Twenty-four hour total and dietary fat oxidation in lean, obese and reduced-obese adults with and without a bout of exercise

Audrey Bergouignan, Elizabeth H Kealey, Stacy L Schmidt, Matthew R Jackman, Daniel H Bessesen, Audrey Bergouignan, Elizabeth H Kealey, Stacy L Schmidt, Matthew R Jackman, Daniel H Bessesen

Abstract

Background: It has been hypothesized that obese and reduced-obese individuals have decreased oxidative capacity, which contributes to weight gain and regain. Recent data have challenged this concept.

Objective: To determine (1) whether total and dietary fat oxidation are decreased in obese and reduced-obese adults compared to lean but increase in response to an acute exercise bout and (2) whether regular physical activity attenuates these metabolic alterations.

Design: We measured 24-hr total (whole-room calorimetry) and dietary fat (14C-oleate) oxidation in Sedentary Lean (BMI = 21.5±1.6; n = 10), Sedentary Obese (BMI = 33.6±2.5; n = 9), Sedentary Reduced-Obese (RED-SED; BMI = 26.9±3.7; n = 7) and in Physically Active Reduced-Obese (RED-EX; BMI = 27.3±2.8; n = 12) men and women with or without an acute exercise bout where energy expended during exercise was not replaced.

Results: Although Red-SED and Red-EX had a similar level of fatness, aerobic capacity and metabolic profiles were better in Red-EX only compared to Obese subjects. No significant between-group differences were seen in 24-hr respiratory quotient (RQ, Lean: 0.831±0.044, Obese: 0.852±0.023, Red-SED: 0.864±0.037, Red-EX: 0.842±0.039), total and dietary fat oxidation. A single bout of exercise increased total (+27.8%, p<0.0001) and dietary (+6.6%, p = 0.048) fat oxidation across groups. Although exercise did not impact RQ during the day, it decreased RQ during sleep (p = 0.01) in all groups. Red-EX oxidized more fat overnight than Red-SED subjects under both resting (p = 0.036) and negative energy balance (p = 0.003) conditions, even after adjustment for fat-free mass.

Conclusion: Obese and reduced-obese individuals oxidize as much fat as lean both under eucaloric and negative energy balance conditions, which does not support the hypothesis of reduced oxidative capacity in these groups. Reduced-obese individuals who exercise regularly have markers of metabolic health similar to those seen in lean adults. Both the acute and chronic effects of exercise were primarily observed at night suggesting an important role of sleep in the regulation of lipid metabolism.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Protocol of the tests in…
Figure 1. Protocol of the tests in the room calorimeter.
Figure 2. Cumulative responses of plasma triglycerides…
Figure 2. Cumulative responses of plasma triglycerides (top) and free fatty acids (FFA; bottom) concentrations expressed as the area under the curve (AUC) over 24 h in lean (n = 10), obese (n = 9), sedentary reduced-obese (Red-SED, n = 7) and exercising reduced-obese (Red-Ex, n = 12).
Statistics are presented on the Figure.
Figure 3. Twenty four hour total fat…
Figure 3. Twenty four hour total fat (top), carbohydrate (middle) and protein (bottom) oxidation in lean (n = 10), obese (n = 9), sedentary reduced-obese (Red-SED, n = 7) and exercising reduced-obese (Red-Ex, n = 12) after adjustment for differences in fat-free mass (FFM).
Statistics are presented on the Figure.
Figure 4. Respiratory quotient during waking (top)…
Figure 4. Respiratory quotient during waking (top) and sleeping (middle) periods and total fat oxidation during sleep in lean (n = 10), obese (n = 9), sedentary reduced-obese (Red-SED, n = 7) and exercising reduced-obese (Red-Ex, n = 12).
Statistics are presented on the Figure.
Figure 5. Dietary fat oxidation, i.e. the…
Figure 5. Dietary fat oxidation, i.e. the amount of fat oxidized over 24-hr coming from the breakfast meal only before (top) and after adjustment for fat-free mass (FFM) (middle), and the ratio of total and dietary fat oxidation (bottom) in lean (n = 10), obese (n = 9), sedentary reduced-obese (Red-SED, n = 7) and exercising reduced-obese (Red-Ex, n = 12).
Statistics are presented on the Figure.

References

    1. Li Z, Maglione M, Tu W, Mojica W, Arterburn D, et al. (2005) Meta-analysis: pharmacologic treatment of obesity. Ann Intern Med 142: 532–546.
    1. Maggard MA, Shugarman LR, Suttorp M, Maglione M, Sugerman HJ, et al. (2005) Meta-analysis: surgical treatment of obesity. Ann Intern Med 142: 547–559.
    1. Wadden TA, Butryn ML (2003) Behavioral treatment of obesity. Endocrinol Metab Clin North Am 32: : 981–1003, x.
    1. Weiss EC, Galuska DA, Kettel Khan L, Gillespie C, Serdula MK (2007) Weight regain in U.S. adults who experienced substantial weight loss, 1999-2002. Am J Prev Med 33: 34–40.
    1. Anderson JW, Konz EC, Frederich RC, Wood CL (2001) Long-term weight-loss maintenance: a meta-analysis of US studies. Am J Clin Nutr 74: 579–584.
    1. Maclean PS, Bergouignan A, Cornier MA, Jackman MR (2011) Biology's response to dieting: the impetus for weight regain. Am J Physiol Regul Integr Comp Physiol 301: R581–600.
    1. Raben A, Andersen HB, Christensen NJ, Madsen J, Holst JJ, et al. (1994) Evidence for an abnormal postprandial response to a high-fat meal in women predisposed to obesity. Am J Physiol 267: E549–559.
    1. Menshikova EV, Ritov VB, Toledo FG, Ferrell RE, Goodpaster BH, et al. (2005) Effects of weight loss and physical activity on skeletal muscle mitochondrial function in obesity. Am J Physiol Endocrinol Metab 288: E818–825.
    1. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, et al. (2005) Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8–14.
    1. Bandyopadhyay GK, Yu JG, Ofrecio J, Olefsky JM (2006) Increased malonyl-CoA levels in muscle from obese and type 2 diabetic subjects lead to decreased fatty acid oxidation and increased lipogenesis; thiazolidinedione treatment reverses these defects. Diabetes 55: 2277–2285.
    1. Holloway GP, Thrush AB, Heigenhauser GJ, Tandon NN, Dyck DJ, et al. (2007) Skeletal muscle mitochondrial FAT/CD36 content and palmitate oxidation are not decreased in obese women. Am J Physiol Endocrinol Metab 292: E1782–1789.
    1. Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, et al. (2007) Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56: 1592–1599.
    1. Kelley DE, He J, Menshikova EV, Ritov VB (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944–2950.
    1. Kim JY, Hickner RC, Cortright RL, Dohm GL, Houmard JA (2000) Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 279: E1039–1044.
    1. Astrup A, Buemann B, Christensen NJ, Toubro S (1994) Failure to increase lipid oxidation in response to increasing dietary fat content in formerly obese women. Am J Physiol 266: E592–599.
    1. Jackman MR, Kramer RE, MacLean PS, Bessesen DH (2006) Trafficking of dietary fat in obesity-prone and obesity-resistant rats. Am J Physiol Endocrinol Metab 291: E1083–1091.
    1. MacLean PS, Higgins JA, Jackman MR, Johnson GC, Fleming-Elder BK, et al. (2006) Peripheral metabolic responses to prolonged weight reduction that promote rapid, efficient regain in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 290: R1577–1588.
    1. Bessesen DH, Rupp CL, Eckel RH (1995) Dietary fat is shunted away from oxidation, toward storage in obese Zucker rats. Obes Res 3: 179–189.
    1. Hodson L, McQuaid SE, Karpe F, Frayn KN, Fielding BA (2009) Differences in partitioning of meal fatty acids into blood lipid fractions: a comparison of linoleate, oleate, and palmitate. Am J Physiol Endocrinol Metab 296: E64–71.
    1. Hodson L, McQuaid SE, Humphreys SM, Milne R, Fielding BA, et al. (2010) Greater dietary fat oxidation in obese compared with lean men: an adaptive mechanism to prevent liver fat accumulation? Am J Physiol Endocrinol Metab 299: E584–592.
    1. Bergouignan A, Trudel G, Simon C, Chopard A, Schoeller DA, et al. (2009) Physical inactivity differentially alters dietary oleate and palmitate trafficking. Diabetes 58: 367–376.
    1. Santosa S, Hensrud DD, Votruba SB, Jensen MD (2008) The influence of sex and obesity phenotype on meal fatty acid metabolism before and after weight loss. Am J Clin Nutr 88: 1134–1141.
    1. Binnert C, Pachiaudi C, Beylot M, Hans D, Vandermander J, et al. (1998) Influence of human obesity on the metabolic fate of dietary long- and medium-chain triacylglycerols. Am J Clin Nutr 67: 595–601.
    1. Westerterp KR, Smeets A, Lejeune MP, Wouters-Adriaens MP, Westerterp-Plantenga MS (2008) Dietary fat oxidation as a function of body fat. Am J Clin Nutr 87: 132–135.
    1. Horton TJ, Commerford SR, Pagliassotti MJ, Bessesen DH (2002) Postprandial leg uptake of triglyceride is greater in women than in men. Am J Physiol Endocrinol Metab 283: E1192–1202.
    1. Sonko BJ, Fennessey PV, Donnelly JE, Bessesen D, Sharp TA, et al. (2005) Ingested fat oxidation contributes 8% of 24-h total energy expenditure in moderately obese subjects. J Nutr 135: 2159–2165.
    1. Ogden LG, Stroebele N, Wyatt HR, Catenacci VA, Peters JC, et al. (2012) Cluster analysis of the national weight control registry to identify distinct subgroups maintaining successful weight loss. Obesity (Silver Spring) 20: 2039–2047.
    1. Catenacci VA, Wyatt HR (2007) The role of physical activity in producing and maintaining weight loss. Nat Clin Pract Endocrinol Metab 3: 518–529.
    1. Sidossis LS, Gastaldelli A, Klein S, Wolfe RR (1997) Regulation of plasma fatty acid oxidation during low- and high-intensity exercise. Am Physiol Soc 272: E1065–E1070.
    1. Votruba SB, Atkinson RL, Schoeller DA (2005) Sustained increase in dietary oleic acid oxidation following morning exercise. Int J Obes 29: 100–107.
    1. Votruba SB, Atkinson RL, Hirvonen MD, Schoeller DA (2002) Prior exercise increases subsequent utilization of dietary fat. Med Sci Sports Exerc 34: 1757–1765.
    1. Hansen K, Shriver T, Schoeller D (2005) The effects of exercise on the storage and oxidation of dietary fat. Sports Med 35: 363–373.
    1. Melanson EL, Gozansky WS, Barry DW, Maclean PS, Grunwald GK, et al. (2009) When energy balance is maintained, exercise does not induce negative fat balance in lean sedentary, obese sedentary, or lean endurance-trained individuals. J Appl Physiol 107: 1847–1856.
    1. .
    1. Bergouignan A, Gozansky WS, Barry DW, Leitner W, MacLean PS, et al. (2010) Increasing dietary fat elicits similar changes in fat oxidation and markers of muscle oxidative capacity in lean and obese humans. PLoS One 7: e30164.
    1. Blaak EE (2004) Basic disturbances in skeletal muscle fatty acid metabolism in obesity and type 2 diabetes mellitus. Proc Nutr Soc 63: 323–330.
    1. Blaak EE, van Aggel-Leijssen DP, Wagenmakers AJ, Saris WH, van Baak MA (2000) Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes 49: 2102–2107.
    1. Kelley DE, Goodpaster B, Wing RR, Simoneau JA (1999) Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 277: E1130–1141.
    1. Bergouignan A, Momken I, Schoeller DA, Simon C, Blanc S (2009) Metabolic fate of saturated and monounsaturated dietary fats: the Mediterranean diet revisited from epidemiological evidence to cellular mechanisms. Prog Lipid Res 48: 128–147.
    1. Jackman MR, Steig A, Higgins JA, Johnson GC, Fleming-Elder BK, et al. (2008) Weight regain after sustained weight reduction is accompanied by suppressed oxidation of dietary fat and adipocyte hyperplasia. Am J Physiol Regul Integr Comp Physiol 294: R1117–1129.
    1. Hawkins KR, Hansen KC, Schoeller DA, Cooper JA (2012) Effect of exercise on the diurnal variation in energy substrate use during a high-fat diet. Eur J Appl Physiol 112: 3775–3785.
    1. Redman LM, Heilbronn LK, Martin CK, Alfonso A, Smith SR, et al. (2007) Effect of calorie restriction with or without exercise on body composition and fat distribution. J Clin Endocrinol Metab 92: 865–872.
    1. Larson-Meyer DE, Redman L, Heilbronn LK, Martin CK, Ravussin E (2010) Caloric restriction with or without exercise: the fitness versus fatness debate. Med Sci Sports Exerc 42: 152–159.
    1. Weiss EP, Racette SB, Villareal DT, Fontana L, Steger-May K, et al. (2006) Improvements in glucose tolerance and insulin action induced by increasing energy expenditure or decreasing energy intake: a randomized controlled trial. Am J Clin Nutr 84: 1033–1042.

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir