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X-linked agammaglobulinemia (XLA):Phenotype, diagnosis, and therapeutic challenges around the world

Zeinab A El-Sayed 1, Irina Abramova 2, Juan Carlos Aldave 3, Waleed Al-Herz 4, Liliana Bezrodnik 5, Rachida Boukari 6, Ahmed Aziz Bousfiha 7, Caterina Cancrini 8, Antonio Condino-Neto 9, Ghassan Dbaibo 10, Beata Derfalvi 11, Figen Dogu 12, J David M Edgar 13, Brian Eley 14, Rasha Hasan El-Owaidy 1, Sara Elva Espinosa-Padilla 15, Nermeen Galal 16, Filomeen Haerynck 17 18, Rima Hanna-Wakim 10, Elham Hossny 1, Aydan Ikinciogullari 12, Ebtihal Kamal 19, Hirokazu Kanegane 20, Nadia Kechout 6, Yu Lung Lau 20, Tomohiro Morio 21, Viviana Moschese 22, Joao Farela Neves 23, Monia Ouederni 24, Roberto Paganelli 25, Kenneth Paris 26, Claudio Pignata 27, Alessandro Plebani 28, Farah Naz Qamar 29, Sonia Qureshi 29, Nita Radhakrishnan 30, Nima Rezaei 31, Nelson Rosario 32, John Routes 33, Berta Sanchez 34, Anna Sediva 35, Mikko Rj Seppanen 36, Edith Gonzalez Serrano 15, Anna Shcherbina 2, Surjit Singh 37, Sangeetha Siniah 38 39 40, Guiseppe Spadaro 26, Mimi Tang 41, Ana Maria Vinet 42, Alla Volokha 43, Kathleen E Sullivan 44

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Pediatric Allergy and Immunology Unit, Children's Hospital, Ain Shams University, Cairo, Egypt.
Department of Immunology, National Medical and Research Center for Pediatric Hematology, Oncology and Immunology, Moscow, Russia.
Primary Immunodeficiency Unit, Allergy and Immunology Division, Hospital Nacional Edgardo Rebagliati Martins, Lima, Peru.
Department of Pediatrics, Faculty of Medicine, Kuwait University, Allergy and Clinical Immunology Unit, Al-Sabah Hospital, Kuwait City, Kuwait.
Immunology Unit Hospital de Niños Ricardo Gutiérrez and CIC (Clinical Immunology Center), CABA, Buenos Aires, Argentina.
Department of Immunology, Institut Pasteur d'Algérie, Faculty of Medicine, Algiers, Algeria.
Clinical Immunology Unit, P1, Ibn Rushd Hospital, Laboratoire d'Immunologie Clinique, Inflammation et Allergie LICIA and Medicine and Pharmacy Faculty of Hassan II University, Casablanca, Morocco.
University Department of Pediatrics, Unit of Immune and Infectious Diseases, Childrens' Hospital Bambino Gesù, "University of Rome Tor Vergata", Rome, Italy.
Department of Immunology, Institute of Biomedical Sciences, University of Sao Paulo, Sao Paulo - Sp, Brazil.
Division of Pediatric Infectious Diseases and Center for Infectious Diseases Research, Department of Pediatrics and Adolescent Medicine, American University of Beirut, Beirut, Lebanon.
Dalhousie University, IWK Health Centre, Halifax, Nova Scotia, Canada.
Ankara University School of Medicine, Department of Pediatric Immunology and Allergy, Ankara, Turkey.
The Royal Hospitals & Queen's University Belfast, United Kingdom.
Paediatric Infectious Diseases Unit, Red Cross War Memorial Children's Hospital and the Department of Paediatrics and Child Health, University of Cape Town, Cape Town, South Africa.
The Immunodeficiencies Research Unit, National Institute of Pediatrics, Mexico City, Mexico.
Department of Pediatrics, Faculty of Medicine, Cairo University, Egypt.
Primary Immunodeficiency Research Lab, Ghent University, Belgium.
Centre for Primary Immunodeficiency, Department of Pediatric Pulmonology and Immunology, Ghent University Hospital, Belgium.
Department of Microbiology, Parasitology and Immunology, Faculty of Medicine, University of Khartoum, Sudan.
Department of Child Health and Development, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University (TMDU), Tokyo, Japan.
Department of Paediatrics and Adolescent Medicine, Queen Mary Hospital, The University of Hong Kong, Hong Kong, China.
Pediatric Immunopathology and Allergology Unit, Tor Vergata University Hospital, University of Rome Tor Vergata, Rome, Italy.
Primary Immunodeficiencies Unit, Hospital Dona Estefânia, Centro Hospitalar de Lisboa Central and CEDOC Nova Medical School, Lisboa, Portugal.
Pediatric Immuno-hematology Unit, Bone Marrow Transplantation Center, University Tunis El Manar, Faculty of Medicine, Tunis, Tunisia.
Department of Medicine and Sciences of Aging, University "G. d'Annunzio" of Chieti-Pescara, Italy.
LSU Health Sciences Center, New Orleans, LA, USA.
Department of Translational Medical Sciences, Section of Pediatrics, Federico II University, Naples, Italy.
Pediatrics Clinic and Institute for Molecular Medicine A. Nocivelli, Department of Clinical and Experimental Sciences, University of Brescia and ASST-Spedali Civili of Brescia, Brescia, Italy.
Department of Pediatric and Child Health, Aga Khan University Hospital, Karachi, Pakistan.
Department of Pediatric Hematology Oncology, Super Speciality Pediatric Hospital and PG Teaching Institute, Noida, India.
Research Center for Immunodeficiencies, Children's Medical Center, Tehran University of Medical Sciences, and Network of Immunity in Infection, Malignancy and Autoimmunity (NIIMA), Universal Scientific Education and Research Network (USERN), Tehran, Iran.
Federal University of Parana, Curitiba, Brazil.
Division of Allergy and Clinical Immunology, Department of Pediatrics, Medical College of Wisconsin, Milwaukee, WI, USA.
Servicio de Inmunología, Hospital Universitario Virgen del Rocío, Seville, Spain.
Department of Immunology, 2nd Faculty of Medicine, Charles University and Motol University Hospital, Prague, Czech Republic.
Rare Diseases Center, Children's Hospital and Adult Immunodeficiency Unit, Infectious Diseases, Inflammation Center, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
Department of Pediatrics and Chief, Allergy Immunology Unit, Advanced Pediatrics Centre, Post Graduate Institute of Medical Education and Research (PGIMER), Chandigarh, India.
Paediatric Institute Kuala Lumpur General Hospital, Kuala Lumpur, Malaysia.
Department of Allergy and Immunology, The Royal Children's Hospital Melbourne, Australia.
Murdoch Children's Research Institute, Melbourne, Australia.
The University of Melbourne, Australia.
Hospital HHA, Universidad de la Frontera, Temuco, Chile.
Department of Pediatric Infectious Diseases and Immunology, Shupyk National Medical Academy of Postgraduate Education and Center for Clinical Immunology, City Children's Hospital N1, Kiev, Ukraine.
Division of Allergy Immunology, Department of Pediatrics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA.

22 March 2019

doi: 10.1016/j.waojou.2019.100018

Abstract

Background: X-linked agammaglobulinemia is an inherited immunodeficiency recognized since 1952. In spite of seven decades of experience, there is still a limited understanding of regional differences in presentation and complications. This study was designed by the Primary Immunodeficiencies Committee of the World Allergy Organization to better understand regional needs, challenges and unique patient features.

Methods: A survey instrument was designed by the Primary Immunodeficiencies Committee of the World Allergy Organization to collect both structured and semi-structured data on X-linked agammaglobulinemia. The survey was sent to 54 centers around the world chosen on the basis of World Allergy Organization participation and/or registration in the European Society for Immunodeficiencies. There were 40 centers that responded, comprising 32 countries.

Results: This study reports on 783 patients from 40 centers around the world. Problems with diagnosis are highlighted by the reported delays in diagnosis>24 months in 34% of patients and the lack of genetic studies in 39% of centers Two infections exhibited regional variation. Vaccine-associated paralytic poliomyelitis was seen only in countries with live polio vaccination and two centers reported mycobacteria. High rates of morbidity were reported. Acute and chronic lung diseases accounted for 41% of the deaths. Unusual complications such as inflammatory bowel disease and large granular lymphocyte disease, among others were specifically enumerated, and while individually uncommon, they were collectively seen in 20.3% of patients. These data suggest that a broad range of both inflammatory, infectious, and autoimmune conditions can occur in patients. The breadth of complications and lack of data on management subsequently appeared as a significant challenge reported by centers. Survival above 20 years of age was lowest in Africa (22%) and reached above 70% in Australia, Europe and the Americas. Centers were asked to report their challenges and responses (n = 116) emphasized the difficulties in access to immunoglobulin products (16%) and reflected the ongoing need for education of both patients and referring physicians.

Conclusions: This is the largest study of patients with X-linked agammaglobulinemia and emphasizes the continued morbidity and mortality of XLA despite progress in diagnosis and treatment. It presents a world view of the successes and challenges for patients and physicians alike. A pivotal finding is the need for education of physicians regarding typical symptoms suggesting a possible diagnosis of X-linked agammaglobulinemia and sharing of best practices for the less common complications.

Keywords: Agammaglobulinemia; Autoimmunity; CLD, Chronic lung disease; FH, Family history; GI, Gastrointestinal; Immunoglobulin; Infection; JIA, juvenile idiopathic arthritis; Outcomes; SCIG, Subcutaneous immunoglobulin; Therapy; VAPP, Vaccine associated paralytic poliomyelitis; XLA; XLA, X-linked agammaglobulinemia.

Figures

Fig. 1 A world map is displayed with the approximate locations of the reporting centers indicated with asterisks.

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A Registry Study of 240 Patients with X-Linked Agammaglobulinemia Living in the USA.

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SARS-CoV-2 spike antibody concentration in gamma globulin products from high-prevalence COVID-19 countries are transmitted to X-linked agammaglobulinemia patients.

Raphael A, Shamriz O, Tvito A, Magen S, Goldberg S, Megged O, Lev A, Simon AJ, Tal Y, Somech R, Eisenberg R, Toker O.Front Immunol. 2023 Mar 29;14:1156823. doi: 10.3389/fimmu.2023.1156823. eCollection 2023.PMID: 37063907 Free PMC article.

Co-Occurring X-Linked Agammaglobulinemia and X-Linked Chronic Granulomatous Disease: Two Isolated Pathogenic Variants in One Patient.

Gunderman L, Brown J, Chaudhury S, O'Gorman M, Fuleihan R, Khanolkar A, Ahmed A.Biomedicines. 2023 Mar 21;11(3):959. doi: 10.3390/biomedicines11030959.PMID: 36979938 Free PMC article.

Real-World Evidence of Tolerability of 20% Subcutaneous Immunoglobulin Treatment.

Rosenbach K, Park M, Sanchirico M, Nwose O, Paris K.J Clin Immunol. 2023 Feb 21. doi: 10.1007/s10875-023-01436-4. Online ahead of print.PMID: 36809598

BT595, a 10% Human Normal Immunoglobulin, for Replacement Therapy of Primary Immunodeficiency Disease: Results of a Subcohort Analysis in Children.

Kriván G, Borte M, Soler-Palacin P, Church JA, Csurke I, Harris JB, Lieberman JA, Melamed IR, Moy JN, Simon R, Aigner S, Lentze S, Staiger C.J Clin Immunol. 2023 Apr;43(3):557-567. doi: 10.1007/s10875-022-01397-0. Epub 2022 Nov 16.PMID: 36383294 Free PMC article.

KMEL References

https://pubmed.ncbi.nlm.nih.gov/

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X-linked agammaglobulinemia (XLA):Phenotype, diagnosis, and therapeutic challenges around the world

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