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. 2023 Jul;152(1):117-125.
doi: 10.1016/j.jaci.2023.02.032. Epub 2023 Mar 12.

Stratification of asthma by lipidomic profiling of induced sputum supernatant

Joost Brandsma  1 , James P R Schofield  2 , Xian Yang  3 , Fabio Strazzeri  4 , Clair Barber  5 , Victoria M Goss  6 , Grielof Koster  6 , Per S Bakke  7 , Massimo Caruso  8 , Pascal Chanez  9 , Sven-Erik Dahlén  10 , Stephen J Fowler  11 , Ildikó Horváth  12 , Norbert Krug  13 , Paolo Montuschi  14 , Marek Sanak  15 , Thomas Sandström  16 , Dominick E Shaw  17 , Kian Fan Chung  18 , Florian Singer  19 , Louise J Fleming  18 , Ian M Adcock  18 , Ioannis Pandis  3 , Aruna T Bansal  20 , Julie Corfield  21 , Ana R Sousa  22 , Peter J Sterk  23 , Rubén J Sánchez-García  4 , Paul J Skipp  24 , Anthony D Postle  25 , Ratko Djukanović  6 ; U-BIOPRED Study Group
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Free article

Stratification of asthma by lipidomic profiling of induced sputum supernatant

Joost Brandsma et al. J Allergy Clin Immunol. 2023 Jul.
Free article

Abstract

Background: Asthma is a chronic respiratory disease with significant heterogeneity in its clinical presentation and pathobiology. There is need for improved understanding of respiratory lipid metabolism in asthma patients and its relation to observable clinical features.

Objective: We performed a comprehensive, prospective, cross-sectional analysis of the lipid composition of induced sputum supernatant obtained from asthma patients with a range of disease severities, as well as from healthy controls.

Methods: Induced sputum supernatant was collected from 211 adults with asthma and 41 healthy individuals enrolled onto the U-BIOPRED (Unbiased Biomarkers for the Prediction of Respiratory Disease Outcomes) study. Sputum lipidomes were characterized by semiquantitative shotgun mass spectrometry and clustered using topologic data analysis to identify lipid phenotypes.

Results: Shotgun lipidomics of induced sputum supernatant revealed a spectrum of 9 molecular phenotypes, highlighting not just significant differences between the sputum lipidomes of asthma patients and healthy controls, but also within the asthma patient population. Matching clinical, pathobiologic, proteomic, and transcriptomic data helped inform the underlying disease processes. Sputum lipid phenotypes with higher levels of nonendogenous, cell-derived lipids were associated with significantly worse asthma severity, worse lung function, and elevated granulocyte counts.

Conclusion: We propose a novel mechanism of increased lipid loading in the epithelial lining fluid of asthma patients resulting from the secretion of extracellular vesicles by granulocytic inflammatory cells, which could reduce the ability of pulmonary surfactant to lower surface tension in asthmatic small airways, as well as compromise its role as an immune regulator.

Keywords: Asthma; epithelial lining fluid; extracellular vesicles; granulocytic inflammation; induced sputum; lipidomics; molecular phenotyping; pulmonary surfactant.

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