Prospects and Challenges towards Sustainable Liver Fluke Control

Abstract

The liver fluke Opisthorchis viverrini (Ov) is endemic in Southeast Asia where more than 10 million people are estimated to be infected. The infection is associated with several hepatobiliary diseases, including cholangiocarcinoma (CCA). Northeast Thailand is a hotspot for Ov transmission, and, despite extensive public health prevention campaigns led by the government, the prevalence of Ov infection is still high. High infection rates result from cultural and ecological complexities where wet-rice agrarian habitats, centuries-old raw-food culture, and the parasite's complex biology combine to create an ideal transmission arena. Here we review the state of our knowledge regarding the social-ecological determinants underlying Ov transmission. We also describe an integrative research rationale for liver fluke control better aligned with sustainable health development.

Keywords: Opisthorchis viverrini; disease ecology; global health; integrated control; landscape epidemiology; transdisciplinarity.

Figure 1. Opisthorchis viverrini transmission cycle

Human infection occurs when cyprinid fish bearing metacercariae in their tissues and organs are consumed raw or partially cooked (including smoked, pickled and salted). Metacercariae in the fish excyst in the duodenum and enter the bile ducts, where they mature sexually. The adult worms produce eggs which are passed out in faeces to the environment. When freshwater Bithynia snails ingest the eggs, miracidium hatch and develop into sporocysts which undergo asexual multiplication, and develop into rediae and cercariae. Upon release in the environment, free-swimming cercariae actively search for a fish host, most often from the cyprinidae family, to penetrate the tissues and skin and develop into metacercariae infective to humans and other fish-eating mammals.

Figure 2. Environmental influences on Opisthorchis viverrini natural hosts and infection prevalence

Kriging geographic analysis of the abundance of A) cyprinid fish and B) Bithynia siamensis goniomphalos in relation to salinity (top panel) and nitrite (middle panel). Bottom panel shows the prevalence of Opisthorchis viverrini infection. Data for the rainy season, cool season and hot season is shown. Adapted from [37].

Figure 3. Blueprint illustrating environmental factors known or suspected to be associated with transmission of Opisthorchis viverrini

Regional environmental change, which is influenced significantly by population growth, resource consumption, economic development projects, agriculture intensification and waste generation, plays an important role in the emergence of infectious disease in general especially in tropical developing regions. In the case of Opisthorchis viverrini (Ov), although the importance of these broader determinants have been evoked more than a decade ago [2], formal research acknowledging their significance in modulating transmission dynamics and disease manifestation has just begun. Of particular concern in the case of Ov is the unprecedented land use and transformation of resource production (urbanization, agricultural expansion and intensification, and natural habitat alteration) that has intensified during the last decade in the region, and that is increasingly recognized to have produced changes in ecological systems, notably in landscapes and, in turn, their natural communities and ultimately in their parasites, animal host, and human populations. Thus the entire host-parasite dynamics is being modified, including pattern of exposure and susceptibility to disease. Designing research and interventions that integrate these broad scale determinants of transmission and their interactions is key for the proper contextualization of Opisthorchis viverrini control. Overarching systemic factors related to public health infrastructure and climate variability, and their interactions with regional environmental change, also contribute significantly to disease emergence although more diffusely.

Figure I

* Food sharing and infection. A) All else being equal, sharing raw fish dishes among community members may contribute to increase the number of individuals infected (prevalence) but also dilute disease risk associated with inflammation as infection intensity per capita will be lower on average. B) Depending on social network group member occupations, likelihood for consumption of raw fish dishes varies. For example, rice farmers and fishermen are more likely to consume raw fish dishes and defecate in or near wetlands and rice fields due to their daily activities. Accordingly, the quantity of Ov eggs to be released in environments where Bithynia snails are found (wetlands, rice fields), thus transmission risk, will also vary among individuals having different occupations.