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Sex Hormones and Substrate Metabolism During Endurance Exercise

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Sex Hormones, Exercise and Women

Abstract

During endurance exercise, carbohydrates and fat are the main energy sources to ensure muscle contraction. Their relative contribution depends on the exercise modality (intensity and duration) and individual factors, such as age, sex, diet, training, nutritional and weight status. As research protocol standardization is difficult in women’s populations due to the frequent hormonal status changes throughout their life span, studies are predominantly conducted in men. Yet results are frequently extended also to women despite the sexual dimorphism in substrate metabolism during endurance exercise, mainly due to ovarian hormones. Animal and human studies demonstrated the influence of estrogen, and to a lesser extent of progesterone, on fuel mobilization and utilization. However, conflicting results have been obtained on the effect of natural hormone fluctuations during the different phases of the menstrual cycle. Similarly, the influence of oral contraceptives on fuel metabolism is not well understood, although recent formulations seem to favor lipolysis during endurance exercise. Finally, the decline in natural ovarian hormone concentrations observed with the menopause is associated with body composition and substrate metabolism changes. Hormone replacement therapy may also affect substrate metabolism during endurance exercise, but the available results are still contradictory. This chapter describes the sex differences and the effects of menstrual cycle, oral contraceptives, menopause and hormone replacement therapy on substrate metabolism during endurance exercise. Results are sometimes conflicting, mainly due to methodological discrepancies, and further studies are, therefore, needed.

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Abbreviations

AMPC:

Cyclic adenosine monophosphate

AMPK:

Adenosine monophosphate-activated protein kinase

ANP:

Atrial natriuretic peptide

CHO:

Carbohydrates

CPT-I:

Carnitine palmitoyltransferase I

CS:

Citrate synthase

E2:

17β-estradiol

EE:

Ethinyl estradiol

ER:

Estrogen receptors

FFA:

Free fatty acids

FP:

Follicular phase

GH:

Growth hormone

GLUT4:

Glucose transporter type 4

GMPC:

Cyclic guanosine monophosphate

HRT:

Hormone replacement therapy

HSL:

Hormone-sensitive lipase

IGF-1:

Insulin-like growth factor 1

IMCL:

Intramyocellular lipid

LP:

Luteal phase

LPL:

Lipoprotein lipase

MCAD:

Medium-chain acylCoA dehydrogenase

MLOR:

Maximal lipid oxidation rates

mRNA:

Messenger ribonucleic acid

OC:

Oral contraceptives

OC−:

Oral contraceptive nonusers

OC+:

Oral contraceptive users

PDK4:

Pyruvate dehydrogenase kinase isozyme 4

PGC-1α:

Peroxisome proliferator-activated receptor- γ coactivator 1α

PPAR:

Peroxisome proliferator-activated receptor

Ra:

Rate of appearance

Rd:

Rate of disappearance

RER:

Respiratory exchange ratio

SREBP-1c:

Sterol regulatory element-binding protein-1c

VO2max :

Maximal oxygen consumption

β-HAD:

β-hydroxy acyl-CoA dehydrogenase

References

  • Abildgaard J, Pedersen AT, Green CJ, Harder-Lauridsen NM, Solomon TP, Thomsen C, et al. Menopause is associated with decreased whole body fat oxidation during exercise. Am J Physiol Endocrinol Metab. 2013;304(11):E1227–36.

    Article  CAS  PubMed  Google Scholar 

  • Achten J, Gleeson M, Jeukendrup AE. Determination of the exercise intensity that elicits maximal fat oxidation. Med Sci Sports Exerc. 2002;34(1):92–7.

    Article  PubMed  Google Scholar 

  • Bailey SP, Zacher CM, Mittleman KD. Effect of menstrual cycle phase on carbohydrate supplementation during prolonged exercise to fatigue. J Appl Physiol. 2000;88(2):690–7.

    CAS  PubMed  Google Scholar 

  • Beckett T, Tchernof A, Toth MJ. Effect of ovariectomy and estradiol replacement on skeletal muscle enzyme activity in female rats. Metabolism. 2002;51(11):1397–401.

    Article  CAS  PubMed  Google Scholar 

  • Belo NO, Sairam MR, Dos Reis AM. Impairment of the natriuretic peptide system in follitropin receptor knockout mice and reversal by estradiol: implications for obesity-associated hypertension in menopause. Endocrinology. 2008;149(3):1399–406.

    Article  CAS  PubMed  Google Scholar 

  • Bemben DA, Boileau RA, Bahr JM, Nelson RA, Misner JE. Effects of oral contraceptives on hormonal and metabolic responses during exercise. Med Sci Sports Exerc. 1992;24(4):434–41.

    Article  CAS  PubMed  Google Scholar 

  • Benagiano G, Bastianelli C, Farris M. Hormonal contraception: present and future. Drugs Today (Barc). 2008;44(12):905–23.

    Article  CAS  Google Scholar 

  • Bennell K, White S, Crossley K. The oral contraceptive pill: a revolution for sportswomen? Br J Sports Med. 1999;33(4):231–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benoit V, Valette A, Mercier L, Meignen JM, Boyer J. Potentiation of epinephrine-induced lipolysis in fat cells from estrogen-treated rats. Biochem Biophys Res Commun. 1982;109(4):1186–91.

    Article  CAS  PubMed  Google Scholar 

  • 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;79(1):24–9.

    Article  CAS  PubMed  Google Scholar 

  • Berthon PM, Howlett RA, Heigenhauser GJ, Spriet LL. Human skeletal muscle carnitine palmitoyltransferase I activity determined in isolated intact mitochondria. J Appl Physiol (1985). 1998;85(1):148–53.

    CAS  Google Scholar 

  • Bjorntorp P. The regulation of adipose tissue distribution in humans. Int J Obes Relat Metab Disord. 1996;20(4):291–302.

    CAS  PubMed  Google Scholar 

  • Blatchford FK, Knowlton RG, Schneider DA. Plasma FFA responses to prolonged walking in untrained men and women. Eur J Appl Physiol Occup Physiol. 1985;53(4):343–7.

    Article  CAS  PubMed  Google Scholar 

  • Boardman HM, Hartley L, Eisinga A, Main C, Roque i Figuls M, Bonfill Cosp X, et al. Hormone therapy for preventing cardiovascular disease in post-menopausal women. Cochrane Database Syst Rev. 2015;3, CD002229.

    Google Scholar 

  • Boisseau N, Rannou F, Delamarche P, Bentue-Ferrer D, Gratas-Delamarche A. Glucose tolerance during moderate prolonged exercise in women with oral contraceptives as compared to non-users. J Sports Med Phys Fitness. 2001;41(2):203–9.

    CAS  PubMed  Google Scholar 

  • Bonen A, Haynes FW, Graham TE. Substrate and hormonal responses to exercise in women using oral contraceptives. J Appl Physiol. 1991;70(5):1917–27.

    CAS  PubMed  Google Scholar 

  • Bordenave S, Metz L, Flavier S, Lambert K, Ghanassia E, Dupuy AM, et al. Training-induced improvement in lipid oxidation in type 2 diabetes mellitus is related to alterations in muscle mitochondrial activity. Effect of endurance training in type 2 diabetes. Diabetes Metab. 2008;34(2):162–8.

    Article  CAS  PubMed  Google Scholar 

  • Brooks GA, Mercier J. Balance of carbohydrate and lipid utilization during exercise: the “crossover” concept. J Appl Physiol. 1994;76(6):2253–61.

    CAS  PubMed  Google Scholar 

  • Bunt JC. Metabolic actions of estradiol: significance for acute and chronic exercise responses. Med Sci Sports Exerc. 1990;22(3):286–90.

    Article  CAS  PubMed  Google Scholar 

  • Burguera B, Proctor D, Dietz N, Guo Z, Joyner M, Jensen MD. Leg free fatty acid kinetics during exercise in men and women. Am J Physiol Endocrinol Metab. 2000;278(1):E113–7.

    CAS  PubMed  Google Scholar 

  • Burrows M, Peters CE. The influence of oral contraceptives on athletic performance in female athletes. Sports Med. 2007;37(7):557–74.

    Article  PubMed  Google Scholar 

  • 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;281(4):E803–8.

    CAS  PubMed  Google Scholar 

  • Campbell SE, Febbraio MA. Effect of the ovarian hormones on GLUT4 expression and contraction-stimulated glucose uptake. Am J Physiol Endocrinol Metab. 2002;282(5):E1139–46.

    Article  CAS  PubMed  Google Scholar 

  • Campbell SE, Angus DJ, Febbraio MA. Glucose kinetics and exercise performance during phases of the menstrual cycle: effect of glucose ingestion. Am J Physiol Endocrinol Metab. 2001;281(4):E817–25.

    CAS  PubMed  Google Scholar 

  • Carter S, McKenzie S, Mourtzakis M, Mahoney DJ, Tarnopolsky MA. Short-term 17beta-estradiol decreases glucose R(a) but not whole body metabolism during endurance exercise. J Appl Physiol (1985). 2001a;90(1):139–46.

    CAS  Google Scholar 

  • Carter SL, Rennie C, Tarnopolsky MA. Substrate utilization during endurance exercise in men and women after endurance training. Am J Physiol Endocrinol Metab. 2001b;280(6):E898–907.

    CAS  PubMed  Google Scholar 

  • Casazza GA, Jacobs KA, Suh SH, Miller BF, Horning MA, Brooks GA. Menstrual cycle phase and oral contraceptive effects on triglyceride mobilization during exercise. J Appl Physiol. 2004;97(1):302–9.

    Article  CAS  PubMed  Google Scholar 

  • Clark BA, Elahi D, Epstein FH. The influence of gender, age, and the menstrual cycle on plasma atrial natriuretic peptide. J Clin Endocrinol Metab. 1990;70(2):349–52.

    Article  CAS  PubMed  Google Scholar 

  • Constantini NW, Dubnov G, Lebrun CM. The menstrual cycle and sport performance. Clin Sports Med. 2005;24(2):e51–82. xiii-xiv.

    Article  PubMed  Google Scholar 

  • Costill DL, Daniels J, Evans W, Fink W, Krahenbuhl G, Saltin B. Skeletal muscle enzymes and fiber composition in male and female track athletes. J Appl Physiol. 1976;40(2):149–54.

    CAS  PubMed  Google Scholar 

  • Davidson BJ, Rea CD, Valenzuela GJ. Atrial natriuretic peptide, plasma renin activity, and aldosterone in women on estrogen therapy and with premenstrual syndrome. Fertil Steril. 1988;50(5):743–6.

    Article  CAS  PubMed  Google Scholar 

  • de Melo NR, Aldrighi JM, Faggion Jr D, Reyes VR, Souza JB, Fernandes CE, et al. A prospective open-label study to evaluate the effects of the oral contraceptive Harmonet (gestodene75/EE20) on body fat. Contraception. 2004;70(1):65–71.

    Article  PubMed  CAS  Google Scholar 

  • De Souza MJ, Maguire MS, Rubin KR, Maresh CM. Effects of menstrual phase and amenorrhea on exercise performance in runners. Med Sci Sports Exerc. 1990;22(5):575–80.

    Article  PubMed  Google Scholar 

  • D’Eon TM, Sharoff C, Chipkin SR, Grow D, Ruby BC, Braun B. Regulation of exercise carbohydrate metabolism by estrogen and progesterone in women. Am J Physiol Endocrinol Metab. 2002;283(5):E1046–55.

    Article  PubMed  Google Scholar 

  • D’Eon TM, Souza SC, Aronovitz M, Obin MS, Fried SK, Greenberg AS. Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J Biol Chem. 2005;280(43):35983–91.

    Article  PubMed  CAS  Google Scholar 

  • D’Eon TM, Rogers NH, Stancheva ZS, Greenberg AS. Estradiol and the estradiol metabolite, 2-hydroxyestradiol, activate AMP-activated protein kinase in C2C12 myotubes. Obesity (Silver Spring). 2008;16(6):1284–8.

    Article  CAS  Google Scholar 

  • Devries MC, Hamadeh MJ, Graham TE, Tarnopolsky MA. 17beta-estradiol supplementation decreases glucose rate of appearance and disappearance with no effect on glycogen utilization during moderate intensity exercise in men. J Clin Endocrinol Metab. 2005;90(11):6218–25.

    Article  CAS  PubMed  Google Scholar 

  • Devries MC, Hamadeh MJ, Phillips SM, Tarnopolsky MA. 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;291(4):R1120–8.

    Article  CAS  PubMed  Google Scholar 

  • Devries MC, Lowther SA, Glover AW, Hamadeh MJ, Tarnopolsky MA. IMCL area density, but not IMCL utilization, is higher in women during moderate-intensity endurance exercise, compared with men. Am J Physiol Regul Integr Comp Physiol. 2007;293(6):R2336–42.

    Article  CAS  PubMed  Google Scholar 

  • Dombovy ML, Bonekat HW, Williams TJ, Staats BA. Exercise performance and ventilatory response in the menstrual cycle. Med Sci Sports Exerc. 1987;19(2):111–7.

    Article  CAS  PubMed  Google Scholar 

  • dos Reis CM, de Melo NR, Meirelles ES, Vezozzo DP, Halpern A. Body composition, visceral fat distribution and fat oxidation in postmenopausal women using oral or transdermal oestrogen. Maturitas. 2003;46(1):59–68.

    Article  PubMed  CAS  Google Scholar 

  • Ellis GS, Lanza-Jacoby S, Gow A, Kendrick ZV. Effects of estradiol on lipoprotein lipase activity and lipid availability in exercised male rats. J Appl Physiol. 1994;77(1):209–15.

    CAS  PubMed  Google Scholar 

  • Esbjornsson-Liljedahl M, Sundberg CJ, Norman B, Jansson E. Metabolic response in type I and type II muscle fibers during a 30-s cycle sprint in men and women. J Appl Physiol (1985). 1999;87(4):1326–32.

    CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Genazzani AR, Lemarchand-Beraud T, Aubert ML, Felber JP. Pattern of plasma ACTH, hGH, and cortisol during menstrual cycle. J Clin Endocrinol Metab. 1975;41(3):431–7.

    Article  CAS  PubMed  Google Scholar 

  • Gower BA, Nagy TR, Blaylock ML, Wang C, Nyman L. Estradiol may limit lipid oxidation via Cpt 1 expression and hormonal mechanisms. Obes Res. 2002;10(3):167–72.

    Article  CAS  PubMed  Google Scholar 

  • Hackney AC. Effects of the menstrual cycle on resting muscle glycogen content. Horm Metab Res. 1990;22(12):647.

    Article  CAS  PubMed  Google Scholar 

  • Hackney AC. Influence of oestrogen on muscle glycogen utilization during exercise. Acta Physiol Scand. 1999;167(3):273–4.

    Article  CAS  PubMed  Google Scholar 

  • 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;4(3):299–308.

    Article  CAS  PubMed  Google Scholar 

  • Hackney AC, Muoio D, Meyer WR. The Effect of sex steroid hormones on substrate oxidation during prolonged submaximal exercise in women. Jpn J Physiol. 2000;50(5):489–94.

    Article  CAS  PubMed  Google Scholar 

  • 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;90(6):3592–9.

    Article  CAS  PubMed  Google Scholar 

  • Hatta H, Atomi Y, Shinohara S, Yamamoto Y, Yamada S. The effects of ovarian hormones on glucose and fatty acid oxidation during exercise in female ovariectomized rats. Horm Metab Res. 1988;20(10):609–11.

    Article  CAS  PubMed  Google Scholar 

  • Heiling VJ, Jensen MD. Free fatty acid metabolism in the follicular and luteal phases of the menstrual cycle. J Clin Endocrinol Metab. 1992;74(4):806–10.

    Article  CAS  PubMed  Google Scholar 

  • Hoffman DM, O’Sullivan AJ, Freund J, Ho KK. Adults with growth hormone deficiency have abnormal body composition but normal energy metabolism. J Clin Endocrinol Metab. 1995;80(1):72–7.

    CAS  PubMed  Google Scholar 

  • Hong M, Yan Q, Tao B, Boersma A, Han KK, Vantyghem MC, et al. Estradiol, progesterone and testosterone exposures affect the atrial natriuretic peptide gene expression in vivo in rats. Biol Chem Hoppe Seyler. 1992;373(4):213–8.

    Article  CAS  PubMed  Google Scholar 

  • Horton TJ, Pagliassotti MJ, Hobbs K, Hill JO. Fuel metabolism in men and women during and after long-duration exercise. J Appl Physiol. 1998;85(5):1823–32.

    CAS  PubMed  Google Scholar 

  • Horton TJ, Miller EK, Glueck D, Tench K. No effect of menstrual cycle phase on glucose kinetics and fuel oxidation during moderate-intensity exercise. Am J Physiol Endocrinol Metab. 2002;282(4):E752–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horton TJ, Miller EK, Bourret K. No effect of menstrual cycle phase on glycerol or palmitate kinetics during 90 min of moderate exercise. J Appl Physiol (1985). 2006;100(3):917–25.

    Article  CAS  Google Scholar 

  • Isacco L, Duche P, Boisseau N. Influence of hormonal status on substrate utilization at rest and during exercise in the female population. Sports Med. 2012a;42(4):327–42.

    Article  PubMed  Google Scholar 

  • Isacco L, Thivel D, Pelle AM, Zouhal H, Duclos M, Duche P, et al. Oral contraception and energy intake in women: impact on substrate oxidation during exercise. Appl Physiol Nutr Metab. 2012b;37(4):646–56.

    Article  CAS  PubMed  Google Scholar 

  • Isacco L, Thivel D, Meddahi-Pelle A, Lemoine-Morel S, Duclos M, Boisseau N. Exercise per se masks oral contraceptive-induced postprandial lipid mobilization. Appl Physiol Nutr Metab. 2014;1–8.

    Google Scholar 

  • Isacco L, Thivel D, Pereira B, Duclos M, Boisseau N. Maximal fat oxidation, but not aerobic capacity, is affected by oral contraceptive use in young healthy women. Eur J Appl Physiol. 2015;115(5):937–45.

    Article  CAS  PubMed  Google Scholar 

  • Jacobs KA, Casazza GA, Suh SH, Horning MA, Brooks GA. Fatty acid reesterification but not oxidation is increased by oral contraceptive use in women. J Appl Physiol. 2005;98(5):1720–31.

    Article  CAS  PubMed  Google Scholar 

  • Jensen MD, Levine J. Effects of oral contraceptives on free fatty acid metabolism in women. Metabolism. 1998;47(3):280–4.

    Article  CAS  PubMed  Google Scholar 

  • Jensen MD, Martin ML, Cryer PE, Roust LR. Effects of estrogen on free fatty acid metabolism in humans. Am J Physiol. 1994;266(6 Pt 1):E914–20.

    CAS  PubMed  Google Scholar 

  • Jeukendrup AE. Modulation of carbohydrate and fat utilization by diet, exercise and environment. Biochem Soc Trans. 2003;31(Pt 6):1270–3.

    Article  CAS  PubMed  Google Scholar 

  • Jeukendrup AE, Wallis GA. Measurement of substrate oxidation during exercise by means of gas exchange measurements. Int J Sports Med. 2005;26 Suppl 1:S28–37.

    Article  CAS  PubMed  Google Scholar 

  • Johnson LG, Kraemer RR, Haltom R, Kraemer GR, Gaines HE, Castracane VD. Effects of estrogen replacement therapy on dehydroepiandrosterone, dehydroepiandrosterone sulfate, and cortisol responses to exercise in postmenopausal women. Fertil Steril. 1997;68(5):836–43.

    Article  CAS  PubMed  Google Scholar 

  • Johnson LG, Kraemer RR, Kraemer GR, Haltom RW, Cordill AE, Welsch MA, et al. Substrate utilization during exercise in postmenopausal women on hormone replacement therapy. Eur J Appl Physiol. 2002;88(3):282–7.

    Article  CAS  PubMed  Google Scholar 

  • Kanaley JA, Boileau RA, Bahr JA, Misner JE, Nelson RA. Substrate oxidation and GH responses to exercise are independent of menstrual phase and status. Med Sci Sports Exerc. 1992;24(8):873–80.

    Article  CAS  PubMed  Google Scholar 

  • Kelley DE. Skeletal muscle fat oxidation: timing and flexibility are everything. J Clin Invest. 2005;115(7):1699–702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kendrick ZV, Steffen CA, Rumsey WL, Goldberg DI. Effect of estradiol on tissue glycogen metabolism in exercised oophorectomized rats. J Appl Physiol. 1987;63(2):492–6.

    CAS  PubMed  Google Scholar 

  • Kiens B, Roepstorff C, Glatz JF, Bonen A, Schjerling P, Knudsen J, et al. Lipid-binding proteins and lipoprotein lipase activity in human skeletal muscle: influence of physical activity and gender. J Appl Physiol (1985). 2004;97(4):1209–18.

    Article  CAS  Google Scholar 

  • Klein S, Coyle EF, Wolfe RR. Fat metabolism during low-intensity exercise in endurance-trained and untrained men. Am J Physiol. 1994;267(6 Pt 1):E934–40.

    CAS  PubMed  Google Scholar 

  • Kocjan T, Prelevic GM. Hormone replacement therapy update: who should we be prescribing this to now? Curr Opin Obstet Gynecol. 2003;15(6):459–64.

    Article  PubMed  Google Scholar 

  • 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;84(5):1506–12.

    CAS  PubMed  Google Scholar 

  • Konarzewski M, Diamond JM. Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution. 1995;49:1239–48.

    Article  Google Scholar 

  • Koppo K, Larrouy D, Marques MA, Berlan M, Bajzova M, Polak J, et al. Lipid mobilization in subcutaneous adipose tissue during exercise in lean and obese humans. Roles of insulin and natriuretic peptides. Am J Physiol Endocrinol Metab. 2010;299(2):E258–65.

    CAS  PubMed  Google Scholar 

  • Kraemer RR, Johnson LG, Haltom R, Kraemer GR, Gaines H, Drapcho M, et al. Effects of hormone replacement on growth hormone and prolactin exercise responses in postmenopausal women. J Appl Physiol. 1998;84(2):703–8.

    CAS  PubMed  Google Scholar 

  • Lafontan M, Moro C, Sengenes C, Galitzky J, Crampes F, Berlan M. An unsuspected metabolic role for atrial natriuretic peptides: the control of lipolysis, lipid mobilization, and systemic nonesterified fatty acids levels in humans. Arterioscler Thromb Vasc Biol. 2005;25(10):2032–42.

    Article  CAS  PubMed  Google Scholar 

  • Lambert EV, Hawley JA, Goedecke J, Noakes TD, Dennis SC. Nutritional strategies for promoting fat utilization and delaying the onset of fatigue during prolonged exercise. J Sports Sci. 1997;15(3):315–24.

    Article  CAS  PubMed  Google Scholar 

  • Lavoie JM, Dionne N, Helie R, Brisson GR. Menstrual cycle phase dissociation of blood glucose homeostasis during exercise. J Appl Physiol (1985). 1987;62(3):1084–9.

    CAS  Google Scholar 

  • Lebrun CM. The effect of the phase of the menstrual cycle and the birth control pill on athletic performance. Clin Sports Med. 1994;13(2):419–41.

    CAS  PubMed  Google Scholar 

  • Lovejoy JC, Champagne CM, de Jonge L, Xie H, Smith SR. Increased visceral fat and decreased energy expenditure during the menopausal transition. Int J Obes (Lond). 2008;32(6):949–58.

    Article  CAS  Google Scholar 

  • Lupo M, Dains JE, Madsen LT. Hormone replacement therapy: an increased risk of recurrence and mortality for breast cancer patients? J Adv Pract Oncol. 2015;6(4):322–30.

    PubMed  PubMed Central  Google Scholar 

  • Lwin R, Darnell B, Oster R, Lawrence J, Foster J, Azziz R, et al. Effect of oral estrogen on substrate utilization in postmenopausal women. Fertil Steril. 2008;90(4):1275–8.

    Article  PubMed  Google Scholar 

  • Maffei S, Del Ry S, Prontera C, Clerico A. Increase in circulating levels of cardiac natriuretic peptides after hormone replacement therapy in postmenopausal women. Clin Sci (Lond). 2001;101(5):447–53.

    Article  CAS  Google Scholar 

  • Magkos F, Patterson BW, Mittendorfer B. No effect of menstrual cycle phase on basal very-low-density lipoprotein triglyceride and apolipoprotein B-100 kinetics. Am J Physiol Endocrinol Metab. 2006;291(6):E1243–9.

    Article  CAS  PubMed  Google Scholar 

  • Maher AC, Akhtar M, Vockley J, Tarnopolsky MA. Women have higher protein content of beta-oxidation enzymes in skeletal muscle than men. PLoS One. 2010;5(8), e12025.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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;7(3):181–7.

    Article  CAS  PubMed  Google Scholar 

  • Matute ML, Kalkhoff RK. Sex steroid influence on hepatic gluconeogenesis and glucogen formation. Endocrinology. 1973;92(3):762–8.

    Article  CAS  PubMed  Google Scholar 

  • Mc KK, Coulomb B, Kaleita E, De Renzo EC. Some effects of in vivo administered estrogens on glucose metabolism and adrenal cortical secretion in vitro. Endocrinology. 1958;63(6):709–22.

    Article  Google Scholar 

  • McKenzie S, Phillips SM, Carter SL, Lowther S, Gibala MJ, Tarnopolsky MA. Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans. Am J Physiol Endocrinol Metab. 2000;278(4):E580–7.

    CAS  PubMed  Google Scholar 

  • McLay RT, Thomson CD, Williams SM, Rehrer NJ. Carbohydrate loading and female endurance athletes: effect of menstrual-cycle phase. Int J Sport Nutr Exerc Metab. 2007;17(2):189–205.

    Article  CAS  PubMed  Google Scholar 

  • Minson CT, Halliwill JR, Young TM, Joyner MJ. Sympathetic activity and baroreflex sensitivity in young women taking oral contraceptives. Circulation. 2000;102(13):1473–6.

    Article  CAS  PubMed  Google Scholar 

  • Moro C, Crampes F, Sengenes C. Atrial natriuretic peptide contributes to the physiological control of lipid mobilization in humans. FASEB J. 2004;18:908–10.

    CAS  PubMed  Google Scholar 

  • Nicklas BJ, Hackney AC, Sharp RL. The menstrual cycle and exercise: performance, muscle glycogen, and substrate responses. Int J Sports Med. 1989;10(4):264–9.

    Article  CAS  PubMed  Google Scholar 

  • Norrelund H. Consequences of growth hormone deficiency for intermediary metabolism and effects of replacement. Front Horm Res. 2005;33:103–20.

    PubMed  Google Scholar 

  • Numao S, Hayashi Y, Katayama Y, Matsuo T, Tanaka K. Sex differences in substrate oxidation during aerobic exercise in obese men and postmenopausal obese women. Metabolism. 2009;58(9):1312–9.

    Article  CAS  PubMed  Google Scholar 

  • Oosthuyse T, Bosch AN. The effect of the menstrual cycle on exercise metabolism: implications for exercise performance in eumenorrhoeic women. Sports Med. 2010;40(3):207–27.

    Article  PubMed  Google Scholar 

  • Oosthuyse T, Bosch AN. Oestrogen’s regulation of fat metabolism during exercise and gender specific effects. Curr Opin Pharmacol. 2012;12(3):363–71.

    Article  CAS  PubMed  Google Scholar 

  • O’Sullivan AJ, Ho KK. A comparison of the effects of oral and transdermal estrogen replacement on insulin sensitivity in postmenopausal women. J Clin Endocrinol Metab. 1995;80(6):1783–8.

    PubMed  Google Scholar 

  • O’Sullivan AJ, Crampton LJ, Freund J, Ho KK. The route of estrogen replacement therapy confers divergent effects on substrate oxidation and body composition in postmenopausal women. J Clin Invest. 1998;102(5):1035–40.

    Article  PubMed  PubMed Central  Google Scholar 

  • Perez-Martin A, Dumortier M, Raynaud E, Brun JF, Fedou C, Bringer J, et al. Balance of substrate oxidation during submaximal exercise in lean and obese people. Diabetes Metab. 2001;27(4 Pt 1):466–74.

    CAS  PubMed  Google Scholar 

  • Picard F, Wanatabe M, Schoonjans K, Lydon J, O’Malley BW, Auwerx J. Progesterone receptor knockout mice have an improved glucose homeostasis secondary to beta -cell proliferation. Proc Natl Acad Sci U S A. 2002;99(24):15644–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piers LS, Diggavi SN, Rijskamp J, van Raaij JM, Shetty PS, Hautvast JG. 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;61(2):296–302.

    CAS  PubMed  Google Scholar 

  • Redman LM, Scroop GC, Westlander G, Norman RJ. Effect of a synthetic progestin on the exercise status of sedentary young women. J Clin Endocrinol Metab. 2005;90(7):3830–7.

    Article  CAS  PubMed  Google Scholar 

  • Reilly T. The menstrual cycle and human performance: an overview. Biol Rhythm Res. 2000;31(1):29–40.

    Article  CAS  Google Scholar 

  • Reinke U, Ansah B, Voigt KD. Effect of the menstrual cycle on carbohydrate and lipid metabolism in normal females. Acta Endocrinol (Copenh). 1972;69(4):762–8.

    CAS  Google Scholar 

  • Roepstorff C, Steffensen CH, Madsen M, Stallknecht B, Kanstrup IL, Richter EA, et al. Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab. 2002;282(2):E435–47.

    Article  CAS  PubMed  Google Scholar 

  • Roepstorff C, Donsmark M, Thiele M, Vistisen B, Stewart G, Vissing K, 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;291(5):E1106–14.

    Article  CAS  PubMed  Google Scholar 

  • Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, et al. Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol. 1993;265(3 Pt 1):E380–91.

    CAS  PubMed  Google Scholar 

  • Romijn JA, Coyle EF, Sidossis LS, Rosenblatt J, Wolfe RR. Substrate metabolism during different exercise intensities in endurance-trained women. J Appl Physiol. 2000;88(5):1707–14.

    CAS  PubMed  Google Scholar 

  • Ruby BC, Robergs RA, Waters DL, Burge M, Mermier C, Stolarczyk L. Effects of estradiol on substrate turnover during exercise in amenorrheic females. Med Sci Sports Exerc. 1997;29(9):1160–9.

    Article  CAS  PubMed  Google Scholar 

  • Sengenes C, Bouloumie A, Hauner H, Berlan M, Busse R, Lafontan M, et al. Involvement of a cGMP-dependent pathway in the natriuretic peptide-mediated hormone-sensitive lipase phosphorylation in human adipocytes. J Biol Chem. 2003;278(49):48617–26.

    Article  CAS  PubMed  Google Scholar 

  • Sengenes C, Moro C, Galitzky J, Berlan M, Lafontan M. Natriuretic peptides: a new lipolytic pathway in human fat cells. Med Sci (Paris). 2005;21 Spec No:29–33.

    Google Scholar 

  • Shufelt CL, Bairey Merz CN. Contraceptive hormone use and cardiovascular disease. J Am Coll Cardiol. 2009;53(3):221–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson ER, Clyne C, Rubin G, Boon WC, Robertson K, Britt K, et al. Aromatase--a brief overview. Annu Rev Physiol. 2002;64:93–127.

    Article  CAS  PubMed  Google Scholar 

  • Sitruk-Ware R, Nath A. Metabolic effects of contraceptive steroids. Rev Endocr Metab Disord. 2011;12(2):63–75.

    Article  CAS  PubMed  Google Scholar 

  • Sladek CD. Gluconeogenesis and hepatic glycogen formation in relation to the rat estrous cycle. Horm Metab Res. 1974;6(3):217–21.

    Article  CAS  PubMed  Google Scholar 

  • Snow-Harter CM. Bone health and prevention of osteoporosis in active and athletic women. Clin Sports Med. 1994;13(2):389–404.

    CAS  PubMed  Google Scholar 

  • Sowers M, Zheng H, Tomey K, Karvonen-Gutierrez C, Jannausch M, Li X, et al. Changes in body composition in women over six years at midlife: ovarian and chronological aging. J Clin Endocrinol Metab. 2007;92(3):895–901.

    Article  CAS  PubMed  Google Scholar 

  • Steffensen CH, Roepstorff C, Madsen M, Kiens B. Myocellular triacylglycerol breakdown in females but not in males during exercise. Am J Physiol Endocrinol Metab. 2002;282(3):E634–42.

    Article  CAS  PubMed  Google Scholar 

  • Suh SH, Casazza GA, Horning MA, Miller BF, Brooks GA. Luteal and follicular glucose fluxes during rest and exercise in 3-h postabsorptive women. J Appl Physiol. 2002;93(1):42–50.

    Article  CAS  PubMed  Google Scholar 

  • Suh SH, Casazza GA, Horning MA, Miller BF, Brooks GA. Effects of oral contraceptives on glucose flux and substrate oxidation rates during rest and exercise. J Appl Physiol. 2003;94(1):285–94.

    Article  CAS  PubMed  Google Scholar 

  • Sutter-Dub MT, Vergnaud MT. Progesterone and glucose metabolism in the female rat adipocyte: effect on hexokinase activity. J Endocrinol. 1982;95(3):369–75.

    Article  CAS  PubMed  Google Scholar 

  • Tarnopolsky MA. Sex differences in exercise metabolism and the role of 17-beta estradiol. Med Sci Sports Exerc. 2008;40(4):648–54.

    Article  CAS  PubMed  Google Scholar 

  • Tarnopolsky LJ, MacDougall JD, Atkinson SA, Tarnopolsky MA, Sutton JR. Gender differences in substrate for endurance exercise. J Appl Physiol. 1990;68(1):302–8.

    CAS  PubMed  Google Scholar 

  • Tarnopolsky MA, Atkinson SA, Phillips SM, MacDougall JD. Carbohydrate loading and metabolism during exercise in men and women. J Appl Physiol (1985). 1995;78(4):1360–8.

    CAS  Google Scholar 

  • Tarnopolsky MA, Zawada C, Richmond LB, Carter S, Shearer J, Graham T, et al. Gender differences in carbohydrate loading are related to energy intake. J Appl Physiol (1985). 2001;91(1):225–30.

    CAS  Google Scholar 

  • Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, Hamadeh MJ. Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol. 2007;292(3):R1271–8.

    Article  CAS  PubMed  Google Scholar 

  • Toth MJ, Gardner AW, Arciero PJ, Calles-Escandon J, Poehlman ET. Gender differences in fat oxidation and sympathetic nervous system activity at rest and during submaximal exercise in older individuals. Clin Sci (Lond). 1998;95(1):59–66.

    Article  CAS  Google Scholar 

  • Tremblay J, Peronnet F, Massicotte D, Lavoie C. Carbohydrate supplementation and sex differences in fuel selection during exercise. Med Sci Sports Exerc. 2010;42(7):1314–23.

    Article  CAS  PubMed  Google Scholar 

  • Tremollieres F. Oral combined contraception: is there any difference between ethinyl-estradiol and estradiol? Gynecol Obstet Fertil. 2012;40(2):109–15.

    Article  CAS  PubMed  Google Scholar 

  • Uranga AP, Levine J, Jensen M. Isotope tracer measures of meal fatty acid metabolism: reproducibility and effects of the menstrual cycle. Am J Physiol Endocrinol Metab. 2005;288(3):E547–55.

    Article  CAS  PubMed  Google Scholar 

  • Vieira-Potter VJ, Zidon TM, Padilla J. Exercise and estrogen make fat cells “Fit”. Exerc Sport Sci Rev. 2015;43(3):172–8.

    Google Scholar 

  • Weinstein I, Cook GA, Heimberg M. Regulation by oestrogen of carnitine palmitoyltransferase in hepatic mitochondria. Biochem J. 1986;237(2):593–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenz M, Berend JZ, Lynch NA, Chappell S, Hackney AC. Substrate oxidation at rest and during exercise: effects of menstrual cycle phase and diet composition. J Physiol Pharmacol. 1997;48(4):851–60.

    CAS  PubMed  Google Scholar 

  • White LJ, Ferguson MA, McCoy SC, Kim H. Intramyocellular lipid changes in men and women during aerobic exercise: a (1)H-magnetic resonance spectroscopy study. J Clin Endocrinol Metab. 2003;88(12):5638–43.

    Article  CAS  PubMed  Google Scholar 

  • Wolfe RR, Peters EJ, Klein S, Holland OB, Rosenblatt J, Gary Jr H. Effect of short-term fasting on lipolytic responsiveness in normal and obese human subjects. Am J Physiol. 1987;252(2 Pt 1):E189–96.

    CAS  PubMed  Google Scholar 

  • Yasui T, Uemura H, Takikawa M, Irahara M. Hormone replacement therapy in postmenopausal women. J Med Invest. 2003;50(3-4):136–45.

    PubMed  Google Scholar 

  • Zderic TW, Coggan AR, Ruby BC. Glucose kinetics and substrate oxidation during exercise in the follicular and luteal phases. J Appl Physiol. 2001;90(2):447–53.

    CAS  PubMed  Google Scholar 

  • Zehnder M, Ith M, Kreis R, Saris W, Boutellier U, Boesch C. Gender-specific usage of intramyocellular lipids and glycogen during exercise. Med Sci Sports Exerc. 2005;37(9):1517–24.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Prognostic Markers and Regulatory Factors of Cardiovascular Diseases and Exercise Performance Health Innovation Platform, University of Bourgogne Franche-Comte, Besançon, France

    Laurie Isacco Ph.D.

  2. Laboratory of the Metabolic Adaptations to Exercise under Physiological and Pathological condition, Clermont Auvergne University, Clermont-Ferrand, France

    Nathalie Boisseau Ph.D.

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  1. Laurie Isacco Ph.D.
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  2. Nathalie Boisseau Ph.D.
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Correspondence to Laurie Isacco Ph.D. .

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  1. Department of Nutrition, University of North Carolina, Chapel Hill, North Carolina, USA

    Anthony C. Hackney

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Isacco, L., Boisseau, N. (2017). Sex Hormones and Substrate Metabolism During Endurance Exercise. In: Hackney, A. (eds) Sex Hormones, Exercise and Women. Springer, Cham. https://doi.org/10.1007/978-3-319-44558-8_3

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