Recombinant envelope protein-based enzyme immunoassay for IgG antibodies is comparable to neutralization tests for epidemiological studies of dengue infection

Journal of Virological Methods

Volumn 187, Issue 1, 2013, Pages 114-120

  Rocha, Eliseu Soares de Oliveira ^a   de Oliveira, Jaquelline Germano ^a,b   dos Santos, João Rodrigues ^a   Rodrigues, Gisele Olinto Libânio ^a   Figueiredo, Leandra Barcelos ^a   Pessanha, José Eduardo Marques ^c   Proietti, Fernando Augusto ^a   da Fonseca, Flávio Guimarães ^a   Bonjardim, Claudio Antonio ^a   Ferreira, Paulo Cesar Peregrino ^a   Kroon, Erna Geessien ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Prefeitura Municipal de Belo Horizonte   (Brazil)

Author keywords

Dengue virus; Diagnosis; ELISA; Recombinant envelope proteins; Serology

Indexed keywords

ENVELOPE PROTEIN; IMMUNOGLOBULIN G ANTIBODY; RECOMBINANT ANTIGEN;

ANIMAL CELL; ANTIBODY DETECTION; ANTIBODY TITER; ARTICLE; BLOOD SAMPLING; DENGUE; DENGUE VIRUS; DENGUE VIRUS 1; DENGUE VIRUS 2; DENGUE VIRUS 3; DENGUE VIRUS 4; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; ELISA KIT; ENZYME IMMUNOASSAY; HUMAN; HUMAN EXPERIMENT; IMMUNOGLOBULIN G ENZYME IMMUNOASSAY; INTERMETHOD COMPARISON; NONHUMAN; NORMAL HUMAN; PLAQUE REDUCTION NEUTRALIZATION TEST; PREDICTIVE VALUE; PRIORITY JOURNAL; PROCESS DEVELOPMENT; RECEIVER OPERATING CHARACTERISTIC; REFERENCE VALUE; SENSITIVITY AND SPECIFICITY; SERODIAGNOSIS; SEROEPIDEMIOLOGY; VIRUS NEUTRALIZATION;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; DENGUE; DENGUE VIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOGLOBULIN G; NEUTRALIZATION TESTS; RECOMBINANT PROTEINS; SENSITIVITY AND SPECIFICITY; SEROEPIDEMIOLOGIC STUDIES; SEROLOGIC TESTS; VIRAL ENVELOPE PROTEINS;

ARBOVIRUS; DENGUE VIRUS;

EID: 84871780272     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2012.09.012     Document Type: Article

References (49)

1. ANVISA, 2003. Projeto de Avaliação Comparativa dos Produtos para Uso Diagnóstico in vitro para Dengue. Brasilia. Available at: (accessed 21.12.11). http://www.anvisa.gov.br/.
2. Buerano C.C., Ibrahim I.N., Contreras R.C., Hasebe F., Matias R.R., Natividad F.F., Igarashi A. IgM-capture ELISA of serum samples collected from Filipino dengue patients. The Southeast Asian Journal of Tropical Medicine and Public Health 2000, 31:524-529.
3. Clements D.E., Coller B.A., Lieberman M.M., Ogata S., Wang G., Harada K.E., Putnak J.R., Ivy J.M., McDonell M., Bignami G.S., Peters I.D., Leung J., Weeks-Levy C., Nakano E.T., Humphreys T. Development of a recombinant tetravalent dengue virus vaccine: immunogenicity and efficacy studies in mice and monkeys. Vaccine 2010, 28:2705-2715.
4. Cuzzubbo A.J., Vaughn D.W., Nisalak A., Solomon T., Kalayanarooj S., Aaskov J., Dung N.M., Devine P.L. Comparison of PanBio dengue duo enzyme-linked immunosorbent assay (ELISA) and MRL dengue fever virus immunoglobulin M capture ELISA for diagnosis of dengue virus infections in Southeast Asia. Clinical and Diagnostic Laboratory Immunology 1999, 6:705-712.
5. Cuzzubbo A.J., Endy T.P., Nisalak A., Kalayanarooj S., Vaughn D.W., Ogata S.A., Clements D.E., Devine P.L. Use of recombinant envelope proteins for serological diagnosis of dengue virus infection in an immunochromatographic assay. Clinical and Diagnostic Laboratory Immunology 2001, 8:150-155.
6. Deen J.L., Harris E., Wills B., Balmaseda A., Hammond S.N., Rocha C., Dung N.M., Hung N.T., Hien T.T., Farrar J.J. The WHO dengue classification and case definitions: time for a reassessment. Lancet 2006, 368:170-173.
7. Delenda C., Staropoli I., Frenkiel M.P., Cabanié L., Deubel V. Analysis of C-terminally truncated dengue 2 and dengue 3 virus envelope glycoproteins: processing in insect cells and immunogenic properties in mice. Journal of General Virology 1994, 75:1569-1578.
8. de Paula S.O., Fonseca B.A. Dengue: a review of the laboratory tests a clinician must know to achieve a correct diagnosis. Brazilian Journal of Infectious Diseases 2004, 8:390-398.
9. dos Santos F.B., Miagostovich M.P., Nogueira R.M., Schatzmayr H.G., Riley L.W., Harris E. Analysis of recombinant dengue virus polypeptides for dengue diagnosis and evaluation of the humoral immune response. American Journal of Tropical Medicine and Hygiene 2004, 71:144-152.
10. dos Santos F.B., Nogueira R.M., Lima M.R., De Simone T.S., Schatzmayr H.G., Lemes E.M., Harris E., Miagostovich M.P. Recombinant polypeptide antigen-based immunoglobulin G enzyme-linked immunosorbent assay for serodiagnosis of dengue. Clinical and Vaccine Immunology 2007, 14:641-643.
11. Figueiredo R.M.P., Thatcher B.D., Lima M.L., Almeida T.C., Alecrim W.D., Guerra M.V. Exanthematous diseases and the first epidemic of dengue to occur in Manaus, Amazonas State, Brazil, during 1998-1999. Revista da Sociedade Brasileira de Medicina Tropical 2004, 37:476-479.
12. Gubler D.J. Epidemic dengue/dengue hemorrhagic fever as a public health social and economic problem in the 21st century. Trends in Microbiology 2002, 10:100-103.
13. Guzmán M.G., Kourí G. Dengue diagnosis advances and challenges. International Journal of Infectious Diseases 2004, 8:69-80.
14. Halstead S.B. Dengue. Lancet 2007, 370:1644-1652.
15. Koraka P., Zeller H., Niedrig M., Osterhaus A.D., Groen J. Reactivity of serum samples from patients with a flavivirus infection measured by immunofluorescence assay and ELISA. Microbes and Infection 2002, 4:1209-1215.
16. Lai C.Y., Tsai W.Y., Lin S.R., Kao C.L., Hu H.P., King C.C., Wu H.C., Chang G.J., Wang W.K. Antibodies to envelope glycoprotein of dengue virus during the natural course of infection are predominantly cross-reactive and recognize epitopes containing highly conserved residues at the fusion loop of domain II. Journal of Virology 2008, 82:6631-6643.
17. Lima V.L.C., Figueiredo L.T.M., Correa Filho H.R., Leite O.F., Rangel O., Vido A.A., Oliveira S.S., Owa M.A., Carlucci R.H. Dengue fever: a post-epidemic sero-epidemiological survey in an urban area setting at a northwestern county of São Paulo State, Brazil. Revista de Saude Publica 1999, 33:566-574.
18. Lima V.L., Rangel O., Andrade V.R., Silveira N.Y., Oliveira S.S., Figueiredo L.T. Dengue: sero-epidemiological survey and virological surveillance in Campinas, São Paulo, Brazil. Cadernos de Saude Publica 2007, 23:669-680.
19. Lin B., Parrish C.R., Murray J.M., Wright P.J. Localization of a neutralizing epitope on the envelope protein of dengue virus type 2. Virology 1994, 202:885-890.
20. Ludolfs D., Schilling S., Altenschmidt J., Schmitz H. Serological differentiation of infections with dengue virus serotypes 1 to 4 by using recombinant antigens. Journal of Clinical Microbiology 2002, 40:4317-4320.
21. Makino Y., Tadano M., Arakaki S., Fukunaga T. Potential use of a baculovirus-expressed dengue-4 E protein as a diagnostic antigen in regions endemic for dengue and Japanese encephalitis. American Journal of Tropical Medicine and Hygiene 1991, 45:636-643.
22. Men R.H., Bray M., Lai C.J. Carboxy-terminally truncated dengue virus envelope glycoproteins expressed on the cell surface and secreted extracellularly exhibit increased immunogenicity in mice. Journal of Virology 1991, 65(3):1400-1407.
23. Men R., Wyatt L., Tokimatsu I., Arakaki S., Shameem G., Elkins R., Chanock R., Moss B., Lai C.J. Immunization of rhesus monkeys with a recombinant of modified vaccinia virus Ankara expressing a truncated envelope glycoprotein of dengue type 2 virus induced resistance to dengue type 2 virus challenge. Vaccine 2000, 18:3113-3122.
24. Morens D.M., Halstead S.B., Larsen L.K. Comparison of dengue virus plaque reduction neutralization by macro and semi-micro methods in LLC-MK2 cells. Microbiology and Immunology 1985, 29:1197-1205.
25. Nawa M., Yamada K.I., Takasaki T., Akatsuka T., Kurane I. Serotype-cross-reactive immunoglobulin M responses in dengue virus infections determined by enzyme-linked immunosorbent assay. Clinical and Diagnostic Laboratory Immunology 2000, 7:774-777.
26. Nunes M.R., Nunes Neto J.P., Casseb S.M., Nunes K.N., Martins L.C., Rodrigues S.G., Matheus S., Dussart P., Casseb L.M., Vasconcelos P.F. Evaluation of an immunoglobulin M-specific capture enzyme-linked immunosorbent assay for rapid diagnosis of dengue infection. Journal of Virological Methods 2011, 171:13-20.
27. Osanai C.H., Travassos da Rosa A.P., Tang A.T., do Amaral R.S., Passos A.D., Tauil P.L. Dengue outbreak in Boa Vista Roraima preliminary report. Revista do Instituto de Medicina Tropical de Sao Paulo 1983, 25:53-54.
28. Palmer C.J., King S.D., Cuadrado R.R., Perez E., Baum M., Ager A.L. Evaluation of the MRL diagnostics dengue fever virus IgM capture ELISA and the PanBio Rapid Immunochromatographic Test for diagnosis of dengue fever in Jamaica. Journal of Clinical Microbiology 1999, 37:1600-1601.
29. Parida M.M., Upadhyay C., Saxena P., Dash P.K., Jana A.M., Seth P. Evaluation of a dipstick ELISA and a rapid immunochromatographic test for diagnosis of Dengue virus infection. Acta Virologica 2001, 45:299-304.
30. Pessanha J.E., Caiaffa W.T., Kroon E.G., Proietti F.A. Dengue fever in three sanitary districts in the city of Belo Horizonte Brazil: a population-based seroepidemiological survey, 2006 to 2007. Revista Panamericana de Salud Publica 2010, 27:252-258.
31. Putnak, R., 1994. Progress in the development of recombinant vaccines against dengue and other arthropod-borne flaviviruses. In: Kurstak, E. (Ed.), Modern Vaccinology. Plenum Publishing Corp., New York.
32. Putnak J.R., Coller B.A., Voss G., Vaughn D.W., Clements D., Peters I., Bignami G., Houng H.S., Chen R.C., Barvir D.A., Seriwatana J., Cayphas S., Garçon N., Gheysen D., Kanesa-Thasan N., McDonell M., Humphreys T., Eckels K.H., Prieels J.P., Innis B.L. An evaluation of dengue type-2 inactivated recombinant subunit, and live-attenuated vaccine candidates in the rhesus macaque model. Vaccine 2005, 23:4442-4452.
33. Raviprakash K., Kochel T.J., Ewing D., Simmons M., Phillips I., Hayes C.G., Porter K.R. Immunogenicity of dengue virus type 1 DNA vaccines expressing truncated and full length envelope protein. Vaccine 2000, 18:2426-2434.
34. Rivetz B., Siman-Tov D., Ambal E., Jaramillo A.C., Ben-Zvi A., Tartakovsky B., Fish F. New dengue antibody assay with unique differential detection of IgG and IgM antibodies. Clinical Biochemistry 2009, 42:180-184.
35. Russell P.K., Nisalak A., Sukhavachana P., Vivona S. A plaque reduction test for dengue virus neutralizing antibodies. Journal of Immunology 1967, 99:285-290.
36. Sathish N., Manayani D.J., Shankar V., Abraham M., Nithyanandam G., Sridharan G. Comparison of IgM capture ELISA with a commercial rapid immunochromatographic card test & IgM microwell ELISA for the detection of antibodies to dengue viruses. Indian Journal of Medical Research 2002, 115:31-36.
37. Siqueira J.B., Martelli C.M., Maciel I.J., Oliveira R.M., Ribeiro M.G., Amorim F.P., Moreira B.C., Cardoso D.D., Souza W.V., Andrade A.L. Household survey of dengue infection in central Brazil: spatial point pattern analysis and risk factors assessment. American Journal of Tropical Medicine and Hygiene 2004, 71:646-651.
38. SVS (Secretaria de Vigilância em Saúde). Informe Epidemiológico da Dengue, Janeiro a Dezembro de 2007. Available at: (accessed 21.12.11). http://portal.saude.gov.br/.
39. Teixeira M.G., Costa M.C., Barreto M.L., Mota E. Dengue and dengue hemorrhagic fever epidemics in Brazil: what research is needed based on trends, surveillance, and control experiences?. Cadernos de Saude Publica 2005, 21:1307-1315.
40. Thomas S.J., Nisalak A., Anderson K.B., Libraty D.H., Kalayanarooj S., Vaughn D.W., Putnak R., Gibbons R.V., Jarman R., Endy T.P. Dengue plaque reduction neutralization test (PRNT) in primary and secondary dengue virus infections How alterations in assay conditions impact performance. American Journal of Tropical Medicine and Hygiene 2009, 81:825-833.
41. Tripathi N.K., Babu J.P., Shrivastva A., Parida M., Jana A.M., Rao P.V. Production and characterization of recombinant dengue virus type 4 envelope domain III protein. Journal of Biotechnology 2008, 134:278-286.
42. Vasconcelos P.F., Lima J.W., Raposo M.L., Rodrigues S.G., da Rosa J.F., Amorim S.M., da Rosa E.S., Moura C.M., Fonseca N., da Rosa A.P. A seroepidemiological survey on the island of São Luis during a dengue epidemic in Maranhão. Revista da Sociedade Brasileira de Medicina Tropical 1999, 32:171-179.
43. Vasconcelos P.F., Mota K., Straatmann A., Santos-Torres S., da Rosa A.P., Tavares Neto J. A dengue epidemic in Ipupiara and Prado Bahia. A seroepidemiologic survey. Revista da Sociedade Brasileira de Medicina Tropical 2000, 33:61-67.
44. Vaughn D.W., Nisalak A., Solomon T., Kalayanarooj S., Nguyen M.D., Kneen R., Cuzzubbo A., Devine P.L. Rapid serologic diagnosis of dengue virus infection using a commercial capture ELISA that distinguishes primary and secondary infections. American Journal of Tropical Medicine and Hygiene 1999, 60:693-698.
45. Videa E., Coloma M.J., dos Santos F.B., Balmaseda A., Harris E. Immunoglobulin M enzyme-linked immunosorbent assay using recombinant polypeptides for diagnosis of dengue. Clinical and Diagnostic Laboratory Immunology 2005, 12:882-884.
46. WHO, 2007. Guidelines for Plaque Reduction Neutralizing Testing of Human Antibodies to Dengue Viruses. Geneva, Switzerland.
47. Wu S.J., Hanson B., Paxton H., Nisalak A., Vaughn D.W., Rossi C., Henchal E.A., Porter K.R., Watts D.M., Hayes C.G. Evaluation of a dipstick enzyme-linked immunosorbent assay for detection of antibodies to dengue virus. Clinical and Diagnostic Laboratory Immunology 1997, 4:452-457.
48. Yew Y.W., Ye T., Ang L.W., Ng L.C., Yap G., James L., Chew S.K., Goh K.T. Seroepidemiology of dengue virus infection among adults in Singapore. Annals of the Academy of Medicine, Singapore 2009, 38:667-675.
49. Zweig M.H., Campbell G. Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clinical Chemistry 1993, 39:561-577.