Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-23T08:50:18.145Z Has data issue: false hasContentIssue false
  • English
  • Français

Canine echinococcosis: genetic diversity of Echinococcus granulosus sensu stricto (s.s.) from definitive hosts

Published online by Cambridge University Press:  16 July 2015

B. Boufana ,
W. Lett ,
S. Lahmar ,
A. Griffiths ,
D.J. Jenkins ,
I. Buishi ,
S.A. Engliez ,
M.A. Alrefadi ,
A.A. Eljaki  and
F.M. Elmestiri
...Show all authors
B. Boufana*
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, United Kingdom
W. Lett
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, United Kingdom
S. Lahmar
Affiliation:
Parasitology Laboratory, National School of Veterinary Medicine, Sidi Thabet, Tunisia
A. Griffiths
Affiliation:
School of Biological Sciences, University of Bristol, Life Sciences Building, Bristol, BS8 1TQ, UK
D.J. Jenkins
Affiliation:
School of Animal and Veterinary Sciences, Charles Sturt University, NSW2678, Australia
I. Buishi
Affiliation:
The University of Tripoli, PO Box 606, Tripoli, Libya
S.A. Engliez
Affiliation:
Department of Zoology, University of Benghazi, PO Box 1308, Benghazi, Libya
M.A. Alrefadi
Affiliation:
Department of Zoology, University of Benghazi, PO Box 1308, Benghazi, Libya
A.A. Eljaki
Affiliation:
Department of Zoology, University of Omar Almukhtar, Al Bayda, Libya
F.M. Elmestiri
Affiliation:
Department of Zoology, University of Benghazi, PO Box 1308, Benghazi, Libya
M.M. Reyes
Affiliation:
Alberto Hurtado School of Medicine, Universidad Peruana Cayetano Heredia, Lima, Peru
S. Pointing
Affiliation:
Department of Agriculture, Stanley, Falkland Islands, FIQQ 1ZZ
A. Al-Hindi
Affiliation:
The Islamic University of Gaza, Faculty of Health Sciences, Medical Laboratory Sciences Department, Gaza, Palestine
P.R. Torgerson
Affiliation:
Section of Veterinary Epidemiology, University of Zürich, Switzerland
M. Okamoto
Affiliation:
Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan
P.S. Craig
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, United Kingdom
*
*E-mail: bboufana@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Canids, particularly dogs, constitute the major source of cystic echinococcosis (CE) infection to humans, with the majority of cases being caused by Echinococcus granulosus (G1 genotype). Canine echinococcosis is an asymptomatic disease caused by adult tapeworms of E. granulosus sensu lato (s.l.). Information on the population structure and genetic variation of adult E. granulosus is limited. Using sequenced data of the mitochondrial cytochrome c oxidase subunit 1 (cox1) we examined the genetic diversity and population structure of adult tapeworms of E. granulosus (G1 genotype) from canid definitive hosts originating from various geographical regions and compared it to that reported for the larval metacestode stage from sheep and human hosts. Echinococcus granulosus (s.s) was identified from adult tapeworm isolates from Kenya, Libya, Tunisia, Australia, China, Kazakhstan, United Kingdom and Peru, including the first known molecular confirmation from Gaza and the Falkland Islands. Haplotype analysis showed a star-shaped network with a centrally positioned common haplotype previously described for the metacestode stage from sheep and humans, and the neutrality indices indicated population expansion. Low Fst values suggested that populations of adult E. granulosus were not genetically differentiated. Haplotype and nucleotide diversities for E. granulosus isolates from sheep and human origin were twice as high as those reported from canid hosts. This may be related to self-fertilization of E. granulosus and/or to the longevity of the parasite in the respective intermediate and definitive hosts. Improved nuclear single loci are required to investigate the discrepancies in genetic variation seen in this study.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 6 , November 2015 , pp. 689 - 698
