Surge of Pediatric Respiratory Tract Infections after the COVID-19 Pandemic and the Concept of "Immune Debt"

Lea Lenglart¹, Luigi Titomanlio², Zsolt Bognar³, Silvia Bressan⁴, Danilo Buonsenso⁵, Tisham De⁶, Ruth Farrugia⁷, Kate Honeyford⁸, Ian K Maconochie⁹, Henriette A Moll¹⁰, Rianne Oostenbrink¹⁰, Niccolo Parri¹¹, Damian Roland¹², Esra Akyüz Özkan¹³, Laura Almeida¹⁴, Ilaria Alberti¹⁵, François Angoulvant¹⁶, Zein Assad¹⁷, Camille Aupiais¹⁸, Michael Barrett¹⁹, Romain Basmaci²⁰, Dorine Borensztajn²¹, Susana Castanhinha²², Antonio Chiaretti⁵, Robert Cohen²³, Sheena Durnin²⁴, Patrick Fitzpatrick²⁵, Susanne Greber-Platzer²⁶, Romain Guedj²⁷, Florian Hey²⁸, Lina Jankauskaite²⁹, Kristina Keitel³⁰, Ines Mascarenhas³¹, Gregorio P Milani¹⁵, Anna Maria Musolino³², Zanda Pučuka³³, Malin Ryd Rinder³⁴, Maria Chiara Supino³², Francesca Tirelli⁴, Ruud G Nijman³⁵, Naim Ouldali³⁶; EPISODES Study Group

Collaborators, Affiliations

Collaborators

EPISODES Study Group:
Tobias Alfven, Vanda Anacleto, Orkun Aydin, Clarissa Barber, Elena Bellelli, Ron Berant, Thibault De Groc, Laszlo Fodor, Sara Geitoeira, Borja Gomez, Florian Hoffmann, Daniela Kohlfuerst, Mojca Kolnik, Franziska Leeb, Fiona Leonard, Mark Lyttle, Patrícia Mação, Lia Mano, Rosa Morello, Sofia Reis, Ruben Rocha, Katy Rose, Alexis Rybak, Petra Salamon, Francisca Saraiva, Matthias Schaffert, Keren Shahar-Nissan, Gabor Simon, Ines Silva Costa, Joao Sousa Marques, Carl Alessandro Starvaggi, Ozlem Teksam, Valtýr Stefánsson Thors, Jonas Thüminger, Caner Turan, Roberto Velasco, Corinne Vasilico, Anna Chiara Vittucci, Christoph Zurl

