Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T12:41:55.623Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of in utero conditions on adult feeding preferences

Published online by Cambridge University Press:  06 March 2012

A. K. Portella ,
E. Kajantie ,
P. Hovi ,
M. Desai ,
M. G. Ross ,
M. Z. Goldani ,
T. J. Roseboom  and
P. P. Silveira
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, Brazil
E. Kajantie
Affiliation:
Children's Hospital, Helsinki University Central Hospital and University of Helsinki, Helsinki, Finland Department of Chronic Disease Prevention, Diabetes Prevention Unit, National Institute for Health and Welfare, Helsinki, Finland
P. Hovi
Affiliation:
Children's Hospital, Helsinki University Central Hospital and University of Helsinki, Helsinki, Finland Department of Chronic Disease Prevention, Diabetes Prevention Unit, National Institute for Health and Welfare, Helsinki, Finland
M. Desai
Affiliation:
Department of Obstetrics and Gynecology, Harbor-UCLA Medical Center, Los Angeles Biomedical Research Institute at Harbor-UCLA, David Geffen School of Medicine at UCLA, Torrance, California, USA
M. G. Ross
Affiliation:
Department of Obstetrics and Gynecology, Harbor-UCLA Medical Center, Los Angeles Biomedical Research Institute at Harbor-UCLA, David Geffen School of Medicine at UCLA, Torrance, California, USA
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, Brazil
T. J. Roseboom
Affiliation:
Department of Clinical Epidemiology and Biostatistics and Department of Obstetrics and Gynaecology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
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, 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

The fetal or early origins of adult disease hypothesis states that environmental factors, particularly nutrition, act in early life to program the risks for chronic diseases in adult life. As eating habits can be linked to the development of several diseases including obesity, diabetes and cardiovascular disease, it could be proposed that persistent food preferences across the life-span in people who were exposed to an adverse fetal environment may partially explain their increased risk to develop metabolic disease later in life. In this paper, we grouped the clinical and experimental evidence demonstrating that the fetal environment may impact the individual's food preferences. In addition, we review the feeding preferences development and regulation (homeostatic and hedonic pathways, the role of taste/olfaction and the reward/pleasure), as well as propose mechanisms linking early life conditions to food preferences later in life. We review the evidence suggesting that in utero conditions are associated with the development of specific food preferences, which may be involved in the risk for later disease. This may have implications in terms of public health and primary prevention during early ages.

Keywords

DOHaDfeeding preferencesfetal programmingthrifty behavior
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 3 , June 2012 , pp. 140 - 152
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012

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. Barker, DJ, Eriksson, JG, Forsen, T, et al. . Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002; 31, 1235–1239.CrossRefGoogle ScholarPubMed
2. Eriksson, JG, Forsen, T, Tuomilehto, J, et al. . Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia. 2002; 45, 342–348.CrossRefGoogle ScholarPubMed
3. Whincup, PH, Kaye, SJ, Owen, CG, et al. . Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008; 300, 2886–2897.Google ScholarPubMed
4. Lauren, L, Jarvelin, MR, Elliott, P, et al. . Relationship between birthweight and blood lipid concentrations in later life: evidence from the existing literature. Int J Epidemiol. 2003; 32, 862–876.CrossRefGoogle ScholarPubMed
5. Davies, AA, Smith, GD, Ben-Shlomo, Y, et al. . Low birth weight is associated with higher adult total cholesterol concentration in men: findings from an occupational cohort of 25,843 employees. Circulation. 2004; 110, 1258–1262.CrossRefGoogle Scholar
6. Szathmari, M, Vasarhelyi, B, Szabo, M, et al. . Higher osteocalcin levels and cross-links excretion in young men born with low birth weight. Calcif Tissue Int. 2000; 67, 429–433.CrossRefGoogle ScholarPubMed
7. Dennison, E, Syddall, H, Sayer, A, et al. . Birth weight and weight at 1 year are independent determinants of bone mass in the seventh decade: the Hertfordshire cohort study. Pediatr Res. 2005; 57, 582–586.CrossRefGoogle ScholarPubMed
8. Laitinen, J, Kiukaanniemi, K, Heikkinen, J, et al. . Body size from birth to adulthood and bone mineral content and density at 31 years of age: results from the northern Finland 1966 birth cohort study. Osteoporos Int. 2005; 16, 1417–1424.CrossRefGoogle ScholarPubMed
9. Hovi, P, Andersson, S, Jarvenpaa, A, et al. . Decreased bone mineral density in adults born with very low birth weight: a cohort study. PLoS Med. 2009; 6, e1000135.CrossRefGoogle ScholarPubMed
10. Jones, A, Beda, A, Ward, AM, et al. . Size at birth and autonomic function during psychological stress. Hypertension. 2007; 49, 548–555.CrossRefGoogle ScholarPubMed
11. Kajantie, E, Raikkonen, K. Early life predictors of the physiological stress response later in life. Neurosci Biobehav Rev. 2010; 35, 23–32.CrossRefGoogle ScholarPubMed
12. Painter, RC, de Rooij, SR, Bossuyt, PM, et al. . Maternal nutrition during gestation and carotid arterial compliance in the adult offspring: the Dutch famine birth cohort. J Hypertens. 2007; 25, 533–540.CrossRefGoogle ScholarPubMed
13. de Rooij, SR, Painter, RC, Phillips, DI, et al. . Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care. 2006; 29, 1897–1901.CrossRefGoogle Scholar
14. Jones, A, Godfrey, KM, Wood, P, et al. . Fetal growth and the adrenocortical response to psychological stress. J Clin Endocrinol Metab. 2006; 91, 1868–1871.CrossRefGoogle ScholarPubMed
15. Rice, F, Harold, GT, Thapar, A. The effect of birth-weight with genetic susceptibility on depressive symptoms in childhood and adolescence. Eur Child Adolesc Psychiatry. 2006; 15, 383–391.CrossRefGoogle ScholarPubMed
16. Thompson, C, Syddall, H, Rodin, I, et al. . Birth weight and the risk of depressive disorder in late life. Br J Psychiatry. 2001; 179, 450–455.CrossRefGoogle ScholarPubMed
17. Gross, LS, Li, L, Ford, ES, et al. . Increased consumption of refined carbohydrates and the epidemic of type 2 diabetes in the United States: an ecologic assessment. Am J Clin Nutr. 2004; 79, 774–779.CrossRefGoogle ScholarPubMed
18. Oh, K, Hu, FB, Cho, E, et al. . Carbohydrate intake, glycemic index, glycemic load, and dietary fiber in relation to risk of stroke in women. Am J Epidemiol. 2005; 161, 161–169.CrossRefGoogle ScholarPubMed
19. Liu, S, Willett, WC, Stampfer, MJ, et al. . A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease in US women. Am J Clin Nutr. 2000; 71, 1455–1461.CrossRefGoogle ScholarPubMed
20. 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; 133, 411–417.CrossRefGoogle ScholarPubMed
21. Plagemann, A, Harder, T, Rake, A, et al. . Increased number of galanin-neurons in the paraventricular hypothalamic nucleus of neonatally overfed weanling rats. Brain Res. 1999; 818, 160–163.CrossRefGoogle ScholarPubMed
22. Bayol, SA, Farrington, SJ, Stickland, NC. A maternal ‘junk food’ diet in pregnancy and lactation promotes an exacerbated taste for ‘junk food’ and a greater propensity for obesity in rat offspring. Br J Nutr. 2007; 98, 843–851.CrossRefGoogle Scholar
23. Silveira, P, Portella, A, Clemente, Z, et al. . Neonatal handling alters feeding behavior of adult rats. Physiol Behav. 2004; 80, 739–745.CrossRefGoogle ScholarPubMed
24. Bouret, SG, Simerly, RB. Development of leptin-sensitive circuits. J Neuroendocrinol. 2007; 19, 575–582.CrossRefGoogle ScholarPubMed
25. Plagemann, A. Perinatal nutrition and hormone-dependent programming of food intake. Horm Res. 2006; 65(Suppl 3), 83–89.Google ScholarPubMed
26. El-Haddad, MA, Desai, M, Gayle, D, et al. . In utero development of fetal thirst and appetite: potential for programming. J Soc Gynecol Investig. 2004; 11, 123–130.CrossRefGoogle ScholarPubMed
27. Breier, BH, Vickers, MH, Ikenasio, BA, et al. . Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001; 185, 73–79.CrossRefGoogle ScholarPubMed
28. Bouret, SG. Leptin, nutrition, and the programming of hypothalamic feeding circuits. Nestle Nutr Workshop Ser Pediatr Program. 2010; 65, 25–35; discussion 35-29.CrossRefGoogle ScholarPubMed
29. Craig, W. Appetites and aversions as constituents of instincts. Proc Natl Acad Sci USA. 1917; 3, 685–688.CrossRefGoogle ScholarPubMed
30. Swanson, LW, Mogenson, GJ. Neural mechanisms for the functional coupling of autonomic, endocrine and somatomotor responses in adaptive behavior. Brain Res. 1981; 228, 1–34.CrossRefGoogle ScholarPubMed
31. Watts, AG. Understanding the neural control of ingestive behaviors: helping to separate cause from effect with dehydration-associated anorexia. Horm Behav. 2000; 37, 261–283.CrossRefGoogle ScholarPubMed
32. Berthoud, HR. Multiple neural systems controlling food intake and body weight. Neurosci Biobehav Rev. 2002; 26, 393–428.CrossRefGoogle ScholarPubMed
33. Nicklaus, S, Boggio, V, Chabanet, C, et al. . A prospective study of food variety seeking in childhood, adolescence and early adult life. Appetite. 2005; 44, 289–297.CrossRefGoogle ScholarPubMed
34. Skinner, JD, Carruth, BR, Wendy, B, et al. . Children's food preferences: a longitudinal analysis. J Am Diet Assoc. 2002; 102, 1638–1647.CrossRefGoogle ScholarPubMed
35. Nicklas, TA, Webber, LS, Berenson, GS. Studies of consistency of dietary intake during the first four years of life in a prospective analysis: Bogalusa Heart Study. J Am Coll Nutr. 1991; 10, 234–241.CrossRefGoogle Scholar
36. Devine, CM, Wolfe, WS, Frongillo, EA Jr, et al. . Life-course events and experiences: association with fruit and vegetable consumption in 3 ethnic groups. J Am Diet Assoc. 1999; 99, 309–314.CrossRefGoogle ScholarPubMed
37. Bradley, RM, Stern, IB. The development of the human taste bud during the foetal period. J Anat. 1967; 101, 743–752.Google ScholarPubMed
38. Davis, ME, Potter, EL. Intrauterine respiration of the human fetus. J Am Med Assoc. 1946; 131, 1194–1201.CrossRefGoogle ScholarPubMed
39. Windle, WF. Physiology of the Fetus; Origin and Extent of Function in Prenatal Life. W. B. Saunders Company: Philadelphia, 1940.CrossRefGoogle Scholar
40. Brien, JF, Loomis, CW, Tranmer, J, et al. . Disposition of ethanol in human maternal venous blood and amniotic fluid. Am J Obstet Gynecol. 1983; 146, 181–186.CrossRefGoogle ScholarPubMed
41. Mennella, J, Jagnow, C, Beauchamp, G. Prenatal and postnatal flavor learning by human infants. Pediatrics. 2001; 107, E88.CrossRefGoogle ScholarPubMed
42. Mennella, JA, Johnson, A, Beauchamp, GK. Garlic ingestion by pregnant women alters the odor of amniotic fluid. Chem Senses. 1995; 20, 207–209.CrossRefGoogle ScholarPubMed
43. Mennella, JA, Beauchamp, GK. Maternal diet alters the sensory qualities of human milk and the nursling's behavior. Pediatrics. 1991; 88, 737–744.Google Scholar
44. Mennella, JA, Beauchamp, GK. The effects of repeated exposure to garlic-flavored milk on the nursling's behavior. Pediatr Res. 1993; 34, 805–808.CrossRefGoogle Scholar
45. Mennella, J, Beauchamp, G. The human infants’ response to vanilla flavors in mother's milk and formula. Infant Behav Dev. 1996; 19, 13–19.CrossRefGoogle Scholar
46. Schwartz, C, Issanchou, S, Nicklaus, S. Developmental changes in the acceptance of the five basic tastes in the first year of life. Br J Nutr. 2009; 102, 1375–1385.CrossRefGoogle ScholarPubMed
47. Mennella, J, Nicklaus, S, Jagolino, A, et al. . Variety is the spice of life: strategies for promoting fruit and vegetable acceptance during infancy. Physiol Behav. 2008; 94, 29–38.CrossRefGoogle ScholarPubMed
48. Sullivan, S, Birch, L. Infant dietary experience and acceptance of solid foods. Pediatrics. 1994; 93, 271–277.CrossRefGoogle ScholarPubMed
49. Gerrish, CJ, Mennella, JA. Flavor variety enhances food acceptance in formula-fed infants. Am J Clin Nutr. 2001; 73, 1080–1085.CrossRefGoogle ScholarPubMed
50. Liem, DG, de Graaf, C. Sweet and sour preferences in young children and adults: role of repeated exposure. Physiol Behav. 2004; 15; 83, 421–429.CrossRefGoogle Scholar
51. Scaglioni, S, Salvioni, M, Galimberti, C. Influence of parental attitudes in the development of children eating behaviour. Br J Nutr. 2008; 99(Suppl 1), S22–S25.CrossRefGoogle ScholarPubMed
52. Breer, H. The sense of smell – reception of flavors. maillard reaction: recent advances in food and biomedical sciences book series. Ann N Y Acad Sci. 2008; 1126, 1–6.CrossRefGoogle Scholar
53. Djordjevic, J, Zatorre, R, Jones-Gotman, M. Odor-induced changes in taste perception. Exp Brain Res. 2004; 159, 405–408.CrossRefGoogle ScholarPubMed
54. Rozin, P, Vollmecke, T. Food likes and dislikes. Annu Rev Nutr. 1986; 6, 433–456.CrossRefGoogle ScholarPubMed
55. Bolles, RC. The Hedonics of Taste, 1991. L. Erlbaum Associates: Hillsdale, NJ.Google Scholar
56. Rogers, P, Hill, A. Breakdown of dietary restraint following mere exposure to food stimuli – interrelationships between restraint, hunger, salivation, and food-intake. Addict Behav. 1989; 14, 387–397.CrossRefGoogle ScholarPubMed
57. Johnson, W, Wildman, H. Influence of external and covert food stimuli on insulin-secretion in obese and normal persons. Behav Neurosci. 1983; 97, 1025–1028.CrossRefGoogle ScholarPubMed
58. Louissylvestre, J, Lemagnen, J. Palatability and pre-absorptive insulin release. Neurosci Biobehav Rev. 1980; 4, 43–46.CrossRefGoogle Scholar
59. Feldman, M, Richardson, C. Role of thought, sight, smell, and taste of food in the cephalic phase of gastric-acid secretion in humans. Gastroenterology. 1986; 90, 428–433.CrossRefGoogle ScholarPubMed
60. Rolls, E, Rolls, J. Olfactory sensory-specific satiety in humans. Physiol Behav. 1997; 61, 461–473.CrossRefGoogle ScholarPubMed
61. Anliker, J, Bartoshuk, L, Ferris, A, et al. . Childrens food preferences and genetic sensitivity to the bitter taste of 6-normal-propylthiouracil (prop). Am J Clin Nutr. 1991; 54, 316–320.CrossRefGoogle Scholar
62. Birch, L. Childrens preferences for high-fat foods. Nutr Rev. 1992; 50, 249–255.CrossRefGoogle ScholarPubMed
63. Drewnowski, A, Henderson, S, Driscoll, A, et al. . Salt taste perceptions and preferences are unrelated to sodium consumption in healthy older adults. J Am Diet Assoc. 1996; 96, 471–474.CrossRefGoogle ScholarPubMed
64. Gibney, M, Sigmangrant, M, Stanton, J, et al. . Consumption of sugars. Am J Clin Nutr. 1995; 62, S178–S194; discussion 194S.CrossRefGoogle ScholarPubMed
65. Anderson, G. Sugars, sweetness, and food-intake. Am J Clin Nutr. 1995; 62, S195–S202; discussion 201S–202S.CrossRefGoogle ScholarPubMed
66. Frank, R, Vanderklaauw, N. The contribution of chemosensory factors to individual-differences in reported food preferences. Appetite. 1994; 22, 101–123.CrossRefGoogle ScholarPubMed
67. Markskaufman, R, Kanarek, R. Morphine selectively influences macronutrient intake in the rat. Pharmacol Biochem Behav. 1980; 12, 427–430.CrossRefGoogle ScholarPubMed
68. Markskaufman, R. Increased fat consumption induced by morphine administration in rats. Pharmacol Biochem Behav. 1982; 16, 949–955.CrossRefGoogle ScholarPubMed
69. Romsos, D, Gosnell, B, Morley, J, et al. . Effects of kappa-opiate agonists, cholecystokinin and bombesin on intake of diets varying in carbohydrate-to-fat ratio in rats. J Nutr. 1987; 117, 976–985.CrossRefGoogle ScholarPubMed
70. Stanley, B, Daniel, D, Chin, A, et al. . Paraventricular nucleus injections of peptide-YY and neuropeptide-Y preferentially enhance carbohydrate ingestion. Peptides. 1985; 6, 1205–1211.CrossRefGoogle ScholarPubMed
71. Baldwin, A, Sadeghian, K, Holahan, M, et al. . Appetitive instrumental learning is impaired by inhibition of cAMP-dependent protein kinase within the nucleus accumbens. Neurobiol Learn Mem. 2002; 77, 44–62.CrossRefGoogle ScholarPubMed
72. Corbit, L, Muir, J, Balleine, B. The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell. J Neurosci. 2001; 21, 3251–3260.CrossRefGoogle ScholarPubMed
73. Killgore, W, Young, A, Femia, L, et al. . Cortical and limbic activation during viewing of high- versus low-calorie foods. Neuroimage. 2003; 19, 1381–1394.CrossRefGoogle ScholarPubMed
74. Rothemund, Y, Preuschhof, C, Bohner, G, et al. . Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. Neuroimage. 2007; 37, 410–421.CrossRefGoogle ScholarPubMed
75. Abizaid, A, Liu, Z, Andrews, Z, et al. . Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest. 2006; 116, 3229–3239.CrossRefGoogle ScholarPubMed
76. Jerlhag, E, Egecioglu, E, Dickson, S, et al. . Ghrelin stimulates locomotor activity and accumbal dopamine-overflow via central cholinergic systems in mice: implications for its involvement in brain reward. Addict Biol. 2006; 11, 45–54.CrossRefGoogle ScholarPubMed
77. Figlewicz, D. Adiposity signals and food reward: expanding the CNS roles of insulin and leptin. Am J Physiol Regul Integr Comp Physiol. 2003; 284, R882–R892.CrossRefGoogle ScholarPubMed
78. Plagemann, A. A matter of insulin: developmental programming of body weight regulation. J Matern Fetal Neonatal Med. 2008; 21, 143–148.CrossRefGoogle ScholarPubMed
79. Ahima, RS, Prabakaran, D, Flier, JS. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest. 1998; 101, 1020–1027.CrossRefGoogle ScholarPubMed
80. Oliver, G, Wardle, J, Gibson, E. Stress and food choice. A laboratory study. Psychosom Med. 2000; 62, 853–865.CrossRefGoogle Scholar
81. Mccann, B, Warnick, G, Knopp, R. Changes in plasma-lipids and dietary-intake accompanying shifts in perceived workload and stress. Psychosom Med. 1990; 52, 97–108.CrossRefGoogle ScholarPubMed
82. Wardle, J, Steptoe, A, Oliver, G, et al. . Stress, dietary restraint and food intake. J Psychosom Res. 2000; 48, 195–202.CrossRefGoogle ScholarPubMed
83. Michaud, C, Kahn, J, Musse, N, et al. . Relationships between a critical life event and eating behavior in high-school-students. Stress Med. 1990; 6, 57–64.CrossRefGoogle Scholar
84. Epel, E, Lapidus, R, McEwen, B, et al. . Stress may add bite to appetite in women: a laboratory study of stress-induced cortisol and eating behavior. Psychoneuroendocrinology. 2001; 26, 37–49.CrossRefGoogle ScholarPubMed
85. Dallman, M, Pecoraro, N, Akana, S, et al. . Chronic stress and obesity: a new view of ‘comfort food’. Proc Natl Acad Sci USA. 2003; 100, 11696–11701.CrossRefGoogle ScholarPubMed
86. Bembich, S, Lanzara, C, Clarici, A, et al. . Individual differences in prefrontal cortex activity during perception of bitter taste using fNIRS methodology. Chem Senses. 2010; 35, 801–812.CrossRefGoogle ScholarPubMed
87. Zald, D. Orbitofrontal cortex contributions to food selection and decision making. Ann Behav Med. 2009; 38(Suppl 1), S18–S24.CrossRefGoogle ScholarPubMed
88. Davids, S, Lauffer, H, Thoms, K, et al. . Increased dorsolateral prefrontal cortex activation in obese children during observation of food stimuli. Int J Obes (Lond). 2010; 34, 94–104.CrossRefGoogle ScholarPubMed
89. Leitner, Y, Fattal-Valevski, A, Geva, R, et al. . Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol. 2007; 22, 580–587.CrossRefGoogle ScholarPubMed
90. Geva, R, Eshel, R, Leitner, Y, et al. . Memory functions of children born with asymmetric intrauterine growth restriction. Brain Res. 2006; 1117, 186–194.CrossRefGoogle ScholarPubMed
91. Franzek, E, Sprangers, N, Janssens, A, et al. . Prenatal exposure to the 1944–45 Dutch ‘hunger winter’ and addiction later in life. Addiction. 2008; 103, 433–438.CrossRefGoogle Scholar
92. Heinonen, K, Raikkonen, K, Pesonen, A, et al. . Behavioural symptoms of attention deficit/hyperactivity disorder in preterm and term children born small and appropriate for gestational age: a longitudinal study. BMC Pediatr. 2010; 10, 91.CrossRefGoogle ScholarPubMed
93. Tonkiss, J, Shukitthale, B, Formica, R, et al. . Prenatal protein-malnutrition alters response to reward in adult-rats. Physiol Behav. 1990; 48, 675–680.CrossRefGoogle ScholarPubMed
94. Farooqi, I, Bullmore, E, Keogh, J, et al. . Leptin regulates striatal regions and human eating behavior. Science. 2007; 317, 1355–1355.CrossRefGoogle ScholarPubMed
95. Figlewicz, D, Bennett, J, Aliakbari, S, et al. . Insulin acts at different CNS sites to decrease acute sucrose intake and sucrose self-administration in rats. Am J Physiol Regul Integr Comp Physiol. 2008; 295, R388–R394.CrossRefGoogle ScholarPubMed
96. Koistinen, H, Koivisto, V, Andersson, S, et al. . Leptin concentration in cord blood correlates with intrauterine growth. J Clin Endocrinol Metab. 1997; 82, 3328–3330.Google ScholarPubMed
97. Jaquet, D, Leger, J, Levy-Marchal, C, et al. . Ontogeny of leptin in human fetuses and newborns: effect of intrauterine growth retardation on serum leptin concentrations. J Clin Endocrinol Metab. 1998; 83, 1243–1246.CrossRefGoogle ScholarPubMed
98. Jaquet, D, Leger, J, Tabone, M, et al. . High serum leptin concentrations during catch-up growth of children born with intrauterine growth retardation. J Clin Endocrinol Metab. 1999; 84, 1949–1953.Google ScholarPubMed
99. Jaquet, D, Gaboriau, A, Czernichow, P, et al. . Relatively low serum leptin levels in adults born with intra-uterine growth retardation. Int J Obes Relat Metab Disord. 2001; 25, 491–495.CrossRefGoogle ScholarPubMed
100. Jensen, C, Storgaard, H, Dela, F, et al. . Early differential defects of insulin secretion and action in 19-year-old caucasian men who had low birth weight. Diabetes. 2002; 51, 1271–1280.CrossRefGoogle ScholarPubMed
101. de Rooij, S, Painter, R, Phillips, D, et al. . Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care. 2006; 29, 1897–1901.CrossRefGoogle Scholar
102. Ravelli, A, van der Meulen, J, Michels, R, et al. . Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998; 351, 173–177.CrossRefGoogle ScholarPubMed
103. Forsen, T, Eriksson, J, Tuomilehto, J, et al. . The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med. 2000; 133, 176–182.CrossRefGoogle ScholarPubMed
104. Wang, GJ, Volkow, ND, Thanos, PK, Fowler, JS. Imaging of brain dopamine pathways: implications for understanding obesity. J Addict Med. 2009; 3, 8–18.CrossRefGoogle ScholarPubMed
105. Blumenthal, DM, Gold, MS. Neurobiology of food addiction. Curr Opin Clin Nutr Metab Care. 2010; 13, 359–365.CrossRefGoogle ScholarPubMed
106. Kenny, PJ. Reward mechanisms in obesity: new insights and future directions. Neuron. 2011; 69, 664–679.CrossRefGoogle ScholarPubMed
107. Avena, NM, Rada, P, Hoebel, BG. Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev. 2008; 32, 20–39.CrossRefGoogle ScholarPubMed
108. Colantuoni, C, Schwenker, J, McCarthy, J, et al. . Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain. NeuroReport. 2001; 12, 3549–3552.CrossRefGoogle ScholarPubMed
109. Colantuoni, C, Rada, P, McCarthy, J, et al. . Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res. 2002; 10, 478–488.CrossRefGoogle ScholarPubMed
110. 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
111. Avena, NM, Carrillo, CA, Needham, L, Leibowitz, SF, Hoebel, BG. Sugar-dependent rats show enhanced intake of unsweetened ethanol. Alcohol. 2004; 34, 203–209.CrossRefGoogle ScholarPubMed
112. Davis, C, Strachan, S, Berkson, M. Sensitivity to reward: implications for overeating and overweight. Appetite. 2004; 42, 131–138.CrossRefGoogle ScholarPubMed
113. Martin, B, Maudsley, S, White, C, et al. . Hormones in the naso-oropharynx: endocrine modulation of taste and smell. Trends Endocrinol Metab. 2009; 20, 163–170.CrossRefGoogle ScholarPubMed
114. Touzani, K, Bodnar, R, Sclafani, A. Neuropharmacology of learned flavor preferences. Pharmacol Biochem Behav. 2010; 97, 55–62.CrossRefGoogle ScholarPubMed
115. Greenwood, P, Hunt, A, Hermanson, J, et al. . Effects of birth weight and postnatal nutrition on neonatal sheep: I. Body growth and composition, and some aspects of energetic efficiency. J Anim Sci. 1998; 76, 2354–2367.CrossRefGoogle ScholarPubMed
116. Ozanne, S, Lewis, R, Jennings, B, et al. . Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet. Clin Sci. 2004; 106, 141–145.CrossRefGoogle ScholarPubMed
117. Zambrano, E, Bautista, C, Deas, M, et al. . A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571, 221–230.CrossRefGoogle ScholarPubMed
118. Desai, M, Gayle, D, Babu, J, et al. . Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R91–R96.CrossRefGoogle ScholarPubMed
119. Vickers, MH, Breier, BH, Cutfield, WS, et al. . Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 2000; 279, E83–E87.CrossRefGoogle ScholarPubMed
