- Email: [email protected]
The emory perspective of the distal splenorenal shunt in 1990
The Emory Perspective of the Distal Splenorenal Shunt in 1990 J. Michael Henderson, FRCS, William J. Millikan, Jr., MD, John R. Galloway, MD, Atlanta.Georgia The distal splenorenal shunt (DSRS) has been extensively studied at Emory University over the past 18 years to define its role in the management of variceal bleeding. DSRS has been applied broadly in many different patient groups and has been evaluated in prospective randomized trials; thus, a considerable amount of data has accrued on the metabolic and hemodynamic consequences of selective variceal decompression. Its current role is defined as primary therapy for variceal bleeding in patients with portal vein thrombosis and good-risk patients with nonalcoholic cirrhosis. As a therapy for patients whose bleeding is not controlled by sclerotherapy, it should be used as the shunt procedure of choice, but patient evaluation must focus on the choice between DSRS and liver transplantation.
cess in which he viewed DSR_S not simply as an operation, but as a management concept. New information would change concepts, and new ideas would be tried and either accepted or discarded. Few therapies can have been so stringently tested by their innovator in an attempt to define their true role.
PATIENT EVALUATION In reaching a decision on how to treat the patient with variceal bleeding, two risks must be balanced: the risk of further bleeding and the risk of liver failure. Methods of evaluation have been presented in detail elsewhere in this issue [4]. In the context of selecting patients with DSRS, the key questions to be answered are: Does the patient need variceal decompression to control bleeding? Are the portal and systemic venous anatomy suitable for DSRS? Is the liver disease sufficiently good to sustain a reasonable period of quality life? In addressing these questions, the clinician is actually weighing the choice of DSRS against the other therapy choices of endoscopic sclerotherapy or liver transplantation in the patient who has bled from varices. r hen Dr. Warren came to Emory University in 1971, The first two questions are relatively easily answered. the distal splenorenal shunt (DSRS) had been Currently, most patients with bleeding esophageal varused for 5 years. The ability of this procedure to selective- ices are initially treated with sclerotherapy [5-7]. The ly decompress varices while maintaining portal hyperten- risk of rebleeding with sclerotherapy is approximately sion and portal flow was documented, and the initial 50%, and overall, sclerotherapy fails in about 25% to 30% clinical studies looked promising [1]. But this was only of patients who rebleed. Variceal decompression is needthe beginning. The next 18 years encompassed an in- ed in the patient in whom sclerotherapy has failed or in depth study of DSRS to define precisely its clinical, meta- the patient in whom the risk of rebleeding is considered bolic, and hemodynamic effects in patients with portal unacceptable. The anatomic suitability of candidates for hypertension and variceal bleeding. DSRS is defined by visceral angiography [8]. The splenic Prospective, randomized clinical trials compared vein is usually visualized on the venous phase of the splenDSRS with the total portal systemic shunt [2] and later ic artery injection, but occasionally splenoportography with endoscopic variceal sclerotherapy [3]. Both of these may be required. The left renal vein should be assessed by Emory studies were the first in a series of similar trials direct catheterization and phlebography; anomalies may conducted by other centers. However, apart from these increase the technical difficulty of DSRS [9]. randomized trials, the requirement has always been to The most complex issue to be addressed in making a fully evaluate and study all patients; each case has some- decision on suitability for DSRS is the state of the liver thing to teach the investigator. Such studies have taught [4]. The life expectancy of a patient with cirrhosis may be investigators much about the clinical outcomes of bleed- limited to days or extend to a normal span. The main ing control and survival and have yielded metabolic and factors contributing to this are the cause of the cirrhosis, hemodynamic data that have led to changes and improve- the activity of the process, the hepatocellular reserve, and ments in management methods. the systemic effects of the liver disease. Ideally, a candiThis review will summarize how the DSRS evolved date for DSRS should have stable disease with a reasonunder Dr. Warren. This was a continuing, dynamic pro- able hepatocyte reserve. This ideal cannot always be From the Department of Surgery and Clinical Research Facility, achieved, and compromise is sometimes required. EmoryUniversitySchoolof Medicine,Atlanta,Georgia.Supportedin part by GeneralClinicalResearchCenterPublicHealthServiceGrant OPERATIVE TECHNIQUES 5M01 RR 00039 from the National Institutes of Health, Bethesda, The technical goals of DSRS remain the same as Maryland. originally stated: selective reduction of pressure and volRequestsfor reprintsshouldbe addressedto J. MichaelHenderson, FRCS,DepartmentofSurgery,RoomF-511, 1364CliftonRoad,N.E., ume of flow through gastrcesophageal varices, mainteAtlanta, Georgia30322. nance of portal venous perfusion of the liver, and mainte-
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nance of continued venous hypertension in the intestinal bed [I]. Modification in how these goals are achieved has occurred in the past 20 years, with the acquisition of new knowledge and implementation of new techniques to overcome problems. The shunt: Dissection of the splenic vein out of the pancreas is the major technical facet of DSRS [10]. Full mobilization of the pancreas, from the superior mesenteric vessels to the splenic hilus, allows full caudad rotation of the pancreas and adequate visualization of the splenic vein. Dissection of the vein out of the pancreas entails dissecting directly on the vein, clearing the inferior and posterior surfaces before the superior and anterior surfaces, and accurately identifying and ligating the small pancreatic perforating tributaries. Isolation and mobilization of the left renal vein is aided by preoperative contrast evaluation. The shunt is fashioned by bringing the splenic vein down without tension or kinking to the antedor/superior surface of the left renal vein. Disconnection: This component of the operation is most important in achieving the goals of maintaining portal perfusion. While it was originally recognized that "portal azygos" disconnection was required as a component of DSRS, the initial emphasis was largely limited to ligation of the left gastric venous system [1]. This remains important, but extensive angiographic study [11] has shown that collateral pathways develop from the highpressure portal to low-pressure splenic vein through the pancreas, along the mesocolon, and as other transgastric collaterals. These are schematically illustrated in Figure 1. There are degrees of technical difficulty in achieving primary interruption of all these pathways at the time of DSRS [12]. The inferior mesenteric vein should always be ligated at its origin on the portal or splenic vein since it serves as an outflow from the hypertensive portal vein. The collaterals along the mesocolon are easily prevented by taking down the splenic flexure of the colon; this interrupts their final common path into the inferior ramus of the splenic vein. Meticulous dissection of the left gastric system should occlude its origin on the portal or splenic vein, and in addition, should ligate the vein and its tributaries on the lesser curve of the stomach and at the gastric esophageal junction. The right gastric vein should be ligated just superior to the pylorus. The most difficult collateral pathway to prevent is that through the pancreas, but data have shown that this siphon is most detrimental in loss of portal perfusion after standard DSRS, particularly in patients with alcoholic cirrhosis [11]. Completely dissecting the splenic vein entirely free from the pancreas will prevent development of this pathway [13]. This is shown conceptually in Figure 2. This addition to the disconnection component of DSRS has improved outcome in alcoholic patients. However, the additional technical hazard of possible splenic vein injury close to the hilus and subsequent loss of the shunt must be weighed by the operating surgeon in each individual case. RESULTS OF DSRS Control of variceal bleeding: Experience with DSRS at Emory in different trials and study groups has
Figure 1. The pathways of collateral developmentafter standard DSRS. Operative techniques to minimize this relentless collateralization are described in the text. (Reproduced with permission from [ 11].)
