Osteoporosis International

, Volume 23, Issue 9, pp 2369–2379 | Cite as

Relative impact of neuromuscular and cardiovascular factors on bone strength index of the hemiparetic distal radius epiphysis among individuals with chronic stroke

  • M. Y. C. PangEmail author
  • A. Q. Cheng
  • D. E. Warburton
  • A. Y. M. Jones



The objective of this study was to examine the associations of neuromuscular and cardiovascular impairments with the bone strength index of the hemiparetic distal radius epiphysis in chronic stroke survivors. The results showed that grip strength is the most predominant predictor of the bone strength index.


The pupose of the study was to examine the associations of neuromuscular and cardiovascular impairments with the bone strength index of the hemiparetic distal radius epiphysis in chronic stroke survivors.


Sixty-five chronic stroke survivors and 34 healthy control subjects underwent scanning of the distal radius epiphyseal site on both sides using peripheral quantitative computed tomography to measure trabecular volumetric bone mineral density (vBMD) (mg/cm3), total vBMD (mg/cm3), total area (mm2), and compressive bone strength index (cBSI) (g2/cm4). Various indicators of neuromuscular (grip strength, spasticity) and cardiovascular function (vascular elasticity, oxygen consumption during 6-min walk test) were evaluated.


Analysis of variance revealed a significant main effect of side (p < 0.001) and group × side interaction (p < 0.05) for total BMC, total vBMD, trabecular vBMD, and cBSI (p < 0.05), with the stroke group showing greater side-to-side difference in these variables. However, no significant side-to-side difference in total area was detected in either group (p > 0.05). Sex-specific analysis yielded similar results. Multiple regression analyses revealed that the cBSI of the hemiparetic distal radius epiphysis had a stronger association with neuromuscular factors than cardiovascular factors. Overall, grip strength was the strongest determinant of the cBSI of the hemiparetic distal radius epiphysis (p < 0.01).


Muscle weakness is the most predominant determinant of cBSI in the hemiparetic distal radius epiphysis among chronic stroke patients. Future studies should investigate the efficacy of different muscle-strengthening strategies in enhancing bone strength of this skeletal site in the chronic stroke population.


Cerebrovascular accident Hemiplegia Muscle Osteoporosis Rehabilitation 



AQC was supported by a Research Studentship provided by the Hong Kong Polytechnic University. This study was supported by research grants from the Hong Kong Polytechnic University (87-SK), and Research Grants Council (General Research Fund no. 525607, no. 526708).

