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Impact of maternal prenatal smoking on fetal to infant neurobehavioral development

Published online by Cambridge University Press:  02 August 2018

Laura R. Stroud
Affiliation:
Brown University
Meaghan McCallum
Affiliation:
Brown University
Amy L. Salisbury*
Affiliation:
Brown University
*
Address correspondence and reprint requests to: Amy Salisbury, Brown Center for the Study of Children at Risk, Women and Infants' Hospital, 101 Dudley St., Providence, RI 02905; Email: [email protected].

Abstract

Despite recent emphasis on the profound importance of the fetal environment in “programming” postnatal development, measurement of offspring development typically begins after birth. Using a novel coding strategy combining direct fetal observation via ultrasound and actocardiography, we investigated the impact of maternal smoking during pregnancy (MSDP) on fetal neurobehavior; we also investigated links between fetal and infant neurobehavior. Participants were 90 pregnant mothers and their infants (52 MSDP-exposed; 51% minorities; ages 18–40). Fetal neurobehavior at baseline and in response to vibro-acoustic stimulus was assessed via ultrasound and actocardiography at M = 35 weeks gestation and coded via the Fetal Neurobehavioral Assessment System (FENS). After delivery, the NICU Network Neurobehavioral Scale was administered up to seven times over the first postnatal month. MSDP was associated with increased fetal activity and fetal limb movements. Fetal activity, complex body movements, and cardiac–somatic coupling were associated with infants' ability to attend to stimuli and to self-regulate over the first postnatal month. Furthermore, differential associations emerged by MSDP group between fetal activity, complex body movements, quality of movement, and coupling, and infant attention and self-regulation. The present study adds to a growing literature establishing the validity of fetal neurobehavioral measures in elucidating fetal programming pathways.

Type
Special Issue Articles
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

This research was supported by the National Institutes of Health Grants R01 DA019558 and R01 DA036999 (to L.R.S.) and the Flight Attendant Medical Research Institute Clinical Innovator Award (to L.R.S.). We gratefully acknowledge the families who contributed to this study and the Maternal–Infant Studies Laboratory staff for their assistance with data collection. We are also grateful to Cheryl Boyce and Nicolette Borek, Program Officers, for their support of this work and this field.

References

Alexander, B. T., Dasinger, J. H., & Intapad, S. (2015). Fetal programming and cardiovascular pathology. Comprehensive Physiology, 5, 9971025. doi:10.1002/cphy.c140036Google Scholar
Alhusen, J. L., Gross, D., Hayat, M. J., Woods, A. B., & Sharps, P. W. (2012). The influence of maternal-fetal attachment and health practices on neonatal outcomes in low-income, urban women. Research in Nursing and Health, 35, 112120. doi:10.1002/nur.21464Google Scholar
Andonotopo, W., & Kurjak, A. (2006). The assessment of fetal behavior of growth restricted fetuses by 4D sonography. Journal of Perinatal Medicine, 34, 471478.Google Scholar
Appleton, A. A., Murphy, M. A., Koestler, D. C., Lesseur, C., Paquette, A. G., Padbury, J. F., … Marsit, C. J. (2016). Prenatal programming of infant neurobehaviour in a healthy population. Paediatric Perinatal Epidemiology, 30, 367375. doi:10.1111/ppe.12294Google Scholar
Arabin, B., & Riedewald, S. (1992). An attempt to quantify characteristics of behavioral states. American Journal of Perinatology, 9, 115119.Google Scholar
Bale, T. L. (2011). Sex differences in prenatal epigenetic programming of stress pathways. Stress, 14, 348356. doi:10.3109/10253890.2011.586447Google Scholar
Banister, C. E., Koestler, D. C., Maccani, M. A., Padbury, J. F., Houseman, E. A., & Marsit, C. J. (2011). Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas. Epigenetics, 6, 920927. doi:10.4161/epi.6.7.16079Google Scholar
Bardy, A. H., Seppala, T., Lillsunde, P., Kataja, J. M., Koskela, P., Pikkarainen, J., & Hiilesmaa, V. K. (1993). Objectively measured tobacco exposure during pregnancy: Neonatal effects and relation to maternal smoking. British Journal of Obstetrics and Gynaecology, 100, 721726.Google Scholar
Barker, D. J. (2002). Fetal programming of coronary heart disease. Trends in Endocrinology and Metabolism, 13, 364368.Google Scholar
Bertalanffy, L. v. (1968). General systems theory. New York: Brazilier.Google Scholar
Bidwell, L. C., Palmer, R. H., Brick, L., Madden, P. A., Heath, A. C., & Knopik, V. S. (2016). A propensity scoring approach to characterizing the effects of maternal smoking during pregnancy on offspring's initial responses to cigarettes and alcohol. Behavior Genetics, 46, 416430. doi:10.1007/s10519-016-9791-5Google Scholar
Bornstein, E., Monteagudo, A., Santos, R., Keeler, S. M., & Timor-Tritsch, I. E. (2010). A systematic technique using 3-dimensional ultrasound provides a simple and reproducible mode to evaluate the corpus callosum. American Journal of Obstetrics and Gynecology, 202, 201. doi:10.1016/j.ajog.2009.10.705Google Scholar
Cao-Lei, L., de Rooij, S. R., King, S., Matthews, S. G., Metz, G. A. S., Roseboom, T. J., & Szyf, M. (2017). Prenatal stress and epigenetics. Neuroscience and Biobehavioral Reviews. Advance online publication. doi:10.1016/j.neubiorev.2017.05.016Google Scholar
Clark, C. A., Espy, K. A., & Wakschlag, L. (2016). Developmental pathways from prenatal tobacco and stress exposure to behavioral disinhibition. Neurotoxicology and Teratology, 53, 6474. doi:10.1016/j.ntt.2015.11.009Google Scholar
Cowperthwaite, B., Hains, S. M., & Kisilevsky, B. S. (2007). Fetal behavior in smoking compared to non-smoking pregnant women. Infant Behavior and Development, 30, 422430. doi:10.1016/j.infbeh.2006.12.004Google Scholar
Coyle, M. G., Salisbury, A. L., Lester, B. M., Jones, H. E., Lin, H., Graf-Rohrmeister, K., & Fischer, G. (2012). Neonatal neurobehavior effects following buprenorphine versus methadone exposure. Addiction, 107(Suppl. 1), 6373. doi:10.1111/j.1360-0443.2012.04040.xGoogle Scholar
Curtin, S. C., & Matthews, T. J. (2016). Smoking prevalence and cessation before and during pregnancy: Data from the Birth Certificate, 2014. National Vital Statistics Report, 65, 114.Google Scholar
Davies, P. T., Manning, L. G., & Cicchetti, D. (2013). Tracing the cascade of children's insecurity in the interparental relationship: The role of stage-salient tasks. Child Development, 84, 297312. doi:10.1111/j.1467-8624.2012.01844.xGoogle Scholar
de Vries, J. I., Visser, G. H., & Prechtl, H. F. (1982). The emergence of fetal behaviour: I. Qualitative aspects. Early Human Development, 7, 301322.Google Scholar
de Vries, J. I., Visser, G. H., & Prechtl, H. F. (1985). The emergence of fetal behaviour: II. Quantitative aspects. Early Human Development, 12, 99120.Google Scholar
de Vries, J. I., Visser, G. H., & Prechtl, H. F. (1988). The emergence of fetal behaviour: III. Individual differences and consistencies. Early Human Development, 16, 85103.Google Scholar
Denenberg, V. H. (1980). General systems theory, brain organization, and early experiences. American Journal of Physiology, 7, R3R13.Google Scholar
Dietz, P. M., England, L. J., Shapiro-Mendoza, C. K., Tong, V. T., Farr, S. L., & Callaghan, W. M. (2010). Infant morbidity and mortality attributable to prenatal smoking in the U.S. American Journal of Preventive Medicine, 39, 4552.Google Scholar
Dietz, P. M., Homa, D., England, L. J., Burley, K., Tong, V. T., Dube, S. R., & Bernert, J. T. (2011). Estimates of nondisclosure of cigarette smoking among pregnant and nonpregnant women of reproductive age in the United States. American Journal of Epidemiology, 173, 355359. doi:10.1093/aje/kwq381Google Scholar
DiPietro, J. (2001). Fetal neurobehavioral assessment. In Zeskind, P. S. & Singer, J. E. (Eds.), Biobehavioral assessment. Amsterdam: Elsevier.Google Scholar
DiPietro, J. (2010). In the beginning. In Zimmerman, A. W. & Connors, S. L. (Eds.), Maternal influences on fetal neurodevelopment: Clinical and research aspects. London: Springer.Google Scholar
DiPietro, J. A., Bornstein, M. H., Costigan, K. A., Pressman, E. K., Hahn, C. S., Painter, K., … Yi, L. J. (2002). What does fetal movement predict about behavior during the first two years of life? Developmental Psychobiology, 40, 358371.Google Scholar
DiPietro, J. A., Costigan, K. A., Kivlighan, K. T., Chen, P., & Laudenslager, M. L. (2011). Maternal salivary cortisol differs by fetal sex during the second half of pregnancy. Psychoneuroendocrinology, 36, 588591. doi:10.1016/j.psyneuen.2010.09.005Google Scholar
DiPietro, J. A., Costigan, K. A., & Pressman, E. K. (1999). Fetal movement detection: Comparison of the Toitu actograph with ultrasound from 20 weeks gestation. Journal of Maternal–Fetal Medicine, 8, 237242. doi:10.1002/(SICI)1520-6661(199911/12)8:6<237::AID-MFM1>3.0.CO;2-F3.0.CO;2-F>Google Scholar
DiPietro, J. A., Costigan, K. A., & Pressman, E. K. (2002). Fetal state concordance predicts infant state regulation. Early Human Development, 68, 113.Google Scholar
DiPietro, J. A., Costigan, K. A., Pressman, E. K., & Doussard-Roosevelt, J. A. (2000). Antenatal origins of individual differences in heart rate. Developmental Psychobiology, 37, 221228.Google Scholar
DiPietro, J. A., Costigan, K. A., & Voegtline, K. M. (2015). Studies in fetal behavior: Revisited, renewed, and reimagined. Monographs of the Society for Research in Child Develpoment, 80(No. 3), 194. doi:10.1111/mono.v80.3Google Scholar
