Antibody response and safety of COVID-19 vaccine in peritoneal dialysis patients

Abstract

We read with interest a recent article reported by Ao et al.1Ao G. Li A. Wang Y. Tran C. Gao M. Chen M. The effect of SARS-CoV-2 double vaccination on the outcomes of hemodialysis patients with COVID-19: a meta-analysis.J Infect. 2022; https://doi.org/10.1016/j.jinf.2022.09.022Abstract Full Text Full Text PDF Google Scholar The authors reported a meta-analysis describing the outcomes of hemodialysis patients infected with COVID-19 after SARS-CoV-2 double vaccination. They found that two doses of SARS-CoV-2 vaccination was associated with reduced mortality and need for oxygen supplementation in hemodialysis patients with COVID-19. Peritoneal dialysis (PD) patients are another group of immunocompromised patients. They are vulnerable to COVID-19 infection like hemodialysis patients due to their immunocompromised state. They are also at increased risk of developing serious complications if they contract the virus. COVID-19 vaccine can contribute to reduce the risk of infection of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). However, it is well recognized that chronic kidney disease patients have reduced vaccine response. Hence, meta-analysis of the antibody response and safety of COVID-19 vaccine in patients with PD is of great significance. An extensive literature search was performed in PubMed, Web of Science, and EMBASE to find all relevant studies published from January 1, 2020, to October 05, 2022. We screened the references of the retrieved studies and restricted the language of the search to English. The following keywords were used in the search: COVID-19 vaccines (SARS-CoV-2 vaccines, SARS2 vaccines, SARS Coronavirus 2 vaccines, Coronavirus Disease 2019 vaccines, 2019-nCoV vaccine, and 2019 Novel Coronavirus vaccines) and peritoneal dialysis. The inclusion criteria included: (1) patients diagnosed with chronic kidney disease patients receiving PD and receiving COVID-19 vaccines, and (2) English article. The exclusion criteria were as follows: (1) irrelevant to the research direction, (2) no relevant data, (3) case reports, (4) repeated articles, and (5) review papers. The analysis was conducted using Review Manager statistical software, version 5.3. A binary controlled study was used to calculate the number of positive rates of anti-SARS-CoV-2 spike protein IgG or adverse events. Odds ratio (OR) and 95% confidence interval (CI) were used to assess the effect in a whole random-effects meta-analysis model. The I2 and P value was used to quantify the heterogeneity of the effects among the included studies. A total of eighteen studies involving 4434 patients were identified in the final analysis, and the details of the included studies are listed in Table 1.2Bassi J. Giannini O. Silacci-Fregni C. Pertusini L. Hitz P. Terrot T. et al.Poor neutralization and rapid decay of antibodies to SARS-CoV-2 variants in vaccinated dialysis patients.PLoS ONE. 2022; 17e0263328https://doi.org/10.1371/journal.pone.0263328Crossref Scopus (9) Google Scholar, 3Bruminhent J. Setthaudom C. Kitpermkiat R. Kiertiburanakul S. Malathum K. Assanatham M. et al.Immunogenicity of ChAdOx1 nCoV-19 vaccine after a two-dose inactivated SARS-CoV-2 vaccination of dialysis patients and kidney transplant recipients.Sci Rep. 2022; 12: 3587https://doi.org/10.1038/s41598-022-07574-wCrossref PubMed Scopus (4) Google Scholar, 4Crespo M. Barrilado-Jackson A. Padilla E. Eguia J. Echeverria-Esnal D. Cao H. et al.Negative immune responses to two-dose mRNA COVID-19 vaccines in renal allograft recipients assessed with simple antibody and interferon gamma release assay cellular monitoring.Am J Transplant. 2022; 22: 786-800https://doi.org/10.1111/ajt.16854Crossref PubMed Scopus (19) Google Scholar, 5Duarte R. Roldao M. Figueiredo C. Luz I. Ferrer F. Goncalves H. et al.Humoral response to BNT162b2 mRNA COVID-19 vaccine in peritoneal and hemodialysis patients: a comparative study.Ther Apher Dial. 2022; 26: 790-796https://doi.org/10.1111/1744-9987.13766Crossref PubMed Scopus (3) Google Scholar, 6Haase M. Lesny P. Haase-Fielitz A. Anderson M. Cloherty G. Stec M. et al.Immunogenicity and tolerability of COVID-19 vaccination in peritoneal dialysis patients-A prospective observational cohort study.Semin Dial. 2022; 35: 269-277https://doi.org/10.1111/sdi.13043Crossref PubMed Scopus (2) Google Scholar, 7Lesny P. Anderson M. Cloherty G. Stec M. Haase-Fielitz A. Haarhaus M. et al.Immunogenicity of a first dose of mRNA- or vector-based SARS-CoV-2 vaccination in dialysis patients: a multicenter prospective observational pilot study.J Nephrol. 2021; 34: 975-983https://doi.org/10.1007/s40620-021-01076-0Crossref PubMed Scopus (19) Google Scholar, 8Longlune N. Nogier M.B. Miedouge M. Gabilan C. Cartou C. Seigneuric B. et al.High immunogenicity of a messenger RNA-based vaccine against SARS-CoV-2 in chronic dialysis patients.Nephrol Dial Transplant. 2021; 36: 1704-1709https://doi.org/10.1093/ndt/gfab193Crossref PubMed Scopus (61) Google Scholar, 9Matsunami M. Suzuki T. Terao T. Kuji H. Matsue K. Immune response to SARS-CoV-2 vaccination among renal replacement therapy patients with CKD: a single-center study.Clin Exp Nephrol. 2022; 26: 305-307https://doi.org/10.1007/s10157-021-02156-yCrossref PubMed Scopus (5) Google Scholar, 10Murt A. Altiparmak M.R. Ozbey D. Yalin S.F. Sert Yadigar S. et al.Antibody responses to inactivated SARS-CoV-2 vaccine in peritoneal dialysis patients.Semin Dial. 2022; 35: 264-268https://doi.org/10.1111/sdi.13049Crossref PubMed Scopus (2) Google Scholar, 11Murt A. Dinc H.O. Altiparmak M.R. Yalin S.F. Yadigar S. Parmaksiz E. et al.Waning of SARS-CoV-2 vaccine-induced immune response over 6 months in peritoneal dialysis patients and the role of a booster dose in maintaining seropositivity.Nephron. 2022; : 1-5https://doi.org/10.1159/000524658Crossref PubMed Scopus (1) Google Scholar, 12Nacasch N. Cohen-Hagai K. Benchetrit S. Zitman-Gal T. Einbinder Y. Erez D. et al.Comparison of long-term antibody response to mRNA SARS-CoV-2 vaccine among peritoneal dialysis and hemodialysis patients.Nephrol Dial Transplant. 2022; 37: 602-604https://doi.org/10.1093/ndt/gfab321Crossref PubMed Scopus (3) Google Scholar, 13Patecki M. Merscher S. Dumann H. Bernhardt W. Dopfer-Jablonka A. Cossmann A. 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: 100-101https://doi.org/10.1177/08968608211055631Crossref PubMed Scopus (4) Google Scholar, 14Piotrowska M. Zielinski M. Tylicki L. Biedunkiewicz B. Kubanek A. Slizien Z. et al.Local and systemic immunity are impaired in end-stage-renal-disease patients treated with hemodialysis, peritoneal dialysis and kidney transplant recipients immunized with BNT162b2 Pfizer-BioNTech SARS-CoV-2 vaccine.Front Immunol. 2022; 13832924https://doi.org/10.3389/fimmu.2022.832924Crossref PubMed Scopus (2) Google Scholar, 15Polewska K. Tylicki P. Biedunkiewicz B. Rucinska A. Szydlowska A. Kubanek A. et al.Safety and tolerability of the BNT162b2 mRNA COVID-19 vaccine in dialyzed patients. COViNEPH project.Medicina (Kaunas). 2021; 57https://doi.org/10.3390/medicina57070732Crossref PubMed Scopus (18) Google Scholar, 16Speer C. Schaier M. Nusshag C. Tollner M. Buylaert M. Kalble F. et al.Longitudinal humoral responses after COVID-19 vaccination in peritoneal and hemodialysis patients over twelve weeks.Vaccines (Basel). 2021; 9https://doi.org/10.3390/vaccines9101130Crossref Scopus (20) Google Scholar, 17Tylicki L. Piotrowska M. Biedunkiewicz B. Zielinski M. Dabrowska M. Tylicki P. et al.Humoral response to COVID19 vaccination in patients treated with peritoneal dialysis: the COViNEPH project.Pol Arch Intern Med. 2021; 131https://doi.org/10.20452/pamw.16091Crossref Scopus (6) Google Scholar, 18Wang H.H. Wu J.L. Chang M.Y. Wu H.M. Ho L.C. Chi P.J. et al.Antibody response and adverse events of AZD1222 COVID-19 vaccination in patients undergoing dialysis: a prospective cohort study.Vaccines (Basel). 2022; 10https://doi.org/10.3390/vaccines10091460Crossref Scopus (0) Google Scholar, 19Yanay N.B. Freiman S. Shapira M. Wishahi S. Hamze M. Elhaj M. et al.Experience with SARS-CoV-2 BNT162b2 mRNA vaccine in dialysis patients.Kidney Int. 2021; 99: 1496-1498https://doi.org/10.1016/j.kint.2021.04.006Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar Eighteen studies showed that the overall OR of positive rates of anti-SARS-CoV-2 spike protein IgG following COVID-19 vaccination in PD patients vs. healthy control subtyped for dose of vaccine was 0.36 (95% CI, 0.16−0.83, P = 0.02), the single dose vaccine was 0.44 (95% CI, 0.09−2.16, P = 0.31), and the double dose vaccine was 0.36 (95% CI, 0.13−0.98, P = 0.04) (Fig. 1). The positive rate in PD patients were significantly lower than that in healthy group, especially the double doses vaccine.Table 1Baseline characteristics of the included studies.StudyGroupEventsNumber of events (n)Total (n)Dose of vaccineBassi et al.2Bassi J. Giannini O. Silacci-Fregni C. Pertusini L. Hitz P. Terrot T. et al.Poor neutralization and rapid decay of antibodies to SARS-CoV-2 variants in vaccinated dialysis patients.PLoS ONE. 2022; 17e0263328https://doi.org/10.1371/journal.pone.0263328Crossref Scopus (9) Google ScholarPDspike IgG12122Healthyspike IgG47472Hemodialysisspike IgG1141212Bruminhent et al. 3Bruminhent J. Setthaudom C. Kitpermkiat R. Kiertiburanakul S. Malathum K. Assanatham M. et al.Immunogenicity of ChAdOx1 nCoV-19 vaccine after a two-dose inactivated SARS-CoV-2 vaccination of dialysis patients and kidney transplant recipients.Sci Rep. 2022; 12: 3587https://doi.org/10.1038/s41598-022-07574-wCrossref PubMed Scopus (4) Google ScholarPDspike IgG23282Healthyspike IgG16162Hemodialysisspike IgG29312Crespo et al. 4Crespo M. Barrilado-Jackson A. Padilla E. Eguia J. Echeverria-Esnal D. Cao H. et al.Negative immune responses to two-dose mRNA COVID-19 vaccines in renal allograft recipients assessed with simple antibody and interferon gamma release assay cellular monitoring.Am J Transplant. 2022; 22: 786-800https://doi.org/10.1111/ajt.16854Crossref PubMed Scopus (19) Google ScholarPDspike IgG28292Healthyspike IgG32322Hemodialysisspike IgG55582Duarte et al. 5Duarte R. Roldao M. Figueiredo C. Luz I. Ferrer F. Goncalves H. et al.Humoral response to BNT162b2 mRNA COVID-19 vaccine in peritoneal and hemodialysis patients: a comparative study.Ther Apher Dial. 2022; 26: 790-796https://doi.org/10.1111/1744-9987.13766Crossref PubMed Scopus (3) Google ScholarPDspike IgG22251Hemodialysisspike IgG21421PDspike IgG25252Hemodialysisspike IgG36422Haase et al. 6Haase M. Lesny P. Haase-Fielitz A. Anderson M. Cloherty G. Stec M. et al.Immunogenicity and tolerability of COVID-19 vaccination in peritoneal dialysis patients-A prospective observational cohort study.Semin Dial. 2022; 35: 269-277https://doi.org/10.1111/sdi.13043Crossref PubMed Scopus (2) Google ScholarPDspike IgG21212Healthyspike IgG24242PDLocal adverse events10281HealthyLocal adverse events23281PDLocal adverse events7232HealthyLocal adverse events16262PDSystemic adverse events3281HealthySystemic adverse events20281PDSystemic adverse events2232HealthySystemic adverse events16262Lesny et al.7Lesny P. Anderson M. Cloherty G. Stec M. Haase-Fielitz A. Haarhaus M. et al.Immunogenicity of a first dose of mRNA- or vector-based SARS-CoV-2 vaccination in dialysis patients: a multicenter prospective observational pilot study.J Nephrol. 