Skip to main content

Advertisement

Log in

Immunodiagnosis of human neurocysticercosis: comparative performance of serum diagnostic tests in Mexico

  • Helminthology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Immunodiagnosis has a supportive role in the diagnosis of neurocysticercosis (NCC). The aim of this study was to compare the validity of seven immunodiagnostic tests among serum samples from 58 patients with NCC, 26 patients with neurological diseases other than NCC, and 15 healthy controls. One test for viable parasite detection (HP10 antigen assay) and six for antibody detection were evaluated. For the entire sample, sensitivities ranged from 55.2% (NOVALISA) to 81.0% (enzyme-linked immunosorbent assay [ELISA] Taenia solium antibody), with the sensitivity of the latter test significantly higher than that of the in-house ELISA Taenia crassiceps, NOVALISA, enzyme-linked immunoelectrotransfer blot (EITB) CDC, and HP10. Overall, specificities were high, ranging from 85.4% (ELISA Ts) to 97.1% (NOVALISA), with no statistically significant differences. Detection of HP10 antigen was significantly associated with the presence of vesicular parasites. The simple and low-cost ELISA Taenia solium antibody Ab instead of EITB is recommended to support NCC diagnosis in both rural and hospital settings in Mexico.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arruda GC, da Silva AD, Quagliato EM, Maretti MA, Rossi CL (2005) Evaluation of Taenia solium and Taenia crassiceps cysticercal antigens for the serodiagnosis of neurocysticercosis. Tropical Med Int Health 10:1005–1012

    Article  CAS  Google Scholar 

  • Bobes RJ, Hernández M, Márquez C, Fragoso G, García E, Parkhouse RM, Harrison LJ, Sciutto E, Fleury A (2006) Subarachnoidal and intraventricular human neurocysticercosis: application of an antigen detection assay for the diagnosis and follow-up. Tropical Med Int Health 11:943–950

    Article  Google Scholar 

  • Brandt JRA, Geerts S, De Deken R, Kumar V, Ceulemans F, Brijs L, Falla N (1992) A monoclonal antibody-based ELISA for the detection of circulating excretory-secretory antigens in Taenia saginata cysticercosis. Int J Parasitol 22:471–477. https://doi.org/10.1016/0020-7519(92)90148-E

    Article  CAS  PubMed  Google Scholar 

  • Cardona-Arias JA, Carrasquilla-Agudelo YE, Restrepo-Posada DC (2017) Validity of three methods for inmuno-diagnostic of neurocysticercosis: systematic review of the literature with meta-analysis 1960-2014. Rev Chil Infectol 34:33–44. https://doi.org/10.4067/S0716-10182017000100005

    Article  Google Scholar 

  • Carod JF, Randrianarison M, Razafimahefa J, Mamitiana Ramahefarisoa R, Rakotondrazaka M, Debruyne M, Dautigny M, Cazalf P, Lalaoarisoa Andriantseheno M, Ramarokoto Charles E (2012) Evaluation of the performance of 5 commercialized enzyme immunoassays for the detection of Taenia solium antibodies and for the diagnosis of neurocysticercosis. Diagn Microbiol Infect Dis 72:85–89. https://doi.org/10.1016/j.diagmicrobio.2011.09.014

    Article  CAS  PubMed  Google Scholar 

  • Carpio A, Fleury A, Romo ML, Abraham R, Fandiño J, Durán JC, Cárdenas G, Moncayo J, Leite Rodrigues C, San-Juan D, Serrano-Dueñas M, Takayanagui O, Sander JW (2016) New diagnostic criteria for neurocysticercosis: reliability and validity. Ann Neurol 80:434–442. https://doi.org/10.1002/ana.24732

    Article  PubMed  PubMed Central  Google Scholar 

  • Donadeu M, Fahrion AS, Olliaro PL, Abela-Ridder B (2017) Target product profiles for the diagnosis of Taenia solium taeniasis, neurocysticercosis and porcine cysticercosis. PLoS Negl Trop Dis 11:e0005875. https://doi.org/10.1371/journal.pntd.0005875

    Article  PubMed  PubMed Central  Google Scholar 

  • Estrada JJ, Kuhn RE (1985) Immunochemical detection of antigens of larval Taenia solium and anti-larval antibodies in the cerebrospinal fluid of patients with neurocysticercosis. J Neurol Sci 71:39–48

    Article  CAS  PubMed  Google Scholar 

  • Fleury A, Hernández M, Fragoso G, Parkhouse RM, Harrison LJ, Sciutto E (2003) Detection of secreted cysticercal antigen: a useful tool in the diagnosis of inflammatory neurocysticercosis. Trans R Soc Trop Med Hyg 97:542–546

    Article  CAS  PubMed  Google Scholar 

  • Fleury A, Hernández M, Avila M, Cárdenas G, Bobes RJ, Huerta M, Fragoso G, Uribe-Campero L, Harrison LJ, Parkhouse RM, Sciutto E (2007) Detection of HP10 antigen in serum for diagnosis and follow-up of subarachnoidal and intraventricular human neurocysticercosis. J Neurol Neurosurg Psychiatry 78:970–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabriël S, Blocher J, Dorny P, Abatih EN, Schmutzhard E, Ombay M, Mathias B, Winkler AS (2012) Added value of antigen ELISA in the diagnosis of neurocysticercosis in resource poor settings. PLoS Negl Trop Dis 6:e1851. https://doi.org/10.1371/journal.pntd.0001851

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia HH, O'Neal SE, Noh J, Handali S, Cysticercosis Working Group in Peru (2018a) Laboratory diagnosis of neurocysticercosis (Taenia solium). J Clin Microbiol 56:e00424–e00418. https://doi.org/10.1128/JCM.00424-18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia HH, Castillo Y, Gonzales I, Bustos JA, Saavedra H, Jacob L, Del Brutto OH, Wilkins PP, Gonzalez AE, Gilman RH, Cysticercosis Working Group in Peru (2018b) Low sensitivity and frequent cross-reactions in commercially available antibody detection ELISA assays for Taenia solium cysticercosis. Tropical Med Int Health 23:101–105. https://doi.org/10.1111/tmi.13010

    Article  CAS  Google Scholar 

  • Harrison LJS, Joshua GWP, Wright SH, Parkhouse RME (1989) Specific detection of circulating surface/secreted glycoproteins of viable cysticerci in Taenia saginata cysticercosis. Parasite Immunol 11:351–370. https://doi.org/10.1111/j.1365-3024.1989.tb00673.x

    Article  CAS  PubMed  Google Scholar 

  • Kojic EM, White AC Jr (2003) A positive enzyme-linked immunoelectrotransfer blot assay result for a patient without evidence of cysticercosis. Clin Infect Dis 36:e7–e9

    Article  PubMed  Google Scholar 

  • Larralde C, Laclette JP, Owen CS, Madrazo I, Sandoval M, Bojalil R, Sciutto E, Contreras L, Arzate J, Diaz ML et al (1986) Reliable serology of Taenia solium cysticercosis with antigens from cyst vesicular fluid: ELISA and hemagglutination tests. Am J Trop Med Hyg 35:965–973

    Article  CAS  PubMed  Google Scholar 

  • Maravilla P, Gonzalez-Guzman R, Zuñiga G, Peniche A, Dominguez-Alpizar JL, Reyes-Montes R, Flisser A (2008) Genetic polymorphism in Taenia solium cysticerci recovered from experimental infections in pigs. Infect Genet Evol 8:213–216. https://doi.org/10.1016/j.meegid.2007.11.006

    Article  CAS  PubMed  Google Scholar 

  • Michelet L, Fleury A, Sciutto E, Kendjo E, Fragoso G, Paris L, Bouteille B (2011) Human neurocysticercosis: comparison of different diagnostic tests using cerebrospinal fluid. J Clin Microbiol 49:195–200. https://doi.org/10.1128/JCM.01554-10

    Article  CAS  PubMed  Google Scholar 

  • Nieto D (1956) Cysticercosis of the nervous system. Diagnosis by means of the spinal fluid complement fixation text. Neurology 6:725–738

    Article  CAS  PubMed  Google Scholar 

  • O'Neal SE, Flecker RH (2015) Hospitalization frequency and charges for neurocysticercosis, United States, 2003-2012. Emerg Infect Dis 21:969–976. https://doi.org/10.3201/eid2106.1413243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parkhouse RME, Carpio A, Campoverde A, Sastre P, Rojas G, Cortez MM (2018) Reciprocal contribution of clinical studies and the HP10 antigen ELISA for the diagnosis of extraparenchymal neurocysticercosis. Acta Trop 178:119–123. https://doi.org/10.1016/j.actatropica.2017.11.005

    Article  CAS  PubMed  Google Scholar 

  • Proaño-Narvaez JV, Meza-Lucas A, Mata-Ruiz O, García-Jerónimo RC, Correa D (2002) Laboratory diagnosis of human neurocysticercosis: double-blind comparison of enzyme-linked immunosorbent assay and electroimmunotransfer blot assay. J Clin Microbiol 40:2115–2118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos-Kuri M, Montoya RM, Padilla A, Govezensky T, Díaz ML, Sciutto E, Sotelo J, Larralde C (1992) Immunodiagnosis of neurocysticercosis. Disappointing performance of serology (enzyme-linked immunosorbent assay) in an unbiased sample of neurological patients. Arch Neurol 49:633–636

    Article  CAS  PubMed  Google Scholar 

  • Suzuki LA, Arruda GC, Quagliato EM, Rossi QL (2007) Evaluation of Taenia solium and Taenia crassiceps cysticercal antigens for immunodiagnosis of neurocysticercosis using ELISA on cerebrospinal fluid samples. Rev Soc Bras Med Trop 40:152–155

    Article  PubMed  Google Scholar 

  • Torgerson PR, Devleesschauwer B, Praet N, Speybroeck N, Willingham AL, Kasuga F, Rokni MB, Zhou XN, Fèvre EM, Sripa B, Gargouri N, Fürst T, Budke CM, Carabin H, Kirk MD, Angulo FJ, Havelaar A, de Silva N (2015) World Health Organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: a data synthesis. PLoS Med 12:e1001920. https://doi.org/10.1371/journal.pmed.1001920

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsang VC, Brand JA, Boyer AE (1989) An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis 159:50–59

    Article  CAS  PubMed  Google Scholar 

  • Vega R, Piñero 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. Int J Parasitol 33:1479–1485

    Article  CAS  PubMed  Google Scholar 

  • Wilson M, Bryan RT, Fried JA, Ware DA, Schantz PM, Pilcher JB, Tsang VC (1991) Clinical evaluation of the cysticercosis enzyme-linked immunoelectrotransfer blot in patients with neurocysticercosis. J Infect Dis 164:1007–1009

    Article  CAS  PubMed  Google Scholar 

  • Zea-Vera A, Cordova EG, Rodriguez S, Gonzales I, Pretell EJ, Castillo Y, Castro-Suarez S, Gabriël S, Tsang VC, Dorny P, Garcia HH, Cysticercosis working group in Peru (2013) Parasite antigen in serum predicts the presence of viable brain parasites in patients with apparently calcified cysticercosis only. Clin Infect Dis 57:e154–e159. https://doi.org/10.1093/cid/c

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was partially supported by the “Programa Iberoamericano de Ciencia y TecnologÍa para el Desarrollo, CYTED” [211RT0432] and by the “Programa de Investigación para el Desarrollo y la Optimización de Vacunas, Inmunomoduladores y Métodos Diagnósticos del IIB” (PROVACADI, Instituto de Investigaciones Biomédicas, UNAM, México).

Author information

Authors and Affiliations

Authors

Contributions

This study was designed, supervised, and coordinated by RMEP, TG, ES, and AF. MH, OGA, GD, JLRA, AML, RGR, and AT carried out the clinical assessment and the immunoassays; MLR and AF carried out the analysis and interpretation of these data. JLRA, RMEP, ES, and AF drafted the manuscript. All authors critically revised the manuscript for intellectual content, read, and approved the final manuscript. ES and AF are guarantors of the paper.

Corresponding author

Correspondence to Agnès Fleury.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Section Editor: David Bruce Conn

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Dr. Teresa Garate passed away before the submission of the final version of this manuscript.

Electronic supplementary material

ESM 1

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hernández, M., Astudillo, OG., Diego, G. et al. Immunodiagnosis of human neurocysticercosis: comparative performance of serum diagnostic tests in Mexico. Parasitol Res 118, 2891–2899 (2019). https://doi.org/10.1007/s00436-019-06425-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06425-4

Keywords

Navigation