Effects of a westernized diet on the reflexes and physical maturation of male rat offspring during the perinatal period

Lipids

Volumn 48, Issue 11, 2013, Pages 1157-1168

  Ferro Cavalcante, Taisy Cinthia ^a   Lima Da Silva, Jennyffer Mayara ^a   Da Marcelino Da Silva, Amanda Alves ^a   Muniz, Gisélia Santana ^a   Da Luz Neto, Laércio Marques ^a   Lopes De Souza, Sandra ^a   Manhães De Castro, Raul ^a   Ferraz, Karla Mônica ^a   Do Nascimento, Elizabeth ^a  

^a FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

Author keywords

Gestation; Lactation; Neuro development; Rats; Somatic growth; Western diet

Indexed keywords

GLUCOSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY GROWTH; BODY HEIGHT; BODY WEIGHT; CONTROLLED STUDY; DIETARY INTAKE; FEMALE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GROWTH RATE; LACTATION; MALE; MOLECULAR DYNAMICS; NERVE CELL DIFFERENTIATION; NONHUMAN; PHYSICAL DEVELOPMENT; PRENATAL PERIOD; PROGENY; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RAT; REFLEX; REPRODUCTIVE SUCCESS; WESTERNIZED DIET;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; BIRTH WEIGHT; DIET; FEMALE; INTRA-ABDOMINAL FAT; MALE; MOTOR ACTIVITY; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; RATS; RATS, WISTAR; REFLEX, ACOUSTIC; STARTLE REACTION; WEIGHT GAIN;

EID: 84890122230     PISSN: 00244201     EISSN: 15589307     Source Type: Journal    
DOI: 10.1007/s11745-013-3833-z     Document Type: Article

References (73)

1. Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ et al (2011) National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet 377(9765):557-567 pii:S0140-6736(10)62037-5
2. Organization WHO (2011) World Health Organization-Obesity and overweight; Fact sheet N 311 Updated March http://www.who.int/mediacentre/factsheets/fs311/ en/
3. Ferreira VAMR (2006) Obesidade no Brasil: Tendências atutais. Revista portuguesa de Saúde Pública;v. 13:234-41. http://www.ensp.unl.pt/dispositivos-de-apoio/cdi/cdi/sector-de-publicacoes/ revista/2000-2008/pdfs/2-06-2006.pdf
4. Popkin BM (2001) The nutrition transition and obesity in the developing world. J NutrMar 131(3):871S-873S pii:131/3/871S
5. Batista Filho M, Rissin A (2003) Nutritional transition in Brazil: geographic and temporal trends. Cad Saude Publica 19(Suppl 1):S181-S191 pii:S0102-311X2003000700019
6. Buettner R, Scholmerich J, Bollheimer LC (2007) High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 15(4):798-808. doi: 10.1038/oby.2007.608
7. Okun N, Verma A, Mitchell BF, Flowerdew G (1997) Relative importance of maternal constitutional factors and glucose intolerance of pregnancy in the development of newborn macrosomia. J Matern Fetal Med 6(5):285-290. doi: 10.1002/(SICI)1520-6661(199709/10)6:5<285
8. Bayol SA, Farrington SJ, Stickland NC (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. Br J Nutr 98(4):843-851. doi: 10.1017/S0007114507812037
9. Bayol SA, Simbi BH, Bertrand JA, Stickland NC (2008) Offspring from mothers fed a 'junk food'' diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol 586(13):3219-3230. doi: 10.1113/jphysiol.2008.153817
10. Chen H, Simar D, Lambert K, Mercier J, Morris MJ (2008) Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology 149(11):5348-5356. doi: 10.1210/en.2008-0582
11. Shafat A, Murray B, Rumsey D (2009) Energy density in cafeteria diet induced hyperphagia in the rat. Appetite 52(1):34-38. doi: 10.1016/j.appet.2008. 07.004
12. Ferreira SR, Lerario DD, Gimeno SG, Sanudo A, Franco LJ (2002) Obesity and central adiposity in Japanese immigrants: role of the Western dietary pattern. J Epidemiol 12(6):431-438
13. Mehta SH (2008) Nutrition and pregnancy. Clin Obstet Gynecol 51(2):409-418. doi: 10.1097/GRF.0b013e31816fda53
14. Kunz LH, King JC (2007) Impact of maternal nutrition and metabolism on health of the offspring. Semin Fetal Neonatal Med 12(1):71-77 pii:S1744-165X(06)00104-1
15. Villar J, Cogswell M, Kestler E, Castillo P, Menendez R, Repke JT (1992) Effect of fat and fat-free mass deposition during pregnancy on birth weight. Am J Obstet Gynecol 167(5):1344-1352
16. Mielke JG, Nicolitch K, Avellaneda V, Earlam K, Ahuja T, Mealing G et al (2006) Longitudinal study of the effects of a high-fat diet on glucose regulation, hippocampal function, and cerebral insulin sensitivity in C57BL/6 mice. Behav Brain Res 175(2):374-382. doi: 10.1016/j.bbr.2006.09.010
17. Wainwright PE (1992) Do essential fatty acids play a role in brain and behavioral development? Neurosci Biobehav Rev 19:193-205 pii:S0149763405801800
18. Welby M, O'Halloran MW, Welby ML (1973) Maternal diet and lipid composition of breast milk. Lancet 2(7826):458-459
19. Huffman SL, Harika RK, Eilander A, Osendarp SJ (2011) Essential fats: how do they affect growth and development of infants and young children in developing countries? A literature review. Matern Child Nutr 7(Suppl 3):44-65. doi: 10.1111/j.1740-8709.2011.00356.x
20. Reeves PG (1997) Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 127(5 Suppl):838S-8341S
21. Hartman L, Lago RC (1973) Rapid preparation of fatty acid methyl esters from lipids. Lab Pract 22(6):475-476
22. Passos PP, Borba JM, Rocha-de-Melo AP, Guedes RC, da Silva RP, Filho WT et al (2012) Dopaminergic cell populations of the rat substantia nigra are differentially affected by essential fatty acid dietary restriction over two generations. J Chem Neuroanat 44(2):66-75. doi: 10.1016/j.jchemneu.2012.05.003
23. Bayol S, Jones D, Goldspink G, Stickland NC (2004) The influence of undernutrition during gestation on skeletal muscle cellularity and on the expression of genes that control muscle growth. Br J Nutr 91(3):331-339. doi: 10.1079/BJN20031070
24. Novelli EL, Diniz YS, Galhardi CM, Ebaid GM, Rodrigues HG, Mani F et al (2007) Anthropometrical parameters and markers of obesity in rats. Lab Anim 41(1):111-119. doi: 10.1258/002367707779399518
25. Silva HB, Barros KMFT, Cunha DA, Santos FAS, Soares EB, Silva CNS et al (2005) Protocol of mensuration to avaliation [sic] of indicators of somatic development of Wistar rats. Int J Morphl 23(3):227-30. http://dx.doi.org/10. 4067/S0717-95022005000300006
26. Fox WM (1965) Reflex-ontogeny and behavioural development of the mouse. Anim Behav 13(2):234-241
27. Simopoulos AP (2011) Evolutionary aspects of diet: the omega-6/omega-3 ratio and the brain. Mol Neurobiol 44(2):203-215. doi: 10.1007/s12035-010-8162-0
28. White CL, Purpera MN, Morrison CD (2009) Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol 296(5):R1464-R1472. doi: 10.1152/ajpregu.91015.2008
29. Connor KL, Vickers MH, Beltrand J, Meaney MJ, Sloboda DM (2012) Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol 590(Pt 9):2167-2180. doi: 10.1113/jphysiol.2011.223305
30. Purcell RH, Sun B, Pass LL, Power ML, Moran TH, Tamashiro KL (2011) Maternal stress and high-fat diet effect on maternal behavior, milk composition, and pup ingestive behavior. Physiol Behav 104(3):474-479. doi: 10.1016/j.physbeh.2011.05.012
31. Shaw MA, Rasmussen KM, Myers TR (1997) Consumption of a high fat diet impairs reproductive performance in Sprague-Dawley rats. J Nutr 127(1):64-69
32. Akyol A, McMullen S, Langley-Evans SC (2011) Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet. Br J Nutr 24:1-15 pii:S0007114511003916
33. Nakashima Y, Sato A (2011) Pups of dams fed low-fat diet during pregnancy and lactation showed strong preference for high-fat diet to achieve optimal growth. J Nutr Sci Vitaminol (Tokyo) 57(5):355-363 pii:JST.JSTAGE/jnsv/57.355
34. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH et al (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51(2):383-392. doi: 10.1161/HYPERTENSIONAHA.107.101477
35. Del Prado M, Delgado G, Villalpando S (1997) Maternal lipid intake during pregnancy and lactation alters milk composition and production and litter growth in rats. J Nutr 127(3):458-462 ISSN: 0022-3166
36. Herrera E, Amusquivar E, Lopez-Soldado I, Ortega H (2006) Maternal lipid metabolism and placental lipid transfer. Horm Res 65(Suppl 3):59-64. doi: 10.1159/000091507
37. Herrera E, Amusquivar E (2000) Lipid metabolism in the fetus and the newborn. Diabetes Metab Res Rev 16(3):202-210. doi: 10.1002/1520-7560(200005/06) 16:3<202
38. Bauman DE, Currie WB (1980) Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homeostasis and homeorhesis. J Dairy Sci 63(9):1514-1529 pii:S0022030280831110
39. Levin BE, Dunn-Meynell AA (2002) Defense of body weight depends on dietary composition and palatability in rats with diet-induced obesity. Am J Physiol Regul Integr Comp Physiol 282(1):R46-R54
40. Ahima RS, Bjorbaek C, Osei S, Flier JS (1999) Regulation of neuronal and glial proteins by leptin: implications for brain development. Endocrinology 140(6):2755-2762 0013-7227/99/03.00/0
41. Akyol A, Langley-Evans SC, McMullen S (2009) Obesity induced by cafeteria feeding and pregnancy outcome in the rat. Br J Nutr 102(11):1601-1610 pii:S0007114509990961
42. Howie GJ, Sloboda DM, Kamal T, Vickers MH (2009) Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol 587(Pt 4):905-915. doi: 10.1113/jphysiol.2008.163477
43. Bayol SA, Simbi BH, Stickland NC (2005) A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567(Pt 3):951-961. doi: 10.1113/jphysiol.2005.088989
44. Klaus S (2005) Increasing the protein: carbohydrate ratio in a high-fat diet delays the development of adiposity and improves glucose homeostasis in mice. J Nutr 135(8):1854-1858
45. Xu RY, Wan YP, Tang QY, Wu J, Cai W (2010) Carbohydrate-to-fat ratio affects food intake and body weight in Wistar rats. Exp Biol Med (Maywood) 235(7):833-838. doi: 10.1258/ebm.2010.009276
46. Lopez-Luna P, Munoz T, Herrera E (1986) Body fat in pregnant rats at mid- and late-gestation. Life Sci 39(15):1389-1393
47. King JC, Butte NF, Bronstein MN, Kopp LE, Lindquist SA (1994) Energy metabolism during pregnancy: influence of maternal energy status. Am J Clin Nutr 59(2 Suppl):439S-445S
48. Elliott JA (1975) The effect of pregnancy on the control of lipolysis in fat cells isolated from human adipose tissue. Eur J Clin Invest 5(2):159-163. doi: 10.1111/j.1365-2362.1975.tb02282.x
49. Herrera E, Gomez-Coronado D, Lasuncion MA (1987) Lipid metabolism in pregnancy. Biol Neonate 51(2):70-77. doi: 10.1159/000242635
50. Martin-Hidalgo A, Holm C, Belfrage P, Schotz MC, Herrera E (1994) Lipoprotein lipase and hormone-sensitive lipase activity and mRNA in rat adipose tissue during pregnancy. Am J Physiol 266(6 Pt 1):E930-E935
51. Cetin I, Alvino G, Cardellicchio M (2009) Long chain fatty acids and dietary fats in fetal nutrition. J Physiol 587(Pt 14):3441-3451. doi: 10.1113/jphysiol.2009.173062
52. Levin BE (2006) Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis. Philos Trans R Soc Lond B Biol Sci 361(1471):1107-1121. doi: 10.1098/rstb.2006.1851
53. Howie GJ, Sloboda DM, Reynolds CM, Vickers MH (2013) Timing of maternal exposure to a high fat diet and development of obesity and hyperinsulinemia in male rat offspring: same metabolic phenotype, different developmental pathways? J Nutr Metab 2013:517384. doi: 10.1155/2013/517384
54. Brandorff NP (1980) The effect of dietary fat on the fatty acid composition of lipids secreted in rats' milk. Lipids 15(4):276-278. doi: 10.1007/BF02535840
55. Karaolis-Danckert N, Gunther AL, Kroke A, Hornberg C, Buyken AE (2007) How early dietary factors modify the effect of rapid weight gain in infancy on subsequent body-composition development in term children whose birth weight was appropriate for gestational age. Am J Clin Nutr 86(6):1700-1708
56. Wells JC, Hallal PC, Wright A, Singhal A, Victora CG (2005) Fetal, infant and childhood growth: relationships with body composition in Brazilian boys aged 9 years. Int J Obes (Lond) 29(10):1192-1198. doi: 10.1038/sj.ijo.0803054
57. Victora CG, Sibbritt D, Horta BL, Lima RC, Cole T, Wells J (2007) Weight gain in childhood and body composition at 18 years of age in Brazilian males. Acta Paediatr 96(2):296-300. doi: 10.1111/j.1651-2227.2007.00110.x
58. Murrin C, Shrivastava A, Kelleher CC (2013) Maternal macronutrient intake during pregnancy and 5 years postpartum and associations with child weight status aged five. Eur J Clin Nutr 24. doi: 10.1038/ejcn.2013.76
59. Medina JM, Tabernero A (2002) Astrocyte-synthesized oleic acid behaves as a neurotrophic factor for neurons. J Physiol Paris 96(3-4):265-271 pii:S0928-4257(02)00015-3
60. Polo-Hernandez E, De Castro F, Garcia-Garcia AG, Tabernero A, Medina JM (2010) Oleic acid synthesized in the periventricular zone promotes axonogenesis in the striatum during brain development. J Neurochem 114(6):1756-1766. doi: 10.1111/j.1471-4159.2010.06891.x
61. Crawford MA, Hassam AG, Williams G (1976) Essential fatty acids and fetal brain growth. Lancet 1(7957):452-453 pii:S0140673676914768
62. Crawford MA, Hassam AG, Stevens PA (1981) Essential fatty acid requirements in pregnancy and lactation with special reference to brain development. Prog Lipid Res 20:31-40 pii:0163-7827(81)90011-4
63. Walker CD, Naef L, d'Asti E, Long H, Xu Z, Moreau A et al (2008) Perinatal maternal fat intake affects metabolism and hippocampal function in the offspring: a potential role for leptin. Ann N Y Acad Sci 1144:189-202. doi: 10.1196/annals.1418.023
64. Chang GQ, Gaysinskaya V, Karatayev O, Leibowitz SF (2008) Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 28(46):12107-12119. doi: 10.1523/JNEUROSCI.2642-08.2008
65. Barros KM, Manhaes-De-Castro R, Lopes-De-Souza S, Matos RJ, Deiro TC, Cabral-Filho JE et al (2006) A regional model (Northeastern Brazil) of induced mal-nutrition delays ontogeny of reflexes and locomotor activity in rats. Nutr Neurosci 9(1-2):99-104
66. McGraw MB (1940) Neuromuscular development of the human infant as exemplified in the achievement of erect locomotion. J Pediatr 17:747-771 pii:S0022347640800218
67. Walton KD, Lieberman D, Llinas A, Begin M, Llinas RR (1992) Identification of a critical period for motor development in neonatal rats. Neuroscience 51(4):763-767 pii:0306-4522(92)90517-6
68. Gramsbergen A (1998) Posture and locomotion in the rat: independent or interdependent development? Neurosci Biobehav Rev 22(4):547-553 pii:S0149763497000432
69. Raygada M, Cho E, Hilakivi-Clarke L (1998) High maternal intake of polyunsaturated fatty acids during pregnancy in mice alters offsprings' aggressive behavior, immobility in the swim test, locomotor activity and brain protein kinase C activity. J Nutr 128(12):2505-2511
70. Soulis G, Papalexi E, Kittas C, Kitraki E (2007) Early impact of a fat-enriched diet on behavioral responses of male and female rats. Behav Neurosci 121(3):483-490. doi: 10.1037/0735-7044.121.3.483
71. Sharma S, Zhuang Y, Gomez-Pinilla F (2012) High-fat diet transition reduces brain DHA levels associated with altered brain plasticity and behaviour. Sci Rep 2:431. doi: 10.1038/srep00431
72. Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomes-Pinilla F (2002) A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112(4):803-814 pii:S0306452202001239
73. Granholm AC, Bimonte-Nelson HA, Moore AB, Nelson ME, Freeman LR, Sambamurti K (2008) Effects of a saturated fat and high cholesterol diet on memory and hippocampal morphology in the middle-aged rat. J Alzheimers Dis 14(2):133-145