Antibody response durability following three-dose coronavirus disease 2019 vaccination in people with HIV receiving suppressive antiretroviral therapy.
Journal
AIDS (London, England)
ISSN: 1473-5571
Titre abrégé: AIDS
Pays: England
ID NLM: 8710219
Informations de publication
Date de publication:
01 04 2023
01 04 2023
Historique:
pubmed:
23
12
2022
medline:
17
3
2023
entrez:
22
12
2022
Statut:
ppublish
Résumé
Limited data exist regarding longer term antibody responses following three-dose coronavirus disease 2019 (COVID-19) vaccination, and the impact of a first SARS-CoV-2 infection during this time, in people with HIV (PWH) receiving suppressive antiretroviral therapy (ART). We quantified wild-type-specific, Omicron BA.1-specific and Omicron BA.5-specific responses up to 6 months post-third dose in 64 PWH and 117 controls who remained COVID-19-naive or experienced their first SARS-CoV-2 infection during this time. Longitudinal observational cohort. We quantified wild-type-specific and Omicron-specific anti-Spike receptor-binding domain IgG concentrations, ACE2 displacement activities and live virus neutralization at 1, 3 and 6 months post-third vaccine dose. Third doses boosted all antibody measures above two-dose levels, but BA.1-specific responses remained significantly lower than wild-type-specific ones, with BA.5-specific responses lower still. Serum IgG concentrations declined at similar rates in COVID-19-naive PWH and controls post-third dose (median wild-type-specific and BA.1-specific half-lives were between 66 and 74 days for both groups). Antibody function also declined significantly yet comparably between groups: 6 months post-third dose, BA.1-specific neutralization was undetectable in more than 80% of COVID-19 naive PWH and more than 90% of controls. Breakthrough SARS-CoV-2 infection boosted antibody concentrations and function significantly above vaccine-induced levels in both PWH and controls, though BA.5-specific neutralization remained significantly poorer than BA.1 even post-breakthrough. Following three-dose COVID-19 vaccination, antibody response durability in PWH receiving ART is comparable with controls. PWH also mounted strong responses to breakthrough infection. Due to temporal response declines, however, COVID-19-naive individuals, regardless of HIV status, would benefit from a fourth dose within 6 months of their third.
Sections du résumé
BACKGROUND
Limited data exist regarding longer term antibody responses following three-dose coronavirus disease 2019 (COVID-19) vaccination, and the impact of a first SARS-CoV-2 infection during this time, in people with HIV (PWH) receiving suppressive antiretroviral therapy (ART). We quantified wild-type-specific, Omicron BA.1-specific and Omicron BA.5-specific responses up to 6 months post-third dose in 64 PWH and 117 controls who remained COVID-19-naive or experienced their first SARS-CoV-2 infection during this time.
DESIGN
Longitudinal observational cohort.
METHODS
We quantified wild-type-specific and Omicron-specific anti-Spike receptor-binding domain IgG concentrations, ACE2 displacement activities and live virus neutralization at 1, 3 and 6 months post-third vaccine dose.
RESULTS
Third doses boosted all antibody measures above two-dose levels, but BA.1-specific responses remained significantly lower than wild-type-specific ones, with BA.5-specific responses lower still. Serum IgG concentrations declined at similar rates in COVID-19-naive PWH and controls post-third dose (median wild-type-specific and BA.1-specific half-lives were between 66 and 74 days for both groups). Antibody function also declined significantly yet comparably between groups: 6 months post-third dose, BA.1-specific neutralization was undetectable in more than 80% of COVID-19 naive PWH and more than 90% of controls. Breakthrough SARS-CoV-2 infection boosted antibody concentrations and function significantly above vaccine-induced levels in both PWH and controls, though BA.5-specific neutralization remained significantly poorer than BA.1 even post-breakthrough.
CONCLUSION
Following three-dose COVID-19 vaccination, antibody response durability in PWH receiving ART is comparable with controls. PWH also mounted strong responses to breakthrough infection. Due to temporal response declines, however, COVID-19-naive individuals, regardless of HIV status, would benefit from a fourth dose within 6 months of their third.
Identifiants
pubmed: 36545783
doi: 10.1097/QAD.0000000000003469
pii: 00002030-202304010-00002
pmc: PMC9994797
doi:
Substances chimiques
COVID-19 Vaccines
0
Immunoglobulin G
0
Antibodies, Viral
0
Antibodies, Neutralizing
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
709-721Subventions
Organisme : Wellcome Trust
ID : 107752/Z/15/Z
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Informations de copyright
Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc.
Références
Barda N, Dagan N, Cohen C, Hernan MA, Lipsitch M, Kohane IS, et al. Effectiveness of a third dose of the BNT162b2 mRNA COVID-19 vaccine for preventing severe outcomes in Israel: an observational study . Lancet 2021; 398:2093–2100.
Eliakim-Raz N, Leibovici-Weisman Y, Stemmer A, Ness A, Awwad M, Ghantous N, et al. Antibody titers before and after a third dose of the SARS-CoV-2 BNT162b2 vaccine in adults aged >/=60 years . JAMA 2021; 326:2203–2204.
Moreira ED Jr, Kitchin N, Xu X, Dychter SS, Lockhart S, Gurtman A, et al. Safety and efficacy of a third dose of BNT162b2 Covid-19 vaccine . N Engl J Med 2022; 386:1910–1921.
Yoon SK, Hegmann KT, Thiese MS, Burgess JL, Ellingson K, Lutrick K, et al. HEROES-RECOVER Network Investigators, HEROES-RECOVER Network Investigators. Protection with a third dose of mRNA vaccine against SARS-CoV-2 variants in frontline workers . N Engl J Med 2022; 386:1855–1857.
Tegally H, Moir M, Everatt J, Giovanetti M, Scheepers C, Wilkinson E, et al. Emergence of SARS-CoV-2 Omicron lineages BA.4 and BA.5 in South Africa . Nat Med 2022; 28:1785–1790.
Abu-Raddad LJ, Chemaitelly H, Ayoub HH, AlMukdad S, Yassine HM, Al-Khatib HA, et al. Effect of mRNA vaccine boosters against SARS-CoV-2 Omicron infection in Qatar . N Engl J Med 2022; 386:1804–1816.
Andrews N, Stowe J, Kirsebom F, Toffa S, Rickeard T, Gallagher E, et al. Covid-19 vaccine effectiveness against the Omicron (B.1.1.529) variant . N Engl J Med 2022; 386:1532–1546.
Christensen PA, Olsen RJ, Long SW, Snehal R, Davis JJ, Ojeda Saavedra M, et al. Signals of significantly increased vaccine breakthrough, decreased hospitalization rates, and less severe disease in patients with coronavirus disease 2019 caused by the omicron variant of severe acute respiratory syndrome coronavirus 2 in Houston, Texas . Am J Pathol 2022; 192:642–652.
Stærke NB, Reekie J, Nielsen H, Benfield T, Wiese L, Knudsen LS, et al. Levels of SARS-CoV-2 antibodies among fully vaccinated individuals with Delta or Omicron variant breakthrough infections . Nat Commun 2022; 13:4466.
Seki Y, Yoshihara Y, Nojima K, Momose H, Fukushi S, Moriyama S, et al. Safety and immunogenicity of the Pfizer/BioNTech SARS-CoV-2 mRNA third booster vaccine dose against the BA.1 and BA.2 Omicron variants . Med (N Y) 2022; 3:406.e4–421.e4.
Seroprevalence in Canada. 2022. Available at: https://www.covid19immunitytaskforce.ca/seroprevalence-in-canada/ ; 2022. [Accessed 20 October 2022]
Epidemiological summary of COVID-19 cases in Canada. Public Health Agency of Canada; 2022.
Skowronski DM, Kaweski SE, Irvine MA, Kim S, Chuang ES, Sabaiduc S, et al. Serial cross-sectional estimation of vaccine-and infection-induced SARS-CoV-2 seroprevalence in British Columbia, Canada . CMAJ 2022; 194:E1599–E1609.
