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Levels of sparganum infections and phylogenetic analysis of the tapeworm Spirometra erinaceieuropaei sparganum in wild frogs from Henan Province in central China

Published online by Cambridge University Press:  13 May 2014

T. Wei
Affiliation:
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou450052, The People's Republic of China
X. Zhang
Affiliation:
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou450052, The People's Republic of China
J. Cui*
Affiliation:
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou450052, The People's Republic of China
L.N. Liu
Affiliation:
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou450052, The People's Republic of China
P. Jiang
Affiliation:
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou450052, The People's Republic of China
Z.Q. Wang*
Affiliation:
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou450052, The People's Republic of China
*
*Fax: +86-371-66997182 E-mails: cuij@zzu.edu.cn, wangzq@zzu.edu.cn
*Fax: +86-371-66997182 E-mails: cuij@zzu.edu.cn, wangzq@zzu.edu.cn

Abstract

Sparganosis is a serious food-borne parasitic zoonosis caused by infection with Spirometra spargana. The prevalence of sparganum infection in wild frogs (Rana nigromaculata, R. limmochari, R. temporaria and Bufo gargarizans) was investigated in Henan Province of central China during 2008–2012. Of 3482 caught wild frogs, 565 (16.23%) were found to be infected with plerocercoids (spargana) of the genus Spirometra. Spargana were found in 14.85% (320/2155) of R. nigromaculata, 20.82% (233/1119) of R. limmochari and 10.91% (12/110) of R. temporaria frogs. However, no sparganum was found in B. gargarizans. To investigate the phylogenetic position of collected spargana, three mitochondrial DNA (mtDNA) regions, namely cytochrome c oxidase subunits 1 and 3 (cox1 and cox3), and NADH dehydrogenase subunit 4 (nad4), were amplified, sequenced and analysed. Sequences of cox1, cox3 and pnad4 were 417, 390 and 578 bp in length, respectively. The base composition of cox1, cox3 and pnad4 were generally AT rich with a mean of 63.5%, 68.3% and 67% AT, respectively. Phylogenetic analysis showed that all the sparganum isolates in Henan Province represented Spirometra erinaceieuropaei and were a well-supported clade. These findings demonstrated clearly the usefulness of the three mtDNA sequences for molecular identification and population genetics studies of S. erinaceieuropaei spargana of human and animal health significance.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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References

Anantaphruti, M.T., Nawa, Y. & Vanvanitchai, Y. (2011) Human sparganosis in Thailand: an overview. Acta Tropica 118, 171176.CrossRefGoogle ScholarPubMed
Bogitsch, B.J., Carter, C.E. & Oeltmann, T.N. (2005) Human parasitology. 3rd edn. New York, Academic Press.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, 165173.CrossRefGoogle ScholarPubMed
Chen, X.T. (1965) Medical parasitology. 2nd edn. Beijing, People's Health.Google Scholar
Cui, J., Li, N., Wang, Z.Q., Jiang, P. & Lin, X.M. (2011a) Serodiagnosis of experimental sparganum infections of mice and human sparganosis by ELISA using ES antigens of Spirometra mansoni spargana. Parasitology Research 108, 15511556.CrossRefGoogle ScholarPubMed
Cui, J., Lin, X.M., Zhang, H.W., Xu, B.L. & Wang, Z.Q. (2011b) Sparganosis, Henan Province, central China. Emerging Infectious Diseases 17, 146147.CrossRefGoogle ScholarPubMed
Dai, R.S., Liu, G.H., Song, H.Q., Lin, R.Q., Yuan, Z.G., Li, M.W., Huang, S.Y., Liu, W. & Zhu, X.Q. (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, 245251.CrossRefGoogle ScholarPubMed
Fukushima, T. & Yamane, Y. (1999) How does the sparganosis occur? Parasitology Today 15, 124.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.CrossRefGoogle ScholarPubMed
Higgins, D.G., Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D. & Gibson, T.J. (2007) Clustal W and clustal X version 2.0. Bioinformatics 23, 29472948.Google Scholar
Li, M.W., Lin, R.Q., Song, H.Q., Sani, R.A., Wu, X.Y. & Zhu, X.Q. (2008) Electrophoretic analysis of sequence variability in three mitochondrial DNA regions for ascaridoid parasites of human and animal health significance. Electrophoresis 29, 29122917.CrossRefGoogle ScholarPubMed
Liu, G.H., Li, C., Li, J.Y., Zhou, D.H., Xiong, R.C., Lin, R.Q., Zou, F.C. & Zhu, X.Q. (2012) Characterization of the complete mitochondrial genome sequence of Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidae) from China. International Journal of Biological Sciences 8, 640649.CrossRefGoogle ScholarPubMed
Liu, W., Zhao, G.H., Tan, M.Y., Zeng, D.L., Wang, K.Z., Yuan, Z.G., Lin, R.Q., Zhu, X.Q. & Liu, Y. (2010) Survey of Spirometra erinaceieuropaei spargana infection in the frog Rana nigromaculata of the Hunan Province of China. Veterinary Parasitology 173, 152156.CrossRefGoogle ScholarPubMed
Liu, W., Liu, G.H., Li, F., He, D.S., Wang, T., Sheng, X.F., Zeng, D.L., Yang, F.F. & Liu, Y. (2012) Sequence variability in three mitochondrial DNA regions of Spirometra erinaceieuropaei spargana of human and animal health significance. Journal of Helminthology 86, 271275.CrossRefGoogle ScholarPubMed
Lopez, P., Forterre, P. & Philippe, H. (1999) The root of the tree of life in the light of the covarion model. Journal of Molecular Evolution 49, 496508.CrossRefGoogle ScholarPubMed
Magnino, S., Colin, P., Dei-Cas, E., Madsen, M., McLauchlin, J., Nöckler, K., Maradona, M.P., Tsigarida, E., Vanopdenbosch, E. & Van Peteghem, C. (2009) Biological risks associated with consumption of reptile products. International Journal of Food Microbiology 134, 163175.CrossRefGoogle ScholarPubMed
Nakao, M., Sako, Y., Yokoyama, N., Fukunaga, M. & Ito, A. (2000) Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415424.CrossRefGoogle ScholarPubMed
Nithiuthai, S., Anantaphruti, M.T., Waikagul, J. & Gajadhar, A. (2004) Waterborne zoonotic helminthiases. Veterinary Parasitology 126, 167193.CrossRefGoogle ScholarPubMed
Ooi, H.K., Chang, S.L., Huang, C.C., Kawakami, Y. & Uchida, A. (2000) Survey of Spirometra erinaceieuropaei in frogs in Taiwan and its experimental infection in cats. Journal of Helminthology 74, 173176.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Qiu, M.H. & Qiu, M.D. (2009) Human plerocercoidosis and sparganosis: II. A historical review on pathology, clinics, epidemiology and control. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 27, 251260.Google Scholar
Rambaut, A. (2002) Se-Al: Sequence Alignment EditorVersion 2.0. Available athttp://tree.bio.ed.ac.uk/software/seal/ (accessed accessed 8 June 2013).Google Scholar
Rambaut, A. & Drummond, A.J. (2007) Tracer v1.5. Available athttp://beast.bio.ed.ac.uk/ Tracer (accessed 29 March 2014).Google Scholar
Roberts, L.S., Janovy, J. Jr & Gerald, D. (2009) Foundations of parasitology. 8th edn. New York, McGraw-Hill.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Shirakawa, K., Yamasaki, H., Ito, A. & Miyajima, H. (2010) Cerebral sparganosis: the wandering lesion. Neurology 74, 180.CrossRefGoogle ScholarPubMed
Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0b10. Sunderland, Massachusetts, Sinauer Associates.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, 27312739.CrossRefGoogle ScholarPubMed
Wardle, R.A. & McLeod, J.A. (1952) The zoology of tapeworms. Minneapolis, University of Minnesota Press.Google Scholar
Xia, X. & Xie, Z. (2001) DAMBE: software package for data analysis in molecular biology and evolution. Journal of Heredity 92, 371373.CrossRefGoogle ScholarPubMed
Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 17.CrossRefGoogle ScholarPubMed
Zarowiecki, M.Z., Huyse, T. & Littlewood, D.T. (2007) Making the most of mitochondrial genomes – markers for phylogeny, molecular ecology and barcodes in Schistosoma (Platyhelminthes: Digenea). International Journal for Parasitology 37, 14011418.CrossRefGoogle ScholarPubMed