Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-28T04:05:24.923Z Has data issue: false hasContentIssue false
  • English
  • Français

The fetal programming of food preferences: current clinical and experimental evidence

Part of: Ibero-American DOHaD

Published online by Cambridge University Press:  28 September 2015

R. Dalle Molle Open the ORCID record for R. Dalle Molle [Opens in a new window] ,
A. R. Bischoff Open the ORCID record for A. R. Bischoff [Opens in a new window] ,
A. K. Portella  and
P. P. Silveira Open the ORCID record for P. P. Silveira [Opens in a new window]
R. Dalle Molle
Affiliation:
Departamento de Pediatria, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
A. R. Bischoff
Affiliation:
Programa de Residência Médica em Pediatria, Hospital de Clínicas de Porto Alegre, Porto Alegre, Brazil
A. K. Portella
Affiliation:
Departamento de Pediatria da Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre, Brazil
P. P. Silveira*
Affiliation:
Departamento de Pediatria, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil Programa de Residência Médica em Pediatria, Hospital de Clínicas de Porto Alegre, Porto Alegre, 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

Increased energy consumption is one of the major factors implicated in the epidemic of obesity. There is compelling evidence, both clinical and experimental, that fetal paucity of nutrients may have programming effects on feeding preferences and behaviors that can contribute to the development of diseases. Clinical studies in different age groups show that individuals born small for their gestational age (SGA) have preferences towards highly caloric foods such as carbohydrates and fats. Some studies have also shown altered eating behaviors in SGA children. Despite an apparent discrepancy in different age groups, all studies seem to converge to an increased intake of palatable foods in SGA individuals. Small nutrient imbalances across lifespan increase the risk of noncommunicable diseases in adult life. Homeostatic factors such as altered responses to leptin and insulin and alterations in neuropeptides associated with appetite and satiety are likely involved. Imbalances between homeostatic and hedonic signaling are another proposed mechanism, with the mesocorticolimbic dopaminergic pathway having differential reward and pleasure responses when facing palatable foods. Early exposure to undernutrition also programs hypothalamic–pituitary–adrenal axis, with SGA having higher levels of cortisol in different ages, leading to chronic hyperactivity of this neuroendocrine axis. This review summarizes the clinical and experimental evidence related to fetal programming of feeding preferences by SGA.

Keywords

feeding behaviorfetal programmingfood preferencesIUGR
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 3: Themed Issue: Ibero-American DOHaD Society , June 2016 , pp. 222 - 230
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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.)

Footnotes

†

These two authors contributed equally to the work.

References

1. Barker, DJ, Lampl, M. Commentary: the meaning of thrift. Int J Epidemiol. 2013; 42, 1229–1230.CrossRefGoogle ScholarPubMed
2. Vickers, MH, Breier, BH, McCarthy, D, Gluckman, PD. Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol. 2003; 285, R271–R273.Google ScholarPubMed
3. Kaseva, N, Wehkalampi, K, Strang-Karlsson, S, et al. Lower conditioning leisure-time physical activity in young adults born preterm at very low birth weight. PLoS One. 2012; 7, e32430.CrossRefGoogle ScholarPubMed
4. 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.Google Scholar
5. El-Haddad, MA, Desai, M, Gayle, D, Ross, MG. In utero development of fetal thirst and appetite: potential for programming. J Soc Gynecol Invest. 2004; 11, 123–130.CrossRefGoogle ScholarPubMed
6. Ross, MG, Desai, M. Developmental programming of offspring obesity, adipogenesis, and appetite. Clin Obstet Gynecol. 2013; 56, 529–536.Google Scholar
7. Portella, AK, Silveira, PP. Neurobehavioral determinants of nutritional security in fetal growth-restricted individuals. Ann N Y Acad Sci. 2014; 1331, 15–33.Google Scholar
8. Portella, AK, Kajantie, E, Hovi, P, et al. Effects of in utero conditions on adult feeding preferences. J Dev Orig Hlth Dis. 2012; 3, 140–152.Google Scholar
9. Low, YQ, Lacy, K, Keast, R. The role of sweet taste in satiation and satiety. Nutrients. 2014; 6, 3431–3450.Google Scholar
10. Lampure, A, Deglaire, A, Schlich, P, et al. Liking for fat is associated with sociodemographic, psychological, lifestyle and health characteristics. Br J Nutr. 2014; 112, 1353–1363.Google Scholar
11. Legradi, G, Lechan, RM. The arcuate nucleus is the major source for neuropeptide Y-innervation of thyrotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology. 1998; 139, 3262–3270.CrossRefGoogle ScholarPubMed
12. Beaulieu, J, Champagne, D, Drolet, G. Enkephalin innervation of the paraventricular nucleus of the hypothalamus: distribution of fibers and origins of input. J Chem Neuroanat. 1996; 10, 79–92.Google Scholar
13. Marcus, JN, Aschkenasi, CJ, Lee, CE, et al. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol. 2001; 435, 6–25.CrossRefGoogle ScholarPubMed
14. Trivedi, P, Yu, H, MacNeil, DJ, Van der Ploeg, LH, Guan, XM. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett. 1998; 438, 71–75.CrossRefGoogle ScholarPubMed
15. Zamir, N, Skofitsch, G, Jacobowitz, DM. Distribution of immunoreactive melanin-concentrating hormone in the central nervous system of the rat. Brain Res. 1986; 373, 240–245.Google Scholar
16. Rodaros, D, Caruana, DA, Amir, S, Stewart, J. Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience. 2007; 150, 8–13.CrossRefGoogle Scholar
17. Sakanaka, M, Magari, S, Shibasaki, T, Inoue, N. Co-localization of corticotropin-releasing factor- and enkephalin-like immunoreactivities in nerve cells of the rat hypothalamus and adjacent areas. Brain Res. 1989; 487, 357–362.CrossRefGoogle ScholarPubMed
18. Kampe, J, Tschop, MH, Hollis, JH, Oldfield, BJ. An anatomic basis for the communication of hypothalamic, cortical and mesolimbic circuitry in the regulation of energy balance. Eur J Neurosci. 2009; 30, 415–430.CrossRefGoogle ScholarPubMed
19. Fadel, J, Deutch, AY. Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience. 2002; 111, 379–387.CrossRefGoogle ScholarPubMed
20. Beckstead, RM, Domesick, VB, Nauta, WJ. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 1979; 175, 191–217.CrossRefGoogle ScholarPubMed
21. Heimer, L, Zahm, DS, Churchill, L, Kalivas, PW, Wohltmann, C. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience. 1991; 41, 89–125.Google Scholar
22. Kita, H, Oomura, Y. Reciprocal connections between the lateral hypothalamus and the frontal complex in the rat: electrophysiological and anatomical observations. Brain Res. 1981; 213, 1–16.CrossRefGoogle ScholarPubMed
23. 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; 65, 215–220.Google Scholar
24. Stein, AD, Rundle, A, Wada, N, Goldbohm, RA, Lumey, LH. 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.Google Scholar
25. 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.Google Scholar
26. Perälä, MM, Männistö, S, Kaartinen, NE, et al. Body size at birth is associated with food and nutrient intake in adulthood. PLoS One. 2012; 7, e46139.Google Scholar
27. Kaseva, N, Wehkalampi, K, Hemiö, K, et al. Diet and nutrient intake in young adults born preterm at very low birth weight. J Pediatr. 2013; 163, 43–48.Google Scholar
28. Silveira, PP, Agranonik, M, Faras, H, et al. Preliminary evidence for an impulsivity-based thrifty eating phenotype. Pediatr Res. 2012; 71, 293–298.Google Scholar
29. Migraine, A, Nicklaus, S, Patricia, PP, et al. Effect of preterm birth and birth weight on eating behavior at 2 y of age. Am J Clin Nutr. 2013; 97, 1270–1277.Google Scholar
30. Oliveira, A, de Lauzon-Guillain, B, Jones, L, et al. Birth weight and eating behaviors of young children. J Pediatr. 2015; 166, 59–65.Google Scholar
31. Crume, TL, Scherzinger, A, Stamm, E, et al. The long-term impact of intrauterine growth restriction in a diverse U.S. cohort of children: the EPOCH study. Obesity. 2014; 22, 608–615.Google Scholar
32. Ayres, C, Agranonik, M, Portella, AK, et al. Intrauterine growth restriction and the fetal programming of the hedonic response to sweet taste in newborn infants. Int J Pediatr. 2012; 2012, 657379.Google Scholar
33. Rotstein, M, Stolar, O, Uliel, S, et al. Facial expression in response to smell and taste stimuli in small and appropriate for gestational age newborns. J Child Neurol. 2015; pii: 0883073815570153 [Epub ahead of print].Google Scholar
34. Laureano, DP, Molle, RD, Portella, AK, Silveira, PP. Facial expressions in small for gestational age newborns. J Child Neurol. 2015; pii: 0883073815592225 [Epub ahead of print].Google ScholarPubMed
35. Mucellini, ABM, Manfro, GG, Silveira, PP. Tackling obesity: challenges ahead. Lancet. 2015; 386, 740.Google Scholar
36. Desai, M, Gayle, D, Babu, J, Ross, MG. Programmed obesity in intrauterine growth-restricted newborns: modulation by. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R91–R96.Google Scholar
37. Desai, M, Gayle, D, Han, G, Ross, MG. Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reprod Sci. 2007; 14, 329–337.Google Scholar
38. George, LA, Zhang, L, Tuersunjiang, N, et al. Early maternal undernutrition programs increased feed intake, altered glucose metabolism and insulin secretion, and liver function in aged female offspring. Am J Physiol Regul Integr Comp Physiol. 2012; 302, R795–R804.Google Scholar
39. Dellschaft, NS, Alexandre-Gouabau, MC, Gardner, DS, et al. Effect of pre- and postnatal growth and post-weaning activity on glucose metabolism in the offspring. J Endocrinol. 2015; 224, 171–182.Google Scholar
40. Ovilo, C, Gonzalez-Bulnes, A, Benitez, R, et al. Prenatal programming in an obese swine model: sex-related effects of maternal energy restriction on morphology, metabolism and hypothalamic gene expression. Br J Nutr. 2014; 111, 735–746.Google Scholar
41. Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595–601.Google Scholar
42. Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. 1992. Int J Epidemiol. 2013; 42, 1215–1222.Google Scholar
43. Vickers, MH, Breier, BH, Cutfield, WS, Hofman, PL, Gluckman, PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 2000; 279, E83–E87.Google Scholar
44. Vickers, MH, Breier, BH, McCarthy, D, Gluckman, PD. Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol Regul Integr Comp Physiol. 2003; 285, R271–R273.Google Scholar
45. Bellinger, L, Lilley, C, Langley-Evans, SC. Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Br J Nutr. 2004; 92, 513–520.Google Scholar
46. Bellinger, L, Langley-Evans, SC. Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clin Sci. 2005; 109, 413–420.Google Scholar
47. Bellinger, L, Sculley, DV, Langley-Evans, SC. Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Int J Obes. 2006; 30, 729–738.Google Scholar
48. Cunha Fda, S, Dalle Molle, R, Portella, AK, et al. Both food restriction and high-fat diet during gestation induce low birth weight and altered physical activity in adult rat offspring: the ‘Similarities in the Inequalities’ model. PLoS One. 2015; 10, e0118586.Google Scholar
49. Alves, MB, Dalle Molle, R, Desai, M, Ross, MG, Silveira, PP. Increased palatable food intake and response to food cues in intrauterine growth-restricted rats are related to tyrosine hydroxylase content in the orbitofrontal cortex and nucleus accumbens. Behav Brain Res. 2015; 287, 73–81.CrossRefGoogle ScholarPubMed
50. Molle, RD, Laureano, DP, Alves, MB, et al. Intrauterine growth restriction increases the preference for palatable foods and affects sensitivity to food rewards in male and female adult rats. Brain Res. 2015; 1618, 41–49.Google Scholar
51. da Silva, AA, Borba, TK, de Almeida Lira, L, et al. Perinatal undernutrition stimulates seeking food reward. Int J Dev Neurosci. 2013; 31, 334–341.Google Scholar
52. de Melo Martimiano, PH, da Silva, GR, Coimbra, VF, et al. Perinatal malnutrition stimulates motivation through reward and enhances drd receptor expression in the ventral striatum of adult mice. Pharmacol Biochem Behav. 2015; 134, 106–114.Google Scholar
53. Vucetic, Z, Totoki, K, Schoch, H, et al. Early life protein restriction alters dopamine circuitry. Neuroscience. 2010; 168, 359–370.CrossRefGoogle ScholarPubMed
54. Grissom, NM, Reyes, TM. Gestational overgrowth and undergrowth affect neurodevelopment: similarities and differences from behavior to epigenetics. Int J Dev Neurosci. 2013; 31, 406–414.Google Scholar
55. Shin, BC, Dai, Y, Thamotharan, M, Gibson, LC, Devaskar, SU. Pre- and postnatal calorie restriction perturbs early hypothalamic neuropeptide and energy balance. J Neurosci Res. 2012; 90, 1169–1182.Google Scholar
56. Puglianiello, A, Germani, D, Cianfarani, S. Exposure to uteroplacental insufficiency reduces the expression of signal transducer and activator of transcription 3 and proopiomelanocortin in the hypothalamus of newborn rats. Pediatr Res. 2009; 66, 208–211.Google Scholar
57. Delahaye, F, Breton, C, Risold, PY, et al. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology. 2008; 149, 470–475.Google Scholar
58. Yousheng, J, Nguyen, T, Desai, M, Ross, MG. Programmed alterations in hypothalamic neuronal orexigenic responses to ghrelin following gestational nutrient restriction. Reprod Sci. 2008; 15, 702–709.Google Scholar
59. Remmers, F, Verhagen, LA, Adan, RA, Delemarre-van de Waal, HA. Hypothalamic neuropeptide expression of juvenile and middle-aged rats after early postnatal food restriction. Endocrinology. 2008; 149, 3617–3625.Google Scholar
60. Garcia, AP, Palou, M, Priego, T, et al. Moderate caloric restriction during gestation results in lower arcuate nucleus NPY- and alphaMSH-neurons and impairs hypothalamic response to fed/fasting conditions in weaned rats. Diabetes Obes Metab. 2010; 12, 403–413.Google Scholar
61. Plagemann, A, Harder, T, Rake, A, et al. Hypothalamic nuclei are malformed in weanling offspring of low protein malnourished rat dams. J Nutr. 2000; 130, 2582–2589.Google Scholar
62. Fukami, T, Sun, X, Li, T, Desai, M, Ross, MG. Mechanism of programmed obesity in intrauterine fetal growth restricted offspring: paradoxically enhanced appetite stimulation in fed and fasting states. Reprod Sci. 2012; 19, 423–430.Google Scholar
63. Desai, M, Li, T, Ross, MG. Fetal hypothalamic neuroprogenitor cell culture: preferential differentiation paths induced by leptin and insulin. Endocrinology. 2011; 152, 3192–3201.Google Scholar
64. Desai, M, Li, T, Ross, MG. Hypothalamic neurosphere progenitor cells in low birth-weight rat newborns: neurotrophic effects of leptin and insulin. Brain Res. 2011; 1378, 29–42.Google Scholar
65. Orozco-Solis, R, Matos, RJ, Guzman-Quevedo, O, et al. Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus. PLoS One. 2010; 5, e13537.Google Scholar
66. Ross, MG, Desai, M. Developmental programming of appetite/satiety. Ann Nutr Metab. 2014; 64(Suppl. 1), 36–44.CrossRefGoogle ScholarPubMed
67. Smith, JW, Fetsko, LA, Xu, R, Wang, Y. Dopamine D2L receptor knockout mice display deficits in positive and negative reinforcing properties of morphine and in avoidance learning. Neuroscience. 2002; 113, 755–765.Google Scholar
68. Kademian, S, Perez, MF, Keller, EA. Perinatal undernutrition: changes in brain opiate receptor density. Nutr Neurosci. 2002; 5, 53–57.Google Scholar
69. Vieau, D, Sebaai, N, Leonhardt, M, et al. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology. 2007; 32(Suppl. 1), S16–S20.Google Scholar
70. Lesage, J, Blondeau, B, Grino, M, Breant, B, Dupouy, JP. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology. 2001; 142, 1692–1702.Google Scholar
71. Reis, RS, Bernardi, JR, Steiner, M, et al. Poor infant inhibitory control predicts food fussiness in childhood – a possible protective role of n-3 PUFAs for vulnerable children. Prostaglandins Leukot Essential Fatty Acids. 2015; 97, 21–25.Google Scholar
72. Escobar, RS, O’Donnell, KA, Colalillo, S, et al. Better quality of mother-child interaction at 4 years of age decreases emotional overeating in IUGR girls. Appetite. 2014; 81, 337–342.CrossRefGoogle ScholarPubMed
73. Braga, CL, Farias, BL, Reis, RS, Agranonik, M, Silveira, PP. Musical intervention and food preferences in girls born with lower birth weight. Early Hum Dev. 2015; http://dx.doi.org/10.1016/j.earlhumdev.2015.08.004.Google Scholar
74. Portella, AK, Silveira, PP. Parenting: roots of the sweet tooth. Science. 2014; 345, 1571–1572.CrossRefGoogle ScholarPubMed