Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T06:28:22.987Z Has data issue: false hasContentIssue false
  • English
  • Français

Genotyping and phylogenetic analysis of unusually located hydatid cysts isolated from humans in north-east Iran

Published online by Cambridge University Press:  23 July 2019

R. Shafiei ,
M.A. Ghatee ,
F. Jafarzadeh ,
Z. Javanshir  and
M. Karamian Open the ORCID record for M. Karamian [Opens in a new window]
R. Shafiei
Affiliation:
Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran
M.A. Ghatee
Affiliation:
Cellular and Molecular Research Center, Yasuj University of Medical Sciences, Yasuj, Iran Department of Parasitology, School of Medicine, Yasuj University of Medical Sciences, Yasuj, Iran
F. Jafarzadeh
Affiliation:
Department of Parasitology, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Z. Javanshir
Affiliation:
Student Research Committee, North Khorasan University of Medical Sciences, Bojnurd, Iran
M. Karamian*
Affiliation:
Cellular and Molecular Research Center, Birjand University of Medical Sciences, Birjand, Iran
*
Author for correspondence: Mehdi Karamian, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite several studies conducted to determine the genotypes of cystic echinococcosis (CE) agents in humans and other intermediate hosts, the relationship between parasite genotype and clinical presentation of hydatidosis is yet to be well defined. The aim of this study was to compare the genotypes/haplotypes of CE agents of human extra-hepatopulmonary hydatid cysts and common hydatid cysts of the liver. A comparative analysis was carried out between partial cox1 sequences of ten extra-hepatopulmonary hydatid cysts, two liver cysts and reliable sequences from the GenBank database. All the studied hydatid cysts had the Echinococcus granulosus sensu stricto (G1-G2-G3) genotypes. The liver CE cysts were caused by common G1 genotype, while six of the extra-hepatopulmonary cysts had genotypes different from common G1 cysts. The sequences of these six isolates were identical to the G2 and G3 genotypes of E. granulosus sensu stricto; the kidney and peritoneum cysts and most of the brain cysts were identified as G2 genotype, while G3 genotype was only reported in a cyst belonging to the pelvic region. Given the observed differences between the sequences of hydatid cysts, it seems that the replacement of hydatid cysts in organs other than the liver and lungs can be related to their genotypes and probably intra-genotypic characteristics. It was hypothesized that in each geographic area, less frequent genotypes were likely to be more consistent with placement in the host's unusual organs.

Keywords

Echinococcus granulosusextra-hepatopulmonaryG2 gonotypeG3 genotypephylogenetics
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e64
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbassioun, K and Amirjamshidi, A (2001) Diagnosis and management of hydatid cyst of the central nervous system: part 1: general considerations and hydatid disease of the brain. Neurosurgery Quarterly 11, 1–9.Google Scholar
Addy, F, Wassermann, M, Kagendo, D, et al. (2017) Genetic differentiation of the G6/7 cluster of Echinococcus canadensis based on mitochondrial marker genes. International Journal for Parasitology 47, 923–931.Google Scholar
Aksakal, N, Kement, M, Okkabaz, N, Altuntaş, YE and Öncel, M (2016) Unusually located primary hydatid cysts. Turkish Journal of Surgery/Ulusal cerrahi dergisi 32, 130–133.Google Scholar
Beato, S, Parreira, R, Roque, C, Gonçalves, M, Silva, L, Maurelli, MP, Cringoli, G and Grácio, MA (2013) Echinococcus granulosus in Portugal: the first report of the G7 genotype in cattle. Veterinary Parasitology 198, 235–239.Google Scholar
Beyhan, YE and Umur, Ş (2011) Molecular characterization and prevalence of cystic Echinococcosis in slaughtered water buffaloes in Turkey. Veterinary Parasitology 181, 174–179.Google Scholar
Bhattacharya, D, Bera, AK, Bera, BC, Maity, A and Das, SK (2007) Genotypic characterisation of Indian cattle, buffalo and sheep isolates of Echinococcus granulosus. Veterinary Parasitology 143, 371–374.Google Scholar
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.Google Scholar
Cao, M, Chen, K, Li, W, Ma, J, Xiao, Z, Wang, H and Gao, J (2018) Genetic characterization of human-derived hydatid fluid based on mitochondrial gene sequencing in individuals from northern and western China. Journal of Helminthology, 1–5. doi:10.1017/S0022149X18000883.Google Scholar
Ciurea, AV, Fountas, KN, Coman, TC, Machinis, TG, Kapsalaki, EZ, Fezoulidis, NI and Robinson, JS (2006) Long-term surgical outcome in patients with intracranial hydatid cyst. Acta Neurochirurgica 148, 421–426.Google Scholar
Fadakar, B, Tabatabaei, N, Borji, H and Naghibi, A (2015) Genotyping of Echinococcus granulosus from goats and sheep indicating G7 genotype in goats in the Northeast of Iran. Veterinary Parasitology 214, 204–207.Google Scholar
Geramizadeh, B (2013) Unusual locations of the hydatid cyst: a review from Iran. Iranian Journal of Medical Sciences 38, 2–14.Google Scholar
Geramizadeh, B (2017) Isolated peritoneal, mesenteric, and omental hydatid cyst: a clinicopathologic narrative review. Iranian Journal of Medical Sciences 42, 517–523.Google Scholar
Gholami, S, Jahandar, H, Abastabar, M, Pagheh, A, Mobedi, I and Sharbatkhori, M (2016) Echinococcus granulosus sensu stricto in dogs and jackals from Caspian Sea region, northern Iran. Iranian Journal of Parasitology 11, 186–194.Google Scholar
Gorgani-Firouzjaee, T, Kalantrai, N, Ghaffari, S, Alipour, J and Siadati, S (2019) Genotype characterization of livestock and human cystic echinococcosis in Mazandaran province, Iran. Journal of Helminthology 93, 255–259.Google Scholar
Hall, T, Biosciences, I and Carlsbad, C (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2, 60–61.Google Scholar
Hamamci, EO, Besim, H and Korkmaz, A (2004) Unusual locations of hydatid disease and surgical approach. ANZ Journal of Surgery 74, 356–360.Google Scholar
Kamelli, M, Borji, H and Naghibi, A (2016) Genetic identification of cattle hydatid cyst isolates from northeast and southwest of Iran. Annals of Parasitology 62, 301–305.Google Scholar
Karakoc, ZC, Kasimcan, MO, Pipia, AP, Tore, G, Alberti, A, Varcasia, A, Sav, A and Oruçkaptan, H (2016) A life-threatening brainstem compression by cerebral Echinococcus granulosus. Le infezioni in medicina: rivista periodica di eziologia, epidemiologia, diagnostica, clinica e terapia delle patologie infettive 24, 62–66.Google Scholar
Karamian, M, Haghighi, F, Hemmati, M, Taylor, WR, Salehabadi, A and Ghatee, MA (2017) Heterogenity of Echinococcus canadensis genotype 6− the main causative agent of cystic echinococcosis in Birjand, Eastern Iran. Veterinary Parasitology 245, 78–85.Google Scholar
Khademvatan, S, Majidiani, H, Foroutan, M, Tappeh, KH, Aryamand, S and Khalkhali, HR (2019) Echinococcus granulosus genotypes in Iran: a systematic review. Journal of Helminthology 93, 131–138.Google Scholar
Kinkar, L, Laurimäe, T, Sharbatkhori, M, et al. (2017) New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto. Infection, Genetics and Evolution 52, 52–58.Google Scholar
Laatamna, AE, Ebi, D, Brahimi, K, Bediaf, K, Wassermann, M, Souttou, K and Romig, T (2019) Frequency and genetic diversity of Echinococcus granulosus sensu stricto in sheep and cattle from the steppe region of Djelfa, Algeria. Parasitology Research 118, 89–96.Google Scholar
