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Model systems for investigating disease processes in neurocysticercosis

Published online by Cambridge University Press:  15 November 2018

Anja de Lange Open the ORCID record for Anja de Lange [Opens in a new window] ,
Siddhartha Mahanty  and
Joseph V. Raimondo
Anja de Lange
Affiliation:
Division of Cell Biology, Department of Human Biology, Neuroscience Institute and Institute of Infectious Disease and Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Anzio Road, Observatory, Cape Town, Western Cape 7935, South Africa
Siddhartha Mahanty
Affiliation:
Department of Medicine, The Peter Doherty Institute for Infection and Immunity and the Victorian Infectious Diseases Service, University of Melbourne/The Royal Melbourne Hospital, 792 Elizabeth Street, Melbourne, VIC 3000, Australia
Joseph V. Raimondo*
Affiliation:
Division of Cell Biology, Department of Human Biology, Neuroscience Institute and Institute of Infectious Disease and Molecular Medicine, Faculty of Health Sciences, University of Cape Town, Anzio Road, Observatory, Cape Town, Western Cape 7935, South Africa
*
Author for correspondence: Joseph V. Raimondo, E-mail: joseph.raimondo@uct.ac.za
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Abstract

Neurocysticercosis (NCC) occurs following brain infection by larvae of the cestode Taenia solium. It is the leading cause of preventable epilepsy worldwide and therefore constitutes a critical health challenge with significant global relevance. Despite this, much is still unknown about many key pathogenic aspects of the disease, including how cerebral infection with T. solium results in the development of seizures. Over the past century, valuable mechanistic insights have been generated using both clinical studies and animal models. In this review, we critically assess model systems for investigating disease processes in NCC. We explore the respective strengths and weaknesses of each model and summarize how they have contributed to current knowledge of the disease. We call for the continued development of animal models of NCC, with a focus on novel strategies for understanding this debilitating but often neglected disorder.

Keywords

Animal modelscestodeepilepsyMesocestoides cortineurocysticercosisTaenia crassicepsTaenia solium
Type
Review Article
Information
Parasitology , Volume 146 , Issue 5 , April 2019 , pp. 553 - 562
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Copyright
Copyright © Cambridge University Press 2018 

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References

Alvarez, JI and Teale, JM (2006) Breakdown of the blood brain barrier and blood-cerebrospinal fluid barrier is associated with differential leukocyte migration in distinct compartments of the CNS during the course of murine NCC. Journal of Neuroimmunology 173, 45–55.Google Scholar
Alvarez, JI and Teale, JM (2007) Evidence for differential changes of junctional complex proteins in murine neurocysticercosis dependent upon CNS vasculature. Brain Research 1169, 98–111.Google Scholar
Alvarez, JI, Londoo, DP, Alvarez, AL, Trujillo, J, Jaramillo, MM and Restrepo, BI (2002) Granuloma formation and parasite disintegration in porcine cysticercosis: comparison with human neurocysticercosis. Journal of Comparative Pathology 127, 186–193.Google Scholar
Alvarez, JI, Mishra, BB, Gundra, UM, Mishra, PK and Teale, JM (2010) Mesocestoides corti intracranial infection as a murine model for neurocysticercosis. Parasitology 137, 359–372.Google Scholar
Amit, P, Nath, K, Rakesh, G, Shweta, T, Sanjeev, J, Vimal, P and Mukesh, T (2011) Immune response to different fractions of Taenia solium cyst fluid antigens in patients with neurocysticercosis. Experimental Parasitology 127, 687–692.Google Scholar
Arce-Sillas, A, Álvarez-Luquín, DD, Cárdenas, G, Casanova-Hernández, D, Fragoso, G, Hernández, M, Proaño Narváez, JV, García-Vázquez, F, Fleury, A, Sciutto, E and Adalid-Peralta, L (2016) Interleukin 10 and dendritic cells are the main suppression mediators of regulatory T cells in human neurocysticercosis. Clinical and Experimental Immunology 183, 271–279.Google Scholar
Arora, N, Tripathi, S, Kumar, P, Mondal, P, Mishra, A and Prasad, A (2017) Recent advancements and new perspectives in animal models for neurocysticercosis immunopathogenesis. Parasite Immunology 39, e12439.Google Scholar
Bhattarai, R, Budke, CM, Carabin, H, Proaño, JV, Flores-Rivera, J, Corona, T, Cowan, LD, Ivanek, R, Snowden, KF and Flisser, A (2011) Quality of life in patients with neurocysticercosis in Mexico. American Journal of Tropical Medicine and Hygiene 84, 782–786.Google Scholar
Burneo, JG and Cavazos, JE (2014) Neurocysticercosis and epilepsy. Epilepsy Currents 14, 23–28.Google Scholar
Cangalaya, C, Bustos, JA, Calcina, J, Vargas-Calla, A, Suarez, D, Gonzalez, AE, Chacaltana, J, Guerra-Giraldez, C, Mahanty, S, Nash, TE and García, HH (2016) Perilesional inflammation in neurocysticercosis – relationship between contrast-enhanced magnetic resonance imaging, Evans blue staining and histopathology in the pig model. PLoS Neglected Tropical Diseases 10, 1–13.Google Scholar
Carabin, H, Ndimubanzi, PC, Budke, CM, Nguyen, H, Qian, Y, Cowan, LD, Stoner, JA, Rainwater, E and Dickey, M (2011) Clinical manifestations associated with neurocysticercosis: a systematic review. PLoS Neglected Tropical Diseases 5, e1152.Google Scholar
Cardona, AE and Teale, JM (2002) Γ/δ T cell-deficient mice exhibit reduced disease severity and decreased inflammatory response in the brain in murine neurocysticercosis. The Journal of Immunology 169, 3163–3171.Google Scholar
Cardona, AE, Restrepo, BI, Jaramillo, JM and Teale, JM (1999) Development of an animal model for neurocysticercosis: immune response in the central nervous system is characterized by a predominance of γ δ T cells. The Journal of Immunology 162, 995–1002.Google Scholar
Cardona, AE, Gonzalez, PA and Teale, JM (2003) CC chemokines mediate leukocyte trafficking into the central nervous system during murine neurocysticercosis: role of yo T cells in amplification of the host immune response. Infection and Immunity 71, 2634–2642.Google Scholar
Carpio, A (2002) Neurocysticercosis: an update. The Lancet Infectious Diseases 2, 751–762.Google Scholar
Carpio, A and Romo, ML (2014) The relationship between neurocysticercosis and epilepsy: an endless debate. Arquivos de Neuro-Psiquiatria 75, 383–390.Google Scholar
Chowdhury, N, Saleque, A, Sood, NK and Singla, LD (2014) Induced neurocysticercosis in rhesus monkeys (Macaca mulatta) produces clinical signs and lesions similar to natural disease in man. The Scientific World Journal 2014, 248049.Google Scholar
Christensen, NM, Trevisan, C, Leifsson, PS and Johansen, MV (2016) The association between seizures and deposition of collagen in the brain in porcine Taenia solium neurocysticercosis. Veterinary Parasitology 228, 180–182.Google Scholar
Chung, J, Bahk, Y, Huh, S, Kang, S-Y, Kong, Y and Cho, S-Y (1999) A recombinant 10-kDa protein of Taenia solium metacestodes specific to active neurocysticercosis. The Journal of Infectious Diseases 180, 1307–1315.Google Scholar
Crosbie, PR, Padgett, KA and Boyce, WM (2000) Mesocestoides spp. tapeworm infections in dogs in California. California Veterinarian May/June, pp. 15–28.Google Scholar
Das, K, Mondal, GP, Banerjee, M, Mukherjee, BB and Singh, OP (2007) Role of antiparasitic therapy for seizures and resolution of lesions in neurocysticercosis patients: an 8 year randomised study. Journal of Clinical Neuroscience 14, 1172–1177.Google Scholar
de Aluja, AS, Villalobos, ANM, Plancarte, A, Rodarte, LF, Hernandez, M and Sciutto, E (1996) Experimental Taenia solium cysticercosis in pigs: characteristics of the infection and antibody response. Veterinary Parasitology 61, 49–59.Google Scholar
De Simoni, A and Yu, LMY (2006) Preparation of organotypic hippocampal slice cultures: interface method. Nature Protocols 1, 1439–1445.Google Scholar
Del Brutto, OH, Roos, KL, Coffey, CS and Garcia, HH (2006) Meta-analysis: cysticidal drugs for neurocysticercosis: albendazole and praziquantel. Annals of Internal Medicine 145, 43–51.Google Scholar
Ferrer, E, Gonzalez, LM, Foster-Cuevas, M, Cortez, MM, Davila, I, Rodrıguez, M, Scuitto, E, Harrison, LJS, Parkhouse, RME and Garate, T (2005) Taenia solium: characterization of a small heat shock protein (Tsol-sHSP35.6) and its possible relevance to the diagnosis and pathogenesis of neurocysticercosis. Experimental Parasitology 110, 1–11.Google Scholar
Fleury, A, Dessein, A, Marie, PP, Dumas, M, Tapia, G, Larralde, C and Sciutto, E (2004) Symptomatic human neurocysticercosis: age, sex and exposure factors relating with disease heterogeneity. Journal of Neurology 251, 830–837.Google Scholar
Fleury, A, Trejo, A, Cisneros, H, García-Navarrete, R, Villalobos, N, Hernández, M, Hernández, JV, Hernández, B, Rosas, G, Bobes, RJ, de Aluja, AS, Sciutto, E and Fragoso, G (2015) Taenia solium: development of an experimental model of porcine neurocysticercosis. PLoS Neglected Tropical Diseases 9, 1–18.Google Scholar
Fleury, A, Cardenas, G, Adalid-Peralta, L, Fragoso, G and Sciutto, E (2016) Immunopathology in Taenia solium neurocysticercosis. Parasite Immunology 38, 147–157.Google Scholar
Flisser, A (1994) Taeniasis and cysticercosis due to Taenia solium. Progress in Clinical Parasitology 4, 77–116.Google Scholar
Fox, M (2009) The legal regulation of primate research. The American Journal of Bioethics 9, 13–15.Google Scholar
Garcia, HH, Gonzales, I, Lescano, AG, Bustos, JA, Pretell, JE, Saavedra, H and Nash, TE (2014) Enhanced steroid dosing reduces seizures during antiparasitic treatment for cysticercosis and early after. Epilepsia 55, 1452–1459.Google Scholar
Gonzales, I, Rivera, JT and Garcia, HH (2016) Pathogenesis of Taenia solium taeniasis and cysticercosis. Parasite Immunology 38, 136–146.Google Scholar
Greene, M, Schill, K, Takahashi, S, Bateman-House, A, Beauchamp, T, Bok, H, Cheney, D, Coyle, J, Deacon, T, Dennett, D, Donovan, P, Flanagan, O, Goldman, S, Greely, H, Martin, L, Miller, E, Mueller, D, Siegel, A, Solter, D, Gearhart, J, McKhann, G and Faden, R (2005) Moral issues of human-non-human primate neural grafting. Science 309, 385–386.Google Scholar
Guerra-Giraldez, C, Marzal, M, Cangalaya, C, Balboa, D, Orrego, MÁ, Paredes, A, Gonzales-Gustavson, E, Arroyo, G, García, HH, González, AE, Mahanty, S and Nash, TE (2013) Disruption of the blood-brain barrier in pigs naturally infected with Taenia solium, untreated and after anthelmintic treatment. Experimental Parasitology 134, 443–446.Google Scholar
Gundra, UM, Mishra, BB, Wong, K and Teale, JM (2011) Increased disease severity of parasite-infected TLR2-/-mice is correlated with decreased central nervous system inflammation and reduced numbers of cells with alternatively activated macrophage phenotypes in a murine model of neurocysticercosis. Infection and Immunity 79, 2586–2596.Google Scholar
