Immunogenicity of SARS-CoV-2 vaccines in patients with cancer
2022; Elsevier BV; Volume: 28; Issue: 12 Linguagem: Inglês
10.1016/j.molmed.2022.07.006
ISSN1471-499X
AutoresHelen Kakkassery, Esme Carpenter, Piers Patten, Sheeba Irshad,
Tópico(s)COVID-19 and healthcare impacts
ResumoCOVID-19 mRNA and viral vector-based vaccines can safely generate humoral and cellular immune responses in patients with cancer, albeit at diminished levels compared to those in the general population.Patients at higher risk of no response to vaccines include patients with haematological malignancies treated with anti-CD20, anti-BCMA/CD38, active chemotherapy, and high-dose steroids. Patients on immunotherapy and endocrine/targeted therapies are less affected.Some seronegative patients can generate robust T-cell responses, showing disparate responses to vaccines in patients with cancer, and potentiating roles for T-cell responses as a possible correlate of protection.Third booster doses have shown benefit in a few patients, but seronegative patients who are also negative for T-cell responses remain unprotected. Transmission of the SARS-CoV-2 virus and its corresponding disease (COVID-19) has been shown to impose a higher burden on cancer patients than on the general population. Approved vaccines for use include new technology mRNA vaccines such as BNT162b2 (Pfizer–BioNTech) and mRNA-1273 (Moderna), and nonreplicating viral vector vaccines such as Ad26.COV2.S (Johnson & Johnson) and AZD1222 (AstraZeneca). Impaired or delayed humoral and diminished T-cell responses are evident in patients with cancer, especially in patients with haematological cancers or those under active chemotherapy. Herein we review the current data on vaccine immunogenicity in cancer patients, including recommendations for current practice and future research. Transmission of the SARS-CoV-2 virus and its corresponding disease (COVID-19) has been shown to impose a higher burden on cancer patients than on the general population. Approved vaccines for use include new technology mRNA vaccines such as BNT162b2 (Pfizer–BioNTech) and mRNA-1273 (Moderna), and nonreplicating viral vector vaccines such as Ad26.COV2.S (Johnson & Johnson) and AZD1222 (AstraZeneca). Impaired or delayed humoral and diminished T-cell responses are evident in patients with cancer, especially in patients with haematological cancers or those under active chemotherapy. Herein we review the current data on vaccine immunogenicity in cancer patients, including recommendations for current practice and future research. Transmission of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus has led to the ongoing global coronavirus disease 2019 (COVID-19) pandemic. Patients with cancer are at higher risk of significant COVID-19-associated morbidity and mortality than the general population [1.Kuderer N.M. et al.Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study.Lancet. 2020; 395: 1907-1918Abstract Full Text Full Text PDF PubMed Scopus (949) Google Scholar,2.Bakouny Z. et al.COVID-19 and cancer: current challenges and perspectives.Cancer Cell. 2020; 38: 629-646Abstract Full Text Full Text PDF PubMed Scopus (116) Google Scholar]. Prolonged viral shedding, delayed seroconversion (see Glossary), and an exhausted T-cell phenotype have been demonstrated in SARS-CoV-2-infected cancer patients [3.Abdul-Jawad S. et al.Acute immune signatures and their legacies in severe acute respiratory syndrome coronavirus-2 infected cancer patients.Cancer Cell. 2021; 39: 257-275.e6Abstract Full Text Full Text PDF PubMed Scopus (57) Google Scholar]. Patients with lung cancer and haematological malignancies are at highest risk, as are recipients of stem-cell transplants and adoptive cellular therapies [4.Zhang H. et al.Clinical characteristics and outcomes of COVID-19-infected cancer patients: a systematic review and meta-analysis.JNCI J. Natl. Cancer Inst. 2021; 113: 371-380Crossref PubMed Scopus (0) Google Scholar, 5.Sahu K.K. et al.Challenges of cellular therapy during the COVID-19 pandemic.Adv. Exp. Med. Biol. 2021; 1318: 657-672Crossref PubMed Scopus (2) Google Scholar, 6.Leclerc M. Maury S. A rationale to prioritise vaccination of HSCT patients against COVID-19.Lancet Haematol. 2021; 8: e163-e164Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, 7.Ribas A. et al.Priority COVID-19 vaccination for patients with cancer while vaccine supply is limited.Cancer Discov. 2021; 11: 233-236Crossref PubMed Scopus (117) Google Scholar]. Effective measures taken to protect patients with cancer from contracting COVID-19 have included prioritisation of vaccination against SARS-CoV-2 and public health measures. Approved vaccines for use include new technology mRNA vaccines such as BNT162b2 (Pfizer–BioNTech) and mRNA-1273 (Moderna), and nonreplicating viral vector vaccines such as Janssen's Ad26.COV2.S (Johnson & Johnson) and AZD1222 (AstraZeneca) (Figure 1, Key figure) [8.Polack F.P. et al.Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine.N. Engl. J. 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The exclusion of patients with cancer and other immunocompromised groups from registration in COVID-19 vaccine trials has meant that vaccine efficacy in this patient population has had to be elucidated from small prospective observational studies focused on immunological or antibody responses [12.Monin L. 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; 22: 765-778Abstract Full Text Full Text PDF PubMed Google Scholar, 13.Fendler A. 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; 2: 1305-1320Crossref PubMed Scopus (0) Google Scholar, 14.Lim S.H. et al.Antibody responses after SARS-CoV-2 vaccination in patients with lymphoma.Lancet Haematol. 2021; 8: e542-e544Abstract Full Text Full Text PDF PubMed Google Scholar], as opposed to data on protection against breakthrough or symptomatic coronavirus infections, coronavirus hospitalisation, or death. Herein we review the available evidence evaluating the safety and the antibody and cellular responses in cancer patients to COVID-19 vaccinations, and the longevity of those responses. Assessment of vaccine-induced immune responses in patients with cancer has largely focused on evaluating the presence of antibodies binding the SARS-CoV-2 spike protein to establish rates of seroconversion and mean antibody titres (Table 1, Figure 2). First data reporting on the immunogenicity of the BNT162b2 mRNA vaccine in patients with cancer confirmed that only 38% of patients with solid tumours and <20% of patients with haematological malignancies developed SARS-CoV-2 S-specific IgG following the primary vaccine inoculum, contrasting with 94% in the control cohort of predominantly healthcare workers without cancer [12.Monin L. 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; 22: 765-778Abstract Full Text Full Text PDF PubMed Google Scholar]. The poor immune efficacy of the priming dose of COVID-19 vaccines in patients with solid cancer has been shown to be rescued by a subsequent second dose of the vaccine administered with seropositivity reported as ranging between 75% and 95% across the studies [15.Thakkar A. et al.Seroconversion rates following COVID-19 vaccination among patients with cancer.Cancer Cell. 2021; 39: 1081-1090.e2Abstract Full Text Full Text PDF PubMed Scopus (153) Google Scholar, 16.Barrière J. et al.Impaired immunogenicity of BNT162b2 anti-SARS-CoV-2 vaccine in patients treated for solid tumors.Ann. 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Cancer Res. 2021; 27: 6815-6823Crossref PubMed Scopus (21) Google Scholar, 25.Figueiredo J.C. et al.Longitudinal SARS-CoV-2 mRNA vaccine-induced humoral immune responses in patients with cancer.Cancer Res. 2021; 81: 6273-6280Crossref PubMed Scopus (7) Google Scholar, 26.Shmueli E.S. et al.Efficacy and safety of BNT162b2 vaccination in patients with solid cancer receiving anticancer therapy – a single centre prospective study.Eur. J. Cancer. 2021; 157: 124-131Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar, 27.Palich R. et al.High seroconversion rate but low antibody titers after two injections of BNT162b2 (Pfizer-BioNTech) vaccine in patients treated with chemotherapy for solid cancers.Ann. 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Patients on active cytotoxic chemotherapy and immune-cell-depleting agents (anti-CD20, anti-CD38) show the poorest seroconversion, unlike those on endocrine therapy and immune checkpoint inhibitors where reduced antibody responses are less common [31.Tran S. et al.Evaluation of COVID-19 vaccine response in patients with cancer: an interim analysis.Eur. J. Cancer. 2021; 159: 259-274Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar]. Therefore, given the adequate antibody protection provided by two vaccine doses in patients with solid cancer, a third vaccine dose is strongly encouraged particularly for individuals with haematological malignancies, in whom two doses do not provide sufficient immune protection.Table 1Summary table of studies defining seroconversion ratesCancer typeControlCountryMedian age (years)(IQR/range)VaccineSeroconversion (cancer)Seroconversion (control)RefsHaematologicalMDS (n = 36)Control (n = 26)UKPatient: 67.5 (59–73)Control: 35 (27–49)BNT162b2AZD12221st dose: NAAZD1222 2nd dose: 76.2%BNT162b2 2nd dose: 100%1st dose: NA2nd dose: 100%[39.Abdul-Jawad S. et al.BNT162b2 COVID-19 and ChAdOx1 nCoV-19 vaccination in patients with myelodysplastic syndromes.Haematologica. 2022; 107: 1181-1184Crossref PubMed Scopus (1) Google Scholar]Solid cancer (n = 106)Haematological (n = 25)NAUSASwitzerlandPatient: 63 (55–69)BNT162b2mRNA-1273Solid cancer1st dose: 83%2nd dose: 98%Haematological1st dose: 72%2nd dose: 77%NA[23.Addeo A. et al.Immunogenicity of SARS-CoV-2 messenger RNA vaccines in patients with cancer.Cancer Cell. 2021; 39: 1091-1098.e2Abstract Full Text Full Text PDF PubMed Scopus (116) Google Scholar]HaematologicalMM (n = 171)Control (n = 64)IsraelPatient: 70 (38–94)BNT162b21st dose: NA2nd dose: 78%1st dose: NA2nd dose: 98%[104.Avivi I. et al.Humoral response rate and predictors of response to BNT162b2 mRNA COVID19 vaccine in patients with multiple myeloma.Br. J. Haematol. 2021; 195: 186-193Crossref PubMed Scopus (37) Google Scholar]Solid cancer (n = 122)Control (n = 29)FrancePatient: 69.5 (44–90)Control: 53 (21–81)BNT162b21st dose: 47.5%2nd dose: 95.2%1st dose: 100%2nd dose: 100%[16.Barrière J. et al.Impaired immunogenicity of BNT162b2 anti-SARS-CoV-2 vaccine in patients treated for solid tumors.Ann. Oncol. 2021; 32: 1053-1055Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar]Solid cancer (n = 136)Haematological (n = 123)NAAustriaPatient: 65.1 (12.2)BNT162b21st dose (solid cancer): 60%1st dose (haematological): 43.4%2nd dose (solid cancer): 94.5%2nd dose (haematological): 71·4%NA[105.Benda M. et al.Serological SARS-CoV-2 antibody response, potential predictive markers and safety of BNT162b2 mRNA COVID-19 vaccine in haematological and oncological patients.Br. J. Haematol. 