Journal Information
Vol. 43. Issue. 3.May - June 2023
Pages 269-382
Vol. 43. Issue. 3.May - June 2023
Pages 269-382
Letter to the Editor
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Suboptimal humoral immunological response to the 2nd dose of anti-COVID19 mRNA-1273 vaccine (Moderna) in kidney transplant patients
Respuesta inmunológica humoral insuficiente a la 2.a dosis de vacuna anti-COVID19 mRNA-1273 (Moderna) en pacientes portadores de trasplante renal
Jesús Martín-García
Corresponding author

Corresponding author.
, Gilda Carreño Cornejo, Rosario Manzanedo Bueno, Consolación Rosado Rubio, David Menéndez González, Dolores Barreda Grande, Carmen Felipe Fernández
Sección de Nefrología, Complejo asistencial de Ávila, Ávila, Spain
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Dear Editor,

Since the start of vaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), various groups of researchers have found a weak immune response in patients with solid organ transplants.1,2 This finding and the fact that some transplant patients have suffered from COVID-19 after being fully vaccinated with two doses, has led to the recommendation, in some countries, of a third dose of vaccine in these patients.3,4

We prospectively studied the humoural response to the mRNA-1273 (Moderna) vaccine in 73 kidney transplant recipients by quantitatively determining anti-Spike IgG antibodies to SARS-CoV-2, immediately before the second dose and eight weeks after vaccine administration, analysed by microparticle chemiluminescence (Abbott Alinity system [ref. value + >50 AU/ml]). The results were compared with the response to the same mRNA-1273 vaccine administered to 30 patients on haemodialysis (HD), 12 on peritoneal dialysis (PD), 21 pre-dialysis (pre-D) and 47 controls, who were healthy hospital workers.

As this was a prospective study, it was approved by the Independent Ethics Committee for Clinical Trials with medicines (IECm) of the institution, Gerencia de Asistencia Sanitaria de Ávila [Ávila Healthcare Management].

The mean age of the transplant recipients was 60.12 ± 10.4 and the time since transplantation was 123–11,888 days; 56.1% were male. Four patients who had previous SARS-CoV-2 infection and three patients who had been in close contact and had a high suspicion of infection had very high titres (40,374.6 ± 55,211.5 AU/ml) and were excluded from the analysis. The response to the first dose of the vaccine, defined by IgG levels >50 AU/ml, was only found in 16.4% (11 patients) with a mean anti-Spike IgG antibody (Ab) titre of 270.8 ± 322.0 (median: 172.9; r = 52.6–19,650.3); 79.8% had levels below 50 AU/ml, and 21 (28.7%) were anergic (0–<1 AU/ml). Eight patients on HD, one on PD and two pre-D had already had clinical SARS-CoV-2 infection and all developed a strong anti-Spike Ab response to the first dose of vaccine (patients on HD: 42,181 ± 22,798; PD: 35,418.4 AU/ml; pre-D: 36,934.3 ± 35,026.7). Of the rest, 90.9% of patients on HD, 72.7% of those on PD and 78.9% of the pre-D developed an Ab response >50 AU/ml, with mean figures of 377.5 ± 350.4 AU/ml (median: 314.9) in HD; 1176.5 ± 1823.8 (median: 646.7) in PD and 1158.3 ± 1431.1 (median: 683.6) in pre-D, with significant differences compared to the transplant recipients (p = 0.004). The transplant recipients with IgG anti-Spike <50 AU/ml were older, 63.7 ± 9 vs 58.5 ± 10 (p = 0.1), with more lymphopenia 1568 ± 731 vs 2060 ± 680 (p = 0.05); and there was a correlation between IgG anti-Spike and lymphocytes: R = 0.32 (p = 0.007); a certain negative correlation was also detected with tacrolimus, R = −0.24, and prednisone, R = −0.14, although not statistically significant (p = 0.1). Eight weeks after the second dose of mRNA-1273, another antibody determination was performed; 35 transplant recipients already had levels >50 AU/ml, (53.03% vs 100% of patients on HD, PD, pre-D and healthy controls) (Fig. 1). The anti-Spike Ab titre was also lower than the rest of the groups: mean 1544.11 ± 4279.58 AU/ml (95% CI: 2576.58–511.6) vs 4000.3 ± 5567.2 (95% CI: 6683.62–1317.03) on HD; 3709.3 ± 2889.6 (95% CI: 5650.61–1768.03) on PD; 7288.4 ± 7849.1 (95% CI: 12,031.6–2545.2) in pre-D; and significantly lower than those of healthy controls: mean 16,226.3 ± 11,319.8 (95% CI: 19,462.5–2545.2) (Fig. 2). There was no evidence of any serious events after the first or second doses, or any rejection phenomenon or variation in serum creatinine. In the follow-up period, none of the patients or controls developed COVID-19 infection, despite having a low antibody titre, perhaps related to a certain degree of cellular immunity.5

Fig. 1.

Percentage of patients and controls who had developed anti-Spike SARS-CoV-2 Ab, at a titre above 50 AU/ml, at eight weeks after administration of the second dose of mRNA-1273 (Moderna) vaccine.

Fig. 2.

Titres of anti-Spike SARS-CoV-2 antibodies of patients and controls 8 weeks after the 2nd dose of mRNA-1273 (Moderna) vaccine. Mean and 95% CI.


This study shows that, in transplant recipients, the immunisation achieved with the second dose of mRNA-1273 (Moderna) vaccine improves considerably, but without reaching a prevalence of at least 70% in this population, with anti-Spike anti-IgG Ab titres significantly lower than the controls and the rest of the groups of patients with advanced chronic kidney disease (ACKD). As a large proportion of transplant recipients remain at risk of COVID-19, another third dose of vaccine should be provided as soon as possible, as is already being done in other countries.6

B.J. Boyarsky, W.A. Werbel, R.K. Avery, A.A.R. Tobian, A. Massie, D.L. Segey, et al.
Antibody response to 2-dose SARS-CoV-2 mRNA vaccine series in solid organ transplant recipients.
JAMA, 325 (2021), pp. 2204-2206
O. Marion, A. del Bello, F. Abravanel, C. Couat, S. Faguer, L. Esposito, et al.
Safety and immunogenicity of anti-SARS-CoV-2 messenger RNA vaccines in recipients of solid organ transplants.
Ann Intern Med, (2021), pp. M21-1341
H.M. Wadei, T.A. Gonwa, J.C. Leoni, S.Z. Shah, N. Aslam, L.L. Speicher.
COVID-19 infection in solid organ transplant recipients after SARS-CoV-2 vaccination.
Am J Transplant, 23 (2021),
DGS-Urgent. Vaccins contre la Covid-19: modalities d’administration des rappels, (2021),
M. Anft, A. Blazquez-Navarro, U. Stervbo, S. Skrzypczyk, O. Witzke, R. Wirth, et al.
Detection of pre-existing SARS-Cov-2-reactive T cells in unexposed renal transplant patient.
J Nephrol, 34 (2021), pp. 1025-1037
N. Kamar, F. Abravanel, O. Marion, J. Izopet, A. del Bello.
Three doses of an mRNA Covid-19 vaccine in solid-organ transplant recipients.
N Engl J Med, 38 (2021), pp. 661-662
Copyright © 2021. Sociedad Española de Nefrología
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