Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-06-21T03:34:05.049Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic diversity and haplotypes of paediatric hydatid cyst isolates and first occurrence of E. canadensis (G6/G7) in paediatric cases in Turkey

Published online by Cambridge University Press:  30 June 2021

Unal Bakal ,
Figen Celik ,
Sami Simsek Open the ORCID record for Sami Simsek [Opens in a new window] ,
Harun Kaya Kesik  and
Seyma Gunyakti Kilinc
Unal Bakal
Affiliation:
Department of Pediatric Surgery, Faculty of Medicine, University of Firat, Elazig, Turkey
Figen Celik
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, Elazig, Turkey
Sami Simsek*
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Firat, Elazig, Turkey
Harun Kaya Kesik
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Bingol, Bingol, Turkey
Seyma Gunyakti Kilinc
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, University of Bingol, Bingol, Turkey
*
Author for correspondence: Sami Simsek, E-mail: ssimsek@firat.edu.tr
Get access Rights & Permissions [Opens in a new window]

Abstract

Cystic echinococcosis (CE) is a neglected zoonotic tropical disease caused by Echinococcus granulosus sensu lato. The aim of this study was to investigate the genetic variation of hydatid cyst isolates obtained from surgically confirmed paediatric cases originating from two different regions in eastern Turkey. Seventeen paediatric cases aged between 6 and 16 were operated by open surgery, and the germinal layers of their cysts were obtained for further molecular analyses. After genomic DNA isolation, 875 bp mt-CO1 gene fragments were amplified in all samples by PCR. Then, the unidirectional sequence analyses of the PCR products were carried out. According to the BLAST analyses of 17 sequences, 16 of these sequences were matched with E. granulosus sensu stricto, while one sequence was identified as E. canadensis (G6/G7) for the first time in paediatric cases in Turkey. High haplotype diversity and low nucleotide diversity were observed in the E. granulosus s.s. sequences.

Keywords

Echinococcus granulosus sensu strictohaplotype analysispaediatric hydatid cyst
Type
Research Article
Information
Parasitology , Volume 148 , Issue 12 , October 2021 , pp. 1482 - 1489
Check for updates
Copyright
Copyright © The Author(s), 2021. 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

Abdulhameed, MF, Habib, I, Al-Azizz, SA and Robertson, I (2018) A retrospective study of human cystic echinococcosis in Basrah province, Iraq. Acta Tropica 178, 130–133.CrossRefGoogle ScholarPubMed
Altintas, N (2003) Past to present: echinococcosis in Turkey. Acta Tropica 85, 105–112.CrossRefGoogle ScholarPubMed
Altintas, N (2008) Parasitic zoonotic diseases in Turkey. Veterinaria Italiana 44, 633–646.Google ScholarPubMed
Anadol, D, Göçmen, A, Kiper, N and Özçelik, U (1998) Hydatid disease in childhood: a retrospective analysis of 376 cases. Pediatric Pulmonology 26, 190–196.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Aslanabadi, S, Zarrintan, S, Abdoli-Oskouei, S, Salehpour, F, Zarrintan, A, Beheshtirouy, S, Abdollahi, H and Badebarin, D (2013) Hydatid cyst in children: a 10-year experience from Iran. African Journal of Paediatric Surgery 10, 140.Google ScholarPubMed
Bakal, U, Simsek, S and Kazez, A (2015) Surgical and molecular evaluation of pediatric hydatid cyst cases in eastern Turkey. The Korean Journal of Parasitology 53, 785.CrossRefGoogle ScholarPubMed
Bandelt, HJ, Forster, P and Röhl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Battelli, G (2009) Echinococcosis: costs, losses and social consequences of a neglected zoonosis. Veterinary Research Communications 33, 47–52.CrossRefGoogle ScholarPubMed
Budke, CM, Deplazes, P and Torgerson, PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerging Infectious Diseases 12, 296.CrossRefGoogle ScholarPubMed
Budke, CM, Carabin, H, Ndimubanzi, PC, Nguyen, H, Rainwater, E, Dickey, M, Bhattarai, R, Zeziulin, O and Qian, MB (2013) A systematic review of the literature on cystic echinococcosis frequency worldwide and its associated clinical manifestations. The American Journal of Tropical Medicine and Hygiene 88, 1011–1027.CrossRefGoogle ScholarPubMed
Cangir, AK, Şahin, E, Enön, S, Kavukçu, Ş, Akay, H, Ökten, İ and Yavuzer, Ş (2001) Surgical treatment of pulmonary hydatid cysts in children. Journal of Pediatric Surgery 36, 917–920.CrossRefGoogle ScholarPubMed
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 and Evolution 12, 377–383.CrossRefGoogle ScholarPubMed
Craig, P and Larrieu, E (2006) Control of cystic echinococcosis/hydatidosis: 1863–2002. Advances in Parasitology 61, 443–508.CrossRefGoogle ScholarPubMed
Deplazes, P, Rinaldi, L, Rojas, CA, Torgerson, P, Harandi, M, Romig, T, Antolova, D, Schurer, J, Lahmar, S and Cringoli, G (2017) Global distribution of alveolar and cystic echinococcosis. Advances in Parasitology 95, 315–493.CrossRefGoogle ScholarPubMed
Eckert, J and Deplazes, P (2004) Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107–135.CrossRefGoogle ScholarPubMed
Ergin, S, Saribas, S, Yuksel, P, Zengin, K, Midilli, K, Adas, G, Arikan, S, Aslan, M, Uysal, H and Caliskan, R (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, I (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 Sakru, N (2012) Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan Medical Journal 29, 261.Google ScholarPubMed
Fu, YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Fu, YX and Li, WH (1993) Statistical tests of neutrality of mutations. Genetics 133, 693–709.CrossRefGoogle ScholarPubMed
Gollackner, B, Längle, F, Auer, H, Maier, A, Mittlböck, M, Agstner, I, Karner, J, Langer, F, Aspöck, H and Loidolt, H (2000) Radical surgical therapy of abdominal cystic hydatid disease: factors of recurrence. World Journal of Surgery 24, 717–721.CrossRefGoogle ScholarPubMed
Gonlugur, U, Ozcelik, S, Gonlugur, T, Arici, S, Celiksoz, A, Elagoz, S and Cevit, R (2009) The retrospective annual surgical incidence of cystic echinococcosis in Sivas, Turkey. Zoonoses and Public Health 56, 209–214.CrossRefGoogle ScholarPubMed
Jordanova, D, Harizanov, R, Kaftandjiev, I, Rainova, I and Kantardjiev, T (2015) Cystic echinococcosis in Bulgaria 1996–2013, with emphasis on childhood infections. European Journal of Clinical Microbiology and Infectious Diseases 34, 1423–1428.CrossRefGoogle ScholarPubMed
Khan, A, Ahmed, H, Simsek, S, Liu, H, Yin, J, Wang, Y, Shen, Y and Cao, J (2020). Molecular characterization of human Echinococcus isolates and first report of E. canadensis (G6/7) and E. multilocularis from the Punjab province of Pakistan using sequence analysis. BMC Infectious Diseases 20, 262.CrossRefGoogle Scholar
Kinkar, L, Laurimäe, T, Acosta-Jamett, G, Andresiuk, V, Balkaya, I, Casulli, A, Gasser, RB, van der Giessen, J, González, LM and Haag, KL (2018) Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. International Journal for Parasitology 48, 729–742.CrossRefGoogle ScholarPubMed
Kocer, B, Gulbahar, G, Han, S, Ilhan, MN, Dural, K and Sakinci, U (2008) Analysis of pulmonary hydatidosis according to their segmentary locations. Clinical Pulmonary Medicine 15, 8–12.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lymbery, A and Thompson, R (2012) The molecular epidemiology of parasite infections: tools and applications. Molecular and Biochemical Parasitology 181, 102–116.CrossRefGoogle ScholarPubMed
Maddison, DR, Swofford, DL and Maddison, WP (1997) NEXUS: an extensible file format for systematic information. Systematic Biology 46, 590–621.CrossRefGoogle ScholarPubMed
Maillard, S, Benchikh-Elfegoun, M, Knapp, J, Bart, J, Koskei, P, Gottstein, B and Piarroux, R (2007) Taxonomic position and geographical distribution of the common sheep G1 and camel G6 strains of Echinococcus granulosus in three African countries. Parasitology Research 100, 495–503.CrossRefGoogle ScholarPubMed
Mehmood, S, Simsek, S, Celik, F, Kesik, HK, Gunyakti Kilinc, S and Ahmed, H (2020) Molecular survey on cattle and sheep hydatidosis and first detection of Echinococcus canadensis (G6/G7) in sheep in Turkey. Parasitology, 147, 1055–1062.CrossRefGoogle ScholarPubMed
Montazeri, V, Sokouti, M and Rashidi, MR (2007) Comparison of pulmonary hydatid disease between children and adults. Tanaffos, 6, 13–18.Google Scholar
Moro, P and Schantz, PM (2009) Echinococcosis: a review. International Journal of Infectious Diseases 13, 125–133.CrossRefGoogle ScholarPubMed
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, Lavikainen, A and Hoberg, E (2015) Is Echinococcus intermedius a valid species. Trends in Parasitology 31, 342–343.CrossRefGoogle ScholarPubMed
Nejad, MR, Taghipour, N, Nochi, Z, Mojarad, EN, Mohebbi, S, Harandi, MF and Zali, M (2012) Molecular identification of animal isolates of Echinococcus granulosus from Iran using four mitochondrial genes. Journal of Helminthology 86, 485–492.CrossRefGoogle Scholar
Nouir, NB, Nunez, S, Gianinazzi, C, Gorcii, M, Müller, N, Nouri, A, Babba, H and Gottstein, B (2008) Assessment of Echinococcus granulosus somatic protoscolex antigens for serological follow-up of young patients surgically treated for cystic echinococcosis. Journal of Clinical Microbiology 46, 1631–1640.CrossRefGoogle ScholarPubMed
Obwaller, A, Schneider, R, Walochnik, J, Gollackner, B, Deutz, A, Janitschke, K, Aspöck, H and Auer, H (2004) Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitology 128, 569.CrossRefGoogle ScholarPubMed
Ok, UZ, Ozkol, M, Kilimcioglu, AA, Dinc, G, Bayindir, P, Ostan, I, Pabuscu, Y, Ozcan, C, Korkmaz, M and Coskun, S (2007) A province-based study using sampling method to investigate the prevalence of cystic echinococcosis among primary school children in Manisa, Turkey. Acta Tropica 103, 116–122.CrossRefGoogle ScholarPubMed
Pawlowski, Z (2001) Echinococcosis in humans: clinical aspects, diagnosis and treatment. WHO/OIE manual on echinococcosis in humans and animals.Google Scholar
Rojas, CAA, 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 Scholar
Rokni, M (2008) The present status of human helminthic diseases in Iran. Annals of Tropical Medicine and Parasitology 102, 283–295.CrossRefGoogle ScholarPubMed
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, K and De La Rue, M (2017) Ecology and life cycle patterns of Echinococcus species. In Advances in Parasitology 95, 213–314.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299–3302.CrossRefGoogle ScholarPubMed
Salzburger, W, Ewing, GB and Von Haeseler, A (2011). The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology 20, 1952–1963.CrossRefGoogle ScholarPubMed
Sarkari, B, Arefkhah, N, Ghorbani, F, Meskini, F, Yektaeian, N, Shahriarirad, S and Mostafavi-Pour, Z (2020) Seroprevalence of cystic echinococcosis and related risk factors for infection among children in a rural community in Fars Province, Southern Iran. Clinical Epidemiology and Global Health 8, 13–16.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Şehitoğulları, A (2007) Our results in surgical treatment of hydatid cyst of the lungs. European Journal General Medicine 4, 5–8.CrossRefGoogle Scholar
Simsek, S, Balkaya, I, Ciftci, AT and Utuk, AE (2011a) Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Veterinary Parasitology 178, 367–369.CrossRefGoogle ScholarPubMed
Simsek, S, Kaplan, M and Ozercan, IH (2011b) 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
Šnábel, V, Altintas, N, D'amelio, S, Nakao, M, Romig, T, Yolasigmaz, A, Gunes, K, Turk, M, Busi, M and Hüttner, M (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
Tajima, F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Talaiezadeh, AH and Maraghi, S (2006) Hydatid disease in children: a different pattern than adults. Pakistan Journal of Medical Sciences 22, 329.Google Scholar
Tamarozzi, F, Akhan, O, Cretu, CM, Vutova, K, Akinci, D, Chipeva, R, Ciftci, T., Constantin, CM, Fabiani, M and Golemanov, B (2018) Prevalence of abdominal cystic echinococcosis in rural Bulgaria, Romania, and Turkey: a cross-sectional, ultrasound-based, population study from the HERACLES project. The Lancet Infectious Diseases 18, 769–778.CrossRefGoogle Scholar
Tantawy, IM (2010) Hydatid cyst in children. Annals of Pediatric Surgery 6, 98–104.Google Scholar
Tavakoli, H, Bayat, M and Kousha, A (2008) Hydatidosis infection study in human and livestock populations during 2002–2007. American-Eurasian Journal of Agricultural and Environmental Sciences 4, 473–477.Google Scholar
Thompson, R (2017) Biology and systematics of Echinococcus. Advances in Parasitology 95, 65–109.CrossRefGoogle ScholarPubMed
Thompson, R, McManus, D, Eckert, J, Gemmell, M, Meslin, F and Pawlowski, Z (2001) WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. Eckert J, Gemmell MA, Meslin FX, Pawlowski ZSParis, France: World Organisation for Animal Health, pp. 1–19.Google Scholar
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 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.CrossRefGoogle Scholar
WHO (2017) Integrating neglected tropical diseases into global health and development: fourth WHO report on neglected tropical diseases, World Health Organization.Google Scholar
Yolasigmaz, A, Reiterová, K, Turk, M, Reyhan, E, Bozdag, A, Karababa, A, Altintas, N and Altintas, N (2006) Comparison of serological and clinical findings in Turkish patients with cystic echinococcosis. Helminthologia 43, 220–225.CrossRefGoogle Scholar
Zhang, T, Yang, D, Zeng, Z, Zhao, W, Liu, A, Piao, D, Jiang, T, Cao, J, Shen, Y and Liu, H (2014) 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 9, 109059.CrossRefGoogle ScholarPubMed
Supplementary material: File

Bakal et al. supplementary material

Bakal et al. supplementary material

Download Bakal et al. supplementary material(File)
File 14.6 KB