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Evoked spinal electrogram in a quadriplegic patient
659
Electroencephalography and Clinical Neurophysiology, 1973, 35:659-662 ,~ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
CLINICAL
NOTE
EVOKED SPINAL ELECTROGRAM I N A QUADRIPLEGIC P A T I E N T 1 KOKI SHIMOJ], TATSUHIKO KANO, TOHRU MORIOKA AND ETSUTARO IKEZONO
Department of Anesthesiology, Tokyo Medical and Dental University, Tokyo, and Department of Anesthesioloqy, Kumamoto University Medical School, Kumamoto (Japan) (Accepted for publication: June 7, 1973)
Recently, we have succeeded in recording the human evoked spinal electrogram (ESEG) from the dorsal epidural space simply and safely (Shimoji et al. 1971), based on the technique of epidural anesthesia, and analyzed it in detail (Shimoji et al. 1972). The present report will describe the patterns of ESEG recorded from both the epidural and intrathecal spaces in a quadriplegic patient.
i This work was supported in part by a Grant from the Japanese Ministry of Education.
MATERIAL AND METHOD A 23-year-old male had a quadriplegia caused by an accident 5 days previous to admission. On admission, physical examinations revealed complete motor paralysis and sensory loss below the level of C 5 with paresis of the diaphragm which caused respiratory insufficiency. X-ray examination disclosed dislocation of the 5th cervical vertebra (Fig. 1, A). For the management of respiratory inadequacy, an intratracheal tube was intubated through a tracheotomized opening and ventilation was assisted or controlled through a cm
~2 E~ C5 E _}S..~."R~ /
2 ~'E3 2
4
cm
8
42
6
8cm
.. -)
~
E
2
4
6
6
8cm
Fig. 1. A: X-ray showing the site of dislocation of the C5 vertebra. B: Drawing with reference to the X-ray, showing the position of electrodes in the epidural space (El, E2, E3, E, and E6), the intrathecal space (Es) and the supraspinous ligaments (reference electrodes, R l for El, E 2 and E3, R 2 for E4, E5 and E6).
K. SHIMOJI et al.
660 volume-preset ventilator arranged to keep PaCO2 at around 40 mmHg. On the 5th day, PO 2, PCO2, pH and base excess in the arterial blood were 76 mmHg, 38 mmHg, 7.460 and + 3.2 mEq/L, respectively. Serum electrolytes were within the normal range (Na 140, K 4.3, CI 116, Ca 4.7 mEq/L). Blood pressure varied between 140/90 and 110/70 mmHg. The condition of the patient remained much the same for 3 weeks after admission except for the gradual increase in spinal reflexes. Thereafter, the general condition of the patient gradually deteriorated. He died of respiratory disturbances on the 49th day after admission. Autopsy revealed vertebral impingement upon the anterior surface of the spinal cord at the C5 level, and cerebral edema. On the 7th and 8th days after admission, recording of the ESEG had been undertaken. Stainless-steel electrodes 150/t in diameter insulated up to 5 mm from the tip, were inserted into the dorsal epidural space at C2, C7, T12, and L 1 levels as shown in Fig. 1, B. The procedures used to introduce the electrodes into the epidural space have been described in detail in a previous paper (Shimoji et al. 1971). One electrode was also introduced into the intrathecal space at the L1 level. The indifferent needle electrode was inserted into the supraspinous ligament of the adjacent segment. Placement of the tips of the electrodes was verified radiologically at the end of recording. Square pulses of 0.5 msec duration and of varying intensities were delivered by the chlorided silver needle electrodes through a stimulator (NIHONKOHDEN MSE-3 i
K
,
i
with an isolation unit, to the ulnar nerve at the elbow or posterior tibial nerve at the popliteal fossa every 1-2 sec. The ESEG in responses to the direct stimulation of the spinal cord by epidural electrodes were also recorded. The rostral part of the spinal cord was stimulated with E2 (cathode) and E 3 (anode) electrodes, and the caudal part of it, with E4 (cathode) and E 6 (anode) electrodes (Fig. 1, B). The ESEG and the evoked electromyogram (EEMG) were led to a polygraph (NIHONKOHDEN RM-150M), and an oscilloscope (NIHONKOHDEN VC-7) and were averaged through a computer (ATAC-501-10). The time constants adopted were 0.3 sec for recording the EEG and SEG, and 0.01 sec for the EEMG. RESULTS The ESEG, recorded from the dorsal epidural space directly activated by somatosensory stimulation (the "segmental" ESEG)consisted of early positive (P a), negative (N1) and positive (Pz) deflections followed by delayed components (Fig. 2). Although P2 and delayed components were sometimes impaired by the EKG artifact, PI and N 1 components were hardly affected by the EKG or other artifacts during the course of averaging. This is shown in Fig. 2 and 3, in which early P1 and N~ deflections remain constant in three series of averaged responses, whereas P2 and delayed components show a relative variability. Peak latencies and durations of these early deflections are shown in Table I with approximate P2
J
SuV
A
/
P2
E6
B E5
N,
[5uV
ii
t 25uV
__llOOuV psec
50msec
Fig. 2. Simultaneous recording from the dorsal epidural space (E6) and from the antero-lateral intrathecal space (Es) of the ESEG in response to electrical stimulation (25 V) of left (A) and right (B) posterior tibial nerves. Left: polygraphic tracing. K : electrocardiogram. Arrows indicate the ESEG noticeable in the polygraphic record. Right : Superimposition of three sequentially averaged series of ESEGs (N = 50). Note the different calibration between the epidural and intrathecal recordings in left B (5#V for the epidural recording; 25 #V for the intrathecal recording). The start of the sweep corresponds to the electrical shocks in this and the following records. Upward deflection denotes positivity in all records. Refer to Fig. I, B, for the position of electrodes.
661
EVOKED SPINAL ELECTROGRAM IN QUADRIPLEGIA TABLE I Peak latencies and durations of the early components in the "segmental" ESEGs. Stim.
Record
Ulnar n Post. tib. n
C7(E3) LI(E6)
Peak latency (msec)
Duration* (msec)
Distance (cm)
P1
Nt
P2
P,
N1
P2
6.5 12.5
13.0 17.5
41.8 35.0
1.8___0.01 2.2_+0.01
11.2-t-0.2 11.0_+0.4
55.0_+6.5 24.2_+4.0
45 65
Stim. : Nerve and site stimulated. Ulnar n : Ulnar nerve at the elbow. Post. tib. n : Posterior tibial nerve at the popliteal fossa. Record : Position of the recording electrode. Distance : Distance between recording and stimulating electrodes. * Means and standard errors of each component are calculated in three sequentially averaged ESEGs of 50 responses.
2~uV
E~
E~ L~
[)
IO~JV
Io~ug
distances between stimulating and recording electrodes. On the other hand, the ESEG, recorded with an electrode located antero-laterally in the intrathecal space, showed different patterns. The polarity of the early deflections in the intrathecal recording was inverted against that in the epidural recording (Fig. 2). The ESEG from a remote upper segment rostral to those directly activated by somatosensory stimulus, the "conducted" ESEG, consisted of a small, sharp deflection (S 1wave) Fig. 3, A, B). The ESEG in response to the direct stimulation of the spinal cord epidurally built up a potential pattern (Fig. 3, C) similar to that evoked by peripheral stimulation. The conduction velocity along the spinal cord was approximately 57 m/sec in ascending and 32 m/sec in descending volleys, calculated from the peak latencies and the distance between stimulating and recording electrodes. Total suppression of the epidural recording cephalad to the C2 level supported the clinical signs of quadriplegia (Fig. 3, D). DISCUSSION
r)
'
~
N,
IO~V
Fig. 3. The ESEGs recorded under complete neuromuscular block by the administration of Pancuronium (6 mg), monitored by the EEMG. Three series of averaged responses (N=50) were superimposed in each recording. Sweep duration is 204.8 msec in all records except that in left C and right D (102.4 msec). A: The "conducted" ESEG (S 1 wave), in response to left (left in the figure) and right (right in the figure) posterior tibial nerve stimulations (40 V). B: Simultaneous recordings of the "segmental" (upper traces) and the "'conducted" ESEGs (lower traces) in response to left posterior tibial nerve stimulation (25 V). C: The ESEGs evoked by direct stimulation of the spinal cord epidurally. Left: Recording from cervical level (E2, E3) by stimulation of lower spinal cord with E4 (cathode) and E 6 electrodes (10 V). Right: Recording from lower spinal cord intrathecally (Es) and epidurally (E6) in response to the stimulation of upper spinal cord with E 2 (cathode) and E3 electrodes (10 V). D : The recording from the C 2 and C7 levels in response to the stimulation of left ulnar nerve (left) and of the lower spinal cord with E 4 and E 6 electrodes (right).
The fundamental pattern of the epidural ESEG in this quadriplegic patient has been shown to be similar to that in normal subjects described in a previous paper (Shimoji et al. 1972). Magladery et al. (1951) recorded the ESEG in volunteers with electrodes inserted intrathecally. However, they could not confirm the location of the intrathecal electrodes. In reference to the "segmental" ESEG recorded from the dorsal epidural space in the present study, it is presumed that they recorded the "S-waves" from the dorsal part of the spinal cord. The similarity of the fundamental pattern of the "segmental" ESEGs between normal and quadriplegic man indicates that the origin of the potentials is a local phenomenon rather than a more central influence. The ESEG pattern recorded with an electrode located antero-laterally to the spinal cord in the present study is identical to that in the spinal cat, as described by Hughes et al. (1937). The recording of the ESEG might be valuable in detecting a functional block of a spinal pathway. However, it needs further study to ascertain cord function in terms of detecting spinal cord diseases by recording the ESEG.
K. SHIMOJI et al.
662 SUMMARY The somatosensory evoked spinal electrogram (ESEG) was recorded from the dorsal epidural space and from anterior intrathecal space in a quadriplegic patient. The "segmental" ESEG, recorded intrathecally from the antero-lateral surface of the cord, showed deflections with reversed polarity to those recorded from the dorsal epidural space. The ESEG evoked by the direct stimulation of the spinal cord showed a similar pattern to that evoked by peripheral nerve stimulation. Thus, the ESEG in this quadriplegic patient showed a pattern similar to that in the normal subject. RESUME ELECTROGRAMME SPINAL EVOQUE CHEZ UN MALADE QUADRIPLEGIQUE L'electrogramme somato-sensitif spinal 6voqu6 (ESEG) est enregistr6 au niveau de l'espace 6pidural dorsal et de l'espace intrath6cal ant6rieur chez un malade quadripl6gique. Le ESEG "'s6quentiel'" de la surface ant6ro-lat6rale de la moelle, enregistr6 dans l'espace intrath6cal montre des d6flexions de polarit6 inverse ~ celles de I'ESEG enregistr6 au niveau de l'espace 6pidural dorsal.
Le ESEG 6voqu6 par stimulation directe de la moelle montre un pattern similaire au ESEG 6voqu6 par stimulation nerveuse p6riph6rique. Ainsi. I'ESEG de ce malade quadripl6gique montre un pattern semblable ~ celui du sujet normal. REFERENCES HUGHES. J., McCOUCH, G. P. and STEWART. W. B. Cord potentials in the spinal cat. Amer. J. Physiol., 1937,
118:415-421. MAGLADERY, J. W., PORTER, W. E., PARK, A. M. and TEASDALL, R. D. Electrophysiological studies of nerve and reflex activity in normal man. IV. The two-neuron reflex and identification of certain action potentials tYom spinal roots and cord. Bull. Johns Hopk. Hosp.. 1951, 88 : 499-519. SHIMOJ1, K., HIGASHI, H. and KANO. T. Epidural recording of spinal electrogram in man. Electroenceph. olin. Neurophysiol., 1971, 30: 23(~239. SHIMOJI, K., KANO, T. HIGASHI, H., MORIOKA, T. and HENSCHEL, E. O. Evoked spinal electrograms recorded from epidural space in man. J. appl. Physiol.. 1972. 33: 468471.
Electroencephalography and Clinical Neurophysiology, 1973, 35:659-662 ,~ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
CLINICAL
NOTE
EVOKED SPINAL ELECTROGRAM I N A QUADRIPLEGIC P A T I E N T 1 KOKI SHIMOJ], TATSUHIKO KANO, TOHRU MORIOKA AND ETSUTARO IKEZONO
Department of Anesthesiology, Tokyo Medical and Dental University, Tokyo, and Department of Anesthesioloqy, Kumamoto University Medical School, Kumamoto (Japan) (Accepted for publication: June 7, 1973)
Recently, we have succeeded in recording the human evoked spinal electrogram (ESEG) from the dorsal epidural space simply and safely (Shimoji et al. 1971), based on the technique of epidural anesthesia, and analyzed it in detail (Shimoji et al. 1972). The present report will describe the patterns of ESEG recorded from both the epidural and intrathecal spaces in a quadriplegic patient.
i This work was supported in part by a Grant from the Japanese Ministry of Education.
MATERIAL AND METHOD A 23-year-old male had a quadriplegia caused by an accident 5 days previous to admission. On admission, physical examinations revealed complete motor paralysis and sensory loss below the level of C 5 with paresis of the diaphragm which caused respiratory insufficiency. X-ray examination disclosed dislocation of the 5th cervical vertebra (Fig. 1, A). For the management of respiratory inadequacy, an intratracheal tube was intubated through a tracheotomized opening and ventilation was assisted or controlled through a cm
~2 E~ C5 E _}S..~."R~ /
2 ~'E3 2
4
cm
8
42
6
8cm
.. -)
~
E
2
4
6
6
8cm
Fig. 1. A: X-ray showing the site of dislocation of the C5 vertebra. B: Drawing with reference to the X-ray, showing the position of electrodes in the epidural space (El, E2, E3, E, and E6), the intrathecal space (Es) and the supraspinous ligaments (reference electrodes, R l for El, E 2 and E3, R 2 for E4, E5 and E6).
K. SHIMOJI et al.
660 volume-preset ventilator arranged to keep PaCO2 at around 40 mmHg. On the 5th day, PO 2, PCO2, pH and base excess in the arterial blood were 76 mmHg, 38 mmHg, 7.460 and + 3.2 mEq/L, respectively. Serum electrolytes were within the normal range (Na 140, K 4.3, CI 116, Ca 4.7 mEq/L). Blood pressure varied between 140/90 and 110/70 mmHg. The condition of the patient remained much the same for 3 weeks after admission except for the gradual increase in spinal reflexes. Thereafter, the general condition of the patient gradually deteriorated. He died of respiratory disturbances on the 49th day after admission. Autopsy revealed vertebral impingement upon the anterior surface of the spinal cord at the C5 level, and cerebral edema. On the 7th and 8th days after admission, recording of the ESEG had been undertaken. Stainless-steel electrodes 150/t in diameter insulated up to 5 mm from the tip, were inserted into the dorsal epidural space at C2, C7, T12, and L 1 levels as shown in Fig. 1, B. The procedures used to introduce the electrodes into the epidural space have been described in detail in a previous paper (Shimoji et al. 1971). One electrode was also introduced into the intrathecal space at the L1 level. The indifferent needle electrode was inserted into the supraspinous ligament of the adjacent segment. Placement of the tips of the electrodes was verified radiologically at the end of recording. Square pulses of 0.5 msec duration and of varying intensities were delivered by the chlorided silver needle electrodes through a stimulator (NIHONKOHDEN MSE-3 i
K
,
i
with an isolation unit, to the ulnar nerve at the elbow or posterior tibial nerve at the popliteal fossa every 1-2 sec. The ESEG in responses to the direct stimulation of the spinal cord by epidural electrodes were also recorded. The rostral part of the spinal cord was stimulated with E2 (cathode) and E 3 (anode) electrodes, and the caudal part of it, with E4 (cathode) and E 6 (anode) electrodes (Fig. 1, B). The ESEG and the evoked electromyogram (EEMG) were led to a polygraph (NIHONKOHDEN RM-150M), and an oscilloscope (NIHONKOHDEN VC-7) and were averaged through a computer (ATAC-501-10). The time constants adopted were 0.3 sec for recording the EEG and SEG, and 0.01 sec for the EEMG. RESULTS The ESEG, recorded from the dorsal epidural space directly activated by somatosensory stimulation (the "segmental" ESEG)consisted of early positive (P a), negative (N1) and positive (Pz) deflections followed by delayed components (Fig. 2). Although P2 and delayed components were sometimes impaired by the EKG artifact, PI and N 1 components were hardly affected by the EKG or other artifacts during the course of averaging. This is shown in Fig. 2 and 3, in which early P1 and N~ deflections remain constant in three series of averaged responses, whereas P2 and delayed components show a relative variability. Peak latencies and durations of these early deflections are shown in Table I with approximate P2
J
SuV
A
/
P2
E6
B E5
N,
[5uV
ii
t 25uV
__llOOuV psec
50msec
Fig. 2. Simultaneous recording from the dorsal epidural space (E6) and from the antero-lateral intrathecal space (Es) of the ESEG in response to electrical stimulation (25 V) of left (A) and right (B) posterior tibial nerves. Left: polygraphic tracing. K : electrocardiogram. Arrows indicate the ESEG noticeable in the polygraphic record. Right : Superimposition of three sequentially averaged series of ESEGs (N = 50). Note the different calibration between the epidural and intrathecal recordings in left B (5#V for the epidural recording; 25 #V for the intrathecal recording). The start of the sweep corresponds to the electrical shocks in this and the following records. Upward deflection denotes positivity in all records. Refer to Fig. I, B, for the position of electrodes.
661
EVOKED SPINAL ELECTROGRAM IN QUADRIPLEGIA TABLE I Peak latencies and durations of the early components in the "segmental" ESEGs. Stim.
Record
Ulnar n Post. tib. n
C7(E3) LI(E6)
Peak latency (msec)
Duration* (msec)
Distance (cm)
P1
Nt
P2
P,
N1
P2
6.5 12.5
13.0 17.5
41.8 35.0
1.8___0.01 2.2_+0.01
11.2-t-0.2 11.0_+0.4
55.0_+6.5 24.2_+4.0
45 65
Stim. : Nerve and site stimulated. Ulnar n : Ulnar nerve at the elbow. Post. tib. n : Posterior tibial nerve at the popliteal fossa. Record : Position of the recording electrode. Distance : Distance between recording and stimulating electrodes. * Means and standard errors of each component are calculated in three sequentially averaged ESEGs of 50 responses.
2~uV
E~
E~ L~
[)
IO~JV
Io~ug
distances between stimulating and recording electrodes. On the other hand, the ESEG, recorded with an electrode located antero-laterally in the intrathecal space, showed different patterns. The polarity of the early deflections in the intrathecal recording was inverted against that in the epidural recording (Fig. 2). The ESEG from a remote upper segment rostral to those directly activated by somatosensory stimulus, the "conducted" ESEG, consisted of a small, sharp deflection (S 1wave) Fig. 3, A, B). The ESEG in response to the direct stimulation of the spinal cord epidurally built up a potential pattern (Fig. 3, C) similar to that evoked by peripheral stimulation. The conduction velocity along the spinal cord was approximately 57 m/sec in ascending and 32 m/sec in descending volleys, calculated from the peak latencies and the distance between stimulating and recording electrodes. Total suppression of the epidural recording cephalad to the C2 level supported the clinical signs of quadriplegia (Fig. 3, D). DISCUSSION
r)
'
~
N,
IO~V
Fig. 3. The ESEGs recorded under complete neuromuscular block by the administration of Pancuronium (6 mg), monitored by the EEMG. Three series of averaged responses (N=50) were superimposed in each recording. Sweep duration is 204.8 msec in all records except that in left C and right D (102.4 msec). A: The "conducted" ESEG (S 1 wave), in response to left (left in the figure) and right (right in the figure) posterior tibial nerve stimulations (40 V). B: Simultaneous recordings of the "segmental" (upper traces) and the "'conducted" ESEGs (lower traces) in response to left posterior tibial nerve stimulation (25 V). C: The ESEGs evoked by direct stimulation of the spinal cord epidurally. Left: Recording from cervical level (E2, E3) by stimulation of lower spinal cord with E4 (cathode) and E 6 electrodes (10 V). Right: Recording from lower spinal cord intrathecally (Es) and epidurally (E6) in response to the stimulation of upper spinal cord with E 2 (cathode) and E3 electrodes (10 V). D : The recording from the C 2 and C7 levels in response to the stimulation of left ulnar nerve (left) and of the lower spinal cord with E 4 and E 6 electrodes (right).
