HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Kazutomo Goh Norihiko Shiiya Keishu Yasuda Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Matsui, Y. Articles by Tanabe, T. Search for Related Content PubMed PubMed Citation Articles by Matsui, Y. Articles by Tanabe, T.

J Thorac Cardiovasc Surg 1994;107:1519-1527
© 1994 Mosby, Inc.

CARDIOPULMONARY BYPASS, MYOCARDIAL MANAGEMENT, AND SUPPORT TECHNIQUES

Clinical application of evoked spinal cord potentials elicited by direct stimulation of the cord during temporary occlusion of the thoracic aorta

Hokkaido, Japan

From the Department of Cardiovascular Surgery and Second Department of Surgery, Hokkaido University of Medicine, Hokkaido, Japan.

Received for publication March 25, 1993. Accepted for publication Nov. 2, 1993. Address for reprints: Yoshiro Matsui, MD, Department of Cardiovascular Surgery, Hokkaido University of Medicine, Kita-14, Nishi-5, Kita-ku, Sapporo, Hokkaido, Japan.

Abstract

Evoked spinal cord potentials elicited by direct stimulation of the cord were used to monitor spinal cord ischemia in 68 patients undergoing temporary occlusion of the thoracic aorta (29 thoracic nondissecting aortic aneurysms, 9 nondissecting thoracoabdominal aneurysms, and 30 dissecting aneurysms). "Immediate" postoperative paraplegia developed in three patients and "immediate" paraparesis developed in one, whereas "delayed" paraplegia developed in two others. During aortic crossclamping, four response patterns of the spinal cord potentials were obtained: (1) no change ( n = 53), (2) change with return ( n = 10), (3) change with inconsistent return ( n = 2), and (4) change without return ( n = 3). Neurologic complications occurred in 2%, 0%, 100%, and 100% of these groups, respectively. Delayed paraplegia developed on the second postoperative day in only one patient with a false-negative result, and the potentials correlated well with this patient's clinical neurologic recovery. The aortic crossclamp time was significantly longer in the patients with "change with inconsistent return" and "change without return" than in the other two groups ( p < 0.01). Femoral artery pressure and the cardiopulmonary bypass flow rate were also significantly lower in these groups than in the other two groups ( p < 0.02 and p < 0.01, respectively). We conclude that intraoperative monitoring of direct spinal cord responses is useful for the early detection of spinal cord ischemia for assessing the efficacy of surgical countermeasures. (J THORAC CARDIOVASC SURG 1994;107:1519-27)

Paraplegia is a severe and disastrous complication of operations on the thoracic aorta, and its prevalence after such operations has been reported to range from 0% to 23%. ^1-8 Many authors have discussed procedures for the prevention of spinal cord injury during aortic crossclamping. ^9-14 However, all the methods proposed are controversial, and it remains difficult to predict this complication before or during the operation.

After the introduction of spinal cord monitoring during aortic crossclamping by Cunningham and Laschinger, somatosensory cortical evoked potentials (SEPs) elicited by peripheral nerve stimulation have been widely used to directly monitor spinal cord function. ^15-21 However, SEPs only reflect sensory function, and relatively high false-positive and false-negative response rates have been reported in both clinical and experimental studies. ^21,22 In addition, SEPs are easily influenced by electrical noise or anesthesia and especially by peripheral nerve dysfunction resulting from ischemia. ^22,23

For these reasons, the use of motor evoked potentials (MEPs) or evoked spinal cord potentials elicited by direct stimulation of the cord (ESPs-dsc) has been proposed recently. ^22-30 The aim of this study was to evaluate the efficacy of ESPs-dsc monitoring for the prevention of spinal cord ischemia during aortic crossclamping and for the selection of intraoperative countermeasures in patients undergoing thoracic and thoracoabdominal aortic operations.

