Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Maternal preconceptional nutrition leads to variable fat deposition and gut dimensions of adult offspring mice (C57BL/6JBom)

International Journal of Obesity volume 34, pages 1618–1624 (2010)Cite this article

Subjects

Abstract

Background:

Maternal nutrition during pregnancy or lactation may affect the chance of offspring becoming obese as adults, but little is known regarding the possible role of maternal nutrition before conception. In this study, we investigate how variable protein and carbohydrate content of the diet consumed before pregnancy affects fat deposition and gut dimensions of offspring mice.

Methods:

Eight-week-old female mice (C57BL/6JBom) were fed isocaloric low protein (8.4% protein; LP), standard protein (21.5% protein; ST) or high protein (44.2% protein; HP) diets. After 8 weeks of feeding, females were mated and fed a standard laboratory chow diet (22.5% protein) throughout periods of mating, gestation, lactation and weaning. Offspring mice were fed the same standard diet up to 46 days of age. Then offspring were killed and measures of dissected fat deposits and of the digestive system were taken.

Results:

Fat deposition of the offspring was significantly affected by preconceptional maternal nutrition and the effects differed between sexes. Male offspring deposited most fat when mothers were fed the LP diet, whereas female offspring deposited most fat when mothers were fed the ST diet. The mass and length of the digestive organs were affected by preconceptional maternal nutrition. Total gut from pyloric sphincter to anus was significantly shorter and dry mass was heavier in mice whose mothers were fed LP diets compared with offspring of mothers fed ST diets or HP diets. There was no significant effect of maternal nutrition on dry mass of the stomach or ceca.

Conclusion:

Our study shows that preconceptional nutrition can have important influence on several body features of offspring in mice, including body composition and dimensions of the digestive system.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  1. WHO homepage. (http://www.who.int/mediacentre/factsheets/fs311/en/index.html).

  2. Hossain P, Kawar B, El Nahas M . Obesity and diabetes in the developing world—a growing challenge. N Engl JMed 2007; 356: 213–215.

    Article  CAS  Google Scholar 

  3. Bellinger L, Langley-Evans SC . Fetal programming of appetite by exposure to a maternal low-protein diet in the rat. Clin Sci 2005; 109: 413–420.

    Article  CAS  Google Scholar 

  4. Taylor PD, Poston L . Developmental programming of obesity in mammals. Exp Physiol 2007; 92: 287–298.

    Article  CAS  Google Scholar 

  5. Rasmussen KM, Kjolhede CL . Maternal obesity: a problem for both mother and child. Obesity 2008; 16: 929–931.

    Article  Google Scholar 

  6. Lucas A . Programming by early nutrition: an experimental approach. J Nutr 1998; 128: 401S–406S.

    Article  CAS  Google Scholar 

  7. Patel MS, Srinivasan M . Metabolic programming: causes and consequences. J Biol Chem 2002; 277: 1629–1632.

    Article  CAS  Google Scholar 

  8. Robinson S . Metabolic programming during pregnancy: epidemiological studies in humans. Genes Nutr 2007; 2: 31–32.

    Article  CAS  Google Scholar 

  9. Berney DM, Desai M, Palmer DJ, Greenwald S, Brown A, Hales CN et al. The effects of maternal protein deprivation on the fetal rat pancreas: major structural changes and their recuperation. J Pathol 1997; 183: 109–115.

    Article  CAS  Google Scholar 

  10. Latorraca MQ, Reis MAB, Carneiro EM, Mello MAR, Velloso LA, Saad MJA et al. Protein deficiency and nutritional recovery modulate insulin secretion and the early steps of insulin action in rats. J Nutr 1998; 128: 1643–1649.

    Article  CAS  Google Scholar 

  11. Ozanne SE, Lewis R, Jennings BJ, Hales CN . Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet. Clin Sci 2004; 106: 141–145.

    Article  CAS  Google Scholar 

  12. Bellinger L, Lilley C, Langley-Evans SC . Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Br J Nutr 2004; 92: 513–520.

    Article  CAS  Google Scholar 

  13. Ravelli GP, Stein ZA, Susser MW . Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 1976; 295: 349–353.

    Article  CAS  Google Scholar 

  14. Baker JL . Maternal prepregnant body mass index, duration of breastfeeding, and timing of complementary food introduction are associated with infant weight gain. Am J Clin Nutr 2004; 80: 1579–1588.

    Article  CAS  Google Scholar 

  15. Demmelmair H, von Rosen J, Koletzko B . Long-term consequences of early nutrition. Early Hum Dev 2006; 82: 567–574.

    Article  Google Scholar 

  16. Langley-Evans SC, Welham SJM, Jackson AA . Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 1999; 64: 965–974.

    Article  CAS  Google Scholar 

  17. Lucas A, Baker BA, Desai M, Hales CN . Nutrition in pregnant or lactating rats programs lipid metabolism in the offspring. Br J Nutr 1996; 76: 605–612.

    Article  CAS  Google Scholar 

  18. Joshi S, Garole V, Daware M, Girigosavi S, Rao S . Maternal protein restriction before pregnancy affects vital organs of offspring in Wistar rats. Metabolism 2003; 52: 13–18.

    Article  CAS  Google Scholar 

  19. Hartvigsen MS, Mu HL, Høy CE . Influence of maternal dietary n-3 fatty acids on breast milk and liver lipids of rat dams and offspring—a preliminary study. Nutr Res 2003; 23: 747–760.

    Article  Google Scholar 

  20. Joshi S, Rao S, Golwilkar A, Patwardhan M, Bhonde R . Fish oil supplementation of rats during pregnancy reduces adult disease risks in their offspring. J Nutr 2003; 133: 3170–3174.

    Article  CAS  Google Scholar 

  21. Mathews F, Yudkin P, Neil A . Influence of maternal nutrition on outcome of pregnancy: prospective cohort study. BMJ 1999; 319: 339–343.

    Article  CAS  Google Scholar 

  22. Javaid MK, Crozier SR, Harvey NC, Gale CR, Dennison EM, Boucher BJ et al. Maternal vitamin D status during pregnancy and childhood bone mass at age 9 years: a longitudinal study. Lancet 2006; 367: 36–43.

    Article  CAS  Google Scholar 

  23. Watson PE, McDonald BW . Seasonal variation of nutrient intake in pregnancy: effects on infant measures and possible influence on diseases related to season of birth. Eur J Clin Nutr 2007; 61: 1271–1280.

    Article  CAS  Google Scholar 

  24. Hostetler CE, Kincaid RL, Mirando MA . The role of essential trace elements in embryonic and fetal development in livestock. Vet J 2003; 166: 125–139.

    Article  CAS  Google Scholar 

  25. Saldana TM, Siega-Riz AM, Adair LS . Effect of macronutrient intake on the development of glucose intolerance during pregnancy. Am J Clin Nutr 2004; 79: 479–486.

    Article  CAS  Google Scholar 

  26. Moore VM, Davies MJ . Diet during pregnancy, neonatal outcomes and later health. Reprod Fertil Dev 2005; 17: 341–348.

    Article  Google Scholar 

  27. Gorski JN, Dunn-Meynell AA, Hartman TG, Levin BE . Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol 2006; 291: R768–R778.

    CAS  Google Scholar 

  28. Howie GJ, Sloboda DM, Kamal T, Vickers MH . Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol 2009; 587: 905–915.

    Article  CAS  Google Scholar 

  29. Hill RB, Prosper J, Hirschfield JS, Kern Jr F . Protein starvation and the small intestine. 1. The growth and morphology of the small intestine in weanling rats. Exp Mol Pathol 1968; 8: 66–74.

    Article  Google Scholar 

  30. Buddington RK, Chen JW, Diamond J . Genetic and phenotypic adaptation of intestinal nutrient transport to diet in fish. J Physiol 1987; 393: 261–281.

    Article  CAS  Google Scholar 

  31. Raubenheimer D, Bassil K . Separate effects of macronutrient concentration and balance on plastic gut responses in locusts. J Comp Physiol B 2007; 177: 849–855.

    Article  CAS  Google Scholar 

  32. Sørensen A, Mayntz D, Raubenheimer D, Simpson SJ . Protein-leverage in mice: the geometry of macronutrient balancing and consequences for fat deposition. Obesity 2008; 16: 566–571.

    Article  Google Scholar 

  33. Simpson SJ, Batley R, Raubenheimer D . Geometric analysis of macronutrient intake in humans: the power of protein? Appetite 2003; 41: 123–140.

    Article  CAS  Google Scholar 

  34. Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, Wood JT et al. Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 2009; 20: 685–690.

    Article  Google Scholar 

  35. Simpson SJ, Raubenheimer D . Obesity: the protein leverage hypothesis. Obes Rev 2005; 6: 133–142.

    Article  CAS  Google Scholar 

  36. Villar J, Cogswell M, Kestler E, Castillo P, Menendez R, Repke JT . Effect of fat and fat-free mass deposition during pregnancy on birth-weight. Am J Obstet Gynecol 1992; 167: 1344–1352.

    Article  CAS  Google Scholar 

  37. Mardonese-Santander F, Salazar G, Rosso P, Villarroel L . Maternal body composition near term and birth weight. Obstet Gynecol 1998; 91: 873–877.

    Google Scholar 

  38. Cripps RL, Green LR, Thompson J, Martin-Gronert MS, Monk M, Sheldon IM et al. The effect of maternal body composition score before and during pregnancy on the glucose tolerance of adult sheep offspring. Reprod Sci 2008; 15: 448–456.

    Article  CAS  Google Scholar 

  39. Bouret SG . Early life origins of obesity: role of hypothalamic programming. J Pediatr Gastroenterol Nutr 2009; 48: S31–S38, Supplement 1.

    Article  Google Scholar 

  40. Grove KL, Allen S, Grayson BE, Smith MS . Postnatal development of the hypothalamic neuropeptide Y system. Neuroscience 2003; 116: 393–406.

    Article  CAS  Google Scholar 

  41. Grove KL, Grayson BE, Glavas MM, Xiao XQ, Smith MS . Development of metabolic systems. Physiol Behav 2005; 86: 646–660.

    Article  CAS  Google Scholar 

  42. Rinaman L . Postnatal development of hypothalamic inputs to the dorsal vagal complex in rats. Physiol Behav 2003; 79: 65–70.

    Article  CAS  Google Scholar 

  43. Vickers MH, Breier BH, McCarthy D, Gluckman PD . Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol 2003; 285: R271–R273.

    CAS  Google Scholar 

  44. Sørensen A, Mayntz D, Simpson SJ, Raubenheimer D . Dietary ratio of protein to carbohydrate induces plastic responses in the gastrointestinal tract of mice. J Comp Physiol (B) 2010; 180: 259–266.

    Article  Google Scholar 

  45. Buddington RK, Diamond JM . Pyloric caeca of fish: a ‘new’ absorptive organ. Am J Physiol 1987; 252: G65–G67 (part 1).

    CAS  PubMed  Google Scholar 

  46. Ong KK, Diderholm B, Salzano G, Wingate D, Hughes IA, MacDougall J et al. Pregnancy insulin, glucose, and BMI contribute to birth outcomes in nondiabetic mothers. Diabetes Care 2008; 31: 2193–2197.

    Article  CAS  Google Scholar 

  47. Hull HR, Dinger MK, Knehans AW, Thompson DM, Fields DA . Impact of maternal body mass index on neonate birthweight and body composition. Am J Obstet Gynecol 2008; 198, (Article Number: 416.e1).

    Article  Google Scholar 

  48. Yang W, Kelly T, He J . Genetic epidemiology of obesity. Epidemiol Rev 2007; 29: 49–61.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Allan Sørensen who instructed us in the dissection of fat deposits and intestines in the mice. We are grateful to Heidi Meldgaard, Rasmus Østergaard and Vibeke H Lund for assistance with care-taking of the mice. This study was supported by grants from the Danish Research Council to DM, TW and HM. DR receives support from the National Research Centre for Growth and Development, New Zealand.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Zoophysiology, Aarhus University, Aarhus, Denmark

    E L K Mortensen, T Wang & H Malte

  2. Institute of Natural Sciences, Massey University, Albany, New Zealand

    D Raubenheimer

  3. Department of Ecology and Genetics, University of Aarhus, Aarhus, Denmark

    D Mayntz

  4. Department of Genetics and Biotechnology, Research Centre Foulum, University of Aarhus, Tjele, Denmark

    D Mayntz

Authors
  1. E L K Mortensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H Malte
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D Raubenheimer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D Mayntz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D Mayntz.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mortensen, E., Wang, T., Malte, H. et al. Maternal preconceptional nutrition leads to variable fat deposition and gut dimensions of adult offspring mice (C57BL/6JBom). Int J Obes 34, 1618–1624 (2010). https://doi.org/10.1038/ijo.2010.91

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2010.91

Keywords

This article is cited by

Search

Advanced search

Quick links