{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T21:40:22Z","timestamp":1790199622837,"version":"4.1.0"},"reference-count":44,"publisher":"SAGE Publications","issue":"5-6","license":[{"start":{"date-parts":[[2023,3,1]],"date-time":"2023-03-01T00:00:00Z","timestamp":1677628800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Human Gene Therapy"],"published-print":{"date-parts":[[2023,3]]},"abstract":"<jats:p>Dual-targeting chimeric antigen receptor (CAR)-T cell therapy has been proposed as a potential solution for overcoming antigen escape during anti-CD19 CAR-T treatment. We performed this systematic review and meta-analysis to investigate the efficacy and safety of this novel treatment in patients with B cell non-Hodgkin lymphoma (B-NHL) and B cell acute lymphoblastic leukemia (B-ALL). We systematically searched relevant literature based on databases (PubMed, Web of Science, Embase and Cochrane) and conference abstracts. The primary outcomes measured were the best objective response rate (ORR) or complete response (CR), 12-month overall survival (OS) and progression-free survival (PFS), cytokine release syndrome (CRS), and neurotoxicity. Fifteen registered prospective open-label clinical trials were included. Among the 260 patients with B-NHL, the pooled best ORR and CR were 77% (95% confidence interval [CI]: 0.71\u20130.82) and 52% (95% CI: 0.40\u20130.63), respectively, and the pooled 12-month PFS and OS were 54.0% (95% CI: 0.47\u20130.61) and 66.0% (95% CI: 0.56\u20130.77), respectively. In the 159 patients with B-ALL, the combined best CR was observed to be 92% (95% CI: 0.82\u20130.99) and the pooled 12-month PFS and OS were 65.0% (95% CI: 0.51\u20130.77) and 73.0% (95% CI: 0.56\u20130.92), respectively. Moreover, in B-NHL patients, grade \u22653 CRS was observed in 14.0% (95% CI: 0.04\u20130.29) of these patients, and 5.0% (95% CI: 0.02\u20130.08) showed grade \u22653 neurotoxicity; in the case of B-ALL patients, grade \u22653 CRS and neurotoxicity occurred in 11.0% (95% CI: 0.04\u20130.19) and 2.0% (95% CI: 0.00\u20130.06), respectively. This study demonstrates the safety and clinical efficacy of dual-targeting CAR-T cell therapies in B cell malignancies. Further, well-designed randomized controlled trials are required to establish the role of dual-targeting CAR-T cell therapy in patients with B cell malignancies.<\/jats:p>","DOI":"10.1089\/hum.2022.183","type":"journal-article","created":{"date-parts":[[2023,2,3]],"date-time":"2023-02-03T07:11:36Z","timestamp":1675408296000},"page":"192-202","update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":8,"title":["Efficacy and Safety of Dual-Targeting Chimeric Antigen Receptor-T Therapy for Relapsed or Refractory B Cell Lymphoid Malignancies: A Systematic Review and Meta-Analysis"],"prefix":"10.1177","volume":"34","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1469-6307","authenticated-orcid":false,"given":"Min","family":"Yu","sequence":"first","affiliation":[{"name":"Center of Hematology, The First Affiliated Hospital of Nanchang University, Nanchang, China"},{"name":"Institute of Hematology, Academy of Clinical Medicine of Jiangxi Province, Nanchang, China"},{"name":"National Clinical Research Sub-Center for Blood Diseases, Jiangxi Clinical Research Center of Hematology, Nanchang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Zhang","sequence":"additional","affiliation":[{"name":"Center of Hematology, The First Affiliated Hospital of Nanchang University, Nanchang, China"},{"name":"Institute of Hematology, Academy of Clinical Medicine of Jiangxi Province, Nanchang, China"},{"name":"National Clinical Research Sub-Center for Blood Diseases, Jiangxi Clinical Research Center of Hematology, Nanchang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fancong","family":"Kong","sequence":"additional","affiliation":[{"name":"Center of Hematology, The First Affiliated Hospital of Nanchang University, Nanchang, China"},{"name":"Institute of Hematology, Academy of Clinical Medicine of Jiangxi Province, Nanchang, China"},{"name":"National Clinical Research Sub-Center for Blood Diseases, Jiangxi Clinical Research Center of Hematology, Nanchang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling","family":"Qi","sequence":"additional","affiliation":[{"name":"Center of Hematology, The First Affiliated Hospital of Nanchang University, Nanchang, China"},{"name":"Institute of Hematology, Academy of Clinical Medicine of Jiangxi Province, Nanchang, China"},{"name":"National Clinical Research Sub-Center for Blood Diseases, Jiangxi Clinical Research Center of Hematology, Nanchang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yafang","family":"Pu","sequence":"additional","affiliation":[{"name":"Center of Hematology, The First Affiliated Hospital of Nanchang University, Nanchang, China"},{"name":"Institute of Hematology, Academy of Clinical Medicine of Jiangxi Province, Nanchang, China"},{"name":"National Clinical Research Sub-Center for Blood Diseases, Jiangxi Clinical Research Center of Hematology, Nanchang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lugui","family":"Qiu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, National Clinical Research Center for Blood Diseases, Institute of Hematology and Blood Diseases Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, China."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9437-9151","authenticated-orcid":false,"given":"Jianxiang","family":"Wang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Experimental Hematology, National Clinical Research Center for Blood Diseases, Institute of Hematology and Blood Diseases Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, China."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fei","family":"Li","sequence":"additional","affiliation":[{"name":"Center of Hematology, The First Affiliated Hospital of Nanchang University, Nanchang, China"},{"name":"Institute of Hematology, Academy of Clinical Medicine of Jiangxi Province, Nanchang, China"},{"name":"National Clinical Research Sub-Center for Blood Diseases, Jiangxi Clinical Research Center of Hematology, Nanchang, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"179","published-online":{"date-parts":[[2023,3,20]]},"reference":[{"key":"e_1_3_5_2_2","doi-asserted-by":"publisher","DOI":"10.1200\/JCO.20.02262"},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1470-S2045(21)00375-2"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1470-2045(18)30864-7"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa1709919"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1189\/jlb.5RU0817-315R"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1002\/ecy.3299"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1182\/blood.2021010930"},{"key":"e_1_3_5_9_2","doi-asserted-by":"publisher","DOI":"10.3390\/cancers12051075"},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.1111\/cas.14799"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1186\/s40164-022-00270-5"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.omto.2018.10.006"},{"key":"e_1_3_5_13_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-021-01497-1"},{"key":"e_1_3_5_14_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-020-1081-3"},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-021-01436-0"},{"key":"e_1_3_5_16_2","doi-asserted-by":"publisher","DOI":"10.1182\/blood.2019000017"},{"key":"e_1_3_5_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41408-020-00371-6"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.1002\/(sici)1097-0258(19981230)17:24<2815::aid-sim110>3.0.co;2-8"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2021.664421"},{"key":"e_1_3_5_20_2","doi-asserted-by":"publisher","DOI":"10.1186\/s13045-020-00856-8"},{"key":"e_1_3_5_21_2","doi-asserted-by":"publisher","DOI":"10.1158\/2326-6066.CIR-20-0675"},{"key":"e_1_3_5_22_2","doi-asserted-by":"crossref","unstructured":"Osborne W Marzolini M Tholouli E et al. Phase I Alexander Study of AUTO3 the First CD19\/CD22 Dual Targeting CAR-T Therapy with Pembrolizumab in Patients with Relapsed\/Refractory (r\/r) DLBCL. 2020 ASCO Virtual Scientific Program Abstract 8001. Available from: https:\/\/ascopubs.org\/doi\/abs\/10.1200\/JCO.2020.38.15-suppl.8001 [Last accessed: May 9 2022].","DOI":"10.1200\/JCO.2020.38.15_suppl.8001"},{"key":"e_1_3_5_23_2","doi-asserted-by":"publisher","DOI":"10.1002\/ajh.26160"},{"key":"e_1_3_5_24_2","doi-asserted-by":"publisher","DOI":"10.1158\/1078-0432.CCR-20-3863"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41375-021-01345-8"},{"key":"e_1_3_5_26_2","doi-asserted-by":"publisher","DOI":"10.1002\/cam4.3259"},{"key":"e_1_3_5_27_2","doi-asserted-by":"publisher","DOI":"10.1182\/blood.2019003293"},{"key":"e_1_3_5_28_2","doi-asserted-by":"publisher","DOI":"10.1182\/blood.2022015795"},{"key":"e_1_3_5_29_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.hemonc.2021.09.004"},{"key":"e_1_3_5_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.clml.2021.07.002"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.3389\/fphar.2022.834113"},{"key":"e_1_3_5_32_2","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2021.698607"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1002\/cac2.12126"},{"key":"e_1_3_5_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/S2352-3026(20)30277-5"},{"key":"e_1_3_5_35_2","doi-asserted-by":"publisher","DOI":"10.1182\/bloodadvances.2020003482"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa1707447"},{"key":"e_1_3_5_37_2","doi-asserted-by":"publisher","DOI":"10.1182\/blood-2018-99-117199"},{"key":"e_1_3_5_38_2","doi-asserted-by":"publisher","DOI":"10.1182\/blood-2019-126218"},{"key":"e_1_3_5_39_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-019-0549-5"},{"key":"e_1_3_5_40_2","doi-asserted-by":"publisher","DOI":"10.1200\/JCO.20.03585"},{"key":"e_1_3_5_41_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1907056116"},{"key":"e_1_3_5_42_2","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.887866"},{"issue":"1","key":"e_1_3_5_43_2","first-page":"156","article-title":"Development of GPC3 and EGFR-dual-targeting chimeric antigen receptor-T cells for adoptive T cell therapy","volume":"13","author":"Li K","year":"2021","unstructured":"Li K, , Qian S, , Huang M, et al. Development of GPC3 and EGFR-dual-targeting chimeric antigen receptor-T cells for adoptive T cell therapy. Am J Transl Res, 2021; 13(1):156\u2013167.","journal-title":"Am J Transl Res"},{"key":"e_1_3_5_44_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00262-016-1949-8"},{"key":"e_1_3_5_45_2","doi-asserted-by":"publisher","DOI":"10.3892\/mco.2020.2103"}],"container-title":["Human Gene Therapy"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.sagepub.com\/doi\/full-xml\/10.1089\/hum.2022.183","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/hum.2022.183","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/hum.2022.183","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T07:56:52Z","timestamp":1777449412000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.sagepub.com\/doi\/10.1089\/hum.2022.183"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3]]},"references-count":44,"journal-issue":{"issue":"5-6","published-print":{"date-parts":[[2023,3]]}},"alternative-id":["10.1089\/hum.2022.183"],"URL":"https:\/\/doi.org\/10.1089\/hum.2022.183","relation":{},"ISSN":["1043-0342","1557-7422"],"issn-type":[{"value":"1043-0342","type":"print"},{"value":"1557-7422","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3]]}}}