Core outcome measurement set for research and clinical practice in post-COVID-19 condition (long COVID) in children and young people: an international Delphi consensus study "PC-COS Children"

doi:10.1183/13993003.01761-2023

Review

. 2024 Mar 14;63(3):2301761.

doi: 10.1183/13993003.01761-2023. Print 2024 Mar.

Core outcome measurement set for research and clinical practice in post-COVID-19 condition (long COVID) in children and young people: an international Delphi consensus study "PC-COS Children"

Nina Seylanova^{1

2}, Anastasia Chernyavskaya^{3

4

2}, Natalia Degtyareva⁵, Aigun Mursalova⁶, Ali Ajam⁶, Lin Xiao⁶, Khazhar Aktulaeva⁶, Philipp Roshchin⁶, Polina Bobkova⁶, Olalekan Lee Aiyegbusi⁶, Anbarasu Theodore Anbu⁷, Christian Apfelbacher⁸, Ali Akbar Asadi-Pooya^{9

10}, Liat Ashkenazi-Hoffnung¹¹, Caroline Brackel^{12

13}, Danilo Buonsenso^{14

15}, Wouter de Groote¹⁶, Janet V Diaz¹⁷, Daniele Dona¹⁷, Audrey Dunn Galvin¹⁸, Jon Genuneit¹⁹, Helen Goss²⁰, Sarah E Hughes²¹, Christina J Jones²², Krutika Kuppalli¹⁷, Laura A Malone^{23

24}, Sammie McFarland²¹, Dale M Needham^{25

26

27}, Nikita Nekliudov²⁸, Timothy R Nicholson²⁹, Carlos R Oliveira^{30

31

32}, Nicoline Schiess³³, Terry Y Segal³⁴, Louise Sigfrid³⁵, Claire Thorne³⁶, Susanne Vijverberg³⁷, John O Warner³⁸, Wilson Milton Were¹⁷, Paula R Williamson³⁹, Daniel Munblit^{40

41

42

2}; PC-COS Children Study Group

Collaborators, Affiliations

Collaborators

PC-COS Children Study Group:
Asiah Kassim, Jennifer R Chevinsky, Karen Choong, Rae Duncan, Susanna Esposito, Rebecca Foster, Alla Guekht, Allison Jaure, Carrie Mackenzie, Vivienne Matthies-Bonn, Karen Matvienko-Sikar, Lorraine McCloud, Donna C McParland, Victor Daniel Miron, Srinivas Murthy, Sarah O Connel, Margaret O'Hara, Anna Ogonowska-Slodownik, Jana Pavare, Paula Robertson, Jeremy Rossman, Oana Săndulescu, Sharon H Saydah, Jochen Schmitt, Malcolm Calum G Semple, Roz Shafran, Ausra Snipaitiene, Arne Søraas, Terence Stephenson, Lola Tulen, Gonzalo Valenzuela Galaz, David Vickers, Daniel Christian Vilser, Michaela Waak, Julie Wells, Elizabeth Whittaker, Michelle Winer, Alan Asmanov, Pasquale Comberiati

Affiliations

¹ Independent researcher, London, UK.
² Authors contributed equally to the study; apart from the two joint first authors, who contributed equally, the primary study team members and the last author, authors are listed in alphabetical order.
³ Department of Paediatrics and Paediatric Rheumatology, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia.
⁴ National Medical Research Center for Children's Health, Moscow, Russia.
⁵ Department of Paediatrics and Paediatric Infectious Diseases, Institute of Child's Health, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia.
⁶ University of Birmingham, Birmingham, UK.
⁷ Alder Hey Children's NHS Foundation Trust, Liverpool, UK.
⁸ University of Magdeburg, Magdeburg, Germany.
⁹ Epilepsy Research Center, Shiraz University of Medical Sciences, Shiraz, Iran.
¹⁰ Jefferson Comprehensive Epilepsy Center, Thomas Jefferson University, Philadelphia, PA, USA.
¹¹ Schneider Children's Medical Center of Israel, Petah Tikva, Israel.
¹² Department of Paediatric Pulmonology, Emma Children's Hospital, Amsterdam University Medical Centers, Amsterdam, The Netherlands.
¹³ Department of Pediatrics, Tergooi Hospital, Blaricum, The Netherlands.
¹⁴ Center for Global Health Research and Studies, Università Cattolica del Sacro Cuore, Rome, Italy.
¹⁵ Department of Woman and Child Health and Public Health, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy.
¹⁶ World Health Organization, Geneva, Switzerland.
¹⁷ Department for Women's and Children's Health, University of Padua, Padua, Italy.
¹⁸ University of Cork, Cork, Ireland.
¹⁹ Pediatric Epidemiology, Department of Pediatrics, Medical Faculty, Leipzig University, Leipzig, Germany.
²⁰ Long Covid Kids Charity, Salisbury, UK.
²¹ Institute of Applied Health Research, University of Birmingham, Birmingham, UK.
²² School of Psychology, University of Surrey, Guildford, UK.
²³ Kennedy Krieger Institute, Baltimore, MD, USA.
²⁴ Departments of Neurology and Physical Medicine and Rehabilitation, Johns Hopkins University, Baltimore, MD, USA.
²⁵ Outcomes After Critical Illness and Surgery (OACIS) Research Group, Johns Hopkins University, Baltimore, MD, USA.
²⁶ Pulmonary and Critical Care Medicine, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²⁷ Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²⁸ Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA.
²⁹ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
³⁰ Yale University School of Medicine, Department of Pediatrics, Section of Infectious Diseases, New Haven, CT, USA.
³¹ Yale University School of Public Health, Department of Biostatistics, Division of Health Informatics, New Haven, CT, USA.
³² Yale New Haven Children's Hospital, New Haven, CT, USA.
³³ Brain Health Unit, Mental Health and Substance Use Department, World Health Organization, Geneva, Switzerland.
³⁴ University College London Hospitals NHS Foundation Trust, London, UK.
³⁵ ISARIC Global Support Centre, Centre for Tropical Medicine and Global Health, University of Oxford, Oxford, UK.
³⁶ Population, Policy and Practice Research and Teaching Dept, University College London GOS Institute of Child Health, London, UK.
³⁷ Amsterdam University Medical Centers, Amsterdam, The Netherlands.
³⁸ Imperial College London, London, UK.
³⁹ MRC-NIHR Trials Methodology Research Partnership, Department of Health Data Science, University of Liverpool, Liverpool, UK.
⁴⁰ Department of Paediatrics and Paediatric Infectious Diseases, Institute of Child's Health, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia daniel.munblit@kcl.ac.uk.
⁴¹ Division of Care in Long Term Conditions, Florence Nightingale Faculty of Nursing, Midwifery and Palliative Care, King's College London, London, UK.
⁴² Research and Clinical Center for Neuropsychiatry, Moscow, Russia.

PMID: 38359962
PMCID: PMC10938351
DOI: 10.1183/13993003.01761-2023

Review

Core outcome measurement set for research and clinical practice in post-COVID-19 condition (long COVID) in children and young people: an international Delphi consensus study "PC-COS Children"

Nina Seylanova et al. Eur Respir J. 2024.

. 2024 Mar 14;63(3):2301761.

doi: 10.1183/13993003.01761-2023. Print 2024 Mar.

Authors

Collaborators

PC-COS Children Study Group:
Asiah Kassim, Jennifer R Chevinsky, Karen Choong, Rae Duncan, Susanna Esposito, Rebecca Foster, Alla Guekht, Allison Jaure, Carrie Mackenzie, Vivienne Matthies-Bonn, Karen Matvienko-Sikar, Lorraine McCloud, Donna C McParland, Victor Daniel Miron, Srinivas Murthy, Sarah O Connel, Margaret O'Hara, Anna Ogonowska-Slodownik, Jana Pavare, Paula Robertson, Jeremy Rossman, Oana Săndulescu, Sharon H Saydah, Jochen Schmitt, Malcolm Calum G Semple, Roz Shafran, Ausra Snipaitiene, Arne Søraas, Terence Stephenson, Lola Tulen, Gonzalo Valenzuela Galaz, David Vickers, Daniel Christian Vilser, Michaela Waak, Julie Wells, Elizabeth Whittaker, Michelle Winer, Alan Asmanov, Pasquale Comberiati

Affiliations

¹ Independent researcher, London, UK.
² Authors contributed equally to the study; apart from the two joint first authors, who contributed equally, the primary study team members and the last author, authors are listed in alphabetical order.
³ Department of Paediatrics and Paediatric Rheumatology, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia.
⁴ National Medical Research Center for Children's Health, Moscow, Russia.
⁵ Department of Paediatrics and Paediatric Infectious Diseases, Institute of Child's Health, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia.
⁶ University of Birmingham, Birmingham, UK.
⁷ Alder Hey Children's NHS Foundation Trust, Liverpool, UK.
⁸ University of Magdeburg, Magdeburg, Germany.
⁹ Epilepsy Research Center, Shiraz University of Medical Sciences, Shiraz, Iran.
¹⁰ Jefferson Comprehensive Epilepsy Center, Thomas Jefferson University, Philadelphia, PA, USA.
¹¹ Schneider Children's Medical Center of Israel, Petah Tikva, Israel.
¹² Department of Paediatric Pulmonology, Emma Children's Hospital, Amsterdam University Medical Centers, Amsterdam, The Netherlands.
¹³ Department of Pediatrics, Tergooi Hospital, Blaricum, The Netherlands.
¹⁴ Center for Global Health Research and Studies, Università Cattolica del Sacro Cuore, Rome, Italy.
¹⁵ Department of Woman and Child Health and Public Health, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy.
¹⁶ World Health Organization, Geneva, Switzerland.
¹⁷ Department for Women's and Children's Health, University of Padua, Padua, Italy.
¹⁸ University of Cork, Cork, Ireland.
¹⁹ Pediatric Epidemiology, Department of Pediatrics, Medical Faculty, Leipzig University, Leipzig, Germany.
²⁰ Long Covid Kids Charity, Salisbury, UK.
²¹ Institute of Applied Health Research, University of Birmingham, Birmingham, UK.
²² School of Psychology, University of Surrey, Guildford, UK.
²³ Kennedy Krieger Institute, Baltimore, MD, USA.
²⁴ Departments of Neurology and Physical Medicine and Rehabilitation, Johns Hopkins University, Baltimore, MD, USA.
²⁵ Outcomes After Critical Illness and Surgery (OACIS) Research Group, Johns Hopkins University, Baltimore, MD, USA.
²⁶ Pulmonary and Critical Care Medicine, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²⁷ Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
²⁸ Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA.
²⁹ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
³⁰ Yale University School of Medicine, Department of Pediatrics, Section of Infectious Diseases, New Haven, CT, USA.
³¹ Yale University School of Public Health, Department of Biostatistics, Division of Health Informatics, New Haven, CT, USA.
³² Yale New Haven Children's Hospital, New Haven, CT, USA.
³³ Brain Health Unit, Mental Health and Substance Use Department, World Health Organization, Geneva, Switzerland.
³⁴ University College London Hospitals NHS Foundation Trust, London, UK.
³⁵ ISARIC Global Support Centre, Centre for Tropical Medicine and Global Health, University of Oxford, Oxford, UK.
³⁶ Population, Policy and Practice Research and Teaching Dept, University College London GOS Institute of Child Health, London, UK.
³⁷ Amsterdam University Medical Centers, Amsterdam, The Netherlands.
³⁸ Imperial College London, London, UK.
³⁹ MRC-NIHR Trials Methodology Research Partnership, Department of Health Data Science, University of Liverpool, Liverpool, UK.
⁴⁰ Department of Paediatrics and Paediatric Infectious Diseases, Institute of Child's Health, Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia daniel.munblit@kcl.ac.uk.
⁴¹ Division of Care in Long Term Conditions, Florence Nightingale Faculty of Nursing, Midwifery and Palliative Care, King's College London, London, UK.
⁴² Research and Clinical Center for Neuropsychiatry, Moscow, Russia.

PMID: 38359962
PMCID: PMC10938351
DOI: 10.1183/13993003.01761-2023

Abstract

The coronavirus disease 2019 (COVID-19) pandemic substantially impacted different age groups, with children and young people not exempted. Many have experienced enduring health consequences. Presently, there is no consensus on the health outcomes to assess in children and young people with post-COVID-19 condition. Furthermore, it is unclear which measurement instruments are appropriate for use in research and clinical management of children and young people with post-COVID-19. To address these unmet needs, we conducted a consensus study, aiming to develop a core outcome set (COS) and an associated core outcome measurement set (COMS) for evaluating post-COVID-19 condition in children and young people. Our methodology comprised of two phases. In phase 1 (to create a COS), we performed an extensive literature review and categorisation of outcomes, and prioritised those outcomes in a two-round online modified Delphi process followed by a consensus meeting. In phase 2 (to create the COMS), we performed another modified Delphi consensus process to evaluate measurement instruments for previously defined core outcomes from phase 1, followed by an online consensus workshop to finalise recommendations regarding the most appropriate instruments for each core outcome. In phase 1, 214 participants from 37 countries participated, with 154 (72%) contributing to both Delphi rounds. The subsequent online consensus meeting resulted in a final COS which encompassed seven critical outcomes: fatigue; post-exertion symptoms; work/occupational and study changes; as well as functional changes, symptoms, and conditions relating to cardiovascular, neuro-cognitive, gastrointestinal and physical outcomes. In phase 2, 11 international experts were involved in a modified Delphi process, selecting measurement instruments for a subsequent online consensus workshop where 30 voting participants discussed and independently scored the selected instruments. As a result of this consensus process, four instruments met a priori consensus criteria for inclusion: PedsQL multidimensional fatigue scale for "fatigue"; PedsQL gastrointestinal symptom scales for "gastrointestinal"; PedsQL cognitive functioning scale for "neurocognitive" and EQ-5D for "physical functioning". Despite proposing outcome measurement instruments for the remaining three core outcomes ("cardiovascular", "post-exertional malaise", "work/occupational and study changes"), a consensus was not achieved. Our international, consensus-based initiative presents a robust framework for evaluating post-COVID-19 condition in children and young people in research and clinical practice via a rigorously defined COS and associated COMS. It will aid in the uniform measurement and reporting of relevant health outcomes worldwide.

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Conflict of interest statement

Conflict of interest: D. Munblit is a Co-Chair of International Severe Acute Respiratory and Emerging Infection Consortium (ISARIC) Global Paediatric Long COVID Working Group, member of ISARIC working group on long-term follow-up in adults. C. Apfelbacher reports grants or contracts from Dr Wolff Group, Bionorica and The European Cooperation in Science and Technology (COST); he also acknowledges consulting fees from the Dr Wolff Group, Bionorica, Sanofi and LEO Pharma; he serves as a Co-Chair Harmonising Outcome Measures for Eczema (HOME) initiative and is Co-Chair of the Hand Eczema Core Outcome Set (HECOS) initiative and is core principal investigator of the KUNOKids Health Study (Regensburg, Germany). J.V. Diaz is the lead of the clinical management response pillar for COVID-19 and in that capacity convenes the WHO Clinical Characterization and Management Research working group; the Post COVID-19 COS steering committee was a sub-working group of this bigger group. O.L. Aiyegbusi has received research grants from UCB, Kidney Research UK, Gilead Sciences Ltd, The Health Foundation, NIHR Birmingham BRC, NIHR ARC, NIHR BTRU, Innovate UK, Merck, GSK, Anthony Nolan and Sarcoma UK; he has also received personal fees from GSK, Gilead Sciences, Innovate UK and Merck. C.R. Oliveira receives grant support from the National Institutes of Health (NIH), grant numbers OT2HL161847 and K23AI159518. P.R. Williamson is chair of the Core Outcome Measures in Effectiveness Trials (COMET) Management Group. Other authors declare that they have no competing interests.

Figures

**FIGURE 1**
Overview of the core outcome set (COS) and core outcome measurement set (COMS) development process.

**FIGURE 2**
Core outcome measurement set (COMS) for post-coronavirus disease 2019 (COVID-19) condition in children and young people. Green indicates core outcomes and instruments reaching consensus for use in relation to a particular outcome; blue indicates instruments not reaching consensus, with more than a half of consensus meeting participants voting for this instrument prioritisation; brown indicates instruments not reaching consensus, with less than a half of consensus meeting participants voting for this instrument prioritisation. COS: core outcome set; SBQ: Symptom Burden Questionnaire; CDC: Centers for Disease Control and Prevention; CFS: chronic fatigue syndrome; PEM: post-exertional malaise; WHODAS: World Health Organization Disability Assessment Schedule.

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References

1. Munblit D, O'Hara ME, Akrami A, et al. . Long COVID: aiming for a consensus. Lancet Respir Med 2022; 10: 632–634. 10.1016/S2213-2600(22)00135-7 - DOI - PMC - PubMed
1. Lopez-Leon S, Wegman-Ostrosky T, Ayuzo Del Valle NC, et al. . Long-COVID in children and adolescents: a systematic review and meta-analyses. Sci Rep 2022; 12: 9950. doi:10.1038/s41598-022-13495-5 - DOI - PMC - PubMed
1. Zimmermann P, Pittet LF, Curtis N. How common is long COVID in children and adolescents? Pediatr Infect Dis J 2021; 40: e482–e487. doi:10.1097/INF.0000000000003328 - DOI - PMC - PubMed
1. Global Burden of Disease Long COVID Collaborators , Wulf Hanson S, Abbafati C, et al. . Estimated global proportions of individuals with persistent fatigue, cognitive, and respiratory symptom clusters following symptomatic COVID-19 in 2020 and 2021. JAMA 2022; 328: 1604–1615. doi:10.1001/jama.2022.18931 - DOI - PMC - PubMed
1. Rea M, Pawelek P, Ayoubkhani D. Prevalence of Ongoing Symptoms Following Coronavirus (COVID-19) Infection in the UK. 2023. www.ons.gov.uk/peoplepopulationandcommunity/healthandsocialcare/conditio.... Date last accessed: 17 September 2023. Date last updated: 30 March 2023.

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[1] Munblit D, O'Hara ME, Akrami A, et al. . Long COVID: aiming for a consensus. Lancet Respir Med 2022; 10: 632–634. 10.1016/S2213-2600(22)00135-7 - DOI - PMC - PubMed

[2] Munblit D, O'Hara ME, Akrami A, et al. . Long COVID: aiming for a consensus. Lancet Respir Med 2022; 10: 632–634. 10.1016/S2213-2600(22)00135-7 - DOI - PMC - PubMed

[3] Lopez-Leon S, Wegman-Ostrosky T, Ayuzo Del Valle NC, et al. . Long-COVID in children and adolescents: a systematic review and meta-analyses. Sci Rep 2022; 12: 9950. doi:10.1038/s41598-022-13495-5 - DOI - PMC - PubMed

[4] Lopez-Leon S, Wegman-Ostrosky T, Ayuzo Del Valle NC, et al. . Long-COVID in children and adolescents: a systematic review and meta-analyses. Sci Rep 2022; 12: 9950. doi:10.1038/s41598-022-13495-5 - DOI - PMC - PubMed

[5] Zimmermann P, Pittet LF, Curtis N. How common is long COVID in children and adolescents? Pediatr Infect Dis J 2021; 40: e482–e487. doi:10.1097/INF.0000000000003328 - DOI - PMC - PubMed

[6] Zimmermann P, Pittet LF, Curtis N. How common is long COVID in children and adolescents? Pediatr Infect Dis J 2021; 40: e482–e487. doi:10.1097/INF.0000000000003328 - DOI - PMC - PubMed

[7] Global Burden of Disease Long COVID Collaborators , Wulf Hanson S, Abbafati C, et al. . Estimated global proportions of individuals with persistent fatigue, cognitive, and respiratory symptom clusters following symptomatic COVID-19 in 2020 and 2021. JAMA 2022; 328: 1604–1615. doi:10.1001/jama.2022.18931 - DOI - PMC - PubMed

[8] Global Burden of Disease Long COVID Collaborators , Wulf Hanson S, Abbafati C, et al. . Estimated global proportions of individuals with persistent fatigue, cognitive, and respiratory symptom clusters following symptomatic COVID-19 in 2020 and 2021. JAMA 2022; 328: 1604–1615. doi:10.1001/jama.2022.18931 - DOI - PMC - PubMed

[9] Rea M, Pawelek P, Ayoubkhani D. Prevalence of Ongoing Symptoms Following Coronavirus (COVID-19) Infection in the UK. 2023. www.ons.gov.uk/peoplepopulationandcommunity/healthandsocialcare/conditio.... Date last accessed: 17 September 2023. Date last updated: 30 March 2023.

[10] Rea M, Pawelek P, Ayoubkhani D. Prevalence of Ongoing Symptoms Following Coronavirus (COVID-19) Infection in the UK. 2023. www.ons.gov.uk/peoplepopulationandcommunity/healthandsocialcare/conditio.... Date last accessed: 17 September 2023. Date last updated: 30 March 2023.

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Core outcome measurement set for research and clinical practice in post-COVID-19 condition (long COVID) in children and young people: an international Delphi consensus study "PC-COS Children"

Collaborators

Affiliations

Core outcome measurement set for research and clinical practice in post-COVID-19 condition (long COVID) in children and young people: an international Delphi consensus study "PC-COS Children"

Authors

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Abstract

Conflict of interest statement

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