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Surgeon at Work Caval Inflow to the Graft: A Successful Way to Overcome Diffuse Portal System Thrombosis in Liver Transplantation Daniel Azoulay, MD, PhD, Guillermo M Hargreaves, MD, Denis Castaing, MD, Henri Bismuth, MD, FACS (Hon) Diffuse portal thrombosis is a well-established con- traindication to liver transplantation, because ade- quate hepatopetal portal flow to the liver graft is required 1,2 at least in the short term. Possible salvage solutions in this situation are: combined liver and small-bowel transplantation, permanent 3 or tempo- rary 4 arterialization of the graft portal vein, or cavoportal hemitransposition. 5 On the basis of the principle (experimental and clinical) of cavoportal transposition, we report our experience in anastomosis of the vena cava or one of its main tributaries to the portal vein, when con- fronted with diffuse thrombosis of the portal system. CLINICAL BACKGROUND Three cases of cavoportal transposition have been reported so far in clinical applications. The first two patients in whom this operation was done showed improvement in their condition, 6,7 but early death from overperfusion of the liver’s portal system, caus- ing hepatic congestion and uncontrollable acidosis in the third child, 8 led to the adoption of the safer procedure of end to side portacaval shunt. 9 Recently the principle of this technique has been reintroduced in clinical practice for liver trans- plantation, in nine cases of diffuse portal vein thrombosis. 5 A modification has become obligatory in the absence of the portal vein and only cavoportal hemitransposition, half of the reconstruction, is carried out. In this series of nine patients from four centers, five patients were alive after 6 to 11 months, and four patients died from causes not re- lated to the technique. EXPERIENCE AT THE PAUL BROUSSE HOSPITAL From our series of more than 1,000 patients receiv- ing transplants, in two of them caval flow was di- verted into the portal vein to overcome the problem of diffuse portal vein thrombosis, permitting suc- cessful liver transplantation. Patient 1 Indication for liver transplantation. A 48-year- old man presented with cryptogenetic cirrhosis to- gether with severe chronic encephalopathy, intrac- table ascites, and repeated variceal bleeding despite sclerotherapy. Progressive ligation of the umbilical vein for chronic encephalopathy 10 was followed by progression from Child grade B to Child grade C cirrhosis, and diffuse portal vein thrombosis was confirmed by coeliomesenteric arteriography. Orthotopic liver transplantation. Orthotopic liver transplantation (OLT) was performed on No- vember 14, 1996. At laparotomy no vein of the portal system was found to be patent. A lateroterminal anastomosis was constructed between the native in- frahepatic vena cava and the graft portal vein (Fig. 1A). Cold ischemia time was 7 hours 30 minutes, 14 units of blood were transfused, and bile produc- tion from the graft was obtained immediately. Peroperative doppler ultrasonography showed portal flow to be hepatofugal, so a clip had to be No competing interests declared. Received December 19, 1999; Accepted November 23, 1999. From the Centre He ´pato-Biliaire, Ho ˆpital Paul Brousse, Villejuif, and Uni- versite ´ Paris-Sud, Paris, France. Correspondence address: Daniel Azoulay, MD, PhD, Centre He ´pato-Biliaire, Ho ˆpital Paul Brousse, 12 avenue Paul Vaillant Couturier, 94800, Villejuif, France. 493 © 2000 by the American College of Surgeons ISSN 1072-7515/00/$21.00 Published by Elsevier Science Inc. PII S1072-7515(99)00299-9

Caval inflow to the graft: a successful way to overcome diffuse portal system thrombosis in liver transplantation

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Surgeon at Work

Caval Inflow to the Graft: A Successful Way to OvercomeDiffuse Portal System Thrombosis in Liver Transplantation

Daniel Azoulay, MD, PhD, Guillermo M Hargreaves, MD, Denis Castaing, MD,Henri Bismuth, MD, FACS (Hon)

Diffuse portal thrombosis is a well-established con-traindication to liver transplantation, because ade-quate hepatopetal portal flow to the liver graft isrequired1,2 at least in the short term. Possible salvagesolutions in this situation are: combined liver andsmall-bowel transplantation, permanent3 or tempo-rary4 arterialization of the graft portal vein, orcavoportal hemitransposition.5

On the basis of the principle (experimental andclinical) of cavoportal transposition, we report ourexperience in anastomosis of the vena cava or one ofits main tributaries to the portal vein, when con-fronted with diffuse thrombosis of the portal system.

