Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control.

Christina Sunyoung Kim,Pierre Echaubard,Apiporn Suwannatrai,Bruce A Wilcox,Sasithorn Kaewkes,Banchob Sripa,Hans-Peter Fuehrer

doi:10.1371/journal.pntd.0005121

Christina Sunyoung Kim, Pierre Echaubard + Show 5 more

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https://doi.org/10.1371/journal.pntd.0005121

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Abstract

BackgroundOpisthorchis viverrini (Ov) is a complex-life-cycle trematode affecting 10 million people in SEA (Southeast Asia). Human infection occurs when infected cyprinid fish are consumed raw or undercooked. Ov requires three hosts and presents two free-living parasitic stages. As a consequence Ov transmission and infection in intermediate and human hosts are strongly mediated by environmental factors and understanding how environmental variability influences intermediate host abundance is critical. The objectives of this study were 1) to document water parameters, intermediate hosts abundance and infection spatio-temporal variation, 2) to assess their causal relationships and identify windows of transmission risk.Methodology/Principal FindingsFish and snails were collected monthly for one year at 12 sites in Lawa Lake, an Ov-endemic region of Khon Kaen Province in Northeast Thailand. Physicochemical water parameters [pH, temperature (Tp), dissolved oxygen (DO), Salinity, electrical conductivity (EC), total dissolved solid (TDS), nitrite nitrogen (NO2-N), lead (Pb), total coliform bacteria (TCB) and fecal coliform bacteria (FCB)] were measured. Multivariate analyses, linear models and kriging were used to characterize water parameter variation and its influence on host abundance and infection prevalence. We found that sampling sites could be grouped in three clusters and discriminated along a nitrogen-salinity gradient where higher levels in the lake’s southern region predicted higher Bithynia relative abundance (P<0.05) and lower snail and fish species diversity (P<0.05). Highest Bithynia abundance occurred during rainy season (P<0.001), independently of site influence. Cyprinids were the most abundant fish family and higher cyprinid relative abundance was found in areas with higher Bithynia relative abundance (P<0.05). Ov infection in snails was anecdotal while Ov infection in fish was higher in the southern region (P<0.001) at sites showing high FCB.Conclusions/SignificanceOur results indicate that water contamination and waterways configuration can influence freshwater communities’ assemblages possibly creating ideal conditions for sustained transmission. Sustainable control may require a better appreciation of the system’s ecology with wise governance and development planning particularly in the current context of SEA agricultural intensification and landscape modification.

Highlights

Opisthorchis viverrini (Ov), the Southeast Asian liver fluke, is a fish-borne complex life cycle trematode endemic in Thailand, Lao PDR, Cambodia and southern parts of Vietnam where an under-estimate of 10 million people are reported to be at risk of Ov infection [1, 2]
Our study investigated the influences of water parameters on snail and fish abundance and Ov infection rates
We found that salinity and nitrite-nitrogen were positively correlated to Bithynia snail relative abundance and inversely correlated to snail and fish species diversity

Summary

Introduction

Opisthorchis viverrini (Ov), the Southeast Asian liver fluke, is a fish-borne complex life cycle trematode endemic in Thailand, Lao PDR, Cambodia and southern parts of Vietnam where an under-estimate of 10 million people are reported to be at risk of Ov infection [1, 2]. The parasite complex lifecycle begins when Ov eggs are released in the environment through the feces of a definitive human host or reservoir host, which are mostly cats and dogs [8]. The sporocysts develop to rediae and to their free-swimming cercaria stage that will be released in the environment. Thousands of cercariae can be released as free-swimming parasites into the aquatic environment where they actively search for certain species of freshwater fish of the Cyprinidae family, the second intermediate host. The objectives of this study were 1) to document water parameters, intermediate hosts abundance and infection spatio-temporal variation, 2) to assess their causal relationships and identify windows of transmission risk

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