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Expert meeting report: towards a joint European roadmap to address the unmet needs and priorities of paediatric asthma patients on biologic therapy

Korneliusz Golebski, Lente H.M. Dankelman, Sofia Björkander, Klaus Bønnelykke, Paul Brinkman, Antoine Deschildre, Yoni E. van Dijk, Louise Fleming, Jonathan Grigg, Eckard Hamelmann, Simone Hashimoto, Michael Kabesch, Susanna Klevebro, Anke-Hilse Maitland-van der Zee, Simon K. Merid, Antonio Nieto, Jakob Niggel, Caroline Nilsson, Uroš Potočnik, Graham Roberts, Franca Rusconi, Sejal Saglani, Elisangela Valente, Cornelis van Drunen, Gang Wang, Erik Melén, Susanne J.H. Vijverberg
ERJ Open Research 2021 7: 00381-2021; DOI: 10.1183/23120541.00381-2021
Korneliusz Golebski
1Dept of Respiratory Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
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Lente H.M. Dankelman
1Dept of Respiratory Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
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Sofia Björkander
2Dept of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden
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Klaus Bønnelykke
3COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark
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Paul Brinkman
1Dept of Respiratory Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
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Antoine Deschildre
4CHU Lille, Pediatric Pulmonology and Allergy Unit, Hôpital Jeanne de Flandre, Université Nord de France, Lille, France
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Yoni E. van Dijk
1Dept of Respiratory Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
5Dept of Pediatric Pulmonology, Emma Children's Hospital, Amsterdam UMC, Amsterdam, The Netherlands
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Louise Fleming
6Paediatric Respiratory Medicine, National Heart and Lung Institute, Imperial College and Royal Brompton Harefield NHS Foundation Trust, London, UK
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Jonathan Grigg
7Centre for Paediatrics, Blizard Institute, Queen Mary, University of London, London, UK
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Eckard Hamelmann
8Klinik für Kinder and Jugendmedizin Kinderzentrum, Bethel Evangelisches Krankenhaus, Allergy Center, Ruhr University Bochum, Bielefeld, Germany
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Simone Hashimoto
1Dept of Respiratory Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
5Dept of Pediatric Pulmonology, Emma Children's Hospital, Amsterdam UMC, Amsterdam, The Netherlands
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Michael Kabesch
9Dept of Pediatric Pneumology and Allergy, University Children's Hospital Regensburg (KUNO) at the Hospital St Hedwig of the Order of St John and the University Hospital, University of Regensburg, Regensburg, Germany
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Susanna Klevebro
2Dept of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden
10Sachs’ Children and Youth Hospital, Södersjukhuset, Stockholm, Sweden
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Anke-Hilse Maitland-van der Zee
1Dept of Respiratory Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
5Dept of Pediatric Pulmonology, Emma Children's Hospital, Amsterdam UMC, Amsterdam, The Netherlands
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Simon K. Merid
2Dept of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden
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Antonio Nieto
11Children's Hospital La Fe, Pediatric Pulmonology and Allergy Unit, Instituto de Investigacion Sanitaria La Fe, Valencia, Spain
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Jakob Niggel
9Dept of Pediatric Pneumology and Allergy, University Children's Hospital Regensburg (KUNO) at the Hospital St Hedwig of the Order of St John and the University Hospital, University of Regensburg, Regensburg, Germany
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Caroline Nilsson
2Dept of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden
10Sachs’ Children and Youth Hospital, Södersjukhuset, Stockholm, Sweden
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Uroš Potočnik
12Center for Human Molecular Genetics and Pharmacogenomics, Faculty of Medicine, University of Maribor, Maribor, Slovenia
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Graham Roberts
13Department of Child Health, University of Southampton Hospital, Southampton, UK
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Franca Rusconi
14Epidemiology Unit, Meyer Children's University Hospital, Florence, Italy
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Sejal Saglani
6Paediatric Respiratory Medicine, National Heart and Lung Institute, Imperial College and Royal Brompton Harefield NHS Foundation Trust, London, UK
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Elisangela Valente
9Dept of Pediatric Pneumology and Allergy, University Children's Hospital Regensburg (KUNO) at the Hospital St Hedwig of the Order of St John and the University Hospital, University of Regensburg, Regensburg, Germany
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Cornelis van Drunen
15Department of Otorhinolaryngology, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
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Gang Wang
2Dept of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden
16Department of Integrated Traditional Chinese and Western Medicine, West China Hospital, Sichuan University, Sichuan, China
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Erik Melén
2Dept of Clinical Science and Education, Södersjukhuset, Karolinska Institutet, Stockholm, Sweden
10Sachs’ Children and Youth Hospital, Södersjukhuset, Stockholm, Sweden
17These authors contributed equally
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Susanne J.H. Vijverberg
1Dept of Respiratory Medicine, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands
5Dept of Pediatric Pulmonology, Emma Children's Hospital, Amsterdam UMC, Amsterdam, The Netherlands
17These authors contributed equally
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  • For correspondence: s.j.vijverberg@amsterdamumc.nl
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Abstract

A digital multidisciplinary European expert meeting took place on the 9 July 2020 to identify the unmet needs of paediatric severe asthma patients, and set the priorities for clinical and research activities ahead https://bit.ly/3CeLBHB

Biologics use in severe paediatric asthma

The global prevalence of severe asthma among adolescents ranges from 4% to 11%; and up to 7% of children with asthma display an uncontrolled and severe form that is often associated with a substantial burden on the quality of life of patients and their families, and increasing costs of healthcare [1, 2]. “Childhood asthma” is an umbrella term describing a heterogeneous disease comprising different phenotypes and a wide range of symptoms [3–5].

Despite decades of basic and clinical research, tailored strategies to modify the natural course of asthma, prevent severe exacerbations and inhibit lung function decline are still lacking. In addition, clinical phenotypes are only moderately reliable in the prediction of treatment responses and our current understanding of asthma endotypes is limited. Most asthma endotypes involve concomitant inflammatory pathways and distorted immune parameters. Advances in understanding severe paediatric asthma pathophysiological mechanisms and immunological pathways mediating the airway inflammation would allow better characterisation of these patients as well as optimised intervention, guided by treatable traits and biomarkers [6, 7].

Recent studies have demonstrated the effectiveness of monoclonal antibodies (mAbs), also known as biologics, targeting type 2 inflammation in controlling the symptoms of severe asthma. Currently, four human mAbs are approved for use in children: mAbs that target interleukin (IL)-5 or IL-5 receptor (R) (mepolizumab and benralizumab), mAbs that target IL-4R (dupilumab), and mAbs that target immunoglobulin E (omalizumab). Omalizumab was the first biologic approved to treat moderate-to-severe allergic asthma (≥6 years of age). Mepolizumab and dupilumab have been approved for severe eosinophilic asthma (≥6 and ≥12 years of age, respectively), while benralizumab has been approved in the USA to treat children (≥12 years of age) with severe eosinophilic asthma [8–13].

The introduction of mAb agents in asthma treatment is a milestone in the application of personalised medicine. However, comparative studies and standardised algorithms for the management of paediatric severe asthma to guide the best therapeutic option for paediatric patients with severe asthma are lacking [14]. More personalised medicine approaches may benefit the patient by better matching patients with the most appropriate therapy. Risk stratification, remote monitoring and the integration of multiple data sources could help tailor management for the individual child with severe asthma.

A digital multidisciplinary European expert meeting took place on 9 July 2020. In this workshop, we brought together European respiratory/allergy paediatricians, immunologists, epidemiologists and basic scientists to identify the unmet needs of paediatric severe asthma patients, and set the priorities for clinical and research activities ahead. The participants discussed ongoing initiatives and knowledge gaps, and formulated proposals on how to address these challenges. In this report, we describe the main findings of this expert meeting.

Current knowledge gaps and challenges

Except for omalizumab, a major constraint to the optimal and consistent use of biologics in paediatric severe asthmatic is the limited evidence regarding the safety and efficacy of biologics in children [15, 16] (table S1). This especially holds true for biologics that entered the market recently. In the large phase 3 trials of these treatments, children were underrepresented and constituted only 1–6% of included patients [10, 17–20]. Although it might be challenging to recruit paediatric patients, assessing efficacy and safety in this population is essential since their immune system is under development and asthma progression is related to age and sex [21]. Studies that assessed the safety of omalizumab or mepolizumab in severe asthmatic children after 52 weeks of treatment did not observe any treatment-related severe adverse events [9, 22] but potential long-term effects remain unclear. Furthermore, the mepolizumab studies included very few children and adolescents. Finally, there are, to date, no data on biologics in the preschool-age severe asthma. How these treatments might impact underlying disease mechanisms is only partly clear and potential disease-modifying effects are not well understood. Since these expensive drugs may require lifelong administration [23], careful consideration is needed to assess which child is eligible for which biologic. A better understanding of paediatric asthma endotypes that can evolve over time might also lead to novel insights into whether biologics that previously showed no efficacy in adults could still be promising candidates for children [24].

The American Thoracic Society and the European Respiratory Society (ERS) define severe asthma as asthma that requires treatment with high-dose inhaled corticosteroids plus a second controller (and/or systemic corticosteroids) to prevent it from becoming “uncontrolled” or “which remains uncontrolled despite this therapy” [25]. Application of adult definitions and treatment guidelines may not always be appropriate; children with severe asthma have more atopy, less airflow limitation and less association with obesity [26]. The lack of clear definitions of “paediatric severe asthma” and “treatment response” were also identified as important hurdles. Moreover, there is an urgent need to formulate a definition of severe preschool asthma/wheeze. A consensus is needed both for research on biologics in the paediatric population as well as for uniform clinical management across Europe, in accordance with the Paediatric Investigational Plans of the European Medicines Agency. Moreover, the lack of research funding for paediatric studies on biologics and lack of scientific collaboration with other inflammatory disease areas where biologics have been applied in the paediatric population were identified as important challenges.

Lastly, the COVID-19 era has led to significant changes in how healthcare is accessed and provided [27]. This brings new challenges, as well as opportunities, for the management of children on biologics. There is now a stronger focus on remote care and monitoring, on the use and development of digital tools that might help with this, and on possible home administration of biologics. Self- or caregiver-administered injections make it possible for patients that live further away from a clinic to receive treatment more consistently, but also requires proper training, as well as careful remote monitoring for complications and to ensure good adherence [28].

Ongoing initiatives: bringing European experts together

The high socioeconomic burden of uncontrolled disease, and the lack of clear indicators for treatment choice and responses to administrated treatment, especially for biologics, underline the need for better characterisation of paediatric asthma phenotypes/endotypes and novel therapeutic options. Several ongoing studies and initiatives within European consortia address those needs (table S2). Hurdles in recruitment and underrepresentation of children in severe asthma studies provide an urgent need for collaborative efforts between European medical centres. Therefore, bringing together the data that are already available from existing consortia may be the first step towards more efficient characterisation of the disease and treatment options. Pan-European standardisation of inclusion and exclusion criteria for study participants and operating protocols, as well as an agreement on sample and data collection, would further provide better validity of outcomes and enable access to large biobanks.

There was consensus on the need for new collaborative trials, real-life cohorts and in vitro pre-clinical models with standardised protocols on applicable paediatric antiasthmatic drugs. An urgent update and uniformisation of treatment guidelines that take into account switching from one biologic to another, compatibility of more than one biologic, dose adjustment and long-term (side-)effects of these therapies was considered essential. This requires a development of specific paediatric tools for evaluating severity, level of control and response to treatment, and as well as data harmonisation.

Identified research priorities

Seven priority research areas were identified: 1) early identification of young asthma patients, including preschoolers, with a high risk of progression to severe disease; 2) exploring molecular mechanisms underlying poor response to treatment; 3) prediction of response to biologics; 4) understanding mechanistic differences underlying paediatric and adult severe asthma phenotypes; 5) long-term efficacy and safety; 6) understanding patient and caregiver perspectives on biologics use; and 7) harmonising (access to) biologics for asthmatic children treatment across Europe (table 1).

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TABLE 1

Identified research priorities

The early identification of asthmatic children at greatest risk of progression to severe disease requires longitudinal follow-up combined with in-depth pheno-endotyping [29]. Since various European initiatives are ongoing in this area, connecting different paediatric initiatives was identified as an important next step, in addition to linking with other ERS Clinical Research Collaborations with an adult focus, such as SHARP (focusing on severe asthma in adults) [30] and CADSET (focusing on lung function trajectories).

To predict which patients will respond to which biologics, ideally, comparative crossover clinical trials are needed. However, these kinds of trials are likely to be very challenging. Pragmatic and noninferiority trials, such as the recently initiated TREAT trial in the UK, which aims to compare the efficacy of mepolizumab versus omalizumab in reducing asthma attacks in children, might be more feasible [31]. Real-life efficacy data, combined with prospectively collected biomarkers, have the potential to provide additional valuable information [32, 33]. International and multidisciplinary collaboration is critical to reaching a consensus on response definitions (as is currently ongoing with the 3TR consortium), to recruit enough patients and to harmonise research protocols.

Understanding molecular mechanisms and immunological pathways are essential for the assessment of biomarker candidates for treatment response as well as an acceleration of the development of novel therapeutics. Successful modern research collaborations increasingly include scientists and clinicians of different expertise. Today, ex vivo translational models, including monolayer cultures, coculture systems or organ-on-chip lung models, provide an unprecedented opportunity to study in vitro effects of promising drugs. Introduction of novel technologies, i.e. single-cell sequencing or CRISPR-Cas9, enable a functional validation of potential biomarkers predicted by genome-wide association studies in ex vivo airway cell/tissue models [34, 35].

Knowledge as to which asthmatic patients progress into severe adult asthma is lacking, although risk factors like atopy, multiple allergic comorbidities, impaired lung function, obesity and environmental exposures are well-described [29]. Severe disease may differ substantially between children and adults. For example, blood eosinophils or airway eosinophils might not equal T2 inflammation in children, while they often do in adults [36]. Upcoming results from initiatives and consortia such as VIRASTHMA2, COBRAPed, UBIOPRED paediatric cohorts and SysPharmPediA might be able to shed more light on paediatric endotypes of severe disease.

The patient and caregiver perspectives must also be heard, as beliefs about treatment are known to influence treatment satisfaction and adherence [37]. Qualitative studies and active collaborations between researchers and patient representatives [38, 39] are needed to address the needs and beliefs of patients and their caregivers. A young patient working group, as currently being established within 3TR, is a great first step to including the patients’ voice in treatment considerations.

Next steps

Collaboration is essential to address the unmet clinical needs and priorities of paediatric severe asthma patients. Joining forces will help bring the field forward and pave the way for a new joint effort to optimise treatment for this vulnerable patient population. This requires a broad engagement to represent all stakeholders and involvement of national respiratory societies and patients to ensure optimal implementation of the research findings into clinical practice. As such, we aim to establish a European working group on joint research and clinical protocols, establish a common European database for paediatric asthma patients, and obtain research funding together. Discussions are ongoing, and we are now reaching out to clinicians, scientists, technology, regulators, healthcare providers and, most importantly, patients into collaborative efforts. This initiative is open for new collaborators to help lead the way for precision medicine of severe paediatric asthma.

Supplementary material

Supplementary Material

Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

Supplementary tables 00381-2021.supplement

Footnotes

  • Provenance: Submitted article, peer reviewed.

  • This article has supplementary material available from openres.ersjournals.com

  • Conflict of interest: K. Golebski received funds from STIMAG and from the Amsterdam Infection & Immunity Institute.

  • Conflict of interest: L.H.M. Dankelman has nothing to disclose.

  • Conflict of interest: S. Björkander has nothing to disclose.

  • Conflict of interest: K. Bønnelykke has nothing to disclose.

  • Conflict of interest: P. Brinkman has nothing to disclose.

  • Conflict of interest: A. Deschildre has nothing to disclose.

  • Conflict of interest: Y.E. van Dijk has nothing to disclose.

  • Conflict of interest: L. Fleming reports grants from Asthma UK, and speakers fees or fees for expert consultation from Teva, AstraZeneca, Sanofi, Respiri and Novartis; all fees paid directly to her institution and outside the submitted work.

  • Conflict of interest: J. Grigg reports personal fees from GSK, AstraZeneca and Novartis during the conduct of the study.

  • Conflict of interest: E. Hamelmann has nothing to disclose.

  • Conflict of interest: S. Hashimoto has nothing to disclose.

  • Conflict of interest: M. Kabesch has nothing to disclose.

  • Conflict of interest: S. Klevebro has nothing to disclose.

  • Conflict of interest: A-H. Maitland-van der Zee has received research grants outside the submitted work from GSK, Boehringer Ingelheim and Vertex; she is the principal investigator of a P4O2 (Precision Medicine for more Oxygen) public–private partnership sponsored by Health Holland involving many private partners that contribute in cash and/or in kind (Boehringer Ingelheim, Breathomix, Fluidda, Ortec Logiqcare, Philips, Quantib-U, Smartfish, SODAQ, Thirona, TopMD and Novartis); and she has served in advisory boards for AstraZeneca, GSK and Boehringer Ingelheim with money paid to her institution.

  • Conflict of interest: S.K. Merid has nothing to disclose.

  • Conflict of interest: A. Nieto reports grants and personal fees from Novartis outside the submitted work.

  • Conflict of interest: J. Niggel has nothing to disclose.

  • Conflict of interest: C. Nilsson has nothing to disclose.

  • Conflict of interest: U. Potocnik reports grants from the Ministry of Education, Science and Sport.

  • Conflict of interest: G. Roberts reports grants from the EU during the conduct of the study.

  • Conflict of interest: F. Rusconi has nothing to disclose.

  • Conflict of interest: S. Saglani has nothing to disclose.

  • Conflict of interest: E. Valente has nothing to disclose.

  • Conflict of interest: C. van Drunen has nothing to disclose.

  • Conflict of interest: G. Wang has nothing to disclose.

  • Conflict of interest: E. Melén reports personal fees from AstraZeneca, Chiesi, Novartis and Sanofi (advisory board activities) outside the submitted work.

  • Conflict of interest: S.J.H. Vijverberg reports grants from ZonMW during the conduct of the study.

  • Support statement: The PERMEABLE consortium is supported by ZonMW (project number: 456008004), the Swedish Research Council (project number 2018-05619), the Ministry of Education, Science and Sport of the Republic of Slovenia (contract number C3330-19-252012), and the German Ministry of Education and Research (BMBF) (project number FKZ01KU1909A), under the frame of the ERA PerMed JTC 2018 Call. Funding information for this article has been deposited with the Crossref Funder Registry.

  • Received June 7, 2021.
  • Accepted July 28, 2021.
  • Copyright ©The authors 2021
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Expert meeting report: towards a joint European roadmap to address the unmet needs and priorities of paediatric asthma patients on biologic therapy
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Expert meeting report: towards a joint European roadmap to address the unmet needs and priorities of paediatric asthma patients on biologic therapy
Korneliusz Golebski, Lente H.M. Dankelman, Sofia Björkander, Klaus Bønnelykke, Paul Brinkman, Antoine Deschildre, Yoni E. van Dijk, Louise Fleming, Jonathan Grigg, Eckard Hamelmann, Simone Hashimoto, Michael Kabesch, Susanna Klevebro, Anke-Hilse Maitland-van der Zee, Simon K. Merid, Antonio Nieto, Jakob Niggel, Caroline Nilsson, Uroš Potočnik, Graham Roberts, Franca Rusconi, Sejal Saglani, Elisangela Valente, Cornelis van Drunen, Gang Wang, Erik Melén, Susanne J.H. Vijverberg
ERJ Open Research Oct 2021, 7 (4) 00381-2021; DOI: 10.1183/23120541.00381-2021

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Expert meeting report: towards a joint European roadmap to address the unmet needs and priorities of paediatric asthma patients on biologic therapy
Korneliusz Golebski, Lente H.M. Dankelman, Sofia Björkander, Klaus Bønnelykke, Paul Brinkman, Antoine Deschildre, Yoni E. van Dijk, Louise Fleming, Jonathan Grigg, Eckard Hamelmann, Simone Hashimoto, Michael Kabesch, Susanna Klevebro, Anke-Hilse Maitland-van der Zee, Simon K. Merid, Antonio Nieto, Jakob Niggel, Caroline Nilsson, Uroš Potočnik, Graham Roberts, Franca Rusconi, Sejal Saglani, Elisangela Valente, Cornelis van Drunen, Gang Wang, Erik Melén, Susanne J.H. Vijverberg
ERJ Open Research Oct 2021, 7 (4) 00381-2021; DOI: 10.1183/23120541.00381-2021
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  • Article
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    • Biologics use in severe paediatric asthma
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