Hepatobiliary Fascioliasis: Sonographic and CT Findings in 87 Patients During the Initial Phase and Long-Term Follow-Up

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1 Sonography and CT of Hepatobiliary Fascioliasis Hepatobiliary Imaging Clinical Observations dnan Kabaalioglu 1 Kagan Ceken 1 Emel limoglu 1 Rabin Saba 2 Metin Cubuk 1 Gokhan rslan 1 li paydin 1 Kabaalioglu, Ceken K, limoglu E, et al. Keywords: CT, Fasciola hepatica, fascioliasis, liver disease, sonography DOI: /JR Received February 26, 2007; accepted after revision May 13, Supported by the kdeniz University Scientific Research Projects Unit. 1 Department of Radiology, kdeniz University Hospital, Dumlupınar Cad , ntalya, Turkey. ddress correspondence to. Kabaalioglu (adnank@akdeniz.edu.tr). 2 Department of Infectious Diseases and Clinical Microbiology, kdeniz University Hospital, ntalya, Turkey. JR 2007; 189: X/07/ merican Roentgen Ray Society Hepatobiliary Fascioliasis: Sonographic and CT Findings in 87 Patients During the Initial Phase and Long-Term Follow-Up OJECTIVE. The purpose of our study was to describe the initial and long-term imaging findings in hepatobiliary fascioliasis. CONCLUSION. Most patients with fascioliasis have typical hepatobiliary imaging findings. It is important to know that residual fibrotic or necrotic foci may remain for years after cure. Long-term complications are rare in fascioliasis, and malignancy or cirrhosis related to the disease has not been observed. epatobiliary fascioliasis is caused H by the trematode Fasciola hepatica. The worldwide increase in the diagnosis of fascioliasis is related to the increased availability and use of sonography and CT, awareness of the important role of imaging in diagnosis, and recent development of specific serologic tests. Several case reports from 51 countries in five continents show that fascioliasis is not a rare disease [1]. Fascioliasis is endemic in some parts of South merica (olivia, Peru, Chile), Cuba, Egypt, and Iran. Endemic regions have also been reported from Europe (Portugal, France, Spain, Turkey) and Eastern sia (Vietnam, Japan, Korea) [1]. The main sources of infestation are watercress and similar green vegetables on which the infective metacercaria form of the parasite are attached. The swallowed larvae penetrate the bowel wall and find their way to the liver. In a patient with fascioliasis, common symptoms are right upper quadrant pain, fever, weight loss, fatigue, pruritus, skin rashes, dyspepsia, nausea, and vomiting. The differential diagnosis includes a large spectrum of diseases: hepatitis, cholecystitis, cholangitis, liver abscess, brucellosis, and primary and secondary hepatobiliary malignancies. ecause fascioliasis may mimic several hepatobiliary disorders, misdiagnosis or late diagnosis is still frequent and may lead to unnecessary surgical procedures such as cholecystectomy and hepatic segmentectomy [2 4]. Furthermore, delay in treatment may cause the patient to suffer long-standing biliary symptoms and face an increased risk of pigment gallstones [1]. Therefore, appropriate imaging is important in the differential diagnosis. Confirmation of the diagnosis should be based on serology or visualization of eggs in endoscopically or percutaneously aspirated bile, liver tissue, or stool [1, 5]. lthough chronic hepatobiliary damage in human fascioliasis is unusual, in some patients the incidental imaging of fibrotic liver nodules after months or years may be confusing for radiologists who are not familiar with the long-term findings of this disease. Our purpose is to report the initial diagnostic radiologic findings of the disease and the imaging features at long-term follow-up. Materials and Methods In our hospital, 87 patients with fascioliasis were diagnosed between 1995 and ll patients underwent upper abdominal sonography and CT. Diagnosis was confirmed in all patients by serologic methods using enzyme-linked immunosorbent assay (ELIS). Forty-nine patients were female and 38 were male, with an age range of 9 75 years (mean, 47 years). Written permission for this study was obtained from the institutional ethics board. Sonography was performed with a 3.75-MHz convex probe (SS 270 or pplio 80, Toshiba). Sonographic follow-up was planned at 1, 3, 6, and 12 months after treatment or until the lesions resolved. Triphasic helical CT was performed (Toshiba X-Press) using 120 ml of IV contrast material injected at a rate of 4 ml/s. CT was repeated if there was suspicion of recurrence. In all patients, initial sonographic and CT findings were recorded and analyzed. The length of the 824 JR:189, October 2007

2 Sonography and CT of Hepatobiliary Fascioliasis spleen was measured, and 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. Regular follow-ups until the lesions faded were available for 64 patients. For longterm evaluation (beyond 1 year), the patients who were diagnosed in 2006 (n = 8) and those who were lost to follow-up (n = 12) were excluded. The mean follow-up period was 62 months. Results Initial Hepatic and Perihepatic Imaging Findings Liver lesions were detected in 78 patients (90%) (Table 1). In 12 patients the lesions could not be seen on sonography. On CT, nine patients did not have detectable liver lesions. Liver lesions, which did not show any contrast enhancement, were best seen on portal venous phase CT images. Liver lesions were multiple in 69 patients and solitary in nine. Typical liver lesions were multiple small (up to 2 3 cm in diameter), confluent, and subcapsular nodules with illdefined borders (Fig. 1). The lesions were hypoechoic (96%) on sonography and hypodense on CT, except in three patients (4%) in whom the lesions were hyperechoic or anechoic at a certain stage. Necrotic areas in the lesions were not rare, especially in bigger lesions. minimal amount of perihepatic or subcapsular fluid was seen in four patients (5%) on sonography and CT. Capsular enhancement was not observed in any patient on CT. In 44 patients (51%), periportal hilar lymph node enlargement was detected on sonography and CT (Fig. 1). The enlarged lymph nodes were usually multiple; their largest diameters were 7 38 mm. Initial iliary Tract Imaging Findings iliary tract changes were best seen on sonography. iliary abnormalities were detected in 39 patients (45%) (Table 1). Parasites were seen in the gallbladder lumen of 32 patients, nine of them showing free motility. They were leaf-shaped or snaillike echoes measuring 6 22 mm (Fig. 2). Eight patients showed parasites in the common bile duct (Fig. 3). Five patients had gallbladder wall thickening, 20 had dilatation (7 20 mm) and edema of the common bile duct, and six showed biliary wall enhancement on CT. Other Initial Imaging Findings Mild splenomegaly was detected in 19 patients (22%). Ectopic inflammation was observed in three patients. The ectopic sites were anterior abdominal muscles in two patients and the bowel wall in one. The bowel wall inflammation and infarction could not be documented radiologically but was confirmed after pathologic examination of the resected bowel. Improvement in Imaging Findings In 34 patients the lesions improved within 1 3 months; in 10 patients, in 3 6 months; and in five patients, in 6 12 months. Residual fibrotic or necrotic liver lesions, biliary abnormalities, or periportal lymph node en- TLE 1: Initial and Long-Term Imaging Findings of Hepatobiliary Fascioliasis Initial Findings in 87 Patients Long-Term Findings a in 67 Patients Finding No. of Patients % No. of Patients % Liver lesions present Multiple Solitary 9 10 iliary system changes Living parasites in gallbladder Edema and dilatation of CD Calcified parasites in gallbladder 2 3 Intrahepatic biliary dilatation Periportal lymphadenopathy b 3 Splenomegaly Subcapsular effusion 4 5 Ectopic inflammation 3 3 Few small dots of liver calcification 6 9 Note CD = common bile duct. a fter 1 year. b With liver lesions. Fig year-old man with typical liver nodules of fascioliasis., Multiple small subcapsular, confluent, ill-defined hypoechoic nodules (arrows) are seen on transverse sonogram. (Fig. 1 continues on next page) JR:189, October

3 Fig. 1 (continued) 45-year-old man with typical liver nodules of fascioliasis., Transverse (left) and oblique (right) sonograms show enlarged (2-cm) periportal lymph node (between calipers) and parenchymal hypoechoic nodules. indicates first caliper measurement. C, Portal venous phase CT scan shows hypodense, nonenhancing multiple confluent nodules (arrows). largements could still be seen on imaging after 1 year in 15 patients. The residual fibrotic. lesions were hypoechoic on sonography and hypodense on CT. The necrotic remnants were seen as cystic foci on sonography and as fluid density on CT. The biliary abnormalities that could be observed on sonography in the long term were echogenic particles in the gallbladder, wall thickening, and dilatation of the common bile duct Long-Term Imaging Findings In nine patients, fibrotic liver lesions could be detected after 1 year of treatment (Fig. 4 and Table 1). ges of the lesions ranged between 2 and 7 years (average, 4.3 years). Common bile duct dilatation and edema were prolonged in two patients. oth patients had symptoms, signs, and laboratory indications of recurrent cholangitis. One patient recovered after 2 years and the other after 7 years. Two patients had motile parasites in their gallbladder after 8 and 9 years, respectively (Fig. 5). oth patients were asymptomatic and their laboratory values were normal. Two patients had gallbladder echoes with partial acoustic shadowing that were interpreted as calcifying dead parasites because of their spheric or ellipsoid shapes (Fig. 5). Two patients had chronic liver disease; however, further examination revealed that their disease was due to coexisting hepatitis. In six patients, residual tiny dots of calcific foci were observed. No patient had remarkable curvilinear or spherical calcification. Discussion In recent years, human fascioliasis has been indicated to be an important public health problem by the World Health Organization. n extensive review has compiled thousands of cases, including 3,267 cases from merica and 2,951 cases from Europe in the past 25 years [1]. The incubation period of the disease is usually 1 month. There is a wide range of disease severity; although some patients may be asymptomatic or have mild symptoms, others may experience severe abdominal pain and distention, significant weight loss, high fever, and prostration [4, 6]. bdominal pain is due to the hepatic capsular irritation and subcapsular abscesses created by the parasites [7]. Eosinophilia and leukocytosis are present in this hepatic phase, and subcapsular nodules can be detected on both sonography and CT. The biliary phase, which occurs next, is characterized by cholangitic fevers and dyspepsia caused by partial biliary obstruction, which is best appreciated on sonography as echogenic floating particles in the biliary system and edema of the gallbladder and distal biliary ducts [4, 6, 8]. No biliary changes may be present if the patient is imaged early during the initial hepatic phase. Depending on the immunologic response of the patient and the number of parasites, the disease may never progress to the biliary phase. In many patients, hepatic and biliary lesions may overlap. Finally, in some patients, only biliary changes may be detected because the liver lesions may have healed [1, 2, 6]. Subcapsular effusions may be detected at the site where the parasite entered the liver [7]. During migration of parasites, multiple small confluent abscesses are formed; these can be detected as tracts or tunnels on imaging [6]. The abscesses are best seen on portal venous phase CT because they do not show contrast enhancement and therefore are better seen in the normal enhancing liver parenchyma [4, 8]. The liver lesions may be missed on sonography if it is not performed when the disease is in the acute stage or if it is performed when the lesions are few and slightly hypoechoic or isoechoic. Important imaging features in the differential diagnosis are multiplicity, ill-defined borders of confluent nodules, absence of a halo, and absence of contrast enhancement. If the lesions are solitary and largely necrotic, they may be confused with necrotic metastases and abscesses of other causes [3, 7, 9]. Periportal lymph node enlargement or lymphadenopathy is helpful in the diagnosis. lthough it was reported in 1979 by costa-ferreira et al. [3] in the surgical specimen of a patient with fascioliasis, the frequent radiologic detection of periportal lymphadenopathy in fascioliasis was first mentioned by Kabaalioglu et al. [4]. C 826 JR:189, October 2007

4 Sonography and CT of Hepatobiliary Fascioliasis Fig. 2 Sonogram shows 10-mm floating echo (arrow) with no acoustic shadowing in gallbladder of 75-year-old woman with fascioliasis. JR:189, October Fig. 3 Two patients with biliary involvement in fascioliasis., Typical double-layered walls of dilated common bile duct (CD, arrows) reflect biliary ductal edema in sonogram of 62-year-old woman., Multiple flukes and thickening of common bile duct wall (arrows) are shown on sonogram of 46-year-old woman with fascioliasis. C Fig. 4 Fibrotic lesions in long-term follow-up of two asymptomatic patients with fascioliasis., In 68-year-old woman, sonogram shows multiple hypoechoic nodules (arrows) in third year of follow-up. and C, In 69-year-old woman, portal venous phase CT scan () shows hypodense subcapsular nodules (arrow). Patient was asymptomatic and nodules were detected on fifth-year follow-up. Sonogram (C) shows appearance of subcapsular necrotic and solid nodules (arrows). Fig. 5 Long-term biliary findings in two asymptomatic patients., 61-year-old woman with motile parasites in gallbladder. Sonogram shows gallbladder walls are thickened and irregular. Patient was treated 8 years earlier., Sonogram in 67-year-old woman shows gallbladder echoes (arrow) have partial weak acoustic shadow. Patient was treated 9 years earlier when biliary parasites were seen in her common bile duct and gallbladder.

5 The parasite or multiple parasites may be seen in the common bile duct or gallbladder. They are leaflike or curvilinear snaillike echoes; their length varies from 5 to 25 mm. They are usually approximately 1 cm long because most of them are juvenile [2, 5, 10]. They may be vital, and their movements can be observed on sonography. When dead, they may lose their leaflike shape. However, they can easily be differentiated from stones and sludge because they do not cause acoustic shadowing and do not form a layer. If the parasites are attached to the gallbladder wall, they may be confused with polyps. Color Doppler sonography may help in the differential diagnosis. iliary involvement in fascioliasis usually manifests as cholangitis. Thickening of the gallbladder wall or the common bile duct and mild intrahepatic biliary ductal dilatation are not infrequent [2, 5, 10]. Total biliary obstruction is rare and was seen in only one patient in our series. In this case, multiple parasites had formed a conglomerate mass in the distal common bile duct, and the patient was treated by urgent surgical extraction of the parasites. In hyperendemic regions, heavy infestations and biliary obstructions are much more common [11]. Usually, the parasitic secretions cause biliary epithelial hyperplasia, which is best observed on sonography as edema of the biliary ductal walls [3]. Enhancement of biliary ductal walls can also be observed on CT, but, as in our series, the detection rate of biliary ductal thickening is less than with sonography. lthough we have seen biliary abnormalities in nearly half of our patients, the ratio may be lower or higher depending on the endemicity of the region and the frequency of sonography follow-up [6, 10]. Splenomegaly may be observed in a number of patients; it is usually mild and transient, a nonspecific sign that is seen in the acute phase of fascioliasis [3, 5, 10]. Ectopic inflammation in extrahepatic locations has been reported in the literature; it was radiologically detected in two patients in this series as inflammation and enlargement of anterior abdominal wall muscles. In this study, hepatobiliary abnormalities were seen in nearly half the patients after 3 months of treatment and after laboratory values had returned to normal. This finding is consistent with previous reports [5, 6, 8, 10]. Even after 1 year, some patients had hypoechoic and hypodense nodules in the liver, although they were reduced in number and size. These nodules may mimic reactivation of fascioliasis or liver malignancies, but animal studies and human pathology reports have shown that these nodules reflect necrotic granulomas and fibrosis of the affected liver tissue [3, 9]. Shrinkage of the enlarged periportal lymph nodes may also take months or even years; in two patients in our series, the enlarged nodes disappeared after 2 and 3 years, respectively. In the long term, two patients had symptoms and laboratory signs of recurrent cholangitis as well as sonographic evidence of biliary ductal edema and dilatation. Prolonged cholangitis due to fascioliasis is well documented in sheep and cattle, but in humans it has become rare because of advanced diagnostic methods and effective treatment [9]. Two asymptomatic patients in our series were found to carry vital parasites in their gallbladders 7 and 8 years after treatment. nother two patients had dead parasites in their gallbladder that created partial acoustic shadowing that was not present earlier. Similar to our observation, Richter et al. [10], in a sonographic follow-up study of fascioliasis, showed partial calcification of the contents of the biliary system. Dead parasites may be expelled to the intestine or stay in the gallbladder to act as a nidus for cholelithiasis, as has been experimentally proven in animals [3, 12]. Cirrhosis due to fascioliasis has been reported in long-standing heavy infestations of cattle and sheep; however, to our knowledge, it has not been proven in humans. mong our cases, two patients had cirrhosis, but those were found to be coincidence only. lthough long-term systematic observations of large human series are not available, it is usually agreed that fascioliasis does not increase the risk of cholangiocarcinoma or other liver malignancies [1, 3]. In our series we did not observe any malignancy. Parenchymal calcifications were observed in six cases. On imaging they appeared as a few scattered tiny dots, never curvilinear or extensive. In humans parenchymal and biliary ductal calcifications seem to be rare, whereas in animals they are more frequent. In conclusion, several imaging findings in hepatobiliary fascioliasis are helpful in the early diagnosis of the disease. Fibrotic liver tissues after necrosis may be imaged as hypoechoic or hypodense nodules for years after the infestation. In a few patients, recurrent cholangitis, gallstones, or asymptomatic viability of the flukes may be observed in the long term. No cirrhosis or malignancy was documented during our follow-up. References 1. Mas-Coma S, argues MD, Valero M. Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol 2005; 35: Ooms HW, Puylaert JCM, van der Werf SDJ. iliary fascioliasis: US and endoscopic retrograde cholangiopancreatography findings. Eur Radiol 1995; 5: costa-ferreira W, Vercelli-Retta J, Falconi LM. Fasciola hepatica human infection: histopathological study of sixteen cases. rch Pathol nat Histol 1979; 383: Kabaalioglu, Cubuk M, Senol U, et al. Fascioliasis: US, CT, and MRI findings with new observations. bdom Imaging 2000; 25: Kabaalioglu, paydin, Sindel T, Luleci E. USguided gallbladder aspiration: a new diagnostic method for biliary fascioliasis. 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