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ORIGINAL ARTICLE  
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Evaluation of COVID-19 antibodies with demographic profiles, vaccination, and infection


1 Department of Transfusion Medicine, King George Medical University, Lucknow, Uttar Pradesh, India
2 Department of Community Medicine, King George Medical University, Lucknow, Uttar Pradesh, India
3 Department of Otolaryngology and Head and Neck Surgery, King George Medical University, Lucknow, Uttar Pradesh, India
4 Era Lucknow Medical college and Hospital, Lucknow, Uttar Pradesh, India

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Date of Submission29-May-2022
Date of Decision17-Aug-2022
Date of Acceptance28-Aug-2022
Date of Web Publication12-Dec-2022
 

   Abstract 

OBJECTIVE: COVID-19 infection has raised concern regarding the short duration of immunity afforded by vaccines and antibodies elicited by natural infection. This aim was to examine differences in antibody titers associated with age, sex, vaccination doses, and infection in healthcare workers with previous positive quantitative reverse transcription polymerase chain reaction tests. Antibodies detection by the enzyme-linked immunoassay (ELISA) was validated by electrochemiluminescence immunoassay (ECLIA) to find a cost-effective antibody test.
MATERIALS AND METHODOLOGY: The study was carried out in 530 healthcare professionals, who were previously infected with COVID-19 infection, had received two doses of Covidshield vaccine. COVID antibody titer was performed and analyzed with different aspects of subgroups, with respect to gender, age and duration at how long COVID-19 antibodies persist in the plasma; after COVID-19 infection. The duration was seen after the first and second dose of COVID vaccine. Previously, COVID-negative participants with both doses of vaccine showed a significant level of antibodies antibody detection were carried out by ELISA and ECLIA taking latter as the gold standard.
RESULTS: Maximum people who had antibodies, the duration was within 100 days after COVID-19 infection. Highest number of people showing good antibodies titer was seen between 101 and 150 days after the 1st vaccine while between 50 and 100 days after the second vaccine. Maximum antibody titer was seen after both doses of vaccination with COVID infection. Correlation between ELISA and ECLIA test and efficacy of ELISA test was calculated, taking ECLIA as the gold standard.
CONCLUSION: More than 50-year age have slightly higher levels of IgG COVID-19 antibodies but gender has no effect. Duration of antibody persistence was maximum between 100 and 150 days after the first dose and 50–100 days after the second dose; hence, a booster was needed early. COVID infection increased the duration of antibodies persistence. ELISA is a cost-effective and accurate method for COVID antibody testing.

Keywords: COVID-19 antibodies, demography, vaccination


How to cite this URL:
Chandra T, Singh VK, Bharti J, Agarwal D, Agarwal M. Evaluation of COVID-19 antibodies with demographic profiles, vaccination, and infection. Asian J Transfus Sci [Epub ahead of print] [cited 2023 Jan 28]. Available from: https://www.ajts.org/preprintarticle.asp?id=363236



   Introduction Top


COVID-19 pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), led to serious mortality and morbidity, since its emergence in January 2020. It became important to identify people with COVID infection and those with a positive immune response to the virus to control the infection. The response of an individual's immune system is the most important marker for the determination of mortality and morbidity. Although the vaccines presently approved by the WHO have been designed using different technologies, the goal of all of them is to stimulate a person's immune system. Various tests have been developed capable of detecting immunoglobulin M (IgM), IgA, and IgG antibodies from blood samples of patients who were previously or are currently infected with SARS-CoV-2. These serological tests are performed using various viral antigens and recombinant proteins to capture SARS-CoV-2-specific antibodies. Moreover, accurate measurement of the antibody response that occurs as a consequence of vaccinations plays an important role in determining the success rate of the vaccine and whether people are protected against the infection. However, the antibody response stimulated by the vaccine is affected by many factors depending on both the individual and the vaccine, which can positively or negatively affect the protection against the virus.[1] The gold standard diagnostic method for COVID-19 is quantitative reverse transcription polymerase chain reaction (RT-qPCR) testing, which detects viral RNA in the respiratory tract samples. Only acute cases may be identified by RT-qPCR testing, and the test provides no information on patient immunity or other characteristics. Antibodies such as IgG, IgM, and IgA are the most sensitive and are early serological markers of infection, with levels beginning to rise as early as the 2nd week after the onset of symptoms. Although serum IgM and IgG can be positive with low titers as early as the 4th day after symptom onset, higher levels appear during the 2nd and 3rd week of the disease. Asymptomatic individuals and others with suspected infection and negative nucleic acid tests can be diagnosed using serological antibody assays. Experience with other human coronaviruses demonstrated an average duration of immunity of 12 years. SARS-CoV-2 appears to elicit similar antibody responses compared with other human coronaviruses based on early clinical studies. It is crucial to understand how the immune response to COVID-19 changes with age, disease duration, severity, as well as the duration of postinfection protection afforded by the antibody response. Concerns have been raised regarding the short duration of immunity afforded by vaccines and antibodies elicited by natural infection. This study's goal was to examine the differences in antibody titers associated with age and sex in patients with COVID-19 with previous positive RT-qPCR tests.[2]


