Conventional Therapy of Ulcerative Colitis: Corticosteroids

Chapter

Abstract

Corticosteroids are efficacious in patients with active ulcerative colitis, and this, together with their generally low cost, has ensured that they remain an attractive therapeutic option for inducing remission. However, side effects and complications are common, leading to the idea that they are a “necessary evil.” In this chapter, the evidence base for efficacy of various formulations, including oral and topical second-generation corticosteroids, are discussed and complications outlined. Optimal use of corticosteroids (maximizing benefits and minimizing side effects) involves not only the appropriate choice of formulation in specific scenarios, but also sensible management of withdrawal, corticosteroid resistance, and corticosteroid dependence, and institution of strategies to reduce the risks of side effects and complications. The judicious use of corticosteroids should be an integral part of care for all clinicians managing patients with ulcerative colitis.

Keywords

Ulcerative colitis Corticosteroids Hydrocortisone Prednisolone Budesonide Belcomethasone Topical therapy Infection Osteoporosis Neuropsychiatric complications Glucose intolerance 

References

  1. 1.
    Truelove SC, Witts LJ. Cortisone in ulcerative colitis. Br Med J. 1955;2:1041–8.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Edwards FC, Truelove SC. The course and prognosis of ulcerative colitis. Gut. 1963;4:299–315.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    McKay LI, Cidlowski JA. Cross-talk between nuclear factor-kappa B and the steroid hormone receptors: mechanisms of mutual antagonism. Mol Endocrinol. 1998;12:45–56.PubMedCrossRefGoogle Scholar
  4. 4.
    Barnes PJ. How corticosteroids control inflammation: Quintiles Prize Lecture 2005. Br J Pharmacol. 2006;148(3):245–54.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Sandle GI, Hayslett JP, Binder HJ. Effect of glucocorticoids on rectal transport in normal subjects and patients with ulcerative colitis. Gut. 1986;27(3):309–16.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Meyers S, Sachar DB, Goldberg JD, Janowitz HD. Corticotropin versus hydrocortisone in the intravenous treatment of ulcerative colitis. A prospective, randomized, double-blind clinical trial. Gastroenterology. 1983;85(2):351–7.PubMedGoogle Scholar
  7. 7.
    Truelove SC, Witts LJ. Cortisone in ulcerative colitis; preliminary report on a therapeutic trial. Br Med J. 1954;2(4884):375–8.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Hawthorne AB, Record CO, Holdsworth CD, Giaffer MH, Burke DA, Keech ML, et al. Double blind trial of oral fluticasone propionate v prednisolone in the treatment of active ulcerative colitis. Gut. 1993;34(1):125–8.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Lennard-Jones JE, Longmore AJ, Newell AC, Wilson CW, Jones FA. An assessment of prednisone, salazopyrin, and topical hydrocortisone hemisuccinate used as out-patient treatment for ulcerative colitis. Gut. 1960;1:217–22.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Topical 5-aminosalicylic acid versus prednisolone in ulcerative proctosigmoiditis. A randomized, double-blind multicenter trial. Danish 5-ASA Group. Digest Dis Sci. 1987;32(6):598–602.Google Scholar
  11. 11.
    Angus P, Snook JA, Reid M, Jewell DP. Oral fluticasone propionate in active distal ulcerative colitis. Gut. 1992;33(5):711–4.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Lofberg R, Danielsson A, Suhr O, Nilsson A, Schioler R, Nyberg A, et al. Oral budesonide versus prednisolone in patients with active extensive and left-sided ulcerative colitis. Gastroenterology. 1996;110(6):1713–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Gross V, Bunganic I, Belousova EA, Mikhailova TL, Kupcinskas L, Kiudelis G, et al. 3 g mesalazine granules are superior to 9 mg budesonide for achieving remission in active ulcerative colitis: a double-blind, double-dummy, randomised trial. J Crohns Colitis. 2011;5(2):129–38.PubMedCrossRefGoogle Scholar
  14. 14.
    D'Haens GR, Kovacs A, Vergauwe P, Nagy F, Molnar T, Bouhnik Y, et al. Clinical trial: preliminary efficacy and safety study of a new Budesonide-MMX(R) 9 mg extended-release tablets in patients with active left-sided ulcerative colitis. J Crohns Colitis. 2010;4(2):153–60.PubMedCrossRefGoogle Scholar
  15. 15.
    Sandborn WJ, Travis S, Moro L, Jones R, Gautille T, Bagin R, et al. Once-daily budesonide MMX(R) extended-release tablets induce remission in patients with mild to moderate ulcerative colitis: results from the CORE I study. Gastroenterology. 2012;143(5):1218–26.e1–2.Google Scholar
  16. 16.
