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Control of Taenia solium taeniasis/cysticercosis: past practices and new possibilities

Published online by Cambridge University Press:  15 August 2013

MARSHALL W. LIGHTOWLERS
MARSHALL W. LIGHTOWLERS*
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
*
*Corresponding author: Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia. Tel: +61 (0) 3 9731 2284. E-mail: marshall@unimelb.edu.au
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Summary

Neurocysticercosis continues to be a major health burden on humans living in many regions of the world, despite the availability of highly effective taeniacides and identification of the cause, Taenia solium, as being potentially eradicable. Several T. solium control trials have been undertaken, generally achieving limited success and none that has been fully documented has achieved what was demonstrated to be a sustainable level of disease control. Pigs act as intermediate hosts for T. solium and two new control tools have become available for application in pigs – single-dose oxfendazole treatment of porcine cysticercosis and the TSOL18 vaccine. Three potential intervention scenarios for pigs are compared for control of cysticercosis, using either oxfendazole or vaccination. A control scenario involving vaccination plus oxfendazole treatment delivered at 4 monthly intervals was predicted to achieve the best outcome, with no pigs slaughtered at 12 months of age having viable T. solium cysticerci. Now that new control tools are available, there are opportunities to concentrate research attention on evaluation of novel control scenarios leading to the implementation of effective and sustainable control programmes and a reduction in the global burden of neurocysticercosis.

Keywords

Taenia soliumneurocysticercosiscysticercosiscontrol optionsvaccinationoxfendazole
Type
Research Article
Information
Parasitology , Volume 140 , Special Issue 13: Control of cestode zoonoses in Asia: role of basic and applied science , November 2013 , pp. 1566 - 1577
Copyright
Copyright © Cambridge University Press 2013 

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References

Allan, J. C., Velasquez-Tohom, M., Fletes, C., Torres-Alvarez, R., Lopez-Virula, G., Yurrita, P., Soto De Alfaro, H., Rivera, A. and Garcia-Noval, J. (1997). Mass chemotherapy for intestinal Taenia solium infection: effect on prevalence in humans and pigs. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 595–598.CrossRefGoogle ScholarPubMed
Alvarez, L., Saumell, C., Fuse, L., Moreno, L., Ceballos, L., Domingue, G., Donadeu, M., Dungu, B. and Lanusse, C. (2013). Efficacy of a single high oxfendazole dose against gastrointestinal nematodes in naturally infected pigs. Veterinary Parasitology 194, 70–74. http://dx.doi.org/10.1016/j.vetpar.2013.01.003.CrossRefGoogle ScholarPubMed
Anonymous (1992). Update: international task force for disease eradication, 1992. Morbidity and Mortality Weekly Report 41, 691, 697–691, 698.Google Scholar
Arundel, J. H. (1972). A review of cysticercoses of sheep and cattle in Australia. Australian Veterinary Journal 48, 140–155.CrossRefGoogle ScholarPubMed
Assana, E., Kyngdon, C. T., Gauci, C. G., Geerts, S., Dorny, P., De Deken, R., Anderson, G. A., Zoli, A. P. and Lightowlers, M. W. (2010). Elimination of Taenia solium transmission to pigs in a field trial of the TSOL18 vaccine in Cameroon. International Journal for Parasitology 40, 515–519.CrossRefGoogle Scholar
Cruz, M., Davis, A., Dixon, H., Pawlowski, Z. S. and Proano, J. (1989). Operational studies on the control of Taenia solium taeniasis/cysticercosis in Ecuador. Bulletin of the World Health Organization 67, 401–407.Google ScholarPubMed
