Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines

Ilki, Arzu; karabiber, esra; atik, özge; Tepetam, Fatma Merve; Ergan, Bilgehan; Karakoc-Aydiner, Elif; OZEN, AHMET; Özyer, Fatma; Baris, Safa

doi:10.5578/tt.20239705

Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines

Esra KARABİBER, (Marmara Üniversitesi Pendik Eğitim ve Araştırma Hastanesi, Erişkin İmmünolojisi ve Alerji Bilim Dalı, Göğüs Hastalıkları Kliniği, İstanbul, Türkiye)

Özge ATİK, (Süreyyapaşa Eğitim ve Araştırma Hastanesi, Göğüs Hastalıkları Kliniği, Yetişkin İmmünolojisi ve Alerji Bilim Dalı, İstanbul, Türkiye)

Fatma Merve TEPETAM, (Süreyyapaşa Eğitim ve Araştırma Hastanesi, Göğüs Hastalıkları Kliniği, Yetişkin İmmünolojisi ve Alerji Bilim Dalı, İstanbul, Türkiye)

Bilgehan ERGAN, (Marmara Üniversitesi, Tıp Fakültesi, Tıbbi Mikrobiyoloji Anabilim Dalı, İstanbul, Türkiye)

Arzu İLKİ, (Marmara Üniversitesi, Tıp Fakültesi, Tıbbi Mikrobiyoloji Anabilim Dalı, İstanbul, Türkiye)

Elif KARAKOÇ AYDINER, (Marmara Üniversitesi, Tıp Fakültesi, Çocuk Alerji ve İmmünoloji Anabilim Dalı, İstanbul, Türkiye)

Ahmet ÖZEN, (Marmara Üniversitesi, Tıp Fakültesi, Çocuk Alerji ve İmmünoloji Anabilim Dalı, İstanbul, Türkiye)

Fatma ÖZYER, (Marmara Üniversitesi Pendik Eğitim ve Araştırma Hastanesi, Erişkin İmmünolojisi ve Alerji Bilim Dalı, Göğüs Hastalıkları Kliniği, İstanbul, Türkiye)

Safa BARIŞ (Marmara Üniversitesi, Tıp Fakültesi, Çocuk Alerji ve İmmünoloji Anabilim Dalı, İstanbul, Türkiye)

Tüberküloz ve Toraks

3 0

Yıl: 2023 Cilt: 71 Sayı: 3 Sayfa Aralığı: 236 - 249 Metin Dili: İngilizce DOI: 10.5578/tt.20239705 İndeks Tarihi: 27-10-2023

Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines

Öz:

Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines Introduction: Vaccines against severe acute respiratory syndrome-coronavi- rus-2 (SARS-CoV-2) provide successful control of the coronavirus-2019 (COVID-19) pandemic. The safety and immunogenicity studies are encourag- ing in patients with inborn errors of immunity (IEI); however, data about mortality outcomes and severe disease after vaccination still need to be fully addressed. Therefore, we aimed to determine the clinical and immunological outcomes of SARS-CoV-2 infection in patients with IEI who have received vac- cination. Materials and Methods: Eighty-eight patients with a broad range of molecular etiologies were studied; 45 experienced SARS-CoV-2 infection. Infection out- comes were analyzed in terms of genetic etiology, background clinical char - acteristics, and immunization history, including the type and number of doses received and the time elapsed since vaccination. In addition, anti-SARS-CoV-2 antibodies were quantified using electrochemiluminescent immunoassay. Results: Patients were immunized using one of the three regimens: inactivated (Sinovac, Coronavac®), mRNA (BNT162b2, Comirnaty®, Pfizer-Biontech), and a combination. All three regimens induced comparable anti-SARS-CoV-2 IgG levels, with no differences in the adverse events. Among 45 patients with COVID-19, 26 received a full course of vaccination, while 19 were vaccine-naive or received incomplete dosing. No patients died due to COVID-19 infection. The fully immunized group had a lower hospitalization rate (23% vs. 31.5%) and a shorter sympto- matic phase than the others. Among the fully vaccinated patients, serum IgM and E levels were significantly lower in hospitalized patients than non-hospitalized patients. Conclusion: COVID-19 vaccines were well-tolerated by the IEI patients, and a full course of immunization was associated with lower hospitalization rates and a shorter duration of COVID-19 symptoms.

Anahtar Kelime: Inborn errors of immunity the Pfizer/BioNTech BNT162b2 Sinovac SARS-CoV-2 COVID-19 vaccines

İmmün sistemin doğuştan gelen kusurları olan hastalarda farklı marka ve dozlarda uygulanan SARS-CoV-2 aşısı sonrası SARS- CoV-2 enfeksiyonunun klinik ve immünolojik sonuçları

Öz:

Giriş: Şiddetli akut solunum sendromu koronavirüs-2 (SARS-CoV-2) aşıları koronavirüs (COVID-19) pandemisinin başarılı şekilde kontrol edilmesinde etkili olmuştur. İmmün sistemin doğuştan gelen kusurları (IEI) olan hastalarda aşıların güvenilirlik ve immünoje- nite çalışmaları ümit verici sonuçlar vermis olsa da aşı sonrası mortalite sonuçları ve hastalık şiddeti hakkındaki veriler henüz kısıtlıdır. Bu nedenle SARS-CoV-2 aşıları uygulanan IEI hastalarında SARS-CoV-2 enfeksiyonunun klinik ve immünolojik sonuçlarını değerlendir- meyi amaçladık. Materyal ve Metod: Kırk beşi SARS-CoV-2 enfeksiyonunu geçiren, farklı moleküler etiyolojiye sahip 88 IEI hastası çalışmaya dahil edildi. Enfeksiyon sonuçları, altta yatan genetik etiyoloji, klinik özellikler, uygulanan aşı doz sayısı, aşı markası ve aşılamadan hastalık oluşana kadar geçen süreye göre analiz edildi. Ayrıca anti-SARS-CoV-2 antikor düzeyleri elektrokemilüminesan yöntemi ile ölçüldü. Bulgular: COVID-19 geçiren 45 hastadan 26’sı tam doz aşılı iken, 19’u eksik doz ya da hiç aşı olmayan hastalardan oluşmaktaydı. Hastaların aşı şeması, inaktif (Sinovac, Coronavac®), mRNA (BNT162b2, Comirnaty®, Pfizer-BioNTech) ve iki aşının kombinasyonu olmak üzere üç farklı grupta değerlendirildi. Her üç grupta da benzer anti-SARS-CoV-2 antikor düzeyleri saptandı ve yan etki profili benzerdi. Tüm gruplarda COVID-19 enfeksiyonu ile ilişkili ölüm olmadı. Tam doz aşılı grupta hastane yatış oranı (%23’e karşı %31,5) ve semptomatik gün sayısı diğer gruba göre daha düşük idi. Tam doz aşılı olup hastane yatışı olanlarda serum IgM ve IgE düzeyleri hastaneye yatmayanlara kıyasla anlamlı olarak düşük saptandı. Sonuç: IEI hastalarında tam doz SARS-CoV-2 aşılaması iyi tolere edilir ve daha düşük oranda hastane yatışı ve daha az COVID-19 semptom süresiyle ilişkilidir.

Anahtar Kelime: İmmün sistemin doğuştan gelen kusurları Pfizer/BioNTech BNT162b2 Sinovac SARS-CoV-2 COVID-19 aşıları

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

1. Worldometer. Coronavirus (COVID-19) mortality rate 2023. Updated May 26, 2023. Available from: https:// www.worldometers.info/coronavirus/.
2. Korber B, Fischer WM, Gnanakaran S, Yoon H, Theiler J, Abfalterer W, et al. Tracking changes in SARS-CoV-2 spike: Evidence that D614G increases infectivity of the COVID19 virus. Cell 2020; 182(4): 812-27. https://doi. org/10.1016/j.cell.2020.06.043
3. World Health Organization (WHO). SARS-COV-2- variants-of-concern, 2022. Available from: https://www. who.int/news/item/16-03-2023-statement-on-the-updateof-who-s-working-definitions-and-tracking-system-for-sarscov-2-variants-of-concern-and-variants-of-interest.
4. Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and Is blocked by a clinically proven protease inhibitor. Cell 2020; 181(2): 271-80. https://doi.org/10.1016/j.cell.2020.02.052
5. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 2020; 395(10229): 1054-62. https://doi. org/10.1016/S0140-6736(20)30566-3
6. Weiss P, Murdoch DR. Clinical course and mortality risk of severe COVID-19. Lancet 2020; 395(10229): 1014-5. https://doi.org/10.1016/S0140-6736(20)30633-4
7. Gao Y, Chen Y, Liu M, Shi S, Tian J. Impacts of immunosuppression and immunodeficiency on COVID-19: A systematic review and meta-analysis. J Infect 2020; 81(2): e93- e5. https://doi.org/10.1016/j.jinf.2020.05.017
8. Karakoc Aydiner E, Bilgic Eltan S, Babayeva R, Aydiner O, Kepenekli E, Kolukisa B, et al. Adverse COVID-19 outcomes in immune deficiencies: Inequality exists between subclasses. Allergy 2022; 77(1): 282-95. https://doi. org/10.1111/all.15025
9. Manners C, Larios Bautista E, Sidoti H, Lopez OJ. Protective adaptive immunity against severe acute respiratory syndrome coronaviruses 2 (SARS-CoV-2) and implications for vaccines. Cureus 2020; 12(6): e8399. https://doi. org/10.7759/cureus.8399
10. Brodin P. Immune determinants of COVID-19 disease presentation and severity. Nat Med 2021; 27(1): 28-33. https://doi.org/10.1038/s41591-020-01202-8
11. Baek WK, Sohn SY, Mahgoub A, Hage R. A comprehensive review of severe acute respiratory syndrome coronavirus 2. Cureus 2020; 12(5): e7943. https://doi.org/10.7759/ cureus.7943
12. Bastard P, Michailidis E, Hoffmann HH, Chbihi M, Le Voyer T, Rosain J, et al. Auto-antibodies to type I IFNs can underlie adverse reactions to yellow fever live attenuated vaccine. J Exp Med 2021; 218(4). https://doi.org/10.1084/ jem.20202486
13. Chouaki Benmansour N, Carvelli J, Vivier E. Complement cascade in severe forms of COVID-19: Recent advances in therapy. Eur J Immunol 2021; 51(7): 1652-9. https://doi. org/10.1002/eji.202048959
14. Zhou Y, Liu Z, Li S, Xu W, Zhang Q, Silva IT, et al. Enhancement versus neutralization by SARS-CoV-2 antibodies from a convalescent donor associates with distinct epitopes on the RBD. Cell Rep 2021; 34(5): 108699. https://doi.org/10.1016/j.celrep.2021.108699
15. Weiskopf D, Schmitz KS, Raadsen MP, Grifoni A, Okba NMA, Endeman H, et al. Phenotype and kinetics of SARSCoV-2-specific T cells in COVID-19 patients with acute respiratory distress syndrome. Sci Immunol 2020; 5(48). https://doi.org/10.1126/sciimmunol.abd2071
16. Meckiff BJ, Ramirez-Suastegui C, Fajardo V, Chee SJ, Kusnadi A, Simon H, et al. Imbalance of regulatory and cytotoxic SARS-CoV-2-Reactive CD4 (+) T Cells in COVID19. Cell 2020; 183(5): 1340-53. https://doi.org/10.1016/j. cell.2020.10.001
17. Tan AT, Linster M, Tan CW, Le Bert N, Chia WN, Kunasegaran K, et al. Early induction of functional SARSCoV-2-specific T cells associates with rapid viral clearance and mild disease in COVID-19 patients. Cell Rep 2021; 34(6): 108728. https://doi.org/10.1016/j.celrep.2021.108728
18. Rydyznski Moderbacher C, Ramirez SI, Dan JM, Grifoni A, Hastie KM, Weiskopf D, et al. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell 2020; 183(4): 996-1012. https://doi.org/10.1016/j.cell.2020.09.038
19. Casado JL, Häemmerle J, Vizcarra P, Velasco H, Velasco T, Fernandez-Escribano M, et al. SARS CoV-2 infections in healthcare workers with a pre-existing T-cell response: A prospective cohort study. Clin Microbiol Infect 2021; 27(6): 916.e1-.e4. https://doi.org/10.1016/j. cmi.2021.02.020
20. Kołtan S, Ziętkiewicz M, Grześk E, Becht R, Berdej-Szczot E, Cienkusz M, et al. COVID-19 in unvaccinated patients with inborn errors of immunity-polish experience. Front Immunol 2022; 13. https://doi.org/10.3389/ fimmu.2022.953700
21. Cohen B, Rubinstein R, Gans MD, Deng L, Rubinstein A, Eisenberg R. COVID-19 infection in 10 common variable immunodeficiency patients in New York City. J Allergy Clin Immunol Pract 2021; 9(1): 504-7.e1. https://doi. org/10.1016/j.jaip.2020.11.006
22. Mullur J, Wang A, Feldweg A. A fatal case of coronavirus disease 2019 in a patient with common variable immunodeficiency. Ann Allergy Asthma Immunol 2021; 126(1): 90-2. https://doi.org/10.1016/j.anai.2020.08.017
23. Marcus N, Frizinsky S, Hagin D, Ovadia A, Hanna S, Farkash M, et al. Minor clinical impact of COVID-19 pandemic on patients with primary immunodeficiency in Israel. Front Immunol 2020; 11: 614086. https://doi. org/10.3389/fimmu.2020.614086
24. Ribeiro LC, Benites BD, Ulaf RG, Nunes TA, Costa-Lima C, Addas-Carvalho M, et al. Rapid clinical recovery of a SARS-CoV-2 infected common variable immunodeficiency patient following the infusion of COVID-19 convalescent plasma. Allergy Asthma Clin Immunol 2021; 17(1): 14. https://doi.org/10.1186/s13223-021-00518-5
25. Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, et al. Safety and efficacy of the BNT162b2 mRNA COVID-19 vaccine. N Engl J Med 2020; 383(27): 2603-15. https://doi.org/10.1056/NEJMoa2034577
26. Saad-Roy CM, Morris SE, Metcalf CJE, Mina MJ, Baker RE, Farrar J, et al. Epidemiological and evolutionary considerations of SARS-CoV-2 vaccine dosing regimes. Science 2021; 372(6540): 363-70. https://doi.org/10.1126/science.abg8663
27. T.C. Sağlık Bakanlığı. COVID-19 aşısı ulusal uygulama stratejisi (2021). Available from: https://covid19asi.saglik. gov.tr/TR-77706/covid-19-asisi-ulusal-uygulama-stratejisi. html.
28. World Health Organization (WHO). COVID-19 vaccines advice (2023). Available from: https://www.who.int/ emergencies/diseases/novel-coronavirus-2019/covid-19- vaccines/advice.
29. European Society for Immunodeficiencies. 2022, updated March 2022. Available from: https://esid.org/NewsEvents/ESID-COVID-19-Statement-March-2022.
30. Sobh A, Bonilla FA. Vaccination in primary immunodeficiency disorders. J Allergy Clin Immunol Pract 2016; 4(6): 1066-75. https://doi.org/10.1016/j.jaip.2016.09.012
31. Delmonte OM, Bergerson JRE, Burbelo PD, Durkee-Shock JR, Dobbs K, Bosticardo M, et al. Antibody responses to the SARS-CoV-2 vaccine in individuals with various inborn errors of immunity. J Allergy Clin Immunol 2021; 148(5): 1192-7. https://doi.org/10.1016/j.jaci.2021.08.016
32. Hagin D, Freund T, Navon M, Halperin T, Adir D, Marom R, et al. Immunogenicity of Pfizer-BioNTech COVID-19 vaccine in patients with inborn errors of immunity. J Allergy Clin Immunol 2021; 148(3): 739-49. https://doi. org/10.1016/j.jaci.2021.05.029
33. Squire J, Joshi A. Seroconversion after coronavirus disease 2019 vaccination in patients with immune deficiency. Ann Allergy Asthma Immunol 2021; 127(3): 383-4. https:// doi.org/10.1016/j.anai.2021.05.015
34. Tangye SG; COVID Human Genetic Effort consortium. Impact of SARS-CoV-2 infection and COVID-19 on patients with inborn errors of immunity. J Allergy Clin Immunol 2023; 151(4): 818-31. https://doi.org/10.1016/j. jaci.2022.11.010
35. Seidel MG, Kindle G, Gathmann B, Quinti I, Buckland M, van Montfrans J, 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. https:// doi.org/10.1016/j.jaip.2019.02.004
36. Bousfiha A, Jeddane L, Picard C, Al-Herz W, Ailal F, Chatila T, et al. Human inborn errors of immunity: 2019 update of the IUIS phenotypical classification. J Clin Immunol 2020; 40(1): 66-81. https://doi.org/10.1007/s10875-020- 00758-x
37. Baris S, Abolhassani H, Massaad MJ, Al-Nesf M, Chavoshzadeh Z, Keles S, et al. The Middle East and North Africa Diagnosis and Management Guidelines for inborn errors of immunity. J Allergy Clin Immunol Pract 2023; 11(1): 158-80.e11. https://doi.org/10.1016/j. jaip.2022.10.003
38. Bucciol G, Tangye SG, Meyts I. Coronavirus disease 2019 in patients with inborn errors of immunity: Lessons learned. Curr Opin Pediatr 2021; 33(6): 648-56. https://doi.org/10.1097/MOP.0000000000001062
39. World Health Organization (WHO). WHO weekly epidemiological update on COVID-19- edition 51.Geneva: WHO; 2021. Available from: https://www.who.int/publications/m/item/weekly-epidemiological-up - date-on-covid-19-3-august-2021 (Accessed date: 24.08.2021).
40. Dong E, Du H, Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis 2020; 20(5): 533-4. https://doi.org/10.1016/S1473- 3099(20)30120-1
41. Bergman P, Blennow O, Hansson L, Mielke S, Nowak P, Chen P, et al. Safety and efficacy of the mRNA BNT162b2 vaccine against SARS-CoV-2 in five groups of immunocompromised patients and healthy controls in a prospective open-label clinical trial. EBioMedicine 2021; 74: 103705. https://doi.org/10.1016/j.ebiom.2021.103705
42. Arroyo-Sánchez D, Cabrera-Marante O, Laguna-Goya R, Almendro-Vázquez P, Carretero O, Gil-Etayo FJ, et al. Immunogenicity of Anti-SARS-CoV-2 vaccines in common variable immunodeficiency. J Clin Immunol 2022; 42(2): 240-52. https://doi.org/10.1007/s10875-021-01174-5
43. Salinas AF, Mortari EP, Terreri S, Quintarelli C, Pulvirenti F, Di Cecca S, et al. SARS-CoV-2 vaccine induced atypical immune responses in antibody defects: Everybody does their best. J Clin Immunol 2021; 41(8): 1709-22. https:// doi.org/10.1007/s10875-021-01133-0
44. Shields AM, Faustini SE, Hill HJ, Al-Taei S, Tanner C, Ashford F, et al. SARS-CoV-2 vaccine responses in individuals with antibody deficiency: Findings from the COV-AD Study. J Clin Immunol 2022; 42(5): 923-34. https://doi. org/10.1007/s10875-022-01231-7
45. Guan WJ, Liang WH, Zhao Y, Liang HR, Chen ZS, Li YM, et al. Comorbidity and its impact on 1590 patients with COVID-19 in China: A nationwide analysis. Eur Respir J 2020; 55(5). https://doi.org/10.1183/13993003.01227- 2020
46. Minotti C, Tirelli F, Barbieri E, Giaquinto C, Donà D. How is immunosuppressive status affecting children and adults in SARS-CoV-2 infection? A systematic review. J Infect 2020; 81(1): e61-e6. https://doi.org/10.1016/j. jinf.2020.04.026
47. Van Damme KFA, Tavernier S, Van Roy N, De Leeuw E, Declercq J, Bosteels C, et al. Case report: Convalescent plasma, a targeted therapy for patients with COVID and severe COVID-19. Front Immunol 2020; 11: 596761. https://doi.org/10.3389/fimmu.2020.596761
48. Gupta S, Su H, Narsai T, Agrawal S. SARS-CoV-2-associated T-Cell responses in the presence of humoral immunodeficiency. Int Arch Allergy Immunol 2021; 182(3): 195-209. https://doi.org/10.1159/000514193
49. Meyts I, Bucciol G, Quinti I, Neven B, Fischer A, Seoane E, et al. Coronavirus disease 2019 in patients with inborn errors of immunity: An international study. J Allergy Clin Immunol 2021; 147(2): 520-31. https://doi.org/10.1016/j. jaci.2020.09.010
50. Quinti I, Lougaris V, Milito C, Cinetto F, Pecoraro A, Mezzaroma I, et al. A possible role for B cells in COVID19? Lesson from patients with agammaglobulinemia. J Allergy Clin Immunol 2020; 146(1): 211-3.e4. https://doi.org/10.1016/j.jaci.2020.04.013
51. Milito C, Lougaris V, Giardino G, Punziano A, Vultaggio A, Carrabba M, et al. Clinical outcome, incidence, and SARSCoV-2 infection-fatality rates in Italian patients with inborn errors of immunity. J Allergy Clin Immunol Pract 2021; 9(7): 2904-6.e2. https://doi.org/10.1016/j. jaip.2021.04.017
52. Ho HE, Mathew S, Peluso MJ, Cunningham-Rundles C. Clinical outcomes and features of COVID-19 in patients with primary immunodeficiencies in New York City. J Allergy Clin Immunol Pract 2021; 9(1): 490-3 e2. https:// doi.org/10.1016/j.jaip.2020.09.052
53. Aljaberi R, Wishah K. Positive outcome in a patient with coronavirus disease 2019 and common variable immunodeficiency after intravenous immunoglobulin. Ann Allergy Asthma Immunol 2020; 125(3): 349-50. https://doi. org/10.1016/j.anai.2020.06.006
54. Pulvirenti F, Fernandez Salinas A, Milito C, Terreri S, Piano Mortari E, Quintarelli C, et al. B Cell response induced by SARS-CoV-2 infection Is boosted by the BNT162b2 vaccine in primary antibody deficiencies. Cells 2021; 10(11). https://doi.org/10.3390/cells10112915
55. Cousins K, Defelice N, Jeong S, Feng J, Lee A, Rotella K, et al. SARS-COV-2 infections in inborn errors of immunity: A single center study. Front Immunol 2022; 13. https://doi. org/10.3389/fimmu.2022.1035571
56. Leung D, Mu X, Duque J, Cheng S, Wang M, Zhang W, et al. Safety and immunogenicity of 3 doses of BNT162b2 and CoronaVac in children and adults with inborn errors of immunity 2022; 13: 982155. https://doi.org/10.22541/ au.165629347.75546543/v1
57. Bitzenhofer M, Suter-Riniker F, Moor MB, Sidler D, Horn MP, Gschwend A, et al. Humoral response to mRNA vaccines against SARS-CoV-2 in patients with humoral immunodeficiency disease. PLoS One 2022; 17(6): e0268780. https://doi.org/10.1371/journal.pone.0268780
58. Kinoshita H, Durkee-Shock J, Jensen-Wachspress M, Kankate VV, Lang H, Lazarski CA, et al. Robust antibody and T Cell responses to SARS-CoV-2 in patients with antibody deficiency. J Clin Immunol 2021; 41(6): 1146-53. https://doi.org/10.1007/s10875-021-01046-y
59. Amodio D, Ruggiero A, Sgrulletti M, Pighi C, Cotugno N, Medri C, et al. Humoral and cellular response following vaccination with the BNT162b2 mRNA COVID-19 vaccine in patients affected by primary immunodeficiencies. Front Immunol 2021; 12: 727850. https://doi. org/10.3389/fimmu.2021.727850
60. Abo-Helo N, Muhammad E, Ghaben-Amara S, Panasoff J, Cohen S. Specific antibody response of patients with common variable immunodeficiency to BNT162b2 coronavirus disease 2019 vaccination. Ann Allergy Asthma Immunol 2021; 127(4): 501-3. https://doi.org/10.1016/j. anai.2021.07.021
61. Romano C, Esposito S, Donnarumma G, Marrone A. Detection of neutralizing anti-severe acute respiratory syndrome coronavirus 2 antibodies in patients with common variable immunodeficiency after immunization with messenger RNA vaccines. Ann Allergy Asthma Immunol 2021; 127(4): 499-501. https://doi.org/10.1016/j. anai.2021.07.026
62. US Center for Disease Control and Prevention. COVID-19 vaccines for moderately to severely immunocompromised people, 2023. Available from: https://www.cdc.gov/vaccines/covid-19/clinical-considerations/interim-considerations-us.html#immunocompromised.
63. Di Germanio C, Simmons G, Thorbrogger C, Martinelli R, Stone M, Gniadek T, et al. Vaccination of COVID-19 convalescent plasma donors increases binding and neutralizing antibodies against SARS-CoV-2 variants. Transfusion 2022; 62(3): 563-9. https://doi.org/10.1111/trf.16823

APA	karabiber e, atik ö, Tepetam F, Ergan B, Ilki A, Karakoc-Aydiner E, OZEN A, Özyer F, Baris S (2023). Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. , 236 - 249. 10.5578/tt.20239705
Chicago	karabiber esra,atik özge,Tepetam Fatma Merve,Ergan Bilgehan,Ilki Arzu,Karakoc-Aydiner Elif,OZEN AHMET,Özyer Fatma,Baris Safa Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. (2023): 236 - 249. 10.5578/tt.20239705
MLA	karabiber esra,atik özge,Tepetam Fatma Merve,Ergan Bilgehan,Ilki Arzu,Karakoc-Aydiner Elif,OZEN AHMET,Özyer Fatma,Baris Safa Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. , 2023, ss.236 - 249. 10.5578/tt.20239705
AMA	karabiber e,atik ö,Tepetam F,Ergan B,Ilki A,Karakoc-Aydiner E,OZEN A,Özyer F,Baris S Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. . 2023; 236 - 249. 10.5578/tt.20239705
Vancouver	karabiber e,atik ö,Tepetam F,Ergan B,Ilki A,Karakoc-Aydiner E,OZEN A,Özyer F,Baris S Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. . 2023; 236 - 249. 10.5578/tt.20239705
IEEE	karabiber e,atik ö,Tepetam F,Ergan B,Ilki A,Karakoc-Aydiner E,OZEN A,Özyer F,Baris S "Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines." , ss.236 - 249, 2023. 10.5578/tt.20239705
ISNAD	karabiber, esra vd. "Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines". (2023), 236-249. https://doi.org/10.5578/tt.20239705

APA	karabiber e, atik ö, Tepetam F, Ergan B, Ilki A, Karakoc-Aydiner E, OZEN A, Özyer F, Baris S (2023). Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. Tüberküloz ve Toraks, 71(3), 236 - 249. 10.5578/tt.20239705
Chicago	karabiber esra,atik özge,Tepetam Fatma Merve,Ergan Bilgehan,Ilki Arzu,Karakoc-Aydiner Elif,OZEN AHMET,Özyer Fatma,Baris Safa Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. Tüberküloz ve Toraks 71, no.3 (2023): 236 - 249. 10.5578/tt.20239705
MLA	karabiber esra,atik özge,Tepetam Fatma Merve,Ergan Bilgehan,Ilki Arzu,Karakoc-Aydiner Elif,OZEN AHMET,Özyer Fatma,Baris Safa Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. Tüberküloz ve Toraks, vol.71, no.3, 2023, ss.236 - 249. 10.5578/tt.20239705
AMA	karabiber e,atik ö,Tepetam F,Ergan B,Ilki A,Karakoc-Aydiner E,OZEN A,Özyer F,Baris S Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. Tüberküloz ve Toraks. 2023; 71(3): 236 - 249. 10.5578/tt.20239705
Vancouver	karabiber e,atik ö,Tepetam F,Ergan B,Ilki A,Karakoc-Aydiner E,OZEN A,Özyer F,Baris S Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines. Tüberküloz ve Toraks. 2023; 71(3): 236 - 249. 10.5578/tt.20239705
IEEE	karabiber e,atik ö,Tepetam F,Ergan B,Ilki A,Karakoc-Aydiner E,OZEN A,Özyer F,Baris S "Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines." Tüberküloz ve Toraks, 71, ss.236 - 249, 2023. 10.5578/tt.20239705
ISNAD	karabiber, esra vd. "Clinical and immunological outcomes of SARS-CoV-2 infection in patients with inborn errors of immunity receiving different brands and doses of COVID-19 vaccines". Tüberküloz ve Toraks 71/3 (2023), 236-249. https://doi.org/10.5578/tt.20239705