Immune Checkpoint Inhibitor-Induced Colitis: Diagnosis and Management

Targeted Oncology

Volumn 12, Issue 3, 2017, Pages 301-308

  Prieux Klotz, Caroline ^a   Dior, Marie ^a,b   Damotte, Diane ^a   Dreanic, Johann ^a,b   Brieau, Bertrand ^a,b   Brezault, Catherine ^a,b   Abitbol, Vered ^a   Chaussade, Stanislas ^a,b   Coriat, Romain ^a,b  

^a Institut Cochin   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETORPHAN; ATEZOLIZUMAB; BUDESONIDE; CORTICOSTEROID; IMMUNE CHECKPOINT INHIBITOR; INFLIXIMAB; IPILIMUMAB; METRONIDAZOLE; NIVOLUMAB; PEMBROLIZUMAB; PLACEBO; UNCLASSIFIED DRUG; VANCOMYCIN; MONOCLONAL ANTIBODY; T LYMPHOCYTE RECEPTOR;

ADJUVANT THERAPY; CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; COLON BIOPSY; COLONOSCOPY; COLORECTAL CANCER; DEHYDRATION; DIARRHEA; DRUG DOSE INCREASE; DRUG WITHDRAWAL; ENTEROCOLITIS; GASTROINTESTINAL SYMPTOM; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HISTOPATHOLOGY; HODGKIN DISEASE; HUMAN; ILEUS; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; INTESTINE PERFORATION; KIDNEY CARCINOMA; LUNG CANCER; MELANOMA; MERKEL CELL CARCINOMA; ORAL REHYDRATION THERAPY; OVARY CANCER; PATIENT EDUCATION; PRIORITY JOURNAL; REVIEW; SIGMOIDOSCOPY; SINGLE DRUG DOSE; STOMACH CANCER; TRANSITIONAL CELL CARCINOMA; ADVERSE DRUG REACTION; CHEMICALLY INDUCED; IMMUNOLOGY; IMMUNOTHERAPY; INTERDISCIPLINARY COMMUNICATION; NEOPLASM; PROCEDURES;

ADRENAL CORTEX HORMONES; ANTIBODIES, MONOCLONAL; COLITIS; COSTIMULATORY AND INHIBITORY T-CELL RECEPTORS; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; HUMANS; IMMUNOTHERAPY; INFLIXIMAB; INTERDISCIPLINARY COMMUNICATION; NEOPLASMS;

EID: 85019544439     PISSN: 17762596     EISSN: 1776260X     Source Type: Journal    
DOI: 10.1007/s11523-017-0495-4     Document Type: Review

References (54)

