Skip to main content

Advertisement

SpringerLink
Log in

Differences in Bone Mineral Density, Markers of Bone Turnover and Extracellular Matrix and Daily Life Muscular Activity Among Patients with Recent Motor-Incomplete Versus Motor-Complete Spinal Cord Injury

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Spinal cord injury (SCI) leads to severe bone loss, but the associated mechanisms are poorly described in incomplete SCI individuals. The purpose of the study is to compare alterations in bone mineral density (BMD) and serum biomarkers of bone turnover in recent motor-incomplete to -complete SCI men, as well as to describe their physical activity and spasticity. We studied 31 men with acute SCI. Whole-body DXA scans, serum biomarkers and self-reported activity and spasticity were examined 1 and/or 3 and 12 months after the injury. We observed a decrease in proximal femur BMD (p < 0.02) in both the groups. Serum phosphate and carboxy-terminal-collagen crosslinks were significantly lower in motor-incomplete versus complete SCI men, whereas albumin-corrected Ca2+ (p = 0.02) were lower only 3 months after injury. When data from all 31 SCI participants were pooled, we observed increased serum matrix metalloproteinase-2 (MMP-2) and tissue inhibitors of MMP-2 (TIMP-2) (p < 0.02) whereas TIMP-1 decreased (p = 0.03). BMD correlated positively with self-reported activity (r = 0.59, p = 0.04) and negatively with spasticity (r = 0.74, p = 0.02) 12 months after injury. As a summary, men with motor-incomplete SCI developed significant proximal femur bone loss 12 months after injury and exhibited increased bone resorption throughout the first year after the injury. Compared with complete SCI men, incomplete SCI men show attenuated bone resorption. Our pooled data show increased turnover of extracellular matrix after injury and that increased exercise before and after injury correlated with reduced bone loss.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Gifre L, Vidal J, Carrasco J, Portell E, Puig J, Monegal A, Guanabens N, Peris P (2014) Incidence of skeletal fractures after traumatic spinal cord injury: a 10-year follow-up study. Clin Rehabil 28:361–369

    Article  PubMed  Google Scholar 

  2. 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 Endocrinol Metab 83:415–422

    CAS  PubMed  Google Scholar 

  3. Charmetant C, Phaner V, Condemine A, Calmels P (2010) Diagnosis and treatment of osteoporosis in spinal cord injury patients: a literature review. Ann Phys Rehabil Med 53:655–668

    Article  CAS  PubMed  Google Scholar 

  4. Jiang SD, Jiang LS, Dai LY (2006) Mechanisms of osteoporosis in spinal cord injury. Clin Endocrinol (Oxf) 65:555–565

    Article  CAS  Google Scholar 

  5. Jiang SD, Dai LY, Jiang LS (2006) Osteoporosis after spinal cord injury. Osteoporos Int 17:180–192

    Article  PubMed  Google Scholar 

  6. Battaglino RA, Lazzari AA, Garshick E, Morse LR (2012) Spinal cord injury-induced osteoporosis: pathogenesis and emerging therapies. Curr Osteoporos Rep 10:278–285

    Article  PubMed Central  PubMed  Google Scholar 

  7. Garland DE, Stewart CA, Adkins RH, Hu SS, Rosen C, Liotta FJ, Weinstein DA (1992) Osteoporosis after spinal cord injury. J Orthop Res 10:371–378

    Article  CAS  PubMed  Google Scholar 

  8. Lazo MG, Shirazi P, Sam M, Giobbie-Hurder A, Blacconiere MJ, Muppidi M (2001) Osteoporosis and risk of fracture in men with spinal cord injury. Spinal Cord 39:208–214

    Article  CAS  PubMed  Google Scholar 

  9. Garland DE, Adkins RH, Scott M, Singh H, Massih M, Stewart C (2004) Bone loss at the os calcis compared with bone loss at the knee in individuals with spinal cord injury. J Spinal Cord Med 27:207–211

    PubMed  Google Scholar 

  10. Garland DE, Adkins RH, Stewart CA (2008) Five-year longitudinal bone evaluations in individuals with chronic complete spinal cord injury. J Spinal Cord Med 31:543–550

    PubMed Central  PubMed  Google Scholar 

  11. Maimoun L, Fattal C, Micallef JP, Peruchon E, Rabischong P (2006) Bone loss in spinal cord-injured patients: from physiopathology to therapy. Spinal Cord 44:203–210

    Article  CAS  PubMed  Google Scholar 

  12. Singh R, Rohilla RK, Saini G, Kaur K (2014) Longitudinal study of body composition in spinal cord injury patients. Ind J Orthop 48:168–177

    Article  Google Scholar 

  13. Giangregorio LM, Webber CE, Phillips SM, Hicks AL, 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 31:283–291

    Article  PubMed  Google Scholar 

  14. National Spinal Cord Injury Statistical C (2011) National Spinal Cord Injury Statistical Center, University of Alabama at Birmingham, 2010 Annual Statistical Report, March, 2011.

  15. Maynard FM Jr, Bracken MB, Creasey G, Ditunno JF Jr, Donovan WH, Ducker TB, Garber SL, Marino RJ, Stover SL, Tator CH, Waters RL, Wilberger JE, Young W (1997) International standards for neurological and functional classification of spinal cord injury. American spinal injury association. Spinal Cord. 35:266–274

    Article  PubMed  Google Scholar 

  16. Graff-Iversen S, Anderssen SA, Holme IM, Jenum AK, Raastad T (2008) Two short questionnaires on leisure-time physical activity compared with serum lipids, anthropometric measurements and aerobic power in a suburban population from Oslo, Norway. Eur J Epidemiol 23:167–174

    Article  PubMed  Google Scholar 

  17. Aires N, Selmer R, Thelle D (2003) The validity of self-reported leisure time physical activity, and its relationship to serum cholesterol, blood pressure and body mass index. A population based study of 332,182 men and women aged 40–42 years. Eur J Epidemiol 18:479–485

    Article  PubMed  Google Scholar 

  18. Marcus BH, Rakowski W, Rossi JS (1992) Assessing motivational readiness and decision making for exercise. Health Psychol 11:257–261

    Article  CAS  PubMed  Google Scholar 

  19. Nigg CR, Courneya KS (1998) Transtheoretical model: examining adolescent exercise behavior. J Adolesc Health 22:214–224

    Article  CAS  PubMed  Google Scholar 

  20. Prapavessis H, Maddison R, Brading F (2004) Understanding exercise behavior among New Zealand adolescents: a test of the transtheoretical. J Adolesc Health 35:346.e317–346.e327

    Google Scholar 

  21. Lee RE, Nigg CR, DiClemente CC, Courneya KS (2001) Validating motivational readiness for exercise behavior with adolescents. Res Q Exerc Sport 72:401–410

    Article  CAS  PubMed  Google Scholar 

  22. Bulley C (2008) Stages of exercise behavior change: a pilot study of behavioral measures. J Int Health Promot 46:6

    Google Scholar 

  23. Priebe MM, Sherwood AM, Thornby JI, Kharas NF, Markowski J (1996) Clinical assessment of spasticity in spinal cord injury: a multidimensional problem. Arch Phys Med Rehabil 77:713–716

    Article  CAS  PubMed  Google Scholar 

  24. Hsieh JT, Wolfe DL, Miller WC, Curt A (2008) Spasticity outcome measures in spinal cord injury: psychometric properties and clinical utility. Spinal Cord 46:86–95

    Article  CAS  PubMed  Google Scholar 

  25. Mazess RB, Barden HS, Bisek JP, Hanson J (1990) Dual-energy x-ray absorptiometry for total-body and regional bone-mineral and soft-tissue composition. Am J Clin Nutr 51:1106–1112

    CAS  PubMed  Google Scholar 

  26. Miller PD (2006) Guidelines for the diagnosis of osteoporosis: T-scores vs fractures. Rev Endocr Metab Disord 7:75–89

    Article  PubMed  Google Scholar 

  27. Boesen AP, Dideriksen K, Couppe C, Magnusson SP, Schjerling P, Boesen M, Kjaer M, Langberg H (2013) Tendon and skeletal muscle matrix gene expression and functional responses to immobilisation and rehabilitation in young males: effect of growth hormone administration. J Physiol 591:6039–6052

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Allal-Elasmi M, Zayani Y, Zidi W, Zaroui A, Feki M, Mourali S, Mechmeche R, Kaabachi N (2014) The measurement of circulating matrix metalloproteinase-8 and its tissue inhibitor and their association with inflammatory mediators in patients with acute coronary syndrome. Clin Lab 60:951–956

    CAS  PubMed  Google Scholar 

  29. 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 33:674–677

    Article  CAS  PubMed  Google Scholar 

  30. Maynard FM, Imai K (1977) Immobilization hypercalcemia in spinal cord injury. Arch Phys Med Rehabil 58:16–24

    CAS  PubMed  Google Scholar 

  31. Niemann I, Hannemann A, Nauck M, Spielhagen C, Volzke H, Wallaschofski H, Friedrich N (2013) The association between insulin-like growth factor I and bone turnover markers in the general adult population. Bone 56:184–190

    Article  CAS  PubMed  Google Scholar 

  32. Paker N, Bugdayci D, Ersoy S, Uysal E, Elbirlik S (2007) Bone loss and bone turnover in acute and chronic spinal cord injured patients. Neurosciences (Riyadh) 12:232–235

    Google Scholar 

  33. Astorino TA, Harness ET, Witzke KA (2013) 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Maimoun L, Couret I, Mariano-Goulart D, Dupuy AM, Micallef JP, Peruchon E, Ohanna F, Cristol JP, Rossi M, Leroux JL (2005) Changes in osteoprotegerin/RANKL system, bone mineral density, and bone biochemicals markers in patients with recent spinal cord injury. Calcif Tissue Int 76:404–411

    Article  CAS  PubMed  Google Scholar 

  35. 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 Central  PubMed  Google Scholar 

  36. 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 

  37. 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 

  38. Dudley-Javoroski S, Saha PK, Liang G, Li C, Gao Z, Shields RK (2012) High dose compressive loads attenuate bone mineral loss in humans with spinal cord injury. Osteoporos Int 23:2335–2346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Frotzler A, Coupaud S, Perret C, Kakebeeke TH, Hunt KJ, DonaldsonNde 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 

  40. 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 

  41. Ben M, Harvey L, Denis S, Glinsky J, Goehl G, Chee S, Herbert RD (2005) Does 12 weeks of regular standing prevent loss of ankle mobility and bone mineral density in people with recent spinal cord injuries? Aust J Physiother 51:251–256

    Article  PubMed  Google Scholar 

  42. Wannapakhe J, Arrayawichanon P, Saengsuwan J, Amatachaya S (2013) Medical complications and falls in patients with spinal cord injury during the immediate phase after completing a rehabilitation program. J Spinal Cord Med [Epub ahead of print]

  43. Lidal IB, Jensen AE, Larsen TW, Stanghelle JK (2013) Fatigue in persons who have lived with spinal cord injury for >20 years. Spinal Cord 51:103–108

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank the staff at Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo University Hospital Oslo, Norway for all the help with the DXA-measurements and analysis, and Anne Lannem, the Department of Science, Sunnaas Rehabilitation Hospital, Nesoddtangen, Norway for the help with the physical activity questionnaires. A special thanks to Ingeborg Lidal, for allowing us to quote her unpublished data; Jan Falck and Kåre Birkeland, the Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo University Hospital Oslo, Norway for expert advice; and Hilde Einerkjær, Mariann Madsen Voll and Sunnaas Rehabilitation Hospital, Nesoddtangen, for performing the blood sampling.

Conflicts of Interest

No conflicts of interest, financial or otherwise, are declared by the authors Emil Kostovski, Nils Hjeltnes, Erik Fink Eriksen, Svein Olav Kolset, and Per Ole Iversen.

Human and Animal Rights and Informed Consent

Each study participant gave verbal and written informed consent prior to the study.

Author information

Authors and Affiliations

  1. Department of Science, Sunnaas Rehabilitation Hospital, Nesoddtangen, Norway

    E. Kostovski

  2. Sunnaas Rehabilitation Hospital, Nesoddtangen, Norway

    N. Hjeltnes

  3. Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo University Hospital, Oslo, Norway

    E. F. Eriksen

  4. Department of Nutrition, University of Oslo, Oslo, Norway

    S. O. Kolset & P. O. Iversen

  5. Department of Hematology, Oslo University Hospital, Oslo, Norway

    P. O. Iversen

Authors
  1. E. Kostovski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Hjeltnes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. F. Eriksen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. O. Kolset
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. O. Iversen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Kostovski.

Appendix

Appendix

See Table 4.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kostovski, E., Hjeltnes, N., Eriksen, E.F. et al. Differences in Bone Mineral Density, Markers of Bone Turnover and Extracellular Matrix and Daily Life Muscular Activity Among Patients with Recent Motor-Incomplete Versus Motor-Complete Spinal Cord Injury. Calcif Tissue Int 96, 145–154 (2015). https://doi.org/10.1007/s00223-014-9947-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-014-9947-3

Keywords

Search

Navigation