Best Practice & Research Clinical Rheumatology
Volume 22, Issue 4 , Pages 709-723 , August 2008

Ankylosing spondylitis and reactive arthritis in the developing world

  • Najia Hajjaj-Hassouni, MD (Professor of Rheumatology, Head of Department)

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +212 37 77 04 21; Fax: +212 37 77 37 01.

References 

  1. Nash P, Mease PJ, Braun J, et al. Seronegative spondyloarthropathies: to lump or split?. Annals of the Rheumatic Diseases. 2005;64(suppl 2):9–13
  2. Brown MA. Breakthroughs in genetic studies of ankylosing spondylitis. Rheumatology. 2008;47:132–137
  3. 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. Rheumatology International. 2003;23:61–66
  4. Akkoc N, Khan MA. Epidemiology of ankylosing spondylitis and related spondyloarthropathies. In:  Weisman MH,  Reveille JD,  van der Heijde D editor. Ankylosing spondylitis and the spondyloarthropathies. London: Mosby; 2005;p. 117–131
  5. Braun J, Sieper J. Ankylosing spondylitis. Lancet 2007; 369: 1379–90.
  6. Reveille JD, Ball EJ. Khan MA.HLA-B27 and genetic predisposing factors in spondylarthropathies. Current Opinion in Rheumatology. 2001;13:265–272
  7. Brown MA, Kennedy LG, MacGregor AJ, et al. Susceptibility to AS in twins: the role of genes, HLA, and the environment. Arthritis and Rheumatism. 1997;40:1823–1828
  8. Rowland-Jones S, Colbert RA, Dong T, et al. Distinct recognition of closely-related HIV-1 and HIV-2 cytotoxic T-cell epitopes presented by HLA-B*2703 and B*2705. AIDS. 1998;12:1391–1393
  9. López-Larrea C, Gonzalez-Roces S, Peña M, et al. Characterization of B27 haplotypes by oligotyping and genomic sequencing in the Mexican Mestizo population with ankylosing spondylitis: juvenile and adult onset. Human Immunology. 1995;43:174–180
  10. Vargas-Alarcón G, Londoño JD, Hernández-Pacheco G, et al. Effect of HLA-B and HLA-DR genes on susceptibility to and severity of spondyloarthropathies in Mexican patients. Annals of the Rheumatic Diseases. 2002;61:714–717
  11. Martínez B, Caraballo L, Hernández M, et al. HLA-B27 subtypes in patients with ankylosing spondylitis (As) in Colombia. Revista de investigación clínica; organo del Hospital de Enfermedades de la Nutrición. 1999;51:221–226
  12. Conde RA, Sampaio-Barros PD, Donadi EA, et al. Frequency of the HLA-B27 alleles in Brazilian patients with AS. The Journal of Rheumatology. 2003;30:2512
  13. Cipriani A, Rivera S, Hassanhi M, et al. HLA-B27 subtypes determination in patients with ankylosing spondylitis from Zulia, Venezuela. Human Immunology. 2003;64:745–749
  14. Sampaio-Barros PD, Conde RA, Donadi EA, et al. Frequency of HLA-B27 and its alleles in patients with Reiter syndrome: comparison with the frequency in other spondyloarthropathies and a healthy control population. Rheumatology International. 2008;28:483–486
  15. Bonfiglioli R, Conde RA, Sampaio-Barros PD, et al. Frequency of HLA-B27 alleles in Brazilian patients with psoriatic arthritis. Clinical Rheumatology. 2007 Nov 3;[Epub ahead of print]
  16. Ma HJ, Hu FP. Diversity of human leukocyte antigen-B27 alleles in Han population of Hunan province, southern China. Tissue Antigens. 2006;68:163–166
  17. Hou TY, Chen HC, Chen CH, et al. Usefulness of human leucocyte antigen-B27 subtypes in predicting ankylosing spondylitis: Taiwan experience. Internal Medicine Journal. 2007;37:749–752
  18. Shankarkumar U, Ghosh K, Mohanty D. HLA-B27 polymorphism in Western India. Tissue Antigens. 2002;60:98–101
  19. Madhavan R, Parthiban M, Rajendran CP, et al. HLA class I and class II association with ankylosing spondylitis in a southern Indian population. Annals of the New York Academy of Sciences. 2002;958:403–407
  20. Askari A, Al-Bdour MD, Saadeh A, Sawalha AH. Ankylosing spondylitis in north Jordan: descriptive and analytical study. Annals of the Rheumatic Diseases. 2000;59:571–573
