Distinguishing the Vaccine Effectiveness of Inactivated BBIBP-CorV Vaccine Booster Against the Susceptibility, Infectiousness, and Transmission of Omicron Stains: A Retrospective Cohort Study in Urumqi, China

Zeng, Ting; Wang, Kailu; Guo, Zihao; Sun, Shengzhi; Zhai, Ziyu; Lu, Yaoqin; Teng, Zhidong; He, Daihai; Wang, Kai; Tian, Maozai; Zhao, Shi

doi:10.1007/s40121-023-00873-3

Distinguishing the Vaccine Effectiveness of Inactivated BBIBP-CorV Vaccine Booster Against the Susceptibility, Infectiousness, and Transmission of Omicron Stains: A Retrospective Cohort Study in Urumqi, China

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Published: 28 September 2023

Volume 12, pages 2405–2416, (2023)
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Distinguishing the Vaccine Effectiveness of Inactivated BBIBP-CorV Vaccine Booster Against the Susceptibility, Infectiousness, and Transmission of Omicron Stains: A Retrospective Cohort Study in Urumqi, China

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Ting Zeng¹^na1,
Kailu Wang²^na1,
Zihao Guo²^na1,
Shengzhi Sun³,
Ziyu Zhai⁴,
Yaoqin Lu^1,5,
Zhidong Teng⁶,
Daihai He⁴,
Kai Wang⁶,
Maozai Tian⁶ &
…
Shi Zhao ORCID: orcid.org/0000-0001-8722-6149⁷

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Abstract

Introduction

With COVID-19 vaccination rolled out globally, increasing numbers of studies have shown that booster vaccines can enhance an individual’s protection against the infection, hospitalization, and death caused by SARS-CoV-2. This study evaluated the effectiveness of COVID-19 vaccine BBIBP-CorV booster against being infected (susceptibility), infecting others (infectiousness), and spreading the disease from one to another (transmission).

Methods

This retrospective cohort study investigated the close contacts of all officially ascertained COVID-19 confirmed cases in Urumqi, China between August 1 and September 7, 2022. Eligible records were divided into four subcohorts based on the vaccination status of both the close contact and their source case: group 2-2, 2-dose contacts seeded by 2-dose source case (as the reference level); group 2-3, 3-dose contacts seeded by 2-dose source case; group 3-2, 2-dose contacts seeded by 3-dose source case; and group 3-3, 3-dose contacts seeded by 3-dose source case. In the four subcohorts, multivariate logistic regression models were used to examine the vaccine effectiveness (VE) for the BBIBP-CorV booster dose. We adjusted for potential confounding variables, including the sex and age of source cases and close contacts, the calendar week of contact history and contact settings. We evaluated the statistical uncertainty using a 95% confidence interval (CI). In addition, we conducted subgroup analyses to evaluate VE by sex.

Results

The sample sizes of groups 2-2, 2-3, 3-2, and 3-3 were 1184, 3773, 4723, and 27,136 individuals, respectively. Overall VE against susceptibility (group 2-3 vs 2-2) was 42.1% (95% CI 10.6, 62.5), VE against infectiousness (group 3-2 vs 2-2) was 62.0% (95% CI 37.2, 77.0), and VE against transmission (group 3-3 vs 2-2) was 83.7% (95% CI 75.1, 89.4). In the sex-stratified subgroups, male close contacts showed similar VE compared to the overall. However, among female close contacts, while the booster dose improved VE against infectiousness and VE against susceptibility, the VEs were not significantly different from zero.

Conclusion

BBIBP-CorV vaccine booster was associated with mild to moderate levels of protection against Omicron susceptibility, infectiousness, and transmission. Real-world assessment of protective performance of COVID-19 vaccines against the risk of Omicron strains is continuously needed, and may provide information that helps vaccination strategy.

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FormalPara Key Summary Points

*Why carry out this study?*
The vaccines conferred multiple protection against infectious diseases.
By using contact tracing data, we evaluated the vaccine effectiveness of BBIBP-CorV booster against the susceptibility, infectiousness, and transmission of Omicron strains.
*What was learned from the study?*
BBIBP-CorV vaccine booster was associated with mild to moderate levels of protection against Omicron’s susceptibility, infectiousness, and transmission.
Real-world assessment of vaccine performance against the risk of emerging SARS-CoV-2 genetic variants is continuously needed.

Introduction

Since the outbreak of the COVID-19, vaccination has been regarded as one of the most effective measures to combat the disease [1,2,3]. Vaccine developers and manufacturers have conducted large-scale clinical trials worldwide and reported corresponding vaccine efficacy results [Full size image

Table 1 Baseline characteristics of close contacts of COVID-19 who received 2-dose and 3-dose vaccine

Full size table

The overall VE were shown in Table 2. After adjustment for potential confounding variables, the VE against infectiousness was 62.0% (95% CI 37.2–77.0), the VE against susceptibility was 42.1% (95% CI 10.6–62.5), and the VE against transmission was 83.7% (95% CI 75.1–89.4). In the subgroup analyses, male close contacts showed similar VE compared to the overall sample. However, among female close contacts, while the booster dose improved the VE against infectiousness and VE against susceptibility, the VE estimations were not significantly different from zero.

Table 2 Summary of the effectiveness of 3-dose inactivated vaccine, versus 2-dose (reference level), against SARS-CoV-2 Omicron BA.5 infection

Full size table

Discussion

Since 2022, the Omicron variant and its genetic subtypes have posed a new threat to global public health. Apart from a shortened incubation period, most Omicron infections are either asymptomatic or present with mild symptoms, leading to relatively low risks of hospitalization and mortality [30, 31]. Consequently, researchers have increasingly focused on assessing the effectiveness of vaccines against the Omicron variant. In Urumqi, when there were no reported local cases, close contacts underwent RT-PCR testing once a week. In the presence of sporadic local transmission chains, testing was conducted every 2–3 days, while daily testing was carried out during local outbreaks. These testing efforts provide an ideal research context allowing us to evaluate, in a real-world scenario, the efficacy of a booster dose of inactivated vaccine against Omicron BA.5 infection. This evaluation comprised VE of the booster dose against being infected (susceptibility), infecting others (infectiousness), and spreading the disease from one to another (transmission) combining the VE against being infected and infecting others.

Similar to our findings, a population-based observational study in Hong Kong evaluated the relative VE of three doses versus two doses of CoronaVac during the circulation of the BA.2 variant [6]. The study found that for mild or moderate disease, the third dose increased VE in adults aged 20–59 years (35.7% [95% CI 22.1–47.3]) and adults aged 60 or above (46.9% [95% CI 29.6–60.6]). For severe or fatal disease, the study found that receiving a third dose of the vaccine had additional benefits for adults in all age groups. A systematic review on the real-world effectiveness of inactivated SARS-CoV-2 vaccines reported a pooled booster dose VE of 65.2% (95% CI 48.3–76.6) against the SARS-CoV-2 Delta variant, which decreased to 20.3% (95% CI 10.5-28.0) for the Omicron variant [32] The VE measured in these studies is limited to assessing against susceptibility and is not comprehensive enough.

Our findings indicated that the booster dose of inactivated vaccine provided considerable protection against Omicron infection. Specifically, compared to the reference level group 2-2, group 3-2 achieved a VE against infectiousness, which refers to the extent to which the vaccine reduces infectivity among individuals already infected. The booster dose of inactivated vaccine also conferred a significant reduction in infectivity among the infected individuals. This implied that individuals who received the booster vaccine were likely to have lower transmissibility and therefore transmitted the virus to others at a lower rate. Group 2-3 obtained a VE against susceptibility, which indicated the extent to which the vaccine reduces individual susceptibility. Group 3-3 obtained a VE against transmission, which refers to the vaccine’s ability to break the chain of virus transmission and interrupt community spread. The booster vaccine exhibited significant effectiveness in preventing transmission. Our research suggests that individuals who received the booster dose would have an 83.7% reduced risk of transmitting the virus to others compared to those in group 2-2. This contributes to controlling the spread of the pandemic within communities.

The subgroup analysis was conducted on the three-dose inactivated vaccine by sex. It was found that the protective effect was not significant in the female close contact population, which may be attributed to the fact that female are more frequently engaged in social settings such as supermarkets, shop** malls, and social gathering places, which were focal points of disease transmission during the local outbreak. Thus, female residents were likely associated with a higher infection risk than male[33]. Further research is needed to confirm the impact of sex differences on the vaccine’s protective effects. Additionally, we observed a VE of over 80% against transmission in both male and female individuals , implying that the effect of vaccination for controlling the spread of the epidemic is insensitive of sex.

Limitations

The study has several limitations. Firstly, there were no participants under the age of 18 in group 3-2 and group 3-3 as a result of different vaccination policies for minors and adults in mainland China. Therefore, there was an imbalance in the distribution of adults and minors used for comparison. Secondly, our dataset did not record information regarding clinical severity, so the findings on vaccine effectiveness cannot be extended to a more severe clinical range of COVID-19. Thirdly, the duration and pattern of exposure (e.g., conversation, shared room) could be potential confounding factors in our study, which were not considered in the analysis as a result of limited data collection. Moreover, among the target population of this study, most of the unvaccinated individuals had existing medical conditions that made them ineligible for vaccination. Thus, we excluded these unvaccinated individuals from the analysis, who accounted for less than 10% of the total population in Urumqi, while participants who received two doses of the vaccine were considered as the reference group for booster analysis. Lastly, the social distancing and personal protection behaviors that may affect the risk of infection were not recorded in the dataset, while the intensive non-pharmaceutical measures made most of these characteristics aligned.

Conclusions

This retrospective cohort study showed that the booster dose of BBIBP-CorV vaccine was associated with mild to moderate levels of protection against Omicron susceptibility, infectiousness, and transmission. Real-world assessment of protective performance of COVID-19 vaccines against the risk of Omicron strains is continuously needed, and may provide information that helps vaccination strategy.

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Funding

This work and the journal’s rapid service fee were supported by the Youth science and technology innovation talent of Tianshan Talent Training Program in **njiang (Grant No. :2022TSYCCX0099) and the Technology Innovation Team (Tianshan Innovation Team) Project (Grant No.: 2022TSYCTD0015).

Author information

Ting Zeng, Kailu Wang, and Zihao Guo contributed equally, and they are joint-first authors.

Authors and Affiliations

School of Public Health, **njiang Medical University, Ürümqi, 830017, China
Ting Zeng & Yaoqin Lu
JC School of Public Health and Primary Care, Chinese University of Hong Kong, Hong Kong, 999077, China
Kailu Wang & Zihao Guo
Department of Epidemiology and Biostatistics, School of Public Health, Capital Medical University, Bei**g, 100069, China
Shengzhi Sun
Department of Applied Mathematics, Hong Kong Polytechnic University, Hong Kong, 999077, China
Ziyu Zhai & Daihai He
Urumqi Center for Disease Control and Prevention, Ürümqi, 830026, China
Yaoqin Lu
Department of Medical Engineering and Technology, **njiang Medical University, Ürümqi, 830017, China
Zhidong Teng, Kai Wang & Maozai Tian
Centre for Health Systems and Policy Research, Chinese University of Hong Kong, Hong Kong, 999077, China
Shi Zhao

Authors

Ting Zeng
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Kailu Wang
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Zihao Guo
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Shengzhi Sun
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Ziyu Zhai
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Yaoqin Lu
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Zhidong Teng
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Daihai He
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Kai Wang
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Maozai Tian
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Shi Zhao
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Contributions

Conceptualization: Shi Zhao and Kai Wang. Methodology: Shi Zhao, Ting Zeng, and Yaoqin Lu. Software: Kai Wang and Ting Zeng. Validation: Kailu Wang, Zihao Guo and Shi Zhao. Formal analysis: Kai Wang, Maozai Tian, and Zhidong Teng. Investigation: Kai Wang, Ting Zeng, Yaoqin Lu, and Shi Zhao. Resources: Yaoqin Lu and Kai Wang. Data Curation: Yaoqin Lu and Kai Wang. Writing—Original Draft: Ting Zeng and Kailu Wang. Writing—Review and Editing: Kailu Wang, Zihao Guo, Shengzhi Sun, Ziyu Zhai, Zhidong Teng, Daihai He, Maozai Tian, and Shi Zhao. Visualization: Ting Zeng. Supervision: Kai Wang, Maozai Tian, and Shi Zhao. Project Administration: Kai Wang and Yaoqin Lu. Funding acquisition: Kai Wang and Yaoqin Lu. All authors critically read the manuscript and gave final approval for publication.

Corresponding authors

Correspondence to Kai Wang, Maozai Tian or Shi Zhao.

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Conflict of interest

Ting Zeng, Kailu Wang, Zihao Guo, Shengzhi Sun, Ziyu Zhai, Yaoqin Lu, Zhidong Teng, Daihai He, Kai Wang, Maozai Tan, and Shi Zhao declared no competing interests. The funders of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report.

Ethics approval

The collection of specimens, epidemiological and clinical data for SARS-CoV-2 infected individuals and their close contacts is a part of a continuing public health investigation of COVID-19 outbreaks, ruled in the Protocol on the Prevention and Control of COVID-19 by the National Health Commission of the People’s Republic of China, which was exempt from ethical approval (i.e., institutional review board assessment). This study was approved by the institutional ethics committee of **njiang Medical University (IRB No.: XJYKDXR20221001001). Individual verbal consent was obtained from parents or legal guardians of participants when collecting personal information and human samples by governmental healthcare professionals in the field. This study presents no more than minimal risk of harm to all subjects, and involves no procedures for which written consent is normally required outside of the research context. The institutional ethics committee of **njiang Medical University waived written informed consent, and approved verbal consent for this study.

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Zeng, T., Wang, K., Guo, Z. et al. Distinguishing the Vaccine Effectiveness of Inactivated BBIBP-CorV Vaccine Booster Against the Susceptibility, Infectiousness, and Transmission of Omicron Stains: A Retrospective Cohort Study in Urumqi, China. Infect Dis Ther 12, 2405–2416 (2023). https://doi.org/10.1007/s40121-023-00873-3

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Received: 15 August 2023
Accepted: 11 September 2023
Published: 28 September 2023
Issue Date: October 2023
DOI: https://doi.org/10.1007/s40121-023-00873-3

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Distinguishing the Vaccine Effectiveness of Inactivated BBIBP-CorV Vaccine Booster Against the Susceptibility, Infectiousness, and Transmission of Omicron Stains: A Retrospective Cohort Study in Urumqi, China