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      Detection of anti‐NS1 antibodies after pandemic influenza exposure: Evaluation of a serological method for distinguishing H1N1pdm09 infected from vaccinated cases

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          Abstract

          Background

          Reliable exposure information is crucial for assessing health outcomes of influenza infection and vaccination. Current serological methods are unable to distinguish between anti‐hemagglutinin (HA) antibodies induced by infection or vaccination.

          Objectives

          We aimed to explore an alternative method for differentiating influenza infection and vaccination.

          Methods

          Sera from animals inoculated with influenza viruses or purified H1N1pdm09 HA were obtained. Human samples were selected from a pregnancy cohort established during the 2009 H1N1 pandemic. Unvaccinated, laboratory‐confirmed cases (N = 18), vaccinated cases without influenza‐like‐illness (N = 18) and uninfected, unvaccinated controls (N = 18) were identified based on exposure data from questionnaires, national registries and maternal hemagglutination inhibition (HI) titres at delivery. Animal and human samples were tested for antibodies against the non‐structural protein 1 (NS1) and HA from H1N1pdm09, using a Luciferase Immunoprecipitation System (LIPS).

          Results

          Anti‐NS1 H1N1pdm09 antibodies were detected in sera from experimentally infected, but not from vaccinated, animals. Anti‐HA H1N1pdm09 antibodies were detectable after either of these exposures. In human samples, 28% of individuals with laboratory‐confirmed influenza were seropositive for H1N1pdm09 NS1, whereas vaccinated cases and controls were seronegative. There was a trend for H1N1pdm09 NS1 seropositive cases reporting more severe and longer duration of symptomatic illness than seronegative cases. Anti‐HA H1N1pdm09 antibodies were detected in all cases and in 61% of controls.

          Conclusions

          The LIPS method could differentiate between sera from experimentally infected and vaccinated animals. However, in human samples obtained more than 6 months after the pandemic, LIPS was specific, but not sufficiently sensitive for ascertaining cases by exposure.

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          Most cited references20

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          Serologic assays for influenza surveillance, diagnosis and vaccine evaluation.

          Xiyan Xu, Kathy Hancock, Mindy J. Katz (2011)
          Serological techniques play a critical role in various aspects of influenza surveillance, vaccine development and evaluation, and sometimes in diagnosis, particularly for novel influenza virus infections of humans. Because individuals are repeatedly exposed to antigenically and genetically diverse influenza viruses over a lifetime, the gold standard for detection of a recent influenza virus infection or response to current vaccination is the demonstration of a seroconversion, a fourfold or greater rise in antibody titer relative to a baseline sample, to a circulating influenza strain or vaccine component. The hemagglutination-inhibition assay remains the most widely used assay to detect strain-specific serum antibodies to influenza. The hemagglutination-inhibition assay is also used to monitor antigenic changes among influenza viruses which are constantly evolving; such antigenic data is essential for consideration of changes in influenza vaccine composition. The use of the hemagglutinin-specific microneutralization assay has increased, in part, owing to its sensitivity for detection of human antibodies to novel influenza viruses of animal origin. Neutralization assays using replication-incompetent pseudotyped particles may be advantageous in some laboratory settings for detection of antibodies to influenza viruses with heightened biocontainment requirements. The use of standardized protocols and antibody standards are important steps to improve reproducibility and interlaboratory comparability of results of serologic assays for influenza viruses.
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            Estimating the annual attack rate of seasonal influenza among unvaccinated individuals: A systematic review and meta-analysis

            Anthony Newall, Liam J. Dwyer, Robin M Turner … (2018)
            Article 0 comments Cited 74 times – based on 0 reviews     Review now
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              Complications and outcomes of pandemic 2009 Influenza A (H1N1) virus infection in hospitalized adults: how do they differ from those in seasonal influenza?

              Karry L. K. Ngai, Jessica Lee, Paul K S Chan … (2011)
              It is unclear whether pandemic 2009 influenza A (pH1N1) infection caused more significant disease among hospitalized adults than seasonal influenza. A prospective, observational study was conducted in adults hospitalized with polymerase chain reaction-confirmed pH1N1 infection in 2 acute-care general hospitals from June 2009 to May 2010 (n = 382). Complications and outcomes were described and compared with those in a seasonal influenza cohort (2007-2008, same hospitals; n = 754). Hospitalized patients with pH1N1 influenza were younger than those with seasonal influenza (mean age ± standard deviation, 47 ± 20 vs 70 ± 19 years) and fewer had comorbid conditions (48% vs 64%). The rate of positive immunofluorescence assay results was low (54% vs 84%), and antiviral use was frequent (96% vs 52%). Most patients in both cohorts developed complicated illnesses (67.8% vs 77.1%), but patients with pH1N1 influenza had higher rates of extrapulmonary complications (23% vs 16%; P = .004) and intensive care unit admission and/or death (patient age 65 years, 13.5% vs 8.5%; adjusted odds ratio [OR] 2.13; 95% confidence interval [CI], 1.25-3.62; P = .005). Patients who received antiviral treatment within 96 h after onset had better survival (log-rank test, P < .001). However, without timely treatment, the mortality risk was higher with pH1N1 infection (9.0% vs 5.8% for seasonal influenza; adjusted OR, 6.85; 95% CI, 1.64-28.65; P = .008]. Bacterial superinfection worsened outcomes. Adults hospitalized for pH1N1 influenza had significant complications and mortality despite being younger than patients with seasonal influenza. Antiviral treatment within 96 h may improve survival.
              Article 0 comments Cited 63 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Anna Hayman Robertson:
                ORCID: https://orcid.org/0000-0001-6295-0528
                Anna.Hayman.Robertson@fhi.no
                Journal
                Journal ID (nlm-ta): Influenza Other Respir Viruses
                Journal ID (iso-abbrev): Influenza Other Respir Viruses
                Journal ID (doi): 10.1111/(ISSN)1750-2659
                Journal ID (publisher-id): IRV
                Title: Influenza and Other Respiratory Viruses
                Publisher: John Wiley and Sons Inc. (Hoboken )
                ISSN (Print): 1750-2640
                ISSN (Electronic): 1750-2659
                Publication date (Electronic): 19 January 2020
                Publication date (Print): May 2020
                Volume: 14
                Issue: 3 ( doiID: 10.1111/irv.v14.3 )
                Pages: 294-301
                Affiliations
                [ 1 ] Division of Infection Control and Environmental Health Norwegian Institute of Public Health Oslo Norway
                [ 2 ] Center for Infection and Immunity Mailman School of Public Health Columbia University New York NY USA
                [ 3 ] KG Jebsen Center for Influenza Vaccine Research Oslo Norway
                [ 4 ] WHO National Influenza Centre Oslo Norway
                [ 5 ]Present address: GSK Biologicals S.A. Wavre Belgium
                Author notes
                [*] [* ] Correspondence

                Anna Hayman Robertson, Division of Infection Control and Environmental Health, Norwegian Institute of Public Health, Oslo, Norway.

                Email: Anna.Hayman.Robertson@ 123456fhi.no

                Author information
                https://orcid.org/0000-0001-6295-0528
                https://orcid.org/0000-0002-8280-8243
                Article
                Publisher ID: IRV12712
                DOI: 10.1111/irv.12712
                PMC ID: 7182603
                PubMed ID: 31955522
                SO-VID: 374d3d57-aff2-4001-9cf2-b99d406d8832
                Copyright © © 2019 The Authors. Influenza and Other Respiratory Viruses Published by John Wiley & Sons Ltd.
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 12 June 2019
                Date revision received : 05 December 2019
                Date accepted : 08 December 2019
                Page count
                Figures: 2, Tables: 1, Pages: 8, Words: 5335
                Funding
                Funded by: Norwegian Ministry of Health and Care Services
                Funded by: Research Council of Norway , open-funder-registry 10.13039/501100005416;
                Award ID: 221122
                Funded by: Norwegian Institute of Public Health
                Funded by: KG Jebsen Centre for Influenza Vaccine Research
                Funded by: Jane Botsford Johnson Foundation
                Categories
                Subject: Original Article
                Subject: Original Articles
                Custom metadata
                source-schema-version-number 2.0
                cover-date May 2020
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.1 mode:remove_FC converted:24.04.2020

                ScienceOpen disciplines: Infectious disease & Microbiology
                Keywords: h1n1pdm09,influenza,ns1,pandemic,serology,vaccination
                Data availability:
                ScienceOpen disciplines: Infectious disease & Microbiology
                Keywords: h1n1pdm09, influenza, ns1, pandemic, serology, vaccination

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