Maternal cigarette-smoking during pregnancy disrupts rhythms in fetal heart rate.

OBJECTIVE To examine the effects of maternal cigarette smoking during pregnancy on the developing infant's autonomic regulation before the possible effects of parturition and neonatal withdrawal could alter outcome measures. METHODS Heart rate variability (HRV) was assessed for 10 min during late gestation for 21 cigarette-exposed (CE) and 22 nonexposed (NE) fetuses. RESULTS HRV was significantly lower in fetuses whose mothers smoked cigarettes during pregnancy. Spectrum analysis of that variability showed temporally organized rhythms at a frequency similar to rhythms previously found in fetal cyclic motility (approximately .3 cycles per min). Lower powered rhythms--associated with poorer development--at the first, second, and dominant rhythms, as well as lower overall power of the power spectrum, were found for CE fetuses. Pearson correlations showed significant negative correlations between the amount of maternal cigarette smoking during the first trimester of pregnancy and measures of fetal HRV and power of spectral peaks. CONCLUSIONS Results show that CE fetuses have lower HRV and disrupted temporal organization of autonomic regulation before effects of parturition, postnatal adaptation, and possible nicotine withdrawal contributes to differences in infant neurobehavioral function.

[1]  R. Vertes.  Brainstem control of the events of rem sleep , 1984, Progress in Neurobiology.

[2]  Davenport Hooker,et al.  The prenatal origin of behavior , 1952 .

[3]  P. S. Zeskind,et al.  Rhythmic organization of neonatal heart rate and its relation to atypical fetal growth. , 1991, Developmental psychobiology.

[4]  P. S. Zeskind,et al.  Rhythmic organization of heart rate in breast‐fed and bottle‐fed newborn infants , 1992 .

[5]  S. Robertson.  Intrinsic temporal patterning in the spontaneous movement of awake neonates. , 1982, Child development.

[6]  Stephen W. Porges,et al.  Heart rate patterns in neonates: A potential diagnostic window to the brain , 1982 .

[7]  C. Dulberg,et al.  Neonatal Neurological Status in a Low‐Risk Population after Prenatal Exposure to Cigarettes, Marijuana, and Alcohol , 1987, Journal of developmental and behavioral pediatrics : JDBP.

[8]  Jing Liu,et al.  Smoking during pregnancy and newborn neurobehavior. , 2003, Pediatrics.

[9]  J. Golding.  Sudden infant death syndrome and parental smoking--a literature review. , 1997, Paediatric and perinatal epidemiology.

[10]  T. Slotkin.  Fetal nicotine or cocaine exposure: which one is worse? , 1998, The Journal of pharmacology and experimental therapeutics.

[11]  E. Rosenthal,et al.  Prolongation of the QT interval and the sudden infant death syndrome. , 1998, The New England journal of medicine.

[12]  G. Visser,et al.  Delayed emergence of fetal behaviour in type-1 diabetic women. , 1985, Early human development.

[13]  C. Calhaz-Jorge,et al.  Acute effects of maternal cigarette smoking on fetal heart rate and fetal body movements felt by the mother , 1991, Journal of perinatal medicine.

[14]  E Thelen,et al.  Spontaneous kicking in month-old infants: manifestation of a human central locomotor program. , 1981, Behavioral and neural biology.

[15]  G. Fox,et al.  AUTONOMIC DYSFUNCTION AT DIFFERENT AMBIENT TEMPERATURES IN INFANTS AT RISK OF SUDDEN INFANT DEATH SYNDROME , 1989, The Lancet.

[16]  E. Mitchell,et al.  Smoking and the Sudden Infant Death Syndrome , 2006, Reviews on Environmental Health.

[17]  Mathews Tj,et al.  Smoking during pregnancy in the 1990s. , 2001 .

[18]  T. Matthews.  The autonomic nervous system--a role in sudden infant death syndrome. , 1992, Archives of disease in childhood.

[19]  P. Fried,et al.  Neonatal behavioural correlates of prenatal exposure to marihuana, cigarettes and alcohol in a low risk population. , 1987, Neurotoxicology and teratology.

[20]  H. Kranzler,et al.  The Effect of Cigarette Smoking on Fetal Heart Rate Characteristics , 2002, Obstetrics and gynecology.

[21]  J. Jacobson,et al.  Neonatal correlates of prenatal exposure to smoking, caffeine, and alcohol*** , 1984 .

[22]  G. Visser,et al.  Abnormal motor behaviour in anencephalic fetuses. , 1985, Early human development.

[23]  H Nau,et al.  Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. , 1985, Developmental pharmacology and therapeutics.

[24]  K. Clark,et al.  The maternal and fetal physiologic effects of nicotine. , 1996, Seminars in perinatology.

[25]  Stephen W. Porges,et al.  Research methods for measurement of heart rate and respiration , 1992, Biological Psychology.

[26]  T. J. Mathews.  Smoking during pregnancy in the 1990s. , 2001, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[27]  K. Suzuki,et al.  Effect of nicotine upon uterine blood flow in the pregnant rhesus monkey. , 1980, American journal of obstetrics and gynecology.

[28]  B. Richardson,et al.  Patterns of gross fetal body movements over 24-hour observation intervals during the last 10 weeks of pregnancy. , 1982, American journal of obstetrics and gynecology.

[29]  L. Longo.  The biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant. , 1977, American journal of obstetrics and gynecology.

[30]  P. S. Zeskind,et al.  Relation Between Maternal Cigarette Smoking During Pregnancy and Behavioral and Physiological Measures of Autonomic Regulation in Neonates. , 2001, Infancy : the official journal of the International Society on Infant Studies.

[31]  J. Cacioppo,et al.  Perspectives in cardiovascular psychophysiology , 1982 .

[32]  L. Allen,et al.  Pregnancy outcome in North American women. II. Effects of diet, cigarette smoking, stress, and weight gain on placentas, and on neonatal physical and behavioral characteristics. , 1982, The American journal of clinical nutrition.

[33]  S. Robertson.  Human cyclic motility: fetal-newborn continuities and newborn state differences. , 1987, Developmental psychobiology.

[34]  C. Sullivan,et al.  Altered autonomic function and reduced arousability in apparent life-threatening event infants with obstructive sleep apnea. , 2002, American journal of respiratory and critical care medicine.

[35]  S. Robertson,et al.  Cyclic motor activity in the human fetus after midgestation. , 1985, Developmental psychobiology.

[36]  H. Junge,et al.  Behavioral states in the fetus near term , 1981, Journal of perinatal medicine.

[37]  J. Behren,et al.  Exposure to environmental and mainstream tobacco smoke and risk of spontaneous abortion. , 1999, American journal of epidemiology.

[38]  B. Lester,et al.  The effects of maternal alcohol consumption and cigarette smoking during pregnancy on acoustic cry analysis. , 1996, Child development.

[39]  A Garfinkel,et al.  Dynamic Analysis of Cardiac R-R Intervals in Normal Infants and in Infants Who Subsequently Succumbed to the Sudden Infant Death Syndrome , 1992, Pediatric Research.

[40]  S. Robertson,et al.  The development of cyclic motility in fetuses of diabetic mothers. , 1986, Developmental psychobiology.

[41]  R. Harper.  Sudden Infant Death Syndrome: A Failure of Compensatory Cerebellar Mechanisms? , 2000, Pediatric Research.

[42]  H. Hoffman,et al.  Sudden infant death syndrome and smoking in the United States and Sweden. , 1997, American journal of epidemiology.

[43]  Stephen W. Porges,et al.  Heart rate variability: An index of attentional responsivity in human newborns. , 1973 .

[44]  P. S. Zeskind,et al.  Cry threshold predicts regulatory disorder in newborn infants. , 1996, Journal of pediatric psychology.

[45]  K. Lewis,et al.  Deficient hypoxia awakening response in infants of smoking mothers: possible relationship to sudden infant death syndrome. , 1995, The Journal of pediatrics.

[46]  D. G. Watts,et al.  Spectral analysis and its applications , 1968 .

[47]  C. Henderson,et al.  Intellectual impairment in children of women who smoke cigarettes during pregnancy. , 1994, Pediatrics.

[48]  C. A. Mercer.  Spectral analysis and its applications 1969: G. M. Jenkins and D. G. Watts. San Francisco: Holden-Day, 525 pages. $20.00 , 1971 .