Spotlight for healthy adolescents and adolescents with preexisting chronic diseases during the COVID-19 pandemic

Clovis Artur Silva Lígia Bruni Queiroz Claudia de Brito Fonseca Luís Eduardo Vargas da Silva Benito Lourenço Heloisa Helena Sousa Marques About the authors

Recently, coronavirus disease (COVID-19) was declared a pandemic by the World Health Organization (WHO). The virus that causes the emerging infectious disease was designated by the International Committee on Taxonomy of Viruses as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (11. Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. N Engl J Med. 2020;382(8):727-33. https://doi.org/10.1056/NEJMoa2001017.
https://doi.org/10.1056/NEJMoa2001017...
,22. Park SE. Epidemiology, virology, and clinical features of severe acute respiratory syndrome -coronavirus-2 (SARS-CoV-2; Coronavirus Disease-19). Clin Exp Pediatr. 2020;63(4):119-24. https://doi.org/10.3345/cep.2020.00493.
https://doi.org/10.3345/cep.2020.00493...
).

COVID-19 has been reported predominantly in adult patients. The clinical, laboratorial, and radiographic abnormalities for adults with COVID-19 include fever, dry cough, myalgia, fatigue, chest discomfort, respiratory frequency >30/min, blood oxygen saturation <93%, leukopenia, lymphopenia, and chest radiographic or computed tomographic scan with mild to severe pneumonia (11. Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A Novel Coronavirus from Patients with Pneumonia in China, 2019. N Engl J Med. 2020;382(8):727-33. https://doi.org/10.1056/NEJMoa2001017.
https://doi.org/10.1056/NEJMoa2001017...

2. Park SE. Epidemiology, virology, and clinical features of severe acute respiratory syndrome -coronavirus-2 (SARS-CoV-2; Coronavirus Disease-19). Clin Exp Pediatr. 2020;63(4):119-24. https://doi.org/10.3345/cep.2020.00493.
https://doi.org/10.3345/cep.2020.00493...
-33. Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020. https://doi.org/10.1001/jama.2020.2648.
https://doi.org/10.1001/jama.2020.2648...
). The most important risk factors or comorbidities in adult COVID-19 patients include: age more than 60 years, cardiovascular disease, diabetes mellitus, arterial hypertension, chronic respiratory disease, and cancer (22. Park SE. Epidemiology, virology, and clinical features of severe acute respiratory syndrome -coronavirus-2 (SARS-CoV-2; Coronavirus Disease-19). Clin Exp Pediatr. 2020;63(4):119-24. https://doi.org/10.3345/cep.2020.00493.
https://doi.org/10.3345/cep.2020.00493...

3. Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020. https://doi.org/10.1001/jama.2020.2648.
https://doi.org/10.1001/jama.2020.2648...
-44. Chen ATC, Moniz CMV, Ribeiro-Júnior U, Diz MDPE, Salvajoli JV, Da Conceição Vasconcelos KGM, et al. How should health systems prepare for the evolving COVID-19 pandemic? Reflections from the perspective of a Tertiary Cancer Center. Clinics. 2020;75:e1864. https://doi.org/10.6061/clinics/2020/e1864.
https://doi.org/10.6061/clinics/2020/e18...
).

In contrast to adults with COVID-19, the majority of children and adolescents infected with SARS-CoV-2 exhibited milder disease and also presented with nasal congestion, rhinorrhea, pharyngeal erythema, diarrhea, and vomiting. These young patients showed an adequate treatment response and a short duration to COVID-19 resolution (55. Zheng F, Liao C, Fan QH, Chen HB, Zhao XG, Xie ZG, et al. Clinical Characteristics of Children with Coronavirus Disease 2019 in Hubei, China. Curr Med Sci. 2020. https://doi.org/10.1007/s11596-020-2172-6.
https://doi.org/10.1007/s11596-020-2172-...
,66. Lu X, Zhang L, Du H, Zhang J, Li YY, Qu J, et al. SARS-CoV-2 Infection in Children. N Engl J Med. 2020;382(17):1663-5. https://doi.org/10.1056/NEJMc2005073.
https://doi.org/10.1056/NEJMc2005073...
).

Adolescent populations have rarely been evaluated in the context of this emerging infectious disease. A recent study reported on 72,314 patients with COVID-19 from the Chinese Center for Disease Control and Prevention, 1% of whom were adolescents (10-19 years) (33. Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020. https://doi.org/10.1001/jama.2020.2648.
https://doi.org/10.1001/jama.2020.2648...
). Notably, this infectious disease occurred in 169/4,212 (4%) adolescents in the Republic of Korea study (77. Korean Society of Infectious Diseases; Korean Society of Pediatric Infectious Diseases; Korean Society of Epidemiology; Korean Society for Antimicrobial Therapy; Korean Society for Healthcare-associated Infection Control and Prevention; Korea Centers for Disease Control and Prevention. Report on the Epidemiological Features of Coronavirus Disease 2019 (COVID-19) Outbreak in the Republic of Korea from January 19 to March 2, 2020. J Korean Med Sci. 2020;35(10):e112. https://doi.org/10.3346/jkms.2020.35.e112.
https://doi.org/10.3346/jkms.2020.35.e11...
).

Another Chinese study, including 2,143 pediatric patients, showed that 35% of the patients were adolescents. Disease severity was higher in infants than in other pediatric ages. Severe and critical cases were uncommon in adolescents, with an occurrence rate of 4% and 3% in the age groups 11-15 and ≥16 years, respectively (88. Dong Y, Mo X, Hu Y, Qi X, Jiang F, Jiang Z, et al. Epidemiological Characteristics of 2143 Pediatric Patients With 2019 Coronavirus Disease in China. Pediatrics. 2020. https://doi.org/10.1542/peds.2020-0702
https://doi.org/10.1542/peds.2020-0702...
).

Moreover, silent infection is defined as positivity for SARS-CoV-2, without any clinical manifestations or chest imaging abnormalities (99. Shen K, Yang Y, Wang T, Zhao D, Jiang Y, Jin R, et al. Diagnosis, treatment, and prevention of 2019 novel coronavirus infection in children: experts' consensus statement. World J Pediatr. 2020. https://doi.org/10.1007/s12519-020-00343-7
https://doi.org/10.1007/s12519-020-00343...
). Adolescent populations frequently present with asymptomatic SARS-CoV-2 infection, and these infected populations are the main source of SARS-CoV-2 infections in the pediatric age group (99. Shen K, Yang Y, Wang T, Zhao D, Jiang Y, Jin R, et al. Diagnosis, treatment, and prevention of 2019 novel coronavirus infection in children: experts' consensus statement. World J Pediatr. 2020. https://doi.org/10.1007/s12519-020-00343-7
https://doi.org/10.1007/s12519-020-00343...
,1010. Xu R, Du M, Li L, Zhen Z, Wang H, Hu X. CT imaging of one extended family cluster of corona virus disease 2019 (COVID-19) including adolescent patients and “silent infection”. Quant Imaging Med Surg. 2020;10(3):800-4. https://doi.org/10.21037/qims.2020.02.13.
https://doi.org/10.21037/qims.2020.02.13...
).

Regarding the pathogenesis of COVID-19, one of the possible reasons for the lower prevalence of COVID-19 in children and adolescents than in adults is the lower expression of the angiotensin-converting enzyme 2 receptor (ACE-2) in the pediatric age group. This receptor is necessary for the entry of SARS-CoV-2 into the cells, particularly in the lung, heart, and intestine (1111. Brodin P. Why is COVID-19 so mild in children? Acta Paediatr. 2020. https://doi.org/10.1111/apa.15271
https://doi.org/10.1111/apa.15271...
). ACE-2 expression may increase angiotensin II production, resulting in an increase in vasoconstriction and pulmonary vascular permeability (1212. Haşlak F, Yıldız M, Adrovic A, Barut K, Kasapçopur Ö. Childhood Rheumatic Diseases and COVID-19 Pandemic: An Intriguing Linkage and a New Horizon. Balkan Med J. 2020. https://doi.org/10.4274/balkanmedj.galenos.2020.2020.4.43
https://doi.org/10.4274/balkanmedj.galen...
). A recent meta-analysis showed that comorbidities may also be changed by epigenetic regulation, with increased expression of ACE-2 in human lung cells associated with severe COVID-19 (1313. Pinto BGG, Oliveira AER, Singh Y, Jimenez L, Goncalves ANA, Ogava RLT, et al. ACE2 Expression is Increased in the Lungs of Patients with Comorbidities Associated with Severe COVID-19. Available from: https://www.medrxiv.org/content/10.1101/2020.03.21.20040261v1. https://doi.org/10.1101/2020.03.21.20040261
https://www.medrxiv.org/content/10.1101/...
).

