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Molecular identification of cryptic cysticercosis: Taenia ovis krabbei in wild intermediate and domestic definitive hosts

Published online by Cambridge University Press:  28 March 2017

N. Formenti
Affiliation:
Department of Veterinary Medicine, Università degli Studi di Milano, via Celoria 10, 20133 Milan, Italy Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna ‘Bruno Ubertini’ (IZSLER), Department of Bergamo, via Rovelli 53, I-24100 Bergamo, Italy
M. Chiari
Affiliation:
Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna ‘Bruno Ubertini’, Department of Brescia, via Bianchi 7/9, 25124 Brescia, Italy
T. Trogu
Affiliation:
Department of Veterinary Medicine, Università degli Studi di Milano, via Celoria 10, 20133 Milan, Italy
A. Gaffuri
Affiliation:
Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna ‘Bruno Ubertini’ (IZSLER), Department of Bergamo, via Rovelli 53, I-24100 Bergamo, Italy
C. Garbarino
Affiliation:
Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna ‘Bruno Ubertini’, Department of Piacenza, strada della Faggiola 1, 29027 Gariga di Podenzano (PC), Italy
M.B. Boniotti
Affiliation:
Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna ‘Bruno Ubertini’, Department of Brescia, via Bianchi 7/9, 25124 Brescia, Italy
C. Corradini
Affiliation:
Veterinary Practitioner, Via Bosco 1, Scandiano (RE), Italy
P. Lanfranchi
Affiliation:
Department of Veterinary Medicine, Università degli Studi di Milano, via Celoria 10, 20133 Milan, Italy
N. Ferrari*
Affiliation:
Department of Veterinary Medicine, Università degli Studi di Milano, via Celoria 10, 20133 Milan, Italy Centro di Ricerca Coordinata Epidemiologia e Sorveglianza Molecolare delle Infezioni, via Celoria 10, 20133 Milan, Italy
*

Abstract

The complex life cycle of taeniids represents an ideal model of a multi-host system. The complexity of these parasites can therefore cover the epidemiological issues of the interface between wild and domestic animals, especially once spatial overlap between wild and domestic definitive and intermediate hosts occurs. Here we use the occurrence of Taenia ovis krabbei in two model areas as an example of this epidemiological complexity. In two contiguous areas in the Italian northern Apennines, two hunted roe deer (Capreolus capreolus) showed numerous cysticerci in the muscles of their whole body and an adult tapeworm was recorded in a semi-stray dog (Canis lupus familiaris). Through molecular typing of the mitochondrial cytochrome c oxidase I (cox1) gene, cysticerci and the adult tapeworm of T. krabbei were identified. Taenia krabbei cysticercosis was recorded for the first time in Italy. Although the role of dogs in the parasite's life cycle emerges, the overlap between wild and domestic definitive hosts and the increase of wild population densities raise concerns about the temporal (old or new) introduction and the spread of this parasite by one of these canid species (wolf (Canis lupus) or dog). Although T. krabbei is not a public health issue, economic concerns emerged for hunters and meat producers, related to the damage of carcasses by cysticerci. Therefore, there is a need to evaluate the spread of T. krabbei in the intermediate and definitive host populations, and to ensure the relevant sanitary education for hunters in order to avoid practices that could favour the spread and maintenance of its life cycle.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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References

Al-Sabi, M.N.S., Chriél, M., Holm, E., Jensen, T.K., Ståhl, M. & Enemark, H.L. (2013) Reappearance of Taenia ovis krabbei muscle cysts in a roe deer (Capreolus capreolus) in Denmark after 60+ years. Veterinary Parasitology 196, 225229.Google Scholar
Bagrade, G., Kirjušina, M., Vismanis, K. & Ozoliņš, J. (2009) Helminth parasites of the wolf Canis lupus from Latvia. Journal of Helminthology 83, 6368.Google Scholar
Bowles, J., Blair, D. & McManus, D.P. (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165174.Google Scholar
Cantó, G.J., García, M.P., García, A., Guerrero, M.J. & Mosqueda, J. (2011) The prevalence and abundance of helminth parasites in stray dogs from the city of Queretaro in central Mexico. Journal of Helminthology 85, 263269.Google Scholar
Chilton, N.B., O'Callaghan, M.G., Beveridge, I. & Andrews, R.H. (2007) Genetic markers to distinguish Moniezia expansa from M. benedeni (Cestoda: Anoplocephalidae) and evidence of the existence of cryptic species in Australia. Parasitology Research 100, 11871192.Google Scholar
Di Cerbo, A.R., Manfredi, M.T., Trevisiol, K., Bregoli, M., Ferrari, N., Pirinesi, F. & Bazzoli, S. (2008) Intestinal helminth communities of the red fox (Vulpes vulpes L.) in the Italian Alps. Acta Parasitologica 53, 302311.Google Scholar
Flueck, W.T. & Jones, A. (2006) Potential existence of a sylvatic cycle of Taenia ovis krabbei in Patagonia, Argentina. Veterinary Parasitology 135, 381383.Google Scholar
Formenti, N., Gaffuri, A., Trogu, T., Viganò, R., Ferrari, N. & Lanfranchi, P. (2016) Spread and genotype of Toxoplasma gondii in naturally infected alpine chamois (Rupicapra r. rupicapra). Parasitology Research 115, 21152120.Google Scholar
Galimberti, A., Romano, D.F., Genchi, M., Paoloni, D., Vercillo, F., Bizzarri, L., Sassera, D., Bandi, C., Genchi, C., Ragni, B. & Casiraghi, M. (2012) Integrative taxonomy at work: DNA barcoding of taeniids harboured by wild and domestic cats. Molecular Ecology Resources 12, 403413.Google Scholar
Gasser, R.B., Zhu, X. & McManus, D.P. (1999) NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda). International Journal for Parasitology 29, 19651970.Google Scholar
Godfroid, J. (2002) Brucellosis in wildlife. Scientific and Technical Review of the Office International des Epizooties (Paris) 21, 277286.Google Scholar
Goldová, M., Tóth, Š., Letková, V., Mojžišová, J., Kožarová, I. & Pomfy, M. (2008) Comparison of the histological methods in the diagnostic of deer cysticercosis. Helminthologia 45, 121125.Google Scholar
Gori, F., Armua-Fernandez, M.T., Milanesi, P., Serafini, M., Magi, M., Deplazes, P. & Macchioni, F. (2015) The occurrence of taeniids of wolves in Liguria (northern Italy). International Journal for Parasitology: Parasites and Wildlife 4, 252255.Google ScholarPubMed
Gortázar, C., Ferroglio, E., Höfle, U., Frölich, K. & Vicente, J. (2007) Diseases shared between wildlife and livestock: a European perspective. European Journal of Wildlife Research 53, 241256.Google Scholar
Guberti, V., Stancampiano, L. & Francisci, F. (1993) Intestinal helminth parasite community in wolves (Canis lupus) in Italy. Parassitologia 35, 5965.Google ScholarPubMed
Guberti, V., Stancampiano, L. & Ferrari, N. (2014) Surveillance, monitoring and surveys of wildlife diseases: a public health and conservation approach. Hystrix, the Italian Journal of Mammalogy 25, 38.Google Scholar
Haukisalmi, V., Lavikainen, A., Laaksonen, S. & Meri, S. (2011) Taenia arctos n. sp. (Cestoda: Cyclophyllidea: Taeniidae) from its definitive (brown bear Ursus arctos Linnaeus) and intermediate (moose/elk Alces spp.) hosts. Systematic Parasitology 80, 217230.Google Scholar
Haydon, D.T., Cleaveland, S., Taylor, L.H. & Laurenson, M.K. (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8, 14681473.Google ScholarPubMed
Hoberg, E.P. (2002) Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes and Infection 4, 859866.Google Scholar
Laaksonen, S. & Paulsen, P. (2015) Hunting hygiene. Wageningen, Wageningen Academic Publishers.Google Scholar
Lavikainen, A., Haukisalmi, V., Lehtinen, M.J., Laaksonen, S., Holmström, S., Isomursu, M., Oksanen, A. & Meri, S. (2010) Mitochondrial DNA data reveal cryptic species within Taenia krabbei . Parasitology International 59, 290293.Google Scholar
Lavikainen, A., Laaksonen, S., Beckmen, K., Oksanen, A., Isomursu, M. & Meri, S. (2011) Molecular identification of Taenia spp. in wolves (Canis lupus), brown bears (Ursus arctos) and cervids from North Europe and Alaska. Parasitology International 60, 289295.Google Scholar
Lavikainen, A., Haukisalmi, V., Deksne, G., Holmala, K., Lejeune, M., Isomursu, M., Jokelainen, P., Näreaho, A., Laakkonen, J., Hoberg, E.P. & Sukura, A. (2013) Molecular identification of Taenia spp. in the Eurasian lynx (Lynx lynx) from Finland. Parasitology 140, 653662.Google Scholar
Letková, V., Lazar, P., Soroka, J., Goldová, M. & Čurlík, J. (2008) Epizootiology of game cervid cysticercosis. Natura Croatica 17, 311318.Google Scholar
Loos-Frank, B. (2000) An up-date of Verster's (1969) ‘Taxonomic revision of the genus Taenia Linnaeus’ (Cestoda) in table format. Systematic Parasitology 45, 155183.CrossRefGoogle Scholar
Malpica, J.M., Sacristán, S., Fraile, A. & García-Arenal, F. (2006) Association and host selectivity in multi-host pathogens. PLoS ONE 1, e41. doi:10.1371/journal.pone.0000041.Google Scholar
McCormack, R.K. & Allen, L.J.S. (2007) Disease emergence in multi-host epidemic models. Mathematical Medicine and Biology 24, 1734.Google Scholar
Miller, R.S., Farnsworth, M.L. & Malmberg, J.L. (2013) Diseases at the livestock–wildlife interface: status, challenges, and opportunities in the United States. Preventive Veterinary Medicine 110, 119132.Google Scholar
Moniez, R. (1879) Note sur le Taenia krabbei, espèce nouvelle de Taenia armé. Bulletin Scientifique du Département du Nord et des Pays Voisins 2, 61163.Google Scholar
Morgan, E.R., Milner-Gulland, E.J., Torgerson, P.R. & Medley, G.F. (2004) Ruminating on complexity: macroparasites of wildlife and livestock. Trends in Ecology & Evolution 19, 181188 Google Scholar
Murai, É. & Sugár, L. (1979) Taeniid species in Hungary (Cestoda, Taeniidae). I. Cysticercosis, Coenurosis and Hydatidosis. Parasitologia Hungarica 12, 4152.Google Scholar
Nadler, S.A. & Pérez-Ponce de León, G. (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 16881709.Google Scholar
Otranto, D., Cantacessi, C., Dantas-Torres, F., Brianti, E., Pfeffer, M., Genchi, C., Guberti, V., Capelli, G. & Deplazes, P. (2015) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: Helminths and arthropods. Veterinary Parasitology 213, 2437.Google Scholar
Perkins, S.L. (2000) Species concepts and malaria parasites: detecting a cryptic species of Plasmodium . Proceedings of the Royal Society of London B 267, 23452350.Google Scholar
Poulin, R. (2001) Interactions between species and the structure of helminth communities. Parasitology 122, S3S11.Google Scholar
Poulin, R. (2011) Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241244.Google Scholar
Priemer, J., Krone, O. & Schuster, R. (2002) Taenia krabbei (Cestoda: Cyclophyllidea) in Germany and its delimitation from T. ovis . Zoologische Anzeige 241, 333337.Google Scholar
Renwick, A.R., White, P.C.L. & Bengis, R.G. (2007) Bovine tuberculosis in southern African wildlife: a multi-species host–pathogen system. Epidemiology and Infection 135, 529540.Google Scholar
Sawyer, T.W., Cowgill, L.M. & Andersen, F.L. (1976) Helminth parasites of cats and dogs from central Utah. The Great Basin Naturalist 36, 471474.Google Scholar
Turchetto, S., Obber, F., Permunian, R., Vendrami, S., Lorenzetto, M., Ferré, N., Stancampiano, L., Rossi, L. & Citterio, C.V. (2014) Spatial and temporal explorative analysis of sarcoptic mange in Alpine chamois (Rupicapra r. rupicapra). Hystrix, the Italian Journal of Mammalogy 25, 2530.Google Scholar
Willingham, A.L., Ockens, N.W., Kapel, C.M.O. & Monrad, J. (1996) A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. Journal of Helminthology 70, 259263.Google Scholar
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