Achieving energy balance with a high-fat meal does not enhance skeletal muscle adaptation and impairs glycaemic response in a sleep-low training model

José L Areta, Juma Iraki, Daniel J Owens, Sophie Joanisse, Andrew Philp, James P Morton, Jostein Hallén, José L Areta, Juma Iraki, Daniel J Owens, Sophie Joanisse, Andrew Philp, James P Morton, Jostein Hallén

Abstract

New findings: What is the central question of this study? Does achieving energy balance mainly with ingested fat in a 'sleep-low' model of training with low muscle glycogen affect the early training adaptive response during recovery? What is the main finding and its importance? Replenishing the energy expended during exercise mainly from ingested fat to achieve energy balance in a 'sleep-low' model does not enhance the response of skeletal muscle markers of early adaptation to training and impairs glycaemic control the morning after compared to training with low energy availability. These findings are important for optimizing post-training dietary recommendations in relation to energy balance and macronutrient intake.

Abstract: Training with low carbohydrate availability (LCHO) has been shown to acutely enhance endurance training skeletal muscle response, but the concomitant energy deficit (ED) in LCHO interventions has represented a confounding factor in past research. This study aimed at determining if achieving energy balance with high fat (EB-HF) acutely enhances the adaptive response in LCHO compared to ED with low fat (ED-LF). In a crossover design, nine well-trained males completed a 'sleep-low' protocol: on day 1 they cycled to deplete muscle glycogen while reaching a set energy expenditure (30 kcal (kg of fat free mass (FFM))-1 ). Post-exercise, low carbohydrate, protein-matched meals completely (EB-HF, 30 kcal (kg FFM)-1 ) or partially (ED-LF, 9 kcal (kg FFM)-1 ) replaced the energy expended, with the majority of energy derived from fat in EB-HF. In the morning of day 2, participants exercised fasted, and skeletal muscle and blood samples were collected and a carbohydrate-protein drink was ingested at 0.5 h recovery. Muscle glycogen showed no treatment effect (P < 0.001) and decreased from 350 ± 98 to 192 ± 94 mmol (kg dry mass)-1 between rest and 0.5 h recovery. Phosphorylation status of the mechanistic target of rapamycin and AMP-activated protein kinase pathway proteins showed only time effects. mRNA expression of p53 increased after exercise (P = 0.005) and was higher in ED-LF at 3.5 h compared to EB-HF (P = 0.027). Plasma glucose and insulin area under the curve (P < 0.04) and peak values (P ≤ 0.05) were higher in EB-HF after the recovery drink. Achieving energy balance with a high-fat meal in a 'train-low' ('sleep-low') model did not enhance markers of skeletal muscle adaptation and impaired glycaemia in response to a recovery drink following training in the morning.

Keywords: endurance; energy availability; high-fat feeding; muscle glycogen; train low.

© 2020 The Authors. Experimental Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.

References

REFERENCES

    1. Andrade-Souza, V. A., Ghiarone, T., Sansonio, A., Santos Silva, K. A., Tomazini, F., Arcoverde, L., … Lima-Silva, A. E. (2019). Exercise twice-a-day potentiates markers of mitochondrial biogenesis in men. FASEB Journal, 34(1), 1602-1619.
    1. Areta, J. L. (2020). Case study: Resumption of eumenorrhea in parallel with high training load after 4 years of menstrual dysfunction: A 5-year follow-up of an elite female cyclist. International Journal of Sport Nutrition and Exercise Metabolism, .
    1. Areta, J. L., Austarheim, I., Wangensteen, H., & Capelli, C. (2018). Metabolic and performance effects of Yerba Mate on well-trained cyclists. Medicine & Science in Sports & Exercise, 50(4), 817-826.
    1. Areta, J. L., Burke, L. M., Camera, D. M., West, D. W. D., Crawshay, S., Moore, D. R., … Coffey, V. G. (2014). Reduced resting skeletal muscle protein synthesis is rescued by resistance exercise and protein ingestion following short-term energy deficit. American Journal of Physiology. Endocrinology and Metabolism, 306(8), E989-E997.
    1. Areta, J. L., & Hopkins, W. G. (2018). Skeletal muscle glycogen content at rest and during endurance exercise in humans: A meta-analysis. Sports Medicine, 48(9), 2091-2102.
    1. Bartlett, J. D., Hawley, J. A., & Morton, J. P. (2015). Carbohydrate availability and exercise training adaptation: Too much of a good thing? European Journal of Sport Science, 15(1), 3-12.
    1. Bartlett, J. D., Louhelainen, J., Cochran, A. J., Gibala, M. J., Gregson, W., Close, G. L., … Morton, J. P. (2013). Reduced carbohydrate availability enhances exercise-induced p53 signaling in human skeletal muscle: Implications for mitochondrial biogenesis. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 304(6), R450-R458.
    1. Bergström, J., Hermansen, L., Hultman, E., & Saltin, B. (1967). Diet, muscle glycogen and physical performance. Acta Physiologica, 71(2-3), 140-150.
    1. Cameron-Smith, D., Burke, L. M., Angus, D. J., Tunstall, R. J., Cox, G. R., Bonen, A., … Hargreaves, M. (2003). A short-term, high-fat diet up-regulates lipid metabolism and gene expression in human skeletal muscle. American Journal of Clinical Nutrition, 77(2), 313-318.
    1. Civitarese, A. E., Carling, S., Heilbronn, L. K., Hulver, M. H., Ukropcova, B., Deutsch, W. A., … Ravussin, E. (2007). Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Medicine, 4(3), e76.
    1. Cluberton, L. J., McGee, S. L., Murphy, R. M., & Hargreaves, M. (2005). Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression. Journal of Applied Physiology, 99(4), 1359-1363.
    1. Coen, P. M., Menshikova, E. V., Distefano, G., Zheng, D., Tanner, C. J., Standley, R. A., … Goodpaster, B. H. (2015). Exercise and weight loss improve muscle mitochondrial respiration, lipid partitioning, and insulin sensitivity after gastric bypass surgery. Diabetes, 64(11), 3737-3750.
    1. De Souza, M. J., Koltun, K. J., & Williams, N. I. (2019). What is the evidence for a Triad-like syndrome in exercising men? Current Opinion in Physiology, 10, 27-34.
    1. De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., & Mallinson, R. J. … Expert Panel. (2014) 2014 Female athlete triad coalition consensus statement on treatment and return to play of the female athlete triad: 1st international conference held in San Francisco, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. British Journal of Sports Medicine, 48(4), 289-289.
    1. Fox, A. K., Kaufman, A. E., & Horowitz, J. F. (2004). Adding fat calories to meals after exercise does not alter glucose tolerance. Journal of Applied Physiology, 97(1), 11-16.
    1. Goedecke, J. H., Christie, C., Wilson, G., Dennis, S. C., Noakes, T. D., Hopkins, W. G., & Lambert, E. V. (1999). Metabolic adaptations to a high-fat diet in endurance cyclists. Metabolism, 48(12), 1509-1517.
    1. Hammond, K. M., Impey, S. G., Currell, K., Mitchell, N., Shepherd, S. O., Jeromson, S., … Morton, J. P. (2016). Postexercise high-fat feeding suppresses p70S6K1 activity in human skeletal muscle. Medicine & Science in Sports & Exercise, 48(11), 2108-2117.
    1. Hammond, K. M., Sale, C., Fraser, W., Tang, J., Shepherd, S. O., Strauss, J. A., … Morton, J. P. (2019). Post-exercise carbohydrate and energy availability induce independent effects on skeletal muscle cell signalling and bone turnover: Implications for training adaptation. Journal of Physiology, 597(18), 4779-4796.
    1. Havemann, L., West, S. J., Goedecke, J. H., Macdonald, I. A., St Clair Gibson, A., Noakes, T. D., & Lambert, E. V. (2006). Fat adaptation followed by carbohydrate loading compromises high-intensity sprint performance. Journal of Applied Physiology, 100(1), 194-202.
    1. Ihle, R., & Loucks, A. B. (2004). Dose-response relationships between energy availability and bone turnover in young exercising women. Journal of Bone and Mineral Research, 19(8), 1231-1240.
    1. Impey, S. G., Hammond, K. M., Shepherd, S. O., Sharples, A. P., Stewart, C., Limb, M., … Morton, J. P. (2016). Fuel for the work required: A practical approach to amalgamating train-low paradigms for endurance athletes. Physiological Reports, 4(10), e12803.
    1. Jensen, J., Tantiwong, P., Stuenaes, J. T., Molina-Carrion, M., DeFronzo, R. A., Sakamoto, K., & Musi, N. (2012). Effect of acute exercise on glycogen synthase in muscle from obese and diabetic subjects. American Journal of Physiology. Endocrinology and Metabolism, 303(1), E82-E89.
    1. Lane, S. C., Camera, D. M., Lassiter, D. G., Areta, J. L., Bird, S. R., Yeo, W. K., … Hawley, J. A. (2015). Effects of sleeping with reduced carbohydrate availability on acute training responses. Journal of Applied Physiology, 119(6), 643-655.
    1. Leckey, J. J., Hoffman, N. J., Parr, E. B., Devlin, B. L., Trewin, A. J., Stepto, N. K., … Hawley, J. A. (2018). High dietary fat intake increases fat oxidation and reduces skeletal muscle mitochondrial respiration in trained humans. FASEB Journal, 32(6), 2979-2991.
    1. Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCTmethod. Methods, 25(4), 402-408.
    1. Loucks, A. B., Kiens, B., & Wright, H. H. (2011). Energy availability in athletes. Journal of Sports Sciences, 29(suppl 1), S7-S15.
    1. MacInnis, M. J., & Gibala, M. J. (2017). Physiological adaptations to interval training and the role of exercise intensity: Training adaptations and the nature of the stimulus. Journal of Physiology, 595(9), 2915-2930.
    1. McConell, G. K., Lee-Young, R. S., Chen, Z.-P., Stepto, N. K., Huynh, N. N., Stephens, T. J., … Kemp, B. E. (2005). Short-term exercise training in humans reduces AMPK signalling during prolonged exercise independent of muscle glycogen: Abolished AMPK activation during exercise after short-term training. Journal of Physiology, 568(2), 665-676.
    1. McConell, G. K., Wadley, G. D., Le plastrier, K., & Linden, K. C. (2020). Skeletal muscle AMPK is not activated during 2 hours of moderate intensity exercise at ∼65% V̇O2peak in endurance trained men. Journal of Physiology, .
    1. Moore, D. R., Camera, D. M., Areta, J. L., & Hawley, J. A. (2014). Beyond muscle hypertrophy: Why dietary protein is important for endurance athletes. Applied Physiology, Nutrition, and Metabolism, 39(9), 987-997.
    1. Morton, J. P., Croft, L., Bartlett, J. D., MacLaren, D. P. M., Reilly, T., Evans, L., … Drust, B. (2009). Reduced carbohydrate availability does not modulate training-induced heat shock protein adaptations but does upregulate oxidative enzyme activity in human skeletal muscle. Journal of Applied Physiology, 106(5), 1513-1521.
    1. Moseley, L., & Jeukendrup, A. E. (2001). The reliability of cycling efficiency. Medicine and Science in Sports and Exercise, 33(4), 621-627.
    1. Mountjoy, M., Sundgot-Borgen, J., Burke, L., Ackerman, K. E., Blauwet, C., Constantini, N., … Budgett, R. (2018). International Olympic Committee (IOC) consensus statement on relative energy deficiency in sport (RED-S): 2018 update. International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 316-331.