PATIENTS AND METHODS

Patient selection
The ESPs-dsc method was used to monitor spinal cord ischemia during operations on 68 patients with various aortic lesions. There were 29 cases of nondis secting thoracic aortic aneurysm, 9 cases of nondissecting thoracoabdominal aneurysm, and 30 cases of dissecting aneurysm (DeBakey type III). The dissecting and nondissecting thoracoabdominal aneurysms were divided into four types according to the classification of Crawford and associates, ²¹ because of the considerable variation in neurologic risk and surgical factors between each type. Aneurysms involving the descending thoracic aorta and the upper abdominal aorta were classified as type I, those involving the entire descending thoracic aorta and most of the abdominal aorta were type II, those involving less than half of the descending thoracic aorta and most of the abdominal aorta were type III, and those mostly confined to the abdominal aorta were type IV.

Forty-eight operative procedures used the graft inclusion technique with Dacron fabric tube grafts. The other operative techniques used included 3 patch aortoplasties, 11 entry closures for dissecting aneurysms, and 6 extraanatomic permanent bypasses. In the 17 graft or entry closure procedures that were done for dissecting aneurysms, pieces of Ivalon sponge (Ivalon, Inc., San Diego, Calif.) were placed into dissected lumen to promote early thrombus formation. ³¹ All the patients had some form of temporary or permanent shunt, cardiopulmonary bypass, or left heart bypass as a circulatory adjunct during aortic crossclamping.

Patients who died during the operation and those with preexisting neurologic deficits were excluded from this study.

Recording of ESPs-dsc
ESPs-dsc were generated by electric stimulation with a tube-shaped bipolar electrode with two platinum tips that protruded through the end of an 18-gauge polyethylene tube that was inserted in the epidural space at the twelfth thoracic to first lumbar vertebral levels and were recorded with bipolar electrodes inserted into the epidural space at the seventh cervical to first thoracic vertebral levels (Fig. 1). The electrodes were usually inserted through 15-gauge Tuohy needles (Portex Ltd., Hythe Kent, England) on the day before the operation. An MS-91 apparatus (Medelec Ltd., Surrey, England) was used for both production and recording of ESPs-dsc. Square-wave pulses of 0.05 msec in duration and supramaximal intensity (10 to 20 mA) were generated at a rate of 10 to 20 per second. The recorded signals were passed through low- and high-frequency filters (20 and 2000 Hz, respectively) and were averaged 5 to 20 times to eliminate electric noise. Baseline measurement of ESPs-dsc was done before aortic crossclamping, and the potentials were also recorded throughout aortic crossclamping and after declamping. The mean distal aortic pressure was recorded simultaneously via a catheter in the femoral artery.

View larger version (100K): [in this window] [in a new window]   Fig. 1. Diagram of ESPs-dsc monitoring and electrode positions. Two tube-shaped bipolar electrodes (inset) with two platinum tips were placed in C7-T1 and T12-L1 epidural spaces for monitoring ESPs-dsc (with MS-91 apparatus) to detect spinal cord ischemia.

The statistical significance of differences was determined by analysis of variance and Fisher's exact test. All values are reported as the mean ± standard deviation. This study was approved by our institutional review board and informed consent was obtained from all patients involved.

RESULTS

Factors related to neurologic complications
Of the 68 patients, three had "immediate" paraplegia after operation and one had "immediate" paraparesis, whereas two other patients had "delayed" paraplegia (Table I). Only patients with dissecting and nondissecting thoracoabdominal aneurysms had neurologic deficits after operation. Total replacement of the descending aorta caused neurologic deficits in three of five patients. In addition, five of the 30 patients with dissecting aneurysms had neurologic deficits after operation, whereas only one of the 38 patients with nondissecting aneurysms did so. However, this difference was not statistically significant. Among the 48 patients treated with inclusion techniques, neurologic deficits developed in five, and the prevalence was not significantly different from that after the other procedures used. Cardiopulmonary bypass was used in 63% of the patients and neurologic deficits developed in five of them, so there was no significant difference from the patients with other circulatory adjuncts.