    Travis SP, Danese S, Kupcinskas L, Alexeeva O, D'Haens G, Gibson PR, et al. Once-daily budesonide MMX in active, mild-to-moderate ulcerative colitis: results from the randomised CORE II study. Gut. 2014;63(3):433–41.PubMedCrossRefGoogle Scholar
  17. 17.
    Bossa F, Latiano A, Rossi L, Magnani M, Palmieri O, Dallapiccola B, et al. Erythrocyte-mediated delivery of dexamethasone in patients with mild-to-moderate ulcerative colitis, refractory to mesalamine: a randomized, controlled study. Am J Gastroenterol. 2008;103(10):2509–16.PubMedCrossRefGoogle Scholar
  18. 18.
    Rizzello F, Gionchetti P, D'Arienzo A, Manguso F, Di Matteo G, Annese V, et al. Oral beclometasone dipropionate in the treatment of active ulcerative colitis: a double-blind placebo-controlled study. Aliment Pharmacol Ther. 2002;16(6):1109–16.PubMedCrossRefGoogle Scholar
  19. 19.
    Van Assche G, Manguso F, Zibellini M, Cabriada Nuno JL, Goldis A, Tkachenko E, et al. Oral prolonged release beclomethasone dipropionate and prednisone in the treatment of active ulcerative colitis: results from a double-blind, randomized, parallel group study. Am J Gastroenterol. 2015;110(5):708–15.PubMedCrossRefGoogle Scholar
  20. 20.
    Rhodes JM, Robinson R, Beales I, Pugh S, Dickinson R, Dronfield M, et al. Clinical trial: oral prednisolone metasulfobenzoate (Predocol) vs. oral prednisolone for active ulcerative colitis. Aliment Pharmacol Ther. 2008;27(3):228–40.PubMedCrossRefGoogle Scholar
  21. 21.
    Hanauer SB, Robinson M, Pruitt R, Lazenby AJ, Persson T, Nilsson LG, et al. Budesonide enema for the treatment of active, distal ulcerative colitis and proctitis: a dose-ranging study. U.S. Budesonide enema study group. Gastroenterology. 1998;115(3):525–32.PubMedCrossRefGoogle Scholar
  22. 22.
    Lindgren S, Lofberg R, Bergholm L, Hellblom M, Carling L, Ung KA, et al. Effect of budesonide enema on remission and relapse rate in distal ulcerative colitis and proctitis. Scand J Gastroenterol. 2002;37(6):705–10.PubMedCrossRefGoogle Scholar
  23. 23.
    Sandborn WJ, Bosworth B, Zakko S, Gordon GL, Clemmons DR, Golden PL, et al. Budesonide foam induces remission in patients with mild to moderate ulcerative proctitis and ulcerative proctosigmoiditis. Gastroenterology. 2015;148(4):740–50.e2.Google Scholar
  24. 24.
    Bansky G, Buhler H, Stamm B, Hacki WH, Buchmann P, Muller J. Treatment of distal ulcerative colitis with beclomethasone enemas: high therapeutic efficacy without endocrine side effects. A prospective, randomized, double-blind trial. Dis Colon Rectum. 1987;30(4):288–92.PubMedCrossRefGoogle Scholar
  25. 25.
    van der Heide H, van den Brandt-Gradel V, Tytgat GN, Endert E, Wiltink EH, Schipper ME, et al. Comparison of beclomethasone dipropionate and prednisolone 21-phosphate enemas in the treatment of ulcerative proctitis. J Clin Gastroenterol. 1988;10(2):169–72.PubMedCrossRefGoogle Scholar
  26. 26.
    Halpern Z, Sold O, Baratz M, Konikoff F, Halak A, Gilat T. A controlled trial of beclomethasone versus betamethasone enemas in distal ulcerative colitis. J Clin Gastroenterol. 1991;13(1):38–41.PubMedCrossRefGoogle Scholar
  27. 27.
    Mulder CJ, Fockens P, Meijer JW, van der Heide H, Wiltink EH, Tytgat GN. Beclomethasone dipropionate (3 mg) versus 5-aminosalicylic acid (2 g) versus the combination of both (3 mg/2 g) as retention enemas in active ulcerative proctitis. Eur J Gastroenterol Hepatol. 1996;8(6):549–53.PubMedCrossRefGoogle Scholar
  28. 28.
    Campieri M, Cottone M, Miglio F, Manenti F, Astegiano M, D'Arienzo A, et al. Beclomethasone dipropionate enemas versus prednisolone sodium phosphate enemas in the treatment of distal ulcerative colitis. Aliment Pharmacol Ther. 1998;12(4):361–6.PubMedCrossRefGoogle Scholar
  29. 29.
    Biancone L, Gionchetti P, Blanco Gdel V, Orlando A, Annese V, Papi C, et al. Beclomethasone dipropionate versus mesalazine in distal ulcerative colitis: a multicenter, randomized, double-blind study. Dig Liver Dis. 2007;39(4):329–37.PubMedCrossRefGoogle Scholar
  30. 30.
    McIntyre PB, Macrae FA, Berghouse L, English J, Lennard-Jones JE. Therapeutic benefits from a poorly absorbed prednisolone enema in distal colitis. Gut. 1985;26(8):822–4.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Riley SA, Gupta I, Mani V. A comparison of sucralfate and prednisolone enemas in the treatment of active distal ulcerative colitis. Scand J Gastroenterol. 1989;24(8):1014–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Cobden I, al-Mardini H, Zaitoun A, Record CO. Is topical therapy necessary in acute distal colitis? Double-blind comparison of high-dose oral mesalazine versus steroid enemas in the treatment of active distal ulcerative colitis. Aliment Pharmacol Ther. 1991;5(5):513–22.PubMedCrossRefGoogle Scholar
  33. 33.
    Mulder CJ, Tytgat GN, Wiltink EH, Houthoff HJ. Comparison of 5-aminosalicylic acid (3 g) and prednisolone phosphate sodium enemas (30 mg) in the treatment of distal ulcerative colitis. A prospective, randomized, double-blind trial. Scand J Gastroenterol. 1988;23(8):1005–8.PubMedCrossRefGoogle Scholar
  34. 34.
    O'Donnell LJ, Arvind AS, Hoang P, Cameron D, Talbot IC, Jewell DP, et al. Double blind, controlled trial of 4-aminosalicylic acid and prednisolone enemas in distal ulcerative colitis. Gut. 1992;33(7):947–9.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Sharma MP, Duphare HV, Dasarathy S. A prospective randomized double blind trial comparing prednisolone and 4-aminosalicylic acid enemas in acute distal ulcerative colitis. J Gastroenterol Hepatol. 1992;7(2):173–7.PubMedCrossRefGoogle Scholar
  36. 36.
    Campieri M, Gionchetti P, Belluzzi A, Brignola C, Migaldi M, Tabanelli GM, et al. Efficacy of 5-aminosalicylic acid enemas versus hydrocortisone enemas in ulcerative colitis. Dig Dis Sci. 1987;32(12 Suppl):67s–70s.PubMedCrossRefGoogle Scholar
  37. 37.
    Bianchi Porro G, Ardizzone S, Petrillo M, Fasoli A, Molteni P, Imbesi V. Low Pentasa dosage versus hydrocortisone in the topical treatment of active ulcerative colitis: a randomized, double-blind study. Am J Gastroenterol. 1995;90(5):736–9.PubMedGoogle Scholar
  38. 38.
    Ford AC, Bernstein CN, Khan KJ, Abreu MT, Marshall JK, Talley NJ, et al. Glucocorticosteroid therapy in inflammatory bowel disease: systematic review and meta-analysis. Am J Gastroenterol. 2011;106(4):590–9.PubMedCrossRefGoogle Scholar
  39. 39.
    Elliott PR, Powell-Tuck J, Gillespie PE, Laidlow JM, Lennard-Jones JE, English J, et al. Prednisolone absorption in acute colitis. Gut. 1980;21(1):49–51.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Baron JH, Connell AM, Kanaghinis TG, Lennard-Jones JE, Jones AF. Out-patient treatment of ulcerative colitis. Comparison between three doses of oral prednisone. Br Med J. 1962;2(5302):441–3.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Powell-Tuck J, Bown RL, Lennard-Jones JE. A comparison of oral prednisolone given as single or multiple daily doses for active proctocolitis. Scand J Gastroenterol. 1978;13(7):833–7.PubMedCrossRefGoogle Scholar
  42. 42.
    Dignass A, Lindsay JO, Sturm A, Windsor A, Colombel JF, Allez M, et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis. Part 2: Current management. J Crohns Colitis. 2012;6(10):991–1030.PubMedCrossRefGoogle Scholar
  43. 43.
    Centre for Drug Evaluation and Research. Pharmacology review. Budesonide modified release capsules. 2001. Available from: http://www.accessdata.fda.gov/drugsatfda_docs/nda/2001/21-324_Entocort_pharmr.pdf. Accessed 20 July 2015.
  44. 44.
    Seow CH, Benchimol EI, Griffiths AM, Otley AR, Steinhart AH. Budesonide for induction of remission in Crohn’s disease. Cochrane Database Syst Rev. 2008;(3):Cd000296.Google Scholar
  45. 45.
    Ferring Pharmaceuticals Ltd. Cortiment 9 mg, prolonged release tablets: summary of product characteristics 2014. Available from: http://www.mhra.gov.uk/home/groups/spcpil/documents/spcpil/con1437715186489.pdf. Accessed 20 July 2015.
