Abstract

The objective was to perform a spatial analysis of the hospital mortality rate (HMR) due to severe acute respiratory syndrome (SARS) attributed to COVID-19 among children and adolescents in Brazil from 2020 to 2021. A cluster method was used to group federal units (FUs) based on HMR. In 2020, clusters with high HMRs were formed by north/northeast FUs. In 2021, there was a reduction in HMR. Clusters with higher rates remained in the N/NE region. Regional differences were observed in the HMR. The findings may reflect social inequalities and access to hospital care, especially in the under 1-year-old age group due to the severity of the disease in this group.

Key words:
Severe acute respiratory syndrome; Child; Adolescent; COVID-19; Spatial analysis

Resumo

Objetivou-se realizar uma análise espacial da taxa de mortalidade hospitalar (TMH) por síndrome respiratória aguda grave (SRAG) atribuída à COVID-19 em crianças e adolescentes no Brasil no período de 2020 a 2021. Utilizou-se o método de cluster para agrupar as unidades federativas (UFs) com base na TMH. Em 2020, clusters com altas TMHs foram formados por UFs Norte/Nordeste. Em 2021, houve redução na TMH. Os clusters com maiores taxas permaneceram na região N/NE. Diferenças regionais foram observadas nas TMHs. Os achados podem refletir as desigualdades sociais e o acesso à atenção hospitalar, principalmente na faixa etária de menores de 1 ano pela gravidade da doença neste grupo.

Palavras-chave:
Síndrome respiratória aguda grave; Criança; Adolescente; COVID-19; Análise espacial

Introduction

On January 30, 2020, the outbreak of the new coronavirus was declared a Public Health Emergency of International Importance. On March 11, 2020, COVID-19 was considered a pandemic by the World Health Organization¹1 World Health Organization (WHO). Novel Coronavirus (2019-nCoV) technical guidance [Internet]. Geneva: WHO; 2020 [cited 2023 mar 18]. Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019.. In late May 2020, Latin America was declared the epicenter of the COVID-19 pandemic, mainly because of Brazil, one of the most severely affected countries by COVID-19 with more than 37 million cases and 699,634 deaths reported by March 2023²2 World Health Organization (WHO). Coronavirus disease (COVID-19) situation dashboard (COVID-19), 2023 [Internet]. [cited 2023 fev 28]. Available from: https://covid19.who.int/region/amro/country/br.
https://covid19.who.int/region/amro/coun... .

COVID-19 is associated with severe acute respiratory syndrome (SARS), which can progress to death³3 Coronaviridae Study Group of the International Committee on Taxonomy of Viruses. The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol 2020; 5(4):536-544.. Since the beginning of the COVID-19 pandemic in March 2020, accumulated deaths due to SARS have increased among children and adolescents in Brazil⁴4 Brasil. Ministério da Saúde (MS). Doença pelo Coronavírus COVID-19. Boletim Epidemiológico Especial 78, 2021 [Internet]. [acessado 2022 abr 8]. Disponível em: https://www.gov.br/saude/pt-br/centrais-deconteudo/publicacoes/boletins/boletins-epidemiologicos/covid19/2021/boletim_epidemiologico_covid_78-1.pdf.
https://www.gov.br/saude/pt-br/centrais-... . As the pandemic of COVID-19 progressed, severe and fatal manifestations appeared, and the emergence of multiple variants, especially Delta and Omicron, contributed to an increase in the number of cases and pediatric hospitalizations⁵5 Ferreira LS, Müller GC, Campos FEM, Borges ME, Almeida GB, Poloni S, Simon LM, Bagattini ÂM, Rosa MQM, Diniz Filho JAF, Kraenkel RA, Coutinho RM, Camey AS, Kuchenbecker RS, Toscano CM. Modelagem do Impacto Estimado da Vacinação de Crianças de 5-11 anos Contra a COVID-19 no Brasil [Internet]. 2022 [acessado 2023 mar 18]. Disponível em: https://sbim.org.br/images/files/modelagem-vacinacao-criancas-15fev2022.pdf.
https://sbim.org.br/images/files/modelag... .

A report published by the WHO points out that the risks due to exposure, biological factors, economic implications and social determinants show variability among those exposed to infection¹1 World Health Organization (WHO). Novel Coronavirus (2019-nCoV) technical guidance [Internet]. Geneva: WHO; 2020 [cited 2023 mar 18]. Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019.^,66 Nepomuceno MR, Acosta E, Alburez-Gutierrez D, Aburto JM, Gagnon A, Turra CM. Besides population age structure, health and other demographic factors can contribute to understanding the COVID-19 burden. Proceedings of the National Academy of Sciences of the USA 2020; 117(25):13881-13883.. The pandemic is strongly influenced by social and economic inequalities, which increase the challenge for prevention and control of COVID-19⁷7 Rosalva RS, Soares GGM, Oliveira Neto BL, Lira Neto JB. A Interiorização da COVID-19 nos municípios do Estado de Pernambuco, Nordeste do Brasil. Rev Bras Saude Mater Infant 2021; 21(1):109-120.. In this context, looking at the territory allows us to recognize the particularities of the dynamics of the evolution of the pandemic, which favors the design of specific strategies for its confrontation in the territory⁸8 Costa MA, Lui L, Santos RMD, Curi RLC, Albuquerque CGD, Tavares SR, Krause CH. Apontamentos sobre a dimensão territorial da pandemia da COVID-19 e os fatores que contribuem para aumentar a vulnerabilidade socioespacial nas unidades de desenvolvimento humano de áreas metropolitanas brasileiras. Nota Técnica IPEA 2020 [Internet]. [acessado 2022 maio 18]. Disponível em: http://repositorio.ipea.gov.br/handle/11058/9985.
http://repositorio.ipea.gov.br/handle/11... . In a pandemic, deaths reveal problems such as social inequalities and health inequalities, including difficulty accessing health services, care gaps, the low quality of outpatient and hospital care provided, and weaknesses in the death surveillance system⁹9 Branco MRFC. Excesso de mortes no Brasil durante a pandemia de COVID-19. In: Carbonari PC, Peruzzo NA, Rosa E, editores. Sociedade Maranhense de Direitos Humanos. Violações dos direitos humanos no Brasil: denúncias e análises no contexto da COVID-19. São Luís: Passo Fundo; 2021. p. 23-33..

Analyses of hospitalizations, deaths, and mortality rates are essential for developing preventive measures and coping with COVID-19, especially among hospitalized children and adolescents¹⁰10 Hillesheim D, Tomasi YT, Figueiró TH, Paiva KM. Síndrome respiratória aguda grave por COVID-19 em crianças e adolescentes no Brasil: perfil dos óbitos e letalidade hospitalar até a 38ª Semana Epidemiológica de 2020. Epidemiol Serv Saude 2020; 29:e2020644.. In addition, the results of such analyses can contribute to better allocation of resources for vaccination processes and COVID-19 hospital services for children and adolescents. The aim of this study was to perform a spatial analysis of the hospital mortality rate (HMR) due to SARS attributed to COVID-19 among children and adolescents per federal unit (FU) in Brazil.

Methods

This was an ecological study with spatial analysis of deaths by HMR for SARS attributed to COVID-19 among individuals 0-19 years of age. Data were obtained from hospitalization records in the Influenza Epidemiological Surveillance Information System (SIVEP-Gripe) from March 2020 (date of first case report) to December 2021 (for the first two years of the pandemic and the start of vaccination of children in the second half of 2021). The data were collected on February 27, 2023, on the portal https://opendatasus.saude.gov.br/dataset. SIVEP-Gripe is an official system of the Ministry of Health, with national coverage, for the registration of cases and deaths from SARS.

For notification purposes, individuals with a combination of the following symptoms are considered to be SARS cases and should be compulsorily notified: high fever (above 37.8 ºC) and cough or sore throat and respiratory distress or dyspnea or O₂ saturation <95% and requested hospitalization or died having presented the symptoms mentioned, regardless of hospitalization¹¹11 Brasil. Ministério da Saúde (MS). Sistema de Informação de Vigilância Epidemiológica da Gripe. Secretaria de Vigilância em Saúde. Ficha de Registro Individual - Casos de Síndrome Respiratória Aguda Grave Hospitalizados [Internet]. [acessado 2023 mar 18]. Disponível em: https://opendatasus.saude.gov.br/dataset/39a4995f-4a6e-440f-8c8f-b00c81fae0d0/resource/9f0edb83-f8c2-4b53-99c1-099425ab634c/download/ficha_srag_hospitalizado_23.03.2021.pdf.
https://opendatasus.saude.gov.br/dataset... .

The final SARS classification in SIVEP-Gripe is based on the following criteria: laboratory, clinical-epidemiological; clinical-only, and clinical-imaging. One can then classify SARS according to the etiologic agent: 1) influenza virus; 2) other respiratory virus; 3) other etiologic agent; 4) unspecified; or 5) SARS by COVID-19, and only the latter was used in this study; additionally, the option “death” of the evolution field of the Individual Record Form - hospitalized SARS cases was used. Cases that progressed to cure, deaths from other causes, and unknown progression were not considered. The analyses were carried out by place of residence, considering that there are few municipalities of reference for SARS hospitalization¹²12 Maximino FDS, Branco MRFC. Análise Espacial da Letalidade por Síndrome Respiratória Aguda Grave por COVID-19 no Maranhão, Brasil, 2020-2022. Saude Colet (Barueri) 2023; 13(85):12674-12687..

The outcome of interest was HMR by FU among individuals aged 0-19 years according to the World Health Organization classification¹³13 Organização Mundial da Saúde (OMS). Saúde reprodutiva do adolescente: uma estratégia para ação. Genebra: OMS/FNUAP/UNICEF; 1989., subdivided into 0-28 days, 29-11 months, 1-2 years, 3-5 years, 6-9 years, 10-14 years and 15-19 years. All registered cases with ages from 0 days to 19 years were considered. From these patients, 162 cases with ages recorded with negative numbers and with inconsistencies between the information on birth dates and recorded ages were excluded.

Deaths attributed to COVID-19 caused by SARS were aggregated by the FU. The HMR was calculated from the ratio of the number of deaths to the number of cases multiplied by 100. Subsequently, the rates were smoothed using Local empirical Bayes estimates to reduce random variations HMR. Smoothed local rates are more stable because they consider both the population of the FU and that of neighboring states¹⁴14 Druck S, Carvalho MS, Câmara G, Monteiro AVM. Análise espacial de dados geográficos [Internet]. Brasília: EMBRAPA; 2004 [acessado 2023 fev 28]. Disponível em: http://www.dpi.inpe.br/gilberto/livro/analise/..

Cluster analysis was used to group the FUs using HMR. This analysis aimed to identify patterns of similarity among FUs, considering the variables used in this study. This type of analysis classifies all elements into groups that are similar to each other, seeking to homogenize each group and heterogenize all groups, that is, the objects in each group are similar to each other but different from objects in other groups¹⁵15 Linden R. Técnicas de agrupamentos. Rev Sis Infor FSMA 2009; 4:18-31..

Hierarchical and k-means clustering methods were used. The hierarchical method is based on the definition of a hierarchy that seeks to aggregate similar elements (FUs) in the same group using a similarity criterion, forming a graphical reproduction (dendrogram)¹⁵15 Linden R. Técnicas de agrupamentos. Rev Sis Infor FSMA 2009; 4:18-31.. Three linkage methods were tested using the hierarchical technique: complete linkage, average linkage, and Ward linkage.

K-means is a non-hierarchical method that partitions elements to form clusters with less internal heterogeneity¹⁵15 Linden R. Técnicas de agrupamentos. Rev Sis Infor FSMA 2009; 4:18-31.. Clusters were selected using the highest value of the ratio of the total sum of squares. Statistical analyses were performed using the Stata® 16.0, QGIS 3.6.0, and Geoda 1.14.

The study was approved by the Research Ethics Committee (CEP) of the University Hospital of the Federal University of Maranhão (HUUFMA) and by the National Research Ethics Committee (CONEP) under Ruling number: 4.098.427 and CAAE 32206620.0.0000.5086, dated June 19, 2020, according to the requirements demanded by Resolution No. 466/2012 of the National Health Council.

Results

Between March 2020 and December 2021, 56,468 cases and 3,958 deaths due to COVID-19 were recorded in Brazil among individuals 0-19 years of age. The description of the number of cases and deaths, HMR per FU, by age group, and year of occurrence are presented in Table 1.

The K-means clustering method identified five HMR clusters in 2020/2021 (Table 2). In 2020, the clusters with high HMRs comprised mainly the UFs in the North/Northeast (N/NE) regions (Figure 1). The age groups clustered with the highest HMRs were 0 to 28 days, 29 days to under 1 year, and 1 year to 2 years (Table 2). The age group from 0 to 28 days showed the highest number of FHUs grouped in the High HMR Cluster (Table 2), they are: Amazonas, Pará, Roraima and Acre in the North and Maranhão, Piauí and Pernambuco in the Northeast of the country (Figure 1). Roraima was evidenced in the Clusters with high HMR in the age groups highlighted in 2020 and the UF Santa Catarina composing the cluster with the highest HMR in the age group of 3 to 5 years (Figure 1).

In 2021, the clusters with the highest rates remained especially in the Northeast region. The age groups clustered with the highest HMRs were 0 to 28 days, 29 days to under 1 year, and 3 to 5 years (Table 2). There was an increase in the HMRs in 2021 for all age groups, except for the age groups 1 to 2 years and 10 to 14 years, in the country (Table 2). However, fewer FHUs were found in the cluster with high HMR in the 0 to 28-day age group (Table 2), composed of the following FHUs: Ceará, Paraíba, and Pernambuco in the Northeast of the country (Figure 1).

Discussion

The analysis of the first two years of the pandemic in Brazil shows that children from 29 days to 1 year of age are the most vulnerable and account for almost half of the deaths among children under 5 years of age¹⁶16 Levy B. COVID-19 mata dois menores de 5 anos por dia no Brasil [Internet]. Agência Fiocruz de Noticías; 2022 [acessado 2023 mar 18]. Disponível em: https://portal.fiocruz.br/noticia/covid-19-mata-dois-menores-de-5-anos-por-dia-no-brasil.
https://portal.fiocruz.br/noticia/covid-... . Pereira et al.¹⁷17 Pereira AR, Branco MRFC, Costa SSB, Lopes DAM, Pinheiro VV, Oliveira DC, Pasklan ANP, Gomes JA, Santos AM, Gama MEA. COVID-19 severe acute respiratory syndrome in Brazilian newborns in 2020-2021. Rev Bras Epidemiol 2023; 26:e230012., when describing cases of SARS by COVID-19 in newborns in the country, showed the severity of COVID-19 from the proportion of ICU admissions and deaths. These data reinforce the importance of analyses in this age group, despite the possible occurrences of under-recording of deaths due to difficulties in confirming the diagnosis of SARS-COVID-19, especially in poorer regions and with care gaps.

Based on the results of the cluster analysis, the highest HMR occurred in FUs in the N/NE regions in both years, particularly among individuals who were 0-28-days and 29 days to less than 1 year. These findings corroborate the severity of the disease in the under-1 age group. Research in China¹⁸18 Dong Y, Mo XI, Hu Y, Qi X, Jiang F, Jiang Z, Tong S. Epidemiological characteristics of 2143 pediatric patients with 2019 Coronavirus Disease in China. J Emerg Med 2020; 58(4):712-713. and Italy¹⁹19 Garazzino S, Lo Vecchio A, Pierantoni L, Calò Carducci FI, Marchetti F, Meini A, Castagnola E, Vergine G, Donà D, Bosis S, Dodi I, Venturini E, Felici E, Giacchero R, Denina M, Pierri L, Nicolini G, Montagnani C, Krzysztofiak A, Bianchini S, Marabotto C, Tovo PA, Pruccoli G, Lanari M, Villani A, Castelli Gattinara G; Italian SITIP-SIP Pediatric Infection Study Group. Epidemiology, Clinical Features and Prognostic Factors of Pediatric SARS-CoV-2 Infection: Results From an Italian Multicenter Study. Front Pediatr 2021; 9:649358. observed greater vulnerability to the severe type of infection in children younger than 1 year and requiring more hospitalization and admission to intensive care compared to older children¹⁹19 Garazzino S, Lo Vecchio A, Pierantoni L, Calò Carducci FI, Marchetti F, Meini A, Castagnola E, Vergine G, Donà D, Bosis S, Dodi I, Venturini E, Felici E, Giacchero R, Denina M, Pierri L, Nicolini G, Montagnani C, Krzysztofiak A, Bianchini S, Marabotto C, Tovo PA, Pruccoli G, Lanari M, Villani A, Castelli Gattinara G; Italian SITIP-SIP Pediatric Infection Study Group. Epidemiology, Clinical Features and Prognostic Factors of Pediatric SARS-CoV-2 Infection: Results From an Italian Multicenter Study. Front Pediatr 2021; 9:649358..

COVID-19 in children and adolescents presents unevenly among countries²⁰20 Kitano T, Kitano M, Krueger C, Jamal H, Al Rawahi H, Lee-Krueger R, Sun RD, Isabel S, García-Ascaso MT, Hibino H, Camara B, Isabel M, Cho L, Groves HE, Piché-Renaud PP, Kossov M, Kou I, Jon I, Blanchard AC, Matsuda N, Mahood Q, Wadhwa A, Bitnun A, Morris SK. The differential impact of pediatric COVID-19 between high-income countries and low- and middle-income countries: A systematic review of fatality and ICU admission in children worldwide. PLoS ONE 2021; 16(1):e0246326.. Study on the impact of COVID-19 in children with data from different countries showed that most pediatric fatalities were reported in low- and middle-income countries. In these countries, adverse circumstances as precarious sanitation conditions, food insecurity, lower application of resources in health have contributed to disproportionate risk of deaths as well as social impacts²¹21 Zar HJ, Dawa J, Fischer GB, Castro-Rodriguez JA. Challenges of COVID-19 in children in low- and middle-income countries. Paediatr Respir Rev 2020; 35:70-74..

Horton²²22 Horton R. Offline: COVID-19 Is Not a Pandemic. Lancet 2020; 396(10255):874. suggested applying the term “syndemic” to COVID-19 because of its clustering and interactions with pre-existing conditions and the influence of broader political, economic, and social factors, additionally obesity can also be considered a syndemic condition, so are important for prognosis, treatment, and health policy. Marked weight gain among children aged 8-12 years²³23 Brooks CG, Spencer JR, Sprafka JM, Roehl KA, Ma J, Londhe AA, He F, Cheng A, Brown CA, Page J. Pediatric BMI Changes during COVID-19 Pandemic:An Electronic Health Record-Based Retrospective Cohort Study. Clin Med 2021; 38:101026. and 6-11 years²⁴24 Hu J, Liu J, Wang J, Shen M, Ge W, Shen H, Zhang T, Yang H, Yin J. Unfavorable Progression of Obesity in Children and Adolescents Due to COVID-19 Pandemic: A School-Based Survey in China. Obesity 2021; 29(11):1907-1915. has been pointed out in the literature, probably related to a more significant increase in sedentary behavior, electronic games and screen time, especially in younger children, in addition a significant increase in the risk of severe illness by COVID-19 and consequently hospital/ICU admission in overweight/obese youth has been observed²⁵25 Graff K, Smith C, Silveira L, Jung S, Curran-Hays S, Jarjour J, Carpenter L, Pickard K, Mattiucci M, Fresia J, McFarland EJ, Dominguez SR, Abuogi L. Risk Factors for Severe COVID-19 in Children. Pediatr Infect Dis J 2021; 40(4):137-145.. It is possible that this aspect also interfered with our results.

In the Brazilian context, the difficulty of access to health services and ICU beds is uneven among the states²⁶26 Oliveira VS, Oliveira LG, Bastos GS, Dias LA, Pinto RM, Souza CSB. Fatores Determinantes de evolução grave e crítica da COVID-19 em crianças: revisão sistemática e metanálise. Resid Pediatr 2020; 10(2):1-8.. HMR in FUs may be related to factors such as socioeconomic development level, diagnostic conditions, assistance to symptomatic patients, and prevention and control capacity through nonpharmacological measures²⁷27 Freitas CM, Barcellos C, Villela DAM, Matta GC, Reis LGC, Portela MC, Saldanha RF, Silva IVM. Balanço dos Cenários Epidemiológicos da Pandemia de COVID-19 em 2020. In: Freitas CM, Barcellos C, Villela DAM, editores. COVID-19 no Brasil: cenários epidemiológicos e vigilância em saúde. Rio de Janeiro: Fiocruz; 2021. p. 57-74..

There was a disparity in the availability of human and hospital resources between the S/SE and N/NE regions, revealing an unequal capacity to cope with the crisis, which probably impacted the COVID-19 mortality rates²⁸28 Castro CS, Holzgrefe Júnior JV, Reis RB, Andrade BB, Quintanilha LF. COVID-19 pandemic: scenario of the Brazilian health system for coping with the crisis. Res Soc Dev 2020; 9:e516974383.. In 2020, in Brazil, 31% of children/adolescents with SARS who died were not admitted to the ICU, probably due to the absence of these facilities, reinforcing regional socioeconomic inequalities²⁹29 Oliveira EA, Colosimo EA, Silva ACS, Mak RH, Martelli DB, Silva LR, Martelli-Júnior H, Oliveira MCL. Clinical characteristics and risk factors for death among hospitalised children and adolescents with COVID-19 in Brazil: an analysis of a nationwide database. Lancet Child Adolesc Health 2021; 5(8):559-568..

Some states in the Northeast stand out from other FUs in the same region when composing high HMR clusters. The heterogeneity among the Northeastern states indicates the need for resources and a focus on the precariousness of timely diagnoses³⁰30 Marinelli NP, Albuquerque LPA, Sousa IDB, Batista FMA, Mascarenhas MDM, Rodrigues MTP. Evolução de indicadores e capacidade de atendimento no início da epidemia de COVID-19 no Nordeste do Brasil, 2020. Epidemiol Serv Saude 2020; 29:e2020226., which enables the isolation of patients and surveillance of their contacts to reduce transmission.

The North region has high poverty indicators, a low human development index, and insufficient resources for public health, resulting in difficulties facing the pandemic³¹31 Valenzuela EV, Morais TC, Daboin BG, Cavalcanti MPE, Portugal IBM, Souza IS, Ribeiro MAL, Monteiro CBM, Abreu LC. Evolution of mortality and lethality due to COVID-19 in the State of Roraima, Brazil, from March 2020 to July 2021. J Hum Growth Dev 2021; 31(3):447-457.. Roraima stood out in the clusters with the largest HMR. The weaknesses in the health system and the presence of illegal mining near villages may have contributed to the spread of this disease in Roraima³²32 Oliveira U, Soares Filho B, Oviedo A, Santos TM, Carlos S, João Ricardo Rampinelli Alves JR, Piaz A. Modelagem da vulnerabilidade dos povos indígenas no Brasil ao COVID-19 [Internet]. [acessado 2022 abr 8]. Disponível em: https://ds.saudeindigena.icict.fiocruz.br/handle/bvs/3687.
https://ds.saudeindigena.icict.fiocruz.b... . Another important aspect in Roraima is the vulnerability, in the midst of the pandemic, of indigenous immigrants originating from groups in Venezuela, with no command of the language and limited access to the health network, and also the situation of unaccompanied Venezuelan children and adolescents³³33 Bomfim LBC, Porto F, Silva CSM, Silva CJM, Silva AS. Prevalence of death by COVID-19 in ICU in the age group from 0 to 19 years of Roraima state. RSD 2022; 11(11):e584111133554., may have converged to a difficult control of COVID-19 in this state.

To address the pandemic, it is necessary to consider social vulnerabilities related to sanitary, structural, and organizational conditions and the quality of health services in each territory³⁴34 Natividade MS, Bernardes K, M Pereira, Miranda SS, Bertoldo J, Teixeira MG, Livramento HL, Aragão E. Distanciamento social e condições de vida na pandemia COVID-19 em Salvador-Bahia, Brasil. Cien Saude Colet 2020; 25(9):3385-3392.. High mortality rates may lead to serious failures in the health care and surveillance system in a state²⁷27 Freitas CM, Barcellos C, Villela DAM, Matta GC, Reis LGC, Portela MC, Saldanha RF, Silva IVM. Balanço dos Cenários Epidemiológicos da Pandemia de COVID-19 em 2020. In: Freitas CM, Barcellos C, Villela DAM, editores. COVID-19 no Brasil: cenários epidemiológicos e vigilância em saúde. Rio de Janeiro: Fiocruz; 2021. p. 57-74.. The mortality rate may be influenced by the lack of diagnosis of the disease, including among patients hospitalized with SARS, owing to difficulties in testing and performing imaging tests. The high number of deaths without a confirmed cause compromises the quality of the records³⁵35 Souza DF, Paiva JPS, Leal TC, Silva LFD, Santos LG. Spatiotemporal evolution of case fatality rates of COVID-19 in Brazil, 2020. J Bras Pneumol 2020; 46(4):e20200208..

Among the limitations of this study is the use of secondary data with possible inconsistencies, possibility of under/recording, especially in localities where deaths without hospital care may occur and level of aggregation used (FU), which does not allow for more detailed analyses. The strengths of the study include the amount of data analyzed, national coverage, and spatial analysis of HMR among individuals 0-19 years of age and with subdivisions of the age groups and most recent period that have not been analyzed in similar studies so far³⁶36 Faria RM, Jantsch LB, Neves ET, Hausen CF, Zubiaurre AP, Sehnem BGD, Miranda MJ. Social and territorial inequalities in the mortality of children and adolescents due to COVID-19 in Brazil. Rev Bras Enferm 2022; 75(6):e20210482.^,3737 Santos VS, Siqueira TS, Atienzar AC, Santos MARR, Vieira SCF, Lopes ASA. Spatial clusters, social determinants of health and risk of COVID-19 mortality in Brazilian children and adolescents: A nationwide population-based ecological study. Lancet Reg Health Am 2022; 3:e100311..

Regional differences were observed in the HMR. States were grouped with others from different regions, showing the importance of the spatial issue by revealing the heterogeneity in the behavior of rates within each region and among regions. These findings may reflect social and access inequalities among the Brazilian population regarding hospital care and structural weaknesses in the health surveillance system. It is essential to acknowledge the vulnerabilities of each region, particularly the N/NE region.

The findings show a worsening of the mortality rate picture for COVID-19 in the study age group from 2020 to 2021, which follows the general increase in deaths in Brazil, probably due to issues related to the relaxation of preventive measures to SARS-CoV-2³⁸38 Cavatão F, Rodrigues G, Souza A. Infecção por adenovírus (ADE), influenza a (FLUA), influenza B (FLUB), parainfluenza 1, 2 e 3 e vírus respiratório sincicial (VRS) em crianças &lt;5 anos hospitalizadas: antes e durante a pandemia de COVID-19. Braz J Infect Dis 2022; 26(1):102273., presence of variants with high transmissibility³⁹39 Michelon CM. Principais variantes do SARS-CoV-2 notificadas no Brasil. RBAC 2021; 53(2):109-116., vaccine hesitancy⁴⁰40 Vignoli RG, Silva RC, Maran MFIA, Vitoriano MCCP. Movimento antivacina e hesitação vacinal na covid-19: reflexões e percepções para a ciência da informação. Inf Inf 2022; 27(1):457-484. and in particular for children, the late introduction of vaccines⁴¹41 Brasil. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Departamento de Imunização e Doenças Transmissíveis. Nota técnica nº 213/2022-CGPNI/DEIDT/SVS/MS. Aprovação pela Anvisa da Vacina CoronaVac (covid-19) para crianças de 3 a 5 anos de idade e orientações do Programa Nacional de Imunizações para vacinação deste público infantil [Internet]. Brasília: MS; 2022 [acessado 2023 fev 28]. Disponível em: https://www.gov.br/saude/pt-br/assuntos/coronavirus/notas-tecnicas/2022/nota-tecnica-213-2022-cgpni-deidt-svs-ms..

The number of notifications of cases and deaths by COVID-19 in children is lower when compared to adults, probably due to previous immunity from contacts with similar and common viruses in early childhood generating a faster and more efficient immune response, and immunity acquired from recent vaccinations, since the childhood vaccination calendar is broad⁴²42 Oliveira IG. Quais são os possíveis fatores protetores que protegem as crianças de manifestar quadros severos da Síndrome Respiratória Aguda do Coronavírus 2 - uma revisão literária. Braz J Health Rev 2022; 5(1):2498-2505.. In addition, they present fewer risk factors for severe cases, such as the presence of comorbidities and age itself, thus being protective factors for children⁴²42 Oliveira IG. Quais são os possíveis fatores protetores que protegem as crianças de manifestar quadros severos da Síndrome Respiratória Aguda do Coronavírus 2 - uma revisão literária. Braz J Health Rev 2022; 5(1):2498-2505.. On the other hand, the pandemic brought negative impacts on the vaccination schedule for children in 2020, because there was a reduction in vaccination coverage throughout the Brazilian territory⁴³43 Procianoy GS, Rossini Junior F, Lied AF, Jung LFPP, Souza MCSCD. Impacto da pandemia do COVID-19 na vacinação de crianças de até um ano de idade: um estudo ecológico. Cien Saude Colet 2022; 27(3):969-978. especially in the North and Northeast regions, and may be one of the reasons for morbidity and mortality of this population⁴⁴44 Donalisio MR, Boing AC, Sato APS, Martinez EZ, Xavier MO, Almeida RLF, Moreira RDS, Queiroz RCS, Matijasevich A. Vacinação contra poliomielite no Brasil de 2011 a 2021: sucessos, reveses e desafios futuros. Cien Saude Colet 2023; 28(2):337..

According to Müller et al.⁴⁵45 Müller GC, Ferreira LS, Campos MFE, Borges ME, Almeida BG, Poloni S. Modeling the impact of child vaccination (5-11 y) on overall COVID-19 related hospitalizations and mortality in a context of omicron variant predominance and different vaccination coverage paces in Brazil. Lancet Reg Health Am 2023; 17:100396., vaccination at the maximum rate could have prevented, between January and April 2022, about 5,400 hospitalizations and 410 deaths in children aged 5 to 11 years. On the other hand, a national survey of 15,297 respondents found that the vaccination hesitancy rate against COVID-19 of caregivers of children aged 0 to 4 years, 5 to 11 years, and adolescents was 16%, 13%, 15%, respectively, an aspect considered adverse to increasing vaccination coverage⁴⁶46 Nehab FM, Camacho GK, Reis TA, Junqueira-Marinho MF, Abramov MD, Azevedo AZM, Salú MS, Vasconcelos ZFM, Gomes Junior SCS, Silva Filho OC, Salvador PTCO, Alves KYA, Carvalho KRS, Moore DCBC. Willingness of Brazilian caregivers in having their children and adolescents vaccinated against COVID-19. Vaccine 2023; 41(3):735-743..

Children/adolescents represent a relevant age group in the transmission dynamics, but they also present factors of disease aggravation, especially among younger age groups. Immunization against COVID-19 in children older than 5 years was started in Brazil in January 2022. In Brazil, a study with different age groups, when comparing COVID-19 mortality, identified higher mortality rates in 2022 in the age groups 0 to 11 years compared to the previous year and lower rates in the 12-to-17-year age groups⁴⁷47 Orellana JDY, Marrero L, Horta BL. Mortalidade por COVID-19 no Brasil em distintos grupos etários: diferenciais entre taxas extremas de 2021 e 2022. Cad Saude Publica 2022; 38(7):e00041922.. They found opposite patterns in mortality among children and individuals included in the national vaccination campaign, which likely contributed to the reduction in mortality in adolescents older than 11 years that started the vaccine in July 2021 and progressed in the following months⁴⁷47 Orellana JDY, Marrero L, Horta BL. Mortalidade por COVID-19 no Brasil em distintos grupos etários: diferenciais entre taxas extremas de 2021 e 2022. Cad Saude Publica 2022; 38(7):e00041922.. The importance of vaccination especially in children under 5 years of age is reinforced to reduce severe forms and deaths from COVID-19 in this age group.

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