Skip to main content

Advertisement

SpringerLink
Log in

Alteration of Volumetric Bone Mineral Density Parameters in Men with Spinal Cord Injury

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

Abstract

Spinal cord injury (SCI) induces severe losses of trabecular and cortical volumetric bone mineral density (vBMD), which cannot be discriminated with conventional dual-energy X-ray absorptiometry (DXA) analysis. The objectives were to: (i) determine the effects of SCI on areal BMD (aBMD) and vBMD determined by advanced 3D-DXA-based methods at various femoral regions and (ii) model the profiles of 3D-DXA-derived parameters with the time since injury. Eighty adult males with SCI and 25 age-matched able-bodied (AB) controls were enrolled in this study. Trabecular and cortical vBMD, cortical thickness and derived strength parameters were assessed by 3D-SHAPER® software at various femoral subregions. Individuals with SCI had significantly lower integral vBMD, trabecular vBMD, cortical vBMD, cortical thickness and derived bone strength parameters (p < 0.001 for all) in total proximal femur compared with AB controls. These alterations were approximately to the same degree for all three femoral subregions, and the difference between the two groups tended to be greater for cortical vBMD than trabecular vBMD. There were minor differences according to the lesion level (paraplegics vs tetraplegics) for all 3D-DXA-derived parameters. For total proximal femur, the decreasing bone parameters tended to reach a new steady state after 5.1 years for integral vBMD, 7.4 years for trabecular vBMD and 9.2 years for cortical vBMD following SCI. At proximal femur, lower vBMD (integral, cortical and trabecular) and cortical thickness resulted in low estimated bone strength in individuals with SCI. It remains to be demonstrated whether these new parameters are more closely associated with fragility fracture than aBMD.

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

Similar content being viewed by others

References

  1. 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 

  2. 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 

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

    Article  CAS  PubMed  Google Scholar 

  4. 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 

  5. Bauman WA, Spungen AM, Wang J, Pierson RN Jr, Schwartz E (1999) Continuous loss of bone during chronic immobilization: a monozygotic twin study. Osteoporos Int 10:123–127

    Article  CAS  PubMed  Google Scholar 

  6. Frisbie JH (1997) Fractures after myelopathy: the risk quantified. J Spinal Cord Med 20:66–69

    Article  CAS  PubMed  Google Scholar 

  7. Fattal C, Mariano-Goulart D, Thomas E, Rouays-Mabit H, Verollet C, Maimoun L (2011) Osteoporosis in persons with spinal cord injury: the need for a targeted therapeutic education. Arch Phys Med Rehabil 92:59–67

    Article  PubMed  Google Scholar 

  8. Morse LR, Battaglino RA, Stolzmann KL, Hallett LD, Waddimba A, Gagnon D, Lazzari AA, Garshick E (2009) Osteoporotic fractures and hospitalization risk in chronic spinal cord injury. Osteoporos Int 20:385–392

    Article  CAS  PubMed  Google Scholar 

  9. Grassner L, Klein B, Maier D, Buhren V, Vogel M (2018) Lower extremity fractures in patients with spinal cord injury characteristics, outcome and risk factors for non-unions. J Spinal Cord Med 41:676–683

    Article  PubMed  Google Scholar 

  10. Biering-Sorensen F, Bohr H, Schaadt O (1988) Bone mineral content of the lumbar spine and lower extremities years after spinal cord lesion. Paraplegia 26:293–301

    CAS  PubMed  Google Scholar 

  11. Zheng X, Qi Y, Zhou H, Kang H, Tong Y, Bi L (2021) Bone mineral density at the distal femur and proximal tibia and related factors during the first year of spinal cord injury. Int J Gen Med 14:1121–1129

    Article  PubMed  PubMed Central  Google Scholar 

  12. Vestergaard P, Krogh K, Rejnmark L, Mosekilde L (1998) Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord 36:790–796

    Article  CAS  PubMed  Google Scholar 

  13. Carbone LD, Chin AS, Burns SP, Svircev JN, Hoenig H, Heggeness M, Weaver F (2013) Morbidity following lower extremity fractures in men with spinal cord injury. Osteoporos Int 24:2261–2267

    Article  CAS  PubMed  Google Scholar 

  14. Lala D, Craven BC, Thabane L, Papaioannou A, Adachi JD, Popovic MR, Giangregorio LM (2014) Exploring the determinants of fracture risk among individuals with spinal cord injury. Osteoporos Int 25:177–185

    Article  CAS  PubMed  Google Scholar 

  15. Nielsen SP (2000) The fallacy of BMD: a critical review of the diagnostic use of dual X-ray absorptiometry. Clin Rheumatol 19:174–183

    Article  CAS  PubMed  Google Scholar 

  16. Bauman WA, Kirshblum S, Cirnigliaro C, Forrest GF, Spungen AM (2010) Underestimation of bone loss of the spine with posterior-anterior dual-energy X-ray absorptiometry in patients with spinal cord injury. J Spinal Cord Med 33:214–220

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ghasem-Zadeh A, Galea MP, Nunn A, Panisset M, Wang XF, Iuliano S, Boyd SK, Forwood MR, Seeman E (2021) Heterogeneity in microstructural deterioration following spinal cord injury. Bone 142:115778

    Article  PubMed  Google Scholar 

  18. Abdelrahman S, Ireland A, Winter EM, Purcell M, Coupaud S (2021) Osteoporosis after spinal cord injury: aetiology, effects and therapeutic approaches. J Musculoskelet Neuronal Interact 21:26–50

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515

    Article  CAS  PubMed  Google Scholar 

  20. Sheu Y, Zmuda JM, Boudreau RM, Petit MA, Ensrud KE, Bauer DC, Gordon CL, Orwoll ES, Cauley JA, O Fractures in Men Mr OSRG (2011) Bone strength measured by peripheral quantitative computed tomography and the risk of nonvertebral fractures: the osteoporotic fractures in men (MrOS) study. J Bone Miner Res 26:63–71

    Article  PubMed  Google Scholar 

  21. Adams JE (2009) Quantitative computed tomography. Eur J Radiol 71:415–424

    Article  PubMed  Google Scholar 

  22. Humbert L, Martelli Y, Fonolla R, Steghofer M, Di Gregorio S, Malouf J, Romera J, Barquero LM (2017) 3D-DXA: assessing the femoral shape, the trabecular macrostructure and the Cortex in 3D from DXA images. IEEE Trans Med Imaging 36:27–39

    Article  PubMed  Google Scholar 

  23. Maimoun L, Ben Bouallegue F, Gelis A, Aouinti S, Mura T, Philibert P, Souberbielle JC, Piketty M, Garnero P, Mariano-Goulart D, Fattal C (2019) Periostin and sclerostin levels in individuals with spinal cord injury and their relationship with bone mass, bone turnover, fracture and osteoporosis status. Bone 127:612–619

    Article  CAS  PubMed  Google Scholar 

  24. Humbert L, Hazrati Marangalou J, Del Rio Barquero LM, van Lenthe GH, van Rietbergen B (2016) Technical Note: Cortical thickness and density estimation from clinical CT using a prior thickness-density relationship. Med Phys 43:1945

    Article  PubMed  Google Scholar 

  25. Clotet J, Martelli Y, Di Gregorio S, Del Rio Barquero LM, Humbert L (2018) Structural parameters of the proximal femur by 3-dimensional Dual-energy X-ray absorptiometry software: comparison With quantitative computed tomography. J Clin Densitom 21:550–562

    Article  PubMed  Google Scholar 

  26. Cohen J (1988) Statistical Power Analysis for the Behavioral Sciences. Routledge, New York, p 567

    Google Scholar 

  27. Sawilowsky S (2009) New effect size rules of thumb. J Mod Appl Stat Methods 8:467–474

    Article  Google Scholar 

  28. Bang H, Mazumdar M, Spence JD (2006) Tutorial in biostatistics: Analyzing associations between total plasma homocysteine and B vitamins using optimal categorization and segmented regression. Neuroepidemiology 27:188–200

    Article  PubMed  Google Scholar 

  29. 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 

  30. Winzenrieth R, Humbert L, Di Gregorio S, Bonel E, Garcia M, Del Rio L (2018) Effects of osteoporosis drug treatments on cortical and trabecular bone in the femur using DXA-based 3D modeling. Osteoporos Int 29:2323–2333

    Article  CAS  PubMed  Google Scholar 

  31. Maimoun L, Renard E, Humbert L, Aouinti S, Mura T, Boudousq V, Lefebvre P, Mahadea K, Philibert P, de Santa-Barbara P, Avignon A, Guillaume S, Sultan A, Nocca D, Mariano-Goulart D (2021) Modification of bone mineral density, bone geometry and volumetric BMD in young women with obesity. Bone 150:116005

    Article  CAS  PubMed  Google Scholar 

  32. Freitas L, Amorim T, Humbert L, Fonolla R, Flouris AD, Metsios GS, Jamurtas AZ, Koutedakis Y (2019) Cortical and trabecular bone analysis of professional dancers using 3D-DXA: a case-control study. J Sports Sci 37:82–89

    Article  PubMed  Google Scholar 

  33. Brance ML, Pons-Estel BA, Quagliato NJ, Jorfen M, Berbotto G, Cortese N, Raggio JC, Palatnik M, Chavero I, Soldano J, Dieguez C, Sanchez A, Del Rio L, Di Gregorio S, Brun LR (2021) Trabecular and cortical bone involvement in rheumatoid arthritis by DXA and DXA-based 3D modelling. Osteoporos Int 32:705–714

    Article  CAS  PubMed  Google Scholar 

  34. Dionyssiotis Y, Trovas G, Galanos A, Raptou P, Papaioannou N, Papagelopoulos P, Petropoulou K, Lyritis GP (2007) Bone loss and mechanical properties of tibia in spinal cord injured men. J Musculoskelet Neuronal Interact 7:62–68

    CAS  PubMed  Google Scholar 

  35. Rittweger J, Gerrits K, Altenburg T, Reeves N, Maganaris CN, de Haan A (2006) Bone adaptation to altered loading after spinal cord injury: a study of bone and muscle strength. J Musculoskelet Neuronal Interact 6:269–276

    CAS  PubMed  Google Scholar 

  36. Frey-Rindova P, de Bruin ED, Stussi E, Dambacher MA, Dietz V (2000) Bone mineral density in upper and lower extremities during 12 months after spinal cord injury measured by peripheral quantitative computed tomography. Spinal Cord 38:26–32

    Article  CAS  PubMed  Google Scholar 

  37. Bauman WA, Wecht JM, Kirshblum S, Spungen AM, Morrison N, Cirnigliaro C, Schwartz E (2005) Effect of pamidronate administration on bone in patients with acute spinal cord injury. J Rehabil Res Dev 42:305–313

    Article  PubMed  Google Scholar 

  38. Gifre L, Humbert L, Muxi A, Del Rio L, Vidal J, Portell E, Monegal A, Guanabens N, Peris P (2018) Analysis of the evolution of cortical and trabecular bone compartments in the proximal femur after spinal cord injury by 3D-DXA. Osteoporos Int 29:201–209

    Article  CAS  PubMed  Google Scholar 

  39. Maimoun L, Couret I, Micallef JP, Peruchon E, Mariano-Goulart D, Rossi M, Leroux JL, Ohanna F (2002) Use of bone biochemical markers with dual-energy x-ray absorptiometry for early determination of bone loss in persons with spinal cord injury. Metabolism 51:958–963

    Article  CAS  PubMed  Google Scholar 

  40. Frotzler A, Berger M, Knecht H, Eser P (2008) Bone steady-state is established at reduced bone strength after spinal cord injury: a longitudinal study using peripheral quantitative computed tomography (pQCT). Bone 43:549–555

    Article  PubMed  Google Scholar 

  41. Biggin A, Briody JN, Ramjan KA, Middleton A, Waugh MC, Munns CF (2013) Evaluation of bone mineral density and morphology using pQCT in children after spinal cord injury. Dev Neurorehabil 16:391–397

    Article  PubMed  Google Scholar 

  42. Coupaud S, McLean AN, Purcell M, Fraser MH, Allan DB (2015) Decreases in bone mineral density at cortical and trabecular sites in the tibia and femur during the first year of spinal cord injury. Bone 74:69–75

    Article  PubMed  Google Scholar 

  43. McCarthy ID, Bloomer Z, Gall A, Keen R, Ferguson-Pell M (2012) Changes in the structural and material properties of the tibia in patients with spinal cord injury. Spinal Cord 50:333–337

    Article  CAS  PubMed  Google Scholar 

  44. Frotzler A, Cheikh-Sarraf B, Pourtehrani M, Krebs J, Lippuner K (2015) Long-bone fractures in persons with spinal cord injury. Spinal Cord 53:701–704

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to express their thanks to the individuals with spinal cord injury and the controls for their participation.

Author information

Authors and Affiliations

  1. Département de Médecine Nucléaire, Hôpital Lapeyronie, CHU Montpellier, Montpellier, France

    Laurent Maïmoun & Denis Mariano-Goulart

  2. Département de Biophysique, Service de Médecine Nucléaire, PhyMedExp, INSERM, CNRS, Université de Montpellier, Hôpital Lapeyronie, 371, Avenue du Doyen Gaston Giraud, 34295, cedex 5, Montpellier, France

    Laurent Maïmoun, Pascal de Santa-Barbara & Denis Mariano-Goulart

  3. Centre Mutualiste PROPARA, Montpellier, France

    Anthony Gelis

  4. Department of Biostatistics, Clinical Epidemiology, Public Health, and Innovation in Methodology, Nimes University Hospital, University of Montpellier, Nîmes, France

    Chris Serrand & Thibault Mura

  5. 3D-Shaper Medical, Barcelona, Spain

    Ludovic Humbert

  6. Département de Médecine Nucléaire, Hôpital Carémeau, CHRU Nîmes, Nîmes, France

    Vincent Boudousq

  7. Institut d’Electronique Et Des Système, UMR CNRS 5214, Université de Montpellier, Montpellier, France

    Didier Laux

  8. CRF Bouffard-Vercelli USSAP, Perpignan, France

    Charles Fattal

Authors
  1. Laurent Maïmoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony Gelis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris Serrand
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thibault Mura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ludovic Humbert
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vincent Boudousq
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pascal de Santa-Barbara
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Didier Laux
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Charles Fattal
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Denis Mariano-Goulart
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LM and DM-G contributed to conceptualisation. LM, CS and TM contributed to methodology. LM, LH, CS and TM contributed to software. LM, CS and TM contributed to validation. CS and TM contributed to formal analysis. LM, AG, VB, CF and DM-G contributed to investigation. LM, AG, PdS-B, CF contributed to resources . LM, CS and TM contributed to data curation. LM, DM-G contributed to writing—original draft. LM, AG, CS, TM, LH, VB, PdS-B, DL, CF and DM-G writing—review & editing. LM, CS and TM contributed to visualisation. LM, AG, CF and DM-G contributed to supervision. LM, AG, CF and DM-G contributed to project administration.

Corresponding author

Correspondence to Laurent Maïmoun.

Ethics declarations

Conflict of interest

I certify that neither I (Laurent Maimoun) nor my co-authors (Anthony Gelis, Chris Serrand, Thibault Mura, Vincent Boudousq, Pascal de Santa-Barbara, Didier Laux, Charles Fattal, Denis Mariano-Goulart) have a conflict of interest that is relevant to the subject matter or materials included in this work. Ludovic Humbert is an employee and shareholder of 3D-Shaper Medical.

Human Rights and Informed Consent

Approval was obtained from Regional Research Ethics Committee (Comité de Protection des Personnes Sud-Mediterranee IV, Montpellier, France). All procedures used adhere to the tenets of the Declaration of Helsinki. Participants were given oral and written information and then delivered written informed consent.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maïmoun, L., Gelis, A., Serrand, C. et al. Alteration of Volumetric Bone Mineral Density Parameters in Men with Spinal Cord Injury. Calcif Tissue Int 113, 304–316 (2023). https://doi.org/10.1007/s00223-023-01110-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-023-01110-2

Keywords

Search

Navigation