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Common E-Cigarette Flavoring Chemicals Impair Neutrophil Phagocytosis and Oxidative Burst

  • Elise Hickman
    Elise Hickman
    Curriculum in Toxicology & Environmental Medicine  and  Center for Environmental Medicine, Asthma, and Lung Biology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27514, United States
  • Carolina A. Herrera
    Carolina A. Herrera
    Department of Pathology and Laboratory Medicine, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27514, United States
  • , and 
  • Ilona Jaspers*
    Ilona Jaspers
    Curriculum in Toxicology & Environmental Medicine  and  Center for Environmental Medicine, Asthma, and Lung Biology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27514, United States
    *E-mail: [email protected]
Cite this: Chem. Res. Toxicol. 2019, 32, 6, 982–985
Publication Date (Web):May 22, 2019
https://doi.org/10.1021/acs.chemrestox.9b00171
Copyright © 2019 American Chemical Society

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    Abstract

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    E-cigarette flavorings have not been thoroughly evaluated for inhalational toxicity. We have shown that the flavoring chemical cinnamaldehyde impairs human neutrophils, macrophages, and natural killer cells. Here we investigated the effects of other common e-liquid flavoring chemicals on phagocytosis and oxidative burst in neutrophils. We demonstrate that cinnamaldehyde and ethyl vanillin dose-dependently decrease oxidative burst and that benzaldehyde and benzaldehyde propylene glycol acetal dose-dependently impair phagocytosis. Isoamyl acetate did not affect either measure of neutrophil function. These data suggest that inhaling aromatic aldehydic flavoring chemicals, such as cinnamaldehyde, benzaldehyde, benzaldehyde propylene glycol acetal, or ethyl vanillin, could impair neutrophil function.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.chemrestox.9b00171.

    • Overall study demographics; maximum OCR for each flavoring chemical; time to maximum OCR for each flavoring chemical; maximum ECAR for each flavoring chemical; time to maximum ECAR for each flavoring chemical; IC50 values for neutrophil oxidative burst AUC and phagocytosis; neutrophil oxidative burst rate graphs; neutrophil glycolysis during oxidative burst (PDF)

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    3. Esther E. Omaiye, Wentai Luo, Kevin J. McWhirter, James F. Pankow, Prue Talbot. Disposable Puff Bar Electronic Cigarettes: Chemical Composition and Toxicity of E-liquids and a Synthetic Coolant. Chemical Research in Toxicology 2022, 35 (8) , 1344-1358. https://doi.org/10.1021/acs.chemrestox.1c00423
    4. Paul J. Kerber, David H. Peyton. Kinetics of Aldehyde Flavorant-Acetal Formation in E-Liquids with Different E-Cigarette Solvents and Common Additives Studied by 1H NMR Spectroscopy. Chemical Research in Toxicology 2022, 35 (8) , 1410-1417. https://doi.org/10.1021/acs.chemrestox.2c00159
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    6. Brittany P. Rickard, Henry Ho, Jacqueline B. Tiley, Ilona Jaspers, Kim L. R. Brouwer. E-Cigarette Flavoring Chemicals Induce Cytotoxicity in HepG2 Cells. ACS Omega 2021, 6 (10) , 6708-6713. https://doi.org/10.1021/acsomega.0c05639
    7. Jonas M. Ndeke, James E. Klaunig, Sarah Commodore. Nicotine or marijuana vaping exposure during pregnancy and altered immune responses in offspring. Journal of Environmental Exposure Assessment 2024, 3 (1) https://doi.org/10.20517/jeea.2024.03
