Cognitive and behavioral impairments evoked by low-level exposure to tobacco smoke components: comparison with nicotine alone
Open accessAbstract
Active maternal smoking has adverse effects on neurobehavioral development of the offspring, with nicotine (Nic) providing much of the underlying causative mechanism. To determine whether the lower exposures caused by second-hand smoke are deleterious, we administered tobacco smoke extract (TSE) to pregnant rats starting preconception and continued through the second postnatal week, corresponding to all 3 trimesters of fetal brain development. Dosing was adjusted to produce maternal plasma Nic concentrations encountered with second-hand smoke, an order of magnitude below those seen in active smokers. We then compared TSE effects to those of an equivalent dose of Nic alone, and to a 10-fold higher Nic dose. Gestational exposure to TSE and Nic significantly disrupted cognitive and behavioral function in behavioral tests given during adolescence and adulthood (postnatal weeks 4-40), producing hyperactivity, working memory deficits, and impairments in emotional processing, even at the low exposure levels corresponding to second-hand smoke. Although TSE effects were highly correlated with those of Nic, the effects of TSE were much larger than could be attributed to just the Nic in the mixture. Indeed, TSE effects more closely resembled those of the 10-fold higher Nic levels, but still exceeded their magnitude. In combination with our earlier findings, this study thus completes the chain of causation to prove that second-hand smoke exposure causes neurodevelopmental deficits, originating in disruption of neurodifferentiation, leading to miswiring of neuronal circuits, and as shown here, culminating in behavioral dysfunction. As low level exposure to Nic alone produced neurobehavioral teratology, 'harm reduction' Nic products do not abolish the potential for neurodevelopmental damage.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Health Consequences of Involuntary Exposure to Tobacco Smoke: A Report of the Surgeon General
(2006) · PsycEXTRA Dataset · doi:10.1037/e601432007-001 · Cited by 1,877 · see citing works
Prenatal and postnatal environmental tobacco smoke exposure and children's health.
Difranza, J., Aligne, C., & Weitzman, M. (2004) · Pediatrics · doi:10.1542/peds.113.s3.1007 · Cited by 806 · see citing works
Exposure to environmental tobacco smoke and cognitive abilities among u.S. Children and adolescents
Yolton, K., Dietrich, K., Auinger, P., Lanphear, B. P., & Hornung, R. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7210 · Cited by 331 · see citing works
Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment
Herrmann, M. S., King, K., & Weitzman, M. (2008) · Current opinion in pediatrics · doi:10.1097/mop.0b013e3282f56165 · Cited by 254 · see citing works
Maternal tobacco smoking, nicotine replacement and neurobehavioural development
Pauly, J. R., & Slotkin, T. A. (2008) · Acta Paediatrica · doi:10.1111/j.1651-2227.2008.00852.x · Cited by 214 · see citing works
Slotkin, T. A. (2008) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2007.09.002 · Cited by 206 · see citing works
Trauth, J. A., Seidler, F. J., & Slotkin, T. A. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02208-3 · Cited by 189 · see citing works
Ballbè, M., Martínez-Sánchez, J. M., Sureda, X., Fu, M., Pérez-Ortuño, R., Pascual, J. A., Saltó, E., & Fernández, E. (2014) · Environmental Research · doi:10.1016/j.envres.2014.09.005 · Cited by 188 · see citing works
Secondhand Smoke Exposure and Mental Health Among Children and Adolescents
