Surgical Treatment of Thoracic Ossification of the Posterior Longitudinal Ligament: Intraoperative Spinal Cord Monitoring
Yukihiro Matsuyama, Taichi Tsuji, Hisatake Yoshihara, Yoshihito Sakai, Hiroshi Nakamura, and Naoki Ishiguro
Introduction
Myelopathy caused by ossifi cation of the posterior lon- gitudinal ligament (OPLL) of the thoracic spine cannot be treated adequately by conservative therapy and therefore demands surgical intervention. However, surgical outcomes reported to date have not been sat- isfactory [1–12], and effective surgical procedures for this disease have still to be established. One reason for the poor surgical outcomes is the presence of physio- logical kyphosis in the thoracic spine, which does not exist in the cervical or lumbar spine and which may compromise the effects of spinal cord decompression via a posterior approach. In addition, anterior approaches are technically challenging because: (1) adhesion of the dura mater to ossifi ed ligaments may hamper surgical manipulations; (2) median sternotomy is required for an approach to the upper thoracic spine, in which visualization of the surgical fi eld [3–7] is limited; and (3) mid or lower thoracic spinal surgery requires an anterolateral approach involving rib resec- tion [9,12]. We have recently reported four cases of neurological deterioration after an operation for tho- racic OPLL, all of which exhibited a sharply protruding, segmental form of ossifi cation [1,2]. When severe spinal cord compression is present as a result of adhesion of the ossifi ed yellow ligament to the dura mater or ossi- fi cation of the dura mater itself, laminectomy can easily compromise the vulnerable spinal cord. Laminectomy may also augment thoracic kyphosis, which causes spinal cord injury. This report describes a method of intraoperative spinal cord monitoring during posterior decompression surgery for thoracic OPLL performed to avoid spinal cord injury, the most serious complication associated with these surgical procedures for thoracic OPLL.
Surgical Procedures for Thoracic OPLL
Posterior decompression is indicated for many cases of thoracic OPLL because of the frequent combination of OPLL with ossifi cation of the yellow ligament (OYL).
We routinely perform a posterior decompression pro- cedure with corrective spinal instrumentation. We gen- erally complete the operation by using intraoperative ultrasonography (IOUS) to confi rm that the correction of thoracic kyphosis has resulted in adequate decom- pression of the spinal cord. If the neurogical recovery is not satisfactory, an additional decompression proce- dure via an anterior or posterior approach is performed in one or two stages, depending on the operating time and the amount of blood lost. Posterior decompression with corrective fusion is usually associated with a good postoperative outcome, and two-stage surgery is not necessary.
Significance of Intraoperative Spinal Cord Monitoring
In Japan, spinal cord evoked potentials (SCEPs), as described by Tamaki et al., have generally been used to monitor spinal cord function. Although this method is reliable for obtaining stable evoked potentials, the dis- advantages of this procedure are that it requires intri- cate manipulation of recording electrodes placed in the epidural or subarachnoidal space, that it does not allow adjusting the electrode position in areas outside the surgical fi eld, and it does not allow direct monitoring of the integrity of the spinal motor tract [13,14]. Recent advances in spinal cord monitoring techniques have led to the wide use of electromyographic monitoring using high-frequency transcranial electrical stimulation [15].
This technique allows the surgeon to monitor motor tract function easily and directly.
Since July 2000, we have introduced intraoperative recording of compound muscle action potentials (CMAPs) using high-frequency transcranial electrical Department of Orthopaedic Surgery, Nagoya University
School of Medicine, 65 Tsuruma-cho, Showa-ku, Nagoya 466-8550, Japan
279
stimulation to monitor spinal motor tract function.
Only four channels were used initially, but 16-channel monitoring has been utilized since August 2002. This method allows intraoperative monitoring of all spinal cord function and easily detects technical failures. We believe that the current CMAP method can reduce the high false-positive rate, which has prevented wide- spread use of conventional monitoring methods.
CMAP Monitoring Method
Instruments
A D185 MultiPulse Stimulator (Digitimer, Welwyn Garden City, UK) was used for the electrical stimula- tion. Electromyography (EMG) recording was per- formed using Neuropack and MEB-2200 software, Version 04.02 (Nihon Kohden, Tokyo, Japan). Silver/
silver chloride disk electrodes with a diameter of 15 mm and disk or needle electrodes with a diameter of 6 mm were used as the stimulating and recording electrodes, respectively. Anal plug electrodes (Inter Medical, Nagoya, Japan) were used for EMG of the external anal sphincter, with some modifi cations. Pad electrodes commonly used for cautery knives were used for grounding.
Electrode Placement
Scalp regions above the motor cortex, 2 cm anterior and 3 cm lateral to Cz (according to the international 10–20 system), were selected for transcranial electrical stimulation (Fig. 1). A generous quantity of the elec-
trode paste Flefi x (Nihon Kohden), used for electroen- cephalography (EEG), was applied, and the stimulating electrodes were placed on the scalp regions. For precise monitoring of upper extremity function, disk- or needle-type recording electrodes were placed on muscles, including the deltoid, biceps brachii, triceps brachii, interosseous, and extensor pollicis brevis.
Although needle electrodes were superior for obtain- ing a sharply defi ned waveform, disk electrodes were also useful when the electrodes were placed by the medical staff. Disk electrodes were generally used for the distal muscles, as EMG could be recorded more easily from distal muscles than from proximal muscles.
For monitoring lower extremity function, electrodes were placed on muscles that included the quadriceps femoris, hamstrings, tibialis anterior, gastrocnemius, and peroneus brevis. In addition, anal plug electrodes designed by the authors were placed on the external anal sphincter [16]. The anal electrodes were quad- ripolar, and EMG could be recorded from either side of the external anal sphincter. EMG recording channels were selected (up to a maximum of 16 channels) from these electrodes, depending on the level of the spine undergoing operation or the type of procedure employed. Electrical stimulation consisted of four or fi ve trains at a stimulation voltage of approximately 600 V [17]. Recording conditions were as outlined in Table 1.
Anesthesia
Selecting an appropriate type of anesthesia is important for CMAP recording because the recording is easily affected by it, especially muscle relaxants. We therefore informed the anesthesiologist about the CAMP moni- toring in advance and requested intravenous induction and maintenance of anesthesia with propofol and fen- tanyl alone, without the use of inhalation anesthetics.
Muscle relaxation was maintained at the level of 2/4, using train-of-four (TOF) stimulation and a neuromus- cular monitor TOF Guard (Biometer, Odense, Denmark) by continuous intravenous infusion of vecuronium using a syringe pump. This level of muscle relaxation was generally obtained with vecuronium at a dose of 1.5–2.0 mg/h.
Cz
Fig. 1. Stimulating electrodes are placed bilaterally at points 2 cm anterior and 3 cm lateral to Cz on the scalp. When prior- ity was given to the recording from the lower extremities, intervals between the electrodes were shortened
Table 1. Conditions for stimulation and recording
Train stimulation 4∼ 5 times
Interstimulus interval 2 ms
Stimulus 450∼ 630 V
Filtering 50∼ 1000 Hz
Recording time 100 ms
Multichannel CMAP Monitoring
A total of 142 patients have undergone spinal surgery with intraoperative spinal cord monitoring at Nagoya University Hospital since July 2000. CMAP monitoring was performed in all of these patients; in addition, 39 recent patients who underwent multichannel CMAP monitoring were evaluated. The average number of recorded muscles per patient was 13.4± 2.7, and all 16 channels were used in nine patients. CMAPs could be obtained in all patients from one or more muscles in both the upper and lower extremities. CMAPs were recordable from 146 (93.6%) of 156 upper extremity muscles monitored in total, 296 (98.7%) of 300 lower extremity muscles, and 71 (92.2%) of the 77 external anal sphincter muscles examined. In some patients, recording was diffi cult at the beginning of the opera- tion owing to a relatively high dose of the muscle relaxant for anesthesia induction, but good CMAPs were obtained before starting the more invasive opera- tive procedures. We consulted constantly with the anesthesiologist and monitored TOF Guard values during the operation to maintain stable muscle relaxa- tion. When the recording was unstable, the conditions of both the stimulating and recording electrodes were examined and corrected from areas outside the surgi- cal fi eld.
Case Report
The patient described here experienced a reduction in CMAPs during laminectomy and subsequent recovery of the potentials after a 5-min interruption of the lami- nectomy procedure.
A 58-year-old woman presented with gait distur- bance. Neurological examination revealed a slight sensory disturbance in the lower extremities, hyperre- fl exia, and ankle clonus; her muscle strength was normal. Imaging studies demonstrated spinal cord compression by OPLL extending from the cervical to the thoracic spine, accompanied by OYL at the T5-T6 level (Fig. 2a,b). Laminoplasty (Kurokawa method) was initially performed at the C3-T2 level followed by tem- porary fi xation using pedicle screw placement at T3, T4, T8, and T9 to prevent progression of kyphosis during the thoracic laminectomy. No alterations in CMAPs were observed during these procedures. Laminectomy was subsequently performed at the T3-T6 level. Severe OYL, as well as complete ossifi cation of the dura mater, were identifi ed at the T5-T6 level. An air drill diamond bur was used to excise the laminae and ossifi ed liga- ments. The spinal cord was not compressed during this procedure; twitches occurred in the lower extremities, and CMAPs diminished in amplitude approximately
10 min later. We assumed that the heat created by the surgical air form affected the vulnerable spinal cord.
During a 5-min interruption of the laminectomy, CMAPs recovered gradually until normal waveforms were apparent 10 min later (Fig. 2c). In contrast, motor evoked potentials (MEPs), which were monitored simultaneously, did not change.
These observations suggest that CMAP monitoring is superior to MEP monitoring for detecting small changes in spinal cord function, and therefore CMAP monitor- ing is suitable for surgery involving thoracic OPLL or intramedullary spinal cord tumors, during which the spinal cord is extremely vulnerable. We believe that spinal cord injury was avoided in this patient because CMAPs were used for spinal cord monitoring. IOSS (Fig. 2d), postoperative radiography, and computed tomography (CT) (Fig. 2e) demonstrated that correc- tion of kyphosis led to indirect spinal cord decompres- sion, and the patient’s gait disturbance diminished after the operation.
Discussion
Neurological deterioration following posterior decom- pression of thoracic OPLL is related to the surgical manipulations involved in these technically challenging procedures as well as alterations in spinal alignment induced by destruction of the posterior spinal struc- tures during posterior decompression. The patients presented herein exhibited spinal dysfunction second- ary to progression of kyphosis following decompres- sion. IOSS demonstrated that the spinal cord was further compressed anteriorly as a result of increased kyphosis (which was subsequently corrected by spinal instrumentation) and led indirectly to decompression of the spinal cord. The decline in CMAPs associated with spinal decompression also recovered following the correction of kyphosis. Dysfunction of the vulnerable spinal cord as a result of mechanical compression or heat produced by the laminectomy procedure was detected early by CMAP monitoring, which contributed signifi cantly to preventing spinal cord paralysis.
Choice of Monitoring Technique
Intraoperative spinal cord monitoring techniques include SCEP monitoring described above, which records spinal cord potentials evoked by spinal cord stimulation as well as monitoring of spinal cord poten- tials evoked by transcranial stimulation, muscle action potentials evoked by spinal cord stimulation, and muscle action potentials evoked by transcranial stimu- lation, which are routinely performed by our group [15,18,19]. The ideal technique for intraoperative
4
4 5
6
T5/T6
T5/T6
T6/T7 T8/T9
4 5
6
12 7
8 9
10 11
a
b Fig. 2.
Fig. 2. aMagnetic resonance imaging (MRI) demonstrates spinal cord compression by ossifi cation of the posterior longi- tudinal ligament (OPLL) and of the yellow ligament (OYL) around the T5-T6 level. b Myelography-computed tomography (myelo-CT) image demonstrating continuous OPLL extending from T5 to T9, with prominent spinal cord compression by OPLL and OYL at the T5-T6 level. c Intraoperative recording
of compound muscle action potentials (CMAPs) and motor evoked potentials (MEPs). CMAPs diminished when the twitches in the left lower extremity appeared, but no alterations in MEPs were observed. CMAPs recovered to the baseline waveform after 10 min. d Intraoperative ultrasonography (IOSS) demonstrates that correction of kyphosis leads to spinal cord decompression and restoration of good pulsation.
Left leg CMAP MEP
10 min later
After laminectomy
After correction of kyphosis
Spinal cord
Spinal cord
c
d
monitoring of spinal cord function remains a contro- versial issue. SCEPs and spinal cord potentials evoked by transcranial stimulation are not suitable for moni- toring motor tract function because the origin of the potentials cannot be differentiated between the motor tract and the sensory tract. Muscle action potentials evoked by spinal cord stimulation are diffi cult to record because of the low amplitude of the waveforms. Thus, CMAP recording using high-frequency transcranial electrical stimulation (the CMAP method) is the most practical technique, at present, for monitoring spinal motor function intraoperatively.
