Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-19T16:30:13.672Z Has data issue: false hasContentIssue false
  • English
  • Français

Investigation of the relationship between CE cyst characteristics and genetic diversity of Echinococcus granulosus sensu lato in humans from Turkey

Published online by Cambridge University Press:  17 August 2020

Serra Örsten Open the ORCID record for Serra Örsten [Opens in a new window] ,
Türkmen Çiftçi ,
Aynur Azizova ,
Gökhan Yüce ,
Aycan Uysal ,
Çetin İmamoğlu ,
Ergun Karaağaoğlu ,
Devrim Akıncı ,
Yakut Akyön  and
Adriano Casulli Open the ORCID record for Adriano Casulli [Opens in a new window]
...Show all authors
Serra Örsten*
Affiliation:
Vocational School of Health Services, Hacettepe University, Ankara, Turkey
Türkmen Çiftçi
Affiliation:
Department of Radiology, Faculty of Medicine, Hacettepe University, Ankara, Turkey
Aynur Azizova
Affiliation:
Department of Radiology, Faculty of Medicine, Hacettepe University, Ankara, Turkey
Gökhan Yüce
Affiliation:
Department of Radiology, Ministry of Health, Ankara City Hospital, Ankara, Turkey
Aycan Uysal
Affiliation:
Department of Radiology, Ministry of Health, Gülhane Training and Research Hospital, Ankara, Turkey
Çetin İmamoğlu
Affiliation:
Department of Radiology, Ministry of Health, Dr Abdurrahman Yurtaslan Ankara Oncology Training and Research Hospital, Ankara, Turkey
Ergun Karaağaoğlu
Affiliation:
Department of Biostatistics, Faculty of Medicine, Hacettepe University, Ankara, Turkey
Devrim Akıncı
Affiliation:
Department of Radiology, Faculty of Medicine, Hacettepe University, Ankara, Turkey
Yakut Akyön
Affiliation:
Department of Medical Microbiology, Faculty of Medicine, Hacettepe University, Ankara, Turkey
Adriano Casulli
Affiliation:
WHO Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis, Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy European Reference Laboratory for Parasites (EURLP), Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy
Okan Akhan
Affiliation:
Department of Radiology, Faculty of Medicine, Hacettepe University, Ankara, Turkey
*
Author for correspondence: Serra Örsten, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Cystic echinococcosis (CE) is one of the most common zoonotic diseases worldwide, particularly in rural areas. This study aimed at the identification of the genotype/species belonging to Echinococcus granulosus sensu lato (s.l.) specimens in retrieved percutaneously from the human host and to investigate their relationship with cyst characteristics. The genetic identification of cyst material was performed by mt-CO1 gene polymerase chain reaction, and confirmed via sequencing. A total of 110 CE cysts were identified as E. granulosus s.l. In detail, 104 belonged to E. granulosus sensu stricto (G1 and G3) and six isolates were in the E. canadensis cluster (G6/7). All clusters were tested for the relationship between demographics, cyst features and genetic diversity. The relationship between genetic variation and certain clinical characteristics such as cyst volume and location were statistically significant for G6/7 cluster. Further studies are required with a larger sample set to investigate the relationship between the genetic variability of E. granulosus s.l. and cyst features.

Keywords

Echinococcus granulosus sensu latogenetic diversityhuman cystic echinococcosisparasitic cyst characteristics
Type
Research Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1712 - 1717
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Altintas, N (2008) Parasitic zoonotic diseases in Turkey. Veterinaria Italiana 44, 633–646.Google ScholarPubMed
Altıntaş, N (2003) Past to present: echinococcosis in Turkey. Acta Tropica 85, 105–112.CrossRefGoogle ScholarPubMed
Alvarez Rojas, CA, Romig, T and Lightowlers, MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. International Journal for Parasitology 44, 9–18.CrossRefGoogle ScholarPubMed
Bakal, U, Simsek, S and Kazez, A (2015) Surgical and molecular evaluation of pediatric hydatid cyst cases in Eastern Turkey. Korean Journal of Parasitology 53, 785–788.CrossRefGoogle ScholarPubMed
Beyhan, Y and Umur, S (2011) Molecular characterization and prevalence of cystic echinococcosis in slaughtered water buffaloes in Turkey. Veterinary Parasitology 181, 174–179.CrossRefGoogle ScholarPubMed
Boufana, B, Lahmar, S, Rebai, W, Ben Safta, Z, Jebabli, L, Ammar, A, Kachti, M, Aouadi, S and Craig, PS (2014) Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 706–714.CrossRefGoogle ScholarPubMed
Brunetti, E, Kern, P and Vuitton, DA and Writing Panel for the WHO-IWGE. (2010). Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Tropica 114, 1–16.CrossRefGoogle ScholarPubMed
Busi, M, Snabel, V, Varcasia, A, Garippa, G, Perrone, V, De Liberato, C and D'Amelio, S (2007) Genetic variation within and between G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Veterinary Parasitology 150, 75–83. http://dx.doi.org/10.1016/j.vetpar.2007.09.003.CrossRefGoogle Scholar
Casulli, A, Interisano, M, Sreter, T, Chitimia, L, Kirkova, Z, La Rosa, G and Pozio, E (2012) Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infection Genetics Evolution 12, 377–383.CrossRefGoogle ScholarPubMed
Casulli, A, Siles-Lucas, M and Tamarozzi, F (2019) Echinococcus granulosus sensu lato. Trends in Parasitology 35, 663–664.CrossRefGoogle ScholarPubMed
Deplazes, P, Rinaldi, L, Alvarez Rojas, CA, Torgerson, PR, Harandi, MF, Romig, T, Antolova, D, Schurer, JM, Lahmar, S, Cringoli, G, Magambo, J, Thompson, RC and Jenkins, EJ (2017) Global distribution of alveolar and cystic echinococcosis. Advances in Parasitology 95, 315–493.CrossRefGoogle ScholarPubMed
Eckert, J, Gemmell, MA, Meslin, FX and Pawlowski, ZS. (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Paris OIE, pp. 1–265.Google Scholar
Erdoğan, E, Özkan, B, Mutlu, F, Karaca, S and Şahin, İ (2017) Molecular characterization of Echinococcus granulosus isolates obtained from different hosts. Mikrobiyoloji Bülteni 51, 79–86.CrossRefGoogle ScholarPubMed
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, Torun, MM and Kocazeybek, B (2010) Genotypic characterisation of Echinococcus granulosus isolated from human in Turkey. African Journal of Microbiology Research 4, 551–555.Google Scholar
Eroglu, F, Genc, A and Koltas, IS (2016) The genotyping of Echinococcus granulosus isolates with PCR-RFLP methods in Adana Province. Zirve Medical Journal 1, 22–25.Google Scholar
Eryildiz, C and Şakru, N (2012) Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan Medical Journal 29, 261–267.Google ScholarPubMed
Hassan, ZI, Meerkhan, AA, Boufana, B, Hama, AA, Ahmed, BD, Mohammed, W, Mero, S, Orsten, S, Interisano, M, Pozio, E and Casulli, A (2017) Two haplotype clusters of Echinococcus granulosus sensu stricto in northern Iraq (Kurdistan region) support the hypothesis of a parasite cradle in the Middle East. Acta Tropica 172, 201–207.CrossRefGoogle ScholarPubMed
Hüttner, M, Nakao, M, Wassermann, T, Siefert, L, Boomker, JDF, Dinkel, A, Sako, Y, Mackenstedt, U, Romig, T and Ito, A (2008) Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 39, 861–868.CrossRefGoogle Scholar
Kinkar, L, Laurimäe, T, Sharbatkhori, M, Mirhendi, H, Kia, EB, Ponce-Gordo, F, Andresiuk, V, Simsek, S, Lavikainen, A, Irshadullah, M, Umhang, G, Oudni-M'rad, M, Acosta-Jamett, G, Rehbein, S and Saarma, U (2017) New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto. Infection Genetics Evolution 52, 52–58.CrossRefGoogle ScholarPubMed
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ and Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Librado, P and Rozas, J (2009) DnaDP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle Scholar
Nakao, M, Sako, Y, Yokoyama, N, Fukunaga, M and Ito, A (2000) Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415–424.CrossRefGoogle ScholarPubMed
Nakao, M, McManus, DP, Schantz, PM, Craig, PS and Ito, A (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713–722.CrossRefGoogle ScholarPubMed
Nakao, M, Yanagida, T, Okamoto, M, Knapp, J, Nkouawa, A, Sako, Y and Ito, A (2010) State-of-the-art Echinococcus and Taenia: phylogenetic taxonomy of human-pathogenic tapeworms and its application to molecular diagnosis. Infection Genetics Evolution 10, 444–452.CrossRefGoogle ScholarPubMed
Nakao, M, Yanagida, T, Konyaev, S, Lavikainen, A, Odnokurtsev, VA, Zaikov, VA and Ito, A (2013) Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 140, 1625–1636.CrossRefGoogle ScholarPubMed
Oral Babaoğlu, A, Soyder, A, Malatyalı, E, Ertuğ, S and Ertabaklar, H (2018) Genotyping of Echinococcus granulosus isolates by sequencing of mitochondrial cytochrome C oxidase subunit 1 (cox1) gene in Aydin. Mikrobiyoloji Bülteni 52, 198–205.CrossRefGoogle ScholarPubMed
Orsten, S, Boufana, B, Ciftci, T, Akinci, D, Karaagaoglu, E, Ozkuyumcu, C, Casulli, A and Akhan, O (2018) Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients. Parasitology Research 117, 1257–1263.CrossRefGoogle Scholar
Romig, T, Ebi, D and Wassermann, M (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology 213, 76–84.CrossRefGoogle ScholarPubMed
Romig, T, Deplazes, P, Jenkins, D, Giraudoux, P, Massolo, A, Craig, PS, Wassermann, M, Takahashi, M and de la Rue, M (2017) Ecology and life cycle patterns of Echinococcus species. Advances in Parasitology 95, 213–314.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Salzburger, W, Ewing, GB and Haeseler, A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology 20, 1952–1963.CrossRefGoogle Scholar
Schneider, R, Gollackner, B, Schindl, M, Tucek, G and Auer, H (2010) Echinococcus canadensis G7 (pig strain): an underestimated cause of cystic echinococcosis in Austria. The American Journal of Tropical Medicine and Hygiene 82, 871–874.CrossRefGoogle ScholarPubMed
Simsek, S, Kaplan, M and Ozercan, IF (2011) A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitology Research 109, 411–416.CrossRefGoogle ScholarPubMed
Snabel, V, Altintas, N, D'Amelio, S, Nakao, M, Romig, T, Yolasigmaz, A, Gunes, K, Turk, M, Busi, M, Hüttner, M, Sevcová, D, Ito, A, Altintas, N and Dubinský, P (2009) Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitology Research 105, 145–154.CrossRefGoogle ScholarPubMed
Tamarozzi, F, Akhan, O, Cretu, CM, Vutova, K, Akinci, D, Chipeva, R, Ciftci, T, Constantin, CM, Fabiani, M, Golemanov, B, Janta, D, Mihailescu, P, Muhtarov, M, Orsten, S, Petrutescu, M, Pezzotti, P, Popa, AC, Popa, LG, Popa, MI, Velev, V, Siles-Lucas, M, Brunetti, E and Casulli, A (2018) Prevalence of abdominal cystic echinococcosis in rural Bulgaria, Romania, and Turkey: a cross-sectional, ultrasound-based, population study from the HERACLES project. Lancet Infectious Diseases 18, 769–778.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Thompson, RCA (2008) The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439–446.CrossRefGoogle ScholarPubMed
Utuk, AE, Simsek, S, Koroglu, E and McManus, DP (2008) Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta Tropica 107, 192–194.CrossRefGoogle Scholar
Vural, G, Baca, AU, Gauci, CG, Bagci, O, Gicik, Y and Lightowlers, MW (2008) Variability in the 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.CrossRefGoogle Scholar
Wen, H, Vuitton, L, Tuxun, T, Li, J, Vuitton, DA, Zhang, W and McManus, DP (2019) Echinococcosis: advances in the 21st century. Clinical Microbiology Reviews 32, e00075–18.CrossRefGoogle ScholarPubMed
Yanagida, T, Mohammadzadeh, T, Kamhawi, S, Nakao, M, Sadjjadi, SM, Hijjawi, N, Abdel-Hafez, SK, Sako, Y, Okamoto, M and Ito, A (2012) Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitology International 61, 599–603.CrossRefGoogle ScholarPubMed
Yazar, S, Ozkan, AT, Hökelek, M, Polat, E, Yilmaz, H, Özbilge, H, Ustun, S, Koltaş, IS, Ertek, M, Sakru, N, Alver, O, Cetinkaya, Z, Koç, Z, Demirci, M, Aktaş, H, Parsak, CK, Ozerdem, D, Sakman, G, Cengiz, ZT, Ozer, A, Keklik, K, Yemenici, N, Turan, M, Daştan, A, Kaya, E, Tamer, GS, Girginkardeşler, N, Türk, M, Sinirtaş, M, Evci, C, Kiliçturgay, S, Mutlu, F and Artiş, T (2008) Cystic echinococcosis in Turkey from 2001–2005. Türkiye Parazitoloji Dergisi 32, 208–220.Google ScholarPubMed
Supplementary material: File

Örsten et al. supplementary material

Örsten et al. supplementary material 1

Download Örsten et al. supplementary material(File)
File 18.2 KB
Supplementary material: File

Örsten et al. supplementary material

Örsten et al. supplementary material 2

Download Örsten et al. supplementary material(File)
File 15.5 KB