Free access

COVID-19 outcomes in immunocompromised individuals: seroconversion and vaccine effectiveness

Publication: LymphoSign Journal
23 May 2022
As we round the corner on the 6th coronavirus disease 2019 (COVID-19) wave amid gradual lifting of social distancing and masking restrictions, it is timely to review the guidance measures for individuals with compromised immune systems, particularly those with primary immunodeficiency (PID) (Roifman 2020). The clinical spectrum of COVID-19 varies from those who are asymptomatic, experience mild symptoms such as fever, cough, and dyspnea, to more severe outcomes including acute respiratory distress, pneumonia, renal failure, and death. Comorbidities predisposing to complications and severe illness include older age (>65 y), males, obesity, cancer, serious cardiovascular disease, chronic obstructive pulmonary disease, type II diabetes mellitus, and immunodeficiency (including PID) (Chen et al. 2020; Huang et al. 2020; Li et al. 2020).
Over the past 2 years since the pandemic took hold, those with PID have been advised to practice rigorous social distancing, hand hygiene, and if appropriate — COVID-19 vaccination, given the possibility of more severe outcomes (Roifman and Vong 2021b, 2021a). During this period, studies examining the effectiveness of the COVID-19 vaccine and longevity of antibody titers have been instrumental in guiding the need for additional ‘boosters’, allowing for additional protection due to insufficient seroconversion — the development of specific antibodies following vaccination (or exposure to an infectious agent), or waning immunity. In Canada, individuals with moderate to severe PID have been advised to a receive 3-dose primary series with the Pfizer-BioNTech mRNA vaccine (or a 2-dose primary series using the Moderna adenoviral vector-based vaccine), and 2 booster doses — up to 5 doses in total.
Early clinical trials demonstrated the safety and efficacy of mRNA and adenoviral-vector based COVID-19 vaccines, including against symptomatic SARS-CoV-2 infection and more severe outcomes (Baden et al. 2021; Voysey et al. 2021). Seroconversion was shown to be high regardless of the type of vaccine administered (Eyre et al. 2021; Wang et al. 2021). Further, several studies supported the use of neutralizing antibody titers as surrogate markers of protection (Khoury et al. 2021; Garcia-Beltran et al. 2021). However, such data rarely extrapolate to subpopulations with immune deficits especially given that immunocompromised individuals were excluded from evaluations of vaccine effectiveness. In Canada, 4–5 times more immunocompromised individuals, including those on immunosuppressive medications, solid organ transplant recipients, malignancy, and PID, have been hospitalized or admitted to hospital with COVID-19 than the general population (NACI 2021).
More recently, case series and reports of disease course in those with PID indicate variable outcomes, from those who remain asymptomatic to severe complications. Nevertheless, seroconversion rates remain lower than the general population suggesting the need for continued caution.
There remains limited data on efficacy following the 3-dose vaccine primary series in PID, with most studies reporting outcomes following a 2-dose schedule. This likely reflects the initial lack of access to sufficient doses/boosters of COVID-19 vaccines globally and the lag time during transition from a 2-dose to 3-dose schedule. In a U.S. study, among 100 immunocompromised individuals who received a 2-dose mRNA vaccine, half were able to produce an antibody-mediated (humoral) immune response while 69% raised a cell-mediated (interferon-γ release) response (Ramanathan et al. 2021). Separately, an Italian study reported that 7 out of 34 (20%) patients with common variable immunodeficiency (CVID) with no prior exposure to SARS-COV-2 were able to produce IgG and IgA antibody responses to the COVID-19 vaccine spike protein, while 6 out of 7 who had previously been infected showed boosted antibody responses after vaccination. Spike protein antibodies were absent in patients with X-linked agammaglobulinemia, although reassuringly, in 5 out of 6 of this cohort, vaccination specific T cell responses were still detectable (Salinas et al. 2021). Similarly, an Israeli study of 26 patients with PID reported that 18 were able to develop specific antibody responses following the Pfizer-BioNtech COVID-19 vaccine, while 19 raised specific T cell responses (Hagin et al. 2021). Overall, a recent meta-analysis assessing seroconversion rates among immunocompromised individuals reported significantly lower rates between the first and second dose of the vaccine (Lee et al. 2022). A third dose boosted antibody levels, although some may not respond to a fourth dose.
