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Clinical and Developmental Immunology
Volume 2013, Article ID 631408, 12 pages
http://dx.doi.org/10.1155/2013/631408
Review Article

Enteropathic Spondyloarthritis: From Diagnosis to Treatment

1Rheumatology Research Unit, University Federico II, 80131 Naples, Italy
2Department of Clinical and Experimental Medicine, University Federico II, 80131 Naples, Italy
3Regional Reference Center for Coagulation Disorders, University Federico II, 80131 Naples, Italy
4Complex Operating Unit of Gastroenterology, AORN “A.Cardarelli,” Via Sergio Pansini 5, 80131 Naples, Italy
5Gastroenterology Research Unit, University Federico II, 80131 Naples, Italy

Received 19 October 2012; Accepted 25 March 2013

Academic Editor: Chung Tei Chou

Copyright © 2013 Rosario Peluso et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Leirisalo-Repo, “Enteropathic arthritis, Whipple's disease, juvenile spondyloarthropathy, and uveitis,” Current Opinion in Rheumatology, vol. 6, no. 4, pp. 385–390, 1994. View at Google Scholar · View at Scopus
  2. A. Orlando, S. Renna, G. Perricone, and M. Cottone, “Gastrointestinal lesions associated with spondyloarthropathies,” World Journal of Gastroenterology, vol. 15, no. 20, pp. 2443–2448, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Smith, “Treatment of rheumatoid arthritis by colectomy,” Annals of Surgery, vol. 76, pp. 515–578, 1922. View at Publisher · View at Google Scholar
  4. J. A. Bargen, R. J. Jackman, and J. G. Kerr, “Complications and sequel of chronic ulcerative colitis,” Annals of Internal Medicine, vol. 3, pp. 335–352, 1929. View at Google Scholar
  5. P. S. Hench, “Acute and chronic arthritis,” in Nelson’s Loose Leaf of Surgery, G. H. Whipple, Ed., p. 104, Thomas Nelson Sons, New York, NY, USA, 1935. View at Google Scholar
  6. E. G. Bywaters and B. M. Ansell, “Arthritis associated with ulcerative colitis; a clinical and pathological study,” Annals of the Rheumatic Diseases, vol. 17, no. 2, pp. 169–183, 1958. View at Google Scholar · View at Scopus
  7. J. A. McBride, M. J. King, A. G. Baikie, G. P. Crean, and W. Sircus, “Ankylosing spondylitis and chronic inflammatory diseases of the intestines,” British Medical Journal, vol. 2, no. 5355, pp. 483–486, 1963. View at Google Scholar · View at Scopus
  8. V. L. Steinberg and G. Storey, “Ankylosing spondylitis and chronic inflammatory lesions of the intestines,” British Medical Journal, vol. 2, no. 5054, pp. 1157–1159, 1957. View at Publisher · View at Google Scholar
  9. J. S. Stewart and B. M. Ansell, “Ankylosing spondylitis associated with regional enteritis,” Gastroenterology, vol. 45, pp. 265–268, 1963. View at Google Scholar · View at Scopus
  10. B. S. Blumberg, J. J. Bunim, E. Calkins, C. L. Pirani, and N. J. Zvaifler, “Aranomenclature and classification of arthritis and rheumatism (tentative),” Arthritis and Rheumatism, vol. 7, pp. 93–97, 1964. View at Google Scholar · View at Scopus
  11. V. Wright and J. H. M. Moll, Seronegative Polyarthritis, North Holland Publishing Company, Amsterdam, The Netherlands, 1976.
  12. R. H. Puite and H. Tesluk, “Whipple's disease,” The American Journal of Medicine, vol. 19, no. 3, pp. 383–400, 1955. View at Google Scholar · View at Scopus
  13. J. J. Kelly III and B. B. Weisiger, “The arthritis of Whipple's disease,” Arthritis and Rheumatism, vol. 6, pp. 615–632, 1963. View at Google Scholar · View at Scopus
  14. J. Friis and A. Svejgaard, “Letter: Salmonella arthritis and HL-A27,” The Lancet, vol. 1, no. 7870, p. 1350, 1974. View at Google Scholar · View at Scopus
  15. K. Aho, P. Ahvonen, and A. Lassus, “Yersinia arthritis and related diseases,” in Infection and Immunology in the Rheumatic Diseases, D. C. P. Dumond, Ed., pp. 341–344, Oxford Blackwell, 1976. View at Google Scholar
  16. J. Braun and J. Sieper, “Building consensus on nomenclature and disease classification for ankylosing spondylitis: results and discussion of a questionnaire prepared for the International Workshop on New Treatment Strategies in Ankylosing Spondylitis, Berlin, Germany, 18-19 January 2002,” Annals of the Rheumatic Diseases, vol. 61, supplement 3, pp. iii61–iii67, 2002. View at Google Scholar · View at Scopus
  17. M. Dougados, S. van der Linden, R. Juhlin et al., “The European Spondylarthropathy Study Group preliminary criteria for the classification of spondylarthropathy,” Arthritis and Rheumatism, vol. 34, no. 10, pp. 1218–1227, 1991. View at Google Scholar · View at Scopus
  18. J. Cosnes, C. Gower-Rousseau, P. Seksik, and A. Cortot, “Epidemiology and natural history of inflammatory bowel diseases,” Gastroenterology, vol. 140, no. 6, pp. 1785–1794, 2011. View at Publisher · View at Google Scholar
  19. C. Salvarani and W. Fries, “Clinical features and epidemiology of spondyloarthritides associated with inflammatory bowel disease,” World Journal of Gastroenterology, vol. 15, no. 20, pp. 2449–2455, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Turkcapar, M. Toruner, I. Soykan et al., “The prevalence of extraintestinal manifestations and HLA association in patients with inflammatory bowel disease,” Rheumatology International, vol. 26, no. 7, pp. 663–668, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Scarpa, A. del Puente, A. D'Arienzo et al., “The arthritis of ulcerative colitis: clinical and genetic aspects,” Journal of Rheumatology, vol. 19, no. 3, pp. 373–377, 1992. View at Google Scholar · View at Scopus
  22. K. de Vlam, H. Mielants, C. Cuvelier, F. de Keyser, E. M. Veys, and M. de Vos, “Spondyloarthropathy is underestimated in inflammatory bowel disease: prevalence and HLA association,” Journal of Rheumatology, vol. 27, no. 12, pp. 2860–2865, 2000. View at Google Scholar · View at Scopus
  23. P. Wordsworth, “Arthritis and inflammatory bowel disease,” Current Rheumatology Reports, vol. 2, no. 2, pp. 87–88, 2000. View at Google Scholar · View at Scopus
  24. T. S. Rodríguez-Reyna, C. Martínez-Reyes, and J. K. Yamamoto-Furusho, “Rheumatic manifestations of inflammatory bowel disease,” World Journal of Gastroenterology, vol. 15, no. 44, pp. 5517–5524, 2009. View at Publisher · View at Google Scholar
  25. O. Palm, B. Moum, J. Jahnsen, and J. T. Gran, “The prevalence and incidence of peripheral arthritis in patients with inflammatory bowel disease, a prospective population-based study (the IBSEN study),” Rheumatology, vol. 40, no. 11, pp. 1256–1261, 2001. View at Google Scholar · View at Scopus
  26. T. R. Orchard, B. P. Wordsworth, and D. P. Jewell, “Peripheral arthropathies in inflammatory bowel disease: their articular distribution and natural history,” Gut, vol. 42, no. 3, pp. 387–391, 1998. View at Google Scholar · View at Scopus
  27. I. Yüksel, H. Ataseven, O. Başar et al., “Peripheral arthritis in the course of inflammatory bowel diseases,” Digestive Diseases and Sciences, vol. 56, no. 1, pp. 183–187, 2011. View at Publisher · View at Google Scholar
  28. S. R. Vavricka, L. Brun, P. Ballabeni et al., “Frequency and risk factors for extraintestinal manifestations in the swiss inflammatory bowel disease cohort,” American Journal of Gastroenterology, vol. 106, no. 1, pp. 110–119, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. F. T. Veloso, J. Carvalho, and F. Magro, “Immune-related systemic manifestations of inflammatory bowel disease: a prospective study of 792 patients,” Journal of Clinical Gastroenterology, vol. 23, no. 1, pp. 29–34, 1996. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Manguso, T. Staiano, C. Astarita et al., “Consecutive occurrence of rhinoconjunctivitis, seronegative spondyloarthritis and pyoderma gangrenosum in a patient with ulcerative colitis,” International Journal of Colorectal Disease, vol. 20, no. 1, pp. 79–80, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Manguso, M. Sanges, T. Staiano et al., “Cigarette smoking and appendectomy are risk factors for extraintestinal manifestations in ulcerative colitis,” American Journal of Gastroenterology, vol. 99, no. 2, pp. 327–334, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Cuvelier, C. Barbatis, H. Mielants, M. de Vos, H. Roels, and E. Veys, “Histopathology of intestinal inflammation related to reactive arthritis,” Gut, vol. 28, no. 4, pp. 394–401, 1987. View at Google Scholar · View at Scopus
  33. M. de Vos, C. Cuvelier, H. Mielants, E. Veys, F. Barbier, and A. Elewaut, “Ileocolonoscopy in seronegative spondylarthropathy,” Gastroenterology, vol. 96, no. 2, part 1, pp. 339–344, 1989. View at Google Scholar · View at Scopus
  34. H. Mielants, E. M. Veys, R. Joos, C. Cuvelier, and M. de Vos, “Repeat ileocolonoscopy in reactive arthritis,” Journal of Rheumatology, vol. 14, no. 3, pp. 456–458, 1987. View at Google Scholar · View at Scopus
  35. H. Mielants, E. M. Veys, C. Cuvelier, M. de Vos, and L. Botelberghe, “HLA-B27 related arthritis and bowel inflammation—part 2: ileocolonoscopy and bowel histology in patients with HLA-B27 related arthritis,” Journal of Rheumatology, vol. 12, no. 2, pp. 294–298, 1985. View at Google Scholar · View at Scopus
  36. R. Scarpa, F. Manguso, A. D'Arienzo et al., “Microscopic inflammatory changes in colon of patients with both active psoriasis and psoriatic arthritis without bowel symptoms,” Journal of Rheumatology, vol. 27, no. 5, pp. 1241–1246, 2000. View at Google Scholar · View at Scopus
  37. P. Jacques, D. Elewaut, and H. Mielants, “Interactions between gut inflammation and arthritis/spondylitis,” Current Opinion in Rheumatology, vol. 22, no. 4, pp. 368–374, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Jacques and D. Elewaut, “Joint expedition: linking gut inflammation to arthritis,” Mucosal Immunology, vol. 1, no. 5, pp. 364–371, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Schlosstein, P. I. Terasaki, R. Bluestone, and C. M. Pearson, “High association of an HL-A antigen, W27, with ankylosing spondylitis,” The New England Journal of Medicine, vol. 288, no. 14, pp. 704–706, 1973. View at Google Scholar · View at Scopus
  40. M. A. Brown, K. D. Pile, L. G. Kennedy et al., “HLA class I associations of ankylosing spondylitis in the white population in the United Kingdom,” Annals of the Rheumatic Diseases, vol. 55, no. 4, pp. 268–270, 1996. View at Google Scholar · View at Scopus
  41. E. G. Mallas, P. Mackintosh, P. Asquith, and W. T. Cooke, “Histocompatibility antigens in inflammatory bowel disease; their clinical significance and their association with arthropathy with special reference to HLA B27 (W27),” Gut, vol. 17, no. 11, pp. 906–910, 1976. View at Google Scholar · View at Scopus
  42. H. Peeters, B. Vander Cruyssen, H. Mielants et al., “Clinical and genetic factors associated with sacroiliitis in Crohn's disease,” Journal of Gastroenterology and Hepatology, vol. 23, no. 1, pp. 132–137, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. T. R. Orchard, S. Thiyagaraja, K. I. Welsh, B. P. Wordsworth, J. S. H. Gaston, and D. P. Jewell, “Clinical phenotype is related to HLA genotype in the peripheral arthropathies of inflammatory bowel disease,” Gastroenterology, vol. 118, no. 2, pp. 274–278, 2000. View at Google Scholar · View at Scopus
  44. W. Kuon and J. Sieper, “Identification of HLA-B27-restricted peptides in reactive arthritis and other spondyloarthropathies: computer algorithms and fluorescent activated cell sorting analysis as tools for hunting of HLA-B27-restricted chlamydial and autologous crossreactive peptides involved in reactive arthritis and ankylosing spondylitis,” Rheumatic Disease Clinics of North America, vol. 29, no. 3, pp. 595–611, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. A. K. H. Mertz, P. Wu, T. Sturniolo et al., “Multispecific CD4+ T cell response to a single 12-mer epitope of the immunodominant heat-shock protein 60 of Yersinia enterocolitica in Yersinia- triggered reactive arthritis: overlap with the B27-restricted CD8 epitope, functional properties, and epitope presentation by multiple DR alleles,” Journal of Immunology, vol. 164, no. 3, pp. 1529–1537, 2000. View at Google Scholar · View at Scopus
  46. A. Thiel, P. Wu, R. Lauster, J. Braun, A. Radbruch, and J. Sieper, “Analysis of the antigen-specific T cell response in reactive arthritis by flow cytometry,” Arthritis & Rheumatism, vol. 43, no. 12, pp. 2834–2842, 2000. View at Google Scholar
  47. R. H. Scofield, B. Kurien, T. Gross, W. L. Warren, and J. B. Harley, “HLA-B27 binding of peptide from its own sequence and similar peptides from bacteria: implications for spondyloarthropathies,” The Lancet, vol. 345, no. 8964, pp. 1542–1544, 1995. View at Google Scholar · View at Scopus
  48. M. Ramos, I. Alvarez, L. Sesma, A. Logean, D. Rognan, and J. A. de López Castro, “Molecular mimicry of an HLA-B27-derived ligand of arthritis-linked subtypes with chlamydial proteins,” Journal of Biological Chemistry, vol. 277, no. 40, pp. 37573–37581, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Frauendorf, H. von Goessel, E. May, and E. Märker-Hermann, “HLA-B27-restricted T cells from patients with ankylosing spondylitis recognize peptides from B*2705 that are similar to bacteria-derived peptides,” Clinical & Experimental Immunology, vol. 134, no. 2, pp. 351–359, 2003. View at Publisher · View at Google Scholar
  50. M. C. Fantini, F. Pallone, and G. Monteleone, “Common immunologic mechanisms in inflammatory bowel disease and spondylarthropathies,” World Journal of Gastroenterology, vol. 15, no. 20, pp. 2472–2478, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Baeten, F. de Keyser, H. Mielants, and E. M. Veys, “Immune linkages between inflammatory bowel disease and spondyloarthropathies,” Current Opinion in Rheumatology, vol. 14, no. 4, pp. 342–347, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Uchanska-Ziegler and A. Ziegler, “Ankylosing spondylitis: a β2m-deposition disease?” Trends in Immunology, vol. 24, no. 2, pp. 73–76, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Mielants, E. M. Veys, S. Goemaere, K. Goethals, C. Cuvelier, and M. de Vos, “Gut inflammation in the spondyloarthropathies: clinical, radiologic, biologic and genetic features in relation to the type of histology. A prospective study,” Journal of Rheumatology, vol. 18, no. 10, pp. 1542–1551, 1991. View at Google Scholar · View at Scopus
  54. R. E. Hammer, S. D. Maika, J. A. Richardson, J. P. Tang, and J. D. Taurog, “Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human β2m: an animal model of HLA-B27-associated human disorders,” Cell, vol. 63, no. 5, pp. 1099–1112, 1990. View at Publisher · View at Google Scholar · View at Scopus
  55. J. D. Taurog, J. A. Richardson, J. T. Croft et al., “The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats,” Journal of Experimental Medicine, vol. 180, no. 6, pp. 2359–2364, 1994. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Hammer, H. Zeidler, S. Klimsa, and J. Heesemann, “Yersinia enterocolitica in the synovial membrane of patients with Yersinia-induced arthritis,” Arthritis and Rheumatism, vol. 33, no. 12, pp. 1795–1800, 1990. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Granfors, S. Jalkanen, R. von Essen et al., “Yersinia antigens in synovial-fluid cells from patients with reactive arthritis,” The New England Journal of Medicine, vol. 320, no. 4, pp. 216–221, 1989. View at Google Scholar · View at Scopus
  58. K. Granfors, S. Jalkanen, P. Toivanen, J. Koski, and A. A. Lindberg, “Bacterial lipopolysaccharide in synovial fluid cells in Shigella triggered reactive arthritis,” Journal of Rheumatology, vol. 19, no. 3, p. 500, 1992. View at Google Scholar · View at Scopus
  59. K. Granfors, S. Jalkanen, A. A. Lindberg et al., “Salmonella lipopolysaccharide in synovial cells from patients with reactive arthritis,” The Lancet, vol. 335, no. 8691, pp. 685–688, 1990. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Kirveskari, S. Jalkanen, O. Mäki-Ikola, and K. Granfors, “Increased synovial endothelium binding and transendothelial migration of mononuclear cells during Salmonella infection,” Arthritis & Rheumatism, vol. 41, no. 6, pp. 1054–1063, 1998. View at Google Scholar
  61. M. Wuorela, S. Tohka, K. Granfors, and S. Jalkanen, “Monocytes that have ingested Yersinia enterocolitica serotype O:3 acquire enhanced capacity to bind to nonstimulated vascular endothelial cells via P-selectin,” Infection and Immunity, vol. 67, no. 2, pp. 726–732, 1999. View at Google Scholar · View at Scopus
  62. M. Wuorela, S. Jalkanen, J. Kirveskari, P. Laitio, and K. Granfors, “Yersinia enterocolitica serotype O:3 alters the expression of serologic HLA-B27 epitopes on human monocytes,” Infection and Immunity, vol. 65, no. 6, pp. 2060–2066, 1997. View at Google Scholar · View at Scopus
  63. A. Ebringer, T. Rashid, H. Tiwana, and C. Wilson, “A possible link between Crohn's disease and ankylosing spondylitis via Klebsiella infections,” Clinical Rheumatology, vol. 26, no. 3, pp. 289–297, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. R. H. Duerr, K. D. Taylor, S. R. Brant et al., “A genome-wide association study identifies IL23R as an inflammatory bowel disease gene,” Science, vol. 314, no. 5804, pp. 1461–1463, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. L. van Praet, F. van den Bosch, H. Mielants, and D. Elewaut, “Mucosal inflammation in spondylarthritides: past, present, and future,” Current Rheumatology Reports, vol. 13, no. 5, pp. 409–415, 2011. View at Publisher · View at Google Scholar
  66. D. Laukens, H. Peeters, D. Marichal et al., “CARD15 gene polymorphisms in patients with spondyloarthropathies identify a specific phenotype previously related to Crohn's disease,” Annals of the Rheumatic Diseases, vol. 64, no. 6, pp. 930–935, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Miceli-Richard, H. Zouali, S. Lesage et al., “CARD15/NOD2 analyses in spondylarthropathy,” Arthritis and Rheumatism, vol. 46, no. 5, pp. 1405–1406, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. M. de Vos, P. Hindryckx, and D. Laukens, “Novel development in extraintestinal manifestations and spondylarthropathy,” Best Practice and Research: Clinical Gastroenterology, vol. 25, no. 1, pp. S19–S26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. L. van Praet, P. Jacques, F. van den Bosch, and D. Elewaut, “The transition of acute to chronic bowel inflammation in spondyloarthritis,” Nature Reviews Rheumatology, vol. 8, no. 5, pp. 288–295, 2012. View at Publisher · View at Google Scholar
  70. W. Holden, T. Orchard, and P. Wordsworth, “Enteropathic arthritis,” Rheumatic Disease Clinics of North America, vol. 29, no. 3, pp. 513–530, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. E. M. Gravallese and F. G. Kantrowitz, “Arthritic manifestations of inflammatory bowel disease,” American Journal of Gastroenterology, vol. 83, no. 7, pp. 703–709, 1988. View at Google Scholar · View at Scopus
  72. S. Smale, R. S. Natt, T. R. Orchard, A. S. Russell, and I. Bjarnason, “Inflammatory bowel disease and spondylarthropathy,” Arthritis & Rheumatism, vol. 44, no. 12, pp. 2728–2736, 2001. View at Google Scholar
  73. K. S. Rothfuss, E. F. Stange, and K. R. Herrlinger, “Extraintestinal manifestations and complications in inflammatory bowel diseases,” World Journal of Gastroenterology, vol. 12, no. 30, pp. 4819–4831, 2006. View at Google Scholar · View at Scopus
  74. A. Calin and D. Robertson, “Spondylodiscitis and pseudarthrosis in a patient with enteropathic spondyloarthropathy,” Annals of the Rheumatic Diseases, vol. 50, no. 2, pp. 117–119, 1991. View at Google Scholar · View at Scopus
  75. O. Andersson, “Röntgenbilden vid spondylarthritis ankylopoetica,” Nordisk Medicinsk Tidskrift, vol. 14, pp. 2000–2002, 1937. View at Google Scholar
  76. E. Zöld, Z. Barta, and M. Zeher, “Spondylodiscitis representing as the very first sign of Crohn's disease,” Inflammatory Bowel Diseases, vol. 13, no. 8, p. 1058, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. R. G. W. Lambert, S. J. Pedersen, W. P. Maksymowych, P. Chiowchanwisawakit, and M. Østergaard, “Active inflammatory lesions detected by magnetic resonance imaging in the spine of patients with spondyloarthritis—definitions, assessment system, and reference image set,” Journal of Rheumatology, vol. 36, supplement 84, pp. 3–17, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Østergaard, W. P. Maksymowych, S. J. Pedersen, P. Chiowchanwisawakit, and R. G. W. Lambert, “Structural lesions detected by magnetic resonance imaging in the spine of patients with spondyloarthritis—definitions, assessment system, and reference image set,” Journal of Rheumatology, vol. 36, supplement 84, pp. 18–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. E. Soscia, R. Scarpa, M. A. Cimmino et al., “Magnetic resonance imaging of nail unit in psoriatic arthritis,” Journal of Rheumatology. Supplement, vol. 36, no. 83, pp. 42–45, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. Y. Kabasakal, S. L. Garrett, and A. Calin, “The epidemiology of spondylodiscitis in ankylosing spondylitis. A controlled study,” British Journal of Rheumatology, vol. 35, no. 7, pp. 660–663, 1996. View at Google Scholar · View at Scopus
  81. R. Scarpa, “Discovertebral erosions and destruction in psoriatic arthritis,” Journal of Rheumatology, vol. 27, no. 4, pp. 975–978, 2000. View at Google Scholar · View at Scopus
  82. R. Peluso, M. N. Di Minno, V. Bruner et al., “Discovertebral erosions in patients with enteropathic spondyloarthritis,” The Journal of Rheumatology, vol. 39, no. 12, pp. 2332–2340, 2012. View at Publisher · View at Google Scholar
  83. E. Toussirot and D. Wendling, “Crohn's disease associated with seropositive rheumatoid arthritis,” Clinical and Experimental Rheumatology, vol. 15, no. 3, pp. 307–311, 1997. View at Google Scholar · View at Scopus
  84. E. Y. Rhew, R. Ramsey-Goldman, and A. L. Buchman, “Sjogren's syndrome in association with Crohn's disease,” Journal of Clinical Gastroenterology, vol. 37, no. 4, pp. 312–314, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Aoyagi, H. Akashi, T. Kawara et al., “Aortic root replacement for Takayasu arteritis associated with ulcerative colitis and ankylosing spondylitis: report of a case,” Japanese Circulation Journal, vol. 62, no. 1, pp. 64–68, 1998. View at Publisher · View at Google Scholar · View at Scopus
  86. M. O. E. Hilário, M. T. R. A. Terreri, G. Prismich et al., “Association of anky-losing spondylitis, Crohn's disease and Takayasu's arteritis in a child,” Clinical and Experimental Rheumatology, vol. 16, no. 1, pp. 92–94, 1998. View at Google Scholar · View at Scopus
  87. O. Palm, B. Moum, J. Jahnsen, and J. T. Gran, “Fibromyalgia and chronic widespread pain in patients with inflammatory bowel disease: a cross sectional population survey,” Journal of Rheumatology, vol. 28, no. 3, pp. 590–594, 2001. View at Google Scholar · View at Scopus
  88. C. N. Bernstein, J. F. Blanchard, P. Rawsthorne, and N. Yu, “The prevalence of extraintestinal diseases in inflammatory bowel disease: a population-based study,” American Journal of Gastroenterology, vol. 96, no. 4, pp. 1116–1122, 2001. View at Publisher · View at Google Scholar · View at Scopus
  89. I. Yüksel, O. Başar, H. Ataseven et al., “Mucocutaneous manifestations in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 15, no. 4, pp. 546–550, 2009. View at Publisher · View at Google Scholar
  90. R. Peluso, G. A. Lupoli, A. Del Puente et al., “Prevalence of thyroid autoimmunity in patients with spondyloarthropathies,” Journal of Rheumatology, vol. 38, no. 7, pp. 1371–1377, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. J. K. Triantafillidis, C. A. Manoussakis, C. Tsafaras, and A. Koutsorizof, “Coexistence of thyreotoxicosis and exacerbation of ulcerative colitis,” American Journal of Gastroenterology, vol. 85, no. 7, pp. 908–910, 1990. View at Google Scholar · View at Scopus
  92. G. Järnerot, A. K. Azad Khan, and S. C. Truelove, “The thyroid in ulcerative colitis and Crohn's disease. II. Thyroid enlargement and hyperthyroidism in ulcerative colitis,” Acta Medica Scandinavica, vol. 197, no. 1-2, pp. 83–87, 1975. View at Google Scholar · View at Scopus
  93. C. Ha, S. Magowan, N. A. Accortt, J. Chen, and C. D. Stone, “Risk of arterial thrombotic events in inflammatory bowel disease,” American Journal of Gastroenterology, vol. 104, no. 6, pp. 1445–1451, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. A. J. Yarur, A. R. Deshpande, D. M. Pechman, L. Tamariz, M. T. Abreu, and D. A. Sussman, “Inflammatory bowel disease is associated with an increased incidence of cardiovascular events,” The American Journal of Gastroenterology, vol. 106, no. 4, pp. 741–747, 2011. View at Publisher · View at Google Scholar
  95. A. Papa, A. Santoliquido, S. Danese et al., “Increased carotid intima-media thickness in patients with inflammatory bowel disease,” Alimentary Pharmacology and Therapeutics, vol. 22, no. 9, pp. 839–846, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Efremidis, E. Prappa, and F. Kardaras, “Acute myocardial infarction in a young patient during an exacerbation of ulcerative colitis,” International Journal of Cardiology, vol. 70, no. 2, pp. 211–212, 1999. View at Publisher · View at Google Scholar · View at Scopus
  97. B. Mutlu, C. M. H. Ermeydan, F. Enç et al., “Acute myocardial infarction in a young woman with severe ulcerative colitis,” International Journal of Cardiology, vol. 83, no. 2, pp. 183–185, 2002. View at Publisher · View at Google Scholar · View at Scopus
  98. R. Calderón, M. R. Cruz-Correa, and E. A. Torres, “Cerebral thrombosis associated with active Crohn's disease,” Puerto Rico Health Sciences Journal, vol. 17, no. 3, pp. 293–295, 1998. View at Google Scholar · View at Scopus
  99. E. Cognat, I. Crassard, C. Denier, K. Vahedi, and M. G. Bousser, “Cerebral venous thrombosis in inflammatory bowel diseases: eight cases and literature review,” International Journal of Stroke, vol. 6, no. 6, pp. 487–492, 2011. View at Publisher · View at Google Scholar
  100. M. Aloi, L. Tromba, G. Di Nardo et al., “Premature subclinical atherosclerosis in pediatric inflammatory bowel disease,” The Journal of Pediatrics, vol. 161, no. 4, pp. 589–594, 2012. View at Publisher · View at Google Scholar
  101. E. Yorulmaz, G. Adali, H. Yorulmaz, C. Ulasoglu, G. Tasan, and I. Tuncer, “Metabolic syndrome frequency in inflammatory bowel diseases,” Saudi Journal of Gastroenterology, vol. 17, no. 6, pp. 376–382, 2011. View at Publisher · View at Google Scholar
  102. A. Oussalah, J. L. Guéant, and L. Peyrin-Biroulet, “Meta-analysis: hyperhomocysteinaemia in inflammatory bowel diseases,” Alimentary Pharmacology & Therapeutics, vol. 34, no. 10, pp. 1173–1184, 2011. View at Publisher · View at Google Scholar
  103. A. Canero, D. Parmeggiani, N. Avenia et al., “Thromboembolic tendency (TE) in IBD, (Inflammatory bowel disease) patients,” Annali Italiani di Chirurgia, vol. 83, no. 4, pp. 313–317, 2012. View at Google Scholar
  104. X. Roblin, E. Germain, J. M. Phelip et al., “Factors associated with hyperhomocysteinemia in inflammatory bowel disease: prospective study in 81 patients,” Revue de Medecine Interne, vol. 27, no. 2, pp. 106–110, 2006. View at Publisher · View at Google Scholar · View at Scopus
  105. C. E. McGowan, P. Jones, M. D. Long, and A. S. Barritt IV, “Changing shape of disease: nonalcoholic fatty liver disease in Crohn's disease-a case series and review of the literature,” Inflammatory Bowel Diseases, vol. 18, no. 1, pp. 49–54, 2012. View at Publisher · View at Google Scholar
  106. M. N. Di Minno, A. Tufano, A. Rusolillo, G. Di Minno, and G. Tarantino, “High prevalence of nonalcoholic fatty liver in patients with idiopathic venous thromboembolism,” World Journal of Gastroenterology, vol. 16, no. 48, pp. 6119–6122, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. M. N. Di Minno, S. Iervolino, R. Peluso et al., “Hepatic steatosis and disease activity in subjects with psoriatic arthritis receiving tumor necrosis factor-α blockers,” The Journal of Rheumatology, vol. 39, no. 5, pp. 1042–1046, 2012. View at Publisher · View at Google Scholar
  108. J. Haapamäki, R. P. Roine, U. Turunen, M. A. Färkkilä, and P. E. T. Arkkila, “Increased risk for coronary heart disease, asthma, and connective tissue diseases in inflammatory bowel disease,” Journal of Crohn's and Colitis, vol. 5, no. 1, pp. 41–47, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. A. R. M. Sridhar, S. Parasa, U. Navaneethan, M. D. Crowell, and K. Olden, “Comprehensive study of cardiovascular morbidity in hospitalized inflammatory bowel disease patients,” Journal of Crohn's and Colitis, vol. 5, no. 4, pp. 287–294, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. M. T. Osterman, Y. X. Yang, C. Brensinger, K. A. Forde, G. R. Lichtenstein, and J. D. Lewis, “No increased risk of myocardial infarction among patients with ulcerative colitis or Crohn’s disease,” Clinical Gastroenterology and Hepatology, vol. 9, no. 10, pp. 875–880, 2011. View at Google Scholar
  111. S. D. Dorn and R. S. Sandler, “Inflammatory bowel disease is not a risk factor for cardiovascular disease mortality: results from a systematic review and meta-analysis,” American Journal of Gastroenterology, vol. 102, no. 3, pp. 662–667, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. M. N. Di Minno, S. Iervolino, R. Peluso, R. Scarpa, and G. Di Minno, “TNF-α blockers and carotid intima-media thickness: an emerging issue in the treatment of psoriatic arthritis,” Internal and Emergency Medicine, vol. 7, supplement 2, pp. 97–98, 2012. View at Google Scholar
  113. M. N. Di Minno, S. Iervolino, R. Peluso, R. Scarpa, and G. Di Minno, “Carotid intima-media thickness in psoriatic arthritis: differences between tumor necrosis factor-α blockers and traditional disease-modifying antirheumatic drugs,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 3, pp. 705–712, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. R. J. Bisoendial, E. S. G. Stroes, and P. P. Tak, “Where the immune response meets the vessel wall,” Netherlands Journal of Medicine, vol. 67, no. 8, pp. 328–333, 2009. View at Google Scholar · View at Scopus
  115. M. N. Di Minno, S. Iervolino, R. Lupoli et al., “Cardiovascular risk in rheumatic patients: the link between inflammation and atherothrombosis,” Seminars in Thrombosis and Hemostasis, vol. 38, no. 5, pp. 497–505, 2012. View at Publisher · View at Google Scholar
  116. C. Gonzalez-Juanatey, J. Llorca, E. Amigo-Diaz, T. Dierssen, J. Martin, and M. A. Gonzalez-Gay, “High prevalence of subclinical atherosclerosis in psoriatic arthritis patients without clinically evident cardiovascular disease or classic atherosclerosis risk factors,” Arthritis Care and Research, vol. 57, no. 6, pp. 1074–1080, 2007. View at Publisher · View at Google Scholar · View at Scopus
  117. I. Sari, T. Okan, S. Akar et al., “Impaired endothelial function in patients with ankylosing spondylitis,” Rheumatology, vol. 45, no. 3, pp. 283–286, 2006. View at Publisher · View at Google Scholar · View at Scopus
  118. S. Mathieu, H. Joly, G. Baron et al., “Trend towards increased arterial stiffness or intima-media thickness in ankylosing spondylitis patients without clinically evident cardiovascular disease,” Rheumatology, vol. 47, no. 8, pp. 1203–1207, 2008. View at Publisher · View at Google Scholar · View at Scopus
  119. M. Caliskan, D. Erdogan, H. Gullu et al., “Impaired coronary microvascular and left ventricular diastolic functions in patients with ankylosing spondylitis,” Atherosclerosis, vol. 196, no. 1, pp. 306–312, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. D. Malesci, A. Niglio, G. A. Mennillo, R. Buono, G. Valentini, and G. La Montagna, “High prevalence of metabolic syndrome in patients with ankylosing spondylitis,” Clinical Rheumatology, vol. 26, no. 5, pp. 710–714, 2007. View at Publisher · View at Google Scholar · View at Scopus
  121. J. Y. Choe, M. Y. Lee, I. Rheem, M. Y. Rhee, S. H. Park, and S. K. Kim, “No differences of carotid intima-media thickness between young patients with ankylosing spondylitis and healthy controls,” Joint Bone Spine, vol. 75, no. 5, pp. 548–553, 2008. View at Publisher · View at Google Scholar · View at Scopus
  122. M. N. Di Minno, A. Tufano, W. Ageno, P. Prandoni, and G. Di Minno, “Identifying high-risk individuals for cardiovascular disease: similarities between venous and arterial thrombosis in perspective. A 2011 update,” Internal and Emergency Medicine, vol. 7, no. 1, pp. 9–13, 2012. View at Publisher · View at Google Scholar · View at Scopus
  123. I. Ferrer, G. Benavent, G. Bastida et al., “Peripheral arterial thromboembolism in Crohn's disease,” Gastroenterología y Hepatología, vol. 36, no. 1, pp. 30–34, 2013. View at Publisher · View at Google Scholar
  124. J. H. Tabibian and M. B. Streiff, “Inflammatory bowel disease-associated thromboembolism: a systematic review of outcomes with anticoagulation versus catheter-directed thrombolysis,” Inflammatory Bowel Diseases, vol. 18, no. 1, pp. 161–171, 2012. View at Publisher · View at Google Scholar
  125. H. Issa, S. Al-Momen, B. Bseiso et al., “Thomboembolism in inflammatory bowel diseases: a report from Saudi Arabia,” Clinical and Experimental Gastroenterology, vol. 4, no. 1, pp. 1–7, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Danese, A. Papa, S. Saibeni, A. Repici, A. Malesci, and M. Vecchi, “Inflammation and coagulation in inflammatory bowel disease: the clot thickens—CME,” American Journal of Gastroenterology, vol. 102, no. 1, pp. 174–186, 2007. View at Publisher · View at Google Scholar · View at Scopus
  127. K. Kume, M. Yamasaki, M. Tashiro, I. Yoshikawa, and M. Otsuki, “Activations of coagulation and fibrinolysis secondary to bowel inflammation in patients with ulcerative colitis,” Internal Medicine, vol. 46, no. 17, pp. 1323–1330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  128. E. Chiarantini, R. Valanzano, A. A. Liotta et al., “Hemostatic abnormalities in inflammatory bowel disease,” Thrombosis Research, vol. 82, no. 2, pp. 137–146, 1996. View at Publisher · View at Google Scholar · View at Scopus
  129. P. Weber, S. Husemann, H. Vielhaber, K. P. Zimmer, and U. Nowak-Göttl, “Coagulation and fibrinolysis in children, adolescents, and young adults with inflammatory bowel disease,” Journal of Pediatric Gastroenterology and Nutrition, vol. 28, no. 4, pp. 418–422, 1999. View at Publisher · View at Google Scholar · View at Scopus
  130. A. A. van Bodegraven, M. Schoorl, R. K. Linskens, P. C. Bartels, and H. A. Tuynman, “Persistent activation of coagulation and fibrinolysis after treatment of active ulcerative colitis,” European Journal of Gastroenterology and Hepatology, vol. 14, no. 4, pp. 413–418, 2002. View at Publisher · View at Google Scholar · View at Scopus
  131. S. Ghosh, M. J. Mackie, B. A. McVerry, M. Galloway, A. Ellis, and J. McKay, “Chronic inflammatory bowel disease, deep-venous thrombosis and antithrombin activity,” Acta Haematologica, vol. 70, no. 1, pp. 50–53, 1983. View at Google Scholar · View at Scopus
  132. A. Papa, F. Scaldaferri, S. Danese et al., “Vascular involvement in inflammatory bowel disease: pathogenesis and clinical aspects,” Digestive Diseases, vol. 26, no. 2, pp. 149–155, 2008. View at Publisher · View at Google Scholar · View at Scopus
  133. S. Horowitz, D. G. Binion, V. M. Nelson et al., “Increased arginase activity and endothelial dysfunction in human inflammatory bowel disease,” American Journal of Physiology, vol. 292, no. 5, pp. G1323–G1336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. D. A. Morowitz, L. W. Allen, and J. B. Kirsner, “Thrombocytosis in chronic inflammatory bowel disease,” Annals of Internal Medicine, vol. 68, no. 5, pp. 1013–1021, 1968. View at Google Scholar · View at Scopus
  135. O. Yüksel, K. Helvaci, O. Başar et al., “An overlooked indicator of disease activity in ulcerative colitis: mean platelet volume,” Platelets, vol. 20, no. 4, pp. 277–281, 2009. View at Publisher · View at Google Scholar
  136. C. E. Collins, M. R. Cahill, A. C. Newland, and D. S. Rampton, “Platelets circulate in an activated state in inflammatory bowel disease,” Gastroenterology, vol. 106, no. 4, pp. 840–845, 1994. View at Google Scholar · View at Scopus
  137. P. M. Irving, M. G. Macey, U. Shah, L. Webb, L. Langmead, and D. S. Rampton, “Formation of platelet-leukocyte aggregates in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 10, no. 4, pp. 361–372, 2004. View at Publisher · View at Google Scholar · View at Scopus
  138. C. N. Bernstein, A. Wajda, and J. F. Blanchard, “The clustering of other chronic inflammatory diseases in inflammatory bowel disease: a population-based study,” Gastroenterology, vol. 129, no. 3, pp. 827–836, 2005. View at Publisher · View at Google Scholar · View at Scopus
  139. H. J. Kaufmann and H. L. Taubin, “Nonsteroidal anti-inflammatory drugs activate quiescent inflammatory bowel disease,” Annals of Internal Medicine, vol. 107, no. 4, pp. 513–516, 1987. View at Google Scholar · View at Scopus
  140. I. Bjarnason, J. Hayllar, A. J. MacPherson, and A. S. Russell, “Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans,” Gastroenterology, vol. 104, no. 6, pp. 1832–1847, 1993. View at Google Scholar · View at Scopus
  141. H. L. Kaufman, A. H. Fischer, M. Carroll, and J. M. Becker, “Colonic ulceration associated with nonsteroidal anti-inflammatory drugs: report of three cases,” Diseases of the Colon and Rectum, vol. 39, no. 6, pp. 705–710, 1996. View at Publisher · View at Google Scholar · View at Scopus
  142. A. S. Dissanayake and S. C. Truelove, “A controlled therapeutic trial of long term maintenance treatment of ulcerative colitis with sulphasalazine (Salazopyrin),” Gut, vol. 14, no. 12, pp. 923–926, 1973. View at Google Scholar · View at Scopus
  143. A. P. Dick, M. J. Grayson, R. G. Carpenter, and A. Petrie, “Controlled trial of sulphasalazine in the treatment of ulcerative colitis,” Gut, vol. 5, pp. 437–442, 1964. View at Publisher · View at Google Scholar
  144. M. B. Ferraz, P. Tugwell, C. H. Goldsmith, and E. Atra, “Meta-analysis of sulfasalazine in ankylosing spondylitis,” Journal of Rheumatology, vol. 17, no. 11, pp. 1482–1486, 1990. View at Google Scholar · View at Scopus
  145. L. Rodríguez-Bores, J. Barahona-Garrido, and J. K. Yamamoto-Furusho, “Basic and clinical aspects of osteoporosis in inflammatory bowel disease,” World Journal of Gastroenterology, vol. 13, no. 46, pp. 6156–6165, 2007. View at Publisher · View at Google Scholar · View at Scopus
  146. M. Padovan, G. Castellino, M. Govoni, and F. Trotta, “The treatment of the rheumatologicalmanifestations of the inflammatoryboweldiseases,” Rheumatology International, vol. 26, no. 11, pp. 953–958, 2006. View at Publisher · View at Google Scholar
  147. F. de Keyser, N. van Damme, M. de Vos, H. Mielants, and E. M. Veys, “Opportunities for immune modulation in the spondyloarthropathies with special reference to gut inflammation,” Inflammation Research, vol. 49, no. 2, pp. 47–54, 2000. View at Publisher · View at Google Scholar · View at Scopus
  148. J. Chen and C. Liu, “Methotrexate for ankylosing spondylitis,” Cochrane Database of Systematic Reviews, no. 3, Article ID CD004524, 2004. View at Google Scholar · View at Scopus
  149. H. Haibel, M. Rudwaleit, J. Braun, and J. Sieper, “Six months open label trial of leflunomide in active ankylosing spondylitis,” Annals of the Rheumatic Diseases, vol. 64, no. 1, pp. 124–126, 2005. View at Publisher · View at Google Scholar · View at Scopus
  150. R. Peluso, M. Atteno, S. Iervolino et al., “Methotrexate in the treatment of peripheral arthritis in ulcerative colitis,” Reumatismo, vol. 61, no. 1, pp. 15–20, 2009. View at Google Scholar · View at Scopus
  151. F. van den Bosch, E. Kruithof, M. de Vos, F. de Keyser, and H. Mielants, “Crohn's disease associated with spondyloarthropathy: effect of TNF-α blockade with infliximab on articular symptoms,” The Lancet, vol. 356, no. 9244, pp. 1821–1822, 2000. View at Google Scholar · View at Scopus
  152. H. Marzo-Ortega, D. McGonagle, P. O'Connor, and P. Emery, “Efficacy of etanercept for treatment of Crohn's related spondyloarthritis but not colitis,” Annals of the Rheumatic Diseases, vol. 62, no. 1, pp. 74–76, 2003. View at Publisher · View at Google Scholar · View at Scopus
  153. S. Iervolino, G. Tramontano, M. Lofrano et al., “Etanercept nel trattamento dell’artrite enteropatica associata a malattia di Crohn: descrizione di un caso clinico,” Reumatismo, vol. 63, supplement 3, p. 125, 2011. View at Google Scholar
  154. M. G. Neuman and R. M. Nanau, “Inflammatory bowel disease: role of diet, microbiota, life style,” Translational Research, vol. 160, no. 1, pp. 29–44, 2012. View at Google Scholar
  155. G. R. Veerappan, J. Betteridge, and P. E. Young, “Probiotics for the treatment of inflammatory bowel disease,” Current Gastroenterology Reports, vol. 14, no. 4, pp. 324–333, 2012. View at Publisher · View at Google Scholar
  156. O. Karimi and A. S. Peña, “Probiotics in arthralgia and spondyloarthropathies in patients with inflammatory bowel disease. Prospective randomized trials are necessary,” Revista Espanola de Enfermedades Digestivas, vol. 97, no. 8, pp. 570–574, 2005. View at Google Scholar · View at Scopus
  157. M. Rudwaleit and D. Baeten, “Ankylosing spondylitis and bowel disease,” Best Practice and Research: Clinical Rheumatology, vol. 20, no. 3, pp. 451–471, 2006. View at Publisher · View at Google Scholar · View at Scopus
  158. B. W. Behm and S. J. Bickston, “Tumor necrosis factor-alpha antibody for maintenance of remission in Crohn's disease,” Cochrane Database of Systematic Reviews, no. 1, Article ID CD006893, 2008. View at Google Scholar · View at Scopus
  159. S. Gandhi, N. Narula, J. K. Marshall, and M. Farkouh, “Are patients with inflammatory bowel disease at increased risk of coronary artery disease?” The American Journal of Medicine, vol. 125, no. 10, pp. 956–962, 2012. View at Publisher · View at Google Scholar