    1. Newsom, S. A., Schenk, S., Thomas, K. M., Harber, M. P., Knuth, N. D., Goldenberg, N., & Horowitz, J. F. (2010). Energy deficit after exercise augments lipid mobilization but does not contribute to the exercise-induced increase in insulin sensitivity. Journal of Applied Physiology, 108(3), 554-560.
    1. Park, J.-Y., Wang, P., Matsumoto, T., Sung, H. J., Ma, W., Choi, J. W., … Hwang, P. M. (2009). P53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circulation Research, 105(7), 705-712.
    1. Pehmoller, C., Brandt, N., Birk, J. B., Hoeg, L. D., Sjoberg, K. A., Goodyear, L. J., … Wojtaszewski, J. F. P. (2012). Exercise alleviates lipid-induced insulin resistance in human skeletal muscle-signaling interaction at the level of TBC1 domain family member 4. Diabetes, 61(11), 2743-2752.
    1. Pilegaard, H., Osada, T., Andersen, L. T., Helge, J. W., Saltin, B., & Neufer, P. D. (2005). Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise. Metabolism, 54(8), 1048-1055.
    1. Schenk, S., Cook, J. N., Kaufman, A. E., & Horowitz, J. F. (2005). Postexercise insulin sensitivity is not impaired after an overnight lipid infusion. American Journal of Physiology. Endocrinology and Metabolism, 288(3), E519-E525.
    1. Sparti, A., & Décombaz, J. (1992). Effect of diet on glucose tolerance 36 hours after glycogen-depleting exercise. European Journal of Clinical Nutrition, 46(6), 377-385.
    1. Steenberg, D. E., Jørgensen, N. B., Birk, J. B., Sjøberg, K. A., Kiens, B., Richter, E. A., & Wojtaszewski, J. F. P. (2019). Exercise training reduces the insulin-sensitizing effect of acute exercise in human skeletal muscle. Journal of Physiology, 597(1), 89-103.
    1. Stellingwerff, T. (2018). Case study: Body composition periodization in an olympic-level female middle-distance runner over a 9-year career. International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 428-433.
    1. Stellingwerff, T., Spriet, L. L., Watt, M. J., Kimber, N. E., Hargreaves, M., Hawley, J. A., & Burke, L. M. (2006). Decreased PDH activation and glycogenolysis during exercise following fat adaptation with carbohydrate restoration. American Journal of Physiology. Endocrinology and Metabolism, 290(2), E380-E388.
    1. Stocks, B., Dent, J. R., Ogden, H. B., Zemp, M., & Philp, A. (2019). Postexercise skeletal muscle signaling responses to moderate- to high-intensity steady-state exercise in the fed or fasted state. American Journal of Physiology. Endocrinology and Metabolism, 316(2), E230-E238.
    1. Torrens, S. L., Areta, J. L., Parr, E. B., & Hawley, J. A. (2016). Carbohydrate dependence during prolonged simulated cycling time trials. European Journal of Applied Physiology, 116(4), 781-790.
    1. Weir, J. B. de B. (1949). New methods for calculating metabolic rate with special reference to protein metabolism. Journal of Physiology, 109(1-2), 1-9.
    1. Wojtaszewski, J. F. P., MacDonald, C., Nielsen, J. N., Hellsten, Y., Hardie, D. G., Kemp, B. E., … Richter, E. A. (2003). Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. American Journal of Physiology. Endocrinology and Metabolism, 284(4), E813-E822.
    1. Yeo, W. K., Lessard, S. J., Chen, Z. P., Garnham, A. P., Burke, L. M., Rivas, D. A., … Hawley, J. A. (2008). Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans. Journal of Applied Physiology, 105(5), 1519-1526.
    1. Yeo, W. K., McGee, S. L., Carey, A. L., Paton, C. D., Garnham, A. P., Hargreaves, M., & Hawley, J. A. (2010). Acute signalling responses to intense endurance training commenced with low or normal muscle glycogen: Glycogen availability and training adaptation. Experimental Physiology, 95(2), 351-358.
    1. Yeo, W. K., Paton, C. D., Garnham, A. P., Burke, L. M., Carey, A. L., & Hawley, J. A. (2008). Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. Journal of Applied Physiology, 105(5), 1462-1470.

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