Accessibility / Report Error

The relationship between oestrogen and muscle strength: a current perspective

Abstract

The relationship between muscle strength and oestrogen is ambiguous and is still largely unresolved. The evidence for and against an effect of oestradiol on determinants of muscle function is equivocal and often contradictory. The bulk of the research in this area was performed during the eighties and nineties, using models of reproductive functioning such as; the menstrual cycle, the menopause and hormone replacement therapy, oral contraceptives and in vitro fertilisation treatment, to alter the female hormonal milieu. In the last decade, approximately 15 papers have demonstrated a relationship, both positive and negative, between the concentration of oestrogen and skeletal muscle strength. Conversely, around 20 articles have not shown any influence of oestrogen on a number of strength measures. The majority of these studies were performed using post-menopausal and eumenorrheic females. Most current studies use hormonal assays to confirm oestrogen status, however no recent studies have reported the bioavailable concentration of oestradiol. Similarly, no research in the last 10 years has used in vitro fertilisation treatment or pregnancy as acute and chronic models of supra-physiological changes in sex hormone concentration. Future work should focus on performing meta-analyses on each of the key components of muscle strength in an attempt to elucidate a causal relationship. In addition, models of reproductive functioning that cause the greatest magnitude of change to oestrogen concentration should be used, while controlling as many confounding factors as possible.

Oestradiol; Reproductive hormones; Muscular system; Females; Performance


Introduction

During the eighties and nineties there was much debate and controversy about the effects of ovarian hormones on muscle strength in females1. Higgs SL, Robertson LA. Cyclic variations in perceived exertion and physical work capacity in females. Can J Appl Sport Sci. 1981;6:191-6.

. Cauley JA, Petrini AM, LaPorte RE, et al. The decline in grip strength in the menopause: relationship to physical activity, estrogen use and anthropometric factors. J Chronic Dis. 1987;40:115-20.

. Davies BN, Elford JCC, Jamieson KF. Variations in performance in simple muscle tests at different phases of the menstrual cycle. J Sports Med Phys Fitness. 1991;31:532-7.

. Phillips SK, Sanderson AG, Birch K, Bruce SA, Woledge RC. Changes in maximal voluntary force of human adductor pollicis muscle during the menstrual cycle. J Physiol. 1996;496:551-7.
-5. White MJ, Weeks C. No evidence for a change in the voluntary or electrically evoked contractile characteristics of the triceps surae during the human menstrual cycle. J Physiol. 1998;506:119.. Researchers used various models of reproductive functioning to investigate this relationship including; the menstrual cycle6. Bassey EJ, Coates L, Culpen J, Littlewood JJ, Owen M, Wilson K. Natural variations in oestrogen and FSH levels in eumenorrheic women in negative association with voluntary muscle strength. J Physiol. 1995;489:45., the menopause7. Armstrong AL, Oborne J, Coupland CAC, MacPearson MB, Bassey EL, Wallace WA. Effects of hormone replacement therapy on muscle performance and balance in postmenopausal women. Clin Sci (Lond). 1996;91:685-90., in vitro fertilisation (IVF) treatment8. Greeves JP, Cable NT, Luckas MJM, Reilly T, Biljan MM. Effects of acute changes in oestrogen on muscle function of the first dorsal interosseus muscle in humans. J Physiol. 1997;500:265-70., pregnancy9. Elliott KJ, Cable NT, Reilly T, Sefton V, Kingsland C, Diver M. Effects of supra-physiological changes in human ovarian hormone levels on maximum force production of the first dorsal interosseus muscle. Exp Physiol. 2005;90:215-23., oral contraceptives1010 . Sarwar, R, Niclos BB, Rutherford OM. Changes in muscle strength, relaxation rate and fatigability during the human menstrual cycle. J Physiol. 1996;493:267-72. (OC’s) and hormone replacement therapies1111 . Skelton DA, Phillips SK, Bruce SA, Naylor CH, Woledge RC. Hormone replacement therapy increases isometric muscle strength of adductor pollicis in post-menopausal women. Clin Sci (Lond). 1999;96:357-64. (HRT’s). Since then, numerous review papers1212 . Cable NT, Elliott KJ. The influence of reproductive hormones on muscle strength. Biol Rhythm Res. 2004;35:235-44.

13 . Burrows M, Peters CE. The influence of oral contraceptives on athletic performance in female athletes. Sports Med. 2007;37:557-74.
-1414 . Rechichi C, Dawson B, Goodman C. Athletic performance and the oral contraceptive. Int J Sports Physiol Perform. 2009;4:151-62. have been published, yet the number of original research outputs has declined. To date, there is still no consensus regarding the role of oestrogen in force production or universal guidelines for advising females about reproductive status and skeletal muscle function. This review will consider data from the last ten years examining the relationship between oestrogen and muscle strength. It is important to study this relationship as the female hormonal milieu changes across the lifespan and muscle strength is an enabling factor which facilitates functional independence and athletic performance.

