International Journal of Gastrointestinal Intervention

Gastrointest Interv 2018;7:142–149

Gastrointestinal Intervention

journal homepage: www.gi-intervention.org

Review Article Essential vascular anatomy and choice of embolic materials in gastrointestinal bleeding Somrach Thamtorawat,1,* Chandran Nadarajan,2 Satit Rojwatcharapibarn1

A B S T R A C T

Non-variceal gastrointestinal bleeding is the significant emergency problem to manage in the hospital. Transcatheter arterial embolization is mini- mally invasive treatment, which becomes an essential role in controlling bleeding, leading to lifesaving. To reach the goal, the interventional radiologist should have fundamental of vascular anatomy and choice of embolic material, which is the key to success. Copyright © 2018, Society of Gastrointestinal Intervention.

Keywords: Anatomy; Embolization; Gastrointestinal bleeding

Introduction celiac artery (CA), superior mesenteric artery (SMA), inferior mesenteric artery (IMA), and the internal iliac artery. The CA arises Gastrointestinal (GI) bleeding is a typical scenario that can be from the abdominal aorta at T12–L1 level. Trifurcation of the CA present in an emergency situation which can be a life-threatening is found in the majority of the population (89%), composing of a condition. Mortality rates as high as 10% to 14% have been re- left gastric artery (LGA), a common hepatic artery, and a splenic ported.1 The estimated annual incidence is approximately 20 to artery. A total of twelve variations of the CA was reported by 150 cases per 10,000 persons.2 Cause of GI bleeding can be clas- Song et al.4 The SMA provides the primary blood supply to the sified into variceal and non-variceal bleeding. A multidisciplinary small bowel, the ascending colon, and the transverse colon via team consisting of members of the endoscopy, surgery, and radi- the inferior pancreaticoduodenal artery, jejunal artery, ileal artery, ology department are necessary for the initiation of the appropri- ileocolic artery, and the middle colic artery (MCA). Sometimes, a ate treatment strategy. Most of the time, conservative medical and replaced hepatic artery may arise from the proximal part of SMA.4 endoscopic treatments are the primary treatment choices used The IMA is a small artery arising anteriorly from the abdominal to achieve hemostasis in GI bleeding patients. However, uncon- aorta at L3–L4 level. The IMA provides the left colic artery (LCA) trolled bleeding after a failure of endoscopic treatment can occur, which supplies the descending colon and anastomoses with the especially in non-variceal GI bleeding. Nowadays, endovascular SMA at splenic flexure. The sigmoidal artery also originates from treatment is the preferred option comparing to surgical treatment the IMA, and it supplies the sigmoid colon. The terminal branch due to the less invasive nature of the procedure and associated of this artery is the superior rectal artery which supplies the up- less morbidity and mortality rates.3 Adequate knowledge of the per rectum. Lastly, the anterior division of the internal iliac artery GI vascular anatomy is utmost necessary to perform angiography gives rise to the middle and inferior rectal arteries which supply and transcatheter arterial embolization (TAE) successfully in treat- the middle and lower rectum. ing GI bleeding patients. Stomach Vascular Anatomy for GI Bleeding The stomach is the largest alimentary tract organ. It has Four major abdominal vessels that supply the GI tract are the several vascular supplies which mainly arises from the CA. The

1Department of Radiology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, Thailand 2Department of Radiology, School of Medical Sciences, Health Campus, Universiti Sains Malaysia, Kelantan, Malaysia Received July 16, 2018; Revised September 1, 2018; Accepted September 1, 2018 * Corresponding author. Department of Radiology, Faculty of Medicine Siriraj Hospital, Mahidol University, 2 Prannok Road, Bangkoknoi, Bangkok 10700, Thailand. E-mail address: [email protected] (S. Thamtorawat). ORCID: https://orcid.org/0000-0003-2977-4723 pISSN 2213-1795 eISSN 2213-1809 https://doi.org/10.18528/gii180028 This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Somrach Thamtorawat et al. / TAE for GI bleeding 143 gastric cardia and fundus are supplied by the LGA and short gas- branch arises either from a common ascending branch with the tric artery (ShGA). The lesser curvature is supplied mainly by the LCA or as a separate descending branch.8 LGA. The proximal greater curvature is supplied by the ShGA and left gastroepiploic artery (LGEA). The distal greater curvature of Rectum the stomach receives arterial supply from the right gastroepiploic arteries (RGEA) in 42% to 78% of cases while the rest is from Rectum receives blood supply from branches of the IMA and the right gastric artery (RGA).5 The anterior wall of the antrum is the internal iliac arteries. The superior rectal artery which arises supplied by the RGEA and the lower anterior branch of the LGA from the IMA supplies the upper rectum. This artery forms an while the posterior wall is supplied by the RGA and the lower anastomosis with the middle rectal artery, inferior rectal artery posterior branch of LGA. The RGEA and RGA supply pylorus. and the marginal artery.8 Middle and inferior rectal arteries are The ShGA and LGEA arise from the splenic artery while the branches of the internal iliac artery and internal pudendal artery, LGA arises directly from the CA in more than 90% of cases. An respectively. A dominant retrosigmoid collateral supply from the accessory LGA is reported in 1.8% to 2% of the European popula- internal iliac has been reported previously.9 tion.5 The RGA commonly arises from either the common hepatic artery or left hepatic artery. In a small portion of the population, Key Collateral Pathway it could arise from the gastroduodenal artery (GDA), the middle hepatic artery or the right hepatic artery. The RGEA arises from Extensive collateral blood flow is common, especially in the the GDA. The GDA arises from the common hepatic branch of the upper GI tract but it is rare in the colon. Collateral pathway has CA in 75% of cases. In the rest, it arises from the left or right he- a role in preventing end-organ ischemia. However, in the case of patic artery or the SMA.5 GI bleeding, the collateral pathway can also be a risk factor for treatment failure. This phenomenon is commonly seen in the case Duodenum of the duodenal bleeding, which has dual blood supply from both the GDA and the inferior pancreaticoduodenal artery. Emboliza- Duodenum is the first part of the small intestine, supplied tion of only one of the arterial branches may result in treatment mainly by the GDA. Ligament of Treitz, which is found in the failure (Fig. 1). The collateral pathways could be formed between duodenojejunal junction, divides the location of the GI bleeding branches of the same trunk such as between LGA and RGA, or into the upper and lower GI tract which is essential in bleeding it could be between branches of two different trunks such as the management.3,6 The duodenal bulb is supplied by the supraduode- anastomosis of SMA branches and CA branches in the pancreati- nal artery, which is a proximal branch of GDA.7 The anterior and coduodenal arcade. The common pathways are as below. posterior pancreaticoduodenal arcades supply the anterior and posterior surface of the duodenum. The arcades are formed by Collateral between the branches of CA (Fig. 2) the anterior superior pancreaticoduodenal artery, retroduodenal artery and the inferior pancreaticoduodenal artery. Both anterior 1. The branch of the LGA anastomoses with ShGA at the level superior pancreaticoduodenal artery and retroduodenal artery are of the fundus.5 branches of the GDA while the inferior pancreaticoduodenal is 2. The branch of the LGA and the RGA anastomose with each a right branch of SMA. The inferior pancreaticoduodenal artery other at the level of the body and pylorus. arise as dual anterior and posterior branch in 60% of the popula- 3. A right side branch of the dorsal pancreatic artery anasto- tion while the rest of the population will have a single artery.8 moses with the branches from the anterior superior pancreaticoduodenal artery or the RGEA. Jejunum and ileum 4. The epiploic branches of the RGEA and LGEA forms the posterior omental arcade of Barkow. Branches from this arcade Jejunum and ileum are supplied by the respective branches forms anastomoses with the branches from the inferior pancre- arising from the SMA. There are 4 to 6 jejunal branches and 9 to aticoduodenal artery, transverse pancreatic artery, MCA and the 13 ileal branches. Terminal ileum, cecum and inferior half of the LCA.5,8 ascending colon are supplied by the ileocolic artery arising as the terminal branch of SMA. The ileal and colic branches form the il- Collateral between the branches of CA, SMA, IMA and internal eocolic loop. This loop gives rise to appendicular and anterior and iliac artery (Fig. 3) posterior cecal arteries which supply appendix and cecum.8 1. The persistent embryonic anastomotic branch between CA Colon and SMA is called the arc of Buhler. 2. Anterior and posterior gastroduodenal arcade formed by Main vascular supply of the colon is SMA and IMA. The the anastomosis between the superior pancreaticoduodenal artery ascending colon and the right half of the transverse colon are and retroduodenal artery of the GDA with the inferior pancreati- supplied by the right and middle colic arteries which arise from coduodenal artery of the SMA. the right side of the SMA. Splenic flexure and descending colon 3. The ascending branch of the LCA anastomoses with the are supplied by LCA which is an ascending branch of the IMA. branch of the MCA, creating the arc of Riolan (medial) and mar- The sigmoidal branch of the IMA supplies the sigmoid colon. The ginal artery of Drummond (lateral).8,9 right and middle colic arteries arise as a common trunk in more 4. Superior rectal artery of the IMA forms an anastomosis than half of populations. In some case, MCA arises from the CA.8 with the middle rectal artery and inferior rectal artery which are The MCA is also reported to be absent in 2% to 22% of subjects,9 the branches of the internal iliac artery and internal pudendal ar- while the right colic artery, could be absent in up to 50% of the tery, respectively.8 population.10 The MCA extends to supply the splenic flexure when the LCA is absent in about 7% of populations.9 The sigmoidal 144 Gastrointestinal Intervention 2018 7(3), 142–149

A B C

D E

Fig. 1. A 30-year-old man had a motor vehicle accident. Computed tomography scan found small pseudoaneurysm of gastroduodenal artery (GDA). (A) GDA angiogram found a small pseudoaneurysm (arrow). (B) Microcoil (arrow) embolization was performed at the proximal part of the parent artery. (C) Backflow filling into the pseudoaneurysm (arrow) was detected from inferior pancreaticoduodenal artery angiogram. (D) Further microcoil packing at the distal parent artery was done (arrowhead). (E) The celiac angiogram showed no demonstrable of pseudoaneurysm (arrow).

LGA 1 ShGA 1 CA

RGA SPA CA LGA HA GDA SMA proper 2 MCA 2 SPA

GDA LGEA 3 3 DPA 3 IMA

LCA 4 RGEA SRA

4 IIA

Fig. 2. Collateral between the branches of celiac artery. CA, celiac artery; LGA, left gastric artery; SPA, splenic artery; ShGA, short gastric artery; LGEA, left gastroepiploic artery; DPA, dorsal pancreatic artery; RGEA, right gastroepiploic artery; GDA, gastroduodenal artery; HA proper, hepatic artery proper; RGA, Fig. 3. Collateral between the branches of CA, SMA, IMA and internal iliac right gastric artery. Refer to “Collateral between the branches of CA” section artery. LGA, left gastric artery; CA, celiac artery; SPA, splenic artery; GDA, in the main text for the definition of 1 to 4. gastroduodenal artery; SMA, superior mesenteric artery; MCA, middle colic artery; IMA, inferior mesenteric artery; LCA, left colic artery; SRA, superior rectal artery; IIA, internal iliac artery. Refer to “Collateral between the branches of CA, SMA, IMA and internal iliac artery” section in the main text for the definition of 1 to 4. Somrach Thamtorawat et al. / TAE for GI bleeding 145

Extra-alimentary Source of GI Bleeding a patient with a clinical presentation of GI bleeding and a history of prior biliary intervention or liver trauma, hemobilia should be Hemobilia considered.12,13 TAE is one of the good options to treat hemobilia. Hepatic artery and GDA pathology should be focused during an- Hemobilia is defined as bleeding into the biliary system which giography in case of iatrogenic bleeding (Fig. 4).14 could be either bleeding into the intrahepatic or extrahepatic duct. It is an unusual source of GI bleeding in daily practice. The Hemosuccus pancreaticus blood from the biliary system could pass into the bowel, and the patient can present with GI bleeding signs and symptoms. Over Hemosuccus pancreaticus is a rare source of GI bleeding. It 50% of the etiology has iatrogenic cause such as secondary to is defined as bleeding from ampulla of Vater via the pancreatic biliary intervention procedure which accidentally created a fistu- duct.15,16 Possible causes of hemosuccus pancreaticus include acute lous communication between vessels and bile ducts. Pathologic or chronic pancreatitis, pancreatic trauma, vascular malformation vessels commonly from the artery however portal vein injury and pancreatic tumor. Chronic pancreatitis is the most common could be the cause of the hemobilia.11 Other known causes are cause. It occurs due to pancreatic enzyme induced peripancreatic biliary tumor or cholelithiasis but they are a less common occur- vascular wall injury and leads to the development of pseudoan- rence. The most common presentation of hemobilia is melena. In eurysm. The GI bleeding can occur from the splenic artery, GDA, pancreatic artery, and pancreaticoduodenal artery in this condition (Fig. 5).17 The endovascular intervention plays a significant role in treating this condition.

Imaging Evaluation for GI Bleeding

The site of bleeding identification is the key to success in either surgical or endovascular treatment. Multi-detector computed tomography (MDCT) is the non-invasive imaging modality of choice due to diagnostic ability and fast acquisition time.18 Newer generation MDCTs have increased temporal and spatial resolution which allows it to provide better details regarding the site and cause of bleeding. Such data helps interventionist in plan- ning TAE approach.19 CT angiography (CTA) able to detect bleeding which is at the rate of 0.35 mL/min.18,19 Images are acquired in the arterial phase, venous phase, and delayed phase. Arterial phase imaging is done roughly 30 seconds after intravenous (IV) contrast infusion. This phase is crucial in mapping the mesenteric vasculature and identifying the site of bleeding. Cross-referencing the arterial phase with either the non-contrast or venous phase (acquired roughly 60 seconds post IV contrast injection) helps in differentiating hemorrhage with intrinsically hyperdense bowel 18 Fig. 4. A 76-year-old woman had recurrent gallstone pancreatitis. She under- contents (e.g., old ingested barium or suture). The important went endoscopic retrograde cholangiopancreatography with biliary stent limitation of CTA is the inability to detect intermittent bleeding. placement to relieve biliary obstruction. After biliary stent removal, she de- However, in patients with lower GI tract bleeding with stable he- veloped hematemesis. Angiogram found active contrast extravasation from modynamic status, the risk of rebleeding is reported as low if the the right hepatic artery (arrowhead) into common bile duct (arrow), suggested 18 hepatic artery injury causing hemobilia and upper gastrointestinal bleeding. initial CTA is negative. Tagged red blood cell scintigraphy can detect bleeding as