Bandiera, F. C., Richardson, A. K., Lee, D. J., He, J.-P., & Merikangas, K. R. (2011) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpediatrics.2011.30 · Cited by 181 · see citing works
Vaglenova, J., Birru, S., Pandiella, N. M., & Breese, C. R. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.07.005 · Cited by 180 · see citing works
Gaysina, D., Fergusson, D. M., Leve, L. D., Horwood, J., Reiss, D., Shaw, D. S., Elam, K. K., Natsuaki, M. N., Neiderhiser, J. M., & Harold, G. T. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.127 · Cited by 152 · see citing works
Slotkin, T. A., MacKillop, E. A., Rudder, C. L., Ryde, I. T., Tate, C. A., & Seidler, F. J. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301231 · Cited by 149 · see citing works
Jacobsen, L. K., Slotkin, T. A., Mencl, W. E., Frost, S. J., & Pugh, K. R. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301398 · Cited by 144 · see citing works
Prenatal nicotine effects on memory in rats: pharmacological and behavioral challenges
Levin, E. D., Wilkerson, A., Jones, J. P., Channelle Christopher, N., & Briggs, S. J. (1996) · Developmental Brain Research · doi:10.1016/s0165-3806(96)00144-7 · Cited by 137 · see citing works
Prenatal nicotine exposure and cognitive performance in rats
Levin, E. D., Briggs, S. J., Christopher, N. C., & Rose, J. E. (1993) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(93)90006-a · Cited by 130 · see citing works
Schneider, T., Ilott, N., Brolese, G., Bizarro, L., Asherson, P. J. E., & Stolerman, I. P. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.249 · Cited by 97 · see citing works
Slikker, W., Xu, Z., Levin, E., & Slotkin, T. (2005) · Critical Reviews in Toxicology · doi:10.1080/10408440591007421 · Cited by 95 · see citing works
Slotkin, T. A., Pinkerton, K. E., & Seidler, F. J. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.8286 · Cited by 69 · see citing works
Effects of maternal intravenous nicotine administration on locomotor behavior in pre-weanling rats.
Lesage, M., Gustaf, E., Dufek, M., & Pentel, P. (2006) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2006.10.012 · Cited by 59 · see citing works
Fewell, J. E., Smith, F. G., & Ng, V. K. Y. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.5.1968 · Cited by 55 · see citing works
Gender-related response in open-field activity following developmental nicotine exposure in rats
Romero, R. D., & Chen, W. A. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.04.033 · Cited by 53 · see citing works
Slotkin, T. A., Skavicus, S., Card, J., Stadler, A., Levin, E. D., & Seidler, F. J. (2015) · Toxicological Sciences · doi:10.1093/toxsci/kfv123 · Cited by 52 · see citing works
Slotkin, T. A., Pinkerton, K. E., Tate, C. A., & Seidler, F. J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.06.094 · Cited by 51 · see citing works
Liu, J., Leung, P. W. L., McCauley, L., Ai, Y., & Pinto-Martin, J. (2013) · NeuroToxicology · doi:10.1016/j.neuro.2012.11.005 · Cited by 46 · cited 1× · see citing works
“, 2005), with increased externalizing behavior (Liu et al., 2013), with emotional disorders (Bandiera et al.”
BackgroundNeurobehavioral phenotype of C57BL/6J mice prenatally and neonatally exposed to cigarette smoke
Amos‐Kroohs, R. M., Williams, M. T., Braun, A. A., Graham, D. L., Webb, C. L., Birtles, T. S., Greene, R. M., Vorhees, C. V., & Pisano, M. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2013.01.001 · Cited by 44 · see citing works
Yoon, K. H., Lee, B. D., Park, J., & Park, J. H. (2001) · Journal of Applied Physics · doi:10.1063/1.1388572 · Cited by 43 · see citing works
Chronic neonatal nicotine increases anxiety but does not impair cognition in adult rats.
Huang, L. Z., Liu, X., Griffith, W. H., & Winzer‐Serhan, U. H. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.6.1342 · Cited by 42 · see citing works
Slotkin, T. A., Ryde, I. T., & Seidler, F. J. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.05.007 · Cited by 37 · see citing works
Evlampidou, I., Bagkeris, M., Vardavas, C. I., Koutra, K., Patelarou, E., Koutis, A. D., Chatzi, L., & Kogevinas, M. (2015) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2015.03.006 · Cited by 34 · see citing works
Levin, E. D., Hao, I., Burke, D. A., Cauley, M. C., Hall, B. J., & Rezvani, A. H. (2014) · Journal of Psychopharmacology · doi:10.1177/0269881114543721 · Cited by 34 · see citing works
Terra Cognita: Using Earth Observing Systems to Understand Our World
Schmidt, C. W. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.113-a98 · Cited by 33 · see citing works
Golub, M. S., Slotkin, T. A., Tarantal, A. F., & Pinkerton, K. E. (2007) · Brain Research · doi:10.1016/j.brainres.2007.03.001 · Cited by 22 · see citing works
Fuller, B. F., Cortes, D. F., Landis, M. K., Yohannes, H., Griffin, H. E., Stafflinger, J. E., Bowers, M. S., Lewis, M. H., Fox, M. A., & Ottens, A. K. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104857 · Cited by 21 · see citing works
Slotkin, T. A., Card, J., Stadler, A., Levin, E. D., & Seidler, F. J. (2014) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2014.03.002 · Cited by 20 · see citing works
Secondhand Tobacco Smoke Exposure and Neuromotor Function in Rural Children
Yeramaneni, S., Dietrich, K. N., Yolton, K. A., Parsons, P. J., Aldous, K. M., & Haynes, E. N. (2015) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2015.03.014 · Cited by 19 · see citing works
Slotkin, T. A., Card, J., & Seidler, F. J. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1306528 · Cited by 19 · see citing works
Gospe, S. M., Joyce, J. A., Siebert, J. R., Jack, R. M., & Pinkerton, K. E. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.11.049 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
England, L. J., Aagaard, K., Bloch, M., Conway, K., Cosgrove, K., Grana, R., Gould, T. J., Hatsukami, D., Jensen, F., Kandel, D., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.013 · Cited by 181 · see citing works
Self-citationFetal programming of neuropsychiatric disorders
Faa, G., Manchia, M., Pintus, R., Gerosa, C., Marcialis, M. A., & Fanos, V. (2016) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21139 · Cited by 160 · see citing works
Nicotine exposure of male mice produces behavioral impairment in multiple generations of descendants
McCarthy, D. M., Morgan, T. J., Lowe, S. E., Williamson, M. J., Spencer, T. J., Biederman, J., & Bhide, P. G. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006497 · Cited by 140 · see citing works
Paternal THC exposure in rats causes long-lasting neurobehavioral effects in the offspring
Levin, E. D., Hawkey, A. B., Hall, B. J., Cauley, M. C., Slade, S. K., Yazdani, E., Kenou, B., White, H., Wells, C., Rezvani, A. H., et al. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.04.003 · Cited by 78 · see citing works
Attention and working memory deficits in a perinatal nicotine exposure mouse model
Zhang, L., Spencer, T., Biederman, J., & Bhide, P. (2018) · PLoS ONE · doi:10.1371/journal.pone.0198064 · Cited by 65 · see citing works
Vorhees, C. V., Williams, M. T., Hawkey, A. B., & Levin, E. D. (2021) · Frontiers in Toxicology · doi:10.3389/ftox.2021.629229 · Cited by 58 · see citing works
A systematic review of possible serious adverse health effects of nicotine replacement therapy
Lee, P. N., & Fariss, M. (2016) · Archives of Toxicology · doi:10.1007/s00204-016-1856-y · Cited by 56 · see citing works
Zhu, J., Fan, F., McCarthy, D. M., Zhang, L., Cannon, E. N., Spencer, T. J., Biederman, J., & Bhide, P. G. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.01.014 · Cited by 54 · see citing works
Alkam, T., Mamiya, T., Kimura, N., Yoshida, A., Kihara, D., Tsunoda, Y., Aoyama, Y., Hiramatsu, M., Kim, H.-C., & Nabeshima, T. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4591-z · Cited by 50 · see citing works
Yang, X., Guo, A., Pang, Y., Cheng, X., Xu, T., Li, X., Liu, J., Zhang, Y., & Liu, Y. (2019) · Marine Drugs · doi:10.3390/md17010024 · Cited by 44 · see citing works
Paternal Nicotine Exposure in Rats Produces Long-lasting Neurobehavioral Effects in the Offspring
Hawkey, A., White, H., Pippen, E., Greengrove, E., Rezvani, A., Murphy, S. K., & Levin, E. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.05.001 · Cited by 30 · see citing works
Impact of maternal prenatal smoking on fetal to infant neurobehavioral development
Stroud, L. R., McCallum, M., & Salisbury, A. L. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000676 · Cited by 35 · see citing works
Holloway, Z. R., Hawkey, A. B., Pippin, E., White, H., Wells, C., Kenou, B., Rezvani, A. H., Murphy, S. K., & Levin, E. D. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2020.01.009 · Cited by 34 · see citing works
Nguyen, T., Li, G. E., Chen, H., Cranfield, C. G., McGrath, K. C. Y., & Gorrie, C. A. (2019) · Toxicological Sciences · doi:10.1093/toxsci/kfz194 · Cited by 33 · see citing works
Martin, M. M., McCarthy, D. M., Schatschneider, C. W., Trupiano, M. X., Jones, S. K., Kalluri, A., & Bhide, P. G. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz207 · Cited by 25 · see citing works
Slotkin, T. A., Skavicus, S., Ko, A., Levin, E. D., & Seidler, F. J. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy241 · Cited by 23 · see citing works
Prenatal Nicotine Exposure in Rodents: Why Are There So Many Variations in Behavioral Outcomes?
Polli, F. S., & Kohlmeier, K. A. (2019) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntz196 · Cited by 23 · see citing works
Hawkey, A. B., Piatos, P., Holloway, Z., Boyda, J., Koburov, R., Fleming, E., Giulio, R. T. D., & Levin, E. D. (2022) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2022.107121 · Cited by 22 · see citing works
Holloway, Z. R., Hawkey, A. B., Torres, A. K., Evans, J., Pippen, E., White, H., Katragadda, V., Kenou, B., Wells, C., Murphy, S. K., et al. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2020.10.007 · Cited by 22 · see citing works
Prenatal Nicotine Exposure Disrupts Infant Neural Markers of Orienting
King, E., Campbell, A., Belger, A., & Grewen, K. (2017) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntx177 · Cited by 21 · see citing works
Gatzke‐Kopp, L. M., Willoughby, M. T., Warkentien, S., Petrie, D. J., Mills-Koonce, R., & Blair, C. (2019) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13157 · Cited by 23 · see citing works
Heritable consequences of paternal nicotine exposure: from phenomena to mechanisms†
McCarthy, D. M., & Bhide, P. G. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab116 · Cited by 17 · see citing works
An Epigenetic Synopsis of Parental Substance Use
Lo, J. O.-T., D'Mello, R. J., Watch, L., Schust, D. J., & Murphy, S. K. (2023) · Epigenomics · doi:10.2217/epi-2023-0064 · Cited by 18 · see citing works
Hawkey, A. B., Junaid, S., Yao, L., Spiera, Z., White, H., Cauley, M. C., & Levin, E. D. (2019) · Birth Defects Research · doi:10.1002/bdr2.1568 · Cited by 18 · see citing works
Curcumin prevents cigarette smoke extract induced cognitive impairment
Thilagavathi, L., Jabeen, S., Ravishankar, S. B., Ahmed, S. S., George, T., Rishitha, N., Muthuraman, A., & Paramakrishnan, N. (2018) · Frontiers in Bioscience-Elite · doi:10.2741/e850 · Cited by 16 · see citing works
Shang, Y.-Z., Liu, Q., Ding, S., & Zhang, H. (2021) · Combinatorial Chemistry & High Throughput Screening · doi:10.2174/1386207324666210506152320 · Cited by 16 · see citing works
Cauley, M. C., Hall, B. J., Abreu‐Villaça, Y., Junaid, S., White, H., Kiany, A., Slotkin, T. A., & Levin, E. D. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.07.012 · Cited by 15 · see citing works
Shiohama, T., Hisada, A., Yamamoto, M., Sakurai, K., Takatani, R., Fujii, K., Shimojo, N., Mori, C., the Japan Environment Children’s Study (JECS) Group, Kamijima, M., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-98311-2 · Cited by 14 · see citing works
Is There a Critical Period for the Developmental Neurotoxicity of Low-Level Tobacco Smoke Exposure?
Slotkin, T. A., Stadler, A., Skavicus, S., Card, J., Ruff, J., Levin, E. D., & Seidler, F. J. (2016) · Toxicological Sciences · doi:10.1093/toxsci/kfw180 · Cited by 14 · see citing works
Child and family health in the era of prevention: new opportunities and challenges
Fuemmeler, B. F., Behrman, P., Taylor, M. B., Sokol, R. L., Rothman, E. F., Jacobson, L. T., Wischenka, D. M., & Tercyak, K. P. (2016) · Journal of Behavioral Medicine · doi:10.1007/s10865-016-9791-1 · Cited by 11 · see citing works
Wang, Z., Shi, H. C., Peng, L., Zhou, Y., Wang, Y., & Jiang, F. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-21767-w · Cited by 9 · see citing works
Li, Q., Cai, X., Zhou, H., Ma, D., & Li, N. (2024) · Frontiers in Public Health · doi:10.3389/fpubh.2024.1386137 · Cited by 8 · see citing works
Investigation of white matter functional networks in young smokers
Wang, J., Xue, T., Song, D., Dong, F., Cheng, Y., Wang, J., Ma, Y., Zou, M., Ding, S., Tao, Z., et al. (2024) · NeuroImage · doi:10.1016/j.neuroimage.2024.120917 · Cited by 8 · see citing works
Neurotoxicology of nicotine and tobacco
Levin, E. D. (2022) · Advances in neurotoxicology · doi:10.1016/bs.ant.2022.06.003 · Cited by 6 · see citing works
Hawkey, A. B., Natarajan, S., Kelly, O. J., Gondal, A., Wells, C., Jones, M. L., Rezvani, A. H., Murphy, S. K., & Levin, E. D. (2024) · NeuroToxicology · doi:10.1016/j.neuro.2024.05.005 · Cited by 6 · see citing works
Faure, A., Zoratto, F., Chirico, D., Romano, E., Mancinelli, R., Saso, L., Callebert, J., Giovanni Laviola, A., Granon, S., & Adriani, W. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.06.014 · Cited by 6 · see citing works
Addicott, M. (2020) · Cognition and Addiction · doi:10.1016/b978-0-12-815298-0.00009-5 · Cited by 3 · see citing works
World no-tobacco: effects of second-hand smoke (SHS) and vapors on the developing and adult brain
Kisby, G. E., & Raber, J. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1466332 · Cited by 6 · see citing works
on behalf of the Canadian Neonatal Network, Ediger, K., The Canadian Neonatal Follow-Up Network, Hasan, S. U., Synnes, A. R., Shah, J. P., Creighton, D., Isayama, T., Shah, P. S., & Lodha, A. K. (2019) · Journal of Perinatology · doi:10.1038/s41372-019-0356-3 · Cited by 5 · see citing works
Developmental nicotine exposure and masculinization of the rat preoptic area
Joglekar, R., Cauley, M. C., Lipsich, T., Corcoran, D. L., Patisaul, H. B., Levin, E. D., Meyer, J. N., McCarthy, M. M., & Murphy, S. K. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.01.005 · Cited by 5 · see citing works
Developmental Neurotoxicity of Nicotine and Tobacco
Levin, E. D., & Abreu‐Villaça, Y. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809405-1.00039-0 · Cited by 5 · see citing works
Holloway, Z., Koburov, R., Hawkey, A. B., & Levin, E. D. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173069 · Cited by 4 · see citing works
Castellví, J. R., Murphy, M. M., Voltas, N., Solé-Navais, P., Cavallé, P., Fernandez-Ballart, J. D., Ballesteros, M., & Canals, J. (2021) · Journal of Child and Family Studies · doi:10.1007/s10826-021-01978-4 · Cited by 4 · see citing works
Ukkirapandian, K., Kayalvizhi, E., Revathy, K., Brindha, T. R., Rangasmy, M., & Chandrasekar, M. (2021) · Biomedicine · doi:10.51248/.v41i1.526 · Cited by 4 · see citing works
Neurobehavioral effects of choninergic drugs in prenatal period
Владимировна, С. Е., Алексеевич, Г. Н., & Shabanov, P. D. (2017) · Reviews on Clinical Pharmacology and Drug Therapy · doi:10.17816/rcf1535-21 · Cited by 3 · see citing works
Prenatal Nicotine Exposure and Neuronal Progenitor Cells
Alkam, T., & Nabeshima, T. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813035-3.00006-x · Cited by 2 · see citing works
Frontal Cortex Proteome Perturbation after Juvenile Rat Secondhand Smoke Exposure
Lewis, L. S. C., Muldoon, P. P., Pilaka, P. P., & Ottens, A. K. (2018) · PROTEOMICS · doi:10.1002/pmic.201800268 · Cited by 2 · see citing works
Goutal, S., Tran, T., Leroy, C., Benhamouda, N., Leterrier, S., Saba, W., Lafont, B., Tartour, É., Roelens, M., & Tournier, N. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.4c00204 · Cited by 1 · see citing works
Secondhand Smoke Exposure and Depressive Symptoms Among Nonsmokers in China
Cui, X., Zhang, W. S., & Xu, L. (2025) · Behavioural Neurology · doi:10.1155/bn/1170641 · Cited by 1 · see citing works
Stadnikov, A. A., Kuz'micheva, N. A., Пушкарева, Л. А., Ермолина, Е. В., Mikhailova, I. V., & Smolyagin, A. I. (2023) · Journal of Anatomy and Histopathology · doi:10.18499/2225-7357-2023-12-1-64-71 · Cited by 1 · see citing works
Chronic Nicotine Effects on Memory and Nicotine Self-Administration: Age of Exposure is Key
Levin, E. D. (2018) · Advances in neurotoxicology · doi:10.1016/bs.ant.2018.03.003 · Cited by 1 · see citing works
PEMIKIRAN JIHAD KH. HASYIM ASY'ARI DAN IMAM SAMUDRA : STUDI PERBANDINGAN
Rahmatullah, M. (2013) · Digilib UIN Sunan Ampel Surabaya (UIN Sunan Ampel) · Cited by 1 · see citing works
Prenatal Nicotine Exposure and Impact on the Behaviors of Offspring
Alkam, T., & Nabeshima, T. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813035-3.00024-1
Nicotine exposure and mild cognitive impairment in the elderly：A mixtures approachPreprint
王, 佳., zhang, J., Ren, X., Liu, P., Fu, Y., Zhi, Y., Zhou, Q., Xu, B., Chen, X. D., Wu, D., et al. (2023) · Research Square · doi:10.21203/rs.3.rs-3168718/v1
Kisby, G. E., & Raber, J. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-29090-9.00021-0
Prenatal Cannabis and Tobacco: Studies in Animal Models
Edenfield, R. C., D'Mello, R. J., Shorey‐Kendrick, L. E., Crosland, A., Hagen, O. L., McEvoy, C. T., Spindel, E. R., Murphy, S. K., Lo, J. O.-T., & Wetendorf, M. (2026) · Advances in experimental medicine and biology · doi:10.1007/978-3-032-12741-9_9
Nicotine Exposure During Gestation: From Placental Dysfunction to Long‐Term Neurobehavioral Outcomes
Dave, H., Maru, S., & Johar, K. (2026) · Birth Defects Research · doi:10.1002/bdr2.70115
- Authors
- Hall, B. J., Cauley, M., Burke, D. A., Kiany, A., Slotkin, T. A., & Levin, E. D.
- Affiliations
- Duke University (US)
- Corresponding author
- Levin, Edward D.
- Venue
- Toxicological Sciences
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-02-26
- Volume
- 151
- Issue
- 2
- Pages
- 236-244
- ISSN
- 1096-0929 (ISSN-L)
- 1096-6080
- PMC
- PMC4880133
- OpenAlex
- W2288701263
- Cited by
- 57
- References
- 37
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 4 · 2021: 6 · 2020: 3 · 2019: 13 · 2018: 9 · 2017: 4 · 2016: 5 · 2013: 1
- FWCI
- 12.02
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Toxicological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- U.S. Environmental Protection Agency (83543701)
- Acorda Therapeutics
- National Institutes of Health (ES022831)
- National Institute of Environmental Health Sciences (P01ES022831)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- passive smoking, nicotine, prenatal exposure, fetal brain development, neurodevelopmental deficits, hyperactivity, working memory deficits, emotional processing, maternal smoking
- MeSH terms
- Age Factors, Animals, Behavior, Animal, Cognition, Cognition Disorders, Emotions, Female, Gestational Age, Male, Memory, Memory Disorders, Motor Activity, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Tobacco Smoke Pollution, Rats, Sprague-Dawley, Risk Assessment, Nicotinic Agonists, Maze Learning, Recognition, Psychology
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
