1,216
Views
0
CrossRef citations to date
0
Altmetric
Coronavirus

Immunogenicity of COVID-19 vaccines in patients with cirrhosis: A meta-analysis

, &
Article: 2326316 | Received 15 Jan 2024, Accepted 29 Feb 2024, Published online: 11 Mar 2024

References

  • World Health Organization. Coronavirus (COVID-19) Dashboard. [ accessed 2023 Aug 30]. https://covid19.who.int/.
  • Middleton P, Hsu C, Lythgoe MP. Clinical outcomes in COVID-19 and cirrhosis: a systematic review and meta-analysis of observational studies. BMJ Open Gastroenterol. 2021;8(1):e000739. doi:10.1136/bmjgast-2021-000739.
  • Ge J, Pletcher MJ, Lai JC, Consortium NC. Outcomes of SARS-CoV-2 infection in patients with chronic liver disease and cirrhosis: a national COVID cohort collaborative study. Gastroenterology. 2021;161:1487–501 e5. doi:10.1053/j.gastro.2021.07.010.
  • Kovalic AJ, Satapathy SK, Thuluvath PJ. Prevalence of chronic liver disease in patients with COVID-19 and their clinical outcomes: a systematic review and meta-analysis. Hepatol Int. 2020;14(5):612–9. doi:10.1007/s12072-020-10078-2.
  • Fix OK, Blumberg EA, Chang KM, Chu J, Chung RT, Goacher EK, Hameed B, Kaul DR, Kulik LM, Kwok RM, et al. American association for the study of liver diseases expert panel consensus statement: vaccines to prevent coronavirus disease 2019 infection in patients with liver disease. Hepatology. 2021;74(2):1049–64. doi:10.1002/hep.31751.
  • Marjot T, Eberhardt CS, Boettler T, Belli LS, Berenguer M, Buti M, Jalan R, Mondelli MU, Moreau R, Shouval D, et al. Impact of COVID-19 on the liver and on the care of patients with chronic liver disease, hepatobiliary cancer, and liver transplantation: an updated EASL position paper. J Hepatol. 2022;77(4):1161–97. doi:10.1016/j.jhep.2022.07.008.
  • Harmala S, Parisinos CA, Shallcross L, O’Brien A, Hayward A. Effectiveness of influenza vaccines in adults with chronic liver disease: a systematic review and meta-analysis. BMJ Open. 2019;9(9):e031070. doi:10.1136/bmjopen-2019-031070.
  • McCashland TM, Preheim LC, Gentry MJ. Pneumococcal vaccine response in cirrhosis and liver transplantation. J Infect Dis. 2000;181(2):757–60. doi:10.1086/315245.
  • Aggeletopoulou I, Davoulou P, Konstantakis C, Thomopoulos K, Triantos C. Response to hepatitis B vaccination in patients with liver cirrhosis. Rev Med Virol. 2017;27(6):27. doi:10.1002/rmv.1942.
  • Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB, et al. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med. 2021;384(5):403–16. doi:10.1056/NEJMoa2035389.
  • Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, Perez JL, Pérez Marc G, Moreira ED, Zerbini C, et al. Safety and efficacy of the BNT162b2 mRNA COVID-19 vaccine. N Engl J Med. 2020;383(27):2603–15. doi:10.1056/NEJMoa2034577.
  • Voysey M, Clemens SAC, Madhi SA, Weckx LY, Folegatti PM, Aley PK, Angus B, Baillie VL, Barnabas SL, Bhorat QE, et al. Safety and efficacy of the ChAdOx1 nCoV-19 vaccine (AZD1222) against SARS-CoV-2: an interim analysis of four randomised controlled trials in Brazil, South Africa, and the UK. Lancet. 2021;397(10269):99–111. doi:10.1016/S0140-6736(20)32661-1.
  • Al-Dury S, Waern J, Waldenström J, Alavanja M, Saed HH, Törnell A, Arabpour M, Wiktorin HG, Einarsdottir S, Ringlander J, et al. Impaired SARS-CoV-2-specific T-cell reactivity in patients with cirrhosis following mRNA COVID-19 vaccination. JHEP Rep. 2022;4(7):100496. doi:10.1016/j.jhepr.2022.100496.
  • Willuweit K, Frey A, Passenberg M, Korth J, Saka N, Anastasiou OE, Möhlendick B, Schütte A, Schmidt H, Rashidi-Alavijeh J, et al. Patients with liver cirrhosis show high immunogenicity upon COVID-19 vaccination but develop premature deterioration of antibody titers. Vaccines (Basel). 2022;10(3):10. doi:10.3390/vaccines10030377.
  • Ai J, Wang J, Liu D, Xiang H, Guo Y, Lv J, Zhang Q, Li J, Zhang X, Li Q, et al. Safety and immunogenicity of SARS-CoV-2 vaccines in patients with chronic liver diseases (CHESS-NMCID 2101): a multicenter study. Clin Gastroenterol Hepatol. 2022;20:1516–24 e2. doi:10.1016/j.cgh.2021.12.022.
  • Biliotti E, Caioli A, Sorace C, Lionetti R, Milozzi E, Taibi C, Visco Comandini U, Maggi F, Puro V, D’Offizi G, et al. Humoral immune response after COVID-19 mRNA vaccination in patients with liver cirrhosis: a prospective real-life single center study. Biomedicines. 2023;11(5):11. doi:10.3390/biomedicines11051320.
  • Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev. 2021;10(1):89. doi:10.1186/s13643-021-01626-4.
  • Balduzzi S, Rucker G, Schwarzer G. How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health. 2019;22(4):153–60. doi:10.1136/ebmental-2019-300117.
  • Bakasis A-D, Bitzogli K, Mouziouras D, Pouliakis A, Roumpoutsou M, Goules AV, Androutsakos T. Antibody responses after SARS-CoV-2 vaccination in patients with liver diseases. Viruses-Basel. 2022;14:14. doi:10.3390/v14020207.
  • Song R, Yang C, Wang J, Li Q, Chen J, Sun K, Lv H, Yang Y, Liang J, Ye Q, et al. Immune response of primary and booster immunity of SARS-CoV-2 vaccination among patients with chronic liver disease. medRxiv. 2022;14.
  • Goel A, Verma A, Tiwari P, Katiyar H, Aggarwal A, Khetan DM, Kishore RVK, Kumar P, Singh TP, Sheikh S, et al. Serological immune response following ChAdOx1 nCoV-19 vaccine (Covishield®) in patients with liver cirrhosis. Nato Adv Sci Inst Se. 2022;10:10. doi:10.3390/vaccines10111837.
  • Chen Z, Zhang Y, Song R, Wang L, Hu X, Li H, Cai D, Hu P, Shi X, Ren H. Waning humoral immune responses to inactivated SARS-CoV-2 vaccines in patients with severe liver disease. Sig Transduct Target Ther. 2022;7(1). doi:10.1038/s41392-022-01032-9.
  • Wang J, Zhang Q, Ai J, Liu D, Liu C, Xiang H, Gu Y, Guo Y, Lv J, Huang Y, et al. Safety and immunogenicity of SARS-CoV-2 vaccines in Chinese patients with cirrhosis: a prospective multicenter study. Hepatol Int. 2022;16:691–701. doi:10.1007/s12072-022-10332-9.
  • Thuluvath PJ, Robarts P, Chauhan M. Analysis of antibody responses after COVID-19 vaccination in liver transplant recipients and those with chronic liver diseases. J Hepatol. 2021;75(6):1434–9. doi:10.1016/j.jhep.2021.08.008.
  • Singh A, De A, Singh MP, Rathi S, Verma N, Premkumar M, Taneja S, Duseja A, Singh V. Antibody response and safety of ChAdOx1-nCOV (covishield) in patients with cirrhosis: a cross-sectional, observational study. Dig Dis Sci. 2023;68:676–84. doi:10.1007/s10620-022-07641-2.
  • Giambra V, Piazzolla AV, Cocomazzi G, Squillante MM, De Santis E, Totti B, Cavorsi C, Giuliani F, Serra N, Mangia A, et al. Effectiveness of booster dose of anti SARS-CoV-2 BNT162b2 in cirrhosis: longitudinal evaluation of humoral and cellular response. Vaccines (Basel). 2022;10(8):10. doi:10.3390/vaccines10081281.
  • Kulkarni AV, Jaggaiahgari S, Iyengar S, Simhadri V, Gujjarlapudi D, Rugwani H, Vemula VK, Gora BA, Shaik S, Sharma M, et al. Poor immune response to coronavirus disease vaccines in decompensated cirrhosis patients and liver transplant recipients. Vaccine. 2022;40(48):6971–8. doi:10.1016/j.vaccine.2022.10.042.
  • Cossiga V, Capasso M, Guarino M, Loperto I, Brusa S, Cutolo FM, Attanasio MR, Lieto R, Portella G, Morisco F. Safety and immunogenicity of anti-SARS-CoV-2 booster dose in patients with chronic liver disease. J Clin Med. 2023;12(6):2281. doi:10.3390/jcm12062281.
  • Ruether DF, Schaub GM, Duengelhoef PM, Haag F, Brehm TT, Fathi A, Wehmeyer M, Jahnke-Triankowski J, Mayer L, Hoffmann A, et al. SARS-CoV2-specific humoral and T-cell immune response after second vaccination in liver cirrhosis and transplant patients. Clin Gastroenterol Hepatol. 2022;20:162–72.e9. doi:10.1016/j.cgh.2021.09.003.
  • Iavarone M, Tosetti G, Facchetti F, Topa M, Er JM, Hang SK, Licari D, Lombardi A, D’Ambrosio R, Degasperi E, et al. Spike-specific humoral and cellular immune responses after COVID-19 mRNA vaccination in patients with cirrhosis: a prospective single center study. Dig Liver Dis. 2023;55(2):160–8. doi:10.1016/j.dld.2022.09.010.
  • Cheung KS, Mok CH, Mao X, Zhang R, Hung IF, Seto WK, Yuen MF. COVID-19 vaccine immunogenicity among chronic liver disease patients and liver transplant recipients: a meta-analysis. Clin Mol Hepatol. 2022;28:890–911. doi:10.3350/cmh.2022.0087.
  • Luo D, Chen X, Du J, Mei B, Wang A, Kuang F, Fang C, Gan Y, Peng F, Yang X, et al. Immunogenicity of COVID-19 vaccines in chronic liver disease patients and liver transplant recipients: a systematic review and meta-analysis. Liver Int. 2023;43(1):34–48. doi:10.1111/liv.15403.
  • Khoury DS, Cromer D, Reynaldi A, Schlub TE, Wheatley AK, Juno JA, Subbarao K, Kent SJ, Triccas JA, Davenport MP, et al. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med. 2021;27(7):1205–11. doi:10.1038/s41591-021-01377-8.
  • Marjot T, Webb GJ, Barritt AS, Gines P, Lohse AW, Moon AM, Pose, E, Trivedi, P, Barnes, E, et al. SARS-CoV-2 vaccination in patients with liver disease: responding to the next big question. Lancet Gastroenterol Hepatol. 2021;6:156–8. doi:10.1016/S2468-1253(21)00008-X.
  • Simao AL, Palma CS, Izquierdo-Sanchez L, Putignano A, Carvalho-Gomes A, Posch A, Zanaga P, Girleanu I, Henrique MM, Araújo C, et al. Cirrhosis is associated with lower serological responses to COVID-19 vaccines in patients with chronic liver disease. JHEP Rep. 2023;5(5):100697. doi:10.1016/j.jhepr.2023.100697.
  • Ahmed SF, Quadeer AA, McKay MR. SARS-CoV-2 T cell responses elicited by COVID-19 vaccines or infection are expected to remain robust against Omicron. Viruses. 2022;14(1):14. doi:10.3390/v14010079.
  • Le Bert N, Tan AT, Kunasegaran K, Tham CYL, Hafezi M, Chia A, Chng MHY, Lin M, Tan N, Linster M, et al. SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature. 2020;584(7821):457–62. doi:10.1038/s41586-020-2550-z.
  • Pearce FA, Lim SH, Bythell M, Lanyon P, Hogg R, Taylor A, Powter G, Cooke GS, Ward H, Chilcot J, et al. Antibody prevalence after three or more COVID-19 vaccine doses in individuals who are immunosuppressed in the UK: a cross-sectional study from MELODY. Lancet Rheumatol. 2023;5:461–73. doi:10.1016/S2665-9913(23)00160-1.
  • Romano C, Esposito S, Donnarumma G, Marrone A. Detection of neutralizing anti-severe acute respiratory syndrome coronavirus 2 antibodies in patients with common variable immunodeficiency after immunization with messenger RNA vaccines. Ann Allergy Asthma Immunol. 2021;127:499–501. doi:10.1016/j.anai.2021.07.026.
  • Zhu Q, Wang L, Hu X, Zhang Y, Huang T, He T, Chen Z, Zhang G, Peng M, Chen M, et al. Dynamic humoral immune response to primary and booster inactivated SARS-CoV-2 vaccination in patients with cirrhosis. J Clin Transl Hepatol. 2023;11(7):1476–84. doi:10.14218/JCTH.2023.00108.
  • Sripongpun P, Pinpathomrat N, Sophonmanee R, Ongarj J, Seepathomnarong P, Seeyankem B, Chamroonkul N, Piratvisuth T, Kaewdech A. Heterologous COVID-19 vaccination and booster with mRNA vaccine provide enhanced immune response in patients with cirrhosis: a prospective observational study. Vaccines (Basel). 2023;11:11. doi:10.3390/vaccines11091455.
  • John BV, Deng Y, Schwartz KB, Taddei TH, Kaplan DE, Martin P, Chao H-H, Dahman B. Postvaccination COVID-19 infection is associated with reduced mortality in patients with cirrhosis. Hepatology. 2022;76:126–38. doi:10.1002/hep.32337.
  • Diaz LA, Fuentes-Lopez E, Lazo M, Kamath PS, Arrese M, Arab JP. Vaccination against COVID-19 decreases hospitalizations in patients with cirrhosis: results from a nationwide analysis. Liver Int. 2022;42(4):942–4. doi:10.1111/liv.15193.
  • Stroffolini T, Ciancio A, Federico A, Benigno RG, Colloredo G, Lombardi A, Niro GA, Verucchi G, Ferrigno L, Gioli F, et al. COVID-19 vaccination among cirrhotics in Italy: high coverage and effectiveness of 3 doses versus 2 in preventing breakthrough infection and hospitalization. Dig Liver Dis. 2023;55(3):316–21. doi:10.1016/j.dld.2022.11.016.
  • John BV, Ferreira RD, Doshi A, Kaplan DE, Taddei TH, Spector SA, Paulus E, Deng Y, Bastaich D, Dahman B, et al. Third dose of COVID-19 mRNA vaccine appears to overcome vaccine hyporesponsiveness in patients with cirrhosis. J Hepatol. 2022;77(5):1349–58. doi:10.1016/j.jhep.2022.07.036.
  • Murray SM, Pose E, Wittner M, Londono MC, Schaub G, Cook J, Dimitriadis S, Meacham G, Irwin S, Lim Z, et al. Immune responses and clinical outcomes after COVID-19 vaccination in patients with liver disease and liver transplant recipients. J Hepatol. 2024;80(1):109–23. doi:10.1016/j.jhep.2023.10.009.
  • John BV, Bastaich DR, Ferreira RD, Doshi A, Taddei TH, Kaplan DE, Spector S, Deng Y, Dahman B. Covid-1 vaccine effectiveness and community prevalence of alpha, delta and omicron variants in patients with cirrhosis. Hepatology. 2022;76(9):573–4. doi:10.1136/gutjnl-2022-327799.
  • Gaborit B, Fernandes S, Loubet P, Ninove L, Dutour A, Cariou B, Coupaye M, Clement K, Czernichow S, Carette C, et al. Early humoral response to COVID-19 vaccination in patients living with obesity and diabetes in France. The COVPOP OBEDIAB study with results from the ANRS0001S COV-POPART cohort. Metabolism. 2023;142:155412. doi:10.1016/j.metabol.2023.155412.
  • Porntharukchareon T, Chartisathian W, Navinpipat M, Samdaengpan C, Cheirsilpa K, Lueprasitsakul A, Worawichawong S, Muangsillapasart V, Pumuthaivirat P, Dechates B, et al. The immunogenicity of the ChAdOx1 nCoV-19 vaccination in participants with underlying comorbidity diseases: a prospective cohort study. Hum Vaccin Immunother. 2023;19:2251850. doi:10.1080/21645515.2023.2251850.
  • Chen JJ, Lee TH, Tian YC, Lee CC, Fan PC, Chang CH. Immunogenicity rates after SARS-CoV-2 vaccination in people with end-stage kidney disease: a systematic review and meta-analysis. JAMA Netw Open. 2021;4:e2131749. doi:10.1001/jamanetworkopen.2021.31749.
  • Li H, Wang Y, Ao L, Ke M, Chen Z, Chen M, Peng M, Ling N, Hu P, Cai D, et al. Association between immunosuppressants and poor antibody responses to SARS-CoV-2 vaccines in patients with autoimmune liver diseases. Front Immunol. 2022;13:988004. doi:10.3389/fimmu.2022.988004.