Skip to main content Accessibility help

IgY antibody and human neurocysticercosis: a novel approach on immunodiagnosis using Taenia crassiceps hydrophobic antigens

  • Guilherme M. P. Carrara (a1), Gabriela B. Silva (a1), Lucas S. Faria (a1), Daniela S. Nunes (a1), Vanessa S. Ribeiro (a1), Camila A. Lopes (a1), Maria do Rosário F. Gonçalves-Pires (a1), Malu M. Santos (a2), Isabela P. Borges (a3), Álvaro Ferreira-Junior (a2), Veridiana M. R. Ávila (a3) and Julia M. Costa-Cruz (a1)...


Human neurocysticercosis (NCC) is a worldwide neglected disease caused by Taenia solium metacestode and responsible for various complications and neurological disorders. This study aimed to evaluate the use of specific immunoglobulin Y (IgY) produced by laying hens immunized with a hydrophobic fraction of Taenia crassiceps metacestodes (hFTc) in NCC diagnosis. Egg yolk IgY antibodies were fractionated, purified and characterized. Enzyme-linked immunosorbent assay (ELISA) was carried out to evaluate the production kinetics and avidity maturation of anti-hFTc IgY antibodies throughout the IgY obtention process. Antigen recognition tests were carried out by Western blotting and immunofluorescence antibody test using purified and specific anti-hFTc IgY antibodies for detection of parasitic antigens of T. crassiceps and T. solium metacestodes. Sandwich ELISA was performed to detect circulating immune complexes formed by IgG and parasitic antigens in human sera. The results showed high diagnostic values (93.2% sensitivity and 94.3% specificity) for immune complexes detection in human sera with confirmed NCC. In conclusion, specific IgY antibodies produced from immunized hens with hFTc antigens were efficient to detect T. solium immune complexes in human sera, being an innovative and potential tool for NCC immunodiagnosis.


Corresponding author

Author for correspondence: Julia M. Costa-Cruz, E-mail:


Hide All
Akita, EM and Nakai, S (1993) Comparison of four purification methods for the production of immunoglobulins from eggs laid by hens immunized with an enterotoxigenic E. coli strain. Journal of Immunological Methods 160, 207214.
Amro, WA, Al-Qaisi, W and Al-Razem, F (2018) Production and purification of IgY antibodies from chicken egg yolk. Journal of Genetic Engineering and Biotechnology 16, 99103.
Baermann, G (1917) Eine Einfache Methode zur Auffindung von Ankylostomum (nematoden) Larven in Erdproben. Mededeel. Mith H. Geneesk. Batavia, Lab Weltevreden Feestbundel 57, 4147.
Barnett, EV (1986) Circulating immune complexes: their biologic and clinical significance. Journal of Allergy and Clinical Immunology 78, 10891096.
Bueno, EC, Vaz, AJ, Machado, LD, Livramento, JA and Mielle, SR (2000) Specific Taenia crassiceps and Taenia solium antigenic peptides for neurocysticercosis immunodiagnosis using serum samples. Journal of Clinical Microbiology 38, 146151.
Cai, YC, Guo, J, Chen, SH, Tian, LG, Steinmann, P, Chen, MX, Li, H, Ai, L and Chen, JX (2012) Chicken egg yolk antibodies (IgY) for detecting circulating antigens of Schistosoma japonicum. Parasitology International 61, 385390.
Carpio, A, Fleury, A, Romo, ML and Abraham, R (2018) Neurocysticercosis: the good, the bad, and the missing. Expert Review of Neurotherapeutics 18, 289301.
da Silva Raposo, R, Santarém, VA, Merigueti, YFFB, Rubinsky-Elefant, G, de Lima Cerazo, LM, Pereira, L, Zampieri, BP, da Silva, AV and Laposy, CB (2016) Kinetic and avidity of IgY anti-Toxocara antibodies in experimentally infected chickens. Experimental Parasitology 171, 3341.
Del Brutto, OH (2012) Diagnostic criteria for neurocysticercosis, revisited. Pathogens and Global Health 106, 299304.
Del Brutto, OH, Nash, TE, White, AC Jr, Rajshekhar, V, Wilkins, PP, Singh, G, Vasquez, CM, Salgado, P, Gilman, RH and Garcia, HH (2017) Revised diagnostic criteria for neurocysticercosis. Journal of the Neurological Sciences 372, 202210.
Faria, LS, de Souza, DLN, Ribeiro, RP, Sousa, JEN, Borges, IP, Ávila, VMR, Ferreira-Júnior, A, Goulart, LR and Costa-Cruz, JM (2019) Highly specific and sensitive anti-Strongyloides venezuelensis IgY antibodies applied to the human strongyloidiasis immunodiagnosis. Parasitology International 72, 101933.
Ferreira-Junior, A, Santiago, FM, Silva, MV, Ferreira, FB, MacedoJunior, AG, Mota, CM, Faria, MS, Silva-Filho, HH, Silva, DA, Cunha-Junior, JP, Mineo, JR and Mineo, TW (2012) Production, characterization and applications for Toxoplasma gondii-specific polyclonal chicken egg yolk immunoglobulins. PLoS ONE 7, e40391.
Gabriël, S, Blocher, J, Dorny, P, Abatih, EN, Schmutzhard, E, Ombay, M, Mathias, B and Winkler, AS (2012) Added value of antigen ELISA in the diagnosis of neurocysticercosis in resource poor settings. PLoS Neglected Tropical Diseases 6, e1851.
Garcia, HH, Nash, TE and Del Brutto, OH (2014) Clinical symptoms, diagnosis, and treatment of neurocysticercosis. The Lancet Neurology 13, 12021215.
Garcia, HH, Castillo, Y, Gonzales, I, Bustos, JA, Saavedra, H, Jacob, L, Del Brutto, OH, Wilkins, PP, Gonzalez, AE and Gilman, RH (2018) Low sensitivity and frequent cross-reactions in commercially available antibody detection ELISA assays for Taenia solium cysticercosis. Tropical Medicine and International Health 23, 101105.
Gonçalves, FA, Machado, GA, Oliveira, HB, Rezende, MT, Mineo, JR and Costa-Cruz, JM (2010) Hydrophobic fraction of Taenia saginata metacestodes, rather than hydrophilic fraction, contains immunodominant markers for diagnosing human neurocysticercosis. Revista da Sociedade Brasileira de Medicina Tropical 43, 254259.
Gottstein, B and Hemmeler, E (1985) Egg yolk immunoglobulin Y as an alternative antibody in the serology of echinococcosis. Zeitschrift für Parasitenkunde 71, 273276.
Gripper, LB and Welburn, SC (2017) Neurocysticercosis infection and disease-A review. Acta Tropica 166, 218224.
Hernández-González, A, Noh, J, Perteguer, MJ, Gárate, T and Handali, S (2017) Comparison of T24H-his, GST-T24H and GST-Ts8B2 recombinant antigens in western blot, ELISA and multiplex bead-based assay for diagnosis of neurocysticercosis. Parasites and Vectors 10, 237.
Hodek, P, Trefil, P, Simunek, J, Hudecek, J and Stiborova, M (2013) Optimized protocol of chicken antibody (IgY) purification providing electrophoretically homogenous preparations. International Journal of Electrochemical Science 8, 113124.
Kousted, TM, Kalliokoski, O, Christensen, SK, Winther, JR and Hau, J (2017) Exploring the antigenic response to multiplexed immunizations in a chicken model of antibody production. Heliyon 3, e00267.
Laemmli, UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680685.
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 with sera from neurocysticercosis and hydatid disease patients. American Journal of Tropical Medicine and Hygiene 40, 282290.
Larralde, C, Sotelo, J, Montoya, RM, Palencia, G, Padilla, A, Govezensky, T, Diaz, ML and Sciutto, E (1990) Immunodiagnosis of human cysticercosis in cerebrospinal fluid. Antigens from murine Taenia crassiceps cysticerci effectively substitute those from porcine Taenia solium. Archives of Pathology & Laboratory Medicine 114, 926928.
Lee, W, Syed Atif, A, Tan, SC and Leow, CH (2017) Insights into the chicken IgY with emphasis on the generation and applications of chicken recombinant monoclonal antibodies. Journal of Immunological Methods 447, 7185.
Lopes, CA, de Faria, LS, de Sousa, JEN, Borges, IP, Ribeiro, RP, Bueno, LL, Rodrigues Ávila, VM, Ferreira-Júnior, Á and Costa-Cruz, JM (2019) Anti-Ascaris suum immunoglobulin Y as a novel biotechnological tool for the diagnosis of human ascariasis. Journal of Helminthology, 110. doi: 10.1017/S0022149X19000701.
Lowry, OH, Rosebrough, NJ, Farr, AL and Randall, RJ (1951) Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry 193, 265275.
Lutz, A (1919) O Schistosoma mansoni e a schistosomose segundo observações feitas no Brasil. Memórias do Instituto Oswaldo Cruz 11, 121125.
Machado, GA, Santiago, FM, Mineo, JR and Costa-Cruz, JM (2007) Assessment of antigenic fractions of varying hydrophobicity from Taenia solium metacestodes for the diagnosis of human neurocysticercosis. Tropical Medicine and International Health 12, 13691376.
Manhani, MN, Ribeiro, VS, Cardoso, R, Ueira-Vieira, C, Goulart, LR and Costa-Cruz, JM (2011) Specific phage-displayed peptides discriminate different forms of neurocysticercosis by antibody detection in the serum samples. Parasite Immunology 33, 322329.
Moraes, RG (1948) Contribuição para o estudo do Strongyloides stercoralis e da estrongiloidíase no Brasil. Revista de Saúde Pública 1, 507624.
Pardini, AX, Vaz, AJ, dos Ramos Machado, L and Livramento, JA (2001) Cysticercus antigens in cerebrospinal fluid samples from patients with neurocysticercosis. Journal of Clinical Microbiology 39, 33683372.
Ritchie, LS (1948) An ether sedimentation technique for routine stoll examination. Bulletin of the US Army Medicine Department 8, 326340.
Schade, R, Calzado, EG, Sarmiento, R, Chacana, PA, Porankiewicz-Asplund, J and Terzolo, HR (2005) Chicken egg yolk antibodies (IgY-technology): a review of progress in production and use in research and human and veterinary medicine. Alternatives to Laboratory Animals: ATLA 33, 129154.
Schniering, A, Schade, R and Hiepe, T (1996) Development of an IgY-based assay for the detection of Ascaris suum antigens. ALTEX 13, 6265.
Schwarzkopf, C, Staak, C, Behn, I and Erhard, M (2001) Immunisation. In Schade, R, Behn, I, Erhard, M, Hlinak, A and Staak, C (eds), Chicken Egg Yolk Antibodies, Production and Application-IgY-Technology. Berlin, Heidelberg: Springer-Verlag, pp. 2564.
Silva, GB, Nunes, DS, Sousa, JEN, Gonçalves-Pires, MRF, Levenhagen, MA and Costa-Cruz, JM (2017) Antigenic fractions from Taenia crassiceps metacestodes obtained by hydrophobicity for the immunodiagnosis of active and inactive forms of neurocysticercosis in human cerebrospinal fluid samples. Parasitology International 66, 134138.
Sotelo, J, Guerrero, V and Rubio, F (1985) Neurocysticercosis: a new classification based on active and inactive forms. A study of 753 cases. Archives of Internal Medicine 45, 442445.
Vaz, AJ, Nunes, CM, Piazza, RME, Livramento, JA, Silva, MV, Nakamura, PM and Ferreira, AW (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, 354357.
Wang, ZQ, Fu, GY, Jing, FJ, Jin, J, Ren, HJ, Jiang, P and Cui, J (2012) Detection of Trichinella spiralis circulating antigens in serum of experimentally infected mice by an IgY-mAb sandwich ELISA. Foodborne Pathogens and Disease 9, 727733.
World Health Organization (2019) Teniasis/Cisticercosis. Fact-sheets. Geneva, Switzerland: World Health Organization.


Type Description Title
Supplementary materials

Carrara et al. supplementary material
Figure S1

 Unknown (188 KB)
188 KB

IgY antibody and human neurocysticercosis: a novel approach on immunodiagnosis using Taenia crassiceps hydrophobic antigens

  • Guilherme M. P. Carrara (a1), Gabriela B. Silva (a1), Lucas S. Faria (a1), Daniela S. Nunes (a1), Vanessa S. Ribeiro (a1), Camila A. Lopes (a1), Maria do Rosário F. Gonçalves-Pires (a1), Malu M. Santos (a2), Isabela P. Borges (a3), Álvaro Ferreira-Junior (a2), Veridiana M. R. Ávila (a3) and Julia M. Costa-Cruz (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed