Therapeutic options for CTLA-4 insufficiency.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
02 2022
Historique:
received: 19 11 2020
revised: 23 03 2021
accepted: 23 04 2021
pubmed: 11 6 2021
medline: 4 3 2022
entrez: 10 6 2021
Statut: ppublish

Résumé

Heterozygous germline mutations in cytotoxic T lymphocyte-associated antigen-4 (CTLA4) impair the immunomodulatory function of regulatory T cells. Affected individuals are prone to life-threatening autoimmune and lymphoproliferative complications. A number of therapeutic options are currently being used with variable effectiveness. Our aim was to characterize the responsiveness of patients with CTLA-4 insufficiency to specific therapies and provide recommendations for the diagnostic workup and therapy at an organ-specific level. Clinical features, laboratory findings, and response to treatment were reviewed retrospectively in an international cohort of 173 carriers of CTLA4 mutation. Patients were followed between 2014 and 2020 for a total of 2624 months from diagnosis. Clinical manifestations were grouped on the basis of organ-specific involvement. Medication use and response were recorded and evaluated. Among the 173 CTLA4 mutation carriers, 123 (71%) had been treated for immune complications. Abatacept, rituximab, sirolimus, and corticosteroids ameliorated disease severity, especially in cases of cytopenias and lymphocytic organ infiltration of the gut, lungs, and central nervous system. Immunoglobulin replacement was effective in prevention of infection. Only 4 of 16 patients (25%) with cytopenia who underwent splenectomy had a sustained clinical response. Cure was achieved with stem cell transplantation in 13 of 18 patients (72%). As a result of the aforementioned methods, organ-specific treatment pathways were developed. Systemic immunosuppressants and abatacept may provide partial control but require ongoing administration. Allogeneic hematopoietic stem cell transplantation offers a possible cure for patients with CTLA-4 insufficiency.

Sections du résumé

BACKGROUND
Heterozygous germline mutations in cytotoxic T lymphocyte-associated antigen-4 (CTLA4) impair the immunomodulatory function of regulatory T cells. Affected individuals are prone to life-threatening autoimmune and lymphoproliferative complications. A number of therapeutic options are currently being used with variable effectiveness.
OBJECTIVE
Our aim was to characterize the responsiveness of patients with CTLA-4 insufficiency to specific therapies and provide recommendations for the diagnostic workup and therapy at an organ-specific level.
METHODS
Clinical features, laboratory findings, and response to treatment were reviewed retrospectively in an international cohort of 173 carriers of CTLA4 mutation. Patients were followed between 2014 and 2020 for a total of 2624 months from diagnosis. Clinical manifestations were grouped on the basis of organ-specific involvement. Medication use and response were recorded and evaluated.
RESULTS
Among the 173 CTLA4 mutation carriers, 123 (71%) had been treated for immune complications. Abatacept, rituximab, sirolimus, and corticosteroids ameliorated disease severity, especially in cases of cytopenias and lymphocytic organ infiltration of the gut, lungs, and central nervous system. Immunoglobulin replacement was effective in prevention of infection. Only 4 of 16 patients (25%) with cytopenia who underwent splenectomy had a sustained clinical response. Cure was achieved with stem cell transplantation in 13 of 18 patients (72%). As a result of the aforementioned methods, organ-specific treatment pathways were developed.
CONCLUSION
Systemic immunosuppressants and abatacept may provide partial control but require ongoing administration. Allogeneic hematopoietic stem cell transplantation offers a possible cure for patients with CTLA-4 insufficiency.

Identifiants

pubmed: 34111452
pii: S0091-6749(21)00891-5
doi: 10.1016/j.jaci.2021.04.039
pii:
doi:

Substances chimiques

CTLA-4 Antigen 0
CTLA4 protein, human 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

736-746

Subventions

Organisme : NCI NIH HHS
ID : K08 CA219473
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021. Published by Elsevier Inc.

