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Bone impairment assessed by HR-pQCT in juvenile-onset systemic lupus erythematosus

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Abstract

Summary

High-resolution peripheral quantitative computed tomography (HR-pQCT) analysis of female juvenile-onset systemic lupus erythematosus (JoSLE) patients revealed trabecular/cortical bone damage and reduced bone strength primarily at the distal radius compared to healthy controls. We demonstrated for the first time that JoSLE patients with vertebral fracture (VF) present trabecular impairment at the distal radius.

Introduction

This study investigated the volumetric bone mineral density (vBMD), microarchitecture, and biomechanical features at the distal radius and tibia using HR-pQCT and laboratory bone markers in JoSLE patients compared to controls to determine whether this method discriminates JoSLE patients with or without VF.

Methods

We compared 56 female JoSLE patients to age- and Tanner-matched healthy controls. HR-pQCT was performed at the distal radius and tibia. Serum levels of the amino-terminal pro-peptide of type I collagen, the C-terminal telopeptide of type I collagen, intact parathormone, sclerostin, and 25-hydroxyvitamin D (25OHD) were evaluated. VFs were analyzed using VFA-dual-energy X-ray absorptiometry (DXA) (Genant’s method).

Results

Reduced density and strength parameters and microarchitecture alterations of cortical and trabecular bones were observed in JoSLE patients compared to controls, primarily at the distal radius (p < 0.05). Patients with VF exhibited a significant decrease in trabecular bone parameters solely at the distal radius (Total.BMD, p = 0.034; Trabecular.BMD [Tb.BMD], p = 0.034; bone volume (BV)/trabecular volume (TV), p = 0.034; apparent modulus, p = 0.039) and higher scores for disease damage (Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index (SLICC/ACR-DI), p = 0.002). Bone metabolism markers were similar in all groups. Logistic regression analysis of parameters that were significant in univariate analysis revealed that Tb.BMD (OR 0.98, 95 % CI 0.95–0.99, p = 0.039) and SLICC/ACR-DI (OR 7.37, 95 % CI 1.75–30.97, p = 0.006) were independent risk factors for VF.

Conclusion

In conclusion, this study is the first demonstration of bone microstructure and strength deficits in JoSLE patients, particularly at the distal radius. Our results demonstrated that VF was associated with trabecular radius alteration and emphasized the potential detrimental effect of disease damage on this condition.

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References

  1. Lee C, Ramsey-Goldman R (2005) Osteoporosis in systemic lupus erythematosus mechanisms. Rheum Clin North Am 31:363–385, viii

    Article  Google Scholar 

  2. Burnham JM, Leonard MB (2004) Bone disease in pediatric rheumatologic disorders. Curr Rheumatol Rep 6(1):70–78, Review

    Article  PubMed  Google Scholar 

  3. Hernandez CJ, Beaupré GS, Carter DR (2003) A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteopath Int 14:843–847

    Article  CAS  Google Scholar 

  4. 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 

  5. Santiago RA, Silva CA, Caparbo VF et al (2008) Bone mineral apparent density in juvenile dermatomyositis: the role of lean body mass and glucocorticoid use. Scand J Rheumatol 37(1):40–47

    Article  CAS  PubMed  Google Scholar 

  6. Tan EM, Cohen AS, Fries JF et al (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25:1271–1277

    Article  CAS  PubMed  Google Scholar 

  7. Duke PM, Litt IF, Gross RT (1980) Adolescents’ self-assessment of sexual maturation. Pediatrics 66:918–920

    CAS  PubMed  Google Scholar 

  8. Farias Junior JC, Lopes AS, Mota J et al (2012) Validity and reproductibility of a physical activity questionnaire for adolescents: adapting the self-administered physical activity checklist. Rev Bras Epidemiol 15:198–210

    Article  Google Scholar 

  9. Ibanez D, Gladman DD, Urowitz MB (2005) Adjusted mean Systemic Lupus Erythematosus Disease Activity Index-2K is a predictor of outcome in SLE. J Rheumatol 32:824–827

    PubMed  Google Scholar 

  10. Gladman D, Ginzler E, Goldsmith C et al (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 39:363–369

    Article  CAS  PubMed  Google Scholar 

  11. Domiciano DS, Figueiredo CP, Lopes JB et al (2013) Vertebral fracture assessment by dual X-ray absorptiometry: a valid tool to detect vertebral fractures in community-dwelling older adults in a population-based survey. Arthritis Care Res 65(5):809–815

    Article  CAS  Google Scholar 

  12. Seguro LP, Casella CB, Caparbo VF et al (2015) Lower P1NP serum levels: a predictive marker of bone loss after 1 year follow-up in premenopausal systemic lupus erythematosus patients. Osteoporos Int 26(2):459–467

    Article  CAS  PubMed  Google Scholar 

  13. Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative method. J Bone Miner Res 8:1137–1148

    Article  CAS  PubMed  Google Scholar 

  14. Siminoski K, Lee KC, Jen H et al. (2012) Anatomical distribution of vertebral fractures: a comparison of pediatric and adult spine STOPP Consortium. Osteoporos Int 23(7): 1999–2008.

  15. Fuller H, Fuller R, Pereira RMR (2015) High resolution peripheral quantitative computed tomography (HR-pQCT) for the assessment of morphological and mechanical bone parameters. Rev Bras Reumatol 55(4):352–362

    Article  PubMed  Google Scholar 

  16. Burrows M, Liu D, Perdios A et al (2010) Assessing bone microstructure at the distal radius in children and adolescents using HR-pQCT: a methodological pilot study. J Clin Densitom 13(4):451–455

    Article  PubMed  Google Scholar 

  17. Burghardt AJ, Pialat JB, Kazakia GJ et al (2013) Multicenter precision of cortical and trabecular bone quality measures assessed by high-resolution peripheral quantitative computed tomography. J Bone Miner Res 28(3):524–536

    Article  PubMed  PubMed Central  Google Scholar 

  18. Saad CG, Ribeiro AC, Moraes JC et al (2012) Low sclerostin levels: a predictive marker of persistent inflammation in ankylosing spondylitis during anti-tumor necrosis factor therapy? Arthritis Res Ther 14(5):R216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tang XL, Griffith JF, Qin L et al (2013) SLE disease per se contributes to deterioration in bone mineral density, microstructure and bone strength. Lupus 22(11):1162–1168

    Article  CAS  PubMed  Google Scholar 

  20. Kirmani S, Christen D, van Lenthe GH et al (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24(6):1033–1042

    Article  PubMed  PubMed Central  Google Scholar 

  21. Beerhorst K, Tan IY, De Krom M et al (2013) Antiepileptic drugs and high prevalence of low bone mineral density in a group of inpatients with chronic epilepsy. Acta Neurol Scand 128(4):273–280

    Article  CAS  PubMed  Google Scholar 

  22. Arya V, Bhambri R, Godbole MM, Mithal A (2004) Vitamin D status and its relationship with bone mineral density in healthy Asian Indians. Osteoporos Int 15(1):56–61

    Article  CAS  PubMed  Google Scholar 

  23. Sasimontonkul S, Bay BK, Pavol MJ (2007) Bone contact forces on the distal tibia during the stance phase of running. J Biomech 40(15):3503–3509

    Article  PubMed  Google Scholar 

  24. Wehner T, Claes L, Simon U (2009) Internal loads in the human tibia during gait. Clin Biomech (Bristol, Avon) 24(3):299–302

    Article  Google Scholar 

  25. Burr BD, Matrtin RB (1983) The effects of composition, structure and age on the torsional properties of the human radius. J Biomech 16:603–608

    Article  CAS  PubMed  Google Scholar 

  26. Paggiosi MA, Eastell R, Walsh JS (2014) Precision of high-resolution peripheral quantitative computed tomography measurement variables: influence of gender, examination site, and age. Calcif Tissue Int 94(2):191–201

    Article  CAS  PubMed  Google Scholar 

  27. Regio P, Bonfá E, Takayama L, Pereira RM (2008) The influence of lean mass in trabecular and cortical bone in juvenile onset systemic lupus erythematosus. Lupus 17:787–792

    Article  PubMed  Google Scholar 

  28. Borba VZ, Matos PG, da Silva Viana PR et al (2005) High prevalence of vertebral deformity in premenopausal systemic lupus erythematosus patients. Lupus 14(7):529–533

    Article  CAS  PubMed  Google Scholar 

  29. Almehed K, Hetényi S, Ohlsson C et al (2010) Prevalence and risk factors of vertebral compression fractures in female SLE patients. Arthritis Res Ther 12(4):R153

    Article  PubMed  PubMed Central  Google Scholar 

  30. LeBlanc CM, Ma J, Taljaard M et al (2015) Canadian STeroid-associated osteoporosis in the pediatric population (STOPP) consortium. Incident vertebral fractures and risk factors in the first three years following glucocorticoid initiation among pediatric patients with rheumatic disorders. J Bone Miner Res 30(9):1667–1675

    Article  CAS  PubMed  Google Scholar 

  31. Rodd C, Lang B, Ramsay T et al (2012) Canadian Steroid-Associated Osteoporosis in the Pediatric Population (STOPP) Consortium. Incident vertebral fractures among children with rheumatic disorders 12 months after glucocorticoid initiation: a national observational study. Arthritis Care Res 64(1):122–131

    Article  Google Scholar 

  32. Huber AM, Gaboury I, Cabral DA et al (2010) Canadian steroid-associated osteoporosis in the pediatric population (STOPP) consortium. Prevalent vertebral fractures among children initiating glucocorticoid therapy for the treatment of rheumatic disorders. Arthritis Care Res 62(4):516–526

    Article  CAS  Google Scholar 

  33. Rouster-Stevens KA, Klein-Gitelman MS (2005) Bone health in pediatric rheumatic disease. Curr Opin Pediatr 17:703–708

    Article  PubMed  Google Scholar 

  34. Viswanathan A, Sylvester FA (2008) Chronic pediatric inflammatory diseases: effects on bone. Rev Endocr Metab Disord 9:107–122

    Article  PubMed  Google Scholar 

  35. Bultink IEM (2012) Osteoporosis and fractures in systemic lupus erythematosus. Arthritis Care Res 64(1):2–8

    Article  Google Scholar 

  36. Tang XL, Qin L, Kwok AW 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(6):1817–1826

    Article  CAS  PubMed  Google Scholar 

  37. Bultink IE, Lems WF, Kostense PJ et al (2005) Prevalence of and risk factors for low bone mineral density and vertebral fractures in patients with systemic lupus erythematosus. Arthritis Rheum 52(7):2044–2050

    Article  PubMed  Google Scholar 

  38. Kalla AA, Fataar AB, Jessop SJ, Bewerunge L (1993) Loss of trabecular bone mineral density in systemic lupus erythematosus. Arthritis Rheum 36:1726–1734

    Article  CAS  PubMed  Google Scholar 

  39. Yee CS, Crabtree N, Skan J et al (2005) Prevalence and predictors of fragility fractures in systemic lupus erythematosus. Ann Rheum Dis 64(1):111–113

    Article  PubMed  PubMed Central  Google Scholar 

  40. Vasikaran S, Eastell R, Bruyère O et al. (2011) IOF-IFCC Bone Marker Standards Working Group. 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.

  41. Bhattoa HP, Bettembuk P, Balogh A et al (2004) The effect of 1-year transdermal estrogen replacement therapy on bone mineral density and biochemical markers of bone turnover in osteopenic postmenopausal systemic lupus erythematosus patients: a randomized, double-blind, placebo-controlled trial. Osteoporos Int 15(5):396–404

    Article  CAS  PubMed  Google Scholar 

  42. Tang XL, Zhu TY, Hung VW 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(10):1955–1963

    Article  PubMed  Google Scholar 

  43. Dhillon VB, Davies MC, Hall ML et al (1990) Assessment of the effect of oral corticosteroids on bone mineral density in systemic lupus erythematosus: a preliminary study with dual energy x ray absorptiometry. Ann Rheum Dis 49(8):624–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hansen M, Halberg P, Kollerup G et al (1998) Bone metabolism in patients with systemic lupus erythematosus: effect of disease activity and glucocorticoid treatment. Scand J Rheumatol 27(3):197–206

    Article  CAS  PubMed  Google Scholar 

  45. Pineau CA, Urowitz MB, Fortin PJ et al (2004) Osteoporosis in systemic lupus erythematosus: factors associated with referral for bone mineral density studies, prevalence of osteoporosis and factors associated with reduced bone density. Lupus 13(6):436–441

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Prof J. M. Burnham, Pediatric Rheumatology, The Children’s Hospital of Philadelphia, University of Philadelphia, USA for revising the paper and Rogerio Ruscuitto, PhD for the statistical analysis.

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Authors and Affiliations

  1. Bone Metabolism Laboratory, Rheumatology Division, Faculdade de Medicina da Universidade de São Paulo, Av Dr Arnaldo, 455, 3° Andar, Sala 3193, Sao Paulo, SP, 01246-903, Brazil

    J. A. Paupitz, G. L. Lima, J. C. Alvarenga, E. Bonfa & R. M. R. Pereira

  2. RDO Diagnosticos Medicos, Sao Paulo, Brazil

    R. M. Oliveira

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  1. J. A. Paupitz
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  2. G. L. Lima
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  3. J. C. Alvarenga
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  4. R. M. Oliveira
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  5. E. Bonfa
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  6. R. M. R. Pereira
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Corresponding author

Correspondence to R. M. R. Pereira.

Ethics declarations

The Local Ethics Committee approved the study, and written informed consent was obtained from all participants or their legal guardians.

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None.

Funding statement

This study was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ #472754/2013-0), individual grants (CNPQ #301805/2013-0 to RMRP and #301411/2009-3 to EB) and Federico Foundation grants (to RMRP and EB).

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Paupitz, J.A., Lima, G.L., Alvarenga, J.C. et al. Bone impairment assessed by HR-pQCT in juvenile-onset systemic lupus erythematosus. Osteoporos Int 27, 1839–1848 (2016). https://doi.org/10.1007/s00198-015-3461-y

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  • DOI: https://doi.org/10.1007/s00198-015-3461-y

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