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Pancreatic head resection for chronic pancreatitis in patients with extrahepatic generalized portal hypertension
Pancreatic head resection for chronic pancreatitis in patients with extrahepatic generalized portal hypertension Ulrich Adam, MD, Frank Makowiec, MD, Hartwig Riediger, MD, Tobias Keck, MD, Jens C. Kro¨ger, MD, Peter Uhrmeister, MD, and Ulrich T. Hopt, MD, Freiburg and Rostock, Germany
Background. Five percent to 10% of chronic pancreatitis (CP) cases are complicated by portal venous occlusion leading to extrahepatic generalized portal hypertension (GPH). Pancreatic head resections (PHR) are regarded risky or contraindicated in patients with extrahepatic GPH. The aim of our study was to analyze the outcome of patients with extrahepatic GPH undergoing PHR for CP and to propose recommendations for surgical strategy. Methods. Sixteen of 185 patients with PHR suffered from extrahepatic GPH . Perioperative and follow-up data were documented prospectively and analyzed to assess the outcome. Results. Preoperative interventional thrombolysis of the portal vein was successfully performed in 5 patients and alleviated further PHR. Median operative time and blood transfusions were higher in patients with extrahepatic GPH compared with patients without extrahepatic GPH ( P < .01). Overall complication rate was not statistically different (44% vs 34%). One death occurred in each group. At the end of follow-up (median, 18 months) 13 of 15 patients with extrahepatic GPH were free of pain. No variceal bleeding or cholestasis was documented. All patients judged their status as subjectively improved. Conclusion. Although technically demanding in the presence of extrahepatic GPH, PHR can be performed with an acceptable morbidity and mortality in an experienced center. Preoperative interventional recanalization of portal vein thrombosis may render PHR possible by restoring normal splanchnic blood flow in selected cases indicated for surgery. (Surgery 2004;135:411-8.) From the Departments of Surgery and Radiology, University of Freiburg, Freiburg, Germany; and the Institute for Diagnostic and Interventional Radiology, University of Rostock, Rostock, Germany
CHRONIC PANCREATITIS (CP) is frequently characterized by an involvement of the portal venous system.1,2 Compression of the veins by pseudocysts or enlarged and fibrotic pancreatic tissue is a common factor leading to vascular occlusion.3 Surrounding inflammation leading to intimal changes in veins has also been reported to cause thrombosis.4 In older series, up to half of the patients with CP had splenic vein thrombosis, often accompanied by regional ‘‘left-sided’’ portal hypertension.5,6 In more recent series, however, splenic Parts of this manuscript were presented as a poster at the meeting ‘‘Progress in Pancreatology—20 years in and outside Ulm,’’ held in Ulm, Germany, September, 6-8, 2001, and were published as an abstract in Langenbeck’s Arch Surg 2001; 386:392. Accepted for publication August 18, 2003. Reprint requests: Ulrich Adam, MD, Department of Surgery, University of Freiburg, Hugstetter Strasse 55, D-79106 Freiburg, Germany. 0039-6060/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.surg.2003.08.021
vein thrombosis was present in approximately 10% of the patients only.1,7-9 In contrast to the more frequent splenic vein occlusion, portal and-or mesenteric vein occlusion has been reported with an incidence of 5% in a large follow-up series.1 Portal vein occlusion and superior mesenteric vein occlusion, as well as subtotal stenosis of those vessels, may lead to extrahepatic generalized portal hypertension (GPH) in the absence of liver cirrhosis. Portal vein occlusion and the presence of extrahepatic GPH are often regarded as a contraindication or a great endeavor for a pancreatic head resection (PHR). Portal and mesenteric vein occlusion have been identified as important risk factors for pancreatic resection.1,8,10,11 Some younger patients with CP, however, present with urgent indications for surgery, even in the presence of extrahepatic GPH. One option to reduce the perioperative risk might be decompression of the portal vein with subsequent resolution of vascular occlusion and portal hypertension. Few data are reported on pancreatic surgery in patients with extrahepatic GPH,1,8,10-13 and only SURGERY 411
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Table I. Basic patient characteristics and type of surgery in 185 patients with CP undergoing PHR GPH
P
No GPH
n 16 169 Male 88% 84% Age (y) (median and 39.8 (34-62) 42.7 (26-77) range) Duration of CP, (mo) 34 (3-180) 36 (1-148) (median and range) Etiology Alcohol 81.3% 75.1% Biliary — 1,8% Other 18.8% 23.1% Preoperative diabetes 43.8% 30.8% Preoperative jaundice 62.5% 24.3% Biliary drainage 43.8% 22.5% Pseudocysts 75% 61.5% Infected pseudocysts — 3.6% Type of surgery Whipple 2 21 PPPD 4 85 DPPHR 10 63 Beger 4 29 Frey 6 34
NS NS
NS NS NS NS .002 .06 NS
CP, Chronic pancreatitis; PHR, pancreatic head resection; GPH, generalized portal hypertension; PPPD, pylorus-preserving pancreatoduodenectomy; DPPHR, duodenum-preserving pancreatic head resection.
a few PHRs performed under these challenging conditions have been described.1,10,12 The aim of our study was to analyze our experience with PHRs in the presence of extrahepatic GPH in a large number of patients with CP and to describe our surgical strategy developed successively in dealing with this problem. During the study period, we started to use an interventional method to recanalize the occluded superior mesenteric and portal veins preoperatively to decrease portal hypertension, which allowed or facilitated subsequent PHR with complete transection of the pancreatic neck. PATIENTS AND METHODS From July 1994 to August 2002, 231 primary operations were performed electively in patients with CP. The principal perioperative data were prospectively documented in a computerized database. Additional data necessary for our analysis were obtained from the complete inhospital charts. Twenty-one patients were identified to have extrahepatic GPH due to portal vein occlusion (n = 15), high-grade stenosis of the portal vein (n = 4), or high-grade stenosis of the splenic and portalsuperior mesenteric veins (n = 2).
Only patients undergoing PHR (n = 185) were considered for this study. Sixteen of those 185 (8.6%) patients had extrahepatic GPH (GPH group), whereas the remaining pre- and intraoperative 169 patients (91.4%) had no signs of GPH (no-GPH group). Five of the 21 patients with extrahepatic GPH did not undergo PHR. These patients presented with limited disease. In 3 cases, solitary pseudocysts with gastric outlet obstruction were present, and pseudocystojejunostomy was performed. In 1 case, where we performed a hepaticojejunostomy, jaundice was the only symptom. A preoperative biliodigestive anastomosis was already planned because of known extrahepatic GPH in 4 of the 5 patients. In the fifth patient, the operation was switched intraoperatively from a planned PHR to a pseudocystojejunostomy due to severe bleeding during preparation. Basic demographic and disease-related data of the 185 study patients are shown in Table I. It is of note that 10 of 16 patients with portal hypertension had jaundice due to high-grade stenosis of the distal common bile duct. Preoperative biliary drainage was performed more frequently in these patients compared with patients without portal hypertension. Further indications or coindications for surgery in the 16 patients with extrahepatic GPH were intractable pain (n = 9), gastric outlet obstruction (n = 2), gastrointestinal bleeding from an aneurysm of inferior pancreatoduodenal artery (n = 1), and a pancreatopleural fistula (n = 1). The last postoperative follow-up of the 15 patients with portal hypertension who survived PHR was obtained during outpatient visits (n = 10) or by telephone contact with the patients and their home physicians (n = 5). Diagnosis of portal hypertension. Preoperative workup of the 185 patients before elective PHR included computed tomography scan (96%), visceral angiography (94%), and/or magnetic resonance angiography (11%). Radiologic signs of extrahepatic GPH were total or subtotal occlusion of the portal-superior mesenteric vein combined with an extensive net of collateral veins, localized mainly around the duodenum and pancreatic head. In all cases, except 1, portovenous thrombosis and portal hypertension were correctly diagnosed preoperatively by visceral angiography. In this 1 case, the portovenous system was free of obstruction during preoperative workup by angiography, endosonography, and computed tomography scan. This patient most likely developed portal vein thrombosis in the time period between diagnostic workup and surgery.