A B C

Fig. 5. A 37-year-old man with chronic pancreatitis presented with upper gastrointestinal bleeding. (A) Non-enhanced computed tomography (CT) scan found multiple pancreatic calcifications (arrowheads) with a large hyperdense mass at the tail of the pancreas (arrow). (B) Arterial-phase CT scan showed large pseudoaneurysm (arrow) originating from the distal transverse pancreatic artery (arrowhead). (C) Superior mesenteric artery angiogram found a prominent size of transverse pancreatic artery and pseudoaneurysm (arrowhead) at the distal part, causing hemosuccus pancreaticus. 146 Gastrointestinal Intervention 2018 7(3), 142–149 slow as 0.1 mL/min and have the ability to detect intermittent target vessels as possible. Careful monitoring of reflux is essential bleeding through sequential scans. However, it has a poor spatial to prevent non-target embolization. resolution, and it is difficult to pinpoint the exact site of bleeding The advantages of GS are easy to use, widely available, inex- especially in the small bowel.18 It is also time-consuming and not pensive and has a temporary embolic effect. In the cases where appropriate in the acute setting.19 the micro-catheter cannot reach to the target point, GS can be Angiography meanwhile plays a dual role, both as a diagnos- infused to reduce the blood flow and promote hemostasis. The GS tic tool as well as a therapeutic tool in dealing with GI bleeding. particle can achieve a temporary embolic effect and disperse eas- It has the sensitivity of detecting the bleeding rate of 0.5 to 1.0 ily in case of massive extravasation (Fig. 6). mL/min.18 It should be considered in cases of recent ongoing GI bleeding even if the CTA is negative.19 The diagnostic accuracy of Polyvinyl alcohol and microsphere arteriography is reported as high if it is performed during the epi- sode of active bleeding.6 Polyvinyl alcohol (PVA) or microsphere is a permanent embolic material, with particle sizes ranging from 40 to 1200 µm. Choice of Embolic Materials The PVA is an old particulate embolic material which is a non- radioopaque material with an irregular surface. The PVA can be TAE is effective in controlling acute GI bleeding, especially in mixed with contrast medium to make it visible during injection. circumstances where an endoscopic or surgical approach is not However, clumping of the PVA particle does occur commonly due suitable. TAE aims to stop bleeding without significant collateral to the irregular surface and obstructs the catheter. damage. Interventionist should have a good knowledge of various Microsphere agents are made from acrylics, hydrogels, resins, embolic material used to achieve the goal of treatment. Optimal polymers, or glass. Its major advantage is the uniform shape and embolization depends on the vascular pathology and bleeding smooth surface which reduces the clumping effect. It allows easier site. In general, embolization should be performed as close to the delivery through the small micro-catheters. bleeding site as possible to reduce the risk of complications. The use of permanent particle agent is to reduce the vascular supply of the bleeder. The size of the particulate agent chosen in Gelatin sponge GI bleeding should not be smaller than 500 µm to avoid ischemic complication.22 However, due to the risk of infarction, the opera- Gelatin sponge (GS) is a widely available embolic material tor must be cautious during embolization particularly in colonic used by interventional radiologist especially in the management bleeding.23 of hepatocellular carcinoma and acute arterial bleeding. GS is made from either the bovine or porcine collagen. It is a water- Coil insoluble hemostatic agent. GS is a temporary embolic material as it resolves spontaneously over a period of 2 to 6 weeks. However, The coil is considered as a large permanent embolic material. it can produce permanent embolization effect by inducing arte- It is available in a variety of sizes, lengths, and shapes. It occludes ritis effect and intimal hyperplasia.20 The embolic effect of GS is the bleeding vessel by causing mechanical obstruction as well dependent on the coagulation profile of the patient. Therefore, in as promotes hemostasis at the pathologic vessels. The diameter a patient with severe coagulopathy, clinical failure of the hemo- of the coil ranges from 2 to 18 mm. Two delivery systems of the stasis can occur.21 coil are available in the market which is the detachable and non- GS slurry can be prepared via two steps. Firstly, the GS is cut detachable type. The detachable coil is safer to be used during the into small 1 mm cubes and mixed with contrast medium. It is coil packing. It prevents non-target embolization and misplace- followed by another step which is called ‘the pumping method’. ment of the coil. Two diameters of coil wire are available cur- It uses two syringes to pump the GS across a three-way stopcock rently which is the 0.035 inch and 0.018 inch systems. Nowadays, valve to form the slurry consistency. The accurate size and con- the 0.018 inch microcoil systems are becoming more popular due centration of GS are very challenging to be accurately estimated. to the ability to be used in a more distal embolization. During embolization, the catheter should be placed as close to the The main advantage of the coil is it could be placed at a pre-

A B C

Fig. 6. A 70-year-old man with a history of advanced colonic cancer of descending colon. (A) Coronal computed tomography image showed circumferential colonic mass (arrow) at the descending colon. (B) The middle colic angiogram demonstrated a hypervascular mass (arrow) with no contrast extravasation at descending colon. (C) Gelatin sponge was used to embolize this mass, angiogram after embolization revealed marked decreased vascularization of the tumor (arrow). Somrach Thamtorawat et al. / TAE for GI bleeding 147 cise location. If a medium or large pathologic vessel is needed to and needed to be handled by an experienced interventional radi- embolize, such as GDA, the coil is the most suitable choice. A coil ologist.26 is also commonly used in the treatment of GI bleeding secondary NBCA must be delivered mixed with lipiodol and under fluo- to pseudoaneurysm. It is used to occlude the parent artery. The roscopic guidance. Such a mixture has two significant roles; one drawback is that the coagulation disorder may affect the efficacy it opacify the liquid to allow visualization during injection, and of embolization. Post coiling recurrent hemorrhage rate of up to another one is it allows the control of the polymerization time. 20% was reported among GI bleeding patients with coagulopa- The lesser the concentration of NBCA in the mixture, the longer it thy.21,24 A single coil is rarely enough to get total vascular occlu- takes to polymerize and therefore allows a more distal emboliza- sion; therefore most procedure requires the usage of a few coils. It tion. The operator could control the NBCA flow by adjusting the leads to longer operation time and higher cost (Fig. 7). mixture concentration and injection rate. A forceful injection can In cases of patients with positive GI bleeding findings in ei- make the NBCA go fast but also increases the risk of the reflux ther endoscopic or CTA but negative findings in the conventional into the proximal non-target vessel. Before NBCA injection, flush- angiography, the coil embolization can be used as an empirical ing the delivery catheter with 5% dextrose solution is crucial to treatment as it is safe and effective.25 Two vessels which are com- prevent premature polymerization within the catheter and thus monly embolized empirically are the LGA and GDA. occluding it. Immediately pull out of the catheter is also vital to prevent adherence of the catheter to vessel wall. N-butyl cyanoacrylate The critical complication that could occur during the NBCA embolization, particularly in the colon, is ischemia secondary to N-butyl cyanoacrylate (NBCA) is a liquid embolic material insufficient collateral flow. The animal studies had shown that the which has been used in the interventional radiology field for sev- embolization of three or fewer vasa recta is safe and have a low eral years. There are many advantages of NBCA. Firstly, the NBCA risk of infarction. In a human study, it is reported that one vasa can reach the pathology point via bloodstream even in cases recta embolization is relatively safe but two or more branches where the microcatheter cannot reach the target especially due to may cause insignificant or self-limited ischemic damage.27 Risk the severe tortuosity of the vessel. Secondly, it helps to prevent of bowel ischemia evaluated by large meta-analysis states the the retrograde backdoor filling of the collateral vessel. Lastly, the complication rate secondary to NBCA embolization for upper GI NBCA can cause vascular blockage by polymerization, indepen- bleeding and lower GI bleeding was 5.4% and 6.1%, respectively. dent of coagulation status of the patient. The major drawback of This number is within the reported complication range of TAE for NBCA is the difficulty to handle the rate and flow of the material GI bleeding which ranges from 0% to 12% (Fig. 8).28,29

A B C

D E

Fig. 7. A 70-year-old man, who had a history of chronic pancreatitis, presented with upper gastrointestinal bleeding. (A) Non-enhanced computed tomography (CT) scan found diffuse swelling of the pancreas (arrow) and small hematoma at distal common bile duct (arrowhead). (B) Arterial-phase CT scan showed a small pseudoaneurysm (arrowhead) at distal gastroduodenal artery (GDA) (arrow). (C) GDA angiogram revealed small pseudoaneurysm (arrowhead) at distal GDA. (D) Super- selective angiogram found active contrast extravasation from an aneurysm (arrowhead) into the duodenum (arrow). (E) Then, four pieces of 2-mm interlocking coil were placed into the targeted vessel (arrow). Angiogram after embolization found absent of contrast extravasation. 148 Gastrointestinal Intervention 2018 7(3), 142–149

Fig. 8. A 38-year-old man had recurrent hematochezia. (A) Superior mesenteric artery (SMA) angiogram demonstrated a point of extravasation at jejunum (arrowhead). (B) Superselective angiogram into vasa recta of the pathologic vessel (arrow) was performed. Then, 50% N-butyl cyanoacrylate was used to embolize it. (C) SMA angiogram post embolization showed absence of contrast extravasation (arrow).

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is a unique multidisciplinary society to encourage and facilitate clinical and scientific collaboration

between radiologists, surgeons and gastroenterologists.

Endoscopy Radiology Surgery

Our Goals:

Multi-disciplinary Collaboration to promote world-wide Expertise Establish a comprehensive GI intervention network among endoscopists, interventional radiologists and gastrointestinal surgeons for multidisciplinary collaboration and interaction

Sharing and advancing technological Innovations Inform, promote and globalize the many outstanding technological innovations of each of the specialties

Foster future Specialists Aid young brilliant doctors to make an early debut on the international stage through SGI

Become a Role Model Showcasing the benefits of multi-disciplinary collaboration in science, education and clinical practice