Detection of Nonhemagglutinating Influenza A(H3) Viruses by Enzyme-Linked Immunosorbent Assay in Quantitative Influenza Virus Culture

Baalen, Carel A. van; Els, C.; Beek, Ruud van; Vries, Erhard van der; Osterhaus, Albert D. M. E.; Rimmelzwaan, Guus F.

doi:10.1128/jcm.03575-13

Cited by 34 publications

(26 citation statements)

References 26 publications

(25 reference statements)

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“…Initially, the A(H3N2) virus in the 2014-2015 season could not be cultured efficiently with the widely used MDCK cells when measuring the virus titer; consequently, the virus titer of the 2014-2015 season virus could not be obtained by this traditional method. As has been reported previously [15], this was because of the change of receptor-binding properties of the hemagglutinin of the recent prevalent virus. MDCK-SIAT1 cells, which express enhanced levels of α-2,6-linked sialic acid receptors, have the potential to improve the growth of A (H3N2) viruses to a higher titer than that obtained with MDCK cells [15].…”

Section: Cell Culturementioning

confidence: 57%

“…As has been reported previously [15], this was because of the change of receptor-binding properties of the hemagglutinin of the recent prevalent virus. MDCK-SIAT1 cells, which express enhanced levels of α-2,6-linked sialic acid receptors, have the potential to improve the growth of A (H3N2) viruses to a higher titer than that obtained with MDCK cells [15]. These results (Supplemental figure) indicated that titer measurements using MDCK-SIAT1 cells can be applied to all viruses obtained from the 2013-2015 seasons.…”

Section: Cell Culturementioning

confidence: 57%

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Clinical and virologic effects of four neuraminidase inhibitors in influenza A virus-infected children (aged 4–12 years): an open-label, randomized study in Japan

Hirotsu¹,

Saisho

Hasegawa

et al. 2017

Expert Review of Anti-infective Therapy

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Section: Cell Culturementioning

confidence: 57%

Section: Cell Culturementioning

confidence: 57%

Clinical and virologic effects of four neuraminidase inhibitors in influenza A virus-infected children (aged 4–12 years): an open-label, randomized study in Japan

Hirotsu¹,

Saisho

Hasegawa

et al. 2017

Expert Review of Anti-infective Therapy

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“…Recently, the circulating strains of A/H3N2 influenza virus have displayed a phenomenon of reduced hemagglutination activity. The mechanistic explanation for this appears to be the presence of amino acid substitutions in the receptor binding site of the HA molecule (3). This mutation poses a technical challenge for the use of the HI assay for both antigenic analysis and measurement of serologic immune response to vaccination against the A/H3N2 strain; a concern most acute for cell-derived vaccines because of their similarity to the circulating virus (4,5).…”

mentioning

confidence: 99%

Comparability of Titers of Antibodies against Seasonal Influenza Virus Strains as Determined by Hemagglutination Inhibition and Microneutralization Assays

Heeringa¹,

Leav

Smolenov

et al. 2020

J Clin Microbiol

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We compared hemagglutination inhibition (HI) and microneutralization (MN) assays pre- and post-vaccination antibody titers against A/H1N1, A/H3N2, and B influenza strains using data from two vaccine trials: Study 1 with a cell-grown trivalent influenza vaccine (TIVc) using cell-grown target virus in both assays and Study 2 with an egg-grown adjuvanted quadrivalent influenza vaccine (aQIVe) using egg-grown target virus. The relationships between HI- and MN-derived log-transformed titers were examined using different statistical techniques. Deming regression analyses showed point estimates for slopes generally close to 1 across studies and strains. The slope of regression was closest to 1 for A/H3N2 strain when either cell- or egg-grown viral target virus was used. Bland-Altman plots indicated a very small percentage of results outside 2 and 3 standard deviations. The magnitude and direction of differences between titers in the two assays varied by study and strain. Mean differences favored the MN assay for A/H1N1 and B strains in Study 1, whereas HI resulted in higher titers compared to MN against the A/H3N2 strain. In Study 2, mean differences favored the MN assay for A/H3N2 and B strains. Overall the direction and magnitude of mean differences were similar between the two vaccines. The concordance correlation coefficients ranged from 0.74 (A/H1N1 strain, Study 1) to 0.97 (A/H3N2 strain, Study 1). The comparative analysis demonstrates an overall strong positive correlation between HI and MN assays. These data support the use of the MN assay to quantify the immune response of influenza vaccines in clinical studies, particularly for A/H3N2 strain.

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“…Since the early 2000s, several groups have observed changes in the haemagglutination behaviour of influenza A(H3N2) viruses, i.e. reduced haemagglutination of commonly used erythrocytes (turkey, chicken and guinea pig erythrocytes) and poor inhibition of haemagglutination by reference post-infection ferret antisera [11,[18][19][20][21][22]. In addition to the changes in the haemagglutination behaviour of HA, the NA activity of influenza A(H3N2) viruses isolated between 2005 and 2009 was also affected [18].…”

Section: Introductionmentioning

confidence: 99%

Neuraminidase-mediated haemagglutination of recent human influenza A(H3N2) viruses is determined by arginine 150 flanking the neuraminidase catalytic site

Mögling

Richard

Vliet

et al. 2017

Journal of General Virology

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Over the last decade, an increasing proportion of circulating human influenza A(H3N2) viruses exhibited haemagglutination activity that was sensitive to neuraminidase inhibitors. This change in haemagglutination as compared to older circulating A(H3N2) viruses prompted an investigation of the underlying molecular basis. Recent human influenza A(H3N2) viruses were found to agglutinate turkey erythrocytes in a manner that could be blocked with either oseltamivir or neuraminidase-specific antisera, indicating that agglutination was driven by neuraminidase, with a low or negligible contribution of haemagglutinin. Using representative virus recombinants it was shown that the haemagglutinin of a recent A(H3N2) virus indeed had decreased activity to agglutinate turkey erythrocytes, while its neuraminidase displayed increased haemagglutinating activity. Viruses with chimeric and mutant neuraminidases were used to identify the amino acid substitution histidine to arginine at position 150 flanking the neuraminidase catalytic site as the determinant of this neuraminidase-mediated haemagglutination. An analysis of publicly available neuraminidase gene sequences showed that viruses with histidine at position 150 were rapidly replaced by viruses with arginine at this position between 2005 and 2008, in agreement with the phenotypic data. As a consequence of neuraminidase-mediated haemagglutination of recent A(H3N2) viruses and poor haemagglutination via haemagglutinin, haemagglutination inhibition assays with A(H3N2) antisera are no longer useful to characterize the antigenic properties of the haemagglutinin of these viruses for vaccine strain selection purposes. Continuous monitoring of the evolution of these viruses and potential consequences for vaccine strain selection remains important.

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Detection of Nonhemagglutinating Influenza A(H3) Viruses by Enzyme-Linked Immunosorbent Assay in Quantitative Influenza Virus Culture

Cited by 34 publications

References 26 publications

Clinical and virologic effects of four neuraminidase inhibitors in influenza A virus-infected children (aged 4–12 years): an open-label, randomized study in Japan

Clinical and virologic effects of four neuraminidase inhibitors in influenza A virus-infected children (aged 4–12 years): an open-label, randomized study in Japan

Comparability of Titers of Antibodies against Seasonal Influenza Virus Strains as Determined by Hemagglutination Inhibition and Microneutralization Assays

Neuraminidase-mediated haemagglutination of recent human influenza A(H3N2) viruses is determined by arginine 150 flanking the neuraminidase catalytic site

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