Somatosensory evoked potentials during reversible spinal cord ischemia in man

Electroencephalographv and climcal Neurophvstoh~v, 1984, 58:120-126

120

Elsevier Scientific Publishers Ireland, Ltd.

S O M A T O S E N S O R Y EVOKED P O T E N T I A L S D U R I N G R E V E R S I B L E S P I N A L C O R D | S C H E M I A IN MAN t E L I M. M I Z R A H I

..2 a n d E. S T A N L E Y C R A W F O R D

Departments of * Neurology (Section of Neurophysiology) Houston, TX 77030 (U.S.A.)

**

and ** Surgery. B~o'lor College of Medicine, and The Methodist tlo~'pital,

(Accepted for publication: January 17. 1984)

During surgery to prevent the catastrophic consequences of aneurysms of the descending aorta, the aorta is completely occluded at a level distal to the left subclavian artery (Crawford et al. 1981). This occlusion interrupts circulation to the anterior spinal artery, which is supplied by intercostal arteries originating in the aorta, and thus creates a significant risk of postoperative paraplegia (Crawford et al. 1978, 1981). The characterization and determination of the clinical significance of changes in the somatosensory evoked potential (SEP) produced by progressive, but reversible, ischemia to the spinal cord may provide a basis for minimizing neurological sequelae. This report describes an initial experience in continuous recording of the SEP during interruption and then restoration of blood flow to the spinal cord in man. Material and Methods

Subjects Thirteen patients who had aneurysms of the descending aorta that required replacement were studied; their ages ranged from 23 to 74 years. Eight had thoracico-abdominal aneurysms and were at relatively high risk for postoperative paraplegia. One patient had both thoracic and abdominal aneurysms, one had only an abdominal aneurysm, and the remainder had thoracic aneurysms. All patients were given neurological 1 Supported in part by USPHS Grant No. RR-05424. 2 Address reprint requests to Dr. Mizrahi at Department of Neurology, Section of Neurophysiology, Baylor College of Medicine, 1200 Moursund Avenue, Houston, TX 77030, U.S.A.

examinations (by E.M.M.) before and after surgery. Informed consent was obtained from each patient following a full explanation of the monitoring procedure.

Surgical procedure After the descending aorta was exposed, the anatomical limits of the aneurysm were defined, and clamps were applied across the aorta at the distal and proximal aspects of the abnormality. Thus, aortic blood flow was completely occluded. The level of clamping above the aneurysm varied from just caudal to the left subclavian artery to the diaphragm. Blood was suctioned from the confined aneurysm, and that segment of aorta was removed. Patent intercostal or lumbar arteries originating in the aorta were preserved during removal of the aneurysms, as were the celiac, superior mesenteric, and renal arteries. The removed segment of aorta was replaced by a woven Dacron graft, and the preserved arteries that originated in the diseased aorta were reattached to the graft. The clamps were then removed, restoring circulation through the descending aorta. This procedure has been described in detail by Crawford et al. (1982).

SEP recording techniques Responses were obtained with a sensory evoked potential system. Stimuli 0.1 msec in duration and up to 300 V in intensity were delivered at a rate of 4.9 Hz through a pair of electrodes placed in the left popliteal fossa over the peroneal nerve. Cephalic responses were obtained from a scalp electrode placed 2 cm posterior to C z (international

0013-4649/84/$03.00 '~ 1984 Elsevier Scientific Publishers Ireland, Ltd.

SEPs DURING REVERSIBLE SPINAL CORD ISCHEMIA

12l

e l e c t r o d e p l a c e m e n t system) a n d 2 cm lateral to the m i d l i n e over the region of the p o s t c e n t r a l gyrus and referred to an electrode on the forehead. T h e l u m b a r response was r e c o r d e d from one elect r o d e placed over the third l u m b a r v e r t e b r a (L3) a n d one over the right iliac crest. All recording a n d s t i m u l a t i n g electrodes were a p p l i e d with coll o d i o n a n d filled with a c o n d u c t i v e paste; i m p e d ance was m a i n t a i n e d at below 5000 ~2. R e s p o n s e s were filtered with a b a n d p a s s of 5 - 3 0 0 0 Hz. The e p o c h of r e c o r d i n g after each stimulus ranged from 75 to 100 msec. Each trial was d i s p l a y e d on a 9 in. television m o n i t o r as the response was obtained, a n d 300 responses were averaged for each trial. Averages were stored on f l o p p y discs for later detailed analysis.

arteries and the time of u n c l a m p i n g of the a o r t a a n d restoration of circulation were noted. In a d d i tion, b l o o d pressure, core b o d y temperature, a n d a d m i n i s t r a t i o n of m e d i c a t i o n s were r e c o r d e d and d i d not vary significantly after SEP recording began. SEP m o n i t o r i n g c o n t i n u e d for 3 0 - 1 6 0 rain after restoration of circulation.

Data analysis In a d d i t i o n to online analysis d u r i n g surgery, the response for each trial was e x a m i n e d in detail after the r e c o r d i n g period. T h e wave form was d i s p l a y e d on the c o m p u t e r - t e r m i n a l monitor. The negative a n d positive peaks of the cephalic and l u m b a r responses were identified, a n d their latencies and a m p l i t u d e s were m e a s u r e d through an interactive p r o g r a m .

Intraoperative monitoring protocol A f t e r i n d u c t i o n of anesthesia ( F e n t a n y l ) , positioning of the patient, a n d initiation of the surgical p r o c e d u r e , 10 consecutive SEP trials were r e c o r d e d to establish baseline cephalic a n d l u m b a r responses. T h e earliest negative wave form that could be identified consistently in the cephalic r e c o r d i n g was selected as the response to m o n i t o r i n t r a o p e r atively. T h e time of aortic c r o s s - c l a m p i n g was recorded, a n d one SEP trial was o b t a i n e d every 90 sec t h r o u g h o u t surgery. The time, n u m b e r , and l o c a t i o n of r e a n a s t o m o s e s of intercostal or l u m b a r

Results

The d u r a t i o n of aortic occlusion ranged from 18 to 87 min (Table I). T y p i c a l responses of the cephalic SEP to aortic occlusion are shown in detail in Figs. 1 and 2. T h e r e was a g r a d u a l p r o l o n g a t i o n of l a t e n c y a n d d i m i n u t i o n of a m p l i tude after aortic occlusion in all patients, a n d in 10 patients, the SEP eventually b e c a m e non-recordable. W i t h r e s t o r a t i o n of circulation, the re-

TABLE I Clinical and operative findings. Patient

Age (years)

Site of aneurysm

Site of aortic clamp

No. of lumbar intercostal reattachments

Clamp time (min)

A B C D E F G H

23 34 69 74 45 60 67 55 55 70 50 62 51

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L. subclavian L. subclavian L. subclavian L. subclavian Midthoracic + diaphragm L. subclavian Diaphragm Midthoracic L. subclavian Midthoracic L. subclavian L. subclavian L. subclavian

1 2 3 1 5 1 2

18 24 24 26 29 46 47 49 57 59 68 69 87

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Fig. 1: Below: complete cross-clamping of the aorta produced a gradual prolongation of latency and diminution of amplitude of the SEP. The response eventually was non-recordable but rapidly returned and improved when the clamp was removed. Above: superimposed consecutive trials of selected cephalic responses are shown at various times following clamping. Letters ( A - D ) of each response in the figure above correspond to the letters in the graph below, indicating when each response was obtained.

