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Eur J Cardiothorac Surg 2001;19:785-792
© 2001 Elsevier Science NL

Effect of fenestration on the sub-diaphragmatic venous hemodynamics in the total-cavopulmonary connection

Great Ormond Street Hospital for Children, NHS Trust, Great Ormond Street, London WC1N 3JH, UK

Received 9 October 2000; received in revised form 19 February 2001; accepted 23 March 2001.

Corresponding author. Tel.: +44-20-7404-4383; fax: +44-20-7831-4931
e-mail: hsia{at}welchlink.welch.jhu.edu

	Abstract

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

 
Objective: To understand differences in the sub-diaphragmatic venous physiology between patients with fenestrated and non-fenestrated total-cavopulmonary connections (TCPC). Methods: We studied the effects of respiration, retrograde flow, and gravity on the sub-diaphragmatic venous flows in 20 normal healthy volunteers (control), 25 Fontan patients with non-fenestrated TCPC, and 21 with fenestrated TCPC. Subhepatic inferior vena cava (IVC), hepatic vein (HV), and portal vein (PV) flow rates were measured with Doppler ultrasonography during inspiration and expiration in both supine and upright positions. The supine inspiratory-to-expiratory flow rate ratio was calculated to reflect the effect of respiration, the supine-to-upright flow rate ratio was calculated to assess the effect of gravity, and the magnitude of retrograde flow was evaluated with respect to total antegrade flow. Mean IVC, HV, and wedged hepatic venous (WHV) pressures were measured during cardiac catheterization in four TCPC patients before and after fenestration closure. The transhepatic venous pressure gradient (TVPG) was calculated as the difference between the HV and WHV pressure. Results: Compared with control, HV flow in TCPC was heavily dependent on respiration; this inspiratory capacity was greater in fenestrated than non-fenestrated subjects (inspiratory-to-expiratory flow ratio 1.7, 4.4, and 3.0, respectively P<0.001). Normal retrograde HV flow was diminished in TCPC patients, furthermore, fenestrated subjects had less flow reversal than non-fenestrated (retrograde as percent of antegrade flow 43, 19, and 30%, respectively P<0.001). Gravity decreased IVC and HV flows more in TCPC subjects than control, but this effect was not different between the two TCPC groups. Closure of the fenestration resulted in higher IVC and HV pressures (pre-closure versus post-closure pressures [mmHg]: 11.2±4.0 vs. 12.3±3.9, and 11.5±3.8 vs. 12.4±3.8, respectively P0.001). The normal TVPG was reduced in fenestrated TCPC, and worsened after fenestration closure (0.9±0.3 and 0.7±0.4, respectively P<0.04). Conclusions: Fenestration of the inferior venous connection has important influences on sub-diaphragmatic venous return in TCPC patients. Although fenestration lowers venous pressures and partially restores TVPG, its beneficial effects on flow in TCPC patients are mediated primarily by an increase in inspiration-derived forward HV flow and reduced flow reversal. These observations suggest fenestration results in a more efficient and less congested splanchnic circulation in TCPC patients, and may have important implications in the early and late management of Fontan patients.

Key Words: Fontan procedure • Fenestration • Hemodynamics • Physiology • Veins • Portal vein

	1. Introduction

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

 
Modifications of the Fontan procedure have resulted in marked improvements in both survival and early functional outcome in patients undergoing single ventricle palliation [1]. More recently, surgical creation of a right-to-left shunt in the total cavopulmonary connection (TCPC) via a fenestration of the inferior venous pathway has been shown to reduce mortality rates, especially in high risk patients [2,3]. It has been suggested that by reducing the venous pressure and maintaining cardiac output and oxygen delivery, even at the expense of some systemic arterial hypoxemia, fenestration has additionally been reported to decrease early postoperative pleural effusion, shorten hospital stay, and improve or eliminate protein losing enteropathy in long term survivors [4]. Little is known however, about the primary or secondary effect a fenestration may have on venous pressure and flow dynamics, abnormalities of which, at least in part, may be important in the pathogenesis of some or all of these problems.

In a Fontan circulation, there is an inevitable rise in systemic venous pressure [1]. Furthermore, the sub-diaphragmatic venous circulation is affected by gravity interactions with the diaphragm, and the interposition of the liver between the portal and hepatic veins We have previously demonstrated unique but variable flow and pressure characteristics in the hepatic vein (HV), portal vein (PV), and subhepatic inferior vena cava (IVC) in healthy and failing Fontan patients, [5–7] but the mechanisms through which a fenestration placed within the venous circuit may influence its pressure flow haemodynamics has not been explored. The purpose of this study was to compare the pressure-flow characteristics of the subdiaphragmatic venous return in fenstrated and non-fenestrated TCPC patients, in order to understand the potential benefits of a fenestration within the Fontan circulation.

