Abstract
Cystic echinococcosis is a neglected, zoonotic disease in Turkey. The disease is commonly seen in rural areas where the local population is in close contact with livestock and dogs. This research aimed to molecularly identify of hydatid cysts in cattle and human isolates from Konya, Turkey. Following sample collection, direct microscopy was performed. After direct examination, total DNA was extracted, and positive PCR products of cox 1 mitochondrial gene (~ 875 bp) were sequenced. A total of 83 hydatid cysts (cattle n = 57 and human n = 26), 82 were identified as Echinococcus granulosus sensu stricto (G1–G3 genotypes), and one human isolate was characterized as Echinococcus equinus (G4 genotype). Fertility rates of cysts belonging to cattle for liver and lung cysts were 93.3% and 80%, respectively. Out of 26 human originated isolates, 18 (69.2%) of cysts were found to be fertile. To the best of our knowledge, this is the first report of E. equinus from human host in Turkey.
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Abiyot J, Beyene D, Abunna F (2011) Prevalence of hydatidosis in small ruminants and its economic significance in Modjo Modern Export Abattoir, Ethiopia. J Public Health Epidemiol 3:454–461
Alvarez Rojas CA, Romig T, Lightowlers MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. Int J Parasitol 44:9–18. https://doi.org/10.1016/j.ijpara.2013.08.008
Bakal U, Simsek S, Kazez A (2015) Surgical and molecular evaluation of pediatric hydatid cyst cases in eastern Turkey. Korean J Parasitol 53:785–788. https://doi.org/10.3347/kjp.2015.53.6.785
Boufana B, Stidworthy MF, Bell S, Chantrey J, Masters N, Unwin S, Wood R, Lawrence RP, Potter A, McGarry J, Redrobe S, Killick R, Foster AP, Mitchell S, Greenwood AG, Sako Y, Nakao M, Ito A, Wyatt K, Lord B, Craig PS (2012) Ecinococcus and Taenia spp. from captive mammals in the United Kingdom. Vet parasitol 190:95–103. https://doi.org/10.1016/j.vetpar.2012.05.023
Boufana B, Lahmar S, Rebai W et al (2014) Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Trans R Soc Trop Med Hyg 108:706–714
Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–174. https://doi.org/10.1016/0166-6851(92)90109-w
Busi M, Snábel V, Varcasia A, Garippa G, Perrone V, De Liberato C, D’Amelio S (2007) Genetic variation within and between G1 and G3 genotypes of Echinococcus granulosus in Italy revealed by multilocus DNA sequencing. Vet Parasitol 150:75–83. https://doi.org/10.1016/j.vetpar.2007.09.003
Cardona GA, Carmena D (2013) A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet parasitol 192:10–32. https://doi.org/10.1016/j.vetpar.2012.09.027
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, Jenkins EJ (2017) Global distribution of alveolar and cystic echinococcosis. Adv Parasitol 95:315–493. https://doi.org/10.1016/bs.apar.2016.11.001
Eckert J, Schantz PM, Gasser RB, Torgerson PR, Bessonov AS, Movsessian SO (2001) Geographic distribution and prevalence. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (eds) WHO/OIE Manual on echinococcosis in human and animals: a public health problem of global concern. World Organisation for Animal Health, Paris, pp 100–142
Erdoğan E, Özkan B, Mutlu F, Karaca S, Şahin İ (2017) Molecular characterization of Echinococcus granulosus isolates obtained from different hosts. Mikrobiyol Bul 51:79–86. https://doi.org/10.5578/mb.45452
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, Kocazeybek B (2010) Genotypic characterisation of Echinococcus granulosus isolated from human in Turkey. Afr J Microbiol Res 4:551–555
Eroglu F, Genc A, Koltas IS (2016) The genotyping of Echinococcus granulosus isolates with PCR-RFLP Methods in Adana Province. Zirve Med J 1:22–25
Eryıldız C, Sakru N (2012) Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan Med J 29:261–267. https://doi.org/10.5152/balkanmedj.2012.072
Esatgil MU, Tuzer E (2007) Prevalence of hydatidosis in slaughtered animals in Thrace, Turkey. Türkiye Parazitol Derg 31:41–45
