Cardiac Complications Associated With Checkpoint Inhibition: A Systematic Review of the Literature in an Important Emerging Area

Immune checkpoint inhibitors, including programmed cell death-1, programmed cell death ligand-1 and cytotoxic lymphocyte antigen-4 inhibitors, have emerged as important therapeutic alternatives for advanced malignancies. This drug class upregulates T-cell activity, leading to an immune response agai...

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Published in:Canadian journal of cardiology Vol. 34; no. 8; pp. 1059 - 1068
Main Authors: Mir, Hassan, Alhussein, Muhammad, Alrashidi, Sulaiman, Alzayer, Hussain, Alshatti, Ahmad, Valettas, Nicholas, Mukherjee, Som D., Nair, Vidhya, Leong, Darryl P.
Format: Journal Article
Language:English
Published: England Elsevier Inc 01.08.2018
ISSN:0828-282X, 1916-7075, 1916-7075
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Abstract Immune checkpoint inhibitors, including programmed cell death-1, programmed cell death ligand-1 and cytotoxic lymphocyte antigen-4 inhibitors, have emerged as important therapeutic alternatives for advanced malignancies. This drug class upregulates T-cell activity, leading to an immune response against cancer cells. However, the increased activity of T cells can lead to autoimmune reactions. We conducted a systematic review of all published articles and grey literature in PubMed, Medline, and Embase on cardiac complications associated with checkpoint inhibitor use from September 1, 1996 to November 10, 2017. The search strategy yielded 908 unique articles. Of these, 835 were excluded on the basis of abstract and full-text review. A total of 73 studies met eligibility criteria and were included. We found a total of 99 cases of cardiotoxicity with the use of checkpoint inhibitors. Myocarditis (45%) was the most common cardiotoxicity. The overall case fatality rate was 35%. This was notably higher in patients with myocarditis, complete heart block, or conduction abnormalities, and ventricular arrhythmias. There was no difference in outcomes for patients treated with or without steroids. Immunosuppressive therapies such as infliximab, mycophenolate, intravenous immunoglobulin, antithymocyte globulin, and/or plasmapheresis were used in 12 patients leading to survival in 9 of these patients (75%). Immune checkpoint inhibitors are associated with cardiotoxicity. Because of the high case fatality rate, close surveillance and prompt empiric therapy for cardiovascular complications of checkpoint inhibitors should be considered. Aggressive treatment with immunosuppressive agents and/or plasmapheresis might lead to clinical improvement and increased survival. Les inhibiteurs de points de contrôle immunitaire, par exemple ceux dirigés contre la Programmed Cell Death Protein-1 (PD-1), le Programmed Cell Death Ligand-1 (PD-L1) et l’antigène-4 des lymphocytes cytotoxiques sont devenus des options thérapeutiques de rechange importantes dans les tumeurs malignes de stade avancé. Les agents de cette classe thérapeutique régulent positivement l’activité des lymphocytes T, ce qui stimule la réponse immunitaire contre les cellules cancéreuses. Toutefois, l’activité accrue des lymphocytes T peut entraîner des réactions auto-immunes. Nous avons réalisé une revue systématique de tous les articles publiés ainsi que de la littérature grise répertoriés dans les bases de données PubMed, Medline et Embase sur les complications cardiaques associées à l’utilisation des inhibiteurs de points de contrôle entre le 1er septembre 1996 et le 10 novembre 2017. La stratégie de recherche a permis de recenser 908 articles uniques, dont 835 ont été exclus après examen du résumé et du texte intégral. Au total 73 études satisfaisaient aux critères d’admissibilité et ont été incluses. Nous avons relevé 99 cas de cardiotoxicité associés à l’utilisation des inhibiteurs de points de contrôle immunitaire. La myocardite (45 %) était l’effet cardiotoxique le plus fréquent. Le taux global de létalité était de 35 % et était sensiblement plus élevé chez les patients présentant une myocardite, un bloc cardiaque complet, ou encore des anomalies de la conduction ou des arythmies ventriculaires. Aucune différence sur le plan des résultats n’a été observée entre les patients ayant reçu des stéroïdes et ceux qui n’en avaient pas reçu. Des traitements immunosuppresseurs comme l’infliximab, le mycophénolate, les immunoglobulines intraveineuses, la globuline antithymocyte ou la plasmaphérèse ont été utilisés chez 12 patients, dont 9 ont survécu (75 %). Les inhibiteurs de points de contrôle immunitaire sont associés à des effets cardiotoxiques. En raison du taux de létalité élevé, il est important de surveiller étroitement l’apparition des complications cardiovasculaires de ces agents et, le cas échéant, d’intervenir en administrant rapidement un traitement empirique. Un traitement énergique par des agents immunosuppresseurs, la plasmaphérèse, ou les deux pourrait entraîner une amélioration clinique et une meilleure survie.
