Journal of Parasitic Diseases

, Volume 40, Issue 3, pp 785–790 | Cite as

Molecular characterization and sequence analysis of Echinococcus granulosus from sheep isolates in East Azerbaijan province, northwest of Iran

  • Mahmoud Mahami Oskouei
  • Nader Ghabouli MehrabaniEmail author
  • Abolfazl Miahipour
  • Esmaeil Fallah
Original Article


Echinococcus granulosus as an etiologic agent of hydatid cyst is one of the most important zoonotic helminthes in the world that causing enormous economic and health losses. The aim of this study was to evaluate genotype of E. granulosus isolated from sheep using mitochondrial cytochrome c oxidase subunit 1 (cox1) gene and sequencing method in East Azerbaijan province, northwest of Iran. Nineteen sheep hydatid cyst samples were collected. Genomic DNA was extracted from protoscoleces using commercial DNA extraction kit. Mitochondrial cox1 region was amplified by polymerase chain reaction (PCR) and all isolates were sequenced. Afterward, sequences were analyzed for determination of genotypes by related software. G1 (94.73 %) and G3 (5.27 %) genotypes were identified from the isolates which out of 19 hydatid cysts, 17 samples were G1B, 1 sample G1D and the other one had G3 genotype. Results of this study indicate that common sheep strain (G1); especially G1B is the dominant subtype of E. granulosus in East Azerbaijan province.


Echinococcus granulosus Cox1 Sheep Sequencing Iran 



This work was supported fully by Tabriz Infectious and Tropical Diseases Research Center (Grant no: 92-01), Tabriz University of Medical Sciences, Tabriz, Iran. This is a report of a database from thesis of Nader Ghabouli Mehrabani entitled “Genotyping of Echinococcus granulosus isolates from human and herbivores using mitochondrial cytochrome oxidase 1(cox1) gene by sequencing method in Tabriz” registered in Tabriz University of Medical Sciences.

Conflict of interest

The authors declare that there is no conflict of interest.


