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Licensed Unlicensed Requires Authentication Published by De Gruyter October 18, 2018

Molecular characterization and phylogenetic analysis of Taenia multiceps from China

L. Tan, A.B. Wang, S.Q. Zheng, X.L. Zhang, C.J. Huang and W. Liu
From the journal Acta Parasitologica

Abstract

Taenia multiceps, one of the most widely distributed zoonotic tapeworm parasites, is able to parasitize the small intestine of canids. The metacestode of T.multiceps is fatal to ruminants and causes important economic losses in livestock. However, molecular characteristics of T.multiceps and coenurus in China are still unclear. In this study, 36 goat isolates of the coenurus stage and 18 dog isolates of the adult stage of T.multiceps were obtained from three geographical areas in China and the isolated parasite above were analyzed by amplifying the partial of cytochrome coxidase subunit 1(pcox1), 12S ribosomal RNA (12S rRNA) from mitochondrial DNA (mtDNA) regions and an internal transcribed spacer (ITS) of ribosomal DNA (rDNA). These DNA sequences obtained from T.multiceps and coenurus were employed to evaluate the nucleotide diversity and confirm the relationship between T.multiceps and coenurus. Sequences variation were 0–1.4%, 0–1.5%, 0–4.2% for pcox1, 12S rRNA and ITS, respectively, among T.multiceps and coenurus isolates obtained in this study. In Sichuan province, sequence variations for Coenurus cerebralis isolated from Yaan city were 0–1.4% for pcox1, 0–1.0% for 12S rRNA and 0–2.1% for ITS. In Hunan province, variations were 0–1.0%, 0–1.5% and 0–3.3% for corresponding genes for non-coenurus cerebralis isolated from Changsha city, while variations of T.multiceps isolates from Xiangxi autonomous prefecture were 0–1.0%, 0–1.1% and 0–3.4% for pcox1, 12S rRNA and ITS, respectively. Phylogenetic analysis based on pcox1 sequences indicated that all cerebral and noncerebral metacestodes belong to T.multiceps. These results provide reference values for future molecular epidemiological and biological study on T.multiceps in dogs and intermediate hosts.

  1. Consent for publication. All animal studies/procedures of this project were approved by Hunan Agricultural University Research Ethics Committee as well as the Guide for the Care and Use of Laboratory Animals of the Ministry of Health, China.

  2. Conflict of interest None

Acknowledgments

We thank Guangyou Yang for contributing C.cerebralis samples. Project support was provided in part by the Bureau of Animal Husbandry and Fisheries, Hunan Province (20160875), the Department of Science and Technology, Hunan Province (2016NK2014) and the Program of Local Standards in Hunan Province (5026301-1112006), University Student Innovation Program in Veterinary Medicine college of Hunan Agricultural University ( dycx1604).

References

Akbari M., Moazeni M., Oryan A., Sharifiyazdi H., Amrabadi O. 2015. Experimental cerebral and non-cerebral coenurosis in goats: acomparative study on the morphological and molecular characteristics of the parasite. Veterina"ry Parasitology, 211, 201–207. 10.1016/j.vetpar.2015.06.013Search in Google Scholar PubMed

Al-Riyami S., Ioannidou E., Koehler A.V., Hussain M.H., Al-Rawahi A.H., Giadinis N.D., et al. 2016. Genetic characterisation of Taenia multiceps cysts from ruminants in Greece. Infection Genetics & Evolution, 38, 110–116. 10.1016/j.meegid. 2015.12.008Search in Google Scholar

Amer S., ElKhatam A., Fukuda Y., Bakr L.I., Zidan S., Elsify A., et al. 2017. Prevalence and identity of Taenia multiceps cysts "Coenurus cerebralis" in sheep in egypt. Acta Tropica, 176, 270–276. 10.1016/j.actatropica.2017.08.012Search in Google Scholar PubMed

Avcioglu H., Yildirim A., Duzlu O., Inci A., Terim K.A., Balkaya I. 2011. Prevalence and molecular characterization of bovine Coenurosis from Eastern Anatolian region of Turkey. Veterinary Parasitology, 176, 59–64. DOI: /10.1016/j.vetpar.2010.10.033/10.1016/j.vetpar.2010.10.033Search in Google Scholar

Benifla M., Barrelly R., Shelef I., El-On J., Cohen A., Cagnano E. 2007. Huge hemispheric intraparenchymal cyst caused by Taenia multiceps in a child. Journal of Neurosurgery, 107, 511–51410.3171/PED-07/12/511Search in Google Scholar PubMed

Burland T.G. 2000. DNASTAR’s Lasergene sequence analysis software. Methods in Molecular Biology, 132, 71–9110.1385/1-59259-192-2:71Search in Google Scholar

Cheng T., Gao D.Z., Zhu W.N., Fang S.F., Chen N., Zhu X.Q., et al. 2016. Genetic variability among Hymenolepis nana isolates from different geographical regions in China revealed by sequence analysis of three mitochondrial genes. Mitochondrial DNA, 27, 4646–4650. 10.3109/19401736.2015.1101595Search in Google Scholar PubMed

Christodoulopoulos G., Kassab A., Theodoropoulos G. 2015. Characteristics of non-cerebral coenurosis in tropical goats. Veterinary Parasitology, 211, 216–222. 10.1016/j.vetpar.2015.05.020Search in Google Scholar PubMed

Christodoulopoulos G., Dinkel A., Romig T., Ebi D., Mackensted U., Loos-Frank B. 2016. Cerebral and non-cerebral coenurosis: on the genotypic and phenotypic diversity of Taenia multiceps. Veterinary Parasitology, 115, 4543–4558. 10.1007/s00436-016-5246-4Search in Google Scholar PubMed

Collomb J., Machouart M., Biava M.F., Brizion M., Montagne K., Plénat F., Fortier B. 2007. Contribution of NADH dehydrogenase subunit I and cytochrome C oxidase subunit I sequences toward identifying a case of human Coenuriasis in France. Journal of Parasitology, 93, 934–93710.1645/GE-1160R.1Search in Google Scholar PubMed

Dai R.S., Liu G.H., Song H.Q., Lin R.Q., Yuan Z.G., Li M.W., et al. 2012. Sequence variability -in two mitochondrial DNA regions and internal transcribed spacer among three cestodes infecting animals and humans from China. Journal of Helminthology, 86, 245–251. 10.1017/S0022149X11000319Search in Google Scholar

El-On J., Shelef I., Cagnano E., Benifla M. 2008. Taenia multiceps: a rare human cestode infection in Israel. Veterinaria Italiana, 44, 621–631Search in 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, 1965–197010.1016/S0020-7519(99)00153-8Search in Google Scholar

Gasser R.B. 2006. Molecular tools-advances, opportunities and prospects. Veterinary Parasitology, 136, 69–89. 10.1016/j.vetpar.2005.12.002Search in Google Scholar PubMed

Jia W.Z., Yan H.B., Guo A.J., Zhu X.Q., Wang Y.C., Shi W.G., et al. 2010. Complete mitochondrial genomes of Taenia multiceps, T.hydatigena and T.pisiformis: additional molecular markers for a tapeworm genus of human and animal health significance. BMC Genomics, 11, 447. 10.1186/1471-216411-447Search in Google Scholar

Librado P., Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–145210.1093/bioinformatics/btp187Search in Google Scholar PubMed

Liu G.H., Lin R.Q., Li M.W., Liu W., Liu Y., Yuan Z.G, et al. 2011.The complete mitochondrial genomes of three cestode species of Taenia infecting animals and humans. Molecular Biology Reports, 38, 2249–2256. 10.1007/s11033-0100355-0Search in Google Scholar

Li W.H., Jia W.Z., Qu Z.G., Xie Z.Z., Luo J.X., Yin H., et al. 2013. Molecular Characterization of Taenia multiceps Isolates from Gansu Province, China by Sequencing of Mitochondrial Cytochrome C Oxidase Subunit 1. Korean Journal of Parasitology, 51, 197–201. 10.3347/kjp.2013.51.2.197Search in Google Scholar PubMed PubMed Central

Nakao M., Lavikainen A., Iwaki T., Haukisalmi V., Konyaev S., Oku Y., et al. 2013. Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria. International Journal of Parasitology, 2013, 427–437. 10.1016/j.ijpara.2012.11.014Search in Google Scholar PubMed

Oryan A., Nazifi S., Sharifiyazdi H., Ahmadnia S. 2010. Pathological, molecular, and biochemical characterization of Coenurus gaigeri in Iranian native goats. Journal of Parasitology, 96, 961–96710.1645/GE-2399.1Search in Google Scholar PubMed

Oryan A., Akbari M., Moazeni M., Amrabadi O. R. 2015. Cerebral and non-cerebral Coenurosis in small ruminants. Tropical Biomedicine, 31, 1–16Search in Google Scholar

Oryan A., Moazeni M., Amrabadi O., Akbari M., Sharifiyazdi H. 2015. Comparison of distribution pattern, pathogenesis and molecular characteristics of larval stages of taenia multiceps, in sheep and goats. Small Ruminant Research, 132, 44–4910.1016/j.smallrumres.2015.10.008Search in Google Scholar

Rostami S., Salavati R., Beech R.N., Sharbatkhori M., Babaei Z., Saedi S., Harandi M.F. 2013. Cytochrome c oxidase subunit 1 and 12S ribosomal RNA characterization of Coenurus cerebralis from sheep in Iran. Veterinary Parasitology. 197, 141– 151. 10.1016/j.vetpar.2013.07.001Search in Google Scholar

Schuster R.K., Sivakumar S., Wieckowsky T. 2010. Non-cerebral coenurosis in goats. Parasitology Research, 107, 721–72610.1007/s00436-010-1919-6Search in Google Scholar

Sonmez B., Koroglu E., Simsek S. 2017. Molecular characterization and detection of variants of Taenia multiceps in sheep in Turkey. Parasitology, 144, 220–225. 10.1017/S0031182016001669Search in Google Scholar

Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739. 10.1093/molbev/msr121Search in Google Scholar

Tappe D., Berkholz J., Mahlke U., Lobeck H., Nagel T., Haeupler A., et al. 2016. Molecular Identification of Zoonotic TirrnSe-Invasive Tapeworm Larvae Other than Taenia solium in Suspected Human. Cysticercosis Cases. Journal of Clinical Microbiology, 54, 172–174. 10.1128/JCM.02171-15Search in Google Scholar

Thompson J.D., Gibson T.J., Plewniak F.D.R., Jeanmougin F.O., Higgins D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–488210.1093/nar/25.24.4876Search in Google Scholar

Varcasia A., Pipia A.P., Arru D., Pes A.M., Tamponi C., Dore, et al. 2013. Morphological and molecular characterization of bovine coenurosis in sardinia, italy. Parasitology Research, 112, 2079–2082. 10.1007/s00436-012-3257-3Search in Google Scholar

Yan H., Lou Z., Li L., Ni X., Guo A., Li H., et al. 2013. The nuclear 18S ribosomal RNA gene as a source of phylogenetic information in the genus Taenia. Parasitology Research, 112, 1343–1347. 10.1645/0022-3395(2000)086[0089:APHFSO]2.0.CO;2Search in Google Scholar

Zhang L., Hu M., Jones A., Allsopp B.A., Beveridge I., Schindler A.R., Gasser R.B. 2007. Characterization of Taenia madoquae and Taenia regis from carnivores in Kenya using genetic markers in nuclear and mitochondrial DNA, and their relationships with other selected taeniids. Molecular and Cellular Probes, 21, 379-385. 10.1016/j.mcp.2007.05.003Search in Google Scholar

Zhang Y., Zhao W., Yang D., Tian Y., Zhang W., Liu A. 2018. Genetic characterization of three mitochondrial gene sequences of goat/sheep-derived coenurus cerebralis and cysticercus tenuicollis isolates in inner Mongolia, China. Parasite, 25, 1. 10.1051/parasite/2018002Search in Google Scholar

Zhu X., Chilton N.B., Jacobs D.E., Boes J., Gasser R.B. 1999. Characterisation of Ascaris from human and pig hosts by nuclear ribosomal DNA sequences. International Journal for Parasitology, 29, 469–47810.1016/S0020-7519(98)00226-4Search in Google Scholar

Received: 2017-12-12
Revised: 2018-05-25
Accepted: 2018-07-06
Published Online: 2018-10-18
Published in Print: 2018-12-19

© 2018 W. Stefański Institute of Parasitology, PAS