Metabolomic profiles during early childhood and risk of food allergies and asthma in multiethnic children from a prospective birth cohort

Xiumei Hong; Kari Nadeau; Guoying Wang; Ben Larman; Kellie N Smith; Colleen Pearson; Hongkai Ji; Pamela Frischmeyer-Guerrerio; Liming Liang; Frank B Hu; Xiaobin Wang

doi:10.1016/j.jaci.2024.02.024

Metabolomic profiles during early childhood and risk of food allergies and asthma in multiethnic children from a prospective birth cohort

J Allergy Clin Immunol. 2024 Mar 26:S0091-6749(24)00295-1. doi: 10.1016/j.jaci.2024.02.024. Online ahead of print.

Authors

Xiumei Hong¹, Kari Nadeau², Guoying Wang³, Ben Larman⁴, Kellie N Smith⁵, Colleen Pearson⁶, Hongkai Ji⁷, Pamela Frischmeyer-Guerrerio⁸, Liming Liang⁹, Frank B Hu¹⁰, Xiaobin Wang¹¹

Affiliations

¹ Department of Population, Family and Reproductive Health, Center on the Early Life Origins of Disease, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Md. Electronic address: xhong3@jhu.edu.
² Department of Environmental Health, Harvard T. H. Chan School of Public Health, Boston, Mass.
³ Department of Population, Family and Reproductive Health, Center on the Early Life Origins of Disease, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Md.
⁴ Department of Pathology, Division of Immunology, Johns Hopkins University School of Medicine, Baltimore, Md.
⁵ Department of Oncology, Johns Hopkins University School of Medicine, Baltimore, and the Bloomberg-Kimmel Institute for Cancer Immunotherapy and Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, Md.
⁶ Department of Pediatrics, Boston University School of Medicine and Boston Medical Center, Boston, Mass.
⁷ Department of Biostatistics, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Md.
⁸ Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Md.
⁹ Department of Epidemiology and Biostatistics, T. H. Chan School of Public Health, Harvard University, Boston, Mass.
¹⁰ Department of Epidemiology and Biostatistics, T. H. Chan School of Public Health, Harvard University, Boston, Mass; Department of Nutrition, T. H. Chan School of Public Health, Harvard University, Boston, Mass; Department of Medicine, Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass.
¹¹ Department of Population, Family and Reproductive Health, Center on the Early Life Origins of Disease, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Md; Department of Pediatrics, Division of General Pediatrics & Adolescent Medicine, Johns Hopkins University School of Medicine, Baltimore, Md.

PMID: 38548091
DOI: 10.1016/j.jaci.2024.02.024

Abstract

Background: There are increasing numbers of metabolomic studies in food allergy (FA) and asthma, which, however, are predominantly limited by cross-sectional designs, small sample size, and being conducted in European populations.

Objective: We sought to identify metabolites unique to and shared by children with FA and/or asthma in a racially diverse prospective birth cohort, the Boston Birth Cohort.

Methods: Mass spectrometry-based untargeted metabolomic profiling was performed using venous plasma collected in early childhood (n = 811). FA was diagnosed according to clinical symptoms consistent with an acute hypersensitivity reaction at food ingestion and food specific-IgE > 0.35 kU/L. Asthma was defined on the basis of physician diagnosis. Generalized estimating equations were applied to analyze metabolomic associations with FA and asthma, adjusting for potential confounders.

Results: During a mean ± standard deviation follow-up of 11.8 ± 5.2 years from birth, 78 children developed FA and 171 developed asthma. Androgenic and pregnenolone steroids were significantly associated with a lower risk of FA, especially for egg allergy. N,N,N-trimethyl-5-aminovalerate (odds ratio [OR] = 0.65, 95% confidence interval [CI] = 0.48-0.87), and 1-oleoyl-2-arachidonoyl-sn-glycero-3-phosphoinositol (OR = 0.77; 95% CI = 0.66-0.90) were inversely associated with FA risk. Orotidine (OR = 4.73; 95% CI = 2.2-10.2) and 4-cholesten-3-one (OR = 0.52; 95% CI = 0.35-0.77) were the top 2 metabolites associated with risk of asthma, although they had no association with FA. In comparison, children with both FA and asthma exhibited an altered metabolomic profile that aligned with that of FA, including altered levels of lipids and steroids.

Conclusion: In this US multiethnic prospective birth cohort, unique and shared alterations in plasma metabolites during early childhood were associated with risk of developing FA and/or asthma. These findings await further validation.

Keywords: Food allergy; asthma; metabolomic profiles; multiethnic children; prospective birth cohort; steroid metabolites.

Abstract

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