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Diagnostic accuracy of somatic and excretory−secretory antigens from Strongyloides venezuelensis infective larvae for the immunodiagnosis of human strongyloidiasis

Published online by Cambridge University Press:  05 July 2021

William Henry Roldán Gonzáles
Affiliation:
Laboratório de Imunopatologia da Esquistossomose (Laboratório de Investigação Médica, LIM-06) Hospital das Clínicas, Faculdade de Medicina Universidade de São Paulo, São Paulo, Brazil
Dirce Mary Correia Lima Meisel
Affiliation:
Laboratório de Imunopatologia da Esquistossomose (Laboratório de Investigação Médica, LIM-06) Hospital das Clínicas, Faculdade de Medicina Universidade de São Paulo, São Paulo, Brazil
Fabiana Martins de Paula*
Affiliation:
Laboratório de Imunopatologia da Esquistossomose (Laboratório de Investigação Médica, LIM-06) Hospital das Clínicas, Faculdade de Medicina Universidade de São Paulo, São Paulo, Brazil Instituto de Medicina Tropical, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
Ronaldo Cesar Borges Gryschek
Affiliation:
Laboratório de Imunopatologia da Esquistossomose (Laboratório de Investigação Médica, LIM-06) Hospital das Clínicas, Faculdade de Medicina Universidade de São Paulo, São Paulo, Brazil Instituto de Medicina Tropical, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil
*
Author for correspondence: Fabiana Martins de Paula, E-mail: [email protected]

Abstract

To evaluate the diagnostic accuracy of three types of antigenic preparations from Strongyloides venezuelensis infective larvae for detection of serum IgG anti-Strongyloides antibodies by enzyme-linked immunosorbent assay (ELISA). Soluble somatic fractions (SSF) and membrane somatic fractions (MSF) and excretory−secretory (E/S) products from S. venezuelensis infective larvae were evaluated against 71 sera from individuals with strongyloidiasis, 105 sera from healthy individuals, and 84 sera from individuals with other helminth infections. Using an ELISA cut-off for 100% sensitivity, E/S products were 97.88% specific followed by MSF (93.12%) and then by SSF (85.2%). The occurrence of cross-reactivity with other helminths was 4.76% (4/84) with E/S products, 8.33% (7/84) with MSF, and 17.86% (15/84) with SSF. For a cut-off for 100% specificity, E/S products showed a sensitivity of 88.73% whereas MSF and SSF showed sensitivities of 59.15% and 53.52%, respectively. In conclusion, E/S products were the best antigenic option for the serodiagnosis of human strongyloidiasis.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Brindley, PJ, Gam, AA, Pearce, EJ, Poindexter, RW and Neva, FA (1988) Antigens from the surface and excretions/secretions of the filariform larva of Strongyloides stercoralis. Molecular and Biochemical Parasitology 28, 171180.CrossRefGoogle ScholarPubMed
Buonfrate, D, Requena-Mendez, A, Angheben, A, Cinquini, M, Cruciani, M, Fittipaldo, A, Giorli, G, Gobbi, F, Piubelli, C and Bisoffi, Z (2018) Accuracy of molecular biology techniques for the diagnosis of Strongyloides stercoralis infection: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 12, e0006229.CrossRefGoogle ScholarPubMed
Buonfrate, D, Bisanzio, D, Giorli, G, Odermatt, P, Fürst, T, Greenaway, C, French, M, Reithinger, R, Gobbi, F, Montresor, A and Bisoffi, Z (2020) The global prevalence of Strongyloides stercoralis infection. Pathogens (Basel, Switzerland) 9, 468.Google ScholarPubMed
Casado, L, Rodriguez-Guardado, A, Boga, JA, Fernández-Suarez, J, Martínez-Camblor, P, Rodríguez-Perez, M, García-Pérez, A, Vazquez, F and Gascon, J (2019) Use of serology in a systematic screening programme for strongyloidiasis in an immigrant population. International Journal of Infectious Diseases 88, 6064.CrossRefGoogle Scholar
Conway, DJ, Atkins, NS, Lillywhite, JE, Bailey, JW, Robinson, RD, Lindo, JF, Bundy, DA and Bianco, AE (1993) Immunodiagnosis of Strongyloides stercoralis infection: a method for increasing the specificity of the indirect ELISA. Transactions of the Royal Society of Tropical Medical and Hygiene 87, 173176.CrossRefGoogle ScholarPubMed
Corral, MA, Paula, FM, Gottardi, M, Meisel, DM, Chieffi, PP and Gryschek, RC (2015a) Membrane fractions from Strongyloides venezuelensis in the immunodiagnosis of human strongyloidiasis. Revista do Instituto de Medicina Tropical de São Paulo 57, 7780.CrossRefGoogle ScholarPubMed
Corral, MA, Paula, FM, Gottardi, M, Meisel, DM, Castilho, VL, Gonçalves, EM, Chieffi, PP and Gryschek, RC (2015b) Immunodiagnosis of human strongyloidiasis: use of six different antigenic fractions from Strongyloides venezuelensis parasitic females. Revista do Instituto de Medicina Tropical de São Paulo 57, 427430.CrossRefGoogle ScholarPubMed
Corral, MA, Paula, FM, Meisel, DM, Castilho, VL, Gonçalves, EM, Levy, D, Bydlowski, SP, Chieffi, PP, Castro-Borges, W and Gryschek, RC (2017) Potential immunological markers for diagnosis of human strongyloidiasis using heterologous antigens. Parasitology 144, 124130.CrossRefGoogle ScholarPubMed
Cunha, RA, de Carvalho, EFG, de Sousa, JEN and Costa-Cruz, JM (2017) Excretory/secretory antigens of Strongyloides venezuelensis applied to IgG detection in human strongyloidosis. Parasitology International 66, 671676.CrossRefGoogle ScholarPubMed
Eamudomkarn, C, Sithithaworn, P, Sithithaworn, J, Kaewkes, S, Sripa, B and Itoh, M (2015) Comparative evaluation of Strongyloides ratti and S. stercoralis larval antigen for diagnosis of strongyloidiasis in an endemic area of opisthorchiasis. Parasitology Research 114, 25432551.CrossRefGoogle Scholar
Eusebi, P (2013) Diagnostic accuracy measures. Cerebrovascular Diseases 36, 267272.CrossRefGoogle ScholarPubMed
Feliciano, ND, Gonzaga, HT, Gonçalves-Pires Mdo, R, Gonçalves, AL, Rodrigues, RM, Ueta, MT and Costa-Cruz, JM (2010) Hydrophobic fractions from Strongyloides venezuelensis for use in the human immunodiagnosis of strongyloidiasis. Diagnostic Microbiology and Infectious Disease 67, 153161.CrossRefGoogle ScholarPubMed
Gonçalves, AL, Rocha, CA, Gonzaga, HT, Gonçalves-Pires Mdo, R, Ueta, MT and Costa-Cruz, JM (2012) Specific IgG and IgA to larvae, parthenogenetic females, and eggs of Strongyloides venezuelensis in the immunodiagnosis of human strongyloidiasis. Diagnostic Microbiology and Infectious Disease 72, 7984.CrossRefGoogle ScholarPubMed
Harnett, W (2014) Secretory products of helminth parasites as immunomodulators. Molecular and Biochemical Parasitology 195, 130136.CrossRefGoogle ScholarPubMed
Kalantari, N, Chehrazi, M, Ghaffari, S and Gorgani-Firouzjaee, T (2020) Serological assays for the diagnosis of Strongyloides stercoralis infection: a systematic review and meta-analysis of diagnostic test accuracy. Transactions of the Royal Society of Tropical Medical and Hygiene 114, 459469.CrossRefGoogle ScholarPubMed
Koga, K, Kasuya, S, Khamboonruang, C, Sukhavat, K, Ieda, M, Takatsuka, N, Kita, K and Ohtomo, H (1991) A modified agar plate method for detection of Strongyloides stercoralis. American Journal of Tropical Medicine and Hygiene 45, 518521.CrossRefGoogle ScholarPubMed
Koosha, S, Fesharaki, M and Rokni, MB (2004) Comparison of enzyme-linked immunosorbent assay and indirect immunofluorescence assay in the diagnosis of human strongyloidiasis. Indian Journal of Gastroenterology 23, 214216.Google ScholarPubMed
Lightowlers, MW and Rickard, MD (1988) Excretory−secretory products of helminth parasites: effects on host immune responses. Parasitology 96, S123S166.CrossRefGoogle ScholarPubMed
Lok, JB (2007) Strongyloides Stercoralis: A Model for Translational Research on Parasitic Nematode Biology. In Elegans C, The elegans Research Community, WormBook, pp. 118. doi:10.1895/wormbook.1.134.1Google Scholar
Lowry, OH, Rosebrough, NJ, Farr, AL and Randall, RJ (1951) Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265275.CrossRefGoogle ScholarPubMed
Maeda, Y, Palomares-Rius, JE, Hino, A, Afrin, T, Mondal, SI, Nakatake, A, Maruyama, H and Kikuchi, T (2019) Secretome analysis of Strongyloides venezuelensis parasitic stages reveals that soluble and insoluble proteins are involved in its parasitism. Parasite and Vectors 12, 21.CrossRefGoogle ScholarPubMed
Marcos, LA, Terashima, A, Dupont, HL and Gotuzzo, E (2008) Strongyloides hyperinfection syndrome: an emerging global infectious disease. Transactions of the Royal Society of Tropical Medical and Hygiene 102, 314318.CrossRefGoogle ScholarPubMed
Norsyahida, A, Riazi, M, Sadjjadi, SM, Muhammad Hafiznur, Y, Low, HC, Zeehaida, M and Noordin, R (2013) Laboratory detection of strongyloidiasis: IgG-, IgG4 – and IgE-ELISAs and cross-reactivity with lymphatic filariasis. Parasite Immunology 35, 174179.CrossRefGoogle ScholarPubMed
Nunes, JB, Emídio, TCO, Marques, MJ, Caldas, IS, Souza, RLM, Kanamura, HY and Costa-Cruz, JM (2018) Seroepidemiological aspects of human infection by Strongyloides stercoralis in Alfenas, southern Minas Gerais, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 51, 855859.CrossRefGoogle ScholarPubMed
Nutman, TB (2017) Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology 144, 263273.CrossRefGoogle ScholarPubMed
Requena-Méndez, A, Chiodini, P, Bisoffi, Z, Buonfrate, D, Gotuzzo, E and Muñoz, J (2013) The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Neglected Tropical Diseases 7, e2002.CrossRefGoogle ScholarPubMed
Rokni, MB and Kia, EB (2005) Evaluation of enzyme- linked immunosorbaent assay, using somatic and excretory−secretory antigens of Strongyloides stercoralis for the serodiagnosis of strongyloidosis. Iranian Journal of Public Health 34, 812.Google Scholar
Soblik, H, Younis, AE, Mitreva, M, Renard, BY, Kirchner, M, Geisinger, F, Steen, H and Brattig, NW (2011) Life cycle stage-resolved proteomic analysis of the excretome/secretome from Strongyloides ratti-identification of stage-specific proteases. Molecular & Cellular Proteomics 10, M111.010157.CrossRefGoogle ScholarPubMed
Tello, R, Terashima, A, Marcos, LA, Machicado, J, Canales, M and Gotuzzo, E (2012) Highly effective and inexpensive parasitological technique for diagnosis of intestinal parasites in developing countries: spontaneous sedimentation technique in tube. International Journal of Infectious Diseases 16, e414e416.CrossRefGoogle ScholarPubMed
Toledo, B, Corral, MA, Meisel, DMCL, Gottardi, M, Abdala, E, Costa, SF, Pierrotti, LC, Lescano, SAZ, Gonçalves, EMN, Castilho, VLP, Chieffi, PP, Gryschek, RCB and Paula, FM (2019) Screening of Strongyloides infection using an ELISA test in transplant candidates. Clinics 74, e698.CrossRefGoogle Scholar
Tsang, VC, Brand, JA and Boyer, AE (1989) An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). The Journal of Infectious Diseases 159, 5059.CrossRefGoogle ScholarPubMed
Vadlamudi, RS, Chi, DS and Krishnaswamy, G (2006) Intestinal strongyloidiasis and hyperinfection syndrome. Clinical and Molecular Allergy 4, 8.CrossRefGoogle ScholarPubMed
Viney, M and Kikuchi, T (2017) Strongyloides ratti and S. venezuelensis: rodent models of Strongyloides infection. Parasitology 144, 285294.CrossRefGoogle ScholarPubMed
White, MAF, Whiley, H and Ross, KE (2019) A review of Strongyloides spp. environmental sources worldwide. Pathogens (Basel, Switzerland) 8, 91.Google Scholar