	2. Methods

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

 
2.1. Study groups
2.1.1. Flow dynamics
Forty-six patients were studied two to thirteen years (mean 7.6±3.4 years) after TCPC. Twenty-one (46%) patients had a patent fenestration of the inferior venous connection on transthoracic echocardiogram. All patients were in self-reported New York Heart Association (NYHA) functional class 1 or 2; none had clinical signs of congestive heart failure, arrhythmia, major pulmonary arteriovenous malformations, protein losing enteropathy or other known complications of the Fontan circulation. Twenty age- and sex- matched normal volunteers were studied as control subjects.

All subjects underwent HV, PV, and IVC Doppler ultrasonographic interrogation under simultaneous dynamic respiratory and electrocardiographic monitoring. A tilt table was used to allow measurements in the supine and upright (85–90° from horizontal plane) positions.

2.1.2. Fenestration closure
Four patients, 3–7 years after their fenestrated TCPC procedure, underwent device closure of the fenestration for relief of symptomatic cyanosis and decreased exercise tolerance. One patient had an extracardiac conduit, the rest lateral tunnel TCPC. None of the patients had protein losing enteropathy or hepatic cirrhosis. In all patients, the IVC, HV, and wedged HV pressures were measured in supine position and during respiratory apnea to minimize effects of positive pressure ventilation.

Room air oxygen saturation was obtained from all Fontan patients with a pulse oximeter (Ohmeda, USA). The study protocols were approved by the hospital Research Ethics Committee and informed consents were obtained for all subjects.

2.2. Doppler ultrasonongraphic recordings
Measurements were made with an Acuson 128XP system, using a 2.5 MHz transducer. Pulsed-wave Doppler recordings in the HV, IVC, and PV were made with each subject breathing quietly in supine and then upright position. At least 5 min were allowed prior to the upright examination for the subject to adjust to the postural change. A minimum of three full respiratory cycles was recorded for each patient in both supine and upright positions.

For each vessel, the site of sampling was guided by colour flow mapping to position the sample volume at the centre of the colour signal and to create the smallest angle of insonation between the direction of blood flow and Doppler beam.

Recordings were made in the left or middle HV (approximately 1 cm distal to junction with IVC) and the subhepatic IVC (1–2 cm distal to junction with HV). The portal flow signal was obtained in the main portal trunk prior to its division into the right and left branches following previously published protocols [8]. The instantaneous diameters of each vessel (d) in both the supine and upright positions were measured from the B-mode images at the same location as the Doppler interrogation; signals in the upright position were obtained as close to the identical location in the supine position as possible. Each Doppler flow signal was recorded on videotape and hard copy for off-line analysis.

2.2.1. Flow rate calculations
Mean flow rate (Q) was computed by the division of volume of blood (V) moving through the vessel by the time interval (T=T₂-T₁) needed for this volume to cross.

((1))

A rigorous treatment of the volume flow relationship required the continuous computation of the product of mean instantaneous velocity (v (t)) and cross sectional area (A (t)), or an integration,

((2))

over T. We assumed that changes in A(t) within one respiratory cycle were small in the moderately sized HV, IVC, and PV, all of which were trans-hepatic in location. Eq. 1 could then be replaced as,

((3))

where A equalled to (d/2)², d the cross-sectional diameter of the vein, and v(t)dt the velocity-time integral (VTI) determined from the Doppler recording taken over time interval T.

2.3. Respiratory effect
As demonstrated in Fig. 1, with dynamic respiratory monitoring, the Doppler signal could be evaluated during inspiration, during expiration, or throughout a complete respiratory cycle.

View larger version (127K): [in this window] [in a new window]   Fig. 1. A pulsed wave Doppler ultrasound flow recording from the subhepatic inferior vena cava (IVC) of a normal subject. Electrocardiogram is the upper line. The low frequency tracing shows spontaneous respiration, with upward (up arrows) and downward (down arrow) deflections indicating the onset of inspiration and expiration, respectively. Flow below the zero reference line is antegrade towards the heart; above zero flow is retrograde. Note reversal of flow with atrial contractions (oblique arrows)

2.4. Retrograde flow rate
Qre was obtained through an evaluation of the VTI of the retrograde Doppler signal throughout a respiratory cycle. Antegrade flow rate (Qan) corresponding to the same time interval was also calculated. The ratio of Qre/Qan represents the magnitude of retrograde flow with respect to antegrade flow.

