Postoperative arterial bleeding after gastrointestinal surgery is a potentially fatal complication. The reported incidence of arterial bleeding after gastrointestinal surgery, which depends on the surgical site, varies from 0.9% to 15%.^1–4

Traditionally, surgical repair is performed as a standard treatment option. However, the bleeding site is difficult to establish because of local inflammatory response after surgery.⁵ In addition, patients with postoperative gastrointestinal bleeding are reported to be poor candidates for emergency surgery because of cicatrization and the friability of postoperative tissues.^5,6 Therefore, transcatheter arterial embolization (TAE) has been considered a less invasive alternative treatment option despite the risk of organ infarction.⁷ Furthermore, with the recent advances in endovascular devices, stent-graft placement, which can preserve arterial flow, is recommended as a first-line treatment option in patients with suitable anatomy.⁸ However, according to recent reports of stent-graft placement for pseudoaneurysm of hepatic arteries, stent-graft patency rates decreased over time.⁹ This review discusses the techniques and clinical outcomes of interventional management for postoperative arterial bleeding in gastrointestinal surgery.

Enhanced computed tomography (CT) using multi-detector row CT is a standard imaging modality for postoperative arterial bleeding.¹⁰ Enhanced CT has greater availability, speed, and noninvasiveness. Pre-contrast scan is obtained to evaluate hemorrhage. Hemorrhage with high-attenuation mass may be masked after contrast administration; therefore, pre-contrast scan is essential.² Contrast scans of early and late phases using intravenous bolus injection of contrast medium are performed to evaluate arterial abnormalities including extravasation, pseudoaneurysm, and irregularity. Moreover, contrast scans can provide information on portal flow and vascular anatomy for pre-interventional planning.¹¹ In an animal model, CT angiography was shown to detect bleeding rates as low as 0.3 mL/min more successfully than conventional angiography.¹²

Angiographic findings

The typical angiographic findings of arterial bleeding are visualization of the extravasation of contrast medium and pseudoaneurysm. Chatani et al⁴ reported extravasation and pseudoaneurysm in 12 of 28 (42.9%) and 12 of 28 (42.9%) procedures for bleeding after abdominal surgery, respectively. Other indirect signs of bleeding on angiography include irregular arterial wall, vessel spasm, and cut-off.¹⁰ With reference to clinical information and enhanced CT findings, areas with other indirect signs should be selected even in the absence of typical findings (Fig. 1). Moreover, contact with the surgical clip and surgical drain tube may cause arterial bleeding (Fig. 2).

Figure 1. Indirect signs of bleeding on angiography after gastrectomy. (A) Enhanced computed tomography shows intra-abdominal hemorrhage around the liver surface and surgical clip (arrows). (B) Superior mesenteric artery angiography shows no extravasation and pseudoaneurysm (arrow, surgical clip). (C) Celiac artery angiography does not show the gastroduodenal artery clearly because of hepatopetal flow. (D) The irregular arterial wall of the anterior superior pancreaticoduodenal artery is observed (arrowhead). The microcatheter is navigated to this portion around the surgical clip, and just after cannulation, extravasation is visualized (arrows). (E) Transcatheter arterial embolization using metallic coils (arrows) is performed.

Figure 2. Continuous slight bleeding from the surgical drain tube after pancreaticoduodenectomy. (A) Enhanced computed tomography shows the inserted surgical drain tube around the left inferior epigastric artery (arrow). (B) Celiac artery angiography shows no extravasation and pseudoaneurysm. (C) Angiography of the left inferior epigastric artery shows no extravasation and pseudoaneurysm. (D) After the surgical drain tube was exchanged to a seeking catheter, angiography shows extravasation to the drain tract (arrows). (E) A microcatheter is navigated to the bleeding point, and the mixture of n-butyl-2-cyanoacrylate and lipiodol (ratio, 1 : 4) is injected after the seeking catheter was exchanged to a guide wire (arrowheads).

Transcatheter arterial embolization

Despite the possibility of organ infarction, TAE has been widely performed for arterial bleeding after gastrointestinal surgery.^4,5,7 In most cases, TAE is performed using a 4-Fr or 5-Fr angiographic catheter with a coaxial 1.7- to 2.4-Fr micro-catheter. When the micro-catheter could not be advanced to the bleeding portion because of tortuous vessel, a triple coaxial system may be useful.¹³ In the case of embolization of the hepatic artery, portal vein (PV) patency should be confirmed through superior mesenteric angiography.⁸

Embolization techniques are classified into isolation, packing, and selective techniques.⁴ Isolation is defined as the embolization of both distal and proximal arteries, packing as the occlusion of the pseudoaneurysm, and selective embolization as the occlusion of the end artery. Basically, the isolation technique should be performed.^4,7 The micro-catheter is advanced to the distal part of the bleeding portion, and metallic coils were deployed from the distal to the proximal part of the bleeding portion, which is also known as the sandwich or trapping technique.^7,14 When navigation to the distal portion was difficult because of a tortuous vessel or spasm, a 20% to 50% mixture of n-butyl-2-cyanoacrylate (NBCA) and lipiodol was used.^10,15 To prevent the distal migration of embolic materials in high-flow condition, arterial flow control with balloon catheter may be useful (Fig. 3). The packing technique is performed when other techniques are not feasible because of the risk of post-embolization ischemia (Fig. 4). Moreover, when catheter navigation to the bleeding point was impossible, percutaneous direct puncture and packing of pseudoaneurysm may be an optional technique.^16,17 However, the packing technique is technically more challenging and frequently associated with bleeding recurrence, which eventually leads to major complications such as mortality.⁷ The selective embolization technique is used for peripheral end artery. In this technique, the micro-catheter is navigated to the bleeding point as distal as possible, and embolization is performed using metallic coils, NBCA–lipiodol mixture, and gelatin sponge (Fig. 5).

Figure 3. Embolization with the isolation technique for bleeding after gastrectomy. (A) CA angiography shows no extravasation and pseudoaneurysm (arrow, SPA stump). (B) SMA angiography shows HAs due to the hepatopetal flow. (C) A 5-Fr balloon catheter is placed at the distal portion of the common HA to prevent distal migration (arrow). (D) Another 5-Fr balloon catheter is placed at the CA to prevent proximal migration. Obvious extravasation is visualized along with the drain tube (arrowheads). (E) Metallic coils are deployed from the distal to the proximal part of the bleeding portion including the SPA stump (arrowheads). (F) SMA angiography shows the patent HAs. CA, celiac artery; SPA, splenic artery; SMA, superior mesenteric artery; HA, hepatic artery.

Figure 4. Embolization with the packing technique for bleeding after pancreaticoduodenectomy with HA reconstruction. (A) Enhanced computed tomography shows pseudoaneurysm (arrow) and intra-abdominal hemorrhage around the liver surface. (B) Celiac artery angiography shows pseudoaneurysm at the reconstructed right HA stump (arrow) and irregular arterial wall of the proper HA. (C) Appropriate SG devices are not prepared given the emergency setting. The pseudoaneurysm was embolized with the packing technique to maintain the HA flow (arrow). (D) Next day, rebleeding occurred, and expansion of the embolized pseudoaneurysm and another pseudoaneurysm at the distal portion are visualized (arrowheads). (E) SG placement using VIABAHN^® is performed (arrowheads). HA, hepatic artery; SG, stent graft.

Figure 5. Selective embolization technique for bleeding after low anterior resection. (A) Enhanced computed tomography shows hemorrhage and extravasation at the abdominal wall (arrowheads). (B) Angiography shows extravasation from the branch of the left inferior epigastric artery (arrow). (C) A microcatheter is navigated to this branch, and extravasation is visualized at the peripheral end artery (arrow). (D) n-butyl-2-cyanoacrylate lipiodol mixture (ratio, 1 : 4) is injected (arrowheads).

Types of embolic agent

With the recent advancements in endovascular devices, embolic agents such as pushable and detachable metallic coils, NBCA, gelatin sponge, particulate embolic materials, and vascular plug are available.^4,18 The choice of embolic agents depends on the combination of the vascular anatomy, angiographic findings, achievable catheter position, and operator’s preference.¹⁸ Detachable coil and vascular plug can reduce the risk of distal migration.¹⁹ NBCA is a liquid embolic material with a non-radiopaque nature; thus, it should be mixed with lipiodol to provide radiopacity and control viscosity.¹⁵ Moreover, adjusting the NBCA–lipiodol mixing ratio is necessary depending on the situation. Usually, the NBCA–lipiodol ratio ranges from 1:1 to 1:4.^20,21 Operators should decrease the amount of lipiodol when attempting to embolize short segments and should increase for long segments. It is advantageous for massive bleeding that requires urgent hemostasis, especially in patients with coagulopathy caused by rapid polymerization with blood.^10,15

Stent-graft placement

Stent-graft placement for pseudoaneurysms can preserve the arterial flow and thereby decrease the risk of organ ischemia, such as hepatic failure.⁹ Previously, no stent-grafts for visceral arteries were commercially available; hence, covered biliary metallic stent as an alternative device was off-label used owing to the risk of organ ischemia.²² Recently, polytetrafluoroethylene covered stent-graft (GORE^® VIABAHN^®; Gore & Associates Inc., Flagstaff, AZ, USA) was commercially available for bleeding visceral arteries in Japan. Stent-graft placement is indicated for pseudoaneurysms common to the lobar hepatic artery, superior mesenteric artery, and splenic artery.^9,23 In the procedure using VIABAHN^®, a 6 to 7-Fr guiding sheath is inserted to the target artery as distal as possible, and the stent delivery system is advanced distal to the pseudoaneurysm along with a stiff 0.018-inch guidewire. Then, a stent-graft is deployed across the neck of the pseudoaneurysm, and balloon dilation is performed from the distal to the proximal portion of the stent-graft to prevent endoleak (Fig. 6).⁹ Stent-graft placement is not feasible because of potential technical difficulties, such as a tortuous vessel, celiac artery stenosis, or small-caliber target artery.⁸

Figure 6. SG placement for pseudoaneurysm after pancreaticoduodenectomy. (A, B) Enhanced CT and 3D image shows pseudoaneurysm at the RHA (anterior segment artery stump) (arrows). (C) Celiac artery angiography shows pseudoaneurysm at the tortuous RHA (anterior segment artery stump) (arrow). (D) The stent delivery system is advanced distal to the pseudoaneurysm along with a stiff 0.018-inch guidewire via a 6-Fr guiding sheath (arrowheads). (E) Stent-graft (VIABAHN^®, 6-mm diameter, 50-mm–long) is deployed across the neck of the pseudoaneurysm, and balloon dilation is performed from the distal to the proximal portion of stent-graft to prevent the endoleak (arrowheads). (F) Angiography shows the disappearance of the pseudoaneurysm (arrow). (G) 3D image of enhanced CT performed on the next day shows the patent SG and intrahepatic arteries (arrow). SG, stent graft; CT, computed tomography; RHA, right hepatic artery.

Technical success is defined as the elimination of active bleeding and pseudoaneurysm as detected by angiography after the initial intervention. Clinical success is generally defined as the absence of active rebleeding and no further management is necessary, such as repeated angiography or surgery, during the same admission.⁸ According to previous reports, the technical and clinical success rates of interventional management including TAE and stent-graft placement ranged from 78% to 100% and 60% to 100%, respectively.^4,7,8,24-30 Moreover, the technical and clinical success rates of stent-graft placement ranged from 83% to 100% and from 71% to 100%, respectively.^8,9,23,29

Despite the relatively high success rates, the packing technique is frequently associated with rebleeding with respect to the embolization techniques.^7,25 Hur et al⁷ investigated two techniques of TAE of pseudoaneurysms after pancreaticoduodenectomy (PD). No rebleeding occurred after TAE using isolation techniques (n = 13); on the contrary, all patients who underwent TAE using the packing technique (n = 3) experienced rebleeding after the initial hemostasis.

However, TAE using the isolation technique can cause post-embolization ischemia. Specifically, hepatic infarction caused by TAE for extrahepatic artery hemorrhage after PD may lead to fatal outcomes. The incidence of hepatic infarction of these TAE procedures ranged from 8.3% to 45.5%.^7,8,31 These incidences were possibly different because of hepatic artery variations. In patients with hepatic artery variations, intrahepatic collateral vessels via replaced hepatic arteries were exclusively evident on angiograms obtained immediately after TAE. Therefore, TAE of hepatic artery using the isolation technique was found to be safe in patients with replaced hepatic arteries.²⁷

Generally, the dual blood supply from the hepatic artery and PV and the extensive collateral pathways including the inferior phrenic arteries, intercostal arteries, and gastric arteries provide protection against hepatic infarction.⁸ In the case of poor hepatic collaterals in TAE after PD, PV flow was important for determining hepatic infarction because PV stenosis is a common complication of PD.³² In a recent study, transhepatic PV stent placement was performed immediately after hepatic artery embolization in patients with PV obstruction after PD, and it led to successful PV flow restoration and crucial rescue.²⁷

Stent-graft placement can overcome hepatic infarction after TAE. In a recent study of stent-graft placement for pseudoaneurysms of the hepatic artery, the technical success rate was 92% in pseudoaneurysm exclusion, with the maintenance of the hepatic arterial flow in 88% of the cases.⁹ High stent patency rates (81%) were observed at short-term (< 6 weeks) follow-up, but with decreased to 40% at mid- (> 6 weeks to 1 year) to long- (> 1 year) term follow-up. However, stent occlusion was mainly asymptomatic because of the development of collateral vessels that provided sufficient hepatic blood supply in most patients (86%) (Fig. 7). To prevent stent occlusion, anticoagulation and antiplatelet regimens after stent-graft placement are generally administered.^33,34 According to the guidelines of the European Societies of Cardiology and for Vascular Surgery, no recommendations were provided regarding single- or dual-antiplatelet therapy after endovascular treatments in visceral arteries.³⁵ Most centers empirically prescribe a combination of daily clopidogrel (75 mg) and aspirin (low dose) from 1 month to 1 year.³⁵ However, considering the rebleeding risk, these antithrombotic treatments may be contraindicated in the perioperative period. Other major complications of stent-graft placement, such as arterial dissection and stent-graft infection, were reported.^8,23

Figure 7. Enhanced computed tomography shows the stent occlusion 14 days after stent graft placement (arrow). However, it is asymptomatic because of collateral vessel development. In this case, considering the risk of rebleeding, antithrombotic treatments are not administered (the same case in Fig. 3).

With the recent advancements in endovascular devices, interventional management including TAE and stent-graft placement has been considered a first-line treatment for arterial bleeding after gastrointestinal surgery. Stent-graft placement, which can preserve the hepatic arterial flow, is better than TAE in patients with extrahepatic artery hemorrhage. However, in patients with anatomical changes such as a tortuous vessel, celiac artery stenosis, or small-caliber target artery, stent-graft placement is technically difficult; therefore, TAE should be initially performed. Moreover, TAE can be performed in patients with replaced hepatic arteries because of the low risk of hepatic infarction.

We thank the members of Department of Diagnostic and Interventional Radiology, Aichi Cancer Center Hospital.

None.

No potential conflict of interest relevant to this article was reported.