Immune Effector Cell-Associated Hemophagocytic Lymphohistiocytosis-Like Syndrome
•Hemophagocytic lymphohistiocytosis (HLH)-like toxicities occur after CAR T-cells•This is now termed immune effector cell (IEC) associated HLH-like syndrome (IEC-HS)•Independent of cytokine release syndrome (CRS) and neurotoxicity, IEC-HS can be fatal•Consensus for identification and grading of IEC-...
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| Published in | Transplantation and cellular therapy Vol. 29; no. 7; pp. 438.e1 - 438.e16 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.07.2023
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| Subjects | |
| Online Access | Get full text |
| ISSN | 2666-6367 2666-6375 2666-6367 |
| DOI | 10.1016/j.jtct.2023.03.006 |
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| Abstract | •Hemophagocytic lymphohistiocytosis (HLH)-like toxicities occur after CAR T-cells•This is now termed immune effector cell (IEC) associated HLH-like syndrome (IEC-HS)•Independent of cytokine release syndrome (CRS) and neurotoxicity, IEC-HS can be fatal•Consensus for identification and grading of IEC-HS has been developed by experts•Treatment, supportive care, and future research are imperative to improving outcomes of IEC-HS
T cell-mediated hyperinflammatory responses, such as cytokine release syndrome (CRS) and immune effector cell-associated neurotoxicity syndrome (ICANS), are now well-established toxicities of chimeric antigen receptor (CAR) T cell therapy. As the field of CAR T cells advances, however, there is increasing recognition that hemophagocytic lymphohistiocytosis (HLH)-like toxicities following CAR T cell infusion are occurring broadly across patient populations and CAR T cell constructs. Importantly, these HLH-like toxicities are often not as directly associated with CRS and/or its severity as initially described. This emergent toxicity, however ill-defined, is associated with life-threatening complications, creating an urgent need for improved identification and optimal management. With the goal of improving patient outcomes and formulating a framework to characterize and study this HLH-like syndrome, we established an American Society for Transplantation and Cellular Therapy panel composed of experts in primary and secondary HLH, pediatric and adult HLH, infectious disease, rheumatology and hematology, oncology, and cellular therapy. Through this effort, we provide an overview of the underlying biology of classical primary and secondary HLH, explore its relationship with similar manifestations following CAR T cell infusions, and propose the term “immune effector cell-associated HLH-like syndrome (IEC-HS)” to describe this emergent toxicity. We also delineate a framework for identifying IEC-HS and put forward a grading schema that can be used to assess severity and facilitate cross-trial comparisons. Additionally, given the critical need to optimize outcomes for patients experiencing IEC-HS, we provide insight into potential treatment approaches and strategies to optimize supportive care and delineate alternate etiologies that should be considered in a patient presenting with IEC-HS. By collectively defining IEC-HS as a hyperinflammatory toxicity, we can now embark on further study of the pathophysiology underlying this toxicity profile and make strides toward a more comprehensive assessment and treatment approach. |
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| AbstractList | T cell-mediated hyperinflammatory responses, such as cytokine release syndrome (CRS) and immune effector cell-associated neurotoxicity syndrome (ICANS), are now well-established toxicities of chimeric antigen receptor (CAR) T cell therapy. As the field of CAR T cells advances, however, there is increasing recognition that hemophagocytic lymphohistiocytosis (HLH)-like toxicities following CAR T cell infusion are occurring broadly across patient populations and CAR T cell constructs. Importantly, these HLH-like toxicities are often not as directly associated with CRS and/or its severity as initially described. This emergent toxicity, however ill-defined, is associated with life-threatening complications, creating an urgent need for improved identification and optimal management. With the goal of improving patient outcomes and formulating a framework to characterize and study this HLH-like syndrome, we established an American Society for Transplantation and Cellular Therapy panel composed of experts in primary and secondary HLH, pediatric and adult HLH, infectious disease, rheumatology and hematology, oncology, and cellular therapy. Through this effort, we provide an overview of the underlying biology of classical primary and secondary HLH, explore its relationship with similar manifestations following CAR T cell infusions, and propose the term "immune effector cell-associated HLH-like syndrome (IEC-HS)" to describe this emergent