PROGNOSTIC FACTORS IN CROHN’S DISEASE

Cover Page


Cite item

Full Text

Abstract

The paper contains a review of the literature data concerning the demographic, clinical, laboratory, genetic, immunohistochemical, endoscopic, and imaging features with a potential role of prognostic factors for clinical management of patients with Crohn’s
disease.

About the authors

O. B. Shchukina

North-Western State Medical University named after I.I. Mechnikov; 41 Kirochnaya ul., Saint-Petersburg, 191015, Russian Federation

Author for correspondence.
Email: burmao@gmail.com

PhD, Associate Professor, Department of Gastroenterology and Nutrition, North-Western State Medical University named after I.I. Mechnikov

Russian Federation

References

  1. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology. 1998;115(1):182-205.
  2. Solberg IC, Vatn MH, Høie O, Stray N, Sauar J, Jahnsen J, Moum B, Lygren I; IBSEN Study Group. Clinical course in Crohn’s disease: results of a Norwegian population-based ten-year follow-up study. Clin Gastroenterol Hepatol. 2007;5(12):1430-8.
  3. Rieder F, Lawrance IC, Leite A, Sans M. Predictors of fibrostenotic Crohn’s disease. Inflamm Bowel Dis. 2011;17(9):2000-7.
  4. Lichtenstein GR, Yan S, Bala M, Blank M, Sands BE. Infliximab maintenance treatment reduces hospitalizations, surgeries, and procedures in fistulizing Crohn’s disease. Gastroenterology. 2005;128(4):862-9.
  5. Szamosi T, Banai J, Lakatos L, Czegledi Z, David G, Zsigmond F, Pandur T, Erdelyi Z, Gemela O, Papp M, Papp J, Lakatos PL. Early azathioprine/biological therapy is associated with decreased risk for first surgery and delays time to surgery but not reoperation in both smokers and nonsmokers with Crohn’s disease, while smoking decreases the risk of colectomy in ulcerative colitis. Eur J Gastroenterol Hepatol. 2010;22(7):872-9.
  6. Papay P, Reinisch W, Ho E, Gratzer C, Lissner D, Herkner H, Riss S, Dejaco C, Miehsler W, Vogelsang H, Novacek G. The impact of thiopurines on the risk of surgical recurrence in patients with Crohn’s disease after first intestinal surgery. Am J Gastroenterol. 2010;105(5):1158-64.
  7. Schreiber S, Reinisch W, Colombel JF, Sandborn WJ, Hommes DW, Robinson AM, Huang B, Lomax KG, Pollack PF. Subgroup analysis of the placebo-controlled CHARM trial: increased remission rates through 3 years for adalimumab-treated patients with early Crohn’s disease. J Crohns Colitis. 2013;7(3):213-21.
  8. Magro F, Rodrigues-Pinto E, Coelho R, Andrade P, Santos-AntunesJ, Lopes S, Camila-Dias C, Macedo G. Is it possible to change phenotype progression in Crohn’s disease in the era of immunomodulators? Predictive factors of phenotype progression. Am J Gastroenterol. 2014;109(7):1026-36.
  9. Gupta N, Cohen SA, Bostrom AG, Kirschner BS, Baldassano RN, Winter HS, Ferry GD, Smith T, Abramson O, Gold BD, Heyman MB. Risk factors for initial surgery in pediatric patients with Crohn’s disease. Gastroenterology. 2006;130(4):1069-77.
  10. Wang JP, Huang MX, Yin L, Qian Q, Lan P, Wang T, He XS. Risk factors of operation and reoperation in patients with Crohn disease. Zhonghua Wei Chang Wai Ke Za Zhi. 2007;10(3):208-11.
  11. Mazor Y, Maza I, Kaufman E, Ben-Horin S, Karban A, Chowers Y, Eliakim R. Prediction of disease complication occurrence in Crohn’s disease using phenotype and genotype parameters at diagnosis. J Crohns Colitis. 2011;5(6):592-7.
  12. Bernell O, Lapidus A, Hellers G. Risk factors for surgery and postoperative recurrence in Crohn’s disease. Ann Surg. 2000;231(1):38-45.