As previously mentioned, critically ill cases have been infrequently reported in adolescents. Adolescents with severe acute respiratory failure and multi-organ dysfunction syndrome may present signs and symptoms of cytokine storm syndrome, triggered by SARS-CoV-2. Indeed, this subgroup of adolescents with COVID-19 may present with high fever; confusion; anemia; thrombocytopenia; neutropenia; coagulopathy; hyperferritinemia; and elevated liver enzyme, D-dimer, lactate dehydrogenase, and soluble CD25 levels (1414. Cron RQ, Chatham WW. The Rheumatologist's Role in Covid-19. J Rheumatol. 2020. https://doi.org/10.3899/jrheum.200334
https://doi.org/10.3899/jrheum.200334...
). An elevated cytokine profile associated with this complication mainly includes increases in interleukin (IL)-2, IL-7, granulocyte-colony stimulating factor, and tumor necrosis factor-alfa levels (1515. Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ, et al. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet. 2020;395(10229):1033-4. https://doi.org/10.1016/S0140-6736(20)30628-0.
https://doi.org/10.1016/S0140-6736(20)30...
). Notably, these findings were similar to the findings in adolescents with familial hemophagocytic lymphohistiocytosis or macrophage activation syndrome due to systemic juvenile idiopathic arthritis and in systemic lupus erythematosus patients (1616. Davi S, Minoia F, Pistorio A, Horne A, Consolaro A, Rosina S, et al. Performance of current guidelines for diagnosis of macrophage activation syndrome complicating systemic juvenile idiopathic arthritis. Arthritis Rheumatol. 2014;66(10):2871-80. https://doi.org/10.1002/art.38769.
https://doi.org/10.1002/art.38769...

17. Minoia F, Bovis F, Davì S, Horne A, Fischbach M, Frosch M, et al. Development and initial validation of the MS score for diagnosis of macrophage activation syndrome in systemic juvenile idiopathic arthritis. Ann Rheum Dis. 2019;78(10):1357-62. https://doi.org/10.1136/annrheumdis-2019-215211.
https://doi.org/10.1136/annrheumdis-2019...
-1818. Gormezano NW, Otsuzi CI, Barros DL, da Silva MA, Pereira RM, Campos LM, et al. Macrophage activation syndrome: A severe and frequent manifestation of acute pancreatitis in 362 childhood-onset compared to 1830 adult-onset systemic lupus erythematosus patients. Semin Arthritis Rheum. 2016;45(6):706-10. https://doi.org/10.1016/j.semarthrit.2015.10.015.
https://doi.org/10.1016/j.semarthrit.201...
).

Furthermore, the prevalence of adolescents with preexisting chronic diseases has been rising in the last years, resulting in considerable morbidity and mortality. These patients may present high disease complexity and severity with an unpredictable course, requiring multiple medications, several physician appointments in outpatient clinics and emergency departments, several hospital admissions, and an undoubtedly high risk of infectious diseases. The most prevalent diagnoses of these chronic conditions in adolescents are asthma, obesity, cancer, diabetes mellitus, transplantation, and autoimmune diseases (1919. Alveno RA, Miranda CV, Passone CG, Waetge AR, Hojo ES, Farhat SCL, et al. Pediatric chronic patients at outpatient clinics: a study in a Latin American University Hospital. J Pediatr. 2018;94(5):539-45. https://doi.org/10.1016/j.jped.2017.07.014.
https://doi.org/10.1016/j.jped.2017.07.0...

20. Passone CGB, Grisi SJ, Farhat SC, Manna TD, Pastorino AC, Alveno RA, et al. Complexity of pediatric chronic disease: cross-sectional study with 16,237 patients followed by multiple medical specialties. Rev Paul Pediatr. 2019;38:e2018101. https://doi.org/10.1590/1984-0462/2020/38/2018101.
https://doi.org/10.1590/1984-0462/2020/3...
-2121. Ramos GF, Ribeiro VP, Mercadante MP, Ribeiro MP, Delgado AF, Farhat SCL, et al. Mortality in adolescents and young adults with chronic diseases during 16 years: a study in a Latin American tertiary hospital. J Pediatr. 2019;95(6):667-73. https://doi.org/10.1016/j.jped.2018.06.006.
https://doi.org/10.1016/j.jped.2018.06.0...
).

Thus, preexisting chronic conditions in adolescents with confirmed COVID-19 may be associated with the risk of progression to severe disease (acute respiratory failure and/or multi-organ dysfunction syndrome) and death (2222. Dayal D. We urgently need guidelines for managing COVID-19 in children with comorbidities. Acta Paediatr. 2020. https://doi.org/10.1111/apa.15304.
https://doi.org/10.1111/apa.15304...
). Despite recent publications, the real predisposition and risk of COVID-19 in adolescent populations with preexisting chronic conditions are still unknown.

