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Systematic Review
Revised

A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals

[version 2; peer review: 2 approved]
Soniya A. Malik1, Kavindiya Modarage1, Paraskevi Goggolidou
https://orcid.org/0000-0001-9711-7747
1
Soniya A. Malik1, Kavindiya Modarage1, Paraskevi Goggolidou
https://orcid.org/0000-0001-9711-7747
1
PUBLISHED 22 Nov 2022
Author details Author details
OPEN PEER REVIEW
REVIEWER STATUS

This article is included in the Emerging Diseases and Outbreaks gateway.

Abstract

Background: SARS-CoV-2 is a coronavirus that has rapidly spread across the world with a detrimental effect on the global population. Several reports have highlighted an increased mortality rate and a higher severity of COVID-19 infection in chronic kidney disease (CKD) individuals. Upon the development of various SARS-CoV-2 vaccines, mRNA vaccines including BNT162b2 and mRNA-1273 were deemed safe, with a high efficacy in preventing COVID-19 in the general population. This review investigates whether  SARS-CoV-2 mRNA vaccines are as effective in triggering an immune response in Dialysis Patients (DPs) and Kidney Transplant Recipients (KTRs) and if a third dose is required in this  population.
Methods: A systematic search employing the PRISMA criteria was conducted in several major databases, with the data being extracted from publications for the period January 2021 to May 2022 (PROSPERO: CRD42022338514, June 15, 2022).
Results: 80 studies were included in this analysis with a total cohort number of 15,059 participants. Overall, 85.29% (OR = 17.08, 95% CI = 15.84-18.42, I2 = 98%) and 41.06% (OR = 0.52, 95% CI = 0.48-0.5, I2 = 95%) of DPs and KTRs included in this review showed positive seroconversion after two doses of either mRNA vaccine, respectively. A total 76% (OR = 6.53, 95% CI = 5.63-7.5, I2 = 96%) of the cohort given a third dose of an mRNA vaccine demonstrated positive seroconversion, with 61.86% (OR = 2.31, 95% CI = 1.95-2.75 I2 = 95%) of the cohort that was assessed for a cellular response displaying a positive response.
Conclusions: This data emphasises a reduced incidence of a positive immune response in DPs and KTRs compared to healthy controls, albeit a better response in DPs than when compared to KTRs alone was observed. A third dose  appears to increase the occurrence of an immune response in the overall DP/KTR cohort.

Keywords

Chronic Kidney Disease, COVID-19, Dialysis, IgAN, mRNA Vaccines, Kidney Transplant

Corresponding author: Paraskevi Goggolidou
Competing interests: No competing interests were disclosed.
Grant information: The author(s) declared that no grants were involved in supporting this work.
Copyright:  © 2022 Malik SA et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
How to cite: Malik SA, Modarage K and Goggolidou P. A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals [version 2; peer review: 2 approved]. F1000Research 2022, 11:909 (https://doi.org/10.12688/f1000research.122820.2) First published: 08 Aug 2022, 11:909 (https://doi.org/10.12688/f1000research.122820.1) Latest published: 22 Nov 2022, 11:909 (https://doi.org/10.12688/f1000research.122820.2)

Revised Amendments from Version 1

The revised version has incorporated the reviewers comments and it is addressing the issue of antibody thresholds, positive seroconversion in DPs and KTRs and antibody titers for the kits that were examined in this study. A new Table 1 was added.

See the authors' detailed response to the review by Katherine Karakoula
See the authors' detailed response to the review by Marios Papasotiriou

Introduction

In December 2019, an outbreak of atypical respiratory disease was reported in Wuhan, Hubei Province, China (Kumar et al., 2021). This was later confirmed to be caused by a novel coronavirus, formally recognised by the World Health Organisation (WHO) as Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) or Coronavirus Disease-2019 (COVID-19) (Tsang et al., 2021). SARS-CoV-2 rapidly spread across the globe, with WHO declaring it a Public Health Emergency of International Concern (PHEIC) on January 30, 2020 (Cucinotta and Vanelli, 2020). Shortly after, COVID-19 was declared a pandemic by WHO on March 11, 2020, with current data from WHO reporting a cumulative total number of 521,920,560 cases and 6,274,323 total deaths as of May 23, 2022 (Cucinotta and Vanelli, 2020; WHO Coronavirus (COVID-19) Dashboard).

SARS-CoV-2 is a β-coronavirus; coronaviruses consist of enveloped, positive-sense, single-stranded RNA, and non-structural, structural and accessory proteins (Chan et al., 2020; Yadav et al., 2021). Each of these proteins play a crucial role in the process of viral-host invasion. In the initial stages of infection, the spike (S) protein is a crucial factor for viral entry. The S protein is composed of two functional subunits, S1 and S2. The S1 subunit of the S protein in SARS-CoV-2 is responsible for binding to the cellular ligand on Angiotensin Converting Enzyme 2 (ACE2) receptor on the host cell surface (Tsang et al., 2021; Yuki, Fujiogi and Koutsogiannaki, 2020; Hoffmann et al., 2020; Li et al., 2003). Following this interaction, transmembrane protease serine 2 (TMPRSS2) plays a crucial role in priming the S1/S2 cleavage site, leading to the stabilisation and subsequent cleavage of the S2 subunit (Hoffmann et al., 2020; Tsang et al., 2021; Belouzard, Chu and Whittaker, 2009). This presumably activates the S protein, facilitating the viral and host cell membrane fusion (Belouzard, Chu and Whittaker, 2009; Hoffmann et al., 2020; Ou et al., 2020). Upon cell entry, the replicase complex begins the process of transcription and translation, leading to the synthesis of new viral RNA and proteins. At this stage, the nucleocapsid (N) protein will begin virion assembly and bind new genomic RNA, whilst the S, envelope (E) and membrane (M) structural proteins, which comprise trafficking signal sequences, translocate to the endoplasmic reticulum (Chang et al., 2005; Chen, Liu and Guo, 2020; Yadav et al., 2021; Tsang et al., 2021). The M protein plays a crucial role in shaping virions and binding to the nucleocapsid, whilst the E protein then plays a direct role in viral pathogenesis, assembly and eventual release out of the cell via exocytosis (Neuman et al., 2011; Chen, Liu and Guo, 2020; Yadav et al., 2021).

The initial point of entry for SARS-CoV-2 is the respiratory tract, where the virus will enter and bind to nasal epithelial cells in the upper respiratory tract, via ACE2 (Sungnak et al., 2020). ACE2 is expressed in several organs including the heart, lungs and intestine (Tsang et al., 2021; Zou et al., 2020). Importantly, the highest levels of expression of ACE2 can be found in the kidneys, especially in renal tubular cells (Hamming et al., 2004). However, it has been reported that ACE2 expression can vary within kidney disease and renal transplant patients, with a reduced level of ACE2 expression also reported in diabetic nephropathy (Tikellis et al., 2003; Lely et al., 2004). Upon investigation, one in vivo study highlighted that chronic pharmacologic inhibition of ACE2 could worsen glomerular injury (Soler et al., 2007). Kidney cells also express TMPRSSs, a co-receptor to viral entry (Chen et al., 2021). Since the kidney is a target organ for SARS-CoV-2, viral invasion and consequent replication in kidney cells have the potential to trigger a cytokine storm, initiating possible organ damage in patients (Jin et al., 2020). Population studies revealed that older patients were more prone to a severe clinical outcome alongside those who were clinically vulnerable and suffered from conditions including but not limited to diabetes, cardiovascular disease (CVD) and chronic kidney disease (CKD) (Hu and Wang, 2021; Gansevoort and Hilbrands, 2020).

Developing research has quickly recognised that CKD patients are more susceptible and prone to developing severe outcomes due to SARS-CoV-2 infection. High mortality risk was associated with CKD for patients with eGFR <30 mL/min/1.73 m2 (adjusted hazard ratio (aHR) 2.52), dialysis patients (aHR 3.69) and transplant patients (aHR 3.53), constituting some of the top risk categories in this study (Williamson et al., 2020). Similar to this, the 28-day mortality was 20.0% (95% confidence interval (CI) 18.7% - 21.4%) and 19.9% (17.5% - 22.5%) in 3285 dialysis patients (DPs) and 1013 kidney transplant recipients (KTRs), respectively (Jager et al., 2020). Another meta-analysis established a higher mortality rate in CKD patients with COVID-19 infection compared to those without COVID-19 infection (pooled OR 5.81 (95% CI 3.78 – 8.94)) (Cai et al., 2021).

Nearing the end of 2021, several SARS-CoV-2 vaccines have emerged for use with authorisation across the globe. According to WHO, as of May 17, 2022, a total of 12,186,798,032 vaccine doses have been administered (WHO Coronavirus (COVID-19) Dashboard). Despite several studies investigating the safety and efficacy of vaccinations, there is no conclusive evidence as to whether the SARS-CoV-2 vaccines provide the same level of immunity in CKD patients. Overall, it has been deemed safe to use the mRNA vaccines BNT162b2 (Pfizer-BioNTech) and mRNA-1273 (Moderna) in immunocompromised patients, including CKD patients (Windpessl et al., 2021). Clinical trials have detected a higher level of efficacy in mRNA vaccines compared to viral-vectored vaccines (95% for BNT162b2, 94.1% for mRNA-1273, 70.4% for ChAdOx1 nCoV-19) (Baden et al., 2021; Polack et al., 2020; Voysey et al., 2021). All three vaccines have got the ability to induce a strong S-specific antibody response followed by T-cell immunity after two parenteral injections (Folegatti et al., 2020; Jackson et al., 2020). However, since characteristics such as kidney disease, and dialysis treatment/transplantation could affect vaccination efficacy, this study will focus on investigating the evidence on whether the SARS-CoV-2 mRNA vaccines can indeed provide effective immunity to CKD individuals and if further action is required.

Methods

Search strategy and eligibility criteria

This systematic review was conducted in accordance with Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, published in 2020. See Reporting guidelines (Goggolidou, 2022) for the completed checklist. The study was registered in PROSPERO: CRD42022338514, on June 15, 2022 (Page et al., 2021). A preliminary search was first conducted on PubMed for publications detailing the efficacy of SARS-CoV-2 vaccination in CKD patients to validate the research question. This was followed by a systematic search by two independent reviewers which was last conducted on May 23, 2022 on PubMed, Google Scholar, Semantic Scholar, CORE, Science Open and BioMed Central using search terms and phrases of ‘efficacy of COVID-19 vaccine’, ‘immunogenicity of COVID-19 vaccine’, ‘chronic kidney disease’ and ‘COVID-19 booster’. Filters were applied whereby only studies published between January 2021 and May 2022 were included, with unpublished studies i.e. pre-prints also being included in this analysis. Inclusion and exclusion criteria were defined to ensure all relevant studies were identified. Only studies with an adult human cohort of any sex and published in any country were included. Patients under the age of 18 were excluded from this analysis. As well as this, studies or trials that specify the vaccine type including BNT162b2 and mRNA-1273 vaccinations were only included. Patients who received any other form of COVID-19 vaccine were excluded, since there was limited information available. The studies must have also mentioned at least the treatment regimen that patients were undertaking including dialysis or transplantation. If this was unclear, studies were excluded. Studies were grouped into categories according to the treatment regimen patients undertook and the vaccine that patients were given, including the number of doses. As well as this, studies were separated according to the type of analysis that was undertaken i.e., seroconversion and/or cellular analysis.

Data extraction

Studies were grouped together as described above with two independent reviewers assessing whether they met the inclusion criteria (S.A.M, K.M). Studies were assessed and data was collected via Microsoft Excel 2016 by the same reviewers. The information extracted included sample size and sample groups, treatment regimen, number of doses, whether there is a history of COVID-19 and how long after vaccination any assessments took place. The effects and responses to the vaccination including humoral and cellular immunity responses after the second and third doses were also reviewed (the PRISMA flow diagram is given as Figure 1). Any disputes were overlooked by P. G. Studies with missing or unclear data were removed from the analysis. The risk of bias and heterogeneity were assessed with the Cochrane’s Q test and I2 test using RevMan (version 5.4) by two independent reviewers (S.A.M, K.M).

ea37e890-29d4-4b1a-b7b3-42c021f4df52_figure1.gif

Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement demonstrating the different phases of study selection of the systematic review.

Data analysis

Two independent reviewers assessed studies for eligibility for each synthesis using Microsoft Excel 2016. Studies were grouped in accordance with data availability before being included in the synthesis, with those with missing data being excluded from analysis. Funnel plots, forest plots and statistical analysis were performed using RevMan (version 5.4). Odds ratios (OR) and 95% confidence intervals (CI) were calculated to evaluate the seroconversion and cellular response in DPs and KTRs after two and/or three doses of the BNT162b2 and mRNA-1273 vaccinations. The seroconversion is a measure of antibody response to SARS-CoV-2-specific antibodies including IgG, IgA, and IgM antibodies. The cellular response incorporated the number of patients that developed a T-cell response across the studies included in this analysis, including CD4+ and CD8+ T cells. The population was divided into subgroups i.e., dialysis patients and transplant recipients; two dose and three dose groups; seroconversion and cellular response group. A pooled 95% CI not including 1 for the OR was considered as statistically significant. Risk of bias/heterogeneity was assessed using RevMan (version 5.4) with the Cochrane’s Q test and I2 test and presented in funnel and forest plots. If a P value of < 0.1 and/or I2 was > 50%, heterogeneity was determined as significant.

Results

A total of 80 studies (76 published, 4 preprints) were included in this work, with an overall cohort number of 15,059 participants. Of these, 11,509 participants were recipients of the BNT162b2 vaccine, with 4,263 being KTRs and 7,246 participants being DPs. Separately, a total of 3,550 participants were vaccinated with the mRNA-1273 vaccine. Of these, 826 participants were KTR, and 2,724 participants were DP. Finally, 292 participants had been given the ChAdOx-1 nCoV-19 vaccination, with 11 participants being KTR and 281 participants being DP. Due to the lack of studies for ChAdOx-1 nCoV-19 vaccination in this population, this data was excluded from analysis and one study was ruled out (Meshram et al., 2021). Seroconversion and cellular response were assessed to investigate whether the mRNA vaccines were able to trigger a response in immunocompromised patients; to determine if a particular vaccine was more appropriate for DPs or KTRs; and to determine the ability of a third dose in inducing an antibody or cellular response in this population type.

57 studies with a total of 9,913 participants were included to determine how effective two doses of the mRNA vaccines, including BNT162b2 and mRNA-1273, were in DPs. Overall, the mRNA vaccines prove to be effective in inducing seroconversion, with around 85.29% of participants positively seroconverting. All but five studies in this cohort favoured positive seroconversion with the remaining 14.71% of participants favouring no seroconversion response (OR = 17.08, 95% CI = 15.84-18.42, Figure 2A). Significant heterogeneity was observed (P < 0.00001, I2 = 98%, Figure 2B).

ea37e890-29d4-4b1a-b7b3-42c021f4df52_figure2.gif

Figure 2. A total of 85% of Dialysis Patients (DPs) seroconvert after receiving two doses of a COVID-19 mRNA vaccine.

(A) Forest plot comparison of the number of DPs who seroconverted or had no response after two doses of an mRNA vaccination (OR = 17.08, 95% CI = 15.84-18.42, P < 0.00001, I2 = 98%). (B) Funnel plot evaluating heterogeneity when comparing seroconversion response in DPs after two doses of an mRNA vaccine. Significant heterogeneity was observed (P < 0.00001, I2 = 98%).

Comparatively, 33 studies with a total of 4,822 participants were included to determine the effectiveness of two doses of the mRNA vaccines including BNT162b2 and mRNA-1273 in KTRs. Compared to the seroconversion rate in DPs, the mRNA vaccines were not able to effectively trigger a positive seroconversion in the KTR population. 41.06% of participants displayed positive seroconversion, with the remaining 58.94% of participants showing no response (OR = 0.52, 95% CI = 0.48-0.56, Figure 3A). Significant heterogeneity was observed (P < 0.00001, I2 = 95%, Figure 3B).

ea37e890-29d4-4b1a-b7b3-42c021f4df52_figure3.gif

Figure 3. Only 41% of Kidney Transplant Recipients (KTRs) seroconvert after receiving a COVID-19 mRNA vaccine.

(A) Forest plot comparison of the number of KTRs who seroconverted or had no response after two doses of an mRNA vaccination (OR = 0.52, 95% CI = 0.48-0.56, P <0.00001, I2 = 95%). (B) Funnel plot evaluating heterogeneity when comparing seroconversion response in KTRs after two doses of an mRNA vaccine. Significant heterogeneity was observed (P <0.00001, I2 = 95%).

Aside from this, 17 studies with a total of 1,513 participants were included to determine the effectiveness of three doses of the mRNA vaccines, consisting of either the BNT162b2 or the mRNA-1273 in DPs and KTRs. The percentage of DPs and KTRs individuals who displayed positive seroconversion after a third dose of an mRNA vaccine was estimated at 89.13% and 61.29%, respectively. It should be noted however that due to the limited number of studies published, it was not possible to perform statistical analysis for separate DP and KTR individuals. Thus, statistical analysis was conducted on both DP and KTR individuals collectively.

Of the participants that were included in this assessment, 76% displayed seroconversion after three doses of an mRNA vaccine, with 24% of participants showing no response; multiple studies included in this analysis demonstrate a strong, positive seroconversion after a third dose of an mRNA vaccine (OR = 6.53, 95% CI = 5.63-7.58, Figure 4A). Significant heterogeneity was however observed (P < 0.00001, I2 = 96%, Figure 4B).

ea37e890-29d4-4b1a-b7b3-42c021f4df52_figure4.gif

Figure 4. After three doses of a COVID-19 mRNA vaccine, 76% of Dialysis Patients (DPs) and Kidney Transplant Patients (KTRs) seroconverted.

(A) Forest plot comparison of the number of DPs and KTRs who positively seroconverted after three doses of an mRNA vaccine (OR = 6.53, 95% CI = 5.63-7.58, P < 0.00001, I2 = 96%). (B) Funnel plot evaluating heterogeneity when comparing seroconversion in DPs and KTRs after three doses of an mRNA vaccine. Significant heterogeneity was observed (P < 0.00001, I2 = 96%).

Further to this, 12 studies with a total of 978 participants were included for this analysis to determine how many DPs and KTRs developed a cellular response after being vaccinated with two doses of either the BNT162b2 or mRNA-1273 vaccines. Overall, in this cohort, 61.86% of participants favoured an effective cellular response with a further 38.14% of participants showing no cellular response (OR = 2.31, 95% CI = 1.95-2.75) (Figure 5A), nevertheless significant heterogeneity was observed (P < 0.00001, I2 = 95%; Figure 5B).

ea37e890-29d4-4b1a-b7b3-42c021f4df52_figure5.gif

Figure 5. A total of 62% of Dialysis Patients (DPs) and Kidney Transplant Recipients (KTRs) elicited an effective cellular response following two doses of a COVID-19 mRNA vaccine.

(A) Forest plot comparison of the number of DPs and KTRs who developed a cellular response after two doses of an mRNA vaccine (OR = 2.31, 95% CI = 1.95-2.75, P < 0.00001, I2 = 95%). (B) Funnel plot evaluating heterogeneity when comparing cellular response in DPs and KTRs after two doses of an mRNA vaccine. Significant heterogeneity was observed (P < 0.00001, I2 = 95%).

It is important to note that it is not possible to deem immunity levels or identify protective thresholds from antibody testing alone. Further to this, we can confirm there is no specific antibody titre for protection against severe COVID-19. Upon performing an extensive review of the studies in this meta-analysis, antibody titres and thresholds varied significantly between studies due to the use of different immunoassays. Table 1 summarises some of the common types of immunoassays used and thresholds used to deem an individual seropositive.

Table 1. An overview of the commercially available kits used to assess seroconversion against COVID-19 and the thresholds that deem an individual seropositive per kit.

KitThreshold
AdviseDx SARS-CoV-2 IgG II Quant assay (Abbott)≥50 AU/mL
Anti-SARS-CoV-2 Quantivac ELISA (IgG), (Euroimmun)10 UR/mL
Anti–SARS-CoV-2 S enzyme immunoassay (Roche)> 29 U/mL - >200 U/mL
ARCHITECT IgG II Quant test (Abbott)>50 AU/ml
COVID-19 QuantiGEM SARS-CoV-2 IgG ELISA Kit (Biogem)>0.170 AU/mL
Elecsys anti-SARS-CoV-2 serological assay (Roche)≥1:50
Elecsys Assay (Roche) >250 AU/mL
Elecsys® Anti-SARS-CoV-2 immunoassay (Roche)>0.8 U/mL
Elecsys® Anti-SARS-CoV-2 S enzyme immunoassay (Roche)>0.80 U/mL or ≥15 U/mL
ELISA-based analysis of SARS-CoV-2 spike S1 domain–specific IgG and IgA (Euroimmun)Index >1.0
LIAISON SARS-CoV-2 S1/S2 IgG chemiluminescent assay>15.0 AU/mL
LIAISON SARS‐CoV‐2 S1/S2 IgG chemiluminescent assay against a recombinant Spike (S) protein (S1/S2)>12.0 AU/mL
LIAISON SARS-CoV-2 TrimericS IgG>13 AU/mL
QuantiVac ELISA assay (Euroimmun)≥35.2 BAU/mL
SARS-CoV-2 immunoassay (Abbott)≥660 AU/mL
SARS-CoV-2 immunoassay (Abbott)≥224 AU/mL
Siemens Atellica-IM SARS-CoV-2 immunoassayIndex >1.0
Siemens Healthineers Atellica IM SARS-CoV-2 IgG (sCOVG) assay>150 U/mL
US Food and Drug Administration–approved chemiluminescent assay (ADVIA Centaur XP/XPT COV2G)≥20 U/L
V-PLEX® SARS-CoV-2 Panel 2 (IgA) Kit≥50 AU/mL

It has also been reported that IgAN or other kidney diseases could be triggered as a response to the COVID-19 mRNA vaccinations in certain populations (Wisnewski, Campillo Luna and Redlich, 2021). IgA nephropathy (IgAN) is an autoimmune kidney disease characterised by the deposition of IgA in the glomerulus, which causes inflammation and damage in the kidney (Selvaskandan et al., 2019). We found five studies where it was reported that nine patients were diagnosed with IgAN or presented with hallmarks of IgAN, such as gross haematuria after having either the BNT162b2 or mRNA-1273 vaccine administered (Table 2). Of these, six patients had previously diagnosed IgAN, with a further two patients having no significant medical history besides gestational diabetes and hyperlipidaemia. The final patient also had no significant past medical history. Most of these individuals were female with an average age of ~42 years old, with one study not specifying the age of the female and instead, using the description ‘older woman’ (Perrin et al., 2021; Rahim, Lin and Wang, 2021; Tan et al., 2021; Sacker, Kung and Andeen, 2021; Negrea and Rovin, 2021). One case study reported the IgAN phenotype in a 22-year-old male (Perrin et al., 2021). Overall, five of these individuals were vaccinated with the BNT162b2 vaccine, with the remaining individuals having received the mRNA-1273 vaccination. There was a report of one separate case study where a 42-year-old woman who went into full remission after being diagnosed and treated for lupus nephritis class V in 2016, had relapsed a week after the first dose of the BNT162b2 vaccine. The patient went on to develop nephrotic syndrome with hyperlipoproteinemia and hypalbuminaemia (Tuschen et al., 2021). This data brings about the question as to whether there is a link between being vaccinated with an COVID-19 mRNA vaccine and the glomerulonephritis response and whether the COVID-19 mRNA vaccines are completely safe for use in certain vulnerable populations.

Table 2. Onset of IgAN in individuals after having the COVID-19 mRNA vaccines administered.

PatientAge/Gender/raceVaccine typePrevious IgAN history?Onset of gross haematuria after first doseOnset of gross haematuria after second doseCommentsReference
141yrs/FBNT162b2YesDay 2Did not receive second doseN/A(Perrin et al., 2021)
227yrs/FBNT162b2YesN/ADay 2N/A(Perrin et al., 2021)
352yrs/F/AsianBNT162b2YesN/AWithin 24hrsN/A(Rahim, Lin and Wang, 2021)
441yrs/F/ChineseBNT162b2NoN/AWithin 24hrsUnderlying gestational diabetes prior to vaccine. Undiagnosed IgAN revealed upon investigation(Tan et al., 2021)
560yrs/F/MalayBNT162b2NoN/AWithin 24hrsPatient diagnosed with Hyperlipidaemia prior to any vaccination. Crescentic glomerulonephritis revealed upon investigation.(Tan et al., 2021)
622yrs/MmRNA-1273YesDay 2 and Day 25Day 2N/A(Perrin et al., 2021)
7FmRNA-1273NoN/AWithin 2 weeksCrescentic glomerulonephritis revealed upon investigation.(Sacker, Kung and Andeen, 2021)
838yrs/F/WhitemRNA-1273YesN/A< 24hrsN/A(Negrea and Rovin, 2021)
938yrs/F/WhitemRNA-1273YesN/A< 24hrsN/A(Negrea and Rovin, 2021)

Discussion

This study set out to establish the efficacy of the COVID-19 mRNA vaccines in DPs and KTRs. The seroconversion and cellular response were assessed in 15,072 participants after either two or three doses of an mRNA vaccine. The vaccines that were included in this analysis include BNT162b2 and mRNA-1273, with ChAdOx-1 nCoV-19 being excluded due to lack of available data.

Of the 9,913 DPs that were assessed for seroconversion after two doses of an mRNA vaccination, 85.29% showed positive seroconversion, with 14.71% of participants displaying no response. Comparatively, in the 4,822 KTRs that were assessed, the response was deemed ineffective when compared to DPs. 41.06% of KTRs displayed positive seroconversion, with the remaining 58.94% of participants showing no significant response to the vaccinations after two doses.

We also assessed the seroconversion response after three doses of an mRNA vaccine. Of 1,513 participants, 76% of patients showed positive seroconversion with the remaining 24% of patients showing no response. It was not confirmed in the studies whether seroconversion after a third dose was compared to unvaccinated individuals or individuals who had received a second dose. Thus, in our study, we were unable to conclude whether there was an increase in antibody production after the third dose in those who did not show positive seroconversion after the second dose. When assessing cellular response in DPs and KTRs after two doses, 978 participants were included in the analysis, with a positive cellular response being observed in 61.86% of patients. The remaining 38.14% of participants showed no or little cellular response.

The BNT162b2 and mRNA-1273 vaccines both demonstrated a ~95% and ~94.1% efficacy at preventing COVID-19 in the general population respectively, during phase III clinical trials (ClinicalTrials.gov number: NCT04470427; ClinicalTrials.gov number: NCT04368728) (Polack et al., 2020; Baden et al., 2021). Comparatively, the seroconversion was also reported to be ~95% - 100% in healthy controls when fully vaccinated with either of the mRNA vaccines in four separate studies (Stumpf et al., 2021b; Ben-Dov et al., 2022b; Grupper et al., 2021; Sattler et al., 2021). Our findings have highlighted a reduced seroconversion rate when compared to healthy controls of 85.29% and 41.06% in DPs and KTRs, respectively, albeit a better response in DPs when compared to KTRs alone. This could be due to several factors that should be taken into consideration. For example, age may play a factor in individual response to the vaccinations, with some studies showing younger KTRs may respond better to vaccination (Broseta et al., 2021; Torreggiani et al., 2021). As well as this, it has also been highlighted that immunosuppression can impair immunity to COVID-19, with post-vaccination humoral response being inhibited by immunosuppressive therapy in KTRs (Rincon-Arevalo et al., 2021; Danthu et al., 2021; Rozen-Zvi et al., 2021; Deepak et al., 2021; Strengert et al., 2021). It is interesting to note that being fully vaccinated with BNT162b2 instead of mRNA-1273 was associated with a reduced immune response and yielded lower antibody titres in DPs and KTRs across several studies (Affeldt et al., 2021; Ionita et al., 2022; Haller et al., 2022; Broseta et al., 2021; Stumpf et al., 2021a).

This study also assessed whether a third dose of an mRNA vaccine generates an immune response in DPs and KTRs and whether this is stronger than the immune response observed after two doses. For this analysis, both DPs and KTRs were combined with 76% of the overall population favouring seroconversion after three doses compared to an average of 63.18% of DPs and KTRs favouring seroconversion after two doses. This strongly suggests an increase in the number of patients that display an immune response after a third dose of an mRNA vaccine. Further to this, there have also been some reports where it is noted that the immune response after two doses of an mRNA vaccine has declined, when reassessed at a later time point (Boedecker-Lips et al., 2022; Agur et al., 2021; Dulovic et al., 2022). From this, and since there appears to be an increase in the number of patients displaying an immune response in both DPs and KTRs after three doses, and no significant adverse side effects were reported, we do recommend administering a third dose to both population types.

As well as assessing seroconversion in DPs and KTRs, this study also looked at the cellular response upon being double vaccinated with an mRNA vaccine. Albeit a limited number of studies available, we found that 61.86% of 978 DPs and KTRs included in this assessment displayed a cellular response after two doses of an mRNA vaccine. This compares to ~97% - 100% of healthy controls displaying a positive cellular response in some studies (Espi et al., 2021; Strengert et al., 2021; Sattler et al., 2021; Bertrand et al., 2021b). There has also been reports of an overall weaker T-cell response in DPs and especially KTRs compared to healthy controls (Bertrand et al., 2021a; Espi et al., 2021; Strengert et al., 2021; Sattler et al., 2021). T-cell immunity is considered essential for long-lasting protection against infection, with reports of T-cell immunity being elicited after up to 17 years in patients who had recovered from Severe Acute Respiratory Syndrome (SARS) (Le Bert et al., 2020). Given that seroconversion or the antibody response can begin to wane overtime (Boedecker-Lips et al., 2022; Dulovic et al., 2022; Agur et al., 2021), eliciting a poor T-cell response can be associated with a worse prognosis for COVID-19 patients (Mann et al., 2020). With the production of broadly reactive T-cells, an individual may be able to develop better, long-term immunity, and the ability to better recognise potential variants in the future (Peng et al., 2020). Further work is now being undertaken to establish a mechanism to trigger broadly reactive T-helper cells and killer T-cells for an overall greater protective immunity to COVID-19 (Dolgin, 2022; Heitmann et al., 2022).

Separately, in the cohort that developed a glomerulonephritis response, albeit intriguing, it cannot be confirmed that the vaccination alone has triggered this response (Klomjit et al., 2021). Despite this, patients 1, 2, 3, 6, 8, and 9 had previously diagnosed IgAN with patients 4 and 5 having underlying medical health conditions, including gestational diabetes and hyperlipidaemia respectively. Upon investigation, both latter patients revealed previously undiagnosed IgAN and crescentic glomerulonephritis alongside patient 7, who also had a clear medical history revealing crescentic glomerulonephritis after examination. Further to this, patient 10 is the only case study with a relapse in lupus nephritis class V and II being reported, however, this further brings about the question as to whether the mRNA COVID-19 vaccines trigger a relapse in immune-mediated disease. Since it cannot be confirmed whether these relapses in disease are completely co-incidental due to the limited evidence highlighting this possible relationship, we recommend caution when administering COVID-19 mRNA vaccines in cases where glomerulonephritis may be present, with further investigation also being required for conclusive data.

It is important to note that there were certain limitations to this study. Firstly, the type of immunoassay used to evaluate seroconversion and cellular response was not standardised and thus, there may be some variation between studies and thresholds that were used to determine a positive test. It should also be considered that we were only able to assess whether there was an immune response rather than whether the immune response was sustained at different time points. In addition to this, across all the studies that met the inclusion criteria of this analysis, the type of reactive antibody measured to assess seroconversion was not standardised due to the variation between studies. Thus, upon evaluating the rate of seroconversion and antibody response after vaccination administration, we deemed it appropriate to group together the different antibody responses including IgG, IgA and IgM antibodies. One study also evaluated the number of detectable SARS-CoV-2-specific and receptor-binding domain (RBD)-specific antibodies (Tai et al., 2020). For similar reasons, the cellular response was also evaluated in a similar manner with the grouping of responses from different T-cell types, including CD4+ and CD8+ T cells. Further to this, although we had tried to limit our analysis to infection-naïve participants only, this was not always possible since some studies did not specify or clarify this information. There was also a great degree of variability between studies on the timing between doses and the timing between the last dose given and the assessment of the patients’ immune response to the vaccination. As a result, all studies were included, regardless of when the doses were given, and assessment was performed.

From the analysis performed in this study, there appears to be some publication bias and significant heterogeneity amongst studies. It is important to note that systematic heterogeneity is inevitable in this type of analysis due to the nature of the studies being investigated. Both publication bias and heterogeneity, as well as the limitations reported above must be taken into consideration when interpreting the results reported in this study. Overall, we have still been able to highlight the efficacy of the BNT162b2 and mRNA-1273 vaccines in DPs and KTRs. In conclusion, our analysis has highlighted that the mRNA vaccines yield an immune response in fewer CKD patients than when compared to healthy controls, albeit a better immune response in DPs than when compared to KTRs. Further to this, a third dose appears to be well-tolerated in both DPs and KTRs, and thus we recommend a third dose being administered to this population type to boost and ensure longevity in the patient’s immune response.

Data availability

Underlying data

All data underlying the results are available as part of the article and no additional source data are required.

Reporting guidelines

Open Science Framework: PRISMA checklist for ‘A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals’. https://doi.org/10.17605/OSF.IO/63PJX (Goggolidou, 2022).

Data are available under the terms of the Creative Commons Zero “No rights reserved” data waiver (CC0 1.0 Public domain dedication).

References

  •  Affeldt P, Koehler FC, Brensing KA, et al.: Immune Responses to SARS-CoV-2 Infection and Vaccination in Dialysis Patients and Kidney Transplant Recipients. Microorganisms. 2021; 10(1). PubMed Abstract | Publisher Full Text
  •  Agur T, Ben-Dor N, Goldman S, et al.: Antibody response to mRNA SARS-CoV-2 vaccine among dialysis patients—a prospective cohort study. Nephrol. Dial. Transplant. 2021; 36(7): 1347–1349. PubMed Abstract | Publisher Full Text
  •  Agur T, Ben-Dor N, Herman-Edelstein M, et al.: Longevity of Humoral Response Six Months Following BNT162b2 Vaccine in Dialysis Patients. Front. Med. 2022; 9: 781888. PubMed Abstract | Publisher Full Text
  •  Fucci A, Giacobbe S, Guerriero I, et al.: The DiaCoVAb study in South Italy: immune response to Sars-CoV-2 vaccination in dialysis patients. Kidney Blood Press. Res. 2022; 47: 467–474. PubMed Abstract | Publisher Full Text
  •  Angel-Korman A, Peres E, Bryk G, et al.: Diminished and waning immunity to COVID-19 vaccination among hemodialysis patients in Israel: the case for a third vaccine dose. Clin. Kidney J. 2022; 15(2): 226–234. PubMed Abstract | Publisher Full Text
  •  Attias P, Sakhi H, Rieu P, et al.: Antibody response to the BNT162b2 vaccine in maintenance hemodialysis patients. Kidney Int. 2021; 99(6): 1490–1492. PubMed Abstract | Publisher Full Text
  •  Baden LR, El Sahly HM, Essink B, et al.: Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N. Engl. J. Med. 2021; 384(5): 403–416. PubMed Abstract | Publisher Full Text
  •  Belouzard S, Chu VC, Whittaker GR: Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 5871–5876. PubMed Abstract | Publisher Full Text
  •  Ben-Dov IZ, Oster Y, Tzukert K, et al.: Impact of tozinameran (BNT162b2) mRNA vaccine on kidney transplant and chronic dialysis patients: 3-5 months follow-up. J. Nephrol. 2022a; 35(1): 153–164. PubMed Abstract | Publisher Full Text
  •  Ben-Dov IZ, Tzukert K, Aharon M, et al.: Response to tozinameran (BNT162b2) booster in twice-vaccinated kidney transplant and maintenance dialysis patients. J. Nephrol. 2022b; 35(3): 761–763. PubMed Abstract | Publisher Full Text
  •  Benning L, Klein K, Morath C, et al.: Neutralizing Antibody Activity Against the B.1.617.2 (delta) Variant Before and After a Third BNT162b2 Vaccine Dose in Hemodialysis Patients. Front. Immunol. 2022; 13: 840136. PubMed Abstract | Publisher Full Text
  •  Benotmane I, Gautier G, Perrin P, et al.: Antibody Response After a Third Dose of the mRNA-1273 SARS-CoV-2 Vaccine in Kidney Transplant Recipients With Minimal Serologic Response to 2 Doses. JAMA. 2021a; 326(11): 1063–1065. PubMed Abstract | Publisher Full Text
  •  Benotmane I, Gautier-Vargas G, Cognard N, et al.: Low immunization rates among kidney transplant recipients who received 2 doses of the mRNA-1273 SARS-CoV-2 vaccine. Kidney Int. 2021b; 99(6): 1498–1500. PubMed Abstract | Publisher Full Text
  •  Bensouna I, Caudwell V, Kubab S, et al.: SARS-CoV-2 Antibody Response After a Third Dose of the BNT162b2 Vaccine in Patients Receiving Maintenance Hemodialysis or Peritoneal Dialysis. Am. J. Kidney Dis. 2021; 79: 185–192.e1. PubMed Abstract | Publisher Full Text
  •  Bertrand D, Hamzaoui M, Lemée V, et al.: Antibody and T Cell Response to SARS-CoV-2 Messenger RNA BNT162b2 Vaccine in Kidney Transplant Recipients and Hemodialysis Patients. J Am Soc Nephrol. 2021a; 32: 2147–2152. PubMed Abstract | Publisher Full Text
  •  Bertrand D, Hanoy M, Edet S, et al.: Antibody response to SARS-CoV-2 mRNA BNT162b2 vaccine in kidney transplant recipients and in-centre and satellite centre haemodialysis patients. Clin. Kidney J. 2021b; 14(9): 2127–2128. PubMed Abstract | Publisher Full Text
  •  Boedecker-Lips SC, Lautem A, Runkel S, et al.: 'Six-Month Follow-Up after Vaccination with BNT162b2: SARS-CoV-2 Antigen-Specific Cellular and Humoral Immune Responses in Hemodialysis Patients and Kidney Transplant Recipients. Pathogens (Basel, Switzerland). 2022; 11(1). PubMed Abstract | Publisher Full Text
  •  Broseta JJ, Rodríguez-Espinosa D, Cuadrado E, et al.: Humoral Response after Three Doses of mRNA-1273 or BNT162b2 SARS-CoV-2 Vaccines in Hemodialysis Patients. Vaccines (Basel). 2022; 10(4): 522. PubMed Abstract | Publisher Full Text
  •  Broseta JJ, Rodríguez-Espinosa D, Rodríguez N, et al.: Humoral and Cellular Responses to mRNA-1273 and BNT162b2 SARS-CoV-2 Vaccines Administered to Hemodialysis Patients. Am. J. Kidney Dis. 2021; 78(4): 571–581. PubMed Abstract | Publisher Full Text
  •  Butt AA, Talisa VB, Yan P, et al.: Real-world Effectiveness of the SARS-CoV-2 mRNA Vaccines in Preventing Confirmed Infection in Patients on Chronic Hemodialysis. Clin. Infect. Dis. 2022. PubMed Abstract | Publisher Full Text
  •  Cai R, Zhang J, Zhu Y, et al.: Mortality in chronic kidney disease patients with COVID-19: a systematic review and meta-analysis. Int. Urol. Nephrol. 2021; 53(8): 1623–1629. PubMed Abstract | Publisher Full Text
  •  Chan JF, Kok K, Zhu Z, et al.: Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg. Microbes Infect. 2020; 9(1): 221–236. PubMed Abstract | Publisher Full Text
  •  Chang C, Sue S, Yu T, et al.: Modular organization of SARS coronavirus nucleocapsid protein. J. Biomed. Sci. 2005; 13(1): 59–72. PubMed Abstract | Publisher Full Text
  •  Chang D, Lin M, Wei L, et al.: Epidemiologic and Clinical Characteristics of Novel Coronavirus Infections Involving 13 Patients Outside Wuhan, China. JAMA. 2020; 323(11): 1092–1093. PubMed Abstract | Publisher Full Text
  •  Chen Y, Liu Q, Guo D: Emerging coronaviruses: Genome structure, replication, and pathogenesis. J. Med. Virol. 2020; 92(10): 2249. PubMed Abstract | Publisher Full Text
  •  Chen Z, Hu J, Liu L, et al.: SARS-CoV-2 Causes Acute Kidney Injury by Directly Infecting Renal Tubules. Front. Cell Dev. Biol. 2021; 9PubMed Abstract | Publisher Full Text
  •  Chukwu CA, Mahmood K, Elmakki S, et al.: Evaluating the antibody response to SARS-COV-2 vaccination amongst kidney transplant recipients at a single nephrology centre. PLoS One. 2022; 17(3): e0265130. PubMed Abstract | Publisher Full Text
  •  Clarke C, Martin P, Gleeson S, et al.: Comparison of immunogenicity between BNT162b2 and ChAdOx1 SARS-CoV-2 vaccines in a large haemodialysis population. Medrxiv. 2021. Publisher Full Text
  •  Cucinotta D, Vanelli M: WHO Declares COVID-19 a Pandemic. Acta bio-medica: Atenei Parmensis. 2020; 91(1): 157–160. PubMed Abstract | Publisher Full Text
  •  Danthu C, Hantz S, Dahlem A, et al.: Humoral Response after SARS-CoV-2 mRNA Vaccination in a Cohort of Hemodialysis Patients and Kidney Transplant Recipients. J Am Soc Nephrol. 2021; 32(9): 2153–2158. PubMed Abstract | Publisher Full Text
  •  Deepak P, Kim W, Paley MA, et al.: Effect of Immunosuppression on the Immunogenicity of mRNA Vaccines to SARS-CoV-2: A Prospective Cohort Study. Ann. Intern. Med. 2021; 174(11): 1572–1585. PubMed Abstract | Publisher Full Text
  •  Dekervel M, Henry N, Torreggiani M, et al.: Humoral response to a third injection of BNT162b2 vaccine in patients on maintenance haemodialysis. Clin. Kidney J. 2021; 14(11): 2349–2355. PubMed Abstract | Publisher Full Text
  •  Dolgin E: T-cell vaccines could top up immunity to COVID, as variants loom large. Nat. Biotechnol. 2022; 40(1): 3–4. PubMed Abstract | Publisher Full Text
  •  Ducloux D, Colladant M, Chabannes M, et al.: Factors associated with humoral response after BNT162b2 mRNA COVID-19 vaccination in kidney transplant patients. Clin. Kidney J. 2021a; 14(10): 2270–2272. PubMed Abstract | Publisher Full Text
  •  Ducloux D, Colladant M, Chabannes M, et al.: Humoral response after BNT162b2 mRNA COVID-19 vaccination in patients on haemodialysis depends on immune status. Clin. Kidney J. 2021b; 14: 2266–2267. PubMed Abstract | Publisher Full Text
  •  Dulovic A, Strengert M, Ramos GM, et al.: Diminishing Immune Responses against Variants of Concern in Dialysis Patients 4 Months after SARS-CoV-2 mRNA Vaccination. Emerg. Infect. Dis. 2022; 28(4): 743–750. PubMed Abstract | Publisher Full Text
  •  Duni A, Markopoulos GS, Mallioras I, et al.: The Humoral Immune Response to BNT162b2 Vaccine Is Associated With Circulating CD19+ B Lymphocytes and the Naïve CD45RA to Memory CD45RO CD4+ T Helper Cells Ratio in Hemodialysis Patients and Kidney Transplant Recipients. Front. Immunol. 2021; 12: 760249. PubMed Abstract | Publisher Full Text
  •  Espi M, Charmetant X, Barba T, et al.: The ROMANOV study found impaired humoral and cellular immune responses to SARS-CoV-2 mRNA vaccine in virus-unexposed patients receiving maintenance hemodialysis. Kidney Int. 2021; 100(4): 928–936. PubMed Abstract | Publisher Full Text
  •  Espi M, Charmetant X, Barba T, et al.: A prospective observational study for justification, safety, and efficacy of a third dose of mRNA vaccine in patients receiving maintenance hemodialysis. Kidney Int. 2022; 101(2): 390–402. PubMed Abstract | Publisher Full Text
  •  Folegatti PM, Ewer KJ, Aley PK, et al.: Safety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trial. Lancet (London, England). 2020; 396(10249): 467–478. PubMed Abstract | Publisher Full Text
  •  Frantzen L, Cavaillé G, Thibeaut S, et al.: Efficacy of the BNT162b2 mRNA COVID-19 vaccine in a haemodialysis cohort. Nephrol. Dial. Transplant. 2021; 36(9): 1756–1757. PubMed Abstract | Publisher Full Text
  •  Gansevoort RT, Hilbrands LB: CKD is a key risk factor for COVID-19 mortality. Nat. Rev. Nephrol. 2020; 16(12): 705–706. PubMed Abstract | Publisher Full Text
  •  Georgery H, Devresse A, Yombi J, et al.: High response rate to BNT162b2 mRNA COVID-19 vaccine among self-care dialysis patients. Clin. Kidney J. 2021; 14: 2129–2131. PubMed Abstract | Publisher Full Text
  •  Giot M, Fourié T, Lano G, et al.: Spike and neutralizing antibodies response to COVID-19 vaccination in haemodialysis patients. Clin. Kidney J. 2021; 14(10): 2239–2245. PubMed Abstract | Publisher Full Text
  •  Goggolidou P: COVID-19 mRNA vaccine effectiveness in Chronic Kidney Disease. Dataset. 2022, July 1. Publisher Full Text
  •  Grant MC, Geoghegan L, Arbyn M, et al.: The prevalence of symptoms in 24,410 adults infected by the novel coronavirus (SARS-CoV-2; COVID-19): A systematic review and meta-analysis of 148 studies from 9 countries. PLoS One. 2020; 15(6). Publisher Full Text
  •  Grupper A, Katchman E, Ben-Yehoyada M, et al.: Kidney transplant recipients vaccinated before transplantation maintain superior humoral response to SARS-CoV-2 vaccine. Clin. Transpl. 2021; 35(12): e14478-n/a. PubMed Abstract | Publisher Full Text
  •  Grupper A, Rabinowich L, Ben-Yehoyada M, et al.: Humoral Response to the Third Dose of Sars-Cov-2 Vaccine in Kidney Transplant Recipients. Transplant. Proc. 2022. PubMed Abstract | Publisher Full Text
  •  Haller MC, Kaiser RA, Langthaler S, et al.: Comparison of mRNA-1273 and BNT162b2 SARS-CoV-2 mRNA Vaccine Immunogenicity in Kidney Transplant Recipients. Transpl. Int. 2022; 35PubMed Abstract | Publisher Full Text
  •  Hamaya T, Hatakeyama S, Yoneyama T, et al.: Seroprevalence of SARS-CoV-2 spike IgG antibodies after the second BNT162b2 mRNA vaccine in Japanese kidney transplant recipients. Sci. Rep. 2022; 12(1): 5876. PubMed Abstract | Publisher Full Text
  •  Hamming I, Timens W, Bulthuis MLC, et al.: Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 2004; 203(2): 631–637. PubMed Abstract | Publisher Full Text
  •  Heitmann JS, Bilich T, Tandler C, et al.: A COVID-19 peptide vaccine for the induction of SARS-CoV-2 T cell immunity. Nature. 2022; 601(7894): 617–622. PubMed Abstract | Publisher Full Text
  •  Hod T, Ben-David A, Olmer L, et al.: BNT162b2 Third Booster Dose Significantly Increases the Humoral Response Assessed by Both RBD IgG and Neutralizing Antibodies in Renal Transplant Recipients. Transpl. Int. 2022; 35: 10239. PubMed Abstract | Publisher Full Text
  •  Hoffmann M, Kleine-Weber H, Schroeder S, et al.: SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell. 2020; 181(2): 271–280.e8. PubMed Abstract | Publisher Full Text
  •  Hsu CM, Weiner DE, Aweh GN, et al.: Seroresponse to SARS-CoV-2 Vaccines Among Maintenance Dialysis Patients. Am. J. Kidney Dis. 2022; 79(2): 307–310. PubMed Abstract | Publisher Full Text
  •  Hu J, Wang Y: The Clinical Characteristics and Risk Factors of Severe COVID-19. Gerontology. 2021; 67(3): 255–266. PubMed Abstract | Publisher Full Text
  •  Huang C, Wang Y, Li X, et al.: Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet (British edition). 2020; 395(10223): 497–506. PubMed Abstract | Publisher Full Text
  •  Ionita C, Marcelli D, Nita C, et al.: Comparison of antibody response to two different mRNA Covid-19 vaccines in patients on hemodialysis. J. Nephrol. 2022; 35(1): 143–151. PubMed Abstract | Publisher Full Text
  •  Jackson LA, Anderson EJ, Rouphael NG, et al.: An mRNA Vaccine against SARS-CoV-2 — Preliminary Report. N. Engl. J. Med. 2020; 383(20): 1920–1931. PubMed Abstract | Publisher Full Text
  •  Jager KJ, Kramer A, Chesnaye NC, et al.: Results from the ERA-EDTA Registry indicate a high mortality due to COVID-19 in dialysis patients and kidney transplant recipients across Europe. Kidney Int. 2020; 98(6): 1540–1548. Publisher Full Text
  •  Jahn M, Korth J, Dorsch O, et al.: Humoral Response to SARS-CoV-2-Vaccination with BNT162b2 (Pfizer-BioNTech) in Patients on Hemodialysis. Vaccines. 2021; 9(4). PubMed Abstract | Publisher Full Text
  •  Jin Y, Yang H, Ji W, et al.: Virology, Epidemiology, Pathogenesis, and Control of COVID-19. Viruses. 2020; 12(4). PubMed Abstract | Publisher Full Text
  •  Kaiser RA, Haller MC, Apfalter P, et al.: Comparison of BNT162b2 (Pfizer-BioNtech) and mRNA-1273 (Moderna) SARS-CoV-2 mRNA vaccine immunogenicity in dialysis patients. Kidney Int. 2021; 100(3): 697–698. PubMed Abstract | Publisher Full Text
  •  Kitamura M, Takazono T, Yamaguchi K, et al.: Favorable Humoral Response to Third Dose of BNT162b2 in Patients Undergoing Hemodialysis. J. Clin. Med. 2022; 11(8): 2090. PubMed Abstract | Publisher Full Text
  •  Klomjit N, Alexander M, Fervenza F, et al.: COVID-19 Vaccination and Glomerulonephritis. Kidney International Reports. 2021; 6(12): 2969–2978. PubMed Abstract | Publisher Full Text
  •  Kolb T, Fischer S, Müller L, et al.: Impaired Immune Response to SARS-CoV-2 Vaccination in Dialysis Patients and in Kidney Transplant Recipients. Kidney360. 2021; 2(9): 1491–1498. PubMed Abstract | Publisher Full Text
  •  Korth J, Jahn M, Dorsch O, et al.: Impaired Humoral Response in Renal Transplant Recipients to SARS-CoV-2 Vaccination with BNT162b2 (Pfizer-BioNTech). Viruses. 2021; 13(5). PubMed Abstract | Publisher Full Text
  •  Kumar A, Singh R, Kaur J, et al.: Wuhan to World: The COVID-19 Pandemic. Front. Cell. Infect. Microbiol. 2021; 11: 596201. PubMed Abstract | Publisher Full Text
  •  Kwiatkowska E, Safranow K, Wojciechowska-Koszko I, et al.: SARS-CoV-2 mRNA Vaccine-Induced Cellular and Humoral Immunity in Hemodialysis Patients. Biomedicines. 2022; 10(3): 636. PubMed Abstract | Publisher Full Text
  •  Labriola L, Scohy A, Regemorter EV, et al.: Immunogenicity of BNT162b2 SARS-CoV-2 Vaccine in a Multicenter Cohort of Nursing Home Residents Receiving Maintenance Hemodialysis. Am. J. Kidney Dis. 2021; 78: 766–768. PubMed Abstract | Publisher Full Text
  •  Lacson E, Argyropoulos C, Manley H, et al.: 'Immunogenicity of SARS-CoV-2 Vaccine in Dialysis', Journal of the American Society of Nephrology. JASN. 2021; 32: 2735–2742. PubMed Abstract | Publisher Full Text
  •  le Bert N, Tan AT, Kunasegaran K, et al.: SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature. 2020; 584(7821): 457–462. Publisher Full Text
  •  Lely AT, Hamming I, Goor H, et al.: Renal ACE2 expression in human kidney disease. J. Pathol. 2004; 204(5): 587–593. Publisher Full Text
  •  Li H, Liu S, Yu X, et al.: Coronavirus disease 2019 (COVID-19): current status and future perspectives. Int. J. Antimicrob. Agents. 2020; 55(5): 105951. Publisher Full Text
  •  Li W, Moore MJ, Vasilieva N, et al.: Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003; 426(6965): 450–454. Publisher Full Text
  •  Longlune N, Nogier MB, Miedougé M, et al.: High immunogenicity of a messenger RNA-based vaccine against SARS-CoV-2 in chronic dialysis patients. Nephrology, Dialysis, Transplantation: Official Publication of the European Dialysis and Transplant Association - European Renal Association. 2021; 36(9): 1704–1709. PubMed Abstract | Publisher Full Text
  •  Lu R, Zhao X, Li J, et al.: Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet (London, England). 2020; 395(10224): 565–574. Publisher Full Text
  •  Malha L, Mueller FB, Pecker MS, et al.: COVID-19 and the Renin-Angiotensin System. Kidney international reports. 2020; 5(5): 563–565. PubMed Abstract | Publisher Full Text
  •  Mann ER, Menon M, Knight SB, et al.: Longitudinal immune profiling reveals key myeloid signatures associated with COVID-19. Science Immunology. 2020; 5(51). PubMed Abstract | Publisher Full Text
  •  Massa F, Cremoni M, Gérard A, et al.: Safety and cross-variant immunogenicity of a three-dose COVID-19 mRNA vaccine regimen in kidney transplant recipients. EBioMedicine. 2021; 73: 103679. PubMed Abstract | Publisher Full Text
  •  Masset C, Kerleau C, Garandeau C, et al.: A third injection of the BNT162b2 mRNA COVID-19 vaccine in kidney transplant recipients improves the humoral immune response. Kidney Int. 2021; 100(5): 1132–1135. PubMed Abstract | Publisher Full Text
  •  Matsunami M, Suzuki T, Fukuda J, et al.: Comparison of antibody response following the second dose of SARS-CoV-2 mRNA vaccine in elderly patients with late-stage chronic kidney disease. Ren. Replace. Ther. 2022; 8(1): 13. PubMed Abstract | Publisher Full Text
  •  Matsunami M, Suzuki T, Terao T, et al.: Immune response to SARS-CoV-2 vaccination among renal replacement therapy patients with CKD: a single-center study. Clin. Exp. Nephrol. 2021; 26(3): 305–307. PubMed Abstract | Publisher Full Text
  •  Melin J, Svensson MK, Albinsson B, et al.: Humoral and cellular response to SARS-CoV-2 BNT162b2 mRNA vaccine in hemodialysis patients. BMC Immunol. 2021; 22(1): 70. PubMed Abstract | Publisher Full Text
  •  Meshram HS, Kute VB, Shah N, et al.: COVID-19 in Kidney Transplant Recipients Vaccinated With Oxford-AstraZeneca COVID-19 Vaccine (Covishield): A Single-center Experience From India. Transplantation. 2021; 105(9): e100–e103. PubMed Abstract | Publisher Full Text
  •  Nacasch N, Erez D, Lishner M, et al.: Long-term Antibody Response to the BNT162b2 Vaccine Among Maintenance Hemodialysis Patients. Am. J. Kidney Dis. 2022; 79(1): 137–139. PubMed Abstract | Publisher Full Text
  •  Negrea L, Rovin BH: Gross hematuria following vaccination for severe acute respiratory syndrome coronavirus 2 in 2 patients with IgA nephropathy. Kidney Int. 2021; 99(6): 1487. PubMed Abstract | Publisher Full Text
  •  Neuman BW, Kiss G, Kunding AH, et al.: A structural analysis of M protein in coronavirus assembly and morphology. J. Struct. Biol. 2011; 174(1): 11–22. Publisher Full Text
  •  Ou X, Liu Y, Lei X, et al.: Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV. Nat. Commun. 2020; 11: 1620. PubMed Abstract | Publisher Full Text
  •  Page MJ, McKenzie JE, Bossuyt PM, et al.: The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (Clinical research ed.). 2021; 372: n71. PubMed Abstract | Publisher Full Text
  •  Patecki M, Merscher S, Dumann H, et al.: Similar humoral immune responses in peritoneal dialysis and haemodialysis patients after two doses of the SARS-CoV-2 vaccine BNT162b2. Perit. Dial. Int. 2022; 42(1): 100–101. PubMed Abstract | Publisher Full Text
  •  Peng Y, Mentzer AJ, Liu G, et al.: Broad and strong memory CD4.sup.+ and CD8.sup.+ T cells induced by SARS-CoV-2 in UK convalescent individuals following COVID-19. Nat. Immunol. 2020; 21(11): 1336–1345. PubMed Abstract | Publisher Full Text
  •  Perrin P, Bassand X, Benotmane I, et al.: Gross hematuria following SARS-CoV-2 vaccination in patients with IgA nephropathy. Kidney Int. 2021; 100(2): 466–468. PubMed Abstract | Publisher Full Text
  •  Polack FP, Thomas SJ, Kitchin N, et al.: Safety and Efficacy of the BNT162b2 mRNA Covid-19 Vaccine. N. Engl. J. Med. 2020; 383(27): 2603–2615. PubMed Abstract | Publisher Full Text
  •  Rabi FA, Al Zoubi MS, Kasasbeh GA, et al.: SARS-CoV-2 and Coronavirus Disease 2019: What We Know So Far. Pathogens. 2020; 9(3). PubMed Abstract | Publisher Full Text
  •  Rahim SEG, Lin JT, Wang JC: A case of gross hematuria and IgA nephropathy flare-up following SARS-CoV-2 vaccination. Kidney Int. 2021; 100(1): 238. Publisher Full Text
  •  Raj R: Analysis of non-structural proteins, NSPs of SARS-CoV-2 as targets for computational drug designing. Biochemistry and Biophysics Reports. 2021; 25: 100847. PubMed Abstract | Publisher Full Text
  •  Rincon-Arevalo H, Choi M, Stefanski A, et al.: Impaired humoral immunity to SARS-CoV-2 BNT162b2 vaccine in kidney transplant recipients and dialysis patients. Sci. Immunol. 2021; 6(60): eabj1031. PubMed Abstract | Publisher Full Text
  •  Rozen-Zvi B, Yahav D, Agur T, et al.: Antibody response to SARS-CoV-2 mRNA vaccine among kidney transplant recipients: a prospective cohort study. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases. 2021; 27(8): 1173.e1–1173.e4. PubMed Abstract | Publisher Full Text
  •  Russo G, Lai Q, Poli L, et al.: SARS-COV-2 vaccination with BNT162B2 in renal transplant patients: Risk factors for impaired response and immunological implications. Clin. Transpl. 2022; 36(1): e14495. PubMed Abstract | Publisher Full Text
  •  Sacker A, Kung V, Andeen N: Anti-GBM nephritis with mesangial IgA deposits after SARS-CoV-2 mRNA vaccination. Kidney Int. 2021; 100(2): 471–472. PubMed Abstract | Publisher Full Text
  •  Santos-Araújo C, Mota Veiga P, Santos MJ, et al.: Time-dependent evolution of IgG antibody levels after first and second dose of mRNA-based SARS-CoV-2 vaccination in haemodialysis patients: a multicentre study. Nephrol. Dial. Transplant. 2022; 37(2): 375–381. Publisher Full Text
  •  Sattler A, Schrezenmeier E, Weber UA, et al.: Impaired humoral and cellular immunity after SARS-CoV-2 BNT162b2 (tozinameran) prime-boost vaccination in kidney transplant recipients. J. Clin. Invest. 2021; 131(14). PubMed Abstract | Publisher Full Text
  •  Schrezenmeier E, Bergfeld L, Hillus D, et al.: Immunogenicity of COVID-19 Tozinameran Vaccination in Patients on Chronic Dialysis. Front. Immunol. 2021; 12: 690698. PubMed Abstract | Publisher Full Text
  •  Seija M, Rammauro F, Santiago J, et al.: Comparison of antibody response to SARS-CoV-2 after two doses of inactivated virus and BNT162b2 mRNA vaccines in kidney transplant. Clin. Kidney J. 2022; 15(3): 527–533. Publisher Full Text
  •  Selvaskandan H, Cheung CK, Muto M, et al.: New strategies and perspectives on managing IgA nephropathy. Clin. Exp. Nephrol. 2019; 23(5): 577–588. PubMed Abstract | Publisher Full Text
  •  Shashar M, Nacasch N, Grupper A, et al.: Humoral Response to Pfizer BNT162b2 Vaccine Booster in Maintenance Hemodialysis Patients. Am. J. Nephrol. 2022; 53(2-3): 207–214. PubMed Abstract | Publisher Full Text
  •  Shi H, Han X, Jiang N, et al.: Radiological findings from 81 patients with COVID-19 pneumonia in Wuhan, China: a descriptive study. Lancet Infect. Dis. 2020; 20(4): 425–434. PubMed Abstract | Publisher Full Text
  •  Simon B, Rubey H, Treipl A, et al.: Haemodialysis patients show a highly diminished antibody response after COVID-19 mRNA vaccination compared with healthy controls. Nephrology, Dialysis, Transplantation: Official Publication of the European Dialysis and Transplant Association - European Renal Association. 2021; 36(9): 1709–1716. PubMed Abstract | Publisher Full Text
  •  Soler MJ, Wysocki J, Ye M, et al.: ACE2 inhibition worsens glomerular injury in association with increased ACE expression in streptozotocin-induced diabetic mice. Kidney Int. 2007; 72(5): 614–623. PubMed Abstract | Publisher Full Text
  •  Speer C, Göth D, Benning L, et al.: Early Humoral Responses of Hemodialysis Patients after COVID-19 Vaccination with BNT162b2. Clinical Journal of the American Society of Nephrology: CJASN. 2021; 16(7): 1073–1082. PubMed Abstract | Publisher Full Text
  •  Strengert M, Becker M, Ramos GM, et al.: Cellular and humoral immunogenicity of a SARS-CoV-2 mRNA vaccine in patients on haemodialysis. EBioMedicine. 2021; 70: 103524. PubMed Abstract | Publisher Full Text
  •  Stumpf J, Siepmann T, Lindner T, et al.: Humoral and cellular immunity to SARS-CoV-2 vaccination in renal transplant versus dialysis patients: A prospective, multicenter observational study using mRNA-1273 or BNT162b2 mRNA vaccine. The Lancet Regional Health. Europe. 2021a; 9: 100178. PubMed Abstract | Publisher Full Text
  •  Stumpf J, Tonnus W, Paliege A, et al.: Cellular and Humoral Immune Responses After 3 Doses of BNT162b2 mRNA SARS-CoV-2 Vaccine in Kidney Transplant. Transplantation. 2021b; 105(11): e267–e269. Publisher Full Text
  •  Sungnak W, Huang N, Bécavin C, et al.: SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat. Med. 2020; 26(5): 681–687. PubMed Abstract | Publisher Full Text
  •  Tai W, He L, Zhang X, et al.: Characterization of the receptor-binding domain (RBD) of 2019 novel coronavirus: implication for development of RBD protein as a viral attachment inhibitor and vaccine. Cell. Mol. Immunol. 2020; 17(6): 613–620. Publisher Full Text
  •  Tan HZ, Tan RY, Choo JCJ, et al.: Is COVID-19 vaccination unmasking glomerulonephritis?. Kidney Int. 2021; 100(2): 469–471. PubMed Abstract | Publisher Full Text
  •  Tikellis C, Johnston CI, Forbes JM, et al.: Characterization of Renal Angiotensin-Converting Enzyme 2 in Diabetic Nephropathy. Hypertension. 2003; 41(3): 392–397. PubMed Abstract | Publisher Full Text
  •  Torreggiani M, Blanchi S, Fois A, et al.: Neutralizing SARS-CoV-2 antibody response in dialysis patients after the first dose of the BNT162b2 mRNA COVID-19 vaccine: the war is far from being won. Kidney Int. 2021; 99(6): 1494–1496. PubMed Abstract | Publisher Full Text
  •  Tsang HF, Chan LWC, Cho WCS, et al.: An update on COVID-19 pandemic: the epidemiology, pathogenesis, prevention and treatment strategies. Expert Rev. Anti-Infect. Ther. 2021; 19(7): 877–888. PubMed Abstract | Publisher Full Text
  •  Tuschen K, Bräsen JH, Schmitz J, et al.: Relapse of class V lupus nephritis after vaccination with COVID-19 mRNA vaccine. Kidney Int. 2021; 100(4): 941–944. PubMed Abstract | Publisher Full Text
  •  Vaiciuniene R, Sitkauskiene B, Bumblyte IA, et al.: Immune Response after SARS-CoV-2 Vaccination in Kidney Transplant Patients. Medicina (Kaunas). 2021; 57(12): 1327. PubMed Abstract | Publisher Full Text
  •  Villanego F, Cazorla JM, Vigara LA, et al.: Protecting kidney transplant recipients against SARS-CoV-2 infection: A third dose of vaccine is necessary now. Am. J. Transplant. 2022; 22(4): 1275–1276. PubMed Abstract | Publisher Full Text
  •  Voysey M, Clemens SAC, Madhi SA, et al.: Safety and efficacy of the ChAdOx1 nCoV-19 vaccine (AZD1222) against SARS-CoV-2: an interim analysis of four randomised controlled trials in Brazil, South Africa, and the UK. Lancet. 2021; 397(10269): 99–111. PubMed Abstract | Publisher Full Text
  •  Wang D, Hu B, Hu C, et al.: 'Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus–Infected Pneumonia in Wuhan, China. JAMA. 2020; 323(11): 1061–1069. PubMed Abstract | Publisher Full Text
  •  Weigert A, Bergman M, Gonçalves L, et al.: Longitudinal analysis of antibody responses to the Pfizer BNT162b2 vaccine in Patients Undergoing Maintenance Hemodialysis. Medrxiv. 2021. Publisher Full Text
  •  WHO Coronavirus (COVID-19) Dashboard.Accessed: Nov 4, 2021.Reference Source
  •  Williamson EJ, Walker AJ, Bhaskaran K, et al.: Factors associated with COVID-19-related death using OpenSAFELY. Nature. 2020; 584(7821): 430–436. PubMed Abstract | Publisher Full Text
  •  Windpessl M, Bruchfeld A, Anders H, et al.: COVID-19 vaccines and kidney disease. Nat. Rev. Nephrol. 2021; 17(5): 291–293. Publisher Full Text
  •  Wisnewski A, Campillo Luna J, Redlich C: Human IgG and IgA responses to COVID-19 mRNA vaccines. PLoS One. 2021; 16(6): e0249499. PubMed Abstract | Publisher Full Text
  •  Wrapp D, Wang N, Corbett KS, et al.: Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science (New York, N.Y.). 2020; 367(6483): 1260–1263. PubMed Abstract | Publisher Full Text
  •  Yadav R, Chaudhary JK, Jain N, et al.: Role of Structural and Non-Structural Proteins and Therapeutic Targets of SARS-CoV-2 for COVID-19. Cells. 2021; 10(4). PubMed Abstract | Publisher Full Text
  •  Yahav D, Rahamimov R, Mashraki T, et al.: Immune Response to Third Dose BNT162b2 COVID-19 Vaccine Among Kidney Transplant Recipients-A Prospective Study. Transpl. Int. 2022; 35: 10204. PubMed Abstract | Publisher Full Text
  •  Yanay NB, Freiman S, Shapira M, et al.: Experience with SARS-CoV-2 BNT162b2 mRNA vaccine in dialysis patients. Kidney Int. 2021; 99(6): 1496–1498. Publisher Full Text
  •  Yau K, Abe KT, Naimark D, et al.: Evaluation of the SARS-CoV-2 Antibody Response to the BNT162b2 Vaccine in Patients Undergoing Hemodialysis. JAMA Netw. Open. 2021; 4(9): e2123622. PubMed Abstract | Publisher Full Text
  •  Yau K, Chan CT, Abe KT, et al.: Differences in mRNA-1273 (Moderna) and BNT162b2 (Pfizer-BioNTech) SARS-CoV-2 vaccine immunogenicity among patients undergoing dialysis. Canadian Medical Association Journal (CMAJ). 2022; 194(8): E297–E305. PubMed Abstract | Publisher Full Text
  •  Yi SG, Moore LW, Eagar T, et al.: Risk Factors Associated With an Impaired Antibody Response in Kidney Transplant Recipients Following 2 Doses of the SARS-CoV-2 mRNA Vaccine. Transplant. Direct. 2022; 8(1): e1257. PubMed Abstract | Publisher Full Text
  •  Yuki K, Fujiogi M, Koutsogiannaki S: COVID-19 pathophysiology: A review. Clinical Immunology (Orlando, Fla.). 2020; 215: 108427. PubMed Abstract | Publisher Full Text
  •  Zhou P, Yang X, Wang X, et al.: A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020; 579(7798): 270–273. PubMed Abstract | Publisher Full Text
  •  Zitt E, Davidovic T, Schimpf J, et al.: The Safety and Immunogenicity of the mRNA-BNT162b2 SARS-CoV-2 Vaccine in Hemodialysis Patients. Front. Immunol. 2021; 12: 704773. PubMed Abstract | Publisher Full Text
  •  Zou X, Chen K, Zou J, et al.: Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection. Front. Med. 2020; 14(2): 185–192. PubMed Abstract | Publisher Full Text

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Malik SA, Modarage K and Goggolidou P. A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals [version 2; peer review: 2 approved]. F1000Research 2022, 11:909 (https://doi.org/10.12688/f1000research.122820.2)
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Reviewer Report 08 Dec 2022
Marios Papasotiriou, Department of Nephrology and Kidney Transplantation, University Hospital of Patras, Patras, Greece 
Approved
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https://doi.org/10.5256/f1000research.141313.r156324
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Papasotiriou M. Reviewer Report For: A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals [version 2; peer review: 2 approved]. F1000Research 2022, 11:909 (https://doi.org/10.5256/f1000research.141313.r156324)
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Katherine Karakoula, School of Pharmacy, University of Wolverhampton, Wolverhampton, UK 
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https://doi.org/10.5256/f1000research.141313.r156323
I thank the authors for their time to address my comments appropriately.
I also understand their response on the limited number of studies available to enable them to perform statistical analysis for the detection of positive seroconversion for DPs ... Continue reading
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Karakoula K. Reviewer Report For: A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals [version 2; peer review: 2 approved]. F1000Research 2022, 11:909 (https://doi.org/10.5256/f1000research.141313.r156323)
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Katherine Karakoula, School of Pharmacy, University of Wolverhampton, Wolverhampton, UK 
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https://doi.org/10.5256/f1000research.134859.r151580
The authors present a thorough systematic review on the effectiveness of mRNA vaccines for COVID-19 infection in DPs and KTRs patients.

Overall, the review is well-presented with a detailed description of methods used for the analysis and ... Continue reading
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Karakoula K. Reviewer Report For: A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals [version 2; peer review: 2 approved]. F1000Research 2022, 11:909 (https://doi.org/10.5256/f1000research.134859.r151580)
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  • Author Response 25 Nov 2022
    Paraskevi Goggolidou, Research Institute in Healthcare Science, Faculty of Science and Engineering, University of Wolverhampton, Wulfruna Street, Wolverhampton, WV1 1LY, UK
    25 Nov 2022
    Author Response
    We thank the reviewer for their comments. We have taken their points on board and edits to the initial manuscript can be seen as tracked changes. Please note that unfortunately, ... Continue reading
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  • Author Response 25 Nov 2022
    Paraskevi Goggolidou, Research Institute in Healthcare Science, Faculty of Science and Engineering, University of Wolverhampton, Wulfruna Street, Wolverhampton, WV1 1LY, UK
    25 Nov 2022
    Author Response
    We thank the reviewer for their comments. We have taken their points on board and edits to the initial manuscript can be seen as tracked changes. Please note that unfortunately, ... Continue reading
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Reviewer Report 08 Sep 2022
Marios Papasotiriou, Department of Nephrology and Kidney Transplantation, University Hospital of Patras, Patras, Greece 
Approved with Reservations
VIEWS 20
https://doi.org/10.5256/f1000research.134859.r149323
In this systematic review the authors assessed the response rate and overall effectiveness of vaccination against Covid-19 with mRNA vaccines in patients on dialysis or patients after kidney transplantation.

The work overall is clearly presented and the ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Papasotiriou M. Reviewer Report For: A systematic review assessing the effectiveness of COVID-19 mRNA vaccines in chronic kidney disease (CKD) individuals [version 2; peer review: 2 approved]. F1000Research 2022, 11:909 (https://doi.org/10.5256/f1000research.134859.r149323)
The direct URL for this report is:
https://f1000research.com/articles/11-909/v1#referee-response-149323
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Report a concern
  • Author Response 25 Nov 2022
    Paraskevi Goggolidou, Research Institute in Healthcare Science, Faculty of Science and Engineering, University of Wolverhampton, Wulfruna Street, Wolverhampton, WV1 1LY, UK
    25 Nov 2022
    Author Response
    We thank the reviewer for their comments. In response to them, we have submitted a revised version of the article, with any amendments shown as tracked changes. Please note:

    ... Continue reading
    Report a concern
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COMMENTS ON THIS REPORT
  • Author Response 25 Nov 2022
    Paraskevi Goggolidou, Research Institute in Healthcare Science, Faculty of Science and Engineering, University of Wolverhampton, Wulfruna Street, Wolverhampton, WV1 1LY, UK
    25 Nov 2022
    Author Response
    We thank the reviewer for their comments. In response to them, we have submitted a revised version of the article, with any amendments shown as tracked changes. Please note:

    ... Continue reading
    Report a concern

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Approved
The paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations
A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved
Fundamental flaws in the paper seriously undermine the findings and conclusions

Reviewer Reports

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Version 2
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  1. Marios Papasotiriou, University Hospital of Patras, Patras, Greece
  2. Katherine Karakoula, University of Wolverhampton, Wolverhampton, UK

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    Alongside their report, reviewers assign a status to the article:
    Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
    Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
    Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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