Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T13:52:59.430Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  23 October 2019

Guilherme M. P. Carrara ,
Gabriela B. Silva ,
Lucas S. Faria ,
Daniela S. Nunes ,
Vanessa S. Ribeiro ,
Camila A. Lopes ,
Maria do Rosário F. Gonçalves-Pires ,
Malu M. Santos ,
Isabela P. Borges  and
Álvaro Ferreira-Junior
...Show all authors
Guilherme M. P. Carrara
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
Gabriela B. Silva
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
Lucas S. Faria
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
Daniela S. Nunes
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
Vanessa S. Ribeiro
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
Camila A. Lopes
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
Maria do Rosário F. Gonçalves-Pires
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
Malu M. Santos
Affiliation:
Programa de Pós-Graduação em Sanidade e Produção Animal nos Trópicos, Universidade de Uberaba, Campus Aeroporto. Av. Nenê Sabino, sala 2D05, Uberaba, Minas Gerais38055-500, Brasil
Isabela P. Borges
Affiliation:
Laboratório de Bioquímica e Toxinas Animais, Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Av. Pará 1720, Uberlândia, Minas Gerais38400-902, Brasil
Álvaro Ferreira-Junior
Affiliation:
Programa de Pós-Graduação em Sanidade e Produção Animal nos Trópicos, Universidade de Uberaba, Campus Aeroporto. Av. Nenê Sabino, sala 2D05, Uberaba, Minas Gerais38055-500, Brasil
Veridiana M. R. Ávila
Affiliation:
Laboratório de Bioquímica e Toxinas Animais, Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Av. Pará 1720, Uberlândia, Minas Gerais38400-902, Brasil
Julia M. Costa-Cruz*
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Av. Amazonas s/n, bloco 4C, Uberlândia, MinasGerais38400-902, Brasil
*
Author for correspondence: Julia M. Costa-Cruz, E-mail: costacruz@ufu.br
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Egg yolk IgYELISAimmune complexesneurocysticercosisTaenia solium
Type
Research Article
Information
Parasitology , Volume 147 , Issue 2 , February 2020 , pp. 240 - 247
Check for updates
Copyright
Copyright © Cambridge University Press 2019

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

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, 207–214.CrossRefGoogle ScholarPubMed
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, 99–103.CrossRefGoogle ScholarPubMed
Baermann, G (1917) Eine Einfache Methode zur Auffindung von Ankylostomum (nematoden) Larven in Erdproben. Mededeel. Mith H. Geneesk. Batavia, Lab Weltevreden Feestbundel 57, 41–47.Google Scholar
Barnett, EV (1986) Circulating immune complexes: their biologic and clinical significance. Journal of Allergy and Clinical Immunology 78, 1089–1096.CrossRefGoogle ScholarPubMed
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, 146–151. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC86041.Google ScholarPubMed
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, 385–390.CrossRefGoogle ScholarPubMed
Carpio, A, Fleury, A, Romo, ML and Abraham, R (2018) Neurocysticercosis: the good, the bad, and the missing. Expert Review of Neurotherapeutics 18, 289–301.CrossRefGoogle ScholarPubMed
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, 33–41.CrossRefGoogle ScholarPubMed
Del Brutto, OH (2012) Diagnostic criteria for neurocysticercosis, revisited. Pathogens and Global Health 106, 299–304.CrossRefGoogle ScholarPubMed
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, 202–210.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Garcia, HH, Nash, TE and Del Brutto, OH (2014) Clinical symptoms, diagnosis, and treatment of neurocysticercosis. The Lancet Neurology 13, 1202–1215.CrossRefGoogle ScholarPubMed
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, 101–105.CrossRefGoogle ScholarPubMed
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, 254–259.CrossRefGoogle Scholar
Gottstein, B and Hemmeler, E (1985) Egg yolk immunoglobulin Y as an alternative antibody in the serology of echinococcosis. Zeitschrift für Parasitenkunde 71, 273–276.CrossRefGoogle ScholarPubMed
Gripper, LB and Welburn, SC (2017) Neurocysticercosis infection and disease-A review. Acta Tropica 166, 218–224.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 113–124.Google Scholar
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.CrossRefGoogle Scholar
Laemmli, UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
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, 282–290.CrossRefGoogle Scholar
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, 926–928.Google ScholarPubMed
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, 71–85.CrossRefGoogle ScholarPubMed
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, 1–10. doi: 10.1017/S0022149X19000701.Google Scholar
Lowry, OH, Rosebrough, NJ, Farr, AL and Randall, RJ (1951) Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry 193, 265–275.Google ScholarPubMed
Lutz, A (1919) O Schistosoma mansoni e a schistosomose segundo observações feitas no Brasil. Memórias do Instituto Oswaldo Cruz 11, 121–125.CrossRefGoogle Scholar
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, 1369–1376.CrossRefGoogle Scholar
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, 322–329.CrossRefGoogle ScholarPubMed
Moraes, RG (1948) Contribuição para o estudo do Strongyloides stercoralis e da estrongiloidíase no Brasil. Revista de Saúde Pública 1, 507–624.Google Scholar
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, 3368–3372.CrossRefGoogle ScholarPubMed
Ritchie, LS (1948) An ether sedimentation technique for routine stoll examination. Bulletin of the US Army Medicine Department 8, 326–340.Google Scholar
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, 129–154.CrossRefGoogle ScholarPubMed
Schniering, A, Schade, R and Hiepe, T (1996) Development of an IgY-based assay for the detection of Ascaris suum antigens. ALTEX 13, 62–65.Google ScholarPubMed
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. 25–64.CrossRefGoogle Scholar
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, 134–138.CrossRefGoogle ScholarPubMed
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, 442–445.CrossRefGoogle Scholar
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, 354–357.CrossRefGoogle ScholarPubMed
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, 727–733.CrossRefGoogle ScholarPubMed
World Health Organization (2019) Teniasis/Cisticercosis. Fact-sheets. Geneva, Switzerland: World Health Organization.Google Scholar
Supplementary material: Image

Carrara et al. supplementary material

Figure S1

Download Carrara et al. supplementary material(Image)
Image 188.3 KB