Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: A study with monozygotic twin pairs

Journal of Applied Physiology

Volumn 107, Issue 1, 2009, Pages 25-33

  Ronkainen, Paula H A ^a   Kovanen, Vuokko ^a   Alén, Markku ^a,b   Pöllänen, Eija ^a   Palonen, Eeva Maija ^a   Ankarberg Lindgren, Carina ^c   Hämäläinen, Esa ^d   Turpeinen, Ursula ^d   Kujala, Urho M ^a   Puolakka, Jukka ^e   Kaprio, Jaakko ^f,g   Sipilä, Sarianna ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b OULU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e Central Finland Central Hospital   (Finland)

^f UNIVERSITY OF HELSINKI   (Finland)

^g NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

Aging; Menopause; Muscle power; Muscle strength; Sex hormones

Indexed keywords

ESTROGEN; TIBOLONE;

ADULT; ARTICLE; BODY COMPOSITION; BODY FAT; CLINICAL ARTICLE; CONTROLLED STUDY; ESTROGEN THERAPY; FEMALE; GRIP STRENGTH; HAND GRIP; HORMONE SUBSTITUTION; HUMAN; JUMPING; KNEE FUNCTION; LEG MUSCLE; LONG TERM CARE; MONOZYGOTIC TWINS; MUSCLE FUNCTION; MUSCLE ISOMETRIC CONTRACTION; MUSCLE MASS; MUSCLE STRENGTH; MUSCLE WEAKNESS; POSTMENOPAUSE; PRIORITY JOURNAL; SKELETAL MUSCLE; TREATMENT DURATION; WALKING SPEED;

ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; HAND STRENGTH; HUMANS; ISOMETRIC CONTRACTION; MENOPAUSE; MIDDLE AGED; MUSCLE CONTRACTION; MUSCLE, SKELETAL; TOMOGRAPHY, X-RAY COMPUTED; TWIN STUDIES AS TOPIC; TWINS, MONOZYGOTIC; WALKING;

EID: 67650084403     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.91518.2008     Document Type: Article

References (66)

1. Albu JB, Kovera AJ, Allen L, Wainwright M, Berk E, Raja-Khan N, Janumala I, Burkey B, Heshka S, Gallagher D. Independent association of insulin resistance with larger amounts of intermuscular adipose tissue and a greater acute insulin response to glucose in African American than in white nondiabetic women. Am J Clin Nutr 82: 1210-1217, 2005.
2. Aloia JF, Vaswani A, Russo L, Sheehan M, Flaster E. The influence of menopause and hormonal replacement therapy on body cell mass and body fat mass. Am J Obstet Gynecol 172: 896-900, 1995.
3. Ankarberg-Lindgren C, Norjavaara E. A purification step prior to commercial sensitive immunoassay is necessary to achieve clinical usefulness when quantifying serum 17beta-estradiol in prepubertal children. Eur J Endocrinol 158: 117-124, 2008.
4. Baumgartner RN, Wayne SJ, Waters DL, Janssen I, Gallagher D, Morley JE. Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly. Obes Res 12: 1995-2004, 2004.
5. Bean JF, Leveille SG, Kiely DK, Bandinelli S, Guralnik JM, Ferrucci L. A comparison of leg power and leg strength within the InCHIANTI study: which influences mobility more? J Gerontol A Biol Sci Med Sci 58: 728-733, 2003.
6. Bjornerem A, Straume B, Midtby M, Fonnebo V, Sundsfjord J, Svartberg J, Acharya G, Oian P, Berntsen GK. Endogenous sex hormones in relation to age, sex, lifestyle factors, and chronic diseases in a general population: the Tromso Study. J Clin Endocrinol Metab 89: 6039-6047, 2004.
7. Bosco C, Luhtanen P, Komi PV. A simple method for measurement of mechanical power in jumping. Eur J Appl Physiol Occup Physiol 50: 273-282, 1983.
8. Bouchard C, Tremblay A, Despres JP, Nadeau A, Lupien PJ, Theriault G, Dussault J, Moorjani S, Pinault S, Fournier G. The response to long-term overfeeding in identical twins. N Engl J Med 322: 1477-1482, 1990.
9. Brann DW, Dhandapani K, Wakade C, Mahesh VB, Khan MM. Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids 72: 381-405, 2007.
10. de Ferranti S, Mozaffarian D. The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem 54: 945-955, 2008.
11. D'Eon TM, Souza SC, Aronovitz M, Obin MS, Fried SK, Greenberg AS. Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J Biol Chem 280: 35983-35991, 2005.
12. Genazzani AD, Gamba O, Nappi L, Volpe A, Petraglia F. Modulatory effects of a synthetic steroid (tibolone) and estradiol on spontaneous and GH-RH-induced GH secretion in postmenopausal women. Maturitas 28: 27-33, 1997.
13. Genazzani AR, Pluchino N, Luisi S, Luisi M. Estrogen, cognition and female ageing. Hum Reprod Update 13: 175-187, 2007.
14. Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R. Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol 89: 104-110, 2000.
15. Greeves JP, Cable NT, Luckas MJ, Reilly T, Biljan MM. Effects of acute changes in oestrogen on muscle function of the first dorsal interosseus muscle in humans. J Physiol 500: 265-270, 1997.
16. Grimby G. Physical activity and muscle training in the elderly. Acta Med Scand Suppl 711: 233-237, 1986.
17. Guralnik JM, Ferrucci L, Simonsick EM, Salive ME, Wallace RB. Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N Engl J Med 332: 556-561, 1995.
18. Haarbo J, Marslew U, Gotfredsen A, Christiansen C. Postmenopausal hormone replacement therapy prevents central distribution of body fat after menopause. Metabolism 40: 1323-1326, 1991.
19. Hakim AA, Petrovitch H, Burchfiel CM, Ross GW, Rodriguez BL, White LR, Yano K, Curb JD, Abbott RD. Effects of walking on mortality among nonsmoking retired men. N Engl J Med 338: 94-99, 1998.
20. Hanggi W, Lippuner K, Jaeger P, Birkhauser MH, Horber FF. Differential impact of conventional oral or transdermal hormone replacement therapy or tibolone on body composition in postmenopausal women. Clin Endocrinol (Oxf) 48: 691-699, 1998.
21. Iannuzzi-Sucich M, Prestwood KM, Kenny AM. Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy, older men and women. J Gerontol A Biol Sci Med Sci 57: M772-M777, 2002.
22. Jacobsen DE, Samson MM, Kezic S, Verhaar HJ. Postmenopausal HRT and tibolone in relation to muscle strength and body composition. Maturitas 58: 7-18, 2007.
23. Jensen LB, Vestergaard P, Hermann AP, Gram J, Eiken P, Abrahamsen B, Brot C, Kolthoff N, Sorensen OH, Beck-Nielsen H, Nielsen SP, Charles P, Mosekilde L. Hormone replacement therapy dissociates fat mass and bone mass, and tends to reduce weight gain in early postmenopausal women: a randomized controlled 5-year clinical trial of the Danish Osteoporosis Prevention Study. J Bone Miner Res 18: 333-342, 2003.
24. Kallman DA, Plato CC, Tobin JD. The role of muscle loss in the age-related decline of grip strength: cross-sectional and longitudinal perspectives. J Gerontol 45: M82-M88, 1990.
25. Kaprio J, Koskenvuo M. Genetic and environmental factors in complex diseases: the older Finnish Twin Cohort. Twin Res 5: 358-365, 2002.
26. Kaprio J, Sarna S, Koskenvuo M, Rantasalo I. The Finnish Twin Registry: formation and compilation, questionnaire study, zygosity determination procedures, and research program. Prog Clin Biol Res 24: 179-184, 1978.
27. Kenny AM, Kleppinger A, Wang Y, Prestwood KM. Effects of ultralow-dose estrogen therapy on muscle and physical function in older women. J Am Geriatr Soc 53: 1973-1977, 2005.
28. Kloosterboer HJ. Tibolone: a steroid with a tissue-specific mode of action. J Steroid Biochem Mol Biol 76: 231-238, 2001.
29. Kristensen K, Pedersen SB, Vestergaard P, Mosekilde L, Richelsen B. Hormone replacement therapy affects body composition and leptin differently in obese and non-obese postmenopausal women. J Endocrinol 163: 55-62, 1999.
30. Kujala UM, Kaprio J, Sarna S, Koskenvuo M. Relationship of leisure-time physical activity and mortality: the Finnish twin cohort. JAMA 279: 440-444, 1998.
31. Lamberts SW, van den Beld AW, van der Lely AJ. The endocrinology of aging. Science 278: 419-424, 1997.
32. Laustiola KE, Lassila R, Kaprio J, Koskenvuo M. Decreased beta-adrenergic receptor density and catecholamine response in male cigarette smokers. A study of monozygotic twin pairs discordant for smoking. Circulation 78: 1234-1240, 1988.
33. Lemoine S, Granier P, Tiffoche C, Rannou-Bekono F, Thieulant ML, Delamarche P. Estrogen receptor alpha mRNA in human skeletal muscles. Med Sci Sports Exerc 35: 439-443, 2003.
34. Meeuwsen IB, Samson MM, Duursma SA, Verhaar HJ. The effect of tibolone on fat mass, fat-free mass, and total body water in postmenopausal women. Endocrinology 142: 4813-4817, 2001.
35. Nelson RE, Grebe SK, OKane DJ, Singh RJ. Liquid chromatography-tandem mass spectrometry assay for simultaneous measurement of estradiol and estrone in human plasma. Clin Chem 50: 373-384, 2004.
36. Onambele NG, Skelton DA, Bruce SA, Woledge RC. Follow-up study of the benefits of hormone replacement therapy on isometric muscle strength of adductor pollicis in postmenopausal women. Clin Sci (Lond) 100: 421-422, 2001.
37. Pajala S, Era P, Koskenvuo M, Kaprio J, Alen M, Tolvanen A, Tiainen K, Rantanen T. Contribution of genetic and environmental factors to individual differences in maximal walking speed with and without second task in older women. J Gerontol A Biol Sci Med Sci 60: 1299-1303, 2005.
38. Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci (Lond) 84: 95-98, 1993.
39. Pietiläinen KH, Naukkarinen J, Rissanen A, Saharinen J, Ellonen P, Keränen H, Suomalainen A, Gotz A, Suortti T, Yki-Järvinen H, Oresic M, Kaprio J, Peltonen L.Global transcript profiles of fat in monozygotic twins discordant for BMI: pathways behind acquired obesity. PLoS Med 5: e51, 2008.
40. Pöllänen E, Ronkainen PH, Suominen H, Takala T, Koskinen S, Puolakka J, Sipilä S, Kovanen V. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res 10: 485-500, 2007.
41. Rantanen T, Era P, Heikkinen E. Physical activity and the changes in maximal isometric strength in men and women from the age of 75 to 80 years. J Am Geriatr Soc 45: 1439-1445, 1997.
42. Rantanen T, Era P, Heikkinen E. Maximal isometric strength and mobility among 75-year-old men and women. Age Ageing 23: 132-137, 1994.
43. Rantanen T, Guralnik JM, Ferrucci L, Penninx BW, Leveille S, Sipilä S, Fried LP. Coimpairments as predictors of severe walking disability in older women. J Am Geriatr Soc 49: 21-27, 2001.
44. Rantanen T, Guralnik JM, Foley D, Masaki K, Leveille S, Curb JD, White L. Midlife hand grip strength as a predictor of old age disability. JAMA 281: 558-560, 1999.
45. Rantanen T, Volpato S, Ferrucci L, Heikkinen E, Fried LP, Guralnik JM. Handgrip strength and cause-specific and total mortality in older disabled women: exploring the mechanism. J Am Geriatr Soc 51: 636-641, 2003.
46. Ribom EL, Piehl-Aulin K, Ljunghall S, Ljunggren O, Naessen T. Six months of hormone replacement therapy does not influence muscle strength in postmenopausal women. Maturitas 42: 225-231, 2002.
47. Samson MM, Meeuwsen IB, Crowe A, Dessens JA, Duursma SA, Verhaar HJ. Relationships between physical performance measures, age, height and body weight in healthy adults. Age Ageing 29: 235-242, 2000.
48. Seeley DG, Cauley JA, Grady D, Browner WS, Nevitt MC, Cummings SR. Is postmenopausal estrogen therapy associated with neuromuscular function or falling in elderly women? Study of Osteoporotic Fractures Research Group. Arch Intern Med 155: 293-299, 1995.
49. Sipilä S, Heikkinen E, Cheng S, Suominen H, Saari P, Kovanen V, Alen M, Rantanen T. Endogenous hormones, muscle strength, and risk of fall-related fractures in older women. J Gerontol A Biol Sci Med Sci 61: 92-96, 2006.
50. Sipilä S, Taaffe DR, Cheng S, Puolakka J, Toivanen J, Suominen H. Effects of hormone replacement therapy and high-impact physical exercise on skeletal muscle in post-menopausal women: a randomized placebo-controlled study. Clin Sci (Lond) 101: 147-157, 2001.
51. Sites CK, L'Hommedieu GD, Toth MJ, Brochu M, Cooper BC, Fairhurst PA. The effect of hormone replacement therapy on body composition, body fat distribution, and insulin sensitivity in menopausal women: a randomized, double-blind, placebo-controlled trial. J Clin Endocrinol Metab 90: 2701-2707, 2005.
52. Skelton DA, Greig CA, Davies JM, Young A. Strength, power and related functional ability of healthy people aged 65-89 years. Age Ageing 23: 371-377, 1994.
53. 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) 96: 357-364, 1999.
54. Taaffe DR, Newman AB, Haggerty CL, Colbert LH, de Rekeneire N, Visser M, Goodpaster BH, Nevitt MC, Tylavsky FA, Harris TB. Estrogen replacement, muscle composition, and physical function: the Health ABC Study. Med Sci Sports Exerc 37: 1741-1747, 2005.
55. Taaffe DR, Sipilä S, Cheng S, Puolakka J, Toivanen J, Suominen H. The effect of hormone replacement therapy and/or exercise on skeletal muscle attenuation in postmenopausal women: a yearlong intervention. Clin Physiol Funct Imaging 25: 297-304, 2005.
56. Tommaselli GA, Di Carlo C, Di Spiezio Sardo A, Bifulco G, Cirillo D, Guida M, Capasso R, Nappi C. Serum leptin levels and body composition in postmenopausal women treated with tibolone and raloxifene. Menopause 13: 660-668, 2006.
57. Turpeinen U, Linko S, Itkonen O, Hämäläinen E. Determination of testosterone in serum by liquid chromatography-tandem mass spectrometry. Scand J Clin Lab Invest 68: 50-57, 2008.
58. Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 84: 3666-3672, 1999.
59. Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci 60: 324-333, 2005.
60. Visser M, Harris TB, Langlois J, Hannan MT, Roubenoff R, Felson DT, Wilson PW, Kiel DP. Body fat and skeletal muscle mass in relation to physical disability in very old men and women of the Framingham Heart Study. J Gerontol A Biol Sci Med Sci 53: M214-M221, 1998.
61. Völgyi E, Tylavsky FA, Lyytikäinen A, Suominen H, Alen M, Cheng S. Assessing body composition with DXA and bioimpedance: effects of obesity, physical activity, and age. Obesity (Silver Spring) 16: 700-705, 2008.
62. von Bonsdorff M, Rantanen T, Laukkanen P, Suutama T, Heikkinen E. Mobility limitations and cognitive deficits as predictors of institutionalization among community-dwelling older people. Gerontology 52: 359-365, 2006.
63. Wiik A, Ekman M, Johansson O, Jansson E, Esbjörnsson M. Expression of both oestrogen receptor alpha and beta in human skeletal muscle tissue. Histochem Cell Biol 131: 181-189, 2009.
64. Wiik A, Glenmark B, Ekman M, Esbjornsson-Liljedahl M, Johansson O, Bodin K, Enmark E, Jansson E. Oestrogen receptor beta is expressed in adult human skeletal muscle both at the mRNA and protein level. Acta Physiol Scand 179: 381-387, 2003.
65. Woods D, Onambele G, Woledge R, Skelton D, Bruce S, Humphries SE, Montgomery H. Angiotensin-I converting enzyme genotype-dependent benefit from hormone replacement therapy in isometric muscle strength and bone mineral density. J Clin Endocrinol Metab 86: 2200-2204, 2001.
66. Zoico E, Di Francesco V, Guralnik JM, Mazzali G, Bortolani A, Guariento S, Sergi G, Bosello O, Zamboni M. Physical disability and muscular strength in relation to obesity and different body composition indexes in a sample of healthy elderly women. Int J Obes Relat Metab Disord 28: 234-241, 2004.