Skip to main content
Erschienen in: European Journal of Nutrition 6/2016

22.08.2015 | Original Contribution

Disproportionately increased 24-h energy expenditure and fat oxidation in young men with low birth weight during a high-fat overfeeding challenge

verfasst von: Charlotte Brøns, Søren K. Lilleøre, Arne Astrup, Allan Vaag

Erschienen in: European Journal of Nutrition | Ausgabe 6/2016

Einloggen, um Zugang zu erhalten

Abstract

Background

Low birth weight (LBW) associates with increased risk of developing type 2 diabetes. LBW individuals exhibit disproportionately reduced peripheral insulin action and increased fat oxidation after a 5-day high-fat overfeeding (HFO) challenge. Furthermore, LBW men exhibit increased nocturnal fat oxidation during energy balance and low energy expenditure (EE) during fasting. We hypothesized that short-term HFO could further unmask key defects of whole-body energy metabolism in LBW men.

Methods

Eighteen LBW (2717 ± 268 g) and 26 normal birth weight (NBW) (3893 ± 207 g) healthy young men were included in a 5-day HFO (60 E % fat, +50 % calories) study. The 24-h EE, respiratory quotient and substrate oxidation rates were assessed by indirect calorimetry using respiratory chambers.

Results

After adjusting for body composition, the LBW subjects displayed increased nighttime EE (P = 0.02) compared with NBW controls during HFO. Nighttime glucose oxidation rate was decreased (P = 0.06, adjusted P = 0.05), while both adjusted 24-h (P = 0.07) and nighttime (P = 0.02) fat oxidation rate was elevated in LBW subjects. The relative contribution of fat oxidation to EE was increased in LBW compared with NBW men during the entire 24-h period (P = 0.06) and during nighttime (P = 0.03).

