Abstract
Introduction
Cystic echinococcosis is a globally distributed zoonotic disease of great medical and veterinary importance, which is caused by the cestode Echinococcus granulosus sensu lato. In Ukraine, two areas of the prominent circulation of the parasite are established, the southern steppe zone with sheep as the main transmitter, and the northern forest-steppe zone and Polissia, where pigs are mainly responsible for maintaining the E. granulosus transmission.
Methods
Given that only a few studies have so far addressed the genetic diversity of the parasite in Ukraine, we have sequenced partial mitochondrial genes of cytochrome c oxidase 1 (789 bp), NADH dehydrogenase 1 (602 bp) and 12S rRNA (333–334 bp) in pig metacestodes from the Sumy region (farms close to Sumy, northeastern Ukraine) and the Kyiv region (a farm in Bila Tserkva, central Ukraine).
Results
Four isolates from four pigs in the Sumy region were identified as E. canadensis (G7 genotype), the major E. granulosus s.l. species circulating in Eastern Europe, including the three microvariants (G7A, G7B, G7C). Three isolates from the two pigs in the Kyiv region were classified as E. granulosus s.s. (G1 genotype), including one microvariant (G1A).
Conclusion
To our knowledge, this is the first genetic record of E. granulosus s.s. with the presumed highest infectivity and virulence among the E. granulosus s.l. species in Ukraine. The finding has implications for public health as local control programmes should take into consideration different development rate of this parasite in dogs and the greater risk of the species for human infection.
Similar content being viewed by others
References
Batsch AJGK (1786) Naturgeschichte der bandwurmgattung überhaupt und ihrer arten insbesondere, nach den neuern beobachtungen in einem systematischen auszuge. JJ Gebauer, Halle
FAO/WHO (2014) Multicriteria-based ranking for risk management of food-borne parasites. Microbiological risk assessment series no 23, Rome. p. 302
Torgerson PR, Macpherson CN (2011) The socioeconomic burden of parasitic zoonoses: global trends. Vet Parasitol 182:79–95. https://doi.org/10.1016/j.vetpar.2011.07.017
Budke CM, Deplazes P, Torgerson PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12:296–303. https://doi.org/10.3201/eid1202.050499
Kia EB, Ouma FF, Mulambalah CS, Okoth PK (2019) The burden of cystic echinococcosis in Kenya: a review article. Iran J Parasitol 14:502–509
Webster GA, Cameron TWM (1961) Observations on experimental infections with Echinococcus in rodents. Can J Zool 39:877–889
Lopez-Neyra CR, Soler Planas MA (1943) Revision del genero Echinococcus Rud y description de una especie nuéva Parasita intestinal del porro en Almeria. Rev Iber Parasitol 3:169–194
Ortlepp JR (1937) South African Helminths - Part I. Onderstepoort J Vet Sci Anim Ind 9:311–336
Williams RJ, Sweatmen 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
Romig T, Ebi D, Wassermann M (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol 213:76–84. https://doi.org/10.1016/j.vetpar.2015.07.035
Vuitton DA, McManus DP, Rogan MT, Romig T, Gottstein B, Naidich A, Tuxun T, Wen H, Menezes da Silva A, World Association of Echinococcosis (2020) International consensus on terminology to be used in the field of echinococcoses. Parasite 27:41. https://doi.org/10.1051/parasite/2020024
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
Romig T, Dinkel A, Mackenstedt U (2006) The present situation of echinococcosis in Europe. Parasitol Int 55(Suppl):S187-191. https://doi.org/10.1016/j.parint.2005.11.028
Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, Wassermann M, Takahashi K, de la Rue M (2017) Ecology and life cycle patterns of Echinococcus species. In: Thompson RCA, Deplazes P, Lymbery AJ (eds) Echinococcus and echinococcosis, part A, vol 95. Academic Press, London, pp 213–314. https://doi.org/10.1016/bs.apar.2016.11.002
