Efficacy and Safety of COVID-19 Vaccines for Patients with Solid Cancer: A Systematic Review and Meta-Analysis
Main Article Content
Abstract
This systematic review and meta-analysis compared the efficacy and safety of COVID-19 vaccines between solid cancer patients and general people. We searched five electronic databases on July 18, 2021. The inclusion criteria for a study were: i) solid cancer patients; ii) receiving at least one dose of COVID-19 vaccine; iii) reporting of anti-spike(S) IgG seropositivity rates (primary outcome) and other efficacy and safety outcomes; and iv) comparing the outcomes between solid cancer patients and general people or within solid cancer patients. We assessed the study quality and pooled the outcomes using relative risks (RRs) and 95% confidence intervals (95% CIs). This review included ten studies, seven for meta-analyses. Almost all participants received the BNT162b2 vaccine. In comparison to the controls’ anti-S IgG seropositivity rates, those of solid cancer patients were significantly lower after the first vaccination (RR = 0.46, 95% CI 0.37 to 0.57) and slightly lower (RR = 0.94, 95% CI 0.91 to 0.96) after the second vaccination. In conclusion, the BNT162b2 vaccine is relatively safe for solid cancer patients. These patients may have a lower seropositivity rate after the first vaccination. However, the seropositivity rate increases considerably and is comparable to general people after the second vaccination.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
© Journal of Asian Medical Students’ Association (JAMSA). Released under a Creative Commons license.
References
Johns Hopkins University of Medicine Coronavirus Resource Center. COVID-19 Map. Johns Hopkins Coronavirus Resource Center n.d. https://coronavirus.jhu.edu/map.html (accessed July 14, 2021).
World Health Organization. WHO lists additional COVID-19 vaccine for emergency use and issues interim policy recommendations n.d. https://www.who.int/news/item/07-05-2021-who-lists-additional-covid-19-vaccine-for-emergency-use-and-issues-interim-policy-recommendations (accessed July 14, 2021).
Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, et al. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N Engl J Med 2021;384:403–16. https://doi.org/10.1056/NEJMoa2035389.
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;383:2603–15. https://doi.org/10.1056/NEJMoa2034577.
Voysey M, Clemens SAC, Madhi SA, Weckx LY, Folegatti PM, Aley PK, 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. The Lancet 2021;397:99–111. https://doi.org/10.1016/S0140-6736(20)32661-1.
Sadoff J, Gray G, Vandebosch A, Cárdenas V, Shukarev G, Grinsztejn B, et al. Safety and Efficacy of Single-Dose Ad26.COV2.S Vaccine against Covid-19. New England Journal of Medicine 2021;384:2187–201. https://doi.org/10.1056/NEJMoa2101544.
Shi C, Wang L, Ye J, Gu Z, Wang S, Xia J, et al. Predictors of mortality in patients with coronavirus disease 2019: a systematic review and meta-analysis. BMC Infect Dis 2021;21:663. https://doi.org/10.1186/s12879-021-06369-0.
Tian J, Yuan X, Xiao J, Zhong Q, Yang C, Liu B, et al. Clinical characteristics and risk factors associated with COVID-19 disease severity in patients with cancer in Wuhan, China: a multicentre, retrospective, cohort study. Lancet Oncol 2020;21:893–903. https://doi.org/10.1016/S1470-2045(20)30309-0.
Bakouny Z, Hawley JE, Choueiri TK, Peters S, Rini BI, Warner JL, et al. COVID-19 and Cancer: Current Challenges and Perspectives. Cancer Cell 2020;38:629–46. https://doi.org/10.1016/j.ccell.2020.09.018.
Yekedüz E, Utkan G, Ürün Y. A systematic review and meta-analysis: the effect of active cancer treatment on severity of COVID-19. Eur J Cancer 2020;141:92–104. https://doi.org/10.1016/j.ejca.2020.09.028.
Robilotti EV, Babady NE, Mead PA, Rolling T, Perez-Johnston R, Bernardes M, et al. Determinants of COVID-19 disease severity in patients with cancer. Nat Med 2020;26:1218–23. https://doi.org/10.1038/s41591-020-0979-0.
Thakkar A, Gonzalez-Lugo JD, Goradia N, Gali R, Shapiro LC, Pradhan K, et al. Seroconversion rates following COVID-19 vaccination among patients with cancer. Cancer Cell 2021:S1535-6108(21)00285-3. https://doi.org/10.1016/j.ccell.2021.06.002.
Addeo A, Shah PK, Bordry N, Hudson RD, Albracht B, Di Marco M, et al. Immunogenicity of SARS-CoV-2 messenger RNA vaccines in patients with cancer. Cancer Cell 2021:S1535-6108(21)00330-5. https://doi.org/10.1016/j.ccell.2021.06.009.
Palich R, Veyri M, Vozy A, Marot S, Gligorov J, Benderra M-A, 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 Oncol 2021:S0923-7534(21)02075-5. https://doi.org/10.1016/j.annonc.2021.06.018.
Barrière J, Gal J, Hoch B, Cassuto O, Leysalle A, Chamorey E, et al. Acceptance of SARS-CoV-2 vaccination among French patients with cancer: a cross-sectional survey. Ann Oncol 2021;32:673–4. https://doi.org/10.1016/j.annonc.2021.01.066.
Di Noia V, Renna D, Barberi V, Di Civita M, Riva F, Costantini G, et al. The first report on coronavirus disease 2019 (COVID-19) vaccine refusal by patients with solid cancer in Italy: Early data from a single-institute survey. Eur J Cancer 2021:S0959-8049(21)00310-5. https://doi.org/10.1016/j.ejca.2021.05.006.
Higgins J, Thomas J, Chandler J, Cumpston M, Li T, Page M, et al. Cochrane Handbook for Systematic Reviews of Interventions. 2nd Edition. Chichester (UK): John Wiley & Sons; 2019.
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.org/10.1136/bmj.n71.
Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses n.d. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (accessed July 18, 2020).
Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Medical Research Methodology 2014;14:135. https://doi.org/10.1186/1471-2288-14-135.
RStudio Team. RStudio: Integrated Development Environment for R. Boston, MA: RStudio, Inc.; 2020.
Balduzzi S, Rücker G, Schwarzer G. How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health 2019;22:153–60. https://doi.org/10.1136/ebmental-2019-300117.
R Core Team. A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria: 2021.
Guyatt GH, Oxman AD, Schünemann HJ, Tugwell P, Knottnerus A. GRADE guidelines: a new series of articles in the Journal of Clinical Epidemiology. J Clin Epidemiol 2011;64:380–2. https://doi.org/10.1016/j.jclinepi.2010.09.011.
Barrière J, Chamorey E, Adjtoutah Z, Castelnau O, Mahamat A, Marco S, et al. Impaired immunogenicity of BNT162b2 anti-SARS-CoV-2 vaccine in patients treated for solid tumors. Ann Oncol 2021:S0923-7534(21)01183-2. https://doi.org/10.1016/j.annonc.2021.04.019.
Goshen-Lago T, Waldhorn I, Holland R, Szwarcwort-Cohen M, Reiner-Benaim A, Shachor-Meyouhas Y, et al. Serologic Status and Toxic Effects of the SARS-CoV-2 BNT162b2 Vaccine in Patients Undergoing Treatment for Cancer. JAMA Oncol 2021. https://doi.org/10.1001/jamaoncol.2021.2675.
Iacono D, Cerbone L, Palombi L, Cavalieri E, Sperduti I, Cocchiara RA, et al. Serological response to COVID-19 vaccination in patients with cancer older than 80 years. J Geriatr Oncol 2021:S1879-4068(21)00136-3. https://doi.org/10.1016/j.jgo.2021.06.002.
Massarweh A, Eliakim-Raz N, Stemmer A, Levy-Barda A, Yust-Katz S, Zer A, et al. Evaluation of Seropositivity Following BNT162b2 Messenger RNA Vaccination for SARS-CoV-2 in Patients Undergoing Treatment for Cancer. JAMA Oncol 2021. https://doi.org/10.1001/jamaoncol.2021.2155.
Monin L, Laing AG, Muñoz-Ruiz M, McKenzie DR, Del Molino Del Barrio I, Alaguthurai T, 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;22:765–78. https://doi.org/10.1016/S1470-2045(21)00213-8.
Palich R, Veyri M, Marot S, Vozy A, Gligorov J, Maingon P, et al. Weak immunogenicity after a single dose of SARS-CoV-2 mRNA vaccine in treated cancer patients. Ann Oncol 2021:S0923-7534(21)01184-4. https://doi.org/10.1016/j.annonc.2021.04.020.
Shroff RT, Chalasani P, Wei R, Pennington D, Quirk G, Schoenle MV, et al. Immune Responses to COVID-19 mRNA Vaccines in Patients with Solid Tumors on Active, Immunosuppressive Cancer Therapy. MedRxiv 2021:2021.05.13.21257129. https://doi.org/10.1101/2021.05.13.21257129.
Terpos E, Zagouri F, Liontos M, Sklirou AD, Koutsoukos K, Markellos C, et al. Low titers of SARS-CoV-2 neutralizing antibodies after first vaccination dose in cancer patients receiving checkpoint inhibitors. J Hematol Oncol 2021;14:86. https://doi.org/10.1186/s13045-021-01099-x.
Waissengrin B, Agbarya A, Safadi E, Padova H, Wolf I. Short-term safety of the BNT162b2 mRNA COVID-19 vaccine in patients with cancer treated with immune checkpoint inhibitors. Lancet Oncol 2021;22:581–3. https://doi.org/10.1016/S1470-2045(21)00155-8.
Meerveld-Eggink A, de Weerdt O, van der Velden AMT, Los M, van der Velden AWG, Stouthard JML, et al. Response to influenza virus vaccination during chemotherapy in patients with breast cancer. Ann Oncol 2011;22:2031–5. https://doi.org/10.1093/annonc/mdq728.
Rydyznski Moderbacher C, Ramirez SI, Dan JM, Grifoni A, Hastie KM, Weiskopf D, et al. Antigen-Specific Adaptive Immunity to SARS-CoV-2 in Acute COVID-19 and Associations with Age and Disease Severity. Cell 2020;183:996-1012.e19. https://doi.org/10.1016/j.cell.2020.09.038.