Figure. Global migration dynamics of seasonal influenza viruses lineages before, during, and after COVID-19 pandemic

Supported by the National Natural Science Foundation of China (Grant Nos. 82130093, 82073613, and 823B2089), Professor Hongjie Yu’s team from Fudan University, collaborating with Professor Moritz Kraemer from Oxford University, Professor Philippe Lemey from KU Leuven, and Professor Oliver Pybus from Royal Veterinary College, has made progress in global dispersal pattern of seasonal influenza viruses. The relevant results were published online in Science on November 8, 2024, entitled "COVID-19 pandemic interventions reshaped the global dispersal of seasonal influenza viruses". The link to the paper is: https://www.science.org/doi/10.1126/science.adq3003.

Influenza viruses are featured by antigenic variability and host diversity, which can cause periodic global pandemics and threaten human health. Understanding global dispersal pattern of influenza viruses is of great scientific significance for formulating influenza prevention and control measures. The non-pharmaceutical interventions (NPIs) implemented during the COVID-19 pandemic broke the "normal" of seasonal influenza transmission, but it has not yet been revealed how changes in human behavior (especially human movement) disturb the dispersal pattern of global influenza viruses.

After combining global epidemiological surveillance data, genetic sequence data, and air traffic data, the research team divided the world into 12 regions and reconstructed the dispersal patterns of seasonal influenza viruses in four periods under Bayesian phylodynamic framework, and then estimated the relevant transmission parameters and potential drivers. The team found that the activity level of seasonal influenza viruses and inter-region air traffic both experienced a process of "decline and recovery". Under time-inhomogeneous phylodynamic framework after accommodating with genetic sequence data, inter-region air traffic (representing long-distance population movement) was identified as the main factor for the global spread of seasonal influenza viruses across four periods (pre-pandemic, acute phase of pandemic, transition phase of pandemic, and post-pandemic periods). By estimating the trunk locations in the geography-annotated phylogenetic trees, South Asia and West Asia were inferred as the key areas for maintaining the circulation of influenza A and B/Victoria viruses during the COVID-19 pandemic, respectively. To assess the similarity of transmission patterns and intensity in different influenza seasons, the team further used multidimensional scaling analysis to explore the recovery of seasonal influenza viruses transmission. The results showed that in the post-pandemic period (May 2023-March 2024), the pattern and intensity of global seasonal influenza transmission had basically returned to pre-pandemic levels (Figure).

The research team further used influenza A H3N2 virus as an example to estimate the dwell times (also referred to as persistence times) of strains circulating in Africa, Southeast Asia and South Asia, and found an increased pattern during the COVID-19 pandemic, suggesting relatively independent evolution and circulation. By constructing a hierarchical Bayesian regression model, antigenic drift and inter-region population movement were significantly associated with increased dwell time during the pandemic period. Finally, the genetic diversity and selection pressure of each seasonal influenza subtype/lineage in recent years were evaluated, and the possible reasons for the potential "disappearance" of the B/Yamagata lineage were also explored.

The study identified the dispersal patterns and key transmission areas of seasonal influenza viruses during the pandemic period, clarified the impact of NPIs in response to COVID-19 on the evolution and circulation of influenza viruses at regional level. It also highlighted robustness of global lineage dispersal patterns to substantial perturbation. The uncertainty of the emergence of novel influenza strains emphasized the importance of strengthening virological and genomic surveillance of respiratory pathogens, and timely adjusting vaccination strategies and monitoring directions, thus providing empirical evidence for future comprehensive responses to influenza epidemics.