Maternal smoking during pregnancy and infant stress response: test of a prenatal programming hypothesis
Open accessAbstract
Background Maternal smoking during pregnancy (MSDP) is associated with early and long-term neurobehavioral deficits; however mechanisms remain unknown. We tested the hypothesis that MSDP programs the hypothalamic pituitary adrenocortical (HPA) axis of the offspring leading to adverse outcomes. In an intensive, prospective study, we investigated associations between MSDP and infant cortisol stress response and explored whether alterations in cortisol response were mediated by epigenetic modulation of the placental glucocorticoid receptor gene (NR3C1).Methods Participants were 100 healthy mother-infant pairs (53% MSDP-exposed; 42% female) from a low income, racially/ethnically diverse sample (55% minorities). MSDP was assessed by timeline followback interview verified by saliva and meconium cotinine. Infant cortisol responses to a neurobehavioral exam were assessed seven times over the first postnatal month. Methylation of placental NR3C1 promoter exon 1F was assessed using bisulfite pyrosequencing in a subsample (n=45).Results MSDP-exposed infants showed significantly and persistently attenuated basal and reactive cortisol levels over the first postnatal month vs. unexposed infants. Exploratory analyses revealed that MSDP was associated with altered methylation of the placental NR3C1 promoter; degree of methylation of the placental NR3C1 was associated with infant basal and reactive cortisol over the first postnatal month and mediated effects of MSDP on infant basal cortisol.Conclusions Results provide initial support for our hypothesis that MSDP programs offspring HPA (dys)regulation. Epigenetic regulation of placental GR may serve as a novel underlying mechanism. Results may have implications for delineating pathways to adverse outcomes from MSDP.
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.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Infants aged 1-7 months show altered cortisol response to stress.
“infants aged 1-7 months showed altered cortisol response to stress.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [135]
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
1 retracted
Owen, D., Andrews, M. H., & Matthews, S. G. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.004 · Cited by 207 · see citing works
RetractedBaron, R. M., & Kenny, D. A. (1986) · Journal of Personality and Social Psychology · doi:10.1037//0022-3514.51.6.1173 · Cited by 91,542 · see citing works
Baron, R. M., & Kenny, D. A. (1986) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.51.6.1173 · Cited by 91,532 · see citing works
Hamilton, M. (1960) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.23.1.56 · Cited by 32,817 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Effect of In Utero and Early-Life Conditions on Adult Health and Disease
Gluckman, P. D., Hanson, M. A., Cooper, C., & Thornburg, K. L. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0708473 · Cited by 3,898 · see citing works
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00108-7 · Cited by 3,638 · see citing works
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Births: preliminary data for 2012.
Hamilton, B. E., Martin, J. A., & Ventura, S. J. (2013) · PubMed · Cited by 1,509 · see citing works
Oberlander, T. F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., & Devlin, A. M. (2008) · Epigenetics · doi:10.4161/epi.3.2.6034 · Cited by 1,432 · see citing works
Comparison of tests used to distinguish smokers from nonsmokers
Jarvis, M. J., Tunstall-Pedoe, H., Feyerabend, C., Vesey, C., & Saloojee, Y. (1987) · American Journal of Public Health · doi:10.2105/ajph.77.11.1435 · Cited by 994 · cited 2× · see citing works
“Bioassays Saliva cotinine is a reliable biomarker for nicotine levels (Jarvis et al., 1987).”
BackgroundWadhwa, P. D., Buß, C., Entringer, S., & Swanson, J. (2009) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1237424 · Cited by 986 · see citing works
National Vital Statistics Reports NCHS.pdf
Hoyert, D. (2012) · Medical Entomology and Zoology · Cited by 982 · see citing works
Child maltreatment and the developing HPA axis
Tarullo, A. R., & Gunnar, M. R. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.010 · Cited by 737 · see citing works
Reliability of the Timeline Followback for cocaine, cannabis, and cigarette use
Robinson, S. M., Sobell, L. C., Sobell, M. B., & Leo, G. I. (2014) · Psychology of Addictive Behaviors · doi:10.1037/a0030992 · Cited by 699 · see citing works
Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health
Meaney, M. J., Moshe Szyf, A., & Seckl, J. R. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.05.003 · Cited by 660 · see citing works
Prenatal stress, glucocorticoids and the programming of adult disease
Cottrell, E. C. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.019.2009 · Cited by 640 · see citing works
Tong, V. T., Dietz, P. M., Morrow, B., D’Angelo, D. V., Farr, S. L., Rockhill, K. M., & England, L. J. (2009) · PubMed · Cited by 619 · see citing works
Gunnar, M. R., Talge, N. M., & Herrera, A. M. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.02.010 · Cited by 567 · see citing works
Radtke, K. M., Ruf, M., Gunter, H. M., Dohrmann, K., Schauer, M., Meyer, A., & Elbert, T. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.21 · Cited by 511 · cited 1× · see citing works
“…studies of prenatal depression and adversity, in which maternal stress/depression was associated with altered methylation of NR3C1 in cord or peripheral blood, to prenatal substance exposure and a focus on placental NR3C1 methylation (Mulligan et al 2012; Oberlander et al 2008; Radtke et al 2011).”
BackgroundTyrka, A. R., Price, L. H., Marsit, C., Walters, O. C., & Carpenter, L. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030148 · Cited by 486 · see citing works
Shah, N. R., & Bracken, M. B. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(00)70240-7 · Cited by 394 · cited 1× · see citing works
“Offspring exposed to MSDP are at increased risk for costly and adverse medical outcomes, including low birth weight, preterm delivery, andincreased length of neonatal intensive care unit stays (Shah and Bracken, 2000; Dietz et al., 2010; Adams et al., 2011).”
BackgroundInfant Morbidity and Mortality Attributable to Prenatal Smoking in the U.S.
Dietz, P. M., England, L. J., Shapiro-Mendoza, C. K., Tong, V. T., Farr, S. L., & Callaghan, W. M. (2010) · American Journal of Preventive Medicine · doi:10.1016/j.amepre.2010.03.009 · Cited by 363 · see citing works
Brain development under stress: Hypotheses of glucocorticoid actions revisited
Oitzl, M. S., Champagne, D. L., van der Veen, R., & de Kloet, E. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.07.006 · Cited by 358 · see citing works
Mulligan, C., D'Errico, N., Stees, J., & Hughes, D. (2012) · Epigenetics · doi:10.4161/epi.21180 · Cited by 342 · see citing works
Buka, S. L., Shenassa, E. D., & NIAURA, R. S. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.11.1978 · Cited by 326 · see citing works
Bonnin, A., & Levitt, P. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.10.005 · Cited by 311 · see citing works
Smoking during pregnancy and newborn neurobehavior
Law, K. L., Stroud, L. R., LaGasse, L. L., Niaura, R., Liu, J., & Lester, B. M. (2003) · PEDIATRICS · doi:10.1542/peds.111.6.1318 · Cited by 307 · see citing works
Conradt, E. D., Lester, B. M., Appleton, A. A., Armstrong, D. A., & Marsit, C. J. (2013) · Epigenetics · doi:10.4161/epi.26634 · Cited by 299 · see citing works
The Neonatal Intensive Care Unit Network Neurobehavioral Scale procedures
Lester, B. M., Tronick, E. Z., & in collaboration with T. Berry Brazelton, M. (2004) · PEDIATRICS · doi:10.1542/peds.113.s2.641 · Cited by 295 · see citing works
Maternal care, the epigenome and phenotypic differences in behavior
Moshe Szyf, A., Weaver, I. C. G., & Meaney, M. J. (2007) · Reproductive Toxicology · doi:10.1016/j.reprotox.2007.05.001 · Cited by 263 · see citing works
De novo quantitative bisulfite sequencing using the pyrosequencing technology
Dupont, J.-M., Tost, J., Jammes, H., & Gut, I. G. (2004) · Analytical Biochemistry · doi:10.1016/j.ab.2004.05.007 · Cited by 253 · see citing works
Langley, K., Rice, F. J., van den Bree, M. B. M., & Thapar, A. (2005) · PubMed · Cited by 225 · see citing works
Developmental consequences of prenatal tobacco exposure
Cornelius, M. D., & Day, N. L. (2009) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328326f6dc · Cited by 209 · see citing works
Measures of Socioeconomic Status in Child Development Research: Data and Recommendations.
Gottfried, A. W. (1985) · Merrill-palmer Quarterly · Cited by 202 · see citing works
REVIEW ARTICLE: Epigenetics in the Placenta
Maccani, M. A., & Marsit, C. J. (2009) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2009.00716.x · Cited by 198 · see citing works
In utero tobacco exposure epigenetically modifies placental CYP1A1 expression
Suter, M., Abramovici, A., Showalter, L., Hu, M., Shope, C. D., Varner, M., & Aagaard-Tillery, K. (2010) · Metabolism · doi:10.1016/j.metabol.2010.01.013 · Cited by 188 · see citing works
Role of the hypothalamic–pituitary–adrenal axis in developmental programming of health and disease
Xiong, F., & Zhang, L. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.11.002 · Cited by 177 · see citing works
Filiberto, A. C., Maccani, M. A., Koestler, D. C., Wilhelm-Benartzi, C. S., Avissar-Whiting, M., Banister, C. E., Gagne, L. A., & Marsit, C. J. (2011) · Epigenetics · doi:10.4161/epi.6.5.15236 · Cited by 162 · see citing works
Determination of drugs of abuse in meconium
Moore, C. M., Negrusz, A., & Lewis, D. (1998) · Journal of Chromatography B Biomedical Sciences and Applications · doi:10.1016/s0378-4347(97)00479-9 · Cited by 140 · see citing works
Bromer, C., Marsit, C. J., Armstrong, D. A., Padbury, J. F., & Lester, B. M. (2012) · Developmental Psychobiology · doi:10.1002/dev.21061 · Cited by 116 · see citing works
Field, T. L., McCabe, P. M., Schneiderman, N., & Field, T. M. (2013) · Psychology Press eBooks · doi:10.4324/9780203781722 · Cited by 103 · see citing works
Maternal Smoking during Pregnancy and Newborn Neurobehavior: Effects at 10 to 27 Days
Stroud, L. R., Paster, R. L., Papandonatos, G. D., Niaura, R., Salisbury, A. L., Battle, C., Lagasse, L. L., & Lester, B. (2009) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2008.07.048 · Cited by 102 · cited 1× · see citing works
“Previous work has also revealed effects of MSDP on behavioral dysregulation in the neonatal period, including increased irritability and motor activity, and attention and self-regulation deficits (Law et al., 2003; Stroud et al., 2009; Yolton et al., 2009).”
BackgroundMaccani, J. Z. J., Koestler, D., Houseman, E., Marsit, C., & Kelsey, K. (2013) · Epigenomics · doi:10.2217/epi.13.63 · Cited by 95 · see citing works
Ramsay, D. S., Bendersky, M. I., & Lewis, M. (1996) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/21.6.833 · Cited by 86 · see citing works
Roles of the placenta in fetal brain development
Zeltser, L. M., & Leibel, R. L. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112239108 · Cited by 83 · see citing works
Wakschlag, L. S., LEVENTHAL, B. L., Pine, D. S., Pickett, K. E., & Carter, A. S. (2006) · Child Development · doi:10.1111/j.1467-8624.2006.00909.x · Cited by 82 · see citing works
Grandchild of the NBAS : The NICU N etwork N eurobehavioral S cale ( NNNS )
Tronick, E., & Lester, B. M. (2013) · Journal of Child and Adolescent Psychiatric Nursing · doi:10.1111/jcap.12042 · Cited by 68 · see citing works
Schuetze, P. A., Lopez, F. A., Granger, D. A., & Eiden, R. D. (2008) · Developmental Psychobiology · doi:10.1002/dev.20334 · Cited by 68 · see citing works
The effect of tobacco exposure on the fetal hypothalamic-pituitary-adrenal axis
McDonald, S., Walker, M., Perkins, S., Beyene, J., Murphy, K., Gibb, W., & Ohlsson, A. (2006) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2006.01089.x · Cited by 66 · see citing works
Gray, T. R., Shakleya, D. M., & Huestis, M. A. (2009) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-009-2680-5 · Cited by 63 · see citing works
Ostrea, E. M. (1999) · Current Problems in Pediatrics · doi:10.1016/s0045-9380(99)80046-2 · Cited by 59 · see citing works
Low-level prenatal exposure to nicotine and infant neurobehavior
Yolton, K., Khoury, J., Xu, Y., Succop, P., Lanphear, B., Bernert, J. T., & Lester, B. (2009) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2009.07.004 · Cited by 52 · see citing works
Gray, T. R., LaGasse, L. L., Smith, L. M., Derauf, C., Grant, P., Shah, R., Arria, A. M., Grotta, S. A. D., Strauss, A. A., Haning, W., et al. (2009) · Therapeutic Drug Monitoring · doi:10.1097/ftd.0b013e3181bb438e · Cited by 48 · see citing works
Varvarigou, A. A., Liatsis, S. G., Vassilakos, P., Decavalas, G., & Beratis, N. G. (2009) · Journal of Perinatal Medicine · doi:10.1515/jpm.2009.028 · Cited by 41 · see citing works
Infant delivery costs related to maternal smoking: an update
Adams, E. K., Melvin, C. L., Raskind-Hood, C., Joski, P. J., & Galactionova, E. (2011) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntr042 · Cited by 36 · see citing works
What changes in DNA Methylation take Place in Individuals Exposed to Maternal Smoking in Utero ?