  46. 46.
    Steed KP, Hooper G, Ventura P, Musa R, Wilding IR. The in vivo behaviour of a colonic delivery system: a pilot study in man. Int J Pharm. 1994;112(3):199–206.CrossRefGoogle Scholar
  47. 47.
    Fasci Spurio F, Aratari A, Margagnoni G, Doddato MT, Chiesara F, Papi C. Oral beclomethasone dipropionate: a critical review of its use in the management of ulcerative colitis and Crohn’s disease. Curr Clin Pharmacol. 2012;7(2):131–6.PubMedCrossRefGoogle Scholar
  48. 48.
    Campieri M, Adamo S, Valpiani D, D'Arienzo A, D'Albasio G, Pitzalis M, et al. Oral beclometasone dipropionate in the treatment of extensive and left-sided active ulcerative colitis: a multicentre randomised study. Aliment Pharmacol Ther. 2003;17(12):1471–80.PubMedCrossRefGoogle Scholar
  49. 49.
    Ford GA, Oliver PS, Shepherd NA, Wilkinson SP. An Eudragit-coated prednisolone preparation for ulcerative colitis: pharmacokinetics and preliminary therapeutic use. Aliment Pharmacol Ther. 1992;6(1):31–40.PubMedCrossRefGoogle Scholar
  50. 50.
    Bell GD EJ, Spiers C, Nylander D, Hancock JM, Rowland RS. Colonic mucosal concentrations of prednisolone following oral administration of a novel formulation of prednisolone metasulphobenzoate (Predocol) [Abstract]. Gut. 2000;(Suppl 46):T29.Google Scholar
  51. 51.
    Manguso F, Balzano A. Meta-analysis: the efficacy of rectal beclomethasone dipropionate vs. 5-aminosalicylic acid in mild to moderate distal ulcerative colitis. Aliment Pharmacol Ther. 2007;26(1):21–9.PubMedCrossRefGoogle Scholar
  52. 52.
    Lemann M, Galian A, Rutgeerts P, Van Heuverzwijn R, Cortot A, Viteau JM, et al. Comparison of budesonide and 5-aminosalicylic acid enemas in active distal ulcerative colitis. Aliment Pharmacol Ther. 1995;9(5):557–62.PubMedCrossRefGoogle Scholar
  53. 53.
    Farmer RG, Schumacher OP. Treatment of ulcerative colitis with hydrocortisone enemas. Comparison of absorption and clinical response with hydrocortisone alcohol and hydrocortisone acetate. Am J Gastroenterol. 1970;54(3):229–36.PubMedGoogle Scholar
  54. 54.
    Mollmann H, Barth J, Mollmann C, Tunn S, Krieg M, Derendorf H. Pharmacokinetics and rectal bioavailability of hydrocortisone acetate. J Pharm Sci. 1991;80(9):835–6.PubMedCrossRefGoogle Scholar
  55. 55.
    Lima JJ, Giller J, Mackichan JJ, Jusko WJ. Bioavailability of hydrocortisone retention enemas in normal subjects. Am J Gastroenterol. 1980;73(3):232–7.PubMedGoogle Scholar
  56. 56.
    Petitjean O, Wendling JL, Tod M, Louchahi K, Nicolas P, Perret G, et al. Pharmacokinetics and absolute rectal bioavailability of hydrocortisone acetate in distal colitis. Aliment Pharmacol Ther. 1992;6(3):351–7.PubMedCrossRefGoogle Scholar
  57. 57.
    Tarpila S, Turunen U, Seppala K, Aukee S, Pikkarainen P, Elomaa I, et al. Budesonide enema in active haemorrhagic proctitis—a controlled trial against hydrocortisone foam enema. Aliment Pharmacol Ther. 1994;8(6):591–5.PubMedCrossRefGoogle Scholar
  58. 58.
    Lofberg R, Ostergaard Thomsen O, Langholz E, Schioler R, Danielsson A, Suhr O, et al. Budesonide versus prednisolone retention enemas in active distal ulcerative colitis. Aliment Pharmacol Ther. 1994;8(6):623–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Gross V, Bar-Meir S, Lavy A, Mickisch O, Tulassay Z, Pronai L, et al. Budesonide foam versus budesonide enema in active ulcerative proctitis and proctosigmoiditis. Aliment Pharmacol Ther. 2006;23(2):303–12.PubMedCrossRefGoogle Scholar
  60. 60.
    Turner D, Walsh CM, Steinhart AH, Griffiths AM. Response to corticosteroids in severe ulcerative colitis: a systematic review of the literature and a meta-regression. Clin Gastroenterol Hepatol. 2007;5(1):103–10.PubMedCrossRefGoogle Scholar
  61. 61.
    Travis SP, Farrant JM, Ricketts C, Nolan DJ, Mortensen NM, Kettlewell MG, et al. Predicting outcome in severe ulcerative colitis. Gut. 1996;38(6):905–10.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Travis S, Satsangi J, Lémann M. Predicting the need for colectomy in severe ulcerative colitis: a critical appraisal of clinical parameters and currently available biomarkers. Gut. 2011;60(1):3–9.PubMedCrossRefGoogle Scholar
  63. 63.
    Truelove SC, Witts LJ. Cortisone and corticotrophin in ulcerative colitis. Br Med J. 1959;1(5119):387–94.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Lennard-Jones JE, Misiewicz JJ, Connell AM, Baron JH, Jones FA. Prednisone as maintenance treatment for ulcerative colitis in remission. Lancet. 1965;1(7378):188–9.PubMedCrossRefGoogle Scholar
  65. 65.
    Powell-Tuck J, Bown RL, Chambers TJ, Lennard-Jones JE. A controlled trial of alternate day prednisolone as a maintenance treatment for ulcerative colitis in remission. Digestion. 1981;22(5):263–70.PubMedCrossRefGoogle Scholar
  66. 66.
    Lichtenstein GR, Abreu MT, Cohen R, Tremaine W. American Gastroenterological Association Institute technical review on corticosteroids, immunomodulators, and infliximab in inflammatory bowel disease. Gastroenterology. 2006;130(3):940–87.PubMedCrossRefGoogle Scholar
  67. 67.
    Keenan GF. Management of complications of glucocorticoid therapy. Clin Chest Med. 1997;18(3):507–20.PubMedCrossRefGoogle Scholar
  68. 68.
    Faubion Jr WA, Loftus Jr EV, Harmsen WS, Zinsmeister AR, Sandborn WJ. The natural history of corticosteroid therapy for inflammatory bowel disease: a population-based study. Gastroenterology. 2001;121(2):255–60.PubMedCrossRefGoogle Scholar
  69. 69.
    Chen HL, Li LR. Glucocorticoid receptor gene polymorphisms and glucocorticoid resistance in inflammatory bowel disease: a meta-analysis. Dig Dis Sci. 2012;57(12):3065–75.PubMedCrossRefGoogle Scholar
  70. 70.
    Franchimont D, Martens H, Hagelstein MT, Louis E, Dewe W, Chrousos GP, et al. Tumor necrosis factor alpha decreases, and interleukin-10 increases, the sensitivity of human monocytes to dexamethasone: potential regulation of the glucocorticoid receptor. J Clin Endocr Metab. 1999;84(8):2834–9.PubMedGoogle Scholar
  71. 71.
    Ishiguro Y. Mucosal proinflammatory cytokine production correlates with endoscopic activity of ulcerative colitis. J Gastroenterol. 1999;34(1):66–74.PubMedCrossRefGoogle Scholar
  72. 72.
    Jarnerot G, Hertervig E, Friis-Liby I, Blomquist L, Karlen P, Granno C, et al. Infliximab as rescue therapy in severe to moderately severe ulcerative colitis: a randomized, placebo-controlled study. Gastroenterology. 2005;128(7):1805–11.PubMedCrossRefGoogle Scholar
  73. 73.
    Lichtiger S, Present DH, Kornbluth A, Gelernt I, Bauer J, Galler G, et al. Cyclosporine in severe ulcerative colitis refractory to steroid therapy. N Engl J Med. 1994;330(26):1841–5.PubMedCrossRefGoogle Scholar
  74. 74.
    Chow DK, Leong RW. The use of tacrolimus in the treatment of inflammatory bowel disease. Expert Opin Drug Saf. 2007;6(5):479–85.PubMedCrossRefGoogle Scholar
  75. 75.
    Sands BE, Sandborn WJ, Creed TJ, Dayan CM, Dhanda AD, Van Assche GA, et al. Basiliximab does not increase efficacy of corticosteroids in patients with steroid-refractory ulcerative colitis. Gastroenterology. 2012;143(2):356–64.e1.Google Scholar
  76. 76.
    Beattie RM, Nicholls SW, Domizio P, Williams CB, Walker-Smith JA. Endoscopic assessment of the colonic response to corticosteroids in children with ulcerative colitis. J Pediatr Gastroenterol Nutr. 1996;22(4):373–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Turner D, Levine A, Escher JC, Griffiths AM, Russell RK, Dignass A, et al. Management of pediatric ulcerative colitis: joint ECCO and ESPGHAN evidence-based consensus guidelines. J Pediatr Gastroenterol Nutr. 2012;55(3):340–61.PubMedCrossRefGoogle Scholar
  78. 78.
