Imaging Findings of Liver Clonorchiasis
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1 J Radiol Sci 2011; 36: Imaging Findings of Liver Clonorchiasis I-Hao Su Sung-Yu Chu Chien-Ming Chen Kuang-Tse Pan Ming-Yi Hsu Ren-Fu Shi Jeng-Hwei Tseng Kee-Min Yeow Chien-Fu Hung Department of Medical Imaging and Intervention, Chang Gung Memorial Hospital at Linkou, Chang Gung University College of Medicine, Taoyuan, Taiwan ABSTRACT The objective of this study was to analyze the hepatic imaging findings concerning clinical data on clonorchiasis. From August 1994 to September 2009, 13 patients were diagnosed with hepatic clonorchiasis by identification of adult flukes in the biliary tract through biliary drainage and/or surgery at a single institution. We analyzed their medical records and imaging findings by cholangiography and computed tomography (CT). The 13 enrolled patients were all men ranging in age from 44 to 80 years (mean ± standard deviation, 62.1 ± 10.0 years). The most common admission diagnosis was biliary tract infection (84.6%). Cholangitis and cholecystitis were the two most common biliary diseases of the enrolled patients (92.3%), followed by biliary lithiasis (46.2%). Five hepatopancreatobiliary tumors were detected, including three cholangiocarcinomas, one pancreatic head cancer, and one hepatocellular carcinoma. The patient who had pancreatic head cancer also had swollen duodenal papilla, chronic inflammation of the ampulla of Vater, and pancreatitis. Diffuse, pipelike, mild dilatation of peripheral intrahepatic ducts up to the subcapsular region of the liver was the most common finding on cholangiography and CT (76.9%), followed by uniform, leaflike, filamentous, tiny intraductal filling defects (69.2% on cholangiography and 61.5% on CT) and biliary lithiasis (46.2% on cholangiography and 38.5% on CT). The diagnosis of clonorchiasis is often delayed, and it is usually identified incidentally by biliary drainage or surgery in symptomatic patients with high parasite burdens. The characteristic imaging findings with a history of raw freshwater fish consumption and the presence of hepatobiliary symptoms can help the physician to suspect or diagnose clonorchiasis. INTRODUCTION Clonorchis sinensis, the most common human liver fluke in East Asia, is actively transmitted in endemic areas of Korea, China, Russia, Taiwan, and Vietnam [1]. Prior reports have shown three important endemic areas of clonorchiasis in Taiwan: Miaoli in the north, Sun-moon Lake in central Taiwan, and Mei-Nung in the south [2]. Because of increased immigration and traveling, and the dietary habit of eating raw freshwater fish in some endemic areas, clonorchiasis in Taiwan still cannot be completely eradicated despite a marked decrease in epidemic prevalence [3]. Misdiagnosis or underdiagnosis of clonorchiasis may be made due to patients coming from non-endemic areas, asymptomatic patients, nonspecific symptoms of gastrointestinal or hepatobiliary problems, or negligence by Correspondence Author to: Chien-Fu Hung Department of Medical Imaging and Intervention, Chang Gung Memorial Hospital at Linkou, Chang Gung University College of Medicine, Taoyuan, Taiwan No. 5, Fu-Hsing Street, Kuei-Shan, Taoyuan 333, Taiwan 145
2 inexperienced doctors. The diagnosis is often delayed and made incidentally by biliary drainage or surgery. As medical imaging has become a major tool to aid in the diagnosis of disease, and imaging findings of clonorchiasis are relatively characteristic and easily recognized if radiologists suspect the disease, we undertook a retrospective study to discuss hepatic imaging findings regarding clinical data. MATERIALS AND METHODS Patient enrollment Between August 1994 and September 2009, 18 patients were diagnosed with hepatic clonorchiasis by identification of adult flukes in the biliary tract using endoscopic retrograde cholangiopancreatography (ERCP) and/or percutaneous transhepatic cholangiography and drainage (PTCD) or surgery at a single institution. Of these 18 patients, five were not enrolled owing to loss of cholangiography or computed tomography (CT) images. Contrast-injected cholangiography and CT scan The cholangiography of enrolled patients included PTCD (2 in 13 patients) and ERCP (11 in 13 patients) using manually injected iodinated contrast media. CT of the abdomen was scanned contiguously using a 10-mm interval/thickness and by performing a pre-/post-contrast study from the dome of the diaphragm to the iliac crest using intravenous iodinated contrast media. Leaflike filling defects in the biliary tree on cholangiography and CT were defined as adult flukes of variable length. Filling defects with uneven sizes and shapes on cholangiography and CT were defined as biliary stones. Data collection All data were collected from medical records and radiological reports and included data regarding gender, age, admission diagnosis, imaging findings, intervention surgical history, and other hepatopancreatobiliary disease. Diagnosis of hepatopancreatobiliary tumors was made by surgical or biopsy pathology. Other hepatopancreatobiliary diseases were diagnosed by pathology or imaging findings. All images were reviewed and a consensus was reached from interpretation by two attending radiologists with 6 and 27 years of experience, respectively, with cholangiography and CT. RESULTS The clinical features of enrolled patients with C. sinensis are shown in Table 1. The 13 enrolled patients were men ranging in age from 44 to 80 years [mean ± standard deviation (SD), 62.1 ± 10.0 years]. One patient was admitted with sigmoid colon cancer and one with esophageal cancer, who both subsequently received ERCP for evaluation of nonspecific right upper quadrant dull abdominal pain and biliary tree dilatation that was noted on CT for tumor staging. Eleven patients had an admission diagnosis of biliary tract infection, and 10 of those had obstructive jaundice. Cholangitis and cholecystitis were the two most common biliary diseases of the enrolled patients (92.3%), followed by biliary lithiasis (46.2%). Concerning biliary lithiasis, two had gallstones only; two had stones in the intrahepatic ducts, common bile duct, and gallbladder; one had stones in the intrahepatic ducts and common bile duct; and one had stones in the gallbladder and cystic duct that resulted in Mirizzi s syndrome. Two patients had unusual disseminated microabscesses with multiple uneven-sized small intrahepatic collections on cholangiography and innumerable small hypodense areas on CT. Five tumors were detected in the hepatopancreatobiliary system, including three cholangiocarcinomas, one pancreatic head cancer, and one hepatocellular carcinoma. The patient who had pancreatic head cancer also had swollen duodenal papilla, chronic inflammation of the ampulla of Vater, and pancreatitis. The imaging findings of the hepatopancreatobiliary system of these patients are shown in Table 2. The presence Table 1. Clinical Features in Enrolled Patients with Clonorchis sinensis Characteristics Age (years) ± 10.0 Sex (male: female) 13:0 Admission diagnosis Biliary tract infection 11 (84.6%) Jaundice 10 (76.9%) Others (sigmoid colon cancer, esophageal cancer) Other final diagnosis of hepatopancreatobiliary system 2 (15.4%) Cholangitis 12 (92.3%) Disseminated microabscesses 2 (15.4%) Cholecystitis 12 (92.3%) Adenomyomatosis 3 (23.1%) Liver cirrhosis 4 (30.8%) Biliary lithiasis 6 (46.2%) Cholangiocarcinoma 3 (23.1%) Hepatocellular carcinoma 1 (7.7%) Pancreatic head cancer with chronic inflammation 1 (7.7%) of ampulla of Vater and pancreatitis Abbreviations: 1 Date are the means ± standard deviation, data in the parentheses are the percentages. 146
3 of diffuse, pipelike, mild dilatation of intrahepatic ducts on cholangiography, and diffuse, uniform, mild dilatation of peripheral intrahepatic ducts up to the subcapsular region of the liver on CT were the most common findings (76.9%), followed by uniform, leaflike, filamentous, tiny intraductal filling defects (69.2% on cholangiography and 61.5% on CT) and then biliary lithiasis (46.2% on cholangiography and 38.5% on CT). DISCUSSION Clonorchiasis, a food-borne helminthiasis, is caused by C. sinensis, which is transmitted via some species of snails and freshwater fish, the first and second intermediate hosts, respectively, and then to fish-eating mammals serving as reservoir hosts [1, 4]. In cases reported in non-endemic areas, the infection is found in Asian immigrants through ingestion of imported raw, undercooked, or improperly stored dried, smoked, or pickled freshwater fish containing metacercariae [1, 4]. In the present study, all patients were adult men who had a history of eating raw or undercooked freshwater fish. Many other reports have also shown higher infection rates in adult males and people who had a dietary habit of raw and undercooked freshwater fish consumption [2, 3, 5]. The prevalence of symptoms is related to the number of flukes, frequency of infection, and immunity of the host. Most patients with clonorchiasis are asymptomatic and others have nonspecific symptoms such as epigastric or right upper abdominal pain, general malaise, anorexia, nausea, fever, or diarrhea. Some severe cases may have obstructive jaundice, pyogenic cholangitis, or liver cirrhosis [1, 5]. Symptomatic infection is most common in older adults due to the longevity of C. sinensis, large worm burden, and intensity of cumulative infection [6]. In the present study, most patients were admitted with a diagnosis of biliary tract infection and obstructive jaundice. The cause may have been severe infection with numerous C. sinensis where the flukes were found incidentally by biliary drainage or surgery. In areas of endemic infection, more clonorchiasis cases are now diagnosed incidentally during radiological examinations such as cholangiography, ultrasonography, and CT. Radiological findings are regarded as pathognomonic for clonorchiasis because they reflect the unique pathological changes of this disorder [7-15]. Sonographic findings of clonorchiasis include diffusely dilated intrahepatic ducts, bile duct wall thickening, and non-shadowing echogenic foci within the bile ducts and floating in the gallbladder [5, 7, 8, 10, 13, 15, 16]. These findings have low sensitivity and low specificity because of variable worm burden and persistent residual pathology after cure [17], but increased periductal echogenicity and floating echogenic foci in the gallbladder indicate heavy infection of active clonorchiasis [18]. The major imaging findings of hepatic C. sinensis on cholangiography are diffuse, mild dilatation of the intrahepatic bile ducts without obvious dilatation of the extrahepatic biliary tree, and leaflike or filamentous small filling defects within the peripheral intrahepatic ducts (Fig. 1) [3, 7, 8, 10, 13]. The most common CT findings of clonorchiasis are essentially the same as those observed by cholangiography: i.e., diffuse, uniform dilatation of the peripheral intrahepatic bile ducts without obvious dilatation of the extrahepatic biliary tree or a focal obstructing lesion. Adult flukes in the biliary tree of severely infected patients can also be demonstrated on CT as small, intraluminal, leaflike elliptic filling defects, measuring from several millimeters to 10 mm in length (Fig. 2) [3, 7, 8, 10-14, 19, 20]. Similar Table 2. Imaging findings in Enrolled Patients with Clonorchis sinensis Imaging findings Cholangiography Computed tomography Pipelike dilatation of peripheral IHD diffusely 10 (76.9%) 10 (76.9%) Mildly dilated EHD 4 (30.8%) 4 (30.8%) Biliary obstruction 3 (23.1%) 3 (23.1%) Leaflike, filamentous, tiny filling defect in biliary tree 9 (69.2%) 8 (61.5%) Filling defect with uneven size and shape / Biliary lithiasis 6 (46.2%) 5 (38.5%) Multiple uneven-sized small intrahepatic collections / Microabscesses 2 (15.4%) 2 (15.4%) Liver cysts 2 (15.4%) Diffuse calcified spots 1 (7.7%) Tumors 4 (30.8%) 5 (38.5%) Abbreviations: IHD: intrahepatic duct; EHD: extrahepatic duct. Data are expressed in patient number and (percentages). 147
4 Figure 1 1a 1b 1c Figure 1. a-c: Endoscopic retrograde cholangiography of clonorchiasis in (a) a 60-year-old male, (b) an 80-yearold male, and (c) a 68-year-old male. Note the diffuse, uniform, mild dilatation of intrahepatic bile ducts with leaflike, filamentous, tiny filling defects in the biliary tracts, which correspond to the flukes (arrowheads). Fig. 1c shows an 18-mm stone in the cystic duct resulting in Mirizzi's syndrome (*). to previous studies, we found the presence of diffuse, pipelike dilatation of intrahepatic ducts up to the subcapsular region of the liver, and some of them had club-like blunt tips. This may be related to the migrating tendency and occupancy of these flukes in the peripheral small bile ducts with chronic inflammation that result in bile duct dilatation, mechanical obstruction, and bile duct wall thickening [13, 20]. Contrast-enhanced duct wall thickening is believed to reflect prominent periductal inflammation and fibrosis; however, Choi et al. found it difficult to see on CT [11]. Lee et al. revealed periductal arterial proliferation and hepatic sinusoidal congestion during the acute phase of clonorchiasis that may result in CT findings with dilatation of the peripheral intrahepatic bile ducts and their club-like blunt tips, tubular contrast-enhanced duct walls, and transient hepatic attenuation differences. They also considered 148
5 Figure 2 2a 2b 2c 2d Figure 2. a-d: Computed tomography of clonorchiasis in (a) a 56-year-old male, (b) a 58-year-old male, (c) a 63-year-old male and (d) a 73-year-old male. a. Note the numerous leaflike, elliptical, tiny hyperdensities (arrowheads), which correspond to the flukes, within the diffuse, mild dilatation of intrahepatic bile ducts. b. Note the numerous leaflike, filamentous, tiny hyperdensities (arrowheads), assumed to be the flukes, within the dilated intrahepatic ducts and suspected microabscesses. c. Leaflike, elliptical hyperdensities (box), resembling flukes, are observed within the dilated intrahepatic ducts. Note the dilated intrahepatic ducts expand entirely with a pipelike appearance and up to the subcapsular region of the liver, and some of them have club-like blunt tips. The cholongiocarcinoma in S7 of the liver, subsequently proved by biopsy, is also demonstrated (T). d. Note the diffuse and uniform dilatation of the peripheral intrahepatic bile ducts with some tiny leaflike intraductal hyperdensities (arrowheads). The heterogeneous-enhanced lobulated mass (T) in S7 of the liver was subsequently diagnosed as hepatocellular carcinoma. that severe disease activity and dynamic CT usage may contribute to discovery of these CT findings [20]. Cholelithiasis, cholangitis, cholecystitis, biliary tract obstruction, pyogenic hepatic abscess, pancreatitis, and cholangiocarcinoma are reported to be long-term complications of clonorchiasis [8, 10, 21]. These complications may result from chronic irritation and damage to biliary epithelial cells, leading to hyperplasia, metaplasia, and fibrosis [1, 4, 10, 20]. Our study showed several other diseases of the hepatopancreatobiliary system, of which cholangitis and cholecystitis occurred in most patients. Additionally, Chan et al. found cholangitis to be the most common representation of clonorchiasis [3]. Dead helminthes, which can serve as a nidus of stone and chronic parasitic biliary infection, 149
6 can also lead to lithiasis. A significant correlation between biliary stones and evidence of clonorchiasis, including a history of the disease, was shown by Choi et al. [16]. Only one patient had diffuse punctate calcifications in our study. Lee et al. found dot-like hepatic calcifications in cured clonorchiasis that may be dystrophic calcifications of the proliferating ductal epithelium [20]. Secondary hepatic disseminated microabscesses caused by clonorchiasis were observed in the present study, which are unusual and have not been reported previously. Jang et al. and Choi et al. presented a few cases of unusual hepatic parasitic macroabscesses with clonorchiasis [11, 22]. Many studies have documented high incidences of concurrent cholangiocarcinoma and clonorchiasis [1, 4, 8, 9, 11, 19, 23]. Additionally, duodenal papillitis [24], carcinoma of the ampulla of Vater [11], and pancreatitis [21] associated with clonorchiasis have also been reported. We surmise that this may be related to the life cycle of C. sinensis: ingested metacercariae excyst in the duodenum and then pass through the ampulla of Vater, causing chronic irritation to the bile ducts. However, in the report by Kim et al., clonorchiasis did not correlate with choledocholithiasis, cholecystolithiasis, cholangitis, hepatocellular carcinoma, or biliary pancreatitis [23]. The actual etiology is unknown and requires further study. Differential diagnoses of clonorchiasis on CT include intraductal papillary mucinous biliary neoplasm, cholangiocarcinoma, hepatocholedocholithiasis, recurrent pyogenic cholangitis, primary sclerosing cholangitis, and Caroli s disease [10, 11]. Intraductal papillary mucinous biliary neoplasm typically manifests as diffuse or segmental dilatation with or without a visible mass or stenosis. Cholangiocarcinoma usually shows nodular masses or segmental stenoses of the bile ducts with proximal dilatation. Hepatocholedocholithiasis typically represents uneven-sized intraluminal filling defects with or without biliary obstruction. Recurrent pyogenic cholangitis typically shows segmental stenosis with abrupt tapering of the peripheral hepatic ducts, along with dilatation of the extrahepatic bile duct and stones. Primary sclerosing cholangitis typically manifests skip stenosis and pruning of the irregularly dilated intrahepatic bile ducts with thickening of duct wall. Caroli s disease is characterized by saccular dilatation of the intrahepatic bile ducts with the central dot sign. However, the characteristic CT findings of clonorchiasis, which appear as uniform, pipelike, mild dilatation of the intrahepatic ducts up to the subcapsular region of the liver, are quite different from those of other bile duct diseases. Clonorchiasis is commonly diagnosed incidentally by routine radiological study, biliary drainage, or surgery. Every physician, whether in endemic or non-endemic areas, should be familiar with and aware of its radiological findings. The characteristic imaging findings with a history of raw freshwater fish consumption and the presence of hepatobiliary symptoms can help physicians to suspect or diagnose clonorchiasis. REFERENCES 1. Hong ST, Fang Y. Clonorchis sinensis and clonorchiasis, an update. Parasitol Int 2011; doi: /j. parint Chen ER. Clonorchiasis in Taiwan. Southeast Asian J Trop Med Public Health 1991; 22: Chan HH, Lai KH, Lo GH, et al. The clinical and cholangiographic picture of hepatic clonorchiasis. J Clin Gastroenterol 2002; 34: Rim HJ. Clonorchiasis: an update. J Helminthol 2005; 79: Wang KX, Zhang RB, Cui YB, Tian Y, Cai R, Li CP. Clinical and epidemiological features of patients with clonorchiasis. World J Gastroenterol 2004; 10: Liu LX, Harinasuta KT. Liver and intestinal flukes. Gastroenterol Clin North Am 1996; 25: Choi D, Hong ST. Imaging diagnosis of clonorchiasis. 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