  13. Romberg-Camps MJ, Dagnelie PC, Kester AD, Hesselink-van de KruijsMA, CilissenM, Engels LG, VanDeursen C, HameetemanWH, Wolters FL, Russel MG, Stockbrügger RW. Influence of phenotype at diagnosis and of other potential prognostic factors on the course of inflammatory bowel disease. Am J Gastroenterol. 2009;104(2):371-83.
  14. Beaugerie L, Seksik P, Nion-Larmurier I, Gendre JP, Cosnes J. Predictors of Crohn’s disease. Gastroenterology. 2006;130(3):650-6.
  15. Wolters FL, Russel MG, Sijbrandij J, Ambergen T, Odes S, Riis L, Langholz E, Politi P, Qasim A, KoutroubakisI, Tsianos E, Vermeire S, Freitas J, van Zeijl G, Hoie O, Bernklev T, Beltrami M, Rodriguez D, Stockbrügger RW, Moum B. Phenotype at diagnosis predicts recurrence rates in Crohn’s disease. Gut. 2006;55(8):1124-30.
  16. Tarrant KM, Barclay ML, Frampton CM, Gearry RB. Perianal disease predicts changes in Crohn’s disease phenotype-results of a population-based study of inflammatory bowel disease phenotype. Am J Gastroenterol. 2008;103(12):3082-93.
  17. Munkholm P, Langholz E, Davidsen M, Binder V. Disease activity courses in a regional cohort of Crohn’s disease patients. Scand J Gastroenterol. 1995;30(7):699-706.
  18. Louis E, Michel V, Hugot JP, Reenaers C, Fontaine F, Delforge M, El Yafi F, Colombel JF, Belaiche J. Early development of stricturing or penetrating pattern in Crohn’s disease is influenced by disease location, number of flares, and smoking but not by NOD2/CARD15 genotype. Gut. 2003;52(4):552-7.
  19. Lakatos PL, Czegledi Z, Szamosi T, Banai J, David G, Zsigmond F, Pandur T, Erdelyi Z, Gemela O, Papp J, Lakatos L. Perianal disease, small bowel disease, smoking, prior steroid or early azathioprine/ biological therapy are predictors of disease behavior change in patients with Crohn’s disease. World J Gastroenterol. 2009;15(28):3504-10.
  20. Louis E, Collard A, Oger AF, Degroote E, Aboul Nasr El Yafi FA, Belaiche J. Behaviour of Crohn’s disease according to the Vienna classification: changing pattern over the course of the disease. Gut. 2001;49(6):777-82.
  21. Chow DK, Sung JJ, Wu JC, Tsoi KK, Leong RW, Chan FK. Upper gastrointestinal tract phenotype of Crohn’s disease is associated with early surgery and further hospitalization. Inflamm Bowel Dis. 2009;15(4):551-7.
  22. Hellers G, Bergstrand O, Ewerth S, Holmström B. Occurrence and outcome after primary treatment of anal fistulae in Crohn’s disease. Gut. 1980;21(6):525-7.
  23. Loly C, Belaiche J, Louis E. Predictors of severe Crohn’s disease. Scand J Gastroenterol. 2008;43(8):948-54.
  24. Sands BE, Arsenault JE, Rosen MJ, Alsahli M, Bailen L, Banks P, Bensen S, Bousvaros A, Cave D, Cooley JS, Cooper HL, Edwards ST, Farrell RJ, Griffin MJ, Hay DW, John A, Lidofsky S, Olans LB, Peppercorn MA, Rothstein RI, Roy MA, Saletta MJ, Shah SA, Warner AS, Wolf JL, Vecchio J, Winter HS, Zawacki JK. Risk of early surgery for Crohn’s disease: implications for early treatment strategies. Am J Gastroenterol. 2003;98(12):2712-8.
  25. Lazarev M, Huang C, Bitton A, Cho JH, Duerr RH, McGovern DP, Proctor DD, Regueiro M, Rioux JD, Schumm PP, Taylor KD, Silverberg MS, Steinhart AH, Hutfless S, Brant SR. Relationship between proximal Crohn’s disease location and disease behavior and surgery: a cross-sectional study of the IBD Genetics Consortium. Am J Gastroenterol. 2013;108(1):106-12.
