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JOP. J (Online) 2017 Jul 31; 18(4):339-344.

CASE SERIES

Portal Vein Bleeding after Pancreatectomy: Diagnosis and Stent Graft Repair - A Consecutive Case Series

Kojiro Suzuki1,2, Tomoki Ebata3, Tomohiro Komada2, Masaya Matsushima2, Takashi Mizuno3, Tsuyoshi Igami3, Gen Sugawara3, Yukihiro Yokoyama3, Shinji Naganawa2, Masato Nagino3

1

2 Department of , Aichi Medical University, 1-1 Yazako Karimata, Nagakute, 480-1195, Japan

3 Department of Radiology, Nagoya University Graduate School of , 65 Tsurumai-cho, Showa- ku, Nagoya, 466-8550, Japan Division of Surgical Oncology, Department of Surgery, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, 466-8550, Japan ABSTRACT Objective Postoperative bleeding is a severe complication that can occur after pancreatectomy. Bleeding mainly arises from peripancreatic , but the portal venous system can also rarely cause bleeding. This study assessed portal vein bleeding after pancreatectomy. Methods

Between November 2013 and August 2016, five patients (three males, two females; median age, 75 years; age range,Results 66-78 Allyears) patients with developed postoperative pancreatic portal veinleakage bleeding after surgery. underwent stent graft demonstrated repair. Angiography portal vein and fistulography were in one performed patient inand four no evidenceand five patients, of bleeding respectively. in the other Patients three werepatients. retrospectively Fistulography analyzed demonstrated with regard the peritonealto radiological cavity findings with pancreatic and clinical leakage outcome. connecting patients were discharged and one patient died of multiorgan failure in hospital. Conclusions Fistulography is useful to depict sources of with the portal venous system in all five patients. Stent grafts achieved hemostasis with portal flow preservation in all patients. Four portal vein bleeding. Stent grafts appear to offer effective treatment for portal vein bleeding after pancreatectomy. INTRODUCTION bleeding after pan comparing endovascular therapy and laparotomy for Despite declining mortality rates after pancreatic postpancreatectomy bleedingcreatectomy. have revealed Systematic that hemostasis reviews surgery, postoperative bleeding remains one of the most

stays about the same (endovascular therapy, 76-80%; serious complications, particularly in high-volume centers with endovascular therapy appears lower than that with laparotomy, 73-76%).vs. However, the mortality rate associated. structures[1, 2, 3]. Bleeding that may occurs be sources in 1-8% of of bleeding cases, but are accounts mainly thefor stump11-38% of of the mortality gastroduodenal [4, 5, 6]. , The peripancreatic hepatic artery, vascular splenic laparotomyAs to bleeding (20-22% from 43-47%, the portal respectively) vein, no [10, case 11] series artery, or a branch of the superior mesenteric artery [1, 3, . Although quite a rare occurrence, the portal venous appear to have been reported. We describe herein the five system can also be a source of postoperative bleeding. The the portal vein after pancreatectomy in which stent graft consecutive patients with intra-abdominal bleeding from frequency4, 5, 6] of portal vein bleeding after pancreatectomy is repair was performed. MATERIALS AND METHODS reportedly <1% (0.1-0.7%) [7, 8, 9]. Like arterial bleeding, Patients portalWith vein recent bleeding advances also can in cause interventional morbidity [7].procedures, used, gaining acceptance for the treatment of arterial retrospective collection of data and data analysis for this embolization and stent grafts have been widely study,Our and institutional the requirement review for informed board consent approved from the Received Accepted patients was waived. Between November 2013 and August Keywords Correspondence April 28th, 2017- May 10th, 2017 Department , of Radiology False; Pancreas; Pancreatectomy; Portal vein Aichi Medical University Kojiro Suzuki vein2016, bleeding five consecutive after pancreatic patients surgery (three underwent males, two placement females; ofmedian a stent age, graft 75 at years;the portal age vein. range, The 66-78 primary years) tumor with was portal bile

Tel1-1 Yazako Karimata, Nagakute duct carcinoma in two patients, and gall bladder carcinoma, Fax480-1195, Japan ampullary carcinoma, and metastatic pancreatic tumor from E-mail +81-561-62-3311 renal cell carcinoma in one patient each. +81-561-63-3268 [email protected] JOP. Journal of the Pancreas - http://pancreas.imedpub.com/ - Vol. 18 No. 4 –Jul 2017. [ISSN 1590-8577] 339 JOP. J Pancreas (Online) 2017 Jul 31; 18(4):339-344.

The resection procedure for the tumor was and clinical outcome. To clarify the effects of stent graft pancreaticoduodenectomy in three patients, extrahepatic repair, results were assessed with regard to technical resection and partial resection of the pancreatic head in one patient, and distal pancreatectomy in one patient. Two patients also underwent right hepatectomy thesuccess site of and portal clinical venous efficacy. injury without Technical complication, success wasand and caudate lobectomy combined with resection and defined as exact deployment of the stent graft to cover reconstruction of the portal vein. afterpreservation stent graft of deployment. portal flow at final angiography. Clinical Stent Graft Procedures efficacy was defined as freedom from portal vein bleeding Placement of a stent graft was performed as follows. In RESULTS Clinical and Radiological Findings the first patient, definitive surgical repair for portal vein bleeding was attempted at the start. However, surgical Table 1 abdominal adhesions. The therapeutic strategy was thus Clinical and radiological findings are summarized in changedrepair was intraoperatively difficult because to of stent severe graft postoperative deployment. intra- The Group on. AllPancreatic five patients developed grading [12], pancreatic four patients leakage sufferedafter pancreatectomy. grade B pancreatic According leakage to the International and one patient Study portal venous system was accessed by an ultrasound- guided transhepatic approach. An 18-gauge Cliny suffered grade C pancreatic leakage. ultrasound puncture needle (Create Medic, Yokohama, Japan) was placed into a peripheral portal vein branch days)Intra-abdominal after initial surgery. bleeding All through patients the were intraoperatively managed by portalof the vein. left Direct lateral segment of was the then liver. performed The Seldinger using placed drains was identified 10-14 days (median, 11 technique was used to place a 5-Fr sheath into the main transfusion of red blood cell and/or intravenous fluids. a 4-Fr . The diameter and length of the portal vein According to the International Study Group of Pancreatic and the superior mesenteric vein were measured. The 5-Fr Surgery grading [13], four patients suffered grade B Then, a stent graft was deployed from the superior Emergency angiography was performed as the initial sheath was exchanged for a 12-Fr sheath over a guidewire. bleeding and one patient suffered grade C bleeding. was performed with a balloon catheter. At the end of the mesenteric vein to the main portal vein. Post-dilatation procedure, the punctured hepatic tract was closed with hepatic,management and superior tool for intra-abdominalmesenteric artery bleeding demonstrated in four patients. Selective angiography of the celiac, common angiography was also acquired as indirect portography. 0.035-inchIn the remaining coils. four patients, stent graft repair was planned from the start. The portal venous system was Indirectno evidence portography of arterial demonstrated bleeding. Venous-phase no evidence of selective venous accessed by a transileocolic approach. The ileocolic

mesentericleakage. However, vein (Figure one patient 1a, b). showed pseudoaneurysm vein was punctured with an 18-gauge needle under at the splenic vein near the confluence with the superior laparotomy. And, a 12-Fr sheath (n=2), 14-Fr sheath mesenteric vein over a guidewire. Direct portography was the peripancreatic drain, traction was placed on the drains (n=1), or 10-Fr sheath (n=1) was inserted to the superior andFollowing contrast mediumangiography was toinjected reposition via the and/or drains exchange in four and length of the portal vein and superior mesenteric vein patients. In three of these four patients, this contrast then performed using a 4-Fr catheter, and the diameter study showed communication between the peritoneal dilatation was performed with a balloon catheter. cavity and portal venous system, indicating portal vein were measured. A stent graft was then deployed. Post- The stent graft was selected based on the diameters bleeding (Figure 2a, b). In the other patient, no bleeding of the portal vein and superior mesenteric vein. A Gore site was identified at that time and tentative bleeding Associates, Flagstaff, AZ) was used in four patients, and Excluder contralateral leg endoprosthesis (W. L. Gore & present.repeated Induring the remainingfollow-up. Atpatient 15 days without after firstangiography, bleeding, fistulography showed the portal vein and re-bleeding was patient. a Fluency stent graft (Bard, Tempe, AZ) was used in one In two patients, the bleeding site was near the bleeding occurred during fistulography, and the portal vein was demonstrated on fistulography. Finally, portal vein. The splenic vein and inferior mesenteric vein were infectionsvein bleeding such as was bacteremia. diagnosed by fistulography in all confluence of the splenic vein and superior mesenteric patients. After fistulography, no patients developed severe The bleeding site of the portal venous system was the graftthus deployment. embolized with 0.035-inch coils and/or Amplatzer vascular plug (St Jude Medical, St Paul, MN) before stent superior mesenteric vein and portal vein in one patient, Assessments themain stump portal of the vein splenic in two vein patients, in one patient, the confluence and the splenic of the diagnosis of portal vein bleeding, stent graft deployment, the bleeding site was where the operatively placed Patients were analyzed with regard to clinical findings, vein near the confluence in one patient. In four patients,

JOP. Journal of the Pancreas - http://pancreas.imedpub.com/ - Vol. 18 No. 4 –Jul 2017. [ISSN 1590-8577] 340 JOP. J Pancreas (Online) 2017 Jul 31; 18(4):339-344.

Table 1. Initial surgical procedure Intra- Diagnosis of PV bleeding Clinical and radiological findings. Pancreatic Patient Primary PPH abdominal Age/Sex Combined resection fistula Angiography Fistulography No. tumor Type of gradingc bleeding after gradingb pancreatectomy Hepatectomy PVR surgery Distal 1 bile duct PD a B 11 days + carcinoma 75/M Ampullary - - C - 2 PD B B 13 days + carcinoma PR of pancreatic 3 69/F - +- B B 14 days + carcinoma head 66/M Metastatic RH - 4 pancreatic DP B B 10 days + tumor 77/M Diffuse PR of S3, 8 - - bile duct PD + B 10 days +d + carcinoma 5 78/F RH C PVR RH rightDP distal hepatectomy pancreatectomy with resection with splenectomy; of the caudate PD lobepancreaticoduodenectomy; and extrahepatic bile duct PPH postpancreatectomy hemorrhage;a Right hepatic PR lobe partial was resection;previously PV resected portal duevein; to liver portal metastasis vein resection from colon and cancer reconstruction; b c International Study Group on Pancreatic Fistula (ISGPF) definition d Pseudoaneurysm of portal venous system International Study Group of Pancreatic Surgery (ISGPS) definition a b c

Figure 1. (a). Indirect portography after selective celiac arteriography and (b). (c). Patient No. 5: 3-dimensional CT angiography show pseudoaneurysm of the splenic vein near the confluence (arrow). Portography after stent graft deployment (arrowhead) shows good portal flow. The splenic vein (white arrow) and inferior mesenteric vein (black arrow) are embolized with a vascular plug and coils, respectively. a b c

Figure 2.

Patient No. 3: (a). Fistulography from the drain shows the cavity of the pancreatic leakage that communicates with the portal venous system. (b). Direct portography from the superior mesenteric vein shows contrast extravasation into the tract of the drain. (c). Portography after stent graft deployment shows no contrast extravasation and good portal flow. JOP. Journal of the Pancreas - http://pancreas.imedpub.com/ - Vol. 18 No. 4 –Jul 2017. [ISSN 1590-8577] 341 JOP. J Pancreas (Online) 2017 Jul 31; 18(4):339-344.

therapy using warfarin after placement of a stent graft. veinperipancreatic pseudoaneurysm, drain crossed the bleeding on both site was fistulography separate from and discontinued in one of the three patients because of poor thecomputed drain, buttomography was enclosed (CT) byscan. pancreatic In one patient leakage. with portal generalHowever, condition. anticoagulation All three patients therapy remained was immediatelyfree of stent Stent Graft Repair DISCUSSIONgraft thrombus during follow-up. Table 2. The interval between primary surgery and stent Although the exact mechanisms underlying The results of stent graft repair are summarized in postpancreatectomy bleeding remain elusive, pancreatic patients, stent grafts were successfully deployed to cover graft deployment was 10-25 days (median, 13 days). In all andleakage pancreatic and localized juices likely infection weaken are thoughtand erode to representthe blood (Figurethe site 1c, of portal2c). venous injury. And, final portography vesselmajor contributorswalls. Mechanical [5, 14]. irritation The effects by ofthe localized drain is infection another after stent graft deployment showed good portal flow Thus, clinical efficacy was achieved in all occurred in all patients, and the drain was in contact with fiveClinical patients. Course cause of bleeding [15]. In our series, pancreatic leakage articles of portal vein bleeding have also reported bleeding Table 3. the bleeding site in four of the five. patients. Previous Clinical courses after stent graft placement are summarizedpatients remained in free of The further follow-up portal period vein wasbleeding. 2-23 sitesIndirect in proximity portography to the drain following [16, 17]selective arteriography months (median, 9 months). After the procedure, the could not detect a bleeding source in three of the four Four patients were discharge in good health, but the patients. Previous article has also reported postulated remainingThus, clinical patient efficacy died wasof multiorgan achieved infailure all five two patients. months after placement of a stent graft. intermittent bleeding or a venous origin of bleeding, which causes of false-negative angiography, including pauses in indirect portography could demonstrate pseudoaneurysm atis difficultthe splenic to identify vein. Burke after et arteriography al. [2]. In one patient, During follow-up, patency of the stent graft was in which portal vein pseudoaneurysm was diagnosed by assessed by Doppler ultrasonography and/or contrast- graft was occluded with thrombus after 13 months in indirect portography. When arteriography [17] reported fails a similar to identify case enhanced CT scan every three-six months. The stent a bleeding source, consideration of the possibility of patient. The two earliest patients had not been receiving bleeding from the portal venous system is also important. the first patient, and after four months in the second chronic anticoagulation therapy. Systemic anticoagulation threetherapy patients was initiated therefore after received stent graft chronic occlusion. anticoagulation However, patients.On the Fistulography other hand, fistulography demonstrated was not helpful only to a identify cavity recanalization of portal flow was not achieved. The last bleeding sites involving the portal venous system in all five Table 2. Patient SG after PV SMV SG Combined Technical Stent grafts forBleeding portal vein site bleeding.Approach SG diameter SG length No. surgery diameter diameter deployment embolization success

