Whipple pancreatoduodenectomy

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1 Vascular and Interventional Radiology Pictorial Essay Puppala et al. Hemorrhagic Complications After Whipple Surgery Vascular and Interventional Radiology Pictorial Essay Sapna Puppala 1 Jai Patel Simon McPherson Anthony Nicholson David Kessel Puppala S, Patel J, McPherson S, Nicholson A, Kessel D Keywords: CT angiography, digital subtraction angiography, embolization, pancreatoduodenectomy, stent DOI: /AJR Received April 1, 2010; accepted after revision June 7, All authors: Department of Radiology, Leeds Teaching Hospital NHS Trust, Great George St., Leeds, West Yorkshire LS1 3EX, United Kingdom. Address correspondence to S. Puppala. AJR 2011; 196: X/11/ American Roentgen Ray Society Hemorrhagic Complications After Whipple Surgery: Imaging and Radiologic Intervention OBJECTIVE. The aim of this pictorial essay is to illustrate the radiologic patterns, sites of bleeding, and vascular interventional techniques used in the management of postpancreatectomy hemorrhage. CONCLUSION. Hemorrhagic complications occur in fewer than 10% of patients after Whipple pancreatoduodenectomy but account for as many as 38% of deaths. Bleeding typically occurs from the stump of the gastroduodenal artery, but other sites of bleeding are increasingly recognized. Whipple pancreatoduodenectomy is most often performed for tumors of the head of the pancreas. The procedure involves resection of the head of the pancreas, the duodenum, the proximal jejunum, the distal third of the stomach, and the lower half of the common bile duct followed by biliary, pancreatic, and gastric anastomoses to the jejunum. The gastroduodenal artery (GDA) is cut and ligated at its origin from the hepatic artery. A variation is a pylorus-sparing Whipple operation performed to improve gastrointestinal function. Pancreatoduodenectomy has 30 40% morbidity and 5% mortality. Early surgical complications include anastomotic leak, hemorrhage, sepsis, pancreaticojejunal fistula, acute pancreatitis of the remnant pancreas, and peritonitis [1, 2]. Postpancreatectomy Hemorrhage Postpancreatectomy hemorrhage is seen in less than 10% of patients but accounts for 11 38% of mortality [1]. A range of vascular lesions and sources have been incriminated. The International Study Group of Pancreatic Surgery has clinically graded postpancreatectomy hemorrhage on the basis of onset, location, and severity [2]. Time of Onset Early postpancreatectomy hemorrhage is that which occurs within 24 hours of surgery. It often is caused by GDA stump insufficiency due to technical failure. Late postpancre- atectomy hemorrhage occurs more than 24 hours after the operation. It can be caused by an ulcer, vascular erosion from pancreatic leak, fistula, pseudoaneurysm, or anastomotic dehiscence. Location Intraluminal postpancreatectomy hemorrhage manifests itself as hematemesis, bleeding from the nasogastric tube, or melena. Extraluminal postpancreatectomy hemorrhage is characterized by bleeding from drains or an abdominal wound or intraabdominal bleeding. True extraluminal bleeding has an extraluminal source. False extraluminal bleeding is a manifestation of primary intraluminal bleeding that becomes extraluminal owing to coexisting anastomotic disruption. Intraluminal bleeding is often managed by endoscopy and extraluminal bleeding by radiologic intervention [3 5]. Severity Postpancreatectomy hemorrhage can be mild or severe. Sentinel Bleeding Sentinel or herald bleeding refers to isolated bleeding, usually from an abdominal drain. It implies the presence of a structural vascular defect and requires immediate evaluation [6]. Sentinel bleeding can be associated with local sepsis and anastomotic dehiscence and warns of impending major postpancreatectomy hemorrhage [7]. 192 AJR:196, January 2011

2 Hemorrhagic Complications After Whipple Surgery Imaging There is no role for imaging in the evaluation of patients who are exsanguinating; they need immediate laparotomy [8]. Patients who are in relatively stable hemodynamic condition should undergo CT at the time of active bleeding, when sensitivity is highest. Delaying imaging reduces the positive yield unless there is a clear structural vascular abnormality or pseudoaneurysm. Ultrasound imaging may depict a false aneurysm but has no role in the investigation of acute bleeding. MDCT Angiography CT angiography shows the cause, site, and nature of bleeding [9, 10]. A triple-phase examination (unenhanced, arterial, and venous phases) is performed with iodinated contrast material. Images are reviewed with multiplanar reformatting, which contributes to the diagnosis and aids in the planning of endovascular or surgical intervention (Fig. 1A). Unenhanced scans depict collections and high attenuation from beam-hardening and streak artifacts that can mimic bleeding. The arterial phase shows active contrast extravasation and the arterial anatomy. The venous phase shows contrast pooling and other complications that can follow a Whipple procedure (Fig. 2). Digital Subtraction Angiography The role of digital subtraction angiography has changed from diagnostic to therapeutic [11]. If the site of bleeding is uncertain, angiography of the celiac axis and superior mesenteric artery should be performed (Fig. 3). Active contrast extravasation and pseudoaneurysms (Fig. 1B) are evidence of early or delayed filling. Spasm and irregularity of a vessel are indirect signs of a source of bleeding (Figs. 2 and 4). If extravasation from the expected sites is not seen, selective angiography can be performed (Fig. 4). Anatomic variation is common and can simplify or complicate embolization (Figs. 5 and 6). A brachial artery approach is useful if awkward angulation of the celiac axis is present (Fig. 1B). Radiologic Management Embolization sacrifices distal blood flow but is suitable for challenging anatomy and small vessels [11]. The embolic materials used are coils, glue, thrombin, and absorbable gelatin sponge. Coils are commonly used and suitable when there is a single feeding vessel, which can be sacrificed (Figs. 5 and 6). It is essential to embolize both the inflow and outflow vessels, or bleeding will recur (Fig. 3). Glue can be used to embolize small vessels that cannot be directly catheterized or to seal the GDA stump (Fig. 7). Balloon occlusion can be used for protection of distal circulation (Fig. 8), but tissue infarction is more likely than with coils (Fig. 9). Stent grafting [12, 13] preserves distal perfusion, such as that to the liver and spleen, but can be impossible in tortuous and small vessels. Guide catheters add stability, especially in stent grafting (Figs. 4 and 10). Intentional dissection is an option if the bleeding site cannot be reached selectively for embolization. Pseudoaneurysms that persist after embolization can be managed with percutaneous injection of thrombin under ultrasound or CT guidance [13] (Fig. 9). The limitations of intervention must be recognized; in some cases embolization is only a temporizing measure before surgery to repair anastomoses [8, 14]. Scenarios Gastroduodenal Artery Stump The gastroduodenal artery stump is the first place to look for complications. Surgical clips adjacent to the hepatic artery indicate the position of the stump. Active extravasation from the stump or pseudoaneurysm is readily recognized and managed by embolization with glue or coils or excluded with a covered stent (Figs. 1C, 5, and 6). Common and Proper Hepatic Artery Erosions Common and proper hepatic artery erosions are increasingly recognized and occur as the result of pancreatic leaks. Embolotherapy is a temporizing measure in the presence of sepsis and pancreatic leak. Continued vascular damage can lead to recurrence of bleeding from the same site or other sites (Fig. 9). Covered stents are useful and have the added benefit of preserving distal perfusion (Figs. 8 and 11). Celiac Axis Erosion Celiac axis erosion is uncommon, and endovascular stent grafting is an option in its management, although this procedure may involve sacrificing either the hepatic or the splenic branch. An alternative is to embolize the whole vessel to ensure no back filling from the celiac axis branches (Fig. 3). Splenic Artery Erosion Splenic artery erosion is uncommon and secondary to pancreatic leak or intraoperative trauma (Figs. 10 and 12). Management depends on the site and tortuosity of the splenic artery. A covered stent can be used in straight arteries. In tortuous vessels, embolization is required. Proximal lesions can be embolized with preservation of splenic perfusion via the short gastric arteries and other collateral vessels. Embolization of distal lesions increases the risk of splenic infarction. Inferior Pancreatoduodenal Artery Aneurysm Inferior pancreatoduodenal artery aneurysm is rarely seen after the Whipple procedure but is presumed to occur as the result of increased flow in the inferior pancreatoduodenal artery after GDA ligation (Fig. 6). If bleeding is present, the vessel can be managed with embolization. Arc of Buhler Aneurysm and Pseudoaneurysm The arc of Buhler is a mesenteric collateral vessel that originates from the common hepatic artery proximal to the GDA (Fig. 7). Hemobilia due to involvement of the residual common bile duct in the inflammatory process can manifest itself as false extraluminal bleeding through a disrupted anastomosis. The hepatic artery can be embolized (Fig. 2). Superior mesenteric artery pseudoaneurysms also occur [13, 15]. Conclusion Postpancreatectomy hemorrhage is an important complication with high mortality. Early recognition and treatment are essential. CT angiography is used in diagnosis, and endovascular intervention is preferred to surgery because of a lower mortality. When anastomotic leak and sepsis are ongoing, radiologic intervention, although life-saving, should be considered only a bridge to definitive treatment, which is surgery. References 1. Jagad RB, Koshariya M, Kawamoto J, Chude GS, Neeraj RV, Lygidakis NJ. Postoperative hemorrhage after major pancreatobiliary surgery: an update. Hepatogastroenterology 2008; 55: Wente MN, Veit JA, Bassi C, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 2007; 142: Sohn TA, Yeo CJ, Cameron JL, et al. Pancreaticoduodenectomy: role of interventional radiologists in managing patients and complications. J Gastrointest Surg 2003; 7: Beyer L, Bonmardion R, Marciano S, et al. Results of non-operative therapy for delayed hemorrhage AJR:196, January

3 Puppala et al. after pancreaticoduodenectomy. J Gastrointest Surg 2009; 13: [Epub 2009 Feb 18] 5. Standop J, Schäfer N, Overhaus M, et al. Endoscopic management of anastomotic hemorrhage from pancreatogastrostomy. Surg Endosc 2009; 23: [Epub 2008 Dec 6] 6. Tien YW, Wu YM, Liu KL, Ho CM, Lee PH. Angiography is indicated for every sentinel bleed after pancreaticoduodenectomy. Ann Surg Oncol 2008; 15: [Epub 2008 Apr 16] 7. Tsirlis T, Vasiliades G, Koliopanos A, et al. Pancreatic leak related hemorrhage following pancreaticoduodenectomy a case series. JOP 2009; 10: Blanc T, Cortes A, Goere D, et al. Haemorrhage after pancreaticoduodenectomy: when is surgery Fig. 1 Patient with cancer. A, Coronal contrast-enhanced arterial phase reformatted MDCT image confirms arterial anatomy of origin of pseudoaneurysm (arrow) from gastroduodenal artery stump. B, Digital subtraction angiogram obtained through left brachial artery because of angulations of celiac axis confirms extravasation and filling of pseudoaneurysm (arrow). Arrowhead indicates catheter. Fig year-old woman who has undergone Whipple procedure and has bleeding from external skin wound and in drain. A, Venous phase CT angiogram shows contrast pooling (arrow). Arterial phase image (not shown) showed intraabdominal collection of blood with no extravasation, illustrating importance of performing triple-phase CT. Late pooling can be due to delayed filling of pseudoaneurysm or false extraluminal bleeding, as in this case. Initial digital subtraction angiogram showed no extravasation, and patient was taken to operating theater when bleeding from common bile duct (hemobilia) that had become secondary extraluminal bleeding via disrupted anastomosis was noticed. B, Repeat digital subtraction angiogram of hepatic artery shows irregularity and spasm of artery (arrow) but no bleeding. C, Digital subtraction angiogram shows embolization coil (arrow) and no further hemorrhage. still indicated? Am J Surg 2007; 194: Smith SL, Hampson F, Duxbury M, Rae DM, Sinclair MT. Computed tomography after radical pancreaticoduodenectomy (Whipple s procedure). Clin Radiol 2008; 63: [Epub 2008 Feb 1] 10. Lepanto L, Gianfelice D, Déry R, Dagenais M, Lapointe R, Roy A. Postoperative changes, complications, and recurrent disease after Whipple s operation: CT features. AJR 1994; 163: Makowiec F, Riediger H, Euringer W, Uhl M, Hopt UT, Adam U. Management of delayed visceral arterial bleeding after pancreatic head resection. J Gastrointest Surg 2005; 9: Kaw LL Jr, Saeed M, Brunson M, Delaria GA, Dilley RB. Use of a stent graft for bleeding hepatic artery pseudo aneurysm following pancreaticoduodenectomy. Asian J Surg 2006; 29: Wallace MJ, Choi E, McRae S, Madoff DC, Ahrar K, Pisters P. Superior mesenteric artery pseudo aneurysm following pancreaticoduodenectomy: management by endovascular stent-graft placement and transluminal thrombin injection. Cardiovasc Intervent Radiol 2007; 30: Sato N, Yamaguchi K, Shimizu S, et al. Coil embolization of bleeding visceral pseudoaneurysms following pancreatectomy: the importance of early angiography. Arch Surg 1998; 133: Otah E, Cushin BJ, Rozenblit GN, Neff R, Otah KE, Cooperman AM. Visceral artery pseudoaneurysms following pancreatoduodenectomy. Arch Surg 2002; 137: AJR:196, January 2011

4 Hemorrhagic Complications After Whipple Surgery Fig. 3 Patient with cancer. A, Transverse CT angiogram shows extravasation of contrast material into false aneurysm (arrow) from celiac axis. B, Digital subtraction angiogram confirms presence of extravasation (arrow), which was initially managed with coil embolization of proximal artery via celiac axis. C, Angiogram obtained through inferior pancreaticoduodenal artery (arrowhead) shows bleeding through distal artery (arrow). D, Digital subtraction angiogram shows distal arterial supply (arrow) embolized with coil. Bleeding stopped completely. Fig. 4 Patient with cancer. A, Digital subtraction angiogram of celiac axis shows spasm and blind stump arising from common hepatic artery (arrow). B, Digital subtraction angiogram obtained with selective injection shows active extravasation (large arrow) from hepatic artery. Small arrow indicates catheter in common hepatic artery. C, Digital subtraction angiogram shows deployed covered stent astride eroded artery (arrow). Long sheath was used to increase stability. Guide catheter can be used if operator prefers. Fig. 5 Patient with cancer. A, Digital subtraction angiogram shows bleeding from aberrant gastroduodenal artery (GDA) stump (arrow) arising from left hepatic artery and pouring into abdominal cavity and outward via drain in keeping with true extraluminal bleeding. B, Digital subtraction angiogram shows stump embolized with coil. GDA (arrow) can originate from left hepatic artery and is seen when double hepatic artery, in which one or both hepatic arteries originate from celiac axis directly or from aorta, is present. Double hepatic artery can be differentiated from distal origin of GDA by presence of common hepatic artery. In case of double hepatic artery, there is no common hepatic artery, and GDA originates from either hepatic artery. Fig. 6 Patient with cancer. A, Digital subtraction angiogram obtained through superior mesenteric artery shows replaced right hepatic artery (arrow) (normal variation seen in approximately 11% of cases) and inferior pancreatoduodenal artery aneurysm (arrowhead). B, Digital subtraction angiogram obtained through celiac axis shows active extravasation from gastroduodenal artery stump (arrow), which was treated by coil embolization. C, Digital subtraction angiogram shows embolization coil (arrowhead) placed in inferior pancreatoduodenal artery aneurysm as prophylactic measure. Arrow indicates gastroduodenal artery stump. AJR:196, January

5 Puppala et al. Fig. 7 Patient with cancer. A, Transverse CT angiogram shows tiny focus of high attenuation in front of drain (arrow). B, Coronal maximum-intensity-projection image shows feeding artery and aneurysm (arrow). Because of its location, artery may be arc of Buhler. C, Digital subtraction angiogram confirms CT findings before embolization (arrow). D, Digital subtraction angiogram obtained after glue embolization shows cast of glue in line of artery and aneurysm (arrow). Case shows advantage of glue embolization when one cannot get close to lesion. Fig. 8 Patient with cancer. A, Digital subtraction angiogram of hepatic artery shows extravasation of contrast material from hepatic artery proper immediately distal to gastroduodenal artery stump (arrow). B, Digital subtraction angiogram shows initial treatment with glue (arrow). Protective balloon in hepatic artery prevents nontarget embolization. Bleeding recurred within 24 hours. C, Digital subtraction angiogram shows covered stent (arrow) used to manage recurrent bleeding at treatment site. Fig. 9 Patient with cancer. Transverse contrast-enhanced MDCT scan shows pseudoaneurysm (arrow) persistent after coil embolization and transcatheter placement of glue, both of which failed to occlude pseudoaneurysm, which increased in size. Incidental nontarget embolization of glue caused hepatic and splenic infarction later successfully managed with percutaneous thrombin injection. 196 AJR:196, January 2011

6 Hemorrhagic Complications After Whipple Surgery Fig. 10 Patient with cancer. A, Transverse contrast-enhanced arterial phase MDCT scan shows active extravasation (arrow) splenic artery close to its origin. Locules of air in hematoma and collection suggest sepsis. B, Digital subtraction angiogram shows bleeding (arrow). Splenic artery was inaccessible, impeding embolization. C, Angiogram shows covered stent (arrow) placed in hepatic artery to cover splenic origin and minimize distal arterial bleeding. Long sheath (white arrowhead) is used to add to stability. Guide catheter can be used depending on operator preference. Normal gastroduodenal artery stump (black arrowhead) is incidental finding. Fig. 11 Patient with cancer. A, Transverse venous phase contrast-enhanced MDCT scan shows hematoma (arrow) but no active extravasation. B, Digital subtraction angiogram obtained because patient was in hemodynamically unstable condition shows active bleeding from common hepatic artery (arrow). C, Digital subtraction angiogram shows beginning of glue embolization (arrow). Gastroduodenal artery stump (arrowhead) is normal. D, Digital subtraction angiogram shows completed glue embolization (arrow). Fig. 12 Patient with cancer. A, CT angiogram obtained 1 day after Whipple procedure shows active extravasation (arrow) from splenic artery secondary to possible traction injury at surgery. B, Coronal maximum-intensity-projection reformatted CT image shows vascular anatomy and site of bleeding (arrow). C, Digital subtraction angiogram obtained before embolization confirms presence of bleeding (arrow). D, Digital subtraction angiogram obtained after embolization of inflow artery with coils (arrow) shows distal artery closed by absorbable gelatin foam embolization because bleeding site could not be crossed. AJR:196, January