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1 ORIGINAL ARTICLES Preliminary Report of Localization of Spinal Cord Blood Supply by Hydrogen During Aortic Operations Lars G. Svensson, MB, PhD, Vasishta Patel, MD, Joseph S. Coselli, MD, and E. Stanley Crawford, MD Departments of Surgery and Neurophysiology, Baylor College of Medicine and The Methodist Hospital, Houston, Texas One source of paraplegia after aortic operations is the failure to reattach the spinal cord blood supply, the origins of which are not evident at operation. This report is concerned with a rapid new method of identifying these vessels intraoperatively. In 9 pigs, a specially designed catheter with platinum and stainless steel electrodes was inserted intrathecally. Saline solution saturated with hydrogen was injected sequentially into arterial ostia at T-15 to L-4 inclusive, and the generated current impulses from the conditioned platinum electrode were recorded. Of 90 potential segmental arteries supplying the spinal cord, 28 gave rise to spinal radicular arteries. Hydrogen-induced current impulses correctly located 25 of the radicular arteries and all those larger than 180 pm in diameter. When injected with indigo carmine, the vessels localized by the hydrogen-induced current impulses filled the entire anterior spinal artery from the low thoracic to the sacral region, whereas injection of the other vessels did not show filling. After refinement and testing for safety, this method has been employed clinically to rapidly localize and reattach routes of critical cord circulation. (Ann Thoruc Surg 1990;49:528-36) he incidence of paraplegia in patients after replace- T ment of the descending thoracic or thoracoabdominal aorta is reported to be 40% or greater [l-31 despite available modern techniques. Most of these techniques, which include the application of distal aortic perfusion, deep hypothermia, oxygen radical scavengers, allopurinol, calcium-channel blockers, and cerebrospinal fluid drainage alone without other adjuncts have, in our experience, been ineffective in adequately preventing paraplegia [l-2, 4-10]. The likely reason is that the etiology of paraplegia is multifactorial, and thus more than one strategy is needed for the effective elimination of paraplegia. For editorial comment see page 522. The major causes of paraplegia that should be addressed are the degree and the duration of ischemia during aortic cross-clamping [l, 8, 101, and ischemia occurring after unclamping because of failure to reattach to the aortic graft those segmental intercostal and lumbar arteries that supply the spinal cord radicular arteries, including the arteria radicularis magna (ARM) (artery of Adamkiewicz) [lo-161. The latter point poses a dilemma in that, in the interest of reducing the duration of ischemia during aortic cross-clamping, the general practice is to reattach none or only a few of the segmental arteries [l, 2, lo]. Clearly, if there is a failure to reattach the segmental Presented at the Twenty-fifth Anniversary Meeting of The Society of Thoracic Surgeons, Baltimore, MD, Sep 11-13, Address reprint requests to Dr Svensson, Department of Surgery, Baylor College of Medicine, One Baylor Plaza, Houston, TX arteries that supply the spinal cord (not all of them do [Fig l]), this will result in the spinal cord being deprived of its normal source of blood flow when the aorta is unclamped. Amelioration of the depth and duration of ischemia during aortic cross-clamping has been addressed by the use of intrathecal administration of papaverine hydrochloride combined with cerebrospinal fluid drainage [l, 3, 7, 10, 14, 151, which successfully prevented immediate postoperative paraplegia, despite long cross-clamp times, in a series of 34 patients followed up prospectively by one of us (L.G.S.) [15]. Nonetheless, a few days after operation, delayed paraplegia developed in 1 patient and delayed paraparesis developed in 2 patients when the effect of the papaverine would have worn off and the spinal cord was once again dependent on its normal source of blood supply from segmental arteries [l, 151. In none of these patients were the segmental arteries reattached. Both patients with paraparesis recovered. The diverse and complex anatomy of the spinal cord blood supply in nonhuman primates and humans [16] has resulted in a major problem in determining which of the 13 or more pairs of segmental vessels (intercostal or lumbar arteries) arising from the aorta supply the spinal radicular arteries (Fig 2; see Fig 1). Although preoperative highly selective angiography has been advocated [3], the risks involved [ 161, particularly of paraplegia complicating the procedure both in humans and nonhuman primates [13,16,17], has made this an unpopular procedure except in expert hands [3]. In this preliminary report, we present a new hydrogeninduced current impulse (HICI) technique to identify the spinal cord blood supply. This is a qualitative method by The Society of Thoracic Surgeons /90/$3.50

