Exercise training during normobaric hypoxic confinement does not alter hormonal appetite regulation

Tadej Debevec, Elizabeth J Simpson, Ian A Macdonald, Ola Eiken, Igor B Mekjavic, Tadej Debevec, Elizabeth J Simpson, Ian A Macdonald, Ola Eiken, Igor B Mekjavic

Abstract

Background: Both exposure to hypoxia and exercise training have the potential to modulate appetite and induce beneficial metabolic adaptations. The purpose of this study was to determine whether daily moderate exercise training performed during a 10-day exposure to normobaric hypoxia alters hormonal appetite regulation and augments metabolic health.

Methods: Fourteen healthy, male participants underwent a 10-day hypoxic confinement at ∼ 4000 m simulated altitude (FIO2 = 0.139 ± 0.003%) either combined with daily moderate intensity exercise (Exercise group; N = 8, Age = 25.8 ± 2.4 yrs, BMI = 22.9 ± 1.2 kg · m(-2)) or without any exercise (Sedentary group; N = 6 Age = 24.8 ± 3.1 yrs, BMI = 22.3 ± 2.5 kg · m(-2)). A meal tolerance test was performed before (Pre) and after the confinement (Post) to quantify fasting and postp randial concentrations of selected appetite-related hormones and metabolic risk markers. 13C-Glucose was dissolved in the test meal and 13CO2 determined in breath samples. Perceived appetite ratings were obtained throughout the meal tolerance tests.

Results: While body mass decreased in both groups (-1.4 kg; p = 0.01) following the confinement, whole body fat mass was only reduced in the Exercise group (-1.5 kg; p = 0.01). At Post, postprandial serum insulin was reduced in the Sedentary group (-49%; p = 0.01) and postprandial plasma glucose in the Exercise group (-19%; p = 0.03). Fasting serum total cholesterol levels were reduced (-12%; p = 0.01) at Post in the Exercise group only, secondary to low-density lipoprotein cholesterol reduction (-16%; p = 0.01). No differences between groups or testing periods were noted in fasting and/or postprandial concentrations of total ghrelin, peptide YY, and glucagon-like peptide-1, leptin, adiponectin, expired 13CO2 as well as perceived appetite ratings (p>0.05).

Conclusion: These findings suggest that performing daily moderate intensity exercise training during continuous hypoxic exposure does not alter hormonal appetite regulation but can improve the lipid profile in healthy young males.

Conflict of interest statement

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

Figures

Figure 1. Study protocol and meal tolerance…
Figure 1. Study protocol and meal tolerance test outline.
The meal tolerance test (MTT) was performed in the morning, one day before (Day -1) and just prior to exiting the 10-day confinement (morning of Day +1). FIO2, Fraction of inspired oxygen; VAS, Visual analogue scale for perceived appetite rating; AIR, Exhaled air sampling for determination of 13C isotope; MET, Blood sampling for determination of metabolic markers: total ghrelin, peptide YY, Glucagon-like peptide-1 and insulin at all samplings and leptin, adiponectin, free fatty acids, triacylglycerols, cholesterol, and catecholamines during fasting samplings only; GLU, Blood sampling for plasma glucose concentration determination.
Figure 2. Total ghrelin and peptide YY…
Figure 2. Total ghrelin and peptide YY (PYY) kinetics during the meal tolerance test in both Exercise (A, C) and Sedentary (B, D) group, respectively.
The meal tolerance test (MTT) was performed before (Pre; closed circles) and after (Post; open squares) the confinement. Two-way repeated measures ANOVA analysis, followed by a Tukey's HSD post hoc test; # indicates significant differences compared to fasting values (# p<0.05; ## p<0.01). Values are mean ± SEM.
Figure 3. Glucagon-like peptide-1 (GLP-1) and insulin…
Figure 3. Glucagon-like peptide-1 (GLP-1) and insulin kinetics during the meal tolerance test in Exercise (A, C) and Sedentary (B, D) group, respectively.
The meal tolerance test (MTT) was performed before (Pre; closed circles) and after (Post; open squares) the confinement. Two-way repeated measures ANOVA analysis, followed by a Tukey's HSD post hoc test; # indicates significant differences compared to fasting values (# p<0.05; ## p<0.01). * indicates significant differences compared to Pre values (p<0.05). Values are mean ± SEM.
Figure 4. Composite satiety scores before (Fast)…
Figure 4. Composite satiety scores before (Fast) and at 30-min intervals throughout the meal tolerance test for both Exercise (A) and Sedentary group (B).
One-way repeated measures ANOVA followed by Tukey's HSD post hoc test; # indicates significant differences compared to fasting values (p<0.05). Values are mean ± SEM.
Figure 5. Plasma glucose kinetics and atom…
Figure 5. Plasma glucose kinetics and atom percent excess (APE) of expired CO2 isotopic enrichment changes during the meal tolerance test in Exercise (A, C) and Sedentary group (B, D), respectively.
The meal tolerance test (MTT) was performed before (Pre; closed circles) and after (Post; open squares) the confinement. Two-way repeated measures ANOVA followed by Tukey's HSD post hoc test; ## indicates significant differences compared to fasting values (p<0.01). * indicates significant differences compared to Pre values (p<0.05). Values are mean ± SEM.
Figure 6. Fasting total cholesterol (A) and…
Figure 6. Fasting total cholesterol (A) and low-density lipoprotein cholesterol (LDL-C) levels in both Exercise and Sedentary group before (Pre), following the first 24-hrs of confinement (Day 2) and immediately after the confinement (Post).
One-way repeated measures ANOVA followed by Tukey's HSD post hoc test; # indicates significant differences compared to Pre (# p<0.05; ## p<0.01). * indicates significant differences compared to the Sedentary group (p<0.05). Values are mean ± SEM.