   Materials and Methodology Top


The study was carried out between May 2021 and September 2021 in the King George's University in Lucknow, U. P. 530 healthcare professionals including both who were infected as well as not infected with COVID-19 infection but had received both doses of Covidshield vaccine participated in the study. We performed COVID antibody titer and analyzed with different aspects of subgroups, with respect to gender, age (1829 years, 3049 years, >50 years) and duration at how long COVID-19 antibodies persist in the plasma after COVID-19 infection both after first and second dose of covid vaccine. We also analyzed antibodies titer with increasing days which was, 0100 days, 101200 days, 201300 days, 301400 days, and more than 400 days.

Study design and participants

It is a prospective observational study, designed to assess the antibody response in the population of healthcare professionals. Informed consent was taken from all participants. The study was approved by a central ethical committee. Participants having COVID-19 infection received the first vaccine dose from January 2021 to July 2021. The second dose was administered either 21 days or 84 days after the first one. Samples were then collected from December 05, 2021 to March 09, 2022. Antibodies against the SARS-CoV-2 nucleocapsid and the receptor binding domain (RBD) of the S1 subunit of the spike protein were measured by the enzyme-linked immunoassay (ELISA) test and Electrochemiluminescence immunoassay (ECLIA) test. ECLIA was taken as a gold standard for COVID-19 antibodies titers in participant's plasma.

Laboratory study

510 ml of venous blood was collected and centrifuged at 2500 rpm for 15 min and serum was separated. All antibodies including IgG formed against the RBD of the spike protein were quantitatively studied by the sandwich enzyme-linked immunosorbent assay (ELISA) method using AntiSARSCoV-2 S kit (Q-LISA), and the total antibodies formed against the nucleocapsid protein (NCP) were qualitatively studied by electrochemiluminescence (ECLIA) using Elecsys Anti-SARS-CoV-2 kit (Architect i20). Antibodies developed against NCP were measured according to the Cut-Off Index (COI) value. A COI ≥1.0 was considered positive for ELISA and ≥50 OD value positive for ECLIA.

Statistical analysis

Statistical analysis was performed using SPSS version 23.0 (IBM Corporation) Lucknow. Conformity of data to the normal distribution was determined by histogram and Chi-square tests. The difference between the groups was calculated with Chi-squared, Fisher's exact, Mann–Whitney U, and Kruskal–Wallis tests in line with suitability. The Wilcoxon test was used to compare the change in S-RBD antibody titers at COVID-19 infection, first dose of vaccine and after the second dose of vaccine. P value lower than 0.05 was considered to indicate statistically significant results.


