Skip to main content Accessibility help
Hostname: page-component-59b7f5684b-ns2hh Total loading time: 0.46 Render date: 2022-09-28T18:56:33.689Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": false, "useSa": true } hasContentIssue true

Article contents

First report of pre-Hispanic Fasciola hepatica from South America revealed by ancient DNA

Published online by Cambridge University Press:  20 December 2019

María Ornela Beltrame*
Grupo de investigación: Paleoparasitología. Instituto de Investigaciones en Producción, Sanidad y Ambiente (IIPROSAM), Facultad de Ciencias Exactas y Naturales, UNMdP-CONICET, Mar del Plata, Buenos Aires, Argentina
Cesar Pruzzo
Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata (UNLP), La Plata, Argentina
Rodrigo Sanabria
Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata (UNLP), La Plata, Argentina Instituto Tecnológico Chascomús (INTECH) – CONICET-Universidad Nacional de San Martín (UNSAM), Chascomús, Argentina
Alberto Pérez
Departamento de Antropología, Universidad Católica de Temuco, Campus San Francisco, Temuco, Región de La Araucanía, Chile
Matías Sebastián Mora
Instituto de Investigaciones Marinas y Costeras (IIMyC), CONICET, Universidad Nacional de Mar del Plata (UNMDP), Mar del Plata, Argentina
Author for correspondence: María Ornela Beltrame, E-mail:


It is generally assumed that the digenean human liver fluke, Fasciola hepatica, gained entry to South America during the 15th century upon arrival of Europeans and their livestock. Nonetheless in Patagonia, Argentina, digenean eggs similar to F. hepatica have been observed in deer coprolites dating back to 2300 years B.P. The main objective of our present study was to identify and characterize these eggs using an ancient DNA (aDNA) study. Eggs were isolated and used for aDNA extraction, amplification and sequencing of partial regions from the cytochrome c oxidase subunit 1 and the nicotinamide adenine dinucleotide dehydrogenase subunit 1 mitochondrial genes. Also, phylogenetic trees were constructed using Bayesian and maximum likelihood. Our results confirm the presence of F. hepatica in South America from at least 2300 years B.P. This is the first report and the first aDNA study of this trematode in South America prior to the arrival of the European cattle in the 15th century. The present work contributes to the study of phylogenetic and palaeobiogeographical aspects of F. hepatica and its settlement across America.