2 Ann Thorac Surg 1990; SVENSSON ET AL 529 c4 I I fi, V,Intercostal a. Fig I. Statistical composite of spinal cord blood supply in primates. The sites of the radicular arteries reflect the most common levels of origin and arrangements found on anatomical dissections. The sizes of the arteries are those of nonhuman primates. The equivalent sizes in humans are: arteria radicularis magna (ARM), 871 pm; anterior spinal artery above the ARM, 231 pm; and anterior spinal artery below the ARM, 941 pm. (After Svensson et a1 [16].) with the potential for allowing the surgeon to determine intraoperatively which segmental vessels can be safely oversewn during aortic operation and which vessels should be reanastomosed to the aortic graft to avoid depriving the spinal cord of its vital blood supply. We also present a new method of eliciting spinal motor evoked potentials directly from the spinal cord. Hydrogen in solution, when in contact with platinum, produces a weak current that can be measured by a sensitive ammeter [18, 191. For our new technique, we hypothesized the following: First, because hydrogen readily crosses tissue membranes [18], if injected into a segmental artery supplying the anterior spinal artery, it would readily traverse the anterior spinal artery wall and the spinal cord pia mater and thus be detected by a platinum electrode lying on the surface of the spinal cord, as opposed to being detected by an electrode within the neural tissue of the spinal cord. Second, that if the platinum electrode was close enough to the anterior spinal artery, the response to a hydrogen injection would be almost immediate. Third, that if an HICI was elicited, this would indicate that a segmental artery supplying the spinal cord had been injected. The results of this new technique in a series of porcine experiments and the application of these findings with respect to humans are discussed. Material and Methods Nine domestic pigs, 27.5 to 32 kg in weight (mean weight, 29.7 t 1.5 kg), were sedated with ketamine hydrochloride (20 mg/kg), intubated, and ventilated by a Harvard ventilator with halothane, oxygen, and nitrous oxide. Catheters were placed through the femoral vein into the right atrium for central venous pressure monitoring and fluid administration, through the femoral artery into the infrarenal abdominal aorta for distal aortic pressure monitoring, and through the brachial artery into the proximal aorta for proximal aortic pressure monitoring. The electrocardiographic tracing was monitored continuously on a Beckman oscilloscope and recorder. The animals were turned on their right sides, and a specially constructed spinal catheter with platinum and stainless steel electrodes was introduced intrathecally either by a lumbar puncture (n = 1) or a laminectomy (n = 8) into the spinal canal alongside the spinal cord. The electrodes were connected respectively to a sensitive ammeter and an electrical stimulator for elicitation of motor evoked responses and potentials. A potentiating current was applied to the platinum electrode to condition it as described by others [ A thoracoabdominal incision was performed, and the aorta was cross-clamped above the diaphragm and at the aortic trifurcation. In 4 animals, an intrathecal injection k 1 Anterior spinal a., w Fig 2. Arrangements of segmental intercostal or lumbar arteries and the origin of radicular arteries coursing to the anterior spinal artery. Note that the radicular arteries cannot be seen intraoperatively unless the overlying tissues are dissected ojf the vertebral bodies, including the psoas muscle in the abdomen. Both radicular arteries, one radicular artery, or no radicular artery can be present at any specific level.

3 530 SVENSSON ET AL Ann Thorac Surg 1990;49:52%36 Fig 3. Experimental procedure. Note that the proximal aorta, lying on the vertebral bodies (Ll- U), has been cross-clamped. The more distal aorta has been opened, and saline solution saturated with hydrogen has been injected into the lumbar artery giving off a radicular artery that supplies the anterior spinal artery (Ant. spinal a.) and spinal cord. The more distal platinum electrode (P) detects the hydrogen-induced current impulse. (ARM = arteria radicularis magna; S = stainless steel electrode.) of papaverine was administered before aortic crossclamping. The aorta was opened and segmental arteries, that is, the intercostal and lumbar arteries, were sequentially injected by hand with 10 ml of saline solution saturated with hydrogen (Fig 3). Each injection procedure took approximately 30 seconds to one minute to perform, and the HICI response was noted within 5 seconds of injection. The HICI produced was monitored and recorded to see if any hydrogen reached the spinal cord. Figure 4 shows an example of an HICI tracing. If an HICI was elicited, the artery was noted for later dye studies. After all the arteries from T-15 to L-4 inclusive had been injected, those arteries that had been shown to be associated with an HICI were reinjected to confirm the current response. The animals were then given a lethal concentrated solution of potassium chloride. Indigo carmine was injected into the ostia of segmental arteries as follows: In 3 animals, the dye was injected into the HICI-localized arteries and then the segmental arteries were dissected out from the aorta to the spinal radicular arteries on the spinal cord. In 2 animals, the segmental arteries were dissected free, the anterior vertebral column was removed, the spinal cord was exposed, and the segmental arteries were then injected. In 1 animal, the arteries not localized by the HICI technique were injected. Fig 4. Tracing of hydrogen-induced current impulses in animal 3. (L = lumbar level;.l and.r = left and right lumbar artery ostium, respectively.) In another 3 animals, the nonlocalized arteries were injected, the cord was exposed, and then the localized arteries were injected. In none of the animals were the segmental arteries damaged or dissected by the injections on gross examination. The accuracy of the HICI technique in detecting the spinal radicular arteries compared with that of the anatomical dissections of the dye-stained arteries was then correlated. The diameter of the anterior spinal artery above and below the ARM and of the other radicular arteries was measured with a vernier using magnification. Spinal motor evoked potentials were elicited in 5 pigs using a Metraco stimulator and evoked potential system, and the motor evoked potentials were viewed on a Kikusui C oscilloscope and recorded continuously on an Apple IIE computer for later analysis of the waveform. Electrode deviations in the right and left hip extensor muscles were recorded. The electromyographic activity was filtered using a low-frequency filter of 0.5 Hz and a high-frequency filter of 3,000 Hz. Full-scale gain was initially set at 2800 mv. Stimulus intensity was gradually increased to 10% above the threshold level using 100-ms pulse duration. Usually single responses were measured. At times, up to ten spinal motor evoked potentials were averaged, at a stimulus rate of 9.7 per second. Spinal motor evoked potentials were elicited at a maximum of five-minute intervals. When the evoked potentials markedly decreased in amplitude or disappeared, larger stimulus voltages were used to try to elicit a response. The animals received humane care in compliance with the Guide for the Care and Use of Laboratory Animals published by the National Institutes of Health (NIH Publication No , revised 1985). Results Hydrogen-induced current impulses were detected in every animal and occurred immediately after injection of

