Allogeneic Hematopoietic Stem Cell Transplantation in Immunodeficiency-Centromeric Instability-Facial Dysmorphism (ICF) Syndrome: an EBMT/ESID Inborn Errors Working Party Study.


Journal

Journal of clinical immunology
ISSN: 1573-2592
Titre abrégé: J Clin Immunol
Pays: Netherlands
ID NLM: 8102137

Informations de publication

Date de publication:
21 Aug 2024
Historique:
received: 27 03 2024
accepted: 06 08 2024
medline: 21 8 2024
pubmed: 21 8 2024
entrez: 21 8 2024
Statut: epublish

Résumé

Immunodeficiency-Centromeric instability-Facial dysmorphism (ICF) syndrome is an inborn error of immunity characterized by progressive immune dysfunction and multi-organ disease usually treated with antimicrobial prophylaxis and immunoglobulin substitution. Allogeneic hematopoietic stem cell transplantation (HSCT) is the only curative treatment, but data on outcome are scarce. We provide a detailed description of disease characteristics and HSCT outcome in an international cohort of ICF syndrome patients. Eighteen patients (including all four genotypes) were enrolled. Main HSCT indications were infections (83%), enteropathy/failure to thrive (56%), immune dysregulation (22%) and myelodysplasia/haematological malignancy (17%). Two patients underwent pre-emptive HSCT after early diagnosis. Patients were transplanted between 2003-2021, at median age 4.3 years (range 0.5-19), after myeloablative or reduced-intensity conditioning, from matched sibling or matched family donors, matched unrelated or mismatched donors in 39%, 50% and 12% of cases respectively. Overall survival was 83% (all deaths occurred within the first 5 months post-HSCT; mean follow-up 54 months (range 1-185)). Acute GvHD occurred in 35% of patients, severe (grade III) in two (12%), while none developed chronic GvHD. At latest follow-up (median 2.2 years (range 0.1-14)), complete donor chimerism was achieved in 15/17 surviving patients. All survivors demonstrated normalized T and B cell numbers. Immunoglobulin substitution independence was achieved in all but two patients. All survivors recovered from pre-transplant infections, enteropathy/failure to thrive and immune dysregulation. All three patients transplanted at young age (≤ 3 years), after early diagnosis, survived. The favourable clinical and immunological HSCT outcome in this cohort of patients supports the timely use of this curative treatment in ICF syndrome.

Identifiants

pubmed: 39167297
doi: 10.1007/s10875-024-01786-7
pii: 10.1007/s10875-024-01786-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

182

Informations de copyright

© 2024. The Author(s).

Références

Hagleitner MM, et al. Clinical spectrum of immunodeficiency, centromeric instability and facial dysmorphism (ICF syndrome). J Med Genet. 2008;45(2):93–9.
pubmed: 17893117
Weemaes CM, et al. Heterogeneous clinical presentation in ICF syndrome: correlation with underlying gene defects. Eur J Hum Genet. 2013;21(11):1219–25.
pubmed: 23486536 pmcid: 3798845
Thijssen PE, et al. Mutations in CDCA7 and HELLS cause immunodeficiency-centromeric instability-facial anomalies syndrome. Nat Commun. 2015;6:7870.
pubmed: 26216346
Blanco-Betancourt CE, et al. Defective B-cell-negative selection and terminal differentiation in the ICF syndrome. Blood. 2004;103(7):2683–90.
pubmed: 14645008
Helfricht A, et al. Loss of ZBTB24 impairs nonhomologous end-joining and class-switch recombination in patients with ICF syndrome. J Exp Med 2020;217(11):e20191688.
von Bernuth H, et al. Combined immunodeficiency develops with age in Immunodeficiency-centromeric instability-facial anomalies syndrome 2 (ICF2). Orphanet J Rare Dis. 2014;9:116.
Rechavi E, et al. A novel mutation in a critical region for the methyl donor binding in DNMT3B causes immunodeficiency, centromeric instability, and facial anomalies syndrome (ICF). J Clin Immunol. 2016;36(8):801–9.
pubmed: 27734333
Sterlin D, et al. Genetic, cellular and clinical features of ICF syndrome: a French national survey. J Clin Immunol. 2016;36(2):149–59.
pubmed: 26851945
Kamae C, et al. Clinical and immunological characterization of ICF syndrome in Japan. J Clin Immunol. 2018;38(8):927–37.
pubmed: 30353301
Sogkas G, et al. Progressive immunodeficiency with gradual depletion of B and CD4(+) T cells in immunodeficiency, centromeric instability and facial anomalies syndrome 2 (ICF2). Diseases. 2019;7(2):34.
Staudacher O, et al. Screening newborns for low T cell receptor excision circles (TRECs) fails to detect immunodeficiency, centromeric instability, and facial anomalies syndrome. J Allergy Clin Immunol Pract. 2023;11(9):2872–83.
pubmed: 37302792
Bilgic Eltan S, et al. Evaluation of clinical and immunological alterations associated with ICF syndrome. J Clin Immunol. 2023;44(1):26.
pubmed: 38129713
Unoki M. Exploring the intersection of epigenetics, DNA repair, and immunology from studies of ICF syndrome, an inborn error of immunity. Front Immunol. 2024;15: 1405022.
pubmed: 38799442 pmcid: 11116680
Brown DC, et al. ICF syndrome (immunodeficiency, centromeric instability and facial anomalies): investigation of heterochromatin abnormalities and review of clinical outcome. Hum Genet. 1995;96(4):411–6.
pubmed: 7557962
Gennery AR, et al. Hematopoietic stem cell transplantation corrects the immunologic abnormalities associated with immunodeficiency-centromeric instability-facial dysmorphism syndrome. Pediatrics. 2007;120(5):e1341–4.
pubmed: 17908720
Harnisch E, et al. Hematopoietic stem cell transplantation in a patient with ICF2 syndrome presenting with EBV-induced hemophagocytic lymphohystiocytosis. Transplantation. 2016;100(7):e35–6.
pubmed: 27326813
Gossling KL, et al. Hematopoietic stem cell transplantation in an infant with immunodeficiency, centromeric instability, and facial anomaly syndrome. Front Immunol. 2017;8: 773.
pubmed: 28713390 pmcid: 5491950
Alghamdi HA, et al. Three types of immunodeficiency, centromeric instability, and facial anomalies (ICF) syndrome identified by whole-exome sequencing in Saudi hypogammaglobulinemia patients: clinical, molecular, and cytogenetic features. J Clin Immunol. 2018;38(8):847–53.
pubmed: 30511102
Burk CM, et al. Immunodeficiency, centromeric instability, and facial anomalies (ICF) syndrome with NK dysfunction and EBV-driven malignancy treated with stem cell transplantation. J Allergy Clin Immunol Pract. 2020;8(3):1103-1106 e3.
pubmed: 31520839
Kraft MT, et al. Immune reconstitution after hematopoietic stem cell transplantation in immunodeficiency-centromeric instability-facial anomalies syndrome type 1. J Clin Immunol. 2021;41(5):1089–94.
pubmed: 33544358 pmcid: 7862860
Seidel MG, et al. The European society for immunodeficiencies (ESID) registry working definitions for the clinical diagnosis of inborn errors of immunity. J Allergy Clin Immunol Pract. 2019;7(6):1763–70.
pubmed: 30776527
Lankester AC, et al. EBMT/ESID inborn errors working party guidelines for hematopoietic stem cell transplantation for inborn errors of immunity. Bone Marrow Transplant. 2021;56(9):2052–62.
pubmed: 34226669 pmcid: 8410590
Bader P. Documentation of engraftment and Chimerism after HSCT. In: Carreras E, et al., editors. The EBMT handbook: hematopoietic stem cell transplantation and cellular therapies. Cham (CH); 2019. pp. 143–7.
Jagasia MH, et al. National institutes of health consensus development project on criteria for clinical trials in chronic g-versus-host disease: I. The 2014 diagnosis and staging working group report. Biol Blood Marrow Transplant 2015;21(3):389–401 e1.
Schatorje EJ, et al. Paediatric reference values for the peripheral T cell compartment. Scand J Immunol. 2012;75(4):436–44.
pubmed: 22420532
Ueda Y, et al. Roles for Dnmt3b in mammalian development: a mouse model for the ICF syndrome. Development. 2006;133(6):1183–92.
pubmed: 16501171
Gaballa A, et al. Evaluating thymic function after human hematopoietic stem cell transplantation in the personalized medicine era. Front Immunol. 2020;11: 1341.
pubmed: 32849495 pmcid: 7412601
Chiesa R, et al. Hematopoietic cell transplantation in chronic granulomatous disease: a study of 712 children and adults. Blood. 2020;136(10):1201–11.
pubmed: 32614953
Albert MH, et al. Hematopoietic stem cell transplantation for Wiskott-Aldrich syndrome: an EBMT inborn errors working party analysis. Blood. 2022;139(13):2066–79.
pubmed: 35100336
Lankester AC, et al. Hematopoietic cell transplantation in severe combined immunodeficiency: The SCETIDE 2006–2014 European cohort. J Allergy Clin Immunol. 2022;149(5):1744–1754 e8.
pubmed: 34718043
Tangye SG, Palendira U, Edwards ES. Human immunity against EBV-lessons from the clinic. J Exp Med. 2017;214(2):269–83.
pubmed: 28108590 pmcid: 5294862

Auteurs

Dagmar Berghuis (D)

Willem-Alexander Children's Hospital, Department of Pediatrics, Division of Pediatric Immunology, Hematology and Stem Cell Transplantation, Leiden University Medical Center, Leiden, The Netherlands. d.berghuis@lumc.nl.

Lubna S Mehyar (LS)

Division of Pediatric Hematology, Oncology, Blood and Marrow Transplant, Dayton Children's Hospital/Department of Pediatrics, Boonshoft School of Medicine, Wright State University, Dayton, OH, USA.

Rolla Abu-Arja (R)

The Blood and Marrow Transplant Program, Nationwide Children's Hospital, Colombia, OH, USA.

Michael H Albert (MH)

Department of Pediatrics, Dr. Von Hauner Children's Hospital, University Hospital, LMU, Munich, Germany.

Jessie L Barnum (JL)

Division of Blood and Marrow Transplantation and Cellular Therapies, University of Pittsburgh Medical Center (UPMC) and Children's Hospital of Pittsburgh, Pittsburgh, PA, USA.

Horst von Bernuth (H)

Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Department of Pediatric Respiratory Medicine, Immunology and Critical Care Medicine, University Hospital Center, Berlin, Germany.
Department of Immunology, Labor Berlin GmbH, Berlin, Germany.
Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health (BIH), Berlin-Brandenburg Center for Regenerative Therapies (BCRT), Berlin, Germany.

Reem Elfeky (R)

Great Ormond Street (GOS) Hospital for Children National Health Service (NHS) Foundation Trust, University College London Great Ormond Street (GOS) Institute of Child Health, and National Institute for Health and Care Research (NIHR), Great Ormond Street Hospital (GOSH), Biomedical Research Centre (BRC), London, UK.

Philippe Lewalle (P)

Hematology Department, Hopital Universitaire de Bruxelles (HUB)-Institut Jules Bordet, Brussels, Belgium.

Alexandra Laberko (A)

Department of Hematopoietic Stem Cell Transplantation, Oncology and Immunology, Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Moscow, Russia.

Sujal Ghosh (S)

Department of Pediatric Oncology, Hematology and Clinical Immunology, Medical Faculty, Center of Child and Adolescent Health, Heinrich-Heine-University, Duesseldorf, Germany.

Mary A Slatter (MA)

Children's Haemopoietic Stem Cell Transplant Unit, Great North Children's Hospital, Newcastle-upon-Tyne Hospital NHS Foundation Trust, Newcastle Upon Tyne, UK.

Corry M R Weemaes (CMR)

Department of Pediatrics, Radboud University Medical Centre Nijmegen, Nijmegen, the Netherlands.

Akif Yesilipek (A)

Department of Pediatric Hematology and Pediatric Stem Cell Transplantation Unit, Medicalpark Antalya Hospital, Antalya, Turkey.

Tiarlan Sirait (T)

EBMT Leiden Study Unit, Leiden, The Netherlands.

Bénédicte Neven (B)

Immuno-hematology and rheumatology Unit, Necker Children Hospital, Imagine Institute, UMR 1163, University of Paris Cite, Paris, France.

Andrew R Gennery (AR)

Children's Haemopoietic Stem Cell Transplant Unit, Great North Children's Hospital, Newcastle-upon-Tyne Hospital NHS Foundation Trust, Newcastle Upon Tyne, UK.

Arjan C Lankester (AC)

Willem-Alexander Children's Hospital, Department of Pediatrics, Division of Pediatric Immunology, Hematology and Stem Cell Transplantation, Leiden University Medical Center, Leiden, The Netherlands.

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