Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-22T22:12:43.390Z Has data issue: false hasContentIssue false
  • English
  • Français

Unique genetic structure of the human tapeworm Dibothriocephalus latus from the Alpine lakes region – a successful adaptation?

Published online by Cambridge University Press:  16 May 2022

Alžbeta Radačovská Open the ORCID record for Alžbeta Radačovská [Opens in a new window] ,
Eva Čisovská Bazsalovicsová Open the ORCID record for Eva Čisovská Bazsalovicsová [Opens in a new window] ,
Katarína Šoltys Open the ORCID record for Katarína Šoltys [Opens in a new window] ,
Jan Štefka Open the ORCID record for Jan Štefka [Opens in a new window] ,
Gabriel Minárik ,
Andrea Gustinelli ,
Julia K. Chugunova Open the ORCID record for Julia K. Chugunova [Opens in a new window]  and
Ivica Králová-Hromadová Open the ORCID record for Ivica Králová-Hromadová [Opens in a new window]
Alžbeta Radačovská
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 04001 Košice, Slovakia
Eva Čisovská Bazsalovicsová
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 04001 Košice, Slovakia
Katarína Šoltys
Affiliation:
Department of Microbiology and Virology, Faculty of Natural Sciences, Comenius University in Bratislava, Ilkovičova 6, 84215 Bratislava, Slovakia
Jan Štefka
Affiliation:
Biology Centre CAS, Institute of Parasitology, Branišovská 31, 37005 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 1760, 37005 České Budějovice, Czech Republic
Gabriel Minárik
Affiliation:
Medirex, a.s., Galvaniho 17/C, P.O. Box 143, 82016 Bratislava, Slovakia
Andrea Gustinelli
Affiliation:
Department of Veterinary Medical Sciences, University of Bologna, Via Tolara di Sopra 50, 40064 Ozzano Emilia, BO, Italy
Julia K. Chugunova
Affiliation:
Krasnoyarsk Branch of the Russian Federal Research Institute of Fisheries and Oceanography ‘VNIRO’, Parizhskoi Kommuny, 33, 660097 Krasnoyarsk, Russia
Ivica Králová-Hromadová*
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 04001 Košice, Slovakia
*
Author for correspondence: Ivica Králová-Hromadová, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Dibothriocephalus latus is the most frequent causative agent of fish-borne zoonosis (diphyllobothriosis) in Europe, where it is currently circulating mainly in the Alpine lakes region (ALR) and Russia. Three mitochondrial genes (cox1, cob and nad3) and 6 microsatellite loci were analysed to determine how is the recently detected triploidy/parthenogenesis in tapeworms from ALR displayed at the DNA level. A geographically distant population from the Krasnoyarsk Reservoir in Russia (RU-KR) was analysed as a comparative population. One or 2 alleles of each microsatellite locus was detected in plerocercoids from RU-KR, corresponding to the microsatellite pattern of a diploid organism. In contrast, 1–3 alleles were observed in tapeworms from ALR, in accordance with their triploidy. The high diversity of mitochondrial haplotypes in D. latus from RU-KR implied an original and relatively stable population, but the identical structure of mitochondrial genes of tapeworms from ALR was probably a consequence of a bottleneck typical of introduced populations. These results indicated that the diploid/sexually reproducing population from RU-KR was ancestral, located within the centre of the distribution of the species, and the triploid/parthenogenetically reproducing subalpine population was at the margin of the distribution. The current study revealed the allelic structure of the microsatellite loci in the triploid tapeworm for the first time.

Keywords

Asexual populationDiphyllobothriosisfish-borne zoonosishaplotypesmicrosatellitesmitochondrial DNAparthenogenesistriploid tapeworms
Type
Research Article
Information
Parasitology , Volume 149 , Issue 8 , July 2022 , pp. 1106 - 1118
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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.)

Footnotes

*

Equal contribution of both authors.

References

Anneville, O, Molinero, JC, Souissi, S, Balvay, G and Gerdeaux, D (2007) Long-term changes in the copepod community of lake Geneva. Journal of Plankton Research 29, 49–59.CrossRefGoogle Scholar
Bagrade, G, Králová-Hromadová, I, Bazsalovicsová, E, Radačovská, A and Kołodziej-Sobocińska, M (2021) The first records of Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidae), a causative agent of human sparganosis, in Latvian wildlife. Parasitology Research 120, 365–371.CrossRefGoogle Scholar
Bazin, E, Glémin, S and Galtier, N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312, 570–572.CrossRefGoogle Scholar
Bazsalovicsová, E, Koleničová, A, Králová-Hromadová, I, Minárik, G, Šoltys, K, Kuchta, R and Štefka, J (2018) Development of microsatellite loci in zoonotic tapeworm Dibothriocephalus latus (Linnaeus, 1758), Lühe, 1899 (syn. Diphyllobothrium latum) using microsatellite library screening. Molecular and Biochemical Parasitology 225, 1–3.CrossRefGoogle ScholarPubMed
Bazsalovicsová, E, Minárik, G, Šoltys, K, Radačovská, A, Kuhn, JA, Karlsbakk, E, Skírnisson, K and Králová-Hromadová, I (2020) Development of 14 microsatellite markers for zoonotic tapeworm Dibothriocephalus dendriticus (Cestoda: Diphyllobothriidea). Genes 11, 782.CrossRefGoogle Scholar
Bielat, I, Legierko, M and Sobecka, E (2015) Species richness and diversity of the parasites of two predatory fish species – perch (Perca fluviatilis Linnaeus, 1758) and zander (Sander lucioperca Linnaeus, 1758) from the Pomeranian Bay. Annals of Parasitology 61, 85–92.Google ScholarPubMed
Bombarová, M and Špakulová, M (2015) New chromosome characteristics of the monozoic tapeworm Caryophyllaeus laticeps (Cestoda, Caryophyllidea). Helminthologia 52, 336–340.CrossRefGoogle Scholar
Bouvier, G, Hörning, B and Matthey, G (1963) La diphyllobothriose (Bothriocéphalose) en Suisse, plus spécialement en Suisse romande. Bulletin de l'Académie Suisse des Sciences Medicales 19, 364–374 (in French).Google Scholar
Chugunova, JK, Ronzhina, TY and Syromyatnikov, AA (2020) The contribution of perch (Perca fluviatilis L. 1758) to maintaining the diphyllobothriasis focus in the Krasnoyarsk reservoir and the Yenisei river. Journal of Siberian Federal University Biology 13, 297–309.CrossRefGoogle Scholar
Čisovská Bazsalovicsová, E, Radačovská, A, Lavikainen, A, Kuchta, R and Králová-Hromadová, I (2022) Genetic interrelationships of Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidea), the causative agent of sparganosis in Europe. Parasite 29, 8.CrossRefGoogle Scholar
Clement, M, Posada, D and Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
Dommelier, S, Bentrad, S, Paicheler, JC, Pétrequin, P and Bouchet, F (1998) Parasitoses liées à l'alimentation chez les populations néolithiques du lac de Chalain (Jura, France). Anthropozoologica 27, 41–49 (in French).Google Scholar
Dugarov, ZN and Pronin, NM (2017) Faunal diversity and dynamics of species richness and dominance of parasite communities in age series of the perch (Perca fluviatilis). Russian Journal of Ecology 48, 38–44.CrossRefGoogle Scholar
Dupouy-Camet, J and Peduzzi, R (2004) Current situation of human diphyllobothriasis in Europe. Eurosurveillance 9, 31–35.CrossRefGoogle ScholarPubMed
Dupouy-Camet, J, Haidar, M, Dei-Cas, E, Yera, H, Espinat, L, Benmostefa, A, Guillard, J and Aliouat-Denis, CM (2015) Prévalence de l'infestation par Diphyllobothrium latum de différents poissons des lacs Léman, du Bourget et d'Annecy et évaluation de l'incidence des cas humains auprès des laboratoires d'analyse médicale de la région (2011–2013). Bulletin épidémiologique, santé animale, et alimentation 67, 2–5 (in French).Google Scholar
Flammer, PG, Dellicour, S, Preston, SG, Rieger, D, Warren, S, Tan, CKW, Nicholson, R, Přichystalová, R, Bleicher, N, Wahl, J, Faria, NR, Pybus, OG, Pollard, M and Smith, AL (2018) Molecular archaeoparasitology identifies cultural changes in the Medieval Hanseatic trading centre of Lübeck. Proceedings of the Royal Society B: Biological Sciences 285, 20180991.CrossRefGoogle ScholarPubMed
Gonçalves, MLC, Araújo, A and Ferreira, LF (2003) Human intestinal parasites in the past: new findings and a review. Memorias do Instituto Oswaldo Cruz 98, 103–118.CrossRefGoogle ScholarPubMed
Górski, P, Zalewski, A and Łakomy, M (2006) Parasites of carnivorous mammals in Białowieża Primeval forest. Wiadomości Parazytologiczne 52, 49–53.Google ScholarPubMed
Górski, P, Zalewski, A, Kazimierczak, K and Kotomski, G (2010) Coproscopical investigations of the European otter (Lutra lutra) from Białowieża Primeval forest. Wiadomości Parazytologiczne 56, 179–180.Google ScholarPubMed
Gouy, M, Guindon, S and Gascuel, O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.CrossRefGoogle ScholarPubMed
Grant, F (1930) Bothriocephalus tapeworms in a sick person. Klinische Wochenschrift 9, 502 (in German).CrossRefGoogle Scholar
Grey, AJ and Mackiewicz, JS (1980) Chromosomes of caryophyllidean cestodes: diploidy, triploidy, and parthenogenesis in Glaridacris catostomi. International Journal for Parasitology 10, 397–407.CrossRefGoogle Scholar
Grove, DI (1990) A History of Human Helminthology. Wallingford, UK: C.A.B. International.Google Scholar
Gustinelli, A, Menconi, V, Prearo, M, Caffara, M, Righetti, M, Scanzio, T, Raglio, A and Fioravanti, ML (2016) Prevalence of Diphyllobothrium latum (Cestoda: Diphyllobothriidae) plerocercoids in fish species from four Italian lakes and risk for the consumers. International Journal of Food Microbiology 235, 109–112.CrossRefGoogle ScholarPubMed
Haak, W, Lazaridis, I, Patterson, N, Rohland, N, Mallick, S, Llamas, B, Brandt, G, Nordenfelt, S, Harney, E, Stewardson, K, Fu, Q, Mittnik, A, Bánffy, E, Economou, C, Francken, M, Friederich, S, Pena, RG, Hallgren, F, Khartanovich, V, Khokhlov, A, Kunst, M, Kuznetsov, P, Meller, H, Mochalov, O, Moiseyev, V, Nicklisch, N, Pichler, SL, Risch, R, Rojo Guerra, MA, Roth, C, Szécsényi-Nagy, A, Wahl, J, Meyer, M, Krause, J, Brown, D, Anthony, D, Cooper, A, Ait, KW and Reich, D (2015) Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211. doi: 10.1038/nature14317.CrossRefGoogle ScholarPubMed
Jackson, Y, Pastore, R, Sudre, P, Loutan, L and Chappuis, F (2007) Diphyllobothrium latum outbreak from marinated raw perch, lake Geneva, Switzerland. Emerging Infectious Diseases 13, 1957–1958.CrossRefGoogle ScholarPubMed
Jenkins, EJ, Castrodale, LJ, de Rosemond, SJ, Dixon, BR, Elmore, SA, Gesy, KM, Hoberg, EP, Polley, L, Schurer, JM, Simard, M and Thompson, RC (2013) Tradition and transition: parasitic zoonoses of people and animals in Alaska, northern Canada, and Greenland. Advances in Parasitology 82, 33–204.CrossRefGoogle ScholarPubMed
Katkar, N (2011) After last glacial maximum: the third migration. Comptes Rendus Palevol 10, 665–678.CrossRefGoogle Scholar
Kondrateva, GP (1961) Some epidemiological questions of diphyllobothriosis in Estonian SSR. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 30, 95–98 (in Russian).Google Scholar
Kondzior, E, Kowalczyk, R, Tokarska, M, Borowik, T, Zalewski, A and Kołodziej-Sobocińska, M (2020) Multispecies reservoir of Spirometra erinaceieuropaei (Cestoda: Diphyllobothridae) in carnivore communities in north-eastern Poland. Parasites & Vectors 10, 560.CrossRefGoogle Scholar
Králová-Hromadová, I, Minárik, G, Bazsalovicsová, E, Mikulíček, P, Oravcová, A, Pálková, L and Hanzelová, V (2015) Development of microsatellite markers in Caryophyllaeus laticeps (Cestoda: Caryophyllidea), monozoic fish tapeworm, using next-generation sequencing approach. Parasitology Research 114, 721–726.CrossRefGoogle Scholar
Králová-Hromadová, I, Radačovská, A, Čisovská Bazsalovicsová, E and Kuchta, R (2021) Ups and downs of infections with the broad fish tapeworm Dibothriocephalus latus in Europe from 1900 to 2020: part I. Advances in Parasitology 114, 75–166.CrossRefGoogle ScholarPubMed
Kuchta, R, Radačovská, A, Bazsalovicsová, E, Viozzi, G, Semenas, L, Arbetman, M and Scholz, T (2019) Host switching of zoonotic broad fish tapeworm (Dibothriocephalus latus) to salmonids, Patagonia. Emerging Infectious Diseases 25, 2156–2158.CrossRefGoogle ScholarPubMed
Lang, C (1989) Eutrophication of Lake Neuchâtel indicated by the oligochaete communities. Hydrobiologia 174, 57–65.CrossRefGoogle Scholar
Ledger, ML, Grimshaw, E, Fairey, M, Whelton, HL, Bull, ID, Ballantyne, R, Knight, M and Mitchell, PD (2019) Intestinal parasites at the Late Bronze age settlement of Must Farm, in the fens of East Anglia, UK (9th century B.C.E.). Parasitology 146, 1583–1594.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
Levron, C, Brunaňská, M and Poddubnaya, LG (2006) Spermatological characters in Diphyllobothrium latum (Cestoda, Pseudophyllidea). Journal of Morphology 267, 1110–1119.CrossRefGoogle Scholar
Lorch, S, Zeuss, D, Brandl, R and Brändle, M (2016) Chromosome numbers in three species groups of freshwater flatworms increase with increasing latitude. Ecology and Evolution 6, 1420–1429.CrossRefGoogle ScholarPubMed
Manca, M, Torretta, B, Comoli, P, Amsinck, SL and Jeppesen, E (2007) Major changes in trophic dynamics in large, deep sub-alpine lake Maggiore from 1940s to 2002: a high resolution comparative palaeo-neolimnological study. Freshwater Biology 52, 2256–2269.CrossRefGoogle Scholar
Meirmans, PG (2020) Genodive version 3.0: easy-to-use software for the analysis of genetic data of diploids and polyploids. Molecular Ecology Resources 20, 1126–1131.CrossRefGoogle ScholarPubMed
Meirmans, PG and Van Tienderen, PH (2004) GenoType and Genodive: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4, 792–794.CrossRefGoogle Scholar
Menconi, V, Pastorino, P, Momo, I, Mugetti, D, Bona, MC, Levetti, S, Tomasoni, M, Pizzul, E, Ru, G, Dondo, A and Prearo, M (2020) Occurrence and spatial distribution of Dibothriocephalus latus (Cestoda: Diphyllobothriidea) in lake Iseo (Northern Italy): an update. International Journal of Environmental Research and Public Health 17, e5070.CrossRefGoogle ScholarPubMed
Menconi, V, Zoppi, S, Pastorino, P, Di Blasio, A, Tedeschi, R, Pizzul, E, Mugetti, D, Tomasoni, M, Dondo, A and Prearo, M (2021) Relationship between the prevalence of Dibothriocephalus latus (Cestoda: Diphyllobothriidea) and the load of Escherichia coli: new findings in a neglected fish-borne parasitic zoonosis. Zoonoses and Public Health 68, 965–972.CrossRefGoogle Scholar
Nei, M (1972) Genetic distance between populations. American Naturalist 106, 283–292.CrossRefGoogle Scholar
Nesbø, CL, Fossheim, T, Vøllestad, LA and Jakobsen, KS (1999) Genetic divergence and phylogeographic relationships among European perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization. Molecular Ecology 8, 1387–1404.CrossRefGoogle ScholarPubMed
Nicoulaud, J, Yéra, H and Dupouy-Camet, J (2005) Prévalence de l'infestation par Diphyllobothrium latum, L., 1758 chez les perches (Perca fluviatilis) du lac Léman. Parasite 12, 362–364.CrossRefGoogle Scholar
Ohari, Y, Hayashi, K, Takashima, Y and Itagaki, T (2021 a) Do aspermic (parthenogenetic) Fasciola forms have the ability to reproduce their progeny via parthenogenesis? Journal of Helminthology 95, E36.CrossRefGoogle ScholarPubMed
Ohari, Y, Matsuo, K, Yoshida, A, Nonaka, N, Sato, H and Itagaki, T (2021 b) Genetic diversity and population structure analyses based on microsatellite DNA of parthenogenetic Fasciola flukes obtained from cattle and sika deer in Japan. Parasitology Research 120, 1341–1350.CrossRefGoogle ScholarPubMed
Orosová, M, Marková, A, Provazníková, I, Oros, M, Radačovská, A, Čadková, Z and Marec, F (2021) Molecular cytogenetic analysis of a triploid population of the human broad tapeworm, Dibothriocephalus latus (Diphyllobothriidea). Parasitology 148, 787–797.CrossRefGoogle Scholar
Otto, SP and Whitton, J (2000) Polyploid incidence and evolution. Annual Review of Genetics 34, 401–437.CrossRefGoogle ScholarPubMed
Peakall, R and Smouse, PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.CrossRefGoogle ScholarPubMed
Petkevičiūtė, R (1996) A chromosome study in the progenetic cestode Cyathocephalus truncatus (Cestoda: Spathebothriidea). International Journal for Parasitology 26, 1211–1216.CrossRefGoogle Scholar
Petkevičiūtė, R and Kuperman, BI (1992) Karyological investigations of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea). Folia Parasitologica 39, 115–121.Google Scholar
Pongratz, N, Storhas, M, Carranza, S and Michiels, NK (2003) Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations. BMC Evolutionary Biology 3, 23–37.CrossRefGoogle ScholarPubMed
Radačovská, A, Bazsalovicsová, E, Blasco Costa, I, Orosová, M, Gustinelli, A and Králová-Hromadová, I (2019 a) Occurrence of Dibothriocephalus latus in European perch from Alpine lakes, an important focus of diphyllobothriosis in Europe. Revue Suisse de Zoologie 126, 219–225.Google Scholar
Radačovská, A, Bazsalovicsová, E and Králová-Hromadová, I (2019 b) Results on search for the broad fish tapeworm Dibothriocephalus latus (Linnaeus, 1758), (syn. Diphyllobothrium latum) (Cestoda: Diphyllobothriidea), in the Danube river. Helminthologia 56, 256–260.CrossRefGoogle Scholar
Radačovská, A, Bazsalovicsová, E, Linowska, A, Kołodziej-Sobocińska, M and Králová-Hromadová, I (2019 c) Endohelminths of European perch (Perca fluviatilis) from selected localities in Poland with an emphasis on search of the broad fish tapeworm Dibothriocephalus latus. Acta Parasitologica 64, 544–550.CrossRefGoogle ScholarPubMed
Rossolovskaya, AA (1968) Diphyllobothriosis in the Saratov Region. In Prokopenko, LI, Semenova, NE, Pov, NN, Leikina, ES and Khodakova, VI, (eds). Diphyllobothriosis. Moscow, Russia: Ministry of Health of the USSR. Institute of Medical Parasitology and Tropical Medicine Marinovsky M.E.I., pp. 131–133 (in Russian).Google Scholar
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299–3302.CrossRefGoogle ScholarPubMed
Rumyantsev, EA (1984) History of the formation of parasite fauna of fish in water reservoirs in the European circle of the Arctic Ocean province. Folia Parasitologica 31, 5–10.Google Scholar
Rumyantsev, EA (2007) Fish Parasites in Lakes of the European North. Petrozavodsk: PetrGU (in Russian).Google Scholar
Spötl, C, Koltai, G, Jarosch, AH and Cheng, H (2021) Increased autumn and winter precipitation during the Last Glacial Maximum in the European Alps. Nature Communications 12, 1839.CrossRefGoogle Scholar
Štefka, J, Gilleard, JS, Grillo, V and Hypša, V (2007) Isolation and characterization of microsatellite loci in the tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea). Molecular Ecology Notes 7, 794–796.CrossRefGoogle Scholar
Štefka, J, Hypša, V and Scholz, T (2009) Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology 18, 1187–1206.CrossRefGoogle Scholar
Szczęsna, J, Popiołek, M, Schmidt, K and Kowalczyk, R (2008). Coprological study on helminth fauna in Eurasian lynx (Lynx lynx) from the Białowieza Primeval forest in eastern Poland. The Journal of Parasitology 94, 981–984.CrossRefGoogle Scholar
Torres, P and Yera, H (2018) Diphyllobothriidae. In Rose, JB and Jiménez-Cisneros, B (eds), Global Water Pathogen Project. Part 3: Specific Excreted Pathogens: Environmental and Epidemiology Aspects. MI, USA: Michigan State University, pp. 1–61. doi: 10.14321/waterpathogens.38.Google Scholar
Vishegorodtsev, AA, Kosmakov, IV, Anufrieva, TN and Kuznetsova, OV (2005) The Krasnoyarsk Reservoir. Novosibirsk: Nauka.Google Scholar
von Bonsdorff, B (1977) Diphyllobothriasis in Man. New York: Academic Press.Google Scholar
von Bonsdorff, CH and Telkkä, A (1965) The flagellar structure of the flame cell in fish tapeworm (Diphyllobothrium latum). Zeitschrift für Zellforschung und Mikroskopische Anatomie 70, 169–179.CrossRefGoogle Scholar
Whitfield, PJ and Evans, NA (1983) Parthenogenesis and asexual multiplication among parasitic platyhelminths. Parasitology 86, 121–160.CrossRefGoogle ScholarPubMed
Wicht, B (2008) Ecology, Epidemiology and Molecular Identification of the Genus Diphyllobothrium Cobbold, 1858 in the Sub-Alpine Region (Thesis). University of Geneva, Geneva, Switzerland. Available at https://archive-ouverte.unige.ch/unige:1699.Google Scholar
Wicht, B, de Marval, F and Peduzzi, R (2007) Diphyllobothrium nihonkaiense (Yamane et al., 1986) in Switzerland: first molecular evidence and case reports. Parasitology International 56, 195–199.CrossRefGoogle ScholarPubMed
Wicht, B, Ruggeri-Bernardi, N, Yanagida, T, Nakao, M, Peduzzi, R and Ito, A (2010 a) Inter- and intra-specific characterization of tapeworms of the genus Diphyllobothrium (Cestoda: Diphyllobothriidea) from Switzerland, using nuclear and mitochondrial DNA targets. Parasitology International 59, 35–39.CrossRefGoogle ScholarPubMed
Wicht, B, Yanagida, T, Scholz, T, Ito, A, Jiménez, JA and Brabec, J (2010 b) Multiplex PCR for differential identification of broad tapeworms (Cestoda: Diphyllobothrium) infecting humans. Journal of Clinical Microbiology 48, 3111–3116.CrossRefGoogle ScholarPubMed
Wikgren, BJP and Gustafsson, MKS (1965) The chromosomes of somatic cells of three Diphyllobothrium species, with notes on the mode of cell division. Acta Academiae Abonensis 25, 1–12.Google Scholar
Yera, H, Estran, C, Delaunay, P, Gari-Toussaint, M, Dupouy-Camet, J and Marty, P (2006) Putative Diphyllobothrium nihonkaiense acquired from a Pacific salmon (Oncorhynchus keta) eaten in France; genomic identification and case report. Parasitology International 55, 45–49.CrossRefGoogle ScholarPubMed
Yera, H, Nicoulaud, J and Dupouy-Camet, J (2008) Use of nuclear and mitochondrial DNA PCR and sequencing for molecular identification of Diphyllobothrium isolates potentially infective for humans. Parasite 15, 402–407.CrossRefGoogle ScholarPubMed
Zottler, EM, Bieri, M, Basso, W and Schnyder, M (2019) Intestinal parasites and lungworms in stray, shelter and privately owned cats of Switzerland. Parasitology International 69, 75–81.CrossRefGoogle ScholarPubMed
Supplementary material: File

Radačovská et al. supplementary material

Figure S1
Download Radačovská et al. supplementary material(File)
File 65.6 KB
Supplementary material: File

Radačovská et al. supplementary material

Table S1
Download Radačovská et al. supplementary material(File)
File 247.3 KB
Supplementary material: File

Radačovská et al. supplementary material

Table S2
Download Radačovská et al. supplementary material(File)
File 17.3 KB