There is an ongoing worldwide pandemic involving a novel virus belonging to the family of coronaviruses (CoVs), including large, enveloped, positive-sense single-stranded RNA viruses (1). The virus that caused this pandemic is the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), and the disease it causes is the coronavirus disease 2019 (COVID-19). As of September 20, 2021, 228,506,698 COVID-19 cases have been confirmed, including 4,692,361 deaths reported to the World Health Organization (2), and this number continues to increase.

According to current epidemiological trends, children are less likely to be infected with SARS-CoV-2 than adults, and most pediatric cases are asymptomatic or mild (3). Pediatric COVID-19 typically presents with mild symptoms, such as cough, fever, sore throat, and diarrhea. However, some children, especially those with underlying diseases, may present with severe clinical manifestations such as hyperinflammatory syndrome (4, 5), increased severity of childhood-onset type 1 diabetes (6), and multisystem inflammatory syndrome (7). Acute myocarditis with intense systemic inflammation and atypical Kawasaki disease have also emerged as severe pediatric diseases after SARS-CoV-2 infection (4, 8).

Because most children with COVID-19 are asymptomatic or have mild symptoms, supportive treatment is usually sufficient, and hospitalization is unnecessary (9). Ensuring sufficient calorie and water intake, maintaining water-electrolyte balance and homeostasis, and strengthening psychotherapy for older children usually comprise adequate treatment (10). COVID-19 vaccines have been determined to be safe for adults, and trials to determine their safety for children are ongoing. When the evidence or epidemiological situation justifies a change in the vaccine policy, the World Health Organization will update its recommendations (11). With the continuing COVID-19 pandemic, children's mental health has begun to receive more attention. Many factors such as fear influence children's mental health. COVID-19 has instilled fear in children because they are worried about becoming sick and their parents having to stay home from work (12). Furthermore, changes in family economic conditions, protective confinement, social isolation, and deaths of loved ones have had varying degrees of effect on children's mental health (13–15). Therefore, innovative approaches that increase access to mental health services and promote resilience and mental well-being, such as maintaining social connections despite the isolation and renewing social ties during the recovery phase, should be explored. Similarly, increasing the identification of and support for children, adolescents, and families experiencing disproportionate effects of the pandemic and implementing preventive measures may reduce long-term mental health sequelae for children and adolescents (16).

Bibliometrics, the method we use in this study, applies statistics and mathematics to analyze written publications such as books and journal articles. Bibliometric methods can be used to analyze scientific literature in a specific field to assess the popularity and impact of specific publications, authors, and institutions. Bibliometric analyses provide quantitative and qualitative evaluations of publications and provide the developing trends of research domains (17). So far, there was one article about bibliometric analyses of pediatric COVID-19 that studied the articles for 6 months, from January 1, 2020, to June 11, 2020 (18). There were no similar bibliometric analyses of pediatric COVID-19 after June 11, 2020. Thus, in this study, we performed a bibliometric analysis to analyze various aspects of pediatric COVID-19 from the COVID-19 outbreak to September 20, 2021 and further identified its research hotspots and trends.

COVID-19 outbreak has resulted in global effects on adults and children. Wei et al. first published an article about COVID-19 in children in February 2020 (21). Since then, reports about this topic have significantly increased. In 2020, the number of reports was 1,357; however, by September 2021, the number had increased to 3,561. This increasing trend is consistent with the trend of the COVID-19 pandemic. More articles will be published to reveal the characteristics, effects, and treatment of pediatric COVID-19.

In another bibliometric analysis of pediatric COVID-19, their result showed that the United States, China, Italy and India were the counties that contributed the most articles by June 11, 2020. Our data showed, by September 20 2021, the United States had the most published articles, followed by Italy, the United Kingdom, and China. The published articles of United States, China and Italy maintain the increasing trends (18). The United States had the most published articles, followed by Italy, the United Kingdom, and China. China was the first country to discover and to report COVID-19. The United States experienced the highest number of new coronavirus infections and deaths. In March 2020, SARS-CoV-2 infections began to exponentially increase in the United States, placing a substantial burden on the healthcare system (22). Later, the COVID-19 pandemic forced the Italian government to enforce extreme measures and to place the entire country under lockdown conditions (23). On February 28, 2020, Lillie et al. reported the first two patients in the United Kingdom with person-to-person transmission (24). In terms of cooperation among countries, the United States cooperated most with different countries, especially Japan and India. Seven of the 10 countries that lead in cooperation are European, indicating that cooperation among European countries is quite frequent.

The 10 most highly cited articles were from the United States and the United Kingdom. Furthermore, the 10 most cited articles were related to clinical features and epidemiological characteristics of pediatric COVID-19, indicating that this is a hotspot for pediatric COVID-19 research and that researchers are focusing on this topic. The article “Epidemiology of COVID-19 Among Children in China” by Dong et al. was published during the early stages of the pandemic, enrolled 2,135 pediatric patients with COVID-19, and explored epidemiological characteristics and transmission patterns in mainland China (20). Therefore, this report has gained widespread attention and has been widely cited.

Among the 10 institutions with the most published articles, 70% were in the United States. Among the 10 institutions with the most frequently cited articles, 40% were in the United States, indicating that the United States performs more research on this topic. It is worth noting that of the 10 institutions with the most publications, only one was in China; however, five of the 10 institutions with the most frequently cited articles were in China. Huazhong University of Science and Technology published the most articles and the citation numbers was the top two institutions. Shanghai Jiao Tong University, with 16 articles, is not among the 10 institutions with the most articles; however, it has the most frequently cited articles. Xi'an Jiao Tong University, Nanjing Medical University and Anhui Medical University published <10 articles but their article owned high citation. The reason may due to that China was the first country to study and report cases of COVID-19, and its effective treatment experience has provided a clinical reference for more physicians and scholars. The University of Pennsylvania was the institution with the third highest number of published articles and these articles were the most frequently cited in the institutional analysis.

Compared with Monzani et al.'s article (18), the most highly cited articles and top 10 institutions were different. The reason is not just due to the time of bibliometric analysis, but because of the different search strategies. To focus on the specific pediatric trends, the search strategy that we used was keywords in author keywords and titles. To cover all the children, besides pediatric and child, we also used the keywords including baby, newborn, infant, and toddler.

The authors Alberto Villani from the Bambino Gesù Children's Hospital, IRCCS, in Italy and Shao Jianbo from Huazhong University of Science and Technology in China have published the most articles about COVID-19 in children and have performed more research in the field and might be more knowledgeable about research trends. Therefore, following their research developments and trends may help us understand the forefront of pediatric COVID-19 academics. For example, researchers focused on clinically relevant research of COVID-19 in children, such as the diagnosis (25, 26), clinical features (27, 28), clinical management (29–31), and treatment of COVID-19 in combination with other diseases (32, 33). The articles by Shao are mainly related to the differentiation of COVID-19 and other pulmonary infections in children (34–36), clinical and computed tomography features (37–40), and COVID-19-related immunology studies (41–43).

Pediatrics was one of the most authoritative journals and was classified as Q1 by JCR. The impact factor of Pediatrics was the highest of the top 10 most active journals. The aforementioned most cited article was published by Pediatrics (20). The articles from Pediatrics were widely cited by researchers. Frontiers in Pediatrics contributed the most pediatric COVID-19 articles, but was not the most cited journal. The Pediatric Infectious Disease Journal was the journal which published the second largest number of articles and had the second largest number of citations, after Pediatrics. We can, therefore, follow these active journals to learn the trends of pediatric COVID-19.

Researchers in the USA collaborated with the most countries, including the UK, China, India and Australia. Together, these countries formed the biggest cluster of collaborating countries. Researchers in European countries frequently cooperated with each other and formed the second cluster of collaborating countries. Italian researchers most frequently worked with other European researchers, which may due to the geographical position and the widespread incidence of COVID-19 in Italy (44). Of the collaborating authors, the biggest cluster was from Italy.

In terms of co-authorship, Alberto Villani, Danilo Buonsenso and Andrea Campana, who are all from Rome, Italy, had the largest number of collaborations. Alberto Villani and Andrea Campana are both affiliated with the University Department of Pediatrics, Bambino Gesù Children's Hospital. Danilo Buonsenso is affiliated with the Department of Woman and Child Health and Public Health, Fondazione Policlinico Universitario A. These authors are all in the rank of top 10 greatest number of publications. They have contributed the most co-authored articles and have close academic ties with other authors, which allows us to more clearly recognize this excellent team of scholars.

Our analysis of the clinical research related keywords identified that the most frequent keywords were MIS-C, infections, epidemiology, disease, infant, Kawasaki-disease, diagnosis, and pneumonia. These words draw more attention to COVID-19 research. Initially, the clinical manifestations of pediatric COVID-19 were unknown; therefore, manifestation and diagnosis were the most important keywords. The morbidity and mortality of COVID-19 disease in children were low, but MIS-C and Kawasaki disease are more serious diseases which occur as a result of SARS-CoV-2 infection (7, 8). Kawasaki-like disease associated with COVID-19 has been increasingly reported. Large case series of Kawasaki disease related to SARS-CoV-2 infection from the UK, Italy, America, and France have been published (45). MIS-C is a newly defined condition, caused by a storm of inflammatory factors associated with COVID-19. Critically ill children with COVID-19 associated MIS-C have a spectrum of severity broad damage (46). Similar to Kawasaki disease, MIS-C has multi-system involvement and can lead to severe myocardial damage (47).

Our results showed that pandemic, adolescents, mental health, health, impact, care, parents, and stress were the frequently occurrence keywords. These keywords appeared later than the clinical research. This remind us the new hotspot for pediatric COVID-19 research is gradually shifting from COVID-19 itself and its related clinical studies to studies of the psychological impact and social impact on children; this may be because, as the epidemic continues, home isolation, social distancing, and fear of disease have had significant effects on the schooling, lives, and mental health of children (16, 48). The World Health Organization focusses their attention on the social effects of COVID-19 on children and adolescents, including ensuring safe schooling, minimizing the disruption of health systems for children, safeguarding the quality of their care and so on (49).

The data analysis is comprehensive and objective. However, some limitations remain. Firstly, we only enrolled publications in English which may exclude some important non-English studies related to the pediatric COVID-19. Second, because we need keywords to analyze the research trends, we excluded the letters in bibliometric analysis. Moreover, as the database is still being updated, the bibliometric analysis results may differ slightly from the present research situation.

In conclusion, this bibliometric analysis provided an overview of pediatric COVID-19 studies and identified some significant issues. The topic of pediatric COVID-19 has attracted considerable attention worldwide, thus leading to a considerable number of articles published over the past 2 years. This study demonstrated that the United States, China, and Italy have leading roles in pediatric COVID-19 research. Furthermore, the new research hotspot is gradually shifting from COVID-19 and related clinical studies to studies of psychological and social impacts on children.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

SH and HC conceived the study. SH, YM, and XW analyzed the data. HC designed and supervised the study. All authors contributed to the data analysis and reviewed and edited the manuscript.

This work was supported by the National Natural Science Foundation of China (Grant No. 81800021) and the Jilin Provincial Key Laboratory of Biotherapy (Grant No. 20200201464JC).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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