4 Ann Thorac Surg 1990;49: SVENSSON ET AL 531 Table 1. Hydrogen-Induced Current Impulse-Localized Spinal Radicular Arteries and Those Identified During Anatomical Dissections Anterior Spinal Arteria Artery Diameter Radicularis Magna and Animal Diameter No. Ostia Localized" Radicular Arteries Identified and Diameter (pm)b*' Aboved,' Belowd,' (pm) Rt L-2 Lt L-2, Lt L-4 Lt L-2, Lt L-3, Rt L-3" Lt L-4, Rt L-4 L-2, Lt L-4 L-2, L-4, L-2, Lt L-4, Rt L-4 Lt L-2, Lt L-3, Lt L-4 Lt T-15, Lt L-1, Lt L-2, Rt L-3, Lt L-4 Lt L-3, Lt L-4, Rt L-4 Rt L-2, 250 Lt L-2, 200; Lt L-4, 225 Lt L-2, 325; Lt L-3, 250 Lt L-4, 430; Rt L-4, 300 Rt L-1, Mob; Rt L-2, 351; Lt L-4, 450 Rt L-2, 275; Rt L-4, 325 Lt L-1, 180b; Lt L-2, 205; Lt L-4, 275; Rt L-4, 300 Lt L-1, 180b; Lt L-2, 351; Lt L-3, 405; Lt L-4, 455 Lt T-15, 380; Lt L-1, 380; Lt L-2, 200; Rt L-3, 430; Lt L-4, 550 Lt L-3, 180; Lt L-4, 225; Rt L-4, Lt L-5, 250 Lt L-5, 300 Lt L-4, 430 Lt L-4, 450 Lt L-5, 355 Rt L-5, 275 Rt L-5, 385 Rt L-5, 550 Rt L-5, 500 a There were 26 ostia localized with one false-positive result. There were 28 arteries identified with three false-negative results. The radicular artery diameters were significantly greater in the papaverine-treated animals (p < 0.025; Mann-Whitney U test = 107) compared with the nontreated animals. Above and below arteria radicularis magna. Significance: p = 0.05 between papaverine-treated animals and nontreated animals. Significance: p = 0.02 between papaverine-treated animals and nontreated animals. g This animal received papaverine. L = lumbar level; Lt = left; Rt = right; T = thoracic level the hydrogen solution. Furthermore, in every animal, radicular arteries supplying the spinal cord were correctly localized on postmortem examination (Table 1). Moreover, these localized radicular arteries were shown to perfuse the entire spinal cord from the lower thoracic segment to the caudal tip of the spinal cord with dye injections. None of the nonlocalized arteries injected with dye filled the anterior spinal artery. Of interest, in every animal, the anterior spinal artery was also found to be continuous over these segments. Of 90 potential segmental arteries supplying the spinal cord radicular arteries, some arising as pairs from a common aortic ostium, 28 supplied the spinal cord on postmortem examination, and of these, 25 (89%) were correctly localized as supplying the spinal cord by hydrogen injections. The three radicular arteries that were not identified were 180 pm in size and at least three vertebral levels further away from the platinum electrode (see Table 1). However, by increasing the sensitivity of the technique, we would probably have been able to detect these vessels. In 1 animal (animal 3; see Table l), a small HICI measuring 16% of the highest recorded amplitude in this animal was noted, but no radicular artery was identified on the right at that level, although large radicular arteries, which had been correctly localized, were present on the left and at the segments immediately adjacent to it. Collateral blood flow to the correctly localized adjacent radicular artery may have accounted for this weak response. In this same animal, in which five radicular arteries were localized, there was a direct correlation between the size of the radicular artery and the height of the recorded current peak impulse (12 = 0.98; standard error of the mean, 0.147; p < 0.01) (Fig 5). The initial upstroke height of the HICI peak appears to be the best indicator of vessel size rather than the downstroke or area under the curve; however, this requires further research. Figures 6 and 7 show spinal cord specimens and the HICI-identified arteries from animals 2 and 4, respectively. Figure 8A shows a spinal cord specimen (animal 8) after the lumbar arteries not supplying the spinal cord, as determined by the hydrogen-saline technique, were injected with indigo carmine. None of the dye reached the anterior spinal artery. Figure 8B shows the same spinal cord after the localized lumbar arteries were dissected free to their respective vertebral foramens where the spinal radicular arteries arise. The lumbar artery ostia were then injected with dye. Note that the radicular arteries and the continuous anterior spinal artery were then filled with dye for the entire extent from the lower thoracic spinal T I Arbitary Current Units I L3RT.. L4RT. L2RT L3LT. L4Ll Size (Urn) Fig 5. Linear correlation between radicular artery size and hydrogeninduced current impulse amplitudes in animal 3 (? = 0.098; p < 0.01). See Table I. (L = lumbar level; LT = left; RT = right.)

