Influence of hormonal status on substrate utilization at rest and during exercise in the female population

Sports Medicine

Volumn 42, Issue 4, 2012, Pages 327-342

  Isacco, Laurie ^a   Duch, Pascale ^a   Boisseau, Nathalie ^a  

^a CLERMONT AUVERGNE UNIVERSITY   (France)

Author keywords

Adults; Contraceptives, general; Diet; Exercise; Hormones, therapeutic use; Menopause; Training

Indexed keywords

ESTROGEN RECEPTOR; ORAL CONTRACEPTIVE AGENT; SEX HORMONE;

DRUG EFFECT; ENERGY METABOLISM; EXERCISE; FEMALE; HORMONE SUBSTITUTION; HUMAN; MALE; MENOPAUSE; MENSTRUAL CYCLE; PHYSIOLOGY; REVIEW; SEX DIFFERENCE; SEXUAL MATURATION;

CONTRACEPTIVES, ORAL, HORMONAL; ENERGY METABOLISM; EXERCISE; FEMALE; GONADAL STEROID HORMONES; HORMONE REPLACEMENT THERAPY; HUMANS; MALE; MENOPAUSE; MENSTRUAL CYCLE; RECEPTORS, ESTROGEN; SEX FACTORS; SEXUAL MATURATION;

EID: 84858262332     PISSN: 01121642     EISSN: 11792035     Source Type: Journal    
DOI: 10.2165/11598900-000000000-00000     Document Type: Review

References (103)

