DNA multigene characterization of Fasciola hepatica and Lymnaea neotropica and its fascioliasis transmission capacity in Uruguay, with historical correlation, human report review and infection risk analysis

PLoS Negl Trop Dis. 2017 Feb 3;11(2):e0005352. doi: 10.1371/journal.pntd.0005352. eCollection 2017 Feb.

Abstract

Background: Fascioliasis is a pathogenic disease transmitted by lymnaeid snails and recently emerging in humans, in part due to effects of climate changes, anthropogenic environment modifications, import/export and movements of livestock. South America is the continent presenting more human fascioliasis hyperendemic areas and the highest prevalences and intensities known. These scenarios appear mainly linked to altitude areas in Andean countries, whereas lowland areas of non-Andean countries, such as Uruguay, only show sporadic human cases or outbreaks. A study including DNA marker sequencing of fasciolids and lymnaeids, an experimental study of the life cycle in Uruguay, and a review of human fascioliasis in Uruguay, are performed.

Methodology/principal findings: The characterization of Fasciola hepatica from cattle and horses of Uruguay included the complete sequences of the ribosomal DNA ITS-2 and ITS-1 and mitochondrial DNA cox1 and nad1. ITS-2, ITS-1, partial cox1 and rDNA 16S gene of mtDNA were used for lymnaeids. Results indicated that vectors belong to Lymnaea neotropica instead of to Lymnaea viator, as always reported from Uruguay. The life cycle and transmission features of F. hepatica by L. neotropica of Uruguay were studied under standardized experimental conditions to enable a comparison with the transmission capacity of F. hepatica by Galba truncatula at very high altitude in Bolivia. On this baseline, we reviewed the 95 human fascioliasis cases reported in Uruguay and analyzed the risk of human infection in front of future climate change estimations.

Conclusions/significance: The correlation of fasciolid and lymnaeid haplotypes with historical data on the introduction and spread of livestock into Uruguay allowed to understand the molecular diversity detected. Although Uruguayan L. neotropica is a highly efficient vector, its transmission capacity is markedly lower than that of Bolivian G. truncatula. This allows to understand the transmission and epidemiological differences between Andean highlands and non-Andean lowlands in South America. Despite rainfall increase predictions for Uruguay, nothing suggests a trend towards a worrying human infection scenario as in Andean areas.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acanthaceae / parasitology*
  • Animals
  • Cattle
  • Cluster Analysis
  • DNA, Helminth / chemistry
  • DNA, Helminth / genetics
  • DNA, Ribosomal / chemistry
  • DNA, Ribosomal / genetics
  • DNA, Ribosomal Spacer / chemistry
  • DNA, Ribosomal Spacer / genetics
  • Fasciola hepatica / classification*
  • Fasciola hepatica / genetics
  • Fasciola hepatica / isolation & purification*
  • Fascioliasis / epidemiology
  • Fascioliasis / transmission*
  • Genetic Variation*
  • Genotype
  • Horses
  • Humans
  • Phylogeny
  • RNA, Ribosomal, 16S / genetics
  • Risk Assessment
  • Sequence Analysis, DNA
  • Uruguay

Substances

  • DNA, Helminth
  • DNA, Ribosomal
  • DNA, Ribosomal Spacer
  • RNA, Ribosomal, 16S

Grants and funding

Joint coordination activities carried out within Project No. RLA5049 of the International Atomic Energy Agency (Animal Production and Health Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Department of Nuclear Sciences and Applications, IAEA Headquaters Vienna, Austria). Spanish collaboration supported by Projects Nos. SAF2006-09278 and SAF2010-20805 of the Ministry of Economy and Competitiveness, Madrid, Spain; by the Red de Investigación Cooperativa en Enfermedades Tropicales – RICET (Projects Nos. RD12/0018/0013 and RD16/0027/0023 of the PN de I+D+I 2008-2011 and 2013-2016, ISCIII-Subdirección General de Redes y Centros de Investigación Cooperativa RETICS), Ministry of Health and Consumption, Madrid; and by Projects Nos. 2012/042 and 2016/099 of the PROMETEO Program, Generalitat Valenciana, Valencia, Spain. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.