Fikire Z, Tolosa T, Nigussie Z, Macias C, Kebede N (2012) Prevalence and characterization of hydatidosis in animals slaughtered at Addis Ababa abattoir, Ethiopia. J Parasitol Vector Biol 4:1–6
Galeh TM, Spotin A, Mahami-Oskouei M, Carmena D, Rahimi MT, Barac A, Ghoyounchi R, Berahmat R, Ahmadpour E (2018) The seroprevalence rate and population genetic structure of human cystic echinococcosis in the Middle East: a systematic review and meta-analysis. Int J Surg 51:39–48. https://doi.org/10.1016/j.ijsu.2018.01.025
Kesik HK, Kilinc SG, Simsek S, Gul A (2019) Occurrence of liver hydatid cysts in a donkey and molecular characterization of Echinococcus equinus. J Parasitol 105:442–445. https://doi.org/10.1645/19-3
King CH (2005) Cestodes (Tapeworms). In: Mandell GL, Bennet JE, Dolin R (eds) Mandell, Douglas, and Bennett’s principles and practice of infectious diseases, 6th edn. Elsevier Churchill Livingstone, Philadelphia, pp 3285–3293
Knapp J, Gottstein B, Saarma U, Millon L (2015) Taxonomy, phylogeny and molecular epidemiology of Echinococcus multilocularis: from fundamental knowledge to health ecology. Vet Parasitol 213:85–91. https://doi.org/10.1016/j.vetpar.2015.07.030
Kose M, Sevimli KF (2008) Prevalence of cystic echinococcosis in slaughtered cattle in Afyonkarahisar. Turkiye Parazitol Derg 32:27–30
Kumaratilake LM, Thompson RCA, Eckert J (1986) Echinococcus granulosus of equine origin from different countries possess uniform morphological characteristics. Int J Parasitol 16:529–540. https://doi.org/10.1016/0020-7519(86)90089-5
Kurt A, Avcioglu H, Guven E, Balkaya I, Oral A, Kirman R, Bia MM, Akyuz M (2020) 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 Zoonotic Dis Online ahead of print. 20:593–602. https://doi.org/10.1089/vbz.2019.2594
Nakao M, Yangıda T, Okomoto M, Knapp J, Nkouawa A, Sako Y, Ito A (2010) State-of-the-art Echinococcus and Taenia: phylogenetic taxonomy of human pathogenic tapeworms an its application to molecular diagnosis. Infect Genet Evol 10:444–452. https://doi.org/10.1016/j.meegid.2010.01.011
Nakao M, Lavikainen A, Yanagida T, Ito A (2013) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). Int J Parasitol 43:1017–1029. https://doi.org/10.1016/j.ijpara.2013.06.002
Orsten S, Boufana B, Ciftci T, Akinci D, Karaagaoglu E, Ozkuyumcu C, Casulli A, Akhan O (2018) Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients. Parasitol Res 117:1257–1263. https://doi.org/10.1007/s00436-018-5807-9
Örsten S, Çiftçi T, Azizova A, Yüce G, Uysal A, İmamoğlu Ç, Karaağaoğlu E, Akıncı D, Akyön Y, Casulli A, Akhan O (2020) Investigation of the relationship between CE cyst characteristics and genetic diversity of Echinococcus granulosus sensu lato in humans from Turkey. Parasitology. 147(14):1712–1717. https://doi.org/10.1017/S0031182020001535
Ponce Gordo F, Cuesta BC (1998) Observations on the Echinococcus granulosus horse strain in Spain. Vet Parasitol 76:65–70. https://doi.org/10.1016/s0304-4017(97)00087-3
Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, De La Rue M (2017) Ecology and life cycle patterns of Echinococcus species. Adv parasit 95:213–314. https://doi.org/10.1016/bs.apar.2016.11.002
Sadjjadi SM (2006) Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol Int 55:197–202. https://doi.org/10.1016/j.parint.2005.11.030
Schneider R, Gollackner B, Edel B, Schmid K, Wrba F, Tucek G, Walochnik J, 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. Int J Parasitol 38:1065–1071. https://doi.org/10.1016/j.ijpara.2007.11.008
Simsek S, Cevik A (2014) First detection and molecular characterization of Echinococcus equinus in a mule in Turkey. Acta parasitol 59:773–777
Simsek S, Balkaya I, Ciftci AT, Utuk AE (2011) Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Vet Parasitol 178:367–369. https://doi.org/10.1016/j.vetpar.2011.01.033
Smyth MB (1977) Effectively given domains. Theor Comput Sci 5:257–274
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, Dubinský P (2009) Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitol Res 105:145–154. https://doi.org/10.1007/s00436-009-1376-2
Thompson RCA, Mc Manus DP (2001) Aetiology: parasites and life cycles. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (eds) WHO/OIE manual on echinococcosis in human and animals: a public health problem of global concern. World Organisation for Animal Health, Paris, pp 1–19
Thompson RA, McManus DP (2002) Towards a taxonomic revision of the genus Echinococcus. Trends Parasitol 18:452–457. https://doi.org/10.1016/s1471-4922(02)02358-9
Umhang G, Chihai O, Boué F (2014a) Molecular characterization of Echinococcus granulosus in a hyperendemic European focus, the Republic of Moldova. Parasitol Res 113:4371–4376. https://doi.org/10.1007/s00436-014-4112-5
Umhang G, Richomme C, Hormaz V, Boucher JM, Boué F (2014b) Pigs and wild boar in Corsica harbor Echinococcus canadensis G6/7 at levels of concern for public health and local economy. Acta trop 133:64–68. https://doi.org/10.1016/j.actatropica.2014.02.005
Umur S (2003) Prevalence and economic importance of cystic echinococcosis in slaughtered ruminants in Burdur, Turkey. J Vet Med B 50:247–252. https://doi.org/10.1046/j.1439-0450.2003.00667.x
Utuk AE, Simsek S (2013) Molecular characterization of the horse isolate of Echinococcus granulosus in Turkey. J Helminthol 87:305–308. https://doi.org/10.1017/S0022149X12000363
Utuk AE, Simsek S, Koroglu E, McManus DP (2008) Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta Trop 107:192–194. https://doi.org/10.1016/j.actatropica.2008.05.026
Varcasia A, Canu S, Kogkos A, Pipia AP, Scala A, Garippa G, Seimenis A (2007) Molecular characterization of Echinococcus granulosus in sheep and goats of Peloponnesus, Greece. Parasitol Res 101:1135–1139. https://doi.org/10.1007/s00436-007-0568-x
Varcasia A, Garippa G, Pipia AP, Scala A, Brianti E, Giannetto S, Micagni G (2008) Cystic echinococcosis in equids in Italy. Parasitol res 102:815–818. https://doi.org/10.1007/s00436-007-0862-7
Williams RJ, Sweatman GK (1963) On the transmission, biology and morphology of Echinococcus granulosus equinus, a new subspecies of hydatid tapeworm in horses in Great Britain. Parasitology 53:391–407. https://doi.org/10.1017/s0031182000073844
Yildiz K, Gurcan S (2003) Prevalence of hydatidosis and fertility of hydatid cysts in sheep in Kırıkkale, Turkey. Acta Vet Hung 51:181–187. https://doi.org/10.1556/AVet.51.2003.2.6
Yildiz K, Tunçer C (2005) Prevalence of hydatid cysts in cattle in the province of Kırıkkale. Turkiye Parazitol Derg 29:247–250
Tamarozzi F, Legnardi M, Fittipaldo A, Drigo M, Cassini R (2020) Epidemiological distribution of Echinococcus granulosus s.l. infection in human and domestic animal hosts in European Mediterranean and Balkan countries: A systematic review. PLoS Negl Trop Dis 14(8):e0008519
Casulli A, Siles-Lucas M, Tamarozzi F (2019) Echinococcus granulosus sensu lato. Trends Parasitol 35(8):663–664
Chihai O, Umhang G, Erhan D, Boué F, Tălămbuţă N, Rusu Ş, Zamornea M (2016) Slaughterhouse survey of cystic echinococcosis in cattle and sheep from the Republic of Moldova. J Helminthol 90(3):279–83
Founta A, Chliounakis S, Antoniadou Sotiriadou K, Koidou M, Bampidis V (2016) Prevalence of hydatidosis and fertility of hydatid cysts in food animals in Northern Greece. Vet Ital 52(2):123–7
Boufana B, Lett W, Lahmar S, Griffiths A, Jenkins DJ, Buishi I, Engliez SA, Alrefadi MA, Eljaki AA, Elmestiri FM, Reyes MM, Pointing S, Al-Hindi A, Torgerson PR, Okamoto M, Craig PS (2015) Canine echinococcosis: genetic diversity of Echinococcus granulosus sensu stricto (s.s.) from definitive hosts. J Helminthol 89(6):689-98
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This project is supported by the Selcuk University Scientific Research Coordination Centre (project number: BAP/18401134).
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Macin, S., Orsten, S., Samadzade, R. et al. Human and animal cystic echinococcosis in Konya, Turkey: molecular identification and the first report of E. equinus from human host in Turkey. Parasitol Res 120, 563–568 (2021). https://doi.org/10.1007/s00436-021-07050-w
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DOI: https://doi.org/10.1007/s00436-021-07050-w