The fundamental pattern of the epidural ESEG in this quadriplegic patient has been shown to be similar to that in normal subjects described in a previous paper (Shimoji et al. 1972). Magladery et al. (1951) recorded the ESEG in volunteers with electrodes inserted intrathecally. However, they could not confirm the location of the intrathecal electrodes. In reference to the "segmental" ESEG recorded from the dorsal epidural space in the present study, it is presumed that they recorded the "S-waves" from the dorsal part of the spinal cord. The similarity of the fundamental pattern of the "segmental" ESEGs between normal and quadriplegic man indicates that the origin of the potentials is a local phenomenon rather than a more central influence. The ESEG pattern recorded with an electrode located antero-laterally to the spinal cord in the present study is identical to that in the spinal cat, as described by Hughes et al. (1937). The recording of the ESEG might be valuable in detecting a functional block of a spinal pathway. However, it needs further study to ascertain cord function in terms of detecting spinal cord diseases by recording the ESEG.
K. SHIMOJI et al.
662 SUMMARY The somatosensory evoked spinal electrogram (ESEG) was recorded from the dorsal epidural space and from anterior intrathecal space in a quadriplegic patient. The "segmental" ESEG, recorded intrathecally from the antero-lateral surface of the cord, showed deflections with reversed polarity to those recorded from the dorsal epidural space. The ESEG evoked by the direct stimulation of the spinal cord showed a similar pattern to that evoked by peripheral nerve stimulation. Thus, the ESEG in this quadriplegic patient showed a pattern similar to that in the normal subject. RESUME ELECTROGRAMME SPINAL EVOQUE CHEZ UN MALADE QUADRIPLEGIQUE L'electrogramme somato-sensitif spinal 6voqu6 (ESEG) est enregistr6 au niveau de l'espace 6pidural dorsal et de l'espace intrath6cal ant6rieur chez un malade quadripl6gique. Le ESEG "'s6quentiel'" de la surface ant6ro-lat6rale de la moelle, enregistr6 dans l'espace intrath6cal montre des d6flexions de polarit6 inverse ~ celles de I'ESEG enregistr6 au niveau de l'espace 6pidural dorsal.
Le ESEG 6voqu6 par stimulation directe de la moelle montre un pattern similaire au ESEG 6voqu6 par stimulation nerveuse p6riph6rique. Ainsi. I'ESEG de ce malade quadripl6gique montre un pattern semblable ~ celui du sujet normal. REFERENCES HUGHES. J., McCOUCH, G. P. and STEWART. W. B. Cord potentials in the spinal cat. Amer. J. Physiol., 1937,
118:415-421. MAGLADERY, J. W., PORTER, W. E., PARK, A. M. and TEASDALL, R. D. Electrophysiological studies of nerve and reflex activity in normal man. IV. The two-neuron reflex and identification of certain action potentials tYom spinal roots and cord. Bull. Johns Hopk. Hosp.. 1951, 88 : 499-519. SHIMOJ1, K., HIGASHI, H. and KANO. T. Epidural recording of spinal electrogram in man. Electroenceph. olin. Neurophysiol., 1971, 30: 23(~239. SHIMOJI, K., KANO, T. HIGASHI, H., MORIOKA, T. and HENSCHEL, E. O. Evoked spinal electrograms recorded from epidural space in man. J. appl. Physiol.. 1972. 33: 468471.