Clinical, immunologic, and genetic spectrum of 696 patients with combined immunodeficiency

Journal of Allergy and Clinical Immunology

Volumn 141, Issue 4, 2018, Pages 1450-1458

  Abolhassani, Hassan ^a,b   Chou, Janet ^c   Bainter, Wayne ^c   Platt, Craig D ^c   Tavassoli, Mahmood ^d   Momen, Tooba ^d   Tavakol, Marzieh ^e   Eslamian, Mohammad Hossein ^f   Gharagozlou, Mohammad ^g   Movahedi, Masoud ^g   Ghadami, Mohsen ^a   Hamidieh, Amir Ali ^h   Azizi, Gholamreza ⁱ   Yazdani, Reza ^a,j   Afarideh, Mohsen ^a   Ghajar, Alireza ^a   Havaei, Arash ^a   Chavoshzadeh, Zahra ^k   Mahdaviani, Seyed Alireza ^l   Cheraghi, Taher ^m   Behniafard, Nasrin ⁿ   Amin, Reza ^o   Aleyasin, Soheila ^o   Faridhosseini, Reza ^p   Jabbari Azad, Farahzad ^p   Nabavi, Mohammamd ^q   Bemanian, Mohammad Hassan ^q   Arshi, Saba ^q   Molatefi, Rasol ^q,r   Sherkat, Roya ^s   Mansouri, Mahboubeh ^k   Mesdaghi, Mehrnaz ^k   Babaie, Delara ^k   Mohammadzadeh, Iraj ^t   Ghaffari, Javad ^u   Shafiei, Alireza ^v   Kalantari, Najmeddin ^w   Ahanchian, Hamid ^p   Khoshkhui, Maryam ^p   Soheili, Habib ^x   Dabbaghzadeh, Abbas ^t   Shirkani, Afshin ^y   Nasiri Kalmarzi, Rasoul ^z   Mortazavi, Seyed Hamidreza ^aa   Tafaroji, Javad ^ab   Khalili, Abbas ⁿ   Mohammadi, Javad ^ac   Negahdari, Babak ^a   Joghataei, Mohammad Taghi ^ad   al Ramadi, Basel K ^ae   Picard, Capucine ^af   Parvaneh, Nima ^a   Rezaei, Nima ^a,ag   Chatila, Talal A ^c   Massaad, Michel J ^c   Keles, Sevgi ^c   Hammarström, Lennart ^b   Geha, Raif S ^c   Aghamohammadi, Asghar ^a,ag   more..

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e ALBORZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^f HAMADAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^g TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^h TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

ⁱ ALBORZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^j ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^k SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^l SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^m GUILAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

ⁿ SHAHID SADOUGHI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^o SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^p MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^q IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^r ARDABIL UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^s ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^t BABOL UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^u MAZANDARAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^v TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^w GOLESTAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^x ARAK UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^y BUSHEHR UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^z KURDISTAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^aa KERMANSHAH UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^ab QOM UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^ac UNIVERSITY OF TEHRAN   (Iran)

^ad TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^ae UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

^af HÔPITAL NECKER ENFANTS MALADES   (France)

^ag UNIVERSAL SCIENTIFIC EDUCATION AND RESEARCH NETWORK USERN   (Iran)

more..

Author keywords

Combined immunodeficiencies; next generation DNA sequencing; targeted gene panel sequencing; whole exome sequencing

Indexed keywords

ATM PROTEIN; STAT3 PROTEIN;

ARTICLE; CHILD; CHROMOSOME DELETION 22Q11; CHROMOSOME DELETION 22Q11.21; COHORT ANALYSIS; COMBINED IMMUNODEFICIENCY; CONSANGUINITY; DEMOGRAPHY; DIAGNOSTIC VALUE; DNA REPAIR; DNA SEQUENCE; FEMALE; GENE MUTATION; HUMAN; HYPER IGE SYNDROME; INFANT; IRAN; IRANIAN PEOPLE; LABORATORY TEST; MAJOR CLINICAL STUDY; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SURVIVAL RATE; VDJ RECOMBINATION; ADOLESCENT; GENETIC PREDISPOSITION; GENETICS; HIGH THROUGHPUT SEQUENCING; IMMUNE DEFICIENCY; IMMUNOLOGY; MORTALITY; MUTATION; PHENOTYPE; PROCEDURES; RECESSIVE GENE; RETROSPECTIVE STUDY;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; CONSANGUINITY; FEMALE; GENES, RECESSIVE; GENETIC PREDISPOSITION TO DISEASE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; INFANT; IRAN; JOB SYNDROME; MALE; MUTATION; PHENOTYPE; RETROSPECTIVE STUDIES; SEQUENCE ANALYSIS, DNA; STAT3 TRANSCRIPTION FACTOR; SURVIVAL RATE;

EID: 85031108441     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2017.06.049     Document Type: Article

References (54)

1. Boyle, J.M., Buckley, R.H., Population prevalence of diagnosed primary immunodeficiency diseases in the United States. J Clin Immunol 27 (2007), 497–502.
2. Buckley, R.H., Primary immunodeficiency diseases due to defects in lymphocytes. N Engl J Med 343 (2000), 1313–1324.
3. Picard, C., Al-Herz, W., Bousfiha, A., Casanova, J.L., Chatila, T., Conley, M.E., et al. Primary immunodeficiency diseases: an update on the Classification from the International Union of Immunological Societies Expert Committee for Primary Immunodeficiency 2015. J Clin Immunol 35 (2015), 696–726.
4. Lipstein, E.A., Vorono, S., Browning, M.F., Green, N.S., Kemper, A.R., Knapp, A.A., et al. Systematic evidence review of newborn screening and treatment of severe combined immunodeficiency. Pediatrics 125 (2010), e1226–e1235.
5. Al-Herz, W., Notarangelo, L.D., Sadek, A., Buckley, R., Consortium U. Combined immunodeficiency in the United States and Kuwait: comparison of patients' characteristics and molecular diagnosis. Clin Immunol 161 (2015), 170–173.
6. Kwan, A., Abraham, R.S., Currier, R., Brower, A., Andruszewski, K., Abbott, J.K., et al. Newborn screening for severe combined immunodeficiency in 11 screening programs in the United States. JAMA 312 (2014), 729–738.
7. Azarsiz, E., Gulez, N., Edeer Karaca, N., Aksu, G., Kutukculer, N., Consanguinity rate and delay in diagnosis in Turkish patients with combined immunodeficiencies: a single-center study. J Clin Immunol 31 (2011), 106–111.
8. Suliaman, F., Al-Ghonaium, A., Harfi, H., High incidence of severe combined immune deficiency in the Eastern Province of Saudi Arabia. Pediatr Asthma Allergy Immunol 19 (2006), 14–18.
9. Felgentreff, K., Perez-Becker, R., Speckmann, C., Schwarz, K., Kalwak, K., Markelj, G., et al. Clinical and immunological manifestations of patients with atypical severe combined immunodeficiency. Clin Immunol 141 (2011), 73–82.
10. Fischer, A., Le Deist, F., Hacein-Bey-Abina, S., Andre-Schmutz, I., Basile Gde, S., de Villartay, J.P., et al. Severe combined immunodeficiency. A model disease for molecular immunology and therapy. Immunol Rev 203 (2005), 98–109.
11. Fischer, A., Hacein-Bey-Abina, S., Cavazzana-Calvo, M., Gene therapy of primary T cell immunodeficiencies. Gene 525 (2013), 170–173.
12. Pai, S.Y., Logan, B.R., Griffith, L.M., Buckley, R.H., Parrott, R.E., Dvorak, C.C., et al. Transplantation outcomes for severe combined immunodeficiency, 2000-2009. N Engl J Med 371 (2014), 434–446.
13. Brown, L., Xu-Bayford, J., Allwood, Z., Slatter, M., Cant, A., Davies, E.G., et al. Neonatal diagnosis of severe combined immunodeficiency leads to significantly improved survival outcome: the case for newborn screening. Blood 117 (2011), 3243–3246.
14. Maguire, A.M., High, K.A., Auricchio, A., Wright, J.F., Pierce, E.A., Testa, F., et al. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 374 (2009), 1597–1605.
15. van der Spek, J., Groenwold, R.H., van der Burg, M., van Montfrans, J.M., TREC based newborn screening for severe combined immunodeficiency disease: a systematic review. J Clin Immunol 35 (2015), 416–430.
16. Vrijenhoek, T., Kraaijeveld, K., Elferink, M., de Ligt, J., Kranendonk, E., Santen, G., et al. Next-generation sequencing-based genome diagnostics across clinical genetics centers: implementation choices and their effects. Eur J Hum Genet 23 (2015), 1142–1150.
17. Matthijs, G., Souche, E., Alders, M., Corveleyn, A., Eck, S., Feenstra, I., et al. Guidelines for diagnostic next-generation sequencing. Eur J Hum Genet, 24, 2016, 1515.
18. Stranneheim, H., Wedell, A., Exome and genome sequencing: a revolution for the discovery and diagnosis of monogenic disorders. J Intern Med 279 (2016), 3–15.
19. Modell, V., Knaus, M., Modell, F., Roifman, C., Orange, J., Notarangelo, L.D., Global overview of primary immunodeficiencies: a report from Jeffrey Modell Centers worldwide focused on diagnosis, treatment, and discovery. Immunol Res 60 (2014), 132–144.