Lapointe HR, Mwimanzi F, Cheung PK, Sang Y, Yaseen F, Umviligihozo G, et al. People with HIV receiving suppressive antiretroviral therapy show typical antibody durability after dual COVID-19 vaccination, and strong third dose responses . J Infect Dis 2022; jiac229[Epub ahead of print].
Vergori A, Cozzi Lepri A, Cicalini S, Matusali G, Bordoni V, Lanini S, et al. HIV-VAC study group. Immunogenicity to COVID-19 mRNA vaccine third dose in people living with HIV . Nat Commun 2022; 13:4922.
Fidler S, Fox J, Tipoe T, Longet S, Tipton T, Abeywickrema M, et al. Booster vaccination against SARS-CoV-2 induces potent immune responses in people with HIV . Clin Infect Dis 2022; ciac796[Epub ahead of print].
Brumme ZL, Mwimanzi F, Lapointe HR, Cheung PK, Sang Y, Duncan MC, et al. Humoral immune responses to COVID-19 vaccination in people living with HIV receiving suppressive antiretroviral therapy . NPJ Vaccines 2022; 7:28.
BC Centre for Disease Control. Weekly update on variants of concern. 2022.
Mwimanzi F, Lapointe HR, Cheung PK, Sang Y, Yaseen F, Umviligihozo G, et al. Older adults mount less durable humoral responses to two doses of COVID-19 mRNA vaccine, but strong initial responses to a third dose . J Infect Dis 2022; 226:983–994.
Tan CW, Chia WN, Qin X, Liu P, Chen MI-C, Tiu C, et al. A SARS-CoV-2 surrogate virus neutralization test based on antibody-mediated blockage of ACE2–spike protein–protein interaction . Nat Biotechnol 2020; 38:1073–1078.
Government of British Columbia. Immunize BC: Covid-19 vaccines. Public Health Association of BC; 2022.
Lapointe HR, Mwimanzi F, Cheung PK, Sang Y, Yaseen F, Kalikawe R, et al. Serial infection with SARS-CoV-2 Omicron BA.1 and BA.2 following three-dose COVID-19 vaccination . Front Immunol 2022; 13:947021.
European Centre for Disease Control. Situation updates on COVID-19: SARS-CoV-2 variants of concern. 2022.
Government of Canada. COVID-19 epidemiology update. 2022.
Centers for Disease Control and Prevention U. COVID Data Tracker: variant proportions. 2022.
World Health Organization. Coronavirus update 80: what we know about new COVID-19 Variants of Concern. In: EPI-WIN Updates 2022.
Khan K, Karim F, Ganga Y, Bernstein M, Jule Z, Reedoy K, et al. Omicron BA.4/BA.5 escape neutralizing immunity elicited by BA. 1 infection . Nat Commun 2022; 13:4686.
Aggarwal A, Akerman A, Milogiannakis V, Silva MR, Walker G, Stella AO, et al. SARS-CoV-2 Omicron BA.5: Evolving tropism and evasion of potent humoral responses and resistance to clinical immunotherapeutics relative to viral variants of concern . EBioMedicine 2022; 84:104270.
Cao Y, Yisimayi A, Jian F, Song W, Xiao T, Wang L, et al. BA.2.12.1, BA.4 and BA.5 escape antibodies elicited by Omicron infection . Nature 2022; 608:593–602.
Nault L, Marchitto L, Goyette G, Tremblay-Sher D, Fortin C, Martel-Laferrière V, et al. Covid-19 vaccine immunogenicity in people living with HIV-1 . Vaccine 2022; 40:3633–3637.
Madhi SA, Koen AL, Izu A, Fairlie L, Cutland CL, Baillie V, et al. Wits VIDA COVID team. Safety and immunogenicity of the ChAdOx1 nCoV-19 (AZD1222) vaccine against SARS-CoV-2 in people living with and without HIV in South Africa: an interim analysis of a randomised, double-blind, placebo-controlled, phase 1B/2A trial . Lancet HIV 2021; 8:e568–e580.
Tuan JJ, Zapata H, Critch-Gilfillan T, Ryall L, Turcotte B, Mutic S, et al. Qualitative assessment of anti-SARS-CoV-2 spike protein immunogenicity (QUASI) after COVID-19 vaccination in older people living with HIV . HIV Med 2022; 23:178–185.
Frater J, Ewer KJ, Ogbe A, Pace M, Adele S, Adland E, et al. Oxford COVID Vaccine Trial Group. Safety and immunogenicity of the ChAdOx1 nCoV-19 (AZD1222) vaccine against SARS-CoV-2 in HIV infection: a single-arm substudy of a phase 2/3 clinical trial . Lancet HIV 2021; 8:e474–e485.
Woldemeskel BA, Karaba AH, Garliss CC, Beck EJ, Wang KH, Laeyendecker O, et al. The BNT162b2 mRNA vaccine elicits robust humoral and cellular immune responses in people living with human immunodeficiency virus (HIV) . Clin Infect Dis 2022; 74:1268–1270.
Hassold N, Brichler S, Ouedraogo E, Leclerc D, Carroue S, Gater Y, et al. Impaired antibody response to COVID-19 vaccination in advanced HIV infection . AIDS 2022; 36:F1–F5.
Spinelli MA, Peluso MJ, Lynch KL, Yun C, Glidden DV, Henrich TJ, et al. Differences in postmRNA vaccination severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) immunoglobulin G (IgG) concentrations and surrogate virus neutralization test response by human immunodeficiency virus (HIV) status and type of vaccine: a matched case-control observational study . Clin Infect Dis 2022; 75:e916–e919.
Antinori A, Cicalini S, Meschi S, Bordoni V, Lorenzini P, Vergori A, et al. HIV-VAC Study Group. Humoral and cellular immune response elicited by mRNA vaccination against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in people living with human immunodeficiency virus receiving antiretroviral therapy based on current CD4 T-lymphocyte count . Clin Infect Dis 2022; 75:e552–e563.
Jedicke N, Stankov MV, Cossmann A, Dopfer-Jablonka A, Knuth C, Ahrenstorf G, et al. Humoral immune response following prime and boost BNT162b2 vaccination in people living with HIV on antiretroviral therapy . HIV Med 2022; 23:558–563.
Coburn SB, Humes E, Lang R, Stewart C, Hogan BC, Gebo KA, et al. Corona-Infectious-Virus Epidemiology Team (CIVETs) of the NA-ACCORD of IeDEA. Analysis of postvaccination breakthrough COVID-19 infections among adults with HIV in the United States . JAMA Netw Open 2022; 5:e2215934.
Cao Y, Song W, Wang L, Liu P, Yue C, Jian F, et al. Characterization of the enhanced infectivity and antibody evasion of Omicron BA.2.75 . Cell Host Microbe 2022; 30:1527.e5–1539.e5.
Sheward DJ, Kim C, Fischbach J, Sato K, Muschiol S, Ehling RA, et al. Omicron sublineage BA.2.75. 2 exhibits extensive escape from neutralising antibodies . Lancet Infect Dis 2022; 22:1538–1540.
Qu P, Evans JP, Zheng YM, Carlin C, Saif LJ, Oltz EM, et al. Evasion of neutralizing antibody responses by the SARS-CoV-2 BA.2.75 variant . Cell Host Microbe 2022; 30:1518.e4–1526.e4.
Wang Q, Iketani S, Li Z, Guo Y, Yeh AY, Liu M, et al. Antigenic characterization of the SARS-CoV-2 Omicron subvariant BA.2.75 . Cell Host Microbe 2022; 30:1512.e4–1517.e4.
Shen X, Chalkias S, Feng J, Chen X, Zhou H, Marshall JC, et al. Neutralization of SARS-CoV-2 Omicron BA.2.75 after mRNA-1273 vaccination . N Engl J Med 2022; 387:1234–1236.