5 532 SVENSSON ET AL Ann Thorac Surg 1990;49:52%36 Fig 6. Spinal cord specimen from and identified radicular arteries in animal 2. The catheter with the electrodes is 1.6 mm (1,600 p m ) in diameter. Arterial diameters are given in Table 1. ( x 2 before 38% reduction.) (ARM = arteria radicularis magna; ASA = anterior spinal artery: ASV = anterior spinal vein; CaSC = caudal spinal cord: CrSC = cranial spinal cord: L = lumbar artery level; LA = lumbar artery; Lt = left; Pt = platinum electrode; SS = stainless steel electrode.) cord down to the sacrum. In every other animal in which the localized lumbar artery ostia were injected with dye, both the radicular arteries and the anterior spinal arteries were filled with dye. The spinal motor evoked potential amplitudes progressively decreased with time after cross-clamping, and by 18.5 minutes (standard deviation,? 3.1 minutes), they were unrecordable or reduced to less than 10%of baseline values. In 3 animals in which responses were evoked at one-minute intervals, this decrease was observed to be briefly preceded Fig 7. Spinal cord specimen from and identified radicular arteries in animal 4. Arterial diameters are given in Table I. ( ~ 1. 5before 38% reduction.) (AB = aortic button; Rt = right; other abbreviations are the same as in Figure 6.) by an initial increase in amplitude of the responses. As expected, the systolic blood pressure increased after aortic cross-clamping(before, 92? 10.2 mm Hg [mean? standard error of the mean], and after, 108? 12.3 mm Hg; p < 0.05) as did the central venous pressure (before, 16? 1.8 mm Hg, and after, 19? 3.3 mm Hg; p < 0.05) [8, 151. Comment This study has shown that the critical segmental lumbar or intercostal arteries that supply the spinal cord can be

6 SVENSSON ET AL 533 Fig 8. (A) Spinal cord specimen from animal 8 shows the failure of dye to reach the spinal cord when injected into the segmental arteries not identified as supplying the spinal cord. ( X 1.7 before 38% reduction.) (B)After injection of dye into the segmental arteries shown by hydrogeninduced current impulses to supply the spinal cord, the spinal radicular arteries and the entire continuous anterior spinal artery are opacified. ( ~ 2. before 8 38% reduction.) (C = catheter for dye injection; all other abbreviations are the same as in Figure 7.) A B accurately and rapidly localized intraoperatively by the use of HICIs. Thus, we propose that if these localized segmental artery ostia can be successfully reanastomosed to a new aortic graft, then the blood supply should be reestablished to the spinal cord. With this new technique, with further testing in live animal experiments for safety and influence on postoperative paraplegia rate, and with appropriate refinement for clinical use, it is likely that the incidence of postoperative paraplegia, particularly delayed paraplegia, can be reduced in humans. Our three hypotheses concerning our technique have been confirmed by the findings. First, hydrogen readily crosses the intervening membranes between the blood and the platinum electrode placed on the spinal cord, as opposed to being placed in the neural tissue. Second, the HICI is immediately detected in the recording platinum electrode. Third, the ostium of a segmental artery that supplies a spinal radicular artery and is injected with hydrogen-saturated saline solution can be accurately localized to supply the anterior spinal artery. Previously, the hydrogen polarographic technique was used to measure tissue blood flow [18, 191 by insertion of a platinum probe into the tissue under study. This was done by achieving a constant concentration of hydrogen

7 534 SVENSSON ET AL Ann Thorac Surg 1990;49:52%36 E- 1.fi 0.2 L3 L4-5 ARM Site Fig 9. Approximate frequency of origin of the arteria radicularis magna (ARM) according to vertebi,al levels in humans. (L = lumbar artey level; T = thoracic artey level.) (After Svensson et a ) and a steady-state in the tissues [18, 191. The hydrogen source was then discontinued, and the rate of tissue clearance of hydrogen was used to calculate the tissue blood flow by the Fick principle [18, 191. In these experiments, however, we could not measure spinal cord blood flow per se in milliliters per 100 grams of tissue per minute with our present methods probably because the hydrogen was injected under pressure and the sensing electrode was on, rather than in, the spinal cord tissue. Furthermore, the rate of decline of HICI appeared to be dependent on the distance the electrode was from the anterior spinal artery. Thus, many of the elicited HICI peaks were asymmetrical. Nevertheless, the source of the spinal cord blood supply was accurately localized. Although we [l, 161 have previously noted on lateral roentgenograms that intrathecal catheters lie anterior to the spinal cord in humans, in these experiments, if the platinum electrode was not situated exactly alongside