www.kidney-international.org commentary

protein (anti–nucleocapsid protein) and Immune response to SARS- receptor-binding domain (RBD; anti- CoV-2 infection and RBD) antibodies at time 0 (baseline) and at month 6 to assess durability and in patients functionality of the immune response to SARS-CoV-2 infection.3 They also receiving kidney replacement screened for SARS-CoV-2–specificT- cell responses in those who became seronegative at 6 months. Their results T. Alp Ikizler1, P. Toby Coates2, Brad H. Rovin3 and Pierre Ronco4,5 showed that in 136 patients who were antibody-positive at baseline, up to 85% of patients maintained serologic evi- In this issue of Kidney International, the initial experience regarding dence of immune responses at 6 the immunogenicity of prior coronavirus disease 2019 (COVID-19) months. In 8 of 11 patients who became infection and the response to the COVID-19 among patients seronegative at 6 months, there was on maintenance dialysis and kidney transplant recipients is evidence of robust cellular immunity summarized. Preliminary data suggest that there is durability of measured by T-cell response to SARS- immune response after COVID-19 infection. Although immune CoV-2 structural proteins, suggesting that >95% of patients receiving MHD response to the first dose of is less in infection-naïve patients maintained serologic or cellular evi- than healthy individuals in both groups, after the second vaccine dose dence of immune responses at 6 a significant portion of patients receiving maintenance dialysis months. Prior seropositivity seemed to develop robust antibody titers, whereas kidney transplant recipients be protective against subsequent SARS- show a less-strong immune response. CoV-2 infection. These results are Kidney International - - - consistent with the report by Forbes (2021) , – ; https://doi.org/10.1016/j.kint.2021.04.007 et al. Copyright ª 2021, International Society of . Published by Elsevier Inc. All rights reserved. , who suggested in a study of 122 patients receiving MHD, there is robust see clinical investigation on page XXX and letters to the editor on and sustained antibody response after pages xxx, xxx, xxx, xxx, xxx, xxx, xxx, xxx, and xxx confirmed COVID-19 infection with no suggestion that immunosuppression weakens this response.4 They also re- atients with end-stage kidney Efforts are underway to vaccinate as ported that seroconversion rates in- P disease (ESKD) receiving main- many individuals as possible crease over time, suggesting a longer tenance dialysis or who have had throughout the world to get the than usual immune response adaptation 2 a kidney transplant are at increased risk pandemic under control. Although the in patients receiving MHD compared for morbidity and mortality after nephrology community has called for with healthy controls. Of note, in a infection with severe acute respiratory ESKD patients to have priority for small cohort of 14 pediatric patients syndrome coronavirus 2 (SARS-CoV-2) vaccination as a vulnerable population, receiving MHD, Canas et al. reported a 1 compared with the general population. there has been an underlying concern seroconversion rate of 38% at 13 weeks, that these patients may not mount a which may reflect a time-dependent good response to vaccination or even early response because other data sug- 1 Department of , Division of Nephrology after a previous infection with SARS- gest a longer time interval to full and Hypertension, Vanderbilt University Medical CoV-2. In this issue of Kidney Interna- 6 2 immunization. Center, Nashville, Tennessee, USA; Centre for tional, we present the initial experience Clinical and Experimental Transplantation, The In a separate smaller but more 3 of nephrologists from around the world University of Adelaide, Adelaide, Australia; Inter- thoroughly examined cohort, Anft et al. – regarding the immunogenicity of prior nal Medicine Nephrology, The Ohio State Uni- performed an observational case- versity Wexner Medical Center, Columbus, Ohio, coronavirus disease 2019 (COVID-19) 4 control study comparing the fre- USA; Unité Mixte de Recherche S 1155, Sorbonne infection and the response to the quencies and functionality of SARS- Université, Université Pierre et Marie Curie Paris 06 COVID-19 vaccines among patients and Institut National de la Santé et de la CoV-2 reactive T cells as well as anti- 5 with ESKD receiving kidney replace- Recherche Médicale, Paris, France; and Division – body titers in 14 COVID-19 convales- ment therapy (Table 13 14). of Nephrology, Centre Hospitalier du Mans, Le cent hemodialysis patients compared Mans, France with 14 age- and sex-matched healthy Correspondence: T. Alp Ikizler, Division of What do the studies show? controls.5 They showed that not only Nephrology and Hypertension, Vanderbilt Uni- fi versity Medical Center, 1161 21st Avenue South, S- In a study of 356 patients receiving were spike-speci c antibody titers 3223 Medical Center North, Nashville, Tennessee maintenance hemodialysis (MHD), comparable in both groups, frequencies þ 37232-2372, USA. E-mail: [email protected] Clark et al. screened for nucleocapsid of SARS-CoV-2–reactive CD4 and

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Table 1 | Characteristics of studies examining immune response to COVID-19 infection and the response to the COVID-19 vaccines among ESKD patients receiving kidney replacement therapy Patient Infection vs. Author population vaccine Sample size Follow-up Outcome Result Clark et al.3 MHD Infection 136 6 mo Anti-NP 85% Seropositive; Anti-RBD 70% T-cell response in seronegative patients Forbes et al.4 MHD Infection 122 184 d Anti-NP 100% Seropositive Increasing Ab over time

Anft et al.5 MHD and Infection 14 and 14 Not provided T-cell Robust response in MHD control response

Canas et al.6 MHD/ Infection 14 13 wk Anti-S IgG 38% Seropositive pediatric patients Torreggiani et al.7 MHD Vaccine/ 101 3 wk after first Anti-S IgG 35% Seropositive Pfizer vaccination Billany et al.8 MHD Vaccine/ 94 28 d after first Anti-S IgG 80% Seropositive Pfizer þ AZ dose Attias et al.9 MHD Vaccine/ 69 Weekly until 3 wk Anti-S IgG 80% Seropositive previous infection Pfizer after second dose better response after first dose Simon et al.10 MHD and Vaccine/ 81 and 80 3 wk after second Anti-NP Low titers in MHD (171 vs. 478) control Pfizer vaccine Berar Yanar et al.11 MHD, PD, Vaccine/ 127, 33, and 21–35 d after the Anti-S IgG Low titers in dialysis patients, 6 de and control Pfizer 132 second dose novo infections in dialysis patients Boyarsky et al.12 Kidney Tx Vaccine/ 436 20 d Anti-S IgG 17% Seropositive both mRNA vaccines Benotmane et al.13 Kidney Tx Vaccine/ 242 28 d Anti-S IgG 11% Seropositive mRNA 1273 Benotmane et al.14 Kidney Tx Vaccine/ 205 28 d after second Anti-S IgG 48% Seropositive mRNA 1273 dose AZ, AstraZeneca; COVID-19, coronavirus disease 2019; ESKD, end-stage kidney disease; MHD, maintenance hemodialysis; NP, nucleocapsid protein; PD, peritoneal dialysis; RBD, receptor-binding domain; S, spike; Tx, transplantation.

þ CD8 T cells, producing the effector the first dose of BNT162b2 COVID-19 baseline. Anti–spike 1 levels were higher cytokines granzyme B, interleukin-2, mRNA vaccine, only 35% developed in these patients compared with pa- tumor necrosis factor, and interferon- detectable antibodies to spike protein.7 tients who were seronegative at baseline. g, were similar or for certain cytokines On the other hand, Billany et al. re- Although seropositivity was at 6% (3 of even significantly higher in patients ported somewhat different preliminary 56) at the time of the second dose in receiving MHD. These data are consis- results, with robust antibody response patients without prior history of disease tent with those of Clark et al., and (80%) 28 days after the first vaccination or seropositivity, the overall seroposi- strongly suggest patients receiving dose against COVID-19 in a cohort of tivity rate reached >80% in the entire MHD can generate an efficient T-cell 95 prevalent patients receiving MHD in cohort at the end of the follow-up immune response to SARS-CoV-2 the United Kingdom.8 Although these 2 period, suggesting a delayed but robust infection, albeit only shown in a small, reports present data after 1 dose of humoral immune response to the full selected cohort. vaccine, Attias et al. examined anti– course of mRNA-based vaccination in In addition to the assessment of spike 1 IgG antibody levels in 69 pa- patients receiving MHD. These findings native response to SARS-CoV-2 infec- tients receiving MHD as a measure of are important in instances in which a tion, several important early reports of antibody response to 2 consecutive required second dosing of the vaccina- immunogenicity to COVID-19 vacci- BNT162b2 vaccine administrations.9 tion might be delayed. In a preliminary nation in patients receiving MHD are They reported antibody titers weekly report in 81 patients receiving MHD published in this issue of Kidney Inter- up to 7 weeks after the first injection. and 80 individuals without kidney dis- national. In a preliminary report, Tor- Among the entire cohort, 13 (19%) ease who received 2 consecutive reggiani et al. showed that in 101 patients either had a previous COVID- BNT162b2 vaccine administrations, patients receiving MHD who received 19 infection or positive serology at Simon et al. reported anti–spike

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Table 2 | A summary of methods for the assessment of immunogenicity against solid organ transplants (219 received a infection and vaccination kidney transplant).12 At a median of 20 – fi Notes days (IQR, 17 24 days) after the rst Humoral response to dose of mRNA vaccines, antibody (anti– structural proteins spike 1 or anti-RBD) was detectable in IgG/IgM against spike ELISA: most commonly reported; correlate with infection severity; 76 of 436 participants (17%; 95% con- protein likely reflects subsequent response; unclear disease prevention and fi – IgG against receptor- efficacy dence interval, 14% 21%). These data binding domain suggest a diminished humoral response IgG against membrane to mRNA-based vaccination in patients protein who received a kidney transplant and Neutralization assay Pseudovirus Most time-consuming highlight the need for the second vac- Live virus SARS-CoV-2 spiked lentivirus cine administration and vigilant Focus reduction Readout usually reflects half maximal inhibitory concentration continued surveillance. They also sug- neutralization assay gest a response comparable or slightly Plaque reduction neutralization assay less than observed in patients receiving Cellular response MHD after the first dose of an mRNA ELISpot: either T or B cell Activation of single cells by specific Ag (i.e., spike protein, membrane vaccine. Of concern, also published in – protein, or a panel of SARS-CoV-2 related peptides) this edition of Kidney International is Requires PBMCs Cytokine response IFN-g, TNF, IL-2 the follow-up data of 205 patients who Ag-specific T cells CD4/CD8þ cells received a kidney transplant who had Memory B-cell responses Flow cytometry using tetramer staining received 2 doses of the mRNA-1273 Ag, antigen; ELISA, enzyme-linked immunosorbent assay; IFN-g, interferon-g; IL-2, interleukin-2; PBMC, peripheral blood SARS-CoV-2 vaccine from France.14 At mononuclear cell; SARS-CoV-2, severe acute respiratory syndrome coronavirus 2; TNF, tumor necrosis factor. 28 days after the second dose, only 48% of KTRs responded, generating a titer of antibody titers 21 days after the second important to advise all patients >50 with a median antibody titer of 803 dose.10 Although seropositivity rates receiving dialysis to adhere to strict (IQR, 142–4609). Patients who received based on the manufacturer’s cutoff level infection control measures regardless of their first transplant, had a longer were not reported, they showed sub- full vaccination. These data also bring duration from transplant, experienced stantially lower antibody titers in pa- up the potential consideration for better graft function, and experienced tients receiving MHD versus individuals additional booster dosing in certain lower levels of overall immunosup- without kidney disease (median, 171 dialysis patients based on their risk pression mounted a stronger immune U/ml vs. 2500 U/ml, respectively). profile once that is fully established by response. These important real-world Finally, in a study from Israel, Berar further data. observations indicate that vaccination Yanay et al. reported anti–spike anti- Patients with a functioning kidney of the most vulnerable in our renal body levels 21 to 35 days after the sec- transplant on immunosuppression are community does not fully protect and ond dose of the BNT162b2 COVID-19 at increased risk for severe complica- therefore should not promote any mRNA vaccine in 127 patients receiving tions of COVID-19 infection. In this complacency about protection provided hemodialysis, 33 patients receiving issue of Kidney International, Benot- by COVID-19 vaccines in immuno- peritoneal dialysis, and a control group mane et al. assessed anti–SARS-CoV-2 compromised patients. of 132 hospital employees.11 Although antibody response against the spike the median anti–spike antibody levels protein 28 days after the first injection What do these studies mean for were statistically significantly lower in of the Moderna mRNA-1273 vaccine patients with advanced kidney disease? the patients receiving dialysis compared (100 mg) in 242 kidney transplant re- To interpret these early data, one should with controls (116.5 [interquartile cipients (KTRs).13 These KTRs had no revisit the basic methods of assessment range {IQR}, 66–160] arbitrary unit history of prior COVID-19 infection of immunogenicity to native infection [AU]/ml vs. 176.5 [IQR, 142–235] AU/ and were negative for anti–SARS-CoV-2 and vaccination, which are good but ml, respectively), there was >90% antibodies. Only 26 (10.8%) KTRs had not perfect correlates of acquired pro- seropositivity in the group of patients a positive serology 28 days after injec- tection or vaccine efficacy. Table 2 receiving dialysis. Of some concern, 6 tion, with a median IgG titer of 224 AU/ provides a summary of methods for (4%) patients receiving dialysis devel- ml (IQR, 76496 AU/ml) compared assessment of immunogenicity. This oped COVID-19 infection 7 days after with a median IgG titer of <6.8 AU/ml inclusive, although not exhaustive, list the second vaccination, whereas there in seronegative KTRs. These data are covers humoral and cellular response to were no infections in the control group. consistent with the report by Boyarsky infection and vaccines.15 For the hu- Although the circumstances related to et al., who measured antibodies against moral response, the most used and re- these infections need to be clarified the RBD of the SARS-CoV-2 spike ported method is antibody (IgM or before making conclusions, it is protein in 436 patients who received IgG) titer. These could be total antibody

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levels or levels against specific structural antibody from memory B cells despite a kidney disease. It should be kept in proteins, such as spike or membrane drop in measured antibody responses to mind that patients with ESKD do have proteins of SARS-CoV-2. The antibody RBD, suggesting that durable long-term other comorbidities that could nega- response can be reported as positive or immunity in the B-cell compartment tively influence their immune response, negative based on the manufacturer’s can be generated.19,20 There are yet no and it is premature to claim that criteria, actual titers, or relative titers as reports regarding the neutralizing advanced kidney disease per se has a ratio to an internal control. Not sur- capability against live viruses or pseu- major impact on immunogenicity to prisingly, the variations in reporting are doviruses in patients with kidney SARS-CoV-2 and its variants. For not only confusing for the lay reader, disease. example, it is well-established that old but also make assessment of immune Finally, assessment of cellular age is associated with less immunoge- response more complex and less pre- response is also important in terms of nicity against live viruses, although this cise. Accordingly, a more standardized long-term response to infection and may not be applicable to mRNA- or reporting was recommended by the vaccination. An important question adjuvant-based vaccines. It is yet to be World Health Organization Interna- has been raised in the lay public as established whether comorbidities, such tional Standards for Anti–SARS-CoV-2 well as scientific literature concerning as diabetes, heart disease, hypertension, Immunoglobulin Group.16 Although whether durable immunity to SARS- and obesity, individually or in combi- there are some data to suggest that these CoV-2 infection can be achieved. nation with advanced kidney disease methods do reflect adequate prevention That humans can retain a long-term and immunosuppression, lessen from subsequent infection or vaccine immune response against SARS-CoV-2 immunogenicity to SARS-CoV-2 infec- efficacy, as shown in recent randomized has been studied by Le Bert et al., tion and vaccination. Third, in new clinical trials in healthy individuals, who demonstrated peripheral T-cell studies going forward is the need for there are no adequately powered com- responses in patients previously comprehensive immunophenotyping of parisons available in patients with kid- infected with SARS-CoV-2 18 years patients with kidney disease using state- ney disease. after their original infection.21 Reas- of-the-art immune monitoring. Measurement of neutralizing capa- suringly, spike-specific memory B cells Measuring all components, not just an bility against live viruses or pseudovi- were more abundant at 6 months antibody response, is critical to ruses is another well-established than at 1 month after symptom onset measuring the immune response. As method to assess immunogenicity in in a recent study by Dan et al.22 antibody-dependent cell cytotoxicity is humans. These tests are more reflective Because patients with ESKD and important, then it is important not of the robustness of humoral immune those on immunosuppressive just to measure total IgG to spike pro- response because they directly measure are known to have abnormalities in teins, but to also measure IgG1 and the capability to suppress virus growth. their innate and adaptive immune IgG3 subtypes, as well as detailed The readouts usually reflect half response, it is crucial to assess their responses in T- and B-cell compart- maximal inhibitory concentration of cellular immunity after SARS-CoV-2 ments (ELISpot and tetramer staining). the antibodies obtained from in- infection or vaccination. In that Accordingly, data to date in patients dividuals either previously infected or respect, the data by Anft et al.are with ESKD should be considered vaccinated. For example, Anderson promising but not conclusive. preliminary. et al. showed that the 100-mg dose of Most important, the follow-up data SARS-CoV-2 mRNA-1273 vaccine What should be done going forward? on seroconversion following 2 doses of induced higher binding and The early publications noted in this vaccine in KTRs from Benotmane et al. neutralizing-antibody titers than the 25- issue of Kidney International are are concerning, as <50% of recipients mg dose, which supported the use of the noticeably instructive in terms of developed a positive antibody titer. This 100-mg dose in the phase 3 vaccine trial several strategies going forward. First study highlights further work on the that was proven to be highly effective in and foremost, the data conclusively frequency of vaccination that will be the study and the real world.17 suggest that ESKD patients do mount required in this population to achieve Furthermore, Edara et al. reported an immune response to SARS-CoV-2 seropositivity, and whether this will robust neutralizing activity of infection- infection and vaccination; albeit it is translate into durable long-term and vaccine-elicited antibodies against not immediate, but increases over time. immunity. four SARS-CoV-2 variants, including Based on published data to date, it is Finally, these data suggest that full B.1.1.7.18 It is notable that the vaccine- premature to conclude whether KTRs vaccination protocols should be imple- elicited response was stronger than one will behave similarly to patients mented in patients receiving MHD and induced by previous or acute infection. receiving maintenance dialysis. Second, KTRs. Preliminary data by Attias et al., Although antibody responses and in the data published to date do not Simon et al., Torreggiani et al., and particular neutralizing antibody re- inform as to whether the immune Boyarsky et al. all highlight a limited sponses are important, recent studies response in patients with ESKD is humoral response after a single dose of have shown a persistence of RBD comparable to individuals without vaccine. The adverse consequences of

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inadequate vaccination, such as infec- to this devastating disease by the pa- ahead of print]. Kidney Int. https://doi.org/1 0.1016/j.kint.2021.04.006. tion by highly virulent variants, could be tients and clinicians. 12. Boyarsky BJ, Werbel WA, Avery RK, et al. devastating in these individuals. These Immunogenicity of a single dose of data also emphasize the importance of DISCLOSURE SARS-CoV-2 messenger RNA vaccine in early vaccination of these patients in All the authors declared no competing solid organ transplant recipients [e-pub interests. ahead of print]. JAMA. https://doi.org/10.1 general and the important regulatory 001/jama.2021.4385. Accessed April 15, decisions for full vaccination in these 2021. patients. Although the recent decision by REFERENCES 13. Benotmane I, Gautier-Vargas G, Gongnard N, 1. Ng JH, Hirsch JS, Wanchoo R, et al. Outcomes et al. 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