The effects of electronic cigarette aerosol exposure on inflammation and lung function in mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 313, Issue 1, 2017, Pages L67-L79

  Larcombe, Alexander N ^a,b   Janka, Maxine A ^a   Mullins, Benjamin J ^b   Berry, Luke J ^a   Bredin, Arne ^b   Franklin, Peter J ^c,d  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b CURTIN UNIVERSITY   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d DEPARTMENT OF HEALTH   (Australia)

Author keywords

Airway hyperresponsiveness; Electronic cigarette; Inflammation; Lung function

Indexed keywords

CIGARETTE SMOKE; EOTAXIN; GAMMA INTERFERON; GLYCEROL; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 9; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; METHACHOLINE; MONOCYTE CHEMOTACTIC PROTEIN 1; NICOTINE; PROPYLENE GLYCOL; RANTES; TOBACCO SMOKE; TUMOR NECROSIS FACTOR; AEROSOL; AUTACOID; METHACHOLINE CHLORIDE;

ADULT; AEROSOL; AIR QUALITY CONTROL; AIRWAY RESISTANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRONIC CIGARETTE; FEMALE; FUNCTIONAL RESIDUAL CAPACITY; HISTOLOGY; LIMIT OF QUANTITATION; LUNG COMPLIANCE; LUNG FUNCTION; LUNG LAVAGE; LUNG MECHANICS; LUNG VOLUME; MOUSE; NONHUMAN; PLETHYSMOGRAPHY; PNEUMONIA; POSITIVE END EXPIRATORY PRESSURE; PRESSURE VOLUME CURVE; PRIORITY JOURNAL; RESPIRATORY TRACT ALLERGY; ADVERSE EFFECTS; ANIMAL; BAGG ALBINO MOUSE; BODY WEIGHT; COMPLICATION; DRUG EFFECTS; ELASTICITY; INFLAMMATION; LUNG; MASS FRAGMENTOGRAPHY; METABOLISM; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; SMOKING; THORAX;

AEROSOLS; AIRWAY RESISTANCE; ANIMALS; BODY WEIGHT; ELASTICITY; ELECTRONIC CIGARETTES; FEMALE; FUNCTIONAL RESIDUAL CAPACITY; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; INFLAMMATION; INFLAMMATION MEDIATORS; LUNG; METHACHOLINE CHLORIDE; MICE, INBRED BALB C; ORGAN SIZE; PLETHYSMOGRAPHY; RESPIRATORY HYPERSENSITIVITY; SMOKING; THORAX;

EID: 85021781745     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00203.2016     Document Type: Article

References (53)

1. Albanes D, Jones DY, Micozzi MS, Mattson ME. Associations between smoking and body weight in the US population: analysis of NHANES II. Am J Public Health 77: 439-444, 1987. doi:10.2105/AJPH.77.4.439.
2. Blanchet MR, Israël-Assayag E, Cormier Y. Modulation of airway inflammation and resistance in mice by a nicotinic receptor agonist. Eur Respir J 26: 21-27, 2005. doi:10.1183/09031936.05.00116104.
3. Cakmak S, Dales RE, Liu L, Kauri LM, Lemieux CL, Hebbern C, Zhu J. Residential exposure to volatile organic compounds and lung function: results from a population-based cross-sectional survey. Environ Pollut 194: 145-151, 2014. doi:10.1016/j.envpol.2014.07.020.
4. Card JW, Carey MA, Bradbury JA, DeGraff LM, Morgan DL, Moorman MP, Flake GP, Zeldin DC. Gender differences in murine airway responsiveness and lipopolysaccharide-induced inflammation. J Immunol 177: 621-630, 2006. doi:10.4049/jimmunol.177.1.621.
5. Centers for Disease Control and Prevention. CDC. National Youth Tobacco Survey. Atlanta, GA: US Dept of Health and Human Services, CDC, 2013.
6. Cheng T. Chemical evaluation of electronic cigarettes. Tob Control 23, Suppl 2: ii11-ii17, 2014. doi:10.1136/tobaccocontrol-2013-051482.
7. Choi H, Schmidbauer N, Sundell J, Hasselgren M, Spengler J, Bornehag C-G. Common household chemicals and the allergy risks in preschool age children. PLoS One 5: e13423, 2010. doi:10.1371/journal.pone.0013423.
8. Etter JF, Bullen C. Electronic cigarette: users profile, utilization, satisfaction and perceived efficacy. Addiction 106: 2017-2028, 2011. doi:10.1111/j.1360-0443.2011.03505.x.
9. Famele M, Ferranti C, Abenavoli C, Palleschi L, Mancinelli R, Draisci R. The chemical components of electronic cigarette cartridges and refill fluids: review of analytical methods. Nicotine Tob Res 17: 271-279, 2015. doi:10.1093/ntr/ntu197.
10. Foong RE, Sly PD, Larcombe AN, Zosky GR. No role for neutrophil elastase in influenza-induced cellular recruitment, cytokine production or airway hyperresponsiveness in mice. Respir Physiol Neurobiol 173: 164-170, 2010. doi:10.1016/j.resp.2010.08.003.
11. Geraghty P, Dabo J, Garcia-Arcos I, Cummins N, Foronjy R. Latebreaking abstract: e-cigarette exposure induces pathological responses that result in lung tissue destruction and airway hyper reactivity in mice (Abstract). Eur Respir J 44: 3435, 2014.
12. Goldsmith Caroll-Ann W. Particulate air pollution and asthma: a review of epidemiological and biological studies. Rev Environ Health 14: 121-134, 1999. doi:10.1515/REVEH.1999.14.3.121.
13. Goniewicz ML, Knysak J, Gawron M, Kosmider L, Sobczak A, Kurek J, Prokopowicz A, Jablonska-Czapla M, Rosik-Dulewska C, Havel C, Jacob P III, Benowitz N. Levels of selected carcinogens and toxicants in vapour from electronic cigarettes. Tob Control 23: 133-139, 2014. doi: 10.1136/tobaccocontrol-2012-050859.
14. Hansson L, Choudry NB, Karlsson JA, Fuller RW. Inhaled nicotine in humans: effect on the respiratory and cardiovascular systems. J Appl Physiol (1985) 76: 2420-2427, 1994.
15. Hwang JH, Lyes M, Sladewski K, Enany S, McEachern E, Mathew DP, Das S, Moshensky A, Bapat S, Pride DT, Ongkeko WM, Crotty Alexander LE. Electronic cigarette inhalation alters innate immunity and airway cytokines while increasing the virulence of colonizing bacteria. J Mol Med (Berl) 94: 667-679, 2016. doi:10.1007/s00109-016-1378-3.
16. James AL, Hogg JC, Dunn LA, Paré PD. The use of the internal perimeter to compare airway size and to calculate smooth muscle shortening. Am Rev Respir Dis 138: 136-139, 1988. doi:10.1164/ajrccm/138.1.136.
17. Jánosi TZ, Adamicza A, Zosky GR, Asztalos T, Sly PD, Hantos Z. Plethysmographic estimation of thoracic gas volume in apneic mice. J Appl Physiol (1985) 101: 454-459, 2006. doi:10.1152/japplphysiol.00011.2006.
18. Johnson T, Cabot R, Yerteri C, Treacy C, Dickens C, McAughey J, Symonds J, Olfert J. Revisiting cigarette smoke density measurements using a DMA and CPMA. Inhaled Particles XI: Nottingham, UK: September 23-25, 2013: Poster: 0085.