Affiliations

¹ Pediatric Emergency Department, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris Cité University, Paris, France. Electronic address: lea.lenglart@aphp.fr.
² Pediatric Emergency Department, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris Cité University, Paris, France; Paris Cité University, INSERM U1141, DHU Protect, Paris, France.
³ Pediatric Emergency Department, Heim Pal National Pediatric Institute, Budapest, Hungary.
⁴ Division of Pediatric Emergency Medicine, Department of Women's and Children's Health - University Hospital of Padova, Padova, Italy.
⁵ Department of Woman and Child Health and Public Health, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy.
⁶ Section of Pediatric Infectious Diseases, Faculty of Medicine, Department of Infectious Diseases, Imperial College London, London, United Kingdom.
⁷ Department of Child and Adolescent Health, Mater Dei Hospital, Msida, Malta.
⁸ Health Informatics Team, Division of Clinical Studies, Institute of Cancer Research, London, United Kingdom.
⁹ Division of Medicine, Department of Pediatric Emergency Medicine, St. Mary's Hospital, Imperial College NHS Healthcare Trust, London, United Kingdom; Faculty of Medicine, Center for Pediatrics and Child Health, Imperial College London, London, United Kingdom.
¹⁰ Department General Pediatrics, ErasmusMC - Sophia, Rotterdam, The Netherlands.
¹¹ Emergency Department & Trauma Center, Ospedale Pediatrico Meyer Firenze, Florence, Italy.
¹² SAPPHIRE Group, Health Sciences, Leicester University, Leicester, United Kingdom; Pediatric Emergency Medicine Leicester Academic (PEMLA) Group, Leicester Hospitals, Leicester, United Kingdom.
¹³ Pediatric Emergeny Department, Ondokuz Mayıs University, Samsun, Turkey.
¹⁴ Centro Hospitalar e Universitário de São João, University of Porto, Porto, Portugal.
¹⁵ Pediatric Emergency Department, Forndazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy; Department of Clinical Science and Community Health, University of Milan, Milan, Italy.
¹⁶ Paris Sorbonne University, Center de Recherche des Cordeliers, INSERM UMRS 1138, Paris, France.
¹⁷ Department of General Pediatrics, Pediatric Infectious Disease and Internal Medicine, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France, Paris Cité University, Paris, France.
¹⁸ Pediatric Emergency Department, Jean Verdier Hospital, Bondy, Assistance Publique-Hôpitaux de Paris, Sorbonne Paris cité, Paris, France; Institut National de la Santé et de la Recherche Médicale UMR 1123, ECEVE, Paris, France.
¹⁹ Pediatric Emergency Department, Children's Health Ireland at Crumlin, Dublin, Ireland; Women's and Children's Health, University College Dublin, Dublin, Ireland.
²⁰ Pediatric Emergency Department, Louis Mourier Hospital, Colombes, Assistance Publique-Hôpitaux de Paris, Université De Paris, Paris, France.
²¹ Department of Pediatrics, NoordWest Ziekenhuisgroep, Alkmaar, Netherlands.
²² Hospital Dona Estefania, Centro Hospitalar de Lisboa Central, Lisbon, Portugal.
²³ Association Clinique et Thérapeutique Infantile du Val-de-Marne (ACTIV), St Maur-des-Fossés, France; Center Hospitalier Intercommunal, Research Center, Université Paris Est, IMRB-GRC GEMINI, Créteil, France.
²⁴ Department of Pediatric Emergency Medicine, Children's Health Ireland at Tallaght, Baile Átha Cliath, Ireland.
²⁵ Pediatric Emergency Department, Children's Health Ireland at Temple Street, Dublin, Ireland.
²⁶ Pediatric Emergency Unit, Clinical Division of Pediatric Pulmonology, Allergology and Endocrinology, Department of Pediatrics and Adolescent Medicine, Medical University of Vienna, Vienna, Austria.
²⁷ Pediatric Emergency Department, Armand Trousseau Hospital, Assistance Publique-Hôpitaux de Paris, Sorbonne Université, CRESS Inserm U-1153 Paris, Epopé Team, Paris, France.
²⁸ Pediatric Intensive Care Unit and Emergency Department, Dr. von Hauner Children's Hospital, Ludwig-Maximilians-University Munich, Munich, Germany.
²⁹ Department of Pediatrics, Lithuanian University of Health Sciences, Kaunas, Lithuania.
³⁰ Paediatric Emergency Department, Kinderklinik Inselspital, Bern, Switzerland.
³¹ Departamento da Criança e do Jovem-Urgencia Pediatrica, Hospital Prof. Doutor Fernando da Fonseca, Amadora, Portugal.
³² Emergency Department, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.
³³ Paediatric Emergency Department, Children's Clinical University Hospital, Riga Stradins University, Riga, Latvia.
³⁴ Pediatric Emergency Department, Astrid Lindgrens Children's hospital, Karolinska University Hospital, Karolinska, Sweden.
³⁵ Section of Pediatric Infectious Diseases, Faculty of Medicine, Department of Infectious Diseases, Imperial College London, London, United Kingdom; Division of Medicine, Department of Pediatric Emergency Medicine, St. Mary's Hospital, Imperial College NHS Healthcare Trust, London, United Kingdom; Faculty of Medicine, Center for Pediatrics and Child Health, Imperial College London, London, United Kingdom.
³⁶ Department of General Pediatrics, Pediatric Infectious Disease and Internal Medicine, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France, Paris Cité University, Paris, France; INSERM UMR 1137, Infection, Antimicrobials, Modelling, Evolution (IAME), Paris, France.

PMID: 39579868
DOI: 10.1016/j.jpeds.2024.114420

Free article

Multicenter Study

Surge of Pediatric Respiratory Tract Infections after the COVID-19 Pandemic and the Concept of "Immune Debt"

Lea Lenglart et al. J Pediatr. 2025 Sep.

Free article

. 2025 Sep:284:114420.

doi: 10.1016/j.jpeds.2024.114420. Epub 2024 Nov 22.

Authors

Collaborators

EPISODES Study Group:
Tobias Alfven, Vanda Anacleto, Orkun Aydin, Clarissa Barber, Elena Bellelli, Ron Berant, Thibault De Groc, Laszlo Fodor, Sara Geitoeira, Borja Gomez, Florian Hoffmann, Daniela Kohlfuerst, Mojca Kolnik, Franziska Leeb, Fiona Leonard, Mark Lyttle, Patrícia Mação, Lia Mano, Rosa Morello, Sofia Reis, Ruben Rocha, Katy Rose, Alexis Rybak, Petra Salamon, Francisca Saraiva, Matthias Schaffert, Keren Shahar-Nissan, Gabor Simon, Ines Silva Costa, Joao Sousa Marques, Carl Alessandro Starvaggi, Ozlem Teksam, Valtýr Stefánsson Thors, Jonas Thüminger, Caner Turan, Roberto Velasco, Corinne Vasilico, Anna Chiara Vittucci, Christoph Zurl

Affiliations

¹ Pediatric Emergency Department, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris Cité University, Paris, France. Electronic address: lea.lenglart@aphp.fr.
² Pediatric Emergency Department, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris Cité University, Paris, France; Paris Cité University, INSERM U1141, DHU Protect, Paris, France.
³ Pediatric Emergency Department, Heim Pal National Pediatric Institute, Budapest, Hungary.
⁴ Division of Pediatric Emergency Medicine, Department of Women's and Children's Health - University Hospital of Padova, Padova, Italy.
⁵ Department of Woman and Child Health and Public Health, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy.
⁶ Section of Pediatric Infectious Diseases, Faculty of Medicine, Department of Infectious Diseases, Imperial College London, London, United Kingdom.
⁷ Department of Child and Adolescent Health, Mater Dei Hospital, Msida, Malta.
⁸ Health Informatics Team, Division of Clinical Studies, Institute of Cancer Research, London, United Kingdom.
⁹ Division of Medicine, Department of Pediatric Emergency Medicine, St. Mary's Hospital, Imperial College NHS Healthcare Trust, London, United Kingdom; Faculty of Medicine, Center for Pediatrics and Child Health, Imperial College London, London, United Kingdom.
¹⁰ Department General Pediatrics, ErasmusMC - Sophia, Rotterdam, The Netherlands.
¹¹ Emergency Department & Trauma Center, Ospedale Pediatrico Meyer Firenze, Florence, Italy.
¹² SAPPHIRE Group, Health Sciences, Leicester University, Leicester, United Kingdom; Pediatric Emergency Medicine Leicester Academic (PEMLA) Group, Leicester Hospitals, Leicester, United Kingdom.
¹³ Pediatric Emergeny Department, Ondokuz Mayıs University, Samsun, Turkey.
¹⁴ Centro Hospitalar e Universitário de São João, University of Porto, Porto, Portugal.
¹⁵ Pediatric Emergency Department, Forndazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy; Department of Clinical Science and Community Health, University of Milan, Milan, Italy.
¹⁶ Paris Sorbonne University, Center de Recherche des Cordeliers, INSERM UMRS 1138, Paris, France.
¹⁷ Department of General Pediatrics, Pediatric Infectious Disease and Internal Medicine, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France, Paris Cité University, Paris, France.
¹⁸ Pediatric Emergency Department, Jean Verdier Hospital, Bondy, Assistance Publique-Hôpitaux de Paris, Sorbonne Paris cité, Paris, France; Institut National de la Santé et de la Recherche Médicale UMR 1123, ECEVE, Paris, France.
¹⁹ Pediatric Emergency Department, Children's Health Ireland at Crumlin, Dublin, Ireland; Women's and Children's Health, University College Dublin, Dublin, Ireland.
²⁰ Pediatric Emergency Department, Louis Mourier Hospital, Colombes, Assistance Publique-Hôpitaux de Paris, Université De Paris, Paris, France.
²¹ Department of Pediatrics, NoordWest Ziekenhuisgroep, Alkmaar, Netherlands.
²² Hospital Dona Estefania, Centro Hospitalar de Lisboa Central, Lisbon, Portugal.
²³ Association Clinique et Thérapeutique Infantile du Val-de-Marne (ACTIV), St Maur-des-Fossés, France; Center Hospitalier Intercommunal, Research Center, Université Paris Est, IMRB-GRC GEMINI, Créteil, France.
²⁴ Department of Pediatric Emergency Medicine, Children's Health Ireland at Tallaght, Baile Átha Cliath, Ireland.
²⁵ Pediatric Emergency Department, Children's Health Ireland at Temple Street, Dublin, Ireland.
²⁶ Pediatric Emergency Unit, Clinical Division of Pediatric Pulmonology, Allergology and Endocrinology, Department of Pediatrics and Adolescent Medicine, Medical University of Vienna, Vienna, Austria.
²⁷ Pediatric Emergency Department, Armand Trousseau Hospital, Assistance Publique-Hôpitaux de Paris, Sorbonne Université, CRESS Inserm U-1153 Paris, Epopé Team, Paris, France.
²⁸ Pediatric Intensive Care Unit and Emergency Department, Dr. von Hauner Children's Hospital, Ludwig-Maximilians-University Munich, Munich, Germany.
²⁹ Department of Pediatrics, Lithuanian University of Health Sciences, Kaunas, Lithuania.
³⁰ Paediatric Emergency Department, Kinderklinik Inselspital, Bern, Switzerland.
³¹ Departamento da Criança e do Jovem-Urgencia Pediatrica, Hospital Prof. Doutor Fernando da Fonseca, Amadora, Portugal.
³² Emergency Department, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.
³³ Paediatric Emergency Department, Children's Clinical University Hospital, Riga Stradins University, Riga, Latvia.
³⁴ Pediatric Emergency Department, Astrid Lindgrens Children's hospital, Karolinska University Hospital, Karolinska, Sweden.
³⁵ Section of Pediatric Infectious Diseases, Faculty of Medicine, Department of Infectious Diseases, Imperial College London, London, United Kingdom; Division of Medicine, Department of Pediatric Emergency Medicine, St. Mary's Hospital, Imperial College NHS Healthcare Trust, London, United Kingdom; Faculty of Medicine, Center for Pediatrics and Child Health, Imperial College London, London, United Kingdom.
³⁶ Department of General Pediatrics, Pediatric Infectious Disease and Internal Medicine, Robert Debré University Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France, Paris Cité University, Paris, France; INSERM UMR 1137, Infection, Antimicrobials, Modelling, Evolution (IAME), Paris, France.

PMID: 39579868
DOI: 10.1016/j.jpeds.2024.114420

Abstract

Objective: To investigate a dose-response relationship between the magnitude of decrease in pediatric respiratory tract infections (RTIs) during the 2020 implementation of nonpharmaceutical interventions (NPIs) and the increase thereafter during NPI lifting.

Study design: We conducted an interrupted, time-series analysis based on a multinational surveillance system. All patients <16 years of age coming to medical attention with various symptoms and signs of RTI at 25 pediatric emergency departments from 13 European countries between January 2018 and June 2022 were included. We used generalized additive models to correlate the magnitude of decrease of each RTI during NPI (such as social distancing) implementation and its subsequent increase during NPI lifting. Urinary tract infections served as control outcome.

Results: In total, 528 055 patients were included. We observed reductions in cases during the NPI period, from -76% (95% CI -113 to -53 in pneumonia) to -65% (95% CI -100 to -39 for tonsillitis/pharyngitis), followed by strong increases during NPI lifting, from +83% (95% CI 29-150 for tonsillitis/pharyngitis) to +329% (95% CI 149-517 for bronchiolitis). For each RTI, we found a significant association between the magnitude of decrease during NPI implementation and the increase during NPI lifting. Urinary tract infection cases remained stable.

Conclusions: The magnitude of increase in RTI observed after NPI lifting was directly correlated to the magnitude of case reduction during NPI implementation, suggesting a "dose-response" relationship from an "immune debt" phenomenon. The likely rebound in RTIs should be expected when implementing and lifting NPI in the future.

Keywords: COVID-19; nonpharmaceutical interventions; pediatrics; respiratory tract infection.

PubMed Disclaimer

Conflict of interest statement

Declaration of Competing Interest N.O. is supported by 2023 ATIP Avenir grant/INSERM and R.N. by the National Institute for Health and Care ResearchAcademic Clinical Lecturer (NIHR ACL) 2018-021-007 award. The other authors received no additional funding. N.O. reports travel grants from Pfizer, GSK, and Sanofi. No other authors have conflicts of interest to disclose.

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

LinkOut - more resources

Full Text Sources
Medical
- MedlinePlus Health Information

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Surge of Pediatric Respiratory Tract Infections after the COVID-19 Pandemic and the Concept of "Immune Debt"

Collaborators

Affiliations

Surge of Pediatric Respiratory Tract Infections after the COVID-19 Pandemic and the Concept of "Immune Debt"

Authors

Collaborators

Affiliations

Abstract

Conflict of interest statement

Publication types

MeSH terms

LinkOut - more resources

Full Text Sources

Medical