Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Prevalence and Molecular Characterization of Echinococcus granulosus Sensu Stricto in Northern Xinjiang, China

  • Guo, Baoping (College of Animal Science and Technology, Shihezi University) ;
  • Zhang, Zhuangzhi (Veterinary Research Institute, Xinjiang Academy of Animal Sciences) ;
  • Zheng, Xueting (State Key Laboratory for Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asian, First Affiliated Hospital of Xinjiang Medical University) ;
  • Guo, Yongzhong (The Friendship Hospital of Yili Kazak Autonomous Prefecture) ;
  • Guo, Gang (State Key Laboratory for Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asian, First Affiliated Hospital of Xinjiang Medical University) ;
  • Zhao, Li (Veterinary Research Institute, Xinjiang Academy of Animal Sciences) ;
  • Cai, Ren (State Key Laboratory for Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asian, First Affiliated Hospital of Xinjiang Medical University) ;
  • Wang, Bingjie (Veterinary Research Institute, Xinjiang Academy of Animal Sciences) ;
  • Yang, Mei (Basic Medical College of Xinjiang Medical University) ;
  • Shou, Xi (State Key Laboratory for Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asian, First Affiliated Hospital of Xinjiang Medical University) ;
  • Zhang, Wenbao (State Key Laboratory for Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asian, First Affiliated Hospital of Xinjiang Medical University) ;
  • Jia, Bin (College of Animal Science and Technology, Shihezi University)
  • Received : 2018.08.05
  • Accepted : 2018.12.17
  • Published : 2019.04.30
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Abstract

Echinococcus granulosus is an important zoonotic parasite globally causing cystic echinococcosis (CE) in humans and animals. In this study, prevalence of CE and variation of cox1 gene sequence were analyzed with isolates E. granulosus collected from different areas in northern Xinjiang, China. The survey showed that 3.5% of sheep and 4.1% of cattle were infected with CE. Fragment of cox1 was amplified from all the positive sheep and cattle samples by PCR. In addition, 26 positive samples across the 4 areas were included. The isolates were all E. granulosus sensu stricto (s.s.) containing 15 haplotypes (Hap1-15), and clustered into 2 genotypes, G1 (90.1%, 91/101) and G3 (9.9%, 10/101). Hap1 was the most common haplotype (48.5%, 49/101). Hap9 were found in humans samples, indicating that sheep and cattle reservoir human CE. It is indicate that E. granulosus may impact on control of CE in livestock and humans in the region.

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References

  1. Addy F, Wassermann M, Kagendo D, Ebi D, Zeyhle E, Elmahdi IE, Umhang G, Casulli A, Harandi MF, Aschenborn O, Kern p, Mackenstedt U, Roming T. Genetic differentiation of the G6/7 cluster of Echinococcus canadensis based on mitochondrial marker genes. Int J Parasitol 2017; 47: 923-931. https://doi.org/10.1016/j.ijpara.2017.06.003
  2. Eckert J, Thompson RC. Historical Aspects of Echinococcosis. Adv Parasit 2017; 95: 1-64. https://doi.org/10.1016/bs.apar.2016.07.003
  3. Beato S, Parreira R, Calado M, Gracio MA. Apparent dominance of the G1-G3 genetic cluster of Echinococcus granulosus strains in the central inland region of Portugal. Parasitol Int 2010; 59: 638-642. https://doi.org/10.1016/j.parint.2010.08.004
  4. Oudni-M'rad M, M'rad S, Ksia A, Lamiri R, Mekki M, Nouri A, Mezhoud H, Babba H. First molecular evidence of the simultaneous human infection with two species of Echinococcus granulosus sensu lato: Echinococcus granulosus sensu stricto and Echinococcus canadensis. Parasitol Res 2016; 115: 1065-1069. https://doi.org/10.1007/s00436-015-4836-x
  5. Otero-Abad B, Torgerson PR. A systematic review of the epidemiology of echinococcosis in domestic and wild animals. PLoS Negl Trop Dis 2013; 7: e2249. https://doi.org/10.1371/journal.pntd.0002249
  6. Lahmar S, Lahmar S, Boufana B, Bradshaw H, Craig PS. Screening for Echinococcus granulosus in dogs: Comparison between arecoline purgation, coproELISA and coproPCR with necropsy in pre-patent infections. Vet Parasitol 2007; 144: 287-292. https://doi.org/10.1016/j.vetpar.2006.10.016
  7. Zhang W, Ross AG, McManus DP. Mechanisms of Immunity in Hydatid Disease: Implications for Vaccine Development. J Immunol 2008; 181: 6679-6685. https://doi.org/10.4049/jimmunol.181.10.6679
  8. Wang N, Xie Y, Liu T, Zhong X, Wang J, Hu D, Wang S, Gu X, Peng X, Yang G. The complete mitochondrial genome of G3 genotype of Echinococcus granulosus (Cestoda: Taeniidae). Mitochondrial DNA A DNA Mapp Seq Anal 2016; 27: 1701-1702.
  9. Qingling M, Guanglei W, Jun Q, Xinquan Z, Tianli L, Xuemei S, Jinsheng Z, Huisheng W, Kuojun C, Chuangfu C. Prevalence of Hydatid Cysts in Livestock Animals in Xinjiang, China. Korean J Parasitol 2014; 52: 331-334. https://doi.org/10.3347/kjp.2014.52.3.331
  10. Nakao M, Lavikainen A, Iwaki T, Haukisalmi V, Konyaev S, Oku Y, Okamoto M, Ito A. Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): Proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria. Int J Parasitol 2013; 43: 427-437. https://doi.org/10.1016/j.ijpara.2012.11.014
  11. Zhang W, Zhang Z, Wu W, Shi B, Li J, Zhou X, Wen H, McManus DP. Epidemiology and control of echinococcosis in central Asia, with particular reference to the People's Republic of China. Acta Trop 2015; 141: 235-243. https://doi.org/10.1016/j.actatropica.2014.03.014
  12. Josephine Bowles DavidBaDonaldPMcManus. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 1992; 54: 165-174. https://doi.org/10.1016/0166-6851(92)90109-W
  13. Ahmed ME, Eldigail MH, Elamin FM, Ali IA, Grobusch MP, Aradaib IE. Development and evaluation of real-time loop-mediated isothermal amplification assay for rapid detection of cystic echinococcosis. BMC Vet Res 2016; 12: 202. https://doi.org/10.1186/s12917-016-0809-2
  14. Graichen DAS, Gottstein B, Matsumoto J, Muller N, Zanotto PMA, Ayala FJ, Haag KL. Expression and diversity of Echinococcus multilocularis AgB genes in secondarily infected mice: evaluating the influence of T-cell immune selection on antigenic variation. Gene 2007; 392: 98-105. https://doi.org/10.1016/j.gene.2006.11.015
  15. Nakao M, Li T, Han X, Ma X, Xiao N, Qiu J, Wang H, Yanagida T, Mamuti W, Wen H, Moro PL, Giraudoux P, Craig PS, Ito A. Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. Int J Parasitol 2010; 40: 379-385. https://doi.org/10.1016/j.ijpara.2009.09.006
  16. Nakao M, Yanagida T, Konyaev S, Lavikainen A, Odnokurtsev VA, Zaikov VA, Ito A. Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 2013; 140: 1625-1636. https://doi.org/10.1017/S0031182013000565
  17. Wang K, Zhang X, Jin Z, Ma H, Teng Z, Wang L. Modeling and analysis of the transmission of Echinococcosis with application to Xinjiang Uygur Autonomous Region of China. J Theor Biol 2013; 333: 78-90. https://doi.org/10.1016/j.jtbi.2013.04.020
  18. Farhadi M, Fazaeli A, Haniloo A. Genetic characterization of livestock and human hydatid cyst isolates from northwest Iran, using the mitochondrial cox1 gene sequence. Parasitol Res 2015; 114: 4363-4370. https://doi.org/10.1007/s00436-015-4673-y
  19. Rongsheng Mi XW, Yan Huang, Peng Zhou, Yuxuan Liu, Yongjun Chen, Jun Chen, Wei Zhu, Zhaoguo Chen. Prevalence and molecular characterization of Cryptosporidium in goats across four provincial level areas in China. PLoS One 2014; 9: e111164. https://doi.org/10.1371/journal.pone.0111164
  20. Liu F, Che X, Chang Q. Prevalence of Hydatid Cysts in livestock in the Xinjiang Uygur Autonomous Region, PRC. Provo, USA. Brigham Young University Print Services. 1993, pp 177-189.
  21. Zhang W, Zhang Z, Yimit T, Shi B, Aili H, Tulson G, You H, Li J, Gray DJ, McManus DP, Wang J. A Pilot Study for Control of Hyperendemic Cystic Hydatid Disease in China. PLoS Negl Trop Dis 2009; 3: e534. https://doi.org/10.1371/journal.pntd.0000534
  22. Yang S, Wu W, Tian T, Zhao J, Chen K, Wang Q, Feng Z. Prevalence of cystic echinococcosis in slaughtered sheep as an indicator to assess control progress in Emin County, Xinjiang, China. Korean J Parasitol 2015; 53: 355-359. https://doi.org/10.3347/kjp.2015.53.3.355
  23. Romig T, Ebi D, Wassermann M: Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol 2015; 213: 76-84. https://doi.org/10.1016/j.vetpar.2015.07.035
  24. Kamenetzky L, Gutierrez AM, Canova SG, Haag KL, Guarnera EA, Parra A, Garcia GE, Rosenzvit MC. Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infect Genet Evol 2002; 2: 129-136. https://doi.org/10.1016/S1567-1348(02)00131-4
  25. Vural G, Baca AU, Gauci CG, Bagci O, Gicik Y, Lightowlers MW. Variability in the Echinococcus granulosus Cytochrome C oxidase 1 mitochondrial gene sequence from livestock in Turkey and a re-appraisal of the G1-3 genotype cluster. Vet Parasitol 2008; 154: 347-350. https://doi.org/10.1016/j.vetpar.2008.03.020
  26. Busi M, Snabel V, Varcasia A, Garippa G, Perrone V, De Liberato C, D'Amelio S. Genetic variation within and between G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Vet Parasitol 2007; 150: 75-83. https://doi.org/10.1016/j.vetpar.2007.09.003
  27. Mahami Oskouei M, Ghabouli Mehrabani N, Miahipour A, Fallah E. Molecular characterization and sequence analysis of echinococcus granulosus, from sheep isolates in east azerbaijan province, northwest of iran. J Parasit Dis 2016; 40: 1-6. https://doi.org/10.1007/s12639-014-0450-6
  28. Capuano F, Rinaldi L, Maurelli MP, Perugini AG, Veneziano V, Garippa G, Genchi C, Musella V, Cringoli G. Cystic echinococcosis in water buffaloes: epidemiological survey and molecular evidence of ovine (G1) and buffalo (G3) strains. Vet Parasitol 2006; 137: 262-268. https://doi.org/10.1016/j.vetpar.2006.01.016
  29. Sharma M, Sehgal R, Fomda BA, Malhotra A, Malla N. Molecular Characterization of Echinococcus granulosus Cysts in North Indian Patients: Identification of G1, G3, G5 and G6 Genotypes. PLoS Negl Trop Dis 2013; 7: e2262. https://doi.org/10.1371/journal.pntd.0002262
  30. Jia WZ, Yan HB, Guo AJ, Zhu XQ, Wang YC, Shi WG, Chen HT, Zhan F, Zhang SH, Fu BQ, Littlewood DT, Cai XP. 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 2010; 11: 447. https://doi.org/10.1186/1471-2164-11-447
  31. Casulli A, Manfredi MT, La Rosa G, Cerbo AR, Genchi C, Pozio E. Echinococcus ortleppi and E. granulosus G1, G2 and G3 genotypes in Italian bovines. Vet Parasitol 2008; 155: 168-172. https://doi.org/10.1016/j.vetpar.2008.04.004
  32. Hassan ZI, Meerkhan AA, Boufana B, Hama AA, Ahmed BD, Mero WMS, Orsten S, Interisano M, Pozio E, Casulli A. Two haplotype clusters of Echinococcus granulosus sensu stricto in northern Iraq (Kurdistan region) support the hypothesis of a parasite cradle in the Middle East. Acta Trop 2017; 172: 201-207. https://doi.org/10.1016/j.actatropica.2017.04.028
  33. Laurimae T, Kinkar L, Andresiuk V, Haag KL, Ponce-Gordo F, Acosta-Jamett G, Garate T, Gonzalez LM, Saarma U. Genetic diversity and phylogeography of highly zoonotic Echinococcus granulosus genotype G1 in the Americas (Argentina, Brazil, Chile and Mexico) based on 8279bp of mtDNA. Infect Genet Evol 2016; 45: 290-296. https://doi.org/10.1016/j.meegid.2016.09.015
  34. Konyaev SV, Yanagida T, Nakao M, Ingovatova GM, Shoykhet YN, Bondarev AY, Odnokurtsev VA, Loskutova KS, Lukmanova GI, Dokuchaev NE, Spiridonov S, Alshinecky MV, Sivkova TN, Andreyanov ON, Abramov SA, Krivopalov AV, Karpenko SV, Lopatina NV, Dupal TA, Sako Y, Ito A. Genetic diversity of Echinococcus spp. in Russia. Parasitology 2013; 140: 1637-1647. https://doi.org/10.1017/S0031182013001340
  35. Casulli A, Bart JM, Knapp J, La Rosa G, Dusher G, Gottstein B, Di Cerbo A, Manfredi MT, Genchi C, Piarroux R, Pozio E. Multi-locus microsatellite analysis supports the hypothesis of an autochthonous focus of Echinococcus multilocularis in northern Italy. Int J Parasitol 2009; 39: 837-842. https://doi.org/10.1016/j.ijpara.2008.12.001
  36. Ma J, Wang H, Lin G, Craig PS, Ito A, Cai Z, Zhang T, Han X, Ma X, Zhang J Liu Y, Zhao Y, Wang Y. Molecular identification of Echinococcus species from eastern and southern Qinghai, China, based on the mitochondrial cox1 gene. Parasitol Res 2012; 111: 179-184. https://doi.org/10.1007/s00436-012-2815-z
  37. Ma J, Wang H, Lin G, Zhao F, Li C, Zhang T, Ma X, Zhang Y, Hou Z, Cai H, Liu P, Wang Y. Surveillance of Echinococcus isolates from Qinghai, China. Vet Parasitol 2015; 207: 44-48. https://doi.org/10.1016/j.vetpar.2014.11.012
  38. Yanagida T, Mohammadzadeh T, Kamhawi S, Nakao M, Sadjjadi SM, Hijjawi N, Abdel-Hafez SK, Sako Y, Okamoto M, Ito A. Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitol Int 2012; 61: 599-603. https://doi.org/10.1016/j.parint.2012.05.014
  39. Pour AA, Hosseini SH, Shayan P. The prevalence and fertility of hydatid cysts in buffaloes from Iran. J Helminthol 2012; 86: 373-377. https://doi.org/10.1017/S0022149X11000514

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