Domestic pig prioritized in one health action against fascioliasis in human endemic areas: Experimental assessment of transmission capacity and epidemiological evaluation of reservoir role

Abstract

The Northern Bolivian Altiplano is the human fascioliasis hyperendemic area where the highest prevalences and intensities in humans have been reported. Preventive chemotherapy was implemented in the last ten years. Surveillance showed high human infection and re-infection rates in between the annual triclabendazole monodose treatments. A complementary One Health control action was launched to decrease the infection risk. Among the multidisciplinary axes, there is the need to establish animal reservoir species priorities for a more efficient control. Laboratory and field studies were performed for the first time to assess the Fasciola hepatica transmission capacity of the pig and its potential reservoir role. The experimental follow-up of altiplanic pig isolates through altiplanic Galba truncatula snail vector isolates were performed at different miracidial doses and different day/night temperatures. Experiments included egg embryonation, miracidial infectivity, lymnaeid snail infection, intramolluscan larval development, cercarial production, chronobiology of the cercarial shedding, vector survival to infection, metacercarial infectivity of mammal host, and adult stage development. Surveys included the assessment of prevalence, intensity, egg measurements and egg shedding rates in nature. Pig contribution was evaluated by comparing with the main altiplanic reservoirs sheep and cattle. Results demonstrated that the pig assures the whole F. hepatica life cycle and participates in its transmission in this area. The fast egg embryonation, high cercarial production, long multi-wave shedding chronobiological pattern in monomiracidial infections at permanent 20 °C temperature, and the high daily egg outputs per pig are worth mentioning. The high infection risk suggests early infection of freely running piglets and evolutionary long-term adaptation of the liver fluke to this omnivorous mammal, despite its previously evoked resistance or non-suitability. Genetic, physiological and immune similarities with humans may also underlie the parasite adaptation to humans in this area. The pig should be accordingly included for appropriate control measures within a One Health action against human fascioliasis. The pig should henceforth be considered in epidemiological studies and control initiatives not only in fascioliasis endemic areas with human infection risk on other Andean countries, but also in rural areas of Latin America, Africa and Asia where domestic pigs are allowed to run freely.

Very High Fascioliasis Intensities in Schoolchildren from Nile Delta Governorates, Egypt: The Old World Highest Burdens Found in Lowlands

“…In Egypt, subjects were treated after active detection by qualitative coprological diagnosis with the fast and simple Kato-Katz technique [ 29 , 30 ], by the survey teams of the Ministry of Health and Population (MoHP) located throughout the endemic rural areas and already working on another freshwater snail-borne trematodiasis such as schistosomiasis [ 31 ]. Moreover, a multidisciplinary One Health intervention is underway to complement preventive chemotherapy in Bolivia, to decrease infection and re-infection risks in between the annual treatment campaigns [ 4 , 6 , 32 , 33 ].…”

Spread of the fascioliasis endemic area assessed by seasonal follow-up of rDNA ITS-2 sequenced lymnaeid populations in Cajamarca, Peru

“…Galba truncatula and L. schirazensis are amphibious snails that share the capacity of being passively transported when they remain in dried mud stuck to the feet of ruminants, then go into hibernation or estivation during the drought, and be able to reactivate once in a new location following contact with water [ 4 , 33 ]. The detection of Galba truncatula indicates the freshwater collection to be of risk for liver fluke infection, as it has proved to transmit liver fluke isolates from the different mammal host species in the highlands [ [61] , [62] , [63] ]. The non- transmitting species L. schirazensis has proved to be a useful biomarker for the follow-up of livestock movements and fascioliasis spread, inter- and intra-continentally and also locally [ 33 ].…”

One Health Action against Human Fascioliasis in the Bolivian Altiplano: Food, Water, Housing, Behavioural Traditions, Social Aspects, and Livestock Management Linked to Disease Transmission and Infection Sources

“…Consequently, terms as outbreak or epidemics [89] should be considered misinterpretations of the transmission and epidemiological situation. Only human action appears to modify given transmission foci, as for instance along the construction of paved roads, implementation of irrigations, and improvement of water sources [48].…”

“…Sheep and cattle have demonstrated that they are able to participate as the main reservoirs, even at such a high altitude [47]. The domestic pig has proven to be the third most important reservoir, despite many previous studies arguing against the potential role of this animal in fascioliasis [48]. The donkey demonstrated that it was the fourth reservoir species involved, with a problematic role in the geographical diffusion of both liver fluke and snail vector [49].…”