Conclusions

We suggest that disproportionally enhanced fat oxidation in LBW individuals during short-term HFO represents a compensatory response to reduced subcutaneous adipose tissue expandability and storage capacity. The extent to which this mechanism may lead to, or be replaced by insulin resistance, ectopic fat accumulation and/or glucose intolerance during long-term HFO in LBW needs further studies.
Literatur
1.
Zurück zum Zitat Alibegovic AC, Højbjerre L, Sonne MP, Van HG, Alsted TJ, Kiens B, Stallknecht B, Dela F, Vaag A (2010) Increased rate of whole body lipolysis before and after 9 days of bed rest in healthy young men born with low birth weight. Am J Physiol Endocrinol Metab 298:E555–E564CrossRef Alibegovic AC, Højbjerre L, Sonne MP, Van HG, Alsted TJ, Kiens B, Stallknecht B, Dela F, Vaag A (2010) Increased rate of whole body lipolysis before and after 9 days of bed rest in healthy young men born with low birth weight. Am J Physiol Endocrinol Metab 298:E555–E564CrossRef
2.
Zurück zum Zitat Astrup A, Buemann B, Christensen NJ, Madsen J (1992) 24-hour energy expenditure and sympathetic activity in postobese women consuming a high-carbohydrate diet. Am J Physiol 262:E282–E288 Astrup A, Buemann B, Christensen NJ, Madsen J (1992) 24-hour energy expenditure and sympathetic activity in postobese women consuming a high-carbohydrate diet. Am J Physiol 262:E282–E288
3.
Zurück zum Zitat Brøns C, Jacobsen S, Hiscock N, White A, Nilsson E, Dunger D, Astrup A, Quistorff B, Vaag A (2012) Effects of high-fat overfeeding on mitochondrial function, glucose and fat metabolism, and adipokine levels in low-birth-weight subjects. Am J Physiol Endocrinol Metab 302:E43–E51CrossRef Brøns C, Jacobsen S, Hiscock N, White A, Nilsson E, Dunger D, Astrup A, Quistorff B, Vaag A (2012) Effects of high-fat overfeeding on mitochondrial function, glucose and fat metabolism, and adipokine levels in low-birth-weight subjects. Am J Physiol Endocrinol Metab 302:E43–E51CrossRef
4.
Zurück zum Zitat Brøns C, Lilleøre SK, Jensen CB, Toubro S, Vaag A, Astrup A (2013) Increased nocturnal fat oxidation in young healthy men with low birth weight: results from 24-h whole-body respiratory chamber measurements. Metabolism 62:709–716CrossRef Brøns C, Lilleøre SK, Jensen CB, Toubro S, Vaag A, Astrup A (2013) Increased nocturnal fat oxidation in young healthy men with low birth weight: results from 24-h whole-body respiratory chamber measurements. Metabolism 62:709–716CrossRef
5.
Zurück zum Zitat Brøns C, Jacobsen S, Nilsson E, Rönn T, Jensen CB, Storgaard H, Poulsen P, Groop L, Ling C, Astrup A, Vaag A (2010) Deoxyribonucleic acid methylation and gene expression of PPARGC1A in human muscle is influenced by high-fat overfeeding in a birth-weight-dependent manner. J Clin Endocrinol Metab 95:3048–3056CrossRef Brøns C, Jacobsen S, Nilsson E, Rönn T, Jensen CB, Storgaard H, Poulsen P, Groop L, Ling C, Astrup A, Vaag A (2010) Deoxyribonucleic acid methylation and gene expression of PPARGC1A in human muscle is influenced by high-fat overfeeding in a birth-weight-dependent manner. J Clin Endocrinol Metab 95:3048–3056CrossRef
6.
Zurück zum Zitat Brøns C, Jensen CB, Storgaard H, Alibegovic A, Jacobsen S, Nilsson E, Astrup A, Quistorff B, Vaag A (2008) Mitochondrial function in skeletal muscle is normal and unrelated to insulin action in young men born with low birth weight. J Clin Endocrinol Metab 93:3885–3892CrossRef Brøns C, Jensen CB, Storgaard H, Alibegovic A, Jacobsen S, Nilsson E, Astrup A, Quistorff B, Vaag A (2008) Mitochondrial function in skeletal muscle is normal and unrelated to insulin action in young men born with low birth weight. J Clin Endocrinol Metab 93:3885–3892CrossRef
7.
Zurück zum Zitat Brøns C, Jensen CB, Storgaard H, Hiscock NJ, White A, Appel JS, Jacobsen S, Nilsson E, Larsen CM, Astrup A, Quistorff B, Vaag A (2009) Impact of short-term high-fat feeding on glucose and insulin metabolism in young healthy men. J Physiol 587:2387–2397CrossRef Brøns C, Jensen CB, Storgaard H, Hiscock NJ, White A, Appel JS, Jacobsen S, Nilsson E, Larsen CM, Astrup A, Quistorff B, Vaag A (2009) Impact of short-term high-fat feeding on glucose and insulin metabolism in young healthy men. J Physiol 587:2387–2397CrossRef
8.
Zurück zum Zitat Elia M, Livesey G (1992) Energy expenditure and fuel selection in biological systems: the theory and practice of calculations based on indirect calorimetry and tracer methods. World Rev Nutr Diet 70:68–131CrossRef Elia M, Livesey G (1992) Energy expenditure and fuel selection in biological systems: the theory and practice of calculations based on indirect calorimetry and tracer methods. World Rev Nutr Diet 70:68–131CrossRef
9.
Zurück zum Zitat Evans MD, Cooke MS (2004) Factors contributing to the outcome of oxidative damage to nucleic acids. Bioessays 26:533–542CrossRef Evans MD, Cooke MS (2004) Factors contributing to the outcome of oxidative damage to nucleic acids. Bioessays 26:533–542CrossRef
10.
Zurück zum Zitat Gillberg L, Jacobsen SC, Ronn T, Brons C, Vaag A (2014) PPARGC1A DNA methylation in subcutaneous adipose tissue in low birth weight subjects—impact of 5 days of high-fat overfeeding. Metabolism 63:263–271CrossRef Gillberg L, Jacobsen SC, Ronn T, Brons C, Vaag A (2014) PPARGC1A DNA methylation in subcutaneous adipose tissue in low birth weight subjects—impact of 5 days of high-fat overfeeding. Metabolism 63:263–271CrossRef
11.
Zurück zum Zitat Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303:1019–1022CrossRef Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD (1991) Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303:1019–1022CrossRef
12.
Zurück zum Zitat Hales CN, Barker DJP (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601CrossRef Hales CN, Barker DJP (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595–601CrossRef
13.
Zurück zum Zitat Harder T, Rodekamp E, Schellong K, Dudenhausen JW, Plagemann A (2007) Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol 165:849–857CrossRef Harder T, Rodekamp E, Schellong K, Dudenhausen JW, Plagemann A (2007) Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol 165:849–857CrossRef
14.
Zurück zum Zitat Højbjerre L, Alibegovic AC, Sonne MP, Dela F, Vaag A, Bruun JM, Stallknecht B (2011) Increased lipolysis but diminished gene expression of lipases in subcutaneous adipose tissue of healthy young males with intrauterine growth retardation. J Appl Physiol 111:1863–1870CrossRef Højbjerre L, Alibegovic AC, Sonne MP, Dela F, Vaag A, Bruun JM, Stallknecht B (2011) Increased lipolysis but diminished gene expression of lipases in subcutaneous adipose tissue of healthy young males with intrauterine growth retardation. J Appl Physiol 111:1863–1870CrossRef
15.
Zurück zum Zitat Holloszy JO (2013) “Deficiency” of mitochondria in muscle does not cause insulin resistance. Diabetes 62:1036–1040CrossRef Holloszy JO (2013) “Deficiency” of mitochondria in muscle does not cause insulin resistance. Diabetes 62:1036–1040CrossRef
16.
Zurück zum Zitat Jacobsen SC, Gillberg L, Bork-Jensen J, Ribel-Madsen R, Lara E, Calvanese V, Ling C, Fernandez AF, Fraga MF, Poulsen P, Brons C, Vaag A (2014) Young men with low birthweight exhibit decreased plasticity of genome-wide muscle DNA methylation by high-fat overfeeding. Diabetologia 57:1154–1158CrossRef Jacobsen SC, Gillberg L, Bork-Jensen J, Ribel-Madsen R, Lara E, Calvanese V, Ling C, Fernandez AF, Fraga MF, Poulsen P, Brons C, Vaag A (2014) Young men with low birthweight exhibit decreased plasticity of genome-wide muscle DNA methylation by high-fat overfeeding. Diabetologia 57:1154–1158CrossRef
17.
Zurück zum Zitat Jørgensen SW, Brons C, Bluck L, Hjort L, Faerch K, Thankamony A, Gillberg L, Friedrichsen M, Dunger DB, Vaag AA (2015) Metabolic response to 36 hours of fasting in young men born small vs appropriate for gestational age. Diabetologia 58:178–187CrossRef Jørgensen SW, Brons C, Bluck L, Hjort L, Faerch K, Thankamony A, Gillberg L, Friedrichsen M, Dunger DB, Vaag AA (2015) Metabolic response to 36 hours of fasting in young men born small vs appropriate for gestational age. Diabetologia 58:178–187CrossRef
18.
Zurück zum Zitat Jumpertz R, Hanson RL, Sievers ML, Bennett PH, Nelson RG, Krakoff J (2011) Higher energy expenditure in humans predicts natural mortality. J Clin Endocrinol Metab 96:E972–E976CrossRef Jumpertz R, Hanson RL, Sievers ML, Bennett PH, Nelson RG, Krakoff J (2011) Higher energy expenditure in humans predicts natural mortality. J Clin Endocrinol Metab 96:E972–E976CrossRef
19.
Zurück zum Zitat Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7:45–56CrossRef Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7:45–56CrossRef
20.
Zurück zum Zitat Lowell BB, Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307:384–387 (New York, N Y) CrossRef Lowell BB, Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307:384–387 (New York, N Y) CrossRef
21.
Zurück zum Zitat Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC (2003) PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267–273CrossRef Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC (2003) PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34:267–273CrossRef
22.
Zurück zum Zitat Ozanne S, Jensen C, Tingey K, Martin-Gronert M, Grunnet L, Brons C, Storgaard H, Vaag A (2006) Decreased protein levels of key insulin signalling molecules in adipose tissue from young men with a low birthweight—potential link to increased risk of diabetes? Diabetologia 49:2993–2999CrossRef Ozanne S, Jensen C, Tingey K, Martin-Gronert M, Grunnet L, Brons C, Storgaard H, Vaag A (2006) Decreased protein levels of key insulin signalling molecules in adipose tissue from young men with a low birthweight—potential link to increased risk of diabetes? Diabetologia 49:2993–2999CrossRef
23.
Zurück zum Zitat Ozanne SE, Jensen CB, Tingey KJ, Storgaard H, Madsbad S, Vaag AA (2005) Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 48:547–552CrossRef Ozanne SE, Jensen CB, Tingey KJ, Storgaard H, Madsbad S, Vaag AA (2005) Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia 48:547–552CrossRef
24.
Zurück zum Zitat Ozanne SE, Wang CL, Coleman N, Smith GD (1996) Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am J Physiol Endocrinol Metab 271:E1128–E1134 Ozanne SE, Wang CL, Coleman N, Smith GD (1996) Altered muscle insulin sensitivity in the male offspring of protein-malnourished rats. Am J Physiol Endocrinol Metab 271:E1128–E1134
25.
Zurück zum Zitat Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H, Poulsen P, Pilgaard K, Schou JH, Madsbad S, Astrup A, Vaag A (2005) Altered fat tissue distribution in young adult men who had low birth weight. Diabetes Care 28:151–153CrossRef Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H, Poulsen P, Pilgaard K, Schou JH, Madsbad S, Astrup A, Vaag A (2005) Altered fat tissue distribution in young adult men who had low birth weight. Diabetes Care 28:151–153CrossRef
26.
Zurück zum Zitat Ravelli ACJ, van der Meulen JHP, Michels RPJ, Osmond C, Barker DJP, Hales CN, Bleker OP (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351:173–177CrossRef Ravelli ACJ, van der Meulen JHP, Michels RPJ, Osmond C, Barker DJP, Hales CN, Bleker OP (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351:173–177CrossRef
27.
Zurück zum Zitat Ribel-Madsen R, Brons C, Friedrichsen M, Poulsen P, Vaag A (2011) Retinol-binding protein 4 in young men with low versus normal birth weight: physiological response to short-term overfeeding. Obesity 19:1304–1306 (Silver Spring) CrossRef Ribel-Madsen R, Brons C, Friedrichsen M, Poulsen P, Vaag A (2011) Retinol-binding protein 4 in young men with low versus normal birth weight: physiological response to short-term overfeeding. Obesity 19:1304–1306 (Silver Spring) CrossRef
28.
Zurück zum Zitat Schmidt SL, Kealey EH, Horton TJ, VonKaenel S, Bessesen DH (2013) The effects of short-term overfeeding on energy expenditure and nutrient oxidation in obesity-prone and obesity-resistant individuals. Int J Obes 37:1192–1197 (Lond) CrossRef Schmidt SL, Kealey EH, Horton TJ, VonKaenel S, Bessesen DH (2013) The effects of short-term overfeeding on energy expenditure and nutrient oxidation in obesity-prone and obesity-resistant individuals. Int J Obes 37:1192–1197 (Lond) CrossRef
29.
Zurück zum Zitat Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56:2085–2092CrossRef Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56:2085–2092CrossRef
30.
Zurück zum Zitat Vienberg SG, Brons C, Nilsson E, Astrup A, Vaag A, Andersen B (2012) Impact of short-term high-fat feeding and insulin-stimulated FGF21 levels in subjects with low birth weight and controls. Eur J Endocrinol 167:49–57CrossRef Vienberg SG, Brons C, Nilsson E, Astrup A, Vaag A, Andersen B (2012) Impact of short-term high-fat feeding and insulin-stimulated FGF21 levels in subjects with low birth weight and controls. Eur J Endocrinol 167:49–57CrossRef
Metadaten
Titel
Disproportionately increased 24-h energy expenditure and fat oxidation in young men with low birth weight during a high-fat overfeeding challenge
verfasst von
Charlotte Brøns
Søren K. Lilleøre
Arne Astrup
Allan Vaag
Publikationsdatum
22.08.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 6/2016
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-1018-7

Weitere Artikel der Ausgabe 6/2016

European Journal of Nutrition 6/2016 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.