Abstract
In Romania, cystic echinococcosis is endemic and affects, besides humans, various animal species including sheep, cattle, and swine. As yet, no molecular-genetic typing has been carried out to clearly identify the putative strains being transmitted there. Parasite samples (protoscoleces or germinal layers) were collected from infected intermediate hosts and subsequently analyzed by comparing the PCR-amplified DNA sequences of three targets: one nuclear (BG1/3) and two mitochondrial (cox1 and nadI). Three strains were identified with the mitochondrial sequences: (i) the common sheep strain (G1) which circulates between sheep and cattle and is infective for humans, (ii) the Tasmanian sheep strain (G2) infecting sheep and cattle, and (iii) the pig strain (G7) predominantly found in swine. To our knowledge, this is the first report which demonstrates the occurrence of the Tasmanian sheep strain in cattle and the sympatric occurrence of these three strains (G1, G2, and G7) in Europe.
Similar content being viewed by others
References
Arnaud-Haond S, Bonhomme F, Blanc F (2003) Large discrepancies in differentiation of allozymes, nuclear and mitochondrial DNA loci in recently founded Pacific populations of the pearl oyster Pinctada margaritifera. J Evol Biol 16:388–398
Bardonnet K, Benchikh-Elfegoun MC, Bart JM, Harraga S, Hannache N, Haddad S, Dumon H, Vuitton DA, Piarroux R (2003) Cystic echinococcosis in Algeria: cattle act as reservoirs of a sheep strain and may contribute to human contamination. Vet Parasitol 116:35–44
Bart JM, Bardonnet K, Elfegoun MC, Dumon H, Dia L, Vuitton DA, Piarroux R (2004) Echinococcus granulosus strain typing in North Africa: comparison of eight nuclear and mitochondrial DNA fragments. Parasitology 128:229–234
Boissinot S, Boursot P (1997) Discordant phylogeographic patterns between the Y chromosome and mitochondrial DNA in the house mouse: selection on the Y chromosome? Genetics 146:1019–1034
Bowles J, McManus DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol 23:969–972
Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54:165–173
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 93:127–130
Draganescu C (1997) Romanian sheep production spectacular past decline, uncertain future. In: Sheep and goat husbandry in the Central and Eastern European Countries, Budapest, Hungary
Eckert J, Thompson RC (1997) Intraspecific variation of Echinococcus granulosus and related species with emphasis on their infectivity to humans. Acta Trop 64:19–34
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Gottstein B, Mowatt MR (1991) Sequencing and characterization of an Echinococcus multilocularis DNA probe and its use in the polymerase chain reaction. Mol Biochem Parasitol 44:183–193
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
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98
Hobbs RP, Lymbery AJ, Thompson RC (1990) Rostellar hook morphology of Echinococcus granulosus (Batsch, 1786) from natural and experimental Australian hosts, and its implications for strain recognition. Parasitology 101(Pt 2):273–281
Iacobiciu I, Stefanoiu V, Lazar Z, Olariu R, Negrutiu L, Nitu A, Birsan M, Radus S, Dan L (1996) Aspects of hydatidosis in the adult population in Banat. Roum Arch Microbiol Immunol 55:263–274
Iacobiciu I, Siko-Barabasi S, Olariu R, Stefanoiu V, Darabus G, Tirnea L (2003) Investigations on spread of hydatidosis in humans in Caras-Severin county. J Rom Parasitol 13:27–30
Junie M, Coroiu Z, Costache C (2000) Epidemiological aspects on hydatidosis in Cluj-Napoca. J Rom Parasitol 10:8–11
Kamenetzky L, Canova S, Guarnera E, Rosenzvit M (2000) Echinococcus granulosus: DNA extraction from germinal layers allows strain determination in fertile and nonfertile hydatid cysts. Exp Parasitol 95:122–127
Kamenetzky L, Gutierrez AM, Canova SG, Haag KL, Guarnera EA, Parra A, Garcia GE, Rosenzvit MC (2002) Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infect Genet Evol 2:129–136
Kedra AH, Swiderski Z, Tkach V, Dubinski P, Pawlowski Z, Stephaniak 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
Kedra 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
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 124:97–112
Lemaire C, Versini JJ, Bonhomme F (2005) Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. J Evol Biol 18:70–80
Malczewski A (2002) CE and AE in Eastern Europe. In: Craig P, Pawlowski Z (eds) Cestode zoonoses: echinococcosis and cysticercosis, an emergent and global problem. IOS, Amsterdam, The Netherlands, pp 81–89
McManus DP, Thompson RC (2003) Molecular epidemiology of cystic echinococcosis. Parasitology 127(Suppl):S37–S51
Morariu S (2000) Morphological characteristics of adult Echinococcus granulosus of cattle origin. In: I Congresso Iberico de Hidatidologia, VII Congresso Nacional de Hidatidologia, Beja, Portugal
Morariu S (2004) Etiologic and epidemiologic study and parasitic control. PhD Thesis Faculty of Veterinary Medicine, Timisoara, Romania
Morariu S, Cosoroaba I, Darabus G, Oprescu I, Radbea N (1999) Morphological characteristics of adult Echinococcus granulosus of pig and sheep origin from western Romania. Arch Int Hidatid 33:324
Olsen GJ, Matsuda H, Hagstrom R, Overbeek R (1994) fastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci 10:41–48
Olteanu C, Panaitescu D, Ghernian I (1997) Echinococcosis/hydatidosis (E/H) in man and animals in Romania. Arch Int Hidatid 32:292–293
Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Pawlowski Z, Stefaniak J (2003) The pig strain of Echinococcus granulosus in humans: a neglected issue? Trends Parasitol 19:439
Rosenzvit MC, Zhang LH, Kamenetzky L, Canova SG, Guarnera EA, McManus DP (1999) Genetic variation and epidemiology of Echinococcus granulosus in Argentina. Parasitology 118:523–530
Scott JC, Stefaniak J, Pawlowski ZS, McManus DP (1997) Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114(Pt 1):37–43
Shaikenov BS, Torgerson PR, Usenbayev AE, Baitursynov KK, Rysmukhambetova AT, Abdybekova AM, Karamendin KO (2003) The changing epidemiology of echinococcosis in Kazakhstan due to transformation of farming practices. Acta Trop 85:287–293
Shaw KL (2002) Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sci USA 99:16122–16127
Snabel V, D'Amelio S, Mathiopoulos K, Turcekova L, Dubinsky P (2000) Molecular evidence for the presence of a G7 genotype of Echinococcus granulosus in Slovakia. J Helminthol 74:177–181
Todorov T, Boeva V (1999) Human echinococcosis in Bulgaria: a comparative epidemiological analysis. Bull WHO 77:110–118
Torgerson PR, Budke CM (2003) Echinococcosis—an international public health challenge. Res Vet Sci 74:191–202
Torgerson PR, Burtisurnov KK, Shaikenov BS, Rysmukhambetova AT, Abdybekova AM, Ussenbayev AE (2003) Modelling the transmission dynamics of Echinococcus granulosus in sheep and cattle in Kazakhstan. Vet Parasitol 114:143–153
Torgerson PR, Shaikenov BS, Baitursinov KK, Abdybekova AM (2002) The emerging epidemic of echinococcosis in Kazakhstan. Trans R Soc Trop Med Hyg 96:124–128
Turcekova L, Snabel V, D'Amelio S, Busi M, Dubinsky P (2003) Morphological and genetic characterization of Echinococcus granulosus in the Slovak Republic. Acta Trop 85:223–229
Acknowledgement
We are extremely grateful to Dr. Petre Brăilă from Reşiţa, Dr. Gheorghe Ciobanu from Arad, Dr. Petru Muntean from Timişoara, and Dr. Eugen Avram from Satu-Mare for assistance and for supplying the material for our study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bart, J.M., Morariu, S., Knapp, J. et al. Genetic typing of Echinococcus granulosus in Romania. Parasitol Res 98, 130–137 (2006). https://doi.org/10.1007/s00436-005-0015-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-005-0015-9