Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-23T03:58:17.130Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic polymorphism and population structure of Echinococcus ortleppi

Published online by Cambridge University Press:  12 December 2016

F. ADDY ,
M. WASSERMANN ,
F. BANDA ,
H. MBAYA ,
J. ASCHENBORN ,
O. ASCHENBORN ,
P. KOSKEI ,
G. UMHANG ,
M. DE LA RUE  and
I. E. ELMAHDI
...Show all authors
F. ADDY*
Affiliation:
University of Hohenheim, Parasitology Unit, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
M. WASSERMANN
Affiliation:
University of Hohenheim, Parasitology Unit, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
F. BANDA
Affiliation:
Ministry of Fisheries and Livestock, Western Province, P.O. Box 910034, Mongu, Zambia
H. MBAYA
Affiliation:
National Biosafety Authority, P. O. Box 28251 00100, Nairobi, Kenya
J. ASCHENBORN
Affiliation:
University of Zürich, Institut für Parasitologie, Winterthurerstr. 266a, CH-8057 Zürich, Switzerland
O. ASCHENBORN
Affiliation:
University of Hohenheim, Parasitology Unit, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
P. KOSKEI
Affiliation:
Moi University, School of Public Health, P. O. Box 4606 30100, Eldoret, Kenya
G. UMHANG
Affiliation:
Anses Wildlife Surveillance and Eco-epidemiology unit, Technopôle Agricole et Vétérinaire, B.P. 40009, 54220 Malzéville, France
M. DE LA RUE
Affiliation:
Department of Microbiology and Parasitology, Federal University of Santa Maria, Prédio 20–Sala 4226, CEP 97105–970 Santa Maria, Brazil
I. E. ELMAHDI
Affiliation:
University of Gezira, Faculty of Health and Environmental Sciences, P.O. Box 20, Wad Medani, Sudan
U. MACKENSTEDT
Affiliation:
University of Hohenheim, Parasitology Unit, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
P. KERN
Affiliation:
Ulm University Hospitals, Comprehensive Infectious Diseases Center, Albert-Einstein-Allee 23 D-89081, Ulm, Germany
T. ROMIG
Affiliation:
University of Hohenheim, Parasitology Unit, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany
*
*Corresponding author: University of Hohenheim, Parasitology Unit, Emil-Wolff-Str. 34, 70599 Stuttgart, Germany. Email: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The zoonotic cestode Echinococcus ortleppi (Lopez-Neyra and Soler Planas, 1943) is mainly transmitted between dogs and cattle. It occurs worldwide but is only found sporadically in most regions, with the notable exception of parts of southern Africa and South America. Its epidemiology is little understood and the extent of intraspecific variability is unknown. We have analysed in the present study the genetic diversity among 178 E. ortleppi isolates from sub-Saharan Africa, Europe and South America using the complete mitochondrial cox1 (1608 bp) and nad1 (894 bp) DNA sequences. Genetic polymorphism within the loci revealed 15 cox1 and six nad1 haplotypes, respectively, and 20 haplotypes of the concatenated genes. Presence of most haplotypes was correlated to geographical regions, and only one haplotype had a wider spread in both eastern and southern Africa. Intraspecific microvariance was low in comparison with Echinococcus granulosus sensu stricto, despite the wide geographic range of examined isolates. In addition, the various sub-populations showed only subtle deviation from neutrality and were mostly genetically differentiated. This is the first insight into the population genetics of the enigmatic cattle adapted Echinococcus ortleppi. It, therefore, provides baseline data for biogeographical comparison among E. ortleppi endemic regions and for tracing its translocation paths.

Keywords

Echinococcus ortleppimicrodiversityhaplotypecox1nad1AfricaBrazilFrance
Type
Research Article
Information
Parasitology , Volume 144 , Issue 4 , April 2017 , pp. 450 - 458
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Addy, F., Alakonya, A., Wamae, N., Magambo, J., Mbae, C., Mulinge, E., Zeyhle, E., Wassermann, M., Kern, P. and Romig, T. (2012). Prevalence and diversity of cystic echinococcosis in livestock in Maasailand, Kenya. Parasitology Research 111, 2289–2294.Google Scholar
Alvarez Rojas, C. A., Romig, T. and Lightowlers, M. W. (2014). Echinococcus granulosus sensu lato genotypes infecting humans–review of current knowledge. International Journal for Parasitology 44, 9–18.CrossRefGoogle ScholarPubMed
Alvarez Rojas, C. A., Ebi, D., Gauci, C. G., Scheerlinck, J. P., Wassermann, M., Jenkins, D. J., Lightowlers, M. W. and Romig, T. (2016). Microdiversity of Echinococcus granulosus sensu stricto in Australia. Parasitology 1–8.Google Scholar
Balbinotti, H., Santos, G. B., Badaraco, J., Arend, A. C., Graichen, D. Â. S., Haag, K. L. and Zaha, A. (2012). Echinococcus ortleppi (G5) and Echinococcus granulosus sensu stricto (G1) loads in cattle from Southern Brazil. Veterinary Parasitology 188, 255–260.Google Scholar
Boufana, B., Lahmar, S., Rebai, W., Safta, Z. B., Jebabli, L., Ammar, A., Kachti, M., Aouadi, S. and Craig, P. S. (2014). Genetic variability and haplotypes of Echinococcus isolates from Tunisia. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 706–714.CrossRefGoogle ScholarPubMed
Boufana, B., Lett, W. S., Lahmar, S., Buishi, I., Bodell, A. J., Varcasia, A., Casulli, A., Beeching, N. J., Campbell, F., Terlizzo, M., McManus, D. P. and Craig, P. S. (2015). Echinococcus equinus and Echinococcus granulosus sensu stricto from the United Kingdom: genetic diversity and haplotypic variation. International Journal for Parasitology 45, 161–166.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Cardona, G. A. and Carmena, D. (2013). A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Veterinary Parasitology 192, 10–32.CrossRefGoogle ScholarPubMed
Casulli, A., Interisano, M., Sreter, T., Chitimia, L., Kirkova, Z., La Rosa, G. and Pozio, E. (2012). Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 12, 377–383.Google Scholar
Clement, M., Posada, D. and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.Google Scholar
Decker, J. E., McKay, S. D., Rolf, M. M., Kim, J. W., Molina Alcalá, A., Sonstegard, T. S., Hanotte, O., Götherström, A., Seabury, C. M., Praharani, L., Babar, M. E., Correia de Almeida Regitano, L., Yildiz, M. A., Heaton, M. P., Liu, W. S., Lei, C. Z., Reecy, J. M., Saif-Ur-Rehman, M., Schnabel, R. D. and Taylor, J. F. (2014). Worldwide patterns of ancestry, divergence, and admixture in domesticated Cattle. PLoS Genetics 10, 1–14.Google Scholar
Dinkel, A., Von Nickisch-Rosenegk, M., Bilger, B., Merli, M., Lucius, R. and Romig, T. (1998). Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. Journal of Clinical Microbiology 36, 1871–1876.Google Scholar
Excoffier, L., Laval, G. and Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.Google Scholar
Grenouillet, F., Umhang, G., Arbez-Gindre, F., Mantion, G., Delabrousse, E., Millon, L. and Boué, F. (2014). Echinococcus ortleppi infections in humans and cattle, France. Emerging Infectious Diseases 20, 2100–2102.Google Scholar
Haag, K. L., Araújo, A. M., Gottstein, B., Siles-Lucas, M., Thompson, R. C. and Zaha, A. (1999). Breeding systems in Echinococcus granulosus (Cestoda; Taeniidae): selfing or outcrossing? Parasitology 118, 63–71.CrossRefGoogle ScholarPubMed
Hüttner, M., Nakao, M., Wassermann, T., Siefert, L., Boomker, J. D. F., Dinkel, A., Sako, Y., Mackenstedt, U., Romig, T. and Ito, A. (2008). Genetic characterization and phylogenetic position of Echinococcus felidis Ortlepp, 1937 (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 38, 861–868.Google Scholar
Kamenetzky, L., Gutierrez, A. M., Canova, S. G., Haag, K. L., Guarnera, E. A., Parra, A., García, G. E. and Rosenzvit, M. C. (2002). Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infection, Genetics and Evolution 2, 129–136.CrossRefGoogle ScholarPubMed
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.Google Scholar
Lopez-Neyra, C. R. and Soler Planas, M. A. (1943). Revision del genero Echinococcus Rudy description de una especie nuéva Parasita intestinal del porro en Almeria. Revista ibérica de parasitología 3, 169–194.Google Scholar
Lymbery, A. J., Jenkins, E. J., Schurer, J. M. and Thompson, R. C. A. (2015 a). Echinococcus canadensis, E. borealis, and E. intermedius. What's in a name? Trends in Parasitology 31, 23–29.Google Scholar
Lymbery, A. J., Jenkins, E. J., Schurer, J. M. and Thompson, R. C. A. (2015 b). Response to Nakao et al. –is Echinococcus intermedius a valid species? Trends in Parasitology 31, 343–344.Google Scholar
Mbaya, H., Magambo, J., Njenga, S., Zeyhle, E., Mbae, C., Mulinge, E., Wassermann, M., Kern, P. and Romig, T. (2014). Echinococcus spp. in central Kenya: a different story. Parasitology Research 113, 3789–3794.Google Scholar
McManus, D. P., Knight, M. and Simpson, A. J. G. (1985). Isolation and characterisation of nucleic acids from the hydatid organisms, Echinococcus spp. (cestoda). Molecular and Biochemical Parasitology 16, 251–266.Google Scholar
Nakao, M., Sako, Y., Yokoyama, N., Fukunaga, M. and Ito, A. (2000). Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415–424.Google Scholar
Nakao, M., Sako, Y. and Ito, A. (2003). Isolation of polymorphic microsatellite loci from the tapeworm Echinococcus multilocularis . Infection, Genetics and Evolution 3, 159–163.CrossRefGoogle ScholarPubMed
Nakao, M., Li, T., Han, X., Ma, X., Xiao, N., Qiu, J., Wang, H., Yanagida, T., Mamuti, W., Wen, H., Moro, P. L., Giraudoux, P., Craig, P. S. and Ito, A. (2010). Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. International Journal for Parasitology 40, 379–385.Google Scholar
Nakao, M., Yanagida, T., Konyaev, S., Lavikainen, A., Odnokurtsev, V. A., Zaikov, V. A. and Ito, A. (2013). Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 140, 1625–1636.Google Scholar
Nakao, M., Lavikainen, A. and Hoberg, E. (2015). Is Echinococcus intermedius a valid species? Trends in Parasitology 31, 342–343.CrossRefGoogle ScholarPubMed
Pednekar, R. P., Gatne, M. L., Thompson, R. C. A. and Traub, R. J. (2009). Molecular and morphological characterisation of Echinococcus from food producing animals in India. Veterinary Parasitology 165, 58–65.Google Scholar
Romig, T., Omer, R. A., Zeyhle, E., Huettner, M., Dinkel, A., Siefert, L., Elmahdi, I. E., Magambo, J., Ocaido, M., Menezes, C. N., Ahmed, M. E., Mbae, C., Grobusch, M. P. and Kern, P. (2011). Echinococcosis in sub-Saharan Africa: emerging complexity. Veterinary Parasitology 181, 43–47.Google Scholar
Romig, T., Ebi, D. and Wassermann, M. (2015). Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology 213, 76–84.Google Scholar
Santos, G. B., Soares, M. do C. P., Elisabete, E. M., Rodrigues, A. L., Siqueira, N. G., Gomes-Gouvêa, M. S., Alves, M. M., Carneiro, L. A., Malheiros, A. P., Póvoa, M. M., Zaha, A. and Haag, K. L. (2012). Mitochondrial and nuclear sequence polymorphisms reveal geographic structuring in Amazonian populations of Echinococcus vogeli (Cestoda: Taeniidae). International Journal for Parasitology 42, 1115–1118.Google Scholar
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Templeton, A. R., Crandall, K. A. and Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.Google Scholar
Thompson, R. C. A. (2008). The taxonomy, phylogeny and transmission of Echinococcus . Experimental Parasitology 119, 439–446.Google Scholar
Thompson, R. C. A. and Lymbery, A. J. (1988). The nature, extent and significance of variation within the genus Echinococcus . Advances in Parasitology 27, 209–258.Google Scholar
Thompson, R. C. A. and Lymbery, A. J. (1990). Echinococcus: biology and strain variation. International Journal for Parasitology 20, 457–470.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and McManus, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus . Trends in Parasitology 18, 452–457.Google Scholar
Tigre, W., Deresa, B., Haile, A., Gabriël, S., Victor, B., Pelt, J. V., Devleesschauwer, B., Vercruysse, J. and Dorny, P. (2016). Molecular characterization of Echinococcus granulosus s.l. cysts from cattle, camels, goats and pigs in Ethiopia. Veterinary Parasitology 215, 17–21.Google Scholar
Wassermann, M., Aschenborn, O., Aschenborn, J., Mackenstedt, U. and Romig, T. (2015). A sylvatic lifecycle of Echinococcus equinus in the Etosha National Park, Namibia. International Journal for Parasitology: Parasites and Wildlife 4, 97–103.Google Scholar
Yanagida, T., Mohammadzadeh, T., Kamhawi, S., Nakao, M., Sadjjadi, S. M., Hijjawi, N., Abdel-Hafez, S. K., Sako, Y., Okamoto, M. and Ito, A. (2012). Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitology International 61, 599–603.Google Scholar
Supplementary material: File

Addy supplementary material

Addy supplementary material 1

Download Addy supplementary material(File)
File 14 KB