Abstract
Although few case reports of human fascioliasis have been reported from different parts of India, there is no case reported from the Kashmir valley to date. Herein we report two cases of human fascioliasis. Both patients presented with fever, marked eosinophilia, and liver lesions on imaging. Hepatobiliary imaging showed vague features like mild biliary dilatation and liver lesions representing burrows. A liver biopsy in one of the patients revealed eosinophilic granuloma. Both patients were diagnosed definitively with endoscopic retrograde cholangiopancreatography (ERCP) by demonstrating live adult fasciola worms. Any patient presenting with fever, marked eosinophilia, and liver lesions on imaging should be evaluated for fascioliasis.
Keywords: fasciola, eosinophilia, ERCP
Abbreviations: ERCP, Endoscopic retrograde cholangiopancreatography; MRCP, Magnetic resonance cholangiopancreatography; CT, Computed Tomography; LFT, Liver function test
Human fascioliasis is a water and food-borne zoonosis. In humans, it is characterized by fever, eosinophilia, and abdominal pain, with many, however, being asymptomatic.1 Fascioliasis is distributed worldwide, being more common in geographic areas, where the rearing of cattle is extensive. This disease is infrequently reported from India in the form of case reports, and most of the time being a surprise diagnosis.2 It is caused by two parasites of class Trematoda, genus Fasciola and species, Fasciola hepatica and Fasciola gigantica.3 Sheep and cattle are the usual definitive hosts; however, humans are incidental hosts. Humans are infected by consuming contaminated water or food like watercress.4 We report the first two cases of fascioliasis from Kashmir valley. In the first case it was a surprise diagnosis, while the second case diagnosis was anticipated.
Case 1
A 32-year-old male from rural background presented with complaints of fever and mild pain in right upper abdomen of 3 months duration. Patient was referred to our department as a case of secondaries liver in view of long standing fever and hypodense liver lesions on abdominal Computed Tomography (CT). Clinical examination was unremarkable except for mild hepatomegaly. Haemogram showed haemoglobin 11.5 g/dl; white cell count, 21,000 cells/mm3 (71% eosinophils) and platelets, 4.5 lacs/mm3. Liver function tests revealed bilirubin, 0.8 mg/dl; alanine aminotransferase, 70IU/L; aspartate aminotransferase 65 IU/L and alkaline phosphatase, 319 IU/L (30–145). Mantoux, Widal, and Brucella serology was negative. Multiple blood cultures were reported sterile. Bone marrow examination revealed increased eosinophils and eosinophilic precursors. Chest X-ray and echocardiography were normal. Ultrasonography showed mild central biliary dilatation and small periportal lymph nodes. The patient was treated with antipyretics and antibiotics but patient continued to be febrile. CT scan of abdomen already done in the previous hospital showed multiple subcapsular hypodense lesions in both lobes of the liver with central biliary dilatation (Figure 1a). A percutaneous liver biopsy was done, which was reported as an eosinophilic abscess (Figure 1b). Magnetic resonance cholangiopancreatography (MRCP) revealed dilated common bile duct and vague signal void debris inside the common bile duct (CBD). ERCP was done with a provisional diagnosis of biliary ascariasis, a common biliary disease in our geographic region but surprisingly revealed multiple live leaf-like Fasciola hepatica worms that lead to the final diagnosis (Figure 1c). Bile microscopy showed operculated eggs of fasciola hepatica (Figure 1d). The patient was treated with a single oral dose of triclabendazole 10 mg/kg. On follow-up after 2 months, the patient was afebrile, and eosinophilia settled, and liver imaging (CT) was normal. The family was screened by stool examination for ova but all household were negative.
Figure 1.
(a)CT abdomen showing multiple subcapsular hypodense lesions in the liver,(b) Percutaneous liver biopsy showing eosinophilic granuloma. (c) Duodenoscope view of D2 showing F. Hepatica. (d) Microscopy of bile showing operculated eggs.
Case 2
A 20-year-old female came to our hospital with history of fever 3 months back, which had lasted for five to 6 weeks. She was evaluated in many hospitals. Investigations included baseline investigations, imaging, serology, bone marrow, and liver biopsy. Fever subsequently settled, but liver function tests showed a three-fold rise in alkaline phosphatase and persistent marked eosinophilia (50%) and abdominal pain. On reviewing old records, we saw multiple hypodense liver lesions on abdominal CT (Figure 2a) and marked eosinophilia in haemogram (54% of total leukocyte count). A liver biopsy done earlier showed necrotizing inflammation with ill-defined granulomas and increased eosinophils. Taking lessons from the previous case, we were almost confident that we were dealing with a case of fascioliasis. Ultrasonography revealed mild biliary tract dilatation and thickened wall of the bile duct; however, liver lesions had vanished by now (2b). MRCP revealed central biliary tract dilatation with some debris (2c). ERCP was done, which showed multiple live Fasciola worms. The worms this time were identified by microbiologists as Fasciola gigantica (2d). The patient was treated with a single oral dose of triclabendazole 10 mg/kg. On follow up the LFT and eosinophilia normalized. Repeat imaging (MRI/CT) showed clearance of liver lesions (3a,b) (Figure 3).
Figure 2.
(a) CT abdomen showing extensive hypodense lesions in the liver. (b) USG abdomen showing mildly dilated bile duct and thickened walls. (c) MRCP revealing mild biliary tract dilatation with signal voids inside. (d) Photograph of Fasciola worm removed by ERCP.
Figure 3.
Follow up imaging of case 2 showing clearance of liver lesions on follow up CT and MRI abdomen.
Discussion
Fascioliasis is a zoonotic disease caused by Fasciola hepatica and Fasciola gigantica. Although the disease is distributed worldwide, it is more prevalent in countries associated with extensive livestock rearing. Fasciola life cycle usually runs between livestock (cattle and sheep) that act as definitive host and snail that acts as the intermediate host. Humans become incidental hosts by consuming contaminated water and food like watercress, etc. Fasciola infection needs close association and the presence of both definitive and intermediate hosts.5,6
Sharma et al. reported seven different aquatic snails from Kashmir, Lymnae auricularia sensu stricta being most common. It was also demonstrated that Lymnae auricularia sensu stricta can support the development of Fasciola gigantica under laboratory conditions.7 Many studies reported a high prevalence of fascioliasis in livestock (cattle 85%, sheep 51%, goats15%) in Kashmir, Fasciola gigantica being more common.8, 9, 10
By keeping in view the disease prevalence in animals and the presence of snail, it is surprising that no human cases were reported from Jammu and Kashmir to date, possibly a missed diagnosis. Fascioliasis has been reported from other states of India but mostly being a surprise diagnosis.2
Diagnosis of fascioliasis may be delayed because of the wide spectrum of the differential diagnosis and the low incidence of Fasciola hepatica infection. A high index of suspicion and specific radiological findings are very helpful in the diagnosis, especially in nonendemic places. Both of our patients had a fever, hypereosinophilia, and liver hypodensities on CT imaging of the liver. Magnetic resonance cholangiopancreatography (MRCP) showed nonspecific mild biliary dilatation with some signal voids inside the common bile duct.6
A serological test, indirect hemagglutination test (IHA) using purified adult Fasciola hepatica antigen F1 has a specificity of 96.9% for Fasciola hepatica infection.11 These serological tests are not routinely available in our country, and our patients were not tested serologically. However, for the confirmation of diagnosis, demonstrating live parasites or eggs in the bile or feces are required.1,3 In both our cases diagnosis was confirmed by retrieving live worms of Fasciola on ERCP and demonstrating eggs in bile.
We report two cases of fascioliasis, one of Fasciola hepatica and the other of Fasciola gigantic, within a span of 6 months time. The first case was challenging as we were not aware of the presence of fascioliasis in the Kashmir valley. However, the second case was diagnosed with ease in view of our experience of the first case in the form of clinical presentation, laboratory investigations, and imaging findings.
The drug of choice for fascioliasis is triclabendazole (10 mg/kg).12 This drug is not available for human use in India. Nitazoxanide, bithionol, metronidazole have also been found effective.
CRediT authorship contribution statement
Ghulam N. Yattoo: Conceptualization, Methodology. Kowsar Jan: Data collection, compilation, , Writing - original draft. Jaswinder S. Sodhi: Data collection, compilation, Methodology, Writing - original draft, Writing - original draft, Data collection. Zubaida Rasool: Data collection. Saurabh Kaushik: Writing - original draft, Data collection. Suresh Gorka: Writing - original draft, Data collection.
Conflicts of interest
The authors have none to declare.
Funding
None.
References
- 1.Mas-Coma S., Valero M.A., Bargues M.D. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol. 2009;69 doi: 10.1016/S0065-308X(09)69002-3. 41-14. [DOI] [PubMed] [Google Scholar]
- 2.Ramachandran J., Ajjampur S., Chandramohan A., Varghese G.M. Cases of human fascioliasis in India: tip of the iceberg. J Postgrad Med. 2012;58:150–152. doi: 10.4103/0022-3859.97180. [DOI] [PubMed] [Google Scholar]
- 3.Soliman M.F. Epidemiological review of human and animal fascioliasis in Egypt. J Infect Dev Ctries. 2008;2:182–189. doi: 10.3855/jidc.260. [DOI] [PubMed] [Google Scholar]
- 4.Keiser J., Utzinger J. Emerging foodborne trematodiasis. Emerg Infect Dis. 2005;11:1507–1514. doi: 10.3201/eid1110.050614. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Mas-Coma M.S., Esteban J.G., Bargues M.D. Epidemiology of human fascioliasis: a review and proposed new classification. Bull World Health Organ. 1999;77:340–346. [PMC free article] [PubMed] [Google Scholar]
- 6.Lim J.H., Mairiang E., Ahn G.H. Biliary parasitic diseases including clonorchiasis, opisthorchiasis and fascioliasis. Abdom Imag. 2007;33:157–165. doi: 10.1007/s00261-007-9326-x. [DOI] [PubMed] [Google Scholar]
- 7.Sharma R.L., Dhar D.N., Raina O.K. Br Vet J. 1989;145:57–61. doi: 10.1016/0007-1935(89)90010-9. Jan-Feb. [DOI] [PubMed] [Google Scholar]
- 8.Gul N., Tak H., Fazilli K.M., Abdullah I., Sofi T.A. Prevalence of fasciola infection in slaughtered animals in Kashmir. Int J Veterin ci Animal Husbandry. 2016;1:30–36. [Google Scholar]
- 9.Fatima M., Chishti M.Z., Ahmad F., Lone B.A. Epidemiological study of fasciolosis in cattle of Kashmir valley. Adv Biol Res. 2012;3:106–109. [Google Scholar]
- 10.Iram A., Tak H., Ganie S.A. Prevalence of fasciolosis and dicroceliosis in sheep slaughtered in Kashmir valley. Int J Scientif Technol Res. 2020;9:2020. [Google Scholar]
- 11.Azab M el-S, el Zayat E.A. Evaluation of purified antigens in haemagglutination test (IHA) for determination of cross reactivities in diagnosis of fascioliasis and schistosomiasis. J Egypt Soc Parasitol. 1996;26:677–685. [PubMed] [Google Scholar]
- 12.López-Vélez R., Domínguez-Castellano A., Garrón C., et al. Successful treatment of human fascioliasis with triclabendazole. Eur J Clin Microbiol Infect Dis. 1999;18:525–526. doi: 10.1007/s100960050338. [DOI] [PubMed] [Google Scholar]