{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T17:36:56Z","timestamp":1787506616950,"version":"build-2736575974"},"reference-count":28,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2025,3,1]],"date-time":"2025-03-01T00:00:00Z","timestamp":1740787200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2025,3,1]],"date-time":"2025-03-01T00:00:00Z","timestamp":1740787200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Targ Oncol"],"published-print":{"date-parts":[[2025,3]]},"DOI":"10.1007\/s11523-025-01135-7","type":"journal-article","created":{"date-parts":[[2025,3,4]],"date-time":"2025-03-04T14:34:18Z","timestamp":1741098858000},"page":"339-347","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Differential Disease Behavior of Immune-Mediated Colitis Among Different Types of Immune Checkpoint Inhibition"],"prefix":"10.1007","volume":"20","author":[{"given":"Malek","family":"Shatila","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Farzin","family":"Eshaghi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carolina Colli","family":"Cruz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio Pizuorno","family":"Machado","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antony","family":"Mathew","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dan","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bilal A.","family":"Siddiqui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anusha Shirwaikar","family":"Thomas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suresh T.","family":"Chari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5148-6130","authenticated-orcid":false,"given":"Yinghong","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,3,4]]},"reference":[{"key":"1135_CR1","doi-asserted-by":"crossref","first-page":"405","DOI":"10.12998\/wjcc.v7.i4.405","volume":"7","author":"A Som","year":"2019","unstructured":"Som A, Mandaliya R, Alsaadi D, Farshidpour M, et al. Immune checkpoint inhibitor-induced colitis: a comprehensive review. World J Clin Cases. 2019;7:405\u201318.","journal-title":"World J Clin Cases."},{"key":"1135_CR2","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1158\/2326-6066.cir-16-0237","volume":"5","author":"G De Velasco","year":"2017","unstructured":"De Velasco G, Je Y, Boss\u00e9 D, Awad MM, et al. Comprehensive meta-analysis of key immune-related adverse events from CTLA-4 and PD-1\/PD-L1 inhibitors in cancer patients. Cancer Immunol Res. 2017;5:312\u20138. https:\/\/doi.org\/10.1158\/2326-6066.cir-16-0237.","journal-title":"Cancer Immunol Res"},{"key":"1135_CR3","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1007\/s40261-018-0735-0","volume":"39","author":"H-H Ji","year":"2019","unstructured":"Ji H-H, Tang X-W, Dong Z, Song L, et al. Adverse event profiles of anti-CTLA-4 and anti-PD-1 monoclonal antibodies alone or in combination: analysis of spontaneous reports submitted to FAERS. Clin Drug Investig. 2019;39:319\u201330. https:\/\/doi.org\/10.1007\/s40261-018-0735-0.","journal-title":"Clin Drug Investig"},{"key":"1135_CR4","first-page":"10","volume":"6","author":"DY Wang","year":"2017","unstructured":"Wang DY, Ye Y, Zhao S, Johnson DB. Incidence of immune checkpoint inhibitor-related colitis in solid tumor patients: a systematic review and meta-analysis. OncoImmunology. 2017;6:10.","journal-title":"OncoImmunology."},{"key":"1135_CR5","doi-asserted-by":"publisher","first-page":"1721","DOI":"10.1001\/jamaoncol.2018.3923","volume":"4","author":"DY Wang","year":"2018","unstructured":"Wang DY, Salem JE, Cohen JV, Chandra S, et al. Fatal toxic effects associated with immune checkpoint inhibitors: a systematic review and meta-analysis. JAMA Oncol. 2018;4:1721\u20138. https:\/\/doi.org\/10.1001\/jamaoncol.2018.3923.","journal-title":"JAMA Oncol"},{"key":"1135_CR6","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.pharmthera.2017.07.005","volume":"181","author":"S Cousin","year":"2018","unstructured":"Cousin S, Seneschal J, Italiano A. Toxicity profiles of immunotherapy. Pharmacol Ther. 2018;181:91\u2013100.","journal-title":"Pharmacol Ther"},{"key":"1135_CR7","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/s41571-019-0218-0","volume":"16","author":"F Martins","year":"2019","unstructured":"Martins F, Sofiya L, Sykiotis GP, et al. Adverse effects of immune-checkpoint inhibitors: epidemiology, management and surveillance. Nat Rev Clin Oncol. 2019;16:563\u201380.","journal-title":"Nat Rev Clin Oncol"},{"key":"1135_CR8","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1093\/ecco-jcc\/jjx081","volume":"11","author":"C Coutzac","year":"2017","unstructured":"Coutzac C, Adam J, Soularue E, Collins M, et al. Colon immune-related adverse events: anti-CTLA-4 and anti-PD-1 blockade induce distinct immunopathological entities. J Crohns Colitis. 2017;11:1238\u201346.","journal-title":"J Crohns Colitis"},{"issue":"1","key":"1135_CR9","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1186\/s40425-018-0411-1","volume":"6","author":"H Abu-Sbeih","year":"2018","unstructured":"Abu-Sbeih H, Ali FS, Luo W, Qiao W, et al. Importance of endoscopic and histological evaluation in the management of immune checkpoint inhibitor-induced colitis. J Immunother Cancer. 2018;6(1):95. https:\/\/doi.org\/10.1186\/s40425-018-0411-1.","journal-title":"J Immunother Cancer"},{"key":"1135_CR10","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1016\/j.cell.2020.06.001","volume":"182","author":"AM Luoma","year":"2020","unstructured":"Luoma AM, Suo S, Williams HL, Sharova T, et al. Molecular pathways of colon inflammation induced by cancer immunotherapy. Cell. 2020;182:655-71.e22. https:\/\/doi.org\/10.1016\/j.cell.2020.06.001.","journal-title":"Cell"},{"key":"1135_CR11","doi-asserted-by":"crossref","first-page":"86","DOI":"10.3389\/fonc.2018.00086","volume":"8","author":"JA Seidel","year":"2018","unstructured":"Seidel JA, Otsuka A, Kabashima K. Anti-PD-1 and anti-CTLA-4 therapies in cancer: mechanisms of action, efficacy, and limitations. Front Oncol. 2018;8:86.","journal-title":"Front Oncol"},{"key":"1135_CR12","doi-asserted-by":"publisher","first-page":"600","DOI":"10.1126\/science.1202947","volume":"332","author":"OS Qureshi","year":"2011","unstructured":"Qureshi OS, Zheng Y, Nakamura K, Attridge K, et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA4. Science. 2011;332:600\u20133. https:\/\/doi.org\/10.1126\/science.1202947.","journal-title":"Science"},{"key":"1135_CR13","doi-asserted-by":"crossref","first-page":"2691","DOI":"10.1200\/JCO.2012.41.6750","volume":"30","author":"JS Weber","year":"2012","unstructured":"Weber JS, K\u00e4hler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol. 2012;30:2691\u20137.","journal-title":"J Clin Oncol"},{"key":"1135_CR14","doi-asserted-by":"crossref","first-page":"2377","DOI":"10.1093\/annonc\/mdx286","volume":"28","author":"L Khoja","year":"2017","unstructured":"Khoja L, Day D, Wei-Wu Chen T, Siu LL, et al. Tumour- and class-specific patterns of immune-related adverse events of immune checkpoint inhibitors: a systematic review. Ann Oncol. 2017;28:2377\u201385.","journal-title":"Ann Oncol"},{"issue":"30","key":"1135_CR15","doi-asserted-by":"publisher","first-page":"2738","DOI":"10.1200\/JCO.19.00320","volume":"37","author":"H Abu-Sbeih","year":"2019","unstructured":"Abu-Sbeih H, Ali FS, Naqash AR, et al. Resumption of immune checkpoint inhibitor therapy after immune-mediated colitis. J Clin Oncol. 2019;37(30):2738\u201345. https:\/\/doi.org\/10.1200\/JCO.19.00320.","journal-title":"J Clin Oncol"},{"issue":"1","key":"1135_CR16","doi-asserted-by":"publisher","DOI":"10.1136\/esmoopen-2017-000278","volume":"3","author":"MH Geukes Foppen","year":"2018","unstructured":"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(1): e000278. https:\/\/doi.org\/10.1136\/esmoopen-2017-000278.","journal-title":"ESMO Open."},{"issue":"2","key":"1135_CR17","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/j.gie.2024.01.024","volume":"100","author":"Y Wang","year":"2024","unstructured":"Wang Y, Abu-Sbeih H, Tang T, et al. Novel endoscopic scoring system for immune mediated colitis: a multicenter retrospective study of 674 patients. Gastrointest Endosc. 2024;100(2):273-82.e4. https:\/\/doi.org\/10.1016\/j.gie.2024.01.024.","journal-title":"Gastrointest Endosc"},{"key":"1135_CR18","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1111\/his.13224","volume":"71","author":"P Bavi","year":"2017","unstructured":"Bavi P, Butler M, Serra S, Chetty R. Immune modulator-induced changes in the gastrointestinal tract. Histopathology. 2017;71:494\u20136.","journal-title":"Histopathology"},{"key":"1135_CR19","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1111\/his.13118","volume":"70","author":"RS Gonzalez","year":"2017","unstructured":"Gonzalez RS, Salaria SN, Bohannon CD, Huber AR, et al. PD-1 inhibitor gastroenterocolitis: case series and appraisal of \u2018immunomodulatory gastroenterocolitis.\u2019 Histopathology. 2017;70:558\u201367.","journal-title":"Histopathology"},{"key":"1135_CR20","doi-asserted-by":"crossref","first-page":"748","DOI":"10.5858\/arpa.2015-0451-RA","volume":"140","author":"EC Marginean","year":"2016","unstructured":"Marginean EC. The ever-changing landscape of drug-induced injury of the lower gastrointestinal tract. Arch Pathol Lab Med. 2016;140:748\u201358.","journal-title":"Arch Pathol Lab Med"},{"key":"1135_CR21","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1097\/PAS.0b013e31817150e3","volume":"32","author":"DA Oble","year":"2008","unstructured":"Oble DA, Mino-Kenudson M, Goldsmith J, Hodi FS, et al. Alpha-CTLA-4 mAb-associated panenteritis: a histologic and immunohistochemical analysis. Am J Surg Pathol. 2008;32:1130\u20137.","journal-title":"Am J Surg Pathol"},{"key":"1135_CR22","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2022.831407","volume":"12","author":"Y Wei","year":"2022","unstructured":"Wei Y, Li Z. LAG3-PD-1 combo overcome the disadvantage of drug resistance. Front Oncol. 2022;12: 831407. https:\/\/doi.org\/10.3389\/fonc.2022.831407.","journal-title":"Front Oncol"},{"key":"1135_CR23","doi-asserted-by":"publisher","first-page":"176","DOI":"10.18632\/genesandcancer.180","volume":"9","author":"L Long","year":"2018","unstructured":"Long L, Zhang X, Chen F, Pan Q, et al. The promising immune checkpoint LAG-3: from tumor microenvironment to cancer immunotherapy. Genes Cancer. 2018;9:176\u201389. https:\/\/doi.org\/10.18632\/genesandcancer.180.","journal-title":"Genes Cancer"},{"key":"1135_CR24","doi-asserted-by":"publisher","first-page":"1446","DOI":"10.1093\/ecco-jcc\/jjaa054","volume":"14","author":"SM Slevin","year":"2020","unstructured":"Slevin SM, Garner LC, Lahiff C, Tan M, et al. Lymphocyte activation gene (LAG)-3 is associated with mucosal inflammation and disease activity in ulcerative colitis. J Crohns Colitis. 2020;14:1446\u201361. https:\/\/doi.org\/10.1093\/ecco-jcc\/jjaa054.","journal-title":"J Crohns Colitis"},{"key":"1135_CR25","doi-asserted-by":"crossref","first-page":"255","DOI":"10.6004\/jnccn.2019.0013","volume":"17","author":"JA Thompson","year":"2019","unstructured":"Thompson JA, Schneider BJ, Brahmer J, et al. Management of immunotherapy-related toxicities, version 1.2019. J Natl Compr Canc Netw. 2019;17:255\u201389.","journal-title":"J Natl Compr Canc Netw"},{"key":"1135_CR26","first-page":"29","volume":"44","author":"H Abu-Sbeih","year":"2021","unstructured":"Abu-Sbeih H, Ali FS, Wang X, Mallepally N, et al. Early introduction of selective immunosuppressive therapy associated with favorable clinical outcomes in patients with immune checkpoint inhibitor-induced colitis. J Immunother Cancer. 2021;44:29\u201335.","journal-title":"J Immunother Cancer"},{"key":"1135_CR27","doi-asserted-by":"crossref","first-page":"387","DOI":"10.6004\/jnccn.2022.0020","volume":"20","author":"JA Thompson","year":"2022","unstructured":"Thompson JA, Schneider BJ, Brahmer J, Achufusi A, et al. Management of immunotherapy-related toxicities, version 1.2022, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2022;20:387\u2013405.","journal-title":"J Natl Compr Canc Netw"},{"key":"1135_CR28","doi-asserted-by":"crossref","first-page":"1804","DOI":"10.1038\/s41591-018-0238-9","volume":"24","author":"Y Wang","year":"2018","unstructured":"Wang Y, Wiesnoski DH, Helmink BA, Gopalakrishnan V, et al. Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis. Nat Med. 2018;24:1804\u20138.","journal-title":"Nat Med"}],"container-title":["Targeted Oncology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11523-025-01135-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s11523-025-01135-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11523-025-01135-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,26]],"date-time":"2025-03-26T22:14:13Z","timestamp":1743027253000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s11523-025-01135-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3]]},"references-count":28,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2025,3]]}},"alternative-id":["1135"],"URL":"https:\/\/doi.org\/10.1007\/s11523-025-01135-7","relation":{},"ISSN":["1776-2596","1776-260X"],"issn-type":[{"value":"1776-2596","type":"print"},{"value":"1776-260X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3]]},"assertion":[{"value":"11 February 2025","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 March 2025","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"No external funding was used in the preparation of this article.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Funding"}},{"value":"Malek Shatila, Farzin Eshaghi, Carolina Colli Cruz, Antonio Pizuorno Machado, Antony Mathew, Dan Zhao, Bilal A. Siddiqui, Anusha Shirwaikar Thomas, Suresh T. Chari, and Yinghong Wang have no conflicts of interest that are directly relevant to the content of this article.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"This study was performed in line with the principles of the Declaration of Helsinki. Approval for this study was granted by the institutional review board at The University of Texas MD Anderson Cancer Center (2018-0472).","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"Patient consent was waived for this study.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"Not applicable.","order":6,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The datasets used and analyzed in this study are available from the corresponding author on reasonable request.","order":7,"name":"Ethics","group":{"name":"EthicsHeading","label":"Availability of data and material"}},{"value":"Not applicable.","order":8,"name":"Ethics","group":{"name":"EthicsHeading","label":"Code availability"}},{"value":"YW was the senior author of the study; she developed the concept, designed the study, interpreted the results, ensured that data accuracy and integrity were preserved at all stages, agreed to be accountable for all aspects of the study, was in charge of the overall direction and planning of the study, and contributed to the writing of the manuscript. FE, MS, APM, and AM collected the data for the study. MS conducted and interpreted the analysis. FE wrote the manuscript. BS, DZ, AST, and SC critically revised the final version of the manuscript. All authors provided input during writing of the manuscript and read and approved the final manuscript.","order":9,"name":"Ethics","group":{"name":"EthicsHeading","label":"Author contributions"}}]}}