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Ann Thorac Surg 1999;68:1278-1284
© 1999 The Society of Thoracic Surgeons
a Department of Anesthesiology, University of Amsterdam, Amsterdam, The Netherlands
b Department of Vascular Surgery, Academic Hospital, University of Amsterdam, Academic Medical Center, Amsterdam, The Netherlands
Address reprint requests to Dr de Haan, Department of Anesthesiology, Academic Hospital, University of Amsterdam, Postbus 22660, 1100 DD Amsterdam, The Netherlands
e-mail: p.dehaan{at}amc.uva.nl
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Abstract |
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Methods. The thoracoabdominal aorta was exposed in 10 pigs. Functional integrity of spinal cord motor pathways was assessed with myogenic motor-evoked potentials after transcranial electrical stimulation (tc-MEPs). Using this technique, a group of segmental arteries not critical for spinal cord blood supply was identified. Before, during, and after clamping of the noncritical segmental arteries, spinal cord ischemia was produced by decreasing SCPP by means of increasing CSF pressure, and the SCPP threshold at which tc-MEPs showed evidence of spinal cord ischemia was determined. Ischemic SCPP thresholds, obtained during and after clamping of the noncritical segmental arteries, were compared with the ischemic threshold obtained before clamping (control value).
Results. Before noncritical segmental arteries were clamped, ischemic tc-MEP changes occurred when the SCPP was below 15 ± 5 (SD) mm Hg. With a total of 9 ± 3 (SD) segmental arteries clamped, the ischemic SCPP threshold was 48 ± 14 mm Hg (p < 0.01). After the release of all clamps, ischemia occurred at a SCPP of 15 ± 5 (SD) mm Hg.
Conclusions. In this porcine experiment, clamping of originally noncritical segmental arteries significantly reduced the tolerance of the spinal cord to a decrease in SCPP.
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Introduction |
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Segmental arteries, other than the ARM, contribute to spinal cord blood supply. It is conceivable that these originally noncritical vessels become important to spinal cord blood supply in circumstances of a decreased spinal cord perfusion pressure (SCPP). Indeed, during TAA surgery, factors that decrease SCPP are associated with the development of spinal cord ischemia. For example, increased cerebrospinal fluid (CSF) pressure, as a result of thoracic aortic cross-clamping, is believed to play a role in the pathogenesis of paraplegia [5]. Similarly, in a prospective randomized study of cerebrospinal fluid (CSF) drainage during TAA surgery, postoperative hypotension has been described as a predictor of delayed neurological deficits [6].
The aim of the present porcine study was to determine whether spinal cord blood supply becomes dependent on originally noncritical segmental arteries if SCPP is decreased. Adequacy of spinal cord blood flow was assessed with myogenic motor-evoked potentials to transcranial electrical stimulation of the motor cortex (tc-MEP). Tc-MEPs selectively reflect transmission in spinal cord motoneuronal pathways and can detect ischemia within minutes after the interruption of spinal cord blood supply [7].
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsCommentReferences |
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Anesthesia
The animals were premedicated with ketamine 15 mg/kg IM. Anesthesia was induced with 2.0% isoflurane by mask in a mixture of 50% O2 in N2O. Two intravenous catheters (18 G) were placed in an ear vein. Isoflurane was discontinued and anesthesia was maintained with continuous infusion of ketamine (15 mg/kg/h), sufentanil (5 µg/kg/h), clonidine 1 µg/kg/h and N2O (60%). Normal saline was infused at a rate of 15 mL/kg/h. The animals were ventilated using intermittent positive pressure ventilation. Ventilation was adjusted to maintain end-tidal CO2 within 4.8 to 5.3 kPa throughout the experiment. Arterial blood pressure was measured with an axillary arterial line and central venous pressure was measured by means of a catheter placed in the superior caval vein. Heart rate from the electrocardiogram and nasopharyngeal temperature were monitored continuously. Arterial pH, PaO2, PaCO2, hemoglobin concentration, and hematocrit were measured before CSF manipulations and segmental artery clamping.
Technique of motor-evoked potential recording
Tc-MEPs were evoked with a transcranial electrical stimulator (Digitimer D 185 cortical stimulator, Welwyn Garden City, UK). The stimuli were applied to the scalp with four needle electrodes. The stimulus consisted of a train of five pulses. The interstimulus interval between pulses was 1.5 ms. The pulse duration was 50 µs. The anode was placed at the occiput. The cathode consisted of three interconnected cathodes placed behind the ears and one in the soft palate. Compound muscle action potentials (CMAP) were recorded from the skin over the left and right quadriceps muscles using adhesive gel Ag/AgCl electrodes. The signals were amplified 5,000 to 20,000 times (adjusted to obtain maximum vertical resolution), and filtered between 30 and 1500 Hz. Data acquisition, processing, and analysis were performed on a computer with software written in the LabVIEW programming environment (National Instruments, Austin, Texas). The supramaximal stimulus intensity was assessed and tc-MEPs were recorded at a stimulus intensity of 10% above the level that obtained maximal amplitude, typically 500–600 V, resulting in an amperage of 0.8–1.2 A. A reduction of tc-MEP amplitude of one or both quadriceps muscles to less than 25% of baseline was considered an indication of ischemic spinal cord dysfunction.
Operative procedure
Two catheters were placed in the subarachnoid space through an epidural needle at the L4-L5 level. Correct position was confirmed by free flow of cerebrospinal fluid. One catheter was used for monitoring CSF pressure and one was used for CSF pressure manipulations.
The thoracoabdominal aorta was mobilized, and the intercostal and lumbar arteries were exposed from the left subclavian artery to the bifurcation. At each segmental level, the pig usually has one artery that preferentially branches from the left side from the aorta and divides in two separate arteries within 1 cm. At the end of the experiment the aorta was opened and we examined whether all intercostal arteries had been identified.
Experimental protocol
During the experimental protocol tc-MEP responses were acquired every minute. The SCPP was calculated as MAP minus CSF pressure. MAP was maintained between 60 and 80 mm Hg. Deliberate reduction of SCPP was achieved by increasing the CSF pressure (5 mm Hg every 5 minutes). CSF pressure was increased by infusing normal saline at 37°C in the subarachnoid space with an infusion pump. The ischemic SCPP threshold was defined as the SCPP at which a tc-MEP amplitude decrease indicative of spinal cord ischemia was observed in one or two legs. Figure 1 shows the experimental design with the sequence of experimental manipulations.
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Identification of a set of segmental arteries that can be clamped without signs of spinal cord ischemia
Segmental arteries were successively clamped in a cranial to caudal direction, starting just below the level of the left subclavian artery. Clamps remained in place until tc-MEPs showed evidence of spinal cord ischemia. Between placement of each clamp an observation period of 5 minutes was regarded in order to allow detection of ischemia. After detection of spinal cord ischemia, clamps were released from caudal to rostral at 5-minute intervals until tc-MEP amplitude returned above 25% of baselinein both legs. The set of segmental arteries remained clamped and a 15-minute waiting period was observed for the spinal cord to recover. This set of clamped segmental arteries was considered "noncritical" to spinal cord blood supply under normal pressure conditions.
Ischemic SCPP threshold with the set of noncritical segmental arteries clamped
With the clamps on noncritical intercostal arteries, the SCPP was again decreased to determine the ischemic SCPP threshold.Thereafter, CSF was allowed to drain spontaneously until CSF pressure and tc-MEPs returned to baseline values.
Ischemic SCPP threshold with all segmental artery clamps released
To rule out the possible occurrence of ischemic spinal cord injury during the course of the experiment, all clamps were released and the ischemic SCPP threshold was again determined.
Spinal cord perfusion pressures at which spinal cord ischemia was detected, both during and after clamping of the set of noncritical segmental arteries, were compared with the baseline ischemic SCPP threshold. Occurrence of spinal cord ischemia at a higher SCPP during clamping the set of segmental arteries would confirm the hypothesis that noncritical segmental arteries become important for spinal cord blood supply in conditions of a decreased SCPP.
Statistical analysis
All data are expressed as means ± standard deviation. The spinal cord perfusion pressures at which evidence of spinal cord ischemia was detected with the tc-MEPs were analyzed with the Wilcoxon sign-rank for paired data.
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Results |
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Spinal cord perfusion pressure manipulations
Table 1 shows the ischemic SCPP thresholds before, during, and after clamping of segmental arteries and the accompanying values for CSF pressure and MAP. Table 2 shows the results of individual animals. The subarachnoid infusion rate needed to increase CSF pressure was 250–635 mL/h. The infusion rate needed to maintain CSF pressure at a certain level was 60–110 mL/h. Before clamping of segmental arteries, the SCPP had to be reduced to 15 ± 5 (SD) mm Hg to produce ischemic tc-MEP changes (baseline ischemic SCPP threshold). In contrast, ischemic SCPP threshold when 9 ± 3 segmental arteries were clamped was 48 ± 14 mm Hg (p = 0.005 compared with baseline). At the end of the experiment, with all clamps released, the ischemic SCPP threshold was 15 ± 5 mm Hg.
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Comment |
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In the present study we opted to investigate the impact of "noncritical" segmental arteries on spinal cord blood supply by manipulating SCPP. The division of noncritical segmental arteries in relation to SCPP was described by Svensson and associates [8]. In that study, paraplegia developed in 1 pig subjected to hemorrhagic shock after the division of individual segmental arteries. It is possible to decrease SCPP by either increasing CSF pressure or by decreasing MAP. For several reasons, we preferred to manipulate CSF pressure rather than decrease MAP. It has been demonstrated that drugs used to reduce blood pressure may directly alter spinal cord blood flow [9], while the detrimental systemic effects of hemorrhagic shock may not allow multiple blood-pressure decreases. In addition, an increase in CSF pressure following aortic cross-clamping is thought to play a role in the pathogenesis of postoperative neurological deficits during TAA surgery [5]. A model of spinal cord ischemia based on increased CSF pressure may therefore be representative of the clinical situation during TAA surgery. The technique for producing spinal cord ischemia by increasing CSF pressure was first described by Blaisdell and Cooley [10]. The effect of a raised CSF pressure on spinal cord blood flow (SCBF) is well established. Griffiths and associates altered CSF pressure by subarachnoid infusion in order to manipulate SCPP in the dog [11]. Similar to autoregulation of cerebral blood flow, autoregulation of SCBF (measured by the hydrogen clearance technique) above a SCPP of 50 mm Hg was observed. Below perfusion pressures of 50 mm Hg, SCBF decreased in proportion with decreasing perfusion pressure.
Adequacy of spinal cord perfusion was assessed with tc-MEPs. Using this technique, functional integrity of the ischemia-sensitive motoneuronal pathways, including the anterior horn motor neurons, can be determined. These pathways are mainly located in the anterior two-thirds of the spinal cord and are supplied by the ASA. In humans undergoing TAA surgery, an acute interruption of spinal cord blood supply resulted in a rapid decrease of tc-MEP amplitude to values below 25% of baseline without significant latency prolongation [7]. We choose not to measure actual SCBF, because below an SCPP of 50 mm Hg, blood flow is reduced proportionally to the decreasing pressures, and the measured flow would provide no information regarding whether flow was adequate to maintain cellular activity. In contrast, tc-MEP monitoring provides a functional monitor and can determine the point at which spinal cord blood supply becomes insufficient to maintain synaptic activity. The criterion for spinal cord ischemia used in the present study was a decrease of tc-MEP amplitude to less than 25% of baseline. When somatosensory-evoked potentials are monitored, a 50% amplitude decrease is regarded as evidence of ischemic spinal cord dysfunction [12]. As a result of the larger amplitude variability of the tc-MEP signals, a more restrictive criterion was selected.
During the identification of a group of segmental arteries that was not critical for spinal cord blood supply, multiple segmental arteries were clamped in a caudal direction. In 8 animals, tc-MEPs only recovered after unclamping several segmental arteries extending to a higher level than the level of the clamp placement that resulted in tc-MEP evidence of spinal cord ischemia. One possible explanation for this apparent hysteresis might be a prolonged tc-MEP recovery after an ischemic episode [7]. To avoid the occurrence of irreversible spinal cord damage, the observation period for tc-MEPs to recover following unclamping each segmental artery did not exceed 5 minutes. As a consequence, if tc-MEP recovery after an ischemic episode took more than 5 minutes, more than one segmental artery was unclamped.
The porcine ARM arises mainly in the lower lumbar area [13]. As a result of the extent of segmental artery clamping, we can not exclude the possibility that in some of the experiments the ARM was included in the clamped segmental arteries during the perfusion pressure manipulations. However, this possibility is probably small because clamping the ARM and all segmental arteries arising above the level of the ARM is likely to result in tc-MEP evidence of spinal cord ischemia.
To appreciate the possible relevance of the present porcine findings in humans, the discrepancies in spinal cord blood supply need to be considered. In both species the spinal cord has a complex vascular anatomy. The feeding arteries originate from cervical thoracic and lumbar segments with a large variability of patterns. As in humans, the ARM of the pig is the largest feeder of the thoracolumbar spinal cord [14, 15]. The porcine ARM is located at the L3-L5 level in 87% of the cases [15]. In humans, the T5 to L5 segmental arteries can all give rise to the ARM, and in 85% of the cases the ARM originates between T9 and L2 [16].
In humans, the ASA is continuous from the medulla oblongata to the conus medullaris [14]. In the present study an average of 9 ± 3 intercostal arteries could be clamped without signs of ischemic spinal cord dysfunction, and in 2 animals all segmental arteries could be clamped without signs of ischemia. This observation supports the notion that the ASA is continuous in the pig as it is in humans [15].
Spinal cord blood supply in the pig is always plurisegmental; ie, five or more segmental arteries have a radicular branch supplying the spinal cord [15]. Although in humans a paucisegmental spinal cord blood supply, ie less than five radicular arteries supplying the spinal cord, was described in 45% of the cases [17], Domisse described in 32 postmortem specimens a mean of eight radicular feeders of the ASA [14].
The ARM has a downward hairpin bend with a relatively small diameter of the ASA above the junction with the ARM in both humans and pigs [14, 15]. Because blood flow is inversely proportional to the fourth power of the radius (Poiseuille’s equation), this caliber change has consequences for the distribution of blood flow to the thoracolumbar spinal cord. Calculations on postmortem specimens in humans have revealed that the resistance to upward flow is at least 11 times greater [18], thus forcing blood in a caudal direction along the length of the spinal cord. Accordingly, the ARM will preferentially perfuse the lumbar spinal cord. Indeed, the lower thoracic cord has been referred to as the critical zone of the spinal cord blood supply [14].
Thoracic radicular arteries and iliolumbar arteries do not have a hairpin bend at their junction with the ASA and blood can flow up and down the ASA [14, 15]. It is conceivable that in circumstances with an occluded thoracic aortic segment or ligated intercostal arteries a pressure gradient develops along the thoracic part of the ASA. Under these conditions the thoracic spinal cord might become susceptible to a decrease in SCPP. In accordance with these anatomical observations, the present study confirmed that the spinal cord becomes more vulnerable to a decrease in perfusion pressure after clamping of originally noncritical segmental arteries. As a result, spinal cord ischemia developed earlier; ie, at a significantly higher SCPP.
The present findings might have clinical relevance for patients undergoing TAA repair. If a protective strategy is used that concentrates on reattachment of the ARM, it was advocated to reattach all segmental arteries at the level of T11–L1 [3]. However, if the results of the present study are applicable in humans, the spinal cord may still remain vulnerable to a decrease in SCPP when only the ARM is revascularized and other segmental arteries are sacrificed. Therefore, it might be beneficial to reattach patent intercostal arteries at other levels. This hypothesis is supported by clinical observations of Griepp and associates [19]. Their finding that neurological deficits after TAA repair occurred only if more than ten segmental arteries had been severed, independent of the level, was suggestive of an anterior spinal artery with multiple interchangeable inputs. The authors argued that the thoracolumbar spinal cord blood supply in humans is unlikely to depend on a single ARM.
Segmental arteries that are normally noncritical can become crucial to spinal cord perfusion during a period of increased CSF pressure. Therefore, CSF drainage to prevent an increase in CSF pressure seems a logical protective measure. However, both in experimental models of spinal cord ischemia [10, 20, 21], and after TAA repair [6, 22, 23], contradictory results have been reported when CSF drainage was used in an attempt to prevent paraplegia. The results of the present study attest that a rise in CSF pressure might be more detrimental when noncritical segmental arteries are ligated.
Increased CSF pressures have been observed during epidural perfusion cooling for spinal cord protection [24]. Although this strategy significantly decreased lower extremity neurological deficits following TAA repair, the CSF pressures during aortic cross-clamping ranged from 24 to 44 mm Hg. The present data give reason for concern that regional cooling protocols that increase CSF pressure may actually produce spinal cord ischemia.
In conclusion, a number of segmental arteries in the pig could be clamped without tc-MEP evidence of spinal cord ischemia. However, after clamping these segmental arteries, a significantly smaller increase in CSF pressure resulted in spinal cord ischemia. These findings demonstrate that spinal cord blood supply can become dependent on originally noncritical segmental arteries during a deliberate increase in CSF pressure and a concomitant decrease in spinal cord perfusion pressure.
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Acknowledgments |
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References |
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This article has been cited by other articles:
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