  21. Al Attia HM, Sherif AM, Hossain MM, Ahmed YH. The demographic and clinical spectrum of Arab versus Asian patients with ankylosing spondylitis in the UAE. Rheumatology International. 1998;17:193–196
  22. Oguz FS, Ocal L, Diler AS, et al. HLA B-27 subtypes in Turkish patients with spondyloarthropathy and healthy controls. Disease Markers. 2004;20:309–312
  23. Hajjaj-Hassouni N, Maetzel A, Dougados M, Amor B. Comparison of patients evaluated for spondylarthropathy in France and Morocco. Revue du Rhumatisme. 1993;6:420–425
  24. Claudepierre P, Gueguen A, Hajjaj-Hassouni N, et al. Predictive factors of severity of spondyloarthropathy in North Africa. British Journal of Rheumatology. 1995;34:1139–1145
  25. Amroun H, Djoudi H, Busson M, et al. Early-onset ankylosing spondylitis is associated with a functional MICA polymorphism. Human Immunology. 2005;10:1057–1061
  26. Mijiyawa M, Oniankitan O, Khan MA. Spondyloarthropathies in sub-Saharan Africa. Current Opinion in Rheumatology. 2000;12:281–286
  27. Mbayo K, Mbuyi-Muamba JM, Lurhuma AZ, et al. Low frequency of HLA-B27 and scarcity of ankylosing spondylitis in a Zairean Bantu population. Clinical Rheumatology. 1998;17:309–310
  28. Adebajo A, Davis P. Rheumatic diseases in African blacks. Seminars in Arthritis and Rheumatism. 1994;24:139–153
  29. Smith JA. Pathogenesis of ankylosing spondylitis. Best Practice and Research Clinical Rheumatology. 2006;3:571–591
  30. Cauli A, Dessole G, Fiorillo MT, et al. Increased level of HLA-B27 expression in ankylosing spondylitis patients compared with healthy HLA-B27-positive subjects: a possible further susceptibility factor for the development of disease. Rheumatology (Oxford, England). 2002;41:1375–1379
  31. Olivieri I, Ciancio G, Padula A, et al. The HLA-B*2709 subtype confers susceptibility to spondyloarthropathy. Arthritis and Rheumatism. 2003;46:553–554
  32. Cauli A, Dessole G, Cappai L, et al. The lack of association between HLA-B*2709 and ankylosing spondylitis is not due to a defective cellular expression of the B*2709 molecules. Arthritis and Rheumatism. 2005;52:S394
  33. Nasution AR, Mardjuadi A, Kunmartini S, et al. HLA-B27 subtypes positively and negatively associated with spondyloarthropathy. The Journal of Rheumatology. 1997;24:1111–1114
  34. Ramos M, Paradela A, Vazquez M, et al. Differential association of HLA-B*2705 and B*2709 to ankylosing spondylitis correlates with limited peptide subsets but not with altered cell surface stability. The Journal of Biological Chemistry. 2002;277:28749–28756
  35. Dangoria NS, DeLay ML, Kingsbury DJ, et al. HLA-B27 misfolding is associated with aberrant intermolecular disulfide bond formation (dimerization) in the endoplasmic reticulum. The Journal of Biological Chemistry. 2002;277:23459–23468
  36. Brown MA, Jepson A, Young A, et al. Ankylosing spondylitis in West Africans, evidence for a non-HLA-B27 protective effect. Annals of the Rheumatic Diseases. 1997;56:68–70
  37. Hammer RE, Maika SD, Richardson JA, et al. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human β2m: an animal model of HLA-B27 associated disorder. Cell. 1990;63:1099–1112
  38. Taurog JD, Richardson JA, Croft JT, et al. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. The Journal of Experimental Medicine. 1994;180:2359–2364
  39. Onderdonk AB, Richardson JA, Hammer RE, Taurog JD. Correlation of cecal microflora of HLA-B27 transgenic rats with inflammatory bowel disease. Infection and Immunity. 1998;66:6022–6023
  40. Turner MJ, Delay ML, Bai S, et al. HLA-B27 up-regulation causes accumulation of misfolded heavy chains and correlates with the magnitude of the unfolded protein response in transgenic rats: implications for the pathogenesis of spondylarthritis-like disease. Arthritis and Rheumatism. 2007;1:215–223
  41. Sims AM, Wordsworth BP, Brown MA. Genetic susceptibility to ankylosing spondylitis. Current Molecular Medicine. 2004;4:13–20
  42. Wei JC, Tsai WC, Lin HS, et al. HLA-B60 and B61 are strongly associated with ankylosing spondylitis in HLA-B27-negative Taiwan Chinese patients. Rheumatology. 2004;43:839–842
  43. Lopez-Larrea C, Mijiyawa M, Gonzalez S, et al. Association of ankylosing spondylitis with HLA-B* 1403 in a West African population. Arthritis and Rheumatism. 2002;46:2968–2971
  44. Maksymowych WP, Gorodezky C, Olivo A, et al. HLA-DRB1*08 influences the development of disease in Mexican Mestizo with spondyloarthropathy. The Journal of Rheumatology. 1997 May;(5):904–907
  45. Monowarul Islam SM, Numaga J, Fujino Y, et al. HLA-DR8 and acute anterior uveitis in ankylosing spondylitis. Arthritis and Rheumatism. 1995;38:547–550
  46. Sims AM, Barnardo M, Herzberg I, et al. Non-B27 MHC associations of ankylosing spondylitis. Genes and Immunity. 2007;8:115–123
  47. Wellcome Trust Case Control Consortium & The Australo-Anglo-American Spondylitis Consortium (TASC) Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nature Genetics. 2007;39:1329–1337
  48. Kanaseki T, Blanchard N, Hammer GE, et al. ERAAP synergizes with MHC class I molecules to make the final cut in the antigenic peptide precursors in the endoplasmic reticulum. Immunity. 2006;25:795–806
  49. Sims AM, Timms AE, Bruges-Armas J, et al. Prospective meta-analysis of IL-1 gene complex polymorphisms confirms associations with ankylosing spondylitis. Published Online First Annals of the Rheumatic Diseases. 6 December 2007;
  50. Chou CT, Timms AE, Wei JC, et al. Replication of association of IL1 gene complex members with ankylosing spondylitis in Taiwanese Chinese. Annals of the Rheumatic Diseases. 2006;65:1106–1109
  51. Howe HS, Zhao L, Song YW, et al. Seronegative spondyloarthropathy studies from the Asia Pacific region. Annals of the Academy of Medicine, Singapore. 2007;36:135–141
  52. Lau CS, Burgos-Vargas R, Louthrenoo W, et al. Features of spondyloarthritis around the world. Rheumatic Diseases Clinics of North America. 1998;24:753–770
  53. Claudepierre P, Gueguen A, Hajjaj-Hassouni N, et al. Features associated with juvenile onset of spondylarthropathies in North Africa. Revue du rhumatisme (English ed.). 1996;63:87–91
  54. Stein M, Davis P. HIV and arthritis-causal or casual acquaintances?. The Journal of Rheumatology. 1989;16(10):1287–1290
  55. Gensler LS, Ward MM, Reveille JD, et al. Clinical, radiographic and functional differences between juvenile-onset and adult–onset ankylosing spondylitis: results from the PSOAS cohort. Annals of the Rheumatic Diseases. Feb 2008;67:233–237
  56. Guillemin F, Briançon S, Pourel J, Gaucher A. Long term disability and prolonged sick leaves as outcome measurements in Ankylosing Spondylitis. Possible predictive factors. Arthritis and Rheumatism. 1990;33:1001–1006
  57. Hamersma J, Cardon LR, Bradbury L, et al. Is disease severity in ankylosing spondylitis genetically determined?. Arthritis and Rheumatism. 2001;44:1396–1400
  58. Chopra A, Patil J, Billempelly V, et al. Prevalence of rheumatic diseases in a rural population in western India: a WHO-ILAR COPCORD Study. The Journal of the Association of Physicians India. 2001;49:240–246
  59. Chopra A, Raghunath D, Singh A. Spectrum of seronegative spondarthritides (SSA) with special reference to HLA profiles. The Journal of the Association of Physicians India. 1990;38:351–355
  60. Deesomchok U, Tumrasvin T. Clinical comparison of patients with ankylosing spondylitis, Reiter's syndrome and psoriatic arthritis. Journal of the Medicine Association of Thailand. 1993;76:61–70
  61. Pacheco-Tena C, Burgos-Vargas R, Vázquez-Mellado J, et al. A proposal for the classification of patients for clinical and experimental studies on reactive arthritis. The Journal of Rheumatology. 1999;26:1338–1346
  62. Martínez A, Pacheco-Tena C, Vázquez-Mellado J, Burgos-Vargas R. Relationship between disease activity and infection in patients with spondyloarthropathies. Annals of the Rheumatic Diseases. 2004;63:1338–1340
  63. Dominguez-López ML, Burgos-Vargas R, Galicia-Serrano H, et al. IgG antibodies to enterobacteria 60 kDa heat shock proteins in the sera of HLA-B27 positive ankylosing spondylitis patients. Scandinavian Journal of Rheumatology. 2002;31:260–265
  64. Madhavan R, Porkodi R, Rajendran CP, et al. IgM, IgG, and IgA response to enterobacteria in patients with ankylosing spondylitis in southern India. Annals of the New York Academy of Sciences. 2002;958:408–411
  65. Cuchacovich R, Japa S, Huang WQ, et al. Detection of bacterial DNA in Latin American patients with reactive arthritis by polymerase chain reaction and sequencing analysis. The Journal of Rheumatology. 2002;29:1426–1429
  66. Chou CT, Tsai CY, Huo AP. Failure to identify salmonella bacteria DNA by polymerase chain reaction in peripheral blood and synovial fluid cells in Chinese patients with rheumatoid arthritis and ankylosing spondylitis. Journal of Clinical Rheumatology: Practical Reports on Rheumatic and Musculoskeletal Diseases. 2004;10:285–286
  67. Prakash S, Mehra NK, Bhargava S, Malaviya AN. Reiter's disease in northern India. A clinical and immunogenetic study. Rheumatology International. 1983;3:101–104
  68. Vargas-Alarcón G, Casasola-Vargas J, Rodríguez-Pérez JM, et al. Tumor necrosis factor-alpha promoter polymorphisms in Mexican patients with spondyloarthritis. Human Immunology. 2006;67:826–832
  69. Njobvu P, McGill P, Kerr H, et al. Spondyloarthropathy and human immunodeficiency virus infection in Zambia. The Journal of Rheumatology. 1998;25:1553–1559
  70. Amor B, Santos RS, Nahal R, et al. Predictive factors for the longterm outcome of spondyloarthropathies. The Journal of Rheumatology. 1994;21:1883–1887
  71. Dougados M, van der Linden S, Juhlin R, et al. The European Spondylarthropathy Study Group preliminary criteria for the classification of spondylarthropathy. Arthritis and Rheumatism. 1991;34:1218–1227
  72. Rudwaleit M, Khan MA, Sieper J. The challenge of diagnosis and classification in early ankylosing spondylitis: do we need new criteria?. Arthritis and Rheumatism. 2005;52:1000–1008
  73. Sieper J, Rudwaleit M. Early referral recommendations for ankylosing spondylitis (including pre-radiographic and radiographic forms) in primary care. Annals of the Rheumatic Diseases. 2005;64:659–663
  74. Zochling J, Baraliakos X, Hermann KG, Braun J. Magnetic resonance imaging in ankylosing spondylitis. Current Opinion in Rheumatology. 2007;4:346–352
  75. Braun J, Bollow M, Sieper J. Radiologic diagnosis and pathology of the spondyloarthropathies. Rheumatic Diseases Clinics of North America. 1998;24:697–735
  76. McGonagle D, Gibbon W, O'Connor P, et al. Characteristic magnetic resonance imaging entheseal changes of knee synovitis in spondylarthropathy. Arthritis and Rheumatism. 1998;41:694–700
  77. Balint PV, Kane D, Wilson H, et al. Ultrasonography of entheseal insertions in the lower limb in spondyloarthropathy. Annals of the Rheumatic Diseases. 2002;61:905–910
  78. Heuft-Dorenbosch L, Landewe R, Weijers R, et al. Combining information obtained from magnetic resonance imaging and conventional radiographs to detect sacroiliitis in patients with recent onset inflammatory back pain. Annals of the Rheumatic Diseases. 2006;65:804–808
  79. Braun J, Landewe R, Hermann KG, et al. Major reduction in spinal inflammation in patients with ankylosing spondylitis after treatment with infliximab: results of a multicenter, randomized, double-blind, placebo-controlled magnetic resonance imaging study. Arthritis and Rheumatism. 2006;54:1646–1652
  80. Baraliakos X, Listing J, Rudwaleit M, et al. Progression of radiographic damage in patients with ankylosing spondylitis- defining the central role of syndesmophytes. Annals of the Rheumatic Diseases. 2007 Jul;7:910–915
  81. Zochling J, van der Heijde D. R Burgos-Vargas et al. ASAS/EULAR recommendations for the management of ankylosing spondylitis. Annals of the Rheumatic Diseases. 2006;65:442–452
  82. Sidiropoulos PI, Hatemi G, Song IH, et al. Evidence-based recommendations for the management of ankylosing spondylitis: systematic literature search of the 3E Initiative in Rheumatology involving a broad panel of experts and practising rheumatologists. Rheumatology (Oxford). 2008 Mar;47(3):355–361
  83. Wanders A, van der Heijde D, Landewe´ R, et al. Nonsteroidal antiinflammatory drugs reduce radiographic progression in patients with ankylosing spondylitis. Arthritis and Rheumatism. 2005;52:1756–1765
  84. Haibel H, Brandt J, Rudwaleit M, et al. Treatment of active ankylosing spondylitis with pamidronate. Rheumatology (Oxford). 2003;42:1018–1020
  85. Baraliakos X, Listing J, Brandt J, et al. Radiographic progression in patients with ankylosing spondylitis after 4 yrs of treatment with the anti-TNF-alpha antibody infliximab. Rheumatology (Oxford). 2007;9:1450–1453
  86. Diarra D, Stolina M, Polzer K, et al. Dickkopf-1 is a master regulator of joint remodeling. Nature Medicine. 2007;2:156–163
  87. Zwerina J, Tuerk B, Redlich K, et al. Imbalance of local bone metabolism in inflammatory arthritis and its reversal upon tumor necrosis factor blockade: direct analysis of bone turnover in murine arthritis. Arthritis Research and Therapy. 2006;1:R22
  88. Lories RJ, Derese I, de Bari C, Luyten FP. Evidence for uncoupling of inflammation and joint remodeling in a mouse model of spondylarthritis. Arthritis and Rheumatism. 2007;2:489–497
  89. Brandt J, Khariouzov A, Listing J, et al. Successful short term treatment of patients with severe undifferentiated spondyloarthritis with the anti-tumor necrosis factor-alpha fusion receptor protein etanercept. The Journal of Rheumatology. 2004;31:531–538
  90. Brandt J, Haibel H, Reddig J, et al. Successful short term treatment of severe undifferentiated spondyloarthropathy with the anti-tumor necrosis factor-alpha monoclonal antibody infliximab. The Journal of Rheumatology. 2002;29:118–122
  91. Furst DE, Breedveld FC, Kalden JR, et al. Updated consensus statement on biological agents for the treatment of rheumatic diseases, 2007. Annals of the Rheumatic Diseases. Nov 2007;66:iii2–iii22
  92. Strangfeld A, Listing J. Infection and musculoskeletal conditions: Bacterial and opportunistic infections during anti-TNF therapy. Best Practice and Research Clinical Rheumatology. 2006;6:1181–1195
  93. Lambert RG, Salonen D, Rahman P, et al. Adalimumab significantly reduces both spinal and sacroiliac joint inflammation in patients with ankylosing spondylitis: a multicenter, randomized, double-blind, placebo-controlled study. Arthritis and Rheumatism. 2007;12:4005–4014
  94. Wailoo A, Bansback N, Chilcott J. Infliximab, etanercept and adalimumab for the treatment of ankylosing spondylitis: cost-effectiveness evidence and NICE guidance. Rheumatology (Oxford). 2008;2:119–120
  95. Song IH, Sieper J, Rudwaleit M. Diagnosing early ankylosing spondylitis. Current Rheumatology Reports. 2007;5:367–374
  96. Iorio R, Healy WL. Heterotopic ossification after hip and knee arthroplasty: risk factors, prevention, and treatment. The Journal of the American Academy of Orthopaedic Surgeons. 2002;6:409–416
  97. Ara RM, Packham JC, Haywood KL. The direct healthcare costs associated with ankylosing spondylitis patients attending a UK secondary care rheumatology unit. Rheumatology. 2008;47:68–71
  98. Rkain H, Allali F, Hajjaj-Hassouni N, et al. Socioeconomic impact of ankylosing spondylitis in Morocco. Clinical Rheumatology. 2007;12:2081–2088

PII: S1521-6942(08)00067-3

doi: 10.1016/j.berh.2008.05.005

Best Practice & Research Clinical Rheumatology
Volume 22, Issue 4 , Pages 709-723 , August 2008