Distinguishing Secondary Dengue Virus Infection From Zika Virus Infection With Previous Dengue by a Combination of 3 Simple Serological Tests

Overview

Journal Clin Infect Dis

Publisher Oxford University Press

Specialty Infectious Diseases

Date 2017 Oct 12

PMID 29020159

Citations 41

Authors

Wen-Yang Tsai

Han Ha Youn

Carlos Brites

Jih-Jin Tsai

Jasmine Tyson

Celia Pedroso

Jan Felix Drexler

Mars Stone

Graham Simmons

Michael P Busch

Marion Lanteri

Susan L Stramer

Angel Balmaseda

Eva Harris

Wei-Kung Wang

Affiliations

Soon will be listed here.

Abstract

Background: The explosive spread of Zika virus (ZIKV) and associated microcephaly present an urgent need for sensitive and specific serodiagnostic tests, particularly for pregnant women in dengue virus (DENV)-endemic regions. Recent reports of enhanced ZIKV replication by dengue-immune sera have raised concerns about the role of previous DENV infection on the risk and severity of microcephaly and other ZIKV complications.

Methods: Enzyme-linked immunosorbent assays (ELISAs) based on ZIKV and DENV nonstructural protein 1 (NS1) were established to test acute, convalescent phase, and post-convalescent phase serum/plasma samples from reverse-transcription polymerase chain reaction-confirmed cases including 20 primary ZIKV, 25 ZIKV with previous DENV, 58 secondary DENV, and 16 primary DENV1 infections.

Results: ZIKV-NS1 immunoglobulin M (IgM) and immunoglobulin G (IgG) ELISAs combined can detect ZIKV infection with a sensitivity of 95% and specificity of 66.7%. The ZIKV-NS1 IgG cross-reactivity by samples from secondary DENV infection cases ranged from 66.7% to 28.1% (within 1 month to 1-2 years post-illness, respectively). Addition of DENV1-NS1 IgG ELISA can distinguish primary ZIKV infection; the ratio of absorbance of ZIKV-NS1 to DENV1-NS1 IgG ELISA can distinguish ZIKV with previous DENV and secondary DENV infections with a sensitivity of 87.5% and specificity of 81.3%. These findings were supported by analysis of sequential samples.

Conclusions: An algorithm for ZIKV serodiagnosis based on 3 simple ELISAs is proposed to distinguish primary ZIKV, ZIKV with previous DENV, and secondary DENV infections; this could be applied to serodiagnosis for ZIKV, serosurveillance, and monitoring ZIKV infection during pregnancy to understand the epidemiology, pathogenesis, and complications of ZIKV in dengue-endemic regions.

Citing Articles

Detection of anti-premembrane antibody as a specific marker of four flavivirus serocomplexes and its application to serosurveillance in endemic regions.

Chen G, Dai Y, Hsieh S, Tsai J, Sy A, Jiz M Emerg Microbes Infect. 2024; 13(1):2301666.

PMID: 38163752 PMC: 10810658. DOI: 10.1080/22221751.2023.2301666.

Arbovirus surveillance in pregnant women in north-central Nigeria, 2019-2022.

Ogwuche J, Chang C, Ige O, Sagay A, Chaplin B, Kahansim M J Clin Virol. 2023; 169:105616.

PMID: 37944259 PMC: 10841754. DOI: 10.1016/j.jcv.2023.105616.

Re-mining serum proteomics data reveals extensive post-translational modifications upon Zika and dengue infection.

Allgoewer K, Wu S, Choi H, Vogel C Mol Omics. 2023; 19(4):308-320.

PMID: 36810580 PMC: 10175154. DOI: 10.1039/d2mo00258b.

Development of a Molecular Aptamer Beacon Applied to Magnetic-Assisted RNA Extraction for Detection of Dengue and Zika Viruses Using Clinical Samples.

da Silva A, Goulart L, Loffler P, Code C, Neves A Int J Mol Sci. 2022; 23(22).

PMID: 36430340 PMC: 9693377. DOI: 10.3390/ijms232213866.

Development of an Anti-Zika and Anti-Dengue IgM ELISA Assay: Evaluation of Cross Reactivity and Validation.

Cerutti H, Tesi G, Soldatini C, Bandini T, Castria M, Brogi A Trop Med Infect Dis. 2022; 7(11).

PMID: 36355890 PMC: 9693240. DOI: 10.3390/tropicalmed7110348.

References

Brooks R, Carlos M, Myers R, White M, Bobo-Lenoci T, Aplan D . Likely Sexual Transmission of Zika Virus from a Man with No Symptoms of Infection - Maryland, 2016. MMWR Morb Mortal Wkly Rep. 2016; 65(34):915-6. DOI: 10.15585/mmwr.mm6534e2. View

Lai C, Williams K, Wu Y, Knight S, Balmaseda A, Harris E . Analysis of cross-reactive antibodies recognizing the fusion loop of envelope protein and correlation with neutralizing antibody titers in Nicaraguan dengue cases. PLoS Negl Trop Dis. 2013; 7(9):e2451. PMC: 3777924. DOI: 10.1371/journal.pntd.0002451. View

Galel S, Williamson P, Busch M, Stanek D, Bakkour S, Stone M . First Zika-positive donations in the continental United States. Transfusion. 2017; 57(3pt2):762-769. DOI: 10.1111/trf.14029. View

Kuan G, Gordon A, Aviles W, Ortega O, Hammond S, Elizondo D . The Nicaraguan pediatric dengue cohort study: study design, methods, use of information technology, and extension to other infectious diseases. Am J Epidemiol. 2009; 170(1):120-9. PMC: 2700880. DOI: 10.1093/aje/kwp092. View

Steinhagen K, Probst C, Radzimski C, Schmidt-Chanasit J, Emmerich P, Van Esbroeck M . Serodiagnosis of Zika virus (ZIKV) infections by a novel NS1-based ELISA devoid of cross-reactivity with dengue virus antibodies: a multicohort study of assay performance, 2015 to 2016. Euro Surveill. 2016; 21(50). PMC: 5291135. DOI: 10.2807/1560-7917.ES.2016.21.50.30426. View

Dejnirattisai W, Supasa P, Wongwiwat W, Rouvinski A, Barba-Spaeth G, Duangchinda T . Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat Immunol. 2016; 17(9):1102-8. PMC: 4994874. DOI: 10.1038/ni.3515. View

Priyamvada L, Quicke K, Hudson W, Onlamoon N, Sewatanon J, Edupuganti S . Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc Natl Acad Sci U S A. 2016; 113(28):7852-7. PMC: 4948328. DOI: 10.1073/pnas.1607931113. View

Lai C, Tsai W, Lin S, Kao C, Hu H, King C . 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. J Virol. 2008; 82(13):6631-43. PMC: 2447043. DOI: 10.1128/JVI.00316-08. View

Paz-Bailey G, Rosenberg E, Doyle K, Munoz-Jordan J, Santiago G, Klein L . Persistence of Zika Virus in Body Fluids - Final Report. N Engl J Med. 2017; 379(13):1234-1243. PMC: 5831142. DOI: 10.1056/NEJMoa1613108. View

10.

Van der Linden V, Pessoa A, Dobyns W, Barkovich A, Junior H, Rolim Filho E . Description of 13 Infants Born During October 2015-January 2016 With Congenital Zika Virus Infection Without Microcephaly at Birth - Brazil. MMWR Morb Mortal Wkly Rep. 2016; 65(47):1343-1348. DOI: 10.15585/mmwr.mm6547e2. View

11.

Vaughn D, Nisalak A, Solomon T, Kalayanarooj S, Nguyen M, Kneen R . Rapid serologic diagnosis of dengue virus infection using a commercial capture ELISA that distinguishes primary and secondary infections. Am J Trop Med Hyg. 1999; 60(4):693-8. DOI: 10.4269/ajtmh.1999.60.693. View

12.

Waggoner J, Gresh L, Mohamed-Hadley A, Ballesteros G, Davila M, Tellez Y . Single-Reaction Multiplex Reverse Transcription PCR for Detection of Zika, Chikungunya, and Dengue Viruses. Emerg Infect Dis. 2016; 22(7):1295-7. PMC: 4918162. DOI: 10.3201/eid2207.160326. View

13.

Paldanius M, Bloigu A, Leinonen M, Saikku P . Measurement of Chlamydia pneumoniae-specific immunoglobulin A (IgA) antibodies by the microimmunofluorescence (MIF) method: comparison of seven fluorescein-labeled anti-human IgA conjugates in an in-house MIF test using one commercial MIF and one.... Clin Diagn Lab Immunol. 2003; 10(1):8-12. PMC: 145278. DOI: 10.1128/cdli.10.1.8-12.2003. View

14.

Johnson A, Martin D, KARABATSOS N, Roehrig J . Detection of anti-arboviral immunoglobulin G by using a monoclonal antibody-based capture enzyme-linked immunosorbent assay. J Clin Microbiol. 2000; 38(5):1827-31. PMC: 86600. DOI: 10.1128/JCM.38.5.1827-1831.2000. View

15.

Wang W, Chen H, Yang C, Hsieh S, Juan C, Chang S . Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin Infect Dis. 2006; 43(8):1023-30. DOI: 10.1086/507635. View

16.

Foy B, Kobylinski K, Chilson Foy J, Blitvich B, da Rosa A, Haddow A . Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg Infect Dis. 2011; 17(5):880-2. PMC: 3321795. DOI: 10.3201/eid1705.101939. View

17.

Petersen L, Jamieson D, Powers A, Honein M . Zika Virus. N Engl J Med. 2016; 374(16):1552-63. DOI: 10.1056/NEJMra1602113. View

18.

Frey A, Di Canzio J, Zurakowski D . A statistically defined endpoint titer determination method for immunoassays. J Immunol Methods. 1999; 221(1-2):35-41. DOI: 10.1016/s0022-1759(98)00170-7. View

19.

Rabe I, Staples J, Villanueva J, Hummel K, Johnson J, Rose L . Interim Guidance for Interpretation of Zika Virus Antibody Test Results. MMWR Morb Mortal Wkly Rep. 2016; 65(21):543-6. DOI: 10.15585/mmwr.mm6521e1. View

20.

Stone M, Lanteri M, Bakkour S, Deng X, Galel S, Linnen J . Relative analytical sensitivity of donor nucleic acid amplification technology screening and diagnostic real-time polymerase chain reaction assays for detection of Zika virus RNA. Transfusion. 2017; 57(3pt2):734-747. DOI: 10.1111/trf.14031. View