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A Mechanical Mechanism for Vitamin E Acetate in E-cigarette/Vaping-Associated Lung Injury

  • Mitchell DiPasquale
    Mitchell DiPasquale
    Department of Chemistry and Biochemistry, University of Windsor, Windsor, Ontario, Canada N9B 3P4
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  • , 
  • Omotayo Gbadamosi
    Omotayo Gbadamosi
    Department of Chemistry and Biochemistry, University of Windsor, Windsor, Ontario, Canada N9B 3P4
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  • , 
  • Michael H. L. Nguyen
    Michael H. L. Nguyen
    Department of Chemistry and Biochemistry, University of Windsor, Windsor, Ontario, Canada N9B 3P4
    More by Michael H. L. Nguyen
  • , 
  • Stuart R. Castillo
    Stuart R. Castillo
    Department of Chemistry and Biochemistry, University of Windsor, Windsor, Ontario, Canada N9B 3P4
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  • , 
  • Brett W. Rickeard
    Brett W. Rickeard
    Department of Chemistry and Biochemistry, University of Windsor, Windsor, Ontario, Canada N9B 3P4
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  • , 
  • Elizabeth G. Kelley
    Elizabeth G. Kelley
    NIST Center for Neutron Research, National Institute of Standards and Technology, Gaithersburg, Maryland 20899, United States
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    Orcidhttp://orcid.org/0000-0002-6128-8517
  • , 
  • Michihiro Nagao
    Michihiro Nagao
    NIST Center for Neutron Research, National Institute of Standards and Technology, Gaithersburg, Maryland 20899, United States
    Center for Exploration of Energy and Matter, Department of Physics, Indiana University, Bloomington, Indiana 47408, United States
    Department of Physics and AstronomyUniversity of DelawareNewarkDelaware19716United States
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    Orcidhttp://orcid.org/0000-0003-3617-251X
  • , and 
  • Drew Marquardt*
    Drew Marquardt
    Department of Chemistry and Biochemistry  and  Department of Physics, University of Windsor, Windsor, Ontario, Canada N9B 3P4
    *Email: [email protected]
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    Orcidhttp://orcid.org/0000-0001-6848-2497
Cite this: Chem. Res. Toxicol. 2020, 33, 9, 2432–2440
Publication Date (Web):August 26, 2020
https://doi.org/10.1021/acs.chemrestox.0c00212
Copyright © 2020 American Chemical Society
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    Abstract

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    The outbreak of electronic-cigarette/vaping-associated lung injury (EVALI) has made thousands ill. This lung injury has been attributed to a physical interaction between toxicants from the vaping solution and the pulmonary surfactant. In particular, studies have implicated vitamin E acetate as a potential instigator of EVALI. Pulmonary surfactant is vital to proper respiration through the mechanical processes of adsorption and interface stability to achieve and maintain low surface tension at the air–liquid interface. Using neutron spin echo spectroscopy, we investigate the impact of vitamin E acetate on the mechanical properties of two lipid-only pulmonary surfactant mimics: pure 1,2-dipalmitoyl-sn-glycero-3-phosphocholine and a more comprehensive lipid mixture. It was found that increasing vitamin E acetate concentration nonlinearly increased membrane fluidity and area compressibility to a plateau. Softer membranes would promote adsorption to the air–liquid interface during inspiration as well as collapse from the interface during expiration. These findings indicate the potential for the failure of the pulmonary surfactant upon expiration, attributed to monolayer collapse. This collapse could contribute to the observed EVALI signs and symptoms, including shortness of breath and pneumonitis.

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    • Dynamic light scattering intensity plot; bilayer structural parameters derived from small-angle neutron scattering; quantification of vitamin E acetate content by UV–vis spectroscopy; membrane elastic parameters measured by neutron spin–echo (PDF)

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    Cited By

    This article is cited by 29 publications.