View larger version (25K): [in this window] [in a new window]   Fig. 2. Delayed paraplegia in patient with "no change" of ESPs-dsc. Entry closure and insertion of Ivalon sponge to promote early thrombosis was done. Because ESPs-dsc showed no change during 26 minutes of aortic crossclamping (Aoclamp), reconstruction of intercostal arteries was not done. However, delayed paraplegia occurred on second postoperative day and ESPs-dsc responses corresponded well to pattern of clinical neurologic recovery. This was only false-negative case in which patient's deficit was not predicted by intraoperative ESPs-dsc monitoring.

During aortic crossclamping, four types of response pattern were observed on the basis of a modified Crawford-Cunningham classification. ^15,21 The potentials were considered to be "no change" if the amplitude did not decrease by more than 5%, and this was the most common pattern (n = 53). A decrease of amplitude with a return to the control level after less than 30 minutes was classified as "change with return" (n = 10) (Figs. 3 and 4). When the amplitude decreased and then improved but did not remain constantly within the normal range after 30 minutes, it was classified as "change with inconsistent return" (n = 2). Finally, when the amplitude decreased and did not improve again, it was classified as "change without return" (n = 3). Neurologic complications occurred in 2% of the patients with "no change" pattern, 0% of those with "change with return," and 100% of those with "change with inconsistent return" or "change without return." The one patient with neurologic deficits despite a "no change" response had "delayed" paraplegia on the second postoperative day (Table II). There were no significant differences in relation to the extent of the lesions, the presence of dissection, the procedure used, or the method of intraoperative support among these four response groups, probably because of the small number of subjects.

View larger version (21K): [in this window] [in a new window]   Fig. 3. ESPs-dsc responses during total replacement of descending aorta (Ao) for nondissecting aneurysm. After initial crossclamping of upper and lower thoracic aorta (AXC I), ESPs-dsc amplitude decreased. After reimplantation of intercostal arteries (AXC II), ESPs-dsc amplitude recovered to normal. This patient was classified as showing "change with return." CPB, Cardiopulmonary bypass.

View larger version (23K): [in this window] [in a new window]   Fig. 4. ESPs-dsc responses during complete replacement of descending thoracic aorta (Ao). ESPs-dsc amplitude decreased when aortic crossclamps were located proximal to left subclavian artery and descending aorta just above diaphragm (AXC I). However, ESPs-dsc recovered after distal clamp was relocated to upper part of descending aorta (AXC II). Then ESPs-dsc revealed no change after relocation of distal clamp to just above diaphragm and placement of proximal clamp on graft to allow perfusion of left subclavian artery (AXC III). This patient was classified as showing "change with return." CPB, Cardiopulmonary bypass.

View larger version (80K): [in this window] [in a new window]   Fig. 5. Relationship of clamp time, femoral arterial pressure, and cardiopulmonary bypass (CPB) flow to ESPs-dsc response. STD, Standard deviation; NS, not significant.

The main cause of changes in the ESPs-dsc was considered to be low distal perfusion in nine patients, low or absent perfusion of the intercostal arteries in five patients, and unknown in one patient.

The intraoperative surgical countermeasures used were shortening of the aortic crossclamping time with rapid manipulation in five patients, shortening of the time for reimplantation of intercostal arteries in two patients, changing the aortic clamp position in three patients (serial clamping), and changing the cannulation site for shunt or bypass in two patients. No countermeasures could be taken in the three patients with "change without return" of the potentials because intraoperative prolonged hypotensive shock developed (Table III).

Paraplegia is a major operative complication of the repair of thoracic aortic aneurysms. Temporary occlusion of the thoracic aorta causes a reduction in distal aortic perfusion, and the transection or exclusion of spinal radicular vessels may cause inadequate spinal cord perfusion during operation.

Various techniques to prevent cord injury, including shunting, ^1,2,9 partial bypass, ^3,4 drainage of cerebrospinal fluid, ^10,11 and pharmacologic interventions, ¹⁴ have been used both clinically and experimentally. However, their ability to prevent ischemic spinal cord damage remains controversial. ^1-7,9-14

Intraoperative SEP monitoring has been proposed by Cunningham and Laschinger ^15-20 because it directly reflects the ischemic changes of spinal cord function. However, SEPs elicited by peripheral nerve stimulation are not easy to interpret, because they reflect sensory rather than motor function and because they are easily influenced by electric noise, anesthesia, and peripheral nerve dysfunction. ^23,29,30 Because peripheral nerve function is definitely influenced by ischemia, the monitoring of spinal cord function with the use of peripheral nerves (SEPs and some kinds of MEPs ²⁶) does not necessarily reflect spinal cord function during aortic crossclamping. ^16,17,20

MEPs have also been proposed for the intraoperative monitoring of spinal cord function. However, it is hard to obtain large amplitude waves during clinical use of MEPs because of the difficulty of placing the stimulating electrodes onto the dura as is done in the experimental setting ^22,27 and peripheral nerves should not be used in patients with low distal perfusion. ²⁶ In addition, the origins and conduction pathways of the direct spinal cord MEPs that can be elicited by transcranial magnetic stimulation are not well known yet. ^24,28 Furthermore, MEPs elicited by direct cord stimulation do not only reflect motor function and thus should be considered to be ESPs-dsc. ²⁵ Finally, the relationship of MEPs to ischemic spinal cord damage has been controversial in experimental studies. ^22,25-27

The ESPs-dsc method that we used can produce a large signal amplitude and is less sensitive to anesthesia than SEPs. ³² This method has been investigated in the orthopedic and neurosurgical fields since 1972. ^33,34 The basic ESPs-dsc pattern consists of two components, an initial spike and a polyphasic component. The initial spike was once thought to reflect dorsal column function, ^35,36 but this component is now considered to originate from large fibers in all quadrants of the spinal cord. ^37,38 In contrast, the polyphasic component is considered to be conducted mainly through the dorsal column. ^35,36 In the present study, we observed four types of ESPs-dsc responses, which were grouped on the basis of a modified Crawford-Cunningham classification. ^15,21 Although these authors defined the potentials as "no change" if the latency did not increase by more than 10% and the amplitude did not decrease by more than 25%, we defined the amplitude criterion more strictly as a 5% decrease, because ESPs-dsc are highly reproducible and 53 of our 68 patients were included in this narrow range.

ESPs-dsc monitoring was extremely effective in detecting neurologic deficits, with a false-negative rate of 2% and a false-positive rate of 0% (Table II). The only false-negative case involved a patient with "no change" potentials whose condition was normal at the time of recovery from anesthesia, but in whom paraplegia developed on the second postoperative day (a "delayed" deficit). ³⁹ In this case, entry closure of a dissecting aneurysm was done with packing of Ivalon sponge into the false lumen to promote thrombus formation. ³¹ Because the crossclamp time was only 26 minutes, embolization of the anterior spinal artery was considered likely to be the cause of this delayed deficit and its prediction by intraoperative monitoring would thus have been impossible (Fig. 2).

A long aortic clamping time is thought to increase the risk of neurologic deficits. In the present series, the clamp time of five of the six patients with neurologic deficits exceeded 112 minutes (Table I). The ESPs-dsc responses were also related to the clamp time. The mean clamp times of the "no change" group and "change with return" group were not significantly different, whereas the mean clamp time of the other two groups was significantly longer than the times of both the former groups. Our findings suggested that severe ESPs-dsc changes occurred when reperfusion of the spinal cord could not be done during complicated procedures (Fig. 5).

Some investigators have reported the benefits of shunt or bypass procedures for spinal cord ischemia, ^1-5,7 but others have not supported these contentions. ^5,6 We consider that these adjuncts are not necessary when the continuity between the anterior spinal artery and the vertebral or collateral arteries is maintained. ²³ However, a definite possibility of postoperative neurologic deficits exists if distal perfusion is inadequate. In our study, the mean femoral artery pressure and the flow rate during partial cardiopulmonary bypass were significantly lower in the groups with "change with inconsistent return" or "change without return" of the potentials than these values in the other two groups (Fig. 5). We currently use shunt or bypass procedures in almost all of our patients. In addition, if major spinal radicular arteries are involved, we perfuse those arteries through a branch of the circuit. Because Cunningham, ¹⁵ Laschinger, ¹⁶ and their associates reported that a distal mean arterial pressure higher than 60 mm Hg is adequate for preventing spinal cord ischemia, and because Crawford and associates ²¹ mentioned that a larger flow at a lower pressure was associated with less neurologic injury than a lower flow at a higher pressure, we consider that a pressure of 50 to 80 mm Hg and a cardiopulmonary bypass flow rate of 1.5 to 2.5 L/min should be adequate in adults. It is better to improve the spinal cord blood flow by perfusion of the intercostal arteries if the ESPs-dsc amplitude diminishes despite such circulatory support, because the major radicular arteries must be involved in the site of resection.

In response to changes of the ESPs-dsc, the following surgical interventions are possible: (1) shortening the aortic crossclamping time if the major radicular artery is not involved by the site of resection, (2) relocation of the aortic clamp (serial clamping), (3) selective perfusion and/or reimplantation of critical intercostal vessels and shortening the time until reimplantation, and (4) moving the cannulation site for shunt or bypass. In 12 of the 15 patients with ESPs-dsc changes, we tried to improve spinal cord blood flow by various maneuvers. However, we could not use any additional protective techniques in the three patients who showed no recovery of ESP-dsc because of hypotensive shock caused by massive intraoperative bleeding. Shortening of the aortic crossclamping time with rapid manipulation of the clamps was the most common countermeasure (used in five patients), because the resection site was outside T9-L2, which is commonly the origin of the major radicular arteries, and the ESPs-dsc potentials changed slowly. The time for reimplantation of critical intercostal arteries was shortened in two cases, and the aortic clamping site was moved in three cases. This serial clamping maneuver may potentially be the most important method of preventing postoperative neurologic deficits inasmuch as it is simple to do. We also consider that perfusion of the left subclavian artery is important when the continuity between the anterior spinal artery and the vertebral arteries is sufficient to perfuse the entire spinal cord and distal perfusion is inadequate or critical intercostal arteries are involved in the site of resection. When the expected clamping time was long, we also relocated the cannulation site for the shunt or bypass. Although these countermeasures were unsuccessful in 2 of the 12 patients, our interventions may have avoided paraplegia in the other cases (Table III).

Although there are some limits to intraoperative ESPs-dsc monitoring, because it will not completely prevent paraplegia and it cannot necessarily predict delayed neurologic deficits, this study indicated that it is a useful method for the early detection of spinal cord ischemia and for monitoring adjunctive maneuvers to improve the outcome.

Acknowledgments

We thank Barbara Robinson, MD (Mayo Clinic, Rochester, Minn.) for reading this manuscript.

References

1. Culliford AT, Ayvalioyis B, Shemin R, Colvin SB, Isom OW, Spencer FC. Aneurysms of the descending aorta: surgical experience in 48 patients. J THORAC CARDIOVASC SURG 1983;85:98-104. [Abstract]
   
2. Lawrence GH, Hessel EA, Sauvage LR, Krause AH. Results of the use of the TDMAC-heparin shunt in the surgery of aneurysms of the descending thoracic aorta. J THORAC CARDIOVASC SURG 1977;78:393-8.
   
3. May IA, Ecker RR, Iverson LIG. Heparinless femoral venoarterial bypass without an oxygenator for surgery on the descending thoracic aorta. J THORAC CARDIOVASC SURG 1977;73:387-92. [Abstract]
   
4. Carlson DE, Karp RB, Kouchoukos NT. Surgical treatment of aneurysms of the descending thoracic aorta: an analysis of 85 patients. Ann Thorac Surg 1983;35:58-69. [Abstract]
   
5. Crawford ES, Walker HSJ III, Saleh SA, Normann NA. Graft replacement of aneurysms in the descending thoracic aorta: results without bypass or shunting. Surgery 1981;89:73-85. [Medline]
   
6. Crawford ES, Crawford JL, Safi HJ, Coselli JS, Hess KR. Thoracoabdominal aortic aneurysms: preoperative and intraoperative factors determining immediate and long-term results after operation in 605 patients. J Vasc Surg 1986;3:389-404. [Medline]
   
7. Livesay JJ, Cooley DA, Ventemiglia RA, et al. Surgical experience in descending thoracic aneurysmectomy with and without adjuncts to avoid ischemia. Ann Thorac Surg 1985;39:37-46. [Abstract]
   
8. Katz NM, Blackstone EH, Kirklin JW, Karp RB. Incremental risk factors for spinal cord injury following operation for acute traumatic aortic transection. J THORAC CARDIOVASC SURG 1981;81:669-74. [Abstract]
   
9. Molina JE, Cogordan J, Einzig S, et al. Adequacy of ascending aorta–descending aorta shunt during cross-clamping of the thoracic aorta for prevention of spinal cord injury. J THORAC CARDIOVASC SURG 1985;90:126-36. [Abstract]
   
10. Miyamoto K, Keno A, Wada T, Kimoto S. A new and simple method of preventing spinal cord damage following temporary occlusion of the thoracic aorta by draining the cerebrospinal fluid. J Cardiovasc Surg 1960;16:188-99.
    
11. Blaisdell FW, Cooley DA. The mechanism of paraplegia after temporary thoracic aortic occlusion and its relationship to spinal fluid pressure. Surgery 1962;51:351-5. [Medline]
    
12. Wadouh F, Lindemann EM, Arndt CF, Hetzer R, Borst HG. The arteria radicularis magna anterior as a decisive factor influencing spinal cord damage during aortic occlusion. J THORAC CARDIOVASC SURG 1984;88:1-10. [Abstract]
    
13. Wadouh F, Arndt CF, Metzger H, Hartmann M, Wadouh R, Borst HG. Direct measurements of oxygen tension on the spinal cord surface of pigs after occlusion of the descending aorta. J THORAC CARDIOVASC SURG 1985;89:787-94. [Abstract]
    
14. Qayumi AK, Janusz MT, Jamieson WRE, Lyster DM. Pharmacologic interventions for prevention of spinal cord injury caused by aortic crossclamping. J THORAC CARDIOVASC SURG 1992;104:256-61. [Abstract]
    
15. Cunningham LN, Lashinger JC, Merklin HA, et al. Measurement of spinal cord ischemia during operations upon the thoracic aorta. Ann Surg 1982;196:285-96. [Medline]
    
16. Laschinger JC, Cunningham JN, Catinella FP, Nathan IM, Knopp EA, Spencer FC. Detection and prevention of intraoperative spinal cord ischemia after cross-clamping of the thoracic aorta: use of somatosensory evoked potentials. Surgery 1982;92:1109-17. [Medline]
    
17. Coles JG, Wilson GJ, Sima AF, Klement P, Tait GA. Intraoperative detection of spinal cord ischemia using somatosensory cortical evoked potentials during thoracic aortic occlusion. Ann Thorac Surg 1982;34:299-306. [Abstract]
    
18. Pollock JC, Jamieson MP, McWilliam R. Somatosensory evoked potentials in the detection of spinal cord ischemia in aortic coarctation repair. Ann Thorac Surg 1986;41:251-4. [Abstract]
    
19. Laschinger JC, Cunningham JN, Nathan IM, Knopp EA, Cooper MM, Spencer FC. Experimental and clinical assessment of the adequacy of partial bypass in maintenance of spinal cord blood flow during operations on the thoracic aorta. Ann Thorac Surg 1983;36:417-26. [Abstract]
    
20. Coles JG, Wilson GJ, Sima AF, et al. Intraoperative management of thoracic aortic aneurysm: experimental evaluation of perfusion cooling of the spinal cord. J THORAC CARDIOVASC SURG 1983;85:292-9. [Medline]
    
21. Crawford ES, Mizrahi EM, Hess KR, Coselli JS, Safi HJ, Patel VM. The impact of distal aortic perfusion and somatosensory evoked potential monitoring on prevention of paraplegia after aortic aneurysm operation. J THORAC CARDIOVASC SURG 1988;95:357-67. [Abstract]
    
22. Elmore JR, Gloviczki P, Harper CM, et al. Failure of motor evoked potentials to predict neurologic outcome in experimental thoracic aortic occlusion. J Vasc Surg 1991;14:131-9. [Medline]
    
23. Matsui Y, Goh K, Okude J, Sakuma M, Yasuda K, Tanabe T. The prevention of spinal cord ischemia during surgery on the thoracic aorta utilizing the evoked spinal cord potential: evoked spinal cord potential (ESP) versus somatosensory evoked potential (SEP) for spinal ischemic change. J Jpn Assoc Thorac Surg 1986;34:172-9.
    
24. York DH. Review of descending motor pathways involved with transcranial stimulation. Neurosurgery 1987;20:70-3. [Medline]
    
25. Laschinger JC, Owen J, Rosenbloom M, Cox JL, Kouchoukos NT. Direct noninvasive monitoring of spinal cord motor function during thoracic aortic occlusion: use of motor evoked potentials. J Vasc Surg 1988;7:161-71. [Medline]
    
26. Svensson LG, Patel V, Robinson MF, Ueda T, Roehm JOF, Crawford ES. Influence of preservation or perfusion of intraoperatively identified spinal cord blood supply on spinal motor evoked potentials and paraplegia after aortic surgery. J Vasc Surg 1991;13:355-65. [Medline]
    
27. Reuter DG, Tacker WA Jr, Badylak SF, Voorhees WD III, Konrad PE. Correlation of motor evoked potential response to ischemic spinal cord damage. J THORAC CARDIOVASC SURG 1992;104:262-72. [Abstract]
    
28. Kawai N, Nagao S. Origins and conducting pathways of motor evoked potentials elicited by transcranial magnet stimulation in cats. Neurosurgery 1992;31:520-7. [Medline]
    
29. North RB, Drenger B, Beattie C, et al. Monitoring of spinal cord stimulation evoked potentials during thoracoabdominal aneurysm surgery. Neurosurgery 1991;28:325-30. [Medline]
    
30. Okamoto Y, Murakami M, Nakagawa T, Murata A, Moriya H. Intraoperative spinal cord monitoring during surgery for aortic aneurysm: application of spinal cord evoked potential. Electroencephalogr Clin Neurophysiol 1992;84:315-20. [Medline]
    
31. Tanabe T, Hashimoto M, Sakai K, et al. Surgical treatment of aortic dissection: application of Ivalon sponge to the dissecting lumen. Ann Thorac Surg 1986;41:169-75. [Abstract]
    
32. Tamaki T, Tsuji H, Inoue S, Kobayashi H. The prevention of iatrogenic spinal cord injury utilizing the evoked spinal cord potential. Int Orthop 1981;4:313-7. [Medline]
    
33. Tamaki T, Yamashita T, Kobayashi H, Hirayama H. Spinal cord monitoring. Jpn J Electroencephalogr 1976;1:196.
    
34. Kurokawa T. Spinal cord action potentials evoked by epidural stimulation of cord: a report of human and animal record. Jpn J Electroencephalogr Electromyogr Clin Neurophysiol 1972;1:64-6.
    
35. Imai T. Human electrospinogram evoked by direct stimulation on the spinal cord through epidural space. J Jpn Orthop Assoc 1976;50:1037-56.
    
36. Tsuyama N, Tsuzuki N, Kurokawa T, Imai T. Clinical application of spinal cord action potential measurement. Int Orthop 1978;3:39-46.
    
37. Harada Y, Takemitsu Atsuta Y, Imai M. Determination of the pathway of ascending and descending conductive spinal cord evoked potentials (SCEP). In: Homma S, Tamaki T, eds. Fundamentals and clinical application of spinal cord monitoring. Tokyo: Saikon Press, 1984:211-21.
    
38. Toyoda A, Kanda K. Origins of spinal cord potentials evoked by stimulation of the cat spinal cord. In: Homma S, Tamaki T, eds. Fundamentals and clinical application of spinal cord monitoring. Tokyo: Saikon Press, 1984:99-111.
    
39. Moore WM, Hollier LH. The influence of severity of spinal cord ischemia in the etiology of delayed-onset paraplegia. Ann Surg 1991;213:427-32.[Medline]
    

This article has been cited by other articles:

				M. Sakurai, G. Takahashi, K. Abe, T. Horinouchi, Y. Itoyama, and K. Tabayashi Endoplasmic reticulum stress induced in motor neurons by transient spinal cord ischemia in rabbits J. Thorac. Cardiovasc. Surg., September 1, 2005; 130(3): 640 - 645. [Abstract] [Full Text] [PDF]

				T. B. Sloan Electrophysiologic Monitoring during Surgery to Repair the Thoracoabdominal Aorta Seminars in Cardiothoracic and Vascular Anesthesia, June 1, 2004; 8(2): 113 - 125. [Abstract] [PDF]

				M. Sakurai, T. Nagata, K. Abe, T. Horinouchi, Y. Itoyama, and K. Tabayashi Survival and death-promoting events after transient spinal cord ischemia in rabbits: Induction of Akt and caspase3 in motor neurons J. Thorac. Cardiovasc. Surg., February 1, 2003; 125(2): 370 - 377. [Abstract] [Full Text] [PDF]

				M. Sakurai, T. Hayashi, K. Abe, Y. Itoyama, K. Tabayashi, and W. I. Rosenblum Cyclin D1 and Cdk4 Protein Induction in Motor Neurons After Transient Spinal Cord Ischemia in Rabbits Editorial Comment Stroke, January 1, 2000; 31(1): 200 - 207. [Abstract] [Full Text] [PDF]

				J.-M. Guerit, C. Witdoeckt, R. Verhelst, A. J. Matta, L. M. Jacquet, and R. A. Dion Sensitivity, specificity, and surgical impact of somatosensory evoked potentials in descending aorta surgery Ann. Thorac. Surg., June 1, 1999; 67(6): 1943 - 1946. [Abstract] [Full Text] [PDF]

				M. Sakurai, T. Hayashi, K. Abe, M. Sadahiro, and K. Tabayashi Delayed and selective motor neuron death after transient spinal cord ischemia: A role of apoptosis? J. Thorac. Cardiovasc. Surg., June 1, 1998; 115(6): 1310 - 1314. [Abstract] [Full Text] [PDF]

				S. Ishimaru, S. Kawaguchi, N. Koizumi, Y. Obitsu, and M. Ishikawa Preliminary report on prediction of spinal cord ischemia in endovascular stent graft repair of thoracic aortic aneurysm by retrievable stent graft J. Thorac. Cardiovasc. Surg., April 1, 1998; 115(4): 811 - 818. [Abstract] [Full Text] [PDF]

This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Kazutomo Goh Norihiko Shiiya Keishu Yasuda Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Matsui, Y. Articles by Tanabe, T. Search for Related Content PubMed PubMed Citation Articles by Matsui, Y. Articles by Tanabe, T.