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Gastroenterology Research and Practice
Volume 2016, Article ID 1619053, 9 pages
http://dx.doi.org/10.1155/2016/1619053
Review Article

The Changing Phenotype of Inflammatory Bowel Disease

Department of Medicine and the APC Microbiome Institute, University College Cork, National University of Ireland, Cork, Ireland

Received 8 September 2016; Revised 1 November 2016; Accepted 8 November 2016

Academic Editor: Bjørn Moum

Copyright © 2016 Carthage Moran 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. N. A. Molodecky, I. S. Soon, D. M. Rabi et al., “Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review,” Gastroenterology, vol. 142, no. 1, pp. 46–54, 2012. View at Google Scholar
  2. 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 · View at Scopus
  3. D. Sheehan, C. Moran, and F. Shanahan, “The microbiota in inflammatory bowel disease,” Journal of Gastroenterology, vol. 50, no. 5, pp. 495–507, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Jess, L. Riis, I. Vind et al., “Changes in clinical characteristics, course, and prognosis of inflammatory bowel disease during the last 5 decades: a population-based study from Copenhagen, Denmark,” Inflammatory Bowel Diseases, vol. 13, no. 4, pp. 481–489, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. V. J. A. A. Nuij, Z. Zelinkova, M. C. M. Rijk et al., “Phenotype of inflammatory bowel disease at diagnosis in the Netherlands: a population-based inception cohort study (the Delta Cohort),” Inflammatory Bowel Diseases, vol. 19, no. 10, pp. 2215–2222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. K. T. Thia, W. J. Sandborn, W. S. Harmsen, A. R. Zinsmeister, and E. V. Loftus Jr., “Risk factors associated with progression to intestinal complications of Crohn's disease in a population-based cohort,” Gastroenterology, vol. 139, no. 4, pp. 1147–1155, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Moum, M. H. Vatn, A. Ekbom et al., “Incidence of ulcerative colitis and indeterminate colitis in four counties of southeastern Norway, 1990–93: a prospective population-based study,” Scandinavian Journal of Gastroenterology, vol. 31, no. 4, pp. 362–366, 1996. View at Publisher · View at Google Scholar · View at Scopus
  8. S. C. Ng, W. Tang, J. Y. Ching et al., “Incidence and phenotype of inflammatory bowel disease based on results from the Asia-Pacific Crohn's and colitis epidemiology study,” Gastroenterology, vol. 145, no. 1, pp. 158–165.e2, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. S. J. Park, W. H. Kim, and J. H. Cheon, “Clinical characteristics and treatment of inflammatory bowel disease: a comparison of Eastern and Western perspectives,” World Journal of Gastroenterology, vol. 20, no. 33, pp. 11525–11537, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Asakura, Y. Nishiwaki, N. Inoue, T. Hibi, M. Watanabe, and T. Takebayashi, “Prevalence of ulcerative colitis and Crohn's disease in Japan,” Journal of Gastroenterology, vol. 44, no. 7, pp. 659–665, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. S. C. Ng, Z. Zeng, O. Niewiadomski et al., “Early course of inflammatory bowel disease in a population-based inception cohort study from 8 countries in Asia and Australia,” Gastroenterology, vol. 150, no. 1, pp. 86–95, 2016. View at Publisher · View at Google Scholar
  12. K. Boonstra, K. J. van Erpecum, K. M. J. van Nieuwkerk et al., “Primary sclerosing cholangitis is associated with a distinct phenotype of inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 18, no. 12, pp. 2270–2276, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Penna, R. Dozois, W. Tremaine et al., “Pouchitis after ileal pouch-anal anastomosis for ulcerative colitis occurs with increased frequency in patients with associated primary sclerosing cholangitis,” Gut, vol. 38, no. 2, pp. 234–239, 1996. View at Publisher · View at Google Scholar · View at Scopus
  14. H. H. Zheng and X. L. Jiang, “Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and inflammatory bowel disease: a meta-analysis of 16 observational studies,” European Journal of Gastroenterology & Hepatology, vol. 28, no. 4, pp. 383–390, 2016. View at Google Scholar