Suter, M., & Aagaard, K. M. (2012) · Epigenomics · doi:10.2217/epi.12.7 · Cited by 36 · see citing works
Varvarigou, A. A., Petsali, M., Vassilakos, P., & Beratis, N. G. (2006) · Journal of Perinatal Medicine · doi:10.1515/jpm.2006.091 · Cited by 31 · see citing works
Poland, R. E., Lutchmansingh, P., Au, D., Edelstein, M., Lydecker, S., Hsieh, C., & McCracken, J. T. (1994) · Life Sciences · doi:10.1016/0024-3205(94)00318-1 · Cited by 16 · see citing works
Slotkin, T. A., Ryde, I. T., & Seidler, F. J. (2009) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2009.11.003 · Cited by 13 · see citing works
Poland, R. E., Lutchmansingh, P., Au, D., Hsieh, C., Afrane, S., Lydecker, S., & McCracken, J. T. (1994) · Developmental Brain Research · doi:10.1016/0165-3806(94)00143-x · Cited by 10 · see citing works
(1996) · PubMed · Cited by 8 · see citing works
Flagged first, then by citations
2 of the 64 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Palma-Gudiel, H., Córdova-Palomera, A., Leza, J. C., & Fañanás, L. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.016 · Cited by 347 · see citing works
Palma-Gudiel, H., Córdova-Palomera, A., Eixarch, E., Deuschle, M., & Fañanás, L. (2015) · Epigenetics · doi:10.1080/15592294.2015.1088630 · Cited by 240 · see citing works
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-citationParade, S. H., Huffhines, L. P., Daniels, T. E., Stroud, L. R., Nugent, N. R., & Tyrka, A. R. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01207-y · Cited by 177 · see citing works
Maternal Factors that Induce Epigenetic Changes Contribute to Neurological Disorders in Offspring
Banik, A., Kandilya, D., Ramya, S., Stünkel, W., Chong, Y. S., & Dheen, S. T. (2017) · Genes · doi:10.3390/genes8060150 · Cited by 157 · see citing works
Tyrka, A. R., Parade, S. H., Welch, E. S., Ridout, K. K., Price, L. H., Marsit, C., Philip, N. S., & Carpenter, L. L. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.112 · Cited by 135 · see citing works
Self-citationParade, S. H., Ridout, K. K., Seifer, R., Armstrong, D. A., Marsit, C. J., McWilliams, M. A., & Tyrka, A. R. (2016) · Child Development · doi:10.1111/cdev.12484 · Cited by 109 · see citing works
Prenatal maternal cortisol concentrations predict neurodevelopment in middle childhood
Davis, E. P., Head, K., Buß, C., & Sandman, C. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.10.005 · Cited by 110 · see citing works
Fetal lung and placental methylation is associated with in utero nicotine exposure
Chhabra, D., Sharma, S., Kho, A. T., Gaedigk, R., Vyhlidal, C. A., Leeder, J. S., Morrow, J., Carey, V. J., Weiss, S. T., Tantisira, K. G., et al. (2014) · Epigenetics · doi:10.4161/15592294.2014.971593 · Cited by 102 · see citing works
Stroud, L. R., Papandonatos, G. D., Parade, S. H., Salisbury, A. L., PHIPPS, M. G., Lester, B. M., Padbury, J. F., & Marsit, C. J. (2016) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000410 · Cited by 82 · see citing works
Epigenetics and neurodegeneration: role of early-life nutrition
Gabbianelli, R., & Damiani, E. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.01.014 · Cited by 81 · see citing works
Marked for Life: Epigenetic Effects of Endocrine Disrupting Chemicals
Jacobs, M. N., Marczylo, E. L., Guerrero‐Bosagna, C., & Rüegg, J. (2017) · Annual Review of Environment and Resources · doi:10.1146/annurev-environ-102016-061111 · Cited by 81 · see citing works
Appleton, A. A., Jackson, B. P., Karagas, M. R., & Marsit, C. J. (2017) · Epigenetics · doi:10.1080/15592294.2017.1320637 · Cited by 76 · see citing works
Parent, J., Parade, S. H., Laumann, L. E., Ridout, K. K., Yang, B.-Z., Marsit, C. J., Seifer, R., & Tyrka, A. R. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001298 · Cited by 72 · see citing works
Examining the joint contribution of placental NR3C1 and HSD11B2 methylation for infant neurobehavior
Appleton, A. A., Lester, B. M., Armstrong, D. A., Lesseur, C., & Marsit, C. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.11.004 · Cited by 72 · see citing works
Blunted Diurnal Cortisol Activity in Healthy Adults with Childhood Adversity
Kuras, Y. I., Assaf, N., Thoma, M. V., Gianferante, D., Hanlin, L. C., Chen, X., Fiksdal, A. S., & Rohleder, N. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00574 · Cited by 71 · see citing works
Altered placental DNA methylation patterns associated with maternal smoking: current perspectives
Maccani, J. Z. J., & Maccani, M. (2015) · Advances in Genomics and Genetics · doi:10.2147/agg.s61518 · Cited by 62 · see citing works
Paquette, A. G., Lester, B. M., Lesseur, C., Armstrong, D. A., Guerin, D. J., Appleton, A. A., & Marsit, C. J. (2015) · Epigenomics · doi:10.2217/epi.15.28 · Cited by 61 · see citing works
Huizink, A. C., & de Rooij, S. R. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000354 · Cited by 62 · see citing works
Gottschalk, M. G., Domschke, K., & Schiele, M. A. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00163 · Cited by 59 · see citing works
Prenatal substance exposure and offspring development: Does DNA methylation play a role?