Interestingly, the association between sex hormones and the muscular system was first noted almost 100 years before the majority of research in this field was conducted: JACOBI1515 . Jacobi MP. The question of rest for women during menstruation. New York: G.P. Putnam’s sons; 1877. observed periodic changes in muscle strength during the menstrual cycle. Since then, several authors have linked cyclical changes in muscle strength, in eumenorrheic females, with fluctuations in ovarian hormone levels across the menstrual cycle3. Davies BN, Elford JCC, Jamieson KF. Variations in performance in simple muscle tests at different phases of the menstrual cycle. J Sports Med Phys Fitness. 1991;31:532-7.,4. Phillips SK, Sanderson AG, Birch K, Bruce SA, Woledge RC. Changes in maximal voluntary force of human adductor pollicis muscle during the menstrual cycle. J Physiol. 1996;496:551-7.,1010 . Sarwar, R, Niclos BB, Rutherford OM. Changes in muscle strength, relaxation rate and fatigability during the human menstrual cycle. J Physiol. 1996;493:267-72.,1616 . Wirth JC, Lohman TG. The relationship of static muscle function to use of oral contraceptives. Med Sci Sports Exerc. 1982;14:16-20.-1717 . Beltran Niclos B, Welsh L, Sarwar R, Rutherford OM. Gender and age comparisons of the contractile properties of human quadriceps muscle. J Physiol. 1995;483:131.. However, there is also substantial evidence to the contrary1. Higgs SL, Robertson LA. Cyclic variations in perceived exertion and physical work capacity in females. Can J Appl Sport Sci. 1981;6:191-6.,5. White MJ, Weeks C. No evidence for a change in the voluntary or electrically evoked contractile characteristics of the triceps surae during the human menstrual cycle. J Physiol. 1998;506:119.,1818 . Dibrezzo R, Fort IL, Brown B. Relationship among strength, endurance, weight and body fat during three phases of the menstrual cycle. J Sports Med Phys Fitness. 1991;31:89-94.

19 . Lebrun CM, McKenzie DC, Prior JC, Taunton JE. Effects of menstrual cycle phase on athletic performance. Med Sci Sports Exerc. 1995;27:437-44.
-2020 . Gur H. Concentric and eccentric isokinetic measurements in knee muscles during the menstrual cycle: a special reference to reciprocal moment ratios. Arch Phys Med Rehabil. 1997;78:501-5.. During the same period, numerous authors have reported a notable reduction in strength at the onset on the menopause that can be preserved by HRT1111 . Skelton DA, Phillips SK, Bruce SA, Naylor CH, Woledge RC. Hormone replacement therapy increases isometric muscle strength of adductor pollicis in post-menopausal women. Clin Sci (Lond). 1999;96:357-64.,2121 . Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC. Muscle weakness in women occurs at an earlier age than in men, but is preserved by hormone replacement therapy. Clin Sci (Lond). 1993;84:95-8.

22 . Calmels P, Vico L, Alexandre C, Minaire P. Cross-sectional study of muscle strength and bone mineral density in a population of 106 women between the ages of 44 and 87 years: relationship with age and menopause. Eur J Appl Physiol Occup Physiol. 1995;70:180-6.
-2323 . Greeves JP, Cable NT, Reilly T, Kingsland C. Changes in muscle strength in women following the menopause: a longitudinal assessment of the efficacy of hormone replacement therapy. Clin Sci (Lond). 1999;97:79-84.. In contrast, a similar number of reports have contradicted this evidence and have shown no relationship2. Cauley JA, Petrini AM, LaPorte RE, et al. The decline in grip strength in the menopause: relationship to physical activity, estrogen use and anthropometric factors. J Chronic Dis. 1987;40:115-20.,7. Armstrong AL, Oborne J, Coupland CAC, MacPearson MB, Bassey EL, Wallace WA. Effects of hormone replacement therapy on muscle performance and balance in postmenopausal women. Clin Sci (Lond). 1996;91:685-90.,2424 . Taaffe DR, Villa ML, Delay R, Marcus R. Maximal muscle strength of elderly women is not influenced by oestrogen status. Age Ageing. 1995;24:329-33.-2525 . Bassey EJ, Mockett SP, Fentem PH. Lack of variation in muscle strength with menstrual status in healthy women aged 45-54 years: data from a national survey. Eur J Appl Physiol Occup Physiol. 1996;73:382-6.. The influence of OC’s on muscle function is also confusing with some authors1616 . Wirth JC, Lohman TG. The relationship of static muscle function to use of oral contraceptives. Med Sci Sports Exerc. 1982;14:16-20.,2626 . Thompson HS, Hyatt JP, De Souza MJ, Clarkson PM. The effects of oral contraceptives on delayed onset muscle soreness following exercise. Contraception. 1997;56:59-65. suggesting an effect and others showing no difference4. Phillips SK, Sanderson AG, Birch K, Bruce SA, Woledge RC. Changes in maximal voluntary force of human adductor pollicis muscle during the menstrual cycle. J Physiol. 1996;496:551-7.,1010 . Sarwar, R, Niclos BB, Rutherford OM. Changes in muscle strength, relaxation rate and fatigability during the human menstrual cycle. J Physiol. 1996;493:267-72.. For a comprehensive review of the literature published between 1980 and 2000 see CABLE and ELLIOTT1212 . Cable NT, Elliott KJ. The influence of reproductive hormones on muscle strength. Biol Rhythm Res. 2004;35:235-44..

Data from this era was impaired by a variety of design issues such as; inconsistent terminologies (e.g. menstrual cycle phase and postmenopausal status), inaccurate methods (e.g. basal body temperature assessment to confirm ovulation), subjective measures (e.g. retrospective questionnaires to establish menstrual cycle phase), grouping non-homogenous participants (e.g. using OC and HRT users on different brands and types of exogenous steroid supplementation) and comparing incompatible strength measures (e.g. different test modalities and muscle types). For a detailed summary of these and other issues see CABLE and ELLIOTT1212 . Cable NT, Elliott KJ. The influence of reproductive hormones on muscle strength. Biol Rhythm Res. 2004;35:235-44., ELLIOTT-SALE et al.2727 . Elliott-Sale KJ, Smith S, Bacon J, et al. Examining the role of oral contraceptive users as an experimental and/or control group in athletic performance studies. Contraception. 2013;88:408-12. and ELLIOTT-SALE and Martin2828 . Elliott-Sale KJ, Martin D. The use of different models of female reproductive status in human performance research; with a specific focus on muscle strength. [Short Communication]. Androl Gynecol: Curr Res. 2013;1:4.. The purpose of this current perspective is to summarise the research published since 2004 and to critically evaluate if the research from the eighties and nineties has influenced and informed the research design of recent studies.

