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Review

Lessons to be learned from serum biomarkers in psoriasis and IBD – the potential role in SpA

, &
Pages 333-344 | Received 25 Sep 2015, Accepted 29 Sep 2016, Published online: 21 Oct 2016

References

  • Dougados M, Baeten D. Spondyloarthritis. Lancet. 2011;377:2127–2137.
  • Sieper J, Rudwaleit M, Baraliakos X, et al. The Assessment of SpondyloArthritis international Society (ASAS) handbook: a guide to assess spondyloarthritis. Ann Rheum Dis. 2009;68(Suppl 2):ii1–44.
  • Van den Bosch F, Kruithof E, Baeten D, et al. Randomized double-blind comparison of chimeric monoclonal antibody to tumor necrosis factor alpha (infliximab) versus placebo in active spondylarthropathy. Arthritis Rheum. 2002;46:755–765.
  • Braun J, Brandt J, Listing J, et al. Treatment of active ankylosing spondylitis with infliximab: a randomised controlled multicentre trial. Lancet. 2002;359:1187–1193.
  • Mease PJ, Goffe BS, Metz J, et al. Etanercept in the treatment of psoriatic arthritis and psoriasis: a randomised trial. Lancet. 2000;356:385–390.
  • Paramarta JE, De Rycke L, Heijda TF, et al. Efficacy and safety of adalimumab for the treatment of peripheral arthritis in spondyloarthritis patients without ankylosing spondylitis or psoriatic arthritis. Ann Rheum Dis. 2013;72:1793–1799.
  • Sieper J, Van der Heijde D, Dougados M, et al. Efficacy and safety of adalimumab in patients with non-radiographic axial spondyloarthritis: results of a randomised placebo-controlled trial (ABILITY-1). Ann Rheum Dis. 2013;72:815–822.
  • Landewé R, Braun J, Deodhar A, et al. Efficacy of certolizumab pegol on signs and symptoms of axial spondyloarthritis including ankylosing spondylitis: 24-week results of a double-blind randomised placebo-controlled Phase 3 study. Ann Rheum Dis. 2014;73:39–47.
  • Feldtkeller E, Khan MA, Van der Heijde D, et al. Age at disease onset and diagnosis delay in HLA-B27 negative vs. positive patients with ankylosing spondylitis. Rheumatol Int. 2003;23:61–66.
  • Salvadorini G, Bandinelli F, Delle Sedie A, et al. Ankylosing spondylitis: how diagnostic and therapeutic delay have changed over the last six decades. Clin Exp Rheumatol. 2012;30:561–565.
  • Sorensen J, Hetland ML. Decreases in diagnostic delay are supported by sensitivity analyses. Ann Rheum Dis. 2014;73:e45–e45.
  • De Gruttola VG, Clax P, Demets DL, et al. Considerations in the evaluation of surrogate endpoints in clinical trials: summary of a national institutes of health workshop. Control Clin Trials. 2001;1998:485–502.
  • Rudwaleit M, Van der Heijde D, Landewé R, et al. The Assessment of SpondyloArthritis International Society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann Rheum Dis. 2011;70:25–31.
  • Benhamou M, Gossec L, Dougados M. Clinical relevance of C-reactive protein in ankylosing spondylitis and evaluation of the NSAIDs/coxibs’ treatment effect on C-reactive protein. Rheumatology (Oxford). 2010;49:536–541.
  • Poddubnyy DA, Rudwaleit M, Listing J, et al. Comparison of a high sensitivity and standard C reactive protein measurement in patients with ankylosing spondylitis and non-radiographic axial spondyloarthritis. Ann Rheum Dis. 2010;69:1338–1341.
  • Visvanathan S, Wagner C, Marini JC, et al. Inflammatory biomarkers, disease activity and spinal disease measures in patients with ankylosing spondylitis after treatment with infliximab. Ann Rheum Dis. 2008;67:511–517.
  • De Vries MK, Van Eijk IC, Van der Horst-Bruinsma IE, et al. Erythrocyte sedimentation rate, C-reactive protein level, and serum amyloid a protein for patient selection and monitoring of anti-tumor necrosis factor treatment in ankylosing spondylitis. Arthritis Rheum. 2009;61:1484–1490.
  • Poddubnyy D, Rudwaleit M, Haibel H, et al. Rates and predictors of radiographic sacroiliitis progression over 2 years in patients with axial spondyloarthritis. Ann Rheum Dis. 2011;70:1369–1374.
  • Gratacós J, Collado A, Filella F, et al. Serum cytokines (IL-6, TNF-alpha, IL-1 beta and IFN-gamma) in ankylosing spondylitis: a close correlation between serum IL-6 and disease activity and severity. Br J Rheumatol. 1994;33:927–931.
  • Pedersen SJ, Hetland ML, Sørensen IJ, et al. 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 TNFα inhibitors. Clin Rheumatol. 2010;29:1301–1309.
  • Kane D, Roth J, Frosch M, et al. Increased perivascular synovial membrane expression of myeloid-related proteins in psoriatic arthritis. Arthritis Rheum. 2003;48:1676–1685.
  • Kruithof E, De Rycke L, Vandooren B, et al. Identification of synovial biomarkers of response to experimental treatment in early-phase clinical trials in spondylarthritis. Arthritis Rheum. 2006;54:1795–1804.
  • De Rycke L, Baeten D, Foell D, et al. Differential expression and response to anti-TNFalpha treatment of infiltrating versus resident tissue macrophage subsets in autoimmune arthritis. J Pathol. 2005;206:17–27.
  • Turina MC, Sieper J, Yeremenko N, et al. Calprotectin serum level is an independent marker for radiographic spinal progression in axial spondyloarthritis. Ann Rheum Dis. 2014;73:1746–1748.
