Estrogen and Substrate Metabolism

Estrogen and Substrate MetabolismA Review of Contradictory Research

Candi D. Ashley,1 Marianne Leverone Kramer2 and Phillip Bishop3

1 School of Physical Education, Wellness, and Sports Studies, University of South Florida, Tampa,Florida, USA

2 Department of Biochemistry, East Tennessee State University, Johnson City, Tennessee, USA3 College of Education, The University of Alabama, Tuscaloosa, Alabama, USA

Abstract The increasing number of females participating in physical activity has height-ened our awareness of changes in the menstrual cycle which often accompanyphysical activity. As such, there has been a considerable amount of research investi-gating the relationships between menstrual cycle changes and bone mineral den-sity, performance, ventilation and substrate metabolism. Anumber of researchershave concluded that there may be enhanced fat metabolism in eumenorrhoeicversus amenorrhoeic females, or in the follicular phase versus the luteal phase ofthe menstrual cycle, due to the theoretical estrogen level in eumenorrhoeic versusamenorrhoeic females or the luteal phase versus the follicular phase. However, adefinite relationship between resting estrogen level and substrate metabolism hasnot been clearly established. In addition, the mechanisms which may be respon-sible for the effect of estrogen on substrate metabolism have not been addressed.It appears that the effects of estrogen on metabolism may be via the effect ofestrogen on glucogenic hormones or lipolytic enzymes. Therefore, the primarypurpose of this review is to explore the effects of estrogen on substrate metabolism.Menstrual cycle physiology and possible mechanisms for the effects of estrogenon metabolism, as well as previous research on estrogen and metabolism in ratsand humans, will be discussed.

LEADING ARTICLE Sports Med 2000 Apr; 29 (4): 221-2270112-1642/00/0004-0221/$20.00/0

© Adis International Limited. All rights reserved.

Some researchers suggest that there is a tendencytoward enhanced fat metabolism in eumenorrhoeicversus amenorrhoeic individuals or in the follicularphase (FP) versus the luteal phase (LP) as a resultof estrogen-mediated fatty acid mobilisation.[1-6]However, a definite role of estrogen in substratemetabolism has not been clearly established. There-fore, the primary purpose of this review is to ex-plore the possible role of estrogen in substrate me-tabolism at rest and during exercise. In order tofully explore this issue, menstrual cycle physiology,menstrual cycle alterations associated with exer-

cise and previous research on the relationship be-tween estrogen andmetabolism in rats and humans,as well as possible mechanisms for the effects ofestrogen on metabolism, will be discussed.

1. Physiology of the Menstrual Cycle

The menstrual cycle can be divided into 3 phases:the FP, the ovulatory phase, and the LP. The FP ischaracterised by the initial development and matura-tion of ovarian follicles. Follicle stimulatinghormone(FSH) and luteinising hormone (LH) are releasedfrom the anterior pituitary under the stimulation of

gonadotropin releasing hormone (GnRH) secretedby the hypothalamus. Initial development of theovarian follicles is dependent on adequate FSH se-cretion, with further growth of the ovarian folliclesdependent upon LH secretion. FSH and LH stimu-late the ovarian follicles to produce estrogen. Asthe ovarian follicles grow and mature, they secretean increased amount of estrogen. In the ovulatoryphase, increased estrogen stimulates a surge in LHand causes the rupture of the ovarian follicles andrelease of the immature ovum. This marks the be-ginning of the LP. Upon release of the ovum, theempty follicle or ‘corpus luteum’continues to secreteestrogen aswell as progesterone. The increased levelsof estrogen and progesterone inhibit the release ofGnRH and result in decreased LH secretion. Re-duced levels of LH lead to the degeneration of thecorpus luteum and the onset of menstrual bleedingas well as a decrease in plasma levels of estrogenand progesterone. Due to the negative feedbackmechanism of the hypothalamic-pituitary-ovarianaxis, decreased blood levels of estrogen and pro-gesterone stimulate GnRH release from the hypo-thalamus, initiating another menstrual cycle.[7,8]

2. Metabolic Effects of Estrogen

While estrogens are considered primarily repro-ductive hormones, it has been postulated that estra-diol may have an effect on resting fat and carbohy-drate metabolism by acting either directly on liver,muscle and/or adipose tissue or indirectly via alter-ations in thermogenic hormones.[9]

2.1 Estrogen and Substrate Metabolism at Rest

Studies examining the relationship between ovar-ian hormones and metabolic processes in humanshave produced conflicting results. The majority ofthese studies have examined the effects of differentphases of the menstrual cycle on fat and carbohy-drate metabolism based on the theoretical estrogenlevel in the LP and FP of the menstrual cycle. Al-though estrogen has wide fluctuations, there is gen-erally an increase in plasma estrogen as well asprogesterone level in the LP.

Most researchers have observed no between-phasedifferences in resting levels of blood glucose,[6,10]plasma lipoproteins,[11] plasma triglycerides[11,12]or blood lactate levels.[6,10,13,14] However, the resultsof Berend et al.[13] provide evidence of a relation-ship between menstrual cycle phase effects on sub-strate metabolism and nutritional status with restinglactate level lower in the LPwith a low-carbohydratediet when compared with any other menstrual phase-diet combination, suggesting a strong dietary effecton substrate metabolism. Hackney[15] performedmuscle biopsies of the vastus lateralis muscle in 10healthy females in the mid-FP and mid-LP and founda greater resting muscle glycogen content in themid-LP, suggesting a glycogen sparing effect dur-ing the LP. Reinke et al.[10] found greater restingblood levels of free fatty acids in the LPwhen com-pared to the FP and ovulatory phase in 10 healthywomen. In addition, while Nicklas et al.[6] observedno between-phase differences in resting levels offree fatty acids in moderately-trained eumenorrhoeicindividuals, the investigators did report a lowerresting respiratory exchange ratio (RER) in the LPthan in the FP (RER = 0.71 ± 0.02 and 0.86 ± 0.04in the LP and FP, respectively).

2.2 Estrogen and Substrate MetabolismDuring Exercise

Studies examining the effects of estrogen onmetabolism during exercise in animals suggest thatestradiol may enhance fatty acid oxidation and util-isation,[2,16] as well as spare hepatic glycogen util-isation.[2] Kendrick et al.[2] found a greater run timeto exhaustion in rats receiving estradiol when com-pared to a control group injected with sesame oil.The results of Hatta and colleagues[16] revealedgreater fatty acid oxidation in rats injected withestrogen during a 60-minute exercise bout and agreater glucose utilisation in rats injected with es-trogen and progesterone in combination.Research examining the effects ofmenstrual cycle

phase on fat and carbohydrate metabolism duringexercise in humans has produced conflicting re-sults. Most researchers examining the menstrualphase effects on lactate production have found a

222 Ashley et al.

© Adis International Limited. All rights reserved. Sports Med 2000 Apr; 29 (4)

greater lactate level during exercise[17] and well aspost-exercise in the FP.[14] In contrast, Bonen etal.[18] observed similar lactate levels in the FP andLPof the menstrual cycle. It seems noteworthy thatthe studies which found a between-phase differencein lactate level used an incremental protocol. Basedon basic principles of substrate utilisation duringexercise, it seems logical that previous exercisebouts might decrease glycogen availability forlater exercise. As intensity and duration of exerciseincrease in incremental exercise, a greater amountof muscle glycogen is utilised and thus a greateramount of lactate is produced.[19] If estrogen doeshave an effect on substrate metabolism, it might bemore pronounced with a greater lactate level.As RER measured via indirect calorimetry is a

relatively easy and widely accepted method to mea-sure substrate metabolism during exercise, manyauthors have examined menstrual cycle phase ef-fects on RER during exercise. Several researchershave observed a greater RER in the FP than in theLP in untrained[20] and trained[1] females duringincremental exercise, suggesting greater fat meta-bolism in the LP. However, in a study comparingsubstrate metabolism during the FP and LP as wellas during ovulation, Hackney and others[21] observeda significantly lower RER at ovulation than duringthe FP (RER = 0.86 ± 0.02 and 0.94 ± 0.02, respec-tively). This suggests that more fat was metabo-lised during ovulation than during the FP.However, several authors have found no signif-

icant menstrual phase effect on fat metabolism dur-ing prolonged submaximal exercise.[22,23] Further,Nicklas et al.[6] observed no between-phase differ-ences in the RER of 6 moderately trained, eumenor-rhoeic individuals during a 90-minute cycling boutat 60%maximal oxygen uptake (V

.O2max) followed

by four 1-minute bouts at 100%V.O2max (DE). Three

days following DE, the volunteers performed anexhaustive exercise (EE) bout, cycling at 70%V.O2max until exhaustion. Although there was a ten-

dency toward greater time to exhaustion in the LPthe difference was not statistically significant.Muscle biopsies of the vastus lateralis taken post-

DE, as well as pre- and post-EE, revealed greatermuscle glycogen repletion following DE in the LP.Most authors studying the effects of menstrual

status on substrate metabolism have observed nodifference in RER between amenorrhoeic and eu-menorrhoeic runners during a prolonged submaxi-mal exercise bout.[22-24] However, Wilmore andcolleagues[24] found a significantly greater RER ineumenorrhoeic than amenorrhoeic runners in thehighest workload of an incremental cycle ergometerbout, and a greater RER in the amenorrhoeic run-ners at the 2 lowest workloads during an incremen-tal treadmill run. It seems noteworthy that the RERof the amenorrhoeic runners during the 2 lowerworkloads of the incremental cycle bout as well asduring the last workload of the treadmill run re-vealed a trend of being greater than that of the eu-menorrhoeic runners.

2.3 Possible Mechanisms for the Effect ofEstrogen on Fat Metabolism

Increased low density lipoproteins (LDL) anddecreased high density lipoproteins (HDL) observedin post-menopausal females are believed to be theresult of decreased estrogen associated with meno-pause,[25,26] while estrogen replacement therapy re-sults in an increase in total HDL, HDL2 and apo-lipoprotein A-I.[25,26] It has also been postulatedthat estrogen administration may aid in the mobil-isation of adipocyte free fatty acids[10,27] as well asincrease plasma triglyceride levels.[25,28] However,in a group of women runners with irregular men-ses, there was no significant correlation betweenestradiol and measured blood lipid parameters,specifically total cholesterol, LDL, HDL or tri-glycerides.[29] The estradiol effects on lipid and li-poprotein levels may be due to estrogen-mediatedinhibition of hepatic lipase (HL) and lipoproteinlipase activity (LPL).[27,30] Hamosh and Hamosh[27]observed a decrease in adipose tissue LPL activityand an increase in plasma triglycerides in male ratsand oovariectomised female rats injected with es-tradiol, with the decrease in LPL directly related tothe dosage of estradiol. HL is an enzyme whichfunctions in the conversion of chylomicrons and

Estrogen and Substrate Metabolism 223


very low density lipoproteins to LDL. Along withcholesteryl ester transfer proteins (enzymes that cata-lyse the transfer of cholesterol), HL participates inthe degradation of HDL, specifically HDL2, by re-moving cholesterol ester from the core of the HDL2molecule.[31] LPL is a lipopytic enzyme that removestriglycerides from chylomicrons and hydrolyses thetriglycerides to provide free fatty acids and glyc-erol for use by tissue cells.It appears that some of the metabolic effects of

estrogen may be indirect through alteration of in-sulin, growth hormone (GH) and the catecholaminesadrenaline (epinephrine) and noradrenaline (nor-epinephrine).[32-35] Estrogen has been proposed tostimulate GH synthesis and decrease secretion ofGH.[5] In addition, estrogen replacement therapybrings about larger GH pulses and higher basal GHlevels in postmenopausal females.[36] GH antagon-ises the effects of insulin, thus hindering uptake ofglucose and increasing mobilisation of adipocytefree fatty acids.[37] There appears to be no between-phase difference in resting levels of GH in healthyfemales,[38] and no difference in GH response toexercise between amenorrhoeic and eumenorrhoeicathletes.[23] Also, Bonen and colleagues[18] observedno between-phase difference in GH response to in-tense exercise in either control or glucose-loadedindividuals. However, there appeared to be greaterincrements in GH during heavy exercise in the LPin a group of fasted volunteers.Estrogen has also been implicated in the inhibi-

tion of catecholamine uptake, primarily affectingadrenaline.[35] However, Chin and colleagues[39] re-ported no difference in resting levels of adrenalineand noradrenaline between individuals of differentmenstrual statuses. All individuals experienced asignificant increase in levels of noradrenaline aftermaximal exercise, with the magnitude of the in-crease directly related to the severity of menstrualdysfunction.Bonen et al.[33] propose that the most significant

effect of estrogen on substrate metabolism is throughestrogen-mediated alterations in insulin action. Inresearch comparing exercise responses of femalestaking oral contraceptives (OC)with those not taking

OC, Bonen et al.,[33] as well as Bemben and col-leagues,[32] found a lower estrogen level accompa-nied by a lower glucose level in individuals takingOC. Further, Bonen et al.[33] observed a greater de-crease in insulin during exercise as well as a lowerpost-exercise insulin level in individuals takingOC. However, Lavoie et al.[28] found no significantdifference in resting insulin levels between the FPand LP in active females.A number of investigators have used the ovari-

ectomised rat injected with varying doses of estro-gen and progesterone to determine their effects onfat and carbohydrate metabolism at rest and duringexercise. Matute and Kalkhoff[5] and Mandour etal.[4] found that estrogen and progesterone in com-bination resulted in an increase in plasma insulinlevels and hepatic glycogen in oovarectomised rats.However, administration of estrogen alone produceda decrease in resting levels of insulin, glucagon andthe gluconeogenic enzyme phosphoenol pyruvatecarboxykinase, and an increase in resting levels ofthe lipogenic enzymes acetyl CoAcarboxylase andfatty acid synthetase.[4] The changes in insulin andglucagon and enzymes suggest an increased hepaticlipogenesis and decreased gluconeogenesis with es-trogen administration. These findings are confirmedby Sladek,[40] who found higher blood glucose andlower serum insulin levels in rats in diestrous, whenestrogen is lowest, than in estrous, proestrous ormetestrous.[41]

3. Conclusions

Estrogen appears to have secondary effects onsubstrate metabolism. While estrogen may affectLPL and HL levels, this probably does not greatlyinfluence fat utilisation during exercise. HL andLPL increase serum triglyceride levels, which arenot a significant source of fatty acids during exer-cise.[42] The effect of estrogen on gluconeogenichormones, specifically by increasing adrenaline andgrowth hormone levels and decreasing insulin levels,would affect fat metabolism. The release of adi-pocyte free fatty acids is controlled by hormone-sensitive lipase. Hormone sensitive lipase is stim-ulated by adrenaline and GH, and inhibited largely

224 Ashley et al.


by insulin. As such, any stimulus which increaseadrenaline and GH (e.g. intense exercise, stress,estrogen) and decreases insulin (exercise, diet, es-trogen) may affect fat metabolism.Many women strive to achieve the ‘ideal body’,

one that is exceedingly lean, primarily by increas-ing physical activity and decreasing caloric intake.The combined effects of intense exercise and calo-ric restriction tend to increase metabolic efficiencyand hindermenstrual function, resulting in decreasedbasal estrogen levels.[43] If estrogen does enhancefat metabolism, a rigorous regimen of increasedenergy expenditure and decreased energy intakemight hinder fat metabolism, leading to more in-tense exercise, greater caloric restriction and lowerbasal estrogen levels. The negative health effectsof low estrogen are well documented and includeosteoperosis, osteopenia and other skeletal prob-lems, as well as increased risk of endometrial andbreast cancer.[44]Determining the relationship between estrogen

and fat metabolism has numerous implications forreducing the risk of chronic diseases. Heart diseaseand stroke are the most common causes of cardio-vascular death for women in the US. Several vari-ables have been identified with increased cardio-vascular risk in females with decreased serum HDLlevels, with hypertriglycerides and diabetes mellitusbeing the most potent cardiovascular risk factors.[45]Determining the relationship between estrogen andmetabolic processes may reduce the risk of severalchronic diseases, specifically coronary artery dis-ease, arteriosclerosis and diabetes mellitus.

4. Future Research

It is a well known axiom that many female ath-letes experience menstrual irregularities and resul-tant lowered estrogen levels. Decreased fatty acidmobilisation, which may be the result of decreasedestrogen, might hinder endurance performance byusing glycogen stores for energy.The role of estrogen in fat metabolism has not

been resolved. There are a number of issues regard-ing the effects of estradiol on metabolic processesthat need investigating before a definite relation-

ship between estradiol and substrate metabolismcan be established. Major issues to be addressedshould include the following:Differences in individual training status. It is

widely accepted that more highly trained femalesusually have lower basal estradiol levels as well asa blunted estradiol response to exercise. Also, theglycogen sparing effect of endurance training is awidely accepted paradigm.[31] It is difficult to sep-arate the effects of enhanced fat utilisation due toaerobic training from the effects of a reduced rest-ing estradiol level due to aerobic training.Hormonal profiles. As repeatedly mentioned,

female athletes may experience ‘normal’menstrualcycles but have altered hypothalamic-pituitary-ovarian hormone profiles. As such, it seems of para-mount importance to fully assess basal hormonelevels as well as hormone response to exercise inexamining the relationship between estradiol andsubstrate metabolism. As ovarian hormone levelsfluctuate widely over the course of the menstrualcycle, hormone levels should be assessed at regularintervals over a period of time to accurately depicthormone fluctuations and menstrual status.Further, a number of variables may affect the

glucoregulatory hormones GH, insulin, adrenalineand noradrenaline, suggested as possible mecha-nisms for estrogen-mediated effects on substrateutilisation. Endurance trained athletes have a lesserGH reponse to exercise than their untrained coun-terparts.[46] Also, secretion of adrenaline and nor-adrenaline is decreased at rest and during exerciseafter aerobic training. Further, insulin effectivenessat rest and during exercise is enhanced with aerobictraining. In addition, nutritional status and mealcomposition have a large effect on insulin levels aswell as insulin response to exercise. As such, allfactors which may affect glucoregulatory as wellas menstrual hormones should be controlled.Nutritional/energy balance status.While estra-

diol may have a secondary effect on substrate meta-bolism, nutritional status is probably the primaryaffector of substrate metabolism. Studies whichtightly control dietary intake of participants through-out the menstrual cycle would provide a better in-



dication of the effect of estradiol on substrate meta-bolism. Assessing long term dietary intake as wellas food intake immediately prior to assessment ofsubstrate metabolism might provide an accuraterepresentation of macronutrient status. In addition,as ‘normal’ patterns of substrate utilisation may bealtered in individuals with a negative energy balance,energy expenditure as well as energy intake shouldbe assessed to determine energy balance status.

References1. Hackney AC, McCracken-Compton MA, Ainsworth B. Sub-

strate responses to submaximal exercise in the midfollicularand midluteal phases of the menstrual cycle. Int J Sport Nutr1994; 4: 299-308

2. Kendrick ZV, Steffen CA, RumseyWL, et al. Effect of estradiolon tissue glycogen metabolism in exercised oopherectomizedrats. J Appl Physiol 1987; 63 (2): 492-6

3. Loucks AB, Mortola JF, Girton L, et al. Alterations in the hypo-thalamic-pituitary-ovarian and the hypotholamic-pituitary-adrenal axes in athletic women. J Clin Endocrinol Metab 1989;68 (2): 402-11

4. Mandour T, Kissebah AH, Wynn V. Mechanism of oestrogenand progesterone effects on lipid and carbohydrate metabolism:Alteration in the insulin: glucagon molar ratio and hepaticenzyme activity. Eur J Clin Invest 1977; 7: 181-7

5. MatuteML, Kalkhoff RK. Sex steroid influence on hepatic gluco-neogenesis and glycogen formation. Endocrinology 1973; 92:762-8

6. Nicklas BJ, Hackney AC, Sharp RL. The menstrual cycle andexercise: performance, muscle glycogen, and substrate re-sponses. Int J Sports Med 1989; 10: 264-9

7. Puhl JL, Brown CH, editors. The menstrual cycle and physicalactivity. Champaign (IL): Human Kinetics, 1986

8. Wells CL, editor. Women, sport and performance: a physiologicalperspective. Champaign (IL): Human Kinetics, 1991

9. Bunt J.Metabolic actions of estradiol: significance for acute andchronic exercise responses. Med Sci Sports Exerc 1990; 22:286-90

10. Reinke U, Ansah B, Voigt KD. Effect of the menstrual cycle oncarbohydrate and lipid metabolism in normal females. ActaEndocrinol 1972; 69: 762-8

11. Lebech AM, Kjer A. Lipid metabolism and coagulation duringthe normal menstrual cycle. HormMetab Res 1989; 21: 445-8

12. Hemer HA, de Bourges VV, Ayala JJ, et al. Variations in serumlipids and lipoproteins throughout the menstrual cycle. FertilSteril 1985; 44: 80-4

13. Berend J, Brammeier M, Jones N, et al. Effect of the menstrualcycle phase and diet on blood lactate responses to exercise.Biol Sport 1994; 11: 241-8

14. McCracken M, Ainsworth B, Hackney A. Effects of the men-strual cycle phase on the blood lactate responses to exercise.Eur J Appl Physiol 1994; 69: 174-5

15. Hackney AC. Effects of the menstrual cycle on resting muscleglycogen content. Horm Metab Res 1990; 22: 647

16. Hatta H, Atomi Y, Shinohara S, et al. The effects of ovarian hor-mones on glucose and fatty acid oxidation during exercise infemale ovariectomized rats. HormMetab Res 1988; 20: 609-11

17. Jurkowski-Hall JE, Jones NL, Toews CJ, et al. Effects of men-strual cycle on blood lactate, O2 delivery, and performanceduring exercise. J Appl Physiol 1981; 51: 1493-9

18. Bonen A, Haynes F, Watson-Wright W, et al. Effects of men-strual cycle onmetabolic responses to exercise. JAppl Physiol1983; 55: 1506-13

19. Coyle EF, Coggan AR, Hemmert MK, et al. Muscle glycogenutilization during prolonged strenuous exercise when fed carbo-hydrate. J Appl Physiol 1986; 61: 165-72

20. Dombovy ML, Bonekat HW, Williams TJ, et al. Exercise per-formance and ventilatory response in the menstrual cycle. MedSci Sports Exerc 1987; 19: 111-7

21. Hackney AC, Curley CS, Nicklas BJ. Physiological responsesto submaximal exercise at the mid-follicular, ovulatory andmid-luteal phases of the menstrual cycle. Scand J Med SciSports 1991; 1: 94-8

22. DeSouza MJ, Maguire MS, Rubin KR, et al. Effects of menstrualphase and amenorrhea on exercise performance in runners.Med Sci Sports Exerc 1990; 22: 575-80

23. Kanaley JA, Boileau RA, Bahr JA, et al. Substrate oxidationand GH responses to exercise are independent of menstrualphase and status. Med Sci Sports Exerc 1992; 24: 873-80

24. Wilmore JH, Wambsgans KC, Brenner M, et al. Is there energyconservation in amenorrheic compared with eumenorrheicrunners? J Appl Physiol 1992; 72 (1): 15-22

25. Lamon-Fava S, Fisher EC, Nelson ME, et al. Effect of exerciseand menstrual cycle status on plasma lipids, low density lipo-protein particle size, and apolipoproteins. J Clin EndocrinolMetab 1989; 68 (1): 17-21

26. Schaefer EJ, Foster DM, Zech LA, et al. The effects of estrogenadministration on plasma lipoproteinmetabolism in premeno-pausal females. J Clin Endocrin Metab 1983; 57 (2): 262-7

27. Hamosh M, Hamosh P. The effect of estrogen on the lipoproteinlipase activity of rat adipose tissue. J Clin Invest 1975; 55:1132-5

28. Lavoie JM, Dionne N, Helie R, et al. Menstrual cycle phasedissociation of blood glucose homeostasis during exercise. JAppl Physiol 1987; 62 (3): 1084-9

29. Thompson DL, Snead DB, Seip RL, et al. Serum lipid levelsand steroidal hormones in women runners with irregular men-ses. Can J Appl Physiol 1997; 22: 66-77

30. Schaefer EJ, Lamon-Fava S, Spiegelman D, et al. Changes inplasma lipoprotein concentrations and composition in responseto a low-fat, high-fiber diet are associated with changes inserum estrogen concentrations in premenopausal women. Me-tabolism 1995; 44: 749-56

31. Durstine JL, Haskell WL. Effects of exercise training on plasmalipids and lipoproteins. Exerc Sport Sci Rev 1994; 22: 477-521

32. Bemben D, Bolilea R, Bahr J, et al. Effects of oral contraceptiveson hormonal and metabolic responses during exercise. MedSci Sports Exerc 1992; 24: 434-41

33. Bonen A, Haynes F, Graham T. Substrate and hormonal responsesto exercise in women using oral contraceptives. J Appl Physiol1991; 70: 1917-27

34. Briggs M, Briggs M. Oral contraception. Montreal (QC): EdenPress, 1977

35. Heritage AS, Stumpf WE, Sar M, et al. Brainstem catecholamineneurons are target sites for sex steroid hormones. Science 1980;207: 1377-9

36. Friend KE, Hartman ML, Pezzoli SS, et al. Both oral and trans-dermal estrogen increase growth hormone release in post-menopausal women: a clinical research center study. J ClinEndocrinol Metab 1996; 81: 2250-6

226 Ashley et al.


37. Kahn CR, Goldfine ED, Neville DM, et al. Alterations in insulinbinding induced by changes in vivo in the levels of gluco-corticoids and GH. Endocrinology 1978; 103: 1054-66

38. Heiling VJ, Jensen MD. Free fatty acid metabolism in the fol-licular and luteal phases of the menstrual cycle. J Clin En-docrinol Metab 1992; 74: 806-10

39. Chin NW, Frank MD, DoddsWG, et al. Acute effects of exerciseon plasma catecholamines in sedentary and athletic womenwith normal and abnormalmenses. Am J Obstet Gynecol 1987;157: 938-44

40. Sladek C. Gluconeogenesis and hepatic glycogen formation in re-lation to the rat estrous cycle. HormMetab Res 1974; 6: 217-21

41. Brinkley HJ. Endocrine signaling and female reproduction. BiolReprod 1981; 24: 22-43

42. Tate C, Holtz RW. Gender and fat metabolism. Can J ApplPhysiol 1998; 23: 570-82

43. Pirke KM, Schweiger U, Lemmel W, et al. The influence ofdieting on the menstrual cycle of healthy young women. JClin Endocrinol Metab 1985; 60: 1174-9

44. Brownell KD, Rodin J,Wilmore JH, editors. Eating, bodyweight,and performance in athletes. Philadelphia (PA): Lea & Febiger,1992

45. Klimis-Tavantzis DJ, Wolinsky I. Nutrition, cardiovascular dis-ease, and women. In: Klimis-Tavantzis DJ, Wolinsky I, editors.Nutritional concerns ofwomen. Boca Raton (FL): CRCPress,1996: 135-50

46. Sutton JR. Hormonal and metabolic responses to exercise insubjects of high and low work capacities. Med Sci SportsExerc 1978; 10: 1-11

Correspondence and offprints: Candi D. Ashley, School ofPhysical Education, Wellness, and Sports Studies, Univer-sity of South Florida, 4202 E. Fowler Ave, PED 214, Tampa,Florida 33620-8600, USA.



Estrogen and Substrate Metabolism

Documents

Transcript of Estrogen and Substrate Metabolism