Oligofructose supplementation during pregnancy and lactation impairs offspring development and alters the intestinal properties of 21-d-old pups

Lipids in Health and Disease

Volumn 13, Issue 1, 2014, Pages

  Mennitti, Laís Vales ^a   Oyama, Lila Missae ^a   De Oliveira, Juliana Lopez ^a   Hachul, Ana Claudia Losinskas ^a   Santamarina, Aline Boveto ^a   De Santana, Aline Alves ^a   Okuda, Marcos Hiromu ^a   Ribeiro, Eliane Beraldi ^a   Do Nascimento, Claudia Maria Da Penha Oller ^a   Pisani, Luciana Pellegrini ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Corporal composition; Hydrogenated vegetable fat; Lactation; Lactobacillus spp; Lipopolysaccharides; Oligofructose; Pregnancy

Indexed keywords

ADMINISTRATION, ORAL; ANIMALS; COLON; DIETARY SUPPLEMENTS; ENDOTOXEMIA; FATTY ACIDS, NONESTERIFIED; FECES; FEMALE; GROWTH DISORDERS; HYDROGENATION; INTRA-ABDOMINAL FAT; LACTATION; LACTOBACILLUS; LIPOPOLYSACCHARIDES; OLIGOSACCHARIDES; PLANT OILS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; WEIGHT GAIN;

EID: 84893156188     PISSN: None     EISSN: 1476511X     Source Type: Journal    
DOI: 10.1186/1476-511X-13-26     Document Type: Article

References (63)

1. In utero programming of chronic disease. Barker DJ, Clin Sci (Lond) 1998 95 2 115 128 10.1042/CS19980019 9680492 (Pubitemid 28401260)
2. Maternal regulation of fetal development and health in adult life. Godfrey KM, Eur J Obstet Gynecol Reprod Biol 1998 78 2 141 150 10.1016/S0301-2115(98)00060-8 9622311 (Pubitemid 28201104)
3. The role of the placenta in fetal programming-a review. Godfrey KM, Suppl A, Placenta 2002 23 20 27 11978056
4. Fetal origins of adult disease? Morley R, Dwyer T, Clin Exp Pharmacol Physiol 2001 28 11 962 966 10.1046/j.1440-1681.2001.03557.x 11703406 (Pubitemid 33071077)
5. Functional food for pregnant, lactating women and in perinatal nutrition: a role for dietary fibres? Champ M, Hoebler C, Curr Opin Clin Nutr Metab Care 2009 12 6 565 574 10.1097/MCO.0b013e328331b4aa 19741518
6. The diversity of health effects of individual trans fatty acid isomers. Gebauer SK, Psota TL, Kris-Etherton PM, Lipids 2007 42 9 787 799 10.1007/s11745-007-3095-8 17694343 (Pubitemid 47592099)
7. Dietary intake of trans fatty acids and systemic inflammation in women. Mozaffarian D, Pischon T, Hankinson SE, Rifai N, Joshipura K, Willett WC, Rimm EB, Am J Clin Nutr 2004 79 4 606 612 15051604 (Pubitemid 41103904)
8. Hydrogenated fat intake during pregnancy and lactation modifies serum lipid profile and adipokine mRNA in 21-day-old rats. Pisani LP, Oyama LM, Bueno AA, Biz C, Albuquerque KT, Ribeiro EB, Oller do Nascimento CM, Nutrition 2008 24 3 255 261 10.1016/j.nut.2007.12.001 18178060
9. 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. de Oliveira JL, Oyama LM, Hachul AC, Biz C, Ribeiro EB, Oller do Nascimento CM, Pisani LP, Lipids Health Dis 2011 10 22 10.1186/1476-511X-10-22 21266050
10. Hydrogenated fat diet intake during pregnancy and lactation modifies the PAI-1 gene expression in white adipose tissue of offspring in adult life. Pisani LP, Nascimento CM O d, Bueno AA, Biz C, Albuquerque KT, Ribeiro EB, Oyama LM, Lipids Health Dis 2008 7 13 10.1186/1476-511X-7-13 18394153 (Pubitemid 351641919)
11. Trans fatty acids in maternal milk lead to cardiac insulin resistance in adult offspring. Osso FS, Moreira ASB, Teixeira MT, Pereira RO, Tavares do Carmo MG, Moura AS, Nutrition 2008 24 7-8 727 732 18499400
12. Obesity and impaired fibrinolysis: role of adipose production of plasminogen activator inhibitor-1. Skurk T, Hauner H, Int J Obes Relat Metab Disord 2004 28 11 1357 1364 10.1038/sj.ijo.0802778 15356668 (Pubitemid 39481839)
13. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Hajer GR, van Haeften TW, Visseren FL, Eur Heart J 2008 29 24 2959 2971 10.1093/eurheartj/ehn387 18775919
14. Metabolic, inflammatory, endothelial and haemostatic markers in a group of Italian obese children and adolescents. Giordano P, Del Vecchio GC, Cecinati V, Delvecchio M, Altomare M, De Palma F, De Mattia D, Cavallo L, Faienza MF, Eur J Pediatr 2011 170 7 845 850 10.1007/s00431-010-1356-7 21210148
15. Intake of trans fatty acids during gestation and lactation leads to hypothalamic inflammation via TLR4/NFκBp65 signaling in adult offspring. 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, Nascimento CM O d, Watanabe RH, Ribeiro EB, Pisani LP, J Nutr Biochem 2012 23 3 265 271 10.1016/j.jnutbio.2010.12.003 21543208
16. Evaluation of safety of inulin and oligofructose as dietary fiber. Carabin IG, Flamm WG, Regul Toxicol Pharmacol 1999 30 3 268 282 10.1006/rtph.1999.1349 10620476 (Pubitemid 30048997)
17. Dietary fructans and serum triacylglycerols: a meta-analysis of randomized controlled trials. Brighenti F, J Nutr 2007 137 11 2552S 2556S 17951501 (Pubitemid 350058734)
18. Inulin and oligofructose modulate lipid metabolism in animals: review of biochemical events and future prospects. Delzenne NM, Daubioul C, Neyrinck A, Lasa M, Taper HS, Br J Nutr 2002 87 Suppl 2 255 S259 12088526
19. Oligofructose modulates lipid metabolism alterations induced by a fat-rich diet in rats. Kok NN, Taper HS, Delzenne NM, J Appl Toxicol 1998 18 1 47 53 10.1002/(SICI)1099-1263(199801/02)18:1<47::AID-JAT474>3.0.CO;2-S 9526834 (Pubitemid 28101518)
20. Introducing inulin-type fructans. Roberfroid MB, Br J Nutr 2005 93 Suppl 1 13 S25 15877886
21. Inulin-type fructans: functional food ingredients. Roberfroid MB, J Nutr 2007 137 11 Suppl 2493S 2502S 17951492 (Pubitemid 350058725)
22. Inulin-type prebiotics-a review: part 1. Kelly G, Altern Med Rev 2008 13 4 315 329 19152479
23. Applications of inulin and oligofructose in health and nutrition. Kaur N, Gupta AK, J Biosci 2002 27 703 714 10.1007/BF02708379 12571376 (Pubitemid 36091305)
24. Inulin and oligofructose in the dietary fibre concept. Cherbut C, Br J Nutr 2002 87 Suppl 2 159 S162 12088513
25. Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Kleessen B, Hartmann L, Blaut M, Br J Nutr 2001 86 2 291 300 10.1079/BJN2001403 11502244 (Pubitemid 32780636)
26. Chicory fructooligosaccharides and the gastrointestinal tract. Roberfroid MB, Nutrition 2000 16 7-8 677 679 10906595 (Pubitemid 30445148)
27. Worlds within worlds: evolution of the vertebrate gut microbiota. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI, Nat Rev Microbiol 2008 6 10 776 788 10.1038/nrmicro1978 18794915
28. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Gibson GR, Roberfroid MB, J Nutr 1995 125 6 1401 1412 7782892
29. Gut microbiota and obesity. Krznarić Z, Vranešić Bender D, Kunović A, Kekez D, Stimac D, Dig Dis 2012 30 2 196 200 10.1159/000336965 22722438
30. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. Kim KA, Gu W, Lee IA, Joh EH, Kim DH, PLoS One 2012 7 10 47713 10.1371/journal.pone.0047713 23091640
31. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM, Diabetologia 2007 50 11 2374 2383 10.1007/s00125-007- 0791-0 17823788 (Pubitemid 47512397)
32. Metabolic diseases and pro- and prebiotics: mechanistic insights. Nakamura YK, Omaye ST, Nutr Metab (Lond) 2012 9 1 60 10.1186/1743-7075-9-60 22713169
33. TLR4 links innate immunity and fatty acid-induced insulin resistance. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS, J Clin Invest 2006 116 11 3015 3025 10.1172/JCI28898 17053832 (Pubitemid 44684486)
34. Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kappaB pathway in rat liver. Boden G, She P, Mozzoli M, Cheung P, Gumireddy K, Reddy P, Xiang X, Luo Z, Ruderman N, Diabetes 2005 54 12 3458 3465 10.2337/diabetes.54.12.3458 16306362 (Pubitemid 43334336)
35. Obesity and free fatty acids. Boden G, Endocrinol Metab Clin North Am 2008 37 3 635 646 10.1016/j.ecl.2008.06.007 18775356
36. Dietary fructans. Roberfroid MB, Delzenne NM, Annu Rev Nutr 1998 18 117 143 10.1146/annurev.nutr.18.1.117 9706221 (Pubitemid 28366863)
37. Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics. Macfarlane GT, Macfarlane S, J Clin Gastroenterol 2011 45 Suppl 3 120 127 21992950
38. Butyrate: implications for intestinal function. Leonel AJ, Alvarez-Leite JI, Curr Opin Clin Nutr Metab Care 2012 15 5 474 479 10.1097/MCO. 0b013e32835665fa 22797568
39. Milk oligosaccharides and metabolism in infants. Rudloff S, Kunz C, Adv Nutr 2012 3 3 398S 405S 10.3945/an.111.001594 22585918
40. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Kunz C, Rudloff S, Baier W, Klein N, Strobel S, Annu Rev Nutr 2000 20 699 722 10.1146/annurev.nutr.20.1.699 10940350
41. The human milk microbiota: origin and potential roles in health and disease. Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM, Pharmacol Res 2013 69 1 1 10 10.1016/j.phrs.2012.09.001 22974824
42. AIN-93 purified diets for laboratory rodents: final report of the american institute of nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. Reeves PG, Nielsen FH, Fahey GC Jr, J Nutr 1993 123 11 1939 1951 8229312 (Pubitemid 23342492)
43. Components of the AIN-93 diets as improvements in the AIN-76A diet. Reeves PG, J Nutr 1997 127 5 Suppl 838S 841S 9164249 (Pubitemid 27209452)
44. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Livak KJ, Schmittgen TD, Methods 2001 25 4 402 408 10.1006/meth.2001.1262 11846609 (Pubitemid 34164012)
45. Inulin-type prebiotics: a review (part 2). Greg Kelly ND, Altern Med Rev 2009 14 1 36 55 19364192
46. A maternal high-protein diet predisposes female offspring to increased fat mass in adulthood whereas a prebiotic fibre diet decreases fat mass in rats. Hallam MC, Reimer RA, Br J Nutr 2013 110 9 1732 1741 10.1017/S0007114513000998 23561448
47. 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. Maurer AD, Reimer RA, Br J Nutr 2011 105 3 329 338 10.1017/ S0007114510003533 21129233
48. Impaired barrier function by dietary fructo-oligosaccharides (FOS) in rats is accompanied by increased colonic mitochondrial gene expression. Rodenburg W, Keijer J, Kramer E, Vink C, van der Meer R, Bovee-Oudenhoven IM, BMC Genomics 2008 9 144 10.1186/1471-2164-9-144 18371188 (Pubitemid 351546702)
49. Effect of prebiotic fibre supplementation on hepatic gene expression and serum lipids: a dose-response study in JCR:LA-cp rats. Parnell JA, Reimer RA, Br J Nutr 2010 103 11 1577 1584 10.1017/S0007114509993539 20021705
50. Role of body fat distribution and the metabolic complications of obesity. Jensen MD, J Clin Endocrinol Metab 2008 93 11 Suppl 1 57 S63 18987271
51. Pioglitazone increases non-esterified fatty acid clearance in upper body obesity. Shadid S, Jensen MD, Diabetologia 2006 49 1 149 157 10.1007/s00125-005-0051-0 16323003 (Pubitemid 43151626)
52. Effects of inulin-type fructans on lipid metabolism in man and in animal models. Beylot M, Br J Nutr 2005 93 Suppl 1 163 168 15877890
53. Involvement of lipogenesis in the lower VLDL secretion induced by oligofructose in rats. Kok NN, Roberfroid M, Robert A, Delzenne N, Br J Nutr 1996 76 6 881 890 10.1079/BJN19960094 9014656 (Pubitemid 27029128)
54. Gastrointestinal effects of prebiotics. Cummings JH, Macfarlane GT, Br J Nutr 2002 87 Suppl 2 145 S151 12088511
55. Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. Pan XD, Chen FQ, Wu TX, Tang HG, Zhao ZY, J Zhejiang Univ Sci B 2009 10 4 258 263 10.1631/jzus.B0820261 19353743
56. Prebiotic fibres dose-dependently increase satiety hormones and alter bacteroidetes and firmicutes in lean and obese JCR:LA-cp rats. Parnell JA, Reimer RA, Br J Nutr 2012 107 4 601 613 10.1017/S0007114511003163 21767445
57. Lactobacillus plantarum 299v inhibits escherichia coli-induced intestinal permeability. Mangell P, Nejdfors P, Wang M, Ahrné S, Weström B, Thorlacius H, Jeppsson B, Dig Dis Sci 2002 47 3 511 516 10.1023/A:1017947531536 11911334 (Pubitemid 34218876)
58. Adhesive capability of lactobacillus plantarum 299v is important for preventing bacterial translocation in endotoxemic rats. Mangell P, Lennernäs P, Wang M, Olsson C, Ahrné S, Molin G, Thorlacius H, Jeppsson B, APMIS 2006 114 9 611 618 10.1111/j.1600-0463.2006.apm-369.x 16948813 (Pubitemid 44337339)
59. Effect of probiotics lactobacillus and Bifidobacterium on gut-derived lipopolysaccharides and inflammatory cytokines: an in vitro study using a human colonic microbiota model. Rodes L, Khan A, Paul A, Coussa-Charley M, Marinescu D, Tomaro-Duchesneau C, Shao W, Kahouli I, Prakash S, J Microbiol Biotechnol 2013 23 4 518 526 10.4014/jmb.1205.05018 23568206
60. Dietary fructooligosaccharides increase intestinal permeability in rats. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Van der Meer R, J Nutr 2005 135 4 837 842 15795444 (Pubitemid 40464114)
61. Dietary fructooligosaccharides affect intestinal barrier function in healthy men. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Katan MB, van der Meer R, J Nutr 2006 136 1 70 74 16365061 (Pubitemid 43156487)
62. Dietary fructo-oligosaccharides dose-dependently increase translocation of salmonella in rats. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Van der Meer R, J Nutr 2003 133 7 2313 2318 12840199 (Pubitemid 36841558)
63. Oligofructose supplementation (10%) during pregnancy and lactation does not change the inflammatory effect of concurrent trans fatty acid ingestion on 21-day-old offspring. Hachul AC, Mennitti LV, de Oliveira JL, Moreno MF, Okuda MH, Dos Santos B, Oyama LM, Ribeiro EB, do Nascimento CM, Pisani LP, Lipids Health Dis 2013 12 59 10.1186/1476-511X-12-59 23634906