Johnston, JM, Dyer, CD, Madison-Antenucci, S, Mergen, KA, Veeder, CL and Brice, AK (2016) Neurocysticercosis in a Rhesus Macaque (Macaca mulatta). Comparative Medicine 66, 499–502.Google Scholar
Jull, P, Browne, E, Boufana, BS, Schöniger, S and Davies, E (2012) Cerebral coenurosis in a cat caused by Taenia serialis: neurological, magnetic resonance imaging and pathological features. Journal of Feline Medicine and Surgery 14, 646–649.Google Scholar
Kroeze, WK and Freeman, RS (1982) Taenia crassiceps: fate of cysticerci ingestion by the mouse. Experimental Parasitology 54, 425–431.Google Scholar
Kuntz, RE (1973) Models for investigation in parasitology. In Bourne, GH (ed.) Nonhuman Primates and Medical Research. New York, USA: Academic Press Inc, pp. 184–185.Google Scholar
Larralde, C, Montoya, RM, Sciutto, E, Diaz, ML, Govezensky, T and Coltorti, E (1989) Deciphering western blots of tapeworm antigens (Taenia solium, Echinococcus Granulosus, and Taenia Crassiceps) reacting sera from neurocysticercosis and hydatid disease patients. American Journal of Tropical Medicine 40, 282–290.Google Scholar
Leandro, LDA, Fraga, CM, de Souza Lino, R Jr and Vinaud, MC (2014) Partial reverse of the TCA cycle is enhanced in Taenia crassiceps experimental neurocysticercosis after in vivo treatment with anthelminthic drugs. Parasitology Research 113, 1313–1317.Google Scholar
Leon, A, Saito, EK, Mehta, B and McMurtray, AM (2015) Calcified parenchymal central nervous system cysticercosis and clinical outcomes in epilepsy. Epilepsy & Behavior 43, 77–80.Google Scholar
Liu, YJ, Li, QZ and Hao, YH (2002) Oncospheres of Taenia solium develop into cysticerci in normal mice. Journal of Veterinary Medicine, Series B 49, 371–372.Google Scholar
Madisen, L, Zwingman, TA, Sunkin, SM, Oh, SW, Zariwala, HA, Gu, H, Ng, LL, Palmiter, RD, Hawrylycz, MJ, Jones, AR, Lein, ES and Zeng, H (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neuroscience 13, 133–140.Google Scholar
Mahanty, S and Garcia, HH (2010) Cysticercosis and neurocysticercosis as pathogens affecting the nervous system. Progress in Neurobiology 91, 172–184.Google Scholar
Mahanty, S, Orrego, MA, Mayta, H, Marzal, M, Cangalaya, C, Paredes, A, Gonzales-Gustavson, E, Arroyo, G, Gonzalez, AE, Guerra-Giraldez, C, Garcia, HH and Nash, TE (2015) Post-treatment vascular leakage and inflammatory responses around brain cysts in porcine neurocysticercosis. PLoS Neglected Tropical Diseases 9, 1–18.Google Scholar
Marzal, M, Guerra-Giraldez, C, Paredes, A, Cangalaya, C, Rivera, A, Gonzalez, AE, Mahanty, S, Garcia, HH, Nash, TE, Gilman, RH, Arroyo, G, Gonzales-Gustavson, E, Tsang, VCW, Verastegui, M, Zimic, M, Mayta, H, Orrego, MA, Saenz, P, Gonzales, I and Saavedra, H (2014) Evans blue staining reveals vascular leakage associated with focal areas of host-parasite interaction in brains of pigs infected with Taenia solium. PLoS ONE 9, e97321.Google Scholar
Matos-silva, H, Reciputti, BP, De Paula, ÉC, Oliveira, AL, Moura, VBL, Vinaud, MC, Oliveira, MAP and Lino-Júnior, RDS (2012) Experimental encephalitis caused by Taenia crassiceps cysticerci in mice. Arquivos de Neuro-Psiquiatria 70, 287–292.Google Scholar
Mishra, BB, Gundra, UM and Teale, JM (2011) STAT6-/-mice exhibit decreased cells with alternatively activated macrophage phenotypes and enhanced disease severity in murine neurocysticercosis. Journal of Neuroimmunology 232, 26–34.Google Scholar
Moguel, B, Moreno-Mendoza, N, Bobes, RJ, Carrero, JC, Chimal-Monroy, J, Díaz-Hernández, ME, Herrera-Estrella, L and Laclette, JP (2015) Transient transgenesis of the tapeworm Taenia crassiceps. SpringerPlus 4, 496.Google Scholar
Molinari, JL, Meza, R and Tato, P (1983) Taenia solium: cell reactions to the larva (Cysticercus cellulosae) in naturally parasitized, immunized hogs. Experimental Parasitology 56, 327–338.Google Scholar
Nash, TE, Singh, G, White, AC, Rajshekhar, V, Loeb, JA, Praono, JV, Takayanagui, OM, Gonzalez, DVM, Butman, JA, DeGiorgio, C, Del Brutto, OH, Delgado-Escueta, A, Evans, CAW, Gilman, RH, Martinez, SM, Medina, MT, Pretell, EJ, Teale, J and Garcia, HH (2006) Treatment of neurocysticercosis: current status and future research needs. Neurologic Clinics 67, 1120–1127.Google Scholar
Nash, TE, Mahanty, S, Loeb, JA, Theodore, WH, Friedman, A, Sander, JW, Singh, G, Cavalheiro, E, Del Brutto, OH, Takayanagui, OM, Fleury, A, Verastegui, M, Preux, P, Montano, S, Pretell, EJ, White, AC Jr, Gonzales, AE, Gilman, RH and Garcia, HH (2015) Neurocysticercosis: a natural human model of epileptogenesis. Epilepsia 56, 177–183.Google Scholar
Navarrete-Perea, J, Isasa, M, Paulo, JA, Corral-Corral, R, Flores-Bautista, J, Hernández-Téllez, B, Bobes, RJ, Fragoso, G, Sciutto, E, Soberón, X, Gygi, SP and Laclette, JP (2017) Quantitative multiplexed proteomics of Taenia solium cysts obtained from the skeletal muscle and central nervous system of pigs. doi: 10.1371/journal.pntd.0005962.Google Scholar
Ndlovu, H and Brombacher, F (2014) Role of IL-4Rα during acute schistosomiasis in mice. Parasite Immunology 36, 421–427.Google Scholar
Nguekam, A, Zoli, AP, Vondou, L, Pouedet, SMR, Assana, E, Dorny, P, Brandt, J, Losson, B and Geerts, S (2003) Kinetics of circulating antigens in pigs experimentally infected with Taenia solium eggs. Veterinary Parasitology 111, 323–332.Google Scholar
Orioles, M, Beltran, E, Stewart, J, Boufana, B and Holloway, A (2014) Cerebral coenurosis in a cat. Veterinary Record Case Reports 2, e000124.Google Scholar
Patel, R, Jha, S and Yadav, RK (2006) Pleomorphism of the clinical manifestations of neurocysticercosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 134–141.Google Scholar
Peon, AN, Ledesma-Soto, Y and Terrazas, LI (2016) Regulation of immunity by Taeniids: lessons from animal models and in vitro studies. Parasite Immunology 38, 124–135.Google Scholar
Pradhan, S, Kathuria, MK and Gupta, RK (2000) Perilesional gliosis and seizure outcome: a study based on magnetization transfer magnetic resonance imaging in patients with neurocysticercosis. Annals of Neurology 48, 181–187.Google Scholar
Pradhan, S, Kumar, R and Gupta, RK (2003) Intermittent symptoms in neurocysticercosis: could they be epileptic? Acta Neurologica Scandinavica 107, 260–266.Google Scholar
Prasad, KN, Chawla, S, Prasad, A, Tripathi, M, Husain, N and Gupta, RK (2006) Clinical signs for identification of neurocysticercosis in swine naturally infected with Taenia solium. Parasitology International 55, 151–154.Google Scholar
Prasad, A, Gupta, RK, Pradhan, S, Tripathi, M, Pandey, CM and Prasad, KN (2008) What triggers seizures in neurocysticercosis? A MRI-based study in pig farming community from a district of North India. Parasitology International 57, 166–171.Google Scholar
Preet, S and Prakash, S (2011) Haematological profile in Rattus norvegicus during experimental cysticercosis. Journal of Parasitic Diseases 35, 144–147.Google Scholar
Restrepo, BI, Llaguno, P, Sandoval, MA, Enciso, JA and Teale, JM (1998) Analysis of immune lesions in neurocysticercosis patients: central nervous system response to helminth appears Th1-like instead of Th2. Journal of Neuroimmunology 89, 64–72.Google Scholar
Robinson, P, Garza, A, Weinstock, J, Serpa, JA, Goodman, JC, Eckols, KT, Firozgary, B and Tweardy, DJ (2012) Substance P causes seizures in neurocysticercosis. PLoS Pathogens 8, e1002489.Google Scholar
Rogers, SE, Pandey, VS and Bleakley, JS (1989) Neurocysticercosis in a dog. Annales de la Société Belge de Médecine Tropicale 69, 337–338.Google Scholar
Roman, G, Sotelo, J, Del Brutto, O, Flisser, A, Dumas, M, Wadia, N, Botero, D, Cruz, M, Garcia, H, de Bittencourt, PRM, Trelles, L, Arriagada, C, Lorenzana, P, Nash, TE and Spina-Franca, A (2000) A proposal to declare neurocysticercosis an international reportable disease. Bulletin of the World Health Organization 78, 399–406.Google Scholar
Saenz, B, Ramirez, J, Aluja, A, Escobar, A, Fragoso, G, Morales, J, Perez-Tamayo, R, Rosetti, F, Larralde, C, Sciutto, E and Fleury, A (2008) Human and porcine neurocysticercosis: differences in the distribution and developmental stages of cysticerci. Tropical Medicine and International Health 13, 697–702.Google Scholar
Saleque, A, Chowdhury, N, Iyer, PK and Baruah, G (1988) Induced Taenia solium cysticercosis in rhesus monkeys (Macaca mulatta): a clinicopathological study. Annals of Tropical Medicine and Parasitology 82, 103–105.Google Scholar
Santamaria, E, Plancarte, A and de Aluja, AS (2002) The experimental infection of pigs with different numbers of Taenia solium eggs: immune response and efficiency of establishment. The Journal of Parasitology 88, 69–73.Google Scholar
Schmidt, J and Todd, K (1978) Life cycle of Mesocestoides corti in the dog (Canis familiaris). American Journal of Veterinary Research 39, 1490–1493.Google Scholar
Sciutto, E, Fragoso, G, Trueba, L, Lemus, D, Montoya, RM, Diaz, ML, Govezensky, T, Lomeli, C, Tapia, G and Larralde, C (1990) Cysticercosis vaccine: cross protecting immunity with T. solium antigens against experimental murine T. crassiceps cysticercosis. Parasite Immunology 12, 687–696.Google Scholar
Sciutto, E, Fragoso, G and Larralde, C (2011) Taenia crassiceps as a model for Taenia solium and the S3Pvac vaccine. Parasite Immunology 33, 79–80.Google Scholar
Shukla, N, Husain, N, Jyotsna, , Gupta, S and Husain, M (2008) Comparisons between scolex and membrane antigens of Cysticercus fasciolaris and Cysticercus cellulosae larvae for immunodiagnosis of neurocysticercosis. Journal of Microbiology, Immunology and Infection 41, 519–524.Google Scholar
Sikasunge, CS, Johansen, MV, Phiri, IK, Willingham, AL and Leifsson, PS (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.Google Scholar
Singh, AK, Prasad, KN, Prasad, A, Tripathi, M, Gupta, RK and Husain, N (2013) Immune responses to viable and degenerative metacestodes of Taenia solium in naturally infected swine. International Journal for Parasitology 43, 1101–1107.Google Scholar
Stringer, JL, Marks, LM, White, AC Jr and Robinson, P (2003) Epileptogenic activity of granulomas associated with murine cysticercosis. Experimental Neurology 183, 532–536.Google Scholar
Sun, Y, Chauhan, A, Sukumaran, P, Sharma, J, Singh, BB and Mishra, BB (2014) Inhibition of store-operated calcium entry in microglia by helminth factors: implications for immune suppression in neurocysticercosis. Journal of Neuroinflammation 11, 210.Google Scholar
Trevisan, C, Mkupasi, EM, Ngowi, HA, Forkman, B and Johansen, MV (2016) Severe seizures in pigs naturally infected with Taenia solium in Tanzania. Veterinary Parasitology 220, 67–71.Google Scholar
Tsai, IJ, Zarowiecki, M, Holroyd, N, Garciarrubio, A, Sanchez-Flores, A, Brooks, KL, Tracey, A, Bobes, RJ, Fragoso, G, Sciutto, E, Aslett, M, Beasley, H, Bennett, HM, Cai, J, Camicia, F, Clark, R, Cucher, M, De Silva, N, Day, TA, Deplazes, P, Estrada, K, Fernandez, C, Holland, PWH, Hou, J, Hu, S, Huckvale, T, Hung, SS, Kamenetzky, L, Keane, JA, Kiss, F, Koziol, U, Lambert, O, Liu, K, Luo, X, Luo, Y, Macchiaroli, N, Nichol, S, Paps, J, Parkinson, J, Pouchkina-Stantcheva, N, Riddiford, N, Rosenvit, M, Salinas, G, Wasmuth, JD, Zamanian, M, Zheng, Y, Consortium, TTSG, Cai, X, Soberon, X, Olson, PD, Laclette, JP, Brehm, K and Berriman, M (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63.Google Scholar
Uddin, J, Garcia, HH, Gilman, RH, Gonzalez, AE and Friedland, JS (2005) Monocyte-astrocyte networks and the regulation of chemokine secretion in neurocysticercosis. The Journal of Immunology 175, 3273–3281.Google Scholar
Uddin, J, Gonzalez, AE, Gilman, RH, Thomas, LH, Rodriguez, S, Evans, CAW, Remick, DG, Garcia, HH and Friedland, JS (2010) Mechanisms regulating monocyte CXCL8 secretion in neurocysticercosis and the effect of antiparasitic therapy. The Journal of Immunology 185, 4478–4484.Google Scholar
Vendelova, E, Hrckova, G, Lutz, MB, Brehm, K and Komguep, JN (2016) In vitro culture of Mesocestoides corti metacestodes and isolation of immunomodulatory excretory – secretory products. Parasite Immunology 38, 403–413.Google Scholar
Verastegui, MR, Mejia, A, Clark, T, Gavidia, CM, Mamani, J, Ccopa, F, Angulo, N, Chile, N, Carmen, R, Medina, R, Garcia, HH, Rodriguez, S, Ortega, Y and Gilman, RH (2015) Novel rat model for neurocysticercosis using Taenia solium. The American Journal of Pathology 185, 2259–2268.Google Scholar
Verma, A, Prasad, KN, Gupta, RK, Singh, AK, Nyati, KK, Rizwan, A, Pandey, CM and Paliwal, VK (2010) Toll-like receptor 4 polymorphism and its association with symptomatic neurocysticercosis. Journal of Infectious Diseases 202, 1219–1225.Google Scholar
Voge, M and Coulombe, LS (1966) Growth and asexual multiplication in vitro of mesocestoides tetrathyridia. American Journal of Tropical Medicine and Hygiene 15, 902–907.Google Scholar
White, AC Jr (2000) Neurocysticercosis: updates on epidemiology, pathogenesis, diagnosis, and management. Annual Review of Medicine 51, 187–206.Google Scholar
Willms, K and Zurabian, R (2010) Taenia crassiceps: in vivo and in vitro models. Parasitology 137, 333–346.Google Scholar
Wünschmann, A, Garlie, V, Averbeck, G, Kurtz, H and Hoberg, EP (2003) Cerebral cysticercosis by Taenia crassiceps in a domestic cat. Journal of Veterinary Diagnostic Investigation 15, 484–488.Google Scholar
Wykes, RC, Heeroma, JH, Mantoan, L, Zheng, K, MacDonald, DC, Deisseroth, K, Hashemi, KS, Walker, MC, Schorge, S and Kullmann, DM (2012) Optogenetic and potassium channel gene therapy in a rodent model of focal neocortical epilepsy. Science Translational Medicine 4, 161ra152.Google Scholar
Yakoleff-Greenhouse, V, Flisser, A, Sierra, A and Larralde, C (1982) Analysis of antigenic variation in cysticerci of Taenia solium. The Journal of Parasitology 68, 39–47.Google Scholar
Zhao, B, Jiang, H, Ma, W, Jin, D, Li, H, Lu, H, Nakajima, H, Huang, T, Sun, K, Chen, S and Chen, K-B (2016) Albendazole and corticosteroids for the treatment of solitary cysticercus granuloma: a network meta-analysis. PLoS Neglected Tropical Diseases 10, e0004418.Google Scholar
Zurabian, R, Aguilar, L, Jiménez, JA, Robert, L and Willms, K (2008) Evagination and infectivity of Taenia crassiceps cysticerci in experimental animals. The Journal of Parasitology 94, 1–6.Google Scholar