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Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients

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Abstract

Cystic echinococcosis caused by the larval stages of Echinococcus granulosus sensu lato s.l is endemic in Turkey with a high public health impact particularly in rural areas. The aim of this study was to investigate the genetic variation and population structure of E. granulosus s.s using metacestode isolates removed from surgically confirmed patients originating from several regions in Turkey and to investigate the occurrence of autochthonous transmission. Using DNA extracted from a total of 46 human-derived CE isolates, we successfully analysed an 827-bp fragment within the cox1 mitochondrial gene and confirmed the causative agent of human cystic echinococcosis in patients included in this study to be Echinococcus granulosus s.s (G1 and G3 genotypes). The haplotype parsimony network consisted of 28 haplotypes arranged within three main clusters and the neutrality indices were both negative and significant indicating negative selection or population expansion. The assessment carried out in this study using GenBank nucleotide sequence data from Turkey for sheep and cattle hosts demonstrated the importance of autochthonous transmission with sheep, cattle and humans harbouring the same haplotypes. Further studies are required to investigate the biological significance, if any, of E. granulosus s.s haplotypes and the genetic variability of CE from human patients using longer nucleotide sequences and a larger sample set.

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References

  • Abdulhameed MF, Habib I, Al-Azizz SA, Robertson I (2018) A retrospective study of human cystic echinococcosis in Basrah province, Iraq. Acta Trop 178:130–133

    Article  PubMed  Google Scholar 

  • Acioz M (2008) The investigation of prevalence of echinococcosis in human by ELISA, in slaughter animals by observation and in dogs by PCR in Muş province. Dissertation, Cunhuriyet University

  • Altintas N (2003) Past to present: echinococcosis in Turkey. Acta Trop 85:105–112

    Article  PubMed  Google Scholar 

  • Altintas N (2008) Parasitic zoonotic diseases in Turkey. Vet Ital 44:633–646

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Beyhan YE, Umur S (2011) Molecular characterization and prevalence of cystic echinococcosis in slaughtered water buffaloes in Turkey. Vet Parasitol 181:174–179

    Article  PubMed  Google Scholar 

  • Boufana B, Lahmar S, Rebai W, Ben Safta Z, Jebabli L, Ammar A, Kachti M, Aouadi S, Craig PS (2014) Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Trans R Soc Trop Med Hyg 108:706–714

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–174

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (2001) In: WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. Paris OIE. pp. 1–265

  • 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

    CAS  Google Scholar 

  • Eroğlu 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

    Google Scholar 

  • Eryildiz C, Şakru N (2012) Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan Med J 29:261–267

    CAS  PubMed  PubMed Central  Google Scholar 

  • Esatgil MU, Tuzer E (2007) Prevalence of hydatidosis in slaughtered animals in Thrace, Turkey. Türkiye Parazitol Derg 31:41–45

    PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guzel M, Yaman M, Koltas IS, Demirkazik M, Aktas H (2008) Detection of Echinococcus granulosus coproantigens in dogs from Antakya Province, Turkey. Helminthologia 45:150–153

    Article  Google Scholar 

  • Hakverdi S, Culha G, Canda MS, Yaldiz M, Altintas S (2008) Problem of cystic Echinococcoss in Hatay. Türkiye Parazitol Derg 32:340–342

    PubMed  Google Scholar 

  • Hassan ZI, Meerkhan AA, Boufana B, Hama AA, Ahmed BD, Mohammed W, Mero S, Orsten S, Interisano M, Pozio E, 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 Trop 172:201–207

    Article  PubMed  Google Scholar 

  • Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JDF, Dinkel A, Sako Y, Mackenstedt U, Romig T, Ito A (2008) Genetic characterization and phylogenetic position of Echinococcus felidis Ortlepp, 1937 (Cestoda: Taeniidae) from the African lion. Int J Parasitol 39:861–868

