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 and/or schools, and should therefore be considered during disease control planning. The remarkable southward expansion implies that a fifth province, Aroma, should now be included within preventive chemotherapy programmes. This study highlights the need for lymnaeid molecular identification, transmission foci stability monitoring, and potential vector spread assessment.

Keywords: Galba truncatula; Geographical spread; Habitat modifications; Human fascioliasis; Lymnaeids; Northern Bolivian Altiplano; One Health; mtDNA; rDNA.

Fig. 1

Location of the northern Bolivian Altiplano human fascioliasis hyperendemic area. a Map showing the location of Bolivia in South America. b Topographic map showing the location of the endemic area in the very high-altitude region of the northern Altiplano close to Lake Titicaca and eastern Andean chain. c Political map showing the endemic area inside the Bolivian Department of La Paz. d Political and geographical map showing the endemic area throughout the corridors and zones between Lake Titicaca and the Bolivian capital of La Paz, dispersed within the five provinces of Omasuyos, Los Andes, Murillo, Ingavi and Aroma of the Department of La Paz. Background for b from composed satellite map of South America orthographic projection by NASA (full resolution of 1215 × 1712 pixels; public domain) via Wikimedia Commons. Hand-made drawing for d created using Microsoft® PowerPoint for Mac v. 16.25. Original SM-C

Fig. 2

Northern Bolivian Altiplano human fascioliasis hyperendemic area. a Map showing the location of the lymnaeid vector populations studied. b Magnified map showing northward lymnaeid population spread into the Peñas-Kerani corridor. c Magnified map showing altitudinal lymnaeid population spread into the hill chain between the Tambillo-Huacullani corridor and the Tiwanaku-Guaqui corridor. d Magnified map showing southward lymnaeid population spread up to the Patacamaya zone. Hand-made drawing created using Microsoft® PowerPoint for Mac v. 16.25. Original SM-C. Key: Blue triangles, freshwater habitats presenting lymnaeid populations; red circles, localities where cattle was proved to be infected by the liver fluke in previous studies; green squares, human villages; grey shaded areas, large cities of La Paz and El Alto; brown outline, mountainous areas delimiting flatlands and corridors; green-shaded parts in b, c and d, zones of altitudes suitable for lymnaeid existence in the past; numbers/letters correspond to lymnaeid vector populations studied (see Table 1) inside/outside the past established boundaries of the endemic area [34]

Fig. 3

Lymnaeids, their habitats and distribution boundaries in the northern Bolivian Altiplano. aGalba truncatula Morph I (Lymnaea viatrix sensu Ueno et al. [58]) of the northern Bolivian Altiplano. bGalba truncatula Morph II (Lymnaea cubensis sensu Ueno et al. [58]) of the northern Bolivian Altiplano. c Bolivian shore of Lake Titicaca covered by typical totora (Schoenoplectus californicus totora). d Achocalla, a small fascioliasis endemic sub-valley of the large La Paz Valley. e Large amounts of salts on the terrestrial surface in the Catari-Capiri zone southward from Viacha. f Community of the Huacullani corridor showing dispersed dwellings, lymnaeid-inhabited water bodies in between and free livestock running throughout. g Overview of eastern part of the large corridor from Tambillo to Huacullani. h Subsoil effluence presenting lymnaeids close to the village of Yanarico with liver fluke infected children, in the Tiwanaku-Guaqui corridor. Photographs: SM-C

Fig. 4

Nucleotide and amino acid differences found in the mtDNA cox1 sequence of Galba truncatula populations studied from the northern Bolivian Altiplano and other G. truncatula haplotypes of the same species. Position (numbers to be read in vertical) refer to variable positions obtained in the alignment made with MEGA 6.0.6 (“ . ”, identical; *, present paper). Haplotype codes are only provisional due to incomplete sequences of the gene

Fig. 5

Aspects of lymnaeid control in the Northern Bolivian Altiplano. a Children along their daily way from home to school and back in the Huacullani zone. b External faucet and basin in front of a health center in Huacullani. c Installation of metal fences surrounding lymnaeid-inhabited water bodies close to Huacullani village. d Unused artificial drinking trough for livestock despite infection risk due to lymnaeid presence in neighboring river. e Potential large-scale lymnaeid spread due to cattle transport with trucks along the El Alto-Batallas/Peñas route. f Potential small-scale lymnaeid spread linked to goods and merchandise transport by donkeys in the Suriquiña zone. Photographs: SM-C

Fig. 6

Lymnaeid freshwater habitats found outside the past-established boundaries of the human fascioliasis hypendendemic area in the northern Bolivian Altiplano. a–c Corridor of Peñas. a Peñas: small stream inside the village. b San Calixto: river margin close to the village. c Suriquiña: zone inside village flooded by stream from eastern Andean chain. d, e Rosa Pata hilly zone. d Rosa Pata: small stream close to school. e Rosa Pata surroundings: covered water well on hill side, dry stream, and lymnaeid-inhabited natural subsoil effluence preferred as water source by livestock instead of close artificial drinking trough. f-h Patacamaya zone. f Challapata: river margin close to rural dwellings. g Ayo Ayo: flooded zone next to the river under bridge on route to neighbouring village. h Viscachani: small stream running under train bridge with village in the background. Photographs: SM-C