  • Baeten DL, Demetter P, Cuvelier C, et al. Comparative study of the synovial histology in rheumatoid arthritis, spondyloarthropathy, and osteoarthritis: influence of disease duration and activity. Ann Rheum Dis. 2000;59:945–953.
  • Baeten D, Kruithof E, De Rycke L, et al. Diagnostic classification of spondylarthropathy and rheumatoid arthritis by synovial histopathology: a prospective study in 154 consecutive patients. Arthritis Rheum. 2004;50:2931–2941.
  • Drouart M, Saas P, Billot M, et al. High serum vascular endothelial growth factor correlates with disease activity of spondylarthropathies. Clin Exp Immunol. 2003;132:158–162.
  • Poddubnyy D, Conrad K, Haibel H, et al. Elevated serum level of the vascular endothelial growth factor predicts radiographic spinal progression in patients with axial spondyloarthritis. Ann Rheum Dis. 2014;73:2137–2143.
  • Braun J, Baraliakos X, Hermann KG, et al. Serum vascular endothelial growth factor levels lack predictive value in patients with active ankylosing spondylitis treated with golimumab. J Rheumatol. 2016;43:901–906.
  • Vandooren B, Kruithof E, Yu DTY, 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;50:2942–2953.
  • Chen C-H, Lin K-C, Yu DTY, 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;45:414–420.
  • Yang C, Gu J, Rihl 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;51:691–699.
  • Pedersen SJ, Sørensen IJ, Lambert RGW, et al. Radiographic progression is associated with resolution of systemic inflammation in patients with axial spondylarthritis treated with tumor necrosis factor α inhibitors: a study of radiographic progression, inflammation on magnetic resonance imaging, and c. Arthritis Rheum. 2011;63:3789–3800.
  • Maksymowych WP, Landewé R, Conner-Spady B, et al. Serum matrix metalloproteinase 3 is an independent predictor of structural damage progression in patients with ankylosing spondylitis. Arthritis Rheum. 2007;56:1846–1853.
  • Diarra D, Stolina M, Polzer K, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med. 2007;13:156–163.
  • Klingberg E, Nurkkala M, Carlsten H, et al. Biomarkers of bone metabolism in ankylosing spondylitis in relation to osteoproliferation and osteoporosis. J Rheumatol. 2014;41:1349–1356.
  • Kwon S-R, Lim M-J, Suh C-H, 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;32:2523–2527.
  • Heiland GR, Appel H, Poddubnyy D, et al. High level of functional dickkopf-1 predicts protection from syndesmophyte formation in patients with ankylosing spondylitis. Ann Rheum Dis. 2012;71:572–574.
  • Appel H, Ruiz-Heiland G, Listing J, et al. Altered skeletal expression of sclerostin and its link to radiographic progression in ankylosing spondylitis. Arthritis Rheum. 2009;60:3257–3262.
  • Taylan A, Sari I, Akinci B, et al. Biomarkers and cytokines of bone turnover: extensive evaluation in a cohort of patients with ankylosing spondylitis. BMC Musculoskelet Disord. 2012;13:191.
  • De Andrade KR, De Castro GRW, Vicente G, et al. Evaluation of circulating levels of inflammatory and bone formation markers in axial spondyloarthritis. Int Immunopharmacol. 2014;21:481–486.
  • Korkosz M, Gąsowski J, Leszczyński P, et al. High disease activity in ankylosing spondylitis is associated with increased serum sclerostin level and decreased wingless protein-3a signaling but is not linked with greater structural damage. BMC Musculoskelet Disord. 2013 Mar 19;14:99. doi:10.1186/1471-2474-14-99.
  • Chou C-L, Wu M-J, Yu C-L, et al. Anti-agalactosyl IgG antibody in ankylosing spondylitis and psoriatic arthritis. Clin Rheumatol. 2010;29:875–881.
  • Wright C, Sibani S, Trudgian D, et al. Detection of multiple autoantibodies in patients with ankylosing spondylitis using nucleic acid programmable protein arrays. Mol Cell Proteomics. 2012 Feb;11(2):M9.00384. doi:10.1074/mcp.M9.00384.
  • Duftner C, Dejaco C, Klauser A, et al. High positive predictive value of specific antibodies cross-reacting with a 28-kDa Drosophila antigen for diagnosis of ankylosing spondylitis. Rheumatology (Oxford). 2006;45:38–42.
  • Baerlecken NT, Nothdorft S, Stummvoll GH, et al. Autoantibodies against CD74 in spondyloarthritis. Ann Rheum Dis. 2014;73:1211–1214.
  • Baraliakos X, Baerlecken N, Witte T, et al. High prevalence of anti-CD74 antibodies specific for the HLA class II-associated invariant chain peptide (CLIP) in patients with axial spondyloarthritis. Ann Rheum Dis. 2014;73:1079–1082.
  • Baeten D, Breban M, Lories R, et al. Are spondylarthritides related but distinct conditions or a single disease with a heterogeneous phenotype? Arthritis Rheum. 2013;65:12–20.
  • Fredriksson T, Pettersson U. Severe psoriasis–oral therapy with a new retinoid. Dermatologica. 1978;157:238–244.
  • Beygi S, Lajevardi V, Abedini R. C-reactive protein in psoriasis: a review of the literature. J Eur Acad Dermatol Venereol. 2014;28:700–711.
  • Coimbra S, Oliveira H, Reis F, et al. C-reactive protein and leucocyte activation in psoriasis vulgaris according to severity and therapy. J Eur Acad Dermatology Venereol. 2010;24:789–796.
