Global Statistics

All countries
531,352,960
Confirmed
Updated on May 28, 2022 10:09 pm
All countries
487,788,350
Recovered
Updated on May 28, 2022 10:09 pm
All countries
6,310,323
Deaths
Updated on May 28, 2022 10:09 pm
Saturday, May 28, 2022

Global Statistics

All countries
531,352,960
Confirmed
Updated on May 28, 2022 10:09 pm
All countries
487,788,350
Recovered
Updated on May 28, 2022 10:09 pm
All countries
6,310,323
Deaths
Updated on May 28, 2022 10:09 pm
Molderizer and Safe Shield

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Search results and characteristics of included studies

As of March 7, 2022, the literature search initially identified 14,571 articles. We then selected articles according to the defined inclusion and exclusion criteria. Figure 1 depicts the process of study selection and reasons for exclusions. A total of 4212 duplicate articles in different databases were removed. We screened the title and abstract of the remaining articles and excluded ineligible articles. Finally, 52 full-text articles were further assessed for eligibility. Twenty-two studies were not included in our review because they don’t use the heterologous prime-boost vaccination. Five studies without mRNA or adenoviral vectored COVID-19 vaccine, six studies without homologous prime-boost COVID-19 vaccination as control groups, one study without immunogenicity, one with a sample size less than ten, one with a pre-existing clinical disease, one review, one case report, and one animal study were excluded, respectively.

Fig. 1
figure 1

Finally, 13 studies [12,13,14,15, 21,22,23,24,25,26,27,28,29] from 52 articles were identified that fulfilled our inclusion and exclusion criteria, Nine studies were conducted in Germany [12, 13, 15, 2124, 26, 27] two in UK [14, 29], and two in France [25, 28]. Of these studies, 12 were observational studies [12, 13, 15, 21,22,23,24,25,26,27,28,29] and one was randomized trial [14]. All studies involved ChAd/BNT (mRNA-1273) schedule and two study involved BNT/ChAd schedule [14, 24]. The characteristics of the included studies are summarized in Table 1.

Table 1 Main characteristics of included studies and subjects

The quality assessment scores for included cohorts are shown in Additional file 1: Table S1. Overall, four high-quality cohort studies [22, 25, 28, 29] and eight fair-quality cohort studies [12, 13, 15, 21, 23, 26, 27, 30] were included in this systematic review. The randomized trial [14] was considered to have a low risk of bias.

Characteristics of various prime-boost vaccination strategies

In this systematic review, prime-boost vaccination schedules include ChAd/BNT (mRNA-1273) and BNT/ChAd. All studies involved ChAd/BNT (mRNA-1273) heterologous schedule and had BNT/BNT (mRNA-1273) as the control group, and meanwhile, ten of which also had ChAd/ChAd as the control group [12,13,14,15, 21, 23, 24, 26, 27, 29].

Effect of immunogenicity with heterologous strategy on outcomes

ChAd/BNT(mRNA-1273) vs BNT/BNT

Thirteen studies [12,13,14,15, 21,22,23,24,25,26,27,28,29] involved 14 times of comparisons between ChAd/BNT(mRNA-1273) heterologous schedule and homologous BNT/BNT (mRNA-1273/mRNA-1273), four of them studies reported comparative efficacy on anti-RBD IgG and all of them did not find significant difference on this outcome [13, 21, 25, 26]. Eight studies [12,13,14, 21, 22, 25, 28, 29] reported comparative effectiveness on anti-S protein IgG, seven of them [12,13,14, 21, 25, 28, 29] showed comparable efficacy on this indicator, and one of them [22] found that ChAd/BNT induced higher cumulative anti-spike-IgM and IgG concentrations. Ten studies [13,14,15, 21,22,23,24,25,26,27] supplied 11 times of comparison on neutralizing antibody, six of them [13, 15, 22, 25,26,27] with seven times of comparison found that ChAd/BNT(mRNA-1273) heterologous schedule could induce better response on neutralizing antibody involving against B.1.351 variant and B.1.1.7 variant, two of them [14, 21] found similar response, and two of them [23, 24] found a lower reciprocal titres of neutralizing antibody against Delta variant. Four studies [13, 15, 25, 26] explored spike-specific IFN-γ secretion, three of them [13, 15, 26] discovered that heterologous ChAd/BNT(mRNA-1273) immunisation could induce higher spike-specific IFN-γ secretion, and one of them found similar whole-blood IFN-γ [25] (Table 2). In conclusion, it seemed that the majority of studies indicated heterologous ChAd/BNT(mRNA-1273) immunisation schedule induced superior or at least comparable humoral and cellular response against SARS-CoV-2 compared with homologous BNT/BNT immunisation schedule, while definite conclusion has yet been reached on the response against variants.

Table 2 Comparison of different prime-boost immunization strategies on immunogenicity in included studies

ChAd/BNT(mRNA-1273) vs ChAd/ChAd

Of the ten studies [12,13,14,15, 21, 23, 24, 26, 27, 29] involved ChAd/BNT (mRNA-1273) heterologous schedule with homologous ChAd/ChAd as a control group, two studies [13, 26] reported comparative efficacy on anti-RBD IgG, one of which showed similar and another showed higher RBD IgG in ChAd/BNT(mRNA-1273) groups compared with that in homologous ChAd/ChAd groups. Six studies [12, 14, 15, 21, 26, 29] reported comparative efficacy on anti-S protein IgG, all of which showed a higher anti-S IgG level in ChAd/BNT (mRNA-1273) groups compared with that in homologous ChAd/ChAd groups. Nine studies [12,13,14,15, 21, 23, 24, 26, 27] reported comparative efficacy on neutralizing antibody and found better responses in ChAd/BNT (mRNA-1273) groups compared with homologous ChAd/ChAd groups; especially, two study [15, 24] found that ChAd/BNT (mRNA-1273) heterologous schedule could induce better response on neutralizing antibody capacities against B.1.351 variant, B.1.1.7 variant, or P.1 variant compared with that in homologous ChAd/ChAd groups. Four studies [12, 13, 15, 26] explored spike-specific T-cell-mediated immune response and all of them [12, 13, 15, 26] indicated that heterologous ChAd/BNT(mRNA-1273) could induce higher spike-specific IFN-γ secretion compared with homologous ChAd/ChAd groups (Table 2). Overall, heterologous ChAd/BNT (mRNA-1273) immunisation schedule induced superior humoral and cellular response against SARS-CoV-2 compared with homologous ChAd/ChAd immunisation schedule.

BNT/ ChAd vs BNT/BNT or ChAd/ChAd

Two studies [14, 29] investigated the difference of specific immune response between heterologous BNT/ChAd and homologous BNT/BNT vaccination, one of which found that heterologous BNT/ChAd induced inferior anti-S IgG and neutralizing antibody while similar T cell response compared with homologous BNT/BNT vaccination, the other found similar response in anti-S rotein IgG. Meanwhile, the two studies also compared the immune response between heterologous BNT/ChAd and homologous ChAd/ChAd vaccination, both of which found heterologous BNT/ChAd schedule induced higher anti-S IgG and one study also found heterologous BNT/ChAd schedule induced higher neutralizing antibody compared with homologous ChAd/ChAd schedule (Table 2).

Adverse events with heterologous strategy on outcomes

Four studies [13, 14, 21, 26] compared AEs incidences between heterologous ChAd/BNT (mRNA-1273) and homologous BNT/BNT or ChAd/ChAd vaccination. All of them used standardized questionnaires to collected AEs after vaccination (Additional file 1: Table S2). We conducted a meta-analysis to compare the frequencies of any reaction, local reaction and systemic reaction after prime-boost vaccination. There was a similar risk of any reaction (RR = 1.30, 95% CI: 0.86−1.96, I2 = 78%) while a higher risk of local reactions (RR = 1.65, 95% CI: 1.27−2.15, I2 = 45%) and systemic reactions (RR = 1.49, 95% CI: 1.17−1.90, I2 = 0%; Fig. 2A) in heterologous ChAd/BNT (mRNA-1273) groups compared with that in homologous ChAd/ChAd group. Similarly, there was a higher risk of local reactions (RR = 1.16, 95% CI: 1.03−1.31, I2 = 12%) in heterologous ChAd/BNT (mRNA-1273) vaccination compared with homologous BNT/BNT but similar risk of any reaction (RR = 1.03, 95% CI: 0.79−1.34, I2 = 80%) and systemic reactions (RR = 0.89, 95% CI: 0.60−1.30, I2 = 84%; Fig. 2B). One study reported the frequencies of severe adverse events (SAE) were 9.5% in ChAd/ChAd, 11.3% in ChAd/BNT, 1.2% in BNT/BNT, and 7.8% in BNT/ChAd, respectively [14]. Another study reported the frequencies of severe local adverse events were 4% in BNT/BNT, 3% in ChAd/ChAd, and 7% in ChAd/BNT, respectively; the frequencies of severe systemic adverse events were 6% in BNT/BNT, 6% in ChAd/ChAd, and 2% in ChAd/BNT, respectively [13]. However, statistic tests were not conducted in the frequencies of SAE between heterologous and homologous vaccination in the two studies. Based on these crude data, the frequencies of SAE seemed to be comparable between heterologous and homologous vaccination.

Fig. 2
figure 2

Estimates of risk ratio of reactions stratified by any, local, and systematic reactions. Figure shows the risk ratio of any, local, and systemic events in participants who received heterologous ChAd/BNT schedule compared with those in homologous ChAd/ChAd (A) and the risk ratio of any, local, and systemic events in participants who received heterologous ChAd/BNT schedule compared with those in homologous BNT/BNT (B). BNT BNT162b2 vaccine, Pfizer–BioNTech, ChAd ChAdOx1 nCoV-19 vaccine, AstraZeneca, CI confidence intervals, RR risk ratio

Heterogeneity

The P value for Cochrane’s Q test suggested high heterogeneity across studies for ChAd/BNT (mRNA-1273) vs BNT/BNT strategy in the assessment of any events and systematic and studies for ChAd/BNT (mRNA-1273) vs ChAd/ChAd strategy in any events assessment (P < 0.01, Fig. 2). Potential publication bias was not assessed because the number of studies was small (< 10) in all of the above meta-analyses.



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