{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,4]],"date-time":"2026-09-04T10:47:31Z","timestamp":1788518851996,"version":"build-2803163510"},"reference-count":19,"publisher":"The Endocrine Society","issue":"10","license":[{"start":{"date-parts":[[2019,9,5]],"date-time":"2019-09-05T00:00:00Z","timestamp":1567641600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["RO1HD060860"],"award-info":[{"award-number":["RO1HD060860"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01HL145396"],"award-info":[{"award-number":["R01HL145396"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["P50HL120100"],"award-info":[{"award-number":["P50HL120100"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000968","name":"American Heart Association","doi-asserted-by":"publisher","award":["18POST33960353"],"award-info":[{"award-number":["18POST33960353"]}],"id":[{"id":"10.13039\/100000968","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Electronic nicotine delivery system (e-cigarette) use is prevalent among pregnant women as a seemingly safe alternative to traditional tobacco use, known to result in fetal developmental abnormalities and impaired fertility of male offspring. However, little is known about the effects of e-cigarette use on fertility or pregnancy outcomes. A successful pregnancy is initiated by a multitude of dynamic molecular alterations in the uterus resulting in embryo implantation at day 4.5 in the mouse. We examined whether e-cigarette exposure impairs implantation and offspring health. Pregnant C57BL\/6J mice were exposed five times a week to e-cigarette vapor or sham. After 4 months, e-cigarette exposed dams exhibited a significant delay in the onset of the first litter. Furthermore, exposure of new dams in early pregnancy significantly impaired embryo implantation, as evidenced by nearly complete absence of implantation sites in e-cigarette\u2013exposed animals at day 5.5, despite exhibiting high levels of progesterone, an indicator of pregnancy. RNA microarray from day 4.5 pseudopregnant mice revealed significant changes in the integrin, chemokine, and JAK signaling pathways. Moreover, female offspring exposed to e-cigarettes in utero exhibited a significant weight reduction at 8.5 months, whereas males exhibited a slight but nonsignificant deficiency in fertility. Thus, e-cigarette exposure in mice impairs pregnancy initiation and fetal health, suggesting that e-cigarette use by reproductive-aged women or during pregnancy should be considered with caution.<\/jats:p>","DOI":"10.1210\/js.2019-00216","type":"journal-article","created":{"date-parts":[[2019,9,5]],"date-time":"2019-09-05T09:06:41Z","timestamp":1567674401000},"page":"1907-1916","source":"Crossref","is-referenced-by-count":58,"title":["E-Cigarette Exposure Delays Implantation and Causes Reduced Weight Gain in Female Offspring Exposed In Utero"],"prefix":"10.1210","volume":"3","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0473-9422","authenticated-orcid":false,"given":"Margeaux","family":"Wetendorf","sequence":"first","affiliation":[{"name":"Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lewis T","family":"Randall","sequence":"additional","affiliation":[{"name":"Department of Medicine, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mahlet T","family":"Lemma","sequence":"additional","affiliation":[{"name":"Department of Medicine, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophia H","family":"Hurr","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2407-2944","authenticated-orcid":false,"given":"John B","family":"Pawlak","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8598-2642","authenticated-orcid":false,"given":"Robert","family":"Tarran","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2638-3321","authenticated-orcid":false,"given":"Claire M","family":"Doerschuk","sequence":"additional","affiliation":[{"name":"Department of Medicine, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7033-9232","authenticated-orcid":false,"given":"Kathleen M","family":"Caron","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, North Carolina"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"80","published-online":{"date-parts":[[2019,9,5]]},"reference":[{"issue":"2","key":"2019100408462994500_bib1","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1002\/bdrc.21128","article-title":"The effects of nicotine on human fetal development","volume":"108","author":"Holbrook","year":"2016","journal-title":"Birth Defects Res C Embryo Today"},{"issue":"8","key":"2019100408462994500_bib2","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1007\/s10995-016-2257-9","article-title":"Prevalence and perceptions of electronic cigarette use during pregnancy","volume":"21","author":"Wagner","year":"2017","journal-title":"Matern Child Health J"},{"issue":"3","key":"2019100408462994500_bib3","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1002\/bdra.23333","article-title":"Is there evidence for potential harm of electronic cigarette use in pregnancy","volume":"103","author":"Suter","year":"2015","journal-title":"Birth Defects Res A Clin Mol Teratol"},{"key":"2019100408462994500_bib4","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.drugalcdep.2018.08.016","article-title":"Harm perceptions of electronic cigarettes and nicotine: a nationally representative cross-sectional survey of young people in Great Britain","volume":"192","author":"East","year":"2018","journal-title":"Drug Alcohol Depend"},{"issue":"3","key":"2019100408462994500_bib5","first-page":"329","article-title":"E-smoking: emerging public health problem","volume":"30","author":"Jankowski","year":"2017","journal-title":"Int J Occup Med Environ Health"},{"key":"2019100408462994500_bib6","first-page":"6","volume-title":"Evidence Review of E-Cigarettes and Heated Tobacco Products 2018: A Report Commissioned by Publich Health England","author":"McNeill","year":"2018"},{"issue":"2","key":"2019100408462994500_bib7","doi-asserted-by":"crossref","first-page":"1801151","DOI":"10.1183\/13993003.01151-2018","article-title":"Electronic cigarettes: a task force report from the European Respiratory Society","volume":"53","author":"Bals","year":"2019","journal-title":"Eur Respir J"},{"issue":"12","key":"2019100408462994500_bib8","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1038\/nm.3012","article-title":"Mechanisms of implantation: strategies for successful pregnancy","volume":"18","author":"Cha","year":"2012","journal-title":"Nat Med"},{"issue":"1\u20132","key":"2019100408462994500_bib9","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.mce.2011.10.028","article-title":"The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network","volume":"357","author":"Wetendorf","year":"2012","journal-title":"Mol Cell Endocrinol"},{"issue":"1","key":"2019100408462994500_bib10","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1186\/1741-7015-11-154","article-title":"New insights into mechanisms behind miscarriage","volume":"11","author":"Larsen","year":"2013","journal-title":"BMC Med"},{"issue":"3","key":"2019100408462994500_bib11","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1165\/rcmb.2017-0206RC","article-title":"Maternal e-cigarette exposure in mice alters DNA methylation and lung cytokine expression in offspring","volume":"58","author":"Chen","year":"2018","journal-title":"Am J Respir Cell Mol Biol"},{"issue":"9","key":"2019100408462994500_bib12","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1097\/OGX.0000000000000595","article-title":"The use of electronic cigarettes in pregnancy: a review of the literature","volume":"73","author":"Whittington","year":"2018","journal-title":"Obstet Gynecol Surv"},{"issue":"6","key":"2019100408462994500_bib13","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1095\/biolreprod.110.088989","article-title":"Classification of mouse sperm motility patterns using an automated multiclass support vector machines model","volume":"84","author":"Goodson","year":"2011","journal-title":"Biol Reprod"},{"issue":"6","key":"2019100408462994500_bib14","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1007\/s00418-015-1361-z","article-title":"Claudin-3, claudin-7, and claudin-10 show different distribution patterns during decidualization and trophoblast invasion in mouse and human","volume":"144","author":"Schumann","year":"2015","journal-title":"Histochem Cell Biol"},{"issue":"1","key":"2019100408462994500_bib15","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1007\/s00424-016-1921-7","article-title":"One gene, two paracellular ion channels-claudin-10 in the kidney","volume":"469","author":"Milatz","year":"2017","journal-title":"Pflugers Arch"},{"issue":"4","key":"2019100408462994500_bib16","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1113\/jphysiol.1933.sp003015","article-title":"Size changes in the seminal vesicles of the mouse during development and after castration","volume":"78","author":"Deanesly","year":"1933","journal-title":"J Physiol"},{"issue":"4","key":"2019100408462994500_bib17","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1093\/humupd\/dmu006","article-title":"Ion channels in the endometrium: regulation of endometrial receptivity and embryo implantation","volume":"20","author":"Ruan","year":"2014","journal-title":"Hum Reprod Update"},{"key":"2019100408462994500_bib18","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.neulet.2018.07.001","article-title":"Modulation of neural regulators of energy homeostasis, and of inflammation, in the pups of mice exposed to e-cigarettes","volume":"684","author":"Chen","year":"2018","journal-title":"Neurosci Lett"},{"issue":"2","key":"2019100408462994500_bib19","doi-asserted-by":"crossref","first-page":"e0118344","DOI":"10.1371\/journal.pone.0118344","article-title":"The effects of electronic cigarette emissions on systemic cotinine levels, weight and postnatal lung growth in neonatal mice","volume":"10","author":"McGrath-Morrow","year":"2015","journal-title":"PLoS One"}],"container-title":["Journal of the Endocrine Society"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jes\/advance-article-pdf\/doi\/10.1210\/js.2019-00216\/29582555\/js.2019-00216.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jes\/article-pdf\/3\/10\/1907\/30101999\/js.2019-00216.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jes\/article-pdf\/3\/10\/1907\/30101999\/js.2019-00216.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,10,4]],"date-time":"2019-10-04T08:46:48Z","timestamp":1570178808000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jes\/article\/3\/10\/1907\/5560172"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,9,5]]},"references-count":19,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2019,10,1]]}},"URL":"https:\/\/doi.org\/10.1210\/js.2019-00216","relation":{},"ISSN":["2472-1972"],"issn-type":[{"value":"2472-1972","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,10]]},"published":{"date-parts":[[2019,9,5]]}}}