Outcomes and Treatment Strategies for Autoimmunity and Hyperinflammation in Patients with RAG Deficiency.


Journal

The journal of allergy and clinical immunology. In practice
ISSN: 2213-2201
Titre abrégé: J Allergy Clin Immunol Pract
Pays: United States
ID NLM: 101597220

Informations de publication

Date de publication:
Historique:
received: 13 10 2018
revised: 15 02 2019
accepted: 19 02 2019
pubmed: 17 3 2019
medline: 25 9 2020
entrez: 17 3 2019
Statut: ppublish

Résumé

Although autoimmunity and hyperinflammation secondary to recombination activating gene (RAG) deficiency have been associated with delayed diagnosis and even death, our current understanding is limited primarily to small case series. Understand the frequency, severity, and treatment responsiveness of autoimmunity and hyperinflammation in RAG deficiency. In reviewing the literature and our own database, we identified 85 patients with RAG deficiency, reported between 2001 and 2016, and compiled the largest case series to date of 63 patients with prominent autoimmune and/or hyperinflammatory pathology. Diagnosis of RAG deficiency was delayed a median of 5 years from the first clinical signs of immune dysregulation. Most patients (55.6%) presented with more than 1 autoimmune or hyperinflammatory complication, with the most common etiologies being cytopenias (84.1%), granulomas (23.8%), and inflammatory skin disorders (19.0%). Infections, including live viral vaccinations, closely preceded the onset of autoimmunity in 28.6% of cases. Autoimmune cytopenias had early onset (median, 1.9, 2.1, and 2.6 years for autoimmune hemolytic anemia, immune thrombocytopenia, and autoimmune neutropenia, respectively) and were refractory to intravenous immunoglobulin, steroids, and rituximab in most cases (64.7%, 73.7%, and 71.4% for autoimmune hemolytic anemia, immune thrombocytopenia, and autoimmune neutropenia, respectively). Evans syndrome specifically was associated with lack of response to first-line therapy. Treatment-refractory autoimmunity/hyperinflammation prompted hematopoietic stem cell transplantation in 20 patients. Autoimmunity/hyperinflammation can be a presenting sign of RAG deficiency and should prompt further evaluation. Multilineage cytopenias are often refractory to immunosuppressive treatment and may require hematopoietic cell transplantation for definitive management.

Sections du résumé

BACKGROUND
Although autoimmunity and hyperinflammation secondary to recombination activating gene (RAG) deficiency have been associated with delayed diagnosis and even death, our current understanding is limited primarily to small case series.
OBJECTIVE
Understand the frequency, severity, and treatment responsiveness of autoimmunity and hyperinflammation in RAG deficiency.
METHODS
In reviewing the literature and our own database, we identified 85 patients with RAG deficiency, reported between 2001 and 2016, and compiled the largest case series to date of 63 patients with prominent autoimmune and/or hyperinflammatory pathology.
RESULTS
Diagnosis of RAG deficiency was delayed a median of 5 years from the first clinical signs of immune dysregulation. Most patients (55.6%) presented with more than 1 autoimmune or hyperinflammatory complication, with the most common etiologies being cytopenias (84.1%), granulomas (23.8%), and inflammatory skin disorders (19.0%). Infections, including live viral vaccinations, closely preceded the onset of autoimmunity in 28.6% of cases. Autoimmune cytopenias had early onset (median, 1.9, 2.1, and 2.6 years for autoimmune hemolytic anemia, immune thrombocytopenia, and autoimmune neutropenia, respectively) and were refractory to intravenous immunoglobulin, steroids, and rituximab in most cases (64.7%, 73.7%, and 71.4% for autoimmune hemolytic anemia, immune thrombocytopenia, and autoimmune neutropenia, respectively). Evans syndrome specifically was associated with lack of response to first-line therapy. Treatment-refractory autoimmunity/hyperinflammation prompted hematopoietic stem cell transplantation in 20 patients.
CONCLUSIONS
Autoimmunity/hyperinflammation can be a presenting sign of RAG deficiency and should prompt further evaluation. Multilineage cytopenias are often refractory to immunosuppressive treatment and may require hematopoietic cell transplantation for definitive management.

Identifiants

pubmed: 30877075
pii: S2213-2198(19)30260-0
doi: 10.1016/j.jaip.2019.02.038
pmc: PMC6612449
mid: NIHMS1024055
pii:
doi:

Substances chimiques

Homeodomain Proteins 0
Immunosuppressive Agents 0
RAG-1 protein 128559-51-3

Types de publication

Case Reports Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1970-1985.e4

Subventions

Organisme : NIAID NIH HHS
ID : K08 AI103035
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI100887
Pays : United States
Organisme : NIAMS NIH HHS
ID : R01 AR059703
Pays : United States
Organisme : NICHD NIH HHS
ID : K12 HD043245
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL116275
Pays : United States

Informations de copyright

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

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Auteurs

Jocelyn R Farmer (JR)

Massachusetts General Hospital, Harvard Medical School, Boston, Mass.

Zsofia Foldvari (Z)

Department of Cancer Immunology, Institute for Cancer Research, Oslo University Hospital, Radiumhospitalet, Oslo, Norway.

Boglarka Ujhazi (B)

University of South Florida and Johns Hopkins All Children's Hospital, Saint Petersburg, Fla.

Suk See De Ravin (SS)

Laboratory of Host Defenses, National Institutes of Allergy and Infectious Diseases, NIH, Bethesda, Md.

Karin Chen (K)

Division of Allergy and Immunology, Department of Pediatrics, University of Utah School of Medicine, Salt Lake City, Utah.

Jack J H Bleesing (JJH)

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

Catharina Schuetz (C)

Department of Pediatrics, Medizinische Fakultät Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany.

Waleed Al-Herz (W)

Faculty of Medicine, Pediatrics Department, Kuwait University, Kuwait City, Kuwait; Allergy and Clinical Immunology Unit, Pediatrics Department, Alsabah Hospital, Kuwait City, Kuwait.

Roshini S Abraham (RS)

Department of Pathology and Laboratory Medicine, Nationwide Children's Hospital, Columbus, Ohio; Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minn.

Avni Y Joshi (AY)

Division of Pediatric Allergy/Immunology, Mayo Clinic Children's Center Rochester, Rochester, Minn.

Beatriz T Costa-Carvalho (BT)

Department of Pediatrics, UNIFESP-EPM, São Paulo, Brazil.

David Buchbinder (D)

Pediatrics/Hematology, CHOC Children's Hospital - UC Irvine, Irvine, Calif.

Claire Booth (C)

Department of Paediatric Immunology, Great Ormond Street Hospital, London, United Kingdom.

Andreas Reiff (A)

Division of Rheumatology, Children's Hospital Los Angeles, Keck School of Medicine, USC, Los Angeles, Calif.

Polly J Ferguson (PJ)

Department of Pediatrics, University of Iowa Carver College of Medicine, Iowa City, Iowa.

Asghar Aghamohammadi (A)

Research Center for Immunodeficiencies, Pediatrics Center of Excellence, Children's Medical Center, Tehran University of Medical Sciences, Tehran, Iran.

Hassan Abolhassani (H)

Research Center for Immunodeficiencies, Pediatrics Center of Excellence, Children's Medical Center, Tehran University of Medical Sciences, Tehran, Iran.

Jennifer M Puck (JM)

Department of Pediatrics, University of California San Francisco and UCSF Benioff Children's Hospital, San Francisco, Calif.

Mehdi Adeli (M)

Sidra Medicine, Weill Cornell Medicine, and Hamad Medical Corporation, Doha, Qatar.

Caterina Cancrini (C)

Academic Department of Pediatrics (DPUO), Unit of Immune and Infectious Diseases, Childrens' Hospital Bambino Gesù, Rome, Italy; Department of Systems Medicine, University of Rome Tor Vergata, Rome, Italy.

Paolo Palma (P)

Academic Department of Pediatrics (DPUO), Research Unit in Congenital and Perinatal Infection, Children's Hospital Bambino Gesù, Rome, Italy.

Alice Bertaina (A)

Department of Pediatric Hematology/Oncology and Cell and Gene Therapy, IRCCS, Ospedale Bambino Gesù, Rome, Italy.

Franco Locatelli (F)

Department of Pediatric Hematology/Oncology and Cell and Gene Therapy, IRCCS, Ospedale Bambino Gesù, Rome, Italy; Department of Pediatrics, Sapienza, University of Rome, Rome, Italy.

Gigliola Di Matteo (G)

Academic Department of Pediatrics (DPUO), Unit of Immune and Infectious Diseases, Childrens' Hospital Bambino Gesù, Rome, Italy; Department of Systems Medicine, University of Rome Tor Vergata, Rome, Italy.

Raif S Geha (RS)

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

Maria G Kanariou (MG)

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

Lilia Lycopoulou (L)

1st Department of Pediatrics, University of Athens, Aghia Sofia Children's Hospital, Athens, Greece.

Marianna Tzanoudaki (M)

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

John W Sleasman (JW)

Division of Allergy, Immunology and Pulmonary Medicine, Duke University School of Medicine, Durham, NC.

Suhag Parikh (S)

Division of Pediatric Blood and Marrow Transplantation, Duke University School of Medicine, Durham, NC.

Gloria Pinero (G)

Division of Allergy, Immunology and Pulmonary Medicine, Duke University School of Medicine, Durham, NC.

Bernard M Fischer (BM)

Division of Allergy, Immunology and Pulmonary Medicine, Duke University School of Medicine, Durham, NC.

Ghassan Dbaibo (G)

Department of Pediatrics and Adolescent Medicine, Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.

Ekrem Unal (E)

Division of Pediatric Hematology and Oncology & HCST Unit, Department of Pediatrics, Faculty of Medicine, Erciyes University, Kayseri, Turkey.

Turkan Patiroglu (T)

Division of Pediatric Hematology and Oncology & HCST Unit, Department of Pediatrics, Faculty of Medicine, Erciyes University, Kayseri, Turkey; Division of Pediatric Immunology, Department of Pediatrics, Faculty of Medicine, Erciyes University, Kayseri, Turkey.

Musa Karakukcu (M)

Division of Pediatric Hematology and Oncology & HCST Unit, Department of Pediatrics, Faculty of Medicine, Erciyes University, Kayseri, Turkey.

Khulood Khalifa Al-Saad (KK)

Salmanyia Medical Complex, Department of Pediatrics, Division of Pediatric Hematology and Oncology, Manama, Bahrain.

Meredith A Dilley (MA)

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

Sung-Yun Pai (SY)

Division of Hematology-Oncology, Boston Children's Hospital, Boston, Mass; Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, Mass; Harvard Medical School, Boston, Mass.

Cullen M Dutmer (CM)

Division of Allergy & Immunology, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, Colo.

Erwin W Gelfand (EW)

Department of Pediatrics, National Jewish Health, Denver, Colo.

Christoph B Geier (CB)

Immunology Outpatient Clinic, Vienna, Austria.

Martha M Eibl (MM)

Immunology Outpatient Clinic, Vienna, Austria; Biomedizinische Forschungs GmbH, Vienna, Austria.

Hermann M Wolf (HM)

Immunology Outpatient Clinic, Vienna, Austria; Sigmund Freud Private University-Medical School, Vienna, Austria.

Lauren A Henderson (LA)

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

Melissa M Hazen (MM)

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

Carmem Bonfim (C)

Hospital Infantil Pequeno Principe, Curitiba, Brazil.

Beata Wolska-Kuśnierz (B)

Immunology Department, Children's Memorial Health Institute, Warsaw, Poland.

Manish J Butte (MJ)

Division of Immunology, Allergy, and Rheumatology, Department of Pediatrics and Jeffrey Modell Diagnostic and Research Center, University of California, Los Angeles, Los Angeles, Calif.

Joseph D Hernandez (JD)

Department of Pediatrics, Division of Allergy, Immunology and Rheumatology, Stanford University, Stanford, Calif.

Sarah K Nicholas (SK)

Section of Immunology, Allergy, and Rheumatology, Baylor College of Medicine, Texas Children's Hospital, Houston, Texas.

Polina Stepensky (P)

Department of Bone Marrow Transplantation, Hadassah Hebrew University Hospital, Jerusalem, Israel.

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.

Maurizio Miano (M)

Haematology Unit, Department of Pediatric Haematology-Oncology, IRCCS Istituto Giannina Gaslini, Genova, Italy.

Emma Westermann-Clark (E)

Department of Internal Medicine, Division of Allergy/Immunology, University of South Florida Morsani College of Medicine, Tampa, Fla.

Vera Goda (V)

Department for Pediatric Hematology and Hemopoietic Stem Cell Transplantation, Central Hospital of Southern Pest- National Institute of Hematology and Infectious Diseases, Budapest, Hungary.

Gergely Kriván (G)

Department for Pediatric Hematology and Hemopoietic Stem Cell Transplantation, Central Hospital of Southern Pest- National Institute of Hematology and Infectious Diseases, Budapest, Hungary.

Steven M Holland (SM)

Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, Md.

Olajumoke Fadugba (O)

Division of Pulmonary, Allergy and Critical Care, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pa.

Sarah E Henrickson (SE)

Allergy Immunology Division, Department of Pediatrics, The Children's Hospital of Philadelphia, Philadelphia, Pa; Institute for Immunology, the University of Pennsylvania, Philadelphia, Pa.

Ahmet Ozen (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.

Safa Baris (S)

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

Ayca Kiykim (A)

Ministry of Health, Marmara University Pendik Training and Research Hospital, Istanbul, Turkey.

Robbert Bredius (R)

Department of Pediatrics, Section Pediatric Immunology, Infections and Stem Cell Transplantation, Leiden University Medical Center, Leiden, the Netherlands.

Birgit Hoeger (B)

Ludwig Boltzmann Institute for Rare and Undiagnosed Diseases, Vienna, Austria; CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria.

Kaan Boztug (K)

Ludwig Boltzmann Institute for Rare and Undiagnosed Diseases, Vienna, Austria; CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria; St Anna Kinderspital and Children's Cancer Research Institute, Department of Pediatrics, Medical University of Vienna, Vienna, Austria; Department of Pediatrics and Adolescent Medicine, Medical University of Vienna, Vienna, Austria.

Olga Pashchenko (O)

Department of Immunology, Pirogov Russian National Research Medical University, Russian Clinical Children's Hospital, Moscow, Russia.

Benedicte Neven (B)

Paris Descartes Sorbonne Paris Cité University, Imagine Institute, Paris, France; Pediatric Hematology-Immunology and Rheumatology Unit, Necker-Enfants Malades University Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France; Laboratory "Immunogenetics of Pediatric Autoimmune Diseases", INSERM UMR1163, Université Paris Descartes Sorbonne Paris Cité, Institut Imagine, Paris, France.

Despina Moshous (D)

Paris Descartes Sorbonne Paris Cité University, Imagine Institute, Paris, France; Pediatric Hematology-Immunology and Rheumatology Unit, Necker-Enfants Malades University Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France; Laboratory "Genome Dynamics in The Immune System", INSERM UMR1163, Université Paris Descartes Sorbonne Paris Cité, Institut Imagine, Paris, France.

Jean-Pierre de Villartay (JP)

Laboratory "Genome Dynamics in The Immune System", INSERM UMR1163, Université Paris Descartes Sorbonne Paris Cité, Institut Imagine, Paris, France.

Ahmed Aziz Bousfiha (AA)

Laboratoire d'Immunologie Clinique, d'Inflammation et d'Allergie LICIA, Faculty of Medicine and Pharmacy, Hassan II University, Casablanca, Morocco; Clinical Immunology Unit, Casablanca Children's Hospital, Ibn Rochd Medical School, Hassan II University, Casablanca, Morocco.

Harry R Hill (HR)

Division of Clinical Immunology, Departments of Pathology, Pediatrics and Medicine, University of Utah, Salt Lake City, Utah.

Luigi D Notarangelo (LD)

Haematology Unit, Department of Pediatric Haematology-Oncology, IRCCS Istituto Giannina Gaslini, Genova, Italy.

Jolan E Walter (JE)

University of South Florida and Johns Hopkins All Children's Hospital, Saint Petersburg, Fla; Division of Allergy and Immunology, Massachusetts General Hospital for Children, Boston, Mass. Electronic address: jolanwalter@health.usf.edu.

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Classifications MeSH