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Ann Thorac Surg 1995;60:1230-1237
© 1995 The Society of Thoracic Surgeons
Department of Cardiovascular and Pediatric Cardiac Surgery, and Experimental Surgical Laboratory, Marie Lannelongue Hospital, Paris-Sud University, Paris, France
Accepted for publication June 2, 1995.
| Abstract |
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Methods. Three different degrees of right heart bypass were investigated in 5 mongrel dogs: (1) superior vena cava to both pulmonary arteries shunt (SCP); (2) inferior vena cava to both pulmonary arteries shunt (ICP); and (3) both venae cavae to both pulmonary arteries shunt (BCP). Hemodynamic studies included evaluation of the cardiac index and left atrial pressure as a function of the degree of right heart bypass.
Results. By maintaining the mean left atrial pressure at 5 mm Hg, cardiac indexes were 1.98 ± 0.25, 1.67 ± 0.29, and 1.33 ± 0.21 L min-1 m-2 for SCP, ICP, and BCP shunts, respectively (p = 0.001). When keeping the cardiac index constant, mean left atrial pressures were 5.2 ± 0.8, 5.5 ± 0.9, and 7 ± 0.7 mm Hg for SCP, ICP, and BCP shunts, respectively (p = 0.001).
Conclusions. Increasing degrees of right heart bypass are associated with a significant decrease in ventricular performance in this experimental model.
| Introduction |
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| Material and Methods |
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Operative Protocol
CARDIOPULMONARY BYPASS.
After general heparinization (300 IU/kg), cardiopulmonary bypass was established between both venae cavae cannulated through the right atrium, and the right femoral artery, using a console with three roller pumps (Sarns Travenol, Inc, Ann Arbor, MI) and a membrane oxygenator (type CML, Cobe, Inc, Denver, CO), which was primed with 50% homologous blood and 50% of a balanced salt solution containing 3% of modified gelatine (Plasmion, Roger Bellon, Paris, France). Further fluid additions were made using the same proportions.
TOTAL RIGHT HEART EXCLUSION.
After establishment of full flow cardiopulmonary bypass, snares were tightened around the caval cannulae and ventricular fibrillation was electrically induced. Through a right atriotomy, a large atrial septal defect was created. The posterolateral flap of the right atrial wall was sutured to the atrial septum to create a channel diverting the blood from both venae cavae and the coronary sinus into the left atrium through the atrial septal defect. The anterior wall of the right atrium was sutured over the posterolateral flap (Fig 1
). The heart was defibrillated after usual deairing maneuvers.
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2. Inferior vena cava to both pulmonary arteries shunt (ICP).
This shunt was obtained by tightening the inferior caval snare and clamping the superior limb of the conduit. This allowed inferior vena cava flow to return into the main pulmonary artery and superior vena cava flow to return into the left atrium. This shunt accounts for 60% of venous return [10]. It has no surgical equivalent but is similar, only in terms of pulmonary-to-systemic blood flow ratio, to a fenestrated Fontan, which theoretically allows a 33% right to left shunt [5].
3. Superior and inferior venae cavae to both pulmonary arteries shunt (BCP).
This shunt was obtained by tightening both caval snares and unclamping both conduit limbs so that all systemic venous blood except coronary sinus was diverted toward the main pulmonary artery. This shunt is similar to the clinically used total cavopulmonary connection [3].
WEANING FROM CARDIOPULMONARY BYPASS.
A silicone tube, 5 mm in diameter, was placed through pursestring sutures between the right ventricular outflow tract and the left appendage, to divert the remaining blood flow return to the right ventricle. An occluding snare was tightened around the main pulmonary artery, inducing total and definitive right heart exclusion. The animals were weaned from cardiopulmonary bypass with the right heart bypassed with an SCP shunt. The venous cannulas were removed, and the arterial cannula was left in place to allow subsequent volume loading adjustments.
Hemodynamic Studies
Hemodynamic data were obtained with volume loading adjustments, without inotropic support, and included two successive periods:
PERIOD 1: MEASUREMENTS WITH A CONSTANT MEAN LEFT ATRIAL PRESSURE.
During this phase, the mean left atrial pressure (LAP) was continuously kept at 5 mm Hg. The first hemodynamic assessment, in the SCP situation, was made 20 minutes after weaning from cardiopulmonary bypass. The degree of RHB was changed to ICP and a stabilization period of 20 minutes was again respected before the hemodynamic assessment. Then, the degree of RHB was changed to BCP and hemodynamic values were recorded 20 minutes later.
PERIOD 2: MEASUREMENTS WITH A CONSTANT CARDIAC INDEX.
The RHB degree was returned to SCP, and 20 minutes were allowed before the next hemodynamic assessment. The level of cardiac index was chosen to be for each dog similar to its first SCP value. We studied the hemodynamic variations using the same sequence of RHB every 20 minutes.
Pulmonary artery pressure was defined as the pressure in the corresponding limb of each derivation. No pressure gradient along the conduit limbs was found at any time during hemodynamic assessments. No abdominal banding was used throughout all experiments. The postoperative period was limited to 2 hours after the completion of the operation. Postmortem macroscopic examination was performed in all animals.
Statistical Analysis
All values were expressed as mean ± standard error of the mean. Comparisons in Tables 1 and 2![]()
were made with the repeated-measures analysis of variance, in search of an ``overall degree effect,'' followed by the Student's and Newman-Keuls tests for multiple comparisons if the analysis of variance was significant. Otherwise, paired Student's t tests were performed. In all cases, a p value of less than 0.05 was considered statistically significant.
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| Results |
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Period 1: Measurements With a Constant Mean Left Atrial Pressure
Hemodynamic data measured at a constant mean LAP of 5 mm Hg are summarized in Table 1
. Heart rate showed no statistically significant changes. Peak aortic pressure decreased progressively with increasing RHB degree, whereas mean aortic pressure showed no significant change. The mean pulmonary artery pressure increased significantly between SCP and BCP (p < 0.05). The degree of RHB had a significant influence on CI (p = 0.001). The CI, when changing from SCP to BCP, showed a statistically significant decrease of 34.1% ± 6.2%, as well as from ICP to BCP for which the decrease was of 19.4% ± 5% (Fig 3
). The arterial oxygen saturations increased significantly with increasing degrees of RHB. Indexed total vascular resistances (TVR), defined as (mean aortic pressure - mean left atrial pressure) x 80/CI, increased between SCP and ICP or BCP (p < 0.05).
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| Comment |
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A total right heart exclusion was created, under cardiopulmonary bypass, with the aid of a short period of ventricular fibrillation, avoiding aortic cross-clamping [6] or perfusion of inotropic drugs [8]. It is important to observe that no time-dependent changes in ventricular performance occurred during the hemodynamic study, as each animal served as its own control, and no significant changes in CI, mean LAP and indexed TVR were observed between the first and second periods of SCP. Previous experimental models have reported on complete RHB by creating cavopulmonary connections [8, 11]. One study [8], similar to ours for a complete RHB, did not allow any possibility of partial RHB because of the absence of tricuspid exclusion. Different types of partial RHB have been studied previously in separate preparations. Bidirectional cavopulmonary anastomoses were experimentally performed by Haller and associates [12]. Inferior vena cava to pulmonary artery anastomoses were experimentally investigated [13], but were associated with the occurrence of ascites and congestion of intraabdominal organs due to blood sequestration in the splanchnic area. These connections were performed toward only one branch of the pulmonary artery and not bidirectionally as in our experiments, explaining that such complications were never observed in ICP degree of RHB. None of these previously reported models allowed a direct comparative assessment of different degrees of RHB in the same animal. Important arterial desaturation occurred in SCP degree, in agreement with previously reported data in dogs [14], whereas arterial oxygen saturation was at an intermediary step in ICP degree despite the high venous flow and oxygen saturation of the renal veins [10].
Ventricular Performance and Right Heart Bypass
During complete RHB, volume loading adjustments were reported to increase simultaneously the mean LAP and cardiac output [11, 15]; a mean LAP of 6 mm Hg for a cardiac output of 94 mL min-1 kg-1 and a mean LAP of 10.2 mm Hg for a cardiac output of 146.5 mL min-1 kg-1 were observed by Nawa and associates [8]. Therefore, the ventricular performance was controlled according to the characteristic ventricular function curve (ie, the Frank-Starling curve) [11]. Our results during BCP shunt are fully consistent with these data at two different stages of our hemodynamic protocol (ie, BCP first and second periods).
In our model, hemodynamic variations were highly dependent on the degree of RHB. In the first period, at a constant mean LAP, a dramatic fall in CI occurred when the degree of RHB was increased. Conversely, during the second period, the mean LAP had to be significantly increased to keep the CI constant. It meant that the ventricular performance at a given degree of derivation was still controlled according to a characteristic ventricular function curve as volume loading adjustments, while increasing the mean LAP, could reverse the cardiac output at its higher initial level. Moreover, comparative assessments of the ventricular performance at different degrees of derivation showed significant changes because the same mean LAP resulted in significantly different levels of cardiac output for each degree of derivation. This showed that the ventricle worked on a family of ventricular function curves rather than on a single characteristic curve [16]; each curve corresponded to a degree of derivation, the most favorable curve belonging to the SCP degree.
Total Vascular Resistances and Right Heart Bypass
Within a biventricular circulation, the left ventricular afterload is proportional to SVR. In complete RHB, SVR are located in series with the pulmonary vascular resistances (PVR) because of the absence of interposition of a subpulmonary ventricle. Therefore, assessment of TVR, which could be expressed for a steady flow by the formula TVR = SVR + PVR [17], seems to be more meaningful. Thus, TVR in a Fontan circulation are higher than SVR in a biventricular circulation, and this increase in the ventricular afterload cannot always be considered as negligible. Senzaki and co-workers [17] reported that the total impedance, which represents in a more accurate fashion all the factors contributive to the ventricular afterload, abruptly increased to a level that should cause ``the unstable hemodynamics'' after the Fontan operation when the pulmonary artery index was below a critical value.
In our model, location of PVR could be represented diagrammatically by analogy with an electrical model of the circulatory system for the three degrees of RHB (Fig 5
). When resistances are in parallel, the resistance of the circuit is 1/R = 1/R1 + ...+ 1/Rn, whereas the value is R = R1 + ...+ Rn when they are in series. Therefore, location of PVR, partly in series with SVR (ie, partial RHB) or completely in series with SVR (ie, complete RHB), modified the resistances of the circulatory system that gradually increased at each successive degree of RHB even if PVR were expected to decrease because of the distention or recruitment of the pulmonary vessels due to a higher transpulmonary blood flow [15]. Absence of pulmonary arterial blood flow measurements did not allow us to perform that separate calculation of PVR and SVR. Nevertheless, indexed TVR increased significantly in the first period, probably in part due to baroreceptor influence, and, although not significantly due to the small number of experiments, indexed TVR increased by 23.2% ± 5.7% during the second period for a constant CI.
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Reciprocal Influence of Venous Return and Total Vascular Resistances
The relationship between venous return and TVR is clearly established by Guyton and co-workers [21]. Their study has shown ``the extreme importance of venous resistances in regulating venous return in contradistinction to almost insignificant effect of arterial resistances in most instances.'' Within a biventricular circulation, venous resistances are negligible. Conversely, PVR acting as venous resistances are of a tremendous importance in complete RHB because they are located at the outflow part of the major systemic veins and downstream to the great venous capacitance vessels, situated principally in the splanchnic area. Resulting blood sequestration decreases the venous return. Volume loading adjustments, by themselves, could overcome this decrease in cardiac output [21].
In our model, although energy loss along the conduits could have resulted in a greater level of venous resistances [3], increasing percentages of the systemic venous return go through the pulmonary vascular bed at each successive degree of RHB. In turn, this increased gradually the resistances to the venous return. Thereby, the venous return curves, according to the description of Guyton [22], are expected to be different at each degree of RHB.
Cardiac Output and Venous Return Curves Applied to Right Heart Bypass Operations
In our opinion, an integrated view of these hemodynamic changes could be approached by applying the principle of the equality of the cardiac output and venous return with an obligatory equilibrium point (ie, the point where cardiac output and venous return are equal) [22, 23]. After RHB operations, the cardiac output could be thought of as regulated by two separate groups of factors: (1) Those that could affect the ability of the heart itself to pump blood (ie, total afterload and myocardial contractility [23]) with the resulting consequences on the cardiac output curve. (2) Those that could affect the flow of blood from the systemic vessels to the heart (ie, the PVR and blood volume [23]) with the resulting consequences on the venous return curve.
Hemodynamic measurements performed while closing a fenestrated Fontan demonstrated a 20% to 30% decrease in cardiac output associated with a decrease in mean LAP in the absence of volume loading adjustments [5]. Such results, as well as those experimentally observed while opening an adjustable interatrial communication [6], could be explained by a modification of the venous return curve with an obligatory change in the equilibrium point [22] (Fig 6A
). Conversely, if there is a simultaneous change in both the venous return and cardiac output curves, as expected in our model (ie, between ICP versus BCP degrees), a greater decrease in cardiac output will occur due to the downward shift of the cardiac output curve (Fig 6B
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Our study allowed us to evaluate this latter specific aspect of hemodynamics associated with RHB operations. Obviously, direct clinical inferences might be considered debatable because the conditions of our experimental model were different from those observed in the clinical practice. Therefore, we are aware that it is necessary to further elucidate the different mechanisms involved in the ventricular performance after RHB operations using more sophisticated indices of ventricular function (ie, pressurevolume relationship) [24] and by analyzing the effects of the different factors that take part in the afterload in RHB operations [17]. However, the preliminary results obtained with our model in acute experiments would appear to warrant further and long-term studies to get certainty about the real cost, in terms of left ventricular performance, of the absence of a subpulmonary ventricle in a circulatory system placing the PVR more or less in series with the SVR.
| Acknowledgments |
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We wish to thank Gérard Allain, Michèle Gaillard, Philippe Fernette, Serge Litchenko, and Chantal Verriest for their excellent technical assistance. We gratefully acknowledge the critical suggestions provided by Paolo Macchiarini, MD, Thierry Folliguet, MD, Stephane Hatem, MD, Jean-Michel Grinda, MD, Sami Abdelmoulah, MD, and Jean-Jacques Mercadier, MD, PhD.
| Footnotes |
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| References |
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