Immune response to the recombinant herpes zoster vaccine in people living with HIV over 50 years of age compared to non-HIV age-/gender-matched controls (SHINGR'HIV): a multicenter, international, non-randomized clinical trial study protocol.

AS01 Aging HIV infection Herpes zoster Immunogenicity Prevention Recombinant zoster vaccine Shingrix® Varicella-zoster virus

Journal

BMC infectious diseases
ISSN: 1471-2334
Titre abrégé: BMC Infect Dis
Pays: England
ID NLM: 100968551

Informations de publication

Date de publication:
19 Mar 2024
Historique:
received: 14 02 2024
accepted: 05 03 2024
medline: 20 3 2024
pubmed: 20 3 2024
entrez: 20 3 2024
Statut: epublish

Résumé

The burden of herpes zoster (shingles) virus and associated complications, such as post-herpetic neuralgia, is higher in older adults and has a significant impact on quality of life. The incidence of herpes zoster and post-herpetic neuralgia is increased in people living with HIV (PLWH) compared to an age-matched general population, including PLWH on long-term antiretroviral therapy (ART) with no detectable viremia and normal CD4 counts. PLWH - even on effective ART may- exhibit sustained immune dysfunction, as well as defects in cells involved in the response to vaccines. In the context of herpes zoster, it is therefore important to assess the immune response to varicella zoster virus vaccination in older PLWH and to determine whether it significantly differs to that of HIV-uninfected healthy adults or younger PLWH. We aim at bridging these knowledge gaps by conducting a multicentric, international, non-randomised clinical study (SHINGR'HIV) with prospective data collection after vaccination with an adjuvant recombinant zoster vaccine (RZV) in two distinct populations: in PLWH on long-term ART (> 10 years) over 50 years of and age/gender matched controls. We will recruit participants from two large established HIV cohorts in Switzerland and in France in addition to age-/gender-matched HIV-uninfected controls. Participants will receive two doses of RZV two months apart. In depth-evaluation of the humoral, cellular, and innate immune responses and safety profile of the RZV will be performed to address the combined effect of aging and potential immune deficiencies due to chronic HIV infection. The primary study outcome will compare the geometric mean titer (GMT) of gE-specific total IgG measured 1 month after the second dose of RZV between different age groups of PLWH and between PLWH and age-/gender-matched HIV-uninfected controls. The SHINGR'HIV trial will provide robust data on the immunogenicity and safety profile of RZV in older PLWH to support vaccination guidelines in this population. ClinicalTrials.gov NCT05575830. Registered on 12 October 2022. Eu Clinical Trial Register (EUCT number 2023-504482-23-00).

Sections du résumé

BACKGROUND BACKGROUND
The burden of herpes zoster (shingles) virus and associated complications, such as post-herpetic neuralgia, is higher in older adults and has a significant impact on quality of life. The incidence of herpes zoster and post-herpetic neuralgia is increased in people living with HIV (PLWH) compared to an age-matched general population, including PLWH on long-term antiretroviral therapy (ART) with no detectable viremia and normal CD4 counts. PLWH - even on effective ART may- exhibit sustained immune dysfunction, as well as defects in cells involved in the response to vaccines. In the context of herpes zoster, it is therefore important to assess the immune response to varicella zoster virus vaccination in older PLWH and to determine whether it significantly differs to that of HIV-uninfected healthy adults or younger PLWH. We aim at bridging these knowledge gaps by conducting a multicentric, international, non-randomised clinical study (SHINGR'HIV) with prospective data collection after vaccination with an adjuvant recombinant zoster vaccine (RZV) in two distinct populations: in PLWH on long-term ART (> 10 years) over 50 years of and age/gender matched controls.
METHODS METHODS
We will recruit participants from two large established HIV cohorts in Switzerland and in France in addition to age-/gender-matched HIV-uninfected controls. Participants will receive two doses of RZV two months apart. In depth-evaluation of the humoral, cellular, and innate immune responses and safety profile of the RZV will be performed to address the combined effect of aging and potential immune deficiencies due to chronic HIV infection. The primary study outcome will compare the geometric mean titer (GMT) of gE-specific total IgG measured 1 month after the second dose of RZV between different age groups of PLWH and between PLWH and age-/gender-matched HIV-uninfected controls.
DISCUSSION CONCLUSIONS
The SHINGR'HIV trial will provide robust data on the immunogenicity and safety profile of RZV in older PLWH to support vaccination guidelines in this population.
TRIAL REGISTRATION BACKGROUND
ClinicalTrials.gov NCT05575830. Registered on 12 October 2022. Eu Clinical Trial Register (EUCT number 2023-504482-23-00).

Identifiants

pubmed: 38504173
doi: 10.1186/s12879-024-09192-5
pii: 10.1186/s12879-024-09192-5
doi:

Banques de données

ClinicalTrials.gov
['NCT05575830']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

329

Informations de copyright

© 2024. The Author(s).

Références

Matthews I, Duong M, Parsons VL, Nozad B, Qizilbash N, Patel Y, et al. Burden of disease from shingles and post-herpetic neuralgia in the over 80 year olds in the UK. PLoS ONE. 2020;15(2):e0229224.
pubmed: 32097441 pmcid: 7041808 doi: 10.1371/journal.pone.0229224
Neuzil KM, Griffin MR. Preventing shingles and its complications in older persons. N Engl J Med. 2016;375(11):1079–80.
pubmed: 27626522 doi: 10.1056/NEJMe1610652
Blank LJ, Polydefkis MJ, Moore RD, Gebo KA. Herpes zoster among persons living with HIV in the current ART era. J Acquir Immune Defic Syndr 1999. 2012;61(2):203–7.
doi: 10.1097/QAI.0b013e318266cd3c
McKay SL, Guo A, Pergam SA, Dooling K. Herpes zoster risk in immunocompromised adults in the United States: a systematic review. Clin Infect Dis off Publ Infect Dis Soc Am. 2020;71(7):e125–34.
doi: 10.1093/cid/ciz1090
Marra F, Parhar K, Huang B, Vadlamudi N. Risk factors for herpes zoster infection: a Meta-analysis. Open Forum Infect Dis. 2020;7(1):ofaa005.
pubmed: 32010734 pmcid: 6984676 doi: 10.1093/ofid/ofaa005
Gilbert L, Wang X, Deiss R, Okulicz J, Maves R, Schofield C, et al. Herpes Zoster Rates continue to decline in people living with Human Immunodeficiency Virus but remain higher Than Rates reported in the General US Population. Clin Infect Dis off Publ Infect Dis Soc Am. 2019;69(1):155–8.
doi: 10.1093/cid/ciy1041
Ku HC, Tsai YT, Konara-Mudiyanselage SP, Wu YL, Yu T, Ko NY. Incidence of herpes zoster in HIV-Infected patients undergoing antiretroviral therapy: a systematic review and Meta-analysis. J Clin Med. 2021;10(11):2300.
pubmed: 34070645 pmcid: 8198877 doi: 10.3390/jcm10112300
Hawkins KL, Gordon KS, Levin MJ, Weinberg A, Battaglia C, Rodriguez-Barradas MC, HERPES ZOSTER AND HERPES ZOSTER VACCINE RATES AMONG ADULTS LIVING WITH AND WITHOUT HIV IN THE VETERANS AGING COHORT STUDY. J Acquir Immune Defic Syndr. 1999. 2018;79(4):527–33.
Appay V, Kelleher AD. Immune activation and immune aging in HIV infection. Curr Opin HIV AIDS. 2016;11(2):242–9.
pubmed: 26845675 doi: 10.1097/COH.0000000000000240
Lagathu C, Cossarizza A, Béréziat V, Nasi M, Capeau J, Pinti M. Basic science and pathogenesis of ageing with HIV: potential mechanisms and biomarkers. AIDS Lond Engl. 2017;31(Suppl 2):S105–19.
doi: 10.1097/QAD.0000000000001441
Babu H, Ambikan AT, Gabriel EE, Svensson Akusjärvi S, Palaniappan AN, Sundaraj V, et al. Systemic inflammation and the increased risk of Inflamm-Aging and Age-Associated diseases in people living with HIV on Long Term suppressive antiretroviral therapy. Front Immunol. 2019;10:1965.
pubmed: 31507593 pmcid: 6718454 doi: 10.3389/fimmu.2019.01965
Wheatley AK, Kristensen AB, Lay WN, Kent SJ. HIV-dependent depletion of influenza-specific memory B cells impacts B cell responsiveness to seasonal influenza immunisation. Sci Rep. 2016;6(1):26478.
pubmed: 27220898 pmcid: 4879526 doi: 10.1038/srep26478
Cole ME, Saeed Z, Shaw AT, Guo Y, Höschler K, Winston A, et al. Responses to Quadrivalent Influenza Vaccine reveal distinct circulating CD4 + CXCR5 + T cell subsets in men living with HIV. Sci Rep. 2019;9(1):15650.
pubmed: 31666568 pmcid: 6821795 doi: 10.1038/s41598-019-51961-9
Moysi E, Pallikkuth S, De Armas LR, Gonzalez LE, Ambrozak D, George V, et al. Altered immune cell follicular dynamics in HIV infection following influenza vaccination. J Clin Invest. 2018;128(7):3171–85.
pubmed: 29911996 pmcid: 6025971 doi: 10.1172/JCI99884
George VK, Pallikkuth S, Parmigiani A, Alcaide M, Fischl M, Arheart KL, et al. HIV infection worsens Age-Associated defects in antibody responses to Influenza Vaccine. J Infect Dis. 2015;211(12):1959–68.
pubmed: 25556252 pmcid: 4836723 doi: 10.1093/infdis/jiu840
Parmigiani A, Alcaide ML, Freguja R, Pallikkuth S, Frasca D, Fischl MA, et al. Impaired antibody response to Influenza Vaccine in HIV-Infected and uninfected aging women is Associated with Immune activation and inflammation. PLoS ONE. 2013;8(11):e79816.
pubmed: 24236161 pmcid: 3827419 doi: 10.1371/journal.pone.0079816
Royston L, Isnard S, Lin J, Routy JP. Cytomegalovirus as an uninvited guest in the response to vaccines in people living with HIV. Viruses. 2021;13(7):1266.
pubmed: 34209711 pmcid: 8309982 doi: 10.3390/v13071266
George VK, Pallikkuth S, Pahwa R, de Armas LR, Rinaldi S, Pan L, et al. Circulating inflammatory monocytes contribute to impaired influenza vaccine responses in HIV-infected participants. AIDS Lond Engl. 2018;32(10):1219–28.
doi: 10.1097/QAD.0000000000001821
Del Giudice G, Rappuoli R, Didierlaurent AM. Correlates of adjuvanticity: a review on adjuvants in licensed vaccines. Semin Immunol. 2018;39:14–21.
pubmed: 29801750 doi: 10.1016/j.smim.2018.05.001
Verbeke R, Hogan MJ, Loré K, Pardi N. Innate immune mechanisms of mRNA vaccines. Immunity. 2022;55(11):1993–2005.
pubmed: 36351374 pmcid: 9641982 doi: 10.1016/j.immuni.2022.10.014
O’Hagan DT, Lodaya RN, Lofano G. The continued advance of vaccine adjuvants– ‘we can work it out’. Semin Immunol. 2020;50:101426.
pubmed: 33257234 doi: 10.1016/j.smim.2020.101426
Manuel O, Pascual M, Hoschler K, Giulieri S, Alves D, Ellefsen K, et al. Humoral response to the Influenza A H1N1/09 monovalent AS03-Adjuvanted vaccine in immunocompromised patients. Clin Infect Dis. 2011;52(2):248–56.
pubmed: 21288852 doi: 10.1093/cid/ciq104
Calmy A, Bel M, Nguyen A, Combescure C, Delhumeau C, Meier S, et al. Strong serological responses and HIV RNA increase following AS03-adjuvanted pandemic immunization in HIV-infected patients. HIV Med. 2012;13(4):207–18.
pubmed: 22093373 doi: 10.1111/j.1468-1293.2011.00961.x
Durando P, Fenoglio D, Boschini A, Ansaldi F, Icardi G, Sticchi L, et al. Safety and immunogenicity of two influenza virus subunit vaccines, with or without MF59 adjuvant, administered to human immunodeficiency virus type 1-seropositive and -seronegative adults. Clin Vaccine Immunol CVI. 2008;15(2):253–9.
pubmed: 18003811 doi: 10.1128/CVI.00316-07
Benson CA, Andersen JW, Macatangay BJC, Mailliard RB, Rinaldo CR, Read S, et al. Safety and Immunogenicity of Zoster Vaccine live in human immunodeficiency virus-infected adults with CD4 + cell counts > 200 Cells/mL virologically suppressed on antiretroviral therapy. Clin Infect Dis off Publ Infect Dis Soc Am. 2018;67(11):1712–9.
doi: 10.1093/cid/ciy242
Weinberg A, Levin MJ, Macgregor RR. Safety and immunogenicity of a live attenuated varicella vaccine in VZV-seropositive HIV-infected adults. Hum Vaccin. 2010;6(4):318–21.
pubmed: 20372089 doi: 10.4161/hv.6.4.10654
Parikh R, Singer D, Chmielewski-Yee E, Dessart C. Effectiveness and safety of recombinant zoster vaccine: a review of real-world evidence. Hum Vaccines Immunother. 2023;19(3):2263979.
doi: 10.1080/21645515.2023.2263979
Cunningham AL, Lal H, Kovac M, Chlibek R, Hwang SJ, Díez-Domingo J, et al. Efficacy of the herpes zoster subunit vaccine in adults 70 years of age or older. N Engl J Med. 2016;375(11):1019–32.
pubmed: 27626517 doi: 10.1056/NEJMoa1603800
Lal H, Cunningham AL, Godeaux O, Chlibek R, Diez-Domingo J, Hwang SJ, et al. Efficacy of an adjuvanted herpes zoster subunit vaccine in older adults. N Engl J Med. 2015;372(22):2087–96.
pubmed: 25916341 doi: 10.1056/NEJMoa1501184
Boutry C, Hastie A, Diez-Domingo J, Tinoco JC, Yu CJ, Andrews C, et al. The Adjuvanted recombinant zoster vaccine confers long-term protection against herpes zoster: interim results of an extension study of the pivotal phase 3 clinical trials ZOE-50 and ZOE-70. Clin Infect Dis off Publ Infect Dis Soc Am. 2022;74(8):1459–67.
doi: 10.1093/cid/ciab629
Giannelos N, Ng C, Curran D. Cost-effectiveness of the recombinant zoster vaccine (RZV) against herpes zoster: an updated critical review. Hum Vaccines Immunother. 2023;19(1):2168952.
doi: 10.1080/21645515.2023.2168952
Singer D, Salem A, Stempniewicz N, Ma S, Poston S, Curran D. The potential impact of increased recombinant zoster vaccine coverage on the burden of herpes zoster among adults aged 50–59 years. Vaccine. 2023;41(37):5360–7.
pubmed: 37541822 doi: 10.1016/j.vaccine.2023.07.025
Strezova A, Diez-Domingo J, Al Shawafi K, Tinoco JC, Shi M, Pirrotta P, et al. Long-term protection against herpes zoster by the Adjuvanted recombinant zoster vaccine: Interim Efficacy, Immunogenicity, and Safety results up to 10 years after initial vaccination. Open Forum Infect Dis. 2022;9(10):ofac485.
pubmed: 36299530 pmcid: 9588150 doi: 10.1093/ofid/ofac485
Kim JH, Johnson R, Kovac M, Cunningham AL, Amakrane M, Sullivan KM, et al. Adjuvanted recombinant zoster vaccine decreases herpes zoster-associated pain and the use of pain medication across 3 randomized, placebo-controlled trials. Pain. 2023;164(4):741–8.
pubmed: 36066965 doi: 10.1097/j.pain.0000000000002760
Lecrenier N, Beukelaers P, Colindres R, Curran D, De Kesel C, De Saegher JP, et al. Development of adjuvanted recombinant zoster vaccine and its implications for shingles prevention. Expert Rev Vaccines. 2018;17(7):619–34.
pubmed: 30028651 doi: 10.1080/14760584.2018.1495565
Cunningham AL, Heineman TC, Lal H, Godeaux O, Chlibek R, Hwang SJ, et al. Immune responses to a recombinant glycoprotein E herpes zoster vaccine in adults aged 50 years or older. J Infect Dis. 2018;217(11):1750–60.
pubmed: 29529222 pmcid: 5946839 doi: 10.1093/infdis/jiy095
Levin MJ, Kroehl ME, Johnson MJ, Hammes A, Reinhold D, Lang N, et al. Th1 memory differentiates recombinant from live herpes zoster vaccines. J Clin Invest. 2018;128(10):4429–40.
pubmed: 30024861 pmcid: 6159998 doi: 10.1172/JCI121484
Berkowitz EM, Moyle G, Stellbrink HJ, Schürmann D, Kegg S, Stoll M, et al. Safety and immunogenicity of an adjuvanted herpes zoster subunit candidate vaccine in HIV-infected adults: a phase 1/2a randomized, placebo-controlled study. J Infect Dis. 2015;211(8):1279–87.
pubmed: 25371534 doi: 10.1093/infdis/jiu606
Kolber MA, Gabr AH, De La Rosa A, Glock JA, Jayaweera D, Miller N, et al. Genotypic analysis of plasma HIV-1 RNA after influenza vaccination of patients with previously undetectable viral loads. AIDS Lond Engl. 2002;16(4):537–42.
doi: 10.1097/00002030-200203080-00004
Staprans SI, Hamilton BL, Follansbee SE, Elbeik T, Barbosa P, Grant RM, et al. Activation of virus replication after vaccination of HIV-1-infected individuals. J Exp Med. 1995;182(6):1727–37.
pubmed: 7500017 doi: 10.1084/jem.182.6.1727
Yek C, Gianella S, Plana M, Castro P, Scheffler K, García F, et al. Standard vaccines increase HIV-1 transcription during antiretroviral therapy. AIDS Lond Engl. 2016;30(15):2289–98.
doi: 10.1097/QAD.0000000000001201
Weinberg A, Schmid DS, Leung J, Johnson MJ, Miao C, Levin MJ. Predictors of five-year persistence of antibody responses to Zoster vaccines. J Infect Dis. 2023;jiad132.
López-Fauqued M, Campora L, Delannois F, El Idrissi M, Oostvogels L, De Looze FJ, et al. Safety profile of the adjuvanted recombinant zoster vaccine: pooled analysis of two large randomised phase 3 trials. Vaccine. 2019;37(18):2482–93.
pubmed: 30935742 doi: 10.1016/j.vaccine.2019.03.043
Summary of product characteristics, Shingrix powder and suspension for suspension for injection Herpes zoster vaccine (recombinant, adjuvanted) [Internet]. Available from: https://www.ema.europa.eu/en/documents/product-information/shingrix-epar-product-information_en.pdf

Auteurs

Maxime Hentzien (M)

HIV/AIDS Unit, Division of Infectious Diseases, Geneva University Hospitals, Geneva, Switzerland.
University of Reims Champagne-Ardenne, Reims, France.

Fabrice Bonnet (F)

CHU de Bordeaux, Hôpital Saint-André, Service de Médecine Interne et Maladies Infectieuses, Bordeaux, France.
Université de Bordeaux, INSERM, Institut Bergonié, BPH, U1219, CIC-EC 1401, Bordeaux, F-33000, France.

Enos Bernasconi (E)

Department of Infectious Diseases, Ente Ospedaliero Cantonale, Lugano, Switzerland.

Emmanuel Biver (E)

Division of Bone Diseases, Geneva University Hospitals, Geneva, Switzerland.

Dominique L Braun (DL)

Division Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

Aline Munting (A)

Service of Infectious Diseases, Centre Hospitalier Universitaire Vaudoise (CHUV), Lausanne, Switzerland.

Karoline Leuzinger (K)

Clinical Virology, University Hospital Basel, Basel, Switzerland.

Olivier Leleux (O)

Université de Bordeaux, INSERM, Institut Bergonié, BPH, U1219, CIC-EC 1401, Bordeaux, F-33000, France.

Stefano Musardo (S)

HIV/AIDS Unit, Division of Infectious Diseases, Geneva University Hospitals, Geneva, Switzerland.

Virginie Prendki (V)

Division of Infectious Disease, Geneva University Hospital, Geneva, Switzerland.

Patrick Schmid (P)

Division of Infectious Diseases and Hospital Epidemiology, Kantonsspital, St Gallen, Switzerland.

Cornelia Staehelin (C)

Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.

Marcel Stoeckle (M)

Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, Basel, Switzerland.

Carla S Walti (CS)

Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, Basel, Switzerland.

Linda Wittkop (L)

CHU de Bordeaux, Hôpital Saint-André, Service de Médecine Interne et Maladies Infectieuses, Bordeaux, France.
CHU de Bordeaux, Service d'information médicale, INSERM, Institut Bergonié, CIC-EC 1401, Bordeaux, F-33000, France.
Inria équipe SISTM team, Talence, France.

Victor Appay (V)

Université de Bordeaux, CNRS UMR 5164, INSERM ERL 1303, ImmunoConcEpT, Bordeaux, 33000, France.

Arnaud M Didierlaurent (AM)

Department of Pathology and Immunology, Center of Vaccinology, Faculty of Medicine, University of Geneva, Geneva, Switzerland. arnaud.didierlaurent@unige.ch.

Alexandra Calmy (A)

HIV/AIDS Unit, Division of Infectious Diseases, Geneva University Hospitals, Geneva, Switzerland. Alexandra.Calmy@hug.ch.

Classifications MeSH