   Results Top


In our study, 184 (34.7%) of the participants were female and 346 (65.3%) were male. Participants in age group between 18 years and 29 years were 121 (22.8%), 30 years to 49 years were 305 (57.5%), >50 years were 104 (19.6%) It was seen that COVID-19 antibody detected by ELISA in all age groups and gender was almost same [Table 1]. Maximum people who had antibodies, the duration was within 100 days after COVID-19 infection [Table 2]. It was found that maximum peoples showed antibodies after the 1st dose of COVID-19 vaccine between 100 and 150 days, both by ELISA and ECLIA [Table 3]. Maximum antibody titer was seen in both, by ELISA and ECLIA after 2nd dose of vaccination between 50 and 100 days [Table 4]. All the cases show association between COVID positivity and antibodies found by ELISA and ECLIA among all cases both vaccinated and nonvaccinated [Table 5]. People who become COVID positive after the 1st dose of COVID vaccination showed maximum antibody among all cases signifying that associated COVID infection with its natural antibodies enhanced the level of immunity of an individual [Table 6]. Our study showed the, after 1st dose of vaccination 94.9% by ELISA and 98.2% by ECLIA cases showed significant presence of antibodies [Table 7]. Our study also showed that after 2nd dose of COVID vaccination 94.9% by ELISA and 99.2% by ECLIA [Table 8] showed significant presence of antibodies titer. 92.7% by ELISA and 97.4% by ECLIA of all COVID negative cases also showed significant titer of COVID antibodies after 1st dose of COVID vaccination while 92.6% by ELISA and 98.8% by ECLIA of all COVID negative cases showed significant titer of COVID antibodies after 2nd dose of COVID vaccination [Table 9]. Maximum antibodies titer was seen in cases who had become COVID positive and then vaccinated with 1st and 2nd dose. It was 98.8% by ELISA and 99.4% by ECLIA. Correlation between ELISA and ECLIA test and efficacy of ELISA test can be calculated, tacking ECLIA as the gold standard by the equation mentioned in [Table 10] and [Figure 1].
Table 1: Covid antibodies with respect to age and gender

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Table 2: COVID antibodies in all COVID positive cases with respect to duration

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Table 3: COVID antibodies after 1st dose of vaccination by enzyme linked immunosorbent assay and electrochemiluminescence immunoassay

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Table 4: COVID antibodies after 2nd dose of vaccination by enzyme linked immunosorbent assay and electrochemiluminescence immunoassay

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Table 5: Association between COVID positivity and antibodies found by enzyme linked immunosorbent assay and electrochemiluminescence immunoassay among all vaccinated and nonvaccinated cases

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Table 6: Association between COVID positivity and antibodies found by enzyme linked immunosorbent assay among all the cases who received first dose of vaccination

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Table 7: Association between first dose vaccine and antibodies found by enzyme linked immunosorbent assay and electrochemiluminescence immunoassay among all the cases either COVID positive or negative

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Table 8: Association between second dose vaccine and antibodies found by enzyme linked immunosorbent assay and electrochemiluminescence immunoassay among all the cases of either COVID positive or negative

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Table 9: Association between second dose of vaccine and antibodies found by electrochemiluminescence immunoassay among COVID negative cases

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Table 10: Relation between enzyme linked immunosorbent assay and electrochemiluminescence immunoassay test

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Figure 1: Graphical representation of detection of covid antibodies by ELISA and chemiluminiscence

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   Discussion Top


The study of the antibody response to SARS-CoV-2 identifies the effectiveness of vaccines. The serological response can affect the quality of the immune response of the infected person and the duration of immunity, due to both individual characteristics and vaccine-related both are different.[1]

According to Yang et al. study, SARS-CoV-2 viral specific antibody response profiles are distinct in different age groups.[3] In our study, we found that there was no statistically significant relationship between age and antibodies, however, those in the age group of >50 years (93.3%) had slightly higher antibody titers than other age groups.

According to R. Pellini, A. Venuti, F. Pimpinelli et al. study, antibody responses of greater magnitude were shown in women vs in men; this difference was statistically significant.[4] In our study, we observed that there was no significant relationship between gender specific COVID infected participants; male 319 (92.2%) and female 174 (94.6%) had COVID antibodies titer.

According to Harrington et al., they observed that mild COVID-19 infection, nearly all of the participants developed antibodies and that anti-S trimer and anti-RBD IgG persisted relatively unchanged through at least 6 months.[5] In our study, we had found antibodies titer was maximum up to 100 days after natural COVID-19 infections, which, gradually decreased with days passed on.

