Pharmacological and physiological response in Apoe^−/− mice exposed to cigarette smoke or e-cigarette aerosols

References

• Alderman SL, Ingebrethsen BJ. 2011. Characterization of mainstream cigarette smoke particle size distributions from commercial cigarettes using a DMS500 fast particulate spectrometer and smoking cycle simulator. Aerosol Sci Technol. 45(12):1409–1421.
   Web of Science ®Google Scholar
• Asgharian B, Price OT, Oldham M, Chen LC, Saunders EL, Gordon T, Mikheev VB, Minard KR, Teeguarden JG. 2014. Computational modeling of nanoscale and microscale particle deposition, retention and dosimetry in the mouse respiratory tract. Inhal Toxicol. 26(14):829–842.
   PubMed Web of Science ®Google Scholar
• Benowitz N, Hukkanen J, Jacob IP. 2009. Nicotine chemistry metabolism and kinetics and biomarkers. Handb Exp Pharmacol. 192:29–60.
   PubMedGoogle Scholar
• Benowitz NL, Burbank AD. 2016. Cardiovascular toxicity of nicotine: implications for electronic cigarette use. Trends Cardiovasc Med. 26(6):515–523.
   PubMed Web of Science ®Google Scholar
• Benowitz NL, St. Helen G, Liakoni E. 2021. Clinical pharmacology of electronic nicotine delivery systems (ENDS): implications for benefits and risks in the promotion of the combusted tobacco endgame. J Clin Pharmacol. 61(S2):S18–S36.
   PubMedGoogle Scholar
• Catanzaro DF, Zhou Y, Chen R, Yu F, Catanzaro SE, De Lorenzo MS, Subbaramaiah K, Zhou XK, Pratico D, Dannenberg AJ, et al. 2007. Potentially reduced exposure cigarettes accelerate atherosclerosis: evidence for the role of nicotine. Cardiovasc Toxicol. 7(3):192–201.
   PubMedGoogle Scholar
• Choi J-I, Kim CS. 2007. Mathematical analysis of particle deposition in human lungs: an improved single path transport model. Inhal Toxicol. 19(11):925–939.
   PubMed Web of Science ®Google Scholar
• Creamer MLR, Wang TW, Babb S, Cullen KA, Day H, Willis G, Jamal A, Neff L. 2019. Tobacco product use and cessation indicators among adults – United States, 2018. MMWR Morb Mortal Wkly Rep. 68(45):1013–1019.
   PubMed Web of Science ®Google Scholar
• Crotty Alexander LE, Drummond CA, Hepokoski M, Mathew D, Moshensky A, Willeford A, Das S, Singh P, Yong Z, Lee JH, et al. 2018. Chronic inhalation of e-cigarette vapor containing nicotine disrupts airway barrier function and induces systemic inflammation and multiorgan fibrosis in mice. Am J Physiol – Regul Integr Comp Physiol. 314(6):R834–R847.
   PubMed Web of Science ®Google Scholar
• Cullen KA, Gentzke AS, Sawdey MD, Chang JT, Anic GM, Wang TW, Creamer MR, Jamal A, Ambrose BK, King BA. 2019. E-cigarette use among youth in the United States, 2019. J Am Med Assoc. 322(21):2095–2103.
   PubMed Web of Science ®Google Scholar
• Drorbaugh JE, Fenn WO. 1955. A barometric method for measuring ventilation in newborn infants. Pediatrics. 16(1):81–87.
   PubMedGoogle Scholar
• Eissenberg T. 2010. Electronic nicotine delivery devices: ineffective nicotine delivery and craving suppression after acute administration. Tob Control. 19(1):87–88.
   PubMed Web of Science ®Google Scholar
• Escobar YNH, Nipp G, Cui T, Petters SS, Surratt JD, Jaspers I. 2020. In vitro toxicity and chemical characterization of aerosol derived from electronic cigarette humectants using a newly developed exposure system. Chem Res Toxicol. 33(7):1677–1688.
   PubMedGoogle Scholar
• Espinoza-Derout J, Hasan KM, Shao XM, Jordan MC, Sims C, Lee DL, Sinha S, Simmons Z, Mtume N, Liu Y, et al. 2019. Chronic intermittent electronic cigarette exposure induces cardiac dysfunction and atherosclerosis in apolipoprotein-E knockout mice. Am J Physiol Heart Circ Physiol. 317(2):H445–H459.
   PubMed Web of Science ®Google Scholar
• Etter JF. 2010. Electronic cigarettes: a survey of users. BMC Public Health. 10(231):231–237.
   PubMedGoogle Scholar
• Etter JF. 2014. Levels of saliva cotinine in electronic cigarette users. Addiction. 109(5):825–829.
   PubMedGoogle Scholar
• Farra YM, Eden MJ, Coleman JR, Kulkarni P, Ferris CF, Oakes JM, Bellini C. 2020. Acute neuroradiological, behavioral, and physiological effects of nose-only exposure to vaporized cannabis in C57BL/6 mice.
   Google Scholar
• Farra YM, Matz J, Ramkhelawon B, Oakes JM, Bellini C. 2021. Structural and functional remodeling of the female Apoe−/− mouse aorta due to chronic cigarette smoke exposure. Am J Physiol Heart Circ Physiol. 320(6):H2270–H2282.
   PubMedGoogle Scholar
• Fearon IM, Eldridge A, Gale N, Shepperd CJ, McEwan M, Camacho OM, Nides M, McAdam K, Proctor CJ. 2017. E-cigarette nicotine delivery: data and learnings from pharmacokinetic studies. Am J Health Behav. 41(1):16–32.
   PubMed Web of Science ®Google Scholar
• Fuoco FC, Buonanno G, Stabile L, Vigo P. 2014. Influential parameters on particle concentration and size distribution in the mainstream of e-cigarettes. Environ Pollut. 184:523–529.
   PubMed Web of Science ®Google Scholar
• Garcia-Arcos I, Geraghty P, Baumlin N, Campos M, Dabo AJ, Jundi B, Cummins N, Eden E, Grosche A, Salathe M, et al. 2016. Chronic electronic cigarette exposure in mice induces features of COPD in a nicotine-dependent manner. Thorax. 71(12):1119–1129.
   PubMed Web of Science ®Google Scholar
• Glynos C, Bibli SI, Katsaounou P, Pavlidou A, Magkou C, Karavana V, Topouzis S, Kalomenidis I, Zakynthinos S, Papapetropoulos A. 2018. Comparison of the effects of e-cigarette vapor with cigarette smoke on lung function and inflammation in mice. Am J Physiol Lung Cell Mol Physiol. 315(5):L662–L672.
   PubMed Web of Science ®Google Scholar
• Glynos C, Bibli S-I, Pavlidou A, Katsaounou P, Kalomenidis I, Zakynthinos S, Papapetropoulos A. 2015. Comparison of the effects of e-cigarette vapor vs cigarette smoke on lung function and inflammation in mice. Am J Physiol Lung Cell Mol Physiol. 315:L662–L672.
   Google Scholar
• Gorukanti A, Delucchi K, Ling P, Fisher-Travis R, Halpern-Felsher B. 2017. Adolescents’ attitudes towards e-cigarette ingredients, safety, addictive properties, social norms, and regulation. Prev Med. 94:65–71.
   PubMed Web of Science ®Google Scholar
• Guerassimov A, Hoshino Y, Takubo Y, Turcotte A, Yamamoto M, Ghezzo H, Triantafillopoulos A, Whittaker K, Hoidal JR, Cosio MG. 2004. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am J Respir Crit Care Med. 170(9):974–980.
   PubMed Web of Science ®Google Scholar
• Ha MA, Smith GJ, Cichocki JA, Fan L, Liu YS, Caceres AI, Jordt SE, Morris JB. 2015. Menthol attenuates respiratory irritation and elevates blood cotinine in cigarette smoke exposed mice. PLOS One. 10(2):e0117128.
   PubMed Web of Science ®Google Scholar
• Haass M, Kübler W. 1997. Nicotine and sympathetic neurotransmission. Cardiovasc Drugs Ther. 10(6):657–665.
   PubMedGoogle Scholar
• Haghnegahdar A, Feng Y, Chen X, Lin J. 2018. Computational analysis of deposition and translocation of inhaled nicotine and acrolein in the human body with e-cigarette puffing topographies. Aerosol Sci Technol. 52(5):483–493.
   PubMed Web of Science ®Google Scholar
• Hajek P, Pittaccio K, Pesola F, Myers Smith K, Phillips‐Waller A, Przulj D. 2020. Nicotine delivery and users’ reactions to Juul compared with cigarettes and other e‐cigarette products. Addiction. 115(6):1141–1148.
   PubMed Web of Science ®Google Scholar
• Hamm JT, Yee S, Rajendran N, Morrissey RL, Richter SJ, Misra M. 2007. Histological alterations in male A/J mice following nose-only exposure to tobacco smoke. Inhal Toxicol. 19(5):405–418.
   PubMed Web of Science ®Google Scholar
• Harvanko AM, Havel CM, Jacob P, Benowitz NL. 2020. Characterization of nicotine salts in 23 electronic cigarette refill liquids. Nicotine Tob Res. 22(7):1239–1243.
   PubMedGoogle Scholar
• Hernandez AB, Kirkness JP, Smith PL, Schneider H, Polotsky M, Richardson RA, Hernandez WC, Schwartz AR. 2012. Novel whole body plethysmography system for the continuous characterization of sleep and breathing in a mouse. J Appl Physiol. 112(4):671–680.
   PubMedGoogle Scholar
• Heyder J. 1975. Gravitational deposition of aerosol particles within a system of randomly oriented tubes. J Aerosol Sci. 6(2):133–137.
   Google Scholar
• Huang J, Duan Z, Kwok J, Binns S, Vera LE, Kim Y, Szczypka G, Emery SL. 2019. Vaping versus JUULing: how the extraordinary growth and marketing of JUUL transformed the US retail e-cigarette market. Tob Control. 28(2):146–151.
   PubMed Web of Science ®Google Scholar
• Huerta TR, Walker DM, Mullen D, Johnson TJ, Ford EW. 2017. Trends in e-cigarette awareness and perceived harmfulness in the U.S. Am J Prev Med. 52(3):339–346.
   PubMed Web of Science ®Google Scholar
• Hukkanen J, Jacob IP, Benowitz NL. 2005. Metabolism and disposition kinetics of nicotine. Pharmacol Rev. 57(1):79–115.
   PubMed Web of Science ®Google Scholar
• Hunt CA, Givens GH, Guzy S. 1998. Bootstrapping for pharmacokinetic models: visualization of predictive and parameter uncertainty. Pharm Res. 15(5):690–697.
   PubMedGoogle Scholar
• Jackler RK, Ramamurthi D. 2019. Nicotine arms race: JUUL and the high-nicotine product market. Tob Control. 28(6):623–628.
   PubMed Web of Science ®Google Scholar
• Jackson A, Grobman B, Krishnan-Sarin S. 2020. Recent findings in the pharmacology of inhaled nicotine: preclinical and clinical in vivo studies. Neuropharmacology. 176:108218.
   PubMedGoogle Scholar
• Johnson TJ, Olfert JS, Cabot R, Treacy C, Yurteri CU, Dickens C, McAughey J, Symonds JPR. 2014. Steady-state measurement of the effective particle density of cigarette smoke. J Aerosol Sci. 75:9–16.
   Web of Science ®Google Scholar
• Kolli AR, Kuczaj AK, Martin F, Hayes AW, Peitsch MC, Hoeng J. 2019. Bridging inhaled aerosol dosimetry to physiologically based pharmacokinetic modeling for toxicological assessment: nicotine delivery systems and beyond. Crit Rev Toxicol. 49(9):725–741.
   PubMed Web of Science ®Google Scholar
• Larcombe AN, Janka MA, Mullins BJ, Berry LJ, Bredin A, Franklin PJ. 2017. The effects of electronic cigarette aerosol exposure on inflammation and lung function in mice. Am J Physiol Lung Cell Mol Physiol. 313(1):L67–L79.
   PubMed Web of Science ®Google Scholar
• Lee L-Y. 1990. Inhibitory effect of gas phase cigarette smoke on breathing: role of hydroxyl radical. Respir Physiol. 82(2):227–238.
   PubMedGoogle Scholar
• Lee LY, Beck ER, Morton RF, Kou YR, Frazier DT. 1987. Role of bronchopulmonary C-fiber afferents in the apneic response to cigarette smoke. J Appl Physiol. 63(4):1366–1373.
   PubMedGoogle Scholar
• Lee LY, Morton RF, Hord AH, Frazier DT. 1983. Reflex control of breathing following inhalation of cigarette smoke in conscious dogs. J Appl Physiol Respir Environ Exerc Physiol. 54(2):562–570.
   PubMedGoogle Scholar
• Lerner CA, Sundar IK, Yao H, Gerloff J, Ossip DJ, McIntosh S, Robinson R, Rahman I. 2015. 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(2):e0116732.
   PubMed Web of Science ®Google Scholar
• Leventhal AM, Madden DR, Peraza N, Schiff SJ, Lebovitz L, Whitted L, Barrington-Trimis J, Mason TB, Anderson MK, Tackett AP. 2021. Effect of exposure to e-cigarettes with salt vs free-base nicotine on the appeal and sensory experience of vaping: a randomized clinical trial. JAMA Netw Open. 4(1):e2032757.
   PubMedGoogle Scholar
• Li L, Lee ES, Nguyen C, Zhu Y. 2020. Effects of propylene glycol, vegetable glycerin, and nicotine on emissions and dynamics of electronic cigarette aerosols. Aerosol Sci Technol. 54(11):1270–1281.
   PubMed Web of Science ®Google Scholar
• Lo Sasso G, Schlage WK, Boué S, Veljkovic E, Peitsch MC, Hoeng J. 2016. The Apoe−/− mouse model: a suitable model to study cardiovascular and respiratory diseases in the context of cigarette smoke exposure and harm reduction. J Transl Med. 14(1):1–16.
   PubMedGoogle Scholar
• Mandel WJ, Laks M, Hayakawa H, Obayashi K, McCullen A. 1973. Cardiovascular effects of nicotine in the conscious dog: modification by changes in autonomic tone. Am J Cardiol. 32(7):947–955.
   PubMedGoogle Scholar
• Margham J, McAdam K, Forster M, Liu C, Wright C, Mariner D, Proctor C. 2016. Chemical composition of aerosol from an e-cigarette: a quantitative comparison with cigarette smoke. Chem Res Toxicol. 29(10):1662–1678.
   PubMed Web of Science ®Google Scholar
• Miliano C, Scott ER, Murdaugh LB, Gnatowski ER, Faunce CL, Anderson MS, Reyes MM, Gregus AM, Buczynski MW. 2020. Modeling drug exposure in rodents using e-cigarettes and other electronic nicotine delivery systems. J Neurosci Methods. 330:108458.
   PubMed Web of Science ®Google Scholar
• Milton PL, Dickinson H, Jenkin G, Lim R. 2012. Assessment of respiratory physiology of C57BL/6 mice following bleomycin administration using barometric plethysmography. Respiration. 83(3):253–266.
   PubMedGoogle Scholar
• Monjezi M, Dastanpour R, Saidi MS, Pishevar AR. 2012. Prediction of particle deposition in the respiratory track using 3D-1D modeling. Sci Iran. 19(6):1479–1486.
   Google Scholar
• Ni F, Ogura T, Lin W. 2020. Electronic cigarette liquid constituents induce nasal and tracheal sensory irritation in mice in regionally dependent fashion. Nicotine Tob Res. 22(Suppl 1):S35–S44.
   PubMedGoogle Scholar
• Oakes JM, Shadden SC, Grandmont C, Vignon-Clementel IE. 2017. Aerosol transport throughout inspiration and expiration in the pulmonary airways. Int J Numer Method Biomed Eng. 33(9):1–19.
   Google Scholar
• Obot CJ, Lee KM, Fuciarelli AF, Renne RA, McKinney WJ. 2004. Characterization of mainstream cigarette smoke-induced biomarker responses in ICR and C57BI/6 mice. Inhal Toxicol. 16(10):701–719.
   PubMed Web of Science ®Google Scholar
• Oldham MJ, Phalen RF, Schum GM, Daniels DS. 1994. Predicted nasal and tracheobronchial particle deposition efficiencies for the mouse. Ann Occup Hyg. 38(inhaled particles VII):135–141.
   Google Scholar
• Olfert IM, DeVallance E, Hoskinson H, Branyan KW, Clayton S, Pitzer CR, Sullivan DP, Breit MJ, Wu Z-X, Klinkhachorn P, et al. 2018. Chronic exposure to electronic cigarette (E-cig) results in impaired cardiovascular function in mice. J Appl Physiol. 124(3):573–582.
   PubMed Web of Science ®Google Scholar
• Omaiye EE, McWhirter KJ, Luo W, Pankow JF, Talbot P. 2019. High-nicotine electronic cigarette products: toxicity of JUUL fluids and aerosols correlates strongly with nicotine and some flavor chemical concentrations. Chem Res Toxicol. 32(6):1058–1069.
   PubMed Web of Science ®Google Scholar
• Pappas RS, Gray N, Halstead M, Valentin-Blasini L, Watson C. 2021. Toxic metal-containing particles in aerosols from pod-type electronic cigarettes. J Anal Toxicol. 45(4):337–347.
   PubMedGoogle Scholar
• Petersen DR, Norris KJ, Thompson JA. 1984. A comparative study of the disposition of nicotine and its metabolites in three inbred strains of mice. Drug Metab Depos. 12(6):725–731.
   PubMedGoogle Scholar
• Phillips B, Veljkovic E, Boué S, Schlage WK, Vuillaume G, Martin F, Titz B, Leroy P, Buettner A, Elamin A, et al. 2016. An 8-month systems toxicology inhalation/cessation study in Apoe−/− mice to investigate cardiovascular and respiratory exposure effects of a candidate modified risk tobacco product, THS 2.2, compared with conventional cigarettes. Toxicol Sci. 149(2):411–432.
   PubMedGoogle Scholar
• Pratte P, Cosandey S, Goujon-Ginglinger C. 2016. A scattering methodology for droplet sizing of e-cigarette aerosols. Inhal Toxicol. 28(12):537–545.
   PubMed Web of Science ®Google Scholar
• Sahu SK, Tiwari M, Bhangare RC, Pandit GG. 2013. Particle size distribution of mainstream and exhaled cigarette smoke and predictive deposition in human respiratory tract. Aerosol Air Qual Res. 13(1):324–332.
   Google Scholar
• Salway R, Wakefield J. 2008. Gamma generalized linear models for pharmacokinetic data. Biometrics. 64(2):620–626.
   PubMedGoogle Scholar
• Shao XM, Friedman TC. 2020. Pod-mod vs. conventional e-cigarettes: nicotine chemistry, pH, and health effects. J Appl Physiol. 128(4):1056–1058.
   PubMed Web of Science ®Google Scholar
• Shao XM, Lopez B, Nathan D, Wilson J, Bankole E, Tumoyan H, Munoz A, Espinoza-Derout J, Hasan KM, Chang S, et al. 2019. A mouse model for chronic intermittent electronic cigarette exposure exhibits nicotine pharmacokinetics resembling human vapers. J Neurosci Methods. 326(July):108376.
   PubMedGoogle Scholar
• Shi H, Fan X, Horton A, Haller ST, Kennedy DJ, Schiefer IT, Dworkin L, Cooper CJ, Tian J. 2019. The effect of electronic-cigarette vaping on cardiac function and angiogenesis in mice. Sci Rep. 9(1):1–9.
   PubMedGoogle Scholar
• Siu ECK, Tyndale RF. 2007. Characterization and comparison of nicotine and cotinine metabolism in vitro and in vivo in DBA/2 and C57BL/6 mice. Mol Pharmacol. 71(3):826–834.
   PubMedGoogle Scholar
• Sosnowski TR, Odziomek M. 2018. Particle size dynamics: toward a better understanding of electronic cigarette aerosol interactions with the respiratory system. Front Physiol. 9(853):1–8.
   PubMedGoogle Scholar
• Szafran BN, Pinkston R, Perveen Z, Ross MK, Morgan T, Paulsen DB, Penn AL, Kaplan BLF, Noël A. 2020. Electronic-cigarette vehicles and flavoring affect lung function and immune responses in a murine model. IJMS. 21(17):6022–6022.