toxicity. We also delineate a framework for identifying IEC-HS and put forward a grading schema that can be used to assess severity and facilitate cross-trial comparisons. Additionally, given the critical need to optimize outcomes for patients experiencing IEC-HS, we provide insight into potential treatment approaches and strategies to optimize supportive care and delineate alternate etiologies that should be considered in a patient presenting with IEC-HS. By collectively defining IEC-HS as a hyperinflammatory toxicity, we can now embark on further study of the pathophysiology underlying this toxicity profile and make strides toward a more comprehensive assessment and treatment approach. •Hemophagocytic lymphohistiocytosis (HLH)-like toxicities occur after CAR T-cells•This is now termed immune effector cell (IEC) associated HLH-like syndrome (IEC-HS)•Independent of cytokine release syndrome (CRS) and neurotoxicity, IEC-HS can be fatal•Consensus for identification and grading of IEC-HS has been developed by experts•Treatment, supportive care, and future research are imperative to improving outcomes of IEC-HS T cell-mediated hyperinflammatory responses, such as cytokine release syndrome (CRS) and immune effector cell-associated neurotoxicity syndrome (ICANS), are now well-established toxicities of chimeric antigen receptor (CAR) T cell therapy. As the field of CAR T cells advances, however, there is increasing recognition that hemophagocytic lymphohistiocytosis (HLH)-like toxicities following CAR T cell infusion are occurring broadly across patient populations and CAR T cell constructs. Importantly, these HLH-like toxicities are often not as directly associated with CRS and/or its severity as initially described. This emergent toxicity, however ill-defined, is associated with life-threatening complications, creating an urgent need for improved identification and optimal management. With the goal of improving patient outcomes and formulating a framework to characterize and study this HLH-like syndrome, we established an American Society for Transplantation and Cellular Therapy panel composed of experts in primary and secondary HLH, pediatric and adult HLH, infectious disease, rheumatology and hematology, oncology, and cellular therapy. Through this effort, we provide an overview of the underlying biology of classical primary and secondary HLH, explore its relationship with similar manifestations following CAR T cell infusions, and propose the term “immune effector cell-associated HLH-like syndrome (IEC-HS)” to describe this emergent toxicity. We also delineate a framework for identifying IEC-HS and put forward a grading schema that can be used to assess severity and facilitate cross-trial comparisons. Additionally, given the critical need to optimize outcomes for patients experiencing IEC-HS, we provide insight into potential treatment approaches and strategies to optimize supportive care and delineate alternate etiologies that should be considered in a patient presenting with IEC-HS. By collectively defining IEC-HS as a hyperinflammatory toxicity, we can now embark on further study of the pathophysiology underlying this toxicity profile and make strides toward a more comprehensive assessment and treatment approach. T cell-mediated hyperinflammatory responses, such as cytokine release syndrome (CRS) and immune effector cell-associated neurotoxicity syndrome (ICANS), are now well-established toxicities of chimeric antigen receptor (CAR) T cell therapy. As the field of CAR T cells advances, however, there is increasing recognition that hemophagocytic lymphohistiocytosis (HLH)-like toxicities following CAR T cell infusion are occurring broadly across patient populations and CAR T cell constructs. Importantly, these HLH-like toxicities are often not as directly associated with CRS and/or its severity as initially described. This emergent toxicity, however ill-defined, is associated with life-threatening complications, creating an urgent need for improved identification and optimal management. With the goal of improving patient outcomes and formulating a framework to characterize and study this HLH-like syndrome, we established an American Society for Transplantation and Cellular Therapy panel composed of experts in primary and secondary HLH, pediatric and adult HLH, infectious disease, rheumatology and hematology, oncology, and cellular therapy. Through this effort, we provide an overview of the underlying biology of classical primary and secondary HLH, explore its relationship with similar manifestations following CAR T cell infusions, and propose the term "immune effector cell-associated HLH-like syndrome (IEC-HS)" to describe this emergent toxicity. We also delineate a framework for identifying IEC-HS and put forward a grading schema that can be used to assess severity and facilitate cross-trial comparisons. Additionally, given the critical need to optimize outcomes for patients experiencing IEC-HS, we provide insight into potential treatment approaches and strategies to optimize supportive care and delineate alternate etiologies that should be considered in a patient presenting with IEC-HS. By collectively defining IEC-HS as a hyperinflammatory toxicity, we can now embark on further study of the pathophysiology underlying this toxicity profile and make strides toward a more comprehensive assessment and treatment approach.T cell-mediated hyperinflammatory responses, such as cytokine release syndrome (CRS) and immune effector cell-associated neurotoxicity syndrome (ICANS), are now well-established toxicities of chimeric antigen receptor (CAR) T cell therapy. As the field of CAR T cells advances, however, there is increasing recognition that hemophagocytic lymphohistiocytosis (HLH)-like toxicities following CAR T cell infusion are occurring broadly across patient populations and CAR T cell constructs. Importantly, these HLH-like toxicities are often not as directly associated with CRS and/or its severity as initially described. This emergent toxicity, however ill-defined, is associated with life-threatening complications, creating an urgent need for improved identification and optimal management. With the goal of improving patient outcomes and formulating a framework to characterize and study this HLH-like syndrome, we established an American Society for Transplantation and Cellular Therapy panel composed of experts in primary and secondary HLH, pediatric and adult HLH, infectious disease, rheumatology and hematology, oncology, and cellular therapy. Through this effort, we provide an overview of the underlying biology of classical primary and secondary HLH, explore its relationship with similar manifestations following CAR T cell infusions, and propose the term "immune effector cell-associated HLH-like syndrome (IEC-HS)" to describe this emergent toxicity. We also delineate a framework for identifying IEC-HS and put forward a grading schema that can be used to assess severity and facilitate cross-trial comparisons. Additionally, given the critical need to optimize outcomes for patients experiencing IEC-HS, we provide insight into potential treatment approaches and strategies to optimize supportive care and delineate alternate etiologies that should be considered in a patient presenting with IEC-HS. By collectively defining IEC-HS as a hyperinflammatory toxicity, we can now embark on further study of the pathophysiology underlying this toxicity profile and make strides toward a more comprehensive assessment and treatment approach. |
| Author | Hines, Melissa R. Marsh, Rebecca A. Perales, Miguel-Angel Teachey, David T. Johnson, William T. Maron, Gabriela M. Berliner, Nancy Shah, Nirav N. Jain, Tania Nikiforow, Sarah Knight, Tristan E. Neelapu, Sattva S. Vatsayan, Anant Leick, Mark B. Frank, Matthew J. Frigault, Matthew J. Mahadeo, Kris M. Turicek, David Wong, Sandy W. Komanduri, Krishna V. Frey, Noelle V. Shah, Nirali N. McNerney, Kevin O. Talleur, Aimee C. Jain, Michael D. Maus, Marcela V. Ombrello, Amanda K. Lin, Yi Ahmed, Sairah Hill, Joshua A. Henter, Jan-Inge |
| AuthorAffiliation | 15 Inflammatory Disease Section, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 19 Division of Blood and Marrow Transplantation, Children’s National Health System, Washington, DC 22 Division of Pediatric Oncology and Surgery, Department of Women’s and Children’s Health, Karolinska Institute, and Department of Paediatric Oncology, Astrid Lindgren Children’s Hospital, Karolinska University Hospital, Stockholm, Sweden 3 Cancer and Blood Disorders Institute, Johns Hopkins All Children’s Hospital, St. Petersburg, FL 16 Bone Marrow Transplant and Cellular Therapy Program, Division of Hematology and Oncology, Medical College of Wisconsin, Milwaukee, WI 26 Division of Blood and Marrow Transplantation and Cellular Therapy, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA 5 Division of Hematological Malignancies and Bone Marrow Transplantation, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD 11 Pedi |
| AuthorAffiliation_xml | – name: 5 Division of Hematological Malignancies and Bone Marrow Transplantation, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD – name: 25 Division of Oncology, The Children’s Hospital of Philadelphia, Philadelphia, PA – name: 12 Department of Infectious Diseases, St. Jude Children’s Research Hospital, Memphis, TN, and Department of Pediatrics, University of Tennessee Health Science Center College of Medicine – name: 22 Division of Pediatric Oncology and Surgery, Department of Women’s and Children’s Health, Karolinska Institute, and Department of Paediatric Oncology, Astrid Lindgren Children’s Hospital, Karolinska University Hospital, Stockholm, Sweden – name: 2 Pediatric Hematology and Oncology, Seattle Children’s Hospital and the University of Washington School of Medicine, Seattle, WA – name: 13 University of Cincinnati, and Division of Bone Marrow Transplantation and Immune Deficiency, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH – name: 24 Division of Hematology-Oncology, Abramson Cancer Center and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA – name: 20 UCSF Health Division of Hematology and Oncology and Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA – name: 18 Pediatric Oncology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD – name: 19 Division of Blood and Marrow Transplantation, Children’s National Health System, Washington, DC – name: 4 Cellular Immunotherapy Program and Blood and Marrow Transplant Program, Cancer Center, Massachusetts General Hospital, Boston, MA – name: 21 Brigham and Women’s Hospital, Boston, MA – name: 16 Bone Marrow Transplant and Cellular Therapy Program, Division of Hematology and Oncology, Medical College of Wisconsin, Milwaukee, WI – name: 26 Division of Blood and Marrow Transplantation and Cellular Therapy, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, CA – name: 1 Department of Pediatric Medicine, Division of Critical Care, St Jude Children’s Research Hospital, Memphis, TN – name: 9 Department of Medicine, Cellular Therapy Service, Memorial Sloan Kettering Cancer Center, New York, NY – name: 8 Department of Medicine, Sylvester Comprehensive Cancer Center, University of Miami, Miami, FL – name: 6 Departments of Lymphoma and Myeloma and Stem Cell Transplantation, The University of Texas MD Anderson Cancer Center, Houston, TX – name: 15 Inflammatory Disease Section, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD – name: 14 Division of Hematologic Oncology, Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA – name: 3 Cancer and Blood Disorders Institute, Johns Hopkins All Children’s Hospital, St. Petersburg, FL – name: 7 Vaccine and Infectious Diseases Division, Fred Hutchinson Cancer Center, Seattle, WA – name: 10 Division Hematology-Oncology and Blood and Marrow Transplantation Program, Mayo Clinic, Rochester, MN – name: 17 Department of Bone Marrow Transplantation and Cellular Therapy, St. Jude Children’s Research Hospital, Memphis, TN and Department of Pediatrics, University of Tennessee Health Science Center College of Medicine – name: 11 Pediatric Transplantation and Cellular Therapy, Duke University, Durham, NC – name: 23 Department of Medicine, Adult Bone Marrow Transplant Service, Memorial Sloan Kettering Cancer Center, New York, NY |
| Author_xml | – sequence: 1 givenname: Melissa R. surname: Hines fullname: Hines, Melissa R. organization: Department of Pediatric Medicine, Division of Critical Care, St. Jude Children's Research Hospital, Memphis, Tennessee – sequence: 2 givenname: Tristan E. orcidid: 0000-0002-7828-1522 surname: Knight fullname: Knight, Tristan E. organization: Pediatric Hematology and Oncology, Seattle Children's Hospital and the University of Washington School of Medicine, Seattle, Washington – sequence: 3 givenname: Kevin O. orcidid: 0000-0002-4359-3569 surname: McNerney fullname: McNerney, Kevin O. organization: Cancer and Blood Disorders Institute, Johns Hopkins All Children's Hospital, St. Petersburg, Florida – sequence: 4 givenname: Mark B. orcidid: 0000-0003-3111-0221 surname: Leick fullname: Leick, Mark B. organization: Cellular Immunotherapy Program and Blood and Marrow Transplant Program, Cancer Center, Massachusetts General Hospital, Boston, Massachusetts – sequence: 5 givenname: Tania orcidid: 0000-0001-6854-773X surname: Jain fullname: Jain, Tania organization: Division of Hematological Malignancies and Bone Marrow Transplantation, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, Maryland – sequence: 6 givenname: Sairah surname: Ahmed fullname: Ahmed, Sairah organization: Departments of Lymphoma and Myeloma and Stem Cell Transplantation, The University of Texas MD Anderson Cancer Center, Houston, Texas – sequence: 7 givenname: Matthew J. orcidid: 0000-0002-6774-5694 surname: Frigault fullname: Frigault, Matthew J. organization: Cellular Immunotherapy Program and Blood and Marrow Transplant Program, Cancer Center, Massachusetts General Hospital, Boston, Massachusetts – sequence: 8 givenname: Joshua A. orcidid: 0000-0002-7665-7100 surname: Hill fullname: Hill, Joshua A. organization: Vaccine and Infectious Diseases Division, Fred Hutchinson Cancer Center, Seattle, Washington – sequence: 9 givenname: Michael D. orcidid: 0000-0002-7789-1257 surname: Jain fullname: Jain, Michael D. organization: Moffitt Cancer Center, Tampa, Florida – sequence: 10 givenname: William T. surname: Johnson fullname: Johnson, William T. organization: Department of Medicine, Cellular Therapy Service, Memorial Sloan Kettering Cancer Center, New York, New York – sequence: 11 givenname: Yi orcidid: 0000-0002-1556-6416 surname: Lin fullname: Lin, Yi organization: Division Hematology-Oncology and Blood and Marrow Transplantation Program, Mayo Clinic, Rochester, Minnesota – sequence: 12 givenname: Kris M. surname: Mahadeo fullname: Mahadeo, Kris M. organization: Pediatric Transplantation and Cellular Therapy, Duke University, Durham, North Carolina – sequence: 13 givenname: Gabriela M. orcidid: 0000-0001-5247-5399 surname: Maron fullname: Maron, Gabriela M. organization: Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, and Department of Pediatrics, University of Tennessee Health Science Center College of Medicine, Memphis, Tennessee – sequence: 14 givenname: Rebecca A. surname: Marsh fullname: Marsh, Rebecca A. organization: University of Cincinnati, and Division of Bone Marrow Transplantation and Immune Deficiency, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio – sequence: 15 givenname: Sattva S. surname: Neelapu fullname: Neelapu, Sattva S. organization: Departments of Lymphoma and Myeloma and Stem Cell Transplantation, The University of Texas MD Anderson Cancer Center, Houston, Texas – sequence: 16 givenname: Sarah surname: Nikiforow fullname: Nikiforow, Sarah organization: Division of Hematologic Oncology, Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts – sequence: 17 givenname: Amanda K. surname: Ombrello fullname: Ombrello, Amanda K. organization: Inflammatory Disease Section, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland – sequence: 18 givenname: Nirav N. orcidid: 0000-0002-4336-1071 surname: Shah fullname: Shah, Nirav N. organization: Bone Marrow Transplant and Cellular Therapy Program, Division of Hematology and Oncology, Medical College of Wisconsin, Milwaukee, Wisconsin – sequence: 19 givenname: Aimee C. orcidid: 0000-0002-6558-6706 surname: Talleur fullname: Talleur, Aimee C. organization: Department of Bone Marrow Transplantation and Cellular Therapy, St. Jude Children's Research Hospital, Memphis, Tennessee and Department of Pediatrics, University of Tennessee Health Science Center College of Medicine, Memphis, Tennessee – sequence: 20 givenname: David orcidid: 0000-0003-0837-2688 surname: Turicek fullname: Turicek, David organization: Pediatric Oncology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland – sequence: 21 givenname: Anant orcidid: 0000-0003-2993-0490 surname: Vatsayan fullname: Vatsayan, Anant organization: Division of Blood and Marrow 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givenname: Jan-Inge orcidid: 0000-0002-0629-2126 surname: Henter fullname: Henter, Jan-Inge organization: Division of Pediatric Oncology and Surgery, Department of Women's and Children's Health, Karolinska Institute, and Department of Paediatric Oncology, Astrid Lindgren Children's Hospital, Karolinska University Hospital, Stockholm, Sweden – sequence: 27 givenname: Miguel-Angel orcidid: 0000-0002-5910-4571 surname: Perales fullname: Perales, Miguel-Angel organization: Department of Medicine, Adult Bone Marrow Transplant Service, Memorial Sloan Kettering Cancer Center, New York, New York – sequence: 28 givenname: Noelle V. orcidid: 0000-0003-3688-9836 surname: Frey fullname: Frey, Noelle V. organization: Division of Hematology-Oncology, Abramson Cancer Center and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania – sequence: 29 givenname: David T. orcidid: 0000-0001-7373-8987 surname: Teachey fullname: Teachey, David T. organization: Division of Oncology, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania – sequence: 30 givenname: Matthew J. surname: Frank fullname: Frank, Matthew J. organization: Division of Blood and Marrow Transplantation and Cellular Therapy, Stanford Cancer Institute, Stanford University School of Medicine, Stanford, California – sequence: 31 givenname: Nirali N. orcidid: 0000-0002-8474-9080 surname: Shah fullname: Shah, Nirali N. email: Nirali.Shah@nih.gov organization: Pediatric Oncology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36906275$$D View this record in MEDLINE/PubMed |
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| Snippet | •Hemophagocytic lymphohistiocytosis (HLH)-like toxicities occur after CAR T-cells•This is now termed immune effector cell (IEC) associated HLH-like syndrome... T cell-mediated hyperinflammatory responses, such as cytokine release syndrome (CRS) and immune effector cell-associated neurotoxicity syndrome (ICANS), are... |
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| SubjectTerms | Adult Child Chimeric antigen receptor T cell Cytokine Release Syndrome - complications Cytokine Release Syndrome - therapy Hemophagocytic lymphohistiocytosis Humans Immunotherapy, Adoptive - adverse effects Lymphohistiocytosis, Hemophagocytic - etiology Lymphohistiocytosis, Hemophagocytic - therapy Macrophage activation syndrome Neurotoxicity Syndromes - etiology T-Lymphocytes United States |
| Title | Immune Effector Cell-Associated Hemophagocytic Lymphohistiocytosis-Like Syndrome |
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