1 11 days Transhepatic 13 mm Confluence of 2 13 days Main PV Transileocolic 159 mm mm PV-SMVPV 16-14.510 mm mm 7040 mm IMV, SpV, LGV Yes SMV and SpV a 3 14 days Main PV Transileocolic 14 mm 811 mm mm - Yes 4 10 days Transileocolic 13 mm PV-left PV 16-14.5 mm 70 mm - Yes Stump of SpV Transileocolic 1513 mm 10 mm PV-SMV 16-14.5 mm 70 mm - Yes 5 25 days SpV PV-SMV 16-12 mm 70 mm IMV, SpV Yes aRight hepatic lobe had already been resected by intimal surgery IMV inferior mesenteric vein; LGV left gastric vein; PV portal vein; SG stent graft; SMV superior mesenteric vein; SpV splenic vein Table 3. Clinical Patient No.Clinical course after stentDischarge graft deployment.SG Occlusion Chronic Anticoagulation Follow-Up Cause Of Death Efficacy 1 13 months Recurrence

2 Yes Yes 4 months - 23 months (dead) 3 Yes Yes -+ 9 months (dead) LiverRecurrence failure 4 Yes Yes - + 12 months (dead)

a b Yes NoYes - + 7 months (alive) Multiorgan failure SG5 stent graft Yes - 2 months (dead) a b Anticoagulation was discontinued because of poor general condition Arterial bleeding from the pancreatic cut surface was embolized five weeks after stent graft deployment

JOP. Journal of the Pancreas - http://pancreas.imedpub.com/ - Vol. 18 No. 4 –Jul 2017. [ISSN 1590-8577] 342 JOP. J Pancreas (Online) 2017 Jul 31; 18(4):339-344. associated with leakage, but also the portal vein, indicating CONCLUSION et al et al. In conclusion, the portal vein has the potential to portal vein bleeding. Yoshida . [8] and Ginsburg [16] also described the utility of fistulography to diagnose Fistulography appears useful in diagnosing portal vein bleeding,cause intra-abdominal and placement bleeding of a afterstent pancreaticgraft is availablesurgery. modalityportal vein to elucidate bleeding. bleeding Our study sites agreesof the portal with vein. previous reports, and fistulography seems to offer the valuable as a therapeutic option for portal vein bleeding after pancreatectomy. pancreatectomy may depend on the clinical presentation. ReportedChoice approaches of treatment to for treatment portal vein include bleeding surgical after Conflict of Interest . repair [9, 17], stent grafting [16], and temporary balloon interest. occlusion and conservation [8] In our first patient, we The authors declare that they have no conflict of thereforeabandoned changed definitive to stent surgical graft repair repair because intraoperatively. of severe intra-abdominal adhesions. The treatment strategy was References Our experience with this patient led us to select stent 1. The use of stent grafts in the treatment of postoperative grafts as the first-line treatment in the next four patients. Correa-Gallego C, BrennanMF, D'Angelica MI, Dematteo RP, Fong Y, Kingham TP, et al. Contemporary experience with postpancreatectomy hemorrhage: results of 1,122 patients resected between 2006 and 2011. J Am2. Coll Surg 2012; 215:616-21. 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