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Cross-reactive immunity potentially drives global oscillation and opposed alternation patterns of seasonal influenza A viruses.

ABSTRACT: Several human pathogens exhibit distinct patterns of seasonality and circulate as pairs. For instance, influenza A virus subtypes oscillate and peak during winter seasons of the world's temperate climate zones. Alternation of dominant strains in successive influenza seasons makes epidemic forecasting a major challenge. From the start of the 2009 influenza pandemic we enrolled influenza A virus infected patients (n = 2980) in a global prospective clinical study. Complete hemagglutinin sequences were obtained from 1078 A/H1N1 and 1033 A/H3N2 viruses. We used phylodynamics to construct high resolution spatio-temporal phylogenetic hemagglutinin trees and estimated global influenza A effective reproductive numbers (R) over time (2009-2013). We demonstrate that R oscillates around R = 1 with a clear opposed alternation pattern between phases of the A/H1N1 and A/H3N2 subtypes. Moreover, we find a similar alternation pattern for the number of global viral spread between the sampled geographical locations. Both observations suggest a between-strain competition for susceptible hosts on a global level. Extrinsic factors that affect person-to-person transmission are a major driver of influenza seasonality. The data presented here indicate that cross-reactive host immunity is also a key intrinsic driver of influenza seasonality, which determines the influenza A virus strain at the onset of each epidemic season.

SUBMITTER: Gatti L

PROVIDER: S-EPMC9131982 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Cross-reactive immunity potentially drives global oscillation and opposed alternation patterns of seasonal influenza A viruses.

Gatti Lorenzo L Koenen Mischa H MH Zhang Jitao David JD Anisimova Maria M Verhagen Lilly M LM Schutten Martin M Osterhaus Ab A van der Vries Erhard E

Scientific reports 20220525 1

Several human pathogens exhibit distinct patterns of seasonality and circulate as pairs. For instance, influenza A virus subtypes oscillate and peak during winter seasons of the world's temperate climate zones. Alternation of dominant strains in successive influenza seasons makes epidemic forecasting a major challenge. From the start of the 2009 influenza pandemic we enrolled influenza A virus infected patients (n = 2980) in a global prospective clinical study. Complete hemagglutinin sequences w ...[more]

PMID: 35614123

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Project description:BackgroundMany human infectious diseases are caused by pathogens that have multiple strains and show oscillation in infection incidence and alternation of dominant strains which together are referred to as epidemic cycling. Understanding the underlying mechanisms of epidemic cycling is essential for forecasting outbreaks of epidemics and therefore important for public health planning. Current theoretical effort is mainly focused on the factors that are extrinsic to the pathogens themselves ("extrinsic factors") such as environmental variation and seasonal change in human behaviours and susceptibility. Nevertheless, co-circulation of different strains of a pathogen was usually observed and thus strains interact with one another within concurrent infection and during sequential infection. The existence of these intrinsic factors is common and may be involved in the generation of epidemic cycling of multi-strain pathogens.Methods and findingsTo explore the mechanisms that are intrinsic to the pathogens themselves ("intrinsic factors") for epidemic cycling, we consider a multi-strain SIRS model including cross-immunity and infectivity enhancement and use seasonal influenza as an example to parameterize the model. The Kullback-Leibler information distance was calculated to measure the match between the model outputs and the typical features of seasonal flu (an outbreak duration of 11 weeks and an annual attack rate of 15%). Results show that interactions among strains can generate seasonal influenza with these characteristic features, provided that: the infectivity of a single strain within concurrent infection is enhanced 2-7 times that within a single infection; cross-immunity as a result of past infection is 0.5-0.8 and lasts 2-9 years; while other parameters are within their widely accepted ranges (such as a 2-3 day infectious period and the basic reproductive number of 1.8-3.0). Moreover, the observed alternation of the dominant strain among epidemics emerges naturally from the best fit model. Alternative modelling that also includes seasonal forcing in transmissibility shows that both external mechanisms (i.e. seasonal forcing) and the intrinsic mechanisms (i.e., strain interactions) are equally able to generate the observed time-series in seasonal flu.ConclusionsThe intrinsic mechanism of strain interactions alone can generate the observed patterns of seasonal flu epidemics, but according to Kullback-Leibler information distance the importance of extrinsic mechanisms cannot be excluded. The intrinsic mechanism illustrated here to explain seasonal flu may also apply to other infectious diseases caused by polymorphic pathogens.

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Cross-reactive immunity potentially drives global oscillation and opposed alternation patterns of seasonal influenza A viruses.

Publications

Cross-reactive immunity potentially drives global oscillation and opposed alternation patterns of seasonal influenza A viruses.

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