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The optimum cut-off value to differentiate Echinococcus granulosus sensu stricto from other species of E. granulosus sensu lato using larval rostellar hook morphometry

Published online by Cambridge University Press:  10 July 2013

S.V. Soriano*
Affiliation:
Microbiology and Parasitology Department, School of Medical Sciences, Comahue National University, Buenos Aires1400, (8300)Neuquén, Argentina
N.B. Pierangeli
Affiliation:
Microbiology and Parasitology Department, School of Medical Sciences, Comahue National University, Buenos Aires1400, (8300)Neuquén, Argentina
L.A. Pianciola
Affiliation:
Central Laboratory, Department of Public Health, Province of Neuquén, Gregorio Martínez 65, (8300)Neuquén, Argentina
M. Mazzeo
Affiliation:
Central Laboratory, Department of Public Health, Province of Neuquén, Gregorio Martínez 65, (8300)Neuquén, Argentina
L.E. Lazzarini
Affiliation:
Microbiology and Parasitology Department, School of Medical Sciences, Comahue National University, Buenos Aires1400, (8300)Neuquén, Argentina
M.F. Debiaggi
Affiliation:
Microbiology and Parasitology Department, School of Medical Sciences, Comahue National University, Buenos Aires1400, (8300)Neuquén, Argentina
H.F.J. Bergagna
Affiliation:
Zoonoses and Vectors Division, Municipality of Neuquén, Argentina Av. 307, (8300), Neuquén, Argentina
J.A. Basualdo
Affiliation:
Microbiology and Parasitology Department, School of Medical Sciences, La Plata National University, 60 and 120 St., (1900), La Plata, Buenos Aires, Argentina
*
*Fax: 54 299 443 0820 E-mail: viviana.soriano@gmail.com

Abstract

Cystic echinococcosis caused by Echinococcus granulosus sensu lato is one of the most important helminth zoonoses in the world; it affects both humans and livestock. The disease is endemic in Argentina and highly endemic in the province of Neuquén. Considerable genetic and phenotypic variation has been demonstrated in E. granulosus, and ten different genotypes (G1–G10) have been identified using molecular tools. Echinococcus granulosus sensu lato may be considered a species complex, comprised of E. granulosus sensu stricto (G1–G3), E. equinus (G4), E. ortleppi (G5) and E. canadensis (G6–G10). In endemic areas, the characterization of cystic echinococcosis molecular epidemiology is important in order to apply adequate control strategies. A cut-off value for larval large hook total length to distinguish E. granulosus sensu stricto isolates from those produced by other species of the complex was defined for the first time. Overall, 1780 larval hooks of 36 isolates obtained from sheep (n= 11, G1), goats (n= 10, G6), cattle (n= 5, G6) and pigs (n= 10, G7) were analysed. Validation against molecular genotyping as gold standard was carried out using the receiver operating characteristic (ROC) curve analysis. The optimum cut-off value was defined as 26.5 μm. The proposed method showed high sensitivity (97.8%) and specificity (91.1%). Since in most endemic regions the molecular epidemiology of echinococcosis includes the coexistence of the widely distributed E. granulosus sensu stricto G1 strain and other species of the complex, this technique could be useful as a quick and economical tool for epidemiological and surveillance field studies, when fertile cysts are present.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2013 

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References

Aaty, H.E., Abdel-Hameed, D.M., Alam-Eldin, Y.H., El-Shennawy, S.F., Aminou, H.A., Makled, S.S. & Darweesh, S.K. (2012) Molecular genotyping of Echinococcus granulosus in animal and human isolates from Egypt. Acta Tropica 121, 125128.CrossRefGoogle ScholarPubMed
Ahmadi, N.A. (2004) Using morphometry of the larval rostellar hooks to distinguish Iranian strains of Echinococcus granulosus. Annals of Tropical Medicine and Parasitology 98, 211220.Google Scholar
Ahmadi, N.A. & Dalimi, A. (2006) Characterization of Echinococcus granulosus isolates from human, sheep and camel in Iran. Infection, Genetics and Evolution 6, 8590.Google Scholar
Almeida, F.B., Rodrigues-Silva, R., Neves, R.H., Romani, E.L.S. & Machado-Silva, J.R. (2007) Intraspecific variation of Echinococcus granulosus in livestock from Peru. Veterinary Parasitology 143, 5058.CrossRefGoogle ScholarPubMed
Andresiuk, M.V., Ponce Gordo, F., Cuesta Bandera, C., Elissondo, M.C., Dopchiz, M. & Denegri, G. (2009) Echinococcus granulosus: biological comparison of cattle isolates from endemic regions of Argentina and Spain. Revista Argentina de Microbiología 41, 218225.Google Scholar
Bart, J.M., Bardonnet, K., Elfegoun, M.C.B., Dumon, H., Dia, L., Vuitton, D.A. & Piarroux, R. (2004) Echinococcus granulosus strain typing in North Africa: comparison of eight nuclear and mitochondrial DNA fragments. Parasitology 128, 229234.Google Scholar
Bart, J.M., Morariu, S., Knapp, J., Hie, M.S., Pitulescu, M., Anghel, A., Cosoroaba, I. & Piarroux, R. (2006) Genetic typing of Echinococcus granulosus in Romania. Parasitology Research 98, 130137.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, 165174.Google Scholar
Calderini, P., Gabrielli, S. & Cancrini, G. (2012) Is the goat a new host for the G3 Indian Buffalo Strain of Echinococcus granulosus? Scientific World Journal doi:10.1100/2012/286357.CrossRefGoogle Scholar
De La Rue, M.L., Dinkel, A., Mackenstedt, U. & Romig, T. (2006) New data on Echinococcus spp. in Southern Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 48, 103104.Google 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, 536544.CrossRefGoogle ScholarPubMed
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, 4248.CrossRefGoogle ScholarPubMed
Harandi, M.F., Hobbs, R.P., Adams, P.J., Mobedi, I., Morgan-Ryan, U.M. & Thompson, R.C.A. (2002) Molecular and morphological characterization of Echinococcus granulosus of human and animal origin in Iran. Parasitology 125, 367373.Google ScholarPubMed
Harandi, M.F., Hajialilo, E. & Shokouhi, M. (2012) Larval hook measurement for differentiating G1 and G6 genotypes of Echinococcus granulosus sensu lato. Turkiye Parazitoloji Dergisi 36, 215218.Google Scholar
Hobbs, R.P., Lymbery, A.J. & Thompson, R.C.A. (1990) Rostellar hook characters of Echinococcus granulosus (Batsch, 1786) from natural and experimental Australian hosts, and its implications for strain recognition. Parasitology 101, 273281.Google Scholar
Hosseini, S.H. & Eslami, A. (1998) Morphological and developmental characteristics of Echinococcus granulosus derived from sheep, cattle and camels in Iran. Journal of Helminthology 72, 337341.Google Scholar
Konyaev, S.V., Yanagida, T., Ingovatova, G.N., Shoikhet, Y.N., Nakao, M., Sako, Y., Bondarev, A.Y. & Ito, A. (2012) Molecular identification of human echinococcosis in the Altai region of Russia. Parasitology International 61, 711714.Google Scholar
Kumaratilake, L.M., Thompson, R.C.A. & Eckert, E. (1986) Echinococcus granulosus of equine origin from different countries possess uniform morphological characteristics. International Journal for Parasitology 16, 529540.Google Scholar
Latif, A.A., Tanveer, A., Maqbool, A., Siddiqi, N., Kyaw-Tanner, M. & Traub, R.J. (2010) Morphological and molecular characterization of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Veterinary Parasitology 170, 4449.Google Scholar
Lavikainen, A., Lehtinen, M.J., Meri, T., Hirvelä-Koski, V. & Meri, S. (2003) Molecular genetic characterisation of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127, 207215.CrossRefGoogle Scholar
Maillard, S., Benchikh-Elfegoun, M.C., Knapp, J., Bart, J.M., Koskei, P., Gottstein, B. & Piarroux, R. (2007) Taxonomic position and genetic distribution of the common sheep G1 and camel G6 strains of Echinococcus granulosus in three African countries. Parasitology Research 100, 495503.Google Scholar
Manterola, C., Benavente, F., Melo, A., Vial, M. & Roa, J.C. (2008) Description of Echinococcus granulosus genotypes in human hydatidosis in a region of southern Chile. Parasitology International 57, 342346.Google Scholar
McManus, D.P. & Thompson, R.C.A. (2003) Molecular epidemiology of cystic echinococcosis. Parasitology 127, S37S51.Google Scholar
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, 184186.CrossRefGoogle ScholarPubMed
Mowlavi, G., Salehi, M., Eshraghian, M., Rokni, M.B., Harandi, M.H., Mohajeran, E. & Salahi-Moghaddam, A. (2012) Morphometric differentiation between camel and sheep strains of Echinococcus granulosus using computer image analysis system (CIAS). Asian Pacific Journal of Tropical Medicine 5, 5861.Google Scholar
M'rad, S., Filisetti, D., Oudni, M., Mekki, M., Belguith, M., Nouri, A., Sayadi, T., Lahmar, S., Candolfi, E., Azaiez, R., Mezhoud, H. & Babba, H. (2005) Molecular evidence of ovine (G1) and camel (G6) strains of Echinococcus granulosus in Tunisia and putative role of cattle in human contamination. Veterinary Parasitology 129, 267272.Google Scholar
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, 713722.Google Scholar
Pednekar, R.P., Mukulesh, L., Gatne, R.C., Thompson, R.C.A. & Traub, R.J. (2009) Molecular and morphological characterization of Echinococcus from food producing animals in India. Veterinary Parasitology 165, 5865.Google Scholar
Pierangeli, N.B., Soriano, S.V., Roccia, I., Giménez, J., Lazzarini, L.E., Grenóvero, M.S., Menestrina, C. & Basualdo, J.A. (2007) Heterogeneous distribution of human cystic echinococcosis after a long-term control program in Neuquén, Patagonia Argentina. Parasitology International 56, 149155.Google Scholar
Ponce Gordo, F. & Cuesta Bandera, C. (1997) Echinococcus granulosus: characterization of the Spanish strains using in vitro vesicular development. Journal of Helminthology 71, 6167.Google Scholar
Rajabloo, M., Hosseini, S.H. & Jalousian, F. (2012) Morphological and molecular characterization of Echinococcus granulosus from goat isolates in Iran. Acta Tropica 123, 6771.Google Scholar
Soriano, S.V., Pierangeli, N.B., Pianciola, L.A., Mazzeo, M., Lazzarini, L.E., Saiz, M.S., Kossman, A.V., Bergagna, H.F.J., Chartier, K. & Basualdo, J.A. (2010) Molecular characterization of Echinococcus isolates indicates goats as reservoir for Echinococcus canadensis G6 genotype in Neuquén, Patagonia Argentina. Parasitology International 59, 626628.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, 369381.CrossRefGoogle ScholarPubMed
Thompson, R.C.A. (2008) The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439446.Google Scholar
Thompson, R.C.A. & Lymbery, A.J. (1988) The nature, extent and significance of variation within the genus Echinococcus. Advances in Parasitology 27, 209258.Google Scholar
Thompson, R.C.A. & McManus, D.P. (2001) Aetiology: parasites and life-cycles. pp. 119in Eckert, J., Gemmell, M.A., Meslin, F.X. & Pawlowski, Z. (Eds) WHO/OIE Manual on echinococcosis in humans and animals: a public health problem of global concern. Geneva/Paris, WHO/OIE.Google 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, 283291.CrossRefGoogle ScholarPubMed
Thompson, R.C.A., Boxel, A.C., Ralston, B.J., Constantine, C.C., Hobbs, R.P., Shury, T. & Olson, M.E. (2006) Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology 132, 439447.CrossRefGoogle ScholarPubMed
Varcasia, A., Canu, S., Kogkos, A., Pipia, A.P., Scala, A., Garippa, G. & Seimenis, A. (2007) Molecular characterization of Echinococcus granulosus in sheep and goats of Peloponnesus, Greece. Parasitology Research 101, 11351139.Google Scholar
Villalobos, N., González, L.M., Morales, J., de Aluja, A.S., Jiménez, M.I., Blanco, M.A., Harrison, L.J.S., Parkhouse, R.M.E. & Gárate, T. (2007) Molecular identification of Echinococcus granulosus genotypes (G1 and G7) isolated from pigs in Mexico. Veterinary Parasitology 147, 185189.Google Scholar
Zhang, L.H., Chai, J.J., Jiao, W., Osman, Y. & McManus, D.P. (1998) Mitochondrial genomic markers confirm the presence of the camel strain (G6 genotype) of Echinococcus granulosus in north-western China. Parasitology 116, 2933.Google Scholar