  26. Cosnes J, Seksik P, Nion-Larmurier I, Beaugerie L, Gendre JP. Prior appendectomy and the phenotype and course of Crohn’s disease. World J Gastroenterol. 2006;12(8):1235-42.
  27. Mahid SS, Minor KS, Stevens PL, Galandiuk S. The role of smoking in Crohn’s disease as defined by clinical variables. Dig Dis Sci. 2007;52(11):2897-903.
  28. Seksik P, Nion-Larmurier I, Sokol H, Beaugerie L, Cosnes J. Effects of light smoking consumption on the clinical course of Crohn’s disease. Inflamm Bowel Dis. 2009;15(5):734-41.
  29. Picco MF, Bayless TM. Tobacco consumption and disease duration are associated with fistulizing and stricturing behaviors in the first 8 years of Crohn’s disease. Am J Gastroenterol. 2003;98(2):363-8.
  30. Nunes T, Etchevers MJ, Domènech E, García-Sánchez V, Ber Y, Peñalva M, Merino O, Nos P, Garcia-Planella E, Casbas AG, Esteve M, Taxonera Samsó C, Montoro Huguet M, Gisbert JP, Martín Arranz MD, García-Sepulcre MF, Barreiro-de Acosta M, Beltrán B, Alcaide Suárez N, Saro Gismera C, Cabriada JL, Cañas-Ventura A, Gomollón F, Panés J; Tobacco-Eneida Study Group of GETECCU. Smoking does influence disease behaviour and impacts the need for therapy in Crohn’s disease in the biologic era. Aliment Pharmacol Ther. 2013;38(7):752-60.
  31. Lawrance IC, Murray K, Batman B, Gearry RB, Grafton R, Krishnaprasad K, Andrews JM, Prosser R, Bampton PA, Cooke SE, Mahy G, Radford-Smith G, Croft A, Hanigan K. Crohn’s disease and smoking: is it ever too late to quit? J Crohns Colitis. 2013;7(12):e665-71.
  32. Lakatos PL, Vegh Z, Lovasz BD, David G, Pandur T, Erdelyi Z, Szita I, Mester G, Balogh M, Szipocs I, Molnar C, Komaromi E, Golovics PA, Mandel M, Horvath A, Szathmari M, Kiss LS, Lakatos L. Is current smoking still an important environmental factor in inflammatory bowel diseases? Results from a population-based incident cohort. Inflamm Bowel Dis. 2013;19(5):1010-7.
  33. Lindberg E, Järnerot G, Huitfeldt B. Smoking in Crohn’s disease: effect on localisation and clinical course. Gut. 1992;33(6): 779-82.
  34. Russel MG, Volovics A, Schoon EJ, van Wijlick EH, Logan RF, Shivananda S, Stockbrügger RW. Inflammatory bowel disease: is there any relation between smoking status and disease presentation? European Collaborative IBD Study Group. Inflamm Bowel Dis. 1998;4(3):182-6.
  35. Aldhous MC, Drummond HE, Anderson N, Smith LA, Arnott ID, Satsangi J. Does cigarette smoking influence the phenotype of Crohn’s disease? Analysis using the Montreal classification. Am J Gastroenterol. 2007;102(3):577-88.
  36. Tobin MV, Logan RF, Langman MJ, McConnell RB, Gilmore IT. Cigarette smoking and inflammatory bowel disease. Gastroenterology. 1987;93(2):316-21.
  37. Cosnes J, Carbonnel F, Beaugerie L, Le Quintrec Y, Gendre JP. Effects of cigarette smoking on the long-term course of Crohn’s disease. Gastroenterology. 1996;110(2):424-31.
  38. Zabana Y, Garcia-Planella E, Van Domselaar M, Mañosa M, Gordillo J, López San Román A, Cabré E, Domènech E. Does active smoking really influence the course of Crohn’s disease? A retrospective observational study. J Crohns Colitis. 2013;7(4):280-5.
  39. Mahid SS, Minor KS, Stevens PL, Galandiuk S. The role of smoking in Crohn’s disease as defined by clinical variables. Dig Dis Sci. 2007;52(11):2897-903.
  40. Sutherland LR, Ramcharan S, Bryant H, Fick G. Effect of cigarette smoking on recurrence of Crohn’s disease. Gastroenterology. 1990;98(5 Pt 1):1123-8.
  41. Cottone M, Rosselli M, Orlando A, Oliva L, Puleo A, Cappello M, Traina M, Tonelli F, Pagliaro L. Smoking habits and recurrence in Crohn’s disease. Gastroenterology. 1994;106(3):643-8.
  42. Gustavsson A, Magnuson A, Blomberg B, Andersson M, Halfvarson J, Tysk C. Smoking is a risk factor for recurrence of intestinal stricture after endoscopic dilation in Crohn’s disease. Aliment Pharmacol Ther. 2013;37(4):430-7.
  43. Parsi MA, Achkar JP, Richardson S, Katz J, Hammel JP, Lashner BA, Brzezinski A. Predictors of response to infliximab in patients with Crohn’s disease. Gastroenterology. 2002;123(3):707-13.
  44. Arnott ID, McNeill G, Satsangi J. An analysis of factors influencing short-term and sustained response to infliximab treatment for Crohn’s disease. Aliment Pharmacol Ther. 2003;17(12): 1451-7.
  45. Cosnes J, Beaugerie L, Carbonnel F, Gendre JP. Smoking cessation and the course of Crohn’s disease: an intervention study. Gastroenterology. 2001;120(5):1093-9.
  46. Fowler SA, Ananthakrishnan AN, Gardet A, Stevens CR, Korzenik JR, Sands BE, Daly MJ, Xavier RJ, Yajnik V. SMAD3 gene variant is a risk factor for recurrent surgery in patients with Crohn’s disease. J Crohns Colitis. 2014;8(8):845-51.
  47. Parkes GC, Whelan K, Lindsay JO. Smoking in inflammatory bowel disease: Impact on disease course and insights into the aetiology of its effect. J Crohns Colitis. 2014;8(8):717-25.
  48. Beattie RM, Walker-Smith JA, Murch SH. Indications for investigation of chronic gastrointestinal symptoms. Arch Dis Child. 1995;73(4):354-5.
  49. Poullis AP, Zar S, Sundaram KK, Moodie SJ, Risley P, Theodossi A, Mendall MA. A new, highly sensitive assay for C-reactive protein can aid the differentiation of inflammatory bowel disorders from constipation- and diarrhoea-predominant functional bowel disorders. Eur J Gastroenterol Hepatol. 2002;14(4): 409-12.
  50. André C, Descos L, Vignal J, Gillon J. C-reactive protein as a predictor of relapse in asymptomatic patients with Crohn’s disease. Scott Med J. 1983;28(1):26-9.
  51. Consigny Y, Modigliani R, Colombel JF, Dupas JL, Lémann M, Mary JY; Groupe d’Etudes Thérapeutiques des Affections Inflammatoires Digestives (GETAID). A simple biological score for predicting low risk of short-term relapse in Crohn’s disease. Inflamm Bowel Dis. 2006;12(7):551-7.
  52. Henriksen M, Jahnsen J, Lygren I, Stray N, Sauar J, Vatn MH, Moum B; IBSEN Study Group. C-reactive protein: a predictive factor and marker of inflammation in inflammatory bowel disease. Results from a prospective population-based study. Gut. 2008;57(11):1518-23.
  53. Reinisch W, Gasché C, Tillinger W, Wyatt J, Lichtenberger C, Willheim M, Dejaco C, Waldhör T, Bakos S, Vogelsang H, Gangl A, Lochs H. Clinical relevance of serum interleukin-6 in Crohn’s disease: single point measurements, therapy monitoring, and prediction of clinical relapse. Am J Gastroenterol. 1999;94(8):2156-64.
  54. Louis E, Belaiche J, Van Kemseke C, Schaaf N, Mahieu P, Mary JY. Soluble interleukin-2 receptor in Crohn’s disease. Assessment of disease activity and prediction of relapse. Dig Dis Sci. 1995;40(8):1750-6.
  55. De Bruyn M, Bessissow T, Billiet T, Cleynen I, Kirkland R, Liu X, Hauenstein S, Drake K, Singh S, Ferrante M, Rutgeerts P, Van Assche G, Arijs I, Opdenakker G, Vermeire S. Biomarker panel for prediction of mucosal healing in patients with Crohn’s disease under infliximab therapy. J Crohns Colitis. 2014;8 Suppl 1:S45-6.
  56. Quinton JF, Sendid B, Reumaux D, Duthilleul P, Cortot A, Grandbastien B, Charrier G, Targan SR, Colombel JF, Poulain D. AntiSaccharomyces cerevisiae mannan antibodies combined with antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease: prevalence and diagnostic role. Gut. 1998;42(6):788-91.
  57. Ruemmele FM, Targan SR, Levy G, Dubinsky M, Braun J, Seidman EG. Diagnostic accuracy of serological assays in pediatric inflammatory bowel disease. Gastroenterology. 1998;115(4): 822-9.
  58. Landers CJ, Cohavy O, Misra R, Yang H, Lin YC, Braun J, Targan SR. Selected loss of tolerance evidenced by Crohn’s disease-associated immune responses to auto- and microbial antigens. Gastroenterology. 2002;123(3):689-99.
  59. Vasiliauskas EA, Kam LY, Karp LC, Gaiennie J, Yang H, Targan SR. Marker antibody expression stratifies Crohn’s disease into immunologically homogeneous subgroups with distinct clinical characteristics. Gut. 2000;47(4):487-96.
  60. Arnott ID, Landers CJ, Nimmo EJ, Drummond HE, Smith BK, Targan SR, Satsangi J. Sero-reactivity to microbial components in Crohn’s disease is associated with disease severity and progression, but not NOD2/CARD15 genotype. Am J Gastroenterol. 2004;99(12):2376-84.
  61. Targan SR, Landers CJ, Yang H, Lodes MJ, Cong Y, Papadakis KA, Vasiliauskas E, Elson CO, Hershberg RM. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn’s disease. Gastroenterology. 2005;128(7):2020-8.
  62. Rieder F, Lawrance IC, Leite A, Sans M. Predictors of fibrostenotic Crohn’s disease. Inflamm Bowel Dis. 2011;17(9):2000-7.
  63. Bien AC, Kuemmerle JFK. Fibrosis in Crohn’s disease. Inflamm Bowel Dis Monit. 2012;12(3):102-9.
  64. Amre DK, Lambrette P, Law L, Krupoves A, Chotard V, Costea F, Grimard G, Israel D, Mack D, Seidman EG. Investigating the hygiene hypothesis as a risk factor in pediatric onset Crohn’s disease: a case-control study. Am J Gastroenterol. 2006;101(5):1005-11.
  65. Dubinsky MC, Lin YC, Dutridge D, Picornell Y, Landers CJ, Farrior S, Wrobel I, Quiros A, Vasiliauskas EA, Grill B, Israel D, Bahar R, Christie D, Wahbeh G, Silber G, Dallazadeh S, Shah P, Thomas D, Kelts D, Hershberg RM, Elson CO, Targan SR, Taylor KD, Rotter JI, Yang H; Western Regional Pediatric IBD Research Alliance. Serum immune responses predict rapid disease progression among children with Crohn’s disease: immune responses predict disease progression. Am J Gastroenterol. 2006;101(2):360-7.
  66. Vasiliauskas EA, Plevy SE, Landers CJ, Binder SW, Ferguson DM, Yang H, Rotter JI, Vidrich A, Targan SR. Perinuclear antineutrophil cytoplasmic antibodies in patients with Crohn’s disease define a clinical subgroup. Gastroenterology. 1996;110(6):1810-9.
  67. Zhang Z, Li C, Zhao X, Lv C, He Q, Lei S, Guo Y, Zhi F. Anti-Saccharomyces cerevisiae antibodies associate with phenotypes and higher risk for surgery in Crohn’s disease: a meta-analysis. Dig Dis Sci. 2012;57(11):2944-54.
  68. Beaugerie L, Sokol H. Clinical, serological and genetic predictors of inflammatory bowel disease course. World J Gastroenterol. 2012;18(29):3806-13.
  69. Carbonnel F, Macaigne G, Beaugerie L, Gendre JP, Cosnes J. Crohn’s disease severity in familial and sporadic cases. Gut. 1999;44(1):91-5.
  70. Khor B, Gardet A, Xavier RJ. Genetics and pathogenesis of inflammatory bowel disease. Nature. 2011;474(7351):307-17.
  71. Cleynen I, González JR, Figueroa C, Franke A, McGovern D, Bortlík M, Crusius BJ, Vecchi M, Artieda M, Szczypiorska M, Bethge J, Arteta D, Ayala E, Danese S, van Hogezand RA, Panés J, Peña SA, Lukas M, Jewell DP, Schreiber S, Vermeire S, Sans M. Genetic factors conferring an increased susceptibility to develop Crohn’s disease also influence disease phenotype: results from the IBDchip European Project. Gut. 2013;62(11):1556-65.
  72. Lesage S, Zouali H, Cézard JP, Colombel JF, Belaiche J, Almer S, Tysk C, O’Morain C, Gassull M, Binder V, Finkel Y, Modigliani R, Gower-Rousseau C, Macry J, Merlin F, Chamaillard M, Jannot AS, ОБЗОРЫ, ЛЕКЦИИ, КЛИНИЧЕСКИЕ РЕКОМЕНДАЦИИ Альманах клинической медицины 13 № 33’2014 Thomas G, Hugot JP; EPWG-IBD Group; EPIMAD Group; GETAID Group. CARD15/NOD2 mutational analysis and genotype-phenotype correlation in 612 patients with inflammatory bowel disease. Am J Hum Genet. 2002;70(4):845-57.
  73. Abreu MT, Taylor KD, Lin YC, Hang T, Gaiennie J, Landers CJ, Vasiliauskas EA, Kam LY, Rojany M, Papadakis KA, Rotter JI, Targan SR, Yang H. Mutations in NOD2 are associated with fibrostenosing disease in patients with Crohn’s disease. Gastroenterology. 2002;123(3):679-88.
  74. Alvarez-Lobos M, Arostegui JI, Sans M, Tassies D, Plaza S, Delgado S, Lacy AM, Pique JM, Yagüe J, PanésJ. Crohn’s disease patients carrying Nod2/CARD15 gene variants have an increased and early need for first surgery due to stricturing disease and higher rate of surgical recurrence. Ann Surg. 2005;242(5):693-700.
  75. Renda MC, Cottone M. Prevalence of CARD15/NOD2 mutations in the Sicilian population. Am J Gastroenterol. 2008;103(1):248-9.
  76. Weersma RK, Stokkers PC, Cleynen I, Wolfkamp SC, Henckaerts L, Schreiber S, Dijkstra G, Franke A, Nolte IM, Rutgeerts P, Wijmenga C, Vermeire S. Confirmation of multiple Crohn’s disease susceptibility loci in a large Dutch-Belgian cohort. Am J Gastroenterol. 2009;104(3):630-8.
  77. Hampe J, Grebe J, Nikolaus S, Solberg C, Croucher PJ, Mascheretti S, Jahnsen J, Moum B, Klump B, Krawczak M, Mirza MM, Foelsch UR, Vatn M, Schreiber S. Association of NOD2 (CARD 15) genotype with clinical course of Crohn’s disease: a cohort study. Lancet. 2002;359(9318):1661-5.
  78. Heliö T, Halme L, Lappalainen M, Fodstad H, Paavola-Sakki P, Turunen U, Färkkilä M, Krusius T, Kontula K. CARD15/NOD2 gene variants are associated with familially occurring and complicated forms of Crohn’s disease. Gut. 2003;52(4):558-62.
  79. Cuthbert AP, Fisher SA, Mirza MM, King K, Hampe J, Croucher PJ, Mascheretti S, Sanderson J, Forbes A, Mansfield J, Schreiber S, Lewis CM, Mathew CG. The contribution of NOD2 gene mutations to the risk and site of disease in inflammatory bowel disease. Gastroenterology. 2002;122(4):867-74.
  80. Ahmad T, Armuzzi A, Bunce M, Mulcahy-Hawes K, Marshall SE, Orchard TR, Crawshaw J, Large O, de Silva A, Cook JT, Barnardo M, Cullen S, Welsh KI, Jewell DP. The molecular classification of the clinical manifestations of Crohn’s disease. Gastroenterology. 2002;122(4):854-66.
  81. Vavassori P, Borgiani P, D’Apice MR, De Negris F, Del Vecchio Blanco G, Monteleone I, Biancone L, Novelli G, Pallone E. 3020insC mutation within the NOD2 gene in Crohn’s disease: frequency and association with clinical pattern in an Italian population. Dig Liver Dis. 2002;34(2):153.
  82. Brant SR, Picco MF, Achkar JP, Bayless TM, Kane SV, Brzezinski A, Nouvet FJ, Bonen D, Karban A, Dassopoulos T, Karaliukas R, Beaty TH, Hanauer SB, Duerr RH, Cho JH. Defining complex contributions of NOD2/CARD15 gene mutations, age at onset, and tobacco use on Crohn’s disease phenotypes. Inflamm Bowel Dis. 2003;9(5):281-9.
  83. Economou M, Trikalinos TA, Loizou KT, Tsianos EV, IoannidisJP. Differential effects of NOD2 variants on Crohn’s disease risk and phenotype in diverse populations: a metaanalysis. Am J Gastroenterol. 2004;99(12):2393-404.
  84. Prager M, Büttner J, Haas V, Baumgart DC, Sturm A, Zeitz M, Büning C. The JAK2 variant rs10758669 in Crohn’s disease: altering the intestinal barrier as one mechanism of action. Int J Colorectal Dis. 2012;27(5):565-73.
  85. Figueroa C, Cleynen I, Franke A, McGovern DP, Bortlik M, Crusius JBA, Vecchi M, Artieda M, Szczypiorska M, Arteta D, Ayala E, González JR, Danese S, van Hogezand RA, Peña AS, Lukas M, Jewell DP, Schreiber S, Vermeire S, Sans M. Genetic factors conferring an increased susceptibility to develop Crohn’s disease also influence disease phenotype, but do not predict it. Results from the IBDChip European Project. Gastroenterology. 2010;138(5 Suppl 1): S677-8.
  86. Pierik M, Joossens S, Van Steen K, Van Schuerbeek N, Vlietinck R, Rutgeerts P, Vermeire S. Toll-like receptor-1, -2, and -6 polymorphisms influence disease extension in inflammatory bowel diseases. Inflamm Bowel Dis. 2006;12(1):1-8.
  87. Meijer MJ, Mieremet-Ooms MA, van Hogezand RA, Lamers CB, Hommes DW, Verspaget HW. Role of matrix metalloproteinase, tissue inhibitor of metalloproteinase and tumor necrosis factoralpha single nucleotide gene polymorphisms in inflammatory bowel disease. World J Gastroenterol. 2007;13(21):2960-6.
  88. Rieder F, Lawrance IC, Leite A, Sans M. Predictors of fibrostenotic Crohn’s disease. Inflamm Bowel Dis. 2011;17(9):2000-7.
  89. Henckaerts L, Van Steen K, Verstreken I, Cleynen I, Franke A, Schreiber S, Rutgeerts P, Vermeire S. Genetic risk profiling and prediction of disease course in Crohn’s disease patients. Clin Gastroenterol Hepatol. 2009;7(9):972-80.
  90. Adler J, Rangwalla SC, Dwamena BA, Higgins PD. The prognostic power of the NOD2 genotype for complicated Crohn’s disease: a meta-analysis. Am J Gastroenterol. 2011;106(4):699-712.
  91. Cucchiara S, Latiano A, Palmieri O, Canani RB, D’Incà R, Guariso G, Vieni G, De Venuto D, Riegler G, De’Angelis GL, Guagnozzi D, Bascietto C, Miele E, Valvano MR, Bossa F, Annese V; Italian Society of Pediatric Gastroenterology and Nutrition. Polymorphisms of tumor necrosis factor-alpha but not MDR1 influence response to medical therapy in pediatric-onset inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2007;44(2):171-9.
  92. Farrell RJ, Kelleher D. Glucocorticoid resistance in inflammatory bowel disease. J Endocrinol. 2003;178(3):339-46.
  93. Potocnik U, Ferkolj I, Glavac D, Dean M. Polymorphisms in multidrug resistance 1 (MDR1) gene are associated with refractory Crohn disease and ulcerative colitis. Genes Immun. 2004;5(7): 530-9.
