SARI surveillance
During the 2020/21 season, only Belgium and Malta reported SARI data, but only Belgium reported 144 cases identified among 682 patients tested (21% positivity). This compares to an average of 200 detections from 7 countries in pre-COVID-19 pandemic seasons (Table 1). Detections peaked in week 20/2021 with 55% positivity (n=17) (Figure 1D, E). Of the 480 patients with known age (all from Belgium), 136 tested positive (28% positivity), with children ≤4 years representing 90% of patients (41% positivity). Children aged 5 to 14 years saw 26% positivity which was higher than in the oldest age group (7%) (Table 2).
During the 2021 inter-season, seven countries (Armenia, Belgium, Georgia, Ireland, Malta, Russian Federation and Ukraine) reported SARI data with a total of 148 RSV detections from 1,983 patients (7% positivity). This compares to up to 15 detections from up to three countries in pre-COVID-19 pandemic seasons (Table 1, Supplementary Table 1). Between weeks 24 and 37/2021, the percentage positivity ranged between 2% and 9%, except for week 30/2021 when no detections were reported. Percentage positivity peaked in week 39/2021 at 10%, leading into the 2021/22 season (Figure 1E, supplementary Figure 3). When possible to compare with sentinel systems (Georgia, Ireland, Russian Federation and Ukraine), all countries but Ireland saw a delayed peak in SARI positivity after the one in sentinel detections. Among 898 patients with known age tested in five countries, 89 (10%) were positive. Children ≤4 years accounted for 81% (n=72) of all cases with known age, and 18% of their samples tested positive for RSV. Only Belgium reported over 10% positivity in another age group (those ≥65 years) (Figure 3, Table 2).
During the 2021/22 season, 948 SARI cases were reported among 9,478 patients tested (10% positivity) in 16 countries (Figure 1 D, E, Table 1). A peak of 25% positivity was observed in week 47/2021 in Georgia and Türkiye, after which it fell until week 3/2022 and mostly ranged between 1% and 5% until the end of the season (Figure 1E). Among 5,220 patients with known age, 569 detections (11%) were reported by 12 countries. These included 506 (89%) in children ≤4 years and 13 (2%) in persons ≥65 years with a percentage positivity of 20% and 1%, respectively (Table 2). Positive specimens in the youngest age group peaked at the start of the season and in week 18/2022 (Figure 3).
During the 2022 inter-season, 136 RSV detections were reported from 4,238 patients tested (3% positivity) in 11 countries, with positivity ranging between 1% and 6% and peaking in week 24/2022 (Table 1, Figure 1E, Supplementary Table 1, Supplementary figure 3). Of the 32 cases reported with known age, 29 were ≤ 4 years from 6 countries (4% positivity) (Table 2).

Discussion

We showed that the COVID-19 pandemic and its response has impacted the circulation of RSV in Europe since the Autumn of 2020. Very little circulation was seen during the 2020/21 season, but unusual inter-seasonal activity was seen in summer 2021, followed by early and high peaks of activity during the 2021/22 season as observed in all surveillance systems. This atypical inter-seasonal activity continued in many countries in the summer months of 2022. Hospitalised cases of RSV have been predominantly in those aged ≤4 years.
Although countries included in this analysis have tested more specimens from sentinel surveillance systems for RSV during the COVID-19 pandemic than in prior seasons, fewer viruses were detected during the usual weeks of RSV circulation of the 2020/21 season. The similar findings from three separate surveillance systems (primary care sentinel, non-sentinel and SARI) and a higher number of countries reporting compared to pre-COVID-19 pandemic seasons provide some assurance that this is a true observation of reduced circulation of RSV, likely due to the impact of public health and social measures in the early phase of the pandemic rather than a change in testing practices.
Many countries also observed an unusual increase in RSV activity in the summer months of 2021 and 2022, representing out-of-season activity, in all systems, usually translating into an early start of the next epidemic season. In primary care sites in some countries (Denmark, Germany and Slovenia, among others), the 2021/22 season began earlier than during pre-COVID-19-pandemic seasons. In other parts of the Region (such as in France, Ireland and the Netherlands among others), seasonality returned to similar timing to those observed in pre-COVID-19-pandemic seasons, but with much higher positivity. Both observations may be associated with the lack of RSV circulation observed during the 2020/21 season and hence a widespread lack of exposure to RSV, particularly in younger cohorts, resulting in the build-up of an increased pool of susceptibles.
When comparing SARI activity to historical data, a higher peak of detections was seen late in the 2020/21 season and early during the 2021/22 season. Due to a lack of historical denominator data, it was not possible to compare the patterns of positivity. Children aged ≤4 years were disproportionately more affected than any other age group, accounting for at least 89% of all SARI cases during all four periods considered whereas those aged ≥65 years accounted for 2% of cases, fewer than would be expected 15. This may be a result of PHSM against COVID-19 and continued behavioural changes, especially in older generations, such as continued social distancing or mask wearing even after measures have been lifted. However, it may also be explained by some countries (in eastern Europe and Central Asia) having a lower threshold for hospitalising young children than other age groups3 or changing their testing practices during the COVID-19 pandemic.
Previous studies have looked at the importance of RSV infection causing hospitalisation in the first two years of life 7,16. Given that children born during the COVID-19 pandemic are unlikely to have been exposed to RSV in their first or second year of life, it is possible that when they are older, the severity of a primary RSV infection is reduced. However, it is also possible that the number of children hospitalised during the 2022/23 season will still be greater due to the large number of RSV-naïve children born since the start of the pandemic, resulting in a high burden of disease and hospitalisation rate 5. Combined with hospitalisations resulting from other respiratory viruses across all age groups, RSV has the potential to cause high pressure on healthcare systems across the Region8.
This significant shift in circulation patterns was also observed in other parts of the world where RSV typically also circulates during the winter months such as in Australia and New Zealand5,10 or South Africa 5,8,10,17. RSV circulation was not uniform across these countries, with some experiencing stronger than expected out-of-season activity8, while others experienced delayed or continued circulation 5. A delayed circulation of RSV during the summer months had previously been reported after the 2009 A(H1N1) influenza pandemic 18. The overall reduction in transmission was a very possible result of PHSM implemented (such as mask wearing, stay-at-home orders and school orders) to restrict the spread of SARS-CoV-2 within and between countries 9 by breaking transmission chains. We know this implementation was neither uniform between countries nor over time and may be an important factor; similar results were found by other groups 19.
This analysis contains several limitations, including the limited and varying number of countries that report data through various surveillance systems, some of which are not an integral part of routine surveillance but have been part of ECDC projects initiated during the COVID-19 pandemic. Changes in testing practices and number of reporting sites because of the COVID-19-pandemic were not considered here. The MEM thresholds were based on only four historical seasons, and very few countries could be included due to the intermittent absence of weekly data or denominators. The interpretation of the calculated epidemic thresholds should therefore be taken with caution, and do not necessarily represent the national epidemic threshold that are set by the individual countries. There were too few countries for a robust investigation into geo-temporal patterns of increased activity across countries in the Region. The lack non-sentinel denominator data did not allow systematic percentage positivity calculations, a potential weakness of this data source when interpreted alone. However, the consistency of non-sentinel trends with those from other surveillance systems provides some reassurance to the validity of the results. Additionally, the availability of age data for sentinel, non-sentinel and historical SARI surveillance systems would have allowed a better understanding of which age groups have been most affected by these unusual circulation patterns and whether children were overrepresented. Finally, the limited number of countries reporting SARI age data may not be representative of the Region (also given that these countries are mostly located in its Eastern part) or of the age distribution of patients at large (it is unclear if cases have an a priori equal chance of being tested for RSV regardless of their age). Unfortunately, the absence of historical SARI denominator data and the large age groups into which cases are grouped do not allow for more detailed interpretation of our results. In addition, during the COVID-19 pandemic there was varying degrees of disruption to national sentinel surveillance systems due to changes in health seeking behaviours and limitations in the capacity of sites to receive cases and take specimens, impacting the ability of these systems to monitor respiratory viruses, including RSV.
Despite these limitations, this descriptive study illustrates how the emergence of a novel respiratory virus and associated public health measures can significantly disrupt the circulation of established seasonal respiratory viruses. It is likely that absence of circulation of seasonal respiratory pathogens during a season led to out-of-season activity, and potentially, to larger than expected peaks of activity thereafter, as observed in summer 2021 and the early 2021/22 season. RSV activity during the 2022/23 season continues to follow unusual patterns and the implementation of integrated surveillance systems monitoring multiple respiratory viruses simultaneously may prove invaluable to both monitor RSV and other seasonal viral respiratory infections, but also in planning for the future emergence of a novel pandemic respiratory virus.

Conclusion

The emergence and spread of SARS-CoV-2 and associated control measures in the EU/EEA and in the WHO European Region have significantly impacted the spread and timing of seasonal respiratory viruses such as RSV. For the last two winter seasons, and for the summer periods in between, much higher proportions of RSV detections or a temporal shift in transmissions were detected compared to pre-COVID-19 pandemic seasons. Further work is required to determine the possible explanatory factors including the implementation and relaxation in PHSM and factors such as possible SARS-CoV-2 viral interference to this shift in timing, activity and potential difference in age distribution of RSV cases. These results highlight the importance of being aware of and preparing for continued potential unusual patterns in the epidemiology of RSV (and other respiratory viruses). It is also a lesson learnt with regard to the impact of future emergence and spread of respiratory viruses with pandemic potential on the epidemiology of seasonal respiratory viruses.
Addendum :
The WHO European Region respiratory network group authorship consists of:
Anissa Lakhani2, Maria Zambon2, Odette Popovici3, Mihaela Lazăr4, Amela Dedeić Ljubović5, Nina Rodić Vukmir6, 7, Ayşe Başak Altaş8, Emine Avci8, Katarzyna Łuniewska9, Karol Szymański9, Greta Gargasiene10, Svajune Muralyte11, Ausra Dziugyte12, Graziella Zahra12, Ana Rita Gonçalves13, Tania Spedaliero13, Guillaume Fournier14, Daniel Alvarez-Vaca14, Goranka Petrović15, Irena Tabain15, Katarina Prosenc16, Maja Socan17, Jelena Protic18, Dragana Dimitrijevic19, Alina Druc20, Mariana Apostol20, Kate Karolina Kalasnikova21, Sergejs Nikisins22, Janine Reiche23, Wei Cai23, Adam Meijer24, Anne Teirlinck24, Amparo Larrauri25, Inmaculada Casas25, Vincent Enouf26, Sophie Vaux27, Frederikke Kristensen Lomholt28, Ramona Trebbien28, Helena Jirincova29, Helena Sebestova29, Mónika Rózsa30, Zsuzsanna Molnár30, Gudrun Aspelund31, Gudrun Erna Baldvinsdottir32, Simon Cottrell33, Catherine Moore33, Athanasios Kossyvakis34, Kassiani Mellou35, Olga Sadikova36, Johanna Kristina Tamm36, Nathalie Bossuyt37, Isabelle Thomas37, Edita Staroňová38, Lyudmila Kudasheva39, Boris Pleshkov39, Niina Ikonen40, Otto Helve40, Emma Dickson41, Tanya Curran42, Kseniya Komissarova43, Kirill Stolyarov43, Veronika Vysotskaya44, Natallia Shmialiova45, Božidarka Rakočević46, Danijela Vujošević46, Romella Abovyan47, Shushan Sargsyan47, Khatuna Zakhashvili48, Ann Machablishvili48, Oksana Koshalko49, Iryna Demchyshyna49, Michal Mandelboim50, Aharona Glatman-Freedman50, Rory Gunson51, Shivani Karanwal52, Raquel Guiomar53, Ana Paula Rodrigues54, Charlene Bennett54, Lisa Domegan55, Arijana Kalaveshi56, Xhevat Jakupi56, Gurbangul Ovliyakulova57, Neli Korsun58, Nadezhda Vladimirova58