REVIEW PAPER
Exposure to Smoke During Development: Fetal Programming of Adult Disease
 
 
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Dept. of Human Anatomy & Cell Science, University of Manitoba, Canada
 
 
Publication date: 2006-08-15
 
 
Tobacco Induced Diseases 2006;3(August):5
 
KEYWORDS
ABSTRACT
It is well established that smoking has potent effects on a number of parameters including food intake, body weight, metabolism, and blood pressure. For example, it is well documented that 1) there is an inverse relationship between smoking and body weight, and 2) smoking cessation is associated with weight gain. However, there is increasing evidence that smoking can exert deleterious effects on energy balance through maternal exposure during fetal development. Specifically, there appears to be an increased incidence of metabolic disease (including obesity), and cardiovascular disease in children and adults that were exposed to smoke during fetal development. The present review will examine the relationship between maternal smoke and adult disease in offspring. The epidemiological studies highlighting this relationship will be reviewed as well as the experimental animal models that point to potential mechanisms underlying this relationship. A better understanding of how smoking effects changes in energy balance may lead to treatments to ameliorate the long-lasting effects of perinatal exposure to smoke as well as increasing the health benefits associated with smoking cessation.
 
REFERENCES (86)
1.
Gluckman PD, Hanson MA: Living with the past: evolution, development, and patterns of disease. Science. 2004, 305: 1733-1736. 10.1126/science.1095292.
 
2.
Remacle C, Bieswal F, Reusens B: Programming of obesity and cardiovascular disease. Int J Obes Relat Metab Disord. 2004, 28 (Suppl 3): S46-S53. 10.1038/sj.ijo.0802800.
 
3.
Barker DJ, Osmond C, Law CM: The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health. 1989, 43: 237-240. 10.1136/jech.43.3.237.
 
4.
Hales CN, Barker DJ: The thrifty phenotype hypothesis. Br Med Bull. 2001, 60: 5-20. 10.1093/bmb/60.1.5.
 
5.
Ozanne SE, Fernandez-Twinn D, Hales CN: Fetal growth and adult diseases. Semin Perinatol. 2004, 28: 81-87. 10.1053/j.semperi.2003.10.015.
 
6.
Plagemann A: 'Fetal programming' and 'functional teratogenesis': on epigenetic mechanisms and prevention of perinatally acquired lasting health risks. J Perinat Med. 2004, 32: 297-305. 10.1515/JPM.2004.055.
 
7.
Stocker CJ, Arch JR, Cawthorne MA: Fetal origins of insulin resistance and obesity. Proc Nutr Soc. 2005, 64: 143-151. 10.1079/PNS2005417.
 
8.
Ong KK, Dunger DB: Perinatal growth failure: the road to obesity, insulin resistance and cardiovascular disease in adults. Best Pract Res Clin Endocrinol Metab. 2002, 16: 191-207. 10.1053/beem.2002.0195.
 
9.
Hales CN, Barker DJ: Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothes is. Diabetologia. 1992, 35: 595-601. 10.1007/BF00400248.
 
10.
Ravelli GP, Stein ZA, Susser MW: Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976, 295: 349-353.
 
11.
Barker DJ: In utero programming of chronic disease. Clin Sci (Lond). 1998, 95: 115-128.
 
12.
Aerts L, Van Assche FA: Intra-uterine transmission of disease. Placenta. 2003, 24: 905-911. 10.1016/S0143-4004(03)00115-2.
 
13.
Simmons R: Developmental origins of adult metabolic disease. Endocrinol Metab Clin North Am. 2006, 35: 193-204. 10.1016/j.ecl.2005.09.006.
 
14.
Sallout B, Walker M: The fetal origin of adult diseases. J Obstet Gynaecol. 2003, 23: 555-560. 10.1080/0144361031000156483.
 
15.
Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ: Weight in infancy and death from ischaemic heart disease. Lancet. 1989, 2: 577-580. 10.1016/S0140-6736(89)90710-1.
 
16.
Levin BE: Metabolic imprinting on genetically predisposed neural circuits perpetuates obesity. Nutrition. 2000, 16: 909-915. 10.1016/S0899-9007(00)00408-1.
 
17.
McMillen IC, Robinson JS: Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005, 85: 571-633. 10.1152/physrev.00053.2003.
 
18.
McArdle HJ, Andersen HS, Jones H, Gambling L: Fetal Programming: Causes and Consequences as Revealed by Studies of Dietary Manipulation in Rats – A Review. Placenta. 2006, 27 (Suppl A): S56-S60. 10.1016/j.placenta.2006.01.014.
 
19.
Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L: Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals?. J Physiol. 2004, 561: 355-377. 10.1113/jphysiol.2004.072009.
 
20.
Montgomery SM, Ekbom A: Smoking during pregnancy and diabetes mellitus in a British longitudinal birth cohort. BMJ. 2002, 324: 26-27. 10.1136/bmj.324.7328.26.
 
21.
von Kries R, Toschke AM, Koletzko B, Slikker W: Maternal smoking during pregnancy and childhood obesity. Am J Epidemiol. 2002, 156: 954-961. 10.1093/aje/kwf128.
 
22.
Vik T, Jacobsen G, Vatten L, Bakketeig LS: Pre- and post-natal growth in children of women who smoked in pregnancy. Early Human Development. 1996, 45: 245-255. 10.1016/0378-3782(96)01735-5.
 
23.
Ellard GA, Johnstone FD, Prescott RJ, Ji-Xian W, Jian-Hua M: Smoking during pregnancy: the dose dependence of birthweight deficits. Br J Obstet Gynaecol. 1996, 103: 806-813.
 
24.
Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB: Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000, 320: 967-971. 10.1136/bmj.320.7240.967.
 
25.
Dulloo AG, Jacquet J, Montani JP: Pathways from weight fluctuations to metabolic diseases: focus on maladaptive thermogenesis during catch-up fat. Int J Obes Relat Metab Disord. 2002, 26 (Suppl 2): S46-S57. 10.1038/sj.ijo.0802127.
 
26.
Ross MG, Desai M: Gestational programming: population survival effects of drought and famine during pregnancy. Am J Physiol Regul Integr Comp Physiol. 2005, 288: R25-33.
 
27.
Dubois L, Girard M: Early determinants of overweight at 4.5 years in a population-based longitudinal study. Int J Obes (Lond). 2006, 30: 610-617. 10.1038/sj.ijo.0803141.
 
28.
Power C, Jefferis BJ: Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol. 2002, 31: 413-419. 10.1093/ije/31.2.413.
 
29.
Wideroe M, Vik T, Jacobsen G, Bakketeig LS: Does maternal smoking during pregnancy cause childhood overweight?. Paediatric and Perinatal Epidemiology. 2003, 17: 171-179. 10.1046/j.1365-3016.2003.00481.x.
 
30.
Toschke AM, Koletzko B, Slikker W, Hermann M, von Kries R: Childhood obesity is associated with maternal smoking in pregnancy. Eur J Pediatr. 2002, 161: 445-448. 10.1007/s00431-002-0983-z.
 
31.
Adams AK, Harvey HE, Prince RJ: Association of maternal smoking with overweight at age 3 y in American Indian children. Am J Clin Nutr. 2005, 82: 393-398.
 
32.
Horta BL, Victora CG, Menezes AM, Halpern R, Barros FC: Low birthweight, preterm births and intrauterine growth retardation in relation to maternal smoking. Paediatr Perinat Epidemiol. 1997, 11: 140-151. 10.1046/j.1365-3016.1997.d01-17.x.
 
33.
Fox NL, Sexton M, Hebel JR: Prenatal exposure to tobacco: I. Effects on physical growth at age three. Int J Epidemiol. 1990, 19: 66-71. 10.1093/ije/19.1.66.
 
34.
Toschke AM, Montgomery SM, Pfeiffer U, von Kries R: Early intrauterine exposure to tobacco-inhaled products and obesity. Am J Epidemiol. 2003, 158: 1068-1074. 10.1093/aje/kwg258.
 
35.
Oken E, Huh SY, Taveras EM, Rich-Edwards JW, Gillman MW: Associations of maternal prenatal smoking with child adiposity and blood pressure. Obes Res. 2005, 13: 2021-2028. 10.1038/oby.2005.248.
 
36.
Hill SY, Shen S, Locke Wellman J, Rickin E, Lowers L: Offspring from families at high risk for alcohol dependence: increased body mass index in association with prenatal exposure to cigarettes but not alcohol. Psychiatry Res. 2005, 135: 203-216. 10.1016/j.psychres.2005.04.003.
 
37.
Law CM, Shiell AW: Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature. J Hypertens. 1996, 14: 935-941. 10.1097/00004872-199608000-00002.
 
38.
Blake KV, Gurrin LC, Evans SF, Beilin LJ, Landau LI, Stanley FJ, Newnham JP: Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev. 2000, 57: 137-147. 10.1016/S0378-3782(99)00064-X.
 
39.
Lawlor DA, Najman JM, Sterne J, Williams GM, Ebrahim S, Smith GD: Associations of Parental, Birth, and Early Life Characteristics With Systolic Blood Pressure at 5 Years of Age: Findings From the Mater-University Study of Pregnancy and Its Outcomes. Circulation. 2004, 110: 2417-2423. 10.1161/01.CIR.0000145165.80130.B5.
 
40.
Oken E, Gillman MW: Fetal origins of obesity. Obes Res. 2003, 11: 496-506. 10.1038/oby.2003.69.
 
41.
Levy-Marchal C, Jaquet D, Czernichow P: Long-term metabolic consequences of being born small for gestational age. Semin Neonatol. 2004, 9: 67-74. 10.1016/j.siny.2003.08.001.
 
42.
Albanes D, Jones DY, Micozzi MS, Mattson ME: Associations between smoking and body weight in the US population: analysis of NHANES II. Am J Public Health. 1987, 77: 439-444. 10.2105/AJPH.77.4.439.
 
43.
Hofstetter A, Schutz Y, Jequier E, Wahren J: Increased 24-hour energy expenditure in cigarette smokers. N Engl J Med. 1986, 314: 79-82.
 
44.
Jessen A, Buemann B, Toubro S, Skovgaard IM, Astrup A: The appetite-suppressant effect of nicotine is enhanced by caffeine. Diabetes Obes Metab. 2005, 7: 327-333. 10.1111/j.1463-1326.2004.00389.x.
 
45.
Grunberg NE: Nicotine as a psychoactive drug: appetite regulation. Psychopharmacol Bull. 1986, 22: 875-881.
 
46.
Klesges RC, Eck LH, Isbell TR, Fulliton W, Hanson CL: Smoking status: effects on the dietary intake, physical activity, and body fat of adult men. Am J Clin Nutr. 1990, 51: 784-789.
 
47.
Leischow SJ, Stitzer ML: Effects of smoking cessation on caloric intake and weight gain in an in patient unit. Psychopharmacology (Berl). 1991, 104: 522-526. 10.1007/BF02245660.
 
48.
Collins LC, Walker J, Stamford BA: Smoking multiple high-versus low-nicotine cigarettes: impact on resting energy expenditure. Metabolism. 1996, 45: 923-926. 10.1016/S0026-0495(96)90256-5.
 
49.
Lambers DS, Clark KE: The maternal and fetal physiologic effects of nicotine. Semin Perinatol. 1996, 20: 115-126. 10.1016/S0146-0005(96)80079-6.
 
50.
Andersen KV, Hermann N: Placenta flow reduction in pregnant smokers. Acta Obstet Gynecol Scand. 1984, 63: 707-709.
 
51.
Lindblad A, Marsal K, Andersson KE: Effect of nicotine on human fetal blood flow. Obstet Gynecol. 1988, 72: 371-382.
 
52.
Castro LC, Allen R, Ogunyemi D, Roll K, Platt LD: Cigarette smoking during pregnancy: acute effects on uterine flow velocity waveforms. Obstet Gynecol. 1993, 81: 551-555.
 
53.
Salafia C, Shiverick K: Cigarette smoking and pregnancy II: vascular effects. Placenta. 1999, 20: 273-279. 10.1053/plac.1998.0378.
 
54.
Jauniaux E, Burton GJ: The effect of smoking in pregnancy on early placental morphology. Obstet Gynecol. 1992, 79: 645-648.
 
55.
Burton GJ, Palmer ME, Dalton KJ: Morphometric differences between the placental vasculature of non-smokers, smokers and ex-smokers. Br J Obstet Gynaecol. 1989, 96: 907-915.
 
56.
Larsen LG, Clausen HV, Jonsson L: Stereologic examination of placentas from mothers who smoke during pregnancy. Am J Obstet Gynecol. 2002, 186: 531-537. 10.1067/mob.2002.120481.
 
57.
Bush PG, Mayhew TM, Abramovich DR, Aggett PJ, Burke MD, Page KR: A quantitative study on the effects of maternal smoking on placental morphology and cadmium concentration. Placenta. 2000, 21: 247-256. 10.1053/plac.1999.0470.
 
58.
Genbacev O, Bass KE, Joslin RJ, Fisher SJ: Maternal smoking inhibits early human cytotrophoblast differentiation. Reprod Toxicol. 1995, 9: 245-255. 10.1016/0890-6238(95)00006-V.
 
59.
Genbacev O, McMaster MT, Zdravkovic T, Fisher SJ: Disruption of oxygen-regulated responses underlies pathological changes in the placentas of women who smoke or who are passively exposed to smoke during pregnancy. Reprod Toxicol. 2003, 17: 509-518. 10.1016/S0890-6238(03)00094-7.
 
60.
Pastrakuljic A, Derewlany LO, Koren G: Maternal Cocaine Use and Cigarette Smoking in Pregnancy in Relation to Amino Acid Transport and Fetal Growth. Placenta. 1999, 20: 499-512. 10.1053/plac.1999.0418.
 
61.
Mantzoros CS, Varvarigou A, Kaklamani VG, Beratis NG, Flier JS: Effect of birth weight and maternal smoking on cord blood leptin concentrations of full-term and preterm newborns. J Clin Endocrinol Metab. 1997, 82: 2856-2861. 10.1210/jc.82.9.2856.
 
62.
Coutant R, Boux de Casson F, Douay O, Mathieu E, Rouleau S, Beringue F, Gillard P, Limal JM, Descamps P: Relationships between Placental GH Concentration and Maternal Smoking, Newborn Gender, and Maternal Leptin: Possible Implications for Birth Weight. J Clin Endocrinol Metab. 2001, 86: 4854-4859. 10.1210/jc.86.10.4854.
 
63.
Sanigorski A, Fahey R, Cameron-Smith D, Collier GR: Nicotine treatment decreases food intake and body weight via a leptin-independent pathway in Psammomys obesus. Diabetes Obes Metab. 2002, 4: 346-350. 10.1046/j.1463-1326.2002.00216.x.
 
64.
Miyata G, Meguid MM, Fetissov SO, Torelli GF, Kim HJ: Nicotine's effect on hypothalamic neurotransmitters and appetite regulation. Surgery. 1999, 126: 255-263.
 
65.
Yang ZJ, Blaha V, Meguid MM, Oler A, Miyata G: Infusion of nicotine into the LHA enhances dopamine and 5-HT release and suppresses food intake. Pharmacol Biochem Behav. 1999, 64: 155-159. 10.1016/S0091-3057(99)00111-2.
 
66.
Winders SE, Grunberg NE: Effects of nicotine on body weight, food consumption and body composition in male rats. Life Sci. 1990, 46: 1523-1530. 10.1016/0024-3205(90)90425-Q.
 
67.
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 Dev Brain Res. 2002, 133: 175-179. 10.1016/S0165-3806(02)00284-5.
 
68.
Slotkin TA, Seidler FJ, Qiao D, Aldridge JE, Tate CA, Cousins MM, Proskocil BJ, Sekhon HS, Clark JA, Lupo SL, others: Effects of prenatal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin C: neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of rhesus monkeys. Neuropsychopharmacology. 2005, 30: 129-144. 10.1038/sj.npp.1300544.
 
69.
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. 10.1016/S0014-2999(00)00925-0.
 
70.
Muneoka K, Ogawa T, Kamei K, Muraoka S, Tomiyoshi R, Mimura Y, Kato H, Suzuki MR, Takigawa M: Prenatal nicotine exposure affects the development of the central serotonergic system as well as the dopaminergic system in rat offspring: involvement of route of drug administrations. Brain Res Dev Brain Res. 1997, 102: 117-126. 10.1016/S0165-3806(97)00092-8.
 
71.
Muneoka K, Nakatsu T, Fuji J, Ogawa T, Takigawa M: Prenatal administration of nicotine results in dopaminergic alterations in the neocortex. Neurotoxicol Teratol. 1999, 21: 603-609. 10.1016/S0892-0362(99)00028-8.
 
72.
Yanai J, Pick CG, Rogel-Fuchs Y, Zahalka EA: Alterations in hippocampal cholinergic receptors and hippocampal behaviors after early exposure to nicotine. Brain Res Bull. 1992, 29: 363-368. 10.1016/0361-9230(92)90069-A.
 
73.
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. 10.1073/pnas.0409782102.
 
74.
Grove KL, Sekhon HS, Brogan RS, Keller JA, Smith MS, Spindel ER: Chronic maternal nicotine exposure alters neuronal systems in the arcuate nucleus that regulate feeding behavior in the newborn rhesus macaque. J Clin Endocrinol Metab. 2001, 86: 5420-5426. 10.1210/jc.86.11.5420.
 
75.
Xu Z, Seidler FJ, Ali SF, Slikker W, Slotkin TA: Fetal and adolescent nicotine administration: effects on CNS serotonergic systems. Brain Res. 2001, 914: 166-178. 10.1016/S0006-8993(01)02797-4.
 
76.
Abreu-Villaca Y, Seidler FJ, Tate CA, Cousins MM, Slotkin TA: Prenatal nicotine exposure alters the response to nicotine administration in adolescence: effects on cholinergic systems during exposure and withdrawal. Neuropsychopharmacology. 2004, 29: 879-890. 10.1038/sj.npp.1300401.
 
77.
Li MD, Kane JK: Effect of nicotine on the expression of leptin and forebrain leptin receptors in the rat. Brain Res. 2003, 991: 222-231. 10.1016/j.brainres.2003.08.024.
 
78.
Das UN: Pathophysiology of metabolic syndrome X and its links to the perinatal period. Nutrition. 2005, 21: 762-773. 10.1016/j.nut.2004.11.005.
 
79.
Cripps RL, Martin-Gronert MS, Ozanne SE: Fetal and perinatal programming of appetite. Clin Sci (Lond). 2005, 109: 1-11.
 
80.
Ahima RS, Bjorbaek C, Osei S, Flier JS: Regulation of neuronal and glial proteins by leptin: implications for brain development. Endocrinology. 1999, 140: 2755-2762. 10.1210/en.140.6.2755.
 
81.
Bouret SG, Draper SJ, Simerly RB: Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004, 304: 108-110. 10.1126/science.1095004.
 
82.
Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X, Friedman JM, Horvath TL: Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science. 2004, 304: 110-115. 10.1126/science.1089459.
 
83.
Horvath TL, Bruning JC: Developmental programming of the hypothalamus: a matter of fat. Nat Med. 2006, 12: 52-53. 10.1038/nm0106-52.
 
84.
Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, Gertler A, Breier BH, Harris M: Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005, 146: 4211-4216. 10.1210/en.2005-0581.
 
85.
Bouret SG, Simerly RB: Minireview: Leptin and development of hypothalamic feeding circuits. Endocrinology. 2004, 145: 2621-2626. 10.1210/en.2004-0231.
 
86.
Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, Nakao K, Kawamura M, Takemura M, Kakui K, Ogawa Y, others: Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab. 2005, 1: 371-378. 10.1016/j.cmet.2005.05.005.
 
 
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