References

    1. Tschop M, Morrison KM (2001) Weight loss at high altitude. Adv Exp Med Biol 502: 237–247.
    1. Kayser B, Verges S (2013) Hypoxia, energy balance and obesity: from pathophysiological mechanisms to new treatment strategies. Obes Rev 14: 579–592.
    1. Westerterp-Plantenga MS, Westerterp KR, Rubbens M, Verwegen CR, Richelet JP, et al. (1999) Appetite at “high altitude” [Operation Everest III (Comex-'97)]: a simulated ascent of Mount Everest. J Appl Physiol 87: 391–399.
    1. Rose MS, Houston CS, Fulco CS, Coates G, Sutton JR, et al. (1988) Operation Everest. II: Nutrition and body composition. J Appl Physiol (1985) 65: 2545–2551.
    1. Hackett PH, Roach RC (2001) High-altitude illness. N Engl J Med 345: 107–114.
    1. Riepl RL, Fischer R, Hautmann H, Hartmann G, Muller TD, et al. (2012) Influence of acute exposure to high altitude on basal and postprandial plasma levels of gastroenteropancreatic peptides. PLoS One 7: e44445.
    1. Shukla V, Singh SN, Vats P, Singh VK, Singh SB, et al. (2005) Ghrelin and leptin levels of sojourners and acclimatized lowlanders at high altitude. Nutr Neurosci 8: 161–165.
    1. Wasse LK, Sunderland C, King JA, Batterham RL, Stensel DJ (2012) Influence of rest and exercise at a simulated altitude of 4,000 m on appetite, energy intake, and plasma concentrations of acylated ghrelin and peptide YY. J Appl Physiol 112: 552–559.
    1. Benso A, Broglio F, Aimaretti G, Lucatello B, Lanfranco F, et al. (2007) Endocrine and metabolic responses to extreme altitude and physical exercise in climbers. Eur J Endocrinol 157: 733–740.
    1. Snyder EM, Carr RD, Deacon CF, Johnson BD (2008) Overnight hypoxic exposure and glucagon-like peptide-1 and leptin levels in humans. Appl Physiol Nutr Metab 33: 929–935.
    1. Tschop M, Strasburger CJ, Hartmann G, Biollaz J, Bartsch P (1998) Raised leptin concentrations at high altitude associated with loss of appetite. Lancet 352: 1119–1120.
    1. Sierra-Johnson J, Romero-Corral A, Somers VK, Johnson BD (2008) Effect of altitude on leptin levels, does it go up or down? J Appl Physiol (1985) 105: 1684–1685.
    1. Broglio F, Gottero C, Prodam F, Gauna C, Muccioli G, et al. (2004) Non-acylated ghrelin counteracts the metabolic but not the neuroendocrine response to acylated ghrelin in humans. J Clin Endocrinol Metab 89: 3062–3065.
    1. Schubert MM, Sabapathy S, Leveritt M, Desbrow B (2013) Acute Exercise and Hormones Related to Appetite Regulation: A Meta-Analysis. Sports Med.
    1. Stensel D (2010) Exercise, appetite and appetite-regulating hormones: implications for food intake and weight control. Ann Nutr Metab 57 Suppl 236–42.
    1. Russel RR, Willis KS, Ravussin E, Larson-Meyer ED (2009) Effects of endurance running and dietary fat on circulating ghrelin and peptide YY. J Sports Sci Med 8: 574–583.
    1. Martins C, Kulseng B, King NA, Holst JJ, Blundell JE (2010) The effects of exercise-induced weight loss on appetite-related peptides and motivation to eat. J Clin Endocrinol Metab 95: 1609–1616.
    1. Guelfi KJ, Donges CE, Duffield R (2013) Beneficial effects of 12 weeks of aerobic compared with resistance exercise training on perceived appetite in previously sedentary overweight and obese men. Metabolism 62: 235–243.
    1. Debevec T, Amon M, Keramidas ME, Kounalakis SN, Pisot R, et al. (2010) Normoxic and hypoxic performance following 4 weeks of normobaric hypoxic training. Aviat Space Environ Med 81: 387–393.
    1. Wiesner S, Haufe S, Engeli S, Mutschler H, Haas U, et al. (2010) Influences of normobaric hypoxia training on physical fitness and metabolic risk markers in overweight to obese subjects. Obesity (Silver Spring) 18: 116–120.
    1. Netzer NC, Chytra R, Kupper T (2008) Low intense physical exercise in normobaric hypoxia leads to more weight loss in obese people than low intense physical exercise in normobaric sham hypoxia. Sleep Breath 12: 129–134.
    1. Wenger RH (2002) Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J 16: 1151–1162.
    1. Semenza GL (2001) Hypoxia-inducible factor 1: control of oxygen homeostasis in health and disease. Pediatr Res 49: 614–617.
    1. Katayama K, Goto K, Ishida K, Ogita F (2010) Substrate utilization during exercise and recovery at moderate altitude. Metabolism 59: 959–966.
    1. Haufe S, Wiesner S, Engeli S, Luft FC, Jordan J (2008) Influences of normobaric hypoxia training on metabolic risk markers in human subjects. Med Sci Sports Exerc 40: 1939–1944.
    1. Morishima T, Kurihara T, Hamaoka T, Goto K (2014) Whole body, regional fat accumulation, and appetite-related hormonal response after hypoxic training. Clin Physiol Funct Imaging 34: 90–97.
    1. Mackenzie R, Maxwell N, Castle P, Elliott B, Brickley G, et al. (2012) Intermittent exercise with and without hypoxia improves insulin sensitivity in individuals with type 2 diabetes. J Clin Endocrinol Metab 97: E546–555.
    1. Roach RC, Bartsch P, Hackett PH, Oelz O (1993) The Lake Louise AMS Scoring Consensus Committee. The Lake Louise acute mountain sickness scoring system. In: Sutton JR, Houston CS, Coates G, Burlington VT, editors. Hypoxia and Molecular Medicine: Queen City Printers. pp. 272–274.
    1. Mifflin MD, St Jeor ST, Hill LA, Scott BJ, Daugherty SA, et al. (1990) A new predictive equation for resting energy expenditure in healthy individuals. Am J Clin Nutr 51: 241–247.
    1. Jequier E, Constant F (2010) Water as an essential nutrient: the physiological basis of hydration. Eur J Clin Nutr 64: 115–123.
    1. Debevec T, Pialoux V, Mekjavic IB, Eiken O, Mury P, et al. (2014) Moderate exercise blunts oxidative stress induced by normobaric hypoxic confinement. Med Sci Sports Exerc 46: 33–41.
    1. Debevec T, McDonnell AC, Macdonald IA, Eiken O, Mekjavic IB (2014) Whole body and regional body composition changes following 10-day hypoxic confinement and unloading-inactivity. Appl Physiol Nutr Metab 39: 386–395.
    1. Hind K, Oldroyd B, Truscott JG (2011) In vivo precision of the GE Lunar iDXA densitometer for the measurement of total body composition and fat distribution in adults. Eur J Clin Nutr 65: 140–142.
    1. Forster CD, Macdonald IA (1999) The assay of the catecholamine content of small volumes of human plasma. Biomedical Chromatography 13: 209–215.
    1. Stubbs RJ, Hughes DA, Johnstone AM, Rowley E, Reid C, et al. (2000) The use of visual analogue scales to assess motivation to eat in human subjects: a review of their reliability and validity with an evaluation of new hand-held computerized systems for temporal tracking of appetite ratings. British Journal of Nutrition 84: 405–415.
    1. Gibbons C, Caudwell P, Finlayson G, King N, Blundell J (2011) Validation of a new hand-held electronic data capture method for continuous monitoring of subjective appetite sensations. International Journal of Behavioral Nutrition and Physical Activity 8: 57.
    1. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, et al. (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412–419.
    1. Anini Y, Brubaker PL (2003) Role of leptin in the regulation of glucagon-like peptide-1 secretion. Diabetes 52: 252–259.
    1. Martins C, Morgan LM, Bloom SR, Robertson MD (2007) Effects of exercise on gut peptides, energy intake and appetite. J Endocrinol 193: 251–258.
    1. Bailey DM, Davies B, Castell LM, Newsholme EA, Calam J (2001) Physical exercise and normobaric hypoxia: independent modulators of peripheral cholecystokinin metabolism in man. J Appl Physiol (1985) 90: 105–113.
    1. Chen SM, Lin HY, Kuo CH (2013) Altitude Training Improves Glycemic Control. Chin J Physiol 56.
    1. Zoll J, Ponsot E, Dufour S, Doutreleau S, Ventura-Clapier R, et al. (2006) Exercise training in normobaric hypoxia in endurance runners. III. Muscular adjustments of selected gene transcripts. J Appl Physiol (1985) 100: 1258–1266.
    1. Brooks GA, Butterfield GE, Wolfe RR, Groves BM, Mazzeo RS, et al. (1991) Increased dependence on blood glucose after acclimatization to 4,300 m. J Appl Physiol (1985) 70: 919–927.
    1. Seals DR, Johnson DG, Fregosi RF (1991) Hypoxia potentiates exercise-induced sympathetic neural activation in humans. J Appl Physiol (1985) 71: 1032–1040.
    1. Bailey DM, Davies B, Baker J (2000) Training in hypoxia: modulation of metabolic and cardiovascular risk factors in men. Med Sci Sports Exerc 32: 1058–1066.
    1. Dinmore AJ, Edwards JS, Menzies IS, Travis SP (1994) Intestinal carbohydrate absorption and permeability at high altitude (5,730 m). J Appl Physiol 76: 1903–1907.
    1. Kalson NS, Hext F, Davies AJ, Chan CW, Wright AD, et al. (2010) Do changes in gastro-intestinal blood flow explain high-altitude anorexia? Eur J Clin Invest 40: 735–741.
    1. King JA, Wasse LK, Ewens J, Crystallis K, Emmanuel J, et al. (2011) Differential acylated ghrelin, peptide YY3-36, appetite, and food intake responses to equivalent energy deficits created by exercise and food restriction. J Clin Endocrinol Metab 96: 1114–1121.
    1. Hamad N, Travis SP (2006) Weight loss at high altitude: pathophysiology and practical implications. Eur J Gastroenterol Hepatol 18: 5–10.
    1. Faiss R, Pialoux V, Sartori C, Faes C, Deriaz O, et al. (2013) Ventilation, Oxidative Stress and Nitric Oxide in Hypobaric vs. Normobaric Hypoxia. Med Sci Sports Exerc 45: 253–260.

Source: PubMed

3
Sottoscrivi