Use of Electronic Nicotine Delivery Systems (ENDS) by pregnant women I: Risk of small-for-gestational-age birth
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Department of Epidemiology, Fay W. Boozman College of Public Health, University of Arkansas for Medical Sciences, Little Rock, United States
The Winthrop P. Rockefeller Cancer Institute, University of Arkansas for Medical Sciences, Little Rock, United States
Department of Environmental and Occupational Health, Fay W. Boozman College of Public Health, University of Arkansas for Medical Sciences, Little Rock, United States
Department of Obstetrics and Gynecology, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, United States
Department of Community Health, Faculty of Clinical Sciences, University of Uyo, Uyo, Nigeria
Arkansas Department of Health, Little Rock, United States
Victor M. Cardenas   

Department of Epidemiology, Fay W. Boozman College of Public Health, University of Arkansas for Medical Sciences, Little Rock, United States
Publish date: 2019-05-21
Tob. Induc. Dis. 2019;17(May):44
The 2016 US Surgeon General’s Report suggests that the use of electronic nicotine delivery systems (ENDS) is a fetal risk factor. However, no previous study has estimated their effect on adverse pregnancy outcomes. We assessed the prevalence of current ENDS use in pregnant women and explored the effect on birth weight and smallness-for-gestational-age (SGA), correcting for misclassification from nondisclosure of smoking status.

We conducted a cohort study with 248 pregnant women using questionnaire data and biomarkers (salivary cotinine, exhaled carbon monoxide, and hair nicotine). We evaluated the association between birth weight and the risk of SGA by applying multivariate linear and log-binomial regression to reproductive outcome data for 232 participants. Participants who did not disclose their smoking status were excluded from the referent group. Sensitivity analysis corrected for misclassification of smoking/ENDS use status.

The prevalence of current ENDS use among pregnant women was 6.8% (95% CI: 4.4–10.2%); most of these (75%) were concurrent smokers. Using self-reports, the estimated risk ratio of SGA for ENDS users was nearly two times the risk in the unexposed (RR=1.9, 95% CI: 0.6–5.5), and over three times that for ENDS-only users versus the unexposed (RR=3.1, 95% CI: 0.8–11.7). Excluding from the referent group smokers who did not disclose their smoking status, the risk of SGA for ENDS-only use was 5 times the risk in the unexposed (RR=5.1, 95% CI: 1.1– 22.2), and almost four times for all types of ENDS users (RR=3.8, 95% CI: 1.3–11.2). SGA risk ratios for ENDS users, corrected for misclassification due to self-report, were 6.5–8.5 times that of the unexposed.

Our data suggest that ENDS use is associated with an increased risk of SGA.

This work was supported in part by a grant from the Arkansas Department of Health (ADH) to the University of Arkansas at Pine Bluff Minority Research Center (MRC) on Tobacco and Addictions, sub-awarded to VM Cardenas. Funding available from the UAMS Fay W. Boozman College of Public Health for personal development to VM Cardenas and RR Delongchamp was also used to support part of the data collection. HL Moody, P Murphy and A Ward, from the SARA Study at the UAMS Department of Obstetrics and Gynecology, provided assistance with primary data collection and data abstraction. We were also supported by the UAMS Translational Research Institute (grant UL1TR000039) through the National Institutes of Health (NIH) National Center for Research Resources and National Center for Advancing Translational Sciences. We are very thankful to Howraa-Al Mousawi, Chief of the Vital Statistics Section at the ADH, and to other members of the ADH leadership for their support in obtaining birth records for participants who did not deliver their babies at UAMS. The manuscript content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH, MRC, or ADH. We also acknowledge the support of past and current staff of the UAMS Women’s Clinic, JC Brothers, MK Robinson, P Ward, and S Eastham, for their support in data collection. We thank SL Thomas for her valuable assistance with the literature search. Finally, we thank the UAMS Science Communication Group for editing this manuscript.
Authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none was reported.
There was no source of funding for this research.
Not commissioned; externally peer reviewed.
Kurti AN, Redner R, Lopez AA, Keith DR, Stanton CA, Gaalema DE, et al. Tobacco and nicotine delivery product use in a national sample of pregnant women. Prev Med. 2017;104:50-56. doi:10.1016/j.ypmed.2017.07.030
Agaku IT, King BA, Husten CG, Bunnell R, Ambrose BK, Hu SS, et al. Tobacco product use among adults--United States, 2012-2013. MMWR Morb Mortal Wkly Rep. 2014;63(25):542-547. PMID: 24964880.
Hu SS, Neff L, Agaku IT, Cox S, Day HR, Holder-Hayes E, et al. Tobacco product use among adults - United States, 2013-2014. MMWR Morb Mortal Wkly Rep. 2016;65(27):685-691. doi:10.15585/mmwr.mm6527a1
Phillips E, Wang TW, Husten CG, Corey CG, Appelberg BJ, Jamal A, et al. Tobacco product use among adults - United States, 2015. MMWR Morb Mortal Wkly Rep. 2017;66(44):1209-1215. doi:10.15585/mmwr.mm6644a2
Franck C, Budlovsky T, Windle SB, Filion KB, Eisenberg MJ. Electronic cigarettes in North America: History, use, and implications for smoking cessation. Circulation. 2014;129(19):1945-1952. doi:10.1161/CIRCULATIONAHA.113.006416
Grana R, Benowitz N, Glantz SA. E-cigarettes: A scientific review. Circulation. 2014;129(19):1972-1986. doi:10.1161/CIRCULATIONAHA.114.007667
Willett JG, Bennett M, Hair EC, Xiao H, Greenberg MS, Harvey E, et al. Recognition, use and perceptions of JUUL among youth and young adults. Tob Control. 2018;28(1):115-116. doi:10.1136/tobaccocontrol-2018-054273
National Academies of Sciences; Engineering; and Medicine, Health and Medicine Division, Board on Population Health and Public Health Practice, Committee on the Review of the Health Effects of Electronic Nicotine Delivery Systems. Public Health Consequences of E-Cigarettes. In: Eaton DL, Kwan LY, Stratton K, eds. Washington (DC): National Academies Press (US); 2018.
Whittington JR, Simmons PM, Phillips A, Gambell S, Cen R, Magann EF, Cardenas VM. The use of electronic cigarettes in pregnancy: A review of the literature. Obstet Gynecol Surv. 2018;73:544-549. doi:10.1097/OGX.0000000000000595
U.S. Department of Health and Human Services. E-Cigarette Use among Youth and Young Adults: A Report of the Surgeon General. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2016. https://e-cigarettes.surgeonge.... Accessed September 21, 2018.
England LJ, Aagaard K, Bloch M, Conway K, Cosgrove K, Grana R et al. Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products. Neurosci Biobehav Rev. 2017;72:176-189. doi:10.1016/j.neubiorev.2016.11.013
U.S. Department of Health and Human Services. The health consequences of smoking: 50 years of progress. A report of the surgeon general. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2014. Accessed September 21, 2018.
Grana RA, Ling PM, Benowitz N, Glantz S. Electronic cigarettes. Circulation. 2014;129(19):e490-e492. doi:10.1161/CIRCULATIONAHA.114.008545
Baeza-Loya S, Viswanath H, Carter A, Molfese DL, Velasquez KM, Baldwin PR, et al. Perceptions about e-cigarette safety may lead to e-smoking during pregnancy. Bull Menninger Clin. 2014;78(3):243-252. doi:10.1521/bumc.2014.78.3.243
Mark KS, Farquhar B, Chisolm MS, Coleman-Cowger VH, Terplan M. Knowledge, attitudes, and practice of electronic cigarette use among pregnant women. J Addict Med. 2015;9(4):266-272. doi:10.1097/ADM.0000000000000128
Kahr MK, Padgett S, Shope CD, Griffin EN, Xie SS, Gonzalez PJ, et al. A qualitative assessment of the perceived risks of electronic cigarette and hookah use in pregnancy. BMC Public Health. 2015;15(1):1273. doi:10.1186/s12889-015-2586-4
Ashford K, Wiggins A, Butler K, Ickes M, Rayens MK, Hahn E. E-cigarette use and perceived harm among women of childbearing age who reported tobacco use during the past year. Nurs Res. 2016;65(5):408-414. doi:10.1097/NNR.0000000000000176
McCubbin A, Fallin-Bennett A, Barnett J, Ashford K. Perceptions and use of electronic cigarettes in pregnancy. Health Educ Res. 2017;32(1):22-32. doi:10.1093/her/cyw059
Oncken C, Ricci KA, Kuo CL, Dornelas E, Kranzler HR, Sankey HZ. Correlates of electronic cigarettes use before and during pregnancy. Nicotine Tob Res. 2017;19(5):585-590. doi:10.1093/ntr/ntw225
England LJ, Anderson BL, Tong VT, Mahoney J, Coleman-Cowger VH, Melstrom P et al. Screening practices and attitudes of obstetricians-gynecologists toward new and emerging tobacco products. Am J Obstet Gynecol. 2014;211(6):695.e1-695.e7. doi:10.1016/j.ajog.2014.05.041
England LJ, Tong VT, Koblitz A, Kish-Doto J, Lynch MM, Southwell BG. Perceptions of emerging tobacco products and nicotine replacement therapy among pregnant women and women planning a pregnancy. Prev Med Rep. 2016;4:481-485. doi:10.1016/j.pmedr.2016.09.002
Committee opinion no. 721 summary: Smoking cessation during pregnancy. Obstet Gynecol. 2017;130(4):929-930. doi:10.1097/AOG.0000000000002348
Cnattingius S. The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob Res. 2004;6(Suppl 2):S125-S140. doi:10.1080/14622200410001669187
Dietz PM, Homa D, England LJ, Burley K, Tong V, Dube SR et al. Estimates of nondisclosure of cigarette smoking among pregnant and nonpregnant women of reproductive age in the United States. Am J Epidemiol. 2011;173(3):355-359. doi:10.1093/aje/kwq381
England LJ, Grauman A, Qian C, Wilkins DG, Schisterman EF, Yu FK, et al. Misclassification of maternal smoking status and its effects on an epidemiologic study of pregnancy outcomes. Nicotine Tob Res. 2007;9(10):1005-1013. doi:10.1080/14622200701491255
Avila-Tang E, Al-Delaimy WK, Ashley DL, Benowitz N, Bernert JT, Kim S, Samet JM, Hecht SS. Assessing secondhand smoke using biological markers. Tob Control. 2013;22(3):164-171. doi:10.1136/tobaccocontrol-2011-050298
Kim S, Apelberg BJ, Avila-Tang E, Hepp L, Yun D, Samet JM et al. Utility and cutoff value of hair nicotine as a biomarker of long-term tobacco smoke exposure, compared to salivary cotinine. Int J Environ Res Public Health. 2014;11(8):8368-8382. doi:10.3390/ijerph110808368
Almeida ND, Koren G, Platt RW, Kramer MS. Hair biomarkers as measures of maternal tobacco smoke exposure and predictors of fetal growth. Nicotine Tob Res. 2011;13(5):328-335. doi:10.1093/ntr/ntq259
Nafstad P, Fugelseth D, Qvigstad E, Zahlen K, Magnus P, Lindemann R. Nicotine concentration in the hair of nonsmoking mothers and size of offspring. Am J Public Health. 1998;88(1):120-124. doi:10.2105/AJPH.88.1.120
Sabra S, Malmqvist E, Almeida L, Gratacos E, Gomez Roig MD. Differential correlations between maternal hair levels of tobacco and alcohol with fetal growth restriction clinical subtypes. Alcohol. 2018;70:43-49. doi:10.1016/j.alcohol.2018.01.001
Jamal A, Agaku IT, O'Connor E, King BA, Kenemer JB, Neff L. Current cigarette smoking among adults--united states, 2005-2013. MMWR Morb Mortal Wkly Rep. 2014;63(47):1108-1112. PMID: 25426653.
Jamal A, Homa DM, O'Connor E, Babb SD, Caraballo RS, Singh T, et al. Current cigarette smoking among adults - United States, 2005-2014. MMWR Morb Mortal Wkly Rep. 2015;64(44):1233-1240. doi:10.15585/mmwr.mm6444a2
Ekanem US, Cardenas VM, Cen R, Simon W, Chedjueu IP, Woodward M et al. Electronic nicotine delivery systems and smoking cessation in Arkansas, 2014. Public Health Rep. 2017;132(2):210-219. doi:10.1177/0033354916689611
Board on Children; Youth; and Families, Institute of Medicine, National Research Council. An Update on Research Issues in the Assessment of Birth Settings: Workshop Summary. Washington (DC): National Academies Press (US); 2013. doi:10.17226/18368
Mullen PD, Carbonari JP, Tabak ER, Glenday MC. Improving disclosure of smoking by pregnant women. Am J Obstet Gynecol. 1991;165(2):409-413. doi:10.1016/0002-9378(91)90105-Z
Clemens MM, Cardenas VM, Fischbach LA, Cen R, Siegel ER, Eswaran H, et al. Use of Electronic Nicotine Delivery Systems by Pregnant Women II: Hair biomarkers for Exposures to Nicotine and Tobacco-Specific Nitrosamines. Tob Induc Dis. 2019;17(April). doi:10.18332/tid/105387
Talge NM, Mudd LM, Sikorskii A, Basso O. United States birth weight reference corrected for implausible gestational age estimates. Pediatrics. 2014;133(5):844-853. doi:10.1542/peds.2013-3285
Duryea EL, Hawkins JS, McIntire DD, Casey BM, Leveno KJ. A revised birth weight reference for the United States. Obstet Gynecol. 2014;124(1):16-22. doi:10.1097/AOG.0000000000000345
Brown LD, Cai TT, DasGupta A. Interval estimation for a binomial proportion. Statistical Science. 2001;16(2):101-133. doi:10.1214/ss/1009213286
Greenland S, Robins JM. Estimation of a common effect parameter from sparse follow-up data. Biometrics. 1985;41(1):55-68. doi:10.2307/2530643
Spiegelman D, Hertzmark E. Easy SAS calculations for risk or prevalence ratios and differences. Am J Epidemiol. 2005;162(3):199-200. doi:10.1093/aje/kwi188
Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic Research: Principles and Quantitative Methods. Mishawaka, IN: Wiley and Sons; 1982.
VanderWeele TJ, Ding P. Sensitivity analysis of observational research: Introducing the E-value. Ann Intern Med. 2017;167(4):268-274. doi:10.7326/M16-2607
Dempsey DA, Benowitz NL. Risks and benefits of nicotine to aid smoking cessation in pregnancy. Drug Saf. 2001;24(4):277-322. doi:10.2165/00002018-200124040-00005
Slama R, Ballester F, Casas M, Cordier S, Eggesbø M, Iniguez C, et al. Epidemiologic tools to study the influence of environmental factors on fecundity and pregnancy-related outcomes. Epidemiol Rev. 2014;36(1):148-164. doi:10.1093/epirev/mxt011
Woodby LL, Windsor RA, Snyder SW, Kohler CL, Diclemente CC. Predictors of smoking cessation during pregnancy. Addiction. 1999;94(2):283-292. doi:10.1046/j.1360-0443.1999.94228311.x
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Tobacco Induced Diseases