Abstract
Taenia hydatigena is a cosmopolitan tapeworm that uses canids or felines as definitive hosts, while the larval stage (metacestode), formerly referred to as cysticercus tenuicollis, infects a wide variety of intermediate hosts, in particular ruminants. In the present study, we used partial nucleotide sequences of the cox1 and nad1 genes of T. hydatigena from different animal species to analyse the intraspecies genetic diversity of this economically important parasite. Twenty-four samples of metacestodes or adults of T. hydatigena from infected sheep, chamois, roe deer, fallow deer, wild boar, and dogs from Slovakia were collected and further analysed. Several haplotypes of T. hydatigena were identified with unique mutations that have not been previously recorded in Slovakia. Analysis of nucleotide polymorphism revealed the existence of 9 and 13 haplotypes, with relatively low nucleotide pairwise divergence ranging between 0.3–1.3 and 0.2–1.8% for the Hcox and Hnad haplotypes, respectively. In general, low nucleotide and high haplotype diversities in the overall population of T. hydatigena from the study indicate a high number of closely related haplotypes within the explored population; nucleotide diversity per site was low for cox1 (Pi = 0.00540) and slightly higher for nad1 (Pi = 0.00898). A molecular study confirmed the existence of genetic variation within T. hydatigena isolates from Slovakia. However, further investigations with more samples collected from different intermediate and definitive hosts are required in order to investigate the epidemiological significance of the apparent genetic differences observed in this study.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbas I, El-Alfy E, Janecek-Erfurth E, Strube C (2021) Molecular characterization of Cysticercus tenuicollis isolates from sheep in the Nile Delta, Egypt and a review on Taenia hydatigena infections worldwide. Parasitology 148(8):913–933. https://doi.org/10.1017/S0031182021000536
Alvi MA, Ohiolei JA, Saqib M, Li L, Muhammad N, Tayyab MH, Qamar W, Alvi AA, Wu YD, Li XR, Fu BQ, Yan HB, Jia WZ (2020) Preliminary information on the prevalence and molecular description of Taenia hyatigena isolates in Pakistan based on mitochondrial cox1 gene. Infect Genet Evol 85:104481. https://doi.org/10.1016/j.meegid.2020.104481
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Blažek K, Schramlová J, Hulínská D (1985) Pathology of the migration phase of Taenia hydatigena (Pallas, 1766) larvae. Folia Parasitol 32(2):127–137
Boufana B, Scala A, Lahmar S, Pointing S, Craig PS, Dessì G, Zidda A, Pipia AP, Varcasia A (2015) A preliminary investigation into the genetic variation and population structure of Taenia hydatigena from Sardinia. Italy Vet Parasitol 214(1–2):67–74. https://doi.org/10.1016/j.vetpar.2015.08.003
Bowles J, McManus DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol 23:969–972
Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54(2):165–173
Cengiz G, Yucel Tenekeci G, Bilgen N (2019) Molecular and morphological characterization of Cysticercus tenuicollis in red deer (Cervus elaphus) from Turkey. Acta Parasitol 64(3):652–657. https://doi.org/10.2478/s11686-019-00085-1
Christodoulopoulos G, Theodoropoulos G, Petrakos G (2008) Epidemiological survey of cestode-larva disease in Greek sheep flocks. Vet Parasitol 153:368–373. https://doi.org/10.1016/j.vetpar.2008.02.002
Colwell DD, Dantas-Torres F, Otranto D (2011) Vector-borne parasitic zoonoses: emerging scenarios and new perspectives. Vet Parasitol 182:14–21. https://doi.org/10.1016/j.vetpar.2011.07.012
Corda A, Dessì G, Varcasia A, Carta S, Tamponi C, Sedda G, Scala M, Marchi B, Salis F, Scala E, Pinna Parpaglia ML (2020) Αcute visceral cysticercosis caused by Taenia hydatigena in lambs: ultrasonographic findings. Parasit Vectors 13:568. https://doi.org/10.1186/s13071-020-04439-x
Craig HL, Craig PS (2005) Helminth parasites of wolves (Canis lupus): a species list and an analysis of published prevalence studies in Nearctic and Palaearctic populations. J Helminthol 79(2):95–103. https://doi.org/10.1079/JOH2005828
Filip KJ, Demiaszkiewicz AW (2016) Internal parasitic fauna of elk (Alces alces) in Poland. Acta Parasitol 61:657–664. https://doi.org/10.1515/ap-2016-00922
Filip KJ, Pyziel AM, Jezewski W, Myczka AW, Demiaszkiewicz AW, Laskowski Z (2019) First molecular identification of Taenia hydatigena in wild ungulates in Poland. EcoHealth 16:161–170. https://doi.org/10.1007/s10393-019-01392-9
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925. https://doi.org/10.1093/genetics/147.2.915
Gasser RB, Zhu X, McManus DP (1999) NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda). Int Parasitol 29:1965–1970
Gomez-Puerta L, Pacheco J, Gonzales-Viera O, Gonzalez AE (2015) The taruca (Hippocamelus antisensis) and the red brocket deer (Mazama americana) as intermediate hosts of Taenia hydatigena in Peru, morphological and molecular evidence. Vet Parasitol 212:465–468. https://doi.org/10.1016/j.vetpar.2015.08.0044
Harandi M, Moazezi S, Saba M, Grimm F, Kamyabi H, Sheikhza-Deh F, SharifI I, Deplazes P (2011) Sonographical and serolog-ical survey of human cystic echinococcosis and analysis of risk factors associated with seroconversion in rural communities of Kerman. Iran Zoonoses Public Health 58(8):582–588. https://doi.org/10.1111/j.1863-2378.2011.01407.x
Järvis T, Kapel Ch, Moks E, Talvik H, Magi E (2007) Helminths of wild boar in the isolated population close to the northern border of its habitat area. Vet Parasitol 150:366–369. https://doi.org/10.1016/j.vetpar.2007.09.0155
Juránková J, Hulva P, Černá Bolfíková B, Hrazdilová K, Frgelecová L, Daněk O, Modrý D (2021) Identification of tapeworm species in genetically characterised grey wolves recolonising central Europe. Acta Parasitol 66(3):1063–1067. https://doi.org/10.1007/s11686-020-00327-7
Kaufmann J (2013) Parasitic infections of domestic animals: a diagnostic manual. Basel-Boston-Berlin: Birkhauser; 1996. 423p
Kedra AH, Tkach VV, Świderski Z, Pawłowski Z (2001) Intraspecific variability among NADH dehydrogenase subunit 1 sequences of Taenia hydatigena. Parasitol Int 50:145–148. https://doi.org/10.1016/s1383-5769(01)00064-2
Kinkar L, Laurimäe T, Balkaya I, Casulli A, Zait H, Irshadullah M, Sharbatkhori M, Mirhendi H, Rostami-Nejad M, Ponce-Gordo F (2018) Genetic diversity and phylogeography of the elusive, but epidemiologically important Echinococcus granulosus sensu stricto genotype G3. Parasitology 145(12):1613–1622. https://doi.org/10.1017/S0031182018000549
Kumar S, Stecher G, Li M, Knyaz Ch, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Lahmar S, Arfa I, Othmen SB, Jguirim W, Saïd Y, Dhibi A, Boufana B (2017) Intestinal helminths of stray dogs from Tunisia with special reference to zoonotic infections. Parasitol Open 3. https://doi.org/10.1017/pao.2017.21
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. Parasitol Int 60 (3):289–295. https://doi.org/10.1016/j.parint.2011.04.004
Letková V, Lazar P, Soroka J, Goldová M, Čurlík J (2008) Epizootiology of game cervid cysticercosis. Nat Croat 17(4):311–318
Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Ann Rev Ecol Syst 18:269–292
Mohammed A, Kadir MA (2020) Estimation of some biochemical parameters and trace elements in sheep infested with Taenia hydatigena cysts in Sulaymaniyah province/Iraq. Iraq J Vet Sci 34(1):39–44. https://doi.org/10.33899/ijvs.2019.125543.1065
Muku RJ, Yan HB, Ohiolei JO, Saaid AA, Ahmed S, Jia WZ, Fu BQ (2020) Molecular identification of Taenia hydatigena from sheep in Khartoum. Sudan Korean J Parasitol 58(1):93–97. https://doi.org/10.3347/kjp.2020.58.1.93
Murat K (2005) Investigation of antigenic specificity against Cysticercus tenuicollis cyst fluid antigen in dogs experimentally infected with Taenia hydatigena. Turk J Vet Animal Sci 29:835–840
Murrell KD, Dorny P, Flisser A, Geerts S, Kyvsgaard NC and McManus DP (2005) WHO/FAO/OIE guidelines for the surveillance, prevention and control of taeniasis/cysticercosis. Oie (world organisation for animal health). WHO (World Health Organization) and FAO (Food and Agriculture Organization)
Nguyen MT, Gabriël S, Abatih EN, Dorny P (2016) A systematic review on the global occurrence of Taenia hydatigena in pigs and cattle. Vet Parasitol 15(226):97–103. https://doi.org/10.1016/j.vetpar.2016.06.034
Ohiolei JA, Luka J, Zhu GQ, Yan HB, Li L, Magaji AA, Alvi MA, Wu YT, Li JQ, Fu BQ, Jia WZ (2019) First molecular description, phylogeny and genetic variation of Taenia hydatigena from Nigerian sheep and goats based on three mitochondrial genes. Parasite Vector 12:250. https://doi.org/10.1186/s13071-019-3780-5
Ohiolei JA, Yan HB, Li L, Li WH, Wu YD, Alvi MA, Zhang NZ, Fu BQ, Wang XL, Jia WZ (2021) A new molecular nomenclature for Taenia Hydatigena: mitochondrial DNA sequences reveal sufficient diversity suggesting the assignment of major haplotype divisions. Parasitology 148(3):311–326. https://doi.org/10.1017/S003118202000205X
Otranto D, Cantacessi C, Pfeffer M, Dantas-Torres F, Brianti E, Deplazes P, Genchi C, Guberti V, Capelli G (2015) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part I: protozoa and tick-borne agents.Vet Parasitol 213(1–2):12–23. https://doi.org/10.1016/j.vetpar.2015.04.022
Rostami S, Salavati R, Beech RN, Babaei Z, Sharbatkhori M, Baneshi MR, Hajialilo E, Shad H, Harandi MF (2015) Molecular and morphological characterization of the tapeworm Taenia hydatigena (Pallas, 1766) in sheep from Iran. J Helminthol 89:150–157. https://doi.org/10.1017/S0022149X13000667
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JA, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248
Scala A, Pipia AP, Dore F, Sanna G, Tamponi C, Marrosu R, Bandino E, Carmona C, Boufana B, Varcasia A (2015) Epidemiological updates and economic losses due to Taenia hydatigena in sheep from Sardinia, Italy. Parasitol Res 114:3137–3143. https://doi.org/10.1007/s00436-015-4532-x
Sgroi G, Varcasia A, Dessì G, D’Alessio N, Pacifico L, Buono F, Neola B, Fusco G, Santoro M, Toscano V, Fioretti A, Veneziano V (2019) Massive Taenia hydatigena cysticercosis in a wild boar (Sus scrofa) from Italy. Acta Parasitol 64(4):938–941. https://doi.org/10.2478/s11686-019-00110-3
Shimalov VV, Shimalov VT (2003) Helminth fauna of cervids in Belorussian Polesie. Parasitol Res 89:75–76. https://doi.org/10.1007/s00436-002-0700-x
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595. https://doi.org/10.1093/genetics/123.3.585
Takács A, Szabó L, Jhász L, Takács A, Lanszki J, Takács P, Heltai M (2014) Data on the parasitological status of golden jackal (Canis aureus L., 1758) in Hungary. Acta Vet Hung 62(1):33–41. https://doi.org/10.1556/avet.2013.058
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochon-drial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Thompson RC, Lymbery AJ, Smith A (2010) Parasites, emerging disease and wildlife conservation. Int J Parasitol 40:1163–1170. https://doi.org/10.1016/j.ijpara.2010.04.009
Tompkins DM, Carver S, Jones ME, Krkošek M, Skerratt LF (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends Parasitol 31(4):149–159. https://doi.org/10.1016/j.pt.2015.01.007
Tropiło J, Kiszczak L (1995) Cysticercosis in roe deer caused by Cysticercus tennuicollis and C. cervi. Magazyn Weterynaryjny 4:433
Varcasia A, Tanda B, Giobbe M, Solinas C, Pipia AP, Mal-Gor R, Carmona C, Garippa G, Scala A (2011) Cystic echinococcosis in Sardinia: farmers’ knowledge and dog infection in sheep farms. Vet Parasitol 181(2–4):335–340. https://doi.org/10.1016/j.vetpar.2011.05.006
Acknowledgements
The study was supported by the Scientific Grant Agency VEGA, project No. 2/0107/20.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
The authors claim that all parasitological and genetic procedures contributing to this work are in accordance with the ethical standards of the relevant national and institutional guides. Sheep samples were collected from slaughterhouses in Slovakia after the sheep were humanely slaughtered for meat. Free-living ruminants were legally hunted by hunters or found dead.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Bruno Gottstein
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jarošová, J., Antolová, D., Iglodyová, A. et al. Molecular identification of Taenia hydatigena from domestic and free-living animals in Slovakia, Central Europe. Parasitol Res 121, 1345–1354 (2022). https://doi.org/10.1007/s00436-022-07481-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-022-07481-z