Characteristics and clinical outcomes of adolescents infected by SARS-CoV-2: a systematic review

Campos, Cezenário Gonçalves; Muniz, Luciene Aparecida; Belo, Vinícius Silva; Costa, Cássia Cristina; Borges Neto, Juscelino de Souza; Novais, Rommel Larcher Rachid; Rabelo, Fernanda Lívia Dutra; Martins Júnior, Charles Henrique; Romano, Márcia Christina Caetano; Lamounier, Joel Alves

doi:10.1590/1984-0462/2024/42/2022241

Cezenário Gonçalves Campos ^**Corresponding author: E-mail: cezenario@yahoo.com.br (C. G. Campos)

Study design

Manuscript writing

Data collection

Data analysis

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0001-5650-0096

Luciene Aparecida Muniz

Study design

Manuscript writing

Data collection

Data analysis

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0003-2185-1595

Vinícius Silva Belo

Manuscript revision

Study supervision

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0003-0183-1175

Cássia Cristina Costa

Data collection

Data analysis

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0002-1924-8116

Juscelino de Souza Borges Neto

Data collection

Data analysis

Instituto Federal de Educação, Ciência e Tecnologia do Ceará, Limoeiro do Norte, CE, Brazil.

https://orcid.org/0000-0002-4551-3278

Rommel Larcher Rachid Novais

Data collection

Data analysis

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0002-6433-5454

Fernanda Lívia Dutra Rabelo

Data collection

Data analysis

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0002-9946-6710

Charles Henrique Martins Júnior

Data collection

Data analysis

Centro Federal de Educação Tecnológica de Minas Gerais, Divinópolis, MG, Brazil.

https://orcid.org/0000-0003-4693-6704

Márcia Christina Caetano Romano

Manuscript revision

Study supervision

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0002-1819-4689

Joel Alves Lamounier

Manuscript revision

Study supervision

Universidade Federal de São João del-Rei, Divinópolis, MG, Brazil.

https://orcid.org/0000-0002-8386-4140

*Corresponding author: E-mail: cezenario@yahoo.com.br (C. G. Campos)

Conflict of interests

The authors declare there is no conflict of interests.