the anterior spinal artery, an HICI response was still measurable, even if the electrode was alongside the ligamenta denticulata of the spinal cord. Furthermc,ie, in our experience, radicular arteries were localized up to five spinal cord vertebral segments from the platinum electrode. Nonetheless, we did try to position the electrode as distally as possible on the anterior spinal cord, as we [7, 161 have previously shown that, during aortic crossclamping, blood flow is probably in a cranial to caudal direction in the anterior spinal artery. Using two platinum electrodes, this appeared to be confirmed in 2 animals. Thus, any hydrogen injected upstream from the catheter is detected further caudally. We therefore speculate that as we have placed the tip of intrathecal spinal catheters as high as vertebral level T-10 in humans, approximately the level of spinal cord segments L-2 to L-3, then those radicular arteries, including the largest, the ARM, that usually arise in 90% of patients between T-8 and L-3 (Fig 9) [16] should be able to be accurately localized. Although three very small radicular arteries at the furthest cranial distance from the platinum electrode were missed in these animal experiments, in similar-weight nonhuman primates (Pupio ursinus), we [16] have shown that the ARM (mean, 688 pm) and anterior spinal artery (means: above ARM, 278 pm; and below ARM, 744 pm [see Fig 11) are considerably larger than those in untreated pigs (means: ARM, 391 pm; above ARM, 199 pm; and below ARM, 443 pm [see Table 11) and therefore are less likely to be missed. Furthermore, in our human adult spinal cord dissections, both the ARM (mean, 871 pm) and the anterior spinal artery (means: above ARM, 231 pm, and below ARM, 941 pm) were generally even larger [ 161. Although the purpose of this study was not to statistically analyze the comparative anatomy of human, nonhuman primate, canine, and porcine spinal cords, we did examine injected postmortem specimens of both canine and porcine spinal cords with a view to their suitability for this study. We selected the pig for these experiments because the ARM (artery of Adamkiewicz) arises fairly consistently from the lower lumbar arteries, which simplifies the experimental procedure. Furthermore, the arrangement of the spinal radicular arteries above the ARM were analogous to those present at a higher level in primates [16], although the porcine radicular arteries are smaller and more numerous. Of interest, in the 9 porcine spinal cord specimens we studied, the anterior spinal artery, although small when compared with that of primates, was continuous from the midthorax to the sacrum. An important difference, which has been noted before [21], is that the spinal cord in the pig terminates at a lower vertebral level than in primates, and therefore, a laminectomy is the preferable route for introducing a catheter rather than through a percutaneous lumbar puncture. We have previously reported our success in protecting the spinal cord from ischemia during aortic crossclamping in both nonhuman primates [7] and humans [l, 14, 151 by the use of intrathecal administration of papaverine. However, in the nonhuman primate experiments, the segmental intercostal or lumbar arteries were rarely sacrificed, and thus the spinal cord blood supply was reestablished when the aorta was unclamped. The advantage of intrathecal administration of papaverine combined with this new HICI technique is that, apart from possibly increasing its sensitivity by dilating the radicular arteries (p < 0.025; see Table 1) and anterior spinal artery (p < 0.05; see Table l), the papaverine may allow more time for the reanastomosis of critical segmental arteries. The additive protection of both these evolving techniques and the use of distal aortic perfusion under certain circumstances [lo, 221 requires further research but may reduce the incidence of paraplegia after aortic operations. The role of spinal and cortical motor evoked potentials requires further evaluation; however, our [7, 81 earlier results with cortical and spinal stimulation were accurate and encouraging reviews have been published [23]. In conclusion, this study has addressed the problem of localizing segmental arteries that supply the spinal cord so that they can be reattached during aortic replacement, thus reestablishing the blood supply to the spinal cord. We have shown that in the porcine model, the radicular arteries supplying the spinal cord can be accurately and rapidly localized using HICIs and that the entire spinal

8 Ann Thorac Surg 1990; SVENSSON ET AL 535 cord from the lower thoracic segments to further caudally can be perfused by these radicular arteries. Currently we are studying the safety of this method and the influence of preservation or occlusion or perfusion of HICI-localized segmental arteries, combined with motor evoked potentials, on the incidence of postoperative paraplegia in the porcine model. With further refinement and testing for safety, we have used this technique, including spinal motor evoked potentials, in humans to rapidly identify segmental arteries that supply the spinal cord, which then have been reattached during aortic replacement to preserve spinal cord function. Supported by Dr Michael E. DeBakey, Chairman of the Department of Surgery, through The DeBakey Heart Fund. Carol Pienta Larson, Department of Medical Illustration, prepared the artwork, and J. C. Brown IV prepared the manuscript. Cedric Sheffield, MD, assisted with five of the experiments. References Svensson LG, Stewart RW, Cosgrove DM, et al. Intrathecal papaverine for the prevention of paraplegia after operation on the thoracic or thoracoabdominal aorta. J Thorac Cardiovasc Surg 1988;96: Crawford ES, Crawford JL, Safi HJ, et al. Thoraco-abdominal aortic aneurysms: preoperative and intraoperative factors determining immediate and long-term results of operations in 605 patients. J Vasc Surg 1986;3: Kieffer E, Richard T, Chivas J, Godet G, Cormier E. Preoperative spinal cord arteriography in aneurysmal disease of the descending thoracic and thoracoabdominal aorta: preliminary results in 45 patients. Ann Vasc Surg 1989;3:344. Crawford ES, Mizrahi EM, Hess KR, Coselli JS, Safi HJ, Pate1 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: Crawford ES, Walker HSJ 111, Saleh SA, Norman NA. Graft replacement of aneurysm in descending thoracic aorta: results without bypass or shunting. Surgery 1981;89:83-5. Crawford ES, Coselli JS, Safi HJ. Partial cardiopulmonary bypass, hypothermic circulatory arrest, and posterolateral exposure for thoracic aortic aneurysms operation. J Thorac Cardiovasc Surg 1987;94: Svensson LG, Von Ritter CM, Groeneveld HT, et al. Crossclamping of the thoracic aorta: influence of aortic shunts, laminectomy, papaverine, calcium channel blockers, allopurinol, and superoxide dismutase on spinal cord blood flow and paraplegia in baboons. Ann Surg 1986;204: Svensson LG, Rickards E, Coull A, et al. Relationship of spinal cord blood flow to vascular anatomy during thoracic aortic cross-clamping and shunting. J Thorac Cardiovasc Surg 1986;91: Svensson LG, Antunes MDJ, Kinsley RH. Traumatic rupture of the thoracic aorta: a report of 14 cases and a review of the literature. S Afr Med J 1985; Svensson LG, Loop FD. Prevention of spinal cord ischemia in aortic surgery. In: Bergan JJ, Yao JST, eds. Arterial surgery: new diagnostic and operative techniques. New York Grune & Stratton, Crawford ES, Palamara AE, Saleh SA, Roehm JOF. Aortic aneurysms: current status of surgical treatment. Surg Clin North Am 1979;59: Fried LC, DiChiro G, Doppman JL. Ligation of major thoraco-lumbar spinal cord arteries in monkeys. J Neurosurg 1969;31: Svensson LG, Hinder RA. Hemodynamics of aortic crossclamping: experimental observations and clinical applications. Surg Annu 1987;19: Svensson LG, Stewart RW, Cosgrove DM, et al. Preliminary results and rationale for the use of intrathecal papaverine for the prevention of paraplegia after aortic surgery. S Afr J Surg 1988;26: Svensson LG, Grum DF, Bednarskii M, et al. Appraisal of CSF alterations during aortic surgery with intrathecal papaverine administration and CSF drainage. J Vasc Surg 1990; Svensson LG, Klepp P, Hinder RA. Spinal cord anatomy of the baboon: comparison with man and implications on spinal cord blood flow during thoracic aortic cross-clamping. S Afr J Surg 1986; DiChiro G, Fried LC, Doppman JL. Experimental spinal cord angiography. Br J Radio1 1970;43: Young W. H, clearance measurement of blood flow: a review of technique and polarographic principles. Stroke 1980; 11: Aukland K, Bower BF, Berliner RW. Measurement of local blood flow with hydrogen gas. Circ Res 1964; Senter HJ, Burgess DH, Metzler J. An improved technique for measurement of spinal cord blood flow. Brain Res 1978; 149: Delmann H-D, McClure RC. Porcine nervous system. In: Getty R, ed. Sisson and Grossman s the anatomy of the domestic animals. Philadelphia: W.B. Saunders, 1975: Svensson LG, Coselli JS, Safi HJ, Hess KR, Crawford ES. Appraisal of adjuncts to prevent acute renal failure after surgery on the thoracic or thoracoabdominal aorta. J Vasc Surg 1989; 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: DISCUSSION DR AHMAD RAJAII-KHORASANI (Boston, MA): The importance of localization of the spinal cord blood supply becomes more evident when I discuss my technique for aortic operations. First, however, let me point out that both Dr Cooley and Dr Crawford have mentioned that whether you reimplant the intercostal arteries or not, the chance of paraplegia is the same. This bitter experience is, in a way, predictable considering the sensitivity of the central nervous system tissues to ischemia. In other words, if these vessels are critical to the spinal cord blood supply, by the time they are reimplanted, the damage has already been done. The technique that I have used since 1986 involves use of a high-flow shunt with a branched sidearm. (The sidearm can also originate from the inflow line of the bypass machine.) This system makes possible adequate distal perfusion as well as perfusion of the excluded intercostals. Adherence to the follow-

