Osteoporosis International

, Volume 17, Issue 1, pp 61–67 | Cite as

Sarcopenia in premenopausal and postmenopausal women with osteopenia, osteoporosis and normal bone mineral density

  • Marianne C. Walsh
  • Gary R. Hunter
  • Margaret Barbara Livingstone
Original Article

Abstract

Sarcopenia, the decline of muscle mass with age, causes impaired gait, disability and falls. It may therefore increase the risk of fracture for osteoporotic women. The aims of this study were to determine the prevalence of sarcopenia in osteopenic and osteoporotic women, and to determine if hormone replacement therapy (HRT), diet, or physical activity (PA) has a role in the prevention of sarcopenia. One hundred and thirty-one premenopausal and 82 postmenopausal (54 taking HRT) healthy women (17–77 years) volunteered for the study. Body composition was measured by dual X-ray absorptiometry (DXA). Sarcopenia was defined as a relative skeletal muscle index (RSMI) (appendicular skeletal muscle mass divided by height) below 5.45 kg/m2. Osteopenia was defined by a densitometric t -score for bone mineral density (BMD) (g/cm2) below −1.0 and osteoporosis by a t -score below −2.5. Nutrient intake was assessed using 3-day food records and physical activity (PA) was measured using the Baecke Physical Activity Questionnaire. Pearson chi-squared, independent t -tests, simple correlation and multiple regression were used to analyze the data. In premenopausal osteopenic women the prevalence of sarcopenia was 12.5%. In postmenopausal women it was 25% for those with osteopenia, and 50% for those with osteoporosis. PA was independently related to RSMI (β=0.222, p =0.0001), but diet and HRT were not. After adjusting for PA, RSMI was not significantly related to BMD. These data suggest that the relationship between RSMI, BMD and risk of osteoporosis may largely be mediated through participation in PA. Sarcopenia screening simultaneous to BMD examinations by DXA, may be of value in identifying osteoporotic women with sarcopenia, a group that may be most in need of exercise interventions to increase muscle and BMD.

Keywords

Fracture risk HRT Osteopenia Osteoporosis Sarcopenia 

Abbreviations

BF

Body fat

BMC

Bone mineral content

BMD

Bone mineral density

DXA

Dual X-ray absorptiometry

FFM

Fat free mass

FM

Fat mass

LM

Lean mass

HRT

Hormone replacement therapy

PA

Physical activity

RSMI

Relative skeletal muscle index

References

  1. 1.
    Rosenberg IR, Roubenoff R (1995) Stalking sarcopenia. Ann Intern Med 123:727–728PubMedGoogle Scholar
  2. 2.
    Baumgartner RN, Koehler KM, Romero LJ, Lindeman RD, Garry PJ (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147:744-63Google Scholar
  3. 3.
    Janssen I, Heymsfield S, Wang Z, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 years. J Appl Physiol 89:81–88PubMedGoogle Scholar
  4. 4.
    Gallagher D, Ruts E, Visser M, Heshka, Baumgartner RN, Wang J, Pierson RN, Pi-Sunyer FX, Heymsfield SB (2000) Weight stability masks sarcopenia in elderly men and women. Am J Physiol Endocrinol Metab 279:E366–375PubMedGoogle Scholar
  5. 5.
    Martini G, Valenti R, Giovani S, Nuti R (1997) Age-related changes in body composition of healthy and osteoporotic women. Maturitas 27:25–33PubMedCrossRefGoogle Scholar
  6. 6.
    Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA (2002) Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 76:473–481PubMedGoogle Scholar
  7. 7.
    Kyle UG, Genton L, Hans D, Karsegard VL, Michel JP, Slosman DO, Pichard C (2001) Total body mass, fat mass, fat-free mass, and skeletal muscle in older people: cross-sectional differences in 60-year-old persons. J Am Geriatr Soc 49:1633–1640PubMedCrossRefGoogle Scholar
  8. 8.
    Iannuzzi-Sucich M, Prestwood KM, Kenny AM (2002) Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy older men and women. J Gerontol A Biol Sci Med Sci 57:M772–777PubMedGoogle Scholar
  9. 9.
    Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896PubMedCrossRefMathSciNetGoogle Scholar
  10. 10.
    Tankó LB, Movsesyan L, Mouritzen U, Christiansen C, Svendsen OL (2002) Appendicular lean tissue mass and the prevalence of sarcopenia among healthy women. Metabolism 51:69–74PubMedCrossRefGoogle Scholar
  11. 11.
    Looker AC, Orwoll ES, Johnston Jr CC, Lindsay RL, Wahner HW, Dunn WL, Calvo MS, Harris TB, Heyse SP (1997) Prevalence of low femoral bone density in older US adults from NHANES III. J Bone Miner Res 12:1769–1771PubMedCrossRefGoogle Scholar
  12. 12.
    Holt G, Khaw KT, Reid DM, Compston JE, Bhalla A, Woolf AD, Crabtree NJ, Dalzell N, Wardley-Smith B, Lunt M, Reeve J (2002) Prevalence of osteoporotic bone mineral density at the hip in Britain differs substantially from the US over 50 years of age: implications for clinical densitometry. Br J Radiol 75:736–742PubMedGoogle Scholar
  13. 13.
    US Department of Health and Human Services (2000) Healthy People 2010: understanding and improving health. US Government Printing Office, Washington DCGoogle Scholar
  14. 14.
    Aloia JF, McGowan GM, Vaswani AN, Ross P, Cohn GD (1991) Relationship of menopause to skeletal and muscle mass. Am J Clin Nutr 53:1378–1383PubMedGoogle Scholar
  15. 15.
    Ley CJ, Lees B, Stevenson JC (1992) Sex- and menopause-associated changes in body fat distribution. Am J Clin Nutr 55:950–954PubMedGoogle Scholar
  16. 16.
    Douchi T, Yamamoto S, Nackamura S (1998) The effect of menopause on regional and body lean mass. Maturitas 29:247–252PubMedCrossRefGoogle Scholar
  17. 17.
    Douchi T, Yamamoto S, Yoshimitsu N, Andoh T, Matsuo T, Nagata Y (2002) Relative contribution of aging and menopause to changes in lean and fat mass in segmental regions. Maturitas 42:301–306PubMedCrossRefGoogle Scholar
  18. 18.
    Douchi T, Oki T, Nakamura S, Ijuin H, Yamamoto S, Nagata Y (1997) The effect of body composition on bone density in pre- and post-menopausal women. Maturitas 27:55–60PubMedCrossRefGoogle Scholar
  19. 19.
    Visser M, Kiel DP, Langois J, Hannan MT, Felson DT, Wilson PW, Harris TB (1998) Muscle mass and fat mass in relation to bone mineral density in very old men and women: the Framingham Heart Study. Appl Radiat Isot 49:745–747PubMedCrossRefGoogle Scholar
  20. 20.
    Douchi T, Yamamoto S, Oki T, Maruta K, Kuwahata R, Nagata Y (2000) Relationship between body fat distribution and bone mineral density in premenopausal Japanese women. Obstet Gynecol 95:722–755PubMedCrossRefGoogle Scholar
  21. 21.
    Winters KM, Snow CM (2000) Body composition predicts bone mineral density and balance in premenopausal women. J Womens Health Gend Based Med 9:865–872PubMedCrossRefGoogle Scholar
  22. 22.
    Blain H, Vuillemin A, Teissier A, Hanesse B, Guillemin F, Jeandel C (2001) Influence of muscle strength and body weight and composition on regional bone mineral density in healthy women aged 60 years and over. Gerontology 47:207–212PubMedCrossRefGoogle Scholar
  23. 23.
    Bakker I, Twisk JW, Van Mechelen W, Kemper HC (2003) Fat-free body mass is the most important body composition determinant of 10-year longitudinal development of lumbar bone in adult men and women. J Clin Endocrinol Metab 88:2607–2613PubMedCrossRefGoogle Scholar
  24. 24.
    Gillette-Guyonnet S, Nourhashemi F, Laque S, Grandjean H, Vellas B (2000) Body composition and osteoporosis in elderly women. Gerontology 46:189–193PubMedCrossRefGoogle Scholar
  25. 25.
    Baecke JAH, Burema J, Frijters JER (1982) A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 36:936–942PubMedGoogle Scholar
  26. 26.
    Jacobs DR Jr, Ainsworth BE, Hartman TJ, Leon AS (1993) A simultaneous evaluation of 10 commonly used physical activity questionnaires. Med Sci Sports Exerc 25:81–91PubMedCrossRefGoogle Scholar
  27. 27.
    Philippaerts RM, Westerterp KR, Lefevre J (1999) Doubly labelled water validation of three physical activity questionnaires. Int J Sports Med 20:284–289PubMedCrossRefGoogle Scholar
  28. 28.
    Bonnefoy M, Normand S, Pachiaudi C, Lacour JR, Laville M, Kostka T (2001) Simultaneous validation of ten physical activity questionnaires in older men: a doubly labelled water study. J Am Geriatr Soc 49:28–35PubMedCrossRefGoogle Scholar
  29. 29.
    Newman AB, Kupelian V, Visser M, Simonsick E, Goodpaster B, Nevitt M, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB (2003) Sarcopenia: Alternative definitions and associations with lower extremity function. J Am Geriatr Soc 51:1602–1609PubMedCrossRefGoogle Scholar
  30. 30.
    Cummings SR, Bates D, Black DM (2002) Clinical use of bone densitometry: scientific review. JAMA 288:1889–1897PubMedCrossRefGoogle Scholar
  31. 31.
    Visser M, Fuerst T, Lang T, Salamone L, Harris T (1999) Validity of fan-beam dual X-ray absorptiometry for measuring the fat-free mass and leg muscle mass. J Appl Physiol 87:1513–1520PubMedGoogle Scholar
  32. 32.
    Burger H (2003) Hormone replacement therapy in the post-women’s health initiative era. Report of a meeting held in Funchal, Maderia, February 24–25, 2003. Climacteric 6[Suppl 1]:11–36Google Scholar
  33. 33.
    Austin P, Mamdani M, Tu K, Jaakkimainen L (2003) Prescriptions for estrogen replacement therapy in Ontario before and after publication of the Women’s Health Initiative Study. JAMA 289:3241–3242PubMedCrossRefGoogle Scholar
  34. 34.
    Sørensen MB, Rosenfalck AM, Højgaad L, Ottsen B (2001) Obesity and sarcopenia after menopause are reversed by sex hormone replacement therapy. Obes Res 9:622–626PubMedCrossRefGoogle Scholar
  35. 35.
    Kenny AM, Dawson L, Kleppinger A, Iannuzzi-Sucich, Judge JO (2003) Prevalence of sarcopenia and predictors of skeletal muscle mass in non-obese women who are long-term users of estrogen replacement therapy. J Gerontol A Biol Sci Med Sci 58A:436–440Google Scholar
  36. 36.
    Fiatarone MA, Marks E, Ryan N, Meredith C, Lipsitz, Evans W (1990) High intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 263:1038–1044CrossRefGoogle Scholar
  37. 37.
    Fiatarone Singh MA, Ding W, Manfredi TJ, Solares GS, O’Neill EF (1999) Insulin-like growth factor 1 in skeletal muscle after weight-lifting exercise in frail elders. Am J Physiol 277:E135–143PubMedGoogle Scholar
  38. 38.
    Hunter GR, Treuth MS (1995) Relative training intensity and increases in strength in older women. J Strength Cond Res 9:188–191CrossRefGoogle Scholar
  39. 39.
    Nelson M, Fiatarone MA, Morganti C, Trice I, Greenberg R, Evans W (1994) Effect of high intensity strength training on multiple risk factors for osteoporotic fracture. JAMA 272:1909–1914PubMedCrossRefGoogle Scholar
  40. 40.
    Kohrt W, Ehsani A, Birge S (1997) Effects of exercise involving predominantly either joint-reaction or ground-reaction forces on bone mineral density in older women. J Bone Miner Res 12:1253–1261PubMedCrossRefGoogle Scholar
  41. 41.
    Cussler E, Lohman T, Going S (2003) Weight lifted in strength training predicts bone change in postmenopausal women. Med Sci Sports Exerc 35:10–17PubMedCrossRefGoogle Scholar
  42. 42.
    Capozza RF, Cointry GR, Cure-Ramírez PC, Ferretti JL, Cure-Cure C (2004) A DXA study of muscle-bone relationships in the whole body and limbs of 2512 normal men and pre- and post-menopausal women. Bone 35:283–295PubMedCrossRefGoogle Scholar
  43. 43.
    American College of Sports Medicine (1998) Position stand: the recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness, and flexibility in healthy adults. Med Sci Sports Exerc 30:975–991PubMedCrossRefGoogle Scholar
  44. 44.
    Hunter GR, McCarthy JP, Bamman MM (2004) Effects of resistance training on older adults. Sports Med 34:329–348PubMedCrossRefGoogle Scholar
  45. 45.
    Friedman DR (2003) Are you doing all you can to fight sarcopenia? Tufts University Health and Nutrition Letter 21:1–5Google Scholar
  46. 46.
    Kerstetter JE, Looker AC, Insogna KL (2000) Low protein intake and low bone density. Calcif Tissue Int 66:313–321PubMedCrossRefGoogle Scholar
  47. 47.
    Kerstetter JE, O’Brien KO, Insogna KL (2003) Dietary protein, calcium metabolism, and skeletal homeostasis revisited. Am J Clin Nutr 78:584S–592SPubMedGoogle Scholar
  48. 48.
    Chiechi LM, Secreto G, D’Amore M, Fanelli E, Venturelli F, Cantatore F, Loizzi P (2002) Efficacy of a soy rich diet in preventing postmenopausal osteoporosis: the Menfis randomised trial. Maturitas 42:295–300PubMedCrossRefGoogle Scholar
  49. 49.
    Delmas PD (2002) Treatment of postmenopausal osteoporosis. Lancet 359:2018–2026PubMedCrossRefGoogle Scholar
  50. 50.
    Klesges RC, Eck LH, Melton MW, Fulliton W, Sommes GW, Hanson CL (1990) The accuracy of self reports of physical activity. Med Sci Sports Exerc 22:690–697PubMedCrossRefGoogle Scholar
  51. 51.
    Irwin MI, Ainsworth BE, Conway JM (2001) Estimation of energy expenditure from physical activity measures: Determinants of accuracy. Obes Res 9:517–525PubMedCrossRefGoogle Scholar
  52. 52.
    Hill RJ, Davies PSW (2001) The validity of self-reported energy intake as determined using the doubly labelled water technique. Br J Nutr 85:415–430PubMedCrossRefGoogle Scholar
  53. 53.
    Hebert JR, Patterson RE, Gorfine M, Ebbelling CB, Jeor ST, Chlebowski RT (2003) Differences between estimated calorie requirements and self-reported calorie intake in the Women’s Health Initiative. Ann Epidemiol 13:629–637PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2005

Authors and Affiliations

  • Marianne C. Walsh
    • 1
  • Gary R. Hunter
    • 2
    • 3
  • Margaret Barbara Livingstone
    • 1
  1. 1.Northern Ireland Centre for Diet and HealthUniversity of UlsterColeraine, Co. LondonderryUK
  2. 2.Division of Physiology and Metabolism, Departments of Human Studies and Nutritional SciencesUniversity of Alabama at BirminghamBirminghamUSA
  3. 3.Room 205 Education BuildingUniversity of Alabama at BirminghamBirminghamUSA

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