Perinatal programming effects on feeding behavior

Authors

  • Ana Patricia Zepeda Salvador Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico https://orcid.org/0000-0003-2909-8649
  • Ana Cristina Espinoza Gallardo Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico https://orcid.org/0000-0002-0882-0914
  • Dalila Betsabee Meza Rodríguez Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico https://orcid.org/0000-0003-0683-0067
  • Yadira Vianet Martínez Vázquez Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico https://orcid.org/0000-0002-1311-7836
  • Aida Gabriela Anaya Flores Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico https://orcid.org/0009-0006-0761-3506
  • Sofía Castro Botero Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico
  • Fernando Chávez Corona Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico https://orcid.org/0009-0004-1836-319X
  • Jorge Adalberto Ramos López Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico
  • Berenice Sánchez Caballero Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico
  • Alma Gabriela Martínez Moreno Instituto de Investigaciones en Comportamiento Alimentario y Nutrición, Universidad de Guadalajara, Mexico https://orcid.org/0000-0002-7495-1007

DOI:

https://doi.org/10.32870/jbf.v4i8.67

Keywords:

feeding behavior, hyperphagia, diet, obesity, perinatal programming

Abstract

To address the growing prevalence of obesity and its associated metabolic consequences, it is essential to understand the evolutionary origins of health and disease. Current evidence attributes the rise in obesity to environmental factors, such as the Western diet and unhealthy lifestyles. However, this review argues that adverse conditions during early developmental stages significantly influence adult health outcomes. It has been proposed that an adverse perinatal environment triggers adaptive physiological changes that ensure fetal survival but simultaneously increase the long-term risk of chronic diseases. In addition to structural and functional alterations in the organism, changes in feeding behavior have been identified and linked to the presence of chronic non-communicable diseases. This narrative review aims to present the last half century’s worth of evidence regarding the impact of in-utero environmental changes on eating behavior within the framework of perinatal programming theory.

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References

Aguayo-Guerrero, J. A., León-Cabrera, S., & Escobedo, G. (2023). Molecular mechanisms involved in fetal programming and disease origin in adulthood. Journal of Pediatric Endocrinology and Metabolism, 36(7), 615-627. http://doi.org/10.1515/jpem-2022-0491

Barbero, A., Astiz, S., Ovilo, C., Lopez-Bote, C. J., Perez-Solana, M. L., Ayuso, M., Garcia-Real, I., & Gonzalez-Bulnes, A. (2014). Prenatal programming of obesity in a swine model of leptin resistance: Modulatory effects of controlled postnatal nutrition and exercise. Journal of Developmental Origins of Health and Disease, 5, 248-258. http://doi.org/10.1017/S2040174414000208

Barker, D. J. P. (1990). The fetal and infant origins of adult disease. BMJ, 301, 1111. http://doi.org/10.1136/bmj.301.6761.1111

Barker, D. J. P. (2004). The developmental origins of chronic adult disease. Acta Paediatrica, 93, 26-33. http://doi.org/10.1080/08035320410022730

Bayol, S. A., Farrington, S. J., & Stickland, N. C. (2007). 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. British Journal of Nutrition, 98, 843-851. http://doi.org/10.1017/S0007114507812037

Bellinger, L, Sculley, D. V, & Langley-Evans, S. C. (2006). Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. International Journal of Obesity, 30, 729-738. http://doi.org/10.1038/sj.ijo.0803205

Bellinger, L., & Langley-Evans, S. C. (2005). Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clinical Science, 109, 413-420. http://doi.org/10.1042/CS20050127

Bellinger, L., Lilley, C., & Langley-Evans, S. C. (2004). Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. British Journal of Nutrition, 92, 513. http://doi.org/10.1079/BJN20041224

Breier, B. H., Vickers, M. H., Ikenasio, B. A., Chan, K. Y., & Wong, W. P. S. (2001). Fetal programming of appetite and obesity. Molecular and Cellular Endocrinology, 185, 73–79. http://doi.org/10.1016/S0303-7207(01)00634-7

Camacho-Morales, A., Caballero-Benitez, A., Vázquez-Cruz, E., Maldonado-Ruíz, R., Cardenas-Tueme, M., Rojas-Martínez, A., & Caballero-Hernández, D. (2022). Maternal programming by high-energy diets primes ghrelin sensitivity in the offspring of ras exposed to chronic immobilization stress. Nutrition Research, 107, 37-47. https://doi.org/10.1016/j.nutres.2022.08.007

Colombo, J., Gustafson, K. M., & Carlson, S. E. (2019). Critical and sensitive periods in development and nutrition. Annals of Nutrition and Metabolism, 75, 34-42. https://doi.org/10.1159/000508053.

Cripps, R. L., Martin-Gronert, M. S., & Ozanne, S. E. (2005). Fetal and perinatal programming of appetite. Clinical Science, 109, 1-11. http://doi.org/10.1042/CS20040367

Da Silva Cunha, F., Dalle Molle, R., Portella, A. K., Da Silva Benetti, C., Noschang, C., Goldani, M. Z., & Silveira, P. P. (2015). 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, 10, 1-18. http://doi.org/10.1371/journal.pone.0118586

Dalle Molle, R., Laureano, D. P., Alves, M. B., Reis, T. M., Desai, M., Ross, M. G., & Silveira, P. P. (2015). Intrauterine growth restriction increases the preference for palatable foods and affects sensitivity to food rewards in male and female adult rats. Brain Research, 1618, 41-49. http://doi.org/10.1016/j.brainres.2015.05.019

de Boo, H. A., & Harding, J. E. (2006). The developmental origins of adult disease (Barker) hypothesis. Australian and New Zealand Journal of Obstetrics Gynaecology, 46(1), 4-14. http://doi.org/10.1111/j.1479-828X.2006.00506.x

De Moura, E. G., & Passos, M. C. F. (2005). Neonatal programming of body weight regulation and energetic metabolism. Bioscience Reports, 25, 251-269. http://doi.org/10.1007/s10540-005-2888-3

De Oliveira, J. C., Grassiolli, S., Gravena, C., & De Mathias, P. C. F. (2012). Early postnatal low-protein nutrition, metabolic programming and the autonomic nervous system in adult life. Nutrition and Metabolism, 9, 1-8. http://doi.org/10.1186/1743-7075-9-80

Desai, M., Gayle, D., Han, G., & Ross, M. G. (2007). Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reproductive Sciences, 14, 329-337. http://doi.org/10.1177/1933719107303983

Desai, M., & Hales, C. N. (1997). Role of fetal and infant growth in programming metabolism in later life. Biological Reviews of the Cambridge Philosophical Society, 72, 329-348. http://doi.org/10.1017/S0006323196005026

Dötsch, J., Alejandre-Alcazar, M., Janoschek, R., Nüsken, E., Weber, L. T., & Nüsken, K. D. (2016). Perinatal programming of renal function. Current Opinion in Pediatrics, 28(2), 188-94. http://doi.org/10.1097/MOP.0000000000000312

Drake, A. J., Walker, B. R., & Seckl, J. R. (2005). Intergeneracional consequences of fetal programming by in utero exposure to glucocorticoids in rats. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 288, 34-38. http://doi.org/10.1152/ajpregu.00106.2004

Erhuma, A., Bellinger, L., Langley-Evans, S. C., & Bennett, A. J. (2007). Prenatal exposure to undernutrition and programming of responses to high-fat feeding in the rat. British Journal of Nutrition, 98, 517. http://doi.org/10.1017/S0007114507721505

Fowden, A. L. (2006). Intrauterine programming of physiological systems: Causes and consequences. Physiology, 21, 29-37. https://org/10.1152/physiol.00050.2005

Fowden, A. L., Forhead, A. J., Coan, P. M., & Burton, G. J. (2008). The placenta and intrauterine programming. Journal of Neuroendocrinology, 20, 439-450. http://doi.org/10.1111/j.1365-2826.2008.01663.x

Galjaard, S., Devlieger, R., & Van Assche, F. A. (2013) Fetal growth and developmental programming. Journal of Perinatal Medicine, 41(1), 101-105. http://doi.org/10.1515/jpm-2012-0020

Godfrey, K. M., & Barker, D. J. (2001). Fetal programming and adult health. Public Health Nutrition, 4. http://doi.org/10.1079/PHN2001145

Grigore, D., Ojeda, N. B., & Alexander, B. T. (2008). Sex differences in the fetal programming of cardiovascular disease. Gender Medicine, 5, 121-132. http://doi.org/10.1016/j.genm.2008.03.012

Hales, C. N., & Barker, D. J. P. (2001). The thrifty phenotype hypothesis: Type 2 diabetes. British Medical Bulletin, 60, 5-20. http://doi.org/10.1093/bmb/60.1.5

Han, W., Song, Z., Shan, D., & Shi, Q. (2023). Fetal origins of obesity: a novel pathway of regulating appetite neurons in the hypothalamus of growth-restricted rat offspring. Archives of Gynecology and Obstetrics, 309(6), 2411-2419. http://doi.org/10.1007/s00404-023-07108-3.

Hong, J. Y. (2022). Developmental programming by perinatal glucocorticoids. Molecules and Cells, 45(10), 685-691. http://doi.org/10.14348/molcells.2022.0042

Jones, J. E., Jurgens, J. A., Evans, S. A., Ennis, R. C., Villar, V. A. M., & Jose, P. A. (2012). Mechanisms of fetal programming in hypertension. International Journal of Pediatrics, 2012(1), 584831. http://doi.org/10.1155/2012/584831

Kulhanek, D., Abrahante Llorens, J. E., Buckley, L., Tkac, I., Rao, R., & Paulsen, M. E. (2022). Female and male C57BL/6J offspring exposed to maternal obesogenic diet develop altered hypothalamic energy metabolism in adulthood. American Journal of Physiology-Endocrinology and Metabolism, 323(5), E448-E466. http://doi.org/10.1152/ajpendo.00100.2022

Langley-Evans, S. C. (2009). Nutritional programming of disease: Unravelling the mechanism. Journal of Anatomy, 215, 36-51. http://doi.org/10.1111/j.1469-7580.2008.00977.x

Langley-Evans, S. C., Bellinger, L., & McMullen, S. (2005). Animal models of programming: Early life influences on appetite and feeding behaviour. Maternal and Child Nutrition, 1, 142-148. http://doi.org/10.1111/j.1740-8709.2005.00015.x

Lesage, J., Del-Favero, F., Leonhardt, M., Louvart, H., Maccari, S., Vieau, D., & Darnaudery, M. (2004). Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. Journal of Endocrinology, 181, 291-296. http://doi.org/10.1677/joe.0.1810291

López, M., Seoane, L. M., Tovar, S., García, M. C., Nogueiras, R., Diéguez, C., & Señarís, R. M. (2005). A posible role of neuropeptide Y, agouti-related protein and leptin receptor isoforms in hypothalamic programming. Diabetologia, 48, 140-148. http://doi.org/10.1007/s00125-004-1596-z

Micho?ska, I., ?uszczki, E., Zieli?ska, M., Oleksy, ?., Stolarczyk, A., & Dere?, K. (2022). Nutritional programming: History, hypotheses, and the role of prenatal factors in the prevention of metabolic diseases - a narrative review. Nutrients, 14(20), 4422. http://doi.org/ 10.3390/nu14204422.

Miles, J. L., Landon, J., Davison, M., Krägeloh, C. U., Thompson, N. M., Triggs, C. M., & Breier, B. H. (2009). Prenatally undernourished rats show increased preference for wheel running v. lever pressing for food in a choice task. British Journal of Nutrition, 101, 902-908. http://doi.org/10.1017/S0007114508043353

Nathanielsz, P. W. (2006). Animal models that elucidate basic principles of the developmental origins of adult diseases. ILAR Journal, 47, 73–82. http://doi.org/10.1093/ILAR.47.1.73

Ong, Z. Y., & Muhlhausler, B. S. (2014). Consuming a low-fat diet from weaning to adulthood reverses the programming of food preferences in male, but not in female, offspring of ’junk food’-fed rat dams. Acta Physiologica, 210, 127-141. http://doi.org/10.1111/apha.12132

Orozco-Sólis, R., Lopes de Souza, S., Barbosa Matos, R. J., Grit, I., Le Bloch, J., Nguyen, P., Manhães de Castro, R., & Bolaños-Jiménez, F. (2009). Perinatal undernutrition-induced obesity is independent of the developmental programming of feeding. Physiology and Behavior, 96, 481-492. http://doi.org/10.1016/j.physbeh.2008.11.016

Oscai, L. B., & McGarr, J. A. (1978). Evidence that the amount of food consumed in early life fixes appetite in the rat. The American Journal of Physiology, 235, 141-144. http://doi.org/10.1152/ajpregu.1978.235.3.R141

Passos, M. C. da F., Ramos, C. da F., Teixeira, C. V., & De Moura, E. G. (2001). Comportamento alimentar de ratos adultos submetidos à restrição protéica cujas mães sofreram desnutrição durante a lactação. Revista de Nutricao, 14, 7-11. http://doi.org/10.1590/S1415-52732001000400002

Pecorelli, R. (1997). Elementos Básicos de Psicología. Trillas.

Plageman, A., Heidrich, I., Götz, F., Rohde, W., & Dörner, G. (1992). Obesity and enhanced diabetes and cardiovascular risk in adult rats due to early postnatal overfeeding. Experimental and Clinical Endocrinology, 99, 154-158. http://doi.org/10.1055/s-0029-1211159

Portella, A. K., Kajantie, E., Hovi, P., Desai, M., Ross, M. G., Goldani, M. Z., Roseboom, T. J., & Silveira, P. P. (2012). Effects of in utero conditions on adult feeding preferences. Journal of Developmental Origins of Health and Disease, 3, 140-152. http://doi.org/10.1017/S2040174412000062

Ravelli, G.-P., Stein, Z., & Susser, M. (1976). Obesity in young men after famine exposure in utero and early infancy. New England Journal of Medicine, 295, 349-353. http://doi.org/10.1056/NEJM197608122950701

Remmers, F., Fodor, M., & Delemarre-van de Waal, H. A. (2008). Neonatal food restriction permanently alters rat body dimensions and energy intake. Physiology and Behavior, 95, 208-215. http://doi.org/10.1016/j.physbeh.2008.05.021

Schredelseker, T., Veit, F., Dorsky, R. I., & Driever, W. (2020). Bsx is essential for differentiation of multiple neuromodulatory cell populations in the secondary prosencephalon. Frontiers in Neuroscience, 14, 525. http://doi.org/10.3389/fnins.2020.00525.

Sefcikova, Z., & Mozes, S. (2002). Effect of early nutritional experience on the feeding behaviour of adult female rats. Veterinary Medicine, 47, 315-322. http://doi.org/10.17221/5841-VETMED

Silveira, P. P., Portella, A. K., & Goldani, M. Z. (2007). Developmental origins of health and disease (DOHaD). Jornal de Pediatria, 83, 494-504. http://doi.org/10.2223/JPED.1728

Simmons, R. A., Templeton, L. J., & Gertz, S. J. (2001). Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes, 50, 2279-2286. http://doi.org/10.2337/diabetes.50.10.2279

Skowronski, A. A., Leibel, R. L., & LeDuc, C. A. (2024). Neurodevelopmental programming of adiposity, contributions to obesity risk. Endocrine Reviews, 45, 253-280. https://doi.org/10.1210/endrev/bnad031

Smart, J. L., & Dobbing, J. (1977). Increased thirst and hunger in adult rats undernourished as infants: an alternative explanation. The British Journal of Nutrition, 37, 421-430. http://doi.org/10.1079/BJN19770045

Tarry-Adkins, J. L., & Ozanne, S. E. (2011). Mechanisms of early life programming: current knowledge and. American Journal of Clinical Nutrition, 94, 1765-1771. http://doi.org/10.3945/ajcn.110.000620.1

Vickers, M. H., Breier, B. H., Cutfield, W. S., Hofman, P. L., Gluckman, P. D., Amiel, S., Caprio, S., Sherwin, R., Plewe, G., Haymond, M., Tamborlane, W., Amiel, S., Sherwin, R., Simonson, D., Anderson, E., Mark, A., Barker, D., Barker, D., Barker, D., … Gluckman, P. (2000). Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. American Journal of Physiology. Endocrinology and Metabolism, 279, 83-87. http://doi.org/10.1210/jcem-72-2-277

Warren, M. A, & Bedi, K. S. (1985). The effects of a lengthy period of undernutrition on food intake and on body and organ growth during rehabilitation. Journal of Anatomy, 141, 65-75.

Widdowson, E. M., & McCance, R. A. (1963). The effect of finite periods of undernutrition at different ages on the composition and subsequent development of the rat. Proceedings of the Royal Society of London. Series B, 158, 329-342. http://doi.org/10.1098/rspb.1963.0051

Zambrano, E., Guzmán, C., Rodríguez-González, G. L., Durand-Carbajal, M., & Nathanielsz P. W. (2014). Fetal programming of sexual development and reproductive function. Molecular and Cellular Endocrinology, 382(1), 538-549. http://doi.org/10.1016/j.mce.2013.09.008

Published

2025-01-30

How to Cite

Zepeda Salvador, Ana Patricia, Ana Cristina Espinoza Gallardo, Dalila Betsabee Meza Rodríguez, Yadira Vianet Martínez Vázquez, Aida Gabriela Anaya Flores, Sofía Castro Botero, Fernando Chávez Corona, Jorge Adalberto Ramos López, Berenice Sánchez Caballero, and Alma Gabriela Martínez Moreno. 2025. “Perinatal Programming Effects on Feeding Behavior”. Journal of Behavior and Feeding 4 (8):28-33. https://doi.org/10.32870/jbf.v4i8.67.

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