An overview of the genetic diversity of Echinococcus granulosus sensu lato in Turkey
Year 2022,
Volume: 12 Issue: 6, 1025 - 1029, 30.11.2022
Sümeyye Başer
,
Salih Maçin
,
Gülay Maçin
,
Serra Örsten
Abstract
Echinococcus granulosus is a parasite that lives as a host in animals and humans, causes great economic damage and poses a serious threat to health. Morphological differences and intermediate host preference are used to distinguish the species of this parasite. Ten genotypes and lion strains of Echinococcus granulosus have been identified in molecular studies to date. It contributes to the fact that the effects of cystic echinococcosis detected in humans and the disease process caused by different genotypes can be handled differently. In genetic diversity analysis, species were classified as Echinococcus granulosus sensu stricto, Echinococcus equinus, Echinococcus ortleppi, Echinococcus canadensis and Echinococcus felidis genotypes. Echinococcus granulosus sensu stricto is the most common cause of human cystic echinococcosis worldwide and in Turkey. In this review, the distribution and epidemiology of Echinococcus granulosus genotypes detected in humans and animals in Turkey are discussed.
References
- 1- World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases: a roadmap for implementation: executive summary. Geneva: World Health Organization; 2012.
- 2- Food and Agriculture Organization of the United Nations/World Health Organization. Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series No. 23. Rome: FAO/WHO; 2014.
- 3- Başer S, Ismayıl A, Maçin S. Evaluation of the seropositivity of patients with cystic echinococcosis in Konya, Turkey. Journal of Contemporary Medicine. 2021; 11(2):139-41.
- 4- Macin S, Samadzade R. (2022). Investigation of Direct Microscopy and Indirect Hemagglutination Test Results in the Diagnosis of Echinococcus granu-losus in Selçuk University Hospital. International Journal of Echinococcoses 2022; 1 (2): 33-7.
- 5- McManus DP, Gray DJ, Zhang W, Yang Y. Diagnosis, treatment, and management of echinococcosis. BMJ. 2012;344: e3866.
- 6- Korhonen PK, Kinkar L, Young ND, Cai H, Lightowlers MW, Gauci C. et al. Chromosome-scale Echinococcus granulosus (genotype G1) genome reveals the Eg95 gene family and conservation of the EG95-vaccine molecule. Communications biology. 2022; 5(1): 199.
- 7- Manterola C, Totomoch-Serra A, Rojas C, Riffo-Campos ÁL, García-Méndez N. Echinococcus granulosus sensu lato Genotypes in Different Hosts Worldwide: A Systematic Review. Acta parasitologica. 2022; 67(1): 161-85.
- 8- Manterola C, Otzen T. Molecular epidemiology of cystic echinococcosis: genotypic characterization in humans and different livestock. Int J Morphol. 2016; 34:1472-81.
- 9- Busi M, Snábel V, Varcasia A, Garippa G, Perrone V, Liberato CD. et al. Genetic variation within and between G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Vet Parasitol. 2007;150:75–83.
- 10- Miambo RD, Afonso SMS, Noormahomed EV, Pondja A, Mukaratirwa S. Echinococcosis in humans and animals in Southern Africa development community countries: a systematic review. Food Waterborne Parasitol. 2020; 20:e00087.
- 11- Mansoor Jadaan AA. Molecular detection of Hydatid cyst isolated from Goats in AL-Qadisiyia province by Polymerase Chain Reaction. Kufa J Vet Sci. 2015; 6:191-5
- 12- Eckert J, Thompson RCA. Intraspesific variation of Echinococcus granulosus and related species with emphises on their infectivity to humans. Acta Tropica. 1997;64: 19-34.
- 13- Daniel Mwambete K, Ponce-Gordo F, Cuesta-Bandera C. Genetic identification and host range of the Spanish strains of Echinococcus granulosus. Acta Trop. 2004; 91: 87-93.
- 14- Capuano F, Rinaldi L, Maurelli MP, Perugini AG, Veneziano V, Garippa G. et al. Cystic echinococcosis in water buffaloes: epidemiological survey and molecular evidence of ovine (G1) and buffalo (G3) strains. Vet Parasitol. 2006;137(3-4): 262-8.
- 15- Cystic echinococcal liver disease: new insights into an old disease and an algorithm for therapy planning. Rozanes I, Güven K, Acunaş B, Emre A Cardiovasc Intervent Radiol. 2007; 30(6):1112-6
- 16- Kowalczyk M., Kurpiewski W., Zieliński E., Zadrożny D., Klepacki Ł., Juśkiewicz W., Lasocki J., Dyśko Ł., Batia K., Pesta W. A rare case of the simultaneous location of Echinococcus multilocularis in the liver and the head of the pancreas: Case report analysis and review of literature. BMC Infect. Dis. 2019;19:1–6.
- 17- Dinkel A, Njoroge EM, Zimmermann A. A PCR system for detection of species and genotypes of the Echinococcus granulosus complex, with reference to the epidemiological situation in eastern Africa. Int J Parasitol. 2004; 34: 645-53.
- 18- Bowles J, McManus DP. Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Mol Biochem Parasitol. 1993;57(2):231-9.
- 19- Snábel V, Altintas N, D'Amelio S, Nakao M, Romig T, Yolasigmaz A. et al Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitology research, 2009;105(1):145-54.
- 20- Simsek S, Kaplan M, Ozercan IH. A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitology research. 2011; 109(2): 411-6.
- 21- Eryıldız C, Sakru N. Molecular Characterization of Human and Animal Isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan medical journal. 2012; 29(3):261-7.
- 22- Bakal U, Simsek S, Kazez A. Surgical and Molecular Evaluation of Pediatric Hydatid Cyst Cases in Eastern Turkey. Korean J Parasitol. 2015;53(6):785-8.
- 23- Fadime Eroğlu, Genç A, Koltaş SA. Adana İlindeki Echinococcus granulosus izolatlarının PCR-RFLP Yöntemi ile Genotiplendirilmesi. Zirve Tıp Dergisi. 2016; 1 ( 1): 22-5.
- 24- Oral Babaoğlu A, Soyder A, Malatyalı E, Ertuğ S, Ertabaklar H. Aydın’da Echinococcus granulosus izolatlarının mitokondriyal sitokrom C oksidaz alt ünite 1 geni (cox1) dizi analizi ile genotiplendirilmesi [Genotyping of Echinococcus granulosus isolates by sequencing of mitochondrial cytochrome C oxidase subunit 1 (cox1) gene in Aydin]. Mikrobiyoloji bülteni. 2018; 52(2):198–205.
- 25- Orsten S, Boufana B, Ciftci T, Akinci D, Karaagaoglu E, Ozkuyumcu C. et al. Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients. Parasitology research. 2018;117(4): 1257-63.
- 26- Kurt A, Avcioglu H, Guven E, Balkaya I, Oral A, Kirman R.et al. Molecular Characterization of Echinococcus multilocularis and Echinococcus granulosus from Cysts and Formalin-Fixed Paraffin-Embedded Tissue Samples of Human Isolates in Northeastern Turkey. Vector borne and zoonotic diseases (Larchmont, N.Y.). 2020; 20(8): 593–602.
- 27- Örsten S, Çiftçi T, Azizova A, Yüce G, Uysal A, İmamoğlu Ç. et al. Investigation of the relationship between CE cyst characteristics and genetic diversity of Echinococcus granulosus sensu lato in humans from Turkey. Parasitology. 2020; 147(14): 1712-7.
- 28- Beyhan YE, Çobanoğlu U, Çelik S, Yılmaz H, Halidi AG. Molecular characterization of human lung and liver cystic echinococcosis isolates in Van Province, Turkey. Acta tropica. 2020;206: 105451.
- 29- Macin S, Orsten S, Samadzade R, Colak B, Cebeci H, Fındık D. Human and animal cystic echinococcosis in Konya, Turkey: molecular identification and the first report of E. equinus from human host in Turkey. Parasitology research. 2021;120(2): 563–8.
- 30- Shahabi S, Sarkari B, Barazesh A. Echinococcus granulosus sensu stricto G1 is the predominant genotype in human and livestock isolates from Turkey and Iran, based on mitochondrial nad5 gene differentiation. Parasites & vectors. 2021; 14(1): 369.
- 31- Eroglu F, Dokur M, Ulu Y. The Molecular Epidemiology of Cystic and Alveolar Echinococcosis in Southeast Turkey. Iranian journal of parasitology. 2021; 16(2): 327–35.
- 32- Vural G, Baca AU, Gauci CG, Bagci O, Gicik Y, Lightowlers, MW. 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. 2008; 154(3-4): 347-50.
- 33- Utuk AE, Simsek S, Koroglu E, McManus DP. Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta tropica. 2008;107(2):192-4.
- 34- Simsek S, Balkaya I, Koroglu E. Epidemiological survey and molecular characterization of Echinococcus granulosus in cattle in an endemic area of eastern Turkey. Veterinary parasitology. 2010; 172(3-4): 347-9.
- 35- Simsek S, Balkaya I, Ciftci AT, Utuk AE. Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Veterinary parasitology. 2011; 178(3-4): 367-9.
- 36- Beyhan YE, Umur S. Molecular characterization and prevalence of cystic echinococcosis in slaughtered water buffaloes in Turkey. Veterinary parasitology. 2011; 181(2-4): 174-9.
- 37- Utuk AE, Simsek S. Molecular characterization of the horse isolate of Echinococcus granulosus in Turkey. Journal of helminthology. 2013; 87(3): 305-8.
- 38- Oguz B, Ozdal N, Kilinc OO, Serdar Deger M. Preliminary Studies on the Prevalence and Genotyping of Echinococcus Granulosus Infection in Stray Dogs in Van Province, Turkey. Journal of veterinary research. 2018; 62(4):497–502.
- 39- Kesik HK, Kilinc SG, Simsek S, Gul A. Occurrence of Liver Hydatid Cysts in a Donkey and Molecular Characterization of Echinococcus equinus. The Journal of parasitology. 2019; 105(3): 442-5.
- 40- Barazesh A, Sarkari B, Sarısu G, Hami M, Mikaeili F, Aydın A. Comparative Genotyping of Echinococcus granulosus Infecting Livestock in Turkey and Iran. Turkiye parazitolojii dergisi. 2019; 43(3):123–9.
- 41- Mehmood S, Simsek S, Celik F, Kesik HK, Kilinc SG, Ahmed H. Molecular survey on cattle and sheep hydatidosis and first detection of Echinococcus canadensis (G6/G7) in sheep in Turkey. Parasitology. 2020;147(9): 1055–62.
- 42- Cengiz G, Gonenc B. Comparison of molecular and morphological characterization and haplotype analysis of cattle and sheep isolates of cystic echinococcosis. Veterinary parasitology. 2020; 282, 109132.
- 43- Kesik HK, Celik F, Simsek S, Kilinc SG, Ahmed H, Gul A. Molecular Characterization and Haplotype Analyses of Lung Hydatid Cyst Isolates of Cattle and First Report of Echinococcus canadensis (G6/G7) in Cattle Isolates in Turkey. Acta parasitologica. 2021;66(4):1538-47.
- 44- Kesik HK, Çelik F, Günyaktı Kılınç Ş, Karabulut B, Çevik A, Şimşek, S. Molecular Characterization of Hydatid Cysts Cases in a Wild Boar and Mule in Turkey. Türkiye’de Bir Yaban Domuzu ile Bir Katırda Hidatid Kist Olgusu ve Moleküler Karakterizasyonu. Turkiye parazitolojii dergisi. 2021; 45(1): 28–33.
Türkiye'deki Echinococcus granulosus sensu lato'nun genetik çeşitliliğine genel bir bakış
Year 2022,
Volume: 12 Issue: 6, 1025 - 1029, 30.11.2022
Sümeyye Başer
,
Salih Maçin
,
Gülay Maçin
,
Serra Örsten
Abstract
Echinococcus granulosus hayvanlarda ve insanlarda konak olarak yaşayarak büyük ekonomik zarar oluşturan ve sağlık açısından önemli tehdit oluşturan bir parazittir. Morfolojik farklılıkları ve ara konak tercihi bu parazitin türlerini ayırt etmede kullanılmaktadır. Günümüze kadar yapılan moleküler çalışmalarda Echinococcus granulosus'un on genotipi ve aslan suşu tespit edilmiştir. İnsanlarda tespit edilen kistik ekinokokkoz ile farklı genotiplerin oluşturduğu hastalık sürecinde de etkilerinin de farklı olarak ele alınabilmesi açısından katkı sağlamaktadır. Genetik çeşitlilik analizinde Echinococcus granulosus sensu stricto, Echinococcus equinus, Echinococcus ortleppi, Echinococcus canadensis ve Echinococcus felidis genotipi şeklinde türler sınıflandılmıştır. Echinococcus granulosus sensu stricto insan kistik ekkinokkozunda dünya ve Türkiye çapında en çok görülen etkendir. Bu derlemede de, Türkiye'de insan ve hayvanlarda tespit edilen Echinococcus granulosus genotiplerinin dağılımı ve epidemiyolojisi tartışılmıştır.
References
- 1- World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases: a roadmap for implementation: executive summary. Geneva: World Health Organization; 2012.
- 2- Food and Agriculture Organization of the United Nations/World Health Organization. Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series No. 23. Rome: FAO/WHO; 2014.
- 3- Başer S, Ismayıl A, Maçin S. Evaluation of the seropositivity of patients with cystic echinococcosis in Konya, Turkey. Journal of Contemporary Medicine. 2021; 11(2):139-41.
- 4- Macin S, Samadzade R. (2022). Investigation of Direct Microscopy and Indirect Hemagglutination Test Results in the Diagnosis of Echinococcus granu-losus in Selçuk University Hospital. International Journal of Echinococcoses 2022; 1 (2): 33-7.
- 5- McManus DP, Gray DJ, Zhang W, Yang Y. Diagnosis, treatment, and management of echinococcosis. BMJ. 2012;344: e3866.
- 6- Korhonen PK, Kinkar L, Young ND, Cai H, Lightowlers MW, Gauci C. et al. Chromosome-scale Echinococcus granulosus (genotype G1) genome reveals the Eg95 gene family and conservation of the EG95-vaccine molecule. Communications biology. 2022; 5(1): 199.
- 7- Manterola C, Totomoch-Serra A, Rojas C, Riffo-Campos ÁL, García-Méndez N. Echinococcus granulosus sensu lato Genotypes in Different Hosts Worldwide: A Systematic Review. Acta parasitologica. 2022; 67(1): 161-85.
- 8- Manterola C, Otzen T. Molecular epidemiology of cystic echinococcosis: genotypic characterization in humans and different livestock. Int J Morphol. 2016; 34:1472-81.
- 9- Busi M, Snábel V, Varcasia A, Garippa G, Perrone V, Liberato CD. et al. Genetic variation within and between G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Vet Parasitol. 2007;150:75–83.
- 10- Miambo RD, Afonso SMS, Noormahomed EV, Pondja A, Mukaratirwa S. Echinococcosis in humans and animals in Southern Africa development community countries: a systematic review. Food Waterborne Parasitol. 2020; 20:e00087.
- 11- Mansoor Jadaan AA. Molecular detection of Hydatid cyst isolated from Goats in AL-Qadisiyia province by Polymerase Chain Reaction. Kufa J Vet Sci. 2015; 6:191-5
- 12- Eckert J, Thompson RCA. Intraspesific variation of Echinococcus granulosus and related species with emphises on their infectivity to humans. Acta Tropica. 1997;64: 19-34.
- 13- Daniel Mwambete K, Ponce-Gordo F, Cuesta-Bandera C. Genetic identification and host range of the Spanish strains of Echinococcus granulosus. Acta Trop. 2004; 91: 87-93.
- 14- Capuano F, Rinaldi L, Maurelli MP, Perugini AG, Veneziano V, Garippa G. et al. Cystic echinococcosis in water buffaloes: epidemiological survey and molecular evidence of ovine (G1) and buffalo (G3) strains. Vet Parasitol. 2006;137(3-4): 262-8.
- 15- Cystic echinococcal liver disease: new insights into an old disease and an algorithm for therapy planning. Rozanes I, Güven K, Acunaş B, Emre A Cardiovasc Intervent Radiol. 2007; 30(6):1112-6
- 16- Kowalczyk M., Kurpiewski W., Zieliński E., Zadrożny D., Klepacki Ł., Juśkiewicz W., Lasocki J., Dyśko Ł., Batia K., Pesta W. A rare case of the simultaneous location of Echinococcus multilocularis in the liver and the head of the pancreas: Case report analysis and review of literature. BMC Infect. Dis. 2019;19:1–6.
- 17- Dinkel A, Njoroge EM, Zimmermann A. A PCR system for detection of species and genotypes of the Echinococcus granulosus complex, with reference to the epidemiological situation in eastern Africa. Int J Parasitol. 2004; 34: 645-53.
- 18- Bowles J, McManus DP. Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Mol Biochem Parasitol. 1993;57(2):231-9.
- 19- Snábel V, Altintas N, D'Amelio S, Nakao M, Romig T, Yolasigmaz A. et al Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitology research, 2009;105(1):145-54.
- 20- Simsek S, Kaplan M, Ozercan IH. A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitology research. 2011; 109(2): 411-6.
- 21- Eryıldız C, Sakru N. Molecular Characterization of Human and Animal Isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan medical journal. 2012; 29(3):261-7.
- 22- Bakal U, Simsek S, Kazez A. Surgical and Molecular Evaluation of Pediatric Hydatid Cyst Cases in Eastern Turkey. Korean J Parasitol. 2015;53(6):785-8.
- 23- Fadime Eroğlu, Genç A, Koltaş SA. Adana İlindeki Echinococcus granulosus izolatlarının PCR-RFLP Yöntemi ile Genotiplendirilmesi. Zirve Tıp Dergisi. 2016; 1 ( 1): 22-5.
- 24- Oral Babaoğlu A, Soyder A, Malatyalı E, Ertuğ S, Ertabaklar H. Aydın’da Echinococcus granulosus izolatlarının mitokondriyal sitokrom C oksidaz alt ünite 1 geni (cox1) dizi analizi ile genotiplendirilmesi [Genotyping of Echinococcus granulosus isolates by sequencing of mitochondrial cytochrome C oxidase subunit 1 (cox1) gene in Aydin]. Mikrobiyoloji bülteni. 2018; 52(2):198–205.
- 25- Orsten S, Boufana B, Ciftci T, Akinci D, Karaagaoglu E, Ozkuyumcu C. et al. Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients. Parasitology research. 2018;117(4): 1257-63.
- 26- Kurt A, Avcioglu H, Guven E, Balkaya I, Oral A, Kirman R.et al. Molecular Characterization of Echinococcus multilocularis and Echinococcus granulosus from Cysts and Formalin-Fixed Paraffin-Embedded Tissue Samples of Human Isolates in Northeastern Turkey. Vector borne and zoonotic diseases (Larchmont, N.Y.). 2020; 20(8): 593–602.
- 27- Örsten S, Çiftçi T, Azizova A, Yüce G, Uysal A, İmamoğlu Ç. et al. Investigation of the relationship between CE cyst characteristics and genetic diversity of Echinococcus granulosus sensu lato in humans from Turkey. Parasitology. 2020; 147(14): 1712-7.
- 28- Beyhan YE, Çobanoğlu U, Çelik S, Yılmaz H, Halidi AG. Molecular characterization of human lung and liver cystic echinococcosis isolates in Van Province, Turkey. Acta tropica. 2020;206: 105451.
- 29- Macin S, Orsten S, Samadzade R, Colak B, Cebeci H, Fındık D. Human and animal cystic echinococcosis in Konya, Turkey: molecular identification and the first report of E. equinus from human host in Turkey. Parasitology research. 2021;120(2): 563–8.
- 30- Shahabi S, Sarkari B, Barazesh A. Echinococcus granulosus sensu stricto G1 is the predominant genotype in human and livestock isolates from Turkey and Iran, based on mitochondrial nad5 gene differentiation. Parasites & vectors. 2021; 14(1): 369.
- 31- Eroglu F, Dokur M, Ulu Y. The Molecular Epidemiology of Cystic and Alveolar Echinococcosis in Southeast Turkey. Iranian journal of parasitology. 2021; 16(2): 327–35.
- 32- Vural G, Baca AU, Gauci CG, Bagci O, Gicik Y, Lightowlers, MW. 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. 2008; 154(3-4): 347-50.
- 33- Utuk AE, Simsek S, Koroglu E, McManus DP. Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta tropica. 2008;107(2):192-4.
- 34- Simsek S, Balkaya I, Koroglu E. Epidemiological survey and molecular characterization of Echinococcus granulosus in cattle in an endemic area of eastern Turkey. Veterinary parasitology. 2010; 172(3-4): 347-9.
- 35- Simsek S, Balkaya I, Ciftci AT, Utuk AE. Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Veterinary parasitology. 2011; 178(3-4): 367-9.
- 36- Beyhan YE, Umur S. Molecular characterization and prevalence of cystic echinococcosis in slaughtered water buffaloes in Turkey. Veterinary parasitology. 2011; 181(2-4): 174-9.
- 37- Utuk AE, Simsek S. Molecular characterization of the horse isolate of Echinococcus granulosus in Turkey. Journal of helminthology. 2013; 87(3): 305-8.
- 38- Oguz B, Ozdal N, Kilinc OO, Serdar Deger M. Preliminary Studies on the Prevalence and Genotyping of Echinococcus Granulosus Infection in Stray Dogs in Van Province, Turkey. Journal of veterinary research. 2018; 62(4):497–502.
- 39- Kesik HK, Kilinc SG, Simsek S, Gul A. Occurrence of Liver Hydatid Cysts in a Donkey and Molecular Characterization of Echinococcus equinus. The Journal of parasitology. 2019; 105(3): 442-5.
- 40- Barazesh A, Sarkari B, Sarısu G, Hami M, Mikaeili F, Aydın A. Comparative Genotyping of Echinococcus granulosus Infecting Livestock in Turkey and Iran. Turkiye parazitolojii dergisi. 2019; 43(3):123–9.
- 41- Mehmood S, Simsek S, Celik F, Kesik HK, Kilinc SG, Ahmed H. Molecular survey on cattle and sheep hydatidosis and first detection of Echinococcus canadensis (G6/G7) in sheep in Turkey. Parasitology. 2020;147(9): 1055–62.
- 42- Cengiz G, Gonenc B. Comparison of molecular and morphological characterization and haplotype analysis of cattle and sheep isolates of cystic echinococcosis. Veterinary parasitology. 2020; 282, 109132.
- 43- Kesik HK, Celik F, Simsek S, Kilinc SG, Ahmed H, Gul A. Molecular Characterization and Haplotype Analyses of Lung Hydatid Cyst Isolates of Cattle and First Report of Echinococcus canadensis (G6/G7) in Cattle Isolates in Turkey. Acta parasitologica. 2021;66(4):1538-47.
- 44- Kesik HK, Çelik F, Günyaktı Kılınç Ş, Karabulut B, Çevik A, Şimşek, S. Molecular Characterization of Hydatid Cysts Cases in a Wild Boar and Mule in Turkey. Türkiye’de Bir Yaban Domuzu ile Bir Katırda Hidatid Kist Olgusu ve Moleküler Karakterizasyonu. Turkiye parazitolojii dergisi. 2021; 45(1): 28–33.