AbstractList Immune checkpoint inhibitors, including programmed cell death-1, programmed cell death ligand-1 and cytotoxic lymphocyte antigen-4 inhibitors, have emerged as important therapeutic alternatives for advanced malignancies. This drug class upregulates T-cell activity, leading to an immune response against cancer cells. However, the increased activity of T cells can lead to autoimmune reactions. We conducted a systematic review of all published articles and grey literature in PubMed, Medline, and Embase on cardiac complications associated with checkpoint inhibitor use from September 1, 1996 to November 10, 2017. The search strategy yielded 908 unique articles. Of these, 835 were excluded on the basis of abstract and full-text review. A total of 73 studies met eligibility criteria and were included. We found a total of 99 cases of cardiotoxicity with the use of checkpoint inhibitors. Myocarditis (45%) was the most common cardiotoxicity. The overall case fatality rate was 35%. This was notably higher in patients with myocarditis, complete heart block, or conduction abnormalities, and ventricular arrhythmias. There was no difference in outcomes for patients treated with or without steroids. Immunosuppressive therapies such as infliximab, mycophenolate, intravenous immunoglobulin, antithymocyte globulin, and/or plasmapheresis were used in 12 patients leading to survival in 9 of these patients (75%). Immune checkpoint inhibitors are associated with cardiotoxicity. Because of the high case fatality rate, close surveillance and prompt empiric therapy for cardiovascular complications of checkpoint inhibitors should be considered. Aggressive treatment with immunosuppressive agents and/or plasmapheresis might lead to clinical improvement and increased survival. Les inhibiteurs de points de contrôle immunitaire, par exemple ceux dirigés contre la Programmed Cell Death Protein-1 (PD-1), le Programmed Cell Death Ligand-1 (PD-L1) et l’antigène-4 des lymphocytes cytotoxiques sont devenus des options thérapeutiques de rechange importantes dans les tumeurs malignes de stade avancé. Les agents de cette classe thérapeutique régulent positivement l’activité des lymphocytes T, ce qui stimule la réponse immunitaire contre les cellules cancéreuses. Toutefois, l’activité accrue des lymphocytes T peut entraîner des réactions auto-immunes. Nous avons réalisé une revue systématique de tous les articles publiés ainsi que de la littérature grise répertoriés dans les bases de données PubMed, Medline et Embase sur les complications cardiaques associées à l’utilisation des inhibiteurs de points de contrôle entre le 1er septembre 1996 et le 10 novembre 2017. La stratégie de recherche a permis de recenser 908 articles uniques, dont 835 ont été exclus après examen du résumé et du texte intégral. Au total 73 études satisfaisaient aux critères d’admissibilité et ont été incluses. Nous avons relevé 99 cas de cardiotoxicité associés à l’utilisation des inhibiteurs de points de contrôle immunitaire. La myocardite (45 %) était l’effet cardiotoxique le plus fréquent. Le taux global de létalité était de 35 % et était sensiblement plus élevé chez les patients présentant une myocardite, un bloc cardiaque complet, ou encore des anomalies de la conduction ou des arythmies ventriculaires. Aucune différence sur le plan des résultats n’a été observée entre les patients ayant reçu des stéroïdes et ceux qui n’en avaient pas reçu. Des traitements immunosuppresseurs comme l’infliximab, le mycophénolate, les immunoglobulines intraveineuses, la globuline antithymocyte ou la plasmaphérèse ont été utilisés chez 12 patients, dont 9 ont survécu (75 %). Les inhibiteurs de points de contrôle immunitaire sont associés à des effets cardiotoxiques. En raison du taux de létalité élevé, il est important de surveiller étroitement l’apparition des complications cardiovasculaires de ces agents et, le cas échéant, d’intervenir en administrant rapidement un traitement empirique. Un traitement énergique par des agents immunosuppresseurs, la plasmaphérèse, ou les deux pourrait entraîner une amélioration clinique et une meilleure survie.
Immune checkpoint inhibitors, including programmed cell death-1, programmed cell death ligand-1 and cytotoxic lymphocyte antigen-4 inhibitors, have emerged as important therapeutic alternatives for advanced malignancies. This drug class upregulates T-cell activity, leading to an immune response against cancer cells. However, the increased activity of T cells can lead to autoimmune reactions.BACKGROUNDImmune checkpoint inhibitors, including programmed cell death-1, programmed cell death ligand-1 and cytotoxic lymphocyte antigen-4 inhibitors, have emerged as important therapeutic alternatives for advanced malignancies. This drug class upregulates T-cell activity, leading to an immune response against cancer cells. However, the increased activity of T cells can lead to autoimmune reactions.We conducted a systematic review of all published articles and grey literature in PubMed, Medline, and Embase on cardiac complications associated with checkpoint inhibitor use from September 1, 1996 to November 10, 2017.METHODSWe conducted a systematic review of all published articles and grey literature in PubMed, Medline, and Embase on cardiac complications associated with checkpoint inhibitor use from September 1, 1996 to November 10, 2017.The search strategy yielded 908 unique articles. Of these, 835 were excluded on the basis of abstract and full-text review. A total of 73 studies met eligibility criteria and were included. We found a total of 99 cases of cardiotoxicity with the use of checkpoint inhibitors. Myocarditis (45%) was the most common cardiotoxicity. The overall case fatality rate was 35%. This was notably higher in patients with myocarditis, complete heart block, or conduction abnormalities, and ventricular arrhythmias. There was no difference in outcomes for patients treated with or without steroids. Immunosuppressive therapies such as infliximab, mycophenolate, intravenous immunoglobulin, antithymocyte globulin, and/or plasmapheresis were used in 12 patients leading to survival in 9 of these patients (75%).RESULTSThe search strategy yielded 908 unique articles. Of these, 835 were excluded on the basis of abstract and full-text review. A total of 73 studies met eligibility criteria and were included. We found a total of 99 cases of cardiotoxicity with the use of checkpoint inhibitors. Myocarditis (45%) was the most common cardiotoxicity. The overall case fatality rate was 35%. This was notably higher in patients with myocarditis, complete heart block, or conduction abnormalities, and ventricular arrhythmias. There was no difference in outcomes for patients treated with or without steroids. Immunosuppressive therapies such as infliximab, mycophenolate, intravenous immunoglobulin, antithymocyte globulin, and/or plasmapheresis were used in 12 patients leading to survival in 9 of these patients (75%).Immune checkpoint inhibitors are associated with cardiotoxicity. Because of the high case fatality rate, close surveillance and prompt empiric therapy for cardiovascular complications of checkpoint inhibitors should be considered. Aggressive treatment with immunosuppressive agents and/or plasmapheresis might lead to clinical improvement and increased survival.CONCLUSIONSImmune checkpoint inhibitors are associated with cardiotoxicity. Because of the high case fatality rate, close surveillance and prompt empiric therapy for cardiovascular complications of checkpoint inhibitors should be considered. Aggressive treatment with immunosuppressive agents and/or plasmapheresis might lead to clinical improvement and increased survival.
Immune checkpoint inhibitors, including programmed cell death-1, programmed cell death ligand-1 and cytotoxic lymphocyte antigen-4 inhibitors, have emerged as important therapeutic alternatives for advanced malignancies. This drug class upregulates T-cell activity, leading to an immune response against cancer cells. However, the increased activity of T cells can lead to autoimmune reactions. We conducted a systematic review of all published articles and grey literature in PubMed, Medline, and Embase on cardiac complications associated with checkpoint inhibitor use from September 1, 1996 to November 10, 2017. The search strategy yielded 908 unique articles. Of these, 835 were excluded on the basis of abstract and full-text review. A total of 73 studies met eligibility criteria and were included. We found a total of 99 cases of cardiotoxicity with the use of checkpoint inhibitors. Myocarditis (45%) was the most common cardiotoxicity. The overall case fatality rate was 35%. This was notably higher in patients with myocarditis, complete heart block, or conduction abnormalities, and ventricular arrhythmias. There was no difference in outcomes for patients treated with or without steroids. Immunosuppressive therapies such as infliximab, mycophenolate, intravenous immunoglobulin, antithymocyte globulin, and/or plasmapheresis were used in 12 patients leading to survival in 9 of these patients (75%). Immune checkpoint inhibitors are associated with cardiotoxicity. Because of the high case fatality rate, close surveillance and prompt empiric therapy for cardiovascular complications of checkpoint inhibitors should be considered. Aggressive treatment with immunosuppressive agents and/or plasmapheresis might lead to clinical improvement and increased survival.
Author Mukherjee, Som D.
Alshatti, Ahmad
Valettas, Nicholas
Alzayer, Hussain
Alrashidi, Sulaiman
Mir, Hassan
Alhussein, Muhammad
Nair, Vidhya
Leong, Darryl P.
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  surname: Alhussein
  fullname: Alhussein, Muhammad
  organization: The Division of Cardiology, Department of Medicine, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
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  givenname: Sulaiman
  surname: Alrashidi
  fullname: Alrashidi, Sulaiman
  organization: The Division of Cardiology, Department of Medicine, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
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  givenname: Hussain
  orcidid: 0000-0002-8965-9690
  surname: Alzayer
  fullname: Alzayer, Hussain
  organization: The Division of Cardiology, Department of Medicine, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
– sequence: 5
  givenname: Ahmad
  surname: Alshatti
  fullname: Alshatti, Ahmad
  organization: The Division of Cardiology, Department of Medicine, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
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  givenname: Nicholas
  surname: Valettas
  fullname: Valettas, Nicholas
  organization: The Division of Cardiology, Department of Medicine, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
– sequence: 7
  givenname: Som D.
  surname: Mukherjee
  fullname: Mukherjee, Som D.
  organization: Department of Oncology, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
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  givenname: Vidhya
  surname: Nair
  fullname: Nair, Vidhya
  organization: Department of Pathology and Molecular Medicine, McMaster University, Hamilton, Ontario, Canada
– sequence: 9
  givenname: Darryl P.
  surname: Leong
  fullname: Leong, Darryl P.
  email: leongd@phri.ca
  organization: The Population Health Research Institute, McMaster University and Hamilton Health Sciences, Hamilton, Ontario, Canada
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29980467$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2018 Canadian Cardiovascular Society
Copyright © 2018 Canadian Cardiovascular Society. Published by Elsevier Inc. All rights reserved.
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