Osteoporosis International

, Volume 16, Issue 12, pp 1769–1779

Reduced hip bone mineral density is related to physical fitness and leg lean mass in ambulatory individuals with chronic stroke

  • Marco Y. C. Pang
  • Janice J. Eng
  • Heather A. McKay
  • Andrew S. Dawson
Original Article

Abstract

Following a stroke, the reduced level of physical activity and functional use of the paretic leg may lead to bone loss and muscle atrophy. These factors and the high incidence of falls may contribute to hip fractures in the stroke population. This study was the first to examine total proximal femur bone mineral content (BMC) and bone mineral density (BMD) and their relationship to stroke-specific impairments in ambulatory individuals with chronic stroke (onset >1 year). We utilized dual-energy X-ray absorptiometry (DXA) to acquire proximal femur and total body scans on 58 (23 women) community-dwelling individuals with chronic stroke. We reported total proximal femur BMC (g) and BMD (g/cm2) derived from the proximal femur scans, and lean mass (g) and fat mass (g) for each leg derived from the total body scans. Each subject was evaluated for ambulatory capacity (Six-Minute Walk Test), knee extension strength (hand-held dynamometry), physical fitness [maximal oxygen uptake (VO2max)] and spasticity (Modified Ashworth Scale). Results showed that the paretic leg had significantly lower proximal femur BMD, lean mass and percent lean mass, but higher fat mass than the non-paretic leg for both men and women. Proximal femur BMD of the paretic leg was significantly related to ambulatory capacity ( r =0.33, P =0.011), muscle strength ( r =0.39, P =0.002), physical fitness ( r =0.57, P <0.001), but not related to spasticity ( r =−0.23, P =0.080). Multiple regression analysis showed that lean mass in the paretic leg was a major predictor ( r 2=0.371, P <0.001) of the paretic proximal femur BMD. VO2max was a significant predictor of both paretic proximal femur BMD ( r 2=0.325, P <0.001) and lean mass in the paretic leg ( r 2=0.700, P <0.001). Further study is required to determine whether increasing physical fitness and lean mass are important to improve hip bone health in chronic stroke.

Keywords

Aerobic capacity Cerebrovascular accident Osteoporosis Physical activity Rehabilitation 

References

  1. 1.
    Forster A, Young J (1995) Incidence and consequences of falls due to stroke: a systematic injury. BMJ 311:83–86PubMedGoogle Scholar
  2. 2.
    Jorgensen L, Engstad T, Jacobsen BK (2002) Higher incidence of falls in long-term stroke survivors than in population controls. Depressive symptoms predict falls after stroke. Stroke 33:542–547CrossRefPubMedGoogle Scholar
  3. 3.
    Cheng PT, Liaw MY, Wong MK, Tang FT, Lee MY, Lin PS (1998) The sit-to-stand movement in stroke patients and its correlation with falling. Arch Phys Med Rehabil 79:1043–1046CrossRefPubMedGoogle Scholar
  4. 4.
    Lamb SE, Ferrucci L, Volapto S, Fried LP, Guralnik JM (2003) Risk factors for falling in home-dwelling older women with stroke. The women’s health and aging study. Stroke 34:494–501CrossRefGoogle Scholar
  5. 5.
    Teasell R, McRae M, Foley N, Bhardwaj A (2002) The incidence and consequences of falls in stroke patients during inpatient rehabilitation: factors associated with high risk. Arch Phys Med Rehabil 83:329–333CrossRefPubMedGoogle Scholar
  6. 6.
    Iversen E, Hassager C, Christiansen C (1989) The effect of hemiplegia on bone mass and soft tissue body composition. Acta Neurol Scand 79:155–159PubMedGoogle Scholar
  7. 7.
    Jorgensen L, Jacobsen BK (2001) Changes in muscle mass, fat mass and bone mineral content in the legs after stroke: a 1 year prospective study. Bone 28:655–659CrossRefPubMedGoogle Scholar
  8. 8.
    Poole KE, Reeve J, Warburton EA (2002) Falls, fractures and osteoporosis after stroke: time to think about protection? Stroke 33:1432–1436CrossRefPubMedGoogle Scholar
  9. 9.
    Ramnemark A, Nyberg L, Lorentzon R, Olsson T, Gustafson Y (1999) Hemiosteoporosis after severe stroke, independent of changes in body composition and weight. Stroke 30:755–760PubMedGoogle Scholar
  10. 10.
    Ramnemark A, Nyberg L, Borssen B, Olsson T, Gustafson Y (1998) Fractures after stroke. Osteoporos Int 8:92–95CrossRefPubMedGoogle Scholar
  11. 11.
    Ramnemark A, Nilsson M, Borssen B, Gustafson Y (2000) Stroke, a major and increasing risk factor for femoral neck fractures. Stroke 31:1572–1577PubMedGoogle Scholar
  12. 12.
    Prince RL, Price RI, Ho S (1988) Forearm bone loss in hemiplegia: a model for the study of immobilization osteoporosis. J Bone Miner Res 3:305–310PubMedGoogle Scholar
  13. 13.
    Giangregorio L, Blimkie CJR (2002) Skeletal adaptations to alterations in weight-bearing activity. A comparison of models of disuse osteoporosis. Sports Med 32:459–476PubMedGoogle Scholar
  14. 14.
    Frost HM, Ferretti JL, Jee WSS (1998) Perspectives: some roles of mechanical usage, muscle strength, and the mechanostat in skeletal physiology, disease, and research. Calcif Tissue Int 62:1–7CrossRefPubMedGoogle Scholar
  15. 15.
    Del Puente A, Pappone N, Mandes MG, Mantova D, Scarpa R, Oriente P (1996) Determinants of bone mineral density in immobilization: a study on hemiplegic patients. Osteoporos Int 6:50–54CrossRefPubMedGoogle Scholar
  16. 16.
    Ramnemark A, Nyberg L, Lorentzon R, Englund U, Gustafson Y (1999) Progressive hemiosteoporosis on the paretic side and increased bone mineral density in the nonparetic arm the first year after severe stroke. Osteoporos Int 9:269–275CrossRefPubMedGoogle Scholar
  17. 17.
    Gresham GE, Fitzpatrick TE, Wolf PA, McNamara PM, Kannel WB, Dawber TR (1975) Residual disability in survivors of stroke—The Framingham Study. N Eng J Med 293:954–956Google Scholar
  18. 18.
    Hyndman D, Ashburn A, Stack E (2002) Fall events among people with stroke living in the community: circumstances of falls and characteristics of fallers. Arch Phys Med Rehabil 83:165–170CrossRefPubMedGoogle Scholar
  19. 19.
    Nyberg L, Gustafson Y (1997) Fall prediction index for patients in stroke rehabilitation. Stroke 28:716–721PubMedGoogle Scholar
  20. 20.
    Jorgensen L, Jacobsen BK, Wilsgaard T, Magnus JH (2000) Walking after stroke: does it matter? Changes in bone mineral density within the first 12 months after stroke. A longitudinal study. Osteoporos Int 11:381–387CrossRefPubMedGoogle Scholar
  21. 21.
    Iwamoto J, Tsukimura T, Takeda T (1999) Bone mineral density of metatarsus in hemiplegic subjects. Am J Phys Med Rehabil 78:202–207CrossRefPubMedGoogle Scholar
  22. 22.
    Sahin L, Ozoran K, Gunduz OH, Ucan H, Yucel M (2001) Bone mineral density in patients with stroke. Am J Phys Med Rehabil 80:592–596CrossRefPubMedGoogle Scholar
  23. 23.
    Takamoto A, Masuyama T, Nakajima M, Sekiya K, Kosaka H, Morimoto S, Ogihara T, Onishi T (1995) Alterations of bone mineral density of the femurs in hemiplegia. Calcif Tissue Int 56:259–262CrossRefPubMedGoogle Scholar
  24. 24.
    Turner CH, Robling AG (2003) Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev 31:45–50CrossRefPubMedGoogle Scholar
  25. 25.
    Nevitt M (1994) Bone mineral density predicts non-spine fractures in very elderly women. Osteoporos Int 4:235–241CrossRefGoogle Scholar
  26. 26.
    Schott AM, Cormier C, Hans D, Favier F, Hausherr E, Dargent-Molina P, Delmas PD, Ribot C, Sebert JL, Breart G, Meunier PJ (1998) How hip and whole body bone mineral density predict hip fracture in elderly women: the EPIDOS Prospective Study. Osteoporos Int 8:247–254CrossRefPubMedGoogle Scholar
  27. 27.
    Fraul F, Erdfelder E (1992) G POWER: a priori, post-hoc and compromise analysis: for MS-DOS (computer program). Department of Psychology, Bonn University, Bonn, GermanyGoogle Scholar
  28. 28.
    Folstein MF, Folstein, SE, McHugh PR (1975) Mini-Mental State: a practical method for grading the state of patients for the clinician. J Psychiat Res 12:189–198CrossRefPubMedGoogle Scholar
  29. 29.
    Eng JJ, Chu KS, Dawson AS, Kim CM, Hepburn KE (2002) Functional walk tests in individuals with stroke. Relation to perceived exertion and myocardial exertion. Stroke 33:756–761CrossRefPubMedGoogle Scholar
  30. 30.
    American Thoracic Society (2002) ATS Statement: Guidelines for the Six-Minute Walk Test. Am J Respir Crit Care Med 166:111–117PubMedGoogle Scholar
  31. 31.
    Kim CM, Eng JJ (2003) The relationship of lower-extremity muscle torque to locomotor performance in people with stroke. Phys Ther 83:49–57PubMedGoogle Scholar
  32. 32.
    Bohannon RW (1997) Measurement and nature of muscle strength in patients with stroke. J Neuro Rehabil 11:115–25Google Scholar
  33. 33.
    Nguyen TV, Center JR, Eisman JA (2000) Osteoporosis in elderly men and women: effects of dietary calcium, physical activity, and body mass index. J Bone Miner Res 15:322–331PubMedGoogle Scholar
  34. 34.
    Uusi-Rasi K, Sievanen H, Pasanen M, Oja P, Vuori I (2001) Maintenance of body weight, physical activity and calcium intake helps preserve bone mass in elderly women. Osteoporos Int 12:373–379CrossRefPubMedGoogle Scholar
  35. 35.
    American College of Sports Medicine (2000) ACSM’s guidelines for exercise testing and prescription, 6th edn. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  36. 36.
    Berthouze SE, Minaire PM, Castells J, Busso T, Vico L, Lacour J-R (1995) Relationship between mean habitual daily energy expenditure and maximal oxygen uptake. Med Sci Sports Exerc 27:1170–1179PubMedGoogle Scholar
  37. 37.
    Potempa K, Lopez M, Braun LT, Szidon JP, Fogg L, Tincknell T (1995) Physiological outcomes of aerobic exercise training in hemiparetic stroke patients. Stroke 26:101–105PubMedGoogle Scholar
  38. 38.
    Howley ET, Bassett DR, Welch HG (1995) Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 27:1292–1301PubMedGoogle Scholar
  39. 39.
    Hsu A-L, Tang P-F, Jan M-H (2003) Analysis of impairments influencing gait velocity and asymmetry of hemiplegic patients after mild and moderate stroke. Arch Phys Med Rehabil 84:1185–1193CrossRefPubMedGoogle Scholar
  40. 40.
    Bohannon BW, Smith MB (1987) Interrater reliability of a Modified Ashworth Scale of muscle spasticity. Phys Ther 67:206–207PubMedGoogle Scholar
  41. 41.
    Looker AC, Orwall ES, Johnston Jr CC, Lindsay RL, Wahner HW, Dunn WL, Calvo MS, Harris TB, Heyse SP (1997) Prevalence of low bone density in older US adults from NHANES III. J Bone Miner Res 12:1761–1768PubMedGoogle Scholar
  42. 42.
    Kanis JA, Gluer C-C (2000) An update on the diagnosis and assessment of osteoporosis with densitometry. Osteoporos Int 11:192–202CrossRefPubMedGoogle Scholar
  43. 43.
    Leib ES, Lewiecki EM, Binkley N, Hamdy RC (2004) Official positions of the International Society for Clinical Densitometry. J Clin Densitom 7:1–6CrossRefPubMedGoogle Scholar
  44. 44.
    Looker, AC, Wahner HW, Dunn WL, Calvo MS, Harris TB, Heyse SP, Johnston CC, Lindsay R (1998) Updated data on proximal femur bone mineral levels of US adults. Osteoporos Int 8:468–489CrossRefPubMedGoogle Scholar
  45. 45.
    Warming L, Hassager C, Christiansen C (2002) Changes in bone mineral density with age in men and women: a longitudinal study. Osteoporos Int 13:105–112CrossRefPubMedGoogle Scholar
  46. 46.
    Kim CM, Eng JJ (2003) Symmetry in vertical ground reaction force is accompanied by symmetry in temporal but not distance variables of gait in persons with stroke. Gait Posture 8:23–28CrossRefGoogle Scholar
  47. 47.
    Jorgensen L, Crabtree NJ, Reeve J, Jacobsen BK (2000) Ambulatory level and asymmetrical weight bearing after stroke affects bone loss in the upper and lower part of the femoral neck differently: bone adaptation after decreased mechanical loading. Bone 27:701–707CrossRefPubMedGoogle Scholar
  48. 48.
    De Laet CEDH, van der Klift M, Hofman A, Pols HAP (2002) Osteoporosis in men and women: a story about bone mineral density thresholds and hip fracture risk. J Bone Miner Res 17:2231–2236PubMedGoogle Scholar
  49. 49.
    White HC. Post-stroke hip fractures (1988) Arch Orthop Trauma Surg 107:345–347CrossRefPubMedGoogle Scholar
  50. 50.
    Hamdy RC, Krishnaswamy G, Cancellaro V, Whalen K, Harvill L (1993) Changes in bone mineral content and density after stroke. Am J Phys Med Rehabil 72:188–191PubMedGoogle Scholar
  51. 51.
    Liu M, Tsuji T, Higuchi Y, Domen K, Tsujiuchi K, Chino N (1999) Osteoporosis in hemiplegic stroke patients as studied with dual-energy X-ray absorptiometry. Arch Phys Med Rehabil 80:1219–1226CrossRefPubMedGoogle Scholar
  52. 52.
    Yavuzer G, Ataman S, Sulder N, Mesut A (2002) Bone mineral density in patients with stroke. Int J Rehabil Res 25:235–239CrossRefPubMedGoogle Scholar
  53. 53.
    Faulkner H, Munz M, Scherrer M (1997) Bone mineral density of opposing hips using dual energy X-ray absorptiometry in single-beam and fan-beam design. Calcif Tissue Int 61:445–447CrossRefPubMedGoogle Scholar
  54. 54.
    Mazess RB, Nord RH, Hanson JA, Barden HS (2000) Bilateral measurement of femoral bone mineral density. J Clin Densitom 3:133–140CrossRefPubMedGoogle Scholar
  55. 55.
    Ryan AS, Dobrovolny L, Smith GV, Silver KH, Macko RF (2002) Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil 83:1703–1707CrossRefPubMedGoogle Scholar
  56. 56.
    Chen Z, Lohman TG, Stini WA, Ritenbaugh C, Aickin M (1997) Fat or lean mass: which one is the major determinant of bone mineral mass in healthy postmenopausal women? J Bone Miner Res 12:144–151PubMedGoogle Scholar
  57. 57.
    Van Langendonck L, Claessens AL, Lefevre J, Thomis M, Philippaerts R, Delvaux K, Lysens R, Vanden Eynde B, Beunen G (2002) Association between bone mineral density (DXA), body structure, and body composition in middle-aged men. Am J Human Biol 14:735–742CrossRefGoogle Scholar
  58. 58.
    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 or older. Gerontology 47:207–212CrossRefPubMedGoogle Scholar
  59. 59.
    Pluijim SM, Visser M, Smit JH, Popp-Snijders C, Roos JC, Lips P (2001) Determinants of bone mineral density in older men and women: body composition as mediator. J Bone Miner Res 16:2142–2151PubMedGoogle Scholar
  60. 60.
    Vico L, Pouget JF, Calmels P, Chatard JC, Rehailia M, Minaire P, Geyssant A, Alexandre C (1995) The relations between physical ability and bone mass in women aged over 65 years. J Bone Miner Res 10:374–383PubMedGoogle Scholar
  61. 61.
    Hughes VA, Frontera WR, Dallal GE, Lutz KJ, Fisher EC, Evans WJ (1995) Muscle strength and body composition associations with bone density in older subjects. Med Sci Sports Exerc 27:967–974PubMedGoogle Scholar
  62. 62.
    Winter DA (1991) Biomechanics and motor control of human gait: normal, elderly and pathological, 2nd edn. Waterloo Biomechanics, Waterloo, CanadaGoogle Scholar
  63. 63.
    Wilmet E, Ismail AA, Heilporn A, Welraeds D, Bergmann P (1995) Longitudinal study of the bone mineral content and of soft tissue composition after spinal cord section. Paraplegia 33:674–677PubMedGoogle Scholar
  64. 64.
    Ross PD, He Y-F, Yates AJ, Coupland C, Ravn P, McClung M, Thompson D, Wasnich RD (1996) Body size accounts for most differences in bone density between Asian and Caucasian women. Calcif Tissue Int 59:339–343CrossRefPubMedGoogle Scholar
  65. 65.
    Russell-Aulet M, Wang J, Thornton J, Colt EWD, Pierson RN (1991) Bone mineral density and mass by total-body dual-photon absorptiometry in normal white and Asian men. J Bone Miner Res 10:1109–1113Google Scholar
  66. 66.
    Wu XP, Liao EY, Huang G, Dai RC, Zhang H (2003) A comparison study of the reference curves of bone mineral density at different skeletal sites in native Chinese, Japanese, and American Caucasian women. Calcif Tissue Int 73:122–132PubMedGoogle Scholar
  67. 67.
    Frost HM (2003) Absorptiometry and “osteoporosis”: problems. J Bone Miner Metab 21:255–260CrossRefPubMedGoogle Scholar
  68. 68.
    Ryan AS, Ivey FM, Hurlbut DE, Martel GF, Lemmer JT, Sorkin JD, Metter EJ, Fleg JL, Hurley BF (2004) Regional bone mineral density after resistive training in young and older men and women. Scand J Med Sci Sports14:16–23CrossRefGoogle Scholar
  69. 69.
    Chien MY, Wu YT, Hsu AT, Yang RS, Lai JS (2000) Efficacy of a 24-week aerobic exercise program for osteopenic postmenopausal women. Calcif Tissue Int 67:443–448CrossRefPubMedGoogle Scholar
  70. 70.
    Kemmler W, Lauber D, Weineck J, Hensen J, Kalender W, Engelke K (2004) Benefits of 2 years of intense exercise on bone density, physical fitness, and blood lipids in early postmenopausal osteopenic women; results of the Erlangen Fitness Osteoporosis Prevention Study (EFOPS). Arch Int Med 164:1084–1091CrossRefGoogle Scholar
  71. 71.
    Kerr D, Ackland T, Maslen B, Morton A, Prince R (2001) Resistance training over 2 years increases bone mass in calcium-replete postmenopausal women. J Bone Miner Res 16:175–181PubMedGoogle Scholar
  72. 72.
    Ryan AS, Treuth MS, Hunter GR, Elahi D (1998) Positive training maintains bone mineral density in postmenopausal women. Calcif Tissue Int 62:295–299CrossRefPubMedGoogle Scholar
  73. 73.
    Vincent KR, Braith RW (2002) Resistance exercise and bone turnover in elderly men and women. Med Sci Sports Exerc 34:17–23CrossRefPubMedGoogle Scholar
  74. 74.
    Melton III LJ (2001) The prevalence of osteoporosis: gender and racial comparison. Calcif Tissu Int 69:179–181CrossRefGoogle Scholar
  75. 75.
    Tanaka N, Sonoda S, Kondo K, Chino N (1997) Reproducibility of dual-energy X-ray absorptiometry in the upper extremities in stroke patients. Disabil Rehabil 19:523–527PubMedGoogle Scholar
  76. 76.
    Going SB, Massett MP, Hall MC, Bare LA, Root PA, Williams DP, Lohman TG (1993) Detection of small changes in body composition by dual-energy X-ray absorptiometry. Am J Clin Nutr 57:845–850PubMedGoogle Scholar
  77. 77.
    Gibberd FB, Gould SR, Marks P (1976) Incidence of deep vein thrombosis and leg oedema in patients with strokes. J Neurol Neurosurg Psychiatry 39:1222–1225PubMedGoogle Scholar
  78. 78.
    Tothill P, Laskey MA, Orphanidou CI, van Wijk M (1999) Anomalies in dual-energy X-ray absorptiometry measurements of total-body mineral during weight change using Lunar, Hologic and Norland instruments. Br J Radiol 72:661–669PubMedGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2005

Authors and Affiliations

  • Marco Y. C. Pang
    • 1
    • 2
  • Janice J. Eng
    • 1
    • 2
  • Heather A. McKay
    • 3
    • 4
  • Andrew S. Dawson
    • 2
    • 5
  1. 1.School of Rehabilitation SciencesUniversity of British ColumbiaVancouverCanada
  2. 2.Rehabilitation Research LaboratoryGF Strong CenterVancouverCanada
  3. 3.Department of OrthopedicsUniversity of British ColumbiaVancouverCanada
  4. 4.Department of Family PracticeUniversity of British ColumbiaVancouverCanada
  5. 5.Acquired Brain Injury ProgramGF Strong CenterVancouverCanada

Personalised recommendations