Neutralization against SARS-CoV-2 Delta/Omicron variants and B cell response after inactivated vaccination among COVID-19 convalescents

doi:10.1007/s11684-022-0954-x

Front. Med.

2023, Vol. 17

Issue (4) : 747-757 https://doi.org/10.1007/s11684-022-0954-x

RESEARCH ARTICLE

Neutralization against SARS-CoV-2 Delta/Omicron variants and B cell response after inactivated vaccination among COVID-19 convalescents

Hao Wang¹, Yu Yuan¹, Bihao Wu^2,³, Mingzhong Xiao^4,⁵, Zhen Wang¹, Tingyue Diao¹, Rui Zeng¹, Li Chen^2,³, Yanshou Lei¹, Pinpin Long¹, Yi Guo¹, Xuefeng Lai¹, Yuying Wen¹, Wenhui Li¹, Hao Cai¹, Lulu Song¹, Wei Ni^4,⁵, Youyun Zhao^4,⁵, Kani Ouyang^4,⁵, Jingzhi Wang^4,⁵, Qi Wang¹, Li Liu¹, Chaolong Wang¹, An Pan¹, Xiaodong Li^4,⁵(

), Rui Gong²(

), Tangchun Wu¹(

)

¹. Ministry of Education and State Key Laboratory of Environmental Health (Incubating), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
². CAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan 430071, China
³. University of Chinese Academy of Sciences, Beijing 100049, China
⁴. Affiliated Hospital of Hubei University of Chinese Medicine, Wuhan 430061, China
⁵. Hubei Provincial Hospital of Traditional Chinese Medicine, Wuhan 430061, China

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Abstract

Emerging SARS-CoV-2 variants have made COVID-19 convalescents susceptible to re-infection and have raised concern about the efficacy of inactivated vaccination in neutralization against emerging variants and antigen-specific B cell response. To this end, a study on a long-term cohort of 208 participants who have recovered from COVID-19 was conducted, and the participants were followed up at 3.3 (Visit 1), 9.2 (Visit 2), and 18.5 (Visit 3) months after SARS-CoV-2 infection. They were classified into three groups (no-vaccination (n = 54), one-dose (n = 62), and two-dose (n = 92) groups) on the basis of the administration of inactivated vaccination. The neutralizing antibody (NAb) titers against the wild-type virus continued to decrease in the no-vaccination group, but they rose significantly in the one-dose and two-dose groups, with the highest NAb titers being observed in the two-dose group at Visit 3. The NAb titers against the Delta variant for the no-vaccination, one-dose, and two-dose groups decreased by 3.3, 1.9, and 2.3 folds relative to the wild-type virus, respectively, and those against the Omicron variant decreased by 7.0, 4.0, and 3.8 folds, respectively. Similarly, the responses of SARS-CoV-2 RBD-specific B cells and memory B cells were boosted by the second vaccine dose. Results showed that the convalescents benefited from the administration of the inactivated vaccine (one or two doses), which enhanced neutralization against highly mutated SARS-CoV-2 variants and memory B cell responses. Two doses of inactivated vaccine among COVID-19 convalescents are therefore recommended for the prevention of the COVID-19 pandemic, and vaccination guidelines and policies need to be updated.

Keywords COVID-19 convalescent SARS-CoV-2 inactivated vaccination neutralizing antibody B cell response

Corresponding Author(s): Xiaodong Li,Rui Gong,Tangchun Wu

Just Accepted Date: 02 December 2022 Online First Date: 07 February 2023 Issue Date: 12 October 2023

Cite this article:

Hao Wang,Yu Yuan,Bihao Wu, et al. Neutralization against SARS-CoV-2 Delta/Omicron variants and B cell response after inactivated vaccination among COVID-19 convalescents[J]. Front. Med., 2023, 17(4): 747-757.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-022-0954-x
https://academic.hep.com.cn/fmd/EN/Y2023/V17/I4/747

Fig.1 Study profile. Abbreviation: NAb, neutralizing antibody; PBMC, peripheral blood mononuclear cell; RBD, receptor-binding domain.

	Total(n = 208)	No-vaccination group(n = 54)	One-dose group(n = 62)	Two-dose group(n = 92)	P
Age (year)	58 (50–65)	58 (45–66)	57 (49–65)	59 (52–64)	0.705
Sex					0.341
Men	100 (48.1%)	30 (55.6%)	26 (41.9%)	44 (47.8%)
Women	108 (51.9%)	24 (44.4%)	36 (58.1%)	48 (52.2%)
Education					0.296
Middle school or lower	140 (67.3%)	33 (61.1%)	40 (64.5%)	67 (72.8%)
College or higher	68 (22.7%)	21 (38.9%)	22 (35.5%)	25 (27.2%)
Cigarette smoking					0.097
Never smoker	183 (88.0%)	47 (87.0%)	59 (95.2%)	77 (83.7%)
Ever smoker	25 (12.0%)	7 (13.0%)	3 (4.8%)	15 (16.3%)
Alcohol consumption					0.038
Never drinker	183 (88.0%)	45 (83.3%)	60 (96.8%)	78 (84.8%)
Ever drinker	25 (12.0%)	9 (16.7%)	2 (3.2%)	14 (15.2%)
Body mass index	24.3 (22.6– 26.5)	24.1 (22.7–26.0)	24.5 (22.1–26.8)	24.3 (22.8–26.5)	0.793
Waist circumference (cm)	90.0 (83.0–97.0)	92.0 (82.0–96.5)	88.0 (79.3–95.0)	91.0 (85.3–98.0)	0.163
Comorbidity
Hypertension	75 (36.1%)	19 (35.2%)	22 (35.5%)	34 (37.0%)	0.971
Diabetes	23 (11.1%)	5 (9.3%)	9 (14.5%)	9 (9.8%)	0.582
CVD	14 (6.7%)	4 (7.4%)	5 (8.1%)	5 (2.4%)	0.794
Severity					0.724
Mild	146 (70.2%)	36 (66.7%)	43 (69.4%)	67 (72.8%)
Severe	62 (29.8%)	18 (33.3%)	19 (30.6%)	25 (27.2%)
Time from infection to Visit 1 (month)	3.3 (1.3–4.4)	3.0 (1.0–4.0)	3.2 (1.4– 4.2)	3.5 (1.6–4.6)	0.143
Time from infection to Visit 2 (month)	9.2 (9.0–9.6)	9.2 (9.0–9.4)	9.3 (9.0–9.7)	9.2 (8.8–9.9)	0.440
Time from infection to Visit 3 (month)	18.5 (18.2–19.1)	18.4 (18.1–19.0)	18.4 (18.2–18.9)	18.7 (18.2–19.3)	0.148
Time from infection to the first vaccination (month)	–	–	16.7 (15.9– 17.3)	15.9 (15.1– 16.6)	< 0.001
Time from infection to the second vaccination (month)	–	–	–	17.1 (16.4–17.5)	–
Time from infection to the last vaccination (month)^a	–	–	16.7 (15.9–17.3)	17.1 (16.4–17.5)	0.043
Time from the last vaccination to Visit 3 (month)	–	–	1.7 (1.1–2.9)	1.6 (1.1–2.3)	0.263

Tab.1 Characteristics of COVID-19 patients by vaccination status

Fig.2 Longitudinal assessment of neutralizing antibody (NAb) against wild-type SARS-CoV-2. (A) Graph manifesting temporal changes in NAb against the wild-type virus in each individual from the no-vaccination, one-dose, and two-dose groups. (B) Boxplots indicating the median values with the 25th and 75th percentiles of NAb against the wild-type virus at Visits 1, 2, and 3. The whiskers show the 1.5 interquartile range. *P≤ 0.05, **P≤ 0.01, ***P≤ 0.001.

Fig.3 Neutralizing antibody (NAb) against wild-type, Delta, and Omicron variants of SARS-CoV-2 at Visit 3. (A) NAb against wild-type, Delta, and Omicron variants at Visit 3 in each individual from the no-vaccination, one-dose, and two-dose groups. (B) Boxplots illustrating NAb against the wild-type, Delta, or Omicron variants in the no-vaccination, one-dose, and two-dose vaccination groups at Visit 3. The fold decrease of median NAb titers for the Delta and Omicron variants relative to wild-type variant was calculated and denoted as a number with the × symbol. (C) Calculated fold decrease of NAb titers against the Delta and Omicron variants relative to the wild-type variant in each individual (Fold decrease =(NAb titers against wild-type / NAb titers against Delta or Omicron variant)). A significant difference in the fold decrease of NAb titers against the Omicron variant was observed between no-vaccination and two-dose vaccination groups at Visit 3 (calculated by the Mann–Whitney U-test). We divided the participants according to the fold decrease of NAb titers against the Delta variant relative to the wild-type virus (D) and the Omicron variant relative to the wild-type virus (E) and categorized the fold decrease into four groups (Delta variant: < 2 folds, 2–4 folds, 4–6 folds, > 6 folds; Omicron variant: < 4 folds, 4–8 folds, 8–12 folds, > 12 folds). The proportion of participants was expressed as the percentage of each group and presented as stacked bar graphs. P > 0.05, not significant (ns); *P≤ 0.05, **P≤ 0.01, ***P≤ 0.001.

Fig.4 SARS-CoV-2 RBD-specific B cells and memory B cells among the COVID-19 patients at Visit 3 by vaccination status. (A) Graph summarizing the sorting of SARS-CoV-2 RBD-specific B cells and memory B cells. (B) Percentage of SARS-CoV-2 RBD-specific B cells and (C) percentage of SARS-CoV-2 RBD-specific memory B cells. The boxplots indicate the median values with the 25th and 75th percentiles, and the whiskers show the 1.5 interquartile range. Statistical significance was determined using the Mann–Whitney U-test. P > 0.05, not significant (ns); *P≤ 0.05, **P≤ 0.01, ***P≤ 0.001.

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