Hematopoiesis and immune reconstitution after CD19 directed chimeric antigen receptor T-cells (CAR-T): A comprehensive review on incidence, risk factors and current management.
CAR-T cells
cytopenia
hematopoiesis
hypogammaglobulinemia
Journal
European journal of haematology
ISSN: 1600-0609
Titre abrégé: Eur J Haematol
Pays: England
ID NLM: 8703985
Informations de publication
Date de publication:
25 Jul 2023
25 Jul 2023
Historique:
revised:
10
07
2023
received:
02
06
2023
accepted:
10
07
2023
medline:
26
7
2023
pubmed:
26
7
2023
entrez:
26
7
2023
Statut:
aheadofprint
Résumé
Impaired function of hematopoiesis after treatment with chimeric antigen T-cells (CAR-T) is a frequent finding and can interest a wide range of patients, regardless of age and underlying disease. Trilinear cytopenias, as well as hypogammaglobulinemia, B-cell aplasia, and T-cell impairment, can severely affect the infectious risk of CAR-T recipients, as well as their quality of life. In this review, we provide an overview of defects in hematopoiesis after CAR-T, starting with a summary of different definitions and thresholds. We then move to summarize the main pathogenetic mechanisms of cytopenias, and we offer insight into cytomorphological aspects, the role of clonal hematopoiesis, and the risk of secondary myeloid malignancies. Subsequently, we expose the major findings and reports on T-cell and B-cell quantitative and functional impairment after CAR-T. Finally, we provide an overview of current recommendations and leading experiences regarding the management of cytopenias and defective B- and T-cell function.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Centro di Ricerca sulle cellule staminali emopoietiche e le terapie cellulari, Università Cattolica del Sacro Cuore, Roma
Informations de copyright
© 2023 The Authors. European Journal of Haematology published by John Wiley & Sons Ltd.
Références
Lemoine J, Bachy E, Cartron G, et al. Causes and risk factors of early and late non-relapse mortality after CD19 CAR T-cell therapy for diffuse large B-cell lymphoma (DLBCL): a Lysa study from the Descar-T registry. Blood. 2022;140(Suppl 1):1859-1861. https://www.researchgate.net/publication/365828112_Causes_and_Risk_Factors_of_Early_and_Late_Non-Relapse_Mortality_after_CD19_CAR_T-Cell_Therapy_for_Diffuse_Large_B-Cell_Lymphoma_DLBCL_A_Lysa_Study_from_the_Descar-T_Registry
Johnsrud A, Craig J, Baird J, et al. Incidence and risk factors associated with bleeding and thrombosis following chimeric antigen receptor T-cell therapy. Blood Adv. 2021;5(21):4465-4475. https://ashpublications.org/bloodadvances/article/5/21/4465/476900/Incidence-and-risk-factors-associated-with
Nahas GR, Komanduri KV, Pereira D, et al. Incidence and risk factors associated with a syndrome of persistent cytopenias after CAR-T cell therapy (PCTT). Leuk Lymphoma. 2020;61(4):940-943. https://pubmed.ncbi.nlm.nih.gov/31793821/
Taneja A, Jain T, Correspondence T, Jain S. CAR-T-OPENIA: chimeric antigen receptor T-cell therapy-associated cytopenias. EJHaem. 2021;3(Suppl 1):32-38. doi:10.1002/jha2.350
Rejeski K, Aljurf King Faisal Specialist Hospital M, Arabia Emmanuel Bachy S, et al. Immune effector cell-associated hematotoxicity (ICAHT): EHA/EBMT consensus grading and best practice recommendations. Blood. 2023. doi:10.1182/blood.2023020578/2056087/blood.2023020578.pdf
Rejeski K, Perez A, Sesques P, et al. CAR-HEMATOTOX: a model for CAR T-cell-related hematologic toxicity in relapsed/refractory large B-cell lymphoma. Blood. 2021;138(24):2499-2513. https://pubmed.ncbi.nlm.nih.gov/34166502/
Jain T, Olson TS, Locke FL. How I treat cytopenias after CAR-T cell therapy. Blood. 2023;141(20):2460-2469. https://pubmed.ncbi.nlm.nih.gov/36800563/
Fried S, Avigdor A, Bielorai B, et al. Early and late hematologic toxicity following CD19 CAR-T cells. Bone Marrow Transplant. 2019;54(10):1643-1650. https://pubmed.ncbi.nlm.nih.gov/30809033/
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;26(1):26-33. https://pubmed.ncbi.nlm.nih.gov/31419568/
Strati P, Varma A, Adkins S, et al. Hematopoietic recovery and immune reconstitution after axicabtagene ciloleucel in patients with large B-cell lymphoma. Haematologica. 2021;106(10):2667-2672. https://pubmed.ncbi.nlm.nih.gov/32732355/
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;396(10254):839-852. https://pubmed.ncbi.nlm.nih.gov/32888407/
Jain T, Knezevic A, Pennisi M, et al. Hematopoietic recovery in patients receiving chimeric antigen receptor T-cell therapy for hematologic malignancies. Blood Adv. 2020;4(15):3776-3787. https://pubmed.ncbi.nlm.nih.gov/32780846/
Juluri KR, Wu QV, Voutsinas J, et al. Severe cytokine release syndrome is associated with hematologic toxicity following CD19 CAR T-cell therapy. Blood Adv. 2022;6(7):2055-2068. https://pubmed.ncbi.nlm.nih.gov/34666344/
Liévin R, Di Blasi R, Morin F, et al. Effect of early granulocyte-colony-stimulating factor administration in the prevention of febrile neutropenia and impact on toxicity and efficacy of anti-CD19 CAR-T in patients with relapsed/refractory B-cell lymphoma. Bone Marrow Transplant. 2022;57(3):431-439. https://pubmed.ncbi.nlm.nih.gov/35094012/
Zhou J, Zhang Y, Shan M, et al. Cytopenia after chimeric antigen receptor T cell immunotherapy in relapsed or refractory lymphoma. Front Immunol. 2022;13:997589. https://pubmed.ncbi.nlm.nih.gov/36131934/
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;23(1):91-103. https://pubmed.ncbi.nlm.nih.gov/34895487/
Teipel R, Kroschinsky F, Kramer M, et al. Prevalence and variation of CHIP in patients with aggressive lymphomas undergoing CD19-directed CAR T-cell treatment. Blood Adv. 2022;6(6):1941-1946. https://pubmed.ncbi.nlm.nih.gov/35008107/
Penack O, Peczynski C, Koenecke C, et al. Severe cytopenia after CD19 CAR T-cell therapy: a retrospective study from the EBMT transplant complications working party. J Immunother Cancer. 2023;11(4):e006406. https://pubmed.ncbi.nlm.nih.gov/37072350/
Iqbal M, Bansal R, Yassine F, et al. Impact of rituximab and corticosteroids on late Cytopenias post-chimeric antigen receptor T cell therapy. Transplant Cell Ther. 2022;28(10):668.e1-668.e6. https://pubmed.ncbi.nlm.nih.gov/35842124/
Kitamura W, Asada N, Naoi Y, et al. Bone marrow microenvironment disruption and sustained inflammation with prolonged haematologic toxicity after CAR T-cell therapy. Br J Haematol. 2023;202(2):294-307. https://pubmed.ncbi.nlm.nih.gov/36890790/
Mullanfiroze K, Lazareva A, Chu J, et al. CD34+-selected stem cell boost can safely improve cytopenias following CAR T-cell therapy. Blood Adv. 2022;6(16):4715-4718. https://pubmed.ncbi.nlm.nih.gov/35790110/
Wang J, Zhang M, Lyu H, et al. Low-dose administration of prednisone has a good effect on the treatment of prolonged hematologic toxicity post-CD19 CAR-T cell therapy. Front Immunol. 2023;14(14):1139559.
Kuhnl A, Kirkwood AA, Roddie C, et al. CAR T in patients with large B-cell lymphoma not fit for autologous transplant. Br J Haematol. 2023. https://pubmed.ncbi.nlm.nih.gov/37082780/;202:65-73.
Wang L, Hong R, Zhou L, et al. New-onset severe cytopenia after CAR-T cell therapy: analysis of 76 patients with relapsed or refractory acute lymphoblastic leukemia. Front Oncol. 2021;11(1-10):702644. https://pubmed.ncbi.nlm.nih.gov/34277448/
Wudhikarn K, Pennisi M, Garcia-Recio M, et al. DLBCL patients treated with CD19 CAR T cells experience a high burden of organ toxicities but low nonrelapse mortality. Blood Adv. 2020;4(13):3024-3033. https://pubmed.ncbi.nlm.nih.gov/32614964/
Guo H, Qian L, Cui J. Focused evaluation of the roles of macrophages in chimeric antigen receptor (CAR) T cell therapy associated cytokine release syndrome. Cancer Biol Med. 2021;19(3):333-342. https://pubmed.ncbi.nlm.nih.gov/34570442/
Hines MR, Knight TE, McNerney KO, et al. Immune effector cell-associated hemophagocytic lymphohistiocytosis-like syndrome. Transplant Cell Ther. 2023;29(7):438. https://pubmed.ncbi.nlm.nih.gov/36906275/
Morales-Mantilla DE, King KY. The role of interferon-gamma in hematopoietic stem cell development, homeostasis, and disease. Curr Stem Cell Rep. 2018;4(3):264-271. https://pubmed.ncbi.nlm.nih.gov/30148048/
Feng X, Scheinberg P, Wu CO, et al. Cytokine signature profiles in acquired aplastic anemia and myelodysplastic syndromes. Haematologica. 2011;96(4):602-606. https://pubmed.ncbi.nlm.nih.gov/21160069/
Teachey DT, Lacey SF, Shaw PA, et al. Identification of predictive biomarkers for cytokine release syndrome after chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Cancer Discov. 2016;6(6):664-679. https://pubmed.ncbi.nlm.nih.gov/27076371/
Alvarado LJ, Huntsman HD, Cheng H, et al. Eltrombopag maintains human hematopoietic stem and progenitor cells under inflammatory conditions mediated by IFN-γ. Blood. 2019;133(19):2043 PMC6509545.
Zhou L, Fu W, Wu S, et al. Derivation and validation of a novel score for early prediction of severe CRS after CAR-T therapy in haematological malignancy patients: a multi-centre study. Br J Haematol. 2023;1-8. https://pubmed.ncbi.nlm.nih.gov/37192741/
Savoldo B, Ramos CA, Liu E, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest. 2011;121(5):1822-1826. https://pubmed.ncbi.nlm.nih.gov/21540550/
Hines MR, Keenan C, Maron Alfaro G, et al. Hemophagocytic lymphohistiocytosis-like toxicity (carHLH) after CD19-specific CAR T-cell therapy. Br J Haematol. 2021;194(4):701-707. https://pubmed.ncbi.nlm.nih.gov/34263927/
Lichtenstein DA, Schischlik F, Shao L, et al. Characterization of HLH-like manifestations as a CRS variant in patients receiving CD22 CAR T cells. Blood. 2021;138(24):2469-2484. https://pubmed.ncbi.nlm.nih.gov/34525183/
Wudhikarn K, Perales MA. Infectious complications, immune reconstitution, and infection prophylaxis after CD19 chimeric antigen receptor T-cell therapy. Bone Marrow Transplant. 2022;57(10):1477-1488. https://pubmed.ncbi.nlm.nih.gov/35840746/
Hill JA, Li D, Hay KA, et al. Infectious complications of CD19-targeted chimeric antigen receptor-modified T-cell immunotherapy. Blood. 2018;131(1):121-130. https://pubmed.ncbi.nlm.nih.gov/29038338/
Du M, Huang L, Kou H, Li C, Hu Y, Mei H. Case report: ITP treatment after CAR-T cell Therapy in patients with multiple myeloma. Front Immunol. 2022;13:898341. https://pubmed.ncbi.nlm.nih.gov/35784357/
Wu MS, Koirala A. Thrombotic microangiopathy following chimeric antigen receptor T-cell therapy. Clin Nephrol Case Stud. 2023;11(1):17-21. https://pubmed.ncbi.nlm.nih.gov/36844260/
Galli E, Bellesi S, Viscovo M, et al. Cytomorphology of chimeric antigen receptor T-cells (CAR-T). Mediterr J Hematol Infect Dis. 2021;13(1):e2021066. https://pubmed.ncbi.nlm.nih.gov/34804440/
Brooks S, Frey N, Porter D, June C, Lacey S, Bagg A. The cytological features of CAR(T) cells. Br J Haematol. 2016;175:366. https://pubmed.ncbi.nlm.nih.gov/27612286/
Han X, Wang C, Zhou J. Chimeric antigen receptor T (CAR-T) cells present with reactive and pleomorphic morphology in bone marrow. Am J Hematol. 2019;94:1297-1298. https://pubmed.ncbi.nlm.nih.gov/31124159/
Faude S, Wei J, Muralidharan K, et al. Absolute lymphocyte count proliferation kinetics after CAR T-cell infusion impact response and relapse. Blood Adv. 2021;5(8):2128-2136. https://pubmed.ncbi.nlm.nih.gov/33881465/
Qasrawi A, Arora R, Ramlal R, Munker R, Hildebrandt GC. Allogenic hematopoietic stem cell transplantation for prolonged bone marrow aplasia after chimeric antigen receptor (CAR) T-cell therapy for relapsed diffuse large B-cell lymphoma. Am J Hematol. 2020;95(4):E89-E91.
Chandra H, Chandra S, Bhat NK, Sharma A. Clinicohaematological profile of infections in bone marrow - single centre experience in north Himalayan region of India. Hematology. 2011;16(4):255-257. https://pubmed.ncbi.nlm.nih.gov/21756544/
Laurenti L, Chiusolo P, Garzia MG, et al. Periodic morphologic, cytogenetic and clonality evaluation after autologous peripheral blood progenitor cell transplantation in patients with lymphoproliferative malignancies. Haematologica. 2002;87(1):59-66. https://pubmed.ncbi.nlm.nih.gov/11801466/
Frioni F, Galli E, Sorà F, Zini G, Sica S, Chiusolo P. Spontaneous resolution of “therapy-related myelodysplasia” occurred after treatment with CAR-T cells: all that glitters is not gold. Int J Lab Hematol [Internet]. 2023. doi:10.1111/ijlh.14099
Mangaonkar AA, Patnaik MM. Clonal hematopoiesis of indeterminate potential and clonal cytopenias of undetermined significance: 2023 update on clinical associations and management recommendations. Am J Hematol. 2023. https://pubmed.ncbi.nlm.nih.gov/36938794/;98:951-964.
Guermouche H, Ravalet N, Gallay N, et al. High prevalence of clonal hematopoiesis in the blood and bone marrow of healthy volunteers. Blood Adv. 2020;4(15):3550-3557. https://pubmed.ncbi.nlm.nih.gov/32761230/
von Bonin M, Jambor HK, Teipel R, et al. Clonal hematopoiesis and its emerging effects on cellular therapies. Leukemia. 2021;35(10):2752-2758. https://pubmed.ncbi.nlm.nih.gov/34215849/
Reinhardt B, Lee P, Sasine JP. Chimeric antigen receptor T-cell therapy and hematopoiesis. Cells. 2023;12(4):531. https://pubmed.ncbi.nlm.nih.gov/36831198/
Miller PG, Sperling AS, Brea EJ, et al. Clonal hematopoiesis in patients receiving chimeric antigen receptor T-cell therapy. Blood Adv. 2021;5(15):2982-2986. https://pubmed.ncbi.nlm.nih.gov/34342642/
Saini NY, Swoboda DM, Greenbaum U, et al. Clonal hematopoiesis is associated with increased risk of severe neurotoxicity in Axicabtagene Ciloleucel therapy of large B-cell lymphoma. Blood Cancer Discov. 2022;3(5):385-393. https://pubmed.ncbi.nlm.nih.gov/35533245/
Gamper CJ, Agoston AT, Nelson WG, Powell JD. Identification of DNA methyltransferase 3a as a T cell receptor-induced regulator of Th1 and Th2 differentiation. J Immunol. 2009;183(4):2267-2276. https://pubmed.ncbi.nlm.nih.gov/19625655/
Yue X, Lio CWJ, Samaniego-Castruita D, Li X, Rao A. Loss of TET2 and TET3 in regulatory T cells unleashes effector function. Nat Commun. 2019;10(1):2011. https://pubmed.ncbi.nlm.nih.gov/31043609/
Uslu U, June CH. CAR T-cell therapy meets clonal hematopoiesis. Blood Cancer Discov. 2022;3(5):382-384. https://pubmed.ncbi.nlm.nih.gov/35896010/
Fraietta JA, Nobles CL, Sammons MA, et al. Disruption of TET2 promotes the therapeutic efficacy of CD19-targeted T cells. Nature. 2018;558(7709):307-312. https://pubmed.ncbi.nlm.nih.gov/29849141/
Shah NN, Qin H, Yates B, et al. Clonal expansion of CAR T cells harboring lentivector integration in the CBL gene following anti-CD22 CAR T-cell therapy. Blood Adv. 2019;3(15):2317-2322. https://pubmed.ncbi.nlm.nih.gov/31387880/
Alkhateeb HB, Mohty R, Greipp P, et al. Therapy-related myeloid neoplasms following chimeric antigen receptor T-cell therapy for non-Hodgkin lymphoma. Blood Cancer J. 2022;12(7):1-5. https://www.nature.com/articles/s41408-022-00707-4
Eder LN, Martinovic D, Mazzeo P, et al. Fatal progression of mutated TP53-associated clonal hematopoiesis following anti-CD19 CAR-T cell Therapy. Curr Oncol. 2023;30(1):1146-1150. https://pubmed.ncbi.nlm.nih.gov/36661736/
Jacobson CA, Locke FL, Ma L, et al. Real-world evidence of Axicabtagene Ciloleucel for the treatment of large B cell lymphoma in the United States. Transplant Cell Ther. 2022;28(9):581.e1-581.e8. https://pubmed.ncbi.nlm.nih.gov/35609867/
Chong EA, Ruella M, Schuster SJ. Five-year outcomes for refractory B-cell lymphomas with CAR T-cell therapy. N Engl J Med. 2021;384(7):673-674. https://pubmed.ncbi.nlm.nih.gov/33596362/
Wang M, Munoz J, Goy A, et al. Three-year follow-up of KTE-X19 in patients with relapsed/refractory mantle cell lymphoma, including high-risk subgroups, in the ZUMA-2 study. J Clin Oncol. 2023;41(3). https://pubmed.ncbi.nlm.nih.gov/35658525/:555-567.
Hsieh EM, Myers RM, Yates B, et al. Low rate of subsequent malignant neoplasms after CD19 CAR T-cell therapy. Blood Adv. 2022;6(17):5222-5226. https://pubmed.ncbi.nlm.nih.gov/35834728/
Zhao A, Zhao M, Qian W, Liang A, Li P, Liu H. Secondary myeloid neoplasms after CD19 CAR T therapy in patients with refractory/relapsed B-cell lymphoma: case series and review of literature. Front Immunol. 2023;13:1063986. https://pubmed.ncbi.nlm.nih.gov/36713414/
Locke FL, Neelapu SS, Bartlett NL, et al. Phase 1 results of ZUMA-1: a multicenter study of KTE-C19 anti-CD19 CAR T cell Therapy in refractory aggressive lymphoma. Mol Ther. 2017;25(1):285-295.
Cornetta K, Duffy L, Turtle CJ, et al. Absence of replication-competent lentivirus in the clinic: analysis of infused T cell products. Mol Ther. 2018;26(1):280-288. https://pubmed.ncbi.nlm.nih.gov/28970045/
Cornetta K, Duffy L, Feldman SA, et al. Screening clinical cell products for replication competent retrovirus: the National Gene Vector Biorepository Experience. Mol Ther Methods Clin Dev. 2018;10:371-378. https://pubmed.ncbi.nlm.nih.gov/30211249/
Bhoj VG, Arhontoulis D, Wertheim G, et al. Persistence of long-lived plasma cells and humoral immunity in individuals responding to CD19-directed CAR T-cell therapy. Blood. 2016;128(3):360-370. https://pubmed.ncbi.nlm.nih.gov/27166358/
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;5(1):143-155. https://pubmed.ncbi.nlm.nih.gov/33570626/
Wang Y, Li H, Song X, et al. Kinetics of immune reconstitution after anti-CD19 chimeric antigen receptor T cell therapy in relapsed or refractory acute lymphoblastic leukemia patients. Int J Lab Hematol. 2021;43(2):250-258. https://pubmed.ncbi.nlm.nih.gov/33112046/
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;106(4):978-986. https://pubmed.ncbi.nlm.nih.gov/32327504/
Deyà-Martínez A, Alonso-Saladrigues A, García AP, et al. Kinetics of humoral deficiency in CART19-treated children and young adults with acute lymphoblastic leukaemia. Bone Marrow Transplant. 2021;56(2):376-386. https://pubmed.ncbi.nlm.nih.gov/32801317/
Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507-1517. https://pubmed.ncbi.nlm.nih.gov/25317870/
Hayden PJ, Roddie C, Bader P, et al. Management of adults and children receiving CAR T-cell therapy: 2021 best practice recommendations of the European Society for Blood and Marrow Transplantation (EBMT) and the Joint Accreditation Committee of ISCT and EBMT (JACIE) and the European Haematology Association (EHA). Ann Oncol. 2022;33(3):259-275. http://www.annalsofoncology.org/article/S0923753421048766/fulltext
Foukaneli T, Kerr P, Bolton-Maggs PHB, et al. Guidelines on the use of irradiated blood components. Br J Haematol. 2020;191(5):704-724. http://www.gradeworkinggroup.org
Nagle SJ, Murphree C, Raess PW, et al. Prolonged hematologic toxicity following treatment with chimeric antigen receptor T cells in patients with hematologic malignancies. Am J Hematol. 2021;96(4):455-461. https://pubmed.ncbi.nlm.nih.gov/33529419/
Giammarco S, Sica S, Chiusolo P, et al. Eltrombopag for the treatment of poor graft function following allogeneic stem cell transplant: a retrospective multicenter study. Int J Hematol. 2021;114(2):228-234. https://pubmed.ncbi.nlm.nih.gov/33886103/
Peffault de Latour R, Kulasekararaj A, Iacobelli S, et al. Eltrombopag added to immunosuppression in severe aplastic anemia. N Engl J Med. 2022;386(1):11-23. https://pubmed.ncbi.nlm.nih.gov/34986284/
Rejeski K, Greco R, Onida F, et al. An international survey on grading, diagnosis, and management of immune effector cell-associated hematotoxicity (ICAHT) following CAR T-cell therapy on behalf of the EBMT and EHA. Hemasphere. 2023;7(5):e889. https://pubmed.ncbi.nlm.nih.gov/37125259/
Baur R, Jitschin R, Kharboutli S, et al. Thrombopoietin receptor agonists for acquired thrombocytopenia following anti-CD19 CAR-T-cell therapy: a case report. J Immunother Cancer. 2021;9(7):e002721. https://pubmed.ncbi.nlm.nih.gov/34272307/
Beyar-Katz O, Perry C, On YB, et al. Thrombopoietin receptor agonist for treating bone marrow aplasia following anti-CD19 CAR-T cells-single-center experience. Ann Hematol. 2022;101(8):1769-1776. https://pubmed.ncbi.nlm.nih.gov/35731278/
Gaut D, Tang K, Sim MS, Duong T, Young P, Sasine J. Filgrastim associations with CAR T-cell therapy. Int J Cancer. 2021;148(5):1192-1196. https://pubmed.ncbi.nlm.nih.gov/33091961/
Sterner RM, Sakemura R, Cox MJ, et al. GM-CSF inhibition reduces cytokine release syndrome and neuroinflammation but enhances CAR-T cell function in xenografts. Blood. 2019;133(7):697-709. https://pubmed.ncbi.nlm.nih.gov/30463995/
Miller KC, Johnson PC, Abramson JS, et al. Effect of granulocyte colony-stimulating factor on toxicities after CAR T cell therapy for lymphoma and myeloma. Blood Cancer J. 2022;12(10):146. https://pubmed.ncbi.nlm.nih.gov/36316312/
Galli E, Allain V, Di Blasi R, et al. G-CSF does not worsen toxicities and efficacy of CAR-T cells in refractory/relapsed B-cell lymphoma. Bone Marrow Transplant. 2020;55(12):2347-2349. https://pubmed.ncbi.nlm.nih.gov/32719501/
Barreto JN, Bansal R, Hathcock MA, et al. The impact of granulocyte colony stimulating factor on patients receiving chimeric antigen receptor T-cell therapy. Am J Hematol. 2021;96(10):E399-E402. https://pubmed.ncbi.nlm.nih.gov/34350612/
Bindal P, Elavalakanar P, Trottier CA, et al. G-CSF administration is associated with worse treatment response and survival after CAR T-cell therapy. Blood. 2022;140(Suppl 1):5238-5240. https://ashpublications.org/blood/article/140/Supplement%201/5238/492500/G-CSF-Administration-Is-Associated-with-Worse
Waight JD, Hu Q, Miller A, Liu S, Abrams SI. Tumor-derived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism. PLoS One. 2011;6(11):27690 PMC3218014.
Gödel P, Sieg N, Heger JM, et al. Hematologic rescue of CAR T-cell-mediated prolonged pancytopenia using autologous peripheral blood hematopoietic stem cells in a lymphoma patient. Hemasphere. 2021;5(3):E545. https://pubmed.ncbi.nlm.nih.gov/33623885/
Gagelmann N, Wulf GG, Duell J, et al. Hematopoietic stem cell boost for persistent neutropenia after CAR T-cell therapy: a GLA/DRST study. Blood Adv. 2023;7(4):555-559. https://pubmed.ncbi.nlm.nih.gov/35696759/
Lipsitt A, Beattie L, Harstead E, et al. Allogeneic CD34+ selected hematopoietic stem cell boost following CAR T-cell therapy in a patient with prolonged cytopenia and active infection. Pediatr Blood Cancer. 2023;70(3):e30166. https://pubmed.ncbi.nlm.nih.gov/36565276/
Xue F, Zheng P, Liu R, et al. The autologous hematopoietic stem cells transplantation combination-based chimeric antigen receptor T-cell Therapy improves outcomes of relapsed/refractory central nervous system B-cell lymphoma. J Oncol. 2022;2022:2900310. https://pubmed.ncbi.nlm.nih.gov/36483984/
Yang F, Shi H, Xu T, et al. Allogeneic stem cell transplantation combined with conditioning regimen including donor-derived CAR-T cells for refractory/relapsed B-cell lymphoma. Bone Marrow Transplant. 2023;58(4). https://pubmed.ncbi.nlm.nih.gov/36550201/:440-442.
Santomasso BD, Nastoupil LJ, Adkins S, et al. Management of immune-related adverse events in patients treated with chimeric antigen receptor T-cell therapy: ASCO guideline. J Clin Oncol. 2021;39(35):3978-3992. https://pubmed.ncbi.nlm.nih.gov/34724386/
Wat J, Barmettler S. Hypogammaglobulinemia after chimeric antigen receptor (CAR) T-cell therapy: characteristics, management, and future directions. J Allergy Clin Immunol Pract. 2022;10(2):460-466. https://pubmed.ncbi.nlm.nih.gov/34757064/
Gea-Banacloche JC. Infectious complications of chimeric antigen receptor (CAR) T-cell therapies. Semin Hematol. 2023;60(1). https://pubmed.ncbi.nlm.nih.gov/37080711/:52-58.
Spanjaart AM, Ljungman P, de La Camara R, et al. Poor outcome of patients with COVID-19 after CAR T-cell therapy for B-cell malignancies: results of a multicenter study on behalf of the European Society for Blood and Marrow Transplantation (EBMT) infectious diseases working party and the European Hematology Association (EHA) lymphoma group. Leukemia. 2021;35(12):3585-3588.