Skip to main content

Advertisement

Log in

Non-radiographic axial spondyloarthritis in Tunisia: main characteristics and detailed comparison with ankylosing spondylitis

  • Original Article
  • Published:
Clinical Rheumatology Aims and scope Submit manuscript

Abstract

Objectives

The aim of the present study is to compare the clinical features, disease activity, and physical impairment between non-radiographic axial spondyloarthritis and ankylosing spondylitis in Tunisian patients.

Methods

This is a retrospective study conducted in a single rheumatology center in Tunisia. Patients with axial spondyloarthritis fulfilling the 2009 ASAS criteria were included. The various spondyloarthritis-related variables were compared between non-radiographic axial spondyloarthritis and ankylosing spondylitis. p Values below 0.05 were considered statistically significant.

Results

Among 200 patients with axial spondyloarthritis, 40 had non-radiographic axial spondyloarthritis and 160 had ankylosing spondylitis. The non-radiographic axial spondyloarthritis patients were more frequently female, were younger, and had shorter disease duration. Patients with non-radiographic axial spondyloarthritis experienced enthesitis more frequently compared with ankylosing spondylitis patients. Psoriasis was more frequent in non-radiographic axial spondyloarthritis group, while inflammatory bowel disease was more frequent in ankylosing spondylitis group. The C-reactive protein level and functional score were significantly higher in patients with ankylosing spondylitis compared with non-radiographic axial spondyloarthritis. Tumor necrosis factor inhibitors were offered significantly more often to the ankylosing spondylitis group. There was no statistically significant difference between the 2 groups in other spondyloarthritis parameters.

Conclusion

The non-radiographic axial spondyloarthritis is characterized mainly by a marked female prevalence, a higher enthesitis prevalence, and a better physical function.

Key points:

• Patients with nr-axSpA in Tunisia are more frequently female and have shorter disease duration compared with those with AS.

• Peripheral manifestations were similar between nr-axSpA and AS patients except for enthesitis which were more frequent within nr-axSpA patients.

• The disease activity is similar between the 2 groups of axSpA but the physical function is better within nr-axSpA patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Sieper J, Hu X, Black CM, Grootscholten K, van den Broek RWM, Kachroo S (2017) Systematic review of clinical, humanistic, and economic outcome comparisons between radiographic and non-radiographic axial spondyloarthritis. Semin Arthritis Rheum 46(6):746–753

    Article  Google Scholar 

  2. Deodhar A, Reveille JD, van den Bosch F, Braun J, Burgos-Vargas R, Caplan L, Clegg DO, Colbert RA, Gensler LS, van der Heijde D, van der Horst-Bruinsma IE, Inman RD, Maksymowych WP, Mease PJ, Raychaudhuri S, Reimold A, Rudwaleit M, Sieper J, Weisman MH, Landewé RBM (2014) The concept of axial spondyloarthritis: joint statement of the spondyloarthritis research and treatment network and the Assessment of SpondyloArthritis international Society in response to the US Food and Drug Administration’s comments and concerns. Arthritis Rheumatol Hoboken NJ 66(10):2649–2656

    Article  CAS  Google Scholar 

  3. Braun J, Baraliakos X, Kiltz U, Heldmann F, Sieper J (2015) Classification and diagnosis of axial spondyloarthritis--what is the clinically relevant difference? J Rheumatol 42(1):31–38

    Article  Google Scholar 

  4. Poddubnyy D, Sieper J (2014) Similarities and differences between nonradiographic and radiographic axial spondyloarthritis: a clinical, epidemiological and therapeutic assessment. Curr Opin Rheumatol 26(4):377–383

    Article  CAS  Google Scholar 

  5. Zhao SS, Ermann J, Xu C, Lyu H, Tedeschi SK, Liao KP, Yoshida K, Moots RJ, Goodson NJ, Solomon DH (2019) Comparison of comorbidities and treatment between ankylosing spondylitis and non-radiographic axial spondyloarthritis in the United States. Rheumatol Oxf Engl 58(11):2025–2030

    Article  CAS  Google Scholar 

  6. Erol K, Gok K, Cengiz G, Kilic G, Kilic E, Ozgocmen S (2018) Extra-articular manifestations and burden of disease in patients with radiographic and non-radiographic axial spondyloarthritis. Acta Reumatol Port 43(1):32–39

    PubMed  Google Scholar 

  7. Glintborg B, Sørensen IJ, Østergaard M, Dreyer L, Mohamoud AA, Krogh NS, Hendricks O, Andersen LS, Raun JL, Kowalski MR, Danielsen L, Pelck R, Nordin H, Pedersen JK, Kraus DGA, Christensen SR, Hansen IMJ, Esbesen J, Schlemmer A, Loft AG, al Chaer N, Salomonsen L, Hetland ML (2017) Ankylosing spondylitis versus nonradiographic axial spondyloarthritis: comparison of tumor necrosis factor inhibitor effectiveness and effect of HLA-B27 status. An Observational Cohort Study from the Nationwide DANBIO Registry. J Rheumatol 44(1):59–69

    Article  CAS  Google Scholar 

  8. Kilic E, Kilic G, Akgul O, Ozgocmen S (2015) Discriminant validity of the Ankylosing Spondylitis Disease Activity Score (ASDAS) in patients with non-radiographic axial spondyloarthritis and ankylosing spondylitis: a cohort study. Rheumatol Int 35(6):981–989

    Article  Google Scholar 

  9. Ciurea A, Scherer A, Exer P, Bernhard J, Dudler J, Beyeler B, Kissling R, Stekhoven D, Rufibach K, Tamborrini G, Weiss B, Müller R, Nissen MJ, Michel BA, van der Heijde D, Dougados M, Boonen A, Weber U, on behalf of the Rheumatologists of the Swiss Clinical Quality Management Program for Axial Spondyloarthritis (2013) Tumor necrosis factor α inhibition in radiographic and nonradiographic axial spondyloarthritis: results from a large observational cohort. Arthritis Rheum 65(12):3096–3106

    Article  CAS  Google Scholar 

  10. Hong C, Kwan YH, Leung Y-Y, Lui NL, Fong W (2019) Comparison of ankylosing spondylitis and non-radiographic axial spondyloarthritis in a multi-ethnic Asian population of Singapore. Int J Rheum Dis 22(8):1506–1511

    CAS  PubMed  Google Scholar 

  11. Malaviya AN, Kalyani A, Rawat R, Gogia SB (2015) Comparison of patients with ankylosing spondylitis (AS) and non-radiographic axial spondyloarthritis (nr-axSpA) from a single rheumatology clinic in New Delhi. Int J Rheum Dis 18(7):736–741

    Article  Google Scholar 

  12. Rudwaleit M, van der Heijde D, Landewé R, Listing J, Akkoc N, Brandt J et al (2009) The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis 68(6):777–783

    Article  CAS  Google Scholar 

  13. Mease PJ, Heijde DVD, Karki C, Palmer JB, Liu M, Pandurengan R, Park Y, Greenberg JD (2018) Characterization of patients with ankylosing spondylitis and nonradiographic axial spondyloarthritis in the US-based Corrona Registry. Arthritis Care Res 70(11):1661–1670

    Article  Google Scholar 

  14. de Winter JJ, van Mens LJ, van der Heijde D, Landewé R, Baeten DL (2016) Prevalence of peripheral and extra-articular disease in ankylosing spondylitis versus non-radiographic axial spondyloarthritis: a meta-analysis. Arthritis Res Ther 18:196

    Article  Google Scholar 

  15. López-Medina C, Ramiro S, van der Heijde D, Sieper J, Dougados M, Molto A (2019) Characteristics and burden of disease in patients with radiographic and non-radiographic axial Spondyloarthritis: a comparison by systematic literature review and meta-analysis. RMD Open 5(2):e001108

    Article  Google Scholar 

  16. Wallis D, Haroon N, Ayearst R, Carty A, Inman RD (2013) Ankylosing spondylitis and nonradiographic axial spondyloarthritis: part of a common spectrum or distinct diseases? J Rheumatol 40(12):2038–2041