Figure 2. DSRS with entire splenopancreatic disconnection. Complete separation of the splenic vein from the pancreas prevents the developmentof the pancreatic siphon (Reproducedwith permission from [29] .)
shown control of variceal bleeding in 88% to 97% of patients [1,15-17]. The primary cause for rebleeding is shunt thrombosis, which occurs in 3% to 14% of patients [14-16]. An occluded shunt identified no more than 2 weeks after surgery may be corrected by reoperation. Late shunt thrombosis occurred in 2% or less of patients who were followed up by serial angiography [14,16]. Early rebleeding after DSRS may also occur with a patent shunt and inadequate varieeal decompression [17]. Variceal decompression by DSRS requires an adequate outflow through the short gastric veins, the splenic vein and shunt, and the left renal vein to the inferior vena cava.
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Development of an adequate outflow for completegastroesophageal decompression may take 4 to 6 weeks in some patients, making this the highest- risk time for rebleeding. Direct shunt catheterization and pressure measurement should be performed prior to hospital discharge and are the key diagnostic steps for upper gastrointestinal bleeding after shunt [17,18]. Data from 66 patients studied 1 to 2 weeks after DSRS showed a 7.8 mm Hg mean pressure gradient from the splenic vein to the vena cava [17]; however, 16 patients (24%) had a gradient more than 10 mm Hg, which suggests inadequate immediate decompression. Management of rebleeding with a patent shunt should be conservative, with vasopressin, tamponade, and/or sclerotherapy. The place of DSRS in the emergent setting of acute variceal bleeding not controlled by sclerotherapy, tamponade, or vasopressin has been controversial, the question being if adequate immediate decompression will be achieved by DSRS. The data cited previously suggest that 76% of patients have a rapid decrease in variceal pressure. However, in those who maintain some hypertension initially, the major gradient is from the renal vein to the vena cava. The alternative of splenocaval anastomosis should be considered in the emergent setting, particularly when the renal vein is small or abnormal or the spleen is large [19]. The clinical experience with emergent DSRS has shown control of variceal bleeding in 95% of patients, with mortality being related to the underlying liver disease [20]. Shunt stenosis can lead to variceal rebleeding at late follow-up. The risk of stenosis is greatest in patients with an abnormally thickened vein identified at the time of initial shunt and has been highest in our experience in patients with extrahepatic portal vein thrombosis [21]. The suspicion of stenosis is raised by late variceal rebleeding in a patient with a previously documented patent shunt. Diagnosis is made by shunt catheterization and the measurement of a gradient across the anastomosis. Management is by balloon dilation [22], Variceal bleeding control in other series has ranged from 73% to 95% [18,23-26]. In the randomized studies comparing DSRS with total shunts, bleeding control has been equivalent with both therapies in all but one series [23]. A uniform feature of the randomized studies comparing DSRS with endoscopic sclerotherapy has been the significantly better control of variceal bleeding with DSRS [3,27,28]. These factors are discussed in more detail elsewhere in this issue. Survival: Data on survival following DSRS at Emory have been generated in several different settings. The initial 10-year experience up to 198! with 348 patients undergoing DSRS showed an overall 5-year survival of 58% [14]. This was achieved in a population with 86% of patients in Child's class A and B and 56% of patients having alcoholic cirrhosis. The 5-year survival pattern was significantly (p <0.03) different between nonalcoholic (70%) compared with alcoholic (42%) patients. Data from the Emory randomized trial comparing DSRS with total shunt showed no significant difference in survival in Child's class A and B patients [2,15]. The 56
overall 10-year survival in the DSRS group was 41% whereas that in the total shunt group was 28%. In the nonalcoholic subset, 65% of patients were alive at 10 years in the DSRS group whereas only 29% of patients were alive in the total shunt group. Although these differences are not statistically significant, they reinforce the trends noted in the larger series [14]. The era of sclerotherapy at Emory resulted in a randomized trial comparing DSRS and sclerotherapy in a patient population with cirrhosis; 39% of patients were nonalcoholic, and 43% were in Child's class C. The 4-year survival after DSRS in this poorer-risk population was 43%. The differing survival pattern for alcoholic (35%) and nonalcoholic (54%) patients is again seen in this study group. Interestingly, there was no significant difference in survival in nonalcoholic patients in the two randomized groups between DSRS or endoscopic sclerotherapy. In contrast, there was a survival advantage (p <0.01) for alcoholic patients with cirrhosis randomized to sclerotherapy, provided surgical rescue was used for patients bleeding after sclerotherapy [16]. Finally, data from Emory studies show survival in alcoholic patients after DSRS appears to have improved with splenopancreatic disconnection [29]. In a nonrandomized, consecutive series of 78 patients undergoing DSRS with splenopancreatic disconnection, not only was portal perfusion better maintained in alcoholic patients than after standard DSRS, but survival was also improved. In 35 patients with alcoholic cirrhosis (40% in Child's class C), the 4-year survival was 60%. This improvement is shown in Figure 3, where the DSRS with splenopancreatic disconnection survival data is compared with standard DSRS survival data for patients with alcoholic and nonalcoholic cirrhosis. These data support the use of DSRS with splenopancreatic disconnection in patients with alcoholic cirrhosis. How do these data compare with other reported survival data for DSRS? The other randomized studies comparing DSRS with total shunts have shown no significant difference in survival between these therapies [2326,30]. These trials have been either exclusively or predominantly in alcoholic populations. The alcoholic versus nonalcoholic survival difference after DSRS was first documented by Zeppa and co-workers [31] in 1977, but has not been confirmed in other reported nonrandomized series [32-34]. The key questions in survival after variceal bleeding are: Will stopping the bleeding improve survival? Will the procedure used to stop the bleeding alter liver function in a positive or negative manner? What is the life expectancy of the patient, based on the underlying liver disease irrespective of bleeding? It is only by developing improved methods of classification and standardization between groups that meaningful comparison can be made in the analysis of survival data. Eneephalopathy: Hepatic encephalopathy is a complication of severe liver disease and may be either precipitated or spontaneous. In patients with variceal bleeding, it is a key marker of the severity of disease. In reaching a decision about the optimal therapy for a given patient, a history of recurrent encephalopathy suggests the need for
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1 9 8 2 A I c vs. N o n - A I c
AIc vs. N o n - A I c 1.0
"
.8
~
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/
.6 Figure 3. Kaplan-Meier survival curves for alcoholic and non-alcoholic patients after DSRS with splenopancreatic disconnection (left) and standard DSRS (right). There has been a significant impact on survival in alcoholic patients with the addition of splenopancreatic disconnection. AIc = alcoholic. (Reproduced with permission from [29] .)