In this regard, this emerging infectious disease appears to have a milder course and a less aggressive attack rate in the pediatric population with asthma (2323. Shaker MS, Oppenheimer J, Grayson M, Stukus D, Hartog N, Hsieh EWY, et al. COVID-19: Pandemic Contingency Planning for the Allergy and Immunology Clinic. J Allergy Clin Immunol Pract. 2020. pii: S2213-2198(20)30253-1. https://doi.org/10.1016/j.jaip.2020.03.012
https://doi.org/10.1016/j.jaip.2020.03.0...
). In contrast, obese patients may be at a higher risk of impaired outcomes associated with COVID-19 (2424. Puig-Domingo M, Marazuela M, Giustina A. COVID-19 and endocrine diseases. A statement from the European Society of Endocrinology. Endocrine. 2020;68(1):2-5. https://doi.org/10.1007/s12020-020-02294-5.
https://doi.org/10.1007/s12020-020-02294...
). Chronic hyperglycemia may impact the immune function and also increases the morbimortality risk due to this acute infectious disease (2424. Puig-Domingo M, Marazuela M, Giustina A. COVID-19 and endocrine diseases. A statement from the European Society of Endocrinology. Endocrine. 2020;68(1):2-5. https://doi.org/10.1007/s12020-020-02294-5.
https://doi.org/10.1007/s12020-020-02294...
). The long-term effects of this global health emergency, with school closure, physical inactivity, sedentary behavior, and consumption of calories-dense comfort foods, may increase the risk of weight gain in teenagers, particularly those living in urban districts (2525. Rundle AG, Park Y, Herbstman JB, Kinsey EW, Wang YC. COVID-19-Related School Closings and Risk of Weight Gain Among Children. Obesity (Silver Spring). 2020. https://doi.org/10.1002/oby.22813
https://doi.org/10.1002/oby.22813...

26. Joob B, Wiwanitkit V. COVID-19, School Closings and Weight Gain. Obesity (Silver Spring). 2020. https://doi.org/10.1002/oby.22825
https://doi.org/10.1002/oby.22825...
-2727. Pinto AJ, Roschel H, de Sá Pinto AL, Lima FR, Pereira RMR, Silva CA, et al. Physical inactivity and sedentary behavior: Overlooked risk factors in autoimmune rheumatic diseases? Autoimmun Rev. 2017;16(7):667-74. https://doi.org/10.1016/j.autrev.2017.05.001.
https://doi.org/10.1016/j.autrev.2017.05...
).

The data of immunocompromised children and adolescents with cancer and COVID-19 are scarce (2828. Bouffet E, Challinor J, Sullivan M, Biondi A, Rodriguez-Galindo C, Pritchard-Jones K. Early advice on managing children with cancer during the COVID-19 pandemic and a call for sharing experiences. Pediatr Blood Cancer. 2020. https://doi.org/10.1002/pbc.28327
https://doi.org/10.1002/pbc.28327...
-2929. Kotecha RS. Challenges posed by COVID-19 to children with cancer. Lancet Oncol. 2020. pii: S1470-2045(20)30205-9. https://doi.org/10.1016/S1470-2045(20)30205-9
https://doi.org/10.1016/S1470-2045(20)30...
), as well as in adult cancer patients (44. Chen ATC, Moniz CMV, Ribeiro-Júnior U, Diz MDPE, Salvajoli JV, Da Conceição Vasconcelos KGM, et al. How should health systems prepare for the evolving COVID-19 pandemic? Reflections from the perspective of a Tertiary Cancer Center. Clinics. 2020;75:e1864. https://doi.org/10.6061/clinics/2020/e1864.
https://doi.org/10.6061/clinics/2020/e18...
). The majority of childhood cancers are aggressive, requiring prompt and intensive multiagent chemotherapy or stem cell transplantation, and postponing these treatments are not indicated during this pandemic (2828. Bouffet E, Challinor J, Sullivan M, Biondi A, Rodriguez-Galindo C, Pritchard-Jones K. Early advice on managing children with cancer during the COVID-19 pandemic and a call for sharing experiences. Pediatr Blood Cancer. 2020. https://doi.org/10.1002/pbc.28327
https://doi.org/10.1002/pbc.28327...
-2929. Kotecha RS. Challenges posed by COVID-19 to children with cancer. Lancet Oncol. 2020. pii: S1470-2045(20)30205-9. https://doi.org/10.1016/S1470-2045(20)30205-9
https://doi.org/10.1016/S1470-2045(20)30...
).

In addition, there are limited data regarding COVID-19 in adolescents and adults with preexisting chronic conditions, particularly those with autoimmune rheumatic diseases (22. Park SE. Epidemiology, virology, and clinical features of severe acute respiratory syndrome -coronavirus-2 (SARS-CoV-2; Coronavirus Disease-19). Clin Exp Pediatr. 2020;63(4):119-24. https://doi.org/10.3345/cep.2020.00493.
https://doi.org/10.3345/cep.2020.00493...
,1212. Haşlak F, Yıldız M, Adrovic A, Barut K, Kasapçopur Ö. Childhood Rheumatic Diseases and COVID-19 Pandemic: An Intriguing Linkage and a New Horizon. Balkan Med J. 2020. https://doi.org/10.4274/balkanmedj.galenos.2020.2020.4.43
https://doi.org/10.4274/balkanmedj.galen...
,3030. Figueroa-Parra G, Aguirre-Garcia GM, Gamboa-Alonso CM, Camacho-Ortiz A, Galarza-Delgado DA. Are my patients with rheumatic diseases at higher risk of COVID-19? Ann Rheum Dis. 2020. pii: annrheumdis-2020-217322. https://doi.org/10.1136/annrheumdis-2020-217322
https://doi.org/10.1136/annrheumdis-2020...

31. Favalli EG, Ingegnoli F, De Lucia O, Cincinelli G, Cimaz R, Caporali R. COVID-19 infection and rheumatoid arthritis: Faraway, so close! Autoimmun Rev. 2020;19(5):102523. https://doi.org/10.1016/j.autrev.2020.102523
https://doi.org/10.1016/j.autrev.2020.10...
-3232. Caso F, Costa L, Ruscitti P, Navarini L, Del Puente A, Giacomelli R, et al. Could Sars-coronavirus-2 trigger autoimmune and/or autoinflammatory mechanisms in genetically predisposed subjects? Autoimmun Rev. 2020;19(5):102524. https://doi.org/10.1016/j.autrev.2020.102524.
https://doi.org/10.1016/j.autrev.2020.10...
), inflammatory bowel disease (3333. Monteleone G, Ardizzone S. Are patients with inflammatory bowel disease at increased risk for Covid-19 infection? J Crohns Colitis. 2020. pii:jjaa061. https://doi.org/10.1093/ecco-jcc/jjaa061
https://doi.org/10.1093/ecco-jcc/jjaa061...
), autoimmune hepatitis, and those undergoing liver transplantation (3434. D’Antiga L. Coronaviruses and immunosuppressed patients. The facts during the third epidemic. Liver Transpl. 2020. https://doi.org/10.1002/lt.25756
https://doi.org/10.1002/lt.25756...
). Patients with these chronic diseases have particular concerns with regard to their risk of severe infection and to the management of their immunosuppressive or immune-modifying drug treatments during the pandemic (3535. Rubin DT, Feuerstein JD, Wang AY, Cohen RD. AGA Clinical Practice Update on Management of Inflammatory Bowel Disease During the COVID-19 Pandemic: Expert Commentary. Gastroenterology. 2020. pii:S0016-5085(20)30482-0. https://doi.org/10.1053/j.gastro.2020.04.012
https://doi.org/10.1053/j.gastro.2020.04...
). However, recent data do not indicate an increased risk of SARS-CoV-2 infection in patients with these chronic conditions (3030. Figueroa-Parra G, Aguirre-Garcia GM, Gamboa-Alonso CM, Camacho-Ortiz A, Galarza-Delgado DA. Are my patients with rheumatic diseases at higher risk of COVID-19? Ann Rheum Dis. 2020. pii: annrheumdis-2020-217322. https://doi.org/10.1136/annrheumdis-2020-217322
https://doi.org/10.1136/annrheumdis-2020...

31. Favalli EG, Ingegnoli F, De Lucia O, Cincinelli G, Cimaz R, Caporali R. COVID-19 infection and rheumatoid arthritis: Faraway, so close! Autoimmun Rev. 2020;19(5):102523. https://doi.org/10.1016/j.autrev.2020.102523
https://doi.org/10.1016/j.autrev.2020.10...

32. Caso F, Costa L, Ruscitti P, Navarini L, Del Puente A, Giacomelli R, et al. Could Sars-coronavirus-2 trigger autoimmune and/or autoinflammatory mechanisms in genetically predisposed subjects? Autoimmun Rev. 2020;19(5):102524. https://doi.org/10.1016/j.autrev.2020.102524.
https://doi.org/10.1016/j.autrev.2020.10...

33. Monteleone G, Ardizzone S. Are patients with inflammatory bowel disease at increased risk for Covid-19 infection? J Crohns Colitis. 2020. pii:jjaa061. https://doi.org/10.1093/ecco-jcc/jjaa061
https://doi.org/10.1093/ecco-jcc/jjaa061...

34. D’Antiga L. Coronaviruses and immunosuppressed patients. The facts during the third epidemic. Liver Transpl. 2020. https://doi.org/10.1002/lt.25756
https://doi.org/10.1002/lt.25756...
-3535. Rubin DT, Feuerstein JD, Wang AY, Cohen RD. AGA Clinical Practice Update on Management of Inflammatory Bowel Disease During the COVID-19 Pandemic: Expert Commentary. Gastroenterology. 2020. pii:S0016-5085(20)30482-0. https://doi.org/10.1053/j.gastro.2020.04.012
https://doi.org/10.1053/j.gastro.2020.04...
).

