclusion criteria. Separate informed consent was obtained from the patients before the procedure. The study protocol was reviewed and approved by the Lahey Clinic institutional review board. Intraoperative Monitoring Methodology Standard intraoperative monitoring methodologies were used in this study. These tests included free-running EMG and triggered EMG with compound muscle action potential recordings, and somatosensory evoked potentials and motor evoked potentials recorded in cervical surgeries (the standard protocol at our institution). Electromyography electrodes were placed in the muscle groups that are generally accepted to be innervated by the roots under study. Table 2 lists the muscles commonly studied in the patients who were enrolled in this study. All recordings and stimulation were performed with a Cadwell Cascade intraoperative monitoring system (Cadwell Inc.) Triggered EMG responses of the exposed spinal roots were performed after surgical decompression was completed. A unipolar Prass neural stimulator (Medtronic Inc.) was used to stimulate the axilla, midportion, and shoulder of the nerve root sleeve separately. Stimulation began at 0.0 ma and was raised in 0.1 ma increments every second until a response was noted. The pulse width was 200 μsec and the stimulation repetition rate was 2.48 Hz. Once a response was noted, the stimulation was continued for at least 5 seconds to ensure a repeatable response. This was noted as the threshold response of that portion of the nerve root. Stability was defined by at least a 100 mv amplitude triggered EMG response in 1 or more muscles. The root, stimulation threshold amplitude, and activated muscle or muscles were recorded prospectively in a database. To investigate the potential for excess current spread, the stimulation amplitude was raised 1 ma above the threshold level. If all the muscles on a particular side activated, or all muscles that are standardly defined for the roots above and below the study level activated, then these data were removed because of a potential data corruption due to excessive current spread. The maximum stimulation level was 5 ma. If no response was found above this level, the root was marked as none. Short-acting paralytic agents were used for induction only (primarily succinylcholine). During the TABLE 1: Inclusion and exclusion criteria for the patients enrolled in the study Inclusion criteria cervical or lumbar spinal procedure w/ the surgeon requesting intraop neurophysiological monitoring participant must be 18 yrs of age or 85 yrs of age participant, or legally authorized representative, has been informed of the nature of the study & has provided written informed consent, approved by the Lahey Clinic institutional review board Preop exclusion criteria peripheral neuropathy diabetes neuromuscular disease Intraop exclusion criteria need for muscle relaxants after patient has been intubated for op myopathy that interferes w/ recordings J Neurosurg: Spine / Volume 15 / July

3 C. M. Schirmer et al. TABLE 2: Standard set of muscles monitored in this study upper-extremity muscles trapezius deltoid biceps brachii triceps brachii flexor carpi radialis flexor carpi ulnaris extensor digitorum communis extensor carpi ulnaris abductor pollicis brevis abductor digiti minimi first dorsal interosseous lower-extremity muscles iliopsoas adductor longus quadriceps biceps femoris tibialis anterior gastrocnemius abductor hallucis remaining portion of each case, general anesthesia was achieved through total intravenous anesthesia that included propofol with a narcotic. The total intravenous anesthetic regimen using propofol and either fentanyl or remifentanil with volatile inhalational agents administered only during intubation is standard protocol at our institution. Muscle relaxants (succinylcholine or rocuronium) are used only at intubation while root testing takes place a minimum of 1 hour after administration of the muscle relaxant. To ensure that all muscle relaxants have worn off, a train-of-4 test is performed by stimulating the left median nerve and recording the response at the adductor pollicis brevis muscle. We require 4 full EMG responses before testing is performed. Any deviation from this protocol was one of the exclusion criteria. Because stimulation is distal to the alpha motor neuron, the neuromuscular junction is the only area at which anesthetics can have any major effect on the response. Thus, it is critical that all muscle relaxants are out of the system and the reason for the extremely stringent criteria of a complete 4-of-4 response. Results A total of 2295 stimulation locations on nerve roots in 129 patients (mean age 57 ± 15 years, 47 female [36%]) were studied between June 2005 and February Of these 2295 stimulation locations, 1971 stimulations (85.9%) met quality criteria and represented acceptable stimulations performed after decompression of the nerve root. Three hundred eighty-two responses were recorded with stimulation above the 5-mA threshold and were not considered in the analysis, leaving a total of 1589 responses that were analyzed. Four hundred ninety-five stimulations (31.2%) were performed on roots contributing to the cervical and brachial plexus from C-3 to T-1. One