Citation: Ngare, I.; Tan, T.S.; Toyoda,
M.; Kuwata, T.; Takahama, S.;
Nakashima, E.; Yamasaki, N.;
Motozono, C.; Fujii, T.; Minami, R.;
et al. Factors Associated with
Neutralizing Antibody Responses
following 2-Dose and 3rd Booster
Monovalent COVID-19 Vaccination in
Japanese People Living with HIV.
Viruses 2024, 16, 555. https://doi.org/
10.3390/v16040555
Academic Editor: Cynthia Derdeyn
Received: 8 February 2024
Revised: 8 March 2024
Accepted: 25 March 2024
Published: 2 April 2024
Copyright: © 2024 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
viruses
Article
Factors Associated with Neutralizing Antibody Responses
following 2-Dose and 3rd Booster Monovalent COVID-19
Vaccination in Japanese People Living with HIV
Isaac Ngare
1,2
, Toong Seng Tan
1
, Mako Toyoda
1
, Takeo Kuwata
1
, Soichiro Takahama
3
, Eriko Nakashima
3
,
Naoya Yamasaki
4
, Chihiro Motozono
1
, Teruhisa Fujii
4
, Rumi Minami
3
, Godfrey Barabona
1
and
Takamasa Ueno
1,2,5,
*
1
Joint Research Center for Human Retrovirus Infection, Kumamoto University, 2-2-1 Honjo, Chuo-ku,
Kumamoto 860-8555, Japan; ngareisaac@yahoo.com (I.N.); tstan@mgh.harvard.edu (T.S.T.);
makotoyo@kumamoto-u.ac.jp (M.T.); tkuwata@kumamoto-u.ac.jp (T.K.);
motozono@kumamoto-u.ac.jp (C.M.); barabona@kumamoto-u.ac.jp (G.B.)
2
Graduate School of Medical Sciences, Kumamoto University, 1-1-1 Honjo, Chuo-ku,
Kumamoto 860-0811, Japan
3
NHO, Kyushu Medical Center, 1-8-1 Jigyohama, Chuo-ku, Fukuoka 810-8563, Japan;
takahama.soichiro.bt@mail.hosp.go.jp (S.T.); nakashima.eriko.rj@mail.hosp.go.jp (E.N.);
minami.rumi.ad@mail.hosp.go.jp (R.M.)
4
Division of Transfusion Medicine, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-ku,
Hiroshima 734-8551, Japan; naoya64@hiroshima-u.ac.jp (N.Y.); teruchan@hiroshima-u.ac.jp (T.F.)
5
Joint Research Center for Human Retrovirus Infection, Kagoshima University, 8-35-1, Sakuragaoka,
Kagoshima 890-8544, Japan
* Correspondence: uenotaka@kumamoto-u.ac.jp
Abstract: People living with HIV (PLWH) could be at risk of blunted immune responses to COVID-19
vaccination. We investigated factors associated with neutralizing antibody (NAb) responses against
SARS-CoV-2 and variants of concern (VOCs), following two-dose and third booster monovalent
COVID-19 mRNA vaccination in Japanese PLWH. NAb titers were assessed in polyclonal IgG
fractions by lentiviral-based pseudovirus assays. Overall, NAb titers against Wuhan, following two-
dose vaccination, were assessed in 82 PLWH on treatment, whereby 17/82 (20.73%) were classified
as low-NAb participants. Within the low-NAb participants, the third booster vaccination enhanced
NAb titers against Wuhan and VOCs, albeit to a significantly lower magnitude than the rest. In the
multivariate analysis, NAb titers against Wuhan after two-dose vaccination correlated with age and
days since vaccination, but not with CD4
+
count, CD4
+
/CD8
+
ratio, and plasma high-sensitivity
C-Reactive protein (hsCRP). Interestingly, an extended analysis within age subgroups revealed NAb
titers to correlate positively with the CD4
+
count and negatively with plasma hsCRP in younger,
but not older, participants. In conclusion, a third booster vaccination substantially enhances NAb
titers, but the benefit may be suboptimal in subpopulations of PLWH exhibiting low titers at baseline.
Considering clinical and immune parameters could provide a nuanced understanding of factors
associated with vaccine responses in PLWH.
Keywords: SARS-CoV-2; neutralizing antibodies; COVID-19 vaccination; HIV; variants of concern
1. Introduction
The rollout of global COVID-19 vaccination raised concerns over the ability of people
living with HIV (PLWH) to elicit optimal immune responses given their underrepresen-
tation in preceding clinical trials [1,2]. A growing body of literature now suggests that
although PLWH on antiretroviral therapy (ART) can mount antibody responses at a compa-
rable magnitude to non-HIV-infected individuals [3,4], certain subpopulations of PLWH,
such as those with suboptimal CD4
+
count recovery, have shown attenuated antibody
Viruses 2024, 16, 555. https://doi.org/10.3390/v16040555 https://www.mdpi.com/journal/viruses