Real-world data describing the severity and level of protection following vaccination against COVID-19 in patients with PID continue to emerge, and paint a conflicting scenario. It is noteworthy that, given the assumption of severe outcomes, many with PID have remained vigilant in sheltering from exposure, resulting in relatively low infection rates. Further, the presence of COVID antibodies in antibody replacement products likely confer some additional level of protection (Karbiener et al. 2021; Romero et al. 2021). Some regions have documented only mild COVID-19 symptoms (Drabe et al. 2021; Goudouris et al. 2021; Deyà-Martínez et al. 2021), perhaps due to the innate inability of those with PID to mobilize inflammatory responses. Marcus and colleagues reported minimal impact of COVID-19 in a cohort of 19 patients with PID from Israel — none were hospitalized (Marcus et al. 2021). However, with a high proportion of asymptomatic cases and most on antibody replacement therapy, this cohort is hard to assess. Our own experience with a cohort of pediatric patients (including those with humoral immunodeficiency, combined immunodeficiency and phagocytic defects) revealed similarly mild COVID-19 disease course (fever, sore throat, nasal congestion, and rhinitis) which resolved without complications (Roifman et al. unpublished observations).
In contrast, globally, overall rates of hospital admissions stand at closer to 50% of reported PID cases of COVID-19 (Fill et al. 2020; Van Damme et al. 2020; Soresina et al. 2020; Ahanchian et al. 2020; Jin et al. 2020; Quinti et al. 2020; Delavari et al. 2020; Ho et al. 2021; Mullur et al. 2021; Meyts et al. 2021; Esenboga et al. 2021; Shields et al. 2021; Castano-Jaramillo et al. 2021; Goudouris et al. 2021). Shields and colleagues reported the outcome of 60 patients with PID, with just over half requiring hospital admission and overall higher case fatality ratios compared to control (Shields et al. 2021). A study by Delavari and colleagues reported 10-fold higher mortality rate in those with PID compared to the general population, despite only 1.23-fold higher COVID-19 infection (Delavari et al. 2020). What is clear is that a more severe clinical course is documented in patients with defects in type I interferon signaling (Bastard et al. 2020; van der Made et al. 2020; Zhang et al. 2020), including those with defects in IFNAR1, IFNAR2, STAT1, STAT2, TICAM1, TRAF3, TBK1, TLR3, and IRF3.
It would be of paramount importance to obtain stratified data on the impact of COVID-19 over the 2-year period of the pandemic. Currently, patients with PID are more protected now with an effective vaccine, effective anti-viral treatments, and gradual enrichment of immunoglobulin products with neutralizing anti-SARS-CoV-2 antibodies.
We propose to differentiate between PID patients who responded well to vaccination with sustained antibody levels and/or those receiving immunoglobulin replacement, from non-responders, especially if they have significant T cell deficiency or an interferon-γ pathway defect.
We also believe that after a prolonged period of home schooling for children with PID, further extension of this practice may be more harmful than exposure to the virus. We recommend that with the advice and guidance of an immunologist, many of these children could relatively safely attend physical school. Yet, we still advise they adhere to masking at school, hand hygiene, and distancing as much as possible. The introduction of new preventative and therapeutic medications renders this transition to normal life easier.
In summary, despite gradual lifting of COVID-19 mandates, continued evidence of impaired immunity and COVID-19 disease course in individuals with PID indicate that this population should continue to remain cautious — but with gradual and selective relaxation of practices.

REFERENCES

Ahanchian H., Moazzen N., Sezavar M., Khalighi N., Khoshkhui M., Aelami M.H., Motevalli Haghi N.S., and Rezaei N. 2020. COVID-19 in a child with primary antibody deficiency. Clin Case Rep 9: 755–758.
Baden L.R., El Sahly H.M., Essink B., Kotloff K., Frey S., Novak R., Diemert D., Spector S.A., Rouphael N., Creech C.B., Mcgettigan J., Khetan S., Segall N., Solis J., Brosz A., Fierro C., Schwartz H., Neuzil K., Corey L., Gilbert P., Janes H., Follmann D., Marovich M., Mascola J., Polakowski L., Ledgerwood J., Graham B.S., Bennett H., Pajon R., Knightly C., Leav B., Deng W., Zhou H., Han S., Ivarsson M., Miller J., and Zaks T. 2021. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N. Engl. J. Med. 384: 403–416.
Bastard P., Rosen L.B., Zhang Q., Michailidis E., Hoffmann H.-H., Zhang Y., Dorgham K., Philippot Q., Rosain J., Béziat V., Manry J., Shaw E., Haljasmägi L., Peterson P., Lorenzo L., Bizien L., Trouillet-Assant S., Dobbs K., De Jesus A.A., Belot A., Kallaste A., Catherinot E., Tandjaoui-Lambiotte Y., Le Pen J., Kerner G., Bigio B., Seeleuthner Y., Yang R., Bolze A., Spaan A.N., Delmonte O.M., Abers M.S., Aiuti A., Casari G., Lampasona V., Piemonti L., Ciceri F., Bilguvar K., Lifton R.P., Vasse M., Smadja D.M., Migaud M., Hadjadj J., Terrier B., Duffy D., Quintana-Murci L., Van De Beek D., Roussel L., Vinh D.C., Tangye S.G., Haerynck F., Dalmau D., Martinez-Picado J., Brodin P., Nussenzweig M.C., Boisson-Dupuis S., Rodríguez-Gallego C., Vogt G., Mogensen T.H., Oler A.J., Gu J., Burbelo P.D., Cohen J.I., Biondi A., Bettini L.R., D’angio M., Bonfanti P., Rossignol P., Mayaux J., Rieux-Laucat F., Husebye E.S., Fusco F., Ursini M.V., Imberti L., Sottini A., Paghera S., Quiros-Roldan E., Rossi C., Castagnoli R., Montagna D., Licari A., Marseglia G.L., Duval X., Ghosn J., Tsang J.S., Goldbach-Mansky R., Kisand K., Lionakis M.S., Puel A., Zhang S.-Y., Holland S.M., Gorochov G., Jouanguy E., Rice C.M., Cobat A., Notarangelo L.D., Abel L., Su H.C., and Casanova J.-L. 2020. Autoantibodies against type I IFNs in patients with life-threatening COVID-19. Science, 370: eabd4585.
Castano-Jaramillo L.M., Yamazaki-Nakashimada M.A., O’farrill-Romanillos P.M., Muzquiz Zermeño D., Scheffler Mendoza S.C., Venegas Montoya E., García Campos J.A., Sánchez-Sánchez L.M., Gámez González L.B., Ramírez López J.M., Bustamante Ogando J.C., Vásquez-Echeverri E., Medina Torres E.A., Lopez-Herrera G., Blancas Galicia L., Berrón Ruiz L., Staines-Boone A.T., Espinosa-Padilla S.E., Segura Mendez N.H., and Lugo Reyes S.O. 2021. COVID-19 in the Context of Inborn Errors of Immunity: A Case Series of 31 Patients from Mexico. J. Clinical Immunol. 41: 1463–1478.
Chen N., Zhou M., Dong X., Qu J., Gong F., Han Y., Qiu Y., Wang J., Liu Y., Wei Y., Xia J., Yu T., Zhang X., and Zhang L. 2020. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study. Lancet, 395: 507–513.
Delavari S., Abolhassani H., Abolnezhadian F., Babaha F., Iranparast S., Ahanchian H., Moazzen N., Nabavi M., Arshi S., Fallahpour M., Bemanian M.H., Shokri S., Momen T., Sadeghi-Shabestari M., Molatefi R., Shirkani A., Vosughimotlagh A., Safarirad M., Sharifzadeh M., Pashangzadeh S., Salami F., Shirmast P., Rezaei A., Moeini Shad T., Mohraz M., Rezaei N., Hammarström L., Yazdani R., and Aghamohamamdi A. 2020. Impact of SARS-CoV-2 Pandemic on Patients with Primary Immunodeficiency. J. Clinical Immunol. 41: 345–355.
Deyà-Martínez A., García-García A., Gonzalez-Navarro E.A., Yiyi L., Vlagea A., Jordan I., Fumadó V., Fortuny C., Español M., Launes C., Esteve-Solé A., Juan M., Pascal M., and Alsina L. 2021. COVID-19 in children and young adults with moderate/severe inborn errors of immunity in a high burden area in pre-vaccine era. Clinical Immunol. 230: 108821.
Drabe C.H., Hansen A.-B.E., Rasmussen L.D., Larsen O.D., Møller A., Mogensen T.H., Helweg-Larsen J., and Katzenstein T.L. 2021. Low morbidity in Danish patients with common variable immunodeficiency disorder infected with severe acute respiratory syndrome coronavirus 2. Infect Dis (Auckl), pp. 1–6.
Esenboga S., Ocak M., Akarsu A., Bildik H.N., Cagdas D., Iskit A.T., and Tezcan I. 2021. COVID-19 in Patients with Primary Immunodeficiency. J. Clinical Immunol. 41: 1515–1522.
Eyre D.W., Lumley S.F., Wei J., Cox S., James T., Justice A., Jesuthasan G., O’donnell D., Howarth A., Hatch S.B., Marsden B.D., Jones E.Y., Stuart D.I., Ebner D., Hoosdally S., Crook D.W., Peto T.E.A., Walker T.M., Stoesser N.E., Matthews P.C., Pouwels K.B., Walker A.S., and Jeffery K. 2021. Quantitative SARS-CoV-2 anti-spike responses to Pfizer–BioNTech and Oxford–AstraZeneca vaccines by previous infection status. Clinical Microbiol. Infection, 27: 1516.e7–1516.e14.
Fill L., Hadney L., Graven K., Persaud R., and Hostoffer R. 2020. The clinical observation of a patient with common variable immunodeficiency diagnosed as having coronavirus disease 2019. Annal. Allergy, Asthma Immunol. 125: 112–114.
Garcia-Beltran W.F., Lam E.C., Astudillo M.G., Yang D., Miller T.E., Feldman J., Hauser B.M., Caradonna T.M., Clayton K.L., Nitido A.D., Murali M.R., Alter G., Charles R.C., Dighe A., Branda J.A., Lennerz J.K., Lingwood D., Schmidt A.G., Iafrate A.J., and Balazs A.B. 2021. COVID-19-neutralizing antibodies predict disease severity and survival. Cell, 184: 476–488.e11.
Goudouris E.S., Pinto-Mariz F., Mendonça L.O., Aranda C.S., Guimarães R.R., Kokron C., Barros M.T., Anísio F., Alonso M.L.O., Marcelino F., Valle S.O.R., Junior S.D., Barreto I.D.P., Ferreira J.F.S., Roxo-Junior P., Do Rego Silva A.M., Campinhos F.L., Bonfim C., Loth G., Fernandes J.F., Garcia J.L., Capelo A., Takano O.A., Nadaf M.I.V., Toledo E.C., Cunha L.A.O., Di Gesu R.S.W., Schidlowski L., Fillipo P., Bichuetti-Silva D.C., Soldateli G., Ferraroni N.R., De Oliveira Dantas E., Pestana S., Mansour E., Ulaf R.G., Prando C., Condino-Neto A., and Grumach A.S. 2021. Outcome of SARS-CoV-2 Infection in 121 Patients with Inborn Errors of Immunity: A Cross-Sectional Study. J. Clinical Immunol. 41(7): 1479–1489.
Hagin D., Freund T., Navon M., Halperin T., Adir D., Marom R., Levi I., Benor S., Alcalay Y., and Freund N.T. 2021. Immunogenicity of Pfizer-BioNTech COVID-19 vaccine in patients with inborn errors of immunity. J. Allergy Clinical Immunol. 148: 739–749.
Ho H.-E., Mathew S., Peluso M.J., and Cunningham-Rundles C. 2021. Clinical outcomes and features of COVID-19 in patients with primary immunodeficiencies in New York City. The J. Allergy Clinical Immunol.: In Practice, 9: 490–493.e2.
Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y., Zhang L., Fan G., Xu J., Gu X., Cheng Z., Yu T., Xia J., Wei Y., Wu W., Xie X., Yin W., Li H., Liu M., Xiao Y., Gao H., Guo L., Xie J., Wang G., Jiang R., Gao Z., Jin Q., Wang J., and Cao B. 2020. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 395: 497–506.
Jin H., Reed J.C., Liu S.T.H., Ho H.-E., Lopes J.P., Ramsey N.B., Waqar O., Rahman F., Aberg J.A., Bouvier N.M., Cunningham-Rundles C., Liu S.T.H., Lin H.-M., Abrams-Downey A., Cascetta K.P., Glatt A.E., Koshy S.C., Kojic E., Mazo D.S., Perlman D., Rudolph S., Steinberg J., Schneider T., Baine I., Wajnberg A., Gumprecht J.P., Rahman F., Rodriguez D., Sanky C., Dupper A., Altman D.R., Krammer F., Mendu D.R., Firpo-Betancourt A., Cordon-Cardo C., Jhang J.S., Arinsberg S.A., Reich D.L., Aberg J.A., and Bouvier N.M. 2020. Three patients with X-linked agammaglobulinemia hospitalized for COVID-19 improved with convalescent plasma. J. Allergy Clinical Immunol.: In Practice, 8: 3594–3596.e3.
Karbiener M., Farcet M.R., Schwaiger J., Powers N., Lenart J., Stewart J.M., Tallman H., and Kreil T.R. 2021. Highly Potent SARS-CoV-2 Neutralization by Intravenous Immunoglobulins manufactured from Post-COVID-19 and COVID-19-Vaccinated Plasma Donations. J. Infect. Dis. 224(10): 1707–1711.
Khoury D.S., Cromer D., Reynaldi A., Schlub T.E., Wheatley A.K., Juno J.A., Subbarao K., Kent S.J., Triccas J.A., and Davenport M.P. 2021. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat. Med. 27: 1205–1211.
Lee A.R.Y.B., Wong S.Y., Chai L.Y.A., Lee S.C., Lee M.X., Muthiah M.D., Tay S.H., Teo C.B., Tan B.K.J., Chan Y.H., Sundar R., and Soon Y.Y. 2022. Efficacy of covid-19 vaccines in immunocompromised patients: systematic review and meta-analysis. BMJ, 376: e068632.
Li Q., Guan X., Wu P., Wang X., Zhou L., Tong Y., Ren R., Leung K.S.M., Lau E.H.Y., Wong J.Y., Xing X., Xiang N., Wu Y., Li C., Chen Q., Li D., Liu T., Zhao J., Liu M., Tu W., Chen C., Jin L., Yang R., Wang Q., Zhou S., Wang R., Liu H., Luo Y., Liu Y., Shao G., Li H., Tao Z., Yang Y., Deng Z., Liu B., Ma Z., Zhang Y., Shi G., Lam T.T.Y., Wu J.T., Gao G.F., Cowling B.J., Yang B., Leung G.M., and Feng Z. 2020. Early Transmission Dynamics in Wuhan, China, of Novel Coronavirus-Infected Pneumonia. N. Engl. J. Med. 382: 1199–1207.
Marcus N., Frizinsky S., Hagin D., Ovadia A., Hanna S., Farkash M., Maoz-Segal R., Agmon-Levin N., Broides A., Nahum A., Rosenberg E., Kuperman A.A., Dinur-Schejter Y., Berkun Y., Toker O., Goldberg S., Confino-Cohen R., Scheuerman O., Badarneh B., Epstein-Rigbi N.A., Etzioni A., Dalal I., and Somech R. 2021. Minor clinical impact of COVID-19 pandemic on patients with primary immunodeficiency in Israel. Front. Immunol. 11: 614086.
Meyts I., Bucciol G., Quinti I., Neven B., Fischer A., Seoane E., Lopez-Granados E., Gianelli C., Robles-Marhuenda A., Jeandel P.-Y., Paillard C., Sankaran V.G., Demirdag Y.Y., Lougaris V., Aiuti A., Plebani A., Milito C., Dalm V.A.S.H., Guevara-Hoyer K., Sánchez-Ramón S., Bezrodnik L., Barzaghi F., Gonzalez-Granado L.I., Hayman G.R., Uzel G., Mendonça L.O., Agostini C., Spadaro G., Badolato R., Soresina A., Vermeulen F., Bosteels C., Lambrecht B.N., Keller M., Mustillo P.J., Abraham R.S., Gupta S., Ozen A., Karakoc-Aydiner E., Baris S., Freeman A.F., Yamazaki-Nakashimada M., Scheffler-Mendoza S., Espinosa-Padilla S., Gennery A.R., Jolles S., Espinosa Y., Poli M.C., Fieschi C., Hauck F., Cunningham-Rundles C., Mahlaoui N., Warnatz K., Sullivan K.E., and Tangye S.G. 2021. Coronavirus disease 2019 in patients with inborn errors of immunity: An international study. J. Allergy Clinical Immunol. 147: 520–531.
Mullur J., Wang A., and Feldweg A. 2021. A fatal case of coronavirus disease 2019 in a patient with common variable immunodeficiency. Annal. Allergy Asthma Immunol. 126: 90–92.
NACI. 2021. National Advisory Committee on Immunization (NACI) rapid response: Additional dose of COVID-19 vaccine in immunocompromised individuals following 1- or 2- dose primary series, Public Health Agency of Canada, Ottawa ON [Online]. Available from https://www.canada.ca/en/public-health/services/immunization/national-advisory-committee-on-immunization-naci/statement-september-10-2021-additional-dose-covid-19-vaccine-immunocompromised-following-1-2-dose-series.html.
Quinti I., Lougaris V., Milito C., Cinetto F., Pecoraro A., Mezzaroma I., Mastroianni C.M., Turriziani O., Bondioni M.P., Filippini M., Soresina A., Spadaro G., Agostini C., Carsetti R., and Plebani A. 2020. A possible role for B cells in COVID-19? Lesson from patients with agammaglobulinemia. J. Allergy Clinical Immunol. 146: 211–213.e4.
Ramanathan M., Murugesan K., Yang L.M., Costales C., Bulterys P.L., Schroers-Martin J., Alizadeh A.A., Boyd S.D., Brown J.M., Nadeau K.C., Nadimpalli S.S., Wang A.X., Busque S., Pinsky B.A., and Banaei N. 2021. Cell-Mediated and Humoral Immune Response to 2-Dose SARS-CoV2 mRNA vaccination in Immunocompromised patient population. medRxiv, 2021.07.21.21260921.
Roifman C.M. 2020. Managing primary immunodeficiency during the COVID-19 pandemic. LymphoSign J. 7: 85–89.
Roifman C.M. and Vong L. 2021a. COVID-19 post-vaccination recommendations in primary immunodeficiency. LymphoSign J. 12: 21526567211056239.
Roifman D.C.M. and Vong D.L. 2021b. COVID-19 post-vaccination recommendations in primary immunodeficiency. LymphoSign J. 8(3).
Romero C., Díez J.M., and Gajardo R. 2021. Anti-SARS-CoV-2 antibodies in healthy donor plasma pools and IVIG products. Lancet Infect. Dis. 21: 765–766.
Salinas A.F., Mortari E.P., Terreri S., Quintarelli C., Pulvirenti F., Di Cecca S., Guercio M., Milito C., Bonanni L., Auria S., Romaggioli L., Cusano G., Albano C., Zaffina S., Perno C.F., Spadaro G., Locatelli F., Carsetti R., and Quinti I. 2021. SARS-CoV-2 vaccine induced atypical immune responses in antibody defects: everybody does their best. J. Clinical Immunol. 41: 1709–1722.
Shields A.M., Burns S.O., Savic S., Richter A.G., Anantharachagan A., Arumugakani G., Baker K., Bahal S., Bermingham W., Bhole M., Boules E., Bright P., Burns S., Cleave B., Dempster J., Devlin L., Dhalla F., Drewe E., Duncan C., Dziadzio M., Elkhalifa S., Gennery A., Goddard S., Grigoriadou S., Hayman G., Herwadkar A., Huissoon A., Jain R., Jolles S., Johnston S., Leeman L., Mahabir S., Maclochlainn D., Mcdermott E., Misbah S., Morsi H., Murng S., Noorani S., O’brien R., Patel S., Price A., Richter A., Savic S., Seneviratne S., Shields A., Shrimpton A., Stroud C., Vaitla P., and Verma N. 2021. COVID-19 in patients with primary and secondary immunodeficiency: the United Kingdom experience. J. Allergy Clinical Immunol., 147: 870–875.e1.
Soresina A., Moratto D., Chiarini M., Paolillo C., Baresi G., Focà E., Bezzi M., Baronio B., Giacomelli M., Badolato R., and Eigenmann P. 2020. Two X-linked agammaglobulinemia patients develop pneumonia as COVID-19 manifestation but recover. Pediatric Allergy Immunol. 31: 565–569.
Van Damme K.F.A., Tavernier S., Van Roy N., De Leeuw E., Declercq J., Bosteels C., Maes B., DE Bruyne M., Bogaert D., Bosteels V., Hoste L., Naesens L., Maes P., Grifoni A., Weiskopf D., Sette A., Depuydt P., Van Braeckel E., Haerynck F., and Lambrecht B.N. 2020. Case Report: convalescent plasma, a targeted therapy for patients with cvid and severe COVID-19. Front. Immunol. 11.
Van Der Made C.I., Simons A., Schuurs-Hoeijmakers J., Van Den Heuvel G., Mantere T., Kersten S., Van Deuren R.C., Steehouwer M., Van Reijmersdal S.V., Jaeger M., Hofste T., Astuti G., Corominas Galbany J., Van Der Schoot V., Van Der Hoeven H., Hagmolen of Ten Have W., Klijn E., Van Den Meer C., Fiddelaers J., De Mast Q., Bleeker-Rovers C.P., Joosten L.A.B., Yntema H.G., Gilissen C., Nelen M., Van Der Meer J.W.M., Brunner H.G., Netea M.G., Van De Veerdonk F.L., and Hoischen A. 2020. Presence of genetic variants among young men with severe COVID-19. Jama, 324: 663.
Voysey M., Clemens S.A.C., Madhi S.A., Weckx L.Y., Folegatti P.M., Aley P.K., Angus B., Baillie V.L., Barnabas S.L., Bhorat Q.E., Bibi S., Briner C., Cicconi P., Collins A.M., Colin-Jones R., Cutland C.L., Darton T.C., Dheda K., Duncan C.J.A., Emary K.R.W., Ewer K.J., Fairlie L., Faust S.N., Feng S., Ferreira D.M., Finn A., Goodman A.L., Green C.M., Green C.A., Heath P.T., Hill C., Hill H., Hirsch I., Hodgson S.H.C., Izu A., Jackson S., Jenkin D., Joe C.C.D., Kerridge S., Koen A., Kwatra G., Lazarus R., Lawrie A.M., Lelliott A., Libri V., Lillie P.J., Mallory R., Mendes A.V.A., Milan E.P., Minassian A.M., Mcgregor A., Morrison H., Mujadidi Y.F., Nana A., O’reilly P.J., Padayachee S.D., Pittella A., Plested E., Pollock K.M., Ramasamy M.N., Rhead S., Schwarzbold A.V., Singh N., Smith A., Song R., Snape M.D., Sprinz E., Sutherland R.K., Tarrant R., Thomson E.C., Török M.E., Toshner M., Turner D.P.J., Vekemans J., Villafana T.L., Watson M.E.E., Williams C.J., Douglas A.D., Hill A.V.S., Lambe T., Gilbert S.C., Pollard A.J., Aban M., Abayomi F., Abeyskera K., Aboagye J., Adam M., Adams K., Adamson J., Adelaja Y.A., Adewetan G., Adlou S., Ahmed K., Akhalwaya Y., Akhalwaya S., Alcock A., Ali A., Allen E.R., Allen L., and Almeida T.C.D.S.C. 2021. Safety and efficacy of the ChAdOx1 nCoV-19 vaccine (AZD1222) against SARS-CoV-2: an interim analysis of four randomised controlled trials in Brazil, South Africa, and the UK. Lancet, 397: 99–111.
Wang Z., Schmidt F., Weisblum Y., Muecksch F., Barnes C.O., Finkin S., Schaefer-Babajew D., Cipolla M., Gaebler C., Lieberman J.A., Oliveira T.Y., Yang Z., Abernathy M.E., Huey-Tubman K.E., Hurley A., Turroja M., West K.A., Gordon K., Millard K.G., Ramos V., Da Silva J., Xu J., Colbert R.A., Patel R., Dizon J., Unson-O’brien C., Shimeliovich I., Gazumyan A., Caskey M., Bjorkman P.J., Casellas R., Hatziioannou T., Bieniasz P.D., and Nussenzweig M.C. 2021. mRNA vaccine-elicited antibodies to SARS-CoV-2 and circulating variants. Nature, 592: 616–622.
Zhang Q., Bastard P., Liu Z., Le Pen J., Moncada-Velez M., Chen J., Ogishi M., Sabli I.K.D., Hodeib S., Korol C., Rosain J., Bilguvar K., Ye J., Bolze A., Bigio B., Yang R., Arias A.A., Zhou Q., Zhang Y., Onodi F., Korniotis S., Karpf L., Philippot Q., Chbihi M., Bonnet-Madin L., Dorgham K., Smith N., Schneider W.M., Razooky B.S., Hoffmann H.-H., Michailidis E., Moens L., Han J.E., Lorenzo L., Bizien L., Meade P., Neehus A.-L., Ugurbil A.C., Corneau A., Kerner G., Zhang P., Rapaport F., Seeleuthner Y., Manry J., Masson C., Schmitt Y., Schlüter A., Le Voyer T., Khan T., Li J., Fellay J., Roussel L., Shahrooei M., Alosaimi M.F., Mansouri D., Al-Saud H., Al-Mulla F., Almourfi F., Al-Muhsen S.Z., Alsohime F., Al Turki S., Hasanato R., Van De Beek D., Biondi A., Bettini L.R., D’angio’ M., Bonfanti P., Imberti L., Sottini A., Paghera S., Quiros-Roldan E., Rossi C., Oler A.J., Tompkins M.F., Alba C., Vandernoot I., Goffard J.-C., Smits G., Migeotte I., Haerynck F., Soler-Palacin P., Martin-Nalda A., Colobran R., Morange P.-E., Keles S., Çölkesen F., Ozcelik T., Yasar K.K., Senoglu S., Karabela Ş.N., Rodríguez-Gallego C., Novelli G., Hraiech S., Tandjaoui-Lambiotte Y., Duval X., Laouénan C., Snow A.L., Dalgard C.L., Milner J.D., and Vinh D.C. 2020. Inborn errors of type I IFN immunity in patients with life-threatening COVID-19. Science, 370: eabd4570.

Information & Authors

Information

Published In

cover image LymphoSign Journal
LymphoSign Journal
Volume 9Number 2June 2022
Pages: 33 - 39

History

Received: 12 May 2022
Accepted: 15 May 2022
Accepted manuscript online: 23 May 2022
Version of record online: 23 May 2022

Authors

Affiliations

Linda Vong, PhD [email protected]
Canadian Centre for Primary Immunodeficiency and the Division of Immunology & Allergy, Department of Paediatrics, The Hospital for Sick Children, Toronto, ON
Chaim M. Roifman, CM, MD, FRCPC, FCACB
Canadian Centre for Primary Immunodeficiency and the Division of Immunology & Allergy, Department of Paediatrics, The Hospital for Sick Children, Toronto, ON
University of Toronto, Toronto, ON.

Metrics & Citations

Metrics

Other Metrics

Citations

Cite As

Export Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

View Options

View options

PDF

View PDF

Get Access

Login options

Check if you access through your login credentials or your institution to get full access on this article.

Subscribe

Click on the button below to subscribe to LymphoSign Journal

Purchase options

Purchase this article to get full access to it.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

Media

Media

Other

Tables

Share Options

Share

Share the article link

Share on social media