ROBERT W. OGILVIE, PH.D., AND J. DOUGLAS BALENTINE, M.D.
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1 Oxygen tension in spinal cord gray matter during exposure to hyperbaric oxygen ROBERT W. OGILVIE, PH.D., AND J. DOUGLAS BALENTINE, M.D. Departments of Anatomy and Pathology (Neuropathology), Medical University of South Carolina, Charleston, South Carolina va Adult female rats were exposed to 60 psig of 100% oxygen for 60 minutes. Oxygen tensions in the gray matter of the lumbosacral enlargement of the spinal cord, electroencephalograms, electrocardiograms, and respirations were monitored before, during, and after the compression periods. Oxygen tensions were found to rise sharply to as high as 1050 mm Hg during compression and remained at significantly high levels throughout the entire hour of exposure. These data support the hypothesis that spinal cord lesions induced by exposure to hyperbaric oxygen are the result of excessive tissue oxygenation. KEYWoRDS 9 oxygen tensions 9 hyperbaric oxygen 9 pentobarbital 9 spinal cord 9 globus pallidus S ELECTIVE light and electron microscopic lesions of spinal anterior horn gray matter have been reported in rats exposed to hyperbaric oxygen. 1,3,4 Dendritic and axonal degeneration in the presence of intact anterior horn cell perikarya, occur following a single 30-minute exposure to 5 atm oxygen) Repeated intermittent 1-hour exposures to 5 atm oxygen on consecutive days until the onset of motor paralysis resulted in random selective necrosis of individual neuronal cell bodies throughout the anteromedial spinal gray matter, 4 while similar intermittent exposures until death are accompanied by extensive necrosis of the central gray matter of the cervical and lumbosacral enlargements? The pathogenesis of the selective central nervous system (CNS) lesions induced by hyperbaric oxygen could result either from excessive tissue oxygenation, or paradoxically, from ischemia caused by oxygen- induced vasoconstriction. Since cerebral ischemia prevents the necrotic forebrain lesions characteristic of hyperbaric oxygen exposures, 2 CNS lesions of hyperbaric oxygen exposure have been suggested to be the results of excessive tissue oxygenation. In order to test this hypothesis, more direct methods of measuring the available oxygen tensions within the regions of the CNS susceptible to oxygen-induced necrosis were employed. The present communication reports data obtained from measuring oxygen tensions in rat spinal cord gray matter continuously during a 1-hour exposure to 60 psig (5 atm) of oxygen. Material and Methods Nine adult female Sprague-Dawley rats, weighing 150 to 200 gm, were anesthetized with sodium pentobarbital (40 mg/kg) and prepared for electrocardiograms (EKG), elec- 156 J. Neurosurg. / Volume 43 / August, 1975
2 Cord oxygen tension in hyperbaric oxygen exposure troencephalograms (EEG), and measurement of respiratory rates and spinal cord oxygen tensions. The skull was surgically exposed and two EEG electrodes, metallic cups filled with electrode paste, were put into place, a reference lead over the nasal area and an active lead over the parietooccipital region. Two EKG leads, also metallic cup electrodes, were used; one was attached to one forelimb and the other to the opposite forelimb. The biopotentials were amplified and displayed on an ink-writing Grass polygraph.* After this, a polyethylene tube was surgically inserted into the trachea to provide a free airway and to allow monitoring of the respiratory rate by recording the differential temperature during inspiration and expiration throughout the course of the experiment. The latter was accomplished by a thermistor placed in the tracheal tube; another thermistor was placed in the rectum to monitor body temperature. The polygraph tracings of EEG, EKG, and respirations were omitted in two animals; in these, slow recordings of oxygen tensions were made to display more effectively the character of the oxygen tracings over a l-hour period. Respirations were monitored by clinical observations through plexiglass chamber windows. Oxygen tensions were recorded polarographically with platinum wire glass-insulated electrodest with tip diameters between 5 and 10 u. External reference silver-silver chloride electrodes were employed. The polarographic current produced by changes in oxygen tension was amplified and monitored by a Transidyne picoammeteri" and simultaneously displayed on an ink-writing Grass polygraph. Each electrode was calibrated before and after the experiment by measurement of the current obtained when the sensor cathode and reference anode were immersed in a constant temperature saline bath equilibrated with nitrogen (0% oxygen), compressed air (21% oxygen), and 100% oxygen. The electrodes were calibrated at temperatures within ranges equivalent to the rectal temperatures of the animals following *Grass polygraph made by Grass Instrument Company, 101 Old Colony Avenue, Quincy, Massachusetts telectrodes and picoammeter manufactured by Transidyne General Corporation, 903 Airport Drive, Box 1088, Ann Arbor, Michigan anesthesia (29 ~ to 34~ If the electrode calibration values at the beginning and end of each experiment failed to agree within 5% that given experiment was disregarded. Satisfactory experiments were obtained in five out of the nine animals. Each rat was prepared for measurement of spinal cord oxygen tension by a laminectomy performed in the lower thoracic and upper lumbar regions of the vertebral column overlying the lumbosacral enlargement. After surgery, the rat was fixed in a stereotaxic apparatus and with the aid of surface landmarks, the microelectrode tip was positioned within the anteromedial gray matter of the spinal cord. At this time, a baseline recording of oxygen tension was obtained with the animal breathing room air. Then the rat was put into a Bethlehem small animal hyperbaric chambers (Fig. i). The chamber was flushed with oxygen for a 10-minute period. After this time interval, the outflow gas from the chamber was measured with a Servomex oxygen analyzerw to insure that the chamber atmosphere was pure oxygen before proceeding. Compression of the chamber with pure oxygen to a pressure of 60 psig (5 atm) was accomplished over a 4-minute period. After 1 hour at 60 psig, decompression was completed in 8 minutes, with periodic stops at 45, 30, 15, 7'/~, and 4 psig. Following decompression the polarographic determination of oxygen was continued in ambient air for 10 to 15 minutes. The animals were then killed by reclosing the chamber and flushing it with pure nitrogen. Following the death of the animal the chamber was flushed with oxygen and recompressed with 60 psig of pure oxygen; polarographic monitoring for oxygen tensions was continued in the dead animal to provide an additional control for the methodology used in measuring tissue oxygen levels. The oxygen electrode was removed at the end of each experiment; a 25-gauge spinal needle was positioned stereotaxically in the spinal cord using the same coordinates as those employed for the electrode, except that SBethlehem small animal hyperbaric chamber made by Bethlehem Corporation, 225 West Second Street, Bethlehem, Pennsylvania. w oxygen analyzer manufactured by Servomex Controls Limited, Crowborough, Sussex, England. J. Neurosurg. / Volume 43 / August,
3 R. W. Ogilvie and J. D. Balentine FIG. 1. Entrance to the small animal hyperbaric chamber showing a rat in the stereotaxic apparatus with an oxygen electrode in the spinal cord. the depth was reduced by 1 mm to prevent the needle obscuring the terminal portion of the electrode track. The needle was filled with trypan blue and slowly removed, with the dye allowed to stain the track. The spinal cord was removed and sliced to locate the track and position of the electrode. With the amount of vertical displacement of the electrode known, the site of the electrode tip was estimated by measurement from the dorsal cord surface in the direction of the stained track. Results Control spinal cord oxygen values (measured under ambient conditions) ranged from approximately 7 mm Hg to 40 mm Hg (average = 16 mm Hg). Under compression the oxygen tension rose to its highest value in each experiment very soon after achieving 60 psig in the chamber. These values ranged from 350 mm Hg to 1050 mm Hg (average = 608 mm Hg) and occurred anywhere from 2 to 5 minutes (average = 3.4 minutes) after full compression. The level of oxygen tensions in the spinal cord remained at an average value equal to 36 times the ambient values during the 60-minute period of compression. A typical oxygen tension curve measured over 1 hour of compression to 60 psig of oxygen is illustrated in Fig. 2. A variable sloping of the curve during the middle of the exposure, sometimes associated with a rise in values toward the end, was observed; however, high oxygen tensions were maintained throughout the 1-hour exposure in all experiments. The respiration rates fell from an average of 56/min after anesthesia and before hyperbaric oxygen exposure to an average of "158 J. Neurosurg. / Volume 43 / August, 1975
4 Cord oxygen tension in hyperbaric oxygen exposure F~. 2. Slow polygraph record (5 mm/min) of the tracing of oxygen tension in the rat spinal cord before, during, and after exposure to 60 psig of oxygen. Fic. 3. Fast polygraph recording of oxygen tension in the rat spinal cord, respiration, EEG, and EKG at about midpoint during the hour's exposure to 60 psig of oxygen. 32/min near the end of the compression period. Typical tracings of the rats' EEG's before and during hyperbaric oxygen exposure are shown in Fig. 3. Rare bursts of increased amplitude lasting 1 to 2 seconds were noted in some animals, but no definitive sustained seizure activity was observed in the EEG tracings or clinically in any of the rats. The EKG's revealed normal sinus rhythms throughout each experiment. Control heart rates after anesthesia ranged from 300 to 480 beats/min, usually slowing by about 100 beats/min during the hour's exposure to hyperbaric oxygen, although in two experiments no change could be noted. At the time the animals were killed with 100% N~, a good correlation of physiological features of death was obtained, that is, respiratory efforts ceased within 5 minutes and the EEG's became flat. Following recompression of the chamber to 60 psig of oxygen, the physiological parameters of death remained unaltered and no spinal cord oxygen tensions were recordable, even after 15 minutes (Fig. 4). J. Neurosurg. / Volume 43 / August, 1975 ]59
