EASL position paper on the use of COVID-19 vaccines in patients with chronic liver diseases, hepatobiliary cancer and liver transplant recipients

Markus Cornberg, Maria Buti, Christiane S Eberhardt, Paolo Antonio Grossi, Daniel Shouval, Markus Cornberg, Maria Buti, Christiane S Eberhardt, Paolo Antonio Grossi, Daniel Shouval

Abstract

According to a recent World Health Organization estimate, the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic, which originated in China in 2019, has spread globally, infecting nearly 100 million people worldwide by January 2021. Patients with chronic liver diseases (CLD), particularly cirrhosis, hepatobiliary malignancies, candidates for liver transplantation, and immunosuppressed individuals after liver transplantation appear to be at increased risk of infections in general, which in turn translates into increased mortality. This is also the case for SARS-CoV-2 infection, where patients with cirrhosis, in particular, are at high risk of a severe COVID-19 course. Therefore, vaccination against various pathogens including SARS-CoV-2, administered as early as possible in patients with CLD, is an important protective measure. However, due to impaired immune responses in these patients, the immediate and long-term protective response through immunisation may be incomplete. The current SARS-CoV-2 pandemic has led to the exceptionally fast development of several vaccine candidates. A small number of these SARS-CoV-2 vaccine candidates have already undergone phase III, placebo-controlled, clinical trials in healthy individuals with proof of short-term safety, immunogenicity and efficacy. However, although regulatory agencies in the US and Europe have already approved some of these vaccines for clinical use, information on immunogenicity, duration of protection and long-term safety in patients with CLD, cirrhosis, hepatobiliary cancer and liver transplant recipients has yet to be generated. This review summarises the data on vaccine safety, immunogenicity, and efficacy in this patient population in general and discusses the implications of this knowledge on the introduction of the new SARS-CoV-2 vaccines.

Keywords: COVID-19; Cirrhosis; Influenza; Liver transplantation; SARS-CoV-2; Vaccine.

Conflict of interest statement

Conflict of interest MC reports personal fees from Abbvie, personal fees from Gilead Sciences, personal fees from Merck Sharp & Dohme (MSD), personal fees from GlaxoSmithKline (GSK), personal fees from Janssen-Cilag, personal fees from Spring Bank Pharmaceuticals, personal fees from Novartis, from Swedish Orphan Biovitrum (SOBI), personal fees from Falk Foundation, grants and personal fees from Roche, outside the submitted work. PAG reports personal fees from Merck, Sharp & Dohme, personal fees from Biotest, personal fees from Angelini, personal fees from Nordic Pharma, personal fees from Vertex, personal fees from Gilead, personal fees from Astellas, outside the submitted work. MB, CSE and DS have nothing to disclose.

Copyright © 2021 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

References

    1. Angeli P., Bernardi M., Villanueva C., Francoz C., Mookerjee R.P., Trebicka J. EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis. J Hepatol. 2018;69:406–460. doi: 10.1016/j.jhep.2018.03.024.
    1. McMahon B.J., Wainwright K., Bulkow L., Parkinson A.J., Lindenbaum M., Wainwright R. Response to hepatitis B vaccine in Alaska Natives with chronic alcoholism compared with non-alcoholic control subjects. Am J Med. 1990;88:460–464. doi: 10.1016/0002-9343(90)90423-B.
    1. Shouval D. Hepatitis B vaccines. J Hepatol. 2003;39:S70–S76. doi: 10.1016/s0168-8278(03)00152-1. Elsevier.
    1. Mendenhall C., Roselle G.A., Lybecker L.A., Marshall L.E., Grossman C.J., Myre S.A. Hepatitis B vaccination - response of alcoholic with and without liver injury. Dig Dis Sci. 1988;33:263–269. doi: 10.1007/BF01535747.
    1. Wörns M.A., Teufel A., Kanzler S., Shrestha A., Victor A., Otto G. Incidence of HAV and HBV infections and vaccination rates in patients with autoimmune liver diseases. Am J Gastroenterol. 2008;103:138–146. doi: 10.1111/j.1572-0241.2007.01609.x.
    1. Shouval D., Roggendorf H., Roggendorf M. Enhanced immune response to hepatitis B vaccination through immunization with a Pre-S1/Pre-S2/S Vaccine. Med Microbiol Immunol. 2015;204:57–68. doi: 10.1007/s00430-014-0374-x.
    1. Vesikari T., Langley J., Segall N., Ward B., Cooper C., Poliquin G. Higher proportion of responders with hepatitis B antibody levels ≥100 miu/ml with the trivalent HepB vaccine, Sci-B-Vac, compared to Engerix-B: results from the phase 3 double-blind, randomized study comparing immunogenicity and safety (PROTECT) J Hepatol. 2020;73:S579. doi: 10.1016/s0168-8278(20)31633-0.
    1. Leroux-Roels G. Old and new adjuvants for hepatitis B vaccines. Med Microbiol Immunol. 2015;204:69–78. doi: 10.1007/s00430-014-0375-9.
    1. Albillos A., Lario M., Álvarez-Mon M. Cirrhosis-associated immune dysfunction: distinctive features and clinical relevance. J Hepatol. 2014;61:1385–1396. doi: 10.1016/j.jhep.2014.08.010.
    1. ESMO . 2020. COVID-19 vaccination in cancer patients: ESMO statements.
    1. Bitterman R., Eliakim-Raz N., Vinograd I., Zalmanovici Trestioreanu A., Leibovici L., Paul M. Influenza vaccines in immunosuppressed adults with cancer. Cochrane Database Syst Rev. 2018;2018 doi: 10.1002/14651858.CD008983.pub3.
    1. Läubli H., Balmelli C., Kaufmann L., Stanczak M., Syedbasha M., Vogt D. Influenza vaccination of cancer patients during PD-1 blockade induces serological protection but may raise the risk for immune-related adverse events. J Immunother Canc. 2018;6 doi: 10.1186/s40425-018-0353-7.
    1. Chong C.R., Park V.J., Cohen B., Postow M.A., Wolchok J.D., Kamboj M. Safety of inactivated influenza vaccine in cancer patients receiving immune checkpoint inhibitors. Clin Infect Dis. 2020;70:193–199. doi: 10.1093/cid/ciz202.
    1. Failing J.J., Ho T.P., Yadav S., Majithia N., Riaz !I Bin, Shin J.Y. Safety of influenza vaccine in patients with cancer receiving pembrolizumab. JCO Oncol Pract. 2020;16:e573–e580. doi: 10.1200/jop.19.00495.
    1. Sahin U., Oehm P., Derhovanessian E., Jabulowsky R.A., Vormehr M., Gold M. An RNA vaccine drives immunity in checkpoint-inhibitor-treated melanoma. Nature. 2020;585:107–112. doi: 10.1038/s41586-020-2537-9.
    1. Burris H.A., Patel M.R., Cho D.C., Clarke J.M., Gutierrez M., Zaks T.Z. A phase I multicenter study to assess the safety, tolerability, and immunogenicity of mRNA-4157 alone in patients with resected solid tumors and in combination with pembrolizumab in patients with unresectable solid tumors. J Clin Oncol. 2019;37 doi: 10.1200/jco.2019.37.15_suppl.2523. 2523–2523.
    1. Bauman J., Burris H., Clarke J., Patel M., Cho D., Gutierrez M. Safety, tolerability, and immunogenicity of mRNA-4157 in combination with pembrolizumab in subjects with unresectable solid tumors (KEYNOTE-603): an update. J Immunother Canc. 2020;8 doi: 10.1136/jitc-2020-sitc2020.0798. A846–A846.
    1. Marjot T., Webb G.J., Barritt A.S., Ginà P., Lohse A.W., Moon A.M. SARS-CoV-2 vaccination in patients with liver disease: responding to the next big question. Lancet Gastroenterol Hepatol. 2021 doi: 10.1016/S2468-1253(21)00008-X.
    1. Gaeta G.B., Stornaiuolo G., Precone D.F., Amendola A., Zanetti A.R. Immunogenicity and safety of an adjuvanted influenza vaccine in patients with decompensated cirrhosis. Vaccine. 2002;20 doi: 10.1016/S0264-410X(02)00510-8.
    1. Härmälä S., Parisinos C.A., 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 doi: 10.1136/bmjopen-2019-031070.
    1. McCashland T.M., Preheim L.C., Gentry-Nielsen M.J. Pneumococcal vaccine response in cirrhosis and liver transplantation. J Infect Dis. 2000;181:757–760. doi: 10.1086/315245.
    1. Arguedas M.R., Johnson A., Eloubeidi M.A., Fallon M.B. Immunogenicity of hepatitis A vaccination in decompensated cirrhotic patients. Hepatology. 2001;34:28–31. doi: 10.1053/jhep.2001.25883.
    1. Amjad W., Alukal J., Zhang T., Maheshwari A., Thuluvath P.J. Two-dose hepatitis B vaccine (heplisav-B) results in better seroconversion than three-dose vaccine (engerix-B) in chronic liver disease. Dig Dis Sci. 2020 doi: 10.1007/s10620-020-06437-6.
    1. Liu J., Wu H., Chen H. Immune response to hepatitis B vaccine in patients with chronic hepatitis C infection: a systematic review and meta-analysis. Hepatol Res. 2018;48:119–126. doi: 10.1111/hepr.13008.
    1. Villeneuve E., Vincelette J., Villeneuve J.P. Ineffectiveness of hepatitis B vaccination in cirrhotic patients waiting for liver transplantation. Can J Gastroenterol. 2000;14 doi: 10.1155/2000/548206.
    1. Domínguez M., Bárcena R., García M., López-Sanroman A., Nuño J. Vaccination against hepatitis B virus in cirrhotic patients on liver transplant waiting list. Liver Transpl. 2000 doi: 10.1053/jlts.2000.8313.
    1. Stucchi R.S.B., Lopes M.H., Kumar D., Manuel O. Vaccine recommendations for solid-organ transplant recipients and donors. Transplantation. 2018;102:S72–80. doi: 10.1097/TP.0000000000002012.
    1. Danziger-Isakov L., Kumar D. Vaccination of solid organ transplant candidates and recipients: guidelines from the American society of transplantation infectious diseases community of practice. Clin Transpl. 2019;33 doi: 10.1111/ctr.13563.
    1. Fagiuoli S., Colli A., Bruno R., Craxì A., Gaeta G.B., Grossi P. Management of infections pre- and post-liver transplantation: report of an AISF consensus conference. J Hepatol. 2014 doi: 10.1016/j.jhep.2013.12.021.
    1. Croce E., Hatz C., Jonker E.F., Visser L.G., Jaeger V.K., Bühler S. Safety of live vaccinations on immunosuppressive therapy in patients with immune-mediated inflammatory diseases, solid organ transplantation or after bone-marrow transplantation – a systematic review of randomized trials, observational studies and case re. Vaccine. 2017;35:1216–1226. doi: 10.1016/j.vaccine.2017.01.048.
    1. Mulley W.R., Dendle C., Ling J.E.H., Knight S.R. Does vaccination in solid-organ transplant recipients result in adverse immunologic sequelae? A systematic review and meta-analysis. J Hear Lung Transpl. 2018;37:844–852. doi: 10.1016/j.healun.2018.03.001.
    1. Eckerle I., Rosenberger K.D., Zwahlen M., Junghanss T. Serologic vaccination response after solid organ transplantation: a systematic review. PLoS One. 2013;8 doi: 10.1371/journal.pone.0056974.
    1. Karbasi-Afshar R., Izadi M., Fazel M., Khedmat H. Response of transplant recipients to influenza vaccination based on type of immunosuppression: a meta-analysis. Saudi J Kidney Dis Transpl. 2015;26:877–883. doi: 10.4103/1319-2442.164556.
    1. Chong P.P., Handler L., Weber D.J. A systematic review of safety and immunogenicity of influenza vaccination strategies in solid organ transplant recipients. Clin Infect Dis. 2018;66:1802–1811. doi: 10.1093/cid/cix1081.
    1. Liao Z., Xu X., Liang Y., Xiong Y., Chen R., Ni J. Effect of a booster dose of influenza vaccine in patients with hemodialysis, peritoneal dialysis and renal transplant recipients: a systematic literature review and meta-analysis. Hum Vaccin Immunother. 2016;12:2909–2915. doi: 10.1080/21645515.2016.1201623.
    1. Beck C.R., McKenzie B.C., Hashim A.B., Harris R.C., Nguyen-Van-Tam J.S. Influenza vaccination for immunocompromised patients: systematic review and meta-analysis by etiology. J Infect Dis. 2012;206:1250–1259. doi: 10.1093/infdis/jis487.
    1. É Racine, Gilca V., Amini R., Tunis M., Ismail S., Sauvageau C. A systematic literature review of the recombinant subunit herpes zoster vaccine use in immunocompromised 18–49 year old patients. Vaccine. 2020;38:6205–6214. doi: 10.1016/j.vaccine.2020.07.049.
    1. Garcia Garrido H.M., Veurink A.M., Leeflang M., Spijker R., Goorhuis A., Grobusch M.P. Hepatitis A vaccine immunogenicity in patients using immunosuppressive drugs: a systematic review and meta-analysis. Trav Med Infect Dis. 2019;32 doi: 10.1016/j.tmaid.2019.101479.
    1. Mellet J., Pepper M.S. A COVID-19 vaccine: big strides come with big challenges. Vaccines. 2021;9:39. doi: 10.3390/vaccines9010039.
    1. Connors M., Graham B.S., Lane H.C., Fauci A.S. SARS-CoV-2 vaccines: much accomplished, much to learn. Ann Intern Med. 2021:M21–0111. doi: 10.7326/M21-0111.
    1. Krammer F. SARS-CoV-2 vaccines in development. Nature. 2020;586:516–527. doi: 10.1038/s41586-020-2798-3.
    1. Polack F.P., Thomas S.J., Kitchin N., Absalon J., Gurtman A., Lockhart S. Safety and efficacy of the BNT162b2 mRNA covid-19 vaccine. N Engl J Med. 2020 doi: 10.1056/NEJMoa2034577. NEJMoa2034577.
    1. Baden L.R., El Sahly H.M., Essink B., Kotloff K., Frey S., Novak R. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med. 2020 doi: 10.1056/NEJMoa2035389. NEJMoa2035389.
    1. Voysey M., Clemens S.A.C., Madhi S.A., Weckx L.Y., Folegatti P.M., Aley P.K. 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 (London, England) 2020 doi: 10.1016/S0140-6736(20)32661-1.
    1. L’Huillier A.G., Meyer B., Andrey D.O., Arm-Vernez I., Baggio S., Didierlaurent A. Antibody persistence in the first six months following SARS-CoV-2 infection among hospital workers: a prospective longitudinal study. Clin Microbiol Infect. 2021 doi: 10.1016/j.cmi.2021.01.005.
    1. Moreau R., Jalan R., Gines P., Pavesi M., Angeli P., Cordoba J. Acute-on-chronic liver failure is a distinct syndrome that develops in patients with acute decompensation of cirrhosis. Gastroenterology. 2013;144 doi: 10.1053/j.gastro.2013.02.042.
    1. Jalan R., Fernandez J., Wiest R., Schnabl B., Moreau R., Angeli P. Bacterial infections in cirrhosis: a position statement based on the EASL Special Conference 2013. J Hepatol. 2014;60:1310–1324. doi: 10.1016/j.jhep.2014.01.024.
    1. Trebicka J., Fernandez J., Papp M., Caraceni P., Laleman W., Gambino C. PREDICT identifies precipitating events associated with the clinical course of acutely decompensated cirrhosis. J Hepatol. 2020 doi: 10.1016/j.jhep.2020.11.019.
    1. Boettler T., Marjot T., Newsome P.N., Mondelli M.U., Maticic M., Cordero E. Impact of COVID-19 on the care of patients with liver disease: EASL-ESCMID position paper after 6 months of the pandemic. JHEP Rep. 2020;2:100169. doi: 10.1016/j.jhepr.2020.100169.
    1. Marjot T., Moon A.M., Cook J.A., Abd-Elsalam S., Aloman C., Armstrong M.J. Outcomes following SARS-CoV-2 infection in patients with chronic liver disease: an international registry study. J Hepatol. 2020 doi: 10.1016/j.jhep.2020.09.024.
    1. Leise M.D., Talwalkar J.A. Immunizations in chronic liver disease: what should be done and what is the evidence. Curr Gastroenterol Rep. 2013;15 doi: 10.1007/s11894-012-0300-6.
    1. Pellegrino P., Clementi E., Radice S. On vaccine’s adjuvants and autoimmunity: current evidence and future perspectives. Autoimmun Rev. 2015;14:880–888. doi: 10.1016/j.autrev.2015.05.014.
    1. Gershwin L.J. Adverse reactions to vaccination: from anaphylaxis to autoimmunity. Vet Clin North Am–small Anim Pract. 2018;48:279–290. doi: 10.1016/j.cvsm.2017.10.005.
    1. Orbach H., Agmon-Levin N., Zandman-Goddard G. Vaccines and autoimmune diseases of the adult. Discov Med. 2010;9:90–97.
    1. Liang Z., Zhu H., Wang X., Jing B., Li Z., Xia X. Adjuvants for coronavirus vaccines. Front Immunol. 2020;11 doi: 10.3389/fimmu.2020.589833.
    1. Elwood J.M., Ameratunga R. Autoimmune diseases after hepatitis B immunization in adults: literature review and meta-analysis, with reference to ‘autoimmune/autoinflammatory syndrome induced by adjuvants’ (ASIA) Vaccine. 2018;36:5796–5802. doi: 10.1016/j.vaccine.2018.07.074.
    1. Genovese C., La Fauci V., Squeri A., Trimarchi G., Squeri R. HPV vaccine and autoimmune diseases: systematic review and meta-analysis of the literature. J Prev Med Hyg. 2018;59:E194–E199. doi: 10.15167/2421-4248/jpmh2018.59.3.998.
    1. Gabay C., Bel M., Combescure C., Ribi C., Meier S., Posfay-Barbe K. Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum. 2011;63:1486–1496. doi: 10.1002/art.30325.
    1. Mahmud S.M., Bozat-Emre S., Mostaço-Guidolin L.C., Marrie R.A. Registry cohort study to determine risk for multiple sclerosis after vaccination for pandemic influenza a(H1N1) with arepanrix, manitoba, Canada. Emerg Infect Dis. 2018;24:1267–1274. doi: 10.3201/eid2407.161783.
    1. Confavreux C., Suissa S., Saddier P., Bourdès V., Vukusic S. Vaccinations and the risk of relapse in multiple sclerosis. N Engl J Med. 2001;344:319–326. doi: 10.1056/nejm200102013440501.
    1. Fishman J.A. Infection in organ transplantation. Am J Transpl. 2017;17:856–879. doi: 10.1111/ajt.14208.
    1. Webb G.J., Moon A.M., Barnes E., Barritt A.S., Marjot T. Determining risk factors for mortality in liver transplant patients with COVID-19. Lancet Gastroenterol Hepatol. 2020;5:643–644. doi: 10.1016/S2468-1253(20)30125-4.

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir