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Ann Thorac Surg 2000;70:2096-2101
© 2000 The Society of Thoracic Surgeons

Original article: cardiovascular

Model of complete separation of the hepatic veins from the systemic venous system

Christian P.R. Brizard, MDa, Nathalie Goussef, BSa, Juan Carlos Chachques, MD, PhDa, Alain F. Carpentier, MD, PhDa

a Laboratoire d’étude des Greffes et Prothèses Cardiaques, Hôpital Broussais, Paris, France

Accepted for publication March 31, 2000.

Address reprints requests to Dr Brizard, Cardiac Surgery Unit, Royal Children’s Hospital, Parkville, Victoria, 3052, Australia
e-mail: cardiac{at}cryptic.rch.unimelb.edu.au


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. In patients undergoing a Fontan operation, partial diversion of the hepatic veins to the pulmonary venous atrium has been tried with various techniques. They failed because of the development of intrahepatic collaterals leading to an unacceptable right-to-left shunting. We postulate that to avoid the formation of intrahepatic collaterals, the totality of the liver has to be drained into the same pressure compartment. We have designed a model of cavopulmonary anastomosis in which a prosthetic conduit reproduces an azygos continuation, associated with the diversion of the totality of the hepatic venous return. This article reports on the early hemodynamics and the fate of the separation of the two venous compartments in long-term survivors.

Methods. Eighteen goats were operated on; the pulmonary artery and hepatic vein pressures were recorded. During month 2, an opacification of the inferior vena cava and the cavopulmonary connection was performed. Between months 6 and 14, another opacification was performed, together with pressure recording at both ends of the conduit.

Results. Postoperatively the pulmonary artery pressure was pulsatile with a mean of 10 mm Hg and the hepatic vein pressure was 0 mm Hg. The first angiogram showed patent tubes with fast progression of the contrast. Throughout the inferior vena cava injection, there was no opacification of the portal or hepatic veins. The late study showed a narrowed conduit in all animals. During the injection, a collateral was injected, feeding into the inferior mesenteric vein. No collateral circulation could be seen draining directly into the liver. The median gradient between the two ends of the conduit was 11 mm Hg.

Conclusions. The isolation of the entire hepatic venous drainage is feasible and efficient for the separation of two pressure compartments. No intrahepatic collaterals are observed with this model at short- or long-term follow-up. The separation of the hepatic venous drainage should persist without collateral circulation as long as the inferior vena cava pressure stays at the levels observed in Fontan circulation.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
The hepatic arterial buffer response [1] and hepatic venous sphincter are two autoregulatory mechanisms of the hepatic artery and portal vein flows. They also maintain the portal venous pressure at 10 mm Hg when the central venous pressure is below that level. On the other hand, the average normal left atrial pressure is 8 mm Hg [2]. The combination of these two statements characterizes the contradiction of the Fontan circulation. The addition of the pulmonary resistances and the requirement for an adequate preload of the ventricle produces a central venous pressure greater than 10 mm Hg in most patients undergoing the Fontan operation. Above 10 mm Hg the regulation mechanisms are overwhelmed and the central venous pressure is transmitted quantitatively to the hepatic sinusoids and the splanchnic circulation. This profoundly affects the function of the liver and the exchange of fluids. The hepatic venous hypertension is a direct consequence of the Fontan circulation and may be responsible for most of the morbidity of the Fontan physiology [3–5]. This morbidity is not observed in patients with a bidirectional cavopulmonary connection, or in patients with azygos continuation who undergo a Kawashima operation [6]. To a lesser degree, the same applies to a fenestrated Fontan patient, who typically has a lower central venous pressure than a nonfenestrated Fontan [7]. The right-to-left shunt at the atrial level provides an adequate ventricular preload and bypasses the pulmonary circuit, thereby, lowering the central venous pressure.

The partial diversion of the hepatic veins to the pulmonary venous atrium is an alternative to fenestration. It reduces selectively and more effectively the pressure in the concerned hepatic veins. This has been tried in humans in various technical formats [8–10]. In all of the latter procedures, only part of the hepatic venous drainage was deviated. This created two contiguous compartments at different pressure within the liver. The development of intrahepatic venous collateral circulation between these compartments led to an increased right-to-left shunting and cyanosis in most patients, that is, an increasing diversion of inferior vena cava (IVC) blood to the pulmonary venous atrium by way of the liver [8, 11, 12].

To avoid the formation of intrahepatic collaterals, all the liver parenchyma has to be drained into the same pressure compartment. The complexity of the anatomy of the hepatic veins suggests that the retrohepatic IVC as a whole has to be separated from the IVC to exclude the totality of the hepatic venous drainage.

We postulate that total rather than partial diversion of the hepatic venous return should prevent the formation in the long term of these intrahepatic collateral pathways.

We have designed in goats an experimental model where the totality of the hepatic venous drainage is separated from the systemic venous drainage. We used a bidirectional Glenn anastomosis plus a prosthetic conduit reproducing an azygos continuation to generate the gradient of pressure between the hepatic and systemic veins.

Our questions are: Does this model effectively create two venous pressure compartments, and, in the long term, does the separation of the hepatic venous drainage as it is done in our model prevent the development of intrahepatic collaterals?


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
This study conforms to the principles for research use of experimental animals of the American Physiologic Society.

Adult female alpine goats were sedated with 1 mg/kg of acepromazine (Vétranquil; Sanofi Winthrop, Gentilly, France) and anesthetized using 0.5 mg/kg of intravenous propofol (Diprivan; Zeneca Pharma, Cergy, France). Cuffed endotracheal tubes (8F) were inserted and the animals were ventilated with a 900 C Siemens ventilator (Siemens-Elema A.B., Solna, Sweden) with a volume controlled cycle. Anesthesia was maintained throughout the procedure with 1% to 2% isoflurane (Forène; Abbott-France, Rungis, France). A central line was inserted in the right external jugular vein. The electrocardiogram was continuously monitored. Intravenous cefazolin (500 mg) was given before incision and intramuscularly once daily for 3 days.

Procedure
With the animal prepared and draped, a right subcostal flank incision was made and the IVC dissected free and taped between the renal veins and the inferior margin of the liver (Fig 1). A breach was made in the posterior insertion of the diaphragm, allowing entry into the right pleural space close to the midline. The tape was placed in a tourniquet. An externally ringed expanded polytetrafluoroethylene (ePTFE) tube (FEP Ringed GORE-TEX Vascular Graft; W.L. Gore & Associates, Flagstaff, AZ), 16 mm in diameter and 30 cm long was anastomosed in a lateroterminal fashion just above the renal veins. Both tube and tourniquet were slid into the right pleural cavity. The tube was clamped laterally and the clamp was allowed to protrude through the wound. The wound was closed loosely using a rubber glove.



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  		Fig 1. Schematic representation of the procedure. The black area (plus the pulmonary arteries, hatched) is the cavopulmonary connection at high venous pressure.

 
The goats were then placed in a supine position and a median sternotomy was performed. An arterial line was inserted in the internal thoracic artery for blood sampling and monitoring. The superior vena cava (SVC) was dissected free. The SVC was anastomosed end-to-side to the main pulmonary artery with the use of a custom-made T-shaped 16-mm ePTFE conduit (GORE-TEX Stretch Vascular Graft; W.L. Gore & Associates), which was itself connected to the above mentioned ringed ePTFE tube. The two combined conduits were laid in a harmonious S-shaped fashion anterior to the heart. Under the cover of heparin (100 U/kg) and after deairing, the infrahepatic IVC was occluded with the tourniquet that was lying in the right thorax while the clamp protruding through the flank incision was released. From that moment, the equivalent of a bidirectional Glenn anastomosis with azygos continuation was functioning.

Pressures were recorded in the SVC (pulmonary artery pressure) and in the right atrium (hepatic vein pressure). The tourniquet was removed and the tape was tied. The incisions were closed; the animals were allowed to recover and were extubated. All lines and chest tubes were taken out except for the central venous line, and the animals were put back in their cages where they were looked after during the first night with regular checking of the mixed venous saturation. Heparin level was kept at 0.1 UI/mL. Survivors were taken to the animal ward where they were given low molecular weight heparin subcutaneously (Fraxiparine; Sanofi Winthrop, Gentilly, France) 0.8 mL daily for 15 days, then 0.3 mL daily for 2 months. The animals were then sent to a farm, with no medication, and joined a normal herd.

Before leaving our animal ward, between the seventh and the tenth postoperative week, a digital opacification of the IVC and the cavopulmonary connection was performed under sedation using 0.5 mg/kg of intravenous acepromazine, with spontaneous ventilation. Contrast was injected through both saphenous veins simultaneously. Two injections of 40 mL of Hexabrix were used.

The long-term survivors have had a second and, for some of them, a third digital opacification of the IVC and the cavopulmonary connection using the same protocol. These animals underwent a catheterization of the IVC through the saphenous vein and of the SVC through the external jugular vein. Simultaneous pressure of the SVC and the inferior IVC (ie, at both ends of the ePTFE shunt) were recorded under spontaneous ventilation. The animals were killed afterward.

All animals were killed using 100 mg/kg of intravenous pentobarbital. All animals that were killed or died during the follow-up period had a postmortem examination. At autopsy we looked for evidence of early thrombosis of the shunt, anastomotic stenosis, pulmonary embolism, and pleural or peritoneal effusion.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Eighteen animals (37 ± 6 kg) were operated on. Four animals died before the operation could be completed. Death was related to ventricular fibrillation or technical reasons.

Fourteen animals were able to be extubated within 1 hour of the procedure and lived more than 8 hours. Venous pressures for all the 14 animals were available, and results are shown in Figures 2 and 3.



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  		Fig 2. Intraoperative pressure recording at the end of the procedure, with the chest open and volume-controlled ventilation. (IVC = inferior vena cava; HV = hepatic vein; PA = pulmonary artery; SVC = superior vena cava.)

 


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  		Fig 3. Simultaneous pressure recording in inferior vena cava (top right) and superior vena cava (bottom right) on one side, and aorta (top left) and right atrium (bottom left) on the other side. Pressures are in millimeters of mercury.

 
Three animals were killed during the first 12 hours when their survival became obviously dependent on fluid replacement or inotropic support. Postmortem examination found hemorrhage (n = 2) or was inconclusive. Two goats died during the early follow-up before an opacification of the tube could be performed.

Early opacification
Nine animals survived to have a digitalized opacification of the IVC and the cavopulmonary connection between 2 and 3 months postoperatively.

The studies in these animals showed patent ePTFE tubes, with no anastomotic stenosis or wall thrombus. The progression of the contrast was fast and regular, reaching the pulmonary arteries within 5 seconds (±1.5). Opacification was even in both branches. Throughout the IVC injection, there was no opacification of the portal vein, the liver parenchyma, or the retrohepatic IVC (Figs 4 and 5).



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  		Fig 4. Early opacification (day 78). Lateral view of the thoracic part of the graft (black arrow, GRAFT), the superior vena cava (white asterisk), and the pulmonary artery trunk (white star). The white arrows point to the pulmonary cusps. (AV = azygous vein.)

 


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  		Fig 5. Early opacification (day 78). Lateral view of the abdominal part of the graft (white asterisk, GRAFT), showing the inferior vena cava stump (black arrow, inferior vena cava).

 
Three animals died at 3 and 5 months postoperatively, one from tuberculosis and the others from acute thrombosis of the conduit.

Late angiographic studies
Six animals have had late angiographic studies between the sixth and the fourteenth month postoperatively. In two animals, the opacification was identical to the early one and the two animals were kept alive to be recatheterized between the twelfth and the fourteenth month, respectively. The latest study of the IVC eventually showed in the six animals, a severely narrowed ePTFE conduit throughout its entire length with a persisting faint forward flow. Within the same time range, a major collateral system was disclosed, feeding into the inferior mesenteric vein. No collateral circulation could be seen draining directly into the liver (Fig 6). Little contrast could be seen in the left hemiazygos system. No collateral circulation existed with the SVC.



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  		Fig 6. Late opacification (day 251). Lateral view of the abdominal part of the graft. The injection shows the inferior vena cava below the ligation, the inferior vena cava stump, a faint injection of the conduit (white asterisk) and the opacification of the inferior mesenterical vein (white arrow).

 
The catheterization of the IVC inferior to the shunt and the SVC have demonstrated a median gradient of 11 mm Hg (8 to 15 mm Hg) between both ends of the conduit (n = 6). The pressure in the SVC was variable with ventilation, whereas the pressure in the IVC was not (Table 1).


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  		Table 1. Pressure Recording at Both Ends of the Expanded Polytetrafluoroethylene Conduit at the Time of Sacrifice in Six Long-Term Survivors

 
All postmortem examinations brought little information. Acute deaths in the early or late postoperative period were always related to the thrombosis of the conduit. In the early postoperative period, fresh clot occupied the entire lumen. In the late postoperative period, important wall thrombosis was seen, with red clot in the remaining lumen. Animals that were killed in the early postoperative period demonstrated no pleural effusion or ascites. In all animals, anatomic examination of the liver revealed normal gross and microscopic structure.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Anatomy
The anatomy of the hepatic venous drainage is complex. The superior right hepatic vein and a common trunk for the middle and left hepatic veins drain the major part of the hepatic venous return. Upstream, over the entire height of the liver, three other major veins drain consistently into the retrohepatic IVC. They are the middle and inferior right hepatic veins and the vein of the caudate lobe. In 10% to 15% of the specimens studied, the inferior right hepatic vein is large (5 mm or more) [13]. In addition, a multitude of small veins drain directly into the retrohepatic IVC [14]. The anatomy of the hepatic venous drainage in goats is identical to that of humans based on our own preliminary anatomic study.

Absence of intrahepatic collateral pathways
The characteristics of the liver parenchyma allow for the rapid development of intrahepatic collateral circulation. Such collateral circulation has been described in partial Budd Chiari syndrome [15]. Similarly, it can be found in obstruction of the retrohepatic IVC, where the blood from the IVC flows through the inferior right hepatic vein and the vein of the lobe caudate, through the liver into the two main hepatic veins and the right atrium [16–18].

Intraoperative pressure measurements in the SVC (pulmonary artery pressure) and in the right atrium (hepatic veins pressure) have demonstrated, in all animals available, the separation of the two venous compartments. The pressure gradient between the two compartments is 8 to 10 mm Hg. The separation was confirmed with the angiographic studies at 8 weeks, showing no opacification of the hepatic veins, the portal vein, or the liver parenchyma. Up to 2 months postoperatively, in all animals studied, no collateral circulation had developed either directly to the liver or between the infrahepatic IVC and the portal vein. Up to 2 months postoperatively, the hepatic veins remained separated from the systemic venous pressure, and the portal vein received no systemic venous blood. In the long-term angiographic studies no opacification of the liver parenchyma or the hepatic veins could be seen coming directly from the IVC. However, all animals eventually demonstrated collaterals from the IVC to portal vein tributaries.

Collaterals from the inferior vena cava to the portal vein
Collaterals from the IVC to the portal vein were never seen on early angiographic studies. On the other hand, on long-term angiographic studies, all the animals have eventually demonstrated a collateral circulation between the infrahepatic IVC and the portal vein through the inferior mesenteric vein. The origin and termination of the collateral circulation was identical in all animals. There was never any collateral circulation going to the SVC. The left hemiazygos drained normally into the coronary sinus but was not increased significantly in size.

Why did all the long-term survivors have a similar collateral circulation? Is the collateral circulation unavoidable in any situation where the liver is at a lower pressure than the central venous pressure, or is it dependent on the magnitude of the difference of pressure?

By definition, a portal system has a capillary network at each of two extremities. The venous pressure in a portal system is the driving force across the distal capillaries. Therefore, the physiology of a portal system implies that it is resistant to the formation of collaterals that would offload the pressure necessary to its function.

In humans, there are four anatomic types of portacaval collateral circulations [19]. They become functional when the pressure in the portal vein exceeds a certain level [20]. Flow through these collaterals, decompressing the portal vein (portal vein to systemic veins) is commonly seen in portal hypertension. The same anatomic collateral pathways, flowing the other way (IVC to portal vein) are demonstrated decompressing the IVC when it is occluded [16, 17].

By definition, throughout the follow-up, the portal pressure is 8 to 10 mm Hg. The IVC pressure is 10 to 12 mm Hg in the early postoperative pressure recording (gradient with portal vein, 2 mm Hg). Everything acts as if the pressure difference observed in the early follow-up was within physiologic limits. No collaterals toward the portal vein tributaries were generated. Conversely, in the long term, the progressive occlusion of the conduit is driving the IVC pressure to more than 22 mm Hg at the time of sacrifice (gradient with portal vein, 12 mm Hg; Table 1.

In the normal physiology, a 6 to 8 mm Hg difference of pressure exists between the systemic and the portal veins, but they remain separated. When the gradient of pressure is reversed (between IVC and portal vein) but of the same amplitude, there should not be any opening of the collateral circulation.

Our findings, together with the physiology of the portal circulation, suggest that when the absolute value of the gradient between the IVC and the portal vein is less than 10 mm Hg, no collateral circulation should open up between these systems.

Limitations
Our model caries its own limitations. Technically the length of the conduit favors the wall thrombosis; therefore, the demonstration of the separation of the two pressure compartments is not as clear in the long term.

The focus of this report is on the anatomic isolation of the totality of the hepatic venous drainage and the ability to preserve a pressure gradient in the long term. To generate the gradient, we have used a modification of a Fontan circulation close to a total cavopulmonary shunt (Kawashima procedure [6]). Several important issues are implicitly included in this model.

Because of the nature of our model, with a mixture of cavopulmonary physiology and antegrade pulsatile flow, the hemodynamics are complex and cannot be developed in the present report. However, the ultimate aim of a Fontan circulation with exclusion of the hepatic venous return is the improvement of the quality of the palliation provided.

Our model does not include a bypass of the pulmonary circulation for the hepatic venous blood. It is not meant to study the formation of pulmonary arteriovenous fistulas. We have used a modification of our present experimental model to evaluate the long-term effect on the lungs of the derivation of the hepatic venous return to the left atrium. The results are currently being analyzed.

Conclusion
Our study demonstrates that the complete isolation of the retrohepatic IVC provides a total separation of the hepatic venous return. The separation of the hepatic venous return as it is done in our model prevents the formation of intrahepatic collaterals in the short and long term.

Our study suggests that no collaterals between the systemic veins and the portal vein tributaries should appear, even in the long term, if the pressure in the systemic veins remains at levels commonly observed in total cavopulmonary connection.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We are grateful to W. L. Gore & Associates for the provision of FEP Ringed Gore-Tex Vascular Grafts and GORE-TEX Stretch Vascular Grafts.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. McCuskey R.S., Reilly F.D. Hepatic microvasculature:dynamic structure and its regulation. Sem Liver Dis 1993;13:1-12.[Medline]
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  4. Matsuda H., Covino E., Hirose H., et al. Acute liver dysfunction after modified Fontan operation for complex cardiac lesions. J Thorac Cardiovasc Surg 1988;96:219-226.[Abstract]
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  7. Bridges N.D., Mayer J.E., Lock J.E., et al. Effect of baffle fenestration on outcome of the modified Fontan operation. Circulation 1992;86:1762-1769.[Abstract/Free Full Text]
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  12. Schneider D.J., Banerjee A., Mendelsohn M., Noorwood W. Hepatic venous malformation after modified Fontan procedure with partial hepatic vein exclusion. Ann Thorac Surg 1997;63:1177-1179.[Abstract/Free Full Text]
  13. Champetier J., Haouari H., Le Bas J.F., Létoublon C., Alnaasan I., Farah I. Large inferior right hepatic vein. Sur Radiol Anat 1993;15:21-29.
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  19. Ahn J., Cooper J.M., Silberzweig J.E., Mitty H.A. Venographic appearance of portosystemic collateral pathways. B J Radiol 1997;70:1302-1306.[Abstract]
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