Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-28T07:17:26.838Z Has data issue: false hasContentIssue false

Repercussions of maternal exposure to high-fat diet on offspring feeding behavior and body composition: a systematic review

Published online by Cambridge University Press:  27 April 2020

Wenicios Ferreira Chaves
Affiliation:
Graduate Program of Nutrition, Department of Nutrition, Universidade Federal de Pernambuco, Recife, PE50670-901, Brazil
Isabeli Lins Pinheiro
Affiliation:
Physical Education and Sports Sciences Nucleus, Universidade Federal de Pernambuco, Vitória de Santo Antão, PE55608-680, Brazil
Jacqueline Maria da Silva
Affiliation:
Graduate Program of Nutrition, Department of Nutrition, Universidade Federal de Pernambuco, Recife, PE50670-901, Brazil
Raul Manhães-de-Castro
Affiliation:
Graduate Program of Nutrition, Department of Nutrition, Universidade Federal de Pernambuco, Recife, PE50670-901, Brazil
Raquel da Silva Aragão*
Affiliation:
Graduate Program of Nutrition, Department of Nutrition, Universidade Federal de Pernambuco, Recife, PE50670-901, Brazil Physical Education and Sports Sciences Nucleus, Universidade Federal de Pernambuco, Vitória de Santo Antão, PE55608-680, Brazil Graduate Program of Nutrition, Physical Activity and Phenotypic Plasticity, Universidade Federal de Pernambuco, Vitória de Santo Antão, PE55608-680, Brazil
*
Address for correspondence: Raquel da Silva Aragão, Núcleo de Educação Física e Ciências do Esporte, Centro Acadêmico de Vitória, Universidade Federal de Pernambuco, Rua Alto do Reservatório, s/n, Bela Vista, Vitória de Santo Antão, PE55608-680, Brazil. Email: [email protected]

Abstract

Maternal nutrition is an environmental determinant for offspring growth and development, especially in critical periods. Nutritional imbalances during these phases can promote dysregulations in food intake and feeding preference in offspring, affecting body composition. The aim of this review is to summarize and discuss the effects of maternal high-fat diet (HFD) on offspring feeding behavior and body composition. A search was performed in the PUBMED, SCOPUS, Web of Science, and LILACS databases. Inclusion criteria were studies in rodents whose mothers were submitted to HFD that assessed outcomes of food or caloric intake on offspring and food preference associated or not with body weight or body composition analysis. At the end of the search, 17 articles with the proposed characteristics were included. In these studies, 15 articles manipulated diet during pregnancy and lactation, 1 during pregnancy only, and 1 during lactation only. Maternal exposure to a HFD leads to increased food intake, increased preference for HFDs, and earlier food independence in offspring. The offspring from HFD mothers present low birthweight but become heavier into adulthood. In addition, these animals also exhibited greater fat deposition on white adipose tissue pads. In conclusion, maternal exposure to HFD may compromise parameters in feeding behavior and body composition of offspring, impairing the health from conception until adulthood.