5 R. W. Ogilvie and J. D. Balentine Fic. 4. Fast recording of spinal cord oxygen tension, respiration, EEG, and EKG following killing of the rat with nitrogen, and during recompression with 100% oxygen at 60 psig (same animal as illustrated in Fig. 3). Note absence of respiration, fiat EEG, and no detectable spinal cord oxygen tension (the tracing is at the zero baseline). Discussion The findings in this study indicate that oxygen tensions in the anterior horn gray matter of the spinal cord become significantly elevated upon exposure to 60 psig of oxygen and the elevated tensions are maintained throughout an hour's exposure. The physiological data monitored during the hyperbaric oxygen exposures correlate well with those observed in other laboratories. 7 Bradycardia is a well-known response to exposure to hyperbaric oxygen. Depressed respiration is also a characteristic response of anesthetized animals to hyperoxia; this respiration rate decline may in part explain some of the slight variations in the slope of the curve throughout the period. Two animals with elevation of oxygen tensions during the end of the compression had a simultaneous decrease in respiratory rate; this is noteworthy, and suggests that perhaps increased carbon dioxide as a result of decreased respiration may have contributed to increased spinal cord blood flow and therefore increased oxygen tension. The role carbon dioxide plays in increasing oxygen tensions in CNS tissue exposed to hyperbaric oxygen has been observed by others? The EEG tracings during this experiment indicate that the brain remained active during these observations and that no significant seizure activity occurred. The oxygen tensions observed in this study do not reflect the possible influence of anesthesia on the values obtained and therefore do not necessarily reflect the values of hyperoxia in the spinal cord of rats who are awake. However, similar necrotic lesions in the spinal cord of rats exposed to hyperbaric oxygen have been observed in rats anesthetized with pentobarbital? It is interesting that pentobarbital anesthesia protects the rat forebrain from the necrotic lesions of hyperbaric oxygen exposure? Oxygen tension measurements in the globus pallidus, which is vulnerable to O2-induced necrosis, were done in rats anesthetized with pentobarbital under hyperbaric conditions 160 J. Neurosurg. / Volume 43 / August, 1975
6 Cord oxygen tension in hyperbaric oxygen exposure identical to those in this study; high values were initially obtained during the early period of exposure. However, these values dropped precipitously in 5 to 10 minutes after compression, presumably due to vasoconstriction, and leveled off to considerably lower values (but still above ambient values) than those observed throughout exposure in the spinal cord. 8 The sustained oxygen tension values observed in the spinal cord during hyperbaric oxygen exposure in this study probably reflect a lack of significant vasoconstriction. The oxygen tension decline observed in the globus pallidus of rats anesthetized with pentobarbital may explain why the latter protects the globus pallidus from the necrotic lesions of hyperbaric oxygen, and indirectly suggests that sustained elevations of oxygen tensions, as found in the spinal cord, are responsible for the CNS lesions associated with hyperbaric oxygen exposure. References 1. Balentine JD: Central necrosis of the spinal cord induced by hyperbaric oxygen exposure../ Neurosurg 43: , Balentine JD: Pathogenesis of central nervous system lesions induced by exposure to hyperbaric oxygen. Am J Pathol 53: , Balentine JD: Ultrastructural pathology of hyperbaric oxygenation in the central nervous system: observations in anterior horn grey matter. Lab Invest 31: , Balentine JD, Gutsche BB: Central nervous system lesions in rats exposed to oxygen at high pressure. Am J Pathol 48: , Balentine JD, Gutsche BB: Influence of pentobarbitol anesthesia on the distribution of central nervous system lesions in rats exposed to oxygen at high pressure, in Brown IW (ed): Proceedings of the Third International Conference on Hyperbaric Medicine. National Academy of Sciences, 1966, pp Jamieson D, Van Den Brenk HAS: Measurement of oxygen tensions in cerebral tissues of rats exposed to high pressures of oxygen. J Appl Physiol 18: , Lambertsen C J: Physiological effects of oxygen inhalation at high partial pressures, in Fundamentals of Hyperbaric Medicine, Publ # National Academy of Sciences, National Research Council, 1966, pp Ogilvie RW, Balentine JD: Oxygen tensions in the deep grey matter of rats exposed to hyperbaric oxygen. Adv Exp Med Biol 37: , 1973 This work was supported by Grant NS09837 from the National Institute of Neurological Diseases and Stroke, United States Public Health Service. Address reprint requests to: R. W. Ogilvie, Ph.D., Department of Anatomy, Medical University of South Carolina, Charleston, South Carolina J. Neurosurg. / Volume 43 / August, 1975 ]6]
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