Use of the EmsB microsatellite-based next generation sequencing for genotyping of Echinococcus granulosus sensu lato in hydatid cyst tissue samples from animals and humans

. 2024 Aug 05 ; 71 () : . [epub] 20240805

Jazyk angličtina Země Česko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39264026

Echinococcus granulosus (Batsch, 1786), a cestode of the Teniidae family, causes human cystic echinococcosis (CE) also known as hydatid disease. Echinococcus granulosus sensu lato includes the G1, G3, G4, G5, G6/7 and G8/10 genotypes which are known to cause human CE. This study aimed to differentiate genotypes of E. granulosus s.l. complex by employing EmsB, a tandemly repeated multilocus microsatellite, using next-generation sequencing (MIC-NGS). Human and animal histopathology-confirmed hydatid cyst tissue samples and reference DNA samples of E. granulosus G1, G3, G4, G5, G6/7 and G10 underwent MIC-NGS assay with custom primers amplifying a 151 bp EmsB DNA fragment. NGS data were analysed using online Galaxy analysis pipeline, a phylogenetic tree was constructed by MEGA software, and haplotype networking was performed with PopArt 1.7. All sixty samples (49 from animals and 11 from humans) included were successfully identified and genotyped with a 100 % success rate. The study showed improved discrimination power to distinguish all study samples including closely related E. granulosus s.s. genotypes G1-G3. The maximum likelihood tree reaffirmed the monophyly of E. granulosus s.l. The median-joining haplotype networking revealed 12 distinct haplotypes. In conclusion, MIC-NGS assay was shown to be sensitive, specific and simple to apply to clinical samples offering a powerful discriminatory tool for the genotyping of E. granulosus s.l.

Zobrazit více v PubMed

Al-Jawabreh A., Ereqat S., Dumaidi K., Nasereddin A., Al-Jawabreh H., Azmi K., Al-Laham N., Nairat M., Casulli A., Maqboul H., Abdeen Z. 2017: The clinical burden of human cystic echinococcosis in Palestine, 2010-2015. PLoS Negl. Trop. Dis. 11: e0005717.

Alvarez Rojas C.A., Gauci C.G., Lightowlers M.W. 2013: Antigenic differences between the EG95-related proteins from Echinococcus granulosus G1 and G6 genotypes: implications for vaccination. Parasite Immunol. 35: 99-102. DOI

Alvarez Rojas C.A., Romig T., Lightowlers M.W. 2014: Echinococcus granulosus sensu lato genotypes infecting humans-review of current knowledge. Int. J. Parasitol. 44: 9-18. DOI

Bandelt H.J., Forster P., Rohl A. 1999: Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37-48. DOI

Bart J.M., Knapp J., Gottstein B., El-Garch F., Giraudoux P., Glowatzki M.L., Berthoud H., Maillard S., Piarroux R. 2006: EmsB, a tandem repeated multi-loci microsatellite, new tool to investigate the genetic diversity of Echinococcus multilocularis. Infect. Genet. Evol. 6: 390-400. DOI

Bohard L., Lallemand S., Borne R., Courquet S., Bresson-Hadni S., Richou C., Millon L., Bellanger A.P., Knapp J. 2023: Complete mitochondrial exploration of Echinococcus multilocularis from French alveolar echinococcosis patients. Int. J. Parasitol. 53: 555-564. DOI

Bonelli P., Dei Giudici S., Peruzzu A., Mura L., Santucciu C., Maestrale C., Masala G. 2021: Identification of Echinococcus granulosus genotypes G1 and G3 by SNPs genotyping assays. Pathogens 10: 125. DOI

Botezatu C., Mastalier B., Patrascu T. 2018: Hepatic hydatid cyst - diagnose and treatment algorithm. J. Med. Life 11: 203-209. DOI

Bowles J., Blair D., McManus D.P. 1992: Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol. Biochem. Parasitol. 54: 165-173. DOI

Budke C.M., Deplazes P., Torgerson P.R. 2006: Global socioeconomic impact of cystic echinococcosis. Emerg. Infect. Dis. 12: 296-303. DOI

Casulli A., Massolo A., Saarma U., Umhang G., Santolamazza F., Santoro A. 2022: Species and genotypes belonging to Echinococcus granulosus sensu lato complex causing human cystic echinococcosis in Europe (2000-2021): a systematic review. Parasit. Vectors 15: 109. DOI

Centers for Disease Controland Prevention (Ed.) 2023: Echinococcosis. https://www.cdc.gov/dpdx/echinococcosis/index.html. Accessed on 23.5.2023.

Corpet F. 1988: Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16: 10881-10890. DOI

Debeljak Z., Boufana B., Interisano M., Vidanovic D., Kulisic Z., Casulli A. 2016: First insights into the genetic diversity of Echinococcus granulosus sensu stricto (s.s.) in Serbia. Vet. Parasitol 223: 57-62. DOI

Fan S., Zhao X., Danqulamu, Shi B., Tang W., Dong H., Xia C. 2022: Genetic diversity and haplotype analysis of yak and sheep echinococcal cysts isolates from the mitochondrial cox1 gene in parts of Tibet, China. Front. Vet. Sci. 9: 1016972. DOI

Hamamci B., Acikgoz G., Cetinkaya U., Kilic E., Kocal S., Karaaslan K., Durgun Yetim T., Yetim I. 2023: Molecular genotyping of Echinococcus granulosus sensu stricto from human echinococcal cysts in Hatay, Turkiye. Exp. Parasitol. 245: 108454. DOI

Kinkar L., Laurimae T., Acosta-Jamett G., Andresiuk V., Balkaya I., Casulli A., Gasser R.B., Gonzalez L.M., Haag K.L., Zait H., Irshadullah M., Jabbar A., Jenkins D.J., Manfredi M.T., Mirhendi H., M'rad S., Rostami-Nejad M., Oudni-M'rad M., Pierangeli N.B., Ponce-Gordo F., Rehbein S., Sharbatkhori M., Kia E.B., Simsek S., Soriano S.V., Sprong H., Snabel V., Umhang G., Varcasia A., Saarma U. 2018: Distinguishing Echinococcus granulosus sensu stricto genotypes G1 and G3 with confidence: a practical guide. Infect. Genet. Evol. 64: 178-184. DOI

Knapp J., Bart J.M., Glowatzki M.L., Ito A., Gerard S., Maillard S., Piarroux R., Gottstein B. 2007: Assessment of use of microsatellite polymorphism analysis for improving spatial distribution tracking of Echinococcus multilocularis. J. Clin. Microbiol. 45: 2943-2950. DOI

Kumar S., Stecher G., Li M., knyaz C., Tamura K. 2018: MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547-1549. DOI

Lymbery A.J. 2017: Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. Adv. Parasitol. 95: 111-145. DOI

Maillard S., Gottstein B., Haag K.L., Ma S., Colovic I., Benchikh-Elfegoun M.C., Knapp J., Piarroux R. 2009: The EmsB tandemly repeated multilocus microsatellite: a new tool to investigate genetic diversity of Echinococcus granulosus sensu lato. J. Clin. Microbiol. 47: 3608-3616. DOI

Maksimov P., Bergmann H., Wassermann M., Romig T., Gottstein B., Casulli A., Conraths F.J. 2020: Species detection within the Echinococcus granulosus sensu lato complex by novel probe-based real-time PCRs. Pathogens 9: 791. DOI

Mousa W.M., Abdel-Wahab A.M., El-Gameel Sohila M., Mahdy O.A. 2020: Genetic characterization of hydatid cysts of different intermediate hosts. Helminthologia 57: 185-195. DOI

Nakao M., Lavikainen A., Yanagida T., Ito A. 2013: Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). Int. J. Parasitol. 43: 1017-1029. DOI

Nakao M., Mcmanus D.P., Schantz P.M., Craig P.S., Ito A. 2007: A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134: 713-722. DOI

Nasereddin A., Al-Jawabreh A., Dumaidi K., Al-Jawabreh A., Al-Jawabreh H., Ereqat S. 2022: Tracking of SARS-CoV-2 Alpha variant (B.1.1.7) in Palestine. Infect. Genet. Evol. 101: 105279. DOI

Ohiolei J.A., LI L., Yan H.B., Fu B.Q., Jia W.Z. 2020: Complete mitochondrial genome analysis confirms the presence of Echinococcus granulosus sensu lato genotype G6 in Nigeria. Infect.Genet. Evol. 84: 104377. DOI

Rostami S., Talebi S., Babaei Z., Sharbatkhori M., Ziaali N., Rostami H., Harandi M.F. 2013: High resolution melting technique for molecular epidemiological studies of cystic echinococcosis: differentiating G1, G3, and G6 genotypes of Echinococcus granulosus sensu lato. Parasitol. Res. 112: 3441-3447. DOI

Sadjjadi S.M. 2006: Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol. Int. 55: S197-202. DOI

Sakalar C., Kuk S., Erensoy A., Dagli A.F., Ozercan I.H., Cetinkaya U., Yazar S. 2014: Molecular discrimination of Echinococcus granulosus and Echinococcus multilocularis by sequencing and a new PCR-RFLP method with the potential use for other Echinococcus species. Turk. J. Med. Sci. 44: 741-748. DOI

Salant H., Abbasi I., Hamburger J. 2012: The development of a loop-mediated isothermal amplification method (LAMP) for Echinococcus granulosus [corrected] coprodetection. Am. J. Trop. Med. Hyg. 87: 883-887. DOI

Santucciu C., Bonelli P., Peruzzu A., Fancellu A., Fara A., Mastrandrea S., Drocchi G., Cossu A., Profili S., Porcu A., Masala G. 2023: Genetic characterization of Echinococcus granulosus sensu stricto isolated from human cysts from Sardinia, Italy. Diseases 11: 91. DOI

Shang J.Y., Zhang G.J., Liao S., Huang Y., Yu W.J., He W., Yang G.Y., LI T.Y., Chen X.W., Zhong B., Wang Q., Wang Q., Li R.R., Wang H. 2019: A multiplex PCR for differential detection of Echinococcus granulosus sensu stricto, Echinococcus multilocularis and Echinococcus canadensis in China. Infect. Dis. Poverty 8: 68. DOI

Stefanic S., Shaikenov B.S., Deplazes P., Dinkel A., Torgerson P.R., Mathis A. 2004: Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (sheep strain) in naturally infected dogs. Parasitol. Res. 92: 347-351. DOI

Tamura K., Nei M. 1993: Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512-526.

Trachsel D., Deplazes P., Mathis A. 2007: Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134: 911-920. DOI

Valot B., Knapp J., Umhang G., Grenouillet F., Millon L. 2015: Genomic characterization of EmsB microsatellite loci in Echinococcus multilocularis. Infect. Genet. Evol. 32: 338-341. DOI

Widdicombe J., Basanez M.G., Entezami M., Jackson D., Larrieu E., Prada J.M. 2022: The economic evaluation of cystic echinococcosis control strategies focused on zoonotic hosts: a scoping review. PLoS Negl. Trop. Dis. 16: e0010568. DOI

WHO 2023: Echinococcosis - 23 may 2023. https://www.who.int/en/news-room/fact-sheets/detail/echinococcosis. Accessed on 23.5.2023.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...