Copyright
Copyright © Cambridge University Press 2015 

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

Abushhewa, M.H., Abushhiwa, M.H., Nolan, M.J., Jex, A.R., Campbell, B.E., Jabbar, A. & Gasser, R.B. (2010) Genetic classification of Echinococcus granulosus cysts from humans, cattle and camels in Libya using mutation scanning-based analysis of mitochondrial loci. Molecular Cell Probes 24, 346–351.CrossRefGoogle ScholarPubMed
Adwan, G., Adwan, K., Bdir, S. & Abuseir, S. (2013) Molecular characterization of Echinococcus granulosus isolated from sheep in Palestine. Experimental Parasitology 134, 195–209.CrossRefGoogle ScholarPubMed
Allan, J.C. & Craig, P.S. (2006) Coproantigens in taeniasis and echinococcosis. Parasitology International 55 (Suppl.), S75–S80.CrossRefGoogle ScholarPubMed
Al-Qaoud, K.M., Abdel-Hafez, S.K. & Craig, P.S. (2003) Canine echinococcosis in northern Jordan: increased prevalence and dominance of sheep/dog strain. Parasitology Research 90, 187–191.CrossRefGoogle ScholarPubMed
Alvarez Rojas, C., Romig, T. & Lightowlers, M.W. (2014) Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. Internationl Journal for Parasitology 44, 9–18.CrossRefGoogle ScholarPubMed
Bart, J.M., Abdukader, M., Zhang, Y.L., Lin, R.Y., Wang, Y.H., Nakao, M., Ito, A., Craig, P.S., Piarroux, R., Vuitton, D.A. & Wen, H. (2006a) Genotyping of human cystic echinococcosis in Xinjiang, PR China. Parasitology 133, 571–579.CrossRefGoogle ScholarPubMed
Bart, J.M., Morariu, S., Knapp, J., Ilie, M.S., Pitulescu, M., Anghel, A., Cosoroaba, I. & Piarroux, R. (2006b) Genetic typing of Echinococcus granulosus in Romania. Parasitology Research 98, 130–137.CrossRefGoogle ScholarPubMed
Beato, S., Parreira, R., Roque, C., Gonçalves, M., Silva, L., Maurelli, M.P., Cringoli, G. & Grácio, M.A. (2013) Echinococcus granulosus in Portugal: the first report of the G7 genotype in cattle. Veterinary Parasitology 15, 235–239.CrossRefGoogle Scholar
Boufana, B., Lahmar, S., Rebaï, W., Ben Safta, Z., Jebabli, L., Ammar, A., Kachti, M., Aouadi, S. & 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. & 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
Budke, C.M., Deplazes, P. & Torgerson, P.R. (2006) Global socioeconomic impact of cystic echinococcosis. Emerging Infectious Diseases 12, 296–303.CrossRefGoogle ScholarPubMed
Buishi, I., Walters, T., Guildea, Z., Craig, P. & Palmer, S. (2005) Re-emergence of canine Echinococcus granulosus infection, Wales. Emerging Infectious Diseases 11, 568–571.CrossRefGoogle Scholar
Carmena, D. & Cardona, G.A. (2013) Canine echinococcosis: global epidemiology and genotypic diversity. Acta Tropica 128, 441–460.CrossRefGoogle ScholarPubMed
Casulli, A., Interisano, M., Sreter, 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. Infection, Genetics and Evolution 12, 377–383.CrossRefGoogle Scholar
Craig, P.S., Gasser, R.B., Parada, L., Cabera, P., Parietti, S., Borgues, C., Acuttis, A., Aguilla, J., Snowden, K. & Paolillo, E. (1995) Diagnosis of canine echinococcosis: comparison of coproantigen and serum antibody tests with arecoline purgation in Uruguay. Veterinary Parasitology 56, 293–301.CrossRefGoogle ScholarPubMed
