Immune checkpoint inhibitor colitis: the flip side of the wonder drugs

Virchows Archiv

Volumn 472, Issue 1, 2018, Pages 125-133

  Assarzadegan, Naziheh ^a   Montgomery, Elizabeth ^b   Anders, Robert A ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

Colitis; Immune checkpoint inhibitors; PD L1

Indexed keywords

IDELALISIB; IMMUNOMODULATING AGENT; IPILIMUMAB; NIVOLUMAB; PEMBROLIZUMAB; ANTINEOPLASTIC AGENT;

ARTICLE; CLINICAL FEATURE; COLITIS; DRUG MECHANISM; ENDOSCOPY; HISTOLOGY; HUMAN; PRIORITY JOURNAL; SYSTEMATIC REVIEW (TOPIC); CHEMICALLY INDUCED;

ANTINEOPLASTIC AGENTS; COLITIS; HUMANS;

EID: 85034059125     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-017-2267-z     Document Type: Article

References (41)

1. Kyi C, Postow MA (2014) Checkpoint blocking antibodies in cancer immunotherapy. FEBS Lett 588(2):368–376. https://doi.org/10.1016/j.febslet.2013.10.015
2. Dolan DE, Gupta S (2014) PD-1 pathway inhibitors: changing the landscape of cancer immunotherapy. Cancer Control 21(3):231–237. https://doi.org/10.1177/107327481402100308
3. Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D, Biedrzycki B, Donehower RC, Zaheer A, Fisher GA, Crocenzi TS, Lee JJ, Duffy SM, Goldberg RM, de la Chapelle A, Koshiji M, Bhaijee F, Huebner T, Hruban RH, Wood LD, Cuka N, Pardoll DM, Papadopoulos N, Kinzler KW, Zhou S, Cornish TC, Taube JM, Anders RA, Eshleman JR, Vogelstein B, Diaz l Jr et al (2015) PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med 372(26):2509–2520. https://doi.org/10.1056/NEJMoa1500596
4. Topalian SL, Taube JM, Anders RA, Pardoll DM (2016) Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer 16(5):275–287. https://doi.org/10.1038/nrc.2016.36
5. Furman RR, Sharman JP, Coutre SE, Cheson BD, Pagel JM, Hillmen P, Barrientos JC, Zelenetz AD, Kipps TJ, Flinn I, Ghia P, Eradat H, Ervin T, Lamanna N, Coiffier B, Pettitt AR, Ma S, Stilgenbauer S, Cramer P, Aiello M, Johnson DM, Miller LL, Li D, Jahn TM, Dansey RD, Hallek M, O’Brien SM (2014) Idelalisib and rituximab in relapsed chronic lymphocytic leukemia. N Engl J Med 370(11):997–1007. https://doi.org/10.1056/NEJMoa1315226
6. Naidoo J, Page DB, Li BT, Connell LC, Schindler K, Lacouture ME, Postow MA, Wolchok JD (2016) Toxicities of the anti-PD-1 and anti-PD-L1 immune checkpoint antibodies. Ann Oncol 27(7):1362. https://doi.org/10.1093/annonc/mdw141
7. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, Carcereny E, Ahn MJ, Felip E, Lee JS, Hellmann MD, Hamid O, Goldman JW, Soria JC, Dolled-Filhart M, Rutledge RZ, Zhang J, Lunceford JK, Rangwala R, Lubiniecki GM, Roach C, Emancipator K, Gandhi L, KEYNOTE-001 Investigators et al (2015) Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 372(21):2018–2028. https://doi.org/10.1056/NEJMoa1501824
8. Michot JM, Bigenwald C, Champiat S, Collins M, Carbonnel F, Postel-Vinay S, Berdelou A, Varga A, Bahleda R, Hollebecque A, Massard C, Fuerea A, Ribrag V, Gazzah A, Armand JP, Amellal N, Angevin E, Noel N, Boutros C, Mateus C, Robert C, Soria JC, Marabelle A, Lambotte O et al (2016) Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer 54:139–148. https://doi.org/10.1016/j.ejca.2015.11.016
9. Mitchel KA, Kluger H, Sznol M, Hartman DJ (2013) Ipilimumab-induced perforating colitis. J Clin Gastroenterol 47(9):781–785. https://doi.org/10.1097/MCG.0b013e31828f1d51
10. Johnson DB, Sullivan RJ, Ott PA, Carlino MS, Khushalani NI, Ye F, Guminski A, Puzanov I, Lawrence DP, Buchbinder EI, Mudigonda T, Spencer K, Bender C, Lee J, Kaufman HL, Menzies AM, Hassel JC, Mehnert JM, Sosman JA, Long GV, Clark JI (2016) Ipilimumab therapy in patients with advanced melanoma and preexisting autoimmune disorders. JAMA Oncol 2(2):234–240. https://doi.org/10.1001/jamaoncol.2015.4368
11. Chen JH, Pezhouh MK, Lauwers GY, Masia R (2017) Histopathologic features of colitis due to immunotherapy with anti-PD-1 antibodies. Am J Surg Pathol 41(5):643–654. https://doi.org/10.1097/PAS.0000000000000829
12. Oble DA, Mino-Kenudson M, Goldsmith J, Hodi FS, Seliem RM, Dranoff G, Mihm M, Hasserjian R, Lauwers GY (2008) α-CTLA-4 mAb-associated panenteritis: a histologic and immunohistochemical analysis. Am J Surg Pathol 32(8):1130–1137. https://doi.org/10.1097/PAS.0b013e31817150e3
13. Gupta A, De Felice KM, Loftus EV, Khanna S (2015) Systematic review: colitis associated with anti-CTLA-4 therapy. Aliment Pharmacol Ther 42(4):406–417. https://doi.org/10.1111/apt.13281
14. Weidner A-S, Panarelli NC, Geyer JT, Bhavsar EB, Furman RR, Leonard JP, Jessurun J, Yantiss RK (2015) Idelalisib-associated colitis: histologic findings in 14 patients. Am J Surg Pathol 39(12):1661–1667. https://doi.org/10.1097/PAS.0000000000000522
15. Gonzalez RS, Salaria SN, Bohannon CD, Huber AR, Feely MM, Shi C (2017) PD-1 inhibitor gastroenterocolitis: case series and appraisal of ‘immunomodulatory gastroenterocolitis’. Histopathology 70(4):558–567. https://doi.org/10.1111/his.13118
16. Andrade RJ, Lucena MI, Fernandez MC, Pelaez G, Pachkoria K, Garcia-Ruiz E, Garcia-Munoz B, Gonzalez-Grande R, Pizarro A, Duran JA, Jimenez M, Rodrigo L, Romero-Gomez M, Navarro JM, Planas R, Costa J, Borras A, Soler A, Salmeron J, Martin-Vivaldi R (2005) Drug-induced liver injury: an analysis of 461 incidences submitted to the Spanish registry over a 10-year period. Gastroenterology 129(2):512–521. https://doi.org/10.1016/j.gastro.2005.05.006
17. Hofmann L, Forschner A, Loquai C, Goldinger SM, Zimmer L, Ugurel S, Schmidgen MI, Gutzmer R, Utikal JS, Goppner D, Hassel JC, Meier F, Tietze JK, Thomas I, Weishaupt C, Leverkus M, Wahl R, Dietrich U, Garbe C, Kirchberger MC, Eigentler T, Berking C, Gesierich A, Krackhardt AM, Schadendorf D, Schuler G, Dummer R, Heinzerling LM (2016) Cutaneous, gastrointestinal, hepatic, endocrine, and renal side-effects of anti-PD-1 therapy. Eur J Cancer 60:190–209. https://doi.org/10.1016/j.ejca.2016.02.025
18. Weber JS, Dummer R, de Pril V, Lebbe C, Hodi FS (2013) Patterns of onset and resolution of immune-related adverse events of special interest with ipilimumab: detailed safety analysis from a phase 3 trial in patients with advanced melanoma. Cancer 119(9):1675–1682. https://doi.org/10.1002/cncr.27969
19. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbe C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711–723. https://doi.org/10.1056/NEJMoa1003466
20. Linardou H, Gogas H (2016) Toxicity management of immunotherapy for patients with metastatic melanoma. Ann Transl Med 4(14):272. 10.21037/atm.2016.07.10
21. Wolchok JD, Neyns B, Linette G, Negrier S, Lutzky J, Thomas L, Waterfield W, Schadendorf D, Smylie M, Guthrie T Jr, Grob JJ, Chesney J, Chin K, Chen K, Hoos A, O'Day SJ, Lebbe C (2010) Ipilimumab monotherapy in patients with pretreated advanced melanoma: a randomised, double-blind, multicentre, phase 2, dose-ranging study. Lancet Oncol 11(2):155–164. https://doi.org/10.1016/S1470-2045(09)70334-1
22. Villadolid J, Amin A (2015) Immune checkpoint inhibitors in clinical practice: update on management of immune-related toxicities. Transl Lung Cancer Res 4(5):560–575. https://doi.org/10.3978/j.issn.2218-6751.2015.06.06
23. Louie CY, DiMaio MA, Matsukuma KE, Coutre SE, Berry GJ, Longacre TA (2015) Idelalisib-associated enterocolitis: Clinicopathologic features and distinction from other enterocolitides. Am J Surg Pathol 39(12):1653–1660. https://doi.org/10.1097/PAS.0000000000000525
24. McDermott DF, Atkins MB (2013) PD-1 as a potential target in cancer therapy. Cancer Med 2(5):662–673. https://doi.org/10.1002/cam4.106
25. Azuma T, Yao S, Zhu G, Flies AS, Flies SJ, Chen L (2008) B7-H1 is a ubiquitous antiapoptotic receptor on cancer cells. Blood 111(7):3635–3643. https://doi.org/10.1182/blood-2007-11-123141
26. Korman AJ, Peggs KS, Allison JP (2006) Checkpoint blockade in cancer immunotherapy. Adv Immunol 90:297–339. https://doi.org/10.1016/S0065-2776(06)90008-X
27. West NR, Powrie F (2015) Immunotherapy not working? Check your microbiota. Cancer Cell 28(6):687–689. https://doi.org/10.1016/j.ccell.2015.11.010
28. Vanhaesebroeck B, Welham MJ, Kotani K, Stein R, Warne PH, Zvelebil MJ, Higashi K, Volinia S, Downward J, Waterfield MD et al (1997) P110delta, a novel phosphoinositide 3-kinase in leukocytes. Proc Natl Acad Sci U S A 94(9):4330–4335. https://doi.org/10.1073/pnas.94.9.4330
29. Hude I, Sasse S, Engert A, Bröckelmann PJ (2017) The emerging role of immune checkpoint inhibition in malignant lymphoma. Haematologica 102(1):30–42. https://doi.org/10.3324/haematol.2016.150656
30. Lord JD, Hackman RC, Moklebust A, Thompson JA, Higano CS, Chielens D, Steinbach G, McDonald GB et al (2010) Refractory colitis following anti-CTLA4 antibody therapy: analysis of mucosal FOXP3+ T cells. Dig Dis Sci 55(5):1396–1405. https://doi.org/10.1007/s10620-009-0839-8
31. Verschuren EC, van den Eertwegh AJ, Wonders J, Slangen RM, van Delft F, van Bodegraven A, Neefjes-Borst A, de Boer NK et al (2016) Clinical, endoscopic, and histologic characteristics of ipilimumab-associated colitis. Clin Gastroenterol Hepatol 14(6):836–842. https://doi.org/10.1016/j.cgh.2015.12.028
32. Bavi P, Butler M, Serra S, Chetty R (2017) Immune modulator-induced changes in the gastrointestinal tract. Histopathology 71(3):494–496. https://doi.org/10.1111/his.13224
33. Baroudjian B, Lourenco N, Pages C, Chami I, Maillet M, Bertheau P, Bagot M, Gornet JM, Lebbe C, Allez M (2016) Anti-PD1-induced collagenous colitis in a melanoma patient. Melanoma Res 26(3):308–311. https://doi.org/10.1097/CMR.0000000000000252
34. Marginean EC (2016) The ever-changing landscape of drug-induced injury of the lower gastrointestinal tract. Arch Pathol Lab Med 140(8):748–758. https://doi.org/10.5858/arpa.2015-0451-RA
35. Arnold CA, Lam-Himlin DM, Montgomery E (2015) Atlas of gastrointestinal pathology: a pattern based approach to non-neoplastic biopsies. Wolters Kluwer Health, Philadelphia
36. Beck KE, Blansfield JA, Tran KQ, Feldman a, Hughes MS, Royal RE, Kammula US, Topalian SL, Sherry RM, Kleiner D, Quezado M, Lowy I, Yellin M, Rosenberg SA, Yang JC et al (2006) Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 24(15):2283–2289. https://doi.org/10.1200/JCO.2005.04.5716
37. Fecher LA, Agarwala SS, Hodi FS, Weber JS (2013) Ipilimumab and its toxicities: a multidisciplinary approach. Oncologist 18(6):733–743. https://doi.org/10.1634/theoncologist.2012-0483
38. Fay AP, Moreira RB, Nunes Filho PR, Albuquerque C, Barrios CH (2016) The management of immune-related adverse events associated with immune checkpoint blockade. Expert Rev Qual Life Cancer Care 1(1):89–97. https://doi.org/10.1080/23809000.2016.1142827
39. Johnston RL, Lutzky J, Chodhry A, Barkin JS (2009) Cytotoxic T-lymphocyte-associated antigen 4 antibody-induced colitis and its management with infliximab. Dig Dis Sci 54(11):2538–2540. https://doi.org/10.1007/s10620-008-0641-z
40. Weber JS, Yang JC, Atkins MB, Disis ML (2015) Toxicities of immunotherapy for the practitioner. J Clin Oncol 33(18):2092–2099. https://doi.org/10.1200/JCO.2014.60.0379
41. Vieth M, Montgomery E (2017) Medication-associated gastrointestinal tract injury. Virchows Arch 470(3):245–266. https://doi.org/10.1007/s00428-017-2077-3