Skip to main content

Advertisement

SpringerLink
Log in

Clinical and Immunological Features, Genetic Variants, and Outcomes of Patients with CD40 Deficiency

  • Original Article
  • Published:
Journal of Clinical Immunology Aims and scope Submit manuscript

Abstract

Purpose

Inherited deficiencies of CD40 and CD40 ligand (CD40L) reflect the crucial immunological functions of CD40–CD40L interaction/signaling. Although numerous studies have provided a detailed description of CD40L deficiency, reports of CD40 deficiency are scarce. Herein, we describe the characteristics of all reported patients with CD40 deficiency.

Methods

The PubMed, Embase and Web of Science databases were searched for relevant literature published till 7th August 2023. Study deduplication and identification of relevant reports was performed using the online PICO Portal. The data were extracted using a pre-designed data extraction form and the SPSS software was used for analysis.

Results

Systematic literature review revealed 40 unique patients with CD40 deficiency. Respiratory tract and gastrointestinal infections were the predominant clinical manifestations (observed in 93% and 57% patients, respectively). Sclerosing cholangitis has been reported in nearly one-third of patients. Cryptosporidium sp. (29%) and Pneumocystis jirovecii (21%) were the most common microbes identified. Very low to undetectable IgG levels and severely reduced/absent switch memory B cells were observed in all patients tested/reported. Elevated IgM levels were observed in 69% patients. Overall, splice-site and missense variants were the most common (36% and 32%, respectively) molecular defects identified. All patients were managed with immunoglobulin replacement therapy and antimicrobial prophylaxis was utilized in a subset. Hematopoietic stem cell transplantation (HSCT) has been performed in 45% patients (curative outcome observed in 73% of these patients). Overall, a fatal outcome was reported in 21% patients.

Conclusions

We provide a comprehensive description of all important aspects of CD40 deficiency. HSCT is a promising curative treatment option for CD40 deficiency.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

Relevant data/methods utilized in the preparation of this manuscript are provided in the manuscript and electronic supplementary material. Additional data underlying this article will be shared on reasonable request to the corresponding author.

References

  1. van Kooten C, Banchereau J. Functions of CD40 on B cells, dendritic cells and other cells. Curr Opin Immunol. 1997;9(3):330–7. https://doi.org/10.1016/s0952-7915(97)80078-7.

    Article  PubMed  Google Scholar 

  2. Hollenbaugh D, Grosmaire LS, Kullas CD, Chalupny NJ, Braesch-Andersen S, Noelle RJ, et al. The human T cell antigen gp39, a member of the TNF gene family, is a ligand for the CD40 receptor: expression of a soluble form of gp39 with B cell co-stimulatory activity. EMBO J. 1992;11(12):4313–21. https://doi.org/10.1002/j.1460-2075.1992.tb05530.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Laman JD, Claassen E, Noelle RJ. Functions of CD40 and its ligand, gp39 (CD40L). Crit Rev Immunol. 2017;37(2–6):371–420. https://doi.org/10.1615/CritRevImmunol.v37.i2-6.100.

    Article  PubMed  Google Scholar 

  4. Ma DY, Clark EA. The role of CD40 and CD154/CD40L in dendritic cells. Semin Immunol. 2009;21(5):265–72. https://doi.org/10.1016/j.smim.2009.05.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Aruffo A, Farrington M, Hollenbaugh D, Li X, Milatovich A, Nonoyama S, et al. The CD40 ligand, gp39, is defective in activated T cells from patients with X-linked hyper-IgM syndrome. Cell. 1993;72(2):291–300. https://doi.org/10.1016/0092-8674(93)90668-g.

    Article  CAS  PubMed  Google Scholar 

  6. Tangye SG, Al-Herz W, Bousfiha A, Cunningham-Rundles C, Franco JL, Holland SM, et al. Human inborn errors of immunity: 2022 update on the classification from the International Union of Immunological Societies Expert Committee. J Clin Immunol. 2022;42(7):1473–507. https://doi.org/10.1007/s10875-022-01289-3.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Ferrari S, Giliani S, Insalaco A, Al-Ghonaium A, Soresina AR, Loubser M, et al. Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc Natl Acad Sci U S A. 2001;98(22):12614–9. https://doi.org/10.1073/pnas.221456898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. França TT, Barreiros LA, Al-Ramadi BK, Ochs HD, Cabral-Marques O, Condino-Neto A. CD40 ligand deficiency: treatment strategies and novel therapeutic perspectives. Expert Rev Clin Immunol. 2019;15(5):529–40. https://doi.org/10.1080/1744666X.2019.1573674.

    Article  PubMed  Google Scholar 

  9. Hirbod-Mobarakeh A, Aghamohammadi A, Rezaei N. Immunoglobulin class switch recombination deficiency type 1 or CD40 ligand deficiency: from bedside to bench and back again. Expert Rev Clin Immunol. 2014;10(1):91–105. https://doi.org/10.1586/1744666X.2014.864554.

    Article  CAS  PubMed  Google Scholar 

  10. Lougaris V, Badolato R, Ferrari S, Plebani A. Hyper immunoglobulin M syndrome due to CD40 deficiency: clinical, molecular, and immunological features. Immunol Rev. 2005;203:48–66. https://doi.org/10.1111/j.0105-2896.2005.00229.x.

    Article  CAS  PubMed  Google Scholar 

  11. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. https://doi.org/10.1136/bmj.n71.

    Article  PubMed  PubMed Central  Google Scholar 

  12. PICO Portal. Identifying duplicates with PICO Portal. 2022. Available from: https://picoportal.org/2022/02/01/identifying-duplicates-with-pico-portal/. Accessed 7 Aug 2023.

  13. Banday AZ, Jindal AK, Kaur A, Kumar Y, Nameirakpam J, Patra PK, Rawat A. A young girl with hypogammaglobulinemia and granulomatous hepatitis caused by a novel mutation in ZBTB24 gene: a case based analysis. Immunobiology. 2020;225(3):151912. https://doi.org/10.1016/j.imbio.2020.151912.

    Article  CAS  PubMed  Google Scholar 

  14. Kutukculer N, Moratto D, Aydinok Y, Lougaris V, Aksoylar S, Plebani A, et al. Disseminated cryptosporidium infection in an infant with hyper-IgM syndrome caused by CD40 deficiency. J Pediatr. 2003;142(2):194–6. https://doi.org/10.1067/mpd.2003.41.

    Article  PubMed  Google Scholar 

  15. Mazzolari E, Lanzi G, Forino C, Lanfranchi A, Aksu G, Ozturk C, et al. First report of successful stem cell transplantation in a child with CD40 deficiency. Bone Marrow Transplant. 2007;40(3):279–81. https://doi.org/10.1038/sj.bmt.1705713.

    Article  CAS  PubMed  Google Scholar 

  16. Karaca NE, Forveille M, Aksu G, Durandy A, Kutukculer N. Hyper-immunoglobulin M syndrome type 3 with normal CD40 cell surface expression. Scand J Immunol. 2012;76(1):21–5. https://doi.org/10.1111/j.1365-3083.2012.02697.x.

    Article  CAS  PubMed  Google Scholar 

  17. Al-Saud BK, Al-Sum Z, Alassiri H, Al-Ghonaium A, Al-Muhsen S, Al-Dhekri H, et al. Clinical, immunological, and molecular characterization of hyper-IgM syndrome due to CD40 deficiency in eleven patients. J Clin Immunol. 2013;33(8):1325–35. https://doi.org/10.1007/s10875-013-9951-9.

    Article  CAS  PubMed  Google Scholar 

  18. Mishra A, Italia K, Gupta M, Desai M, Madkaikar M. Hyperimmunoglobulin syndrome due to CD40 deficiency: possibly the first case from India. J Postgrad Med. 2015;61(1):46–8. https://doi.org/10.4103/0022-3859.147053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Murguia-Favela L, Sharfe N, Karanxha A, Bates A, Dadi H, Cimpean L, Roifman CM. CD40 deficiency: a unique adult patient with hyper immunoglobulin M syndrome and normal expression of CD40. LymphoSign J. 2017;4(2):70–6. https://doi.org/10.14785/lymphosign-2017-0004.

    Article  Google Scholar 

  20. Bahrami A, Soltani Z, Fazlollahi MR, Rahmani F, Houshmand M, Mazinani M, Rezaei N. Adenoid hyperplasia in a patient with a rare type of hyper immunoglobulin M syndrome due to CD40 deficiency. Acta Med Iran. 2018:811–4. Available from: https://acta.tums.ac.ir/index.php/acta/article/download/7252/5201/. Accessed 30 Nov 2022.

  21. Al-Saud B, Al-Jomaie M, Al-Ghonaium A, Al-Ahmari A, Al-Mousa H, Al-Muhsen S, et al. Haematopoietic stem cell transplant for hyper-IgM syndrome due to CD40 defects: a single-centre experience. Bone Marrow Transplant. 2019;54(1):63–7. https://doi.org/10.1038/s41409-018-0219-0.

    Article  CAS  PubMed  Google Scholar 

  22. Renner ED, Krätz CE, Orange JS, Hagl B, Rylaarsdam S, Notheis G, et al. Class switch recombination defects: impact on B cell maturation and antibody responses. Clin Immunol. 2021;222:108638. https://doi.org/10.1016/j.clim.2020.108638.

    Article  CAS  PubMed  Google Scholar 

  23. Akarsu A, Halaçlı S, Tan Ç, Kuşkonmaz B, Küpesiz A, Çetinkaya D, et al. A single-center study points to diverse features and outcome in patients with hyperimmunoglobulin M syndrome and class‐switch recombination defects. Scand J Immunol. 2022;96(5):e13213. https://doi.org/10.1111/sji.13213.

    Article  CAS  PubMed  Google Scholar 

  24. Rawat A, Sharma M, Vignesh P, Jindal AK, Suri D, Das J, et al. Utility of targeted next generation sequencing for inborn errors of immunity at a tertiary care centre in North India. Sci Rep. 2022;12(1):10416. https://doi.org/10.1038/s41598-022-14522-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hsu J, Massaad M, Notarangelo LD. Successful hematopoietic stem cell transplant for CD40 deficiency manifesting as hyper-IgM syndrome with absent CD40 expression and marked lymphocytosis. J Allergy Clin Immunol. 2014;133(2):AB95. https://doi.org/10.1016/j.jaci.2013.12.354.

    Article  Google Scholar 

  26. Leven EA, Maffucci P, Ochs HD, Scholl PR, Buckley RH, Fuleihan RL, et al. Hyper IgM syndrome: a report from the USIDNET Registry. J Clin Immunol. 2016;36(5):490–501. https://doi.org/10.1007/s10875-016-0291-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Galal N, Meshaal S, Elhawary R, ElAziz DA, Alkady R, Lotfy S, et al. Patterns of primary immunodeficiency disorders among a highly consanguineous population: Cairo University Pediatric Hospital’s 5-year experience. J Clin Immunol. 2016;36(7):649–55. https://doi.org/10.1007/s10875-016-0314-1.

    Article  CAS  PubMed  Google Scholar 

  28. Barbouche MR, Mekki N, Ben-Ali M, Ben-Mustapha I. Lessons from genetic studies of primary immunodeficiencies in a highly consanguineous population. Front Immunol. 2017;8:737. https://doi.org/10.3389/fimmu.2017.00737.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fioredda F, Pierri F, Palmisani E, Finocchi A, Di Matteo G, Palumbo G, et al. Severe chronic neutropenia: primary immunodeficiency mutations are frequent causative agents. Blood. 2018;132(S1):2402. https://doi.org/10.1182/blood-2018-99-114462.

    Article  Google Scholar 

  30. El-Helou SM, Biegner AK, Bode S, Ehl SR, Heeg M, Maccari ME, et al. The German National Registry of primary immunodeficiencies (2012–2017). Front Immunol. 2019;10:1272. https://doi.org/10.3389/fimmu.2019.01272.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Linares NA, Bouchard M, Gutiérrez NS, Colmenares M, Cantor-Garcia A, Gabaldon-Figueira JC, et al. Immunological features in pediatric patients with recurrent and severe infection: identification of primary immunodeficiency diseases in Merida, Venezuela. Allergol Immunopathol (Madr). 2019;47(5):437–48. https://doi.org/10.1016/j.aller.2019.02.002.

    Article  CAS  PubMed  Google Scholar 

  32. Belaid B, Lamara Mahammed L, Drali O, Oussaid AM, Touri NS, Melzi S, et al. Inborn errors of immunity in Algerian children and adults: a single-center experience over a period of 13 years (2008–2021). Front Immunol. 2022;13:900091. https://doi.org/10.3389/fimmu.2022.900091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Vonniessen N, Ahmed E, Hazzazi K, Mourad W, Mazer B. Profiling B-cell response: Hyperimmunoglobulin M syndrome due to CD40 deficiency. J Allergy Clin Immunol. 2023;151(2):AB334. https://doi.org/10.1016/j.jaci.2022.12.774.

    Article  Google Scholar 

  34. Fontana S, Moratto D, Mangal S, De Francesco M, Vermi W, Ferrari S, et al. Functional defects of dendritic cells in patients with CD40 deficiency. Blood. 2003;102(12):4099–106. https://doi.org/10.1182/blood-2003-04-1244.

    Article  CAS  PubMed  Google Scholar 

  35. Lanzi G, Ferrari S, Vihinen M, Caraffi S, Kutukculer N, Schiaffonati L, et al. Different molecular behavior of CD40 mutants causing hyper-IgM syndrome. Blood. 2010;116(26):5867–74. https://doi.org/10.1182/blood-2010-03-274241.

    Article  CAS  PubMed  Google Scholar 

  36. Cicalese MP, Gerosa J, Baronio M, Montin D, Licciardi F, Soresina A, et al. Circulating follicular helper and follicular regulatory T cells are severely compromised in human CD40 deficiency: a case report. Front Immunol. 2018;9:1761. https://doi.org/10.3389/fimmu.2018.01761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kutukculer N, Aksoylar S, Kansoy S, Cetingul N, Notarangelo LD. Outcome of hematopoietic stem cell transplantation in hyper-IgM syndrome caused by CD40 deficiency. J Pediatr. 2003;143(1):141–2. https://doi.org/10.1016/S0022-3476(03)00274-9.

    Article  PubMed  Google Scholar 

  38. Dirim D, Dagci H, Turgay N. Disseminated cryptosporidiosis in Turkey: case report. East Afr Med J. 2003;80(10):550–2. https://doi.org/10.4314/eamj.v80i10.8760.

    Article  CAS  PubMed  Google Scholar 

  39. Al-Dhekri H, Al-Sum Z, Al-Saud B, Al-Mousa H, Ayas M, Al-Muhsen S, et al. Successful outcome in two patients with CD40 deficiency treated with allogeneic HCST. Clin Immunol. 2012;143(1):96–8. https://doi.org/10.1016/j.clim.2012.01.012.

    Article  CAS  PubMed  Google Scholar 

  40. Wintergerst U, Durandy A, Belohradsky BH. Clinical course of a female patient with CD40-deficiency. Clin Exp Immunol. 2008;154(S1):186.

    Google Scholar 

  41. Cella M, Sallusto F, Lanzavecchia A. Origin, maturation and antigen presenting function of dendritic cells. Curr Opin Immunol. 1997;9(1):10–6. https://doi.org/10.1016/s0952-7915(97)80153-7.

    Article  CAS  PubMed  Google Scholar 

  42. Mehta HM, Corey SJ. G-CSF, the guardian of granulopoiesis. Semin Immunol. 2021;54:101515. https://doi.org/10.1016/j.smim.2021.101515.

    Article  CAS  PubMed  Google Scholar 

  43. Mavroudi I, Papadaki V, Pyrovolaki K, Katonis P, Eliopoulos AG, Papadaki HA. The CD40/CD40 ligand interactions exert pleiotropic effects on bone marrow granulopoiesis. J Leukoc Biol. 2011;89(5):771–83. https://doi.org/10.1189/jlb.0610330.

    Article  CAS  PubMed  Google Scholar 

  44. Solanilla A, Déchanet J, El Andaloussi A, Dupouy M, Godard F, Chabrol J, et al. CD40-ligand stimulates myelopoiesis by regulating flt3-ligand and thrombopoietin production in bone marrow stromal cells. Blood. 2000;95(12):3758–64.

    Article  CAS  PubMed  Google Scholar 

  45. Pollheimer MJ, Halilbasic E, Fickert P, Trauner M. Pathogenesis of primary sclerosing cholangitis. Best Pract Res Clin Gastroenterol. 2011;25(6):727–39. https://doi.org/10.1016/j.bpg.2011.10.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Stephens J, Cosyns M, Jones M, Hayward A. Liver and bile duct pathology following Cryptosporidium parvum Infection of immunodeficient mice. Hepatology. 1999;30(1):27–35. https://doi.org/10.1002/hep.510300138.

    Article  CAS  PubMed  Google Scholar 

  47. Ungar BL, Burris JA, Quinn CA, Finkelman FD. New mouse models for chronic Cryptosporidium Infection in immunodeficient hosts. Infect Immun. 1990;58(4):961–9. https://doi.org/10.1128/iai.58.4.961-969.1990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ponnuraj EM, Hayward AR. Requirement for TNF-Tnfrsf1 signalling for sclerosing cholangitis in mice chronically infected by Cryptosporidium parvum. Clin Exp Immunol. 2002;128(3):416–20. https://doi.org/10.1046/j.1365-2249.2002.01861.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Pollheimer MJ, Fickert P. Animal models in primary biliary Cirrhosis and primary sclerosing cholangitis. Clin Rev Allergy Immunol. 2015;48(2–3):207–17. https://doi.org/10.1007/s12016-014-8442-y.

    Article  PubMed  Google Scholar 

  50. Levy J, Espanol-Boren T, Thomas C, Fischer A, Tovo P, Bordigoni P, et al. Clinical spectrum of X-linked hyper-IgM syndrome. J Pediatr. 1997;131(1 Pt 1):47–54. https://doi.org/10.1016/s0022-3476(97)70123-9.

    Article  CAS  PubMed  Google Scholar 

  51. Winkelstein JA, Marino MC, Ochs H, Fuleihan R, Scholl PR, Geha R, et al. The X-linked hyper-IgM syndrome: clinical and immunologic features of 79 patients. Medicine (Baltim). 2003;82(6):373–84. https://doi.org/10.1097/01.md.0000100046.06009.b0.

    Article  CAS  Google Scholar 

  52. Du X, Tang W, Chen X, Zeng T, Wang Y, Chen Z, et al. Clinical, genetic and immunological characteristics of 40 Chinese patients with CD40 ligand deficiency. Scand J Immunol. 2019;90(4):e12798. https://doi.org/10.1111/sji.12798.

    Article  PubMed  Google Scholar 

  53. Mitsui-Sekinaka K, Imai K, Sato H, Tomizawa D, Kajiwara M, Nagasawa M, et al. Clinical features and hematopoietic stem cell transplantations for CD40 ligand deficiency in Japan. J Allergy Clin Immunol. 2015;136(4):1018–24. https://doi.org/10.1016/j.jaci.2015.02.020.

    Article  PubMed  Google Scholar 

  54. Khalil IA, Troeger C, Rao PC, Blacker BF, Brown A, Brewer TG, et al. Morbidity, mortality, and long-term consequences associated with Diarrhoea from Cryptosporidium Infection in children younger than 5 years: a meta-analyses study. Lancet Glob Health. 2018;6(7):e758-68. https://doi.org/10.1016/S2214-109X(18)30283-3.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Hijjawi N, Zahedi A, Al-Falah M, Ryan U. A review of the molecular epidemiology of Cryptosporidium spp. and Giardia Duodenalis in the Middle East and North Africa (MENA) region. Infect Genet Evol. 2022;98:105212. https://doi.org/10.1016/j.meegid.2022.105212.

    Article  CAS  PubMed  Google Scholar 

  56. Aloui C, Prigent A, Sut C, Tariket S, Hamzeh-Cognasse H, Pozzetto B, et al. The signaling role of CD40 ligand in platelet biology and in platelet component transfusion. Int J Mol Sci. 2014;15(12):22342–64. https://doi.org/10.3390/ijms151222342.

    Article  CAS  PubMed  Google Scholar 

  57. de la Morena MT, Leonard D, Torgerson TR, Cabral-Marques O, Slatter M, Aghamohammadi A, et al. Long-term outcomes of 176 patients with X-linked hyper-IgM syndrome treated with or without hematopoietic cell transplantation. J Allergy Clin Immunol. 2017;139(4):1282–92. https://doi.org/10.1016/j.jaci.2016.07.039.

    Article  CAS  PubMed  Google Scholar 

  58. Modell V, Knaus M, Modell F, Roifman C, Orange J, Notarangelo LD. Global overview of primary immunodeficiencies: a report from Jeffrey Modell Centers worldwide focused on diagnosis, treatment, and discovery. Immunol Res. 2014;60(1):132–44. https://doi.org/10.1007/s12026-014-8498-z.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

LDN is supported by the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, Bethesda, MD, USA.

Funding

None.

Author information

Authors and Affiliations

  1. Department of Pediatrics, Government Medical College (GMC), Srinagar, India

    Aaqib Zaffar Banday & Syed Tariq Ahmed Bukhari

  2. Clinical Immunology & Rheumatology Division, Department of Pediatrics, Khyber Medical Institute, Srinagar, India

    Aaqib Zaffar Banday

  3. Rheumatology Division, Kashmir Clinics Group, Srinagar, India

    Aaqib Zaffar Banday

  4. Department of Microbiology, Government Medical College (GMC), Baramulla, India

    Rahila Nisar

  5. Department of Pediatrics, All India Institute of Medical Sciences (AIIMS), Patna, 801507, India

    Pratap Kumar Patra

  6. Department of Translational & Regenerative Medicine, Post Graduate Institute of Medical Education and Research (PGIMER), Chandigarh, India

    Anit Kaur

  7. Division of Genetics, Department of Pediatrics, All India Institute of Medical Sciences (AIIMS), New Delhi, India

    Rohit Sadanand

  8. Suma Genomics, Manipal, India

    Chakshu Chaudhry

  9. Department of Pediatrics, Maharishi Markandeshwar College of Medical Sciences and Research, Ambala, India

    Chakshu Chaudhry

  10. Department of Medical-Hematoncology and Stem Cell Transplant, Paras Hospital, Srinagar, India

    Saquib Zaffar Banday

  11. Advanced Center for Immunology and Rheumatology, Kathmandu, Nepal

    Dharmagat Bhattarai

  12. Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, 20892, USA

    Luigi D. Notarangelo

Authors
  1. Aaqib Zaffar Banday
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rahila Nisar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pratap Kumar Patra
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anit Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rohit Sadanand
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chakshu Chaudhry
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Syed Tariq Ahmed Bukhari
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Saquib Zaffar Banday
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dharmagat Bhattarai
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Luigi D. Notarangelo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AZB, RN: Conception of idea and design of the study; literature review; acquisition, analysis, and interpretation of data; and drafted, edited, and revised the manuscript.

PKP, AK, RS, CC, STAB, SZB: Editing and revision of the manuscript; acquisition, analysis, and interpretation of data; and literature review.

DB, LDN: Editing and critical revision of the manuscript; interpretation of data; literature review; and overall supervision of manuscript preparation.

All authors approve the final version of the manuscript.

Corresponding author

Correspondence to Pratap Kumar Patra.

Ethics declarations

Ethics Approval

As this study pertains to literature review and analysis of previously published data, ethics approval and consent is not mandated.

Consent to Participate and Consent for Publication

Not applicable.

Conflict of Interest or Competing Interests

None.

Note

All figures provided in this article are original and have not been published elsewhere. Multiple affiliations of the first author (AZB) are sequential affiliations that have changed during the course of the work.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Aaqib Zaffar Banday and Rahila Nisar contributed equally and qualify as joint first authors.

Supplementary Information

Below is the link to the electronic supplementary material.

ESM 1

(PDF 270 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Banday, A.Z., Nisar, R., Patra, P.K. et al. Clinical and Immunological Features, Genetic Variants, and Outcomes of Patients with CD40 Deficiency. J Clin Immunol 44, 17 (2024). https://doi.org/10.1007/s10875-023-01633-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10875-023-01633-1

Keywords

Search

Navigation