The evidence for an effect of oestrogen on muscle strength

During the last ten years approximately 15 papers have shown an effect of oestrogen on muscle strength or determinants of muscle strength (TABLE 1). Three studies used the menstrual cycle as a model of reproductive functioning2929 . Kerksick C, Taylor L 4th, Harvey A, Willoughby D. Gender-related differences in muscle injury, oxidative stress, and apoptosis. Med Sci Sports Exerc. 2008;40:1772-80., while two further studies combined the menstrual cycle with OC use3232 . Nicolay CW, Kenney JL, Lucki NC. Grip strength and endurance throughout the menstrual cycle in eumenorrheic and women using oral contraceptives. Int J Ind Ergon. 2007; 35: 605-18.-3333 . Bryant AL, Crossley KM, Bartold S, Hohmann E, Clark RA. Estrogen-induced effects on the neuro-mechanics of hopping in humans. Arbeitsphysiologie. 2011;111:245-52.. One report examined the effects of OC consumption and withdrawal on strength3434 . Rechichi C, Dawson B. Effect of oral contraceptive cycle phase on performance in team sport players. J Sci Med Sport. 2009;12:190-5. and one combined previous OC use with a control group that had never used OC’s3535 . Allali F, El Mansouri L, Abourazzak Fz, et al. The effect of past use of oral contraceptive on bone mineral density, bone biochemical markers and muscle strength in healthy pre and post-menopausal women. BMC Womens Health. 2009;31:3-9.. Undoubtedly, the most common reproductive functioning models used in the literature in the last decade were the menopause and HRT3636 . Onambele GN, Bruce SA, Woledge RC. Oestrogen status in relation to the early training responses in human thumb adductor muscles. Acta Physiol (Oxf). 2006;188:41-52.

37 . Pöllänen E, Ronkainen PH, Suominen H, et al. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res. 2007;10:485-500.

38 . Rolland YM, Perry HM 3rd, Patrick P, Banks WA, Morley JE. Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women. J Gerontol A Biol Sci Med Sci. 2007;62:330-5.

39 . Sowers M, Tomey K, Jannausch M, Eyvazzadeh A, Nan B, Randolph J Jr. Physical functioning and menopause states. Obstet Gynecol. 2007;110:1290-6.

40 . Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Hormone therapy attenuates exercise-induced skeletal muscle damage in postmenopausal women. J Appl Physiol. (1985). 2009;107:853-8.

41 . Ronkainen PH, Kovanen V, Alén M, et al. Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol. 2009;107:25-33.

42 . van Geel TA, Geusens PP, Winkens B, Sels JP, Dinant GJ. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: a cross-sectional study. Eur J Endocrinol. 2009;160:681-7.

43 . Finni T, Noorkoiv M, Pöllänen E, et al. Muscle function in monozygotic female twin pairs discordant for hormone replacement therapy. Muscle Nerve. 2011;44:769-75.
-4444 . Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Hormone therapy and maximal eccentric exercise alters myostatin-related gene expression in postmenopausal women. J Strength Cond Res. 2012;26:1374-82.. These models were used to investigate numerous facets of muscle strength including; muscle stiffness3030 . Bell DR, Blackburn JT, Ondrak KS, et al. The effects of oral contraceptive use on muscle stiffness across the menstrual cycle. Clin J Sport Med. 2011;21:467-73. and soreness2929 . Kerksick C, Taylor L 4th, Harvey A, Willoughby D. Gender-related differences in muscle injury, oxidative stress, and apoptosis. Med Sci Sports Exerc. 2008;40:1772-80., dynamic and isometric force production3838 . Rolland YM, Perry HM 3rd, Patrick P, Banks WA, Morley JE. Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women. J Gerontol A Biol Sci Med Sci. 2007;62:330-5.,4343 . Finni T, Noorkoiv M, Pöllänen E, et al. Muscle function in monozygotic female twin pairs discordant for hormone replacement therapy. Muscle Nerve. 2011;44:769-75., power4141 . Ronkainen PH, Kovanen V, Alén M, et al. Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol. 2009;107:25-33., endurance3232 . Nicolay CW, Kenney JL, Lucki NC. Grip strength and endurance throughout the menstrual cycle in eumenorrheic and women using oral contraceptives. Int J Ind Ergon. 2007; 35: 605-18., performance3333 . Bryant AL, Crossley KM, Bartold S, Hohmann E, Clark RA. Estrogen-induced effects on the neuro-mechanics of hopping in humans. Arbeitsphysiologie. 2011;111:245-52., functional capacity3939 . Sowers M, Tomey K, Jannausch M, Eyvazzadeh A, Nan B, Randolph J Jr. Physical functioning and menopause states. Obstet Gynecol. 2007;110:1290-6. and gene expression3737 . Pöllänen E, Ronkainen PH, Suominen H, et al. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res. 2007;10:485-500.. Generally, the relationship between oestrogen and muscle strength was positive; high concentrations of oestradiol were associated with the preservation of muscle strength and mass in addition to mobility and function3636 . Onambele GN, Bruce SA, Woledge RC. Oestrogen status in relation to the early training responses in human thumb adductor muscles. Acta Physiol (Oxf). 2006;188:41-52.

37 . Pöllänen E, Ronkainen PH, Suominen H, et al. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res. 2007;10:485-500.

38 . Rolland YM, Perry HM 3rd, Patrick P, Banks WA, Morley JE. Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women. J Gerontol A Biol Sci Med Sci. 2007;62:330-5.

39 . Sowers M, Tomey K, Jannausch M, Eyvazzadeh A, Nan B, Randolph J Jr. Physical functioning and menopause states. Obstet Gynecol. 2007;110:1290-6.

40 . Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Hormone therapy attenuates exercise-induced skeletal muscle damage in postmenopausal women. J Appl Physiol. (1985). 2009;107:853-8.

41 . Ronkainen PH, Kovanen V, Alén M, et al. Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol. 2009;107:25-33.

42 . van Geel TA, Geusens PP, Winkens B, Sels JP, Dinant GJ. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: a cross-sectional study. Eur J Endocrinol. 2009;160:681-7.

43 . Finni T, Noorkoiv M, Pöllänen E, et al. Muscle function in monozygotic female twin pairs discordant for hormone replacement therapy. Muscle Nerve. 2011;44:769-75.
-4444 . Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Hormone therapy and maximal eccentric exercise alters myostatin-related gene expression in postmenopausal women. J Strength Cond Res. 2012;26:1374-82.. However, one study showed a negative relationship between oestrogen concentrations and muscle function; ALLALI et al.3535 . Allali F, El Mansouri L, Abourazzak Fz, et al. The effect of past use of oral contraceptive on bone mineral density, bone biochemical markers and muscle strength in healthy pre and post-menopausal women. BMC Womens Health. 2009;31:3-9. showed increased performance in a number of functional tests in previous OC users. Only one study showed a detrimental effect of high concentrations of oestrogen on muscle function; NICOLAY et al.3232 . Nicolay CW, Kenney JL, Lucki NC. Grip strength and endurance throughout the menstrual cycle in eumenorrheic and women using oral contraceptives. Int J Ind Ergon. 2007; 35: 605-18. found that static handgrip endurance was reduced in the late-follicular phase of the menstrual cycle when oestrogen levels are high.

TABLE 1
Studies showing an effect of oestrogen on muscle strength or determinants of muscle strength.

The evidence against an effect of oestrogen on muscle strength

Since 2004, approximately 20 studies have not shown any relationship between oestrogen and muscle strength (TABLE 2). Of these studies, nine employed a menopause model with and without HRT4545 . Maddalozzo GF, Cardinal BJ, Li F, Snow CM. The association between hormone therapy use and changes in strength and body composition in early postmenopausal women. Menopause. 2004;11:438-46.

46 . Dayal M, Sammel MD, Zhao J, Hummel AC, Vandenbourne K, Barnhart KT. Supplementation with DHEA: effect on muscle size, strength, quality of life, and lipids. J Womens Health (Larchmt). 2005;14:391-400.

47 . Schaap LA, Pluijm SM, Smit JH, et al. The association of sex hormone levels with poor mobility, low muscle strength and incidence of falls among older men and women. Clin Endocrinol (Oxf). 2005;63:152-60.

48 . Taaffe DR, Newman AB, Haggerty CL, et al. Estrogen replacement, muscle composition, and physical function: the Health ABC Study. Med Sci Sports Exerc. 2005;37:1741-7.

49 . Lebrun CE, van der Schouw YT, de Jong FH, Pols HA, Grobbee DE, Lamberts SW. Relations between body composition, functional and hormonal parameters and quality of life in healthy postmenopausal women. Maturitas. 2006;55:82-92.

50 . Sipilä S, Heikkinen E, Cheng S, et al. Endogenous hormones, muscle strength, and risk of fall-related fractures in older women. Gerontol A Biol Sci Med Sci. 2006;61:92-6.

51 . Ribom EL, Svensson P, van Os S, Larsson M, Naessen T. Low-dose tibolone (1.25 mg/d) does not affect muscle strength in older women. Menopause. 2011;18:194-7.

52 . Jacobsen DE, Melis RJ, Verhaar HJ, Olde Rikkert MG. Raloxifene and tibolone in elderly women: a randomized, double-blind, double-dummy, placebo-controlled trial. J Am Med Dir Assoc. 2012;13:189.e1-7.
-5353 . Choquette S, Dion T, Brochu M, Dionne IJ. Soy isoflavones and exercise to improve physical capacity in postmenopausal women. Climacteric. 2013;16:70-7., while six used the menstrual cycle5454 . Grundberg E, Ribom EL, Brändström H, Ljunggren O, Mallmin H, Kindmark A. A TA-repeat polymorphism in the gene for the estrogen receptor alpha does not correlate with muscle strength or body composition in young adult Swedish women. Maturitas. 2005;50:153-60.

55 . Hertel J, Williams NI, Olmsted-Kramer LC, Leidy HJ, Putukian M. Neuromuscular performance and knee laxity do not change across the menstrual cycle in female athletes. Knee Surg Sports Traumatol Arthrosc. 2006;14:817-22.

56 . Abt JP, Sell TC, Laudner KG, et al. Neuromuscular and biomechanical characteristics do not vary across the menstrual cycle. Knee Surg Sports Traumatol Arthrosc. 2007;15:901-7.

57 . Burgess KE, Pearson SJ, Onambélé GL. Patellar tendon properties with fluctuating menstrual cycle hormones. J Strength Cond Res. 2010;24:2088-95.

58 . Montgomery MM, Shultz SJ. Isometric knee-extension and knee-flexion torque production during early follicular and postovulatory phases in recreationally active women. J Athl Train. 2010;45:586-93.

59 . Wild CY, Steele JR, Munro BJ. Musculoskeletal and estrogen changes during the adolescent growth spurt in girls. Med Sci Sports Exerc. 2013;45:138-45.
-6060 . Tsampoukos A, Peckham EA, James R, Nevill ME. Effect of menstrual cycle phase on sprinting performance. Eur J Appl Physiol. 2010;109:659-67.. One study used a pubertal model5959 . Wild CY, Steele JR, Munro BJ. Musculoskeletal and estrogen changes during the adolescent growth spurt in girls. Med Sci Sports Exerc. 2013;45:138-45. and the remaining studies used OC’s6161 . Elliott KJ, Cable NT, Reilly T. Does oral contraceptive use affect maximum force production in women? Br J Sports Med. 2005;39:15-9.

62 . Nichols AW, Hetzler RK, Villanueva RJ, Stickley CD, Kimura IF. Effects of combination oral contraceptives on strength development in women athletes. J Strength Cond Res. 2008;22:1625-32.
-6363 . Ekenros L, Hirschberg AL, Heijne A, Fridén C. Oral contraceptives do not affect muscle strength and hop performance in active women. Clin J Sport Med. 2013;23:202-7.. Muscle function was assessed through a variety of measures including; maximal dynamic5353 . Choquette S, Dion T, Brochu M, Dionne IJ. Soy isoflavones and exercise to improve physical capacity in postmenopausal women. Climacteric. 2013;16:70-7. and isometric5858 . Montgomery MM, Shultz SJ. Isometric knee-extension and knee-flexion torque production during early follicular and postovulatory phases in recreationally active women. J Athl Train. 2010;45:586-93. strength, endurance4646 . Dayal M, Sammel MD, Zhao J, Hummel AC, Vandenbourne K, Barnhart KT. Supplementation with DHEA: effect on muscle size, strength, quality of life, and lipids. J Womens Health (Larchmt). 2005;14:391-400., performance6060 . Tsampoukos A, Peckham EA, James R, Nevill ME. Effect of menstrual cycle phase on sprinting performance. Eur J Appl Physiol. 2010;109:659-67., power4545 . Maddalozzo GF, Cardinal BJ, Li F, Snow CM. The association between hormone therapy use and changes in strength and body composition in early postmenopausal women. Menopause. 2004;11:438-46. and functional capacity4848 . Taaffe DR, Newman AB, Haggerty CL, et al. Estrogen replacement, muscle composition, and physical function: the Health ABC Study. Med Sci Sports Exerc. 2005;37:1741-7.. Despite significant changes in oestrogen concentration, none of these studies were able to demonstrate the putative role of oestrogen in determining muscle strength.

TABLE 2
Studies showing no effect of oestrogen on muscle strength or determinants of muscle strength.

Methodological issues and advancements

The menopause and the menstrual cycle remain the most popular models for investigating the effects of oestrogen on muscle strength; accounting for more than two thirds of recent publications. Surprisingly, the IVF model has not been used 2004, despite providing acute supra-physiological changes in oestradiol concentration without the confounding factors associated with the menopause and the menstrual cycle: notably age and inter and intra-individual variability in hormone secretion. In addition, both puberty and pregnancy have been under-utilised, even though they provide substantial chronic natural changes in the female hormonal milieu9. Elliott KJ, Cable NT, Reilly T, Sefton V, Kingsland C, Diver M. Effects of supra-physiological changes in human ovarian hormone levels on maximum force production of the first dorsal interosseus muscle. Exp Physiol. 2005;90:215-23..

It is encouraging to note that the majority of recent studies have used blood samples to confirm reproductive status; post-menopausal3838 . Rolland YM, Perry HM 3rd, Patrick P, Banks WA, Morley JE. Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women. J Gerontol A Biol Sci Med Sci. 2007;62:330-5.,5050 . Sipilä S, Heikkinen E, Cheng S, et al. Endogenous hormones, muscle strength, and risk of fall-related fractures in older women. Gerontol A Biol Sci Med Sci. 2006;61:92-6., menstrual cycle phase2929 . Kerksick C, Taylor L 4th, Harvey A, Willoughby D. Gender-related differences in muscle injury, oxidative stress, and apoptosis. Med Sci Sports Exerc. 2008;40:1772-80.-3030 . Bell DR, Blackburn JT, Ondrak KS, et al. The effects of oral contraceptive use on muscle stiffness across the menstrual cycle. Clin J Sport Med. 2011;21:467-73. and OC use9. Elliott KJ, Cable NT, Reilly T, Sefton V, Kingsland C, Diver M. Effects of supra-physiological changes in human ovarian hormone levels on maximum force production of the first dorsal interosseus muscle. Exp Physiol. 2005;90:215-23.,3434 . Rechichi C, Dawson B. Effect of oral contraceptive cycle phase on performance in team sport players. J Sci Med Sport. 2009;12:190-5.. However, no studies have specifically measured the bioavailable concentration of oestradiol, which may be of particular interest for studies using post-menopausal groups; previous work has shown that the bioavailability of oestradiol did not significantly differ between two phases of the menstrual cycle6464 . Elliott KJ, Cable NT, Reilly T, Diver MJ. Effect of menstrual cycle phase on the concentration of bioavailable β-17-oestradiol and testosterone and muscle strength. Clin Sci. 2003;105:663-9.. The bioavailable part of oestrogen is not a set proportion of the total concentration and is dependent on its affinity to and concentration of its binding protein. Therefore, models of reproductive functioning, such as the menopause, might influence the bioavailable concentration of oestradiol and subsequently its relationship with muscle strength. Moreover, there are still a number of publications that have used a variety of types and brands of OC’s3333 . Bryant AL, Crossley KM, Bartold S, Hohmann E, Clark RA. Estrogen-induced effects on the neuro-mechanics of hopping in humans. Arbeitsphysiologie. 2011;111:245-52.,6363 . Ekenros L, Hirschberg AL, Heijne A, Fridén C. Oral contraceptives do not affect muscle strength and hop performance in active women. Clin J Sport Med. 2013;23:202-7. and HRT’s3939 . Sowers M, Tomey K, Jannausch M, Eyvazzadeh A, Nan B, Randolph J Jr. Physical functioning and menopause states. Obstet Gynecol. 2007;110:1290-6.,4141 . Ronkainen PH, Kovanen V, Alén M, et al. Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol. 2009;107:25-33., which can lead to extremely large variation in hormone concentration when grouped together and may ultimately lead to type II errors2727 . Elliott-Sale KJ, Smith S, Bacon J, et al. Examining the role of oral contraceptive users as an experimental and/or control group in athletic performance studies. Contraception. 2013;88:408-12..

The term “muscle strength” is too ambiguous and makes comparing studies and drawing any conclusions very difficult. In the last decade, over 20 indices of muscle strength or determinants of muscle strength have been investigated (see TABLES 1 and 2 for exact tests). It would be judicious to perform a meta-analysis on each of the main components of strength (dynamic, isometric, endurance, power) in relation to oestrogen status. It is interesting to note that recently several studies have investigated the effect of oestrogen on the gene expression influencing muscle strength and hypertrophy3737 . Pöllänen E, Ronkainen PH, Suominen H, et al. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res. 2007;10:485-500.,4444 . Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Hormone therapy and maximal eccentric exercise alters myostatin-related gene expression in postmenopausal women. J Strength Cond Res. 2012;26:1374-82., indicating a new direction for this type of research.

Conclusions

To date, there is still no unanimous consensus regarding the effect of oestrogen on muscle strength. There is almost the same number of papers supporting an effect of oestrogen on skeletal muscle function as there are showing no effect. Moreover, both positive and negative correlations have been reported when an effect was evident. Future work should focus on discrete elements of muscle strength and use the best and most appropriate models of reproductive functioning available; i.e. models that cause the greatest magnitude of change in sex hormone concentration (e.g. IVF). In addition, future work should aim to control as many confounding factors as possible (e.g. age, smoking, exercise status etc.). Moreover, there is a need to conduct meta-analyses on previous research in order to move towards a conclusion on this topic.

References

  • 1
    Higgs SL, Robertson LA. Cyclic variations in perceived exertion and physical work capacity in females. Can J Appl Sport Sci. 1981;6:191-6.
  • 2
    Cauley JA, Petrini AM, LaPorte RE, et al. The decline in grip strength in the menopause: relationship to physical activity, estrogen use and anthropometric factors. J Chronic Dis. 1987;40:115-20.
  • 3
    Davies BN, Elford JCC, Jamieson KF. Variations in performance in simple muscle tests at different phases of the menstrual cycle. J Sports Med Phys Fitness. 1991;31:532-7.
  • 4
    Phillips SK, Sanderson AG, Birch K, Bruce SA, Woledge RC. Changes in maximal voluntary force of human adductor pollicis muscle during the menstrual cycle. J Physiol. 1996;496:551-7.
  • 5
    White MJ, Weeks C. No evidence for a change in the voluntary or electrically evoked contractile characteristics of the triceps surae during the human menstrual cycle. J Physiol. 1998;506:119.
  • 6
    Bassey EJ, Coates L, Culpen J, Littlewood JJ, Owen M, Wilson K. Natural variations in oestrogen and FSH levels in eumenorrheic women in negative association with voluntary muscle strength. J Physiol. 1995;489:45.
  • 7
    Armstrong AL, Oborne J, Coupland CAC, MacPearson MB, Bassey EL, Wallace WA. Effects of hormone replacement therapy on muscle performance and balance in postmenopausal women. Clin Sci (Lond). 1996;91:685-90.
  • 8
    Greeves JP, Cable NT, Luckas MJM, Reilly T, Biljan MM. Effects of acute changes in oestrogen on muscle function of the first dorsal interosseus muscle in humans. J Physiol. 1997;500:265-70.
  • 9
    Elliott KJ, Cable NT, Reilly T, Sefton V, Kingsland C, Diver M. Effects of supra-physiological changes in human ovarian hormone levels on maximum force production of the first dorsal interosseus muscle. Exp Physiol. 2005;90:215-23.
  • 10
    Sarwar, R, Niclos BB, Rutherford OM. Changes in muscle strength, relaxation rate and fatigability during the human menstrual cycle. J Physiol. 1996;493:267-72.
  • 11
    Skelton DA, Phillips SK, Bruce SA, Naylor CH, Woledge RC. Hormone replacement therapy increases isometric muscle strength of adductor pollicis in post-menopausal women. Clin Sci (Lond). 1999;96:357-64.
  • 12
    Cable NT, Elliott KJ. The influence of reproductive hormones on muscle strength. Biol Rhythm Res. 2004;35:235-44.
  • 13
    Burrows M, Peters CE. The influence of oral contraceptives on athletic performance in female athletes. Sports Med. 2007;37:557-74.
  • 14
    Rechichi C, Dawson B, Goodman C. Athletic performance and the oral contraceptive. Int J Sports Physiol Perform. 2009;4:151-62.
  • 15
    Jacobi MP. The question of rest for women during menstruation. New York: G.P. Putnam’s sons; 1877.
  • 16
    Wirth JC, Lohman TG. The relationship of static muscle function to use of oral contraceptives. Med Sci Sports Exerc. 1982;14:16-20.
  • 17
    Beltran Niclos B, Welsh L, Sarwar R, Rutherford OM. Gender and age comparisons of the contractile properties of human quadriceps muscle. J Physiol. 1995;483:131.
  • 18
    Dibrezzo R, Fort IL, Brown B. Relationship among strength, endurance, weight and body fat during three phases of the menstrual cycle. J Sports Med Phys Fitness. 1991;31:89-94.
  • 19
    Lebrun CM, McKenzie DC, Prior JC, Taunton JE. Effects of menstrual cycle phase on athletic performance. Med Sci Sports Exerc. 1995;27:437-44.
  • 20
    Gur H. Concentric and eccentric isokinetic measurements in knee muscles during the menstrual cycle: a special reference to reciprocal moment ratios. Arch Phys Med Rehabil. 1997;78:501-5.
  • 21
    Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC. Muscle weakness in women occurs at an earlier age than in men, but is preserved by hormone replacement therapy. Clin Sci (Lond). 1993;84:95-8.
  • 22
    Calmels P, Vico L, Alexandre C, Minaire P. Cross-sectional study of muscle strength and bone mineral density in a population of 106 women between the ages of 44 and 87 years: relationship with age and menopause. Eur J Appl Physiol Occup Physiol. 1995;70:180-6.
  • 23
    Greeves JP, Cable NT, Reilly T, Kingsland C. Changes in muscle strength in women following the menopause: a longitudinal assessment of the efficacy of hormone replacement therapy. Clin Sci (Lond). 1999;97:79-84.
  • 24
    Taaffe DR, Villa ML, Delay R, Marcus R. Maximal muscle strength of elderly women is not influenced by oestrogen status. Age Ageing. 1995;24:329-33.
  • 25
    Bassey EJ, Mockett SP, Fentem PH. Lack of variation in muscle strength with menstrual status in healthy women aged 45-54 years: data from a national survey. Eur J Appl Physiol Occup Physiol. 1996;73:382-6.
  • 26
    Thompson HS, Hyatt JP, De Souza MJ, Clarkson PM. The effects of oral contraceptives on delayed onset muscle soreness following exercise. Contraception. 1997;56:59-65.
  • 27
    Elliott-Sale KJ, Smith S, Bacon J, et al. Examining the role of oral contraceptive users as an experimental and/or control group in athletic performance studies. Contraception. 2013;88:408-12.
  • 28
    Elliott-Sale KJ, Martin D. The use of different models of female reproductive status in human performance research; with a specific focus on muscle strength. [Short Communication]. Androl Gynecol: Curr Res. 2013;1:4.
  • 29
    Kerksick C, Taylor L 4th, Harvey A, Willoughby D. Gender-related differences in muscle injury, oxidative stress, and apoptosis. Med Sci Sports Exerc. 2008;40:1772-80.
  • 30
    Bell DR, Blackburn JT, Ondrak KS, et al. The effects of oral contraceptive use on muscle stiffness across the menstrual cycle. Clin J Sport Med. 2011;21:467-73.
  • 31
    Sakamaki M, Yasuda T, Abe T. Comparison of low-intensity blood flow-restricted training-induced muscular hypertrophy in eumenorrheic women in the follicular phase and luteal phase and age-matched men. Clin Physiol Funct Imaging. 2012;32:185-91.
  • 32
    Nicolay CW, Kenney JL, Lucki NC. Grip strength and endurance throughout the menstrual cycle in eumenorrheic and women using oral contraceptives. Int J Ind Ergon. 2007; 35: 605-18.
  • 33
    Bryant AL, Crossley KM, Bartold S, Hohmann E, Clark RA. Estrogen-induced effects on the neuro-mechanics of hopping in humans. Arbeitsphysiologie. 2011;111:245-52.
  • 34
    Rechichi C, Dawson B. Effect of oral contraceptive cycle phase on performance in team sport players. J Sci Med Sport. 2009;12:190-5.
  • 35
    Allali F, El Mansouri L, Abourazzak Fz, et al. The effect of past use of oral contraceptive on bone mineral density, bone biochemical markers and muscle strength in healthy pre and post-menopausal women. BMC Womens Health. 2009;31:3-9.
  • 36
    Onambele GN, Bruce SA, Woledge RC. Oestrogen status in relation to the early training responses in human thumb adductor muscles. Acta Physiol (Oxf). 2006;188:41-52.
  • 37
    Pöllänen E, Ronkainen PH, Suominen H, et al. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res. 2007;10:485-500.
  • 38
    Rolland YM, Perry HM 3rd, Patrick P, Banks WA, Morley JE. Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women. J Gerontol A Biol Sci Med Sci. 2007;62:330-5.
  • 39
    Sowers M, Tomey K, Jannausch M, Eyvazzadeh A, Nan B, Randolph J Jr. Physical functioning and menopause states. Obstet Gynecol. 2007;110:1290-6.
  • 40
    Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Hormone therapy attenuates exercise-induced skeletal muscle damage in postmenopausal women. J Appl Physiol. (1985). 2009;107:853-8.
  • 41
    Ronkainen PH, Kovanen V, Alén M, et al. Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol. 2009;107:25-33.
  • 42
    van Geel TA, Geusens PP, Winkens B, Sels JP, Dinant GJ. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: a cross-sectional study. Eur J Endocrinol. 2009;160:681-7.
  • 43
    Finni T, Noorkoiv M, Pöllänen E, et al. Muscle function in monozygotic female twin pairs discordant for hormone replacement therapy. Muscle Nerve. 2011;44:769-75.
  • 44
    Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Hormone therapy and maximal eccentric exercise alters myostatin-related gene expression in postmenopausal women. J Strength Cond Res. 2012;26:1374-82.
  • 45
    Maddalozzo GF, Cardinal BJ, Li F, Snow CM. The association between hormone therapy use and changes in strength and body composition in early postmenopausal women. Menopause. 2004;11:438-46.
  • 46
    Dayal M, Sammel MD, Zhao J, Hummel AC, Vandenbourne K, Barnhart KT. Supplementation with DHEA: effect on muscle size, strength, quality of life, and lipids. J Womens Health (Larchmt). 2005;14:391-400.
  • 47
    Schaap LA, Pluijm SM, Smit JH, et al. The association of sex hormone levels with poor mobility, low muscle strength and incidence of falls among older men and women. Clin Endocrinol (Oxf). 2005;63:152-60.
  • 48
    Taaffe DR, Newman AB, Haggerty CL, et al. Estrogen replacement, muscle composition, and physical function: the Health ABC Study. Med Sci Sports Exerc. 2005;37:1741-7.
  • 49
    Lebrun CE, van der Schouw YT, de Jong FH, Pols HA, Grobbee DE, Lamberts SW. Relations between body composition, functional and hormonal parameters and quality of life in healthy postmenopausal women. Maturitas. 2006;55:82-92.
  • 50
    Sipilä S, Heikkinen E, Cheng S, et al. Endogenous hormones, muscle strength, and risk of fall-related fractures in older women. Gerontol A Biol Sci Med Sci. 2006;61:92-6.
  • 51
    Ribom EL, Svensson P, van Os S, Larsson M, Naessen T. Low-dose tibolone (1.25 mg/d) does not affect muscle strength in older women. Menopause. 2011;18:194-7.
  • 52
    Jacobsen DE, Melis RJ, Verhaar HJ, Olde Rikkert MG. Raloxifene and tibolone in elderly women: a randomized, double-blind, double-dummy, placebo-controlled trial. J Am Med Dir Assoc. 2012;13:189.e1-7.
  • 53
    Choquette S, Dion T, Brochu M, Dionne IJ. Soy isoflavones and exercise to improve physical capacity in postmenopausal women. Climacteric. 2013;16:70-7.
  • 54
    Grundberg E, Ribom EL, Brändström H, Ljunggren O, Mallmin H, Kindmark A. A TA-repeat polymorphism in the gene for the estrogen receptor alpha does not correlate with muscle strength or body composition in young adult Swedish women. Maturitas. 2005;50:153-60.
  • 55
    Hertel J, Williams NI, Olmsted-Kramer LC, Leidy HJ, Putukian M. Neuromuscular performance and knee laxity do not change across the menstrual cycle in female athletes. Knee Surg Sports Traumatol Arthrosc. 2006;14:817-22.
  • 56
    Abt JP, Sell TC, Laudner KG, et al. Neuromuscular and biomechanical characteristics do not vary across the menstrual cycle. Knee Surg Sports Traumatol Arthrosc. 2007;15:901-7.
  • 57
    Burgess KE, Pearson SJ, Onambélé GL. Patellar tendon properties with fluctuating menstrual cycle hormones. J Strength Cond Res. 2010;24:2088-95.
  • 58
    Montgomery MM, Shultz SJ. Isometric knee-extension and knee-flexion torque production during early follicular and postovulatory phases in recreationally active women. J Athl Train. 2010;45:586-93.
  • 59
    Wild CY, Steele JR, Munro BJ. Musculoskeletal and estrogen changes during the adolescent growth spurt in girls. Med Sci Sports Exerc. 2013;45:138-45.
  • 60
    Tsampoukos A, Peckham EA, James R, Nevill ME. Effect of menstrual cycle phase on sprinting performance. Eur J Appl Physiol. 2010;109:659-67.
  • 61
    Elliott KJ, Cable NT, Reilly T. Does oral contraceptive use affect maximum force production in women? Br J Sports Med. 2005;39:15-9.
  • 62
    Nichols AW, Hetzler RK, Villanueva RJ, Stickley CD, Kimura IF. Effects of combination oral contraceptives on strength development in women athletes. J Strength Cond Res. 2008;22:1625-32.
  • 63
    Ekenros L, Hirschberg AL, Heijne A, Fridén C. Oral contraceptives do not affect muscle strength and hop performance in active women. Clin J Sport Med. 2013;23:202-7.
  • 64
    Elliott KJ, Cable NT, Reilly T, Diver MJ. Effect of menstrual cycle phase on the concentration of bioavailable β-17-oestradiol and testosterone and muscle strength. Clin Sci. 2003;105:663-9.

Publication Dates

  • Publication in this collection
    Apr-Jun 2014

History

  • Received
    20 Mar 2014
  • Accepted
    07 Apr 2014
Escola de Educação Física e Esporte da Universidade de São Paulo Av. Prof. Mello Moraes, 65, 05508-030 São Paulo SP/Brasil, Tel./Fax: (55 11) 3091 3147 - São Paulo - SP - Brazil
E-mail: reveefe@usp.br