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Molecular survey on cattle and sheep hydatidosis and first detection of Echinococcus canadensis (G6/G7) in sheep in Turkey

Published online by Cambridge University Press:  14 May 2020

Sarfraz Mehmood ,
Sami Simsek Open the ORCID record for Sami Simsek [Opens in a new window] ,
Figen Celik ,
Harun Kaya Kesik ,
Seyma Gunyakti Kilinc  and
Haroon Ahmed Open the ORCID record for Haroon Ahmed [Opens in a new window]
Sarfraz Mehmood
Affiliation:
Faculty of Veterinary Medicine, Department of Parasitology, University of Firat, 23119, Elazig, Turkey
Sami Simsek*
Affiliation:
Faculty of Veterinary Medicine, Department of Parasitology, University of Firat, 23119, Elazig, Turkey
Figen Celik
Affiliation:
Faculty of Veterinary Medicine, Department of Parasitology, University of Firat, 23119, Elazig, Turkey
Harun Kaya Kesik
Affiliation:
Faculty of Veterinary Medicine, Department of Parasitology, Bingol University, Bingol, Turkey
Seyma Gunyakti Kilinc
Affiliation:
Faculty of Veterinary Medicine, Department of Parasitology, University of Firat, 23119, Elazig, Turkey Faculty of Veterinary Medicine, Department of Parasitology, Bingol University, Bingol, Turkey
Haroon Ahmed
Affiliation:
Department of Biosciences, COMSATS University Islamabad, Park Road, Chakh Shahzad, Islamabad, Pakistan
*
Author for correspondence: Sami Simsek, E-mail: ssimsek@firat.edu.tr
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Abstract

Larval stage of genus Echinococcus is the causing agent for the zoonotic infection which is life threatening known as Echinococcosis. The purpose of this study was the identification, molecular analysis and characterization of Echinococcus spp. in sheep and cattle. The sampling was done from slaughterhouse of Elazig, Turkey. A total of 85 isolates (sheep, n = 19 and cattle, n = 66) have been collected after slaughtering. Following the gDNA isolation and PCR products of mt-CO1 gene (446 bp) of all the samples were sequenced. Out of 85 isolates, 84 were recognized as Echinococcus granulosus sensu stricto and one sheep isolate was found as Echinococcus canadensis (G6/G7 ) which is identified for the first time in Turkey. However, single nucleotide polymorphism has been observed not only in samples of different animals but also in samples collected from the same cattle. Six liver and three lung hydatid cysts have been detected in cattle. Although no nucleotide differences have been observed in the liver samples, there was single nucleotide polymorphism (C→T) in 40th nucleotide of two lung cysts. As a result of haplotype analysis, 16 haplotypes of E. granulosus s.s. were detected in 66 cattle isolates whereas 7 haplotypes of E. granulosus s.s. were identified in 19 sheep samples.

Keywords

CattleEchinococcus granulosushaplotypePCRsequencesheepTurkey

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Type
Research Article
Information
Parasitology , Volume 147 , Issue 9 , August 2020 , pp. 1055 - 1062
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Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Agudelo Higuita, NI, Brunetti, E and McCloskey, C (2016) Cystic echinococcosis. Journal of Clinical Microbiology 54, 518–523.CrossRefGoogle ScholarPubMed
Al-Kitani, FA, Baqir, S, Hussain, MH and Roberts, D (2014) Cystic hydatidosis in slaughtered goats from various municipal abattoirs in Oman. Tropical Animal Health and Production 46, 1357–1362.CrossRefGoogle ScholarPubMed
Al-Kitani, FA, Baqir, S, Hussain, MH and Robert, D (2015) Prevalence and molecular characterization of Echinococcos granulosus in cattle in Oman. Global Veterinaria 14, 883–891.Google Scholar
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
Alvarez Rojas, CA, Ebi, D, Gauci, CG, Scheerlinck, JP, Wassermann, M, Jenkins, DJ, Lightowlers, MW and Romig, T (2016) Microdiversity of Echinococcus granulosus sensu stricto in Australia. Parasitology 143, 1026–1033.CrossRefGoogle ScholarPubMed
Badaraco, JL, Ayala, FJ, Bart, JM, Gottstein, B and Haag, KL (2008) Using mitochondrial and nuclear markers to evaluate the degree of genetic cohesion among Echinococcus populations. Experimental Parasitology 119, 453–459.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
Bowles, DP, Blair, J and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Casulli, A, Interisano, M, Sreter, T, Chitimia, L, Kirkova, Z, Rosa, GL 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
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
Fu, YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.Google ScholarPubMed
Galeh, TM, Spotin, A, Mahami-Oskouei, M, Carmena, D, Rahimi, MT, Barac, A, Ghoyounchi, R, Berahmat, R and Ahmadpour, E (2018) The seroprevalence rate and population genetic structure of human cystic echinococcosis in the Middle East: a systematic review and meta-analysis. International Journal of Surgery 51, 39–48.CrossRefGoogle ScholarPubMed
Haag, KL, Ayala, FJ, Kamenetzky, L, Gutierrez, AM and Rosenzvit, M (2004) Livestock trade history, geography, and parasite strains: the mitochondrial genetic structure of Echinococcus granulosus in Argentina. Journal of Parasitology 90, 234–239.CrossRefGoogle ScholarPubMed
Kamenetzky, L, Gutierrez, AM, Canova, SG, Haag, KL, Guarnera, EA, Parra, A, García, GE and Rosenzvit, MC (2002) Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infection, Genetics and Evolution 2, 129–136.CrossRefGoogle ScholarPubMed
Kebede, W, Hagos, A, Girna, Z and Lobago, F (2009) Echinococcosis/hydatidosis: its prevalence, economic and public health significance in Tigray region. Tropical Animal Health and Production 41, 865–871.CrossRefGoogle ScholarPubMed
Kesik, HK, Simsek, S, Kilinc, SG and Koroglu, E (2019a) Identification of antigen B (AgB) gene polymorphism in cattle and sheep isolates of Echinococcus granulosus and investigation of effects on serological diagnosis. Acta Tropica 199, 105099.CrossRefGoogle Scholar
Kesik, HK, Kilinc, SG, Simsek, S and Gul, A (2019b) Occurrence of liver hydatid cysts in a donkey and molecular characterization of Echinococcus equinus. Journal of Parasitology 105, 442–445.Google Scholar
Khademvatan, S, Majidiani, H, Foroutan, M, Hazrati Tappeh, K, Aryamand, S and Khalkhali, HR (2019) Echinococcus granulosus genotypes in Iran: a systematic review. Journal of Helminthology 93, 131–138.CrossRefGoogle ScholarPubMed
Kinkar, L, Laurimäe, T, Acosta-Jamett, G, Andresiuk, V, Balkaya, I, Casulli, A, Gasser, RB, van der Giessen, J, González, LM, Haag, KL, Zait, H, Irshadullah, M, Jabbar, A, Jenkins, DJ, Kia, EB, Manfredi, MT, Mirhendi, H, M'rad, S and Rostami-Nejad, M (2018 a) Distinguishing Echinococcus granulosus sensu stricto genotypes G1 and G3 with confidence: a practical guide. Infection, Genetics and Evolution 64, 178–184.CrossRefGoogle Scholar
Kinkar, L, Laurimäe, T, Acosta-Jamett, G, Andresiuk, V, Balkaya, I, Casulli, A, Gasser, RB, van der Giessen, J, González, LM, Haag, KL, Zait, H, Irshadullah, M, Jabbar, A, Jenkins, DJ, Kia, EB, Manfredi, MT, Mirhendi, H, M'rad, S and Rostami-Nejad, M (2018 b) Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. International Journal for Parasitology 48, 729–742.CrossRefGoogle ScholarPubMed
Knudsen, B, Knudsen, T, Flensborg, M, Sandmann, H, Heltzen, M, Andersen, A, Dickenson, M, Bardram, J, Steffensen, PJ, Mansted, S, Lauritzen, T, Forsberg, R, Thanbichler, A, Bendtsen, JD, Gorlitz, L, Rasmussen, J, Tordrup, D, Vaerum, M, Ravn, MN, Hachenberg, C, Fisker, E, Dekker, P, Schultz, J, Hein, AMK and Sinding, JB (2007) CLC Main Workbench. Version 5.5. Aarhus, Denmark: CLC bio.Google 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
Leigh, J, Bryant, D andSteel, M (2015) PopART (Population Analysis with Reticulate Trees) (Technical report, University of Otago, New Zealand, http://popart.otago.ac.nz).Google 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 (2006) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713–722.CrossRefGoogle ScholarPubMed
Nakao, M, Li, M, Han, X, Ma, X, Xiao, N, Qiu, J, Wang, H, Yanagida, T, Mamuti, W, Wen, H, Moro, PL, Giraudoux, P, Craig, PS and Ito, A (2010) Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. International Journal for Parasitology 40, 379–385.CrossRefGoogle ScholarPubMed
Nakao, M, Lavikainen, A, Yanagida, T and Ito, A (2013 a) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). International Journal for Parasitology 43, 1017–1029.CrossRefGoogle Scholar
Nakao, M, Yanagida, T, Konyaev, S, Lavikainen, A, Odnokurtsev, VA and Zaikov, VA (2013 b) Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 140, 1625–1636.CrossRefGoogle ScholarPubMed
Omer, RA, Dinkel, A, Romig, T, Mackenstedt, U, Elnahas, AA, Aradaib, IE, Ahmed, ME, Elmalik, KH and Adam, A (2010) A molecular survey of cystic echinococcosis in Sudan. Veterinary Parasitology 169, 340–346.CrossRefGoogle ScholarPubMed
Roinioti, E, Papathanassopoulou, A, Theodoropoulou, I and Simsek, S (2016) Molecular identification of Echinococcus granulosus isolates from ruminants in Greece. Veterinary Parasitology 226, 138–144.CrossRefGoogle Scholar
Romig, T, Ebi, D and Lato, MW (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology 213, 76–84.CrossRefGoogle ScholarPubMed
Rostami, S, Talebi, S, Babaei, Z, Sharbatkhori, M, Ziaali, N, Rostami, H and Harandi, MF (2013) High resolution melting technique for molecular epidemiological studies of cystic echinococcosis: differentiating G1, G3, and G6 genotypes of Echinococcus granulosus sensu lato. Parasitology Research 112, 3441–3447.CrossRefGoogle Scholar
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
Sevinc, B, Karahan, O, Simsek, G, Bakdik, S, Aksoy, N and Soydan, S (2016) Role of different treatment modalities in cavity volume during the treatment of cystic echinococcosis. Turkiye Parazitoloji Dergisi 40, 63–66.Google Scholar
Simsek, S, Kaplan, M and Ozercan, IH (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
Smyth, JD and Smyth, MM (1964) Natural and experimental hosts of Echinococcus granulosus and E. Multilocularis, with comments on the genetics of speciation in the genus Echinococcus. Parasitology 54, 493–514.CrossRefGoogle Scholar
Snábel, 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
Tajima, F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google ScholarPubMed
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Yazar, S, Ok, AT, Hokelek, M, Polat, E, Yilmaz, H, Ozbilge, H, Ustun, S, Koltas, IS, Ertek, M, Sakru, N, Alver, O, Cetinkaya, Z, Koc, Z, Demirci, M, Aktas, H, Parsak, CK, Ozerdem, D, Sakman, G, Cengiz, ZT, Ozer, A, Keklik, K, Yemenici, N, Turan, M, Dastan, A, Kaya, E, Tamer, GS, Kilimcioglu, AA, Turk, M, Sinirtas, M, Evci, C, Kilicturgay, S, Mutlu, F and Artis, T (2008) Cystic Echinococcosis in Turkey from 2001–2005. Turkiye Parazitoloji Dergisi 32, 208–220, (in Turkish, with English abstract).Google ScholarPubMed