  • Nisa N, Qazi A. High-sensitivity C-reactive protein in psoriasis. Int J Dermatol. 2012;51:1393–1394.
  • Gisondi P, Malerbai M, Malara G, et al. C-reactive protein and markers for thrombophilia in patients with chronic plaque psoriasis. Int J Immunopathol Pharmacol. 2010;23:1195–1202.
  • Rocha-Pereira P, Santos-Silva A, Rebelo I, et al. The inflammatory response in mild and in severe psoriasis. Br J Dermatol. 2004;150:917–928.
  • Coimbra S, Oliveira H, Reis F, et al. Interleukin (IL)-22, IL-17, IL-23, IL-8, vascular endothelial growth factor and tumour necrosis factor-α levels in patients with psoriasis before, during and after psoralen-ultraviolet A and narrowband ultraviolet B therapy. Br J Dermatol. 2010;163:1282–1290.
  • Arican O, Aral M, Sasmaz S, et al. Serum levels of TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm. 2005;2005:273–279.
  • Bonifati C, Trento E, Carducci M, et al. Soluble E-selectin and soluble tumour necrosis factor receptor (60 kD) serum levels in patients with psoriasis. Dermatology. 1995;190:128–131.
  • Ataseven A, Kesli R, Kurtipek GS, et al. Assessment of lipocalin 2, clusterin, soluble tumor necrosis factor receptor-1, interleukin-6, homocysteine, and uric acid levels in patients with psoriasis. Dis Markers. 2014;2014:541709.
  • Serwin AB, Sokolowska M, Chodynicka B. Tumour necrosis factor a (TNF- alpha)-converting enzyme (TACE) and soluble TNF- a receptor type 1 in psoriasis patients treated with narrowband ultraviolet B. Photodermatol Photoimmunol Photomed. 2007;23:130–134.
  • Borská L, Fiala Z, Krejsek J, et al. Selected immunological changes in patients with sICAM-1 and IL-8. Physiol Res. 2006;55:699–706.
  • Elghandour TM, Youssef SES, Aly DG, et al. Effect of narrow band ultraviolet b therapy versus methotrexate on serum levels of interleukin-17 and interleukin-23 in Egyptian patients with severe psoriasis. Dermatol Res Pract. 2013;2013:618269.
  • Caproni M, Antiga E, Melani L, et al. Serum levels of IL-17 and IL-22 are reduced by etanercept, but not by acitretin, in patients with psoriasis: a randomized-controlled trial. J Clin Immunol. 2009;29:210–214.
  • Flisiak I, Klepacki A, Chodynicka B. Plasma and scales levels of interleukin 18 in comparison with other possible clinical and laboratory biomarkers of psoriasis activity. Biomarkers. 2006;11:194–200.
  • Gangemi S, Merendino RA, Guarneri F, et al. Serum levels of interleukin-18 and s-ICAM-1 in patients affected by psoriasis : preliminary considerations. Eur Acad Dermatol Venereol. 2003;17:42–46.
  • Shimauchi T, Hirakawa S, Suzuki T, et al. Serum interleukin-22 and vascular endothelial growth factor serve as sensitive biomarkers but not as predictors of therapeutic response to biologics in patients with psoriasis. J Dermatol. 2013;40:805–812.
  • Czech W, Schopf E, Kapp A. Soluble E-selectin in sera of patients with atopic dermatitis and psoriasis-correlation with disease activity. Br J Dermatol. 1996;134:17–21.
  • Szepietowski J, Wa F, Bielicka E, et al. Soluble E-selectin serum levels correlate with disease activity in psoriatic patients. Exp Dermatol. 1999;24:33–36.
  • Krasowska D, Chodorowska G, Kozioł M, et al. Plasma levels of sICAM-1 in patients affected by psoriasis: no relation to disease severity. Med Sci Monit. 2000;6:353–355.
  • Madej A, Reich A, Orda A, et al. Vascular adhesion protein-1 (VAP-1) is overexpressed in psoriatic patients. J Eur Acad Dermatol Venereol. 2007;21:72–78.
  • Ataseven A, Kesli R. Novel inflammatory markers in psoriasis vulgaris: vaspin, vascular adhesion protein-1 (VAP-1), and YKL-40. G Ital Dermatol Venereol. 2016;151:244–250.
  • Nemati H, Khodarahmi R, Rahmani A, et al. Serum lipid profile in psoriatic patients: correlation between vascular adhesion protein 1 and lipoprotein (a). Cell Biochem Funct. 2013;31(February 2012):36–40.
  • Schonthaler HB, Guinea-Viniegra J, Wculek SK, et al. S100A8-S100A9 protein complex mediates psoriasis by regulating the expression of complement factor C3. Immunity. 2013;39:1171–1181.
  • Benoit S, Toksoy A, Ahlmann M, et al. Elevated serum levels of calcium-binding S 100 proteins A 8 and A 9 reflect disease activity and abnormal differentiation of keratinocytes in psoriasis. Clin Lab Investig. 2006;7:62–66.
  • El-Hadidi H, Samir N, Shaker OG, et al. Estimation of tissue and serum lipocalin-2 in psoriasis vulgaris and its relation to metabolic syndrome. Arch Dermatol Res. 2014;306:239–245.
  • Kamata M, Tada Y, Tatsuta A, et al. Serum lipocalin-2 levels are increased in patients with psoriasis. Clin Exp Dermatol. 2012;37:296–299.
  • Romaní J, Caixàs A, Ceperuelo-Mallafré V, et al. Circulating levels of lipocalin-2 and retinol-binding protein-4 are increased in psoriatic patients and correlated with baseline PASI. Arch Dermatol Res. 2013;305:105–112.
  • Jansen PAM, Rodijk-Olthuis D, Hollox EJ, et al. Beta-defensin-2 protein is a serum biomarker for disease activity in psoriasis and reaches biologically relevant concentrations in lesional skin. PLoS One. 2009;4:e4725.
  • Gambichler T, Bechara FG, Scola N, et al. Serum levels of antimicrobial peptides and proteins do not correlate with psoriasis severity and are increased after treatment with fumaric acid esters. Arch Dermatol Res. 2012;304:471–474.
  • Johnston A, Arnadottir S, Gudjonsson JE, et al. Obesity in psoriasis: leptin and resistin as mediators of cutaneous inflammation. Br J Dermatol. 2008;159:342–350.
  • Ozdemir M, Yüksel M, Gökbel H, et al. Serum leptin, adiponectin, resistin and ghrelin levels in psoriatic patients treated with cyclosporin. J Dermatol. 2012;39:443–448.
  • Kawashima K, Torii K, Furuhashi T, et al. Phototherapy reduces serum resistin levels in psoriasis patients. Photodermatol Photoimmunol Photomed. 2011;27:152–155.
  • Baran A, Flisiak I, Jaroszewicz J, et al. Serum adiponectin and leptin levels in psoriatic patients according to topical treatment. J Dermatolog Treat. 2014;6634:1–5.
  • Karadag AS, Ertugrul DT, Kalkan G, et al. The effect of acitretin treatment on insulin resistance, retinol-binding protein-4, leptin, and adiponectin in psoriasis vulgaris: a noncontrolled study. Dermatology. 2013;227:103–108.
  • Oh YJ, Lim HK, Choi JH, et al. Serum leptin and adiponectin levels in Korean patients with psoriasis. J Korean Med Sci. 2014;29:729–734.
  • Zhu K-J, Zhang C, Li M, et al. Leptin levels in patients with psoriasis: a meta-analysis. Clin Exp Dermatol. 2013;38:478–483.
  • Shibata S, Saeki H, Tada Y, et al. Serum high molecular weight adiponectin levels are decreased in psoriasis patients. J Dermatol Sci. 2009;55:62–63.
  • Shibata S, Tada Y, Hau C, et al. Adiponectin as an anti-inflammatory factor in the pathogenesis of psoriasis: induction of elevated serum adiponectin levels following therapy. Br J Dermatol. 2011;164:667–670.
  • Ucak H, Demir B, Cicek D, et al. Metabolic changes and serum ghrelin level in patients with psoriasis. Dermatol Res Pract. 2014;2014:1–6.
  • Bhushan M, McLaughlin B, Weiss JB, et al. Levels of endothelial cell stimulating angiogenesis factor and vascular endothelial growth factor are elevated in psoriasis. Br J Dermatol. 1999;141:1054–1060.
  • Meki A-RMA, Al-Shobaili H. Serum vascular endothelial growth factor, transforming growth factor β1, and nitric oxide levels in patients with psoriasis vulgaris: their correlation to disease severity. J Clin Lab Anal. 2014;28:496–501.
  • Flisiak I, Zaniewski P, Rogalska-Taranta M, et al. Effect of psoriasis therapy on VEGF and its soluble receptors serum concentrations. J Eur Acad Dermatol Venereol. 2012;26:302–307.
  • Tekin NS, Ilter N, Sancak B, et al. Nitric oxide levels in patients with psoriasis treated with methotrexate. Mediators Inflamm. 2006;2006:1–5.
  • Gokhale N, Belgaumkar V, Pandit D, et al. A study of serum nitric oxide levels in psoriasis. Indian J Dermatol Venereol Leprol. 2005;71:175.
  • Zalewska A, Wyczółkowska J, Narbutt J, et al. Nitric oxide levels in plasma and fibroblast cultures of psoriasis vulgaris patients. J Dermatol Sci. 2007;48:237–240.
  • Strober B, Teller C, Yamauchi P, et al. Effects of etanercept on C-reactive protein levels in psoriasis and psoriatic arthritis. Br J Dermatol. 2008;159:322–330.
  • Serwin AB, Wasowicz W, Chodynicka B. Selenium supplementation, soluble tumor necrosis factor-alpha receptor type 1, and C-reactive protein during psoriasis therapy with narrowband ultraviolet B. Nutrition. 2006;22:860–864.
  • Coimbra S, Oliveira H, Reis F, et al. Circulating adipokine levels in Portuguese patients with psoriasis vulgaris according to body mass index, severity and therapy. J Eur Acad Dermatology Venereol. 2010;24:1386–1394.
  • Gisondi P, Lora V, Bonauguri C, et al. Serum chemerin is increased in patients with chronic plaque psoriasis and normalizes following treatment with infliximab. Br J Dermatol. 2013;168:749–755.
  • Long JW, Tao J, Pi X, et al. Effect of narrow-band UVB phototherapy on soluble cell adhesion molecules in patients with psoriasis vulgaris. J Int Med Reserach. 2014;38:1507–1512.
  • Dekker-Saeys BJ, Meuwissen SG, Van Den Berg-Loonen EM. et al. Ankylosing spondylitis and inflammatory bowel disease. ii. Prevalence of peripheral arthritis, sacroiliitis, and ankylosing spondylitis in patients suffering from inflammatory bowel disease. Ann Rheum Dis. 1978;37:33–35.
  • Orchard TR, Wordsworth BP, Jewell DP. Peripheral arthropathies in inflammatory bowel disease: their articular distribution and natural history. Gut. 1998;42:387–391.
  • Palm O, Moum B, Ongre A, et al. Prevalence of ankylosing spondylitis and other spondyloarthropathies among patients with inflammatory bowel disease: a population study (the IBSEN study). J Rheumatol. 2002;29:511–515.
  • Salvarani C. Clinical features and epidemiology of spondyloarthritides associated with inflammatory bowel disease. World J Gastroenterol. 2009;15:2449.
  • De Vos M, Cuvelier C, Mielants H, et al. Ileocolonoscopy in seronegative spondylarthropathy. Gastroenterology. 1989;96:339–344.
  • Van Praet L, Van den Bosch FE, Jacques P, et al. Microscopic gut inflammation in axial spondyloarthritis: a multiparametric predictive model. Ann Rheum Dis. 2013;72:414–417.
  • Lees CW, Barrett JC, Parkes M, et al. New IBD genetics: common pathways with other diseases. Gut. 2011;60:1739–1753.
  • Harvey D, Pointon JJ, Evans DM, et al. Investigating the genetic association between ERAP1 and ankylosing spondylitis. Hum Mol Genet. 2009;18:4204–4212.
  • Reveille JD, Sims A-M, Danoy P, et al. Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat Genet. 2010;42:123–127.
  • Tremelling M, Cummings F, Fisher SA, et al. IL23R variation determines susceptibility but not disease phenotype in inflammatory bowel disease. Gastroenterology. 2007;132:1657–1664.
  • Bernstein CN, Fried M, Krabshuis JH, et al. World Gastroenterology Organization Practice Guidelines for the diagnosis and management of IBD in 2010. Inflamm Bowel Dis. 2010;16:112–124.
  • Best W, Becktel J, Singleton J Jr., et al. Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology. 1976;70:439–444.
  • Walmsley RS, Ayres RC, Pounder RE, et al. A simple clinical colitis activity index. Gut. 1998;43:29–32.
  • Schroeder K, Tremaine W, Ilstrup D. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. N Engl J Med. 1987;317:1625–1629.
  • Poullis AP, Zar S, Sundaram KK, et al. A new, highly sensitive assay for C-reactive protein can aid the differentiation of inflammatory bowel disorders from constipation- and diarrhoea-predominant functional bowel disorders. Eur J Gastroenterol Hepatol. 2002;14:409–412.
  • Fagan E, Dyck R, Maton P, et al. Serum levels of C-reactive protein in Crohn’s disease and ulcerative colitis. Eur J Clin Invest. 1982;12:351–359.
  • Chamouard P, Richert Z, Meyer N, et al. Diagnostic value of C-reactive protein for predicting activity level of Crohn’s disease. Clin Gastroenterol Hepatol. 2006;4:882–887.
  • Jürgens M, Mahachie John JM, Cleynen I, et al. Levels of C-reactive protein are associated with response to infliximab therapy in patients with Crohn’s disease. Clin Gastroenterol Hepatol. 2011;9:421–7.e1.
  • Louis E, Vermeire S, Rutgeerts P, et al. A positive response to infliximab in crohn disease: association with a higher systemic inflammation before treatment but not with - 308 TNF Gene Polymorphism. Scand J Clin Lab Invest. 2002;7:818–824.
  • Solem CA, Loftus EV, Tremaine WJ, et al. Correlation of C-reactive protein with clinical, endoscopic, histologic, and radiographic activity in inflammatory bowel disease. Inflamm Bowel Dis. 2005;11:707–712.
  • Wright J, Alp M, Young F, et al. Predictors of acute relapse of Crohn ’ s disease: a laboratory and clinical study. Dig Dis Sci. 1987;32:164–170.
  • Gustot T, Lemmers A, Louis E, et al. Profile of soluble cytokine receptors in Crohn’s disease. Gut. 2005;54:488–495.
  • Koutroubakis IE, Petinaki E, Dimoulios P, et al. Increased serum levels of YKL-40 in patients with inflammatory bowel disease. Int J Colorectal Dis. 2003;18:254–259.
  • Vind I, Johansen J, Price P, et al. Serum YKL-40, a potential new marker of disease activity in patients with inflammatory bowel disease. Scand J Gastroenterol. 2003;38:599–605.
  • Erzin Y, Uzun H, Karatas A, et al. Serum YKL-40 as a marker of disease activity and stricture formation in patients with Crohn’s disease. J Gastroenterol Hepatol. 2008;23(8 Pt 2):e357–62.
  • Herrlinger KR, Dittmann R, Weitz G, et al. Serum procalcitonin differentiates inflammatory bowel disease and self-limited colitis. Inflamm Bowel Dis. 2004;10:229–233.
  • Oruç N, Ozütemiz O, Osmanoğlu N, et al. Diagnostic value of serum procalcitonin in determining. Turkish J Gastroenterol. 2009;20:9–12.
  • Oussalah A, Laurent V, Bruot O, et al. Additional benefit of procalcitonin to C-reactive protein to assess disease activity and severity in Crohn’s disease. Aliment Pharmacol Ther. 2010;32:1135–1144.
  • Sachar D, Smith H, Chan S, et al. Erythrocytic sedimentation rate as a measure of clinical activity in iflammatory bowel disease. J Clin Gastroenterol. 1986;8:647–650.
  • Balding J, Livingstone WJ, Conroy J, et al. Inflammatory bowel disease: the role of inflammatory cytokine gene polymorphisms. Mediators Inflamm. 2004;13:181–187.
  • Shanahan F. Crohn’s disease. Lancet. 2002;359:62–69.
  • Gross V, Andus T, Caesar I, et al. Evidence for continuous stimulation of interleukin-6 production in Crohn ’s disease. Gastroenterology. 1992;102:514–519.
  • Hyams JS, Fitzgerald JE, Treem WR, et al. Relationship of functional and antigenic interleukin 6 to disease activity in inflammatory bowel disease. Gastroenterology. 1993;104:1285–1292.
  • Nancey S, Hamzaoui N, Moussata D, et al. Serum interleukin-6, soluble interleukin-6 receptor and Crohn’s disease activity. Dig Dis Sci. 2008;53:242–247.
  • Goke M, Hoffmann JC, Evers J, et al. Elevated serum concentrations of soluble selectin and immunoglobulin type adhesion molecules in patients with inflammatory bowel disease. J Gastroenterol. 1997;32:480–486.
  • Jones SC, Banks RE, Haidar A, et al. Adhesion molecules in inflammatory bowel disease. Gut. 1995;36:724–730.
  • Magro F, Araujo F, Pereira P, et al. Soluble selectins, sICAM, sVCAM, and angiogenic proteins in different activity groups of patients with inflammatory bowel disease. Dig Dis Sci. 2004;49(7–8):1265–1274.
  • Patel RT, Pall AA, Adu D, et al. Circulating soluble adhesion molecules in inflammatory bowel disease. Eur J Gastroenterol Hepatol. 1995;7:1037–1041.
  • Song WB, Lv YH, Zhang ZS, et al. Soluble intercellular adhesion molecule-1, D-lactate and diamine oxidase in patients with inflammatory bowel disease. World J Gastroenterol. 2009;15:3916–3919.
  • Ates Y, Degertekin B, Erdil A, et al. Serum ghrelin levels in inflammatory bowel disease with relation to disease activity and nutritional status. Dig Dis Sci. 2008;53:2215–2221.
  • Peracchi M, Bardella MT, Caprioli F, et al. Circulating ghrelin levels in patients with inflammatory bowel disease. Gut. 2006;55:432–433.
  • Sung EZH, Da Silva NF, Goodyear S, et al. Increased plasma ghrelin following infliximab in Crohn’s disease. Aliment Pharmacol Ther. 2009;29:83–89.
  • Kader N, El-Din F, Khatab E, et al. Does plasma resistin level have a role in predicting inflammatory bowel disease activity? Indian J Gastroenterol. 2010;29:126–127.
  • Konrad A, Lehrke M, Schachinger V, et al. Resistin is an inflammatory marker of inflammatory bowel disease in humans. Eur J Gastroenterol Hepatol. 2007;19:1070–1074.
  • Morisaki T, Takeshima F, Fukuda H, et al. High serum vaspin concentrations in patients with ulcerative colitis. Dig Dis Sci. 2014;59:315–321.
  • Rodrigues VS, Milanski M, Fagundes JJ, et al. Serum levels and mesenteric fat tissue expression of adiponectin and leptin in patients with Crohn’s disease. Clin Exp Immunol. 2012;170:358–364.
  • Karmiris K, Koutroubakis IE, Xidakis C, et al. Circulating levels of leptin, adiponectin, resistin, and ghrelin in inflammatory bowel disease. Inflamm Bowel Dis. 2006;12:100–105.
  • Weigert J, Obermeier F, Neumeier M, et al. Circulating levels of chemerin and adiponectin are higher in ulcerative colitis and chemerin is elevated in Crohn’s disease. Inflamm Bowel Dis. 2010;16:630–637.
  • Franchimont D, Roland S, Gustot T, et al. Impact of infliximab on serum leptin levels in patients with Crohn’s disease. J Clin Endocrinol Metab. 2005;90:3510–3516.
  • Karmiris K, Koutroubakis IE, Xidakis C, et al. The effect of infliximab on circulating levels of leptin, adiponectin and resistin in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2007;19:789–794.
  • Manolakis AC, Kapsoritakis AN, Georgoulias P, et al. Moderate performance of serum S100A12, in distinguishing inflammatory bowel disease from irritable bowel syndrome. BMC Gastroenterol. 2010;10:118.
  • Brinar M, Cleynen I, Coopmans T, et al. Serum S100A12 as a new marker for inflammatory bowel disease and its relationship with disease activity. Gut. 2010;59:1728–1730.
  • Schimid KW, Lugering N, Stoll R, et al. Immunohistochemical demonstration of the calcium-binding proteins MRP8 and MRP14 and their heterodimer (27E 10 Antigen) in Crohn ’ s disease. Hum Pathol. 1995;26:334–337.
  • Lugering N, Stoll R, Schmid K, et al. The myeloic related protein MRP8/14 (27E10 antigen) - usefulness as a potential marker for disease activity in ulcerative colitis and putative biological function. Hum Pathol. 1995;14:659–664.
  • Meuwis M, Vernier-Massouille G, Grimaud JC, et al. Serum calprotectin as a biomarker for Crohn’s disease. J Crohns Colitis. 2013;7:e678–83.
  • Leach ST, Yang Z, Messina I, et al. Serum and mucosal S100 proteins, calprotectin (S100A8/S100A9) and S100A12, are elevated at diagnosis in children with inflammatory bowel disease. Scand J Gastroenterol. 2007;42:1321–1331.
  • Malícková K, Kalousová M, Fucíková T, et al. Anti-inflammatory effect of biological treatment in patients with inflammatory bowel diseases: calprotectin and IL-6 changes do not correspond to sRAGE changes. Scand J Clin Lab Invest. 2010;70:294–299.
  • Von Roon AC, Karamountzos L, Purkayastha S, et al. Diagnostic precision of fecal calprotectin for inflammatory bowel disease and colorectal malignancy. Am J Gastroenterol. 2007;102:803–813.
  • Van Rheenen PF, Van de Vijver E, Fidler V. Faecal calprotectin for screening of patients with suspected inflammatory bowel disease: diagnostic meta-analysis. Bmj. 2010;341:c3369.
  • Lin J-F, Chen J-M, Zuo J-H, et al. Meta-analysis: fecal calprotectin for assessment of inflammatory bowel disease activity. Inflamm Bowel Dis. 2014;20:1407–1415.
  • Wagner M. Fecal markers of inflammation used as surrogate markers for treatment outcome in relapsing inflammatory bowel disease. World J Gastroenterol. 2008;14:5584.
  • Sipponen T, Björkesten C-GAF, Färkkilä M, et al. Faecal calprotectin and lactoferrin are reliable surrogate markers of endoscopic response during Crohn’s disease treatment. Scand J Gastroenterol. 2010;45:325–331.
  • Kolho K-L, Sipponen T. The long-term outcome of anti-tumor necrosis factor-α therapy related to fecal calprotectin values during induction therapy in pediatric inflammatory bowel disease. Scand J Gastroenterol. 2014;49:434–441.
  • Hämäläinen A, Sipponen T, Kolho K-L. Infliximab in pediatric inflammatory bowel disease rapidly decreases fecal calprotectin levels. World J Gastroenterol. 2011;17:5166–5171.
  • Ferreiro-Iglesias R, Barreiro-de Acosta M, Otero Santiago M, et al. Fecal calprotectin as predictor of relapse in patients with inflammatory bowel disease under maintenance infliximab therapy. J Clin Gastroenterol. 2016;50:147–151.
  • Wright EK, Kamm MA, De Cruz P, et al. Measurement of fecal calprotectin improves monitoring and detection of recurrence of Crohn’s disease after surgery. Gastroenterology. 2015;148:938–947.e1.
  • Janas RM, Ochocińska A, Snitko R, et al. Neutrophil gelatinase-associated lipocalin in blood in children with inflammatory bowel disease. J Gastroenterol Hepatol. 2014;29:1883–1889.
  • Oikonomou KA, Kapsoritakis AN, Theodoridou C, et al. Neutrophil gelatinase-associated lipocalin (NGAL) in inflammatory bowel disease: association with pathophysiology of inflammation, established markers, and disease activity. J Gastroenterol. 2012;47:519–530.
  • Yeşil A, Gönen C, Senateş E, et al. Relationship between neutrophil gelatinase-associated lipocalin (NGAL) levels and inflammatory bowel disease type and activity. Dig Dis Sci. 2013;58:2587–2593.
  • Kim JM. Antimicrobial proteins in intestine and inflammatory bowel diseases. Intest Res. 2014;12:20–33.
  • Yamaguchi N, Isomoto H, Mukae H, et al. Concentrations of alpha- and beta-defensins in plasma of patients with inflammatory bowel disease. Inflamm Res. 2009;58:192–197.
  • Zissis M, Afroudakis A, Galanopoulos G, et al. B2 microglobulin: is it a reliable marker of activity in inflammatory bowel disease? Am J Gastroenterol. 2001;96:2177–2183.
  • Yılmaz B, Köklü S, Yüksel O, et al. Serum beta 2-microglobulin as a biomarker in inflammatory bowel disease. World J Gastroenterol. 2014;20:10916–10920.
  • Dotan I. New serologic markers for inflammatory bowel disease diagnosis. Dig Dis. 2010;28:418–423.
  • Homsak E, Micetić-Turk D, Bozic B. Autoantibodies pANCA, GAB and PAB in inflammatory bowel disease: prevalence, characteristics and diagnostic value. Wien Klin Wochenschr. 2010;122(Suppl 2):19–25.
  • Kuna AT. Review Serological markers of inflammatory bowel disease. Biochem Med. 2013;23:28–42.
  • Bossuyt X. Serologic markers in inflammatory bowel disease. Clin Chem. 2006;52:171–181.
  • Prideaux L, De Cruz P, Ng SC, et al. Serological antibodies in inflammatory bowel disease: a systematic review. Inflamm Bowel Dis. 2012;18:1340–1355.
  • Peeters M, Ph D, Joossens S, et al. Diagnostic value of anti- saccharomyces cerevisiae and antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease. Am J Gastroenterol. 2001;96:731–734.
  • Ruemmele FM, Targan SR, Levy G, et al. Diagnostic accuracy of serological assays in pediatric inflammatory bowel disease. Gastroenterology. 1998;115:822–829.
  • Sandborn WJ, Loftus EV, Colombel JF, et al. Evaluation of serologic disease markers in a population-based cohort of patients with ulcerative Colitis and Crohn’s disease. Inflamm Bowel Dis. 2001;7:192–201.
  • Esters N, Vermeire S, Joossens S, et al. Serological markers for prediction of response to anti-tumor necrosis factor treatment in Crohn’s disease. Am J Gastroenterol. 2002;97:1458–1462.
  • Smith BRK, Arnott IDR, Drummond HE, et al. Disease location, anti-saccharomyces cerevisiae Antibody, and NOD2/CARD15 genotype influence the progression of disease behavior in Crohn’s disease. Inflamm Bowel Dis. 2004;10:521–528.
  • Bonneau J, Dumestre-Perard C, Rinaudo-Gaujous M, et al. Systematic review: new serological markers (anti-glycan, anti-GP2, anti-GM-CSF Ab) in the prediction of IBD patient outcomes. Autoimmun Rev. 2015;14:231–245.
  • Karmiris K, Koutroubakis IE, Kouroumalis EA. Leptin, adiponectin, resistin, and ghrelin–implications for inflammatory bowel disease. Mol Nutr Food Res. 2008;52:855–866.
  • Sari I, Kebapcilar L, Taylan A, et al. Fetuin-A and interleukin-18 levels in ankylosing spondylitis. Int J Rheum Dis. 2010;13:75–81.
