Cellular and humoral immune responses to COVID-19 booster vaccination in Japanese dialysis patients

doi:10.1007/s10157-024-02477-8

. 2024 Jul;28(7):674-682.

doi: 10.1007/s10157-024-02477-8. Epub 2024 Mar 8.

Cellular and humoral immune responses to COVID-19 booster vaccination in Japanese dialysis patients

Ayumi Yoshifuji^#^{1

2}, Masataro Toda^#³, Emi Oyama³, Tetsuo Nakayama⁴, Setsuko Mise-Omata⁵, Kan Kikuchi⁶, Mamoru Yoshizawa⁷, Naohiko Kato⁸, Haruki Wakai⁹, Kiyoto Koibuchi¹⁰, Kohkichi Morimoto¹¹, Yoshifumi Uwamino^{12

13}, Ho Namkoong¹², Ayako Shibata¹³, Kaoru Wakabayashi¹⁴, Motoko Fujino¹⁵, Motoaki Komatsu³, Naoki Mochizuki¹⁶, Norihiko Kondo¹⁷, Akihiko Yoshimura⁵, Naoki Hasegawa¹², Munekazu Ryuzaki¹⁸

Affiliations

¹ Department of Nephrology, Tokyo Saiseikai Central Hospital, 1-4-17 Mita, Minato-Ku, Tokyo, 108-0073, Japan. ayutsuranaide@keio.jp.
² Department of Infectious Diseases, Keio University School of Medicine, Tokyo, Japan. ayutsuranaide@keio.jp.
³ Department of Nephrology, Tokyo Saiseikai Central Hospital, 1-4-17 Mita, Minato-Ku, Tokyo, 108-0073, Japan.
⁴ Laboratory of Viral Infection, Kitasato Institute for Life Sciences, Kitasato University, Tokyo, Japan.
⁵ Department of Microbiology and Immunology, Keio University School of Medicine, Tokyo, Japan.
⁶ Division of Nephrology, Shimoochiai Clinic, Tokyo, Japan.
⁷ Division of Nephrology, Yoshizawa Clinic, Saitama, Japan.
⁸ Division of Nephrology, Shinagawa-Jin Clinic, Tokyo, Japan.
⁹ Division of Nephrology, Shinagawa Garden Clinic, Tokyo, Japan.
¹⁰ Department of Nephrology and Dialysis, Saiseikai Yokohamashi Tobu Hospital, Kanagawa, Japan.
¹¹ Apheresis and Dialysis Center, Keio University School of Medicine, Tokyo, Japan.
¹² Department of Infectious Diseases, Keio University School of Medicine, Tokyo, Japan.
¹³ Department of Laboratory Medicine, Keio University School of Medicine, Tokyo, Japan.
¹⁴ Clinical Research Center, Tokyo Saiseikai Central Hospital, Tokyo, Japan.
¹⁵ Department of Pediatrics, Tokyo Saiseikai Central Hospital, Tokyo, Japan.
¹⁶ Department of Nursing, Tokyo Saiseikai Central Hospital, Tokyo, Japan.
¹⁷ Konan-No-Sato, Tokyo, Japan.
¹⁸ Department of Nephrology, Tokyo Saiseikai Central Hospital, 1-4-17 Mita, Minato-Ku, Tokyo, 108-0073, Japan. ryuzaki-m@saichu.jp.

^# Contributed equally.

PMID: 38457030
DOI: 10.1007/s10157-024-02477-8

Cellular and humoral immune responses to COVID-19 booster vaccination in Japanese dialysis patients

Ayumi Yoshifuji et al. Clin Exp Nephrol. 2024 Jul.

. 2024 Jul;28(7):674-682.

doi: 10.1007/s10157-024-02477-8. Epub 2024 Mar 8.

Authors

Affiliations

¹ Department of Nephrology, Tokyo Saiseikai Central Hospital, 1-4-17 Mita, Minato-Ku, Tokyo, 108-0073, Japan. ayutsuranaide@keio.jp.
² Department of Infectious Diseases, Keio University School of Medicine, Tokyo, Japan. ayutsuranaide@keio.jp.
³ Department of Nephrology, Tokyo Saiseikai Central Hospital, 1-4-17 Mita, Minato-Ku, Tokyo, 108-0073, Japan.
⁴ Laboratory of Viral Infection, Kitasato Institute for Life Sciences, Kitasato University, Tokyo, Japan.
⁵ Department of Microbiology and Immunology, Keio University School of Medicine, Tokyo, Japan.
⁶ Division of Nephrology, Shimoochiai Clinic, Tokyo, Japan.
⁷ Division of Nephrology, Yoshizawa Clinic, Saitama, Japan.
⁸ Division of Nephrology, Shinagawa-Jin Clinic, Tokyo, Japan.
⁹ Division of Nephrology, Shinagawa Garden Clinic, Tokyo, Japan.
¹⁰ Department of Nephrology and Dialysis, Saiseikai Yokohamashi Tobu Hospital, Kanagawa, Japan.
¹¹ Apheresis and Dialysis Center, Keio University School of Medicine, Tokyo, Japan.
¹² Department of Infectious Diseases, Keio University School of Medicine, Tokyo, Japan.
¹³ Department of Laboratory Medicine, Keio University School of Medicine, Tokyo, Japan.
¹⁴ Clinical Research Center, Tokyo Saiseikai Central Hospital, Tokyo, Japan.
¹⁵ Department of Pediatrics, Tokyo Saiseikai Central Hospital, Tokyo, Japan.
¹⁶ Department of Nursing, Tokyo Saiseikai Central Hospital, Tokyo, Japan.
¹⁷ Konan-No-Sato, Tokyo, Japan.
¹⁸ Department of Nephrology, Tokyo Saiseikai Central Hospital, 1-4-17 Mita, Minato-Ku, Tokyo, 108-0073, Japan. ryuzaki-m@saichu.jp.

^# Contributed equally.

PMID: 38457030
DOI: 10.1007/s10157-024-02477-8

Abstract

Background: Dialysis patients are susceptible to developing severe coronavirus disease 2019 (COVID-19) due to hypoimmunity. Antibody titers against severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) after the primary vaccinations are lower in hemodialysis (HD) patients than in healthy individuals. This study aimed to evaluate the effect of a SARS-CoV-2 booster vaccination in HD and peritoneal dialysis (PD) patients based on antibody titers and cellular and humoral immunity.

Methods: Participants of the control, HD, and PD groups were recruited from 12 facilities. SARS-CoV-2 antigen-specific cytokine and IgG-antibody levels were measured. Regulatory T cells and memory B cells were counted using flow cytometry at 6 months after primary vaccination with BNT162b2 and 3 weeks after the booster vaccination in HD and PD patients and compared with those of a control group.

Results: Booster vaccination significantly enhanced the levels of antibodies, cytokines, and memory B cells in three groups. The HD group showed significantly higher levels of IgG-antibodies, IL-1β, IL-2, IL-4, IL-17, and memory B cells than those in the control group at 3 weeks after the booster dose. The PD group tended to show similar trends to HD patients but had similar levels of IgG-antibodies, cytokines, and memory B cells to the control group.

Conclusions: HD patients had significantly stronger cellular and humoral immune responses than the control 3 weeks after the booster dose. Our findings will help in developing better COVID-19 vaccination strategies for HD and PD patients.

Keywords: BNT162b2 vaccine; Booster vaccine; COVID-19; Hemodialysis; Hypoimmunity; Peritoneal dialysis.

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Cited by

The Humoral Immune Response Against COVID-19 Through Vaccination in Hemodialysis Patients.
Park JY, Choi SH, Lim YK, Shin J, Kwon S, Kim H, Chung JW. Park JY, et al. Vaccines (Basel). 2025 Feb 10;13(2):170. doi: 10.3390/vaccines13020170. Vaccines (Basel). 2025. PMID: 40006717 Free PMC article.

References

1. Ewer KJ, Barrett JR, Belij-Rammerstorfer S, Sharpe H, Makinson R, Morter R, et al. T cell and antibody responses induced by a single dose of ChAdOx1 nCoV-19 (AZD1222) vaccine in a phase 1/2 clinical trial. Nat Med. 2021;27(2):270–8. https://doi.org/10.1038/s41591-020-01194-5 . - DOI - PubMed
1. Espi M, Charmetant X, Barba T, Koppe L, Pelletier C, Kalbacher E, 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):928–36. https://doi.org/10.1016/j.kint.2021.07.005 . - DOI - PubMed - PMC
1. Tartof SY, Slezak JM, Fischer H, Hong V, Ackerson BK, Ranasinghe ON, et al. Effectiveness of mRNA BNT162b2 COVID-19 vaccine up to 6 months in a large integrated health system in the USA: a retrospective cohort study. Lancet. 2021;398(10309):1407–16. https://doi.org/10.1016/s0140-6736(21)02183-8 . - DOI - PubMed - PMC
1. Yoshifuji A, Toda M, Ryuzaki M, Kikuchi K, Kawai T, Sakai K, et al. Investigation for the efficacy of COVID-19 vaccine in Japanese CKD patients treated with hemodialysis. Ren Replace Ther. 2022;8(1):39. https://doi.org/10.1186/s41100-022-00427-2 . - DOI - PubMed - PMC
1. Bergwerk M, Gonen T, Lustig Y, Amit S, Lipsitch M, Cohen C, et al. Covid-19 breakthrough infections in vaccinated health care workers. N Engl J Med. 2021. https://doi.org/10.1056/NEJMoa2109072 . - DOI - PubMed - PMC

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[1] Ewer KJ, Barrett JR, Belij-Rammerstorfer S, Sharpe H, Makinson R, Morter R, et al. T cell and antibody responses induced by a single dose of ChAdOx1 nCoV-19 (AZD1222) vaccine in a phase 1/2 clinical trial. Nat Med. 2021;27(2):270–8. https://doi.org/10.1038/s41591-020-01194-5 . - DOI - PubMed

[2] Ewer KJ, Barrett JR, Belij-Rammerstorfer S, Sharpe H, Makinson R, Morter R, et al. T cell and antibody responses induced by a single dose of ChAdOx1 nCoV-19 (AZD1222) vaccine in a phase 1/2 clinical trial. Nat Med. 2021;27(2):270–8. https://doi.org/10.1038/s41591-020-01194-5 . - DOI - PubMed

[3] Espi M, Charmetant X, Barba T, Koppe L, Pelletier C, Kalbacher E, 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):928–36. https://doi.org/10.1016/j.kint.2021.07.005 . - DOI - PubMed - PMC

[4] Espi M, Charmetant X, Barba T, Koppe L, Pelletier C, Kalbacher E, 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):928–36. https://doi.org/10.1016/j.kint.2021.07.005 . - DOI - PubMed - PMC

[5] Tartof SY, Slezak JM, Fischer H, Hong V, Ackerson BK, Ranasinghe ON, et al. Effectiveness of mRNA BNT162b2 COVID-19 vaccine up to 6 months in a large integrated health system in the USA: a retrospective cohort study. Lancet. 2021;398(10309):1407–16. https://doi.org/10.1016/s0140-6736(21)02183-8 . - DOI - PubMed - PMC

[6] Tartof SY, Slezak JM, Fischer H, Hong V, Ackerson BK, Ranasinghe ON, et al. Effectiveness of mRNA BNT162b2 COVID-19 vaccine up to 6 months in a large integrated health system in the USA: a retrospective cohort study. Lancet. 2021;398(10309):1407–16. https://doi.org/10.1016/s0140-6736(21)02183-8 . - DOI - PubMed - PMC

[7] Yoshifuji A, Toda M, Ryuzaki M, Kikuchi K, Kawai T, Sakai K, et al. Investigation for the efficacy of COVID-19 vaccine in Japanese CKD patients treated with hemodialysis. Ren Replace Ther. 2022;8(1):39. https://doi.org/10.1186/s41100-022-00427-2 . - DOI - PubMed - PMC

[8] Yoshifuji A, Toda M, Ryuzaki M, Kikuchi K, Kawai T, Sakai K, et al. Investigation for the efficacy of COVID-19 vaccine in Japanese CKD patients treated with hemodialysis. Ren Replace Ther. 2022;8(1):39. https://doi.org/10.1186/s41100-022-00427-2 . - DOI - PubMed - PMC

[9] Bergwerk M, Gonen T, Lustig Y, Amit S, Lipsitch M, Cohen C, et al. Covid-19 breakthrough infections in vaccinated health care workers. N Engl J Med. 2021. https://doi.org/10.1056/NEJMoa2109072 . - DOI - PubMed - PMC

[10] Bergwerk M, Gonen T, Lustig Y, Amit S, Lipsitch M, Cohen C, et al. Covid-19 breakthrough infections in vaccinated health care workers. N Engl J Med. 2021. https://doi.org/10.1056/NEJMoa2109072 . - DOI - PubMed - PMC

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Cellular and humoral immune responses to COVID-19 booster vaccination in Japanese dialysis patients

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Cellular and humoral immune responses to COVID-19 booster vaccination in Japanese dialysis patients

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