PREVALENCE OF SARS-COV-2-IGG ANTIBODIES IN CHILDREN WITH CKD OR IMMUNOSUPPRESSION
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CJASN ePress. Published on June 7, 2021 as doi: 10.2215/CJN.00330121 Prevalence of SARS-CoV-2-IgG Antibodies in Children with CKD or Immunosuppression Journal: Clinical Journal of the American Society of Nephrology Manuscript ID CJASN-0033-01-21.R2 Manuscript Type: Research Letters Date Submitted by the 15-Apr-2021 Author: Complete List of Authors: Morello, William; Fondazione IRCCS Cà Granda, Ospedale Maggiore Policlinico, Pediatric Nephrology, Dialysis and Transplant Unit Mastrangelo, Antonio; Fondazione IRCCS Cà Granda, Ospedale Maggiore Policlinico, Pediatric Nephrology, Dialysis and Transplant Unit Guzzo, Isabella; Bambino Gesù Children’s Hospital, IRCCS, Nephrology and Dialysis Unit, Pediatric Subspecialties Department Cusinato, Lisa; University Hospital of Padua, Pediatric Nephrology, Dialysis and Transplant Unit, Department of Women's and Children's Health Petruzzelli, Luigi; Santobono Children's Hospital, Pediatric Nephrology and Dialysis Unit Benvenuta, Chiara; Regina Margherita Children’s Hospital, AOU Città della Salute e della Scienza di Torino, Pediatric Nephrology Unit Martelli, Laura; Papa Giovanni XXIII Hospital, Paediatric Unit Dall'Amico, Roberto; Azienda per l'Assistenza Sanitaria n 5 Friuli Occidentale, Department of Pediatrics Vianello, Federica Alessandra; Fondazione IRCCS Cà Granda, Ospedale Maggiore Policlinico, Pediatric Nephrology, Dialysis and Transplant Unit Puccio, Giuseppe; University of Palermo, Department of Sciences for Health Promotion Massella, Laura; Bambino Gesù Children’s Hospital, IRCCS, Nephrology and Dialysis Unit, Pediatric Subspecialties Department Benetti, Elisa; University Hospital of Padua, Pediatric Nephrology, Dialysis and Transplant Unit, Department of Women's and Children's Health Pecoraro, Carmine; Santobono Children’s Hospital, Pediatric Nephrology and Dialysis Unit Peruzzi, Licia; Regina Margherita Children’s Hospital, AOU Città della Salute e della Scienza di Torino, Pediatric Nephrology Unit Montini, Giovanni; Fondazione IRCCS Cà Granda, Ospedale Maggiore Policlinico, Pediatric Nephrology, Dialysis and Transplant Unit; University of Milan, Department of Clinical Sciences and Community Health COVID-19, SARS-CoV-2 IgG, CKD, immunosuppression, children, chronic Keywords: kidney disease, idiopathic nephrotic syndrome Clinical Journal of the American Society of Nephrology
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Page 2 of 8 1 2 3 Authors: Morello, William; Mastrangelo, Antonio; Guzzo, Isabella; Cusinato, Lisa; Petruzzelli, Luigi; 4 Benvenuta, Chiara; Martelli, Laura; Dall'Amico, Roberto; Vianello, Federica Alessandra; Puccio, 5 6 Giuseppe; Massella, Laura; Benetti, Elisa; Pecoraro, Carmine; Peruzzi, Licia; Montini, Giovanni 7 8 Title: Prevalence of SARS-CoV-2-IgG Antibodies in Children with CKD or Immunosuppression 9 10 Running head: SARS-CoV-2-IgG in Italian Children with Chronic Nephropathies 11 12 Manuscript Type: Research Letters 13 14 15 Funders: “Associazione del Bambino Nefropatico (ABN onlus)â€, (Grant / Award Number: 'All 16 phases of this study were supported by the “') 17 “La rete del MaReâ€., (Grant / Award Number: 'All phases of this study were supported by the 18 “') 19 20 Financial Disclosure: No L. Annicchiarico Petruzzelli reports employment with Santobono Pausilipon. 21 22 R. Dall'Amico reports employment with Azienda Sanitaria Friuli Occidentale. 23 24 25 I. Guzzo reports employment with Bambino Gesù Children's Hospital. 26 27 L. Martelli reports employment with Ospedale Papa Giovanni XXIII, Bergamo. 28 29 L. Massella reports employment with Bambino Gesù Children's Hospital and Research Institute and 30 serving on the Editorial board of Nephron, section "Case Studies in Genetics." 31 32 33 A. Mastrangelo reports employment with Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico 34 Milano. 35 36 G. Montini reports consultancy agreements with Alnyalam and Bayern. 37 38 W. Morello reports employment with Pediatric Nephrology, Dialysis an Transplant Unit, 39 40 41 Fondazione IRCCS Ca''Granda, Ospedale Maggiore Policlinico Milano and receiving honoraria from 42 Sanofi-Genzyme. 43 44 L. Peruzzi reports employment with Regina Margherita Children's Hospital; Citta della Salute e della 45 Scienza di Torino and receiving honoraria from Alnylam, Chiesi, and Dicerna. 46 47 48 G. Puccio reports receiving honoraria from Associazione per il Bambino Nefropatico ABN-Onlus and 49 serving as a scientific advisor or member of EuroMediterranean Biomedical Journal. 50 51 The remaining authors have nothing to disclose. 52 53 Total number of words: 794 54 55 56 57 58 59 60 Clinical Journal of the American Society of Nephrology
Page 3 of 8 Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. 1 2 Prevalence of SARS-CoV-2 IgG Antibodies in Children with CKD or Immunosuppression 3 4 5 6 William Morello1*, Antonio Mastrangelo1*, Isabella Guzzo2, Lisa Cusinato 3, Luigi 7 8 Annicchiarico Petruzzelli4, Chiara Benvenuta5, Laura Martelli6, Roberto Dall'Amico7, Federica 9 10 Alessandra Vianello1, Giuseppe Puccio8, Laura Massella2, Elisa Benetti3, Carmine Pecoraro4, 11 12 Licia Peruzzi5, Giovanni Montini1,9 on behalf of the Italian Society of Pediatric Nephrology 13 14 15 * Contributed equally as co-first authors 16 17 18 19 Affiliations: 20 1. Pediatric Nephrology, Dialysis and Transplant Unit, Fondazione IRCCS Cà Granda, Ospedale 21 22 Maggiore Policlinico, Milan, Italy 23 24 2. Nephrology and Dialysis Unit, Pediatric Subspecialties Department, Bambino Gesù 25 26 Children’s Hospital, IRCCS, Rome, Italy. 27 3. Pediatric Nephrology, Dialysis and Transplant Unit, Department of Women's and Children's 28 29 Health, University Hospital of Padua, Italy 30 31 4. Pediatric Nephrology and Dialysis Unit Santobono Children’s Hospital, Naples, Italy 32 5. Pediatric Nephrology Unit, Regina Margherita Children’s Hospital, AOU Città della Salute e 33 34 della Scienza di Torino, Turin, Italy 35 36 6. Paediatric Unit, Papa Giovanni XXIII Hospital, Bergamo, Italy 37 38 7. Department of Pediatrics, Azienda per l'Assistenza Sanitaria n 5 Friuli Occidentale, 39 Pordenone, Italy. 40 41 8. Department of Sciences for Health Promotion, University of Palermo, Italy. 42 43 9. Department of Clinical Sciences and Community Health, University of Milan, Milan, Italy 44 45 46 Address correspondence to: Giovanni Montini, Pediatric Nephrology, Dialysis and Transplant 47 48 Unit, Fondazione IRCCS Ca’Granda, Ospedale Maggiore Policlinico, University of Milan, Via 49 50 della Commenda, 9, 20122, Milan, Italy. 51 Telephone: +39.02.5503.2883 52 53 Mail to: giovanni.montini@unimi.it 54 55 56 57 58 59 60 Clinical Journal of the American Society of Nephrology
Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. Page 4 of 8 1 2 COVID-19 TASK FORCE of the Italian Society of Pediatric Nephrology: 3 Licia Peruzzia (coordinator and president of the Italian Society of Pediatric Nephrology), Luigi 4 Annicchiarico Petruzzellib, Francesca Becheruccic, Elisa Benettid, Chiara Benevenutaa, Milena 5 Brugnarae, Luca Casadiof, Roberto Chimenzg, Giovanni Contig, Ciro Corradoh, Viviana 6 D’Agostinoi, Roberto Dall’Amicoj, Bruno Gianoglioa, Mario Giordanok, Chiara Gualenil, Stefano 7 8 Guarinom, Isabella Guzzon, Angela La Mannab, Claudio La Scolao, Laura Martellip, Laura 9 Massellan, Antonio Mastrangeloi, Marco Materassic, Giovanni Montini i,q, William Morelloi, 10 Antonello Panir, Teresa Papalias, Andrea Pasinio, Carmine Pecorarob, Piernicola Pellicciat, Marco 11 Pennesiu, Fabrizio Pugliesev, Ilse Maria Ratschv, Paola Romagnanic, Rosa Maria Ropertoc, Chiara 12 Tamburelloi, Gianluca Verginew, Antonio Vergorii, Federica Alessandra Vianellou, Enrico 13 Vidalx. 14 15 a. Pediatric Nephrology Unit, Regina Margherita Children’s Hospital, AOU Città della 16 Salute e della Scienza di Torino, Turin, Italy 17 b. Pediatric Nephrology and Dialysis Unit Santobono Children’s Hospital, Naples, Italy 18 c. Nephrology and Dialysis Unit, Meyer Children’s Hospital, Florence, Italy 19 d. Pediatric Nephrology, Dialysis and Transplant Unit, Department of Women's and 20 Children's Health, University Hospital of Padua, Italy. 21 e. Department of Surgical Sciences, Dentistry, Gynecology and Pediatrics, Pediatric 22 23 Division, University of Verona, Verona, Italy. 24 f. Pediatric Unit, Ravenna, Italy 25 g. Pediatric Nephrology and Rheumatology Unit with Dialysis, AOU G. Martino, Messina, 26 Italy. 27 h. Pediatric Nephrology Unit, Children’s Hospital ‘G. Di Cristina’, A.R.N.A.S. ‘Civico’, 28 Palermo, Italy. 29 i. Pediatric Nephrology, Dialysis and Transplant Unit, Fondazione IRCCS Cà Granda, 30 31 Ospedale Maggiore Policlinico, Milan, Italy 32 j. Department of Pediatrics, Azienda per l'Assistenza Sanitaria n 5 Friuli Occidentale, 33 Pordenone, Italy. 34 k. Nephrology Unit, Giovanni XXIII Children’s Hospital, Bari, Italy. 35 l. Department of Pediatrics, Azienda Ospedaliera Spedali Civili, Brescia, Italy 36 m. Department of Woman, Child and General and Specialized Surgery, Seconda Universita 37 38 degli Studi di Napoli, Napoli, Italy. 39 n. Nephrology and Dialysis Unit, Pediatric Subspecialties Department, Bambino Gesù 40 Children’s Hospital, IRCCS, Rome, Italy. 41 o. Nephrology and Dialysis Unit, Department of Pediatrics, Azienda Ospedaliero 42 Universitaria, Policlinico Sant’Orsola-Malpighi, Bologna, Italy. 43 p. Paediatric Unit, Papa Giovanni XXIII Hospital, Bergamo, Italy. 44 q. Department of Clinical Sciences and Community Health, University of Milan, Milan, 45 46 Italy 47 r. Struttura complessa di Nefrologia e Dialisi, Azienda Ospedaliera G. Brotzu, Cagliari, 48 Italy. 49 s. Annunziata Hospital, Cosenza, Italy 50 t. Department of Paediatrics, University of Chieti-Pescara, Chieti, Italy 51 u. Institute for Maternal and Child Health-IRCCS Burlo Garofolo, Trieste, Italy. 52 v. Department of Pediatrics, University of Ancona, Ancona, Italy. 53 54 w. Department of Pediatrics, Infermi Hospital Rimini, ASL Romagna, Italy. 55 x. Division of Pediatrics, Department of Medicine, University of Udine, Udine, Italy 56 57 58 59 60 Clinical Journal of the American Society of Nephrology
Page 5 of 8 Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. 1 2 Abbreviations: 3 SARS-CoV-2: Severe Acute Respiratory Syndrome Coronavirus 2 4 CKD: Chronic Kidney Disease 5 COVID-19: 2019 novel coronavirus disease 6 RT-PCR: Real Time Polymerase Chain Reaction 7 8 9 Manuscript word count: 794 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Clinical Journal of the American Society of Nephrology
Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. Page 6 of 8 1 2 Coronavirus Disease (COVID-19) rapidly spread from China as a pandemic, Italy being one of 3 4 the most affected Countries worldwide. Unlike adults, children have a milder presentation, even 5 when affected by Chronic Kidney Diseases (CKD) or on immunosuppressive therapy for 6 7 glomerulopathies and kidney transplantation1. In a nationwide study, by the Italian Society of 8 9 Pediatric Nephrology, involving 1572 pediatric patients with kidney diseases requiring 10 immunosuppressive treatment or CKD stages 3-5d, we have previously reported a low 11 12 prevalence (0.2%) of clinically detectable COVID-19 and no severe cases2. As asymptomatic 13 14 infections are common and the testing, early on in the pandemic, was restricted to a limited 15 16 number of children, we implemented a study in order to evaluate the prevalence of SARS-CoV- 17 2-IgG antibodies in the initial cohort. 18 19 The study population included two subgroups of children who were enrolled in our previous 20 21 study2. The Randomized group consisted of 200 children selected by random sampling, stratified 22 23 by geographical area, to be representative of the whole cohort. Testing was extended to their 24 siblings and cohabitants. The Symptomatic group included all 197 children who had reported 25 26 symptoms suggestive for a viral infection in the original cohort, including 29 subjects from the 27 28 Randomized group (Figure 1). 29 The serological testing for SARS-CoV-2-IgG was initiated 3 months after the clinical study and 30 31 was conducted from July 15th to September 15th, 2020, by a COVID-19 Rapid Test (Model: 32 33 GCCOV-402a). The test has a sensitivity of 93% and a specificity of 99% for IgG, compared to 34 35 Real Time Polymerase Chain Reaction (RT-PCR).3 The rate of seroprevalence was compared 36 with the pediatric report from the Italian Ministry of Health together with the Italian National 37 38 Institute of Statistics,4 and the clinical prevalence of our previous study.2 The study was approved 39 40 by the local Ethics Committees of each participating center. 41 42 As regards the randomized group, a total of 178 patients (median age 11 years), 90 siblings 43 (median age 10 years) and 271 cohabitants (median age 42 years) were tested. Twenty-two 44 45 families denied the consent and 85 cohabitants were not tested due to the restrictions in place for 46 47 the pandemic. Among the enrolled patients, 98 had a glomerular disease treated with 48 immunosuppressive agents (from 1 to 3), 36 were kidney transplant recipients, 32 had CKD and 49 50 12 were on dialysis. 29/178 had reported nonspecific infectious symptoms during the pandemic 51 52 peak. 53 54 A positive test for SARS-CoV-2-IgG was detected in 3/178 patients (1.7%), 6/90 (7%) siblings, 55 and 9/271 (3%) cohabitants. Only the difference between patients and siblings was statistically 56 57 significant (p=0.03; chi-square test). As expected, in the randomized group, patients who had 58 59 previously reported nonspecific infectious symptoms were more likely to be found positive, 60 Clinical Journal of the American Society of Nephrology
Page 7 of 8 Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. 1 2 compared to those who had not (2/29 vs 1/149; p=0.02; chi-square test). The seroprevalence in 3 4 asymptomatic patients was 0.7%. 5 Among the three positive patients, two were transplant recipients, with a history of fever and 6 7 upper respiratory tract infection respectively, and one was an asymptomatic child on 8 9 immunosuppression for idiopathic nephrotic syndrome. In all cases, SARS-CoV-2 infection was 10 not previously documented by swab RT-PCR testing. No child required hospitalization, 11 12 experienced multisystem inflammatory syndrome or worsening of renal function. 13 14 Furthermore, the percentage of children with kidney diseases who tested positive for SARS- 15 16 CoV-2-IgG in our sample was not statistically different from the corresponding Italian healthy 17 population aged 0-17 years (1.7% vs 2.2%; p=0.54; chi-square test).4 Similar to the general 18 19 Italian population,4 in our series the prevalence of humoral response was found to be 8.5 times 20 21 higher than the clinical prevalence of SARS-CoV-2 infection identified in our previous study 22 23 (1.7% vs 0.2%). 24 Overall, during the study we identified SARS-CoV-2 spreading in nine families, all living in the 25 26 most affected areas of Italy: Milan (6), Bergamo (2), and Turin (1). In four families only one 27 28 subject tested positive, none of which was the nephropathic child. This supports the low risk of 29 infection in our population. 30 31 Regarding the Symptomatic group, 161 of 197 children who reported symptoms (mainly upper 32 33 respiratory tract infections and fever) from our previous study were tested, including 29 subjects 34 35 from the Randomized group. Even in this population, potentially considered at higher risk of 36 previous SARS-CoV-2 infection, the seroprevalence was low, with only 6 children (4%) positive 37 38 for SARS-CoV-2-IgG. 39 40 The study has some limitations, such as the relatively small numbers and the timing when 41 42 serological testing was performed. However, since the humoral response to SARS-CoV-2 is 43 proven to last at least 4 months after infection5, our results should not be affected. 44 45 In conclusion, the serological assessment may detect previous asymptomatic infections, not 46 47 clinically identified. Nevertheless, the seroprevalence of SARS-CoV-2 antibodies in pediatric 48 patients with kidney diseases is low and similar to that of general pediatric population. 49 50 According to our data, we do not suggest reducing immunosuppressive therapy in this 51 52 population. Moreover, we do not recommend more stringent protective measures, compared to 53 54 healthy peers. 55 56 57 58 59 60 Clinical Journal of the American Society of Nephrology
Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. Page 8 of 8 1 2 Disclosures: 3 4 L. Annicchiarico Petruzzelli reports employment with Santobono Pausilipon. 5 R. Dall'Amico reports employment with Azienda Sanitaria Friuli Occidentale. 6 7 I. Guzzo reports employment with Bambino Gesù Children's Hospital. 8 9 L. Martelli reports employment with Ospedale Papa Giovanni XXIII, Bergamo. 10 L. Massella reports employment with Bambino Gesù Children's Hospital and Research Institute 11 12 and serving on the Editorial board of Nephron, section "Case Studies in Genetics." 13 14 A. Mastrangelo reports employment with Fondazione IRCCS Ca' Granda Ospedale Maggiore 15 16 Policlinico Milano. 17 G. Montini reports consultancy agreements with Alnyalam and Bayern. 18 19 W. Morello reports employment with Pediatric Nephrology, Dialysis an Transplant Unit, 20 21 Fondazione IRCCS Ca''Granda, Ospedale Maggiore Policlinico Milano and receiving honoraria 22 23 from Sanofi-Genzyme. 24 L. Peruzzi reports employment with Regina Margherita Children's Hospital; Citta della Salute e 25 26 della Scienza di Torino and receiving honoraria from Alnylam, Chiesi, and Dicerna. 27 28 G. Puccio reports receiving honoraria from Associazione per il Bambino Nefropatico ABN- 29 Onlus and serving as a scientific advisor or member of EuroMediterranean Biomedical Journal. 30 31 The remaining authors have nothing to disclose. 32 33 34 35 Funding: All phases of this study were supported by the “Associazione del Bambino 36 Nefropatico (ABN onlus)” and “La rete del MaRe”. 37 38 39 40 Acknowledgments: 41 42 A. Mastrangelo, G. Montini, W. Morello, and L. Peruzzi conceptualized and designed the study; 43 A. Mastrangelo and W.Morello designed the data collection instrument; G. Montini and L. 44 45 Peruzzi coordinated data collection; I. Guzzo, L. Cusinato, L. Annicchiarico Petruzzelli, C. 46 47 Benvenuta, L. Martelli, R. Dall'Amico, F.A. Vianello, L. Massella, E. Benetti, and C. Pecoraro 48 collected data; A. Mastrangelo, G. Montini, W. Morello, and L. Peruzzi supervised data 49 50 collection; G. Puccio performed statistical analysis; A. Mastrangelo and W. Morello drafted the 51 52 initial manuscript; L. Annicchiarico Petruzzelli, C. Benvenuta, E. Benetti, L. Cusinato, R. 53 54 Dall'Amico, I. Guzzo, L. Martelli, R, L. Massella, A. Mastrangelo, W. Morello, C. Pecoraro, G. 55 Puccio, and F.A. Vianello reviewed and revised the manuscript; G. Montini and L. Peruzzi 56 57 critically reviewed the manuscript for important intellectual content; and all authors approved the 58 59 final manuscript as submitted and agree to be accountable for all aspects of the work. 60 Clinical Journal of the American Society of Nephrology
Page 9 of 8 Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. 1 2 W. Morello and A. Mastrangelo contributed equally to this work as co-first authors. 3 4 5 Figure 1 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 Figure 1. Study population: The Randomized group included 200 children, selected by random 33 34 sampling, stratified by geographical area to be representative of the whole cohort. The 35 Symptomatic group included all children who had reported symptoms suggestive for a viral 36 37 infection during the previous study, for a total of 197 subjects. 29 enrolled patients belonged to 38 39 both groups. 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Clinical Journal of the American Society of Nephrology
Copyright 2021 by ASN, Published Ahead of Print on 6/7/21, Accepted/Unedited Version. Page 10 of 8 1 2 REFERENCES 3 4 5 1. Marlais M, Wlodkowski T, Vivarelli M, Pape L, Tönshoff B, Schaefer F, Tullus K: The 6 7 severity of COVID-19 in children on immunosuppressive medication. Lancet Child 8 9 Adolesc. Heal. 4: e17–e18, 2020 10 2. Mastrangelo A, Morello W, Vidal E, Guzzo I, Annicchiarico Petruzzelli L, Benetti E, 11 12 Materassi M, Giordano M, Pasini A, Corrado C, Puccio G, Chimenz R, Pecoraro C, 13 14 Massella L, Peruzzi L, Montini G: Impact of COVID-19 Pandemic in Children with CKD 15 16 or Immunosuppression. Clin. J. Am. Soc. Nephrol. CJN.13120820, 2020 17 3. Hoffman T, Nissen K, Krambrich J, Rönnberg B, Akaberi D, Esmaeilzadeh M, Salaneck 18 19 E, Lindahl J, Lundkvist Å: Evaluation of a COVID-19 IgM and IgG rapid test; an efficient 20 21 tool for assessment of past exposure to SARS-CoV-2. Infect. Ecol. Epidemiol. 10: 2020 22 23 4. https://www.istat.it/it/files/2020/08/ReportPrimiRisultatiIndagineSiero.pdf, Accessed on 24 2020 Dec 23rd 25 26 5. Gudbjartsson DF, Norddahl GL, Melsted P, Gunnarsdottir K, Holm H, Eythorsson E, 27 28 Arnthorsson AO, Helgason D, Bjarnadottir K, Ingvarsson RF, Thorsteinsdottir B, 29 Kristjansdottir S, Birgisdottir K, Kristinsdottir AM, Sigurdsson MI, Arnadottir GA, 30 31 Ivarsdottir E V., Andresdottir M, Jonsson F, Agustsdottir AB, Berglund J, Eiriksdottir B, 32 33 Fridriksdottir R, Gardarsdottir EE, Gottfredsson M, Gretarsdottir OS, Gudmundsdottir S, 34 35 Gudmundsson KR, Gunnarsdottir TR, Gylfason A, Helgason A, Jensson BO, Jonasdottir 36 A, Jonsson H, Kristjansson T, Kristinsson KG, Magnusdottir DN, Magnusson OT, 37 38 Olafsdottir LB, Rognvaldsson S, le Roux L, Sigmundsdottir G, Sigurdsson A, 39 40 Sveinbjornsson G, Sveinsdottir KE, Sveinsdottir M, Thorarensen EA, Thorbjornsson B, 41 42 Thordardottir M, Saemundsdottir J, Kristjansson SH, Josefsdottir KS, Masson G, 43 Georgsson G, Kristjansson M, Moller A, Palsson R, Gudnason T, Thorsteinsdottir U, 44 45 Jonsdottir I, Sulem P, Stefansson K: Humoral Immune Response to SARS-CoV-2 in 46 47 Iceland. N. Engl. J. Med. 383: 1724–1734, 2020 48 49 50 51 52 53 54 55 56 57 58 59 60 Clinical Journal of the American Society of Nephrology
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