Respiratory Infections in Children during the Covid-19 Pandemic

Relevance. Acute respiratory infections (ARI) are a leading cause of morbidity and mortality in children worldwide. The COVID-19 pandemic has significantly influenced the circulation of other respiratory viruses. Understanding the interactions between SARSCoV-2 and other respiratory pathogens is crucial for predicting disease severity, improving diagnostic and treatment methods, and developing effective prevention strategies. 

Aims. This study aims to analyze changes in the circulation of respiratory viruses at different stages of the COVID-19 pandemic, investigate the prevalence and characteristics of viral and bacterial co-infections in children, and assess their impact on disease progression.

Conclusions.  At the initial stage of the COVID-19 pandemic, the incidence of respiratory viral infections declined, followed by a rapid resurgence after the lifting of restrictive measures. In children, COVID19 presents with milder symptoms than in adults and has a high proportion of asymptomatic cases. Mixed SARS-CoV-2 infections with other respiratory viruses are more common in younger children and do not significantly increase disease severity. However, secondary bacterial infections in children with COVID-19 substantially elevate the risk of severe disease progression.

1. Troeger C, Forouzanfar M, Rao PC, et al. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory tract infections in 195 countries: a systematic analysis for the Global Burden of Disease Study 2015. The Lancet Infectious Diseases 2017;17:1133–61. https://doi.org/10.1016/S1473-3099(17)30396-1.

2. Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing. State Report «On the State of the Sanitary and Epidemiological Welfare of the Population in the Russian Federation in 2020.» (In Russ.). Available in: https://www.rospotrebnadzor.ru/upload/iblock/5fa/gd-seb_02.06-_s-podpisyu_.pdf (accessed December 24, 2024).

3. World Health Organization. Coronavirus disease 2019 (COVID-19) Situation Report – 51 n.d. Available in: https://www.who.int/docs/default-source/coronaviruse/situationreports/20200311-sitrep-51-covid-19.pdf (accessed January 24, 2025).

4. Chow EJ, Uyeki TM, Chu HY. The effects of the COVID-19 pandemic on community respiratory virus activity. Nat Rev Microbiol 2023;21:195–210. https://doi.org/10.1038/s41579-022-00807-9.

5. Poole S, Brendish NJ, Clark TW. SARS-CoV-2 has displaced other seasonal respiratory viruses: Results from a prospective cohort study. Journal of Infection 2020;81:966–72. https://doi.org/10.1016/j.jinf.2020.11.010.

6. Yakovlev AS, Belyaletdinova IK, Mazankova LN, et al. SARS-CoV-2 infection in children in Moscow in 2020: clinical features and impact on circulation of other respiratory viruses: SARS-CoV-2 infection in children in Moscow in 2020. International Journal of Infectious Diseases 2022;116:331–8. https://doi.org/10.1016/j.ijid.2021.12.358.

7. Docherty AB, Harrison EM, Green CA, et al. Features of 20 133 UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study. BMJ 2020;369:m1985. https://doi.org/10.1136/bmj.m1985.

8. Castagnoli R, Votto M, Licari A, et al. Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection in Children and Adolescents: A Systematic Review. JAMA Pediatrics 2020;174:882–9. https://doi.org/10.1001/jamapediatrics.2020.1467.

9. Markov P V, Ghafari M, Beer M, et al. The evolution of SARS-CoV-2. Nat Rev Microbiol 2023;21:361–79. https://doi.org/10.1038/s41579-023-00878-2.

10. Groves H E, Piché-Renaud P-P, Peci A, et al. The impact of the COVID-19 pandemic on influenza, respiratory syncytial virus, and other seasonal respiratory virus circulation in Canada: A population-based study. Lancet Reg Health Am 2021;1:100015. https://doi.org/10.1016/j.lana.2021.100015.

11. Liu X, Peng Y, Chen Z, et al. Impact of non-pharmaceutical interventions during COVID-19 on future influenza trends in Mainland China. BMC Infectious Diseases 2023;23:632. https://doi.org/10.1186/s12879-023-08594-1.

12. Piret J, Boivin G. Viral Interference between Respiratory Viruses. Emerg Infect Dis 2022;28:273–81. https://doi.org/10.3201/eid2802.211727.

13. Kurskaya O G, Prokopyeva E A, Sobolev I A, et al. Changes in the Etiology of Acute Respiratory Infections among Children in Novosibirsk, Russia, between 2019 and 2022: The Impact of the SARS-CoV-2 Virus. Viruses 2023;15:934. https://doi.org/10.3390/v15040934.

14. Gushchin V A, Dolzhikova I V, Shchetinin A M, et al. Neutralizing Activity of Sera from Sputnik V-Vaccinated People against Variants of Concern (VOC: B.1.1.7, B.1.351, P.1, B.1.617.2, B.1.617.3) and Moscow Endemic SARS-CoV-2 Variants. Vaccines 2021;9:779. https://doi.org/10.3390/vaccines9070779.

15. Akimkin V G, Popova A Y, Ploskireva A A, et al. COVID-19: the evolution of the pandemic in Russia. Report I: manifestations of the COVID-19 epidemic process. Journal of microbiology, epidemiology and immunobiology. - 2022. - Vol. 99. - N. 3. - P. 269-286. (In Russ.) doi: 10.36233/0372-9311-276

16. Olsen S J, Azziz-Baumgartner E, Budd A P, et al. Decreased Influenza Activity During the COVID-19 Pandemic - United States, Australia, Chile, and South Africa, 2020. MMWR Morb Mortal Wkly Rep 2020;69:1305–9. https://doi.org/10.15585/mmwr.mm6937a6.

17. Abu-Raya B, Viñeta Paramo M, Reicherz F, et al. Why has the epidemiology of RSV changed during the COVID-19 pandemic? EClinicalMedicine 2023;61:102089. https://doi.org/10.1016/j.eclinm.2023.102089.

18. Wagatsuma K, Koolhof I S, Shobugawa Y, et al. Decreased human respiratory syncytial virus activity during the COVID-19 pandemic in Japan: an ecological time-series analysis. BMC Infect Dis 2021;21:734. https://doi.org/10.1186/s12879-021-06461-5.

19. Arellanos-Soto D, Padilla-Rivas G, Ramos-Jimenez J, et al. Decline in influenza cases in Mexico after the implementation of public health measures for COVID-19. Sci Rep 2021;11:10730. https://doi.org/10.1038/s41598-021-90329-w.

20. Park K Y, Seo S, Han J, et al. Respiratory virus surveillance in Canada during the COVID-19 pandemic: An epidemiological analysis of the effectiveness of pandemic-related public health measures in reducing seasonal respiratory viruses test positivity. PLoS One 2021;16:e0253451. https://doi.org/10.1371/journal.pone.0253451.

21. Meningher T, Hindiyeh M, Regev L, et al. Relationships between A(H1N1)pdm09 influenza infection and infections with other respiratory viruses. Influenza Other Respir Viruses 2014;8:422–30. https://doi.org/10.1111/irv.12249.

22. Lansbury L, Lim B, Baskaran V, et al. Co-infections in people with COVID-19: a systematic review and meta-analysis. J Infect 2020;81:266–75. https://doi.org/10.1016/j.jinf.2020.05.046.

23. Avdeeva M G, Kulbuzheva M I, Zotov S V, et al. Microbial landscape in hospital patients with new coronavirus disease (COVID-19), antibiotic resistance comparison vs. Precovid stage: a prospective study. Kuban Scientific Medical Bulletin. 2021;28(5):14-28. (In Russ.) https://doi.org/10.25207/1608-6228-2021-28-5-14-28

24. Brueggemann A B, Jansen van Rensburg M J, Shaw D, et al. Changes in the incidence of invasive disease due to Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis during the COVID-19 pandemic in 26 countries and territories in the Invasive Respiratory Infection Surveillance Initiative: a prospective analysis of surveillance data. Lancet Digit Health 2021;3:e360–70. https://doi.org/10.1016/S2589-7500(21)00077-7.

25. Almeida T, Guimarães J T, Rebelo S. Epidemiological Changes in Respiratory Viral Infections in Children: The Influence of the COVID-19 Pandemic. Viruses 2023;15:1880. https://doi.org/10.3390/v15091880.

26. Westbrook A, Wang T, Bhakta K, et al. Respiratory Coinfections in Children With SARS-CoV-2. The Pediatric Infectious Disease Journal 2023;42:774. https://doi.org/10.1097/INF.0000000000003981.

27. Choudhary R, Webber B J, Womack L S, et al. Factors Associated With Severe Illness in Patients Aged <21 Years Hospitalized for COVID-19. Hosp Pediatr 2022;12:760–83. https://doi.org/10.1542/hpeds.2022-006613.

28. Zeng Z, Guan W, Liu Y, et al. Different Circulation Pattern of Multiple Respiratory Viruses in Southern China During the COVID-19 Pandemic. Front Microbiol 2022;12:801946. https://doi.org/10.3389/fmicb.2021.801946.

29. Lumley S F, Richens N, Lees E, et al. Changes in paediatric respiratory infections at a UK teaching hospital 2016–2021; impact of the SARS-CoV-2 pandemic. J Infect 2021. https://doi.org/10.1016/j.jinf.2021.10.022.

30. CDC. 2021-2022 Season. Influenza (Flu) 2024. Available in: https://www.cdc.gov/flu/season/2021-2022.html (accessed December 24, 2024).

31. Bancej C, Rahal A, Lee L, et al. National FluWatch mid-season report, 2021–2022: Sporadic influenza activity returns. Can Commun Dis Rep 2022;48:39–45. https://doi.org/10.14745/ccdr.v48i01a06.

32. White E B, O’Halloran A, Sundaresan D, et al. High Influenza Incidence and Disease Severity Among Children and Adolescents Aged <18 Years – United States, 2022–23 Season. MMWR Morb Mortal Wkly Rep 2023;72:1108–14. https://doi.org/10.15585/mmwr.mm7241a2.

33. El‐Heneidy A, Ware R S, Robson J M, et al. Respiratory virus detection during the COVID‐19 pandemic in Queensland, Australia. Aust N Z J Public Health 2022;46:10–5. https://doi.org/10.1111/1753-6405.13168.

34. Leung N H, Chu D K, Shiu E Y, et al. Respiratory Virus Shedding in Exhaled Breath and Efficacy of Face Masks. Nat Med 2020;26:676–80. https://doi.org/10.1038/s41591-0200843-2.

35. Park S, Michelow I C, Choe Y J. Shifting patterns of respiratory virus activity following social distancing measures for COVID-19 in South Korea. J Infect Dis 2021:jiab231. https://doi.org/10.1093/infdis/jiab231.

36. Yakovlev A S, Afanasev V V, Alekseenko S I, et al. Prevalence and Clinical Impact of Viral and Bacterial Coinfections in Hospitalized Children and Adolescents Aged under 18 Years with COVID-19 during the Omicron Wave in Russia. Viruses 2024;16:1180. https://doi.org/10.3390/v16081180.

37. Weidmann M D, Green D A, Berry G J, et al. Assessing respiratory viral exclusion and affinity interactions through co-infection incidence in a pediatric population during the 2022 resurgence of influenza and RSV. Front Cell Infect Microbiol 2023;13:1208235. https://doi.org/10.3389/fcimb.2023.1208235.

38. Wu A, Mihaylova V T, Landry M L, et al. Interference between rhinovirus and influenza A virus: a clinical data analysis and experimental infection study. Lancet Microbe 2020;1:e254–62. https://doi.org/10.1016/s2666-5247(20)30114-2.

39. Pinky L, Dobrovolny H M. Coinfections of the Respiratory Tract: Viral Competition for Resources. PLoS ONE 2016;11. https://doi.org/10.1371/journal.pone.0155589.

40. Dee K, Schultz V, Haney J, et al. Influenza A and Respiratory Syncytial Virus Trigger a Cellular Response That Blocks Severe Acute Respiratory Syndrome Virus 2 Infection in the Respiratory Tract. The Journal of Infectious Diseases 2023;227:1396–406. https://doi.org/10.1093/infdis/jiac494.

41. Nickbakhsh S, Mair C, Matthews L, et al. Virus–virus interactions impact the population dynamics of influenza and the common cold. Proceedings of the National Academy of Sciences 2019;116:27142–50. https://doi.org/10.1073/pnas.1911083116.

42. Massey B W, Jayathilake K, Meltzer H Y. Respiratory Microbial Co-infection With SARS-CoV-2. Front Microbiol 2020;11:2079. https://doi.org/10.3389/fmicb.2020.02079.

43. Kanji J N, Zelyas N, Pabbaraju K, et al. Respiratory virus coinfections with severe acute respiratory coronavirus virus 2 (SARS-CoV-2) continue to be rare one year into the coronavirus disease 2019 (COVID-19) pandemic in Alberta, Canada (June 2020–May 2021). Infect Control Hosp Epidemiol n.d.:1–4. https://doi.org/10.1017/ice.2021.495.

44. Uhteg K, Amadi A, Forman M, et al. Circulation of Non-SARS-CoV-2 Respiratory Pathogens and Coinfection with SARS-CoV-2 Amid the COVID-19 Pandemic. Open Forum Infect Dis 2021;9:ofab618. https://doi.org/10.1093/ofid/ofab618.

45. Malveste Ito C R, Moreira A L E, da Silva P A N, et al. Viral Coinfection of Children Hospitalized with Severe Acute Respiratory Infections during COVID-19 Pandemic. Biomedicines 2023;11:1402. https://doi.org/10.3390/biomedicines11051402.

46. Tannis A, Englund J A, Perez A, et al. SARS-CoV-2 Epidemiology and COVID-19 mRNA Vaccine Effectiveness Among Infants and Children Aged 6 Months–4 Years — New Vaccine Surveillance Network, United States, July 2022–September 2023. MMWR Morb Mortal Wkly Rep 2023;72:1300–6. https://doi.org/10.15585/mmwr.mm7248a2.

47. UKHSA. Surveillance of influenza and other seasonal respiratory viruses in the UK, winter 2022 to 2023. GOVUK n.d. Available in: https://www.gov.uk/government/statistics/annual-flu-reports/surveillance-of-influenza-and-other-seasonal-respiratory-viruses-in-the-uk-winter-2022-to-2023 (accessed February 6, 2025).

48. Bahl A, Mielke N, Johnson S, et al. Severe COVID-19 outcomes in pediatrics: an observational cohort analysis comparing Alpha, Delta, and Omicron variants. Lancet Reg Health Am 2022;18:100405. https://doi.org/10.1016/j.lana.2022.100405.

49. Popova A Y, Ezhlova E B, Melnikova A A, et al. The seroprevalence of SARS-CoV-2 among residents of the Khabarovsk Krai during the COVID-19 epidemic // Journal of microbiology, epidemiology and immunobiology. - 2021. - Vol. 98. - N. 1. - P. 7-17. (In Russ.). doi: 10.36233/0372-9311-92

50. Popova A Yu, Ezhlova E B, Mel’nikova A A, et al. Herd Immunity to SARS-CoV-2 among the Population in Saint-Petersburg during the COVID-19 Epidemic. Problems of Particularly Dangerous Infections. 2020;(3):124-130. (In Russ.) https://doi.org/10.21055/0370-1069-2020-3-124-130

51. Hippich M, Holthaus L, Assfalg R, et al. A Public Health Antibody Screening Indicates a 6-Fold Higher SARS-CoV-2 Exposure Rate than Reported Cases in Children. Med 2021;2:149-163.e4. https://doi.org/10.1016/j.medj.2020.10.003.

52. Dondurey E A, Isankina L N, Afanasyeva O I, et al. Characteristics of CoVID-19 in children: the first experience in the hospital of st. Petersburg. Journal Infectology. 2020;12(3):56-63. (In Russ.). https://doi.org/10.22625/2072-6732-2020-12-3-56-63

53. Stopyra L, Kowalik A, Stala J, et al. The Age-Related Course of COVID-19 in Pediatric Patients—1405 Cases in a Single Center. Journal of Clinical Medicine 2022;11:7347. https://doi.org/10.3390/jcm11247347.

54. Lai C-C, Wang C-Y, Hsueh P-R. Co-infections among patients with COVID-19: The need for combination therapy with non-anti-SARS-CoV-2 agents? J Microbiol Immunol Infect 2020;53:505–12. https://doi.org/10.1016/j.jmii.2020.05.013.

55. Steponavičienė A, Burokienė S, Ivaškevičienė I, et al. Influenza and Respiratory Syncytial Virus Infections in Pediatric Patients during the COVID-19 Pandemic: A Single-Center Experience. Children (Basel) 2023;10:126. https://doi.org/10.3390/children10010126.

56. Xie J, Florin T A, Funk A L, et al. Respiratory Viral Co-infection in SARS-CoV-2-Infected Children During the Early and Late Pandemic Periods. The Pediatric Infectious Disease Journal n.d.:10.1097/INF.0000000000004623. https://doi.org/10.1097/INF.0000000000004623.

57. Agathis N T, Patel K, Milucky J, et al. Codetections of Other Respiratory Viruses Among Children Hospitalized With COVID-19. Pediatrics 2023;151:e2022059037. https://doi.org/10.1542/peds.2022-059037.

58. Fan Y, Li X, Zhang L, et al. SARS-CoV-2 Omicron variant: recent progress and future perspectives. Sig Transduct Target Ther 2022;7:1–11. https://doi.org/10.1038/s41392022-00997-x.

59. Hui K P Y, Ho J C W, Cheung M, et al. SARS-CoV-2 Omicron variant replication in human bronchus and lung ex vivo. Nature 2022;603:715–20. https://doi.org/10.1038/s41586022-04479-6.

60. Brigadoi G, Demarin G C, Boracchini R, et al. Comparison between the Viral Illness Caused by SARS-CoV-2, Influenza Virus, Respiratory Syncytial Virus and Other Respiratory Viruses in Pediatrics. Viruses 2024;16:199. https://doi.org/10.3390/v16020199.