. 2022 Apr 21:13:900091.

doi: 10.3389/fimmu.2022.900091. eCollection 2022.

Inborn Errors of Immunity in Algerian Children and Adults: A Single-Center Experience Over a Period of 13 Years (2008-2021)

Brahim Belaid¹, Lydia Lamara Mahammed¹, Ouardia Drali², Aida Mohand Oussaid³, Nabila Souad Touri⁴, Souhila Melzi⁵, Abdelhak Dehimi⁶, Lylia Meriem Berkani¹, Fatma Merah⁷, Zineb Larab⁷, Ines Allam¹, Ouarda Khemici⁸, Sonya Yasmine Kirane⁹, Mounia Boutaba¹⁰, Reda Belbouab¹¹, Hadjira Bekkakcha¹⁰, Assia Guedouar¹⁰, Abdelhakim Chelali¹², Brahim Baamara¹², Djamila Noui¹³, Hadda Baaziz¹³, Radia Rezak¹⁴, Sidi Mohamed Azzouz¹⁵, Malika Aichaoui¹⁶, Assia Moktefi¹⁶, Redha Mohamed Benhatchi¹⁶, Meriem Oussalah¹⁷, Naila Benaissa¹⁸, Amel Laredj¹⁸, Assia Bouchetara¹⁸, Abdelkader Adria¹⁹, Brahim Habireche²⁰, Noureddine Tounsi²⁰, Fella Dahmoun²¹, Rabah Touati²¹, Hamza Boucenna³, Fadila Bouferoua³, Lynda Sekfali³, Nadjet Bouhafs⁵, Rawda Aboura⁵, Sakina Kherra¹⁰, Yacine Inouri²², Saadeddine Dib²³, Nawel Medouri²⁴, Noureddine Khelfaoui²⁴, Aicha Redjedal²⁴, Amara Zelaci²⁵, Samah Yahiaoui²⁶, Sihem Medjadj²⁷, Tahar Khelifi Touhami²⁸, Ahmed Kadi²⁹, Fouzia Amireche³⁰, Imane Frada³¹, Shahrazed Houasnia³², Karima Benarab³³, Chahynez Boubidi¹⁰, Yacine Ferhani¹¹, Hayet Benalioua¹¹, Samia Sokhal¹¹, Nadia Benamar³⁴, Samira Aggoune³⁵, Karima Hadji³⁶, Asma Bellouti³⁷, Hakim Rahmoune⁶, Nada Boutrid⁶, Kamelia Okka⁶, Assia Ammour³⁸, Houssem Saadoune³⁹, Malika Amroun²², Hayet Belhadj²², Amina Ghanem⁴⁰, Hanane Abbaz⁴⁰, Sana Boudrioua⁴¹, Besma Zebiche⁴², Assia Ayad⁴², Zahra Hamadache⁴², Nassima Ouaras⁴³, Nassima Achour⁴³, Nadira Bouchair⁴⁴, Houda Boudiaf⁴⁵, Dahila Bekkat-Berkani⁴⁶, Hachemi Maouche³⁵, Zahir Bouzrar⁵, Lynda Aissat⁴⁷, Ouardia Ibsaine⁴⁸, Belkacem Bioud⁶, Leila Kedji⁴, Djazia Dahlouk²², Manoubia Bensmina⁴⁹, Abdelkarim Radoui¹⁷, Mimouna Bessahraoui¹⁵, Nadia Bensaadi³³, Azzeddine Mekki², Zoulikha Zeroual¹⁰, Koon-Wing Chan⁵⁰, Daniel Leung⁵⁰, Amar Tebaibia⁵¹, Soraya Ayoub⁵², Dalila Mekideche⁵³, Merzak Gharnaout²⁹, Jean Laurent Casanova^{54

55

56

57}, Anne Puel^{54

55

56}, Yu Lung Lau⁵⁰, Nacira Cherif⁹, Samir Ladj⁵⁸, Leila Smati⁴⁶, Rachida Boukari¹¹, Nafissa Benhalla³, Reda Djidjik¹

Affiliations

¹ Department of Medical Immunology, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
² Department of Pediatrics B, Hussein Dey University Hospital Center, University of Algiers 1, Algiers, Algeria.
³ Department of Pediatrics A, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁴ Department of Pediatrics, Blida University Hospital Center, University of Blida, Blida, Algeria.
⁵ Department of Pediatrics, Bab El Oued University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁶ Department of Pediatrics, Setif University Hospital Center, University of Setif 1, Setif, Algeria.
⁷ Department of Medical Immunology, Beni Messous University Hospital Center, Algiers, Algeria.
⁸ Department of Pediatrics B, Beni Messous University Hospital Center, Algiers, Algeria.
⁹ Department of Pediatrics B, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
¹⁰ Department of Pediatrics A, Hussein Dey University Hospital Center, University of Algiers 1, Algiers, Algeria.
¹¹ Department of Pediatrics, Mustapha Pacha University Hospital Center, University of Algiers 1, Algiers, Algeria.
¹² Department of Pediatrics, Djelfa Public Hospital Institution, Djelfa, Algeria.
¹³ Department of Pediatrics, Batna University Hospital center, University of Batna, Batna, Algeria.
¹⁴ Department of Pediatric Gastroenterology and Nutrition, Canastel Children's Hospital, Oran, Algeria.
¹⁵ Department of Pediatric Gastroenterology and Nutrition, Canastel Children's Hospital, University of Oran, Oran, Algeria.
¹⁶ Department of Pediatric Pneumo-Allergology, Canastel Children's Hospital, Oran, Algeria.
¹⁷ Department of Pediatric Pneumo-Allergology, Canastel Children's Hospital, University of Oran, Oran, Algeria.
¹⁸ Department of Children's Infectious Diseases, Canastel Children's Hospital, University of Oran, Oran, Algeria.
¹⁹ Department of Pediatric Hematology, Canastel Children's Hospital, Oran, Algeria.
²⁰ Department of Pediatrics, El Bayadh Public Hospital Institution, EL Bayadh, Algeria.
²¹ Department of Pediatrics, Bejaia University Hospital Center, University of Bejaia, Bejaia, Algeria.
²² Department of Pediatrics, Central Hospital of the Army, University of Algiers 1, Algiers, Algeria.
²³ Department of Pediatrics, Mother & Child Hospital of Tlemcen, University of Tlemcen, Tlemcen, Algeria.
²⁴ Department of Pediatrics, Saida Public Hospital Institution, Saida, Algeria.
²⁵ Department of Pediatrics, El Oued Public Hospital Institution, El Oued, Algeria.
²⁶ Department of Pediatrics, Barika Public Hospital Institution, Batna, Algeria.
²⁷ Department of Pediatrics, Ghardaia Public Hospital Institution, Ghardaia, Algeria.
²⁸ Private Practitioner, Constantine, Algeria.
²⁹ Department of Pneumology A, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
³⁰ Department of Pediatrics, Mother & Child Hospital of EL Mansourah, University of Constantine 3, Constantine, Algeria.
³¹ Department of Pediatrics, Biskra Public Hospital Institution, Biskra, Algeria.
³² Department of Pediatrics, El Harrouche Public Hospital Institution, Skikda, Algeria.
³³ Department of Pediatrics, Tizi Ouzou University Hospital Center, University of Tizi Ouzou, Tizi Ouzou, Algeria.
³⁴ Department of Pediatrics, Tighennif Public Hospital Institution, Mascara, Algeria.
³⁵ Department of Pediatrics, El-Harrach Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
³⁶ Department of Pediatrics, Ain Oulmene Public Hospital Institution, Setif, Algeria.
³⁷ Department of Pediatrics, Ain Azel Public Hospital Institution, Setif, Algeria.
³⁸ Department of Pediatrics, Mother & Child Hospital of Touggourt, Touggourt, Algeria.
³⁹ Department of Pneumology, Mila Public Hospital Institution, Mila, Algeria.
⁴⁰ Department of Pediatrics, Khenchela Public Hospital Institution, Khenchela, Algeria.
⁴¹ Department of Pediatrics, El Khroub Public Hospital Institution, Constantine, Algeria.
⁴² Department of Pediatrics, Kolea Public Hospital Institution, Tipaza, Algeria.
⁴³ Department of Infectious Diseases, EL Kettar Specialized Hospital, University of Algiers 1, Algiers, Algeria.
⁴⁴ Department of Pediatrics, Annaba University Hospital Center, University of Annaba, Annaba, Algeria.
⁴⁵ Department of Pediatric Oncology, Mustapha pacha University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁴⁶ Department of Pediatrics, Bologhine Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
⁴⁷ Department of Pediatrics, Mother & Child Hospital of Tipaza, University of Blida, Algiers, Algeria.
⁴⁸ Department of Pediatrics, Ain Taya Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
⁴⁹ Department of Pediatrics B, Douera University Hospital Center, University of Blida, Algiers, Algeria.
⁵⁰ Department of Pediatrics and Adolescent Medicine, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, Hong Kong SAR, China.
⁵¹ Department of Internal Medicine, El Biar Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
⁵² Department of Internal Medicine, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁵³ Department of Pneumology B, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁵⁴ Laboratory of Human Genetics of Infectious Diseases, Necker Hospital for Sick Children, INSERM UMR 1163, Paris, France.
⁵⁵ Imagine Institute, University of Paris, Paris, France.
⁵⁶ St Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller University, New York, NY, United States.
⁵⁷ Howard Hughes Medical Institute, New York, NY, United States.
⁵⁸ Department of Pediatrics, El Biar Public Hospital Institution, University of Algiers 1, Algiers, Algeria.

PMID: 35529857
PMCID: PMC9069527
DOI: 10.3389/fimmu.2022.900091

Inborn Errors of Immunity in Algerian Children and Adults: A Single-Center Experience Over a Period of 13 Years (2008-2021)

Brahim Belaid et al. Front Immunol. 2022.

. 2022 Apr 21:13:900091.

doi: 10.3389/fimmu.2022.900091. eCollection 2022.

Authors

Affiliations

¹ Department of Medical Immunology, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
² Department of Pediatrics B, Hussein Dey University Hospital Center, University of Algiers 1, Algiers, Algeria.
³ Department of Pediatrics A, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁴ Department of Pediatrics, Blida University Hospital Center, University of Blida, Blida, Algeria.
⁵ Department of Pediatrics, Bab El Oued University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁶ Department of Pediatrics, Setif University Hospital Center, University of Setif 1, Setif, Algeria.
⁷ Department of Medical Immunology, Beni Messous University Hospital Center, Algiers, Algeria.
⁸ Department of Pediatrics B, Beni Messous University Hospital Center, Algiers, Algeria.
⁹ Department of Pediatrics B, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
¹⁰ Department of Pediatrics A, Hussein Dey University Hospital Center, University of Algiers 1, Algiers, Algeria.
¹¹ Department of Pediatrics, Mustapha Pacha University Hospital Center, University of Algiers 1, Algiers, Algeria.
¹² Department of Pediatrics, Djelfa Public Hospital Institution, Djelfa, Algeria.
¹³ Department of Pediatrics, Batna University Hospital center, University of Batna, Batna, Algeria.
¹⁴ Department of Pediatric Gastroenterology and Nutrition, Canastel Children's Hospital, Oran, Algeria.
¹⁵ Department of Pediatric Gastroenterology and Nutrition, Canastel Children's Hospital, University of Oran, Oran, Algeria.
¹⁶ Department of Pediatric Pneumo-Allergology, Canastel Children's Hospital, Oran, Algeria.
¹⁷ Department of Pediatric Pneumo-Allergology, Canastel Children's Hospital, University of Oran, Oran, Algeria.
¹⁸ Department of Children's Infectious Diseases, Canastel Children's Hospital, University of Oran, Oran, Algeria.
¹⁹ Department of Pediatric Hematology, Canastel Children's Hospital, Oran, Algeria.
²⁰ Department of Pediatrics, El Bayadh Public Hospital Institution, EL Bayadh, Algeria.
²¹ Department of Pediatrics, Bejaia University Hospital Center, University of Bejaia, Bejaia, Algeria.
²² Department of Pediatrics, Central Hospital of the Army, University of Algiers 1, Algiers, Algeria.
²³ Department of Pediatrics, Mother & Child Hospital of Tlemcen, University of Tlemcen, Tlemcen, Algeria.
²⁴ Department of Pediatrics, Saida Public Hospital Institution, Saida, Algeria.
²⁵ Department of Pediatrics, El Oued Public Hospital Institution, El Oued, Algeria.
²⁶ Department of Pediatrics, Barika Public Hospital Institution, Batna, Algeria.
²⁷ Department of Pediatrics, Ghardaia Public Hospital Institution, Ghardaia, Algeria.
²⁸ Private Practitioner, Constantine, Algeria.
²⁹ Department of Pneumology A, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
³⁰ Department of Pediatrics, Mother & Child Hospital of EL Mansourah, University of Constantine 3, Constantine, Algeria.
³¹ Department of Pediatrics, Biskra Public Hospital Institution, Biskra, Algeria.
³² Department of Pediatrics, El Harrouche Public Hospital Institution, Skikda, Algeria.
³³ Department of Pediatrics, Tizi Ouzou University Hospital Center, University of Tizi Ouzou, Tizi Ouzou, Algeria.
³⁴ Department of Pediatrics, Tighennif Public Hospital Institution, Mascara, Algeria.
³⁵ Department of Pediatrics, El-Harrach Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
³⁶ Department of Pediatrics, Ain Oulmene Public Hospital Institution, Setif, Algeria.
³⁷ Department of Pediatrics, Ain Azel Public Hospital Institution, Setif, Algeria.
³⁸ Department of Pediatrics, Mother & Child Hospital of Touggourt, Touggourt, Algeria.
³⁹ Department of Pneumology, Mila Public Hospital Institution, Mila, Algeria.
⁴⁰ Department of Pediatrics, Khenchela Public Hospital Institution, Khenchela, Algeria.
⁴¹ Department of Pediatrics, El Khroub Public Hospital Institution, Constantine, Algeria.
⁴² Department of Pediatrics, Kolea Public Hospital Institution, Tipaza, Algeria.
⁴³ Department of Infectious Diseases, EL Kettar Specialized Hospital, University of Algiers 1, Algiers, Algeria.
⁴⁴ Department of Pediatrics, Annaba University Hospital Center, University of Annaba, Annaba, Algeria.
⁴⁵ Department of Pediatric Oncology, Mustapha pacha University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁴⁶ Department of Pediatrics, Bologhine Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
⁴⁷ Department of Pediatrics, Mother & Child Hospital of Tipaza, University of Blida, Algiers, Algeria.
⁴⁸ Department of Pediatrics, Ain Taya Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
⁴⁹ Department of Pediatrics B, Douera University Hospital Center, University of Blida, Algiers, Algeria.
⁵⁰ Department of Pediatrics and Adolescent Medicine, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, Hong Kong SAR, China.
⁵¹ Department of Internal Medicine, El Biar Public Hospital Institution, University of Algiers 1, Algiers, Algeria.
⁵² Department of Internal Medicine, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁵³ Department of Pneumology B, Beni Messous University Hospital Center, University of Algiers 1, Algiers, Algeria.
⁵⁴ Laboratory of Human Genetics of Infectious Diseases, Necker Hospital for Sick Children, INSERM UMR 1163, Paris, France.
⁵⁵ Imagine Institute, University of Paris, Paris, France.
⁵⁶ St Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller University, New York, NY, United States.
⁵⁷ Howard Hughes Medical Institute, New York, NY, United States.
⁵⁸ Department of Pediatrics, El Biar Public Hospital Institution, University of Algiers 1, Algiers, Algeria.

PMID: 35529857
PMCID: PMC9069527
DOI: 10.3389/fimmu.2022.900091

Abstract

Background: Inborn errors of immunity (IEI) predispose patients to various infectious and non-infectious complications. Thanks to the development and expanding use of flow cytometry and increased awareness, the diagnostic rate of IEI has markedly increased in Algeria the last decade.

Aim: This study aimed to describe a large cohort of Algerian patients with probable IEI and to determine their clinical characteristics and outcomes.

Methods: We collected and analyzed retrospectively the demographic data, clinical manifestations, immunologic, genetic data, and outcome of Algerian IEI patients - diagnosed in the department of medical immunology of Beni Messous university hospital center, Algiers, from 2008 to 2021.

Results: Eight hundred and seven patients with IEI (482 males and 325 females) were enrolled, 9.7% of whom were adults. Consanguinity was reported in 50.3% of the cases and a positive family history in 32.34%. The medium age at disease onset was 8 months and at diagnosis was 36 months. The median delay in diagnosis was 16 months. Combined immunodeficiencies were the most frequent (33.8%), followed by antibody deficiencies (24.5%) and well-defined syndromes with immunodeficiency (24%). Among 287 patients tested for genetic disorders, 129 patients carried pathogenic mutations; 102 having biallelic variants mostly in a homozygous state (autosomal recessive disorders). The highest mortality rate was observed in patients with combined immunodeficiency (70.1%), especially in patients with severe combined immunodeficiency (SCID), Omenn syndrome, or Major Histocompatibility Complex (MHC) class II deficiency.

Conclusion: The spectrum of IEI in Algeria is similar to that seen in most countries of the Middle East and North Africa (MENA) region, notably regarding the frequency of autosomal recessive and/or combined immunodeficiencies.

Keywords: Algeria; clinical features; diagnosis; epidemiology; inborn errors of immunity; molecular diagnosis; primary immunodeficiency.

Copyright © 2022 Belaid, Lamara Mahammed, Drali, Oussaid, Touri, Melzi, Dehimi, Berkani, Merah, Larab, Allam, Khemici, Kirane, Boutaba, Belbouab, Bekkakcha, Guedouar, Chelali, Baamara, Noui, Baaziz, Rezak, Azzouz, Aichaoui, Moktefi, Benhatchi, Oussalah, Benaissa, Laredj, Bouchetara, Adria, Habireche, Tounsi, Dahmoun, Touati, Boucenna, Bouferoua, Sekfali, Bouhafs, Aboura, Kherra, Inouri, Dib, Medouri, Khelfaoui, Redjedal, Zelaci, Yahiaoui, Medjadj, Touhami, Kadi, Amireche, Frada, Houasnia, Benarab, Boubidi, Ferhani, Benalioua, Sokhal, Benamar, Aggoune, Hadji, Bellouti, Rahmoune, Boutrid, Okka, Ammour, Saadoune, Amroun, Belhadj, Ghanem, Abbaz, Boudrioua, Zebiche, Ayad, Hamadache, Ouaras, Achour, Bouchair, Boudiaf, Bekkat-Berkani, Maouche, Bouzrar, Aissat, Ibsaine, Bioud, Kedji, Dahlouk, Bensmina, Radoui, Bessahraoui, Bensaadi, Mekki, Zeroual, Chan, Leung, Tebaibia, Ayoub, Mekideche, Gharnaout, Casanova, Puel, Lau, Cherif, Ladj, Smati, Boukari, Benhalla and Djidjik.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

**Figure 1**
Distribution of the frequencies of IEIs according to IUIS categories in 807 Algerian patients in the study. IEI groups are shown according to IUIS classification, 2021. Total number of patients and percentage of all registered patients are shown for each group. AGAM, agammaglobulinemia; ALPS, autoimmune lymphoproliferative syndrome; AID, autoinflammatory diseases; A-T, ataxia- telangiectasia; c, classified; CD, complement deficiencies; CF, cystic fibrosis; CGD, chronic granulomatous disease; CID, combined immunodeficiencies; CVID, common variable immunodeficiency; DGS, DiGeorge syndrome, DID, Dysregulation of immune diseases; f-HLH, familial Hemophagocytic lymphohistiocytosis; GS, good syndrome; HIES, hyper-IgE syndrome; HIDS, hyper-IgD syndrome; IID, innate immune deficiencies; MSMD, mendelian susceptibility to mycobacterial disease; PAD, predominantly antibody deficiencies; PD, phagocytic deficiencies; SCN, severe congenital neutropenia; sIgA; selective IgA deficiency; SP, Somatic phenocopies; SynCID, syndromic combined immunodeficiencies; u, unclassified; WAS, Wiskott Aldrich syndrome; XLT, X linked thrombocytopenia.

**Figure 2**
Distribution of patients according to IEI diagnosis age groups and main IEI categories (N = 807).

**Figure 3**
The median age of disease onset and diagnostic delay in the main IEI categories. **(A)** Median age of disease onset. **(B)** Median of diagnostic delay.

**Figure 4**
Annual numbers of newly diagnosed IEI cases from 2008 to September 2021. The registration of patients into the database has been stopped in September for the year 2021.

**Figure 5**
distribution of patients in the different provinces of Algeria. The base map was created with the permission of data wrapper. The intensity of the blue color is proportional to the number of patients. The registered number includes living and deceased patients. Each number on the map corresponds to a province.

**Figure 6**
**(A)** Mortality rate by PID group and age of the deceased patients (n: 231). Colors represent different IEI categories. Numbers in the plots show the number of patients and the ratio of the deceased patients by IEI group to the total number of the deceased patients of the age-group; **(B)** Overall survival (Kaplan-Meier curve) of patients with IEI showing the probability of survival following diagnosis. **(C)** Kaplan-Meier curve showing overall survival in the 807 studied patients within the 9 categories of IEI. CID, combined immunodeficiencies; SyCID, syndromic combined immunodeficiencies; PAD, predominantly antibody deficiencies; DID, Dysregulation of immune diseases; PD, phagocytic disorders; CD, complement deficiencies; IID, innate immune deficiencies; AID, autoinflammatory diseases; SP, Somatic phenocopies.

**Figure 7**
Comparison of IEI death percentages in our cohort with previously published IEI studies of other countries. Algeria: green; European countries: red; Asian countries and regions: brown, north African countries: blue. Parentheses next to each country name correspond to number of patients followed by year of analysis (number of patients; year of analysis).

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Inborn Errors of Immunity in Algerian Children and Adults: A Single-Center Experience Over a Period of 13 Years (2008-2021)

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Inborn Errors of Immunity in Algerian Children and Adults: A Single-Center Experience Over a Period of 13 Years (2008-2021)

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