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

  • Author Footnotes
    1 These authors contributed equally to this work and should be regarded as co-first authors.
    Qian Zheng
    Footnotes
    1 These authors contributed equally to this work and should be regarded as co-first authors.
    Affiliations
    Department of Neurology, Affiliated Hospital of Guizhou Medical University, Guiyang, China
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  • Author Footnotes
    1 These authors contributed equally to this work and should be regarded as co-first authors.
    Mingwei Wang
    Footnotes
    1 These authors contributed equally to this work and should be regarded as co-first authors.
    Affiliations
    Department of Cardiology, Affiliated Hospital of Hangzhou Normal University, Hangzhou, China
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  • Yongran Cheng
    Affiliations
    School of Public Health, Hangzhou Medical College, Hangzhou, China
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  • Jiming Liu
    Affiliations
    The Affiliated Baiyun Hospital of Guizhou Medical University, China
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  • Zhanhui Feng
    Correspondence
    Corresponding authors
    Affiliations
    Department of Neurology, Affiliated Hospital of Guizhou Medical University, Guiyang, China
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  • Lan Ye
    Correspondence
    Corresponding authors
    Affiliations
    The Medical Science Function Laboratory of Experimental Teaching Center of Basic Medicine, School of Basic Medical Science, Guizhou Medical University, Guiyang, China
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  • Author Footnotes
    1 These authors contributed equally to this work and should be regarded as co-first authors.
Published:October 17, 2022DOI:https://doi.org/10.1016/j.jinf.2022.10.014
      To the Editor:
      We read with interest a recent article reported by Ao et al.
      • Ao 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.
      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.
      • Bassi 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.
      • Bruminhent 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.
      • Crespo 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.
      • Duarte 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.
      • Haase 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.
      • Lesny 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.
      • Longlune 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.
      • Matsunami 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.
      • Murt 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.
      • Murt 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.
      • Nacasch 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.
      • Patecki 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.
      • Piotrowska 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.
      • Polewska 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.
      • Speer 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.
      • Tylicki 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.
      • Wang 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.
      • Yanay 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.
      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 vaccine
      Bassi et al.
      • Bassi 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.
      PDspike IgG12122
      Healthyspike IgG47472
      Hemodialysisspike IgG1141212
      Bruminhent et al.
      • Bruminhent 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.
      PDspike IgG23282
      Healthyspike IgG16162
      Hemodialysisspike IgG29312
      Crespo et al.
      • Crespo 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.
      PDspike IgG28292
      Healthyspike IgG32322
      Hemodialysisspike IgG55582
      Duarte et al.
      • Duarte 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.
      PDspike IgG22251
      Hemodialysisspike IgG21421
      PDspike IgG25252
      Hemodialysisspike IgG36422
      Haase et al.
      • Haase 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.
      PDspike IgG21212
      Healthyspike IgG24242
      PDLocal adverse events10281
      HealthyLocal adverse events23281
      PDLocal adverse events7232
      HealthyLocal adverse events16262
      PDSystemic adverse events3281
      HealthySystemic adverse events20281
      PDSystemic adverse events2232
      HealthySystemic adverse events16262
      Lesny et al.
      • Lesny 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.
      PDspike IgG441
      Healthyspike IgG8141
      Hemodialysisspike IgG4231
      Longlune et al.
      • Longlune 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.
      PDspike IgG10241
      Hemodialysisspike IgG17801
      PDspike IgG17202
      Hemodialysisspike IgG74822
      Matsunami et al.
      • Matsunami 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.
      PDspike IgG26272
      Healthyspike IgG38382
      Hemodialysisspike IgG77782
      Murt et al.
      • Murt 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.
      PDspike IgG19202
      Healthyspike IgG54612
      Hemodialysisspike IgG35412
      Murt et al.
      • Murt 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.
      PDspike IgG22232
      Healthyspike IgG28292
      Hemodialysisspike IgG41512
      Nacasch et al.
      • Nacasch 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.
      PDspike IgG52642
      Hemodialysisspike IgG931182
      Patecki et al.
      • Patecki 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.
      PDspike IgG13301
      Hemodialysisspike IgG15301
      PDspike IgG26302
      Hemodialysisspike IgG30302
      Piotrowska et al.
      • Piotrowska 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.
      PDspike IgG18211
      Healthyspike IgG29341
      PDspike IgG21212
      Healthyspike IgG34342
      Hemodialysisspike IgG20351
      Hemodialysisspike IgG34352
      Polewska et al.
      • Polewska 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.
      PDLocal adverse events16201
      HealthyLocal adverse events1021611
      PDLocal adverse events12202
      HealthyLocal adverse events1021592
      PDSystemic adverse events6201
      HealthySystemic adverse events281611
      PDSystemic adverse events7202
      HealthySystemic adverse events481592
      Speer et al.
      • Speer 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.
      PDspike IgG22411
      Healthyspike IgG17201
      PDspike IgG39412
      Healthyspike IgG20202
      Hemodialysisspike IgG441241
      Hemodialysisspike IgG1091242
      Tylicki et al.
      • Tylicki 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.
      PDspike IgG18211
      Hemodialysisspike IgG20351
      PDspike IgG21212
      Hemodialysisspike IgG34352
      Wang et al.
      • Wang 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.
      PDspike IgG801161
      Healthyspike IgG33341
      PDspike IgG1081162
      Healthyspike IgG34342
      Hemodialysisspike IgG1472041
      Hemodialysisspike IgG1922042
      Yanay et al.
      • Yanay 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.
      PDspike IgG30332
      Healthyspike IgG1321322
      Fig 1
      Fig. 1Positive rates of anti-SARS-CoV-2 spike protein IgG following COVID-19 vaccination in patients with PD and healthy control subtyped for dose of vaccine.
      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.
      Fig 2
      Fig. 2Positive rates of anti-SARS-CoV-2 spike protein IgG following COVID-19 vaccination in patients with PD and hemodialysis subtyped for dose of 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.
      Fig 3
      Fig. 3Local adverse events and systemic adverse events following COVID-19 vaccination in patients with PD.
      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.

      Declaration of Competing Interest

      All authors report that they have no potential conflicts of interest.

      Funding

      This work was supported by National Natural Science Foundation of China (No. 81860248; No. 81960224); and Science and Technology Fund of Guizhou Health Commission (No. gzwjkj2020–2–005, No. gzwkj2021–024); Cultivation project of National Natural Science Foundation of China (No. 19NSP051); the cultivate project 2021 for National Natural Science Foundation of China, Affiliated Hospital of Guizhou Medical University (No. gyfynsfc-2021–14); and the Guiyang Sci-Tech Plan Projects (No. [2022]−4–14–4).

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