AIc
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transplantation and warns against shunt surgery. On the other hand, a history of no encephalopathy, taken in conjunction with data suggesting good hepatocyte function, suggests a role for decompressive shunt rather than transplantation. How does DSRS impinge on the natural history of encephalopathy in liver disease? The overall clinical experience at Emory suggests that DSRS does not accelerate the occurrence or worsen the severity of encephalopathy. Concerning the incidence of encephalopathy in a control, nonshunted population, the data from the Emory randomized study with endoscopic sclerotherapy showed a 12% incidence of encephalopathy after 2 years in a nonoperated group of 26 patients at risk for liver disease [3]. In the parallel group randomized to DSRS, the incidence of encephalopathy was not significantly different (16%) [3]. Data from the Emory randomized trial in patients with Child's A or B disease showed encephalopathy rates of 5% at 2 years [2], 12% at 3 to 6 years [35], and 27% at 10-year follow-up [15]. At all time intervals, this incidence was significantly lower than in patients randomized to total shunts and might represent the expected natural history for the evolution of encephalopathy in such a population. Other studies both in controlled trials and nonrandomized series have shown wide variability in the occurence of encephalopathy after DSRS [36,37]. A recurring theme has been the role of maintenance of portal flow and adequate portal/splenic dissociation in reducing the risk of encephalopathy [38-40]. The highest incidence of encephalopathy after DSRS has occurred in series in which no disconnection has been performed [39], or in which there has been no postoperative documentation of maintenance of portal perfusion [23,25]. Hemodynamie changes with DSRS: Creation of a DSRS provides a low-pressure, high-flow shunt in the left upper quadrant of the abdomen that reduces esophagogastric splenic variceal pressure and controls bleeding. The secondary aim is to maintain portal venous hypertension in the splanchnic bed and thereby maintain sufficient pressure to sustain portal flow through the high-resistance cirrhotic liver. How far is this secondary goal achieved? Data from Emory show that portal flow is maintained
in 90% of nonalcoholic patients but in only 25% to 50% of alcoholic patients over the long term after standard DSRS [11,41]. Portal venous hypertension, measured indirectly as corrected sinusoidal pressure, is sustained in both groups of patients [16]. The development of large siphoning transpancreatic collaterals [13] from the highpressure portal vein to the low-pressure splenic vein is particularly detrimental to loss of portal flow in alcoholic patients. The time frame for development of collaterals and maintenance or loss of portal perfusion appears to be the first 6 to 12 months after DSRS, with few patients having further loss of portal flow thereafter [11]. Dissection of the entire splenic vein out of the pancreas prevents development of this siphon and results in maintenance of portal flow in 84% of alcoholic cirrhotic patients [29]. The incidence of portal vein thrombosis after DSRS is 4% in our experience [42], but nonoccluding thrombus can occur in up to 20% of patients. Subsequent thickening and narrowing of the portal vein can occur, which may complicate subsequent transplantation. Systemic hemodynamic changes characterized by a high cardiac output or low total vascular resistance occur with chronic liver disease and portal hypertension. After DSRS, patients in whom portal perfusion is maintained have a similar systemic hemodynamic profile to their preoperative status. However, patients with loss of portal perfusion have an associated hyperdynamic systemic circulation [41]. It has yet to be resolved whether the hepatic or the systemic hemodynamic change is the primary event. Other studies have documented the development of collaterals after DSRS, which may or may not be associated with total loss of portal flow [40,43,44]. Maintained portal perfusion rates of 50% to 87% have been documented at late follow-up [27,34]. Evaluation of the hemodynamic changes, in an operation with specific hemodynamic goals, is of paramount importance. The plethora of modifications to DSRS in the literature often do not have the hemodynamic data to indicate if the underlying principles of DSRS have been achieved [45-48]. Such studies must be interpreted with caution, Metabolic changes with DSRS: The effect of DSRS on hepatic function has been quantitated at Emory over
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the past 20 years, largely through studies conducted at the Clinical Research Center and supported by grants from the National Institutes of Health. The initial studies focused on nitrogen metabolism, measuring ammonia tolerance, urea synthesis rates, and amino acid metabolism. The data showed maintenance of preoperative levels of function in patients after DSRS but a significant decrease after total shunts [49]. The parallel clinical development of encephalopathy in the group with poorer nitrogen metabolism was interpreted as providing a metabolic basis for their encephalopathy [49], Subsequent studies have documented the critical role of maintained portal perfusion in sustaining hepatic function after DSRS [35] and have quantitated the metabolic and hemodynamic changes serially after DSRS [50]. Patients with extrahepatic portal vein thrombosis as the cause of their variceal bleeding maintain both liver volume and hepatocyte function after DSRS [42]. DSRS IN T H E OVERALL MANAGEMENT OF VARICEAL B L E E D I N G A center that treats patients with variceal bleeding should offer the full range of therapies, which comprise pharmacotherapy, endoscopic sclerotherapy, decompressive shunt, and liver transplantation. The key is being able to select the right therapy for the right patient at the right time. DSRS should be one of these available treatments. We believe it is indicated as primary therapy for Child's A patients with nonalcoholic cirrhosis and patients with portal vein thrombosis, and as rescue therapy for sclerotherapy failure in patients with alcoholic cirrhosis who are at an acceptable risk and patients with nonalcoholic cirrhosis in whom transplantation is not indicated. CONCLUSIONS As we review the status of DSRS at Emory in 1990, the following points bear emphasis. First, the concept of selective variceal decompression holds true. Varices can be decompressed and bleeding controlled by selective transplenic shunt, while portal hypertension and perfusion can be maintained at the same time. Modifications of the original procedure have improved the ability to implement these goals. Second, some patients are best treated for their variceal bleeding by DSRS, In our experience, this occurs in about 30% of patients; the key is appropriate selection. Finally, the study of patients undergoing DSRS has taught us much about the hemodynamic and metabolic pathophysiology of portal hypertension. Dr. Warren's requirements to test hypotheses and generate data have, we believe, helped define the correct role of DSRS among the other therapies discussed in this issue. We are grateful to him for giving us the opportunity to be part of this evolution. REFERENCES 1. Warren WD, Zeppa R, Foman JS. Selectivetransplenic decompression of gastroesophageal varices by distal splenorenal shunt. Ann Surg 1967; 166: 437. 58
2. Galambos JT, Warren WD, Rudman D, et al. Selectiveand total shunts in the treatment of bleedingvarices:a randomized controlled trial. N Engl J Med 1976; 285: 1089-95. 3. Warren WD, Henderson JM, Millikan WJ, et al. Distal splenorenal shunt versus endoscopic sclerotherapy for long-term management of variceal bleeding. Ann Surg 1986; 203: 454-62. 4. Galambos JT. Evaluation of patients with portal hypertension. Am J Surg 1990; 160: 14-8. 5. Terblanche J. Has sclerotherapy altered the management of patients with variceal bleeding? Am J Surg 1990; 160: 37-42. 6, Westaby D, Williams R. Status of sclerotherapy for variceal bleeding in 1990. Am J Surg 1990; 160: 32-6. 7. Paquet K-J, Mercado MA, Gad HA. Surgical procedures for bleeding esophagogastric variceS when sclerotherapy fails: a prospective study. Am J Surg 1990; 160: 43-7. 8. Nordlinger BM, Nordlinger DF, Fulenwider JT, et al. Angiography in portal hypertension: clinical significance in surgery. Am J Surg 1980; 139: 132-41. 9. Sones PJ, Rude JC, Warren WD. Evaluation of the left renal vein in candidates for splenorenal shunts. Radiology 1978; 127: 357-61. 10. Warren WD, Millikan WJ. Selective transplenic decompression procedure: changes in technique after 300 cases. Contemp Surg 1981; 18: 1t-32. 11. Henderson JM, Gong-Liang J, Galloway J, Millikan WJ Jr, S0nes PJ, Warren WD. Portaprival collaterals following distal splenorenal shunt: incidence, magnitude and associated portal perfusion changes. J Hepatol 1985; 1: 649-61. 12. Warren WD, Millikan WJ, Henderson JM, et al. Splenopancreatic disconnection: improved selectivityof the distal splenorenal shunt. Ann Surg 1986; 204: 346-55. 13. Warren WD, Millikan WJ Jr, Henderson JM, Rasheed ME, Salam AA. Selective variceal decompression after splenectomyor splenic vein thrombosis with a note on splenopancreatic disconnection. Ann Surg 1984; 199: 694-702. 14. Warren WD, Millikan WJ, Henderson JM, et al. Ten years of portal hypertensivesurgery at Emory: results and new perspectives. Ann Surg 1982; 195: 530-42. 15. Millikan WJ, Warren WD, Henderson JM, et al. The Emory prospective randomized trial: selectiveversus nonselectiveshunt to control variceal bleeding. Ten-year follow-up.Ann Surg 1985; 201: 712-22. 16. Henderson JM, Kutner MH, Millikan WJ, et al. Endoscopic variceal sclerosiscompared with distal splenorenal shunt to prevent recurrent variceal bleeding in cirrhosis. Ann Intern Med 1990 (in press). 17. Richards WO, Pearson TC, Henderson JM, Millikan WJ, Warren WD. Evaluation and treatment of early hemorrhage of the alimentary tract after selective shunt procedures. Surg Gynecol Obstet 1987; 164: 530-6. 18. Eckhauser KFE, Pomerantz RA, Knol JA, Strode WE, Williams DM, Turcotte JG. Early variceal rebleeding after successful distal splenorenal shunt. Arch Surg 1986; 121: 547-52. 19. Atta HM, Henderson JM, Galloway JR, Millikan WJ. Selective splenocavalshunt: 24 cases and reviewof literature. Arch Surg 1990 (in press). 20. Ports JR III, Henderson JM, Millikan WJ Jr, Warren WD. Emergency distal splenorenal shunts for variceal hemorrhage refractory to non-operative control. Am J Surg 1984; 148: 813-6. 21. Warren WD, Henderson JM, Millikan WJ, et al. Management of variceal bleedingin patients with non-cirrhoticportal vein thrombosis. Ann Surg 1988; 207: 623-34. 22. Henderson JM, Khishen MA, Millikan WJ, Sones PJ, Warren WD. Management of stenosisof distal splenorenalshunt by balloon dilation. Surg Gynecol Obstet 1983; 157: 43-8. 23. Harley HA J, Morgan T, Redeker AG, et al. Results of a randomized trial of end-to-side portacaval shunt and distal splenorenal shunt in alcoholicliverdisease and variceal bleeding. Gastroenterology 1986; 91: 802-9.
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24. Langer B, Taylor BR, Mackenzie DR, et al. Further report of a prospective randomized trial comparing distal splenorenal shunt with end-to-sideportacaval shunt. Gastroenterology 1985; 88: 4249. 25. Grace ND, Corm HC, Resnick RH, et al. Distal splenorenal vs portal systemic shunts after hemorrhage from variees: a randomized controlled trial. Hepatology 1988; 8: 1475-81. 26. Fischer JE, Bower RH, Atamian S, et al. Comparison of distal and proximal splenorenal shunts. A randomized prospective trial. Ann Surg 1981; 194: 531-44. 27. Rikkers LF, Burner DA, Volentine GD, et al. Shunt surgery versus endoscopic sclerotberapy for long-term treatment of varieeal bleeding: early results of a randomized trial. Ann Surg 1987; 206: 261-71. 28. Teres J, Bordas JM, Bravo D, et al. Sclcrotberapy vs distal splenorenal shunt in the elective treatment of variceal hemorrhage: a randomized controlled trial. Hepatology 1987;7: 430-6. 29. Henderson JM, Warren WD, Millikan W J, Galloway JR, Kawasald S, Kutner MH. DiStal splenorenal shunt with splenopanoreatic disconnection: a four year assessment. Ann Surg 1989; 210: 332-41. 30. Reichle FA, Fahmy WE, Golsorkhi M. Prospective comparative clinical trial with distal splenorenal and mesoeaval shunts. Am J Surg 1979; 137: 13-21. 31. Zeppa R, Hensley GT, Levi JU, et al. The comparative survival of alcoholics versus non-alcoholics after distal splenorenal shunt. Ann Surg 1978; 187: 510. 32. Rikkers LF, Soper N J, Cormier RA. Selective operative approach for varieeal hemorrhage. Am J Surg 1984; 147: 89~96. 33. Arson MA, van Hoerden JA, Ilrup DM. The distal splenorcnal shunt. Arch Surg 1984; 119: 609-14. 34. Myburgh JA. Selective shunts: the Johannesburg experience. Am J Surg 1990; 160: 67-74. 35. Rikkers LF, Rudman D, Galambos JT, et al. A randomized, controlled trial of the distal splenorenal shunt. Ann Surg 1978; 188: 271-82. 36. Rikkers LF. Is the distal splenorenal shunt better? Hepatology 1988; 8: 1705-7. 37. Henderson JM. Variceal bleeding: which shunt? Gastroenterology 1986; 91: 1021-3.
38. Hutson DG, Livingstone A, Levi JV, et al. Early hepatic failure or upper gastrointestinal ble,ding following a distal splenorenal shunt. Surg Gynecol Obstet 1982; 155: 46-8. 39. Vang J, Simert G, Hansson JA, et al. Results of a modified distal splenorenal shunt for portal hypertension. Am Surg 1977; 185: 224-8. 40. Maillard JN, Flamant YM, Hay JM, et al. Selectivity of the distal splenorenal shunt. Surgery 1979; 86: 663-71. 41. Henderson JM, Millikan WJ Jr, Wright-Bacon L, Kutner MH, Warren WD. Hemodynamic differences between alcoholic and nonalcoholic cirrhotics following distal splenorenal shunt: effect on survival? Ann Surg 1983; 198: 325-34. 42. Henderson JM, Millikan WJ Jr, Chipponi J, et al. The incidencr and natural history of thrombus in the portal vein following distal splenorenal shunt. Ann Surg 1982; 196: 1-7. 43. Widrich WC, Robbins AH, Johnson WC, et al. Long-term follow-up of distal splenorenal shunts: evaluation by arteriography, shuntography, transbepatic portal venography and cinefluorography. Radiology 1980; 134: 341-5. 44. Belghiti J, Grenier P, Nouel O, et al. Long-term loss of Warren's shunt selectivity. Angiographic demonstration. Arch Surg 1981; 116: 1121-4. 45. Rigau J, Teres J, Visa J, et al. Long-term follow-up of 100 patients with portal hypertension treated by a modified splenorenal shunt. B r J Surg 1986; 73: 708-11. 46. Katoh H, Shimozawa E, Kojima T, Tanabe T. Modified splenorenal shunt with splenopancreatic disconnection. Surgery 1989; 106: 920-4. 47. Nagasue N, Ogawa Y, Yukaya H, Hirose S. Modified distal splenorenal shunt with expanded polytetrafluoroethylene interposition. Surgery 1985; 98: 870-8. 48. Rudo ND, Johnson ND, Harris JP, et al. Assessment of a modified technique of distal splenorenal shunting. Surgery 1981; 90: 602-9. 49. Warren WD, Rudman D, Millikan W J, et al. The metabolic basis of portasystemic eneephalopathy and the effect of selective vs nonselective shunts. Ann Surg 1974; 180: 573-9. 50. Henderson JM, Warren WD. A method of quantitating hepatic function and hemodynamies in cirrhosis: the changes following distal splenorenal shunt. Jpn J Surg 1986; 16: 157-68.
