Skip to main content
×
×
Home

Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet

  • Asli Akyol (a1), Sarah McMullen (a1) and Simon C. Langley-Evans (a1)
Abstract

In addition to being a risk factor for adverse outcomes of pregnancy, maternal obesity may play a role in determining the long-term disease patterns observed in the resulting offspring, with metabolic and dietary factors directly programming fetal development. The present study evaluated the potential for feeding rats an obesogenic cafeteria diet (O) pre-pregnancy, during pregnancy, during lactation and for the offspring post-weaning, to programme glucose tolerance. Early-life exposure to an O diet had no significant effect on offspring food intake. Early-life programming associated with O feeding to induce maternal obesity was associated with reduced adiposity in offspring weaned onto low-fat chow. Adult offspring exposed to an O diet in early life and weaned on a chow diet had low fasting glucose and insulin concentrations and appeared to be more sensitive to insulin during an intraperitoneal glucose tolerance test. When weaned on an O diet, male offspring were more prone to glucose intolerance than females. On the basis of the area under the glucose curve, maternal O feeding at any point from pre-mating to lactation was associated with impaired glucose tolerance. The mechanism for this was not identified, although increased hepatic expression of Akt2 may have indicated disturbance of insulin signalling pathways. The observations in the present study confirm that maternal overnutrition and obesity during pregnancy are risk factors for metabolic disturbance in the resulting offspring. Although the effects on glucose homeostasis were independent of offspring adiposity, the programming of a glucose-intolerant phenotype was only observed when offspring were weaned on a diet that induced greater fat deposition.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Professor S. C. Langley-Evans, fax +44 1159516122, email simon.langley-evans@nottingham.ac.uk
References
Hide All
1 Barker, DJ (2002) Fetal programming of coronary heart disease. Trends Endocrinol Metab 13, 364368.
2 Barker, DJ, Hales, CN, Fall, CH, et al. (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 6267.
3 Eriksson, JG, Forsén, T, Tuomilehto, J, et al. (2002) Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia 45, 342348.
4 Bellinger, L, Sculley, DV & Langley-Evans, SC (2006) Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Intl J Obes (Lond) 30, 729738.
5 Langley-Evans, SC & Jackson, AA (1996) Intrauterine programming of hypertension: nutrient–hormone interactions. Nutr Rev 54, 163169.
6 Langley-Evans, SC & Nwagwu, MO (1998) Impaired growth and increased activities of glucocorticoid sensitive enzyme activities in tissues of rat fetuses exposed to maternal low protein diets. Life Sci 63, 605615.
7 Gambling, L, Dunford, S, Wallace, DI, et al. (2003) Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol 552, 603610.
8 Vickers, MH, Breier, BH, Cutfield, WS, et al. (2000) Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 279, E83E87.
9 Langley-Evans, SC (2009) Nutritional programming of disease: unravelling the mechanism. J Anat 251, 3651.
10 World Health Report (2002) Reducing Risks, Promoting Healthy Life. Geneva: WHO.
11 Bodnar, LM, Siega-Riz, AM, Simhan, HN, et al. (2010) Severe obesity, gestational weight gain, and adverse birth outcomes. Am J Clin Nutr 91, 16421648.
12 Sebire, NJ, Jolly, M, Harris, JP, et al. (2001) Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord 25, 11751182.
13 Walsh, SW (2007) Obesity: a risk factor for preeclampsia. Trends Endocrinol Metab 18, 365370.
14 Calvert, JW, Lefer, DJ, Gundewar, S, et al. (2009) Developmental programming resulting from maternal obesity in mice: effects on myocardial ischaemia–reperfusion injury. Exp Physiol 94, 805814.
15 Byers, BD, Betancourt, A, Lu, F, et al. (2009) The effect of prepregnancy obesity and sFlt-1-induced preeclampsia-like syndrome on fetal programming of adult vascular function in a mouse model. Am J Obstet Gynecol 200, 432e1432e7.
16 Mitra, A, Alvers, KM, Crump, EM, et al. (2009) Effect of high-fat diet during gestation, lactation, or postweaning on physiological and behavioral indexes in borderline hypertensive rats. Am J Physiol Regul Integr Comp Physiol 296, R20R28.
17 Shankar, K, Harrell, A, Liu, X, et al. (2008) Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 294, R528R538.
18 Samuelsson, AM, Matthews, PA, Argenton, M, 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, 383392.
19 Bayol, SA, Simbi, BH, Bertrand, JA, et al. (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, 32193230.
20 Akyol, A, Langley-Evans, SC & McMullen, S (2009) Obesity induced by cafeteria feeding and pregnancy outcome in the rat. Br J Nutr 102, 16011610.
21 Shafat, A, Murray, B & Rumsey, D (2010) Energy density in cafeteria diet induced hyperphagia in the rat. Appetite 52, 3438.
22 Rothwell, NJ & Stock, MJ (1979) Regulation of energy-balance in 2 models of reversible obesity in the rat. J Comp Physiol Psychol 93, 10241034.
23 González-Yanes, C, Serrano, A, Bermúdez-Silva, FJ, et al. (2005) Oleylethanolamide impairs glucose tolerance and inhibits insulin-stimulated glucose uptake in rat adipocytes through p38 and JNK MAPK pathways. Am J Physiol Endocrinol Metab 289, E923E929.
24 Trinder, P (1969) Determination of blood glucose using an oxidase–peroxidase system with a non-carcinogenic chromogen. J Clin Pathol 22, 158161.
25 McMullen, S & Langley-Evans, SC (2005) Maternal low-protein diet in rat pregnancy programs blood pressure through sex-specific mechanisms. Am J Physiol Regul Integr Comp Physiol 288, R85R90.
26 Pirkola, J, Pouta, A, Bloigu, A, et al. (2010) Risks of overweight and abdominal obesity at age 16 years associated with prenatal exposures to maternal prepregnancy overweight and gestational diabetes mellitus. Diabetes Care 33, 11151121.
27 Picó, C, Oliver, P, Sánchez, J, et al. (2007) The intake of physiological doses of leptin during lactation in rats prevents obesity in later life. Int J Obes (Lond) 31, 11991209.
28 Sánchez, J, Priego, T, Palou, M, et al. (2008) Oral supplementation with physiological doses of leptin during lactation in rats improves insulin sensitivity and affects food preferences later in life. Endocrinology 149, 733740.
29 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, 458462.
30 Gorski, JN, Dunn-Meynell, AA, Hartman, TG, et al. (2006) Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol Regul Integr Comp Physiol 291, R768R778.
31 Plagemann, A, Harder, T, Rake, A, et al. (1999) Increased number of galanin-neurons in the paraventricular hypothalamic nucleus of neonatally overfed weanling rats. Brain Res 818, 160163.
32 Bayol, SA, Simbi, BH, Fowkes, RC, et al. (2010) A maternal ‘junk food’ diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology 151, 14511461.
33 Nivoit, P, Morens, C, Van Assche, FA, et al. (2009) Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia 52, 11331142.
34 Shankar, K, Kang, P, Harrell, A, et al. (2010) Maternal overweight programs insulin and adiponectin signaling in the offspring. Endocrinology 151, 25772589.
35 Erhuma, A, Salter, AM, Sculley, DV, et al. (2007) Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab 292, E1702E1714.
36 Langley, SC, Browne, RF & Jackson, AA (1994) Altered glucose tolerance in rats exposed to maternal low protein diets in utero. Comp Biochem Physiol Physiol 109, 223229.
37 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, 951961.
38 Sugden, MC & Holness, MJ (2002) Gender-specific programming of insulin secretion and action. J Endocrinol 75, 757767.
39 Fernandez-Twinn, DS, Wayman, A, Ekizoglou, S, et al. (2005) Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol 288, R368R373.
40 Chamson-Reig, A, Thyssen, SM, Hill, DJ, et al. (2009) Exposure of the pregnant rat to low protein diet causes impaired glucose homeostasis in the young adult offspring by different mechanisms in males and females. Exp Biol Med (Maywood) 234, 14251436.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 13
Total number of PDF views: 207 *
Loading metrics...

Abstract views

Total abstract views: 361 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 23rd June 2018. This data will be updated every 24 hours.