Respiratory dysfunctions induced by prenatal nicotine exposure

Clinical and Experimental Pharmacology and Physiology

Volumn 36, Issue 12, 2009, Pages 1205-1217

  Campos, Marlys ^a   Bravo, Eduardo ^a   Eugenín, Jaime ^a  

^a UNIVERSIDAD DE SANTIAGO DE CHILE   (Chile)

Author keywords

Acetylcholine; Chemosensitivity; Nicotine; Noradrenaline; Respiratory control; Serotonin; Sudden death; Sudden infant death syndrome (SIDS)

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; CARBON DIOXIDE; DOPAMINE; GLUTAMIC ACID; GLYCINE; MUSCARINIC RECEPTOR; NICOTINE; NICOTINIC RECEPTOR; NORADRENALIN; SEROTONIN;

BREATHING; BREATHING RATE; CAROTID BODY; CHEMORECEPTOR REFLEX; CHOLINERGIC TRANSMISSION; ENVIRONMENTAL EXPOSURE; HUMAN; INFANT; NERVE CELL NETWORK; NONHUMAN; OXYGEN SENSING; PATHOGENESIS; PERINATAL PERIOD; PRENATAL EXPOSURE; RESPIRATORY FAILURE; REVIEW; SUDDEN INFANT DEATH SYNDROME; TIDAL VOLUME;

ANIMALS; BRAIN; FEMALE; HUMANS; INFANT; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; NICOTINE; PREGNANCY; RESPIRATORY SYSTEM; SMOKING; SUDDEN INFANT DEATH;

EID: 72149123225     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2009.05214.x     Document Type: Review

References (144)

1. Ward C, Lewis S, Coleman T. Prevalence of maternal smoking and environmental tobacco smoke exposure during pregnancy and impact on birth weight: Retrospective study using Millennium Cohort. BMC Public Health 2007 7 : 81.
2. Mitchell EA, Milerad J. Smoking and the sudden infant death syndrome. Rev. Environ. Health 2006 21 : 81 103.
3. Nattie E, Kinney H. Nicotine, serotonin, and sudden infant death syndrome. Am. J. Respir. Crit. Care Med. 2002 166 : 1530 1531.
4. Rose JE. Nicotine and nonnicotine factors in cigarette addiction. Psychopharmacology 2006 184 : 274 285.
5. Slotkin TA. Fetal nicotine or cocaine exposure: Which one is worse? J. Pharmacol. Exp. Ther. 1998 285 : 931 945.
6. Houdi AA, Dowell RT, Diana JN. Cardiovascular responses to cigarette smoke exposure in restrained conscious rats. J. Pharmacol. Exp. Ther. 1995 275 : 646 653.
7. Suemaru K, Oishi R, Gomita Y, Saeki K, Araki Y. Effect of long-term cigarette smoke exposure on locomotor activity and brain monoamine levels in rats. Pharmacol. Biochem. Behav. 1992 41 : 655 658.
8. Chow JY, Ma L, Zhu M, Cho CH. The potentiating actions of cigarette smoking on ethanol-induced gastric mucosal damage in rats. Gastroenterology 1997 113 : 1188 1197.
9. Benowitz NL, Jacob 3rd P. Daily intake of nicotine during cigarette smoking. Clin. Pharmacol. Ther. 1984 35 : 499 504.
10. Benowitz NL, Hansson A, Jacob 3rd P. Cardiovascular effects of nasal and transdermal nicotine and cigarette smoking. Hypertension 2002 39 : 1107 1112.
11. Luck W, Nau H, Hansen R, Steldinger R. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev. Pharmacol. Ther. 1985 8 : 384 395.
12. Slotkin TA. Cholinergic systems in brain development and disruption by neurotoxicants: Nicotine, environmental tobacco smoke, organophosphates. Toxicol. Appl. Pharmacol. 2004 198 : 132 151.
13. Slotkin TA, Pinkerton KE, Auman JT, Qiao D, Seidler FJ. Perinatal exposure to environmental tobacco smoke upregulates nicotinic cholinergic receptors in monkey brain. Brain Res. 2002 133 : 175 179.
14. van de Kamp JL, Collins AC. Prenatal nicotine alters nicotinic receptor development in the mouse brain. Pharmacol. Biochem. Behav. 1994 47 : 889 900.
15. Pauly JR, Marks MJ, Gross SD, Collins AC. An autoradiographic analysis of cholinergic receptors in mouse brain after chronic nicotine treatment. J. Pharmacol. Exp. Ther. 1991 258 : 1127 1136.
16. Petersen DR, Norris KJ, Thompson JA. A comparative study of the disposition of nicotine and its metabolites in three inbred strains of mice. Drug Metab. Dispos. Biol. Fate Chem. 1984 12 : 725 731.
17. Plowchalk DR, Andersen ME, deBethizy JD. A physiologically based pharmacokinetic model for nicotine disposition in the Sprague-Dawley rat. Toxicol. Appl. Pharmacol. 1992 116 : 177 188.
18. Benowitz NL, Jacob 3rd P. Nicotine and cotinine elimination pharmacokinetics in smokers and nonsmokers. Clin. Pharmacol. Ther. 1993 53 : 316 323.
19. Robinson DM, Peebles KC, Kwok H et al. Prenatal nicotine exposure increases apnoea and reduces nicotinic potentiation of hypoglossal inspiratory output in mice. J. Physiol. 2002 538 : 957 973.
20. Eugenin J, Otarola M, Bravo E et al. Prenatal to early postnatal nicotine exposure impairs central chemoreception and modifies breathing pattern in mouse neonates: A probable link to sudden infant death syndrome. J. Neurosci. 2008 28 : 13 907 17.
21. Monheit AG, Van Vunakis H, Key TC, Resnik R. Maternal and fetal cardiovascular effects of nicotine infusion in pregnant sheep. Am. J. Obstet. Gynecol. 1983 145 : 290 296. (Pubitemid 13188302)
22. Fregosi RF, Pilarski JQ. Prenatal nicotine exposure and development of nicotinic and fast amino acid-mediated neurotransmission in the control of breathing. Respir. Physiol. Neurobiol. 2008 164 : 80 6.
23. Hafstrom O, Milerad J, Sandberg KL, Sundell HW. Cardiorespiratory effects of nicotine exposure during development. Respir. Physiol. Neurobiol. 2005 149 : 325 341.
24. Huang YH, Brown AR, Costy-Bennett S, Luo Z, Fregosi RF. Influence of prenatal nicotine exposure on postnatal development of breathing pattern. Respir. Physiol. Neurobiol. 2004 143 : 1 8.
25. St John WM, Leiter JC. Maternal nicotine depresses eupneic ventilation of neonatal rats. Neurosci. Lett. 1999 267 : 206 208.
26. Bamford OS, Schuen JN, Carroll JL. Effect of nicotine exposure on postnatal ventilatory responses to hypoxia and hypercapnia. Respir. Physiol. 1996 106 : 1 11.
27. Bamford OS, Carroll JL. Dynamic ventilatory responses in rats: Normal development and effects of prenatal nicotine exposure. Respir. Physiol. 1999 117 : 29 40.
28. Simakajornboon N, Vlasic V, Li H, Sawnani H. Effect of prenatal nicotine exposure on biphasic hypoxic ventilatory response and protein kinase C expression in caudal brain stem of developing rats. J. Appl. Physiol. 2004 96 : 2213 2219.
29. Mahliere S, Perrin D, Peyronnet J et al. Prenatal nicotine alters maturation of breathing and neural circuits regulating respiratory control. Respir. Physiol. Neurobiol. 2008 162 : 32 40.
30. Dauger S, Nsegbe E, Vardon G, Gaultier C, Gallego J. The effects of restraint on ventilatory responses to hypercapnia and hypoxia in adult mice. Respir. Physiol. 1998 112 : 215 225.
31. Mortola JP. Influence of temperature on metabolism and breathing during mammalian ontogenesis. Respir. Physiol. Neurobiol. 2005 149 : 155 164.
32. Hafstrom O, Milerad J, Sundell HW. Prenatal nicotine exposure blunts the cardiorespiratory response to hypoxia in lambs. Am. J. Respir. Crit. Care Med. 2002 166 : 1544 1549.
33. Slotkin TA, Saleh JL, McCook EC, Seidler FJ. 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 1997 55 : 177 184.
34. Fewell JE, Smith FG. Perinatal nicotine exposure impairs ability of newborn rats to autoresuscitate from apnea during hypoxia. J. Appl. Physiol. 1998 85 : 2066 2074.
35. Schuen JN, Bamford OS, Carroll JL. The cardiorespiratory response to anoxia: Normal development and the effect of nicotine. Respir. Physiol. 1997 109 : 231 239.
36. Porzionato A, Macchi V, Parenti A, Matturri L, De Caro R. Peripheral chemoreceptors: Postnatal development and cytochemical findings in sudden infant death syndrome. Histol. Histopathol. 2008 23 : 351 365.
37. Perrin DG, Cutz E, Becker LE, Bryan AC, Madapallimatum A, Sole MJ. Sudden infant death syndrome: Increased carotid-body dopamine and noradrenaline content. Lancet 1984 ii : 535 537.
38. Gauda EB, Cooper R, Akins PK, Wu G. Prenatal nicotine affects catecholamine gene expression in newborn rat carotid body and petrosal ganglion. J. Appl. Physiol. 2001 91 : 2157 2165.
39. Berner J, Ringstedt T, Brodin E, Hokfelt T, Lagercrantz H, Wickstrom R. Prenatal exposure to nicotine affects substance P and preprotachykinin-A mRNA levels in newborn rat. Pediatr. Res. 2008 64 : 621 624.
40. Huang ZG, Griffioen KJ, Wang X et al. Differential control of central cardiorespiratory interactions by hypercapnia and the effect of prenatal nicotine. J. Neurosci. 2006 26 : 21 9.
41. Luo Z, McMullen NT, Costy-Bennett S, Fregosi RF. Prenatal nicotine exposure alters glycinergic and GABAergic control of respiratory frequency in the neonatal rat brainstem-spinal cord preparation. Respir. Physiol. Neurobiol. 2007 157 : 226 234.
42. Feldman JL, Mitchell GS, Nattie EE. Breathing: Rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 2003 26 : 239 266.
43. Eugenin J, Nicholls JG. Chemosensory and cholinergic stimulation of fictive respiration in isolated CNS of neonatal opossum. J. Physiol. 1997 501 : 425 437.
44. Eugenin J, von Bernhardi R, Muller KJ, Llona I. Development and pH sensitivity of the respiratory rhythm of fetal mice in vitro. Neuroscience 2006 141 : 223 231.
45. Burton MD, Nouri K, Baichoo S, Samuels-Toyloy N, Kazemi H. Ventilatory output and acetylcholine: Perturbations in release and muscarinic receptor activation. J. Appl. Physiol. 1994 77 : 2275 2284.
46. Hatori E, Sakuraba S, Kashiwagi M et al. Association of nicotinic acetylcholine receptors with central respiratory control in isolated brainstem-spinal cord preparation of neonatal rats. Biol. Res. 2006 39 : 321 330.
47. Monteau R, Morin D, Hilaire G. Acetylcholine and central chemosensitivity: In vitro study in the newborn rat. Respir. Physiol. 1990 81 : 241 254.
48. Burton MD, Johnson DC, Kazemi H. The central respiratory effects of acetylcholine vary with CSF pH. J. Auton. Nerv. Syst. 1997 62 : 27 32.
49. 3H]quinuclidinyl benzilate binding to muscarinic cholinergic receptors in the developing human brainstem. J. Comp. Neurol. 1995 362 : 350 367.
50. Mallios VJ, Lydic R, Baghdoyan HA. Muscarinic receptor subtypes are differentially distributed across brain stem respiratory nuclei. Am. J. Physiol. 1995 268 : L941 9.
51. Dev NB, Loeschcke HH. A cholinergic mechanism involved in the respiratory chemosensitivity. Pflügers Arch. 1979 379 : 29 36.
52. Wonnacott S, Barik J, Dickinson J, Jones IW. Nicotinic receptors modulate transmitter cross talk in the CNS. Nicotinic modulation of transmitters. J. Mol. Neurosci. 2006 30 : 137 140.
53. Vizi ES, Lendvai B. Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res. Brain Res. Rev. 1999 30 : 219 235.
54. Mao C, Yuan X, Cui Y et al. Prenatal exposure to nicotine with associated in utero hypoxia decreased fetal brain muscarinic mRNA in the rat. Brain Res. 2008 1189 : 43 50.
55. Zhu J, Taniguchi T, Konishi Y, Mayumi M, Muramatsu I. Nicotine administration decreases the number of binding sites and mRNA of M1 and M2 muscarinic receptors in specific brain regions of rat neonates. Life Sci. 1998 62 : 1089 1098.
56. Gaimarri A, Moretti M, Riganti L, Zanardi A, Clementi F, Gotti C. Regulation of neuronal nicotinic receptor traffic and expression. Brain Res. Rev. 2007 55 : 134 143.
57. Wang H, Sun X. Desensitized nicotinic receptors in brain. Brain Res. Brain Res. Rev. 2005 48 : 420 437.
58. Slotkin TA, Epps TA, Stenger ML, Sawyer KJ, Seidler FJ. Cholinergic receptors in heart and brainstem of rats exposed to nicotine during development. Implications for hypoxia tolerance and perinatal mortality. Brain Res. 1999 113 : 1 12.
59. Slotkin TA, Southard MC, Adam SJ, Cousins MM, Seidler FJ. Alpha7 nicotinic acetylcholine receptors targeted by cholinergic developmental neurotoxicants: Nicotine and chlorpyrifos. Brain Res. Bull. 2004 64 : 227 235.
60. Frank MG, Srere H, Ledezma C, O'Hara B, Heller HC. Prenatal nicotine alters vigilance states and AchR gene expression in the neonatal rat: Implications for SIDS. Am. J. Physiol. Regul. Intergr. Comp. Physiol. 2001 280 : R1134 40.
61. Lv J, Mao C, Zhu L et al. The effect of prenatal nicotine on expression of nicotine receptor subunits in the fetal brain. Neurotoxicology 2008 29 : 722 726.
62. Shacka JJ, Robinson SE. Exposure to prenatal nicotine transiently increases neuronal nicotinic receptor subunit alpha7, alpha4 and beta2 messenger RNAs in the postnatal rat brain. Neuroscience 1998 84 : 1151 1161.
63. Shao XM, Feldman JL. Pharmacology of nicotinic receptors in preBotzinger complex that mediate modulation of respiratory pattern. J. Neurophysiol. 2002 88 : 1851 1858.
64. Shao XM, Feldman JL. Mechanisms underlying regulation of respiratory pattern by nicotine in preBotzinger complex. J. Neurophysiol. 2001 85 : 2461 2467.
65. Dehkordi O, Haxhiu MA, Millis RM et al. Expression of alpha-7 nAChRs on spinal cord-brainstem neurons controlling inspiratory drive to the diaphragm. Respir. Physiol. Neurobiol. 2004 141 : 21 34.
66. Dehkordi O, Millis RM, Dennis GC et al. Expression of alpha-7 and alpha-4 nicotinic acetylcholine receptors by GABAergic neurons of rostral ventral medulla and caudal pons. Brain Res. 2007 1185 : 95 102.
67. Dwyer JB, Broide RS, Leslie FM. Nicotine and brain development. Birth Defects Res. C Embryo Today 2008 84 : 30 44.
68. Luo Z, Costy-Bennett S, Fregosi RF. Prenatal nicotine exposure increases the strength of GABA(A) receptor-mediated inhibition of respiratory rhythm in neonatal rats. J. Physiol. 2004 561 : 387 393.
69. 3H]hemicholinium-3 binding. Neurotoxicol. Teratol. 1992 14 : 375 382.
70. Slotkin TA, Ryde IT, Seidler FJ. Separate or sequential exposure to nicotine prenatally and in adulthood: Persistent effects on acetylcholine systems in rat brain regions. Brain Res. Bull. 2007 74 : 91 103.
71. Zahalka EA, Seidler FJ, Yanai J, Slotkin TA. Fetal nicotine exposure alters ontogeny of M1-receptors and their link to G-proteins. Neurotoxicol. Teratol. 1993 15 : 107 115.
72. Hobson JA, Pace-Schott EF. The cognitive neuroscience of sleep: Neuronal systems, consciousness and learning. Nat. Rev. 2002 3 : 679 693.
73. Srinivasan M, Lagercrantz H, Yamamoto Y. A possible dopaminergic pathway mediating hypoxic depression in neonatal rabbits. J. Appl. Physiol. 1989 67 : 1271 1276.
74. Goiny M, Lagercrantz H, Srinivasan M, Ungerstedt U, Yamamoto Y. Hypoxia-mediated in vivo release of dopamine in nucleus tractus solitarii of rabbits. J. Appl. Physiol. 1991 70 : 2395 2400.
75. Hilaire G, Viemari JC, Coulon P, Simonneau M, Bevengut M. Modulation of the respiratory rhythm generator by the pontine noradrenergic A5 and A6 groups in rodents. Respir. Physiol. Neurobiol. 2004 143 : 187 197.
76. Viemari JC, Bevengut M, Burnet H et al. Phox2a gene, A6 neurons, and noradrenaline are essential for development of normal respiratory rhythm in mice. J. Neurosci. 2004 24 : 928 937.
77. Navarro HA, Seidler FJ, Whitmore WL, Slotkin TA. Prenatal exposure to nicotine via maternal infusions: Effects on development of catecholamine systems. J. Pharmacol. Exp. Ther. 1988 244 : 940 944.
78. Seidler FJ, Levin ED, Lappi SE, Slotkin TA. Fetal nicotine exposure ablates the ability of postnatal nicotine challenge to release norepinephrine from rat brain regions. Brain Res. 1992 69 : 288 291.
79. Wickstrom HR, Mas C, Simonneau M, Holgert H, Hokfelt T, Lagercrantz H. Perinatal nicotine attenuates the hypoxia-induced up-regulation of tyrosine hydroxylase and galanin mRNA in locus ceruleus of the newborn mouse. Pediatr. Res. 2002 52 : 763 769.
80. Jacobs BL, Azmitia EC. Structure and function of the brain serotonin system. Physiol. Rev. 1992 72 : 165 229.
81. Kinney HC. Abnormalities of the brainstem serotonergic system in the sudden infant death syndrome: A review. Pediatr. Dev. Pathol. 2005 8 : 507 524.
82. Luo X, Persico AM, Lauder JM. Serotonergic regulation of somatosensory cortical development: Lessons from genetic mouse models. Dev. Neurosci. 2003 25 : 173 183.
83. Ponimaskin E, Voyno-Yasenetskaya T, Richter DW, Schachner M, Dityatev A. Morphogenic signaling in neurons via neurotransmitter receptors and small GTPases. Mol. Neurobiol. 2007 35 : 278 287.
84. Duncan JR, Paterson DS, Kinney HC. The development of nicotinic receptors in the human medulla oblongata: Inter-relationship with the serotonergic system. Auton. Neurosci. 2008 144 : 61 75.
85. Muneoka K, Ogawa T, Kamei K, Mimura Y, Kato H, Takigawa M. Nicotine exposure during pregnancy is a factor which influences serotonin transporter density in the rat brain. Eur. J. Pharmacol. 2001 411 : 279 282.
86. Xu Z, Seidler FJ, Ali SF, Slikker Jr W, Slotkin TA. Fetal and adolescent nicotine administration: Effects on CNS serotonergic systems. Brain Res. 2001 914 : 166 178.
87. Slotkin TA, MacKillop EA, Rudder CL, Ryde IT, Tate CA, Seidler FJ. Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions. Indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age. Neuropsychopharmacology 2007 32 : 1082 1097.
88. Neff RA, Wang J, Baxi S, Evans C, Mendelowitz D. Respiratory sinus arrhythmia: Endogenous activation of nicotinic receptors mediates respiratory modulation of brainstem cardioinhibitory parasympathetic neurons. Circ. Res. 2003 93 : 565 572.
89. Kamendi HW, Cheng Q, Dergacheva O et al. Recruitment of excitatory serotonergic neurotransmission to cardiac vagal neurons in the nucleus ambiguus post hypoxia and hypercapnia. J. Neurophysiol. 2008 99 : 1163 1168.
90. Kamendi HW, Cheng Q, Dergacheva O et al. Abolishment of serotonergic neurotransmission to cardiac vagal neurons during and after hypoxia and hypercapnia with prenatal nicotine exposure. J. Neurophysiol. 2009 101 : 1141 1150.
91. Kinney HC, Filiano JJ, White WF. Medullary serotonergic network deficiency in the sudden infant death syndrome: Review of a 15-year study of a single dataset. J. Neuropathol. Exp. Neurol. 2001 60 : 228 247.
92. 3H]nicotine binding in the human brainstem. Neuroscience 1993 55 : 1127 1138.
93. Kinney HC, Filiano JJ, Sleeper LA, Mandell F, Valdes-Dapena M, White WF. Decreased muscarinic receptor binding in the arcuate nucleus in sudden infant death syndrome. Science 1995 269 : 1446 1450.
94. Panigrahy A, Filiano J, Sleeper LA et al. Decreased serotonergic receptor binding in rhombic lip-derived regions of the medulla oblongata in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 2000 59 : 377 384.
95. Mansouri J, Panigrahy A, Filiano JJ, Sleeper LA, St John WM, Kinney HC. Alpha2 receptor binding in the medulla oblongata in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 2001 60 : 141 146.
96. Naeye RL. Brain-stem and adrenal abnormalities in the sudden-infant-death syndrome. Am. J. Clin. Pathol. 1976 66 : 526 530.
97. Kinney HC, Burger PC, Harrell Jr FE, Hudson Jr RP. 'Reactive gliosis' in the medulla oblongata of victims of the sudden infant death syndrome. Pediatrics 1983 72 : 181 187.
98. Matturri L, Ottaviani G, Lavezzi AM. Maternal smoking and sudden infant death syndrome: Epidemiological study related to pathology. Virchows Arch. 2006 449 : 697 706.
99. Kinney HC, Brody BA, Finkelstein DM, Vawter GF, Mandell F, Gilles FH. Delayed central nervous system myelination in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 1991 50 : 29 48.
100. Quattrochi JJ, McBride PT, Yates AJ. Brainstem immaturity in sudden infant death syndrome: A quantitative rapid Golgi study of dendritic spines in 95 infants. Brain Res. 1985 325 : 39 48.
101. Filiano JJ, Kinney HC. Arcuate nucleus hypoplasia in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 1992 51 : 394 403.
102. Kinney HC, McHugh T, Miller K, Belliveau RA, Assmann SF. Subtle developmental abnormalities in the inferior olive: An indicator of prenatal brainstem injury in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 2002 61 : 427 441.
103. Lavezzi AM, Ottaviani G, Matturri L. Adverse effects of prenatal tobacco smoke exposure on biological parameters of the developing brainstem. Neurobiol. Dis. 2005 20 : 601 607.
104. Paus T, Nawazkhan I, Leonard G et al. Corpus callosum in adolescent offspring exposed prenatally to maternal cigarette smoking. Neuroimage 2008 40 : 435 441.
105. Ueda Y, Stick SM, Hall G, Sly PD. Control of breathing in infants born to smoking mothers. J. Pediatr. 1999 135 : 226 232.
106. Thach BT. The role of respiratory control disorders in SIDS. Respir. Physiol. Neurobiol. 2005 149 : 343 353.
107. Sovik S, Lossius K, Eriksen M, Grogaard J, Walloe L. Development of oxygen sensitivity in infants of smoking and non-smoking mothers. Early Hum. Dev. 1999 56 : 217 232.
108. Hafstrom O, Milerad J, Sundell HW. Altered breathing pattern after prenatal nicotine exposure in the young lamb. Am. J. Respir. Crit. Care Med. 2002 166 : 92 7.
109. Shannon DC, Kelly DH, Akselrod S, Kilborn KM. Increased respiratory frequency and variability in high risk babies who die of sudden infant death syndrome. Pediatr. Res. 1987 22 : 158 162.
110. Cohen G, Roux JC, Grailhe R, Malcolm G, Changeux JP, Lagercrantz H. Perinatal exposure to nicotine causes deficits associated with a loss of nicotinic receptor function. Proc. Natl Acad. Sci. USA 2005 102 : 3817 3821.
111. Hanrahan JP, Tager IB, Segal MR et al. The effect of maternal smoking during pregnancy on early infant lung function. Am. Rev. Respir. Dis. 1992 145 : 1129 1135.
112. Tager IB, Ngo L, Hanrahan JP. Maternal smoking during pregnancy. Effects on lung function during the first 18 months of life. Am. J. Respir. Crit. Care Med. 1995 152 : 977 983.
113. Kato I, Groswasser J, Franco P et al. Developmental characteristics of apnea in infants who succumb to sudden infant death syndrome. Am. J. Respir. Crit. Care Med. 2001 164 : 1464 1469.
114. Schechtman VL, Harper RM, Wilson AJ, Southall DP. Sleep apnea in infants who succumb to the sudden infant death syndrome. Pediatrics 1991 87 : 841 846.
115. Kahn A, Groswasser J, Sottiaux M et al. Prenatal exposure to cigarettes in infants with obstructive sleep apneas. Pediatrics 1994 93 : 778 783.
116. Gennser G, Marsal K, Brantmark B. Maternal smoking and fetal breathing movements. Am. J. Obstet. Gynecol. 1975 123 : 861 867.
117. Toubas PL, Duke JC, McCaffree MA, Mattice CD, Bendell D, Orr WC. Effects of maternal smoking and caffeine habits on infantile apnea: A retrospective study. Pediatrics 1986 78 : 159 163.
118. Brady JP, McCann EM. Control of ventilation in subsequent siblings of victims of sudden infant death syndrome. J. Pediatr. 1985 106 : 212 217.
119. Lewis KW, Bosque EM. Deficient hypoxia awakening response in infants of smoking mothers: Possible relationship to sudden infant death syndrome. J. Pediatr. 1995 127 : 691 699.
120. Shannon DC, Kelly DH, O'Connell K. Abnormal regulation of ventilation in infants at risk for sudden-infant-death syndrome. N. Engl. J. Med. 1977 297 : 747 750.
121. Poets CF, Meny RG, Chobanian MR, Bonofiglo RE. Gasping and other cardiorespiratory patterns during sudden infant deaths. Pediatr. Res. 1999 45 : 350 354.
122. Meny RG, Carroll JL, Carbone MT, Kelly DH. Cardiorespiratory recordings from infants dying suddenly and unexpectedly at home. Pediatrics 1994 93 : 44 9.
123. Tirosh E, Libon D, Bader D. The effect of maternal smoking during pregnancy on sleep respiratory and arousal patterns in neonates. J. Perinatol. 1996 16 : 435 438.
124. Kato I, Franco P, Groswasser J et al. Incomplete arousal processes in infants who were victims of sudden death. Am. J. Respir. Crit. Care Med. 2003 168 : 1298 1303.
125. Sawnani H, Jackson T, Murphy T, Beckerman R, Simakajornboon N. The effect of maternal smoking on respiratory and arousal patterns in preterm infants during sleep. Am. J. Respir. Crit. Care Med. 2004 169 : 733 738.
126. Hunt CE. Abnormal hypercarbic and hypoxic sleep arousal responses in near-miss SIDS infants. Pediatr. Res. 1981 15 : 1462 1464.
127. Chang AB, Wilson SJ, Masters IB et al. Altered arousal response in infants exposed to cigarette smoke. Arch. Dis. Child. 2003 88 : 30 3.
128. Horne RS, Franco P, Adamson TM, Groswasser J, Kahn A. Influences of maternal cigarette smoking on infant arousability. Early Hum. Dev. 2004 79 : 49 58.
129. Hafstrom O, Milerad J, Asokan N, Poole SD, Sundell HW. Nicotine delays arousal during hypoxemia in lambs. Pediatr. Res. 2000 47 : 646 652.
130. Sridhar R, Thach BT, Kelly DH, Henslee JA. Characterization of successful and failed autoresuscitation in human infants, including those dying of SIDS. Pediatr. Pulmonol. 2003 36 : 113 122.
131. Fewell JE, Smith FG, Ng VK. Prenatal exposure to nicotine impairs protective responses of rat pups to hypoxia in an age-dependent manner. Respir. Physiol. 2001 127 : 61 73.
132. Fewell JE, Smith FG, Ng VK. Threshold levels of maternal nicotine impairing protective responses of newborn rats to intermittent hypoxia. J. Appl. Physiol. 2001 90 : 1968 1976.
133. Falk L, Nordberg A, Seiger A, Kjaeldgaard A, Hellstrom-Lindahl E. Smoking during early pregnancy affects the expression pattern of both nicotinic and muscarinic acetylcholine receptors in human first trimester brainstem and cerebellum. Neuroscience 2005 132 : 389 397.
134. 3H-nicotine receptor binding in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 1998 57 : 1018 1025.
135. Duncan JR, Randall LL, Belliveau RA et al. The effect of maternal smoking and drinking during pregnancy upon (3)H-nicotine receptor brainstem binding in infants dying of the sudden infant death syndrome: Initial observations in a high risk population. Brain Pathol. 2008 18 : 21 31.
136. 3H]nicotine binding sites in brain regions of rats exposed to nicotine prenatally via maternal injections or infusions. J. Pharmacol. Exp. Ther. 1987 242 : 232 237.
137. Kinney HC, Randall LL, Sleeper LA et al. Serotonergic brainstem abnormalities in Northern Plains Indians with the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 2003 62 : 1178 1191.
138. Paterson DS, Trachtenberg FL, Thompson EG et al. Multiple serotonergic brainstem abnormalities in sudden infant death syndrome. JAMA 2006 296 : 2124 2132.
139. Narita N, Narita M, Takashima S, Nakayama M, Nagai T, Okado N. Serotonin transporter gene variation is a risk factor for sudden infant death syndrome in the Japanese population. Pediatrics 2001 107 : 690 692.
140. Weese-Mayer DE, Ackerman MJ, Marazita ML, Berry-Kravis EM. Sudden infant death syndrome: Review of implicated genetic factors. Am. J. Med. Genet. 2007 143A : 771 788.
141. Ozawa Y, Takashima S, Tada H. Alpha2-adrenergic receptor subtype alterations in the brainstem in the sudden infant death syndrome. Early Hum. Dev. 2003 75 (Suppl S129 38.
142. Carpentier V, Vaudry H, Mallet E, Laquerriere A, Leroux P. Increased density of somatostatin binding sites in respiratory nuclei of the brainstem in sudden infant death syndrome. Neuroscience 1998 86 : 159 166.
143. Panigrahy A, Filiano JJ, Sleeper LA et al. Decreased kainate receptor binding in the arcuate nucleus of the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 1997 56 : 1253 1261.
144. Coddou C, Bravo E, Eugenin J. Alterations in cholinergic sensitivity of respiratory neurons induced by prenatal nicotine: A mechanism for respiratory dysfunction in neonatal mice. Philos. Trans. B 2009 (in press).