Type
Review
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

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

Liu, CM, Kanoski, SE. Homeostatic and non-homeostatic controls of feeding behavior: distinct vs. Common neural systems. Physiol Behav. 2018; 193, 223231.CrossRefGoogle ScholarPubMed
Gahagan, S. Development of eating behavior: Biology and context. J Dev Behav Pediatr. 2012; 33, 261271.CrossRefGoogle Scholar
Roh, E, Kim, M-S. Brain regulation of energy metabolism. Endocrinol Metab. 2016; 31, 519524.CrossRefGoogle ScholarPubMed
Elizondo-Vega, RJ, Recabal, A, Oyarce, K. Nutrient sensing by hypothalamic tanycytes. Front Endocrinol. 2019; 10, 18.CrossRefGoogle ScholarPubMed
Redinger, RN. The pathophysiology of obesity and its clinical manifestations. Gastroenterol Hepatol. 2007; 3, 856863.Google ScholarPubMed
Müller, MJ, Geisler, C. Defining obesity as a disease. Euro J Clin Nutr. 2017; 71, 12561258.CrossRefGoogle ScholarPubMed
Bentham, J, Di Cesare, M, Bilano, V, et al. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet. 2017; 390, 26272642.Google Scholar
Cordain, L, Eaton, SB, Sebastian, A, et al. Origins and evolution of the Western diet: health plications for the 21st century. Am J Clin Nutr. 2005; 81, 341354.CrossRefGoogle Scholar
Genius, JS. Nutritional transition: a determinant of global health. J Epidemiol Community Health 2005; 59, 615616.CrossRefGoogle Scholar
Fox, A, Feng, W, Asal, V. What is driving global obesity trends? Globalization or ‘modernization’? Global Health 2019; 15, 116.CrossRefGoogle ScholarPubMed
Márquez-Valadez, et al. Maternal diabetes and fetal programming toward neurological diseases: beyond neural tube defects. Front Endocrinol (Lausanne). 2018; 9, 110.CrossRefGoogle ScholarPubMed
Jones, JE, Jurgens, JA, Evans, SA, et al. Mechanisms of Fetal Programming in Hypertension. Int J Pediatr. 2012; 2012, 17.CrossRefGoogle ScholarPubMed
Alfaradhi, MZ, Ozanne, SE. Developmental programming in response to maternal overnutrition. Front Genet. 2011; 2, 113.CrossRefGoogle ScholarPubMed
Sullivan, E, Smith, MS, Grove, KL. Perinatal exposure to high-fat diet programs energy balance, metabolism and behavior in adulthood. Neuroendocrinology. 2011; 93, 18.CrossRefGoogle ScholarPubMed
Desai, M, Hales, CN. Role of Fetal and Infant Growth in Programming Metabolism in Later Life. Biol Rev Camb Philos Soc. 1997; 72, 329348.CrossRefGoogle ScholarPubMed
Morgane, PJ, Austin-LaFrance, R, Bronzino, J, et al. Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev. 1993; 17, 91128.CrossRefGoogle ScholarPubMed
Siddeek, B, Mauduit, C, Chehade, H, et al. Long-term impact of maternal high-fat diet on offspring cardiac health: role of micro-RNA biogenesis. Cell Death Discov. 2019; 5, 114.CrossRefGoogle ScholarPubMed
Glendining, KA, Fisher, LC, Jasoni, CL. Maternal high fat diet alters offspring epigenetic regulators, amygdala glutamatergic profile and anxiety. Psychoneuroendocrinology. 2018; 96, 132141.CrossRefGoogle ScholarPubMed
Sullivan, EL, Nousen, EK, Chamlou, KA, et al. The impact of maternal high-fat diet consumption on neural development and behavior of offspring. Int J Obes Suppl. 2012; 2, S7S13.CrossRefGoogle ScholarPubMed
Chang, GQ, Gaysinskaya, V, Karatayev, O, et al. Maternal high-fat diet and fetal programming: Increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci. 2008; 28, 1210712119.CrossRefGoogle ScholarPubMed
Hooijmans, CR, Rovers, MM, De Vries, RBM, et al. SYRCLE’ s risk of bias tool for animal studies. BMC Med Res Methodol. 2014; 14, 19.CrossRefGoogle ScholarPubMed
Landis, JR, Koch, GG. The measurement of observer agreement for categorical data. Biometrics. 1977; 33, 159174.CrossRefGoogle ScholarPubMed
Camacho, A, Montalvo-Martinez, L, Cardenas-Perez, RE, et al. Obesogenic diet intake during pregnancy programs aberrant synaptic plasticity and addiction-like behavior to a palatable food in offspring. Behav Brain Res. 2017; 330, 4655.CrossRefGoogle ScholarPubMed
Cardenas-Perez, RE, Fuentes-Mera, L, De La Garza, AL, et al. Maternal overnutrition by hypercaloric diets programs hypothalamic mitochondrial fusion and metabolic dysfunction in rat male offspring. Nutr Metab. 2018; 15, 116.CrossRefGoogle ScholarPubMed
Lemes, SF, de Souza, ACP, Payolla, TB, et al. Maternal consumption of high-fat diet in mice alters hypothalamic notch pathway, NPY cell population and food intake in offspring. Neuroscience. 2018; 371, 115.CrossRefGoogle ScholarPubMed
Melo, AM, Benatti, RO, Ignacio-Souza, LM, et al. Hypothalamic endoplasmic reticulum stress and insulin resistance in offspring of mice dams fed high-fat diet during pregnancy and lactation. Metabolism. 2014; 63, 682692.CrossRefGoogle ScholarPubMed
Rahman, TU, Ullah, K, Ke, Z-H, et al. Hypertriglyceridemia in female rats during pregnancy induces obesity in male offspring via altering hypothalamic leptin signaling. Oncotarget. 2017; 8, 5345053464.CrossRefGoogle ScholarPubMed
Reynolds, CM, Segovia, SA, Zhang, XD, et al. Conjugated Linoleic acid supplementation during pregnancy and lactation reduces maternal high-fat-diet-induced programming of early-onset puberty and hyperlipidemia in female rat offspring. Biol Reprod. 2015; 92, 110.CrossRefGoogle ScholarPubMed
Segovia, SA, Vickers, MH, Gray, C, et al. Conjugated linoleic acid supplementation improves maternal high fat diet-induced programming of metabolic dysfunction in adult male rat offspring. Sci Rep. 2017; 7, 111.CrossRefGoogle ScholarPubMed
Kozak, R, Mercer, JG, Burlet, A, et al. Hypothalamic neuropeptide Y content and mRNA expression in weanling rats subjected to dietary manipulations during fetal and neonatal life. Regul Pept. 1998; 75–76, 397402.CrossRefGoogle ScholarPubMed
Peleg-Raibstein, D, Sarker, G, Litwan, K, et al. Enhanced sensitivity to drugs of abuse and palatable foods following maternal overnutrition. Transl Psychiatry. 2016; 6, e911.CrossRefGoogle ScholarPubMed
Treesukosol, Y, Sun, B, Moghadam, AA, et al. Maternal high-fat diet during pregnancy and lactation reduces the appetitive behavioral component in female offspring tested in a brief-access taste procedure. Am J Physiol Integr Comp Physiol. 2014; 306, R499R509.CrossRefGoogle Scholar
Tsuduki, T, Yamamoto, K, Shuang, E, et al. High dietary fat intake during lactation promotes the development of social stress-induced obesity in the offspring of mice. Nutrients. 2015; 7, 59165932.CrossRefGoogle ScholarPubMed
Turdi, S, Ge, W, Hu, N, et al. Interaction between maternal and postnatal high fat diet leads to a greater risk of myocardial dysfunction in offspring via enhanced lipotoxicity, IRS-1 serine phosphorylation and mitochondrial defects. J Mol Cell Cardiol. 2013; 55, 117129.CrossRefGoogle ScholarPubMed
Volpato, AM, Schultz, A, Magalhães-Da-Costa, E, et al. Maternal high-fat diet programs for metabolic disturbances in offspring despite leptin sensitivity. Neuroendocrinology. 2012; 96, 272284.CrossRefGoogle ScholarPubMed
Yokomizo, H, Inoguchi, T, Sonoda, N, et al. Maternal high-fat diet induces insulin resistance and deterioration of pancreatic β-cell function in adult offspring with sex differences in mice. Am J Physiol Metab. 2014; 306, E1163E1175.Google ScholarPubMed
Kojima, S, Catavero, C, Rinaman, L. Maternal high-fat diet increases independent feeding in pre-weanling rat pups. Physiol Behav. 2016; 157, 237245.CrossRefGoogle ScholarPubMed
Nakashima, Y. Ratio of high-fat diet intake of pups nursed by dams fed combination diet was lower than that of pups nursed by dams fed high-fat or low-fat diet. J Nutr Sci Vitaminol (Tokyo). 2008; 53, 117123.CrossRefGoogle Scholar
Sun, B, Liang, N-C, Ewald, ER, et al. Early postweaning exercise improves central leptin sensitivity in offspring of rat dams fed high-fat diet during pregnancy and lactation. Am J Physiol Integr Comp Physiol. 2013; 305, R1076R1084.CrossRefGoogle ScholarPubMed
Bae-Gartz, I, Janoschek, R, Breuer, S, et al. Maternal obesity alters neurotrophin-associated MAPK signaling in the hypothalamus of male mouse offspring. Front Neurosci. 2019; 13, 117.CrossRefGoogle ScholarPubMed
Murabayashi, N, Sugiyama, T, Zhang, L, et al. Maternal high-fat diets cause insulin resistance through inflammatory changes in fetal adipose tissue. Eur J Obstet Gynecol Reprod Biol. 2013; 169, 3944.CrossRefGoogle ScholarPubMed
Mendes, NF, Kim, YB, Velloso, LA, et al. Hypothalamic microglial activation in obesity: A mini-review. Front Neurosci. 2018; 12, 18.CrossRefGoogle ScholarPubMed
Kim, DW, Young, SL, Grattan, DR, et al. Obesity during pregnancy disrupts placental morphology, cell proliferation, and inflammation in a sex-specific manner across gestation in the mouse1. Biol Reprod. 2014; 90, 111.CrossRefGoogle Scholar
Yang, X, Li, M, Haghiac, M, et al. Causal relationship between obesity-related traits and TLR4-driven responses at the maternal–fetal interface. Diabetologia. 2016; 59, 24592466.CrossRefGoogle ScholarPubMed
Dias-Rocha, CP, Almeida, MM, Santana, EM, et al. Maternal high-fat diet induces sex-specific endocannabinoid system changes in newborn rats and programs adiposity, energy expenditure and food preference in adulthood. J Nutr Biochem. 2018; 51, 5668.CrossRefGoogle ScholarPubMed
Ramírez-López, MT, Arco, R, Decara, J, et al. Exposure to a highly caloric palatable diet during the perinatal period affects the expression of the endogenous cannabinoid system in the brain, liver and adipose tissue of adult rat offspring. PLoS One. 2016; 11, 132.CrossRefGoogle ScholarPubMed
Reyes, TM. High-fat diet alters the dopamine and opioid systems: effects across development. Int J Obes Suppl. 2012; 2, S25S28.CrossRefGoogle ScholarPubMed
Vucetic, Z, Kimmel, J, Totoki, K, et al. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology. 2010; 151, 47564764.CrossRefGoogle ScholarPubMed
Bloomfield, FH, Spiroski, AM, Harding, JE. Fetal growth factors and fetal nutrition. Semin Fetal Neonatal Med. 2013; 18, 118123.CrossRefGoogle ScholarPubMed
Frias, AE, Morgan, TK, Evans, AE, et al. Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition. Endocrinology 2011; 152, 24562464.CrossRefGoogle Scholar
Harmon, AC, Cornelius, DC, Amaral, LM, et al. The role of inflammation in the pathology of preeclampsia. Clin Sci. 2016; 130, 409419.CrossRefGoogle Scholar
Hayes, EK, Lechowicz, A, Petrik, JJ, et al. Adverse fetal and neonatal outcomes associated with a life-long high fat diet: Role of altered development of the placental vasculature. PLoS One 2012; 7, e33370.CrossRefGoogle ScholarPubMed
Meijnikman, AS, Gerdes, VE, Nieuwdorp, M, et al. Placental lipid processing in response to a maternal high-fat diet and diabetes in rats. Pediatr Res. 2018; 83, 133153.Google Scholar
Liang, X, Yang, Q, Zhang, L, et al. Maternal high-fat diet during lactation impairs thermogenic function of brown adipose tissue in offspring mice. Sci Rep. 2016; 6, 112.CrossRefGoogle ScholarPubMed
Khamoui, A V., Desai, M, Ross, MG, et al. Sex-specific effects of maternal and postweaning high-fat diet on skeletal muscle mitochondrial respiration. J Dev Orig Health Dis. 2018; 9, 670677.CrossRefGoogle ScholarPubMed
Borengasser, SJ, Faske, J, Kang, P, et al. In utero exposure to prepregnancy maternal obesity and postweaning high-fat diet impair regulators of mitochondrial dynamics in rat placenta and offspring. Physiol Genomics. 2014; 46, 841850.CrossRefGoogle ScholarPubMed
Zhang, W, Cline, MA, Gilbert, ER. Hypothalamus-adipose tissue crosstalk: Neuropeptide y and the regulation of energy metabolism. Nutr Metab. 2014; 11, 112.CrossRefGoogle ScholarPubMed
White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol - Regul Integr Comp Physiol. 2009; 296, R1464R1472.CrossRefGoogle ScholarPubMed
Sussman, D, Ellegood, J, Henkelman, M. A gestational ketogenic diet alters maternal metabolic status as well as offspring physiological growth and brain structure in the neonatal mouse. BMC Pregnancy Childbirth. 2013; 13, 110.CrossRefGoogle ScholarPubMed