Fetal behavior in smoking compared to non-smoking pregnant women
Abstract
Objective To determine the effects of maternal smoking on fetal spontaneous behavior and auditory processing.Methods 38 fetuses of smoking (n=18) and non-smoking (n=20) mothers, stratified by gestational age (<37, >or=37 weeks GA), were examined at least 1h following smoking. Observations included spontaneous fetal heart rate (FHR; 20 min) and body movements (20 min) followed by a 2 min audiotape of the mother reading a story while FHR and body movements were recorded.Results There were no differences in spontaneous behaviors; full-term fetuses showed a FHR acceleration and body movement during the mother's voice. A FHR response following voice offset was limited to fetuses less than 37 weeks GA of non-smoking mothers.Conclusion Fetuses less than 37 weeks GA of mothers who smoke throughout pregnancy have a delayed onset of response to the maternal voice, a subtle difference which may have implications for later language development for prematurely born infants which needs further investigation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Fetuses of smokers show more maladaptive responses to the non-stress test, lower heart rate variability, more mouth and self-touch movements, and poorer recognition of maternal voice than fetuses of nonsmokers.
“found greater rates of maladaptive response to the non-stress test (a clinical index of fetal well-being)(96), including reduced heart rate variability, increased mouth and self-touch movements, and impaired recognition of maternal voice in fetuses of smokers compared with those of nonsmokers.”
From Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products (2017) · cites this paper as [97]
Cites
Of Human Bonding: Newborns Prefer Their Mothers' Voices
DeCasper, A. J., & Fifer, W. P. (1980) · Science · doi:10.1126/science.7375928 · Cited by 2,317 · see citing works
Effects of experience on fetal voice recognition
Kisilevsky, B. S., Hains, S. M. J., Lee, K., Xie, X., Huang, H., Ye, H. H., Zhang, K., & Wang, Z. (2003) · Psychological Science · doi:10.1111/1467-9280.02435 · Cited by 526 · see citing works
The biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant
Longo, L. D. (1977) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(77)90824-9 · Cited by 488 · see citing works
Social Development: a Psychobiological Perspective
Mason, W. A. (2008) · Integrative Psychological and Behavioral Science · doi:10.1007/s12124-008-9069-4 · Cited by 344 · see citing works
In utero exposure to cigarette smoking influences lung function at birth
Carlsen, K. L., Jaakkola, J. J. K., Nafstad, P. H. J., & Carlsen, K.-H. (1997) · European Respiratory Journal · doi:10.1183/09031936.97.10081774 · Cited by 260 · see citing works
Maternal smoking, pregnancy complications, and perinatal mortality
Meyer, M. B., & Tonascia, J. A. (1977) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(77)90031-x · Cited by 222 · see citing works
Sai, F. Z. (2004) · Infant and Child Development · doi:10.1002/icd.376 · Cited by 206 · see citing works
564. Maternal smoking, pregnancy complications, and perinatal mortality
&NA; (1977) · Nursing Research · doi:10.1097/00006199-197711000-00099 · Cited by 195 · see citing works
THE ACUTE EFFECT OF SMOKING ON INTERVILLOUS BLOOD FLOW OF THE PLACENTA
Lehtovirta, P., & Forss, M. (1978) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1978.tb15592.x · Cited by 184 · see citing works
Who continues to smoke while pregnant?
Cnattingius, S., Lindmark, G., & Meirik, O. (1992) · Journal of Epidemiology & Community Health · doi:10.1136/jech.46.3.218 · Cited by 167 · see citing works
Passive and active maternal smoking as measured by serum cotinine: the effect on birthweight.
Eskenazi, B., Prehn, A. W., & Christianson, R. E. (1995) · American Journal of Public Health · doi:10.2105/ajph.85.3.395 · Cited by 162 · see citing works
CIGARETTE SMOKING AND FETAL BREATHING MOVEMENTS
Manning, F. A., & Feyerabend, C. (1976) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1976.tb00823.x · Cited by 132 · see citing works
Smoking during pregnancy and preterm birth
Wisborg, K., Henriksen, T. B., Hedegaard, M. S., & Jergen, N. (1996) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1996.tb09877.x · Cited by 128 · see citing works
Development of fetal movement — fetal heart rate coupling from 20 weeks through term
DiPietro, J. A., Hodgson, D. M., Costigan, K. A., Hilton, S. C., & Johnson, T. R. B. (1996) · Early Human Development · doi:10.1016/0378-3782(95)01704-6 · Cited by 125 · see citing works
Effects of maternal smoking on circulating catecholamine levels and fetal heart rates
QUIGLEY, M. E., Sheehan, K. L., Wilkes, M. M., & Yen, S. S. C. (1979) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(79)90019-x · Cited by 109 · see citing works
Smotherman, W. P., & Robinson, S. R. (1990) · Medical Entomology and Zoology · Cited by 108 · see citing works
Human Fetal Behavior: 100 Years of Study
Kisilevsky, B. S., & Low, J. A. (1998) · Developmental Review · doi:10.1006/drev.1998.0452 · Cited by 88 · see citing works
Effect of cigarette smoking on fetal breathing movements in normal pregnancies.
Manning, F. A., Pugh, E. W., & Boddy, K. (1975) · BMJ · doi:10.1136/bmj.1.5957.552 · Cited by 70 · see citing works
Graça, L. M., Cardoso, C. G., Clode, N., & Calhaz–Jorge, C. (1991) · Journal of Perinatal Medicine · doi:10.1515/jpme.1991.19.5.385 · Cited by 58 · see citing works
Maturation of human fetal responses to airborne sound in low- and high-risk fetuses
Kisilevsky, B. S., Pang, L.-H., & Hains, S. M. J. (2000) · Early Human Development · doi:10.1016/s0378-3782(00)00075-x · Cited by 54 · see citing works
Maternal cigarette-smoking during pregnancy disrupts rhythms in fetal heart rate
Zeskind, P. S., & Gingras, J. L. (2006) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/jsj031 · Cited by 53 · see citing works
Effect of Maternal Smoking on Fetal Catecholamine Concentrations at Birth
Oncken, C. A., Henry, K. M., Campbell, W. A., Kuhn, C. M., Slotkin, T. A., & Kranzler, H. R. (2003) · Pediatric Research · doi:10.1203/00006450-200301000-00020 · Cited by 46 · see citing works
Placental diffusing capacity for carbon monoxide and oxygen in unanesthetized sheep
Longo, L. D., & Ching, K. S. (1977) · Journal of Applied Physiology · doi:10.1152/jappl.1977.43.5.885 · Cited by 43 · see citing works
Functional Development of Auditory Sensitivity in the Fetus and Neonate
Sohmer, H., & Freeman, S. (1995) · Journal of Basic and Clinical Physiology and Pharmacology · doi:10.1515/jbcpp.1995.6.2.95 · Cited by 40 · see citing works
The effect of cigarette smoking on fetal heart rate characteristics*1
ONCKEN, C. (2002) · Obstetrics & Gynecology · doi:10.1016/s0029-7844(02)01948-8 · Cited by 34 · see citing works
The behavior of the fetus as an indicator of neural functioning.
Hepper, P. G. (1995) · doi:10.4324/9780203773628-32 · Cited by 34 · see citing works
Change in smoking prevalence among pregnant women 1982-93.
Pj, S., Potter, J., Dulberg, C. S., Niday, P., Nimrod, C. A., & Tawagi, G. (1995) · PubMed · Cited by 32 · see citing works
The beginnings of mind–evidence from the behaviour of the fetus
Hepper, P. G., & Shahidullah, S. (1994) · Journal of Reproductive and Infant Psychology · doi:10.1080/02646839408408880 · Cited by 31 · see citing works
Smoking in pregnancy--a health education problem.
Mcknight, A., & Merrett, J. D. (1986) · PubMed · Cited by 30 · see citing works
Perkins, S. L., Belcher, J., & Livesey, J. F. (1997) · Canadian Journal of Public Health · doi:10.1007/bf03404788 · Cited by 28 · see citing works
Smoking in Dutch pregnant women and birth weight
Adriaanse, H. P., Knottnerus, J. A., Delgado, L. R., Cox, H. H., & Essed, G. G. M. (1996) · Patient Education and Counseling · doi:10.1016/0738-3991(95)00798-9 · Cited by 25 · see citing works
Smoking behaviour among pregnant women prior to antenatal care registration
Cnattingius, S., & Thorslund, M. (1990) · Social Science & Medicine · doi:10.1016/0277-9536(90)90135-f · Cited by 23 · see citing works
Chronic placental insufficiency has long-term effects on auditory function in the guinea pig
Rehn, A., Loeliger, M. M., Hardie, N. A., Rees, S. M., Dieni, S., & Shepherd, R. K. (2002) · Hearing Research · doi:10.1016/s0378-5955(02)00312-x · Cited by 23 · see citing works
Acute effects of nicotine on fetal heart rate variability
LEHTOVIRTA, P., FORSS, M., RAURAMO, I., & KARINIEMI, V. (1983) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1983.tb09299.x · Cited by 20 · see citing works
Interaction of smoking and maternal weight status in influencing infant size.
Muscati, S. K., Gray‐Donald, K., & Ee, N. (1995) · PubMed · Cited by 18 · see citing works
Salten, F. (1923) · Cited by 17 · see citing works
Rees, S. M., Proske, U., & Harding, R. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90282-6 · Cited by 15 · see citing works
RETIRED: Antenatal Fetal Assessment
(2000) · Journal SOGC · doi:10.1016/s0849-5831(16)31431-8 · Cited by 10 · see citing works
Acute Effects of Maternal Smoking on Human Fetal Heart Function
Sørensen, K. E., & Børlum, K. (1987) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016348709020750 · Cited by 9 · see citing works
Effects of Maternal Smoking on Amniotic Fluid Volume and Fetal Urine Output
Coulson, C. C., Thorp, J. M., Purrington, J., Slotchiver, J., Ananth, C. V., & Hartmann, K. E. (1996) · American Journal of Perinatology · doi:10.1055/s-2007-994362 · Cited by 8 · see citing works
Chronic placental insufficiency
Harding, P. G. R. (1970) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(70)90479-5 · Cited by 8 · see citing works
(2000) · Journal SOGC · doi:10.1016/s0849-5831(16)31433-1 · Cited by 5 · see citing works
MASSIVE INTRAPERITONEAL HEMORRHAGE DUE TO RUPTURE OF A TUBERCULOUS PELVIC ABSCESS.
MOSS, M., & Lin, T.-J. (1963) · PubMed · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Fetal sensitivity to properties of maternal speech and language
Kisilevsky, B. S., Hains, S. M. J., Brown, C., Lee, C. T., Cowperthwaite, B., Stutzman, S. S., Swansburg, M. L., Lee, K., Xie, X., Huang, H., et al. (2008) · Infant Behavior and Development · doi:10.1016/j.infbeh.2008.10.002 · Cited by 286 · see citing works
Electronic cigarettes and health outcomes: umbrella and systematic review of the global evidence
Banks, E., Yazidjoglou, A., Brown, S., Nguyen, N. M., Martin, M., Beckwith, K., Daluwatta, A., Campbell, S., & Joshy, G. (2023) · The Medical Journal of Australia · doi:10.5694/mja2.51890 · Cited by 272 · 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
Low Maternal Awareness of Fetal Movement is Associated With Small for Gestational Age Infants
Saastad, E., Ahlborg, T., & Frøen, J. F. (2008) · Journal of Midwifery & Women s Health · doi:10.1016/j.jmwh.2008.03.001 · Cited by 82 · see citing works
Fetal Neurology: The Role of Fetal Stress
Kadić, A. S. (2015) · Donald School Journal of Ultrasound in Obstetrics & Gynecology · doi:10.5005/jp-journals-10009-1386 · Cited by 61 · see citing works
Neuropathology of cigarette smoking
Chang, R. C., Ho, J. Y. S., Wong, C. S., Gentleman, S. M., & Ng, H. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1210-x · Cited by 53 · see citing works
Conde, A., Figueiredo, B., Tendais, I., Teixeira, C., Costa, R. A., Pacheco, A., Rodrigues, M. C., & Nogueira, R. (2010) · Journal of Psychosomatic Obstetrics & Gynecology · doi:10.3109/01674821003681464 · Cited by 53 · see citing works
The impact of maternal smoking on fast auditory brainstem responses
Kable, J. A., Coles, C. D., Lynch, M. E., & Carroll, J. (2009) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2009.02.002 · Cited by 47 · 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
Effects of Prenatal Nicotine Exposure on Infant Language Development: A Cohort Follow Up Study
Hernández‐Martínez, C., Voltas, N., Ribot, B., Arija, V., Macías, J. E., & Canals, J. (2016) · Maternal and Child Health Journal · doi:10.1007/s10995-016-2158-y · Cited by 29 · see citing works
Boerma, T., ter Haar, S. M., Ganga, R., Wijnen, F. N. K., Blom, E., & Wierenga, C. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105398 · Cited by 29 · see citing works
Reissland, N., Francis, B., Kumarendran, K., & Mason, J. (2015) · Acta Paediatrica · doi:10.1111/apa.13001 · Cited by 28 · see citing works
Fetal neurophysiology according to gestational age
Kadić, A. S., & Predojević, M. (2012) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2012.05.007 · Cited by 21 · see citing works
The Impact of Maternal Voice on the Fetus: A Systematic Review
Carvalho, M. E. S., Justo, J. M. R. D. M., Gratier, M., & da Silva, H. M. F. R. (2018) · Current Women s Health Reviews · doi:10.2174/1573404814666181026094419 · Cited by 15 · see citing works
Effects of Prenatal Exposure to Alcohol and Smoking on Fetal Heart Rate and Movement Regulation
Lucchini, M., Shuffrey, L. C., Nugent, J. D., Pini, N., Sania, A., Shair, M. C., Brink, L. T., du Plessis, C., Odendaal, H. J., Nelson, M. E., et al. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.594605 · Cited by 12 · see citing works
Technology for continuous long-term monitoring of pregnant women for safe childbirth
Endo, G. K., Oluwayomi, I., Alexandra, V. C. S., Athavale, Y. R., & Krishnan, S. (2017) · IEEE Canada International Humanitarian Technology Conference · doi:10.1109/ihtc.2017.8058200 · Cited by 11 · see citing works
Auditory Processing in Growth-Restricted Fetuses and Newborns and Later Language Development
Kisilevsky, B. S., Chambers, B., Parker, K. C. H., & Davies, G. (2013) · Clinical Psychological Science · doi:10.1177/2167702613509371 · Cited by 9 · see citing works
Atypical Fetal Response to the Mother's Voice in Diabetic Compared With Overweight Pregnancies
Kisilevsky, B. S., Gilmour, A., Stutzman, S. S., Hains, S. M. J., & Brown, C. A. (2012) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0b013e31823e791e · Cited by 9 · see citing works
Stroud, L. R., Bublitz, M. H., Crespo, F. A., Lester, B. M., & Salisbury, A. L. (2020) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2020.106894 · Cited by 8 · see citing works
Foetal mouth movements: Effects of nicotine
Froggatt, S., Reissland, N., Covey, J., & Kumarendran, K. (2021) · Acta Paediatrica · doi:10.1111/apa.16042 · Cited by 7 · see citing works
The Effect of Abused Substances on Antenatal and Intrapartum Fetal Testing and Well-Being
Kopel, E., & HILL, W. C. (2013) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3182802cad · Cited by 6 · see citing works
What We have Learned from Fetal Neurophysiology?
Salihagič-Kadić, A., & Predojević, M. (2012) · Donald School Journal of Ultrasound in Obstetrics & Gynecology · doi:10.5005/jp-journals-10009-1241 · Cited by 4 · see citing works
FETAL AND NEWBORN AUDITORY PROCESSING OF THE MOTHER'S AND FATHER'S VOICE
Yan, G., & Lee, C. (2010) · Cited by 3 · see citing works
Fetal Cognitive Functions and 3D/4D Ultrasound
Vasilj, O., Tomasović, S., Kadiæ, A. S., & Šurina, A. (2019) · Donald School Journal of Ultrasound in Obstetrics & Gynecology · doi:10.5005/jp-journals-10009-1584 · Cited by 3 · see citing works
Tikvica, A., Mišković, B., & Ahmed, B. I. (2008) · Donald School Journal of Ultrasound in Obstetrics & Gynecology · doi:10.5005/jp-journals-10009-1064 · Cited by 2 · see citing works
Kurjak, A., Stanojević, M., Ahmed, B., Azumendi, G., & Barišić, L. S. (2021) · CRC Press eBooks · doi:10.1201/9781003222590-58 · Cited by 1 · see citing works
Cigarette smoke exposure as a potential risk factor for sleep problems in pregnant women
Ciochoń, A., Balwicki, Ł., Klimek, M., Danel, D. P., Apanasewicz, A., Ziomkiewicz, A., Galbarczyk, A., & Marcinkowska, U. M. (2025) · Peer Community Journal · doi:10.24072/pcjournal.621 · Cited by 1 · see citing works
Kisilevsky, B. S., & Hains, S. M. J. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.01028.x
Justo, J. M. R. D. M., Graça, C. S. S., & Martins, M. S. A. (2019) · International Journal of Developmental and Educational Psychology Revista INFAD de psicología · doi:10.17060/ijodaep.2019.n1.v1.1381
Camacho, J. P. B. (2020) · Universidad Peruana de Ciencias Aplicadas (UPC) · doi:10.19083/tesis/650331
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
Singer, M., Kable, J. A., & Coles, C. D. (2026) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2026.107614
Fetal Behavior in High-risk Pregnancies Assessed by Ultrasound
Kurjak, A., Pooh, R. K., Stanojević, M., & Ahmed, B. (2026) · Donald School Journal of Ultrasound in Obstetrics & Gynecology · doi:10.5005/jp-journals-10009-2128
- Authors
- Cowperthwaite, B., Hains, S. M. J., & Kisilevsky, B. S.
- Affiliations
- Queen's University (CA)
- Corresponding author
- Kisilevsky, B.S.
- Venue
- Infant Behavior and Development
- Publisher
- Elsevier BV
- Published
- 2007-09
- Volume
- 30
- Issue
- 3
- Pages
- 422-430
- ISSN
- 0163-6383 (ISSN-L)
- OpenAlex
- W2024835372
- Cited by
- 33
- References
- 43
- Citations by year
- 2026: 2 · 2025: 1 · 2023: 3 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 1 · 2016: 2 · 2015: 2 · 2013: 3 · 2012: 3
- FWCI
- 1.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Infant Behavior and Development (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Infant Development and Preterm Care
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Keywords
- maternal smoking, fetal behavior, fetal heart rate, fetal movement, gestational age, preterm birth, language development
- MeSH terms
- Acoustic Stimulation, Adolescent, Adult, Analysis of Variance, Female, Fetal Movement, Fetus, Gestational Age, Heart Rate, Fetal, Humans, Pregnancy, Prenatal Exposure Delayed Effects, Respiration, Smoking, Chi-Square Distribution, Pregnant People
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