Immunogenicity and safety of SARS-CoV-2 mRNA vaccine in patients with nephrotic syndrome receiving immunosuppressive agents.
Mycophenolate mofetil
Nephrotic syndrome
Relapse
SARS-CoV-2 S antibody
Seroconversion
Serum IgG
Journal
Pediatric nephrology (Berlin, Germany)
ISSN: 1432-198X
Titre abrégé: Pediatr Nephrol
Pays: Germany
ID NLM: 8708728
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
09
04
2022
accepted:
16
05
2022
revised:
13
05
2022
pubmed:
2
8
2022
medline:
16
2
2023
entrez:
1
8
2022
Statut:
ppublish
Résumé
As there are no large-scale reports of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) mRNA vaccination in patients with nephrotic syndrome using immunosuppressive agents, we conducted the prospective study. SARS-CoV-2 mRNA vaccines were administered to patients with nephrotic syndrome receiving immunosuppressive agents. The titers of SARS-CoV-2 spike protein receptor-binding domain antibodies were measured before and after vaccination. We evaluated factors associated with antibody titers after vaccination and analyzed adverse events. We enrolled 40 patients and evaluated vaccine immunogenicity in 35 of them. Seroconversion (> 0.8 U/mL) was achieved in all patients, and the median antibody titer was 598 U/mL (interquartile range, 89-1380 U/mL). Patients using mycophenolate mofetil (MMF) showed lower antibody titers than those who were not (median: 272 U/mL vs. 2660 U/mL, p = 0.0002), and serum immunoglobulin G (IgG) levels showed a weak linear relationship with antibody titers (R The SARS-CoV-2 mRNA vaccine was immunogenic in patients with nephrotic syndrome using immunosuppressive agents, although the use of MMF and low levels of serum IgG were associated with lower antibody titers after vaccination. Patients with high disease activity may experience a relapse of nephrotic syndrome after vaccination. A higher resolution version of the Graphical abstract is available as Supplementary information.
Sections du résumé
BACKGROUND
As there are no large-scale reports of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) mRNA vaccination in patients with nephrotic syndrome using immunosuppressive agents, we conducted the prospective study.
METHODS
SARS-CoV-2 mRNA vaccines were administered to patients with nephrotic syndrome receiving immunosuppressive agents. The titers of SARS-CoV-2 spike protein receptor-binding domain antibodies were measured before and after vaccination. We evaluated factors associated with antibody titers after vaccination and analyzed adverse events.
RESULTS
We enrolled 40 patients and evaluated vaccine immunogenicity in 35 of them. Seroconversion (> 0.8 U/mL) was achieved in all patients, and the median antibody titer was 598 U/mL (interquartile range, 89-1380 U/mL). Patients using mycophenolate mofetil (MMF) showed lower antibody titers than those who were not (median: 272 U/mL vs. 2660 U/mL, p = 0.0002), and serum immunoglobulin G (IgG) levels showed a weak linear relationship with antibody titers (R
CONCLUSIONS
The SARS-CoV-2 mRNA vaccine was immunogenic in patients with nephrotic syndrome using immunosuppressive agents, although the use of MMF and low levels of serum IgG were associated with lower antibody titers after vaccination. Patients with high disease activity may experience a relapse of nephrotic syndrome after vaccination. A higher resolution version of the Graphical abstract is available as Supplementary information.
Identifiants
pubmed: 35913562
doi: 10.1007/s00467-022-05633-y
pii: 10.1007/s00467-022-05633-y
pmc: PMC9340689
doi:
Substances chimiques
Antibodies, Viral
0
COVID-19 Vaccines
0
Immunoglobulin G
0
Immunosuppressive Agents
0
Mycophenolic Acid
HU9DX48N0T
spike protein, SARS-CoV-2
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1099-1106Informations de copyright
© 2022. The Author(s), under exclusive licence to International Pediatric Nephrology Association.
Références
Azzi Y, Bartash R, Scalea J, Loarte-Campos P, Akalin E (2021) COVID-19 and solid organ transplantation: a review article. Transplantation 105:37–55. https://doi.org/10.1097/TP.0000000000003523
doi: 10.1097/TP.0000000000003523
pubmed: 33148977
Raja MA, Mendoza MA, Villavicencio A, Anjan S, Reynolds JM, Kittipibul V, Fernandez A, Guerra G, Camargo JF, Simkins J, Morris MI, Abbo LA, Natori Y (2021) COVID-19 in solid organ transplant recipients: a systematic review and meta-analysis of current literature. Transplant Rev (Orlando) 35:100588. https://doi.org/10.1016/j.trre.2020.100588
doi: 10.1016/j.trre.2020.100588
pubmed: 33246166
Dong Y, Mo X, Hu Y, Qi X, Jiang F, Jiang Z, Tong S (2020) Epidemiology of COVID-19 among children in China. Pediatrics 145:e20200702. https://doi.org/10.1542/peds.2020-0702
doi: 10.1542/peds.2020-0702
pubmed: 32179660
Götzinger F, Santiago-García B, Noguera-Julián A, Lanaspa M, Lancella L, Calò Carducci FI, Gabrovska N, Velizarova S, Prunk P, Osterman V, Krivec U, Lo Vecchio A, Shingadia D, Soriano-Arandes A, Melendo S, Lanari M, Pierantoni L, Wagner N, L’Huillier AG, Heininger U, Ritz N, Bandi S, Krajcar N, Roglić S, Santos M, Christiaens C, Creuven M, Buonsenso D, Welch SB, Bogyi M, Brinkmann F, Tebruegge M, ptbnet COVID-19 Study Group (2020) COVID-19 in children and adolescents in Europe: a multinational, multicentre cohort study. Lancet Child Adolesc Health 4:653–661. https://doi.org/10.1016/S2352-4642(20)30177-2
doi: 10.1016/S2352-4642(20)30177-2
pubmed: 32593339
pmcid: 7316447
Viner RM, Mytton OT, Bonell C, Melendez-Torres GJ, Ward J, Hudson L, Waddington C, Thomas J, Russell S, van der Klis F, Koirala A, Ladhani S, Panovska-Griffiths J, Davies NG, Booy R, Eggo RM (2021) Susceptibility to SARS-CoV-2 infection among children and adolescents compared with adults: a systematic review and meta-analysis. JAMA Pediatr 175:143–156. https://doi.org/10.1001/jamapediatrics.2020.4573
doi: 10.1001/jamapediatrics.2020.4573
pubmed: 32975552
Marlais M, Wlodkowski T, Al-Akash S, Ananin P, Bandi VK, Baudouin V, Boyer O, Vásquez L, Govindan S, Hooman N, Ijaz I, Loza R, Melgosa M, Pande N, Pape L, Saha A, Samsonov D, Schreuder MF, Sharma J, Siddiqui S, Sinha R, Stewart H, Tasic V, Tönshoff B, Twombley K, Upadhyay K, Vivarelli M, Weaver DJ, Woroniecki R, Schaefer F, Tullus K (2020) COVID-19 in children treated with immunosuppressive medication for kidney diseases. Arch Dis Child 106:798–801. https://doi.org/10.1136/archdischild-2020-320616
doi: 10.1136/archdischild-2020-320616
pubmed: 33355203
Mastrangelo A, Morello W, Vidal E, Guzzo I, Annicchiarico Petruzzelli L, Benetti E, Materassi M, Giordano M, Pasini A, Corrado C, Puccio G, Chimenz R, Pecoraro C, Massella L, Peruzzi L, Montini G, COVID-19 Task Force of the Italian Society of Pediatric Nephrology; COVID-19 TASK FORCE of the Italian Society of Pediatric Nephrology (2021) Impact of COVID-19 pandemic in children with CKD or immunosuppression. Clin J Am Soc Nephrol 16:449–451. https://doi.org/10.2215/CJN.13120820
doi: 10.2215/CJN.13120820
pubmed: 33318026
Hod T, Ben-David A, Olmer L, Levy I, Ghinea R, Mor E, Lustig Y, Rahav G (2021) Humoral response of renal transplant recipients to the BNT162b2 SARS-CoV-2 mRNA vaccine using both RBD IgG and neutralizing antibodies. Transplantation 105:e234-243. https://doi.org/10.1097/TP.0000000000003889
doi: 10.1097/TP.0000000000003889
pubmed: 34310101
pmcid: 8549122
Grupper A, Rabinowich L, Schwartz D, Schwartz IF, Ben-Yehoyada M, Shashar M, Katchman E, Halperin T, Turner D, Goykhman Y, Shibolet O, Levy S, Houri I, Baruch R, Katchman H (2021) Reduced humoral response to mRNA SARS-CoV-2 BNT162b2 vaccine in kidney transplant recipients without prior exposure to the virus. Am J Transplant 21:2719–2726. https://doi.org/10.1111/ajt.16615
doi: 10.1111/ajt.16615
pubmed: 33866672
Benotmane I, Gautier-Vargas G, Cognard N, Olagne J, Heibel F, Braun-Parvez L, Martzloff J, Perrin P, Moulin B, Fafi-Kremer S, Caillard S (2021) Low immunization rates among kidney transplant recipients who received 2 doses of the mRNA-1273 SARS-CoV-2 vaccine. Kidney Int 99:1498–1500. https://doi.org/10.1016/j.kint.2021.04.005
doi: 10.1016/j.kint.2021.04.005
pubmed: 33887315
pmcid: 8055921
Rozen-Zvi B, Yahav D, Agur T, Zingerman B, Ben-Zvi H, Atamna A, Tau N, Mashraki T, Nesher E, Rahamimov R (2021) Antibody response to SARS-CoV-2 mRNA vaccine among kidney transplant recipients: a prospective cohort study. Clin Microbiol Infect 27:1173.e1-1173.e4. https://doi.org/10.1016/j.cmi.2021.04.028
doi: 10.1016/j.cmi.2021.04.028
pubmed: 33957273
Vaiciuniene R, Sitkauskiene B, Bumblyte IA, Dalinkeviciene E, Ziginskiene E, Bagdonas D, Augliene R, Petruliene K, Bagdziuniene I, Skarupskiene I, Stankuviene A, Sauseriene J, Macinskas S, Valius L (2021) Immune response after SARS-CoV-2 vaccination in kidney transplant patients. Medicina (Kaunas) 57:1327. https://doi.org/10.3390/medicina57121327
doi: 10.3390/medicina57121327
pubmed: 34946272
Timmermann L, Globke B, Lurje G, Schmelzle M, Schöning W, Öllinger R, Pratschke J, Eberspächer B, Drosten C, Hofmann J, Eurich D (2021) Humoral immune response following SARS-CoV-2 vaccination in liver transplant recipients. Vaccines (Basel) 9:1422. https://doi.org/10.3390/vaccines9121422
doi: 10.3390/vaccines9121422
pubmed: 34960168
Guarino M, Cossiga V, Esposito I, Furno A, Morisco F (2022) Effectiveness of SARS-CoV-2 vaccination in liver transplanted patients: the debate is open! J Hepatol 76:237–239. https://doi.org/10.1016/j.jhep.2021.07.034
doi: 10.1016/j.jhep.2021.07.034
pubmed: 34358567
Marion O, Del Bello A, Abravanel F, Faguer S, Esposito L, Laure Hebral A, Bellière J, Izopet J, Kamar N (2021) Predictive factors for humoral response after 2-dose SARS-CoV-2 vaccine in solid organ transplant patients. Transplant Direct 8:e1248. https://doi.org/10.1097/TXD.0000000000001248
doi: 10.1097/TXD.0000000000001248
pubmed: 34966837
pmcid: 8710345
Furer V, Eviatar T, Zisman D, Peleg H, Paran D, Levartovsky D, Zisapel M, Elalouf O, Kaufman I, Meidan R, Broyde A, Polachek A, Wollman J, Litinsky I, Meridor K, Nochomovitz H, Silberman A, Rosenberg D, Feld J, Haddad A, Gazzit T, Elias M, Higazi N, Kharouf F, Shefer G, Sharon O, Pel S, Nevo S, Elkayam O (2021) Immunogenicity and safety of the BNT162b2 mRNA COVID-19 vaccine in adult patients with autoimmune inflammatory rheumatic diseases and in the general population: a multicentre study. Ann Rheum Dis 80:1330–1338. https://doi.org/10.1136/annrheumdis-2021-220647
doi: 10.1136/annrheumdis-2021-220647
pubmed: 34127481
Tzioufas AG, Bakasis AD, Goules AV, Bitzogli K, Cinoku II, Chatzis LG, Argyropoulou OD, Venetsanopoulou AI, Mavrommati M, Stergiou IE, Pezoulas V, Voulgari PV, Katsimpari C, Katechis S, Gazi S, Katsifis G, Sfontouris CI, Georgountzos AI, Liossis SN, Papagoras C, Fotiadis DI, Skopouli FN, Vlachoyiannopoulos PG, Moutsopoulos HM (2021) A prospective multicenter study assessing humoral immunogenicity and safety of the mRNA SARS-CoV-2 vaccines in Greek patients with systemic autoimmune and autoinflammatory rheumatic diseases. J Autoimmun 125:102743. https://doi.org/10.1016/j.jaut.2021.102743
doi: 10.1016/j.jaut.2021.102743
pubmed: 34757289
pmcid: 8552665
Braun-Moscovici Y, Kaplan M, Braun M, Markovits D, Giryes S, Toledano K, Tavor Y, Dolnikov K, Balbir-Gurman A (2021) Disease activity and humoral response in patients with inflammatory rheumatic diseases after two doses of the Pfizer mRNA vaccine against SARS-CoV-2. Ann Rheum Dis 80:1317–1321. https://doi.org/10.1136/annrheumdis-2021-220503
doi: 10.1136/annrheumdis-2021-220503
pubmed: 34144967
Izzedine H, Bonilla M, Jhaveri KD (2021) Nephrotic syndrome and vasculitis following SARS-CoV-2 vaccine: true association or circumstantial? Nephrol Dial Transplant 36:1565–1569. https://doi.org/10.1093/ndt/gfab215
doi: 10.1093/ndt/gfab215
pubmed: 34245294
Nakazawa E, Uchimura T, Hirai Y, Togashi H, Oyama Y, Inaba A, Shiga K, Ito S (2021) New-onset pediatric nephrotic syndrome following Pfizer-BioNTech SARS-CoV-2 vaccination: a case report and literature review. CEN Case Rep 11:242–246. https://doi.org/10.1007/s13730-021-00656-0
doi: 10.1007/s13730-021-00656-0
pubmed: 34782983
pmcid: 8592073
Thuluvath PJ, Robarts P, Chauhan M (2021) Analysis of antibody responses after COVID-19 vaccination in liver transplant recipients and those with chronic liver diseases. J Hepatol 75:1434–1439. https://doi.org/10.1016/j.jhep.2021.08.008
doi: 10.1016/j.jhep.2021.08.008
pubmed: 34454993
pmcid: 8387568
Hirotsu Y, Amemiya K, Sugiura H, Shinohara M, Takatori M, Mochizuki H, Omata M (2021) Robust antibody responses to the BNT162b2 mRNA vaccine occur within a week after the first dose in previously infected individuals and after the second dose in uninfected individuals. Front Immunol 12:722766. https://doi.org/10.3389/fimmu.2021.722766
doi: 10.3389/fimmu.2021.722766
pubmed: 34512649
pmcid: 8427169
Callegaro A, Borleri D, Farina C, Napolitano G, Valenti D, Rizzi M, Maggiolo F (2021) Antibody response to SARS-CoV-2 vaccination is extremely vivacious in subjects with previous SARS-CoV-2 infection. J Med Virol 93:4612–4615. https://doi.org/10.1002/jmv.26982
doi: 10.1002/jmv.26982
pubmed: 33788281
pmcid: 8250392
Tanaka S, Saikusa T, Katafuchi Y, Ushijima K, Ohtsu Y, Tsumura N, Ito Y (2015) Serologic response after vaccination against influenza (A/H1N1) pdm09 in children with renal disease receiving oral immunosuppressive drugs. Vaccine 33:5000–5004. https://doi.org/10.1016/j.vaccine.2015.06.049
doi: 10.1016/j.vaccine.2015.06.049
pubmed: 26083312
Poyrazoğlu HM, Düşünsel R, Gündüz Z, Patiroğlu T, Köklü S (2004) Antibody response to influenza A vaccination in children with nephrotic syndrome. Pediatr Nephrol 19:57–60. https://doi.org/10.1007/s00467-003-1301-3
doi: 10.1007/s00467-003-1301-3
pubmed: 14648340
Campos LM, Silva CA, Aikawa NE, Jesus AA, Moraes JC, Miraglia J, Ishida MA, Bueno C, Pereira RM, Bonfa E (2013) High disease activity: an independent factor for reduced immunogenicity of the pandemic influenza A vaccine in patients with juvenile systemic lupus erythematosus. Arthritis Care Res (Hoboken) 65:1121–1127. https://doi.org/10.1002/acr.21948
doi: 10.1002/acr.21948
pubmed: 23818263
Kumar D, Blumberg EA, Danziger-Isakov L, Kotton CN, Halasa NB, Ison MG, Avery RK, Green M, Allen UD, Edwards KM, Miller G, Michaels MG, AST Infectious Diseases Community of Practice (2011) Influenza vaccination in the organ transplant recipient: review and summary recommendations. Am J Transplant 11:2020–2030. https://doi.org/10.1111/j.1600-6143.2011.03753.x
doi: 10.1111/j.1600-6143.2011.03753.x
pubmed: 21957936
Gavaldà J, Cabral E, Perez-Romero P, Len O, Aydillo T, Campins M, Quintero J, Peghin M, Nieto J, Charco R, Pahissa A, Cordero E, Spanish Network for the Research in Infectious Diseases (REIPI) (2013) Immunogenicity of pandemic influenza A H1N1/2009 adjuvanted vaccine in pediatric solid organ transplant recipients. Pediatr Transplant 17:403–406. https://doi.org/10.1111/petr.12084
doi: 10.1111/petr.12084
pubmed: 23692602
Mrak D, Tobudic S, Koblischke M, Graninger M, Radner H, Sieghart D, Hofer P, Perkmann T, Haslacher H, Thalhammer R, Winkler S, Blüml S, Stiasny K, Aberle JH, Smolen JS, Heinz LX, Aletaha D, Bonelli M (2021) SARS-CoV-2 vaccination in rituximab-treated patients: B cells promote humoral immune responses in the presence of T-cell-mediated immunity. Ann Rheum Dis 80:1345–1350. https://doi.org/10.1136/annrheumdis-2021-220781
doi: 10.1136/annrheumdis-2021-220781
pubmed: 34285048
Fernandes P, Jorge S, Lopes JA (2010) Relapse of nephrotic syndrome following the use of 2009 pandemic influenza A (H1N1) vaccine. Am J Kidney Dis 56:185–186. https://doi.org/10.1053/j.ajkd.2010.04.011
doi: 10.1053/j.ajkd.2010.04.011
pubmed: 20620684
Ishimori S, Kamei K, Ando T, Yoshikawa T, Kano Y, Nagata H, Saida K, Sato M, Ogura M, Ito S, Ishikura K (2020) Influenza virus vaccination in children with nephrotic syndrome: insignificant risk of relapse. Clin Exp Nephrol 24:1069–1076. https://doi.org/10.1007/s10157-020-01930-8
doi: 10.1007/s10157-020-01930-8
pubmed: 32720203
pmcid: 7383070
Angeletti A, Bruschi M, Bianchin S, Bonato I, Montobbio C, Verrina E, Lugani F, Cravedi P, Ghiggeri GM (2021) Vaccines and disease relapses in children with nephrotic syndrome. Clin J Am Soc Nephrol 16:937–938. https://doi.org/10.2215/CJN.01890221
doi: 10.2215/CJN.01890221
pubmed: 34117084
pmcid: 8216624
Favresse J, Bayart JL, Mullier F, Elsen M, Eucher C, Van Eeckhoudt S, Roy T, Wieers G, Laurent C, Dogné JM, Closset M, Douxfils J (2021) Antibody titres decline 3-month post-vaccination with BNT162b2. Emerg Microbes Infect 10:1495–1498. https://doi.org/10.1080/22221751.2021.1953403
doi: 10.1080/22221751.2021.1953403
pubmed: 34232116
Erice A, Varillas-Delgado D, Caballero C (2022) Decline of antibody titres 3 months after two doses of BNT162b2 in non-immunocompromised adults. Clin Microbiol Infect 28:139.e1-e139.e4. https://doi.org/10.1016/j.cmi.2021.08.023
doi: 10.1016/j.cmi.2021.08.023
pubmed: 34508885
Naaber P, Tserel L, Kangro K, Sepp E, Jürjenson V, Adamson A, Haljasmägi L, Rumm AP, Maruste R, Kärner J, Gerhold JM, Planken A, Ustav M, Kisand K, Peterson P (2021) Dynamics of antibody response to BNT162b2 vaccine after six months: a longitudinal prospective study. Lancet Reg Health Eur 10:100208. https://doi.org/10.1016/j.lanepe.2021.100208
doi: 10.1016/j.lanepe.2021.100208
pubmed: 34514454
pmcid: 8418937