Abstract
Recent surveys at slaughterhouses confirmed the presence of three different species of Echinococcus granulosus sensu lato in France: E. granulosus sensu stricto, E. ortleppi, and E. canadensis G6/7. The latter species was only identified on the French Mediterranean island of Corsica, with a high prevalence in pigs and wild boar. In order to investigate the life cycle of E. canadensis in this region, dog feces were collected in 31 municipalities, mainly from individual kennels. The analysis of fecal samples from 259 dogs by multiplex real-time PCR shows no infection by E. granulosus sensu stricto, but three dogs were infected by E. canadensis G6/7. Genetic analyses of mitochondrial genes (cox1, nad1, nad3, atp6) revealed in two dogs a haplotype previously identified in pigs. The third dog was infected by a new haplotype differing only from the two others from dogs by two mutations in the nad3 gene. This latter haplotype is genetically closer to those identified in pigs rather than those from wild boars. Analysis of questionnaires completed by the owners revealed that the sampled dog population was almost exclusively composed of hunting dogs that had been infrequently dewormed. Most of the owners (78%) leave carcasses of hunter-harvested wild boar in close proximity to their dogs. Nevertheless, genetic results seem to indicate that the three dogs were infected due to their consumption of a pig’s infected viscera following home slaughtering. This study confirms the role of dogs as definitive hosts of E. canadensis G6/7 in Corsica. Further molecular studies, notably in human cases, are needed to assess the zoonotic impact of E. canadensis G6/7 in this region.
This is a preview of subscription content, log in via an institution to check access.
References
Addy F, Wassermann M, Kagendo D, Ebi D, Zeyhle E, Elmahdi IE, Umhang G, Casulli A, Harandi MF, Aschenborn O, Kern P, Mackenstedt U, Romig T (2017) Genetic differentiation of the G6/7 cluster of Echinococcus canadensis based on mitochondrial marker genes. Int J Parasitol 47(14):923–931. https://doi.org/10.1016/j.ijpara.2017.06.003
Auvray F, Lecureuil C, Dilasser F, Tache J, Derzelle S (2009) Development of a real-time PCR assay with an internal amplification control for the screening of Shiga toxin-producing Escherichia coli in foods. Lett Appl Microbiol 48(5):554–559. https://doi.org/10.1111/j.1472-765X.2009.02561.x
Brunetti E, Kern P, Vuitton DA (2010) Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114(1):1–16. https://doi.org/10.1016/j.actatropica.2009.11.001
Bruzinskaite R, Sarkunas M, Torgerson PR, Mathis A, Deplazes P (2009) Echinococcosis in pigs and intestinal infection with Echinococcus spp. in dogs in southwestern Lithuania. Vet Parasitol 160(3–4):237–241. https://doi.org/10.1016/j.vetpar.2008.11.011
Budke CM, Deplazes P, Torgerson PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12(2):296–303. https://doi.org/10.3201/eid1202.050499
Carmena D, Cardona GA (2014) Echinococcosis in wild carnivorous species: epidemiology, genotypic diversity, and implications for veterinary public health. Vet Parasitol 202(3–4):69–94. https://doi.org/10.1016/j.vetpar.2014.03.009
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.xISTEX
Deschiens R (1960) Considérations épidémiologiques et sanitaires sur l'hydatidose humaine dans le bassin méditérranéen et en Corse. Bull Soc Pathol Exot 53:971–990
Grenouillet F, Umhang G, Arbez-Gindre F, Mantion G, Delabrousse E, Millon L, Boué F (2014) Echinococcus ortleppi infections in humans and cattle, France. Emerg Infect Dis 20(12):2100–2102. https://doi.org/10.3201/eid2012.140641
Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JDF, Dinkel A, Sako Y, Mackenstedt U, Romig T, Ito A (2008) Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. Int J Parasitol 38(7):861–868. https://doi.org/10.1016/j.ijpara.2007.10.013
Laurimäe T, Kinkar L, Moks E, Romig T, Omer RA, Casulli A, Umhang G, Bagrade G, Irshadullah M, Sharbatkhori M, Mirhendi H, Ponce-Gordo F, Soriano SV, Varcasia A, Rostami-Nejad M, Andresiuk V, Saarma U (2018) Molecular phylogeny based on six nuclear genes suggests that Echinococcus granulosus sensu lato genotypes G6/G7 and G8/G10 can be regarded as two distinct species. Parasitology in press 145:1929–1937. https://doi.org/10.1017/S0031182018000719
Lymbery AJ, Jenkins EJ, Schurer JM, Thompson RCA (2015) Echinococcus canadensis, E. borealis, and E. intermedius. What’s in a name? Trends Parasitol 31(1):23–29. https://doi.org/10.1016/j.pt.2014.11.003
Mackenstedt U, Jenkins D, Romig T (2015) The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. Int J Parasitol Parasites Wildl 4(1):71–79. https://doi.org/10.1016/j.ijppaw.2015.01.006
McManus DP (2013) Current status of the genetics and molecular taxonomy of Echinococcus species. Parasitology 140(13):1617–1623. https://doi.org/10.1017/S0031182013000802
Múrias dos Santos A, Cabezas MP, Tavares AI, Xavier R, Branco M (2016) tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics 32(4):627–628. https://doi.org/10.1093/bioinformatics/btv636
Nakao M, McManus DP, Schantz PM, Craig PS, Ito A (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134(Pt 5):713–722. https://doi.org/10.1017/S0031182006001934ISTEX
Nakao M et al (2013) Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 140(3):1625–1636. https://doi.org/10.1017/S0031182013000565
Richomme C (2009) Epidémiologie de zoonoses du sanglier (Sus scrofa) dans un milieu méditerranéen insulaire, la Corse Doctorat d'Université - Spécialité Ecologie, Université Blaise Pascal de Clermont-Ferrand
Soulé C, Fabien JF, Maillot E (1989) Enquête échinococcose-hydatidose. DGAL - Brigade Nationale d'Enquêtes Vétérinaires - CNEVA - Unité Parasitologie, Maisons-Alfort, 173 p
Thompson RCA (2008) The taxonomy, phylogeny and transmission of Echinococcus. Exp Parasitol 119(4):439–446. https://doi.org/10.1016/j.exppara.2008.04.016
Trachsel D, Deplazes P, Mathis A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134(6):911–920. https://doi.org/10.1017/S0031182007002235ISTEX
Umhang G, Richomme C, Boucher JM, Hormaz V, Boué F (2013) Prevalence survey and first molecular characterization of Echinococcus granulosus in France. Parasitol Res 112(4):1809–1812. https://doi.org/10.1007/s00436-012-3245-7ISTEX
Umhang G, Richomme C, Hormaz V, Boucher JM (2014) Pigs and wild boar in Corsica harbor Echinococcus canadensis G6/7 at levels of concern for public health and local economy. Acta Trop 133:64–68. https://doi.org/10.1016/j.actatropica.2014.02.005
Van Cauteren D, Millon L, De Valk H, Grenouillet F (2016) Retrospective study of human cystic echinococcosis over the past decade in France, using a nationwide hospital medical information database. Parasitol Res 115(11):4261–4265. https://doi.org/10.1007/s00436-016-5204-1
Varcasia A, Canu S, Lightowlers MW, Scala A, Garippa G (2006) Molecular characterization of Echinococcus granulosus strains in Sardinia. Parasitol Res 98(3):273–277. https://doi.org/10.1007/s00436-005-0059-xISTEX
Yanagida T, Lavikainen A, Hoberg EP, Konyaev S, Ito A, Sato MO, Zaikov VA, Beckmen K, Nakao M (2017) Specific status of Echinococcus canadensis (Cestoda: Taeniidae) inferred from nuclear and mitochondrial gene sequences. Int J Parasitol 47(14):971–979. https://doi.org/10.1016/j.ijpara.2017.07.001
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Christoph G. Grevelding
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Grech-Angelini, S., Richomme, C., Peytavin de Garam, C. et al. Identification and molecular characterization of Echinococcus canadensis G6/7 in dogs from Corsica, France. Parasitol Res 118, 1313–1319 (2019). https://doi.org/10.1007/s00436-019-06261-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06261-6