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Published in: Arthritis Research & Therapy 1/2017

Open Access 01-12-2017 | Research article

Serum bone-turnover biomarkers are associated with the occurrence of peripheral and axial arthritis in psoriatic disease: a prospective cross-sectional comparative study

Authors: Deepak R. Jadon, Raj Sengupta, Alison Nightingale, Hui Lu, Juliet Dunphy, Amelia Green, James T. Elder, Rajan P. Nair, Eleanor Korendowych, Mark A. Lindsay, Neil J. McHugh

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

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Abstract

Background

A recent systematic review identified four candidate serum-soluble bone-turnover biomarkers (dickkopf-1, Dkk-1; macrophage-colony stimulating factor, M-CSF; matrix metalloproteinase-3, MMP-3; osteoprotegerin, OPG) showing possible association with psoriatic arthritis (PsA). We aimed to: (i) confirm and determine if these four biomarkers are associated with PsA; (ii) differentiate psoriasis cases with and without arthritis; and (iii) differentiate PsA cases with and without axial arthritis.

Methods

A prospective cross-sectional comparative two-centre study recruited 200 patients with psoriasis without arthritis (PsC), 127 with PsA without axial arthritis (pPsA), 117 with PsA with axial arthritis (psoriatic spondyloarthritis, PsSpA), 157 with ankylosing spondylitis (AS) without psoriasis, and 50 matched healthy controls (HC). Serum biomarker concentrations were measured using ELISA. Multivariable regression and receiver operating characteristic analyses were performed.

Results

MMP-3 concentrations were significantly higher and M-CSF significantly lower in each arthritis disease group compared with HC (p ≤ 0.02). MMP-3 concentrations were significantly higher (adjusted odds ratio, ORadj 1.02 per ng/ml increase in concentration; p = 0.0004) and M-CSF significantly lower (ORadj 0.44 per ng/ml increase; p = 0.01) in PsA (pPsA and PsSpA combined) compared with PsC. Dkk-1 concentrations were significantly higher (ORadj 1.22 per ng/mL increase; p = 0.01), and OPG concentrations significantly lower (ORadj 0.20 per ng/mL increase; p = 0.02) in patients with axial arthritis (PsSpA and AS combined) than in those without (pPsA). Furthermore, Dkk-1 concentrations were significantly higher along a spectrum of increasing axial arthritis; Dkk-1 concentrations were higher in AS compared with PsSpA (ORadj 1.18 per ng/mL increase; p = 0.02). Receiver operating characteristic analysis showed MMP-3 to be the best single biomarker for differentiating PsA from PsC (AUC 0.70 for a cut-off of 14.51 ng/mL; sensitivity 0.76, specificity 0.60).

Conclusions

MMP-3 and M-CSF are biomarkers for the presence of arthritis in psoriatic disease, and could therefore be used to screen for PsA in psoriasis cohorts. Dkk-1 and OPG are biomarkers of axial arthritis; they could therefore be used to screen for the presence of axial disease in PsA cases, and help differentiate PsSpA from AS. High concentrations of Dkk-1 in AS and PsSpA compared with HC, support previous reports that Dkk-1 is dysfunctional in the spondyloarthritides.
Literature
1.
go back to reference Jadon DR, Nightingale AL, McHugh NJ, Lindsay MA, Korendowych E, Sengupta R. Serum soluble bone turnover biomarkers in psoriatic arthritis and psoriatic spondyloarthropathy. J Rheumatol. 2014;42(1):21–30.CrossRefPubMed Jadon DR, Nightingale AL, McHugh NJ, Lindsay MA, Korendowych E, Sengupta R. Serum soluble bone turnover biomarkers in psoriatic arthritis and psoriatic spondyloarthropathy. J Rheumatol. 2014;42(1):21–30.CrossRefPubMed
2.
go back to reference Jadon DR, Sengupta R, Nightingale A, Lindsay M, Korendowych E, Robinson G, et al. Axial Disease in Psoriatic Arthritis study: defining the clinical and radiographic phenotype of psoriatic spondyloarthritis. Ann Rheum Dis. 2016;76(4):701–7.CrossRefPubMedPubMedCentral Jadon DR, Sengupta R, Nightingale A, Lindsay M, Korendowych E, Robinson G, et al. Axial Disease in Psoriatic Arthritis study: defining the clinical and radiographic phenotype of psoriatic spondyloarthritis. Ann Rheum Dis. 2016;76(4):701–7.CrossRefPubMedPubMedCentral
3.
go back to reference Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H, et al. Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum. 2006;54(8):2665–73.CrossRefPubMed Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H, et al. Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum. 2006;54(8):2665–73.CrossRefPubMed
4.
go back to reference Tillett W, Jadon D, Costa L, Wallis D, Cavill C, McHugh J, et al. The Classification for Psoriatic Arthritis (CASPAR) criteria - a retrospective feasibility, sensitivity, and specificity study. J Rheumatol. 2012;39(1):154–6.CrossRefPubMed Tillett W, Jadon D, Costa L, Wallis D, Cavill C, McHugh J, et al. The Classification for Psoriatic Arthritis (CASPAR) criteria - a retrospective feasibility, sensitivity, and specificity study. J Rheumatol. 2012;39(1):154–6.CrossRefPubMed
5.
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
6.
go back to reference Jadon D, Tillett W, Wallis D, Cavill C, Bowes J, Waldron N, et al. Exploring ankylosing spondylitis-associated ERAP1, IL23R and IL12B gene polymorphisms in subphenotypes of psoriatic arthritis. Rheumatology (Oxford). 2013;52(2):261–6.CrossRef Jadon D, Tillett W, Wallis D, Cavill C, Bowes J, Waldron N, et al. Exploring ankylosing spondylitis-associated ERAP1, IL23R and IL12B gene polymorphisms in subphenotypes of psoriatic arthritis. Rheumatology (Oxford). 2013;52(2):261–6.CrossRef
7.
go back to reference Chandran V, Barrett J, Schentag CT, Farewell VT, Gladman DD. Axial psoriatic arthritis: update on a longterm prospective study. J Rheumatol. 2009;36(12):2744–50.CrossRefPubMed Chandran V, Barrett J, Schentag CT, Farewell VT, Gladman DD. Axial psoriatic arthritis: update on a longterm prospective study. J Rheumatol. 2009;36(12):2744–50.CrossRefPubMed
8.
go back to reference Lubrano E, Marchesoni A, Olivieri I, D’Angelo S, Spadaro A, Parsons WJ, et al. Psoriatic arthritis spondylitis radiology index: a modified index for radiologic assessment of axial involvement in psoriatic arthritis. J Rheumatol. 2009;36(5):1006–11.CrossRefPubMed Lubrano E, Marchesoni A, Olivieri I, D’Angelo S, Spadaro A, Parsons WJ, et al. Psoriatic arthritis spondylitis radiology index: a modified index for radiologic assessment of axial involvement in psoriatic arthritis. J Rheumatol. 2009;36(5):1006–11.CrossRefPubMed
9.
go back to reference Creemers MCW. Assessment of outcome in ankylosing spondylitis: an extended radiographic scoring system. Ann Rheum Dis. 2005;64(1):127–9.CrossRefPubMed Creemers MCW. Assessment of outcome in ankylosing spondylitis: an extended radiographic scoring system. Ann Rheum Dis. 2005;64(1):127–9.CrossRefPubMed
10.
go back to reference Clowes JA. Effect of feeding on bone turnover markers and its impact on biological variability of measurements. Bone. 2002;30(6):886–90.CrossRefPubMed Clowes JA. Effect of feeding on bone turnover markers and its impact on biological variability of measurements. Bone. 2002;30(6):886–90.CrossRefPubMed
11.
go back to reference Yang C, Gu J, Rihl M, Baeten D, Huang F, Zhao M, et al. Serum levels of matrix metalloproteinase 3 and macrophage colony-stimulating factor 1 correlate with disease activity in ankylosing spondylitis. Arthritis Rheum. 2004;51(5):691–9.CrossRefPubMed Yang C, Gu J, Rihl M, Baeten D, Huang F, Zhao M, et al. Serum levels of matrix metalloproteinase 3 and macrophage colony-stimulating factor 1 correlate with disease activity in ankylosing spondylitis. Arthritis Rheum. 2004;51(5):691–9.CrossRefPubMed
12.
go back to reference Vandooren B, Kruithof E, Yu DTY, Rihl M, Gu J, De Rycke L, et al. Involvement of matrix metalloproteinases and their inhibitors in peripheral synovitis and down-regulation by tumor necrosis factor-alpha blockade in spondylarthropathy. Arthritis Rheum. 2004;50(9):2942–53.CrossRefPubMed Vandooren B, Kruithof E, Yu DTY, Rihl M, Gu J, De Rycke L, et al. Involvement of matrix metalloproteinases and their inhibitors in peripheral synovitis and down-regulation by tumor necrosis factor-alpha blockade in spondylarthropathy. Arthritis Rheum. 2004;50(9):2942–53.CrossRefPubMed
13.
go back to reference Pedersen SJ, Sorensen IJ, Garnero P, Johansen JS, Madsen OR, Tvede N, et al. ASDAS, BASDAI and different treatment responses and their relation to biomarkers of inflammation, cartilage and bone turnover in patients with axial spondyloarthritis treated with TNFalpha inhibitors. Ann Rheum Dis. 2011;70(8):1375–81.CrossRefPubMed Pedersen SJ, Sorensen IJ, Garnero P, Johansen JS, Madsen OR, Tvede N, et al. ASDAS, BASDAI and different treatment responses and their relation to biomarkers of inflammation, cartilage and bone turnover in patients with axial spondyloarthritis treated with TNFalpha inhibitors. Ann Rheum Dis. 2011;70(8):1375–81.CrossRefPubMed
14.
go back to reference Maksymowych WP, Rahman P, Shojania K, Olszynski WP, Thomson GT, Ballal S, et al. Beneficial effects of adalimumab on biomarkers reflecting structural damage in patients with ankylosing spondylitis. J Rheumatol. 2008;35(10):2030–7.PubMed Maksymowych WP, Rahman P, Shojania K, Olszynski WP, Thomson GT, Ballal S, et al. Beneficial effects of adalimumab on biomarkers reflecting structural damage in patients with ankylosing spondylitis. J Rheumatol. 2008;35(10):2030–7.PubMed
15.
go back to reference Daoussis D, Liossis S-NC, Solomou EE, Tsanaktsi A, Bounia K, Karampetsou M, et al. Evidence that Dkk-1 is dysfunctional in ankylosing spondylitis. Arthritis Rheum. 2010;62(1):150–8.CrossRefPubMed Daoussis D, Liossis S-NC, Solomou EE, Tsanaktsi A, Bounia K, Karampetsou M, et al. Evidence that Dkk-1 is dysfunctional in ankylosing spondylitis. Arthritis Rheum. 2010;62(1):150–8.CrossRefPubMed
16.
go back to reference Klingberg E, Nurkkala M, Carlsten H, Forsblad-d’Elia H. Biomarkers of bone metabolism in ankylosing spondylitis in relation to osteoproliferation and osteoporosis. J Rheumatol. 2014;41(7):1349–56.CrossRefPubMed Klingberg E, Nurkkala M, Carlsten H, Forsblad-d’Elia H. Biomarkers of bone metabolism in ankylosing spondylitis in relation to osteoproliferation and osteoporosis. J Rheumatol. 2014;41(7):1349–56.CrossRefPubMed
17.
go back to reference Wang SY, Liu YY, Ye H, Guo JP, Li R, Liu X, et al. Circulating Dickkopf-1 is correlated with bone erosion and inflammation in rheumatoid arthritis. J Rheumatol. 2011;38(5):821–7.CrossRefPubMed Wang SY, Liu YY, Ye H, Guo JP, Li R, Liu X, et al. Circulating Dickkopf-1 is correlated with bone erosion and inflammation in rheumatoid arthritis. J Rheumatol. 2011;38(5):821–7.CrossRefPubMed
18.
go back to reference Yucong Z, Lu L, Shengfa L, Yongliang Y, Ruguo S, Yikai L. Serum functional dickkopf-1 levels are inversely correlated with radiographic severity of ankylosing spondylitis. Clin Lab. 2014;60(9):1527–31.PubMed Yucong Z, Lu L, Shengfa L, Yongliang Y, Ruguo S, Yikai L. Serum functional dickkopf-1 levels are inversely correlated with radiographic severity of ankylosing spondylitis. Clin Lab. 2014;60(9):1527–31.PubMed
19.
go back to reference Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature. 2008;453(7194):524–8.CrossRefPubMed Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature. 2008;453(7194):524–8.CrossRefPubMed
20.
go back to reference Hampton PJ, Ross OK, Reynolds NJ. Increased nuclear beta-catenin in suprabasal involved psoriatic epidermis. Br J Dermatol. 2007;157(6):1168–77.CrossRefPubMed Hampton PJ, Ross OK, Reynolds NJ. Increased nuclear beta-catenin in suprabasal involved psoriatic epidermis. Br J Dermatol. 2007;157(6):1168–77.CrossRefPubMed
21.
go back to reference Teh MT, Blaydon D, Ghali LR, Briggs V, Edmunds S, Pantazi E, et al. Role for WNT16B in human epidermal keratinocyte proliferation and differentiation. J Cell Sci. 2007;120(Pt 2):330–9.CrossRefPubMed Teh MT, Blaydon D, Ghali LR, Briggs V, Edmunds S, Pantazi E, et al. Role for WNT16B in human epidermal keratinocyte proliferation and differentiation. J Cell Sci. 2007;120(Pt 2):330–9.CrossRefPubMed
22.
go back to reference Yamaguchi Y, Passeron T, Watabe H, Yasumoto K, Rouzaud F, Hoashi T, et al. The effects of dickkopf 1 on gene expression and Wnt signaling by melanocytes: mechanisms underlying its suppression of melanocyte function and proliferation. J Invest Dermatol. 2007;127(5):1217–25.CrossRefPubMed Yamaguchi Y, Passeron T, Watabe H, Yasumoto K, Rouzaud F, Hoashi T, et al. The effects of dickkopf 1 on gene expression and Wnt signaling by melanocytes: mechanisms underlying its suppression of melanocyte function and proliferation. J Invest Dermatol. 2007;127(5):1217–25.CrossRefPubMed
23.
go back to reference Reischl J, Schwenke S, Beekman JM, Mrowietz U, Sturzebecher S, Heubach JF. Increased expression of Wnt5a in psoriatic plaques. J Invest Dermatol. 2007;127(1):163–9.CrossRefPubMed Reischl J, Schwenke S, Beekman JM, Mrowietz U, Sturzebecher S, Heubach JF. Increased expression of Wnt5a in psoriatic plaques. J Invest Dermatol. 2007;127(1):163–9.CrossRefPubMed
24.
go back to reference Gudjonsson JE, Johnston A, Stoll SW, Riblett MB, Xing X, Kochkodan JJ, et al. Evidence for altered Wnt signaling in psoriatic skin. J Invest Dermatol. 2010;130(7):1849–59.CrossRefPubMedPubMedCentral Gudjonsson JE, Johnston A, Stoll SW, Riblett MB, Xing X, Kochkodan JJ, et al. Evidence for altered Wnt signaling in psoriatic skin. J Invest Dermatol. 2010;130(7):1849–59.CrossRefPubMedPubMedCentral
25.
go back to reference Seifert O, Soderman J, Skarstedt M, Dienus O, Matussek A. Increased expression of the Wnt signalling inhibitor Dkk-1 in non-lesional skin and peripheral blood mononuclear cells of patients with plaque psoriasis. Acta Derm Venereol. 2015;95(4):407–10.CrossRefPubMed Seifert O, Soderman J, Skarstedt M, Dienus O, Matussek A. Increased expression of the Wnt signalling inhibitor Dkk-1 in non-lesional skin and peripheral blood mononuclear cells of patients with plaque psoriasis. Acta Derm Venereol. 2015;95(4):407–10.CrossRefPubMed
26.
go back to reference Franck H, Meurer T, Hofbauer LC. Evaluation of bone mineral density, hormones, biochemical markers of bone metabolism, and osteoprotegerin serum levels in patients with ankylosing spondylitis. J Rheumatol. 2004;31(11):2236–41.PubMed Franck H, Meurer T, Hofbauer LC. Evaluation of bone mineral density, hormones, biochemical markers of bone metabolism, and osteoprotegerin serum levels in patients with ankylosing spondylitis. J Rheumatol. 2004;31(11):2236–41.PubMed
27.
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
28.
go back to reference Klingberg E, Geijer M, Gothlin J, Mellstrom D, Lorentzon M, Hilme E, et al. 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, Gothlin J, Mellstrom D, Lorentzon M, Hilme E, et al. 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
29.
go back to reference Reddy SM, Anandarajah AP, Fisher MC, Mease PJ, Greenberg JD, Kremer JM, et al. Comparative analysis of disease activity measures, use of biologic agents, body mass index, radiographic features, and bone density in psoriatic arthritis and rheumatoid arthritis patients followed in a large U.S. disease registry. J Rheumatol. 2010;37(12):2566–72.CrossRefPubMed Reddy SM, Anandarajah AP, Fisher MC, Mease PJ, Greenberg JD, Kremer JM, et al. Comparative analysis of disease activity measures, use of biologic agents, body mass index, radiographic features, and bone density in psoriatic arthritis and rheumatoid arthritis patients followed in a large U.S. disease registry. J Rheumatol. 2010;37(12):2566–72.CrossRefPubMed
30.
go back to reference Kim HR, Lee SH, Kim HY. Elevated serum levels of soluble receptor activator of nuclear factors-kappaB ligand (sRANKL) and reduced bone mineral density in patients with ankylosing spondylitis (AS). Rheumatology (Oxford). 2006;45(10):1197–200.CrossRef Kim HR, Lee SH, Kim HY. Elevated serum levels of soluble receptor activator of nuclear factors-kappaB ligand (sRANKL) and reduced bone mineral density in patients with ankylosing spondylitis (AS). Rheumatology (Oxford). 2006;45(10):1197–200.CrossRef
31.
go back to reference Chen CH, Chen HA, Liao HT, Liu CH, Tsai CY, Chou CT. Soluble receptor activator of nuclear factor-kappaB ligand (RANKL) and osteoprotegerin in ankylosing spondylitis: OPG is associated with poor physical mobility and reflects systemic inflammation. Clin Rheumatol. 2010;29(10):1155–61.CrossRefPubMed Chen CH, Chen HA, Liao HT, Liu CH, Tsai CY, Chou CT. Soluble receptor activator of nuclear factor-kappaB ligand (RANKL) and osteoprotegerin in ankylosing spondylitis: OPG is associated with poor physical mobility and reflects systemic inflammation. Clin Rheumatol. 2010;29(10):1155–61.CrossRefPubMed
32.
go back to reference Taylan A, Sari I, Akinci B, Bilge S, Kozaci D, Akar S, et al. Biomarkers and cytokines of bone turnover: extensive evaluation in a cohort of patients with ankylosing spondylitis. BMC Musculoskelet Disord. 2012;13:191.CrossRefPubMedPubMedCentral Taylan A, Sari I, Akinci B, Bilge S, Kozaci D, Akar S, et al. Biomarkers and cytokines of bone turnover: extensive evaluation in a cohort of patients with ankylosing spondylitis. BMC Musculoskelet Disord. 2012;13:191.CrossRefPubMedPubMedCentral
33.
go back to reference Geusens PP, Landewe RB, Garnero P, Chen D, Dunstan CR, Lems WF, et al. The ratio of circulating osteoprotegerin to RANKL in early rheumatoid arthritis predicts later joint destruction. Arthritis Rheum. 2006;54(6):1772–7.CrossRefPubMed Geusens PP, Landewe RB, Garnero P, Chen D, Dunstan CR, Lems WF, et al. The ratio of circulating osteoprotegerin to RANKL in early rheumatoid arthritis predicts later joint destruction. Arthritis Rheum. 2006;54(6):1772–7.CrossRefPubMed
34.
go back to reference Chandran V, Shen H, Pollock RA, Pellett FJ, Carty A, Cook RJ, et al. Soluble biomarkers associated with response to treatment with tumor necrosis factor inhibitors in psoriatic arthritis. J Rheumatol. 2013;40(6):866–71.CrossRefPubMed Chandran V, Shen H, Pollock RA, Pellett FJ, Carty A, Cook RJ, et al. Soluble biomarkers associated with response to treatment with tumor necrosis factor inhibitors in psoriatic arthritis. J Rheumatol. 2013;40(6):866–71.CrossRefPubMed
35.
go back to reference Wagner CL, Visvanathan S, Elashoff M, McInnes IB, Mease PJ, Krueger GG, et al. Markers of inflammation and bone remodelling associated with improvement in clinical response measures in psoriatic arthritis patients treated with golimumab. Ann Rheum Dis. 2013;72(1):83–8.CrossRefPubMed Wagner CL, Visvanathan S, Elashoff M, McInnes IB, Mease PJ, Krueger GG, et al. Markers of inflammation and bone remodelling associated with improvement in clinical response measures in psoriatic arthritis patients treated with golimumab. Ann Rheum Dis. 2013;72(1):83–8.CrossRefPubMed
36.
go back to reference de Andrade KR, de Castro GR, Vicente G, da Rosa JS, Nader M, Pereira IA, et al. Evaluation of circulating levels of inflammatory and bone formation markers in axial spondyloarthritis. Int Immunopharmacol. 2014;21(2):481–6.CrossRefPubMed de Andrade KR, de Castro GR, Vicente G, da Rosa JS, Nader M, Pereira IA, et al. Evaluation of circulating levels of inflammatory and bone formation markers in axial spondyloarthritis. Int Immunopharmacol. 2014;21(2):481–6.CrossRefPubMed
37.
go back to reference Woo JH, Lee HJ, Sung IH, Kim TH. Changes of clinical response and bone biochemical markers in patients with ankylosing spondylitis taking etanercept. J Rheumatol. 2007;34(8):1753–9.PubMed Woo JH, Lee HJ, Sung IH, Kim TH. Changes of clinical response and bone biochemical markers in patients with ankylosing spondylitis taking etanercept. J Rheumatol. 2007;34(8):1753–9.PubMed
38.
go back to reference Pedersen SJ, Hetland ML, Sorensen IJ, Ostergaard M, Nielsen HJ, Johansen JS. Circulating levels of interleukin-6, vascular endothelial growth factor, YKL-40, matrix metalloproteinase-3, and total aggrecan in spondyloarthritis patients during 3 years of treatment with TNF alpha inhibitors. Clin Rheumatol. 2010;29(11):1301–9.CrossRefPubMed Pedersen SJ, Hetland ML, Sorensen IJ, Ostergaard M, Nielsen HJ, Johansen JS. Circulating levels of interleukin-6, vascular endothelial growth factor, YKL-40, matrix metalloproteinase-3, and total aggrecan in spondyloarthritis patients during 3 years of treatment with TNF alpha inhibitors. Clin Rheumatol. 2010;29(11):1301–9.CrossRefPubMed
39.
go back to reference Kwon SR, Lim MJ, Suh CH, Park SG, Hong YS, Yoon BY, et al. Dickkopf-1 level is lower in patients with ankylosing spondylitis than in healthy people and is not influenced by anti-tumor necrosis factor therapy. Rheumatol Int. 2012;32(8):2523–7.CrossRefPubMed Kwon SR, Lim MJ, Suh CH, Park SG, Hong YS, Yoon BY, et al. Dickkopf-1 level is lower in patients with ankylosing spondylitis than in healthy people and is not influenced by anti-tumor necrosis factor therapy. Rheumatol Int. 2012;32(8):2523–7.CrossRefPubMed
40.
go back to reference Appel H, Janssen L, Listing J, Heydrich R, Rudwaleit M, Sieper J. Serum levels of biomarkers of bone and cartilage destruction and new bone formation in different cohorts of patients with axial spondyloarthritis with and without tumor necrosis factor-alpha blocker treatment. Arthritis Res Ther. 2008;10(5):R125.CrossRefPubMedPubMedCentral Appel H, Janssen L, Listing J, Heydrich R, Rudwaleit M, Sieper J. Serum levels of biomarkers of bone and cartilage destruction and new bone formation in different cohorts of patients with axial spondyloarthritis with and without tumor necrosis factor-alpha blocker treatment. Arthritis Res Ther. 2008;10(5):R125.CrossRefPubMedPubMedCentral
41.
go back to reference Arends S, van der Veer E, Groen H, Houtman PM, Jansen TL, Leijsma MK, et al. Serum MMP-3 level as a biomarker for monitoring and predicting response to etanercept treatment in ankylosing spondylitis. J Rheumatol. 2011;38(8):1644–50.CrossRefPubMed Arends S, van der Veer E, Groen H, Houtman PM, Jansen TL, Leijsma MK, et al. Serum MMP-3 level as a biomarker for monitoring and predicting response to etanercept treatment in ankylosing spondylitis. J Rheumatol. 2011;38(8):1644–50.CrossRefPubMed
42.
go back to reference Chen CH, Lin KC, Yu DT, Yang C, Huang F, Chen HA, et al. Serum matrix metalloproteinases and tissue inhibitors of metalloproteinases in ankylosing spondylitis: MMP-3 is a reproducibly sensitive and specific biomarker of disease activity. Rheumatology (Oxford). 2006;45(4):414–20.CrossRef Chen CH, Lin KC, Yu DT, Yang C, Huang F, Chen HA, et al. Serum matrix metalloproteinases and tissue inhibitors of metalloproteinases in ankylosing spondylitis: MMP-3 is a reproducibly sensitive and specific biomarker of disease activity. Rheumatology (Oxford). 2006;45(4):414–20.CrossRef
43.
go back to reference Sun S, Bay-Jensen AC, Karsdal MA, Siebuhr AS, Zheng Q, Maksymowych WP, et al. The active form of MMP-3 is a marker of synovial inflammation and cartilage turnover in inflammatory joint diseases. BMC Musculoskelet Disord. 2014;15:93.CrossRefPubMedPubMedCentral Sun S, Bay-Jensen AC, Karsdal MA, Siebuhr AS, Zheng Q, Maksymowych WP, et al. The active form of MMP-3 is a marker of synovial inflammation and cartilage turnover in inflammatory joint diseases. BMC Musculoskelet Disord. 2014;15:93.CrossRefPubMedPubMedCentral
44.
go back to reference Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci. 2002;115(Pt 19):3719–27.CrossRefPubMed Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci. 2002;115(Pt 19):3719–27.CrossRefPubMed
45.
go back to reference Sottrup-Jensen L. Alpha-macroglobulins: structure, shape, and mechanism of proteinase complex formation. J Biol Chem. 1989;264(20):11539–42.PubMed Sottrup-Jensen L. Alpha-macroglobulins: structure, shape, and mechanism of proteinase complex formation. J Biol Chem. 1989;264(20):11539–42.PubMed
46.
go back to reference Heiland GR, Appel H, Poddubnyy D, Zwerina J, Hueber A, Haibel H, et al. High level of functional dickkopf-1 predicts protection from syndesmophyte formation in patients with ankylosing spondylitis. Ann Rheum Dis. 2012;71(4):572–4.CrossRefPubMed Heiland GR, Appel H, Poddubnyy D, Zwerina J, Hueber A, Haibel H, et al. High level of functional dickkopf-1 predicts protection from syndesmophyte formation in patients with ankylosing spondylitis. Ann Rheum Dis. 2012;71(4):572–4.CrossRefPubMed
47.
go back to reference Ribbens C, Martin y Porras M, Franchimont N, Kaiser MJ, Jaspar JM, Damas P, et al. Increased matrix metalloproteinase-3 serum levels in rheumatic diseases: relationship with synovitis and steroid treatment. Ann Rheum Dis. 2001;61(2):161–6.CrossRef Ribbens C, Martin y Porras M, Franchimont N, Kaiser MJ, Jaspar JM, Damas P, et al. Increased matrix metalloproteinase-3 serum levels in rheumatic diseases: relationship with synovitis and steroid treatment. Ann Rheum Dis. 2001;61(2):161–6.CrossRef
48.
go back to reference Schlemmer A, Hassager C. Acute fasting diminishes the circadian rhythm of biochemical markers of bone resorption. European journal of endocrinology/European Federation of Endocrine Societies. 1999;140(4):332–7.CrossRef Schlemmer A, Hassager C. Acute fasting diminishes the circadian rhythm of biochemical markers of bone resorption. European journal of endocrinology/European Federation of Endocrine Societies. 1999;140(4):332–7.CrossRef
Metadata
Title
Serum bone-turnover biomarkers are associated with the occurrence of peripheral and axial arthritis in psoriatic disease: a prospective cross-sectional comparative study
Authors
Deepak R. Jadon
Raj Sengupta
Alison Nightingale
Hui Lu
Juliet Dunphy
Amelia Green
James T. Elder
Rajan P. Nair
Eleanor Korendowych
Mark A. Lindsay
Neil J. McHugh
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/s13075-017-1417-7

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