  • Wendling D, Racadot E, Auge B, et al. Soluble intercelulular adhesion molecule 1 in spondyloarthritis. Clin Rheumatol. 1998;17:202–204.
  • Kemeny-Beke A, Gesztelyi R, Bodnar N, et al. Increased production of asymmetric dimethylarginine (ADMA) and atherosclerotic disease in ankylosing spondylitis. Joint Bone Spine. 2011;78:184–187.
  • Erre G, Sanna P, Zinellu A, et al. Plasma asymmetric dimethylarginine (ADMA) levels and atherosclerotic disease in akylosing spondylitis: A cross-sectional study. Clin Rheumatol. 2011;30:21–27.
  • O’Shea F, Tsui F, Chiu B, et al. Retinol (vitamin A) and retinol binding protein levels are decreased in ankylosing spondylitis: clinical and genetic analysis. J Rheumatol. 2007;34:2457–2459.
  • Genre F, Lopez-Mejias R, Miranda-Filloy J, et al. Antitumour necrosis factor alpha treatment reduces retinol-binding protein 4 serum levels in non-dianetic ankylosing spondylitis patients. Ann Rheum Dis. 2014;73:941–943.
  • Ozgocmen S, Sogus S, Ardicoglu O, et al. Serum nitric oxide, catalase, superoxide dismtase and malondialdehyde stats in patients with ankylsing spondylitis. Rheumatol Int. 2004;24:80–83.
  • Kozaci L, Sari I, Alacacioglu A, et al. Evaluation of inflammation and oxidative stress in ankylosing spondylitis: a role for macrophage migration inhibitory factor. Mod Rheumatol. 2010;20:34–39.
  • Hoffman I, Dmetter P, Peeters M, et al. Anti-saccharomyces cerevisiae IgA antibodies are raised in ankylosing spondylitis and undifferentiated spondyloarthropathy. Ann Rheum Dis. 2003;62:455–459.
  • Aydin SZ, Atagunduz P, Temel M, et al. Anti-saccharomyces cerevisiae antibodies (ASCA) in spondyloarthropathies: a reassessment. Rheumatology (Oxford). 2008;47:142–144.
  • De Vries M, Van der Horst-Bruinsma I, Van Hoogstraten I, et al. pANCA, ASCA, and OmpC antibodies in patients with ankylosing spondylitis without inflammatory bowel disease. J Rheumatol. 2010;37:2340–2344.
  • Appel H, Maier R, Wu P, et al. Analysis of IL-17(+) cells in facet joints of patients with spondyloarthritis suggests that the innate immune pathway might be of greater relevance than the Th17-mediated adaptive immune response. Arthritis Res Ther. 2011;13:R95.
  • Di Meglio P, Di Cesare A, Laggner U, et al. The IL23R R381Q gene variant protects against immune-mediated diseases by impairing IL-23-induced Th17 effector response in humans. PLoS One. 2011;6:e17160.
  • Sarin R, Wu X, Abraham C. Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4 + and CD8 + human T-cell functional responses. Proc Natl Acad Sci. 2011;108:9560–9565.
  • Raychaudhuri SK, Saxena A, Raychaudhuri SP. Role of IL-17 in the pathogenesis of psoriatic arthritis and axial spondyloarthritis. Clin Rheumatol. 2015;34:1019–1023.
  • DeLay M, Turner M, Klenk E, et al. HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum. 2009;60:2633–2643.
  • Zhang L, Li Y, Li Y, et al. Increased frequencies of Th22 cells as well as Th17 cells in the peripheral blood of patients with ankylosing spondylitis and rheumatoid arthritis. PLoS One. 2012;7:e31000.
  • Kollnberger S, Bird L, Roddis M. HLA-B27 heavy chain homodimers are expressed in HLA-B27 transgenic rodent models of spondyloarthritis and are ligands for paired Ig-like receptors. J Immunol. 2004;173:1699–1710.
  • Smith J, Turner M, DeLay M, et al. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-β induction via X-box binding protein. Eur J Immmunology. 2008;38:1194–1203.
  • Van Duivenvoorde LM, Dorris ML, Satumtira N, et al. Relationship between inflammation, bone destruction, and osteoproliferation in the HLA-B27/human β2 -microglobulin-transgenic rat model of spondylarthritis. Arthritis Rheum. 2012;64:3210–3219.
  • Tran TM, Dorris ML, Satumtira N, et al. Additional human beta2-microglobulin curbs HLA-B27 misfolding and promotes arthritis and spondylitis without colitis in male HLA-B27-transgenic rats. Arthritis Rheum. 2006;54:1317–1327.
  • Hammer RE, Maika SD, Richardson JA, et al. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human Pzm : an animal model of HLRB27-associated human disorders. Cell. 1990;63:1099–1112.
  • Van der Cruyssen B, Ribbens C, Boonen A, et al. The epidemiology of ankylosing spondylitis and the commencement of anti-TNF therapy in daily rheumatology practice. Ann Rheum Dis. 2007;66:1072–1077.
  • Baeten D, Breban M, Lories R, et al. Are spondylarthritides related but distinct conditions or a single disease with a heterogeneous phenotype? Arthritis Rheum. 2013;65:12–20.
  • Takahashi H, Tsuji H, Hashimoto Y, et al. Serum cytokines and growth factor levels in Japanese patients with psoriasis. Clin Exp Dermatol. 2010;35:645–649.
  • Fujino S, Andoh A, Bamba S, et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut. 2003;52:65–70.
  • Melis L, Vandooren B, Kruithof E, et al. Systemic levels of IL-23 are strongly associated with disease activity in rheumatoid arthritis but not spondyloarthritis. Ann Rheum Dis. 2010;69:618–623.