Interval between prior SARS-CoV-2 infection and booster vaccination impacts magnitude and quality of antibody and B cell responses

Buckner, Clarisa M.; Kardava, Lela; Merhebi, Omar El; Narpala, Sandeep; Serebryannyy, Leonid A.; Lin, Bob C.; Wang, Wei; Zhang, Xiaozhen; Assis, Felipe Lopes de; Kelly, Sophie E.M.; Teng, I-Ting; McCormack, Genevieve; Praiss, Lauren H.; Seamon, Catherine; Ali, M. Showkat; Kalish, Heather; Kwong, Peter D.; Proschan, Michael A.; McDermott, Adrian B.; Fauci, Anthony S.; Chun, Tae‐Wook; Moir, Susan

doi:10.1016/j.cell.2022.09.032

Cited by 40 publications

(38 citation statements)

References 38 publications

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“…Besides the RBD, antibodies targeting other regions of the spike, such as the NTD or S2 region may also broaden the humoral response 60,61 . The interval between prior SARS-CoV-2 infection and booster vaccination impacts magnitude and quality of antibody and B cell responses 62 . This raises important questions regarding the frequency of booster doses, particularly in the presence of Omicron variants with greater immune evasion properties.…”

Section: Discussionmentioning

confidence: 99%

Resistance of Omicron subvariants BA.2.75.2, BA.4.6 and BQ.1.1 to neutralizing antibodies

Planas

Bruel

Staropoli

et al. 2022

Preprint

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Convergent evolution of SARS-CoV-2 Omicron BA.2, BA.4 and BA.5 lineages has led to the emergence of several new subvariants, including BA.2.75.2, BA.4.6. and BQ.1.1. The subvariants BA.2.75.2 and BQ.1.1 are expected to become predominant in many countries in November 2022. They carry an additional and often redundant set of mutations in the spike, likely responsible for increased transmissibility and immune evasion. Here, we established a viral amplification procedure to easily isolate Omicron strains. We examined their sensitivity to 6 therapeutic monoclonal antibodies (mAbs) and to 72 sera from Pfizer BNT162b2-vaccinated individuals, with or without BA.1/BA.2 or BA.5 breakthrough infection. Ronapreve (Casirivimab and Imdevimab) and Evusheld (Cilgavimab and Tixagevimab) lost any antiviral efficacy against BA.2.75.2 and BQ.1.1, whereas Xevudy (Sotrovimab) remained weakly active. BQ.1.1 was also resistant to Bebtelovimab. Neutralizing titers in triply vaccinated individuals were low to undetectable against BQ.1.1 and BA.2.75.2, 4 months after boosting. A BA.1/BA.2 breakthrough infection increased these titers, which remained about 18-fold lower against BA.2.75.2 and BQ.1.1, than against BA.1. Reciprocally, a BA.5 breakthrough infection increased more efficiently neutralization against BA.5 and BQ.1.1 than against BA.2.75.2. Thus, the evolution trajectory of novel Omicron subvariants facilitated their spread in immunized populations and raises concerns about the efficacy of most currently available mAbs.

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Section: Discussionmentioning

confidence: 99%

Resistance of Omicron subvariants BA.2.75.2, BA.4.6 and BQ.1.1 to neutralizing antibodies

Planas

Bruel

Staropoli

et al. 2022

Preprint

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“…Our findings are in line with a recent study that reported the quality and magnitude of immune responses (antibodies and B cells) to be higher if the interval between infection and booster vaccination is longer (>180 days). 40 It may therefore be reasonable for individuals with a prior infection and full primary series vaccination to delay subsequent doses of vaccination by six months, while still maintaining high levels of protection against infection and severe disease. That said, pre-vaccination screening for past infections is currently not recommended by WHO 41 , similar to other mass vaccination programmes (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…Nine studies reported information on the sequence of immunological challenges, however there was insufficient data for analysis as the data were split across different types of exposures (e.g., HE with different numbers of vaccine doses) and sequence permutations. Data from studies measuring neutralizing antibodies suggest that the sequence and timing of immunological challenges may interact with the level of protection conferred 40,47 , but further studies are needed to inform policy making. Third, there was limited data for estimates of sublineage-specific protection for the distinct Omicron subvariants, such as BA.1, BA.2 or BA.5.…”

Section: Discussionmentioning

confidence: 99%

Protective effectiveness of prior SARS-CoV-2 infection and hybrid immunity against Omicron infection and severe disease: a systematic review and meta-regression

Bobrovitz

Ware

et al. 2022

Preprint

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Background We aimed to systematically review the magnitude and duration of the protective effectiveness of prior infection (PE) and hybrid immunity (HE) against Omicron infection and severe disease. Methods We searched pre-print and peer-reviewed electronic databases for controlled studies from January 1, 2020, to June 1, 2022. Risk of bias (RoB) was assessed using the Risk of Bias In Non-Randomized Studies of Interventions (ROBINS-I)-Tool. We used random-effects meta-regression to estimate the magnitude of protection at 1-month intervals and the average change in protection since the last vaccine dose or infection from 3 months to 6 or 12 months. We compared our estimates of PE and HE to previously published estimates of the magnitude and durability of vaccine effectiveness (VE) against Omicron. Findings Eleven studies of prior infection and 15 studies of hybrid immunity were included. For prior infection, there were 97 estimates (27 at moderate RoB and 70 at serious RoB), with the longest follow up at 15 months. PE against hospitalization or severe disease was 82.5% [71.8-89.7%] at 3 months, and 74.6% [63.1-83.5%] at 12 months. PE against reinfection was 65.2% [52.9-75.9%] at 3 months, and 24.7% [16.4-35.5%] at 12 months. For HE, there were 153 estimates (78 at moderate RoB and 75 at serious RoB), with the longest follow up at 11 months for primary series vaccination and 4 months for first booster vaccination. Against hospitalization or severe disease, HE involving either primary series vaccination or first booster vaccination was consistently >95% for the available follow up. Against reinfection, HE involving primary series vaccination was 69.0% [58.9-77.5%] at 3 months after the most recent infection or vaccination, and 41.8% [31.5-52.8%] at 12 months, while HE involving first booster vaccination was 68.6% [58.8-76.9%] at 3 months, and 46.5% [36.0-57.3%] at 6 months. Against hospitalization or severe disease at 6 months, hybrid immunity with first booster vaccination (effectiveness 95.3% [81.9-98.9%]) or with primary series alone (96.5% [90.2-98.8%]) provided significantly greater protection than prior infection alone (80.1% [70.3-87.2%]), first booster vaccination alone (76.7% [72.5-80.4%]), or primary series alone (64.6% [54.5-73.6%]). Results for protection against reinfection were similar. Interpretation Prior infection and hybrid immunity both provided greater and more sustained protection against Omicron than vaccination alone. All protection estimates waned quickly against infection but remained high for hospitalisation or severe disease. Individuals with hybrid immunity had the highest magnitude and durability of protection against all outcomes, reinforcing the global imperative for vaccination.

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“…Converging evidence indicates that the time since vaccination/infection as well as the infecting variant dictate the level and quality of immune responses to mRNA boosters vaccination (70, 79). Ongoing affinity maturation shapes immune responses elicited by infection (82, 92–95) and by vaccine boosters, including those based on the original Wuhan strain (37, 40, 41, 82, 84, 86, 87).…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, BA.2-elicited immunity confers cross-protection against BA.5 (16, 64, 77) and BA.2-offspring (16, 64, 77), emphasizing the beneficial impact of reactivation of NAbs targeting common epitopes. Importantly however, mixed immunity resulting from Omicron BA.1-and BA-2-breakthrough infections after 2 or 3 first generation vaccine doses or from reinfection after a first infection with a pre-Omicron strain or from bivalent vaccines combining wild-type + Omicron BA.1, wildtype + Omicron BA.4/5, Delta + Omicron BA.1 or hybrid Omicron BA.1/Delta determinants, all elicit superior NAb as well as T-cell responses against all Omicron sublineages and against pre-Omicron VOCs and confer better protection against severe forms of COVID-19 compared to boosters based on the original Wuhan strain or pre-Omicron (Beta or Delta) (3, 5, 16, 20, 38, 42, 53, 66, 67, 73, 75, 76, 78, 79). Accordingly, second generation bivalent vaccines combining ancestral and Omicron sequences (generally BA.1 or BA.4/BA.5) have been approved by the EMA and FDA in September 2022 as boosters after first generation vaccines based on the original Wuhan strain.…”

Section: Introductionmentioning

confidence: 99%

Vaccine- and BTI-elicited pre-Omicron immunity more effectively neutralizes Omicron sublineages BA.1, BA.2, BA.4 and BA.5 than pre-Omicron infection alone

Silva

Servais

Kohnen

et al. 2022

Preprint

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Since the emergence of SARS-CoV-2 Omicron BA.1 and BA.2, several Omicron sublineages have emerged, supplanting their predecessors. BA.5 is the current dominant sublineage. Here we compared the neutralization of Omicron sublineages BA.1, BA.2, BA.4 and BA.5 by human sera collected from individuals who were infected with the ancestral B.1 (D614G) strain, vaccinated (3 doses), or with hybrid immunity from vaccination (2 doses) followed by pre-Omicron breakthrough infection (BTI) with Gamma or Delta. All Omicron sublineages exhibited extensive escape from all sera compared to the ancestral B.1 strain and to Delta, albeit to different levels depending on the origin of the sera. Convalescent sera were unable to neutralize BA.1, and partly neutralized BA.2, BA.4 and BA.5. Vaccinee sera partly neutralized BA.2, but BA.1, BA.4 and BA.5 evaded neutralizing antibodies. BTI sera were either non-neutralizing or partially neutralizing. In this case, they had similar neutralizing ability against all Omicron sublineages. Despite similar levels of anti-Spike and anti-Receptor Binding Domain (RBD) antibody in all groups, BTI sera had the highest cross-neutralizing ability against all Omicron sublineages and convalescent sera were the least neutralizing. The NT50:antibody titer ratio, which reflects antibody avidity, was significantly higher in sera from BTI patients compared to convalescent sera, underscoring qualitative differences in antibodies elicited by infection alone and by vaccination. Together these findings highlight the importance of vaccination to trigger highly cross-reactive antibodies that neutralize phylogenetically and antigenically distant strains, and suggest that immune imprinting by first generation vaccines may restrict, but not abolish cross-neutralization.

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Interval between prior SARS-CoV-2 infection and booster vaccination impacts magnitude and quality of antibody and B cell responses

Cited by 40 publications

References 38 publications

Resistance of Omicron subvariants BA.2.75.2, BA.4.6 and BQ.1.1 to neutralizing antibodies

Resistance of Omicron subvariants BA.2.75.2, BA.4.6 and BQ.1.1 to neutralizing antibodies

Protective effectiveness of prior SARS-CoV-2 infection and hybrid immunity against Omicron infection and severe disease: a systematic review and meta-regression

Vaccine- and BTI-elicited pre-Omicron immunity more effectively neutralizes Omicron sublineages BA.1, BA.2, BA.4 and BA.5 than pre-Omicron infection alone

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