It is notable that the recent Bergamo report showed that none of the patients who underwent liver transplantation had severe COVID-19, despite 3/700 (0.4%) having tested positive for SARS-CoV-2 (3434. D’Antiga L. Coronaviruses and immunosuppressed patients. The facts during the third epidemic. Liver Transpl. 2020. https://doi.org/10.1002/lt.25756
https://doi.org/10.1002/lt.25756...
). Another Italian case series showed that 13/320 (4%) adult patients with chronic arthritis under immunosuppressant agents had suspected or confirmed COVID-19. Only one (0.3%) patient required hospitalization for oxygen supplementation, and none of them died (3636. Monti S, Balduzzi S, Delvino P, Bellis E, Quadrelli VS, Montecucco C. Clinical course of COVID-19 in a series of patients with chronic arthritis treated with immunosuppressive targeted therapies. Ann Rheum Dis. 2020;79(5):667-8. https://doi.org/10.1136/annrheumdis-2020-217424.
https://doi.org/10.1136/annrheumdis-2020...
).

Since the pandemic has rapidly deteriorated into a global crisis, several national and local public health authorities and international agencies (particularly the WHO) (3737. World Health Organization. Coronavirus disease (COVID-19) advice for the public: Advocacy Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/advice-for-public/healthy-parenting [cited April 14th, 2020].
https://www.who.int/emergencies/diseases...
), have regularly provided updated COVID-19 recommendations. Some additional recommendations are suggested for healthy adolescents and adolescents with chronic illnesses during COVID-19:

  1. There are six WHO advocacies for parents and adolescents during confinement: 1) one-on-one time (including talking about sports, cooking, and physical activities), 2) staying positive in difficult times, 3) creating a daily routine, 4) avoiding bad behavior and habits, 5) keeping calm and managing stress, and 6) being honest and supportive when talking about COVID-19 (3737. World Health Organization. Coronavirus disease (COVID-19) advice for the public: Advocacy Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/advice-for-public/healthy-parenting [cited April 14th, 2020].
    https://www.who.int/emergencies/diseases...
    ).

  2. Adolescents should be encouraged to practice social distancing to limit potential exposure and to wear masks to protect against SARS-CoV-2, particularly outside of the home and during outpatient visits.

  3. Telemedicine seems to be an effective and sustainable technology for adolescents, parents, and multidisciplinary teams. This technology may help conduct online appointments with respect to adolescent physicians and pediatric subspecialties during the COVID-19 pandemic (3838. Verstraete SG, Sola AM, Ali SA. Telemedicine for Pediatric Inflammatory bowel disease in the Era of COVID-19. J Pediatr Gastroenterol Nutr. 2020. https://doi.org/10.1097/MPG.0000000000002747
    https://doi.org/10.1097/MPG.000000000000...

    39. Liu S, Yang L, Zhang C, Xiang YT, Liu Z, Hu S, et al. Online mental health services in China during the COVID-19 outbreak. Lancet Psychiatry. 2020;7(4):e17-e18. https://doi.org/10.1016/S2215-0366(20)30077-8.
    https://doi.org/10.1016/S2215-0366(20)30...
    -4040. Kaufman KR, Petkova E, Bhui KS, Schulze TG. A global needs assessment in times of a global crisis: world psychiatry response to the COVID-19 pandemic. BJPsych Open. 2020. https://doi.org/10.1192/bjo.2020.25
    https://doi.org/10.1192/bjo.2020.25...
    ).

  4. Adolescence is a transitional stage involving biological, psychological, and cultural expressions and cognitive development. During this period, teenagers gradually become more independent, gaining autonomy from parents, bonding with their peers, and beginning romantic interests (4141. Silva CA, Terreri MT, Bonfa E, Saad-Magalhaes C. Pediatric rheumatic disease patients: time to extend the age limit of adolescence? Adv Rheumatol. 2018;58(1):30. https://doi.org/10.1186/s42358-018-0031-y.
    https://doi.org/10.1186/s42358-018-0031-...
    ,4242. Silva CA, Aikawa NE, Pereira RM, Campos LM. Management considerations for childhood-onset systemic lupus erythematosus patients and implications on therapy. Expert Rev Clin Immunol. 2016;12(3):301-13. https://doi.org/10.1586/1744666X.2016.1123621.
    https://doi.org/10.1586/1744666X.2016.11...
    ). Feelings, fear of developing the coronavirus infection and dying, peer relations, closing of schools and universities, suspending sporting events, familial financial loss, domestic conflict, parents’ tension, and novel daily hygiene habits should be discussed in the adolescent appointments. These appointments may be focused on only teenagers or may include adolescents and their parents (4343. Casanova M, Pagani Bagliacca E, Silva M, Patriarca C, Veneroni L, Clerici CA, et al. How young patients with cancer perceive the Covid-19 (coronavirus) epidemic in Milan, Italy: is there room for other fears? Pediatr Blood Cancer. 2020. https://doi.org/10.1002/pbc.28318
    https://doi.org/10.1002/pbc.28318...
    ,4444. Wang G, Zhang Y, Zhao J, Zhang J, Jiang F. Mitigate the effects of home confinement on children during the COVID-19 outbreak. Lancet. 2020;395(10228):945-7. https://doi.org/10.1016/S0140-6736(20)30547-X.
    https://doi.org/10.1016/S0140-6736(20)30...
    ).

