Landscape fire smoke airway exposure impairs respiratory and cardiac function and worsens experimental asthma

Henry M Gomez; Tatt J Haw; Dusan Ilic; Peter Robinson; Chantal Donovan; Amanda J Croft; Kanth S Vanka; Ellen Small; Olivia R Carroll; Richard Y Kim; Jemma R Mayall; Tesfalidet Beyene; Thava Palanisami; Doan T M Ngo; Graeme R Zosky; Elizabeth G Holliday; Megan E Jensen; Vanessa M McDonald; Vanessa E Murphy; Peter G Gibson; Jay C Horvat

doi:10.1016/j.jaci.2024.02.022

Landscape fire smoke airway exposure impairs respiratory and cardiac function and worsens experimental asthma

J Allergy Clin Immunol. 2024 Mar 19:S0091-6749(24)00272-0. doi: 10.1016/j.jaci.2024.02.022. Online ahead of print.

Authors

Henry M Gomez¹, Tatt J Haw², Dusan Ilic³, Peter Robinson³, Chantal Donovan⁴, Amanda J Croft², Kanth S Vanka⁵, Ellen Small¹, Olivia R Carroll¹, Richard Y Kim⁴, Jemma R Mayall¹, Tesfalidet Beyene⁶, Thava Palanisami⁷, Doan T M Ngo², Graeme R Zosky⁸, Elizabeth G Holliday⁹, Megan E Jensen⁶, Vanessa M McDonald⁶, Vanessa E Murphy⁶, Peter G Gibson⁶, Jay C Horvat¹⁰

Affiliations

¹ School of Biomedical Sciences and Pharmacy, University of Newcastle and Immune Health Program, Hunter Medical Research Institute, Newcastle, Australia.
² Heart and Stroke Research Program, Hunter Medical Research Institute, New Lambton Heights, Newcastle, Australia; College of Health, Medicine, and Wellbeing, Centre of Excellence Newcastle Cardio-Oncology Research Group, University of Newcastle, Callaghan, Newcastle, Australia.
³ Newcastle Institute for Energy and Resources, University of Newcastle, Callaghan, Australia.
⁴ School of Biomedical Sciences and Pharmacy, University of Newcastle and Immune Health Program, Hunter Medical Research Institute, Newcastle, Australia; School of Life Sciences, University of Technology Sydney, Faculty of Science, Sydney, Australia.
⁵ School of Biomedical Sciences and Pharmacy, University of Newcastle and Immune Health Program, Hunter Medical Research Institute, Newcastle, Australia; Newcastle Institute for Energy and Resources, University of Newcastle, Callaghan, Australia.
⁶ School of Medicine and Public Health, University of Newcastle and Asthma and Breathing Program, Hunter Medical Research Institute, Newcastle, Australia.
⁷ Global Innovative Centre for Advanced Nanomaterials, University of Newcastle, Callaghan, Australia.
⁸ Menzies Institute for Medical Research, College of Health and Medicine, University of Tasmania, Hobart, Australia; College of Health and Medicine, Tasmanian School of Medicine, University of Tasmania, Hobart, Australia.
⁹ School of Medicine and Public Health, University of Newcastle, Callaghan, Australia.
¹⁰ School of Biomedical Sciences and Pharmacy, University of Newcastle and Immune Health Program, Hunter Medical Research Institute, Newcastle, Australia. Electronic address: jay.horvat@newcastle.edu.au.

PMID: 38513838
DOI: 10.1016/j.jaci.2024.02.022

Abstract

Background: Millions of people are exposed to landscape fire smoke (LFS) globally, and inhalation of LFS particulate matter (PM) is associated with poor respiratory and cardiovascular outcomes. However, how LFS affects respiratory and cardiovascular function is less well understood.

Objective: We aimed to characterize the pathophysiologic effects of representative LFS airway exposure on respiratory and cardiac function and on asthma outcomes.

Methods: LFS was generated using a customized combustion chamber. In 8-week-old female BALB/c mice, low (25 μg/m³, 24-hour equivalent) or moderate (100 μg/m³, 24-hour equivalent) concentrations of LFS PM (10 μm and below [PM₁₀]) were administered daily for 3 (short-term) and 14 (long-term) days in the presence and absence of experimental asthma. Lung inflammation, gene expression, structural changes, and lung function were assessed. In 8-week-old male C57BL/6 mice, low concentrations of LFS PM₁₀ were administered for 3 days. Cardiac function and gene expression were assessed.

Results: Short- and long-term LFS PM₁₀ airway exposure increased airway hyperresponsiveness and induced steroid insensitivity in experimental asthma, independent of significant changes in airway inflammation. Long-term LFS PM₁₀ airway exposure also decreased gas diffusion. Short-term LFS PM₁₀ airway exposure decreased cardiac function and expression of gene changes relating to oxidative stress and cardiovascular pathologies.

Conclusions: We characterized significant detrimental effects of physiologically relevant concentrations and durations of LFS PM₁₀ airway exposure on lung and heart function. Our study provides a platform for assessment of mechanisms that underpin LFS PM₁₀ airway exposure on respiratory and cardiovascular disease outcomes.

Keywords: Landscape fire smoke; air pollution; asthma; cardiovascular disease; lung disease; particulate matter exposure.