Impact of the COVID-19 Pandemic on Acute Bronchiolitis Outbreaks: A Retrospective Study Over Five Epidemic Seasons at Clermont-Ferrand University Hospital

Background: Acute bronchiolitis outbreaks are seasonal winter phenomena caused by various viruses, primarily respiratory syncytial virus (RSV). These outbreaks lead to high hospitalization rates in infants, placing a significant burden on pediatric services. During the SARS-CoV-2 pandemic, public health measures were implemented to curb viral transmission. Objectives: To assess the impact of the COVID-19 pandemic on the incidence of hospitalized acute bronchiolitis cases at Clermont-Ferrand University Hospital. Methods: A retrospective study was conducted, including infants under 12 months of age hospitalized for acute bronchiolitis at the University Hospital of Clermont-Ferrand between September 1, 2018, and August 31, 2023. The five epidemic seasons were compared. Results : A total of 1420 patients were included. A significant decrease in bronchiolitis hospitalizations was observed in 2020–2021 compared to 2018–2019 (p=0.040), 2021–2022 (p=0.018), and 2022–2023 (p=0.001). The epidemic peak in 2020–2021 was delayed to July and involved fewer cases (36 vs. 110.8 in other years). No significant difference was found in hospital stay duration across the five epidemic seasons (p=0.109). Lockdowns were statistically associated with reduced hospitalization cases (p=0.012). Conclusion : Lockdown measures effectively limited respiratory viruses spread, particularly RSV. A marked decrease in the number of hospitalized acute bronchiolitis was observed during the 2020–2021 season, along with an unusual reduction and delay in the epidemic peak durind summer. In 2021–2022, a resurgence of cases was noted, with a distribution of hospitalizations similar to pre-COVID-19 seasons. SARS-CoV-2 was rarely detected, confirming its minor role in acute bronchiolitis epidemics. Impact of the COVID-19 Pandemic on Acute Bronchiolitis Outbreaks: A Retrospective Study Over Five Epidemic Seasons at Clermont-Ferrand University Hospital • Dr. Camille JAILLET ([email protected]), Junior Doctor, Department of General Multidisciplinary Pediatrics, Pediatric Pulmonology and Allergology, Clermont-Ferrand University Hospital • Pr. Cécile HENQUELL ([email protected]), Professor of Medicine, Faculty of Medicine and Allied Health Professions, Department of Virology, Clermont-Ferrand University Hospital • Dr. Valérie JULIAN ([email protected]), Associate Professor, Faculty of Medicine and Allied Health Professions, Department of Sports Medicine and Functional Explorations, Clermont-Ferrand University Hospital • Marie DE ANTONIO ([email protected]), Hospital Engineer, Biostatistician, Clinical Research Department, Clermont-Ferrand University Hospital • Dr. Carole EGRON ([email protected]), Hospital Practitioner, Department of General Multidisciplinary Pediatrics, Pediatric Pulmonology and Allergology, Clermont-Ferrand University Hospital Author contribution statement : • Dr Camille JAILLET : project lead, study conception, data collection and analysis, work coordination, manuscript writing • Pr Cécile HENQUELL : study conception, critical revision, collection of virological data, writing of the virological data collection section • Dr Valérie JULIAN : manuscript proofreading, assistance with manuscript writing • Marie De Antonio : Statistical analyses, writing of the statistical analysis section • Dr Carole EGRON : Study conception, critical revision, project supervision, project lead, final manuscript approval, ethical approval application Conflict of Interest Statement: The authors declare no conflicts of interest related to this study. Funding: This study did not receive any financial support.

Acute bronchiolitis; Infection control measures; COVID-19 pandemic; Respiratory virus; RSV

Background: Acute bronchiolitis outbreaks are seasonal winter phenomena caused by various viruses, primarily respiratory syncytial virus (RSV). These outbreaks lead to high hospitalization rates in infants, placing a significant burden on pediatric services. During the SARS-CoV-2 pandemic, public health measures were implemented to curb viral transmission. Objectives: To assess the impact of the COVID-19 pandemic on the incidence of hospitalized acute bronchiolitis cases at Clermont-Ferrand University Hospital. Methods: A retrospective study was conducted, including infants under 12 months of age hospitalized for acute bronchiolitis at the University Hospital of Clermont-Ferrand between September 1, 2018, and August 31, 2023. The five epidemic seasons were compared. Results : A total of 1420 patients were included. A significant decrease in bronchiolitis hospitalizations was observed in 2020–2021 compared to 2018–2019 (p=0.040), 2021–2022 (p=0.018), and 2022–2023 (p=0.001). The epidemic peak in 2020–2021 was delayed to July and involved fewer cases (36 vs. 110.8 in other years). No significant difference was found in hospital stay duration across the five epidemic seasons (p=0.109). Lockdowns were statistically associated with reduced hospitalization cases (p=0.012). Conclusion : Lockdown measures effectively limited respiratory viruses spread, particularly RSV. A marked decrease in the number of hospitalized acute bronchiolitis was observed during the 2020–2021 season, along with an unusual reduction and delay in the epidemic peak durind summer. In 2021–2022, a resurgence of cases was noted, with a distribution of hospitalizations similar to pre-COVID-19 seasons. SARS-CoV-2 was rarely detected, confirming its minor role in acute bronchiolitis epidemics.

Acute bronchiolitis in infants is defined as a viral bronchiolar obstruction characterized by respiratory distress symptoms such as cough, tachypnea, wheezing, and expiratory rales. Approximately 20% of infants will develop acute bronchiolitis, making it the leading cause of hospitalization in infants under one year of age in developed countries [1, 2, 3] (hospitalization rates ranging from 2 to 4% [1, 2, 4, 5], with a rehospitalization rate of approximately 9% in this age group [4]). The most severe cases occur in infants with underlying comorbidities, including chronic respiratory diseases, congenital heart conditions, or prematurity [4]. Acute bronchiolitis cases occur in seasonal epidemics, with similar annual patterns, including an epidemic onset in the fall and a winter peak [4], primarily caused by respiratory syncytial virus (RSV), although bronchiolitis caused by other annually circulating viruses is also common. These autumn-winter epidemics necessitate a seasonal reorganization of healthcare resources, impacting emergency pediatric services, inpatient units, and intensive care units in terms of human resources and the need for additional bed capacity. The rate of viral detection has significantly increased in recent years (over 90% according to recent series [6]), due to improved diagnostic test sensitivity (particularly through polymerase chain reaction (PCR)) and the development of multiplex tests. RSV is found in 60-80% of cases, either alone or in co-infection [6, 7], and is responsible for the most severe cases, especially in younger infants [8]. Other viruses detected include rhinovirus (RV) (in approximately 20% of cases), parainfluenza virus (PIV), metapneumovirus (MPV), seasonal coronaviruses (CoV), adenovirus (AdV), influenza viruses A and B (IV A-B) and enterovirus (EV) [7]. The viral co-infection rate is estimated to be around 50% [9]. Several seasonal coronaviruses (229E, OC43, NL63, and HKU1) are known to trigger acute bronchiolitis in infants [10]. The SARS-CoV-2 virus (first identified in France in January 2020, with the first positive case in Clermont-Ferrand on March 4, 2020) has also been responsible for acute bronchiolitis, either alone or in co-infection with other viruses [11]. Following the COVID-19 pandemic, barrier measures were implemented to limit virus transmission. In France, the government imposed social distancing, the wearing of facial masks, curfews, lockdowns, and the closing of schools and public venues (Appendix I). These measures reduced the transmission of SARS-CoV-2, as well as other respiratory viruses, particularly RSV [12, 13]. The aim of this study is to assess the impact of the COVID-19 pandemic and associated barrier measures on the incidence, seasonality, severity, and virology of acute bronchiolitis in infants under one year of age hospitalized at Clermont-Ferrand University Hospital between September 1, 2018, and August 31, 2023.

Study Population This is a retrospective, single-center study was approved by the Ethics Committee of the Clermont-Ferrand University Hospital (IRB00013412, ’CHU de Clermont Ferrand IRB #1’), in compliance with French data protection regulations (authorization EI23EC1114). Patients are informed during their hospitalization at the University Hospital of Clermont-Ferrand that their health data may be used for future health studies, unless they object. Subject recruitment was conducted according to the following inclusion criteria: i) children under one year of age at the time of admission; ii) hospitalized in the general pediatrics, continuous monitoring, and intensive care units; iii) admission dates between September 1, 2018 and August 31, 2023; iv) discharge codes corresponding to: Bronchiolitis; Asthma; Pneumonia. After reviewing the medical records, only infants who presented with an episode of acute bronchiolitis with respiratory distress symptoms including cough, tachypnea, wheezing, and expiratory rales were included. Exclusion criteria were: i) subjects who developed another condition during their hospitalization not attributable to the episode of acute bronchiolitis; ii) subjects whose stay was extended or shortened for non-medical reasons; iii) subjects with missing data after transfer to another hospital. Data Collection For each subject, the following information was collected: i) age; ii) sex; iii) admission and discharge dates; iv) length of stay, in calendar days; v) gestational age at birth (with children born strictly before 37 weeks of amenorrhea considered preterm); vi) birth weight; vii) any treatment with PALIVIZUMAB; viii) type of ventilatory support (no respiratory support / low-flow oxygen therapy (O2) / high-flow nasal cannula (HFNC), non-invasive ventilation (NIV) which included bilevel positive airway pressure (BiPAP) and continuous positive airway pressure (CPAP), invasive ventilation (IV)). If a patient experienced multiple episodes of bronchiolitis within 14 days or less, the stays were merged by summing the number of days and retaining the highest level of hospitalization and respiratory support. An epidemic year was defined as spanning from September 1st to August 31st and was divided into four seasonal periods: autumn (September to November), winter (December to February), spring (March to May), and summer (June to August). Respiratory Virology Virological results (virus, test used) were collected from the GLIMS laboratory management system. The virological diagnosis was based on molecular tests (PCR and RT-PCR) targeting one or multiple viruses. Rapid antigen tests were also performed. Figure 1 summarizes the diagnostic strategies used in Clermont-Frrand during the study period. Statistical Analyses Descriptive statistics are presented as counts (n) and percentages (%) for qualitative variables, and as means and standard deviations or medians and interquartile ranges for quantitative variables (depending on their Gaussian distribution). The normality of the distribution was assessed using the Shapiro-Wilk test. The linear relationship between two quantitative variables was examined using Pearson correlation coefficients. To study the association between two qualitative variables, the Chi-square test or Fisher’s exact test was applied (depending on the number of participants). If the association was significant, pairwise dependencies were explored with a correction for multiple comparisons. To compare two groups based on a quantitative variable, Student’s t-test or Wilcoxon test (depending on distribution) was applied. To compare the five periods based on a quantitative variable, either ANOVA or Kruskal-Wallis tests (depending on distribution) were used. A significant result indicates a difference between at least two groups. Post-hoc tests were considered, if applicable, based on clinical relevance, using Tukey’s or Dunn’s tests (depending on distribution). The bronchiolitis cases was numbered weekly, over 260 weeks across the five study periods, divided into four seasons (13 weeks/season/year). Interrupted time series analyses were used to evaluate the impact of the COVID period on the incidence of bronchiolitis. The effect of the period alone was assessed, and then in a multivariate context, the effects of the period, season, and the interaction between period and season, effects of lockdown and mask use, were studied. Time series analysis was performed using segmented negative binomial regression. Negative binomial regression is an extension of Poisson regression that models count data by adding an additional parameter to better estimate variance (overdispersion). All analyses were performed using R software version 4.1.3 (R Foundation for Statistical Computing, Vienna, Austria). Statistical tests were conducted with a two-sided type I error rate of 5%. No corrections were applied except for multiple testing cases.

Study Population and Detected Viruses A total of 1544 cases of hospitalized bronchiolitis were recorded at Clermont-Ferrand University Hospital between September 2018 and August 2023. 84 patients were excluded. Thirty hospital stays were merged in pairs, and five were merged in groups of three ( Figure 2 ). Thus 1420 hospital stays involving 1337 subjects were included. Among them, 75 subjects were hospitalized twice, and 4 were hospitalized three times for separate stays. The majority of hospital stays involved male patients (58.1%). The median age at hospitalization was 2.7 months [1.5 - 5.2]. 86.7% of hospital stays involved term-born infants, while 13.3% involved preterm infants. The median birth weight was 3,200 g [2,830 – 3,550]. 3% of hospital stays concerned subjects who had received RSV immunotherapy with PALIVIZUMAB. The characteristics of the subjects (age, sex, birth weight, gestational age) did not differ significantly between the five study years. Only the proportion of patients who received PALIVIZUMAB was significantly lower in 2022-2023 (1.0%) compared to 2018-2019 (5.1%) (p=0.028). The median length of stay was 4 days [2 - 6]. Regarding the highest level of respiratory support required, 39.8% of patients remained in ambient air, 37.3% required oxygen therapy, and 32.9% required intensive care/critical care respiratory support (of which 94.9% received HFNC, 4.5% received NIV, and 0.6% required IV) ( Table I ). Overall, of the 1420 episodes of bronchiolitis included, 1320 (92.9%) had a respiratory sample, of which 1199 (90.8%) tested positive for at least one virus and 121 (9.2%) returned negative results. The 1199 positive tests found one to three different viruses, identifying a total of 1436 viruses. Among these tests, 979 (81.7%) showed a mono-infection; 203 (16.9%) showed a co-infection with two viruses; and 17 (1.4%) showed a co-infection with three viruses. Among the mono- or co-infections, RSV was identified in 897 cases (74.8%). The other viruses found were rarer, with the following frequencies in descending order: RV, MPV, PIV, SARS-CoV-2, AdV, CoV, and IV A-B ( Table II ). SARS-CoV-2 was detected in 35 cases, representing 2.9% of all positive virological results over the entire study period (n=1199), and 4.4% of positive cases from March 2020 (date of the first COVID-19 case diagnosed in Clermont-Ferrnad) onward (n=788). Incidence and Peak Hospitalizations for Acute Bronchiolitis. The average annual hospitalization incidence over the study period was 284. The minimum hospitalization incidence occurred in 2020-2021 (the first year of the COVID-19 pandemic), with 173 hospitalizations, while the maximum number of hospitalizations occurred in 2022-2023, with 398 hospitalizations. Hospitalization peaks were observed during winter in both the pre-COVID-19 years (2018-2019 and 2019-2020) and the post-lockdown years (2021-2022 and 2022-2023), with the highest number of hospitalizations in January for 2018-2019 and in December for the years 2019-2020, 2021-2022, and 2022-2023. In 2020-2021, the peak was shifted to July. The average peak of hospitalizations over the study period was 95.8 per month. The highest peak occurred in 2021-2022, with 130 hospitalizations in December, while the lowest peak occurred in 2020-2021, with 36 hospitalizations in July ( Figure 3 ). Interannual Comparison INCIDENCE: Using 2020-2021 as the reference year (COVID-19 year), the incidence of hospitalizations was significantly lower compared to the other years (p<0.001), with an average incidence reduction of 35% compared to the of the pre-COVID-19 years (2018-2020) and 52% compared to the post-lockdown years (2021-2023). Regarding its seasonal distribution, the incidence was significantly higher in the summer (p<0.001) and spring (p<0.001) compared to the four other years studied. It was lower in winter compared to the four other years (p<0.001) and in autumn compared to the two post-lockdown years (2021-2022 and 2022-2023) (p<0.001). Using 2018-2019 as the reference year (the year before the emergence of SARS-CoV-2 in France), the incidence only differed in 2020-2021 (p=0.040). Regarding the seasonality of the epidemics, the hospitalization incidence was lower in 2018-2019 summer compared to the 2019-2020 summer (p=0.046), but similar to the other years. The incidence in autumn 2018-2019 was significantly lower than in 2021-2022 (p=0.003) and 2022-2023 (p<0.001), with an earlier onset of the epidemic in the post-lockdown years ( Figure 3 ). Finally, when considering the overall comparison between the incidence of hospitalizations in the pre-COVID-19 years (2018-2020) and the post-lockdown years (2021-2023), there was an average increase of 35.3% in hospitalized cases, but this result was not statistically significant (p=0.093). The overall incidence of bronchiolitis hospitalizations, along with the viruses responsible, the lockdown periods, and the diagnosed COVID-19 cases in the Puy-de-Dôme are presented in Figure 4 . SEVERITY: The maximal respiratory support used varied between 2018-2019 and the other four years (p<0.001). The rate of hospitalization without respiratory support did not differ between the 5 years studied (p=0.363). However, the rate of stays requiring oxygen was higher in 2018-2019 compared to the four other years (p<0.001). Conversely, the rate of patients requiring respiratory support via HFNC, NIV or IV was lower in 2018-2019 compared to the other years (p<0.001). The median length of stay was 4 days (4 days for the years 2018-2019 and 2019-2020, and 3 days for the years 2020-2021, 2021-2022, and 2022-2023), and did not differ across the 5 years (p=0.109) ( Table I ). VIRUS DETECTION: RSV was tested in 1283 of the 1420 hospitalizations included (100 cases without viral testing and 37 cases with viral testing excluding RSV). The rate of patients tested for RSV was lower in 2018-2019 compared to 2020-2021 (p=0.021) and 2021-2022 (p<0.001) ( Table I ). Among the hospitalizations for which RSV was tested, the positivity rate was lower in the post-lockdown years (2021-2023) compared to the pre-COVID-19 years (2018-2020). Specifically, in 2021-2022, the RSV positivity rate was 13% lower than in 2018-2019 (p=0.003) and 17% lower than in 2019-2020 (p=0.001). In 2022-2023, it was 14% lower than in 2018-2019 (p<0.001) and 18% lower than in 2019-2020 (p<0.001) ( Table I ). Attributable Impact of the COVID-19 Pandemic and Barrier Measures The two statistical models, using 2018-2019 (pre-COVID-19) or 2020-2021 (COVID-19) as reference years, highlight that lockdowns are associated with a reduction in the incidence of hospitalizations for acute bronchiolitis (p=0.012). However, strict mask-wearing (from July 20, 2020, to July 21, 2021) does not appear to be associated with a decrease in bronchiolitis hospitalizations (p=0.264). No significant association was found between the incidence of hospitalizations for acute bronchiolitis and the number of COVID-19 cases in the Puy-de-Dôme department (p=0.56).

The objective of this study was to evaluate the impact of the COVID-19 pandemic on the incidence, severity, and virology of hospitalized acute bronchiolitis cases. To our knowledge, this is the first French study documenting five complete years before, during, and after lockdowns, with nearly exhaustive viral documentation for all years (>80%), in infants under one year hospitalized for acute bronchiolitis. Our results suggest that the lockdowns during the COVID-19 pandemic were the only impactful measure on the incidence and seasonality of hospitalized acute bronchiolitis. First, we observed a 35% decrease in hospitalizations in 2020–2021 (the first year of the pandemic) compared to 2018–2020, as well as the absence of an RSV epidemic during the winter following the second lockdown in autumn 2020. This phenomenon has also been described in other studies, with similar proportions in hospitalization incidence reductions (ranging from 35% to 70% depending on the series and countries compared to pre-COVID-19 years). A decrease in general practice consultations and emergency room visits for acute bronchiolitis has also been reported in other works [3, 14, 15, 16, 17]. Following the 2020–2021 year, a 35% rebound in hospitalizations was observed in the years 2021–2023. This phenomenon was also observed by the OSCOUR network and Santé Publique France ’s monitoring, confirming that post-lockdown acute bronchiolitis epidemics were more intense compared to pre-COVID-19 seasons. Additionally, an increase in consultations in general practice, emergency consultations, and hospitalizations has been reported compared to pre-COVID-19 (ranging from 30% to 50% depending on the series and countries) [14, 15, 18]. The autumn 2020 lockdown also disrupted the epidemic calendar, preventing the classic winter RSV peak. Subsequently, an increase in hospitalized cases was observed in March 2021, interrupted by the third lockdown in spring 2021, with a resurgence upon its lifting, leading to a smaller peak in July, which was unprecedented. These results are in agreement with other studies, particularly those from North America [19]. However, some regional or national studies in France describe an epidemic peak in February–March 2021. These results may be related to the absence of patient inclusion in summer [16] or to shifts and variations in viral epidemics between Clermont-Ferrand and other French cities or regions [3]. The pre- and post-pandemic profiles, where hospitalization peaks were concentrated in winter (December–January), are consistent with other national [3, 15] and international sources [20]. The seasonal shift may be related to fluctuations in the circulation of respiratory viruses overall, which were affected by pandemic control measures [21], with RSV remaining the predominantly identified virus [22]. The marked reduction in bronchiolitis cases in 2020–2021 (as with many other infectious diseases) may suggest a potential immunological debt and the possibility of more severe cases in infants after the lifting of barrier measures [23]. Clinically, our data show that the severity of bronchiolitis, as measured by hospital length of stay and the need for respiratory support, remains comparable between the different years studied. Literature data on this point diverge, with median lengths of stay comparable to ours in several studies [1, 2, 4, 5], while others report longer hospitalization durations, increased use of intensive care services, or more frequent oxygen therapy use in the post-lockdown period [16, 19]. Our results show an increase in the use of HFNC, NIV, or IV starting in 2019. This appears to be attributable to a change in our practices, notably the wider use of HFNC, even in conventional wards starting in 2019. These practice changes explain the increased use of HFNC, NIV, and IV from the 2019–2020 year, alongside fewer patients receiving simple oxygen without an extended length of stay. The disruptions caused by the pandemic and the implemented barrier measures had an impact on the seasonality of circulation and the virulence of viruses responsible for acute bronchiolitis. One strength of this study is the high testing rate among hospitalized infants, including before COVID-19, particularly for RSV. Our study shows a very high positivity rate for tests conducted (90.8%), which is comparable to other sources [6]. RSV remained predominant in hospitalized acute bronchiolitis cases (74.8% of positive virological tests, 68% of all tested patients), which is consistent with previously published figures [6, 7, 19]. A wide range of different viruses was identified. We chose to analyze only the data related to RSV, as it was tested for in 97% of patients (only 37 out of 1320 cases had a viral test without RSV testing). Although RSV remains predominant, its percentage among all identified viruses was lower during the 2021–2023 epidemic seasons compared to 2018–2020. Our study, focusing on the most severe cases (those requiring hospitalization), supports the hypothesis of a potential increase in the severity of non-RSV bronchiolitis compared to the pre-pandemic era, aligning with concerns raised by the GPIP. To confirm this hypothesis, subgroup analyses would have been useful but were not possible due to the low rate of multiplex testing pre-pandemic. It should be noted that SARS-CoV-2 is very rarely responsible for acute bronchiolitis (4.4%), and mainly in co-infections, which is also found in other studies [16]. Our models do not find a correlation between the incidences of bronchiolitis hospitalizations and COVID-19 cases. These results highlight that SARS-CoV-2 did not replace other respiratory viruses but temporarily altered their transmission dynamics through lockdown measures [24]. The results of our regression models suggest that, unlike lockdowns, mask-wearing did not impact hospitalization rates, suggesting that only the strictest measures were effective. More broadly, the incidence of all infectious diseases transmitted by airborne or fecal-oral routes significantly decreased following the implementation of all barrier measures [21, 25]. The relaxed barrier measures, including mask-wearing, though mandatory, had little impact, with an epidemic resurgence once the lockdowns were lifted [20]. This study has several biases inherent to its monocentric retrospective protocol. First, this monocentric study only deals with infants hospitalized in a university hospital, which does not reflect the diversity of patients treated in outpatient care or other hospitals. Second, the variability in diagnostic and management practices over the five years of the study must be taken into account. Finally, the primary limitation of our study is the evolution of tests performed for upper respiratory viral infections during the study period, depending on the season and pre- or post-COVID-19 period. However, the consistency of testing in hospitalized infants (particularly for RSV) is a strength of this work, making our results on RSV reliable. We chose to focus on infants under one year old as they represent the majority of hospitalized patients and severe cases [14, 26]. The results of this study could lead us to consider the targeted reinforcement of strict barrier measures. The absence of group settings and avoidance of public places with close contact could be recommended for vulnerable infants to prevent acute bronchiolitis and other viral diseases at risk. Simple barrier measures remain insufficient to prevent acute bronchiolitis epidemics, and new promising measures are now available. Nirsevimab (monoclonal antibody targeting RSV), available in France since September 2023 for all infants at parental request during their first at-risk season. In parallel, vaccines against RSV (notably ABRYSVO) have been offered to pregnant women between 32 and 36 weeks of amenorrhea from September 2024 to January 2025. These new immune therapies already seem promising, and further studies are underway to assess their impacts at Clermont-Ferrand University Hospital.

Although initially intended to contain SARS-CoV-2, the implemented barrier measures effectively limited the spread of other respiratory viruses, particularly RSV, the primary cause of acute bronchiolitis. A marked reduction in the number of hospitalized acute bronchiolitis cases was observed at Clermont-Ferrand University Hospital during the 2020–2021 period, along with a decrease and unusual shift in the epidemic peak to the summer. Starting with the 2021–2022 epidemic season, a resurgence in cases was noted, with the distribution and intensity of hospitalizations resembling that of pre-COVID-19 epidemic seasons, including a winter hospitalization peak. In contrast, SARS-CoV-2 was rarely detected in virological samples related to bronchiolitis, confirming its minor role in the acute bronchiolitis outbreak. 11. A. Waghmare et al. SARS-CoV-2 Infection and COVID-19 in Children. Clin Chest Med. 2023 Jun;44(2):359-371. doi: 10.1016/j.ccm.2022.11.014. Epub 2022 Nov 2 12. D. Van Brusselen et al. Bronchiolitis in COVID-19 times: a nearly absent disease? Eur J Pediatr. 2021 Jun;180(6):1969-1973. doi: 10.1007/s00431-021-03968-6. Epub 2021 Jan 30. PMID: 33517482; PMCID: PMC7847293. 13. C. Delestrain et al. Impact of COVID-19 social distancing on viral infection in France: A delayed outbreak of RSV. Pediatr Pulmonol. 2021 Dec;56(12):3669-3673. doi: 10.1002/ppul.25644. Epub 2021 Sep 2. PMID: 34473914; PMCID: PMC8662089. 14. KA. Remien et al. Admissions for Bronchiolitis at Children’s Hospitals Before and During the COVID-19 Pandemic. JAMA Netw Open. 2023 Oct 2;6(10):e2339884. doi: 10.1001/jamanetworkopen.2023.39884. PMID: 37883085; PMCID: PMC10603547. 15. S. Vaux et al. Bronchiolitis epidemics in France during the SARS-CoV-2 pandemic: The 2020-2021 and 2021-2022 seasons. Infect Dis Now. 2022 Sep;52(6):374-378. doi: 10.1016/j.idnow.2022.06.003. Epub 2022 Jun 23. PMID: 35753628; PMCID: PMC9222408. 16. V. Boccard et al. Bronchiolitis: Increased severity in the post-COVID-19 era. Pediatr Pulmonol. 2024 Jul 11. doi: 10.1002/ppul.27172. Epu…b ahead of print. PMID: 38990099. 17. L. Berdah L et al. Retrospective observational study of the influence of the COVID-19 outbreak on infants’ hospitalisation for acute bronchiolitis. BMJ Open. 2022 Oct 31;12(10):e059626. doi: 10.1136/bmjopen-2021-059626. PMID: 36316083; PMCID: PMC9627576. 18. Santé publique France. Bronchiolite : bilan de la surveillance hivernale 2022-2023. 19. C. Guitart et al. Hospital Network for R. S. V. surveillance in Catalonia. Bronchiolitis, epidemiological changes during the SARS-CoV-2 pandemic. BMC Infect Dis. 2022 Jan 24;22(1):84. doi: 10.1186/s12879-022-07041-x. PMID: 35073855; PMCID: PMC8785150. 20. L. Lenglart et al. Respective roles of non-pharmaceutical interventions in bronchiolitis outbreaks: an interrupted time-series analysis based on a multinational surveillance system Eur Respir J. 2023 Feb 16;61(2):2201172. doi: 10.1183/13993003.01172-2022. PMID: 36356971. 21. F. Angoulvant et al. Coronavirus Disease 2019 Pandemic: Impact Caused by School Closure and National Lockdown on Pediatric Visits and Admissions for Viral and Nonviral Infections. Clin Infect Dis. 2021 Jan 27;72(2):319-322. doi: 10.1093/cid/ciaa710. PMID: 33501967; PMCID: PMC7314162. 22. JS. Casalegno, et al. Characteristics of the delayed respiratory syncytial virus epidemic, 2020/2021, Rhône Loire, France. Euro Surveill. 2021 Jul;26(29):2100630. doi: 10.2807/1560-7917.ES.2021.26.29.2100630. PMID: 34296674; PMCID: PMC8299747. 23. R. Cohen et al. Pediatric Infectious Disease Group (GPIP) position paper on the immune debt of the COVID-19 pandemic in childhood, how can we fill the immunity gap? Infect Dis Now. 2021 Aug;51(5):418-423. doi: 10.1016/j.idnow.2021.05.004. Epub 2021 May 12. PMID: 33991720; PMCID: PMC8114587. 24. G. Cozzi et al. SARS-CoV-2-related bronchiolitis: a multicentre international study. Arch Dis Child. 2023 Sep;108(9):e15. doi: 10.1136/archdischild-2023-325448. Epub 2023 May 2. PMID: 37130726. 25. T. Launay et al. Common communicable diseases in the general population in France during the COVID-19 pandemic. PLoS One. 2021 Oct 11;16(10):e0258391. doi: 10.1371/journal.pone.0258391. PMID: 34634090; PMCID: PMC8504745. 26. M. Korpp et al. Upper age limit for bronchiolitis: 12 months or 6 months? Eur Respir J. 2012 Mar;39(3):787-8; author reply 788-9. doi: 10.1183/09031936.00170511. PMID: 22379159.

1. 1. R. Assathiany et al. Effects of infant bronchiolitis on family life. Front Pediatr. 2024 Jun 19;12:1343045. 38962572; PMCID: PMC11220111. 2. K. Hasegawa et al. Trends in bronchiolitis hospitalizations in the United States, 2000-2009. Pediatrics. 2013 Jul;132(1):28-36. Epub 2013 Jun 3. 23733801; PMCID: PMC3691534. 3. Santé publique France. Bronchiolite : bilan de la surveillance hivernale 2020-2021. 4 . D.Che et al. Bronchiolite aigüe du nourrisson en France bilan des hospitalisés en 2009 et facteurs de létalité. Archives de Pédiatrie, 2012, vol. 19, n°. 7, p. 700-6 5. I. Mitchell et al. Burden of Respiratory Syncytial Virus Hospitalizations in Canada. Can Respir J. 2017;2017:4521302. Epub 2017 Nov 7. 29311757; PMCID: PMC5697123. 6 . C. Marguet et al. In very young infants severity of acute bronchiolitis depends on carried viruses. PLoS One. 2009;4(2):e4596. doi: 10.1371/journal.pone.0004596. Epub 2009 Feb 25. PMID: 19240806; PMCID: PMC2644758. 7 . HC. Meissner Viral Bronchiolitis in Children. N Engl J Med. 2016 Jan 7;374(1):62-72. doi: 10.1056/NEJMra1413456. PMID: 26735994. 8. CB.Hall et al. Respiratory syncytial virus-associated hospitalizations among children less than 24 months of age. Pediatrics. 2013 Aug;132(2):e341-8. Epub 2013 Jul 22. 23878043. 9. H.PETAT et al. High Frequency of Viral Co-Detections in Acute Bronchiolitis. Viruses. 2021 May 26;13(6):990. 34073414; PMCID: PMC8229544. 10. FZ. Alaoui-Inboui et al. Viral Bronchiolo-Alveolitis From Coronavirus OC43 and Rhinovirus-Simulating SARS-CoV-2 Infection. Cureus. 2022 Aug 17;14(8):e28093. doi: 10.7759/cureus.28093. PMID: 36127976; PMCID: PMC9478778. Information & Authors Information Version history Copyright This work is licensed under a Non Exclusive No Reuse License.

Authors Metrics & Citations Metrics Article Usage 170views 114downloads Citations Download citation Camille JAILLET, Cecile Henquell, Valérie JULIAN, et al. Impact of the COVID-19 Pandemic on Acute Bronchiolitis Outbreaks: A Retrospective Study Over Five Epidemic Seasons at Clermont-Ferrand University Hospital. Authorea. 13 May 2025. DOI: https://doi.org/10.22541/au.174714843.35642756/v1 DOI: https://doi.org/10.22541/au.174714843.35642756/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu.