Volume 92, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Cystic echinococcosis (CE), caused by the larval stage of , presents an important medical and veterinary problem globally, including that in Iran. Different genotypes of have been reported from human isolates worldwide. This study identifies the genotype of the parasite responsible for human hydatidosis in three provinces of Iran using formalin-fixed paraffin-embedded tissue samples. In this study, 200 formalin-fixed paraffin-embedded tissue samples from human CE cases were collected from Alborz, Tehran, and Kerman provinces. Polymerase chain reaction amplification and sequencing of the partial mitochondrial cytochrome oxidase subunit 1 gene were performed for genetic characterization of the samples. Phylogenetic analysis of the isolates from this study and reference sequences of different genotypes was done using a maximum likelihood method. In total, 54.4%, 0.8%, 1%, and 40.8% of the samples were identified as the G1, G2, G3, and G6 genotypes, respectively. The findings of the current study confirm the G1 genotype (sheep strain) to be the most prevalent genotype involved in human CE cases in Iran and indicates the high prevalence of the G6 genotype with a high infectivity for humans. Furthermore, this study illustrates the first documented human CE case in Iran infected with the G2 genotype.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Thompson RC, , 2008. The taxonomy, phylogeny and transmission of Echinococcus . Exp Parasitol 119: 439446.[Crossref] [Google Scholar]
  2. Budke CM, Deplazes P, Torgerson PR, , 2006. Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12: 296303.[Crossref] [Google Scholar]
  3. Thompson RCA, McManus DP, Eckert J, Gemmell MA, Meslin F-X, Pawlowski ZS, , 2002. Aetiology: parasites and life-cycles. In: , eds., WHO/OIE. Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Chapter 1, pp. 119. [Google Scholar]
  4. McManus DP, Zhang W, Li J, Bartley PB, , 2003. Echinococcosis. Lancet 362: 12951304.[Crossref] [Google Scholar]
  5. Sadjjadi S, , 2006. Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol Int 55 (Suppl): S197S202.[Crossref] [Google Scholar]
  6. Shareif M, , 2000. The prevalence of hydatid cyst infection in slaughtered animals. J Shahid Sadoughi Univ Med Sci Health Services 8: 8084. [Google Scholar]
  7. Rokni M, , 2009. Echinococcosis/hydatidosis in Iran. Iran J Parasitol 4: 116. [Google Scholar]
  8. Ahmadi N, , 2005. Hydatidosis in camels (Camelus dromedarius) and their potential role in the epidemiology of Echinococcus granulosus in Iran. J Helminthol 79: 119125.[Crossref] [Google Scholar]
  9. Arbabi M, Massoud J, Dalimi-Asl A, Sadjjadi S, , 1998. Prevalence of hydatidosis in slaughtered animals in Hamedan. Daneshvar Sci Res J Shahed Univ 5: 5761. [Google Scholar]
  10. Dalimi A, Motamedi G, Hosseini M, Mohammadian B, Malaki H, Ghamari Z, Far FG, , 2002. Echinococcosis/hydatidosis in western Iran. Vet Parasitol 105: 161171.[Crossref] [Google Scholar]
  11. Eslami A, Hosseini SH, , 1998. Echinococcus granulosus infection of farm dogs of Iran. Parasitol Res 84: 205207.[Crossref] [Google Scholar]
  12. Fallah M, Taherkhani H, Sadjjadi S, , 1995. Echinococcosis in stray dogs in Hamedan, west of Iran. Iran J Med Sci 29: 170172. [Google Scholar]
  13. Maleky F, Moradkhan M, , 2000. Echinococcosis in the stray dogs of Tehran, Iran. Ann Trop Med Parasitol 94: 329331.[Crossref] [Google Scholar]
  14. Mehrabani D, Oryan A, Sadjjadi SM, , 1999. Prevalence of Echinococcus granulosus infection in stray dogs and herbivores in Shiraz, Iran. Vet Parasitol 86: 217220.[Crossref] [Google Scholar]
  15. Mohammadzadeh Hajipirloo H, Bozorgomid A, Alinia T, Hazrati Tappeh K, Mahmodlou R, , 2013. Human cystic echinococcosis in West Azerbaijan, Northwest Iran: a retrospective hospital-based survey from 2000 to 2009. Iran J Parasitol 8: 323326. [Google Scholar]
  16. Fasihi Harandi M, Budke CM, Rostami S, , 2012. The monetary burden of cystic echinococcosis in Iran. PLoS Negl Trop Dis 6: e1915.[Crossref] [Google Scholar]
  17. McManus DP, , 2013. Current status of the genetics and molecular taxonomy of Echinococcus species. Parasitol 140: 16171623.[Crossref] [Google Scholar]
  18. McManus DP, Thompson RC, , 2003. Molecular epidemiology of cystic echinococcosis. Parasitol 127 (Suppl): S37S51.[Crossref] [Google Scholar]
  19. Lavikainen A, Lehtinen MJ, Laaksonen S, Agren E, Oksanen A, Meri S, , 2006. Molecular characterization of Echinococcus isolates of cervid origin from Finland and Sweden. Parasitol 133: 565570.[Crossref] [Google Scholar]
  20. Eckert J, Thompson RCA, , 1997. Intraspecific variation of Echinococcus granulosus and related species with emphasis on their infectivity to humans. Acta Trop 64: 1934.[Crossref] [Google Scholar]
  21. Moks E, Jogisalu I, Valdmann H, Saarma U, , 2008. First report of Echinococcus granulosus G8 in Eurasia and a reappraisal of the phylogenetic relationships of ‘genotypes’ G5–G10. Parasitol 135: 647654.[Crossref] [Google Scholar]
  22. Nakao M, McManus DP, Schantz PM, Craig PS, Ito A, , 2007. A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitol 134: 713722.[Crossref] [Google Scholar]
  23. Huttner M, Romig T, , 2009. Echinococcus species in African wildlife. Parasitol 136: 10891095.[Crossref] [Google Scholar]
  24. Saarma U, Jogisalu I, Moks E, Varcasia A, Lavikainen A, Oksanen A, Simsek S, Andresiuk V, Denegri G, Gonzalez LM, Ferrer E, Garate T, Rinaldi L, Marvilla P, , 2009. A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence. Parasitol 136: 317328.[Crossref] [Google Scholar]
  25. 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, , 2010. Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. Int J Parasitol 40: 379385.[Crossref] [Google Scholar]
  26. Moro P, Schantz PM, , 2009. Echinococcosis: a review. Int J Infect Dis 13: 125133.[Crossref] [Google Scholar]
  27. Zhang L, Eslami A, Hosseini SH, McManus DP, , 1998. Indication of the presence of two distinct strains of Echinococcus granulosus in Iran by mitochondrial DNA markers. Am J Trop Med Hyg 59: 171174. [Google Scholar]
  28. Harandi MF, Hobbs RP, Adams PJ, Mobedi I, Morgan-Ryan UM, Thompson RCA, , 2002. Molecular and morphological characterization of Echinococcus granulosus of human and animal origin in Iran. Parasitol 125: 367373. [Google Scholar]
  29. Hajialilo E, Fasihi Harandi M, 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: 263270.[Crossref] [Google Scholar]
  30. Sharbatkhori M, Fasihi Harandi M, Mirhendi H, Hajialilo E, Kia E, , 2011. Sequence analysis of cox1 and nad1 genes in Echinococcus granulosus G3 genotype in camels (Camelus dromedarius) from central Iran. Parasitol Res 108: 521527.[Crossref] [Google Scholar]
  31. Sharbatkhori M, Mirhendi H, Harandi MF, Rezaeian M, Mohebali M, Eshraghian M, Rahimi H, Kia EB, , 2010. Echinococcus granulosus genotypes in livestock of Iran indicating high frequency of G1 genotype in camels. Exp Parasitol 124: 373379.[Crossref] [Google Scholar]
  32. Sharbatkhori M, Mirhendi H, Jex AR, Pangasa A, Campbell BE, Kia EB, Eshraghian MR, Harandi MF, Gasser RB, , 2009. Genetic categorization of Echinococcus granulosus from humans and herbivorous hosts in Iran using an integrated mutation scanning-phylogenetic approach. Electrophoresis 30: 26482655.[Crossref] [Google Scholar]
  33. Dalimi A, Sattari A, Motamedi G, , 2006. A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Vet Parasitol 142: 129133.[Crossref] [Google Scholar]
  34. Rajabloo M, Hosseini SH, Jalousian F, , 2012. Morphological and molecular characterization of Echinococcus granulosus from goat isolates in Iran. Acta Trop 123: 6771.[Crossref] [Google Scholar]
  35. Amin Pour A, Hosseini SH, Shayan P, , 2011. Comparative genotyping of Echinococcus granulosus infecting buffalo in Iran using cox1 gene. Parasitol Res 108: 12291234.[Crossref] [Google Scholar]
  36. 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: 4752. [Google Scholar]
  37. Parsa F, Fasihi Harandi M, Rostami S, Sharbatkhori M, , 2012. Genotyping Echinococcus granulosus from dogs from Western Iran. Exp Parasitol 132: 308312.[Crossref] [Google Scholar]
  38. Kia EB, Rahimi H, Sharbatkhori M, Talebi A, Fasihi Harandi M, Mirhendi H, , 2010. Genotype identification of human cystic echinococcosis in Isfahan, central Iran. Parasitol Res 107: 757760.[Crossref] [Google Scholar]
  39. Moro PL, Nakao M, Ito A, Schantz PM, Cavero C, Cabrera L, , 2009. Molecular identification of Echinococcus isolates from Peru. Parasitol Int 58: 184186.[Crossref] [Google Scholar]
  40. Shahnazi M, Hejazi H, Salehi M, Andalib AR, , 2011. Molecular characterization of human and animal Echinococcus granulosus isolates in Isfahan, Iran. Acta Trop 117: 4750.[Crossref] [Google Scholar]
  41. Khademvatan S, Yousefi E, Rafiei A, Rahdar M, Saki J, , 2013. Molecular characterization of livestock and human isolates of Echinococcus granulosus from south-west Iran. J Helminthol 87: 240244.[Crossref] [Google Scholar]
  42. Gholami S, Sosari M, Fakhar M, Sharif M, Daryani A, Hashemi M, Vahadi M, , 2012. Molecular characterization of Echinococcus granulosus from hydatid cysts isolated from human and animals in Golestan Province, North of Iran. Iran J Parasitol 7: 816. [Google Scholar]
  43. Manterola C, Benavente F, Melo A, Vial M, Roa JC, , 2008. Description of Echinococcus granulosus genotypes in human hydatidosis in a region of southern Chile. Parasitol Int 57: 342346.[Crossref] [Google Scholar]
  44. Pezeshki A, Akhlaghi L, Sharbatkhori M, Razmjou E, Oormazdi H, Mohebali M, Meamar AR, , 2013. Genotyping of Echinococcus granulosus from domestic animals and humans from Ardabil Province, northwest Iran. J Helminthol 87: 387391.[Crossref] [Google Scholar]
  45. Bowles J, Blair D, McManus DP, , 1992. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54: 165173.[Crossref] [Google Scholar]
  46. Schneider R, Gollackner B, Edel B, Schmid K, Wrba F, Tucek G, Walochnik J, Auer H, , 2008. Development of a new PCR protocol for the detection of species and genotypes (strains) of Echinococcus in formalin-fixed, paraffin-embedded tissues. Int J Parasitol 38: 10651071.[Crossref] [Google Scholar]
  47. 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: 871874.[Crossref] [Google Scholar]
  48. Sharma M, Sehgal R, Fomda BA, Malhotra A, Malla N, , 2013. Molecular characterization of Echinococcus granulosus cysts in North Indian patients: identification of G1, G3, G5 and G6 genotypes. PLoS Negl Trop Dis 7: e2262.[Crossref] [Google Scholar]
  49. De la Rue ML, Takano K, Brochado JF, Costa CV, Soares AG, Yamano K, Yagi K, Katoh Y, Takahashi K, , 2011. Infection of humans and animals with Echinococcus granulosus (G1 and G3 strains) and E. ortleppi in southern Brazil. Vet Parasitol 177: 97103.[Crossref] [Google Scholar]
  50. Busi M, Snabel V, De Liberato C, D'Amelio S, , 2004. Molecular genotyping of Echinococcus granulosus hydatid cysts in Italy reveals the presence of three distinct genotypes. Parasitologia 46 (Suppl 1): 164. [Google Scholar]
  51. Busi M, Snabel 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: 7583.[Crossref] [Google Scholar]
  52. Šnábel V, Altintas N, D'Amelio S, Nakao M, Romig T, Yolasigmaz A, Gunes K, Turk M, Busi M, Hüttner M, Ševcová D, Ito A, Dubinský P, , 2009. Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitol Res 105: 145154.[Crossref] [Google Scholar]
  53. M'rad S, Oudni-M'rad M, Filisetti D, Mekki M, Nouri A, Sayadi T, Candolfi E, Azaiez R, Mezhoud H, Babba H, , 2010. Molecular identification of Echinococcus granulosus in Tunisia: first record of the Buffalo strain (G3) in human and bovine in the country. Open Vet Sci J 4: 2730.[Crossref] [Google Scholar]
  54. Simsek S, Kaplan M, Ozercan I, , 2011. A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitol Res 109: 411416.[Crossref] [Google Scholar]
  55. Piccoli L, Bazzocchi C, Brunetti E, Mihailescu P, Bandi C, Mastalier B, Cordos I, Beuran M, Popa LG, Meroni V, Genco F, Cretu C, , 2013. Molecular characterization of Echinococcus granulosus in south-eastern Romania: evidence of G1–G3 and G6–G10 complexes in humans. Clin Microbiol Infect 19: 578582.[Crossref] [Google Scholar]
  56. Ahmadi N, Dalimi A, , 2006. Characterization of Echinococcus granulosus isolates from human, sheep and camel in Iran. Infect Genet Evol 6: 8590.[Crossref] [Google Scholar]
  57. Santivanez SJ, Gutierrez AM, Rosenzvit MC, Muzulin PM, Rodriguez ML, Vasquez JC, Rodriguez S, Gonzalez AE, Gilman RH, Garcia HH, , 2008. Human hydatid disease in Peru is basically restricted to Echinococcus granulosus genotype G1. Am J Trop Med Hyg 79: 8992. [Google Scholar]
  58. Abushhewa MH, Abushhiwa MH, Nolan MJ, Jex AR, Campbell BE, Jabbar A, Gasser RB, , 2010. Genetic classification of Echinococcus granulosus cysts from humans, cattle and camels in Libya using mutation scanning-based analysis of mitochondrial loci. Mol Cell Probes 24: 346351.[Crossref] [Google Scholar]
  59. 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, , 2012. Molecular identification of Echinococcus species from eastern and southern Qinghai, China, based on the mitochondrial cox1 gene. Parasitol Res 111: 179184.[Crossref] [Google Scholar]
  60. Casulli A, Interisano M, Sreter T, Chitimia L, Kirkova Z, La Rosa G, Pozio E, , 2012. Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infect Genet Evol 12: 377383.[Crossref] [Google Scholar]
  61. Ergin S, Saribas S, Yuksel P, Zengin K, Midilli K, Adas G, Arikan S, Aslan M, Uysal H, Caliskan R, Oner A, Kucukbasmaci O, Kaygusuz A, Mamal Torun M, Kocazeybek B, , 2010. Genotypic characterization of Echinococcus granulosus isolated from human in Turkey. Afr J Microbiol Res 4: 551555. [Google Scholar]
  62. Zhang L, Gasser RB, Zhu X, McManus DP, , 1999. Screening for different genotypes of Echinococcus granulosus within China and Argentina by single-strand conformation polymorphism (SSCP) analysis. Trans R Soc Trop Med Hyg 93: 329334.[Crossref] [Google Scholar]
  63. 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: 129136.[Crossref] [Google Scholar]
  64. Guarnera EA, Parra A, Kamenetzky L, Garcia G, Gutierrez A, , 2004. Cystic echinococcosis in Argentina: evolution of metacestode and clinical expression in various Echinococcus granulosus strains. Acta Trop 92: 153159.[Crossref] [Google Scholar]
  65. Badaraco JL, Ayala FJ, Bart JM, Gottstein B, Haag KL, , 2008. Using mitochondrial and nuclear markers to evaluate the degree of genetic cohesion among Echinococcus populations. Exp Parasitol 119: 453459.[Crossref] [Google Scholar]
  66. Bardonnet K, Piarroux R, Dia L, Schneegans F, Beurdeley A, Godot V, Vuitton DA, , 2002. Combined eco-epidemiological and molecular biology approaches to assess Echinococcus granulosus transmission to humans in Mauritania: occurrence of the camel strain and human cystic echinococcosis. Trans R Soc Trop Med Hyg 96: 383386.[Crossref] [Google Scholar]
  67. Abdel Aaty HE, Abdel-Hameed DM, Alam-Eldin YH, El-Shennawy SF, Aminou HA, Makled SS, Darweesh SK, , 2012. Molecular genotyping of Echinococcus granulosus in animal and human isolates from Egypt. Acta Trop 121: 125128.[Crossref] [Google Scholar]
  68. Omer R, Dinkel A, Roming T, Mackenstedt U, Elamin M, Elnahas A, , 2004. Strain characterization of human hydatidosis in Sudan. Int Arch Hydatid 35: 41. [Google Scholar]
  69. Dinkel A, Njoroge EM, Zimmermann A, Walz M, Zeyhle E, Elmahdi IE, Mackenstedt U, Romig T, , 2004. A PCR system for detection of species and genotypes of the Echinococcus granulosus-complex, with reference to the epidemiological situation in eastern Africa. Int J Parasitol 34: 645653.[Crossref] [Google Scholar]
  70. Casulli A, Zeyhle E, Brunetti E, Pozio E, Meroni V, Genco F, Filice C, , 2010. Molecular evidence of the camel strain (G6 genotype) of Echinococcus granulosus in humans from Turkana, Kenya. Trans R Soc Trop Med Hyg 104: 2932.[Crossref] [Google Scholar]
  71. Konyaev SV, Yanagida T, Ingovatova GM, Shoikhet YN, Nakao M, Sako Y, Bondarev AY, Ito A, , 2012. Molecular identification of human echinococcosis in the Altai region of Russia. Parasitol Int 61: 711714.[Crossref] [Google Scholar]
  72. 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. Mol Cell Probes 25: 4954.[Crossref] [Google Scholar]
  73. Bart JM, Abdukader M, Zhang YL, Lin RY, Wang YH, Nakao M, Ito A, Craig PS, Piarroux R, Vuitton DA, Wen H, , 2006. Genotyping of human cystic echinococcosis in Xinjiang, PR China. Parasitol 133: 571579.[Crossref] [Google Scholar]
  74. Zhang LH, Joshi DD, McManus DP, , 2000. Three genotypes of Echinococcus granulosus identified in Nepal using mitochondrial DNA markers. Trans R Soc Trop Med Hyg 94: 258260.[Crossref] [Google Scholar]
  75. Khalifa NO, Khater HF, Fahmy HA, Radwan MEI, Afify JSA, , 2014. Genotyping and phylogenetic analysis of cystic echinococcosis isolated from camels and humans in Egypt. Am J Epidemiol Infect Dis 2: 7482.[Crossref] [Google Scholar]
  76. Kedra A, Swiderski Z, Tkach VV, Dubinsk P, Pawlowski Z, Stefaniak J, Pawlowski J, , 1999. Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia, and Ukraine. A multicenter study. Acta Parasitol 44: 248254. [Google Scholar]
  77. Turcekova L, Snabel V, D'Amelio S, Busi M, Dubinsky P, , 2003. Morphological and genetic characterization of Echinococcus granulosus in the Slovak Republic. Acta Trop 85: 223229.[Crossref] [Google Scholar]
  78. Obwaller A, Schneider R, Walochnik J, Gollackner B, Deutz A, Janitschke K, Aspock H, Auer H, , 2004. Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitol 128: 569575.[Crossref] [Google Scholar]
  79. Eryıldız C, Şakru N, , 2012. Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan Medical Journal 29: 261267. [Google Scholar]
  80. Dybicz M, Gierczak A, Dąbrowska J, Rdzanek Ł, Michałwicz B, , 2013. Molecular diagnosis of cystic echinococcosis in humans from central Poland. Parasitol Int 62: 364367.[Crossref] [Google Scholar]

Data & Media loading...

  • Received : 16 Sep 2014
  • Accepted : 14 Nov 2014
  • Published online : 04 Mar 2015

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error