Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-26T05:09:13.719Z Has data issue: false hasContentIssue false
  • English
  • Français

Exposure to maternal smoking during fetal life affects food preferences in adulthood independent of the effects of intrauterine growth restriction

Published online by Cambridge University Press:  24 May 2011

C. Ayres ,
P. P. Silveira ,
M. A. Barbieri ,
A. K. Portella ,
H. Bettiol ,
M. Agranonik ,
A. A. Silva  and
M. Z. Goldani
C. Ayres
Affiliation:
Núcleo de Estudos da Saúde da Criança e do Adolescente (NESCA), Hospital de Clínicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
P. P. Silveira*
Affiliation:
Núcleo de Estudos da Saúde da Criança e do Adolescente (NESCA), Hospital de Clínicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
M. A. Barbieri
Affiliation:
Departamento de Pediatria, Faculdade de Medicina de Ribeirão Preto, USP, São Paulo, Brazil
A. K. Portella
Affiliation:
Núcleo de Estudos da Saúde da Criança e do Adolescente (NESCA), Hospital de Clínicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
H. Bettiol
Affiliation:
Departamento de Pediatria, Faculdade de Medicina de Ribeirão Preto, USP, São Paulo, Brazil
M. Agranonik
Affiliation:
Núcleo de Estudos da Saúde da Criança e do Adolescente (NESCA), Hospital de Clínicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
A. A. Silva
Affiliation:
Departamento de Saúde Pública, Universidade Federal do Maranhão, São Luis, Maranhão, Brazil
M. Z. Goldani
Affiliation:
Núcleo de Estudos da Saúde da Criança e do Adolescente (NESCA), Hospital de Clínicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
*
*Address for correspondence: P. P. Silveira, Departamento de Pediatria, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul. Ramiro Barcelos, 2350, Largo Eduardo Zaccaro Faraco, 90035-903 Porto Alegre, Brazil. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Experimental animal studies have shown that nicotine exposure during gestation alters the expression of fetal hypothalamic neuropeptides involved in the control of appetite. We aimed to determine whether the exposure to maternal smoking during gestation in humans is associated with an altered feeding behavior of the adult offspring. A longitudinal prospective cohort study was conducted including all births from Ribeirão Preto (São Paulo, Brazil) between 1978 and 1979. At 24 years of age, a representative random sample was re-evaluated and divided into groups exposed (n = 424) or not (n = 1586) to maternal smoking during gestation. Feeding behavior was analyzed using a food frequency questionnaire. Covariance analysis was used for continuous data and the χ2 test for categorical data. Results were adjusted for birth weight ratio, body mass index, gender, physical activity and smoking, as well as maternal and subjects’ schooling. Individuals exposed to maternal smoking during gestation ate more carbohydrates than proteins (as per the carbohydrate-to-protein ratio) than non-exposed individuals. There were no differences in the consumption of the macronutrients themselves. We propose that this adverse fetal life event programs the individual's physiology and metabolism persistently, leading to an altered feeding behavior that could contribute to the development of chronic diseases in the long term.

Keywords

DOHaDfeeding behaviorprogrammingtobacco smoking during gestation
Type
Original Articles
Information
Journal of Developmental Origins of Health and Disease , Volume 2 , Issue 3 , June 2011 , pp. 162 - 167
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Bernstein, IM, Plociennik, K, Stahle, S, Badger, GJ, Secker-Walker, R. Impact of maternal cigarette smoking on fetal growth and body composition. Am J Obstet Gynecol. 2000; 4, 883–886.CrossRefGoogle Scholar
2. Billaud, N, Lemarie, P. Negative effects of maternal smoking during the course of pregnancy. Arch Pediatr. 2001; 8, 75–81.Google ScholarPubMed
3. Blake, KV, Gurrin, LC, Evans, SF, et al. Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev. 2000; 2, 137–147.CrossRefGoogle Scholar
4. Thapar, A, Fowler, T, Rice, F. Maternal smoking during pregnancy and attention deficit hyperactivity disorder symptoms in offspring. Am J Psychiatry. 2003; 160, 1985–1989.CrossRefGoogle ScholarPubMed
5. Sowan, NA, Stember, ML. Effect of maternal prenatal smoking on infant growth and development of obesity. J Perinat Educ. 2000; 3, 22–29.CrossRefGoogle Scholar
6. Wideroe, M, Vik, T, Jacobsen, G, Bakketeig, LS. Does maternal smoking during pregnancy cause childhood overweight? Paediatr Perinat Epidemiol. 2003; 2, 171–179.CrossRefGoogle Scholar
7. Lussana, F, Painter, RC, Ocke, MC, et al. Prenatal exposure to the Dutch famine is associated with a preference for fatty foods and a more atherogenic lipid profile. Am J Clin Nutr. 2008; 6, 1648–1652.CrossRefGoogle Scholar
8. Barbieri, MA, Portella, AK, Silveira, PP, et al. Severe intrauterine growth restriction is associated with higher spontaneous carbohydrate intake in young women. Pediatr Res. 2009; 2, 215–220.CrossRefGoogle Scholar
9. Grunberg, NE. The effects of nicotine and cigarette smoking on food consumption and taste preferences. Addict Behav. 1982; 4, 317–331.CrossRefGoogle Scholar
10. 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; 4, 439–444.CrossRefGoogle Scholar
11. Grove, KL, Sekhon, HS, Brogan, RS, et al. 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; 11, 5420–5426.CrossRefGoogle Scholar
12. Oliveira, ZAR, Bettiol, H, Barbieri, MA, Gutierrez, MRP, Azenha, VM. Factors associated with infant and adolescence mortality. J Epidemiol Community Health. 2004; 58, 107–108.Google Scholar
13. Barbieri, MA, Bettiol, H, Silva, AA. Health in early adulthood: the contribution of the 1978/79 Ribeirao Preto birth cohort. Braz J Med Biol Res. 2006; 39, 1041–1055.CrossRefGoogle ScholarPubMed
14. Goldani, MZ, Barbieri, MA, Silva, AA, Bettiol, H. Trends in prenatal care use and low birthweight in southeast Brazil. Am J Public Health. 2004; 94, 1366–1371.CrossRefGoogle ScholarPubMed
15. Tomita, LY, Cardoso, MA. Assessment of the food list and serving size of a food frequency questionnaire in an adult population. Cad Saude Publica. 2002; 18, 1747–1756.CrossRefGoogle Scholar
16. Molina, MC, Bettiol, H, Barbieri, MA, et al. Food consumption by young adults living in Ribeirão Preto, SP, 2002/2004. Braz J Med Biol Res. 2007; 40, 1257–1266.CrossRefGoogle Scholar
17. Layman, DK, Boileau, RA, Erickson, DJ, et al. A reduced ratio of dietary carbohydrate to protein improves body composition and blood lipid profiles during weight loss in adult women. J Nutr. 2003; 2, 411–417.CrossRefGoogle Scholar
18. Hallal, PC, Victora, CG. Reliability and validity of the international physical activity questionnaire (IPAQ). Med Sci Sports Exerc. 2004; 3, 556.CrossRefGoogle Scholar
19. LaMonte, MJ, Nahas, MV, Neff, LJ, Bartoli, BP, Ainsworth, BE. Trends in physical activity levels among black and white adults in South Carolina. J S C Med Assoc. 2000; 10, 416–420.Google Scholar
20. Keys, DP, Fidanza, F, Kcarvonen, MJ, Kimura, N, Taylor, HK. Indices of relative weight and obesity. J Chron Dis. 1972; 25, 329–343.CrossRefGoogle ScholarPubMed
21. Kramer, MS, Platt, R, Yang, H, McNamara, H, Usher, RH. Are all growth-restricted newborns created equal(ly)? Pediatrics. 1999; 103, 599–602.CrossRefGoogle ScholarPubMed
22. De Rooij, SR, Painter, RC, Phillips, DI, et al. Hypothalamic-pituitary-adrenal axis activity in adults who were prenatally exposed to the Dutch famine. Eur J Endocrinol. 2006; 1, 153–160.CrossRefGoogle Scholar
23. Chadio, SE, Kotsampasi, B, Papadomichelakis, G, et al. Impact of maternal undernutrition on the hypothalamic-pituitary-adrenal axis responsiveness in sheep at different ages postnatal. J Endocrinol. 2007; 3, 495–503.CrossRefGoogle Scholar
24. Pecoraro, N, Reyes, F, Gomez, F, Bhargava, A, Dallman, MF. Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology. 2004; 145, 3754–3762.CrossRefGoogle ScholarPubMed
25. McDonald, SD, Walker, M, Perkins, SL, et al. The effect of tobacco exposure on the fetal hypothalamic-pituitary-adrenal axis. BJOG. 2006; 11, 1289–1295.CrossRefGoogle Scholar
26. Von Kries, R, Toschke, AM, Koletzko, B, JrSlikker, W. Maternal smoking during pregnancy and childhood obesity. Am J Epidemiol. 2002; 10, 954–961.CrossRefGoogle Scholar
27. Power, C, Jefferis, BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol. 2002; 2, 413–419.CrossRefGoogle Scholar
28. Franke, RM, Park, M, Belluzzi, JD, Leslie, FM. Prenatal nicotine exposure changes natural and drug-induced reinforcement in adolescent male rats. Eur J Neurosci. 2008; 11, 2952–2961.CrossRefGoogle Scholar
29. Law, KL, Stroud, LR, LaGasse, LL, et al. Smoking during pregnancy and newborn neurobehavior. Pediatrics. 2003; 111, 1318–1323.CrossRefGoogle ScholarPubMed
30. Buka, SL, Shenassa, ED, Niaura, R. Elevated risk of tobacco dependence among offspring of mothers who smoked during pregnancy: a 30-year prospective study. Am J Psychiatry. 2003; 160, 1978–1984.CrossRefGoogle ScholarPubMed
31. Avena, NM, Long, KA, Hoebel, BG. Sugar-dependent rats show enhanced responding for sugar after abstinence: evidence of a sugar deprivation effect. Physiol Behav. 2005; 84, 359–362.CrossRefGoogle ScholarPubMed
32. Cadoni, C, Valentini, V, Di Chiara, G. Behavioral sensitization to delta 9-tetrahydrocannabinol and cross-sensitization with morphine: differential changes in accumbal shell and core dopamine transmission. J Neurochem. 2008; 4, 1586–1593.CrossRefGoogle Scholar
33. Le Merrer, J, Stephens, DN. Food-induced behavioral sensitization, its cross-sensitization to cocaine and morphine, pharmacological blockade, and effect on food intake. J Neurosci. 2006; 27, 7163–7171.CrossRefGoogle Scholar
34. Wooters, TE, Neugebauer, NM, Rush, CR, Bardo, MT. Methylphenidate enhances the abuse-related behavioral effects of nicotine in rats: intravenous self-administration, drug discrimination, and locomotor cross-sensitization. Neuropsychopharmacology. 2008; 5, 1137–1148.CrossRefGoogle Scholar
35. Myrsten, A, Elaerot, A, Ednren, B. Effects of abstinence from tobacco smoking on physiological and psychological arousal levels-in habitual smokers. Psychosomatic Med. 1977; 39, 25–38.CrossRefGoogle ScholarPubMed
36. Schaefer, EJ, Augustin, JL, Schaefer, MM, et al. Lack of efficacy of a food-frequency questionnaire in assessing dietary macronutrient intakes in subjects consuming diets of known composition. Am J Clin Nutr. 2000; 71, 746–751.CrossRefGoogle ScholarPubMed
37. Larson, NI, Neumark-Sztainer, DR, Harnack, LJ, et al. Fruit and vegetable intake correlates during the transition to young adulthood. Am J Prev Med. 2008; 35, 33–37.CrossRefGoogle ScholarPubMed
38. Klaus, S. Increasing the protein: carbohydrate ratio in a high-fat diet delays the development of adiposity and improves glucose homeostasis in mice. J Nutr. 2005; 135, 1854–1858.CrossRefGoogle Scholar
39. Layman, DK, Evans, EM, Erickson, D, et al. A moderate-protein diet produces sustained weight loss and long-term changes in body composition and blood lipids in obese adults. J Nutr. 2009; 139, 514–521.CrossRefGoogle ScholarPubMed