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

Santiago Mas-Coma, Maria Mercedes Cafrune, Ilra Renata Funatsu, Atilio Jose Mangold, Rene Angles, Paola Buchon, Maria Cecilia Fantozzi, Patricio Artigas, Maria Adela Valero, Maria Dolores Bargues

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

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 embryogen-esis, miracidial infection of lymnaeid snails, intramolluscan larval development, cercarial produc-tion, 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.

Original languageEnglish
Article number2693
JournalAnimals
Volume11
Issue number9
DOIs
StatePublished - Sep 2021

Bibliographical note

Funding Information:
Funding: This research was funded by Project No. 2017/ACDE/001583 de Innovación para el Desar-rollo 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; Project No. 2017/01 of the V Convocatoria de Proyectos de Cooperación al Desar-rollo de la Universidad de Valencia de 2016, Valencia, Spain; and by CIBER Project CB21/13/00056, ISCIII, Ministry of Science and Education, Madrid, Spain. M.M.C. participated in the experimental procedures during her 6-month stay in the Department of Parasitology, Faculty of Pharmacy, University of Valencia, Spain, funded by a fellowship of the Secretaría de Agricultura, Ganadería y Pesca, Argentina.

Funding Information:
This research was funded by Project No. 2017/ACDE/001583 de Innovaci?n para el Desar-rollo 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; Project No. 2017/01 of the V Convocatoria de Proyectos de Cooperaci?n al Desar-rollo de la Universidad de Valencia de 2016, Valencia, Spain; and by CIBER Project CB21/13/00056, ISCIII, Ministry of Science and Education, Madrid, Spain. M.M.C. participated in the experimental procedures during her 6-month stay in the Department of Parasitology, Faculty of Pharmacy, University of Valencia, Spain, funded by a fellowship of the Secretar?a de Agricultura, Ganader?a y Pesca, Argentina. Acknowledgments: 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 participa-tion 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 organisms, institutions, and centers, as well as their respective representatives or directors: (i) in Argentina: Estaci?n Experimental de Altura Abra Pampa, Abra Pampa, Jujuy; Estaci?n Experimental Agropecuaria Salta, Salta; and Estaci?n Experimental Agropecuaria Rafaela, Rafaela, Santa F?; Mr. Romualdo Suarez and family, owners of the llamas? herd studied in Quichagua, are greatly acknowledged; Ing. Hugo Eduardo Lamas, from Abra Pampa, Jujuy, con-tributed photographs of ?llamas cargueras?. (ii) in Bolivia: 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 (M.A.C.A.) 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).

Publisher Copyright:
© 2021 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

  • Andean fascioliasis endemic areas
  • Argentina
  • Bolivia
  • Experimental transmission
  • Fasciola hepatica
  • Field epidemiology
  • Galba truncatula
  • Llama
  • Reservoir role

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