According to Pellini et al., antibodies that arise as a response to humoral immunity in individuals previously infected with COVID-19 infection or vaccinated against COVID-19 first or second dose are present in the blood for a certain period of time. Although antibodies produced by short-lived plasma cells in secondary lymphoid organs increase rapidly in the blood and then decrease rapidly in the first 3 months, the antibodies produced by long-lived plasma cells in the bone marrow tend to decrease more slowly in the following period.[1] In our study We found that after first dose of COVID-19 vaccine, COVID antibodies titer was maximum up to 150 days, which was gradually decreases with time.

According to Urbanowicz et al., antibody responses in serum samples isolated from naïve individuals and individuals with prior history of SARS-CoV-2 infection at baseline and after vaccination with first and second doses. Although previous studies have shown that antibody responses in previously exposed individuals are greater after a single dose of a COVID-19 vaccine, this study shows that the trend toward higher neutralizing antibody frequency in previously infected people continues after the second dose.[6] According to another study, Yamayoshi et al., the antibody response against the first exposure to the newly emerged SARS-CoV-2 was consistent in the COVID-19 patients of the mild, moderate, and severe groups although levels of neutralizing antibodies tend to decrease as time passes.[7] This was supported by our study.

According to Khoury et al. the possibility of neutralization correlating with immune responses was present.[8] In our study we found that association between COVID positivity and antibodies among all vaccinated and nonvaccinated participants showed strong correlation which was statistically significant.

According to Urbanowicz et al. after one dose of vaccine in individuals with or without prior infection, spike protein–specific IgG and neutralizing antibody concentrations were lower against the B.1.351 variant than lineage A strains.[6] In our study we found that, association between COVID positivity and antibodies among all the cases who received first dose of COVID vaccine but no history of COVID infection had high levels of antibodies signifying probably that they were asymptomatic COVID infected individuals.

According to Wheeler et al., vaccinated people for selecting individuals who need additional boosting because of low responsiveness or might require a third dose of vaccine at an earlier time point or persons who may do not need second dose due to previous SARS-CoV-2 infection. In healthy individuals demonstrates an unexpectedly low response to vaccination, concerns can be raised regarding a particular batch of a vaccine.[9] According to Urbanowicz et al., two-dose BNT162b2 vaccination schedule increased IgG concentration and neutralization of the B.1.351 and P. 1 variants to values comparable to the lineage A virus.[6] According to Uysal et al., postvaccine humoral immune response, seropositivity of 99.6 was observed 4 weeks after the vaccine. A decrease in antibody titer was observed at the 12th week of the inactive whole virion vaccine in the participants who had 75250 U/ml antibodies after excluding those with >250 U/ml antibodies. Although there was a statistically significant decrease in antibody titers.[1] In our study participants showed association between COVID positivity and antibodies found among all the participants who received first and second dose of COVID-19 vaccine. COVID antibody titer was maximum after receiving COVID first and second dose vaccine with associatedcovid positivity.

According to the Urbanowicz et al. after one dose of vaccine in individuals with or without prior infection, spike protein–specific IgG and neutralizing antibody concentrations were lower against the B.1.351 variant than lineage A strains. However, increasing antigenic exposure in humans through natural infection was seen.[6] Our study also supported the fact.

According to Favresse et al. study, a significant antibody decline was seen 3 months postvaccination in both seronegative and seropositive individuals who received two doses of vaccine. The highest mean antibody titer was observed between days 14 and 42 for seropositive participants and between 28 and 42 days for seronegative participants.[10] We found that COVID-19 antibodies titer increased after receiving both doses of COVID-19 vaccine with or without COVID infection and was significantly greater than those after only first dose of vaccine.

According to Levi et al. 1st vaccine dose was sufficient to induce a robust antibody response in SARS-CoV-2–exposed subjects. They stated that a second vaccine dose may be detrimental due to hyper-immune activation, which could switch-off the immune response due to antigen exhaustion, as it occurs after several viral infections.[11] This was in contrast to our observation where no such decrease was observed. Another study, Admin stated that 3 weeks after a single vaccination, persons with recent SARS-CoV-2 infection or seropositive status had higher levels of antibody to four SARS-CoV-2 antigens and higher levels of antibodies with neutralizing characteristics those without a history of infection.[12] Our study showed similar findings.

According to Doria-rose et al. antibody titers and assays that best correlate with vaccine efficacy persisted through 6 months after the second dose, as detected by three distinct serologic assays.[13] According to Singh et al. study it suggested that both vaccines induce seropositivity to anti-spike antigen in 95% of SARS-COV-2 naïve and recovered individuals, 3-week after the completion of two doses. Covishield recipients had a significantly higher rate of seropositivity and GMT of anti-spike antibody com-pared to Covaxin both after the first and second doses.[14] Our study also supports their observation.

According to T. SARS-COV-he demonstrated a significantly higher humoral immunogenicity of the SARS-CoV-2 mRNA-1273 vaccine compared with the BNT162b2 vaccine in infected as well as uninfected participants and also across age categories.[15] According to another study of Wei et al. which showed that postvaccine anti-spike IgG responses vary by prior infection status, age, sex, vaccine type and number of doses received. In those who were previously infected, all age groups achieved high antibody responses after the first vaccination. In those without evidence of prior infection, older participants had lower and slower responses after the first vaccine dose than younger participants.[16] In our study, no significant age difference was seen but prior infection showed better response after vaccination.

According to Wei et al. who showed that after two vaccine doses high response was present across all age groups, and particularly increased the number of older people seroconverting to similar levels to those receiving one dose after prior infection, as recently reported in a smaller number of younger individual.[16] According to Bates et al., SARS-CoV-2 infection before or after vaccination gives a significantly larger boost to the neutralizing antibody response compared with two doses of vaccine alone. The potency and breadth of the antibody response appear to improve concomitantly. It has been well established that natural infection alone provides short-lived protection from infection, showing the importance of vaccination, regardless of infection history. Because vaccination protects against severe disease safer for individuals to be vaccinated before rather than after natural infection and death. It is safer for individuals to be vaccinated before rather than after natural infection.[17] In our study, we found that antibodies generated in those participants who received both vaccine doses with past COVID-19 natural infection were more as compared to those who had only been doubly vaccinated.

In our study, ECLIA test was taken as the gold standard and compared with ELISA which is a more cost-effective test, especially in developing countries. Results were in synchrony and validated. To decipher the level of antibodies by ELISA, an equation was deciphered to correlate the values with the gold standard test.


   Conclusion Top


In our study suggest that there are distinct SARS-CoV-2 viral-specific antibody response profiles that vary based on age, in >50-year age slightly higher levels of IgG COVID-19 antibodies than other age group category. Our data also concluded that COVID-19 antibodies titer is higher with a history of COVID-19 infection in their past (99.98%) as compared to those who only had COVID-19 vaccine first or second dose. Maximum antibody titer was seen after the 2nd dose of vaccination with COVID infection. Booster should be given early within 5 months of second dose to have the maximum response. ELISA is a cost-effective and accurate method for COVID antibodies testing.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Uysal EB, Gümüş S, Bektöre B, Bozkurt H, Gözalan A. Evaluation of antibody response after COVID-19 vaccination of healthcare workers. J Med Virol 2022;94:1060-6.  Back to cited text no. 1
    
2.
Uysal BB, Yavuzer S, Islamoglu MS, Cengiz M. Measurement of antibody levels in patients with COVID-19 over time by immunofluorescence assay: A longitudinal observational study. J Int Med Res 2022;50:3000605211069279.  Back to cited text no. 2
    
3.
Yang HS, Costa V, Racine-Brzostek SE, Acker KP, Yee J, Chen Z, et al. Association of age with SARS-CoV-2 antibody response. JAMA Netw Open 2021;4:e214302.  Back to cited text no. 3
    
4.
Pellini R, Venuti A, Pimpinelli F, Abril E, Blandino G, Campo F, et al. Initial observations on age, gender, BMI and hypertension in antibody responses to SARS-CoV-2 BNT162b2 vaccine. EClinicalMedicine 2021;36:100928.  Back to cited text no. 4
    
5.
Harrington WE, Trakhimets O, Andrade DV, Dambrauskas N, Raappana A, Jiang Y, et al. Rapid decline of neutralizing antibodies is associated with decay of IgM in adults recovered from mild COVID-19. Cell Rep Med 2021;2:100253.  Back to cited text no. 5
    
6.
Urbanowicz RA, Tsoleridis T, Jackson HJ, Cusin L, Duncan JD, Chappell JG, et al. Two doses of the SARS-CoV-2 BNT162b2 vaccine enhance antibody responses to variants in individuals with prior SARS-CoV-2 infection. Sci Transl Med 2021;13:eabj0847.  Back to cited text no. 6
    
7.
Yamayoshi S, Yasuhara A, Ito M, Akasaka O, Nakamura M, Nakachi I, et al. Antibody titers against SARS-CoV-2 decline, but do not disappear for several months. EClinicalMedicine 2021;32:100734.  Back to cited text no. 7
    
8.
Khoury DS, Cromer D, Reynaldi A, Schlub TE, Wheatley AK, Juno JA, et al. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat Med 2021;27:1205-11.  Back to cited text no. 8
    
9.
Wheeler SE, Shurin GV, Yost M, Anderson A, Pinto L, Wells A, et al. Differential antibody response to mRNA COVID-19 vaccines in healthy subjects. Microbiol Spectr 2021;9:e0034121.  Back to cited text no. 9
    
10.
Favresse J, Bayart JL, Mullier F, Elsen M, Eucher C, Van Eeckhoudt S, et al. Antibody titres decline 3-month post-vaccination with BNT162b2. Emerg Microbes Infect 2021;10:1495-8.  Back to cited text no. 10
    
11.
Levi R, Azzolini E, Pozzi C, Ubaldi L, Lagioia M, Mantovani A, et al. One dose of SARS-CoV-2 vaccine exponentially increases antibodies in individuals who have recovered from symptomatic COVID-19. J Clin Invest 2021;131:149154.  Back to cited text no. 11
    
12.
Antibody Responses after a Single Dose of SARS-CoV-2 mRNA Vaccine - Todd Bradley et al. N Engl J Med. 2021 Mar 23: NEJMc2102051.  Back to cited text no. 12
    
13.
Doria-Rose N, Suthar MS, Makowski M, O'Connell S, McDermott AB, Flach B, et al. Antibody persistence through 6 months after the second dose of mRNA-1273 vaccine for Covid-19. N Engl J Med 2021;384:2259-61.  Back to cited text no. 13
    
14.
Singh AK, Phatak SR, Singh R, Bhattacharjee K, Singh NK, Gupta A, et al. Antibody response after first and second-dose of ChAdOx1-nCOV (Covishield TM Ò) and BBV-152 (Covaxin TM Ò) among health care workers in India: The final results of cross-sectional coronavirus vaccine-induced antibody titre (COVAT) study. Vaccine 2021;39:6492-509.  Back to cited text no. 14
    
15.
Steensels D, Pierlet N, Penders J, Mesotten D, Heylen L. Comparison of SARS-CoV-2 antibody response following vaccination with BNT162b2 and mRNA-1273. JAMA 2021;326:1533-5.  Back to cited text no. 15
    
16.
Wei J, Stoesser N, Matthews PC, Ayoubkhani D, Studley R, Bell I, et al. Antibody responses to SARS-CoV-2 vaccines in 45,965 adults from the general population of the United Kingdom. Nat Microbiol 2021;6:1140-9.  Back to cited text no. 16
    
17.
Bates TA, McBride SK, Leier HC, Guzman G, Lyski ZL, Schoen D, et al. Vaccination before or after SARS-CoV-2 infection leads to robust humoral response and antibodies that effectively neutralize variants. Sci Immunol 2022;7:eabn8014.  Back to cited text no. 17
    

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Correspondence Address:
Devisha Agarwal,
A-15 Nirala Nagar, Lucknow - 226 020, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ajts.ajts_64_22



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