SARS-CoV-2 infection, vaccination, and antibody response trajectories in adults: a cohort study in Catalonia

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Abstract

Background

Heterogeneity of the population in relation to infection, COVID-19 vaccination, and host characteristics is likely reflected in the underlying SARS-CoV-2 antibody responses.

Methods

We measured IgM, IgA, and IgG levels against SARS-CoV-2 spike and nucleocapsid antigens in 1076 adults of a cohort study in Catalonia between June and November 2020 and a second time between May and July 2021. Questionnaire data and electronic health records on vaccination and COVID-19 testing were available in both periods. Data on several lifestyle, health-related, and sociodemographic characteristics were also available.

Results

Antibody seroreversion occurred in 35.8% of the 64 participants non-vaccinated and infected almost a year ago and was related to asymptomatic infection, age above 60 years, and smoking. Moreover, the analysis on kinetics revealed that among all responses, IgG RBD, IgA RBD, and IgG S2 decreased less within 1 year after infection. Among vaccinated, 2.1% did not present antibodies at the time of testing and approximately 1% had breakthrough infections post-vaccination. In the post-vaccination era, IgM responses and those against nucleoprotein were much less prevalent. In previously infected individuals, vaccination boosted the immune response and there was a slight but statistically significant increase in responses after a 2nd compared to the 1st dose. Infected vaccinated participants had superior antibody levels across time compared to naïve-vaccinated people. mRNA vaccines and, particularly the Spikevax, induced higher antibodies after 1st and 2nd doses compared to Vaxzevria or Janssen COVID-19 vaccines. In multivariable regression analyses, antibody responses after vaccination were predicted by the type of vaccine, infection age, sex, smoking, and mental and cardiovascular diseases.

Conclusions

Our data support that infected people would benefit from vaccination. Results also indicate that hybrid immunity results in superior antibody responses and infection-naïve people would need a booster dose earlier than previously infected people. Mental diseases are associated with less efficient responses to vaccination.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12916-022-02547-2.

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Most cited references 40

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Rapid Decay of Anti–SARS-CoV-2 Antibodies in Persons with Mild Covid-19

F. Ibarrondo, Jennifer A. Fulcher, David Goodman-Meza … (2020)

To the Editor: A recent article suggested the rapid decay of anti–SARS-CoV-2 IgG in early infection, 1 but the rate was not described in detail. We evaluated persons who had recovered from Covid-19 and referred themselves to our institution for observational research. Written informed consent was obtained from all the participants, with approval by the institutional review board. Blood samples were analyzed by enzyme-linked immunosorbent assay (ELISA) to detect anti–SARS-CoV-2 spike receptor-binding domain IgG. 2 The ELISA was further modified to precisely quantify serum anti–receptor-binding domain activity in terms of equivalence to the concentration of a control anti–receptor-binding domain monoclonal IgG (CR3022, Creative Biolabs). Infection had been confirmed by polymerase-chain-reaction assay in 30 of the 34 participants. The other 4 participants had had symptoms compatible with Covid-19 and had cohabitated with persons who were known to have Covid-19 but were not tested because of mild illness and the limited availability of testing. Most of the participants had mild illness; 2 received low-flow supplemental oxygen and leronlimab (a CCR5 antagonist), but they did not receive remdesivir. There were 20 women and 14 men. The mean age was 43 years (range, 21 to 68) (see the Supplementary Appendix, available with the full text of this letter at NEJM.org). A total of 31 of the 34 participants had two serial measurements of IgG levels, and the remaining 3 participants had three serial measurements. The first measurement was obtained at a mean of 37 days after the onset of symptoms (range, 18 to 65), and the last measurement was obtained at a mean of 86 days after the onset of symptoms (range, 44 to 119). The initial mean IgG level was 3.48 log10 ng per milliliter (range, 2.52 to 4.41). On the basis of a linear regression model that included the participants’ age and sex, the days from symptom onset to the first measurement, and the first log10 antibody level, the estimated mean change (slope) was −0.0083 log10 ng per milliliter per day (range, −0.0352 to 0.0062), which corresponds to a half-life of approximately 36 days over the observation period (Figure 1A). The 95% confidence interval for the slope was −0.0115 to −0.0050 log10 ng per milliliter per day (half-life, 26 to 60 days) (Figure 1B). The protective role of antibodies against SARS-CoV-2 is unknown, but these antibodies are usually a reasonable correlate of antiviral immunity, and anti–receptor-binding domain antibody levels correspond to plasma viral neutralizing activity. Given that early antibody decay after acute viral antigenic exposure is approximately exponential, 3 we found antibody loss that was quicker than that reported for SARS-CoV-1, 4,5 and our findings were more consistent with those of Long et al. 1 Our findings raise concern that humoral immunity against SARS-CoV-2 may not be long lasting in persons with mild illness, who compose the majority of persons with Covid-19. It is difficult to extrapolate beyond our observation period of approximately 90 days because it is likely that the decay will decelerate. 3 Still, the results call for caution regarding antibody-based “immunity passports,” herd immunity, and perhaps vaccine durability, especially in light of short-lived immunity against common human coronaviruses. Further studies will be needed to define a quantitative protection threshold and rate of decline of antiviral antibodies beyond 90 days.