  94. Hlavaty T, Pierik M, Henckaerts L, Ferrante M, Joossens S, van Schuerbeek N, Noman M, Rutgeerts P, Vermeire S. Polymorphisms in apoptosis genes predict response to infliximab therapy in luminal and fistulizing Crohn’s disease. Aliment Pharmacol Ther. 2005;22(7):613-26.
  95. Frøslie KF, Jahnsen J, Moum BA, Vatn MH; IBSEN Group. Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology. 2007;133(2):412-22.
  96. Solberg IC, Lygren I, Jahnsen J, Vatn M, Mourn B. Mucosal healing after initial treatment may be a prognostic marker for longterm outcome in inflammatory bowel disease. Gut. 2008;57 (Suppl II):A15.
  97. Baert F, Moortgat L, Van Assche G, Caenepeel P, Vergauwe P, De Vos M, Stokkers P, Hommes D, Rutgeerts P, Vermeire S, D’Haens G; Belgian Inflammatory Bowel Disease Research Group; North-Holland Gut Club. Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn’s disease. Gastroenterology. 2010;138(2):463-8.
  98. Schnitzler F, Fidder H, Ferrante M, Noman M, ArijsI, Van Assche G, Hoffman I, Van Steen K, Vermeire S, Rutgeerts P. Mucosal healing predicts long-term outcome of maintenance therapy with infliximab in Crohn’s disease. Inflamm Bowel Dis. 2009;15(9):1295-301.
  99. Af Björkesten CG, Nieminen U, Sipponen T, Turunen U, Arkkila P, Färkkilä M. Mucosal healing at 3 months predicts long-term endoscopic remission in anti-TNF-treated luminal Crohn’s disease. Scand J Gastroenterol. 2013;48(5):543-51.
  100. Colombel JF, Rutgeerts P, Sandborn WJ. Achievement of early deep remission predicts better long-term outcomes for adalimumab-treated patients with Crohn’s disease: data from EXTEND. Am J Gastroenterol. 2010;105:S434-5.
  101. Allez M, Lemann M, Bonnet J, Cattan P, Jian R, Modigliani R. Long term outcome of patients with active Crohn’s disease exhibiting extensive and deep ulcerations at colonoscopy. Am J Gastroenterol. 2002;97(4):947-53.
  102. Nuij V, Looman C, Rijk M, Beukers R, Ouwendijk R, Quispel R, van Tilburg A, Tang T, Smalbraak H, Bruin K, Lindenburg F, PeyrinBiroulet L, van der Woude CJ. Microscopic severity is related to earlier surgery in newly diagnosed CD patients: results from the DELTA cohort ЕССО. J Crohns Colitis. 2013;7 Suppl 1:S182.
  103. Mazor Y, Karban A, Nesher S, Weiss B, Leshinsky-Silver E, Levine A, Eliakim R. Granulomas in Crohn’s disease: are newly discovered genetic variants involved? J Crohns Colitis. 2010;4(4):438-43.
  104. Bodily KD, Fletcher JG, Solem CA, Johnson CD, Fidler JL, Barlow JM, Bruesewitz MR, McCollough CH, Sandborn WJ, Loftus EV Jr, Harmsen WS, Crownhart BS. Crohn Disease: mural attenuation and thickness at contrast-enhanced CT Enterography–correlation with endoscopic and histologic findings of inflammation. Radiology. 2006;238(2):505-16.
  105. Low RN, Sebrechts CP, Politoske DA, Bennett MT, Flores S, Snyder RJ, Pressman JH. Crohn disease with endoscopic correlation: single-shot fast spin-echo and gadolinium-enhanced fat-suppressed spoiled gradient-echo MR imaging. Radiology. 2002;222(3):652-60.
  106. Rimola J, Ordás I, Rodriguez S, García-Bosch O, Aceituno M, Llach J, Ayuso C, Ricart E, PanésJ. Magnetic resonance imaging for evaluation of Crohn’s disease: validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis. 2011;17(8):1759-68.
  107. Lawrance IC, Welman CJ, Shipman P, Murray K. Correlation of MRI-determined small bowel Crohn’s disease categories with medical response and surgical pathology. World J Gastroenterol. 2009;15(27):3367-75.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2014 Shchukina O.B.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies