Risk of infection in patients with hematological malignancies receiving CAR T-cell therapy: systematic review and meta-analysis

References

• Auberger P, Tamburini-Bonnefoy J, Puissant A. Drug resistance in hematological malignancies. Int J Mol Sci. 2020 Aug 24;21(17):6091.
   Web of Science ®Google Scholar
• Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018 Nov;68(6):394–424.
   PubMed Web of Science ®Google Scholar
• Holstein SA, Lunning MA. CAR T-cell therapy in hematologic malignancies: a voyage in progress. Clin Pharmacol Ther. 2020 Jan;107(1):112–122.
   PubMed Web of Science ®Google Scholar
• Selim AG, Minson A, Blombery P, et al. CAR-T cell therapy: practical guide to routine laboratory monitoring. Pathology. 2021 Apr;53(3):408–415.
   PubMed Web of Science ®Google Scholar
• Miliotou AN, Papadopoulou LC. CAR T-cell therapy: a new era in cancer immunotherapy. Curr Pharm Biotechnol. 2018;19(1):5–18.
   PubMed Web of Science ®Google Scholar
• Sadelain M, Brentjens R, Riviere I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013 Apr;3(4):388–398.
   PubMed Web of Science ®Google Scholar
• Mehrabadi AZ, Ranjbar R, Farzanehpour M, et al. Therapeutic potential of CAR T cell in malignancies: a scoping review. Biomed Pharmacother. 2022 Feb;146:112512.
   PubMed Web of Science ®Google Scholar
• June CH, O’Connor RS, Kawalekar OU, et al. CAR T cell immunotherapy for human cancer. Science. 2018 Mar 23;359(6382):1361–1365.
   PubMed Web of Science ®Google Scholar
• Boyiadzis MM, Dhodapkar MV, Brentjens RJ, et al. Chimeric antigen receptor (CAR) T therapies for the treatment of hematologic malignancies: clinical perspective and significance. J Immunother Cancer. 2018 Dec 4;6(1):137.
   PubMed Web of Science ®Google Scholar
• Meng J, Wu X, Sun Z, et al. Efficacy and safety of CAR-T cell products axicabtagene ciloleucel, tisagenlecleucel, and lisocabtagene maraleucel for the treatment of hematologic malignancies: a systematic review and meta-analysis. Front Oncol. 2021;11:698607.
   PubMed Web of Science ®Google Scholar
• Chmielewski M, Abken H. TRUCKs: the fourth generation of CARs. Expert Opin Biol Ther. 2015;15(8):1145–1154.
   PubMed Web of Science ®Google Scholar
• Haslauer T, Greil R, Zaborsky N, et al. CAR T-cell therapy in hematological malignancies. Int J Mol Sci. 2021 Aug 20;22(16):8996.
   PubMed Web of Science ®Google Scholar
• Mueller KT, Maude SL, Porter DL, et al. Cellular kinetics of CTL019 in relapsed/refractory B-cell acute lymphoblastic leukemia and chronic lymphocytic leukemia. Blood. 2017 Nov 23;130(21):2317–2325.
   PubMed Web of Science ®Google Scholar
• Landoni E, Savoldo B. Treating hematological malignancies with cell therapy: where are we now? Expert Opin Biol Ther. 2018 Jan;18(1):65–75.
   PubMed Web of Science ®Google Scholar
• Stewart AG, Henden AS. Infectious complications of CAR T-cell therapy: a clinical update. Ther Adv Infect Dis. 2021 Jan-Dec;8:20499361211036773.
   Web of Science ®Google Scholar
• Neelapu SS, Locke FL, Bartlett NL, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017 Dec 28;377(26):2531–2544.
   PubMed Web of Science ®Google Scholar
• Maude SL, Laetsch TW, Buechner J, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018 Feb 1;378(5):439–448.
   PubMed Web of Science ®Google Scholar
• Wang M, Munoz J, Goy A, et al. KTE-X19 CAR T-cell therapy in relapsed or refractory mantle-cell lymphoma. N Engl J Med. 2020 Apr 2;382(14):1331–1342.
   PubMed Web of Science ®Google Scholar
• Raje N, Berdeja J, Lin Y, et al. Anti-BCMA CAR T-cell therapy bb2121 in relapsed or refractory multiple myeloma. N Engl J Med. 2019 May 2;380(18):1726–1737.
   PubMed Web of Science ®Google Scholar
• Schuster SJ, Bishop MR, Tam CS, et al. Tisagenlecleucel in adult relapsed or refractory diffuse large B-cell lymphoma. N Engl J Med. 2019 Jan 3;380(1):45–56.
   PubMed Web of Science ®Google Scholar
• Berdeja JG, Madduri D, Usmani SZ, et al. Ciltacabtagene autoleucel, a B-cell maturation antigen-directed chimeric antigen receptor T-cell therapy in patients with relapsed or refractory multiple myeloma (CARTITUDE-1): a phase 1b/2 open-label study. Lancet. 2021 Jul 24;398(10297):314–324.
   PubMed Web of Science ®Google Scholar
• Sadeqi Nezhad M, Seifalian A, Bagheri N, et al. Chimeric antigen receptor based therapy as a potential approach in autoimmune diseases: how close are we to the treatment? Front Immunol. 2020;11:603237.
   PubMed Web of Science ®Google Scholar
• Zmievskaya E, Valiullina A, Ganeeva I, et al. Application of CAR-T cell therapy beyond Oncology: autoimmune diseases and viral infections. Biomedicines. 2021 Jan 9;9(1):59.
   PubMed Web of Science ®Google Scholar
• Luo W, Li C, Zhang Y, et al. Adverse effects in hematologic malignancies treated with chimeric antigen receptor (CAR) T cell therapy: a systematic review and Meta-analysis. BMC Cancer. 2022 Jan 24;22(1):98.
   PubMed Web of Science ®Google Scholar
• Yang Q, Li X, Zhang F, et al. Efficacy and safety of CAR-T therapy for relapse or refractory multiple myeloma: a systematic review and meta-analysis. Int J Med Sci. 2021;18(8):1786–1797.
   PubMed Web of Science ®Google Scholar
• Wang N, Meng Y, Wu Y, et al. Efficacy and safety of chimeric antigen receptor T cell immunotherapy in B-cell non-Hodgkin lymphoma: a systematic review and meta-analysis. Immunotherapy. 2021 Mar;13(4):345–357.
   PubMed Web of Science ®Google Scholar
• Xu X, Chen S, Zhao Z, et al. Consolidative hematopoietic stem cell transplantation after CD19 CAR-T cell therapy for acute lymphoblastic leukemia: a systematic review and meta-analysis. Front Oncol. 2021;11:651944.
   PubMed Web of Science ®Google Scholar
• Aamir S, Anwar MY, Khalid F, et al. Systematic review and meta-analysis of CD19-specific CAR-T cell therapy in relapsed/refractory acute lymphoblastic leukemia in the pediatric and young adult population: safety and efficacy outcomes. Clin Lymphoma Myeloma Leuk. 2021 Apr;21(4):e334–e347.
   PubMed Web of Science ®Google Scholar
• Dolladille C, Ederhy S, Ezine E, et al. Chimeric antigen receptor T-cells safety: a pharmacovigilance and meta-analysis study. Am J Hematol. 2021 Sep 1;96(9):1101–1111.
   PubMed Web of Science ®Google Scholar
• Brudno JN, Kochenderfer JN. Recent advances in CAR T-cell toxicity: mechanisms, manifestations and management. Blood Rev. 2019 Mar;34:45–55.
   PubMed Web of Science ®Google Scholar
• Maus MV, Lionakis MS. Infections associated with the new ‘nibs and mabs’ and cellular therapies. Curr Opin Infect Dis. 2020 Aug;33(4):281–289.
   PubMed Web of Science ®Google Scholar
• Brudno JN, Kochenderfer JN. Toxicities of chimeric antigen receptor T cells: recognition and management. Blood. 2016 Jun 30;127(26):3321–3330.
   PubMed Web of Science ®Google Scholar
• Fried S, Avigdor A, Bielorai B, et al. Early and late hematologic toxicity following CD19 CAR-T cells. Bone Marrow Transplant. 2019 Oct;54(10):1643–1650.
   PubMed Web of Science ®Google Scholar
• Neelapu SS, Tummala S, Kebriaei P, et al. Chimeric antigen receptor T-cell therapy - assessment and management of toxicities. Nat Rev Clin Oncol. 2018 Jan;15(1):47–62.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009 Oct;62(10):1006–1012.
   PubMed Web of Science ®Google Scholar
• Wells GSB, O’Connell D, Peterson J, et al. The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses July 22, 2022 https://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
   Google Scholar
• Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003 Sep 6;327(7414):557–560.
   PubMed Web of Science ®Google Scholar
• Ramos CA, Grover NS, Beaven AW, et al. Anti-CD30 CAR-T cell therapy in relapsed and refractory Hodgkin lymphoma. J Clin Oncol. 2020 Nov 10;38(32):3794–3804.
   PubMed Web of Science ®Google Scholar
• Locke FL, Ghobadi A, Jacobson CA, et al. Long-term safety and activity of axicabtagene ciloleucel in refractory large B-cell lymphoma (ZUMA-1): a single-arm, multicentre, phase 1-2 trial. Lancet Oncol. 2019 Jan;20(1):31–42.
   PubMed Web of Science ®Google Scholar
• Tong C, Zhang Y, Liu Y, et al. Optimized tandem CD19/CD20 CAR-engineered T cells in refractory/relapsed B-cell lymphoma. Blood. 2020 Oct 1;136(14):1632–1644.
   PubMed Web of Science ®Google Scholar
• Abramson JS, Palomba ML, Gordon LI, et al. Lisocabtagene maraleucel for patients with relapsed or refractory large B-cell lymphomas (TRANSCEND NHL 001): a multicentre seamless design study. Lancet. 2020 Sep 19;396(10254):839–852.
   PubMed Web of Science ®Google Scholar
• Locke FL, Miklos DB, Jacobson CA, et al. Axicabtagene Ciloleucel as Second-Line Therapy for Large B-Cell Lymphoma. N Engl J Med. 2022 Feb 17;386(7):640–654.
   PubMed Web of Science ®Google Scholar
• Shah BD, Ghobadi A, Oluwole OO, et al. KTE-X19 for relapsed or refractory adult B-cell acute lymphoblastic leukaemia: phase 2 results of the single-arm, open-label, multicentre ZUMA-3 study. Lancet. 2021 Aug 7;398(10299):491–502.
   PubMed Web of Science ®Google Scholar
• Cappell KM, Sherry RM, Yang JC, et al. Long-term follow-up of anti-CD19 chimeric antigen receptor T-cell therapy. J Clin Oncol. 2020 Nov 10;38(32):3805–3815.
   PubMed Web of Science ®Google Scholar
• Hu Y, Zhou Y, Zhang M, et al. CRISPR/Cas9-engineered universal CD19/CD22 dual-targeted CAR-T cell therapy for relapsed/refractory B-cell acute lymphoblastic leukemia. Clin Cancer Res. 2021 May 15;27(10):2764–2772.
   PubMed Web of Science ®Google Scholar
• Hill JA, Li D, Hay KA, et al. Infectious complications of CD19-targeted chimeric antigen receptor-modified T-cell immunotherapy. Blood. 2018 Jan 4;131(1):121–130.
   PubMed Web of Science ®Google Scholar
• Azoulay E, Castro P, Maamar A, et al. Outcomes in patients treated with chimeric antigen receptor T-cell therapy who were admitted to intensive care (CARTTAS): an international, multicentre, observational cohort study. Lancet Haematol. 2021 May;8(5):e355–e364.
   PubMed Web of Science ®Google Scholar
• Schuster SJ, Tam CS, Borchmann P, et al. Long-term clinical outcomes of tisagenlecleucel in patients with relapsed or refractory aggressive B-cell lymphomas (JULIET): a multicentre, open-label, single-arm, phase 2 study. Lancet Oncol. 2021 Oct;22(10):1403–1415.
   PubMed Web of Science ®Google Scholar
• Wang D, Wang J, Hu G, et al. A phase 1 study of a novel fully human BCMA-targeting CAR (CT103A) in patients with relapsed/refractory multiple myeloma. Blood. 2021 May 27;137(21):2890–2901.
   PubMed Web of Science ®Google Scholar
• Baumeister SH, Murad J, Werner L, et al. Phase I trial of autologous CAR T cells targeting NKG2D Ligands in patients with AML/MDS and multiple myeloma. Cancer Immunol Res. 2019 Jan;7(1):100–112.
   PubMed Web of Science ®Google Scholar
• Yan Z, Cao J, Cheng H, et al. A combination of humanised anti-CD19 and anti-BCMA CAR T cells in patients with relapsed or refractory multiple myeloma: a single-arm, phase 2 trial. Lancet Haematol. 2019 Oct;6(10):e521–e529.
   PubMed Web of Science ®Google Scholar
• Zhou X, Tu S, Wang C, et al. Phase I trial of fourth-generation anti-CD19 chimeric antigen receptor T cells against relapsed or refractory B cell non-Hodgkin lymphomas. Front Immunol. 2020;11:564099.
   PubMed Web of Science ®Google Scholar
• Jacobson CA, Chavez JC, Sehgal AR, et al. Axicabtagene ciloleucel in relapsed or refractory indolent non-Hodgkin lymphoma (ZUMA-5): a single-arm, multicentre, phase 2 trial. Lancet Oncol. 2022 Jan;23(1):91–103.
   PubMed Web of Science ®Google Scholar
• Gaut D, Tang K, Sim MS, et al. Filgrastim associations with CAR T-cell therapy. Int J Cancer. 2021 Mar 1;148(5):1192–1196.
   PubMed Web of Science ®Google Scholar
• Zettler ME, Feinberg BA, Phillips EG Jr., et al. Real-world adverse events associated with CAR T-cell therapy among adults age>/=65years. J Geriatr Oncol. 2021 Mar;12(2):239–242.
   PubMed Web of Science ®Google Scholar
• Wittmann Dayagi T, Sherman G, Bielorai B, et al. Characteristics and risk factors of infections following CD28-based CD19 CAR-T cells. Leuk Lymphoma. 2021 Jul;62(7):1692–1701.
   PubMed Web of Science ®Google Scholar
• Wu J, Meng F, Cao Y, et al. Sequential CD19/22 CAR T-cell immunotherapy following autologous stem cell transplantation for central nervous system lymphoma. Blood Cancer J. 2021 Jul 15;11(7):131.
   PubMed Web of Science ®Google Scholar
• Ramos CA, Ballard B, Zhang H, et al. Clinical and immunological responses after CD30-specific chimeric antigen receptor-redirected lymphocytes. J Clin Invest. 2017 Sep 1;127(9):3462–3471.
   PubMed Web of Science ®Google Scholar
• Li C, Cao W, Que Y, et al. A phase I study of anti-BCMA CAR T cell therapy in relapsed/refractory multiple myeloma and plasma cell leukemia. Clin Transl Med. 2021 Mar;11(3):e346.
   PubMed Web of Science ®Google Scholar
• Cui R, Lyu C, Li Q, et al. Humanized anti-CD19 chimeric antigen receptor-T cell therapy is safe and effective in lymphoma and leukemia patients with chronic and resolved hepatitis B virus infection. Hematol Oncol. 2021 Feb;39(1):75–86.
   PubMed Web of Science ®Google Scholar
• Li P, Zhou L, Ye S, et al. Risk of HBV reactivation in patients with resolved HBV infection receiving anti-CD19 chimeric antigen receptor T cell therapy without antiviral prophylaxis. Front Immunol. 2021;12:638678.
   PubMed Web of Science ®Google Scholar
• Li C, Zhang Y, Zhang C, et al. Comparation of CART19 and autologous stem-cell transplantation for refractory/relapsed non-Hodgkin’s lymphoma. JCI Insight. 2019 Jul 23;5(17);e130195.
   Google Scholar
• Zeng C, Cheng J, Li T, et al. Efficacy and toxicity for CD22/CD19 chimeric antigen receptor T-cell therapy in patients with relapsed/refractory aggressive B-cell lymphoma involving the gastrointestinal tract. Cytotherapy. 2020 Mar;22(3):166–171.
   PubMed Web of Science ®Google Scholar
• Wudhikarn K, Palomba ML, Pennisi M, et al. Infection during the first year in patients treated with CD19 CAR T cells for diffuse large B cell lymphoma. Blood Cancer J. 2020 Aug 5;10(8):79.
   PubMed Web of Science ®Google Scholar
• Park JH, Romero FA, Taur Y, et al. Cytokine release syndrome grade as a predictive marker for infections in patients with relapsed or refractory B-cell acute lymphoblastic leukemia treated with chimeric antigen receptor T cells. Clin Infect Dis. 2018 Aug 1;67(4):533–540.
   PubMed Web of Science ®Google Scholar
• Kochenderfer JN, Somerville RPT, Lu T, et al. Long-duration complete remissions of diffuse large B cell lymphoma after anti-CD19 chimeric antigen receptor T cell therapy. Mol Ther. 2017 Oct 4;25(10):2245–2253.
   PubMed Web of Science ®Google Scholar
• Zhang H, Liu M, Li Q, et al. Evaluation of the safety and efficacy of humanized anti-CD19 chimeric antigen receptor T-cell therapy in older patients with relapsed/refractory diffuse large B-cell lymphoma based on the comprehensive geriatric assessment system. Leuk Lymphoma. 2022 Feb;63(2):353–361.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wang Y, Liu Y, et al. Long-term activity of tandem CD19/CD20 CAR therapy in refractory/relapsed B-cell lymphoma: a single-arm, phase 1-2 trial. Leukemia. 2022 Jan;36(1):189–196.
   PubMed Web of Science ®Google Scholar
• Beyar-Katz O, Kikozashvili N, Bar OY, et al. Characteristics and recognition of early infections in patients treated with commercial anti-CD19 CAR-T cells. Eur J Haematol. 2022 Jan;108(1):52–60.
   PubMed Web of Science ®Google Scholar
• Ortiz-Maldonado V, Frigola G, Espanol-Rego M, et al. Results of ARI-0001 CART19 cells in patients with chronic lymphocytic leukemia and Richter’s transformation. Front Oncol. 2022;12:828471.
   PubMed Web of Science ®Google Scholar
• Thakkar A, Cui Z, Peeke SZ, et al. Patterns of leukocyte recovery predict infectious complications after CD19 CAR-T cell therapy in a real-world setting. Stem Cell Investig. 2021;8:18.
   PubMedGoogle Scholar
• Cornell RF, Bishop MR, Kumar S, et al. A phase 1, multicenter study evaluating the safety and efficacy of KITE-585, an autologous anti-BCMA CAR T-cell therapy, in patients with relapsed/refractory multiple myeloma. Am J Cancer Res. 2021;11(6):3285–3293.
   PubMed Web of Science ®Google Scholar
• Korell F, Schubert ML, Sauer T, et al. Infection complications after lymphodepletion and dosing of chimeric antigen receptor T (CAR-T) cell therapy in patients with relapsed/refractory acute lymphoblastic leukemia or B cell non-Hodgkin lymphoma. Cancers (Basel). 2021 Apr 2;13(7):1684.
   PubMed Web of Science ®Google Scholar
• Huang C, Wu L, Liu R, et al. Efficacy and safety of CD19 chimeric antigen receptor T cells in the treatment of 11 patients with relapsed/refractory B-cell lymphoma: a single-center study. Ann Transl Med. 2020 Sep;8(17):1048.
   PubMed Web of Science ®Google Scholar
• Logue JM, Zucchetti E, Bachmeier CA, et al. Immune reconstitution and associated infections following axicabtagene ciloleucel in relapsed or refractory large B-cell lymphoma. Haematologica. 2021 Apr 1;106(4):978–986.
   PubMed Web of Science ®Google Scholar
• Baird JH, Epstein DJ, Tamaresis JS, et al. Immune reconstitution and infectious complications following axicabtagene ciloleucel therapy for large B-cell lymphoma. Blood Adv. 2021 Jan 12;5(1):143–155.
   PubMed Web of Science ®Google Scholar
• Munshi NC, Anderson LD Jr., Shah N, et al. Idecabtagene vicleucel in relapsed and refractory multiple myeloma. N Engl J Med. 2021 Feb 25;384(8):705–716.
   PubMed Web of Science ®Google Scholar
• Cordeiro A, Bezerra ED, Hirayama AV, et al. Late events after treatment with CD19-targeted chimeric antigen receptor modified T cells. Biol Blood Marrow Transplant. 2020 Jan;26(1):26–33.
   PubMed Web of Science ®Google Scholar
• Avery DT, Kalled SL, Ellyard JI, et al. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J Clin Invest. 2003 Jul;112(2):286–297.
   PubMed Web of Science ®Google Scholar
• Chiu A, Xu W, He B, et al. Hodgkin lymphoma cells express TACI and BCMA receptors and generate survival and proliferation signals in response to BAFF and April. Blood. 2007 Jan 15;109(2):729–739.
   PubMed Web of Science ®Google Scholar
• Miller BC, Maus MV. CD19-targeted CAR T cells: a new tool in the fight against B cell malignancies. Oncol Res Treat. 2015;38(12):683–690.
   PubMed Web of Science ®Google Scholar
• Pratt G, Goodyear O, Moss P. Immunodeficiency and immunotherapy in multiple myeloma. Br J Haematol. 2007 Sep;138(5):563–579.
   PubMed Web of Science ®Google Scholar
• Atanackovic D, Luetkens T, Omili D, et al. Vaccine-induced T-cell responses against SARS-CoV-2 and its Omicron variant in patients with B cell-depleted lymphoma after CART therapy. Blood. 2022 Jul 14;140(2):152–156.
   PubMed Web of Science ®Google Scholar
• Oh BLZ, Tan N, de Alwis R, et al. Enhanced BNT162b2 vaccine-induced cellular immunity in anti-CD19 CAR T cell-treated patients. Blood. 2022 Jul 14;140(2):156–160.
   PubMed Web of Science ®Google Scholar
• Gudiol C, Lewis RE, Strati P, et al. Chimeric antigen receptor T-cell therapy for the treatment of lymphoid malignancies: is there an excess risk for infection? Lancet Haematol. 2021 Mar;8(3):e216–e228.
   PubMed Web of Science ®Google Scholar
• Vora SB, Waghmare A, Englund JA, et al. Infectious complications following CD19 chimeric antigen receptor T-cell therapy for children, adolescents, and young adults. Open Forum Infect Dis. 2020 May;7(5):ofaa121.
   PubMed Web of Science ®Google Scholar
• Cornely OA, Aversa F, Cook P, et al. Evaluating the role of prophylaxis in the management of invasive fungal infections in patients with hematologic malignancy. Eur J Haematol. 2011 Oct;87(4):289–301.
   PubMed Web of Science ®Google Scholar
• Budde LE, Zaia JA. CD19 CAR-T therapy and sepsis: dancing with the devil. Blood. 2018 Jan 4;131(1):7–8.
   PubMed Web of Science ®Google Scholar
• Ueda M, Berger M, Gale RP, et al. Immunoglobulin therapy in hematologic neoplasms and after hematopoietic cell transplantation. Blood Rev. 2018 Mar;32(2):106–115.
   PubMed Web of Science ®Google Scholar
• Tau N, Shargian-Alon L, Reich S, et al. Reporting infections in clinical trials of patients with haematological malignancies. Clin Microbiol Infect. 2019 Dec;25(12):1494–1500.
   PubMed Web of Science ®Google Scholar