Advertisement

Low bone mineral density of vertebral lateral projections can predict spinal radiographic damage in patients with ankylosing spondylitis

  • Ji-Won Kim
  • Min Kyung Chung
  • Jennifer Lee
  • Seung-Ki Kwok
  • Wan-Uk Kim
  • Sung-Hwan Park
  • Ji Hyeon JuEmail author
Original Article
  • 22 Downloads

Abstract

Objectives

To investigate the association between bone mineral status and spinal radiographic damage in patients with ankylosing spondylitis (AS) and determine whether bone mineral status can predict further spinal radiographic damage after 2 years.

Methods

Bone mineral density (BMD) of the lumbar spine (anteroposterior and lateral projections), femoral neck, and total hip and trabecular bone score (TBS) of the lumbar spine were measured in AS patients (n = 54) who fulfilled the modified New York criteria. Spinal radiographic damage was scored on cervical and lumbar spine radiographs using modified Stoke Ankylosing Spondylitis Spinal Score (mSASSS) at baseline and after 2 years. Simple and multiple linear regression analyses were performed to examine predictors of spinal radiographic damage.

Results

Patients with advanced AS exhibited low BMD on lumbar spine lateral projections, femoral neck, and total hip and low TBS. Low vertebral bone mass at baseline, assessed by BMD of the lateral projections or TBS, was independently associated with baseline mSASSS. After 2 years, mSASSS change from baseline was significantly associated with high baseline mSASSS, high baseline erythrocyte sedimentation rate and C-reactive protein (CRP) levels, and low baseline BMD of the lumbar spine lateral projections. The best predictive model for spinal radiographic progression consisted of baseline mSASSS, baseline CRP, and low BMD of lateral lumbar spine (area under curve = 0.826).

Conclusions

BMD at vertebral lateral projections and TBS were inversely associated with baseline mSASSS in AS patients. Low BMD at vertebral lateral projections, as well as baseline mSASSS and inflammatory markers, might predict spinal radiographic damage in AS.

Key Points

Vertebral bone mineral density of lateral projections and trabecular bone score are inversely associated with baseline mSASSS in patients with ankylosing spondylitis.

Baseline mSASSS, inflammatory markers, and low vertebral bone mineral density might predict spinal radiographic progression in patients with ankylosing spondylitis.

Keywords

Ankylosing spondylitis Bone density Disease progression Osteoporosis 

Notes

Compliance with ethical standards

Informed consent was obtained from the study participants. This study was approved by the ethics committee of Seoul St. Mary’s hospital, the Catholic University of Korea (KC15OISI0012) and was performed in accordance with the Declaration of Helsinki.

Disclosures

None.

Supplementary material

10067_2019_4743_MOESM1_ESM.pdf (258 kb)
ESM 1 (PDF 257 kb)

References

  1. 1.
    Klingberg E, Lorentzon M, Mellstrom D, Geijer M, Gothlin J, Hilme E, Hedberg M, Carlsten H, Forsblad-d'Elia H (2012) Osteoporosis in ankylosing spondylitis - prevalence, risk factors and methods of assessment. Arthritis Res Ther 14:R108.  https://doi.org/10.1186/ar3833 CrossRefGoogle Scholar
  2. 2.
    van der Weijden MA, Claushuis TA, Nazari T, Lems WF, Dijkmans BA, van der Horst-Bruinsma IE (2012) High prevalence of low bone mineral density in patients within 10 years of onset of ankylosing spondylitis: a systematic review. Clin Rheumatol 31:1529–1535.  https://doi.org/10.1007/s10067-012-2018-0 CrossRefGoogle Scholar
  3. 3.
    Wang DM, Zeng QY, Chen SB, Gong Y, Hou ZD, Xiao ZY (2015) Prevalence and risk factors of osteoporosis in patients with ankylosing spondylitis: a 5-year follow-up study of 504 cases. Clin Exp Rheumatol 33:465–470Google Scholar
  4. 4.
    Magrey MN, Lewis S, Asim Khan M (2016) Utility of DXA scanning and risk factors for osteoporosis in ankylosing spondylitis-a prospective study. Semin Arthritis Rheum 46:88–94.  https://doi.org/10.1016/j.semarthrit.2016.03.003 CrossRefGoogle Scholar
  5. 5.
    Jun JB, Joo KB, Her MY, Kim TH, Bae SC, Yoo DH, Kim SK (2006) Femoral bone mineral density is associated with vertebral fractures in patients with ankylosing spondylitis: a cross-sectional study. J Rheumatol 33:1637–1641Google Scholar
  6. 6.
    Klingberg E, Geijer M, Gothlin J, Mellstrom D, Lorentzon M, Hilme E, Hedberg M, Carlsten H, Forsblad-D'Elia H (2012) Vertebral fractures in ankylosing spondylitis are associated with lower bone mineral density in both central and peripheral skeleton. J Rheumatol 39:1987–1995.  https://doi.org/10.3899/jrheum.120316 CrossRefGoogle Scholar
  7. 7.
    Pray C, Feroz NI, Nigil Haroon N (2017) Bone mineral density and fracture risk in ankylosing spondylitis: a meta-analysis. Calcif Tissue Int 101:182–192.  https://doi.org/10.1007/s00223-017-0274-3 CrossRefGoogle Scholar
  8. 8.
    Kang KY, Chung MK, Kim HN, Hong YS, Ju JH, Park SH (2018) Severity of sacroiliitis and erythrocyte sedimentation rate are associated with a low trabecular bone score in young male patients with ankylosing spondylitis. J Rheumatol 45:349–356.  https://doi.org/10.3899/jrheum.170079 CrossRefGoogle Scholar
  9. 9.
    Del Rio L, Pons F, Huguet M, Setoain FJ, Setoain J (1995) Anteroposterior versus lateral bone mineral density of spine assessed by dual X-ray absorptiometry. Eur J Nucl Med 22:407–412CrossRefGoogle Scholar
  10. 10.
    Gilgil E, Kacar C, Tuncer T, Butun B (2005) The association of syndesmophytes with vertebral bone mineral density in patients with ankylosing spondylitis. J Rheumatol 32:292–294Google Scholar
  11. 11.
    Mermerci Baskan B, Pekin Dogan Y, Sivas F, Bodur H, Ozoran K (2010) The relation between osteoporosis and vitamin D levels and disease activity in ankylosing spondylitis. Rheumatol Int 30:375–381.  https://doi.org/10.1007/s00296-009-0975-7 CrossRefGoogle Scholar
  12. 12.
    Ulu MA, Cevik R, Dilek B (2013) Comparison of PA spine, lateral spine, and femoral BMD measurements to determine bone loss in ankylosing spondylitis. Rheumatol Int 33:1705–1711.  https://doi.org/10.1007/s00296-012-2632-9 CrossRefGoogle Scholar
  13. 13.
    Klingberg E, Lorentzon M, Gothlin J, Mellstrom D, Geijer M, Ohlsson C, Atkinson EJ, Khosla S, Carlsten H, Forsblad-d’Elia H (2013) Bone microarchitecture in ankylosing spondylitis and the association with bone mineral density, fractures, and syndesmophytes. Arthritis Res Ther 15:R179.  https://doi.org/10.1186/ar4368 CrossRefGoogle Scholar
  14. 14.
    Lee YS, Schlotzhauer T, Ott SM, van Vollenhoven RF, Hunter J, Shapiro J, Marcus R, McGuire JL (1997) Skeletal status of men with early and late ankylosing spondylitis. Am J Med 103:233–241CrossRefGoogle Scholar
  15. 15.
    Carter S, Lories RJ (2011) Osteoporosis: a paradox in ankylosing spondylitis. Curr Osteoporos Rep 9:112–115.  https://doi.org/10.1007/s11914-011-0058-z CrossRefGoogle Scholar
  16. 16.
    Grazio S, Kusic Z, Cvijetic S, Grubisic F, Balenovic A, Nemcic T, Matijevic-Mikelic V, Punda M, Sieper J (2012) Relationship of bone mineral density with disease activity and functional ability in patients with ankylosing spondylitis: a cross-sectional study. Rheumatol Int 32:2801–2808.  https://doi.org/10.1007/s00296-011-2066-9 CrossRefGoogle Scholar
  17. 17.
    Obermayer-Pietsch BM, Lange U, Tauber G, Fruhauf G, Fahrleitner A, Dobnig H, Hermann J, Aglas F, Teichmann J, Neeck G, Leb G (2003) Vitamin D receptor initiation codon polymorphism, bone density and inflammatory activity of patients with ankylosing spondylitis. Osteoporos Int 14:995–1000.  https://doi.org/10.1007/s00198-003-1501-5 CrossRefGoogle Scholar
  18. 18.
    Deminger A, Klingberg E, Lorentzon M, Geijer M, Gothlin J, Hedberg M, Rehnberg E, Carlsten H, Jacobsson LT, Forsblad-d'Elia H (2017) Which measuring site in ankylosing spondylitis is best to detect bone loss and what predicts the decline: results from a 5-year prospective study. Arthritis Res Ther 19:273.  https://doi.org/10.1186/s13075-017-1480-0 CrossRefGoogle Scholar
  19. 19.
    Maillefert JF, Aho LS, El Maghraoui A, Dougados M, Roux C (2001) Changes in bone density in patients with ankylosing spondylitis: a two-year follow-up study. Osteoporos Int 12:605–609.  https://doi.org/10.1007/s001980170084 CrossRefGoogle Scholar
  20. 20.
    Kang KY, Lee KY, Kwok SK, Ju JH, Park KS, Hong YS, Kim HY, Park SH (2011) The change of bone mineral density according to treatment agents in patients with ankylosing spondylitis. Joint Bone Spine 78:188–193.  https://doi.org/10.1016/j.jbspin.2010.05.010 CrossRefGoogle Scholar
  21. 21.
    Li H, Li Q, Chen X, Ji C, Gu J (2015) Anti-tumor necrosis factor therapy increased spine and femoral neck bone mineral density of patients with active ankylosing spondylitis with low bone mineral density. J Rheumatol 42:1413–1417.  https://doi.org/10.3899/jrheum.150019 CrossRefGoogle Scholar
  22. 22.
    Sarikaya S, Basaran A, Tekin Y, Ozdolap S, Ortancil O (2007) Is osteoporosis generalized or localized to central skeleton in ankylosing spondylitis? J Clin Rheumatol 13:20–24.  https://doi.org/10.1097/01.rhu.0000255688.83037.42 CrossRefGoogle Scholar
  23. 23.
    Deminger A, Klingberg E, Geijer M, Gothlin J, Hedberg M, Rehnberg E, Carlsten H, Jacobsson LT, Forsblad-d’Elia H (2018) A five-year prospective study of spinal radiographic progression and its predictors in men and women with ankylosing spondylitis. Arthritis Res Ther 20:162.  https://doi.org/10.1186/s13075-018-1665-1 CrossRefGoogle Scholar
  24. 24.
    Chiowchanwisawakit P, Lambert RG, Conner-Spady B, Maksymowych WP (2011) Focal fat lesions at vertebral corners on magnetic resonance imaging predict the development of new syndesmophytes in ankylosing spondylitis. Arthritis Rheum 63:2215–2225.  https://doi.org/10.1002/art.30393 CrossRefGoogle Scholar
  25. 25.
    Maksymowych WP, Morency N, Conner-Spady B, Lambert RG (2013) Suppression of inflammation and effects on new bone formation in ankylosing spondylitis: evidence for a window of opportunity in disease modification. Ann Rheum Dis 72:23–28.  https://doi.org/10.1136/annrheumdis-2011-200859 CrossRefGoogle Scholar
  26. 26.
    Karberg K, Zochling J, Sieper J, Felsenberg D, Braun J (2005) Bone loss is detected more frequently in patients with ankylosing spondylitis with syndesmophytes. J Rheumatol 32:1290–1298Google Scholar
  27. 27.
    van der Linden S, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 27:361–368CrossRefGoogle Scholar
  28. 28.
    Kanis JA (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO study group. Osteoporos Int 4:368–381CrossRefGoogle Scholar
  29. 29.
    Gordon CM, Leonard MB, Zemel BS (2014) 2013 pediatric position development conference: executive summary and reflections. J Clin Densitom 17:219–224.  https://doi.org/10.1016/j.jocd.2014.01.007 CrossRefGoogle Scholar
  30. 30.
    Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29:518–530.  https://doi.org/10.1002/jbmr.2176 CrossRefGoogle Scholar
  31. 31.
    Creemers MC, Franssen MJ, van't Hof MA, Gribnau FW, van de Putte LB, van Riel PL (2005) Assessment of outcome in ankylosing spondylitis: an extended radiographic scoring system. Ann Rheum Dis 64:127–129.  https://doi.org/10.1136/ard.2004.020503 CrossRefGoogle Scholar
  32. 32.
    Kang KY, Goo HY, Park SH, Hong YS (2018) Trabecular bone score as an assessment tool to identify the risk of osteoporosis in axial spondyloarthritis: a case-control study. Rheumatology (Oxford) 57:587.  https://doi.org/10.1093/rheumatology/kex431 CrossRefGoogle Scholar
  33. 33.
    Arends S, Spoorenberg A, Efde M, Bos R, Leijsma MK, Bootsma H, Veeger NJ, Brouwer E, van der Veer E (2014) Higher bone turnover is related to spinal radiographic damage and low bone mineral density in ankylosing spondylitis patients with active disease: a cross-sectional analysis. PLoS One 9:e99685.  https://doi.org/10.1371/journal.pone.0099685 CrossRefGoogle Scholar
  34. 34.
    Davey-Ranasinghe N, Deodhar A (2013) Osteoporosis and vertebral fractures in ankylosing spondylitis. Curr Opin Rheumatol 25:509–516.  https://doi.org/10.1097/BOR.0b013e3283620777 CrossRefGoogle Scholar
  35. 35.
    Arends S, Spoorenberg A, Bruyn GA, Houtman PM, Leijsma MK, Kallenberg CG, Brouwer E, van der Veer E (2011) The relation between bone mineral density, bone turnover markers, and vitamin D status in ankylosing spondylitis patients with active disease: a cross-sectional analysis. Osteoporos Int 22:1431–1439.  https://doi.org/10.1007/s00198-010-1338-7 CrossRefGoogle Scholar
  36. 36.
    Maksymowych WP, Elewaut D, Schett G (2012) Motion for debate: the development of ankylosis in ankylosing spondylitis is largely dependent on inflammation. Arthritis Rheum 64:1713–1719.  https://doi.org/10.1002/art.34442 CrossRefGoogle Scholar
  37. 37.
    Magrey MN, Khan MA (2017) The paradox of bone formation and bone loss in ankylosing spondylitis: evolving new concepts of bone formation and future trends in management. Curr Rheumatol Rep 19:17.  https://doi.org/10.1007/s11926-017-0644-x CrossRefGoogle Scholar
  38. 38.
    Poddubnyy D, Haibel H, Listing J, Marker-Hermann E, Zeidler H, Braun J, Sieper J, Rudwaleit M (2012) Baseline radiographic damage, elevated acute-phase reactant levels, and cigarette smoking status predict spinal radiographic progression in early axial spondylarthritis. Arthritis Rheum 64:1388–1398.  https://doi.org/10.1002/art.33465 CrossRefGoogle Scholar
  39. 39.
    Kim HR, Hong YS, Park SH, Ju JH, Kang KY (2018) Low bone mineral density predicts the formation of new syndesmophytes in patients with axial spondyloarthritis. Arthritis Res Ther 20:231.  https://doi.org/10.1186/s13075-018-1731-8 CrossRefGoogle Scholar
  40. 40.
    Larnach TA, Boyd SJ, Smart RC, Butler SP, Rohl PG, Diamond TH (1992) Reproducibility of lateral spine scans using dual energy X-ray absorptiometry. Calcif Tissue Int 51:255–258CrossRefGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2019

Authors and Affiliations

  • Ji-Won Kim
    • 1
    • 2
  • Min Kyung Chung
    • 3
  • Jennifer Lee
    • 1
  • Seung-Ki Kwok
    • 1
  • Wan-Uk Kim
    • 1
  • Sung-Hwan Park
    • 1
  • Ji Hyeon Ju
    • 1
    Email author
  1. 1.Division of Rheumatology, Department of Internal Medicine, Seoul St. Mary’s Hospital, College of MedicineThe Catholic University of KoreaSeoulSouth Korea
  2. 2.Division of Rheumatology, Department of Internal MedicineCatholic University of Daegu School of MedicineDaeguSouth Korea
  3. 3.Division of Rheumatology, Department of Internal MedicineEwha Womans University College of MedicineSeoulSouth Korea

Personalised recommendations