  15. A. F. Gulamhusein, J. E. Eaton, J. H. Tabibian, E. J. Atkinson, B. D. Juran, and K. N. Lazaridis, “Duration of inflammatory bowel disease is associated with increased risk of cholangiocarcinoma in patients with primary sclerosing cholangitis and IBD,” The American Journal of Gastroenterology, vol. 111, no. 5, pp. 705–711, 2016. View at Publisher · View at Google Scholar
  16. T. Nic Suibhne, T. C. Raftery, O. McMahon, C. Walsh, C. O'Morain, and M. O'Sullivan, “High prevalence of overweight and obesity in adults with Crohn's disease: associations with disease and lifestyle factors,” Journal of Crohn's and Colitis, vol. 7, no. 7, pp. e241–e248, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Jia and E. I. Lubetkin, “Trends in quality-adjusted life-years lost contributed by smoking and obesity,” American Journal of Preventive Medicine, vol. 38, no. 2, pp. 138–144, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. V. B. Young, L. H. Raffals, S. M. Huse et al., “Multiphasic analysis of the temporal development of the distal gut microbiota in patients following ileal pouch anal anastomosis,” Microbiome, vol. 1, no. 1, article 9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Steed, S. Walsh, and N. Reynolds, “A brief report of the epidemiology of obesity in the inflammatory bowel disease population of Tayside, Scotland,” Obesity Facts, vol. 2, no. 6, pp. 370–372, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Flores, E. Burstein, D. J. Cipher, and L. A. Feagins, “Obesity in inflammatory bowel disease: a marker of less severe disease,” Digestive Diseases and Sciences, vol. 60, no. 8, pp. 2436–2445, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. G. W. Moran, M.-F. Dubeau, G. G. Kaplan, R. Panaccione, and S. Ghosh, “The increasing weight of Crohn's disease subjects in clinical trials: a hypothesis-generatings time-trend analysis,” Inflammatory Bowel Diseases, vol. 19, no. 13, pp. 2949–2956, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Fink, I. Karagiannides, K. Bakirtzi, and C. Pothoulakis, “Adipose tissue and inflammatory bowel disease pathogenesis,” Inflammatory Bowel Diseases, vol. 18, no. 8, pp. 1550–1557, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Gonçalves, F. Magro, and F. Martel, “Metabolic inflammation in inflammatory bowel disease: crosstalk between adipose tissue and bowel,” Inflammatory Bowel Diseases, vol. 21, no. 2, pp. 453–467, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. S. S. M. Chan, R. Luben, A. Olsen et al., “Body mass index and the risk for crohn's disease and ulcerative colitis: Data from a European Prospective Cohort Study (The IBD in EPIC Study),” American Journal of Gastroenterology, vol. 108, no. 4, pp. 575–582, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. M. A. Mendall, A. V. Gunasekera, B. J. John, and D. Kumar, “Is obesity a risk factor for Crohn's disease?” Digestive Diseases and Sciences, vol. 56, no. 3, pp. 837–844, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Khalili, A. N. Ananthakrishnan, G. G. Konijeti et al., “Measures of obesity and risk of Crohn's disease and ulcerative colitis,” Inflammatory Bowel Diseases, vol. 21, no. 2, pp. 361–368, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Ferguson and D. M. Sedgwick, “Juvenile onset inflammatory bowel disease: height and body mass index in adult life,” British Medical Journal, vol. 308, no. 6939, pp. 1259–1263, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Kugathasan, J. Nebel, J. A. Skelton et al., “Body mass index in children with newly diagnosed inflammatory bowel disease: observations from two multicenter North American inception cohorts,” The Journal of Pediatrics, vol. 151, no. 5, pp. 523–527, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. C. L. Ogden, M. D. Carroll, L. R. Curtin, M. M. Lamb, and K. M. Flegal, “Prevalence of high body mass index in US children and adolescents, 2007-2008,” The Journal of the American Medical Association, vol. 303, no. 3, pp. 242–249, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. M. D. Long, W. V. Crandall, I. H. Leibowitz et al., “Prevalence and epidemiology of overweight and obesity in children with inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 17, no. 10, pp. 2162–2168, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Blain, S. Cattan, L. Beaugerie, F. Carbonnel, J. Gendre, and J. Cosnes, “Crohn's disease clinical course and severity in obese patients,” Clinical Nutrition, vol. 21, no. 1, pp. 51–57, 2002. View at Publisher · View at Google Scholar
  32. A. G. Renehan, M. Tyson, M. Egger, R. F. Heller, and M. Zwahlen, “Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies,” The Lancet, vol. 371, no. 9612, pp. 569–578, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. J. W. Harper, M. N. Sinanan, and T. L. Zisman, “Increased body mass index is associated with earlier time to loss of response to infliximab in patients with inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 19, no. 10, pp. 2118–2124, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Bhalme, A. Sharma, R. Keld, R. Willert, and S. Campbell, “Does weight-adjusted anti-tumour necrosis factor treatment favour obese patients with Crohn's disease?” European Journal of Gastroenterology and Hepatology, vol. 25, no. 5, pp. 543–549, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. M. K. Krane, M. E. Allaix, M. Zoccali et al., “Does morbid obesity change outcomes after laparoscopic surgery for inflammatory bowel disease? review of 626 consecutive cases,” Journal of the American College of Surgeons, vol. 216, no. 5, pp. 986–996, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. Population Division and DESA, United Nations: World Population Ageing 1950–2050, http://www.un.org/esa/population.
  37. G. C. Nguyen, L. Sheng, and E. I. Benchimol, “Health care utilization in elderly onset inflammatory bowel disease: A Population-Based Study,” Inflammatory Bowel Diseases, vol. 21, no. 4, pp. 777–782, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Charpentier, J. Salleron, G. Savoye et al., “Natural history of elderly-onset inflammatory bowel disease: a population-based cohort study,” Gut, vol. 63, no. 3, pp. 423–432, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. A. N. Ananthakrishnan, E. L. McGinley, and D. G. Binion, “Inflammatory bowel disease in the elderly is associated with worse outcomes: a national study of hospitalizations,” Inflammatory Bowel Diseases, vol. 15, no. 2, pp. 182–189, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Cheddani, L. Dauchet, M. Fumery et al., “Cancer in elderly onset inflammatory bowel disease: a population-based study,” The American Journal of Gastroenterology, vol. 111, no. 10, pp. 1428–1436, 2016. View at Publisher · View at Google Scholar
  41. R. W. Lynch, D. Lowe, A. Protheroe, R. Driscoll, J. M. Rhodes, and I. D. R. Arnott, “Outcomes of rescue therapy in acute severe ulcerative colitis: data from the United Kingdom inflammatory bowel disease audit,” Alimentary Pharmacology and Therapeutics, vol. 38, no. 8, pp. 935–945, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Ikeuchi, M. Uchino, H. Matsuoka et al., “Prognosis following emergency surgery for ulcerative colitis in elderly patients,” Surgery Today, vol. 44, no. 1, pp. 39–43, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. A. N. Ananthakrishnan, H. Y. Shi, W. Tang et al., “Systematic review and meta-analysis: phenotype and clinical outcomes of older-onset inflammatory bowel disease,” Journal of Crohn's and Colitis, vol. 10, no. 10, pp. 1224–1236, 2016. View at Publisher · View at Google Scholar
  44. J. K. Hou, L. A. Feagins, and A. K. Waljee, “Characteristics and behavior of elderly-onset inflammatory bowel disease: a multi-center US study,” Inflammatory Bowel Diseases, vol. 22, no. 9, pp. 2200–2205, 2016. View at Publisher · View at Google Scholar
  45. H. J. Freeman, “Crohn's disease initially diagnosed after age 60 years,” Age and Ageing, vol. 36, no. 5, pp. 587–589, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Juneja, L. Baidoo, M. B. Schwartz et al., “Geriatric inflammatory bowel disease: phenotypic presentation, treatment patterns, nutritional status, outcomes, and comorbidity,” Digestive Diseases and Sciences, vol. 57, no. 9, pp. 2408–2415, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. M. J. Wagtmans, H. W. Verspaget, C. B. Lamers, and R. A. van Hogezand, “Crohn's disease in the elderly: a comparison with young adults,” Journal of Clinical Gastroenterology, vol. 27, no. 2, pp. 129–133, 1998. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Hadithi, M. Cazemier, G. A. Meijer et al., “Retrospective analysis of old-age colitis in the Dutch inflammatory bowel disease population,” World Journal of Gastroenterology, vol. 14, no. 20, pp. 3183–3187, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Gizard, A. C. Ford, J.-P. Bronowicki, and L. Peyrin-Biroulet, “Systematic review: the epidemiology of the hepatobiliary manifestations in patients with inflammatory bowel disease,” Alimentary Pharmacology and Therapeutics, vol. 40, no. 1, pp. 3–15, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. 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
  51. A. K. Lunder, J. R. Hov, A. Borthne et al., “Prevalence of sclerosing cholangitis detected by magnetic resonance cholangiography in patients with long-term inflammatory bowel disease,” Gastroenterology, vol. 151, no. 4, pp. 660–669.e4, 2016. View at Publisher · View at Google Scholar
  52. A. Sourianarayanane, G. Garg, T. H. Smith, M. I. Butt, A. J. McCullough, and B. Shen, “Risk factors of non-alcoholic fatty liver disease in patients with inflammatory bowel disease,” Journal of Crohn's and Colitis, vol. 7, no. 8, pp. e279–e285, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Rönnblom, T. Holmström, H. Tanghöj, F. Rorsman, and D. Sjöberg, “Appearance of hepatobiliary diseases in a population-based cohort with inflammatory bowel diseases (Inflammatory Bowel Disease Cohort of the Uppsala Region),” Journal of Gastroenterology and Hepatology, vol. 30, no. 8, pp. 1288–1292, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Bessissow, N. H. Le, K. Rollet, W. Afif, A. Bitton, and G. Sebastiani, “Incidence and predictors of nonalcoholic fatty liver disease by serum biomarkers in patients with inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 22, no. 8, pp. 1937–1944, 2016. View at Publisher · View at Google Scholar
  55. D. L. Nguyen, M. L. Bechtold, and M. M. Jamal, “National trends and inpatient outcomes of inflammatory bowel disease patients with concomitant chronic liver disease,” Scandinavian Journal of Gastroenterology, vol. 49, no. 9, pp. 1091–1095, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Yuhara, C. Steinmaus, D. Corley et al., “Meta-analysis: the risk of venous thromboembolism in patients with inflammatory bowel disease,” Alimentary Pharmacology and Therapeutics, vol. 37, no. 10, pp. 953–962, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Fumery, C. Xiaocang, L. Dauchet, C. Gower-Rousseau, L. Peyrin-Biroulet, and J.-F. Colombel, “Thromboembolic events and cardiovascular mortality in inflammatory bowel diseases: A Meta-Analysis of Observational Studies,” Journal of Crohn's and Colitis, vol. 8, no. 6, pp. 469–479, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. E. A. Scoville, G. G. Konijeti, D. D. Nguyen, J. Sauk, V. Yajnik, and A. N. Ananthakrishnan, “Venous thromboembolism in patients with inflammatory bowel diseases: a case-control study of risk factors,” Inflammatory Bowel Diseases, vol. 20, no. 4, pp. 631–636, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. S. L. Kristensen, O. Ahlehoff, J. Lindhardsen et al., “Inflammatory bowel disease is associated with an increased risk of hospitalization for heart failure: a danish nationwide cohort study,” Circulation: Heart Failure, vol. 7, no. 5, pp. 717–722, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. S. L. Kristensen, J. Lindhardsen, O. Ahlehoff et al., “Increased risk of atrial fibrillation and stroke during active stages of inflammatory bowel disease: a nationwide study,” Europace, vol. 16, no. 4, pp. 477–484, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. W.-S. Huang, C.-H. Tseng, P.-C. Chen et al., “Inflammatory bowel diseases increase future ischemic stroke risk: a Taiwanese population-based retrospective cohort study,” European Journal of Internal Medicine, vol. 25, no. 6, pp. 561–565, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. S. L. Kristensen, O. Ahlehoff, J. Lindhardsen et al., “Disease activity in inflammatory bowel disease is associated with increased risk of myocardial infarction, stroke and cardiovascular death—a Danish nationwide cohort study,” PLoS ONE, vol. 8, no. 2, Article ID e56944, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. J. R. Goodhand, M. Wahed, J. E. Mawdsley, A. D. Farmer, Q. Aziz, and D. S. Rampton, “Mood disorders in inflammatory bowel disease: relation to diagnosis, disease activity, perceived stress, and other factors,” Inflammatory Bowel Diseases, vol. 18, no. 12, pp. 2301–2309, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. E. McDermott, G. Mullen, J. Moloney et al., “Body image dissatisfaction: clinical features, and psychosocial disability in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 21, no. 2, pp. 353–360, 2015. View at Publisher · View at Google Scholar · View at Scopus
  65. C. P. Selinger, J. Eaden, D. Brian Jones et al., “Modifiable factors associated with nonadherence to maintenance medication for inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 19, no. 10, pp. 2199–2206, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. E. Szigethy, S. I. Bujoreanu, A. O. Youk et al., “Randomized efficacy trial of two psychotherapies for depression in youth with inflammatory bowel disease,” Journal of the American Academy of Child and Adolescent Psychiatry, vol. 53, no. 7, pp. 726–735, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. J. R. Goodhand, F. I. S. Greig, Y. Koodun et al., “Do antidepressants influence the disease course in inflammatory bowel disease? A retrospective case-matched observational study,” Inflammatory Bowel Diseases, vol. 18, no. 7, pp. 1232–1239, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. H. N. Iskandar, B. Cassell, N. Kanuri et al., “Tricyclic antidepressants for management of residual symptoms in inflammatory bowel disease,” Journal of Clinical Gastroenterology, vol. 48, no. 5, pp. 423–429, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. C. Rungoe, E. Langholz, M. Andersson et al., “Changes in medical treatment and surgery rates in inflammatory bowel disease: a nationwide cohort study 1979–2011,” Gut, vol. 63, no. 10, pp. 1607–1616, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. G. C. Nguyen, Z. Nugent, S. Shaw, and C. N. Bernstein, “Outcomes of patients with Crohn's disease improved from 1988 to 2008 and were associated with increased specialist care,” Gastroenterology, vol. 141, no. 1, pp. 90–97, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. A. V. Ramadas, S. Gunesh, G. A. O. Thomas, G. T. Williams, and A. B. Hawthorne, “Natural history of Crohn's disease in a population-based cohort from Cardiff (1986–2003): a study of changes in medical treatment and surgical resection rates,” Gut, vol. 59, no. 9, pp. 1200–1206, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. P. L. Lakatos, P. A. Golovics, G. David et al., “Has there been a change in the natural history of Crohn's disease? Surgical rates and medical management in a population-based inception cohort from Western Hungary between 1977–2009,” American Journal of Gastroenterology, vol. 107, no. 4, pp. 579–588, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. M. W. M. D. Lutgens, M. G. H. van Oijen, G. J. M. G. van der Heijden, F. P. Vleggaar, P. D. Siersema, and B. Oldenburg, “Declining risk of colorectal cancer in inflammatory bowel disease: an updated meta-analysis of population-based cohort studies,” Inflammatory Bowel Diseases, vol. 19, no. 4, pp. 789–799, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Jess, J. Simonsen, K. T. Jorgensen, B. V. Pedersen, N. M. Nielsen, and M. Frisch, “Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years,” Gastroenterology, vol. 143, no. 2, pp. 375–381, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. L. Lakatos, L. S. Kiss, G. David et al., “Incidence, disease phenotype at diagnosis, and early disease course in inflammatory bowel diseases in Western Hungary, 2002–2006,” Inflammatory Bowel Diseases, vol. 17, no. 12, pp. 2558–2565, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Sjöberg, T. Holmström, M. Larsson et al., “Incidence and natural history of ulcerative colitis in the Uppsala Region of Sweden 2005–2009—results from the IBD Cohort of the Uppsala Region (ICURE),” Journal of Crohn's and Colitis, vol. 7, no. 9, pp. e351–e357, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. D. Sjöberg, T. Holmström, M. Larsson et al., “Incidence and clinical course of Crohn's disease during the first year—results from the IBD Cohort of the Uppsala Region (ICURE) of Sweden 2005–2009,” Journal of Crohn's and Colitis, vol. 8, no. 3, pp. 215–222, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. J. P. Buckley, M. D. Kappelman, J. K. Allen, S. A. Van Meter, and S. F. Cook, “The burden of comedication among patients with inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 19, no. 13, pp. 2725–2736, 2013. View at Publisher · View at Google Scholar · View at Scopus
  79. A. Parian and C. Y. Ha, “Older age and steroid use are associated with increasing polypharmacy and potential medication interactions among patients with inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 21, no. 6, pp. 1392–1400, 2015. View at Publisher · View at Google Scholar · View at Scopus
  80. R. K. Cross, K. T. Wilson, and D. G. Binion, “Polypharmacy and Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 21, no. 10, pp. 1211–1216, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. R. K. Cross, K. T. Wilson, and D. G. Binion, “Narcotic use in patients with Crohn's disease,” American Journal of Gastroenterology, vol. 100, no. 10, pp. 2225–2229, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. L. E. Targownik, Z. Nugent, H. Singh, S. Bugden, and C. N. Bernstein, “The prevalence and predictors of opioid use in inflammatory bowel disease: a population-based analysis,” The American Journal of Gastroenterology, vol. 109, no. 10, pp. 1613–1620, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. M. D. Long, E. L. Barnes, H. H. Herfarth, and D. A. Drossman, “Narcotic use for inflammatory bowel disease and risk factors during hospitalization,” Inflammatory Bowel Diseases, vol. 18, no. 5, pp. 869–876, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. A. A. Mikocka-Walus, D. Turnbull, G. Holtmann, and J. M. Andrews, “An integrated model of care for inflammatory bowel disease sufferers in Australia: development and the effects of its implementation,” Inflammatory Bowel Diseases, vol. 18, no. 8, pp. 1573–1581, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. D. Duricova, N. Pedersen, M. Elkjaer, M. Gamborg, P. Munkholm, and T. Jess, “Overall and cause-specific mortality in Crohn's disease: a meta-analysis of population-based studies,” Inflammatory Bowel Diseases, vol. 16, no. 2, pp. 347–353, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Bewtra, L. M. Kaiser, T. Tenhave, and J. D. Lewis, “Crohn's disease and ulcerative colitis are associated with elevated standardized mortality ratios: a meta-analysis,” Inflammatory Bowel Diseases, vol. 19, no. 3, pp. 599–613, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. T. Jess, M. Gamborg, P. Munkholm, and T. I. A. Sørensen, “Overall and cause-specific mortality in ulcerative colitis: meta-analysis of population-based inception cohort studies,” The American Journal of Gastroenterology, vol. 102, no. 3, pp. 609–617, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. C. N. Bernstein, Z. Nugent, L. E. Targownik, H. Singh, and L. M. Lix, “Predictors and risks for death in a population-based study of persons with IBD in Manitoba,” Gut, vol. 64, no. 9, pp. 1403–1411, 2015. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Jess, M. Frisch, and J. Simonsen, “Trends in overall and cause-specific mortality among patients with inflammatory bowel disease from 1982 to 2010,” Clinical Gastroenterology and Hepatology, vol. 11, no. 1, pp. 43–48, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. A. O'toole, P. Walsh, D. Keegan et al., “Mortality in inflammatory bowel disease patients under 65 years of age,” Scandinavian Journal of Gastroenterology, vol. 49, no. 7, pp. 814–819, 2014. View at Publisher · View at Google Scholar · View at Scopus
  91. L. H. Wang, Y. J. Yang, W. C. Cheng, W. Wang, S. Lin, and C. Shieh, “Higher risk for hematological malignancies in inflammatory bowel disease: a nationwide population-based study in Taiwan,” The American Journal of Gastroenterology, vol. 111, no. 9, pp. 1313–1319, 2016. View at Publisher · View at Google Scholar
  92. C. Castaño-Milla, M. Chaparro, and J. P. Gisbert, “Systematic review with meta-analysis: the declining risk of colorectal cancer in ulcerative colitis,” Alimentary Pharmacology and Therapeutics, vol. 39, no. 7, pp. 645–659, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. L. Beaugerie and S. H. Itzkowitz, “Cancers complicating inflammatory bowel disease,” New England Journal of Medicine, vol. 372, no. 15, pp. 1441–1452, 2015. View at Publisher · View at Google Scholar · View at Scopus
  94. A. N. Ananthakrishnan, A. Cagan, T. Cai et al., “Colonoscopy is associated with a reduced risk for colon cancer and mortality in patients with inflammatory bowel diseases,” Clinical Gastroenterology and Hepatology, vol. 13, no. 2, pp. 322.e1–329.e1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. H. Brenner, J. Chang-Claude, C. M. Seiler, A. Rickert, and M. Hoffmeister, “Protection from colorectal cancer after colonoscopy: a population-based, case-control study,” Annals of Internal Medicine, vol. 154, no. 1, pp. 22–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. M. D. Kappelman, D. K. Farkas, M. D. Long et al., “Risk of cancer in patients with inflammatory bowel diseases: a nationwide population-based cohort study with 30 years of follow-up evaluation,” Clinical Gastroenterology and Hepatology, vol. 12, no. 2, pp. 265.e1–273.e1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  97. D. S. Kotlyar, J. D. Lewis, L. Beaugerie et al., “Risk of lymphoma in patients with inflammatory bowel disease treated with azathioprine and 6-mercaptopurine: a meta-analysis,” Clinical Gastroenterology and Hepatology, vol. 13, no. 5, pp. 847–858.e4, 2015. View at Publisher · View at Google Scholar · View at Scopus
  98. J. R. Allegretti, E. L. Barnes, and A. Cameron, “Are patients with inflammatory bowel disease on chronic immunosuppressive therapy at increased risk of cervical high-grade dysplasia/cancer? A meta-analysis,” Inflammatory Bowel Diseases, vol. 21, no. 5, pp. 1089–1097, 2015. View at Publisher · View at Google Scholar · View at Scopus
  99. U. Kopylov, M. Vutcovici, A. Kezouh, E. Seidman, A. Bitton, and W. Afif, “Risk of lymphoma, colorectal and skin cancer in patients with IBD treated with immunomodulators and biologics: A Quebec Claims Database Study,” Inflammatory Bowel Diseases, vol. 21, no. 8, pp. 1847–1853, 2015. View at Publisher · View at Google Scholar · View at Scopus
  100. M. D. Long, C. F. Martin, C. A. Pipkin, H. H. Herfarth, R. S. Sandler, and M. D. Kappelman, “Risk of melanoma and nonmelanoma skin cancer among patients with inflammatory bowel disease,” Gastroenterology, vol. 143, no. 2, pp. 390.e1–399.e1, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. A. D. Frolkis, J. Dykeman, M. E. Negrón et al., “Risk of surgery for inflammatory bowel diseases has decreased over time: a systematic review and meta-analysis of population-based studies,” Gastroenterology, vol. 145, no. 5, pp. 996–1006, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. E. K. Wright, M. A. Kamm, P. De Cruz et al., “Effect of intestinal resection on quality of life in Crohn's disease,” Journal of Crohn's and Colitis, vol. 9, no. 6, pp. 452–462, 2015. View at Google Scholar
  103. G. Cullen, A. O'Toole, D. Keegan, K. Sheahan, J. M. Hyland, and D. P. O'Donoghue, “Long-term clinical results of ileocecal resection for Crohn's disease,” Inflammatory Bowel Diseases, vol. 13, no. 11, pp. 1369–1373, 2007. View at Publisher · View at Google Scholar · View at Scopus
  104. C. Ha, T. A. Ullman, C. A. Siegel, and A. Kornbluth, “Patients enrolled in randomized controlled trials do not represent the inflammatory bowel disease patient population,” Clinical Gastroenterology and Hepatology, vol. 10, no. 9, pp. 1002–1007, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. G. E. Reese, T. Nanidis, C. Borysiewicz, T. Yamamoto, T. Orchard, and P. P. Tekkis, “The effect of smoking after surgery for Crohn's disease: a meta-analysis of observational studies,” International Journal of Colorectal Disease, vol. 23, no. 12, pp. 1213–1221, 2008. View at Publisher · View at Google Scholar · View at Scopus