2021; 195: 523-531Crossref PubMed Scopus (10) Google Scholar]CLL (n = 373)NAIsraelPatient: 70 (40–89)BNT162b22nd dose: 43%NA[106.Benjamini O. et al.Safety and efficacy of BNT162b mRNA Covid19 vaccine in patients with chronic lymphocytic leukemia.Haematologica. 2022; 107: 625-634Crossref PubMed Scopus (36) Google Scholar]Multiple myeloma (n =93)Control (n = 177)UKPatient: 67 (47–84)BNT162b2AZD12221st dose: 56% (70% when measuring total antibody)2nd dose: NA1st dose: 99%2nd dose: NA[100.Bird S. et al.Response to first vaccination against SARS-CoV-2 in patients with multiple myeloma.Lancet Haematol. 2021; 8: e389-e392Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar]Solid cancer (n = 169)NAFrancePatient: 66 (27–89)BNT162b21st dose: 15%2nd dose: 65%3rd dose: 75% (27/36) suboptimal responders onlyNA[81.Fenioux C. et al.SARS-CoV-2 antibody response to 2 or 3 doses of the BNT162b2 vaccine in patients treated with anticancer agents.JAMA Oncol. 2022; 8: 612Crossref PubMed Scopus (15) Google Scholar]Solid cancer (n = 257)ControlItalyPatient: 65 (28–86)Control: NABNT162b2mRNA-12731st dose: NA2nd dose: 75.88%1st dose: NA2nd dose: 100%[19.Cavanna L. et al.COVID-19 vaccines in adult cancer patients with solid tumours undergoing active treatment: seropositivity and safety. A prospective observational study in Italy.Eur. J. Cancer. 2021; 157: 441-449Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar]Haematological (n = 241)NASpainPatient: 63 (53–71)mRNA-12731st dose: NA2nd dose: 76.3%NA[60.Jiménez M. et al.Cellular and humoral immunogenicity of the mRNA-1273 SARS-CoV-2 vaccine in patients with hematologic malignancies.Blood Adv. 2022; 6: 774-784Crossref PubMed Scopus (16) Google Scholar]Haematological Myeloid cancer (n = 59)Control (n = 232)UKPatient: 62 (52–73)Control: 62 (60–76)BNT162b2AZD12221st dose: 58%BNT162b21st dose: 98%AZD12221st dose: 92[107.Chowdhury O. et al.Impaired antibody response to COVID-19 vaccination in patients with chronic myeloid neoplasms.Br. J. Haematol. 2021; 194: 1010-1015Crossref PubMed Scopus (0) Google Scholar]Solid cancerHaematological (n = 141)NABelgiumPatient: 62.0 (26.0–86.0)BNT162b2Targeted/hormonal2nd dose: 97%3rd dose: 100%Chemotherapy2nd dose: 75%3rd dose: 83%Chemoimmunotherapy2nd dose: 100% (n = 3)3rd dose: 100% (n = 3)Immunotherapy2nd dose: 88%3rd dose: 88%Rituximab2nd dose: 21%3rd dose: 41%NA[80.Debie Y. et al.Antibody titres before and after a third dose of the SARS-CoV-2 BNT162b2 vaccine in patients with cancer.Eur. J. Cancer. 2022; 163: 177-179Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar]Solid cancer (n = 816)Control (n = 274)ItalyPatient: 62 (21–97)Control: 47 (21–69)BNT162b21st dose: 14.2%2nd dose: 86%1st dose: 33.6%2nd dose: 99.2%[24.Di Noia V. et al.Immunogenicity and safety of COVID-19 vaccine BNT162b2 for patients with solid cancer: a large cohort prospective study from a single institution.Clin. Cancer Res. 2021; 27: 6815-6823Crossref PubMed Scopus (21) Google Scholar]Solid cancer (n = 201)Haematological (n = 323)NADenmarkPatient: 70 (63–75)BNT162b2mRNA-1273Solid cancer1st dose: 77%2nd dose: 93%Haematological1st dose:2nd dose: 66%NA[21.Ehmsen S. et al.Antibody and T cell immune responses following mRNA COVID-19 vaccination in patients with cancer.Cancer Cell. 2021; 39: 1034-1036Abstract Full Text Full Text PDF PubMed Scopus (58) Google Scholar]HaematologicalMM (n = 77)Control (n = 24)GermanyPatient: 67 (60–72)Control: 66 (50.25–77.50)BNT162b21st dose: NA2nd dose: 53%1st dose:2nd dose: 100%[69.Enßle J.C. et al.Severe impairment of T-cell responses to BNT162b2 immunization in patients with multiple myeloma.Blood. 2022; 139: 137-142Crossref PubMed Scopus (11) Google Scholar]Solid cancer (n = 271)Haematological (n = 82)NAUKPatient: 59 (18–87)BNT162b2AZD1222Solid cancer 2nd dose: 96%Blood cancer 2nd dose: 70%NA[85.Fendler A. et al.Immune responses following third COVID-19 vaccination are reduced in patients with hematological malignancies compared to patients with solid cancer.Cancer Cell. 2022; 40: 114-116Abstract Full Text Full Text PDF PubMed Google Scholar]Solid cancer (n = 115)Haematological (n = 84)NAUKPatient: 63 (55–70)BNT162b2AZD1222OmicronSolid cancer 2nd dose: 37%Solid cancer 3rd dose: 90%Blood cancer 2nd dose: 19%Blood cancer 3rd: 56%DeltaSolid cancer 2nd dose: 56%Solid cancer 3rd dose:97%Blood cancer 2nd dose: 39%Blood cancer 3rd dose: 71%WTSolid cancer 2nd dose: 97%Solid cancer 3rd dose: 99%Blood cancer 2nd dose: 89%Blood cancer 3rd dose: 86%NA[86.Fendler A. et al.Omicron neutralising antibodies after third COVID-19 vaccine dose in patients with cancer.Lancet. 2022; 399: 905-907Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar]Solid cancer (n = 447)Haematological (n = 138)NAUKPatient: 60 (52–68)BNT162b2AZD1222Solid cancer1st dose: 44%2nd dose: 85%Haematological1st dose: 27%2nd dose: 59%NA[13.Fendler A. 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; 2: 1305-1320Crossref PubMed Scopus (0) Google Scholar]Solid cancer (n = 171)Haematological (n = 195)Control (n = 1245)USAPatient: 65 (56–63)Control: 38 (32–49)BNT162b2mRNA-1273Solid cancer1st dose: NA2nd dose: 96.9%Haematological1st dose: NA2nd dose: 81.9%NA[25.Figueiredo J.C. et al.Longitudinal SARS-CoV-2 mRNA vaccine-induced humoral immune responses in patients with cancer.Cancer Res. 2021; 81: 6273-6280Crossref PubMed Scopus (7) Google Scholar]Solid cancer (n = 94)Haematological (n = 56)NAItalyPatient: 68 (31–85)BNT162b21st dose: 61%2nd dose: 85.7%NA[108.Fong D. et al.High levels of anti-SARS-CoV-2 IgG antibodies in previously infected patients with cancer after a single dose of BNT 162b2 vaccine.Eur. J. Cancer. 2021; 154: 4-6Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar]Haematological (n = 58)WM, CLL, NHLControl (n = 213)GreecePatient: 75 (40–88)Control: 75 (61–95)BNT162b2AZD12221st dose: 14%1st dose: 54%[88.Gavriatopoulou M. et al.Low neutralizing antibody responses in WM, CLL and NHL patients after the first dose of the BNT162b2 and AZD1222 vaccine.Clin. Exp. Med. 2021; 22: 319-323Crossref PubMed Scopus (15) Google Scholar]B-cell lymphoma (n = 86)Control (n = 201)USAPatient (BCL): 72 (47–91)BNT162b2mRNA-1273Ad26.COV2.S1st dose:2nd dose: 41.9%1st dose:2nd dose: 100%[109.Ghione P. et al.Impaired humoral responses to COVID-19 vaccination in patients with lymphoma receiving B-cell-directed therapies.Blood. 2021; 138: 811-814Crossref PubMed Scopus (52) Google Scholar]Solid cancer (n = 232)Control (n = 261)IsraelPatient: 66 (SD = 12.09)BNT162b21st dose: 29%2nd dose: 86%1st dose: 84%2nd dose: NA[30.Goshen-Lago T. et al.Serologic status and toxic effects of the SARS-CoV-2 BNT162b2 vaccine in patients undergoing treatment for cancer.JAMA Oncol. 2021; 7: 1507Crossref PubMed Scopus (81) Google Scholar]Thoracic cancer (n = 306)Control (n = 18)FrancePatient: 67 (58–74)BNT162b2mRNA-1273AZD12221st dose: NA2nd dose: 93.7%1st dose: NA2nd dose: 100%[29.Gounant V. et al.Efficacy of severe acute respiratory syndrome coronavirus-2 vaccine in patients with thoracic cancer: a prospective study supporting a third dose in patients with minimal serologic response after two vaccine doses.J. Thorac. 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