Abstract
Background
SARS-CoV-2 continues to mutate over time, and reports on children infected with Omicron BA.5 are limited. We aimed to analyze the specific symptoms of Omicron-infected children and to improve patient care.
Methods
We selected 315 consecutively hospitalized children with Omicron BA.5 and 16,744 non-Omicron-infected febrile children visiting the fever clinic at our hospital between December 8 and 30, 2022. Specific convulsions and body temperatures were compared between the two cohorts. We analyzed potential associations between convulsions and vaccination, and additionally evaluated the brain damage among severe Omicron-infected children.
Results
Convulsion rates (97.5% vs. 4.3%, \(P\) < 0.001) and frequencies (median: 2.0 vs. 1.6, \(P\) < 0.001) significantly differed between Omicron-infected and non-Omicron-infected febrile children. The body temperatures of Omicron-infected children were significantly higher during convulsions than when they were not convulsing and those of non-Omicron-infected febrile children during convulsions (median: 39.5 vs. 38.2 and 38.6 °C, both \(P\) < 0.001). In the three Omicron-subgroups, the temperature during convulsions was proportional to the percentage of patients and significantly differed (\(P\) < 0.001), while not in the three non-Omicron-subgroups \((P\) = 0.244). The convulsion frequency was lower in the 55 vaccinated children compared to the 260 non-vaccinated children (average: 1.8 vs. 2.1, \(P\) < 0.001). The vaccination dose and convulsion frequency in Omicron-infected children were significantly correlated (\(P\) < 0.001). Fifteen of the 112 severe Omicron cases had brain damage.
Conclusions
Omicron-infected children experience higher body temperatures and frequencies during convulsions than those of non-Omicron-infected febrile children. We additionally found evidence of brain damage caused by infection with omicron BA.5. Vaccination and prompt fever reduction may relieve symptoms.
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Introduction
Common symptoms in children with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection include fever, cough, sore throat, fatigue, vomiting, and diarrhea [1, 2]. Previous studies have reported that children infected with early variants of SARS-CoV-2 present with symptoms that differ from those observed in adults [3]. SARS-CoV-2 continues to mutate over time [4,5,6,7], and reports on children infected with Omicron BA.5 are limited.
On December 7, 2022, the Chinese government relaxed its dynamic zero-coronavirus disease 2019 (COVID-19) policy, and the country experienced the fastest-increasing wave of Omicron infections globally [8]. The Guangzhou Women and Children's Medical Center is the only hospital the Guangzhou Municipal Government designated to treat children with severe SARS-CoV-2 infection. Previous studies have revealed that febrile convulsions in children occurred in < 7% of cases, with the majority occurring in those < 5 years [9, 10]. However, we observed that the majority of hospitalized children infected with Omicron displayed convulsion signs with cyanosis (blue lips), eyes rolling up and staring, and trembling limbs that did not respond to calls, suggesting that the central nervous system (CNS) of these children may be involved.
Tetsuhara et al. reported severe and repetitive convulsions in a neonate infected with SARS-CoV-2 Omicron [11]. Chongqing University Three Gorges Hospital reported that 84 children infected with Omicron were hospitalized for convulsions between December 11, 2022 and December 26, 2022, similar to our observations [12]. Recently, high rates of convulsions in Omicron-infected children have also been reported [13, 14]. However, the above studies lacked comparative analyses with non-Omicron-infected children.
We aim to evaluate the specific convulsions and body temperature in Omicron-infected children using two cohorts of children—those with and without Omicron fever, analyze the effects of age and vaccination on convulsions, and assess the evidence of brain damage in Omicron-infected children. We also attempted to improve the management of children infected with Omicron based on our findings.
Methods
Design and participants
This study was approved by the Ethics Committee of the Guangzhou Women and Children’s Medical Center ([2023] NO.015A01). Participants included 333 consecutively hospitalized children with SARS-CoV-2 infection and 17,499 non-SARS-CoV-2-infected febrile children attending the fever clinic at the Guangzhou Women and Children’s Medical Center between December 8 and 30, 2022. SARS-CoV-2 infection was confirmed by rapid reverse transcription polymerase chain reaction (RT-PCR). All COVID-19 cases were infected with Omicron BA.5, according to the Municipal Centre for Disease Control and Prevention, which conducted surveillance of the outbreak’s variants using whole-genome sequencing (WGS). Figure 1 illustrates the study flow.
Measurements and instruments
Epidemiological information, including patient vaccinations, medical history, irrational medicine use before hospital admission, and treatment regimens, was collected through standard epidemiological questionnaires and interviews. The frequency and duration of the convulsions were also recorded. Clinical records and laboratory test results were reviewed from electronic medical records. The data retrieved included blood gas electrolytes, routine blood tests, biochemistry, coagulation, respiratory pathology for RT-PCR, and immunoglobulin M (IgM) antibody testing for acute respiratory tract infections.
Ten respiratory pathogens were detected using RT-PCR, including influenza virus types A and B (INFA and IFVB), respiratory syncytial virus (RSV), enterovirus, Mycoplasma pneumoniae (MP), Chlamydia pneumoniae (CP), adenovirus (ADV), metapneumovirus, human bocavirus (HBoV), rhinovirus (RhV), and parainfluenza viruses (PIVs). IgM antibodies for nine acute respiratory tract infection pathogens, including Legionella pneumophila type 1, MP, rickettsia, CP, ADV, RSV, INFA, IFVB, and PIV types 1, 2, and 3, were tested using indirect immunofluorescence. Legionella pneumophila type 1, MP, CP, ADV, and RSV overlapped with the ten pathogens screened using RT-PCR.
Intracranial damage was confirmed via magnetic resonance imaging (MRI) of the brain (Philips Magnetic Resonance Ingenia 3.0 T). Cerebrospinal fluid (CSF) analysis (using CX41 Olympus and BC-7500 CS Mindray), including glucose, chloride, alanine aminotransferase, aspartate aminotransferase, lactate dehydrogenase, and creatine kinase, was performed to diagnose intracranial inflammation.
The patient's temperature on admission was taken via axillary measurement. During an episode of convulsion, the temperature was taken more than once using an electronic forehead thermometer. Finger-clip oximeters were used to obtain functional oxygen saturation readings (SpO2). The highest temperature and lowest SpO2 recorded were used for analyses in this study.
Exclusion criteria
An infectious disease physician, a respiratory physician responsible for patient care, and a medical information engineer jointly examined and confirmed the accuracy of the clinical data. In the Omicron-infected group, cases with simultaneous infections with other microbiological agents were excluded. In the group of febrile children with non-Omicron infection, non-infectious diseases, including those caused by diseases such as tumors, autoimmune diseases, and blood disorders, were excluded, leaving 17,499 cases. Additionally, Omicron and non-Omicron cases with convulsions possibly caused by medications or previous diseases were excluded (Fig. 2).
Statistical analysis
The convulsion rate was compared between Omicron and non-Omicron febrile cases using Pearson’s X2 test. The body temperatures and convulsion frequencies of Omicron and non-Omicron febrile cases were compared using the Mann–Whitney U test. The percentage of patients stratified according to body temperature within both groups was compared using Pearson’s Χ2 test. Vaccination rates were compared between Omicron cases with and without convulsions using Fisher's exact test. The non-parametric Spearman's rank correlation coefficient was conducted in Omicron-infected children with convulsions to assess the effect of age and COVID-19 vaccination dose on convulsion frequency, because the non-normality of these data distributions was assessed beforehand using the Kolmogorov–Smirnov test. We considered \(P\) ≤ 0.05 significant. Data were analyzed using SPSS version 17 (IBM Corp., Chicago, IL, USA).
Results
Characteristics of hospitalized children with Omicron BA.5 infection
The final data included 315 Omicron BA.5-infected children and 16,744 febrile children without Omicron infection after exclusion (Fig. 2). The median age was 2.08 years (0.08–14.00 years) in Omicron-infected children and 2.52 years (0.01–18.00 years) in non-Omicron-infected febrile children. There were 122 (36.6%) and 7454 (42.6%) females in the two groups, respectively. The epidemiological characteristics, clinical features, laboratory test results, and radiological findings of the 315 hospitalized children with Omicron infections are summarized in Table 1. Notably, 260 (82.5%) of these hospitalized children (n = 315) were not vaccinated. The epidemiological characteristics and clinical features of 16,744 febrile children with non-Omicron infection were presented in the Supplementary Information (Supplementary Table 1).
Comparison of symptoms in Omicron-infected children and the control group
Three hundred and seven (97.5%) of the 315 children with Omicron infection convulsed during hospitalization, which is 22.7 times more than that (4.3% or 721/16,744) in febrile children without Omicron attending the hospital’s fever clinic during the same period (Fig. 3a). The number of convulsions was significantly higher in Omicron-infected children with convulsions than in non-Omicron-infected children with convulsions (median: 2.0 vs. 1.6, \(P\) < 0.001). Figure 3b illustrates that the body temperatures of Omicron-infected children were significantly higher than those of non-Omicron-infected febrile children (median body temperature: 39.5 vs. 38.6 °C, \(P\) < 0.001). Furthermore, we stratified the temperature data during convulsions for both cohorts and then compared the percentage of patients within groups. Specifically, 3.3%, 35.5%, and 61.2% of the Omicron-infected children had temperatures of ≤ 38.0, 38.1–39.0, and > 39.0 °C during convulsions (\(P\) < 0.001), while for the three groups of non-Omicron-infected febrile children, the percentages were 30.9%, 34.4%, and 34.7% (\(P\) = 0.244), respectively (Fig. 3c). These findings suggest that higher temperatures in Omicron-infected children may partly be responsible for their higher rates of convulsion compared to non-Omicron-infected febrile children during convulsions.
Comparative analysis between groups of the Omicron-infected children and non-Omicron-infected febrile children. a Comparison of convulsion rates; b Comparison of body temperature during convulsions; c Distribution of body temperatures during convulsions in Omicron-infected children and control children. °C degrees Celsius
Pathogen testing was additionally done after SARS-CoV-2 testing of pharyngeal and nasal swabs from the Omicron-infected and control groups. In the group of hospitalized children infected with Omicron, nine positive RT-PCR tests were detected in 117 cases, and four positive IgM antibody tests were found in 77 cases. In the febrile group of non-Omicron-infected children, 6832 RT-PCR tests were positive in 3431 cases, and 673 IgM antibody tests found 289 positive cases. The pathogens with high positivity rates were, in descending order, MP, RSV, ADV, PIV, HBoV, and RhV.
Within-group analyses of Omicron-infected children
The Mann–Whitney U test revealed that the body temperatures of 307 Omicron-infected children were significantly higher during convulsions than when they were not convulsing (median body temperature: 39.5 vs. 38.2 °C, \(P\) < 0.001) (Fig. 4a). Among the 315 Omicron-infected children, the Mann–Whitney U test showed that 55 vaccinated children had a significantly lower frequency of convulsions than 260 unvaccinated children (mean frequency of convulsions: 1.8 vs. 2.1, \(P\) < 0.001) (Fig. 4b). The vaccination rate was higher among the eight Omicron-infected children without convulsions than in the 307 Omicron-infected children with convulsions (Fisher's exact test; 50.0% vs. 16.6%; \(P\) = 0.034) (Fig. 4c).
Within-group comparative analysis of children hospitalized with Omicron infection. a Comparison of body temperature in Omicron-infected children with and without convulsions; b Comparison of the frequency of convulsions in vaccinated and non-vaccinated children infected with Omicron; c Comparison of the rate of vaccination in convulsed and non-convulsed Omicron-infected children. °C degrees Celsius
A multifactorial correlation analysis of 307 Omicron-infected children with convulsions revealed that the convulsion frequency was significantly correlated with vaccination doses using Spearman's rank correlation coefficients (\(P\) < 0.001) (Table 2). Age was negatively but not significantly correlated with the frequency of convulsions (correlation coefficient = − 0.024, \(P\) = 0.681); older children had relatively fewer frequencies of convulsions (Table 2).
Examination of brain damage
Brain MRI was performed in 112 Omicron-infected children with suspected CNS involvement with peak respiratory frequency > 30 breaths/minute, SpO2 < 94% at rest, and > 2 convulsions among 307 children infected with Omicron and presenting with convulsions. Fifteen of them showed brain damage, with major locations in the thalamus, corpus callosum, frontal lobe, parietal lobe, occipital lobe, and basal ganglia. Figure 5 depicts a patient with thalamic damage. Out of these 15 patients, 14 agreed to undergo biochemical analysis, and 12 exhibited signs of intracranial inflammation. In addition, we reviewed the clinical records and found no vaccination records among these 15 children with brain damage. Among 721 children with fever and convulsions who were non-Omicron-infected, 49 patients with complicated convulsions and suspected brain damage underwent brain examination by MRI or computed tomography (CT), and 43 of them also underwent CSF analysis, which found imaging brain damage in 11 cases and intracranial inflammation in three cases, respectively.
MRI images of a child with Omicron BA.5 infection, showing damage to the thalamus. a T1WI showed a low signal; b T2WI showed a high signal; c FLAIR water suppression showed a significantly high signal; d DWI showed a significantly high signal; e ADC showed a slightly high signal at the lesion's periphery and a low signal at the center; f DWI showed a slightly increased signal in the splenium of the superior corpus callosum. MRI magnetic resonance imaging, FLAIR fluid attenuated inversion recovery, ADC apparent diffusion coefficient, DWI diffusion weight imaging
WGS of 848 cases sampled in the city by the Guangzhou Center for Disease Control and Prevention showed that all were infected with Omicron BA.5. We performed CSF analysis in the pediatric patients mentioned above to diagnose intracranial inflammation for rapid symptomatic treatment. Due to limited medical resources at the time, no further viral testing of the CSF was performed.
Outcomes of patients
For the 315 children with Omicron infection, palliative treatments were administered immediately upon admission—two critically ill patients among them were admitted to the intensive care unit (ICU). Initial treatments mainly included ibuprofen or acetaminophen for fever, oseltamivir for viral infections, and cefazolin sodium for bacterial infections. Nebulizing cough and sputum-clearing treatments were administered. During convulsions, intravenous midazolam at a dose of 0.2–0.3 mg/kg was administered to sedate children who convulsed for over 5 min. Furthermore, children with high-grade fever were wiped with wet towels to reduce the fever. Patients with severe disease were also administered 400 mg/kg of gamma globulin to nourish the nervous system and boost immunity for 3–5 days.
By December 30, 2022, 255 (81.0%) of the 315 patients had been discharged because they were significantly better, had stable vital signs, and had normal temperatures for more than 24 h. Out of the 12 children diagnosed with intracranial inflammation, 10 were discharged as the lesions had disappeared or shrunk on MRI reexamination. Additionally, three of these children developed motor dysfunction that recovered after approximately 2 weeks of rehabilitation. One of the two children who remained in the hospital had improved imaging features and had been discharged from the ICU, but was still being treated for motor deconditioning. The other child remained in the ICU. On December 28, 2023, we reviewed the follow-up records of these two patients with intracranial inflammation. One of them had improved, but not fully recovered, motor skills accompanied by right lower extremity claudication. Sadly, the other patient died on January 4, 2023, in the ICU.
Discussion
This study had several crucial points. First, symptoms of convulsions and fever were comprehensively analyzed based on real-world data from 315 hospitalized children with Omicron infection and 16,744 non-Omicron-infected febrile children during the same period at our hospital. The rate of convulsions in children infected with Omicron was 22.7 times higher than that in non-Omicron-infected febrile children. The body temperatures of Omicron-infected children during convulsions were significantly higher than when not convulsing and the temperatures of non-Omicron-infected febrile children (both \(P\) < 0.05). In the Omicron-subgroup, the temperature during convulsions was proportional to the percentage of patients and significantly differed (\(P\) < 0.001), while it did not differ significantly in the non-Omicron-subgroup (\(P\) = 0.244). These results suggest that prompt fever reduction may reduce the rate of convulsions in Omicron-infected children. Second, there was a significant correlation between the vaccination dose and the frequency of convulsions (\(P\) < 0.05), and whether the vaccine was received or not was significantly correlated with the rate of convulsions (\(P\) < 0.05). Third, potential evidence of brain damage was observed in severe cases of Omicron infection, and among these affected children, those with brain damage had no COVID-19 vaccination records. Finally, the epidemiological characteristics, clinical features, laboratory tests, and radiological findings of children hospitalized with Omicron BA.5 infection were properly summarized. Overall, the results of this study may serve as a useful reference to facilitate clinical workflows and to develop vaccination policies for Omicron-infected children.
A recent study suggested that Omicron subvariants could be changing how it attacks the human body—infecting respiratory systems and targeting the brain [15]. However, it is important to note that the study used animals instead of humans. Another report suggested that convulsions in children may be related to brain damage [16]. Here, we found that among 112 patients with severe infection, 15 (13.4%) showed intracranial damage in MRI, and 12 (10.7%) had intracranial inflammation detected through CSF biochemical tests. Our clinical evidence suggests that close attention needs to be paid to brain damage in the management of children infected with Omicron BA.5. In addition, the long-term outcomes of intracranial damage or inflammation in a subset of children infected with Omicron are unknown; therefore, continued follow-up of these children by clinicians is required.
Studying the differences in the effects of SARS-CoV-2 on humans as it continues to mutate over time is an important step in clinical management. In a meta-analysis by Misra et al., including 350 studies of 145,721 COVID-19 patients of all ages, up to a third of those patients experienced at least one neurological symptom. That study covered 31 December 2019 to 15 December 2020, which was about 1 year before the Omicron wave. However, it was clear from the paper that convulsions had rarely been reported in children with COVID-19 [17]. Another pre-Omicron wave study reported convulsions in 0.5% of COVID-19 children [18]. In contrast, Sahin et al. reported that seizures were more common during the Omicron period compared to the pre-Omicron (nonvariant, Alpha, and Delta) period [19]. In the early stages of the Omicron (B.1.1.529) wave, 31% of hospitalized children in South Africa developed convulsions [20]. The Tokyo Metropolitan Children's Medical Center in Japan and the pediatric department in Örebro, Sweden, also reported convulsions in children who were later tested for Omicron infection [21, 22]. In the Asia University Hospital in Korea, 62.9% of 97 children who developed convulsions during the Omicron wave were COVID-19 positive, with a significantly higher convulsion rate compared to that of the pre-Omicron wave (0.5% vs. 62.9%, \(P\) < 0.001), and patients had a higher mean age and peak body temperature [13]. Thongsing et al. reported increased convulsion rates in infected children (88%, 14/16) during the Omicron wave [14]. A study in Chongqing, China, reported that 84 children hospitalized for the Omicron infection during the Omicron outbreak experienced convulsions [12]. In this study, we observed specific symptoms in a larger group of children infected with Omicron BA.5, found evidence of brain damage in severe patients, investigated strategies to prevent infection in children, and explored palliative treatment approaches.
Our study revealed that both vaccination status and the dosage of the vaccine were significantly associated with disease severity. In addition, these children with brain damage had not received the COVID-19 vaccine. Another study reported that vaccinating children aged 6 months to 5 years reduced the severity of their condition [23]. The Pediatric Pulmonology Department of a University Hospital in Paris observed that during the Omicron wave (between December 15, 2021, and February 28, 2022), the monthly hospitalization rate of unvaccinated children was six times higher than that of fully vaccinated children [24]. A multicenter study conducted in 14 states of the USA reported significant differences in hospitalization rates between vaccinated and unvaccinated children and adolescents [25]. The Centers for Disease Control and Prevention (CDC) in America has expanded the updated COVID-19 vaccines to include children aged 6 months to 5 years [26]. Since January 8, 2023, the Chinese government has implemented "Class B management measures for novel coronavirus infections" [8], implying that more children may be infected with SARS-CoV-2 variants. In this observational study, 83.1% (262) of children hospitalized for Omicron BA.5 infection were under 3 years of age. Currently, children under 3 years are ineligible for vaccination in China. Therefore, if the COVID-19 vaccine is administered to children aged 6 months to 5 years in China, it may potentially reduce the disease severity.
Our study has several limitations. First, the sample size of hospitalized children with Omicron infections was insufficient. Second, owing to the sudden relaxation of epidemic control measures, a short-term surge occurred in hospitalized children with Omicron infection, and many clinicians were also infected. Therefore, the clinical records might be incomplete. In particular, the vast majority of non-Omicron-infected febrile children had mild symptoms and were not hospitalized, and their clinical information was incomplete. Third, pathogen testing, brain MRIs, and CSF analysis were performed at our hospital only when clinically necessary; therefore, not all patients had these tests performed.
In conclusion, our findings demonstrate that children infected with Omicron BA.5 have higher body temperatures than those with common fevers, experience specific convulsions, and may result in brain damage. Vaccination and prompt fever reduction may reduce the disease severity. Further pathophysiologic studies are needed to elucidate the potential effects of Omicron BA.5 on the CNS.
Data availability
Any qualified investigator access to the data for this study will be possible upon request by contacting the corresponding authors and approval by the Ethics Committee of the Guangzhou Women and Children's Medical Center.
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Acknowledgements
The authors would like to thank all included children and their parents for their cooperation with this study.
Funding
This study was supported by the Science and Technology Planning Project of Guangdong Province (No. 2020B1111170001). The funder had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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PYY, WHL, TJL, and GST: conceptualization, formal analysis, and writing—original draft. YGQ, XY, HMX, and WJR: writing—review. TJH, LXH, YXT, FCX, PJZ, WZY, SY, DR, LYF, THM, LYY, QZX, LZC, TJP, ZFS, ZKL, and ZYR: investigation. WHY: investigation and formal analysis. CXJ: information collection. PYY, WHL, YGQ, and XY contributed equally to this work. All the authors had full access to all the data in the study and had final responsibility for the decision to submit for publication.
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No financial or non-financial benefits have been received or will be received from any party related directly or indirectly to the subject of this article. Si-tang Gong is a member of the Editorial Board for World Journal of Pediatrics. The paper was handled by the other Editor and has undergone rigorous peer review process. Si-tang Gong was not involved in the journal's review of, or decisions related to, this manuscript.
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This study was approved by the Ethics Committee of the Guangzhou Women and Children's Medical Center ([2023] NO.015A01).
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Pei, YY., Wang, HL., Yin, GQ. et al. Specific convulsions and brain damage in children hospitalized for Omicron BA.5 infection: an observational study using two cohorts. World J Pediatr (2024). https://doi.org/10.1007/s12519-024-00808-z
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DOI: https://doi.org/10.1007/s12519-024-00808-z