Influence of mother nutrition during pregnancy and/or lactation on offspring food preference in experimental models

Santos, L. S.; Cordeiro, G. S.; Perez, G. S.; Santo, D. A. E.; Macêdo, A. P. A.; Lima, M. S.; Carneiro, I. B. C.; Machado, M. E. P. C.; Deiró, T. C.B. J.; Barreto-Medeiros, J. M.

doi:10.1590/1519-6984.179134

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Brazilian Journal of Biology

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Original Article • Braz. J. Biol. 79 (2) • Apr-Jun 2019 • https://doi.org/10.1590/1519-6984.179134 copy

Influence of mother nutrition during pregnancy and/or lactation on offspring food preference in experimental models

Influência da nutrição materna durante a gestação e/ou lactação na preferência alimentar da prole em modelos experimentais

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Introduction

Understanding associations between food preferences and maternal nutrition during pregnancy and lactation could inform efforts to understanding the obesity mechanisms and provide insight to prevent it. Objective: To identify studies that investigated the effects of nutritional interventions during the pregnancy and lactation on the food preferences of offspring. Method: The review was conducted with search for articles in the databases: Scopus, Pubmed, Medline, LILACS, Scielo and Science Direct. Exclusion criteria were used: reviews, human studies, studies with drugs or other substances not related to food. Results: At the end of the search in the databases, 176 references were found. After use the exclusion criteria, reading the titles, abstracts and full articles, were selected 11 articles to compose the review. Conclusion: The selected studies suggested that unbalanced nutrition in early life alters the food preference and neural components related to the consumption of fatty and sugary foods in offspring rodents.

Keywords:
pregnancy; lactation; rats; diet; food preference

Identification	Methodological aspects								Main results
Main author / year	Species	Sex	Diet early exposure	Macronutrient percentage of diet early exposure	Period exposure of diet	Diet (s) preference test	Percentage of macronutrients	Period and duration of study food preference	Main results
Brenseke et al. (2015) BRENSEKE, B., BAHAMONDE, J., TALANIAN, M., KORNFEIND, E., DALY, J., COBB, G., ZHANG, J., PRATER, M.R., DAVIS, G.C. and GOOD, D.J., 2015. Mitigating or exacerbating effects of maternal-fetal programming of female mice through the food choice environment. Endocrinology , vol. 156, no. 1, pp. 182-192. http://dx.doi.org/10.1210/en.2014-1523. PMid:25386832. http://dx.doi.org/10.1210/en.2014-1523 ...	Mice C57BL / 6	F/M	High fat diet	60,3% LIP 18% PTN	Gestation and Lactation	High fat diet	60,3% LIP 18% PTN	Period: 7th to 18th week of life Duration: 11 weeks	When given the choice of diet compared to the control rats had offspring: • Increased energy consumption; • Increased body weight; • Increased amount of body fat; • Increased serum levels of leptin; • Increased levels of glucose in the blood.
Sanchez-Hernandez et al. (2015) SANCHEZ-HERNANDEZ, D., POON, A.N., KUBANT, R., KIM, H., HUOT, P.S., CHO, C.E., PANNIA, E., PAUSOVA, Z. and ANDERSON, G.H., 2015. A gestational diet high in fat-soluble vitamins alters expression of genes in brain pathways and reduces sucrose preference, but not food intake, in Wistar male rat offspring. Applied Physiology, Nutrition, and Metabolism = Physiologie Appliquee, Nutrition et Metabolisme, vol. 40, no. 4, pp. 424-431. http://dx.doi.org/10.1139/apnm-2014-0480. PMid:25787712. http://dx.doi.org/10.1139/apnm-2014-048...	Wistar rats	F/M	High fat diet with 10 times more vitamins A, D, E and K, based on the AIN 93.	Uninformed	Gestation and Lactation	High fat diet with vitamins	60% LIP	Study Start: 14 weeks post weaning Duration: 2 weeks	High fat diet with vitamins A, D, E, and K during pregnancy has not generated: • Increase in body weight; • Increased food intake; High fat diet with vitamins A, D, E, and K during pregnancy generated: • Increase of 30% of POMC (pro-opiomelanocortin); • Increase of 40% of gene expression of NPY (neuropeptide Y).
Molle et al. (2015) MOLLE, R.D., LAUREANO, D.P., ALVES, M.B., REIS, T.M., DESAI, M., ROSS, M.G. and 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 , vol. 1618, pp. 41-49. http://dx.doi.org/10.1016/j.brainres.2015.05.019. PMid:26006109. http://dx.doi.org/10.1016/j.brainres.20...	Sprague Dawley rats	F/M	Diet Nuvilab(hypocaloric)	50% of food restriction	Gestation	High fat diet and hypercaloric with saccharose	25% PTN 23% LIP 47% CHO 20% saccharose	Study Start: 80 days Adaptation period: 4 days Duration of preference: 4 days	Adult rat offspring who were exposed to food restriction showed: • Increased preference for highly palatable foods; •Increased levels of tyrosine hydroxylase, tyrosine hydroxylase and phospho-2 dopamine receptor in the nucleus accumbens.
Agnoux et al. (2014) AGNOUX, A.M., ANTIGNAC, J.P., SIMARD, G., POUPEAU, G., DARMAUN, D., PARNET, P. and ALEXANDRE-GOUABAU, M.C., 2014. Time window-dependent effect of perinatal maternal protein restriction on insulin sensitivity and energy substrate oxidation in adult male offspring. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 307, no. 2, pp. R184-R197. http://dx.doi.org/10.1152/ajpregu.00015.2014. PMid:24808498. http://dx.doi.org/10.1152/ajpregu.00015...	Sprague Dawley rats	M	Low protein diet	8% PTN	Gestation and Lactation	High carbohydrate diet, high fat diet	Uninformed	Study Start: 120th day of life Adaptation period: 10 days Duration: 10 days	•The group exposed to the control diet in inta-uterine life and low protein diet after weaning showed a strong preference for high-fat diet; •The group exposed only to the control diet showed preference for diet rich in sucrose; •The group exposed only to low protein diet showed preference for diet control; •The group exposed to low protein diet during intrauterine life and control diet after weaning did not provide any food preferences. The rats born with intrauterine growth restriction (IUGR) and fed a Western diet in adulthood were: •Increased predisposition to the weight gain; •Accumulation of more fat. Rats exposed to the control diet in early life and the low protein diet after weaning, despite his preference for high-fat diet: •Do not showed significant increase in adipose tissue; •Lower expression of NPY (neuropeptide Y), enterostatin, MC4R (melanocortin) and tyrosine hydroxylase.
Ong and Muhlhausler (2011) ONG, Z.Y. and MUHLHAUSLER, B.S., 2011. Maternal “junk-food” feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. The FASEB Journal, vol. 25, no. 7, pp. 2167-2179. http://dx.doi.org/10.1096/fj.10-178392. PMid:21427213. http://dx.doi.org/10.1096/fj.10-178392 ...	Wistar rats	F/M	Cafeteria diet	Lard / mix with standard chow kJ:20,9/LIP:19%/CHO:51%/ PTN:17% Peanut butter KJ:26,2/LIP:50%/CHO:25% PTN: 21% Hazelnut KJ:23,3/LIP:36%/CHO: 54% PTN:4% Chocolate cookies KJ:20.0/LIP:15%/CHO: 71% PTN:10% Chips KJ:23.1/LIP:35%/CHO:51% PTN: 7% Sweetened cereal KJ:27,3/LIP:3%/CHO:43% PTN:1% Processed meat KJ:7,3/LIP:12%/CHO: 7%/ PTN:10%	Gestation and Lactation	Hypoproteic	Lard / mix with standard chow kJ:20,9/LIP:19%/CHO:51%/ PTN:17% Peanut butter KJ:26,2/LIP:50%/CHO:25% PTN: 21% Hazelnut KJ:23,3/LIP:36%/CHO: 54% PTN:4% Chocolate cookies KJ:20.0/LIP:15%/CHO: 71% PTN:10% Chips KJ:23.1/LIP:35%/CHO:51% PTN: 7% Sweetened cereal KJ:27,3/LIP:3%/CHO:43% PTN:1% Processed meat KJ:7,3/LIP:12%/CHO: 7%/ PTN:10%	Period (youth group): 6th week of life Duration: 3 weeks Period (adult group): 3 months Duration: 3 weeks	In youth group, male and female descendants of progenitors who consumed cafeteria diet during pregnancy and lactation: • Consumed more energy and carbohydrates during exposure to cafeteria diet; • At 6 weeks of age showed higher body fat. The female offspring showed higher concentration of: • Tyrosine hydroxylase; • Dopamine receptors; • Increased expression of active dopamine transporter in the ventral tegmental area.
Gugusheff et al. (2013) GUGUSHEFF, J.R., VITHAYATHIL, M., ONG, Z.Y. and MUHLHAUSLER, B.S., 2013. The effects of prenatal exposure to a ‘junk food’ diet on offspring food preferences and fat deposition can be mitigated by improved nutrition during lactation. Journal of Developmental Origins of Health and Disease, vol. 4, no. 5, pp. 348-357. http://dx.doi.org/10.1017/S2040174413000330. PMid:24970728. http://dx.doi.org/10.1017/S204017441300...	Wistar rats	F/M	Cafeteria diet	Lard / mix with standard chow kJ:20,9/LIP:19%/CHO:51%/ PTN:17% Peanut butter KJ:26,2/LIP:50%/CHO:25% PTN: 21% Hazelnut KJ:23,3/LIP:36%/CHO: 54% PTN:4% Chocolate cookies KJ:20.0/LIP:15%/CHO: 71% PTN:10% Chips KJ:23.1/LIP:35%/CHO:51% PTN: 7% Sweetened cereal KJ:27,3/LIP:3%/CHO:43% PTN:1% Processed meat KJ:7,3/LIP:12%/CHO: 7%/ PTN:10%	Gestation and Lactation	Cafeteria diet	Lard / mix with standard chow kJ: 20, 9/LIP: 19%/CHO: 51%/ PTN:17% Peanut butter KJ:26,2/LIP:50%/CHO:25% PTN: 21% Hazelnut KJ:23,3/LIP:36%/CHO: 54% PTN:4% Chocolate cookies KJ:20.0/LIP:15%/CHO: 71% PTN:10% Chips KJ:23.1/LIP:35%/CHO:51% PTN: 7% Sweetened cereal KJ:27,3/LIP:3%/CHO:43% PTN:1% Processed meat KJ: 7, 3/LIP: 12%/CHO: 7%/ PTN:10%	Period: 10th to 16th week of life Duration: 6 weeks	Male progenitors of descendants who consumed high-fat diet during pregnancy and lactation and only during lactation were: • Increased intake of fat, carbohydrates and energy; • Females had higher amount of body fat after 3 weeks of cafeteria diet consumption.
Ong and Muhlhausler (2011) ONG, Z.Y. and MUHLHAUSLER, B.S., 2011. Maternal “junk-food” feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. The FASEB Journal, vol. 25, no. 7, pp. 2167-2179. http://dx.doi.org/10.1096/fj.10-178392. PMid:21427213. http://dx.doi.org/10.1096/fj.10-178392 ...	Wistar rats	F/M	Cafeteria diet	Lard / mix with standard chow kJ:20,9/LIP:19%/CHO:51%/ PTN:17% Peanut butter KJ:26,2/LIP:50%/CHO:25% PTN: 21% Hazelnut KJ:23,3/LIP:36%/CHO: 54% PTN:4% Chocolate cookies KJ:20.0/LIP:15%/CHO: 71% PTN:10% Chips KJ:23.1/LIP:35%/CHO:51% PTN: 7% Sweetened cereal KJ:27,3/LIP:3%/CHO:43% PTN:1% Processed meat KJ: 7, 3/LIP: 12%/CHO: 7%/ PTN:10%	Gestation and Lactation	Cafeteria diet	Lard / mix with standard chow kJ: 20, 9/LIP: 19%/CHO: 51%/ PTN:17% Peanut butter KJ:26,2/LIP:50%/CHO:25% PTN: 21% Hazelnut KJ:23,3/LIP:36%/CHO: 54% PTN:4% Chocolate cookies KJ:20.0/LIP:15%/CHO: 71% PTN:10% Chips KJ:23.1/LIP:35%/CHO:51% PTN: 7% Sweetened cereal KJ:27,3/LIP:3%/CHO:43% PTN:1% Processed meat KJ: 7, 3/LIP: 12%/CHO: 7%/ PTN:10%	Period: 21st to 90th day Duration: 10 weeks	At weaning (day 21), male and female descendants of progenitors who consumed cafeteria diet showed: • Less weight; • Increased amount of fat; • Increased concentration of plasma leptin; • Lower insulin levels. In the juvenile period (22 to 42 days), they consumed more fat and protein, and adulthood (43 to 90 days), there was a higher fat intake. The mRNA expression Mu (opioid receptor) in the nucleus accumbens was higher at 6 weeks of age, regardless of sex, in descending progenitors offspring who consumed cafeteria diet.
Palou et al. (2010) PALOU, M., PRIEGO, T., SÁNCHEZ, J., TORRENS, J.M., PALOU, A. and PICÓ, C., 2010. Moderate caloric restriction in lactating rats protects offspring against obesity and insulin resistance in later life. Endocrinology, vol. 151, no. 3, pp. 1030-1041. http://dx.doi.org/10.1210/en.2009-0934. PMid:20068006. http://dx.doi.org/10.1210/en.2009-0934 ...	Wistar rats	F/M	Hypocaloric diet	Hypocaloric diet (restriction 20% of calories)	Gestation	High carbohydrate and high fat diet (food preference) high fat diet (4th to 5th month of life)	High carbohydrate diet (10 g / 100 ml skim milk, 40 g / 100 ml sucrose 4 g / 100 ml of oil, and 0.35 g / 100 mL xanthan gum (Sigma, Madrid, Spain); 3 month fat diet (10 g / 100 ml skim milk, 10 g / 100 ml sucrose 17.3 g / 100 ml of oil, and 0.35 g / 100 mL xanthan gum); High fat diet 4th to 5th month (4.7 kcal / g, with 45% of calories from fat, Research Diets, Inc., NJ, USA)	Period: 3rd month of life Duration: Uninformed	From the 74th day of life, the male animals who have suffered calorie restriction in intrauterine life were: • Increased weight gain; • Increased food intake. In the 5th month, they presented: • Increased adipose tissue. From the 4th to 5th month, females who suffered calorie restriction had: • Increased body weight; • Increased food intake. Males and females (restriction) showed: • Higher levels of insulin at 2 months of age; • Increased HOMA index in males and females (restriction) with 4:05 months old; • Higher leptin levels in males (restriction) with 5 months. • High levels of triglycerides (2.4 and 5 months) in males and females restriction); • Both groups and sexes had higher preference for High carbohydrate diet, however, the preference for high-fat diet was higher in male rats (restriction) when compared to controls.
Vucetic et al. (2010) VUCETIC, Z., KIMMEL, J., TOTOKI, K., HOLLENBECK, E. and REYES, T.M., 2010. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology, vol. 151, no. 10, pp. 4756-4764. http://dx.doi.org/10.1210/en.2010-0505. PMid:20685869. http://dx.doi.org/10.1210/en.2010-0505 ...	Mice (C57BL/6J	M	High fat diet	18,5% PTN 60% LIP 20,5% CHO	Gestation and Lactation	High fat diet Sucrose solution	High fat diet (18.5% PTN, 60% LIP and 20.5% CHO); Sucrose solution (4% sucrose)	Period: 24 weeks of age Duration: 3 days for each diet	All groups preferred the fat diet and sucrose solution, however, progenitors of descendants who consumed high-fat diet during pregnancy and lactation had higher preference for sucrose and the high fat diet.
Bellinger and Langley-Evans (2005) BELLINGER, L. and LANGLEY-EVANS, S.C., 2005. Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clinical Science, vol. 109, no. 4, pp. 413-420. http://dx.doi.org/10.1042/CS20050127. PMid:15992360. http://dx.doi.org/10.1042/CS20050127 ...	Wistar rats	F/M	Low protein diet	90 g casein / kg diet	Gestation	High protein diet High carbohydrate diet High fat diet	High protein diet LIP: 10% PTN: 48,5% CHO: 32,5% High carbohydrate diet LIP: 10% PTN: 20% CHO: 62% High fat diet LIP: 39,5% PTN: 20% CHO: 32,5%	Period: 12th week of life Duration: 3 days	• In week 12, male and female descendants of progenitors who consumed low protein diet showed lower weight; • All groups showed preference for high fat diet (except for the descendants of progenitors females who consumed low protein diet from day 0 to day 7 of gestation) and less consumed high protein diet; • females during the period preferênciaconsumiram more calories than males; • Male, progenitors of descendants who consumed hypoproteic diet showed higher concentration of liver glycogen, hyperinsulinemia, increased concentration of cholesterol in plasma.
Bellinger et al. (2004) BELLINGER, L., LILLEY, C. and 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. The British Journal of Nutrition, vol. 92, no. 3, pp. 513-520. http://dx.doi.org/10.1079/BJN20041224. PMid:15469656. http://dx.doi.org/10.1079/BJN20041224 ...	Wistar rats	F/M	Low protein diet	90 g casein / kg diet As diets differ in the ratio of methionine: casein, which was 1:36 in the control diet and 01:18 in the test diet.	Gestation	High protein diet High carbohydrate diet High fat diet	High protein diet LIP: 10% PTN: 48,5% CHO: 32,5% High carbohydrate diet LIP: 10% PTN: 20% CHO: 62% High fat diet LIP: 39,5% PTN: 20% CHO: 32,5%	Period: 12th and 30th week of age Duration: 3 days per period	• Males and females progenitors who consumed low protein diet during pregnancy consumed significantly more fat diet and less High carbohydrate diet than the control animals; • At 30 weeks of age there were no differences in the pattern of food selection between the two groups of animals; • male offspring of rats who consumed low protein diet apresentouquantidade gonadalsignificativamente fat higher than the control animals, but the analysis of total body fat content indicated that there was no significant difference in overall adiposity.

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