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
Mogoye BK, Menezes CN, Wong ML, Stacey S, von Delft D, Wahlers K, Wassermann M, Romig T, Kern P, Grobusch MP, Frean J (2013) First insights into species and genotypes of Echinococcus in South Africa. Vet Parasitol 196(3–4):427–432. https://doi.org/10.1016/j.vetpar.2013.03.033
Kędra AH, Świderski Z, Tkach VV, Dubinský P, Pawłowski Z, Stefaniak J, Pawlowski J (1999) Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia and Ukraine. A multicenter study. Acta Parasitol 44:248–254
Dybicz M, Gierczak A, Dąbrowska J, Rdzanek Ł, Michałowicz B (2013) Molecular diagnosis of cystic echinococcosis in humans from central Poland. Parasitol Int 62:364–367. https://doi.org/10.1016/j.parint.2013.03.005
Šnábel V, D’Amelio S, Mathiopoulos K, Turčeková Ľ, Dubinský P (2000) Molecular evidence of the presence of a G7 genotype in Slovakia. J Helminthol 74:177–181
Bružinskaite R, Šarkūnas M, Torgerson PR, Mathis A, Deplazes P (2009) Echinococcosis in pigs and intestinal infection with Echinococcus spp. in dogs in southwestern Lithuania. Vet Parasitol 160:237–241. https://doi.org/10.1016/j.vetpar.2008.11.011
Kędra AH, Tkach VV, Swiderski ZP, Pawlowski Z, Emets A, Pawlowski J (2000) Molecular characterisation of Echinococcus granulosus from a wild boar. Acta Parasitol 45:121–122
Šnábel V, Kuzmina T, Cavallero S, D’Amelio S, Georgescu SO, Szénási Z, Cielecka D, Sałamatin R, Yemets A, Kucsera I (2016) A molecular survey of Echinococcus granulosus sensu lato in central-eastern Europe. Open Life Sci 11:524–532. https://doi.org/10.1515/biol-2016-0066
Artemenko LP, Bukalova NV, Nebeschuk AD (2013) Ekhinokokkoz. Vozbuditeli, osobennosti epizootologii [Echinococcosis. Pathogens, features of epizootology]. Modern Veterinary Medicine [Suchasna veterinarna meditsina] part 1:48–51 (in Russian, English Summary)
Litvinenko O, Pavlikovska T (2015) Ekhinokokoz u l'udej i tvaryn v Ukraini [Echinococcosis in human and animals in Ukraine]. Vet Biotechnol 26:102–110 (in Ukrainian, English summary)
Xiao N, Qiu J, Nakao M, Nakaya K, Yamasaki H, Sako Y, Mamuti W, Schantz PM, Craig PS, Ito A (2003) Short report: Identification of Echinococcus species from a yak in the Qinghai-Tibet plateau region of China. Am J Trop Med Hyg 69:445–446
Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JD, Dinkel A, Sako Y, Mackenstedt U, Romig T, Ito A (2008) Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. Int J Parasitol 38:861–868
Dinkel A, von Nickisch-Rosenegk M, Bilger B, Merli M, Lucius R, Romig T (1998) Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. J Clin Microbiol 36:1871–1876. https://doi.org/10.1128/JCM.36.7.1871-1876.1998
Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 9:678–687. https://doi.org/10.1093/oxfordjournals.molbev.a040752
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020
Yanagida T, Mohammadzadeh T, Kamhawi S, Nakao M, Sadjjadi SM, Hijjawi N, Abdel-Hafez SK, Sako Y, Okamoto M, Ito A (2012) Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitol Int 61:599–603. https://doi.org/10.1016/j.parint.2012.05.014
Laurimäe T, Kinkar L, Romig T et al (2018) The benefits of analysing complete mitochondrial genomes: deep insights into the phylogeny and population structure of Echinococcus granulosus sensu lato genotypes G6 and G7. Infect Genet Evol 64:85–94. https://doi.org/10.1016/j.meegid.2018.06.016
Antolová D, Fecková M, Šnábel V, Rosoľanka R, Weissová T, Lukáč B, Nováková M (2019) Cystic echinococcosis in Slovakia—human cases and seroepidemiological study. In Annals of Parasitology: The XXV. Congress of the Polish Parasitological Society, 9–12 September, 2019, Warsaw. Abstracts, 2019, vol. 65: 53–54.
