Abstract
Cystic echinococcosis is a zoonosis caused by the tapeworm Echinococcus granulosus sensu lato. The lifecycle of the parasite is mainly domestic, requiring dogs as definitive hosts and livestock species as intermediate hosts. Although human cystic echinococcosis is a high public health priority in the Republic of Moldova, the rare animal data available concerns only infection in cattle. A preliminary slaughterhouse survey was conducted to assess prevalence and perform the first molecular characterization of E. granulosus sensu lato in sheep and cattle. For the survey, 40 sheep and 19 cattle were inspected. Very high prevalence in sheep (82.5 %) and in cattle (78.9 %) was found. Molecular analyses identified genotypes G1 and G3 of E. granulosus sensu stricto in all the liver and lung samples. Based on the concatenated sequences of cox1 + nad3 (701 bp), 23 different haplotypes were obtained. Mixed infections by different haplotypes/genotypes were frequently identified in both sheep and cattle. The relatively high (20.0 %) cyst fertility observed in cattle argues for the potential contribution of cattle to the lifecycle of E. granulosus sensu stricto, unlike previous observations in Europe. The hyperendemic situation of Moldova can be explained by a high majority of animals slaughtered at home usually without veterinary inspection. Further extensive slaughterhouse surveys with molecular identification also involving pigs and goats are needed to obtain a better overview of the epidemiological situation of E. granulosus sensu lato in this hyperendemic focus in the Republic of Moldova.
Similar content being viewed by others
References
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
Bart JM et al (2006) Genetic typing of Echinococcus granulosus in Romania. Parasitol Res 98(2):130–137. doi:10.1007/s00436-005-0015-9
Bowles J, McManus DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol 23(7):969–972
Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54(2):165–173
Breyer I, Georgieva D, Kurdova R, Gottstein B (2004) Echinococcus granulosus strain typing in Bulgaria: the G1 genotype is predominant in intermediate and definitive wild hosts. Parasitol Res 93(2):127–130. doi:10.1007/s00436-004-1116-6
Brunetti E, Kern P, Vuitton DA (2010) Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114(1):1–16. doi:10.1016/j.actatropica.2009.11.001
Budke CM, Deplazes P, Torgerson PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12(2):296–303
Cardona GA, Carmena D (2013) A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet Parasitol 192(1–3):10–32. doi:10.1016/j.vetpar.2012.09.027
Casulli A et al (2012) Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infect Genet Evol 12(2):377–383
Chihai O (2006) Cattle polyparasitism in different regions of the republic of Moldova. Bul USAMV 63:217–221
Chihai O et al (2012) Diversity of parasitism in bovines in the Republic of Moldova. Bul USAMV 69(1–2):1–4
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1659
Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (2001) WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. O.I.E., Paris, 265 pp
Erhan D, Luncasu M, Grati N (2001) Rolul factorilor antropogeni şi naturali la infestarea animalelor sălbatice cu endo- şi ectoparaziţi in Republica Moldova. Paper presented at the Materialele Conferinţei IV a Zoologilor din RM, Chişinău
Konyaev SV et al (2013) Genetic diversity of Echinococcus spp. in Russia. Parasitology 140(13):1637–1647. doi:10.1017/S0031182013001340
Lavikainen A, Lehtinen MJ, Laaksonen S, Agren E, Oksanen A, Meri S (2006) Molecular characterization of Echinococcus isolates of cervid origin from Finland and Sweden. Parasitology 133(Pt 5):565–570. doi:10.1017/S0031182006000667
Le TH, Pearson MS, Blair D, Dai N, Zhang LH, McManus DP (2002) Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124(1):97–112
Lungu V (2012) Epidemiology of human echinococcosis in the Republic of Moldova. Sci Parasitol 13(2):87–91
McManus DP (2013) Current status of the genetics and molecular taxonomy of Echinococcus species. Parasitology 140(13):1617–1623. doi:10.1017/S0031182013000802
Mitrea IL, Ionita M, Wassermann M, Solcan G, Romig T (2012) Cystic echinococcosis in Romania: an epidemiological survey of livestock demonstrates the persistence of hyperendemicity. Foodborne Pathog Dis 9(11):980–985. doi:10.1089/fpd.2012.1237
Moro P, Schantz PM (2006) Cystic echinococcosis in the Americas. Parasitol Int 55(SUPPL.):S181–S186
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(Pt 5):713–722. doi:10.1017/S0031182006001934
Nakao M et al (2010) State-of-the-art Echinococcus and Taenia: phylogenetic taxonomy of human-pathogenic tapeworms and its application to molecular diagnosis. Infect Genet Evol 10(4):444–452. doi: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(12–13):1017–1029. doi:10.1016/j.ijpara.2013.06.002
Okamoto M, Bessho Y, Kamiya M, Kurosawa T, Horii T (1995) Phylogenetic relationships within Taenia taeniaeformis variants and other taeniid cestodes inferred from the nucleotide sequence of the cytochrome c oxidase subunit I gene. Parasitol Res 81(6):451–458
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(1):175–179. doi:10.1007/s00436-008-0948-x
Snabel V et al (2009) Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitol Res:sous presse
Thompson RC (2008) The taxonomy, phylogeny and transmission of Echinococcus. Exp Parasitol 119(4):439–446. doi:10.1016/j.exppara.2008.04.016
Torgerson PR (2003) Economic effects of echinococcosis. Acta Trop 85(2):113–118
Umhang G, Richomme C, Boucher JM, Hormaz V, Boué F (2013) Prevalence survey and first molecular characterization of Echinococcus granulosus in France. Parasitol Res 112(4):1809–1812
Valieva Z, Sarsembaeva N, Valdovska A, Ussenbayev AE (2014) Impact of echinococcosis on quality of sheep meat in the south eastern Kazakhstan. Asian Australas J Anim Sci 27(3):391–397
Varcasia A, Canu S, Lightowlers MW, Scala A, Garippa G (2006) Molecular characterization of Echinococcus granulosus strains in Sardinia. Parasitol Res 98(3):273–277. doi:10.1007/s00436-005-0059-x
Yanagida T et al (2012) Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitol Int 61(4):599–603. doi:10.1016/j.parint.2012.05.014
Yu SH et al (2008) Cystic and alveolar echinococcosis: an epidemiological survey in a Tibetan population in southeast Qinghai, China. Jpn J Infect Dis 61(3):242–246
Acknowledgments
The authors wish to thank the veterinary authorities and slaughterhouse staff in the Republic of Moldova for sample collections, C. Richomme (Anses, France) for performing statistical analyses and V. Hormaz, C. Peytavin de Garam, and J-M. Boucher (Anses, France) for their skilled technical assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Umhang, G., Chihai, O. & Boué, F. Molecular characterization of Echinococcus granulosus in a hyperendemic European focus, the Republic of Moldova. Parasitol Res 113, 4371–4376 (2014). https://doi.org/10.1007/s00436-014-4112-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-014-4112-5