SARS-CoV-2 infections in pediatric and young adult recipients of chimeric antigen receptor T-cell therapy: an international registry report
BackgroundImmunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for relapsed/refractory B-cell malignancies are uniquely immunosuppressed due to CAR T-mediated B-cell aplasia (BCA). While SARS-CoV-2 mortality rat...
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| Published in | Journal for immunotherapy of cancer Vol. 11; no. 1; p. e005957 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
BMJ Publishing Group Ltd
01.01.2023
BMJ Publishing Group LTD BMJ Publishing Group |
| Series | Original research |
| Subjects | |
| Online Access | Get full text |
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| Abstract | BackgroundImmunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for relapsed/refractory B-cell malignancies are uniquely immunosuppressed due to CAR T-mediated B-cell aplasia (BCA). While SARS-CoV-2 mortality rates of 33%–40% are reported in adult CAR T-cell recipients, outcomes in pediatric and young adult CAR T-cell recipients are limited.MethodsWe created an international retrospective registry of CAR T recipients aged 0–30 years infected with SARS-CoV-2 within 2 months prior to or any time after CAR T infusion. SARS-CoV-2-associated illness was graded as asymptomatic, mild, moderate, or severe COVID-19, or multisystem inflammatory syndrome in children (MIS-C). To assess for risk factors associated with significant SARS-CoV-2 infections (infections requiring hospital admission for respiratory distress or supplemental oxygen), univariate and multivariable regression analyses were performed.ResultsNine centers contributed 78 infections in 75 patients. Of 70 SARS-CoV-2 infections occurring after CAR T infusion, 13 (18.6%) were classified as asymptomatic, 37 (52.9%) mild, 11 (15.7%) moderate, and 6 (8.6%) severe COVID-19. Three (4.3%) were classified as MIS-C. BCA was not significantly associated with infection severity. Prior to the emergence of the Omicron variant, of 47 infections, 19 (40.4%) resulted in hospital admission and 7 (14.9%) required intensive care, while after the emergence of the Omicron variant, of 23 infections, only 1 (4.3%) required admission and the remaining 22 (95.7%) had asymptomatic or mild COVID-19. Death occurred in 3 of 70 (4.3%); each death involved coinfection or life-threatening condition. In a multivariable model, factors associated with significant SARS-CoV-2 infection included having two or more comorbidities (OR 7.73, CI 1.05 to 74.8, p=0.048) and age ≥18 years (OR 9.51, CI 1.90 to 82.2, p=0.014). In the eight patients infected with SARS-CoV-2 before CAR T, half of these patients had their CAR T infusion delayed by 15–30 days.ConclusionsIn a large international cohort of pediatric and young adult CAR-T recipients, SARS-CoV-2 infections resulted in frequent hospital and intensive care unit admissions and were associated with mortality in 4.3%. Patients with two or more comorbidities or aged ≥18 years were more likely to experience significant illness. Suspected Omicron infections were associated with milder disease. |
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| AbstractList | BackgroundImmunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for relapsed/refractory B-cell malignancies are uniquely immunosuppressed due to CAR T-mediated B-cell aplasia (BCA). While SARS-CoV-2 mortality rates of 33%–40% are reported in adult CAR T-cell recipients, outcomes in pediatric and young adult CAR T-cell recipients are limited.MethodsWe created an international retrospective registry of CAR T recipients aged 0–30 years infected with SARS-CoV-2 within 2 months prior to or any time after CAR T infusion. SARS-CoV-2-associated illness was graded as asymptomatic, mild, moderate, or severe COVID-19, or multisystem inflammatory syndrome in children (MIS-C). To assess for risk factors associated with significant SARS-CoV-2 infections (infections requiring hospital admission for respiratory distress or supplemental oxygen), univariate and multivariable regression analyses were performed.ResultsNine centers contributed 78 infections in 75 patients. Of 70 SARS-CoV-2 infections occurring after CAR T infusion, 13 (18.6%) were classified as asymptomatic, 37 (52.9%) mild, 11 (15.7%) moderate, and 6 (8.6%) severe COVID-19. Three (4.3%) were classified as MIS-C. BCA was not significantly associated with infection severity. Prior to the emergence of the Omicron variant, of 47 infections, 19 (40.4%) resulted in hospital admission and 7 (14.9%) required intensive care, while after the emergence of the Omicron variant, of 23 infections, only 1 (4.3%) required admission and the remaining 22 (95.7%) had asymptomatic or mild COVID-19. Death occurred in 3 of 70 (4.3%); each death involved coinfection or life-threatening condition. In a multivariable model, factors associated with significant SARS-CoV-2 infection included having two or more comorbidities (OR 7.73, CI 1.05 to 74.8, p=0.048) and age ≥18 years (OR 9.51, CI 1.90 to 82.2, p=0.014). In the eight patients infected with SARS-CoV-2 before CAR T, half of these patients had their CAR T infusion delayed by 15–30 days.ConclusionsIn a large international cohort of pediatric and young adult CAR-T recipients, SARS-CoV-2 infections resulted in frequent hospital and intensive care unit admissions and were associated with mortality in 4.3%. Patients with two or more comorbidities or aged ≥18 years were more likely to experience significant illness. Suspected Omicron infections were associated with milder disease. Immunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for relapsed/refractory B-cell malignancies are uniquely immunosuppressed due to CAR T-mediated B-cell aplasia (BCA). While SARS-CoV-2 mortality rates of 33%-40% are reported in adult CAR T-cell recipients, outcomes in pediatric and young adult CAR T-cell recipients are limited. We created an international retrospective registry of CAR T recipients aged 0-30 years infected with SARS-CoV-2 within 2 months prior to or any time after CAR T infusion. SARS-CoV-2-associated illness was graded as asymptomatic, mild, moderate, or severe COVID-19, or multisystem inflammatory syndrome in children (MIS-C). To assess for risk factors associated with significant SARS-CoV-2 infections (infections requiring hospital admission for respiratory distress or supplemental oxygen), univariate and multivariable regression analyses were performed. Nine centers contributed 78 infections in 75 patients. Of 70 SARS-CoV-2 infections occurring after CAR T infusion, 13 (18.6%) were classified as asymptomatic, 37 (52.9%) mild, 11 (15.7%) moderate, and 6 (8.6%) severe COVID-19. Three (4.3%) were classified as MIS-C. BCA was not significantly associated with infection severity. Prior to the emergence of the Omicron variant, of 47 infections, 19 (40.4%) resulted in hospital admission and 7 (14.9%) required intensive care, while after the emergence of the Omicron variant, of 23 infections, only 1 (4.3%) required admission and the remaining 22 (95.7%) had asymptomatic or mild COVID-19. Death occurred in 3 of 70 (4.3%); each death involved coinfection or life-threatening condition. In a multivariable model, factors associated with significant SARS-CoV-2 infection included having two or more comorbidities (OR 7.73, CI 1.05 to 74.8, p=0.048) and age ≥18 years (OR 9.51, CI 1.90 to 82.2, p=0.014). In the eight patients infected with SARS-CoV-2 before CAR T, half of these patients had their CAR T infusion delayed by 15-30 days. In a large international cohort of pediatric and young adult CAR-T recipients, SARS-CoV-2 infections resulted in frequent hospital and intensive care unit admissions and were associated with mortality in 4.3%. Patients with two or more comorbidities or aged ≥18 years were more likely to experience significant illness. Suspected Omicron infections were associated with milder disease. Background Immunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for relapsed/refractory B-cell malignancies are uniquely immunosuppressed due to CAR T-mediated B-cell aplasia (BCA). While SARS-CoV-2 mortality rates of 33%–40% are reported in adult CAR T-cell recipients, outcomes in pediatric and young adult CAR T-cell recipients are limited.Methods We created an international retrospective registry of CAR T recipients aged 0–30 years infected with SARS-CoV-2 within 2 months prior to or any time after CAR T infusion. SARS-CoV-2-associated illness was graded as asymptomatic, mild, moderate, or severe COVID-19, or multisystem inflammatory syndrome in children (MIS-C). To assess for risk factors associated with significant SARS-CoV-2 infections (infections requiring hospital admission for respiratory distress or supplemental oxygen), univariate and multivariable regression analyses were performed.Results Nine centers contributed 78 infections in 75 patients. Of 70 SARS-CoV-2 infections occurring after CAR T infusion, 13 (18.6%) were classified as asymptomatic, 37 (52.9%) mild, 11 (15.7%) moderate, and 6 (8.6%) severe COVID-19. Three (4.3%) were classified as MIS-C. BCA was not significantly associated with infection severity. Prior to the emergence of the Omicron variant, of 47 infections, 19 (40.4%) resulted in hospital admission and 7 (14.9%) required intensive care, while after the emergence of the Omicron variant, of 23 infections, only 1 (4.3%) required admission and the remaining 22 (95.7%) had asymptomatic or mild COVID-19. Death occurred in 3 of 70 (4.3%); each death involved coinfection or life-threatening condition. In a multivariable model, factors associated with significant SARS-CoV-2 infection included having two or more comorbidities (OR 7.73, CI 1.05 to 74.8, p=0.048) and age ≥18 years (OR 9.51, CI 1.90 to 82.2, p=0.014). In the eight patients infected with SARS-CoV-2 before CAR T, half of these patients had their CAR T infusion delayed by 15–30 days.Conclusions In a large international cohort of pediatric and young adult CAR-T recipients, SARS-CoV-2 infections resulted in frequent hospital and intensive care unit admissions and were associated with mortality in 4.3%. Patients with two or more comorbidities or aged ≥18 years were more likely to experience significant illness. Suspected Omicron infections were associated with milder disease. |
| Author | Talano, Julie-An Li, Yimei Calkoen, Friso G Davis, Kara Lynn Callahan, Colleen McNerney, Kevin Owen Krajewski, Jennifer Richards, Rebecca M Moskop, Amy Liu, Hongyan Vatsayan, Anant Dave, Hema Aguayo-Hiraldo, Paibel Balduzzi, Adriana Maude, Shannon L |
| AuthorAffiliation | 3 Hematology, Oncology, and Bone Marrow Transplant , University of Wisconsin-Madison , Madison , Wisconsin , USA 12 Department of Biostatistics, Epidemiology and Informatics , University of Pennsylvania , Philadelphia , Pennsylvania , USA 7 Clinica Pediatrica Università degli Studi di Milano Bicocca , Fondazione IRCCS San Gerardo dai Tintori , Milan , Italy 13 Department of Pediatrics , University of Pennsylvania Perelman School of Medicine , Philadelphia , Pennsylvania , USA 11 Division of Oncology and Cancer Immunotherapy Program , The Children's Hospital of Philadelphia , Philadelphia , Pennsylvania , USA 14 Department of Pediatrics , University of Pennsylvania , Philadelphia , Pennsylvania , USA 10 Center for Cancer and Blood Disorders , Children's National Hospital , Washington , District of Columbia , USA 4 Cancer and Blood Disease Institute , Keck School of Medicine of USC , Los Angeles , California , USA 5 Division of Pediatric Oncology , Princess Maxima Center , Utrecht , The Netherla |
| AuthorAffiliation_xml | – name: 3 Hematology, Oncology, and Bone Marrow Transplant , University of Wisconsin-Madison , Madison , Wisconsin , USA – name: 6 Division of Hematology/Oncology/Blood and Marrow TransplantationDepartment of Pediatrics , Medical College of Wisconsin and Children’s Wisconsin , Milwaukee , Wisconsin , USA – name: 11 Division of Oncology and Cancer Immunotherapy Program , The Children's Hospital of Philadelphia , Philadelphia , Pennsylvania , USA – name: 4 Cancer and Blood Disease Institute , Keck School of Medicine of USC , Los Angeles , California , USA – name: 15 Pediatrics , Stanford University School of Medicine , Stanford , California , USA – name: 1 Cancer and Blood Disorders Institute , Johns Hopkins All Children's Hospital , St Petersburg , Florida , USA – name: 17 Division of Oncology, Center for Childhood Cancer Research and Cancer Immunotherapy Program , The Children's Hospital of Philadelphia , Philadelphia , Pennsylvania , USA – name: 14 Department of Pediatrics , University of Pennsylvania , Philadelphia , Pennsylvania , USA – name: 8 Pediatric Blood and Marrow Transplantation , Hackensack Meridian School of Medicine , Hackensack , New Jersey , USA – name: 13 Department of Pediatrics , University of Pennsylvania Perelman School of Medicine , Philadelphia , Pennsylvania , USA – name: 2 Oncology , Johns Hopkins University School of Medicine , Baltimore , Maryland , USA – name: 10 Center for Cancer and Blood Disorders , Children's National Hospital , Washington , District of Columbia , USA – name: 5 Division of Pediatric Oncology , Princess Maxima Center , Utrecht , The Netherlands – name: 9 Cancer Immunology and Microbial Oncology Research Program , Children's National Hospital , Washington , District of Columbia , USA – name: 7 Clinica Pediatrica Università degli Studi di Milano Bicocca , Fondazione IRCCS San Gerardo dai Tintori , Milan , Italy – name: 12 Department of Biostatistics, Epidemiology and Informatics , University of Pennsylvania , Philadelphia , Pennsylvania , USA – name: 16 Center for Cancer Cell Therapy , Stanford Cancer Institute , Stanford , California , USA |
| Author_xml | – sequence: 1 givenname: Kevin Owen orcidid: 0000-0002-4359-3569 surname: McNerney fullname: McNerney, Kevin Owen email: kmcnern1@jhmi.edu organization: Oncology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA – sequence: 2 givenname: Rebecca M surname: Richards fullname: Richards, Rebecca M organization: Hematology, Oncology, and Bone Marrow Transplant, University of Wisconsin-Madison, Madison, Wisconsin, USA – sequence: 3 givenname: Paibel surname: Aguayo-Hiraldo fullname: Aguayo-Hiraldo, Paibel organization: Cancer and Blood Disease Institute, Keck School of Medicine of USC, Los Angeles, California, USA – sequence: 4 givenname: Friso G surname: Calkoen fullname: Calkoen, Friso G organization: Division of Pediatric Oncology, Princess Maxima Center, Utrecht, The Netherlands – sequence: 5 givenname: Julie-An surname: Talano fullname: Talano, Julie-An organization: Division of Hematology/Oncology/Blood and Marrow TransplantationDepartment of Pediatrics, Medical College of Wisconsin and Children’s Wisconsin, Milwaukee, Wisconsin, USA – sequence: 6 givenname: Amy surname: Moskop fullname: Moskop, Amy organization: Division of Hematology/Oncology/Blood and Marrow TransplantationDepartment of Pediatrics, Medical College of Wisconsin and Children’s Wisconsin, Milwaukee, Wisconsin, USA – sequence: 7 givenname: Adriana surname: Balduzzi fullname: Balduzzi, Adriana organization: Clinica Pediatrica Università degli Studi di Milano Bicocca, Fondazione IRCCS San Gerardo dai Tintori, Milan, Italy – sequence: 8 givenname: Jennifer surname: Krajewski fullname: Krajewski, Jennifer organization: Pediatric Blood and Marrow Transplantation, Hackensack Meridian School of Medicine, Hackensack, New Jersey, USA – sequence: 9 givenname: Hema surname: Dave fullname: Dave, Hema organization: Cancer Immunology and Microbial Oncology Research Program, Children's National Hospital, Washington, District of Columbia, USA – sequence: 10 givenname: Anant surname: Vatsayan fullname: Vatsayan, Anant organization: Center for Cancer and Blood Disorders, Children's National Hospital, Washington, District of Columbia, USA – sequence: 11 givenname: Colleen surname: Callahan fullname: Callahan, Colleen organization: Division of Oncology and Cancer Immunotherapy Program, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA – sequence: 12 givenname: Hongyan surname: Liu fullname: Liu, Hongyan organization: Department of Pediatrics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA – sequence: 13 givenname: Yimei surname: Li fullname: Li, Yimei organization: Department of Pediatrics, University of Pennsylvania, Philadelphia, Pennsylvania, USA – sequence: 14 givenname: Kara Lynn surname: Davis fullname: Davis, Kara Lynn organization: Center for Cancer Cell Therapy, Stanford Cancer Institute, Stanford, California, USA – sequence: 15 givenname: Shannon L orcidid: 0000-0003-2210-8736 surname: Maude fullname: Maude, Shannon L organization: Division of Oncology, Center for Childhood Cancer Research and Cancer Immunotherapy Program, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36707090$$D View this record in MEDLINE/PubMed |
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| DOI | 10.1136/jitc-2022-005957 |
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| Keywords | COVID-19 Receptors, Chimeric Antigen Pediatrics Hematologic Neoplasms Immunotherapy |
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| License | This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See http://creativecommons.org/licenses/by-nc/4.0/. Author(s) (or their employer(s)) 2023. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ. |
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| PublicationTitle | Journal for immunotherapy of cancer |
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| Snippet | BackgroundImmunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for... Immunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for... BACKGROUNDImmunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for... Background Immunocompromised patients are at increased risk of SARS-CoV-2 infections. Patients undergoing chimeric antigen receptor (CAR) T-cell therapy for... |
| SourceID | doaj pubmedcentral proquest crossref pubmed bmj |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database Publisher |
| StartPage | e005957 |
| SubjectTerms | Adolescent Adult Antigens Asymptomatic Betacoronavirus Blood cancer Cancer Cancer therapies Cell- and Tissue-Based Therapy Chemotherapy Child Clinical/Translational Cancer Immunotherapy Coronavirus Infections - complications Coronaviruses COVID-19 COVID-19 - complications COVID-19 vaccines Hematologic Neoplasms Hematology Hospitalization Humans Hypertension Immunization Immunotherapy Infections Intensive care Leukemia Lymphoma Medical laboratories Multisystem inflammatory syndrome in children Neoplasm Recurrence, Local Oncology Patients Pediatrics Pneumonia, Viral - complications Receptors, Chimeric Antigen Registries Remission (Medicine) Retrospective Studies SARS-CoV-2 Severe acute respiratory syndrome coronavirus 2 Stem cell transplantation Ventilators Young Adult Young adults |
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| Title | SARS-CoV-2 infections in pediatric and young adult recipients of chimeric antigen receptor T-cell therapy: an international registry report |
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