1. Walker LSK, Sansom DM. The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nat Rev Immunol. 2011;11(12):852–63.
2. Munir S, Andersen GH, Svane IM, Andersen MH. The immune checkpoint regulator PD-L1 is a specific target for naturally occurring CD4(+) T cells. Oncoimmunology. 2013;2(4):e23991.
3. Fife BT, Pauken KE, Eagar TN, Obu T, Wu J, Tang Q, et al. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat Immunol. 2009;10(11):1185–92.
4. Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology. 2012;1(8):1223–5.
5. Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–23.
6. Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372(4):320–30.
7. Weber JS, D’Angelo SP, Minor D, Hodi FS, Gutzmer R, Neyns B, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 2015;16(4):375–84.
8. Wolchok JD, Neyns B, Linette G, Negrier S, Lutzky J, Thomas L, et al. Ipilimumab monotherapy in patients with pretreated advanced melanoma: a randomised, double-blind, multicentre, phase 2, dose-ranging study. Lancet Oncol. 2010;11(2):155–64.
9. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372(21):2018–28.
10. Rizvi NA, Mazières J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol. 2015;16(3):257–65.
11. Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, et al. Nivolumab versus Docetaxel in advanced Nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373(17):1627–39.
12. Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WEE, Poddubskaya E, et al. Nivolumab versus Docetaxel in advanced squamous-cell non–small-cell lung cancer. N Engl J Med. 2015;373(2):123–35.
13. Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet. 2016;387(10030):1837–46.
14. Motzer RJ, Rini BI, McDermott DF, Redman BG, Kuzel TM, Harrison MR, et al. Nivolumab for metastatic renal cell carcinoma: results of a randomized phase II trial. J Clin Oncol. 2015;33(13):1430–7.
15. Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, et al. Nivolumab versus Everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1803–13.
16. Sharma P, Callahan MK, Bono P, Kim J, Spiliopoulou P, Calvo E, et al. Nivolumab monotherapy in recurrent metastatic urothelial carcinoma (CheckMate 032): a multicentre, open-label, two-stage, multi-arm, phase 1/2 trial. Lancet Oncol. 2016;17(11):1590–8.
17. Sharma P, Retz M, Siefker-Radtke A, Baron A, Necchi A, Bedke J, et al. Nivolumab in metastatic urothelial carcinoma after platinum therapy (CheckMate 275): a multicentre, single-arm, phase 2 trial. Lancet Oncol. 2017;18(3):312–22.
18. Rexer H. Study on therapy of metastasized or locally advanced urothelial cancer: a phase III randomized clinical trial of pembrolizumab (MK-3475) versus paclitaxel, docetaxel or vinflunine in subjects with recurrent or progressive metastatic urothelial cancer (Keynote 045) - AP 48/15 der AUO. Urol Ausg A. 2015;54(9):1287–90.
19. Ferris RL, Blumenschein G, Fayette J, Guigay J, Colevas AD, Licitra L, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med. 2016;375(19):1856–67.
20. Seiwert TY, Burtness B, Mehra R, Weiss J, Berger R, Eder JP, et al. Safety and clinical activity of pembrolizumab for treatment of recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-012): an open-label, multicentre, phase 1b trial. Lancet Oncol. 2016;17(7):956–65.
21. Muro K, Chung HC, Shankaran V, Geva R, Catenacci D, Gupta S, et al. Pembrolizumab for patients with PD-L1-positive advanced gastric cancer (KEYNOTE-012): a multicentre, open-label, phase 1b trial. Lancet Oncol. 2016;17(6):717–26. doi:10.1016/S1470-2045(16)00175-3.
22. Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015;372(26):2509–20.
23. Hamanishi J, Mandai M, Ikeda T, Minami M, Kawaguchi A, Murayama T, et al. Safety and antitumor activity of anti-PD-1 antibody, Nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol. 2015;33(34):4015–22.
24. Nghiem PT, Bhatia S, Lipson EJ, Kudchadkar RR, Miller NJ, Annamalai L, et al. PD-1 blockade with Pembrolizumab in advanced Merkel-cell carcinoma. N Engl J Med. 2016;374(26):2542–52.
25. Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin’s lymphoma. N Engl J Med. 2015;372(4):311–9.
26. Hofmann L, Forschner A, Loquai C, Goldinger SM, Zimmer L, Ugurel S, et al. Cutaneous, gastrointestinal, hepatic, endocrine, and renal side-effects of anti-PD-1 therapy. Eur J Cancer. 2016;60:190–209.
27. Robert C, Ribas A, Wolchok JD, Hodi FS, Hamid O, Kefford R, et al. Anti-programmed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. Lancet. 2014;384(9948):1109–17.
28. Rittmeyer A, Barlesi F, Waterkamp D, Park K, Ciardiello F, von Pawel J, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet. 2017;389(10066):21–7.
29. Gupta A, De Felice KM, Loftus EV, Khanna S. Systematic review: colitis associated with anti-CTLA-4 therapy. Aliment Pharmacol Ther. 2015;42(4):406–17.
30. Tarhini A. Immune-mediated adverse events associated with Ipilimumab CTLA-4 blockade therapy: the underlying mechanisms and clinical management. Scientifica. 2013;2013:1–19.
31. Eggermont AMM, Chiarion-Sileni V, Grob J-J, Dummer R, Wolchok JD, Schmidt H, et al. Prolonged survival in stage III melanoma with Ipilimumab adjuvant therapy. N Engl J Med. 2016;375(19):1845–55.
32. De Bruyn G. Diarrhoea in adults (acute). BMJ Clin Evid. 2008;4:2008.
33. Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol. 2017.
34. Barnes MJ, Griseri T, Johnson AMF, Young W, Powrie F, Izcue A. CTLA-4 promotes Foxp3 induction and regulatory T cell accumulation in the intestinal lamina propria. Mucosal Immunol. 2013;6(2):324–34.
35. Romano E, Kusio-Kobialka M, Foukas PG, Baumgaertner P, Meyer C, Ballabeni P, et al. Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc Natl Acad Sci U S A. 2015;112(19):6140–5.
36. Rastogi P. Ipilimumab associated colitis: an IpiColitis case series at MedStar Georgetown University Hospital. World J Gastroenterol. 2015;21(14):4373.
37. Maker AV, Phan GQ, Attia P, et al. Tumor regression and autoimmunity in patients treated with cytotoxic T lymphocyte-associated antigen 4 blockade and interleukin 2: a phase I/II study. Ann Surg Oncol. 2005;12(12):1005–16.
38. Naranjo CA, Busto U, Sellers EM, Sandor P, Ruiz I, Roberts EA, et al. A method for estimating the probability of adverse drug reactions. Clin Pharmacol Ther. 1981;30(2):239–45.
39. Spain L, Larkin J. Combination immune checkpoint blockade with ipilimumab and nivolumab in the management of advanced melanoma. Expert Opin Biol Ther. 2016;16(3):389–96.
40. Jain A, Lipson EJ, Sharfman WH, Brant SR, Lazarev MG. Colonic ulcerations may predict steroid-refractory course in patients with ipilimumab-mediated enterocolitis. World J Gastroenterol. 2017;23(11):2023–8.
41. Beswick L, Ye B, van Langenberg DR. Toward an algorithm for the diagnosis and management of CMV in patients with colitis. Inflamm Bowel Dis. 2016;22(12):2966–76.
42. Coriat R, Lecler A, Lamarque D, Deyra J, Roche H, Nizou C, et al. Quality indicators for colonoscopy procedures: a prospective multicentre method for endoscopy units. PLoS ONE. 2012;7(4):e33957.
43. Dignass A, Eliakim R, Magro F, Maaser C, Chowers Y, Geboes K, et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 1: definitions and diagnosis. J Crohns Colitis. 2012;6(10):965–90.
44. Fischbach W, Andresen V, Eberlin M, Mueck T, Layer P. A comprehensive comparison of the efficacy and tolerability of Racecadotril with other treatments of acute diarrhea in adults. Front Med. 2016;3:44.
45. Cheng R, Cooper A, Kench J, Watson G, Bye W, McNeil C, et al. Ipilimumab-induced toxicities and the gastroenterologist. J Gastroenterol Hepatol. 2015;30(4):657–66.
46. Johnston RL, Lutzky J, Chodhry A, Barkin JS. Cytotoxic T-lymphocyte-associated antigen 4 antibody-induced colitis and its management with infliximab. Dig Dis Sci. 2009;54(11):2538–40.
47. Cooley L, Dendle C, Wolf J, Teh BW, Chen SC, Boutlis C, et al. Consensus guidelines for diagnosis, prophylaxis and management of pneumocystis jirovecii pneumonia in patients with haematological and solid malignancies, 2014. Intern Med J. 2014;44(12b):1350–63.
48. O’Connor A, Marples M, Mulatero C, Hamlin J, Ford AC. Ipilimumab-induced colitis: experience from a tertiary referral center. Ther Adv Gastroenterol. 2016;9(4):457–62.
49. Arriola E, Wheater M, Karydis I, Thomas G, Ottensmeier C. Infliximab for IPILIMUMAB-related colitis-letter. Clin Cancer Res. 2015;21(24):5642–3.
50. Champiat S, Lambotte O, Barreau E, Belkhir R, Berdelou A, Carbonnel F, et al. Management of immune checkpoint blockade dysimmune toxicities: a collaborative position paper. Ann Oncol. 2016;27(4):559–74.
51. Weber J, Thompson JA, Hamid O, Minor D, Amin A, Ron I, et al. A randomized, double-blind, placebo-controlled, phase II study comparing the tolerability and efficacy of ipilimumab administered with or without prophylactic budesonide in patients with unresectable stage III or IV melanoma. Clin Cancer Res. 2009;15(17):5591–8.
52. Kato K, Ohkusa T, Terao S, Chiba T, Murakami K, Yanaka A, et al. Adjunct antibiotic combination therapy for steroid-refractory or -dependent ulcerative colitis: an open-label multicentre study. Aliment Pharmacol Ther. 2014;39(9):949–56.
53. Peyrin-Biroulet L, Bouhnik Y, Roblin X, Bonnaud G, Hagège H, Hébuterne X, et al. French national consensus clinical guidelines for the management of ulcerative colitis. Dig Liver Dis. 2016;48(7):726–33.
54. Dignass A, Lindsay JO, Sturm A, Windsor A, Colombel J-F, 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.