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

Santiago Mas-Coma, Paola Buchon, Ilra R. Funatsu, René Anglés Rivero, Patricio Artigas, M. Adela Valero, M. Dolores Bargues

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8 Scopus citations

Abstract

The Northern Bolivian Altiplano is the human fascioliasis hyperendemic area where the highest prevalences and intensities of infection by Fasciola hepatica in humans have been reported. Four animal species are the reservoir species for F. hepatica in this area, namely, sheep, cattle, pigs, and donkeys. Livestock for the Aymara inhabitants is crucial because vegetable cultures are not viable due to the inhospitality of the very high altitude of 3,820–4,100 m. A One Health initiative has been implemented in this area in recent years, as the first such control action in a human endemic area ever. Among the different control axes included, special focus is devoted to the two main reservoirs sheep and cattle. Egg embryonation, miracidial infectivity, intramolluscan development, cercarial production, infected snail survival, and metacercarial infectivity were experimentally studied in altiplanic sheep and cattle isolates. These laboratory studies were performed using altiplanic isolates of the lymnaeid species Galba truncatula, the only vector present in the hyperendemic area. Experiments were made at constant 12 h day/12 h night and varying 20/20°C and 22/5°C photoperiods. Infections were implemented using mono-, bi-, and trimiracidial doses. Results demonstrate that sheep and cattle have the capacity to assure F. hepatica transmission in this very high-altitude area. Field surveys included prevalence studies by coprology on fecal samples from 1,202 sheep and 2,690 cattle collected from different zones of the Northern Bolivian Altiplano. Prevalences were pronouncedly higher and more homogeneous in sheep (63.1%; range: 38.9–68.5%) than in cattle (20.6%; range: 8.2–43.3%) in each one of the different zones. Although similarities between the prevalences in sheep and cattle appeared in the zones of the highest and lowest infection rates, this disappeared in the other zones due to cattle treatments. Comparison with past surveys demonstrates that this hyperendemic area is stable from the disease transmission point of view. Therefore, the control design should prioritize sheep and cattle within the One Health action. Studies performed in the Bolivian Altiplano furnish a baseline for future initiatives to assess the transmission and epidemiological characteristics of fascioliasis in the way for its control in other high altitude Andean endemic areas.

Original languageEnglish
Article number583204
JournalFrontiers in Veterinary Science
Volume7
DOIs
StatePublished - 27 Oct 2020

Bibliographical note

Funding Information:
Studies of this article were funded by Project No. 2017/ACDE/001583 de Innovación para el Desarrollo of the Agencia Española de Cooperación Internacional para el Desarrollo (AECID), Ministry of Foreign Affairs and Cooperation, Madrid, Spain; by 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 Headquarters Vienna, Austria); by Health Research Project No. PI16/00520, Subprograma Estatal de Generación de Conocimiento de la Acción Estratégica en Salud (AES) y Fondos FEDER, Plan Estatal de Investigación Científica y Técnica y de Innovación, ISCIII-MINECO, Madrid, Spain; by the Red de Investigación de Centros de Enfermedades Tropicales—RICET (Project No. RD16/0027/0023 of the PN de I+D+I, ISCIII-Subdirección General de Redes y Centros de Investigación Cooperativa RETICS), Ministry of Health and Consumption, Madrid; by Project No. 2016/099 of the PROMETEO Program, Programa of Ayudas para Grupos de Investigación de Excelencia, Generalitat Valenciana, Valencia, Spain; and by Project No. 2017/01 of the V Convocatoria de Proyectos de Cooperación al Desarrollo de la Universidad de Valencia de 2016, Valencia, Spain.

Funding Information:
Studies of this article have been performed within the framework of the Worldwide Initiative of WHO against Human Fascioliasis (WHO Headquarters, Geneva, Switzerland). One Health initiative designed within the official meeting Reuni?n de An?lisis con Expertos sobre la Situaci?n Actual y Pr?ximos Pasos para el Control de la Fascioliasis en Bolivia, organized by PAHO/WHO in Hotel Camino Real, Calacoto, La Paz, on 10?12 November 2014, with the participation of (i) Ministerio de Salud de Bolivia, (ii) Ministerio de Desarrollo Rural y Tierras de Bolivia, (iii) Servicio Departamental de Salud de La Paz (SEDES La Paz, (iv) representatives of the Aymara communities from the Northern Altiplano endemic area, (v) delegates from Per?, (vi) experts and advisers of the Programa Regional de Enfermedades Infecciosas Desatendidas of PAHO/WHO, and from the WHO Collaborating Centre on Fascioliasis and its Snail Vectors of Valencia, and (vii) other foreign experts. The authors acknowledge the facilities provided and the collaboration received from the following Bolivian organisms, institutions, and centers, as well as their respective representatives or directors: Servicio Departamental de Salud La Paz (SEDES La Paz); Unidad de Epidemiolog?a of the Bolivian Ministry of Health, La Paz; Office of the Pan American Health Organization in La Paz; Direcci?n Nacional de Producci?n Pecuaria and the Instituto Nacional de Biolog?a Animal of Chasquipampa-Calacoto both of the Ministerio de Asuntos Campesinos y Agropecuarios (MACA) in La Paz; and Granja de Mejoramiento Ganadero de Kallutaca related to the Programa de Fomento Lechero of the Corporaci?n Regional de Desarrollo de La Paz (CORDEPAZ, El Alto). Funding. Studies of this article were funded by Project No. 2017/ACDE/001583 de Innovaci?n para el Desarrollo of the Agencia Espa?ola de Cooperaci?n Internacional para el Desarrollo (AECID), Ministry of Foreign Affairs and Cooperation, Madrid, Spain; by 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 Headquarters Vienna, Austria); by Health Research Project No. PI16/00520, Subprograma Estatal de Generaci?n de Conocimiento de la Acci?n Estrat?gica en Salud (AES) y Fondos FEDER, Plan Estatal de Investigaci?n Cient?fica y T?cnica y de Innovaci?n, ISCIII-MINECO, Madrid, Spain; by the Red de Investigaci?n de Centros de Enfermedades Tropicales?RICET (Project No. RD16/0027/0023 of the PN de I+D+I, ISCIII-Subdirecci?n General de Redes y Centros de Investigaci?n Cooperativa RETICS), Ministry of Health and Consumption, Madrid; by Project No. 2016/099 of the PROMETEO Program, Programa of Ayudas para Grupos de Investigaci?n de Excelencia, Generalitat Valenciana, Valencia, Spain; and by Project No. 2017/01 of the V Convocatoria de Proyectos de Cooperaci?n al Desarrollo de la Universidad de Valencia de 2016, Valencia, Spain.

Publisher Copyright:
© Copyright © 2020 Mas-Coma, Buchon, Funatsu, Angles, Artigas, Valero and Bargues.

Keywords

  • Bolivia
  • epidemiology
  • Fasciola hepatica
  • human hyperendemic
  • reservoirs
  • sheep and cattle
  • transmission
  • very high altitude

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