DiPietro, J. A., Hodgson, D. M., Costigan, K. A., Hilton, S. C., & Johnson, T. R. (1996). Development of fetal movement—Fetal heart rate coupling from 20 weeks through term. Early Human Development, 44, 139151.Google Scholar
DiPietro, J. A., Kivlighan, K. T., Costigan, K. A., Rubin, S. E., Shiffler, D. E., Henderson, J. L., & Pillion, J. P. (2010). Prenatal antecedents of newborn neurological maturation. Child Development, 81, 115130. doi:10.1111/j.1467-8624.2009.01384.xGoogle Scholar
D'Onofrio, B. M., Class, Q. A., Lahey, B. B., & Larsson, H. (2014). Testing the developmental origins of health and disease hypothesis for psychopathology using family-based quasi-experimental designs. Child Development Perspectives, 8, 151157. doi:10.1111/cdep.12078Google Scholar
D'Onofrio, B. M., Singh, A. L., Iliadou, A., Lambe, M., Hultman, C. M., Grann, M., … Lichtenstein, P. (2010). Familial confounding of the association between maternal smoking during pregnancy and offspring criminality: A population-based study in Sweden. Archives of General Psychiatry, 67, 529538. doi:10.1001/archgenpsychiatry.2010.33Google Scholar
Doyle, C., Werner, E., Feng, T., Lee, S., Altemus, M., Isler, J. R., & Monk, C. (2015). Pregnancy distress gets under fetal skin: Maternal ambulatory assessment and sex differences in prenatal development. Developmental Psychobiology, 57, 607625. doi:10.1002/dev.21317Google Scholar
Eiden, R. D., Molnar, D. S., Granger, D. A., Colder, C. R., Schuetze, P., & Huestis, M. A. (2015). Prenatal tobacco exposure and infant stress reactivity: Role of child sex and maternal behavior. Developmental Psychobiology, 57, 212225. doi:10.1002/dev.21284Google Scholar
Ellingson, J. M., Goodnight, J. A., Van Hulle, C. A., Waldman, I. D., & D'Onofrio, B. M. (2014). A sibling-comparison study of smoking during pregnancy and childhood psychological traits. Behavior Genetics, 44, 2535. doi:10.1007/s10519-013-9618-6Google Scholar
England, L. J., Aagaard, K., Bloch, M., Conway, K., Cosgrove, K., Grana, R., … Wakschlag, L. (2016). Developmental toxicity of nicotine: A transdisciplinary synthesis and implications for emerging tobacco products. Neuroscience and Biobehavioral Reviews, 72, 176189. doi:10.1016/j.neubiorev.2016.11.013Google Scholar
Espy, K. A., Fang, H., Johnson, C., Stopp, C., & Wiebe, S. A. (2011). Prenatal tobacco exposure: Developmental outcomes in the neonatal period. Developmental Psychology, 47, 153156. doi:10.1037/a0020724Google Scholar
Estabrook, R., Massey, S. H., Clark, C. A., Burns, J. L., Mustanski, B. S., Cook, E. H., … Wakschlag, L. S. (2016). Separating family-level and direct exposure effects of smoking during pregnancy on offspring externalizing symptoms: Bridging the behavior genetic and behavior teratologic divide. Behavior Genetics, 46, 389402. doi:10.1007/s10519-015-9762-2Google Scholar
Fang, H., Johnson, C., Chevalier, N., Stopp, C., Wiebe, S., Wakschlag, L. S., & Espy, K. A. (2010). Using propensity score modeling to minimize the influence of confounding risks related to prenatal tobacco exposure. Nicotine and Tobacco Research, 12, 12111219. doi:10.1093/ntr/ntq170Google Scholar
Gaysina, D., Fergusson, D. M., Leve, L. D., Horwood, J., Reiss, D., Shaw, D. S., … Harold, G. T. (2013). Maternal smoking during pregnancy and offspring conduct problems: Evidence from 3 independent genetically sensitive research designs. JAMA Psychiatry, 70, 956963. doi:10.1001/jamapsychiatry.2013.127Google Scholar
Gingras, J. L., & O'Donnell, K. J. (1998). State control in the substance-exposed fetus: I. The fetal neurobehavioral profile: An assessment of fetal state, arousal, and regulation competency. Annals of the New York Academy of Science, 846, 262276.Google Scholar
Goodman, J. D., Visser, F. G., & Dawes, G. S. (1984). Effects of maternal cigarette smoking on fetal trunk movements, fetal breathing movements and the fetal heart rate. British Journal of Obstetrics and Gynaecology, 91, 657661.Google Scholar
Gottfried, A. W. (1985). Measures of socioeconomic status in child development research: Data and recommendations. Merrill-Palmer Quarterly, 31, 8592.Google Scholar
Gottleib, G. (1991). Experiential canalization of behavioral development: Results. Developmental Psychobiology, 27, 3539.Google Scholar
Graatsma, E. M., Jacod, B. C., van Egmond, L. A., Mulder, E. J., & Visser, G. H. (2009). Fetal electrocardiography: Feasibility of long-term fetal heart rate recordings. BJOG, 116, 334338. doi:10.1111/j.1471-0528.2008.01951.xGoogle Scholar
Graca, L. M., Cardoso, C. G., Clode, N., & Calhaz-Jorge, C. (1991). Acute effects of maternal cigarette smoking on fetal heart rate and fetal body movements felt by the mother. Journal of Perinatal Medicine, 19, 385390.Google Scholar
Grant-Beuttler, M., Glynn, L. M., Salisbury, A. L., Davis, E. P., Holliday, C., & Sandman, C. A. (2011). Development of fetal movement between 26 and 36-weeks' gestation in response to vibro-acoustic stimulation. Frontiers in Psychology, 2, 350. doi:10.3389/fpsyg.2011.00350Google Scholar
Gray, T. R., LaGasse, L. L., Smith, L. M., Derauf, C., Grant, P., Shah, R., … Huestis, M. A. (2009). Identification of prenatal amphetamines exposure by maternal interview and meconium toxicology in the Infant Development, Environment and Lifestyle (IDEAL) study. Therapeutic Drug Monitoring, 31, 769775. doi:10.1097/FTD.0b013e3181bb438eGoogle Scholar
Groome, L. J., Bentz, L. S., & Singh, K. P. (1995). Behavioral state organization in normal human term fetuses: The relationship between periods of undefined state and other characteristics of state control. Sleep, 18, 7781.Google Scholar
Groome, L. J., Swiber, M. J., Holland, S. B., Bentz, L. S., Atterbury, J. L., & Trimm, R. F. III. (1999). Spontaneous motor activity in the perinatal infant before and after birth: Stability in individual differences. Developmental Psychobiology, 35, 1524.Google Scholar
Hall, B. J., Cauley, M., Burke, D. A., Kiany, A., Slotkin, T. A., & Levin, E. D. (2016). Cognitive and behavioral impairments evoked by low-level exposure to tobacco smoke components: Comparison with nicotine alone. Toxicological Sciences, 151, 236244. doi:10.1093/toxsci/kfw042Google Scholar
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry, 23, 5662.Google Scholar
Harrod, S. B., Lacy, R. T., & Morgan, A. J. (2012). Offspring of prenatal IV nicotine exposure exhibit increased sensitivity to the reinforcing effects of methamphetamine. Frontiers in Pharmacology, 3, 116. doi:10.3389/fphar.2012.00116Google Scholar
Hogg, K., Price, E. M., Hanna, C. W., & Robinson, W. P. (2012). Prenatal and perinatal environmental influences on the human fetal and placental epigenome. Clinical Pharmacology and Therapeutics, 92, 716726. doi:10.1038/clpt.2012.141Google Scholar
Huang, L., Wang, Y., Zhang, L., Zheng, Z., Zhu, T., Qu, Y., & Mu, D. (2018). Maternal smoking and attention-deficit/hyperactivity disorder in offspring: A meta-analysis. Pediatrics, 141. doi:10.1542/peds.2017-2465Google Scholar
Jarvis, M. J., Tunstall-Pedoe, H., Feyerabend, C., Vesey, C., & Saloojee, Y. (1987). Comparison of tests used to distinguish smokers from nonsmokers. American Journal of Public Health, 77, 14351438.Google Scholar
Jo, Y. H., Talmage, D. A., & Role, L. W. (2002). Nicotinic receptor-mediated effects on appetite and food intake. Journal of Neurobiology, 53, 618632. doi:10.1002/neu.10147Google Scholar
Kainer, F., Prechtl, H. F., Engele, H., & Einspieler, C. (1997). Assessment of the quality of general movements in fetuses and infants of women with type-I diabetes mellitus. Early Human Development, 50, 1325.Google Scholar
Kisilevsky, B. S., Gilmour, A., Stutzman, S. S., Hains, S. M., & Brown, C. A. (2012). Atypical fetal response to the mother's voice in diabetic compared with overweight pregnancies. Journal of Developmental and Behavioral Pediatrics, 33, 5561. doi:10.1097/DBP.0b013e31823e791eGoogle Scholar
Kisilevsky, B. S., Muir, D. W., & Low, J. A. (1990). Maturation of responses elicited by a vibroacoustic stimulus in a group of high-risk fetuses. Maternal–Child Nursing Journal, 19, 239250.Google Scholar
Kisilevsky, B. S., Muir, D. W., & Low, J. A. (1992). Maturation of human fetal responses to vibroacoustic stimulation. Child Development, 63, 14971508.Google Scholar
Kiuchi, M., Nagata, N., Ikeno, S., & Terakawa, N. (2000). The relationship between the response to external light stimulation and behavioral states in the human fetus: How it differs from vibroacoustic stimulation. Early Human Development, 58, 153165.Google Scholar
Krasnegor, N. A., Fifer, W., Maulik, D., McNellis, D., Romero, R., & Smotherman, W. (1998). Fetal behavioral development: Measurement of habituation, state transitions, and movement to assess fetal well being and to predict outcome. Journal of Maternal–Fetal Investigation, 8, 5157.Google Scholar
Kurjak, A., Stanojevic, M., Andonotopo, W., Salihagic-Kadic, A., Carrera, J. M., & Azumendi, G. (2004). Behavioral pattern continuity from prenatal to postnatal life—A study by four-dimensional (4D) ultrasonography. Journal of Perinatal Medicine, 32, 346353.Google Scholar
Kurjak, A., Tikvica, A., Stanojevic, M., Miskovic, B., Ahmed, B., Azumendi, G., & Di Renzo, G. C. (2008). The assessment of fetal neurobehavior by three-dimensional and four-dimensional ultrasound. Journal of Maternal–Fetal and Neonatal Mecine, 21, 675684. doi:10.1080/14767050802212166Google Scholar
Law, K. L., Stroud, L. R., LaGasse, L. L., Niaura, R., Liu, J., & Lester, B. M. (2003). Smoking during pregnancy and newborn neurobehavior. Pediatrics, 111(6, Pt. 1), 13181323.Google Scholar
Lecanuet, J. P., Fifer, W., Krasenegor, N. A., & Smotherman, W. P. (Eds.). (1995). Fetal development: A psychobiological perspective. Hillsdale, NJ: Erlbaum.Google Scholar
Lehtovirta, P., Forss, M., Rauramo, I., & Kariniemi, V. (1983). Acute effects of nicotine on fetal heart rate variability. British Journal of Obstetrics and Gynaecology, 90, 710715.Google Scholar
Lester, B., & Tronick, E. (2004). The Neonatal Intensive Care Unit Network Neurobehavioral Scale. Pediatrics, 113(Suppl. 3, Pt .2), 631695.Google Scholar
Lester, B. M., Bagner, D. M., Liu, J., LaGasse, L. L., Seifer, R., Bauer, C. R., … Das, A. (2009). Infant neurobehavioral dysregulation: Behavior problems in children with prenatal substance exposure. Pediatrics, 124, 13551362. doi:10.1542/peds.2008-2898Google Scholar
Lester, B. M., Conradt, E., & Marsit, C. J. (2014). Are epigenetic changes in the intrauterine environment related to newborn neurobehavior? Epigenomics, 6, 175178. doi:10.2217/epi.14.9Google Scholar
Lester, B. M., & Tronick, E. Z. (2004). History and description of the Neonatal Intensive Care Unit Network Neurobehavioral Scale. Pediatrics, 113(3, Pt. 2), 634640.Google Scholar
Lester, B. M., Tronick, E. Z., LaGasse, L., Seifer, R., Bauer, C. R., Shankaran, S., … Lu, J. (2004). Summary statistics of Neonatal Intensive Care Unit Network Neurobehavioral Scale scores from the Maternal Lifestyle Study: A quasinormative sample. Pediatrics, 113(3, Pt. 2), 668675.Google Scholar
Levin, E. D., & Slotkin, T. A. (1998). Development neurotoxicity of nicotine. In Slikker, W. & Chang, L. W. (Eds.), Handbook of development neurotoxicity (pp. 587615). New York: Academic Press.Google Scholar
Lindgren, K. (2001). Relationships among maternal-fetal attachment, prenatal depression, and health practices in pregnancy. Research in Nursing and Health, 24, 203217.Google Scholar
Liu, J., Bann, C., Lester, B., Tronick, E., Das, A., Lagasse, L., … Bada, H. (2010). Neonatal neurobehavior predicts medical and behavioral outcome. Pediatrics, 125, e90e98. doi:peds.2009-0204Google Scholar
Lumbers, E. R., Yu, Z. Y., & Crawford, E. N. (2003). Effects of fetal behavioral states on renal sympathetic nerve activity and arterial pressure of unanesthetized fetal sheep. American Journal of Physiology: Regulatory, Integrative, and Comparative Physiology, 285, R908R916.Google Scholar
Maccani, M. A., & Marsit, C. J. (2009). Epigenetics in the placenta. American Journal of Reproductive Immunology, 62, 7889. doi:10.1111/j.1600-0897.2009.00716.xGoogle Scholar
Maccari, S., Darnaudery, M., Morley-Fletcher, S., Zuena, A. R., Cinque, C., & Van Reeth, O. (2003). Prenatal stress and long-term consequences: Implications of glucocorticoid hormones. Neuroscience and Biobehavioral Reviews, 27, 119127.Google Scholar
MacDorman, M. F., Cnattingius, S., Hoffman, H. J., Kramer, M. S., & Haglund, B. (1997). Sudden infant death syndrome and smoking in the United States and Sweden. American Journal of Epidemiology, 146, 249257.Google Scholar
Macones, G. A., Hankins, G. D., Spong, C. Y., Hauth, J., & Moore, T. (2008). The 2008 National Institute of Child Health and Human Development workshop report on electronic fetal monitoring: Update on definitions, interpretation, and research guidelines. Obstetrics and Gynecology, 112, 661666. doi:10.1097/AOG.0b013e3181841395Google Scholar
Maeda, K., Tatsumura, M., & Nakajima, K. (1991). Objective and quantitative evaluation of fetal movement with ultrasonic Doppler actocardiogram. Biology of the Neonate, 60(Suppl. 1), 4151.Google Scholar
Magee, S. R., Bublitz, M. H., Orazine, C., Brush, B., Salisbury, A., Niaura, R., & Stroud, L. R. (2014). The relationship between maternal-fetal attachment and cigarette smoking over pregnancy. Maternal and Child Health Journal, 18, 10171022. doi:10.1007/s10995-013-1330-xGoogle Scholar
Manning, F. A., Platt, L. D., & Sipos, L. (1980). Antepartum fetal evaluation: Development of a fetal biophysical profile. American Journal of Obstetrics and Gynecology, 136, 787795.Google Scholar
Manning, F. A., Snijders, R., Harman, C. R., Nicolaides, K., Menticoglou, S., & Morrison, I. (1993). Fetal biophysical profile score: VI. Correlation with antepartum umbilical venous fetal pH. American Journal of Obstetrics and Gynecology, 169, 755763.Google Scholar
Martin, J. A., Hamilton, B. E., Sutton, P. D., Ventura, S. J., Menacker, F., Kirmeyer, S., … Prevention National Center for Health Statistics National Vital Statistics. (2007). Births: Final data for 2005. National Vital Statistics Report, 56, 1103.Google Scholar
Masten, A. S., & Cicchetti, D. (2010). Developmental cascades. Development and Psychopathology, 22, 491495. doi:10.1017/S0954579410000222Google Scholar
Mathews, T. J. (2001). Smoking during pregnancy in the 1990s. National Vital Statistics Report, 49, 114.Google Scholar
Meader, N., King, K., Moe-Byrne, T., Wright, K., Graham, H., Petticrew, M., … Sowden, A. J. (2016). A systematic review on the clustering and co-occurrence of multiple risk behaviours. BMC Public Health, 16, 657. doi:10.1186/s12889-016-3373-6Google Scholar
Meaney, M. J., Szyf, M., & Seckl, J. R. (2007). Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends in Molecular Medicine, 13, 269277. doi:10.1016/j.molmed.2007.05.003Google Scholar
Moisiadis, V. G., & Matthews, S. G. (2014). Glucocorticoids and fetal programming: Part 1. Outcomes. Nature Reviews Endocrinology, 10, 391402. doi:10.1038/nrendo.2014.73Google Scholar
Monteagudo, A., & Timor-Tritsch, I. E. (2009). Normal sonographic development of the central nervous system from the second trimester onwards using 2D, 3D and transvaginal sonography. Prenatal Diagnosis, 29, 326339. doi:10.1002/pd.2146Google Scholar
Nasello-Paterson, C., Natale, R., & Connors, G. (1988). Ultrasonic evaluation of fetal body movements over twenty-four hours in the human fetus at twenty-four to twenty-eight weeks' gestation. American Journal of Obstetrics and Gynecology, 158, 312316.Google Scholar
Neil, P. A., Chee-Ruiter, C., Scheier, C., Lewkowicz, D. J., & Shimojo, S. (2006). Development of multisensory spatial integration and perception in humans. Developmental Science, 9, 454464. doi:10.1111/j.1467-7687.2006.00512.xGoogle Scholar
Nijhuis, J. G. (1986). Behavioural states: Concomitants, clinical implications and the assessment of the condition of the nervous system. European Journal of Obstetrics & Gynecology and Reproductive Biology, 21, 301308.Google Scholar
Nijhuis, J. G., Martin, C. B., & Prechtl, H. F. R. (1984). Behavioural states of the human fetus. In Prechtl, H. F. R. (Ed.), Continuity of neural functions from prenatal to postnatal life. (pp. 6578). Oxford: Blackwell.Google Scholar
Nijhuis, J. G., Prechtl, H. F. R., Martin, C. B. Jr., & Bots, R. S. G. M. (1982). Are there behavioural states in the human fetus? Early Human Development, 6, 177195.Google Scholar
Noble, N., Paul, C., Turon, H., & Oldmeadow, C. (2015). Which modifiable health risk behaviours are related? A systematic review of the clustering of Smoking, Nutrition, Alcohol and Physical activity (“SNAP”) health risk factors. Preventive Medicine, 81, 1641. doi:10.1016/j.ypmed.2015.07.003Google Scholar
Novakovic, B., & Saffery, R. (2012). The ever growing complexity of placental epigenetics—Role in adverse pregnancy outcomes and fetal programming. Placenta, 33, 959970. doi:10.1016/j.placenta.2012.10.003Google Scholar
Nugent, B. M., & Bale, T. L. (2015). The omniscient placenta: Metabolic and epigenetic regulation of fetal programming. Frontiers in Neuroendocrinology, 39, 2837. doi:10.1016/j.yfrne.2015.09.001Google Scholar
Ockene, J., Ma, Y., Zapka, J., Pbert, L., Valentine Goins, K., & Stoddard, A. (2002). Spontaneous cessation of smoking and alcohol use among low-income pregnant women. American Journal of Preventive Medicine, 23, 150159.Google Scholar
Oncken, C., Kranzler, H., O'Malley, P., Gendreau, P., & Campbell, W. A. (2002). The effect of cigarette smoking on fetal heart rate characteristics. Obstetrics and Gynecology, 99(5, Pt .1), 751755.Google Scholar
Phelan, J. P. (1980). Diminished fetal reactivity with smoking. American Journal of Obstetrics and Gynecology, 136, 230233.Google Scholar
Pickett, K. E., Wilkinson, R. G., & Wakschlag, L. S. (2009). The psychosocial context of pregnancy smoking and quitting in the Millennium Cohort Study. Journal of Epidemiology and Community Health, 63, 474480. doi:10.1136/jech.2008.082594Google Scholar
Pillai, M., & James, D. (1990). Development of human fetal behavior: A review. Fetal Diagnosis and Therapy, 5, 1532.Google Scholar
Pillai, M., & James, D. (1991). Human fetal mouthing movements: A potential biophysical variable for distinguishing state 1F from abnormal fetal behavior; report of 4 cases. European Journal of Obstetrics & Gynecology and Reproductive Biology, 38, 151156.Google Scholar
Pillai, M., James, D. K., & Parker, M. (1992). The development of ultradian rhythms in the human fetus. American Journal of Obstetrics and Gynecology, 167, 172177.Google Scholar
Pirie, P. L., Lando, H., Curry, S. J., McBride, C. M., & Grothaus, L. C. (2000). Tobacco, alcohol, and caffeine use and cessation in early pregnancy. American Journal of Preventive Medicine, 18, 5461.Google Scholar
Polakowski, L. L., Akinbami, L. J., & Mendola, P. (2009). Prenatal smoking cessation and the risk of delivering preterm and small-for-gestational-age newborns. Obstetrics and Gynecology, 114(2, Pt. 1), 318325.Google Scholar
Prechtl, H. F. R. (1977). Assessment and significance of behavioural states. In Berenberg, S. R. (Ed.), Brain: Fetal and infant (pp. 7990). The Hague, Netherlands: Martinus Nijhoff.Google Scholar
Robertson, S. S., Dierker, L. J., Sorokin, Y., & Rosen, M. G. (1982). Human fetal movement: Spontaneous oscillations near one cycle per minute. Science, 218, 13271330.Google Scholar
Robinson, S. M., Sobell, L. C., Sobell, M. B., & Leo, G. I. (2014). Reliability of the Timeline Followback for cocaine, cannabis, and cigarette use. Psychology of Addictive Behaviors, 28, 154162. doi:10.1037/a0030992Google Scholar
Rosenfeld, C. S. (2015). Sex-specific placental responses in fetal development. Endocrinology, 156, 34223434. doi:10.1210/en.2015-1227Google Scholar
Ruisch, I. H., Dietrich, A., Glennon, J. C., Buitelaar, J. K., & Hoekstra, P. J. (2018). Maternal substance use during pregnancy and offspring conduct problems: A meta-analysis. Neuroscience and Biobehaval Reviews, 84, 325336. doi:10.1016/j.neubiorev.2017.08.014Google Scholar
Salisbury, A. L. (2010). Before infant assessment: Fetal neurobehavior. In Lester, B. M. & Sparrow, J. D. (Eds.), Nurturing children and families: Building on the legacy of T. Berry Brazelton (pp. 2939). West Sussex, UK: Wiley.Google Scholar
Salisbury, A. L., Fallone, M. D., & Lester, B. (2005). Neurobehavioral assessment from fetus to infant: The NICU Network Neurobehavioral Scale and the Fetal Neurobehavior Coding Scale. Mental Retardation and Developmental Disabilities Research Reviews, 11, 1420. doi:10.1002/mrdd.20058Google Scholar
Salisbury, A. L., Ponder, K. L., Padbury, J. F., & Lester, B. M. (2009). Fetal effects of psychoactive drugs. Clinical Perinatology, 36, 595619. doi:10.1016/j.clp.2009.06.002Google Scholar
Sandman, C. A., Glynn, L. M., & Davis, E. P. (2013). Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. Journal of Psychosomatic Research, 75, 327335. doi:10.1016/j.jpsychores.2013.07.009Google Scholar
Schuetze, P., Lopez, F. A., Granger, D. A., & Eiden, R. D. (2008). The association between prenatal exposure to cigarettes and cortisol reactivity and regulation in 7-month-old infants. Developmental Psychobiology, 50, 819834. doi:10.1002/dev.20334Google Scholar
Seckl, J. R. (1998). Physiologic programming of the fetus. Clinical Perinatology, 25, 939962.Google Scholar
Shenassa, E. D., Papandonatos, G. D., Rogers, M. L., & Buka, S. L. (2015). Elevated risk of nicotine dependence among sib-pairs discordant for maternal smoking during pregnancy: Evidence from a 40-year longitudinal study. Epidemiology, 26, 441447. doi:10.1097/EDE.0000000000000270Google Scholar
Shults, J., Sun, W., Tu, X., Kim, H., Amsterdam, J., Hilbe, J. M., & Ten-Have, T. (2009). A comparison of several approaches for choosing between working correlation structures in generalized estimating equation analysis of longitudinal binary data. Statistics in Medicine, 28, 23382355. doi:10.1002/sim.3622Google Scholar
Skoglund, C., Chen, Q., D'Onofrio, B. M., Lichtenstein, P., & Larsson, H. (2014). Familial confounding of the association between maternal smoking during pregnancy and ADHD in offspring. Journal of Child Psychology and Psychiatry, 55, 6168. doi:10.1111/jcpp.12124Google Scholar
Slotkin, T. A. (1998). Fetal nicotine or cocaine exposure: Which one is worse? Journal of Pharmacology and Experimental Therapeutics, 285, 931945.Google Scholar
Slotkin, T. A. (2004). Cholinergic systems in brain development and disruption by neurotoxicants: Nicotine, environmental tobacco smoke, organophosphates. Toxicology and Applied Pharmacology, 198, 132151. doi:10.1016/j.taap.2003.06.001Google Scholar
Slotkin, T. A., Southard, M. C., Adam, S. J., Cousins, M. M., & Seidler, F. J. (2004). Alpha7 nicotinic acetylcholine receptors targeted by cholinergic developmental neurotoxicants: Nicotine and chlorpyrifos. Brain Research Bulletin, 64, 227235. doi:10.1016/j.brainresbull.2004.07.005Google Scholar
Slotkin, T. A., Tate, C. A., Cousins, M. M., & Seidler, F. J. (2002). Functional alterations in CNS catecholamine systems in adolescence and adulthood after neonatal chlorpyrifos exposure. Brain Res: Developmental Brain Research, 133, 163173.Google Scholar
Smith, C. V. (1994). Vibroacoustic stimulation for risk assessment. Clinical Perinatology, 21, 797808.Google Scholar
Smith, C. V., Phelan, J. P., Broussard, P., & Paul, R. H. (1988). Fetal acoustic stimulation testing: III. Predictive value of a reactive test. Journal of Reproductive Medicine, 33, 217218.Google Scholar
Stojakovic, A., Espinosa, E. P., Farhad, O. T., & Lutfy, K. (2017). Effects of nicotine on homeostatic and hedonic components of food intake. Journal of Endocrinology, 235, R13R31. doi:10.1530/JOE-17-0166Google Scholar
Stroud, L. R., Papandonatos, G. D., Parade, S. H., Salisbury, A. L., Phipps, M. G., Lester, B. M., … Marsit, C. J. (2016). Prenatal major depressive disorder, placenta glucocorticoid and serotonergic signaling, and infant cortisol response. Psychosomatic Medicine, 78, 979990. doi:10.1097/PSY.0000000000000410Google Scholar
Stroud, L. R., Papandonatos, G. D., Rodriguez, D., McCallum, M., Salisbury, A. L., Phipps, M. G., … Marsit, C. J. (2014). Maternal smoking during pregnancy and infant stress response: Test of a prenatal programming hypothesis. Psychoneuroendocrinology, 48, 2940. doi:10.1016/j.psyneuen.2014.05.017Google Scholar
Stroud, L. R., Papandonatos, G. D., Salisbury, A. L., Phipps, M. G., Huestis, M. A., Niaura, R., … Lester, B. M. (2016). Epigenetic regulation of placental NR3C1: Mechanism underlying prenatal programming of infant neurobehavior by maternal smoking? Child Development, 87, 4960. doi:10.1111/cdev.12482Google Scholar
Stroud, L. R., Papandonatos, G. D., Shenassa, E., Rodriguez, D., Niaura, R., LeWinn, K. Z., … Buka, S. L. (2014). Prenatal glucocorticoids and maternal smoking during pregnancy independently program adult nicotine dependence in daughters: A 40-year prospective study. Biological Psychiatry, 75, 4755. doi:10.1016/j.biopsych.2013.07.024Google Scholar
Stroud, L. R., Paster, R. L., Goodwin, M. S., Shenassa, E., Buka, S., Niaura, R., … Lipsitt, L. P. (2009). Maternal smoking during pregnancy and neonatal behavior: A large-scale community study. Pediatrics, 123, e842e848. doi:10.1542/peds.2008-2084Google Scholar
Stroud, L. R., Paster, R. L., Papandonatos, G. D., Niaura, R., Salisbury, A. L., Battle, C., … Lester, B. (2009). Maternal smoking during pregnancy and newborn neurobehavior: Effects at 10 to 27 days. Journal of Pediatrics, 154, 1016. doi:10.1016/j.jpeds.2008.07.048Google Scholar
Thaler, I., Goodman, J. D., & Dawes, G. S. (1980). Effects of maternal cigarette smoking on fetal breathing and fetal movements. American Journal of Obstetrics and Gynecology, 138, 282287.Google Scholar
Timor-Tritsch, I. E., & Monteagudo, A. (2007). Three and four-dimensional ultrasound in obstetrics and gynecology. Current Opinion in Obstetrics and Gynecology, 19, 157175. doi:10.1097/GCO.0b013e328099b06700001703-200704000-00011Google Scholar
Tong, V. T., Althabe, F., Aleman, A., Johnson, C. C., Dietz, P. M., Berrueta, M., … Belizan, J. M. (2015). Accuracy of self-reported smoking cessation during pregnancy. Acta Obstetricia Gynecolica Scandinavica, 94, 106111. doi:10.1111/aogs.12532Google Scholar
Tong, V. T., Dietz, P. M., Morrow, B., D'Angelo, D. V., Farr, S. L., Rockhill, K. M., … Centers for Disease Control and Prevention. (2013). Trends in smoking before, during, and after pregnancy—Pregnancy Risk Assessment Monitoring System, United States, 40 sites, 2000–2010. Mortality and Morbidity Weekly Report Surveillance Summaries, 62, 119.Google Scholar
US Department of Health and Human Services. (2014). The health consequences of smoking: 50 years of progress. A report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health.Google Scholar
US Department of Health and Human Services. (2016). E-cigarette use among youth and young adults. A report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health.Google Scholar
Villanti, A. C., Cobb, C. O., Cohn, A. M., Williams, V. F., & Rath, J. M. (2015). Correlates of hookah use and predictors of hookah trial in U.S. young adults. American Journal of Preventive Medicine, 48, 742746. doi:10.1016/j.amepre.2015.01.010Google Scholar
Wakschlag, L. S., Leventhal, B. L., Pine, D. S., Pickett, K. E., & Carter, A. S. (2006). Elucidating early mechanisms of developmental psychopathology: The case of prenatal smoking and disruptive behavior. Child Development, 77, 893906.Google Scholar
Wakschlag, L. S., Pickett, K. E., Cook, E. Jr., Benowitz, N. L., & Leventhal, B. L. (2002). Maternal smoking during pregnancy and severe antisocial behavior in offspring: A review. American Journal of Public Health, 92, 966974.Google Scholar
Xiong, F., & Zhang, L. (2013). Role of the hypothalamic-pituitary-adrenal axis in developmental programming of health and disease. Frontiers in Neuroendocrinology, 34, 2746. doi:10.1016/j.yfrne.2012.11.002Google Scholar
Yolton, K., Khoury, J., Xu, Y., Succop, P., Lanphear, B., Bernert, J. T., & Lester, B. (2009). Low-level prenatal exposure to nicotine and infant neurobehavior. Neurotoxicology and Teratology, 31, 356363. doi:10.1016/j.ntt.2009.07.004Google Scholar
Zeger, S. L., & Liang, K. Y. (1986). Longitudinal data analysis for discrete and continuous outcomes. Biometrics, 42, 121130.Google Scholar
Zeskind, P. S., & Gingras, J. L. (2006). Maternal cigarette-smoking during pregnancy disrupts rhythms in fetal heart rate. Journal of Pediatric Psychology, 31, 514.Google Scholar
Zimmerman, M., Martinez, J. H., Young, D., Chelminski, I., & Dalrymple, K. (2013). Severity classification on the Hamilton Depression Rating Scale. Journal of Affective Disorders, 150, 384388. doi:10.1016/j.jad.2013.04.028Google Scholar