1887
Volume 2023, Issue 3
  • ISSN: 0253-8253
  • EISSN: 2227-0426

Abstract

Background and Aims: As part of the COVID-19 control strategy, a growing number of vaccine portfolios evolved and got fast-tracked through regulatory agencies, with a limited examination of their efficacy and safety in vulnerable populations, such as patients with chronic conditions and immunocompromised states. Patients with chronic liver disease (CLD), and cohorts post liver transplant (LT) in particular, were underrepresented in the determinant trials of vaccine development, hence the paucity of data on their efficacy and safety in published literature. This systematic review aims to examine the available evidence and ascertain the effectiveness and safety of Covid-19 vaccination in patients with CLD and those with LT.

Methods: A systematic review of PubMed (Medline), Google Scholar, Cochrane Library, and ScienceDirect from inception until 1st March 2022 was conducted. We included observational studies and assessed vaccine efficacy regarding seroconversion or immunological rate, whereas serious or significant adverse effects have been considered safety outcomes when reported.

Results: Studies comprised 45275 patients, performed in 11 different countries. Seroconversion or immunological rate after Covid-19 vaccination was mostly the primary endpoint, whereas other endpoints like covid-19 related adverse effects were also reported. Twenty-four of the final analyzed studies are prospective cohort studies, while four are retrospective cohort studies. Twenty-one studies included patients who underwent LT and received the Covid vaccine; nine included patients who had CLD due to various etiologies. The median age range of all included patients varied from 43–69 years. All patients with LT who received at least two doses of Covid vaccine had a seroconversion rate of around 60%. Patients with CLD had a seroconversion rate of about 92% post two doses of Covid vaccination. The average seroconversion rate in post-transplant recipients was around 45% after two doses of the significant Covid vaccines: Pfizer, AstraZeneca, Moderna, and Jansen. Only two studies have reported a higher seroconversion rate of 75% and 73% after the third dose of Covid vaccine. No significant adverse effects were reported in all studies; the most commonly reported negative effect was local injection site pain.

Conclusion: The present systematic review, comprising real-world observational data studies, concludes that Covid-19 vaccination was associated with 92% and 60% seroconversion rates in patients with CLD and LT, respectively. No significant side effects were reported in all studies. This finding helps to resolve the uncertainty associated with Covid-19 vaccination in this cohort of patients.

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2023-09-23
2024-07-27
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References

  1. World Health Organization . Covid-19 clinical management: Living guidance. https://www.who.int/publications/i/item/WHO-2019-nCoV-clinical-2021-1
    [Google Scholar]
  2. Kwok HF. Review of Covid-19 vaccine clinical trials - A puzzle with missing pieces. Int J Biol Sci. 2021; 17:(6):1461–8. https://doi.org/10.7150/ijbs.59170
    [Google Scholar]
  3. Elhence A, Vaishnav M, Biswas S, Anand A, Gunjan D, Kedia, S, et al.. Predictors of in-hospital outcomes in patients with Cirrhosis and Coronavirus disease-2019. J Clin Exp Hepatol. 2022; 12:(3):P876–86. https://doi.org/10.1016/j.jceh.2021.10.014
    [Google Scholar]
  4. Yang J, Zheng Y, Gou X, Pu K, Chen Z, Guo Q, et al.. Prevalence of comorbidities and its effects in patients infected with SARS-CoV-2: A systematic review and meta-analysis. Int J Infect Dis. 2020; 94::91–5. https://doi.org/10.1016/j.ijid.2020.03.017
    [Google Scholar]
  5. Schinas G, Polyzou E, Mitropetrou F, Pazionis A, Gogos C, Triantos C, et al.. COVID-19 vaccination in patients with chronic liver disease. Viruses. 2022 Dec 13; 14:(12):2778.
    [Google Scholar]
  6. Sripongpun P, Pinpathomrat N, Bruminhent J, Kaewdech A. Coronavirus 2019 vaccinations in patients with chronic liver disease and liver transplant recipients: An update. Front Med (Lausanne). 2022 Jun 22; 9::924454.
    [Google Scholar]
  7. Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, et al.. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med. 2020; 383:(27):2603–15. https://doi.org/10.1056/NEJMoa2034577
    [Google Scholar]
  8. Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, et al..; COVE Study Group Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med. 2021; 384:(5):403–16. https://doi.org/10.1056/NEJMoa2035389
    [Google Scholar]
  9. Falsey AR, Sobieszczyk ME, Hirsch I, Sproule S, Robb ML, Corey L, et al.. Phase 3 safety and efficacy of AZD1222 (ChAdOx1 nCoV-19) Covid-19 vaccine. N Engl J Med. 2021; 385::2348–60. https://doi.org/10.1056/NEJMoa2105290
    [Google Scholar]
  10. Al Kaabi N, Zhang Y, Xia S, Yang Y, Al Qahtani MM, Abdulrazzaq N, et al.. Effect of 2 inactivated SARS-CoV-2 vaccines on symptomatic COVID-19 infection in adults: A randomized clinical trial. JAMA. 2021; 326:(1):35–45. doi:10.1001/jama.2021.8565
    [Google Scholar]
  11. Hause AM, Baggs J, Gee J, Marquez P, Myers TR, Shimabukuro, TT, et al.. Safety monitoring of an additional dose of COVID-19 vaccine-United States, August 12-September 19, 2021. MMWR Morb Mortal Wkly Rep. 2021; 70:(39):1379–84. https://doi.org/10.15585/mmwr.mm7039e4
    [Google Scholar]
  12. Furlow B. Immunocompromised patients in the USA and UK should receive a third dose of COVID-19 vaccine. Lancet Rheumatol. 2021; 3:(11):e756. https://doi.org/10.1016/S2665-9913(21)00313-1
    [Google Scholar]
  13. Fix OK, Blumberg EA, Chang K-M, Chu J, Chung RT, Goacher EK, 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. https://doi.org/10.1002/hep.31751
    [Google Scholar]
  14. Cornberg M, Buti M, Eberhardt CS, Grossi PA, Shouval D. EASL position paper on the use of COVID-19 vaccines in patients with chronic liver diseases, hepatobiliary cancer and liver transplant recipients. J Hepatol. 2021; 74:(4):944–51. https://doi.org/10.1016/j.jhep.2021.01.032
    [Google Scholar]
  15. Alqahtani SA, Barry M, Memish Z, Hashim A, Alfares MA, Alghamdi SA, et al.. Use of COVID-19 vaccines in patients with liver disease and post-liver transplantation: Position statement of the Saudi Association for the study of liver diseases and transplantation. Saudi J Gastroenterol. 2021; 27:(4): 201–7. https://doi.org/10.4103/sjg.sjg_223_21
    [Google Scholar]
  16. Kamath PS, Wiesner RH, Malinchoc M, Kremers W, Therneau TM, Kosberg CL, et al.. A model to predict survival in patients with end-stage liver disease. Hepatology. 2001; 33:(2):464–70. doi:10.1053/jhep.2001.22172.
    [Google Scholar]
  17. Leise MD, Kim WR, Kremers WK, Larson JJ, Benson JT, Therneau TM. A revised model for end-stage liver disease optimizes prediction of mortality among patients awaiting liver transplantation. Gastroenterology. 2011; 140:(7):1952–60. doi:10.1053/j.gastro.2011.02.017.
    [Google Scholar]
  18. Kodali L, Budhiraja P, Gea-Banacloche J. COVID-19 in kidney transplantation-implications for immunosuppression and vaccination. Front Med (Lausanne). 2022 Nov 23; 9::1060265. doi:10.3389/fmed.2022.1060265.
    [Google Scholar]
  19. Ejazi SA, Ghosh S, Ali N. Antibody detection assays for COVID-19 diagnosis: An early overview. Immunol Cell Biol. 2021 Jan; 99:(1):21–33. doi:10.1111/imcb.12397.
    [Google Scholar]
  20. Khoury DS, Cromer D, Reynaldi A, Schlub TE, Wheatley AK, Juno JA, et al.. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med. 2021; 27::1205–11. doi:10.1038/s41591-021-01377-8.
    [Google Scholar]
  21. Kulkarni AV, Tevethia HV, Premkumar M, Arab JP, Candia R, Kumar K, et al.. Impact of COVID-19 on liver transplant recipients-A systematic review and meta-analysis. E Clin Med. 2021; 38::101025. https://doi.org/10.1016/j.eclinm.2021.101025
    [Google Scholar]
  22. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al.. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021; 372::n71. https://doi:10.1136/bmj.n71
    [Google Scholar]
  23. Del Bello A, Abravanel F, Marion O, Couat C, Esposito L, Lavayssière L, et al.. Efficiency of a boost with a third dose of anti‐SARS‐CoV‐2 messenger RNA‐based vaccines in solid organ transplant recipients. Am J Transpl. 2022 Jan; 22:(1):322–3.
    [Google Scholar]
  24. Boyarsky BJ, Werbel WA, Avery RK, Tobian AAR, Massie AB, Segev DL, et al.. Antibody response to 2-dose SARS-CoV-2 mRNA vaccine series in solid organ transplant recipients. JAMA. 2021; 325:(21):2204–6.
    [Google Scholar]
  25. Cholankeril G, Al-Hillan A, Tarlow B, Abrams D, Jacobs JS, Flores NP, et al.. Clinical factors associated with lack of serological response to SARS‐CoV‐2 messenger RNA vaccine in liver transplantation recipients. Liver Transpl. 2022 Jan; 28:(1):123–6. doi:10.1002/lt.26351.
    [Google Scholar]
  26. Erol Ç, Yalçın TY, Sarı N, Bayraktar N, Soy EA, Çolak MY, 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:(12):1334–40.
    [Google Scholar]
  27. D’Offizi G, Agrati C, Visco-Comandini U, Castilletti C, Puro V, Piccolo P, et al.. Coordinated cellular and humoral immune responses after two-dose SARS-CoV2 mRNA vaccination in liver transplant recipients. Liver Int. 2022 Jan; 42:(1):180–6.
    [Google Scholar]
  28. Guarino M, Cossiga V, Esposito I, Furno A, Morisco F. Effectiveness of SARS-CoV-2 vaccination in liver transplanted patients: The debate is open. J Hepatol. 2022; 76:(1):237–9.
    [Google Scholar]
  29. Hall VG, Ferreira VH, Ierullo M, Ku T, Marinelli T, Majchrzak-Kita B, et al.. Humoral and cellular immune response and safety of two-dose SARS-CoV-2 mRNA-1273 vaccine in solid organ transplant recipients. Am J Transpl. 2021 Dec; 21:(12):3980–9.
    [Google Scholar]
  30. Herrera S, Colmenero J, Pascal M, Escobedo M, Castel MA, Sole-González E, et al.. Cellular and humoral immune response after mRNA-1273 SARS-CoV-2 vaccine in liver and heart transplant recipients. Am J Transpl. 2021 Dec; 21:(12):3971–9.
    [Google Scholar]
  31. Kamar N, Abravanel F, Marion O, Couat C, Izopet J, Del Bello A. Three doses of an mRNA Covid-19 vaccine in solid-organ transplant recipients. N Engl J Med. 2021 Aug 12; 385:(7):661–2.
    [Google Scholar]
  32. Marion O, Del Bello A, Abravanel F, Couat C, Faguer S, Esposito L, et al.. Safety and immunogenicity of anti–SARS-CoV-2 messenger RNA vaccines in recipients of solid organ transplants. Ann Intern Med. 2021 Sep; 174:(9):1336–8.
    [Google Scholar]
  33. Mazzola A, Todesco E, Drouin S, Hazan F, Marot S, Thabut D, et al.. Poor antibody response after two doses of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccine in transplant recipients. Clin Infect Dis. 2022 Mar 15; 74:(6):1093–6.
    [Google Scholar]
  34. Nazaruk P, Monticolo M, Jędrzejczak AM, Krata N, Moszczuk B, Sańko-Resmer J, et al.. Unexpectedly high efficacy of SARS-CoV-2 BNT162b2 vaccine in liver versus kidney transplant recipients-is it related to immunosuppression only? Vaccines. 2021 Dec 8; 9:(12):1454.
    [Google Scholar]
  35. Rabinowich L, Grupper A, Baruch R, Ben-Yehoyada M, Halperin T, Turner D, et al.. Low immunogenicity to SARS-CoV-2 vaccination among liver transplant recipients. J Hepatol. 2021 Aug 1; 75:(2):435–8.
    [Google Scholar]
  36. Rahav G, Lustig Y, Lavee J, Benjamini O, Magen H, Hod T, et al.. NT162b2 mRNA COVID-19 vaccination in immunocompromised patients: A prospective cohort study. E Clin Med. 2021 Nov 1; 41::101158. doi:10.1016/j.eclinm.2021.101158.
    [Google Scholar]
  37. Rashidi-Alavijeh J, Frey A, Passenberg M, Korth J, Zmudzinski J, Anastasiou O, et al.. Humoral response to SARS-CoV-2 vaccination in liver transplant recipients–a single-center experience. Vaccines. 2021 Jul 4; 9:(7):738.
    [Google Scholar]
  38. Strauss AT, Hallett AM, Boyarsky BJ, Ou MT, Werbel WA, Avery RK, et al.. Antibody response to severe acute respiratory syndrome-coronavirus-2 messenger RNA vaccines in liver transplant recipients. Liver Transpl. 2021 Dec; 27:(12):1852–6.
    [Google Scholar]
  39. Timmermann L, Globke B, Lurje G, Schmelzle M, Schöning W, Öllinger R, et al.. Humoral immune response following SARS-CoV-2 vaccination in liver transplant recipients. Vaccines. 2021 Dec 1; 9:(12):1422.
    [Google Scholar]
  40. Davidov Y, Tsaraf K, Cohen-Ezra O, Likhter M, Yakov GB, Levy I, et al.. Immunogenicity and adverse effects of the 2-Dose BNT162b2 messenger RNA vaccine among liver transplantation recipients. Liver Transpl. 2022 Feb; 28:(2):215–23.
    [Google Scholar]
  41. Yanis A, Haddadin Z, Spieker AJ, Waqfi D, Rankin DA, Talj R, 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 Feb; 24:(1):e13772.
    [Google Scholar]
  42. Ai J, Wang J, Liu D, Xiang H, Guo Y, Lv J, 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 Jul 1; 20:(7):1516–24.
    [Google Scholar]
  43. Bakasis A-D, Bitzogli K, Mouziouras D, Pouliakis A, Roumpoutsou M, Goules AV, et al.. Antibody responses after SARS-CoV-2 vaccination in patients with liver diseases. Viruses. 2022 Jan 21; 14:(2):207.
    [Google Scholar]
  44. Calleri A, Saracco M, Pittaluga F, Cavallo R, Romagnoli R, Martini S. Seroconversion after coronavirus disease 2019 vaccination in patients awaiting liver transplantation: Fact or fancy?. Liver Transpl. 2022 Feb; 28:(2):180–7.
    [Google Scholar]
  45. He T, Zhou Y, Xu P, Ling N, Chen M, Huang T, et al.. Safety and antibody response to inactivated COVID-19 vaccine in patients with chronic hepatitis B virus infection. Liver Int. 2022; 42:(6):1287–96.
    [Google Scholar]
  46. John BV, Deng Y, Scheinberg A, Mahmud N, Taddei TH, Kaplan D, et al.. Association of BNT162b2 mRNA and mRNA-1273 vaccines with COVID-19 infection and hospitalization among patients with cirrhosis. JAMA Intern Med. 2021 Oct 1; 181:(10):1306–14.
    [Google Scholar]
  47. Wang J, Hou Z, Liu J, Gu Y, Wu Y, Chen Z, et al.. Safety and immunogenicity of COVID-19 vaccination in patients with non-alcoholic fatty liver disease (CHESS2101): A multicenter study. J Hepatol. 2021 Aug 1; 75:(2):439–41.
    [Google Scholar]
  48. Ruether DF, Schaub GM, Duengelhoef PM, Haag F, Brehm TT, Fathi A, et al.. SARS-CoV2-specific humoral and T-cell immune response in liver cirrhosis and transplant patients after the second vaccination. Clin Gastroenterol Hepatol. 2022 Jan 1; 20:(1):162–72.
    [Google Scholar]
  49. 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 Dec 1; 75:(6):1434–9.
    [Google Scholar]
  50. Russo FP, Burra P, Zanetto A. COVI, D-19, and liver disease: Where are we now? Nat Rev Gastroenterol Hepatol. 2022 May; 19:(5):277–8.
    [Google Scholar]
  51. Thomson T, Prendecki M, Gleeson S, Martin P, Spensley K, De Aguiar RC, et al.. In kidney transplant recipients, immune responses following 3rd and 4th dose of heterologous and homologous COVID-19 vaccines. EClinicalMedicine. 2022 Nov; 53::101642.
    [Google Scholar]
  52. Sharma A, Patnaik I, Kumar A, Gupta R. COVID-19 vaccines in patients with chronic liver disease. J Clin Exp Hepatol. 2021; 11:(6):720–6.
    [Google Scholar]
  53. Dufour J-F, Marjot T, Becchetti C, Tilg H. COVID-19 and liver disease. Gut. 2022; 1–13.
    [Google Scholar]
  54. Tu Z-H, Jin P-B, Chen D-Y, Chen Z-Y, Li Z-W, Wu J, et al.. Evaluating the Response and Safety of Inactivated COVID-19 Vaccines in Liver Transplant Recipients. Infect Drug Resist. 2022 May; 15::2469–74.
    [Google Scholar]
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