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Ann Thorac Surg 1996;61:1316-1322
© 1996 The Society of Thoracic Surgeons
Institute for Biodiagnostics, National Research Council of Canada, Winnipeg, Manitoba, Canada
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Abstract |
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Methods. Twenty-two pigs were divided into four groups and exposed to either anesthesia alone, 120 minutes of HCA (15°C), 120 minutes of retrograde cerebral perfusion at 15°C during HCA, or 120 minutes of antegrade cerebral perfusion at 15°C during HCA, and then reperfused for 60 minutes under cardiopulmonary bypass at 37°C. The brains were perfusion fixed at the end of the experiments and examined by light microscopy.
Results. There were no morphologic changes in any areas of the brains in the anesthesia group, and very minor changes in some areas of the brains in the antegrade cerebral perfusion group. Varying severity of neuronal damage was found in the brains of all the pigs in the HCA and retrograde cerebral perfusion groups. The severity of ischemic damage in the brain showed the following descending order: hippocampus (CA4), caudate nucleus, cerebral cortex, putamen, thalamus, Purkinje cells of the cerebellum, pons, and mesencephalic gray matter. In the hippocampus the order of damage was CA4, CA3, polymorphous layer of the dentate gyrus, prosubiculum, CA2, CA1, and granule cell layer of the dentate gyrus. The damage in the retrograde cerebral perfusion group was less severe relative to the HCA group in many areas (no significance except mesencephalic gray matter).
Conclusions. These results demonstrate that the pattern of neuronal damage in pigs subjected to HCA and retrograde cerebral perfusion differs from the traditional pattern in that the caudate nucleus and hippocampal CA4 region are the most vulnerable to ischemia-hypoxia. Our results also suggest that antegrade cerebral perfusion prevented ischemic damage to the brain and retrograde cerebral perfusion provided some protection but moderately severe damage occurred.
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Introduction |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Histopathologic changes remain among the most important means for evaluating neuronal damage after ischemia-hypoxia injury. The majority of histologic studies of brain ischemic damage have been performed on small animals [4–6]. The traditional view is that the neurons in the CA1 region of the hippocampus are the most vulnerable to ischemia-hypoxia in both humans and experimental animals, such as the rat and gerbil. A few cerebral pathologic studies have been reported in the neonatal pig [7–9], and the results are controversial. Rootwelt and associates [9] found that brain damage varied considerably, and after severe hypoxia all neonatal pigs showed some damage in white matter/cerebral cortex. Laptook and co-workers [8] observed severe damage in the neocortex, hippocampus, and caudate nucleus from piglets subjected to 15 minutes of incomplete global normothermic brain ischemia. Fessatidis and colleagues [7] reported that in the neonatal pig after hypothermic circulatory arrest, the most severe damage was located in the Purkinje cells of the cerebellum. However, damage was scored over the entire hippocampus rather than in its subregions. There is currently little detailed pathologic information available in young pigs after hypothermic ischemia or in those subjected to retrograde cerebral perfusion. The present study used young pigs to evaluate the neuropathologic changes and the distribution of damage in the brain that arise as a consequence of circulatory arrest and to measure the potential protective effects of retrograde and antegrade brain perfusion during hypothermic circulatory arrest.
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Material and Methods |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Animal Preparation and Cardiopulmonary Bypass
Twenty-two male and female young pigs (commercial farm Yorkshire cross bred, 25 to 30 kg, 89 to 103 days old), which seem to be neurologically mature [10], were used. Preanesthesia was induced with xylazine (2.2 mg/kg), ketamine (20 mg/kg), and atropine (0.03 mg/kg) intramuscularly. After endotracheal intubation, the animal was ventilated mechanically with 60% oxygen and 40% nitrogen. The ventilator rate and tidal volume were adjusted to maintain the arterial carbon dioxide tension at about 40 mm Hg. Anesthesia was maintained with 1.0% to 2.0% isoflurane. A temperature probe was placed in the esophagus to monitor the core temperature. Catheters were placed in the right carotid artery and right external jugular vein for withdrawal of blood samples and measurement of blood pressure. Urine output was collected through a bladder catheter.
The surgical procedures and experimental management of the pigs were as described previously [11]. Briefly, the chest was opened via a median sternotomy. Heparin at 300 IU/kg was given intravenously. A cannula was inserted into the ascending aorta and used for arterial blood return to the body during normal cardiopulmonary bypass as well as for collection of blood returning from the brain during retrograde perfusion of the brain. Venous cannulas were placed into both the superior and inferior venae cavae. The superior vena caval cannula was used for collecting blood into the reservoir during normal bypass or for providing retrograde perfusion of the brain. A cannula was inserted into the innominate artery to provide antegrade perfusion of the brain. The left ventricle was vented via the left atrium. The lungs were not inflated during bypass or circulatory arrest.
The cardiopulmonary bypass circuit consisted of Cobe roller pumps (model C22.2; Cobe Cardiovascular, Arvada, CO), cardiotomy reservoir (Cobe), arterial filter (20 µm; Cobe Sentry), water bath (Lauda MGW type RMSG; Lauda Dr R Wobser GmbH & Co KG, Postfach, Germany), and a membrane oxygenator (Cobe CML) with integral heat exchanger. The circuit was primed with 1.5 L lactated Ringer's solution, 1 L homologous blood, and 5,000 IU heparin. Sodium bicarbonate was given to maintain the pH around 7.40, when necessary. Arterial blood gases were monitored and measured at 37°C with a blood gas analyzer (Stat 7; NOVA Biomedical, Waltham, MA). No correction was made for the temperature during hypothermia, and the alpha-stat approach was used. Blood electrolytes and osmolality were monitored and kept within the normal range. A 15% to 23% hematocrit was maintained (the normal pig hematocrit is about 30%). The bypass circuit was specially designed to be suitable for retrograde or antegrade brain perfusion and normal bypass by simply switching clamps.
Experimental Protocol
The pigs were randomly assigned to one of the following groups: group 1, anesthesia (control) (n = 5); group 2, circulatory arrest (n = 5); group 3, circulatory arrest + retrograde cerebral perfusion (n = 7); and group 4, circulatory arrest + antegrade cerebral perfusion (n = 5). Cardiopulmonary bypass in the pigs was initiated and maintained for a period of approximately 30 minutes at 60 to 100 mL•kg-1•min-1 flow with gradual cooling of the pig until the esophageal temperature was lowered to 15°C. The arterial pressure was maintained between 60 and 100 mm Hg. When the core temperature reached 15°C, the pigs received 120 minutes of circulatory arrest in group 2 and 120 minutes of circulatory arrest plus retrograde or antegrade cerebral perfusion in groups 3 and 4, respectively. During antegrade brain perfusion, the brain was continuously perfused with blood at 15°C via the innominate and carotid arteries. The right carotid artery pressure was monitored continuously and maintained at 65 to 85 mm Hg with a blood flow of 180 to 200 mL/min. In the retrograde group, the brain was continuously perfused with blood at 15°C through the superior vena cava for the entire 120-minute period of hypothermic circulatory arrest. The right jugular venous pressure was monitored continuously and was maintained at 35 to 45 mm Hg with a concomitant blood flow of 300 to 500 mL/min. A water circulation blanket was used to cover the pig to maintain the core temperature at 15°C during circulatory arrest. At the end of circulatory arrest, retrograde perfusion, or antegrade perfusion, bypass was started again in all groups with gradual rewarming to 37°C, and continued for 60 minutes.
Tissue Preparation
At the end of the experiment, which was 180 minutes after the onset of circulatory arrest with or without retrograde or antegrade cerebral perfusion, the brain was perfused under anesthesia with heparinized saline solution through the carotid arteries to wash blood from the brain, which was followed by perfusion with 10% buffered formaldehyde solution. The perfusion pressure was monitored and maintained between 80 and 120 mm Hg. After perfusion fixation, the pig head was immersed in 10% buffered formaldehyde solution and kept at 4°C for 24 hours. The brain was then removed for further fixation by immersion in the same solution at 4°C. After 2 weeks of immersion fixation, the brain was separated into anatomic areas of interest. The tissue blocks were further cut into approximately 1 x 1 x 0.5-cm slabs (samples), which were transferred to a 30% sucrose solution and kept at 4°C overnight. The tissue slabs were placed into 2-methylbutane (-40 to -50°C) for 30 to 60 seconds and then were transferred to a cryostat (-40°C) for 5 minutes. The samples were stored in the deep freezer (-70°C) for at least 24 hours before sectioning.
The prepared samples were cut into 5-, 10-, 15-, and 20-µm-thick slices using a cryostat (at a temperature of -25° to -28°C). The slices were mounted on uncoated slides and dried at room temperature. Hematoxylin and eosin staining was performed on every tenth section. The severity of injury was based on the number of damaged neurons in eight different brain areas including the pons, mesencephalic gray matter, Purkinje cells of the cerebellum, thalamus, putamen, cortex, caudate nucleus, and pyramidal neurons of the hippocampus. During this early period after the onset of hypoxic ischemic brain injury, the minimum criteria for diagnosis of ischemic neuronal damage (ischemic cell change) included mild cytoplasmic eosinophilia, shrunken neurons with scalloping of the margins, and nuclear changes consisting of coarse nuclear chromatin or pyknosis [12, 13]. Injury was graded (0 to 5) based on the number of damaged neurons in eight slices that contained the same areas. The pathologist was blinded to group assignment. Neurons were counted using a rectangular ocular graticule at an ocular magnification of 400. The grades were defined as follows: grade 0, no damaged cells; grade 1, less than 10% damaged cells; grade 2, 10 to 25% damaged cells; grade 3, 25 to 50% damaged cells; grade 4, 50 to 75% damaged cells; and grade 5, greater than 75% damaged cells.
The hippocampus was further divided into seven regions (CA1, CA2, CA3, CA4, polymorphous and granule cell layers of the dentate gyrus, and prosubiculum) based on morphologic criteria. In these regions, the severity of damage was evaluated as the percentage of damaged neurons counted in four different slices that contained the same region.
The total grade damage of the brain was determined by addition of the scores from the ten areas of the brain. The evaluation of total hippocampal damage was made by averaging the percentage of damaged neurons from seven regions of the hippocampus.
Statistical Analysis
All data are presented as mean ± standard error of the mean. Comparisons between groups of results for total brain damage and hippocampal damage were carried out by analysis of variance. The Tukey test was used for comparisons of pathologic results between the different areas of the brain and hippocampus. Values of p less than 0.05 were considered to be significant.
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Results |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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, there were generally no morphologic changes in any region of the brain including the hippocampus, caudate nucleus, and cerebellum in the anesthesia control group (group 1). Very little pathologic change was found in group 4. By contrast, neuronal damage of varying severity was present in all areas of the brains in groups 2 and 3. A characteristic acute degenerative change was found in these damaged neurons in which the cytoplasm of the neuronal soma became shrunken with scalloped margins and distinct acidophilia, pyknosis of the nucleus and rhexis to lysis, and liquefaction of the remnants of condensed cytoplasm (Fig 1). In group 2 significantly more damage was found in the CA4 region of the hippocampus relative to the other regions, including mesencephalic gray matter and the hippocampus CA1 region (Fig 2). The CA4 region of the hippocampus in group 3 showed significantly more damage relative to other areas including the putamen, thalamus, hippocampus CA1, Purkinje cells, pons, and mesencephalic gray matter (Fig 3). In the caudate nucleus, three different sizes of neurons (large, medium, and small) were easily distinguished. The most severe damage was present in clusters of medium-sized neurons, and the least damage was found in foci containing large neurons. In the cortex the damage was more severe in the deep laminae than at the surface. Selective damage subsequent to ischemia showed the following descending order: hippocampus (CA4), caudate nucleus, cerebral cortex, putamen, thalamus, Purkinje cells of the cerebellum, pons, and mesencephalic gray matter. The distribution pattern of tissue damage in the brains from groups 2 and 3 was very similar (see Figs 2, 3). There was no histologic evidence of damage in the white matter at this early stage of injury.
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). However, varying numbers of damaged neurons were found in all regions of the hippocampus except the granule cell layer of the dentate gyrus in groups 2 and 3. The damage was significantly more severe in the CA4 region compared with that in the CA1, CA2, dentate gyrus, and prosubiculum in groups 2 and 3. The hippocampal regions with ischemic damage were, in descending order: CA4, CA3, polymorphous layer of the dentate gyrus, prosubiculum, CA2, CA1, and granule cell layer of the dentate gyrus (Figs 4, 5). There was no difference between groups 2 and 3 in the pattern of damage of the hippocampus.
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, there was no neuronal damage in the control group and little damage in group 4; however, the damage in groups 2 and 3 was significant. The total grade of brain damage in group 2 was significantly higher than that in group 3. However, there was no significant difference in total damage to the hippocampus between groups 2 and 3, even though the average percentage of damaged neurons in group 3 appeared to be lower than that in group 2. The severity of damage in all the brain areas tended to be lower in group 3 than in group 2; however, the difference was statistically significant only in the mesencephalic gray matter (see Table 1
).
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Comment |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Our results showed no morphologic change in the control group of pigs, which confirms that the method of tissue sample preparation is suitable and not susceptible to dark cell artifact, which might be mistaken for early neuronal damage. Various degrees of neuronal damage were observed in most areas of the brains of pigs after 120 minutes of hypothermic circulatory arrest. Those damaged neurons presented characteristic changes and were easily identified. One of the most important findings in the present study is that the pattern of damage in the pig model appears to be different from what has been observed in other animals. The most severe damage was present in the CA4 region of the hippocampus and the caudate nucleus, followed by the hippocampal CA3 region, putamen, and cortex. However, the CA1 region of the hippocampus and Purkinje cells of the cerebellum suffered negligible damage. A similar pattern of damage was also demonstrated in pigs that received 120 minutes of retrograde cerebral perfusion during hypothermic circulatory arrest. Generally, the pyramidal neurons of the hippocampus (CA1 region) are considered to be the most damaged by ischemia-hypoxia, as they are very sensitive to oxygen deprivation [15, 16]. Since selective vulnerability of the CA1 region of the hippocampus has become accepted, many pathologic studies using different models only focus on very narrow areas of the brain rather than on the whole brain. According to our results, the pattern of ischemic damage to the brain is not uniform and may vary with species, age, or model.
The reasons for the different pattern of damage observed in the young pigs of this study are unknown. Several possibilities exist. Firstly, specific areas of the brain may exhibit delayed neuronal death after brain ischemia, and the time required for delayed death could vary with the species and the severity of ischemia [5,17–21]. Therefore, the pattern of selective vulnerability may vary with time after ischemia in different models or even in the same model. The extent of damage observed in the CA1 region after 1 hour of brain reperfusion in this experiment may be incomplete. Regardless of the presence of delayed neuronal death in the CA1 region or its natural resistance to ischemia in the young pig, our results suggest that the neurons in the CA4 region and caudate nucleus are the most vulnerable to ischemic damage. This could be used to evaluate early pathologic changes and assess therapeutic effects. Second, hypothermic conditions may have altered the pattern of sensitivity of the neurons in different areas of the brain. Third, it was reported that age affects the pattern of regional vulnerability to hypoxia-ischemia in the rat [22]. Our results may differ from those of Fessatidis and colleagues [7] as a result of the age difference in the pigs (young pig versus neonatal pig). Finally, the vulnerability of neurons in the young pig may differ from that of other species.
Retrograde cerebral perfusion through a superior vena caval cannula is a technique used to protect the brain during circulatory arrest [2]. Even though this technique has been used clinically, it is not entirely satisfactory. Our current results show that prolonged circulatory arrest (120 minutes) with hypothermia results in significant damage to most areas of the brain. Retrograde perfusion during hypothermic circulatory arrest appears to reduce, but not prevent, the ischemic damage in most brain areas; however, a statistically significant benefit was demonstrated only in total damage to the brain and in the mesencephalic gray area. Our preliminary experiments on blood flow show that the small amount of blood that reaches the brain is delivered mostly to superficial regions. Blood distribution to the brain during retrograde perfusion is not as uniform or as complete as during antegrade perfusion due to low perfusion pressure and flow shunt to the inferior vena cava through many communicating veins (Ye et al; unpublished results).
Based on the pathologic findings, antegrade perfusion is able to prevent ischemic damage of the brain during hypothermic circulatory arrest. It appears to be the superior technique for brain protection. However, this method is not practical in some clinical situations, for example, in patients with vascular diseases, which are quite common in adult patients with heart disease. Therefore, retrograde cerebral perfusion is still an alternative clinical technique.
In summary, we suggest that the pattern of brain damage resulting from ischemia may vary with species and model. In the pig model, the neurons in the CA4 region of the hippocampus and medium-sized neurons of the caudate nucleus are the most vulnerable to hypoxia-ischemic damage. The young pig may provide a good model for studies of early and selective pathologic change to evaluate the effects of ischemia and various therapies. From a pathologic point of view, antegrade cerebral perfusion provides good brain protection and retrograde perfusion of the brain provides only partial protection during prolonged (120-minute) hypothermic circulatory arrest.
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Acknowledgments |
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Footnotes |
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TopFootnotesAbstractIntroductionMaterial and MethodsResultsCommentAcknowledgmentsReferences |
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Address reprint requests to Dr Deslauriers, Institute for Biodiagnostics, National Research Council of Canada, 435 Ellice Ave, Winnipeg, Manitoba, Canada R3B 1Y6.
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|
|
|
|
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|
|
|
|
|
|
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