Evidence map›Paper›PMID 38865660›Full record

ArticleThe New England journal of medicine2024

Risk of Second Tumors and T-Cell Lymphoma after CAR T-Cell Therapy.

Mark P Hamilton, Takeshi Sugio, Troy Noordenbos, Shuyu Shi, Philip L Bulterys, Chih Long Liu, Xiaoman Kang, Mari N Olsen, Zinaida Good, Saurabh Dahiya and 7 more

Abstract readCase Reports
In one paragraph

Article in The New England journal of medicine, 2024. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 130 papers, 3 of them syntheses that pooled it.

0numbers the graph read from it
0cells of the map it votes in
130citing papers in PubMed, 3 pooled it
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

130 citing papers in PubMed, 3 syntheses or guidelines pooled it.

  1. Pooled it
  2. Pooled it
  3. Second Primary Malignancies after CAR T-Cell Therapy: A Systematic Review and Meta-analysis of 5,517 Lymphoma and Myeloma Patients.Clinical cancer research : an official journal of the American Association for Cancer Research · 2024
    Pooled it
  4. Review
  5. Article
  6. Article
  7. Article
  8. Review
  9. Review
  10. Article
  11. Article
  12. Review
  13. Balancing Efficacy and Safety in Multiple Myeloma Patients Receiving B cell Maturation Antigen-Directed CAR T-Cell Therapy.BioDrugs : clinical immunotherapeutics, biopharmaceuticals and gene therapy · 2026
    Review
  14. Review
  15. Article
  16. Emerging strategies to reduce the side effects of CAR-T cell therapy: focusing on gene editing and nanotechnology.Clinical & translational oncology : official publication of the Federation of Spanish Oncology Societies and of the National Cancer Institute of Mexico · 2026
    Review
  17. Clinical translation of epigenome editing technologies.Current opinion in biomedical engineering · 2026
    Article
  18. Review
  19. Review
  20. Article

70 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

17 authors.

Mark P HamiltonFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Takeshi SugioFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).ORCID 0000-0002-4270-1943
Troy NoordenbosFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Shuyu ShiFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Philip L BulterysFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Chih Long LiuFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Xiaoman KangFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Mari N OlsenFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Zinaida GoodFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Saurabh DahiyaFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Matthew J FrankFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Bita SahafFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Crystal L MackallFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).ORCID 0000-0003-0359-9023
Dita GratzingerFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Maximilian DiehnFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).
Ash A AlizadehFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).ORCID 0000-0002-5153-5625
David B MiklosFrom the Divisions of Oncology (M.P.H., T.S., T.N., C.L.L., X.K., M.N.O., A.A.A.) and Blood and Marrow Transplantation and Cellular Therapy (M.P.H., S.D., M.J.F., D.B.M.), Department of Medicine, the Center for Cancer Cell Therapy (M.P.H., Z.G., S.D., M.J.F., B.S., C.L.M., D.B.M.), Stanford Cancer Institute (T.S., T.N., C.L.L., X.K., M.N.O., C.L.M., M.D., A.A.A., D.B.M.), the Department of Pathology (P.L.B., D.G.), the Department of Biomedical Data Science (Z.G.), the Division of Hematology and Oncology, Department of Pediatrics (C.L.M.), the Department of Radiation Oncology (M.D.), and the Institute for Stem Cell Biology and Regenerative Medicine (M.D., A.A.A.), School of Medicine, and the Department of Bioengineering, Schools of Medicine and Engineering (S.S.), Stanford University, Stanford, CA; and the Department of Pathology, Leiden University Medical Center, Leiden, the Netherlands (T.N.).

Funding

TUMOR SPECIFIC CYTOTOXIC T-LYMPHOCYTES IN BONE MARROW TRANSPLANTATIONP01CA049605 · NCI · STANFORD UNIVERSITY · PI David B. Miklos, Robert S Negrin · 1989 to 2026
$73.3M
Circulating Genomic Determinants of Treatment Failure in Hodgkin LymphomaR01CA257655 · NCI · STANFORD UNIVERSITY · PI ALIZADEH, ASH ARASH, DIEHN, MAXIMILIAN · 2021 to 2025
$3.2M
A Noninvasive Integrated Genomic Approach for Early Cancer Detection and Risk Stratification after TransplantationR01CA229766 · NCI · STANFORD UNIVERSITY · PI ALIZADEH, ASH ARASH, KHUSH, KIRAN KAUR · 2019 to 2023
$3.0M
Next Generation Immunotherapies for Pediatric CancersR35CA283888 · NCI · STANFORD UNIVERSITY · PI Crystal Mackall · 2024 to 2026
$2.8M
A Genomic Framework for Molecular Risk Prediction & Individualized Lymphoma TherapyR01CA233975 · NCI · STANFORD UNIVERSITY · PI ALIZADEH, ASH ARASH, DIEHN, MAXIMILIAN · 2019 to 2023
$2.8M
NCI NIH HHS P01 CA049605NCI NIH HHS R01 CA229766NCI NIH HHS R01 CA233975NCI NIH HHS R01 CA257655NCI NIH HHS R35 CA283888NIH HHS CA233975
6 · The paper itself

Abstract

backgroundThe risk of second tumors after chimeric antigen receptor (CAR) T-cell therapy, especially the risk of T-cell neoplasms related to viral vector integration, is an emerging concern.

methodsWe reviewed our clinical experience with adoptive cellular CAR T-cell therapy at our institution since 2016 and ascertained the occurrence of second tumors. In one case of secondary T-cell lymphoma, a broad array of molecular, genetic, and cellular techniques were used to interrogate the tumor, the CAR T cells, and the normal hematopoietic cells in the patient.

resultsA total of 724 patients who had received T-cell therapies at our center were included in the study. A lethal T-cell lymphoma was identified in a patient who had received axicabtagene ciloleucel therapy for diffuse large B-cell lymphoma, and both lymphomas were deeply profiled. Each lymphoma had molecularly distinct immunophenotypes and genomic profiles, but both were positive for Epstein-Barr virus and were associated with

conclusionsOur results highlight the rarity of second tumors and provide a framework for defining clonal relationships and viral vector monitoring. (Funded by the National Cancer Institute and others.).

Indexed as

Antineoplastic Agents, ImmunologicalImmunotherapy, AdoptiveLymphoma, Large B-Cell, DiffuseLymphoma, T-CellNeoplasms, Second PrimaryReceptors, Chimeric AntigenBiological ProductsClonal HematopoiesisFemaleHerpesvirus 4, HumanHumansMiddle AgedVirus IntegrationAntineoplastic Agents, Immunologicalaxicabtagene ciloleucelBiological ProductsReceptors, Chimeric Antigen

Identifiers

PMID38865660
PMCPMC11338600

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.