Int J Gastrointest Interv 2019; 8(2): 63-69  https://doi.org/10.18528/ijgii170028
Embolization of procedure-related upper gastrointestinal bleeding
Yasir Nouri, Ji Hoon Shin* , Heung-Kyu Ko, Jong Woo Kim, Hyun-Ki Yoon
Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea
*Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Korea.
E-mail address:jhshin@amc.seoul.kr (J.H. Shin). ORCID: https://orcid.org/0000-0001-6598-9049
Received: November 20, 2017; Revised: January 15, 2018; Accepted: January 15, 2018; Published online: April 30, 2019.
© Society of Gastrointestinal Intervention. All rights reserved.

cc This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Non-surgical procedure-related, upper gastrointestinal bleeding (UGIB) is considered as one of the rarest of all UGIB causes, although it is a serious complication when it occurs. It presented as hematemesis, melena or hemobilia in which is associated with hepatobiliary intervention. In most patients the bleeding resolves spontaneously and in those in which it does not, the majority respond to conservative management. Endoscopy is the first line of treatment if bleeding does not stop after medical management, although if it failed due to massive bleeding, in hemodynamically unstable patients or in hepatobiliary procedure-related bleeding, endovascular or surgical intervention should be considered. In this manuscript we will discuss the endovascular diagnosis and treatment of non-surgical procedure-related UGIB.

Keywords: Embolization, therapeutic, Hemorrhage, Upper gastrointestinal tract
Introduction

Upper gastrointestinal bleeding (UGIB) is defined as bleeding originating from the distal esophagus to the duodenum at the level of the ligament of Treitz. Since the first use of angiography in the diagnosis and management of UGIB, it has been considered as the first treatment of choice in acute bleeding which is refractory to endoscopic management. Although non-variceal UGIB results in the hospitalization of 30 to 100 patients per a 100,000 population per year, non-surgical procedure-related bleeding is considered one of the rare causes of UGIB and which represents less than 5% of all causes.1,2 There are many published literature reports regarding the angiographic diagnosis and intervention in UGIB due to various causes.3,4 However, information regarding the role of this technique in the management of non-surgical procedure-related UGIB has rarely been published.

Upper gastrointestinal (GI) procedures are done either endoscopically or percutaneously. Procedure-related UGIB could present as hematemesis, melena or hemobilia associated with hepatobiliary intervention. In most cases the bleeding resolves spontaneously and of those that do not, the majority respond to medical management with fluid resuscitation, correction of the coagulopathy, and administration of blood products.5 Endoscopy may be applied to visualize the bleeding and for targeted treatment if bleeding does not respond to medical treatment.6 In failed endoscopic treatment due to massive bleeding or in the case of hemodynamically unstable patients or hepatobiliary procedure-related bleeding, endovascular or surgical intervention should be considered.7 Moreover, endovascular embolization represents the most viable treatment option in patients receiving anticoagulation therapy for various diseases.8 In this article we will discuss the endovascular management of non-surgical procedure-related UGIB.

Clinical Presentation and General Management

Procedure-related UGIB could present as immediate or delayed bleeding. Immediate bleeding is defined as bleeding that occurs at the time of a procedure, while delayed bleeding is that occurs 0 to 30 days after a procedure. Most intra-procedural bleeding resolves without further intervention. On the other hand, delayed bleeding is usually clinically significant.

Direct clinical evidence of active bleeding may present as persistent melena, hematochezia, hematemesis or hemobilia. The vital signs must be closely monitored for signs of active bleeding that could manifest as tachycardia, hypotension, and potential hypoxemia. Hemodynamic instability despite vigorous resuscitation is the best indicator of active bleeding.

Blood loss of 100 mL per day may be asymptomatic, blood loss of 500 mL usually results in systemic abnormalities; i.e., tachycardia and hypotension, and blood loss of 15% of the circulating blood volume results in systemic shock.9 Overall, approximately 75% of patients present with asymptomatic or mild systemic symptoms can be treated conservatively, whereas 25% of patients need immediate medical attention and resuscitation.10

Medical management is the first-line treatment of UGIB. Stabilization of blood pressure and fluid resuscitation are the immediate goals. Blood transfusion should be considered for correction of coagulopathy and which considered an important component of medical management.

Endoscopy is the primary technique for the diagnosis and treatment of UGIB. However, it often fails to depict the exact bleeding focus when massive bleeding (1 mL/min) occurs.5 Vreeburg et al11 reported that no diagnosis could be made at the first endoscopy in 24% of patients with acute UGIB. In their study, excessive blood or clots in the gastroduodenal tract impaired the endoscopic view in 15% of the patients. Endoscopic hemostasis can be achieved via thermocoagulation, sclerosant injection or clips/banding. Endoscopic clip placement, even if ineffectual, can assist subsequent endovascular intervention by directing the interventional radiologist to the area of concern.12,13 However, there are no endoscopic interventions possible if the hepatobiliary source of hemorrhage is identified. The primary therapeutic option in such cases is endovascular or surgical treatment.