Research Article
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Askari, Z, Mas-Coma, S, Bouwman, AS, Boenke, N, Stöllner, T, Aali, A, Rezaiian, M and Mowlavi, G (2018) Fasciola hepatica eggs in paleofaeces of the Persian onager Equus hemionus onager, a donkey from Chehrabad archaeological site, dating back to the Sassanid Empire (224–651 CE), in ancient Iran. Infection, Genetic and Evolution 62, 233243.CrossRefGoogle Scholar
Bargues, MD, Gayo, V, Sanchis, J, Artigas, P, Khoubbane, M, Birriel, S and Mas-Coma, S (2017) 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 Neglected Tropical Diseases 11, e0005352.CrossRefGoogle ScholarPubMed
Beltrame, MO, Tietze, E, Pérez, AE and Sardella, NH (2017) First paleoparasitological record of digenean eggs from a native deer from Patagonia Argentina (Cueva Parque Diana archaeological site). Veterinary Parasitology 235, 8385.Google Scholar
Bouchet, F (1995) Recovery of helminth eggs from archaeological excavations of the Grand Louvre (Paris, France). Journal of Parasitology 81, 785787.CrossRefGoogle Scholar
Bouchet, F, Harter, S and Le Bailly, M (2003) The state of the art of paleoparasitological research in the Old World. Memórias Instituto Oswaldo Cruz 98, 95101.CrossRefGoogle ScholarPubMed
Bouckaert, R, Vaughan, TG, Barido-Sottani, J, Duchêne, S, Fourment, M, Gavryushkina, A, Heled, J, Jones, G, Kühnert, D, De Maio, N, Matschiner, M, Mendes, FK, Müller, NF, Ogilvie, HA, du Plessis, L, Popinga, A, Rambaut, A, Rasmussen, D, Siveroni, I, Suchard, MA, Wu, C, Xie, D, Zhang, C, Stadler, T and Drummond, AJ (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15, e1006650.CrossRefGoogle ScholarPubMed
Bravo Antilef, MJ (2013) Probables causas de muerte y principales hallazgos en la necropsia de pudúes (Pudu puda) examinados durante 20 años en el sur de Chile. Memoria de Título. Universidad Austral de Chile. Facultad de Ciencias Veterinarias. Instituto de Patología Animal. Chile.Google Scholar
Carmona, C and Tort, JF (2016) Fasciolosis in South America: epidemiology and control challenges. Journal of Helminthology 91, 99109.CrossRefGoogle ScholarPubMed
Cortés, M (2006) Identificación de formas reproductivas de parásitos gastrointestinales, en mamíferos nativos presentes en el Buin Zoo, Chile. Memoria de título. Escuela de Medicina Veterinaria, Universidad de Concepción, Chillán, Chile.Google Scholar
Côté, NML, Daligault, J, Pruvost, M, Bennett, EA, Gorgé, O, Guimaraes, S, Capelli, N, Le Bailly, M, Geigl, E and Grange, T (2016) A new high-throughput approach to genotype ancient human gastrointestinal parasites. PLoS ONE 11, e0146230.CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Díaz, NI and Smith-Fluek, JA (2000) El Huemul patagónico: un misterioso cérvido al borde de la extinción. Argentina: L.O.L.A., pp. 156.Google Scholar
Dittmar, K and Teegen, WR (2003) The presence of Fasciola hepatica (liver-fluke) in humans and cattle from a 4500 year old archaeological site in the Saale-Unstrut-Valley, Germany. Memórias do Instituto Oswaldo Cruz 98, 141145.CrossRefGoogle ScholarPubMed
Drummond, AJ and Rambaut, A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Drummond, AJ, Ho, SYW, Phillips, MJ and Rambaut, A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.CrossRefGoogle Scholar
Ferreira, LF (2014) An introduction to paleoparasitology. In Ferreira, LF, Reinhard, K and Araújo, A (eds), Foundations of Paleoparasitology. Rio de Janeiro, Brazil: Fiocruz/International Federation of Tropical Medicine, pp. 2741.CrossRefGoogle Scholar
Flueck, WT and Smith-Flueck, JM (2012) Diseases of red deer introduced to Patagonia and implications for native ungulates. Animal Production Science 52, 766773.CrossRefGoogle Scholar
Ichikawa, M and Itagaki, T (2012) Molecular analysis of aspermic Fasciola flukes from Korea on the basis of the nuclear ITS1 region and mitochondrial DNA markers and comparison with Japanese aspermic Fasciola flukes. The Journal of Veterinary Medical Science 74, 899904.CrossRefGoogle ScholarPubMed
Issia, L, Pietrokovsky, S, Sousa-Figueiredo, J, Russell Stothard, J and Wisnivesky-Colli, C (2009) Fasciola hepatica infections in livestock flock, guanacos and coypus in two wildlife reserves in Argentina. Veterinary Parasitology 165, 341344.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.CrossRefGoogle ScholarPubMed
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ and Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23, 29472948.CrossRefGoogle ScholarPubMed
Le, TH, Blair, D, Agatsuma, T, Humair, PF, Campbell, NJ, Iwagami, M, Littlewood, DT, Peacock, B, Johnston, DA, Bartley, J, Rollinson, D, Herniou, EA, Zarlenga, DS and McManus, DP (2000) Phylogenies inferred from mitochondrial gene orders-a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 11231125.CrossRefGoogle ScholarPubMed
Le Bailly, M, Goepfert, N, Prieto, G, Verano, J and Dufour, B (2019) Camelid gastrointestinal parasites from the Archaeological Site of Huanchaquito (Peru): first results. Environmental Archaeology. doi: 10.1080/14614103.2018.1558804.CrossRefGoogle Scholar
Mas-Coma, S (2005) Epidemiology of fascioliasis in human endemic areas. Journal of Helminthology 79, 207216.CrossRefGoogle ScholarPubMed
Mas-Coma, S, Valero, MA and Bargues, MD (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41146.CrossRefGoogle ScholarPubMed
Mas-Coma, S, Agramunt, VH and Valero, MA (2014) Neurological and ocular fascioliasis in humans. Advances in Parasitology 84, 27149.CrossRefGoogle ScholarPubMed
Pérez, AE (2010) La Localidad Arqueológica Lago Meliquina, Dto. Lácar, Neuquén. El registro arqueológico del interior y borde de bosque en Norpatagonia. Actas y Memorias del XVII Congreso Nacional de Arqueología Chilena, Valdivia, Chile, 2006, pp. 15151528.Google Scholar
Pérez, AE, Aguirre, MG and Graziano, JE (2015) Improntas de cariopsis de gramíneas (Poaceae) en un fragmento de alfarería de Patagonia Noroccidental Argentina. Revista de Antropología del Museo de Entre Ríos 1, 7785.Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901904.CrossRefGoogle ScholarPubMed
Reinhard, KJ (1992) Parasitology as an interpretative tool in archaeology. American Antiquity 57, 231245.CrossRefGoogle Scholar
Serret, A (2001) El Huemul: Fantasma de la Patagonia. Ushuaia, Argentina: Zagier and Urruty.Google Scholar
Søe, MJ, Nejsum, P, Fredensborg, BL and Kapel, CMO (2015) DNA typing of ancient parasite eggs from environmental samples identifies human and animal worm infections in Viking-age settlement. Journal of Parasitology 101, 5764.CrossRefGoogle ScholarPubMed
Søe, MJ, Nejsum, P, Seersholm, FV, Fredensborg, BL, Habraken, R, Haase, K, Hald, MM, Simonsen, R, Højlund, F, Blanke, L and Merkyte, I (2018) Ancient DNA from latrines in Northern Europe and the Middle East (500 BC±1700 AD) reveals past parasites and diet. PLoS ONE 13, e0195481.CrossRefGoogle ScholarPubMed
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google ScholarPubMed
World Health Organization (2013) Sustaining the Drive to Overcome the Global Impact of Neglected Tropical Diseases. Geneva: World Health Organization, WHO Headquarters, 138 pp.Google Scholar
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

First report of pre-Hispanic Fasciola hepatica from South America revealed by ancient DNA
Available formats

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

First report of pre-Hispanic Fasciola hepatica from South America revealed by ancient DNA
Available formats

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

First report of pre-Hispanic Fasciola hepatica from South America revealed by ancient DNA
Available formats

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *