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. 2022 Mar 8;40(11):1634-1642.
doi: 10.1016/j.vaccine.2021.02.047. Epub 2021 Mar 4.

Sex-specific effects of age and body mass index on antibody responses to seasonal influenza vaccines in healthcare workers

Helen Kuo  1 , Janna R Shapiro  1 , Santosh Dhakal  2 , Rosemary Morgan  1 , Ashley L Fink  2 , Hsuan Liu  2 , Jason W Westerbeck  2 , Kristyn E Sylvia  2 , Han-Sol Park  2 , Rebecca L Ursin  3 , Patrick Shea  2 , Kathryn Shaw-Saliba  4 , Katherine Fenstermacher  4 , Richard Rothman  4 , Andrew Pekosz  5 , Sabra L Klein  6
Affiliations

Sex-specific effects of age and body mass index on antibody responses to seasonal influenza vaccines in healthcare workers

Helen Kuo et al. Vaccine. .

Abstract

Healthcare institutions with mandatory influenza vaccination policies have over 90% vaccination rates among healthcare workers (HCWs) resulting in a population that has received the influenza vaccine in many, consecutive years. This study explored the impact of sex and other host factors in pre- and post-vaccination neutralizing antibody (nAb) titers and seroconversion against the H1N1 and H3N2 influenza A viruses (IAVs) among HCWs enrolled into a cross-sectional serosurvey during the annual Johns Hopkins Hospital employee vaccination campaign in the 2017-18 and 2018-19 seasons. The study enrolled 111 participants (male = 38, female = 73) in 2017-18 and 163 (male = 44, female = 119) in 2018-19. Serum samples were collected immediately prior to vaccination and approximately 28 days later and nAb titers to vaccine strains determined. An intersectional approach was used to disaggregate the combined effects of sex with age and body mass index (BMI) in the nAb response. Differences between the pre- or post-vaccination geometric mean nAb titers between male and female HCWs were not observed. Male HCWs were 2.86 times more likely to seroconvert compared to female HCWs in 2017-2018, but the same trend was not observed in the following year. When data were disaggregated by age and sex, older female HCWs had higher H1N1 pre- and post-vaccination nAb titers compared to male HCWs in the same age group for both vaccination campaign seasons. In both years, the decline in H3N2 pre-vaccination titers with increasing BMI was greater in female than male HCW. The sex-specific effects of age and BMI on nAb responses to seasonal influenza vaccines require greater consideration.

Keywords: Aging; Body mass index; Neutralizing antibody; Obesity; Sex difference; Vaccine efficacy.

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Conflict of interest statement

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Figure 1:
Figure 1:. Healthcare workers (HCWs) who did not seroconvert had higher pre-vaccination titers than those who seroconverted.
Log2-transformed neutralizing antibody (nAb) titers pre- and 28 days post-vaccination are shown for HCWs who seroconverted (gray) and those who did not (white) to H1N1 in the 2017-18 season (A), H1N1 in the 2018-19 season (B), H3N2 in the 2017-18 season (C), and H3N2 in the 2018-19 season (D). Dashed lines indicate the median titer for each group and dotted lines indicated the 25th and 75th percentiles. Differences between those who seroconverted and those who did not at each time point for each strain and between pre- and post-vaccination titers were calculated using two-tailed t-tests. Asterisks indicate the significance level with * = p-value <0.05 and **** = p-value <0.0001.
Figure 2:
Figure 2:. Odds of seroconversion are affected by pre-vaccination titers.
Multiple logistic regression models were used to analyze the impact of sex, BMI, race, and the presence of comorbidities on the odds of seroconverting to H1N1 (A) and H3N2 (B) during the 2017-18 and 2018-19 seasons. Point estimates of the log odds ratios with 95% confidence intervals are depicted separately for the 2017-18 (circles) and 2018-19 (squares) seasons. Simple logistic regressions were used to analyze the impact of pre-vaccination titers on the odds of seroconverting to H1N1 (C) and H3N2 (D) titers for males and females in each season. The odds ratios and 95% confidence are depicted. * = p-value < 0.05.
Figure 3:
Figure 3:. Neutralizing antibody titers increased after receiving an influenza vaccine for both male and female HCWs.
Log2-transformed neutralizing antibody titers pre- and 28 days post-vaccination are shown for female (black) and male (white) HCWs to H1N1 in the 2017-18 season (A), H1N1 in the 2018-19 season (B), H3N2 in the 2017-18 season (C), and H3N2 in the 2018-19 season (D). Dashed lines indicate the median titer for each group and dotted lines indicated the 25th and 75th percentiles. Differences between female and male HCWs at each time point for each strain and between pre- and post-vaccination titers were calculated using two-tailed t-tests. Asterisks indicate the significance level with * = p-value <0.05, ** = p-value <0.01, *** = p-value <0.001 and **** = p-value <0.0001.
Figure 4:
Figure 4:. Age intersects with sex to impact neutralizing antibody (nAb) titers in HCWs.
Simple linear regression models were used to analyze the effect of age on nAb titers separately for male and female HCWs before vaccination in H1N1 2017-18 season (A), 28 days post-vaccination H1N1 in the 2017-18 season (B), before vaccination in H1N1 2018-19 season (C), 28 days post-vaccination H1N1 in the 2018-19 season (D), before vaccination in H3N2 in the 2017-18 season (E), and 28 days post-vaccination H3N2 in the 2017-18 season (F) before vaccination in H3N2 in the 2018-19 season (G), and 28 days post-vaccination H3N2 in the 2018-19 season (H).
Figure 5:
Figure 5:. Body mass index (BMI) interacts to sex to affect H3N2 nAb titers in HCWs.
Simple linear regression models were used to analyze the effect of BMI on nAb titers separately for male and female HCWs before vaccination in H3N2 2017-18 season (A), 28 days post-vaccination H3N2 in the 2017-18 season (B), before vaccination in H3N2 2018-19 season (C), 28 days post-vaccination H2N2 in the 2018-19 season (D).
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