   Google Scholar
• Talih S, Salman R, El-Hage R, Karam E, Karaoghlanian N, El-Hellani A, Saliba N, Shihadeh A. 2019. Characteristics and toxicant emissions of JUUL electronic cigarettes. Tob Control. 28(6):678–680.
   PubMedGoogle Scholar
• Taulbee DB, Yu CP. 1975. A theory of aerosol deposition in the human respiratory tract. J Appl Physiol. 38(1):77–85.
   PubMed Web of Science ®Google Scholar
• Teeguarden JG, Housand CJ, Smith JN, Hinderliter PM, Gunawan R, Timchalk CA. 2013. A multi-route model of nicotine-cotinine pharmacokinetics, pharmacodynamics and brain nicotinic acetylcholine receptor binding in humans. Regul Toxicol Pharmacol. 65(1):12–28.
   PubMed Web of Science ®Google Scholar
• Tsai MC, Byun MK, Shin J, Crotty Alexander LE. 2020. Effects of e-cigarettes and vaping devices on cardiac and pulmonary physiology. J Physiol. 598(22):5039–5062.
   PubMedGoogle Scholar
• Tsuji H, Fujimoto H, Matsuura D, Nishino T, Lee KM, Renne R, Yoshimura H. 2011. Comparison of mouse strains and exposure conditions in acute cigarette smoke inhalation studies. Inhal Toxicol. 23(10):602–615.
   PubMed Web of Science ®Google Scholar
• Tuttle AM, Stämpfli M, Foster WG. 2009. Cigarette smoke causes follicle loss in mice ovaries at concentrations representative of human exposure. Hum Reprod. 24(6):1452–1459.
   PubMedGoogle Scholar
• Ulrich CE, Haddock MP, Alarie Y. 1972. Airborne chemical irritants: role of the trigeminal nerve. Arch Environ Health. 24(1):37–42.
   PubMed Web of Science ®Google Scholar
• Vlahos R, Bozinovski S. 2014. Recent advances in pre-clinical mouse models of COPD. Clin Sci. 126(4):253–265.
   PubMed Web of Science ®Google Scholar
• Wagoner KG, King JL, Suerken CK, Reboussin BA, Cornacchione Ross J, Sutfin EL. 2021. Changes in knowledge, perceptions and use of JUUL among a cohort of young adults. Tob Control. 30(6):638–643.
   PubMedGoogle Scholar
• Wang P, Chen W, Liao J, Matsuo T, Ito K, Fowles J, Shusterman D, Mendell M, Kumagai K. 2017. A device-independent evaluation of carbonyl emissions from heated electronic cigarette solvents. PLOS One. 12(1):e0169811.
   PubMed Web of Science ®Google Scholar
• Witschi H, Espiritu I, Dance ST, Miller MS. 2002. A mouse lung tumor model of tobacco smoke carcinogenesis. Toxicol Sci. 68(2):322–330.
   PubMedGoogle Scholar
• Wu W, Jin Y, Carlsten C. 2018. Inflammatory health effects of indoor and outdoor particulate matter. J Allergy Clin Immunol. 141(3):833–844.
   PubMed Web of Science ®Google Scholar
• Xu X, Su Y, Fan ZH. 2014. Cotinine concentration in serum correlates with tobacco smoke-induced emphysema in mice. Sci Rep. 4:3864–3866.
   PubMedGoogle Scholar
• Yamazaki H, Horiuchi K, Takano R, Nagano T, Shimizu M, Kitajima M, Murayama N, Shono F. 2010. Human blood concentrations of cotinine, a biomonitoring marker for tobacco smoke, extrapolated from nicotine metabolism in rats and humans and physiologically based pharmacokinetic modeling. Int J Environ Res Public Health. 7(9):3406–3421.
   PubMedGoogle Scholar
• Zimmerman N, Godri Pollitt KJ, Jeong CH, Wang JM, Jung T, Cooper JM, Wallace JS, Evans GJ. 2014. Comparison of three nanoparticle sizing instruments: the influence of particle morphology. Atmos Environ. 86:140–147.
   Web of Science ®Google Scholar