De Aluja, A. S., Martinez, M. J. and Villalobos, A. N. (1998). Taenia solium cysticercosis in young pigs: age at first infection and histological characteristics. Veterinary Parasitology 76, 71–79.CrossRefGoogle ScholarPubMed
De Aluja, A. S., Villalobos, N. M., Nava, G., Toledo, A., Martinez, J. J., Plancarte, A., Rodarte, L. F., Fragoso, G. and Sciutto, E. (2005). Therapeutic capacity of the synthetic peptide-based vaccine against Taenia solium cysticercosis in pigs. Vaccine 23, 4062–4069.CrossRefGoogle ScholarPubMed
Del Brutto, O. H. and Del Brutto, V. J. (2012). Changing pattern of neurocysticercosis in an urban endemic center (Guayaquil, Ecuador). Journal of the Neurological Sciences 315, 64–66.CrossRefGoogle Scholar
Devleesschauwer, B., Aryal, A., Tharmalingam, J., Joshi, D. D., Rijal, S., Speybroeck, N., Gabriel, S., Victor, B. and Dorny, P. (2013). Complexities in using sentinel pigs to study Taenia solium transmission dynamics under field conditions. Veterinary Parasitology 193, 172–178.CrossRefGoogle ScholarPubMed
Diaz Camacho, S. P., Candil Ruiz, A., Suate Peraza, V., Zazueta Ramos, M. L., Felix Medina, M., Lozano, R. and Willms, K. (1991). Epidemiologic study and control of Taenia solium infections with praziquantel in a rural village of Mexico. American Journal of Tropical Medicine and Hygiene 45, 522–531.CrossRefGoogle Scholar
Dorny, P., Brandt, J. and Geerts, S. (2004 a). Immunodiagnostic approaches for detecting Taenia solium. Trends in Parasitology 20, 259–260.CrossRefGoogle ScholarPubMed
Dorny, P., Phiri, I. K., Vercruysse, J., Gabriel, S., Willingham, A. L. III, Brandt, J., Victor, B., Speybroeck, N. and Berkvens, D. (2004 b). A Bayesian approach for estimating values for prevalence and diagnostic test characteristics of porcine cysticercosis. International Journal for Parasitology 34, 569–576.CrossRefGoogle ScholarPubMed
Fenwick, A., Webster, J. P., Bosque-Oliva, E., Blair, L., Fleming, F. M., Zhang, Y., Garba, A., Stothard, J. R., Gabrielli, A. F., Clements, A. C., Kabatereine, N. B., Toure, S., Dembele, R., Nyandindi, U., Mwansa, J. and Koukounari, A. (2009). The schistosomiasis control initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology 136, 1719–1730.CrossRefGoogle ScholarPubMed
Flisser, A. (2013). Epidemiology of neurocysticercosis in Mexico: from a public health problem to its control. In Novel Aspects on Cysticercosis and Neurocysticercosis (ed. Foyaca Sibat, H.), pp. 255–276. InTech, Rijeka.Google Scholar
Flisser, A. and Correa, D. (2010). Neurocysticercosis may no longer be a public health problem in Mexico. PLoS Neglected Tropical Diseases 4, e831.CrossRefGoogle ScholarPubMed
Flisser, A., Gauci, C. G., Zoli, A., Martinez-Ocana, J., Garza-Rodriguez, A., Dominguez-Alpizar, J. L., Maravilla, P., Rodriguez-Canul, R., Avila, G., Aguilar-Vega, L., Kyngdon, C., Geerts, S. and Lightowlers, M. W. (2004). Induction of protection against porcine cysticercosis by vaccination with recombinant oncosphere antigens. Infection and Immunity 72, 5292–5297.CrossRefGoogle ScholarPubMed
Garcia, H. H. and Del Brutto, O. H. (2005). Neurocysticercosis: updated concepts about an old disease. Lancet Neurology 4, 653–661.CrossRefGoogle ScholarPubMed
Garcia, H. H., Gonzalez, A. E., Evans, C. A. and Gilman, R. H. (2003). Taenia solium cysticercosis. Lancet 362, 547–556.CrossRefGoogle ScholarPubMed
Garcia, H. H., Gonzalez, A. E., Gilman, R. H., Moulton, L. H., Verastegui, M., Rodriguez, S., Gavidia, C. and Tsang, V. C. (2006). Combined human and porcine mass chemotherapy for the control of T. solium. Amercian Journal of Tropical Medicine and Hygiene 74, 850–855.CrossRefGoogle ScholarPubMed
Garcia, H. H., Gonzalez, A. E., Rodriguez, S., Gonzalvez, G., Llanos-Zavalaga, F., Tsang, V. C. and Gilman, R. H. (2010). Epidemiología y control de la cisticercosis en el Perú [Epidemiology and control of cysticercosis in Peru]. Revista Peruana de Medicina Experimental y Salud Publica 27, 592–597.CrossRefGoogle Scholar
Gauci, C. G., Jayashi, C. M., Gonzalez, A. E., Lackenby, J. and Lightowlers, M. W. (2012). Protection of pigs against Taenia solium cysticercosis by immunization with novel recombinant antigens. Vaccine 30, 3824–3828.CrossRefGoogle ScholarPubMed
Gauci, C. G., Verastegui, M. R., Gilman, R. H. and Lightowlers, M. W. (2006). Taenia solium and Taenia ovis: stage-specific expression of the vaccine antigen genes, TSOL18, TSOL16, and homologues, in oncospheres. Experimental Parasitology 113, 272–275.CrossRefGoogle ScholarPubMed
Gavidia, C. M., Verastegui, M. R., Garcia, H. H., Lopez-Urbina, T., Tsang, V. C., Pan, W., Gilman, R. H., Gonzalez, A. E. and Cysticercosis Working Group in Peru (2013). Relationship between serum antibodies and Taenia solium larvae burden in pigs raised in field conditions. PLoS Neglected Tropical Diseases 7, e2192.CrossRefGoogle ScholarPubMed
Geerts, S., Zorloni, A., Kumar, V., Brandt, J. R., De Deken, R. and Eom, K. S. (1992). Experimental infection of pigs with a Taenia species from Korea: parasitological and serological aspects. Parasitology Research 78, 513–515.CrossRefGoogle ScholarPubMed
Gilman, R. H., Gonzalez, A. E., Llanos-Zavalaga, F., Tsang, V. C. and Garcia, H. H. (2012). Prevention and control of Taenia solium taeniasis/cysticercosis in Peru. Pathogens and Global Health 106, 312–318.CrossRefGoogle ScholarPubMed
Gonzales, A. E., Garcia, H. H., Gilman, R. H., Gavidia, C. M., Tsang, V. C., Bernal, T., Falcon, N., Romero, M. and Lopez-Urbina, M. T. (1996). Effective, single-dose treatment or porcine cysticercosis with oxfendazole. American Journal of Tropical Medicine and Hygiene 54, 391–394.CrossRefGoogle ScholarPubMed
Gonzalez, A. E., Falcon, N., Gavidia, C., Garcia, H. H., Tsang, V. C., Bernal, T., Romero, M. and Gilman, R. H. (1997). Treatment of porcine cysticercosis with oxfendazole: a dose-response trial. Veterinary Record 141, 420–422.CrossRefGoogle ScholarPubMed
Gonzalez, A. E., Falcon, N., Gavidia, C., Garcia, H. H., Tsang, V. C., Bernal, T., Romero, M. and Gilman, R. H. (1998). Time-response curve of oxfendazole in the treatment of swine cysticercosis. American Journal of Tropical Medicine and Hygiene 59, 832–836.CrossRefGoogle ScholarPubMed
Gonzalez, A. E., Gauci, C. G., Barber, D., Gilman, R. H., Tsang, V. C., Garcia, H. H., Verastegui, M. and Lightowlers, M. W. (2005). Vaccination of pigs to control human neurocysticercosis. American Journal of Tropical Medicine and Hygiene 72, 837–839.CrossRefGoogle ScholarPubMed
Gonzalez, A. E., Gavidia, C., Falcon, N., Bernal, T., Verastegui, M., Garcia, H. H., Gilman, R. H. and Tsang, V. C. (2001). Protection of pigs with cysticercosis from further infections after treatment with oxfendazole. American Journal of Tropical Medicine and Hygiene 65, 15–18.CrossRefGoogle ScholarPubMed
Gonzalez, A. E., Verastegui, M., Noh, J. C., Gavidia, C., Falcon, N., Bernal, T., Garcia, H. H., Tsang, V. C., Gilman, R. H. and Wilkins, P. P. (1999). Persistence of passively transferred antibodies in porcine Taenia solium cysticercosis. Cysticercosis Working Group in Peru. Veterinary Parasitology 86, 113–118.CrossRefGoogle Scholar
Huerta, M., De Aluja, A. S., Fragoso, G., Toledo, A., Villalobos, N., Hernandez, M., Gevorkian, G., Acero, G., Diaz, 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
Iburg, T. M., Karlsson, M., Spang, F., Sikasunge, C. S. and Johansen, M. V. (2012). The effect of oxfendazole treatment on muscle pathology in pigs infected with Taenia solium cysticercosis. Veterinary Parasitology 190, 442–446.CrossRefGoogle ScholarPubMed
