Gastrointest Interv 2012; 1:3–10

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Gastrointestinal Intervention

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Review Article Diagnosis and management of ectopic varices

Nabeel M. Akhter, Ziv J. Haskal* abstract

Ectopic varices are large portosystemic collaterals in locations other than the gastroesophageal region. They account for up to 5% of all variceal bleeding; however, hemorrhage can be massive with mortality reaching up to 40%. Given their sporadic nature, literature is limited to case reports, small case series and reviews, without guidelines on management. As the source of bleeding can be obscure, the physician managing such a patient needs to establish diagnosis early. Multislice computed tomography with contrast and reformatted images is a rapid and validated modality in establishing diagnosis. Further management is dictated by location, underlying cause of ectopic varices and available expertise. Therapeutic options may include double balloon enteroscopy, transcatheter embolization or sclerotherapy, with or without portosystemic decompression, i.e., transjugular intrahepatic portosystemic shunts. In this article we review the prevalence, etiopathogenesis, anatomy, presentation, and diagnosis of ectopic varices with emphasis on recent advances in management. Copyright Ó 2012, Society of Gastrointestinal Intervention. Published by Elsevier. All rights reserved.

Keywords: Balloon-occluded retrograde transvenous obliteration, Ectopic varices, Portal , Percutaneous embolization, Transjugular intrahepatic portosystemic shunt

Introduction duodenal varices.5 Anorectal varices have been reported in approx- imately 44% of patients with ,6 although only a fraction The term “ectopic varices” has historically been used to describe become symptomatic. Thus, true incidences are likely subject to abnormally dilated associated with gastrointestinal mucosa reporting bias and the modality used for diagnosis and only a fraction with propensity for gastrointestinal hemorrhage, and it has also been of diagnosed ectopic varices are likely to become symptomatic. loosely used for portosystemic collaterals in the abdominal wall and fi retroperitoneum. Ectopic varices may be best de ned as large pres- Etiology and pathogenesis surized portosystemic venous collaterals occurring anywhere in the 1,2 abdomen except in the gastroesophageal region. Ectopic varices represent natural portosystemic shunts 3 Ectopic varices account for up to 5% of all variceal bleeding. secondary to . These collaterals occur where the They may be present in , , , colon, ano- portal venous system is in juxtaposition to the systemic venous , peristomal, biliary, peritoneal, retroperitoneal, umbilical, system. Under normal circumstances the resistance within these urinary bladder, uterine, ovaries, and other locations. collaterals is high, while it is low in the portal venous system. With the development of intrahepatic portal hypertension, these shunts Prevalence act to divert flow from the increased intrahepatic vascular resis- tance. Surgical literature and cadaveric studies have shown porto- In a review of 169 cases of bleeding ectopic varices, 26% bled from systemic communications via (a) gastroesophageal plexus to peristomal varices,17%from duodenal,17%from jejunal and ileal,14% azygous-coronary system, (b) hemorrhoidal plexus, (c) recanalized from colonic, 9% from peritoneal, 8% rectal, and a few from infrequent umbilical , and (d) pancreatoduodenal venous arcade to inferior sites such as the ovary and vagina.1 A study of 37 patients with vena cava through retroperitoneal veins of Retzius. Most reported cirrhosis who underwent capsule endoscopy, 8.1% were found to cases of hemorrhage from ectopic varices in the West are associated have small bowel varices.4 One 1968 angiographic study of patients with intrahepatic portal hypertension in contrast to extrahepatic with portal hypertension demonstrated an unusually high rate of portal hypertension, because of low prevalence of the latter. Prior paraduodenal varices, in 46 out of 106 (40%) patients; this likely abdominal surgery predisposes patients with portal hypertension to described all regional venous collaterals, and not solely submucosal develop varices in unusual locations, like urinary bladder, ovaries

University of Maryland School of Medicine, Baltimore, MD, United States Received 14 July 2012; Revised 14 July 2012; Accepted 31 July 2012 * Corresponding author. Division of Vascular and Interventional Radiology, University of Maryland School of Medicine, 22 South Greene Street, Baltimore, MD 21201, United States. E-mail address: [email protected] (Z.J. Haskal).

2213-1795/$ – see front matter Copyright Ó 2012, Society of Gastrointestinal Intervention. Published by Elsevier. All rights reserved. http://dx.doi.org/10.1016/j.gii.2012.08.001 4 Gastrointestinal Intervention 2012 1(1), 3–10 and bare area of the liver due to adhesions.1,2,7 Finally, ectopic varices diaphragm, splenic ligament or in the rectovesical region may can develop in the absence of portal hypertension due to congenital rupture into the peritoneal cavity, leading to occult, potentially fatal anomalous portosystemic anastomoses,8 abnormal vessel struc- intraperitoneal hemorrhage.19,23,24 tures,9 arteriovenous fistulae,10 rare familial conditions,11 or related Brisk upper gastrointestinal bleeding and should to thromboses.12 be first evaluated with emergency upper gastrointestinal endos- Wall tension in all varices is a recognized risk factor for rupture. copy. If this fails to define an acute source of hemorrhage, intra- Per LaPlace’s law it is proportional to transmural pressure across venous contrast enhanced computed tomography (CT) may be the vessel wall and the radius of the vessel. Hence, portal pressure preferable to colonoscopy (in the unprepped acute setting). Thus, and vessel size are determinants of ectopic variceal hemorrhage.13 presence of ectopic varices should be strongly considered in In our and others’ experience ectopic varices, like patients with known or stigmata of portal hyperten- may bleed at a portosystemic gradient of less than 12 mmHg.14,15 sion, particularly when both upper and lower endoscopies fail to emphasizing the need for different transcatheter treatments then identify a source of bleeding.2 Elective capsule endoscopy has been those used for bleeding . successful in detecting jejunal and small bowel varices,4,25 although its role in acute bleeding is small. Similarly, double balloon Presentation and diagnosis enteroscopy or push enteroscopy has the potential to visualize the greater small bowel and allow intervention.3,26 Endoscopic ultra- Ectopic varices present in a multitude of ways. For example, sound has been reported for the hemodynamic assessment of duodenal varices may manifest with mild or massive rectal27 and biliary varices.28 or lower gastrointestinal bleeding.16 Intestinal varices distal to Color Doppler ultrasound has shown its value in the diagnosis of duodenum, usually present with hematochezia, , or intra- umbilical (Fig. 1A and D), duodenal,29 rectal,30 gall bladder,21 and – peritoneal bleeding.17 19 Urinary bladder varices may present with choledochal varices.31 However, intravenous contrast enhanced hematuria,20 and biliary varices with biliary obstruction,21 or rarely multislice CT (Fig. 2A and B), should be considered the primary hemobilia and gastrointestinal bleeding.22 Ruptured varices at the modality for diagnosis of ectopic varices, given the rapid and right diaphragm can cause hemothoraces and dyspnea.23 Abdom- ubiquitous availability. CT, CT angiography, and CT enteroclysis have inal wall varices (e.g., umbilical) can rupture externally or inter- all been used for successful diagnosis of duodenal32,33 and colonic nally, whereas those located around the falciform ligament, varices.34 While technetium TC-99m red blood cell scintigraphy has

Fig. 1. A 53-year-old female with history of alcoholic cirrhosis transferred from outside the hospital with external bleeding around the umbilicus from cutaneous varices. (A) Preprocedure color Doppler ultrasound in periumbilical region shows flow in varices (white arrow); (B) digital subtraction image DSA from the transjugular intrahepatic porto- systemic shunt (TIPS) procedure during the initial portogram shows the left portal vein (white arrow), with retrograde flow in the recanalized umbilical vein (black arrows), leading to large periumbilical varices (lowest black arrow). Initial portosystemic gradient: 21 mmHg; (C) portogram after TIPS and embolization of umbilical vein varix with liquid embolic agent (Onyx, ev3 Endovascular, Inc. Plymouth, MN. USA), shows antegrade flow without retrograde filling of umbilical vein. Post TIPS portosystemic gradient: 15 mmHg; (D) post- TIPS and embolization ultrasound of periumbilical region shows thrombus in the periumbilical varices (white arrows). Nabeel M. Akhter and Ziv J. Haskal / Diagnosis and management of ectopic varices 5

Fig. 2. A 54-year-old male with history of alcoholic cirrhosis presented with massive lower gastrointestinal bleeding, and was hypotensive with systolic of 50 mmHg. (A) Axial image from contrast-enhanced computed tomography (CT) shows a large superior mesenteric vein (white arrow head), cecal and ascending colon varices (white arrow); (B) coronal reformatted image from contrast enhanced CT shows cecal and ascending colon varices (white arrow), large right pleural effusion representing hepatic hydrothorax (asterisk); (C) DSA from the transjugular intrahepatic portosystemic shunt (TIPS) procedure with catheter in peripheral superior mesenteric vein shows retrograde flow in cecal and ascending colon varices (black arrows) with portosystemic shunt through retroperitoneal veins draining into inferior vena cava (white arrow). Initial portosystemic gradient: 12 mmHg; (D) image during embolization of cecal varices with multiple coils and liquid embolic agent (Onyx), balloon inflated (black arrow) in peripheral superior mesenteric vein to promote ; (E) DSA after TIPS showing antegrade flow in portal vein and non filling of cecal varices. Post TIPS portosystemic gradient: 7 mmHg. After the procedure patient became hemodynamically stable and was extubated 2 days later, with no more episodes of hematochezia.

been used,35 its modern role in this setting is appropriately Jejunal, ileal, colonic, and anorectal varices diminishing. Finally, contrast-enhanced three-dimensional magnetic resonance (MR) angiography36 can equally outline Small bowel varices are commonly seen in patients with intra- unusual portosystemic collaterals, but has little role in the acute hepatic portal hypertension who have previously undergone setting. Of note, barium studies of the colon or small bowel may abdominal surgery. Adhesions bring the parietal surface of the misdiagnose ectopic varices as polyps or tumors,11 emphasizing the viscera in contact with the abdominal wall, and portal hypertension importance of tomographic imaging and clinical suspicion. results in formation of varices below the intestinal mucosa.7 A triad of portal hypertension, hematochezia without hematemesis and prior abdominal surgery characterize hemorrhage from small Specific anatomic locations intestinal varices.43 These varices most commonly flow into systemic circulation through the gonadal veins, and less commonly Duodenal varices through branches of the internal iliac veins. Rectal varices are distinguished from by their Cirrhosis is the most commonly associated cause of duodenal typical presence above the dentate line. The differentiation of varices, accounting for 30% of the cases,37 but causes vary and hemorrhoids and anorectal varices is an important one. Anal vari- include portal and obstruction of the splenic ces collapse with digital pressure, whereas hemorrhoids do not; of vein and inferior vena cava.38,39 Duodenal varices have also note, the prevalence of hemorrhoids in patients with liver disease is developed after band ligation of esophageal varices, presumably as not higher than in the general population.6 These varices represent alternate sites of spontaneous portosystemic shunting.40 These a portosystemic collateral pathway between the superior rectal varices are formed by the collateral veins originating from the veins of the inferior mesenteric system to the middle and inferior portal vein trunk or superior mesenteric vein draining into the rectal veins of the iliac system (Fig. 3). They can be present with inferior vena cava through retroperitoneal veins of Retzius.41 mild or uncontrolled hematochezia.44 The most common colonic Duodenal variceal rupture can lead to severe hemorrhage, with sites are the cecum (Fig. 2C) and rectum,45 although isolated mortality as high as 40% from initial bleeding.42 colonic varices, in the authors experience, rank among the rarest. 6 Gastrointestinal Intervention 2012 1(1), 3–10

Stomal varices

Ectopic stomal varices refer to abnormally dilated veins that have developed in the stomal mucosa, often recognized by a purplish hue around the stoma.2 They are common in patients with intrahepatic portal hypertension secondary to primary sclerosing cholangitis,7 and are frequently seen in patients with ileostomies after procto- colectomy for inflammatory bowel disease associated with primary sclerosing cholangitis (Fig. 4A).46 The mechanism of stomal variceal hemorrhage is related to local trauma and variceal erosion.18 The overall morbidity is high, given the propensity for recurrent bleeding requiring multiple blood transfusions but mortality is low, between 3% and 4%,47 because of the ability to institute local measures such as pressure dressing, epinephrine soaked gauze, gel foam packing, and suture ligation. These therapies are however, not effective in preventing recurrent bleeding.48 Importantly, stomal varices can be missed by endoscopy, emphasizing the need for clinical suspicion and CT imaging in occult cases.

Biliary tract varices

In extrahepatic , gall bladder and common varices can occur in as many as 30% of patients.21 They maybe an incidental finding or present with biliary obstruction secondary to mass effect on extrahepatic bile ducts.31 The appear- ance of biliary tree, by direct endoscopic retrograde chol- angiopancreatography may mimic that of primary sclerosing cholangitis, and is termed as pseudosclerosing cholangitis.21 Rarely, Fig. 3. A 49-year-old female with history of primary biliary cirrhosis presented with biliary varices can lead to hemobilia or even catastrophic upper gastrointestinal hemorrhage. Repeated endoscopy and banding was unable to hemorrhage.22 stop hemorrhage. Balloon tamponade was done with an orogastric tube. DSA during the transjugular intrahepatic portosystemic shunt (TIPS) procedure with the catheter fl fi in the inferior mesenteric vein (black arrows) shows retrograde ow, with lling of Vesical varices and other unusual sites hemorrhoidal plexus and anorectal varices (white arrow). Initial portosystemic gradient: 18 mmHg and post TIPS gradient: 6 mmHg. Post TIPS there was no retrograde flow in inferior mesenteric vein and anorectal varices. The upper gastrointestinal The urinary bladder wall is an unusual collateral route for hemorrhage ceased, and the balloon tamponade tube was deflated at end of procedure. venous splanchnic blood flow and these varices may develop after The patient was discharged from hospital after 5 days. abdominal surgery secondary to adhesions.7 Bleeding from vesical varices is a rare event in patients with portal hypertension and an

Fig. 4. Middle-aged male with uncontrolled bleeding from a recent ileostomy, with no source detected on endoscopy. (A) DSA during the transjugular intrahepatic portosystemic shunt (TIPS) procedure with the catheter in the peripheral superior mesenteric vein shows stomal varices (white arrow), a faint outline of the ileostomy bag is seen (black arrows); (B) post coil embolization (white arrows) of stomal varices, with the catheter in the superior mesenteric vein (black arrows), shows non-filling of stomal varices. The TIPS resulted in cessation of further bleeding from the stoma. Nabeel M. Akhter and Ziv J. Haskal / Diagnosis and management of ectopic varices 7 unusual cause of hematuria20; however, due to intraperitoneal oft-quoted for esophageal varices (12 mmHg). As ectopic varices hemorrhage, this can be catastrophic.19 decompress through varied pathways other then the coronary– Other more unusual sites include right diaphragm,23 splenore- azygous system, procedural endpoints must be individualized. In nal ligament,24 splenoparametrial,49 adnexal,50 vaginal,51 umbilical the authors’ experience, endoscopically verified selective decom- (Fig. 1),52 and cutaneous varices53 leading to unusual manifesta- pression of esophageal, but not gastric varices can occur at tions like pleural effusion, dyspnea, hematuria, and percutaneous 12 mmHgdthe same phenomenon holds for ectopic varices, exsanguination. emphasizing the need for routine definitive embolization or sclerotherapy in cases where TIPS are created. While TIPS provide Management a primary intervention or salvage modality in duodenal,42 small bowel,66 colonic (Fig. 2D and E),66 anorectal (Fig. 3),67 stomal (Fig. 4A There are no randomized trials or set guidelines that dictate the and B),68 urinary,69 umbilical (Fig.1B and C), and cutaneous70 variceal management of bleeding ectopic varices. The management hemorrhage, the need for concomitant embolization must be depends upon location of hemorrhage, presentation, local physi- emphasized. In bleeding ectopic varices, TIPS with embolization was cian expertise, and the underlying causes of portal hypertension. A superior with only two out of seven patients presenting with multidisciplinary team approach is in order, with input from rebleeding in comparison to five out of 12 patients that had TIPS only intensivists, gastroenterologists, interventional radiologists, and without initial embolization.62 The decision to use a TIPS-approach surgeons. The medical management of variceal hemorrhage is depends upon local expertise, and the severity of underlying liver discussed in other texts and we will confine our discussion to disease and comorbidities (e.g., Model of End Stage Liver Disease interventional management. (MELD) score, encephalopathy, ischemic liver disease). Finally, shunts can be reduced or even reversed should portal decompression prove Endoscopic interventional procedures excessive.

Many ectopic varices are within reach of standard endoscopy,7 Balloon occluded retrograde transvenous obliteration (B-RTO) and, with the advent of double balloon or push enteroscopy, the As opposed to TIPS, which is a shunt creation procedure, B- reach has extended even further.26 The options include endoscopic RTO is a shunt occlusion procedure. Further, it uses a retrograde band ligation (EBL) and endoscopic injection sclerotherapy (EIS) rather than antegrade approach. This technique has been with different agents including N-butyl-2-cyanoacrylate (NBCA), employed for control of gastric variceal bleeding, with success thrombin or other sclerosants. EBL was found to be superior to EIS rates reaching 89%,71 without detriment in hepatic function or in for the treatment of esophageal varices, on the basis of lower . However, since increased portal pres- rebleeding rate, mortality, complications, speed of application, and sure is not addressed by this procedure, there is a risk of the need for fewer endoscopic treatments; however, the main increased pressure and bleeding from varices that have not been disadvantage remains the observed higher rate of variceal recur- sclerosed and are at other sites, or development of ascites. rence in comparison to sclerotherapy. Sclerotherapy on the other Aggravation of esophageal varices is recognized after B-RTO of hand may lead to deep ulceration, which can lead to rebleeding, gastric varices.72 To forego or salvage bleeding from varices after B- stricture formation, or perforation.54,55 Combination of two in the RTO, different procedures have been utilized, including TIPS,73 percu- form of endoscopic scleroligation (ESL), has shown to be superior taneous obliteration,74 and endoscopic interventions.57 While largely with decreased recurrence rates.56 No set protocol exists for the use used for primary prophylaxis of gastric varices in the East, increasing of above mentioned modalities for the management of ectopic case reports have described its successful role in treatment of varices varices and the choice is often situation and expertise dependent. within the duodenum,57,75 small bowel,76 colon,77 stoma,78 and Endoscopic band ligation and sclerotherapy have been mesentery.79 successfully used solo or in combination with each other and other interventional radiological modalities in controlling hemorrhage Percutaneous embolization from duodenal,57,58 jejunal,26 colonic,59 anorectal,60 and stomal Percutaneous embolization has been widely reported using varices.61 a transhepatic approach. While, successful embolization rates reach 80%, up to 65% rebleeding rate within 5 months have been Interventional radiological procedures described.80 The earlier use of this approach largely predates the routine role of TIPS for other indications. The transhepatic route Multiple image-guided approaches to management of ectopic may provide more rapid access to portal system for some less- varices have been extensively reported. They include direct experienced operators; however, its added risks include trans- percutaneous access to varices, antegrade and retrograde scle- hepatic tract bleeding, recurrent hemorrhage due to lack of secondary rotherapy and/or embolotherapy, and portosystemic shunts. portal decompression, and added contraindications in ascites Transjugular and transhepatic as well as retrograde transjugular or patients. Certainly embolization is important for durable control of transfemoral venous approaches have been proven useful. varices.81 In cases where decompression is contraindicated, a trans- jugular approach (without shunt creation) can still provide direct Transjugular intrahepatic portosystemic shunts (TIPS) access to the varices. In some cases, portal hypertension leading to Many publications have emphasized the role of TIPS in the varices may be wholly due to extrahepatic obstruction, e.g., after management of bleeding ectopic varices in cirrhotics caused by Whipple or similar surgeries. Correction of portal vein stenoses or intrahepatic portal hypertension.14,42,62 TIPS have proven more thromboses with stents may provide adequate decompression and effective in preventing recurrent esophageal variceal rebleeding restore hepatopetal flow.82 Finally, more recent case reports have than endoscopic therapy.63,64 It has been shown that a >50% described direct, ultrasound guided abdominal wall,52 or stomal reduction in pressure gradient protected patients from rebleeding variceal,83 puncture, and sclerotherapy or coil embolization. Percu- and even a reduction between 25% and 50% was also effective, taneous embolization by itself or in association with other interven- with a probability of rebleeding of only 7% and less risk of tional modalities has been reported for management of hemorrhage encephalopathy and .65 The portosystemic gradient from ectopic varices in duodenum,84 small bowel,25,82 anorectum,85 thresholds for adequate ectopic varix decompression are not those stoma,47,81,83 mesentery,86 umbilicus,52 and urinary bladder.87 8 Gastrointestinal Intervention 2012 1(1), 3–10

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