Biliary Varices on Endoscopic Ultrasonography: Clinical Presentation and Outcome

• Introduction
• Patients and Methods
• Results
• Description of Patients with EPVO
• EUS Findings
• Outcome
• Discussion
• Conclusions
• References

Background and Study Aims: Bile duct varices are not a well-recognized feature of portal venous obstruction. The aim of the present study was to describe the clinical and endosonographic features of biliary involvement in patients with extrahepatic portal venous obstruction (EPVO).

Patients and Methods: A retrospective study was conducted of the clinical features, outcome, and endosonographic findings (using Olympus EUM-3 or EUM-20 probes) in 21 patients with EPVO and endosonographic features of biliary varices. Biliary varices were defined as multiple, large, serpiginous, anechoic vascular channels in and/or surrounding the extrahepatic biliary tracts.

Results: Biliary varices have not previously been visible using conventional imaging methods (computed tomography and ultrasonography). They were identified using EUS in the wall of the common bile duct in 16 patients (76 %), surrounding the common bile duct (CBD) in 11 patients (52 %), and in the gallbladder in nine (43 %). The varices were the cause of obstructive jaundice in three of the 21 patients (14 %), but only when they were in the wall of the CBD. Two of these patients were treated using portosystemic shunting, and the other received a biliary endoprosthesis. The EUS examination also provided evidence of unrecognized pancreatic or biliary tumors in three other patients with EPVO of undetermined origin.

Conclusions: EUS can serve to diagnose biliary varices in patients with EPVO and jaundice. Although biliary varices are mainly asymptomatic, they may cause obstructive jaundice when they are located in the wall of the CBD. EUS can also detect unrecognized malignant tumors in patients with EPVO of undetermined origin.

Buts: Les varices des voies biliaires extra-hépatiques (VVB) au cours du cavernome portal sont mal connues. Le but de cette étude était de décrire les aspects cliniques et évolutifs des sujets avec un cavernome portal et des VVB diagnostiquées par échoendoscopie.

Malades et Méthodes: Les caractéristiques cliniques, évolutives et les aspects échoendoscopiques ont été analysés rétrospectivement chez 21 malades avec un cavernome portal et des VVB diagnostiquées par échoendoscopie (présence de canaux hypoéchogènes multiples au contact ou à l'intérieur des voies biliaires ou de la vésicule).

Résultats: Les VVB n'avaient pas été diagnostiquées par les examens d'imagerie conventionnels (échographie et tomodensitométrie). Les VVB ont été mises en évidence par échoendoscopie dans la paroi (n = 16; 76 %) et/ou au contact de la paroi (n = 11; 52 %) de la voie biliaire principale et/ou au niveau de la vésicule biliaire (n = 9; 43 %). Les VVB étaient responsables d'un ictère par obstruction de la voie biliaire principale dans 3/21 cas (14 %) et uniquement pour des VVB présentes dans la paroi de la voie biliaire. L'ictère a été traité par dérivation porto-cave (n = 2) ou par endoprothèse biliaire (n = 1). Chez trois malades avec un cavernome portal d'origine indéterminée, l'échoendoscopie a permis le diagnostic de tumeurs pancréatiques ou biliaires méconnues.

Conclusion: L'échoendoscopie permet le diagnostic de VVB chez les malades avec un cavernome portal et un ictère. Les VVB sont le plus souvent asymptomatiques, mais peuvent induire un ictère obstructif, uniquement si elles se développent dans la paroi de la voie biliaire principale.

Introduction

Biliary varices and portal cavernoma (cavernous hemangioma) are not well-recognized disorders. They may induce cholangiographic abnormalities and even jaundice, but are difficult to diagnose using conventional imaging procedures [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] . Endoscopic ultrasonography (EUS) may be an appropriate imaging procedure for the diagnosis of biliary involvement in patients with extrahepatic portal venous obstruction (EVPO), but its use has only been reported in a few cases [1] [9] . The aim of the present study was to describe the clinical and endosonographic features and outcome in patients with biliary varices.

Patients and Methods

We reviewed the charts of all patients with EVPO who were examined using EUS between 1991 and 1998 at our institutions. Among them, 21 patients (16 men, five women) with a median age of 50 years (range 22 - 75 years) had EUS features of biliary varices. The clinical findings, EUS features, and outcome were reviewed. In all of these patients, portal vein obstruction and portal hypertension had been diagnosed using transabdominal Doppler ultrasonography, based on the criteria presented by Kane and Katz [16], and also by computed tomography (CT).