Jabbar, A., Verastegui, M., Lackenby, J. A., Walduck, A. K., Gauci, C. G., Gilman, R. H. and Lightowlers, M. W. (2010). Variation in the cellular localization of host-protective oncospheral antigens in Taenia saginata and Taenia solium. Parasite Immunology 32, 684–695.CrossRefGoogle ScholarPubMed
Jayashi, C. M., Kyngdon, C. T., Gauci, C. G., Gonzalez, A. E. and Lightowlers, M. W. (2012). Successful immunization of naturally reared pigs against porcine cysticercosis with a recombinant oncosphere antigen vaccine. Veterinary Parasitology 188, 261–267.CrossRefGoogle ScholarPubMed
Keilbach, N. M., De Aluja, A. S. and Sarti-Gutierrez, E. (1989). A programme to control taeniasis-cysticercosis (T. solium): experiences in a Mexican village. Acta Leidensia 57, 181–189.Google Scholar
Lawson, J. R. and Gemmell, M. A. (1983). Hydatidosis and cysticercosis: the dynamics of transmission. Advances in Parasitology 22, 261–308.CrossRefGoogle ScholarPubMed
Lightowlers, M. W. (2006). Cestode vaccines: origins, current status and future prospects. Parasitology 133, S27–S42.CrossRefGoogle ScholarPubMed
Lightowlers, M. W. (2010 a). Eradication of Taenia solium cysticercosis: a role for vaccination of pigs. International Journal for Parasitology 40, 1183–1192.CrossRefGoogle ScholarPubMed
Lightowlers, M. W. (2010 b). Fact or hypothesis: Taenia crassiceps as a model for Taenia solium, and the S3Pvac vaccine. Parasite Immunology 32, 701–709.CrossRefGoogle ScholarPubMed
Manoutcharian, K., Rosas, G., Hernandez, M., Fragoso, G., Aluja, A., Villalobos, N., Rodarte, L. F. and Sciutto, E. (1996). Cysticercosis: identification and cloning of protective recombinant antigens. Journal of Parasitology 82, 250–254.CrossRefGoogle ScholarPubMed
Molinari, J. L., Soto, R., Tato, P., Rodriguez, D., Retana, A., Sepulveda, J. and Palet, A. (1993). Immunization against porcine cysticercosis in an endemic area in Mexico: a field and laboratory study. American Journal of Tropical Medicine and Hygiene 49, 502–512.CrossRefGoogle Scholar
Molinari, J. L., Rodriguez, D., Tato, P., Soto, R., Arechavaleta, F. and Solano, S. (1997). Field trial for reducing porcine Taenia solium cysticercosis in Mexico by systematic vaccination of pigs. Veterinary Parasitology 69, 55–63.CrossRefGoogle ScholarPubMed
Morales, J., Martinez, J. J., Manoutcharian, K., Hernandez, M., Fleury, A., Gevorkian, G., Acero, G., Blancas, A., Toledo, A., Cervantes, J., Maza, V., Quet, F., Bonnabau, H., De Aluja, A. S., Fragoso, G., Larralde, C. and Sciutto, E. (2008). Inexpensive anti-cysticercosis vaccine: S3Pvac expressed in heat inactivated M13 filamentous phage proves effective against naturally acquired Taenia solium porcine cysticercosis. Vaccine 26, 2899–2905.CrossRefGoogle ScholarPubMed
Moreno, L., Lopez-Urbina, M. T., Farias, C., Domingue, G., Donadeu, M., Dungu, B., Garcia, H. H., Gomez-Puerta, L. A., Lanusse, C. and Gonzalez, A. E. (2012). A high oxfendazole dose to control porcine cysticercosis: pharmacokinetics and tissue residue profiles. Food and Chemical Toxicology 50, 3819–3825.CrossRefGoogle ScholarPubMed
Ngowi, H. A., Carabin, H., Kassuku, A. A., Mlozi, M. R., Mlangwa, J. E. and Willingham, A. L. III (2008). A health-education intervention trial to reduce porcine cysticercosis in Mbulu District, Tanzania. Preventive Veterinary Medicine 85, 52–67.CrossRefGoogle ScholarPubMed
Ngowi, H. A., Mlangwa, J. E. D., Mlozi, M. R. S., Tolma, E. L., Kassuku, A. A., Carabin, H. and Willingham, A. L. III (2009). Implementation and evaluation of a health-promotion strategy for control of Taenia solium infections in northern Tanzania. International Journal of Health Promotion and Education 47, 24–34.CrossRefGoogle Scholar
Pawlowski, Z., Allan, J. and Sarti, E. (2005). Control of Taenia solium taeniasis/cysticercosis: from research towards implementation. International Journal for Parasitology 35, 1221–1232.CrossRefGoogle ScholarPubMed
Pondja, A., Neves, L., Mlangwa, J., Afonso, S., Fafetine, J., Willingham, A. L. III, Thamsborg, S. M. and Johansen, M. V. (2012). Use of oxfendazole to control porcine cysticercosis in a high-endemic area of Mozambique. PLoS Neglected Tropical Diseases 6, e1651.CrossRefGoogle Scholar
Sarti, E. (2002). Epidemiology of Taenia solium taeniasis and cysticercosis in Mexico. In Taenia solium Cysticercosis from Basic to Clinical Science (ed. Singh, G. and Prabhakar, S.), pp. 83–90. CABI Publishing, Wallingford.CrossRefGoogle Scholar
Sarti, E., Flisser, A., Schantz, P. M., 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.CrossRefGoogle Scholar
Sarti, E., Schantz, P. M., Avila, G., Ambrosio, J., Medina-Santillan, 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 of Tropical Medicine and Hygiene 94, 85–89.CrossRefGoogle ScholarPubMed
Sarti Gutierrez, E. J., Schantz, P. M., Lara Aguilera, R., Gomez Dandoy, H. and Flisser, A. (1988). Taenia solium taeniasis and cysticercosis in a Mexican village. Tropical Medicine andParasitology 39, 194–198.Google Scholar
Schantz, P. (2002). Taenia solium cysticercosis: an overview of global distribution and transmission. In Taenia solium Cysticercosis from Basic to Clinical Science (ed. Singh, G. and Prabhakar, S.), pp. 63–73. CABI Publishing, Wallingford.CrossRefGoogle Scholar
Schantz, P. M., Cruz, M., Sarti, E. and Pawlowski, Z. (1993). Potential eradicability of taeniasis and cysticercosis. Bulletin of the Pan American Health Organization 27, 397–403.Google ScholarPubMed
Schantz, P. M., Moore, A. C., Munoz, 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
Sciutto, E., Morales, J., Martinez, J. J., Toledo, A., Villalobos, M. N., Cruz-Revilla, C., Meneses, G., Hernandez, M., Diaz, A., Rodarte, L. F., Acero, G., Gevorkian, G., Manoutcharian, K., Paniagua, J., Fragoso, G., Fleury, A., Larralde, R., De Aluja, A. S. and Larralde, C. (2007). Further evaluation of the synthetic peptide vaccine S3Pvac against Taenia solium cysticercosis in pigs in an endemic town of Mexico. Parasitology 134, 129–133.CrossRefGoogle Scholar
Sikasunge, C. S., Johansen, M. V., Willingham, A. L. III, Leifsson, P. S. and Phiri, I. K. (2008). Taenia solium porcine cysticercosis: viability of cysticerci and persistency of antibodies and cysticercal antigens after treatment with oxfendazole. Veterinary Parasitology 158, 57–66.CrossRefGoogle ScholarPubMed
Tsang, V. C., Pilcher, J. A., Zhou, W., Boyer, A. E., Kamango Sollo, E. I., Rhoads, M. L., Murrell, K. D., Schantz, P. M. and Gilman, R. H. (1991). Efficacy of the immunoblot assay for cysticercosis in pigs and modulated expression of distinct IgM/IgG activities to Taenia solium antigens in experimental infections. Veterinary Immunology and Immunopathology 29, 69–78.CrossRefGoogle ScholarPubMed
Willingham, A. L. III and Engels, D. (2006). Control of Taenia solium cysticercosis/taeniosis. Advances in Parasitology 61, 509–566.CrossRefGoogle ScholarPubMed
World Health Organisation (2010). Working to Overcome the Global Impact of Neglected Tropical Diseases, World Health Organisation. WHO/HTM/NTD/2010.1, Geneva.Google Scholar
Yoshino, K. (1933). Studies on the postembryonal development of Taenia solium. Pt. II. On the youngest form of Cysticercus cellulosae and on the migratory course of the oncosphaera of Taenia solium within the intermediate host. Taiwan Igakkai Zasshi (Journal of the Medical Association of Formosa) 32, 155–158.Google Scholar
Yoshino, K. (1934). On the subjective symptoms caused by the parasitism of Taenia solium and its development in man. Taiwan Igakkai Zasshi (Journal of the Medical Association of Formosa) 33, 183–194, 115.Google Scholar