Imaging Modality

If a patient is hemodynamically stable and the exact site of bleeding is obscure, the bleeding site could be evaluated with a radionuclide technetium 99m-tagged red blood cell scan, as the nuclear scintigraphy study can demonstrate active bleeding at rates as low as 0.1 mL/min.14,15 A positive scintigram increases the likelihood of a positive angiogram from 22% to 53%.16 Although the high sensitivity of nuclear scintigraphy study, it is associated with limitations: it cannot precisely locate the bleeding site or even identify its cause in a positive scan because of the poor spatial resolution, or the tendency of tagged blood moving in GI lumen with peristalsis or position changes.17

A computed tomography angiography (CTA) scan may be useful if a bleeding site cannot be identified endoscopically. CTA has the advantage of greater availability, speed, and noninvasiveness. It also does not suffer from a bowel or respiratory motion artifact. In an animal model, CTA was shown to detect bleeding rates as low as 0.3 mL/min more successfully than conventional angiography.18 In addition to being able to localize a bleeding site, CTA also has the benefit of providing information regarding the vascular anatomy for pre-interventional planning, as well as identifying extraluminal abnormalities.19

Indications and Contraindications of Angiography

Angiography is indicated if there is massive bleeding which could not be treated by endoscopy or if a patient is hemodynamically unstable (systolic blood pressure < 100 mmHg and heart rate > 100 beats per minute or clinical shock). Furthermore, it is indicated in patients with hepatobiliary procedure-related bleeding in which endoscopy has no role in the intervention.

In general, it has no absolute contraindications because angiography and embolization are needed as lifesaving procedures. For patients with severe reactions to iodinated contrast media, alternative contrast agents, such as carbon dioxide, can be used. Relative contraindications include renal insufficiency, contrast allergy, and uncorrectable coagulopathy. There is an increased risk of gastric or duodenal infarction after embolization in patients with previous, extensive UGI surgery or radiotherapy.

Technique of Endovascular Management

Diagnostic angiography

Because UGIB is normally intermittent, the successful angiographic demonstration of the source of bleeding depends on the presence of active bleeding at the time of the examination. In literature reports, bleeding rates of 0.5 to 1.0 mL/min have been considered necessary if contrast extravasation is to be angiographically visible.20 Moreover, digital subtraction angiography (DSA) is five to nine times more sensitive than screen-film arteriography for detecting bleeding, and which seems to be equivalent to the detection rates of scintigraphic images.21,22

Although in most procedure-related UGIB it is possible to identify the source of hemorrhage, in some patients it is difficult to localize it because of the intermittent nature of GI bleeding, which can result if the bleeding has temporarily stopped at the time of the contrast injection. In such circumstances, to enhance the detection rate of bleeding, glucagon and Buscopan may be given before the procedure in order to limit peristalsis and respiratory motion artifacts on DSA.23 Furthermore, longer injection durations of the contrast or the use of carbon dioxide as a contrast medium can also improve the sensitivity for detecting small bleedings.24 Oblique views can provide a clearer view of colic vessels in flexures. In addition, right and left anterior oblique views open up hepatic and splenic flexures, respectively. Endoscopic clips, which are placed around the area of bleeding during pre-embolization endoscopy, can help to accurately localize the bleeding vessels. In such cases, even if no extravasation is seen, the branches terminating at the clip are superselected using microcatheter techniques and are embolized. Administration of vasodilators, anticoagulants, and/or thrombolytics can stimulate bleeding and thus help in detecting the origin of bleeding.25

The vessel selected first should be based on the suspicion of the likely source of bleeding according to the patient’s history, clinical signs, as well as localization provided by previous imaging or endoscopy. Generally, in UGIB, the celiac and superior mesenteric arteries (SMAs) are the primary targets. If there is no sign of active bleeding on contrast injection of the main trunks, more selective injection may be needed. For duodenal or gastric fundus bleeding, the gastroduodenal artery (GDA) or left gastric arteries, respectively, should be studied. And if there is hemobilia, hepatic arteries are the most suspected source of bleeding. Obtaining images should be continued until the venous phase has cleared out in order to help distinguish contrast extravasation from persistent venous opacification.

Angiographic findings

The primary angiographic findings of bleeding are visualization of active contrast extravasation and contrast pooling in the venous phase. A review of studies by Loffroy et al26 found that angiographic evidence of active extravasation was seen in 54% of patients. Other indirect signs of bleeding on angiography include a pseudoaneurysm, vessel spasm or cut-off, and early venous filling.

Empirical or blind embolization of the vessels supplying the area of concern can be performed if no arterial abnormality is seen.27,28 A review of the published series by Loffroy et al26 demonstrated that blind embolization is performed in 46% of endovascular cases. This technique is feasible due to the rich collateral circulation of the upper GI tract. The left gastric artery supplies the distal esophagus, cardia, and fundus, and there is collateralization with branches of the short gastric and right gastric arteries. The GDA supplies the remainder of the stomach and the duodenum. The SMA also provides a duodenal supply via the pancreaticoduodenal arcades. And there are collateral arterial branches to hepatic arteries from the inferior phrenic, intercostal, left gastric arteries, and omental branches from the GDA. Moreover, in the hepatobiliary bleeding origin, transarterial embolization is considered the first-line treatment due to the dual vascular supply of the liver (75% via the portal vein and 25% via the hepatic artery) which permits embolization of hepatic artery branches without significant concern for infarction.29

No statistical difference in outcomes was shown between patients treated with empirical embolization versus embolization after angiographically demonstrated contrast extravasation.27,30 An alternative to blind embolization in cases of negative angiography is to target branches supplying the area of endoscopically placed clips.

Types of embolic agent

The choice of embolic agent depends on a combination of the vascular anatomy, angiographic findings, the achievable catheter position, and the operator’s preference. Vessel diameter and the nature of permanent or temporary embolization should be also considered. The most common embolic agents are metallic coils and gelatin sponge particles (GSPs).1 However, using coils as the only embolic agent is significantly associated with early rebleeding compared with adding polyvinyl alcohol or GSP to coils.27,31 The use of N-butyl cyanoacrylate (NBCA) has recently gained acceptance. As it is a liquid embolic material with a non-radiopaque nature, it should, therefore, be mixed with Lipiodol to provide radiopacity and to control the viscosity. The more diluted the NBCA concentration is, the deeper penetration to the distal is achieved. Usually NBCA: lipiodol ranges from 1:1 to 1:4. It is advantageous for massive bleeding that requires urgent hemostasis, especially in patients with coagulopathy caused by rapid polymerization with blood.32

Types of embolization

Types of embolization depend on the microcatheter superselection accessibility to the bleeding point. There can be localized, proximal or segmental embolizations. In localized embolization, the microcatheter is superselected at the bleeding point. On the other hand when the bleeding point cannot be superselected, either proximal embolization is done in which the embolization is in its parent artery or segmental embolization in which an adjacent branch artery or arteries are included to be embolized. In cases of proximal embolization, recanalization of the bleeding point can occur due to distal back flow, while in segmental embolization, ischemic complications of the involved bowel can occur.

Upper GI Procedures

Upper GI procedures are done either endoscopically or percutaneously. An upper GI endoscopic diagnostic procedure complicated by bleeding is rare and does not have a clinical significance.33 On the other hand, endoscopy for therapeutic purposes carries a risk of bleeding which needs further angiographic management in failed endoscopic treatment.34 Endoscopic mucosal resection (EMR), endoscopic submucosal dissection (ESD), as well as endoscopic ultrasound (EUS)-guided procedures are associated with the risk of bleeding that may necessitate endovascular management, as reported in published literature reports.35 Furthermore, percutaneous endoscopic or radiologic gastrostomy (PEG, PRG) related bleeding is rare, but may be catastrophic when it occurs.36,37

EMR and ESD

EMR and ESD are effective and minimally invasive procedures for management of upper GI epithelial and subepithelial lesions. They are useful techniques for treating early gastric cancer without lymph node metastasis or with a lower risk of local recurrence, as well as other polyps or submucosal tumors.38,39 These endoscopic techniques enable physicians to confirm the histopathologic diagnosis based on the resected specimens. Although these procedures are effective and safe, they could be accompanied by delayed, life-threatening bleeding which may be the most serious complication.40 However, significant bleeding only occurs in approximately 2.8% of esophageal resections and less frequently than in the stomach.41 A recent meta-analysis found no differences in the bleeding rates with EMR and ESD.

Endovascular embolization is considered the first-choice treatment compared with surgery for uncontrolled medical and endoscopic management (Fig. 1). There is no preferable embolic agent which can be used for the management of bleeding and its choice depends on the operator. However, Lee et al42 used microcoils only and Komatsu et al43 used microcoils with GSP for successful embolization of uncontrolled bleeding during ESD of the stomach. Moreover, Lang et al44 proposed prophylactic embolization of the left gastric artery when there is definite prior identification of a lesion in the left gastric artery area or if a patient has a controlled, previous, massive bleeding due to a gastric lesion and the patient is at risk for multi-organ failure if bleeding recurs. Previous reports by Park et al45 support the validity of prophylactic transcatheter arterial embolization in UGIB without extravasation seen on an angiogram in patients with gastric intramural hematoma caused by EMR.

Endoscopic ultrasound-guided Intervention

EUS has been a diagnostic procedure concentrating on structural identification and staging of GI cancers. However, with advancement in this technology, EUS has expanded from diagnostic sampling into the field of therapeutic procedures.46 Numerous procedures have been increasing associated with an increased risk of complications. The incidence of complication rates varies in each diagnostic and therapeutic technique.47 Recently, a systematic review found the overall complication rate and mortality were 0.98% and 0.02%, respectively. The most significant complications were acute pancreatitis (34%), infection (16%), bleeding (13%), and perforation or bile/pancreatic leaks (3%).46 Moreover, reports describing the role of arterial embolization in the management of interventional, EUS-related bleeding are limited (Fig. 2, 3). Brandon et al48 reported embolization of massive arterial hemorrhage following endoscopic, ultrasonography (US)-guided cystogastrostomy for pancreatic pseudocyst drainage. Right and left gastric arteries were successfully embolized by coils. No rebleeding was detected.

Percutaneous gastrostomy

Percutaneous gastrostomy is a well-established procedure for long-term nutritional support or gastric decompression in patients incapable of oral intake due to various disorders. The incidence of major complications after PRG or PEG has been found to range from 0% to 6%.4951 UGIB complicating enterostomy is rare but it is a serious complication if it occurs.52,53 Pseudoaneurysm formation also can occur.54 UGIB complication is usually due to direct puncture of blood vessels, traumatic erosion, ulceration, and pressure necrosis of the gastric mucosa which may occur due to excessive tension of the inner bumper.

Although endoscopy is superior in localizing the bleeding site, characterizing the cause of bleeding, and showing the relationship between the bleeding site and the gastrostomy tube,37 it may be limited by several factors including the presence of comorbid illnesses, active bleeding, bleeding vessels larger than 2 mm, and endoscopic blind spots, all of which may increase endoscopic hemostatic failure for UGIB.55

There have been a few reports regarding endovascular embolization management for bleeding complications after PEG/PRG (Fig. 4).53,54,56 Lewis et al56 reported occlusion of both gastroepiploic arteries by selective embolization which successfully stopped bleeding in a patient with an unstable hemodynamic status after PEG/PRG. Seo et al54 retrospectively evaluated the incidence and management of bleeding complications in 574 patients who underwent PRG. Only eight patients (1.4%) had symptoms or signs of UGIB after PRG. Five patients underwent angiography because bleeding could not be controlled by conservative management as in the other three patients. In one patient, wedge resection, including the tube insertion site, was performed for hemostasis because no bleeding focus was discovered. In three patients, successful hemostasis was achieved by TAE, whereas in the remaining patient failure of embolization was reported because of the difficulty with the microcatheter advancing to the distal part of the bleeding focus, and therefore having persistent bleeding which was managed by surgery. This result supports the concept that if both the proximal and distal parts of the bleeding focus cannot be securely embolized, there is the potential for rebleeding by collaterals.

Hepatobiliary Procedure

Hemobilia is bleeding from the hepatobiliary tract and is considered as one of rare causes of UGIB.2,57 It occurs when the arterial bleeding is so rapid that blood is easily dissolved in bile and passes directly into the duodenum, appearing as hematemesis or melena. However, when the hemorrhage occurs more slowly, the blood and bile do not mix easily and clots obstruct the bile ducts and produce colicky pain and jaundice. It is often caused by trauma to the liver and biliary tract, including percutaneous transhepatic cholangiography (PTC) and percutaneous transhepatic biliary drainage (PTBD), biliary drainage during endoscopic retrograde cholangiopancreatography (ERCP), cholecystectomy, TIPS procedure, liver biopsy, and radiofrequency ablation (RFA).58 The incidence of hemobilia following RFA and liver biopsy is estimated to be 0%–0.5% and 0.06%–1%, respectively; PTC (up to 4%) and PTBD (2%–10%) have a higher risk because of the use of larger needles and the presence of bile stasis.5860 The mechanism of hemobilia after a liver/biliary tract intervention is not completely understood. An arteriobiliary fistula can occur immediately or may be the result of an erosion and breakthrough of a pseudoaneurysm to a nearby bile duct after days or weeks.58 The most frequent cause is a direct trauma associated with the procedure.61,62

Hemobilia from a venous source is rare. It is thought to originate from a source in the liver parenchyma in 50% of patients and from the bile ducts/gallbladder in 45% of them. A pancreatic source has been identified in fewer than 5% of patients.63 The gold standard for diagnosing hemobilia is selective arteriography. In up to 90% of these patients, a vascular abnormality is found. The most common finding is a pseudoaneurysm, followed by an arteriobiliary or an arterioportal fistula.64 Arterial embolization remains the treatment of choice. Success rates of 80%–100% have been reported in the published literature.6567 Complications are rare and include hepatic necrosis, abscess formation, gall-bladder infarction, non-target embolization, and intimal dissection with arterial thrombosis.68 Other endovascular treatment for hemobilia due to pseudoaneurysm include covered stent deployment which has the advantage of maintaining the arterial blood flow, maintaining perfusion of the liver, and minimizing the risk of ischemia seen with embolization. However, using stents is associated with several limitations including the possible challenging navigation of the stent delivery system through the vascular loops, particularly through celiac axis, or SMA, tortuous, and small hepatic artery, and excessive manipulation of the device which may lead to vasospasm, dissection at the ends of the stent, and even vessel rupture.69

PTBD

PTBD is an effective method for primary or palliative treatment of biliary abnormalities. Hemobilia due to hepatic arterial injury is a serious but infrequent complication, occurring in 1.3%–8% of PTBDs.66,70 The most common causes of bleeding are arteriobiliary fistula and pseudoaneurysm.29 Left-sided PTBD seems associated with a greater risk of hepatic artery injury due to the anatomic arrangement of the hepatic arteries and bile ducts.

The reported initial technical and clinical success rates of arterial embolization are 100% and 95.8%, respectively.29,70,71 Coil as well as NBCA embolization is highly effective in order to control bleeding (Fig. 5). The complication rate following embolization of the hepatic artery is low due to its dual vascular supply through the portal vein and hepatic artery as well as the intrahepatic collateral pathways.

ERCP

ERCP is an efficient and safe invasive procedure that is performed to diagnose and treat pancreatic and biliary disease. However, in a prospective multicenter study, 9.8% of the patients had post-ERCP complications. Pancreatitis (5.4%) and hemorrhage (2%) are considered the most common complications associated with ERCP.72 Moreover, the incidence of complications related to therapeutic ERCP procedures was more common than that in diagnostic procedures.73 Bleeding associated with endoscopic sphincterotomy is one of the most frequent complications of ERCP and has been reported in 1%–10% of patients.7274 So et al75 reported 10 patients who underwent selective embolization for post-endoscopic sphincterotomy bleeding and found that most of the bleeding branches arose from the posterior pancreaticoduodenal artery. In their study, they could determine the optimal approach to the bleeding branches by celiac and SMA arteriography, and two bleeding branches were found in two patients. Therefore, multiple branches should be considered because there is no anatomic landmark of the avascular zone on duodenal papilla. Coil, NBCA or GSP were proven to be effective for embolization at the bleeding focus (Fig. 6).

Conclusion

Procedure-related bleeding is considered one of rare causes of UGIB. It could present as hematemesis, melena or hemobilia, all of which are associated with hepatobiliary intervention. In most patients the bleeding resolves spontaneously and in those that do not, the majority respond to medical or endoscopic management. In failed endoscopic treatment due to massive bleeding or in the case of hemodynamically unstable patients or in hepatobiliary procedure-related bleeding, endovascular or surgical intervention should be considered. Endovascular embolization represents the most viable treatment option as it is less invasive and not associated with the complications of general anesthesia.

Acknowledgments

All authors have contributed to the paper and have not submitted the manuscript, in whole or in part, to other journals.

Conflicts of Interest

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

Figures
Fig. 1. Active bleeding after endoscopic submucosal dissection (ESD) for gastric subepithelial tumor. (A) Profuse bleeding was noted on endoscopy. Endoscopic bleeding control was unsuccessful. (B) Left gastric angiogram two hours after ESD shows extravasation of contrast (arrow). (C) After embolization using gelatin sponge particles and coils, spot radiograph shows coils and extravasated contrast into the stomach. (D) Post-embolization, gastroduodenal artery angiogram shows no further bleeding focus.
Fig. 2. Active bleeding after endoscopic ultrasound-guided, fine needle aspiration biopsy of a pancreatic lesion. (A) Common hepatic artery angiography shows a pseudoaneurysm from the gastroduodenal artery (arrow). (B) Superior mesenteric artery (SMA) angiogram shows no other bleeding focus. (C, D) Post-embolization SMA angiograms show no further bleeding focus. The distal portion of the pseudoaneurysm was embolized using microcoils (arrows) and both the pseudoaneurysm and the proximal portion were embolized with N-butyl cyanoacrylate (NBCA; NBCA:lipiodol = 1:3) (arrowheads).
Fig. 3. Active bleeding after endoscopic ultrasound-guided hepatoduodenostomy. (A) On endoscopy, bleeding control was impossible. (B) Common hepatic artery angiogram shows a pseudoaneurysm (arrow) at the right main hepatic artery near the proximal stent end. (C) The post-embolization angiogram shows no further bleeding focus with preserved right hepatic flow via intrahepatic collaterals. The proximal portion of the pseudoaneurysm was embolized using microcoils, followed by embolization of the pseudoaneurysm and its proximal part with N-butyl cyanoacrylate (NBCA; NBCA:lipiodol = 1:3).
Fig. 4. Bleeding complication after percutaneous endoscopic gastrostomy. (A) Enhanced abdomen computed tomography scan shows a large amount of hemoperitoneum with pneumoperitoneum. (B, C) Left gastric artery angiograms show contrast extravasation (arrows) from the left gastric artery. (D) The left gastric artery angiogram after embolization with gelatin sponge particles and a microcoil shows disappearance of contrast extravasation.
Fig. 5. Bleeding complication after right percutaneous transhepatic biliary drainage. (A) Enhanced abdomen computed tomography (coronal reconstruction) shows a large hepatic hematoma with active bleeding (arrow). (B) Selective right hepatic artery angiogram shows a pseudoaneurysm (arrow) with extravasation (arrowhead) from the A6 artery. (C, D) After embolization using N-butyl cyanoacrylate (NBCA; NBCA:lipiodol = 1:3), the spot radiograph (C) shows NBCA cast filling the A6 branch and the pseudoaneurysm. Common hepatic artery angiogram (D) shows no further bleeding focus.
Fig. 6. Active bleeding after endoscopic sphincterotomy for stone removal. (A) An endoscopic image eight hours after EST shows active bleeding from the ampulla. A covered stent was inserted to tamponade the bleeding, however, bleeding persisted. (B) The superior mesenteric artery (SMA) angiogram 10 hours after EST shows contrast extravasation (arrows) from the pancreaticoduodenal arcade. (C, D) Post-embolization SMA angiograms show no definite residual bleeding after embolization with N-butyl cyanoacrylate (NBCA; NBCA:lipiodol = 1:3).
References
  1. Mirsadraee S, Tirukonda P, Nicholson A, Everett SM, McPherson SJ. Embolization for non-variceal upper gastrointestinal tract haemorrhage: a systematic review. Clin Radiol. 2011;66:500-9.
    Pubmed CrossRef
  2. Lee EW, Laberge JM. Differential diagnosis of gastrointestinal bleeding. Tech Vasc Interv Radiol. 2004;7:112-22.
    Pubmed CrossRef
  3. Rösch J, Dotter CT, Brown MJ. Selective arterial embolization. A new method for control of acute gastrointestinal bleeding. Radiology. 1972;102:303-6.
    Pubmed CrossRef
  4. Shin JH. Recent update of embolization of upper gastrointestinal tract bleeding. Korean J Radiol. 2012;13 Suppl 1:S31-9.
    Pubmed KoreaMed CrossRef
  5. Welch CE, Hedberg S. Gastrointestinal hemorrhage. I. General considerations of diagnosis and the rapy. Adv Surg. 1973;7:95-148.
    Pubmed
  6. Barkun A, Fallone CA, Chiba N, Fishman M, Flook N, Martin J, et al. A Canadian clinical practice algorithm for the management of patients with nonvariceal upper gastrointestinal bleeding. Can J Gastroenterol. 2004;18:605-9.
    Pubmed CrossRef
  7. Defreyne L, Vanlangenhove P, De Vos M, Pattyn P, Van Maele G, Decruyenaere J, et al. Embolization as a first approach with endoscopically unmanageable acute nonvariceal gastrointestinal hemorrhage. Radiology. 2001;218:739-48.
    Pubmed CrossRef
  8. Rose PE. Audit of anticoagulant therapy. J Clin Pathol. 1996;49:5-9.
    Pubmed KoreaMed CrossRef
  9. Richter JMIK. Gastrointestinal bleeding. In: Harrison TR, Wilson JD, editors. Harrison’s principles of internal medicine. 12th ed. New York: McGraw-Hill 1991:234-44.
  10. Fallah MA, Prakash C, Edmundowicz S. Acute gastrointestinal bleeding. Med Clin North Am. 2000;84:1183-208.
    Pubmed CrossRef
  11. Vreeburg EM, Snel P, de Bruijne JW, Bartelsman JF, Rauws EA, Tytgat GN. Acute upper gastrointestinal bleeding in the Amsterdam area: incidence, diagnosis, and clinical outcome. Am J Gastroenterol. 1997;92:236-43.
    Pubmed
  12. Eriksson LG, Sundbom M, Gustavsson S, Nyman R. Endoscopic marking with a metallic clip facilitates transcatheter arterial embolization in upper peptic ulcer bleeding. J Vasc Interv Radiol. 2006;17:959-64.
    Pubmed CrossRef
  13. Song JS, Kwak HS, Chung GH. Nonvariceal upper gastrointestinal bleeding: the usefulness of rotational angiography after endoscopic marking with a metallic clip. Korean J Radiol. 2011;12:473-80.
    Pubmed KoreaMed CrossRef
  14. Winzelberg GG, McKusick KA, Froelich JW, Callahan RJ, Strauss HW. Detection of gastrointestinal bleeding with 99mTc-labeled red blood cells. Semin Nucl Med. 1982;12:139-46.
    Pubmed CrossRef
  15. Bentley DE, Richardson JD. The role of tagged red blood cell imaging in the localization of gastrointestinal bleeding. Arch Surg. 1991;126:821-4.
    Pubmed CrossRef
  16. Gunderman R, Leef J, Ong K, Reba R, Metz C. Scintigraphic screening prior to visceral arteriography in acute lower gastrointestinal bleeding. J Nucl Med. 1998;39:1081-3.
    Pubmed
  17. Tabibian JH, Wong Kee Song LM, Enders FB, Aguet JC, Tabibian N. Technetium-labeled erythrocyte scintigraphy in acute gastrointestinal bleeding. Int J Colorectal Dis. 2013;28:1099-105.
    Pubmed CrossRef
  18. Kuhle WG, Sheiman RG. Detection of active colonic hemorrhage with use of helical CT: findings in a swine model. Radiology. 2003;228:743-52.
    Pubmed CrossRef
  19. Geffroy Y, Rodallec MH, Boulay-Coletta I, Jullès MC, Ridereau-Zins C, Zins M. Multidetector CT angiography in acute gastrointestinal bleeding: why, when, and how. Radiographics. 2011;31:E35-46.
    Pubmed CrossRef
  20. Nusbaum M, Baum S. Radiographic demonstration of unknown sites of gastrointestinal bleeding. Surg Forum. 1963;14:374-5.
    Pubmed
  21. Hastings GS. Angiographic localization and transcatheter treatment of gastrointestinal bleeding. Radiographics. 2000;20:1160-8.
    Pubmed CrossRef
  22. Krüger K, Heindel W, Dölken W, Landwehr P, Lackner K. Angiographic detection of gastrointestinal bleeding. An experimental comparison of conventional screen-film angiography and digital subtraction angiography. Invest Radiol. 1996;31:451-7.
    Pubmed CrossRef
  23. Burke SJ, Golzarian J, Weldon D, Sun S. Nonvariceal upper gastrointestinal bleeding. Eur Radiol. 2007;17:1714-26.
    Pubmed CrossRef
  24. Sandhu C, Buckenham TM, Belli AM. Using CO2-enhanced arteriography to investigate acute gastrointestinal hemorrhage. AJR Am J Roentgenol. 1999;173:1399-401.
    Pubmed CrossRef
  25. Ryan JM, Key SM, Dumbleton SA, Smith TP. Nonlocalized lower gastrointestinal bleeding: provocative bleeding studies with intraarterial tPA, heparin, and tolazo-line. J Vasc Interv Radiol. 2001;12:1273-7.
    Pubmed CrossRef
  26. Loffroy R, Rao P, Ota S, De Lin M, Kwak BK, Geschwind JF. Embolization of acute nonvariceal upper gastrointestinal hemorrhage resistant to endoscopic treatment: results and predictors of recurrent bleeding. Cardiovasc Intervent Radiol. 2010;33:1088-100.
    Pubmed CrossRef
  27. Aina R, Oliva VL, Therasse E, Perreault P, Bui BT, Dufresne MP, et al. Arterial embolotherapy for upper gastrointestinal hemorrhage: outcome assessment. J Vasc Interv Radiol. 2001;12:195-200.
    Pubmed CrossRef
  28. Morris DC, Nichols DM, Connell DG, Burhenne HJ. Embolization of the left gastric artery in the absence of angiographic extravasation. Cardiovasc Intervent Radiol. 1986;9:195-8.
    Pubmed CrossRef
  29. Choi SH, Gwon DI, Ko GY, Sung KB, Yoon HK, Shin JH, et al. Hepatic arterial injuries in 3110 patients following percutaneous transhepatic biliary drainage. Radiology. 2011;261:969-75.
    Pubmed CrossRef
  30. Padia SA, Geisinger MA, Newman JS, Pierce G, Obuchowski NA, Sands MJ. Effectiveness of coil embolization in angiographically detectable versus non-detectable sources of upper gastrointestinal hemorrhage. J Vasc Interv Radiol. 2009;20:461-6.
    Pubmed CrossRef
  31. Loffroy R, Guiu B, D’Athis P, Mezzetta L, Gagnaire A, Jouve JL, et al. Arterial embolotherapy for endoscopically unmanageable acute gastroduodenal hemorrhage: predictors of early rebleeding. Clin Gastroenterol Hepatol. 2009;7:515-23.
    Pubmed CrossRef
  32. Toyoda H, Nakano S, Kumada T, Takeda I, Sugiyama K, Osada T, et al. Estimation of usefulness of N-butyl-2-cyanoacrylate-lipiodol mixture in transcatheter arterial embolization for urgent control of life-threatening massive bleeding from gastric or duodenal ulcer. J Gastroenterol Hepatol. 1996;11:252-8.
    Pubmed CrossRef
  33. Blero D, Devière J. Endoscopic complications--avoidance and management. Nat Rev Gastroenterol Hepatol. 2012;9:162-72.
    Pubmed CrossRef
  34. Song LMWK, Baron TH. Endoscopic management of procedure-related bleeding. Gastrointest Interv. 2012;1:43-52.
    CrossRef
  35. Rolanda C, Caetano AC, Dinis-Ribeiro M. Emergencies after endoscopic procedures. Best Pract Res Clin Gastroenterol. 2013;27:783-98.
    Pubmed CrossRef
  36. Hicks ME, Surratt RS, Picus D, Marx MV, Lang EV. Fluoroscopically guided percutaneous gastrostomy and gastroenterostomy: analysis of 158 consecutive cases. AJR Am J Roentgenol. 1990;154:725-8.
    Pubmed CrossRef
  37. Nishiwaki S, Araki H, Takada J, Watanabe N, Asano T, Iwashita M, et al. Clinical investigation of upper gastrointestinal hemorrhage after percutaneous endoscopic gastrostomy. Dig Endosc. 2010;22:180-5.
    Pubmed CrossRef
  38. Min YW, Min BH, Lee JH, Kim JJ. Endoscopic treatment for early gastric cancer. World J Gastroenterol. 2014;20:4566-73.
    Pubmed KoreaMed CrossRef
  39. Facciorusso A, Antonino M, Di Maso M, Muscatiello N. Endoscopic submucosal dissection vs endoscopic mucosal resection for early gastric cancer: a meta-analysis. World J Gastrointest Endosc. 2014;6:555-63.
    Pubmed KoreaMed CrossRef
  40. Libânio D, Pimentel-Nunes P, Dinis-Ribeiro M. Complications of endoscopic resection techniques for upper GI tract lesions. Best Pract Res Clin Gastroenterol. 2016;30:735-48.
    Pubmed CrossRef
  41. Dinis-Ribeiro M, Pimentel-Nunes P. Should antiplatelets be stopped before gastric mucosectomy? For how long and in whom?. Endoscopy. 2012;44:111-3.
    Pubmed CrossRef
  42. Lee CK, Park JY, Lee TH, Lee SH, Chung IK, Park SH, et al. Superselective microcoil embolization for endoscopically uncontrollable bleeding after endoscopic submucosal dissection. Endoscopy. 2009;41 Suppl 2:E109-10.
    Pubmed CrossRef
  43. Komatsu O, Matsushita T, Kishimoto K, Adachi W. Transcatheter arterial embolization for uncontrolled bleeding during endoscopic submucosal dissection of the stomach. Clin J Gastroenterol. 2014;7:219-22.
    Pubmed CrossRef
  44. Lang EV, Picus D, Marx MV, Hicks ME, Friedland GW. Massive upper gastrointestinal hemorrhage with normal findings on arteriography: value of prophylactic embolization of the left gastric artery. AJR Am J Roentgenol. 1992;158:547-9.
    Pubmed CrossRef
  45. Park JJ, Jung SW, Ju SB, Kim HM, Kim JB, Park SH, et al. A case of a large, gastric intramural hematoma caused by endoscopic mucosal resection, and treated with transcatheter arterial embolization. Korean J Med. 2015;89:317-22.
    CrossRef
  46. Anandasabapathy S. Endoscopic ultrasound: indications and applications. Mt Sinai J Med. 2006;73:702-7.
    Pubmed
  47. Adler DG, Jacobson BC, Davila RE, Hirota WK, Leighton JA, Qureshi WA, et al. ASGE guideline: complications of EUS. Gastrointest Endosc. 2005;61:8-12.
    Pubmed CrossRef
  48. Brandon JL, Ruden NM, Turba UC, Bozlar U, Yeaton P, Hagspiel KD. Angiographic embolization of arterial hemorrhage following endoscopic US-guided cystogastrostomy for pancreatic pseudocyst drainage. Diagn Interv Radiol. 2008;14:57-60.
    Pubmed
  49. Silas AM, Pearce LF, Lestina LS, Grove MR, Tosteson A, Manganiello WD, et al. Percutaneous radiologic gastrostomy versus percutaneous endoscopic gastrostomy: a comparison of indications, complications and outcomes in 370 patients. Eur J Radiol. 2005;56:84-90.
    Pubmed CrossRef
  50. Möller P, Lindberg CG, Zilling T. Gastrostomy by various techniques: evaluation of indications, outcome, and complications. Scand J Gastroenterol. 1999;34:1050-4.
    Pubmed CrossRef
  51. Wollman B, D’Agostino HB, Walus-Wigle JR, Easter DW, Beale A. Radiologic, endoscopic, and surgical gastrostomy: an institutional evaluation and meta-analysis of the literature. Radiology. 1995;197:699-704.
    Pubmed CrossRef
  52. Rose DB, Wolman SL, Ho CS. Gastric hemorrhage complicating percutaneous transgastric jejunostomy. Radiology. 1986;161:835-6.
    Pubmed CrossRef
  53. Youn BJ, Hur J, Lee KH, Won JY. Transarterial embolization of massive gastric ulcer bleeding in gastrostomy patients caused by a balloon replacement tube: a case report. J Korean Radiol Soc. 2007;56:137-9.
    CrossRef
  54. Seo N, Shin JH, Ko GY, Yoon HK, Gwon DI, Kim JH, et al. Incidence and management of bleeding complications following percutaneous radiologic gastrostomy. Korean J Radiol. 2012;13:174-81.
    Pubmed KoreaMed CrossRef
  55. Elmunzer BJ, Young SD, Inadomi JM, Schoenfeld P, Laine L. Systematic review of the predictors of recurrent hemorrhage after endoscopic hemostatic therapy for bleeding peptic ulcers. Am J Gastroenterol. 2008;103:2625-32 quiz 2633.
    Pubmed CrossRef
  56. Lewis MB, Lewis JH, Marshall H, Lossef SV. Massive hemorrhage complicating percutaneous endoscopic gastrostomy: treatment by means of transcatheter embolization of the right and left gastroepiploic arteries. J Vasc Interv Radiol. 1999;10:319-23.
    Pubmed CrossRef
  57. Bloechle C, Izbicki JR, Rashed MY, el-Sefi T, Hosch SB, Knoefel WT, et al. Hemobilia: presentation, diagnosis, and management. Am J Gastroenterol. 1994;89:1537-40.
    Pubmed
  58. Green MH, Duell RM, Johnson CD, Jamieson NV. Haemobilia. Br J Surg. 2001;88:773-86.
    Pubmed CrossRef
  59. Rhim H, Lim HK, Kim YS, Choi D, Lee KT. Hemobilia after radiofrequency ablation of hepatocellular carcinoma. Abdom Imaging. 2007;32:719-24.
    Pubmed CrossRef
  60. Goto E, Tateishi R, Shiina S, Masuzaki R, Enooku K, Sato T, et al. Hemorrhagic complications of percutaneous radiofrequency ablation for liver tumors. J Clin Gastroenterol. 2010;44:374-80.
    Pubmed CrossRef
  61. Yoshida J, Donahue PE, Nyhus LM. Hemobilia: review of recent experience with a worldwide problem. Am J Gastroenterol. 1987;82:448-53.
    Pubmed
  62. Velmahos GC, Demetriades D, Chahwan S, Gomez H, Hanks SE, Murray JA, et al. Angiographic embolization for arrest of bleeding after penetrating trauma to the abdomen. Am J Surg. 1999;178:367-73.
    Pubmed CrossRef
  63. Aideyan OA. Gastrointestinal bleeding. In: Ferral H, Bjarnason H, Qian Z, editors. Synopsis of Castaneda’s interventional radiology. Philadelphia: Lippincott Williams & Wilkins 2001:55-65.
  64. Merrell SW, Schneider PD. Hemobilia--evolution of current diagnosis and treatment. West J Med. 1991;155:621-5.
    Pubmed KoreaMed
  65. Srivastava DN, Sharma S, Pal S, Thulkar S, Seith A, Bandhu S, et al. Transcatheter arterial embolization in the management of hemobilia. Abdom Imaging. 2006;31:439-48.
    Pubmed CrossRef
  66. Rivera-Sanfeliz GM, Assar OS, LaBerge JM, Wilson MW, Gordon RL, Ring EJ, et al. Incidence of important hemobilia following transhepatic biliary drainage: left-sided versus right-sided approaches. Cardiovasc Intervent Radiol. 2004;27:137-9.
    Pubmed CrossRef
  67. Sarr MG, Kaufman SL, Zuidema GD, Cameron JL. Management of hemobilia associated with transhepatic internal biliary drainage catheters. Surgery. 1984;95:603-7.
    Pubmed
  68. Czerniak A, Thompson JN, Hemingway AP, Soreide O, Benjamin IS, Allison DJ, et al. Hemobilia. A disease in evolution. Arch Surg. 1988;123:718-21.
    Pubmed CrossRef
  69. Lü PH, Zhang XC, Wang LF, Chen ZL, Shi HB. Stent graft in the treatment of pseudoaneurysms of the hepatic arteries. Vasc Endovascular Surg. 2013;47:551-4.
    Pubmed CrossRef
  70. Savader SJ, Trerotola SO, Merine DS, Venbrux AC, Osterman FA. Hemobilia after percutaneous transhepatic biliary drainage: treatment with transcatheter embolotherapy. J Vasc Interv Radiol. 1992;3:345-52.
    Pubmed CrossRef
  71. Saad WE, Davies MG, Darcy MD. Management of bleeding after percutaneous transhepatic cholangiography or transhepatic biliary drain placement. Tech Vasc Interv Radiol. 2008;11:60-71.
    Pubmed CrossRef
  72. Freeman ML, Nelson DB, Sherman S, Haber GB, Herman ME, Dorsher PJ, et al. Complications of endoscopic biliary sphincterotomy. N Engl J Med. 1996;335:909-18.
    Pubmed CrossRef
  73. Loperfido S, Angelini G, Benedetti G, Chilovi F, Costan F, De Berardinis F, et al. Major early complications from diagnostic and therapeutic ERCP: a prospective multicenter study. Gastrointest Endosc. 1998;48:1-10.
    Pubmed CrossRef
  74. Cotton PB, Lehman G, Vennes J, Geenen JE, Russell RC, Meyers WC, et al. Endoscopic sphincterotomy complications and their management: an attempt at consensus. Gastrointest Endosc. 1991;37:383-93.
    Pubmed CrossRef
  75. So YH, Choi YH, Chung JW, Jae HJ, Song SY, Park JH. Selective embolization for post-endoscopic sphincterotomy bleeding: technical aspects and clinical efficacy. Korean J Radiol. 2012;13:73-81.
    Pubmed KoreaMed CrossRef


This Article


Cited By Articles
  • CrossRef (0)

Services
Social Network Service

e-submission

Archives