Knopik, V. S., Marceau, K., Bidwell, L. C., & Rolan, E. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.01.009 · Cited by 45 · see citing works
Alvarez, H. A. O., Appleton, A. A., Fuller, C. H., Belcourt, A., & Kubzansky, L. D. (2018) · Current Environmental Health Reports · doi:10.1007/s40572-018-0191-2 · Cited by 59 · see citing works
Green, B. B., & Marsit, C. J. (2015) · Current Environmental Health Reports · doi:10.1007/s40572-015-0045-0 · Cited by 52 · see citing works
Stroud, L. R., Papandonatos, G. D., Salisbury, A. L., PHIPPS, M. G., Huestis, M. A., NIAURA, R. S., Padbury, J. F., Marsit, C. J., & Lester, B. M. (2016) · Child Development · doi:10.1111/cdev.12482 · Cited by 51 · see citing works
Is physiological glucocorticoid replacement important in children?
Porter, J., Blair, J., & Ross, R. J. (2017) · Archives of Disease in Childhood · doi:10.1136/archdischild-2015-309538 · Cited by 50 · see citing works
Johnston, Z. C., Bellingham, M., Filis, P., Soffientini, U., Hough, D., Bhattacharya, S., Simard, M., Hammond, G. L., King, P., O’Shaughnessy, P. J., et al. (2018) · BMC Medicine · doi:10.1186/s12916-018-1009-7 · Cited by 44 · see citing works
Maternal Smoking in Pregnancy and Offspring Depression: a cross cohort and negative control study
Taylor, A. E., Carslake, D., de Mola, C. L., Rosenqvist, M. A., Nilsen, T. I. L., Bjørngaard, J. H., Horta, B. L., Pearson, R. M., Rai, D., Galanti, M. R., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-11836-3 · Cited by 46 · see citing works
Epigenetic Biomarkers of Preterm Birth and Its Risk Factors
Knight, A. K., & Smith, A. K. (2016) · Genes · doi:10.3390/genes7040015 · Cited by 45 · see citing works
Clifton, V. L., Cuffe, J. S. M., Moritz, K. M., Cole, T. J., Fuller, P. J., Lu, N. Z., Kumar, S., Chong, S., & Saif, Z. (2016) · Placenta · doi:10.1016/j.placenta.2016.12.017 · Cited by 43 · see citing works
Berretta, E., Guida, E., Forni, D., & Provenzi, L. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.003 · Cited by 44 · see citing works
Froggatt, S., Covey, J. A., & Reissland, N. (2019) · Acta Paediatrica · doi:10.1111/apa.15132 · Cited by 39 · see citing works
The impact of prenatal insults on the human placental epigenome: A systematic review
Palma‐Gudiel, H., Cirera, F., Crispi, F., Eixarch, E., & Fañanás, L. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.01.001 · Cited by 36 · 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
Prenatal tobacco and marijuana co-use: Impact on newborn neurobehavior
Stroud, L. R., Papandonatos, G. D., McCallum, M., Kehoe, T., Salisbury, A. L., & Huestis, M. A. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.09.003 · Cited by 37 · see citing works
Linking Cigarette Smoking/Tobacco Exposure and Cluster Headache: A Pathogenesis Theory
Rozen, T. D. (2018) · Headache The Journal of Head and Face Pain · doi:10.1111/head.13338 · Cited by 34 · see citing works
Eiden, R. D., Shisler, S., Granger, D. A., Schuetze, P. A., Colangelo, J., & Huestis, M. A. (2020) · International Journal of Behavioral Medicine · doi:10.1007/s12529-020-09875-8 · Cited by 32 · see citing works
Medical morbidities and DNA methylation of NR3C1 in preterm infants
Giarraputo, J., DeLoach, J., Padbury, J. F., Uzun, A., Marsit, C. J., Hawes, K., & Lester, B. M. (2016) · Pediatric Research · doi:10.1038/pr.2016.185 · Cited by 29 · see citing works
Massey, S. H., Mroczek, D. K., Reiss, D., Miller, E. S., Jakubowski, J. A., Graham, E. K., Shisler, S., McCallum, M., Huestis, M. A., Ganiban, J. M., et al. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.06.002 · Cited by 29 · see citing works
Prenatal Maternal Smoke, DNA Methylation, and Multi-omics of Tissues and Child Health
Cosín-Tomás, M., Cilleros-Portet, A., Aguilar-Lacasaña, S., Fernández-Jiménez, N., & Bustamante, M. (2022) · Current Environmental Health Reports · doi:10.1007/s40572-022-00361-9 · Cited by 26 · see citing works
Neonatal NR3C1 Methylation and Social-Emotional Development at 6 and 18 Months of Age
Folger, A. T., Ding, L., Ji, H., Yolton, K. A., Ammerman, R. T., Ginkel, J. B. V., & Bowers, K. A. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00014 · Cited by 28 · see citing works
