Genetic uniformity, geographical spread and anthropogenic habitat modifications of lymnaeid vectors found in a One Health initiative in the highest human fascioliasis hyperendemic of the Bolivian Altiplano

Abstract

Background: Fascioliasis is a snail-borne zoonotic trematodiasis emerging due to climate changes, anthropogenic environment modifications, and livestock movements. Many areas where Fasciola hepatica is endemic in humans have been described in Latin America altitude areas. Highest prevalences and intensities were reported from four provinces of the northern Bolivian Altiplano, where preventive chemotherapy is ongoing. New strategies are now incorporated to decrease infection/re-infection risk, assessment of human infection sources to enable efficient prevention measures, and additionally a One Health initiative in a selected zone. Subsequent extension of these pilot interventions to the remaining Altiplano is key. Methods: To verify reproducibility throughout, 133 specimens from 25 lymnaeid populations representative of the whole Altiplano, and 11 used for population dynamics studies, were analyzed by rDNA ITS2 and ITS1 and mtDNA cox1 and 16S sequencing to assess their classification, variability and geographical spread. Results: Lymnaeid populations proved to belong to a monomorphic group, Galba truncatula. Only a single cox1 mutation was found in a local population. Two cox1 haplotypes were new. Comparisons of transmission foci data from the 1990's with those of 2018 demonstrated an endemic area expansion. Altitudinal, northward and southward expansions suggest movements of livestock transporting G. truncatula snails, with increasing temperatures transforming previously unsuitable habitats into suitable transmission areas. Transmission foci appear to be stable when compared to past field observations, except for those modified by human activities, including construction of new roads or control measures undertaken in relation to fascioliasis. Conclusions: For a One Health initiative, the control of only one Fasciola species and snail vector species simplifies efforts because of the lower transmission complexity. Vector monomorphism suggests uniformity of vector population responses after control measure implementation. Hyperendemic area outer boundary instability suggests a climate change impact. All populations outside previously known boundaries were close to villages, human dwellings

Sheep and Cattle Reservoirs in the Highest Human Fascioliasis Hyperendemic Area: Experimental Transmission Capacity, Field Epidemiology, and Control Within a One Health Initiative in Bolivia

“…In digeneans, the uterus is an organ adapted to the developmental time of the eggs (in fasciolids, eggs are laid unembryonated, the miracidium beginning its development in eggs once in freshwater). In the Northern Bolivian Altiplano, climatic conditions (29), together with the characteristics of freshwater collections and lymnaeid ecology (28,38), enable F. hepatica transmission to take place throughout the year, so that egg storage in the uterus is less needed than in the northern hemisphere lowlands where F. hepatica transmission is typically seasonal.…”

“…The presence of only G. truncatula as only lymnaeid species inhabiting the Northern Bolivian Altiplano hyperendemic area has recently been confirmed by the sequencing of complete nuclear ribosomal DNA and mitochondrial DNA markers (38). This species is of European origin and differs from the Neotropical species of the Galba/Fossaria group of lymnaeids which also act as vectors of fascioliasis in South America (46).…”

“…Eggs were similarly isolated by filtration and conserved until used for snail infection in the laboratory. No distinction was made between isolates, which may be considered representative of the whole endemic area, as previous molecular studies have demonstrated the uniformity of parasite and snail involved in the disease throughout the whole Northern Bolivian Altiplano (38).…”

“…All animals that were available to us were sampled in each zone, to assure a representative sample size. The zones studied cover all the flatlands, in between the hilly chains, throughout which the disease is detected affecting humans and lymnaeid vectors involved in the transmission are present (28,38). The term of "herd" can be hardly applied to the Northern Bolivian Altiplano, except to the large flatlands of the farms of Achacachi, Kallutaca, and Viacha where no transmission to humans has been reported.…”

“…Results of surveys in humans (36,37) and interannual monitoring assessments in animals furnished an overall picture showing high infection and reinfection risks. Moreover, global warming has resulted in spread of Galba truncatula, the only lymnaeid species in these hyperendemic areas, and thus impacted on F. hepatica transmission (38).…”