    Article  Google Scholar 

  • Jordanova DP, Harizanov RN, Kaftandjiev IT, Rainova IG, Kantardjiev TV (2015) Cystic echinococcosis in Bulgaria 1996−2013, with emphasis on childhood infections. Eur J Clin Microbiol Infect Dis 34:1423–1428

    Article  CAS  PubMed  Google Scholar 

  • Kinkar L, Laurimae T, Simsek S, Balkaya I, Casulli A, Manfredi MA, Ponce-Gordo F, Varcasia A, Lavikainen A, González LM, Rehbein S, VAN DER Giessen J, Sprong H, Saarma U (2016) High-resolution phylogeography of zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1 with an emphasis on its distribution in Turkey, Italy and Spain. Parasitology 143:1790–1801

    Article  PubMed  Google 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, Saarma U (2017) New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto. Infect Genet Evol 52:52–58

    Article  CAS  PubMed  Google Scholar 

  • Kose M, Sevimli KF (2008) Prevalence of cystic echinococcosis in slaughtered cattle in Afyonkarahisar. Türkiye Parazitol Derg 32:27–30

    PubMed  Google Scholar 

  • Kuru BB, Aypak S, Aysul N (2013) Prevalence of Echinococcus granulosus determined with polymerase chain reaction in dogs in Aydın district. Türkiye Parazitol Derg 37:78–83

    Article  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaDP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Sako Y, Yokoyama N, Fukunaga M, Ito A (2000) Mitochondrial genetic code in cestodes. Mol Biochem Parasitol 111:415–424

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, McManus DP, Schantz PM, Craig PS, Ito A (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134:713–722

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Yanagida T, Okamoto M, Knapp J, Nkouawa A, Sako Y, Ito A (2010) State-of-the-art Echinococcus and Taenia: phylogenetic taxonomy of human-pathogenic tapeworms and its application to molecular diagnosis. Infect Genet Evol 10:444–452

    Article  CAS  PubMed  Google Scholar 

  • Öge H, Oge S, Gonenc B, Sarimehmetoglu O, Ozbakis G (2017) Coprodiagnosis of Echinococcus granulosus infection in dogs from Ankara, Turkey. Vet Parasitol 242:44–46

    Article  PubMed  Google Scholar 

  • Öter K, Bilgin Z, Tınar R, Tuzer E (2011) Tapeworm infections in stray dogs and cats in İstanbul, Turkey. Kafkas Univ Vet Fak Derg 17:595–599

    Google Scholar 

  • Ozekinci S, Bakir S, Mizrak B (2009) Evaluation of cystic echinococcosis cases given a histopathologic diagnosis from 2002 to 2007 in Diyarbakir. Türkiye Parazitol Derg 33:232–235

    PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Possenti A, Manzano-Román R, Sánchez-Ovejero C, Boufana B, La Torre G, Siles-Lucas M, Casulli A (2016) Potential risk factors associated with human cystic echinococcosis: systematic review and meta-analysis. PLoS Negl Trop Dis 10(11):e0005114

    Article  PubMed  PubMed Central  Google Scholar 

  • Rokni MB (2008) The present status of human helminthic diseases in Iran. Ann Trop Med Parasitol 102:283–295

    Article  CAS  PubMed  Google Scholar 

  • Romig T, Ebi D, Wassermann M (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol 213:76–84

    Article  CAS  PubMed  Google Scholar 

  • Salzburger W, Ewing GB, Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20:1952–1963

    Article  PubMed  Google Scholar 

  • Sariozkan S, Yalcin C (2009) Estimating the production losses due to cystic echinococcosis in ruminants in Turkey. Vet Parasitol 163:330–334

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Simsek S, Eroksuz Y (2009) Occurrence and molecular characterization of Echinococcus granulosus in Turkish mouflon (Ovis gmelinii anatolica). Acta Trop 109:167–169

    Article  CAS  PubMed  Google Scholar 

  • Simsek S, Balkaya I, Ciftci AT, Utuk AE (2011a) Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Vet Parasitol 178:367–369

    Article  PubMed  Google Scholar 

  • Simsek S, Kaplan M, Ozercan IF (2011b) A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitol Res 109:411–416

    Article  PubMed  Google Scholar 

  • Šnàbel 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

    Article  PubMed  Google Scholar 

  • Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsinomy (* and other methods). Version 4. Sinauer, Massachusetts

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tavakoli H, Bayat M, Kousha A (2008) Hydatidosis infection study in human and livestock populations during 2002-2007. Am-Eurasian J Agri Environ Sci 4:473–477

    Google Scholar 

  • Thompson RCA (2008) The taxonomy, phylogeny and transmission of Echinoccocus. Exp Parasitol 119:439–446

    Article  CAS  PubMed  Google Scholar 

  • Umur S (2003) Prevalence and economic importance of cystic echinococcosis in slaughtered ruminants in Burdur, Turkey. J Veterinary Med Ser B 50:247–252

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vural G, Baca AU, Gauci CG, Bagci O, Gicik Y, 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. Vet Parasitol 154:347–350

    Article  CAS  PubMed  Google Scholar 

  • 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, Artiş T (2008) Cystic echinococcosis in Turkey from 2001-2005. Türkiye Parazitol Derg 32:208–220

    PubMed  Google Scholar 

  • Yibar A, Selcuk O, Senlik B (2015) Major causes of organ/carcass condemnation and financial loss estimation in animals slaughtered at two abattoirs in Bursa Province, Turkey. Prev Vet Med 118:28–35

    Article  PubMed  Google Scholar 

  • Yildiz K, Gurcan S (2003) Prevalence of hydatidosis and fertility of hydatid cysts in sheep in Kırıkkale, Turkey. Acta Vet Hung 51(2):181–187

    Article  CAS  PubMed  Google Scholar 

  • Yildiz K, Tunçer C (2005) Prevalence of hydatid cysts in cattle in the province of Kırıkkale. Türkiye Parazitol Derg 29:247–250

    PubMed  Google Scholar 

  • Yolasıgmaz A, Reiterova K, Turk M, Reyhan E, Bozdag AD, Karababa AO, Altintas N, Altintas N (2006) Comparison of serological and clinical findings in Turkish patients with cystic echinococcosis. Helminthologia 43:220–225

    Google Scholar 

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Funding

This study was supported by the European Community’s Seventh Framework Programme under the grant agreement 602051 (HERACLES Project; http://www.Heracles-fp7.eu/) and in part by the Overseas Research Fellowship Program (2214) of the Scientific and Technological Research Council of Turkey.

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Author notes

  1. Serra Orsten and Belgees Boufana have contributed equally to this work.

Authors and Affiliations

  1. School of Health Services, Hacettepe University, Ankara, Turkey

    Serra Orsten

  2. Department of Infectious Diseases, WHO Collaborating Centre for the Epidemiology, Detection and Control of CE and AE, European Union Reference Laboratory for Parasites, Istituto Superiore di Sanitá, Rome, Italy

    Belgees Boufana & Adriano Casulli

  3. Faculty of Medicine, Department of Radiology, Hacettepe University, Ankara, Turkey

    Turkmen Ciftci, Devrim Akinci & Okan Akhan

  4. Faculty of Medicine, Department of Biostatistics, Hacettepe University, Ankara, Turkey

    Ergun Karaagaoglu

  5. Faculty of Medicine, Department of Medical Microbiology, Hacettepe University, Ankara, Turkey

    Cumhur Ozkuyumcu

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  1. Serra Orsten
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  2. Belgees Boufana
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  3. Turkmen Ciftci
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Corresponding author

Correspondence to Belgees Boufana.

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The current study was approved by the Ethical Committee of the Faculty of Medicine, Hacettepe University, Ankara, Turkey (GO 14/293-37).

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The authors declare that they have no competing interests.

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Orsten, S., Boufana, B., Ciftci, T. et al. Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients. Parasitol Res 117, 1257–1263 (2018). https://doi.org/10.1007/s00436-018-5807-9

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