Oligofructose supplementation (10%) during pregnancy and lactation does not change the inflammatory effect of concurrent trans fatty acid ingestion on 21-day-old offspring

Lipids in Health and Disease

Luciana Pellegrini Pisani²  Claudia Maria Oller do Nascimento¹  Eliane Beraldi Ribeiro¹  Lila Missae Oyama¹  Bruno dos Santos¹  Marcos Hiromu Okuda¹  Mayara Franzoi Moreno¹  Juliana Lopes de Oliveira¹  Laís Vales Mennitti²  Ana Claudia Losinskas Hachul¹ 

[1] Departamento Fisiologia, Disciplina de Fisiologia da Nutrição, Escola Paulista de Medicina, Universidade Federal de São Paulo, Rua Botucatu, 862, 2º andar, Vila Clementino, São Paulo, SP, Brazil;Departamento de Biociências, Instituto de Saúde e Sociedade, Universidade Federal de São Paulo, Santos, SP, Brazil

关键词: Cytokines;    Lactation;    Pregnancy;    Muscle;    White adipose tissue;    Oligofructose;    Hydrogenated fat;   

Others  :  834734
DOI  :  10.1186/1476-511X-12-59

 received in 2012-12-10, accepted in 2013-04-18,  发布年份 2013

【 摘 要 】

Background

Previously, we demonstrated that trans fatty acid ingestion during pregnancy and lactation caused a pro-inflammatory effect on the newborn. The opposite effect was described for gestational prebiotic intake. In the present study, we examined whether supplementation of the diet of the dams with 10% of oligofructose with or without hydrogenated vegetable fat during pregnancy and lactation affected the pro-inflammatory status on the pups at age 21 days.

Methods

On the first day of pregnancy, rats were divided into four groups, each of which received one of four diets: a control diet (C group), a control diet supplemented with 10% oligofructose (CF group), a diet enriched with hydrogenated vegetable fat containing trans fatty acids (T group) or a diet enriched with hydrogenated vegetable fat containing trans fatty acids supplemented with 10% oligofructose (TF group). The pups were weighed at birth and at 7, 14 and 21 days of life and were euthanized on post-natal day 21. The serum glucose, insulin and adiponectin concentrations were analyzed. The IL-6, IL-10 and TNF-α contents of the retroperitoneal white adipose tissue, liver, soleus and extensor digital longus muscles were analyzed by ELISA. The results are presented as the means ± standard error of the mean. Statistical significance was assessed using two-way ANOVA, followed by Tukey's test and considered significant at p < 0.05

Results

The body weights of the 21-day old pups in the CF and TF groups were significant lower than those of the C (27% and 21%) and T (25% and 19%, respectively) groups. The serum levels of adiponectin in the CF, T and TF groups were lower than in the C group (41%; 34% and 31%, respectively). In the retroperitoneal adipose tissue, the IL-6 content was increased in TF group relative to the C and CF groups (74% for both), and the TNF-α content was higher in the T and TF groups than in the C group (62% and 98%, respectively). In the liver, the TNF-α (56% and 104%) and IL-10 (52% and 73%) contents were increased in the CF group relative to the C and TF groups.

Conclusions

Supplementation of the diet of the dams with 10% of oligofructose during pregnancy and lactation, independent of supplementation with hydrogenated vegetable fat, adversely affected the development of the offspring and contributed to development of a pro-inflammatory status in the pups on postnatal day 21.

【 授权许可】

   
2013 Hachul et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Champ M, Hoebler C: Functional food for pregnant, lactating women and in perinatal nutrition: a role for dietary fibres? Curr Opin Clin Nutr Metab Care 2009, 12:565-574.
• [2]Godfrey KM, Barker DJ: Fetal programming and adult health. Public Health Nutr 2001, 4:611-624.
• [3]Morley R, Dwyer T: Fetal origins of adult disease? Clin Exp Pharmacol Physiol 2001, 28:962-966.
• [4]Gillman MW: Epidemiological challenges in studying the fetal origins of adult chronic disease. Int F Epidemiol 2002, 31:294-299.
• [5]Guzik TJ, Mangalat D, Korbut R: Adipocytokines - novel link between inflammation and vascular function? J Physiol Pharmacol 2006, 57(4):505-528.
• [6]Pisani LP, Oyama LM, Bueno AA, Biz C, Albuquerque KT, Ribeiro EB, Oller do Nascimento CM: Hydrogenated fat intake during pregnancy and lactation modifies serum lipid profile and adipokine mRNA in 21-day-old rats. Nutrition 2008, 24:255-261.
• [7]De Oliveira JL, Oyama LM, Hachul AC, Biz C, Ribeiro EB, Oller do Nascimento CM, Pisani LP: Hydrogenated fat intake during pregnancy and lactation caused increase in TRAF-6 and reduced AdipoR1 in white adipose tissue, but not in muscle of 21 days old offspring rats. Lipids Health Dis 2011, 10:22. BioMed Central Full Text
• [8]Osso FS, Moreira AS, Teixeira MT, Pereira RO, Tavares do Carmo MG, Moura AS: Trans fatty acids in maternal milk lead to cardiac insulin resistance in adult offspring. Nutrition 2008, 24(7–8):727-732.
• [9]Pisani LP, Oller do Nascimento CM, Bueno AA, Biz C, Albuquerque KT, Ribeiro EB, Oyama LM: Hydrogenated fat diet intake during pregnancy and lactation modifies the PAI-1 gene expression in white adipose tissue of offspring in adult life. Lipids Health Dis 2008, 7:13. BioMed Central Full Text
• [10]Pimentel GD, Lira FS, Rosa JC, Oliveira JL, Losinskas-Hachul AC, Souza GI, das Graças T do Carmo M, Santos RV, de Mello MT, Tufik S, Seelaender M, Oyama LM, Oller do Nascimento CM, Watanabe RH, Ribeiro EB, Pisani LP: Intake of trans fatty acids during gestation and lactation leads to hypothalamic inflammation via TLR4/NFκBp65 signaling in adult offspring. J Nutr Biochem 2012, 23(3):265-271.
• [11]Brighenti F: Dietary fructans and serum triacylglycerols: a meta-analysis of randomized controlled trials. J Nutr 2007, 137(11):2552S-2556S.
• [12]Delzenne NM, Daubioul C, Neyrinck A, Lasa M, Taper HS: Inulin and oligofructose modulate lipid metabolism in animals: review of biochemical events and future prospects. Br J Nutr 2002, 87:S255-S259.
• [13]Carabin IG, Flamm WG: Evaluation of safety of inulin and oligofructose as dietary fiber. Regul Toxicol Pharmacol 1999, 30:268-282.
• [14]Kok NN, Taper HS, Delzenne NM: Oligofructose modulates lipid metabolism alterations induced by a Fat-rich diet in rats. J Appl Toxicol 1998, 18:47-53.
• [15]Bonsu NKA, Johnson CS, Mcleod KM: Can dietary fructans lower serum glucose? J Diabetes 2011, 3:58-66.
• [16]Kok N, Roberfroid M, Robert A, Delzenne N: Involvement of lipogenesis in the lower VLDL secretion induced by oligofructose in rats. Br J Nutr 1996, 76:881-890.
• [17]Roberfroid MB: Introducing inulin-type fructans. Br J Nutr 2005, 93:S13-S25.
• [18]Cherbut C: Inulin and oligofructose in the dietary fibre concept. Br J Nutr 2002, 87:S159-S162.
• [19]Kleessen B, Hartmann L, Blaut M: Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr 2001, 86:291-300.
• [20]Kaur N, Gupta AK: Applications of inulin and oligofructose in health and nutrition. J Biosci 2002, 27:703-714.
• [21]Roberfroid MB: Chicory fructooligosaccharides and the gastrointestinal tract. Nutrition 2000, 16:677-679.
• [22]Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM: Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007, 50(11):2374-2383.
• [23]Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, Prada PO, Hirabara SM, Schenka AA, Araújo EP, Vassallo J, Curi R, Velloso LA, Saad MJ: Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 2007, 56(8):1986-1998.
• [24]Nakamura YK, Omaye ST: Metabolic diseases and pro- and prebiotics: mechanistic insights. Nutr Metab (Lond) 2012, 9:60. BioMed Central Full Text
• [25]Rudloff S, Kunz C: Milk oligosaccharides and metabolism in infants. Adv Nutr 2012, 3:398-405.
• [26]Kunz C, Rudloff S, Baier W, Klein N, Strobel S: Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 2000, 20:699-722.
• [27]Reeves PG: Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr 1997, 127(Suppl):838S-841S.
• [28]Stansbie D, Denton RM, Bridges BJ, Pask HT, Randle PJ: Regulation of pyruvate dehydrogenase and pyruvate dehydrogenase phosphate phosphatase activity in rat epididymal fat-pads. Effects of starvation, alloxan-diabetes and high-fat diet. Biochem J 1976, 154:225-236.
• [29]Oller do Nascimento CM, Williamson DH: Evidence for conservation of dietary lipid in the rat during lactation and the immediate period after removal of the litter. Biochem J 1986, 239:233-236.
• [30]Greg Kelly ND: Inulin-type prebiotics: a review (part 2). Altern Med Rev 2009, 14:36-55.
• [31]Maurer AD, Reimer RA: Maternal consumption of high-prebiotic fibre or -protein diets during pregnancy and lactation differentially influences satiety hormones and expression of genes involved in glucose and lipid metabolism in offspring in rats. Br J Nutr 2011, 105(3):329-338.
• [32]Rodenburg W, Keijer J, Kramer E, Vink C, van der Meer R, Bovee-Oudenhoven IM: Impaired barrier function by dietary fructo-oligosaccharides (FOS) in rats is accompanied by increased colonic mitochondrial gene expression. BMC Genomics 2008, 9:144. BioMed Central Full Text
• [33]Zhao SP, Wu ZH, Wu J, Hong SC, Deng P: Effect of atorvastatin on tumor necrosis factor alpha serum concentration and mRNA expression of adipose in hypercholesterolemic rabbits. J Cardiovasc Pharmacol 2005, 46:185-189.
• [34]Díez JJ, Iglesias P: The role of the novel adipocyte-derived hormone adiponectin in human disease. Eur J Endocrinol 2003, 148(3):293-300.
• [35]Wang B, Trayhurn P: Acute and prolonged effects of TNF-alpha on the expression and secretion of inflammation-related adipokines by human adipocytes differentiated in culture. Pflugers Arch 2006, 452(4):418-427.
• [36]Harwood HJ Jr: The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012, 63(1):57-75.
• [37]Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Van der Meer R: Dietary fructo-oligosaccharides dose-dependently increase translocation of salmonella in rats. J Nutr 2003, 133(7):2313-2318.