Molecular Characterization of Echinococcus Granulosus Isolates from Bulgarian Human Cystic Echinococcosis Patients

Overview

Journal Parasitol Res

Specialty Parasitology

Date 2017 Jan 23

PMID 28110440

Citations 7

Authors

Irina Marinova

Markus Spiliotis

Junhua Wang

Marin Muhtarov

Ilias Chaligiannis

Smaro Sotiraki

Iskra Rainova

Bruno Gottstein

Ghalia Boubaker

Affiliations

Soon will be listed here.

Abstract

Although cystic echinococcosis (CE) is highly endemic in Bulgaria, there is still scarce information about species and/or genotypes of the Echinococcus granulosus complex that infect humans. Our study tackled the genetic diversity of E. granulosus complex in a cohort of 30 Bulgarian CE patients. Ten animal E. granulosus isolates from neighboring Greece were additionally included. Specimens were comparatively analyzed for partial sequences of five mitochondrial (mt) (cox I, nad I, rrnS, rrnL, and atp6) and three nuclear (nc) genes (act II, hbx 2, and ef-1α) using a PCR-sequencing approach. All 30 Bulgarian isolates were identified as E. granulosus sensu stricto (s.s.) and were showing identical sequences for each of the three examined partial nc gene markers. Based upon concatenated sequences from partial mtDNA markers, we detected 10 haplotypes: 6 haplotypes (H1-H6) clustering with E. granulosus s.s. (G1) and 4 haplotypes (H9-H13) grouping with E. granulosus s.s. (G3), with H1 and H10 being the most frequent in Bulgarian patients. The haplotypes H1, H4, and H11 were also present in Greek hydatid cyst samples of animal origin. In conclusion, E. granulosus s.s. (G1 and G3 genotypes) is the only causative agent found so far to cause human CE in Bulgaria. However, further studies including larger sample sizes and other additional geographic regions in Bulgaria will have to be performed to confirm our results.

Citing Articles

Epidemiological and genotypic assessment of cystic echinococcosis in ruminant populations of Northern Punjab, Pakistan: a neglected zoonotic disease.

Khan S, Cable J, Masud N, Hailer F, Younus M, Hussain N Parasitol Res. 2025; 124(1):7.

PMID: 39821816 PMC: 11739240. DOI: 10.1007/s00436-025-08451-x.

Establishment and application of unbiased in vitro drug screening assays for the identification of compounds against Echinococcus granulosus sensu stricto.

Kaethner M, Preza M, Kaempfer T, Zumstein P, Tamponi C, Varcasia A PLoS Negl Trop Dis. 2023; 17(8):e0011343.

PMID: 37540716 PMC: 10431624. DOI: 10.1371/journal.pntd.0011343.

Molecular Epidemiology of Cystic Echinococcosis in Rural Baluchistan, Pakistan: A Cross-Sectional Study.

Ullah I, Sattar S, Ali I, Farid A, Ullah A, Eid R Pathogens. 2023; 12(1).

PMID: 36678388 PMC: 9863174. DOI: 10.3390/pathogens12010040.

Alveolar echinococcosis in nutria (), invasive species in Slovenia.

Krizman M, Svara T, Soba B, Rataj A Int J Parasitol Parasites Wildl. 2022; 18:221-224.

PMID: 35783071 PMC: 9241068. DOI: 10.1016/j.ijppaw.2022.06.004.

Species and genotypes belonging to Echinococcus granulosus sensu lato complex causing human cystic echinococcosis in Europe (2000-2021): a systematic review.

Casulli A, Massolo A, Saarma U, Umhang G, Santolamazza F, Santoro A Parasit Vectors. 2022; 15(1):109.

PMID: 35346335 PMC: 8962544. DOI: 10.1186/s13071-022-05197-8.

References

. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011 has been published. Euro Surveill. 2013; 18(15):20449. View

Zhang T, Yang D, Zeng Z, Zhao W, Liu A, Piao D . Genetic characterization of human-derived hydatid cysts of Echinococcus granulosus sensu lato in Heilongjiang Province and the first report of G7 genotype of E. canadensis in humans in China. PLoS One. 2014; 9(10):e109059. PMC: 4199617. DOI: 10.1371/journal.pone.0109059. View

Varcasia A, Canu S, Kogkos A, Pipia A, Scala A, Garippa G . Molecular characterization of Echinococcus granulosus in sheep and goats of Peloponnesus, Greece. Parasitol Res. 2007; 101(4):1135-9. DOI: 10.1007/s00436-007-0568-x. View

Sharbatkhori M, Harandi M, Mirhendi H, Hajialilo E, Kia E . Sequence analysis of cox1 and nad1 genes in Echinococcus granulosus G3 genotype in camels (Camelus dromedarius) from central Iran. Parasitol Res. 2010; 108(3):521-7. DOI: 10.1007/s00436-010-2092-7. View

Dybicz M, Borkowski P, Dabrowska J, Chomicz L . Cases of Echinococcus granulosus Sensu Stricto Isolated from Polish Patients: Imported or Indigenous?. Biomed Res Int. 2015; 2015:728321. PMC: 4605230. DOI: 10.1155/2015/728321. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Thompson R, Boxell A, Ralston B, Constantine C, Hobbs R, Shury T . Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology. 2005; 132(Pt 3):439-47. DOI: 10.1017/S0031182005009170. View

Cann R, Stoneking M, Wilson A . Mitochondrial DNA and human evolution. Nature. 1987; 325(6099):31-6. DOI: 10.1038/325031a0. View

Cucher M, Macchiaroli N, Baldi G, Camicia F, Prada L, Maldonado L . Cystic echinococcosis in South America: systematic review of species and genotypes of Echinococcus granulosus sensu lato in humans and natural domestic hosts. Trop Med Int Health. 2015; 21(2):166-75. DOI: 10.1111/tmi.12647. View

10.

Bart J, Morariu S, Knapp J, Ilie M, Pitulescu M, Anghel A . Genetic typing of Echinococcus granulosus in Romania. Parasitol Res. 2005; 98(2):130-7. DOI: 10.1007/s00436-005-0015-9. View

11.

Jenkins D, Romig T, Thompson R . Emergence/re-emergence of Echinococcus spp.--a global update. Int J Parasitol. 2005; 35(11-12):1205-19. DOI: 10.1016/j.ijpara.2005.07.014. View

12.

Eckert J, Deplazes P . Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev. 2004; 17(1):107-35. PMC: 321468. DOI: 10.1128/CMR.17.1.107-135.2004. View

13.

Beato S, Parreira R, Calado M, Gracio M . Apparent dominance of the G1-G3 genetic cluster of Echinococcus granulosus strains in the central inland region of Portugal. Parasitol Int. 2010; 59(4):638-42. DOI: 10.1016/j.parint.2010.08.004. View

14.

Bobic B, Nikolic A, Radivojevic S, Klun I, Djurkovic-Djakovic O . Echinococcosis in Serbia: an issue for the 21st century?. Foodborne Pathog Dis. 2012; 9(11):967-73. DOI: 10.1089/fpd.2012.1227. View

15.

Zait H, Kouidri M, Grenouillet F, Umhang G, Millon L, Hamrioui B . Molecular characterization of Echinococcus granulosus sensu stricto and Echinococcus canadensis in humans and livestock from Algeria. Parasitol Res. 2016; 115(6):2423-31. DOI: 10.1007/s00436-016-4994-5. View

16.

Wang J, Wang N, Hu D, Zhong X, Wang S, Gu X . Genetic diversity of Echinococcus granulosus in southwest China determined by the mitochondrial NADH dehydrogenase subunit 2 gene. ScientificWorldJournal. 2014; 2014:867839. PMC: 3925532. DOI: 10.1155/2014/867839. View

17.

Bowles J, McManus D . NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol. 1993; 23(7):969-72. DOI: 10.1016/0020-7519(93)90065-7. View

18.

Felsenstein J . CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP. Evolution. 2017; 39(4):783-791. DOI: 10.1111/j.1558-5646.1985.tb00420.x. View

19.

Romig T, Ebi D, Wassermann M . Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol. 2015; 213(3-4):76-84. DOI: 10.1016/j.vetpar.2015.07.035. View

20.

Lymbery A, Jenkins E, Schurer J, Thompson R . Echinococcus canadensis, E. borealis, and E. intermedius. What's in a name?. Trends Parasitol. 2014; 31(1):23-9. DOI: 10.1016/j.pt.2014.11.003. View