Duko, B., Ayano, G., Pereira, G. F., Betts, K. S., & Alati, R. (2020) · Social Psychiatry and Psychiatric Epidemiology · doi:10.1007/s00127-020-01949-y · Cited by 27 · see citing works
Maternal electronic cigarette exposure in relation to offspring development: a comprehensive review
Zhang, Y., Angley, M., Qi, X., Lü, L., D’Alton, M. E., & He, K. (2022) · American Journal of Obstetrics & Gynecology MFM · doi:10.1016/j.ajogmf.2022.100659 · Cited by 29 · see citing works
Neuroendocrine and immune pathways from pre- and perinatal stress to substance abuse
Horn, S. R. G.-V., Roos, L. E., Berkman, E. T., & Fisher, P. A. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.09.004 · Cited by 24 · see citing works
Elevated methylation of the vault RNA2-1 promoter in maternal blood is associated with preterm birth
You, Y., Kwon, E. J., Hwang, H. S., Choi, S., Choi, S. K., & Kim, Y. J. (2021) · BMC Genomics · doi:10.1186/s12864-021-07865-y · Cited by 22 · see citing works
Nagarajan, S., Seddighzadeh, B., Baccarelli, A., Wise, L. A., Williams, M. A., & Shields, A. E. (2016) · Epigenomics · doi:10.2217/epi.16.9 · Cited by 20 · see citing works
Grant, K.-A., Sandman, C. A., Wing, D. A., Dmitrieva, J., & Davis, E. P. (2015) · Psychological Science · doi:10.1177/0956797615580299 · Cited by 20 · see citing works
Prenatal tobacco and marijuana co-use: Sex-specific influences on infant cortisol stress response
Stroud, L. R., Papandonatos, G. D., Jao, N. C., Vergara‐Lopez, C., Huestis, M. A., & Salisbury, A. L. (2020) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2020.106882 · Cited by 19 · see citing works
Varela, R. B., Cararo, J. H., Tye, S. J., Carvalho, A. F., Valvassori, S. S., Fries, G. R., & Quevedo, J. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104579 · Cited by 19 · see citing works
Vester, A. I., Hermetz, K. E., Burt, A., Everson, T. M., Marsit, C. J., & Caudle, W. M. (2020) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2020.106887 · Cited by 19 · see citing works
Prenatal inflammation exposure-programmed cardiovascular diseases and potential prevention
Deng, Y., Song, L., Nie, X., Shou, W., & Li, X. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.05.009 · Cited by 18 · see citing works
Massarsky, A., Jayasundara, N., Glazer, L., Levin, E. D., Prasad, G. L., & Giulio, R. T. D. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.07.003 · Cited by 17 · see citing works
Huang, K., Hu, Y., Sun, Y., Yu, Z., Liu, W. Y., Zhu, P., & Tao, F. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.11.014 · Cited by 17 · see citing works
Stunting at 5 Years Among SGA Newborns
Xie, C., Epstein, L. H., Eiden, R. D., Shenassa, E. D., Li, X., Liao, Y., & Wen, X. (2016) · PEDIATRICS · doi:10.1542/peds.2015-2636 · Cited by 17 · see citing works
Clark, C. A. C., Massey, S. H., Wiebe, S. A., Espy, K. A., & Wakschlag, L. S. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000706 · Cited by 18 · see citing works
Karl, M., Huth, V., Schälicke, S., Müller-Stark, C., Weise, V., Mack, J. T., Kirschbaum, C., Weidner, K., Garthus‐Niegel, S., & Steudte‐Schmiedgen, S. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105952 · Cited by 17 · see citing works
Bandoli, G., Coles, C. D., Kable, J. A., Wertelecki, W., Granovska, I. V., Pashtepa, A. O., Chambers, C., & CIFASD, T. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13081 · Cited by 16 · see citing works
Duko, B., Pereira, G. F., Betts, K. S., Tait, R. J., Newnham, J. P., & Alati, R. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.10.030 · Cited by 14 · see citing works
Effect of maternal smoking on stress physiology in healthy neonates
Haslinger, C., Bamert, H., Rauh, M., Burkhardt, T., & Schäffer, L. (2017) · Journal of Perinatology · doi:10.1038/jp.2017.172 · Cited by 14 · see citing works
Stroud, L. R., Vergara‐Lopez, C., McCallum, M., Gaffey, A. E., Corey, A., & NIAURA, R. S. (2019) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntz142 · Cited by 12 · see citing works
Chen, J., Qiu, M., Huang, Z., Chen, J., Zhou, C., Han, F., Qu, Y., Wang, S., Zhuang, J., & Li, X. (2020) · Reproductive Sciences · doi:10.1007/s43032-019-00095-4 · Cited by 12 · see citing works
de Vocht, F., Simpkin, A. J., Richmond, R. C., Relton, C. L., & Tilling, K. M. (2015) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph121114461 · Cited by 12 · see citing works
Buck, J. M., Yu, L., Knopik, V. S., & Stitzel, J. A. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab138 · Cited by 11 · see citing works
Duko, B., Pereira, G. F., Tait, R. J., Betts, K. S., Newnham, J. P., & Alati, R. (2022) · Psychiatry Research · doi:10.1016/j.psychres.2022.114466 · Cited by 10 · see citing works
Chen, J., Qiu, M., Huang, Z., Chen, J., Zhou, C., Han, F., Qu, Y., Wang, S., Zhuang, J., & Li, X. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00181-y · Cited by 10 · see citing works
Parade, S. H., Newland, R. P., Bublitz, M. H., & Stroud, L. R. (2019) · Stress · doi:10.1080/10253890.2018.1501019 · Cited by 8 · see citing works
Takahashi, M., & Shelton, R. C. (2025) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2025.1666599 · Cited by 10 · see citing works
Prenatal determinants of depressive symptoms in childhood: Evidence from Growing Up in New Zealand
Theunissen, G., D’Souza, S., Peterson, E. R., Walker, C. G., Morton, S., & Waldie, K. E. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.01.076 · Cited by 9 · see citing works
Ayano, G., Betts, K. S., Dachew, B. A., & Alati, R. (2021) · Addictive Behaviors · doi:10.1016/j.addbeh.2021.107072 · Cited by 6 · see citing works
Sex and Stress Hormones Across Development: A Focus on Early Behavior
Peckins, M. K., & Beltz, A. M. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.23624-9 · Cited by 6 · see citing works
Ayano, G., Betts, K. S., Lin, A. P., Tait, R. J., & Alati, R. (2021) · Psychiatry Research · doi:10.1016/j.psychres.2021.113781 · Cited by 5 · see citing works
Developmental Exposure to Air Pollution, Cigarettes, and Lead: Implications for Brain Aging
Finch, C. E., & Morgan, T. E. (2020) · Annual Review of Developmental Psychology · doi:10.1146/annurev-devpsych-042320-044338 · Cited by 5 · see citing works
Halabicky, O. M., Téllez‐Rojo, M. M., Miller, A. L., Goodrich, J. M., Dolinoy, D. C., Hu, H., & Peterson, K. E. (2023) · Environmental Research · doi:10.1016/j.envres.2023.116647 · Cited by 5 · see citing works
Balfour, D., Kleinig, Z., Mittinty, M., & Cohen‐Woods, S. (2026) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2026.111708 · Cited by 4 · see citing works
Duko, B., Bedaso, A., Dachew, B. A., Newnham, E. A., Gebremedhin, A. T., Tessema, G. A., Einarsdóttir, K., Alati, R., & Pereira, G. F. (2024) · Addictive Behaviors · doi:10.1016/j.addbeh.2024.107985 · Cited by 4 · see citing works
Zhang, Z., Yu, J., Li, Q., Zhao, Y., Tang, L., Peng, Y., Liu, Y. M., Gan, C., Liu, K., Wang, J., et al. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.12.075 · Cited by 5 · see citing works
Inhaling Risk: Smoking Impact on Male and Female Reproductive Health
Mishra, A., Khan, S. A., Jadhav, K., & Mehrotra, N. (2025) · Biosciences Biotechnology Research Asia · doi:10.13005/bbra/3338 · Cited by 4 · see citing works
Early-life Tobacco Smoke/Nicotine Exposure and Offspring Health
Kuniyoshi, K. M., Hang, B., & Rehan, V. K. (2020) · Springer eBooks · doi:10.1007/978-981-15-3797-4_2 · Cited by 4 · see citing works
Park, H. Y., Bang, M., Seo, E., Koo, S. J., Lee, E. M., Lee, S., & An, S. K. (2022) · Schizophrenia · doi:10.1038/s41537-022-00258-4 · Cited by 4 · see citing works
Epigenetic Alterations to NR3C1 and HSD11B2 and the Developmental Origins of Mental Disease Risk
Appleton, A. A., Holdsworth, E. A., & Ingle, M. E. (2016) · Epigenetics and human health · doi:10.1007/978-3-319-29901-3_5 · Cited by 4 · see citing works
Argote, M., Hilson, L., Sorkhou, M., & Rabin, R. A. (2025) · Drug and Alcohol Dependence Reports · doi:10.1016/j.dadr.2025.100376 · Cited by 6 · see citing works
Developmental pathways from prenatal substance exposure to reactive aggression
Godleski, S. A., Schuetze, P. A., Eiden, R. D., Nickerson, A. B., & Ostrov, J. M. (2022) · Journal of Applied Developmental Psychology · doi:10.1016/j.appdev.2022.101474 · Cited by 4 · see citing works
Willford, J. A., & Kaufman, J. M. (2024) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2024.107384 · Cited by 2 · see citing works
Cadmium Increases the Sensitivity of Adolescent Female Mice to Nicotine-Related Behavioral Deficits
Adeniyi, P. A., Olatunji, B. P., Ishola, A. O., Ajonijebu, D. C., & Ogundele, O. M. (2014) · Behavioural Neurology · doi:10.1155/2014/360978 · Cited by 2 · see citing works
Perceptions of family functioning impact smoking during pregnancy
Jao, N. C., Tan, M. M., Albanese, A. M., Lee, J.-Y., & Stroud, L. R. (2024) · Journal of Addictive Diseases · doi:10.1080/10550887.2024.2327732 · Cited by 1 · see citing works
de la Rosa, R., Steinmaus, C., Nardone, A., Keller, A., Acevedo, J., Catterina Ferreccio, R., Smith, M. T., & Sillé, F. C. M. (2026) · Environmental Health · doi:10.1186/s12940-026-01304-9 · Cited by 1 · see citing works
Neonatal AVPR1a Methylation and In-Utero Exposure to Maternal Smoking
Nidey, N., Bowers, K. A., Ding, L., Ji, H., Ammerman, R. T., Yolton, K. A., Mahabee‐Gittens, E. M., & Folger, A. T. (2023) · Toxics · doi:10.3390/toxics11100855 · Cited by 1 · see citing works
Salivary Bioscience Research Related to Prenatal Adversity
Shisler, S., Godleski, S. A., Molnar, D. S., & Eiden, R. D. (2020) · Springer eBooks · doi:10.1007/978-3-030-35784-9_25 · Cited by 1 · see citing works
Jassim, S., & Basheer, S. (2025) · medRxiv · doi:10.1101/2025.04.05.25325300 · Cited by 1 · see citing works
Methylome Analysis of Complex Diseases
Neidhart, M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-420194-1.00028-2
Biologically Controlled Mutations are Right for Evolution
Berczi, I. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801770-8.00010-0
Nüsken, E., Lechner, F., & Nüsken, K. (2016) · Frauenheilkunde up2date · doi:10.1055/s-0042-111926
Developmental, epigenetic, and possible transgenerational effects of smoking and vaping
Boyd, R. T. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-819958-9.00011-6
Early developmental risks for tobacco addiction: A probabilistic epigenesis framework
Ortega, L. A., Aragon-Carvajal, D. M., Cortes-Corso, K. T., & Forero-Castillo, F. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105499
Zhang, Z., Luo, H., Wang, X., Zhang, Y., Li, J., Hu, R., Guo, Y., Tan, J., Li, J., Wang, Y., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-3812822/v1
Reis, A. T., Madureira, J., Teixeira, J. P., & Costa, C. (2025) · Public health reviews · doi:10.3389/phrs.2025.1606742
You, Y., Kwon, E. J., Hwang, H.-S., Choi, S.-J., Choi, S. K., & Kim, Y. J. (2021) · Figshare · doi:10.6084/m9.figshare.14954675
You, Y., Kwon, E. J., Hwang, H.-S., Choi, S.-J., Choi, S. K., & Kim, Y. J. (2021) · Figshare · doi:10.6084/m9.figshare.14954669
You, Y., Kwon, E. J., Hwang, H.-S., Choi, S.-J., Choi, S. K., & Kim, Y. J. (2021) · Figshare · doi:10.6084/m9.figshare.14954672
You, Y., Kwon, E. J., Hwang, H.-S., Choi, S.-J., Choi, S. K., & Kim, Y. J. (2021) · Figshare · doi:10.6084/m9.figshare.14954663
- Authors
- Stroud, L. R., Papandonatos, G. D., Rodriguez, D., McCallum, M., Salisbury, A. L., Phipps, M. G., Lester, B., Huestis, M. A., Niaura, R., Padbury, J. F., & Marsit, C. J.
- Affiliations
- Brown University (US)
- La Salle University (US)
- Emory University (US)
- National Institutes of Health (US)
- Truth Initiative (US)
- Dartmouth College (US)
- Corresponding author
- Stroud, Laura R.
- ORCID
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2014-10
- Volume
- 48
- Pages
- 29-40
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC4136384
- OpenAlex
- W2021299571
- Cited by
- 104
- References
- 64
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 5 · 2023: 4 · 2022: 8 · 2021: 12 · 2020: 11 · 2019: 6 · 2018: 15 · 2017: 7 · 2016: 16 · 2015: 8 · 2014: 3
- FWCI
- 10.65
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Drug Abuse (R01DA019558, R01DA031188)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- smoking during pregnancy, infant cortisol, hypothalamic-pituitary-adrenal axis, prenatal programming, glucocorticoid receptor, NR3C1, DNA methylation, placenta, epigenetics, stress response, neurobehavioral outcomes, cotinine
- MeSH terms
- Adolescent, Adult, Female, Humans, Hydrocortisone, Infant, Newborn, Placenta, Pregnancy, Pregnancy Complications, Prenatal Exposure Delayed Effects, Receptors, Glucocorticoid, Smoking, Stress, Physiological, Case-Control Studies, DNA Methylation, Epigenesis, Genetic, Embryonic Development, Young Adult
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