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. 2022 Oct 3;5(6):e874. doi: 10.1002/hsr2.874

Immunogenicity of COVID‐19 mRNA vaccines in hemodialysis patients: Systematic review and meta‐analysis

Shahab Falahi 1, Hojjat Sayyadi 2, Azra Kenarkoohi 1,3,✉
PMCID: PMC9528953  PMID: 36210877

Abstract

Background and Aims

Vaccine response is a concern in hemodialysis patients. Given that hemodialysis patients were not included in clinical trials, we aimed to synthesize the available evidence on the immunogenicity of coronavirus disease 2019 (COVID‐19) mRNA vaccines in hemodialysis patients.

Methods

We searched Scopus, PubMed, Sciencedirect, and finally google scholar databases for studies on COVID‐19 mRNA‐vaccines immunogenicity in hemodialysis patients up to December 1, 2021. Eligible articles measured antibodies against severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) spike or Receptor‐Binding Domain Antibody (S/RBD) postimmunization with COVID‐19 mRNA vaccines. The immunogenicity of the vaccine was evaluated using seroconversion rates measured between 21 and 30 days after the first immunization and between 14 and 36 days post the second dose. We included studies including participants without a history of COVID‐19 before vaccination. Healthy controls or health‐care workers served as the control groups. After selecting eligible articles, the data were finally extracted from included articles. We used a random effects model to estimate the pooled seroconversion rate after COVID‐19 mRNA vaccine administration. We assessed the heterogeneity between studies with the I 2 statistical index.

Result

We selected 39 eligible citations comprising 806 cases and 336 controls for the first dose and 6314 cases and 927 controls for the second dose for statistical analysis. After the first dose of mRNA vaccines, the seroconversion rate was 36% (95% confidence interval [CI]: 0.24–0.47) and 68% (95% CI: 0.45–0.91) in hemodialysis patients and the control group, respectively. While seroconversion rate after the second dose of mRNA vaccines was 86% (95% CI: 0.81–0.91) and 100% (95% CI: 1.00–1.00) in hemodialysis patients and the control group, respectively.

Conclusion

Although the immune response of hemodialysis patients to the second dose of the SARS‐CoV‐2 mRNA vaccine is very promising, the seroconversion rate of dialysis patients is lower than healthy controls. Periodically assessment of antibody levels of hemodialysis patients at short intervals is recommended.

Keywords: chronic kidney disease, COVID‐19 mRNA vaccines, hemodialysis, SARS‐CoV‐2, the seroconversion rate, vaccine immunogenicity

1. INTRODUCTION

Severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) was detected in late 2019 in Wuhan, China. 1 , 2 Coronavirus disease 2019 (COVID‐19) is one of the most critical health problems in the world right now. 3 , 4 , 5 Several vaccines have been licensed for emergency use. 6 , 7 Vaccination remains an essential part of preventive care due to the high infection rate in hemodialysis patients. As kidney function decreases, the antibody response to the vaccine is impaired. Different methods have been used to improve response to influenza A and hepatitis B vaccines, such as higher vaccine doses and more frequent booster vaccinations. 8 Vaccine efficacy in clinical trials has been determined for the general population. However, its efficacy has not been evaluated for vulnerable populations such as hemodialysis patients.

Hemodialysis patients are at high risk in the COVID‐19 pandemic due to increased average age, immunosuppression, renal failure, and frequent visits to dialysis centers. The mortality rate of COVID‐19 in these patients is much higher than in the general population, and up to 32% has been reported. 8 , 9 Including patients with kidney disease in the COVID‐19 vaccine, clinical trials are low. In most trials, people with “severe” or “chronic” kidney disease and people using/undergoing immunosuppression have been excluded. There is not much information about the effectiveness of COVID‐19 vaccines in hemodialysis patients. On the other hand, the effectiveness of previous vaccines such as hepatitis B and influenza in hemodialysis patients has been less than in the general population. The seroconversion rate after influenza virus vaccination is about 33%–80% in hemodialysis patients. 10

The combination of this evidence has raised concerns about the vaccine's efficacy in this group and raised questions: The efficacy of COVID‐19 vaccines and the rate of postvaccination seroresponse in hemodialysis patients has not been fully determined; the duration of immune protection after vaccination is unknown. Seroconversion is related to immune protection from many pathogens, and there is increasing evidence that the same is true for SARS‐CoV‐2. Some studies have found a strong correlation between spike1 antibody titer and neutralization ability, innate immunity and the recruitment of T‐cell‐specific SARS‐CoV‐2 responses. 11

Our objective was to synthesize the available evidence on the immunogenicity of COVID‐19 mRNA vaccines in hemodialysis patients compared with healthy controls.

2. METHODS

2.1. Systematic literature search

We conducted a systematic bibliographic search in the PubMed, Scopus, and Web of Science databases up to December 1, 2021, using the following keywords: (Severe acute respiratory syndrome coronavirus 2 or SARS‐CoV‐2) AND (Coronavirus Disease 2019 or COVID‐19) AND (vaccine efficacy) AND (hemodialysis or dialysis or kidney failure or chronic kidney disease) AND (seroresponse or antibody response or humoral response or serotiter or immunogenicity, effectiveness, or efficacy).

2.2. Eligibility criteria and study selection

Cohort and case–control studies published as of August 1, 2021, were searched. Other publications such as case reports, comments, conference abstracts, and review articles were excluded. We included all original studies on the efficacy or immunogenicity of COVID‐19 mRNA vaccines on hemodialysis patients. Studies written in languages other than English were excluded. Studies with participants without previous or active COVID‐19 infection met the inclusion criteria. In addition, the included studies measured immunoglobulin G (IgG) antibodies against SARS‐CoV‐ 2 S‐protein or RBD fragment. Vaccine immunogenicity was evaluated using seroconversion rates measured between 21 and 30 days after the first immunization and between 14 and 36 days post the second dose of COVID‐19 mRNA vaccines. Healthy controls or health‐care workers served as the control groups. The title and abstract of the articles were read. In the next step, the full text of the articles was evaluated for eligibility. After selecting the relevant studies, the reference list of each article was searched manually. Finally, all eligible articles were included in the study.

2.3. Data extraction

Two researchers independently recorded the following data: first author, year of study, country, type of study, number of cases, number of positive cases, number of the control group, number of positive controls, vaccine type, antibody type, timing post first/second dose (days). Discrepancies among the researchers were resolved through discussions or additional consultations with the third author.

2.4. Statistical analysis

The heterogeneity of studies was assessed using Cochran's Q test and the I 2 index. Due to the high heterogeneity, the random effect model was selected for meta‐analysis. Meta‐regression analysis was used to investigate the relationship between vaccine type and seroconversion rate. We used STATA version 11(STATA Corporation) for the analysis. All levels of significance tests were two‐sided and p‐values less than 0.05 was considered significant.

3. RESULTS

In the first research phase, a total of 2407 relevant articles were identified. After removing 2120 duplicate articles, 287 publications were reviewed for the title and abstract. Of these, 203 were removed due to irrelevance. The full text of another 84 articles was reviewed for eligibility criteria, and 45 articles were excluded due to insufficient data and no measurements of IgG antibody responses against S and RBD. Finally, 39 articles, 8 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 including 806 cases and 336 controls for the first dose and 6314 cases and 927 controls for the second dose, for evaluating immunogenicity were included in the meta‐analysis. The flowchart of the article selection process is shown in Figure 1. Details of all included studies are provided in Tables 1 and 2.

Figure 1.

Figure 1

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Flowchart of article identification and selection in the meta‐analysis

Table 1.

Antibody response data in dialysis patients after the first dose of mRNA vaccines

(8, 12‐15) Year Country Type of study Number of cases Number of positive cases (%) Number of the control group Number of positive controls (%) Vaccine type Antibody type Timing post first dose (days)
1 Goupil et al. 12 2021 Canada Case–Control 131 56 (43%) 20 19 (95%) BNT162b2 Anti‐RBD IgG 28
2 Torregiani et al. 13 2021 France Cohort 95 35 (36.84) None None BNT162b2 Anti‐S IgG 21
3 Speer et al. 8 2021 Germany Case–Control 22 4 (18%) 46 43 (93%) BNT162b2 Anti‐S1 IgG 17–22
4 Yau et al. 14 2021 Canada Case–Control 66 53 (80%) 35 None BNT162b2 Anti‐S IgG 28
5 Attias et al. 15 2021 France Cohort 56 10 (18%) None None BNT162b2 Anti‐S1 IgG 28
6 Longline et al. 16 2021 France Cohort 80 17 (21.5%) None None BNT162b2 Anti‐RBD TOTAL 30
7 Weigert et al. 17 2021 Portugal Case–Control 143 42 (29.4%) 143 71 (49/7%) BNT162b2 Anti S‐IgG 21
8 Broseta et al. 18 2021 Spain Cohort 78 44 (56.4%) None None mRNA‐1273 Anti‐S IgG 28
9 Lesny et al. 19 2021 Germany Cohort 11 2 (18.18) 14 8 BNT162b2 Anti‐S IgG 2
10 Duarte et al. 20 2021 Portugal Cohort 42 21 (50%) None none BNT162b2 Anti‐S IgG 21
11 Kolb et al. 21 2021 Germany Case–Control 32 3 (11%) 78 33 (42%) BNT162b2 Anti‐RBD IgG 20
12 Zitt et al. 22 2021 Austria Cohort 50 21 (42%) None None BNT162b2 Anti‐S IgG 28
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Table 2.

Antibody response data in dialysis patients after the second dose of mRNA vaccines

Author Year Country Type of study Number of cases Number of positive cases (%) Number of the control group Number of positive controls (%) Vaccine type Antibody type Timing post second dose (days)
1 Grupper et al. 23 2021 Israel Case‐Control 56 54 (96%) 95 95 (100%) BNT162b2 Anti–RBD IgG 30
2 Speer et al. 8 2021 Germany Case‐Control 17 14 (82%) 46 46 (100%) BNT162b2 Anti‐S1 IgG 18–22
3 Frantzen et al. 24 2021 France Cohort 244 221 (91%) None None BNT162b2 Anti‐S IgG 30
4 Simon et al. 25 2021 Austria Case‐Control 81 74 (91.35%) 80 80 (100%) BNT162b2 Anti‐S total 21
5 Jahn et al. 26 2021 Germany Case‐Control 72 67 (93%) 16 16 (100%) BNT162b2 Anti‐S IgG 14
6 Yau et al.  14 2021 Canada Case‐Control 72 69 (96%) 35 35 (100%) BNT162b2 Anti S‐IgG 14
7 Attias et al. 15 2021 France Cohort 52 43 (82%) None None BNT162b2 Anti‐S1 IgG 21
8 Schrezenmeier et al. 27 2021 Germany Case‐Control 36 32 (88.9%) 44 40 (91%) BNT162b2 Anti‐RBD IgG 21
9 Agur et al. 28 2021 Israel Prospective Cohort 122 114 (93.4%) None None BNT162b2 Anti‐S IgG 36
10 Arevalo et al. 29 2021 Germany Case‐Control 44 31 (70/5%) 35 35 (100%) BNT162b2 Anti‐S1 IgG 21–28
11 Longlune et al.  16 2021 France Cohort 77 64 (83.11%) NONE NONE BNT162b2 Anti‐RBD TOTAL 30
12 Strengert et al. 30 2021 Germany Case‐Control 81 95% 34 34 (100%) BNT162b2 Anti‐S1 IgG 21
13 Lacson et al. 31 2021 United States Cohort 148 130 (88.1%) None None BNT162b2 Anti‐RBD IgG ≥14
14 Broseta et al. 32 2021 Spain Cohort 75 69 (92%) None None BNT162b2 Anti‐RBD IgG 21
15 Garcia et al. 33 2021 United States Cohort 416 369 (88.6) None None BNT162b2 Anti‐RBD IgG 14–28
16 Ducloux et al. 34 2021 France Cohort 50 45 (90%) None None BNT162b2 Anti‐RBD IgG 30
17 Garcia et al. 33 2021 United States Cohort 1316 1247 (94.8) None None mRNA‐1273 Anti‐RBD IgG 14–28
18 Broseta et al. 32 2021 Spain Cohort 100 98 (98%) None None mRNA‐1273 Anti‐RBD IgG 21
19 Lacson et al. 31 2021 United States Cohort 18 17 (94.4%) None None mRNA‐1273 Anti‐RBD IgG ≥14
20 Espi et al. 18 2021 France Case‐Control 92 73 (79.35) 26 26 (100%) BNT162b2 Anti‐RBD IgG 10–14
21 Espi et al. 32 2021 France Case‐Control 75 63 (84) 30 30 (100%) BNT162b2 Anti‐RBD IgG 10–14
22 Weigert et al. 17 2021 Portugal Case‐Control 143 130 (90.9%) 143 136 (95.1%) BNT162b2 Anti S‐IgG 21
23 Stumpf et al. 35 2021 Germany Cohort 936 908 (97%) None None mRNA‐1273 Anti‐S1 IgG 28
24 Stumpf et al. 35 2021 Germany Cohort 200 176 (88%) None None BNT162b2 Anti‐S1 IgG 35
25 Clarke et al. 36 2021 England Cohort 281 248 (88.3%) None None BNT162b2 Anti S‐IgG ≥14
26 Dulovic et al. 37 2021 Germany 76 72 23 23 BNT162b2 Anti‐RBD IgG 21
27 Hsu et al. 38 2021 USA Cohort 437 381 None None BNT162b2 Anti‐RBD IgG 14
28 Bertrand et al. 39 2021 France Cohort 45 8 (88.9%) None None BNT162b2 Anti‐S1 IgG 14
29 Danthu et al. 40 2021 France Cohort 78 59 (85.5) 7 7 BNT162b2 Anti‐S IgG 14
30 Duarte et al. 20 2021 Portugal Cohort 42 6 (14%) None None BNT162b2 Anti‐S IgG 21
31 Zitt et al. 22 2021 Austria Cohort 48 47(97.9%) None None BNT162b2 Anti‐S IgG 14
32 Paal et al. 41 2021 Germany Cohort 179 173 (96.6) 70 68 (97.1) BNT162b2 Anti‐S IgG 21
33 Giot et al. 42 2021 France Cohort 71 55 (77%) None None BNT162b2 Anti‐S IgG 14
34 Dekervel et al. 43 2021 France Cohort 66 50 None None BNT162b2 Anti‐S IgG 14
35 Labriola et al. 44 2021 Belgium Case‐Control 24 19 (79%) 33 28 (85%) BNT162b2 Anti‐RBD IgG 28
36 Kolb et al. 21 2021 Germany Cohort 32 28 (88%) 78 73 BNT162b2 Anti‐RBD IgG 14
37 Broseta et al. 18 2021 Spain Cohort 78 74 (94.9) None None mRNA‐1273 Anti‐S IgG 21
38 Kaiser et al. 45 2021 Austria Cohort 77 76 (98.7) None None mRNA‐1273 Anti‐RBD IgG 21
39 Kaiser et al. 45 2021 Austria Cohort 39 37 (94.8) None None BNT162b2 Anti‐RBD IgG 21
40 Yanay et al. 46 2021 Israel Cohort 127 115 (90.5%) 132 132 BNT162b2 Anti‐S IgG 21–35
41 Tylicki et al. 47 2021 Poland Cohort 91 87 (95.6) None None BNT162b2 Anti‐S IgG 14–21
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Seroconversion rate after the first dose of mRNA vaccines was 36% (95% CI: 0.24–0.47) and 68% (95% CI: 0.45–0.91) in hemodialysis patients and the control group, respectively (Figure 2). While seroconversion rate after the second dose of mRNA vaccines was 86% (95% CI: 0.81–0.91) and 100% (95% CI: 1.00–1.00) in hemodialysis patients and in the control group, respectively (Figure 3). Evaluation of the relationship between vaccine type and seroconversion rate using a meta‐regression model showed no significant differences between any of BNT162b2 and mRNA1273 vaccines and seroconversion rate after two doses of vaccine.

Figure 2.

Figure 2

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Forest plot for the seroconversion rate after the first dose of mRNA‐based vaccines (A) cases, (B) controls

Figure 3.

Figure 3

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Forest plot for the seroconversion rate after the second dose of mRNA‐based vaccines, (A) Cases, (B) Controls

4. DISCUSSION

The mRNA‐based vaccines showed more than 90% efficacy in preventing COVID‐19 disease. 25 , 48 Patients with severe kidney disease were not present in clinical trials; therefore, the vaccine's efficacy in this high‐risk group has not been evaluated. Compared with the general population, hemodialysis patients have a lower response to hepatitis B and influenza vaccination.

Immunological changes include a distorted Th1/Th2 response, altered function of professional antigen‐presenting cells (APC), and susceptibility of B cells to apoptosis compared with people without kidney disease, making dialysis patients less likely to seroconvert and maintain protective serum titers over time. 31 , 49 After clinical trials and vaccine approval, several studies in dialysis centers examined seroconversion rates following the administration of two doses of mRNA‐based vaccines. The efficacy of vaccination was evaluated 14–30 days post the second injection by quantifying antibodies against spike protein, which shows a strong correlation with neutralizing antibodies.

Our results show that hemodialysis's seroconversion rate after the first dose of mRNA vaccines was 36% (95% CI: 0.24–0.47) and 68% (95% CI: 0.45–0.91) in patients and the control group, respectively. While seroconversion rate after the second dose of mRNA vaccines was 86% (95% CI: 0.81–0.91) and 100% (95% CI: 1.00–1.00) in hemodialysis patients and the control group, respectively.

The results of this meta‐analysis show that the seroconversion rate is low after the first dose of the vaccine, and the administration of the second dose should not be delayed. Although the seroconversion rate after the second dose in hemodialysis patients is lower than in the control group, it is very promising for hemodialysis patients.

Our results showed that mRNA‐based vaccines induce comparable seroconversion rates in hemodialysis patients and healthy controls. Our results indicate that the mRNA platform can be used to improve the immunogenicity of vaccines against other pathogens in hemodialysis patients.

The COVID‐19 mRNA‐based vaccine immunogenicity in hemodialysis patients is much greater than that of influenza and hepatitis B vaccines immunogenicity.

Several factors can contribute to the higher immunogenicity of mRNA‐based vaccines compared with the previous vaccines among hemodialysis patients. First, the vaccine platform is different; second, mRNA‐based vaccines’ efficacy has been studied in hemodialysis patients during the pandemic. It is possible that in some individuals, the combination of natural immunity after infection and vaccine‐generated immunity positively impacts the vaccine efficacy. 15 , 50 However, in some studies, initial/baseline infection or history of the previous infection of COVID‐19 has been actively monitored in the study population; these people were excluded from the study or located in a separate group. 15 , 27 , 28 , 51

The limitations of this study include: the small sample size, and also our study includes articles that assessed the efficacy of mRNA‐based vaccines by antibody titer. seroconversion and antibody titer is an easy method to evaluate the immunological response to vaccination, but it is not equivalent to complete protection. 52 Also, the antibody levels required to protect against COVID‐19 have not yet been determined. 53 However, to assess vaccine responses, it is recommended to assess both humoral and cellular responses. 54 However, due to limited data on vaccine‐mediated cellular immunity, this study focused on investigating humoral immune responses after vaccination.

Although the seroconversion rate is high, many studies have reported that the antibody level of hemodialysis patients after being vaccinated with the COVID‐19 vaccine is lower than that of the control group; as a result, a shorter period of immune protection can be assumed. Therefore, it is necessary to periodically assess the antibody levels of hemodialysis patients at short intervals and renew their vaccination when necessary.

5. CONCLUSION

Although the immune response of hemodialysis patients to the second dose of SARS‐CoV‐2 mRNA vaccine is very promising, the seroconversion rate of dialysis patients is lower than healthy controls. As a result, it is necessary to pay more attention to the vaccination programs of this population, periodically assess the antibody levels of hemodialysis patients at short intervals and renew their vaccination when necessary.

AUTHOR CONTRIBUTIONS

Shahab Falahi: Conceptualization; data curation; formal analysis; supervision; writing – original draft; writing – review & editing. Hojjat Sayyadi: Conceptualization; data curation; formal analysis; methodology; software. Azra Kenarkoohi: Conceptualization; data curation; formal analysis; project administration; supervision; writing – original draft; writing – review & editing.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

TRANSPARENCY STATEMENT

The lead author Azra Kenarkoohi affirms that this manuscript is an honest, accurate, and transparent account of the study being reported; that no important aspects of the study have been omitted; and that any discrepancies from the study as planned (and, if relevant, registered) have been explained.

Falahi S, Sayyadi H, Kenarkoohi A. Immunogenicity of COVID‐19 mRNA vaccines in hemodialysis patients: systematic review and meta‐analysis. Health Sci Rep. 2022;5:e874. 10.1002/hsr2.874

DATA AVAILABILITY STATEMENT

Data sharing does not apply to this article as no datasets were generated or analyzed during the current study.

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Data Availability Statement

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