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Eur J Cardiothorac Surg 2005;28:274-279
© 2005 Elsevier Science NL

Original articles

Immediate ischemic preconditioning based on somatosensory evoked potentials seems to prevent spinal cord injury following descending thoracic aorta cross-clamping

^a Cardiothoracic Surgery, Heart Institute (Incor) Division, University of São Paulo Medical School, São Paulo, SP, Brazil
^b Experimental and Functional Neurosurgery Laboratory, University of São Paulo Medical School, São Paulo, SP, Brazil
^c Department of Pathology, Santa Casa School of Medicine, São Paulo, SP, Brazil

Received 1 December 2004; received in revised form 3 March 2005; accepted 9 March 2005.

^* Corresponding author. Address: Division of Surgery, Heart Institute (Incor), University of São Paulo Medical School, Av. Dr. Enéas Carvalho Aguiar, 44, 2 Level, Block 2, Room 13, 05403-000 São Paulo, SP, Brazil. Tel.: +55 11 30695075; fax: +55 11 30695318. (Email: dcimoreira{at}incor.usp.br).

Abstract

Objective: Delayed ischemic preconditioning has demonstrated neuroprotective effects in spinal cord ischemia. We investigated the effects of immediate ischemic preconditioning based on somatosensory evoked potentials monitoring in a model of spinal cord injury due descending thoracic aorta occlusion in dogs. Methods: Twenty-one dogs were submitted to spinal cord ischemia induced by descending thoracic aorta cross-clamping for 45min. Control group underwent only the aortic cross-clamping (n=7), group A underwent one cycle of ischemic preconditioning (n=7) and group B underwent three equal cycles of ischemic preconditioning (n=7), immediately before the aortic cross-clamping. Ischemic preconditioning cycles were determined by somatosensory evoked potentials monitoring. Neurologic evaluation was performed according to the Tarlov score at 72h of follow-up. The animals were then sacrificed and the spinal cord harvested for histopathology. Results: Aortic pressures before and after the occluded segment were similar in the three groups. Ischemic preconditioning periods corresponded to a mean ischemic time of 3±1min and a mean recovery time of 7±2min. Severe paraplegia was observed in three animals in Control group, in four in group A and in none in group B. Tarlov scores of group B were significantly better in comparison to the Control group (P=0.036). Histopathologic examination showed severe neuronal necrosis in the thoracic and lumbar gray matter in animals who presented paraplegia. Conclusions: Immediate repetitive ischemic preconditioning based on somatosensory evoked potentials monitoring seems to protect spinal cord during descending aorta cross-clamping, reducing paraplegia incidence.

Key Words: Aortic aneurysm • Spinal cord • Paraplegia • Ischemic preconditioning • Evoked potential

1. Introduction

Major causes of spinal cord injury during thoracoabdominal aortic surgery are the duration and degree of ischemia, the failure to re-establish blood flow to the spinal cord after the repair, and a biochemically mediated reperfusion injury. For several years, numerous methods have been attempted to prevent this complication. With the surgical adjuncts of distal aortic perfusion and cerebrospinal fluid drainage [1,2], the probability of neurological deficits decreased considerably. Nevertheless, acute spinal cord ischemia resulting in paraplegia or paraparesis remains a frequent possibility in the treatment of extent thoracoabdominal aortic aneurysms despite these protective strategies. This complication has also been reported even after endovascular repair of these aneurysms [3].

Since the advent of ischemic preconditioning in the myocardium, more and more attention has been paid to the effects of this phenomenon in the spinal cord. Some authors have demonstrated the improvement of ischemic tolerance of the motor neurons several hours after brief periods of ischemic pretreatment in different animal species [4–7]. On the other hand, the immediate effects of ischemic preconditioning on the spinal cord are controversial [8–12]. The ischemic times required to induce preconditioning are species-specific and organ system specific, and the overall incongruity of the spinal cord's vascular anatomy makes it virtually impossible to determine, with any degree of certainty, the correct ischemic and reperfusion times that need to be involved in this process. In this regard, the sensitivity of somatosensory evoked potentials (SSEP) monitoring to the interruption of spinal cord perfusion has led this method as an effective tool for the intraoperative assessment of spinal cord function and viability [13]. Accordingly, the purpose of this study is to investigate the effects of immediate ischemic preconditioning based on SSEP monitoring in a model of spinal cord injury due to descending thoracic aorta occlusion in dogs.

2. Materials and methods

The Scientific and Ethic Committee of the Heart Institute (Incor), University of São Paulo Medical School approved the experimental protocol. All animal care was performed in compliance with the ‘European Convention on Animal Care’.

Twenty-one adult mongrel dogs weighting from 15 to 25kg were randomly assigned to three different groups according to the ischemic preconditioning protocols. Control group was only submitted to a period of 45min of aortic occlusion (n=7), group A underwent one cycle of ischemic preconditioning (n=7) and group B underwent three equal cycles of ischemic preconditioning (n=7), immediately before the period of aortic occlusion.

2.1. Animal preparation
The dogs were anesthetized with intravenous pentobarbital sodium (30mg/kg) and paralyzed with pancuronium bromide (0.3mg/kg). The trachea was intubated and the lungs were ventilated with 100% oxygen. Respiratory settings included a tidal volume of 12ml/kg, and a respiratory rate to maintain the partial tension of oxygen at more than 100mmHg and the partial tension of carbon dioxide between 35 and 45mmHg, as measured by arterial blood gas analysis. The electrocardiogram was recorded using needle electrodes and a rectal temperature probe was inserted. Under sterile conditions, the left jugular vein was catheterized for intravenous administration of complementary anesthetic drugs, fluids and cefalotin (15mg/kg). Catheters were also inserted into the left carotid artery and right femoral artery to record the arterial pressures proximal and distal to aortic cross-clamping. All pressures were continuously monitored with a pressure transducer. To monitor SSEP, two subcutaneous electrodes were placed in the right leg, at the region corresponding to the right tibial nerve. One silver lead was inserted into the midline interspinous ligament to be in contact with the spinal cord lamina at the L1–2 levels, and a reference subcutaneous electrode was also placed at the cranium basis.

In the right lateral position, a left thoracotomy in the sixth intercostal space was performed. The aorta was isolated distal to the left subclavian artery and close to the diaphragm. After anticoagulation with heparin (100U/kg), the aorta was cross-clamped distal to the left subclavian artery and nearby the diaphragm to perform the ischemic preconditioning stages and to induce spinal cord ischemia for 45min. After unclamping the aorta, 1mg/kg of protamine was administered. Sodium bicarbonate was also infused to restore the acid–base status. After 1h of reperfusion, all the animals were hemodynamically stable. All the catheters were removed, the chest was closed in layers, and anesthesia was discontinued. When the dog was breathing spontaneously, the trachea was extubated.

2.2. SSEP monitoring and ischemic preconditioning protocol
Detection of the conduction pathways by SSEP was performed by the stimulation of the right leg. SSEP were recorded in a unipolar fashion with a Medelec Saphire 4ME evoked potential instrument (Medelec, USA). The stimuli used were pulses of 0.1ms duration and 4–7mA intensity delivered at 10Hz. A number of 256 repetitions were averaged. The SSEP were recorded before the initial aortic occlusion, and every minute during the first ischemic preconditioning cycle and for 1h after the final reperfusion of the aorta.

Ischemic preconditioning periods were determined by SSEP monitoring. Initial aortic occlusion was maintained until the time when N1 wave amplitude in SSEP decreased at less than 60% of its original value (Fig. 1 ). The ischemic period was followed by aortic reperfusion for a time that was sustained until the return of N1 wave amplitude to the preischemic level. For the dogs in Group A, these periods corresponded to the single ischemic preconditioning cycle. Three equal cycles according to the first ischemic preconditioning cycle were sequentially performed in Group B, immediately before the extended aortic occlusion.

View larger version (18K): [in this window] [in a new window]   Fig. 1. Recordings of the somatosensory evoked potentials during the first aortic occlusion in the ischemic preconditioning cycle.

2.3. Neurologic evaluation
Neurologic status was assessed on the third postoperative day by an independent observer using the modified Tarlov score [14]. A score of 0–4 was assigned to each animal as follows: grade 0, spastic paraplegia with no movement of the hind limbs; grade 1, spastic paraplegia with slight movement of the hind limbs; grade 2, good movement of the hind limbs, but unable to stand; grade 3, able to stand, but unable to walk normally; and grade 4, complete recovery.

2.4. Histopathologic study
All dogs were submitted to euthanasia 72h after the end of the experiment with an overdose intravenous injection of sodium pentobarbital. The lower thoracic and lumbar spinal cords were fixed in a 10% formalin solution for 120h and subsequently embedded in paraffin. Serial transverse sections (8µm) of lower thoracic (T9–T12) and lumbar (L1–L3) spinal cord segments were obtained from each animal and stained with hematoxylin and eosin. An experienced pathologist unaware of the dog's neurologic outcome examined each slice for evidence of cellular necrosis and presence inflammatory cells. Histopathologic changes of the gray matter were graded in the worst samples as follows: grade 3, severe necrosis corresponding to more than one half of the gray matter area; grade 2, mild to moderate necrosis corresponding to less than one half of the gray matter area; grade 1, presence of moderate to high grade of inflammatory cells infiltrate; grade 0, normal histologic appearance.

2.5. Statistical analysis
Physiologic data are presented as the mean±the standard deviation. Neurologic outcomes, SSEP recovery times and histopathologic scores are expressed as the median and percentiles. The overall group differences regarding physiological variables were compared by single factor analysis of variance, followed by the Tukey procedure. Multiple group differences of neurologic outcomes, SSEP recovery times and histopathologic scores were analyzed using the Kruskal–Wallis procedure, followed by the Mann–Whitney U test with Bonferroni corrections for preconditioning groups' comparison to the Control. The Spearman rank correlation test was used to analyze the relationship between the SSEP recovery times and the neurologic outcome. A P value of less than 0.05 was considered significant as determined with SPSS for Windows, version 10.0 (SPSS, Inc., Chicago, IL).

3. Results

There were no significant differences between the three groups with regard to dogs' weight, and about rectal temperatures, hemoglobin, hematocrit and blood gas analysis during the experimental procedure. No significant differences were also seen between the groups with regard to proximal and distal aortic pressures at baseline, during the aortic cross-clamping and at the reperfusion period (Table 1 ).

Plots of the SSEP recovery times during the final reperfusion period are depicted in Fig. 2 . Most animals in Control group did not recover normal SSEP during the first hour after the unclamping of the aorta, while all dogs in group B and most of the dogs in group A recovered normal SSEP during this period. Nevertheless, the differences between the SSEP recovery times among the three groups were not statistically significant.

View larger version (13K): [in this window] [in a new window]   Fig. 2. Plots of the median and quartiles of the somatosensory evoked potential recovery times up to 1h after spinal cord ischemic induction in the control and ischemic preconditioning groups (Group A, one cycle; Group B, three cycles). Statistical analysis with Kruskal–Wallis test.

View larger version (11K): [in this window] [in a new window]   Fig. 3. Correlation between the somatosensory evoked potential (SSEP) recovery times and the Tarlov score of all the studied animals. Statistical analysis with Spearman correlation test.

The present investigation shows that some degree of ischemic tolerance of the spinal cord to prolonged aortic occlusion can be achieved by immediate ischemic preconditioning, when this process is based on the adequate monitoring of the functional effects of the ischemia and reperfusion phases. This observation represents an important step to add ischemic preconditioning as a neuroprotective strategy in thoracoabdominal aortic surgery, as delayed preconditioning of the human spinal cord would be impractical.

Ischemic preconditioning is the process whereby a sublethal ischemic stress enhances the tolerance of the tissue to a subsequent ischemic insult. This process involves endogenous cellular protective mechanisms, that include an early and a late phase of protection [15]. Although several authors have previously demonstrated the delayed protection seen with brief periods of ischemic induction on the spinal cord [4–7], the acute effects of immediate ischemic preconditioning on that organ have been controversial. Some studies have shown significant impact of previous periods of ischemic induction some minutes before prolonged aortic occlusion in the prevention of spinal cord injury [9,12]. Nevertheless, other authors failed to demonstrate the same effect with the use of shorter ischemic periods and intervals in similar animal species [11].

Residual blood flow in the spinal cord during the aortic occlusion may vary between animal species and from animal to animal [16], situation also suggested by the low incidence of spinal cord dysfunction in this experimental study after the ischemic induction in the control group. Therefore, as determinations of proper duration of ischemia and of adequate duration of reperfusion, before the subsequent ischemic induction, are thought to be the key factors for acquisition of immediate and delayed ischemic tolerance, it is mandatory to monitor spinal cord function and viability during both the ischemic and reperfusion periods. In this regard, determination of SSEP provides helpful diagnostic data about the status of spinal cord function [13]. Variations of either amplitude and or latency of the predominant signal peak, in comparison with baseline values, are decisive in diagnosing spinal cord ischemia. Deterioration of the N1 signal component is indicative of diminishing posterior and lateral spinal column sensory conduction, indicating compromised spinal cord perfusion [13,17]. During an ischemic process, we can also see the sequential disappearance of the component waves of SSEP, which return in reverse order after reperfusion [18]. According to spinal cord vascular anatomy, different types of SSEP responses have been identified and used to indicate the necessity of prophylactic measures to attenuate spinal cord ischemia [13].

In this experimental model, we used the decrease of N1 wave signal amplitude of SSEP to define the ischemic duration for preconditioning. This choice was based on its sensitivity to regional hypoperfusion and on the fact that prolonged spinal cord ischemia would result in total signal degradation, indicating a total absence of conduction. The time for N3 and N4 waves in SSEP to disappear may also define appropriated intervals to induce ischemic tolerance, as proposed by Matsumoto et al. [4]. It appears that N1 and N2 waves are presynaptic components, while the contrasting behavior of N3 and N4 waves suggests a postsynaptic origin [18].

Besides the proper duration of ischemic preconditioning, the adequate duration of the reperfusion time, before a subsequent deleterious event, need to allow the complete recover of the sublethal injury determined by the ischemic induction. In this regard, the recover of N1 component wave amplitude of SSEP to preischemic levels in the present study indicates the complete normalization of the conduction pathways.

How many cycles of sublethal ischemic stress should be used to induce ischemic tolerance has also been controversial. Based on the experience with the myocardium [15], we tested the effectiveness of one and three cycles of ischemia followed by reperfusion as the conditions for ischemic preconditioning. Although only the repetitive ischemic preconditioning process was efficient to prevent neurological deficit after descending aorta cross-clamping in the present study, we cannot assume that it was more effective than one single cycle. The high incidence of neurologic deficits with one cycle of ischemic preconditioning was associated with the occurrence of meningic hemorrhage in two of those experiments, precluding definitive conclusions about its value.

Looking for the lack of neuroprotection by ischemic preconditioning in some previous studies, one can speculate that it might be explained by the insufficient duration of ischemic pretreatment or the inadequate time window between the pretreatment and the subsequent insult. Cheng et al. showed that the later waves of SSEP are more sensitive to ischemia and disappear concomitantly with the decrease of N1 wave amplitude more than 6min after the induction of spinal cord ischemia in rabbits [18]. Using similar animal species, de Haan et al. [19] and Ueno et al. [11] did not demonstrate induction of spinal cord ischemic tolerance with short periods of sudlethal stress, while Matsumoto et al. [4], Munyao et al. [6] and Sakurai et al. [7] successfully used longer periods of ischemic preconditioning. On the other hand, the response of SSEP to spinal cord ischemic induction seems to be more precocious in dogs [17], justifying the use of short periods of aortic cross-clamping in the preconditioning cycles in the present experimental protocol.

Research into the mechanisms of immediate spinal cord preconditioning is limited, but some studies suggest a role for an increase in spinal cord blood flow [11,20]. Ueno et al. [11] speculated that this effect may occur by the attenuation of postischemic capillary no-reflow and by a direct vasodilating action. Meanwhile, Fan and associates demonstrated that positive changes in spinal cord blood flow were associated with decreased concentrations of nor-epinephrine and activation of the A1 adenosine receptor some minutes after the induction of ischemic preconditioning in rabbits [20]. However, further studies are needed to adequately delineate the biochemistry of acute ischemic preconditioning in the spinal cord.

On the other hand, although several mechanisms have been proposed to explain the delayed protection seen with ischemic preconditioning [15], it is likely that changes in gene expression of protective proteins play an important role in the nervous system [21]. Recent studies have demonstrated the presence of enhanced levels of heat shock proteins 24h or more after ischemic preconditioning of the spinal cord and that this fact was associated with the acquisition of ischemic tolerance to subsequent lethal ischemia [4,5,7]. Concomitantly, other authors have shown that the prior induction of the heat shock response in the whole animal may increase the content of stress proteins within the spinal cord and enhance the tolerance to ischemic effects of aortic occlusion [22,23]. It is hypothesized that in response to cellular stresses, heat shock proteins may allow denatured proteins to regain their conformation and facilitate the synthesis of new proteins.

The recover of the signal amplitude of the SSEP component waves after final aortic reperfusion has been correlated with the neurologic outcome in experimental [24] and clinical studies [25]. This fact was also observed in the present experience and is probably the result of a less important immediate compromise of the sensitive and motor pathways of the spinal cord. On the other hand, the existence of significant histopathologic changes in two animals submitted to repetitive ischemic preconditioning without apparent functional compromise opens the possibility of a delayed development of paraparesis or paraplegia. This finding is consistent with the observations of Kakimoto et al. [8] that showed a surprising occurrence of delayed neurologic injury after ischemic preconditioning in a rat model of spinal cord damage.

The present study has some limitations. The number of studied animals was not sufficient to provide an adequate evaluation of possible differences in SSEP recovery times and histopathologic scores, as well as of the difference in neurological outcome observed between the uses of one or three cycles of ischemic preconditioning. In addition, the dogs were followed-up only for 72h, situation that does not eliminate the possibility of delayed neurologic injury occurrence in those animals with some degree of histopathological damage. Nevertheless, we demonstrated that ischemic tolerance could be immediately achieved in the spinal cord against a clinically relevant ischemic insult, since ischemic preconditioning was based on the proper selection of induction times and intervals.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Sérgio A. Oliveira Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Contreras, I. S. B. Articles by Oliveira, S. A. Search for Related Content PubMed PubMed Citation Articles by Contreras, I. S. B. Articles by Oliveira, S. A. Related Collections Cerebral protection Great vessels Peripheral vascular