Reference	Country	Study design	Description of the sample Number of participants (n)/age group (years old)	Methodological quality¹⁴14 Downs S, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52:377-84. https://doi.org/10.1136/jech.52.6.377 https://doi.org/10.1136/jech.52.6.377... and level of evidence¹²12 Diniz IA, Santos KF, Baldoni NR, Braga EJ, Bueno CA, Barcelos AC, et al. Duração do aleitamento materno exclusivo associado a anemia por deficiência de ferro em crianças: uma revisão sistemática. REAS. 2022;15:e9610. https://doi.org/10.25248/REAS.e9610.2022 https://doi.org/10.25248/REAS.e9610.2022...
Oliveira et al.²⁷27 Oliveira EA, Simões AC, Oliveira MC, Colosimo EA, Mak RH, Vasconcelos MA, et al. Comparison of the first and second waves of the coronavirus disease 2019 pandemic in children and adolescents in a middle-income country: clinical impact associated with severe acute respiratory syndrome coronavirus 2 gamma lineage. J Pediatr. 2022;244:178-185.e3. https://doi.org/10.1016/j.jpeds.2022.01.001 https://doi.org/10.1016/j.jpeds.2022.01....	Brazil	Cohort	n=6.725/12–19	17 points/level 3
Clemente et al.¹⁹19 Clemente D, Udaondo C, Inocencio J, Nieto JC, Del Río PG, Fernández AG, et al. Clinical characteristics and COVID-19 outcomes in a regional cohort of pediatric patients with rheumatic diseases. Pediatr Rheumatol Online J. 2021;19:162. https://doi.org/10.1186/s12969-021-00648-5 https://doi.org/10.1186/s12969-021-00648...	Spain	Cohort	n=77/less than 18	16 points/level 3
Drouin et al.²⁰20 Drouin O, Hepburn CM, Farrar DS, Baerg K, Chan K, Cyr C, et al. Characteristics of children admitted to hospital with acute SARS-CoV-2 infection in Canada in 2020. CMAJ. 2021;193:e1483-93. https://doi.org/10.1503/cmaj.210053 https://doi.org/10.1503/cmaj.210053...	Canada	Cohort	n=36/13–17	18 points/level 3
Gomes et al.²¹21 Gomes NT, Haslett MI, Alves AJ, Percio J, Duarte MM, Malta JM, et al. Retrospective cohort of children and adolescents hospitalized by COVID-19 in Brazil from the beginning of the pandemic to August 1st, 2020. Rev Bras Epidemiol. 2021;24:e210026. https://doi.org/10.1590/1980-549720200026 https://doi.org/10.1590/1980-54972020002...	Brazil	Cohort	n=1320/12–18	16 points/level 3
Pinto Júnior et al.²²22 Pinto Júnior VC, Moura LF, Cavalcante RC, Lima JR, Bezerra AS, Dantas DR, et al. Prevalence of COVID-19 in children, adolescents and adults in remote education situations in the city of Fortaleza, Brazil. Int J Infect Dis. 2021;108:20-6. https://doi.org/10.1016/j.ijid.2021.04.086 https://doi.org/10.1016/j.ijid.2021.04.0...	Brazil	Cross-sectional	n=854/10–19	17 points/level 4
Graff et al.²³23 Graff K, Smith C, Silveira L, Jung S, Curran-Hays S, Jarjour J, et al. Risk factors for severe COVID-19 in children. Pediatr Infect Dis J. 2021;40:e137-45. https://doi.org/10.1097/INF.0000000000003043 https://doi.org/10.1097/INF.000000000000...	USA	Cohort	n=220/11–19	17 points/level 3
Macias-Parra et al.²⁴24 Macias-Parra M, Fortes-Gutierrez S, Aguilar-Gomez N, Diaz-Garcia L, Otero-Mendoza F, Arias de la Garza E, et al. Clinical and epidemiological characteristics of paediatric patients diagnosed with COVID-19 in a tertiary hospital in Mexico City. J Trop Pediatr. 2021;67:fmab025. https://doi.org/10.1093/tropej/fmab025 https://doi.org/10.1093/tropej/fmab025...	Mexico	Cross-sectional	n=34/12–18	16 points/level 4
Oliveira et al.²⁵25 Oliveira EA, Colosimo EA, Silva AC, Mak RH, Martelli DB, Silva LR, et al. 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;5:559-68. https://doi.org/10.1016/S2352-4642(21)00134-6 https://doi.org/10.1016/S2352-4642(21)00...	Brazil	Cohort	n=3589/12–19	21 points/level 3
Parcha et al.²⁶26 Parcha V, Booker KS, Kalra R, Kuranz S, Berra L, Arora G, et al. A retrospective cohort study of 12,306 pediatric COVID-19 patients in the United States. Sci Rep. 2021;11:10231. https://doi.org/10.1038/s41598-021-89553-1 https://doi.org/10.1038/s41598-021-89553...	USA	Cohort	n=5573/12–17	18 points/level 3
Prata-Barbosa et al.¹⁵15 Prata-Barbosa A, Lima-Setta F, Santos GR, Lanziotti VS, Castro RE, Souza DC, et al. Pediatric patients with COVID-19 admitted to intensive care units in Brazil: a prospective multicenter study. J Pediatr (Rio J). 2020;96:582-92. https://doi.org/10.1016/j.jped.2020.07.002 https://doi.org/10.1016/j.jped.2020.07.0...	Brazil	Cohort	n=14/12–17	16 points/level 3
DeBiasi et al.¹⁶16 DeBiasi RL, Song X, Delaney M, Bell M, Smith K, Pershad J, et al. Severe coronavirus disease-2019 in children and young adults in the Washington, DC, Metropolitan Region. J Pediatr. 2020;223:199-203.e1. https://doi.org/10.1016/j.jpeds.2020.05.007 https://doi.org/10.1016/j.jpeds.2020.05....	USA	Cohort	n=73/10–19	16 points/level 3

Variables		Frequencies or grouped frequencies
Associated comorbidities (%)
	Neurological diseases	20
	Respiratory diseases	18
	Heart diseases	15
	Metabolic diseases	15
	Immunosuppression and malignancy diseases	15
	Kidney diseases	5
	Rheumatic and musculoskeletal and hematologic diseases	5
	Genetic syndromes	3
	Gastrointestinal diseases	3
	Dermatological diseases	1
Clinical characteristics (%)
	Fever	11–81
	Cough	16–68
	Nasal congestion/Runny nose	18–63
	SpO₂^* * SpO2: peripheral oxygen saturation; <95%	29–53
	Respiratory distress	30–52
	Tachypnea	10–50
	Anosmia	9–48
	Dyspnea	5–46
	Sore throat	9–44
	Gastrointestinal symptoms	4–42
	Headache	6–35
	Myalgia	7–14
	Ageusia	5–11
Diagnostic test (%)
	Laboratory method for virus detection by RT-PCR^† † RT-PCR: reverse transcription-polymerase chain reaction.	65
	Viral immune response tests, antibody tests (serological tests)	15
	Rapid tests for detection of viral antigens	10
	Clinical-epidemiological method	10

Reference	Outcomes
Oliveira et al.²⁷27 Oliveira EA, Simões AC, Oliveira MC, Colosimo EA, Mak RH, Vasconcelos MA, et al. Comparison of the first and second waves of the coronavirus disease 2019 pandemic in children and adolescents in a middle-income country: clinical impact associated with severe acute respiratory syndrome coronavirus 2 gamma lineage. J Pediatr. 2022;244:178-185.e3. https://doi.org/10.1016/j.jpeds.2022.01.001 https://doi.org/10.1016/j.jpeds.2022.01....	ICU admission rate (28%). Use of NIMV (38%) and IMV (22%). Lethality rate: 7.5%. Dyspnea (RR 2.1; 95%CI 1.8–2.4), SP0²2 Sharma A, Farouk IA, Lal SK. COVID-19: a review on the novel coronavirus disease evolution, transmission, detection, control and prevention. Viruses. 2021;13:202. https://doi.org/10.3390/v13020202 https://doi.org/10.3390/v13020202... <95% (RR 3.5; 95%CI 2.5–4.1), adolescents living in the North (RR 1.5; 95%CI 1.3–1.9) and Northeast (RR 2.0; 95%CI 1.7–2.4) regions, ethnic groups black, mixed-race (RR 1.3; 95%CI 1.1–1.5) and indigenous (RR 3.3; 95%CI 2.2–4.9) and the presence of comorbidity which increases the risk of death (RR 2.7; 95%CI 2.3–3.0).^* * study carried out in a hospital environment;
Afonso et al.¹⁷17 Afonso ET, Marques SM, Costa LD, Fortes PM, Peixoto F, Bichuetti-Silva DC, et al. Secondary household transmission of SARS-CoV-2 among children and adolescents: clinical and epidemiological aspects. Pediatr Pulmonol. 2022;57:162-75. https://doi.org/10.1002/ppul.25711 https://doi.org/10.1002/ppul.25711...	Prevalence of SARS-CoV-2: 25% (95%CI 20.3–30.6). 55% were symptomatic. 17.7% had at least one type of comorbidity. Higher proportion of females (53.3%) and self-declared black or mixed-race (48%).^† † study carried out in a non-hospital environment;
Alharbi et al.¹⁸18 Alharbi M, Kazzaz YM, Hameed T, Alqanatish J, Alkhalaf H, Alsadoon A, et al. SARS-CoV-2 infection in children, clinical characteristics, diagnostic findings and therapeutic interventions at a tertiary care center in Riyadh, Saudi Arabia. J Infect Public Health. 2021;14:446-53. https://doi.org/10.1016/j.jiph.2020.12.034 https://doi.org/10.1016/j.jiph.2020.12.0...	Two participants were admitted to the ICU. One female, 12 years old, without comorbidities, no need of MV, hospitalized for 43 days, 14 in the ICU, and was discharged. The second adolescent developed P-MIS, he was male, 12 years old, neuropath, used MV, and died.^* * study carried out in a hospital environment;
Clemente et al.¹⁹19 Clemente D, Udaondo C, Inocencio J, Nieto JC, Del Río PG, Fernández AG, et al. Clinical characteristics and COVID-19 outcomes in a regional cohort of pediatric patients with rheumatic diseases. Pediatr Rheumatol Online J. 2021;19:162. https://doi.org/10.1186/s12969-021-00648-5 https://doi.org/10.1186/s12969-021-00648...	The median hospitalization time was five days (IQR: 2–20). One patient required ICU. There are no death records. Previous use of glucocorticoids is associated with a greater chance of hospitalization (OR 3.5; p=0.001). The comorbidities were not analyzed.^* * study carried out in a hospital environment;
Drouin et al.²⁰20 Drouin O, Hepburn CM, Farrar DS, Baerg K, Chan K, Cyr C, et al. Characteristics of children admitted to hospital with acute SARS-CoV-2 infection in Canada in 2020. CMAJ. 2021;193:e1483-93. https://doi.org/10.1503/cmaj.210053 https://doi.org/10.1503/cmaj.210053...	47% required hospitalization. Comorbidity is associated with severity (p=0.001). Hospitalizations were more frequent in patients with asthma (p=0.003) or metabolic disease (p=0.004). The severe form of the disease was frequent in patients with encephalopathy (p=0.005).^‡ ‡ study carried out in a hospital and non-hospital environment.
Gomes et al.²¹21 Gomes NT, Haslett MI, Alves AJ, Percio J, Duarte MM, Malta JM, et al. Retrospective cohort of children and adolescents hospitalized by COVID-19 in Brazil from the beginning of the pandemic to August 1st, 2020. Rev Bras Epidemiol. 2021;24:e210026. https://doi.org/10.1590/1980-549720200026 https://doi.org/10.1590/1980-54972020002...	Lethality rate: 13.6%. Risk of death: being an adolescent (RR: 1.6; 95%CI 1.1–2.3), SARS-critical (RR 4.6; 95%CI 2.8–7.5), immunosuppressed (RR 2.2; 95%CI 1.6–3.2).^* * study carried out in a hospital environment;
Pinto Júnior et al.²²22 Pinto Júnior VC, Moura LF, Cavalcante RC, Lima JR, Bezerra AS, Dantas DR, et al. Prevalence of COVID-19 in children, adolescents and adults in remote education situations in the city of Fortaleza, Brazil. Int J Infect Dis. 2021;108:20-6. https://doi.org/10.1016/j.ijid.2021.04.086 https://doi.org/10.1016/j.ijid.2021.04.0...	29.3% of prevalence. 32% of cases presented comorbidities. 24% were symptomatic at the time of examination.^† † study carried out in a non-hospital environment;
Graff et al.²³23 Graff K, Smith C, Silveira L, Jung S, Curran-Hays S, Jarjour J, et al. Risk factors for severe COVID-19 in children. Pediatr Infect Dis J. 2021;40:e137-45. https://doi.org/10.1097/INF.0000000000003043 https://doi.org/10.1097/INF.000000000000...	45% presented comorbidities. The presence of comorbidities increases the chance of hospitalization (OR 2.7; p=0.003). The chances increase with each additional comorbidity (OR 1.4; p<0.001). Dyspnea (OR 6.3; 95%CI 2.8–14.3) is associated with chance of hospitalization and increases the chance of using MV (OR 15.7; 95%CI 6.4–38.5).^* * study carried out in a hospital environment;
Macias-Parra et al.²⁴24 Macias-Parra M, Fortes-Gutierrez S, Aguilar-Gomez N, Diaz-Garcia L, Otero-Mendoza F, Arias de la Garza E, et al. Clinical and epidemiological characteristics of paediatric patients diagnosed with COVID-19 in a tertiary hospital in Mexico City. J Trop Pediatr. 2021;67:fmab025. https://doi.org/10.1093/tropej/fmab025 https://doi.org/10.1093/tropej/fmab025...	23% required ICU admission. 17% required MV. 77% presented comorbidities (33% with chronic diseases and 44% with immunosuppressive and/or oncological diseases).^* * study carried out in a hospital environment;
Oliveira et al.²⁵25 Oliveira EA, Colosimo EA, Silva AC, Mak RH, Martelli DB, Silva LR, et al. 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;5:559-68. https://doi.org/10.1016/S2352-4642(21)00134-6 https://doi.org/10.1016/S2352-4642(21)00...	The mean time from onset of symptoms to hospitalization was three days (IQR 1–6). 24% were admitted to the ICU. 10% required IMV. 7.5% died. Residents of the Northeast (RR 2.1; 95%CI 1.7–2.5), and North (RR 1.5; 95%CI 1.2–2.0), regions and indigenous ethnicity (RR 3.4; 95%CI 2.2–5.2), are at a higher risk of death.^* * study carried out in a hospital environment;
Parcha et al.²⁶26 Parcha V, Booker KS, Kalra R, Kuranz S, Berra L, Arora G, et al. A retrospective cohort study of 12,306 pediatric COVID-19 patients in the United States. Sci Rep. 2021;11:10231. https://doi.org/10.1038/s41598-021-89553-1 https://doi.org/10.1038/s41598-021-89553...	5.5% were hospitalized. 1% required ICU. 0.3% MV. The hospitalization risk was higher in black (RR 2.0; 95%CI 1.5–2.6) and in Hispanics (RR 1.3; 95%CI 1.0–1.8).^‡ ‡ study carried out in a hospital and non-hospital environment.
Prata-Barbosa et al.¹⁵15 Prata-Barbosa A, Lima-Setta F, Santos GR, Lanziotti VS, Castro RE, Souza DC, et al. Pediatric patients with COVID-19 admitted to intensive care units in Brazil: a prospective multicenter study. J Pediatr (Rio J). 2020;96:582-92. https://doi.org/10.1016/j.jped.2020.07.002 https://doi.org/10.1016/j.jped.2020.07.0...	All admitted to the ICU. One case developed P-MIS. One death of a female adolescent, 14 years old, with chronic liver disease. Presence of comorbidities is associated with disease severity and need for IMV (OR 5.5; 95%CI 1.4–21.1).^* * study carried out in a hospital environment;
DeBiasi et al.¹⁶16 DeBiasi RL, Song X, Delaney M, Bell M, Smith K, Pershad J, et al. Severe coronavirus disease-2019 in children and young adults in the Washington, DC, Metropolitan Region. J Pediatr. 2020;223:199-203.e1. https://doi.org/10.1016/j.jpeds.2020.05.007 https://doi.org/10.1016/j.jpeds.2020.05....	22% were hospitalized. 55% of those hospitalized presented no comorbidities. 25% of those hospitalized required ICU. There were no death records.^‡ ‡ study carried out in a hospital and non-hospital environment.