2.5. Gravity effect
The effect of gravity on net flow rate was evaluated. Net flow rate (Qnet) was defined as the absolute total flow during a complete respiratory cycle obtained by subtracting retrograde VTI from the antegrade VTI. The effect of gravity on Qnet was represented as the ratio of Qnet in the upright position over that in the supine position. A ratio of less than one implies a reduced Qnet in the upright position.

2.6. Sub-diaphragmatic catheterization
During cardiac catheterization under general anaesthesia, pressures in the sub-diaphragmatic veins were measured. These were recorded through a saline filled, balloon-tipped (Swan-Ganz) catheter (Kimal, Uxbridge, UK) connected to a pressure transducer that was zeroed against atmospheric pressure and level with the mid chest. Measurements were made in the IVC, in one of the HV's, and in ‘wedged’ position within the HV by inflating the balloon. The wedged HV pressure correlates closely with directly measured portal venous pressure [9]. Mean pressure values were obtained during respiratory apnea. Difference between the mean wedged HV and free HV pressures was the trans-hepatic venous pressure gradient (TVPG) which normally ranges between 1 and 4 mmHg [9].

2.7. Statistical analysis
All data were expressed as mean±standard deviation. For both flow data, differences among various groups were assessed by one-way analysis of variance (ANOVA) with Neuman–Keuls multiple comparison test to evaluate all inter-group significance. For pressure data, mean pre- and post-fenestration closure values were compared using the paired-t test. Probability (P) values of <0.05 were considered statistically significant.

	3. Results

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

 
3.1. Study groups characteristics
Characteristics of TCPC patients in the flow dynamics study, including diagnosis at time of surgery and room air oxygen saturation, are listed in Table 1. There were no differences in the underlying diagnosis, type of TCPC, or age at surgery between non-fenestrated and fenestrated TCPC groups. However, the fenestrated TCPC patients were younger (P<0.0001), had a shorter follow-up (P<0.01) and lower oxygen saturation (P<0.02). The control group had a mean age of 14±5 years and a male-to-female ratio of 15:5 (P=NS compared to both patient groups).

3.2. Flow rate calculations
The results of the various Doppler flow rate calculations are summarized in Table 2. There were no differences between the lateral tunnel and extracardiac TCPC subgroups, so their data are presented together.

3.2.2. HV Flow
Control subjects again showed an inspiratory augmentation to flow in the HV, but forward flow in both TCPC groups was markedly higher during the inspiratory phase of the respiratory cycle (Fig. 2). This effect was significantly more pronounced in the fenestrated TCPC patients, whose retrograde flow was also less than non-fenestrated TCPC patients. While gravity retarded forward flow more in both TCPC groups than in control, there was no difference in this effect between them.

View larger version (108K): [in this window] [in a new window]   Fig. 2. Pulsed Doppler ultrasound recording with simultaneous respiratory monitoring from the hepatic vein in a control subject, a non-fenestrated TCPC patient, and a fenestrated TCPC patient. Note in both TCPC patients, predominant forward flow occurs during inspiration, and this is enhanced in the fenestrated patient.

3.3. Pressure measurements
Results of the pressure measurements and room air oxygen saturations before and after fenestration closure are listed in Table 3. Closure of the fenestration resulted in significant increases in oxygen saturation, as well as central and HV pressures, but lowered the TVPG (Fig. 3).

View larger version (50K): [in this window] [in a new window]   Fig. 3. Analogue recordings of the wedged (WHV) and free hepatic venous (HV) pressures in a TCPC patient with the fenestration open (upper panel) and closed (lower panel). Note the complete loss of the transhepatic venous pressure gradient and equalization of HV and PV pressures after fenestration closure.

	4. Discussion

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

Despite this, no study has examined the influence of the fenestration on the physiology of inferior venous return. This circulatory region is composed of two dynamically distinct circulations: the splanchnic – draining the gastrointestinal tract through added resistance of the liver, and the systemic – channelling blood from the lower extremities and kidneys. In our previous studies, [5–7] we described markedly abnormal respiratory and hydrostatic influences on IVC, HV, and PV flow in well and failing Fontan patients. The data in this study demonstrates further differences in flow and pressure dynamics in fenestrated and non-fenestrated TCPC circulations.