Laurimäe, T, Kinkar, L, Moks, E, et al. (2018) Molecular phylogeny based on six nuclear genes suggests that Echinococcus granulosus sensu lato genotypes G6/G7 and G8/G10 can be regarded as two distinct species. Parasitology 145, 1929–1937.Google Scholar
Lockyer, AE, Olson, PD, Østergaard, P, et al. (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203–224.Google Scholar
Moghaddas, E, Borji, H, Naghibi, A, Shayan, P and Razmi, GR (2015) Molecular genotyping of Echinococcus granulosus from dromedaries (Camelus dromedarius) in eastern Iran. Journal of Helminthology 89, 100–104.Google Scholar
Morgan, JA, DeJong, RJ, Kazibwe, F, Mkoji, GM and Loker, ES (2003) A newly-identified lineage of Schistosoma. International Journal for Parasitology 33, 977–985.Google Scholar
Moudgil, AD, Moudgil, P, Asrani, RK and Agnihotri, RK (2019) Hydatidosis in slaughtered sheep and goats in India: prevalence, genotypic characterization and pathological studies. Journal of Helminthology, 1–5. doi:10.1017/S0022149X18001219.Google Scholar
Nakao, M, Lavikainen, A, Yanagida, T and Ito, A (2013) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). International Journal for Parasitology 43, 1017–1029.Google Scholar
Oudni-M'Rad, M, Cabaret, J, M'rad, S, Chaâbane-Banaoues, R, Mekki, M, Zmantar, S, Nouri, A, Mezhoud, H and Babba, H (2016) Genetic relationship between the Echinococcus granulosus sensu stricto cysts located in lung and liver of hosts. Infection, Genetics and Evolution 44, 356–360.Google Scholar
Pezeshki, A, Akhlaghi, L, Sharbatkhori, M, Razmjou, E, Oormazdi, H, Mohebali, M and Meamar, AR (2013) Genotyping of Echinococcus granulosus from domestic animals and humans from Ardabil Province, northwest Iran. Journal of Helminthology 87, 387–391.Google Scholar
Rostami, S, Torbaghan, SS, Dabiri, S, Babaei, Z, Mohammadi, MA, Sharbatkhori, M and Harandi, MF (2015) Genetic characterization of Echinococcus granulosus from a large number of formalin-fixed, paraffin-embedded tissue samples of human isolates in Iran. The American Journal of Tropical Medicine and Hygiene 92, 588–594.Google Scholar
Sadjjadi, SM, Mikaeili, F, Karamian, M, Maraghi, S, Sadjjadi, FS, Shariat-Torbaghan, S and Kia, EB (2013) Evidence that the Echinococcus granulosus G6 genotype has an affinity for the brain in humans. International Journal for Parasitology 43, 875–877.Google Scholar
Salamone, G, Licari, L, Randisi, B, et al. (2016) Uncommon localizations of hydatid cyst. Review of the literature. Il Giornale di chirurgia 37, 180–185.Google Scholar
Salehi, M, Adinezade, A, Khodajo, R, Saberi, Z and Yousefi, A (2013) The epidemiologic survey of operated patients with hydatid cyst in hospitals of North Khorasan province during 2010–2011. Journal of North Khorasan University of Medical Sciences 4, 623–629 (in Persian).Google Scholar
Schneider, R, Gollackner, B, Edel, B, Schmid, K, Wrba, F, Tucek, G, Walochnik, J and 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. International Journal for Parasitology 38, 1065–1071.Google Scholar
Shafiei, R, Teshnizi, SH, Kalantar, K, Gholami, M, Mirzaee, G and Mirzaee, F (2016) The seroprevalence of human cystic echinococcosis in Iran: a systematic review and meta-analysis study. Journal of Parasitology Research 2016, 1425147.Google Scholar
Sharbatkhori, M, Tanzifi, A, Rostami, S, Rostami, M and Harandi, MF (2016) Echinococcus granulosus sensu lato genotypes in domestic livestock and humans in Golestan province, Iran. Revista do Instituto de Medicina Tropical de São Paulo 58, 38.Google Scholar
Sharma, M, Sehgal, R, Fomda, BA, Malhotra, A and Malla, N (2013) Molecular characterization of Echinococcus granulosus cysts in north Indian patients: identification of G1, G3, G5 and G6 genotypes. PLoS Neglected Tropical Diseases 7, e2262.Google Scholar
Shirmen, O, Batchuluun, B, Lkhamjav, A, et al. (2018) Cerebral cystic echinococcosis in Mongolian children caused by Echinococcus canadensis. Parasitology International 67, 584–586.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Thompson, RC (2017) Biology and systematics of Echinococcus. Advances in Parasitology 95, 65–109.Google Scholar
Tsaroucha, AK, Polychronidis, AC, Lyrantzopoulos, N, Pitiakoudis, MS, Karayiannakis, AJ, Manolas, KJ and Simopoulos, CE (2005) Hydatid disease of the abdomen and other locations. World Journal of Surgery 29, 1161–1165.Google Scholar
Vural, G, Baca, AU, Gauci, CG, Bagci, O, Gicik, Y and Lightowlers, MW (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. Veterinary Parasitology 154, 347–350.Google Scholar