key: cord-0852472-a2c5q6a9 authors: Be'er, Moria; Amirav, Israel; Cahal, Michal; Rochman, Mika; Lior, Yotam; Rimon, Ayelet; Lavy, Roni G.; Lavie, Moran title: Unforeseen changes in seasonality of pediatric respiratory illnesses during the first COVID‐19 pandemic year date: 2022-03-31 journal: Pediatr Pulmonol DOI: 10.1002/ppul.25896 sha: 63d9204a332f11cdeaffc85f85a536bf5f09b0fd doc_id: 852472 cord_uid: a2c5q6a9 OBJECTIVES: To investigate whether the three nationwide coronavirus disease 2019 (COVID‐19) lockdowns imposed in Israel during the full first pandemic year altered the traditional seasonality of pediatric respiratory healthcare utilization. METHODS: Month by month pediatric emergency department (ED) visits and hospitalizations for respiratory diagnoses during the first full COVID‐19 year were compared to those recorded for the six consecutive years preceding the pandemic. Data were collected from the patients' electronic files by utilizing a data extraction platform (MDClone(©)). RESULTS: A significant decline of 40% in respiratory ED visits and 54%–73% in respiratory hospitalizations during the first COVID‐19 year compared with the pre‐COVID‐19 years were observed (p < 0.001 and p < 0.001, respectively). The rate of respiratory ED visits out of the total monthly visits, mostly for asthma, peaked during June 2020, compared with proceeding years (109 [5.9%] versus 88 [3.9%] visits; p < 0.001). This peak occurred 2 weeks after the lifting of the first lockdown, resembling the “back‐to‐school asthma” phenomenon of September. CONCLUSIONS: This study demonstrates important changes in the seasonality of pediatric respiratory illnesses during the first COVID‐19 year, including a new “back‐from‐lockdown” asthma peak. These dramatic changes along with the recent resurgence of respiratory diseases may indicate the beginnings of altered seasonality in pediatric pulmonary pathologies as collateral damage of the pandemic. 2 | METHODS This study was conducted at Dana-Dwek Children's Hospital, Tel-Aviv Medical Center between March 1, 2020, and February 28, 2021 (the first COVID- 19 year in Israel). The study population included children aged 0-18 years who visited our hospital with respiratory complaints and/or diagnoses during the first COVID- 19 year. The control group was comprised of children with the same characteristics who visited the hospital throughout the 6 years before the pandemic (from 2014 to 2020). This study was approved by the local ethics committee (approval number TLV-0609-20), and informed consent was waived since it was retrospective and anonymous. Medical and demographic data were collected from the patients' electronic files by means of MDClone © , a data extraction synthetization platform that provides patient-level data around a reference event. 19 For the purposes of this study, the reference event was a pediatric ED visit or hospitalization due to respiratory complaints or diagnosis that included asthma exacerbation, wheezing, dyspnea, cough, bronchiolitis, or pneumonia according to International Statistical Classification of Diseases and Related Health Problems (ICD) classification systems. Data on demographics (e.g., age and sex) and nasal viral swab test were also retrieved. The major outcomes of this study were the incidence of ED visits and hospitalizations in hospital wards (e.g., pediatric ward, intensive care unit, etc.) due to respiratory complaints and the timeline of these events. These values were calculated yearly and monthly by dividing the average number of respiratory ED visits and hospitalizations by the average number of total ED visits and hospitalizations during the study (pandemic) period and the control (pre-pandemic) period. The incidence and yearly seasonality of these events during the first COVID-19 year were compared with those of the pre-COVID-19 years. We also performed a subgroup analysis by diagnosis, focusing upon the three major respiratory diagnoses of asthma and/or wheezing, pneumonia, and bronchiolitis. The Israeli school year routinely starts on September 1 after 2 months of summer vacation. There were three lockdown periods during the COVID-19 year study period, during which all of the educational institutions were closed: the first lockdown took place from March 15 to May 17, 2020 (9 weeks), the second from September 17 to October 18, 2020 (4.5 weeks), and the third from January 8 to February 11, 2021 (5 weeks). The preferred method of analysis for continuous variables, such as age in pre-COVID-19 and COVID-19, was parametric using Student's t test. The non-parametric Mann-Whitney was applied if parametric assumptions could not be satisfied, such as in the case of hospitalization length of stay among pre-COVID-19 and COVID-19 patients, even after attempts at data transformation. Parametric model assumptions were assessed with the normal probability plot or the Shapiro-Wilks statistic for verification of normality and with Levene's test for verification of homogeneity of variances. Categorical variables were tested with Pearson's χ 2 test for contingency tables or Fisher's Exact test, as appropriate. Variable in which this type of analysis was applied to compare pre-COVID-19 and COVID-19 rates include gender, monthly incidence of pneumonia, bronchiolitis, wheezing or asthma, total respiratory cases (both in ED and wards), and positive nasal swabs rates, as well as total ED visits and hospitalizations. All statistical tests and/or confidence intervals were performed at α = 0.05 (two-sided). All p values were rounded to three decimal places. The data were analyzed with IBM SPSS Statistics software. There was a total of 20,527 pediatric ED visits, 2545 pediatric ward hospitalizations, and 401 ICU hospitalizations during the first COVID-19 year compared with an annual mean of 28,435 ED visits, 3142 pediatric ward hospitalizations, and 356 ICU hospitalizations in the pre-COVID-19 years (p < 0.001, p < 0.001 and p = 0.36, respectively). There was a 28% reduction in total ED annual visits and a 19% reduction in total annual hospitalizations during the first COVID-19 year compared to pre-COVID-19 years (p < 0.001 and p < 0.001, respectively). An even greater decrease was observed in respiratoryrelated presentations, with a 40% reduction in respiratory ED visits and a 54% reduction in respiratory hospitalizations compared with the pre-COVID-19 years (p < 0.001 and p < 0.001, respectively). A 73% decrease in respiratory ICU hospitalizations was also observed (p < 0.001). The characteristics of the study participants are presented in Table 1 Interestingly, bronchiolitis seemed to follow normal seasonality trends e.g. no differences in spring and summer, while both asthma and pneumonia did not follow, or did but to a lesser degree. This supports the notion of multiple triggers for asthma/pneumonia (allergies, stress, more exercise in warmer months, and bacterial pathogens) versus the single trigger of bronchiolitis, being viral, which was lessened by the lockdowns. Moreover, there was a significant increase in the age of patients with respiratory ED visits and hospitalizations in the COVID-19 year from pre-COVID-19 years. This could be explained by several factors, including the younger age children who are more prone to viral respiratory illnesses compared to the older children whose respiratory illnesses are more influenced by variable triggers. Another possible explanation might be parental anxiety regarding sending infants to daycares even after a lockdown was lifted. 27 F I G U R E 2 Incidence of specific respiratory diagnoses by month The number of respiratory ED visits (A) and respiratory hospitalizations (B) by month throughout the COVID-19 year (black) compared to pre-COVID-19 mean annual visits and hospitalizations (red). The incidence was calculated by dividing the respiratory ED respiratory visits or respiratory hospitalizations by the total visits or hospitalizations during that month. COVID-19, coronavirus disease 2019; ED, emergency department, ns, nonsignificant. 2020. This peak took place two weeks after the end of the first lockdown, which was the most stringent and longest of all lockdowns in Israel. That peak was most prominent for asthma, and it resembled the phenomenon of BTS asthma with its well-known peak incidence in September after the beginning of the school year. 13, 30 The BTS asthma phenomenon is generally explained by universal seasonality or the return to school per se. 13, 15, 17 Our finding, which we termed back-from-lockdown (BFL) asthma, resembles BTS in many aspects. First, children returning to school after 2 months of social distancing, are re-exposed to viral respiratory infections. 13, 16, 17 Rhinovirus infections, which are the strongest trigger for asthma exacerbations, especially as part of BTS asthma, are known to be most common in early autumn after the summer vacation. 13, 16, 17, 31 Since the examined peak of BFL asthma was in June, the seasonality of the virus would not be expected to have been a contributing factor. 31 Nevertheless, some data suggest that a new pattern of viral seasonality was created due to the newly introduced SARS-CoV-2, 32 as seen, for example, from our data on RSV. Other factors that may explain both BFL and BTS asthma include high stress associated with school return, which can worsen asthmatic symptoms in children, 33, 34 and re-exposure to high levels of sensitizing allergens in the school environment. 13, 17 All of the above factors may also play a role in the BFL asthma phenomenon observed in June 2020. Moreover, it can be argued that these factors are even more prevalent during a lockdown in comparison to a regular school break because of the extreme measures taken (e.g., masks, social distancing, travel restrictions, and pandemic-related stress). However, allergic exposures likely play a much smaller role in respiratory diseases than we had previously imagined. During the lockdown, children were more likely to be exposed to pets, environmental tobacco smoke, and potentially the outside environment rather than sitting in a classroom all day. This may explain, in part, why aggressive allergen mitigation efforts appear to have a negligible impact on asthma exacerbations. 35 The new BFL asthma and the changes observed in time patterns of respiratory illnesses during the first COVID-19 year raise the question of whether the term "seasonality" is adequate when discussing respiratory morbidity, especially with viral etiology. Rather than discussing seasonality, it is time to accept that when viruses are readily transmitted among children it is then we will see an increase in respiratory illnesses, and this is most probably unrelated to a season. Some limitations to our study bear mention. First, the data were from a single center in Israel, therefore it is not clear whether these results would be generalizable to like institutions in other countries. Second, only hospital data and not primary care or telemedicine services were included. Regarding remote medicine, our medical center utilized remote medicine services only for ambulatory care and not as urgent care. Therefore, remote medicine probably did not affect the rate of ED visits or hospitalizations. Moreover, telemedicine services were more accessible at the community clinics, and were likely more accessible in the second and third lockdown periods. Therefore, one may have expected an even larger drop in ED visits in place of online visits, which did not seem to occur, thus making the telemedicine role less likely as the principal reason for decreased ED visits. In conclusion, this study demonstrates important changes in the seasonality of pediatric respiratory illnesses during the first COVID-19 year, including a new "back-from-lockdown" asthma peak. These dramatic changes along with the recent resurgence of respiratory diseases suggest that the last word has not yet been said and may imply a global change in pediatric respiratory medicine as we know it. WHO Timeline -COVID-19. Accessed date World Health Organization. Coronavirus disease (COVID-19) pandemic. Accessed date Updated Guidelines, State of Israel, Ministry of Health. 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Trends in US pediatric hospital admissions in 2020 compared with the decade before the COVID-19 pandemic School holidays and admissions with asthma Asthma exacerbations 1: epidemiology How COVID-19 is changing the cold and flu season The role of acute and chronic stress in asthma attacks in children Asthma exacerbations in children immediately following stressful life events: a Cox's hierarchical regression Allergen avoidance in allergic asthma The authors would like to acknowledge the I-Medata AI Center of the Tel Aviv Sourasky Medical Center for their technical support and to thank Mr. Iddo Jacobi for his help. The authors declare no conflicts of interest. The data that support the findings of this study are available from the corresponding author upon reasonable request.