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J Thorac Cardiovasc Surg 1994;107:1044-1049
© 1994 Mosby, Inc.

CARDIOPULMONARY BYPASS, MYOCARDIAL MANAGEMENT, AND SUPPORT TECHNIQUES

Hemodynamic and cerebral repercussions arising from surgical interruption of the superior vena cavaExperimental model

Valladolid, Spain

From the Department of Thoracic and Cardiovascular Surgery ^a and Division of Neuropathology, ^b Hospital Universitario of Valladolid, Valladolid, Spain.

Received for publication May 13, 1993. Accepted for publication Sept. 27, 1993. Address for reprints: Jose A. Gonzalez-Fajardo, MD, Department of Thoracic and Cardiovascular Surgery, Hospital Universitario, 47011-Valladolid, Spain.

Abstract

This study was designed to analyze the hemodynamic and cerebral repercussions arising from the surgical interruption of the superior vena cava. The experiments were carried out in 12 mongrel dogs under two different conditions: with shunt (group A, n = 6) and without the installation of a shunt (group B, n = 6). The period of occlusion was 35 minutes. The right atrium pressure, pulmonary arterial pressure, and aortic pressure are not significantly modified in the two groups. The intracranial pressure had an important correlation with the central venous pressure (r²= 0.8572). In group B, the intracranial pressure had a sharp increase between the basal period (6.9 ± 1.47 mm Hg) and the clamping superior vena cava (17.2 ± 1.05 mm Hg), accentuated with the interruption of the azygous vein (32.2 ± 0.7 mm Hg). In group A, the use of a shunt avoided this alteration during clamping of the superior vena cava (6.8 ± 2.0 mm Hg) and the azygous vein (8.0 ± 2.24 mm Hg). However, after removal of the clamps in group B, an elevated residual intracranial pressure was observed (21.1 ± 3.33 mm Hg) in contrast to the central venous pressure, which returned to the basal values (4.4 ± 0.7 mm Hg). The biomechanic findings of the volume-pressure curves (with Miller and Marmarou-Shapiro tests) and the cerebral necropsy showed brain damage in group B, without the shunt. Three animals had areas of hemorrhagic infarction. Histologic study demonstrated signs the incipient vasogenic edema. In group A, all findings were compatible with the normal. In conclusion, these results suggest the importance of shunting the blood in those cases of a nonobstructed superior vena cava because the clamping and reconstruction produce hemodynamic compromise and brain damage. (J THORACCARDIOVASCSURG1994;107:1044-9)

The first clinical experiences in relation to the surgical substitution of the superior vena cava (SVC) ^1-3 brought up the question about the repercussions on the encephalic structures that the necessary interruption of the venous flow through the SVC could cause. In fact, in these experiences, the problem of cerebral edema and its clinical consequences arose nearly 60 minutes after the interruption of the venous flow. Coinciding with the perfection of anesthetic, surgical, and resuscitation techniques, a few papers have since been published in the last 10 years ^4-10 that describe the substitution of the SVC with a complete interruption of its flow, without the aid of a shunt, and for periods of 30 to 50 minutes, with no neurologic alterations being registered. However, a detailed analysis of these cases leads to the objection that, in some cases, the respective pulmonary or mediastinal pathologic process did not have the same degree of effect on the SVC wall, which makes it impossible to determine the hemodynamic repercussion that the illness had on SVC flow and, therefore, on the development of collateral pathways.

Recently, Piccione, Faber, and Warren ¹¹ suggested the importance of shunting the blood from the innominate vein to the right atrium in those cases of a nonobstructed SVC because the clamping and reconstruction can result in hemodynamic compromise in the intraoperative period and may also cause irreversible brain damage and the possibility of an intracranial bleeding episode.

In contrast with this study, Masuda, Ogata, and Kikuchi ¹² reported that 1-hour clamping of the SVC with the azygous vein ligated was safe in an experimental model of occlusion of the SVC with six cynomolgus monkeys. Only one monkey showed the effect of congestion in the brain. Although they affirmed that the cerebral perfusion pressure was within the margin of safety during clamping, the perfusion pressure was less than 40 mm Hg, which is the critical physiologic limit (normal level of safety 60 mm Hg). ^13,14 In addition, the use of sodium pentobarbital as an anesthetic (a potent drug that decrease the intracranial hypertension) could explain the lower level of intracranial pressure and its behavior.

This study was designed to analyze the hemodynamic and cerebral repercussions arising from the surgical interruption of the SVC under two different conditions: with and without the installation of a shunt. We have developed, at an experimental level, a substitutive model of the SVC ¹⁵ that is capable of permitting the study of the controversial factors and failures observed at the clinical level and the development of possible solutions.

MATERIAL AND METHODS

These experiments were carried out in 12 mongrel dogs, four male and eight female, with an average weight of 20.8 ± 2.9 kg. Anesthesia was induced with sodium thiopental (10 to 15 mg/kg intravenously) and was maintained with isoflurane (1% to 2%). The animals were intubated endotracheally, and their lungs were ventilated mechanically with oxygen. Tidal volume was set initially at 20 ml/kg, and respiratory rate was set at 12 breaths per minute. These initial parameters were modified after serial blood gas measurements to keep carbon dioxide tension between 25 and 35 mm Hg and oxygen tension and pH within normal limits. An intravenous infusion of saline solution (1000 ml) was administered during the operation.

The SVC were exposed through a right posterolateral thoracotomy at the level of the fourth intercostal space. The phrenic nerve was carefully preserved, and the azygous vein was controlled by means of vessel loops. After systemic heparinization (1.5 mg/kg intravenously), the animals were separated into two different groups: in the first (group A, n = six dogs), a venous cannula (Tygon number 4, Sorin Biomedica, Saluggia, Italy) was introduced as an external shunt into the right atrial appendage from the innominate vein for replacement of the SVC (Fig. 1); in the second (group B, n = six dogs), no shunt was used during the clamping of the SVC. The period of occlusion was 35 minutes. The experiment was divided into four stages: (1) basal or preclamping—the first register performed after the access to the thoracic cavity; (2) 5 minutes of SVC clamping; (3) 30 minutes of SVC and azygous vein clamping; (4) declamping—the first register performed after a period of stabilization. Special attention was given to the changes arising from the occlusin of the SVC and complementary clamping of the azygous vein.

View larger version (40K): [in this window] [in a new window]   Fig. 1. Experimental model with shunt. A venous cannula was introduced as an external shunt into the right atrial appendage from the innominate vein for replacement of the SVC.

Study of the cerebral repercussions
The study of the cerebral repercussions covered, in addition to the constant monitoring of the ICP, the analysis of volume-pressure curves (with Miller and Marmarou-Shapiro tests) ^16-18 and the cerebral necropsy at the end of the experiment.

Miller test. At 15 minutes after the declamping, 1 ml of saline solution was injected in 1 second through the cerebral intraventricular catheter. The gradient of pressure (P) was established by the difference between the initial pressure (Pi) and the final pressure (Pf) after the administration of a known volume ( V = 1 ml). The normal value is VPR < 3 to 4 mm Hg/cc, where VPR is ventricular pressure response, which is P/V.

Marmarou-Shapiro test. This test permits the calculation of the total compliance (C = 0.4343 PVI/Pf) of the craneospinal axis according to what is known as the pressure volume index (PVI = V/log [Pf/Pi]). Where Pi is the initial pressure and Pf the final pressure after the administration of a 1 ml ( V) of saline solution in 1 second through the cerebral intraventricular catheter. Normal value for PVI is 25.4 ± 2.4 ml. The physiologic limit of compliance is 0.4343 ml/mm Hg.

Cerebral necropsy. The animals were killed immediately after the experiment. The brain was fixed and stored in 10% neutral buffered formalin for the histologic study. After being embedding in parafin wax, specimens were sectioned at 5 µm and the sections were stained with hematoxylin and eosin.

Statistical analysis
The values obtained were entered as a data matrix in the statistical program SIGMA (Horus Hardware, Madrid, Spain). Results are shown as the mean ± standard error of the mean. Statistical analysis of the data was carried out by applying nonparametric randomized block analysis of variance (Friedman's test) to compare sequential data. Comparison of the two groups was done by Mann-Whitney U test. Statistical significance was assumed at p < 0.05.

All experiments were conducted in compliance with the "Principles of Laboratory Animals Care" formulated by the National Society for Medical Research and the "Guide for the Care and Use of Laboratory Animals" prepared by the Institute of Laboratory Animal Resources and published by the National Institutes of Health (NIH Publication No. 86-23, revised 1985).

RESULTS

Hemodynamic results
The AP results were similar in the two groups (A = 138.43 ± 12.07 mm Hg, B = 131.75 ± 15.83 mm Hg) during the different stages of the experiment (Fig. 2). The study of the right atrial pressure (A = 1.87 ± 1 mm Hg, B = 1.23 ± 0.68 mm Hg) and pulmonary arterial pressure (A = 21.62 ± 1.89 mm Hg, B = 20.12 ± 0.71 mm Hg) confirmed the stability of its values (Figs. 3 and 4). On the other hand, the CVP in group B, without the use of a shunt, increased sharply between the basal period and the time of SVC clamping—from 3.8 ± 0.4 mm Hg to 17 ± 2.4 mm Hg. This elevation was accentuated by the complementary interruption of the azygous vein (34.7 ± 1.30 mm Hg). Later, after both veins were unclamped, the CVP returned to normal values (4.4 ± 0.7 mm Hg). In group A, the use of a shunt prevented this change during SVC clamping (7.5 ± 0.33 mm Hg) and azygous vein (10.5 ± 0.8 mm Hg). The analysis of variance to compare sequential data was statistically significant (Friedman's test, p < 0.05). The comparison of the two groups was also statistically significant (Mann-Whitney U test, p < 0.05) (Fig. 5).

View larger version (14K): [in this window] [in a new window]   Fig. 2. Hemodynamic changes in systemic arterial pressure.

View larger version (14K): [in this window] [in a new window]   Fig. 3. Hemodynamic changes in right atrial pressure.

View larger version (13K): [in this window] [in a new window]   Fig. 4. Hemodynamic changes in pulmonary arterial pressure.

View larger version (14K): [in this window] [in a new window]   Fig. 5. Hemodynamic changes in central venous pressure. The analysis of variance to compare sequential data and the comparison of the two groups were statistically significant (p < 0.05).

View larger version (15K): [in this window] [in a new window]   Fig. 6. Hemodynamic changes in intracranial pressure. The analysis of variance to compare sequential data and the comparison of the two groups were statistically significant (p < 0.05).

Marmarou-Shapiro test. The calculation of pressure volume index points to the existence of an altered index in group B (13.9772 ± 0.68854), as opposed to group A, where the pressure volume index is within the physiologic limits (24.1587 ± 0.00003). These data correlated with the degree of cerebral distensibility (compliance), lowered in group B (0.1969 ± 0.0076) and normal in group A (3.4593 ± 1.559).

Cerebral necropsy. In group B, the brain was congested and friable, with an elastic tendency, and humid on cutting. The circumvallations were dilated, and the cerebral ventricles had normal dimensions. Three animals had areas of hemorrhagic infarction. The histologic study demonstrated dilation of the Virchow-Robin spaces and radial zones of spongiosis and edema with focal character at the cortical level with extension to the white substance. In group A (with shunt), all findings were compatible with the normal. There was no signs of edema or hemorrhagic infarction.

DISCUSSION

Although the interruption of the SVC flow in the animals without shunts produces a sharp increase in the CVP values, right atrial pressure, pulmonary atrial pressure, and AP levels are not significantly modified and remain normal. The complementary clamping of the azygous vein causes a new rise in the CVP as a consequence of the interruption of one of the most important collateral pathways in the SVC system. Concomitantly, the ICP is elevated from the beginning of clamping, following a linear relation with the CVP values; accordingly, average ICP values are 17.2 ± 1.05 mm Hg when the SVC is clamped and increase to 32.2 ± 0.7 mm Hg when the azygous vein is also ligated. This strong correlation between these two variables (CVP and ICP) is justified because the interruption of the SVC flow produces a venous stasis at the level of the cephalic territory and, therefore, problems in the absorption capacity of the cerebrospinal fluid. On the other hand, the vascular stasis causes difficulty in the carbon dioxide transportation of the tissues, and the slower circulation favors a certain state of cellular hypoxia, which contributes to a slight level of acidosis. Because hypercapnia is a fundamental factor in the production of vasodilation and the increase in the permeability, a vasogenic edema is possible. ^19,20 In this manner, the cerebral blood volume gradually increases because the blood becomes more and more trapped between the dilated arterial vessels and a venous system distended by the venous hypertension created. In addition, the obstruction of the venous flow causes an increase in the capillary pressure and, thus, causes the escape of the intravascular liquid toward the intersticial space (edema). These facts are correlated to the biomechanic findings of the volume-pressures curves, in which the existence of a great rigidity and, thus, slight cerebral distensibility is recorded. These parameters are indicators of brain damage and emphasize the importance of applying a shunt during the sharp interruption of the SVC and azygous vein when suitable collateral pathways have not yet developed.

The increase in the venous pressure and the presence of venous hemorrhagic infarctions in three animals of our series are an expression of the encephalic venous hypertension generated by the clamping of the SVC and azygous vein. The histologic study shows changes in group B with respect to the normal cerebral tissue, although these sometimes are not of a generated character and are not fully developed, what can be justified by two considerations: the abrupt nature of the venous hypertension and its short duration (35 minutes). Nevertheless, marked dilations of the Virchow-Robin spaces are observed, which are compatible with an incipient vasogenic edema in which the cerebrospinal fluid pressure would dissect the perivascular space. ²¹ The occasional presence of radial zones of spongiosis and edema focused on the cortical level and extending toward the white substance confirm the suspicion of neurologic lesion caused by the interruption of the SVC and azygous vein as a consequence of the high intracranial pressures produced. The cellular lesions (cytotoxic edema) cannot be measured objectively because they involve a defect in the cellular metabolic machinery with an accumulation of water for maintenence of osmotic balance.

In view of these data, we suggest that the effects of venous clamping in the human cases vary according to whether an SVC syndrome is already established or, on the contrary, the SVC remains nonobstructed. Two hemodynamic situations, therefore, can be found: For patients with SVC syndrome before operation, the venous clamping during the operation presumably might not cause brain damage, because of the existence of a functioning collateral venous network that supplements the obstruction to the SVC flow; for patients with intrathoracic disease that affects the SVC but without hemodynamic disorders, the sharp clamping of the SVC will significantly alter the venous pressures because of the lack of enough venous pathways. In these patients, the placement of a shunt during the period of clamping becomes imperative to avoid neurologic repercussions.

According to the hemodynamic modifications derived from the complementary occlusion of the azygous vein, we believe that the manipulations to this vein should be clinically limited to attempt to maintain its patency during the surgical intervention because this will ensure the existence of an important physiologic pathway for venous drainage; once the operation has been accomplished, the azygous vein should be ligated to raise the venous pressure through the SVC, thus increasing the percentage of patency. ^22,23

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