The life cycle of a zoonotic parasite reassessed: Experimental infection of Melanoides tuberculata (Mollusca: Thiaridae) with Centrocestus formosanus (Trematoda: Heterophyidae)

Abstract

Centrocestus formosanus is a foodborne intestinal trematode that is native to Asia and has been introduced into the Americas and Europe. Although there are several studies of C. formosanus in definitive vertebrate hosts (birds and mammals, including humans), and in intermediate vertebrate hosts (fish and amphibians), there is little published information regarding interaction with its transmitting mollusc. In this study we studied the miracidial development of C. formosanus using a mouse as a source of eggs. Adult parasites were maintained in water in order to develop miracidia in intrauterine eggs. Miracidia appeared at 12 days of incubation, with no hatching observed for up to 40 days. Subsequently, we placed dead C. formosanus containing eggs with miracidia individually in contact with 48 specimens of Melanoides tuberculata, and observed the absence of the parasites after 1h of exposure, suggesting that they were ingested by the snails. Of the 33 experimentally-infected snails that were alive after 84–89 days post-infection (DPI), seven (21%) shed cercariae. We detected young C. formosanus rediae in 21/33 (64%) M. tuberculata at 90 DPI. To our knowledge, this report is the first to show that, in the life cycle of C. formosanus, infection of molluscs occurs passively by ingestion of eggs, followed by a long intramolluscan phase. We compare these data with those described for other Heterophyidae, and discuss on the phylogenetic background of the pattern of miracidial development verified in these parasites.

Diagnosis of Centrocestus formosanus Infection in Zebrafish (Danio rerio) in Italy: A Window to a New Globalization-Derived Invasive Microorganism

“…The current report draws the attention on C. formosanus as an invasive parasite, as well as on other species that could be similarly introduced in Europe, underlining the need for epidemiological studies and appropriate preventive and control programs, in order to monitor their occurrence and prevent their negative consequences for economy, biodiversity, scientific research, animal and public health [6,17,19,20,22,23,[28][29][30]47,48]. Some aspects of biology and epidemiology, regarding both animal and human hosts, should be further explored in Europe [7,17,20,26,47,49].…”

“…Subsequently, free-swimming cercariae encyst in second intermediate fish hosts, specifically in the gills, where they develop into metacercariae. Piscivorous birds and mammals, ingesting the infected fish, complete the cycle [4,15,16,18,19,23]. Analogously, human infections can occur through consumption of raw or improperly cooked fish, containing metacercariae [12,15,24].…”

“…Among the numerous freshwater fish species affected by C. formosanus [23,25], zebrafish (Danio rerio) have been considered susceptible to infection, but only three reports have been described to date [10,21,32].…”

Current Knowledge of Small Flukes (Digenea: Heterophyidae) from South America

“…Centrocestus formosanus Nishigori, 1924, a species considered of zoonotic importance, was introduced in the Americas within its host snail Melanoides tuberculata. It has been reported from Brazil [43][44][45][46][47], Colombia [48], Peru [50] and Venezuela [51]. The life-cycle includes naturally infected fish (metacercariae in the gills) and birds (adults in the intestine) and experimental infections were performed with G. gallus [45] (Table 1).…”

“…It has been reported from Brazil [ 43 – 47 ], Colombia [ 48 ], Peru [ 50 ] and Venezuela [ 51 ]. The life-cycle includes naturally infected fish (metacercariae in the gills) and birds (adults in the intestine) and experimental infections were performed with G. gallus [ 45 ] ( Table 1 ). To our knowledge there are no reports on human infections by C. formosanus in SA.…”