    1. Maksymilian Dziura, Stuart R. Castillo, Mitchell DiPasquale, Omotayo Gbadamosi, Piotr Zolnierczuk, Michihiro Nagao, Elizabeth G. Kelley, Drew Marquardt. Investigating the Effect of Medium Chain Triglycerides on the Elasticity of Pulmonary Surfactant. Chemical Research in Toxicology 2023, 36 (4) , 643-652. https://doi.org/10.1021/acs.chemrestox.2c00349
    2. Yichen Li, Jiayin Dai, Lillian N. Tran, Kent E. Pinkerton, Eliot R. Spindel, Tran B. Nguyen. Vaping Aerosols from Vitamin E Acetate and Tetrahydrocannabinol Oil: Chemistry and Composition. Chemical Research in Toxicology 2022, 35 (6) , 1095-1109. https://doi.org/10.1021/acs.chemrestox.2c00064
    3. Stuart R. Castillo, Brett W. Rickeard, Mitchell DiPasquale, Michael H. L. Nguyen, Aislyn Lewis-Laurent, Milka Doktorova, Batuhan Kav, Markus S. Miettinen, Michihiro Nagao, Elizabeth G. Kelley, Drew Marquardt. Probing the Link between Pancratistatin and Mitochondrial Apoptosis through Changes in the Membrane Dynamics on the Nanoscale. Molecular Pharmaceutics 2022, 19 (6) , 1839-1852. https://doi.org/10.1021/acs.molpharmaceut.1c00926
    4. Alexa Canchola, C. M. Sabbir Ahmed, Kunpeng Chen, Jin Y. Chen, Ying-Hsuan Lin. Formation of Redox-Active Duroquinone from Vaping of Vitamin E Acetate Contributes to Oxidative Lung Injury. Chemical Research in Toxicology 2022, 35 (2) , 254-264. https://doi.org/10.1021/acs.chemrestox.1c00309
    5. Nathalie Hayeck, Carl Zoghzoghi, Ebrahim Karam, Rola Salman, Nareg Karaoghlanian, Alan Shihadeh, Thomas Eissenberg, Salah Zein El Dine, Najat A. Saliba. Carrier Solvents of Electronic Nicotine Delivery Systems Alter Pulmonary Surfactant. Chemical Research in Toxicology 2021, 34 (6) , 1572-1577. https://doi.org/10.1021/acs.chemrestox.0c00528
    6. Nicolas van Bavel, Patrick Lai, Matthias Amrein, Elmar J. Prenner. Biophysical investigation of vape additives with complex lung surfactant model systems and physiological surfactant extracts. JCIS Open 2023, 10 , 100085. https://doi.org/10.1016/j.jciso.2023.100085
    7. Michihiro Nagao, Hideki Seto. Neutron scattering studies on dynamics of lipid membranes. Biophysics Reviews 2023, 4 (2) https://doi.org/10.1063/5.0144544
    8. Irina Petrache, Arnav Gupta, Patrick S. Hume, Tanner Rivera, Kelly S. Schweitzer, Hong Wei Chu. Pathogenesis of E‐Cigarette Vaping Product Use‐Associated Lung Injury (EVALI). 2023, 4617-4630. https://doi.org/10.1002/cphy.c220022
    9. Meghan E. Rebuli, Jason J. Rose, Alexandra Noël, Daniel P. Croft, Neal L. Benowitz, Alan H. Cohen, Maciej L. Goniewicz, Brandon T. Larsen, Noel Leigh, Matthew D. McGraw, Anne C. Melzer, Arthur L. Penn, Irfan Rahman, Dona Upson, Laura E. Crotty Alexander, Gary Ewart, Ilona Jaspers, Sven Eric Jordt, Seth Kligerman, Ceila E. Loughlin, Rob McConnell, Enid R. Neptune, Tran B. Nguyen, Kent E. Pinkerton, Theodore J. Witek. The E-cigarette or Vaping Product Use–Associated Lung Injury Epidemic: Pathogenesis, Management, and Future Directions: An Official American Thoracic Society Workshop Report. Annals of the American Thoracic Society 2023, 20 (1) , 1-17. https://doi.org/10.1513/AnnalsATS.202209-796ST
    10. Brian Soto, Louis Costanzo, Anoop Puskoor, Nada Akkari, Patrick Geraghty. The implications of Vitamin E acetate in E-cigarette, or vaping, product use-associated lung injury. Annals of Thoracic Medicine 2023, 18 (1) , 1. https://doi.org/10.4103/atm.atm_144_22
    11. Jean-Marc Zingg. Vitamin E physiology and health effects. 2023, 556-568. https://doi.org/10.1016/B978-0-12-821848-8.00095-0
    12. James Y. Liu, Christie M. Sayes. Lung surfactant as a biophysical assay for inhalation toxicology. Current Research in Toxicology 2023, 4 , 100101. https://doi.org/10.1016/j.crtox.2022.100101
    13. Emma Graham, Lynda McCaig, Gloria Shui-Kei Lau, Akash Tejura, Anne Cao, Yi Y. Zuo, Ruud Veldhuizen, . E-cigarette aerosol exposure of pulmonary surfactant impairs its surface tension reducing function. PLOS ONE 2022, 17 (11) , e0272475. https://doi.org/10.1371/journal.pone.0272475
    14. Riccardo Polosa, Thomas B. Casale, Donald P. Tashkin. A Close Look at Vaping in Adolescents and Young Adults in the United States. The Journal of Allergy and Clinical Immunology: In Practice 2022, 10 (11) , 2831-2842. https://doi.org/10.1016/j.jaip.2022.06.005
    15. W. Daear, K. Sule, P. Lai, E. J. Prenner. Biophysical analysis of gelatin and PLGA nanoparticle interactions with complex biomimetic lung surfactant models. RSC Advances 2022, 12 (43) , 27918-27932. https://doi.org/10.1039/D2RA02859J
    16. Meghan E. Rebuli. Phosphatidylethanolamines as biomarkers of e‐cigarette or vaping product use‐associated lung injury. Pediatric Pulmonology 2022, 57 (7) , 1792-1794. https://doi.org/10.1002/ppul.25951
    17. Nicolas van Bavel, Patrick Lai, Raimar Loebenberg, Elmar J Prenner. Vaping additives negatively impact the stability and lateral film organization of lung surfactant model systems. Nanomedicine 2022, 17 (12) , 827-843. https://doi.org/10.2217/nnm-2021-0398
    18. Antonella Marrocco, Dilpreet Singh, David C. Christiani, Philip Demokritou. E-cigarette vaping associated acute lung injury (EVALI): state of science and future research needs. Critical Reviews in Toxicology 2022, 52 (3) , 188-220. https://doi.org/10.1080/10408444.2022.2082918
    19. Vladimir B. Mikheev, Alexander Ivanov. Analysis of the Aerosol Generated from Tetrahydrocannabinol, Vitamin E Acetate, and Their Mixtures. Toxics 2022, 10 (2) , 88. https://doi.org/10.3390/toxics10020088
    20. Nadia Milad, Mathieu C. Morissette. Revisiting the role of pulmonary surfactant in chronic inflammatory lung diseases and environmental exposure. European Respiratory Review 2021, 30 (162) , 210077. https://doi.org/10.1183/16000617.0077-2021
    21. Yan Tian, Yafang Zhang, Yu Wang, Yunxi Chen, Weiping Fan, Jianjun Zhou, Jing Qiao, Youzhen Wei. Hydrogen, a Novel Therapeutic Molecule, Regulates Oxidative Stress, Inflammation, and Apoptosis. Frontiers in Physiology 2021, 12 https://doi.org/10.3389/fphys.2021.789507
    22. Jeffrey Atkinson, Drew Marquardt, Mitchell DiPasquale, Thad Harroun. From fat to bilayers: Understanding where and how vitamin E works. Free Radical Biology and Medicine 2021, 176 , 73-79. https://doi.org/10.1016/j.freeradbiomed.2021.09.015
    23. Alexander J. Kaiser, Cassie Salem, Bob J. Alvarenga, Anthony Pagliaro, Kelly P. Smith, Luis G. Valerio, Kambez H. Benam. A robotic system for real-time analysis of inhaled submicron and microparticles. iScience 2021, 24 (10) , 103091. https://doi.org/10.1016/j.isci.2021.103091
    24. Clive Bates. The outbreak of lung injuries often known as "EVALI" was nothing to do with nicotine vaping. Qeios 2021, https://doi.org/10.32388/ZGVHM7.3
    25. Clive Bates. The outbreak of lung injuries often known as "EVALI" was nothing to do with nicotine vaping. Qeios 2021, https://doi.org/10.32388/ZGVHM7.2
    26. Ryan Feldman, Matthew Stanton, Elizabeth M. Suelzer. Compiling Evidence for EVALI: A Scoping Review of In Vivo Pulmonary Effects After Inhaling Vitamin E or Vitamin E Acetate. Journal of Medical Toxicology 2021, 17 (3) , 278-288. https://doi.org/10.1007/s13181-021-00823-w
    27. Samantha R. McDonough, Irfan Rahman, Isaac Kirubakaran Sundar. Recent updates on biomarkers of exposure and systemic toxicity in e-cigarette users and EVALI. American Journal of Physiology-Lung Cellular and Molecular Physiology 2021, 320 (5) , L661-L679. https://doi.org/10.1152/ajplung.00520.2020
    28. Maria Morel Espinosa, Benjamin C. Blount, Liza Valentin-Blasini. Liquid chromatography-tandem mass spectrometry method for measuring vitamin E acetate in bronchoalveolar lavage fluid. Journal of Chromatography B 2021, 1171 , 122607. https://doi.org/10.1016/j.jchromb.2021.122607
    29. Karin Jacobson, Javier Martinez, Sylvain Larroque, Ian W. Jones, Thilo Paschke. Nicotine pharmacokinetics of electronic cigarettes: A pooled data analysis from the literature. Toxicology Reports 2021, 8 , 84-95. https://doi.org/10.1016/j.toxrep.2020.12.016
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