Increased Airway Pressure and Simulated Branch Pulmonary Artery Stenosis Increase Pulmonary Regurgitation After Repair of Tetralogy of Fallot
Real-Time Analysis With a Conductance Catheter Technique
Background Pulmonary regurgitation (PR) is an important determinant of outcome after repair of tetralogy of Fallot. Baseline PR was measured by magnetic resonance (MR) phase velocity mapping and from real-time right ventricular pressure-volume loops with a conductance catheter. Subsequently, the impact of two loading maneuvers (increased airway pressure, simulated branch pulmonary artery stenosis) on PR was assessed by the conductance catheter method.
Methods and Results Thirteen patients, 3 to 35 years after tetralogy of Fallot repair or pulmonary valvotomy, had PR measured by MR phase velocity mapping while breathing spontaneously. During catheterization under general anesthesia, PR was estimated from right ventricular pressure-volume loops generated by conductance and microtip pressure catheters. The effect of increased airway pressure (continuous positive airway pressure, 20 cm H2O; n=12) and simulated branch pulmonary artery stenosis (transient balloon occlusion of a branch pulmonary artery, n=7) was measured. Basal PR fraction derived by MR and from right ventricular pressure-volume loops had a correlation coefficient of .76 and mean of differences of 2.0±18.2% (95% limits of agreement). Increased airway pressure increased PR (16.3±11.4% to 25.7±17.3%, P<.01). Simulated branch pulmonary artery stenosis increased right ventricular end-systolic pressure (69.1±21.4 to 78.7±23.1 mm Hg, P<.05) and PR (27.5±11.3% to 36.9±12.8%, P<.05).
Conclusions There was reasonable agreement between MR phase velocity–derived PR fraction and that obtained from right ventricular pressure-volume loops generated by use of conductance and pressure-microtip catheters. Exacerbation of PR by increased airway pressure and branch pulmonary stenosis may be relevant to the acute postoperative and long-term management, respectively, of patients after repair of tetralogy of Fallot.
Pulmonary regurgitation is increasingly being recognized as an important factor in late outcome after tetralogy of Fallot repair.1 PR has repeatedly been demonstrated to impair RV function and exercise tolerance,2 3 4 and it may increase the risk of sudden death after repair of tetralogy of Fallot.5 6 For any given patient with PR, there are at least two sets of questions to be addressed: (1) What are the hemodynamic determinants of PR, ie, what anatomic and physiological factors determine how much PR a heart experiences? (2) What determines the effect of this PR on functional outcome and survival, and how is this affected by therapeutic interventions?
To approach the first question requires an assessment of the impact of RV loading conditions on PR. This in turn implies that the technique used to measure PR should be able to quantify changes in PR on a beat-to-beat basis. Our group has previously reported7 a method to quantify PR from RV pressure-volume loops using a microtip pressure catheter and digitized RV angiograms. In this study, the technique has been extended by measuring RV volume with a conductance catheter, allowing real-time assessment of RV pressure-volume loops. The second question involves serial quantification of PR, preferably by a noninvasive method, and relating this to exercise tolerance, survival, and timing of interventions. MR phase velocity mapping has been validated for the measurement of PR8 and offers an excellent opportunity to address these issues.
In patients with symptoms of right heart failure late after RVOT surgery who were undergoing right heart catheterization under general anesthesia, we investigated the impact of two loading conditions (elevated airway pressure and simulated branch pulmonary artery stenosis) on PR. All patients also had PR measured by MR phase velocity mapping while breathing spontaneously to allow comparison between the two techniques.
Thirteen patients late after RVOT surgery were referred for cardiac catheterization to investigate diminished exercise tolerance (n=12) and syncope (n=1, patient 3). All patients gave informed consent to a protocol approved by the Royal Brompton Hospital ethics committee. Patient characteristics are given in the Table⇓. Ten patients had undergone repair of tetralogy of Fallot, and 3 had treatment for critical pulmonary valvar stenosis (2 surgical pulmonary valvotomy, 1 pulmonary valve balloon dilatation in the early experience with the technique in this hospital). These patients were included because the primary purpose of this study was to investigate the effect of two loading maneuvers on PR rather than any features unique to the right ventricle late after repair of tetralogy of Fallot. No patient had evidence of a residual ventricular septal defect or any abnormal source of pulmonary blood flow.
