Skip to main content

Advertisement

Log in

Bone Geometry, Volumetric Bone Mineral Density, Microarchitecture and Estimated Bone Strength in Caucasian Females with Systemic Lupus Erythematosus. A Cross-Sectional Study Using HR-pQCT

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

Abstract

Patients with systemic lupus erythematosus (SLE) have an increased risk of fracture. We used high resolution peripheral quantitative computed tomography (HR-pQCT) to measure bone geometry, volumetric bone mineral density (vBMD), cortical and trabecular microarchitecture and estimated bone strength by finite element analysis (FEA) at the distal radius and tibia to assess bone characteristics beyond BMD that may contribute to the increased risk of fracture. Thirty-three Caucasian women with SLE (median age 48, range 21–64 years) and 99 controls (median age 45, range 21–64 years) were studied. Groups were comparable in radius regarding geometry and vBMD, but SLE patients had lower trabecular number (−7 %, p < 0.05), higher trabecular separation (13 %, p < 0.05) and lower FEA-estimated failure load compared to controls (−10 %, p < 0.05). In tibia, SLE patients had lower total vBMD (−11 %, p < 0.01), cortical area (−14 %, p < 0.001) and cortical thickness (−16 %, p < 0.001) and higher trabecular area (8 %, p < 0.05). In subgroup analyses of the premenopausal participants (SLE n = 21, controls n = 63), SLE patients had significantly lower trabecular bone volume fraction [(BV/TV); −17 %, p < 0.01], trabecular number (−9 %, p < 0.01), trabecular thickness (−9 %, p < 0.05) and higher trabecular separation (13 %, p < 0.01) and trabecular network inhomogeneity (14 %, p < 0.05) in radius along with lower BV/TV (−15 %, p < 0.01) and higher trabecular separation (11 %, p < 0.05) in tibia. FEA-estimated bone strength was lower in both radius (−11 %, p < 0.01) and tibia (−10 %, p < 0.05). In conclusion, Caucasian women with SLE compared to controls had fewer and more widely separated trabeculae and lower estimated bone strength in radius and lower total vBMD, cortical area and thickness in tibia.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Houssiau FA, Lefebvre C, Depresseux G, Lambert M, Devogelaer JP, de Nagant DC (1996) Trabecular and cortical bone loss in systemic lupus erythematosus. Br J Rheumatol 35:244–247

    Article  CAS  PubMed  Google Scholar 

  2. Sels F, Dequeker J, Verwilghen J, Mbuyi-Muamba JM (1996) SLE and osteoporosis: dependence and/or independence on glucocorticoids. Lupus 5:89–92

    Article  CAS  PubMed  Google Scholar 

  3. Yee CS, Crabtree N, Skan J, Amft N, Bowman S, Situnayake D et al (2005) Prevalence and predictors of fragility fractures in systemic lupus erythematosus. Ann Rheum Dis 64:111–113

    Article  PubMed Central  PubMed  Google Scholar 

  4. Angeli A, Guglielmi G, Dovio A, Capelli G, de FD, Giannini S et al (2006) High prevalence of asymptomatic vertebral fractures in post-menopausal women receiving chronic glucocorticoid therapy: a cross-sectional outpatient study. Bone 39:253–259

    Article  CAS  PubMed  Google Scholar 

  5. Ramsey-Goldman R, Dunn JE, Huang CF, Dunlop D, Rairie JE, Fitzgerald S et al (1999) Frequency of fractures in women with systemic lupus erythematosus: comparison with United States population data. Arthritis Rheum 42:882–890

    Article  CAS  PubMed  Google Scholar 

  6. Bultink IE (2012) Osteoporosis and fractures in systemic lupus erythematosus. Arthritis Care Res (Hoboken) 64:2–8

    Article  Google Scholar 

  7. Canalis E, Mazziotti G, Giustina A, Bilezikian JP (2007) Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int 18:1319–1328

    Article  CAS  PubMed  Google Scholar 

  8. Kanis JA, Johansson H, Oden A, Johnell O, De LC, Melton Iii LJ et al (2004) A meta-analysis of prior corticosteroid use and fracture risk. J Bone Miner Res 19:893–899

    Article  PubMed  Google Scholar 

  9. Natsui K, Tanaka K, Suda M, Yasoda A, Sakuma Y, Ozasa A et al (2006) High-dose glucocorticoid treatment induces rapid loss of trabecular BMD and lean body mass. Osteoporos Int 17:105–108

    Article  CAS  PubMed  Google Scholar 

  10. Ton FN, Gunawardene SC, Lee H, Neer RM (2005) Effects of low-dose prednisone on bone metabolism. J Bone Miner Res 20:464–470

    Article  CAS  PubMed  Google Scholar 

  11. 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 

  12. Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S (2010) Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res 25:983–993

    Article  PubMed Central  PubMed  Google Scholar 

  13. MacNeil JA, Boyd SK (2008) Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42:1203–1213

    Article  PubMed  Google Scholar 

  14. Vilayphiou N, Boutroy S, Sornay-Rendu E, Van Rietbergen B, Munoz F, Delmas PD et al (2010) Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in postmenopausal women. Bone 46:1030–1037

    Article  PubMed  Google Scholar 

  15. Vilayphiou N, Boutroy S, Szulc P, Van Rietbergen B, Munoz F, Delmas PD et al (2011) Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res 26:965–973

    Article  PubMed  Google Scholar 

  16. Cheung AM, Adachi JD, Hanley DA, Kendler DL, Davison KS, Josse R et al (2013) High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep 11:136–146

    Article  PubMed Central  PubMed  Google Scholar 

  17. Tang XL, Qin L, Kwok AW, Zhu TY, Kun EW, Hung VW et al (2013) Alterations of bone geometry, density, microarchitecture, and biomechanical properties in systemic lupus erythematosus on long-term glucocorticoid: a case-control study using HR-pQCT. Osteoporos Int 24:1817–1826

    Article  CAS  PubMed  Google Scholar 

  18. Tang XL, Zhu TY, Hung VW, Qin L, Wong CK, Kun EW et al (2012) Increased organ damage associated with deterioration in volumetric bone density and bone microarchitecture in patients with systemic lupus erythematosus on longterm glucocorticoid therapy. J Rheumatol 39:1955–1963

    Article  PubMed  Google Scholar 

  19. Li EK, Zhu TY, Tam LS, Hung VW, Griffith JF, Li TK et al (2010) Bone microarchitecture assessment by high-resolution peripheral quantitative computed tomography in patients with systemic lupus erythematosus taking corticosteroids. J Rheumatol 37:1473–1479

    Article  CAS  PubMed  Google Scholar 

  20. Tang XL, Griffith JF, Qin L, Hung VW, Kwok AW, Zhu TY et al (2013) SLE disease per se contributes to deterioration in BMD, microstructure and bone strength. Lupus 22:1162–1168

    Article  CAS  PubMed  Google Scholar 

  21. Voss A, Green A, Junker P (1998) Systemic lupus erythematosus in Denmark: clinical and epidemiological characterization of a county-based cohort. Scand J Rheumatol 27:98–105

    Article  CAS  PubMed  Google Scholar 

  22. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF et al (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277

    Article  CAS  PubMed  Google Scholar 

  23. Gladman DD, Goldsmith CH, Urowitz MB, Bacon P, Fortin P, Ginzler E et al (2000) The systemic lupus international collaborating clinics/american college of rheumatology (SLICC/ACR) damage index for systemic lupus erythematosus international comparison. J Rheumatol 27:373–376

    CAS  PubMed  Google Scholar 

  24. Griffiths B, Mosca M, Gordon C (2005) Assessment of patients with systemic lupus erythematosus and the use of lupus disease activity indices. Best Pract Res Clin Rheumatol 19:685–708

    Article  PubMed  Google Scholar 

  25. Hansen S, Shanbhogue V, Folkestad L, Nielsen MM, Brixen K (2014) Bone microarchitecture and estimated strength in 499 adult Danish women and men: a cross-sectional, population-based high-resolution peripheral quantitative computed tomographic study on peak bone structure. Calcif Tissue Int 94:269–281

    Article  CAS  PubMed  Google Scholar 

  26. Hanson J (1997) Standardization of femur BMD. J Bone Miner Res 12:1316–1317

    Article  CAS  PubMed  Google Scholar 

  27. Laib A, Ruegsegger P (1999) Calibration of trabecular bone structure measurements of in vivo three-dimensional peripheral quantitative computed tomography with 28-microm-resolution microcomputed tomography. Bone 24:35–39

    Article  CAS  PubMed  Google Scholar 

  28. Muller R, Hildebrand T, Hauselmann HJ, Ruegsegger P (1996) In vivo reproducibility of three-dimensional structural properties of noninvasive bone biopsies using 3D-pQCT. J Bone Miner Res 11:1745–1750

    Article  CAS  PubMed  Google Scholar 

  29. Laib A, Hauselmann HJ, Ruegsegger P (1998) In vivo high resolution 3D-QCT of the human forearm. Technol Health Care 6:329–337

    CAS  PubMed  Google Scholar 

  30. Laib A, Hildebrand T, Hauselmann HJ, Ruegsegger P (1997) Ridge number density: a new parameter for in vivo bone structure analysis. Bone 21:541–546

    Article  CAS  PubMed  Google Scholar 

  31. Buie HR, Campbell GM, Klinck RJ, MacNeil JA, Boyd SK (2007) Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone 41:505–515

    Article  PubMed  Google Scholar 

  32. Nishiyama KK, Macdonald HM, Buie HR, Hanley DA, Boyd SK (2010) Postmenopausal women with osteopenia have higher cortical porosity and thinner cortices at the distal radius and tibia than women with normal aBMD: an in vivo HR-pQCT study. J Bone Miner Res 25:882–890

    PubMed  Google Scholar 

  33. Pistoia W, Van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Ruegsegger P (2002) Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone 30:842–848

    Article  CAS  PubMed  Google Scholar 

  34. Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S (2012) Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone 50:111–118

    Article  CAS  PubMed  Google Scholar 

  35. Schorlemmer S, Ignatius A, Claes L, Augat P (2005) Inhibition of cortical and cancellous bone formation in glucocorticoid-treated OVX sheep. Bone 37:491–496

    Article  CAS  PubMed  Google Scholar 

  36. Li EK, Zhu TY, Hung VY, Kwok AW, Lee VW, Lee KK et al (2010) Ibandronate increases cortical bone density in patients with systemic lupus erythematosus on long-term glucocorticoid. Arthritis Res Ther 12:R198

    Article  PubMed Central  PubMed  Google Scholar 

  37. Pang MY, Ashe MC, Eng JJ (2008) Tibial bone geometry in chronic stroke patients: influence of sex, cardiovascular health, and muscle mass. J Bone Miner Res 23:1023–1030

    Article  PubMed Central  PubMed  Google Scholar 

  38. Armbrecht G, Belavy DL, Backstrom M, Beller G, Alexandre C, Rizzoli R et al (2011) Trabecular and cortical bone density and architecture in women after 60 days of bed rest using high-resolution pQCT: WISE 2005. J Bone Miner Res 26:2399–2410

    Article  PubMed  Google Scholar 

  39. Toloza SM, Cole DE, Gladman DD, Ibanez D, Urowitz MB (2010) Vitamin D insufficiency in a large female SLE cohort. Lupus 19:13–19

    Article  CAS  PubMed  Google Scholar 

  40. Li EK, Tam LS, Young RP, Ko GT, Li M, Lau EM (1998) Loss of BMD in Chinese pre-menopausal women with systemic lupus erythematosus treated with corticosteroids. Br J Rheumatol 37:405–410

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Elsebeth Byrge for managing study logistics, and the technicians at the Osteoporosis Clinic, Odense University Hospital, for excellent technical support. Kim Brixen has received research support from Merck Sharpe & Dohme, Amgen Inc., Novartis and NPS Pharmaceuticals, served as a consultant for Merck Sharpe & Dohme and speaker for Servier, Amgen Inc., GlaxoSmithKline and Novartis.

Conflict of interest

Stinus Hansen, Claire Gudex, Fabian Åhrberg and Anne Voss state that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

The study was approved by the Regional Scientific Ethical Committee for Southern Denmark. All participants provided informed consent. The study did not involve experimental animals.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stinus Hansen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hansen, S., Gudex, C., Åhrberg, F. et al. Bone Geometry, Volumetric Bone Mineral Density, Microarchitecture and Estimated Bone Strength in Caucasian Females with Systemic Lupus Erythematosus. A Cross-Sectional Study Using HR-pQCT. Calcif Tissue Int 95, 530–539 (2014). https://doi.org/10.1007/s00223-014-9918-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-014-9918-8

Keywords

Navigation