Electronic cigarettes and insulin resistance in animals and humans: Results of a controlled animal study and the National Health and Nutrition Examination Survey (NHANES 2013-2016)

Autoři: Olusola A. Orimoloye aff001;  S. M. Iftekhar Uddin aff001;  Lung-Chi Chen aff002;  Albert D. Osei aff001;  Mohammadhassan Mirbolouk aff001;  Marina V. Malovichko aff002;  Israel D. Sithu aff002;  Omar Dzaye aff001;  Daniel J. Conklin aff002;  Sanjay Srivastava aff002;  Michael J. Blaha aff001
Působiště autorů: Johns Hopkins Ciccarone Center for the Prevention of Cardiovascular Disease, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America aff001;  American Heart Association Tobacco Regulation and Addiction Center, Dallas, Texas, United States of America aff002;  Department of Environmental Medicine, New York University School of Medicine, Tuxedo, New York, United States of America aff003;  Envirome Institute, University of Louisville, Louisville, Kentucky, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0226744



The popularity of electronic cigarettes (E-cigarettes) has risen considerably. Several studies have suggested that nicotine may affect insulin resistance, however, the impact of E-cigarette exposure on insulin resistance, an early measure of cardiometabolic risk, is not known.

Methods and results

Using experimental animals and human data obtained from 3,989 participants of the United States National Health and Nutrition Examination Survey (NHANES), respectively, we assessed the association between E-cigarette and conventional cigarette exposures and insulin resistance, as modelled using the homeostatic model assessment of insulin resistance (HOMA-IR) and glucose tolerance tests (GTT). C57BL6/J mice (on standard chow diet) exposed to E-cigarette aerosol or mainstream cigarette smoke (MCS) for 12 weeks showed HOMA-IR and GTT levels comparable with filtered air-exposed controls. In the NHANES cohort, there was no significant association between defined tobacco product use categories (non-users; sole E-cigarette users; cigarette smokers and dual users) and insulin resistance. Compared with non-users of e-cigarettes/conventional cigarettes, sole E-cigarette users showed no significant difference in HOMA-IR or GTT levels following adjustment for age, sex, race, physical activity, alcohol use and BMI.


E-cigarettes do not appear to be linked with insulin resistance. Our findings may inform future studies assessing potential cardiometabolic harms associated with E-cigarette use.

Klíčová slova:

Animal studies – Electronic cigarettes – Glucose tolerance tests – Insulin – Mouse models – Smoking habits – Urine


1. National Academies of Sciences and Medicine E. Public health consequences of e-cigarettes. Washington, DC Natl Acad Press doi. 2018;10: 24952.

2. Dinakar C, O’Connor GT. The Health Effects of Electronic Cigarettes. N Engl J Med. 2016;375: 1372–1381. doi: 10.1056/NEJMra1502466 27705269

3. Grana R, Benowitz N, Glantz SA. E-Cigarettes. Circulation. 2014;129: 1972 LP–1986. http://circ.ahajournals.org/content/129/19/1972.abstract

4. Coleman BN, Rostron B, Johnson SE, Ambrose BK, Pearson J, Stanton CA, et al. Electronic cigarette use among US adults in the Population Assessment of Tobacco and Health (PATH) Study, 2013–2014. Tobacco Control. 2017.

5. Jaber R, Health B, Florida S, Mirbolouk M, Medicine JH, Defilippis A, et al. Electronic Cigarette Use Prevalence, Associated Factors, and Pattern by Cigarette Smoking Status in the United States From NHANES (National Health and Nutrition Examination Survey) 2013–2014. J Am Heart Assoc. 2018.

6. Mirbolouk M, Charkhchi P, Kianoush S, et al. Prevalence and distribution of e-cigarette use among u.s. adults: Behavioral risk factor surveillance system, 2016. Ann Intern Med. 2018. http://dx.doi.org/10.7326/M17-3440

7. Goniewicz ML, Knysak J, Gawron M, Kosmider L, Sobczak A, Kurek J, et al. Levels of selected carcinogens and toxicants in vapour from electronic cigarettes. Tob Control. 2014;23: 133–139. doi: 10.1136/tobaccocontrol-2012-050859 23467656

8. Shahab L, Goniewicz ML, Blount BC, Brown J, McNeill A, Udeni Alwis K, et al. Nicotine, carcinogen, and toxin exposure in long-Term e-cigarette and nicotine replacement therapy users. Ann Intern Med. 2017;166: 390–400. doi: 10.7326/M16-1107 28166548

9. Martin EM, Clapp PW, Rebuli ME, Pawlak EA, Glista-Baker E, Benowitz NL, et al. E-cigarette use results in suppression of immune and inflammatory-response genes in nasal epithelial cells similar to cigarette smoke. Am J Physiol Cell Mol Physiol. 2016;311: L135–L144.

10. Crotty Alexander LE, Drummond CA, Hepokoski M, Mathew D, Moshensky A, Willeford A, et al. Chronic inhalation of e-cigarette vapor containing nicotine disrupts airway barrier function and induces systemic inflammation and multiorgan fibrosis in mice. Am J Physiol Integr Comp Physiol. 2018;314: R834–R847.

11. Chaumont M, de Becker B, Zaher W, Culié A, Deprez G, Mélot C, et al. Differential Effects of E-Cigarette on Microvascular Endothelial Function, Arterial Stiffness and Oxidative Stress: A Randomized Crossover Trial. Sci Rep. 2018;8: 10378. doi: 10.1038/s41598-018-28723-0 29991814

12. Qasim H, Karim ZA, Silva‐Espinoza JC, Khasawneh FT, Rivera JO, Ellis CC, et al. Short‐Term E‐Cigarette Exposure Increases the Risk of Thrombogenesis and Enhances Platelet Function in Mice. J Am Heart Assoc. 2018;7.

13. Benowitz NL, Burbank AD. Cardiovascular toxicity of nicotine: Implications for electronic cigarette use. Trends in Cardiovascular Medicine. 2016. pp. 515–523. doi: 10.1016/j.tcm.2016.03.001 27079891

14. Wu Y, Song P, Zhang W, Liu J, Dai X, Liu Z, et al. Activation of AMPKα2 in adipocytes is essential for nicotine-induced insulin resistance in vivo. Nat Med. 2015;21: 373–382. doi: 10.1038/nm.3826 25799226

15. Willi C, Bodenmann P, Ghali WA, Faris PD, Cornuz J. Active Smoking and the Risk of Type 2 Diabetes. JAMA. 2007;298: 2654. doi: 10.1001/jama.298.22.2654 18073361

16. Sansbury BE, Cummins TD, Tang Y, Hellmann J, Holden CR, Harbeson MA, et al. Overexpression of Endothelial Nitric Oxide Synthase Prevents Diet-Induced Obesity and Regulates Adipocyte Phenotype. Circ Res. 2012;111: 1176–1189. doi: 10.1161/CIRCRESAHA.112.266395 22896587

17. Conklin DJ, Malovichko MV, Zeller I, Das TP, Krivokhizhina TV, Lynch BH, et al. Biomarkers of Chronic Acrolein Inhalation Exposure in Mice: Implications for Tobacco Product-Induced Toxicity. Toxicol Sci. 2017;158: 263–274. http://dx.doi.org/10.1093/toxsci/kfx095 28482051

18. Malovichko M V, Zeller I, Krivokhizhina T V, Xie Z, Lorkiewicz P, Agarwal A, et al. Systemic Toxicity of Smokeless Tobacco Products in Mice. Nicotine Tob Res. 2017 [cited 24 Aug 2018].

19. NHANES—Survey Methods and Analytic Guidelines. [cited 24 Aug 2018]. https://wwwn.cdc.gov/nchs/nhanes/analyticguidelines.aspx

20. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care. 2004. pp. 1487–1495. doi: 10.2337/diacare.27.6.1487 15161807

21. Conklin DJ, Haberzettl P, Jagatheesan G, Kong M, Hoyle GW. Role of TRPA1 in acute cardiopulmonary toxicity of inhaled acrolein. Toxicol Appl Pharmacol. 2017.

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2019 Číslo 12