    8. Joseph J. Hofmann, Victoria C. Poulos, Jiahai Zhou, Maksym Sharma, Grace Parraga, Marrissa J. McIntosh. Review of quantitative and functional lung imaging evidence of vaping-related lung injury. Frontiers in Medicine 2024, 11 https://doi.org/10.3389/fmed.2024.1285361
    9. Rakesh Sahu, Kamal Shah, Rishabha Malviya, Deepika Paliwal, Sakshi Sagar, Sudarshan Singh, Bhupendra G. Prajapati, Sankha Bhattacharya. E-Cigarettes and Associated Health Risks: An Update on Cancer Potential. Advances in Respiratory Medicine 2023, 91 (6) , 516-531. https://doi.org/10.3390/arm91060038
    10. Jaspreet Sachdeva, Anisha Karunananthan, Jianru Shi, Wangde Dai, Michael T Kleinman, David Herman, Robert A Kloner. Flavoring Agents in E-cigarette Liquids: A Comprehensive Analysis of Multiple Health Risks. Cureus 2023, 107 https://doi.org/10.7759/cureus.48995
    11. Taehyun Roh, Kido Uyamasi, Anisha Aggarwal, Alexander Obeng, Genny Carrillo. Association between e-cigarette use and asthma among US adolescents: Youth Risk Behavior Surveillance System 2015–2019. Preventive Medicine 2023, 175 , 107695. https://doi.org/10.1016/j.ypmed.2023.107695
    12. Peter G. Shields, Kevin L. Ying, Theodore M. Brasky, Jo L. Freudenheim, Zihai Li, Joseph P. McElroy, Sarah A. Reisinger, Min-Ae Song, Daniel Y. Weng, Mark D. Wewers, Noah B. Whiteman, Yiping Yang, Ewy A. Mathé. A Pilot Cross-Sectional Study of Immunological and Microbiome Profiling Reveals Distinct Inflammatory Profiles for Smokers, Electronic Cigarette Users, and Never-Smokers. Microorganisms 2023, 11 (6) , 1405. https://doi.org/10.3390/microorganisms11061405
    13. Thivanka Muthumalage, Irfan Rahman. Pulmonary immune response regulation, genotoxicity, and metabolic reprogramming by menthol- and tobacco-flavored e-cigarette exposures in mice. Toxicological Sciences 2023, 193 (2) , 146-165. https://doi.org/10.1093/toxsci/kfad033
    14. Frances S. Grudzinska, Alice Jasper, Elizabeth Sapey, David R. Thickett, Claudio Mauro, Aaron Scott, Jonathan Barlow. Real-time assessment of neutrophil metabolism and oxidative burst using extracellular flux analysis. Frontiers in Immunology 2023, 14 https://doi.org/10.3389/fimmu.2023.1083072
    15. Elise Hickman, Timothy Smyth, Catalina Cobos-Uribe, Robert Immormino, Meghan E. Rebuli, Timothy Moran, Neil E. Alexis, Ilona Jaspers, . Expanded characterization of in vitro polarized M0, M1, and M2 human monocyte-derived macrophages: Bioenergetic and secreted mediator profiles. PLOS ONE 2023, 18 (3) , e0279037. https://doi.org/10.1371/journal.pone.0279037
    16. Lauren Kass Lempert, Bonnie Halpern-Felsher. Adolescent E-cigarette use: Rates, concerns, and policy implications. 2023, 374-387. https://doi.org/10.1016/B978-0-12-818872-9.00139-4
    17. Marissa Love, Selina Gierer. Electronic Cigarettes and Vaping in Allergic and Asthmatic Disease. Immunology and Allergy Clinics of North America 2022, 42 (4) , 787-800. https://doi.org/10.1016/j.iac.2022.06.002
    18. Michelle K Page, Ashleigh C Block, Angel L Santiago, Noel J Leigh, Lisa M Kaiser, Connor D Martin, Bradley E Schurr, Richard J O'Connor, Maciej L Goniewicz. Changes in product labelling practices and the use of flavouring chemical additives in vaping products after enactment of statewide flavour legislation. Tobacco Control 2022, 31 (Suppl 3) , s223-s229. https://doi.org/10.1136/tc-2022-057469
    19. Guy Lalonde, Kubilay Demir, Jenny Yao, Russell L. Wolz, Pasha Kosachevsky, I. Gene Gillman, Michael J. Oldham. Characterization of a rapid condensate collection apparatus for in vitro assays of electronic nicotine delivery systems. Toxicology in Vitro 2022, 84 , 105434. https://doi.org/10.1016/j.tiv.2022.105434