Craig, P.S., Rogan, M.T. & Campos-Ponce, M. (2003) Echinococcosis: disease, detection and transmission. Parasitology 127 (Suppl.), S5–S20.CrossRefGoogle ScholarPubMed
Craig, P.S., McManus, D.P., Lightowlers, M.W., Chabalgoity, J.A., Garcia, H.H., Gavidia, C.M., Gilman, R.H., Gonzalez, A.E., Lorca, M., Naquira, C., Nieto, A. & Schantz, P.M. (2007) Prevention and control of cystic echinococcosis. The Lancet Infectious Diseases 7, 385–394.CrossRefGoogle ScholarPubMed
Davidson, R.K., Romig, T., Jenkins, E., Tryland, M. & Robertson, L.J. (2012) The impact of globalisation on the distribution of Echinococcus multilocularis. Trends in Parasitology 28, 239–247.CrossRefGoogle ScholarPubMed
de la Rue, M.L., Takano, K., Brochado, J.F., Costa, C.V., Soares, A.G., Yamano, K., Yagi, K., Katoh, Y. & Takahashi, K. (2011) Infection of human and animals with Echinococcus granulosus (G1 and G3 strains) and E. ortleppi in Southern Brazil. Veterinary Parasitology 177, 97–103.CrossRefGoogle Scholar
Eckert, J., Gemmell, M.A., Meslin, F.X. & Pawlowski, Z.S. (2001) Manual on echinococcosis in humans and animals; a public health problem of global concern. Paris, World Organisation for Animal Health.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Felsenstein, J. (1989) PHYLIP – phylogeny inference package (version 3.2). Cladistics 5, 164–166.Google Scholar
Fu, Y.X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Gemmell, M.A. (1990) Australasian contributions to an understanding of the epidemiology and control of hydatid disease caused by Echinococcus granulosus – past, present and future. International Journal for Parasitology 20, 431–456.CrossRefGoogle Scholar
Haag, K.L., Araujo, A.M., Gottstein, B., Siles-Lucas, M., Thompson, R.C.A. & Zaha, A. (1999) Breeding systems in Echinococcus granulosus (Cestoda Taeniidae): selfing or outcrossing? Parasitology 118, 63–67.CrossRefGoogle ScholarPubMed
Hüttner, M., Siefert, L., Mackenstedt, U. & Romig, T. (2009) A survey of Echinococcus species in wild carnivores and livestock in East Africa. International Journal for Parasitology 39, 1269–1276.CrossRefGoogle ScholarPubMed
Jenkins, D.J., Lievaart, J.J., Boufana, B., Lett, W.S., Bradshaw, H. & Armua-Fernandezc, M.T. (2014) Echinococcus granulosus and other intestinal helminths: current status of prevalence and management in rural dogs of eastern Australia. Australian Veterinary Journal 92, 292–298.CrossRefGoogle ScholarPubMed
Kagendo, D., Magambo, J., Agola, E.L., Njenga, S.M., Zeyhle, E., Mulinge, E., Gitonga, P., Mbae, C., Muchiri, E., Wassermann, M., Kern, P. & Romig, T. (2014) A survey for Echinococcus spp. of carnivores in six wildlife conservation areas in Kenya. Parasitology International 63, 604–611.CrossRefGoogle ScholarPubMed
Konyaev, S.V., Yanagida, T., Nakao, M., Ingovatova, G.M., Shoykhet, Y.N., Bondarev, A.Y., Odnokurtsev, V.A., Loskutova, K.S., Lukmanova, G.I., Dokuchaev, N.E., Spiridonov, S., Alshinecky, M.V., Sivkova, T.N., Andreyanov, O.N., Abramov, S.A., Krivopalov, A.V., Karpenko, S.V., Lopatina, N.V., Dupal, T.A., Sako, Y. & Ito, A. (2013) Genetic diversity of Echinococcus spp. in Russia. Parasitology 140, 1637–1647.CrossRefGoogle ScholarPubMed
Lahmar, S., Boufana, B.S., Lahmar, S., Inoubli, S., Guadraoui, M., Dhibi, M., Bradshaw, H. & Craig, P.S. (2009) Echinococcus in the wild carnivores and stray dogs of northern Tunisia: the results of a pilot survey. Annals of Tropical Medicine and Parasitology 103, 323–331.CrossRefGoogle ScholarPubMed
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Lett, W. (2013) Detection of Echinococcus granulosus and Echinococcus equinus in dogs and epidemiology of canine echinococcosis in the UK. A thesis submitted for the partial requirement of the degree of Doctor of Philosophy (PhD), University of Salford, UK.Google Scholar
Librado, P. & Rozas, J. (2009) DnaDP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle Scholar
Lymbery, A.J., Constantine, C.C. & Thompson, R.C.A. (1997) Self-fertilization without genomic or population structuring in a parasitic tapeworm. Evolution 51, 289–294.CrossRefGoogle ScholarPubMed
Ma, S.M., Maillard, S., Zhao, H.L., Huang, X., Wang, H., Geng, P.L., Bart, J.M. & Piarroux, R. (2008) Assessment of Echinococcus granulosus polymorphism in Qinghai province, People's Republic of China. Parasitology Research 102, 1201–1206.CrossRefGoogle ScholarPubMed
Moro, P.L., Nakao, M., Ito, A., Schantz, P.M., Cavero, C. & Cabrera, L. (2009) Molecular identification of Echinococcus isolates from Peru. Parasitology International 58, 184–186.CrossRefGoogle ScholarPubMed
Moss, J.E., Chen, X., Li, T., Wang, Q., Giraudoux, P., Ito, A., Torgerson, P.R. & Craig, P.S. (2013) Reinfection studies of canine echinococcosis and role of dogs in transmission of Echinococcus multilocularis in Tibetan communities, Sichuan, China. Parasitology 140, 1685–1692.CrossRefGoogle ScholarPubMed
Nakao, M., Sako, Y., Yokoyama, N., Fukunaga, M. & Ito, A. (2000) Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415–424.CrossRefGoogle ScholarPubMed
Nakao, M., Sako, Y. & Ito, A. (2003) Isolation of polymorphic microsatellite loci from the tapeworm Echinococcus multilocularis. Infection, Genetics and Evolution 3, 159–163.CrossRefGoogle ScholarPubMed
Nakao, M., McManus, D.P., Schantz, P.M., Craig, P.S. & Ito, A. (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713–722.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. & 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.CrossRefGoogle Scholar
Obwaller, A., Schneider, R., Walochnik, J., Gollackner, B., Deutz, A., Janitschke, K., Aspöck, H. & Auer, H. (2004) Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitology 128, 569–575.CrossRefGoogle ScholarPubMed
Parsa, F., Fasihi Harandi, M., Rostami, S. & Sharbatkhori, M. (2012) Genotyping Echinococcus granulosus from dogs from Western Iran. Experimental Parasitology 132, 308–312.CrossRefGoogle ScholarPubMed
Petit, R.J., El Mousadik, A. & Pons, O. (1998) Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12, 844–855.CrossRefGoogle Scholar
Reyes, M.M., Taramona, C.P., Saire-Mendoza, M., Gavidia, C.M., Barron, E., Boufana, B., Craig, P.S., Tello, L., Garcia, H.H. & Santivañez, S.J. (2012) Human and canine Echinococcosis infection in informal, unlicensed abattoirs in Lima, Peru. PLoS Neglected Tropical Diseases 6, e1462.CrossRefGoogle ScholarPubMed
Salzburger, W., Ewing, G.B. & Haeseler, A. (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology 20, 1952–1963.CrossRefGoogle ScholarPubMed
Sharma, M., Fomda, B.A., Mazta, S., Sehgal, R., Singh, B.B. & Malla, N. (2013) Genetic diversity and population genetic structure analysis of Echinococcus granulosus sensu stricto complex based on mitochondrial DNA signature. PLoS One 8, e82904.CrossRefGoogle ScholarPubMed
Sherifi, K., Rexhepi, A., Hamidi, A., Behluli, B., Zessin, K.H., Mathis, A. & Deplazes, P. (2011) Detection of patent infections of Echinococcus granulosus (sheep-strain, G1) in naturally infected dogs in Kosovo. Berliner und Munchener Tierarztliche Wochenschrift 124, 518–521.Google ScholarPubMed
Simsek, S., Kaplan, M. & Ozercan, I.H. (2011) A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitology Research 109, 411–416.CrossRefGoogle ScholarPubMed
Snábel, V., Altintas, N., D'Amelio, S., Nakao, M., Romig, T., Yolasigmaz, A., Gunes, K., Turk, M., Busi, M., Hüttner, M., Sevcová, D., Ito, A., Altintas, N. & Dubinský, P. (2009) Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitology Research 105, 145–154.CrossRefGoogle ScholarPubMed
Soriano, S.V., Pierangelli, N.B., Pianciola, L., Mazzeo, M., Lazzarini, L.E., Saiz, M.S., Kossman, A.V., Bergagna, H.F., Chartier, K. & Basualdo, J.A. (2010) Molecular characterization of Echinococcus isolates indicates goats as reservoir for Echinococcus canadensis G6 genotype in Neuquen, Patagonia Argentina. Parasitology International 59, 626–628.CrossRefGoogle ScholarPubMed
Štefanić, S., Shaikenov, B.S., Deplazes, P., Dinkel, A., Torgerson, P.R. & Mathis, A (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (‘sheep strain’) in naturally infected dogs. Parasitology Research 92, 347–351.CrossRefGoogle ScholarPubMed
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. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thompson, R.C. (2008) The taxonomy, phlogeny and transmission of Echinococcus. Experimental Parasitology 119, 439–446.CrossRefGoogle Scholar
Thompson, R.C. & McManus, D.P. (2002) Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452–457.CrossRefGoogle ScholarPubMed
Trachsel, D., Deplazes, P. & Mathis, A. (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911–920.CrossRefGoogle ScholarPubMed
Utuk, A.E., Simsek, S., Koroglu, E. & McManus, D.P. (2008) Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta Tropica 107, 192–194.CrossRefGoogle Scholar
Wachira, T.M., Macpherson, C.N. & Gathuma, J.M. (1990) Hydatid disease in the Turkana District of Kenya, VII: analysis of the infection pressure between definitive and intermediate hosts of Echinococcus granulosus, 1979–1988. Annals of Tropical Medicine and Parasitology 84, 361–368.CrossRefGoogle ScholarPubMed
Wachira, T.M., Sattran, M., Zeyhle, E. & Njenga, M.K. (1993a) Intestinal helminths of public health importance in dogs in Nairobi. East African Medical Journal 70, 617–619.Google ScholarPubMed
Wachira, T.M., Bowles, J., Zeyhle, E. & McManus, D.P. (1993b) Molecular examination of the sympatry and distribution of sheep and camel strains of Echinococcus granulosus in Kenya. American Journal of Tropical Medicine and Hygiene 48, 473–479.CrossRefGoogle ScholarPubMed
Xhaxhiu, D., Kusi, I., Rapti, D., Kondi, E., Postoli, R., Rinaldi, L., Dimitrova, Z.M., Visser, M., Knaus, M. & Rehbein, S. (2011) Principal intestinal parasites of dogs in Tirana, Albania. Parasitology Research 108, 341–353.CrossRefGoogle ScholarPubMed
Yanagida, T., Mohammadzadeh, T., Kamhawi, S., Nakao, M., Sadjjadi, S.M., Hijjawi, N., Abdel-Hafez, S.K., Sako, Y., Okamoto, M. & Ito, A. (2012) Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitology International 61, 599–603.CrossRefGoogle ScholarPubMed
Zhang, Y., Bart, J.M., Giraudoux, P., Craig, P., Vuitton, D. & Wen, H. (2006) Morphological and molecular characteristic of Echinococcus multilocularis and Echinococcus granulosus mixed infection in a dog from Xinjiang. China. Veterinary Parasitology 139, 244–248.CrossRefGoogle Scholar
Ziadinov, I., Mathis, A., Trachsel, D., Rysmukhambetova, A., Abdyjaparov, T.A., Kuttubaev, O.T., Deplazes, P. & Torgerson, P.R. (2008) Canine echinococcosis in Kyrgyzstan; using prevalence data adjusted for measurement error to develop transmission dynamics models. International Journal for Parasitology 38, 1179–1190.CrossRefGoogle ScholarPubMed