    Jakobsen C, Bartek Jr J, Wewer V, Vind I, Munkholm P, Groen R, et al. Differences in phenotype and disease course in adult and pediatric inflammatory bowel disease—a population-based study. Aliment Pharmacol Ther. 2011;34(10):1217–24.PubMedCrossRefGoogle Scholar
  79. 79.
    Rocha R, Santana GO, Almeida N, Lyra AC. Analysis of fat and muscle mass in patients with inflammatory bowel disease during remission and active phase. Br J Nutr. 2009;101(5):676–9.PubMedCrossRefGoogle Scholar
  80. 80.
    Hokken-Koelega AC, Stijnen T, de Muinck Keizer-Schrama SM, Blum WF, Drop SL. Levels of growth hormone, insulin-like growth factor-I (IGF-I) and -II, IGF-binding protein-1 and -3, and cortisol in prednisone-treated children with growth retardation after renal transplantation. J Clin Endocr Metab. 1993;77(4):932–8.PubMedGoogle Scholar
  81. 81.
    Mushtaq T, Farquharson C, Seawright E, Ahmed SF. Glucocorticoid effects on chondrogenesis, differentiation and apoptosis in the murine ATDC5 chondrocyte cell line. J Endocrinol. 2002;175(3):705–13.PubMedCrossRefGoogle Scholar
  82. 82.
    Uchida K, Araki T, Toiyama Y, Yoshiyama S, Inoue M, Ikeuchi H, et al. Preoperative steroid-related complications in Japanese pediatric patients with ulcerative colitis. Dis Colon Rectum. 2006;49(1):74–9.PubMedCrossRefGoogle Scholar
  83. 83.
    Gurwitz JH, Bohn RL, Glynn RJ, Monane M, Mogun H, Avorn J. Glucocorticoids and the risk for initiation of hypoglycemic therapy. Arch Intern Med. 1994;154(1):97–101.PubMedCrossRefGoogle Scholar
  84. 84.
    Clore JN, Thurby-Hay L. Glucocorticoid-induced hyperglycemia. Endocr Pract. 2009;15(5):469–74.PubMedCrossRefGoogle Scholar
  85. 85.
    Clyburn EB, DiPette DJ. Hypertension induced by drugs and other substances. Semin Nephrol. 1995;15(2):72–86.PubMedGoogle Scholar
  86. 86.
    Hulter HN, Licht JH, Bonner Jr EL, Glynn RD, Sebastian A. Effects of glucocorticoid steroids on renal and systemic acid-base metabolism. Am J Physiol. 1980;239(1):F30–43.PubMedGoogle Scholar
  87. 87.
    Nashel DJ. Is atherosclerosis a complication of long-term corticosteroid treatment? Am J Med. 1986;80(5):925–9.PubMedCrossRefGoogle Scholar
  88. 88.
    Peckett AJ, Wright DC, Riddell MC. The effects of glucocorticoids on adipose tissue lipid metabolism. Metabolism. 2011;60(11):1500–10.PubMedCrossRefGoogle Scholar
  89. 89.
    Bolanos SH, Khan DA, Hanczyc M, Bauer MS, Dhanani N, Brown ES. Assessment of mood states in patients receiving long-term corticosteroid therapy and in controls with patient-rated and clinician-rated scales. Ann Allerg Asthma Immunol. 2004;92(5):500–5.CrossRefGoogle Scholar
  90. 90.
    Lewis DA, Smith RE. Steroid-induced psychiatric syndromes. A report of 14 cases and a review of the literature. J Affect Disorder. 1983;5(4):319–32.CrossRefGoogle Scholar
  91. 91.
    West S, Kenedi C. Strategies to prevent the neuropsychiatric side-effects of corticosteroids: a case report and review of the literature. Curr Opin Organ Transplant. 2014;19(2):201–8.PubMedCrossRefGoogle Scholar
  92. 92.
    Lichtenstein GR, Feagan BG, Cohen RD, Salzberg BA, Diamond RH, Price S, et al. Serious infection and mortality in patients with Crohn’s disease: more than 5 years of follow-up in the TREAT registry. Am J Gastroenterol. 2012;107(9):1409–22.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Toruner M, Loftus Jr EV, Harmsen WS, Zinsmeister AR, Orenstein R, Sandborn WJ, et al. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology. 2008;134(4):929–36.PubMedCrossRefGoogle Scholar
  94. 94.
    Subramanian V, Saxena S, Kang JY, Pollok RC. Preoperative steroid use and risk of postoperative complications in patients with inflammatory bowel disease undergoing abdominal surgery. Am J Gastroenterol. 2008;103(9):2373–81.PubMedCrossRefGoogle Scholar
  95. 95.
    Stuck AE, Minder CE, Frey FJ. Risk of infectious complications in patients taking glucocorticosteroids. Rev Infect Dis. 1989;11(6):954–63.PubMedCrossRefGoogle Scholar
  96. 96.
    Brassard P, Bitton A, Suissa A, Sinyavskaya L, Patenaude V, Suissa S. Oral corticosteroids and the risk of serious infections in patients with elderly-onset inflammatory bowel diseases. Am J Gastroenterol. 2014;109(11):1795–802. quiz 803.PubMedCrossRefGoogle Scholar
  97. 97.
    Ananthakrishnan AN, Cagan A, Cai T, Gainer VS, Shaw SY, Churchill S, et al. Diabetes and the risk of infections with immunomodulator therapy in inflammatory bowel diseases. Aliment Pharmacol Ther. 2015;41(11):1141–8.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Schneeweiss S, Korzenik J, Solomon DH, Canning C, Lee J, Bressler B. Infliximab and other immunomodulating drugs in patients with inflammatory bowel disease and the risk of serious bacterial infections. Aliment Pharmacol Ther. 2009;30(3):253–64.PubMedCrossRefGoogle Scholar
  99. 99.
    Long MD, Farraye FA, Okafor PN, Martin C, Sandler RS, Kappelman MD. Increased risk of Pneumocystis jirovecii pneumonia among patients with inflammatory bowel disease. Inflamm Bowel Dis. 2013;19(5):1018–24.PubMedCrossRefGoogle Scholar
  100. 100.
    Rahier JF, Magro F, Abreu C, Armuzzi A, Ben-Horin S, Chowers Y, et al. Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohns Colitis. 2014;8(6):443–68.PubMedCrossRefGoogle Scholar
  101. 101.
    Matsuoka K, Iwao Y, Mori T, Sakuraba A, Yajima T, Hisamatsu T, et al. Cytomegalovirus is frequently reactivated and disappears without antiviral agents in ulcerative colitis patients. Am J Gastroenterol. 2007;102(2):331–7.PubMedCrossRefGoogle Scholar
  102. 102.
    Sager K, Alam S, Bond A, Chinnappan L, Probert CS. Review article: cytomegalovirus and inflammatory bowel disease. Aliment Pharmacol Ther. 2015;41(8):725–33.PubMedCrossRefGoogle Scholar
  103. 103.
    Roblin X, Pillet S, Oussalah A, Berthelot P, Del Tedesco E, Phelip JM, et al. Cytomegalovirus load in inflamed intestinal tissue is predictive of resistance to immunosuppressive therapy in ulcerative colitis. Am J Gastroenterol. 2011;106(11):2001–8.PubMedCrossRefGoogle Scholar
  104. 104.
    D'Ovidio V, Vernia P, Gentile G, Capobianchi A, Marcheggiano A, Viscido A, et al. Cytomegalovirus infection in inflammatory bowel disease patients undergoing anti-TNFalpha therapy. J Clin Virol. 2008;43(2):180–3.PubMedCrossRefGoogle Scholar
  105. 105.
    Criscuoli V, Mocciaro F, Orlando A, Rizzuto MR, Renda MC, Cottone M. Cytomegalovirus disappearance after treatment for refractory ulcerative colitis in 2 patients treated with infliximab and 1 patient with leukapheresis. Inflamm Bowel Dis. 2009;15(6):810–1.PubMedCrossRefGoogle Scholar
  106. 106.
    Nakase H, Honzawa Y, Toyonaga T, Yamada S, Minami N, Yoshino T, et al. Diagnosis and treatment of ulcerative colitis with cytomegalovirus infection: importance of controlling mucosal inflammation to prevent cytomegalovirus reactivation. Intest Res. 2014;12(1):5–11.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med. 2001;345(15):1098–104.PubMedCrossRefGoogle Scholar
  108. 108.
    Belard E, Semb S, Ruhwald M, Werlinrud AM, Soborg B, Jensen FK, et al. Prednisolone treatment affects the performance of the QuantiFERON gold in-tube test and the tuberculin skin test in patients with autoimmune disorders screened for latent tuberculosis infection. Inflamm Bowel Dis. 2011;17(11):2340–9.PubMedCrossRefGoogle Scholar
  109. 109.
    Tur-Kaspa R, Burk RD, Shaul Y, Shafritz DA. Hepatitis B virus DNA contains a glucocorticoid-responsive element. Proc Natl Acad Sci U S A. 1986;83(6):1627–31.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Park SH, Yang SK, Lim YS, Shim JH, Yang DH, Jung KW, et al. Clinical courses of chronic hepatitis B virus infection and inflammatory bowel disease in patients with both diseases. Inflamm Bowel Dis. 2012;18(11):2004–10.PubMedCrossRefGoogle Scholar
  111. 111.
    EASL clinical practice guidelines: management of chronic hepatitis B virus infection. J Hepatol. 2012;57(1):167–85.Google Scholar
  112. 112.
    Loras C, Gisbert JP, Minguez M, Merino O, Bujanda L, Saro C, et al. Liver dysfunction related to hepatitis B and C in patients with inflammatory bowel disease treated with immunosuppressive therapy. Gut. 2010;59(10):1340–6.PubMedCrossRefGoogle Scholar
  113. 113.
    General recommendations on immunization—recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recommendations and reports: morbidity and mortality weekly report. Centers for Disease Control. 2011;60(2):1–64. http://www.cdc.gov/mmwr/preview/mmwrhtml/rr6002a1.htm?s_cid=rr6002a1_w. Accessed 20 July 2015.
  114. 114.
    Rubin LG, Levin MJ, Ljungman P, Davies EG, Avery R, Tomblyn M, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014;58(3):309–18.PubMedCrossRefGoogle Scholar
  115. 115.
    Heijstek MW, Ott de Bruin LM, Bijl M, Borrow R, van der Klis F, Kone-Paut I, et al. EULAR recommendations for vaccination in pediatric patients with rheumatic diseases. Ann Rheum Dis. 2011;70(10):1704–12.PubMedCrossRefGoogle Scholar
  116. 116.
    Tigas S, Tsatsoulis A. Endocrine and metabolic manifestations in inflammatory bowel disease. Ann Gastroenterol. 2012;25(1):37–44.PubMedPubMedCentralGoogle Scholar
  117. 117.
    Sylvester FA, Wyzga N, Hyams JS, Davis PM, Lerer T, Vance K, et al. Natural history of bone metabolism and bone mineral density in children with inflammatory bowel disease. Inflamm Bowel Dis. 2007;13(1):42–50.PubMedCrossRefGoogle Scholar
  118. 118.
    den Uyl D, Bultink IEM, Lems WF. Advances in glucocorticoid-induced osteoporosis. Curr Rheumatol Rep. 2011;13(3):233–40.CrossRefGoogle Scholar
  119. 119.
    Tannirandorn P, Epstein S. Drug-induced bone loss. Osteoporosis Int. 2000;11(8):637–59.CrossRefGoogle Scholar
  120. 120.
    Adachi JD, Rostom A. Metabolic bone disease in adults with inflammatory bowel disease. Inflamm Bowel Dis. 1999;5(3):200–11.PubMedCrossRefGoogle Scholar
  121. 121.
    Homik J, Suarez-Almazor ME, Shea B, Cranney A, Wells G, Tugwell P. Calcium and vitamin D for corticosteroid-induced osteoporosis. Cochrane Database Syst Rev. 2000;(2):Cd000952.Google Scholar
  122. 122.
    Freeman HJ, Freeman KJ. Prevalence rates and an evaluation of reported risk factors for osteonecrosis (avascular necrosis) in Crohn’s disease. Can J Gastroenterol. 2000;14(2):138–43.PubMedCrossRefGoogle Scholar
  123. 123.
    Vakil N, Sparberg M. Steroid-related osteonecrosis in inflammatory bowel disease. Gastroenterology. 1989;96(1):62–7.PubMedCrossRefGoogle Scholar
  124. 124.
    Klingenstein G, Levy RN, Kornbluth A, Shah AK, Present DH. Inflammatory bowel disease related osteonecrosis: report of a large series with a review of the literature. Aliment Pharmacol Ther. 2005;21(3):243–9.PubMedCrossRefGoogle Scholar
  125. 125.
    Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353(23):2462–76.PubMedCrossRefGoogle Scholar
  126. 126.
    Panaccione R, Ghosh S, Middleton S, Marquez JR, Scott BB, Flint L, et al. Combination therapy with infliximab and azathioprine is superior to monotherapy with either agent in ulcerative colitis. Gastroenterology. 2014;146(2):392–400.e3.Google Scholar
  127. 127.
    Sacco R, Romano A, Mazzoni A, Bertini M, Federici G, Metrangolo S, et al. Granulocytapheresis in steroid-dependent and steroid-resistant patients with inflammatory bowel disease: a prospective observational study. J Crohns Colitis. 2013;7(12):e692–7.PubMedCrossRefGoogle Scholar
  128. 128.
    Bossa F, Annese V, Valvano MR, Latiano A, Martino G, Rossi L, et al. Erythrocytes-mediated delivery of dexamethasone 21-phosphate in steroid-dependent ulcerative colitis: a randomized, double-blind Sham-controlled study. Inflamm Bowel Dis. 2013;19(9):1872–9.PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of GastroenterologyThe Alfred Hospital and Monash UniversityMelbourneAustralia

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