    20. Alys Havard, Jonathan James Chandran, Ju Lee Oei. Tobacco use during pregnancy. Addiction 2022, 117 (6) , 1801-1810. https://doi.org/10.1111/add.15792
    21. Alayna P Tackett, Meghan E Rebuli. Alternative Flavored Inhalable Products—A New Respiratory Hazard?. Toxicological Sciences 2022, 187 (1) , 1-2. https://doi.org/10.1093/toxsci/kfac021
    22. Alexander Larcombe, Sebastien Allard, Paul Pringle, Ryan Mead‐Hunter, Natalie Anderson, Benjamin Mullins. Chemical analysis of fresh and aged Australian e‐cigarette liquids. Medical Journal of Australia 2022, 216 (1) , 27-32. https://doi.org/10.5694/mja2.51280
    23. Terry Gordon, Emma Karey, Meghan E. Rebuli, Yael-Natalie H. Escobar, Ilona Jaspers, Lung Chi Chen. E-Cigarette Toxicology. Annual Review of Pharmacology and Toxicology 2022, 62 (1) , 301-322. https://doi.org/10.1146/annurev-pharmtox-042921-084202
    24. Anand Ranpara, Aleksandr B. Stefaniak, Kenneth Williams, Elizabeth Fernandez, Ryan F. LeBouf. Modeled Respiratory Tract Deposition of Aerosolized Oil Diluents Used in Δ9-THC-Based Electronic Cigarette Liquid Products. Frontiers in Public Health 2021, 9 https://doi.org/10.3389/fpubh.2021.744166
    25. Anna M. Morris, Stephen S. Leonard, Jefferson R. Fowles, Theresa E. Boots, Anna Mnatsakanova, Kathleen R. Attfield. Effects of E-Cigarette Flavoring Chemicals on Human Macrophages and Bronchial Epithelial Cells. International Journal of Environmental Research and Public Health 2021, 18 (21) , 11107. https://doi.org/10.3390/ijerph182111107
    26. Michelle K. Page, Maciej L. Goniewicz. New Analytical Method for Quantifying Flavoring Chemicals of Potential Respiratory Health Risk Concerns in e-Cigarette Liquids. Frontiers in Chemistry 2021, 9 https://doi.org/10.3389/fchem.2021.763940
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    28. Aleksandr B. Stefaniak, Ryan F. LeBouf, Anand C. Ranpara, Stephen S. Leonard. Toxicology of flavoring- and cannabis-containing e-liquids used in electronic delivery systems. Pharmacology & Therapeutics 2021, 224 , 107838. https://doi.org/10.1016/j.pharmthera.2021.107838
    29. Jacob A. Kaslow, Christian Rosas‐Salazar, Paul E. Moore. E‐cigarette and vaping product use‐associated lung injury in the pediatric population: A critical review of the current literature. Pediatric Pulmonology 2021, 56 (7) , 1857-1867. https://doi.org/10.1002/ppul.25384
    30. Rachel Keith, Aruni Bhatnagar. Cardiorespiratory and Immunologic Effects of Electronic Cigarettes. Current Addiction Reports 2021, 8 (2) , 336-346. https://doi.org/10.1007/s40429-021-00359-7
    31. M. P. Ween, A. Moshensky, L. Thredgold, N. A. Bastian, R. Hamon, A. Badiei, P. T. Nguyen, K. Herewane, H. Jersmann, C. M. Bojanowski, J. Shin, P. N. Reynolds, L. E. Crotty Alexander, S. J. Hodge. E-cigarettes and health risks: more to the flavor than just the name. American Journal of Physiology-Lung Cellular and Molecular Physiology 2021, 320 (4) , L600-L614. https://doi.org/10.1152/ajplung.00370.2020
    32. Michelle L. Hernandez, Allison J. Burbank, Neil E. Alexis, Meghan E. Rebuli, Elise D. Hickman, Ilona Jaspers, Guillermo Guidos. Electronic Cigarettes and Their Impact on Allergic Respiratory Diseases: A Work Group Report of the AAAAI Environmental Exposures and Respiratory Health Committee. The Journal of Allergy and Clinical Immunology: In Practice 2021, 9 (3) , 1142-1151. https://doi.org/10.1016/j.jaip.2020.12.065
    33. Madhur D. Shastri, Shakti D. Shukla, Wai Chin Chong, Rajendra KC, Kamal Dua, Rahul P. Patel, Gregory M. Peterson, Ronan F. O'Toole. Smoking and COVID-19: What we know so far. Respiratory Medicine 2021, 176 , 106237. https://doi.org/10.1016/j.rmed.2020.106237