Conflicts of interest



  1. 1.
    Dennis MS, Lo KM, McDowall M, West T (2002) Fractures after stroke: frequency, types, and associations. Stroke 33:728–734PubMedCrossRefGoogle Scholar
  2. 2.
    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 9:269–275PubMedCrossRefGoogle Scholar
  3. 3.
    Jørgensen L, Jacobsen BK (2001) Functional status of the paretic arm affects the loss of bone mineral in the proximal humerus after stroke: a 1-year prospective study. Calcif Tissue Int 68:11–15PubMedCrossRefGoogle Scholar
  4. 4.
    Ashe MC, Fehling P, Eng JJ, Khan KM, McKay HA (2006) Bone geometric response to chronic disuse following stroke: a pQCT study. J Musculoskelet Neuronal Interact 6:226–233PubMedGoogle Scholar
  5. 5.
    Pang MYC, Ashe MA, Eng JJ (2007) Muscle weakness, spasticity and disuse contribute to demineralization and geometric changes in the radius following chronic stroke. Osteoporos Int 18:1243–1252PubMedCrossRefGoogle Scholar
  6. 6.
    Lazoura O, Groumas N, Antoniadou E, Papadaki PJ, Papadimitriou A, Thriskos P, Fezoulidis I, Vlychou M (2008) Bone mineral density alterations in upper and lower extremities 12 months after stroke measured by peripheral quantitative computed tomography and DXA. J Clin Densitom 11:511–517PubMedCrossRefGoogle Scholar
  7. 7.
    Pang MYC, Ashe MA, Eng JJ (2008) Tibial bone geometry in chronic stroke patients: influence of sex, cardiovascular health, and muscle mass. J Bone Miner Res 23:1023–1030PubMedCrossRefGoogle Scholar
  8. 8.
    Pang MY, Ashe MC, Eng JJ (2010) Compromised bone strength index in the hemiparetic distal tibia epiphysis among chronic stroke patients: the association with cardiovascular function, muscle atrophy, mobility, and spasticity. Osteoporos Int 21:997–1007PubMedCrossRefGoogle Scholar
  9. 9.
    Kopunek SP, Michael KM, Shaughnessy M, Resnick B, Nahm ES, Whitall J, Goldberg A, Macko RF (2007) Cardiovascular risk in survivors of stroke. Am J Prev Med 32:408–412PubMedCrossRefGoogle Scholar
  10. 10.
    MacKay-Lyons MJ, Makrides L (2004) Longitudinal changes in exercise capacity after stroke. Arch Phys Med Rehabil 85:1608–1612PubMedCrossRefGoogle Scholar
  11. 11.
    Whitney C, Warburton ER, Frohlich J, Chan SY, McKay H, Khan K (2004) Are cardiovascular disease and osteoporosis directly linked? Sports Med 34:779–807PubMedCrossRefGoogle Scholar
  12. 12.
    Farhat GN, Cauley IA, Matthews KA, Newman AB, Johnston J, Mackey R, Edmundowicz D, Sutton-Tyrrell K (2006) Volumetric BMD and vascular calcification in middle-aged women: the study of women’s health across the nation. J Bone Miner Res 21:1839–1846PubMedCrossRefGoogle Scholar
  13. 13.
    Naves M, Rodríguez-García M, Díaz-López JB, Gómez-Alonso C, Cannata-Andía JB (2008) Progression of vascular calcifications is associated with greater bone loss and increased bone fractures. Osteoporos Int 19:1161–1166PubMedCrossRefGoogle Scholar
  14. 14.
    Griffith JF, Yeung DK, Tsang PH, Choi KC, Kwok TC, Ahuja AT, Leung KS, Leung PC (2008) Compromised bone marrow perfusion in osteoporosis. J Bone Miner Res 23:1068–1075PubMedCrossRefGoogle Scholar
  15. 15.
    Nakayama H, Jorgensen HS, Raaschou HO, Olsen TS (1994) Recovery of upper extremity function in stroke patients: the Copenhagen stroke study. Arch Phys Med Rehabil 75:394–398PubMedCrossRefGoogle Scholar
  16. 16.
    The Government of the Hong Kong Special Administrative Region (2011) Hong Kong Statistics. Accessed 20 October 2011
  17. 17.
    Washburn RA, Smith KW, Jette AM, Janney CA (1993) The physical activity scale for the elderly (PASE): development and evaluation. J Clin Epidemiol 46:153–162PubMedCrossRefGoogle Scholar
  18. 18.
    Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vuori L (2002) Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: a peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res 17:2281–2289PubMedCrossRefGoogle Scholar
  19. 19.
    Macdonald HM, Kontulainen S, Petit M, Janssen P, McKay H (2006) Bone strength and its determinants in pre-and early pubertal boys and girls. Bone 39:598–608PubMedCrossRefGoogle Scholar
  20. 20.
    Kontulainen SA, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA (2008) Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 8:401–409PubMedGoogle Scholar
  21. 21.
    Di Monaco M, Di Monaco R, Manca M, Cavanna A (2000) Handgrip strength is an independent predictor of distal radius bone mineral density in postmenopausal women. Clin Rheumatol 19:473–476PubMedCrossRefGoogle Scholar
  22. 22.
    Frank AW, Lorbergs AL, Chilibeck PD, Farthing JP, Kontulainen SA (2010) Muscle cross sectional area and grip torque contraction types are similarly related to pQCT derived bone strength indices in the radii of older healthy adults. J Musculoskelet Neuronal Interact 10:136–141PubMedGoogle Scholar
  23. 23.
    De Zepetnek JOT, Craven BC, Giangregorio LM (2011) An evaluation of the muscle-bone unit theory among individuals with spinal cord injury. Spinal Cord. doi: 10.1038/sc.2011.99
  24. 24.
    Patten C, Lexell J, Brown HE (2004) Weakness and strength training in persons with poststroke hemiplegia: rationale, method, and efficacy. J Rehabil Res Dev 41:293–312PubMedCrossRefGoogle Scholar
  25. 25.
    Harris JE, Eng JJ (2007) Paretic upper-limb strength best explains arm activity in people with stroke. Phys Ther 87:88–97PubMedCrossRefGoogle Scholar
  26. 26.
    Boissy P, Bourbonnais D, Carlotti MM, Gravel D, Arsenault BA (1999) Maximal grip force in chronic stroke subjects and its relationship to global upper extremity function. Clin Rehabil 13:354–362PubMedCrossRefGoogle Scholar
  27. 27.
    Watkins CL, Leathley MJ, Gregson JM, Moore AP, Smith TL, Sharma AK (2002) Prevalence of spasticity post stroke. Clin Rehabil 16:515–522PubMedCrossRefGoogle Scholar
  28. 28.
    Pandyan AD, Johnson GR, Price CI, Curless RH, Barnes MP, Rodgers H (1999) A review of the properties and limitations of the Ashworth and modified Ashworth scales as measures of spasticity. Clin Rehabil 13:373–383PubMedCrossRefGoogle Scholar
  29. 29.
    Cameron JD, Rajkumar C, Kingwell BA, Jennings GL, Dart AM (1999) Higher systemic arterial compliance is associated with greater exercise time and lower blood pressure in a young older population. J Am Geriatr Soc 47:653–656PubMedGoogle Scholar
  30. 30.
    Agabiti-Rosei E, Muiesan ML (2007) Carotid atherosclerosis, arterial stiffness and stroke events. Adv Cardiol 44:173–186PubMedCrossRefGoogle Scholar
  31. 31.
    HDI Hypertension Diagnostics Inc (2005) HDI/PulseWaveTM CR-2000 Research cardiovascular profiling system manual. HDI Hypertension Diagnostics Inc, EaganGoogle Scholar
  32. 32.
    Zimlichman R, Shargorodsky M, Boaz M, Duprez D, Rahn KH, Rizzoni D, Payeras AC, Hamm C, McVeigh G (2005) Determination of arterial compliance using blood pressure waveform analysis with the CR-2000: reliability, repeatability, and establishment of normal values for healthy European population—the seven European sites study (SESS). Am J Hypertens 18:65–71PubMedCrossRefGoogle Scholar
  33. 33.
    Duprez DA, De Buyzere MM, De Bruyne L, Clement DL, Cohn JN (2001) Small and large artery elasticity indices in peripheral arterial occlusive disease (PAOD). Vasc Med 6:211–214PubMedCrossRefGoogle Scholar
  34. 34.
    Wilson AM, O’Neal D, Nelson CL, Prior DL, Best JD, Jenkins AJ (2004) Comparison of arterial assessments in low and high vascular disease risk groups. Am J Hypertens 17:285–291PubMedCrossRefGoogle Scholar
  35. 35.
    Syeda B, Gottsauner-Wolf M, Denk S, Pichler P, Khorsand A, Glogar D (2003) Arterial compliance: a diagnostic marker for atherosclerotic plaque burden? Am J Hypertens 16:356–362PubMedCrossRefGoogle Scholar
  36. 36.
    Tang A, Sibley KM, Thomas SG, McIlroy WE, Brooks D (2006) Maximal exercise test results in subacute stroke. Arch Phys Med Rehabil 87:1100–1105PubMedCrossRefGoogle Scholar
  37. 37.
    Nieman DC, Austin MD, Benezra L, Pearce S, McInnis T, Unick J, Gross SJ (2006) Validation of Cosmed's FitMate in measuring oxygen consumption and estimating resting metabolic rate. Res Sports Med 14:89–96PubMedGoogle Scholar
  38. 38.
    Eng JJ, Dawson AS, Chu KS (2004) Submaximal exercise in persons with stroke: test-retest reliability and concurrent validity with maximal oxygen consumption. Arch Phys Med Rehabil 85:113–118PubMedCrossRefGoogle Scholar
  39. 39.
    Riggs LB, Melton LJ III, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S (2004) A population-based study of age and sex differences in bone volumetric density, size, geometry and structure at different skeletal sites. J Bone Miner Res 19:1945–1954PubMedCrossRefGoogle Scholar
  40. 40.
    Schoenau E (2005) From mechanostat theory to development of the functional muscle-bone-unit. J Musculoskelet Neuronal Interact 5:232–238PubMedGoogle Scholar
  41. 41.
    MacIntyre NJ, Rombough R, Brouwer B (2010) Relationships between calf muscle density and muscle strength, mobility and bone status in the stroke survivors with subacute and chronic lower limb hemiparesis. J Musculoskelet Neuronal Interact 10:249–255PubMedGoogle Scholar
  42. 42.
    Colebatch JG, Gandevia SC (1989) The distribution of muscular weakness in upper motor neuron lesions affecting the arm. Brain 112:749–763PubMedCrossRefGoogle Scholar
  43. 43.
    Michael KM, Allen JK, Macko RF (2005) Reduced ambulatory activity after stroke: the role of balance, gait, and cardiovascular fitness. Arch Phys Med Rehabil 86:1552–1556PubMedCrossRefGoogle Scholar
  44. 44.
    Adami S, Gatti D, Braga V, Bianchini D, Rossini M (1999) Site-specific effects of strength training on bone structure and geometry of ultradistal radius in postmenopausal women. J Bone Miner Res 14:120–124PubMedCrossRefGoogle Scholar
  45. 45.
    Hangartner TN, Gilsanz V (1996) Evaluation of cortical bone by computed tomography. J Bone Miner Res 11:1518–1525PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2012

Authors and Affiliations

  • M. Y. C. Pang
    • 1
    Email author
  • A. Q. Cheng
    • 1
  • D. E. Warburton
    • 2
  • A. Y. M. Jones
    • 1
  1. 1.Department of Rehabilitation SciencesHong Kong Polytechnic UniversityHung HomChina
  2. 2.Cardiovascular Physiology and Rehabilitation LaboratoryUniversity of British ColumbiaVancouverCanada

Personalised recommendations