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Figure.  Association of Self-reported Symptoms After SARS-CoV-2 Messenger RNA Vaccination With Continuous Log-Transformed Values for Anti-Spike IgG Antibodies Among 928 Fully Vaccinated Framingham Heart Study Participants, February 2021 to January 2022
Association of Self-reported Symptoms After SARS-CoV-2 Messenger RNA Vaccination With Continuous Log-Transformed Values for Anti-Spike IgG Antibodies Among 928 Fully Vaccinated Framingham Heart Study Participants, February 2021 to January 2022

Effect estimates for self-reported symptoms compared with no symptoms with 95% CIs. Plus signs indicate that those factors were sequentially added to the model.

aMedical factors include body mass index, smoking status, diabetes, hypertension, coronary heart disease, heart failure, stroke or transient ischemic attack, and estimated glomerular filtration rate.

Table.  Characteristics of Study Participants by Self-reported Symptoms After SARS-CoV-2 Messenger RNA Vaccinationa
Characteristics of Study Participants by Self-reported Symptoms After SARS-CoV-2 Messenger RNA Vaccinationa
1.
Bauernfeind  S, Salzberger  B, Hitzenbichler  F,  et al.  Association between reactogenicity and immunogenicity after vaccination with BNT162b2.   Vaccines (Basel). 2021;9(10):1089. doi:10.3390/vaccines9101089 PubMedGoogle ScholarCrossref
2.
Held  J, Esse  J, Tascilar  K,  et al.  Reactogenicity correlates only weakly with humoral immunogenicity after COVID-19 vaccination with BNT162b2 mRNA (Comirnaty®).   Vaccines (Basel). 2021;9(10):1063. doi:10.3390/vaccines9101063 PubMedGoogle ScholarCrossref
3.
Hwang  YH, Song  KH, Choi  Y,  et al.  Can reactogenicity predict immunogenicity after COVID-19 vaccination?   Korean J Intern Med. 2021;36(6):1486-1491. doi:10.3904/kjim.2021.210 PubMedGoogle ScholarCrossref
4.
Oelsner  EC, Krishnaswamy  A, Balte  PP,  et al; for the C4R Investigators.  Collaborative cohort of cohorts for COVID-19 research (C4R) study: study design.   Am J Epidemiol. 2022;191(7):1153-1173. doi:10.1093/aje/kwac032 PubMedGoogle ScholarCrossref
5.
Styer  LM, Hoen  R, Rock  J,  et al.  High-throughput multiplex SARS-CoV-2 IgG microsphere immunoassay for dried blood spots: a public health strategy for enhanced serosurvey capacity.   Microbiol Spectr. 2021;9(1):e0013421. doi:10.1128/Spectrum.00134-21 PubMedGoogle ScholarCrossref
6.
Debes  AK, Xiao  S, Colantuoni  E,  et al.  Association of vaccine type and prior SARS-CoV-2 infection with symptoms and antibody measurements following vaccination among health care workers.   JAMA Intern Med. 2021;181(12):1660-1662. doi:10.1001/jamainternmed.2021.4580 PubMedGoogle ScholarCrossref
2 Comments for this article
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Statistical comments
Stacia DeSantis, PhD Biostatistics | University of Texas Health Science Center
We read with great interest the Research Letter, “Association of Symptoms After COVID-19 Vaccination with Anti–SARS-CoV-2 Antibody Response in the Framingham Heart Study,” by Hermann, et al published in JAMA Network Open on Oct 21, 2022.

The Framingham Heart Study (FHS) cohort has been valuable for the epidemiological assessment of cardiovascular disease risk factors as well as many other outcomes. In this Letter, Hermann, et al characterize post vaccination symptoms in a subset of FHS participants receiving two doses of mRNA-1273 SARS-CoV-2 vaccine to determine whether development of no versus local versus systemic post-vaccination symptoms, was associated with a
positive result on SARS-CoV-2 antibodies. This is an important analysis to conduct. Per authors, “A 2-sided P < .05 was considered statistically significant.”

However, 98% (N=365), 99% (N=108), and 99% (N=44) who were asymptomatic, locally symptomatic, and systemically symptomatic, respectively, had antibody reactivity upon Immunoglobin (IgG) assay. This 1% difference was not statistically significantly different despite the study’s large sample size (p=0.08 by chi square test). Further, the paper’s Figure shows that after adjustment of multiple established medical factors known to predict immune response, there is no statistical difference in anti-SARS-Cov-2 IgG titers in those with local symptoms only vs those with local and/or systemic symptoms (given the overlap of the 95% confidence interval). But is also unclear why the groupings within a Factor are not mutually exclusive, and why authors do not include those without symptoms at all, rendering the Figure missing critical information.

In sum, given a nearly identical percentage of vaccinated individuals with and without post-vaccination symptoms who tested positive for antibodies, and insignificant p-value, the conclusions of this study “In a sample of twice-vaccinated, older, community-dwelling US adults, self-reported systemic symptoms after SARS-CoV-2 mRNA vaccination were associated with greater antibody response vs local-only or no symptoms” may overstate the findings given the authors’ 0.05 alpha threshold, and/or may need further characterization.
CONFLICT OF INTEREST: None Reported
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Response to Statistical Comments
Emilia Hermann, MD, MPH | Division of General Medicine, Department of Medicine, Columbia University
The authors would like to thank Dr. DeSantis for her comment and for highlighting two important findings of our work:

First, we did not observe a statistically significant difference in antibody reactivity across groups with no symptoms, local only symptoms, and systemic symptoms after vaccination (p=0.08 by chi-square test). Nearly all participants, regardless of post-vaccination symptoms, developed an anti-S antibody response to vaccination. This finding serves to highlight the effectiveness of available mRNA vaccines in eliciting an immune response.

Our second key finding is highlighted in the figure. We compared antibody response in three mutually exclusive groups: participants
with systemic symptoms (with or without local symptoms), participants with local symptoms only, and participants with no symptoms. A correction to the figure label has been made to clarify these distinct categories of post-vaccination symptoms. The group with no symptoms was treated as the referent category in the analyses. Compared to participants with no symptoms, those with systemic symptoms (with or without local symptoms) had statistically significantly higher antibody levels, even after adjustment for multiple factors known to predict immune response.
CONFLICT OF INTEREST: None Reported
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Research Letter
Public Health
October 21, 2022

Association of Symptoms After COVID-19 Vaccination With Anti–SARS-CoV-2 Antibody Response in the Framingham Heart Study

Author Affiliations
  • 1Division of General Medicine, Department of Medicine, Columbia University, New York, New York
  • 2Department of Pediatrics, Larner College of Medicine at the University of Vermont, Burlington
  • 3Department of Medicine, Boston University School of Medicine, Boston, Massachusetts
  • 4Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts
  • 5Department of Medicine, Larner College of Medicine at the University of Vermont, Burlington
  • 6Department of Microbiology and Molecular Genetics, Larner College of Medicine, University of Vermont, Burlington
JAMA Netw Open. 2022;5(10):e2237908. doi:10.1001/jamanetworkopen.2022.37908
Introduction

SARS-CoV-2 messenger RNA (mRNA) vaccines (BNT162b2 [Pfizer-BioNTech] and mRNA-1273 [Moderna]) are associated with local and systemic symptoms; however, whether postvaccination symptoms are associated with vaccine-induced antibody response is unknown. Previous studies1-3 of COVID-19 vaccine reactogenicity and immunogenicity were limited to convenience samples that may not be generalizable. We studied the association of self-reported postvaccination symptoms with anti–SARS-CoV-2 antibody response among Framingham Heart Study (FHS) participants contributing to the Collaborative Cohort of Cohorts for COVID-19 Research (C4R) study.4

Methods

The FHS is an ongoing, prospective cohort study evaluating cardiovascular disease risk factors. In February 2021, participants were invited to self-administer C4R questions on COVID-19 vaccination (and associated symptoms) and submit a dried blood spot to test for anti–SARS-CoV-2 antibodies (eFigure in the Supplement). This report includes participants who received 2 doses of mRNA vaccine at least 2 weeks before blood spot collection. Postvaccination symptoms were categorized as systemic symptoms (fever, chills, muscle pain, nausea, vomiting, headache, and/or moderate to severe fatigue) or local symptoms (injection site pain and/or rash). IgG antibodies to SARS-CoV-2 spike subunit were measured using microsphere immunoassay (Luminex), chosen for its successful use in population-based serosurveys. Results were reported as median fluorescence intensity (MFI), with batch-specific reactive antibody response MFI cutoffs.5 Associations between postvaccination symptoms and antibody response were assessed by χ2 test and multivariable linear regression, with complete case analyses adjusted for batch, time since vaccination, and sociodemographic and clinical characteristics. A 2-sided P < .05 was considered statistically significant. Protocols were approved by institutional review boards of participating institutions and the National Heart, Lung, and Blood Institute. Written informed consent was obtained from all participants. This study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline.

Results

Of 3200 FHS participants eligible to participate in C4R, 928 (29%) completed the C4R questionnaire and blood spot collection and reported 2 doses of BNT162b2 (414 [45%]) or mRNA-1273 (514 [55%]) vaccines (eFigure in the Supplement). Respondents’ mean (SD) age was 65 (12) years, 360 (39%) were men and 568 (61%) were women, 893 (96%) were non-Hispanic White, and 84 (9%) self-reported prior COVID-19 infection. After either vaccine dose, 446 participants (48%) reported systemic symptoms, 109 (12%) reported local symptoms only, and 373 (40%) reported no symptoms. In bivariate analysis, symptoms were associated with younger age, female sex, prior infection, and the mRNA-1273 vaccine (Table). Antibody reactivity was observed in 365 asymptomatic participants (98%), 108 participants (99%) with only local symptoms, and 444 participants (99%) with systemic symptoms (P = .08). In adjusted models, systemic symptoms were associated with greater antibody response, although associations were attenuated with sequential adjustment for potential confounders (Figure). Similar results were obtained with exclusion of participants with prior COVID-19 infection.

Discussion

In a sample of twice-vaccinated, older, community-dwelling US adults, self-reported systemic symptoms after SARS-CoV-2 mRNA vaccination were associated with greater antibody response vs local-only or no symptoms, although associations were attenuated with sequential adjustment for potential confounders. These results agree with a previous report6 in US health care workers that showed higher postvaccination antibody measurements among those with significant symptoms after an mRNA vaccine. This report identifies age, sex, and Moderna vaccine as factors associated with both vaccine reactogenicity and immunogenicity, consistent with prior observations.3,6 No association was observed between symptoms after vaccination and race or ethnicity, body mass index, or comorbidities. In this generalizable cohort, nearly all participants exhibited a positive antibody response to complete mRNA vaccine series. Nonetheless, systemic symptoms remained associated with greater antibody response in multivariable-adjusted models, highlighting unexplained interpersonal variability. Further research on biological mechanisms underlying heterogeneity in vaccine response is needed. Limitations of this report include an older, predominantly non-Hispanic White, professional cohort; potential recall bias; and use of MFI, which is not standardized against neutralizing antibody titers. In conclusion, these findings support reframing postvaccination symptoms as signals of vaccine effectiveness and reinforce guidelines for vaccine boosters in older adults.

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Article Information

Accepted for Publication: September 7, 2022.

Published: October 21, 2022. doi:10.1001/jamanetworkopen.2022.37908

Correction: This article was corrected on November 28, 2022, to fix some incorrect row headers in the Figure and to add some missing information regarding attenuation of the reported associations in the first sentence of the Discussion.

Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2022 Hermann EA et al. JAMA Network Open.

Corresponding Author: Emilia A. Hermann, MD, MPH, Division of General Medicine, Department of Medicine, Columbia University Medical Center, 630 W 168th St, PH 9 East, Room 105, New York, NY 10032 (eah2191@cumc.columbia.edu).

Author Contributions: Drs Hermann and Balte had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Hermann, Lee, Kirkpatrick, Oelsner.

Acquisition, analysis, or interpretation of data: Hermann, Balte, Xanthakis, Kirkpatrick, Cushman, Oelsner.

Drafting of the manuscript: Hermann, Lee, Kirkpatrick, Oelsner.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Hermann, Balte, Oelsner.

Obtained funding: Cushman, Oelsner.

Administrative, technical, or material support: Kirkpatrick, Cushman, Oelsner.

Supervision: Kirkpatrick, Oelsner.

Conflict of Interest Disclosures: Dr Balte reported receiving grants from the National Institutes of Health during the conduct of the study. Dr Oelsner reported receiving grants from the National Heart, Lung, and Blood Institute during the conduct of the study and outside the submitted work. No other disclosures were reported.

Funding/Support: This research was funded in part by agreement 1OT2HL156812 from the National Institutes of Health.

Role of the Funder/Sponsor: The funding source had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Disclaimer: The views and conclusions contained in this document are those of the authors and should not be interpreted as representing the official policies, either expressed or implied, of the National Institutes of Health.

References
1.
Bauernfeind  S, Salzberger  B, Hitzenbichler  F,  et al.  Association between reactogenicity and immunogenicity after vaccination with BNT162b2.   Vaccines (Basel). 2021;9(10):1089. doi:10.3390/vaccines9101089 PubMedGoogle ScholarCrossref
2.
Held  J, Esse  J, Tascilar  K,  et al.  Reactogenicity correlates only weakly with humoral immunogenicity after COVID-19 vaccination with BNT162b2 mRNA (Comirnaty®).   Vaccines (Basel). 2021;9(10):1063. doi:10.3390/vaccines9101063 PubMedGoogle ScholarCrossref
3.
Hwang  YH, Song  KH, Choi  Y,  et al.  Can reactogenicity predict immunogenicity after COVID-19 vaccination?   Korean J Intern Med. 2021;36(6):1486-1491. doi:10.3904/kjim.2021.210 PubMedGoogle ScholarCrossref
4.
Oelsner  EC, Krishnaswamy  A, Balte  PP,  et al; for the C4R Investigators.  Collaborative cohort of cohorts for COVID-19 research (C4R) study: study design.   Am J Epidemiol. 2022;191(7):1153-1173. doi:10.1093/aje/kwac032 PubMedGoogle ScholarCrossref
5.
Styer  LM, Hoen  R, Rock  J,  et al.  High-throughput multiplex SARS-CoV-2 IgG microsphere immunoassay for dried blood spots: a public health strategy for enhanced serosurvey capacity.   Microbiol Spectr. 2021;9(1):e0013421. doi:10.1128/Spectrum.00134-21 PubMedGoogle ScholarCrossref
6.
Debes  AK, Xiao  S, Colantuoni  E,  et al.  Association of vaccine type and prior SARS-CoV-2 infection with symptoms and antibody measurements following vaccination among health care workers.   JAMA Intern Med. 2021;181(12):1660-1662. doi:10.1001/jamainternmed.2021.4580 PubMedGoogle ScholarCrossref
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