sponse returned rapidly and gradually improved in latency and amplitude. The initial latency prolongation was seen within 10 rain of clamping in all patients. All SEPs that had eventually become non-recordable returned within 2 rain of restoration of circulation. The absolute latency of the lumbar response remained constant, while the cephalic response underwent changes. Thus, the change in the absolute latency of the cephalic SEP paralleled the change in the lumbar-cephalic interpeak latency (Fig. 3). While the initial prolongation of latency was directly related to the duration of the occlusion, not all patients had complete loss of the response. In the 3 patients with preservation of the SEP, clamp time was 18-24 min. In the 10 patients with eventually non-recordable SEPs, the responses were

Fig. 2. In this patient, the latency of all major cortical waves increased in parallel after aortic occlusion and improved similarly with restoration of blood flow.

lost between 17 and 40 min of occlusion. In these patients, total clamp time was 26-87 min (Fig. 4). In 12 patients, the aorta was occluded once during surgery. In two of these, the latency of the SEP returned to the preocclusion baseline level within 30 min after restoration of blood flow. In general, the degree of abnormality at 30 min after unclamping appeared related to the duration of the occlusion and to the duration of the absence of the response (Fig. 5). In the patient with both thoracic and abdominal aneurysms, aortic occlusion was performed, first, just distal to the left subclavian artery, and then below the diaphragm. Each occlusion produced similar changes in the lumbar-cephalic interpeak latency (Fig. 3). Thus, the changes in SEPs did not appear related to the site of the aneurysm or to the location of aortic clamping. Although all patients had normal neurological examinations preoperatively, one had findings typical of anterior spinal artery syndrome after surgery. This patient required the most extensive aortic replacement and had the longest period of

SEPs DURING REVERSIBLE SPINAl, CORD ISCHEMIA

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Fig. 3. In this patient, who had both thoracic and abdominal aneurysms, cross-clamping was performed, first, distal to the left subclavian artery, and then below the diaphragm. In both instances, the changes in cephalic and lumbar responses were similar. The lumbar response remained relatively constant during both periods of occlusion, while the cephalic response changed in a characteristic manner. Calibration A F: 6 msec per division; 1 /*V full scale.

occlusion (87 min) and of n o n - r e c o r d a b l e SEPs (59 rain).

Discussion The initial task in correlating neurological outc o m e with i n t r a o p e r a t i v e SEP changes entails rec o r d i n g of the n e u r o p h y s i o l o g i c a l consequences of spinal cord ischemia. In our study, the observations m a d e d u r i n g c o m p l e t e occlusion of the aorta a n d the s u b s e q u e n t restoration of blood flow allow it p r e l i m i n a r y c h a r a c t e r i z a t i o n to be m a d e of tile response of the SEP to spinal cord ischemia in the

i n t r a o p e r a t i v e setting. This characterization, which m a y eventually p r o v i d e the basis for d e t e r m i n i n g the clinical significance of i n t r a o p e r a t i v e SEP changes in future investigations, includes: (1) progressive latency p r o l o n g a t i o n within the first 10 rain of occlusion, (2) coincident and progressive a m p l i t u d e depression, (3) eventual loss of the SEP, (4) rapid reversal of these changes with restoration of circulation, and (5) preservation of the l u m b a r response when the cephalic response becomes a b n o r m a l . The degree of p r o l o n g a t i o n of latency at 30 min after restoration of blood flow a p p e a r s related to the d u r a t i o n of aortic occlusion and to tile d u r a t i o n of absent SEPs. These findings indi-

124

E.M. MIZRAHI, E.S. CRAWFORD

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Fig. 5. The degree of persistent latency prolongation 30 min after restoration of circulation is expressed as per cent of control latency [(msec of latency 30 min after unclamping/msec of initial latency) ×100] and appears to be related to the total time of ischemia (coefficient of correlation 0.899; standard error of estimate = 4.092) and to the duration of the absence of SEPs (coefficient of correlation = 0.819; standard error of estimate = 5.372). Calculated linear regression is shown for both.

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Fig. 4. Prolongation of latency was noted in all patients within 10 rain of aortic occlusion. In 10 cases, SEPs eventually became non-recordable. In these patients, restoration of circulation resulted in the reappearance of the response and progressive shortening of latency. Not all responses returned to normal during the testing session. Patient M was paraplegic after surgery. Patient E had two periods of occlusion; changes produced by the first clamping are shown. All numbers refer to time from initial aortic clamping (min).

care that c o n d u c t i o n through the spinal p a t h w a y s that m e d i a t e SEPs is sensitive to ischemia p r o d u c e d b y aortic occlusion. Early investigators d e t e r m i n e d the histological a n d clinical effects of spinal c o r d ischemia by ligating the d e s c e n d i n g a o r t a in a n i m a l s (Tureen 1936). M o r e recent a n i m a l studies c h a r a c t e r i z e d the consequences of spinal c o r d ischemia b y rec o r d i n g n e u r o p h y s i o l o g i c a l events ( G e l f a n a n d

T a r l o v 1955; K o b r i n e et al. 1978, 1980; Coles et al. 1982). Coles et al. (1982) m a d e serial measurem e n t s of SEPs in dogs in an e x p e r i m e n t designed to d u p l i c a t e the surgery p e r f o r m e d in m a n for extensive aortic replacement. T h e y n o t e d a timerelated d e t e r i o r a t i o n of the SEP a n d eventual loss of the response after 12 min of c o m p l e t e occlusion of the d e s c e n d i n g aorta. F o u r of 6 animals with p r o l o n g e d loss of SEPs were n e u r o l o g i c a l l y a b n o r m a l after reperfusion, whereas all were normal if reperfusion was established when substantial SEP a t t e n u a t i o n was first evident. Based u p o n these and other e x p e r i m e n t s (Coles et al. 1983) it was suggested that early recognition of spinal cord ischemia, using c o n t i n u o u s SEP m e a s u r e m e n t , w o u l d allow the o p p o r t u n i t y for rational surgical i n t e r v e n t i o n to enhance spinal cord perfusion during o p e r a t i o n s on the thoracic a o r t a in man. Using a similar e x p e r i m e n t a l model, Laschinger et al. (1982) c o n c l u d e d that i n t r a o p e r a t i v e SEP m o n i t o r ing is a highly sensitive, reliable i n d i c a t o r of spinal c o r d b l o o d flow. T h e r e has been limited a p p l i c a t i o n of i n t r a o p e r ative SEP m o n i t o r i n g in h u m a n s requiring aortic occlusion. C u n n i n g h a m et al. (1982) m o n i t o r e d SEPs in 7 p a t i e n t s during surgery involving the d e s c e n d i n g a o r t a for either c o a r c t a t i o n or thoracic o r t h o r a c i c o - a b d o m i n a l aneurysms. In 2 patients, SEP latency a n d a m p l i t u d e changes were n o t e d

SEPs D U R I N G REVERSIBLE SPINAL C O R D ISCHEMIA

within 4 min of aortic occlusion. Complete loss of the response occurred at 8 min after occlusion and returned 40 min after restoration of flow. SEP changes were prevented in 4 patients by either a heparinized shunt, femoral bypass, or intercostal artery reimplantation. These maneuvers were performed to enhance distal perfusion of the spinal cord during surgery. None of these patients had neurological deficits postoperatively. These investigators suggested that shunting procedures to ensure adequate distal aortic perfusion should be performed as necessary adjuncts to obtaining accurate SEP measurements during aortic interruption for surgery of the thoracico-abdominal aorta. It was suggested that changes in the SEP can provide data that may allow the surgeon to alter the operation to prevent postoperative neurological sequelae related to spinal cord ischemia. There is currently much enthusiasm for, and success with, continuous SEP monitoring during surgery of the spinal cord and vertebral column (Grundy 1982; Lueders et al. 1982). However, it is still unknown whether procedures to maintain normal SEPs during extensive aortic replacement will prevent postoperative paraplegia, since the relationship of intraoperative SEP changes to the occurrence and degree of postoperative neurological sequelae has not been established. In the study by Coles et al. (1982), for example, 2 of the 6 animals with prolonged intraoperative absence of SEPs were clinically normal after surgery. None of the patients studied by Cunningham et al. (1982) were neurologically abnormal after surgery, but only one had a thoracico-abdominal aneurysm and was therefore the only patient at significant risk for postoperative paraplegia. In the study reported here, the patient with the longest period of absent SEPs and aortic occlusion was the only patient with postoperative paraplegia. However, no significant conclusion can be drawn from this finding because of the small number of patients in our preliminary investigation. In addition to the limited animal and human data, other considerations make it difficult to correlate SEP changes with clinical outcome. For example, patients with anterior spinal artery syndrome, such as that produced by extensive aortic replacement, may have normal clinical SEPs be-