    Article  Google Scholar 

  17. Rudwaleit M, Haibel H, Baraliakos X, Listing J, Märker-Hermann E, Zeidler H, Braun J, Sieper J (2009) The early disease stage in axial spondylarthritis: results from the German Spondyloarthritis Inception Cohort. Arthritis Rheum 60(3):717–727

    Article  CAS  Google Scholar 

  18. Gavali M, Konda K, Rajasekhar L, Devarasetti PK, Irlapati RV (2015) A comparison of clinical and laboratory profile of non-radiographic axial spondyloarthritis and ankylosing spondylitis. Indian J Rheumatol 10(3):129–132

    Article  Google Scholar 

  19. López-Medina C, Molto A, Claudepierre P, Dougados M (2020) Clinical manifestations, disease activity and disease burden of radiographic versus non-radiographic axial spondyloarthritis over 5 years of follow-up in the DESIR cohort. Ann Rheum Dis 79(2):209–216

    Article  Google Scholar 

  20. Kiltz U, Baraliakos X, Karakostas P, Igelmann M, Kalthoff L, Klink C, Krause D, Schmitz-Bortz E, Flörecke M, Bollow M, Braun J (2012) Do patients with non-radiographic axial spondylarthritis differ from patients with ankylosing spondylitis? Arthritis Care Res 64(9):1415–1422

    Article  Google Scholar 

  21. Khor B, Gardet A, Xavier RJ (2011) Genetics and pathogenesis of inflammatory bowel disease. Nature 474(7351):307–317

    Article  CAS  Google Scholar 

  22. Puig L, Julià A, Marsal S (2014) The Pathogenesis and Genetics of Psoriasis. Actas Dermo-Sifiliográficas Engl Ed 105(6):535–545

    Article  CAS  Google Scholar 

  23. Lu S, Yan Y, Li Z, Chen L, Yang J, Zhang Y, Wang S, Liu L (2017) Determination of genes related to uveitis by utilization of the random walk with restart algorithm on a protein–protein interaction network. Int J Mol Sci 18(5):1045. https://doi.org/10.3390/ijms18051045

    Article  CAS  PubMed Central  Google Scholar 

  24. Feki S, Bouzid D, Abida O, Chtourou L, Elloumi N, Toumi A, Hachicha H, Amouri A, Tahri N, Masmoudi H (2017) Genetic association and phenotypic correlation of TLR4 but not NOD2 variants with Tunisian inflammatory bowel disease. J Dig Dis. 18:625–633. https://doi.org/10.1111/1751-2980.12552

    Article  CAS  PubMed  Google Scholar 

  25. Zouiten-Mekki L, Zaouali H, Boubaker J, Karoui S, Fekih M, Matri S, Hamzaoui S, Filali A, Chaabouni H, Hugot JP (2005) CARD15/NOD2 in a Tunisian population with Crohn’s Disease. Dig Dis Sci 50(1):130–135

    Article  CAS  Google Scholar 

  26. Hama I, Ratbi I, Reggoug S, Elkerch F, Kharrasse G, Errabih I, Ouazzani H, Sefiani A (2012) Non-association of Crohn’s disease with NOD2 gene variants in Moroccan patients. Gene 499(1):121–123

    Article  CAS  Google Scholar 

  27. Serbati N, Badre W, Diakite B, Nadifi S (2014) NOD2/CARD15 gene influences disease behaviour but not IBD susceptibility in a Moroccan population. Turk J Gastroenterol Off J Turk Soc Gastroenterol 25(Suppl 1):122–128

    Google Scholar 

  28. Boukercha A, Mesbah-Amroun H, Bouzidi A, Saoula H, Nakkemouche M, Roy M, Hugot JP, Touil-Boukoffa C (2015) NOD2/CARD15 gene mutations in North Algerian patients with inflammatory bowel disease. World J Gastroenterol WJG 21(25):7786–7794

    Article  CAS  Google Scholar 

  29. Protopopov M, Poddubnyy D (2018) Radiographic progression in non-radiographic axial spondyloarthritis. Expert Rev Clin Immunol 14(6):525–533

    Article  CAS  Google Scholar 

  30. Dougados M, Demattei C, van den Berg R, Vo Hoang V, Thevenin F, Reijnierse M, Loeuille D, Feydy A, Claudepierre P, van der Heijde D (2016) Rate and predisposing factors for sacroiliac joint radiographic progression after a two-year follow-up period in recent-onset spondyloarthritis. Arthritis Rheumatol Hoboken NJ 68(8):1904–1913

    Article  CAS  Google Scholar 

  31. Bubová K, Forejtová Š, Zegzulková K, Gregová M, Hušáková M, Filková M, Hořínková J, Gatterová J, Tomčík M, Szczuková L, Pavelka K, Šenolt L (2019) Cross-sectional study of patients with axial spondyloarthritis fulfilling imaging arm of ASAS classification criteria: baseline clinical characteristics and subset differences in a single-centre cohort. BMJ Open 9(4):e024713

    Article  Google Scholar 

  32. Agafonova E, Dubinina T, Rumiantceva D, Demina A, Smirnov A, Erdes S (2019) Coxitis in early axial spondyloarthritis. Mod Rheumatol J 13:41–47

    Article  Google Scholar 

  33. Claudepierre P, Gueguen A, Ladjouze A, Hajjaj-Hassouni N, Sellami S, Amor B et al (1995) Predictive factors of severity of spondyloarthropathy in North Africa. Br J Rheumatol 34(12):1139–1145

    Article  CAS  Google Scholar 

  34. El Mansouri L, Bahiri R, Abourazzak FE, Abouqal R, Hajjaj-Hassouni N (2009) Two distinct patterns of ankylosing spondylitis in Moroccan patients. Rheumatol Int 29(12):1423–1429

    Article  Google Scholar 

  35. Akasbi N, Siar N, Zoukal S, Kohen KE, Harzy T (2019) Comparison of non-radiographic axial spondyloarthritis and ankylosing spondylitis from a single rheumatology hospital in Morocco. Curr Rheumatol Rev. 15. https://doi.org/10.2174/1573397115666190222195923

  36. Garrett S, Jenkinson T, Kennedy LG, Whitelock H, Gaisford P, Calin A (1994) A new approach to defining disease status in ankylosing spondylitis: the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol 21(12):2286–2291

    CAS  PubMed  Google Scholar 

  37. van der Heijde D, Lie E, Kvien TK, Sieper J, Van den Bosch F, Listing J et al (2009) ASDAS, a highly discriminatory ASAS-endorsed disease activity score in patients with ankylosing spondylitis. Ann Rheum Dis 68(12):1811–1818

    Article  Google Scholar 

  38. Taurog JD, Chhabra A, Colbert RA (2016) Ankylosing spondylitis and axial spondyloarthritis. N Engl J Med 374(26):2563–2574

    Article  Google Scholar 

  39. Calin A, Garrett S, Whitelock H, Kennedy LG, O’Hea J, Mallorie P et al (1994) A new approach to defining functional ability in ankylosing spondylitis: the development of the Bath Ankylosing Spondylitis Functional Index. J Rheumatol 21(12):2281–2285

    CAS  PubMed  Google Scholar 

  40. Chimenti MS, Conigliaro P, Navarini L, Martina FM, Peluso G, Birra D et al (2020) Demographic and clinical differences between ankylosing spondylitis and non-radiographic axial spondyloarthritis: results from a multicentre retrospective study in the Lazio region of Italy. Clin Exp Rheumatol 38(1):88–93

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to gratefully acknowledge the help provided by Dr Rabie Razgallah, Statistician, Department of Community Medicine, Ibn El Jazzar Medical Faculty of Sousse, Tunisia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yosra Gzam.

Ethics declarations

Disclosures

None.

Ethics approval

This study was approved by the institutional ethics committee.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ben Abdelghani, K., Gzam, Y., Fazaa, A. et al. Non-radiographic axial spondyloarthritis in Tunisia: main characteristics and detailed comparison with ankylosing spondylitis. Clin Rheumatol 40, 1361–1367 (2021). https://doi.org/10.1007/s10067-020-05415-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10067-020-05415-7

Keywords

Navigation