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cess in which he viewed DSR_S not simply as an operation, but as a management concept. New information would change concepts, and new ideas would be tried and either accepted or discarded. Few therapies can have been so stringently tested by their innovator in an attempt to define their true role.
PATIENT EVALUATION In reaching a decision on how to treat the patient with variceal bleeding, two risks must be balanced: the risk of further bleeding and the risk of liver failure. Methods of evaluation have been presented in detail elsewhere in this issue [4]. In the context of selecting patients with DSRS, the key questions to be answered are: Does the patient need variceal decompression to control bleeding? Are the portal and systemic venous anatomy suitable for DSRS? Is the liver disease sufficiently good to sustain a reasonable period of quality life? In addressing these questions, the clinician is actually weighing the choice of DSRS against the other therapy choices of endoscopic sclerotherapy or liver transplantation in the patient who has bled from varices. r hen Dr. Warren came to Emory University in 1971, The first two questions are relatively easily answered. the distal splenorenal shunt (DSRS) had been Currently, most patients with bleeding esophageal varused for 5 years. The ability of this procedure to selective- ices are initially treated with sclerotherapy [5-7]. The ly decompress varices while maintaining portal hyperten- risk of rebleeding with sclerotherapy is approximately sion and portal flow was documented, and the initial 50%, and overall, sclerotherapy fails in about 25% to 30% clinical studies looked promising [1]. But this was only of patients who rebleed. Variceal decompression is needthe beginning. The next 18 years encompassed an in- ed in the patient in whom sclerotherapy has failed or in depth study of DSRS to define precisely its clinical, meta- the patient in whom the risk of rebleeding is considered bolic, and hemodynamic effects in patients with portal unacceptable. The anatomic suitability of candidates for hypertension and variceal bleeding. DSRS is defined by visceral angiography [8]. The splenic Prospective, randomized clinical trials compared vein is usually visualized on the venous phase of the splenDSRS with the total portal systemic shunt [2] and later ic artery injection, but occasionally splenoportography with endoscopic variceal sclerotherapy [3]. Both of these may be required. The left renal vein should be assessed by Emory studies were the first in a series of similar trials direct catheterization and phlebography; anomalies may conducted by other centers. However, apart from these increase the technical difficulty of DSRS [9]. randomized trials, the requirement has always been to The most complex issue to be addressed in making a fully evaluate and study all patients; each case has some- decision on suitability for DSRS is the state of the liver thing to teach the investigator. Such studies have taught [4]. The life expectancy of a patient with cirrhosis may be investigators much about the clinical outcomes of bleed- limited to days or extend to a normal span. The main ing control and survival and have yielded metabolic and factors contributing to this are the cause of the cirrhosis, hemodynamic data that have led to changes and improve- the activity of the process, the hepatocellular reserve, and ments in management methods. the systemic effects of the liver disease. Ideally, a candiThis review will summarize how the DSRS evolved date for DSRS should have stable disease with a reasonunder Dr. Warren. This was a continuing, dynamic pro- able hepatocyte reserve. This ideal cannot always be From the Department of Surgery and Clinical Research Facility, achieved, and compromise is sometimes required. EmoryUniversitySchoolof Medicine,Atlanta,Georgia.Supportedin part by GeneralClinicalResearchCenterPublicHealthServiceGrant OPERATIVE TECHNIQUES 5M01 RR 00039 from the National Institutes of Health, Bethesda, The technical goals of DSRS remain the same as Maryland. originally stated: selective reduction of pressure and volRequestsfor reprintsshouldbe addressedto J. MichaelHenderson, FRCS,DepartmentofSurgery,RoomF-511, 1364CliftonRoad,N.E., ume of flow through gastrcesophageal varices, mainteAtlanta, Georgia30322. nance of portal venous perfusion of the liver, and mainte-
W
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nance of continued venous hypertension in the intestinal bed [I]. Modification in how these goals are achieved has occurred in the past 20 years, with the acquisition of new knowledge and implementation of new techniques to overcome problems. The shunt: Dissection of the splenic vein out of the pancreas is the major technical facet of DSRS [10]. Full mobilization of the pancreas, from the superior mesenteric vessels to the splenic hilus, allows full caudad rotation of the pancreas and adequate visualization of the splenic vein. Dissection of the vein out of the pancreas entails dissecting directly on the vein, clearing the inferior and posterior surfaces before the superior and anterior surfaces, and accurately identifying and ligating the small pancreatic perforating tributaries. Isolation and mobilization of the left renal vein is aided by preoperative contrast evaluation. The shunt is fashioned by bringing the splenic vein down without tension or kinking to the antedor/superior surface of the left renal vein. Disconnection: This component of the operation is most important in achieving the goals of maintaining portal perfusion. While it was originally recognized that "portal azygos" disconnection was required as a component of DSRS, the initial emphasis was largely limited to ligation of the left gastric venous system [1]. This remains important, but extensive angiographic study [11] has shown that collateral pathways develop from the highpressure portal to low-pressure splenic vein through the pancreas, along the mesocolon, and as other transgastric collaterals. These are schematically illustrated in Figure 1. There are degrees of technical difficulty in achieving primary interruption of all these pathways at the time of DSRS [12]. The inferior mesenteric vein should always be ligated at its origin on the portal or splenic vein since it serves as an outflow from the hypertensive portal vein. The collaterals along the mesocolon are easily prevented by taking down the splenic flexure of the colon; this interrupts their final common path into the inferior ramus of the splenic vein. Meticulous dissection of the left gastric system should occlude its origin on the portal or splenic vein, and in addition, should ligate the vein and its tributaries on the lesser curve of the stomach and at the gastric esophageal junction. The right gastric vein should be ligated just superior to the pylorus. The most difficult collateral pathway to prevent is that through the pancreas, but data have shown that this siphon is most detrimental in loss of portal perfusion after standard DSRS, particularly in patients with alcoholic cirrhosis [11]. Completely dissecting the splenic vein entirely free from the pancreas will prevent development of this pathway [13]. This is shown conceptually in Figure 2. This addition to the disconnection component of DSRS has improved outcome in alcoholic patients. However, the additional technical hazard of possible splenic vein injury close to the hilus and subsequent loss of the shunt must be weighed by the operating surgeon in each individual case. RESULTS OF DSRS Control of variceal bleeding: Experience with DSRS at Emory in different trials and study groups has
Figure 1. The pathways of collateral developmentafter standard DSRS. Operative techniques to minimize this relentless collateralization are described in the text. (Reproduced with permission from [ 11].)
Figure 2. DSRS with entire splenopancreatic disconnection. Complete separation of the splenic vein from the pancreas prevents the developmentof the pancreatic siphon (Reproducedwith permission from [29] .)
shown control of variceal bleeding in 88% to 97% of patients [1,15-17]. The primary cause for rebleeding is shunt thrombosis, which occurs in 3% to 14% of patients [14-16]. An occluded shunt identified no more than 2 weeks after surgery may be corrected by reoperation. Late shunt thrombosis occurred in 2% or less of patients who were followed up by serial angiography [14,16]. Early rebleeding after DSRS may also occur with a patent shunt and inadequate varieeal decompression [17]. Variceal decompression by DSRS requires an adequate outflow through the short gastric veins, the splenic vein and shunt, and the left renal vein to the inferior vena cava.
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Development of an adequate outflow for completegastroesophageal decompression may take 4 to 6 weeks in some patients, making this the highest- risk time for rebleeding. Direct shunt catheterization and pressure measurement should be performed prior to hospital discharge and are the key diagnostic steps for upper gastrointestinal bleeding after shunt [17,18]. Data from 66 patients studied 1 to 2 weeks after DSRS showed a 7.8 mm Hg mean pressure gradient from the splenic vein to the vena cava [17]; however, 16 patients (24%) had a gradient more than 10 mm Hg, which suggests inadequate immediate decompression. Management of rebleeding with a patent shunt should be conservative, with vasopressin, tamponade, and/or sclerotherapy. The place of DSRS in the emergent setting of acute variceal bleeding not controlled by sclerotherapy, tamponade, or vasopressin has been controversial, the question being if adequate immediate decompression will be achieved by DSRS. The data cited previously suggest that 76% of patients have a rapid decrease in variceal pressure. However, in those who maintain some hypertension initially, the major gradient is from the renal vein to the vena cava. The alternative of splenocaval anastomosis should be considered in the emergent setting, particularly when the renal vein is small or abnormal or the spleen is large [19]. The clinical experience with emergent DSRS has shown control of variceal bleeding in 95% of patients, with mortality being related to the underlying liver disease [20]. Shunt stenosis can lead to variceal rebleeding at late follow-up. The risk of stenosis is greatest in patients with an abnormally thickened vein identified at the time of initial shunt and has been highest in our experience in patients with extrahepatic portal vein thrombosis [21]. The suspicion of stenosis is raised by late variceal rebleeding in a patient with a previously documented patent shunt. Diagnosis is made by shunt catheterization and the measurement of a gradient across the anastomosis. Management is by balloon dilation [22], Variceal bleeding control in other series has ranged from 73% to 95% [18,23-26]. In the randomized studies comparing DSRS with total shunts, bleeding control has been equivalent with both therapies in all but one series [23]. A uniform feature of the randomized studies comparing DSRS with endoscopic sclerotherapy has been the significantly better control of variceal bleeding with DSRS [3,27,28]. These factors are discussed in more detail elsewhere in this issue. Survival: Data on survival following DSRS at Emory have been generated in several different settings. The initial 10-year experience up to 198! with 348 patients undergoing DSRS showed an overall 5-year survival of 58% [14]. This was achieved in a population with 86% of patients in Child's class A and B and 56% of patients having alcoholic cirrhosis. The 5-year survival pattern was significantly (p <0.03) different between nonalcoholic (70%) compared with alcoholic (42%) patients. Data from the Emory randomized trial comparing DSRS with total shunt showed no significant difference in survival in Child's class A and B patients [2,15]. The 56
overall 10-year survival in the DSRS group was 41% whereas that in the total shunt group was 28%. In the nonalcoholic subset, 65% of patients were alive at 10 years in the DSRS group whereas only 29% of patients were alive in the total shunt group. Although these differences are not statistically significant, they reinforce the trends noted in the larger series [14]. The era of sclerotherapy at Emory resulted in a randomized trial comparing DSRS and sclerotherapy in a patient population with cirrhosis; 39% of patients were nonalcoholic, and 43% were in Child's class C. The 4-year survival after DSRS in this poorer-risk population was 43%. The differing survival pattern for alcoholic (35%) and nonalcoholic (54%) patients is again seen in this study group. Interestingly, there was no significant difference in survival in nonalcoholic patients in the two randomized groups between DSRS or endoscopic sclerotherapy. In contrast, there was a survival advantage (p <0.01) for alcoholic patients with cirrhosis randomized to sclerotherapy, provided surgical rescue was used for patients bleeding after sclerotherapy [16]. Finally, data from Emory studies show survival in alcoholic patients after DSRS appears to have improved with splenopancreatic disconnection [29]. In a nonrandomized, consecutive series of 78 patients undergoing DSRS with splenopancreatic disconnection, not only was portal perfusion better maintained in alcoholic patients than after standard DSRS, but survival was also improved. In 35 patients with alcoholic cirrhosis (40% in Child's class C), the 4-year survival was 60%. This improvement is shown in Figure 3, where the DSRS with splenopancreatic disconnection survival data is compared with standard DSRS survival data for patients with alcoholic and nonalcoholic cirrhosis. These data support the use of DSRS with splenopancreatic disconnection in patients with alcoholic cirrhosis. How do these data compare with other reported survival data for DSRS? The other randomized studies comparing DSRS with total shunts have shown no significant difference in survival between these therapies [2326,30]. These trials have been either exclusively or predominantly in alcoholic populations. The alcoholic versus nonalcoholic survival difference after DSRS was first documented by Zeppa and co-workers [31] in 1977, but has not been confirmed in other reported nonrandomized series [32-34]. The key questions in survival after variceal bleeding are: Will stopping the bleeding improve survival? Will the procedure used to stop the bleeding alter liver function in a positive or negative manner? What is the life expectancy of the patient, based on the underlying liver disease irrespective of bleeding? It is only by developing improved methods of classification and standardization between groups that meaningful comparison can be made in the analysis of survival data. Eneephalopathy: Hepatic encephalopathy is a complication of severe liver disease and may be either precipitated or spontaneous. In patients with variceal bleeding, it is a key marker of the severity of disease. In reaching a decision about the optimal therapy for a given patient, a history of recurrent encephalopathy suggests the need for
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1 9 8 2 A I c vs. N o n - A I c
AIc vs. N o n - A I c 1.0
"
.8
~
Non-AIc
/
.6 Figure 3. Kaplan-Meier survival curves for alcoholic and non-alcoholic patients after DSRS with splenopancreatic disconnection (left) and standard DSRS (right). There has been a significant impact on survival in alcoholic patients with the addition of splenopancreatic disconnection. AIc = alcoholic. (Reproduced with permission from [29] .)
AIc
.4
AIc
.2 0 I 10
30
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90
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transplantation and warns against shunt surgery. On the other hand, a history of no encephalopathy, taken in conjunction with data suggesting good hepatocyte function, suggests a role for decompressive shunt rather than transplantation. How does DSRS impinge on the natural history of encephalopathy in liver disease? The overall clinical experience at Emory suggests that DSRS does not accelerate the occurrence or worsen the severity of encephalopathy. Concerning the incidence of encephalopathy in a control, nonshunted population, the data from the Emory randomized study with endoscopic sclerotherapy showed a 12% incidence of encephalopathy after 2 years in a nonoperated group of 26 patients at risk for liver disease [3]. In the parallel group randomized to DSRS, the incidence of encephalopathy was not significantly different (16%) [3]. Data from the Emory randomized trial in patients with Child's A or B disease showed encephalopathy rates of 5% at 2 years [2], 12% at 3 to 6 years [35], and 27% at 10-year follow-up [15]. At all time intervals, this incidence was significantly lower than in patients randomized to total shunts and might represent the expected natural history for the evolution of encephalopathy in such a population. Other studies both in controlled trials and nonrandomized series have shown wide variability in the occurence of encephalopathy after DSRS [36,37]. A recurring theme has been the role of maintenance of portal flow and adequate portal/splenic dissociation in reducing the risk of encephalopathy [38-40]. The highest incidence of encephalopathy after DSRS has occurred in series in which no disconnection has been performed [39], or in which there has been no postoperative documentation of maintenance of portal perfusion [23,25]. Hemodynamie changes with DSRS: Creation of a DSRS provides a low-pressure, high-flow shunt in the left upper quadrant of the abdomen that reduces esophagogastric splenic variceal pressure and controls bleeding. The secondary aim is to maintain portal venous hypertension in the splanchnic bed and thereby maintain sufficient pressure to sustain portal flow through the high-resistance cirrhotic liver. How far is this secondary goal achieved? Data from Emory show that portal flow is maintained
in 90% of nonalcoholic patients but in only 25% to 50% of alcoholic patients over the long term after standard DSRS [11,41]. Portal venous hypertension, measured indirectly as corrected sinusoidal pressure, is sustained in both groups of patients [16]. The development of large siphoning transpancreatic collaterals [13] from the highpressure portal vein to the low-pressure splenic vein is particularly detrimental to loss of portal flow in alcoholic patients. The time frame for development of collaterals and maintenance or loss of portal perfusion appears to be the first 6 to 12 months after DSRS, with few patients having further loss of portal flow thereafter [11]. Dissection of the entire splenic vein out of the pancreas prevents development of this siphon and results in maintenance of portal flow in 84% of alcoholic cirrhotic patients [29]. The incidence of portal vein thrombosis after DSRS is 4% in our experience [42], but nonoccluding thrombus can occur in up to 20% of patients. Subsequent thickening and narrowing of the portal vein can occur, which may complicate subsequent transplantation. Systemic hemodynamic changes characterized by a high cardiac output or low total vascular resistance occur with chronic liver disease and portal hypertension. After DSRS, patients in whom portal perfusion is maintained have a similar systemic hemodynamic profile to their preoperative status. However, patients with loss of portal perfusion have an associated hyperdynamic systemic circulation [41]. It has yet to be resolved whether the hepatic or the systemic hemodynamic change is the primary event. Other studies have documented the development of collaterals after DSRS, which may or may not be associated with total loss of portal flow [40,43,44]. Maintained portal perfusion rates of 50% to 87% have been documented at late follow-up [27,34]. Evaluation of the hemodynamic changes, in an operation with specific hemodynamic goals, is of paramount importance. The plethora of modifications to DSRS in the literature often do not have the hemodynamic data to indicate if the underlying principles of DSRS have been achieved [45-48]. Such studies must be interpreted with caution, Metabolic changes with DSRS: The effect of DSRS on hepatic function has been quantitated at Emory over
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the past 20 years, largely through studies conducted at the Clinical Research Center and supported by grants from the National Institutes of Health. The initial studies focused on nitrogen metabolism, measuring ammonia tolerance, urea synthesis rates, and amino acid metabolism. The data showed maintenance of preoperative levels of function in patients after DSRS but a significant decrease after total shunts [49]. The parallel clinical development of encephalopathy in the group with poorer nitrogen metabolism was interpreted as providing a metabolic basis for their encephalopathy [49], Subsequent studies have documented the critical role of maintained portal perfusion in sustaining hepatic function after DSRS [35] and have quantitated the metabolic and hemodynamic changes serially after DSRS [50]. Patients with extrahepatic portal vein thrombosis as the cause of their variceal bleeding maintain both liver volume and hepatocyte function after DSRS [42]. DSRS IN T H E OVERALL MANAGEMENT OF VARICEAL B L E E D I N G A center that treats patients with variceal bleeding should offer the full range of therapies, which comprise pharmacotherapy, endoscopic sclerotherapy, decompressive shunt, and liver transplantation. The key is being able to select the right therapy for the right patient at the right time. DSRS should be one of these available treatments. We believe it is indicated as primary therapy for Child's A patients with nonalcoholic cirrhosis and patients with portal vein thrombosis, and as rescue therapy for sclerotherapy failure in patients with alcoholic cirrhosis who are at an acceptable risk and patients with nonalcoholic cirrhosis in whom transplantation is not indicated. CONCLUSIONS As we review the status of DSRS at Emory in 1990, the following points bear emphasis. First, the concept of selective variceal decompression holds true. Varices can be decompressed and bleeding controlled by selective transplenic shunt, while portal hypertension and perfusion can be maintained at the same time. Modifications of the original procedure have improved the ability to implement these goals. Second, some patients are best treated for their variceal bleeding by DSRS, In our experience, this occurs in about 30% of patients; the key is appropriate selection. Finally, the study of patients undergoing DSRS has taught us much about the hemodynamic and metabolic pathophysiology of portal hypertension. Dr. Warren's requirements to test hypotheses and generate data have, we believe, helped define the correct role of DSRS among the other therapies discussed in this issue. We are grateful to him for giving us the opportunity to be part of this evolution. REFERENCES 1. Warren WD, Zeppa R, Foman JS. Selectivetransplenic decompression of gastroesophageal varices by distal splenorenal shunt. Ann Surg 1967; 166: 437. 58
2. Galambos JT, Warren WD, Rudman D, et al. Selectiveand total shunts in the treatment of bleedingvarices:a randomized controlled trial. N Engl J Med 1976; 285: 1089-95. 3. Warren WD, Henderson JM, Millikan WJ, et al. Distal splenorenal shunt versus endoscopic sclerotherapy for long-term management of variceal bleeding. Ann Surg 1986; 203: 454-62. 4. Galambos JT. Evaluation of patients with portal hypertension. Am J Surg 1990; 160: 14-8. 5. Terblanche J. Has sclerotherapy altered the management of patients with variceal bleeding? Am J Surg 1990; 160: 37-42. 6, Westaby D, Williams R. Status of sclerotherapy for variceal bleeding in 1990. Am J Surg 1990; 160: 32-6. 7. Paquet K-J, Mercado MA, Gad HA. Surgical procedures for bleeding esophagogastric variceS when sclerotherapy fails: a prospective study. Am J Surg 1990; 160: 43-7. 8. Nordlinger BM, Nordlinger DF, Fulenwider JT, et al. Angiography in portal hypertension: clinical significance in surgery. Am J Surg 1980; 139: 132-41. 9. Sones PJ, Rude JC, Warren WD. Evaluation of the left renal vein in candidates for splenorenal shunts. Radiology 1978; 127: 357-61. 10. Warren WD, Millikan WJ. Selective transplenic decompression procedure: changes in technique after 300 cases. Contemp Surg 1981; 18: 1t-32. 11. Henderson JM, Gong-Liang J, Galloway J, Millikan WJ Jr, S0nes PJ, Warren WD. Portaprival collaterals following distal splenorenal shunt: incidence, magnitude and associated portal perfusion changes. J Hepatol 1985; 1: 649-61. 12. Warren WD, Millikan WJ, Henderson JM, et al. Splenopancreatic disconnection: improved selectivityof the distal splenorenal shunt. Ann Surg 1986; 204: 346-55. 13. Warren WD, Millikan WJ Jr, Henderson JM, Rasheed ME, Salam AA. Selective variceal decompression after splenectomyor splenic vein thrombosis with a note on splenopancreatic disconnection. Ann Surg 1984; 199: 694-702. 14. Warren WD, Millikan WJ, Henderson JM, et al. Ten years of portal hypertensivesurgery at Emory: results and new perspectives. Ann Surg 1982; 195: 530-42. 15. Millikan WJ, Warren WD, Henderson JM, et al. The Emory prospective randomized trial: selectiveversus nonselectiveshunt to control variceal bleeding. Ten-year follow-up.Ann Surg 1985; 201: 712-22. 16. Henderson JM, Kutner MH, Millikan WJ, et al. Endoscopic variceal sclerosiscompared with distal splenorenal shunt to prevent recurrent variceal bleeding in cirrhosis. Ann Intern Med 1990 (in press). 17. Richards WO, Pearson TC, Henderson JM, Millikan WJ, Warren WD. Evaluation and treatment of early hemorrhage of the alimentary tract after selective shunt procedures. Surg Gynecol Obstet 1987; 164: 530-6. 18. Eckhauser KFE, Pomerantz RA, Knol JA, Strode WE, Williams DM, Turcotte JG. Early variceal rebleeding after successful distal splenorenal shunt. Arch Surg 1986; 121: 547-52. 19. Atta HM, Henderson JM, Galloway JR, Millikan WJ. Selective splenocavalshunt: 24 cases and reviewof literature. Arch Surg 1990 (in press). 20. Ports JR III, Henderson JM, Millikan WJ Jr, Warren WD. Emergency distal splenorenal shunts for variceal hemorrhage refractory to non-operative control. Am J Surg 1984; 148: 813-6. 21. Warren WD, Henderson JM, Millikan WJ, et al. Management of variceal bleedingin patients with non-cirrhoticportal vein thrombosis. Ann Surg 1988; 207: 623-34. 22. Henderson JM, Khishen MA, Millikan WJ, Sones PJ, Warren WD. Management of stenosisof distal splenorenalshunt by balloon dilation. Surg Gynecol Obstet 1983; 157: 43-8. 23. Harley HA J, Morgan T, Redeker AG, et al. Results of a randomized trial of end-to-side portacaval shunt and distal splenorenal shunt in alcoholicliverdisease and variceal bleeding. Gastroenterology 1986; 91: 802-9.
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24. Langer B, Taylor BR, Mackenzie DR, et al. Further report of a prospective randomized trial comparing distal splenorenal shunt with end-to-sideportacaval shunt. Gastroenterology 1985; 88: 4249. 25. Grace ND, Corm HC, Resnick RH, et al. Distal splenorenal vs portal systemic shunts after hemorrhage from variees: a randomized controlled trial. Hepatology 1988; 8: 1475-81. 26. Fischer JE, Bower RH, Atamian S, et al. Comparison of distal and proximal splenorenal shunts. A randomized prospective trial. Ann Surg 1981; 194: 531-44. 27. Rikkers LF, Burner DA, Volentine GD, et al. Shunt surgery versus endoscopic sclerotberapy for long-term treatment of varieeal bleeding: early results of a randomized trial. Ann Surg 1987; 206: 261-71. 28. Teres J, Bordas JM, Bravo D, et al. Sclcrotberapy vs distal splenorenal shunt in the elective treatment of variceal hemorrhage: a randomized controlled trial. Hepatology 1987;7: 430-6. 29. Henderson JM, Warren WD, Millikan W J, Galloway JR, Kawasald S, Kutner MH. DiStal splenorenal shunt with splenopanoreatic disconnection: a four year assessment. Ann Surg 1989; 210: 332-41. 30. Reichle FA, Fahmy WE, Golsorkhi M. Prospective comparative clinical trial with distal splenorenal and mesoeaval shunts. Am J Surg 1979; 137: 13-21. 31. Zeppa R, Hensley GT, Levi JU, et al. The comparative survival of alcoholics versus non-alcoholics after distal splenorenal shunt. Ann Surg 1978; 187: 510. 32. Rikkers LF, Soper N J, Cormier RA. Selective operative approach for varieeal hemorrhage. Am J Surg 1984; 147: 89~96. 33. Arson MA, van Hoerden JA, Ilrup DM. The distal splenorcnal shunt. Arch Surg 1984; 119: 609-14. 34. Myburgh JA. Selective shunts: the Johannesburg experience. Am J Surg 1990; 160: 67-74. 35. Rikkers LF, Rudman D, Galambos JT, et al. A randomized, controlled trial of the distal splenorenal shunt. Ann Surg 1978; 188: 271-82. 36. Rikkers LF. Is the distal splenorenal shunt better? Hepatology 1988; 8: 1705-7. 37. Henderson JM. Variceal bleeding: which shunt? Gastroenterology 1986; 91: 1021-3.
38. Hutson DG, Livingstone A, Levi JV, et al. Early hepatic failure or upper gastrointestinal ble,ding following a distal splenorenal shunt. Surg Gynecol Obstet 1982; 155: 46-8. 39. Vang J, Simert G, Hansson JA, et al. Results of a modified distal splenorenal shunt for portal hypertension. Am Surg 1977; 185: 224-8. 40. Maillard JN, Flamant YM, Hay JM, et al. Selectivity of the distal splenorenal shunt. Surgery 1979; 86: 663-71. 41. Henderson JM, Millikan WJ Jr, Wright-Bacon L, Kutner MH, Warren WD. Hemodynamic differences between alcoholic and nonalcoholic cirrhotics following distal splenorenal shunt: effect on survival? Ann Surg 1983; 198: 325-34. 42. Henderson JM, Millikan WJ Jr, Chipponi J, et al. The incidencr and natural history of thrombus in the portal vein following distal splenorenal shunt. Ann Surg 1982; 196: 1-7. 43. Widrich WC, Robbins AH, Johnson WC, et al. Long-term follow-up of distal splenorenal shunts: evaluation by arteriography, shuntography, transbepatic portal venography and cinefluorography. Radiology 1980; 134: 341-5. 44. Belghiti J, Grenier P, Nouel O, et al. Long-term loss of Warren's shunt selectivity. Angiographic demonstration. Arch Surg 1981; 116: 1121-4. 45. Rigau J, Teres J, Visa J, et al. Long-term follow-up of 100 patients with portal hypertension treated by a modified splenorenal shunt. B r J Surg 1986; 73: 708-11. 46. Katoh H, Shimozawa E, Kojima T, Tanabe T. Modified splenorenal shunt with splenopancreatic disconnection. Surgery 1989; 106: 920-4. 47. Nagasue N, Ogawa Y, Yukaya H, Hirose S. Modified distal splenorenal shunt with expanded polytetrafluoroethylene interposition. Surgery 1985; 98: 870-8. 48. Rudo ND, Johnson ND, Harris JP, et al. Assessment of a modified technique of distal splenorenal shunting. Surgery 1981; 90: 602-9. 49. Warren WD, Rudman D, Millikan W J, et al. The metabolic basis of portasystemic eneephalopathy and the effect of selective vs nonselective shunts. Ann Surg 1974; 180: 573-9. 50. Henderson JM, Warren WD. A method of quantitating hepatic function and hemodynamies in cirrhosis: the changes following distal splenorenal shunt. Jpn J Surg 1986; 16: 157-68.
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