CLINICAL BACKGROUND

Three cases of cavoportal transposition have beenreported so far in clinical applications. The first twopatients in whom this operation was done showedimprovement in their condition,6,7 but early deathfrom overperfusion of the liver’s portal system, caus-ing hepatic congestion and uncontrollable acidosisin the third child,8 led to the adoption of the saferprocedure of end to side portacaval shunt.9

Recently the principle of this technique hasbeen reintroduced in clinical practice for liver trans-plantation, in nine cases of diffuse portal veinthrombosis.5 A modification has become obligatoryin the absence of the portal vein and only cavoportal

hemitransposition, half of the reconstruction, iscarried out. In this series of nine patients from fourcenters, five patients were alive after 6 to 11months, and four patients died from causes not re-lated to the technique.

EXPERIENCE AT THEPAUL BROUSSE HOSPITAL

From our series of more than 1,000 patients receiv-ing transplants, in two of them caval flow was di-verted into the portal vein to overcome the problemof diffuse portal vein thrombosis, permitting suc-cessful liver transplantation.

Patient 1Indication for liver transplantation. A 48-year-

old man presented with cryptogenetic cirrhosis to-gether with severe chronic encephalopathy, intrac-table ascites, and repeated variceal bleeding despitesclerotherapy. Progressive ligation of the umbilicalvein for chronic encephalopathy10 was followed byprogression from Child grade B to Child grade Ccirrhosis, and diffuse portal vein thrombosis wasconfirmed by coeliomesenteric arteriography.

Orthotopic liver transplantation. Orthotopicliver transplantation (OLT) was performed on No-vember 14, 1996. At laparotomy no vein of the portalsystem was found to be patent. A lateroterminalanastomosis was constructed between the native in-frahepatic vena cava and the graft portal vein (Fig.1A). Cold ischemia time was 7 hours 30 minutes,14 units of blood were transfused, and bile produc-tion from the graft was obtained immediately.

Peroperative doppler ultrasonography showedportal flow to be hepatofugal, so a clip had to be

No competing interests declared.

Received December 19, 1999; Accepted November 23, 1999.From the Centre Hepato-Biliaire, Hopital Paul Brousse, Villejuif, and Uni-versite Paris-Sud, Paris, France.Correspondence address: Daniel Azoulay, MD, PhD, Centre Hepato-Biliaire,Hopital Paul Brousse, 12 avenue Paul Vaillant Couturier, 94800, Villejuif,France.

493© 2000 by the American College of Surgeons ISSN 1072-7515/00/$21.00Published by Elsevier Science Inc. PII S1072-7515(99)00299-9

applied to the retrohepatic vena cava above thecavoportal anastomosis to obtain hepatopetal flow.

Postoperative course. The patient developedascites (proteins 16 g/L) and renal failure, limitingFK506 (tacrolimus) doses. Two episodes of varicealbleeding were controlled by sclerotherapy.

The patient was finally discharged on the 90thpostoperative day with mild ascites that did notneed evacuation. At this time the biological testswere within the normal range. At 5 months thepatency of the cavoportal anastomosis was con-firmed during transjugular liver biopsy (Fig. 1B).

Outcomes. The patient developed histologi-cally proved chronic rejection with severe jaundice.He died 7 months after OLT from terminal liverfailure while on the waiting list for retransplanta-tion. At autopsy all vessels and anastomosis wereseen to be patent, together with chronic biliary andarterial rejection and normal hepatocytes. The mor-phology of the kidneys was preserved and mild fi-brosis was seen.