thousand ninety-four roots (68.8%) were in the lumbosacral plexus between L-1 and S-2. One hundred thirty procedures were performed in total. Fifty-seven (44%) of the 129 patients underwent a procedure on the cervical spine, while 73 (56%) involved the lumbar spine. Ninety-one patients (70%) presented with symptoms of cervical or lumbar stenosis without radiculopathy and underwent decompression. Thirty-nine patients (30%) suffered from a herniated disc or focal stenosis leading to radiculopathy. The majority of surgeries were performed via a posterior approach, while 5 procedures (3.8%, all in the cervical spine) were performed via an anterior approach. In the cervical spine 22 procedures (16.9%) addressed spinal stenosis, while 33 (25.3%) addressed herniated discs by decompression. One cervical procedure addressed instability and one procedure uncovered nerve roots during decompression for an Arnold-Chiari malformation Type I (2 cases, 1.5%). In the lumbar spine 46 surgical procedures (35.4%) were performed for lumbar stenosis, 16 (12.3%) for a herniated disc, 9 (6.9%) for lumbar instability, and 2 cases (1.5%) for recurrent disc problems requiring fusion. Decompression alone was performed in 81 cases (62.3%), and posterior decompression and discectomy in 32 cases (24.6%). A fusion was performed after decompression in the lumbar spine in 12 cases (9.2%). The stimulation threshold was measured on 3 points along the nerve root sleeve: the shoulder, midpoint, and axilla. With the exception of the C-3, C-5, and L-1 roots, the lowest stimulation threshold was found by stimulating the axilla of the nerve root sleeve (Table 3). For both the C-3 and L-1 roots, stimulation of the shoulder of the nerve root sleeve required the least current. The lowest threshold for the C-5 root was found at the midportion of the nerve root sleeve. Table 4 shows the number of individual stimulations performed by both root level and location on the nerve root sleeve. The differences between locations for each root may be due to the variable surgical exposure permitting stimulation of different locations. Eightythree stimulations resulted in no activation of any muscle covered with EMG electrodes. Table 5 shows the relative percentage contribution of individual spinal roots in the motor responses noted in large muscles commonly affected by spinal stenosis. We found that stimulation of the C-3, C-4, and C-6 roots elicited responses in the biceps muscle more often than previously expected. The C-5 and C-6 roots contributed significantly to all muscles in the upper extremity that were monitored with the exception of the flexor carpi ulnaris, abductor pollicis brevis, and abductor digiti minimi. The C-6 root elicited responses in the latter two muscles in 0.7% and 1.3% of the cases studied. The C-7 and C-8 roots contributed significantly to all arm muscles with the exception of the trapezius, deltoid, and biceps. Stimulation of the C-7 root did show a response in the biceps in 2.8% of cases. Stimulation of the L-1 and L-2 roots revealed an almost identical group of muscle responses in the iliopsoas, adductor group, and quadriceps. The L-1 root contributed 66 J Neurosurg: Spine / Volume 15 / July 2011

4 Human myotomal maps from direct root stimulation TABLE 3: Stimulation threshold for the axilla, midpoint, and shoulder of the nerve roots* Location Average Threshold (ma) C-3 C-4 C-5 C-6 C-7 C-8 T-1 L-1 L-2 L-3 L-4 L-5 S-1 S-2 axilla middle NR NR shoulder NR * NR = none recorded. Lowest mean activation threshold for that location. more to the iliopsoas than the adductor. This relation was almost reversed for the L-2 root. The L-3 and L-4 roots showed a broad range of responses upon stimulation that encompassed all the muscles that were studied in the legs. The L-3 root contributed more to the proximal leg muscles, while stimulation of the L-4 root elicited significant responses in the quadriceps and the anterior tibialis muscles. The majority of L-5 root stimulations resulted in activation of the anterior tibialis muscle (44.5%) and L-5 also provided significant contribution to the gastrocnemius muscle (23.9%). The S-1 root showed an almost reversed pattern with 53.7% responses in the gastrocnemius and 19.5% responses in the anterior tibialis muscle. Figure 1 presents an overview of the responding muscle groups for each stimulated nerve root. A subgroup of 5 patients with specifically unilateral radicular symptoms in the cervical spine underwent anterior decompression procedures that allowed for bilateral stimulation of both the affected and the unaffected side. The activation thresholds were not significantly different between the left and right sides and independent of the location of the stimulation on the nerve root sleeve (p = 0.1). Discussion The preoperative evaluation of patients with cervical and lumbosacral radiculopathies requires a thorough clinical examination and often radiographic imaging. Whereas technological progress has made it possible to image the spine in extreme detail using such modalities as MR imaging, CT, and myelography, the clinician remains the final arbiter to link imaging findings with examination findings. In daily practice, we find that imaging and intraoperative findings do not always correlate with the abnormalities elicited by a clinical examination. 5,6,8,10,12,17 In a prospective study, Wittenberg et al. 17 concluded that there was no correlation between the imaging findings and clinical symptoms when comparing physical examination findings with the findings on MR imaging in patients with lumbar radiculopathies. In a review of 736 cervical discectomies, Henderson and coworkers 5 describe a 71.5% incidence of correlation between preoperative clinical findings (including both sensory and motor deficits) and operative findings. Dykes and Terzis 2 studied 10 African green monkeys and investigated both the dermatomal and afferent myotomal distribution of the nerve roots. After performing laminectomies from C-2 to T-6, the dermatomes were identified by separating each dorsal rootlet (starting proximally) into 1 3 active units and recording action potentials that were generated by rubbing the skin, moving a joint, squeezing a muscle, or activity from a unknown source. Myotomes were identified in a similar fashion by activating the end receptor and looking at the antidromic response at the spinal nerve. The ventral root distribution in the peripheral cervical musculature was not examined in that study and may, in fact, be different. The authors concluded that there are differences in the dermatomal and myotomal afferent distribution in the spinal roots. Previous efforts to study the innervation of the lower extremities were mainly focused on the lower lumbar and sacral roots. Thage 15 found considerable variations of the segmental innervation of the muscles innervated by the L2 S2 roots, which were stimulated during operations. Young and coworkers 18 stimulated the L-5 and S-1 nerve roots and demonstrated that most muscles have dual innervation, usually with 1 dominant nerve root. Philips and Park 11 confirmed these findings. They reported on 123 patients with cerebral palsy who underwent selective posterior rhizotomies for lower-extremity spasticity. They found that the number of nerve roots that produced a response in any given muscle was greater than expected by traditional myotome maps. A more recent study by Levin et al. 9 examined patients with radiographically defined and EMG-defined lesions undergoing decompressive surgery. They demonstrated similar variability to our findings, but did not perform a pure anatomical mapping such as the primate study by Dykes and Terzis. 2 The purpose of our study TABLE 4: Number of roots stimulated, differentiated by location of the root sleeve Location Total* C-3 C-4 C-5 C-6 C-7 C-8 T-1 L-1 L-2 L-3 L-4 L-5 S-1 S-2 axilla middle NR NR shoulder NR * Fourteen stimulations that included agonist/antagonist activations were ultimately excluded from the root-to-muscle analysis. J Neurosurg: Spine / Volume 15 / July

5 C. M. Schirmer et al. TABLE 5: Relative response of muscles per stimulated root* Muscle C-3 C-4 C-5 C-6 C-7 C-8 T-1 L-1 L-2 L-3 L-4 L-5 S-1 S-2 total trapezius deltoid biceps triceps extensor digitorum communis flexor carpi radialis flexor carpi ulnaris abductor pollicis brevis abductor digiti minimi iliopsoas adductor adductor magnus quadriceps biceps femoris gastrocnemius anterior tibialis abductor hallucis none * Values are percentages. Relative highest frequency response. Fig. 1. Overview of the contributions of the individual nerve roots stimulated to individual muscle groups studied. The muscles are color coded to reflect the rate of response. 68 J Neurosurg: Spine / Volume 15 / July 2011

6 Human myotomal maps from direct root stimulation was to perform such an anatomical map in humans. Several cadaveric studies have investigated the anatomical variations of the lumbar roots. Kikuchi et al. 8 found great variation in the arrangement of the lumbar roots with intra- and extradural anastomoses and divisions. These findings were confirmed by other reports, which noted the presence of nerve root variations in 14% 30% of the patients studied. 1,7 As shown in Table 5, we found a broad range of innervation of each individual nerve root, which in many cases exceeded the expected range of muscles to be innervated by a single nerve root. Our myotomal map is a statistical map, and thus may average over individual variabilities that may exist. Our data set represents the largest set of intraoperative nerve root stimulation recordings in patients that we are aware of to date. For most roots, the axilla stimulations had the lowest threshold. This may be due to the proximity of the rootlets in the dural root sleeve to the axillary region of the root. The lowest threshold for the C-5 root was found at the midportion of the nerve root sleeve. This may be due to the midposition of C-5 in the typical cervical lordosis and the particular trajectory the C-5 root takes from its foramen. For C-3 and L-1 nerve roots, the shoulder was the most sensitive with the lowest stimulation threshold. It must be noted that only 7 L-1 nerve roots were stimulated in this study and the finding of a lower stimulation threshold at the shoulder of the L-1 nerve root may be attributable to statistical artifact. Lastly, there is a possibility that our data set may be limited by the fact that we studied potentially pathological roots that may have been injured by spinal stenosis. One could argue that our results are altered by the possible consequence of chronic compression of neural elements and that our results may differ from the classic distributions because we are studying patients who suffer from the effects of myelopathy, radiculopathy, or a combination of the two. One limitation of our study is the lack of a control group without symptoms, but it is clear that those asymptomatic patients could not be enrolled in our study protocol. Moreover, we believe that this limitation represents a strength of our study because we are studying patients with the real problems that practicing neurosurgeons and neurologists are noting in their daily practice. There is no evidence in the literature to suggest that myelopathy would cause a rearrangement of the myotomes akin to plasticity observed in the brain after ischemic injury, which allows recovery of some function in some patients. To address this issue we analyzed a subgroup of 5 patients who presented with unilateral radiculopathy and were treated with anterior cervical decompression, which allowed for bilateral nerve root stimulation. Thus, this subgroup included matched sets of roots that consisted of 1 symptomatic root and another root unaffected by stenosis. We could not find a significant difference between the stenotic and nonstenotic sides. Due to the limited sample size of the group of patients who presented with unilateral symptoms and underwent anterior decompression and exposure of bilateral nerve roots, the probability value of 0.1 might be interpreted as a trend, which may become significant if a larger sample size could be enrolled. Due to the inherent difficulty of exposing a large number of J Neurosurg: Spine / Volume 15 / July 2011 nerve roots through an anterior approach, a study with a balanced sample size might be challenging to perform. Conclusions We present the largest data set of direct intraoperative nerve root stimulations during decompressive surgery to demonstrate the relative contribution of root-level motor input to various muscle groups. Compared with the classic neuroanatomy, a significant number of roots innervate a broader range of muscles than expected, which may account for the variability of presentation between patients with identical number and location of compressed roots. Clinicians should consider this variability when evaluating patients with cervical and lumbosacral radiculopathies. Disclosure Financial support for this study was received from the Robert E. Wise, M.D., Research and Education Institute. Author contributions to the study and manuscript preparation include the following. Conception and design: Magge, Shils, Arle, Cosgrove. Acquisition of data: Magge, Shils, Arle, Cosgrove, Dempsey, Tarlov, Kim, Martin, Feltz, Moul. Analysis and interpretation of data: Shils, Magge, Schirmer. Drafting the article: Schirmer. Critically revising the article: Magge, Schirmer, Shils. Reviewed final version of the manuscript and approved it for submission: all authors. Statistical analysis: Schirmer. Administrative/technical/ material support: Arle, Cosgrove. Study supervision: Magge. References 1. Chotigavanich C, Sawangnatra S: Anomalies of the lumbosacral nerve roots. An anatomic investigation. Clin Orthop Relat Res (278):46 50, Dykes RW, Terzis JK: Spinal nerve distributions in the upper limb: the organization of the dermatome and afferent myotome. Philos Trans R Soc Lond B Biol Sci 293: , Foerster O: The dermatomes in man. Brain 56:1 39, Head H, Campbell AW: The pathology of Herpes Zoster and its bearing on sensory localization. Brain 23: , Henderson CM, Hennessy RG, Shuey HM Jr, Shackelford EG: Posterior-lateral foraminotomy as an exclusive operative technique for cervical radiculopathy: a review of 846 consecutively operated cases. 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7 C. M. Schirmer et al. the lower limb in poliomyelitis; a clinical and pathological study. J Bone Joint Surg Br 37-B: , Sherrington CS: Notes on the arrangement of some motor fibres in the lumbosacral plexus. J Physiol (Lond) 13: , Thage O: The myotomes L2 S2 in man. Acta Neurol Scand Suppl 13: , Tsao BE, Levin KH, Bodner RA: Comparison of surgical and electrodiagnostic findings in single root lumbosacral radiculopathies. Muscle Nerve 27:60 64, Wittenberg RH, Lütke A, Longwitz D, Greskötter KH, Willburger RE, Schmidt K, et al: The correlation between magnetic resonance imaging and the operative and clinical findings after lumbar microdiscectomy. Int Orthop 22: , Young A, Getty J, Jackson A, Kirwan E, Sullivan M, Parry CW: Variations in the pattern of muscle innervation by the L5 and S1 nerve roots. Spine (Phila Pa 1976) 8: , 1983 Manuscript submitted February 1, Accepted February 28, Portions of this work were presented in oral form at the 2009 AANS/CNS Section on Disorders of the Spine and Peripheral Nerves meeting in Phoenix, Arizona, March Please include this information when citing this paper: published online April 8, 2011; DOI: / SPINE1068. Address correspondence to: Subu Magge, M.D., Department of Neurosurgery, Lahey Clinic, 41 Mall Road, Burlington, Massachusetts subu.n.magge@lahey.org. 70 J Neurosurg: Spine / Volume 15 / July 2011