Skip to main content

Advertisement

Log in

Effect of chronic activity-based therapy on bone mineral density and bone turnover in persons with spinal cord injury

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

Osteoporosis is a severe complication of spinal cord injury (SCI). Many exercise modalities are used to slow bone loss, yet their efficacy is equivocal. This study examined the effect of activity-based therapy (ABT) targeting the lower extremities on bone health in individuals with SCI.

Methods

Thirteen men and women with SCI (age and injury duration = 29.7 ± 7.8 and 1.9 ± 2.7 years) underwent 6 months of ABT. At baseline and after 3 and 6 months of training, blood samples were obtained to assess bone formation (serum procollagen type 1 N propeptide (PINP) and bone resorption (serum C-terminal telopeptide of type I collagen (CTX), and participants underwent dual-energy X-ray absorptiometry scans to obtain total body and regional estimates of bone mineral density (BMD).

Results

Results demonstrated significant increases (p < 0.05) in spine BMD (+4.8 %; 1.27 ± 0.22–1.33 ± 0.24 g/cm2) and decreases (p < 0.01) in total hip BMD (−6.1 %; 0.98 ± 0.18–0.91 ± 0.16 g/cm2) from 0 to 6 months of training. BMD at the bilateral distal femur (−7.5 to −11.0 %) and proximal tibia (− 8.0 to −11.2 %) declined but was not different (p > 0.05) versus baseline. Neither PINP nor CTX was altered (p > 0.05) with training.

Conclusions

Chronic activity-based therapy did not reverse bone loss typically observed soon after injury, yet reductions in BMD were less than the expected magnitude of decline in lower extremity BMD in persons with recent SCI.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ABT:

Activity based therapy

BMC:

Bone mineral content

BMD:

Bone mineral density

C:

Cervical

CTX:

Serum C-terminal telopeptide of type I collagen

DXA:

Dual-energy X-ray absorptiometry

FES:

Functional electrical stimulation

L:

Lumbar

PINP:

Procollagen type 1 N propeptide

SCI:

Spinal cord injury

References

  • Alekna V, Tamulaitiene M, Sinevicius T, Juocevicius A (2008) Effect of weight-bearing activities on bone mineral density in spinal cord injured patients during the period of the first two years. Spinal Cord 46:727–732

    Article  CAS  PubMed  Google Scholar 

  • Astorino TA, Witzke KA (2012) Does exercise training slow bone loss in the spinal cord injured? Efficacy, technical considerations, and questions that remain to be answered. Nova Science Publishers Inc., Hauppauge NY

    Google Scholar 

  • Bauman WA, Zhong YG, Schwartz E (1995) Vitamin D deficiency in veterans with chronic spinal cord injury. Metabolism 44(12):1612–1616

    Article  CAS  PubMed  Google Scholar 

  • Bauman WA, Spungen AM, Morrison N, Zhang RL, Schwartz E (2005) Effect of a vitamin D analog on leg bone mineral density in patients with chronic spinal cord injury. J Rehabil Res Devel 42(5):625–634

    Article  Google Scholar 

  • Belanger M, Stein RB, Wheeler GD, Gordon T, Leduc B (2000) Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch Phys Med Rehabil 81:1090–1098

    Article  CAS  PubMed  Google Scholar 

  • Biering-Sorenson F, Bohr HH, Schaadt OP (1990) Longitudinal study of bone mineral content in the lumbar spine, forearm, and the lower extremities after spinal cord injury. Eur J Clin Invest 20:330–335

    Article  Google Scholar 

  • Black DM, Cummings SR, Genant HK, Nevitt MC, Palermo L, Browner W (1992) Axial and appendicular bone density predict fractures in older women. J Bone Min Res 7(6):633–638

    Article  CAS  Google Scholar 

  • Bloomfield SA, Mysiw WJ, Jackson RD (1996) Bone mass and endocrine adaptations to training in spinal cord injured individuals. Bone 19(1):61–68

    Article  CAS  PubMed  Google Scholar 

  • Carvalho DCL, Garlipp CR, Bottini PV, Afaz SH, Moda MA, Cliquet A (2006) Effect of treadmill gait on bone markers and bone mineral density of quadriplegic subjects. Brazilian J Med Biol Res 39:1357–1363

    Article  CAS  Google Scholar 

  • Chain A, Koury JC, Bezerra FF (2012) Physical activity benefits bone density and bone-related hormones in adult men with cervical spinal cord injury. Eur J Appl Physiol 112:3179–3186

    Article  CAS  PubMed  Google Scholar 

  • Chen SC, Lai CH, Chan WP, Hunag MH, Tsai HW, Chen JJ (2005) Increases in bone mineral density after functional electrical stimulation cycling exercises in spinal cord injured patients. Disabil Rehabil 27(22):1337–1341

    Article  PubMed  Google Scholar 

  • Clark JM, Jelbart M, Rischbieth H, Strayer J, Chatterton B, Schultz C, Marshall R (2007) Physiological effects of lower extremity functional electrical stimulation in early spinal cord injury: lack of efficacy to prevent bone loss. Spinal Cord 45:78–85

    Article  CAS  PubMed  Google Scholar 

  • Collins EG, Gater D, Kiratli J, Butler J, Hanson K, Langbein WE (2010) Energy cost of physical activities in persons with spinal cord injury. Med Sci Sports Exerc 42(4):691–700

    Article  PubMed  Google Scholar 

  • Committee to Review Dietary Reference Intakes for Vitamin D and Calcium, Food and Nutrition Board, Institute of Medicine (2010) Dietary Reference Intakes for Calcium and Vitamin D. National Academy Press, Washington, DC

  • Coupaud S, Jack LP, Hunt KJ (2009) Muscle and bone adaptations after treadmill training in incomplete spinal cord injury: a case study using peripheral quantitative computed tomography. J Musculoskelet Neuronal Interact 9(4):288–297

    CAS  PubMed  Google Scholar 

  • Dauty M, Perroun Verbe B, Maugars Y, Dubois C, Mathe JF (2000) Supralesional and sublesional bone mineral density in spinal cord-injured patients. Bone 27:305–309

    Article  CAS  PubMed  Google Scholar 

  • de Bruin ED, Frey-Rindova P, Herzog RE, Dietz V, Dambacher MA, Stussi E (1999) Changes of tibia bone properties after spinal cord injury: effects of early intervention. Arch Phys Med Rehabil 80:214–220

    Article  PubMed  Google Scholar 

  • Delmas PD, Munoz F, Black DM, Cosman F, Boonen S, Watts NB, Kendler N, Eriksen EF, Mesenbrink PG, Eastell R (2009) Effects of yearly zoledronic acid 5 mg on bone turnover markers and relation of PINP with fracture reduction in postmenopausal women with osteoporosis. J Bone Min Res 24(9):1544–1551

    Article  CAS  Google Scholar 

  • Dietz V, Muller R, Colombo G (2002) Locomotor activity in spinal man: significance of afferent input from joint and load receptors. Brain 125(12):2626–2634

    Article  PubMed  Google Scholar 

  • Eastell R, Rogers A, Ni X, Krege JH (2011) Effects of raloxifene and alendronate on bone turnover as assessed by procollagen type I N-terminal propeptide. Osteoporos Int 22:1927–1934

    Article  CAS  PubMed  Google Scholar 

  • Edwards WB, Schnitzer TJ, Troy KL (2013) Bone mineral loss at the proximal femur in acute spinal cord injury. Osteoporos Int 24:2323–2328

    Article  Google Scholar 

  • Eser P, de Bruin ED, Telley I, Lechner HE, Knecht H, Stussi E (2003) Effect of electrical stimulation-induced cycling on bone mineral density in spinal cord-injured patients. Eur J Clin Invest 33:412–419

    Article  CAS  PubMed  Google Scholar 

  • Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, Schiessl H (2004) Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals. Bone 34:869–880

    Article  CAS  PubMed  Google Scholar 

  • Forrest GF, Sisto SA, Barbeau H, Kirshblum SC, Wilen J, Bond Q, Bentson S, Asselin P, Cirnigliaro CM, Harkema S (2008) Neuromotor and musculoskeletal responses to locomotor training for an individual with chronic motor complete AIS-B spinal cord injury. J Spinal Cord Med 31(5):509–521

    PubMed  Google Scholar 

  • Frost HM (1987) Bone ‘mass’ and the ‘mechanostat’: a proposal. Anat Rec 219:1–9

    Article  CAS  PubMed  Google Scholar 

  • Frotzler A, Coupaud S, Perret C, Kakebeeke TH, Hunt KJ, de Donaldson N, Eser P (2008) High-volume FES-cycling partially reverses bone loss in people with chronic spinal cord injury. Bone 43:169–176

    Article  PubMed  Google Scholar 

  • Garland DE, Adkins RH (2001) Bone loss at the knee in spinal cord injury. Top Spinal Cord Inj Rehabil 6:37–46

    Article  Google Scholar 

  • Garland DE, Adkins RH, Stewart CA, Ashford R, Vigil D (2001) Regional osteoporosis in women who have a complete spinal cord injury. J Bone Joint Surg Am 83(A8):1195–1200

    Google Scholar 

  • Giangregorio LM, Hicks AL, Webber CE, Phillips SM, Craven BC, Bugaresti JM, McCartney N (2005) Body weight supported treadmill training in acute spinal cord injury: impact on muscle and bone. Spinal Cord 43:649–657

    Article  CAS  PubMed  Google Scholar 

  • Giangregorio LM, Webber CE, Hicks AL, Phillips SM, Craven BC, Bugaresti JM, McCartney N (2006) Can body weight supported treadmill training increase bone mass and reverse muscle atrophy in individuals with chronic incomplete spinal cord injury? Appl Physiol Nutr Metab 31(3):283–291

    Article  PubMed  Google Scholar 

  • Gilchrist NL, Frampton CM, Acland RH, Nicholls MG, March RL, Maguire P, Heard A, Reilly P, Marshall K (2007) Alendronate prevents bone loss in patients with acute spinal cord injury: a randomized, double-blind, placebo-controlled study. J Clin Endo Metab 92(4):1385–1390

    Article  CAS  Google Scholar 

  • Gordon KE, Wald M, Schnitzer TJ (2013) Effect of parathyroid hormone combined with gait training on bone density and bone architecture in people with chronic spinal cord injury. PM R 5(8):663–671. doi:10.1016/j.pmrj.2013.03.032

    Article  PubMed  Google Scholar 

  • Harness ET, Astorino TA (2011) Acute energy cost of multi-modal activity based therapy in persons with spinal cord injury. J Spinal Cord Med 34(5):495–500

    Article  PubMed  Google Scholar 

  • Harness ET, Yozbatiran N, Cramer SC (2008) Effects of intense exercise in chronic spinal cord injury. Spinal Cord 46(11):733–737

    Article  CAS  PubMed  Google Scholar 

  • Hummel K, Craven BC, Giangregorio L (2012) Serum 25(OH)D, PTH, and correlates of suboptimal 25(OH)D in persons with chronic spinal cord injury. Spinal Cord 50:812–816

    Article  CAS  PubMed  Google Scholar 

  • Kodama Y, Umemura Y, Nagasawa S, Beamer WG, Donahue LR, Rosen CR, Baylink DJ, Farley JR (2000) Exercise and mechanical loading increase periosteal bone formation and whole bone strength in C57BL/6J mice but not in C3H/Hej mice. Calcif Tissue Int 66(4):298–306

    Article  CAS  PubMed  Google Scholar 

  • Lai CH, Chang WH, Chan WP, Peng CW, Shen LK, Chen JJ, Chen SC (2010) Effects of functional electrical stimulation cycling exercise on bone mineral density loss in the early stages of spinal cord injury. J Rehabil Med 42(2):150–154

    Article  PubMed  Google Scholar 

  • Maegele M, Muller S, Wernig A, Edgerton VR, Harkema SJ (2002) Recruitment of spinal motor pools during voluntary movements versus stepping after human spinal cord injury. J Neurotrauma 19(10):1217–1229

    Article  CAS  PubMed  Google Scholar 

  • Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M (1997) Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int 61:22–25

    Article  CAS  PubMed  Google Scholar 

  • Needham-Shropshire BM, Broton JG, Klose KJ, Lebwohl N, Guest RS, Jacobs PL (1997) Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 3. Lack of effect on bone mineral density. Arch Phys Med Rehabil 78:799–803

    Article  CAS  PubMed  Google Scholar 

  • Perret C, Berry H, Hunt KJ, Donaldson N, Kakebeeke TH (2010) Feasibility of functional electrical stimulated cycling in subjects with spinal cord injury: an energetics assessment. J Rehabil Med 42:873–875

    Article  PubMed  Google Scholar 

  • Reiter AL, Volk A, Vollmar J, Fromm B, Gerner HJ (2007) Changes of basic bone turnover parameters in short-term and long-term patients with spinal cord injury. Eur Spine J 16:771–776

    Article  PubMed  Google Scholar 

  • Roberts D, Lee W, Cuneo RC, Wittmann J, Ward G, Flatman R, McWhinney B, Hickman PE (1998) Longitudinal study of bone turnover after acute spinal cord injury. J Clin Endo Metab 83:415–422

    Article  CAS  Google Scholar 

  • Rogers A, Glover SJ, Eastell R (2009) A randomized, double-blinded, placebo-controlled trial to determine the individual response in bone turnover markers to lasofoxifene therapy. Bone 45:1044–1052

    Article  CAS  PubMed  Google Scholar 

  • Sadowsky CL, McDonald JW (2009) Activity-based restorative therapies: concepts and applications in spinal cord injury-related neurorehabilitation. Dev Disabil Res Rev 15(2):112–116

    Article  PubMed  Google Scholar 

  • Shields RK, Schlechte J, Dudley-Javoroski S, Zwart BD, Clark SD, Grant SA, Mattiace VM (2005) Bone mineral density after spinal cord injury: a reliable method for knee assessment. Arch Phys Med Rehabil 86(10):1969–1973

    Article  PubMed  Google Scholar 

  • Shields RK, Dudley-Javoroski S, Frey Law LA (2006) Electrically induced muscle contractions influence bone density decline after spinal cord injury. Spine 31(3):548–553

    Article  PubMed  Google Scholar 

  • Vainionpää A, Korpelainen R, Vihriälä E, Rinta-Paavola A, Leppäluoto J, Jämsä T (2009) Effect of impact exercise on bone metabolism. Osteoporos Int 20(10):1725–1733

    Article  PubMed  Google Scholar 

  • van Nes IJ, Guerts AC, Hendricks HT, Duysen J (2004) Short-term effects of whole-body vibration on postural control in unilateral chronic stroke patients: preliminary evidence. Am J Phys Med Rehabil 83(11):867–873

    Article  PubMed  Google Scholar 

  • Vasikaran S, Eastell R, Bruyère O, Foldes AJ, Garnero P, Griesmacher A et al (2011) Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 22(2):391–420

    Article  CAS  PubMed  Google Scholar 

  • Yang JF, Gorassini M (2006) Spinal and brain control of human walking: implications for retraining of walking. Neuroscientist 12(5):379–389

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This project was funded by a grant from the National Institutes of Health SC3GM095416-02. The authors also thank the subjects for their dedication to this project as well as Brian J. Martin, M.S., L.V.N., John Lyon R.N., and Katya Geronimo L.V.N. for performing the blood draws.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Todd Anthony Astorino.

Additional information

Communicated by Fabio Fischetti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Astorino, T.A., Harness, E.T. & Witzke, K.A. Effect of chronic activity-based therapy on bone mineral density and bone turnover in persons with spinal cord injury. Eur J Appl Physiol 113, 3027–3037 (2013). https://doi.org/10.1007/s00421-013-2738-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-013-2738-0

Keywords

Navigation