Black carbon content in airway macrophages is associated with increased severe exacerbations and worse COPD morbidity in SPIROMICS

Vickram Tejwani; Han Woo; Chen Liu; Anna K Tillery; Amanda J Gassett; Richard E Kanner; Eric A Hoffman; Fernando J Martinez; Prescott G Woodruff; R Graham Barr; Ashraf Fawzy; Kirsten Koehler; Jeffrey L Curtis; Christine M Freeman; Christopher B Cooper; Alejandro P Comellas; Cheryl Pirozzi; Robert Paine; Donald Tashkin; Jerry A Krishnan; Coralynn Sack; Nirupama Putcha; Laura M Paulin; Marina Zusman; Joel D Kaufman; Neil E Alexis; Nadia N Hansel

doi:10.1186/s12931-022-02225-0

Black carbon content in airway macrophages is associated with increased severe exacerbations and worse COPD morbidity in SPIROMICS

Respir Res. 2022 Nov 14;23(1):310. doi: 10.1186/s12931-022-02225-0.

Authors

Vickram Tejwani^{1

2}, Han Woo³, Chen Liu³, Anna K Tillery⁴, Amanda J Gassett⁵, Richard E Kanner⁶, Eric A Hoffman⁷, Fernando J Martinez⁸, Prescott G Woodruff⁹, R Graham Barr¹⁰, Ashraf Fawzy³, Kirsten Koehler¹¹, Jeffrey L Curtis^{12

13}, Christine M Freeman^{12

13}, Christopher B Cooper¹⁴, Alejandro P Comellas¹⁵, Cheryl Pirozzi¹⁶, Robert Paine¹⁶, Donald Tashkin¹⁴, Jerry A Krishnan¹⁷, Coralynn Sack⁵, Nirupama Putcha³, Laura M Paulin¹⁸, Marina Zusman⁵, Joel D Kaufman⁵, Neil E Alexis⁴, Nadia N Hansel³

Affiliations

¹ Division of Pulmonary and Critical Care Medicine, Johns Hopkins University, Baltimore, MD, USA. tejwanv@ccf.org.
² Respiratory Institute, Cleveland Clinic, 9500 Euclid Avenue, A90, 44195, Cleveland, OH, USA. tejwanv@ccf.org.
³ Division of Pulmonary and Critical Care Medicine, Johns Hopkins University, Baltimore, MD, USA.
⁴ Center for Environmental Medicine, Asthma, and Lung Biology, Division of Allergy and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
⁵ Division of Pulmonary and Critical Care Medicine, University of Washington, Seattle, WA, USA.
⁶ Division of Respiratory, Critical Care and Occupational Medicine, University of Utah, Salt Lake City, UT, USA.
⁷ Department of Radiology, Medicine and Biomedical Engineering, University of Iowa, Iowa City, IA, USA.
⁸ Division of Pulmonology and Critical Care Medicine, Weill-Cornell Medical Center, Cornell University, New York, NY, USA.
⁹ Division of Pulmonary, Critical Care and Sleep Medicine, University of California San Francisco, San Francisco, CA, USA.
¹⁰ Department of Medicine, Columbia University College of Physicians and Surgeons, New York, New York, USA.
¹¹ Environmental Health and Engineering, Johns Hopkins University, Baltimore, MD, USA.
¹² Pulmonary and Critical Care Medicine Division, Department of Internal Medicine, University of Michigan Health System, Ann Arbor, MI, USA.
¹³ Veterans Affairs Ann Arbor Healthcare System, Ann Arbor, MI, USA.
¹⁴ Division of Pulmonary and Critical Care Medicine, University of California Los Angeles Medical Center, Los Angeles, CA, USA.
¹⁵ Division of Pulmonary, Critical Care, and Occupational Medicine, College of Medicine, University of Iowa, Iowa City, IA, USA.
¹⁶ University of Utah Hospital, Salt Lake City, UT, USA.
¹⁷ Department of Medicine, University of Illinois at Chicago, Chicago, IL, USA.
¹⁸ Pulmonary/Critical Care, Dartmouth Hitchcock Medical Center, Lebanon, NH, USA.

Abstract

Background: Airway macrophages (AM), crucial for the immune response in chronic obstructive pulmonary disease (COPD), are exposed to environmental particulate matter (PM), which they retain in their cytoplasm as black carbon (BC). However, whether AM BC accurately reflects environmental PM_2.5 exposure, and can serve as a biomarker of COPD outcomes, is unknown.

Methods: We analyzed induced sputum from participants at 7 of 12 sites SPIROMICS sites for AM BC content, which we related to exposures and to lung function and respiratory outcomes. Models were adjusted for batch (first vs. second), age, race (white vs. non-white), income (<$35,000, $35,000~$74,999, ≥$75,000, decline to answer), BMI, and use of long-acting beta-agonist/long-acting muscarinic antagonists, with sensitivity analysis performed with inclusion of urinary cotinine and lung function as covariates.

Results: Of 324 participants, 143 were current smokers and 201 had spirometric-confirmed COPD. Modeled indoor fine (< 2.5 μm in aerodynamic diameter) particulate matter (PM_2.5) and urinary cotinine were associated with higher AM BC. Other assessed indoor and ambient pollutant exposures were not associated with higher AM BC. Higher AM BC was associated with worse lung function and odds of severe exacerbation, as well as worse functional status, respiratory symptoms and quality of life.

Conclusion: Indoor PM_2.5 and cigarette smoke exposure may lead to increased AM BC deposition. Black carbon content in AMs is associated with worse COPD morbidity in current and former smokers, which remained after sensitivity analysis adjusting for cigarette smoke burden. Airway macrophage BC, which may alter macrophage function, could serve as a predictor of experiencing worse respiratory symptoms and impaired lung function.

Keywords: Black carbon; COPD; Macrophage.

MeSH terms

Air Pollutants* / adverse effects
Air Pollutants* / analysis
Carbon
Cotinine
Humans
Macrophages
Morbidity
Particulate Matter / adverse effects
Particulate Matter / analysis
Pulmonary Disease, Chronic Obstructive* / complications
Pulmonary Disease, Chronic Obstructive* / diagnosis
Pulmonary Disease, Chronic Obstructive* / epidemiology
Quality of Life
Soot / adverse effects
Soot / analysis

Substances

Cotinine
Soot
Particulate Matter
Carbon
Air Pollutants

Abstract

MeSH terms

Substances

Grants and funding