2021; 34: 975-983https://doi.org/10.1007/s40620-021-01076-0Crossref PubMed Scopus (19) Google ScholarPDspike IgG441Healthyspike IgG8141Hemodialysisspike IgG4231Longlune et al. 8Longlune N. Nogier M.B. Miedouge M. Gabilan C. Cartou C. Seigneuric B. et al.High immunogenicity of a messenger RNA-based vaccine against SARS-CoV-2 in chronic dialysis patients.Nephrol Dial Transplant. 2021; 36: 1704-1709https://doi.org/10.1093/ndt/gfab193Crossref PubMed Scopus (61) Google ScholarPDspike IgG10241Hemodialysisspike IgG17801PDspike IgG17202Hemodialysisspike IgG74822Matsunami et al.9Matsunami M. Suzuki T. Terao T. Kuji H. Matsue K. Immune response to SARS-CoV-2 vaccination among renal replacement therapy patients with CKD: a single-center study.Clin Exp Nephrol. 2022; 26: 305-307https://doi.org/10.1007/s10157-021-02156-yCrossref PubMed Scopus (5) Google ScholarPDspike IgG26272Healthyspike IgG38382Hemodialysisspike IgG77782Murt et al.10Murt A. Altiparmak M.R. Ozbey D. Yalin S.F. Sert Yadigar S. et al.Antibody responses to inactivated SARS-CoV-2 vaccine in peritoneal dialysis patients.Semin Dial. 2022; 35: 264-268https://doi.org/10.1111/sdi.13049Crossref PubMed Scopus (2) Google ScholarPDspike IgG19202Healthyspike IgG54612Hemodialysisspike IgG35412Murt et al.11Murt A. Dinc H.O. Altiparmak M.R. Yalin S.F. Yadigar S. Parmaksiz E. et al.Waning of SARS-CoV-2 vaccine-induced immune response over 6 months in peritoneal dialysis patients and the role of a booster dose in maintaining seropositivity.Nephron. 2022; : 1-5https://doi.org/10.1159/000524658Crossref PubMed Scopus (1) Google ScholarPDspike IgG22232Healthyspike IgG28292Hemodialysisspike IgG41512Nacasch et al.12Nacasch N. Cohen-Hagai K. Benchetrit S. Zitman-Gal T. Einbinder Y. Erez D. et al.Comparison of long-term antibody response to mRNA SARS-CoV-2 vaccine among peritoneal dialysis and hemodialysis patients.Nephrol Dial Transplant. 2022; 37: 602-604https://doi.org/10.1093/ndt/gfab321Crossref PubMed Scopus (3) Google ScholarPDspike IgG52642Hemodialysisspike IgG931182Patecki et al.13Patecki M. Merscher S. Dumann H. Bernhardt W. Dopfer-Jablonka A. Cossmann A. 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: 100-101https://doi.org/10.1177/08968608211055631Crossref PubMed Scopus (4) Google ScholarPDspike IgG13301Hemodialysisspike IgG15301PDspike IgG26302Hemodialysisspike IgG30302Piotrowska et al.14Piotrowska M. Zielinski M. Tylicki L. Biedunkiewicz B. Kubanek A. Slizien Z. et al.Local and systemic immunity are impaired in end-stage-renal-disease patients treated with hemodialysis, peritoneal dialysis and kidney transplant recipients immunized with BNT162b2 Pfizer-BioNTech SARS-CoV-2 vaccine.Front Immunol. 2022; 13832924https://doi.org/10.3389/fimmu.2022.832924Crossref PubMed Scopus (2) Google ScholarPDspike IgG18211Healthyspike IgG29341PDspike IgG21212Healthyspike IgG34342Hemodialysisspike IgG20351Hemodialysisspike IgG34352Polewska et al.15Polewska K. Tylicki P. Biedunkiewicz B. Rucinska A. Szydlowska A. Kubanek A. et al.Safety and tolerability of the BNT162b2 mRNA COVID-19 vaccine in dialyzed patients. COViNEPH project.Medicina (Kaunas). 2021; 57https://doi.org/10.3390/medicina57070732Crossref PubMed Scopus (18) Google ScholarPDLocal adverse events16201HealthyLocal adverse events1021611PDLocal adverse events12202HealthyLocal adverse events1021592PDSystemic adverse events6201HealthySystemic adverse events281611PDSystemic adverse events7202HealthySystemic adverse events481592Speer et al.16Speer C. Schaier M. Nusshag C. Tollner M. Buylaert M. Kalble F. et al.Longitudinal humoral responses after COVID-19 vaccination in peritoneal and hemodialysis patients over twelve weeks.Vaccines (Basel). 2021; 9https://doi.org/10.3390/vaccines9101130Crossref Scopus (20) Google ScholarPDspike IgG22411Healthyspike IgG17201PDspike IgG39412Healthyspike IgG20202Hemodialysisspike IgG441241Hemodialysisspike IgG1091242Tylicki et al.17Tylicki L. Piotrowska M. Biedunkiewicz B. Zielinski M. Dabrowska M. Tylicki P. et al.Humoral response to COVID19 vaccination in patients treated with peritoneal dialysis: the COViNEPH project.Pol Arch Intern Med. 2021; 131https://doi.org/10.20452/pamw.16091Crossref Scopus (6) Google ScholarPDspike IgG18211Hemodialysisspike IgG20351PDspike IgG21212Hemodialysisspike IgG34352Wang et al.18Wang H.H. Wu J.L. Chang M.Y. Wu H.M. Ho L.C. Chi P.J. et al.Antibody response and adverse events of AZD1222 COVID-19 vaccination in patients undergoing dialysis: a prospective cohort study.Vaccines (Basel). 2022; 10https://doi.org/10.3390/vaccines10091460Crossref Scopus (0) Google ScholarPDspike IgG801161Healthyspike IgG33341PDspike IgG1081162Healthyspike IgG34342Hemodialysisspike IgG1472041Hemodialysisspike IgG1922042Yanay et al.19Yanay N.B. Freiman S. Shapira M. Wishahi S. Hamze M. Elhaj M. et al.Experience with SARS-CoV-2 BNT162b2 mRNA vaccine in dialysis patients.Kidney Int. 2021; 99: 1496-1498https://doi.org/10.1016/j.kint.2021.04.006Abstract Full Text Full Text PDF PubMed Scopus (80) Google ScholarPDspike IgG30332Healthyspike IgG1321322 Open table in a new tab In sixteen studies, we found that the overall OR of positive rate of anti-SARS-CoV-2 spike protein IgG following COVID-19 vaccination in PD vs. hemodialysis patients subtyped for dose of vaccine was 1.64 (95% CI, 1.09−247, P = 0.02), the single dose vaccine was 2.43 (95% CI, 1.24−4.73, P = 0.009), and the double dose vaccine was 1.12(95% CI, 0.72−1.73, P = 0.62) (Fig. 2). The positive rate in PD patients were higher than that in hemodialysis patients. However, there was no significant difference in positive rate between PD patients and hemodialysis patients following the double dose COVID-19 vaccine. In four studies, we found that the overall OR of adverse events following COVID-19 vaccine in PD patients vs. healthy control was 0.42 (95% CI, 0.15−1.13, P = 0.09), the OR of local adverse events was 0.52 (95% CI, 0.15−1.73, P = 0.28), and the OR of systemic adverse events was 0.32 (95% CI, 0.05−2.04, P = 0.23) Fig. 3. There was no significant difference in local and systemic adverse events in PD patients and healthy persons following COVID-19 vaccination. In conclusion, our research showed that PD patients produced lower levels of anti-SARS-CoV-2 spike protein IgG after two doses of COVID-19 vaccine in comparison to healthy persons. However, our study also showed that the positive rate in PD patients were higher than hemodialysis patients. Hence, we think COVID-19 vaccine may serve as a sufficient protective role in reducing the severity of disease and likelihood of overall mortality in PD patients like hemodialysis patients. In addition, the current COVID-19 vaccine for patients with PD was safe. Future studies should determine adverse events of each vaccine type and critically identify mechanisms of severe adverse events following vaccination in PD patients. All authors report that they have no potential conflicts of interest.