  1. Abdel Aaty H, Abdel-Hameed D, Alam-Eldin Y, El-Shennawy S, Aminou H, Makled S, Darweesh S (2012) Molecular genotyping of Echinococcus granulosus in animal and human isolates from Egypt. Acta Trop 121(2):125–128. doi: 10.1016/j.actatropica.2011.10.014 CrossRefGoogle Scholar
  2. Adwan G, Adwan K, Bdir S, Abuseir S (2013) Molecular characterization of Echinococcus granulosus isolated from sheep in Palestine. Exp Parasitol 134:195–199. doi: 10.1016/j.exppara.2013.03.024 CrossRefPubMedGoogle Scholar
  3. Bart JM, Abdukader M, Zhang YL, Lin RY (2006) Genotyping of human cystic echinococcosis in Xinjiang, PR China. Parasitology 133:571–579CrossRefPubMedGoogle Scholar
  4. Beato S, Parreira R, Calado M, Gracio M (2010) Apparent dominance of the G1-G3 genetic cluster of Echinococcus granulosus strains in the central inland region of Portugal. Parasitol Int 59:4. doi: 10.1016/j.parint.2010.08.004 CrossRefGoogle Scholar
  5. Bhattacharya D, Bera AK, Bera BC, Maity A, Das SK (2007) Genotypic characterisation of Indian cattle, buffalo and sheep isolates of Echinococcus granulosus. Vet Parasitol 143:371–374CrossRefPubMedGoogle Scholar
  6. Boufana B, Stidworthy MF, Bell S, Chantrey J (2012) Echinococcus and Taenia spp. from captive mammals in the United Kingdom. Vet Parasitol 190:95–103. doi: 10.1016/j.vetpar.2012.05.023 CrossRefPubMedGoogle Scholar
  7. Bowles J, McManus DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol 23:969–972CrossRefPubMedGoogle Scholar
  8. Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–173CrossRefPubMedGoogle Scholar
  9. Busi M, Šnábel V, Varcasia A, Garippa G, Perrone V, De Liberato C, D’amelio S (2007) Genetic variation within and between G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Vet Parasitol 150:75–83. doi: 10.1016/j.vetpar.2007.09.003 CrossRefPubMedGoogle Scholar
  10. Daniel Mwambete K, Ponce-Gordo F, Cuesta-Bandera C (2004) Genetic identification and host range of the Spanish strains of Echinococcus granulosus. Acta Trop 91(2):87–93. doi: 10.1016/j.actatropica.2004.04.001 CrossRefPubMedGoogle Scholar
  11. Dousti M, Abdi J, Bakhtiyari S, Mohebali M, Mirhendi S, Rokni M (2013) Genotyping of hydatid cyst isolated from human and domestic animals in Ilam province, Western Iran using PCR-RFLP. Iran j Parasitol 8(1):47PubMedCentralPubMedGoogle Scholar
  12. Ergin S, Saribas S, Yuksel P, Zengin K, Midilli K, Adas G, Arikan S, Aslan M, Uysal H, Caliskan R (2010) Genotypic characterisation of Echinococcus granulosus isolated from human in Turkey. Afr J Microbiol Res 4:551–555Google Scholar
  13. Ghabouli Mehrabani N, Kousha A, Khalili M, Mahami Oskouei M, Mohammadzadeh M, Alizadeh S, Maleksabet A, Hamidi F (2014) Hydatid cyst surgeries in patients referred to hospitals in East Azerbaijan province during 2009–2011. Iran J Parasitol 9(2):233–238Google Scholar
  14. Gillespie SH, Pearson RD (2001) Principles and practice of clinical parasitology. Wiley, Chichester,UK, pp 585–612. doi: 10.1002/0470842504.fmatter_indsub CrossRefGoogle Scholar
  15. Hajialilo E, Harandi MF, Sharbatkhori M, Mirhendi H, Rostami S (2012) Genetic characterization of Echinococcus granulosus in camels, cattle and sheep from the south-east of Iran indicates the presence of the G3 genotype. J Helminthol 86(3):263. doi: 10.1017/S0022149X11000320 CrossRefPubMedGoogle Scholar
  16. Jabbar A, Narankhajid M, Nolan MJ, Jex AR, Campbell BE, Gasser RB (2011) A first insight into the genotypes of Echinococcus granulosus from humans in Mongolia. MCP 25:49–54. doi: 10.1016/j.mcp.2010.11.001 CrossRefGoogle Scholar
  17. Kamenetzky L, Gutierrez AM, Canova SG, Haag KL, Guarnera EA, Parra A, García GE, Rosenzvit MC (2002) Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infect. Genet Evol 2:129–136CrossRefPubMedGoogle Scholar
  18. Knapp J, Nakao M, Yanagida T, Okamoto M, Saarma U, Lavikainen A, Ito A (2011) Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Mol Phylogenet Evol 61:628–638. doi: 10.1016/j.ympev.2011.07.022 CrossRefPubMedGoogle Scholar
  19. Konyaev SV, Yanagida T, Nakao M, Ingovatova GM, Shoykhet YN, Bondarev AY (2013) Genetic diversity of Echinococcus spp. in Russia. Parasitology 140:1637–1647. doi: 10.1017/S0031182013001340 CrossRefPubMedGoogle Scholar
  20. Latif AA, Tanveer A, Maqbool A, Siddiqi N, Kyaw-Tanner M, Traub RJ (2010) Morphological and molecular characterisation of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Vet Parasitol 170:44–49. doi: 10.1016/j.vetpar.2010.02.003 CrossRefPubMedGoogle Scholar
  21. Lavikainen A, Lehtinen M, Meri T, Hirvelä-Koski V, Meri S (2003) Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127:207–215CrossRefPubMedGoogle Scholar
  22. M’rad S, Filisetti D, Oudni M, Mekki M, Belguith M, Nouri A, Sayadi T, Lahmar S, Candolfi E, Azaiez R (2005) Molecular evidence of ovine (G1) and camel (G6) strains of Echinococcus granulosus in Tunisia and putative role of cattle in human contamination. Vet Parasitol 129:267–272. doi: 10.1016/j.vetpar.2005.02.006 CrossRefPubMedGoogle Scholar
  23. Ma S, Maillard S, Zhao H, Huang X, Wang H, Geng P, Bart J-M, Piarroux R (2008) Assessment of Echinococcus granulosus polymorphism in Qinghai province, People’s Republic of China. Parasitol Res 102:1201–1206. doi: 10.1007/s00436-008-0894-7 CrossRefPubMedGoogle Scholar
  24. Monteiro DU, Botton SA, Tonin AA, Azevedo MI, Graichen DAS, Noal CB, de la Rue ML (2014) Echinococcus canadensis (G7) and Echinococcus granulosus sensu stricto (G1) in swine of southern Brazil. Vet Parasitol 28:335–338. doi: 10.1016/j.vetpar.2014.01.023 CrossRefGoogle Scholar
  25. Moro P, Schantz P (2008) Echinococcosis: a review. Int J Infect Dis 13:125–133. doi: 10.1016/j.ijid.2008.03.037 CrossRefPubMedGoogle Scholar
  26. Pednekar RP, Gatne ML, Thompson R, Traub RJ (2009) Molecular and morphological characterisation of Echinococcus from food producing animals in India. Vet Parasitol 165(1):58–65. doi: 10.1016/j.vetpar.2009.06.021 CrossRefPubMedGoogle Scholar
  27. Pezeshki A, Akhlaghi L, Sharbatkhori M, Razmjou E, Oormazdi H, Mohebali M, Meamar A (2013) Genotyping of Echinococcus granulosus from domestic animals and humans from Ardabil Province, northwest Iran. J Helminthol 10:10Google Scholar
  28. Piccoli L, Bazzocchi C, Brunetti E, Mihailescu P, Bandi C, Mastalier B, Cordos I, Beuran M, Popa L, Meroni V (2013) Molecular characterization of Echinococcus granulosus in south-eastern Romania: evidence of G1–G3 and G6–G10 complexes in humans. Clin Microbiol Infect 19(6):578–582. doi: 10.1111/j.1469-0691.2012.03993.x CrossRefPubMedGoogle Scholar
  29. Pour AA, Hosseini SH, Shayan P (2011) Comparative genotyping of Echinococcus granulosus infecting buffalo in Iran using cox1 gene. Parasitol Res 108(5):1229–1234. doi: 10.1007/s00436-010-2170-x CrossRefPubMedGoogle Scholar
  30. Rokni MB (2009) Echinococcosis/hydatidosis in Iran. Iran J Parasitol 4:1–16Google Scholar
  31. Sánchez E, Cáceres O, Náquira C, Garcia D, Patiño G, Silvia H, Volotão AC, Fernandes O (2010) Molecular characterization of Echinococcus granulosus from Peru by sequencing of the mitochondrial cytochrome C oxidase subunit 1 gene. Mem Inst Oswaldo Cruz 105:806–810. doi: 10.1590/S0074-02762010000600013 CrossRefPubMedGoogle Scholar
  32. Schantz P (1995) Epidemiology and control of hydatid disease. In Thompson RCA, Lymbery AJ (eds) Echinococcus and hydatid disease, CAB International, Oxon, pp 233–331Google Scholar
  33. Schantz P (2003) Echinococcus species (agents of cystic, alveolar, and polycystic echinococcosis). Principles and practice of pediatric infectious diseases, 2nd edn. Churchill-Livingstone, New York, pp 1357–1361Google Scholar
  34. Schneider R, Gollackner B, Schindl M, Tucek G, Auer H (2010) Echinococcus canadensis G7 (pig strain): an underestimated cause of cystic echinococcosis in Austria. Am J Trop Med Hyg 82(5):871. doi: 10.4269/ajtmh.2010.09-0639 CrossRefPubMedCentralPubMedGoogle Scholar
  35. Sharifiyazdi H, Oryan A, Ahmadnia S, Valinezhad A (2011) Genotypic characterization of Iranian camel (Camelus dromedarius) isolates of Echinoccocus granulosus. J Parasitol 97:251–255. doi: 10.1645/GE-2642.1 CrossRefPubMedGoogle Scholar
  36. Sharma M, Sehgal R, Ahmad Fomda B, Malhotra A (2013) Molecular characterization of Echinococcus granulosus cysts in north Indian patients: identification of G1, G3, G5 and G6 genotypes. PLoS Negl Trop Dis 7:6. doi: 10.1371/journal.pntd.0002262 CrossRefGoogle Scholar
  37. Simsek S, Balkaya I, Ciftci AT, Utuk AE (2011) Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Vet Parasitol 178:367–369. doi: 10.1016/j.vetpar.2011.01.033 CrossRefPubMedGoogle Scholar
  38. Thompsom R (2008) The taxonomy, phylogeny and transmission of Echinococcus. Exp Parasitol 119(4):439–446. doi: 10.1016/j.exppara.2008.04.016 CrossRefGoogle Scholar
  39. Umhang G, Richomme C, Boucher JM, Hormaz V, Boué F (2013) Prevalence survey and first molecular characterization of Echinococcus granulosus in France. Parasitol Res 112:1809–1812. doi: 10.1007/s00436-012-3245-7 CrossRefPubMedGoogle Scholar
  40. Utuk AE, Simsek S, Koroglu E, Mcmanus DP (2008) Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta Trop 107:192–194. doi: 10.1016/j.actatropica.2008.05.026 CrossRefPubMedGoogle Scholar
  41. Varcasia A, Canu S, Lightowlers MW, Scala A, Garippa G (2006) Molecular characterization of Echinococcus granulosus strains in Sardinia. Parasitol Res 98(3):273–277. doi: 10.1007/S00436-005-0059-X CrossRefPubMedGoogle Scholar
  42. Varcasia A, Canu S, Kogkos A, Pipia AP, Scala A, Garippa G, Seimenis A (2007) Molecular characterization of Echinococcus granulosus in sheep and goats of Peloponnesus, Greece. Parasitol Res 101:1135–1139. doi: 10.1007/s00436-007-0568-x CrossRefPubMedGoogle Scholar
  43. Vural G, Baca AU, Gauci CG, Bagci O (2008) 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 154:347–350. doi: 10.1016/j.vetpar.2008.03.020 CrossRefPubMedGoogle Scholar
  44. Youssefi MR, Tabaripour R, Omrani VF, Spotin A, Esfandiari B (2013) Genotypic characterization of Echinococcus granulosus in Iranian goats. Asian Pac J Trop Dis 3:362–366CrossRefGoogle Scholar

Copyright information

© Indian Society for Parasitology 2014

Authors and Affiliations

  • Mahmoud Mahami Oskouei
    • 1
    • 2
  • Nader Ghabouli Mehrabani
    • 1
    • 2
    Email author
  • Abolfazl Miahipour
    • 1
    • 2
  • Esmaeil Fallah
    • 2
  1. 1.Tabriz Infectious and Tropical Diseases Research CenterTabriz University of Medical SciencesTabrizIran
  2. 2.Department of Parasitology, Faculty of MedicineTabriz University of Medical SciencesTabrizIran

Personalised recommendations