Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-24T13:11:00.964Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular epidemiology of cystic echinococcosis

Published online by Cambridge University Press:  04 March 2004

D. P. McMANUS  and
R. C. A. THOMPSON
D. P. McMANUS
Affiliation:
Molecular Parasitology Laboratory, Division of Infectious Diseases and Immunology, Australian Centre for International and Tropical Health and Nutrition, The Queensland Institute of Medical Research and The University of Queensland, Post Office Royal Brisbane Hospital, Queensland 4029, Australia
R. C. A. THOMPSON
Affiliation:
World Health Organization Collaborating Centre for the Molecular Epidemiology of Parasitic Infections, Division of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia 6150, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

Echinococcus granulosus exhibits substantial genetic diversity that has important implications for the design and development of vaccines, diagnostic reagents and drugs effective against this parasite. DNA approaches that have been used for accurate identification of these genetic variants are presented here as is a description of their application in molecular epidemiological surveys of cystic echinococcosis in different geographical settings and host assemblages. The recent publication of the complete sequences of the mitochondrial (mt) genomes of the horse and sheep strains of E. granulosus and of E. multilocularis, and the availability of mt DNA sequences for a number of other E. granulosus genotypes, has provided additional genetic information that can be used for more in depth strain characterization and taxonomic studies of these parasites. This very rich sequence information has provided a solid molecular basis, along with a range of different biological, epidemiological, biochemical and other molecular-genetic criteria, for revising the taxonomy of the genus Echinococcus. This has been a controversial issue for some time. Furthermore, the accumulating genetic data may allow insight to several other unresolved questions such as confirming the occurrence and precise nature of the E. granulosus G9 genotype and its reservoir in Poland, whether it is present elsewhere, why the camel strain (G6 genotype) appears to affect humans in certain geographical areas but not others, more precise delineation of the host and geographic ranges of the genotypes characterised to date, and whether additional genotypes of E. granulosus remain to be identified.

Keywords

EchinococcusEchinococcus granulosusEchinococcus multilocularisechinococcosisstrain variationgenotypehorse-dog strainsheep-dog strainmitochondrial DNAcox1 genenad1 genetaxonomy
Type
Research Article
Information
Parasitology , Volume 127 , Issue S1 , October 2003 , pp. S37 - S51
Copyright
© 2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

BARDONNET, K., PIARROUX, R., DIA, L., SCHNEEGANS, F., BEURDELEY, A., GODOT, V. & VUITTON, D. A. (2002). Combined eco-epidemiological and molecular biology approaches to assess Echinococcus granulosus transmission to humans in Mauritania: occurrence of the ‘camel’ strain and human cystic echinococcosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 383–386.CrossRefGoogle Scholar
BARKER, G. C. (2002). Microsatellite DNA: a tool for population genetic analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene 96 (Suppl.), S21–S24.CrossRefGoogle Scholar
BINZ, T., REUSCH, T. B., WEDEKIND, C., SCHARER, L., STERNBERG, J. M. & MILINSKI, M. (2000). Isolation and characterization of microsatellite loci from the tapeworm Schistocephalus solidus. Molecular Ecology 9, 1926–1927.CrossRefGoogle Scholar
BOWLES, J., BLAIR, D. & McMANUS, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–174.CrossRefGoogle Scholar
BOWLES, J., BLAIR, D. & McMANUS, D. P. (1994). Molecular genetic characterisation of the cervid strain (“northern form”) of Echinococcus granulosus. Parasitology 109, 215–221.CrossRefGoogle Scholar
BOWLES, J., BLAIR, D. & McMANUS, D. P. (1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317–328.CrossRefGoogle Scholar
BOWLES, J. & McMANUS, D. P. (1993 a). NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. International Journal for Parasitology 23, 969–972.Google Scholar
BOWLES, J. & McMANUS, D. P. (1993 b). Rapid discrimination of Echinococcus species and strains using a PCR-based RFLP method. Molecular and Biochemical Parasitology 57, 231–240.Google Scholar
BOWLES, J. & McMANUS, D. P. (1993 c). Molecular variation in Echinococcus and the implications. Acta Tropica 53, 291–305.Google Scholar
BOWLES, J., VAN KNAPEN, F. & McMANUS, D. P. (1992). Genetic evidence that a cattle strain of the hydatid parasite, Echinococcus granulosus, is infective to man. Lancet 339, 1358.Google Scholar
BRETAGNE, S., ASSOULINE, B., VIDAUD, D., HOUIN, R. & VIDAUD, M. (1996). Echinococcus multilocularis: microsatellite polymorphism in U1 snRNA genes. Experimental Parasitology 82, 324–328.CrossRefGoogle Scholar
CABRERA, M., CANOVA, S., ROSENZVIT, M. & GUARNERA, E. (2002). Identification of Echinococcus granulosus eggs. Diagnostic Microbiology and Infectious Disease 44, 29–34.CrossRefGoogle Scholar
CASTRODALE, L. J., BELLER, M., WILSON, J. F., SCHANTZ, P. M., McMANUS, D. P., ZHANG, L. H., FALLICO, F. G. & SACCO, F. D. (2002). Two atypical cases of cystic echinococcosis (Echinococcus granulosus) in Alaska, 1999. American Journal of Tropical Medicine and Hygiene 66, 325–327.CrossRefGoogle Scholar
CURTIS, J. & MINCHELLA, D. J. (2000). Schistosome population genetic structure: when clumping worms is not just splitting hairs. Parasitology Today 16, 68–71.CrossRefGoogle Scholar
CURTIS, J., SORENSEN, R. E. & MINCHELLA, D. J. (2002). Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology 125, S51–S59.CrossRefGoogle Scholar
ECKERT, J., THOMPSON, R. C. A., LYMBERY, A. J., PAWLOWSKI, Z. S., GOTTSTEIN, B. & MORGAN, U. M. (1993). Further evidence for the occurrence of a distinct strain of Echinococcus granulosus in European pigs. Parasitology Research 79, 42–48.CrossRefGoogle Scholar
ECKERT, J., THOMPSON, R. C. A., MICHAEL, S. A., KUMARATILAKE, L. M. & EL-SAWAH, H. M. (1989). Echinococcus granulosus of camel origin: development in dogs and parasite morphology. Parasitology Research 75, 536–544.CrossRefGoogle Scholar
GASSER, R. B. (1997). Mutation scanning methods for the analysis of parasite genes. International Journal for Parasitology 27, 1449–1463.CrossRefGoogle Scholar
GASSER, R. B. & ZHU, X. (1999). Sequence-based analysis of enzymatically amplified DNA fragments by mutation detection techniques. Parasitology Today 15, 462–465.CrossRefGoogle Scholar
GASSER, R. B., ZHU, X. & McMANUS, D. P. (1998 a). Direct display of sequence variation in PCR-amplified mtDNA regions of Echinococcus by single-strand conformation polymorphism, and its implications. Acta Tropica 71, 107–115.Google Scholar
GASSER, R. B., ZHU, X. & McMANUS, D. P. (1998 b). Dideoxy fingerprinting (ddF): application to the genotyping of Echinococcus. International Journal for Parasitology 28, 1775–1779.Google Scholar
GONZALEZ, L. M., DANIEL-MWAMBETE, K., MONTERO, E., ROSENZVIT, M. C., McMANUS, D. P., GARATE, T. & CUESTA-BANDERA, C. (2002). Further molecular discrimination of Spanish strains of Echinococcus granulosus. Experimental Parasitology 102, 46–56.CrossRefGoogle Scholar
HAAG, K. L., ARAUJO, A. M., GOTTSTEIN, B., SILES-LUCAS, M., THOMPSON, R. C. & ZAHA, A. (1999). Breeding systems in Echinococcus granulosus (Cestoda; Taeniidae): selfing or outcrossing? Parasitology 118, 63–71.Google Scholar
HAAG, K. L., ZAHA, A., ARAUJO, A. M. & GOTTSTEIN, B. (1997). Reduced genetic variability within coding and non-coding regions of the Echinococcus multilocularis genome. Parasitology 115, 521–529.CrossRefGoogle Scholar
HARANDI, M. F., HOBBS, R. P., ADAMS, P. J., MOBEDI, I., MORGAN-RYAN, U. M. & THOMPSON, R. C. (2002). Molecular and morphological characterization of Echinococcus granulosus of human and animal origin in Iran. Parasitology 125, 367–373.Google Scholar
HOBBS, R. P., LYMBERY, A. J. & THOMPSON, R. C. A. (1990). Rostellar hook morphology of Echinococcus granulosus (Batsch, 1786) from natural and experimental Australian hosts and its implications for strain recognition. Parasitology 101, 273–281.CrossRefGoogle Scholar
HOPE, M., BOWLES, J. & McMANUS, D. P. (1991). A reconsideration of the Echinococcus granulosus strain situation in Australia following RFLP analysis of cystic material. International Journal for Parasitology 21, 471–475.CrossRefGoogle Scholar
HOPE, M., BOWLES, J., PROCIV, P. & McMANUS, D. P. (1992). A genetic comparison of human and wildlife Echinococcus granulosus in Queensland. Medical Journal of Australia 156, 27–30.Google Scholar
JOSHI, D. D., JOSHI, A. B. & JOSHI, H. (1997). Epidemiology of Echinococcosis in Nepal. South East Asian Journal of Tropical Medicine and Hygiene 28 (Suppl.), 26–31.Google Scholar
KAMHAWI, S. & HIJAWI, N. (1992). Current studies on the epidemiology of unilocular hydatidosis in Jordan and its social implications. Report on Parasitic Diseases of the Middle East. National Institutes of Health, Bethesda, Maryland, p. 8.
KEDRA, A. H., SWIDERSKI, Z., TKACH, V. V., DUBINSKY, P., PAWLOWSKI, Z., STEFANIAK, J. & PAWLOWSKI, J. (1999). Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia and Ukraine. A multicenter study. Acta Parasitologica 44, 248–254.Google Scholar
KEDRA, A. H., SWIDERSKI, Z., TKACH, V. V., ROCKI, B., PAWLOWSKI, J. & PAWLOWSKI, Z. (2000 a). Variability within NADH dehydrogenase sequences of Echinococcus multilocularis. Acta Parasitologica 45, 353–355.Google Scholar
KEDRA, A. H., TKACH, V. V., SWIDERSKI, Z., PAWLOWSKI, Z., EMETS, A. & PAWLOWSKI, J. (2000 b). Molecular characterisation of Echinococcus granulosus from wild boar. Acta Parasitologica 45, 121–122.Google Scholar
KUMARATILAKE, L. M., THOMPSON, R. C. A. & DUNSMORE, J. D. (1983). Comparative strobilar development of Echinococcus granulosus of sheep origin from different geographical areas of Australia in vivo and in vitro. International Journal for Parasitology 13, 151–156.CrossRefGoogle Scholar
LE, T. H., BLAIR, D. & McMANUS, D. P. (2002). Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206–213.CrossRefGoogle Scholar
LE, T. H., PEARSON, M. S., BLAIR, D., DAI, N., ZHANG, L. H. & McMANUS, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97–112.CrossRefGoogle Scholar
LOPEZ-NEYRA, C. R. & SOLER PLANAS, M. A. (1943). Revisión del género Echinococcus Rud. y descipcion de una specie nuéva parasita intestinal del perro en Almeria. Revisita Ibérica Parasitologia 3, 169–194.Google Scholar
MATHIS, A. & DEPLAZES, P. (2002). Role of PCR-DNA detection of Echinococcus multilocularis. In Cestode Zoonoses; Echinococcosis and Cysticercosis ( ed. Craig, P. & Pawlowski, Z.), pp. 195–204. Amsterdam, IOS Press.
McMANUS, D. P. (2002). The molecular epidemiology of Echinococcus granulosus and cystic hydatid disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 96 (Suppl. 1), S151–S157.CrossRefGoogle Scholar
McMANUS, D. P. & BOWLES, J. (1996). Molecular genetic approaches to parasite identification: their value in applied parasitology and systematics. International Journal for Parasitology 26, 687–704.CrossRefGoogle Scholar
McMANUS, D. P. & BRYANT, C. (1995). Biochemistry, physiology and molecular biology of Echinococcus. In Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A. & Lymbery, A. J. ), pp. 135–181. Wallingford, Oxon, UK, CAB International.
McMANUS, D. P., DING, Z. & BOWLES, J. (1994). A molecular genetic survey indicates the presence of a single, homogeneous strain of Echinococcus granulosus in north-western China. Acta Tropica 56, 7–14.CrossRefGoogle Scholar
McMANUS, D. P. & RISHI, A. K. (1989). Genetic heterogeneity within Echinococcus granulosus: isolates from different hosts and geographical areas characterized with DNA probes. Parasitology 99, 17–29.CrossRefGoogle Scholar
McMANUS, D. P. & SIMPSON, A. J. G. (1985). Identification of the Echinococcus (hydatid disease) organisms using cloned DNA markers. Molecular and Biochemical Parasitology 17, 171–178.CrossRefGoogle Scholar
McMANUS, D. P., SIMPSON, A. J. G. & RISHI, A. K. (1987). Characterisation of the hydatid disease organism, Echinococcus granulosus, from Kenya using cloned DNA markers. In Helminth Zoonoses ( ed. Geerts, S., Kumar, V. & Brandt, J. ), pp. 29–36. Martinus Nijhoff, Dordrecht. The Netherlands.CrossRef
McMANUS, D. P., ZHANG, L., CASTRODALE, L. J., LE, T. H., PEARSON, M. & BLAIR, D. (2002). Short report: molecular genetic characterization of an unusually severe case of hydatid disease in Alaska caused by the cervid strain of Echinococcus granulosus. American Journal of Tropical Medicine and Hygiene 67, 296–298.CrossRefGoogle Scholar
NAKAO, M., YOKOYAMA, N., SAKO, Y., FUKUNAGA, M. & ITO, A. (2002). The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 1, 497–509.CrossRefGoogle Scholar
ORTLEPP, R. J. (1934). Echinococcus in dogs from Pretoria and vicinity. Onderspoort Journal of Verinary Science and Animal Industry 3, 97–108.Google Scholar
PAWLOWSKI, Z. (1985). Epidemiological basis for chemotherapy of human echinococcosis. International Journal of Clinical Pharmacological Research 5, 75–78.Google Scholar
PAWLOWSKI, Z., MROZEWICZ, B., STEFANIAK, J., SCHANTZ, P., WILSON, M., ECKERT, J., JAQUIER, P., HAREMSKI, T., NOWOSIELSKI, J. & ZIETA, B. (1993). Echinococcus granulosus pig strain from Poland has a low infectivity to humans. American Journal of Tropical Medicine and Hygience 49 (Suppl.), 342–343.Google Scholar
PEARSON, M., LE, T. H., ZHANG, L. H., BLAIR, D., DAI, T. H. N. & McMANUS, D. P. (2002). Molecular taxonomy and strain analysis in Echinococcus. In Tapeworm Zoonoses an Emergent and Global Problem ( ed. Craig, P. S. & Pawlowski, Z. S. ), pp. 205–219. Van Diemenstraat, Amsterdam, Netherlands, IOS Press.
RAUSCH, R. L. (1967). A consideration of intraspecific categories in the genus Echinococcus Rudolphi, 1801 (Cestoda: Taeniidae). Journal of Parasitology 53, 484–491.CrossRefGoogle Scholar
RAUSCH, R. L. (1986). Life-cycle patterns and geographic distribution of Echinococcus species. In The Biology of Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. ), pp. 44–80. London, George Allen & Unwin.
RAUSCH, R. L. & NELSON, G. S. (1963). A review of the genus Echinococcus Rudolphi, 1801. Annals of Tropical Medicine and Parasitology 57, 127–135.CrossRefGoogle Scholar
RINDER, H., RAUSCH, R. L., TAKAHASHI, K., KOPP, H., THOMSCHKE, A. & LÖSCHER, T. (1997). Limited range of genetic variation in Echinococcus multilocularis. Journal of Parasitology 83, 1045–1050.CrossRefGoogle Scholar
RISHI, A. K. & McMANUS, D. P. (1987). Genomic cloning of human Echinococcus granulosus DNA: isolation of recombinant plasmids and their use as genetic markers in strain characterization. Parasitology 94, 369–383.CrossRefGoogle Scholar
RODRIGUES, N. B., COURA FILHO, P., DE SOUZA, C. P., JANNOTI PASSOS, L. K., DIAS-NETO, E. & ROMANHA, A. J. (2002). Populational structure of Schistosoma mansoni assessed by DNA microsatellites. International Journal for Parasitology 32, 843–851.CrossRefGoogle Scholar
ROSENZVIT, M. C., ZHANG, L.-H., KAMENETZKY, L., CANOVA, S. G., GUARNERA, E. A. & McMANUS, D. P. (1999). Genetic variation and epidemiology of Echinococcus granulosus in Argentina. Parasitology 118, 523–530.CrossRefGoogle Scholar
SCHLOTTERER, C. (2000). Evolutionary dynamics of microsatellite DNA. Chromosoma 109, 365–371.CrossRefGoogle Scholar
SCOTT, J. C. & McMANUS, D. P. (1994). The random amplification of polymorphic DNA can discriminate species and strains of Echinococcus. Tropical Medicine and Parasitology 45, 1–4.Google Scholar
SCOTT, J. C., STEFANIAK, J., PAWLOWSKI, Z. S. & McMANUS, D. P. (1997). Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114, 37–43.CrossRefGoogle Scholar
SILES-LUCAS, M., FELLEISEN, R., CUESTA-BANDERA, C., GOTTSTEIN, B. & ECKERT, J. (1994). Comparative genetic analysis of Swiss and Spanish isolates of Echinococcus granulosus by southern hybridization and random amplified polymorphic DNA technique. Applied Parasitology 35, 107–117.Google Scholar
SMYTH, J. D. (1977). Strain differences in Echinococcus granulosus, with special reference to the status of equine hydatidosis in the United Kingdom. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 93–100.CrossRefGoogle Scholar
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. Journal of Helminthology 74, 177–181.Google Scholar
STEFANIAK, J. & LEMKE, A. (1995). Clinical aspects of hepatic cystic echinococcosis. Differential diagnosis of Echinococcus cysts in the liver by ultrasonography and fine needle aspiration biopsy. Hepatologia Polska 2, 33–38.Google Scholar
TASHANI, O. A., ZHANG, L. H., BOUFANA, B., JEGI, A. & McMANUS, D. P. (2002). Epidemiology and strain characteristics of Echinococcus granulosus in the Benghazi area of eastern Libya. Annals of Tropical Medicine and Parasitology 96, 369–381.CrossRefGoogle Scholar
THOMPSON, R. C. A. (1995). Biology and systematics of Echinococcus. In Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A. & Lymbery, A. J. ), pp. 1–50. Wallingford, Oxon, UK, CAB International.
THOMPSON, R. C. A. & KUMARATILAKE, L. M. (1982). Intraspecific variation in Echinococcus granulosus: the Australian situation and perspectives for the future. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 13–16.CrossRefGoogle Scholar
THOMPSON, R. C. A. & KUMARATILAKE, L. M. (1985). Comparative development of Echinococcus granulosus in dingoes (Canis familiaris dingo) and domestic dogs (Canis familiaris familiaris) with further evidence for the origin of the Australian sylvatic strain. International Journal for Parasitology 15, 535–542.CrossRefGoogle Scholar
THOMPSON, R. C. A., KUMARATILAKE, L. M. & ECKERT, J. (1984). Observations on Echinococcus granulosus of cattle origin in Switzerland. International Journal for Parasitology 14, 283–291.CrossRefGoogle Scholar
THOMPSON, R. C. A. & LYMBERY, A. J.(1988). The nature, extent and significance of variation within the genus Echinococcus. Advances in Parasitology 27, 210–263.CrossRefGoogle Scholar
THOMPSON, R. C. A. & McMANUS, D. P. (2001). Aetiology: parasites and life cycles. In WHO/OIE, Paris. Manual on Echinococcosis in Humans and Animals a Public Health Problem of Global Concern (eds. Eckert, J., Gemmell, M. A., Meslin, F.-X. & Pawlowski, Z. S. ), pp. 1–19. Geneva, World Health Organisation.
THOMPSON, R. C. A. & McMANUS, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452–457.CrossRefGoogle Scholar
TKACH, V. V., SWIDERSKI, Z., DROZDZ, J. & DEMIASZKIEWICZ, A. W. (2002). Molecular identification of Echinococcus granulosus from wild European beaver, Castor fiber (L.) from North-Eastern Poland. Acta Parasitologica 47, 173–176.Google Scholar
TURCEKOVA, L., SNABEL, V., D'AMELIO, S., BUSI, M. & DUBINSKY, P. (2003). Morphological and genetic characterization of Echinococcus granulosus in the Slovak Republic. Acta Tropica 85, 223–229.CrossRefGoogle Scholar
TURCEKOVA, L., SNABEL, V. & DUBINSKY, P. (1998). Genetic variants of Echinococcus granulosus in Slovakia recorded by random amplification of polymorphic DNA. Helminthologia 35, 179–183.Google Scholar
VERSTER, A. J. M. (1965). Review of Echinococcus species in South Africa. Onderstepoort Journal of Veterinary Research 32, 7–118.Google Scholar
WACHIRA, T. M., BOWLES, J., ZEHYLE, E. & McMANUS, D. P. (1993). Molecular examination of the sympatric existence and distribution of sheep and camel strains of Echinococcus granulosus in Kenya. American Journal of Tropical Medicine and Hygiene 48, 473–479.CrossRefGoogle Scholar
WILLIAMS, R. J. & SWEATMAN, G. K. (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.CrossRefGoogle Scholar
YAMASAKI, H., NAKAO, M., SAKO, Y., NAKAYA, K., SATO, M. O., MAMUTI, W., OKAMOTO, M. & ITO, A. (2002). DNA differential diagnosis of human taeniid cestodes by base excision sequence scanning thymine-base reader analysis with mitochondrial genes. Journal of Clinical Microbiology 40, 3818–3821.CrossRefGoogle Scholar
ZHANG, L. H., CHAI, J. J., JIAO, W., OSMAN, Y. & McMANUS, D. P. (1998 a). Mitochondrial genomic markers confirm the presence of the camel strain (G6 genotype) of Echinococcus granulosus in north-western China. Parasitology 116, 29–33.Google Scholar
ZHANG, L. H., ESLAMI, A., HOSSEINI, S. H. & McMANUS, D. P. (1998 b). Mitochondrial DNA markers compared for human and animal isolates indicate the presence of two distinct strains of Echinococcus granulosus in Iran. American Journal of Tropical Medicine and Hygiene 59, 171–174.Google Scholar
ZHANG, L. H., GASSER, R. B., ZHU, X. & McMANUS, D. P. (1999). Screening for different genotypes of Echinococcus granulosus within China and Argentina by single-strand conformation polymorphism (SSCP) analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 329–334.CrossRefGoogle Scholar
ZHANG, L. H., JOSHI, D. D. & McMANUS, D. P. (2000). Three genotypes of Echinococcus granulosus identified in Nepal using mitochondrial DNA markers. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 258–260.CrossRefGoogle Scholar