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Taenia solium: current understanding of laboratory animal models of taeniosis

Published online by Cambridge University Press:  01 March 2010

A. FLISSER ,
G. ÁVILA ,
P. MARAVILLA ,
F. MENDLOVIC ,
S. LEÓN-CABRERA ,
M. CRUZ-RIVERA ,
A. GARZA ,
B. GÓMEZ ,
L. AGUILAR  and
N. TERÁN
...Show all authors
A. FLISSER*
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
G. ÁVILA
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
P. MARAVILLA
Affiliation:
Departamento de Ecología de Agentes Patógenos, Hospital General “Dr. Manuel Gea González” Secretaría de Salud, Calzada de Tlalpan 4800, México14080 DF.
F. MENDLOVIC
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF. Escuela de Ciencias de la Salud, Universidad Anáhuac, México Norte, Av. Universidad Anáhuac 46, Huixquilucan, 52786. Estado de México
S. LEÓN-CABRERA
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
M. CRUZ-RIVERA
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
A. GARZA
Affiliation:
Departamento de Ecología de Agentes Patógenos, Hospital General “Dr. Manuel Gea González” Secretaría de Salud, Calzada de Tlalpan 4800, México14080 DF.
B. GÓMEZ
Affiliation:
Departamento de Ecología de Agentes Patógenos, Hospital General “Dr. Manuel Gea González” Secretaría de Salud, Calzada de Tlalpan 4800, México14080 DF.
L. AGUILAR
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
N. TERÁN
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
S. VELASCO
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
M. BENÍTEZ
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF.
D. E. JIMENEZ-GONZALEZ
Affiliation:
Departamento de Ecología de Agentes Patógenos, Hospital General “Dr. Manuel Gea González” Secretaría de Salud, Calzada de Tlalpan 4800, México14080 DF.
*
*Corresponding author. Ana Flisser, Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Av. Universidad 3000, México04510 DF, telephone: 5255-56232466, fax: 5255-56232382, e-mail: flisser@servidor.unam.mx
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Summary

Neurocysticercosis is a public health problem in many developing countries and is the most frequent parasitic disease of the brain. The human tapeworm carrier is the main risk factor for acquiring neurocysticercosis. Since the parasite lodges only in the human intestine, experimental models of Taenia solium taeniosis have been explored. Macaques, pigs, dogs, cats and rabbits are unsuccessful hosts even in immunodepressed status. By contrast, rodents are adequate hosts since tapeworms with mature, pregravid and, in some cases, gravid proglottids develop after infection. In this review, information that has been generated with experimental models of taeniosis due to T. solium is discussed. Initially, the use of the model for immunodiagnosis of human taeniosis and evaluation of intervention measures is summarized. Next, descriptions of tapeworms and comparison of hamsters, gerbils and other mammals as experimental models are discussed, as well as data on the humoral immune response, the inflammatory reaction and the production of cytokines associated to Th1 and Th2 responses in the intestinal mucosa. Finally, evaluation of protection induced against the development of tapeworms by recombinant T. solium calreticulin in hamsters is summarized and compared to other studies.

Keywords

Chinchillascysticercosiscytokinesexperimental modelsgerbilshamstersimmune responseinflammatory cellsintestinal mucosaTaenia soliumtaeniosisvaccines
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 347 - 357
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Allan, J. C., Avila, G., García-Noval, J., Flisser, A. and Craig, P. S. (1990). Immunodiagnosis of taeniasis by coproantigen detection. Parasitology 101, 473–477.CrossRefGoogle ScholarPubMed
Allan, J. C., García-Domínguez, G., Craig, P. S., Rogan, M. T., Lowe, B. S. and Flisser, A. (1991). Sexual development of Taenia solium in hamsters. Annals in Tropical Medicine and Parasitology 85, 572–576.Google Scholar
Allan, J. C., Velasquez-Tohom, M., Torres-Alvarez, R., Yurrita, P. and García-Noval, J. (1996). Field trial of the coproantigen-based diagnosis of Taenia solium taeniasis by enzyme-linked immunosorbent assay. American Journal of Tropical Medicine and Hygiene 54, 352–356.Google Scholar
Allan, J. C., Wilkins, P. P., Tsang, V. C. W. and Craig, P. S. (2003). Immunodiagnostic tools for taeniosis. Acta Tropica 87, 87–93.Google Scholar
Aluja, A. S., Nuñez, J. F. and Villalobos, A. N. M. (1993). Efecto de la irradiación gamma Co60 sobre el metacestodo de Taenia solium. Veterinaria Mexico 24, 297–301.Google Scholar
Andersen, K. (1978). The development of the tapeworm Diphyllobothrium latum (L. 1756) (Cestoda; Pseudophyllidea) in its definitive hosts, with special references to the growth patterns of D. dendriticum (Nitzsch, 1824) and D. ditremum (Creplin, 1827). Parasitology 77, 111–120.Google Scholar
Anthony, R. M., Rutitzky, L. I., Urban, J. F. Jr, Stadecker, M. J. and Gause, W. C. (2007). Protective immune mechanisms in helminth infection. Nature Reviews in Immunology 7, 975–987.CrossRefGoogle ScholarPubMed
Avila, G., Aguilar, L., Benitez, S., Yepez-Mulia, L., Lavenat, I. and Flisser, A. (2002). Inflammatory response in the intestinal mucosa of gerbils and hamsters experimentally infected with the adult stage of Taenia solium. International Journal for Parasitology 32, 1301–1308.Google Scholar
Avila, G., Aguilar, L., Romero-Valdovinos, M., Garcia-Vasquez, F. and Flisser, A. (2008). Cytokine response in the intestinal mucosa of hamsters infected with Taenia solium. Animal Biodiversity and Emerging Diseases. Annals of the New York Academy of Sciences 1149, 170–173.CrossRefGoogle Scholar
Avila, G., Benitez, M., Aguilar, L. and Flisser, A. (2003). Kinetics of Taenia solium antibodies and antigens in experimental taeniosis. Parasitology Research 89, 284–289.CrossRefGoogle ScholarPubMed
Avila, G., Teran, N., Aguilar, L., Maravilla, P., Mata, P. and Flisser, A. (2006). Laboratory animal models for human Taenia solium. Parasitology International 55, S127–S130.Google Scholar
Buckwell, T. (1999). Classification of rodent suffering due to immunodepression. In Ethics, Animals and Science. (ed. Dolan, K.). Blackwell Science, Great Britain, 1999; p. 160.Google Scholar
Cadigan, F., Santon, J. S., Tanticharoenyus, P. and Chaicumpa, V. (1967). The Lar gibbon as definitive and intermediate host of Taenia solium. Journal of Parasitology 53, 844.Google Scholar
Conchedda, M., Gabriele, F. and Bortoletti, G. (2006). Development and sexual maturation of Echinococcus granulosus adult worms in the alternative definitive host, Mongolian gerbil (Meriones unguiculatus). Acta Tropica 97, 119–125.Google Scholar
Cruz-Revilla, C., Toledo, A., Rosas, G., Huerta, M., Flores-Perez, I., Peña, N., Morales, J., Cisneros-Quiñones, J., Meneses, G., Díaz-Orea, A., Anciart, N., Goldbaum, F., Aluja, A., Larralde, C., Fragoso, G. and Sciutto, E. (2006). Effective protection against experimental Taenia solium tapeworm infection in hamsters by primo-infection and by vaccination with recombinant or synthetic heterologous antigens. Journal of Parasitology 92, 864–867.Google Scholar
El Gengehi, N., El Ridi, R., Tawab, N. A., El Demellawy, M. and Mangold, B. L. (2000). A Schistosoma mansoni 62-kDa band is identified as an irradiated vaccines T-cell antigen and characterized as calreticulin. Journal of Parasitology 86, 993–1000.Google Scholar
Fleury, A., Flisser, A., Flores-Rivera, J. and Corona, T. (2009). Parasitic infections. 13. Taenia solium. In Post-Infectious Sequelae and Long-Term Consequences of Infectious Diseases. (ed. Smith, J. L., Brogden, K. A. and Fratamico, P.), pp. 229–243. American Society for Microbiology Press, USA.Google Scholar
Flisser, A. (1988). Neurocysticercosis in Mexico. Parasitology Today 4, 131–137.Google Scholar
Flisser, A. and Gyorkos, T. (2007). Contribution of immunodiagnostic tests to epidemiological/intervention studies of cysticercosis/taeniosis in Mexico. Parasite Immunology 29, 637–649.Google Scholar
Flores-Perez, I., Fragoso-Gonzalez, G., Sciutto, E. and de Aluja, A. S. (2003). Apoptosis induced by gamma irradiation of Taenia solium metacestodes. Parasitology Research 90, 203–208.Google Scholar
Garcia, H. H., Gilman, R. H., Gonzalez, A. E., Verastegui, M., Rodriguez, S., Gaviria, C., Tsang, V. C., Falcon, N., Lescano, A. G., Moulton, L. H., Bernal, T., Tovar, M. and The Cysticercosis Working Group in Peru. (2003 b). Hyperendemic human and porcine Taenia solium infection in Perú. American Journal of Tropical Medicine and Hygiene 68, 268–275.Google Scholar
Garcia, H. H., Gonzalez, A. E., Evans, C. A., Gilman, R. H. and The Cysticercosis Working Group in Peru. (2003 a). Taenia solium cysticercosis. Lancet 362, 547–556.Google Scholar
Garza-Rodriguez, A., Maravilla, P., Mendlovic, F., Mata-Miranda, P., Robert, L. and Flisser, A. (2007). Lack of postmortem digestion of tapeworms in golden hamsters experimentally infected with Taenia solium. Veterinary Parasitology 145, 172–175.Google Scholar
Gnezdilov, V. G. (1957). The golden hamster (Mesocricetus auratus Watherhouse) as potential definitive host of tapeworm Taenia solium. Zollogicheski Zhurnal 36, 1770–1773.Google Scholar
Guezala, M. C., Rodriguez, S., Zamora, H., Garcia, H. H., Gonzalez, A. E., Tembo, A., Allan, J. C. and Craig, P. S. (2009). Development of a species-specific coproantigen ELISA for human Taenia solium taeniasis. American Journal of Tropical Medicine and Hygiene 81, 433–437.CrossRefGoogle ScholarPubMed
Guillou, F., Roger, E., Mone, Y., Rognon, A., Grunau, C., Theron, A., Mitta, G., Coustau, C. and Gourbal, B. E. (2007). Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Molecular Biochemistry and Parasitology 155, 45–56.Google Scholar
Herd, R. P., Chappel, R. J. and Biddell, D. (1975). Immunization of dogs against Echinococcus granulosus using worm secretory antigens. International Journal for Parasitology 5, 395–399.CrossRefGoogle ScholarPubMed
Huerta, M., de Aluja, A. S., Fragoso, G., Toledo, A., Villalobos, N., Hernandez, M., Gevorkian, G., Acero, G., Díaz, A., Alvarez, I., Avila, R., Beltran, C., Garcia, G., Martinez, J. J., Larralde, C. and Sciutto, E. (2001). Synthetic peptide vaccine against Taenia solium pig cysticercosis: successful vaccination in a controlled field trial in rural Mexico. Vaccine 20, 262–266.CrossRefGoogle Scholar
Kamiya, M. and Sato, H. (1990 a). Complete life cycle of the canid tapeworm, Echinococcus multilocularis, in laboratory rodents. FASEB Journal 4, 3334–3339.Google Scholar
Kamiya, M. and Sato, H. (1990 b). Establishment, development and fecundity of Taenia crassiceps in the intestine of prednisolone-treated Mongolian gerbils and inbred mice. Journal of Helminthology 64, 217–222.Google Scholar
Kasper, G., Brown, A., Eberl, M., Vallar, L., Kieffer, N., Berry, C., Girdwood, K., Eggleton, P., Quinnell, R. and Pritchard, D. I. (2001). A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signalling domains of some integrins. Parasite Immunology 23, 141–152.Google Scholar
Leon-Cabrera, S., Cruz-Rivera, M., Mendlovic, F., Avila-Ramírez, G., Carrero, J. C., Laclette, J. P. and Flisser, A. (2009). Standardization of an experimental model of human taeniosis for oral vaccination. Methods 49, 346–350.CrossRefGoogle ScholarPubMed
Maravilla, P., Avila, G., Cabrera, V., Aguilar, L. and Flisser, A. (1998). Comparative development of Taenia solium in experimental models. Journal of Parasitology 84, 882–886.Google Scholar
Marcelain, K., Colombo, A., Molina, M. C., Ferreira, L., Lorca, M., Aguillon, J. C. and Ferreira, A. (2000). Development of an immunoenzymatic assay for the detection of human antibodies against Trypanosoma cruzi calreticulin, an immunodominant antigen. Acta Tropica 75, 291–300.CrossRefGoogle ScholarPubMed
Mendlovic, F., Carrillo-Farga, J., Torres, J., Laclette, J. P. and Flisser, A. (2006). Differential expression of calreticulin in developmental stages of Taenia solium. Journal of Parasitology 92, 789–795.Google Scholar
Mendlovic, F., Ostoa-Saloma, P., Solis, C., Martínez Ocaña, J., Flisser, A. and Laclette, J. P. (2004). Cloning, characterization and functional expresión of Taenia solium calreticulin. Journal of Parasitology 80, 891–893.Google Scholar
Merchant, M. T., Aguilar, L., Avila, G., Robert, L., Flisser, A. and Willms, K. (1998). Taenia solium: Description of the intestinal implantation sites in experimental hamster infections. Journal of Parasitology 84, 681–685.Google Scholar
Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K. and Opas, M. (1999). Calreticulin: One protein, one gene, many functions. Biochemical Journal 344, 281–292.Google Scholar
Monroy-Ostria, A., Monroy-Ostria, T. J., Gomez, G. J. and Hernandez, M. O. (1993). Some studies on the experimental infection of golden hamsters with Taenia solium. Revista Latinoamericana de Microbiologia 35, 91–98.Google Scholar
Morgan, C., LaCourse, E. J., Rushbrook, B. J., Greetham, D., Hamilton, J. V., Barrett, J., Bailey, K. and Brophy, P. M. (2006). Plasticity demonstrated in the proteome of a parasitic nematode within the intestine of different host strains. Proteomics 6, 4633–4645.Google Scholar
Onah, D. N. and Nawa, Y. (2000). Mucosal immunity against parasitic gastrointestinal nematodos. Korean Journal of Parasitology 38, 209–236.Google Scholar
Pathak, K. and Gaur, S. (1985). Effect of immunosuppressants and antihistaminics on the development of Taenia solium in golden hamsters. Indian Journal of Veterinary Medicine 5, 10–12.Google Scholar
Petavy, A. F., Hormaeche, C., Lahmar, S., Ouhelli, H., Chabalgoity, A., Marchal, T., Azzouz, S., Schreiber, F., Alvite, G., Sarciron, M. E., Maskell, D., Esteves, A. and Bosquet, G. (2008). An oral recombinant vaccine in dogs against Echinococcus granulosus, the causative agent of human hydatid disease: a pilot study. PLoS Neglected Tropical Diseases 2, 1e125.Google Scholar
Restrepo, B. I., Alvarez, J. I., Castaño, J. A., Arias, L. F., Restrepo, M., Trujillo, J., Colegial, C. H. and Teale, J. M. (2001). Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infection and Immunity 69, 4554–4560.Google Scholar
Rokeach, L. A., Zimmerman, P. A. and Unnasch, T. R. (1994). Epitopes of the Onchocerca volvulus RAL1 antigen, a member of the calreticulin family of proteins, recognized by sera from patients with onchocerciasis. Infection and Immunity 62, 3696–3704.Google Scholar
Rzepecka, J., Rausch, S., Klotz, C., Schnöller, C., Kornprobst, T., Hagen, J., Ignatius, R., Lucius, R. and Hartmann, S. (2009). Calreticulin from the intestinal nematode Heligmosomoides polygyrus is a Th2-skewing protein and interacts with murine scavenger receptor-A. Molecular Immunology 46, 1109–1119.CrossRefGoogle ScholarPubMed
Sarti, E., Flisser, A., Schantz, P., Gleizer, M., Loya, M., Plancarte, A., Avila, G., Allan, J., Craig, P., Bronfman, M. and Wijeyaratne, P. (1997). Development and evaluation of a health education intervention against Taenia solium in a rural community in Mexico. American Journal of Tropical Medicine and Hygiene 56, 127–132.Google Scholar
Sarti, E., Schantz, P. M., Avila, G., Ambrosio, J., Medina-Santillán, R. and Flisser, A. (2000). Mass treatment against human taeniasis for the control of cysticercosis: a population-based intervention study. Transactions of the Royal Society for Tropical Medicine and Hygiene 94, 85–89.Google Scholar
Sato, H. and Kamiya, M. (1990). Establishment, development and fecundity of Taenia crassiceps in the intestine of prednisolone-treated Mongolian gerbils and inbred mice. Journal of Helminthology 64, 217–222.Google Scholar
Schantz, P. M., Moore, A. C., Muñoz, J. L., Hartman, B. J., Schaefer, J. A., Aron, A. M., Persaud, D., Sarti, E., Wilson, M. and Flisser, A. (1992). Neurocysticercosis in an orthodox Jewish community in New York City. New England Journal of Medicine 327, 692–695.CrossRefGoogle Scholar
Spady, D., Cuthbert, J. A., Willard, M. N. and Meidell, R. S. (1996). Feedback regulation of hepatic 7a-hydroxylase expression by bile salts in the hamster. Journal of Biological Chemistry 271, 18623–18631.Google Scholar
Suchitra, S. and Joshi, P. (2005). Characterization of Haemonchus contortus calreticulin suggests its role in feeding and immune evasion by the parasite. Biochimica et Biophysica Acta 1722, 293–303.Google Scholar
Torgerson, P. R. (2009). Dogs, vaccines and Echinococcus. Trends in Parasitology 25, 57–58.Google Scholar
Varma, T. K. and Ahluwalia, S. S. (1992). Development of Taenia solium Linnaeus, 1758 in golden hamsters. Indian Journal of Animal Science 62, 48–49.Google Scholar
Verastegui, M., Gilman, R. H., Garcia, H. H., Gonzalez, A. E., Arana, Y., Jeri, C., Tuero, I., Gavidia, C. M., Levine, M., Tsang, V. C. and The Cysticercosis Working Group in Peru. (2003). Prevalence of antibodies to unique Taenia solium oncosphere antigens in taeniasis and human and porcine cysticercosis. American Journal of Tropical Medicine and Hygiene 69, 438–444.Google Scholar
Verster, A. (1971). Preliminary report on the golden hamster as a definitive host of Taenia solium Linneus, 1758 and Taenia saginata Goeze, 1782. Onderspoort Journal of Veterinary Research 38, 63–64.Google Scholar
Verster, A. (1974). The golden hamster as a definitive host of Taenia solium and Taenia saginata. Onderspoort Journal of Veterinary Research 41, 23–28.Google Scholar
Villagran-Uribe, J. and Olvera-Rabiela, J. E. (1989). La cisticercosis en el material de autopsia del Hospital General de México. In Cisticercosis Humana y Porcina. Su Conocimiento e Investigación en México. (ed. Flisser, A. and Malagón, F.), Limusa Noriega y CONACYT, México DF, pp. 97–105.Google Scholar
Wilkins, P. P., Allan, J. C., Verastegui, M., Acosta, M., Eason, A. G., Garcia, H. H., Gonzalez, A. E., Gilman, R. H. and Tsang, V. C. W. (1999). Development of a serologic assay to detect Taenia solium taeniasis. American Journal of Tropical Medicine and Hygiene 60, 199–204.Google Scholar
Winter, J. A., Davies, O. R., Brown, A. P., Garnett, M. C., Stolnik, S. and Pritchard, D. I. (2005). The assessment of hookworm calreticulin as a potential vaccine for necatoriasis. Parasite Immunology 27, 139–146.Google Scholar