A prolonged fast improves overnight substrate oxidation without modulating hepatic glycogen in adults with and without nonalcoholic fatty liver: A randomized crossover trial.


Journal

Obesity (Silver Spring, Md.)
ISSN: 1930-739X
Titre abrégé: Obesity (Silver Spring)
Pays: United States
ID NLM: 101264860

Informations de publication

Date de publication:
03 2023
Historique:
revised: 09 11 2022
received: 08 08 2022
accepted: 11 11 2022
pubmed: 10 2 2023
medline: 25 2 2023
entrez: 9 2 2023
Statut: ppublish

Résumé

Increasing overnight fasting time seems a promising strategy to improve metabolic health in individuals with nonalcoholic fatty liver (NAFL). Mechanisms underlying the beneficial effects of fasting may be related to larger fluctuations in hepatic glycogen and higher fat oxidation. This study investigated whether prolonging an overnight fast depletes hepatic glycogen stores and improves substrate metabolism in individuals with NAFL and healthy lean individuals. Eleven individuals with NAFL and ten control individuals participated in this randomized crossover trial. After a 9.5-hour or 16-hour fast, hepatic glycogen was measured by using carbon-13 magnetic resonance spectroscopy, and a meal test was performed. Nocturnal substrate oxidation was measured with indirect calorimetry. Extending fasting time led to lower nocturnal carbohydrate oxidation and higher fat oxidation in both groups (intervention × time, p < 0.005 for carbohydrate and fat oxidation). In both arms, the respiratory exchange ratio measured during the night remained higher in the group with NAFL compared with the control group (population p < 0.001). No changes were observed in hepatic glycogen depletion with a prolonged overnight fast in the group with NAFL or the control group. These results suggest that acutely prolonging the overnight fast can improve overnight substrate oxidation and that these alterations are not mediated by changes in hepatic glycogen depletion.

Identifiants

pubmed: 36756887
doi: 10.1002/oby.23676
doi:

Substances chimiques

Liver Glycogen 0
Carbohydrates 0

Types de publication

Randomized Controlled Trial Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

757-767

Informations de copyright

© 2023 The Authors. Obesity published by Wiley Periodicals LLC on behalf of The Obesity Society.

Références

Gill S, Panda S. A smartphone app reveals erratic diurnal eating patterns in humans that can Be modulated for health benefits. Cell Metab. 2015;22(5):789-798.
Cahill GF Jr. Fuel metabolism in starvation. Annu Rev Nutr. 2006;26:1-22.
Magnusson I, Rothman DL, Katz LD, Shulman RG, Shulman GI. Increased rate of gluconeogenesis in type II diabetes mellitus. A 13C nuclear magnetic resonance study. J Clin Invest. 1992;90(4):1323-1327.
Krssak M, Brehm A, Bernroider E, et al. Alterations in postprandial hepatic glycogen metabolism in type 2 diabetes. Diabetes. 2004;53(12):3048-3056.
Macauley M, Smith FE, Thelwall PE, Hollingsworth KG, Taylor R. Diurnal variation in skeletal muscle and liver glycogen in humans with normal health and type 2 diabetes. Clin Sci (Lond). 2015;128(10):707-713.
Schrauwen P, van Marken Lichtenbelt WD, Saris WH, Westerterp KR. Role of glycogen-lowering exercise in the change of fat oxidation in response to a high-fat diet. Am J Physiol. 1997;273(3 Pt 1):E623-E629.
Morino K, Petersen KF, Shulman GI. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes. 2006;55(suppl 2):S9-S15.
Moro C, Bajpeyi S, Smith SR. Determinants of intramyocellular triglyceride turnover: implications for insulin sensitivity. Am J Physiol Endocrinol Metab. 2008;294(2):E203-E213.
Summers SA, Nelson DH. A role for sphingolipids in producing the common features of type 2 diabetes, metabolic syndrome X, and Cushing's syndrome. Diabetes. 2005;54(3):591-602.
Browning JD, Baxter J, Satapati S, Burgess SC. The effect of short-term fasting on liver and skeletal muscle lipid, glucose, and energy metabolism in healthy women and men. J Lipid Res. 2012;53(3):577-586.
Hoeks J, van Herpen NA, Mensink M, et al. Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance. Diabetes. 2010;59(9):2117-2125.
Ravussin E, Beyl RA, Poggiogalle E, Hsia DS, Peterson CM. Early time-restricted feeding reduces appetite and increases fat oxidation but does not affect energy expenditure in humans. Obesity (Silver Spring). 2019;27(8):1244-1254.
Bandsma RH, Prinsen BH, van Der Velden MS, et al. Increased de novo lipogenesis and delayed conversion of large VLDL into intermediate density lipoprotein particles contribute to hyperlipidemia in glycogen storage disease type 1a. Pediatr Res. 2008;63(6):702-707.
Lim S, Oh TJ, Koh KK. Mechanistic link between nonalcoholic fatty liver disease and cardiometabolic disorders. Int J Cardiol. 2015;201:408-414.
Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med. 2010;363(14):1341-1350.
Targher G, Byrne CD. Clinical Review: Nonalcoholic fatty liver disease: a novel cardiometabolic risk factor for type 2 diabetes and its complications. J Clin Endocrinol Metab. 2013;98(2):483-495.
van Moorsel D, Hansen J, Havekes B, et al. Demonstration of a day-night rhythm in human skeletal muscle oxidative capacity. Mol Metab. 2016;5(8):635-645.
Wefers J, Connell NJ, Fealy CE, et al. Day-night rhythm of skeletal muscle metabolism is disturbed in older, metabolically compromised individuals. Mol Metab. 2020;41:101050. doi:10.1016/j.molmet.2020.101050
Sutton EF, Beyl R, Early KS, Cefalu WT, Ravussin E, Peterson CM. Early time-restricted feeding improves insulin sensitivity, blood pressure, and oxidative stress even without weight loss in men with prediabetes. Cell Metab. 2018;27(6):1212-1221.e3.
Roumans KH, Lindeboom L, Veeraiah P, et al. Hepatic saturated fatty acid fraction is associated with de novo lipogenesis and hepatic insulin resistance. Nat Commun. 2020;11(1):1891. doi:10.1038/s41467-020-15684-0
Schoffelen PF, Westerterp KR, Saris WH, Ten Hoor F. A dual-respiration chamber system with automated calibration. J Appl Physiol (1985). 1997;83(6):2064-2072.
Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol. 1949;109(1-2):1-9.
Brouwer E. On simple formulae for calculating the heat expenditure and the quantities of carbohydrate and fat oxidized in metabolism of men and animals, from gaseous exchange (oxygen intake and carbonic acid output) and urine-N. Acta Physiol Pharmacol Neerl. 1957;6:795-802.
Taylor R, Magnusson I, Rothman DL, et al. Direct assessment of liver glycogen storage by 13C nuclear magnetic resonance spectroscopy and regulation of glucose homeostasis after a mixed meal in normal subjects. J Clin Invest. 1996;97(1):126-132.
Fletcher JA, Deja S, Satapati S, Fu X, Burgess SC, Browning JD. Impaired ketogenesis and increased acetyl-CoA oxidation promote hyperglycemia in human fatty liver. JCI Insight. 2019;5(11):e127737. doi:10.1172/jci.insight.127737
Sunny NE, Parks EJ, Browning JD, Burgess SC. Excessive hepatic mitochondrial TCA cycle and gluconeogenesis in humans with nonalcoholic fatty liver disease. Cell Metab. 2011;14(6):804-810.
Brouwers B, Schrauwen-Hinderling VB, Jelenik T, et al. Metabolic disturbances of non-alcoholic fatty liver resemble the alterations typical for type 2 diabetes. Clin Sci (Lond). 2017;131(15):1905-1917.
Verwer BJ, Scheffer PG, Vermue RP, Pouwels PJ, Diamant M, Tushuizen ME. NAFLD is related to post-prandial triglyceride-enrichment of HDL particles in association with endothelial and HDL dysfunction. Liver Int. 2020;40(10):2439-2444.
Hutchison AT, Regmi P, Manoogian ENC, et al. Time-restricted feeding improves glucose tolerance in men at risk for type 2 diabetes: a randomized crossover trial. Obesity (Silver Spring). 2019;27(5):724-732.
Parr EB, Devlin BL, Radford BE, Hawley JA. A delayed morning and earlier evening time-restricted feeding protocol for improving glycemic control and dietary adherence in men with overweight/obesity: a randomized controlled trial. Nutrients. 2020;12(2):505. doi:10.3390/nu12020505

Auteurs

Kay H M Roumans (KHM)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.

Anna Veelen (A)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.

Charlotte Andriessen (C)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.

Julian Mevenkamp (J)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.
Department of Radiology and Nuclear Medicine, Maastricht University Medical Center, Maastricht, the Netherlands.

Esther Kornips (E)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.

Pandichelvam Veeraiah (P)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.
Department of Radiology and Nuclear Medicine, Maastricht University Medical Center, Maastricht, the Netherlands.

Bas Havekes (B)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.
Department of Internal Medicine, Division of Endocrinology and Metabolic Disease, Maastricht University Medical Center, Maastricht, the Netherlands.

Harry P F Peters (HPF)

Unilever Food Innovation Center, Wageningen.

Lucas Lindeboom (L)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.
Department of Radiology and Nuclear Medicine, Maastricht University Medical Center, Maastricht, the Netherlands.

Patrick Schrauwen (P)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.

Vera B Schrauwen-Hinderling (VB)

Department of Nutrition and Movement Sciences, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, the Netherlands.
Department of Radiology and Nuclear Medicine, Maastricht University Medical Center, Maastricht, the Netherlands.
Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich Heine University, Düsseldorf, Germany.

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