Patient 2Indication for liver transplantation. A 44-year-

old man with cryptogenetic cirrhosis classed asChild grade C, with chronic encephalopathy andcomplicated by a cardiac output of 18 L/min and amean pulmonary arterial pressure of 38mmHg.

Pretransplantation workup. No portal vein wasfound either on doppler ultrasonography or on coe-liomesenteric angiography, which showed a hugevaricose vein draining into the left renal vein.

OLT. On June 14, 1998, at laparotomy none ofthe veins of the portal system were patent. In thispatient caval flow was diverted into the portal veinthrough an end to end anastomosis from the recip-ient’s left renal vein to the graft’s portal vein asshown in Figure 2A. The cold ischemia time was 7hours, and no blood was transfused. Immediate bileproduction was obtained.

Postoperative course. The postoperative coursewas uneventful; neither ascites nor variceal bleedingcomplicated the hospital stay of 36 days. Dopplerultrasonography confirmed patency of all the ves-sels (hepatic artery, portal vein, hepatic veins, renalveins, and vena cava). At discharge biologic testswere within the normal range.

Outcomes. At 6 months after transplantation,selective arteriography of superior mesenteric andleft renal arteries showed a patent portorenal anas-tomosis (Figs. 2B, 2C). Seventeen months aftertransplantation, the patient remains at home withnormal liver function tests and levels of urea andcreatinine within normal limits. Right heart cathe-terization at 6 months showed cardiac output and

Figure 1. (A) Lateroterminal anastomosis between native vena cava and graft portal vein (patient 1) with retrohepaticvena cava striction. (B) Control of anastomosis during transjugular liver graft biopsy 5 months after transplantation.

494 Azoulay et al Diverting Caval Flow to Grafted Liver J Am Coll Surg

pulmonary arterial pressure to be within the normalrange.

SUMMARY

Portal vein thrombosis was considered to be a majorcontraindication to liver transplantation before theintroduction of vessel grafts from the recipient’s areaof confluence of the splenic and superior mesentericveins, behind the neck of the pancreas, to the graft’sportal vein.11 Refinement in surgical technique hasgiven rise to a large number of possibilities to over-come portal vein thrombosis in OLT recipients, rang-ing from portal vein thrombectomy11-15 to severaldifferent venous graft jump reconstructions.16-25

All these reconstructions require the presence ofa patent vein of the portal system. When neithersplanchnic veins nor sufficiently large venous col-laterals are available, liver transplantation has beenconsidered impossible. Salvage solutions include ar-terialization of the portal vein3,4 with the associatedrisk of liver damage in the longterm, a combinedliver and bowel transplantation has been proposedbut not yet reported (and in any case the results ofcombined liver and bowel transplants are not asgood as those of liver transplantation alone) andfinally the use of blood inflow from the inferiorvena cava as first reported by Tzakis and coworkers.5

Portal flow from the inferior vena cava may beperformed as a last resort. Although the conse-

Figure 2. (A) Terminoterminal anastomosis between native leftrenal vein and graft portal vein (patient 2). (B) Venous phase ofselective superior mesenteric arteriography showing venoussplanchnic drainage into the liver through patent renoportalanastomosis. (C) Venous phase of selective left renal arteriogra-phy showing patent renoportal anastomosis 6 months aftertransplantation.

495Vol. 190, No. 4, April 2000 Azoulay et al Diverting Caval Flow to Grafted Liver

quences of severe pretransplantation portal hyper-tension remain and should be treated before, dur-ing, and after transplantation,5 liver function isnormal in the short and midterm. With this newprocedure, diffuse portal vein thrombosis is nolonger an absolute contraindication to liver trans-plantation. But this needs to be confirmed in lightof further experience and longterm followup.

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496 Azoulay et al Diverting Caval Flow to Grafted Liver J Am Coll Surg