Incidence of immune checkpoint inhibitor-related colitis in solid tumor patients: A systematic review and meta-analysis

OncoImmunology

Volumn 6, Issue 10, 2017, Pages

  Wang, Daniel Y ^a   Ye, Fei ^a   Zhao, Shilin ^a   Johnson, Douglas B ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

immune related colitis; Immunotherapy; melanoma; meta analysis; non small cell lung cancer; renal cell carcinoma

Indexed keywords

ATEZOLIZUMAB; CHECKPOINT KINASE INHIBITOR; IPILIMUMAB; NIVOLUMAB; PEMBROLIZUMAB;

ARTICLE; CANCER CHEMOTHERAPY; CANCER STAGING; CANCER THERAPY; COLITIS; DIARRHEA; HEAD AND NECK CANCER; HUMAN; MERKEL CELL CARCINOMA; META ANALYSIS; NON SMALL CELL LUNG CANCER; RENAL CELL CARCINOMA; SOLID MALIGNANT NEOPLASM; SYSTEMATIC REVIEW;

EID: 85028542426     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2017.1344805     Document Type: Article

References (50)

1. Weber JS, O'Day S, Urba W, Powderly J, Nichol G, Yellin M, Snively J, Hersh E. Phase i/ii study of ipilimumab for patients with metastatic melanoma. J Clin Oncol 2008; 26(36):5950-56; PMID:19018089; https://doi.org/10.1200/JCO.2008.16.1927
2. Weber J, Thompson JA, Hamid O, Minor D, Amin A, Ron I, Ridolfi R, Assi H, Maraveyas A, Berman D, 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):5591-98; PMID:19671877; https://doi.org/10.1158/1078-0432.CCR-09-1024
3. Wolchok JD, Neyns B, Linette G, Negrier S, Lutzky J, Thomas L, Waterfield W, Schadendorf D, Smylie M, Guthrie T, Jr. 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; PMID:20004617; https://doi.org/10.1016/S1470-2045(09)70334-1
4. O'Day SJ, Maio M, Chiarion-Sileni V, Gajewski TF, Pehamberger H, Bondarenko IN, Queirolo P, Lundgren L, Mikhailov S, Roman L, et al. Efficacy and safety of ipilimumab monotherapy in patients with pretreated advanced melanoma: A multicenter single-arm phase ii study. Ann Oncol 2010; 21(8):1712-17; https://doi.org/10.1093/annonc/mdq013
5. Brahmer JR, Drake CG, Wollner I, Powderly JD, Picus J, Sharfman WH, Stankevich E, Pons A, Salay TM, McMiller TL, et al. Phase i study of single-agent anti-programmed death-1 (mdx-1106) in refractory solid tumors: Safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol 2010; 28(19):3167-75; PMID:20516446; https://doi.org/10.1200/JCO.2009.26.7609
6. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363(8):711-23; PMID:20525992; https://doi.org/10.1056/NEJMoa1003466
7. Margolin K, Ernstoff MS, Hamid O, Lawrence D, McDermott D, Puzanov I, Wolchok JD, Clark JI, Sznol M, Logan TF, et al. Ipilimumab in patients with melanoma and brain metastases: An open-label, phase 2 trial. Lancet Oncol 2012; 13(5):459-65; PMID:22456429; https://doi.org/10.1016/S1470-2045(12)70090-6
8. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti-pd-1 antibody in cancer. N Engl J Med 2012; 366(26):2443-54; PMID:22658127; https://doi.org/10.1056/NEJMoa1200690
9. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS, et al. 2013. Safety and tumor responses with lambrolizumab (anti-pd-1) in melanoma. N Engl J Med 369(2):134-44; PMID:23724846; https://doi.org/10.1056/NEJMoa1305133
10. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369(2):122-33; PMID:23724867; https://doi.org/10.1056/NEJMoa1302369
11. Weber JS, Kudchadkar RR, Yu B, Gallenstein D, Horak CE, Inzunza HD, Zhao X, Martinez AJ, Wang W, Gibney G, et al. Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma. J Clin Oncol 2013; 31(34):4311-18; PMID:24145345; https://doi.org/10.1200/JCO.2013.51.4802
12. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, Brahmer JR, Lawrence DP, Atkins MB, Powderly JD, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014; 32(10):1020-30; PMID:24590637; https://doi.org/10.1200/JCO.2013.53.0105
13. Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, Hassel JC, Rutkowski P, McNeil C, Kalinka-Warzocha E, et al. Nivolumab in previously untreated melanoma without braf mutation. N Engl J Med 2015; 372(4):320-30; PMID:25399552; https://doi.org/10.1056/NEJMoa1412082
14. Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN, et al. Predictive correlates of response to the anti-pd-l1 antibody mpdl3280a in cancer patients. Nature 2014; 515(7528):563-7; PMID:25428504; https://doi.org/10.1038/nature14011
15. Motzer RJ, Rini BI, McDermott DF, Redman BG, Kuzel TM, Harrison MR, Vaishampayan UN, Drabkin HA, George S, Logan TF, et al. Nivolumab for metastatic renal cell carcinoma: Results of a randomized phase ii trial. J Clin Oncol 2015; 33(13):1430-7; PMID:25452452; https://doi.org/10.1200/JCO.2014.59.0703
16. Rizvi NA, Mazieres J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, Horn L, Lena H, Minenza E, Mennecier B, 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; PMID:25704439; https://doi.org/10.1016/S1470-2045(15)70054-9
17. Weber JS, D'Angelo SP, Minor D, Hodi FS, Gutzmer R, Neyns B, Hoeller C, Khushalani NI, Miller WH, Jr., Lao CD, 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; PMID:25795410; https://doi.org/10.1016/S1470-2045(15)70076-8
18. McDermott DF, Drake CG, Sznol M, Choueiri TK, Powderly JD, Smith DC, Brahmer JR, Carvajal RD, Hammers HJ, Puzanov I, et al. Survival, durable response, and long-term safety in patients with previously treated advanced renal cell carcinoma receiving nivolumab. J Clin Oncol 2015; 33(18):2013-20; PMID:25800770; https://doi.org/10.1200/JCO.2014.58.1041
19. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 2015; 372(21):2018-28; PMID:25891174; https://doi.org/10.1056/NEJMoa1501824
20. Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M, et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med 2015; 372(26):2521-32; PMID:25891173; https://doi.org/10.1056/NEJMoa1503093
21. Gettinger S, Rizvi NA, Chow LQ, Borghaei H, Brahmer J, Ready N, Gerber DE, Shepherd FA, Antonia S, Goldman JW, et al. Nivolumab monotherapy for first-line treatment of advanced non-small-cell lung cancer. J Clin Oncol 2016; 34(25):2980-87; PMID:27354485; https://doi.org/10.1200/JCO.2016.66.9929
22. Postow MA, Chesney J, Pavlick AC, Robert C, Grossmann K, McDermott D, Linette GP, Meyer N, Giguere JK, Agarwala SS, et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med 2015; 372(21):2006-17; PMID:25891304; https://doi.org/10.1056/NEJMoa1414428
23. Patnaik A, Kang SP, Rasco D, Papadopoulos KP, Elassaiss-Schaap J, Beeram M, Drengler R, Chen C, Smith L, Espino G, et al. Phase i study of pembrolizumab (mk-3475; anti-pd-1 monoclonal antibody) in patients with advanced solid tumors. Clin Cancer Res 2015; 21(19):4286-93; PMID:25977344; https://doi.org/10.1158/1078-0432.CCR-14-2607
24. Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D, et al. Pd-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med 2015; 372(26):2509-20; PMID:26028255; https://doi.org/10.1056/NEJMoa1500596
25. Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 2015; 373(2):123-35; PMID:26028407; https://doi.org/10.1056/NEJMoa1504627
26. Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015; 373(1):23-34; PMID:26027431; https://doi.org/10.1056/NEJMoa1504030
27. Ribas A, Puzanov I, Dummer R, Schadendorf D, Hamid O, Robert C, Hodi FS, Schachter J, Pavlick AC, Lewis KD, et al. Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (keynote-002): A randomised, controlled, phase 2 trial. Lancet Oncol 2015; 16(8):908-18; PMID:26115796; https://doi.org/10.1016/S1470-2045(15)00083-2
28. Hamanishi J, Mandai M, Ikeda T, Minami M, Kawaguchi A, Murayama T, Kanai M, Mori Y, Matsumoto S, Chikuma S, 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; PMID:26351349; https://doi.org/10.1200/JCO.2015.62.3397
29. Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med 2015; 373(19):1803-13; PMID:26406148; https://doi.org/10.1056/NEJMoa1510665
30. Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med 2015; 373(17):1627-39; PMID:26412456; https://doi.org/10.1056/NEJMoa1507643
31. Herbst RS, Baas P, Kim DW, Felip E, Perez-Gracia JL, Han JY, Molina J, Kim JH, Arvis CD, Ahn MJ, et al. Pembrolizumab versus docetaxel for previously treated, pd-l1-positive, advanced non-small-cell lung cancer (keynote-010): A randomised controlled trial. Lancet (London, England) 2016; 387(10027):1540-50; PMID:26712084; https://doi.org/10.1016/S0140-6736(15)01281-7
32. McDermott DF, Sosman JA, Sznol M, Massard C, Gordon MS, Hamid O, Powderly JD, Infante JR, Fasso M, Wang YV, et al. Atezolizumab, an anti-programmed death-ligand 1 antibody, in metastatic renal cell carcinoma: Long-term safety, clinical activity, and immune correlates from a phase ia study. J Clin Oncol 2016; 34(8):833-42; PMID:26755520; https://doi.org/10.1200/JCO.2015.63.7421
33. Rosenberg JE, Hoffman-Censits J, Powles T, van der Heijden MS, Balar AV, Necchi A, Dawson N, O'Donnell PH, Balmanoukian A, Loriot Y, et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: A single-arm, multicentre, phase 2 trial. Lancet 2016; 387(10031):1909-20; PMID:26952546; https://doi.org/10.1016/S0140-6736(16)00561-4
34. Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, Park K, Smith D, Artal-Cortes A, Lewanski C, 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; PMID:26970723; https://doi.org/10.1016/S0140-6736(16)00587-0
35. Nghiem PT, Bhatia S, Lipson EJ, Kudchadkar RR, Miller NJ, Annamalai L, Berry S, Chartash EK, Daud A, Fling SP, et al. Pd-1 blockade with pembrolizumab in advanced merkel-cell carcinoma. N Engl J Med 2016; 374(26):2542-52; PMID:27093365; https://doi.org/10.1056/NEJMoa1603702
36. Ribas A, Hamid O, Daud A, Hodi FS, Wolchok JD, Kefford R, Joshua AM, Patnaik A, Hwu WJ, Weber JS, et al. Association of pembrolizumab with tumor response and survival among patients with advanced melanoma. Jama 2016; 315(15):1600-1609; PMID:27092830; https://doi.org/10.1001/jama.2016.4059
37. Seiwert TY, Burtness B, Mehra R, Weiss J, Berger R, Eder JP, Heath K, McClanahan T, Lunceford J, Gause C, 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):956-965; PMID:27247226; https://doi.org/10.1016/S1470-2045(16)30066-3
38. Eggermont AM, Chiarion-Sileni V, Grob JJ, Dummer R, Wolchok JD, Schmidt H, Hamid O, Robert C, Ascierto PA, Richards JM, et al. Prolonged survival in stage iii melanoma with ipilimumab adjuvant therapy. N Engl J Med 2016; 375(19):1845-55; PMID:27717298; https://doi.org/10.1056/NEJMoa1611299
39. Ferris RL, Blumenschein G, Jr., Fayette J, Guigay J, Colevas AD, Licitra L, Harrington K, Kasper S, Vokes EE, Even C, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med 2016; 375(19):1856-67; PMID:27718784; https://doi.org/10.1056/NEJMoa1602252
40. Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, Gottfried M, Peled N, Tafreshi A, Cuffe S, et al. Pembrolizumab versus chemotherapy for pd-l1-positive non-small-cell lung cancer. N Engl J Med 2016; 375(19):1823-33; PMID:27718847; https://doi.org/10.1056/NEJMoa1606774
41. Naidoo J, Page DB, Li BT, Connell LC, Schindler K, Lacouture ME, Postow MA, Wolchok JD. Toxicities of the anti-pd-1 and anti-pd-l1 immune checkpoint antibodies. Ann Oncol 2015; 26(12):2375-91
42. Weber JS, Yang JC, Atkins MB, Disis ML. Toxicities of immunotherapy for the practitioner. J Clin Oncol 2015; 33(18):2092-99; PMID:25918278; https://doi.org/10.1200/JCO.2014.60.0379
43. Champiat S, Lambotte O, Barreau E, Belkhir R, Berdelou A, Carbonnel F, Cauquil C, Chanson P, Collins M, Durrbach A, et al. Management of immune checkpoint blockade dysimmune toxicities: A collaborative position paper. Ann Oncol 2016; 27(4):559-74; PMID:26715621; https://doi.org/10.1093/annonc/mdv623
44. Nishino M, Giobbie-Hurder A, Hatabu H, Ramaiya NH, Hodi FS. Incidence of programmed cell death 1 inhibitor-related pneumonitis in patients with advanced cancer: A systematic review and meta-analysis. JAMA Oncol 2016; 2(12):1607-16; PMID:27540850; https://doi.org/10.1001/jamaoncol.2016.2453
45. Read S, Malmstrom V, Powrie F. Cytotoxic t lymphocyte-associated antigen 4 plays an essential role in the function of cd25(+)cd4(+) regulatory cells that control intestinal inflammation. The Journal of experimental medicine 2000; 192(2):295-02; PMID:10899916; https://doi.org/10.1084/jem.192.2.295
46. Watanabe K, Rao VP, Poutahidis T, Rickman BH, Ohtani M, Xu S, Rogers AB, Ge Z, Horwitz BH, Fujioka T, et al. Cytotoxic-t-lymphocyte-associated antigen 4 blockade abrogates protection by regulatory t cells in a mouse model of microbially induced innate immune-driven colitis. Infect Immun 2008; 76(12):5834-42; PMID:18824539; https://doi.org/10.1128/IAI.00542-08
47. Barnes MJ, Griseri T, Johnson AM, Young W, Powrie F, Izcue A. 2013. Ctla-4 promotes foxp3 induction and regulatory t cell accumulation in the intestinal lamina propria. Mucosal Immunol 6(2):324-34; PMID:22910217; https://doi.org/10.1038/mi.2012.75
48. Scandiuzzi L, Ghosh K, Hofmeyer KA, Abadi YM, Lazar-Molnar E, Lin EY, Liu Q, Jeon H, Almo SC, Chen L, et al. 2014. Tissue-expressed b7-h1 critically controls intestinal inflammation. Cell Rep 6(4):625-32; PMID:24529703; https://doi.org/10.1016/j.celrep.2014.01.020
49. Totsuka T, Kanai T, Makita S, Fujii R, Nemoto Y, Oshima S, Okamoto R, Koyanagi A, Akiba H, Okumura K, et al. 2005. Regulation of murine chronic colitis by cd4+cd25- programmed death-1+ t cells. Eur J Immunol 35(6):1773-85; PMID:15902682; https://doi.org/10.1002/eji.200425109
50. Bilir SP, Ma Q, Zhao Z, Wehler E, Munakata J, Barber B. Economic burden of toxicities associated with treating metastatic melanoma in the united states. Am Health Drug Benefits 2016; 9(4):203-13; PMID:27688833