590
Views
0
CrossRef citations to date
0
Altmetric
Original Research

Immunogenicity assessment of elder hepatocellular carcinoma patients after inactivated whole-virion SARS-CoV-2 vaccination

, , , , , , , , & show all
Pages 1102-1113 | Received 25 Jun 2023, Accepted 19 Oct 2023, Published online: 10 Nov 2023

References

  • Ribas A, Sengupta R, Locke T, et al. Priority COVID-19 vaccination for patients with Cancer while vaccine supply is limited. Cancer Discov. 2021 Feb;11(2):233–236. PubMed PMID: 33355178; PubMed Central PMCID: PMCPMC8053003. doi: 10.1158/2159-8290.CD-20-1817
  • Becerril-Gaitan A, Vaca-Cartagena BF, Ferrigno AS, et al. Immunogenicity and risk of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection after coronavirus disease 2019 (COVID-19) vaccination in patients with cancer: a systematic review and meta-analysis. Eur J Cancer. 2022 Jan;160:243–260. PubMed PMID: 34794855; PubMed Central PMCID: PMCPMC8548030. doi: 10.1016/j.ejca.2021.10.014.
  • Au L, Boos LA, Swerdlow A, et al. Cancer, COVID-19, and antiviral immunity: the CAPTURE study. Cell. 2020 Oct 1;183(1):4–10. PubMed PMID: 32979319; PubMed Central PMCID: PMCPMC7470737 Diagnostics. L.A., L.B., F.B., S.S., A.F., A.S. have no conflicts of interest to declare. doi: 10.1016/j.cell.2020.09.005
  • Kuderer NM, Choueiri TK, Shah DP, et al. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet. 2020 Jun 20;395(10241):1907–1918. PubMed PMID: 32473681; PubMed Central PMCID: PMCPMC7255743. doi: 10.1016/S0140-6736(20)31187-9.
  • Desai A, Sachdeva S, Parekh T et al. COVID-19 and Cancer: lessons from a Pooled meta-analysis. JCO glob oncol. 2020 Apr;6:557–559. doi: 10.1200/GO.20.00097. PubMed PMID: 32250659; PubMed Central PMCID: PMCPMC7193801 manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO’s conflict of interest policy, please refer to. Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments). No potential conflicts of interest were reported. www.asco.org/rwcorascopubs.org/go/site/misc/authors.html
  • Liebers N, Speer C, Benning L, et al. Humoral and cellular responses after COVID-19 vaccination in anti-CD20-treated lymphoma patients. Blood. 2022 Jan 6;139(1):142–147. PubMed PMID: 34669919; PubMed Central PMCID: PMCPMC8530768. doi: 10.1182/blood.2021013445
  • Polack FP, Thomas SJ, Kitchin N, et al. Safety and efficacy of the BNT162b2 mRNA covid-19 vaccine. N Engl J Med. [2020 Dec 31];383(27):2603–2615. PubMed PMID: 33301246; PubMed Central PMCID: PMCPMC7745181. doi: 10.1056/NEJMoa2034577
  • Walsh EE, Frenck RW Jr., Falsey AR, et al. Safety and immunogenicity of two RNA-Based covid-19 vaccine candidates. N Engl J Med. [2020 Dec 17];383(25):2439–2450. PubMed PMID: 33053279; PubMed Central PMCID: PMCPMC7583697. doi: 10.1056/NEJMoa2027906
  • Xia S, Zhang Y, Wang Y, et al. Safety and immunogenicity of an inactivated SARS-CoV-2 vaccine, BBIBP-CorV: a randomised, double-blind, placebo-controlled, phase 1/2 trial. Lancet Infect Dis. 2021 Jan;21(1):39–51. PubMed PMID: 33069281; PubMed Central PMCID: PMCPMC7561304. doi: 10.1016/S1473-3099(20)30831-8
  • Monin L, Laing AG, Munoz-Ruiz M, et al. Safety and immunogenicity of one versus two doses of the COVID-19 vaccine BNT162b2 for patients with cancer: interim analysis of a prospective observational study. Lancet Oncol. 2021 Jun;22(6):765–778. PubMed PMID: 33930323; PubMed Central PMCID: PMCPMC8078907. doi: 10.1016/S1470-2045(21)00213-8
  • Herzog Tzarfati K, Gutwein O, Apel A, et al. BNT162b2 COVID-19 vaccine is significantly less effective in patients with hematologic malignancies. Am J Hematol. [2021 Oct 1];96(10):1195–1203. PubMed PMID: 34185336; PubMed Central PMCID: PMCPMC8420332 interests. doi: 10.1002/ajh.26284
  • Van Oekelen O, Gleason CR, Agte S, et al. Highly variable SARS-CoV-2 spike antibody responses to two doses of COVID-19 RNA vaccination in patients with multiple myeloma. Cancer Cell. [2021 Aug 9];39(8):1028–1030. PubMed PMID: 34242572; PubMed Central PMCID: PMCPMC8238657. doi: 10.1016/j.ccell.2021.06.014
  • Fendler A, Shepherd STC, Au L, et al. Adaptive immunity and neutralizing antibodies against SARS-CoV-2 variants of concern following vaccination in patients with cancer: the CAPTURE study. Nat Cancer. 2021 Dec;2(12):1321–1337. PubMed PMID: 34950880; PubMed Central PMCID: PMCPMC7612125. doi: 10.1038/s43018-021-00274-w
  • Grinshpun A, Rottenberg Y, Ben-Dov IZ, et al. Serologic response to COVID-19 infection and/or vaccine in cancer patients on active treatment. ESMO Open. 2021 Dec;6(6):100283. PubMed PMID: 34634634; PubMed Central PMCID: PMCPMC8469519. doi: 10.1016/j.esmoop.2021.100283
  • Buttiron Webber T, Provinciali N, Musso M, et al. Predictors of poor seroconversion and adverse events to SARS-CoV-2 mRNA BNT162b2 vaccine in cancer patients on active treatment. Eur J Cancer. 2021 Dec;159:105–112. PubMed PMID: 34742157; PubMed Central PMCID: PMCPMC8502731. doi: 10.1016/j.ejca.2021.09.030
  • Chung DJ, Shah GL, Devlin SM, et al. Disease- and therapy-specific impact on humoral immune responses to COVID-19 vaccination in hematologic malignancies. Blood Cancer Discov. 2021 Nov;2(6):568–576. PubMed PMID: 34778797; PubMed Central PMCID: PMCPMC8580617. doi: 10.1158/2643-3230.BCD-21-0139
  • Sung H, Ferlay J, Siegel RL, et al. Global Cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021 May;71(3):209–249. PubMed PMID: 33538338. doi: 10.3322/caac.21660
  • Zheng RS, Zhang SW, Sun KX, et al. Cancer statistics in China, 2016. Zhonghua Zhong Liu Za Zhi. 2023 Mar 23;45(3): 212–220. PubMed PMID: 36944542. 10.3760/cma.j.cn112152-20220922-00647.
  • Cornberg M, Buti M, Eberhardt CS, et al. 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 Apr;74(4):944–951. PubMed PMID: 33563499; PubMed Central PMCID: PMCPMC7867401. doi: 10.1016/j.jhep.2021.01.032
  • Liu F, Feng X, Du J, et al. Serologic status and safety of inactivated covid-19 vaccine for hepatocellular carcinoma patients with cirrhosis after curative liver resection. Cancer Commun (Lond). 2023 Mar;43(3):409–412. PubMed PMID: 36566347; PubMed Central PMCID: PMCPMC9880698. doi: 10.1002/cac2.12398
  • He T, Zhou Y, Xu P, et al. Safety and antibody response to inactivated COVID-19 vaccine in patients with chronic hepatitis B virus infection. Liver Int. 2022;Jun:421:1287–1296. PubMed PMID: 35107848. doi: 10.1111/liv.15173
  • Wang J, Zhang Q, Ai J, et al. Safety and immunogenicity of SARS-CoV-2 vaccines in Chinese patients with cirrhosis: a prospective multicenter study. Hepatol Int. 2022 Jun;16(3):691–701. PubMed PMID: 35403977; PubMed Central PMCID: PMCPMC8995697. doi: 10.1007/s12072-022-10332-9
  • Ai J, Wang J, Liu D, 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;20(7):1516–1524 e2. PubMed PMID: 34942370; PubMed Central PMCID: PMCPMC8686447. doi: 10.1016/j.cgh.2021.12.022
  • Zhan H, Gao H, Liu Y, et al. Booster shot of inactivated SARS-CoV-2 vaccine induces potent immune responses in people living with HIV. J Med Virol. 2023 Jan;95(1):e28428. PubMed PMID: 36571267; PubMed Central PMCID: PMCPMC9880704. doi: 10.1002/jmv.28428
  • Xia S, Zhang Y, Wang Y, et al. Safety and immunogenicity of an inactivated COVID-19 vaccine, BBIBP-CorV, in people younger than 18 years: a randomised, double-blind, controlled, phase 1/2 trial. Lancet Infect Dis. 2022 Feb;22(2):196–208. PubMed PMID: 34536349; PubMed Central PMCID: PMCPMC8443232 SHZ, JJC, QQL, HF, YX, and XTZ are employees of Beijing Institute of Biological Products, which developed the vaccine and funded the trial. All other authors declare no competing interests. doi: 10.1016/S1473-3099(21)00462-X
  • Ariamanesh M, Porouhan P, PeyroShabany B, et al. Immunogenicity and Safety of the inactivated SARS-CoV-2 vaccine (BBIBP-CorV) in patients with malignancy. Cancer Invest. 2022 Jan;40(1):26–34. PubMed PMID: 34634986; PubMed Central PMCID: PMCPMC8567287. doi: 10.1080/07357907.2021.1992420
  • Huang R, Liu X, Xie F, et al. Safety and immunogenicity of inactivated SARS-CoV-2 vaccine (BBIBP-CorV) in hypertensive and/or diabetic people aged over 60 years: a prospective Open-label study. Diabetes Ther. 2023 Jan;14(1):139–151. PubMed PMID: 36437418; PubMed Central PMCID: PMCPMC9702925. doi: 10.1007/s13300-022-01343-8
  • Al Kaabi N, Zhang Y, Xia S, et al. Effect of 2 inactivated SARS-CoV-2 vaccines on symptomatic COVID-19 infection in adults: a randomized Clinical trial. JAMA. 2021 Jul 6;326(1): 35–45. PubMed PMID: 34037666; PubMed Central PMCID: PMCPMC8156175 Ms Y. Yang, Ms Y. Zhao, Ms H.Wang, and Mr Li reported receiving grants from the Ministry of Science and Technology of the People’s Republic of China (2020YFC0842100) during the conduct of the study. Dr Yuntao Zhang, Ms Y Yang, Ms Xuqin Yang, Mr Lai, Ms Q. Wang, Mr T. Yang, Mr Liu, and Dr Xiaoming Yang are employees of the China National Biotec Group Company Limited; Mr Li, Mr Chen and Drs Huang and Duan are employees of the Wuhan Institute of Biological Products Co, Ltd; and Mr W. Wang, Mr Ma, Ms Y. Zhao, and Ms H. Wang are employees of the Beijing Institute of Biological Products Co, Ltd-all companies that developed the vaccine and sponsored the trial. Drs Jiang and G. Zhao are employees of the Beijing Key-Tech Statistical Consulting Co, Ltd, and received fees from the China National Biotec Group Company Limited to conduct the data analysis. Drs Al Kaabi, Abdalla, Hussein, Al Mazrouei, Al Karam, Hussain, and Khan and Mr Fasihuddin reported being an employee of Abu Dhabi Health Services Company. Drs Mahmoud and Zaher, Mr ElTantawy, Mr Xiao, and Mr Koshy reported being an employee of the G42 Healthcare. Ms H. Wang reported receiving grants from the Beijing Municipal Science & Technology Commission during the conduct of the study and having a patent for 202010575098.9 pending, a patent for 202010537733.4 pending, a patent for 202010537730.0 pending, a patent for 202110052921.2 pending, and a patent for 202110052933.5 pending. Drs Xiaoming Yang and Duan and Mr Li have a patent for 202010559132.3 pending. No other disclosures were reported. doi: 10.1001/jama.2021.8565
  • Yue L, Xie T, Yang T, et al. A third booster dose may be necessary to mitigate neutralizing antibody fading after inoculation with two doses of an inactivated SARS-CoV-2 vaccine. J Med Virol. 2022 Jan;94(1):35–38. PubMed PMID: 34516026; PubMed Central PMCID: PMCPMC8661707. doi: 10.1002/jmv.27334
  • Cheng ZJ, Huang H, Zheng P, et al. Humoral immune response of BBIBP COVID-19 vaccination before and after the booster immunization. Allergy. 2022 Aug;77(8):2404–2414. PubMed PMID: 35255171; PubMed Central PMCID: PMCPMC9111230. doi: 10.1111/all.15271
  • Regev-Yochay G, Gonen T, Gilboa M, et al. Efficacy of a fourth dose of Covid-19 mRNA vaccine against Omicron. N Engl J Med. [2022 Apr 7];386(14):1377–1380. PubMed PMID: 35297591; PubMed Central PMCID: PMCPMC9006792. doi: 10.1056/NEJMc2202542
  • Bar-On YM, Goldberg Y, Mandel M, et al. Protection by a fourth dose of BNT162b2 against Omicron in Israel. N Engl J Med. [2022 May 5];386(18):1712–1720. PubMed PMID: 35381126; PubMed Central PMCID: PMCPMC9006780. doi: 10.1056/NEJMoa2201570
  • Goh YS, Rouers A, Fong SW, et al. Waning of specific antibodies against Delta and Omicron variants five months after a third dose of BNT162b2 SARS-CoV-2 vaccine in elderly individuals. Front Immunol PubMed PMID: 36451833; PubMed Central PMCID: PMCPMC9704817. 2022;13:1031852. doi: 10.3389/fimmu.2022.1031852
  • Lyke KE, Atmar RL, Islas CD, et al. Rapid decline in vaccine-boosted neutralizing antibodies against SARS-CoV-2 Omicron variant. Cell Rep Med. 2022 Jul 19;3(7): 100679. PubMed PMID: 35798000; PubMed Central PMCID: PMCPMC9212999. 10.1016/j.xcrm.2022.100679.
  • Collier DA, Ferreira I, Kotagiri P, et al. Age-related immune response heterogeneity to SARS-CoV-2 vaccine BNT162b2. Nature. 2021 Aug;596(7872):417–422. PubMed PMID: 34192737; PubMed Central PMCID: PMCPMC8373615. doi: 10.1038/s41586-021-03739-1
  • Tober-Lau P, Schwarz T, Vanshylla K, et al. Long-term immunogenicity of BNT162b2 vaccination in older people and younger health-care workers. Lancet Respir Med. 2021 Nov;9(11):e104–e105. PubMed PMID: 34687656; PubMed Central PMCID: PMCPMC8528470 regarding the diagnosis of SARS-CoV-2 by antibody testing (application number EP20158626.0). HG and FKl are named on a patent application regarding neutralising antibodies against SARS-related coronaviruses (application number EP20177354). All other authors declare no competing interests. We thank all study participants at Charite - Universitatsmedizin Berlin for their participation. We also thank the entire staff of the Department for Occupational Medicine, the Charite Clinical Study Center at Charite - Universitatsmedizin Berlin, and the Berlin Institute of Health (BIH) for their support during the study. SARS-CoV-2 RBD variant antigens were kindly provided by InVivo BioTech Services (Hennigsdorf, Germany) to the Seramun Diagnostica (Heidesee, Germany). Parts of this work were supported by grants from the BIH and Berlin University Alliance. This study was further supported by the German Ministry of Education and Research through Forschungsnetzwerk der Universitatsmedizin zu COVID-19, (COVIM, FKZ: 01KX2021) to LES, FKu, FKI, CD, and VMC; through VARIPath projects (01KI2021) to VMC; and through Deutsche Forschungsgemeinschaft (SFB-TR84) to NS and LES. The study was supported by a donation from Zalando to Charite - Universitatsmedizin Berlin. doi: 10.1016/S2213-2600(21)00456-2
  • Banchereau J, Briere F, Caux C, et al. Immunobiology of dendritic cells. Annu Rev Immunol. 2000;18(1):767–811. PubMed PMID: 10837075. doi: 10.1146/annurev.immunol.18.1.767
  • Valentini N, Marchitto L, Raymond M, et al. Innate immunity and SARS-CoV-2 vaccine response in hemodialysis patients. Kidney360. [2022 Oct 27];3(10):1763–1768. PubMed PMID: 36514720; PubMed Central PMCID: PMCPMC9717667. doi: 10.34067/KID.0002542022
  • Lv Z, Li Q, Feng Z, et al. Inactivated SARS-CoV-2 vaccines elicit immunogenicity and T-cell responses in people living with HIV. Int Immunopharmacol. 2022 Jan;102:108383. PubMed PMID: 34824035; PubMed Central PMCID: PMCPMC8599017. doi: 10.1016/j.intimp.2021.108383
  • Feng Y, Zhang Y, He Z, et al. Immunogenicity of an inactivated SARS-CoV-2 vaccine in people living with HIV-1: a non-randomized cohort study. EClinicalMedicine. 2022 Jan;43:101226. PubMed PMID: 34901799; PubMed Central PMCID: PMCPMC8642727. doi: 10.1016/j.eclinm.2021.101226
  • Sahin U, Muik A, Derhovanessian E, et al. COVID-19 vaccine BNT162b1 elicits human antibody and T(H)1 T cell responses. Nature. 2020 Oct;586(7830):594–599. PubMed PMID: 32998157. doi: 10.1038/s41586-020-2814-7