Skip to main content
Top
Published in: Arthritis Research & Therapy 1/2017

Open Access 01-12-2017 | Research article

Which measuring site in ankylosing spondylitis is best to detect bone loss and what predicts the decline: results from a 5-year prospective study

Authors: Anna Deminger, Eva Klingberg, Mattias Lorentzon, Mats Geijer, Jan Göthlin, Martin Hedberg, Eva Rehnberg, Hans Carlsten, Lennart T. Jacobsson, Helena Forsblad-d’Elia

Published in: Arthritis Research & Therapy | Issue 1/2017

Login to get access

Abstract

Background

Studies have shown increased prevalence of osteoporosis and increased risk for vertebral fractures in patients with ankylosing spondylitis (AS). Measurements of bone mineral density (BMD) in the lumbar spine anterior-posterior (AP) projection may be difficult to interpret due to the ligamentous calcifications, and the lateral projection might be a better measuring site. Our objectives were to investigate BMD changes after 5 years at different measuring sites in patients with AS and to evaluate disease-related variables and medications as predictors for BMD changes.

Methods

In a longitudinal study, BMD in Swedish AS patients, 50 ± 13 years old, was measured with dual-energy x-ray absorptiometry (DXA) at the hip, the lumbar spine AP and lateral projections, and the total radius at baseline and after 5 years. Patients were assessed with questionnaires, blood samples, and spinal radiographs for grading of AS-related alterations in the spine with the modified Stoke Ankylosing Spondylitis Spinal Score (mSASSS) and assessment of vertebral fractures by the Genant score. Multiple linear regression analyses were used to investigate predictors for BMD changes.

Results

Of 204 patients included at baseline, 168 (82%) were re-examined after 5 years (92 men and 76 women). BMD decreased significantly at the femoral neck and radius and increased significantly at the lumbar spine, both for AP and lateral projections. Mean C-reactive protein during follow-up predicted a decrease in the femoral neck BMD (change in %, β = –0.15, p = 0.046). Use of bisphosphonates predicted an increase in BMD at all measuring sites (p < 0.001 to 0.013), except for the total radius. Use of tumor necrosis factor inhibitors (TNFi) predicted an increase in AP spinal BMD (β = 3.15, p = 0.012).

Conclusion

The current study (which has a long follow-up, many measuring sites, and is the first to longitudinally assess the lateral projection of the spine in AS patients) surprisingly showed that lateral projection spinal BMD increased. This study suggests that the best site to assess bone loss in AS patients is the femoral neck and that inflammation has an adverse effect, and the use of bisphosphonates and TNFi has a positive effect, on BMD in AS patients.
Literature
1.
go back to reference Donnelly S, Doyle DV, Denton A, Rolfe I, McCloskey EV, Spector TD. Bone mineral density and vertebral compression fracture rates in ankylosing spondylitis. Ann Rheum Dis. 1994;53(2):117–21.CrossRefPubMedPubMedCentral Donnelly S, Doyle DV, Denton A, Rolfe I, McCloskey EV, Spector TD. Bone mineral density and vertebral compression fracture rates in ankylosing spondylitis. Ann Rheum Dis. 1994;53(2):117–21.CrossRefPubMedPubMedCentral
2.
go back to reference Mitra D, Elvins DM, Speden DJ, Collins AJ. The prevalence of vertebral fractures in mild ankylosing spondylitis and their relationship to bone mineral density. Rheumatology (Oxford). 2000;39(1):85–9.CrossRef Mitra D, Elvins DM, Speden DJ, Collins AJ. The prevalence of vertebral fractures in mild ankylosing spondylitis and their relationship to bone mineral density. Rheumatology (Oxford). 2000;39(1):85–9.CrossRef
3.
go back to reference Will R, Palmer R, Bhalla AK, Ring F, Calin A. Osteoporosis in early ankylosing spondylitis: a primary pathological event? Lancet. 1989;2(8678–8679):1483–5.CrossRefPubMed Will R, Palmer R, Bhalla AK, Ring F, Calin A. Osteoporosis in early ankylosing spondylitis: a primary pathological event? Lancet. 1989;2(8678–8679):1483–5.CrossRefPubMed
5.
go back to reference Cooper C, Carbone L, Michet C, Atkinson E, O'Fallon W, Melton L. Fracture risk in patients with ankylosing spondylitis: a population based study. J Rheumatol. 1994;21:1877–82.PubMed Cooper C, Carbone L, Michet C, Atkinson E, O'Fallon W, Melton L. Fracture risk in patients with ankylosing spondylitis: a population based study. J Rheumatol. 1994;21:1877–82.PubMed
6.
go back to reference Kanis JA. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. Osteoporos Int. 1994;4(6):368–81.CrossRefPubMed Kanis JA. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. Osteoporos Int. 1994;4(6):368–81.CrossRefPubMed
7.
go back to reference Lee Y, Schlotzhauer T, Ott S, van Vollenhoven R, Hunter J, Shapiro J. Skeletal status of men with early and late ankylosing spondylitis. Am J Med. 1997;103:233–41.CrossRefPubMed Lee Y, Schlotzhauer T, Ott S, van Vollenhoven R, Hunter J, Shapiro J. Skeletal status of men with early and late ankylosing spondylitis. Am J Med. 1997;103:233–41.CrossRefPubMed
8.
go back to reference Yu W, Gluer CC, Fuerst T, Grampp S, Li J, Lu Y, Genant HK. Influence of degenerative joint disease on spinal bone mineral measurements in postmenopausal women. Calcif Tissue Int. 1995;57(3):169–74.CrossRefPubMed Yu W, Gluer CC, Fuerst T, Grampp S, Li J, Lu Y, Genant HK. Influence of degenerative joint disease on spinal bone mineral measurements in postmenopausal women. Calcif Tissue Int. 1995;57(3):169–74.CrossRefPubMed
9.
go back to reference Gratacos J, Collado A, Pons F, Osaba M, Sanmarti R, Roque M. Significant loss of bone mass in patients with early, active ankylosing spondylitis: a follow-up study. Arthritis Rheum. 1999;42(11):2319–24.CrossRefPubMed Gratacos J, Collado A, Pons F, Osaba M, Sanmarti R, Roque M. Significant loss of bone mass in patients with early, active ankylosing spondylitis: a follow-up study. Arthritis Rheum. 1999;42(11):2319–24.CrossRefPubMed
10.
go back to reference Kaya A, Ozgocmen S, Kamanli A, Ardicoglu O. Bone loss in ankylosing spondylitis: does syndesmophyte formation have an influence on bone density changes? Med Princ Pract. 2009;18(6):470–6.CrossRefPubMed Kaya A, Ozgocmen S, Kamanli A, Ardicoglu O. Bone loss in ankylosing spondylitis: does syndesmophyte formation have an influence on bone density changes? Med Princ Pract. 2009;18(6):470–6.CrossRefPubMed
11.
go back to reference Maillefert JF, Aho LS, El Maghraoui A, Dougados M, Roux C. Changes in bone density in patients with ankylosing spondylitis: a two-year follow-up study. Osteoporos Int. 2001;12(7):605–9.CrossRefPubMed Maillefert JF, Aho LS, El Maghraoui A, Dougados M, Roux C. Changes in bone density in patients with ankylosing spondylitis: a two-year follow-up study. Osteoporos Int. 2001;12(7):605–9.CrossRefPubMed
12.
go back to reference Wang DM, Zeng QY, Chen SB, Gong Y, Hou ZD, Xiao ZY. Prevalence and risk factors of osteoporosis in patients with ankylosing spondylitis: a 5-year follow-up study of 504 cases. Clin Exp Rheumatol. 2015;33(4):465–70.PubMed Wang DM, Zeng QY, Chen SB, Gong Y, Hou ZD, Xiao ZY. Prevalence and risk factors of osteoporosis in patients with ankylosing spondylitis: a 5-year follow-up study of 504 cases. Clin Exp Rheumatol. 2015;33(4):465–70.PubMed
13.
go back to reference Haugeberg G, Bennett AN, McGonagle D, Emery P, Marzo-Ortega H. Bone loss in very early inflammatory back pain in undifferentiated spondyloarthropathy: a 1-year observational study. Ann Rheum Dis. 2010;69(7):1364–6.CrossRefPubMed Haugeberg G, Bennett AN, McGonagle D, Emery P, Marzo-Ortega H. Bone loss in very early inflammatory back pain in undifferentiated spondyloarthropathy: a 1-year observational study. Ann Rheum Dis. 2010;69(7):1364–6.CrossRefPubMed
14.
go back to reference Zmuda JM, Cauley JA, Glynn NW, Finkelstein JS. Posterior-anterior and lateral dual-energy x-ray absorptiometry for the assessment of vertebral osteoporosis and bone loss among older men. J Bone Miner Res. 2000;15(7):1417–24.CrossRefPubMed Zmuda JM, Cauley JA, Glynn NW, Finkelstein JS. Posterior-anterior and lateral dual-energy x-ray absorptiometry for the assessment of vertebral osteoporosis and bone loss among older men. J Bone Miner Res. 2000;15(7):1417–24.CrossRefPubMed
15.
go back to reference Melton 3rd LJ, Khosla S, Atkinson EJ, O’Connor MK, O’Fallon WM, Riggs BL. Cross-sectional versus longitudinal evaluation of bone loss in men and women. Osteoporos Int. 2000;11(7):592–9.CrossRefPubMed Melton 3rd LJ, Khosla S, Atkinson EJ, O’Connor MK, O’Fallon WM, Riggs BL. Cross-sectional versus longitudinal evaluation of bone loss in men and women. Osteoporos Int. 2000;11(7):592–9.CrossRefPubMed
16.
go back to reference van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum. 1984;27(4):361–8.CrossRefPubMed van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum. 1984;27(4):361–8.CrossRefPubMed
17.
go back to reference Calin A, Garrett S, Whitelock H, Kennedy LG, O'Hea J, Mallorie P, Jenkinson T. A new approach to defining functional ability in ankylosing spondylitis: the development of the Bath Ankylosing Spondylitis Functional Index. J Rheumatol. 1994;21(12):2281–5.PubMed Calin A, Garrett S, Whitelock H, Kennedy LG, O'Hea J, Mallorie P, Jenkinson T. A new approach to defining functional ability in ankylosing spondylitis: the development of the Bath Ankylosing Spondylitis Functional Index. J Rheumatol. 1994;21(12):2281–5.PubMed
18.
go back to reference Garrett S, Jenkinson T, Kennedy LG, Whitelock H, Gaisford P, Calin A. A new approach to defining disease status in ankylosing spondylitis: the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol. 1994;21(12):2286–91.PubMed Garrett S, Jenkinson T, Kennedy LG, Whitelock H, Gaisford P, Calin A. A new approach to defining disease status in ankylosing spondylitis: the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol. 1994;21(12):2286–91.PubMed
19.
go back to reference Jenkinson TR, Mallorie PA, Whitelock HC, Kennedy LG, Garrett SL, Calin A. Defining spinal mobility in ankylosing spondylitis (AS). The Bath AS Metrology Index. J Rheumatol. 1994;21(9):1694–8.PubMed Jenkinson TR, Mallorie PA, Whitelock HC, Kennedy LG, Garrett SL, Calin A. Defining spinal mobility in ankylosing spondylitis (AS). The Bath AS Metrology Index. J Rheumatol. 1994;21(9):1694–8.PubMed
20.
go back to reference Jones SD, Steiner A, Garrett SL, Calin A. The Bath Ankylosing Spondylitis Patient Global Score (BAS-G). Br J Rheumatol. 1996;35(1):66–71.CrossRefPubMed Jones SD, Steiner A, Garrett SL, Calin A. The Bath Ankylosing Spondylitis Patient Global Score (BAS-G). Br J Rheumatol. 1996;35(1):66–71.CrossRefPubMed
21.
go back to reference Lukas C, Landewe R, Sieper J, Dougados M, Davis J, Braun J, van der Linden S, van der Heijde D. Development of an ASAS-endorsed disease activity score (ASDAS) in patients with ankylosing spondylitis. Ann Rheum Dis. 2009;68(1):18–24.CrossRefPubMed Lukas C, Landewe R, Sieper J, Dougados M, Davis J, Braun J, van der Linden S, van der Heijde D. Development of an ASAS-endorsed disease activity score (ASDAS) in patients with ankylosing spondylitis. Ann Rheum Dis. 2009;68(1):18–24.CrossRefPubMed
22.
go back to reference van der Heijde D, Lie E, Kvien TK, Sieper J, Van den Bosch F, Listing J, Braun J, Landewe R. ASDAS, a highly discriminatory ASAS-endorsed disease activity score in patients with ankylosing spondylitis. Ann Rheum Dis. 2009;68(12):1811–8.CrossRefPubMed van der Heijde D, Lie E, Kvien TK, Sieper J, Van den Bosch F, Listing J, Braun J, Landewe R. ASDAS, a highly discriminatory ASAS-endorsed disease activity score in patients with ankylosing spondylitis. Ann Rheum Dis. 2009;68(12):1811–8.CrossRefPubMed
23.
go back to reference Dougados M, Simon P, Braun J, Burgos-Vargas R, Maksymowych WP, Sieper J, van der Heijde D. ASAS recommendations for collecting, analysing and reporting NSAID intake in clinical trials/epidemiological studies in axial spondyloarthritis. Ann Rheum Dis. 2011;70(2):249–51.CrossRefPubMed Dougados M, Simon P, Braun J, Burgos-Vargas R, Maksymowych WP, Sieper J, van der Heijde D. ASAS recommendations for collecting, analysing and reporting NSAID intake in clinical trials/epidemiological studies in axial spondyloarthritis. Ann Rheum Dis. 2011;70(2):249–51.CrossRefPubMed
24.
go back to reference Gordon CM, Leonard MB, Zemel BS. 2013 Pediatric Position Development Conference: executive summary and reflections. J Clin Densitom. 2014;17(2):219–24.CrossRefPubMed Gordon CM, Leonard MB, Zemel BS. 2013 Pediatric Position Development Conference: executive summary and reflections. J Clin Densitom. 2014;17(2):219–24.CrossRefPubMed
25.
go back to reference Creemers MC, Franssen MJ, van't Hof MA, Gribnau FW, van de Putte LB, van Riel PL. Assessment of outcome in ankylosing spondylitis: an extended radiographic scoring system. Ann Rheum Dis. 2005;64(1):127–9.CrossRefPubMed Creemers MC, Franssen MJ, van't Hof MA, Gribnau FW, van de Putte LB, van Riel PL. Assessment of outcome in ankylosing spondylitis: an extended radiographic scoring system. Ann Rheum Dis. 2005;64(1):127–9.CrossRefPubMed
26.
go back to reference Genant H, Wu C, van Kuijk C, Nevitt M. Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res. 1993;8:1137–48.CrossRefPubMed Genant H, Wu C, van Kuijk C, Nevitt M. Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res. 1993;8:1137–48.CrossRefPubMed
27.
go back to reference Kang KY, Lee KY, Kwok S-K, Ju JH, Park K-S, Hong YS, Kim H-Y, Park S-H. The change of bone mineral density according to treatment agents in patients with ankylosing spondylitis. Joint Bone Spine. 2011;78(2):188–93.CrossRefPubMed Kang KY, Lee KY, Kwok S-K, Ju JH, Park K-S, Hong YS, Kim H-Y, Park S-H. The change of bone mineral density according to treatment agents in patients with ankylosing spondylitis. Joint Bone Spine. 2011;78(2):188–93.CrossRefPubMed
28.
go back to reference Bone HG, Hosking D, Devogelaer JP, Tucci JR, Emkey RD, Tonino RP, Rodriguez-Portales JA, Downs RW, Gupta J, Santora AC, et al. Ten years’ experience with alendronate for osteoporosis in postmenopausal women. N Engl J Med. 2004;350(12):1189–99.CrossRefPubMed Bone HG, Hosking D, Devogelaer JP, Tucci JR, Emkey RD, Tonino RP, Rodriguez-Portales JA, Downs RW, Gupta J, Santora AC, et al. Ten years’ experience with alendronate for osteoporosis in postmenopausal women. N Engl J Med. 2004;350(12):1189–99.CrossRefPubMed
29.
go back to reference Gilgil E, Kacar C, Tuncer T, Butun B. The association of syndesmophytes with vertebral bone mineral density in patients with ankylosing spondylitis. J Rheumatol. 2005;32(2):292–4.PubMed Gilgil E, Kacar C, Tuncer T, Butun B. The association of syndesmophytes with vertebral bone mineral density in patients with ankylosing spondylitis. J Rheumatol. 2005;32(2):292–4.PubMed
30.
go back to reference Ulu MA, Cevik R, Dilek B. Comparison of PA spine, lateral spine, and femoral BMD measurements to determine bone loss in ankylosing spondylitis. Rheumatol Int. 2013;33(7):1705–11.CrossRefPubMed Ulu MA, Cevik R, Dilek B. Comparison of PA spine, lateral spine, and femoral BMD measurements to determine bone loss in ankylosing spondylitis. Rheumatol Int. 2013;33(7):1705–11.CrossRefPubMed
31.
go back to reference Klingberg E, Lorentzon M, Mellstrom D, Geijer M, Gothlin J, Hilme E, Hedberg M, Carlsten H, Forsblad-d'Elia H. Osteoporosis in ankylosing spondylitis—prevalence, risk factors and methods of assessment. Arthritis Res Ther. 2012;14(3):12.CrossRef Klingberg E, Lorentzon M, Mellstrom D, Geijer M, Gothlin J, Hilme E, Hedberg M, Carlsten H, Forsblad-d'Elia H. Osteoporosis in ankylosing spondylitis—prevalence, risk factors and methods of assessment. Arthritis Res Ther. 2012;14(3):12.CrossRef
32.
go back to reference Chapurlat RD, Garnero P, Sornay-Rendu E, Arlot ME, Claustrat B, Delmas PD. Longitudinal study of bone loss in pre- and perimenopausal women: evidence for bone loss in perimenopausal women. Osteoporos Int. 2000;11(6):493–8.CrossRefPubMed Chapurlat RD, Garnero P, Sornay-Rendu E, Arlot ME, Claustrat B, Delmas PD. Longitudinal study of bone loss in pre- and perimenopausal women: evidence for bone loss in perimenopausal women. Osteoporos Int. 2000;11(6):493–8.CrossRefPubMed
33.
go back to reference Tan S, Yao J, Flynn JA, Yao L, Ward MM. Quantitative measurement of syndesmophyte volume and height in ankylosing spondylitis using CT. Ann Rheum Dis. 2014;73(3):544–50.CrossRefPubMed Tan S, Yao J, Flynn JA, Yao L, Ward MM. Quantitative measurement of syndesmophyte volume and height in ankylosing spondylitis using CT. Ann Rheum Dis. 2014;73(3):544–50.CrossRefPubMed
34.
go back to reference Tan S, Yao J, Flynn JA, Yao L, Ward MM. Quantitative syndesmophyte measurement in ankylosing spondylitis using CT: longitudinal validity and sensitivity to change over 2 years. Ann Rheum Dis. 2015;74(2):437–43.CrossRefPubMed Tan S, Yao J, Flynn JA, Yao L, Ward MM. Quantitative syndesmophyte measurement in ankylosing spondylitis using CT: longitudinal validity and sensitivity to change over 2 years. Ann Rheum Dis. 2015;74(2):437–43.CrossRefPubMed
35.
go back to reference Karberg K, Zochling J, Sieper J, Felsenberg D, Braun J. Bone loss is detected more frequently in patients with ankylosing spondylitis with syndesmophytes. J Rheumatol. 2005;32(7):1290–8.PubMed Karberg K, Zochling J, Sieper J, Felsenberg D, Braun J. Bone loss is detected more frequently in patients with ankylosing spondylitis with syndesmophytes. J Rheumatol. 2005;32(7):1290–8.PubMed
37.
go back to reference Rajamanohara R, Robinson J, Rymer J, Patel R, Fogelman I, Blake GM. The effect of weight and weight change on the long-term precision of spine and hip DXA measurements. Osteoporos Int. 2011;22(5):1503–12.CrossRefPubMed Rajamanohara R, Robinson J, Rymer J, Patel R, Fogelman I, Blake GM. The effect of weight and weight change on the long-term precision of spine and hip DXA measurements. Osteoporos Int. 2011;22(5):1503–12.CrossRefPubMed
38.
go back to reference Khabbazi A, Noshad H, Gafarzadeh S, Hajialiloo M, Kolahi S. Alendronate effect on the prevention of bone loss in early stages of ankylosing spondylitis: a randomized, double-blind, placebo-controlled pilot study. Iran Red Crescent Med J. 2014;16(6):e18022.CrossRefPubMedPubMedCentral Khabbazi A, Noshad H, Gafarzadeh S, Hajialiloo M, Kolahi S. Alendronate effect on the prevention of bone loss in early stages of ankylosing spondylitis: a randomized, double-blind, placebo-controlled pilot study. Iran Red Crescent Med J. 2014;16(6):e18022.CrossRefPubMedPubMedCentral
39.
go back to reference Haroon NN, Sriganthan J, Al Ghanim N, Inman RD, Cheung AM. Effect of TNF-alpha inhibitor treatment on bone mineral density in patients with ankylosing spondylitis: a systematic review and meta-analysis. Semin Arthritis Rheum. 2014;44(2):155–61.CrossRefPubMed Haroon NN, Sriganthan J, Al Ghanim N, Inman RD, Cheung AM. Effect of TNF-alpha inhibitor treatment on bone mineral density in patients with ankylosing spondylitis: a systematic review and meta-analysis. Semin Arthritis Rheum. 2014;44(2):155–61.CrossRefPubMed
40.
go back to reference Bauer DC, Orwoll ES, Fox KM, Vogt TM, Lane NE, Hochberg MC, Stone K, Nevitt MC. Aspirin and NSAID use in older women: effect on bone mineral density and fracture risk. Study of Osteoporotic Fractures Research Group. J Bone Miner Res. 1996;11(1):29–35.CrossRefPubMed Bauer DC, Orwoll ES, Fox KM, Vogt TM, Lane NE, Hochberg MC, Stone K, Nevitt MC. Aspirin and NSAID use in older women: effect on bone mineral density and fracture risk. Study of Osteoporotic Fractures Research Group. J Bone Miner Res. 1996;11(1):29–35.CrossRefPubMed
41.
go back to reference Morton DJ, Barrett-Connor EL, Schneider DL. Nonsteroidal anti-inflammatory drugs and bone mineral density in older women: the Rancho Bernardo study. J Bone Miner Res. 1998;13(12):1924–31.CrossRefPubMed Morton DJ, Barrett-Connor EL, Schneider DL. Nonsteroidal anti-inflammatory drugs and bone mineral density in older women: the Rancho Bernardo study. J Bone Miner Res. 1998;13(12):1924–31.CrossRefPubMed
42.
go back to reference Vestergaard P, Hermann P, Jensen JE, Eiken P, Mosekilde L. Effects of paracetamol, non-steroidal anti-inflammatory drugs, acetylsalicylic acid, and opioids on bone mineral density and risk of fracture: results of the Danish Osteoporosis Prevention Study (DOPS). Osteoporos Int. 2012;23(4):1255–65.CrossRefPubMed Vestergaard P, Hermann P, Jensen JE, Eiken P, Mosekilde L. Effects of paracetamol, non-steroidal anti-inflammatory drugs, acetylsalicylic acid, and opioids on bone mineral density and risk of fracture: results of the Danish Osteoporosis Prevention Study (DOPS). Osteoporos Int. 2012;23(4):1255–65.CrossRefPubMed
43.
go back to reference Briot K, Etcheto A, Miceli-Richard C, Dougados M, Roux C. Bone loss in patients with early inflammatory back pain suggestive of spondyloarthritis: results from the prospective DESIR cohort. Rheumatology (Oxford). 2016;55(2):335–42.CrossRef Briot K, Etcheto A, Miceli-Richard C, Dougados M, Roux C. Bone loss in patients with early inflammatory back pain suggestive of spondyloarthritis: results from the prospective DESIR cohort. Rheumatology (Oxford). 2016;55(2):335–42.CrossRef
44.
go back to reference Klingberg E, Geijer M, Gothln J, Mellstrom D, Lorentzon M, Hilme E, Hedberg M, Carlsten H, Forsblad-D'elia H. Vertebral fractures in ankylosing spondylitis are associated with lower bone mineral density in both central and peripheral skeleton. J Rheumatol. 2012;39(10):1987–95.CrossRefPubMed Klingberg E, Geijer M, Gothln J, Mellstrom D, Lorentzon M, Hilme E, Hedberg M, Carlsten H, Forsblad-D'elia H. Vertebral fractures in ankylosing spondylitis are associated with lower bone mineral density in both central and peripheral skeleton. J Rheumatol. 2012;39(10):1987–95.CrossRefPubMed
45.
go back to reference Maas F, Spoorenberg A, van der Slik BPG, van der Veer E, Brouwer E, Bootsma H, Bos R, Wink FR, Arends S. Clinical risk factors for the presence and development of vertebral fractures in patients with ankylosing spondylitis. Arthritis Care Res (Hoboken). 2017;69(5):694–702.CrossRef Maas F, Spoorenberg A, van der Slik BPG, van der Veer E, Brouwer E, Bootsma H, Bos R, Wink FR, Arends S. Clinical risk factors for the presence and development of vertebral fractures in patients with ankylosing spondylitis. Arthritis Care Res (Hoboken). 2017;69(5):694–702.CrossRef
46.
go back to reference Geusens P, De Winter L, Quaden D, Vanhoof J, Vosse D, van den Bergh J, Somers V. The prevalence of vertebral fractures in spondyloarthritis: relation to disease characteristics, bone mineral density, syndesmophytes and history of back pain and trauma. Arthritis Res Ther. 2015;17(1):294.CrossRefPubMedPubMedCentral Geusens P, De Winter L, Quaden D, Vanhoof J, Vosse D, van den Bergh J, Somers V. The prevalence of vertebral fractures in spondyloarthritis: relation to disease characteristics, bone mineral density, syndesmophytes and history of back pain and trauma. Arthritis Res Ther. 2015;17(1):294.CrossRefPubMedPubMedCentral
Metadata
Title
Which measuring site in ankylosing spondylitis is best to detect bone loss and what predicts the decline: results from a 5-year prospective study
Authors
Anna Deminger
Eva Klingberg
Mattias Lorentzon
Mats Geijer
Jan Göthlin
Martin Hedberg
Eva Rehnberg
Hans Carlsten
Lennart T. Jacobsson
Helena Forsblad-d’Elia
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2017
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-017-1480-0

Other articles of this Issue 1/2017

Arthritis Research & Therapy 1/2017 Go to the issue