1. Brooks GA, Mercier J. Balance of carbohydrate and lipid utilization during exercise: the "crossover" concept. J Appl Physiol 1994 Jun; 76 (6): 2253-61 (Pubitemid 24184739)
2. Achten J, Gleeson M, Jeukendrup AE. Determination of the exercise intensity that elicits maximal fat oxidation. Med Sci Sports Exerc 2002 Jan; 34 (1): 92-7 (Pubitemid 34052381)
3. Achten J, Jeukendrup AE. Maximal fat oxidation during exercise in trainedmen. Int J SportsMed 2003Nov; 24 (8): 603-8 (Pubitemid 37421544)
4. Jeukendrup AE. Modulation of carbohydrate and fat utilization by diet, exercise and environment. Biochem Soc Trans 2003 Dec; 31 (Pt 6): 1270-3 (Pubitemid 38030954)
5. Poortmans JR, editor. Principles of exercise biochemistry. 3rd rev. ed. Basel: Med Sport Sci-Karger, 2004
6. Aucouturier J, Baker JS, Duche P. Fat and carbohydrate metabolism during submaximal exercise in children. Sports Med 2008; 38 (3): 213-38 (Pubitemid 351263720)
7. Tarnopolsky MA. Gender differences in substrate metabolism during endurance exercise. Can J Appl Physiol 2000 Aug; 25 (4): 312-27
8. Timmons BW, Hamadeh MJ, Devries MC, et al. Influence of gender, menstrual phase, and oral contraceptive use on immunological changes in response to prolonged cycling. J Appl Physiol 2005 Sep; 99 (3): 979-85 (Pubitemid 41214512)
9. Veldhuis JD, Roemmich JN, Richmond EJ, et al. Endocrine control of body composition in infancy, childhood, and puberty. Endocr Rev 2005 Feb; 26 (1): 114-46 (Pubitemid 40209389)
10. Tanner JM. Growth at adolescence. 2nd ed. Oxford: Blackwell, 1962
11. Malina R, Bouchard C, Bar Or O. Growth, maturation and physical activity. Champaign (IL): Human Kinetics, 2004
12. Viru A, Laaneots L, Karelson K, et al. Exercise-induced hormone responses in girls at different stages of sexual maturation. Eur J Appl Physiol Occup Physiol 1998 Apr; 77 (5): 401-8 (Pubitemid 28154144)
13. Timmons BW, Bar-Or O, Riddell MC. Energy substrate utilization during prolonged exercise with and without carbohydrate intake in preadolescent and adolescent girls. J Appl Physiol 2007 Sep; 103 (3): 995-1000 (Pubitemid 47358885)
14. Matsudo SMM. Self-assessment and physician assessment of sexual maturation in Brazilian boys and girls: concordance and reproducibility. Am J Hum Biol 1994; 6: 451-5
15. Peronnet F, Massicotte D. Table of nonprotein respiratory quotient: an update. Can J Sport Sci 1991 Mar; 16 (1): 23-9
16. Ellis GS, Lanza-Jacoby S, Gow A, et al. Effects of estradiol on lipoprotein lipase activity and lipid availability in exercised male rats. J Appl Physiol 1994 Jul; 77 (1): 209-15 (Pubitemid 24226137)
17. Kendrick ZV, Steffen CA, Rumsey WL, et al. Effect of estradiol on tissue glycogen metabolism in exercised oophorectomized rats. J Appl Physiol 1987 Aug; 63 (2): 492-6 (Pubitemid 17161949)
18. Bar Or O. Médecine du sport chez l'enfant. Paris: Masson, 1987
19. Boisseau N. Influence du sexe sur le métabolisme à l'exercice et en recuperation: implications nutrionnelles. Sci Sports 2005; 19 (4): 220-7 (Pubitemid 39360349)
20. Boisseau N. Consequence of sport-imposed weight restriction in childhood. Ann Nestlé 2006; 64: 77-84 (Pubitemid 43978940)
21. Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine position stand: the female athlete triad. Med Sci Sports Exerc 2007 Oct; 39 (10): 1867-82
22. Dixon G, Eurman P, Stern BE, et al. Hypothalamic function in amenorrheic runners. Fertil Steril 1984 Sep; 42 (3): 377-83 (Pubitemid 14072155)
23. Manore MM. Dietary recommendations and athletic menstrual dysfunction. Sports Med 2002; 32 (14): 887-901 (Pubitemid 35446297)
24. Czyba JC, Montella A. Biologie de la reproduction humaine. Montpellier: Sauramps Medical, 1993
25. Nahoul K, Roger M. Age-related decline of plasma bioavailable testosterone in adult men. J Steroid Biochem 1990 Feb; 35 (2): 293-9 (Pubitemid 20067775)
26. Loucks AB. The response of luteinizing hormone pulsatility to 5 days of low energy availability disappears by 14 years of gynecological age. J Clin Endocrinol Metab 2006 Aug; 91 (8): 3158-64 (Pubitemid 44271772)
27. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003 Jan; 88 (1): 297-311 (Pubitemid 36115181)
28. Hackney AC. Effects of the menstrual cycle on resting muscle glycogen content. Horm Metab Res 1990 Dec; 22 (12): 647
29. Devries MC, Hamadeh MJ, Phillips SM, et al. Menstrual cycle phase and sex influence muscle glycogen utilization and glucose turnover during moderate-intensity endurance exercise. Am J Physiol Regul Integr Comp Physiol 2006 Oct; 291 (4): R1120-8 (Pubitemid 44498454)
30. Becker KL, Martin B, Boukhris R. Effect of exogenous estrogen and progesterone upon sex chromatin frequency. J Urol 1973 Jan; 109 (1): 79-81
31. Bonen A, Haynes FJ, Watson-Wright W, et al. Effects of menstrual cycle on metabolic responses to exercise. J Appl Physiol 1983 Nov; 55 (5): 1506-13 (Pubitemid 14231458)
32. Bonen A, Haynes FW, Graham TE. Substrate and hormonal responses to exercise in women using oral contraceptives. J Appl Physiol 1991 May; 70 (5): 1917-27
33. Rooney TP, Kendrick ZV, Carlson J, et al. Effect of estradiol on the temporal pattern of exercise-induced tissue glycogen depletion in male rats. J Appl Physiol 1993 Oct; 75 (4): 1502-6 (Pubitemid 23318191)
34. Piers LS, Diggavi SN, Rijskamp J, et al. Resting metabolic rate and thermic effect of a meal in the follicular and luteal phases of the menstrual cycle in well-nourished Indian women. Am J Clin Nutr 1995 Feb; 61 (2): 296-302
35. Horton TJ, Miller EK, Glueck D, et al. No effect of menstrual cycle phase on glucose kinetics and fuel oxidation during moderate-intensity exercise. Am J Physiol Endocrinol Metab 2002 Apr; 282 (4): E752-62 (Pubitemid 34654737)
36. Heiling VJ, Jensen MD. Free fatty acid metabolism in the follicular and luteal phases of the menstrual cycle. J Clin Endocrinol Metab 1992 Apr; 74 (4): 806-10
37. Campbell SE, Febbraio MA. Effects of ovarian hormones on exercise metabolism. Curr Opin Clin Nutr Metab Care 2001 Nov; 4 (6): 515-20 (Pubitemid 34755409)
38. Horton TJ, Hill JO. Prolonged fasting significantly changes nutrient oxidation and glucose tolerance after a normal mixed meal. J Appl Physiol 2001 Jan; 90 (1): 155-63 (Pubitemid 32038516)
39. Zderic TW, Coggan AR, Ruby BC. Glucose kinetics and substrate oxidation during exercise in the follicular and luteal phases. J Appl Physiol 2001 Feb; 90 (2): 447-53 (Pubitemid 32118902)
40. Suh SH, Casazza GA, Horning MA, et al. Effects of oral contraceptives on glucose flux and substrate oxidation rates during rest and exercise. J Appl Physiol 2003 Jan; 94 (1): 285-94 (Pubitemid 36014324)
41. Suh SH, Casazza GA, Horning MA, et al. Luteal and follicular glucose fluxes during rest and exercise in 3-h postabsorptive women. J Appl Physiol 2002 Jul; 93 (1): 42-50 (Pubitemid 34686191)
42. Ruby BC, Robergs RA, Waters DL, et al. Effects of estradiol on substrate turnover during exercise in amenorrheic females. Med Sci Sports Exerc 1997 Sep; 29 (9): 1160-9 (Pubitemid 27407137)
43. Genazzani AR, Lemarchand-Beraud T, Aubert ML, et al. Pattern of plasma ACTH, hGH, and cortisol during menstrual cycle. J Clin Endocrinol Metab 1975 Sep; 41 (3): 431-7
44. Minson CT, Halliwill JR, Young TM, et al. Sympathetic activity and baroreflex sensitivity in young women taking oral contraceptives. Circulation 2000 Sep 26; 102 (13): 1473-6
45. Escalante Pulido JM, Alpizar Salazar M. Changes in insulin sensitivity, secretion and glucose effectiveness during menstrual cycle. Arch Med Res 1999; 30 (1): 19-22
46. Hackney AC, McCracken-Compton MA, Ainsworth B. Substrate responses to submaximal exercise in the midfollicular and midluteal phases of the menstrual cycle. Int J Sport Nutr 1994 Sep; 4 (3): 299-308 (Pubitemid 2139584)
47. De Souza MJ, Maguire MS, Rubin KR, et al. Effects of menstrual phase and amenorrhea on exercise performance in runners. Med Sci Sports Exerc 1990; 22 (5): 575-80 (Pubitemid 20358018)
48. Bailey SP, Zacher CM, Mittleman KD. Effect of menstrual cycle phase on carbohydrate supplementation during prolonged exercise to fatigue. J Appl Physiol 2000 Feb; 88 (2): 690-7 (Pubitemid 30097115)
49. Braun B, Mawson JT, Muza SR, et al. Women at altitude: carbohydrate utilization during exercise at 4,300 m. J Appl Physiol 2000 Jan; 88 (1): 246-56 (Pubitemid 30053852)
50. McLay RT, Thomson CD, Williams SM, et al. Carbohydrate loading and female endurance athletes: effect of menstrual-cycle phase. Int J Sport Nutr Exerc Metab 2007 Apr; 17 (2): 189-205 (Pubitemid 47124228)
51. Bennell K, White S, Crossley K. The oral contraceptive pill: a revolution for sportswomen? Br J Sports Med 1999 Aug; 33 (4): 231-8 (Pubitemid 29373768)
52. Burrows M, Peters CE. The influence of oral contraceptives on athletic performance in female athletes. Sports Med 2007; 37 (7): 557-74 (Pubitemid 47025362)
53. Snow-Harter. Bone health and prevention of osteoporosis in active and athletic women. Clin Sports Med 1994; 13 (2): 389-404
54. Frempong BA, Ricks M, Sen S, et al. Effect of low-dose oral contraceptives on metabolic risk factors in African-American women. J Clin Endocrinol Metab 2008 Jun; 93 (6): 2097-103 (Pubitemid 351831521)
55. Jensen MD, Levine J. Effects of oral contraceptives on free fatty acid metabolism in women. Metabolism 1998 Mar; 47 (3): 280-4 (Pubitemid 28108774)
56. Campbell SE, Febbraio MA. Effect of ovarian hormones on mitochondrial enzyme activity in the fat oxidation pathway of skeletal muscle. Am J Physiol Endocrinol Metab 2001 Oct; 281 (4): E803-8
57. Bemben DA, Boileau RA, Bahr JM, et al. Effects of oral contraceptives on hormonal and metabolic responses during exercise. Med Sci Sports Exerc 1992 Apr; 24 (4): 434-41
58. Casazza GA, Jacobs KA, Suh SH, et al. Menstrual cycle phase and oral contraceptive effects on triglyceride mobilization during exercise. J Appl Physiol 2004 Jul; 97 (1): 302-9 (Pubitemid 38802532)
59. Jacobs KA, Casazza GA, Suh SH, et al. Fatty acid reesterification but not oxidation is increased by oral contraceptive use in women. J Appl Physiol 2005 May; 98 (5): 1720-31 (Pubitemid 40570782)
60. Tremblay J, Peronnet F, Massicotte D, et al. Carbohydrate supplementation and sex differences in fuel selection during exercise. Med Sci Sports Exerc 2010 Jul; 42 (7): 1314-23
61. Boisseau N, Rannou F, Delamarche P, et al. Glucose tolerance during moderate prolonged exercise in women with oral contraceptives as compared to non-users. J Sports Med Phys Fitness 2001 Jun; 41 (2): 203-9 (Pubitemid 32852740)
62. Bernardes RP, Radomski MW. Growth hormone responses to continuous and intermittent exercise in females under oral contraceptive therapy. Eur J Appl Physiol Occup Physiol 1998 Dec; 79 (1): 24-9 (Pubitemid 29041368)
63. Simpson ER, Clyne C, Rubin G, et al. Aromatase: a brief overview. Annu Rev Physiol 2002; 64: 93-127
64. Kotani K, Tokunaga K, Fujioka S, et al. Sexual dimorphism of age-related changes in whole-body fat distribution in the obese. Int J Obes Relat Metab Disord 1994 Apr; 18 (4): 207-2
65. Toth MJ, Tchernof A, Sites CK, et al. Menopause-related changes in body fat distribution. Ann N Y Acad Sci 2000 May; 904: 502-6 (Pubitemid 30389242)
66. Toth MJ, Gardner AW, Arciero PJ, et al. Gender differences in fat oxidation and sympathetic nervous system activity at rest and during submaximal exercise in older individuals. Clin Sci (Lond) 1998 Jul; 95 (1): 59-66 (Pubitemid 28370579)
67. Numao S, Hayashi Y, Katayama Y, et al. Sex differences in substrate oxidation during aerobic exercise in obese men and postmenopausal obese women. Metabolism 2009 Sep; 58 (9): 1312-9
68. Horton TJ, Pagliassotti MJ, Hobbs K, et al. Fuel metabolism in men and women during and after long-duration exercise. J Appl Physiol 1998 Nov; 85 (5): 1823-32 (Pubitemid 28516418)
69. Poehlman ET, Toth MJ, Bunyard LB, et al. Physiological predictors of increasing total and central adiposity in aging men and women. Arch Intern Med 1995 Dec 11-25; 155 (22): 2443-8
70. Lwin R, Darnell B, Oster R, et al. Effect of oral estrogen on substrate utilization in postmenopausal women. Fertil Steril 2008 Oct; 90 (4): 1275-8
71. O'Sullivan AJ, Crampton LJ, Freund J, et al. The route of estrogen replacement therapy confers divergent effects on substrate oxidation and body composition in postmenopausal women. J Clin Invest 1998 Sep 1; 102 (5): 1035-40 (Pubitemid 28419248)
72. dos Reis CM, de Melo NR, Meirelles ES, et al. Body composition, visceral fat distribution and fat oxidation in postmenopausal women using oral or transdermal oestrogen. Maturitas 2003 Sep 25; 46 (1): 59-68 (Pubitemid 37088132)
73. Bjorntorp P. The regulation of adipose tissue distribution in humans. Int J Obes Relat Metab Disord 1996 Apr; 20 (4): 291-302 (Pubitemid 26110403)
74. Kohrt WM, Ehsani AA, Birge Jr SJ. HRT preserves increases in bone mineral density and reductions in body fat after a supervised exercise program. J Appl Physiol 1998 May; 84 (5): 1506-12 (Pubitemid 28225883)
75. Kraemer RR, Johnson LG, Haltom R, et al. Effects of hormone replacement on growth hormone and prolactin exercise responses in postmenopausal women. J Appl Physiol 1998 Feb; 84 (2): 703-8 (Pubitemid 28081126)
76. Johnson LG, Kraemer RR, Haltom R, et al. Effects of estrogen replacement therapy on dehydroepiandrosterone, dehydroepiandrosterone sulfate, and cortisol responses to exercise in postmenopausal women. Fertil Steril 1997 Nov; 68 (5): 836-43 (Pubitemid 27506097)
77. Johnson LG, Kraemer RR, Kraemer GR, et al. Substrate utilization during exercise in postmenopausal women on hormone replacement therapy. Eur J Appl Physiol 2002 Dec; 88 (3): 282-7 (Pubitemid 40824212)
78. Gower BA, Nagy TR, Blaylock ML, et al. Estradiol may limit lipid oxidation via Cpt 1 expression and hormonal mechanisms. Obes Res 2002 Mar; 10 (3): 167-72 (Pubitemid 135687506)
79. Konarzewski M, Diamond JM. Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 1995; 49: 1239-48 (Pubitemid 3025694)
80. Hoffman DM, O'Sullivan AJ, Freund J, et al. Adults with growth hormone deficiency have abnormal body composition but normal energy metabolism. J Clin Endocrinol Metab 1995 Jan; 80 (1): 72-7
81. Kocjan T, Prelevic GM. Hormone replacement therapy update: who should we be prescribing this to now? Curr Opin Obstet Gynecol 2003 Dec; 15 (6): 459-64 (Pubitemid 38333554)
82. Carter SL, Rennie C, Tarnopolsky MA. Substrate utilization during endurance exercise in men and women after endurance training. Am J Physiol Endocrinol Metab 2001 Jun; 280 (6): E898-907
83. Tarnopolsky LJ, MacDougall JD, Atkinson SA, et al. Gender differences in substrate for endurance exercise. J Appl Physiol 1990 Jan; 68 (1): 302-8 (Pubitemid 20075247)
84. Froberg K, Pedersen PK. Sex differences in endurance capacity and metabolic response to prolonged, heavy exercise. Eur J Appl Physiol Occup Physiol 1984; 52 (4): 446-50 (Pubitemid 14084868)
85. Hamadeh MJ, Devries MC, Tarnopolsky MA. Estrogen supplementation reduces whole body leucine and carbohydrate oxidation and increases lipid oxidation in men during endurance exercise. J Clin Endocrinol Metab 2005 Jun; 90 (6): 3592-9 (Pubitemid 41014331)
86. Mittendorfer B, Horowitz JF, Klein S. Effect of gender on lipid kinetics during endurance exercise of moderate intensity in untrained subjects. Am J Physiol Endocrinol Metab 2002 Jul; 283 (1): E58-65 (Pubitemid 34686668)
87. Bunt JC. Metabolic actions of estradiol: significance for acute and chronic exercise responses. Med Sci Sports Exerc 1990 Jun; 22 (3): 286-90 (Pubitemid 20202798)
88. Wideman L, Consitt L, Patrie J, et al. The impact of sex and exercise duration on growth hormone secretion. J Appl Physiol 2006 Dec; 101 (6): 1641-7 (Pubitemid 44904484)
89. Melanson EL, Sharp TA, Seagle HM, et al. Effect of exercise intensity on 24-h energy expenditure and nutrient oxidation. J Appl Physiol 2002 Mar; 92 (3): 1045-52 (Pubitemid 34670959)
90. Roepstorff C, Donsmark M, Thiele M, et al. Sex differences in hormone-sensitive lipase expression, activity, and phosphorylation in skeletal muscle at rest and during exercise. Am J Physiol Endocrinol Metab 2006 Nov; 291 (5): E1106-14
91. Henderson GC, Fattor JA, Horning MA, et al. Lipolysis and fatty acid metabolism in men and women during the postexercise recovery period. J Physiol 2007 Nov 1; 584 (Pt 3): 963-81 (Pubitemid 350031935)
92. D'Eon T, Braun B. The roles of estrogen and progesterone in regulating carbohydrate and fat utilization at rest and during exercise. J Womens Health Gend Based Med 2002 Apr; 11 (3): 225-37
93. Wilson DE, Flowers CM, Carlile SI, et al. Estrogen treatment and gonadal function in the regulation of lipoprotein lipase. Atherosclerosis 1976 Sep; 24 (3): 491-9
94. Mandour T, Kissebah AH, Wynn V. Mechanism of oestrogen and progesterone effects on lipid and carbohydrate metabolism: alteration in the insulin: glucagon molar ratio and hepatic enzyme activity. Eur J Clin Invest 1977 Jun; 7 (3): 181-7 (Pubitemid 8280566)
95. Hansen FM, Fahmy N, Nielsen JH. The influence of sexual hormones on lipogenesis and lipolysis in rat fat cells. Acta Endocrinol (Copenh) 1980 Dec; 95 (4): 566-70 (Pubitemid 11162464)
96. Carrington LJ, Bailey CJ. Effects of natural and synthetic estrogens and progestins on glycogen deposition in female mice. Horm Res 1985; 21 (3): 199-203 (Pubitemid 15090296)
97. Hatta H, Atomi Y, Shinohara S, et al. The effects of ovarian hormones on glucose and fatty acid oxidation during exercise in female ovariectomized rats. Horm Metab Res 1988 Oct; 20 (10): 609-11 (Pubitemid 18264040)
98. Kendrick ZV, Ellis GS. Effect of estradiol on tissue glycogen metabolism and lipid availability in exercised male rats. J Appl Physiol 1991 Nov; 71 (5): 1694-9
99. D'Eon TM, Souza SC, Aronovitz M, et al. Estrogen regulation of adiposity and fuel partitioning: evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J Biol Chem 2005 Oct 28; 280 (43): 35983-91 (Pubitemid 41633867)
100. Alonso A, Fernandez R, Ordonez P, et al. Regulation of estrogen receptor alpha by estradiol in pregnant and estradiol treated rats. Steroids 2006 Dec; 71 (13-14): 1052-61 (Pubitemid 44792164)
101. Heine PA, Taylor JA, Iwamoto GA, et al. Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc Natl Acad Sci USA 2000 Nov 7; 97 (23): 12729-34
102. Cooke PS, Heine PA, Taylor JA, et al. The role of estrogen and estrogen receptor-alpha in male adipose tissue. Mol Cell Endocrinol 2001 Jun 10; 178 (1-2): 147-54 (Pubitemid 32515358)
103. D'Eon TM, Rogers NH, Stancheva ZS, et al. Estradiol and the estradiol metabolite, 2-hydroxyestradiol, activate AMP-activated protein kinase in C2C12 myotubes. Obesity (Silver Spring) 2008 Jun; 16 (6): 1284-8 (Pubitemid 351770527)