Multi-ancestry genome-wide association study of asthma exacerbations

Esther Herrera-Luis, Victor E. Ortega, U-BIOPRED Study Group, Elizabeth J. Ampleford, Yang Yie Sio, Raquel Granell, Emmely de Roos, Natalie Terzikhan, Ernesto Elorduy Vergara, Natalia Hernandez-Pacheco, Javier Perez-Garcia, Elena Martin-Gonzalez, Fabian Lorenzo-Diaz, Simone Hashimoto, Paul Brinkman, Andrea L. Jorgensen, Qi Yan, Erick Forno, Susanne J. Vijverberg, Ryan LethemAntonio Espuela-Ortiz, Mario Gorenjak, Celeste Eng, Ruperto González-Pérez, José M. Hernández-Pérez, Paloma Poza-Guedes, Olaia Sardón, Paula Corcuera, Greg A Hawkins, Annalisa Marsico, Thomas Bahmer, Klaus F. Rabe, Gesine Hansen, Matthias Volkmar Kopp, Raimon Rios, Maria Jesus Cruz, Francisco Javier González-Barcala, José María Olaguibel, Vicente Plaza, Santiago Quirce, Glorisa Canino, Michelle Cloutier, Victoria del Pozo, Jose R. Rodriguez-Santana, Javier Korta-Murua, Jesús Villar, Uroš Potočnik, Camila Figueiredo, Michael Kabesch, Somnath Mukhopadhyay, Guy Brusselle, Esteban G. Burchard, Maria Pino-Yanes

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Abstract

Background: Asthma exacerbations are a serious public health concern due to high healthcare resource utilization, work/school productivity loss, impact on quality of life, and risk of mortality. The genetic basis of asthma exacerbations has been studied in several populations, but no prior study has performed a multi-ancestry meta-analysis of genome-wide association studies (meta-GWAS) for this trait. We aimed to identify common genetic loci associated with asthma exacerbations across diverse populations and to assess their functional role in regulating DNA methylation and gene expression. Methods: A meta-GWAS of asthma exacerbations in 4989 Europeans, 2181 Hispanics/Latinos, 1250 Singaporean Chinese, and 972 African Americans analyzed 9.6 million genetic variants. Suggestively associated variants (p ≤ 5 × 10−5) were assessed for replication in 36,477 European and 1078 non-European asthma patients. Functional effects on DNA methylation were assessed in 595 Hispanic/Latino and African American asthma patients and in publicly available databases. The effect on gene expression was evaluated in silico. Results: One hundred and twenty-six independent variants were suggestively associated with asthma exacerbations in the discovery phase. Two variants independently replicated: rs12091010 located at vascular cell adhesion molecule-1/exostosin like glycosyltransferase-2 (VCAM1/EXTL2) (discovery: odds ratio (ORT allele) = 0.82, p = 9.05 × 10−6 and replication: ORT allele = 0.89, p = 5.35 × 10−3) and rs943126 from pantothenate kinase 1 (PANK1) (discovery: ORC allele = 0.85, p = 3.10 × 10−5 and replication: ORC allele = 0.89, p = 1.30 × 10−2). Both variants regulate gene expression of genes where they locate and DNA methylation levels of nearby genes in whole blood. Conclusions: This multi-ancestry study revealed novel suggestive regulatory loci for asthma exacerbations located in genomic regions participating in inflammation and host defense.

Original languageEnglish
Article numbere13802
JournalPediatric Allergy and Immunology
Volume33
Issue number6
DOIs
Publication statusPublished - Jun 2022

Bibliographical note

Funding Information:
This work was funded by the Spanish Ministry of Science and Innovation MCIN/AEI/10.13039/501100011033, and the European Regional Development Fund “ERDF A way of making Europe” by the European Union (SAF2017-83417R), by MCIN/AEI/10.13039/501100011033 (PID2020-116274RB-I00) and by the Allergopharma-EAACI award 2021. This study was also supported by the SysPharmPedia grant from the ERACoSysMed 1st Joint Transnational Call from the European Union under the Horizon 2020. GALA II and SAGE studies were supported by the Sandler Family Foundation, the American Asthma Foundation, the RWJF Amos Medical Faculty Development Program, Harry Wm. and Diana V. Hind Distinguished Professor in Pharmaceutical Sciences II, the National Heart, Lung, and Blood Institute of the National Institutes of Health (R01HL117004, R01HL128439, R01HL135156, X01HL134589, R01HL141992, and R01HL141845), National Institute of Health and Environmental Health Sciences (R01ES015794 and R21ES24844); the National Institute on Minority Health and Health Disparities (NIMHD) (P60MD006902, R01MD010443, and R56MD013312); the National Institute of General Medical Sciences (NIGMS) (RL5GM118984); the Tobacco-Related Disease Research Program (24RT-0025 and 27IR-0030); and the National Human Genome Research Institute (NHGRI) (U01HG009080) to EGB. The PACMAN study was funded by a strategic alliance between GlaxoSmithKline and Utrecht Institute for Pharmaceutical Sciences. The Slovenia study was financially supported by the Slovenian Research Agency (research core funding No. P3-0067) and from SysPharmPediA grant, co-financed by the Ministry of Education, Science and Sport Slovenia (MIZS) (contract number C3330-16-500106). The SHARE Bioresource (GoSHARE) and SHARE have ongoing funding from NHS Research Scotland and were established by funding from The Wellcome Trust Biomedical Resource [Grant No. 099177/Z/12/Z]. Genotyping of samples from BREATHE, PAGES, and GoSHARE was funded by AC15/00015 and conducted at the Genotyping National Centre (CeGEN) CeGen-PRB3-ISCIII; supported by ISCIII and European Regional Development Fund (ERDF) (PT17/0019). ALSPAC was supported by the UK Medical Research Council and Wellcome (102215/2/13/2) and the University of Bristol. The Swedish Heart-Lung Foundation, the Swedish Research Council, and Region Stockholm (ALF project and database maintenance) funded the BAMSE study. The PASS study was funded by the NHS Chair of Pharmacogenetics via the UK Department of Health. U-BIOPRED was funded by the Innovative Medicines Initiative (IMI) Joint Undertaking, under grant agreement no. 115010, resources for which are composed of financial contribution from the European Union's Seventh Framework Programme (FP7/2007-2013) and kind contributions from companies in the European Federation of Pharmaceutical Industries and Associations (EFPIA). Genotyping of samples from GEMAS and MEGA studies was funded by the Spanish Ministry of Science and Innovation (SAF2017-87417R) at the Spanish National Cancer Research Centre, in the Human Genotyping lab, a member of CeGen, PRB3, and was supported by grant PT17/0019, of the PE I+D+i 2013-2016, funded by ISCIII and ERDF. The genotyping of GEMAS was also partially funded by Fundación Canaria Instituto de Investigación Sanitaria de Canarias (PIFIISC19/17). The Rotterdam Study was funded by Erasmus Medical Center and Erasmus University Rotterdam; Netherlands Organization for the Health Research and Development (ZonMw); the Research Institute for Diseases in the Elderly (RIDE); the Ministry of Education, Culture and Science, the Ministry for Health, Welfare and Sports, the European Commission (DG XII), and the Municipality of Rotterdam. ALLIANCE Cohort was funded by grants from the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung, BMBF) as part of the German Centre for Lung Research (DZL) funding. The Hartford-Puerto Rico study was funded by the U.S. National Institutes of Health (grant HL07966 to JCC). MP-Y was funded by the Ramón y Cajal Program (RYC-2015-17205) by MCIN/AEI/10.13039/501100011033 and by the European Social Fund “ESF Investing in your future”. MP-Y and JV were supported by CIBER de Enfermedades Respiratorias, Instituto de Salud Carlos III, Spain (CB/06/06/1088). EH-L was supported by a fellowship awarded by MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future” (PRE2018-083837). JP-G was supported by a fellowship awarded by Spanish Ministry of Universities (FPU19/02175). AE-O reports funding from the Spanish Ministry of Science, Innovation, and Universities (MICIU) and Universidad de La Laguna (ULL). NH-P was supported by a Medium-Term Research Fellowship by the European Academy of Allergy and Clinical Immunology (EAACI) and a Long-Term Research Fellowship by the European Respiratory Society (ERS) (LTRF202101-00861). UP and MG were supported by the Ministry of Education, Science and Sport of the Republic of Slovenia, grant PERMEABLE (contract number C3330-19-252012). SCSGES results were contributed by authors FTC and YYS. FTC has received research support from the Singapore Ministry of Education Academic Research Fund, Singapore Immunology Network (SIgN), National Medical Research Council (NMRC) (Singapore), Biomedical Research Council (BMRC) (Singapore), and the Agency for Science Technology and Research (A*STAR) (Singapore); Grant Numbers: N-154-000-038-001, R-154-000-191-112, R-154-000-404-112, R-154-000-553-112, R-154-000-565-112, R-154-000-630-112, R-154-000-A08-592, R-154-000-A27-597, R-154-000-A91-592, R-154-000-A95-592, R-154-000-B99-114, BMRC/01/1/21/18/077, BMRC/04/1/21/19/315, SIgN-06-006, SIgN-08-020, NMRC/1150/2008, and H17/01/a0/008. F.T.C. has received consulting fees from Sime Darby Technology Centre; First Resources Ltd; Genting Plantation, and Olam International, outside the submitted work. YYS has received research support from the NUS Resilience & Growth Postdoctoral Fellowships with grant number: R-141-000-036-281. QY conducted the analysis from Hartford-Puerto Rico and United Kingdom Biobank studies. QY was funded by the U.S. National Institutes of Health (HL138098). All funding agencies had no role in the study design, data collection, and analysis, decision to publish, or preparation of the manuscript. The views expressed are those of the authors and not necessarily those of the any funder, National Health Service (NHS), the National Institute for Health Research (NIHR) or the United Kingdom Department of Health. The authors thank the patients, families, recruiters, healthcare providers, and community clinics for their participation in the studies analyzed in this manuscript. The authors also acknowledge the contribution of the high-performance compute cluster Wynton HPC underlying UCSF’s Research Computing Capability to the results of this research and Sandra Salazar for her support as GALA II and SAGE study coordinator. The authors thank the Centro Nacional de Genotipado-Plataforma de Recursos Biomoleculares-Instituto de Salud Carlos III (CeGen-PRB3-ISCIII; www.cegen.org) for providing the genotyping services. The authors also acknowledge all the families who took part in ALSPAC, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists, and nurses.

Funding Information:
AE‐O received grants from the Spanish Ministry of Science, Innovation, and Universities (MICIU) and Universidad de La Laguna (ULL). EH‐L, and MP‐Y report funding from the Spanish Ministry of Science and Innovation (MCIN/AEI/10.13039/501100011033) and by the European Social Fund “ESF Investing in your future” by the European Union. JP‐G reports funding from the Spanish Ministry of Universities. MP‐Y and FLD report grants from MCIN/AEI/10.13039/501100011033 and the European Regional Development Fund “ERDF A way of making Europe” by the European Union. MP‐Y reports grant support from GlaxoSmithKline, Spain paid to Fundación Canaria Instituto de Investigación Sanitaria de Canarias (FIISC) for a project outside the submitted work. MP‐Y and JV reports grants from Instituto de Salud Carlos III, Madrid, Spain. JV also reports funding by ISCIII and the European Regional Development Fund “ERDF A way of making Europe”. JMH‐P has received fees from CSL Behring, GSK, Astra‐Zeneca, laboratorios Menarini, Boehringer Ingelheim, FAES, laboratorios Esteve, Laboratorios Ferrer, Mundipharma, Laboratorios Rovi, Roche, Novartis, GRIFOLS, Pfizer, Acthelion‐Jansen, Chiesi y Laboratorios Bial for the realization of courses, talks, consultancies, and other activities related to his professional activity. FTC has received research support from the Singapore Ministry of Education Academic Research Fund, Singapore Immunology Network (SIgN), National Medical Research Council (NMRC) (Singapore), Biomedical Research Council (BMRC) (Singapore), and the Agency for Science Technology and Research (A*STAR) (Singapore). FTC has received consulting fees from Sime Darby Technology Centre; First Resources Ltd; Genting Plantation, and Olam International, outside the submitted work. YYS has received research support from the NUS Resilience & Growth Postdoctoral Fellowships. UP and MG received grants from the Ministry of Education, Science and Sport from Slovenia, the Slovenian Research Agency. M‐JC received grants from the Instituto de Salud Carlos III. DH received grant support from by NIHR for work on NIHR Alder Hey Clinical Research Facility, received payment for medicolegal report writing not related to asthma or pharmacogenomics for UK family court as an expert in pediatric clinical pharmacology. FJ‐B received fees from ALK, Astra‐Zeneca (AZ), Bial, Chiesi, Gebro Pharma, GlaxoSmithKline (GSK), Menarini, Rovi, Roxall, Sanofi, Stallergenes‐Greer and Teva. G‐B received fees from AZ, GSK, Boehringer‐Ingelheim, Novartis, Chiesi and Sanofi. JC received research materials from Pharmavite and GSK and Merck in order to provide medications free of cost to participants in NIH‐funded studies, unrelated to the current work. VO received grants from the National Heart, Lung, and Blood Institute, has participated in Data Safety Monitoring Boards for Regeneron and Sanofi, and participated as a Chair of the section on Genetics and Genomics of the American Thoracic Society. MVK has received grants from the German Federal Ministry of Education and Research, fees from Allergopharma GmbH, Sanofi Aventis GmbH, Infectopharm GmbH, Vertex GmbH, and Leti GmbH, has participated in Data Safety Monitoring Boards for Sanofi Aventis GmbH, and is the president of the German‐Swiss‐Austrian Society of Pediatric Pulmonology (GPP). NHP received support from the Instituto de Salud Carlos III, the European Social Funds from the European Union “ESF invests in your future,” the European Academy of Allergy and Clinical Immunology, and the European Respiratory Society. MP has received grants from NHS Chair of Pharmacogenetic grant from UK Department of Health, has received partnership funding for the following: MRC Clinical Pharmacology Training Scheme (co‐funded by MRC and Roche, UCB, Eli Lilly and Novartis); Joint PhD funding from EPSRC and AZ, and grant funding from Vistagen Therapeutics. He has also unrestricted educational grant support for the UK Pharmacogenetics and Stratified Medicine Network from Bristol‐Myers Squibb and UCB. He has developed an HLA genotyping panel with MC Diagnostics, but does not benefit financially from this. MP is part of the IMI Consortium ARDAT ( www.ardat.org ). SQ has received fees from GSK, AZ, Sanofi, Teva, Novartis, and Chiesi. SJ‐HV has received grants from SysPharmPediA EraNet. VdP has received fees from AZ and GSK. VP has received fees from Sanofi, AZ, Chiesi, MSD, and Boehringer Ingelheim, grant support from MSD, Chiesi Institutional, and Menarini. EvM has received grants from the German Federal Ministry of Education and Research and the Bavarian State Ministry of Health and Care, royalties/licenses from Elsevier GmbH, Georg Thieme Verlag, Springer‐Verlag GmbH and Elsevier Ltd. EvM has recieved fees from the Chinese University of Hongkong, European Commission, HiPP GmbH & Co KG, AZ, Imperial College London, Massachusetts Medical Society, Springer‐Verlag GmbH, Elsevier Ltd., Böhringer Ingelheim International GmbH, European Respiratory Society (ERS), Universiteit Utrecht, Faculteit Diergeneeskunde, Universität Salzburg, Springer Medizin Verlag GmbH, Japanese Society of Pediatric Allergy and Clinical Immunology (JSPACI), Klinikum Rechts der Isar, University of Colorado, Paul‐Martini‐Stiftung, Astra Zeneca, Imperial College London, Children´s Hospital Research Institute of Manitoba, Kompetenzzentrum für Ernährung (Kern), OM Pharma S.A., Swedish Pediatric Society for Allergy and Lung Medicine, Chinese College of Allergy and Asthma (CCAA), Verein zur Förderung der Pneumologie am Krankenhaus Großhansdorf e.V., Pneumologie Developpement, Mondial Congress & Events GmbH & Co. KG, American Academy of Allergy, Asthma & Immunology, Imperial College London, Margaux Orange, Volkswagen Stiftung, Böhringer Ingelheim International GmbH, European Respiratory Society (ERS), Universiteit Utrecht, Faculteit Diergeneeskunde, Österreichische Gesellschaft f. Allergologie u. Immunologie, Massachusetts Medical Society, OM Pharma S. A., Hanson Wade Ltd., iKOMM GmbH, DSI Dansk Borneastma Center, American Thoracic Society, HiPP GmbH & Co KG, Universiteit Utrecht, Faculteit Bètawetenschappen. EvM has patents No. PCT/EP2019/085016, EP21189353.2. 2021. and PCT/US2021/016918. 2021. pending, royalties paid to ProtectImmun for patent EP2361632 and patents EP1411977, EP1637147, and EP 1964570 licensed to ProtectImmun. EvM is a member of the EXPANSE Scientific Advisory Board, Member of the BEAMS External Scientific Advisory Board (ESAB), Member of the Editorial Board of “The Journal of Allergy and Clinical Immunology: In Practice”, Member of the Scientific Advisory Board of the Children's Respiratory and Environmental Workgroup (CREW), Member of the International Scientific & Societal Advisory Board (ISSAB) of Utrecht Life Sciences (ULS), University of Utrecht, Member of External Review Panel of the Faculty of Veterinary Science, University of Utrecht, Member of the Selection Committee for the Gottfried Wilhelm Leibniz Programme (DFG), Member of the International Advisory Board of Asthma UK Centre for Applied Research (AUKCAR), Member of the International Advisory Board of “The Lancet Respiratory Medicine”, Member of the Scientific Advisory Board of the CHILD (Canadian Healthy Infant Longitudinal Development) study, McMaster University, Hamilton, Canada, Asthma UK Centre for Applied Research and the Pediatric Scientific Advisory Board Iceland. The other authors declare no conflict of interest.

Funding Information:
This work was funded by the Spanish Ministry of Science and Innovation MCIN/AEI/10.13039/501100011033, and the European Regional Development Fund “ERDF A way of making Europe” by the European Union (SAF2017‐83417R), by MCIN/AEI/10.13039/501100011033 (PID2020‐116274RB‐I00) and by the Allergopharma‐EAACI award 2021. This study was also supported by the SysPharmPedia grant from the ERACoSysMed 1 Joint Transnational Call from the European Union under the Horizon 2020. GALA II and SAGE studies were supported by the Sandler Family Foundation, the American Asthma Foundation, the RWJF Amos Medical Faculty Development Program, Harry Wm. and Diana V. Hind Distinguished Professor in Pharmaceutical Sciences II, the National Heart, Lung, and Blood Institute of the National Institutes of Health (R01HL117004, R01HL128439, R01HL135156, X01HL134589, R01HL141992, and R01HL141845), National Institute of Health and Environmental Health Sciences (R01ES015794 and R21ES24844); the National Institute on Minority Health and Health Disparities (NIMHD) (P60MD006902, R01MD010443, and R56MD013312); the National Institute of General Medical Sciences (NIGMS) (RL5GM118984); the Tobacco‐Related Disease Research Program (24RT‐0025 and 27IR‐0030); and the National Human Genome Research Institute (NHGRI) (U01HG009080) to EGB. The PACMAN study was funded by a strategic alliance between GlaxoSmithKline and Utrecht Institute for Pharmaceutical Sciences. The Slovenia study was financially supported by the Slovenian Research Agency (research core funding No. P3‐0067) and from SysPharmPediA grant, co‐financed by the Ministry of Education, Science and Sport Slovenia (MIZS) (contract number C3330‐16‐500106). The SHARE Bioresource (GoSHARE) and SHARE have ongoing funding from NHS Research Scotland and were established by funding from The Wellcome Trust Biomedical Resource [Grant No. 099177/Z/12/Z]. Genotyping of samples from BREATHE, PAGES, and GoSHARE was funded by AC15/00015 and conducted at the Genotyping National Centre (CeGEN) CeGen‐PRB3‐ISCIII; supported by ISCIII and European Regional Development Fund (ERDF) (PT17/0019). ALSPAC was supported by the UK Medical Research Council and Wellcome (102215/2/13/2) and the University of Bristol. The Swedish Heart‐Lung Foundation, the Swedish Research Council, and Region Stockholm (ALF project and database maintenance) funded the BAMSE study. The PASS study was funded by the NHS Chair of Pharmacogenetics via the UK Department of Health. U‐BIOPRED was funded by the Innovative Medicines Initiative (IMI) Joint Undertaking, under grant agreement no. 115010, resources for which are composed of financial contribution from the European Union's Seventh Framework Programme (FP7/2007‐2013) and kind contributions from companies in the European Federation of Pharmaceutical Industries and Associations (EFPIA). Genotyping of samples from GEMAS and MEGA studies was funded by the Spanish Ministry of Science and Innovation (SAF2017‐87417R) at the Spanish National Cancer Research Centre, in the Human Genotyping lab, a member of CeGen, PRB3, and was supported by grant PT17/0019, of the PE I+D+i 2013‐2016, funded by ISCIII and ERDF. The genotyping of GEMAS was also partially funded by Fundación Canaria Instituto de Investigación Sanitaria de Canarias (PIFIISC19/17). The Rotterdam Study was funded by Erasmus Medical Center and Erasmus University Rotterdam; Netherlands Organization for the Health Research and Development (ZonMw); the Research Institute for Diseases in the Elderly (RIDE); the Ministry of Education, Culture and Science, the Ministry for Health, Welfare and Sports, the European Commission (DG XII), and the Municipality of Rotterdam. ALLIANCE Cohort was funded by grants from the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung, BMBF) as part of the German Centre for Lung Research (DZL) funding. The Hartford‐Puerto Rico study was funded by the U.S. National Institutes of Health (grant HL07966 to JCC). MP‐Y was funded by the Ramón y Cajal Program (RYC‐2015‐17205) by MCIN/AEI/10.13039/501100011033 and by the European Social Fund “ESF Investing in your future”. MP‐Y and JV were supported by CIBER de Enfermedades Respiratorias, Instituto de Salud Carlos III, Spain (CB/06/06/1088). EH‐L was supported by a fellowship awarded by MCIN/AEI/10.13039/501100011033 and by “ESF Investing in your future” (PRE2018‐083837). JP‐G was supported by a fellowship awarded by Spanish Ministry of Universities (FPU19/02175). AE‐O reports funding from the Spanish Ministry of Science, Innovation, and Universities (MICIU) and Universidad de La Laguna (ULL). NH‐P was supported by a Medium‐Term Research Fellowship by the European Academy of Allergy and Clinical Immunology (EAACI) and a Long‐Term Research Fellowship by the European Respiratory Society (ERS) (LTRF202101‐00861). UP and MG were supported by the Ministry of Education, Science and Sport of the Republic of Slovenia, grant PERMEABLE (contract number C3330‐19‐252012). SCSGES results were contributed by authors FTC and YYS. FTC has received research support from the Singapore Ministry of Education Academic Research Fund, Singapore Immunology Network (SIgN), National Medical Research Council (NMRC) (Singapore), Biomedical Research Council (BMRC) (Singapore), and the Agency for Science Technology and Research (A*STAR) (Singapore); Grant Numbers: N‐154‐000‐038‐001, R‐154‐000‐191‐112, R‐154‐000‐404‐112, R‐154‐000‐553‐112, R‐154‐000‐565‐112, R‐154‐000‐630‐112, R‐154‐000‐A08‐592, R‐154‐000‐A27‐597, R‐154‐000‐A91‐592, R‐154‐000‐A95‐592, R‐154‐000‐B99‐114, BMRC/01/1/21/18/077, BMRC/04/1/21/19/315, SIgN‐06‐006, SIgN‐08‐020, NMRC/1150/2008, and H17/01/a0/008. F.T.C. has received consulting fees from Sime Darby Technology Centre; First Resources Ltd; Genting Plantation, and Olam International, outside the submitted work. YYS has received research support from the NUS Resilience & Growth Postdoctoral Fellowships with grant number: R‐141‐000‐036‐281. QY conducted the analysis from Hartford‐Puerto Rico and United Kingdom Biobank studies. QY was funded by the U.S. National Institutes of Health (HL138098). All funding agencies had no role in the study design, data collection, and analysis, decision to publish, or preparation of the manuscript. The views expressed are those of the authors and not necessarily those of the any funder, National Health Service (NHS), the National Institute for Health Research (NIHR) or the United Kingdom Department of Health. st Editor

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© 2022 The Authors. Pediatric Allergy and Immunology published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.

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