Reference	Country	Study design	Description of the sample Number of participants (n)/age group (years old)	Methodological quality¹⁴ and level of evidence¹²
Oliveira et al.²⁷	Brazil	Cohort	n=6.725/12-19	17 points/level 3
Clemente et al.¹⁹	Spain	Cohort	n=77/less than 18	16 points/level 3
Drouin et al.²⁰	Canada	Cohort	n=36/13-17	18 points/level 3
Gomes et al.²¹	Brazil	Cohort	n=1320/12-18	16 points/level 3
Pinto Júnior et al.²²	Brazil	Cross-sectional	n=854/10-19	17 points/level 4
Graff et al.²³	USA	Cohort	n=220/11-19	17 points/level 3
Macias-Parra et al.²⁴	Mexico	Cross-sectional	n=34/12-18	16 points/level 4
Oliveira et al.²⁵	Brazil	Cohort	n=3589/12-19	21 points/level 3
Parcha et al.²⁶	USA	Cohort	n=5573/12-17	18 points/level 3
Prata-Barbosa et al.¹⁵	Brazil	Cohort	n=14/12-17	16 points/level 3
DeBiasi et al.¹⁶	USA	Cohort	n=73/10-19	16 points/level 3

Reference	Country	Study design	Description of the sample Number of participants (n)/age group (years old)	Methodological quality¹⁴ and level of evidence¹²
Oliveira et al.²⁷	Brazil	Cohort	n=6.725/12-19	17 points/level 3
^{Afonso et al.17}	Brazil	Cross-sectional	n=49/10-19	17 points/level 4
^{Alharbi et al.18}	Saudi Arabia	Cohort	n=9/11-14	16 points/level 3
Clemente et al.¹⁹	Spain	Cohort	n=77/less than 18	16 points/level 3
Drouin et al.²⁰	Canada	Cohort	n=36/13-17	18 points/level 3
Gomes et al.²¹	Brazil	Cohort	n=1320/12-18	16 points/level 3
Pinto Júnior et al.²²	Brazil	Cross-sectional	n=854/10-19	17 points/level 4
Graff et al.²³	USA	Cohort	n=220/11-19	17 points/level 3
Macias-Parra et al.²⁴	Mexico	Cross-sectional	n=34/12-18	16 points/level 4
Oliveira et al.²⁵	Brazil	Cohort	n=3589/12-19	21 points/level 3
Parcha et al.²⁶	USA	Cohort	n=5573/12-17	18 points/level 3
Prata-Barbosa et al.¹⁵	Brazil	Cohort	n=14/12-17	16 points/level 3
DeBiasi et al.¹⁶	USA	Cohort	n=73/10-19	16 points/level 3

[1] *Corresponding author: E-mail: cezenario@yahoo.com.br (C. G. Campos)

Brasil

Brasil

Characteristics and clinical outcomes of adolescents infected by SARS-CoV-2: a systematic review

Características e desfechos clínicos de adolescentes infectados por SARS-CoV-2: uma revisão sistemática

ABSTRACT

Objective:

Data source:

Data synthesis:

Conclusions: