Cls432.dvi

Clinical Science (2003) 105, 663–669 (Printed in Great Britain)
concentration of bioavailable 17-β oestradiol
K. J. ELLIOTT∗, N. T. CABLE†, T. REILLY† and M. J. DIVER‡
∗Department of Sport and Exercise Sciences, University of Brighton, Eastbourne BN20 7SP, U.K., †Research Institute for Sportand Exercise Sciences, Liverpool John Moores University, Liverpool L3 2ET, U.K., and ‡Department of Clinical Chemistry,University of Liverpool, Liverpool L7 8XP, U.K.
To investigate the effect of changes in sex hormone concentration on muscle strength and thebioavailability of 17-β oestradiol (oestradiol) and testosterone, seven eumenorrheic females weretested during two phases of the menstrual cycle. Maximum voluntary isometric strength of the firstdorsal interosseus muscle was measured during the early follicular and mid-luteal phases of themenstrual cycle. These phases were chosen for testing as the concentration of total oestradiolis significantly different in these two phases. Total oestradiol has been repeatedly associated withchanges in muscle strength in females, whereas the effects of bioavailable oestradiol are unknown.
The concentrations of total and bioavailable oestradiol and testosterone were measured in additionto the concentration of total progesterone. Concentrations of total progesterone and oestradiolwere significantly different between the early follicular and mid-luteal phases of the menstrualcycle (P < 0.05 and P < 0.001 respectively). The concentration of total testosterone (0.7 + − 0.1 nmol · l−1 respectively) and the ratio of total oestradiol to progesterone (153.0 + − 27.8 respectively) did not change significantly between the early follicular and mid- luteal phases. Bioavailable testosterone (102.2 + − 60.6 pmol · l−1 respectively) did not differ significantly between phases. There were no significant differences in muscle strength duringthe menstrual cycle (P = 0.1). Mean maximum voluntary isometric force of the first dorsalinterosseus muscle did not correlate significantly with the mean concentration of any reproductivehormone measured. These results indicate that cyclical variation in endogenous reproductive hor-mones does not affect muscle strength.
INTRODUCTION
reproductive hormones on muscle function in femaleshave been widely debated. Various indices of muscle Research into muscle periodicity as a result of menstrual strength have been shown to increase, decrease or remain cycle phase has been ongoing since 1876 when a Harvard unchanged at different phases of the menstrual cycle [3– student first noted cyclical changes in muscle strength [1].
8]. These ambiguous results may be due to conflicting Moore and Barker [2] extended this work by making daily definitions of ‘reproductive status’ [3,4] and ‘strength’ observations on muscle efficiency in 19 women across 12 [2,9], inaccurate identification of menstrual cycle phase self-reported monthly cycles. Since then, the effects of [5,10], different modalities of strength assessment [8,11], Key words: first dorsal muscle, 17-β oestradiol, maximum voluntary isometric force, menstrual cycle, muscle strength, testosterone.
Abbreviations: EF, early follicular; FDI, first dorsal interosseus; ML, mid-luteal; MVIF, maximum voluntary isometric force; SHBG,
sex hormone binding globulin.
Correspondence: Dr Kirsty Elliott (e-mail k.j.elliott@brighton.ac.uk).
examination of dissimilar muscle groups [6,7] and early follicular (EF) and mid-luteal (ML) phases of recruitment of non-homogenous groups of subjects [12].
the menstrual cycle] have the potential to change the In addition, large inter- and intra-individual variability in equilibrium between free, albumin- and SHBG-bound hormone secretion [8] undermines studies using the oestradiol and testosterone and, consequently, the con- centration of bioavailable oestradiol and testosterone.
Recently, Janse de Jonge et al. [8] addressed some of If the concentration of bioavailable oestradiol and these problems by measuring the concentration of total testosterone changes significantly during the menstrual oestrogen, progesterone, luteinizing hormone and follicle cycle, then this may account for the fluctuations in muscle stimulating hormone and muscle strength, in conjunction strength observed previously [4,5]. The mechanisms with percutaneous electrical stimulation, throughout the behind any possible effects are unknown as, to date, menstrual cycle. They found that maximum isometric no mechanistic work has been performed. Phillips strength and fatigability of the quadriceps muscles did not et al. [4] proposed that the effects of oestrogen on muscle change between the menstrual, late follicular and luteal strength are mediated by the classical steroid receptor phases of the menstrual cycle, despite significant changes for oestrogen, whereas Sarwar et al. [5] suggested that the membrane receptor model probably controls the action of Vermeulen et al. [13] suggested that (in plasma) the oestrogen. Sarwar et al. [5] also proposed that changes in bioavailable fraction, rather than the total concentration the activity of myosin ATPase or the re-uptake of calcium of testosterone, is a more accurate representation of the by the sarcoplasmic reticulum might be responsible for clinical situation. Testosterone is bound specifically to sex hormone binding globulin (SHBG) (66 %) and non- As previous studies have exclusively reported the con- specifically to albumin (30 %), such that only 1–3 % centration of total oestradiol [4,8], the objective of the circulates freely [14]. As testosterone has a low affinity present study was to examine the effects of menstrual with, and is easily dissociated from, albumin, both cycle phase on the bioavailability of oestradiol and the albumin-bound and free portion can be considered testosterone. In addition, this study was designed to ‘bioavailable’ [15]. Further evidence to support this investigate the possible influence of cyclical changes in hypothesis is provided by Van den Beld et al. [16], bioavailable oestradiol and testosterone on maximum who found that albumin-bound testosterone has access voluntary isometric force (MVIF) of the first dorsal inter- to target tissues. As both testosterone and 17-β osseus (FDI) muscle under more rigorous test conditions oestradiol (oestradiol) have a hydroxy group bound to than have been used previously. We hypothesize that, if position C-17, the same biochemical principles apply after all of the aforementioned methodological flaws are overcome, any changes in maximum force production The bioavailable part of oestradiol and testosterone that are observed will coincide with changes in the is not a set proportion of the total concentration. The concentration of bioavailable oestradiol and testosterone.
amount of steroid carried by a particular binding protein EF and ML phases of the menstrual cycle were chosen for depends not only on its affinity for the protein, but also on testing, because the concentration of total oestradiol is its concentration. First, testosterone and oestradiol have low and high respectively, at these times and oestradiol higher affinities with SHBG than albumin; therefore the is the hormone most implicated in strength regulation concentration of free hormone in equilibrium with [4,5,11,18]. Testosterone was measured in the present the albumin-bound hormone will always be smaller.
study as (i) few investigators have examined the effects of Secondly, SHBG becomes saturated with testosterone cyclical changes in testosterone concentration on muscle and oestradiol more easily than albumin, such that strength in females, and (ii) testosterone secretion is large quantities of testosterone and oestradiol should indirectly influenced by oestrogen concentration [19].
result in an increase in the amount of bioavailable The bioavailability of progesterone was not measured as hormone. However, the concentration of SHBG in progesterone is also bound to cortisol-binding hormone humans is not constant. Oestrogen administration and and, to date, cannot be separated into its bioavailable and the thyroid hormones increase SHBG levels, whereas bound portions. Consequently, the concentration of total androgen administration and growth hormone decrease progesterone was measured and reported.
the concentration of SHBG. Gower and Nyman [17]found that oestrogen replacement therapy increasedSHBG levels (due to the first-pass effect, the liver is exposed to supraphysiological concentrations of oes-tradiol) and consequently decreased the amount of Subjects
bioavailable testosterone in postmenopausal women.
Seven healthy female subjects, with mean ( + Therefore, in theory, the hormonal changes that occur during the menstrual cycle [e.g. the concentration of total oestradiol increases significantly between the from the local University. All subjects reported normal Muscle strength and menstrual cycle phase Intra- and inter-assay reproducibility for each hormone
Values are expressed as a percentage coefficient of variation and are from four samples. Coefficient of variation was calculated by dividing the S.D. of the differencesbetween the two tests by the mean of the two tests and multiplying by 100. hCG, human chorionic gonadotropin.
menstrual cycle function, with mean cycle lengths the method of Tremblay and Dube [26]. Intra- (30 times − 1 days. Subjects had not been taking oral in the same run) and inter- (29 different series) assay contraceptives or any other hormonal treatments for reproducibility was determined for each hormone using at least 6 months prior to testing. Only non-smokers were included in the study [20]. Subjects with anymuscular, neurological or skeletal disorders capable ofinfluencing performance of the hand were excluded.
Assessment of MVIF of the FDI muscle
Approval for the experimental protocol was obtained The FDI muscle was chosen for testing for two reasons.
from the institutions Human Ethics Committee and First, the FDI muscle is the only muscle that produces conformed to the Declaration of Helsinki. All subjects abduction of the index finger. Other muscles attached to provided written consent having read and understood the finger are active during abduction but, due to their anatomical arrangement, they do not contribute force inthis direction [27]. Rutherford and Jones [28] found very Experimental design
similar maximum voluntary and stimulated contractionforces for the FDI muscle, therefore demonstrating that All subjects reported to the laboratory in a ‘normal’ the FDI muscle can be maximally activated and isolated fed state, having abstained from alcohol and caffeine from the action of other hand muscles. Secondly, these consumption and any strenuous physical exercise for [28] and other [29] authors have found no difference in 24 h, due to known effects on muscle strength and re- force production between dominant and non-dominant productive hormone concentration [21–24]. A 10 ml ve- hands, suggesting that this muscle is not trainable under nous blood sample was drawn from each subject prior to any physical testing. All testing was undertaken at Prior to assessing the MVIF of the FDI muscle, the the same time of day in order to control for circadian hand and forearm were heated for 10 min to a skin temperature of 40 ◦C using a hotpack (Dreamland Electric Prior to experimentation, subjects were familiarized, Heat Pad; Dreamland Appliances Ltd, Oldham, Lancs., on two occasions, with the experimental environment U.K.). The muscle was warmed due to known effects of and procedures. Following familiarization, subjects were pre-exercise muscle temperature on muscle performance tested on two occasions, day 2 and 21 of the cycle. Day 2 [30]. A reading lamp (60 W bulb) was positioned at a (EF phase) was the day after the onset of menses and standard distance over the muscle throughout the test day 21 (ML phase) was 7 days after ovulation had session in order to maintain skin temperature.
occurred. Ovulation was determined using 1 month of A custom-built finger dynamometer [31] was used to oral temperature measurement (MC 63B; Omron, Vernon assess MVIF of the FDI muscle. The test re-test ratio Hills, IL, U.S.A.) and a urinary luteinizing hormone kit limits of agreement for assessment of MVIF of the FDI (Clearplan, Bedford, U.K.). Subjects (and hence phases) muscle using this equipment is 1.2. Based on a 20 % were tested in random order. MVIF of the FDI muscle error, the nomogram of Atkinson et al. [32] indicates that a sample size of seven is adequate to detect at leasta 10 % change {Phillips et al. [4] found a significant Hormonal analysis
change (10 %) in MVIF of the adductor pollicis muscle} Plasma concentrations of total oestradiol, progesterone in maximum force as a result of changes in reproductive and testosterone were measured using an automated quantitative system (Mini Vidas; bioMerieux, Lyon, The dominant arm was placed in a prone position on France). All samples were analysed using the enzyme- the finger dynamometer. The forearm was secured to the linked fluorescent assay technique, an enzyme im- diagonal slope of the platform, at the wrist, mid-forearm munoassay sandwich method with a final fluorescent and distal portion of the elbow joint, with Velcro straps.
detection. The concentration of bioavailable oestradiol The lateral side of the distal head of the proximal phalanx and testosterone was measured using an adaptation of of the index finger was aligned with the force transducer, which was attached to a strain gauge (Model UL4000; Mean MVIF of the FDI muscle correlated with
Maywood Instruments Ltd, Tilehurst, Berks., U.K.). The the mean concentration of bioavailable oestradiol and
strain gauge was calibrated with known weights prior to testosterone, total oestradiol, testosterone, progesterone,
testing. The thumb was secured, with a strap around the and the ratio of oestradiol to progesterone
shaft of the first phalanx, in a fully abducted position.
The remaining fingers were covered in bubble-wrap andrestrained using a Velcro strap. An adjustable clamp, tightened to the shaft of the second metacarpal, prevented upward movement of the index finger. Hand position was standardized for each test session. MVIF of the FDI muscle was measured while the index finger was fully abducted. Three sub-maximum isometric contractions Force and the ratio of oestradiol to progesterone were carried out prior to maximum force assessment.
Following a rest of 3 min, three maximum voluntaryisometric contractions were performed, the best of whichwas taken as definitive. A rest of 1 min separated each Percutaneous electrical stimulation was used to Total concentrations
superimpose electrical impulses on to the FDI muscle during each contraction. Two self-adhesive surface 28.3 nmol · l−1 in EF and ML phases respectively; electrodes (3S; Healthcare, London, U.K.) delivered P < 0.05) and oestradiol (110.8 + 1 Hz twitches, at a tolerable current, throughout the 83.5 pmol · l−1 in EF and ML phases respectively; test. Individual tolerable currents were established prior P < 0.001) were significantly different between phases.
to assessment of maximum isometric force. The anode was placed directly proximal to the head of the second 0.1 nmol · l−1 in EF and ML phases respectively) and metacarpal and the cathode medially to the head of the ratio of oestradiol to progesterone (153.0 + the first metacarpal. Electrical impulses were applied, − 27.8 in EF and ML phases respectively) did using a computer-driven Digitimer Stimulator (Model not change between the phases of the menstrual cycle.
DS7; Digitimer Ltd, Welwyn Garden City, Herts.,U.K.), at 150 V with a pulse width of 100 µs duration.
Force output was amplified and displayed visually on Bioavailable concentrations
an Apple Macintosh computer interfaced with a data There were no significant differences in the con- acquisition system (MP100WS; Biopac Systems, Goleta, centration of bioavailable testosterone (102.2 + CA, U.S.A.). Maximum activation was confirmed when − 90.2 pmol · l−1 in EF and ML phases no extra force could be generated by the superimposed pmol · l−1 in EF and ML phases respectively) between thetwo phases of the menstrual cycle.
Statistical analysis
Muscle strength
There were no significant differences in MVIF of the Windows (Version 13; Minitab Inc., State College, PA, FDI muscle between the EF and ML phases of the men- U.S.A.) was used for data analysis. Verification that strual cycle (P = 0.1). Mean strength was 28.2 + data were normally distributed was provided by the Anderson–Darling normality test. The level of signific- phase. Mean MVIF did not significantly correlate with the ance was taken as P < 0.05. A two-sample-dependent mean concentration of any of the reproductive hormones Student’s t test was used to detect significant differences (either bioavailable or total concentration) measured in MVIF of the FDI muscle and concentrations of progesterone (total), oestradiol (total and bioavailable),testosterone (total and bioavailable) and the ratio of totaloestradiol to progesterone between the EF and ML phases DISCUSSION
of the menstrual cycle. The relationship between MVIF ofthe FDI muscle and reproductive hormone status was Investigators are not in agreement on either the quanti- examined using Pearson’s correlation coefficient on tative or directional effects of menstrual cycle phase on normally distributed data, and Spearman’s rank cor- strength [3,33,34]. In the present study, muscle strength relation on non-parametric data. Prior to correlation, all was measured under strict test conditions and did not data were averaged so that time was factored out.
differ across the menstrual cycle, despite significant Muscle strength and menstrual cycle phase changes in the concentration of total oestradiol and of oestradiol did not change significantly throughout progesterone. In addition, muscle strength was not the menstrual cycle. This might suggest that cyclical significantly correlated with any of the reproductive changes in the total concentration of oestradiol are hormones measured. Janse de Jonge et al. [8] also found no (i) not sufficient to saturate the concentration of influence of menstrual cycle phase on muscle contractile circulating SHBG and hence increase the concentration properties using a similar research design, measuring of free and albumin-bound oestradiol (i.e. bioavailable MVIF of the quadriceps muscles and the concentration of oestradiol) or (ii) sufficient to cause an increase in the reproductive hormones. These results are consistent with concentration of circulating SHBG, resulting in an in- earlier work by Higgs and Robertson [10], who failed crease in the amount of unavailable (or bound) to detect any significant differences in handgrip strength oestradiol. Future research may benefit from measuring the concentration of circulating SHBG. No significant The present findings do not agree with previous differences in testosterone status (either total or studies, which have implicated oestrogen and proges- bioavailable) were noted between the EF and ML terone in strength regulation [4,5]. Phillips et al. [4] phases. Given that muscle strength and the bioavailable demonstrated a 10 % increase in MVIF of the adductor concentration of oestradiol and testosterone remained pollicis muscle during the follicular phase (days 1–14) unchanged, the possibility that muscle strength could of the menstrual cycle. This was followed by a similar indeed be affected by changes in the bioavailability of drop in strength at the onset of ovulation. Although oestradiol and testosterone cannot be dismissed. A model Phillips et al. [4] did not find a significant relationship that manipulates bioavailability of these hormones might between strength and oestrogen status, they suggested be used to examine this question. In particular, a model that changes in muscle strength across the menstrual cycle that significantly changes the concentration of both total were related to, or caused by, fluctuations in oestrogen.
and bioavailable testosterone is warranted, so that the However, if oestrogen was the hormone responsible independent effects of testosterone on the maximum for cyclical changes in muscle strength, then the largest force-generating capacity of females can be investigated.
strength differences should occur between the ovulatory Bioavailable oestradiol and testosterone have been and follicular phases in which the highest and lowest shown to change as a function of age in men. Van den Beld concentrations of oestrogen are observed respectively.
et al. [16] measured free, albumin-bound, SHBG-bound Indeed, Sarwar et al. [5] found that the greatest dif- and total oestradiol and testosterone levels in elderly men ferences in strength occurred between the ovulatory (> 70 years). They found that bioavailable testosterone (high oestrogen levels) and luteal (high oestrogen and levels decreased with advancing age, whereas the progesterone levels) phases. They suggested that pro- concentration of SHBG-bound testosterone increased.
gesterone might inhibit oestrogen’s inotropic effect or Conversely, total testosterone did not change as a act directly on the muscle to weaken it. However, function of age. Total and bioavailable oestradiol de- this hypothesis is contradicted by the observation that, creased and SHBG-bound oestradiol increased with despite low progesterone levels, post-menopausal skeletal age. In addition, Van den Beld et al. [16] found that muscle is weak for its size [35]. Furthermore Greeves bioavailable testosterone, but not bioavailable oestradiol, et al. [31] reported that maximum muscle strength and was positively related to muscle strength in men. The fatigue did not change when progesterone levels were concentration of total, but not bioavailable, testosterone suppressed and the concentration of oestradiol was has been shown to increase with age in women [36], but raised from hypo- to hyper-oestrogenic levels. Based muscle strength was not assessed in this study.
on this evidence, it is unlikely that either oestrogen or Previous studies that have measured the concentration progesterone significantly affects muscle function.
of free oestradiol and testosterone during the menstrual To the best of our knowledge, this is the first cycle have yielded conflicting results. Wu et al. [37] found investigation of the effects of menstrual cycle phase on that free oestradiol remained constant throughout the the bioavailability of oestradiol and testosterone and cycle. Conversely, Stahl et al. [38] reported significant their effect on muscle strength in females. As stated increases in free testosterone (mid-cycle) and oestradiol previously, the bioavailable fraction of a hormone is (two peaks), even though SHBG levels did not change.
not a set proportion of the total concentration. The Mathor et al. [39] found, using equilibrium dialysis concentration of bioavailable oestradiol and testosterone of undiluted plasma, that the concentration of free largely depends on the amount of circulating SHBG, testosterone increased from the follicular to the luteal which is affected by the concentration of thyroid, phase of the menstrual cycle. In contrast, Schijf et al. [40] growth, oestrogenic and androgenic hormones and the showed that the free androgen index decreased during concentration of total oestradiol and testosterone. In the luteal phase, due to a significant increase in the the present study, the total concentration of oestradiol concentration of SHBG during this phase.
increased significantly between the EF and ML phases In the present study, a large variation (as reflected of the menstrual cycle. However, the bioavailability by the S.D. values) in the concentration of reproductive hormones was noted. In particular, bioavailable testoster- 11 Wirth, J. C. and Lohman, T. G. (1982) The relationship of one ranged from 169 to 103 and 195 to 15 pmol · l−1 static muscle function to use of oral contraceptives.
Med. Sci. Sports Exercise 14, 16–20
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may have masked any potential inotropic effects of 13 Vermeulen, A., Verdonck, L. and Kaufman, J. M. (1999) reproductive hormones on muscle strength.
A critical evaluation of simple methods for the estimation In conclusion, when measured under strict test of free testosterone in serum. J. Clin. Endocrinol. Metab.
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Received 13 December 2002/9 May 2003; accepted 9 July 2003Published as Immediate Publication 9 July 2003, DOI 10.1042/CS20020360

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