Clinical and Experimental Vaccine Research

  • 제12권1호
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  • Pages.13-24
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  • 2023
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  • 2287-3651(pISSN)
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  • 2287-366X(eISSN)
대한백신학회 (The Korean Vaccine Society)
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Seroconversion rates in kidney transplant recipients following SARS-CoV-2 vaccination and its association with immunosuppressive agents: a systematic review and meta-analysis

  • Maria Riastuti Iryaningrum (Department of Internal Medicine, School of Medicine and Health Sciences, Atma Jaya Catholic University of Indonesia) ;
  • Alius Cahyadi (Department of Internal Medicine, School of Medicine and Health Sciences, Atma Jaya Catholic University of Indonesia) ;
  • Fachreza Aryo Damara (Dr Hasan Sadikin Hospital, Faculty of Medicine, Universitas Padjadjaran) ;
  • Ria Bandiara (Department of Internal Medicine, Dr Hasan Sadikin Hospital, Faculty of Medicine, Universitas Padjadjaran) ;
  • Maruhum Bonar Hasiholan Marbun (Department of Internal Medicine, Cipto Mangunkusumo Hospital, Faculty of Medicine, Universitas Indonesia)
  • 투고 : 2022.04.20
  • 심사 : 2022.12.27
  • 발행 : 2023.01.31
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초록

This systematic and meta-analysis aims to evaluate humoral and cellular responses to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine among kidney transplant recipients (KTRs). We conducted a systematic literature search across databases to evaluate seroconversion and cellular response rates in KTRs receiving SARS-CoV-2 vaccines. We extracted studies that assessed seroconversion rates described as the presence of antibody de novo positivity in KTRs following SARS-CoV-2 vaccination published up to January 23rd, 2022. We also performed meta-regression based on immunosuppression therapy used. A total of 44 studies involving 5,892 KTRs were included in this meta-analysis. The overall seroconversion rate following complete dose of vaccines was 39.2% (95% confidence interval [CI], 33.3%-45.3%) and cellular response rate was 41.6% (95% CI, 30.0%-53.6%). Meta-regression revealed that low antibody response rate was significantly associated with the high prevalence of mycophenolate mofetil/mycophenolic acid (p=0.04), belatacept (p=0.02), and antiCD25 induction therapy uses (p=0.04). Conversely, tacrolimus use was associated with higher antibody response (p=0.01). This meta-analysis suggests that postvaccination seroconversion and cellular response rates in KTRs are still low. And seroconversion rate was correlated with the type of immunosuppressive agent and induction therapy used. Additional doses of the SARS-CoV-2 vaccine for this population using a different type of vaccine are considered.

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참고문헌

  1. Udomkarnjananun S, Kerr SJ, Townamchai N, et al. Mortality risk factors of COVID-19 infection in kidney transplantation recipients: a systematic review and meta-analysis of cohorts and clinical registries. Sci Rep 2021;11:20073.
  2. Kremer D, Pieters TT, Verhaar MC, et al. A systematic review and meta-analysis of COVID-19 in kidney transplant recipients: lessons to be learned. Am J Transplant 2021;21:3936-45. https://doi.org/10.1111/ajt.16742
  3. Soetedjo NN, Iryaningrum MR, Damara FA, et al. Prognostic properties of hypoalbuminemia in COVID-19 patients: a systematic review and diagnostic meta-analysis. Clin Nutr ESPEN 2021;45:120-6. https://doi.org/10.1016/j.clnesp.2021.07.003
  4. Permana H, Soeriadi EA, Damara FA, Mulyani Soetedjo NN. The prognostic values of thyroid disorders in predicting COVID-19 composite poor outcomes: a systematic review and meta-analysis. Diabetes Metab Syndr 2022;16:102464.
  5. Polack FP, Thomas SJ, Kitchin N, et al. Safety and efficacy of the BNT162b2 mRNA COVID-19 vaccine. N Engl J Med 2020;383:2603-15. https://doi.org/10.1056/NEJMoa2034577
  6. Tenforde MW, Self WH, Adams K, et al. Association between mRNA vaccination and COVID-19 hospitalization and disease severity. JAMA 2021;326:2043-54. https://doi.org/10.1001/jama.2021.19499
  7. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71.
  8. Tierney JF, Fisher DJ, Vale CL, et al. A framework for prospective, adaptive meta-analysis (FAME) of aggregate data from randomised trials. PLoS Med 2021;18:e1003629.
  9. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010;25:603-5. https://doi.org/10.1007/s10654-010-9491-z
  10. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-58. https://doi.org/10.1002/sim.1186
  11. Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol 2008;61:991-6. https://doi.org/10.1016/j.jclinepi.2007.11.010
  12. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629-34. https://doi.org/10.1136/bmj.315.7109.629
  13. Azzi Y, Raees H, Wang T, et al. Risk factors associated with poor response to COVID-19 vaccination in kidney transplant recipients. Kidney Int 2021;100:1127-8. https://doi.org/10.1016/j.kint.2021.08.019
  14. 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 2022;35:153-64. https://doi.org/10.1007/s40620-021-01210-y
  15. Benning L, Morath C, Bartenschlager M, et al. Neutralization of SARS-CoV-2 variants of concern in kidney transplant recipients after standard COVID-19 vaccination. Clin J Am Soc Nephrol 2022;17:98-106. https://doi.org/10.2215/CJN.11820921
  16. Benotmane I, Gautier-Vargas G, Gallais F, et al. Strong antibody response after a first dose of a SARS-CoV-2 mRNA-based vaccine in kidney transplant recipients with a previous history of COVID-19. Am J Transplant 2021;21:3808-10. https://doi.org/10.1111/ajt.16764
  17. 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 2021;14:2127-8. https://doi.org/10.1093/ckj/sfab100
  18. Bruminhent J, Setthaudom C, Chaumdee P, et al. SARSCoV-2-specific humoral and cell-mediated immune responses after immunization with inactivated COVID-19 vaccine in kidney transplant recipients (CVIM 1 study). Am J Transplant 2022;22:813-22. https://doi.org/10.1111/ajt.16867
  19. Buchwinkler L, Solagna CA, Messner J, et al. Antibody response to mRNA vaccines against SARS-CoV-2 with chronic kidney disease, hemodialysis, and after kidney transplantation. J Clin Med 2021;11:148.
  20. Chavarot N, Morel A, Leruez-Ville M, et al. Weak antibody response to three doses of mRNA vaccine in kidney transplant recipients treated with belatacept. Am J Transplant 2021;21:4043-51. https://doi.org/10.1111/ajt.16814
  21. Cucchiari D, Egri N, Bodro M, et al. Cellular and humoral response after MRNA-1273 SARS-CoV-2 vaccine in kidney transplant recipients. Am J Transplant 2021;21:2727-39. https://doi.org/10.1111/ajt.16701
  22. Correia AL, Leal R, Pimenta AC, et al. The type of SARSCoV-2 vaccine influences serological response in kidney transplant recipients. Clin Transplant 2022;36:e14585.
  23. Crane C, Phebus E, Ingulli E. Immunologic response of mRNA SARS-CoV-2 vaccination in adolescent kidney transplant recipients. Pediatr Nephrol 2022;37:449-53. https://doi.org/10.1007/s00467-021-05256-9
  24. Crespo M, Barrilado-Jackson A, Padilla E, 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;22:786-800. https://doi.org/10.1111/ajt.16854
  25. 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;32:2153-8. https://doi.org/10.1681/ASN.2021040490
  26. Debska-Slizien A, Slizien Z, Muchlado M, et al. Predictors of humoral response to mRNA COVID19 vaccines in kidney transplant recipients: a longitudinal study: the COViNEPH project. Vaccines (Basel) 2021;9:1165.
  27. Devresse A, Saad Albichr I, Georgery H, et al. T-cell and antibody response after 2 doses of the BNT162b2 vaccine in a belgian cohort of kidney transplant recipients. Transplantation 2021;105:e142-3. https://doi.org/10.1097/TP.0000000000003892
  28. Ducloux D, Colladant M, Chabannes M, Bamoulid J, Courivaud C. Factors associated with humoral response after BNT162b2 mRNA COVID-19 vaccination in kidney transplant patients. Clin Kidney J 2021;14:2270-2. https://doi.org/10.1093/ckj/sfab125
  29. Duni A, Markopoulos GS, Mallioras I, et al. The humoral immune response to BNT162b2 vaccine is associated with circulating CD19+ B lymphocytes and the naive CD45RA to memory CD45RO CD4+ T helper cells ratio in hemodialysis patients and kidney transplant recipients. Front Immunol 2021;12:760249.
  30. Eren Sadioglu R, Demir E, Evren E, et al. Antibody response to two doses of inactivated SARS-CoV-2 vaccine (CoronaVac) in kidney transplant recipients. Transpl Infect Dis 2021;23:e13740.
  31. Erol C, Yanik Yalcin T, Sari N, et al. Differences in antibody responses between an inactivated SARS-CoV-2 vaccine and the BNT162b2 mRNA vaccine in solid-organ transplant recipients. Exp Clin Transplant 2021;19:1334-40. https://doi.org/10.6002/ect.2021.0402
  32. Georgery H, Devresse A, Yombi JC, et al. Very low immunization rate in kidney transplant recipients after one dose of the BNT162b2 vaccine: beware not to lower the guard! Transplantation 2021;105:e148-9. https://doi.org/10.1097/TP.0000000000003818
  33. 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 Transplant 2021;35:e14478.
  34. Haskin O, Ashkenazi-Hoffnung L, Ziv N, et al. Serological response to the BNT162b2 COVID-19 mRNA vaccine in adolescent and young adult kidney transplant recipients. Transplantation 2021;105:e226-33. https://doi.org/10.1097/TP.0000000000003922
  35. Hod T, Ben-David A, Olmer L, et al. Humoral response of renal transplant recipients to the BNT162b2 SARS-CoV-2 mRNA vaccine using both RBD IgG and neutralizing antibodies. Transplantation 2021;105:e234-43. https://doi.org/10.1097/TP.0000000000003889
  36. Husain SA, Argyropoulos CP. Boosters and optimizing SARS-CoV-2 vaccine for transplantation: no time to wait. Am J Transplant 2022;22:328-9. https://doi.org/10.1111/ajt.16788
  37. Kantauskaite M, Muller L, Kolb T, et al. Intensity of mycophenolate mofetil treatment is associated with an impaired immune response to SARS-CoV-2 vaccination in kidney transplant recipients. Am J Transplant 2022;22:634-9. https://doi.org/10.1111/ajt.16851
  38. 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;13:756.
  39. Massa F, Cremoni M, Gerard A, et al. Safety and crossvariant immunogenicity of a three-dose COVID-19 mRNA vaccine regimen in kidney transplant recipients. EBioMedicine 2021;73:103679.
  40. Marion O, Del Bello A, Abravanel F, et al. Predictive factors for humoral response after 2-dose SARS-CoV-2 vaccine in solid organ transplant patients. Transplant Direct 2021;8:e1248.
  41. Midtvedt K, Tran T, Parker K, et al. Low immunization rate in kidney transplant recipients also after dose 2 of the BNT162b2 vaccine: continue to keep your guard up! Transplantation 2021;105:e80-1. https://doi.org/10.1097/TP.0000000000003856
  42. Miele M, Busa R, Russelli G, et al. Impaired anti-SARSCoV-2 humoral and cellular immune response induced by Pfizer-BioNTech BNT162b2 mRNA vaccine in solid organ transplanted patients. Am J Transplant 2021;21:2919-21. https://doi.org/10.1111/ajt.16702
  43. Nazaruk P, Monticolo M, Jedrzejczak AM, et al. Unexpectedly high efficacy of SARS-CoV-2 BNT162b2 vaccine in liver versus kidney transplant recipients: is it related to immunosuppression only? Vaccines (Basel) 2021;9:1454.
  44. Ou MT, Boyarsky BJ, Chiang TP, et al. Immunogenicity and reactogenicity after SARS-CoV-2 mRNA vaccination in kidney transplant recipients taking belatacept. Transplantation 2021;105:2119-23. https://doi.org/10.1097/TP.0000000000003824
  45. Pedersen RM, Bang LL, Tornby DS, et al. The SARS-CoV2-neutralizing capacity of kidney transplant recipients 4 weeks after receiving a second dose of the BNT162b2 vaccine. Kidney Int 2021;100:1129-31. https://doi.org/10.1016/j.kint.2021.09.006
  46. Prendecki M, Thomson T, Clarke CL, et al. Immunological responses to SARS-CoV-2 vaccines in kidney transplant recipients. Lancet 2021;398:1482-4. https://doi.org/10.1016/S0140-6736(21)02096-1
  47. Quiroga B, Soler MJ, Ortiz A, et al. Safety and immediate humoral response of COVID-19 vaccines in chronic kidney disease patients: the SENCOVAC study. Nephrol Dial Transplant 2022;37:1868-78. https://doi.org/10.1093/ndt/gfab313
  48. Rahav G, Lustig Y, Lavee J, et al. BNT162b2 mRNA COVID-19 vaccination in immunocompromised patients: a prospective cohort study. EClinicalMedicine 2021;41:101158.
  49. Reischig T, Kacer M, Vlas T, et al. Insufficient response to mRNA SARS-CoV-2 vaccine and high incidence of severe COVID-19 in kidney transplant recipients during pandemic. Am J Transplant 2022;22:801-12. https://doi.org/10.1111/ajt.16902
  50. Rincon-Arevalo H, Choi M, Stefanski AL, et al. Impaired humoral immunity to SARS-CoV-2 BNT162b2 vaccine in kidney transplant recipients and dialysis patients. Sci Immunol 2021;6:eabj1031.
  51. 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. Clin Microbiol Infect 2021;27:1173.
  52. 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 Transplant 2022;36:e14495.
  53. 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:e150175.
  54. 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. Lancet Reg Health Eur 2021;9:100178.
  55. Vaiciuniene R, Sitkauskiene B, Bumblyte IA, et al. Immune response after SARS-CoV-2 vaccination in kidney transplant patients. Medicina (Kaunas) 2021;57:1327.
  56. 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;22:1275-6. https://doi.org/10.1111/ajt.16829
  57. Boyarsky BJ, Werbel WA, Avery RK, et al. Antibody response to 2-dose SARS-CoV-2 mRNA vaccine series in solid organ transplant recipients. JAMA 2021;325:2204-6. https://doi.org/10.1001/jama.2021.7489
  58. Aslam S, Adler E, Mekeel K, Little SJ. Clinical effectiveness of COVID-19 vaccination in solid organ transplant recipients. Transpl Infect Dis 2021;23:e13705.
  59. Fernandez-Ruiz M, Almendro-Vazquez P, Carretero O, et al. Discordance between SARS-CoV-2-specific cell-mediated and antibody responses elicited by mRNA-1273 vaccine in kidney and liver transplant recipients. Transplant Direct 2021;7:e794.
  60. Yanis A, Haddadin Z, Spieker AJ, et al. Humoral and cellular immune responses to the SARS-CoV-2 BNT162b2 vaccine among a cohort of solid organ transplant recipients and healthy controls. Transpl Infect Dis 2022;24:e13772.
  61. Bergman P, Blennow O, Hansson L, et al. Safety and efficacy of the mRNA BNT162b2 vaccine against SARS-CoV-2 in five groups of immunocompromised patients and healthy controls in a prospective open-label clinical trial. EBioMedicine 2021;74:103705.
  62. Candon S, Guerrot D, Drouot L, et al. T cell and antibody responses to SARS-CoV-2: experience from a French transplantation and hemodialysis center during the COVID-19 pandemic. Am J Transplant 2021;21:854-63. https://doi.org/10.1111/ajt.16348
  63. Thieme CJ, Anft M, Paniskaki K, et al. The magnitude and functionality of SARS-CoV-2 reactive cellular and humoral immunity in transplant population is similar to the general population despite immunosuppression. Transplantation 2021;105:2156-64. https://doi.org/10.1097/TP.0000000000003755
  64. Boey L, Curinckx A, Roelants M, et al. Immunogenicity and safety of the 9-valent human papillomavirus vaccine in solid organ transplant recipients and adults infected with human immunodeficiency virus (HIV). Clin Infect Dis 2021;73:e661-71. https://doi.org/10.1093/cid/ciaa1897
  65. Natori Y, Shiotsuka M, Slomovic J, et al. A double-blind, randomized trial of high-dose vs standard-dose influenza vaccine in adult solid-organ transplant recipients. Clin Infect Dis 2018;66:1698-704. https://doi.org/10.1093/cid/cix1082
  66. Leibler C, Thiolat A, Henique C, et al. Control of humoral response in renal transplantation by belatacept depends on a direct effect on B cells and impaired T follicular helper-B cell crosstalk. J Am Soc Nephrol 2018;29:1049-62. https://doi.org/10.1681/ASN.2017060679
  67. Chen J, Yin H, Xu J, et al. Reversing endogenous alloreactive B cell GC responses with anti-CD154 or CTLA-4Ig. Am J Transplant 2013;13:2280-92. https://doi.org/10.1111/ajt.12350
  68. Orcurto A, Pascual M, Hoschler K, Aubert V, Meylan P, Manuel O. Impact of anti-T-cell therapy in the immunogenicity of seasonal influenza vaccine in kidney transplant recipients. Transplantation 2012;94:630-6. https://doi.org/10.1097/TP.0b013e31825f7f82
  69. Ruether DF, Schaub GM, Duengelhoef PM, et al. SARSCoV2-specific humoral and T-cell immune response after second vaccination in liver cirrhosis and transplant patients. Clin Gastroenterol Hepatol 2022;20:162-72. https://doi.org/10.1016/j.cgh.2021.09.003