Immune checkpoint inhibitor-induced gastrointestinal and hepatic injury: Pathologists' perspective

Journal of Clinical Pathology

Volumn 71, Issue 8, 2018, Pages 665-671

  Karamchandani, Dipti M ^a   Chetty, Runjan ^b  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

colon; histopathology; liver

Indexed keywords

ANTINEOPLASTIC MONOCLONAL ANTIBODY; IPILIMUMAB; NIVOLUMAB; IMMUNOLOGICAL ANTINEOPLASTIC AGENT;

ARTICLE; CLINICAL FEATURE; COLITIS; COLON BIOPSY; DIFFERENTIAL DIAGNOSIS; DIGESTIVE SYSTEM INJURY; DRUG MECHANISM; ENDOSCOPY; FOLLOW UP; HISTOPATHOLOGY; HUMAN; LIVER INJURY; PRIORITY JOURNAL; BIOPSY; CHEMICALLY INDUCED; COLON; DRUG EFFECT; IMMUNOLOGY; LIVER; NEOPLASM; PATHOLOGIST; PATHOLOGY; PREDICTIVE VALUE; PROGNOSIS; TOXIC HEPATITIS;

ANTINEOPLASTIC AGENTS, IMMUNOLOGICAL; BIOPSY; CHEMICAL AND DRUG INDUCED LIVER INJURY; COLITIS; COLON; DIAGNOSIS, DIFFERENTIAL; HUMANS; LIVER; NEOPLASMS; PATHOLOGISTS; PREDICTIVE VALUE OF TESTS; PROGNOSIS;

EID: 85049222937     PISSN: 00219746     EISSN: 14724146     Source Type: Journal    
DOI: 10.1136/jclinpath-2018-205143     Document Type: Article

References (48)

1. Assarzadegan N, Montgomery E, Anders RA. Immune checkpoint inhibitor colitis: The flip side of the wonder drugs. Virchows Arch 2018;472:125-33.
2. Cramer P, Bresalier RS. Gastrointestinal and hepatic complications of immune checkpoint inhibitors. Curr Gastroenterol Rep 2017;19:3.
3. Prieux-Klotz C, Dior M, Damotte D, et al. Immune checkpoint inhibitor-induced colitis: Diagnosis and management. Target Oncol 2017;12:301-8.
4. Schadendorf D, Hodi FS, Robert C, et al. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma. J Clin Oncol 2015;33:1889-94.
5. Le DT, Uram JN, Wang H, et al. PD-1 Blockade in tumors with mismatch-repair deficiency. N Engl J Med 2015;372:2509-20.
6. Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 2015;372:320-30.
7. Melosky B, Chu Q, Juergens R, et al. Pointed progress in second-line advanced nonsmall-cell lung cancer: The rapidly evolving field of checkpoint inhibition. J Clin Oncol 2016;34:1676-88.
8. Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med 2015;373:1803-13.
9. Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab for metastatic renal cell carcinoma: Results of a randomized phase II trial. J Clin Oncol 2015;33:1430-7.
10. Topalian SL, Taube JM, Anders RA, et al. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer 2016;16:275-87.
11. Hofmann L, Forschner A, Loquai C, et al. Cutaneous, gastrointestinal, hepatic, endocrine, and renal side-effects of anti-PD-1 therapy. Eur J Cancer 2016;60:190-209.
12. Naidoo J, Page DB, Li BT, Bt L, et al. Toxicities of the anti-PD-1 and anti-PD-L1 immune checkpoint antibodies. Ann Oncol 2016;27:1362.
13. Geukes Foppen MH, Rozeman EA, van Wilpe S, et al. Immune checkpoint inhibition-related colitis: Symptoms, endoscopic features, histology and response to management. ESMO Open 2018;3:e000278.
14. Johncilla M, Misdraji J, Pratt DS, et al. Ipilimumab-associated hepatitis: Clinicopathologic characterization in a series of 11 cases. Am J Surg Pathol 2015;39:1075-84.
15. Zen Y, Yeh MM. Hepatotoxicity of immune checkpoint inhibitors: A histology study of seven cases in comparison with autoimmune hepatitis and idiosyncratic drug-induced liver injury. Mod Pathol 2018.
16. Korman AJ, Peggs KS, Allison JP. Checkpoint blockade in cancer immunotherapy. Adv Immunol 2006;90:297-339.
17. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
18. Gupta A, De Felice KM, Loftus EV, et al. Systematic review: Colitis associated with anti-CTLA-4 therapy. Aliment Pharmacol Ther 2015;42:406-17.
19. Wolchok JD, Neyns B, Linette G, et al. Ipilimumab monotherapy in patients with pretreated advanced melanoma: A randomised, double-blind, multicentre, phase 2, dose-ranging study. Lancet Oncol 2010;11:155-64.
20. Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015;373:23-34.
21. Mitchell KA, Kluger H, Sznol M, et al. Ipilimumab-induced perforating colitis. J Clin Gastroenterol 2013;47:781-5.
22. Weber JS, Dummer R, de Pril V, Pril de V, et al. 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 2013;119:1675-82.
23. Eigentler TK, Hassel JC, Berking C, et al. Diagnosis, monitoring and management of immune-related adverse drug reactions of anti-PD-1 antibody therapy. Cancer Treat Rev 2016;45:7-18.
24. Verschuren EC, van den Eertwegh AJ, Wonders J, et al. Clinical, endoscopic, and histologic characteristics of ipilimumab-associated colitis. Clin Gastroenterol Hepatol 2016;14:836-42.
25. Chen JH, Pezhouh MK, Lauwers GY, et al. Histopathologic features of colitis due to immunotherapy with anti-pd-1 antibodies. Am J Surg Pathol 2017;41:643-54.
26. Gonzalez RS, Salaria SN, Bohannon CD, et al. PD-1 inhibitor gastroenterocolitis: Case series and appraisal of 'immunomodulatory gastroenterocolitis'. Histopathology 2017;70:558-67.
27. Oble DA, Mino-Kenudson M, Goldsmith J, et al. Alpha-CTLA-4 mAb-associated panenteritis: A histologic and immunohistochemical analysis. Am J Surg Pathol 2008;32:1130-7.
28. Garciá-Varona A, Odze RD, Makrauer F. Lymphocytic colitis secondary to ipilimumab treatment. Inflamm Bowel Dis 2013;19:E15-E16.
29. Baroudjian B, Lourenco N, Pagès C, et al. Anti-PD1-induced collagenous colitis in a melanoma patient. Melanoma Res 2016;26:308-11.
30. Bavi P, Butler M, Serra S, et al. Immune modulator-induced changes in the gastrointestinal tract. Histopathology 2017;71:494-6.
31. Beck KE, Blansfield JA, Tran KQ, et al. Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J Clin Oncol 2006;24:2283-9.
32. Parfitt JR, Jayakumar S, Driman DK. Mycophenolate mofetil-related gastrointestinal mucosal injury: Variable injury patterns, including graft-versus-host disease-like changes. Am J Surg Pathol 2008;32:1367-72.
33. Lee S, de Boer WB, Subramaniam K, et al. Pointers and pitfalls of mycophenolateassociated colitis. J Clin Pathol 2013;66:8-11.
34. Soldini D, Gaspert A, Montani M, et al. Apoptotic enteropathy caused by antimetabolites and TNF-antagonists. J Clin Pathol 2014;67:582-6.
35. Louie CY, DiMaio MA, Matsukuma KE, et al. Idelalisib-associated enterocolitis: Clinicopathologic features and distinction from other enterocolitides. Am J Surg Pathol 2015;39:1653-60.
36. Weidner AS, Panarelli NC, Geyer JT, et al. Idelalisib-associated colitis: Histologic findings in 14 patients. Am J Surg Pathol 2015;39:1661-7.
37. Mahajan D, Goldblum JR, Xiao SY, et al. Lymphocytic colitis and collagenous colitis: A review of clinicopathologic features and immunologic abnormalities. Adv Anat Pathol 2012;19:28-38.
38. Weber JS, Postow M, Lao CD, et al. Management of adverse events following treatment with anti-programmed death-1 agents. Oncologist 2016;21:1230-40.
39. Fecher LA, Agarwala SS, Hodi FS, et al. Ipilimumab and its toxicities: A multidisciplinary approach. Oncologist 2013;18:733-43.
40. Johnston RL, Lutzky J, Chodhry A, et al. Cytotoxic T-lymphocyte-associated antigen 4 antibody-induced colitis and its management with infliximab. Dig Dis Sci 2009;54:2538-40.
41. Weber JS, Yang JC, Atkins MB, et al. Toxicities of Immunotherapy for the Practitioner. J Clin Oncol 2015;33:2092-9.
42. Di Giacomo AM, Biagioli M, Maio M. The emerging toxicity profiles of anti-CTLA-4 antibodies across clinical indications. Semin Oncol 2010;37:499-507.
43. Kim KW, Ramaiya NH, Krajewski KM, et al. Ipilimumab associated hepatitis: Imaging and clinicopathologic findings. Invest New Drugs 2013;31:1071-7.
44. Weber JS, Kähler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol 2012;30:2691-7.
45. Kleiner DE, Berman D. Pathologic changes in ipilimumab-related hepatitis in patients with metastatic melanoma. Dig Dis Sci 2012;57:2233-40.
46. Aivazian K, Long GV, Sinclair EC, et al. Histopathology of pembrolizumab-induced hepatitis: A case report. Pathology 2017;49:789-92.
47. Simonelli M, Di Tommaso L, Baretti M, et al. Pathological characterization of nivolumab-related liver injury in a patient with glioblastoma. Immunotherapy 2016;8:1363-9.
48. Everett J, Srivastava A, Misdraji J. Fibrin ring granulomas in checkpoint inhibitorinduced hepatitis. Am J Surg Pathol 2017;41:134-7.