Auteurs

David Egg (D)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Ina Caroline Rump (IC)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Noriko Mitsuiki (N)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Jessica Rojas-Restrepo (J)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Maria-Elena Maccari (ME)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany; Division of Pediatric Hematology and Oncology, Department of Pediatrics and Adolescent Medicine, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Charlotte Schwab (C)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Annemarie Gabrysch (A)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Klaus Warnatz (K)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany; Department of Rheumatology and Clinical Immunology, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Sigune Goldacker (S)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany; Department of Rheumatology and Clinical Immunology, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Virginia Patiño (V)

Immunology Team, American Insurance, Montevideo, Uruguay.

Daniel Wolff (D)

Department of Internal Medicine III, University Hospital Regensburg, Regensburg, Germany.

Satoshi Okada (S)

Department of Pediatrics, Hiroshima University Graduate School of Biomedical and Health Sciences, Hiroshima, Japan.

Seiichi Hayakawa (S)

Department of Pediatrics, Hiroshima University Graduate School of Biomedical and Health Sciences, Hiroshima, Japan.

Yoshiaki Shikama (Y)

Division of Infection, Immunology and Infection, Kanagawa Children's Medical Center, Yokohama, Japan.

Kenji Kanda (K)

Department of Pediatrics, Hikone Municipal Hospital, Shiga, Japan.

Kohsuke Imai (K)

Department of Community Pediatrics, Perinatal and Maternal Medicine, Tokyo Medical and Dental University, Tokyo, Japan.

Manabu Sotomatsu (M)

Department of Hematology/Oncology, Gunma Children's Medical Center, Shibukawa, Japan.

Makoto Kuwashima (M)

Department of Pediatrics, Kiryu Kosei General Hospital, Kiryū, Japan.

Takahiro Kamiya (T)

Department of Lifetime Clinical Immunology, Tokyo Medical and Dental University, Tokyo, Japan.

Tomohiro Morio (T)

Department of Pediatrics and Developmental Biology, Tokyo Medical and Dental University, Tokyo, Japan.

Kazuaki Matsumoto (K)

Department of Pediatrics and Developmental Biology, Tokyo Medical and Dental University, Tokyo, Japan.

Takeshi Mori (T)

Department of Hematology and Oncology, Hyogo Prefectural Kobe Children's Hospital, Kobe, Japan.

Yuri Yoshimoto (Y)

Department of Pediatrics, Center Hospital of the National Center for Global Health and Medicine, Tokyo, Japan.

Ingunn Dybedal (I)

Department of Hematology, Oslo University Hospital, Oslo, Norway.

Maria Kanariou (M)

Department of Immunology and Histocompatibility, Center for Primary Immunodeficiencies-Paediatric Immunology, Aghia Sophia Children's Hospital, Athens, Greece.

Zeynep Yesim Kucuk (ZY)

Division of Bone Marrow Transplantation and Immune Deficiency, Children's Hospital Medical Center, Cincinnati, Ohio.

Hugo Chapdelaine (H)

Division of Clinical Immunology, Montreal Clinical Research Institute, Montreal, Quebec, Canada.

Lenka Petruzelkova (L)

Department of Paediatrics, Motol University Hospital, Second Medical Faculty in Prague, Charles University, Prague, Czech Republic.

Hanns-Martin Lorenz (HM)

Division of Rheumatology, Department of Internal Medicine V, University of Heidelberg, Heidelberg, Germany.

Kathleen E Sullivan (KE)

The Children's Hospital of Philadelphia, Perelman School of Medicine, University of Pennsylvania.

Jennifer Heimall (J)

The Children's Hospital of Philadelphia, Perelman School of Medicine, University of Pennsylvania.

Michel Moutschen (M)

Department of Infectious Diseases and General Internal Medicine, University Hospital of Liège.

Jiri Litzman (J)

Department of Clinical Immunology and Allergology, Medical Faculty, Masaryk University, Brno, Czech Republic; Department of Clinical Immunology and Allergology, St. Anne's University Hospital, Brno, Czech Republic.

Mike Recher (M)

Immunodeficiency Clinic, Medical Outpatient Unit and Immunodeficiency Lab, Department Biomedicine, University Hospital, Basel, Switzerland.

Michael H Albert (MH)

Department of Pediatrics, Dr von Hauner Children's Hospital, University Hospital, Ludwig Maximilians Universität München, Munich, Germany.

Fabian Hauck (F)

Department of Pediatrics, Dr von Hauner Children's Hospital, University Hospital, Ludwig Maximilians Universität München, Munich, Germany.

Suranjith Seneviratne (S)

Institute of Immunology and Transplantation, Royal Free Hospital, University College London, London, United Kingdom.

Jana Pachlopnik Schmid (J)

Division of Immunology, University Children's Hospital Zurich, University of Zurich, Zurich, Switzerland.

Antonios Kolios (A)

Department of Immunology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

Gary Unglik (G)

Department of Clinical Immunology and Allergy, Royal Melbourne Hospital, Melbourne, Australia.

Christian Klemann (C)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany; Division of Pediatric Hematology and Oncology, Department of Pediatrics and Adolescent Medicine, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Scott Snapper (S)

Division of Pediatric Gastroenterology, Hepatology, and Nutrition, Boston Children's Hospital and Department of Pediatrics, Harvard Medical School, Boston, Mass.

Lisa Giulino-Roth (L)

Department of Pediatrics, Division of Pediatric Hematology/Oncology, Weill Cornell Medicine, New York, NY.

Michael Svaton (M)

Childhood Leukaemia Investigation Prague, Department of Paediatric Haematology and Oncology, Second Faculty of Medicine, Charles University and University Hospital Motol, Prague, Czech Republic.

Craig D Platt (CD)

Division of Immunology, Boston Children's Hospital and Department of Pediatrics, Harvard Medical School, Boston, Mass.

Sophie Hambleton (S)

Great North Children's Hospital, Newcastle upon Tyne Hospitals NHS Foundation Trust, and Newcastle University Translational and Clinical Research Institute, Newcastle upon Tyne, United Kingdom.

Olaf Neth (O)

Pediatric Infectious Diseases, Rheumatology and Immunology Unit, Hospital Virgen del Rocío/Instituto de Biomedicina de Sevilla, Sevilla, RECLIP, Spain.

Geraldine Gosse (G)

Montreal Clinical Research Institute, Université de Montréal, Montreal, Quebec, Canada.

Steffen Reinsch (S)

Jena University Hospital, Pediatric Gastroenterology, Jena, Germany.

Dirk Holzinger (D)

Department of Pediatric Hematology-Oncology, University of Duisburg-Essen, Essen, Germany.

Yae-Jean Kim (YJ)

Division of Infectious Diseases and Immunodeficiency, Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.

Shahrzad Bakhtiar (S)

Division of Stem Cell Transplantation and Immunology, Department of Children and Adolescents, University Hospital Frankfurt, Goethe University Frankfurt, Frankfurt am Main, Germany.

Faranaz Atschekzei (F)

Department for Clinical Rheumatology and Immunology, Hannover Medical School, Hannover, Germany.

Reinhold Schmidt (R)

Department for Clinical Rheumatology and Immunology, Hannover Medical School, Hannover, Germany.

Georgios Sogkas (G)

Department for Clinical Rheumatology and Immunology, Hannover Medical School, Hannover, Germany.

Shanmuganathan Chandrakasan (S)

Division of Bone Marrow Transplant, Aflac Cancer and Blood Disorders Center, Children's Healthcare of Atlanta, Emory University School of Medicine, Atlanta, Ga.

William Rae (W)

Department of Immunology, University Hospital Southampton NHSFT, Southampton, United Kingdom; Southampton National Institute for Health Research Clinical Research Facility, University Hospital Southampton NHSFT, Southampton, United Kingdom.

Beata Derfalvi (B)

Division of Immunology, IWK Health Centre and Dalhousie University, Department of Pediatrics, Halifax, Nova Scotia, Canada.

Hanne Vibeke Marquart (HV)

Department of Clinical Immunology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.

Ahmet Ozen (A)

Marmara University School of Medicine, Division of Pediatric Allergy and Immunology, Istanbul, Turkey.

Ayca Kiykim (A)

Marmara University School of Medicine, Division of Pediatric Allergy and Immunology, Istanbul, Turkey.

Elif Karakoc-Aydiner (E)

Marmara University School of Medicine, Division of Pediatric Allergy and Immunology, Istanbul, Turkey.

Pavlína Králíčková (P)

Institute of Clinical Immunology and Allergy, University Hospital Hradec Kralove, Charles University, Faculty of Medicine in Hradec Kralove, Hradec Kralove, Czech Republic.

Godelieve de Bree (G)

Department of Internal Medicine, Division of Infectious Diseases, Amsterdam Institute for Infection and Immunity, Amsterdam University Medical Center, University of Amsterdam, Amsterdam, The Netherlands.

Dimitra Kiritsi (D)

Department of Dermatology, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany.

Markus G Seidel (MG)

Research Unit for Pediatric Hematology and Immunology, Division of Pediatric Hemato-Oncology, Department of Pediatric and Adolescent Medicine, Medical University Graz, Graz, Austria.

Robin Kobbe (R)

Division of Infectious Diseases, First Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Jennifer Dantzer (J)

Division of Pediatric Allergy and Immunology, and Rheumatology, Department of Pediatrics, John Hopkins University School of Medicine, Baltimore, Md.

Laia Alsina (L)

Clinical Immunology and Primary Immunodeficiencies Unit, Pediatric Allergy and Clinical Immunology Department, Hospital Sant Joan de Déu and Institut de Recerca Sant Joan de Déu, Barcelona; Clinical Immunology Unit Hospital Sant Joan de Déu-Hospital Clínic Barcelona, Universitat de Barcelona, Barcelona, Spain.

Thais Armangue (T)

Neuroimmunology Program, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Hospital Clínic, Universitat de Barcelona, Barcelona, Spain.

Vassilios Lougaris (V)

Pediatric Neuroimmunology Unit, Neurology Department, Sant Joan de Déu Children's Hospital, University of Barcelona, Barcelona, Spain.

Philipp Agyeman (P)

Pediatrics Clinic and Institute for Molecular Medicine A. Nocivelli, Department of Clinical and Experimental Sciences, University of Brescia, ASST-Spedali Civili of Brescia, Brescia, Italy.

Sofia Nyström (S)

Department of Pediatrics, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland.

David Buchbinder (D)

Department of Clinical Immunology and Transfusion Medicine, and Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.

Peter D Arkwright (PD)

Division of Pediatric Hematology, Children's Hospital of Orange County, Orange, Calif.

Bodo Grimbacher (B)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany; Department of Rheumatology and Clinical Immunology, Medical Center, Faculty of Medicine, Albert Ludwig University of Freiburg, Freiburg, Germany; Institute of Immunology and Transplantation, Royal Free Hospital, University College London, London, United Kingdom; Lydia Becker Institute of Immunology and Inflammation, University of Manchester, Royal Manchester Children's Hospital, Manchester, United Kingdom; German Center for Infection Research, Satellite Center Freiburg, Freiburg, Germany; Centre for Integrative Biological Signaling Studies, Albert Ludwig University of Freiburg, Freiburg, Germany; RESIST-Cluster of Excellence 2155 to Hannover Medical School, Satellite Center Freiburg, Freiburg, Germany. Electronic address: bodo.grimbacher@uniklinik-freiburg.de.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH