Somatosensory-Evoked Potential for Spine Surgery

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Chapter 177 Somatosensory-Evoked Potential for Spine Surgery

Because degenerative spinal conditions and deformities are relatively prevalent, surgical procedures for the spine are common. Furthermore, the evolution and understanding of spinal mechanics and physiology have allowed the introduction of many newer spinal surgical techniques. Nevertheless, a small proportion, less than 0.5%, of patients may develop a persistent neurologic deficit immediately after surgery. Careful surgical techniques, including stabilization of the spine during surgery, have helped reduce this complication somewhat. However, it is apparent that a neurologic injury related to such an intervention can be disabling. For this reason, the monitoring of somatosensory-evoked potentials (SSEPs) from peripheral nerve stimulation (posterior tiblial, peroneal, or median nerves) during spinal column or spinal cord surgery is common.131

The spinal cord and nerve roots are at risk during a variety of surgical procedures performed on the spinal cord and surrounding structures. The risk varies with the underlying disease, as well as the type and location of surgery.3235 Patients with intramedullary tumors, syringomyelia, spinal arteriovenous malformation, thoracoabdominal aneurysms, and any other disorder associated with a baseline neurologic deficit are at greatest risk. The frequency of neurologic injury following scoliosis surgery, correction of congenital spinal deformities, and decompression (with and without spinal fusion) is low, but when damage to the spinal cord occurs, the resulting deficits are often severe, permanent, and devastating.3537 The detection of significant changes in the monitored-evoked potentials (MEPs) can indicate damage to the motor pathway and may permit appropriate intervention to prevent spinal cord damage.

The “wake-up test” was developed in an attempt to reduce the risk of spinal cord injury in patients undergoing scoliosis surgery. This technique rapidly became the standard against which other monitoring techniques were compared. Although helpful, the wake-up test disrupts the surgical procedure, can be performed only intermittently, and is associated with considerable risks (e.g., extubation, pulmonary embolism). Furthermore, it is not applicable to patients undergoing surgical procedures in which no period of major risk is defined, as in resections of spinal neoplasms.

In the 1970s, SSEP monitoring was developed as an alternative to the wake-up test. SSEP recordings provided the means of monitoring spinal cord function continuously without interfering with surgery or producing additional risk. A large body of data, including clinical experience in thousands of patients, has provided significant information regarding the utility and limitation of SSEP monitoring during spinal surgery, but no prospective controlled trial of SSEP monitoring has ever been published.1,2,5,7,11,14,15,36,38

More recently, several studies from different institutes around the world have proven that a single method of potential recording usually carries a high incidence of misdiagnosing an injury. Based on this, the growing tendency has been to establish a multimodal intraoperative monitoring (MIOM) system that usually combines SSEPs with MEPs and sometimes other varieties. The use of MIOM has documented benefits on specificity and sensitivity as well as for clinical experience and outcome measurements during different spinal surgical procedures.39

Neuroanatomic and Functional Basis

SSEP monitoring evaluates the integrity of the dorsal column. Consequently, if the dorsal columns are preserved, injury to other important pathways could occur without a change in the SSEP.16,40,41

Specifically, SSEPs are used to assess whether the lemniscal somatosensory system is intact. Impulses generated from the median nerve at the wrist (radial aspect) are transmitted through the sensory fibers to the dorsal horn of the cervical spinal cord. Next, impulses follow the dorsal tract (fasciculus cuneatus) to the ipsilateral posterior tract nuclei (nucleus cuneatus) located in the dorsal medulla. Conduction then leaves the medullary nuclei through the medial lemniscus, which, after crossing the midline, terminates in the ventrobasal nucleus of the thalamus. From the thalamus, multiple radiations connect to the primary sensory cortex. When received at the level of the cortex, afferent volleys are processed, both in the somatosensory cortex and in the parietal association fields.

In addition, SSEPs recorded from upper-extremity stimulation do not reflect lower-extremity abnormalities. Posterior tiblial SSEP monitoring must also be recorded if there is concern for damage during surgery to the spinal cord below the midcervical level. Stimulation at the level of the medial malleolus generates afferent volleys that are transmitted by sensory fibers to the dorsal horn at the conus medullaris and then carried by the dorsal tract (fasciculus gracilis) to the dorsal medullary nucleus (nucleus gracilis). Cortical conduction is then achieved via the medial lemniscus and thalamus.

MEP monitoring is typically performed by transcranial electrical stimulation of the scalp. The electrical stimulation is typically a multipulse electrical stimulus applied to the scalp overlying the motor cortex. Motor-evoked responses are recorded by EMG electrodes placed over the limbs. These responses do not require averaging but can result in movement of the patient during stimulation.

Methods of Monitoring

The two basic types of spinal cord monitoring currently used in surgery use noninvasive and invasive techniques.

Noninvasive Techniques

The noninvasive techniques involve the monitoring of potentials generated by spinal, subcortical (brainstem), or cortical pathways from the skin surface or from subdermal needle electrodes. In all the noninvasive studies, peripheral nerves in the upper extremity (median or ulnar nerve) or lower extremity (posterior tiblial or peroneal nerve) are stimulated. Recordings outside the operating field (noninvasive technique) are by far the simplest and can be performed without disturbing the surgeon’s attention from the surgical field. Recordings are most commonly made from standard scalp derivations, usually Cz-Fz (International 10-20 System)42 with leg stimulation, and C3 (C4)-Fz with arm stimulation. Other reference electrodes, such as the ears, are also used. Most of the early studies of surgical monitoring used peripheral stimulation with scalp recording, which generally gives a well-defined, although unstable, response.

The technique of monitoring potentials from a single recording site (i.e., cortical potentials) has some criticisms that must be mentioned. At times technical problems could result in loss of potentials. This result requires that both the technical and professional staff have the expertise to identify significant changes versus technical problems. Another criticism of recording only cortical potentials is that they are very sensitive to the effects of changing levels of anesthesia and decreases in blood pressure as opposed to the subcortical or spinal cord potentials.

Invasive Techniques

A number of methods of recording in the operating field have been developed to facilitate recording closer to the neural tissue.4,12,17,25,4345 These methods include subarachnoid, epidural, spinous process, and intraspinous ligament recordings. The spinal cord recording (not cortical potentials) facilitates direct evaluation of segmental changes that occur above and below the operative site. Dinner et al.4 assessed 70 of 100 scoliotic patients who were monitored with interspinous electrodes and confirmed that the spinal-evoked potentials were both reliable and reproducible, whereas the wires posed little risk to neurologic function. Lüders et al.17 successfully used spinal-evoked responses during 40 spinal procedures, 32 for scoliosis and Harrington rod placement and 8 for syrinx drainage and resection of tumors and arteriovenous malformations.

Although recordings in the surgical field can yield a much larger response, they are associated with technical problems (including disturbing the surgeon’s attention and adding to the risk of infection), with mechanical artifact, and with being limited to those surgical procedures in which the spine is opened to expose the dura. In general, such recordings require considerable technical expertise for satisfactory recordings and require that the surgeon be familiar and cooperative with the procedure. Recordings in the surgical field are most useful for spinal cord surgery (e.g., for tumors or arteriovenous malformations), in which recorded potentials can localize the area of damage or record responses that are too small to detect with other methods.

Spinal cord–evoked potential monitoring, another method of invasive recording, can be achieved by direct, segmental spinal cord stimulation using subdural electrodes. Polyphasic action potentials produced by these subdural electrodes are larger in amplitude and less likely to deteriorate or vary with minimal adjustments in anesthetic concentrations than is the case with those noted during cortical monitoring. Simultaneous ascending and descending signals are generated and can be assessed in shorter periods of time. Recordings are made over 1- to 2-minute intervals with the interspinous ligament or spinous process devices, whereas longer 10- to 230-second intervals are required when extradural or subarachnoid thoracolumbar potentials are followed. Spinal potentials may also be used in conjunction with other monitoring modalities such as the MEP or cortical-evoked responses. Limitations of this technique include intraoperative displacement of monitoring electrodes, which results in unreliable recordings and/or inadvertent neurologic injury.

Monitoring Techniques

SSEPs are recorded from the cortex with only two of the many electrodes composing the cortical array used by the International 10-20 System.42 One electrode is placed in the midsagittal plane (Cz1), and the second is applied more ventrally in the midline. A third ground is always added (Fz). Placing an additional cervical needle electrode (at C2) helps confirm whether cortical changes reflect true spinal cord changes, as opposed to local cortical variations that may occur in response to alterations in anesthetic administration. Such needle electrodes may also be placed over a lumbar spinous process (L5) to differentiate between similar alterations. SSEP skin and surface electrodes are noninvasive and are applied far away from the operative field, and monitoring may begin before induction and continue through closing.

The large mixed peripheral nerves (median, ulnar, peroneal, or posterior tiblial nerves) receive short 200-msec pulses at rates of 3 to 5 per second. The larger-diameter peripheral sensory A alpha and A beta fast-conducting fibers are stimulated with intensities set at two or three times the motor threshold, sufficient to produce a motor twitch.46 Two hundred recordings are then averaged and passed through band-pass filters of 30 Hz to 3 kHz to improve signal-to-noise ratio. Alternate stimulation of the right and left sides allows both waveforms to be simultaneously monitored with a split-screen array. This requires 50 seconds (means of 200 recordings) for two extremities and 100 seconds for all four extremities. Findings may be reproduced by repeating stimulation of one or both sides, enabling the surgeon to be alerted to significant changes in any of the four extremities within minutes (Fig. 177-1).

The most reliable SSEP recordings are produced by electrical stimulation of large mixed nerves in the limbs. Stimulation is applied to distal nerves (e.g., ulnar, median, tiblial) with surface electrodes or to proximal nerves (e.g., sciatic, cauda equina, brachial plexus). Each nerve is stimulated unilaterally in a consecutive fashion so that those pathways carrying information from all potentially affected limbs are monitored. Bilateral simultaneous stimulation may miss a unilateral injury and therefore is performed only when an adequate response cannot be obtained with unilateral stimulation. Stimulation duration and intensity are adjusted (0.2–0.5 msec, 5–90 mA) to produce maximal stimulation of sensory axons. The rate of stimulation is kept under 5 Hz to minimize rate-dependent attenuation of the SSEP, which is accentuated by anesthetics. Rates less than 2 Hz are sometimes required to record cerebral potentials in children and adolescents, especially at deeper levels of anesthesia. Stimulation rates that are even fractions of 60 Hz are avoided to prevent averaging of 60-cycle interference into the recording. The number of stimuli required for averaging varies with the amount of background noise, as well as with the size and reproducibility of the SSEP. In the absence of a preoperative deficit or excessive artifact, 200 to 300 stimuli are usually necessary for recordings made from surface electrodes. The number of stimuli averaged should be kept to a minimum so that the surgeon receives feedback as rapidly as possible.

The type of electrode recording used depends on the location of recording sites and the type of surgery. Typically, needle electrodes are used; they are held in place by staples or taped in place with steri-drape. This allows for rapid placement of electrodes and low impedance during long surgical procedures. Esophageal or nasopharyngeal electrodes are used to record cervical cord potentials outside the surgical field in cervical spine surgery. Needle electrodes inserted between spinous processes or over the laminae of the spine can be used to record spinal cord activity. Needle electrodes placed in the interspinous ligaments can be used within the operative field if the dorsal vertebral elements are left intact. Small cotton-tipped electrodes or platinum electrodes are used to record directly from the surface of the spinal cord or cerebral cortex.

For each of these active electrodes, an appropriate reference must be chosen. Nearby electrodes reduce noise, but distant electrodes enhance signal amplitude. In general, active and reference electrodes should be of the same material to minimize impedance mismatch, which increases noise. Recordings can be made at multiple peripheral and central sites along the sensory pathways. Adherence to this important principle minimizes the incidence of false-positive changes and makes troubleshooting for technical errors more efficient.

Signal amplification and filter settings are similar to those used for diagnostic outpatient SSEP recordings, although at times the sensitivity must be reduced or the band-pass restricted because of the amount of noise in the surgical environment. Amplification of 5 to 10 μV/cm, sweep speed of 2 to 10 msec/cm, low-frequency filters of 30 to 100 Hz, and high-frequency filters of 2000 to 3000 Hz are generally satisfactory. The equipment used for intraoperative SSEP recordings must be versatile and easily tailored to the specific type of procedure being monitored. The ability to record other modalities (e.g., electromyogram [EMG], MEP) concurrently with SSEP may be essential. Preamplifiers need to tolerate high current loads caused by cautery and other sources of electrical interference. Automatic cautery suppression; artifact rejection; and software for digital filtering, trend analysis, data reproduction, and storage are desirable features.

MEPs can be obtained reliably and are useful for monitoring the motor pathway function. They are elicited by either electrical or magnetic stimulation of the cortex or the spinal cord itself. Recordings are obtained as neurogenic potentials in the distal spinal cord or peripheral nerves. They also can be recorded as myogenic potentials from the innervated muscle. Contraindications for MEPs include history of seizures, past surgical skull defects, and/or metal implants in the head.47 Electrical stimulation also can be applied directly over the cord with distal neurogenic potentials recordings if a surgical decompression has been performed.

Anesthesia

Anesthesia reduces the amplitude and increases the latency of cortical SSEP recordings. This is especially true in the presence of disease and in children and adolescents. Because the reduction of amplitude is directly related to depth of anesthesia, the level of anesthetic agents should be kept as light as possible. Anesthetic effect varies with the agent used, with halogenated anesthetics producing the greatest effects, followed by moderate changes with IV barbiturates and nitrous oxide, and the least with narcotics and benzodiazepines. Etomidate and ketamine have been shown to enhance the amplitude of the cortical SSEP potentials. All volatile anesthetics, as well as nitrous oxide, produce a dose-dependent reduction in MEP signal amplitude. Because the signal amplitudes of MEP recordings are already quite small, the effect of these inhalational agents can limit the practitioner’s ability to detect significant changes intraoperatively. These drugs can be used occasionally to record cortical potentials during surgery when responses are absent with standard anesthetics. Alterations in blood pressure can also reduce the amplitude of the evoked response, especially with mean blood pressures lower than 70 mm Hg. Similar effects can be found with hypothermia, which increases latency and decreases conduction velocity.

To further limit perioperative morbidity, a consistent anesthesia protocol should accompany SSEP monitoring. In cervical spine surgery, the risk of spinal cord injury related to intubation led to the adoption of the awake, nasotracheal, fiberoptic intubation protocol, with patients at times immobilized in hard cervical collars. Often, when patients with severe cervical spinal cord compromise are being positioned, the neutral position is not the optimal position. SSEP changes may indicate that a greater or lesser degree of flexion or extension may be warranted. Induction of anesthesia proceeds only after the SSEPs return to baseline levels, because bolus injections of barbiturates transiently compromise the SSEP response for 5 to 10 minutes.

The anesthesia protocol uses preoperative and intraoperative medications. Premedications include hydroxyzine (1 mg/kg), meperidine (1 mg/kg), and atropine (0.2–0.4 mg). Numbing of the nasopharyngeal passageways is achieved with either 4% cocaine applied with cotton swabs to the nasopharynx or 10 mL of 2% lidocaine jelly applied with a no. 14-Fr nasotracheal catheter to the same area. Both regimens include a transtracheal injection with 5 mL (100 mg) of 2% lidocaine (Xylocaine). Next, a 7- to 8-mm anode tube, placed over an adult fiberoptic bronchoscope, is introduced through the nares into the larynx and trachea, with the patient receiving midazolam 1 to 5 mg as needed.

Although patients who undergo ventral surgery remain supine, those who undergo dorsal procedures may be brought to the sitting position. In this case, while the patient is still awake, a Mayfield head holder is applied using 15 mL of 1% Xylocaine and 1:200,000 epinephrine to locally anesthetize the pin sites. Careful attention must be given to positioning the arms. They should be elevated, gently flexed, and padded at the elbows to reduce traction of nerve roots or the brachial plexus.

When bringing a patient to the sitting position, it may be preferable to keep him or her awake to avoid hypotension as well as preserving intact barometric reflexes. However, even with these precautions, some awake patients demonstrate declines in both amplitudes and latency responses. These changes are attributed to a relative drop in spinal cord perfusion despite systemic normotension (relative hypotension). This may readily be reversed by the pharmacologic induction of hypertension.

During induction, infusing a bolus of thiopental (2–3 mg/kg) or propofol (Diprivan, 1–2 mg/kg) results in a transient 5- to 10-minute decline in SSEP responses. As an option, remifentanil (0.2–0.9 μg/kg/min) can be used. Inhalation anesthetic concentrations are kept between 0.2% and 0.4%, and nitrous oxide is maintained below 60% to 70%. Vecuronium is given in a loading dose of 0.1 mg/kg and then administered repeatedly as required. Alternatively, recuronium can be given, but only for intubation. Local anesthetic infiltrated into the operative wound may allow the anesthesiologist to use lower doses of anesthetic throughout surgery, which may be desirable for monitoring. Patients are immediately awakened and neurologically assessed on the operating table after surgery. Only then are the patients brought to the recovery room.

Interpretation

Animal and human studies have shown that SSEP changes can occur when there is injury to adjacent motor pathways at the spinal and brainstem levels.3,35,37,40 Assuming that appropriate stimulation and recording can be achieved, a major issue to be resolved is what constitutes a significant change and how reliably this can be detected. To further complicate matters, the primary disease often produces an SSEP abnormality that can be recognized in baseline recordings.4,12,17,25,4345 Recording methods may have to be modified. Despite averaging, multiple sources of artifacts may result in unstable potentials that are different for each patient. It is essential to determine the limits of SSEP amplitude and latency variation with repeated samples during the early part of the surgery. Significance criteria can be determined that are beyond the baseline limits of variability. In patients with high-amplitude, well-defined potentials at peripheral, spinal, and cortical levels, a reproducible drop in amplitude of 50% or greater or an increase in latency of 2 msec or greater (or >5–10% prolongation of latency), or both, is considered significant. Equally, a complete loss of waveform not explainable by technical malfunction is considered significant.

SSEPs rely on the recording of amplitude and latency values elicited from median and posterior tiblial nerve stimulation. The responses are recorded from the postcentral sulcus (noninvasive technique). Amplitude is measured, in microvolts, from the wave’s height to its trough. The amplitude reflects the integrity of a number of fibers being simultaneously stimulated to form an action potential. Amplitude varies from patient to patient according to age, height, temperature, and integrity of the system being tested. Comparison of right and left sides and assessment of changes compared with the patient’s preoperative baseline are important.

If baseline recordings with the patient under anesthesia show highly variable, low-amplitude cortical or spinal potentials, then all potentials recorded rostral to the area at risk might be required to disappear for the change to be considered significant. Implicit in these judgments is the understanding that effects of a change in physiologic variable, limb position, artifacts, and technical failures be identified and either corrected or accounted for before a final decision is made regarding the significance of a change in the SSEP.

Early in the procedure, an effort is made to identify and eliminate all sources of noise, especially 60-cycle interference. Care must be taken to avoid ground loops. Any conductor in contact with the patient (including IV lines) or electrical equipment in the room can be a source of interference. The recording system should suppress input during cautery and reject high-amplitude artifact. EMG activity from surrounding muscle can also produce unwanted artifact if neuromuscular activity is not blocked. Especially with the patient under light anesthesia, EMG activity can obscure the SSEP. A short, constant, controlled level of short-acting neuromuscular blocking agent or intermittent doses of benzodiazepines can be used to control muscle artifact in cases that require simultaneous monitoring of SSEP and EMG.

In the upper extremities, although the entire waveform from N10 (brachial plexus), N12a/N12b (segmental ascending dorsal column), N13a/N13b (dorsal horn/cuneate nucleus), and P14 (medial lemniscus) is recorded, the final cortical median N20 proves to be the most clinically relevant. Similarly, N22/P22 (dorsal horn T10 to L1), N29 (cervical gracile nucleus), P31 (medial lemniscus), and N34 (thalamus/brainstem) are noted, but the P38/N38 and P40 constitute the most used cortical potentials.

The cortical potential recorded from median nerve stimulation shows three positive peaks before the final negative trough of N20. The first of the waves at P15 indicates the afferent volley arriving at the thalamic level, whereas P16 and P18 indicate transmission via the thalamocortical tract to the primary sensory cortex. Once as the volley arrives at the cortex, additional positive peaks up to P25 indicate additional volley transmission to the surrounding sensory cortical regions.

Cortical responses noted after tiblial nerve stimulation follow a similar but more prolonged pattern. The mean latency for the posterior tiblial response P40 is typically 38.8 msec. Multiple initial negative peaks may also be visualized with these responses. These varied responses reflect the different anatomic locations along the somatosensory pathway of the posterior tiblial nerve to the cauda equina, lumbosacral spinal cord, gracile nucleus, thalamus, and cortex (Table 177-1).

Somatosensory cortical-evoked responses (compared with invasive spinal-evoked responses) have the disadvantage of being more vulnerable to changes in anesthetic techniques and are susceptible to changes in peripheral skin conditions (i.e., temperature). Cortical responses are also smaller in amplitude, and they more readily deteriorate, particularly in the presence of excessive electroencephalographic (EEG) activity or environmental noise. Averaging 200 responses per recording enhances the response, largely by eliminating random noise.

Resuscitative Measures

Anesthetic and surgical resuscitative measures may be instituted as soon as significant SSEP deterioration is detected. This measure may take place either during the first 50 seconds or after findings have been reproduced at 100 seconds. The more rapid the adoption of these techniques in response to imminent tissue damage, the faster the potentials return to baseline.

Medical causes of SSEP changes include hypotension, hypothermia, increased levels of halogenated inhalation anesthetics (>0.4% fluorane), and IV sedation. These may be reversed by inducing hypertension and hyperthermia artificially and by hyperoxygenating the wound with peroxide irrigation while increasing systemic oxygenation. The reduction or elimination of inhalation anesthesia by switching to a barbiturate “balanced” technique may also foster recovery. High-dose methylprednisolone may be emergently administered to limit neurologic injury signaled by persistent SSEP abnormalities.

Surgical maneuvers may require cessation of surgical manipulation, release or elimination of distraction, removal of excessively large grafts resulting in overdistraction, and removal of instrumentation. An example of cortical SSEP changes during spine surgery for scoliosis in shown in Figure 177-2. For patients with ossification of the posterior longitudinal ligament, changes in SSEP responses are common. For these individuals, distraction is therefore avoided until the pathologic abnormality has been fully excised.

References

1. Allen A., Starr A., Nudleman K. Assessment of sensory function in the operating room utilizing cerebral evoked potentials: a study of fifty-six surgically anesthetized patients. Clin Neurosurg. 1981;28:457.

2. Brown J.C., Axelgaard J., Rowe D.E. Monitoring of the human spinal cord. Orthop Trans. 1979;3:123.

3. D’Angelo C.M., VanGilder J.C., Taur A. Evoked cortical potentials in experimental spinal cord trauma. J Neurosurg. 1973;38:332.

4. Dinner D.S., Lüders H., Lesser R.P., et al. Intraoperative spinal somatosensory evoked potentials monitoring. J Neurosurg. 1986;65:807.

5. Engler G.L., Spielholz N.I., Bernhard W.N., et al. Somatosensory evoked potentials during Harrington instrumentation for scoliosis. J Bone Joint Surg [Am]. 1978;60:528.

6. Giblin D.R. Somatosensory evoked potentials in healthy subjects and in patients with lesions of the nervous system. Ann NY Acad Sci. 1964;112:93.

7. Grundy B.L. Monitoring of sensory evoked potentials during neurosurgical operations: methods and applications. Neurosurgery. 1982;11:556.

8. Grundy B.L., Nelson P.B., Doyle E., Procopio P.T. Intraoperative loss of somatosensory-evoked potentials predicts loss of spinal cord function. Anesthesiology. 1982;57:321.

9. Hahn J.F., Lesser R., Klem G., et al. Simple technique for monitoring intraoperative spinal cord function. Neurosurgery. 1981;9:692.

10. Halliday A.M., Wakefield G.S. Cerebral evoked responses in patients with dissociated sensory loss. Electroencephalogr Clin Neurophysiol. 1962;14:786.

11. Jones S.J., Edgar M.A., Ransford A.O., et al. A system for electrophysiological monitoring of the spinal cord during operations for scoliosis. J Bone Joint Surg [Br]. 1983;65:134.

12. Klem G., Andrish J., Gurd A., et al. Spinal cord evoked potentials recorded from ligamentum interspinalis. Electroencephalogr Clin Neurophysiol. 1980;50:221.

13. Kobrine A.I., Evans D.E., Rizzoli H.V. Correlation of spinal cord blood flow, sensory evoked response, and spinal cord function in subacute experimental spinal cord compression. Cervos-Navarro J., Betz E., Ebhardt G., et al, editors. Pathology of cerebrospinal microcirculation: advances in neurology. New York: Raven Press. 1978;vol 20:389.

14. LaMont R.L., Wasson S.L., Green M.A. Spinal cord monitoring during spinal surgery using somatosensory spinal evoked potentials. J Pediatr Orthop. 1983;3:31.

15. Larson S.J., Sances A.Jr., Christenson P.C. Evoked somatosensory potentials in man. Arch Neurol. 1966;15:88.

16. Lesser R.P., Raudzens P., Lüders H., et al. Postoperative neurological deficits may occur despite unchanged intraoperative somatosensory evoked potentials. Ann Neurol. 1986;19:22.

17. Lüders H., Gurd A., Hahn J., et al. A new technique for intraoperative monitoring of spinal cord function: multichannel recording of spinal cord and subcortical evoked potentials. Spine (Phila Pa 1976). 1982;7:110.

18. Maccabee P., Levine D.B., Kahanovitz N., et al. Monitoring of spinal and subcortical somatosensory evoked potentials during Harrington rod instrumentation. Orthop Trans. 1982;6:19.

19. MacEwen G.D., Bunnell W.P., Sriram K. Acute neurological complications in the treatment of scoliosis. A report of the Scoliosis Research Society. J Bone Joint Surg [Am]. 1975;57:404.

20. Macon J.B., Poletti C.E., Sweet W.H., et al. Conducted somatosensory evoked potentials during spinal surgery. Part 2: Clinical applications. J Neurosurg. 1982;57:354.

21. McCallum J.E., Bennett M.H. Electrophysiologic monitoring of spinal cord function during intraspinal surgery. Surg Forum. 1975;26:469.

22. Nash C.L.Jr., Lorig R.A., Schatzinger L.A., et al. Spinal cord monitoring during operative treatment of spine. Clin Orthop Relat Res. 1977;126:100.

23. Nuwer M.R., Dawson E.C. Intraoperative evoked potential monitoring of the spinal cord. A restricted filter, scalp method during Harrington instrumentation for scoliosis. Clin Orthop Relat Res. 1984;183:42.

24. Raudzens P.A. Intraoperative monitoring of evoked potentials. Ann NY Acad Sci. 1982;388:308.

25. Schramm J., Hashizume K., Fukushima T., et al. Experimental spinal cord injury produced by slow, graded compression. Alterations of cortical and spinal evoked potentials. J Neurosurg. 1979;50:48.

26. Spielholz N.I., Benjamin M.V., Engler G.L., et al. Somatosensory evoked potentials during decompression and stabilization of the spine. Methods and findings. Spine (Phila Pa 1976). 1979;4:500.

27. Tamaki T., Tsuji H., Inoue S., et al. The prevention of iatrogenic spinal cord injury utilizing the evoked spinal cord potential. Int Orthop. 1981;4:313.

28. Tsuji S., Lüders H., Lesser R.P., et al. Subcortical and cortical somatosensory potentials evoked by posterior tibial nerve stimulation: normative values. Electroencephalogr Clin Neurophysiol. 1984;59:214.

29. Tsuyama N., Tsuzuki N., Kurokawa T., et al. Clinical application of spinal cord action potential movement. Int Orthop. 1978;2:39.

30. Wilber R.G., Thompson G.H., Shaffer J.W., et al. Postoperative neurological deficits in segmental spinal instrumentation. A study using spinal cord monitoring. J Bone Joint Surg [Am]. 1984;66:1178.

31. Worth R.M., Markand O.N., DeRosa G.P., et al. Intraoperative somatosensory evoked response monitoring during spinal cord surgery. Courjon J., Mauguiere F., Revol M., editors. Clinical applications of evoked potentials in neurology: advances in neurology. New York: Raven Press. 1982;vol 22:p 367.

32. Bennett M.H. Effects of compression and ischemia on spinal cord evoked potentials. Exp Neurol. 1983;80:508.

33. Coles J.G., Wilson G.J., Sima A.F., et al. Intraoperative detection of spinal chord ischemia using somatosensory cortical evoked potentials during thoracic aortic occlusion. Ann Thorac Surg. 1982;34:299.

34. Croft T.J., Brodkey J.S., Nulsen F.E. Reversible spinal cord trauma: a model for electrical monitoring of spinal cord function. J Neurosurg. 1972;36:402.

35. Dolan E.J., Transfeldt E.E., Tator C.H., et al. The effects of spinal distraction on regional spinal cord in cats. J Neurosurg. 1980;53:756.

36. Allison T. Recovery functions of somatosensory evoked responses in man. Electroencephalogr Clin Neurophysiol. 1962;14:331.

37. Brodkey J.S., Richards D.E., Blasingame J.P., et al. Reversible spinal cord trauma in cats. Additive effects of direct pressure and ischemia. J Neurosurg. 1972;37:591.

38. McNeal D., Passoff T., Swank S., et al. Spinal cord monitoring using epidural electrodes for stimulation and recording. Orthop Trans. 1982;6:19.

39. Sutter M., Deletis V., Dvorak J., et al. Current opinions and recommendations on multimodal intraoperative monitoring during spine surgeries. Eur Spine J. 2007;16(Suppl 2):S232.

40. Deecke L., Tator C.H. Neurophysiological assessment of afferent and efferent conduction in the injured spinal cord of monkeys. J Neurosurg. 1973;39:65.

41. Griffiths I.R., Trench J.G., Crawford R.A. Spinal cord blood flow and conduction during experimental cord compression in normotensive and hypotensive dogs. J Neurosurg. 1979;50:353.

42. Jasper H.H. The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol. 1958;10:371.

43. Cusick J.F., Myklebust J., Larson S.J., Sances A.Jr. Spinal evoked potentials in the primate: neural substrate. J Neurosurg. 1978;49:551.

44. Lüders H., Andrish J., Gurd A., et al. Origin of far-field subcortical potentials evoked by stimulation of the posterior tibial nerve. Electroencephalogr Clin Neurophysiol. 1981;52:336.

45. Nordwall A., Axelgaard J., Harada Y., et al. Spinal cord monitoring using evoked potentials recorded from feline vertebral bone. Spine (Phila Pa 1976). 1979;4:486.

46. Lesser R.P., Koehle R., Lueders H. Effect of stimulus intensity on short latency somatosensory evoked potentials. Electroencephalogr Clin Neurophysiol. 1979;47:377.

47. Greenberg M. Electrodiagnostics. Greenbery M., et al, editors, ed 7. Handbook of Neurosurgery. New York: Thieme, 2010. p 266