Management of Delayed Post-Pancreaticoduodenectomy Arterial Bleeding: Interventional Radiological Treatment First

Management of Delayed Post-Pancreaticoduodenectomy Arterial Bleeding: Interventional Radiological Treatment First

Original Paper Received: May 20, 2011 Accepted after revision: July 27, 2011 Published online: September 29, 2011 Pancreatology 2011;11:455–463 DOI: ...

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Original Paper Received: May 20, 2011 Accepted after revision: July 27, 2011 Published online: September 29, 2011

Pancreatology 2011;11:455–463 DOI: 10.1159/000331456

Management of Delayed PostPancreaticoduodenectomy Arterial Bleeding: Interventional Radiological Treatment First Ji Zhang a Xu Zhu b Hui Chen b Hong-Gang Qian a Jia-Hua Leng a Hui Qiu a Jian-Hui Wu a Bo-Nan Liu a Qiao Liu a Ang Lv a Ying-Jie Li a Guo-Quan Zhou a Chun-Yi Hao a   













Departments of a Hepatopancreatobiliary Surgery and b Interventional Radiology, Key Laboratory of Carcinogenesis and Translational Research, Ministry of Education, Peking University School of Oncology, Beijing Cancer Hospital and Institute, Beijing, PR China  


Key Words Clinical studies ⴢ Hepatobiliary malignancy ⴢ Interventional therapy ⴢ Pancreatic surgery ⴢ Delayed postoperative bleeding ⴢ Arterial bleeding

omy with drain replacement. Conclusion: Angiography and TAE are recommended as the first-line diagnostic and treatment choice for DPPAB, respectively. Surgical intervention should be preserved to eliminate the cause of bleeding. Copyright © 2011 S. Karger AG, Basel and IAP

Abstract Objective: To investigate the diagnosis and treatment of delayed post-pancreaticoduodenectomy arterial bleeding (DPPAB). Methods: Records of 336 patients who underwent pancreaticoduodenectomy (PD) between January 2000 and December 2010 were retrospectively analyzed. Detailed data of patients with DPPAB were assessed by a thorough review of medical records. Results: 14 patients developed DPPAB. The mean time interval between the initial surgery and DPPAB was 33 days (range 7–72). Three patients experienced sentinel bleeding 5–8 days before DPPAB. All DPPAB patients had intra-abdominal septic complications before bleeding. The overall prevalence of success of angiography and transcatheter arterial embolization (TAE) was 85.7% (12/14), including 3 patients who achieved complete hemostasis by TAE after unsuccessful re-laparotomy. The prevalence of mortality of DPPAB was 28.6% (4/14). After hemostasis was achieved, intra-abdominal septic complications were controlled by percutaneous catheter drainage or re-laparot-

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Although the prevalence of surgical mortality of pancreaticoduodenectomy (PD) has recently fallen to acceptable levels (0–5%) [1–10], the prevalence of mortality can reach 11–60% [10–15] if postoperative arterial bleeding occurs. Post-PD arterial bleeding usually happens late (15 days postoperatively). Because of the lack of a generally accepted definition, the reported prevalence of this fatal complication varies widely (1.5–20.2%) [16–22]. Delayed post-pancreaticoduodenectomy arterial bleeding (DPPAB) is usually massive, with impairment of the peripheral circulation. It occurs suddenly without distinct indications. Efficient and accurate diagnosis and treatment are essential for saving lives under this circumstance. The etiology of DPPAB is not clear. Most authors believe that intraoperative injury to the arterial wall (usually resulting from vessel skeletonization during lymphProf. Chun-Yi Hao, MD Department of Hepatopancreatobiliary Surgery Peking University School of Oncology, Beijing Cancer Hospital No. 52, Fu-Cheng-Lu Street, Beijing 100142 (PR China)

Table 1. Definitions used in the present study

Bile leakage

Presence of bile in the drain fluid with a bilirubin value five times greater than that of serum

Delayed gastric emptying

Need for postoperative nasogastric decompression for >10 days or the need for reinsertion of a nasogastric tube

Intra-abdominal abscess

A ‘pocket’ of infected fluid and pus located inside the abdominal cavity

Hemodynamic instability

Mean arterial pressure <70 mm Hg (normal range 70–110 mm Hg) before resuscitation with intravenous fluids or administration of blood products

Hemodynamic stability

Regular heart rate <100 bpm and mean arterial blood pressure >70 mm Hg

Successful endovascular management

Cessation of hemorrhage without further transfusion requirements, hemodynamic stabilization and persistent organ perfusion

Hepatic infarction

Coexistence of CT findings (geographic, low attenuation perfusion defects without mass effect) seen in association with an acute increase in the serum level of alanine aminotransaminase to >1,000 IU

Surgical mortality

Death occurring during the hospital stay or as a consequence of a postoperative complication

adenectomy) can make the vessel more susceptible to erosive rupture if intra-abdominal septic complications occur around it. Some authors claim that surgical intervention should be the first-line treatment for postoperative massive hemorrhage after pancreatectomy [23, 24]. With recent advances in interventional radiology, transcatheter arterial embolization (TAE) has become more widely used. Various authors researching TAE for postoperative bleeding have reported a prevalence of success of 55–100% [11, 15, 19, 21, 22, 25–28]. In this article, we reviewed our experiences of DPPAB in 14 patients to analyze the prevalence, mortality, and results of diagnostic and treatment procedures of this lethal complication. Patients and Methods The study protocol was approved by the Ethics Committee of Beijing Cancer Hospital (Beijing, China). Between January 2000 and December 2010, 336 patients underwent PD at Beijing Cancer Hospital. The indications for surgery were pancreatic cancer,


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chronic pancreatitis, distal bile duct cancer, malignant duodenal tumor, ampullary carcinoma, as well as any malignant tumor involving the pancreatic head or duodenum. In all patients, PD was undertaken with an antrectomy and reconstruction with an end-to-side pancreaticogastrostomy or pancreaticojejunostomy. Pancreaticogastrostomy was carried out by hand-sewing with absorbable monofilament sutures on the posterior wall of the gastric body. The pancreas was mobilized 3–5 cm to be well telescoped into the gastric cavity. Pancreaticojejunostomy was done with end-to-side, two-layer sutures. The first layer was a duct-to-mucosa anastomosis, and the second-layer suture was between the capsule of the pancreas and the seromuscle layer of the jejunum. A pancreatic duct stent was usually used in the pancreaticojejunostomy. If the portal vein and/or superior mesenteric vein was involved, resection of the mesentericoportal vein and an end-to-end anastomosis were carried out as reported previously [29]. The stump of the gastroduodenal artery (GDA) was left around 5 mm long and closed with a suture ligature. In patients with cancer, lymphadenectomy was routinely undertaken with skeletonization of the hepatic artery from the hepatic pedicle to the celiac axis along with removal of the retroportal pancreatic lamina on the right aspect of the superior mesenteric artery. After completion of the resection and reconstruction, rubber drains were placed near the biliary and pancreatic anastomosis. The drains were removed progressively from postoperative day (POD) 7. Parenteral antibiotics and octreotide acetate were administered to all patients prophylactically. When the drain fluid turned cloudy with sediment before the abdominal drain was removed, a low-speed intermittent irrigation was added until the drain fluid returned clear. When intra-abdominal collection was detected, an ultrasound-guided percutaneous drainage was performed. DPPAB was defined based on the definition of post-pancreatectomy hemorrhage (PPH) proposed by the International Study Group of Pancreatic Surgery (ISGPS) [30] except that the cut-off point we chose for DPPAB was POD 5. The cases were classified into ISGPS grades A, B and C, and categorized into intraluminal or extraluminal, mild or severe. Intraluminal post-PD bleeding referred to bleeding inside the gastrointestinal (GI) tract, and extraluminal post-PD bleeding was intra-abdominal bleeding outside the GI tract. A sentinel bleed was defined as the presence of blood in the drain or GI hemorrhage without obvious cause 24 h before an episode of DPPAB. A postoperative pancreatic fistula was defined according to the International Study Group on Pancreatic Fistula Definition [31]. Hence, a postoperative pancreatic fistula was output via an operatively placed drain (or a subsequently placed percutaneous drain) of any measurable volume of drain fluid on or after POD 3 with an amylase content greater than three times the upper normal serum value. Other definitions used in this article are listed in table 1. Diagnostic procedures for the management of bleeding included routine blood tests, blood and drain-fluid cultures, abdominal ultrasound and/or CT, upper GI endoscopy (diagnostic or therapeutic) and angiography (diagnostic or with angioembolization). In patients with intraluminal bleeding, upper GI endoscopy was routinely done if the patient did not show signs of hemodynamic instability. Surgical interventions for DPPAB included exploration, suture ligation of the bleeding vessel, and removal of the intra-ab-

Zhang et al.

dominal hematoma, as well as drain replacement. Completion of pancreatectomy and re-reconstruction were carried out if pancreatic fistulae and intra-abdominal complications were so serious that drainage alone could not solve the problem. Angiography was undertaken by experienced interventional radiologists in the Angiography Suite to identify the location of bleeding and evaluate the potential of endovascular treatment according to the surgeon’s request. Angiography and interventional embolization were achieved by puncturing the common femoral artery. The catheter was then advanced in the visceral aortic branches (i.e. hepatic artery, GDA, splenic artery (SPA), superior mesenteric artery). Embolization was carried out using a coaxial technique and microcoils. Vascular stents were not available in our hospital. All procedures were done under local anesthesia. Patients were monitored by electrocardiography and blood-pressure measurements. Arterial and portal venous phases were assessed to detect the site of bleeding and to exclude portal vein thrombosis. After embolization, patients were closely observed for re-bleeding or embolization-related ischemia. Re-bleeding after embolization was treated by re-embolization. Detailed data of patients with DPPAB were retrospectively assessed by a thorough review of medical records from the Beijing Cancer Hospital Clinical Database, a prospectively kept database that was set up 30 years ago. The parameters that were analyzed were: postoperative interval between PD and bleeding; manifestations of bleeding; associated complications (delayed gastric emptying, pancreatic fistula, intra-abdominal abscess); amount of bleeding; number of units of blood transfused; diagnostic procedure; bleeding site; etiology of bleeding; treatment strategy; mortality; success in controlling bleeding, and outcome.

Table 2. Indications for surgery in the 14 patients with DPPAB



Pancreatic head carcinoma Pancreatic neuroendocrine tumor Solid pseudopapillary tumor of the pancreas Ampullary carcinoma Distal cholangiocarcinoma Gallbladder carcinoma Relapsed colonic carcinoma involving the duodenum

8 1 1 1 1 1 1

A total of 188 male and 148 female patients underwent PD between January 2000 and December 2010 at our hospital. The median age of all patients was 59.7 years (range 14–83). The overall prevalence of surgical mortality was 3%. Among them, 14 (4.2%) developed DPPAB (including 2 patients who experienced two episodes of bleeding). Indications for surgery in patients with DPPAB are listed in table 2. At the time of PD, the 14 patients who developed DPPAB (10 males, 4 females) had a median age of 58.9 years (range 25–73). The prevalence of mortality in the DPPAB group was 28.6% (4/14). The median time interval between the initial surgery and the definitive diagnosis of bleeding was 33 days (range 7–72). According to the ISGPS definition [30], there were 10 extraluminal and 4 intraluminal bleedings. All the cases were classified into ‘severe’ and ISGPS grade C. All the cases had intra-abdominal septic complications that resulted from pancreatic fistula in 11 patients (78.6%), bile leakage in 7 (50%), and intra-abdominal collections in 10 (71.4%). The site of bleeding was GDA in 4 patients, common hepatic artery (CHA) in 3, left hepatic artery (LHA)

in 2, SPA in 2, right hepatic artery (RHA) in 1, and celiac trunk in 1. Definite identification of the site of bleeding could not be achieved by angiography in 1 patient. Basic characteristics of the DPPAB patients are listed in table 3. Three patients (Nos. 1, 3, 7) had sentinel bleeding before DPPAB. The mean time interval between sentinel bleeding and DPPAB was 7 days (range 5–8). No evident bleeding source was demonstrated. After initial resuscitation, the 4 patients (Nos. 2, 4, 7, 8) with intraluminal bleeding underwent upper GI endoscopy without a demonstrable bleeding source. After unsuccessful conservative therapy, they underwent angiography and coil embolization. The bleeding site was RHA in patient 2, SPA in patient 4, LHA in patient 7, and GDA in patient 8. All of these patients had hepatojejunal anastomostic insufficiency and intra-abdominal collections around the anastomosis. In all of these patients, angiography showed extravasation of contrast medium from the ruptured artery, and then accumulation in the intra-abdominal collections around the hepatojejunal anastomosis before it came through the ruptured anastomosis into the jejunum. Two patients experienced re-bleeding after initial embolization. One accepted re-embolization, the other re-laparotomy with ruptured vessel suture ligation. The outcomes of these patients were uneventful. Three patients (Nos. 5, 10, 12) underwent a laparotomy immediately after DPPAB. All of them had serious intraabdominal septic complications before bleeding. Blood loss via abdominal drains was noticed 11 days after the initial procedure for patient No. 5. A decrease in hemoglobin level of 6 g/dl was recorded. Laparotomy showed erosive rupture on one small branch of the CHA. The ruptured artery was oversewn with completion pancreatectomy, splenectomy, and by replacing abdominal drains. On POD 23, the patient underwent re-laparotomy because of re-bleeding without a demonstrable bleeding source. Serious gastrojejunal anastomotic insufficiency

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Table 3. Basic characteristics of DPPAB patients

Patient No.

Age years



Bleeding source

Interval days


Intra-abdominal complications

1 2 3 4 5

70 73 50 35 52




44 37 48 26 10



6 7 8 9 10

69 70 67 64 71




7 8 72 63 31

11 12 13 14

58 25 67 54


PHC SPT PHC Relapsed colonic carcinoma involving the duodenum


50 41 18 10




SB = Sentinel bleeding; PHC = pancreatic head cancer; AC = ampullary carcinoma; PET = pancreatic endocine tumor; DCC = distal cholangiocarcinoma; GC = gallbladder carcinoma; SPT = solid pseudopapillary tumor of the pancreas; CHA = common hepatic artery; RHA = right hepatic artery; CT = celiac trunk; SPA = splenic artery; GDA = gastroduodenal artery; LHA = left hepatic artery; NA = not answered; PF = pancreatic fistula; BL = bile leakage; IAC = intra-abdominal collection; IAI = intra-abdominal infection; WI = wound infection.

was recorded. Severe edema of the stomach and jejunum made it extremely difficult to fix the anastomosis. New drains were placed around the anastomosis with a jejunostomy. One day later, the patient experienced another episode of bleeding. Angiography was done followed by coil embolization of the ruptured CHA. Evident bleeding was not recorded afterwards. However, the patient underwent two more laparotomies because of intra-abdominal septic complications. The patient died of multipleorgan failure from severe infections on POD 122. DPPAB occurred 30 days postoperatively in patient No. 10. Immediate laparotomy showed erosive rupture of the CHA, hepatojejunal anastomotic insufficiency, and intra-abdominal collections. The CHA was oversewn with T-tube drainage of the hepatojejunal anastomosis and replacement of intra-abdominal drains. Re-bleeding occurred on POD 56 as observed by angiography. The bleeding source was a ruptured CHA proximal to the previously oversewn site. Coil embolization was carried out. Endovascular intervention and follow-up drainage proved successful with an uneventful outcome. Patient No. 12 underwent laparotomy after DPPAB on POD 40, but the bleeding source could not be identified due to severe ad458

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hesion and infection. Follow-up angiography on POD 41 showed an erosive ruptured SPA. Coil embolization was successful. No further event was recorded after endovascular interventional therapy. Of the 14 patients in our study, 11 underwent angiography immediately after the diagnosis of DPPAB. Nine of these patients experienced successful coil embolization with no further complications. DPPAB occurred in patient No. 3 on POD 48. Angiography showed serious extravasation at the celiac trunk. Coil embolization was undertaken, but bleeding could not be controlled. The patient died of disseminated intravascular coagulation the next day. Erosive rupture at the GDA stump caused DPPAB in patient No. 13 on POD 18. Angiography and coil embolization were successful on the day of treatment. However, the patient suffered allergic hemolysis 1 day after the embolization and died on POD 21. In the 3 DPPAB patients who underwent laparotomy as initial treatment, bleeding could not be controlled due to severe intra-abdominal adhesion and infection. Subsequent angiography and coil embolization recognized and controlled the bleeding. Overall, the success of endovascular intervention was 85.7% (12/14). Zhang et al.

Table 4. Management and outcome in DPPAB patients Patient First-line management No. management site of TAE surgery

ReSecond-line management bleeding surgery site of TAE hemostasis



1 2 3



Complete Complete Incomplete

No Yes No

IAI, MOD. Died

4 5

AG+TAE Laparotomy


Complete Incomplete


6 7 8 9 10 11 12 13



No No No No


Complete Complete Complete Complete Incomplete Complete Incomplete Complete






CHA oversewn + CP + splenectomy + redrainage

CHA oversewn + redrainage No-TAE CHA oversewn + redrainage



Complete Bleeding could not be controlled. Died

RePHA drainage






IAI, MOD. Died

No Yes


Allergic hemolysis. Died

TAE = Transcatheter arterial embolization; AG = angiography; CHA = common hepatic artery; RHA = right hepatic artery; SPA = splenic artery; No-TAE = negative angiographic finding without TAE; PHA = proper hepatic artery; CP = completion pancreatectomy; IAI = intra-abdominal infection; MOD = multiple-organ dysfunction.

Delayed post-pancreatectomy arterial bleeding is a rare but fatal complication. Without a consensus definition, the reported prevalence and mortality of it are varied. In 2007, the ISGPS [30] proposed an objective, universally applicable definition and classification of this unique complication. According to their definition, the bleeding was termed PPH. However, the cut-off point they used for DPPAB was 24 h after surgery. When referring to post-pancreatectomy bleeding, most authors claimed that bleeding at the early and late stage should be categorized as different entities [10, 12, 19, 22, 23, 32, 33]. Late bleeding after PD usually occurred 15–7 days postoperatively, with the time interval between the index operation and delayed bleeding ranging from 5 to 206 days [11, 20, 21, 25, 27, 34–37]. In our study, the mean time of DPPAB was 33 days (range 7–72) postoperatively. Erosive rupture of visceral arteries that can cause massive bleed-

ing seldom occurs before POD 5. Hence, we defined DPPAB as all episodes of post-PD bleeding after POD 5. This was similar to the definition proposed by Choi et al. [38] for delayed massive hemorrhage. The ISGPS classified PPH as ‘intraluminal’ or ‘extraluminal’ according to the location of bleeding. However, the clinical signs of DPPAB can be misleading. A cascade of events (e.g. anastomotic insufficiency; pancreatic or bile leakage; intra-abdominal collections and abscess formation; visceral arterial erosion) may occur before massive bleeding. Blood from the ruptured artery can pass through an insufficient anastomosis into the GI tract. In the present study, 4 patients experienced GI bleeding without the presence of blood in their abdominal drains. Upper GI endoscopy could not demonstrate a definite bleeding source. Angiography showed extravasation of contrast medium into the GI tract. DPPAB is always dramatic and fatal. Angiography can recognize the bleeding source and re-establish hemodynamic stability efficiently. So, for hemodynamically unstable intraluminal PPH patients, we suggest to perform angiography first. Endoscopy could be carried out for hemodynamically stable patients or for further diagnosis after the hemodynamic stability has been re-established (fig. 1).

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Endovascular stents are not available at our hospital. Hence, stents were not used for DPPAB. The management and outcome of DPPAB patients are listed in table 4.



Hemodynamically stable


Bleeding source visualized

Endoscopic hemostasis or conservative therapy or re‐laparotomy


Bleeding source not visualized

DPPAB Hemodynamically unstable

Bleeding  source   not visualized Angiography Re‐laparotomy

Extraluminal Bleeding source visualized

Coil or covered stent

DPPAB not controlled

DPPAB controlled

Fig. 1. Algorithm for the management of DPPAB in Beijing Cancer Hospital.

DPPAB is always dramatic, with a sudden fall in hemoglobin levels and blood pressure. Efficient and accurate diagnosis is crucial. CT has been recommended by some authors [30, 32, 37, 39]. For other authors, surgery is the first choice for the diagnosis and treatment of DPPAB [18, 23, 24, 36]. We believe that time is the key factor that can influence the survival of DPPAB patients. CT may find the bleeding site but cannot facilitate prompt treatment. Identifying the bleeding site and stopping bleeding by suturing can be achieved at a single laparotomy. However, patients with DPPAB might be poor candidates for emergency surgery because of hemodynamic instability and being critically ill [40]. The burden of general anesthesia and extensive surgery would deteriorate his/her condition further or threaten life. Also, reaching the bleeding site at re-laparotomy is often hazardous due to dense adhesion, considerable inflammation, and massive bleeding. In the present study, 3 patients underwent laparotomy before angiography. Ruptured arteries were identified and oversewn in 2 patients, but re-bleeding occurred shortly after. A definite bleeding source could not be identified during laparotomy in the other patient. All of these patients subsequently underwent angiography and embolization with successful results. The development of interventional radiology has led to a minimally 460

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invasive approach to control bleeding with a satisfactory outcome. The success of TAE in the present study was 85.7%, comparable with that reported by other authors [11, 15, 19, 21, 22, 25–28]. We therefore suggest angiography and intravascular embolization as the first-line diagnostic and treatment choice because it is time-saving and effective. After bleeding control, re-laparotomy can be undertaken in hemodynamically stable patients (if necessary). Surgery still plays an important part (especially in eliminating the cause of bleeding). Hemodynamic stability re-established by TAE cannot last if the intra-abdominal septic complication persists. Control of infection can be achieved by completion pancreatectomy, tube pancreatostomy, or appropriate placement of drainage tubes if percutaneous aspiration or catheter drainage fails. If angioembolization fails to stop the bleeding, laparotomy should be carried out. Two patients in our study experienced another episode of bleeding after TAE not because of coil migration but because of uncontrolled infection. Surgical treatment is highly recommended under this circumstance. The liver can tolerate considerable arterial embolization because of its multiple collateral pathways, mainly via subphrenic arteries. As long as subphrenic arteries are Zhang et al.

well developed and the patency of the portal vein is preserved, TAE proximal to the PHA should lead to a successful outcome. However, TAE proximal to the PHA usually risks occlusion of the CHA with the subsequent increased risk of necrosis and liver failure [21, 38]. In our study, embolization of the PHA was needed in 3 patients (Nos. 6, 8, 9). Three patients (Nos. 1, 5, 10), including 1 who underwent segmental portal vein resection during PD, had their CHA embolized. A temporary increase in transaminase levels was recorded without liver failure in all of these patients. It was reported that the prevalence of liver abscess after embolization of the hepatic artery can be 130% [13, 21, 41]. Only 1 patient (No. 1) developed multiple liver abscesses after embolization. He died of multiple-organ dysfunction as a result of severe intra-abdominal infection 103 days after embolization. Although the prevalence of liver failure and abscess formation was relatively low in the present study, uneventful outcomes cannot be guaranteed if the PHA or CHA have to be occluded. The recent use of covered stents has proved to be a successful solution because they arrest bleeding while preserving vessel patency. Covered stents are not available in our institute. We believe that, with the use of covered stents, the prevalence of post-embolization hepatic ischemia could be decreased. Based on our experience and literature review, we suggest a diagnostic and therapeutic algorithm for the management of DPPAB (fig.  1). When a DPPAB was confirmed, it should be classified as intraluminal or extraluminal according to the ISGPS definition and classification [30]. If the intraluminal DPPAB patient is hemodynamically stable, endoscopy should be performed. If the bleeding source could be visualized, the subsequent therapy should be endoscopic hemostasis, or conservative therapy, or re-laparotomy according to the patient’s condition. If the bleeding source could not be visualized, angiography should be performed. For extraluminal DPPAB patients and hemodynamically unstable intraluminal DPPAB patients, angiography is the first-line diagnostic procedure. When an evident bleeding source could be demonstrated by angiography, coil embolization or covered stent should be performed to stop the bleeding. If the interventional management could not stop the bleeding, or angiography could not recognize the bleeding source, re-laparotomy is inevitable. Percutaneous drainage or surgical management should be considered to eliminate the cause of DPPAB after the bleeding has been stopped and hemodynamic stability re-established. According to our knowledge, there is no guideline that is widely accepted for DPPAB prevention. We be-

lieve two aspects should be emphasized. Firstly, post-PD complications should be managed efficiently. The etiology of DPPAB is controversial, but most authors believe that erosive damage of visceral arteries is the main cause. It has been proposed that pancreatic juice, intestinal juice and/or bile from a leaking anastomosis can erode the arterial wall (especially if the visceral artery is injured by vessel skeletonization during lymphadenectomy). In addition, anastomostic insufficiency is usually followed by localized infection and abscess formation in intra-abdominal spaces, which can further erode the arterial wall [10, 18, 20, 23, 27, 30, 40, 42–44]. In the present study, all patients had intra-abdominal septic complications. A total of 78.6% (11/14) patients had a pancreatic fistula before DPPAB. Our finding is consistent with the literatures by Sato et al. [21], Yekebas et al. [22] and Choi et al. [38] who reported a significantly elevated risk of DPPAB in patients with pancreatic fistula. Wei et al. [45] confirmed that pancreatic leakage and intra-abdominal abscess are independent risk factors for post-PD bleeding. Hence, any procedure that can prevent the formation of pancreatic fistula or intra-abdominal abscess can decrease the prevalence of DPPAB. Nakano et al. [46] reported that prophylactic irrigation around a pancreaticojejunostomy could decrease the incidence of pancreatic fistula and infectious complications. We did not perform drain irrigation prophylactically, but a low-speed intermittent irrigation was added when the drain fluid turned cloudy with sediment. Besides, an ultrasoundguided percutaneous drainage was performed when intra-abdominal collection was detected. When the patients experienced ISGPF [31] grade B/C pancreatic fistula, octreotide acetate were administered and drain replacement or surgical intervention were performed according to the patient’s condition. Although a controlled randomized trial is needed, a prompt and effective treatment of post-PD complications is always important to prevent DPPAB. Secondly, sentinel bleeding should not be neglected. Sentinel bleeding has been reported to precede delayed bleeding in 25–100% of cases [10–12, 19, 23, 27, 35]. This probably reflects local sepsis and probable anastomotic dehiscence [20, 32]. Tien et al. [47] recommended angiography for every sentinel bleeding after PD. In the present study, 3 patients showed sentinel bleeding 5–8 days before DPPAB. No evident bleeding source was detected. Miura et al. [11] reported 15 cases of postoperative arterial hemorrhage after pancreatobiliary surgery. When sentinel bleeding occurred, angiography was done in 4 patients. However, neither a pseudoaneurysm nor extrav-

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asation was demonstrated. Sentinel bleeding is less likely to be visualized by angiography, possibly due to the intermittent character of hemorrhage [14, 48]. Nonetheless, angiography can identify pseudoaneurysms, which are believed to be the result of erosion of the arterial wall and which can progress to massive bleeding [49]. Pseudoaneurysms can be embolized before they rupture. Surgeons and interventional radiologists should be particularly alert if a post-PD patient experiences sentinel bleeding, especially if an intra-abdominal abscess has been demonstrated.


DPPAB is a rare but fatal complication. The ISGPS proposed an objective and universally acceptable definition of PPH. We suggest the cut-off point for delayed bleeding should be 5 days postoperatively. Angiograghy and TAE are recommended as the first-line diagnostic and treatment choice for DPPAB, respectively, whereas surgical intervention should be preserved to eliminate the cause of bleeding. Occlusion of the PHA or CHA may cause hepatic infarction. Covered stents are recommended if the bleeding source is the PHA, CHA or the stump of the GDA. To prevent DPPAB, post-PD complications should be managed efficiently. Sentinel bleeding should always be taken seriously.

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