  5. A home schooling plan for adolescents should be applied by schools/universities and teachers using online tools (4444. Wang G, Zhang Y, Zhao J, Zhang J, Jiang F. Mitigate the effects of home confinement on children during the COVID-19 outbreak. Lancet. 2020;395(10228):945-7. https://doi.org/10.1016/S0140-6736(20)30547-X.
    https://doi.org/10.1016/S0140-6736(20)30...
    ).

  6. Healthy foods should be reinforced during quarantine, avoiding ultra-processed foods, reinforcing cooking, and stocking homemade foods.

  7. Physical exercise is essential during the lockdown. There are several specialized online channels with recreational activities and easy access via the internet for adolescents who stay at home. Outdoor activities should be avoided.

  8. Quarantine has been a necessary preventive measure during this pandemic around the world and may result in negative psychological outcomes in adolescents and their families. Therefore, information and communication for adolescents (using telemedicine or telephone support lines) and motivation through social networking by mobile phone should be priorities (4545. Brooks SK, Webster RK, Smith LE, Woodland L, Wessely S, Greenberg N, et al. The psychological impact of quarantine and how to reduce it: rapid review of the evidence. Lancet. 2020;395(10227):912-20. https://doi.org/10.1016/S0140-6736(20)30460-8.
    https://doi.org/10.1016/S0140-6736(20)30...
    ). Psychological and psychiatric issues (such as acute stress, anxiety, depression, post-traumatic stress disorder, and emotional exhaustion) may occur or worsen in healthy adolescents and adolescents with chronic illnesses during the COVID-19 quarantine/lockdown and social isolation, requiring online mental health services (as cognitive behavioral therapy) (3939. Liu S, Yang L, Zhang C, Xiang YT, Liu Z, Hu S, et al. Online mental health services in China during the COVID-19 outbreak. Lancet Psychiatry. 2020;7(4):e17-e18. https://doi.org/10.1016/S2215-0366(20)30077-8.
    https://doi.org/10.1016/S2215-0366(20)30...
    ,4040. Kaufman KR, Petkova E, Bhui KS, Schulze TG. A global needs assessment in times of a global crisis: world psychiatry response to the COVID-19 pandemic. BJPsych Open. 2020. https://doi.org/10.1192/bjo.2020.25
    https://doi.org/10.1192/bjo.2020.25...
    ,4545. Brooks SK, Webster RK, Smith LE, Woodland L, Wessely S, Greenberg N, et al. The psychological impact of quarantine and how to reduce it: rapid review of the evidence. Lancet. 2020;395(10227):912-20. https://doi.org/10.1016/S0140-6736(20)30460-8.
    https://doi.org/10.1016/S0140-6736(20)30...
    ).

  9. Home confinements may induce longer screen time and sleep issues. Regular sleep patterns and parental control of screen time should be reinforced during the lockdown.

  10. Drinking alcohol does not protect against COVID-19 and alcohol intake can increase the risk of health issues in adolescents (3737. World Health Organization. Coronavirus disease (COVID-19) advice for the public: Advocacy Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/advice-for-public/healthy-parenting [cited April 14th, 2020].
    https://www.who.int/emergencies/diseases...
    ).

  11. Since prisons are the epicenters for infectious diseases, the prevention and control of COVID-19 are required for specific adolescents and youth populations in jail, including individual protection measures, social distancing, regular environmental cleaning, and limiting prison visits (4646. Kinner SA, Young JT, Snow K, Southalan L, Lopez-Acuãa D, Ferreira-Borges C, et al. Prisons and custodial settings are part of a comprehensive response to COVID-19. Lancet Public Health. 2020;5(4):e188-e189. https://doi.org/10.1016/S2468-2667(20)30058-X.
    https://doi.org/10.1016/S2468-2667(20)30...
    ,4747. Wurcel AG, Dauria E, Zaller N, Nijhawan A, Beckwith C, Nowotny K, et al. Spotlight on Jails: COVID-19 Mitigation Policies Needed Now. Clin Infect Dis. 2020. pii: ciaa346. https://doi.org/10.1093/cid/ciaa346
    https://doi.org/10.1093/cid/ciaa346...
    ).

  12. During the pandemic, routine appointments and elective surgeries and procedures should be postponed for adolescents.

  13. The number of subjects visiting adolescents with chronic diseases must be reduced in outpatient clinics, day-clinics, and hospitals during the pandemic, especially for those taking immunosuppressive agents or for pediatric transplantation patients (2929. Kotecha RS. Challenges posed by COVID-19 to children with cancer. Lancet Oncol. 2020. pii: S1470-2045(20)30205-9. https://doi.org/10.1016/S1470-2045(20)30205-9
    https://doi.org/10.1016/S1470-2045(20)30...
    ).

  14. Adherence to medications should be reinforced for all adolescents with preexisting chronic disease (4242. Silva CA, Aikawa NE, Pereira RM, Campos LM. Management considerations for childhood-onset systemic lupus erythematosus patients and implications on therapy. Expert Rev Clin Immunol. 2016;12(3):301-13. https://doi.org/10.1586/1744666X.2016.1123621.
    https://doi.org/10.1586/1744666X.2016.11...
    ).

  15. Immunosuppressive and immune-modifying drug treatments, multiagent chemotherapy, and stem cell transplantation should be evaluated for each adolescent without COVID-19, according to their specific preexisting chronic disease.

  16. Medications should be adjusted or stopped for each adolescent who has been infected with for SARS-CoV-2 or has been confirmed as having COVID-19 for each specific preexisting chronic condition. The immunosuppressive agents may be restarted after two weeks if the adolescent has not developed COVID-19 manifestations or after complete sign and symptom resolution, as suggested for inflammatory bowel disease patients (3535. Rubin DT, Feuerstein JD, Wang AY, Cohen RD. AGA Clinical Practice Update on Management of Inflammatory Bowel Disease During the COVID-19 Pandemic: Expert Commentary. Gastroenterology. 2020. pii:S0016-5085(20)30482-0. https://doi.org/10.1053/j.gastro.2020.04.012
    https://doi.org/10.1053/j.gastro.2020.04...
    ).

  17. The comorbidities in adolescents that are associated with a high risk of severe COVID-19 in adult populations should be identified, stopped, and/or treated: smoking, arterial hypertension, diabetes mellitus, asthma, and chronic kidney disease (22. Park SE. Epidemiology, virology, and clinical features of severe acute respiratory syndrome -coronavirus-2 (SARS-CoV-2; Coronavirus Disease-19). Clin Exp Pediatr. 2020;63(4):119-24. https://doi.org/10.3345/cep.2020.00493.
    https://doi.org/10.3345/cep.2020.00493...

    3. Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020. https://doi.org/10.1001/jama.2020.2648.
    https://doi.org/10.1001/jama.2020.2648...
    -44. Chen ATC, Moniz CMV, Ribeiro-Júnior U, Diz MDPE, Salvajoli JV, Da Conceição Vasconcelos KGM, et al. How should health systems prepare for the evolving COVID-19 pandemic? Reflections from the perspective of a Tertiary Cancer Center. Clinics. 2020;75:e1864. https://doi.org/10.6061/clinics/2020/e1864.
    https://doi.org/10.6061/clinics/2020/e18...
    ).

  18. The vaccination card must be updated. During the COVID-19 pandemic, adolescents with preexisting chronic diseases should receive the annual influenza vaccine, regardless of current disease activity and the use of any immunosuppressive drug, as suggested for adolescents with autoimmune rheumatic diseases (4848. Silva CA, Aikawa NE, Bonfa E. Vaccinations in juvenile chronic inflammatory diseases: an update. Nat Rev Rheumatol. 2013;9(9):532-43. https://doi.org/10.1038/nrrheum.2013.95.
    https://doi.org/10.1038/nrrheum.2013.95...
    ). The adolescents in prison should also receive this annual immunization.

  19. Adolescents with autoimmune diseases, who have confirmed COVID-19 must be strictly monitored for the possible risk of reactivation of the disease after the resolution of this viral infection (3232. Caso F, Costa L, Ruscitti P, Navarini L, Del Puente A, Giacomelli R, et al. Could Sars-coronavirus-2 trigger autoimmune and/or autoinflammatory mechanisms in genetically predisposed subjects? Autoimmun Rev. 2020;19(5):102524. https://doi.org/10.1016/j.autrev.2020.102524.
    https://doi.org/10.1016/j.autrev.2020.10...
    ).

  20. Owing to the negative economic impact of this pandemic, vulnerable adolescents and their families should receive financial support.

In conclusion, spotlight and recommendations for healthy adolescents and adolescents with preexisting chronic diseases during the COVID-19 pandemic should be reinforced for all subjects, particularly for those under quarantine/lockdown. Further studies will be necessary to clarify and to assess specific adolescent populations during this emerging infectious disease pandemic.

ACKNOWLEDGMENTS

This study was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 303422/2015-7 to CAS), Fundação de Amparo è Pesquisa do Estado de São Paulo (FAPESP 2015/03756-4 to CAS), and by Núcleo de Apoio è Pesquisa “Saúde da Criança e do Adolescente” da USP (NAP-CriAd) to CAS.

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Publication Dates

  • Publication in this collection
    08 May 2020
  • Date of issue
    2020

History

  • Received
    16 Apr 2020
  • Accepted
    17 Apr 2020
Creative Common - by 4.0
This is an Open Access article distributed under the terms of the Creative Commons License (https://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium or format, provided the original work is properly cited.
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