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