Cardiac catheterization was carried out under general anesthesia with the patients intubated and ventilated according to our usual protocol. Three femoral venous sheaths and one femoral arterial sheath were inserted percutaneously. PR was measured after routine right and left heart catheterization was completed. In one patient, PR was measured before and after left pulmonary artery dilatation and stenting. RV pressure-volume loops were generated with a 7F pigtail eight-electrode, single-field conductance catheter (Webster) with an interelectrode distance of 0.9 to 1.1 cm and a 2.5F micromanometer (Millar) loaded inside a second 7F pigtail catheter (Cordis). Care was taken to place both the pigtail catheters in the RV apex so as to form a gentle curve from the RV apex across the tricuspid valve and into the inferior vena cava.9 No further catheter manipulation was performed after this position was obtained. The conductance catheter signal encoding volume and ECG data were fed to a stimulator/processor unit (Sigma-5, CardioDynamics) and then to a committed microcomputer, in which they were integrated with the amplified pressure signal (Fylde Isotransducer Amplifier) in custom-designed software. All measurements were corrected for blood resistivity. Parallel conductance was determined by the hypertonic saline method10 with injection of 5 mL 6% NaCl into the side arm of a venous sheath and subtracted from the catheter signal. No attempt was made to assess α, the dimensionless scaling factor, which was assumed to be unchanged throughout the studies.
The protocol consisted of RV pressure-volume measurement in three conditions: (1) ventilator switched off in end expiration, (2) continuous positive airway pressure of 20 cm H2O, and (3) ventilator switched off in end expiration with a 20-mL sizing balloon (7F, Cordis) inflated to occlude either the right or left pulmonary artery, with care taken to occlude only the ipsilateral pulmonary artery. When there was a preexisting branch pulmonary artery stenosis or hypoplastic segment, this artery was occluded. All recordings were made for 30 seconds of acquisition and in conditions 2 and 3 were obtained once the pressure-volume loops had reached a steady state, after about 5 beats. In condition 3, recordings were also made during balloon deflation. The pulmonary regurgitant fraction was measured from the pressure-volume loops according to our previously described criteria.7 The pulmonary regurgitant volume (x) was indexed to total RV stroke volume (y); ie, it is expressed as pulmonary regurgitant fraction (x/y, Fig 1⇓).
All patients had PR measured by MR phase velocity mapping as described by Rebergen et al,8 with the patients breathing spontaneously. Only the youngest patient required sedation with 0.1 mg/kg intranasal midazolam. A 0.5-T Picker system was used with cardiac gating. After multislice transaxial spin-echo imaging, an oblique sagittal plane was selected that visualized the right ventricle and its repaired outflow tract, and cine acquisition (TE8) was performed. A transverse plane through either the RVOT or the main pulmonary artery was selected, and through-plane phase velocity mapping was performed with a cine phase difference gradient echo (TE6) sequence with slice-select velocity encoding, interleaved reference, and velocity-encoding steps with two-phase encoding steps of 128 cardiac cycles each. Slice thickness was 8 mm, and there was a 30- to 40-cm field of view. Sixteen frames per cardiac cycle were acquired with an unsampled gap at end diastole of 15% of the cardiac cycle. For each frame, flow was defined as the product of cross-sectional area and mean through-plane velocity. Cross-sectional area was obtained by manually outlining the area of interest. Once a flow-against-time curve was obtained, pulmonary regurgitant fraction was defined as the integral of the retrograde flow divided by the integral of the antegrade flow (Fig 2⇓). The investigator performing the MR scans was blinded to the results of the cardiac catheterization–derived PR and vice versa for the catheterization team.
The effect of the two loading maneuvers (conditions 2 and 3) were compared with the baseline condition 1 by use of the Wilcoxon signed rank test. MR phase velocity–derived PR was compared with conductance-derived PR by the Pearson correlation coefficient and calculation of the mean and SD of the differences between the two values for each patient.11 The null hypothesis was rejected if P<.05. Results are presented as mean±SD unless otherwise stated.
Cardiac Catheterization Results
Two patients had residual pulmonary stenosis, 2 had significant bilateral branch pulmonary artery stenosis, 1 had left pulmonary artery stenosis, and 1 had mild right pulmonary artery stenosis. Patient 6 had severe tricuspid regurgitation. None of the patients had a residual ventricular septal defect.
Comparison of PR Measured by MR Phase Velocity Mapping and Conductance Method (n=13)
Demographic data, MR-derived pulmonary regurgitant fraction, and conductance-derived pulmonary regurgitant fraction in the basal state (condition 1) for each patient are presented in the Table⇑. Despite the very different conditions of ventilation, there is reasonable agreement between the two estimates of PR (Fig 3⇓). PR has been reported as pulmonary regurgitant fraction, ie, pulmonary regurgitant volume divided by RV stroke volume. However, stroke volume by conductance measures total RV stroke volume (both retrograde into the right atrium and antegrade into the pulmonary artery), whereas MR phase velocity mapping was performed only in the RVOT/pulmonary artery and so only antegrade RV stroke volume was obtained, resulting in an underestimate of the denominator of pulmonary regurgitant fraction. Patient 6 had severe tricuspid regurgitation, was the only patient with more than trivial tricuspid regurgitation on Doppler echocardiography, and is a clear outlier. With patient 6 included, there is essentially no relationship between MR- and conductance-derived PR (correlation coefficient, .5; mean of differences, −0.8±26.6% [±95% limits of agreement]); however, with patient 6 excluded, the correlation coefficient is .76; mean of differences, 2.0±18.2% (±95% limits of agreement).
Effect of Increased Airway Pressure (n=12)
There was no significant difference in PR between inspiratory and expiratory phases of routine positive-pressure ventilation (inspiratory PR, 25.5±19.3%; expiratory PR, 14.0±14.9%; P=.49). However, compared with basal measurements (n=13), continuous positive airway pressure of 20 cm H2O led to an increase in the pulmonary regurgitant fraction from 16.3±11.4% to 25.7±17.3% (P<.01). There was no significant change in RV end-systolic pressure, end-diastolic pressure, or RV stroke volume.
Effect of Simulated Branch Pulmonary Artery Stenosis (n=7)
Simulated branch pulmonary artery stenosis resulted in an increase in PR from 27.5±11.3% (SD) to 36.9±12.8% (P<.05) and an increase in RV end-systolic pressure from 69.1±21.4 to 78.7±23.1 mm Hg (P<.05). There was no significant change in RV end-diastolic pressure (balloon up, 16.6±6.0 mm Hg; balloon down, 16.8±6.4 mm Hg; P=.61) or RV stroke volume (balloon up, 15.7±8.3 mL; balloon down, 17.2±8.7 mL; P=.09). Patient 13 had PR measured immediately before balloon dilatation and stenting of a left pulmonary artery stenosis (Fig 4A⇓), after stenting (Fig 4B⇓), and finally with a balloon inflated within the stent (Fig 4C⇓). Before stenting, RV pressure was suprasystemic, with PR=38%; after stenting, the RV pressure fell to two-thirds systemic and PR=24%; however, after balloon inflation within the stent, RV pressure became suprasystemic again and PR=42%, recapitulating the prestent hemodynamics.
The patients in this study were referred for cardiac catheterization because of symptoms and represent a skewed sample. There was a preponderance of residual stenoses and high RV pressures, partially reflecting the increased stroke volume secondary to PR passing across these stenoses. Nonetheless, we believe that our data have implications not only for those with severe residual lesions but also for the approach to assessment and management of these patients in general.
Although the early surgical results of repair of tetralogy of Fallot continue to improve, for cohorts reported to date it is clear that patients are not cured of their disease. Their constant-phase hazard is still double that of the normal population,12 and although a 32-year actuarial survival of 86% is excellent, it is significantly lower than the 96% survival of the control population.13 Residual hemodynamic defects are at least partly responsible for this, the most common defects being branch pulmonary artery stenoses and PR. Current surgical strategy aims to relieve stenoses as completely as possible even at the expense of PR, which is well tolerated in the short term. However, the impact of isolated congenital PR on survival becomes apparent only after 30 to 40 years of follow-up.14 Given that in developed countries the majority of children with tetralogy of Fallot undergo complete repair by 2 years, these data, together with the many reports of the adverse impact of PR on RV function, exercise tolerance, and even ventricular arrhythmias, imply that one can no longer assume that an infant who undergoes surgery will tolerate a lifetime of PR.
Measurement of RV Volumes by the Conductance Catheter
Much of the previous uncertainty about the effect of PR on RV function was due to the difficulty in objectively quantifying either of these variables, the crucial problem being assessment of RV volumes. RV volume measurement is challenging because of the complex geometry of the chamber and its trabeculations.15 Most previous studies have used the presence of clinical surrogates of PR2 13 16 or semiquantitative techniques such as Doppler echocardiography.3 17 Measurement of a single dimension or area is an inadequate representation of RV volume, and more sophisticated analyses have involved geometric assumptions and/or required invasive placement of tissue markers.15 18 Radionuclide and MR methods do not have the temporal resolution to assess the impact of loading maneuvers. Although two-dimensional echocardiography has adequate time resolution to assess the impact of changes in loading conditions, area measurement requires planimetry that is difficult in the presence of trabeculations, and volume measurement necessitates additional geometric assumptions and multiple views that are difficult to repeat exactly.
The conductance catheter has been extensively validated for left ventricular volume measurement, and although its ability to measure absolute volume linearly over a large volume range may be criticized, it excels at measuring real-time relative changes in volume.19 This is sufficient for most clinical studies using standard indices of systolic and diastolic function that require information on relative changes in volume or rates of change of volume with respect to time.
Fewer studies have been performed on conductance catheter RV volumetry. Our group has demonstrated that the conductance catheter provides an accurate estimate of human RV cast volume20 and a linear estimate of human RV volume over a physiological volume range.21 Although Stamato et al22 found that α values (not measured in this study) decreased with RV volume increase, this did not result in a significantly nonlinear RV conductance-volume relation. Dickstein et al23 demonstrated that the conductance catheter could accurately measure relative changes in RV volume and could be used to generate RV pressure-volume loops that responded appropriately to changes in inotropic state produced by esmolol and dobutamine.
It should be appreciated that the majority of contemporary studies using RV deployment of a conductance catheter result in the catheter lying along only one axis of the right ventricle, producing an inhomogeneous electrical field for the right ventricle as a whole. Stamato et al22 described a right internal jugular vein/right ventricle/pulmonary artery catheter course that allowed evaluation of the inlet and outlet of the right ventricle in piglets. However, the pulmonary artery long axis in humans forms a much smaller angle with the sagittal plane than in pigs, because the human interventricular septum lies more vertically. In human subjects, this catheter course is likely to result in a sharper bend at the RV apex and greater potential for volume signal distortion due to variable overlap between electrical fields of segments of the inlet and outlet as the right ventricle contracts. In our study, the infundibulum was not fully interrogated, and so our absolute RV volumes will tend to be systematically underestimated. However, this error should be diminished by our use of pulmonary regurgitant fraction, in which pulmonary regurgitant volume is divided by RV stroke volume. By the same principle of indexing pulmonary regurgitant volume (x) to stroke volume (y), it was not necessary to measure α, because pulmonary regurgitant volume (x/α) was divided by stroke volume (y/α).
PR by MR Phase Velocity Mapping and by Conductance Method
The application of MR phase velocity mapping to measurement of PR was first described by Rebergen et al.8 Phase velocity–derived PR was validated by comparison to PR measured by MR tomographic RV volume measurement, with excellent agreement. Although this was not a primary concern of this study, we were able to compare the values of PR obtained by MR and conductance methods. In this study, MR estimation of PR was averaged over 128 cardiac cycles without respiratory gating and with the patients breathing spontaneously, whereas the conductance-based PR estimates were performed with the patients intubated and under general anesthesia, with all measurements made during suspended ventilation at end expiration. Furthermore, the conductance method measures only the fraction of PR that occurs in the period analogous to isovolumic relaxation before tricuspid valve opening, which in most cases will be less than the total amount of PR. However, the pulmonary regurgitant fraction determined by this technique has previously been shown to correlate with RV end-diastolic volume and stroke volume.7 Given this difference and the disparity in ambient conditions between the two PR measurements, there was good agreement between them, with a correlation coefficient of .76 and mean of the differences of 2.0±18.2% (95% limits of agreement). It is important to appreciate that our main intention in measuring PR by MR and conductance was to ensure that our PR estimates by the relatively novel technique of RV pressure-volume loops generated by conductance and microtip pressure catheters were at least of the same order of magnitude as an established technique and also to ensure that for future studies, noninvasive MR estimates of PR would correspond approximately to estimates in the catheterization laboratory. The outlier with severe tricuspid regurgitation demonstrates important limitations of both techniques. The MR technique will underestimate pulmonary regurgitant fraction if only the flow across the RVOT/pulmonary artery is measured, because this will result in an underestimate of RV stroke volume. This can be overcome by direct comparison of right and left ventricular stroke volumes measured from multislice reconstruction,8 but this increases MR acquisition time, which was already at the limits of tolerance of our subjects.
Despite these qualifications, in our experience and that of Rebergen et al,8 MR phase velocity mapping in the RVOT seems an excellent noninvasive method for serially quantifying PR in the long-term follow-up of patients after repair of tetralogy of Fallot and can be reasonably assumed to reflect the consequences of the changes on loading conditions explored in our acute study.
Effect of Increased Airway Pressure on PR
The first loading maneuver was an increase in airway pressure to 20 cm H2O (n=7) that was held constant at this level for the duration of the recording by adjustment of the ventilator settings to 20 cm H2O continuous positive airway pressure. This is a complex maneuver that increases RV afterload and decreases RV preload. The overall effect was a significant increase in PR but no significant change in stroke volume. The net forward flow (and hence cardiac output) is thus reduced. Animal experiments24 and human studies25 have demonstrated a decrease in RV end-diastolic volume during a Valsalva maneuver. In our patients, there was no decrease in RV end-diastolic volume, presumably because of the increased PR, which offset the reduction in venous preload.
Interestingly, although there was a tendency for PR to increase during the inspiratory phase of intermittent positive-pressure ventilation in our patients, the difference was not significant. It should be remembered, however, that these patients were not in the acute postoperative period and had no additional respiratory problems. An increase in mean airway pressure to 20 cm H2O is within the range of ventilatory pressures used in children undergoing positive-pressure ventilation in the acute postoperative period. Indeed, we have shown that the duration of PR is prolonged during the inspiratory phase of intermittent positive-pressure ventilation in these patients,26 and in a recent report, Shekerdemian et al27 demonstrated that negative-pressure ventilation (reducing mean airway pressure to a negative value) improves cardiac output, a decrease in PR potentially being one component of its effect.28
Effect of Simulated Branch Pulmonary Artery Stenosis on PR
Transient occlusion of one of the branch pulmonary arteries (n=7) produced significant obstruction to RV ejection and resulted in an increase in RV end-systolic pressure (P<.05) and PR (P<.05). The clinical relevance of this observation is best demonstrated by patient 13, who had PR measured before (38%) and after (24%) left pulmonary artery balloon dilatation and stenting. Confirmation of the stability of PR measurement was demonstrated by inflating a balloon within the stent, when PR again increased to 42% and the RV pressure increased to its baseline level (Fig 4⇑). Furthermore, in patient 7, who had a competent pulmonary valve, there was no increase in pulmonary regurgitant fraction. It could be argued that balloon inflation in a branch pulmonary artery may deform RV shape and affect conductance volume measurement; however, it is reassuring that in one study, even when major conformational change was induced by manual squeezing of excised hearts kept at fixed volume, there was no change in observed volume measured with a conductance catheter.29
To the best of our knowledge, this is the first direct demonstration that branch pulmonary artery stenosis increases PR. The corollary from this is that if there is an incompetent pulmonary valve or no pulmonary valve (transannular patch), distal pulmonary stenosis will accelerate PR and result in combined pressure and volume overload on the right ventricle. Our work supports the observations of several other groups28 30 31 that distal pulmonary stenoses and PR are often found together and the combination can have a devastating effect on RV function. Ilbawi et al28 catheterized 74 patients with PR after repair of tetralogy of Fallot and divided them into two groups according to the presence (48 of 74) or absence (26 of 74) of RV dysfunction. RV dysfunction was found to be associated with significant distal pulmonary stenosis, moderate PR, and a large transannular patch. Warner et al31 reported on 16 patients who required homograft pulmonary valve replacement for symptomatic RV failure with RV dilatation. Six of sixteen patients had significant pulmonary artery stenoses that required balloon dilatation either before or after surgery, and the patients (4 of 16) who developed conduit regurgitation after valve replacement as a group had significantly smaller pulmonary artery diameters and cross-sectional areas than the nonregurgitant group.
The clinical implications of our data are clear. All reasonable attempts should be made to preserve pulmonary valve function at the time of surgery. The higher incidence of transannular patches in those series in which repair is performed in early infancy32 33 34 35 must be borne in mind, particularly in the absence of a demonstrable benefit. Sousa Uva et al34 adopted a strategy of less aggressive relief of stenosis in infants undergoing complete repair of tetralogy of Fallot at <6 months of age and were able to reduce their transannular patch rate to 50%. However, they also had a subgroup of infants who received a modified Blalock-Taussig shunt and underwent delayed repair because of low weight, anomalous coronary artery, or small pulmonary arteries. These patients had the lowest rate of transannular patches (13%) despite having some of the most unfavorable anatomy, again demonstrating a potential benefit of delayed correction. Many patients, no matter what age, will require a transannular patch or will be left with the anatomic substrate for severe PR. However, these patients should be observed for the presence of distal stenoses, which should be treated aggressively with balloon dilatation and stenting when present. The question of which patients should undergo pulmonary valve replacement, and when, cannot be meaningfully answered in the absence of a prospective randomized trial. Clearly, if patients are operated on only when there is established RV dysfunction and dilatation with symptoms, recovery of RV function cannot be guaranteed.
The conductance catheter combined with a pressure microtip catheter allows real-time measurement of pressure-volume loops and quantification of PR. Increased airway pressure and simulated branch pulmonary artery stenosis increase PR. Despite the very different conditions under which PR was measured by the conductance catheter and MR phase velocity mapping, there was reasonable agreement between the two techniques. However, the conductance technique is essentially a research tool, whereas MR phase velocity mapping is noninvasive and can be used serially to quantify PR after repair of tetralogy of Fallot. We believe that the two techniques are complementary. Indeed, it is only by combination of serial quantification of PR with detailed analysis of its hemodynamic determinants and consequences that clinical algorithms for the initial surgical strategy and late management of the RVOT in tetralogy of Fallot can be optimized.
Selected Abbreviations and Acronyms
|RVOT||=||right ventricular outflow tract|
This study was supported by the Scott Rhodes Fund and the British Heart Foundation (Dr Kilner). The authors thank Dr Jane Somerville for referring some of the patients in this study for PR measurement.
- Received July 8, 1996.
- Revision received September 23, 1996.
- Accepted September 30, 1996.
- Copyright © 1997 by American Heart Association
Carvalho JS, Shinebourne EA, Busst C, Rigby ML, Redington AN. Exercise capacity after complete repair of tetralogy of Fallot: deleterious effects of residual pulmonary regurgitation. Br Heart J. 1992;67:470-473.
Gatzoulis MA, Till JA, Sommerville J, Redington AN. Mechanoelectric interaction in tetralogy of Fallot: QRS prolongation relates to right ventricular size and predicts malignant ventricular arrhythmias and sudden death. Circulation. 1995;92:231-237.
Redington AN, Oldershaw PJ, Shinebourne EA, Rigby ML. A new technique for the assessment of pulmonary regurgitation and its application to the assessment of right ventricular function before and after repair of tetralogy of Fallot. Br Heart J. 1988;60:57-65.
Rebergen SA, Chin JGJ, Ottenkamp J, van der Wall EE, de Roos A. Pulmonary regurgitation in the late postoperative follow-up of tetralogy of Fallot: volumetric quantitation by nuclear magnetic resonance velocity mapping. Circulation. 1993;88(pt 1):2257-2266.
Baan J, van der Velde ET, de Bruin HG, Smeenk GJ, Koops J, van Dijk AD, Temmerman D, Senden J, Buis B. Continuous measurement of left ventricular volume in animals and humans by conductance catheter. Circulation. 1984;70:812-823.
Altman DG. Practical Statistics for Medical Research. London, UK: Chapman & Hall; 1991:398-403.
Kirklin JW, Barratt-Boyes BG. Cardiac Surgery. 2nd ed. New York, NY: Churchill Livingstone; 1993:919-920.
Kass DA. Measuring right ventricular volumes. Am J Physiol. 1988;254:H619-H621.
Schwiep F, Cassidy SS, Ramanathan M, Johnson RL. Rapid in vivo determination of instantaneous right ventricular pressure and volume in dogs. Am J Physiol. 1988;254:H622-H630.
Burkhoff D. The conductance method of left ventricular volume estimation: methodologic limitations put into perspective. Circulation. 1990;81:703-706.
White PA, Bishop AJ, Conroy B, Oldershaw PJ, Redington AN. The determination of volume of right ventricular casts using a conductance catheter. Eur Heart J. 1995;16:1425-1429.
Bishop A, White P, Oldershaw P, Chaturvedi R, Redington A. The use of conductance catheters to assess human right ventricular volumes: in vitro and in vivo validation. Eur Heart J. 1995;16(abstract supplement):310-P1754.
Stamato TM, Szwarc RS, Benson LN. Measurement of right ventricular volume by conductance catheter in closed-chest pigs. Am J Physiol. 1995;38:H869-H876.
Santamore WP, Heckman JL, Bove AA. Right and left ventricular pressure-volume response to respiratory maneuvers. J Appl Physiol. 1984;57:1520-1527.
Mc Kay RG, Spears JR, Aroesty JM, Baim DS, Royal HD, Heller GV, Lincoln W, Salo RW, Braunwald E, Grossman W. Instantaneous measurement of left and right ventricular stroke volume and pressure-volume relationships with an impedance catheter. Circulation. 1984;69:703-710.
Cullen S, Shore D, Redington AN. Characterization of right ventricular diastolic performance after complete repair of tetralogy of Fallot: restrictive physiology predicts slow postoperative recovery. Circulation. 1995;91:1782-1789.
Shekerdemian LS, Shore DF, Lincoln C, Bush A, Redington AN. Negative pressure ventilation improves cardiac output after right heart surgery. Circulation. 1996;94(suppl II):II-49-II-55.
Warner KG, Anderson JE, Fulton DR, Payne DD, Geggel RL, Marx GR. Restoration of the pulmonary valve reduces right ventricular volume overload after previous repair of tetralogy of Fallot. Circulation. 1993;88(pt 2):189-197.