Fascioliasis associated with chronic cholecystitis in a woman from Sistan and Baluchestan province, a non-endemic region in Southeastern Iran

Fascioliasis is common in many parts of the world, particularly in areas where traditional livestock husbandry is a common practice. In recent years the number of human fascioliasis has increased drastically with the estimates ranging from 2.4 million to 17 million people infected [11]. Fascioliasis is endemic in many countries in Asia including Iran, Pakistan, and Afghanistan. According to 41 studies in 13 Asian countries during 2000–2015, fascioliasis among cattle has been estimated at 0.7–69.2% followed by buffaloes (2.1–68.0%), sheep (0.4–31.4%), and goats (0.0–47.0%) [12]. Sistan and Baluchestan province in southeastern Iran is neighbor to Pakistan and Afghanistan. In Pakistan, fascioliasis is mainly caused by F. gigantica as the predominant Fasciola species, and the overall prevalence in humans and livestock in the region was reported as 0.3% and 20.1%, respectively [12, 13]. Animal fascioliasis in Sistan and Baluchestsn has been investigated from 2008 to 2016. A Survey in four slaughterhouses in Sistan and Baluchestan province showed 3.1% of cattle livers were condemned due to Fasciola infections [14]. Lymnaeid freshwater snails, known as the intermediate hosts of Fasciola species have been found throughout Sistan and Baluchestan province [15], however no study has been performed to determine the extent of the snails infection with the larval stages of Fasciola.

Fascioliasis comprises two main stages: acute or liver phase occurs for about eight weeks when immature juvenile worm migrate from the small intestine to the liver and sometimes other organs through the abdominal cavity. At this stage, the excretory-secretory products synthesized by the fluke are responsible for abdominal pain, anemia, urticaria, diarrhea, and hyper-eosinophilia. The chronic or biliary phase begins following the acute phase during which the juveniles develop into the adult worms and release eggs. [16, 17].

In the present study, we report a human case of fascioliasis in a non-endemic region with a hot and dry climate in Southeastern Iran. This is a significant finding because the patient reports no history of traveling to endemic regions. Our knowledge of the epidemiology and transmission of fascioliasis in Iran, out of the well-known foci of the disease in the north is poor. The transmission of the disease in the north of the country follows the pattern named “Caspian pattern” with a relatively high number of human and animal cases per year with an average annual temperature and humidity of about 13.2–19.2°C and 76–88%, respectively [18]. Most human cases have been limited to the northern province of Gilan, however recently an endemic focus of fascioliasis has been reported from Kohgiluyeh and Boyer Ahmad in the southwest of Iran [19, 20]. The patient of the present report lives in a hot and dry region in southeast Iran. Another case of fascioliasis was reported from this region in 2013 in a 61-year-old man with chronic cholecystitis. During the surgery, one adult Fasciola worm was found in his gall bladder, however no molecular investigation was performed to identify the helminth at the species level. The patient reported consuming fresh vegetables and no history of travel to the endemic regions of fascioliasis in Iran [21]. Findings of a serological survey in Sistan and Baluchestan province indicated the presence of anti-Fasciola antibody in 2.4% of the subjects [22]. Our report is the second report from this region. In the north of the country, human consumption of wild vegetables such as ‘‘Chuchagh’’, ‘‘Bineh’’ and ‘‘Khalvash’’ is common, however the present patient is from an arid area with low rainfall and a dry climate. Moreover, wild vegetable consumption is not common in the region; nonetheless some of the residents consume local vegetables called Kakolak or Siahshour (Suaeda fruticosa), Sowzi (Cardaria draba), and Goshook (Alhagi maurorum which can be a potential source of infection. Further field studies are required to understand the epidemiological status of fascioliasis in the region.

Morphological and molecular analyses of the helminths from our patient identified the isolates as F. hepatica. Isolating adult worms during surgery is a rare observation in the literature [1, 23, 24]. Also, the number of parasites has varied from 1 to 12 worms in different studies [1, 24‐27]. Most of the human cases of fascioliasis in Iran have been identified as F. hepatica. Nevertheless, the first molecular confirmation of F. gigantica was reported in a woman from a village near Mianeh, northwest of the country [28]. In the present study based on molecular investigation and phylogenetic analysis four haplotypes and five polymorphic sites were found among the nine sequenced isolates. The relatively high haplotype variation among the isolates from a patient can suggest that the patient has been frequently exposed to the parasite.

Right upper quadrant, fever, malaise, leukocytosis, weight loss, urticaria, anemia, epigastric pain, sweating, anorexia, jaundice, and hyper-eosinophilia are the most common presentations of human fascioliasis reported from sporadic cases from various parts of the country [18, 26]. Fascioliasis might cause acute attacks of cholangitis, cholecystitis, and biliary obstruction. The formation of stones due to fascioliasis is also possible. Acute cholecystitis due to Fasciola infection is sporadically reported [29]. In moderate and heavy infections mechanical obstruction of the bile ducts and gallbladder is expected due to the large body of these trematodes [26, 30‐32]. The diagnosis can be supported by imaging methods. Sonography appears to be more sensitive than computed tomography in the chronic phase because some specific characters including thickening of the major bile ducts, motile or dead parasites within the ducts or gallbladder, mild dilatation, and edema of the biliary ducts are readily detected by ultrasound [33]. Conventional biliary ultrasonography in fasciolosis usually reveals dilatation and irregular thickened walls with the worms seen as vermiform structures without acoustic shadowing. Only a few reports have described the removal of living flukes (e.g., F. hepatica) from the biliary tract [24, 34, 35].