125

cause of the relative preservation of the dorsal column (Dorfman et al. 1980). The rationale for SEP monitoring during aortic replacement is based on the assumption that dorsal column function cannot be altered by ischemia produced by aortic occlusion unless the remainder of the spinal cord is also affected. However, it is not clear whether the tolerance of motor tracts to ischemia can be determined by monitoring dorsal column function. Intraoperative monitoring of the effects of ischemia on the spinal cord could be of importance in discovering factors critical to the preservation of normal cord function and could provide the basis for devising new surgical and medical regimens to prevent neurological complications if the clinical significance of intraoperative SEP changes is established. Further investigation may prove this monitoring technique to be of value in reducing the neurological morbidity of extensive aortic replacement.

Summary. Somatosensory evoked potentials (SEPs) from peroneal nerve were recorded continuously on 13 patients undergoing extensive aortic replacement of thoracic, abdominal, or thoracico-abdominal aneurysms. During this surgical procedure, the descending aorta is completely occluded, and circulation to the spinal cord may thus be compromised, causing a risk of postoperative paraplegia. This risk may be minimized if changes in the SEP seen during intraoperative monitoring prove to correlate well with clinical outcome. Changes in the SEP observed during complete occlusion of the aorta and subsequent restoration of blood flow included: (1) progressive latency prolongation within the first 10 min of occlusion, (2) coincident and progressive amplitude depression, (3) eventual loss of the SEP, (4) rapid reversal of these changes with restoration of circulation, and (5) preservation of the lumbar response when the cephalic response became abnormal. The degree of prolongation of latency after restoration of blood flow appeared related to the duration of aortic occlusion and to the duration of SEP abscnce. These findings indicate that conduction

126

through the spinal pathways that mediate the SEP is sensitive to ischemia produced by aortic occlusion. Intraoperative monitoring of SEPs as a means of reducing the neurological morbidity of extensive aortic replacement is discussed.

R~sume Potentiels bvoqubs sornatosensoriels au cours d'une

ischbmie spinale rkversible chez l'homme

Les potentiels 6voquds somatosensoriels (PES) du nerf pdrondal ont 6tO enregistres en continu chez 13 patients subissant une importante correction aortique d'un anevrisme thoracique, abdominal ou thoraco-abdominal. Au cours de l'opdration chirurgicale, l'aorte descendante est totalement obturee et la circulation spinale peut ainsi dtre perturbde, entra]nant un risque de paraplegie post-operatoire. Ce risque peut dtre miniraise si les modifications des PES, suivies au cours de l'operation se revelent bien liees aux consequences cliniques. Les modifications des PES observdes au cours d'une occlusion complete de l'aorte suivie d'une restauration subsdquente de la circulation sont: (1) une augmentation progressive de la latence au cours des 10 premieres minutes de l'obturation, (2) une diminution concourrante et progressive de l'amplitude, (3) une 6ventuelle perte du PES, (4) une rapide disparition de ces modifications avec la restauration de la circulation, et (5) la conservation de la reponse lombaire lorsque la reponse cephalique est devenue anormale. Le degre d'augmentation de latence awes restauration de la circulation a semble lid ~_ la duree de l'occlusion aortique et ~_ la durde de la pdriode sans PES. Ces rdsultats indiquent que la conduction dans les votes spinales responsables du PES est sensible ~ l'ischemie produite par obturation aortique. La surveillance peropdratoire des PES comme moyen de reduire les suites neurologiques d'une pose de prothese importante de l'aorte est discutee. The technical assistance of Adrian DeGuire, R.EEG T., and Suzanne Moore, B.A., is gratefully acknowledged.

E.M. MIZRAHI, E.S. CRAWFORD

References Coles, J.G., Wilson, G.J., Sima, A.F., Klement, P. and Tait, G.A. Intraoperative detection of spinal cord ischemia using somatosensory cortical evoked potentials during thoracic occlusion. Ann. thorac. Surg., 1982, 34:299 306. Coles, J+G., Wilson, G.J., Sima, A.F, Klement, P., Tait, G.A., Williams, W.G. and Baird, R.J. Intraoperative management of thoracic aortic aneurysm: experimental evaluation of perfusion cooling of the spinal cord. J. thorac, cardiovasc. Surg., 1983, 85:292 299. Crawford+ E.S., Snyder, D.M., Cho, (,;-.C. and Roehm, Jr., J.O.F. Progress in treatment of thoracoabdominal and abdominal aneurysms involving celiac, superior mesenteric, and renal arteries. Ann. Surg., 1978, 188: 404-422. Crawford+ E.S., Waler, H.S., Saleh, S.A. and Normann+ N.A. Graft replacement of aneurysm in descending thoracic aorta: results with and without bypass or shunting. Surgery, 1981, 89:73 85+ Crawford, E.S+, Snyder, D.M. and Graham, J.M. Aneurysm of the descending thoracic aorta. In: L.H. Cohen (Ed.), Modern Techniques in Surgery: Cardiac/Thoracic Surgery. Futura, New York, 1982: 47/3-47/29. Cunningham, Jr., J.N., Laschinger, J.C., Merkin, H.A., Nathan, I.M., Colvin, S., Ransohoff, J. and Spencer, F.C. Measurement of spinal cord ischemia during operations upon the thoracic aorta. Ann. Surg., 1982, 196: 285-296. Dorfman, L.J., Perkash, 1., Bosley, T.M. and Cummins, K.L. Use of cerebral evoked potentials to evaluate spinal somatosensory function in patients with traumatic and surgical myelopathies. J. Neurosurg., 1980, 52: 654-660. Gelfan, S. and Tarlov, l.M. Differential vulnerability of spinal cord structures to anoxia. J. Neurophysiol., 1955, 18: 170-188. Grundy, B.L+ Monitoring of sensory evoked potentials during neurosurgical operations: methods and applications. Neurosurgery, 1982, 11: 556-575. Kobrine, A.I., Evans, D.E. and Rizzoli, H.V. Correlation of spinal cord blood flow and function in experimental compression. Surg. Neurol., 1978, 10: 54-59. Kobrine, A.I., Evans, D.E. and Rizzoli, H.V. Relative vulnerability of the brain and spinal cord to ischemia. J. neurol. Sci., 1980, 45:65 72. Laschinger, J.C., Cunningham, J.N., Cadnella, F.P., Nathan, I.M., Knopp, E.A. and Spencer, F.C. Detection and prevention of intraoperative spinal cord ischemia after crossclamping of the thoracic aorta: use of somatosensory evoked potentials. Surgery, 1982, 92:1109 1117. Lueders, H., Gurd, A., Hahn, J., Andrish, J.+ Weiker, G. and Klem, G. A new technique for intraoperative monitoring of spinal cord function: multichannel recording of spinal cord and subcortical evoked potentials. Spine, 1982, 7: 110-115. Tureen, L.L. Effect of experimental temporary vascular occlusion on the spinal cord: correlation between structural and functional changes. Arch. Neurol. Psychiat. (Chic.), 1936, 35: 789-807.