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IgA dominates the early neutralizing antibody response to SARS-CoV-2

Delphine Sterlin, Alexis Mathian, Makoto Miyara … (2020)

Early specific antibody responses against SARS-CoV-2 include IgG, IgM, and IgA, but IgA may neutralize virus and control infection to a larger extent.

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Risk factors and disease profile of post-vaccination SARS-CoV-2 infection in UK users of the COVID Symptom Study app: a prospective, community-based, nested, case-control study

Michela Antonelli, Rose S Penfold, Jordi Merino … (2021)

Background COVID-19 vaccines show excellent efficacy in clinical trials and effectiveness in real-world data, but some people still become infected with SARS-CoV-2 after vaccination. This study aimed to identify risk factors for post-vaccination SARS-CoV-2 infection and describe the characteristics of post-vaccination illness. Methods This prospective, community-based, nested, case-control study used self-reported data (eg, on demographics, geographical location, health risk factors, and COVID-19 test results, symptoms, and vaccinations) from UK-based, adult (≥18 years) users of the COVID Symptom Study mobile phone app. For the risk factor analysis, cases had received a first or second dose of a COVID-19 vaccine between Dec 8, 2020, and July 4, 2021; had either a positive COVID-19 test at least 14 days after their first vaccination (but before their second; cases 1) or a positive test at least 7 days after their second vaccination (cases 2); and had no positive test before vaccination. Two control groups were selected (who also had not tested positive for SARS-CoV-2 before vaccination): users reporting a negative test at least 14 days after their first vaccination but before their second (controls 1) and users reporting a negative test at least 7 days after their second vaccination (controls 2). Controls 1 and controls 2 were matched (1:1) with cases 1 and cases 2, respectively, by the date of the post-vaccination test, health-care worker status, and sex. In the disease profile analysis, we sub-selected participants from cases 1 and cases 2 who had used the app for at least 14 consecutive days after testing positive for SARS-CoV-2 (cases 3 and cases 4, respectively). Controls 3 and controls 4 were unvaccinated participants reporting a positive SARS-CoV-2 test who had used the app for at least 14 consecutive days after the test, and were matched (1:1) with cases 3 and 4, respectively, by the date of the positive test, health-care worker status, sex, body-mass index (BMI), and age. We used univariate logistic regression models (adjusted for age, BMI, and sex) to analyse the associations between risk factors and post-vaccination infection, and the associations of individual symptoms, overall disease duration, and disease severity with vaccination status. Findings Between Dec 8, 2020, and July 4, 2021, 1 240 009 COVID Symptom Study app users reported a first vaccine dose, of whom 6030 (0·5%) subsequently tested positive for SARS-CoV-2 (cases 1), and 971 504 reported a second dose, of whom 2370 (0·2%) subsequently tested positive for SARS-CoV-2 (cases 2). In the risk factor analysis, frailty was associated with post-vaccination infection in older adults (≥60 years) after their first vaccine dose (odds ratio [OR] 1·93, 95% CI 1·50–2·48; p<0·0001), and individuals living in highly deprived areas had increased odds of post-vaccination infection following their first vaccine dose (OR 1·11, 95% CI 1·01–1·23; p=0·039). Individuals without obesity (BMI <30 kg/m 2 ) had lower odds of infection following their first vaccine dose (OR 0·84, 95% CI 0·75–0·94; p=0·0030). For the disease profile analysis, 3825 users from cases 1 were included in cases 3 and 906 users from cases 2 were included in cases 4. Vaccination (compared with no vaccination) was associated with reduced odds of hospitalisation or having more than five symptoms in the first week of illness following the first or second dose, and long-duration (≥28 days) symptoms following the second dose. Almost all symptoms were reported less frequently in infected vaccinated individuals than in infected unvaccinated individuals, and vaccinated participants were more likely to be completely asymptomatic, especially if they were 60 years or older. Interpretation To minimise SARS-CoV-2 infection, at-risk populations must be targeted in efforts to boost vaccine effectiveness and infection control measures. Our findings might support caution around relaxing physical distancing and other personal protective measures in the post-vaccination era, particularly around frail older adults and individuals living in more deprived areas, even if these individuals are vaccinated, and might have implications for strategies such as booster vaccinations. Funding ZOE, the UK Government Department of Health and Social Care, the Wellcome Trust, the UK Engineering and Physical Sciences Research Council, UK Research and Innovation London Medical Imaging and Artificial Intelligence Centre for Value Based Healthcare, the UK National Institute for Health Research, the UK Medical Research Council, the British Heart Foundation, and the Alzheimer's Society.

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Author and article information

Contributors

Marianna Karachaliou:

ORCID: http://orcid.org/0000-0002-3014-0747

marianna.karachaliou@isglobal.org

Carlota Dobaño: carlota.dobano@isglobal.org

Journal

Journal ID (nlm-ta): BMC Med

Journal ID (iso-abbrev): BMC Med

Title: BMC Medicine

Publisher: BioMed Central (London )

ISSN (Electronic): 1741-7015

Publication date (Electronic): 16 September 2022

Publication date PMC-release: 16 September 2022

Publication date Collection: 2022

Volume: 20

Electronic Location Identifier: 347

Affiliations

[1 ]GRID grid.434607.2, ISNI 0000 0004 1763 3517, Barcelona Institute for Global Health (ISGlobal), ; Doctor Aiguader, 88, 08003 Barcelona, Spain

[2 ]GRID grid.430579.c, ISNI 0000 0004 5930 4623, Centro de Investigación Biomédica en Red de Enfermedades Infecciosas (CIBERINFEC), ; Barcelona, Spain

[3 ]GRID grid.466571.7, ISNI 0000 0004 1756 6246, Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública (CIBERESP), ; 08036 Madrid, Spain

[4 ]GRID grid.5612.0, ISNI 0000 0001 2172 2676, Universitat Pompeu Fabra (UPF), ; Barcelona, Spain

[5 ]GRID grid.20522.37, ISNI 0000 0004 1767 9005, Hospital del Mar Medical Research Institute (IMIM), ; 08003 Barcelona, Spain

[6 ]Genomes for Life-GCAT lab. Institute for Health Science Research Germans Trias i Pujol (IGTP), Badalona, Spain

[7 ]GRID grid.438280.5, Banc de Sang i Teixits (BST), ; Barcelona, Spain

[8 ]GRID grid.11478.3b, ISNI 0000 0004 1766 3695, Centre for Genomic Regulation (CRG), ; Barcelona, Spain

[9 ]GRID grid.10403.36, ISNI 0000000091771775, Institut d’Investigacions Biomèdiques August Pi Sunyer (IDIBAPS), ; Barcelona, Spain

[10 ]GRID grid.22072.35, ISNI 0000 0004 1936 7697, Department of Microbiology, Immunology and Infectious Diseases, , Snyder Institute for Chronic Diseases, Cumming School of Medicine, University of Calgary, ; Calgary, Alberta Canada

[11 ]GRID grid.22937.3d, ISNI 0000 0000 9259 8492, Department of Epidemiology, , Center for Public Health, Medical University of Vienna, ; Vienna, Austria

[12 ]GRID grid.434607.2, ISNI 0000 0004 1763 3517, Barcelona Institute for Global Health (ISGlobal), ; Carrer Rosello 132, 08036 Barcelona, Spain

Author information

Marianna Karachaliou http://orcid.org/0000-0002-3014-0747

Article

Publisher ID: 2547

DOI: 10.1186/s12916-022-02547-2

PMC ID: 9479347

PubMed ID: 35073935

SO-VID: 968265f6-9427-417c-ac96-a8b40b994d68

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 8 April 2022

Date accepted : 1 September 2022

Funding

Funded by: Incentius a l’Avaluació de Centres CERCA

Funded by: FundRef http://dx.doi.org/10.13039/100014419, EIT HEALTH;

Award ID: BP2020-20873-Certify.Health

Funded by: FundRef http://dx.doi.org/10.13039/501100010336, Fundació Privada Daniel Bravo Andreu;

Award ID: PID2019-110810RB-I00

Funded by: FundRef http://dx.doi.org/10.13039/501100014550, Institut Català de la Salut;

Award ID: PERIS SLT017/20/000224

Award Recipient : Rocío Rubio

Funded by: Junta de Andalucía/EU.

Funded by: Spanish Ministry of Science and Innovation

Award ID: CEX2018-000806-S

Funded by: Acción de Dinamización del ISCIII

Custom metadata

ScienceOpen disciplines: Medicine

Keywords: covid-19 vaccines,sars-cov-2,antibody,kinetics,determinants,adults,smoking,comorbidities

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ScienceOpen disciplines: Medicine

Keywords: covid-19 vaccines, sars-cov-2, antibody, kinetics, determinants, adults, smoking, comorbidities

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SARS-CoV-2 infection, vaccination, and antibody response trajectories in adults: a cohort study in Catalonia

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Most cited references 40

Rapid Decay of Anti–SARS-CoV-2 Antibodies in Persons with Mild Covid-19

IgA dominates the early neutralizing antibody response to SARS-CoV-2

Risk factors and disease profile of post-vaccination SARS-CoV-2 infection in UK users of the COVID Symptom Study app: a prospective, community-based, nested, case-control study

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