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Distribution and histopathological changes induced by cysts of Taenia solium in the brain of pigs from Tanzania

Published online by Cambridge University Press:  06 June 2014

E.M. Mkupasi ,
H.A. Ngowi ,
C.S. Sikasunge ,
P.S. Leifsson  and
M.V. Johansen
E.M. Mkupasi*
Affiliation:
Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Thorvaldsensvej 57, 1871Frederiksberg C, Denmark
H.A. Ngowi
Affiliation:
Department of Veterinary Medicine and Public Health, Sokoine University of Agriculture, PO Box 3021, Morogoro, Tanzania
C.S. Sikasunge
Affiliation:
Department of Para-clinical Studies, School of Veterinary Medicine, University of Zambia, PO Box 32379, Lusaka, Zambia
P.S. Leifsson
Affiliation:
Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Thorvaldsensvej 57, 1871Frederiksberg C, Denmark
M.V. Johansen
Affiliation:
Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Thorvaldsensvej 57, 1871Frederiksberg C, Denmark
*
*E-mail: emkupasi@yahoo.com
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Abstract

Neurocysticercosis (NCC) caused by Taenia solium cysts is a frequent but neglected parasitic disease of the central nervous system (CNS) worldwide. The aim of this study was to describe anatomical locations of cysts in the CNS and the corresponding inflammation. A total of 17 naturally infected pigs were used to evaluate the distribution of cysts and, of these, seven were used to evaluate the corresponding inflammation further, through histopathology. Clinical signs in the pigs included dullness, sluggishness, somnolence, apathy and loss of consciousness. Cysts were distributed in all cerebral lobes, i.e. 39.7% in the frontal lobe, 20.3% in the parietal lobe, 20.0% in the occipital lobe and 19.7% in the temporal lobe, and only 0.4% in the cerebellum. No cysts were found in the spinal cord. Cysts were localized as follows: 47.9% in the dorsal subarachnoid, 46.9% in the parenchyma, 4.4% in the subarachnoid base and 0.9% in the ventricles. The results of the histopathology revealed lesions in an early inflammatory stage, i.e. stage I, in all anatomical locations except for two, which showed more of an inflammatory reaction, stage III, in one pig. It was concluded that clinical signs in pigs were neither pathognomonic nor consistent. These signs, therefore, cannot be used as a reliable indicator of porcine NCC. Furthermore, T. solium cysts were found to be in abundance in all cerebral lobes, and only a few were found in the cerebellum. Regarding the inflammatory response, no significant differences were found in the location and total number of cysts. Thus, further studies are needed to explain the determinants of cyst distribution in the CNS and assess in detail clinical signs associated with porcine NCC.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 5 , September 2015 , pp. 559 - 564
Copyright
Copyright © Cambridge University Press 2014 

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References

Agerholm, J.S. (2011) Necropsy of the brain and spinal cord. pp. 157–177in Jensen, H.E. (Ed.) Necropsy – a handbook and atlas. Frederiksberg, Biofolia Press.Google Scholar
Bandres, J.C., White, A.C., Samo, T., Murphy, E.C. & Harris, R.L. (1992) Extraparenchymal neurocysticercosis: report of five cases and review of management. Clinical Infectious Diseases 15, 799–811.CrossRefGoogle ScholarPubMed
Cardona, A.E., Restrepo, B.I., Jaramillo, J.M. & Teale, J.M. (1999) Development of an animal model for neurocysticercosis: immune response in the central nervous system is characterized by a predominance of gamma delta T cells. Journal of Immunology 162, 995–1002.CrossRefGoogle ScholarPubMed
Carpio, A. (2002) Neurocysticercosis: an update. Lancet Infectious Diseases 2, 751–762.CrossRefGoogle ScholarPubMed
Chavarria, A., Fleury, A., Garcia, E., Marquez, C., Fragoso, G. & Sciutto, E. (2005) Relationship between the clinical heterogeneity of neurocysticercosis and the immune-inflammatory profiles. Clinical Immunology 116, 271–278.CrossRefGoogle ScholarPubMed
De Aluja, A. & Vargas, G. (1988) The histopathology of porcine cysticercosis. Veterinary Parasitology 28, 65–77.CrossRefGoogle ScholarPubMed
De Aluja, A., Gonzalez, D., Carbajal, J.R. & Flisser, A. (1989) Histological description of tomographic images of Taenia solium cysticerci in pig brains. Clinical Imaging 13, 292–298.CrossRefGoogle ScholarPubMed
De Aluja, A.S., Martinez, J.J.M. & Villalobos, A.N.M. (1998) Taenia solium cysticercosis in young pigs: age at first infections and histological characteristics. Veterinary Parasitology 76, 71–79.CrossRefGoogle ScholarPubMed
Del Brutto, O.H. (2012) Neurocysticercosis. A review. Scientific World Journal doi: 101100/2012/159821.CrossRefGoogle ScholarPubMed
Fleury, A., Dessein, A., Preux, P.M., Dumas, M., Tapia, G., Larralde, C. & Sciutto, E. (2004) Symptomatic human neurocysticercosis: age, sex and exposure factors relating with disease heterogeneity. Journal of Neurology 251, 830–837.CrossRefGoogle ScholarPubMed
Fleury, A., Morales, J., Bobes, R.J., Dumas, M., Yánez, O., Piña, J., Carrillo-Mezo, R., Martínez, J.J., Fragoso, G., Dessein, A., Larralde, C. & Sciutto, E. (2006) An epidemiological study of familial neurocysticercosis in an endemic Mexican community. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 551–558.CrossRefGoogle Scholar
Fleury, A., Escobar, A., Fragoso, G., Sciutto, E. & Larralde, C. (2010) Clinical heterogeneity of human neurocysticercosis results from complex interactions among parasite, host and environmental factors. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 243–250.CrossRefGoogle ScholarPubMed
Garcia, H.H., Evans, C.A.W., Nash, T.E., Takanayagui, O.M., White, A.C., Botero, D., Rajshekhar, V., Tsang, V.C., Schantz, P.M., Allan, J.C., Flisser, A., Correa, D., Sarti, E., Friedland, J.S., Martinez, S.M., Gonzalez, A.E., Gilman, R.H. & Del Brutto, O.H. (2002) Current consensus guidelines for treatment of neurocysticercosis. Clinical Microbiology Reviews 15, 747–756.CrossRefGoogle ScholarPubMed
Garcia, H.H., Gilman, R.H., Gonzalez, A.E., Verastegui, M., Rodriguez, S., Gavidia, C., Tsang, C.V.W., Falcon, N., Lescano, A.G., Moulton, L.H., Bernal, T. & Tovar, M. (2003a) Hyperendemic human and porcine Taenia solium infection in Peru. American Journal of Tropical Medicine Hygiene 66, 268–275.CrossRefGoogle Scholar
Garcia, H.H., Gonzalez, A.E., Evans, C.A.W., Gilman, R.H. & The Cysticercosis Working Group in Peru. (2003b) Taenia solium cysticercosis. Lancet 362, 547–556.CrossRefGoogle ScholarPubMed
Gonzalez, D., Rodriguez-Carbajal, J., Aluja, A. & Flisser, A. (1987) Cerebral cysticercosis in pigs studied by computed tomography and necropsy. Veterinary Parasitology 26, 55–69.CrossRefGoogle ScholarPubMed
Grewal, J.S., Kaur, S., Bhatti, G., Sawhney, I.M.S., Ganguly, N.K., Mahajan, R.C. & Malla, N. (2000) Cellular immune responses in human neurocysticercosis. Parasitology Research 86, 500–503.CrossRefGoogle ScholarPubMed
Gupta, S., Singh, P.K., Gupta, B., Singh, V. & Azam, A. (2009) Isolated primary intradural extramedullar spinal neurocysticercosis: a case report and review of literature. Acta Neurologica Taiwanica 18, 187–192.Google Scholar
Ito, A., Yamasaki, H., Nakao, M., Sako, Y., Okamoto, M., Sato, M.O., Nakaya, K., Margono, S.S., Ikejima, T., Kassuku, A.A., Sonia, M.S., Afonso, S.M.S., Ortiz, W.B., Plancarte, A., Zoli, A., Geerts, S. & Craig, P.S. (2003) Multiple genotypes of Taenia solium – ramifications for diagnosis, treatment and control. Acta Tropica 87, 95–101.CrossRefGoogle ScholarPubMed
Jae-Won, J., Jung-Kil, L., Jae-Hyun, L., Bo-Ra, S. & Soo-Han, K. (2010) Recurrent primary spinal subarachnoid neurocysticercosis. Spine 35, 172–175.Google Scholar
Kerstein, A.H. & Massey, A.D. (2010) Neurocysticercosis. Kansas Journal of Medicine 3, 52–54.CrossRefGoogle Scholar
Mkupasi, E.M., Sikasunge, C.S., Ngowi, H.A., Leifsson, P.S. & Johansen, M.V. (2013) Detection of cysteine protease in Taenia solium-induced brain granulomas in naturally infected pigs. Veterinary Parasitology 197, 360–363.CrossRefGoogle ScholarPubMed
Molinari, J.L., Mejia, H., White, A.C. Jr, Garrido, E., Borgonio, V.M., Baig, S. & Tato, P. (2000) Taenia solium: a cysteine protease secreted by metacestodes depletes human CD4 lymphocytes in vitro. Experimental Parasitology 94, 133–142.CrossRefGoogle ScholarPubMed
Mwanjali, G., Kihamia, C.M., Kakoko, D.V.C., Lekule, F., Ngowi, H., Johansen, M.V., Thamsborg, S.M. & Willingham, A.L. III (2013) Prevalence and practices associated with human Taenia solium infection in Mbeya Region, Tanzania. PloS Neglected Tropical Diseases 7, e2102.CrossRefGoogle Scholar
Pawlowski, Z.S. (2002) Taenia solium: basic biology and transmission. pp. 1–14in Singh, G. & Prabhakar, S. (Eds) Taenia solium cysticercosis. From basic to clinical science. Wallingford, UK, CABI Press.Google Scholar
Pérez-Torres, A., Ustarroz, M., Constantino, F., Villalobos, N. & De, A.A. (2002) Taenia solium cysticercosis: lymphocytes in the inflammatory reaction in naturally infected pigs. Parasitology Research 88, 150–152.CrossRefGoogle ScholarPubMed
Phiri, I.K., Dorny, P., Gabriel, S., Willingham, A.L. III, Sikasunge, C., Siziya, S. & Vercruysse, J. (2006) Assessment of routine inspection methods for porcine cysticercosis in Zambian village pigs. Journal of Helminthology 80, 69–72.CrossRefGoogle ScholarPubMed
Pittella, J.E. (1997) Neurocysticercosis. Brain Pathology 7, 681–693.CrossRefGoogle ScholarPubMed
Praet, N., Speybroeck, N., Rodriguez-Hidalgo, R., Benitez-Ortiz, W., Berkvens, D., Brandt, J., Saegerman, C. & Dorny, P. (2010) Age-related infection and transmission patterns of human cysticercosis. International Journal for Parasitology 40, 85–90.CrossRefGoogle ScholarPubMed
Prasad, K., Chawla, S., Prasad, A., Tripathi, M., Husain, N. & Gunta, R. (2006) Clinical signs for identification of neurocysticercosis in swine naturally infected with Taenia solium. Parasitology International 55, 151–154.CrossRefGoogle ScholarPubMed
Rahalkar, M.D., Shetty, D.D., Kelkar, A.B., Kelkar, A.A., Kinare, A.S. & Ambardekar, S.T. (2000) The many faces of cysticercosis. Clinical Radiology 55, 668–674.CrossRefGoogle ScholarPubMed
Ramirez-Zamora, A. & Alarcon, T. (2010) Management of neurocysticercosis. Neurological Research 32, 229–237.CrossRefGoogle ScholarPubMed
Restrepo, B.I., Alvarez, J.I., Castano, J.A., Arias, L.F., Restrepo, M., Trujillo, J., Colegial, C.H. & Teale, J.M. (2001) Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infection and Immunity 69, 4554–4560.CrossRefGoogle ScholarPubMed
Rossi, L.A., Sestari, A. & Cerioni, M. (2006) Intradura-extramedullary spinal cysticercosis with brain involvement: a case report and literature review. Radiologia Brasileira 39, 379–382.CrossRefGoogle Scholar
Saenz, B., Ramirez, J., Aluja, A., Escobar, A., Fragoso, G., Morales, J., Perez-Tamayo, R., Rosetti, F., Larralde, C., Sciutto, C. & Fleury, A. (2008) Human and porcine neurocysticercosis: differences in the distribution and developmental stages of cysticerci. Tropical Medicine and International Health 13, 697–702.CrossRefGoogle ScholarPubMed
Sauleau, P., Lapouble, E., Val-Laillet, D. & Malbert, C.H. (2009) The pig model in brain imaging and neurosurgery. Animal 3, 1138–1151.CrossRefGoogle ScholarPubMed
Sikasunge, C.S., Phiri, I.K., Johansen, M.V., Willingham, A.L. III & Leifsson, P.S. (2008) Host-cell apoptosis in Taenia solium-induced brain granulomas in naturally infected pigs. Veterinary Parasitology 135, 1237–1242.CrossRefGoogle ScholarPubMed
Sikasunge, C.S., Johansen, M.V., Phiri, I.K., Willingham, A.L. III & Leifsson, P.S. (2009) The immune response in Taenia solium neurocysticercosis in pigs is associated with astrogliosis, axonal degeneration and altered blood–brain barrier permeability. Veterinary Parasitology 160, 242–250.CrossRefGoogle ScholarPubMed
Solano, S., Cortés, I.M., Copitin, N.I., Tato, P. & Molinari, J.L. (2006) Lymphocyte apoptosis in the inflammatory reaction around Taenia solium metacestodes in porcine cysticercosis. Veterinary Parasitology 140, 171–176.CrossRefGoogle ScholarPubMed
Suri, A., Goel, R.K., Ahmad, F.U., Vellimana, A.K., Sharma, B.S. & Mahapatra, A.K. (2008) Transventricular, transaqueductal scope-in-scope endoscopic excision of fourth ventricular neurocysticercosis: a series of 13 cases and a review. Emergence Radiology 1, 35–39.Google ScholarPubMed
Swindle, M.M., Makin, A., Herron, A.J., Clubb, F.J. Jr & Frazier, K.S. (2012) Swine as models in biomedical research and toxicology testing. Veterinary Pathology 49, 344–356.CrossRefGoogle ScholarPubMed
Vega, R., Pinero, D., Ramanankandrasana, B., Dumas, M., Bouteille, B., Fleury, A., Sciutto, E., Larralde, C. & Fragoso, G. (2003) Population genetic structure of Taenia solium from Madagascar and Mexico: implications for clinical profile diversity and immunological technology. International Journal of Parasitology 33, 1479–1485.CrossRefGoogle ScholarPubMed
Verastegui, M., Gonzales, A.E., Gilman, R.H., Gavidia, C., Falcon, N., Bernal, T., Garcia, H.H. & The Cysticercosis Working Group in Peru. (2000) Experimental infection model for Taenia solium cysticercosis in swine. Veterinary Parasitology 94, 33–44.CrossRefGoogle ScholarPubMed
White, A.C. (2000) Neurocysticercosis: updates on epidemiology, pathogenesis, diagnosis, and management. Annual Reviews of Medicine 51, 187–206.CrossRefGoogle ScholarPubMed