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Does the direction of portal blood flow determine outcome with small-diameter prosthetic H-graft portacaval shunt?
Does the direction of portal blood flow determine outcome with small-diameter prosthetic H-graft portacaval shunt? Alexander Tampa,
S. Rosemurgy
II, MD, James G. Norman,
MD, and Sarah E. Goode,
RN,
Fla.
Background. Partial portal decompression, as attained by small-diameter prosthetic H-graft portacaval shunting, continues to gain popularity because of favorable outcomes. This study was undertaken to determine whether the direction of preshunt or postshunt portal blood flow or reversal in the direction of portal flow occurred with shunting effect outcome after small-diameter prosthetic H-graft portacaval shunt. Methods. In 56 consecutive patients the direction of portal flow was determined before and after shunting. The direction of portal blood flow before and after shunting and changes in the direction of portal flow that occur with shunting were correlated with 30-day and l-year survival, as well as with the rate of postshunt encephalopathy. Results. Portal pressures significantly decreased in all with shunting. Whether or not stratified by Child’s class@ation, neither the preshunt nor postshunt direction of portal jlow affected 30-day or l-year survival or incidence of encephalopathy. Eleven patients (significant at p
the Department
of Surgery,
University
of South Florida,
TRADITIONAL END-TO-SIDE portacaval shunt is associated with a prohibitive risk of progressive liver dysfunction and consequently has been abandoned as a first-choice treatment option in patients with portal hypertension and bleeding varices.’ Conventional wisdom holds that liver dysfunction after totally diverting portasystemic shunts is due to the loss of portal blood flow into the liver. Because of this belief, most modern strategies for the treatment of portal hypertension aim to maintain prograde portal flow. Portal blood flow is intrinsically related to portal pressure. To maintain prograde portal flow when treating portal hypertension caused by cirrhosis, pressure within the portal vein must remain elevated because of altered sinusoidal anatomy. It is possible to treat the esophagogastric variceal complex complicating portal hypertension without eliminating portal hypertension. THE
Accepted Reprint Hospital,
for publication
May 29, 1996.
requests: Alexander S. Rosemurgy II, MD, Tampa P.O. Box 1289, Room A171, Tampa, FL 33601.
Copyright 0 1997 by Mosby-Year Book, 00396060/97/$5.00 + 0 11/56/75434
Inc.
General
Tampa, Fla.
For example, the distal splenorenal shunt, the most popular selective portosystemic shunt, maintains portal hypertension as it disconnects the splenic venous bed from the portal system and selectively decompresses the hypertensive esophagogastric varices into the systemic circulation transplenically.?After distal splenorenal shunting, portal pressures are not returned to normal. Shunt portal pressures can then be equal to, greater than, or less than preshunt pressures, although portal pressures always remain elevated. Interestingly, after a distal splenorenal shunt, the best outcomes are seen with partial portal decompression.2 The concept of partial portal decompression led to the development of small-diameter H-graft portacaval shunts. Early experience with the prosthetic H-graft shunt was promising, 3, 4 because it seemed to lower portal pressures below a “bleeding threshold” while maintaining some degree of portal hypertension, which promoted maintenance of prograde portal blood flow. Sarfeh and Rypins4a 5 studied the small-diameter prosthetic H-graft portacaval shunt and found that smaller diameter grafts decrease portal hypertension less than larger grafts and better maintain portal blood flow with SURGERY
95
96
Rosemurgy,
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Table I. Preoperative direction of portal blood flow and outcome portacaval shunt, stratified by Child’s classification Child’s classification A B
Preshunt Jaw
portal
Hepatopetal Hepatopetal Hepatofugal Hepatopetal Hepatofugal
C
after small-diameter
prosthetic
SUPY 1997
H-graft
No. of patients
30-Day suruiual (%)
I-Year Survival (%)
Encephalopathy at 1 year (%)
4 29 2 18 3
100 97 100 83 100
100* 90-t 100 72* 67
33* 5t
50 17” 0
*One patient was not included because of death unrelated to shunt/liver disease. tTwo patients were not included because of deaths unrelated to shunt/liver disease.
Table II. Preoperative portacaval
*Four
direction of portal blood flow and outcome shunt, independent of Child’s classification
Preshunt portal jlow
patients
Hepatopetal Hepatofngal
51 5
patients were not included
No.
of
because of deaths unrelated
to shunt/liver
after small-diameter
prosthetic
H-graft
30-Day survival
l-Year survival
Enqbhalopathy at 1 year
(%)
(%)
(%)
92 100
83* 80
13* 25
disease
superior postoperative liver function and clinical outcomes. To Sarfeh and Rypins, maintenance of prograde portal blood flow correlates with superior clinical outcomes. Johansen evaluated “native” small-diameter side-to-side portacaval shunts. Like Sarfeh and Rypins, he found that partial portal decompression is associated with clinical outcomes better than those seen after total portal decompression achieved in his own’ or other studies. Unlike Sarfeh and Rypins, however, Johansen noted that despite maintenance of postshunt portal hypertension, prograde portal blood flow is generally, if not always, lost after construction of a small-diameter side-to-side shunt.6 Johansen’s work suggests that possession of some degree of portal hypertension may be more important in determining outcome than direction of portal blood flow. We used a small-diameter prosthetic H-graft portacaval shunt in 76 patients to treat bleeding esophagogastric varices not amenable to medical management and were pleased with the clinical outcomes seen after H-graft shunting. & ’ It is unclear whether the low incidence of encephalopathy and progressive liver failure occurring after H-graft portacaval shunting is due to maintenance of prograde portal blood flow. Furthermore, it is unclear whether the preshunt or postshunt direction of portal blood flow has any bearing on clinical outcome. This study was therefore undertaken to determine whether the direction of portal blood flow before or after small-diameter prosthetic H-graft portacaval shunt or reversal of portal blood flow with shunting affects clinical outcome. Our hypotheses in under-
taking this study were portal blood flow was outcomes after partial preshunt hepatofugal come.
MATERIAL
that maintenance of prograde important in attaining optimal portal decompression and that flow would portend a poor out-
AND METHODS
Seventy-six patients with bleeding esophagogastric varices caused by portal hypertension underwent smalldiameter prosthetic H-graft portacaval shunting with 8 mm externally reinforced polytetrafluoroethylene at University of South Florida affiliated hospitals since November 1987. Our shunt technique has been described.8 All patients were treated according to protocol and prospectively followed. In 56 patients hemodynamic stability permitted preoperative evaluation of portal blood.flow direction by using visceral angiography, color-flow Doppler scanning, or both (Acuson 128 with linear array 5 MH probe; Acuson Corp., Mountain View, CA). These 56 patients are the population of this study. After shunting, directional blood flow in the portal vein was determined with transfemoral portography or color-flow Doppler scanning or both. Portal pressures were measured during operation before and after shunting. Outcome parameters of survival and clinical encephalopathy were assessed at 30 days and 1 year (12 to 16 months) after shunting. Encephalopathy was defined clinically as absent, mild (resolved with lactulose therapy and dietary protein restriction), or severe (persistent despite medical management). Data were prospectively entered into a spreadsheet
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PROGRADE CIRETROGRADE B REVERSED
Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood flow blood flow blood flow
pre- and postshunt pre- and postshunt preshunt, hepatofugal
portal
flow
postshunt
Fig. 1. 30-day survival and postshunt portal flow rates stratified by Child’s class. Prograde, preshunt and postshunt hepatopetal portal blood flow; retrograde, preshunt and postshunt hepatofugal portal blood flow; reversed, preshunt and postshunt hepatopetal portal blood flow and hepatofugal portal flow. database (dBase Iv, BORLAND, Scottsvalley, CA) on an IBM-compatible personal computer. Direction of portal blood flow was correlated with clinical outcome with and without stratification by Child’s classification. Statistical analysis was undertaken in a two-tailed manner by using TRUE EPISTAT (EPISTAT Services, Richardson, TX). Differences were accepted with 95% confidence. RESULTS Thirty-eight men (68%) and eighteen women (32%) with a mean age of 52 years (range, 42 to 76 year) underwent small-diameter prosthetic H-graft portacaval shunting after the determination of portal vein blood flow direction. Four patients (7%) had Child’s class A disease, 31 (55%) had class B, and 21 (38%) had class C. Portal pressures fell in all patients with shunting. Preshunt portal pressures fell from 29.4 ? 5.5 mm Hg to 19.6 ? 5.8 mm Hg with shunting; (p< 0.01 by paired Student’s t test). The pressure gradient between the portal vein and the inferior vena cava also fell significantly, with a mean decrease of 11 t 1.2 mm Hg (significant at p < 0.001, paired Student’s t test). Six patients had mild encephalopathy after shunting that was well treated in all with lactulose and dietary restriction of red meat. Four patients died of liver failure within 30 days of operation. All of these four were believed to be at high risk for postshunt liver failure because of their advanced Child’s class disease (i.e., Child’s class C) and general ill health. An additional eight patients died more than 30 days but less than 12
to 16 months (1 year) after shunting as a result of trauma (two), suicide (one), alcohol abuse (one), pulmonary embolus (one), and progressive body/liver failure, old age, and ill health (three). One patient has been lost to follow-up but was known to be alive and well more than 5 years after shunting. Four patients who died more than 30 days but within 1 year after shunting were excluded from the analysis of data regarding l-year survival and encephalopathy because their deaths were in no way related to liver function or the preceding shunt (trauma in two, suicide in one, and pulmonary embolus in one). With or without these four patients excluded from data analysis, Child’s classification did not predict encephalopathy or mortality at 30 days or 1 year. Preoperative portalvenous blood flowwas noted to be hepatopetal in 51 (91%) patients and hepatofugal in 5 (9%). When patients were stratified by Child’s classification of disease, preoperative directional blood flow did not predict survival at 30 days (p = 0.29) or at 1 year ($I = 0.46)) nor did it predict the incidence of hepatic encephalopathy (p = 0.52) (analysis of covariance; Table I). Furthermore, when outcome was evaluated independent of Child’s classification, 30-day survival (p = 0.68, Fisher’s exact test), l-year survival (p = 0.65, Yate’s chi-squared test), and the incidence of hepatic encephalopathy (p= 0.47, Fisher’s exact test) did not correlate with the direction of preoperative portal blood flow (Table II). In 40 (78%) of 51 patients hepatopetal flow was maintained after the small-diameter prosthetic H-graft portacaval shunt. In 11 patients (22%) flow reversed
98
Rosemurgy, Norman, Goode January
Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood blood blood
flow flow flow
pre- and postshunt pre- and postshunt preshunt, hepatofugal
por .tal flow
SUWY 1997
postshunt
Fig. 2. l-year survival and postshunt portal flow rates stratified by Child’s class. Prograde, preshunt and postshunt hepatopetal protal blood flow; retrograde, preshunt and postshunt hepatofugal protal blood flow; reversed, preshunt and postshunt hepatopetal protal blood flow and hepatofugal portal flow.
from hepatopetal to hepatofugal flow after shunting. These 11 patients represent a significant number of patients reversing flow (significant at p< 0.001, Fisher’s exact test). Reversal of hepatopetal flow with shunting was not seen in any of the four patients with Child’s class A disease but was seen in 5 (17%) of 29 patients with class B disease and in 6 (33%) of 18 patients with class C disease. When stratified by Child’s classification, the 11 patients who had reversal of preoperative hepatopetal flow with shunting did not differ from the 40 patients who maintained hepatopetal flow with shunting in 30-day survival (p = 0.48; Fig. l), l-year survival (p = 0.49; Fig. 2)) or incidence of hepatic encephalopathy (p = 0.72; Fig. 3) (three category Mantel-Haenszel test). Independent of Child’s classification, reversal of preoperative hepatopetal flow, relative to maintenance of hepatopetal flow, was not associated with an increase in 30-day survival (82% versus 95%; p = 0.20), l-year survival (82% versus 83%; p = 0.73; Fig. 4)) or encephalopathy (11% versus 13%; p = 0.71, Fisher’s exact test). When patients were stratified by Child’s classification, the direction of postshunt portal blood flow did not predict survival at 30 days (p = 0.17) or at 1 year (p = 0.72), nor did it predict the incidence of hepatic encephalopathy at 1 year (p = 0.66; three category Mantel-Haenszel test, Figs. 1 through 3), Similarly, independent of Child’s classification, the direction of portal blood flow after shunting did not affect 30-day survival (95% for hepatopetal flow versus 88% for hepatofugal flow; p = 0.57, Fisher’s exact test), l-year survival (p = 0.83, Yate’s chi-squared test; Fig. 4), or the incidence of encephalopathy (13% for hepatopetal flow
versus 18% for hepatofugal squared test).
flow; p = 0.27, Yate’s chi-
DISCUSSION The direction of blood flow within the portal vein is determined by portal venous pressure and sinusoidal blood flow resistance. As cirrhosis progresses, architectural distortion of the liver increases, thereby increasing sinusoidal resistance to portal blood flow. Further, maintenance of prograde portal blood flow to the liver requires increases in portal blood pressure. Such increases result in the development of venous collaterals from the portal vein, that is, varices. Because varices limit the progressive increase in portal pressures, progressive increases in sinusoidal resistance to portal blood flow eventually result in stagnation of portal flow and ultimately portal vein thrombosis or reversal of flow. Surgical portasystemic shunts provide an alternative path of low resistance that decreases portal pressures and, thereby, variceal pressures and thus reduces the chances of variceal bleeding. It is generally believed that if the shunt is large, portal pressures decrease to approach inferior vena cava pressures and much, if not all, of the portal blood flow is diverted through the shunt and thus away from the liver. This belief has recently been confirmed.5, lo Although portal blood flow in the patient with cirrhosis may account for only 25% or less of the nutrient blood flow to the liver, it is traditionally held that shunting portal blood away from the liver results in a high incidence of liver failure and encephalopathy. An alternative explanation that has received less attention,
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1
PROGRADE 0 RETROGRADE El REVERSED
Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood blood blood
flow flow flow
pre- and pre- and preshunt,
postshunt postshunt hepatofugal
portal
flow
1
postshunt
Fig. 3. l-year encephalopathy and postshunt portal flow rates stratified by Child’s class. Prograde preshunt and postshunt hepatopetal protal blood flow; retrograde, preshunt and postshunt hepatofugal protal blood flow; reversed, preshunt and postshunt hepatopetal protal blood flow and hepatofugal portal flow.
however, is that decreases in portal pressure that occur with total shunts lead to encephalopathy and liver failure. The importance of portal blood flow on hepatic function was first alluded to in work by Pavlov in 1893, whose careful studies of end-to-side portocaval shunts in dogs led to the first description of hepatic encephalopathy. Pavlov’s postmortem examinations documented atrophic livers in dogs with patent shunts and normal livers in dogs with thrombosed shunts, leading him to conclude that portal blood flow was critical to hepatic function. Although his studies may not be directly applicable to human beings with cirrhosis because of inherent species differences, Pavlov’s findings have been supported by decades of experience with total portosystemic shunts. What Pavlov did not consider, however, was an alternative hypothesis emphasizing the importance of portal pressure. Furthermore, none of his experiments controlled for the loss of portal pressure and, thereby, for the role of portal pressure in hepatic encephalopathy in progressive liver failure. In 1967 Warren et al.ll introduced the concept of “selective” shunting by demonstrating, as others* later also did, that by disconnecting the splenic vein from the portal vein and allowing gastroesophageal varices to decompress transsplenically, pressure within the portal vein is maintained to varying degrees, and prograde portal blood flow to the liver is generally maintained. The clinical outcomes associatedwith selective shunting have generally been judged superior to those associated with nonselective (i.e., central) shunts. It has traditionally been held that the improved survival and low rates of encephalopathy after distal splenorenal shunting are
due to maintenance of prograde portal blood flow. With this in mind, it becomes difficult to explain the clinical success of patients after distal splenorenal shunts, knowing that nearly 50% may lose prograde portal perfusion 1 to 3 years after shunting and that a significant number of patients thrombose their portal veins with late follow-up. I*, l3 An alternative explanation offered by Rikkers14 cites altered intestinal absorption in patients with portal hypertension. Rikkers found that persistent mesenteric venous hypertension, as seen in patients after distal splenorenal shunt, may protect against postshunt encephalopathy by reducing the intestinal absorption of cerebral toxins. Although Rikkers demonstrated that maintenance of mesenteric venous hypertension is beneficial, he has also shown that patients with partial portal decompression do best after distal splenorenal shunts.* Sarfeh et al. l5 focused their app roach to portal hypertension on achieving partial portal decompression. They demonstrated continued prograde portal flow in one half of their patients who had partial portal decompression through a 10 mm polytetrafluoroethylene interposition portacaval shunt. With smaller (i.e., 8 mm polytetrafluoroethylene) diameter interposition shunts, prograde portal perfusion is much more likely to be maintained. Sarfeh et al. believe that the lower incidence of encephalopathy after 8 mm diameter prosthetic H-graft shunting is due to better maintenance of portal blood flow.‘O Johansen’ favors a “native” side-toside portacaval shunt, generally 10 to 12 mm long. He alters the anastomosis during operation to maintain a shunt gradient of 8 to 15 mm Hg (average, 10.4 mm Hg). In a reported series of 50 patients, all were noted
100
Rosemurgy, Norman, Goode January
“Qw? 1997
RETROGRADE
*Four patients eliminated because their deaths in no way were related to their previous shunt or liver disease. Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood blood blood
flow flow flow
pre- and postshunt* pre- and postshunt preshunt, hepatofugal
portal
flow
postshunt
Fig. 4. l-year survival and postshunt portal flow rates independent of Child’s class. Prograde, preshunt and postshunt hepatopetal protal blood flow; retrograde, preshunt and postshunt hepatofugal portal blood flow; reversed, preshunt and postshunt hepatopetal protal blood flow and hepatomgal portal flow. to reverse flow in the portal vein cephalad to the shunt.6 During a follow-up period averaging 26 months, only three patients (6%) died of liver failure and only three patients (6%) had encephalopatby. These are excellent results. In light of the fact that 100% of his patients had postshunt hepatofugal flow, Johansen’s experience documents that maintenance of prograde flow to the liver is not necessary to prevent liver failure or encephalopathy after shunting. His studies, those of Sarfeh and Rypins, and this study add credibility to the alternative hypothesis, which emphasizes the importance of the maintenance of portal hypertension after shunting. The apparent contradiction between the collective experiences of Sarfeh and Rypins and Johansen et al. may be less than apparent at first glance. Some differences can certainly be explained by the various methods used to determine directional blood flow. Sarfeh and Rypins used visceral angiography and scintigraphy to determine portal vein directional blood flow, whereas Johansen et al. used color-flow Doppler ultrasonography. We have chosen to study our patients by using visceral angiography, transfemoral venography, and colorflow Doppler ultrasonography, which we have found to be accurate and reproducible. Other differences between the collective experiences of these groups may reflect that Sarfeh and Rypins focused on blood flow, whereas Johansen has seemingly given more attention to portal pressure. In general, we made an attempt not to focus on either portal blood flow or portal pressure as the key determinant of clinical outcome, although through their entangled relationship both are certainly important. The collective work of these investigators and the inseparable relationship between portal blood
flow and pressure add substance and credibility to the alternative hypothesis emphasizing the importance of maintenance of portal hypertension after shunting. We have come to believe that optimal outcome after portosystemic shunting lies more with our maintenance of portal hypertension than with the direction of portal blood flow. This study documents that maintenance of prograde portal blood flow is generally possible after small-diameter (8 mm) prosthetic H-graft shunting, although the direction of portal blood flow before or after shunting is not a critical factor in determining clinical outcome, nor are changes in the direction of portal blood flow with shunting (i.e., reversal of flow). We have previously demonstrated postprandial augmentation of portal blood flow in patients with small-diameter prosthetic H-graft portacaval shunts.16 We have suggested this as a possible explanation of the low rates of liver failure and encephalopathy in our patients after H-graft shunting. It may be, however, that postprandial increases in portal blood pressure, occurring concomitantly with increased portal blood flow, limit intestinal absorption of false neurotransmitters and thereby lead to the superior clinical outcomes seen in our patients. In our series of more than ‘7’5 patients undergoing 8 mm prosthetic interposition portacaval shunts, liver failure, encephalopathy, and rebleeding rates were all below 10%. In explaining these excellent clinical outcomes, only minor roles can be ascribed to the direction of portal blood flow before or after shunting and changes in portal flow occurring with shunting. Outcome after shunting procedures is probably determined by many factors. First of all, differences in defining and quantifying some complications, such as
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Rosemurgy, Norman, Goode 101 121,
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encephalopathy, make the true incidence of these complications difficult to determine. Undoubtedly the choice of shunt, technical skill of the surgeon, quality of the perioperative care, patient’s hepatic reserve, and medical comorbidities play roles in determining outcome after shunting. In addition, variables more difficult to measure, such as sinusoidal resistance to portal blood flow and hepatic arterial and portal venous hemodynamics, play as yet undetermined roles. The presence of hepatotrophic factors in the portal venous blood, the secretion of humoral factors by the hypertensive portal vein endothelium, and the compensatory cardiovascular response seen in patients with cirrhosis add to the complexity of determining the relative importance of many variables determining patient outcome. The direction of preshunt and postshunt portal blood flow is in part related to Child’s classification, with patients with more advanced classes of disease (i.e., classes B and C) more likely to have preshunt hepatofugal flow or to reverse hepatopetal flow with shunting. Nonetheless, it seems that the direction of portal blood flow is simply inadequate in predicting or measuring hepatic reserve, which is presumably a major determinant of outcome after H-graft shunting. Trying to account for clinical differences in patients after placement of portacaval shunts by focusing solely on the maintenance of prograde portal blood flow is at best naive. We can say with certainty that the direction of portal blood flow before or after shunting, as well as changes in the direction of portal blood flow that occur with shunting, are not independent predictors of survival or the incidence of encephalopathy after shunting. Alternative explanations for the success of the small-diameter prosthetic Hgraft portacaval shunt must be sought to better understand these complex patients and their care.
REFERENCES 1. Terblanche J. The surgeon’s role in the management of portal hypertension. Ann Surg 1989;209:381-99. 2. Rikkers LF, Cormier RA, Vo NM Effects of altered portal hemodynamicsafterdistalsplenorenalshunts.AmJSurg 3. Sarfeh IJ, Rypins EB, Fardi M, et al. Clinical tal hemodynamics gery 1984;96:223-7.
after
small
diameter
1987;153:80-5. implications of por-
portacaval
4. Sarfeh IJ, Rypins EB, Conroy RM, Mason relationships of shunt diameter, portal
h-graft.
GR. Portacaval flow patterns
cephalopathy. Ann Surg 1984;197:422-6. 5. Sarfeh IJ, Rypins EB. Partial versus total
shunt
cirrhosis. 6. Johansen
for variceal
Ann Surg K Partial
1994;219:353-61. portal decompression
rhage. Am J Surg 1989;157:479-82. 7. Johansen K Prospective comparison decompression for bleeding necol 1992;175:528-34. 8. Rosemurgy a prosthetic 9. Rosemurgy portacaval
of partial
esophageal
Sur-
H-graft: and en-
in alcoholic hemor-
versus total portal
varices.
Surg Obstet
Gy-
AS, McAllister EW, Kearney RE. Prospective study of h-graft portacaval shunt. Am J Surg 1991;161:159-63. AS, McAllister EW. Small diameter shunt. Surg Annu 1994;26:101-13.
10. Repins EB, Milne N, Sarfeh IJ. Analysis flow after 8 mm vs 16 mm portacaval
prosthetic
of nutrient hepatic blood h-grafts in a prospective
randomized trial. Am J Surg 1995;169:197-200. 11. Warren WD, Zeppa R, Foman JS. Selective transplenic pression of gastroesophageal Ann Surg 1967;166:437-55. 12. MaillardJN, splenorenal
varices
H-graft
decom-
by distal splenorenal
Flamant I’M, Chandler JG. Selectivity shunt. Surgery 1979;86:66371.
shunt.
of the distal
13. Rotstein LE, Makowka L, Langer B, et al. Thrombosis of the portal vein following distal splenorenal shunt. Surg Obstet Gynecol 1979;149:847-51. 14. Rikkers
LF.
Portal
hemodynamics,
intestinal
absorption,
postshunt encephalopathy. Surgery 1983;94:12633. 15. Sarfeh IJ, Rypins EB, Mason GR. A systematic appraisal tacaval H-graft diameters. 16. Rosemurgy AS, McAllister augmentation tacaval shunt.
and of por-
Ann Surg 1986;204:35662. EW, Km-to HZ, CatesJD. Postprandial
of portal hepatic inflow Am J Surg 1992;2:213-5.
after
8 mm
H-graft
por-
S. Rosemurgy
II, MD, James G. Norman,
MD, and Sarah E. Goode,
RN,
Fla.
Background. Partial portal decompression, as attained by small-diameter prosthetic H-graft portacaval shunting, continues to gain popularity because of favorable outcomes. This study was undertaken to determine whether the direction of preshunt or postshunt portal blood flow or reversal in the direction of portal flow occurred with shunting effect outcome after small-diameter prosthetic H-graft portacaval shunt. Methods. In 56 consecutive patients the direction of portal flow was determined before and after shunting. The direction of portal blood flow before and after shunting and changes in the direction of portal flow that occur with shunting were correlated with 30-day and l-year survival, as well as with the rate of postshunt encephalopathy. Results. Portal pressures significantly decreased in all with shunting. Whether or not stratified by Child’s class@ation, neither the preshunt nor postshunt direction of portal jlow affected 30-day or l-year survival or incidence of encephalopathy. Eleven patients (significant at p
the Department
of Surgery,
University
of South Florida,
TRADITIONAL END-TO-SIDE portacaval shunt is associated with a prohibitive risk of progressive liver dysfunction and consequently has been abandoned as a first-choice treatment option in patients with portal hypertension and bleeding varices.’ Conventional wisdom holds that liver dysfunction after totally diverting portasystemic shunts is due to the loss of portal blood flow into the liver. Because of this belief, most modern strategies for the treatment of portal hypertension aim to maintain prograde portal flow. Portal blood flow is intrinsically related to portal pressure. To maintain prograde portal flow when treating portal hypertension caused by cirrhosis, pressure within the portal vein must remain elevated because of altered sinusoidal anatomy. It is possible to treat the esophagogastric variceal complex complicating portal hypertension without eliminating portal hypertension. THE
Accepted Reprint Hospital,
for publication
May 29, 1996.
requests: Alexander S. Rosemurgy II, MD, Tampa P.O. Box 1289, Room A171, Tampa, FL 33601.
Copyright 0 1997 by Mosby-Year Book, 00396060/97/$5.00 + 0 11/56/75434
Inc.
General
Tampa, Fla.
For example, the distal splenorenal shunt, the most popular selective portosystemic shunt, maintains portal hypertension as it disconnects the splenic venous bed from the portal system and selectively decompresses the hypertensive esophagogastric varices into the systemic circulation transplenically.?After distal splenorenal shunting, portal pressures are not returned to normal. Shunt portal pressures can then be equal to, greater than, or less than preshunt pressures, although portal pressures always remain elevated. Interestingly, after a distal splenorenal shunt, the best outcomes are seen with partial portal decompression.2 The concept of partial portal decompression led to the development of small-diameter H-graft portacaval shunts. Early experience with the prosthetic H-graft shunt was promising, 3, 4 because it seemed to lower portal pressures below a “bleeding threshold” while maintaining some degree of portal hypertension, which promoted maintenance of prograde portal blood flow. Sarfeh and Rypins4a 5 studied the small-diameter prosthetic H-graft portacaval shunt and found that smaller diameter grafts decrease portal hypertension less than larger grafts and better maintain portal blood flow with SURGERY
95
96
Rosemurgy,
Norman,
Goode January
Table I. Preoperative direction of portal blood flow and outcome portacaval shunt, stratified by Child’s classification Child’s classification A B
Preshunt Jaw
portal
Hepatopetal Hepatopetal Hepatofugal Hepatopetal Hepatofugal
C
after small-diameter
prosthetic
SUPY 1997
H-graft
No. of patients
30-Day suruiual (%)
I-Year Survival (%)
Encephalopathy at 1 year (%)
4 29 2 18 3
100 97 100 83 100
100* 90-t 100 72* 67
33* 5t
50 17” 0
*One patient was not included because of death unrelated to shunt/liver disease. tTwo patients were not included because of deaths unrelated to shunt/liver disease.
Table II. Preoperative portacaval
*Four
direction of portal blood flow and outcome shunt, independent of Child’s classification
Preshunt portal jlow
patients
Hepatopetal Hepatofngal
51 5
patients were not included
No.
of
because of deaths unrelated
to shunt/liver
after small-diameter
prosthetic
H-graft
30-Day survival
l-Year survival
Enqbhalopathy at 1 year
(%)
(%)
(%)
92 100
83* 80
13* 25
disease
superior postoperative liver function and clinical outcomes. To Sarfeh and Rypins, maintenance of prograde portal blood flow correlates with superior clinical outcomes. Johansen evaluated “native” small-diameter side-to-side portacaval shunts. Like Sarfeh and Rypins, he found that partial portal decompression is associated with clinical outcomes better than those seen after total portal decompression achieved in his own’ or other studies. Unlike Sarfeh and Rypins, however, Johansen noted that despite maintenance of postshunt portal hypertension, prograde portal blood flow is generally, if not always, lost after construction of a small-diameter side-to-side shunt.6 Johansen’s work suggests that possession of some degree of portal hypertension may be more important in determining outcome than direction of portal blood flow. We used a small-diameter prosthetic H-graft portacaval shunt in 76 patients to treat bleeding esophagogastric varices not amenable to medical management and were pleased with the clinical outcomes seen after H-graft shunting. & ’ It is unclear whether the low incidence of encephalopathy and progressive liver failure occurring after H-graft portacaval shunting is due to maintenance of prograde portal blood flow. Furthermore, it is unclear whether the preshunt or postshunt direction of portal blood flow has any bearing on clinical outcome. This study was therefore undertaken to determine whether the direction of portal blood flow before or after small-diameter prosthetic H-graft portacaval shunt or reversal of portal blood flow with shunting affects clinical outcome. Our hypotheses in under-
taking this study were portal blood flow was outcomes after partial preshunt hepatofugal come.
MATERIAL
that maintenance of prograde important in attaining optimal portal decompression and that flow would portend a poor out-
AND METHODS
Seventy-six patients with bleeding esophagogastric varices caused by portal hypertension underwent smalldiameter prosthetic H-graft portacaval shunting with 8 mm externally reinforced polytetrafluoroethylene at University of South Florida affiliated hospitals since November 1987. Our shunt technique has been described.8 All patients were treated according to protocol and prospectively followed. In 56 patients hemodynamic stability permitted preoperative evaluation of portal blood.flow direction by using visceral angiography, color-flow Doppler scanning, or both (Acuson 128 with linear array 5 MH probe; Acuson Corp., Mountain View, CA). These 56 patients are the population of this study. After shunting, directional blood flow in the portal vein was determined with transfemoral portography or color-flow Doppler scanning or both. Portal pressures were measured during operation before and after shunting. Outcome parameters of survival and clinical encephalopathy were assessed at 30 days and 1 year (12 to 16 months) after shunting. Encephalopathy was defined clinically as absent, mild (resolved with lactulose therapy and dietary protein restriction), or severe (persistent despite medical management). Data were prospectively entered into a spreadsheet
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PROGRADE CIRETROGRADE B REVERSED
Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood flow blood flow blood flow
pre- and postshunt pre- and postshunt preshunt, hepatofugal
portal
flow
postshunt
Fig. 1. 30-day survival and postshunt portal flow rates stratified by Child’s class. Prograde, preshunt and postshunt hepatopetal portal blood flow; retrograde, preshunt and postshunt hepatofugal portal blood flow; reversed, preshunt and postshunt hepatopetal portal blood flow and hepatofugal portal flow. database (dBase Iv, BORLAND, Scottsvalley, CA) on an IBM-compatible personal computer. Direction of portal blood flow was correlated with clinical outcome with and without stratification by Child’s classification. Statistical analysis was undertaken in a two-tailed manner by using TRUE EPISTAT (EPISTAT Services, Richardson, TX). Differences were accepted with 95% confidence. RESULTS Thirty-eight men (68%) and eighteen women (32%) with a mean age of 52 years (range, 42 to 76 year) underwent small-diameter prosthetic H-graft portacaval shunting after the determination of portal vein blood flow direction. Four patients (7%) had Child’s class A disease, 31 (55%) had class B, and 21 (38%) had class C. Portal pressures fell in all patients with shunting. Preshunt portal pressures fell from 29.4 ? 5.5 mm Hg to 19.6 ? 5.8 mm Hg with shunting; (p< 0.01 by paired Student’s t test). The pressure gradient between the portal vein and the inferior vena cava also fell significantly, with a mean decrease of 11 t 1.2 mm Hg (significant at p < 0.001, paired Student’s t test). Six patients had mild encephalopathy after shunting that was well treated in all with lactulose and dietary restriction of red meat. Four patients died of liver failure within 30 days of operation. All of these four were believed to be at high risk for postshunt liver failure because of their advanced Child’s class disease (i.e., Child’s class C) and general ill health. An additional eight patients died more than 30 days but less than 12
to 16 months (1 year) after shunting as a result of trauma (two), suicide (one), alcohol abuse (one), pulmonary embolus (one), and progressive body/liver failure, old age, and ill health (three). One patient has been lost to follow-up but was known to be alive and well more than 5 years after shunting. Four patients who died more than 30 days but within 1 year after shunting were excluded from the analysis of data regarding l-year survival and encephalopathy because their deaths were in no way related to liver function or the preceding shunt (trauma in two, suicide in one, and pulmonary embolus in one). With or without these four patients excluded from data analysis, Child’s classification did not predict encephalopathy or mortality at 30 days or 1 year. Preoperative portalvenous blood flowwas noted to be hepatopetal in 51 (91%) patients and hepatofugal in 5 (9%). When patients were stratified by Child’s classification of disease, preoperative directional blood flow did not predict survival at 30 days (p = 0.29) or at 1 year ($I = 0.46)) nor did it predict the incidence of hepatic encephalopathy (p = 0.52) (analysis of covariance; Table I). Furthermore, when outcome was evaluated independent of Child’s classification, 30-day survival (p = 0.68, Fisher’s exact test), l-year survival (p = 0.65, Yate’s chi-squared test), and the incidence of hepatic encephalopathy (p= 0.47, Fisher’s exact test) did not correlate with the direction of preoperative portal blood flow (Table II). In 40 (78%) of 51 patients hepatopetal flow was maintained after the small-diameter prosthetic H-graft portacaval shunt. In 11 patients (22%) flow reversed
98
Rosemurgy, Norman, Goode January
Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood blood blood
flow flow flow
pre- and postshunt pre- and postshunt preshunt, hepatofugal
por .tal flow
SUWY 1997
postshunt
Fig. 2. l-year survival and postshunt portal flow rates stratified by Child’s class. Prograde, preshunt and postshunt hepatopetal protal blood flow; retrograde, preshunt and postshunt hepatofugal protal blood flow; reversed, preshunt and postshunt hepatopetal protal blood flow and hepatofugal portal flow.
from hepatopetal to hepatofugal flow after shunting. These 11 patients represent a significant number of patients reversing flow (significant at p< 0.001, Fisher’s exact test). Reversal of hepatopetal flow with shunting was not seen in any of the four patients with Child’s class A disease but was seen in 5 (17%) of 29 patients with class B disease and in 6 (33%) of 18 patients with class C disease. When stratified by Child’s classification, the 11 patients who had reversal of preoperative hepatopetal flow with shunting did not differ from the 40 patients who maintained hepatopetal flow with shunting in 30-day survival (p = 0.48; Fig. l), l-year survival (p = 0.49; Fig. 2)) or incidence of hepatic encephalopathy (p = 0.72; Fig. 3) (three category Mantel-Haenszel test). Independent of Child’s classification, reversal of preoperative hepatopetal flow, relative to maintenance of hepatopetal flow, was not associated with an increase in 30-day survival (82% versus 95%; p = 0.20), l-year survival (82% versus 83%; p = 0.73; Fig. 4)) or encephalopathy (11% versus 13%; p = 0.71, Fisher’s exact test). When patients were stratified by Child’s classification, the direction of postshunt portal blood flow did not predict survival at 30 days (p = 0.17) or at 1 year (p = 0.72), nor did it predict the incidence of hepatic encephalopathy at 1 year (p = 0.66; three category Mantel-Haenszel test, Figs. 1 through 3), Similarly, independent of Child’s classification, the direction of portal blood flow after shunting did not affect 30-day survival (95% for hepatopetal flow versus 88% for hepatofugal flow; p = 0.57, Fisher’s exact test), l-year survival (p = 0.83, Yate’s chi-squared test; Fig. 4), or the incidence of encephalopathy (13% for hepatopetal flow
versus 18% for hepatofugal squared test).
flow; p = 0.27, Yate’s chi-
DISCUSSION The direction of blood flow within the portal vein is determined by portal venous pressure and sinusoidal blood flow resistance. As cirrhosis progresses, architectural distortion of the liver increases, thereby increasing sinusoidal resistance to portal blood flow. Further, maintenance of prograde portal blood flow to the liver requires increases in portal blood pressure. Such increases result in the development of venous collaterals from the portal vein, that is, varices. Because varices limit the progressive increase in portal pressures, progressive increases in sinusoidal resistance to portal blood flow eventually result in stagnation of portal flow and ultimately portal vein thrombosis or reversal of flow. Surgical portasystemic shunts provide an alternative path of low resistance that decreases portal pressures and, thereby, variceal pressures and thus reduces the chances of variceal bleeding. It is generally believed that if the shunt is large, portal pressures decrease to approach inferior vena cava pressures and much, if not all, of the portal blood flow is diverted through the shunt and thus away from the liver. This belief has recently been confirmed.5, lo Although portal blood flow in the patient with cirrhosis may account for only 25% or less of the nutrient blood flow to the liver, it is traditionally held that shunting portal blood away from the liver results in a high incidence of liver failure and encephalopathy. An alternative explanation that has received less attention,
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PROGRADE 0 RETROGRADE El REVERSED
Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood blood blood
flow flow flow
pre- and pre- and preshunt,
postshunt postshunt hepatofugal
portal
flow
1
postshunt
Fig. 3. l-year encephalopathy and postshunt portal flow rates stratified by Child’s class. Prograde preshunt and postshunt hepatopetal protal blood flow; retrograde, preshunt and postshunt hepatofugal protal blood flow; reversed, preshunt and postshunt hepatopetal protal blood flow and hepatofugal portal flow.
however, is that decreases in portal pressure that occur with total shunts lead to encephalopathy and liver failure. The importance of portal blood flow on hepatic function was first alluded to in work by Pavlov in 1893, whose careful studies of end-to-side portocaval shunts in dogs led to the first description of hepatic encephalopathy. Pavlov’s postmortem examinations documented atrophic livers in dogs with patent shunts and normal livers in dogs with thrombosed shunts, leading him to conclude that portal blood flow was critical to hepatic function. Although his studies may not be directly applicable to human beings with cirrhosis because of inherent species differences, Pavlov’s findings have been supported by decades of experience with total portosystemic shunts. What Pavlov did not consider, however, was an alternative hypothesis emphasizing the importance of portal pressure. Furthermore, none of his experiments controlled for the loss of portal pressure and, thereby, for the role of portal pressure in hepatic encephalopathy in progressive liver failure. In 1967 Warren et al.ll introduced the concept of “selective” shunting by demonstrating, as others* later also did, that by disconnecting the splenic vein from the portal vein and allowing gastroesophageal varices to decompress transsplenically, pressure within the portal vein is maintained to varying degrees, and prograde portal blood flow to the liver is generally maintained. The clinical outcomes associatedwith selective shunting have generally been judged superior to those associated with nonselective (i.e., central) shunts. It has traditionally been held that the improved survival and low rates of encephalopathy after distal splenorenal shunting are
due to maintenance of prograde portal blood flow. With this in mind, it becomes difficult to explain the clinical success of patients after distal splenorenal shunts, knowing that nearly 50% may lose prograde portal perfusion 1 to 3 years after shunting and that a significant number of patients thrombose their portal veins with late follow-up. I*, l3 An alternative explanation offered by Rikkers14 cites altered intestinal absorption in patients with portal hypertension. Rikkers found that persistent mesenteric venous hypertension, as seen in patients after distal splenorenal shunt, may protect against postshunt encephalopathy by reducing the intestinal absorption of cerebral toxins. Although Rikkers demonstrated that maintenance of mesenteric venous hypertension is beneficial, he has also shown that patients with partial portal decompression do best after distal splenorenal shunts.* Sarfeh et al. l5 focused their app roach to portal hypertension on achieving partial portal decompression. They demonstrated continued prograde portal flow in one half of their patients who had partial portal decompression through a 10 mm polytetrafluoroethylene interposition portacaval shunt. With smaller (i.e., 8 mm polytetrafluoroethylene) diameter interposition shunts, prograde portal perfusion is much more likely to be maintained. Sarfeh et al. believe that the lower incidence of encephalopathy after 8 mm diameter prosthetic H-graft shunting is due to better maintenance of portal blood flow.‘O Johansen’ favors a “native” side-toside portacaval shunt, generally 10 to 12 mm long. He alters the anastomosis during operation to maintain a shunt gradient of 8 to 15 mm Hg (average, 10.4 mm Hg). In a reported series of 50 patients, all were noted
100
Rosemurgy, Norman, Goode January
“Qw? 1997
RETROGRADE
*Four patients eliminated because their deaths in no way were related to their previous shunt or liver disease. Prograde Retrograde Reversed
= hepatopetal = hepatofugal = hepatopetal
portal portal portal
blood blood blood
flow flow flow
pre- and postshunt* pre- and postshunt preshunt, hepatofugal
portal
flow
postshunt
Fig. 4. l-year survival and postshunt portal flow rates independent of Child’s class. Prograde, preshunt and postshunt hepatopetal protal blood flow; retrograde, preshunt and postshunt hepatofugal portal blood flow; reversed, preshunt and postshunt hepatopetal protal blood flow and hepatomgal portal flow. to reverse flow in the portal vein cephalad to the shunt.6 During a follow-up period averaging 26 months, only three patients (6%) died of liver failure and only three patients (6%) had encephalopatby. These are excellent results. In light of the fact that 100% of his patients had postshunt hepatofugal flow, Johansen’s experience documents that maintenance of prograde flow to the liver is not necessary to prevent liver failure or encephalopathy after shunting. His studies, those of Sarfeh and Rypins, and this study add credibility to the alternative hypothesis, which emphasizes the importance of the maintenance of portal hypertension after shunting. The apparent contradiction between the collective experiences of Sarfeh and Rypins and Johansen et al. may be less than apparent at first glance. Some differences can certainly be explained by the various methods used to determine directional blood flow. Sarfeh and Rypins used visceral angiography and scintigraphy to determine portal vein directional blood flow, whereas Johansen et al. used color-flow Doppler ultrasonography. We have chosen to study our patients by using visceral angiography, transfemoral venography, and colorflow Doppler ultrasonography, which we have found to be accurate and reproducible. Other differences between the collective experiences of these groups may reflect that Sarfeh and Rypins focused on blood flow, whereas Johansen has seemingly given more attention to portal pressure. In general, we made an attempt not to focus on either portal blood flow or portal pressure as the key determinant of clinical outcome, although through their entangled relationship both are certainly important. The collective work of these investigators and the inseparable relationship between portal blood
flow and pressure add substance and credibility to the alternative hypothesis emphasizing the importance of maintenance of portal hypertension after shunting. We have come to believe that optimal outcome after portosystemic shunting lies more with our maintenance of portal hypertension than with the direction of portal blood flow. This study documents that maintenance of prograde portal blood flow is generally possible after small-diameter (8 mm) prosthetic H-graft shunting, although the direction of portal blood flow before or after shunting is not a critical factor in determining clinical outcome, nor are changes in the direction of portal blood flow with shunting (i.e., reversal of flow). We have previously demonstrated postprandial augmentation of portal blood flow in patients with small-diameter prosthetic H-graft portacaval shunts.16 We have suggested this as a possible explanation of the low rates of liver failure and encephalopathy in our patients after H-graft shunting. It may be, however, that postprandial increases in portal blood pressure, occurring concomitantly with increased portal blood flow, limit intestinal absorption of false neurotransmitters and thereby lead to the superior clinical outcomes seen in our patients. In our series of more than ‘7’5 patients undergoing 8 mm prosthetic interposition portacaval shunts, liver failure, encephalopathy, and rebleeding rates were all below 10%. In explaining these excellent clinical outcomes, only minor roles can be ascribed to the direction of portal blood flow before or after shunting and changes in portal flow occurring with shunting. Outcome after shunting procedures is probably determined by many factors. First of all, differences in defining and quantifying some complications, such as
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encephalopathy, make the true incidence of these complications difficult to determine. Undoubtedly the choice of shunt, technical skill of the surgeon, quality of the perioperative care, patient’s hepatic reserve, and medical comorbidities play roles in determining outcome after shunting. In addition, variables more difficult to measure, such as sinusoidal resistance to portal blood flow and hepatic arterial and portal venous hemodynamics, play as yet undetermined roles. The presence of hepatotrophic factors in the portal venous blood, the secretion of humoral factors by the hypertensive portal vein endothelium, and the compensatory cardiovascular response seen in patients with cirrhosis add to the complexity of determining the relative importance of many variables determining patient outcome. The direction of preshunt and postshunt portal blood flow is in part related to Child’s classification, with patients with more advanced classes of disease (i.e., classes B and C) more likely to have preshunt hepatofugal flow or to reverse hepatopetal flow with shunting. Nonetheless, it seems that the direction of portal blood flow is simply inadequate in predicting or measuring hepatic reserve, which is presumably a major determinant of outcome after H-graft shunting. Trying to account for clinical differences in patients after placement of portacaval shunts by focusing solely on the maintenance of prograde portal blood flow is at best naive. We can say with certainty that the direction of portal blood flow before or after shunting, as well as changes in the direction of portal blood flow that occur with shunting, are not independent predictors of survival or the incidence of encephalopathy after shunting. Alternative explanations for the success of the small-diameter prosthetic Hgraft portacaval shunt must be sought to better understand these complex patients and their care.
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13. Rotstein LE, Makowka L, Langer B, et al. Thrombosis of the portal vein following distal splenorenal shunt. Surg Obstet Gynecol 1979;149:847-51. 14. Rikkers
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