Sonographic Findings of Hepatobiliary ... - Wiley Online Library

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ORIGINAL RESEARCH

Sonographic Findings of Hepatobiliary Fascioliasis Accompanied by Extrahepatic Expansion and Ectopic Lesions Memik Teke, MD, Hakan Önder, MD, Mutalip Çiçek, MD, Cihad Hamidi, MD, Cemil Göya, MD, Mehmet Güli Çetinçakmak, MD, Salih Hattapoğlu, MD, Burak Veli Ülger, MD Article includes CME test

Objectives—The aim of the study was to describe the sonographic findings of hepatobiliary fascioliasis with extrahepatic expansion and ectopic lesions. Methods—The study included 45 patients with fascioliasis. All diagnoses were confirmed via serologic enzyme-linked immunosorbent assays. Sonographic findings in the hepatobiliary system, extrahepatic expansion, and ectopic lesions were defined. Results—The most common hepatic lesions were subcapsular localized, small, confluent, multiple hypoechoic nodules with poorly defined borders. We also detected ectopic lesion in 5 patients (11.1%) and live parasites in the gallbladder and bile duct in 11 (24.4%). Conclusions—The large spectrum of entities in the differential diagnosis of hepatobiliary fascioliasis may lead to misdiagnosis and incorrect treatment. However, the diagnosis can be made when the characteristic sonographic features are seen, such as heterogeneity of the liver with multiple poorly defined hypoechoic-isoechoic lesions and multiple echogenic nonshadowing particles in the gallbladder or common bile ducts. Nonetheless, the differential diagnosis of fascioliasis versus other hepatic lesions may still be difficult. In these situations, pathologic confirmation should be performed to exclude the possibility of malignancy. Key Words—ectopic lesion; extrahepatic expansion; Fasciola hepatica; gastrointestinal ultrasound; sonography

Received January 28, 2014, from the Departments of Radiology (M.T., H.Ö., C.H., C.G., M.G.Ç., S.H.), Microbiology (M.Ç.), and General Surgery (B.V.Ü.), Medical School, Dicle University, Diyarbakir, Turkey. Revision requested February 3, 2014. Revised manuscript accepted for publication March 26, 2014. We thank the Dicle University Bilimsel Araştırma Projeleri for assistance with manuscript preparation. Address correspondence to Memik Teke, MD, Department of Radiology, Medical School, Dicle University, Yenişehir, 21280 Diyarbakir, Turkey. E-mail: [email protected] doi:10.7863/ultra.33.12.2105

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epatobiliary fascioliasis is a parasitic infection that is endemic in sheep- and cattle-farming areas of South America, Europe (Portugal, France, Spain, and Turkey), Eastern Asia, Egypt, and Iran.1 The disease is caused by the trematode Fasciola hepatica. It is transmitted to humans via contaminated water or green vegetables such as watercress (Nasturtium officinale).1–3 When the infectious form of the trematode (metacercariae) reaches the stomach by ingestion, the outer shell of the metacercariae melts. The nematode then penetrates the intestinal wall to reach the peritoneum and climbs to the surface of the liver. Finally, it penetrates the Glisson capsule and enters the liver parenchyma to reach the bile ducts.4 Hepatobiliary fascioliasis has 2 phases: hepatic and biliary, which can be seen separately or together.5 The hepatic phase begins within 1 to 3 months after ingestion of metacercariae. This phase comprises focal hepatic lesions, subcapsular collections, and inflammation of the liver capsule. During the acute invasive stage of the disease, hypoechoic areas inside the liver, expansion of

©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:2105–2111 | 0278-4297 | www.aium.org


Teke et al—Hepatobiliary Fascioliasis with Extrahepatic Expansion and Ectopic Lesions

the capsule into the peritoneal cavity, and splenomegaly are typically observed. In the latent and chronic stages of the disease, worms or eggs may obstruct the extrahepatic biliary ducts and can cause biliary tree obstruction symptoms.6 Knowledge of the diagnostic imaging features of fascioliasis is essential because of the large spectrum of entities in the differential diagnosis of hepatobiliary fascioliasis, which include hepatitis, cholecystitis, cholangitis, liver abscesses, brucellosis, and hepatobiliary malignancies. Misdiagnosis may lead to incorrect treatment or unnecessary surgery. Especially, extrahepatic expansion and ectopic lesions of F hepatica may be confused with tumoral masses or abscesses. The diagnosis of fascioliasis relies on serologic and parasitologic tests and imaging techniques.7 The specificity and sensitivity of the serologic test are high, but the test cannot differentiate between acute and chronic infections; also, the sensitivity of the parasitologic test is low. Therefore, appropriate imaging is important for the differential diagnosis and treatment decisions. The classic computed tomographic findings in fascioliasis have been described by several authors8–10; however, sonographic findings are less frequently described in the literature.2,11 In this study, our primary aim was to describe the sonographic features of fascioliasis. Sonography was chosen because it is a useful, easily accessible, and low-cost imaging method for detection of hepatic and biliary lesions.

Materials and Methods This retrospective study was undertaken at the Department of Radiology of Dicle University. The medical records of 45 patients with a diagnosis of F hepatica infection between January 2011 and September 2013 were systematically reviewed. The diagnosis was confirmed by serologic methods using enzyme-linked immunosorbent assays. Stool examinations were not performed. Patients in this study included 36 women (80%) and 9 men (20%) who ranged from 18 to 72 years old (mean ± SD, 39.7 ± 12.3 years). Five of the patients were from the same family. The study was approved by the Institutional Review Board and Protocol Review Committee. All patients underwent abdominal sonography. Sonographic examinations were performed by 2 radiologists with at least 5 years of experience, using a scanner with a 3.5-MHz convex array broadband probe (Aplio XG; Toshiba Medical Systems Co, Ltd, Tokyo, Japan). Sonographic findings were classified as hepatic lesions, extrahepatic expansion, accompanying ectopic lesions, biliary lesions, and others. Echogenicity, the number and distribution of the lesions, the wall thickness of the bile duct

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and gallbladder, living parasites, and accompanying findings (hepatomegaly, splenomegaly, and abdominal fluid) were recorded. Extrahepatic expansion was defined as the presence of hepatic contour bulging by nodules, whereas an ectopic lesion was defined as involvement of tissue other than the liver due to parasite migration. In the patients with extrahepatic expansion and parenchymal solitary lesions, color Doppler sonography was performed to detect the vascularity in these lesions, if present. A biopsy was performed if necessary. The size of the liver was measured at the right midclavicular line (with measurement from the hepatic dome to the inferior hepatic tip). Hepatomegaly was accepted as a liver length of greater than 15.5 cm.12 The spleen was considered enlarged if it was longer than 12 cm in patients older than 50 years and longer than 14 cm in younger patients.9 Increased wall thickness was defined as a visible wall for the bile duct and greater than 3 mm for the gallbladder.13 Patients who had malignancies were excluded from the study.

Results We detected 56 hepatic lesions in 40 patients (88.9%) in our study. We also detected ectopic lesions in 5 patients (11.1%), periportal lymphadenopathy in 20 (44.4%), gallbladder wall thickening in 22 (48.9%), bile duct thickening in 12 (26.7%), and live parasites in the gallbladder and bile duct in 11 (24.4%). In 5 patients (11.1%), a lesion could not be seen on sonography. Liver echogenicity was hypoechoic in 23 patients, hyperechoic in 6, and heterogeneous in 11. Liver lesions were multiple in 34 patients and solitary in 6. The most common hepatic lesions were subcapsular localized, small (up to 25 mm in diameter), confluent, multiple hypoechoic nodules with poorly defined borders (Figure 1). Color Doppler sonography was performed, and there was no vascularity in any of the lesions (Figure 2). Necrotic areas were seen especially in larger lesions (Figure 3). In 6 patients, sonography revealed a solitary lesion. Four of them were seen as areas of increased echogenicity in the right lobe, and 2 lesions had a subcapsular heterogeneous nodular appearance. Three patients had extrahepatic expanded hypoechoic nodular lesions. Two of them were subdiaphragmatic, and the other was perigastric (Figure 4). Color Doppler sonography and biopsy were performed for confirmation. There was no vascularity in any of the lesions, and histologic examination revealed nongranulomatous eosinophilic infiltrates without evidence of malignant degeneration.

J Ultrasound Med 2014; 33:2105–2111



Ectopic lesions were observed in 5 patients. Ectopic sites included the peritoneum in 3 patients, pancreas in 1, and spleen in 1 (Figure 5). Aspiration biopsy of the peritoneal lesions revealed necrotic material. On follow-up sonography 6 months after the biopsy, no change was visible in the dimensions of the cysts in 2 patients. However, Figure 1. Transverse sonogram showing multiple hypoechoic nodules with poorly defined borders.

there was regression in the splenic, pancreatic, and other dimensions of the cystic lesions after therapy (Figure 6). Biliary abnormalities were observed in 22 patients (48.9%). The most common biliary findings were increased wall thickness of the gallbladder and biliary tree. In 8 patients, live parasites appeared as mildly hyperechoic leaflike mobile structures ranging from 4 to 21 mm in the gallbladder (Figure 7), and nonshadowing echogenic areas in the dilated biliary tree in 3 patients (Figure 8). We found periportal hilar lymph node enlargement in 20 patients (40%). Most of the enlargements were multiple, and their sizes ranged from 8 to 35 mm (Figures 9 and 10).

Figure 4. Transverse sonogram showing a subcapsular hypoechoic expanded nodular lesion (arrow). LN indicates lymph node.

Figure 2. Color Doppler sonogram showing no vascularity in the lesions of an 18-year-old man with fascioliasis.

Figure 5. Transverse sonogram showing a poorly defined heterogeneous hypoechoic ectopic pancreatic lesion (arrow) in a patient with fascioliasis.

Figure 3. Sonogram showing hypoechoic necrotic areas (arrows), especially in larger lesions.


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Hepatomegaly was detected as an accompanying finding in 8 patients, splenomegaly in 4, and perihepatic fluid in 6. On follow-up sonography, hypoechoic residual lesions were detected after 1 year in 4 patients. Wall thickening of the common bile duct and echogenic particles were also observed in the gallbladders of the same patients.

Discussion

Figure 6. Ectopic peritoneal cystic lesion (arrows) before (A) and after (B) treatment. There was a decrease in the cyst size and a partial decrease in debris.

Figure 7. Multiple flukes in the common bile duct (arrows) of a 45-yearold woman.

Since diagnosis and treatment decisions are driven by imaging and serologic tests, it is important to know the imaging features of fascioliasis. The diagnostic accuracy of sonography is high for fascioliasis, with imaging character-

A

Figure 8. Floating echo (arrows) with no acoustic shadowing in the gallbladder of a 52-year-old woman.

B

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istics such as heterogeneity of the liver with multiple poorly defined hypoechoic lesions, dilated bile ducts, thickening of the gallbladder wall, multiple echogenic nonshadowing particles in the gallbladder or common bile ducts, and periportal lymph node enlargement. However, imaging features of fascioliasis may overlap with other hepatic lesions, which may lead to misdiagnosis and unnecessary surgical procedures such as cholecystectomy and hepatic segmentectomy. In this study, we primarily described the sonographic features of fascioliasis. Sonography was used because it is a useful, easily accessible, and low-cost imaging method for detection of hepatic and biliary lesions. Important imaging features in the differential diagnosis of hepatic fascioliasis are multiplicity, poorly defined borders of confluent nodules, and absence of a halo.9 These were the most common findings in our study. However, if Figure 9. Enlarged periportal lymph nodes (arrows). L indicates liver.

Figure 10. Enlarged periportal lymph nodes (LAP, arrow) in another patient.


the lesions are solitary, extrahepatically expanded, or largely necrotic, they may be confused with tumors, metastases, or abscesses.14,15 The differential diagnosis of hepatic fascioliasis is presented in Table 1. In our study, we detected solitary lesions in 6 patients and extrahepatically expanded lesions in 3. For differentiation of these lesions, biopsies were performed. On color Doppler sonography, there was no vascularity in any of the lesions. Histologic examination revealed necrosis and nongranulomatous eosinophilic infiltrates in solitary and extrahepatically expanded lesions. In 1 solitary lesion fragment, migrating larvae were seen. Fasciola hepatica primarily involves the liver; however, ectopic migration to other locations may occur. The precise route of migration toward ectopic sites is unclear but most often occurs in the acute stage of the disease.16 Extrahepatic fascioliasis has been reported in foci such as the subcutaneous tissue, brain, lungs, epididymis, inguinal lymph nodes, stomach, cecum, and colon.4 Although the radiologic presentations of the disease are contradictory, reporting any new set of images related to the unusual organ involvement is of paramount importance. We detected ectopic lesions in 5 patients (3 peritoneal, 1 pancreatic, and 1 splenic). On color Doppler sonography, there was no vascularity in any of the lesions. A pathologic examination of the pancreatic and splenic lesions was not performed for confirmation; however, improvement in the lesions on follow-up imaging studies after treatment indicated the involvement of those regions by the parasite. In our study, 5 of the patients, 4 of whom were female, were members of the same family, who lived in rural areas. Their clinical and sonographic findings differed from each other. These findings may have been due to consumption of the parasite at different times as well as their bodies’ reactions to the parasite. Unlike the other family members, the male patient had an ectopic splenic lesion. Pancreatic fascioliasis is extremely rare, and only 2 cases have been reported in the English medical literature.17,18 The authors believed that abnormal migration of a fluke into the pancreas had caused a chronic inflammatory response, simulating a pancreatic tumor. If there were an assemblage of indirect evidence of ectopic fascioliasis, invasive surgery purely for the discovery of flukes could be avoided.18 One of the patients in our study had a pancreatic lesion as well. On follow-up imaging studies after treatment, there was regression in the size of the pancreatic lesion. In this study, we found no lesions but minimal heterogeneity in 5 patients. Isoechoic or slightly hypoechoic liver lesions may be missed on sonography if not performed in the acute stage of the disease.

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Table 1. Differential Diagnosis of Hepatic Fascioliasis Cause Amoebic liver abscess Hydatid cyst disease Pyogenic liver abscess Pyogenic perihepatic abscess Malignancy

Distinguishing Features Usually solitary, typically round or oval and sharply defined Membranes, daughter cysts, and calcifications can be seen, based on the cyst stage Clusters of small pyogenic abscesses coalesce into a single large cavity (cluster sign) Difficult to differentiate morphologically from hematoma secondary to Fasciola ; may contain gas within the abscess May have internal vascularity and a peripheric halo

Table 2. Differential Diagnosis and Characteristics of Biliary Fascioliasis Mobile Nonshadowing Gallbladder Echogenicity Gallstones