Eur J Cardiothorac Surg 1999;14:250-255
© 1999 Elsevier Science NL
Contribution of the interventricular septum to maximal right ventricular function
Uwe Klimaa,
J. Luis Guerrerob,c,
Gus J. Vlahakesb,c
a Department of Thoracic and Cardiovascular Surgery, Hannover Medical School, Medizinische Hochschule Hannover, Hannover, Germany
b Department of Surgery, Cardiac Surgery Division, Massachusetts General Hospital, Boston, MA, USA
c Harvard Medical School, Boston, MA, USA
Received 2 March 1998;
received in revised form 2 June 1998;
accepted 9 June 1998.
Corresponding author. Abteilung Thorax-Herz- und Gefäßchirurgie, Medizinische Hochschule Hannover, D-30623 Hannover, Germany. Tel.: +49 511 5323453; fax: +49 511 5325404; e-mail: klima@thg.mh-hannover.de
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Abstract
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Objective: Maximal right ventricular (RV) function is influenced by left heart hemodynamics, possibly mediated by the interventricular septum (IVS). We examined the potential contribution of the IVS function to right heart function. Methods: In 12 canine isovolumic right heart preparations, incremental volumes were introduced into a high compliance RV balloon until RV failure occurred. Maximal RV developed pressure (RVDP) and maximal positive RV dP/dt were determined with a working IVS at a constant left ventricular (LV) output of 2 l/min and at a constant mean arterial pressure of 80 mmHg. Thereafter the IVS was thermally inactivated, and measurements were repeated using the same protocol. Results: At constant arterial pressure and constant LV output, thermal inactivation of the IVS led to a significant decrease in maximal RVDP (inactivated vs. working IVS: 36.1±9.8 vs. 56.8±16.2 mmHg, respectively, P<0.001), and RV dP/dt (inactivated vs. working IVS: 720±220 vs. 1350±190 mmHg/s, respectively, P<0.001). Conclusions: These results suggest that the functional status of the IVS is a major determinant of maximal RV function. At constant LV conditions and arterial pressure, an inactivated IVS leads to a significant decrease in maximal RVDP and RV dP/dt under the conditions of this study.
Key Words: Interventricular septum • Right ventricular failure • Cardiac transplantation • Circulatory assist
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Introduction
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The cardiac surgeon is sometimes faced with right ventricular (RV) failure in two situations: (1) as an isolated problem following orthotopic heart transplantation, and (2) following institution of left-heart assist. RV failure is generally accepted as a pathophysiological entity by itself. The assessment of RV volume changes has allowed existing theories about RV failure to be confirmed
[1]. The anatomical disposition and geometry of the right ventricle allow it to adapt to wide variations in preload, but poorly to increases in afterload. In the case of RV failure, the right ventricle dilates and shifts the interventricular septum (IVS) to the left, decreasing left ventricular preload and, hence, the cardiac output. Consequently an often lethal vicious circle is induced. As the right and left ventricles cannot be considered independently of one another (`ventricular interdependence'
[2]
[3]), the IVS may contribute to the function of either ventricle and mediate changes in one ventricle, which will subsequently lead to changes in the other ventricle.
Very early studies in RV function have suggested a possible relationship between systemic hemodynamics and right heart performance
[4]. As an extension of these early studies, Vlahakes et al. showed that right heart performance is related directly to systemic pressure, and that the mechanism may involve the perfusion of the RV free wall. With increasing RV afterload, failure occurs and is associated with ischemia of the RV free wall; by increasing systemic pressure, ischemia and failure can be reversed, suggesting that ischemia is the mechanism of failure in RV overload
[5]. Increased RV afterload and preload can further complicate matters by impeding the circulation to the RV free wall
[6].
The determinants of RV function and the mechanisms involved in RV failure are undoubtedly more complex. Subsequent studies have shown that the relationship between left and right heart hemodynamics has a much more profound effect on right heart performance
[7], suggesting the role of ventricular interaction as determinant of maximal RV function.
The purpose of this experimental study was to investigate the influence of the IVS on maximal RV-function, independent of neural, humoral, pericardial and pulmonary circulatory influence. To achieve this goal, an isovolumic right heart preparation, combined with a controlled, working left heart preparation was implemented.
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Materials and methods
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Surgical preparation
The following protocol was reviewed and approved by the Subcommittee on Research Animal Care, Massachusetts General Hospital, and complies with the `Principles of Laboratory Animal Care' formulated by the National Society for Medical Research and the `Guide for the Care and Use of Laboratory Animals' prepared by the National Academy of Sciences and published by the National Institutes of Health (DHEW Publication No. (NIH) 86–23, revised in 1985, Office of Science and Health Reports, DRR.NIH, Bethesda, MD 20205).
Twelve mongrel dogs with a mean weight of 24.1±3.6 kg were anesthetized with pentobarbital (30–50 mg/kg i.v.), intubated, and ventilated. The chest was entered via a right lateral thoracotomy in the sixth intercostal space; the pericardium was incised and suspended to form a pericardial cradle to support the heart. To control RV volume in vivo, an intracavitary, high-compliance latex balloon was inserted into the RV. In this model, the right ventricle was isolated from the circulation by draining systemic venous return and coronary sinus drainage to a pump oxygenator. Oxygenated blood was returned to the femoral arteries, the left common carotid artery and the left atrium via separate calibrated bidirectional roller pumps. Blood could be pumped into or out of the arterial tree to control systemic pressure independent of cardiac output. The coronary arteries were left perfused directly from the ascending aorta. The high-compliance latex balloon was inserted into the RV through the transected pulmonary artery, and via the right atrium, the tricuspid valve was sutured closed to prevent balloon herniation. To ensure that the balloon could fill the entire RV cavity and conform maximally to its cavitary contours, the tricuspid valve chordae tendinae were cut, and the Thebesian venous blood was drained by a 14-gauge cannula inserted into the RV apex. Conformity of the balloon shape to the RV cavity, confirmed by echocardiographic imaging, indicated no separate space between the balloon and the ventricular cavity. The balloon was ligated at the pulmonary valve level around a 0.75 inch diameter polyurethane tubing. Measured amounts of saline were added or withdrawn through a port at the end of the tubing. The compliance of the latex balloon system was tested for each balloon volume used in the experimental setting (
Fig. 1
). During the experimental protocols, known amounts of saline were introduced in 10 ml increments into the RV balloon-tubing system. Via a separate port at the end of the polyurethane tubing, a micromanometer-tipped catheter (Millar Instruments, Inc., Houston, TX) was introduced into the middle of the latex balloon. The RV cavity balloon volume was determined as the total volume in the balloon-tubing system minus the volume in the tubing. To maintain a constant heart rate, the sinoatrial node was crushed, and the right atrium was paced at 110–120 beats/min.
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Fig. 1. Compliance of the latex balloon system. Known amounts of saline were incrementally introduced at 10 ml steps into the balloon-tubing system ex vivo. Pressure measurements were made with a micromanometer-tipped catheter, which was introduced into the balloon through a tubing side port. For all 12 animals compliance data were identical at each volume step. The linear regression was highly significant [pressure=0.09xvolume (ml)-0.73 (r=0.985; P<0.001)].
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Left heart output was controlled by infusing oxygenated blood from the cardiopulmonary bypass circuit into the left atrium at a known rate. LA pressure was measured via a fluid-filled catheter, inserted via a pulmonary vein and connected to a strain-gauge transducer (Spectramed, Oxnard, CA). LV pressure was measured with a micromanometer-tipped catheter, which was placed in the LV cavity. Systemic blood pressure, which was measured with a fluid-filled catheter in the right internal mammary artery, was adjusted at a constant level of 80 mmHg mean arterial pressure. Right coronary artery (RCA) flow was determined with an ultrasonic flow probe (Transonic Systems, Ithaca, NY).
Experimental protocol
Twelve preparations were studied in a series of hemodynamic stages created by increasing the volume of the RV balloon. Increments of 10 ml of saline were added at each stage until RV failure occurred: the point of RV failure was defined when a decrease in RV developed pressure (RVDP) occurred with the final administered RV balloon volume increment:
This protocol was conducted at a left heart output controlled at 2 l/min; mean arterial pressure was kept constant at 80 mmHg by pumping blood into, or out of, the femoral and left common carotid arteries.
After data were gathered, the IVS was inactivated as described. To investigate the possible contribution to RV function from the interventricular septum, a small right ventriculotomy (maximum length: 2 cm) was made parallel to the LAD; the interventricular septum was rendered non-functional by electrocoagulation and the ventriculotomy was closed. The entire hemodynamic protocol was repeated under the same conditions of left heart output and systemic pressure. The extent and efficiency of septal inactivation was verified at the end of each experiment by staining the heart with 2,3,5-triphenyl-tetrazolium chloride and measuring the non-viable zone of the septum (see
Section 2.3).
2.3 Postmortem studies
To calculate the proportion of right ventricular free wall perfused by the right coronary artery, the RCA was perfused Monastral® blue B suspension (Sigma Chemical Company, St. Louis, MO) at a pressure of 120–140 mmHg. To determine the proportion of the interventricular septum rendered non-viable, the left coronary artery was perfused 2,3,5-triphenyl-tetrazolium-chloride (Sigma Chemical Company, St. Louis, MO). The perfused hearts were incubated at 37°C in normal saline for 30 min, and were then fixed by immersion in phosphate-buffered formalin (pH 7.0). After fixation of the heart, the right ventricular free wall and the septum were separated and weighed. Subsequently, the macroscopically undyed areas were separated and weighed. The proportion of the RV free wall supplied by the RCA and the proportion of septum that was non-viable were calculated by this technique and expressed as a percentage of each entire territory.
Data analyses
Data are expressed as mean±SD. The paired t-test was used to compare peak RVDP between working and inactivated septum configurations. Linear regression analysis was performed to determine RV balloon compliance. To determine the influence of coronary artery flow in the working and inactivated septum preparation, one-way analysis of variance with repeated measures and the Student–Neuman–Keuls test were used. A value of P<0.05 was considered significant.
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Results
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Results of dog heart morphometric analyses are summarized in
Fig. 2
. Also shown in
Fig. 2 is the portion of the right ventricle perfused by the RCA territory and the portion of the interventricular septum rendered non-viable by thermal inactivation.
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Fig. 2. Morphometric data. Mean±SD; (n=12); IVS, interventricular septum; RV, right ventriclular free wall; LV, left ventricular free wall.
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The latex balloon and tubing system can introduce artefact in the measurement of RV pressure. The compliance relationship shown in
Fig. 1 was used to correct these measurements. This was done by subtracting the Pballoon compliance from the absolute developed pressure for every given balloon volume. The compliance test was performed for each balloon used and yielded identical regressions.
As shown in Table 1, there was a substantial and significant difference in maximal RVDP between hearts with a working vs. inactivated septum. Inactivation of the interventricular septum produced a substantial decrement in the global contractility of the right ventricle. There was a consequent significant decrement in the maximal pressure that the right ventricle could generate. Also demonstrated in Table 1 is the left ventricular performance prior to, and after, thermal inactivation of the interventricular septum. At a constant controlled left heart output of 2 l/min global left ventricular function decreased slightly with no statistical significance. Left ventricular systolic pressure with working versus inactivated interventricular septum: P=0.66. However, maximal positive LVdP/dt pressure with working vs. inactivated interventricular septum decreased significantly with P=0.01.
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Table 1. Maximal developed right ventricular pressure: effect of septal function under conditions of constant left heart hemodynamics
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Developed RV pressure was measured at increasing balloon volumes starting at 10 ml, until right heart failure occurred. In this isovolumic preparation, there was no significant increase in RCA flow under the influence of increasing RV balloon volumes as compared to the RCA flow at the starting point of each protocol with a RV balloon volume of 10 ml; however, there was a significant decrease of flow at the onset of RV failure (P<0.001).
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Discussion
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This acute study demonstrates that RV function is influenced not only by the RV free wall, but also by the interventricular septum and the left ventricle. There was a substantial and significant difference in contractility and maximal RVDP between hearts with working versus inactivated septae (P<0.05). Inactivation of the IVS leads to a significant decrease in maximal RVDP and RV dP/dt. Right coronary artery flow is diminished significantly at the onset of RV-failure.
When RV pressure is increased acutely, current evidence suggests that RV failure eventually occurs because of ischemia of the right ventricle
[5]
[8]. Myocardial ischemia results when oxygen demand exceeds oxygen supply. Blood flow to the myocardium is subject to autoregulation. Gregg et al.
[9] were the first to describe that, with increasing RV afterload, RCA flow increased. These observations were later confirmed by other investigators
[10]
[11]. In contrast to these studies, others
[12]
[13] failed to find an increase in RCA flow when RV systolic hypertension was induced. As demonstrated in Table 2 there was only a slight, statistically not-significant, increase in RCA flow from the first stage (balloon volume=10 ml) to the maximally observed RCA flow; an increase in RCA flow in proportion to demand (RV pressure) could not be found. The observations of the present study may have been a result of the fact that an isovolumic preparation was used, while these prior studies utilized ejecting right ventricles. However, at the onset of RV failure, there was significantly lower RCA flow than compared to the first stage (balloon=10 ml) and compared to the peak RCA flow, consistent with the role of RV free wall ischemia as a mechanism of RV failure. In addition to the increase in oxygen demand caused by RV hypertension, RV coronary artery driving pressure, defined as the difference between mean RCA pressure and mean RV pressure
[8]
[10], diminishes as the ventricle is loaded and may contribute to the occurrence of RV free wall ischemia. It may be argued that part of the RV free wall may be perfused from the left coronary system in the dog or that collateral flow from the left coronary system may contribute to the perfusion of the RCA territory, thus complicating the interpretation of RCA flow measurements. However, our postmortem studies revealed, that 81±7% of the RV free wall was supplied by the RCA. This confirms the observation of Murry and Vatner
[14] that, in the dog, minimal collateral flow occurs from the left coronary artery to the RCA territory. Consequently these data suggest that maintaining or increasing systemic pressure, and hence RCA flow, might be important as a treatment strategy in right heart failure.
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Table 2. Right coronary artery flow: Effect of the functional status of the IVS under constant left heart hemodynamics (mean aortic pressure=80 mmHg)
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In contrast to previously reported data
[15]
[16], in our experimental setting the measurements of maximal RVDP were corrected to account for Pballoon compliance in the isovolumic beating RV. Interestingly, none of these previous studies corrected RVDP for Pballoon compliance. However, as shown in
Fig. 1, the balloon and tubing system itself can alter the actual readings of data. This effect may be negligible at low balloon volumes, but certainly falsely increases RV pressure measurements at higher balloon volumes. If uncorrected this can lead to overestimation of maximal RVDP.
The IVS constitutes an important structural part of the heart and contributes to both left and right ventricular function
[17]. Under the influence of LV filling and contraction, circumferencial fibers shared by both ventricles
[2]
[18]
[19] are activated, and shorten. Li and Santamore
[20] implied in their study that the RV response to septal dysfunction depends on the type of dysfunction. In their experiments cutting the IVS of rabbits, horizontally and vertically, had no obvious influence on RVDP, but injecting glutaraldehyde into the IVS decreased RVDP significantly. In our preparation, we deactivated the IVS successfully by means of electrocoagulation. This produces loss of viability, confirmed by biochemical testing; this method of inactivation is thus most similar to the inactivation by glutaraldehyde injection used by Li and Santamore. Due to the fact that left heart hemodynamics are known to influence maximal RVDP
[7], observations in this study were made under conditions of controlled, constant left heart hemodynamics, with constant left heart output and systolic left ventricular (and hence, aortic) pressure. This type of model allows control of potential variables that may influence data obtained on right ventricular function. While such a well controlled and hemodynamically defined model might not correspond to the native physiology and hence the clinical situation, nonetheless such a highly defined model is needed to sort out the factors which might influence RV function. Previously published studies are difficult to interpret because these important variables were not controlled. Nonetheless, previous investigators have suggested that the IVS may play a role in RV function, and its inactivation by glutaraldehyde
[20] or by ischemia
[21] negatively influences RV function.
Critique and limitations of the method
An isovolumic model was selected for this study. While this type of model does not represent the clinical situation, there were specific reasons for its use. RV hemodynamics are complex with many determinants. Furthermore, in experiments where normal right ventricles are subjected to increasing load, tricuspid regurgitation can occur, making interpretation of data very difficult. Thus, in this study, an isovolumic preparation was used where RV volume was precisely controlled. The inlet and outlet of the right ventricle were appropriately managed to prevent balloon herniation, and Thebesian venous drainage was continuously drained to avoid its accumulation, which would increase RV volume. Furthermore, left-sided hemodynamics were precisely controlled to keep this important influence on RV function constant.
Prior to this study, we conducted pilot studies to help optimize the experimental model. In these hearts with small left atria, the amount of volume which can be pumped into the left atrium via the separate line from the roller pump is limited due to the occurrence of mitral regurgitation. Hemodynamic recordings revealed a sudden significant increase in left ventricular diastolic pressure as soon as mitral regurgitation occurred. As described by Katayama et al.
[22], during volume overload of the LV due to mitral regurgitation, the left ventricle accommodates a higher percentage of its total stroke volume during early diastole. This adaptation can be correlated with augmented systolic shortening, and thereby with increased restorative forces or elastic recoil, and with reduced chamber elastance and eccentricity during the early part of diastole. Thus, the pressure-volume overload not only results in depressed LV systolic mechanics, but also is associated with deterioration of global LV energetics and efficiency
[23]. Even though it is mechanically possible to pump more volume into the LA, left heart performance is altered and subsequent data interpretation, not only of the LV, but also of the RV would not be possible. In all dogs studied, the left heart could pump an output of 2 l/min. In some dogs however, mitral regurgitation occurred at a left heart output of 2.5 l/min. We therefore limited the LV volume load to 2 l/min.
Even by using a highly sophisticated animal model, not all of the influencing factors which might contribute to maximal right ventricular function can be separated from each other. Santamore
[24] has stated that right ventricular function is not only influenced by septal function but overall left ventricular dynamics. Thermal inactivation of the IVS led to a minimal, not significant, decrease in left ventricular systolic pressure under the conditions of our study. The inactivation did however show a significant decrease in LV dP/dt after the inactivation of the IVS. This again supports the hypothesis that both ventricles share common, circumferencial fibers
[2]
[18]
[19]. The inactivation of these fibers consequently impacts both ventricles performance. Even though this impact is obvious it cannot be avoided. We therefore considered left heart hemodynamics `constant' as left ventricular systolic pressure did not change after the thermal inactivation of the IVS, left heart output was controlled at 2 l/min and systemic aortic pressure (and hence coronary artery perfusion) was kept constant at 80 mmHg.
To gain access to the IVS and to electrocoagulate it for functional inactivation, a right ventriculotomy was necessary. It may be argued that the ventriculotomy of the RV per se is responsible for an impaired RV function and reduces RVDP. However, we investigated this issue in our pilot studies; peak RVDP did not differ between measurements of RVDP taken before and after the ventriculotomy. The ventriculotomy was performed over a maximum length of 2 cm.
A potential criticism of this preparation is that this type of instrumentation does not permit study with a closed pericardium. As noted by some investigators
[7]
[25], a closed pericardium enhances systolic ventricular interaction; thus the maximum pressure the RV can generate is less with an open pericardium than in the native state with the pericardium closed. Furthermore the influence of displacement of the IVS might actually be less in the open pericardium versus a closed pericardium preparation due do the ability of the RV free wall to expand further when the pericardium is open. Caution is necessary when drawing conclusions from an open pericardium preparation and relating it to human hearts in the clinical setting, unless considering an analogous situation such as after heart surgery.
In conclusion, the results of this experimental study suggest that the functional status of the IVS is a major determinant of maximal RV function. At constant LV loading and systemic pressure, inactivation of the IVS leads to a significant decrease in maximal RV developed pressure and RV dP/dt. In previously published studies describing the relationship between left heart hemodynamics and right heart function, these observations may be influenced, at least in part, by the interventricular septum. This finding supports the principle that, when managing right heart failure in cardiac surgery patients, left heart hemodynamics and developed pressure must be maximized.
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Abstract
Introduction