120. Jia, Y, Nguyen, T, Desai, M, et al. . Programmed alterations in hypothalamic neuronal orexigenic responses to ghrelin following gestational nutrient restriction. Reprod Sci. 2008; 15, 702–709.CrossRefGoogle Scholar
121. Desai, M, Gayle, D, Han, G, et al. . Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reprod Sci. 2007; 14, 329–337.CrossRefGoogle ScholarPubMed
122. Bellinger, L, Langley-Evans, S. Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clin Sci. 2005; 109, 413–420.CrossRefGoogle ScholarPubMed
123. Engeham, S, Haase, A, Langley-Evans, S. Supplementation of a maternal low-protein diet in rat pregnancy with folic acid ameliorates programming effects upon feeding behaviour in the absence of disturbances to the methionine–homocysteine cycle. Br J Nutr. 2010; 103, 996–1007.CrossRefGoogle Scholar
124. Nakashima, Y, Tsukita, Y, Yokoyama, M. Preferential fat intake of pups nursed by dams fed low fat diet during pregnancy and lactation is higher than that of pups nursed by dams fed control diet and high fat diet. J Nutr Sci Vitaminol. 2008; 54, 215–222.CrossRefGoogle ScholarPubMed
125. Samuelsson, A, Matthews, P, Argenton, M, et al. . Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance – a novel murine model of developmental programming. Hypertension. 2008; 51, 383–392.CrossRefGoogle ScholarPubMed
126. Lesage, J, Del-Favero, F, Leonhardt, M, et al. . Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinol. 2004; 181, 291–296.CrossRefGoogle ScholarPubMed
127. Pankevich, D, Mueller, B, Brockel, B, et al. . Prenatal stress programming of offspring feeding behavior and energy balance begins early in pregnancy. Physiol Behav. 2009; 98, 94–102.CrossRefGoogle ScholarPubMed
128. 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; 88, 1648–1652.CrossRefGoogle Scholar
129. Stein, AD, Rundle, A, Wada, N, et al. . Associations of gestational exposure to famine with energy balance and macronutrient density of the diet at age 58 years differ according to the reference population used. J Nutr. 2009; 139, 1555–1561.CrossRefGoogle Scholar
130. Barbieri, M, Portella, A, Silveira, P, et al. . Severe intrauterine growth restriction is associated with higher spontaneous carbohydrate intake in young women. Pediatr Res. 2009; 65, 215–220.CrossRefGoogle ScholarPubMed
131. Cleeman, J, Grundy, S, Becker, D, et al. . Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA. 2001; 285, 2486–2497.Google Scholar
132. Simpson, SJ, Raubenheimer, D. Obesity: the protein leverage hypothesis. Obes Rev. 2005; 6, 133–142.CrossRefGoogle ScholarPubMed
133. Bettiol, H, Rona, R, Chinn, S, et al. . Factors associated with preterm births in southeast Brazil: a comparison of two births cohorts born 15 years apart. Pediatr Res. 1999; 45, 101A–101A.CrossRefGoogle Scholar
134. Da Silva, C, Agranonik, M, Da Silva, A, et al. . Secular trend of very low birth weight rate in Porto Alegre, Southern Brazil. J Biosoc Sci. 2010; 42, 243–253.CrossRefGoogle Scholar
135. Samara, M, Johnson, S, Lamberts, K, et al. . Eating problems at age 6 years in a whole population sample of extremely preterm children. Dev Med Child Neurol. 2010; 52, e16–e22.CrossRefGoogle Scholar
136. Doyle, LW, Faber, B, Callanan, C, et al. . Blood pressure in late adolescence and very low birth weight. Pediatrics. 2003; 111, 252–257.CrossRefGoogle ScholarPubMed
137. Hovi, P, Andersson, S, Räikkönen, K, et al. . Ambulatory blood pressure in young adults with very low birth weight. J Pediatr. 2010; 156, 54–59.CrossRefGoogle ScholarPubMed
138. Hovi, P, Andersson, S, Eriksson, JG, et al. . Glucose regulation in young adults with very low birth weight. N Engl J Med. 2007; 356, 2053–2063.CrossRefGoogle ScholarPubMed
139. Kajantie, E, Strang-Karlsson, S, Hovi, P, et al. . Adults born at very low birth weight exercise less than their peers born at term. J Pediatr. 2010; 157, 610–616, 616.e1.CrossRefGoogle ScholarPubMed
140. Saigal, S, Stoskopf, B, Boyle, M, et al. . Comparison of current health, functional limitations, and health care use of young adults who were born with extremely low birth weight and normal birth weight. Pediatrics. 2007; 119, e562–e573.CrossRefGoogle ScholarPubMed
141. Hack, M, Schluchter, M, Cartar, L, et al. . Growth of very low birth weight infants to age 20 years. Pediatrics. 2003; 112, e30–e38.CrossRefGoogle ScholarPubMed
142. Sipola-Leppänen, M, Hovi, P, Andersson, S, et al. . Resting energy expenditure in adults born preterm at very low birth weight. PLoS One. 2011; 6, e17700.CrossRefGoogle ScholarPubMed
143. Kaseva, N, Wehkalmpi, K, Hemiö, K, et al. . Preterm birth at very low birth weight and nutrient intake in adult life. Abstract 7th World Congress on Developmental Origins of Health and Disease. JDOHaD. 2011; 2, S103.Google Scholar
144. Navarro-Allende, A, Khataan, N, El-Sohemy, A. Impact of genetic and environmental determinants of taste with food preferences in older adults. J Nutr Elder. 2008; 27, 267–276.CrossRefGoogle ScholarPubMed
145. Chapman, K, Ogden, J. How do people change their diet? An exploration into mechanisms of dietary change. J Health Psychol. 2009; 14, 1229–1242.CrossRefGoogle ScholarPubMed
146. Pacak, K, Palkovits, M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev. 2001; 22, 502–548.CrossRefGoogle ScholarPubMed
147. Brunner, E, Mosdol, A, Witte, D, et al. . Dietary patterns and 15-y risks of major coronary events, diabetes, and mortality. Am J Clin Nutr. 2008; 87, 1414–1421.CrossRefGoogle ScholarPubMed
148. Halton, T, Willett, W, Liu, S, et al. . Potato and french fry consumption and risk of type 2 diabetes in women. Am J Clin Nutr. 2006; 83, 284–290.CrossRefGoogle ScholarPubMed
149. van Dam, R, Rimm, E, Willett, W, et al. . Dietary patterns and risk for type 2 diabetes mellitus in US men. Ann Intern Med. 2002; 136, 201–209.CrossRefGoogle ScholarPubMed
150. Fung, T, Schulze, M, Manson, J, et al. . Dietary patterns, meat intake, and the risk of type 2 diabetes in women. Arch Intern Med. 2004; 164, 2235–2240.CrossRefGoogle ScholarPubMed
151. Nettleton, J, Steffen, L, Loehr, L, et al. . Incident heart failure is associated with lower whole-grain intake and greater high-fat dairy and egg intake in the Atherosclerosis Risk in Communities (ARIC) Study. J Am Diet Assoc. 2008; 108, 1881–1887.CrossRefGoogle ScholarPubMed
152. Hu, F, Rimm, E, Stampfer, M, et al. . Prospective study of major dietary patterns and risk of coronary heart disease in men. Am J Clin Nutr. 2000; 72, 912–921.CrossRefGoogle ScholarPubMed
153. Varraso, R, Fung, T, Barr, R, et al. . Prospective study of dietary patterns and chronic obstructive pulmonary disease among US women. Am J Clin Nutr. 2007; 86, 488–495.CrossRefGoogle ScholarPubMed
154. Slattery, M, Boucher, K, Caan, B, et al. . Eating patterns and risk of colon cancer. Am J Epidemiol. 1998; 148, 4–16.CrossRefGoogle ScholarPubMed
155. Flood, A, Rastogi, T, Wirfalt, E, et al. . Dietary patterns as identified by factor analysis and colorectal cancer among middle-aged Americans. Am J Clin Nutr. 2008; 88, 176–184.CrossRefGoogle ScholarPubMed
156. Lopez-Garcia, E, Schulze, M, Fung, T, et al. . Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr. 2004; 80, 1029–1035.CrossRefGoogle Scholar
157. Fung, T, Rimm, E, Spiegelman, D, et al. . Association between dietary patterns and plasma biomarkers of obesity and cardiovascular disease risk. Am J Clin Nutr. 2001; 73, 61–67.CrossRefGoogle ScholarPubMed
158. Barclay, A, Flood, V, Brand-Miller, J, et al. . Glycemic index, glycemic load, and chronic disease risk – reply. Am J Clin Nutr. 2008; 88, 476–477.CrossRefGoogle Scholar
159. Barclay, A, Petocz, P, McMillan-Price, J, et al. . Glycemic index, glycemic load, and chronic disease risk – a metaanalysis of observational studies. Am J Clin Nutr. 2008; 87, 627–637.CrossRefGoogle Scholar
160. Holmberg, S, Thelin, A, Stiernstrom, E. Food choices and coronary heart disease: a population based cohort study of rural swedish men with 12 years of follow-up. Int J Environ Res Public Health. 2009; 6, 2626–2638.CrossRefGoogle ScholarPubMed
161. Mellen, P, Walsh, T, Herrington, D. Whole grain intake and cardiovascular disease: a meta-analysis. Nutr Metab Cardiovasc Dis. 2008; 18, 283–290.CrossRefGoogle ScholarPubMed
162. Mozaffarian, D, Kumanyika, S, Lemaitre, R, et al. . Cereal, fruit, and vegetable fiber intake and the risk of cardiovascular disease in elderly individuals. JAMA. 2003; 289, 1659–1666.CrossRefGoogle ScholarPubMed
163. Joshipura, K, Hu, F, Manson, J, et al. . The effect of fruit and vegetable intake on risk for coronary heart disease. Ann Intern Med. 2001; 134, 1106–1114.CrossRefGoogle ScholarPubMed
164. Joshipura, K, Ascherio, A, Manson, J, et al. . Fruit and vegetable intake in relation to risk of ischemic stroke. JAMA. 1999; 282, 1233–1239.CrossRefGoogle ScholarPubMed
165. Steffen, L, Kroenke, C, Yu, X, et al. . Associations of plant food, dairy product, and meat intakes with 15-y incidence of elevated blood pressure in young black and white adults: the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Am J Clin Nutr. 2005; 82, 1169–1177.CrossRefGoogle ScholarPubMed
166. Liese, A, Roach, A, Sparks, K, et al. . Whole-grain intake and insulin sensitivity: the insulin resistance atherosclerosis study. Am J Clin Nutr. 2003; 78, 965–971.CrossRefGoogle ScholarPubMed
167. Pereira, M, Jacobs, D, Pins, J, et al. . Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am J Clin Nutr. 2002; 75, 848–855.CrossRefGoogle ScholarPubMed
168. Qi, L, Van Dam, R, Liu, S, et al. . Whole-grain, bran, and cereal fiber intakes and markers of systemic inflammation in diabetic women. Diabetes Care. 2006; 29, 207–211.CrossRefGoogle ScholarPubMed
169. Pereira, MA, Pins, JJ. Dietary fiber and cardiovascular disease: experimental and epidemiologic advances. Curr Atheroscler Rep. 2000; 2, 494–502.CrossRefGoogle ScholarPubMed
170. Jenkins, D, Axelsen, M, Kendall, C, et al. . Dietary fibre, lente carbohydrates and the insulin-resistant diseases. Br J Nutr. 2000; 83(Suppl 1), S157–S163.CrossRefGoogle ScholarPubMed
171. Mozaffarian, D, Ascherio, A, Hu, F, et al. . Interplay between different polyunsaturated fatty acids and risk of coronary heart disease in men. Circulation. 2005; 111, 157–164.CrossRefGoogle ScholarPubMed
172. He, K, Rimm, E, Merchant, A, et al. . Fish consumption and risk of stroke in men. JAMA. 2002; 288, 3130–3136.CrossRefGoogle ScholarPubMed
173. Smith, K, McNaughton, S, Gall, S, et al. . Takeaway food consumption and its associations with diet quality and abdominal obesity: a cross-sectional study of young adults. Int J Behav Nutr Phys Act. 2009; 6, 29–41.CrossRefGoogle ScholarPubMed
174. Larson, N, Perry, C, Story, M, et al. . Food preparation by young adults is associated with better diet quality. J Am Diet Assoc. 2006; 106, 2001–2007.CrossRefGoogle ScholarPubMed
175. Holmback, I, Ericson, U, Gullberg, B, et al. . A high eating frequency is associated with an overall healthy lifestyle in middle-aged men and women and reduced likelihood of general and central obesity in men. Br J Nutr. 2010; 104, 1065–1073.CrossRefGoogle ScholarPubMed
176. Masson, LF, McNeill, G, Avenell, A. Genetic variation and the lipid response to dietary intervention: a systematic review. Am J Clin Nutr. 2003; 77, 1098–1111.CrossRefGoogle ScholarPubMed
177. Franco, V, Oparil, S. Salt sensitivity, a determinant of blood pressure, cardiovascular disease and survival. J Am Coll Nutr. 2006; 25, 247S–255S.CrossRefGoogle ScholarPubMed
178. Bennet, AM, Di Angelantonio, E, Ye, Z, et al. . Association of apolipoprotein E genotypes with lipid levels and coronary risk. J Am Med Assoc. 2007; 298, 1300–1311.CrossRefGoogle ScholarPubMed
179. Fontaine-Bisson, B, Wolever, TM, Chiasson, JL, et al. . Genetic polymorphisms of tumor necrosis factor-alpha modify the association between dietary polyunsaturated fatty acids and fasting HDL-cholesterol and apo A-I concentrations. Am J Clin Nutr. 2007; 86, 768–774.CrossRefGoogle ScholarPubMed
180. Nettleton, JA, Volcik, KA, Hoogeveen, RC, Boerwinkle, E. Carbohydrate intake modifies associations between ANGPTL4[E40K] genotype and HDL-cholesterol concentrations in White men from the Atherosclerosis Risk in Communities (ARIC) study. Atherosclerosis. 2009; 203, 214–220.CrossRefGoogle ScholarPubMed
181. Robinson, SM, Batelaan, SF, Syddall, HE, et al. . Combined effects of dietary fat and birth weight on serum cholesterol concentrations: the Hertfordshire Cohort Study. Am J Clin Nutr. 2006; 84, 237–244.CrossRefGoogle ScholarPubMed
182. de Boer, MP, Ijzerman, RG, de Jongh, RT, et al. . Birth weight relates to salt sensitivity of blood pressure in healthy adults. Hypertension. 2008; 51, 928–932.CrossRefGoogle ScholarPubMed
183. Davis, J, Ventura, E, Shaibi, G, et al. . Interventions for improving metabolic risk in overweight Latino youth. Int J Pediatr Obes. 2010; 5, 451–455.CrossRefGoogle ScholarPubMed
184. Davis, J, Tung, A, Chak, S, et al. . Aerobic and strength training reduces adiposity in overweight Latina adolescents. Med Sci Sports Exerc. 2009; 41, 1494–1503.CrossRefGoogle ScholarPubMed
185. Raman, A, Ritchie, L, Lustig, R, et al. . Insulin resistance is improved in overweight African American boys but not in girls following a one-year multidisciplinary community intervention program. J Pediatr Endocrinol Metab. 2010; 23, 109–120.CrossRefGoogle Scholar
186. Savoye, M, Shaw, M, Dziura, J, et al. . Effects of a weight management program on body composition and metabolic parameters in overweight children – a randomized controlled trial. JAMA. 2007; 297, 2697–2704.CrossRefGoogle ScholarPubMed
187. Monzavi, R, Dreimane, D, Geffner, M, et al. . Improvement in risk factors for metabolic syndrome and insulin resistance in overweight youth who are treated with lifestyle intervention. Pediatrics. 2006; 117, E1111–E1118.CrossRefGoogle ScholarPubMed
188. Zhang, C, Schulze, M, Solomon, C, et al. . A prospective study of dietary patterns, meat intake and the risk of gestational diabetes mellitus. Diabetologia. 2006; 49, 2604–2613.CrossRefGoogle ScholarPubMed
189. Silveira, P, Portella, A, Diorio, J, et al. . Preliminary evidence for an impulsivity-based thrifty eating phenotype. Ped Res. 2012; 71, 293–298.CrossRefGoogle ScholarPubMed
190. Ounsted, M, Sleigh, G. Infants self-regulation of food-intake and weight-gain – difference in metabolic balance after growth constraint or acceleration in utero. Lancet. 1975; 1, 1393–1397.CrossRefGoogle ScholarPubMed
191. Hales, CN, Barker, DJ. The thrifty phenotype hypothesis. Br Med Bull. 2001; 60, 5–20.CrossRefGoogle ScholarPubMed
192. Ayres, C, Portella, AK, Filion, F, Johnston, C, Silveira, PP. Correlation between intrauterine growth restriction (IUGR) and hedonic responses to a sucrose solution in newborn infants. Revista HCPA. 2010; 30.Google Scholar