19. Kennedy DJ, Vetteth S, Periyasamy SM, Kanj M, Fedorova L, Khouri S, Kahaleh MB, Xie Z, Malhotra D, Kolodkin NI, Lakatta EG, Fedorova OV, Bagrov AY, Shapiro JI. Central role for the cardiotonic steroid marinobufagenin in the pathogenesis of experimental uremic cardiomyopathy. Hypertension 47: 488-495, 2006. doi:10.1161/01.HYP.0000202594.82271.92.
20. Knudsen L, Weibel ER, Gundersen HJ, Weinstein FV, Ochs M. Assessment of air space size characteristics by intercept (chord) measurement: an accurate and efficient stereological approach. J Appl Physiol (1985) 108: 412-421, 2010. doi:10.1152/japplphysiol.01100.2009.
21. LaKind JS, McKenna EA, Hubner RP, Tardiff RG. A review of the comparative mammalian toxicity of ethylene glycol and propylene glycol. Crit Rev Toxicol 29: 331-365, 1999. doi:10.1080/10408449991349230.
22. Larcombe AN, Foong RE, Berry LJ, Zosky GR, Sly PD. In utero cigarette smoke exposure impairs somatic and lung growth in BALB/c mice. Eur Respir J 38: 932-938, 2011. doi:10.1183/09031936.00156910.
23. Larcombe AN, Foong RE, Bozanich EM, Berry LJ, Garratt LW, Gualano RC, Jones JE, Dousha LF, Zosky GR, Sly PD. Sexual dimorphism in lung function responses to acute influenza A infection. Influenza Other Respi Viruses 5: 334-342, 2011. doi:10.1111/j.1750-2659.2011.00236.x.
24. Larcombe AN, Zosky GR, Bozanich EM, Turner DJ, Hantos Z, Sly PD. Absence of cholinergic airway tone in normal BALB/c mice. Respir Physiol Neurobiol 161: 223-229, 2008. doi:10.1016/j.resp.2008.01.009.
25. Lee S, Grana RA, Glantz SA. Electronic cigarette use among Korean adolescents: a cross-sectional study of market penetration, dual use, and relationship to quit attempts and former smoking. J Adolesc Health 54: 684-690, 2014. doi:10.1016/j.jadohealth.2013.11.003.
26. Lerner CA, Sundar IK, Yao H, Gerloff J, Ossip DJ, McIntosh S, Robinson R, Rahman I. Vapors produced by electronic cigarettes and e-juices with flavorings induce toxicity, oxidative stress, and inflammatory response in lung epithelial cells and in mouse lung. PLoS One 10: e0116732, 2015. doi:10.1371/journal.pone.0116732.
27. Lim HB, Kim SH. Inhallation of e-cigarette cartridge solution aggravates allergen-induced airway inflammation and hyper-responsiveness in mice. Toxicol Res 30: 13-18, 2014. doi:10.5487/TR.2014.30.1.013.
28. Lundblad LK, Irvin CG, Hantos Z, Sly P, Mitzner W, Bates JH. Penh is not a measure of airway resistance! Eur Respir J 30: 805, 2007. doi:10.1183/09031936.00091307.
29. Lutchen KR, Gillis H. Relationship between heterogeneous changes in airway morphometry and lung resistance and elastance. J Appl Physiol (1985) 83: 1192-1201, 1997.
30. Lutchen KR, Greenstein JL, Suki B. How inhomogeneities and airway walls affect frequency dependence and separation of airway and tissue properties. J Appl Physiol (1985) 80: 1696-1707, 1996.
31. Lutchen KR, Hantos Z, Peták F, Adamicza A, Suki B. Airway inhomogeneities contribute to apparent lung tissue mechanics during constriction. J Appl Physiol (1985) 80: 1841-1849, 1996.
32. McCauley L, Markin C, Hosmer D. An unexpected consequence of electronic cigarette use. Chest 141: 1110-1113, 2012. doi:10.1378/chest.11-1334.
33. Mendell MJ. Indoor residential chemical emissions as risk factors for respiratory and allergic effects in children: a review. Indoor Air 17: 259-277, 2007. doi:10.1111/j.1600-0668.2007.00478.x.
34. Mineur YS, Abizaid A, Rao Y, Salas R, DiLeone RJ, Gündisch D, Diano S, De Biasi M, Horvath TL, Gao XB, Picciotto MR. Nicotine decreases food intake through activation of POMC neurons. Science 332: 1330-1332, 2011. doi:10.1126/science.1201889.
35. Moline JM, Golden AL, Highland JH, Wilmarth KR, Kao AS. Health Effects Evaluation of Theatrical Smoke, Haze, and Pyrotechnics. New York: Equity-League Pension and Health Trust Funds, 2000.
36. Nielsen GD, Larsen ST, Olsen O, Løvik M, Poulsen LK, Glue C, Wolkoff P. Do indoor chemicals promote development of airway allergy? Indoor Air 17: 236-255, 2007. doi:10.1111/j.1600-0668.2006.00468.x.
37. Oberdörster G, Gelein RM, Ferin J, Weiss B. Association of particulate air pollution and acute mortality: involvement of ultrafine particles? Inhal Toxicol 7: 111-124, 1995. doi:10.3109/08958379509014275.
38. Palamidas A, Gennimata S, Kaltsakas G, Tsikrika S, Vakali S, Gratziou C, Koulouris N. Acute effect of an e-cigarette with and without nicotine on lung function (Abstract). Eur Resp J, 42, Suppl 57: P1054, 2013.
39. Peták F, Hantos Z, Adamicza A, Asztalos T, Sly PD. Methacholineinduced bronchoconstriction in rats: effects of intravenous vs. aerosol delivery. J Appl Physiol (1985) 82: 1479-1487, 1997.
40. Pinkerton KE, Joad JP. The mammalian respiratory system and critical windows of exposure for children’s health. Environ Health Perspect 108, Suppl 3: 457-462, 2000. doi:10.1289/ehp.00108s3457.
41. Pisinger C, Døssing M. A systematic review of health effects of electronic cigarettes. Prev Med 69: 248-260, 2014. doi:10.1016/j.ypmed.2014.10.009.
42. Pope CA III. Epidemiology of fine particulate air pollution and human health: biologic mechanisms and who’s at risk? Environ Health Perspect 108, Suppl 4: 713-723, 2000. doi:10.2307/3454408.
43. Ramsey KA, Bosco A, McKenna KL, Carter KW, Elliot JG, Berry LJ, Sly PD, Larcombe AN, Zosky GR. In utero exposure to arsenic alters lung development and genes related to immune and mucociliary function in mice. Environ Health Perspect 121: 244-250, 2013. 10.1289/ehp.1205590.
44. Renne R, Wehner A, Greenspan B, Deford H, Ragan H, Westerberg R, Buschbom R, Burger G, Hayes A, Suber R, Mosberg AT. 2-Week and 13-week inhalation studies of aerosolized glycerol in rats. Inhal Toxicol 4: 95-111, 1992. doi:10.3109/08958379209145307.
45. Schraufnagel DE, Blasi F, Drummond MB, Lam DCL, Latif E, Rosen MJ, Sansores R, Van Zyl-Smit R; Forum of International Respiratory Societies. Electronic cigarettes. A position statement of the forum of international respiratory societies. Am J Respir Crit Care Med 190: 611-618, 2014. doi:10.1164/rccm.201407-1198PP.
46. Seaton A, MacNee W, Donaldson K, Godden D. Particulate air pollution and acute health effects. Lancet 345: 176-178, 1995. doi:10.1016/S0140-6736(95)90173-6.
47. Sly PD, Collins RA, Thamrin C, Turner DJ, Hantos Z. Volume dependence of airway and tissue impedances in mice. J Appl Physiol (1985) 94: 1460-1466, 2003. doi:10.1152/japplphysiol.00596.2002.
48. Sussan TE, Gajghate S, Thimmulappa RK, Ma J, Kim JH, Sudini K, Consolini N, Cormier SA, Lomnicki S, Hasan F, Pekosz A, Biswal S. Exposure to electronic cigarettes impairs pulmonary anti-bacterial and anti-viral defenses in a mouse model. PLoS One 10: e0116861, 2015. doi:10.1371/journal.pone.0116861.
49. Tantisuwat A, Thaveeratitham P. Effects of smoking on chest expansion, lung function, and respiratory muscle strength of youths. J Phys Ther Sci 26: 167-170, 2014. doi:10.1589/jpts.26.167.
50. Vardavas CI, Anagnostopoulos N, Kougias M, Evangelopoulou V, Connolly GN, Behrakis PK. Short-term pulmonary effects of using an electronic cigarette: impact on respiratory flow resistance, impedance, and exhaled nitric oxide. Chest 141: 1400-1406, 2012. doi:10.1378/chest.11-2443.
51. Weichenthal S, Kulka R, Bélisle P, Joseph L, Dubeau A, Martin C, Wang D, Dales R. Personal exposure to specific volatile organic compounds and acute changes in lung function and heart rate variability among urban cyclists. Environ Res 118: 118-123, 2012. doi:10.1016/j.envres.2012.06.005.
52. Wieslander G, Norbäck D, Lindgren T. Experimental exposure to propylene glycol mist in aviation emergency training: acute ocular and respiratory effects. Occup Environ Med 58: 649-655, 2001. doi:10.1136/oem.58.10.649.
53. Yang Q, Ge MQ, Kokalari B, Redai IG, Wang X, Kemeny DM, Bhandoola A, Haczku A. Group 2 innate lymphoid cells mediate ozoneinduced airway inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol 137: 571-578, 2016. doi:10.1016/j.jaci.2015.06.037.