9 536 SVENSSON ET AL Ann Thorac Surg 1990;49: ing principles is essential (1) maintain adequate distal circulation; (2) minimize the number of excluded intercostals by proper choice of clamp site and avoid clamp injury to the neighboring intercostals; (3) reperfuse the excluded intercostals immediately after aortotomy; and (4) reimplant these intercostals to the side of the aortic graft without interruption of their blood flow. This technique will minimize the chance of spinal cord ischemia, and with localization of the spinal cord blood supply, the technique can be simplified tremendously. Further investigation, especially with animals that have variation in spinal cord blood supply, is needed. DR SAFEH ATTAR (Baltimore, MD): Dr Svensson, in your experimental results, you indicated that drainage of the cerebrospinal fluid was not helpful in the prevention of paraplegia. Now, you present a series in which you used papaverine and cerebrospinal fluid drainage combined and cerebrospinal fluid drainage by itself. Did you use papaverine by itself to see its effect? Also, in a personal communication, Larry Hollier at the Ochsner Clinic indicated that he had operated on 50 patients with thoracoabdominal aortic aneurysms using cerebrospinal fluid drainage and reimplantation of all the involved intercostal and lumbar arteries. There were only 2 cases of paresis, which improved after onset by drainage of the cerebrospinal fluid. How do you reconcile this? This is a practical way of preventing paraplegia that has been proved clinically. DR SVENSSON Dr Rajaii-Khorasani, with reference to reanastomosis of the intercostals by Dr Cooley and Dr Crawford, I must state on Dr Crawfords behalf that he has stressed the importance of reanastomosis of the intercostals in two reports, one in 1979 in Surgical Clinics of North America and one in 1986 in The Journal of Vascular Surgery. Concerning perfusion of the spinal cord, the matter does not appear to be resolved in human studies. My colleagues and I in Houston do not believe that distal aortic perfusion in humans has much advantage in operations for the medial degeneration type of thoracoabdominal aneurysm, partly for anatomical reasons that I have explained. As for your operative technique, I believe that it is similar to the original technique of repairing thoracoabdominal aneurysms. The reason that technique was abandoned was the high mortality rate. Currently in our prospective randomized study of cerebrospinal fluid drainage, we have a 30-day mortality rate of 3%. The effort to prevent paraplegia should not be accomplished at the expense of an increased mortality rate. Dr Attar, in answer to your questions about intrathecal papaverine, we did not use intrathecal papaverine alone in the animal studies because we had either done a laminectomy or inserted a catheter; therefore, cerebrospinal fluid was lost. Thus, papaverine was used with cerebrospinal fluid drainage. In the study just presented, we did not, however, evaluate the effect of these measures or HICI localization on postoperative paraplegia. This will be the subject of further research. With reference to the results from the Ochsner Clinic under the auspices of Dr Hollier, McCullough and associates reported that many of those patients had Crawford type 111 or IV aneurysms, which have an expected combined rate of paraplegia and paresis of only 3.2% and 2.1%, respectively. Thus, they were low-risk patients. We are currently testing the effect of cerebrospinal fluid drainage alone in a prospective randomized study in high-risk patients with a combined paraplegia and paresis rate in the control group running at about 25% to 30%. To date, we have found no significant advantage with cerebrospinal fluid drainage alone. We will report these results when we have completed the study. Cerebrospinal fluid drainage alone was used in animal experiments more than 20 years ago. Recently, there has been a resurgence of research to try to determine whether such drainage is advantageous. Nonetheless, Dr Cooley and Dr Blaisdell have both commented that cerebrospinal fluid drainage alone did not prevent paraplegia or paresis in experiments they reported in Later in 1965, Dr Killen and colleagues repeated the studies and found no protective effect of cerebrospinal fluid drainage from the cisterna magna in dogs. This is the technique that is still used today in canine experiments. There appears to be little advantage in using cerebrospinal fluid drainage alone without other adjuncts.

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