Spread of Antigenically Drifted Influenza A(H3N2) Viruses and Vaccine Effectiveness in the United States During the 2018–2019 Season

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Abstract

Background

Increased illness due to antigenically drifted A(H3N2) clade 3C.3a influenza viruses prompted concerns about vaccine effectiveness (VE) and vaccine strain selection. We used US virologic surveillance and US Influenza Vaccine Effectiveness (Flu VE) Network data to evaluate consequences of this clade.

Methods

Distribution of influenza viruses was described using virologic surveillance data. The Flu VE Network enrolled ambulatory care patients aged ≥6 months with acute respiratory illness at 5 sites. Respiratory specimens were tested for influenza by means of reverse-transcriptase polymerase chain reaction and were sequenced. Using a test-negative design, we estimated VE, comparing the odds of influenza among vaccinated versus unvaccinated participants.

Results

During the 2018–2019 influenza season, A(H3N2) clade 3C.3a viruses caused an increasing proportion of influenza cases. Among 2763 Flu VE Network case patients, 1325 (48%) were infected with A(H1N1)pdm09 and 1350 (49%) with A(H3N2); clade 3C.3a accounted for 977 (93%) of 1054 sequenced A(H3N2) viruses. VE was 44% (95% confidence interval, 37%–51%) against A(H1N1)pdm09 and 9% (−4% to 20%) against A(H3N2); VE was 5% (−10% to 19%) against A(H3N2) clade 3C.3a viruses.

Conclusions

The predominance of A(H3N2) clade 3C.3a viruses during the latter part of the 2018–2019 season was associated with decreased VE, supporting the A(H3N2) vaccine component update for 2019–2020 northern hemisphere influenza vaccines.

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Most cited references 5

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The test-negative design for estimating influenza vaccine effectiveness.

Michael L Jackson, Jennifer C Nelson (2013)

The test-negative design has emerged in recent years as the preferred method for estimating influenza vaccine effectiveness (VE) in observational studies. However, the methodologic basis of this design has not been formally developed. In this paper we develop the rationale and underlying assumptions of the test-negative study. Under the test-negative design for influenza VE, study subjects are all persons who seek care for an acute respiratory illness (ARI). All subjects are tested for influenza infection. Influenza VE is estimated from the ratio of the odds of vaccination among subjects testing positive for influenza to the odds of vaccination among subjects testing negative. With the assumptions that (a) the distribution of non-influenza causes of ARI does not vary by influenza vaccination status, and (b) VE does not vary by health care-seeking behavior, the VE estimate from the sample can generalized to the full source population that gave rise to the study sample. Based on our derivation of this design, we show that test-negative studies of influenza VE can produce biased VE estimates if they include persons seeking care for ARI when influenza is not circulating or do not adjust for calendar time. The test-negative design is less susceptible to bias due to misclassification of infection and to confounding by health care-seeking behavior, relative to traditional case-control or cohort studies. The cost of the test-negative design is the additional, difficult-to-test assumptions that incidence of non-influenza respiratory infections is similar between vaccinated and unvaccinated groups within any stratum of care-seeking behavior, and that influenza VE does not vary across care-seeking strata. Copyright © 2013 Elsevier Ltd. All rights reserved.

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The case test-negative design for studies of the effectiveness of influenza vaccine.

Ivo Foppa, Michael Haber, Jill M Ferdinands … (2013)

A modification to the case-control study design has become popular to assess vaccine effectiveness (VE) against viral infections. Subjects with symptomatic illness seeking medical care are tested by a highly specific polymerase chain reaction (PCR) assay for the detection of the infection of interest. Cases are subjects testing positive for the virus; those testing negative represent the comparison group. Influenza and rotavirus VE studies using this design are often termed "test-negative case-control" studies, but this design has not been formally described or evaluated. We explicitly state several assumptions of the design and examine the conditions under which VE estimates derived with it are valid and unbiased. We derived mathematical expressions for VE estimators obtained using this design and examined their statistical properties. We used simulation methods to test the validity of the estimators and illustrate their performance using an influenza VE study as an example. Because the marginal ratio of cases to non-cases is unknown during enrollment, this design is not a traditional case-control study; we suggest the name "case test-negative" design. Under sets of increasingly general assumptions, we found that the case test-negative design can provide unbiased VE estimates. However, differences in health care-seeking behavior among cases and non-cases by vaccine status, strong viral interference, or modification of the probability of symptomatic illness by vaccine status can bias VE estimates. Vaccine effectiveness estimates derived from case test-negative studies are valid and unbiased under a wide range of assumptions. However, if vaccinated cases are less severely ill and seek care less frequently than unvaccinated cases, then an appropriate adjustment for illness severity is required to avoid bias in effectiveness estimates. Viral interference will lead to a non-trivial bias in the vaccine effectiveness estimate from case test-negative studies only when incidence of influenza is extremely high and duration of transient non-specific immunity is long. Copyright © 2013 Elsevier Ltd. All rights reserved.

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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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Author and article information

Journal

Title: The Journal of Infectious Diseases

Publisher: Oxford University Press (OUP)

ISSN (Print): 0022-1899

ISSN (Electronic): 1537-6613

Publication date Created: October 30 2019

Publication date (Electronic): October 30 2019

Affiliations

[1 ]Influenza Division, Centers for Disease Control and Prevention, Atlanta, Georgia

[2 ]Baylor Scott & White Health, Texas A&M University College of Medicine, Temple, Texas

[3 ]University of Pittsburgh Schools of Health Sciences and University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania

[4 ]Kaiser Permanente Washington Health Research Institute, Seattle, Washington

[5 ]University of Michigan School of Public Health, Ann Arbor, Michigan

[6 ]Marshfield Clinic Research Institute, Marshfield, Wisconsin

[7 ]Oak Ridge Institute for Science and Education Fellowship Program, Oak Ridge, Tennessee

Article

DOI: 10.1093/infdis/jiz543

PMC ID: 7325528

PubMed ID: 31665373

SO-VID: 50cc21ba-88cb-46ec-bd95-d36c4cce8427

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Spread of Antigenically Drifted Influenza A(H3N2) Viruses and Vaccine Effectiveness in the United States During the 2018–2019 Season

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Abstract

Background

Methods

Results

Conclusions

Related collections

Malaria vaccine development

Most cited references 5

The test-negative design for estimating influenza vaccine effectiveness.

The case test-negative design for studies of the effectiveness of influenza vaccine.

Serologic assays for influenza surveillance, diagnosis and vaccine evaluation.

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