The DOI matches its Crossref record; 61 of the 64 references it cites were found in a registry or an index.
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.
Overview
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
Verification
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?
In the citing paper
“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.
Citations
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 211
RetractedBaron, R. M., & Kenny, D. A. (1986) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.51.6.1173 · Cited by 91,532
Hamilton, M. (1960) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.23.1.56 · Cited by 32,817
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
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
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00108-7 · Cited by 3,638
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708
Births: preliminary data for 2012.
Hamilton, B. E., Martin, J. A., & Ventura, S. J. (2013) · PubMed · Cited by 1,509
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
Wadhwa, P. D., Buß, C., Entringer, S., & Swanson, J. (2009) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1237424 · Cited by 1,045
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×
“Bioassays Saliva cotinine is a reliable biomarker for nicotine levels (Jarvis et al., 1987).”
BackgroundNational Vital Statistics Reports NCHS.pdf
Hoyert, D. (2012) · Medical Entomology and Zoology · Cited by 982
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
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 · cited 3×
“At each interview, mothers completed the calendar/anchor-based Timeline Follow Back (TLFB) interview regarding smoking, drug, and alcohol use over pregnancy and three months prior to conception (Robinson et al., 2014).”
MethodInfluentialEpigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health
Meaney, M. J., Szyf, M., & Seckl, J. R. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.05.003 · Cited by 661
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
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 617
Gunnar, M. R., Talge, N. M., & Herrera, A. M. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.02.010 · Cited by 603
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×
“…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
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×
“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).”
BackgroundBrain 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 372
Infant 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
Mulligan, C., D'Errico, N., Stees, J., & Hughes, D. (2012) · Epigenetics · doi:10.4161/epi.21180 · Cited by 342
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
Conradt, E. D., Lester, B. M., Appleton, A. A., Armstrong, D. A., & Marsit, C. J. (2013) · Epigenetics · doi:10.4161/epi.26634 · Cited by 313
Bonnin, A., & Levitt, P. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.10.005 · Cited by 311
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
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
Maternal care, the epigenome and phenotypic differences in behavior
Szyf, M., Weaver, I. C. G., & Meaney, M. J. (2007) · Reproductive Toxicology · doi:10.1016/j.reprotox.2007.05.001 · Cited by 269
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
Langley, K., Rice, F. J., van den Bree, M. B. M., & Thapar, A. (2005) · PubMed · Cited by 225
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 215
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
Measures of Socioeconomic Status in Child Development Research: Data and Recommendations.
Gottfried, A. W. (1985) · Merrill-palmer Quarterly · Cited by 202
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
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
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
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 142
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
Field, T. L., McCabe, P. M., Schneiderman, N., & Field, T. M. (2013) · Psychology Press eBooks · doi:10.4324/9780203781722 · Cited by 103
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×
“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. C., Houseman, E. A., Marsit, C. J., & Kelsey, K. T. (2013) · Epigenomics · doi:10.2217/epi.13.63 · Cited by 101
Ramsay, D. S., Bendersky, M. I., & Lewis, M. (1996) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/21.6.833 · Cited by 86
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 85
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
Schuetze, P. A., Lopez, F. A., Granger, D. A., & Eiden, R. D. (2008) · Developmental Psychobiology · doi:10.1002/dev.20334 · Cited by 71
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
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
Gray, T. R., Shakleya, D. M., & Huestis, M. A. (2009) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-009-2680-5 · Cited by 63
Ostrea, E. M. (1999) · Current Problems in Pediatrics · doi:10.1016/s0045-9380(99)80046-2 · Cited by 59
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
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
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
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
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
Varvarigou, A. A., Petsali, M., Vassilakos, P., & Beratis, N. G. (2006) · Journal of Perinatal Medicine · doi:10.1515/jpm.2006.091 · Cited by 31
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
Slotkin, T. A., Ryde, I. T., & Seidler, F. J. (2009) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2009.11.003 · Cited by 13
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
(1996) · PubMed · Cited by 8
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
Palma-Gudiel, H., Córdova-Palomera, A., Eixarch, E., Deuschle, M., & Fañanás, L. (2015) · Epigenetics · doi:10.1080/15592294.2015.1088630 · Cited by 240
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
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 192
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 163
Metadata
- 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