Konyaev SV, Yanagida T, Nakao M et al (2013) Genetic diversity of Echinococcus spp. in Russia. Parasitology 140:1637–1647. https://doi.org/10.1017/S0031182013001340
Sałamatin R, Kowal J, Nosal P, Kornaś S, Cielecka D, Jańczak D, Patkowski W, Gawor J, Kornyushin V, Golab E, Šnábel V (2017) Cystic echinococcosis in Poland: genetic variability and the first record of Echinococcus granulosus sensu stricto (G1 genotype) in the country. Parasitol Res 116:3077–3085. https://doi.org/10.1007/s00436-017-5618-4
Laurimaa L, Davison J, Süld K, Plumer L, Oja R, Moks E, Keis M, Hindrikson M, Kinkar L, Laurimäe T, Abner J, Remm J, Anijalg P, Saarma U (2015) First report of highly pathogenic Echinococcus granulosus genotype G1 in dogs in a European urban environment. Parasit Vectors 8:182. https://doi.org/10.1186/s13071-015-0796-3
Konyaev SV, Yanagida T, Ivanov MV, Ruppel VV, Sako Y, Nakao M, Ito A (2012) The first report on cystic echinococcosis in a cat caused by Echinococcus granulosus sensu stricto (G1). J Helminthol 86:391–394. https://doi.org/10.1017/S0022149X1100054X
Artemenko Yu G (1987) The peculiarities in the biology of the echinococcosis agent. Vestnik Selʹskohozâjstvennoj Nauki 5:123–126 (in Russian, English sumamry)
Shablovskaya EA, Bulgakov VA, Ponomareva VE, Dan'ko OP, Voloshchuk SD, Kikoť VI (1989) Echinococcosis in the Ukrainian SSR [Ekhinokokkoz v Ukrainskoj SSR]. Med Parazitol Parazitarn Bol 6:49–51 (in Russian, English summary)
Yastreb VB (2009) Geľmintozoonozy: echinokokkoz i dirofilarioz (biomorfologičeskie osobennosti vozbuditelej, soveršenstvovanie mer borby). [Helminth Zoonoses: Echinococcosis and Dirofilariosis (biomorphological characteristics of pathogens, improvement of control measures)]. Summary of the PhD thesis, The Moscow State Academy of Veterinary Medicine and Biotechnology named after K.I.Skryabin, Moscow (in Russian)
Torgerson PR, Budke CM (2003) Echinococcosis—an international public health challenge. Res Vet Sci 74:191–202. https://doi.org/10.1016/s0034-5288(03)00006-7
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:e0005114. https://doi.org/10.1371/journal.pntd.0005114
Deplazes P, Rinaldi L, Alvarez Rojas CA et al (2017) Global distribution of alveolar and cystic echinococcosis. Adv Parasitol 95:315–493. https://doi.org/10.1016/bs.apar.2016.11.001
Berger S (2020) Echinococcosis: Global Status. GIDEON Informatics Inc, p. 161.
Malczewski A (2002) CE and AE in Eastern Europe. Cestode zoonoses: echinococcosis and cysticercosis: an emergent and global problem. IOS, Amsterdam, pp 81–89
Artemenko LP, Nebeschuk OD, Litvinenko OP (2009) Suchasniy stan problemi gelmintozu-zoonozu ekhinokokozu [the current state of the helminthiasis issue—zoonosis of echinococcosis]. Bila Tserkva, pp. 12–13 (in Ukrainian)
Litvinenko OP (2015a) Ekhinokokoz dribnoi rogatoi khudoby [Echinococcosis in small ruminants]. Tvarynnytsvo Ukrainy 7:30–32 (in Ukrainian, English summary)
Kamenetzky L, Gutierrez AM, Canova SG, Haag KL, Guarnera EA, Parra A, García GE, Rosenzvit MC (2002) Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infect Genet Evol 2:129–136. https://doi.org/10.1016/s1567-1348(02)00131-4
Varcasia A, Canu S, Lightowlers MW, Scala A, Garippa G (2006) Molecular characterization of Echinococcus granulosus strains in Sardinia. Parasitol Res 98:273–277. https://doi.org/10.1007/s00436-005-0059-x
Litvinenko O (2015b) Dynamika epizootychnogo protsesu z ekhinokokozu velykoi rogatoi khudoby [The dynamics of epizootic process on echinococcosis in cattle]. Problemy zooinzhenerii ta veterynarnoi medytsyny 30:219–222 (in Ukrainian, English summary)
Thompson RC, 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
Rinaldi L, Maurelli MP, Veneziano V, Capuano F, Perugini AG, Cringoli S (2008) The role of cattle in the epidemiology of Echinococcus granulosus in an endemic area of southern Italy. Parasitol Res 103:175–179. https://doi.org/10.1007/s00436-008-0948-x
Mitrea IL, Ionita M, Costin II, Predoi G, Avram E, Rinaldi L, Maurelli MP, Cringoli G, Genchi C (2014) Occurrence and genetic characterization of Echinococcus granulosus in naturally infected adult sheep and cattle in Romania. Vet Parasitol 206(3–4):159–166. https://doi.org/10.1016/j.vetpar.2014.10.028
Litvinenko O (2015c) Dynamika poshyrennia ekhinokokoznoi invazii sered svynej v Ukraini [Dynamics of the spread of Echinococcus infections in pig in Ukraine]. Vet Medicina 101:179–181 (in Ukrainian, English summary)
Litvinenko O (2013) Epizootychna sytuatsija z ekhinokokozy svynej na terytorii Ukrainy [Epizootological situation of echinococcosis in pigs in the territory of Ukraine]. Sci J NUBiP Ukr 188 3:208–212 (in Ukrainian, English summary)
Morozov BS (2019) Epizootychna sytuatsija schodo ekhinokokozy v Sumskij oblasti [Epizootic situation as to echinococcosis in Sumy region]. Animal Biol (Biologija tvaryn) 21:35–39 (in Ukrainian, English summary)
Haag KL, Ayala FJ, Kamenetzky L, Gutierrez AM, Rosenzvit M (2004) Livestock trade history, geography, and parasite strains: the mitochondrial genetic structure of Echinococcus granulosus in Argentina. J Parasitol 90:234–239. https://doi.org/10.1645/GE-173R
Šnábel V, Ševcová D, Cavallero S, D´Amelio S, Calma C, Miterpáková M (2011) Genetic variability of Echinococcus granulosus tapeworms in central/eastern Europe. In Proceedings from the IV. International scientific conference "infectious and parasitic diseases of animals", University of Veterinary Medicine and Pharmacy in Košice, Slovakia, pp. 280–281. ISBN 978-80-8077-230-7
Addy F, Wassermann M, Kagendo D et al (2017) Genetic differentiation of the G6/7 cluster of Echinococcus canadensis based on mitochondrial marker genes. Int J Parasitol 47:923–931. https://doi.org/10.1016/j.ijpara.2017.06.003
Gaidutsky PI, Sabluk PT, Lupenko Yu O (2005) Agrarian Reform in Ukraine. NNC IAE, p. 424.
Ibatullin M (2016) Historical aspects of production of swine breeding of Ukraine in the Soviet period. UDC 631.173:658.589 (477)
Casulli A, Interisano M, Sréter T, Chitimia L, Kirkova Z, La Rosa G, Pozio E (2012) Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infect Genet Evol 12:377–383. https://doi.org/10.1016/j.meegid.2011.12.014
Umhang G, Richomme C, Boucher JM, Hormaz V, Boue F (2013) Prevalence survey and first molecular characterization of Echinococcus granulosus in France. Parasitol Res 112:1809–1812. https://doi.org/10.1007/s00436-012-3245-7
Umhang G, Chihai O, Boue F (2014) 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
Hidalgo C, Stoore C, Pereira I, Paredes R, Alvarez Rojas CA (2020) Multiple haplotypes of Echinococcus Granulosus Sensu Stricto in single naturally infected intermediate hosts. Parasitol Res 119:763–770. https://doi.org/10.1007/s00436-019-06578-2
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 90:279–283. https://doi.org/10.1017/S0022149X15000103
Counotte MJ, Minbaeva G, Usubalieva J, Abdykerimov K, Torgerson PR (2016) The burden of zoonoses in Kyrgyzstan: a systematic review. PLoS Negl Trop Dis 10:e0004831. https://doi.org/10.1371/journal.pntd.0004831
Khimich MS, Piven OT, Gorobey OM, Salata VZ, Freiuk DV, Naidich OV (2019) The analysis of the dynamics of detection animal’s invasive diseases during veterinary expertise. SMLNUVMB. https://doi.org/10.32718/nvlvet9326 (UDC 619:614.31:616-02/-033.1:637.513)
Paternoster G, Boo G, Wang C et al (2020) Epidemic cystic and alveolar echinococcosis in Kyrgyzstan: an analysis of national surveillance data. Lancet Glob Health 8:e603–e611. https://doi.org/10.1016/S2214-109X(20)30038-3
Muminov AM, Mahmadov FI, Shodmonov IS (2004) Echinococcosis of people and animals of Tadjikistan. In: Torgerson P, Shaikenov B (eds) Echinococcosis in central Asia: problems and solutions. Dauir Publishing House, Almaty, pp 20–24
Funding
The study was supported by the Scientific Grant Agency VEGA (project No. 2/0107/20).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The authors claim that all parasitological and genetic procedures contributing to this work are in accordance with the ethical standards of the relevant national and institutional guides. Samples were taken from slaughterhouses in Sumy and Bila Tserkva cities in Ukraine after the pigs were humanely slaughtered for meat according to the Law of Ukraine "on Veterinary Medicine" no. 3318 (as amended with changes from February 4, 2021).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Šnábel, V., Kuzmina, T.A., Antipov, A.A. et al. Molecular Study of Echinococcus granulosus Cestodes in Ukraine and the First Genetic Identification of Echinococcus granulosus Sensu Stricto (G1 Genotype) in the Country. Acta Parasit. 67, 244–254 (2022). https://doi.org/10.1007/s11686-021-00450-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11686-021-00450-z