Abstract
Objective
Tobacco smoke exposure increases the risk of premature birth and of dying of sudden infant death syndrome (SIDS). Prematurity significantly increases the risk of dying of SIDS, but mechanisms underlying this epidemiological finding are unclear. The cumulated effect of both prematurity and prenatal exposure to nicotine on autonomic heart rate control has not been studied.
Methods
Using coarse-graining spectral analysis, we compared heart rate variability (HRV) indices of preterm newborns at 33–34 weeks post-conceptional age from smoking (n = 19) and non-smoking (n = 21) mothers. Assessment of tobacco exposure relied on maternal reports and newborns cotinine analysis. We observed how indicators of HRV depended on gestational age at birth.
Results
At 33–34 weeks postconceptional age, the newborns from smoking mothers had lower HRV low frequency power normalised to the total spectral power (LF/TP) than the control group (median values: 8% vs. 15% respectively, p < 0.02). In the non-smoking group, RR-interval values and total HRV power were correlated with gestational age at birth, with a shorter RR and a lower total HRV power in lesser gestational ages (ρ = 0.67, p = 0.03, ρ = 0.71, p = 0.003 respectively). This correlation was not observed for RR values in the group with smoking mothers.
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Abbreviations
- GA:
-
Gestational age at birth
- PCA:
-
Postconceptional age
- HRV:
-
Heart rate variability
- LF:
-
Low frequency band of HRV (0–0.2 Hz)
- HF:
-
High frequency band of HRV (0.2–2 Hz)
- TP:
-
Total spectral power of HRV
- HF/TP:
-
HF power normalised to the total spectral power
- LF/TP:
-
LF power normalised to the total spectral power
- SIDS:
-
Sudden infant death syndrome
References
Browne CA, Colditz PB, Dunster KR (2000) Infant autonomic function is altered by maternal smoking during pregnancy. Early Hum Dev 59:209–218
Bruckert E, Jacob N, Lamaire L, Truffert J, Percheron F, de Gennes JL (1992) Relationship between smoking status and serum lipids in a hyperlipidemic population and analysis of possible confounding factors. Clin Chem 38:1698–1705
Bureau MA, Shapcott D, Berthiaume Y, Monette J, Blouin D, Blanchard P, Begin R (1983) Maternal cigarette smoking and fetal oxygen transport: a study of P50, 2, 3-diphosphoglycerate, total hemoglobin, hematocrit, and type F hemoglobin in fetal blood. Pediatrics 72:22–26
Burguet A, Kaminski M, Truffert P, Menget A, Marpeau L, Voyer M, Roze JC, Escande B, Cambonie G, Hascoet JM, Grandjean H, Breart G, Larroque B (2005) Does smoking in pregnancy modify the impact of antenatal steroids on neonatal respiratory distress syndrome? Results of the Epipage study. Arch Dis Child Fetal Neonatal Ed 90:F41–F45
Buttigieg J, Brown S, Zhang M, Lowe M, Holloway AC, Nurse CA (2008) Chronic nicotine in utero selectively suppresses hypoxic sensitivity in neonatal rat adrenal chromaffin cells. FASEB J 22:1317–1326
Cohen G, Roux JC, Grailhe R, Malcolm G, Changeux JP, Lagercrantz H (2005) Perinatal exposure to nicotine causes deficits associated with a loss of nicotinic receptor function. Proc Natl Acad Sci USA 102:3817–3821
Dempsey D, Jacob P 3rd, Benowitz NL (2000) Nicotine metabolism and elimination kinetics in newborns. Clin Pharmacol Ther 67:458–465
Eiselt M, Curzi-Dascalova L, Clairambault J, Kauffmann F, Medigue C, Peirano P (1993) Heart-rate variability in low-risk prematurely born infants reaching normal term: a comparison with full-term newborns. Early Hum Dev 32:183–195
Fortrat JO (2002) Inaccurate normal values of heart rate variability spectral analysis in newborn infants. The American journal of cardiology 90:346
Fox NA (1983) Maturation of autonomic control in preterm infants. Dev Psychobiol 16:495–504
Franco P, Chabanski S, Szliwowski H, Dramaix M, Kahn A (2000) Influence of maternal smoking on autonomic nervous system in healthy infants. Pediatr Res 47:215–220
Franco P, Szliwowski H, Dramaix M, Kahn A (1998) Polysomnographic study of the autonomic nervous system in potential victims of sudden infant death syndrome. Clin Auton Res 8:243–249
Grenhoff J, Svensson TH (1989) Pharmacology of nicotine. British journal of addiction 84:477–492
Hafstrom O, Milerad J, Sandberg KL, Sundell HW (2005) Cardiorespiratory effects of nicotine exposure during development. Respiratory physiology & neurobiology 149:325–341
Huang ZG, Wang X, Dergacheva O, Mendelowitz D (2005) Prenatal nicotine exposure recruits an excitatory pathway to brainstem parasympathetic cardioinhibitory neurons during hypoxia/hypercapnia in the rat: implications for sudden infant death syndrome. Pediatr Res 58:562–567
Jarvis MJ, Russell MA, Benowitz NL, Feyerabend C (1988) Elimination of cotinine from body fluids: implications for noninvasive measurement of tobacco smoke exposure. Am J Public Health 78:696–698
Johansson S, Norman M, Legnevall L, Dalmaz Y, Lagercrantz H, Vanpee M (2007) Increased catecholamines and heart rate in children with low birth weight: perinatal contributions to sympathoadrenal overactivity. J Intern Med 261:480–487
Kahn A, Sawaguchi T, Sawaguchi A, Groswasser J, Franco P, Scaillet S, Kelmanson I, Dan B (2002) Sudden infant deaths: from epidemiology to physiology. Forensic Sci Int 130(Suppl):S8–S20
Kinney HC, O’Donnell TJ, Kriger P, White WF (1993) Early developmental changes in [3H]nicotine binding in the human brainstem. Neuroscience 55:1127–1138
Lain KY, Powers RW, Krohn MA, Ness RB, Crombleholme WR, Roberts JM (1999) Urinary cotinine concentration confirms the reduced risk of preeclampsia with tobacco exposure. Am J Obstet Gynecol 181:1192–1196
Lambers DS, Clark KE (1996) The maternal and fetal physiologic effects of nicotine. Semin Perinatol 20:115–126
Leach CE, Blair PS, Fleming PJ, Smith IJ, Platt MW, Berry PJ, Golding J (1999) Epidemiology of SIDS and explained sudden infant deaths. CESDI SUDI Research Group. Pediatrics 104:e43
Lindqvist R, Lendahls L, Tollbom O, Aberg H, Hakansson A (2002) Smoking during pregnancy: comparison of self-reports and cotinine levels in 496 women. Acta Obstet Gynecol Scand 81:240–244
Milerad J, Sundell H (1993) Nicotine exposure and the risk of SIDS. Acta Paediatr Suppl 82(Suppl 389):70–72
Neff RA, Simmens SJ, Evans C, Mendelowitz D (2004) Prenatal nicotine exposure alters central cardiorespiratory responses to hypoxia in rats: implications for sudden infant death syndrome. J Neurosci 24:9261–9268
Oncken CA, Henry KM, Campbell WA, Kuhn CM, Slotkin TA, Kranzler HR (2003) Effect of maternal smoking on fetal catecholamine concentrations at birth. Pediatr Res 53:119–124
Patural H, Barthelemy JC, Pichot V, Mazzocchi C, Teyssier G, Damon G, Roche F (2004) Birth prematurity determines prolonged autonomic nervous system immaturity. Clin Auton Res 14:391–395
Peacock JL, Bland JM, Anderson HR, Brooke OG (1991) Cigarette smoking and birthweight: type of cigarette smoked and a possible threshold effect. Int J Epidemiol 20:405–412
Prechtl H, Beintema D (1964) The Neurological Examination of the Full-Term Newborn Infant. A manual for clinical use from the Department of Experimental Neurology, University of Groningen. Spastics Society Medical Education and Information Unit in association with William Heinemann Medical Books, London, p 72
Rosenstock EG, Cassuto Y, Zmora E (1999) Heart rate variability in the neonate and infant: analytical methods, physiological and clinical observations. Acta Paediatr 88:477–482
Schechtman VL, Raetz SL, Harper RK, Garfinkel A, Wilson AJ, Southall DP, Harper RM (1992) Dynamic analysis of cardiac R-R intervals in normal infants and in infants who subsequently succumbed to the sudden infant death syndrome. Pediatr Res 31:606–612
Schellscheidt J, Oyen N, Jorch G (1997) Interactions between maternal smoking and other prenatal risk factors for sudden infant death syndrome (SIDS). Acta Paediatr 86:857–863
Slotkin TA, Saleh JL, McCook EC, Seidler FJ (1997) Impaired cardiac function during postnatal hypoxia in rats exposed to nicotine prenatally: implications for perinatal morbidity and mortality, and for sudden infant death syndrome. Teratology 55:177–184
Sovik S, Lossius K, Walloe L (2001) Heart rate response to transient chemoreceptor stimulation in term infants is modified by exposure to maternal smoking. Pediatr Res 49:558–565
Task Force of the European Society of Cardiology, the North American Society of Pacing, Electrophysiology (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use European heart journal 17:354–381
Wisborg K, Kesmodel U, Henriksen TB, Olsen SF, Secher NJ (2000) A prospective study of smoking during pregnancy and SIDS. Arch Dis Child 83:203–206
Wong T, Wickstrom R, Holgert H (2003) Chronic prenatal nicotine exposure alters enkephalin mRNA regulation in the perinatal rat adrenal medulla. Pediatr Res 53:814–816
Yamamoto Y, Hughson RL (1991) Coarse-graining spectral analysis: new method for studying heart rate variability. J Appl Physiol 71:1143–1150
Yamamoto Y, Hughson RL, Peterson JC (1991) Autonomic control of heart rate during exercise studied by heart rate variability spectral analysis. J Appl Physiol 71:1136–1142
Acknowledgments
We would like to thank Sylvie Cappelle for technical assistance.
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No financial assistance was received in support of the study. Nothing to disclose.
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Thiriez, G., Bouhaddi, M., Mourot, L. et al. Heart rate variability in preterm infants and maternal smoking during pregnancy. Clin Auton Res 19, 149–156 (2009). https://doi.org/10.1007/s10286-009-0003-8
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DOI: https://doi.org/10.1007/s10286-009-0003-8