The primary problem associated with the CMAP method is that the waveforms are easily affected by anesthesia. In addition, some surgeons do not want to use this method because the high sensitivity of the method for detecting spinal cord dysfunction could interfere with performing the surgical procedure. This suggests that the interpretation of the CMAP wave- forms is not easy because, unlike SCEPs, the range of amplitude and the latency that indicate the risk of nervous damage are not well defi ned. Therefore, this method may not be suited for spinal cord monitoring
during cardiovascular surgery because spinal cord isch- emia occurs repeatedly. However, the CMAP method is ideal for spinal surgery, especially for thoracic OPLL (where the spinal cord is vulnerable to injury) and intramedullary spinal cord tumors (which require myelotomy). This is because the CMAP method is sen- sitive, has a high degree of safety, and can detect spinal dysfunction when it is still reversible [20,21]. Our inten- tion is to conduct spinal cord monitoring, which allows safe surgical manipulation, so patients can move their extremities immediately after operation. As for the risk range of CMAP, we consider the loss of waveforms to indicate a risk of spinal damage. When waveforms are lost, the surgeon should cease the procedure and wait until the potentials recover. When spinal damage occurs, the potentials tend to diminish so quickly that the latency prolongation cannot be measured. During the operation, waveforms should be judged as either normal or having loss of potential, so the surgeon can easily and clearly understand the situation. We perform surgery for intramedullary spinal cord tumors and tho- racic OPLL in approximately 15 and 10 patients per year, respectively. Since we started using the sensitive
4 5
6
12 7
8 9 10
11
Fig. 2. e Postoperative radiographs and MR images. The region with the maximum stenosis was decompressed via a transpedicular approach, and it was considered imperative to resect both the superior and inferior articular processes to
decompress the spinal cord completely. Posterior spinal fusion with instrumentation was therefore necessary to com- plete the procedure and effectively corrected the kyphosis e
CMAP monitoring, we have been able to stop surgery when potentials are lost and wait for their recovery.
Postoperative neurological outcomes of intramedullary spinal cord tumors and thoracic OPLL have improved signifi cantly with this method.
Although the methods of anesthesia are different among institutions, the use of propofol and other intra- venous anesthetics has recently gained popularity. A sudden loss of muscle potentials occasionally occurs in these patients owing to an increased dose of muscle relaxant. Suffi cient preoperative discussion and good intraoperative cooperation with the anesthesiologist are essential for successful spinal cord monitoring.
Advantages of Multichannel Monitoring
The primary advantage of our multichannel monitor- ing is that spinal segments at the C5-T1 and L1-S4 levels, which are important to motor functions for activities of daily living, can be monitored simultane- ously. In addition, control waveforms can be obtained from the same patient, which is useful for distinguish- ing actual spinal dysfunction from technical failures.
For example, when potentials in the lower extremities diminish during thoracic spine surgery and similar decreases in potential are observed in the upper extrem- ities, effects other than those due to surgical manipula- tions (primarily the effect of muscle relaxants) are suggested. When potentials from a few muscles dimin- ish that do not correspond to the operated spinal level, technical failures are suspected and the electrodes should be checked from outside the surgical fi eld.
Indeed, in one case we found that the patient’s arm had fallen off the surgical bed; in another case, peripheral nerve compression was suspected and treated success- fully. The multichannel method is useful not only to monitor spinal function but also to monitor the patient’s general condition during the operation. The relatively long preoperative preparation time (approximately 20min) is only a minor disadvantage considering the safety of the operation provided by this method.
The number of channels is determined according to the spinal levels to be operated on and the potential risk of the surgery.
Limitations of the CMAP Method
Currently, the CMAP method cannot be used in patients with intracerebral organic disease, a history of epilepsy, or cardiac disease, especially dysfunction of the con- ducting pathway with an implanted pacemaker. In these cases other monitoring techniques, such as SCEPs or somatosensory evoked potentials, should be used;
and in some cases spinal cord monitoring itself must be abandoned. Also, there are cases in which preoperative muscle strength is so weak that CMAP cannot be recorded. Morota and Nakagawa [18] reported that CMAP recording is diffi cult in patients with manual muscle test (MMT) grades below 4, whereas in our experience CMAPs can be recorded in patients with MMT grade 3 or higher. In these cases, spinal cord monitoring can be attempted by placing a catheter elec- trode in the epidural space. When using multichannel monitoring, surgery can proceed using potentials detectable from any muscles. In these cases, however, sensitive monitoring cannot be expected, which is the technical limitation of the current CMAP method.
Future Directions in Spinal Cord Monitoring
Intraoperative spinal cord monitoring has been recog- nized as a specialized technique that is performed only in some leading medical institutions. This is likely because excessive emphasis has been placed on the sci- entifi c aspects of the technique, which makes under- standing spinal cord monitoring diffi cult for general spine surgeons who had not specialized in electrophysi- ology. The CMAP method, which uses stimulation of the motor cortex to move muscles, is relatively easy to understand and would be accepted by many spinal sur- geons. In addition, considering the recent challenges facing spinal surgeons (i.e., the increasing number of medicolegal problems), CMAP spinal cord monitoring is likely to become a standard essential technique during general spinal surgery.
References
1. Matsuyama Y, Satou K, Kawakami N (2000) Thoracic ossi- fi cation of posterior longitudinal ligament evaluation of postoperative deteriorated cases (in Japanese). Rinsho Seikeigeka 35:39–46
2. Matsuyama Y, Gotou M, Kawakami H (2005) Surgical outcome of ossifi cation of the posterior longitudinal liga- ment (OPLL) of the thoracic spine: implication of the type of ossifi cation and surgical options. J Spinal Disord Tech 18(6):492–497
3. Fujimura Y, Satomi K, Hirabayashi H (1989) Indication and limitation of the anterior decompression for ossifi ca- tion of the posterior longitudinal ligament in the thoracic spine (in Japanese). J Sekitsui Sekizui 2:671–677
4. Fujimura Y, Koyanagi T, Toyama Y (1993) Long-term follow-up of the anterior decompression for ossifi cation of the posterior longitudinal ligament in the thoracic spine (in Japanese). J Sekitsui Sekizui 6:873–879
5. Fujimura Y, Nishi Y, Nakamura M, Toyama Y, Suzuki N (1997) Long-term follow-up study of anterior decompres- sion and fusion for thoracic myelopathy resulting from ossifi cation of the posterior longitudinal ligament. Spine 22:305–311
6. Ohtani K, Masuashi K, Shibasaki K (1977) Anterior decompression for ossifi cation of the posterior longitudi- nal ligament in the thoracic spine (in Japanese). Rinsho Seikeigeka 12:353–359
7. Ohtani K, Nakai S, Fujimura Y, Manzoku S, Shibasaki K (1982) Anterior surgical decompression for thoracic myelopathy as a result of ossifi cation of the posterior lon- gitudinal ligament. Clin Orthop 166:82–88
8. Ohotsuka K, Terayama K, Tsuchiya S (1983) Anterior decompression via posterior approach for the spinal cord in the thoracic lesion (in Japanese) Orthop Surg Trauma- tol 26:1083–1090
9. Tomita K, Kawahara N, Baba H, Kikuchi Y, Nishimura H (1990) Circumspinal decompression for thoracic myelop- athy due to combined ossifi cation of the posterior longi- tudinal ligament and ligamentum fl avum. Spine 15:1114–
1120
10. Tsuzuki N, Tanaka H, Seichi A (1989) Lamino- pedi culoplasty, a new method of reconstructing the posterior elements of the thoracic spine. Int Orthop 13:39–45
11. Tsuzuki N, Hirabayashi S, Abe R, Saiki K (2001) Staged spinal cord decompression through posterior approach for thoracic myelopathy caused by ossifi cation of poste- rior longitudinal ligament. Spine 26:1623–1630
12. Yonenobu K, Korkusuz F, Hosono N, Ebara S, Ono K (1990) Lateral rhachotomy for thoracic spinal lesions.
Spine 15:1121–1125
13. Iizuka T (1993) Spinal cord evoked potential by electric stimulation of brainstem: basic and clinical application.
J Sekitzui Sekizui 6:441–448
14. Imai T (1976) Spinal cord evoked potential by epidural space stimulation: basic fi ndings and meaning. J Niphon Seiekigeka Soc 50:1037–1056
15. Shinomiya F (2000) Intraoperative spinal cord monitor- ing: comparison between multimodality spinal cord mon- itoring (in Japanese). Rinsyo Noha 42:353–359
16. Tuji T, Matsuyama Y, Gotou M (2002) Monitoring of anal sphincter muscle at spinal surgery (in Japanese). Sekitsui Sekizui Shindann 24:76–80
17. Jones SJ, Harrison R, Koh KF (1996) Motor evoked poten- tial monitoring during spinal surgery: responses of distal limb muscles to transcranial cortical stimulation with pulse trains. Electroencephalogr Clin Neurophysiol 100:375–383
18. Morota N, Nakagawa H (1999) Intraoperative spinal cord monitoring at spinal surgery (in Japanese). J Sekitsui Sekizui 12:632–638
19. Iizuka T (1999) Spinal cord monitoring: update and new method for monitoring of motor pathway just after the operation (in Japanese). Orthop Surg Traumatol 42:869–
876
20. Nakagawa Y, Tamaki T, Yamada H, Nishiura H (2002) Discrepancy between decreases in the amplitude of com- pound muscle action potential and loss of motor function caused by ischemic and compressive insults to the spinal cord. J Orthop Sci 7:102–110
21. 21. Machida M, Weinstein SL, Yamada T, Kimura J, Toriyama S (1988) Dissociation muscle action potentials and spinal somatosensory evoked potentials after ischemic damage of spinal cord. Spine 13:1119–1124
