Booster Doses of COVID-19 Vaccines for Patients with Haematological and Solid Cancer: a Systematic Review and Individual Patient Data Meta-analysis

Overview

Journal Eur J Cancer

Specialty Oncology

Date 2022 Jun 26

PMID 35753213

Authors

Aaron Shengting Mai

Ainsley Ryan Yan Bin Lee

Ryan Yong Kiat Tay

Lauren Shapiro

Astha Thakkar

Balazs Halmos

Albert Grinshpun

Yair Herishanu

Ohad Benjamini

Tamar Tadmor

Rachna T Shroff

Bonnie J LaFleur

Deepta Bhattacharya

Siyu Peng

Jeremy Tey

Soo Chin Lee

Louis Yi Ann Chai

Yu Yang Soon

Raghav Sundar

Matilda Xinwei Lee

Affiliations

Soon will be listed here.

Abstract

Importance: Patients with cancer have an increased risk of severe disease and mortality from COVID-19, as the disease and antineoplastic therapy cause reduced vaccine immunogenicity. Booster doses have been proposed to enhance protection, and efficacy data are emerging from several studies.

Objective: To evaluate the proportion of COVID-19 primary vaccination non-responders with cancer who seroconvert after a booster dose.

Methods: PubMed, EMBASE, CENTRAL and medRxiv were searched from 1st January 2021 to 10th March 2022. Quality was assessed using the Joanna Briggs Institute Critical Appraisal checklist.

Results: After the eligibility assessment, 22 studies were included in this systematic review and 17 for meta-analysis of seroconversion in non-responders, pooling a total of 849 patients with haematological cancer and 82 patients with solid cancer. Haematological cancer non-responders exhibited lower seroconversion at 44% (95% CI 36-53%) than solid cancer at 80% (95% CI 69-87%). Individual patient data meta-analysis found the odds of having a meaningful rise in antibody titres to be significantly associated with increased duration between the second and third dose (OR 1.02, 95% CI 1.00-1.03, P ≤ 0.05), age of patient (OR 0.960, 95% CI 0.934-0.987, P ≤ 0.05) and cancer type. With patients with haematological cancer as a reference, patients with lung cancer had 16.8 times the odds of achieving a meaningful increase in antibody titres (OR 16.8, 95% CI 2.95-318, P ≤ 0.05) and gastrointestinal cancer patients had 25.4 times the odds of achieving a meaningful increase in antibody titres (OR 25.4, 95% CI 5.26-492.21, P ≤ 0.05).

Conclusions: administration of a COVID-19 vaccine booster dose is effective in improving seroconversion and antibody levels. Patients with haematological cancer consistently demonstrate poorer response to booster vaccines than patients with solid cancer.

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References

Cho A, Bradley B, Kauffman R, Priyamvada L, Kovalenkov Y, Feldman R . Robust memory responses against influenza vaccination in pemphigus patients previously treated with rituximab. JCI Insight. 2017; 2(12). PMC: 5470882. DOI: 10.1172/jci.insight.93222. View

Ehmsen S, Asmussen A, Jeppesen S, Nilsson A, Osterlev S, Kragh A . Antibody responses following third mRNA COVID-19 vaccination in patients with cancer and potential timing of a fourth vaccination. Cancer Cell. 2022; 40(4):338-339. PMC: 8867110. DOI: 10.1016/j.ccell.2022.02.011. View

Canti L, Arien K, Desombere I, Humblet-Baron S, Pannus P, Heyndrickx L . Antibody response against SARS-CoV-2 Delta and Omicron variants after third-dose BNT162b2 vaccination in allo-HCT recipients. Cancer Cell. 2022; 40(4):335-337. PMC: 8847067. DOI: 10.1016/j.ccell.2022.02.005. View

Lee A, Wong S, Chai L, Lee S, Lee M, Muthiah M . Efficacy of covid-19 vaccines in immunocompromised patients: systematic review and meta-analysis. BMJ. 2022; 376:e068632. PMC: 8889026. DOI: 10.1136/bmj-2021-068632. View

Reimann P, Ulmer H, Mutschlechner B, Benda M, Severgnini L, Volgger A . Efficacy and safety of heterologous booster vaccination with Ad26.COV2.S after BNT162b2 mRNA COVID-19 vaccine in haemato-oncological patients with no antibody response. Br J Haematol. 2021; 196(3):577-584. DOI: 10.1111/bjh.17982. View

Rubin L, Levin M, Ljungman P, Davies E, Avery R, Tomblyn M . 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014; 58(3):309-18. DOI: 10.1093/cid/cit816. View

Bagacean C, Letestu R, Al-Nawakil C, Brichler S, Levy V, Sritharan N . Humoral response to mRNA anti-COVID-19 vaccines BNT162b2 and mRNA-1273 in patients with chronic lymphocytic leukemia. Blood Adv. 2021; 6(1):207-211. PMC: 8632355. DOI: 10.1182/bloodadvances.2021006215. View

Saini K, Tagliamento M, Lambertini M, McNally R, Romano M, Leone M . Mortality in patients with cancer and coronavirus disease 2019: A systematic review and pooled analysis of 52 studies. Eur J Cancer. 2020; 139:43-50. PMC: 7467090. DOI: 10.1016/j.ejca.2020.08.011. View

So A, McGrath H, Ting J, Srikandarajah K, Germanou S, Moss C . COVID-19 Vaccine Safety in Cancer Patients: A Single Centre Experience. Cancers (Basel). 2021; 13(14). PMC: 8304256. DOI: 10.3390/cancers13143573. View

10.

Saiag E, Grupper A, Avivi I, Elkayam O, Ram R, Herishanu Y . The effect of a third-dose BNT162b2 vaccine on anti-SARS-CoV-2 antibody levels in immunosuppressed patients. Clin Microbiol Infect. 2022; 28(5):735.e5-735.e8. PMC: 8853982. DOI: 10.1016/j.cmi.2022.02.002. View

11.

Marlet J, Gatault P, Maakaroun Z, Longuet H, Stefic K, Handala L . Antibody Responses after a Third Dose of COVID-19 Vaccine in Kidney Transplant Recipients and Patients Treated for Chronic Lymphocytic Leukemia. Vaccines (Basel). 2021; 9(10). PMC: 8539204. DOI: 10.3390/vaccines9101055. View

12.

Keam B, Kim M, Choi Y, Choi S, Choe P, Lee K . Optimal timing of influenza vaccination during 3-week cytotoxic chemotherapy cycles. Cancer. 2016; 123(5):841-848. DOI: 10.1002/cncr.30468. View

13.

Straub R, Miller L, Scholmerich J, Zietz B . Cytokines and hormones as possible links between endocrinosenescence and immunosenescence. J Neuroimmunol. 2000; 109(1):10-5. DOI: 10.1016/s0165-5728(00)00296-4. View

14.

Abid M, Rubin M, Ledeboer N, Szabo A, Longo W, Mohan M . Efficacy of a third SARS-CoV-2 mRNA vaccine dose among hematopoietic cell transplantation, CAR T cell, and BiTE recipients. Cancer Cell. 2022; 40(4):340-342. PMC: 8864440. DOI: 10.1016/j.ccell.2022.02.010. View

15.

Shroff R, Chalasani P, Wei R, Pennington D, Quirk G, Schoenle M . Immune responses to two and three doses of the BNT162b2 mRNA vaccine in adults with solid tumors. Nat Med. 2021; 27(11):2002-2011. PMC: 9004706. DOI: 10.1038/s41591-021-01542-z. View

16.

Herishanu Y, Rahav G, Levi S, Braester A, Itchaki G, Bairey O . Efficacy of a third BNT162b2 mRNA COVID-19 vaccine dose in patients with CLL who failed standard 2-dose vaccination. Blood. 2021; 139(5):678-685. PMC: 8648353. DOI: 10.1182/blood.2021014085. View

17.

Rivera D, Peters S, Panagiotou O, Shah D, Kuderer N, Hsu C . Utilization of COVID-19 Treatments and Clinical Outcomes among Patients with Cancer: A COVID-19 and Cancer Consortium (CCC19) Cohort Study. Cancer Discov. 2020; 10(10):1514-1527. PMC: 7541683. DOI: 10.1158/2159-8290.CD-20-0941. View

18.

Gounant V, Ferre V, Soussi G, Charpentier C, Flament H, Fidouh N . 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 Oncol. 2021; 17(2):239-251. PMC: 8593625. DOI: 10.1016/j.jtho.2021.10.015. View

19.

Fung M, Babik J . COVID-19 in Immunocompromised Hosts: What We Know So Far. Clin Infect Dis. 2021; 72(2):340-350. PMC: 7337668. DOI: 10.1093/cid/ciaa863. View

20.

Lee A, Wong S, Tay S . Booster COVID-19 Vaccines for Immune-Mediated Inflammatory Disease Patients: A Systematic Review and Meta-Analysis of Efficacy and Safety. Vaccines (Basel). 2022; 10(5). PMC: 9144569. DOI: 10.3390/vaccines10050668. View