P operations on the thoracic aorta. The reported incidence
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1 Regional Deep Hypothermia of the Spinal Cord Protects Against Ischemic Injury During Thoracic Aortic Cross-Clamping Richard P. Salzano, Jr, MD, Lee H. Ellison, MD, Paul F. Altonji, MD, James Richter, MD, and Peter J. Deckers, MD Departments of Surgery and Anesthesiology, Hartford Hospital, Hartford, Connecticut We tested in pigs the hypothesis that regional deep hypothermia of the spinal cord achieved by cerebrospinal fluid cooling will protect against ischemic injury during thoracic aortic cross-clamping. Eight control animals underwent aortic cross-clamping at the distal aortic arch and just above the diaphragm for 30 minutes. Eight experimental animals had placement of two subarachnoid perfusion catheters through laminectomies at T4 and the lower lumbar region. The subarachnoid space was perfused with normal saline solution at 6 C delivered by gravity infusion, with infusion rates adjusted to maintain cord temperatures at less than 20 C. After 30 minutes of aortic cross-clamping, the infusion was stopped and the cord allowed to warm to body temper- ature. Hind limb neurologic function was graded by Tarlov s scale. All of the animals in the control group had complete hind limb paraplegia (Tarlov grade 0) postoperatively. Seven of the 8 animals in the experimental group had preservation of hind limb motor function (Tarlov grade 2), and 1 animal had complete hind limb paraplegia (Tarlov grade 0) (p = 0.002, Fisher s exact test). We conclude that regional deep hypothermia of the spinal cord in pigs does provide some protection from ischemic injury during thoracic aortic cross-clamping. Clinically this may be a useful adjunct for prevention of paraplegia during thoracic aortic operations. ( 1994;57:65-71) araplegia remains a major devastating complication of P operations on the thoracic aorta. The reported incidence of neurologic complications ranges from 6.5% to 40% [l, 21 and depends on the nature and extent of disease, indications for operation, age of the patient, duration of aortic cross-clamp time, and type of reconstruction. End-organ spinal cord ischemia seems to be the mechanism of injury [3], and numerous adjuncts aimed at preventing ischemia have been tried clinically and experimentally, with conflicting results. The adjuncts include aortic shunts [l], cerebrospinal fluid (CSF) drainage alone [4] or combined with other modalities [57], infusion of free radical scavengers [&lo], calcium-channel blockers [ll], and direct intrathecal injection of agents [ There appears to be a safe time period for aortic crossclamping beyond which the incidence of paraplegia increases greatly [l]. Hypothermia is used widely in clinical surgery as a protective agent for temporary central nervous system ischemia, as it reduces tissue metabolic rate and oxygen requirements. There is a linear relationship between temperature and duration of ischemia tolerated by the spinal cord, with safe ischemic time increased roughly 5 minutes by each 1 C reduction in temperature [16]. Anatomically, the spinal cord is suspended in a fluid bath of subarach- Presented at the Twenty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 2527, Address reprint requests to Dr Ellison, 85 Seymour St, Suite 325, Hartford, CT noid CSF, which can be easily accessed. Selective cooling of this bath might cool the spinal cord while avoiding the untoward effects of systemic hypothermia and thus might prolong safe ischemic time during thoracic aortic crossclamping. The purpose of this study was to examine the effects of selective CSF cooling on spinal cord and systemic temperatures and to determine if selective spinal cord hypothermia is protective against ischemic injury from double thoracic aortic cross-clamping. Material and Methods All experiments were conducted 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). A total of 20 adult pigs weighing 17 to 26 kg were used. The animals were initially immobilized with an intramuscular injection of tiletamine hydrochloride and zolazepam hydrochloride, 100 mg. All animals underwent mask inhalation induction of anesthesia using either an oxygenhalothane or oxygen-isoflurane mixture. Shortly after induction, a cuffed endotracheal tube was inserted, and the lungs were ventilated with an Ohio 560 ventilator. The ventilatory rate, tidal volume, or both were adjusted to maintain the carbon dioxide tension between 35 and 45 mm Hg and the oxygen tension greater than 200 mm Hg, as determined by periodic blood gas measurement (CibaKorning 238 blood gas machine). General by The Society of Thoracic Surgeons /94/$7.00
2 66 SALZANO ET AL 1994; anesthesia was maintained with either oxygen-halothane (0.5% to 1.5%) or oxygen-isoflurane (0.5% to 2.0%), supplemented with intravenously administered fentanyl (10 After intubation, two peripheral venous lines and a right femoral artery line were established. The venous lines were maintained with either normal saline solution or Ringer s lactate at a rate of 50 ml * kg- * h-. There was continuous monitoring of the electrocardiogram, femoral artery or proximal aortic arch pressure, and rectal temperature in all animals (Hewlett-Packard monitor model 78304A). All animals were placed on warming blankets at 40 C to maintain rectal temperatures of 35 to 38 C. Prelimina y Studies on Spinal Cord Temperatures and Pressures The preliminary studies were conducted on 4 animals. The pigs were initially placed in the prone position and underwent laminectomies in the upper thoracic and lower lumbar areas. Direct dural incisions were made at each site at the T4 and L5 levels, and a Codman model drainage ventricular catheter was inserted into the subarachnoid space at each level. The dural incisions were closed with 6-0 Prolene (Ethicon, Somerville, NJ) sutures when necessary to maintain a watertight system. Continuous temperature monitoring at inflow (T4) and outflow (L5) was provided by wire thermistors mounted in side ports on the perfusion lines and connected to a Yellow Springs Instrument model 2100 thermistor telethermometer. Infusion of normal saline solution at 6 C was by gravity at rates of 25 to 30 mumin. In 2 animals, for preliminary measurement of spinal cord core temperatures, needle-tipped thermistors (Yellow Springs Instrument tissue implantation probe model Y00520) were placed through the ldura and directly into the gray matter of the spinal cord at levels T6 and L3 and connected to a Yellow Springs Instrument model 2100 thermistor telethermometer. In the other 2 animals, for preliminary measurement of CSF pressures, a 22-gauge catheter was placed alongside the outflow ventriculostomy catheter, and pressures were continuously transduced. The animals were sacrificed by lethal injection of potassium chloride after the experiments. Experimental Procedure of lschemia and Hypothermia Sixteen pigs underwent the experimental procedure. In the 8 control animals, anesthesia and monitoring were carried out as already described. These animals did not undergo laminectomies. They were placed in the right lateral position and underwent thoracotomies at the fourth and eight interspaces. An 18-gauge catheter was placed in the aortic arch for continuous proximal arterial pressure monitoring. The aorta was cross-clamped just distal to the subclavian artery and just above the diaphragm. The total cross-clamp time was 30 minutes. Proximal aortic pressure during cross-clamping was maintained at 100% to 150% of postinduction levels with supplemental fentanyl when necessary. The 8 experimental animals initially were placed in the Table 1. Preliminam Temperature Studies Temperature ( C) Variable Start Minutes Minutes Minutes Minutes Body T6 Cord L3 Cord Perfusate Effluent prone position and underwent insertion of the subarachnoid ventriculostomy catheters. To minimize mechanical spinal cord trauma, these animals did not have placement of subarachnoid pressure catheters or needle-tipped thermistors. They were turned laterally and had subarachnoid perfusion of iced saline solution exactly as in the preliminary-study animals. After 45 minutes of perfusion, the aorta was double cross-clamped exactly as in the control animals, and the subarachnoid perfusion continued throughout the entire 30 minutes of aortic cross-clamping. Proximal aortic pressure was maintained at 100% to 150% of postinduction levels. With the release of the aortic clamps, the infusion was stopped, the catheters were removed, and the cord w,as allowed to return to core temperature without further perfusion. After release of aortic cross-clamps, all incisions were closed, and the lungs were reexpanded with a chest tube and positive-pressure ventilation. In the experimental animals, the dura was closed to prevent further leak of CSF. All animals were allowed to completely recover from anesthesia and when completely awake, were graded for neurologic function by use of Tarlov s scale [17]: 0 = complete paraplegia, no voluntary movement; 1 = perceptible movement of joints, minimal voluntary movement; 2 = good movement of joints, inability to stand; 3 = ability to stand and walk with some spastic running; 4 = normal, complete recovery. Animals were sacrificed by lethal injection of potassium chloride, and spinal cords were immediately harvested and fixed in formalin for histologic evaluation. Statistical Analysis Differences in mean values and standard deviations were compared by Student s t test. Neurological outcomes between the two groups were compared by Fisher s exact test. Differences were considered significant at a p value of less than Results Prelimina y Studies on Spinal Cord Temperatures and Pressures The thermistors placed inbo the spinal cord in 2 animals allowed continuous cord temperature measurements at two levels during subarachnoid perfusion cooling, and these readings were correlated with measured effluent temperatures. The averaged results for the 2 animals are
3 1994; SALZANO ET AL 67 REGIONAL SPINAL CORD HYFOTHERMIA 0 v) w W a 0 W n BODY TEMP. \-. EFFLUENT - _I L3 CORD T6 CORD ] : I D - - PERFUSATE 0, I 1 A Start Min. Min. Min. Min. TIME Fig 1. Preliminary temperature studies relating cord temperatures to perfusate temperatures over time. shown graphically in Table 1 and plotted in Figure 1. A steady state was achieved in each animal at approximately 30 minutes for a flow rate of 25 ml/min, with little variation subsequently. Effluent temperatures were measured extracorporeally at a distance from the laminectomy site, which may explain why effluent temperatures were higher than distal cord temperatures once a steady state was achieved. At 30 minutes, both animals had a measured lumbar cord temperature of less than 20"C, and it remained there for the remainder of the perfusion. Animals recovered and had normal neurological function. The 2 animals with distal subarachnoid pressure catheters had an opening pressure of 8 mm Hg. There was occasional variation in the pressures during infusion, but neither animal sustained elevations higher than 12 mm Hg during infusion. Experimental Procedure of lschemia and Hypothermia Postinduction mean arterial blood pressure was not significantly different between the control group and the experimental group ( mm Hg versus 76 * 16 mm Hg, respectively; p = 0.651). During the 45-minute period of spinal cord perfusion cooling, the mean blood pressure fell significantly in the experimental group to mm Hg (p = 0.016) just prior to clamping. After 15 minutes of cross-clamping, each group showed an increase in mean blood pressure to levels not significantly different between the groups (controls, mm Hg, and experimental group, 131 f 10 mm Hg; p = 0.5). The mean blood pressure was similar between the two groups 10 minutes after clamp removal (controls, mm Hg, and experimental group, 70 * 6 mm Hg; p = 0.382) and did not differ from postinduction blood pressure in either group. Femoral artery pressures during cross-clamping ranged from 8 to 11 mm Hg in all animals in both groups. Temperature data from the experimental animals showed similar trends to those in the preliminary-study animals (Table 2; Fig 2). Core temperature declined slightly but significantly over the course of subarachnoid perfusion despite attempts to warm the animals (37.6" 0.6"C versus 35.1" 2 1.0"C; p < ). A steady state in Table 2. Mean Effluent and Body Temperatures in Experimental Animals" Time (min) Start Clamps on 15 Clamps off 10 Body Temperature ("C) 37.6 * f f a Data are shown as the mean 5 the standard deviation. Effluent Temperature ("C) f * * f k f 1.0 effluent perfusate temperature was achieved at the time of cross-clamping and did not vary significantly throughout the 30 minutes of ischemia. Measured effluent perfusate temperatures ranged from 8" to 15 C for the duration of cross-clamping in all 8 animals, which should produce gray matter temperatures of less than 20 C based on the preliminary temperature studies. All 8 control animals had complete hind limb paralysis after complete recovery from anesthesia (Tarlov grade 0). Seven of the 8 experimental animals had preservation of motor function with spontaneous hind limb movement and withdrawal to pain but were unable to stand on the hind limbs (Tarlov grade 2), and 1 experimental animal had complete hind limb paralysis (Tarlov grade 0). If the groups are compared for preservation of motor function, this is a significant difference ( p = 0.002). Histologic evaluation was done by a pathologist blinded to the groups. Sections of the lumbar cords in the control animals showed changes characteristic of acute ischemic necrosis (Fig 3), with widespread pyknotic changes, hyperchromatic nuclei, and shrinkage spaces in anterior horn motor cells. Lumbar cord histology in the experimental animals showed much less severe ischemic changes, with only mild shrinkage spaces, minimal hyperchromatic changes in affected areas, and a predominance of preserved normal histology in anterior horn motor cells (Fig 4). An i \ m a 25-l 0 BODY TEMP. 0 EFFLUENT TEMP. 10' p I A Clamps 15 Clamps 10 Start Min. Min. Min. On Min. Off Min. TIME Fig 2. Mean efluent and body temperatures in experimental animals over time.
4 68 SALZANO ET AL 1994; Fig 3. Photomicrograph of section of lumbar cord of control animal showing pyknotic cells, hyperchromatic nuclei, cytoplasmic clumping, and shrinkage spaces in anterior horn motor cells. (Hematoxylin and eosin; X450 before 50% reduction.) Comment Hypothermia, by virtue of its reduction of tissue metabolic rate, has been used experimentally and clinically to provide protection against ischemic organ injury. Deep hypothermia with surface body cooling was first used in experimental cardiac surgery by Bigelow and associates [MI. Since then, deep hypothermia and circulatory arrest have become useful in congenital cardiac surgery and in the treatment of lesions of the ascending aorta and aortic arch. Borst and colleagues [19] first described the technique of hypothermic circulatory arrest for the treatment of aortic disease that requires posterolateral exposure. Subsequent use of deep hypothermia for these indications has been minimal. More recently, Crawford and co-workers [20] reported on 25 patients with thoracic aortic aneurysms who underwent operation with partial cardiopulmonary bypass, Fig 4. Photomicrograph of section of lumbar cord of experimental animal showing only mild shrinkage and clumping changes and areas of normal histology. (Hematoxylin and eosin; x450 before 50% reduction.) profound hypothermia, and circulatory arrest. The incidence of paraplegia was 11% with no other adjuncts used for spinal cord protection. Kouchoukos and colleagues [21] treated 5 patients with thoracic aortic aneurysms with total cardiopulmonary bypass and periods of hypothermic circulatory arrest and low flow. One patient died, and the 4 survivors had no evidence of ischemic spinal cord injury. Both author groups stress that given the higher than expected mortality (16%) and high incidence of pulmonary complications in the Crawford study as well as the potential for both involvement of the aortic sinuses and aortic valvular insufficiiency in these lesions, with limited or no access to the aortic valve through the left chest, hypothermic arrest is a technique reserved for special circumstances only. Applications of hypothermia in experimental aortic surgery for protection against paraplegia are effective. Total-body immersion in ice baths with systemic hypothermia has prevented paraplegia in dogs [22] and rabbits [23]. Techniques of perfusion cooling of the spinal cord through the isolated aortic segment in an attempt to avoid systemic hypothermia have also been protective [24, 251. However, in one [24] of those studies, body temperature was reduced substantially enough to raise the question whether the protection was the result of regional or systemic hypothermia. Experimental systems of regional selective cord hypothermia have been described previously. Albin and coworkers [26] performed subarachnoid perfusion cooling of the spinal cord in dogs to a cord temperature of 10 C for 1 hour with no resultant neurologic sequelae and later demonstrated no histologic changes attributed to cold perfusion [27]. Techniques of selective cord hypothermia, either by perfusion or local application, have been shown to protect against neurological injury resulting from trauma both in experimental [ and clinical [31] situations. It has been demonstrated that this direct local cord cooling does lead to reduced regional spinal cord blood flow in the cooled and adjacent segments, probably from local vasoconstriction These techniques have ~~reviously been applied for protection of the spinal cord during thoracic aortic crossclamping in canine models with systems similar to ours. The functional results, however, have been different. Negrin and Klauber [33] used epidural catheters and perfusion with saline solution at temperatures of 7" to 15"C, with complete preservation of motor function after thoracic aortic cross-clamping. Recently, Berguer and associates [34] used a subarachnoid perfusion system of saline solution at 5"C, with :similar complete preservation of motor function after double aortic cross-clamping for 45 minutes and no histologicall changes noted in harvested spinal cords. Species differentiation in neurological outcome in experimental aortic surgery has been observed before. Cerebrospinal fluid drainage in dogs has consistently provided reduced incidence of paraplegia in aortic crossclamping [4, 6, 7, 351. However, when investigated in pigs, CSF drainage did not reduce the incidence of paraplegia [36]. Similarly, in a baboon model [3], CSF drainage
5 1994; SALZANO ET AL 69 did not protect against paraplegia, but when drainage was combined with intrathecal papaverine, paraplegia was avoided. Conversely, perfusion cooling of the spinal cord through the isolated aortic segment in pigs has been shown to be protective [24], whereas in dogs, the results are equivocal [25, 371. Differences in experimental protocol may account for these differing species results. Variations in technique (single versus double aortic cross-clamping) and duration of cross-clamp time (range, 30 minutes to 60 minutes) in the canine studies were used as standards for producing paraplegia in control animals, whereas in most pig studies, a standard of 30 minutes of double aortic crossclamping has been reproduced faithfully to cause paraplegia in controls [lo, 11, 24, 361. The canine studies of CSF drainage used catheters in the cisterna magna to remove fluid, whereas the pig and baboon studies used laminectomies, which might cause arterial spasm and additional ischemia. Interestingly, a randomized prospective study of CSF drainage alone in humans failed to reduce the incidence of postoperative paraplegia compared with controls [38], a finding correlating with that of the swine study [36]. Previous studies have considered animals with paraparesis but not paraplegia (Tarlov grade 1, 2, or 3) as failures of protection [5, 24, 371. Because of the complete lack of any appreciable motor function in all 8 control animals, we believe that any preservation of motor function in our model is evidence of at least partial cord protection. Although our functional results were discouraging in that no animal had complete neurological preservation as demonstrated in the canine studies [33, 341, our histological findings of some reduction in the extent of changes resulting from ischemic injury were encouraging. We tried a variety of systems to cool the subarachnoid space. An initial attempt was made to keep our system close to what would be acceptable in clinical applications. We tried percutaneous placement of 18-gauge catheters similar to those used for delivery of epidural anesthesia. However, the limiting factor in producing adequate effluent temperatures for cord hypothermia was the ability to drain the subarachnoid space efficiently, and this required a larger-gauge drainage catheter, which could not be easily and reliably placed percutaneously in a pig. We experimented with placement of both catheters through a single lumbar laminectomy and directing one cranially, but this led to major mechanical problems and trauma to the cord. Our system of short, soft ventriculostomy catheters placed through separate laminectomy sites allowed easy positioning with no gross or histological traumatic damage to the spinal cord and a wide range of adjustable perfusion flow rates with minimal CSF pressure changes. In our experimental technique, we also strove to keep regional cord hypothermia the single variable tested. Blood pressure did fall significantly in the experimental group from postinduction levels to preclamping levels, possibly from a reflex sympathetic response to intrathecal cold or from the 45 minutes of cooling under anesthesia with a lack of any surgical stimulus. Nevertheless, during clamping and ischemia, the blood pressure was kept the same between the two groups. If anything, the relative hypotension would be expected to be deleterious neurologically. We switched from halothane to isoflurane as the inhalation agent early in the experimental protocol because of improved hemodynamic stability with isoflurane, and only 2 control animals received halothane. Despite heating pads and warm ambient temperatures, there was a slight, significant amount of systemic hypothermia but not to the degree that has clinically offered any protection against ischemic injury. Leakage of CSF was kept to a minimum during catheter placement and removal and, although not quantified, did not produce any appreciable change in CSF pressures. Flow rates were adjusted gradually to prevent any sudden changes in CSF pressures. The 1 animal with failure of protection in the experimental group had an effluent temperature of 17 C within 15 minutes of spinal cord perfusion and maintained effluent temperatures of 15 C or less throughout the entire cross-clamp period. There was, however, a problem with maintaining adequate drainage during the initial period of perfusion, which was corrected by repositioning. Although the drainage problem was transient, CSF pressures were not measured and may have risen so high as to cause cord compression, thus accounting for the failure of protection. We think that, given the multifactorial nature of spinal cord ischemia and injury during thoracic aortic crossclamping [39], regional cord hypothermia may be a useful adjunct when combined with other methods for protection against spinal cord ischemic injury, with our data demonstrating a reduction in the severity of neurologic injury. In humans, we propose cooling the spinal cord through percutaneously placed thoracic subarachnoid catheters and draining the subarachnoid space through percutaneously placed lumbar catheters. These percutaneous techniques are documented to be safe [40] and when done, result in the catheters lying beneficially anterior to the cord in proximity to the anterior spinal artery and anterior horn motor cells (141. A limitation to this technique in humans may be the need for very high flow rates, calculated as high as 2 L/min [41], to obtain the necessary protective cord temperatures. Prospective standardized studies of selective cord hypothermia by perfusion cooling in humans are necessary to assess this. We thank Dr Dean Uphoff for his preparation and help in interpretation of the histologic specimens and Ms Deborah Turling for graphics. We are greatly indebted to the staff of the Hartford Hospital Animal Research Laboratory, especially Ms Laura Maffucci, for technical assistance and suggestions. References 1. Livesay JJ, Cooley DA, Ventemiglia RA, et al. Surgical experience in descending thoracic aneurysmectomy with and without adjuncts to avoid ischemia. 1985; 39: Crawford ES, Crawford JL, Safi HJ, et al. Thoracoabdominal aortic aneurysms: preoperative and intraoperative factors
6 70 SALZANO ET AL 1994;576%71 determining intermediate and long-term results of operations in 605 patients. J Vasc Surg 1986;3: Svensson LG, Von Ritter CM, Groeneveld HT, et al. Crossclamping of the thoracic aorta: influence of aortic shunts, laminectomy, papaverine, calcium channel blocker, allopurinol, and superoxide dismutase on spinal cord blood flow and paraplegia in baboons. Ann Surg 1986;204: McCullough JL, Hollier LH, Nugent M. Paraplegia after thoracic aortic occlusion: influence of cerebrospinal fluid drainage. J Vasc Surg 1988; Woloszyn TT, Marini CP, Coons MS, et al. Cerebrospinal fluid drainage and steroids provide better spinal cord protection during aortic cross-clamping than does either treatment alone. 1990;49:7% Elmore JR, Gloviczki P, Harper CM, et al. Spinal cord injury in experimental thoracic aortic occlusion: investigation of combined methods of protection. J Vasc Surg 1992;15: Granke K, Hollier LH, Zdrahal P, Moore W. Longitudinal study of cerebral spinal fluid drainage in polyethylene glycolconjugated superoxide dismutase m paraplegia associated with thoracic aortic cross-clamping. J Vasc Surg 1991;13: Agee JM, Flanagan T, Blackbourne LH, Kron IL, Tribble CG. Reducing postischemic paraplegia using conjugated superoxide dismutase. 1991;51: DelRossi AJ, Cernaianu AC, Cilley JH, et al. Preventive effect of Fluosol-DA for paraplegia encountered after surgical treatment of the thoracic aorta. Preliminary results in a dog model. J Thorac Cardiovasc Surg 1990;99: 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: Schittek A, Bennink GBWE, Cooley DA, Langford LA. Spinal cord protection with intravenous nimodipine: a functional and morphologic evaluation. J Thorac Cardiovasc Surg 1992; 104:llOO Breckwoldt WL, Genco CM, Connolly RJ, Cleveland RJ, Diehl JT. Spinal cord protection during aortic occlusion: efficacy of intrathecal tetracaine. 1991;51: Maughan RE, Mohan C, Nathan IM, et al. Intrathecal perfusion of an oxygenated perfluorocarbon prevents paraplegia after aortic occlusion. 1992;54:81% 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, Bednarski M, Cosgrove DM, Loop FD. Appraisal of cerebrospinal fluid alterations during aortic surgery with intrathecal papaverine administration and cerebrospinal fluid drainage. J Vasc Surg 1990;11:42> Hollier LH. Protecting the brain and spinal cord. J Vasc Surg 1987;5: Tarlov IM. Spinal cord compression. Mechanisms of paralysis on treatment. Springfield, IL: Charles C Thomas, Bigelow WG, Lindsay WK, Greenwood WF. Hypothermiaits possible role in cardiac surgery: and investigation of factors governing survival in dogs at low body temperatures. Ann Surg 1950;132: Borst HG, Schaudig A, Rudolph W. Arteriovenous fistula of the aortic arch. Repair during deep hypothermia and circulatory arrest. J Thorac Cardiovasc Surg 1964;48: Crawford ES, Coselli JS, Safi HJ. Partial cardiopulmonary bypass, hypothermic circulatory arrest, and posterolateral exposure for thoracic aortic aneurysm operation. J Thorac Cardiovasc Surg 1987;94: Kouchoukos NT, Wareing TH, Izumoto H, Klausing W, Abboud N. Elective hypothermic cardiopulmonary bypass and circulatory arrest for spinal cord protection during oper- ations on the thoracoabdominal aorta. J Thorac Cardiovasc Surg 1990;99: Beattie EJ, Adovasio D, Keshishian JM, Blades 8. Refrigeration in experimental surgery of the aorta. Surg Gynecol Obstet 1953;96: Naslund TC, Hollier LH, Money SR, Facundus EC, Skenderis BS. Protecting the ischemic spinal cord during aortic clamping: the influence of anesthetics and hypothermia. Ann Surg 1992;215: Colon R, Frazier OH, Cooley DA, McAllister HA. Hypothermic regional perfusion foir protection of the spinal cord during periods of ischemia. 1987;43: 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: Albin MS, White RJ, Donald DE, MacCarty CS, Faulconer A. Hypothermia of the spinal cord by perfusion cooling of the subarachnoid space. Surg Forum 1961;12: Albin MS, White RJ, MacCarty CS. Effects of sustained perfusion cooling on the subarachnoid space. Anesthesiology 1963;24: Albin MS, White RJ, Acosta-Rua G, Yashon D. Study of functional recovery produced by delayed localized cooling after spinal cord injury in primates. J Neurosurg 1968;29: 11> Hansebout RR, Kuchner EF, Romero-Sierra C. Effects of local hypothermia and of steroids upon recovery from experimental spinal cord compression injury. Surg Neurol1975;4: Kuchner EF, Hansebout RR. Combined steroid and hypothermia treatment of expeiimental spinal cord injury. Surg Neurol 1976;6: Bricolo A, Dalle Ore G, Da Pian R, Faccioli F. Local cooling in spinal cord injury. Surg Neurol 1976;6: Sakamoto T, Monafo WW. Regional spinal cord blood flow during local cooling. Neurosurgery 1990;26: Negrin J, Klauber LD. Direct regional hypothermia of the central nervous system: a p:reliminary report of a pilot project on experimental hypothermia. Arch Neurol 1960;3: Berguer R, Porto J, Fedoronko B, Dragovic L. Selective deep hypothermia of the spinal cord prevents paraplegia after aortic cross-clamping in the dog model. J Vasc Surg 1992;15: Bower TC, Murray MJ, Gloviczki P, Yaksh TL, Hollier LH, Pairolero PC. Effects of thoracic aortic occlusion and cerebrospinal fluid drainage on regional spinal cord blood flow in dogs: correlation with neurologic outcome. J Vasc Surg 1989;9: Wadouh F, Lindemann Eh", 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: Kirshner DL, Kirshner RL., Heggeness LM, DeWeese JA. Spinal cord ischemia: an evaluation of pharmacologic agents in minimizing paraplegia after aortic occlusion. J Vasc Surg 1989;9: Crawford ES, Svensson LG, Hess KR, et al. A prospective randomized study of cerebrospinal fluid drainage to prevent paraplegia after high-risk surgery on the thoracoabdominal aorta. J Vasc Surg 1991;13: 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: Phillips OC, Ebren H, Nelson AT, Black MH. 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7 1994; SALZANO ET AL 71 DISCUSSION DR ROBERT J. CERFOLIO (Rochester, MN): I congratulate you on your work and your presentation. In your presentation, you do not distinguish between the length of recovery time and the actual neurologic grading of the animals. I assume it was a short period. If that assumption is correct, would it have made any difference in your controlled population if you had waited longer, that is, days or weeks as opposed to hours? DR SALZANO: I do not think there would have been any difference for two reasons. The first is that in studies done by Albin and co-workers at the Mayo Clinic in the 1960s, preliminary studies when they were looking at spinal cord perfusion for protection against traumatic injury, it was fairly clear that complete neurologic recovery was present fairly soon after discontinuing perfusion cooling, and that, in fact, was confirmed in our experimental preliminary studies. The second reason is that I think most of the data show that there is, if anything, a delayed-onset paraplegia where you see a worsening of neurologic function. Therefore, I do not think that there would be any improvement in neurologic function over time. In fact, there might be a worsening, and this delayed-onset paraplegia seems to be more a reperfusion injury than an acute ischemic injury. DR FRANCIS ROBICSEK (Charlotte, NC): Did you perfuse your control animals with saline solution as well? DR SALZANO: No, we did not. DR ROBICSEK: Then how do you know it is not the saline perfusion that caused the difference or pressure changes induced? I think the real control experiment would have been to use normal-temperature saline solution versus cold saline solution. DR SALZANO: I think we know that perfusion of saline solution by itself caused no neurologic changes in animals, but that is a point of consideration. DR I. AYHAN OZDEMIN (Bursa, Turkey): My colleagues and I used the rabbit as an animal model. We cross-clamped the thoracic aorta and then perfused the aorta with cold saline solution. In the control rabbits, paraplegia occurred in 15 minutes, but in the experimental group with cold saline solution perfusion of the aorta, the period of safety was 30 to 35 minutes. To confirm these findings, we applied this technique clinically. In a number of patients we routinely perfused the distal aorta with cold saline solution. In around 40 patients it was safe, and we had no problems. DR SALZANO: Thank you. I think that the perfusion cooling studies have been done in other animal models with mixed results. The findings in Dr Cooley s laboratory showed clearly that in pigs, there was protection by perfusion cooling through the isolated aortic segment. However, the data obtained in canine studies have been equivocal. DR AGUSTIN ARBULU (Detroit, MI): Did you measure pressures in your control and experimental groups? There is evidence that decreasing the pressure prevents spinal cord injuries. DR SALZANO In an attempt to keep hypothermia the single variable, we tried to minimize the amount of cerebrospinal fluid that was drained at the time of placement through the laminectomy sites. The opening pressures in the animals that had laminectomies and placement of catheters averaged 8 mm Hg, and this did not change significantly during placement. Throughout perfusion, by adjusting our gravity drip rates and adjusting our rate of effluent flow, we were able to keep spinal pressures in a range generally between 8 and 12 mm Hg. We strove to prevent any changes in spinal canal pressure, and I think we accomplished that well.
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