    34. Meghan E. Rebuli, Ellen Glista-Baker, Jessica R. Hoffman, Parker F. Duffney, Carole Robinette, Adam M. Speen, Erica A. Pawlak, Radhika Dhingra, Terry L. Noah, Ilona Jaspers. Electronic-Cigarette Use Alters Nasal Mucosal Immune Response to Live-attenuated Influenza Virus. A Clinical Trial. American Journal of Respiratory Cell and Molecular Biology 2021, 64 (1) , 126-137. https://doi.org/10.1165/rcmb.2020-0164OC
    35. Thomas A. Wills, Samir S. Soneji, Kelvin Choi, Ilona Jaspers, Elizabeth K. Tam. E-cigarette use and respiratory disorders: an integrative review of converging evidence from epidemiological and laboratory studies. European Respiratory Journal 2021, 57 (1) , 1901815. https://doi.org/10.1183/13993003.01815-2019
    36. Zahira Quinones Tavarez, Dongmei Li, Daniel P. Croft, Steven R. Gill, Deborah J. Ossip, Irfan Rahman. The Interplay Between Respiratory Microbiota and Innate Immunity in Flavor E-Cigarette Vaping Induced Lung Dysfunction. Frontiers in Microbiology 2020, 11 https://doi.org/10.3389/fmicb.2020.589501
    37. Sairam V Jabba, Alexandra N Diaz, Hanno C Erythropel, Julie B Zimmerman, Sven-Eric Jordt. Chemical Adducts of Reactive Flavor Aldehydes Formed in E-Cigarette Liquids Are Cytotoxic and Inhibit Mitochondrial Function in Respiratory Epithelial Cells. Nicotine & Tobacco Research 2020, 22 (Supplement_1) , S25-S34. https://doi.org/10.1093/ntr/ntaa185
    38. Teresa I. Fortoul van der Goes. Hacer un hoyo, para tapar otro. Revista de la Facultad de Medicina 2020, 63 (6) , 3-6. https://doi.org/10.22201/fm.24484865e.2020.63.6.01
    39. Elise Hickman, Ilona Jaspers. Current E-Cigarette Research in the Context of Asthma. Current Allergy and Asthma Reports 2020, 20 (10) https://doi.org/10.1007/s11882-020-00952-2
    40. Ariane Lechasseur, Mathieu C. Morissette. The fog, the attractive and the addictive: pulmonary effects of vaping with a focus on the contribution of each major vaping liquid constituent. European Respiratory Review 2020, 29 (157) , 200268. https://doi.org/10.1183/16000617.0268-2020
    41. Silke Schmidt. 关注电子烟独有的毒性特征. Environmental Health Perspectives (Chinese) 2020, 128 (3) https://doi.org/10.1289/EHP6628-zh
    42. Jack Bozier, Emily K. Chivers, David G. Chapman, Alexander N. Larcombe, Nicole A. Bastian, Jorge A. Masso-Silva, Min Kwang Byun, Christine F. McDonald, Laura E. Crotty Alexander, Miranda P. Ween. The Evolving Landscape of e-Cigarettes. Chest 2020, 157 (5) , 1362-1390. https://doi.org/10.1016/j.chest.2019.12.042
    43. Silke Schmidt. Vaper, Beware: The Unique Toxicological Profile of Electronic Cigarettes. Environmental Health Perspectives 2020, 128 (5) https://doi.org/10.1289/EHP6628
    44. Joanna A. Ruszkiewicz, Ziyan Zhang, Filipe Marques Gonçalves, Yousef Tizabi, Judith T. Zelikoff, Michael Aschner. Neurotoxicity of e-cigarettes. Food and Chemical Toxicology 2020, 138 , 111245. https://doi.org/10.1016/j.fct.2020.111245
    45. Hassan El Chebib, Kiah McArthur, Michelle Gorbonosov, Joseph B. Domachowske. Anaerobic Necrotizing Pneumonia: Another Potential Life-threatening Complication of Vaping?. Pediatrics 2020, 145 (4) https://doi.org/10.1542/peds.2019-3204
    46. Anne Griffiths, Anna Rauzi, Katie Stadheim, William Wheeler. Lung Injury Associated with E-Cigarette or Vaping Product Use. Pediatric Annals 2020, 49 (2) https://doi.org/10.3928/19382359-20200120-01
    47. Robert M. Greene, M. Michele Pisano. Developmental toxicity of e‐cigarette aerosols. Birth Defects Research 2019, 111 (17) , 1294-1301. https://doi.org/10.1002/bdr2.1571

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