4.1. Methodology
Instead of using maximal velocities or pulsatility ratios as indicators for flow dynamics in the sub-diaphragmatic venous circulation [13,14], we calculated volumetric flow rate from Doppler recordings as a measure of flow. Since the flow profiles in these veins are not symmetrically parabolic, instantaneous maximal velocities cannot account for the continuous changes of flow throughout a cardiac or respiratory cycle. Similarly, an assessment of pulsatility does not provide information regarding the dynamics of pressure or flow. In this study, volumetric flow rate was calculated by evaluating velocities continuously with respect to time and assuming a constant cross sectional area in all three veins throughout a respiratory cycle. Both the main HV and the IVC just distal to it are trans-hepatic in location and have been shown to remain in rigid configuration during all phases of respiration [15]. Furthermore, M-mode images of the portal vein diameter averaged over several cardiac cycles have produced agreement of ±0.5 mm with the instantaneous diameter measured from B-mode imaging [16]. Separate vein dimension measurements were obtained in supine and in upright positions since there is no evidence for invariability with orthostasis.

4.2. Effects on flow
Our study demonstrates that fenestration does not appear to exert significant influence on the flow dynamics of the systemic inferior (subhepatic IVC) or portal venous return. However, antegrade HV flow in fenestrated TCPC patients is increased during inspiration concomitant with less regurgitation. We have previously demonstrated that the majority of HV flow, which makes up nearly 40% of the total inferior venous return, occurs during inspiration in TCPC circulation; this is the so called cardiopulmonary interaction in Fontan patients [17]. By reducing the venous pressure, and consequently the resistance to venous return [4], fenestration amplifies the cardiopulmonary interaction in the splanchnic circulation with minimal caval contribution. Enhanced hepatic outflow may therefore contribute to the observed improvements in venous return and cardiac output in fenestrated Fontan circulations.

The effect of gravity in the upright position, has been shown by us to exert significant negative impact on the sub-diaphragmatic venous circulation even in the functionally well Fontan circulation [6]. This effect persists in those with a fenestration, suggesting that these gravitational influences are likely to be intrinsic to the Fontan physiology and are not amenable to venous pressure reduction or perfusion augmentation.

4.3. Acute effects of fenestration closure
Closure of the interatrial communication after fenestrated Fontan operation has been shown to result in elevation of the systemic venous pressures and arterial oxygen saturation [18]. This is confirmed in our patients who underwent fenestration closure. Interestingly the portal venous pressure remained unchanged, resulting in a reduction of the TVPG after fenestration closure. Normally, the highly compliant capacitance at the hepatic sinusoidal level maintains a pressure gradient between portal and hepatic veins (TVPG) ranging from 1 to 4 mmHg [9,19,20]. Our patients had a somewhat lowered TVPG prior to fenestration closure. Since a well-maintained transhepatic pressure gradient buffers the portal pressure from changes in caval pressure and volume [20], further loss of the TVPG in non-fenestrated Fontan circulation suggests that this important autoregulatory mechanism may be absent or diminished. In dogs, serial elevations of the IVC pressure resulted in a progressive rise in portal pressure, a fall in hepatic blood flow, and elimination of the TVPG [21]. Furthermore, in patients with congestive heart failure and high right atrial pressures, TVPG is also reduced [22]. A nearly equalized hepatic inflow and outflow pressure increases hepatic blood transit time, which together with enlarged hepatic blood volume due to higher central venous pressure, results in added congestion of the entire splanchnic macro- and micro-circulation [22].

In addition to hepatic congestion, elevation of hepatic venous pressure and impedance of hepatic outflow disturb the balance of Starling forces governing passage of fluid across capillary walls and increases the trans-sinusoidal filtration of protein-rich hepatic fluids into the interstitium [23], and into the gastrointestinal tract [23,24]. While the sequential aetiology of protein losing enteropathy in late Fontan attrition remains unknown, several authors have reported the relief of this debilitating complication by fenestrating the inferior venous connections [4,12]. Our study demonstrates the greatest influence of the fenestration on the inferior venous return in Fontan patients appears to be focused on the splanchnic circulation. By improving splanchnic outflow (HV), and preserving the transhepatic pressure gradient, fenestration results in a more efficient splanchnic circulatory hemodynamics, which may be responsible for the resolution of this yet undefined pathophysiological process.

4.4. Limitations
The fenestrated TCPC patients were younger and have shorter follow-up than non-fenestrated patients. This reflects the more recent adaptation of the fenestrated technique in our surgical practice. Therefore, it is possible that some of the differences reported here are the result of a shorter duration in Fontan-type circulation. However, subjective intragroup analysis did not reveal any variation relating to age or length of follow-up.

For the flow study, we do not know whether differences in such hemodynamic parameters as central venous pressure, pulmonary vascular resistance, or cardiac index existed between the fenestrated and non-fenestrated groups. However, all patients were in good functional state without any late known complications of the Fontan operation. Since the aim of the study was to define the flow dynamics with and without a fenestration, we felt that as long as the functionality is uniform between the two groups, characterization of physiological differences remains valid.

Use of Doppler to evaluate flow rate is known to be prone to error whenever the angle of insonation between the ultrasound beam and blood flow axis is not zero [25]. This error is a cosine function; therefore, a non-zero angle will always underestimate the actual flow rate. In our subjects, despite efforts to align the beam with the vessels, all had non-zero angles of incidence and angle correction protocols were employed. Instead of comparing absolute values of flow rates, we calculated ratios of flow rates to evaluate the various effects using each subject as his/her own control. In this manner, the cosine terms cancel each other and the error is neutralized.

	5. Conclusion

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

 
Fenestration of the inferior venous connection has important influences on sub-diaphragmatic venous return in TCPC patients. Although fenestration lowers venous pressures and partially restores normal TVPG, its beneficial effects on flow in TCPC patients are mediated primarily by an increase in inspiration-derived forward HV flow and reduced flow reversal. These observations suggest fenestration results in a more efficient and less congested splanchnic circulation in TCPC patients, and may have important implications in the management of early and late Fontan attrition. Further studies are required to assess the differential long-term function of the liver and gastrointestinal tract between fenestrated and non-fenestrated patients, including those who underwent late fenestration closure.

	Acknowledgments

 
Dr Hsia is the recipient of the 1999 National Science Foundation International Post-doctoral Research Fellowship Award, Grant no. INT-9802808. We would also like to thank the consultants and staff of the Cardiothoracic Unit at Great Ormond Street Hospital for Children for their support and cooperation.

	Footnotes

 
Presented at the 14th Annual Meeting of the European Association for Cardio-thoracic Surgery, Frankfurt, Germany, October 7–11, 2000.

	Appendix A. Conference discussion

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

 
Dr F. Lacour-Gayet (LePlessis Robinson, France): I have two comments. The first comment regards the consequences of phrenic paralysis. Unfortunately we all have in our series of Fontan following staged repair phrenic paralysis. My first question is if this affects the results.

My second question regards the transhepatic gradient that is reduced following fenestration. I would like to ask you if you have some data to suggest that this transhepatic gradient could generate the production of the angiogenesis factor by the liver.

Dr Hsia: Concerning the first question about the consequences of protein-losing enteropathy, that is something, of course, that anyone who performs this type of surgery will encounter, whether it is early or late follow-up, and it has been a major problem. And actually that is the impetus for this type of research, to sort of understand the sequential pathophysiology of protein-losing enteropathy. In this first initial study that we had performed we basically tried to understand what are the fundamental differences between the Fontan circulation and the normal circulation, and that had been presented both at AHA and AATS. Here we have noticed in the literature recently that there were publications where PLE was reversed in patients after they had their path refenestrated, and which went on to say, well, what is the exact effect of the fenestration, then, on the inferior venous return, since a lot of people are fenestrating the TCPC patients these days. Based on this study, it's hard for me to draw any significant conclusion on the pathophysiology of PLE, but what I can say is that the fenestration certainly allows for efficient splanchnic circulation; that is, it allows for better outflow characteristics, and that in itself may improve or decrease the amount of congestion that all these patients get once they convert to a Fontan type of circulation.

Concerning the second question, the angiogenesis secondary to the transhepatic gradient, I don't have any active evidence of such a physiology. However, the decrease of the transhepatic gradient is something actually not very prevalent in the literature. In the gastroenterology literature most of the gradients are elevated secondary to cirrhosis. Actually this is one of the first papers where we demonstrated a drop of the transhepatic gradient in human pathophysiology. So I'm sorry, I do not have a clear answer for your second question.

	References

Top Abstract 1. Introduction 2. Methods 3. Results 4. Discussion 5. Conclusion Appendix A. Conference... References

 

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