Fascioliasis in Llama, Lama glama, in Andean Endemic Areas: Experimental Transmission Capacity by the High Altitude Snail Vector Galba truncatula and Epidemiological Analysis of Its Reservoir Role

SIMPLE SUMMARY: The infection by the liver fluke Fasciola hepatica in South American camelids, mainly llamas and alpacas, has been the focus of many studies. However, their capacity to participate in the transmission of the disease and their potential reservoir role in human or animal endemic areas have never been studied. Therefore, all development stages of an isolate from Argentine llama of the high Andean plateau have been experimentally investigated, from egg embryogenesis to metacercarial infectivity, by using the vector snail Galba truncatula from the high altitude Bolivian Altiplano human hyperendemic area. Although eggs shed by llamas may successfully develop until the adult stage in a subsequent mammal host, the transmission capacity of the llama proved to be pronouncedly less efficient than that of other hosts as sheep and cattle. Moreover, the low prevalences, intensities, and daily fecal outputs of liver fluke eggs in llama in Andean endemic areas, together with their peculiar defecating behavior in dung piles always far from freshwater collections, indicate that the contribution of this camelid should be considered negligible. Therefore, the llama does not need to receive priority within fascioliasis control initiatives, although it may play a disease-spreading role if used as a pack animal. ABSTRACT: South American camelids are definitive hosts of Fasciola hepatica. However, their capacity to participate in the transmission and epidemiology of fascioliasis has never been appropriately studied. Therefore, an F. hepatica isolate from Argentine llama is for the first time analyzed using Galba truncatula lymnaeids from Bolivia. Experimental follow-up studies included egg embryogenesis, miracidial infection of lymnaeid snails, intramolluscan larval development, cercarial production, chronobiology of cercarial shedding, vector survival to infection, and metacercarial infectivity of mammal host. Shorter prepatent and patent periods were leading to markedly lower cercarial production, shorter cercarial shedding, and a higher negative impact on snail survival. The usually low liver fluke prevalences and intensities and low daily fecal outputs indicate that llamas do not substantially contribute to fascioliasis transmission. The defecating behavior in dung piles far from freshwater collections prevents lymnaeid infection by eggs shed by this camelid. All results suggest the reservoir role of the llama to be negligible and, therefore, no priority within control measures in endemic areas. However, llamas may play a disease-spreading role if used as pack animals in rural areas. In the Northern Bolivian Altiplano human hyperendemic area, neither llamas nor alpacas should be considered for control measures within a One Health action.