Taenia solium: Current understanding of laboratory animal models of taeniosis

Parasitology

Volumn 137, Issue 3, 2010, Pages 347-357

  Flisser, A ^a   Avila G ^a   Maravilla, P ^b   Mendlovic, F ^a,c   Leon Cabrera S ^a   Cruz Rivera, M ^a   Garza, A ^b   Gomez B ^b   Aguilar, L ^a   Teran N ^a   Velasco, S ^a   Benitez M ^a   Jimenez Gonzalez, D E ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b Hospital General dr Manuel Gea González Secretaría de Salud   (United States)

^c UNIVERSIDAD ANÁHUAC   (Mexico)

Author keywords

Chinchillas; Cysticercosis; Cytokines; Experimental models; Gerbils; Hamsters; Immune response; Inflammatory cells; Intestinal mucosa; Taenia solium; Taeniosis; Vaccines

Indexed keywords

CALRETICULIN;

EXPERIMENTAL INFECTION; GERBIL; HAMSTER; HISTOPATHOLOGY; HOST PARASITE INTERACTION; HOST RESISTANCE; HUMORAL IMMUNITY; INFLAMMATION; INTESTINE MUCOSA; NONHUMAN; PARASITE SURVIVAL; PRIORITY JOURNAL; RABBIT; REVIEW; TAENIA SOLIUM; TAENIASIS; TH1 CELL; TH2 CELL;

ANIMALS; DISEASE MODELS, ANIMAL; FECES; HOST-PARASITE INTERACTIONS; HUMANS; TAENIA SOLIUM; TAENIASIS;

ANIMALIA; CANIS FAMILIARIS; CESTODA; CHINCHILLIDAE; CRICETINAE; GERBILLINAE; MACACA; MAMMALIA; ORYCTOLAGUS CUNICULUS; RODENTIA; SUIDAE; TAENIA SOLIUM;

EID: 77949593477     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182010000272     Document Type: Review

References (60)

1. 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.
2. 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.
3. 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.
4. Allan, J. C., Wilkins, P. P., Tsang, V. C. W. and Craig, P. S. (2003). Immunodiagnostic tools for taeniosis. Acta Tropica 87, 87-93.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. Flisser, A. (1988). Neurocysticercosis in Mexico. Parasitology Today 4, 131-137.
19. Flisser, A. and Gyorkos, T. (2007). Contribution of immunodiagnostic tests to epidemiological/intervention studies of cysticercosis/taeniosis in Mexico. Parasite Immunology 29, 637-649.
20. 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.
21. 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). Hyperendemic human and porcine Taenia solium infection in Perú. American Journal of Tropical Medicine and Hygiene 68, 268-275.
22. Garcia, H. H., Gonzalez, A. E., Evans, C. A., Gilman, R. H. and The Cysticercosis Working Group in Peru. (2003). Taenia solium cysticercosis. Lancet 362, 547-556.
23. 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.
24. Gnezdilov, V. G. (1957). The golden hamster (Mesocricetus auratus Watherhouse) as potential definitive host of tapeworm Taenia solium. Zollogicheski Zhurnal 36, 1770-1773.
25. 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.
26. 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.
27. 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.
28. 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.
29. Kamiya, M. and Sato, H. (1990). Complete life cycle of the canid tapeworm, Echinococcus multilocularis, in laboratory rodents. FASEB Journal 4, 3334-3339.
30. Kamiya, M. and Sato, H. (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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. Onah, D. N. and Nawa, Y. (2000). Mucosal immunity against parasitic gastrointestinal nematodos. Korean Journal of Parasitology 38, 209-236.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. Sarti, E., Schantz, P. M., Avila, G., Ambrosio, J., Medina- Santillá n, 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.
49. 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.
50. 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.
51. Spady, D., Cuthbert, J. A., Willard, M. N. and Meidell, R. S. (1996). Feedback regulation of hepatic 7-hydroxylase expression by bile salts in the hamster. Journal of Biological Chemistry 271, 18623-18631.
52. 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.
53. Torgerson, P. R. (2009). Dogs, vaccines and Echinococcus. Trends in Parasitology 25, 57-58.
54. 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.
55. 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.
56. 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.
57. Verster, A. (1974). The golden hamster as a definitive host of Taenia solium and Taenia saginata. Onderspoort Journal of Veterinary Research 41, 23-28.
58. 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.
59. 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.
60. 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.