Immunogenicity of COVID-19 vaccines in solid organ transplant recipients: a systematic review and meta-analysis

Abstract

Background: Solid organ transplant (SOT) recipients are at increased risks of morbidity and mortality associated with COVID-19.

Objectives: This study aimed to evaluate the immunogenicity of COVID-19 vaccines in SOT recipients.

Data sources: Electronic databases were searched for eligible reports published from 1 December 2019 to 31 May 2022.

Study eligibility criteria: We included reports evaluating the humoral immune response (HIR) or cellular immune response rate in SOT recipients after the administration of COVID-19 vaccines.

Participants: SOT recipients who received COVID-19 vaccines.

Assessment of risk of bias: We used the Newcastle-Ottawa scale to assess bias in case-control and cohort studies. For randomised-controlled trials, the Jadad Scale was used.

Methods: We used a random-effects model to calculate the pooled rates of immune response with 95% CI. We used a risk ratio (RR) with 95% CI for a comparison of immune responses between SOT and healthy controls.

Results: A total of 91 reports involving 11 886 transplant recipients (lung: 655; heart: 539; liver: 1946; and kidney: 8746) and 2125 healthy controls revealed pooled HIR rates after the 1st, 2nd, and 3rd COVID-19 vaccine doses in SOT recipients were 9.5% (95% CI, 7-11.9%), 43.6% (95% CI, 39.3-47.8%) and 55.1% (95% CI, 44.7-65.6%), respectively. For specific organs, the HIR rates were still low after 1st vaccine dose (lung: 4.4%; kidney: 9.4%; heart: 13.2%; liver: 29.5%) and 2nd vaccine dose (lung: 28.4%; kidney: 37.6%; heart: 50.3%; liver: 64.5%).

Conclusions: A booster vaccination enhances the immunogenicity of COVID-19 vaccines in SOT; however, a significant share of the recipients still has not built a detectable HIR after receiving the 3rd dose. This finding calls for alternative approaches, including the use of monoclonal antibodies. In addition, lung transplant recipients need urgent booster vaccination to improve the immune response.

Keywords: COVID-19 vaccines; Immune response; Immunogenicity; Meat-analysis; Solid organ transplant.

Graphical abstract

Fig. 1

Flow diagram of the study selection process.

Fig. 2

Meta-analysis of the HIR after 1st, 2nd, and 3rd doses COVID-19 vaccine in SOT recipients and comparison of HIR. (A) HIR after 1st vaccine dose in SOT (9.5%); (B) HIR after 2nd vaccine dose in SOT (43.6%); (C) HIR after 3rd vaccine dose in SOT (55.1%); (D) Comparison of HIR after 1st vaccine dose (SOT vs. healthy controls, RR = 0.036); (E) Comparison of HIR after 2nd vaccine dose (SOT vs. healthy controls, RR = 0.382). HIR, humoral immune response; SOT, solid organ transplant; RR, risk ratio.

Fig. 3

Meta-analysis of the CIR after 1st, 2nd, and 3rd doses COVID-19 vaccine in SOT recipients. (A) CIR after 1st dose in SOT (12.2%); (B) CIR after 2nd dose in SOT (48.3%); (C) CIR after 3rd dose in SOT (57.6%); (D) Comparison of CIR after 2nd dose (SOT vs. healthy controls, RR = 0.477). CIR, cellular immune response; SOT, solid organ transplant; RR, risk ratio.

Fig. 4

Meta-analysis of the HIR and CIR after 1st, 2nd, and 3rd COVID-19 vaccine doses in different types of transplant recipients. (A) HIR in LUT (1st dose: 4.4%, 2nd dose:28.4%), HT (1st dose: 13.2%, 2nd dose: 50.3%), LIT (1st dose: 29.5%, 2nd dose: 64.5%) and KT (1st dose: 9.4%, 2nd dose: 37.6%, 3rd dose: 54.4%); (B) CIR in LIT (2nd dose: 66.3%) and KT (1st dose: 6.9%, 2nd dose: 42.6%, 3rd dose: 57.6%). HIR, humoral immune response; CIR, cellular immune response; KT, kidney transplant; LIT, liver transplant; HT, heart transplant; LUT, lung transplant.