The EUS examinations (using Olympus EU-M3 or EU-M20 probes, with switchable frequencies of 7.5 MHz and 12 MHz) were carried out with the patients under intravenous sedation (midazolam and propofol). A water-filled balloon was used to visualize the portal vein, superior mesenteric vein, common bile duct (CBD), gallbladder, and head of the pancreas, by positioning the probe in the upper duodenal curve and descending duodenum. The splenic vein and body and tail of the pancreas were visualized, and the gastric wall was visualized through the gastric antrum and corpus. Biliary varices were defined as multiple, large, serpiginous, anechoic vascular channels in and/or surrounding the wall of the CBD and/or gall bladder.

Results

Description of Patients with EPVO

The cause of EPVO was recorded as idiopathic in 11 patients (52.3 %), in whom imaging was negative and a bone marrow examination and coagulation tests were normal. EPVO was related to malignant disease in six patients (28.5 %) - with pancreatic tumors in three and hepatocellular carcinoma complicating alcoholic cirrhosis, cholangiocarcinoma, and multiple hepatic metastases of undetermined origin in one patient each. In the remaining four patients, the causes were miscellaneous, as follows: protein S deficiency, antiphospholipid syndrome, acute pancreatitis, and idiopathic neonatal EPVO with no evidence of umbilical sepsis, each in one patient. Abdominal pain was the most frequent mode of presentation (13 of 21 patients; 61.9 %) and was followed by jaundice, bleeding from esophageal varices, carcinoma diagnosis (two patients each), splenomegaly and work-up before liver transplantation for alcoholic cirrhosis (one patient each). Seven of the 21 patients (33.3 %) had biological and/or clinical manifestations of biliary disease, while the remainder were completely asymptomatic. Biliary varices were diagnosed before EUS in only one patient, who had jaundice and had been examined using endoscopic retrograde cholangiopancreatography (ERCP) and portal venography. Biliary varices had never been considered before EUS in the remainder of the patients, although they had all undergone both Doppler ultrasonography and CT imaging.

EUS Findings

Twenty-one patients underwent 24 examinations, with one patient having two (patient 1) and one having three (patient 19). There were no complications of EUS.

Thrombosis of the portal vein was visualized in all the patients as a solid, echogenic thrombus within the lumen of the vessel (Figure [1]). The EUS features of biliary varices were found surrounding the wall of the CBD in 11 patients (Figure [2]), and in the wall of the CBD in 16 patients (Figures [3], [4]). In three patients, obstruction of the CBD by enlarged choledochal varices located in its wall was the only identified cause of jaundice. The gallbladder was visualized in 15 patients (71.4 %; two had had a cholecystectomy, and in four others the gallbladder could not be imaged). Biliary varices were found using EUS in the wall of the gallbladder in nine patients (60 %). Features of biliary varices were found only in the gallbladder of a patient with cholangiocarcinoma who did not have EUS features of biliary varices in the CBD. Biliary varices were subsequently confirmed in eight patients using portal venography and in three patients at autopsy. EUS also detected three malignant tumors that were responsible for EPVO but had not been found on ultrasonography or CT. They included a pancreatic adenocarcinoma complicating chronic calcified pancreatitis, a neuroendocrine tumor of the tail of the pancreas, and a hilar biliary carcinoma with metastases.

Outcome

The follow-up period was an average of 13 months (range 2 - 60 months) in 19 of the 21 patients (90.5 %). In the three patients with CBD compression by biliary varices, jaundice was treated by portosystemic shunting in two cases and by placement of a biliary endoprosthesis in one. The jaundice resolved in one of the first two patients, and EUS examinations conducted four and 11 months after surgery showed regression of the biliary varices, but persistence of a varix on one side of the CBD wall, without duct dilation. Jaundice persisted in the other patient, as the caliber of the splenorenal shunt was too small. In the third patient, the jaundice rapidly improved after insertion of the endoprosthesis. After improvement of his clinical condition, this patient subsequently underwent surgery (splenorenal shunt) to prevent recurrent bleeding from esophageal varices; after that, he was lost to follow-up. Two patients with cholestasis related to carcinoma died of malignant disease progression. The patient with pancreatic carcinoma complicating chronic pancreatitis died of a stroke one month after the EUS diagnosis of cancer, and the patient with hepatocellular carcinoma died of terminal malignancy. The patient with a neuroendocrine tumor in the tail of the pancreas was treated by resection and chemotherapy, and was free of symptoms 60 months later. One patient underwent splenectomy. Eight patients (38.1 %) were treated with anticoagulants or antiplatelet drugs. An EUS examination three months later in patient 1 (who was treated medically, with anticoagulant therapy) showed recanalization of the portal vein, but persistent biliary varices around the CBD. One patient with bleeding from esophageal varices was treated using sclerotherapy and a beta-adrenergic blocking agent, and was asymptomatic 43 months later.

Discussion

EPVO is usually followed by collateral vein formation to bypass the obstruction, which then results in a portal cavernoma [17]. Biliary changes secondary to portal hypertension are not a well-recognized entity, and their clinical effects have been rarely reported [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] [14] [15] . The abnormal venous network surrounding the extrahepatic biliary tract may be difficult to visualize using Doppler ultrasonography and CT [5] [9] [16] , as in our series, and may require more invasive imaging techniques such as a portovenogram or ERCP for diagnosis [6] [7] [8] . There have been three main recent studies on cholangiographic abnormalities in EPVO with biliary involvement [13] [14] [15] . The major ERCP findings were narrowing and nodular extrinsic compression of the extrahepatic and intrahepatic bile ducts, and angulation of the bile duct. These features may mimic those induced by cholangiocarcinoma and sclerosing cholangitis [15]. However, cholangitis can also complicate the ERCP procedure, as reported by Choudhuri et al. [6]. Anecdotal reports have previously suggested the usefulness of EUS for the diagnosis of biliary varices [1] [9] . The present study, in a relatively large series of patients, shows that EUS examination using a radial echo endoscope can provide evidence of biliary varices involving the biliary tract, and may be able to delineate their location precisely in the wall of the CBD or surrounding it. The EUS features of biliary varices were confirmed by portal venography or autopsy in only 11 patients, however, so we are unable to state the precise accuracy of EUS for the diagnosis of biliary tract involvement in patients with EPVO. EUS remains one of the most accurate and least invasive procedures for the diagnosis of extrahepatic cholestasis [18], and should theoretically have a good sensitivity and specificity in diagnosing biliary varices. The transabdominal sonographic features of EPVO in portal hypertension have been well described [16]. The endosonographic abnormalities seen in and surrounding the extrahepatic biliary tree are similar to the sonographic features described in portal hypertension - i.e., multiple, large, serpiginous, anechoic vascular channels.

EUS examination using a linear sectional electronic device can provide Doppler color images, and may theoretically be more appropriate for detecting venous abnormalities in the CBD [19]. However, in our experience electronic linear sectional EUS is not as accurate as mechanical radial EUS for studying the CBD. Magnetic resonance imaging of the bile duct (magnetic resonance cholangiopancreatography, MRCP) appears to be a very accurate noninvasive method of visualizing the biliary tree, but its use in patients with EPVO has rarely been reported [11]. However, MRCP, like ERCP, probably demonstrates only the indirect intraductal effects of biliary varices, rather than visualizing the varices themselves. Clinically, biliary varices were responsible for obstructive jaundice in three of the 21 patients in this series (14.3 %). In all three cases, EUS showed that the varices were in the wall of the CBD. The relative infrequency of jaundice in patients with biliary varices and EPVO is in agreement with the findings of two previous reports in which cholangiographic abnormalities were identified in all patients with EPVO - with obstructive jaundice in only three of 21 patients (14.3 %) in one report, and in one of 20 patients (5 %) in the other [13] [14] . The findings of the present study also show that biliary varices can involve the gallbladder wall in up to 60 % of patients, and may be exclusively located in the gallbladder, as observed in one patient. No symptoms resulted from gallbladder involvement in this series, although a case of hepatic colic related to a portal cavernoma has been reported [20].

It is noteworthy that in this series, EUS examination also detected pancreatic and biliary tumors not identified using conventional ultrasonography or CT in three patients with EPVO. A neoplastic cause of EPVO was found in 28 % of the patients in this study - a higher rate than has usually been reported in the literature, as the main causes of portal vein thrombosis in adults are thrombotic disorders [20]. The frequency of malignant tumors in the present series may be due to a recruitment bias, as EUS was frequently requested for staging of a previously diagnosed carcinoma. Whatever the cause, EUS examination may be of value in patients with EPVO of undetermined origin.

Conclusions

This series of 21 patients with extrahepatic portal venous obstruction and biliary varices suggests that biliary varices may induce bile duct obstruction (14 % of cases). EUS can distinguish between asymptomatic varices surrounding the bile duct and those within the CBD wall, which may obstruct the duct. From a clinical point of view, the indications for EUS in the work-up of patients with EPVO are probably limited. EUS may be of value in two particular subsets of patients: a) those with obstructive jaundice and negative ultrasound and CT findings, as EUS may demonstrate obstructive varices involving the wall of the CBD and thus guide the therapeutic approach; and b) in patients with EPVO of undetermined origin, when EUS may be able to detect an asymptomatic tumor of the pancreas or of the extrahepatic bile ducts.

References

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Ph.D. M.D., CellierC. 

Service de Gastroentérologie Hôpital Laennec and Hôpital Européen Georges Pompidou

42, rue de Sèvres

75007 ParisFrance

Phone: +33-1-44 39 67 99

Email: christophe.cellier@lnc-ap-hop-paris.fr

References

• 1 Béjanin H, Baumann R, Choury A, et al. Cavernome portal comprimant la voie biliaire. Etude de 3 cas.  Gastroenterol Clin Biol. 1993;  17 134-138
  PubMedSearch in Google Scholar
• 2 Spira R, Widrich WC, Keusch KD, et al. Bile duct varices.  Arch Surg. 1985;  120 1194-1196
  PubMedSearch in Google Scholar
• 3 Meredith HC, Vujic I, Schabel ST, O'Brien PH. Obstructive jaundice caused by cavernous transformation of the portal vein.  Br J Radiol. 1978;  51 1011-1012
  PubMedSearch in Google Scholar
• 4 Mackenzie RL, Tubbs HR, Laws JW, et al. Obstructive jaundice and portal vein calcification.  Br J Radiol. 1978;  51 953-955
  PubMedSearch in Google Scholar
• 5 Williams SM, Burnett DA, Mazer MJ. Radiographic demonstration of common bile duct varices.  Gastrointest Radiol. 1982;  7 69-70
  CrossrefPubMedSearch in Google Scholar
• 6 Choudhuri G, Tandon RK, Nundy S, Misra NK. Common bile duct obstruction by portal cavernoma.  Dig Dis Sci. 1988;  33 1626-1628
  CrossrefPubMedSearch in Google Scholar
• 7 Kim S, Chew FS. Choledochal varices.  AJR Am J Roentgenol. 1988;  150 578-580
  PubMedSearch in Google Scholar
• 8 Theravit L, Fauces B, Pissas A, et al. Endoscopic management of obstructive jaundice due to portal cavernoma.  Endoscopy. 1993;  25 423-425
  PubMedSearch in Google Scholar
• 9 Perlemuter G, Béjanin H, Fritsch J, et al. Biliary obstruction caused by portal cavernoma: a study of 8 cases.  J Hepatol. 1996;  25 58-63
  CrossrefPubMedSearch in Google Scholar
• 10 Löhr JM, Kuchenreuter S, Grebmeier H, et al. Compression of the common bile duct due to portal-vein thrombosis in polycythemia vera.  Hepatology. 1993;  17 586-592
  PubMedSearch in Google Scholar
• 11 Ros PR, Viamonte MJR, Soila K, et al. Demonstration of cavernomatous transformation of the portal vein by magnetic resonance imaging.  Gastrointest Radiol. 1986;  11 90-92
  PubMedSearch in Google Scholar
• 12 Hiatt JR, Quinones-Baldrich WJ, Ramming KP, et al. Bile duct varices: an alternative to portoportal anastomosis in liver transplantation.  Transplantation. 1986;  42 85
  PubMedSearch in Google Scholar
• 13 Khuroo MS, Yattoo GN, Zargar SA, et al. Biliary abnormalities associated with extrahepatic portal venous obstruction.  Hepatology. 1993;  17 807-813
  CrossrefPubMedSearch in Google Scholar
• 14 Dilawari JB, Chawla YK. Pseudosclerosing cholangitis in extrahepatic portal venous obstruction.  Gut. 1992;  33 272-276
  PubMedSearch in Google Scholar
• 15 Bayraktar Y, Balkanci F, Kayhan B, et al. Bile duct varices or “pseudo-cholangiocarcinoma sign” in portal hypertension due to cavernous transformation of the portal vein.  Am J Gastroenterol. 1992;  87 1801-1806
  PubMedSearch in Google Scholar
• 16 Kane RA, Katz SG. The spectrum of sonographic findings in portal hypertension: a subject review and new observations.  Radiology. 1982;  142 453-458
  PubMedSearch in Google Scholar
• 17 Webb Q, Sherlock S. The aetiology, presentation and natural history of extra-hepatic portal venous obstructions.  Q J Med. 1979;  192 627-639
  PubMedSearch in Google Scholar
• 18 Amouyal P, Palazzo L, Amouyal G, et al. Endosonography: promising method for diagnosis of extrahepatic cholestasis.  Lancet. 1989;  ii 1195-1198
  PubMedSearch in Google Scholar
• 19 Rösch T. Endoscopic ultrasonography.  Endoscopy. 1994;  26 148-168
  PubMedSearch in Google Scholar
• 20 Valla D, Casadevall N, Huisse MG, et al. Etiology of portal vein thrombosis in adults: a prospective evaluation of primary myeloproliferative disorders.  Gastroenterology. 1988;  94 1063-1069
  PubMedSearch in Google Scholar

Ph.D. M.D., CellierC. 

Service de Gastroentérologie Hôpital Laennec and Hôpital Européen Georges Pompidou

42, rue de Sèvres

75007 ParisFrance

Phone: +33-1-44 39 67 99

Email: christophe.cellier@lnc-ap-hop-paris.fr