20. Lam, D.S., Lee, T.L., Chan, K.W., Ho, H.K., Lau, Y.L., Primary immunodeficiency in Hong Kong and the use of genetic analysis for diagnosis. Hong Kong Med J 11 (2005), 90–96.
21. Zhang, Z.Y., An, Y.F., Jiang, L.P., Liu, W., Liu, D.W., Xie, J.W., et al. Distribution, clinical features and molecular analysis of primary immunodeficiency diseases in Chinese children: a single-center study from 2005 to 2011. Pediatr Infect Dis J 32 (2013), 1127–1134.
22. Lee, W.I., Huang, J.L., Jaing, T.H., Shyur, S.D., Yang, K.D., Chien, Y.H., et al. Distribution, clinical features and treatment in Taiwanese patients with symptomatic primary immunodeficiency diseases (PIDs) in a nationwide population-based study during 1985-2010. Immunobiology 216 (2011), 1286–1294.
23. Chinnabhandar, V., Yadav, S.P., Kaul, D., Verma, I.C., Sachdeva, A., Primary immunodeficiency disorders in the developing world: data from a hospital-based registry in India. Pediatr Hematol Oncol 31 (2014), 207–211.
24. Kilic, S.S., Ozel, M., Hafizoglu, D., Karaca, N.E., Aksu, G., Kutukculer, N., The prevalences [correction] and patient characteristics of primary immunodeficiency diseases in Turkey—two centers study. J Clin Immunol 33 (2013), 74–83.
25. Mellouli, F., Mustapha, I.B., Khaled, M.B., Besbes, H., Ouederni, M., Mekki, N., et al. Report of the Tunisian Registry of Primary Immunodeficiencies: 25-years of experience (1988-2012). J Clin Immunol 35 (2015), 745–753.
26. Gathmann, B., Binder, N., Ehl, S., Kindle, G., Party, E.R.W., The European internet-based patient and research database for primary immunodeficiencies: update 2011. Clin Exp Immunol 167 (2012), 479–491.
27. Aghamohammadi, A., Mohammadinejad, P., Abolhassani, H., Mirminachi, B., Movahedi, M., Gharagozlou, M., et al. Primary immunodeficiency disorders in Iran: update and new insights from the third report of the national registry. J Clin Immunol 34 (2014), 478–490.
28. Latif, A.H., Tabassomi, F., Abolhassani, H., Hammarstrom, L., Molecular diagnosis of primary immunodeficiency diseases in a developing country: Iran as an example. Expert Rev Clin Immunol 10 (2014), 385–396.
29. Arandi, N., Mirshafiey, A., Abolhassani, H., Jeddi-Tehrani, M., Edalat, R., Sadeghi, B., et al. Frequency and expression of inhibitory markers of CD4(+) CD25(+) FOXP3(+) regulatory T cells in patients with common variable immunodeficiency. Scand J Immunol 77 (2013), 405–412.
30. Oraei, M., Aghamohammadi, A., Rezaei, N., Bidad, K., Gheflati, Z., Amirkhani, A., et al. Naive CD4+ T cells and recent thymic emigrants in common variable immunodeficiency. J Investig Allergol Clin Immunol 22 (2012), 160–167.
31. Salek Farrokhi, A., Aghamohammadi, A., Pourhamdi, S., Mohammadinejad, P., Abolhassani, H., Moazzeni, S.M., Evaluation of class switch recombination in B lymphocytes of patients with common variable immunodeficiency. J Immunol Methods 394 (2013), 94–99.
32. Aghamohammadi, A., Moin, M., Kouhi, A., Mohagheghi, M.A., Shirazi, A., Rezaei, N., et al. Chromosomal radiosensitivity in patients with common variable immunodeficiency. Immunobiology 213 (2008), 447–454.
33. Conley, M.E., Notarangelo, L.D., Etzioni, A., Diagnostic criteria for primary immunodeficiencies. Representing PAGID (Pan-American Group for Immunodeficiency) and ESID (European Society for Immunodeficiencies). Clin Immunol 93 (1999), 190–197.
34. Shearer, W.T., Dunn, E., Notarangelo, L.D., Dvorak, C.C., Puck, J.M., Logan, B.R., et al. Establishing diagnostic criteria for severe combined immunodeficiency disease (SCID), leaky SCID, and Omenn syndrome: the Primary Immune Deficiency Treatment Consortium experience. J Allergy Clin Immunol 133 (2014), 1092–1098.
35. Miller, S.A., Dykes, D.D., Polesky, H.F., A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res, 16, 1988, 1215.
36. Aghamohammadi, A., Parvaneh, N., Rezaei, N., Moazzami, K., Kashef, S., Abolhassani, H., et al. Clinical and laboratory findings in hyper-IgM syndrome with novel CD40L and AICDA mutations. J Clin Immunol 29 (2009), 769–776.
37. Abdollahpour, H., Appaswamy, G., Kotlarz, D., Diestelhorst, J., Beier, R., Schaffer, A.A., et al. The phenotype of human STK4 deficiency. Blood 119 (2012), 3450–3457.
38. Safaei, S., Fazlollahi, M.R., Houshmand, M., Hamidieh, A.A., Bemanian, M.H., Alavi, S., et al. Detection of six novel mutations in WASP gene in fifteen Iranian Wiskott-Aldrich patients. Iran J Allergy Asthma Immunol 11 (2012), 345–348.
39. Sanati, M.H., Bayat, B., Aleyasin, A., Atashi Shirazi, H., Isaian, A., Farhoudi, A., et al. ATM gene mutations detection in Iranian ataxia-telangiectasia patients. Iran J Allergy Asthma Immunol 3 (2004), 59–63.
40. Sedghi, M., Nouri, N., Abdali, H., Memarzadeh, M., Nouri, N., A case report of 22q11 deletion syndrome confirmed by array-CGH method. J Res Med Sci 17 (2012), 310–312.
41. Yu, H., Zhang, V.W., Stray-Pedersen, A., Hanson, I.C., Forbes, L.R., de la Morena, M.T., et al. Rapid molecular diagnostics of severe primary immunodeficiency determined by using targeted next-generation sequencing. J Allergy Clin Immunol 138 (2016), 1142–1151.
42. Feng, Y., Chen, D., Wang, G.L., Zhang, V.W., Wong, L.J., Improved molecular diagnosis by the detection of exonic deletions with target gene capture and deep sequencing. Genet Med 17 (2015), 99–107.
43. Fang, M., Abolhassani, H., Lim, C.K., Zhang, J., Hammarstrom, L., Next generation sequencing data analysis in primary immunodeficiency disorders—future directions. J Clin Immunol 36:suppl 1 (2016), 68–75.
44. Saadat, M., Ansari-Lari, M., Farhud, D.D., Consanguineous marriage in Iran. Ann Hum Biol 31 (2004), 263–269.
45. Vakilian, K., Ranjbaran, M., Khorsandi, M., Sharafkhani, N., Khodadost, M., Prevalence of preterm labor in Iran: a systematic review and meta-analysis. Int J Reprod Biomed (Yazd) 13 (2015), 743–748.
46. Stoddard, J.L., Niemela, J.E., Fleisher, T.A., Rosenzweig, S.D., Targeted NGS: a cost-effective approach to molecular diagnosis of PIDs. Front Immunol, 5, 2014, 531.
47. Nijman, I.J., van Montfrans, J.M., Hoogstraat, M., Boes, M.L., van de Corput, L., Renner, E.D., et al. Targeted next-generation sequencing: a novel diagnostic tool for primary immunodeficiencies. J Allergy Clin Immunol 133 (2014), 529–534.
48. Moens, L.N., Falk-Sorqvist, E., Asplund, A.C., Bernatowska, E., Smith, C.I., Nilsson, M., Diagnostics of primary immunodeficiency diseases: a sequencing capture approach. PLoS One, 9, 2014, e114901.
49. Al-Mousa, H., Abouelhoda, M., Monies, D.M., Al-Tassan, N., Al-Ghonaium, A., Al-Saud, B., et al. Unbiased targeted next-generation sequencing molecular approach for primary immunodeficiency diseases. J Allergy Clin Immunol 137 (2016), 1780–1787.
50. Stray-Pedersen, A., Sorte, H.S., Samarakoon, P., Gambin, T., Chinn, I.K., Coban Akdemir, Z.H., et al. Primary immunodeficiency diseases—genomic approaches delineate heterogeneous Mendelian disorders. J Allergy Clin Immunol 139 (2017), 232–245.
51. Gallo, V., Dotta, L., Giardino, G., Cirillo, E., Lougaris, V., D'Assante, R., et al. Diagnostics of primary immunodeficiencies through next-generation sequencing. Front Immunol, 7, 2016, 466.
52. Erman, B., Bilic, I., Hirschmugl, T., Salzer, E., Boztug, H., Sanal, O., et al. Investigation of genetic defects in severe combined immunodeficiency patients from Turkey by targeted sequencing. Scand J Immunol 85 (2017), 227–234.
53. Hartberger J, Frey-Jakobs S, Fliegauf M, Bulashevska A, Fröbel P, Nöltner C, et al. Autosomal-recessive stat-3-like hyper-IgE syndrome caused by a homozygous mutation in a zinc finger transcription factor [abstract no. ESID6-0917]. Abstract presented at: XVIIth ESID; Barcelona, Spain; 2016.
54. Yeganeh, M., Heidarzade, M., Pourpak, Z., Parvaneh, N., Rezaei, N., Gharagozlou, M., et al. Severe combined immunodeficiency: a cohort of 40 patients. Pediatr Allergy Immunol 19 (2008), 303–306.