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Overview of biomarkers and their relationship to axial spondyloarthritis associated with idiopathic inflammatory bowel diseases

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Authors: L. Ondrejčáková;  M. Gregová;  L. Šenolt;  K. Pavelka
Authors‘ workplace: Revmatologická klinika 1. LF UK Praha ;  Revmatologický ústav Praha
Published in: Čes. Revmatol., 29, 2021, No. 2, p. 114-124.
Category:

Overview

Axial spondyloarthritis (spondyloarthropathies or spondyloarthritides – axSpA) accompanied by idiopathic bowel disease (IBD), also known as enteropathic spondyloarthritis, are systemic diseases characterized by chronic inflammation of both the musculoskeletal and gastrointestinal tracts. The incidence of IBD in patients with spondylarthritis (SpA) has been reported in 6–14%, but almost 60% of patients with SpA have subclinical macroscopic or microscopic inflammatory bowel disease on endoscopic examination. The presence of the human leukocyte antigen 27 (HLA-B27) gene in SpA/IBD is around 50–80%. This is significantly less than in ankylosing spondylitis (AS), where about 85–95% of patients are HLA-B27 positive. To date, there are few markers that can predict the development of IBD in axSpA. Endoplasmic reticulum aminopeptidase (ERAP-1) appears to be a promising indicator. ERAP-1 is also considered as one of the possible pathophysiological factors that contribute to the development of ulcerative colitis (UC) in patients with axSpA. Other gene variants related to the IL-17/23 pathway have been described. In IBD, a NOD2/CARD15 polymorphism appears to be the candidate gene. The presence of at least one of the three known gene variants of NOD2/CARD15 increases the risk of developing IBD, especially Crohn’s disease (CD), and is also associated with the risk of developing sacroiliitis in patients with IBD. Unlike HLA-B27, NOD2/CARD15 is not associated with a risk of developing SpA in patients with IBD. Disease-specific shared genes such as IL23R, IL12B, STAT3, PTGER4, and others have also been described. Acute phase reactants (CRP, ESR), composite indices (BASDAI, ASDAS score), a group of cytokines (IL-2, IL-6, IL-11, IL-23), pANCA antibodies, ASCA antibodies, and serum and faecal calprotectin are used to diagnose or evaluate disease activity. Predictors of radiographic progression in axSpA include, e.g., the determination of DKK-1, sclerostin and antisclerostin. In this work, we present an overview of the most promising biomarkers to date and their relationship to axial spondylarthritis associated with IBD. Finding suitable biomarkers could shed light not only on the pathogenesis of the disease but also on the possibility of correlating the mutual activity of axSpA and IBD. 

Keywords:

Ulcerative colitis – biomarkers – Crohn’s disease – axial spondyloarthritis – idiopathic inflammatory boewl disease

Sources
  1. Dougados M, Baeten D. Spondyloarthritis. Lancet 2011; 377(9783): 2127–2137.
  2. Rudwaleit M, Landewé R, van der Heijde D, Listing J, Brandt J, Braun J, et al. The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part I): classification of paper patients by expert opinion including uncertainty appraisal. Ann Rheum Dis 2009; 68(6): 770–776.
  3. Rudwaleit M, van der Heijde D, Landewe R, Listing J, Akkoc N, Brandt J, et al. The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis 2009; 68(6): 777–783.
  4. Stolwijk C, Essers I, van Tubergen A, Boonen A, Bazelier MT, De Bruin ML, et al. The epidemiology of extra-articular manifestations in ankylosing spondylitis: a population-based matched cohort study. Ann Rheum Dis 2015; 74(7): 1373–1378.
  5. Cypers H, Varkas G, Beeckman S, Debusschere K, Vogl T, Roth J, et al. Elevated calprotectin levels reveal bowel inflammation in spondyloarthritis. Ann Rheum Dis 2016; 75(7): 1357–1362. 
  6. Rudwaleit M, Baeten D. Ankylosing spondylitis and bowel disease. Best Pract Res Clin Rheumatol 2006; 20(3): 451–471.
  7. van Praet L, Van den Bosch FE, Jacques P, Carron P, Jans L, Colman R, et al. Microscopic gut inflammation in axial spondyloarthritis: a multiparametric predictive model. Ann Rheum Dis 2013; 72(3): 414–417.
  8. de Vos M, Mielants H, Cuvelier C, Elewaut A, Veys E. Long-term evolution of gut inflammation in patients with spondyloarthropathy. Gastroenterology 1996; 110(6): 1696–1703.
  9. Gilis E, Mortier C, Venken K, Debusschere K, Vereecke L, Elewaut D. The Role of the Microbiome in Gut and Joint Inflammation in Psoriatic Arthritis and Spondyloarthritis. J Rheumatol Suppl 2018; 94: 36–39.
  10. Rudwaleit M, Haibel H, Baraliakos X, Listing J, Märker-Hermann E, Zeidler H, et al. The early disease stage in axial spondylarthritis: results from the German Spondyloarthritis Inception Cohort. Arthritis Rheum 2009; 60(3): 717–727.
  11. Salvarani C, Fries W. Clinical features and epidemiology of spondyloarthritides associated with inflammatory bowel disease. World J Gastroenterol 2009; 15(20): 2449–2455. 
  12. Rothfuss KS, Stange EF, Herrlinger KR. Extraintestinal manifestations and complications in inflammatory bowel diseases. World J Gastroenterol 2006; 12(30): 4819–4831.
  13. Essers I, Ramiro S, Stolwijk C, Blaauw M, Landewé R, van der Heijde D, et al. Characteristics associated with the presence and development of extra-articular manifestations in ankylosing spondylitis: 12-year results from OASIS. Rheumatology (Oxford) 2015; 54(4): 633–640.
  14. Benfaremo D, Luchetti MM, Gabrielli A. Biomarkers in Inflammatory Bowel Disease-Associated Spondyloarthritis: State of the Art and Unmet Needs. J Immunol Res 2019; 2019: 8630871.
  15. Khan MA. Remarkable polymorphism of HLA-B27: an ongoing saga. Curr Rheumatol Rep 2010; 12(5): 337–341.
  16. Schlosstein L, Terasaki PI, Bluestone R, Pearson CM. High association of an HL-A antigen, W27, with ankylosing spondylitis. N Engl J Med 1973; 288(14): 704–706.
  17. Brown MA, Pile KD, Kennedy LG, Calin A, Darke C, Bell J, et al. HLA class I associations of ankylosing spondylitis in the white population in the United Kingdom. Ann Rheum Dis 1996; 55(4): 268–270.
  18. Colombo E, Latiano A, Palmieri O, Bossa F, Andriulli A, Annese V. Enteropathic spondyloarthropathy: a common genetic background with inflammatory bowel disease? World J Gastroenterol 2009; 15(20): 2456–2462.
  19. Brewerton DA, Caffrey M, Nicholls A, Walters D, James DC. HL-A 27 and arthropathies associated with ulcerative colitis and psoriasis. Lancet 1974; 1(7864): 956–958.
  20. Dekker-Saeys BJ, Meuwissen SG, Van Den Berg-Loonen EM, De Haas WH, Meijers KA, Tytgat GN. Ankylosing spondylitis and inflammatory bowel disease. III. Clinical characteristics and results of histocompatibility typing (HLA B27) in 50 patients with both ankylosing spondylitis and inflammatory bowel disease. Ann Rheum Dis 1978; 37(1): 36–41.
  21. Mallas EG, Mackintosh P, Asquith P, Cooke WT. Histocompatibility antigens in inflammatory bowel disease. Their clinical significance and their association with arthropathy with special reference to HLA-B27 (W27). Gut 1976; 17(11): 906–910. 
  22. Danve A, O’Dell J. The ongoing quest for biomarkers in Ankylosing Spondylitis. Int J Rheum Dis 2015; 18(8): 826–834.
  23. Saulle I, Vicentini C, Clerici M, Biasin M. An Overview on ERAP Roles in Infectious Diseases. Cells 2020; 9(3).
  24. Kenna TJ, Robinson PC, Haroon N. Endoplasmic reticulum aminopeptidases in the pathogenesis of ankylosing spondylitis. Rheumatology (Oxford) 2015; 54(9): 1549–1556.
  25. Reeves E, James E. The role of polymorphic ERAP1 in autoinflammatory disease. Biosci Rep 2018; 38(4).
  26. Laukens D, Georges M, Libioulle C, Sandor C, Mni M, Vander Cruyssen B, et al. Evidence for significant overlap between common risk variants for Crohn’s disease and ankylosing spondylitis. PLoS One 2010; 5(11): e13795.
  27. Reveille JD. Genetics of spondyloarthritis – beyond the MHC. Nat Rev Rheumatol 2012; 8(5): 296–304.
  28. Yago T, Nanke Y, Kawamoto M, Kobashigawa T, Yamanaka H, Kotake S. IL-23 and Th17 Disease in Inflammatory Arthritis. J Clin Med 2017; 6(9).
  29. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000; 13(5): 715–725.
  30. Smith JA, Colbert RA. Review: The interleukin-23/interleukin-17 axis in spondyloarthritis pathogenesis: Th17 and beyond. Arthritis Rheumatol 2014; 66(2): 231–241.
  31. van Praet L, Van den Bosch F, Mielants H, Elewaut D. Mucosal inflammation in spondylarthritides: past, present, and future. Curr Rheumatol Rep 2011; 13(5): 409–415.
  32. Abraham C, Cho JH. Functional consequences of NOD2 (CARD15) mutations. Inflamm Bowel Dis 2006; 12(7): 641–650. al. Crohn’s disease and the NOD2 gene: a role for paneth cells. Gastroenterology. 2003; 125(1): 47-57.
  33. Lala S, Ogura Y, Osborne C, Hor SY, Bromfield A, Davies S, et al. Crohn’s disease and the NOD2 gene: a role for paneth cells. Gastroenterology. 2003; 125(1): 47-57.
  34. Ogura Y, Inohara N, Benito A, Chen FF, Yamaoka S, Nunez G. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-kappaB. J Biol Chem 2001; 276(7): 4812–4818.
  35. Kupka T, Simova J, Dvorackova J, Martinek L, Motyka O, Uvirova M, et al. Crohn’s disease – genetic factors and progress of the disease. Biomed Pap Med Fac Univ Palacky Olomouc Czech Republic 2018; 162(2): 139–143.
  36.  Arvikar SL, Fisher MC. Inflammatory bowel disease associated arthropathy. Curr Rev Musculoskelet Med 2011; 4(3): 123–131.
  37. Voulgari PV. Rheumatological manifestations in inflammatory bowel disease. Ann Gastroenterol 2011; 24(3): 173–180.
  38. Brakenhoff LK, van der Heijde DM, Hommes DW, Huizinga TW, Fidder HH. The joint-gut axis in inflammatory bowel diseases. J Crohns Colitis 2010; 4(3): 257–268.
  39. Sheth T, Pitchumoni CS, Das KM. Management of Musculoskeletal Manifestations in Inflammatory Bowel Disease. Gastroenterol Res Pract. 2015; 2015: 387891.
  40. Devlin SM, Yang H, Ippoliti A, Taylor KD, Landers CJ, Su X, et al. NOD2 variants and antibody response to microbial antigens in Crohn’s disease patients and their unaffected relatives. Gastroenterology 2007; 132(2): 576–586.
  41. Karban A, Dagan E, Eliakim R, Herman A, Nesher S, Weiss B, et al. Prevalence and significance of mutations in the familial Mediterranean fever gene in patients with Crohn’s disease. Genes Immun 2005; 6(2): 134–139.
  42. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nuñez G, et al. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005; 307(5710): 731–734.
  43. Hugot JP, Zaccaria I, Cavanaugh J, Yang H, Vermeire S, Lappalainen M, et al. Prevalence of CARD15/NOD2 mutations in Caucasian healthy people. Am J Gastroenterol 2007; 102(6): 1259–1267.
  44. Pauleau AL, Murray PJ. Role of nod2 in the response of macrophages to toll-like receptor agonists. Mol Cell Biol 2003; 23(21): 7531–7539.
  45. Derakhshan F, Naderi N, Farnood A, Firouzi F, Habibi M, Rezvany MR, et al. Frequency of three common mutations of CARD15/NOD2 gene in Iranian IBD patients. Indian J Gastroenterol 2008; 27(1): 8–11.
  46. Economou M, Trikalinos TA, Loizou KT, Tsianos EV, Ioannidis JP. Differential effects of NOD2 variants on Crohn’s disease risk and phenotype in diverse populations: a metaanalysis. Am J Gastroenterol 2004; 99(12): 2393–2404.
  47. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 2003; 3(7): 521–533.
  48. Laukens D, Peeters H, Marichal D, Vander Cruyssen B, Mielants H, Elewaut D, et al. CARD15 gene polymorphisms in patients with spondyloarthropathies identify a specific phenotype previously related to Crohn’s disease. Ann Rheum Dis 2005; 64(6): 930–935.
  49. Ossum AM, Palm Ø, Lunder AK, Cvancarova M, Banitalebi H, Negård A, et al. Ankylosing Spondylitis and Axial Spondyloarthritis in Patients With Long-term Inflammatory Bowel Disease: Results From 20 Years of Follow-up in the IBSEN Study. J Crohns Colitis 2018; 12(1): 96–104.
  50. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, Huett A, et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 2007; 39(5): 596–604.
  51. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, Huse K, et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 2007; 39(2): 207–211.
  52. McGovern DP, Gardet A, Törkvist L, Goyette P, Essers J, Taylor KD, et al. Genome-wide association identifies multiple ulcerative colitis susceptibility loci. Nat Genet 2010; 42(4): 332–337. 
  53. McCarroll SA, Huett A, Kuballa P, Chilewski SD, Landry A, Goyette P, et al. Deletion polymorphism upstream of IRGM associated with altered IRGM expression and Crohn’s disease. Nat Genet 2008; 40(9): 1107–1112.
  54. Sieper J, Rudwaleit M, Khan MA, Braun J. Concepts and epidemiology of spondyloarthritis. Best Pract Res Clin Rheumatol 2006; 20(3): 401–417.
  55. Calin A, Garrett S, Whitelock H, Kennedy LG, O’Hea J, Mallorie P, et al. A new approach to defining functional ability in ankylosing spondylitis: the development of the Bath Ankylosing Spondylitis Functional Index. J Rheumatol 1994; 21(12): 2281–2285.
  56. Poddubnyy DA, Rudwaleit M, Listing J, Braun J, Sieper J. 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(7): 1338–1341.
  57. Chamouard P, Richert Z, Meyer N, Rahmi G, Baumann R. Diagnostic value of C-reactive protein for predicting activity level of Crohn’s disease. Clin Gastroenterol Hepatol 2006; 4(7): 882–887.
  58. Jürgens M, Mahachie John JM, Cleynen I, Schnitzler F, Fidder H, van Moerkercke W, 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(5): 421–427. e1.
  59. Pedersen SJ, Sørensen 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 TNFα inhibitors. Ann Rheum Dis 2011; 70(8): 1375–1381.
  60. Romero-Sanchez C, Jaimes DA, Londoño J, de Avila J, Castellanos JE, Bello JM, et al. Association between Th-17 cytokine profile and clinical features in patients with spondyloarthritis. Clin Exp Rheumatol 2011; 29(5): 828–834.
  61. Sveaas SH, Berg IJ, Provan SA, Semb AG, Olsen IC, Ueland T, et al. Circulating levels of inflammatory cytokines and cytokine receptors in patients with ankylosing spondylitis: a cross-sectional comparative study. Scand J Rheumatol 2015; 44(2): 118–124.
  62. Ugur M, Baygutalp NK, Melikoglu MA, Baygutalp F, Altas EU, Seferoglu B. Elevated serum interleukin-23 levels in ankylosing spondylitis patients and the relationship with disease activity. Nagoya J Med Sci 2015; 77(4): 621–627.
  63. Baeten D, Østergaard M, Wei JC, Sieper J, Järvinen P, Tam LS, et al. Risankizumab, an IL-23 inhibitor, for ankylosing spondylitis: results of a randomised, double-blind, placebo-controlled, proof-of-concept, dose-finding phase 2 study. Ann Rheum Dis 2018; 77(9): 1295–1302. 
  64. Gheita TA, El G, II, El-Fishawy HS, Aboul-Ezz MA, Kenawy SA. Involvement of IL-23 in enteropathic arthritis patients with inflammatory bowel disease: preliminary results. Clin Rheumatol 2014; 33(5): 713–717.
  65. Liu F, Wang F, Wang CC, Li N, Li SF. Expression of IL-2 and IL-11 and its significance in patients with ankylosing spondylitis. Asian Pac J Trop Med 2013; 6(1): 76–78.
  66. Ometto F, Friso L, Astorri D, Botsios C, Raffeiner B, Punzi L, et al. Calprotectin in rheumatic diseases. Exp Biol Med (Maywood) 2017; 242(8): 859–873.
  67. Røseth AG, Fagerhol MK, Aadland E, Schjønsby H. Assessment of the neutrophil dominating protein calprotectin in feces. A methodologic study. Scand J Gastroenterol 1992; 27(9): 793–798
  68. Kruithof E, de Rycke L, Vandooren B, De Keyser F, FitzGerald O, McInnes I, et al. Identification of synovial biomarkers of response to experimental treatment in early-phase clinical trials in spondylarthritis. Arthritis Rheum 2006; 54(6): 1795–1804.
  69. Turina MC, Sieper J, Yeremenko N, Conrad K, Haibel H, Rudwaleit M, et al. Calprotectin serum level is an independent marker for radiographic spinal progression in axial spondyloarthritis. Ann Rheum Dis 2014; 73(9): 1746–1748.
  70. Hu H, Du F, Zhang S, Zhang W. Serum calprotectin correlates with risk and disease severity of ankylosing spondylitis and its change during first month might predict favorable response to treatment. Mod Rheumatol 2019; 29(5): 836–842.
  71. Klingberg E, Strid H, Ståhl A, Deminger A, Carlsten H, Öhman L, et al. A longitudinal study of fecal calprotectin and the development of inflammatory bowel disease in ankylosing spondylitis. Arthritis Res Ther 2017; 19(1): 21.
  72. Klingberg E, Carlsten H, Hilme E, Hedberg M, Forsblad-d’Elia H. Calprotectin in ankylosing spondylitis – frequently elevated in feces, but normal in serum. Scand J Gastroenterol 2012; 47(4): 435–444.
  73. de Rycke L, Baeten D, Foell D, Kruithof E, Veys EM, Roth J, et al. Differential expression and response to anti-TNFalpha treatment of infiltrating versus resident tissue macrophage subsets in autoimmune arthritis. J Pathol 2005; 206(1): 17–27.
  74. Duran A, Kobak S, Sen N, Aktakka S, Atabay T, Orman M. Fecal calprotectin is associated with disease activity in patients with ankylosing spondylitis. Bosn J Basic Med Sci 2016; 16(1): 71–74.
  75. Røseth AG, Schmidt PN, Fagerhol MK. Correlation between faecal excretion of indium-111-labelled granulocytes and calprotectin, a granulocyte marker protein, in patients with inflammatory bowel disease. Scand J Gastroenterol 1999; 34(1): 50–54.
  76. Prideaux L, De Cruz P, Ng SC, Kamm MA. Serological antibodies in inflammatory bowel disease: a systematic review. Inflamm Bowel Dis 2012; 18(7): 1340–1355. 
  77. Hoffenberg EJ, Fidanza S, Sauaia A. Serologic testing for inflammatory bowel disease. J Pediatr 1999; 134(4): 447–452.
  78. Oshitani N, Hato F, Matsumoto T, Jinno Y, Sawa Y, Hara J, et al. Decreased anti-Saccharomyces cerevisiae antibody titer by mesalazine in patients with Crohn’s disease. J Gastroenterol Hepatol 2000; 15(12): 1400–1403.
  79. de Vries M, van der Horst-Bruinsma I, van Hoogstraten I, van Bodegraven A, von Blomberg BM, Ratnawati H, et al. pANCA, ASCA, and OmpC antibodies in patients with ankylosing spondylitis without inflammatory bowel disease. J Rheumatol 2010; 37(11): 2340–2344.
  80. Riente L, Chimenti D, Pratesi F, Delle Sedie A, Tommasi S, Tommasi C, et al. Antibodies to tissue transglutaminase and Saccharomyces cerevisiae in ankylosing spondylitis and psoriatic arthritis. J Rheumatol 2004; 31(5): 920–924.
  81. Romero-Sánchez C, Bautista-Molano W, Parra V, de Avila J, Rueda JC, Bello-Gualtero JM, et al. Gastrointestinal Symptoms and Elevated Levels of Anti-Saccharomyces cerevisiae Antibodies Are Associated with Higher Disease Activity in Colombian Patients with Spondyloarthritis. Int J Rheumatol 2017; 2017: 4029584.
  82. O’Mahony S, Anderson N, Nuki G, Ferguson A. Systemic and mucosal antibodies to Klebsiella in patients with ankylosing spondylitis and Crohn’s disease. Ann Rheum Dis 1992; 51(12): 1296–1300.
  83. Tiwana H, Walmsley RS, Wilson C, Yiannakou JY, Ciclitira PJ, Wakefield AJ, et al. Characterization of the humoral immune response to Klebsiella species in inflammatory bowel disease and ankylosing spondylitis. Br J Rheumatol 1998; 37(5): 525–531.
  84. Tiwana H, Natt RS, Benitez-Brito R, Shah S, Wilson C, Bridger S, et al. Correlation between the immune responses to collagens type I, III, IV and V and Klebsiella pneumoniae in patients with Crohn’s disease and ankylosing spondylitis. Rheumatology (Oxford) 2001; 40(1): 15–23.
  85. Cooper R, Fraser SM, Sturrock RD, Gemmell CG. Raised titres of anti-klebsiella IgA in ankylosing spondylitis, rheumatoid arthritis, and inflammatory bowel disease. Br Med J (Clin Res Ed) 1988; 296(6634): 1432–1434.
  86. Bernardi D, Podswiadek M, Zaninotto M, Punzi L, Plebani M. YKL-40 as a marker of joint involvement in inflammatory bowel disease. Clin Chem 2003; 49(10): 1685–1688.
  87. Zou YC, Yang XW, Yuan SG, Zhang P, Ye YL, Li YK. Downregulation of dickkopf-1 enhances the proliferation and osteogenic potential of fibroblasts isolated from ankylosing spondylitis patients via the Wnt/β-catenin signaling pathway in vitro. Connect Tissue Res 2016; 57(3): 200–211.
  88. Huang J, Song G, Yin Z, Luo X, Ye Z. Elevated miR-29a expression is not correlated with disease activity index in PBMCs of patients with ankylosing spondylitis. Mod Rheumatol 2014; 24(2): 331–334.
  89. Uderhardt S, Diarra D, Katzenbeisser J, David JP, Zwerina J, Richards W, et al. Blockade of Dickkopf (DKK)-1 induces fusion of sacroiliac joints. Ann Rheum Dis 2010; 69(3): 592–597. 
  90. Diarra D, Stolina M, Polzer K, Zwerina J, Ominsky MS, Dwyer D, et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007; 13(2): 156–163.
  91. Daoussis D, Liossis SN, Solomou EE, Tsanaktsi A, Bounia K, Karampetsou M, et al. Evidence that Dkk-1 is dysfunctional in ankylosing spondylitis. Arthritis Rheum 2010; 62(1): 150–158.
  92. 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): 2523–2527.
  93. 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.
  94. 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): 1349–1356.
  95. Perrotta FM, Ceccarelli F, Barbati C, Colasanti T, De Socio A, Scriffignano S, et al. Serum Sclerostin as a Possible Biomarker in Ankylosing Spondylitis: A Case-Control Study. J Immunol Res 2018; 2018: 9101964.
  96. Luchetti MM, Ciccia F, Avellini C, Benfaremo D, Guggino G, Farinelli A, et al. Sclerostin and Antisclerostin Antibody Serum Levels Predict the Presence of Axial Spondyloarthritis in Patients with Inflammatory Bowel Disease. J Rheumatol 2018; 45(5): 630–637.
  97. Gupta L, Bhattacharya S, Aggarwal A. Tenascin-C, a biomarker of disease activity in early ankylosing spondylitis. Clin Rheumatol 2018; 37(5): 1401–1405.
  98. 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.
  99. Ribbens C, Andre B, Kaye O, Kaiser MJ, Bonnet V, Jaspar JM, et al. Synovial fluid matrix metalloproteinase-3 levels are increased in inflammatory arthritides whether erosive or not. Rheumatology (Oxford) 2000; 39(12): 1357–1365.
  100. Murphy G, Nagase H. Progress in matrix metalloproteinase research. Mol Aspects Med 2008; 29(5): 290–308.
  101. Mattey DL, Packham JC, Nixon NB, Coates L, Creamer P, Hailwood S, et al. Association of cytokine and matrix metalloproteinase profiles with disease activity and function in ankylosing spondylitis. Arthritis Res Ther 2012; 14(3): R127.
  102. Drouart M, Saas P, Billot M, Cedoz JP, Tiberghien P, Wendling D, et al. High serum vascular endothelial growth factor correlates with disease activity of spondylarthropathies. Clin Exp Immunol 2003; 132(1): 158–162.
  103. Poddubnyy D, Conrad K, Haibel H, Syrbe U, Appel H, Braun J, 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(12): 2137–2143.
  104. Udalova IA, Ruhmann M, Thomson SJ, Midwood KS. Expression and immune function of tenascin-C. Crit Rev Immunol 2011; 31(2): 115–145.
  105. Juneja SC, Veillette C. Defects in tendon, ligament, and enthesis in response to genetic alterations in key proteoglycans and glycoproteins: a review. Arthritis 2013; 2013: 154812. 
  106. Järvinen TA, Jozsa L, Kannus P, Järvinen TL, Kvist M, Hurme T, et al. Mechanical loading regulates tenascin-C expression in the osteotendinous junction. J Cell Sci 1999; 112 Pt 18: 3157–3166.
  107. de Winter JJ, van de Sande MG, Baerlecken N, Berg I, Ramonda R, van der Heijde D, et al. Anti-CD74 antibodies have no diagnostic value in early axial spondyloarthritis: data from the spondyloarthritis caught early (SPACE) cohort. Arthritis Res Ther 2018; 20(1): 38.
  108. Baerlecken NT, Nothdorft S, Stummvoll GH, Sieper J, Rudwaleit M, Reuter S, et al. Autoantibodies against CD74 in spondyloarthritis. Ann Rheum Dis 2014; 73(6): 1211–1214.
  109. D’Incà R, Podswiadek M, Ferronato A, Punzi L, Salvagnini M, Sturniolo GC. Articular manifestations in inflammatory bowel disease patients: a prospective study. Dig Liver Dis 2009; 41(8): 565–569.
  110. Peeters H, Vander Cruyssen B, Mielants H, de Vlam K, Vermeire S, Louis E, et al. Clinical and genetic factors associated with sacroiliitis in Crohn’s disease. J Gastroenterol Hepatol 2008; 23(1): 132–137.
  111. Orchard TR, Holt H, Bradbury L, Hammersma J, McNally E, Jewell DP, et al. The prevalence, clinical features and association of HLA-B27 in sacroiliitis associated with established Crohn’s disease. Aliment Pharmacol Ther 2009; 29(2): 193–197.
Labels
Dermatology & STDs Paediatric rheumatology Rheumatology
Doporučení České revmatologické společnosti pro farmakologickou léčbu axiálních spondyloartritid
Impact of adherence to pharmacotherapy in rheumatic diseases
Nová doporučení pro léčbu lupusové nefritidy
Jak ovlivňuje biologická léčba práceschopnost u nemocných s axiální spondyloartritidou – výsledky z Českého národního registru ATTRA
Reproductive health care in women with rheumatoid arthritis, psoriasis and psoriatic arthritis of childbearing age in routine clinical practice
NOVÁ DOPORUČENÍ PRO PACIENTY s dnou a zvýšenou hladinou kyseliny močové v krvi
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Czech Rheumatology

Issue 2
2021 Issue 2
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