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During preoperative workup, all 16 patients with portal hypertension received upper gastrointestinal endoscopy. Gastric fundus varices were found in 3 patients, and esophageal varices in 1 patient. The patient with esophageal varices was the only one with a history of variceal bleeding. Despite portal hypertension, none of the 16 patients had ascites intraoperatively. Interventional recanalization of the portal vein. Interventional recanalization of the occluded portal vein was performed in 6 patients to reduce portal blood pressure perioperatively by restoring the normal mesenteric-portal route, thereby making transsection of the pancreatic neck possible. Following catheterization of the right hepatic vein via the right jugular vein, cannulation of the right main branch of the portal vein was performed. Subsequently an 8 F introducer was placed into the portal vein for atraumatic catheterization of the thrombosed portal-superior mesenteric vein. The thrombus was fragmented using an 8 F Amplatz (Bard Peripheral Vascular, Inc - Interventional, Tempe, Ariz) or an 8 F Oasis (Boston Scientific International, Natick, Mass) thrombectomy catheter in pull-back technique. After restoration of the liver-directed blood flow, a 4 F catheter was inserted into the superior mesenteric vein for local thrombolysis. Thrombolysis was performed by application of a bolus of 5 mg recombinant tissue plasminogen activator (rTPA) and subsequent local infusion of 2-5 mg/h rTPA for 12 hours, accompanied by intravenous heparin at 600-800 IU/h. The number of thrombolysis cycles was 1 to 4, depending on localization, size, and age of the thrombus. Smaller thrombi that were washed out into the liver by restored portal blood flow were thrombolysed by direct local intervention with lower doses of rTPA. Basket catheters mechanically minced older thrombi that were not accessible for thrombolysis. Fragments were removed via the introducer. With this technique, thrombi up to 25 cm in length were removed in our patients. After reconstruction of orthograd flow in the mesenteric-portal vein and removal of thrombi from these vessels, a 4 F catheter was inserted in the superior mesenteric vein for local heparin application until operation. All operations were performed 1 to 2 days after recanalization. Surgery and perioperative management. The different types of PHRs performed are shown in Table I. In our series, patients with preoperative GPH were statistically more likely to receive duodenumpreserving head resection (63% of the 16 patients) compared with those patients without GPH (38%
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duodenum-preserving head resections in 169 patients; P = .05). We performed more duodenumpreserving head resections during the second part of the study period in all patients with CP. Since most of the patients with extrahepatic GPH underwent operation in the second part of the study period, the higher frequency of duodenum-preserving resections in this subgroup may partially reflect the overall trend in our surgical management. After resection of the pancreatic head, the remaining pancreatic duct in the pancreatic remnant was carefully cannulated to exclude stenosis. Pancreatic duct stones, if present, were removed after head resection. For reconstruction, a pancreatojejunostomy was carried out in all patients. In cases involving classic Whipple operation, pylorus-preserving pancreatoduodenectomy (PPPD), and duodenum-preserving PHR according to Beger, our preferred technique was pancreatodigestive anastomosis to the pancreatic remnant, consisting of an end-to-side, single-layer, full-thickness anastomosis using interrupted polydioxanone sutures. In cases involving duodenumpreserving pancreatectomy according to Frey, the anastomosis between the remaining pancreatic tissue and the jejunal loop was created by using running polydioxanone sutures. Hepaticojejunostomy during Whipple or PPPD was also created with interrupted polydioxanone sutures. A biliodigestive anastomosis was performed in 21 (33%) of the 63 DPPHR in patients without extrahepatic GPH and in 5 of 10 DPPHR (50%) of those with GPH. All patients received perioperative antibiotic coverage, which was prolonged to the first 3 postoperative days in cases involving preoperative biliary drainage or intraoperative infection (eg, infected pseudocysts). Octreotide 100 lg 3 times a day for 7 days was started intraoperatively and continued postoperatively subcutaneously in 96% of the patients. Postoperatively, all patients were treated at least for 1night at our surgical intensive care unit. Definitions and statistics. Delayed gastric emptying was defined as inability to eat a regular diet beyond day 10 postoperatively. The groups of patients with and without portal hypertension were compared by using the chi-square test, MannWhitney test, or U-test, as applicable. All analyses were performed with the statistical software SPSS (release 10, SPSS Inc, Chicago, Ill). RESULTS Preoperative recanalization of portal vein occlusion. After 1998, 6 patients preoperatively had interventional transhepatic catheter thrombolysis
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Table II. Outcome of PHRs performed in patients with GPH and in patients without generalized portal hypertension GPH
No GPH
n 16 169 Duration of surgery 533 (240-870) 420 (220-740)* (min) (median and range) Blood transfusion 9.3 (0-32) 4 (0-36)* (units) (median and range) Postoperative hospital 16 (10-41) 14 (8-61) stay (d) (median and range)y Death (n)(%) 1 (63%) 1 (0.6%) Complications (n) 7 (43.8%) 57 (33.7%) Pancreatic leakage 0 15 (8.9%) Biliary leakage 0 1 (0.6%) Abdominal bleeding 2 (12.5%) 3 (1.8%)z Gastrointestinal 1 (6.3%) 2 (1.2%) bleeding 3 (20%) 16 (9.5%) Delayed gastric emptyingyz Abdominal abscess 1 (6.3%) 7 (4.1%) Pneumonia 2 (12.5%) 12 (7.1%) Infected drain fluid 0 6 (3.7%) without abscess Wound infection 2 (12.5%) 11 (6.5%) Relaparotomies (n) 1 (8.3%) 9 (5.5%) (%) PHR, Pancreatic head resections; GPH, generalized portal hypertension. *P < .01. y2 deaths excluded, 1 in each group. zP = .06.
of portal vein thrombosis by interventional radiologists. The lysis of the thrombosed portal vein was successful (reestablished blood flow in the superior mesenteric-portal vein at the end of the recanalization procedure) in 5 patients who subsequently underwent PHR (2 PPPD, 1 classical Whipple, and 2 Beger-DPPHR). One of those 5 patients, however, redeveloped portal vein thrombosis detected during laparotomy and underwent operative thrombectomy during PHR. Three of the 6 patients developed interventionassociated complications. One woman had intraabdominal bleeding at the end of the lysis period, which stopped after discontinuing the lysis. One patient had a hemobilia caused by a fistula from an intrahepatic artery to a bile duct that became symptomatic on day 4 after PHR by gastrointestinal bleeding. This complication could be treated successfully by interventional embolization of the arterial branch. Another patient (in whom the recanalization had failed) developed an intrahepatic hematoma treated conservatively.
Despite successful preoperative recanalization, all 5 patients intraoperatively presented with signs of relevant portal hypertension, but the pancreatic body could successfully be transected above the superior mesenteric-portovenous route. Normal venous splanchnic blood flow was thus restored following transection, and thereby the mechanical compression of the veins was alleviated. None of the 5 patients died postoperatively. The sixth patient, in whom preoperative recanalization had failed, received a Frey-DPPHR. At the time of hospital discharge, the portal vein had rethrombosed completely in 1 patient and partially in a second one, as shown by duplex ultrasound. An orthograd flow in the superior mesenteric and portal veins could be documented by duplex ultrasound in all patients. Intraoperative problems with GPH and change of surgical tactic (n = 16). Intraoperative bleeding problems by portal hypertension were documented in 11 of the 16 (69%) patients with extrahepatic GPH who underwent PHR. During 5 of the operations in which PPPD or Beger’s operation was initially planned, portal hypertension led to a change of the surgical strategy and Frey’s operation was performed. None of those 5 patients had undergone preoperative recanalization. As demonstrated in Table II, duration of surgery and the number of intraoperatively transfused units of packed red cells were significantly higher in the GPH group compared to the no-GPH group. In 1 patient, intraoperative bleeding could only be controlled by packing, although the patient had an emergent portocaval anastomosis after a classic Whipple resection of the pancreatic head. As mentioned previously, this was the only patient whose preoperative diagnosis did not show portal vein occlusion. Postoperative complications (all patients). Among the 185 patients, there were 2 postoperative deaths (1.1%): 1 in the extrahepatic GPH group (6.3 %) and 1 in the no-GPH group (0.6%; P = NS). Postoperative complications occurred in 44 % of patients with portal hypertension and in 34 % of patients without portal hypertension (Table II). The rate of postoperative abdominal bleeding was the only sole complication that was notably more frequent in patients with portal hypertension, although it just failed statistical significance (12.5% vs 2% in patients without portal hypertension; P < .06). It is also of note that none of the patients with portal hypertension developed a pancreatic leakage. The relaparotomy rate was comparable in both groups. Although delayed gastric emptying
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was more frequent in the GPH group (20% vs 9.5% in the no-GPH group), this difference did not reach statistical difference (P = .2). The median postoperative length of stay was slightly higher in patients with portal hypertension. However, this value did not reach statistical significance. Postoperative follow-up of 15 patients with portal hypertension. Long-term postoperative follow-up was obtained in all 15 patients with portal hypertension surviving PHR (median follow-up, 18 months; range, 3-61 months). None of these 15 patients developed variceal bleeding, but 1 patient had bleeding into a recurrent pseudocyst 18 months after initial surgery, which was managed conservatively. Except for 1 repair of an incisional hernia, no reoperation had to be performed. Thirteen of 15 patients did not complain about abdominal pain; the other 2 patients had moderate abdominal pain, approximately once per month, that required oral analgesics. The result of the operation was subjectively judged as ‘‘good’’ or ‘‘very good’’ by all 15 patients. No jaundice or other signs of cholestasis occurred postoperatively. DISCUSSION Extrahepatic GPH by total or subtotal occlusion of the splenoportal system is a well-known complication in CP. The incidence of splenic vein obstruction ranges from 2 % to 45 %,1, 5, 14, 15 whereas portal and/or mesenteric vein obstruction has been reported to occur in about 5%-10 % of patients.1,10,12 In our experience with 231 patients who underwent operation for CP, 37% had alterations of the portovenous system. Twenty-one percent of the patients had splenic vein thrombosis. Extrahepatic GPH was found in 9% of all 231 patients with CP who underwent an operation and in 9% of the 185 patients who received PHR. The presence of splenic, mesenteric, and /or portal vein occlusion as a complication of CP per se is not an indication for surgery.8,10,12 Gastrointestinal bleeding from esophageal, gastric, or duodenal varices, which may develop in the context of regional or GPH is a rare complication.1,12 In a prospective longitudinal series, the incidence of splenoportal obstruction was reported to be 13 % in 266 patients; the occurrence of gastrointestinal varices and variceal bleeding, however, was only 2 % and 0.5 %, respectively.1 In a recently published cohort of patients with PHR for CP, an incidence of 23 % for regional or extrahepatic GPH and 3 % for varices was reported. However, no bleeding was observed in this series.12 These results are also
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confirmed by our data. Of the 21 patients with extrahepatic GPH, only 1 had a history of bleeding from varices. The 2 patients in the GPH group with gastrointestinal bleeding as the main indication for pancreatic surgery did not present with variceal bleeding; they presented with bleeding from an aneurysm of the inferior pancreatoduodenal artery and common hepatic artery, respectively. Patients with occlusion of the splenoportal system, however, do sometimes require surgery for other complications of CP. In these cases, surgical strategy depends on the type of portal hypertension (ie, generalized or left-sided). In patients with left-sided portal hypertension and signs of fundus varices, splenectomy is the treatment of choice.7,15-18 Even though splenectomy in CP and left-sided portal hypertension is technically more demanding than in other indications (eg, hematological diseases or trauma), it can safely be added to any kind of pancreatic surgery, whether it is a resection or a drainage procedure. In contrast to left-sided portal hypertension, extrahepatic GPH caused by total or subtotal occlusion of the superior mesenteric-portal vein is by far more difficult to handle during surgery. This type of occlusion leads to an extensive net of collateral veins surrounding the pancreatic head (Fig 1) and can proceed to cavernous transformation in the hepatoduodenal ligament. In this situation, any kind of operation on the pancreatic head can cause relevant bleeding. PHR, therefore, is regarded as too risky in this situation by most surgeons. Surgical intervention due to various symptoms related to portal vein occlusion, however, might be necessary in these patients. Compression and subsequent obstruction of the superior mesenteric and/or portal vein seems to be an indicator of an advanced stage of CP, with a relatively large pancreatic mass and/or advanced fibrosis of the pancreatic head in many cases. Therefore, these patients more often present with other local complications of CP such as common bile duct or gastric outlet obstruction. In a recently published surgical study of 154 patients requiring surgery for CP, it was evident that patients with extrahepatic portal hypertension had a higher prevalence of common bile duct stenosis and segmental duodenal stenosis at the time of surgery.12 Similar findings were seen in our series, in which the rate of common bile duct obstruction in the GPH group was significantly higher than in the no-GPH group. Both the elevated probability of perioperative complications and an increased risk of surgical interventions in the presence of extrahepatic GPH dictate that surgery is indicated only in the
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Fig 1. Magnetic resonance angiography (portovenous phase) in a patient with extrahepatic GPH. Occlusion of the splenic, superior mesenteric, and peripheral portal veins led to the development of extended collaterals.
presence of severe complications of CP and not for extrahepatic GPH per se.10 There are few data regarding the surgical strategy in patients with CP complicated by GPH. In a study of 14 patients with superior mesentericportal vein obstruction, Warshaw and coworkers10 reported on 40 operations for complications of CP. Most of the interventions were drainage procedures and focused on limited symptomatic surgical therapy. Only 1 pancreatoduodenectomy was performed in this series. However, in a prospective randomized trial evaluating nonocclusive segmental portal hypertension due to CP, it was demonstrated that resection—but not drainage—was able to restore normal splanchnic blood flow.13 Patients in the resection group (n = 16) in this series underwent duodenum-preserving resection of the head of the pancreas as originally described by Beger,19 whereas patients in the drainage group (n = 14) underwent a modified procedure introduced by Frey and Smith.20 Decompression of the portal venous system after PHR was also demonstrated by Ruzicka et al21 in 17 patients with CP who underwent PHR. The intraoperative transection of the pancreas above the mesenteric-portal vein during the Beger procedure causes a marked release of the encased vessels. The same effect also can be achieved by
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either the pylorus-preserving PHR (PPPD) or the classic Whipple operation. In addition to treating local and general complications of CP (eg, common bile duct obstruction, duodenal obstruction, main pancreatic duct obstruction, inflammatory tumor of the pancreatic head, pain or recurrent episodes of inflammation), these operations may solve the problem of extrahepatic portal hypertension and its late complications. Risks of bleeding complications dictate that transsection of the pancreas can be recommended only when a nonocclusive portal hypertension exists. Whereas subtotal stenosis of the portal vein or superior mesenteric vein is common and leads to extrahepatic GPH in only a small percentage of cases, complete thrombotic obstruction of the portal vein leads obligatory to extrahepatic GPH. Exposure of the superior mesenteric-portal vein at the level of the pancreatic neck and subsequent transection of the pancreas above these veins is technically demanding and the most hazardous part of the whole operation.11 Complete transection of the pancreatic neck and extensive resection of the pancreatic head seem to be contraindicated when the superior mesenteric-portal vein is totally occluded. In this case, a PHR would result in a substantial reduction of the collateral circuit, leading to a potentially uncontrollable increase of venous pressure and consecutive bleeding. Facing this therapeutic dilemma, we established an interventional approach to preoperatively reopen an already-occluded portal and/or mesenteric vein in cooperation with our interventional radiologists (Fig 2). In addition to the 6 patients with nonocclusive extrahepatic GPH due to subtotal vein stenosis, we were able to transfer 5 more patients from an initially occlusive to a nonocclusive form of portal hypertension. Of these 11 patients, the pancreas was transected over the mesentericoportal axis in 9 patients who received a resection of the pancreatic head. One Whipple operation, 4 PPPDs, and 4 Beger operations were performed. Two of the first patients in this series received a Frey operation even though they had only subtotal stenosis of the portovenous system. During the years after establishment of the interventional approach, we established a standardized workflow in which all patients with extrahepatic GPH requiring PHR are treated. Our decision tree is shown in Figure 3. We try to preoperatively reopen the route of the superior mesenteric-portal vein to enable subsequent transection of the pancreatic neck. In addition to the salvage of extrahepatic GPH, PHRs (Beger procedure, Whipple operation, PPPD) also provide the prospect for a long patent
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Fig 2. A, Angiographic image of portal vein occlusion before recanalization. B, Procedure of recanalization of the portal vein; the angiography catheter passes through the still-occluded vein before lysis. C, Control angiography after successful lysis now demonstrates an open portal vein.
biliodigestive anastomoses because a mucosa-tomucosa anastomosis can be performed. Because common bile duct obstruction is frequent in the presence of extrahepatic GPH, the patency of biliodigestive anastomoses could be an important cofactor regarding the long-term results. Even though the 2 collectives—receiving recanalization or not receiving recanalization—are not comparable in terms of preoperative situation and of the extent of the performed operation, we compared the amount of perioperative blood transfusions and found no significant difference (10.7 units of packed red cells in patients with recanalization vs 8 units in patients without recanalization; P = .8). In 5 patients, the superior mesenteric and portal veins were still occluded at the time of operation. A limited resection of the pancreatic head according to Frey was performed in 4 of these patients. In 2 of these 4 cases, the Frey operation was combined with a Y-Roux side-to-side hepaticojejunostomy. We judge this approach as reasonable, because it can prevent major bleeding in the situation of cavernous transformation in the hepatoduodenal ligament. In contrast to the otherwise common end-to-side technique of hepaticojejunostomy, this side-to-side anastomosis can be performed without circumferential dissection of the common bile duct and the surrounding collateral veins. This approach again allows a mucosa-to-mucosa anastomosis in contrast to performing an incision of the common bile duct on the fibrotic dorsal wall of the Frey-resection cavity and draining bile into this pancreatic cavity, as described by others.11 The patient in whom preoperative diagnostic workup failed to show occlusion of the superior mesenteric-portal vein and who finally died after
Fig 3. Proposed algorithm for patients with surgically treatable complications of CP in the presence of GPH.
classic Whipple operation and an emergent portocaval shunt was the first patient in our series of PHR in the presence of extrahepatic GPH. This fatal outcome prompted us to specific therapeutic strategies and again underlines the importance of a reliable and recent preoperative imaging of the portal venous system with differentiation between total and subtotal occlusion. Our results demonstrate that PHR in patients with extrahepatic GPH is technically demanding and time consuming, and carries the risk of an increased intraoperative bleeding. However, we could show that postoperative morbidity and mortality remain in an acceptable range. The preoperative knowledge of extrahepatic GPH followed by a differentiated surgical approach enabled us to perform 15 consecutive PHRs without mortality in patients with GPH. Although postoperative complications occurred slightly more frequently in patients with portal hypertension than in patients without portal
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hypertension, the 44 % overall morbidity is in the range of overall complication rates of recent reports on pancreatoduodenectomy from other large centers.22-25 To our knowledge, this is the largest series of PHRs in patients with CP complicated by GPH. We can report for the first time on a systematic approach that includes preoperative superior mesenteric-portal vein recanalization. With this approach, PHRs in CP complicated by GPH can be performed with outcomes similar to PHRs in other series. REFERENCES 1. Bernades P, Baetz A, Levy P, Belghiti J, Menu Y, Fekete F. Splenic and portal venous obstruction in chronic pancreatitis. A prospective longitudinal study of a medical-surgical series of 266 patients. Dig Dis Sci 1992;37:340-6. 2. Seiler CA, Boss MA, Czerniak A, Berne TV, Blumgart LH. Vascular complications in chronic pancreatitis. Dig Surg 1997;14:107-12. 3. Rattner DW, Warshaw AL. Venous, biliary, and duodenal obstruction in chronic pancreatitis. Hepatogastroenterology 1990;37:301-6. 4. Kaiser G, Hommel G. Morphometrisch-statistische Analyse der Pankreasarterien bei Chronischer Pankreatitis. Virchows Arch A Pathol Anat 1975;365:103-18. 5. Leger L, Lenriot JP, Lemaigre G. Hypertension and segmental portal stasis in chronic pancreatitis. Apropos of 126 cases examined by splenoportography and splenomanometry. J Chir (Paris) 1968;95:599-608. 6. Rignault D, Mine J, Moine D. Splenoportographic changes in chronic pancreatitis. Surgery 1968;63:571-5. 7. Sakorafas GH, Sarr MG, Farley DR, Farnell MB. The significance of sinistral portal hypertension complicating chronic pancreatitis. Am J Surg 2000;179:129-33. 8. Seiler CA, Friess H, Buchler M. Thrombosis of the portal and splenic vein. In: Beger HG, editor. The Pancreas. 1st ed. Oxford: Blackwell Science Ltd; 2000. p. 854-62. 9. Mariethoz S, Savioz D, Buhler L, Becker C, Morel P. Splenic vein thrombosis and chronic pancreatitis: therapeutic approach. Schweiz Med Wochenschr 1998;128:867-70. 10. Warshaw AL, Jin GL, Ottinger LW. Recognition and clinical implications of mesenteric and portal vein obstruction in chronic pancreatitis. Arch Surg 1987;122:410-5. 11. Gloor B, Friess H, Uhl W, Buchler MW. A modified technique of the Beger and Frey procedure in patients with chronic pancreatitis. Dig Surg 2001;18:21-5.
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12. Izbicki JR, Yekebas EF, Strate T, Eisenberger CF, Hosch SB, Steffani K, et al. Extrahepatic portal hypertension in chronic pancreatitis: an old problem revisited. Ann Surg 2002;236:82-9. 13. Bloechle C, Busch C, Tesch C, Nicolas V, Binmoeller KF, Soehendra N, et al. Prospective randomized study of drainage and resection on non-occlusive segmental portal hypertension in chronic pancreatitis. Br J Surg 1997;84: 477-82. 14. Bradley EL. Complications of chronic pancreatitis. Surg Clin North Am 1989;69:481-97. 15. Madsen MS, Petersen TH, Sommer H. Segmental portal hypertension. Ann Surg 1986;204:72-7. 16. Little AG, Moossa AR. Gastrointestinal hemorrhage from left-sided portal hypertension. An unappreciated complication of pancreatitis. Am J Surg 1981;141:153-8. 17. Malka D, Hammel P, Levy P, Sauvanet A, Ruszniewski P, Belghiti J, et al. Splenic complications in chronic pancreatitis: prevalence and risk factors in a medical-surgical series of 500 patients. Br J Surg 1998;85:1645-9. 18. Evans GR, Yellin AE, Weaver FA, Stain SC. Sinistral (leftsided) portal hypertension. Am Surg 1990;56:758-63. 19. Beger HG, Krautzberger W, Bittner R, Buchler M, Limmer J. Duodenum-preserving resection of the head of the pancreas in patients with severe chronic pancreatitis. Surgery 1985;97:467-73. 20. Frey CF, Smith GJ. Description and rationale of a new operation for chronic pancreatitis. Pancreas 1987;2: 701-7. 21. Ruzicka M, Konecna D, Jordankova E. Portal hypertension as a complication of chronic pancreatitis. Hepatogastroenterology 1999;46:2582-4. 22. Povoski SP, Karpeh MSJ, Conlon KC, Blumgart LH, Brennan MF. Association of preoperative biliary drainage with postoperative outcome following pancreaticoduodenectomy. Ann Surg 1999;230:131-42. 23. Sohn TA, Yeo CJ, Cameron JL, Koniaris L, Kaushal S, Abrams RA, et al. Resected adenocarcinoma of the pancreas—616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 2000;4:567-79. 24. Buchler MW, Friess H, Wagner M, Kulli C, Wagener V, ZÕGraggen K. Pancreatic fistula after pancreatic head resection. Br J Surg 2000;87:883-9. 25. Gouma DJ, van Geenen RC, van Gulik TM, de Haan RJ, de Wit LT, Busch OR, et al. Rates of complications and death after pancreaticoduodenectomy: risk factors and the impact of hospital volume. Ann Surg 2000;232: 786-95.
Background. Five percent to 10% of chronic pancreatitis (CP) cases are complicated by portal venous occlusion leading to extrahepatic generalized portal hypertension (GPH). Pancreatic head resections (PHR) are regarded risky or contraindicated in patients with extrahepatic GPH. The aim of our study was to analyze the outcome of patients with extrahepatic GPH undergoing PHR for CP and to propose recommendations for surgical strategy. Methods. Sixteen of 185 patients with PHR suffered from extrahepatic GPH . Perioperative and follow-up data were documented prospectively and analyzed to assess the outcome. Results. Preoperative interventional thrombolysis of the portal vein was successfully performed in 5 patients and alleviated further PHR. Median operative time and blood transfusions were higher in patients with extrahepatic GPH compared with patients without extrahepatic GPH ( P < .01). Overall complication rate was not statistically different (44% vs 34%). One death occurred in each group. At the end of follow-up (median, 18 months) 13 of 15 patients with extrahepatic GPH were free of pain. No variceal bleeding or cholestasis was documented. All patients judged their status as subjectively improved. Conclusion. Although technically demanding in the presence of extrahepatic GPH, PHR can be performed with an acceptable morbidity and mortality in an experienced center. Preoperative interventional recanalization of portal vein thrombosis may render PHR possible by restoring normal splanchnic blood flow in selected cases indicated for surgery. (Surgery 2004;135:411-8.) From the Departments of Surgery and Radiology, University of Freiburg, Freiburg, Germany; and the Institute for Diagnostic and Interventional Radiology, University of Rostock, Rostock, Germany
CHRONIC PANCREATITIS (CP) is frequently characterized by an involvement of the portal venous system.1,2 Compression of the veins by pseudocysts or enlarged and fibrotic pancreatic tissue is a common factor leading to vascular occlusion.3 Surrounding inflammation leading to intimal changes in veins has also been reported to cause thrombosis.4 In older series, up to half of the patients with CP had splenic vein thrombosis, often accompanied by regional ‘‘left-sided’’ portal hypertension.5,6 In more recent series, however, splenic Parts of this manuscript were presented as a poster at the meeting ‘‘Progress in Pancreatology—20 years in and outside Ulm,’’ held in Ulm, Germany, September, 6-8, 2001, and were published as an abstract in Langenbeck’s Arch Surg 2001; 386:392. Accepted for publication August 18, 2003. Reprint requests: Ulrich Adam, MD, Department of Surgery, University of Freiburg, Hugstetter Strasse 55, D-79106 Freiburg, Germany. 0039-6060/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.surg.2003.08.021
vein thrombosis was present in approximately 10% of the patients only.1,7-9 In contrast to the more frequent splenic vein occlusion, portal and-or mesenteric vein occlusion has been reported with an incidence of 5% in a large follow-up series.1 Portal vein occlusion and superior mesenteric vein occlusion, as well as subtotal stenosis of those vessels, may lead to extrahepatic generalized portal hypertension (GPH) in the absence of liver cirrhosis. Portal vein occlusion and the presence of extrahepatic GPH are often regarded as a contraindication or a great endeavor for a pancreatic head resection (PHR). Portal and mesenteric vein occlusion have been identified as important risk factors for pancreatic resection.1,8,10,11 Some younger patients with CP, however, present with urgent indications for surgery, even in the presence of extrahepatic GPH. One option to reduce the perioperative risk might be decompression of the portal vein with subsequent resolution of vascular occlusion and portal hypertension. Few data are reported on pancreatic surgery in patients with extrahepatic GPH,1,8,10-13 and only SURGERY 411
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Table I. Basic patient characteristics and type of surgery in 185 patients with CP undergoing PHR GPH
P
No GPH
n 16 169 Male 88% 84% Age (y) (median and 39.8 (34-62) 42.7 (26-77) range) Duration of CP, (mo) 34 (3-180) 36 (1-148) (median and range) Etiology Alcohol 81.3% 75.1% Biliary — 1,8% Other 18.8% 23.1% Preoperative diabetes 43.8% 30.8% Preoperative jaundice 62.5% 24.3% Biliary drainage 43.8% 22.5% Pseudocysts 75% 61.5% Infected pseudocysts — 3.6% Type of surgery Whipple 2 21 PPPD 4 85 DPPHR 10 63 Beger 4 29 Frey 6 34
NS NS
NS NS NS NS .002 .06 NS
CP, Chronic pancreatitis; PHR, pancreatic head resection; GPH, generalized portal hypertension; PPPD, pylorus-preserving pancreatoduodenectomy; DPPHR, duodenum-preserving pancreatic head resection.
a few PHRs performed under these challenging conditions have been described.1,10,12 The aim of our study was to analyze our experience with PHRs in the presence of extrahepatic GPH in a large number of patients with CP and to describe our surgical strategy developed successively in dealing with this problem. During the study period, we started to use an interventional method to recanalize the occluded superior mesenteric and portal veins preoperatively to decrease portal hypertension, which allowed or facilitated subsequent PHR with complete transection of the pancreatic neck. PATIENTS AND METHODS From July 1994 to August 2002, 231 primary operations were performed electively in patients with CP. The principal perioperative data were prospectively documented in a computerized database. Additional data necessary for our analysis were obtained from the complete inhospital charts. Twenty-one patients were identified to have extrahepatic GPH due to portal vein occlusion (n = 15), high-grade stenosis of the portal vein (n = 4), or high-grade stenosis of the splenic and portalsuperior mesenteric veins (n = 2).
Only patients undergoing PHR (n = 185) were considered for this study. Sixteen of those 185 (8.6%) patients had extrahepatic GPH (GPH group), whereas the remaining pre- and intraoperative 169 patients (91.4%) had no signs of GPH (no-GPH group). Five of the 21 patients with extrahepatic GPH did not undergo PHR. These patients presented with limited disease. In 3 cases, solitary pseudocysts with gastric outlet obstruction were present, and pseudocystojejunostomy was performed. In 1 case, where we performed a hepaticojejunostomy, jaundice was the only symptom. A preoperative biliodigestive anastomosis was already planned because of known extrahepatic GPH in 4 of the 5 patients. In the fifth patient, the operation was switched intraoperatively from a planned PHR to a pseudocystojejunostomy due to severe bleeding during preparation. Basic demographic and disease-related data of the 185 study patients are shown in Table I. It is of note that 10 of 16 patients with portal hypertension had jaundice due to high-grade stenosis of the distal common bile duct. Preoperative biliary drainage was performed more frequently in these patients compared with patients without portal hypertension. Further indications or coindications for surgery in the 16 patients with extrahepatic GPH were intractable pain (n = 9), gastric outlet obstruction (n = 2), gastrointestinal bleeding from an aneurysm of inferior pancreatoduodenal artery (n = 1), and a pancreatopleural fistula (n = 1). The last postoperative follow-up of the 15 patients with portal hypertension who survived PHR was obtained during outpatient visits (n = 10) or by telephone contact with the patients and their home physicians (n = 5). Diagnosis of portal hypertension. Preoperative workup of the 185 patients before elective PHR included computed tomography scan (96%), visceral angiography (94%), and/or magnetic resonance angiography (11%). Radiologic signs of extrahepatic GPH were total or subtotal occlusion of the portal-superior mesenteric vein combined with an extensive net of collateral veins, localized mainly around the duodenum and pancreatic head. In all cases, except 1, portovenous thrombosis and portal hypertension were correctly diagnosed preoperatively by visceral angiography. In this 1 case, the portovenous system was free of obstruction during preoperative workup by angiography, endosonography, and computed tomography scan. This patient most likely developed portal vein thrombosis in the time period between diagnostic workup and surgery.
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During preoperative workup, all 16 patients with portal hypertension received upper gastrointestinal endoscopy. Gastric fundus varices were found in 3 patients, and esophageal varices in 1 patient. The patient with esophageal varices was the only one with a history of variceal bleeding. Despite portal hypertension, none of the 16 patients had ascites intraoperatively. Interventional recanalization of the portal vein. Interventional recanalization of the occluded portal vein was performed in 6 patients to reduce portal blood pressure perioperatively by restoring the normal mesenteric-portal route, thereby making transsection of the pancreatic neck possible. Following catheterization of the right hepatic vein via the right jugular vein, cannulation of the right main branch of the portal vein was performed. Subsequently an 8 F introducer was placed into the portal vein for atraumatic catheterization of the thrombosed portal-superior mesenteric vein. The thrombus was fragmented using an 8 F Amplatz (Bard Peripheral Vascular, Inc - Interventional, Tempe, Ariz) or an 8 F Oasis (Boston Scientific International, Natick, Mass) thrombectomy catheter in pull-back technique. After restoration of the liver-directed blood flow, a 4 F catheter was inserted into the superior mesenteric vein for local thrombolysis. Thrombolysis was performed by application of a bolus of 5 mg recombinant tissue plasminogen activator (rTPA) and subsequent local infusion of 2-5 mg/h rTPA for 12 hours, accompanied by intravenous heparin at 600-800 IU/h. The number of thrombolysis cycles was 1 to 4, depending on localization, size, and age of the thrombus. Smaller thrombi that were washed out into the liver by restored portal blood flow were thrombolysed by direct local intervention with lower doses of rTPA. Basket catheters mechanically minced older thrombi that were not accessible for thrombolysis. Fragments were removed via the introducer. With this technique, thrombi up to 25 cm in length were removed in our patients. After reconstruction of orthograd flow in the mesenteric-portal vein and removal of thrombi from these vessels, a 4 F catheter was inserted in the superior mesenteric vein for local heparin application until operation. All operations were performed 1 to 2 days after recanalization. Surgery and perioperative management. The different types of PHRs performed are shown in Table I. In our series, patients with preoperative GPH were statistically more likely to receive duodenumpreserving head resection (63% of the 16 patients) compared with those patients without GPH (38%
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duodenum-preserving head resections in 169 patients; P = .05). We performed more duodenumpreserving head resections during the second part of the study period in all patients with CP. Since most of the patients with extrahepatic GPH underwent operation in the second part of the study period, the higher frequency of duodenum-preserving resections in this subgroup may partially reflect the overall trend in our surgical management. After resection of the pancreatic head, the remaining pancreatic duct in the pancreatic remnant was carefully cannulated to exclude stenosis. Pancreatic duct stones, if present, were removed after head resection. For reconstruction, a pancreatojejunostomy was carried out in all patients. In cases involving classic Whipple operation, pylorus-preserving pancreatoduodenectomy (PPPD), and duodenum-preserving PHR according to Beger, our preferred technique was pancreatodigestive anastomosis to the pancreatic remnant, consisting of an end-to-side, single-layer, full-thickness anastomosis using interrupted polydioxanone sutures. In cases involving duodenumpreserving pancreatectomy according to Frey, the anastomosis between the remaining pancreatic tissue and the jejunal loop was created by using running polydioxanone sutures. Hepaticojejunostomy during Whipple or PPPD was also created with interrupted polydioxanone sutures. A biliodigestive anastomosis was performed in 21 (33%) of the 63 DPPHR in patients without extrahepatic GPH and in 5 of 10 DPPHR (50%) of those with GPH. All patients received perioperative antibiotic coverage, which was prolonged to the first 3 postoperative days in cases involving preoperative biliary drainage or intraoperative infection (eg, infected pseudocysts). Octreotide 100 lg 3 times a day for 7 days was started intraoperatively and continued postoperatively subcutaneously in 96% of the patients. Postoperatively, all patients were treated at least for 1night at our surgical intensive care unit. Definitions and statistics. Delayed gastric emptying was defined as inability to eat a regular diet beyond day 10 postoperatively. The groups of patients with and without portal hypertension were compared by using the chi-square test, MannWhitney test, or U-test, as applicable. All analyses were performed with the statistical software SPSS (release 10, SPSS Inc, Chicago, Ill). RESULTS Preoperative recanalization of portal vein occlusion. After 1998, 6 patients preoperatively had interventional transhepatic catheter thrombolysis
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Table II. Outcome of PHRs performed in patients with GPH and in patients without generalized portal hypertension GPH
No GPH
n 16 169 Duration of surgery 533 (240-870) 420 (220-740)* (min) (median and range) Blood transfusion 9.3 (0-32) 4 (0-36)* (units) (median and range) Postoperative hospital 16 (10-41) 14 (8-61) stay (d) (median and range)y Death (n)(%) 1 (63%) 1 (0.6%) Complications (n) 7 (43.8%) 57 (33.7%) Pancreatic leakage 0 15 (8.9%) Biliary leakage 0 1 (0.6%) Abdominal bleeding 2 (12.5%) 3 (1.8%)z Gastrointestinal 1 (6.3%) 2 (1.2%) bleeding 3 (20%) 16 (9.5%) Delayed gastric emptyingyz Abdominal abscess 1 (6.3%) 7 (4.1%) Pneumonia 2 (12.5%) 12 (7.1%) Infected drain fluid 0 6 (3.7%) without abscess Wound infection 2 (12.5%) 11 (6.5%) Relaparotomies (n) 1 (8.3%) 9 (5.5%) (%) PHR, Pancreatic head resections; GPH, generalized portal hypertension. *P < .01. y2 deaths excluded, 1 in each group. zP = .06.
of portal vein thrombosis by interventional radiologists. The lysis of the thrombosed portal vein was successful (reestablished blood flow in the superior mesenteric-portal vein at the end of the recanalization procedure) in 5 patients who subsequently underwent PHR (2 PPPD, 1 classical Whipple, and 2 Beger-DPPHR). One of those 5 patients, however, redeveloped portal vein thrombosis detected during laparotomy and underwent operative thrombectomy during PHR. Three of the 6 patients developed interventionassociated complications. One woman had intraabdominal bleeding at the end of the lysis period, which stopped after discontinuing the lysis. One patient had a hemobilia caused by a fistula from an intrahepatic artery to a bile duct that became symptomatic on day 4 after PHR by gastrointestinal bleeding. This complication could be treated successfully by interventional embolization of the arterial branch. Another patient (in whom the recanalization had failed) developed an intrahepatic hematoma treated conservatively.
Despite successful preoperative recanalization, all 5 patients intraoperatively presented with signs of relevant portal hypertension, but the pancreatic body could successfully be transected above the superior mesenteric-portovenous route. Normal venous splanchnic blood flow was thus restored following transection, and thereby the mechanical compression of the veins was alleviated. None of the 5 patients died postoperatively. The sixth patient, in whom preoperative recanalization had failed, received a Frey-DPPHR. At the time of hospital discharge, the portal vein had rethrombosed completely in 1 patient and partially in a second one, as shown by duplex ultrasound. An orthograd flow in the superior mesenteric and portal veins could be documented by duplex ultrasound in all patients. Intraoperative problems with GPH and change of surgical tactic (n = 16). Intraoperative bleeding problems by portal hypertension were documented in 11 of the 16 (69%) patients with extrahepatic GPH who underwent PHR. During 5 of the operations in which PPPD or Beger’s operation was initially planned, portal hypertension led to a change of the surgical strategy and Frey’s operation was performed. None of those 5 patients had undergone preoperative recanalization. As demonstrated in Table II, duration of surgery and the number of intraoperatively transfused units of packed red cells were significantly higher in the GPH group compared to the no-GPH group. In 1 patient, intraoperative bleeding could only be controlled by packing, although the patient had an emergent portocaval anastomosis after a classic Whipple resection of the pancreatic head. As mentioned previously, this was the only patient whose preoperative diagnosis did not show portal vein occlusion. Postoperative complications (all patients). Among the 185 patients, there were 2 postoperative deaths (1.1%): 1 in the extrahepatic GPH group (6.3 %) and 1 in the no-GPH group (0.6%; P = NS). Postoperative complications occurred in 44 % of patients with portal hypertension and in 34 % of patients without portal hypertension (Table II). The rate of postoperative abdominal bleeding was the only sole complication that was notably more frequent in patients with portal hypertension, although it just failed statistical significance (12.5% vs 2% in patients without portal hypertension; P < .06). It is also of note that none of the patients with portal hypertension developed a pancreatic leakage. The relaparotomy rate was comparable in both groups. Although delayed gastric emptying
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was more frequent in the GPH group (20% vs 9.5% in the no-GPH group), this difference did not reach statistical difference (P = .2). The median postoperative length of stay was slightly higher in patients with portal hypertension. However, this value did not reach statistical significance. Postoperative follow-up of 15 patients with portal hypertension. Long-term postoperative follow-up was obtained in all 15 patients with portal hypertension surviving PHR (median follow-up, 18 months; range, 3-61 months). None of these 15 patients developed variceal bleeding, but 1 patient had bleeding into a recurrent pseudocyst 18 months after initial surgery, which was managed conservatively. Except for 1 repair of an incisional hernia, no reoperation had to be performed. Thirteen of 15 patients did not complain about abdominal pain; the other 2 patients had moderate abdominal pain, approximately once per month, that required oral analgesics. The result of the operation was subjectively judged as ‘‘good’’ or ‘‘very good’’ by all 15 patients. No jaundice or other signs of cholestasis occurred postoperatively. DISCUSSION Extrahepatic GPH by total or subtotal occlusion of the splenoportal system is a well-known complication in CP. The incidence of splenic vein obstruction ranges from 2 % to 45 %,1, 5, 14, 15 whereas portal and/or mesenteric vein obstruction has been reported to occur in about 5%-10 % of patients.1,10,12 In our experience with 231 patients who underwent operation for CP, 37% had alterations of the portovenous system. Twenty-one percent of the patients had splenic vein thrombosis. Extrahepatic GPH was found in 9% of all 231 patients with CP who underwent an operation and in 9% of the 185 patients who received PHR. The presence of splenic, mesenteric, and /or portal vein occlusion as a complication of CP per se is not an indication for surgery.8,10,12 Gastrointestinal bleeding from esophageal, gastric, or duodenal varices, which may develop in the context of regional or GPH is a rare complication.1,12 In a prospective longitudinal series, the incidence of splenoportal obstruction was reported to be 13 % in 266 patients; the occurrence of gastrointestinal varices and variceal bleeding, however, was only 2 % and 0.5 %, respectively.1 In a recently published cohort of patients with PHR for CP, an incidence of 23 % for regional or extrahepatic GPH and 3 % for varices was reported. However, no bleeding was observed in this series.12 These results are also
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confirmed by our data. Of the 21 patients with extrahepatic GPH, only 1 had a history of bleeding from varices. The 2 patients in the GPH group with gastrointestinal bleeding as the main indication for pancreatic surgery did not present with variceal bleeding; they presented with bleeding from an aneurysm of the inferior pancreatoduodenal artery and common hepatic artery, respectively. Patients with occlusion of the splenoportal system, however, do sometimes require surgery for other complications of CP. In these cases, surgical strategy depends on the type of portal hypertension (ie, generalized or left-sided). In patients with left-sided portal hypertension and signs of fundus varices, splenectomy is the treatment of choice.7,15-18 Even though splenectomy in CP and left-sided portal hypertension is technically more demanding than in other indications (eg, hematological diseases or trauma), it can safely be added to any kind of pancreatic surgery, whether it is a resection or a drainage procedure. In contrast to left-sided portal hypertension, extrahepatic GPH caused by total or subtotal occlusion of the superior mesenteric-portal vein is by far more difficult to handle during surgery. This type of occlusion leads to an extensive net of collateral veins surrounding the pancreatic head (Fig 1) and can proceed to cavernous transformation in the hepatoduodenal ligament. In this situation, any kind of operation on the pancreatic head can cause relevant bleeding. PHR, therefore, is regarded as too risky in this situation by most surgeons. Surgical intervention due to various symptoms related to portal vein occlusion, however, might be necessary in these patients. Compression and subsequent obstruction of the superior mesenteric and/or portal vein seems to be an indicator of an advanced stage of CP, with a relatively large pancreatic mass and/or advanced fibrosis of the pancreatic head in many cases. Therefore, these patients more often present with other local complications of CP such as common bile duct or gastric outlet obstruction. In a recently published surgical study of 154 patients requiring surgery for CP, it was evident that patients with extrahepatic portal hypertension had a higher prevalence of common bile duct stenosis and segmental duodenal stenosis at the time of surgery.12 Similar findings were seen in our series, in which the rate of common bile duct obstruction in the GPH group was significantly higher than in the no-GPH group. Both the elevated probability of perioperative complications and an increased risk of surgical interventions in the presence of extrahepatic GPH dictate that surgery is indicated only in the
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Fig 1. Magnetic resonance angiography (portovenous phase) in a patient with extrahepatic GPH. Occlusion of the splenic, superior mesenteric, and peripheral portal veins led to the development of extended collaterals.
presence of severe complications of CP and not for extrahepatic GPH per se.10 There are few data regarding the surgical strategy in patients with CP complicated by GPH. In a study of 14 patients with superior mesentericportal vein obstruction, Warshaw and coworkers10 reported on 40 operations for complications of CP. Most of the interventions were drainage procedures and focused on limited symptomatic surgical therapy. Only 1 pancreatoduodenectomy was performed in this series. However, in a prospective randomized trial evaluating nonocclusive segmental portal hypertension due to CP, it was demonstrated that resection—but not drainage—was able to restore normal splanchnic blood flow.13 Patients in the resection group (n = 16) in this series underwent duodenum-preserving resection of the head of the pancreas as originally described by Beger,19 whereas patients in the drainage group (n = 14) underwent a modified procedure introduced by Frey and Smith.20 Decompression of the portal venous system after PHR was also demonstrated by Ruzicka et al21 in 17 patients with CP who underwent PHR. The intraoperative transection of the pancreas above the mesenteric-portal vein during the Beger procedure causes a marked release of the encased vessels. The same effect also can be achieved by
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either the pylorus-preserving PHR (PPPD) or the classic Whipple operation. In addition to treating local and general complications of CP (eg, common bile duct obstruction, duodenal obstruction, main pancreatic duct obstruction, inflammatory tumor of the pancreatic head, pain or recurrent episodes of inflammation), these operations may solve the problem of extrahepatic portal hypertension and its late complications. Risks of bleeding complications dictate that transsection of the pancreas can be recommended only when a nonocclusive portal hypertension exists. Whereas subtotal stenosis of the portal vein or superior mesenteric vein is common and leads to extrahepatic GPH in only a small percentage of cases, complete thrombotic obstruction of the portal vein leads obligatory to extrahepatic GPH. Exposure of the superior mesenteric-portal vein at the level of the pancreatic neck and subsequent transection of the pancreas above these veins is technically demanding and the most hazardous part of the whole operation.11 Complete transection of the pancreatic neck and extensive resection of the pancreatic head seem to be contraindicated when the superior mesenteric-portal vein is totally occluded. In this case, a PHR would result in a substantial reduction of the collateral circuit, leading to a potentially uncontrollable increase of venous pressure and consecutive bleeding. Facing this therapeutic dilemma, we established an interventional approach to preoperatively reopen an already-occluded portal and/or mesenteric vein in cooperation with our interventional radiologists (Fig 2). In addition to the 6 patients with nonocclusive extrahepatic GPH due to subtotal vein stenosis, we were able to transfer 5 more patients from an initially occlusive to a nonocclusive form of portal hypertension. Of these 11 patients, the pancreas was transected over the mesentericoportal axis in 9 patients who received a resection of the pancreatic head. One Whipple operation, 4 PPPDs, and 4 Beger operations were performed. Two of the first patients in this series received a Frey operation even though they had only subtotal stenosis of the portovenous system. During the years after establishment of the interventional approach, we established a standardized workflow in which all patients with extrahepatic GPH requiring PHR are treated. Our decision tree is shown in Figure 3. We try to preoperatively reopen the route of the superior mesenteric-portal vein to enable subsequent transection of the pancreatic neck. In addition to the salvage of extrahepatic GPH, PHRs (Beger procedure, Whipple operation, PPPD) also provide the prospect for a long patent
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Fig 2. A, Angiographic image of portal vein occlusion before recanalization. B, Procedure of recanalization of the portal vein; the angiography catheter passes through the still-occluded vein before lysis. C, Control angiography after successful lysis now demonstrates an open portal vein.
biliodigestive anastomoses because a mucosa-tomucosa anastomosis can be performed. Because common bile duct obstruction is frequent in the presence of extrahepatic GPH, the patency of biliodigestive anastomoses could be an important cofactor regarding the long-term results. Even though the 2 collectives—receiving recanalization or not receiving recanalization—are not comparable in terms of preoperative situation and of the extent of the performed operation, we compared the amount of perioperative blood transfusions and found no significant difference (10.7 units of packed red cells in patients with recanalization vs 8 units in patients without recanalization; P = .8). In 5 patients, the superior mesenteric and portal veins were still occluded at the time of operation. A limited resection of the pancreatic head according to Frey was performed in 4 of these patients. In 2 of these 4 cases, the Frey operation was combined with a Y-Roux side-to-side hepaticojejunostomy. We judge this approach as reasonable, because it can prevent major bleeding in the situation of cavernous transformation in the hepatoduodenal ligament. In contrast to the otherwise common end-to-side technique of hepaticojejunostomy, this side-to-side anastomosis can be performed without circumferential dissection of the common bile duct and the surrounding collateral veins. This approach again allows a mucosa-to-mucosa anastomosis in contrast to performing an incision of the common bile duct on the fibrotic dorsal wall of the Frey-resection cavity and draining bile into this pancreatic cavity, as described by others.11 The patient in whom preoperative diagnostic workup failed to show occlusion of the superior mesenteric-portal vein and who finally died after
Fig 3. Proposed algorithm for patients with surgically treatable complications of CP in the presence of GPH.
classic Whipple operation and an emergent portocaval shunt was the first patient in our series of PHR in the presence of extrahepatic GPH. This fatal outcome prompted us to specific therapeutic strategies and again underlines the importance of a reliable and recent preoperative imaging of the portal venous system with differentiation between total and subtotal occlusion. Our results demonstrate that PHR in patients with extrahepatic GPH is technically demanding and time consuming, and carries the risk of an increased intraoperative bleeding. However, we could show that postoperative morbidity and mortality remain in an acceptable range. The preoperative knowledge of extrahepatic GPH followed by a differentiated surgical approach enabled us to perform 15 consecutive PHRs without mortality in patients with GPH. Although postoperative complications occurred slightly more frequently in patients with portal hypertension than in patients without portal
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hypertension, the 44 % overall morbidity is in the range of overall complication rates of recent reports on pancreatoduodenectomy from other large centers.22-25 To our knowledge, this is the largest series of PHRs in patients with CP complicated by GPH. We can report for the first time on a systematic approach that includes preoperative superior mesenteric-portal vein recanalization. With this approach, PHRs in CP complicated by GPH can be performed with outcomes similar to PHRs in other series. REFERENCES 1. Bernades P, Baetz A, Levy P, Belghiti J, Menu Y, Fekete F. Splenic and portal venous obstruction in chronic pancreatitis. A prospective longitudinal study of a medical-surgical series of 266 patients. Dig Dis Sci 1992;37:340-6. 2. Seiler CA, Boss MA, Czerniak A, Berne TV, Blumgart LH. Vascular complications in chronic pancreatitis. Dig Surg 1997;14:107-12. 3. Rattner DW, Warshaw AL. Venous, biliary, and duodenal obstruction in chronic pancreatitis. Hepatogastroenterology 1990;37:301-6. 4. Kaiser G, Hommel G. Morphometrisch-statistische Analyse der Pankreasarterien bei Chronischer Pankreatitis. Virchows Arch A Pathol Anat 1975;365:103-18. 5. Leger L, Lenriot JP, Lemaigre G. Hypertension and segmental portal stasis in chronic pancreatitis. Apropos of 126 cases examined by splenoportography and splenomanometry. J Chir (Paris) 1968;95:599-608. 6. Rignault D, Mine J, Moine D. Splenoportographic changes in chronic pancreatitis. Surgery 1968;63:571-5. 7. Sakorafas GH, Sarr MG, Farley DR, Farnell MB. The significance of sinistral portal hypertension complicating chronic pancreatitis. Am J Surg 2000;179:129-33. 8. Seiler CA, Friess H, Buchler M. Thrombosis of the portal and splenic vein. In: Beger HG, editor. The Pancreas. 1st ed. Oxford: Blackwell Science Ltd; 2000. p. 854-62. 9. Mariethoz S, Savioz D, Buhler L, Becker C, Morel P. Splenic vein thrombosis and chronic pancreatitis: therapeutic approach. Schweiz Med Wochenschr 1998;128:867-70. 10. Warshaw AL, Jin GL, Ottinger LW. Recognition and clinical implications of mesenteric and portal vein obstruction in chronic pancreatitis. Arch Surg 1987;122:410-5. 11. Gloor B, Friess H, Uhl W, Buchler MW. A modified technique of the Beger and Frey procedure in patients with chronic pancreatitis. Dig Surg 2001;18:21-5.
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