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1 Prevention and Detection of Spinal Cord Injury During Thoracic and Thoracoabdominal Aortic Repairs Torazo Wada, MD, Hideki Yao, MD, Takashi Miyamoto, MD, Sukemasa Mukai, MD, and Mitsuhiro Yamamura, MD Department of Thoracic and Cardiovascular Surgery, Hyogo College of Medicine, Nishinomiya, Japan Background. Spinal cord injury is a most dreaded and unpredictable complication. In this study, based on our experimental results in dogs and early clinical results, we reviewed the incidence of paraplegia and the detection of spinal cord injury. Methods. Eighty-two patients who underwent elective surgical repair of the descending thoracic and thoracoabdominal aorta over 17 years were subjects for this study. Sixty-two patients were male and 20 were female. Their mean age was 61.6 years (range, 17 to 81 years). Monitoring somatosensory evoked potentials (SEP) and measurement of mean distal aortic pressure and cerebrospinal fluid pressure were performed perioperatively. Results. Sixty patients had no ischemic change in SEP. In 17 patients with significant ischemic changes of SEP, SEP recovered by increasing spinal cord perfusion pressure to more than 40 mm Hg. Two patients with complete loss of SEP experienced paraplegia. One patient had delayed paraplegia. Conclusions. These results strongly suggest that SEP, mean distal aortic pressure, cerebrospinal fluid pressure should be monitored during aortic cross-clamping. Maintaining spinal cord perfusion pressure at more than 40 mm Hg by increasing mean distal aortic pressure or withdrawal of cerebrospinal fluid is valuable for preventing paraplegia. (Ann Thorac Surg 2001;72:80 5) 2001 by The Society of Thoracic Surgeons Accepted for publication March 14, Address reprint requests to Dr Wada, Department of Thoracic and Cardiovascular Surgery, Hyogo College of Medicine, 1-1 Mukogawa-cho Nishinomiya, Hyogo, , Japan; wadatora@hyo-med.ac.jp. Despite recent advances in operative techniques, anesthetic management, and postoperative supportive care, a most dreaded operative complication with surgical treatment of descending thoracic and thoracoabdominal aortic diseases, paraplegia, remains unresolved. At present, the incidence of perioperative paraplegia ranges from 3.8% to 17.6% [1]. In 1960, Miyamoto and associates [2] and Blaisdell and Cooley [3] reported that cerebrospinal fluid pressure (CSFP) is an important factor in spinal cord injury after thoracic aortic crossclamping because elevated CSFP aggravates spinal cord ischemia by compressing the vascular system of the spinal cord. In 1982, Coles and colleagues [4] and Cunningham and associates [5] demonstrated an earlier detection of spinal cord ischemia by using somatosensory evoked potentials (SEP) that were generated by intraoperative stimulation of peripheral nerves. In 1984, Oka and Miyamoto [6, 7] investigated and reported that in a dog experimental study, the effect of spinal cord perfusion pressure (SCPP), defined as the pressure difference between mean distal aortic pressure (MDAP) and CSFP was one of the important factors for perioperative development of spinal cord injury. In 1987, Maeda and coworkers [8] reported that, in clinical experience, maintaining SCPP at more than 40 mm Hg during aortic crossclamping by increasing MDAP or withdrawal of cerebrospinal fluid (CSF) was valuable for the prevention of paraplegia. In this study, we reviewed the incidence of paraplegia and perioperative detection of spinal cord injury in cases of descending thoracic and thoracoabdominal aortic repairs by monitoring SEP, MDAP, and CSFP during aortic cross-clamping. Material and Methods Patients and Methods Between December 1, 1982, and June 31, 1999, 82 patients who underwent elective surgical repairs at Hyogo College of Medicine for descending thoracic aortic aneurysms, thoracoabdominal aortic aneurysms, and coarctation of the aorta were enrolled as subjects in this study. A retrospective review of the patients perioperative and postoperative outcomes was conducted using hospital records and clinic charts. Sixty-two patients were male and 20 were female. Their ages ranged from 17 to 81 years, with a mean age of 61.6 years. In this study, cases with emergent operation and using deep hypothermic circulatory arrest were excluded because we could not monitor SEP. Perioperative Monitoring System Monitoring of SEP and measurement of MDAP and CSFP were performed perioperatively (Fig 1). Somatosensory evoked potentials were measured with a Synax by The Society of Thoracic Surgeons /01/$20.00 Published by Elsevier Science Inc PII S (01)02639-X
2 Ann Thorac Surg WADA ET AL 2001;72:80 5 PREVENTION OF SPINAL CORD INJURY 81 Statistical Analysis Statistical significance was determined by Student s t test for paired data, and all values are described as mean standard deviation. Fig 1. Perioperative monitoring, showing how to record somatosensory evoked potentials (SEP) and evaluate SCPP. (CSFP cerebrospinal fluid pressure; EEG electro-encephalogram; MDAP mean distal aortic pressure; SCPP spinal cord perfusion pressure.) clinical evoked potential system (NEC Co, Ltd, Tokyo, Japan). Somatosensory evoked potential traces were generated by electrical stimulation of the peroneal nerves bilaterally with two bipolar input channels. One hundred consecutive stimuli with a 200-V square-wave stimulation of 0.2 milliseconds at a frequency of 2 Hz were averaged for each SEP trace. When the amplitude of SEP was less than 50%, we judged this as a significant ischemic change. When the amplitude was more than 80%, we judged this as recovery of SEP. Cerebrospinal fluid pressure was measured with a spinal drainage kit (Silascon, Kaneka Medix Co, Tokyo, Japan) placed in the intrathecal space through a lumbar puncture needle. Withdrawal of CSF was performed through this catheter. Arterial pressure in the right radial artery and one of the dorsal pedis arteries was measured constantly. Spinal cord perfusion pressure was calculated as the pressure difference between MDAP and CSFP. Operative Technique All patients had either temporary bypass shunt or partial cardiopulmonary bypass during the aortic crossclamping at normothermia. A temporary axillofemoral shunt using a 10-mm woven polyethylene terephthalate fiber (Dacron) graft (Intervascular Inc, Tampa, FL) were used in 9 patients. Femoral vein to femoral artery bypass was used in 73 patients. All patients were anticoagulated with heparin using 300 IU/kg. When SCPP was less than 40 mm Hg, MDAP was increased intentionally with adjustment of bypass flow and withdrawal of CSF for increasing the SCPP. Type of Aortic Disease The subjects included 38 patients with dissecting aneurysm (Stanford type B), 32 patients with descending thoracic aortic aneurysm, 10 patients with thoracoabdominal aortic aneurysm, and 2 patients with coarctation of the aorta. Results Type of Operation A woven Dacron tube graft was inserted in 29 cases of descending thoracic aortic aneurysm, in 10 cases of dissecting aneurysm with descending thoracic aortic aneurysm, in 10 cases of thoracoabdominal aortic aneurysm, and in 1 case of coarctation of the aorta. Entry closure and aortoplasty was performed in 28 cases in type B aortic dissection. Four cases involved performing patch graft repair with woven Dacron wrapping for descending thoracic aortic aneurysm and coarctation. Five of 22 cases with significant ischemic changes of SEP underwent revascularization of the intercostal-arteries (T9 to T12). The mean aortic cross-clamp time was minutes. Mortality and Morbidity The hospital mortality rate was 7.3% (6 of 82) for elective repairs. Half (3 of 6) of the causes of death were because of thoracic empyema. The other three causes of death included respiratory failure, cerebral infarction, and acute mediastinitis. Late Survival Actuarial analysis of long-term survival rate revealed that 90% of hospital survivors were alive 1 year after operation, 78.7% were alive 5 years, and 56.8% were alive 10 years (Fig 2). The causes of late deaths were rupture of other aortic aneurysm in 3 patients, malignant disease in 3, myocardial infarction in 2, cerebral infarction in 2, hemoptysis in 2, respiratory failure in 2, and unrelated disease in 8. Incidence of Paraplegia Two patients with complete loss of SEP, whose SCPP were 32 and 35 mm Hg, experienced paraplegia. (The mean aortic cross-clamp time was minutes.) One patient Fig 2. Actuarial survival curve (Kaplan-Meier method) showing that 90% of the hospital survivors were alive at 1 year after operation, 78.7% at 5 years, and 56.8% at 10 years.
3 82 WADA ET AL Ann Thorac Surg PREVENTION OF SPINAL CORD INJURY 2001;72:80 5 Fig 3. Relation between somatosensory evoked potential (SEP) monitoring and incidence of paraplegia (n 82). (F-F femoral vein to femoral artery; SCPP spinal cord perfusion pressure.) with significant changes of SEP, whose SCPP was 60 mm Hg, had delayed paraplegia. Although another 19 patients of the remaining 79 patients showed significant ischemic changes of SEP, in 17 of these 19, SEP gradually recovered by increasing the SCPP to more than 40 mm Hg. In the other 60 patients without any ischemic SEP changes, SCPP was kept at more than 40 mm Hg except two. These 2 patients did not develop paraplegia (Fig 3). Cerebrospinal Fluid Pressure The CSFP before and the maximal CSFP during aortic cross-clamping averaged and mm Hg, respectively. A significant increase in CSFP was observed after aortic cross-clamping (p 0.05). Subsequently, CSF was withdrawn (range, 9 to 110 ml; average, 30 ml) in 15 patients. Figure 4 shows the relationship between mean CSFP and SEP. Cerebrospinal fluid pressure rose to more than 20 mm Hg in 2 patients. The two patients who experienced paraplegia showed ischemic changes of SEP. Cerebrospinal fluid pressure did not rise more than 20 mm Hg except 1 patient who had delayed paraplegia. Comment The reported risk of paraplegia is known to be significantly higher after repairs of traumatic aortic transection, emergency, and acute aortic dissection [9 11]. The cause of paraplegia was thought to be insufficient radicular arterial flow caused by interruption of critical intercostal arteries in the replaced aortic segment, insufficient pressure of the distal aorta, or extended aortic cross-clamp time. Other factors, such as intraoperative proximal hypertension, elevation of CSFP, and postoperative hypotension, also have implications. Combination of these factors decreases blood flow to the spinal cord and may lead to spinal cord ischemic changes. All patients had either temporary bypass shunt or femoral vein to femoral artery bypass during aortic cross-clamping. A temporary axillofemoral shunt using a 10-mm woven Dacron graft was used in 9. Two of these 9 patients had paraplegia because the SCPP could not be maintained above 40 mm Hg during temporary bypass shunting. Femoral vein to femoral artery bypass was used in 73 patients; paraplegia did not occur. Femoral vein to femoral artery bypass grafting involving the use of a pump oxygenator has the disadvantage of requiring systemic anticoagulation with heparin, although on the contrary, the advantage of this surgical procedure for unexpected bleeding is avoiding either hypotension or hypertension at proximal and distal aortic pressure [12]. Spinal Cord Perfusion Pressure Figure 5 shows the SCPPs of 60 patients with no significant ischemic SEP changes and 22 with ischemic changes during aortic cross-clamping. Two of the 3 patients whose SCPP was less than 40 mm Hg experienced paraplegia. Significant ischemic SEP changes were seen in 19 patients, and increase of MDAP or withdrawal of CSF was performed to maintain SCPP at more than 40 mm Hg. Somatosensory Evoked Potentials Somatosensory evoked potentials were monitored in 82 patients. Fifty-eight of these maintained no ischemic SEP changes with SCPP more than 40 mm Hg, whereas 2 patients maintained intact SEP with lower pressure. None of the 60 patients with no significant ischemic SEP changes experienced paraplegia (Fig 3). In contrast, 22 patients had ischemic SEP changes, and 2 patients ultimately experienced paraplegia with SCPP pressure less than 40 mm Hg (9.0%). Fig 4. Mean cerebrospinal fluid pressure (CSFP) during aortic cross-clamping in 60 patients with no significant ischemic somatosensory evoked potential (SEP) changes and 22 with significant ischemic SEP changes. Cerebrospinal fluid pressure rose to more than 20 mm Hg in 2 patients, who experienced paraplegia.
4 Ann Thorac Surg WADA ET AL 2001;72:80 5 PREVENTION OF SPINAL CORD INJURY 83 Fig 5. Spinal cord perfusion pressure (SCPP) during aortic crossclamping in 60 patients with no significant ischemic somatosensory evoked potential (SEP) changes and 22 with significant ischemic SEP changes. Spinal cord perfusion pressure was less than 40 mm Hg in 5 patients. Two of 3 patients with significant ischemic SEP changes during aortic cross-clamping experienced paraplegia. Coselli and LeMaire [13] and Schepens and associates [14] presented the use of left heart bypass as beneficial in patients who had thoracoabdominal aortic aneurysm repair. Kouchoukos and Rokkas [15] recommended that hypothermic cardiopulmonary bypass with circulatory arrest is useful in patients at highest risk for development of paraplegia. Laschinger and coworkers [16 18] described the use of monitoring of SEPs in detecting the onset of spinal cord ischemia and assessing the adequacy of distal aortic perfusion in preserving sensory conduction of the posterior and lateral spinal column during proximal aortic cross-clamping. The major disadvantage of SEP is that it could not detect occurrence of motor deficits. Falsepositive tracings are likely, for example, cortical dysfunction, which can be prompted by the effects of anesthetic agents or ischemia, and peripheral nerve ischemia [19]. De Hann and colleagues [20] reported that monitoring motor-evoked potentials is an effective technique to detect spinal cord ischemia for monitoring anterior spinal cord function. Somatosensory evoked potentials may not reflect selective ischemia of the spinal motor system, because the motoneuronal system in the anterior horn receives its blood supply from the anterior spinal artery. But motor-evoked potentials are readily depressed by many commonly used anesthetics, such as nitrous oxide [21], propofol [22], benzodiazepines [23], and volatile anesthetics [24]. Paraplegia did not occur in any patient whose SEPs remained intact. In contrast, when SEPs suggested significant ischemic changes, the surgeon had to assume that spinal cord ischemia would be present. In spite of immediate changes in operative technique to elevate the distal aortic pressure, reattach the intercostal arteries to the graft, or withdraw CSF, paraplegia occurred in 2 (9.1%) of the 22 patients who experienced a significant ischemic change of SEP during aortic cross-clamping. If SEPs are lost, we recommend increasing bypass flow until the SCPP is more than 40 mm Hg and the SEP amplitude and latency improve. If the SCPP is more than 40 mm Hg and the SEP amplitude does not improve, we have to reattach intercostal arteries. Safi and associates [25] reported on the importance of intercostal artery reattachment. The use of SEP monitoring during operation offers the promise of being able to avert neurologic compromise by early detection of abnormal signal transmission from distal extremities to the cerebral cortex [26]. In this study postoperative paraplegia occurred in 3 patients, including 1 with delayed paraplegia. Two patients SCPPs were 32 and 35 mm Hg, and their SEP traces were lost. We could not maintain the high MDAP for using temporary bypass shunt in these 2 patients. Conversely, 1 patient who had normal SEPs during the operation later experienced paraplegia. We reevaluated whether prolongation of SEP monitoring during the postoperative period with careful systemic aortic pressure control is needed to prevent delayed paraplegia [27]. The withdrawal of CSF was undertaken to increase SCPP and enhance blood flow to the spinal cord by decompressing collateral blood vessels to the spinal cord. The elevation of CSFP is one of the major factors causing paraplegia [28]. Increased CSFP is caused by volume changes in venous capacitance beds within the dural space [29]. Proximal hypertension during cross-clamp prompts the autoregulation mechanisms of the cerebral and spinal vasculature to reflexively increase CSFP, effectively lowering SCPP, and thereby diminishing cord blood supply [30]. Conversely, drainage of CSF to reduce CSFP will offset the gradient in favor of augmenting spinal cord perfusion. When the CSFP rises to more than 20 mm Hg, we propose that CSF should be aspirated to keep the SCPP at more than 40 mm Hg at least. Both CSFP and distal aortic pressure are important determinants of spinal cord perfusion. Safi and coworkers [31] recommended that CSFP be maintained at or below 10 mm Hg. Laschinger and associates [32] recommended maintaining a distal aortic pressure of at least 60 mm Hg. In summary, the most important results from these data of 82 patients is that paraplegia did not occur if the SCPP was maintained at more than 40 mm Hg with no significant ischemic changes of SEP. For the prevention
5 84 WADA ET AL Ann Thorac Surg PREVENTION OF SPINAL CORD INJURY 2001;72:80 5 and detection of the perioperative paraplegia, we propose the following: 1. Somatosensory evoked potentials, MDAP, and CSFP should be monitored during aortic cross-clamping. 2. Maintaining SCPP at more than 40 mm Hg by increasing MDAP or withdrawal of CSF is valuable for prevention of perioperative paraplegia. 3. Femoral vein to femoral artery bypass is useful to control the distal aortic perfusion during aortic closs-clamping, as intraoperative adjuncts. This shows that monitoring of SCPP is more reliable and effective in maintaining spinal cord perfusion. References 1. Crawford ES, Rubio PA. Reappraisal of adjuncts to avoid ischemia in the treatment of aneurysms of descending thoracic aorta. J Thorac Cardiovasc Surg 1973;66: Miyamoto K, Ueno 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;1: Blaisdell FW, Cooley DA. The mechanism of paraplegia after temporary thoracic aortic occlusion and its relationship to spinal fluid pressure. Surgery 1962;51: 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: Cunningham JN Jr, Laschinger JC, Merkin HA, et al. Measurement of spinal cord ischemia during operations upon the thoracic aorta. Initial clinical experience. Ann Surg 1982; 196: Oka Y, Miyamoto T. Prevention of spinal cord injury after cross-clamping of thoracic aorta. Jpn J Surg 1984;14: Oka Y, Miyamoto T. Prevention of spinal cord injury after cross-clamping of thoracic aorta. J Cardiovasc Surg 1987;28: Maeda S, Miyamoto T, Murata H, Yamashita K. Prevention of spinal cord ischemia by monitoring spinal cord perfusion pressure and somatosensory evoked potentials. J Cardiovasc Surg 1989;30: Mauney MC, Blackbourne LH, Langenburg SE, Buchanan SA, Kron IL, Tribble CG. Prevention of spinal cord injury after repair of the thoracic or thoracoabdominal aorta. Ann Thorac Surg 1995;59: Turney SZ, Attar S, Ayella R, et al. Traumatic rupture of the aorta: a five year experience. J Thorac Cardiovasc Surg 1976; 72: Crawford ES, Crawford JL, Safi HJ, et al. Thoracoabdominal aortic aneurysms: preoperative and intraoperative factors determining immediate and long-term results of operations in 605 patients. J Thorac Cardiovasc Surg 1986;3: Najafi H. Descending aortic aneurysmectomy without adjuncts to avoid ischemia. Ann Thorac Surg 1993;55: Coselli JS, LeMaire SA. Left heart bypass reduced paraplegia rates after thoracoabdominal aortic aneurysm repair. Ann Thorac Surg 1999;67: Schepens MA, Vermeulen FE, Morshuis WJ, et al. Impact of left heart bypass on the results of thoracoabdominal aortic aneurysm repair. Ann Thorac Surg 1999;67: Kouchoukos NT, Rokkas CK. Hypothermic cardiopulmonary bypass for spinal cord protection: rationale and clinical results. Ann Thorac Surg 1999;67: Laschinger JC, Cunningham JN Jr, Cooper MM, Baumann FG, Spencer FC. Monitoring of somatosensory evoked potentials during surgical procedures on the thoracoabdominal aorta: I. Relationship of aortic cross-clamp duration, changes in somatosensory evoked potentials, and incidence of neurologic dysfunction. J Thorac Cardiovasc Surg 1987;94: Laschinger JC, Cunningham JN Jr, Baumann FG, Isom OW, Spencer FC. Monitoring of somatosensory evoked potentials during surgical procedures on the thoracoabdominal aorta: II. Use of somatosensory evoked potentials to assess adequacy of distal aortic bypass and perfusion after thoracic aortic crossclamping. J Thorac Cardiovasc Surg 1987;94: Laschinger JC, Cunningham JN Jr, Baumann FG, Cooper MM, Krieger KH, Spencer FC. Monitoring of somatosensory evoked potentials during surgical procedures on the thoracoabdominal aorta: III. Intraoperative identification of vessels critical to spinal cord blood supply. J Thorac Cardiovasc Surg 1987;94: Laschinger JC, Izumoto H, Kouchoukos NT. Evolving concepts in prevention of spinal cord injury during operations on the descending thoracic and thoracoabdominal aorta. Ann Thorac Surg 1987;44: de Haan P, Kalkman CJ, de Mol BA, Ubags LH, Veldman DJ, Jacobs MJ. Efficacy of transcranial motor-evoked myogenic potentials to detect spinal cord ischemia during operations for thoracoabdominal aneurysms. J Thorac Cardiovasc Surg 1997;113: Ghaly RF, Stone JL, Levy WL, Kartha R, Aldrete JA. The effect of nitrous oxide on transcranial magnetic-induced electromyographic responses in the monkey. J Neurosurg Anesth 1990;2: Kalkman CJ, Drummond JC, Ribberink AA, Patel PM, Sano T, Bickford RG. Effects of propofol, etomidate, mitazolam and fentanyl on motor evoked responses to transcranial electrical or magnetic stimulation in humans. Anesthesiology 1992;76: Kalkman CJ, Drummond JC, Ribberink AA. Low concentrations of isoflurane abolish motor evoked responses to transcranial electrical stimulation during nitrous oxide/opioid anesthesia in humans. Anesth Analog 1991;73: Kalkman CJ, Drummond JC, Kennelly NA, Patel PM, Partridge BL. Intraoperative monitoring of tibialis anterior muscle motor evoked responses to transcranial electrical stimulation during partial neuromuscular blockade. Anesth Analg 1992;75: Safi HJ, Miller CC III, Carr C, Iliopoulos DC, Dorsay DA, Baldwin JC. Importance of intercostal artery reattachment during thoracoabdominal aortic aneurysm repair. J Vasc Surg 1998;27: Galla JD, Ergin MA, Lansman SL, et al. Use of somatosensory evoked potentials for thoracic and thoracoabdominal aortic resections. Ann Thorac Surg 1999;67: Guerit JM, Witdoeckt C, Verhelst R, Matta AJ, Jacquet LM, Dion RA. Sensitivity, specificity, and surgical impact of somatosensory evoked potentials in descending aorta surgery. Ann Thorac Surg 1999;67: Kouchoukos NT, Rokkas CK. Descending thoracic and thoracoabdominal aortic surgery for aneurysm or dissection: how do we minimize the risk of spinal cord injury? Semin Thorac Cardiovasc Surg 1993;5: Piano G, Gewertz BL. Mechanism of increased cerebrospinal fluid pressure with thoracic aortic occlusion. J Vasc Surg 1990;11: Robertazzi RR, Cunningham JN Jr. Intraoperative adjuncts of spinal cord protection. Semin Thorac Cardiovasc Surg 1998;10: Safi HJ, Campbell MP, Ferreira ML, Azizzadeh A, Miller CC. Spinal cord protection in descending thoracic and thoracoabdominal aortic aneurysm repair. Semin Thorac Cardiovasc Surg 1998;10: Laschinger JC, Cunningham JN Jr, 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:
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