key: cord-0878961-ikxf9g0x
authors: Kronbichler, Andreas; Anders, Hans-Joachim; Fernandez-Juárez, Gema Maria; Floege, Jürgen; Goumenos, Dimitrios; Segelmark, Mårten; Tesar, Vladimir; Turkmen, Kultigin; van Kooten, Cees; Bruchfeld, Annette
title: Recommendations for the use of COVID-19 vaccines in patients with immune-mediated kidney diseases
date: 2021-03-09
journal: Nephrol Dial Transplant
DOI: 10.1093/ndt/gfab064
sha: e5fb18cffd92b23514524a070e09a41fcc594d97
doc_id: 878961
cord_uid: ikxf9g0x

Coronavirus Disease 19 (COVID-19) vaccine platforms are becoming available and are the most promising strategy to curb the spread of SARS-CoV-2 infections. However, numerous uncertainties exist regarding the pros and cons of vaccination, especially in patients with (immune-mediated) kidney diseases on immunosuppressive drugs. Here, members of the Immunonephrology Working Group (IWG) of the European Renal Association-European Dialysis and Transplant Association (ERA-EDTA) discuss thirteen frequently-asked questions regarding safety and efficacy of the most promising vaccine candidates. Post-marketing surveillance should be performed to estimate the rate of vaccine response (humoral and cellular) of different vaccine platforms, and surveillance of disease activity following administration of COVID-19 vaccines. Some of the candidates induce signaling pathways which also promote autoimmune kidney diseases, e.g. type I interferons in systemic lupus erythematosus. Efficacy estimates would thus far favor the use of selected COVID-19 vaccines, such as BNT162b2, mRNA-1273 or Gam-COVID-Vac. Humoral immune response after vaccination should be monitored using appropriate assays. Even in the absence of neutralizing antibodies patients might be protected by a sufficient cellular immune response capable to reduce severity of COVID-19. A reduced vaccine response after the use of CD20-depleting agents is anticipated, and it is particularly important to discuss strategies to improve vaccine response with these patients. Distancing and shielding measures remain important as not all vaccines fully protect from coronavirus infection. In-depth information about the most pressing vaccine questions is essential to reduce vaccine hesitancy of patients.

We do recommend vaccination for everyone (except for those with known allergic reactions to any of the vaccine components).

Patients with immune-mediated disease have typically been excluded from all major trials and data on vaccine efficacy, particular safety (relapse/recurrence risk) and specific adverse events will only become available during the ongoing pharmacovigilance studies. CDC interim clinical guidance states: "Immunocompromised individuals may still receive COVID-19 vaccination if they have no contraindications to vaccination. However, they should be counseled about the unknow vaccine safety profile and effectiveness in immunocompromised populations, as well as the potential for reduced immune responses" [9] . The potential of COVID-19 vaccines to induce immunity protecting from severe COVID-19 should outweigh potential risks in most cases.

Full trial publications of BNT162b2 (Pfizer-BioNTech), mRNA-1273 (Moderna), and Gam-COVID-Vac (Sputnik V, Gamaleya) showed a high efficacy on preventing symptomatic and severe COVID-19, while the duration of protection and the potential of the available vaccines to prevent asymptomatic SARS-Cov-2 infection has not yet been fully explored. It is also not known, if any single vaccine offers advantage for specific patient populations.

Published trials with efficacy estimates included a "healthy" population, with co-morbidities present in 20.9% of participants in the BNT162b2 trial (0.7% with "renal disease") [7] , in a small proportion of participants in the mRNA-1273 trial (9.5% with diabetes, 5.0% with significant cardiac disease, and chronic lung disease in 4.7%) [6] , a similar frequency in the ChAdOx1 nCoV-19 trial (respiratory disease 9.9%, cardiovascular disease 12.6%, and diabetes in 2.8%) [10] [11] and Gam-COVID-Vac trial (concomitant diseases in 24.7%) [8] . Vaccine efficacy in patients with immune-mediated diseases needs to be defined. Estimates of vaccine protection of different platforms are summarized in Table 1 . A specific discussion about differences in trial design and the difference between cellular and humoral immunity is necessary to reduce the existing uncertainty whether a specific vaccine is more effective than others. Importantly, all vaccine candidates showed high efficacy to prevent severe COVID-19 including hospitalizations ( Table 2 ). The total number of severe/hospitalized cases was low, given the selection of the study population.

Efficacy endpoints in the BNT162b2 trial included development of COVID-19 seven days after the second dose (28 days after administration of the first dose) as primary endpoint and severe COVID-19 after the first dose as major secondary endpoint. COVID-19 occurred in 8 patients after the second dose in the BNT162b2 arm compared to 162 trial participants in the placebo arm. These results were consistent among older participants (≥ 65 years; or 75 years) and those considered at risk, defined by having a comorbidity. Severe COVID-19 occurred in one participant randomized to receive the vaccine as compared to 9 in the control arm [7] . The primary endpoint in the mRNA-1273 vaccine trial was defined as SARS-CoV-2 infection two weeks after the second dose (42 days after the first dose). The endpoint was reached by 196 cases, 11 in the mRNA-1273 arm and 185 cases in the placebo group. These findings were consistent across defined subgroups (age, sex, race and ethnic group). Severe COVID-19 occurred in 30 participants, of whom all were assigned to receive placebo. Seven COVID-19 cases were reported after the first mRNA-1273 dose compared to 46 cases in the placebo arm [6] .

The primary objective of the ChAdOx1 nCoV-19 trial was to evaluate the efficacy of the vaccine against nucleic acid amplification test-confirmed COVID-19. Combined efficacy analysis fourteen days after the second dose included patients receiving a low-dose/standarddose (LD/SD) and SD/SD vaccine strategy. Thirty cases (0.5%) among 5807 participants in the ChAdOx1 nCoV-19 group and 101 cases (1.7%) in the control group contracted symptomatic COVID-19, resulting in a vaccine efficacy of 70.4% [10] . Further investigations indicated that a higher vaccine efficacy can be obtained with a longer prime-boost interval, with a vaccine efficacy of 82.4% when the second dose was delayed by 12 weeks or more in comparison to 54.9% in those with a delay below 6 weeks. A similar frequency of asymptomatic infections was reported in both arms, indicating that there is suboptimal protection against transmission of SARS-CoV-2 [11] . No peer-reviewed information is however currently present in participants older than 55 years. Concerns have been raised that the ChAdOx1 nCoV-19 trials included too few elderly trial participants to inform about efficacy. Relevant data will be obtained from real-world experience and ongoing investigations in the UK and Israel, that started earlier than others their vaccination programs. Several authorities have advised against its use in people over 65 years [12] . This hesitancy to use ChAdOx1 nCoV-19 in most vulnerable age groups might also be extended to people with underlying medical conditions, such as patients with immune-mediated kidney diseases where a lower seroconversion rate to vaccination needs to be expected. Nonetheless, preliminary real-life data from Scotland indicated that ChAdOx1 nCoV-19 prevents COVID-19 related hospitalizations even in elderly populations. Twenty-one days after the first dose of Gam-COVID-Vac (Sputnik V, rAd26 at day 0 and rAd5 at day 21), a 91.6% vaccine efficacy was shown. The observed vaccine efficacy was consistent among different age groups, with 91.8% efficacy reported in participants older than 60 years. Importantly, no moderate or severe cases of COVID-19 were reported in the vaccine arm, while 20 such events were recorded in the placebo group [8] . Based on the efficacy estimates provided by the published phase 3 trials, patients with immunemediated kidney diseases should receive the most effective vaccines to improve chances of an adequate protection from COVID-19. Based on this criterion, we would recommend the use of BNT162b2, mRNA-1273 or potentially Gam-COVID-Vac.

Antibodies are decreasing over time, so theoretically there is a benefit, but data on the number of booster injections and an optimal time-point for vaccination after infection are scarce.

As vaccine rollout is slow in most countries and vulnerable patient groups are not being vaccinated in a satisfactory speed, it may be argued that it is unethical to prioritize patients with recent infection and the presence of antibodies. An argument to pursue vaccination is the possibility of reinfection. Single reinfection cases have been reported. These patients did not exhibit immunodeficiency and antibodies to SARS-CoV-2 after the first infection were either absent or not tested. Two of the four cases had a worse disease outcome at reinfection, further underlining that the first infection does not provide lifelong immunity [13] . However, with new mutations evolving the risk of reinfection is real [14] . Persistence of SARS-CoV-2 infections has been reported in patients receiving immunosuppressive drugs, and in particular with rituximab therapy [15, 16] . It has to be determined whether a single dose as a "booster" is sufficient to mount an adequate response and protect against reinfection. Recent data suggest that administration of a single vaccine dose of BNT162b2 or mRNA-1273 in individuals with pre-existing immunity leads to an antibody response which is equal to or even exceed titers found in naïve individuals following their second dose [17] .

States of immunodeficiency, hereditary or acquired, can reduce vaccine responses. A recent dose of rituximab or higher doses of other immunosuppressants may specifically impair vaccine responses. Likely, it is wise for many patients to wait with vaccination until steroid doses are tapered to below 20 mg prednisone equivalent a day and 6 months have eclipsed since last rituximab dose.

There is a paucity of data regarding COVID-19 vaccine reponses in patients with immunemediated kidney diseases. A study of 56 patients with systemic lupus erythematosus (SLE) with low SLEDAI scores indicated that patients had fewer seroconversions or 4-fold titer rises for influenza A/H1N1 and A/H3N2 compared to healthy controls. Response defined as titers ≥40 to influenza A/H3N2 was especially diminished in patients receiving azathioprine [18] . Similarly, in patients with granulomatosis with polyangiitis (GPA) with a good disease control, high seroconversion rates were reported, while seroconversion to A/H1N1 and geometric mean titers were lower in comparison to controls. Patients were either off or had a low intensity of immunosuppression during the study period [19] . Based on these findings, the response to COVID-19 vaccines may be sufficient in patients with low grades of disease activity and no or minimal immunosuppression. A particular concern during the COVID-19 pandemic is the use of rituximab in several immunemediated kidney diseases. Analysis of the COVID-19 Global Rheumatology Alliance indicated that 42/192 (21.9%) of rituximab users died of COVID-19, corresponding to an over 4-fold higher odds ratio of death when methotrexate is used as a reference. No in-depth information about diagnoses, disease state (new diagnosis, flare or maintenance stage) or concomitantly used treatment is given [4] . It is important to acknowledge that most patients survive COVID-19 after rituximab treatment, while there is a need to determine risk factors which are indicative of a poor disease course following rituximab. Rituximab impairs humoral immunity and vaccine response is diminished within the first months of administration. Subdividing patient groups in early vaccination (4-8 weeks) and late vaccination (6-10 months) following rituximab in rheumatoid arthritis showed that the early vaccination group did not exhibit an IgM or IgG response following influenza vaccine administration, while a significant IgG response (2.82fold) was observed in patients receiving the vaccine 6-10 months after rituximab [20] . Fourfold titer increase was achieved in only 2/12 patients receiving an influenza vaccination 7-9 months following rituximab [21] . Thus, a few months should have eclipsed between rituximab administration and vaccination, with an ongoing B cell repopulation that indicates the potential of a humoral vaccine response [22] . Nonetheless, it is unclear thus far, if an impaired humoral vaccine response is tantamount to no protection against COVID-19 at all, or if patients may still be protected against severe disease forms by other mechanisms such as cellular immunity. Vaccination early after rituximab should be weighed against the individual risk of infection with all potential sequela. In kidney transplant recipients, the seroresponse rate after influenza vaccination decreased in a dose-dependent manner in patients receiving mycophenolate mofetil (MMF), while seroprotection was comparable to non-MMF users [23] . This implies that response to vaccines may be appropriate, but the quality of immune response may be impaired and likely depends on the dose of MMF used. Belimumab, which is increasingly used in the management of SLE, was not associated with increased odds of death (1/27), although cautious interpretation is necessary given the number of studied patients [4] . Analysis of a SLE cohort indicated that the addition of belimumab to other treatment modalities did not further impair vaccine response to a 13-valent pneumococcal conjugate vaccine [24] . Limited information is available on the vaccine response in patients currently taking high doses of corticosteroids. In patients with chronic obstructive pulmonary disease, a systemic corticosteroid dose over 10 mg / day did not impair the response to a 23-valent pneumococcal polysaccharide vaccine [25] . In children with nephrotic syndrome, the response to a hepatitis B vaccine was comparable among children without and with (0.4-0.5 mg/kg body weight on alternate days) corticosteroid prescription [26] . Taken together, vaccine antibody response can be expected to be blunted in patients that recently received rituximab, while the impact on cellular immunity needs to be determined. Anti-metabolites impaired the quality of vaccine response following influenza vaccination. The effects of high doses corticosteroids on immune response need to be determined but we do not recommend administrating a COVID-19 vaccine in situations where high doses of steroids are needed.

The approved vaccines are generally well tolerated. Some report "flu-like symptoms" for one or several days following the second dose. Local reactions are frequently reported as with other vaccines.

Based on the currently available data, COVID-19 vaccines in general population seem to be safe. Pharmacovigilance is essential to obtain information about side effects in a real-life setting. In Norway, 23 very frail elderly patients died following BNT162b2 administration [27], but this might have been coincidental. In this regard, a discussion on approved vaccines with a focus on the safety profile is essential to provide relevant information and reduce vaccine hesitancy. In the BNT162b2 phase 3 trial, systemic reactogenicity to the vaccine was more frequent in recipients in the younger age group (16 to 55 years of age). Fatigue and headache were reported in over 50% of trial participants following the second dose. Fever ranging between 38.9 to 40°C was reported in 0.2% and 0.8% after the first and second vaccine dose, respectively. Serious adverse events related to BNT162b2 were reported in 4 (0%) of trial participants, while the overall rate of severe and life-threatening adverse events did not differ between both groups [7] . An increase in severity of systemic events was also found following the second dose in trial participants receiving mRNA-1273, and both injection-site and systemic adverse events were more common among younger participants (16 to <65 years of age). Serious related adverse events were reported more frequently in the mRNA-1273 group in comparison to the placebo arm (6 and 4, respectively). A similar frequency of serious adverse events were reported for mRNA-1273 and placebo-treated participants (147 and 153), with no reported increase in autoimmunity [6] . Serious adverse events were reported in 79 (0.7%) of participants receiving ChAdOx1 nCoV-19 in comparison to 89 events (0.8%) in the control group receiving MenACWY (meningococcal group A, C, W, and Y conjugate vaccine). Potential immune-mediated conditions (such as Crohn's disease, ankylosing spondylitis, and vasculitis rash) were reported in 13 participants in the ChAdOx1 nCoV-19 arm, while 16 such events were recorded in the comparator arm [10] . "Flu-like illness" was the most common side effect following Gam-COVID-Vac administration. Allergic reactions were balanced, and no increase in immune-mediated disease was reported [8] .

Patients with autoimmune diseases were excluded in the early studies. There are insufficient data, but the vaccines seem to be safe and experience from previous vaccine studies does not indicate an increased risk for relapse/recurrence. Most immune-mediated kidney diseases have a relapsing-remitting disease course. The benefits of vaccination outweigh the risk of relapse/recurrence induced by a specific COVID-19 vaccine, as there is a high probability to be protected against severe COVID-19 disease. No increase in SLEDAI scores was found 30 days after influenza vaccination in SLE patients, independent of prescribed treatment modality [18] . Thirty-one patients with anti-neutrophil cytoplasmic antibody (ANCA)-associated vasculitis in remission were randomized to receive either an influenza vaccine or no vaccine. During the follow-up period, there was no change in ANCA titer or inflammatory parameters, and only a single disease relapse episode was recorded in a patient with microscopic polyangiitis 6 months after influenza vaccination [28] , an event unlikely to be associated with the vaccine. A post-marketing surveillance study found a 3.6fold higher incidence of nephrotic syndrome in the year post-vaccination with the 4CMenB vaccine, with the report of 4 cases among 49,000 vaccinated patients [29] .

In conclusion, the risk to develop de novo or relapsing/recurring disease following COVID-19 vaccine administration seems to be low. Several pathways known to be implicated in vaccine response, i.e. Toll-like receptor 7 (TLR7) or production of type I interferon [30] , are also induced in autoimmunity (i.e. in SLE) [31] and thus might pre-dispose patients to disease relapse. Follow-up within registries focusing on immune-mediated kidney diseases (IRoc-GN, COV-GN or others) is necessary to estimate the individual risk of disease flare following COVID-19 vaccination.

In general, "yes", the whole process is supervised. We advise against the use of currently available vaccines in patients with known PEG or polysorbate allergies.

Authorities have issued warnings that individuals with known history of severe allergic reactions to any of the components of the COVID-19 vaccines should not be vaccinated. In case of known other allergies, patients should be monitored for a period of 30 minutes post vaccination, all others should be observed for 15 minutes. Post-marketing experience revealed that among the first 1.9 million doses of BNT162b2 administration, 21 events consistent with anaphylaxis were reported. Anaphylaxis is a rare event, but a risk assessment prior to vaccination should be performed and if allergic to PEG, patients may be ineligible to use a mRNA vaccine. Both, BNT162b2 and mRNA-1273, use excipient PEG to stabilize the lipid nanoparticle containing the mRNA, while the ChAdOx1 nCov-19 and Ad26.COV2.S vaccines use excipient polysorbate 80 as a stabilizer. If a patient develops anaphylaxis after the first dose, it may be justified to withhold the second dose or perform PEG skin testing to evaluate if a second dose can be administered or not [32] . As there is an expanding COVID-19 vaccine platform, patients with known severe anaphylaxis may be vaccinated once other candidates become available.

For now, there is no information about the longevity of immunity following vaccination. Booster injections may become necessary to maintain anti-SARS-CoV-2 immunity. Viral mutations are frequent, and newer/modified vaccines may be used to protect against these variants.

In patients with immune-mediated diseases, a significant decline in antibody levels can be expected between 3 and 6 months (as discussed above). Antibody levels may be measured during routine controls as we need to understand the impact on presence of neutralizing antibodies on risk of SARS-CoV-2 infections and severity.

A particular concern is the development of "escape mutations", the change of the Spike-protein shape and a potential loss of specific neutralizing antibody binding sites induced by COVID-19 vaccines. Wide-spread sequencing has revealed new variants which have been detected worldwide and are characterized by a higher transmissibility. These new variants include B.1.1.7 (the "UK" strain) and B.1.351 or N501Y.V2 (the "South African" variant). A reported lower activity and efficacy of mRNA vaccine-induced neutralizing antibodies, and a lower efficacy in trials reported for other vaccines (NVX-CoV2373, ChAdOx1 nCoV-19, and Ad26.COV2.S) [33, 34] . It is likely that COVID-19 vaccines need to be adjusted to accommodate key sequence changes of these new variants [34] . Thus, regular vaccinations comparable with seasonal influenza vaccination combating new variants may be necessary.

Yes, with the approval of more vaccines, there could be other options (such as respiratory booster vaccines under investigation), which might induce immunity.

We expect that patients on immunosuppressive drugs develop reduced and sometimes insufficient vaccine responses in comparison to individuals without these treatments. Strategies to overcome such impaired response need to be determined and are speculative at this time. Different COVID-19 vaccines will allow administration of several candidates. Absence of seroconversion may not reliably indicate a lack of protection from severe COVID-19. Cellular immunity may still be present but is more difficult to assess. Cytotoxic CD8 + T cells are involved in viral clearance. The relevance of CD8 + T cells was underlined by the finding that subjects with milder COVID-19 disease exhibited a greater number of memory CD8 + T cells in the respiratory tract in comparison to severe cases. A potent CD8+ T cell response is induced by replication-defective viral-vectored vaccines, while it depends on the adjuvant used and formulation of mRNA-based vaccines and shows a weak response upon vaccination with a protein subunit [35] . T cell responses to a variable degree were shown for BNT162b2, mRNA-1273 and ChAdOx1 nCoV-19 [36] [37] [38] . In non-human primates, the intranasal administration of adenovirus-vectored vaccines resulted in reduced shedding, a reduction of viral load in the respiratory tract and a prevention of SARS-CoV-2 infection [39] [40] [41] . Thus, in patients with a non-detectable humoral immunity, T cell response may be measured when possible (i.e. by ELISPOT techniques [42] ) as a cellular immune response may protect against infection or eventually reduce the probability of severe disease courses.

No such interactions are expected.

Based on our current understanding of mode of action of approved vaccines, no interactions between the COVID-19 vaccines and immunosuppression used in patients with immunemediated kidney diseases are expected.

Vaccinated patients should continue to follow current guidance to protect themselves from exposure to COVID-19. Providing the vaccine to patients and their caregivers will reduce risk for infection or clinical COVID-19 disease, but they must continue practices of wearing masks, social distancing, and maintaining good hand hygiene even after vaccination.

At present, there is no evidence that mounting an adequate vaccine response protects others and one might still transmit and contract COVID-19, even if the severity of infections might be reduced. It is important to continue shielding measures, and these should be adapted according to one's individual risk. Vaccination at first protects the vaccinated person from severe COVID- 19 . To what extend the currently available vaccines can help to reduce viral transmission and hence case numbers in the population as a basis for public containment measures, is currently unclear.

There should be a delay of at least two weeks before you should receive your COVID-19 vaccine. We advise that non-urgent vaccinations may be postponed, with the exception of meningococcal/pneumococcal vaccination when eculizumab/ravulizumab are used.

We advise that annual or regular vaccinations are still performed. The year 2020 has seen a dramatic decrease in cases with influenza [43] , presumably due to measures such as washing hands and wearing a mask. Influenza vaccination during the 2019/2020 winter season led to significantly fewer SARS-CoV-2 infections among hospital employers and the general population [44] [45] [46] , indicating that "trained immunity" may play a role in one's individual susceptibility to contract COVID-19. Other vaccines which are not deemed urgent should be postponed and should not be administered within 2 weeks prior/after receipt of the COVID-19 vaccine. Urgent vaccinations include vaccinations against meningococcal/pneumococcal strains when eculizumab or ravulizumab is used in the management of immune-mediated kidney diseases.

This is unclear at the moment. The formation of antibodies is perceived as a surrogate biomarker for antiviral protection but whether the detected antibodies are of a neutralizing type or whether protective immunity is present even at low or absent antibody levels will remain uncertain. Therefore, antibody testing has of yet not generally been recommended.

Most individuals exhibit a strong antibody response following COVID-19 vaccine administration. Eight weeks after receiving a second dose of mRNA-1273 or BNT162b2, high levels of spike protein (S) and receptor binding domain (RBD) neutralizing antibodies were detected [47] . Notably, S1-specific and virus neutralization antibody titers were higher in participants receiving BNT162b2 in comparison to samples of participants following a SARS-CoV-2 infection. Antibody levels peaked around day 29 (a week after the booster dose) and decreased over time but remained above the level of sera from convalescent patients 63 days after the booster dose [48] . A small subset of patients receiving Gam-COVID-Vac had a measurement of RBD and neutralizing antibodies by day 42. Seroconversion rate was close to 100% and the results indicated that antibody response was comparable among different age groups [8] . The published trials did not provide antibody measurements of participants who contracted COVID-19 following vaccination. Thus, there is no information if antibody formation elicits protection against COVID-19, or if specific antibody levels are indicative of protection. Further research in this field is necessary, but we can expect that patients with ongoing immunosuppression will have lower antibody levels compared to healthy subjects. 

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Persisting SARS-CoV-2 viraemia after rituximab therapy: two cases with fatal outcome and a review of the literature

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Wegener's granulomatosis patients show an adequate antibody response to influenza vaccination

Rituximab impairs immunoglobulin (Ig)M and IgG (subclass) responses after influenza vaccination in rheumatoid arthritis patients

Rituximab-treated patients have a poor response to influenza vaccination

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Influenza vaccination is efficacious and safe in renal transplant recipients

Treatment with belimumab in systemic lupus erythematosus does not impair antibody response to 13-valent pneumococcal conjugate vaccine

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