COVID‐19 increased in Italian children in the autumn and winter 2021–2022 period when Omicron was the dominant variant

Abstract

Aim

We examined the prevalence of the severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) in children during the autumn and winter season from 1 September 2021 to 30 January 2022 and compared it with the same period in 2020–2021.

Methods

This study was carried out int the paediatric emergency department (PED) of a tertiary Italian hospital. We compared the clinical and demographical features of all children who presented during the two study periods and tested positive for SARS‐CoV‐2.

Results

During the 2021–2022 autumn and winter season 5813 children presented to the PED, 19.0% were tested for SARS‐CoV‐2 and 133 (12.0%) of those tested positive. In 2020–2021, 2914 presented to the PED, 12.3% were tested, and 30 (8.3%) of those tested positive. There were no statistically significant differences in clinical severity during the two study periods, despite a higher percentage of neurological symptoms in 2020–2021. Of the SARS‐CoV‐2‐positive cases, 29/133 (21.8%) were hospitalised during the 2021–2022 season and 10/30 (33.3%) during the previous one. Only 3/163 children required intensive care.

Conclusion

The greater spread of SARS‐CoV‐2 was probably due to the greater transmissibility of the Omicron variant, but the symptoms were mild and only 3 children required intensive care.

Abbreviations

PED

paediatric emergency department

PICU

paediatric intensive care unit

SARS‐CoV‐2

severe acute respiratory syndrome coronavirus 2

Key Notes.

• We compared the prevalence of the pandemic virus in children who presented to an Italian paediatric emergency department presentations during the 2021–2022 and 2020–2021 autumn and winter seasons.

• Presentations almost doubled from 2914 to 5813 and virus positive cases rose from 30 to 133 of those tested.

• The increased number of positive cases could have been due to the higher transmissibility of the Omicron variant, but the symptoms remained mild.

1. INTRODUCTION

In December 2019, China reported the first signs of the severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2), ¹ which causes COVID‐19, and a global pandemic was declared in March 2020. Children were less affected than adults at the start of the pandemic and Italy reported that only 1.6% of children had COVID‐19 in March 2022. ²

The role that children played in COVID‐19 was controversial, as preliminary studies seemed to show that they were involved in viral transmission and amplification. ³ , ⁴ However, other authors later suggested that children were unlikely to be the main drivers of the pandemic during the first 2020 wave. ⁵ It was suggested that several factors contributed to the small number of cases in paediatric populations, including the theory that younger people had reduced susceptibility to the SARS‐CoV‐2 virus than adults. ⁶ , ⁷ , ⁸ In addition the conservative measures adopted by the Italian Government in 2020, such as schools closure, lockdowns, face masks and social distancing, were not always successful in controlling the spread of the virus among children. ⁹ , ¹⁰ , ¹¹

A meta‐analysis of the role of children in the spread of SARS‐CoV‐2 reported that they were mainly infected by their parents and this could have reduced the pathogenicity of a second or third generation of the virus. ⁸ In late November 2021, the new SARS‐CoV‐2 Omicron variant spread to Italy and its high transmissibility, ¹² which coincided with the reopening of schools, resulted in thousands of infected children being admitted to hospitals. The first Omicron case in Italy was detected on 28 November 2021, and it related to a man who had arrived from Mozambique on 11 November. The Omicron variant was capable of penetrating the immune system of previously infected individuals and of evading antibodies produced against existing vaccines. ¹³ , ¹⁴

Vaccination against SARS‐CoV‐2 was approved in Italy for adolescents from 12 to 18 years of age in June 2021 and for those aged 5–11 years in December 2021. By 11 January 2022, 75.48% of the older children had completed their vaccination cycle, but only 2.43% of the young children had. ¹⁵ In addition, data from the National Institute of Health showed that 826 774 new cases of COVID‐19 had been diagnosed in Italian children and adolescents aged 0–19 by 10 November 2021. ² By 15 January 2022, this had risen to 2 009 862 cases: 12365 had been hospitalised, 300 needed intensive care, and 39 had died. ² One explanation for this was that the Omicron variant mostly bypassed vaccine‐induced immunity. ¹⁰ We hypothesised that the increased prevalence of SARS‐CoV‐2 infections in the paediatric population during the study period of 1 September 2021 to 30 January 2022 could have been partly due to the spread of the new Omicron variant, which was first confirmed in Italy in late November. Our aim was to compare the prevalence of the SARS‐CoV‐2 infections in patients who presented to the paediatric emergency department (PED) with COVID‐19 or flu‐like symptoms during the 2021–2022 study period and the same period in 2020–2021.

2. METHODS

We conducted a retrospective, cross‐sectional, study in the tertiary Fondazione Policlinico Universitario A. Gemelli, IRCSS university hospital in Rome. The PED receives some 15 000 visits per year. We included all children between 0 and 18 years of age who were admitted to the PED during the autumn and winter seasons from 1 September 2021 to 30 January 2022, and the corresponding season in 2020–2021 and had nasopharyngeal swab tests for SARS‐CoV‐2. According to our hospital's internal protocol during the two study periods, each child admitted to the PED with fever, respiratory, gastrointestinal or other symptoms compatible with COVID‐19 underwent this test. We excluded patients who fell outside the age and study date criteria and those whose diagnosis of SARS‐CoV‐2 was not confirmed by real‐time reverse‐transcriptase polymerase‐chain reaction. The data were collected by retrieving the electronic medical records from the PED system. They included information on age, gender, contact with SARS‐CoV‐2‐positive case, SARS‐CoV‐2 vaccination status and the triage colour code. We also included prematurity and comorbidities, such as bronchopulmonary dysplasia, asthma, cardiopathy, immunological deficit and genetic syndromes, clinical features, diagnostic examinations, type of treatments, rate of hospitalisation and ward admittances. The triage colour codes were assigned to patients when they presented to the PED by the triage nurse, based on the child's general conditions, symptoms and vital signs. The hospital triage system in our region is based on 5 numerical codes: 1 is an emergency, 2 is urgent, 3 is moderate urgency, 4 is minor urgency, and 5 is not urgent. Codes 1, 2 and 3 require high to medium intensity of care, while 4–5 require moderate to low intensity. The clinical features included fever, respiratory symptoms, such as cough, rhinitis and dyspnoea and gastrointestinal symptoms, such as vomiting, diarrhoea and abdominal pain. They also included flu‐like symptoms, such as headache, asthenia, muscular pains and pharyngitis and neurological symptoms, such as anosmia, ageusia and convulsions. Children admitted to the PED with symptoms that suggested COVID‐19, according to Parri et al's classification of disease severity, ¹⁶ were divided in two groups. The first group included asymptomatic children and those with mild and moderate symptoms and the second one comprised patients with severe and critical conditions. ¹⁶ We compared all the clinical and demographical features of children admitted to PED during the 2021–2022 with COVID‐19 with the same period in 2020–2021. The study protocol was approved by the Institutional Review Board and Medical Ethics Committee of the Fondazione Policlinico Universitario A. Gemelli, IRCSS. Parental consent was not required because of the retrospective nature of the study.

2.1. Statistical analysis

Categorical variables are reported as numbers and percentages. The normality of distribution of the continuous variables was tested using the Shapiro–Wilk test. Continuous variables are expressed as means and standard deviations (SD) or as medians and inter‐quartile ranges (IQR), if not normally distributed. Statistical comparisons between groups were performed by the chi‐square test or Fisher's exact test, as appropriate, for categorical variables. Differences in normally distributed continuous variables were tested by the two‐tailed unpaired Student's t‐test and the Mann–Whitney U‐test was used for continuous variables that were not normally distributed. The prevalence rate was obtained by dividing the number of children who tested positive for SARS‐CoV‐2 during the study period by the number who underwent nasopharyngeal swab tests. A two‐sided p‐value <0.05 was considered statistically significant. All data analyses were performed using SPSS version 25.0 (IBM Corp, New York, USA).

3. RESULTS

During the 2021–2022 and 2020–2021 autumn and winter seasons, 5813 and 2914 children, respectively, were admitted to our PED. Of those 1106 (19.0%) and 361 (12.3%) were tested for SARS‐CoV‐2. The number who tested positive were 133 (12.0%) in 2021–2022 versus just 30 (8.3%) in 2020–2021 (chi‐square(1) = 3.8, p = 0.029). In particular, we observed a peak of positive cases in the last two months of the 2021–2022 season, which was when the Omicron variant was circulating in Italy. The 48 (29.4%) positive cases in December 2021 and the 58 (35.6%) in January 2022 represented about 80% of all positive cases during the 2021–2022 study period (Figure 1).

FIGURE 1.

Monthly distribution of children who presented to the paediatric emergency department during the autumn and winter seasons in 2020–2021 and 2021–2022 and tested positive for SARS‐CoV‐2.

All the clinical and demographic characteristics of the study population are shown in Table 1. Data on disease severity, according to Parri et al's classification, ¹⁶ are presented for all 163 of the children who tested positive for SARS‐CoV‐2 during the two study years. These showed that 74 (45.5%) were asymptomatic, 54 (33.1%) presented with mild symptoms, 29 (17.8%) had severe symptoms, 3 (1.8%) required intensive care, and 3 (1.8%) had missing values. Oxygen saturation levels on admission were over 95% in 154 (94.5%) patients, while in only 3 (1.8%) they were between 92% and 95% and in the other 3 (1.8%) they were under 92%. Values were missing for 3 (1.8%) children. Of the 163 children who were SARS‐CoV‐2 positive, 76 (46.6%) underwent blood examinations. The average values were within the normal limits, with a slight increase in inflammation indices (C‐reactive Protein = 8.2 mg/L, IQR 0.8–20.3, normal value <0.5 mg/L).

TABLE 1.

Demographics, clinical features, triage codes and hospitalisation of children who tested positive for SARS‐CoV‐2 during the two study periods

		Children who tested SARS‐CoV‐2 positive
	Total study population (n = 163)	Study period (Sept 2021 to Jan 2022) (n = 133)	Previous wave (Sept 2020 to Jan 2021) (n = 30)	p value
Demographics
Age, years, median (25th‐75th percentile)	5.86 (1.43–11.81)	5.82 (1.19–11.69)	5.90 (1.76–12.76)	0.909
Male, n (%)	92 (56.4%)	75 (56.4%)	17 (56.7%)	1.000
Had contact with SARS‐CoV‐2, n (%)	100 (61.3%)	80 (61.5%)	20 (66.7%)	0.679
Immune deficiency, n (%)	1 (0.6%)	0 (0.0%)	1 (3.4%)	0.182
Premature birth, n (%)	6 (3.7%)	5 (3.9%)	1 (3.3%)	0.684
Other comorbidity, n (%)	19 (11.7%)	17 (13.1%)	2 (6.7%)	0.531
Urgency (triage colour code)	160 (98.2%)	131 (98.5%)	29 (96.7%)
Medium to high intensity, n (%)	8 (4.9%)	8 (6.1%)	0 (0.0%)	0.194
Moderate to low intensity, n (%)	152 (93.3%)	123 (94.6%)	29 (96.7%)
Missing values	3 (1.8%)	2 (1.5%)	1 (3.3%)
Clinical symptoms
Fever	99 (60.7%)	80 (62.5%)	19 (63.3%)	1.000
Respiratory symptoms	66 (40.5%)	53 (40.8%)	13 (43.3%)	0.839
Flu‐like symptoms	48 (29.4%)	36 (27.7%)	12 (40%)	0.269
Gastrointestinal symptoms	25 (15.3%)	20 (15.5%)	5 (16.7%)	0.532
Neurological symptoms	7 (4.3%)	3 (2.3%)	4 (13.3%)	0.024
Severity
Asymptomatic	74 (45.4%)	58 (44.6%)	16 (53.3%)	0.060
Mild	54 (33.1%)	42 (32.3%)	12 (40%)
Severe	29 (17.8%)	28 (21.5%)	1 (3.3%)
Critical	3 (1.8%)	2 (1.5%)	1 (3.3%)
Missing values	3 (1.8%)	3 (2.2%)	0 (0.0%)
Vaccination status	8 (4.9%)	8 (8.9%)	0 (0.0%)	0.092
Destination
Discharged home	121 (74.2%)	101 (75.9%)	20 (66.7%)
Hospitalisation	38 (23.3%)	29 (21.8%)	10 (33.3%)	0.233
Ward	35 (21.5%)	27 (93.1%)	9 (90.0%)	1.000
PICU	3 (1.8%)	2 (5.1%)	1 (2.6%)
Missing values	4 (2.5%)	3 (2.2%)	0 (0.0%)

Note: Bold values correspond to statistically significant p‐values. Missing values relate to data not reported in the medical records. IQR removed as no longer used.

Abbreviation: RT‐PCR, real‐time reverse transcriptase‐polymerase chain reaction.

Chest X‐rays were performed on 22 of the 163 (13.5%) children and only 10 (6.1%) were pathological. Of the 163 SARS‐CoV‐2‐positive cases, 121 (74.2%) were discharged at home and 38 (23.3%) were hospitalised, with only 3 (1.8%) children requiring admission to the paediatric intensive care unit. Data for the other 4 (2.5%) were missing.

When it came to treatment, antipyretics were the most frequently prescribed drugs, in 37.4% of cases. Only 11 (6.7%) children received antibiotic therapy and 13 (8%) received corticosteroids (data not shown). One patient presented with multisystem inflammatory syndrome related to COVID‐19, which also required treatment with intravenous immunoglobulins and subcutaneous low molecular weight heparin. Oxygen therapy was only necessary for 7 (4.3%) children.

When we compared the SARS‐CoV‐2‐positive cases admitted to the PED during the 2021–2022 autumn and winter season with the previous season, no statistically significant differences emerged for age, gender, history of contacts with SARS‐CoV‐2‐positive case, prematurity, immunodeficiency or other comorbidities (Table 1). No differences were observed between the two periods with regard to the triage colour code on admission. The clinical symptoms presented by children with COVID‐19 on admission to PED showed no statistically significant differences for fever, respiratory, gastrointestinal and flu‐like symptoms between the two periods. However, during the 2020–21 season, we observed a higher percentage of children presenting with neurological symptoms, such as ageusia, anosmia and convulsions than during the 2021–2022 season (13.3% versus 2.3%, chi‐square(1) = 7.08, p = 0.024). No difference is the severity of the disease was reported during the two periods (p = 0.071). A statistically significant difference in chest X‐rays was observed, as more were required in the 2020–21 season than in the 2021–2022 season (26.7% versus 10.9%, chi‐square(1) = 5.01, p = 0.038) (data not shown). No statistical difference was found with regard to the therapy performed and the frequency of hospitalisation (p = 0.541 and p = 0.233). Finally, only 8 of the 163 SARS‐CoV‐2‐positive children were vaccinated in 2021–2022, which corresponded to 0.72% of those admitted to the PED and tested for SARS‐CoV‐2. Of these, 5 were asymptomatic or had mild symptoms while only 3 had severe or critical symptoms. No statistically significant differences emerged between vaccinated and unvaccinated children with regard to the severity of reported symptoms (chi‐square(1) = 0.155, p = 0.655).

4. DISCUSSION

The main aim of this study was to evaluate the prevalence of SARS‐CoV‐2 infections in children with symptomatic COVID‐19 or flu‐like syndrome children who presented to the PED of an Italian tertiary hospital during the 2021–22 autumn and winter season, compared to the previous season. This enabled us to compare the impact of COVID‐19 periods when different variants were dominant. Our data showed a marked increase in children with COVID‐19 during the 2021–2022 autumn and winter season and the highest peak was reached between December 2021 and January 2022. This finding was in accordance with data provided by the Italian National Institute of Health, which stated that during the same period 19.4% of new cases of COVID‐19 were in patients under 18 years of age. This was much higher than the 7.5% recorded in the same months of the 2020–2021 season. ² , ¹⁷

The significant increase in SARS‐CoV‐2 infections in the paediatric population during the 2021–2022 autumn and winter season could be attributed to several factors. Firstly, the schools remained open during this season despite the increase in SARS‐CoV‐2 infections, unlike in 2020–2021, but there was a widespread use of surveillance tests and distance learning. Secondly, we must not forget the spread of the Omicron variant from November 2021. This variant has more mutations than previous variants. It could have greater or intermediate infectivity and, due to extensive mutations in the spike protein, it could evade immunity in vaccinated individuals. ¹⁴ However, studies performed in South Africa and the United States demonstrated that this variant had reduced virulence and lower COVID‐19 disease severity in adults. ¹⁸ , ¹⁹ , ²⁰ We were unable to find previous studies that assessed the prevalence and clinical profiles of SARS‐CoV‐2 infections in children during the 2021–2022 autumn and winter season, when the first Omicron cases emerged. Despite the increase in paediatric cases during the 2021–2022 season, no significant difference emerged with regard to the ages of infected individuals. When we analysed the symptoms reported by patients who presented to the PED, we found no differences in respiratory, gastrointestinal and flu‐like symptoms during the two study periods. Interestingly, a higher percentage of children with COVID‐19 reported neurological symptoms such as anosmia and ageusia, in the 2020–2021 season than 2021–2022 season. These echoed the findings of adult studies, which reported a low frequency of loss of smell and taste during study periods when Omicron was the dominant variant. ²¹ Even when we considered disease severity, we found no significant differences between the children with COVID‐19 who presented to the PED during the different study periods. During the 2020–2021 season, the most widespread SARS‐CoV‐2 variant was less infectious for children and severe paediatric cases of COVID‐19 were not described. However, the high transmissibility and short incubation period of the Omicron variant, which dominated part of our 2021–2022 study period, meant that the number of paediatric COVID‐19 cases markedly increased. Only mild clinical symptoms were observed in the majority of these patients, as reported by adult studies. ²¹ Some reports described more severe symptoms in children who tested positive for SARS‐CoV‐2 when the Omicron variant was dominant. Ludvigsson hypothesised that there was an association between COVID‐19 infections and convulsions in children infected by the Omicron variant. ²² This finding was not confirmed by our study, which found a low rate of neurological symptoms, particularly convulsions, in SARS‐CoV‐2‐positive children during the 2021–22 season. There were no difference in the PED presentation triage codes and in the hospitalisation rate during the two periods we analysed. This has been reported by other studies on adults presenting to emergency departments. In fact, Veneti et al found that the risk of hospitalisation was lower for people infected with the Omicron variant during this season. ²³ With regard to the examinations we performed, we found that there was a greater demand for chest X‐rays from PED paediatricians during 2020–21, when a more aggressive variant that posed a greater risk of pneumonia in adults was widespread. Thus, we hypothesise that the increased demand for X‐rays was more likely to have been related to physicians' concerns about possible lung disease, and knowing less about COVID‐19, than the children's disease severity. Finally, when we analysed children who had completed a full vaccination cycle, we found no differences in COVID‐19 disease severity. However, we want to highlight that the SARS‐CoV‐2 vaccination was only approved in Italy for children aged 12–18 and 5–11 in June and December 2021, respectively, so the percentage of vaccinated children included in the study was too low for a correct analysis.

Our study had a number of limitations. These included the monocentric nature of the study and the small number of children enrolled, as well as the retrospective nature, which did not allow us to study the variant involved in SARS‐CoV‐2‐positive cases. This was not a routine test in our hospital at the time of the study. The strength of the study was that this was the first paediatric study to describe the prevalence of SARS‐CoV‐2 infections in children when the Omicron variant first emerged.

5. CONCLUSION

This study examined the prevalence of SARS‐CoV‐2 in children during the autumn and winter season from 1 September 2021 to 30 January 2022 and compared it with the same period in 2020–2021. The Omicron variant, which was circulating in Italy from the end of November 2021, was more transmissible than previous ones and this contributed to a greater spread of SARS‐CoV‐2 infections in the paediatric population. The other contributory factor was the low percentage of vaccinated children. However, paediatric cases were relatively mild during both seasons, and hospitalisation rates were low.

FUNDING INFORMATION

This study did not receive any external funding.

CONFLICT OF INTEREST

The authors have no conflicts of interest to declare.

Curatola A, Ferretti S, Graglia B, Capossela L, Menchinelli G, Fiori B, et al. COVID‐19 increased in Italian children in the autumn and winter 2021–2022 period when Omicron was the dominant variant. Acta Paediatr. 2023;112:290–295. 10.1111/apa.16576