Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-16T09:24:59.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Cellular immune response in intraventricular experimental neurocysticercosis

Published online by Cambridge University Press:  02 December 2015

VANIA B. L. MOURA ,
SARAH B. LIMA ,
HIDELBERTO MATOS-SILVA ,
MARINA C. VINAUD ,
PATRICIA R. A. N. LOYOLA  and
RUY S. LINO JR.
VANIA B. L. MOURA
Affiliation:
Department of Microbiology, Immunology, Parasitology and Pathology, Tropical Pathology and Public Health Institute, Federal University of Goias,– Rua 235 S/N, Setor Universitário, 74605-050, Goiânia, Goiás, Brazil
SARAH B. LIMA
Affiliation:
Tropical Pathology and Public Health Post-graduation Programme, Tropical Pathology and Public Health Institute, Federal University of Goias,– Rua 235 S/N, Setor Universitário, 74605-050, Goiânia, Goiás, Brazil
HIDELBERTO MATOS-SILVA
Affiliation:
Tropical Pathology and Public Health Post-graduation Programme, Tropical Pathology and Public Health Institute, Federal University of Goias,– Rua 235 S/N, Setor Universitário, 74605-050, Goiânia, Goiás, Brazil
MARINA C. VINAUD
Affiliation:
Department of Microbiology, Immunology, Parasitology and Pathology, Tropical Pathology and Public Health Institute, Federal University of Goias,– Rua 235 S/N, Setor Universitário, 74605-050, Goiânia, Goiás, Brazil
PATRICIA R. A. N. LOYOLA
Affiliation:
Department of Microbiology, Immunology, Parasitology and Pathology, Tropical Pathology and Public Health Institute, Federal University of Goias,– Rua 235 S/N, Setor Universitário, 74605-050, Goiânia, Goiás, Brazil
RUY S. LINO JR.*
Affiliation:
Department of Microbiology, Immunology, Parasitology and Pathology, Tropical Pathology and Public Health Institute, Federal University of Goias,– Rua 235 S/N, Setor Universitário, 74605-050, Goiânia, Goiás, Brazil
*
*Corresponding author. Department of Microbiology, Immunology, Parasitology and Pathology, Tropical Pathology and Public Health Institute, Federal University of Goias,– Rua 235 S/N, Setor Universitário, 74605-050, Goiânia, Goiás, Brazil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Neurocysticercosis (NCC) is considered a neglected parasitic infection of the human central nervous system. Its pathogenesis is due to the host immune response, stage of evolution and location of the parasite. The aim of this study was to evaluate the in situ and systemic immune response through cytokines dosage (IL-4, IL-10, IL-17 and IFN-γ) as well as the local inflammatory response of the experimental NCC with Taenia crassiceps. The in situ and systemic cellular and inflammatory immune response were evaluated through the cytokines quantification at 7, 30, 60 and 90 days after inoculation and histopathological analysis. All cysticerci were found within the cerebral ventricles. There was a discrete intensity of inflammatory cells of mixed immune profile, polymorphonuclear and mononuclear cells, at the beginning of the infection and predominance of mononuclear cells at the end. The systemic immune response showed a significant increase in all the analysed cytokines and predominance of the Th2 immune profile cytokines at the end of the infection. These results indicate that the location of the cysticerci may lead to ventriculomegaly. The acute phase of the infection showed a mixed Th1/Th17 profile accompanied by high levels of IL-10 while the late phase showed a Th2 immune profile.

Keywords

Neurocysticercosisimmune profilecytokinesinflammationTaenia crassiceps
Type
Research Article
Information
Parasitology , Volume 143 , Issue 3 , March 2016 , pp. 334 - 342
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aguilar-Rebolledo, F., Cedillo-Rivera, R., Llaguno-Violante, P., Torres-López, J., Muñoz-Hernández, O. and Enciso-Moreno, J. A. (2001). Interleukin levels in cerebrospinal fluid from children with neurocysticercosis. The American Journal of Tropical Medicine and Hygiene 64, 35–40.Google Scholar
Alonso-Trujillo, J., Rivera-Montoya, I., Rodriguez-Sosa, M. and Terrazas, L. I. (2007). Nitric oxide contributes to host resistance against experimental Taenia crassiceps cysticercosis. Parasitology Research 100, 1341–1350.Google Scholar
Alvarez, J. I., Mishra, B. B., Gundra, U. M., Mishra, P. K. and Teale, J. M. (2010). Mesocestoides corti intracranial infection as a murine model for neurocysticercosis. Parasitology 137, 359–372.Google Scholar
Agapejev, S. (2003). Clinical and epidemiological aspects of neurocysticercosis in Brazil: a critical approach. Arquivos de Neuropsiquiatria 61, 822–828. doi: http://dx.doi.org/10.1590/S0004-282X2003000500022 Google Scholar
Apuzzo, M. L. J., Dobkin, W. R., Zee, C. S., Chan, J. C., Giannotta, S. L. and Weiss, M. H. (1984). Surgical considerations in the treatment of intraventricular neurocysticercosis: an analysis of 45 cases. Journal of Neurosurgery 60, 400–407.CrossRefGoogle Scholar
Arechavaleta, F., Molinari, J. L. and Tato, P. (1998). A Taenia solium metacestode factor nonspecifically inhibits cytokine production. Parasitology Research 84, 117–122.Google Scholar
Carabin, H., Ndimubanzi, P. C., Budke, C. M., Nguyen, H., Qian, Y., Cowan, L. D., Stoner, J. A., Rainwater, E. and Dickey, M. (2011). Clinical manifestations associated with neurocysticercosis: a systematic review. PLoS Neglected Tropical Diseases 5, e1152.Google Scholar
Cardona, A. E. and Teale, J. M. (2002). Gamma/delta T cell-deficient mice exhibit reduced disease severity and decreased inflammatory response in the brain in murine neurocysticercosis. Journal of Immunology 169, 3163–3171.CrossRefGoogle ScholarPubMed
Cardona, A. E., Gonzalez, P. A. and Teale, J. M. (2003). CC chemokines mediate leukocyte trafficking into the central nervous system during murine neurocysticercosis: role of gamma-delta T cells in amplification of the host immune response. Infection and Immunity 71, 2634–2642.Google Scholar
Cardona, A. E., Restrepo, B. I., Jaramillo, J. M. and 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.Google Scholar
Chavarría, A., Roger, B., Fragoso, G., Tapia, G., Fleury, A., Dumas, M., Dessein, A., Larralde, C. and Sciutto, E. (2003). TH2 profile in asymptomatic Taenia solium human neurocysticercosis. Microbes and Infection 5, 1109–1115.CrossRefGoogle ScholarPubMed
Chavarría, A., Fleury, A., Garcia, E., Marquez, C., Fragoso, G. and Sciutto, E. (2005). Relationship between the clinical heterogeneity of neurocysticercosis and the immune-inflammatory profiles. Clinical Immunology 116, 271–278.Google Scholar
Chavarria, A., Fleury, A., Bobes, R. J., Morales, J., Fragoso, G. and Sciutto, E. (2006). A depressed peripheral cellular immune response is related with symptomatic neurocysticercosis. Microbes and Infection 8, 1082–1089.Google Scholar
Colli, B. O., Martelli, N., Assirati, J. A. Jr., Machado, H. R. and de Vergueiro, F. S. (1986). Results of surgical treatment of neurocysticercosis in 69 cases. Journal of Neurosurgery 65, 309–315.Google Scholar
Cuetter, A. C. and Andrews, R. J. (2002). Intraventricular neurocysticercosis: 18 consecutive patients and review of the literature. Neurosurgical Focus 12, e5.Google Scholar
Del Brutto, O. H. (2014). Neurocysticercosis. The Neurohospitalist 4, 205–212.Google Scholar
Del Brutto, O. H. and García, H. H. (2012). Neurocysticercosis in nonendemic countries: time for a reappraisal. Neuroepidemiology 39, 145–146.Google Scholar
Del Brutto, O. H., Santibanez, R., Idrovo, L., Rodriguez, S., Diaz-Calderon, E., Navas, C., Gilman, R. H., Cuesta, F., Mosquera, A., Gonzalez, A. E., Tsang, V. C. and Garcia, H. H. (2005). Epilepsy and neurocysticercosis in Atahualpa: a door-to-door survey in rural coastal Ecuador. Epilepsia 46, 583–587.Google Scholar
Evans, C. A., Garcia, H. H., Hartnell, A., Gilman, R. H., Jose, P. J., Martinez, M., Remick, D. G., Williams, T. J. and Friedland, J. S. (1998). Elevated concentrations of eotaxin and interleukin-5 in human neurocysticercosis. Infection and Immunity 66, 4522–4525.Google Scholar
Flisser, A. (1991). Taeniasis-cysticercosis: an introduction. The Southeast Asian Journal of Tropical Medicine and Public Health 22, 233–235.Google Scholar
Flisser, A., Sarti, E., Lightowlers, M. and Schantz, P. (2003). Neurocysticercosis: regional status, epidemiology, impact and control measures in the Americas. Acta Tropica 87, 43–51.Google Scholar
Freitas, A. A., Moura, V. B., Gonçalves, S. F., Rodrigues, A. A., Félix, R. M., Soares, T. P., Irusta, V. R., Vinaud, M. C., Oliveira, M. A. and Lino, R. S. Jr. (2012). Kinetics of the inflammatory response in subcutaneous cysticercosis induced in mice by Taenia crassiceps . Journal of Comparative Pathology 147, 267–274.CrossRefGoogle ScholarPubMed
García, H. H. and Del Brutto, O. H. (2005). Neurocysticercosis: updated concepts about an old disease. The Lancet Neurology 4, 653–661.Google Scholar
Garcia, H. H., Nash, T. E. and Del Brutto, O. H. (2014 a). Clinical symptoms, diagnosis, and treatment of neurocysticercosis. The Lancet Neurology 13, 1202–1215.CrossRefGoogle ScholarPubMed
Garcia, H. H., Rodriguez, S. and Friedland, J. S. (2014 b). Immunology of Taenia solium taeniasis and human cysticercosis. Parasite Immunology 36, 388–396.Google Scholar
Gazzinelli, R. T., Talvani, A., Camargo, M. M., Santiago, H. C., Oliveira, M. A., Vieira, L. Q., Martins, G. A., Aliberti, J. C. and Silva, J. S. (1998). Induction of cell-mediated immunity during early stages of infection with intracellular protozoa. Brazilian Journal of Medical and Biological Research 31, 89–104.Google Scholar
Genovesse, M. C., Van Den Bosch, F., Robertson, S. A., Bojin, I. M., Ryan, P. and Sloan-Lancaster, J. (2010). LY2439821, a humanized anti-interleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: a phase I randomized, double-blind, placebo-controlled, proof-of-concept study. Arthritis and Rheumatism 62, 929–939.Google Scholar
Gomez-Garcia, L., Rivera-Montoya, I., Rodriguez-Sosa, M. and Terrazas, L. I. (2006). Carbohydrate components of Taenia crassiceps, metacestodes display Th2-adjuvant and anti-inflammatory properties when co-injected with bystander antigen. Parasitology Research 99, 440–448.CrossRefGoogle ScholarPubMed
Gordon, S. (2003). Alternative activation of macrophages. Nature Reviews Immunology 3, 23–35.CrossRefGoogle ScholarPubMed
Hueber, W., Patel, D. D., Dryja, T., Wright, A. M., Koroleva, I., Bruin, G., Antoni, C., Draelos, Z., Gold, M. H., Psoriasis Study Group, Durez, P., Tak, P. P., Gomez-Reino, J. J., Rheumatoid Arthritis Study Group, Foster, C. S., Kim, R. Y., Samson, C. M., Falk, N. S., Chu, D. S., Callanan, D., Nguyen, Q. D.; Uveitis Study Group, Rose, K., Haider, A. and Di Padova, F. (2010). Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Science Translational Medicine 2, 52ra72.Google Scholar
Kelesidis, T. and Tsiodras, S. (2012). Extraparenchymal neurocysticercosis in the United States. The American Journal of the Medical Sciences 344, 79–82.Google Scholar
Khade, P., Lemos, R. S. and Toussaint, L. G. (2013). What is the utility of postoperative antihelminthic therapy after resection for intraventricular neurocysticercosis? World Neurosurery 79, 558–567.Google Scholar
Laclette, J. P., Merchant, M. T., Damian, R. T. and Willms, K. (1990). Crystals of virus-like particles in the metacestodes of Taenia solium and T. crassiceps . Journal of Invertebrate Pathology 56, 215–221.Google Scholar
Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T., Kastelein, R. A. and Cua, D. J. (2005). IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. The Journal of Experimental Medicine 201, 233–240.CrossRefGoogle ScholarPubMed
Lino, R. S. Jr., Ribeiro, P. M., Antonelli, E. J., Faleiros, A. C., Terra, S. A., Reis, M. A. and Teixeira, V. P. A. (2002). Características evolutivas do Cysticercus cellulosae no encéfalo e no coração. Revista da Sociedade Brasileira de Medicina Tropical 35, 617–622.Google Scholar
Lubberts, E., Koenders, M. I., Oppers-Walgreen, B., van den Bersselaar, L., Coenen-de Roo, C. J., Joosten, L. A. and van den Berg, W. B. (2004). Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis and Rheumatism 50, 650–659.Google Scholar
Matos-Silva, H., Reciputti, B. P., Paula, E. C., Oliveira, A. L., Moura, V. B. L., Vinaud, M. C., Oliveira, M. A. P. and Lino, R. S. Jr., (2012). Experimental encephalitis caused by Taenia crassiceps cysticerci in mice. Arquivos de Neuropsiquiatria 70, 287–292.Google Scholar
Matushita, H., Pinto, F. C., Cardeal, D. D. and Teixeira, M. J. (2011). Hydrocephalus in neurocysticercosis. Childs Nervous System 27, 1709–1721.Google Scholar
Mendlovic, F., Cruz-Rivera, M., Avila, G., Vaughan, G. and Flisser, A. (2015). Cytokine, antibody and proliferative responses elicited by Taenia solium calreticulin upon experimental infection in hamsters. PLoS ONE 10, e0121321.Google Scholar
Moura, V. B. L., Silva, M. M., Batista, L. F., Gomes, C. M., Leenen, P. J. M., Lino, R. S. Jr., and Oliveira, M. A. P. (2013). Arginase activity is associated with fibrosis in experimental infection with Taenia crassiceps, but does not play a major role in resistance to infection. Experimental Parasitology 135, 599–605.Google Scholar
Nash, T. E., Del Brutto, O. H., Butman, J. A., Corona, T., Delgado-Escueta, A., Duron, R. M., Evans, C. A., Gilman, R. H., Gonzalez, A. E., Loeb, J. A., Medina, M. T., Pietsch-Escueta, S., Pretell, E. J., Takayanagui, O. M., Theodore, W., Tsang, V. C. and Garcia, H. H. (2004). Calcific neurocysticercosis and epileptogenesis. Neurology 62, 1934–1938.Google Scholar
Oliveira, M. A. P., Santiago, H. C., Lisboa, C. R., Ceravollo, I. P., Trinchieri, G., Gazinelli, R. T. and Vieira, L. Q. (2000). Leishmania sp: comparative study with Toxoplasma gondii and Trypanosoma cruzi in their ability to initialize IL12 and IFN-g synthesis. Experimental Parasitology 95, 96–105.Google Scholar
Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y. H., Wang, Y., Hood, L., Zhu, Z., Tian, Q. and Dong, C. (2005). A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nature Immunology 6, 1133–1141.Google Scholar
Rathore, C. and Radhakrishnan, K. (2012). What causes seizures in patients with calcified neurocysticercal lesions. Neurology 78, 612–613.CrossRefGoogle ScholarPubMed
Restrepo, B. I., Aguilar, M. I., Melby, P. C. and Teale, J. M. (2001 a). Analysis of the peripheral immune response in patients with neurocysticercosis: evidence for T cell reactivity to parasite glycoprotein and vesicular fluid antigens. The American Journal of Tropical Medicine and Hygiene 65, 366–370.Google Scholar
Restrepo, B. I., Alvarez, J. I., Castano, J. A., Arias, L. F., Restrepo, M., Trujillo, J., Colegial, C. H. and Teale, J. M. (2001 b). Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infection and Immunity 69, 4554–4560.Google Scholar
Reyes, J. L., Terrazas, C. A., Vera-Arias, L. and Terrazas, L. I. (2009). Differential response of antigen presenting cells from susceptible and resistant strains of mice to Taenia crassiceps infection. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 9, 1115–1127.Google Scholar
Rodrigues, V. Jr., De-Mello, F. A., Magalhaes, E. P., Ribeiro, S. B. and Marquez, J. O. (2000). Interleukin-5 and interleukin-10 are major cytokines in cerebrospinal fluid from patients with active neurocysticercosis. Brazilian Journal of Medical and Biological Research 33, 1059–1063. http://dx.doi.org/10.1590/S0100-879X2000000900011 Google Scholar
Rodriguez-Sosa, M., David, J. R., Bojalil, R., Satoskar, A. R. and Terrazas, L. I. (2002). Cutting edge: susceptibility to the larval stage of the helminth parasite Taenia crassiceps is mediated by Th2 response induced via STAT6 signaling. Journal of Immunology 168, 3135–3139.Google Scholar
Sáenz, B., Fleury, A., Chavarría, A., Hernández, M., Crispin, J. C., Vargas-Rojas, M. I., Fragoso, G. and Sciutto, E. (2012). Neurocysticercosis: local and systemic immune-inflammatory features related to severity. Medical Microbiology and Immunology 201, 73–80.Google Scholar
Sciutto, E., Chavarria, A., Fragoso, G., Fleury, A. and Larralde, C. (2007). The immune response in Taenia solium cysticercosis: protection and injury. Parasite Immunology 29, 621–636.Google Scholar
Shook, B. A., Lennington, J. B., Acabchuk, R. L., Halling, M., Sun, Y., Peters, J., Wu, Q., Mahajan, A., Fellows, D. W. and Conover, J. C. (2014). Ventriculomegaly associated with ependymal gliosis and declines in barrier integrity in the aging of human and mouse brain. Aging cell 13, 340–350.Google Scholar
Sotelo, J. and Marin, C. (1987). Hydrocephalus secondary to cysticercotic arachnoiditis. A long-term follow-up review of 92 cases. Journal of Neurosurgery 66, 686–689.Google Scholar
Takayanagui, O. M. (1990). Neurocysticercosis. I. Clinical and laboratory course of 151 cases. Arquivos de Neuropsiquiatria 48, 1–10.Google Scholar
Takayanagui, O. M., Castro e Silva, A. A., Santiago, R. C., Odashima, N. S., Terra, V. C. and Takayanagui, A. M. (1996). Compulsory notification of cysticercosis in Ribeirao Preto—SP, Brazil. Arquivos de Neuropsiquiatria 54, 557–564.Google Scholar
Terrazas, L. I. (2008). The complex role of pro- and anti-inflammatory cytokines in cysticercosis: immunological lessons from experimental and natural hosts. Current Topics in Medicinal Chemistry 8, 383–392.Google Scholar
Terrazas, L. I., Bojalil, R., Govezensky, T. and Larralde, C. (1998). Shift from an early protective Th1-type immune response to a late permissive Th2-type response in murine cysticercosis (Taenia crassiceps). The Journal of Parasitology 84, 74–81.Google Scholar
Toenjes, S. A. and Kuhn, R. E. (2003). The initial immune response during experimental cysticercosis is of the mixed Th1/Th2 type. Parasitology Research 89, 407–413.Google Scholar
Toenjes, S. A., Spolski, R. J., Mooney, K. A. and Kuhn, R. E. (1999). The systemic immune response of BALB/c mice infected with larval Taenia crassiceps is a mixed Th1/Th2-type response. Parasitology 118, 623–33.Google Scholar
Vaz, A. J., Nunes, C. M., Piazza, R. M., Livramento, J. A., da Silva, M. V., Nakamura, P. M. and Ferreira, A. W. (1997). Immunoblot with cerebrospinal fluid from patients with neurocysticercosis using antigen from cysticerci of Taenia solium and Taenia crassiceps . The American Journal of Tropical Medicine and Hygiene 57, 354–357.Google Scholar
Vinaud, M. C., Lino, R. S. Jr., and Bezerra, J. C. B. (2007). Taenia crassiceps organic acids detected in cysticerci. Experimental Parasitology 116, 335–339.Google Scholar
White, A. C. Jr., Robinson, P. and Kuhn, R. (1997). Taenia solium cysticercosis: host-parasite interactions and the immune response. Chemical Immunology 66, 209–230.Google ScholarPubMed
Zee, C. S., Segall, H. D., Destian, S., Ahmadi, J. and Apuzzo, M. L. (1993). MRI of intraventricular cysticercosis: surgical implications. Journal of Computer Assisted Tomography 17, 932–939.Google Scholar