Spontaneous Reversal of Portal Flow in Patients with Bleeding Varices Treated by Emergency Portacaval Shunt
A. Crane Charters, III, MD, La Jolla, California James G. Chandler, MD, La Jolla, California James K. Condon, MD, La Jolla, California David E. Grambort, MD, La Jolla, California Stuart E. Levin, MD, La Jolla, California Thomas I?. Modafferi, MD, La Jolla, California Marshall J. Orloff, MD, La Jolla, California
Stagnation of blood flow develops in the valveless portal vein when hepatic outflow obstruction becomes severe as a result of advanced cirrhosis and spontaneous reversal of flow can occur. The phenomenon of reversal of flow has been well documented by intraoperative manometric studies [I31, umbilical vein portography [4], hepatic vein angiography [5], and radioactive tracer studies [6]. These studies have been performed primarily in patients undergoing elective portacaval shunt and in nonoperated patients with cirrhosis, and reversal of portal flow has been noted infrequently. Little information is available on the hemodynamics of portal blood flow in patients undergoing emergency portacaval shunt for bleeding esophageal varices. The significance of portal pressure measurements taken at the time of acute variceal hemorrhage has not been established. In the presence of retrograde or stagnant blood flow in the portal vein, the liver derives its entire blood supply from the hepatic artery. Theoretical-
From the Department of Surgery, School of Medicine, University of California, San Diego, La Jolla. California. Reprint requests should be addressed to Dr Orloff. Department of Surgery, University Hospital, 225 West Dickinson Street, San Diego, California 92103. Presented at the Fourteenth Annual Meeting of the Society for Surgery of the Alimentary Tract, New York, New York, May 22 and 23, 1973.
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1974
ly, in this situation a portacaval shunt would divert the least amount of portal flow and not deprive the liver of any of its nutrient blood supply. Accordingly, it has been proposed that a portacaval shunt should be well tolerated in patients with stagnant or retrograde portal flow, whereas patients with a large prograde portal flow should tolerate a shunt poorly [2]. However, the small number of cases that have been reported are insufficient to validate this hypothesis, and the relative importance of diversion of portal flow in relation to the response to portacaval shunt is not known. In addition to acute variceal hemorrhage, the clinical manifestations of cirrhosis that have been attributed to increased hepatic outflow occlusion are the development of ascites and hepatic encephalopathy. However, the relation between these complications and stagnant or reversed portal blood flow has not been established. Moreover, the importance of portal diversion in the development of postshunt protein-related encephalopathy is not known. This study reports the incidence of reversal of portal blood flow in patients undergoing emergency portacaval shunt for bleeding esophageal varices, examines the prognostic significance of this finding, and relates it to other clinical manifestations of advanced cirrhosis.
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Material and Methods A prospective program for the evaluation of emergency portacaval shunt was initiated in 1962 and is still in progress. Every patient who entered the hospital with upper gastrointestinal hemorrhage and cirrhosis was subjected to the emergency portacaval shunt protocol, and an intensive diagnostic workup was initiated. If they were. found to be bleeding from esophageal varices, an emergency portacaval shunt was performed. The diagnostic workup was completed and the operation was started within a mean of eight hours from the time of admission to the emergency room. A total of 115 patients were operated on. Five patients were excluded from this review because of insufficient intraoperative pressure measurements to demonstrate the characteristics of portal flow. A detailed evaluation of portal hemodynamics was carried out by measuring the pressures within the portal vein and inferior vena cava at operation. After dissection of the portal vein and prior to the shunt, the following determinations were made (Figure 1): (1) free portal pressure: pressure within the portal vein without interference; (2) hepatic occluded portal pressure (HOPP): pressure on the hepatic side of a clamp occluding the portal vein; (3) splanchnic occluded portal pressure (SOPP): pressure on the splanchnic side of a clamp occluding the portal vein; (4) inferior vena cava pressure. When the splanchnic occluded portal pressure exceeded the hepatic occluded portal pressure by more than 10 mm of saline, a pressure gradient towards the liver prevailed, and normal (hepatopedal) flow in the portal vein was assumed. Stagnant or reversed (hepatofugal) portal flow occurred when HOPP was equal to or greater than SOPP. After construction of the shunt, the portal and inferior vena cava pressures were measured again to determine the degree of portal decompression and the gradient across the shunt. On the basis of
these intraoperative manometric studies, patients were divided into two groups: those with reversed portal blood flow and those with portal flow towards the liver. The patients’ histories, preoperative clinical status, and liver function studies were examined in an effort to characterize the patient with reversal of portal flow. The postoperative course and survival of these two groups were compared to establish the prognostic significance of this operative finding and to correlate it with the development of protein-related encephalopathy. Results Detailed intraoperative pressure measurements were made in 110 patients undergoing emergency portacaval shunt. The mean free portal pressure was 401 mm of saline with a range of 170 to 550 mm of saline. The mean corrected portal pressure (free portal pressure minus the inferior vena cava pressure) was 263 mm of saline. Reversal of portal flow (HOPP > SOPP) occurred in thirty-five patients (32 per cent). Normal flow towards the liver (HOPP < SOPP) occurred in seventy-five patients (68 per cent). All patients with reversal of portal flow underwent side to side portacaval shunt, Sixty-five per cent of the patients with normal flow towards the liver underwent side to side shunt, and the remaining shunts were end to side. In the series as a whole, there was no difference in survival between patients with end to side and those with side to side shunts, and the type of shunt did not appear to be a significant factor in comparing the mean of saline,
the two groups. After portacaval shunt corrected portal pressure fell to 25 mm documenting effective decompression of
the splanchnic
HEPATIC OCCLUDED PORTAL PRESSURE
venous
across
1
50-
40 -
zF
bed. The gradient
30-
F 2 8
zo-
10 -
I
’
I ‘4
SPLANCHNIC bccwm3 PORTAL PRESSURE
Figure 1. Technic for obtaining intraoperative pressure measurements. Flow becomes stagnant or spontaneous reversal occurs when the hepatic occluded portal pressure is equal to or greater than the splanchnic occluded portal pressure.
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post-op ASCITES
ENCEPHALOPATHY
Figure 2. Incidence of ascites and encephalopathy in patients with prograde and retrograde portal flow. The incidence of ascites on admission was the same in both groups. The incidence of encephalopathy on admission and of postshuntprotein-related encephalopathy was higher in patients with retrograde portal flow.
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the shunt was consistently less than 50 mm. The operation was effective in controlling hemorrhage in 96 per cent of the patients. It was not possible to predict patients who had reversal of portal flow by preoperative clinical assessment or liver function studies. The male to female predominance (2.6:1 for the entire series) was less in the group of patients with reversal of flow; 34 per cent of the patients with reversal of flow were females whereas only 28 per cent of the patients with normal flow were females. There was no significant difference in the ages of the two groups. Patients with reversal of flow tended to be on their first bleeding episode; twenty-eight of thirty-five patients (80 per cent) with retrograde flow were bleeding for the first time compared with thirty-nine of seventy-five patients (52 per cent) with prograde portal flow. Ascites on admission was seen in 54 per cent of patients with retrograde flow and in 53 per cent of patients with prograde flow. Encephalopathy on admission was more common in patients who had reversal of flow, occurring in 29 per cent, whereas it was observed in only 17 per cent of patients who had prograde flow. (Figure 2.) In the postoperative period there was a marked difference in the survival of the two groups. (Figure 3.) The operative mortality for patients with reversal of flow was 63 per cent in contrast with an operative mortality of 44 per cent for patients with prograde portal flow. This difference in survival persisted throughout the follow-up period. The cumulative five year survival was 36 per cent for patients with prograde portal flow and 17 per cent for patients with retrograde portal flow. The only significant clinical distinction among the survivors was a twofold greater incidence of proteinrelated encephalopathy in the group of patients with reversal of portal flow. The frequency of encephalopathy in this group was 23 per cent compared to 12 per cent among the survivors with prograde portal flow. (Figure 2.) Comments This is the first report concerned exclusively with the portal hemodynamics of the patient with acute variceal hemorrhage at the time of emergency portacaval shunt. The 32 per cent incidence of reversal of portal blood flow seen in these patients is much higher than that reported previously. (Table I.) It is not surprising that reversal of flow has been reported less frequently in other series since all of these include cirrhotic patients with-
Volume 127, January 1974
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Flow after
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portal
‘11 -’ , - - ,---__e-_--___a \a-
1 YEARS
AFTER
_ _. dretrograde
2
portal
flow
Shunt
I.SOPP> HOPPl .
flowlHOPP>SOPPI
4
3
EMERGENCY
Fartacaval
5
PORTACAVAL
SHUNT
Figure 3. Cumulative survival curves (Me table method) for patients with prograde and retrograde portal flow. A higher mortality is associated with retrograde portal f/o w.
out bleeding from varices as well as those undergoing elective shunts. Spontaneous decrease in portal pressure associated with clinical improvement during a prolonged hospital stay has been well documented [IO]. It is likely that some patients who may have had reversal of portal flow during an acute episode of variceal hemorrhage no longer manifest it at the time of elective portacaval shunt. Furthermore, elective portacaval shunt series necessarily select only those patients who survive the initial bleeding episode. The high mortality of patients with reversal of portal flow suggests that they may well be the patients who would not have survived the nonoperative management of variceal hemorrhage and are therefore selected out of other series. The finding that significantly more patients with reversal of flow were on their first
TABLE
I
Reported Inciderlce of Reversal of Portal Venous Flow
Author Ferguson [7] Kessler, Tice, and Zimmon [4] Moreno et al [8] Price, Voorhees, and Britton [3] Taylor, Hertzer, and Herman [9] Warren et al [5] Charters et al (present study) -____
Year
Number of Patients Studied
Patients with Reversal of Flow
Per cent
1963
48
0
0
1969 1967
150 26
2 0
1 0
1967
24
3
12
1968 1968
62 69
1 6
2 9
1973
110
35
32
27
Charters et al
episode of bleeding supports the probability of this selection. It is interesting to speculate that reversal of portal flow represents an acute change in portal hemodynamics and reflects the rapid onset of hepatic outflow obstruction and an increase in portal hypertension that precipitates variceal hemorrhage. Reilly and colleagues [II] have shown in dogs that there is a greater increase in retrograde portal blood flow with acute hepatic outflow obstruction than with chronic obstruction of the hepatic veins. Indirect support for the speculation that reversal of flow may be an acute phenomenon is the finding of an equal incidence of ascites in the two groups. The formation of ascites is a manifestation of chronic hepatic outflow obstruction and may not parallel acute changes in portal hemodynamics. Pressure studies recorded prior to the construction of a shunt can provide only a rough index of the volume of portal flow. However, a significant pressure differential between the splanchnic and hepatic sides of an occluding clamp on the portal vein should clearly indicate the direction of flow. There is some debate as to the value of differential portal pressure measurements in predicting survival of patients undergoing portacaval shunt. Taylor, Hertzer, and Herman [9], in studying sixty-two patients, found no apparent correlation between differential portal pressures and prognosis. Price, Voorhees, and Britton [3] noted that operative pressures were useful in determining the type of shunt to be performed, but that the functional capacity of the liver was independent of the portal pressuie measurements. Warren and associates [2], conversely, have proposed that operative portal pressure measurements are of prognostic significance and have suggested that patients who have pressure recordings indicative of large prograde portal flow will suffer the greatest diversion of flow after a portacaval shunt and will tolerate the operation least well. In contrast, patients with pressure recordings indicative of low prograde portal flow or reversal of flow will have the least amount of blood diverted from the liver by portacaval shunt and should do well after the shunt. The most striking feature of our study was the marked difference in survival between patients with reversal of portal flow and prograde portal flow. The higher mortality of patients undergoing emergency portacaval shunt with reversal of portal flow is in direct conflict with the proposal of Warren and his associates [2]. It is
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likely that reversal of flow reflects a severe form of hepatic outflow obstruction that is related to far advanced liver disease and that hepatic cellular function is as important a determinant of survival after operation as is the degree of portal diversion. It was not possible preoperatively to identify patients with reversal of portal flow on the basis of liver function tests or clinical examination, and by these parameters, the degree of hepatic dysfunction was not significantly different in the two groups. The finding of reversal of flow at the time of acute variceal hemorrhage is a meaningful prognostic sign and indicates a significantly decreased likelihood of survival and good function after emergency portacaval shunt. The relation of hepatic encephalopathy to portal hemodynamics has been debated since Hahn and colleagues [12], working in Pavlov’s laboratory, described the syndrome of “meat intoxication” in dogs with Eck fistulas in 1893. McDermott [13], and others [Z] have emphasized the importance of hepatic blood flow in the development of encephalopathy. The increased incidence of encephalopathy seen on admission in patients in our series with reversal of portal flow supports that concept. However, McDermott has proposed further that patients who have the least diversion of flow after portacaval shunt (that is, patients with reversal) are relatively protected from the development of encephalopathy. The finding that postshunt protein-related encephalopathy was twice as high in the survivors who had spontaneous reversal of portal flow compared to the survivors with prograde flow is not consistent with that hypothesis and suggests that the development of postshunt encephalopathy is not solely or mainly dependent on the magnitude of portal flow diversion. Conclusions
Spontaneous reversal or stagnation of portal blood flow occurred in 32 per cent of patients undergoing emergency portacaval shunt for bleeding esophageal varices, a much higher incidence than has been noted previously. The survival rate was lower in patients with reversed portal flow (37 per cent) than in those with prograde portal flow (56 per cent). The incidence of encephalopathy on admission and that of protein-related encephalopathy after shunt were twice as high in the survivors who had reversed portal flow. These findings indicate that factors other than magnitude of portal flow diversion are important in determining the response to portacaval shunt.
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References 1. Orloff MJ. Emergency portacaval shunt: a comparative study of shunt, varix ligation, and nonsurgical treatment of bleeding esophageal varices in unselected patients with cirrhosis. Surgery 52: 103, 1962. 2. Warren WD, Restrepo JE, Respess JC, Muller WH: The importance of hemodynamic studies in the management of portal hypertension. Ann Surg 158: 387, 1963. 3. Price JB Jr, Voorhees AG Jr, Britton RC: Operative hemodynamic studies in portal hypertension: significance and limitations. Arch Surg 95: 843, 1967. 4. Kessler RE, Tice DA, Zimmon DS: Retrograde flow of portal vein blood in patients with cirrhosis. Radiology 92. 1038. 1969. 5. Warren WD, Fomon JJ, Viamonte M, Martinez LO, Kalser: Spontaneous reversal of portal venous blood flow in cirrhosis. Surg Gynecol Obstet 126: 315, 1968. 6. Longmire WP Jr, Mulder DG, Mahoney PS, Mellinkoff SW: Srde-to-side portacaval anastomosis for portal hypertension. Ann Surg 147: 881, 1958. 7. Ferguson OJ: Hemodynamics in surgery for portal hyper-
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tension. Ann Surg 158: 383, 1963. 8. Moreno AH, Burchell AR, Rousselot LM, Panke WF. Slafsky SF, Burke JH: Portal blood flow in cirrhosis of the liver. J C/in Invest46: 436, 1967. 9. Taylor PC, Hertzer NR, Herman RE Differential portal pressures in relation to prognosis and to survival of patients undergoing portacaval shunt. Cleveland C/in Quart 35: 183, 1968. 10. Reynolds TB, Geller HM, Kugma OT, ?edeker AG: Spontaneous decrease in portal pressure with clinical tmprovement in cirrhosis. N Engl J Met’ 263: 734, 1960. 11. Reilly JW, Price JB, Swada M, Davidson DB, Voorhees AB: Effect of increased outflow resistance on retrograde portal flow and hepatic metabolic efficiency following a side-lo-side portacaval shunt. Surgery 66: 1026, 1969. 12. Hahn M, Massen 0, Nencki M, Pawlow J: Die Eck’sche Fistel zwischen der unteren Hohlvene under der Pfortader und ihre Folgen fur den Orgaliismus. Arch Exper Path Pharmakoi 32: 161,1893. 13. McDermott WV: Evaluation of the hernodynamics of portal hypertension in the selection o patients for shunt surgery. Ann Surg 176: 449, 1972.
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