Recombinant Herpes Zoster Vaccine in Patients With Autoimmune Rheumatic Diseases (RZVRheum)

Efficacy, Immunogenicity and Safety of Recombinant Vaccine Against Herpes Zoster (RZV or SHINGRIX®) in Patients With Autoimmune Rheumatic Diseases

Introduction: Patients with autoimmune rheumatic diseases (ARDs), rheumatoid arthritis (RA), juvenile idiopathic arthritis (JIA), psoriatic arthritis (PAs), ankylosing spondylitis (AS), systemic lupus erythematosus (SLE), primary Sjögren's syndrome (pSS) , systemic sclerosis (SSc), idiopathic inflammatory myopathies (IIM) and primary vasculitides, have a high risk of herpes zoster (HZ) infection. This increased susceptibility is caused by a deficient cell-mediated immune response due to the underlying disease and glucocorticoid and immunosuppressive treatments that impair the T-cell response, including conventional and unconventional synthetic disease-modifying anti-rheumatic drugs (DMARDs) and biological agents. In this context, the recent availability of a recombinant vaccine against HZ (RZV or Shingrix®), composed of recombinant VZV glycoprotein E (gE) and the AS01B adjuvant system (HZ/su), is a major progress regarding safety for immunosuppressed patients. Its effectiveness, however, has been clearly demonstrated for non-immunosuppressed patients and in selected populations of immunocompromised individuals. There are no prospective controlled studies evaluating the immunogenicity of RZV and its impact on the activity of the underlying disease, as well as its safety in patients with ARDs at high-risk for HZ. Hypothesis: RZV has a good safety profile, including with respect to underlying rheumatic disease activity, in patients with ARDs at high risk of HZ. Objectives: Primary: To assess the short-term safety profile in relation to underlying disease activity in patients with ARDs at high risk of HZ immunized with RZV compared to unvaccinated patients. Secondary: To evaluate the general safety of the vaccine in patients with ARDs at high risk of HZ immunized with RZV and non-immunosuppressed control subjects (CG); the humoral and cellular immunogenicity of RZV in patients with ARDs at high risk of HZ compared to CG; the influence of disease treatment on vaccine response; the 12-month persistence of humoral immunogenicity and incident cases of HZ. Specific studies will also be carried out to evaluate the effect of drug withdrawal (methotrexate-MTX and mycophenolate mofetil-MMF) after vaccination in increasing the immune response in patients with ARDs with controlled underlying disease.

Methods: Subproject A: This is a phase 4 randomized prospective study of adult patients with ARDs who will receive two intramuscular doses of RZV 6 weeks apart. A control group of non-immunosuppressed individuals (CG) aged ≥ 50 years will also be included, in the proportion of 3 patients:1 control. Patients with ARDs will be randomly allocated into two groups: P1 and P2. CG and P1 will receive the vaccine soon after randomization, on D0 and D42. P2 will be vaccinated 12 weeks after randomization, on D84 and D126. All groups will collect blood samples immediately before vaccination, at baseline, and then receive the 1st dose of vaccine on the same day (D0 for CG and P1, and D84 for P2). The second dose will be applied 6 weeks after the first dose (D42 for P1 and CG, and D126 for P2). Blood samples for disease activity and immunogenicity will be collected 6 weeks after the 2nd dose (D84 for CG and P1 and D168 for P2). The influence of vaccination on disease activity will be evaluated in the first three months of follow-up through disease-specific activity indices. Safety analysis regarding adverse effects (AEs) of the vaccine will be performed using standardized questionnaires on D42 and D84 for CG and P1 and on D126 and D168 for P2. Severe AEs and incident cases of HZ will be evaluated throughout the study period. The persistence of immunogenicity will be evaluated one year after the 2nd dose (D407 for CG and P1, and D491 for P2). Subproject B: Specific studies will also be carried out to evaluate the effect of drug withdrawal (MTX and MMF) after vaccination in increasing the immune response in patients with ARDs with controlled baseline disease. Randomization of patients with ARDs with well-controlled disease selected for the MTX discontinuation protocol will divide them into two groups: MTX-suspension, in which MTX will be suspended for 2 weeks after each vaccine dose, and another group that will maintain stable therapy (MTX-maintenance), with assessments of immunogenicity and disease activity. The same applies to patients undergoing the MMF discontinuation protocol (but the MMF suspension time will be one week after each vaccine dose). Based on a recently published study (Petri et al., 2023), discontinuation time of the MMF after each vaccine dose was reduced from two weeks to one week. In fact, these authors observed in a cohort of 334 patients with systemic lupus erythematosus that discontinuing MMF for one week after vaccination against COVID-19 (mRNA vaccine) improved vaccine efficacy without leading to exacerbations of the underlying disease (Petri et al., 2023). Thus, we considered it appropriate to reduce the MMF discontinuation time to one week after each dose of the recombinant vaccine for herpes zoster in our population of patients with autoimmune rheumatic diseases. Total population: The total population will consist of 2005 participants comprising 1180 patients with ARDs (590 in P1 and 590 in P2), 393 healthy controls. 202 patients on the MTX maintenance/discontinuation RA protocol for two weeks after each vaccine dose, and 230 patients with ARDs on the MMF maintenance/discontinuation protocol for one week after each vaccine dose. Immunogenicity analysis: Humoral immunogenicity will be evaluated through serum concentrations of anti-gE antibodies [enzyme-linked immunosorbent assay (ELISA)] of blood samples collected from participants pre-vaccination, 2 months and one year after the second dose of RZV. The frequencies of gE-specific CD4[2+] T cells will be measured after in vitro stimulation with a pool of peptides covering the gE ectodomain, by intracellular cytokine staining and detection by flow cytometry, in a convenience sample (20% of the total number of participants) from patients with ARDs and healthy controls.

Rheumatoid Arthritis, Spondylitis, Ankylosing, Spondyloarthritis, Systemic Lupus Erythematosus, Sjogren's Syndrome, Systemic Sclerosis, Idiopathic Inflammatory Myopathies, Vasculitis, Systemic, Juvenile Idiopathic Arthritis, Dermatomyositis, Juvenile, Behçet Disease

Recombinant herpes zoster vaccine, Herpes zoster, Autoimmune rheumatic diseases, Disease activity, Safety, Immunogenicity, Disease-modifying anti-rheumatic drugs, Biological disease-modifying anti-rheumatic drugs, Glucocorticoid

Subproject A: Randomized prospective study of adult patients with ARDs who will receive two intramuscular doses of RZV 6 weeks apart or placebo. Subproject B: Specific studies will evaluate the effect of drug withdrawal (MTX and MMF) after vaccination in increasing the immune response in patients with ARDs with controlled baseline disease. Randomization of patients with ARDs with well-controlled disease selected for the MTX discontinuation protocol will divide them into two groups: MTX-suspension, in which MTX will be suspended for 2 weeks after each vaccine dose, and another group that will maintain stable therapy (MTX-maintenance), with assessments of immunogenicity and disease activity. The same applies to patients undergoing the MMF discontinuation protocol (but the MMF suspension time will be one week after each vaccine dose).

Subproject A: Randomized prospective study of adult patients with ARDs who will receive two intramuscular doses of RZV 6 weeks apart or placebo. Subproject B: Specific studies will to evaluate the effect of drug withdrawal (MTX and MMF) after vaccination in increasing the immune response in patients with ARDs with controlled baseline disease. Randomization of patients with ARDs with well-controlled disease selected for the MTX discontinuation protocol will divide them into two groups: MTX-suspension, in which MTX will be suspended for 2 weeks after each vaccine dose, and another group that will maintain stable therapy (MTX-maintenance). The same applies to patients undergoing the MMF discontinuation protocol (but the MMF suspension time will be one week after each vaccine dose).

Patients with ARDs who received the vaccine at study entry (P1) (n = 590). ARD patients will be randomly assigned in a 1:1 ratio, with the use of an automated Web and telephone system, to one of two subgroups: P1, patients allocated to receive vaccine right after randomization (at D0 and D42), and P2, patients allocated to receive placebo at D0 and D42. Subsequently, blindness will be broken at D84 and P2 patients will receive vaccine doses at the D84 and D126.

Subproject A: Patients with ARDs who received the placebo at study entry (P2) (n = 590). ARD patients will be randomly assigned in a 1:1 ratio, with the use of an automated Web and telephone system, to one of two subgroups: P1, patients allocated to receive vaccine right after randomization (at D0 and D42), and P2, patients allocated to receive placebo at D0 and D42. Subsequently, blindness will be broken at D84 and P2 patients will receive vaccine doses at the D84 and D126.

Subproject A: Control group of non-immunosuppressed individuals (CG) (n = 393). The control group of non-immunosuppressed individuals (CG) (≥50 years old) will be invited to receive the vaccine at study entry (3 patients:1 control).

Subproject B: MTX-withhold (n = 101). Patients using MTX at a stable dose for at least 12 weeks, prednisone maximum dose of 5 mg/day, in association or not with other drugs except rituximab, to be randomized into two arms: one that will withhold MTX for 2 weeks after each vaccine dose (MTX-withhold) and other that will maintain stable therapy (MTX-maintain).

Subproject B: MTX-maintain (n = 101). Patients using MTX at a stable dose for at least 12 weeks, prednisone maximum dose of 5 mg/day, in association or not with other drugs except rituximab, to be randomized into two arms: one that will withhold MTX for 2 weeks after each vaccine dose (MTX-withhold) and other that will maintain stable therapy (MTX-maintain).

Subproject B: MMF-withhold (n = 115). Patients with ARDs using MMF at a stable dose for at least 12 weeks, prednisone maximum dose of 7.5 mg/day, not associated with other immunosuppressive therapy, will be consecutively evaluated at outpatient clinics regarding disease activity. Those considered to be at stable disease (at remission or low disease activity according to specific standardized disease activity indexes) will be randomized (1:1) into two arms: one that will withhold MMF for one week after each vaccine dose (MMF-withhold) and other that will maintain stable therapy (MMF-maintain).

Subproject B: MMF-maintain (n = 115). Patients with ARDs using MMF at a stable dose for at least 12 weeks, prednisone maximum dose of 7.5 mg/day, not associated with other immunosuppressive therapy, will be consecutively evaluated at outpatient clinics regarding disease activity. Those considered to be at stable disease (at remission or low disease activity according to specific standardized disease activity indexes) will be randomized (1:1) into two arms: one that will withhold MMF for one week after each vaccine dose (MMF-withhold) and other that will maintain stable therapy (MMF-maintain).

RZV comprise 50 μg of recombinant VZV glycoprotein E and the liposome-based AS01B adjuvant system (which contains 50 μg of 3-O-desacyl-4'-monophosphoryl lipid A [MPL] and 50 μg of Quillaja saponaria Molina, fraction 21 (QS21, licensed by GSK from Antigenics, a subsidiary of Agenus)). Vaccine will be administered (0.5 ml) into the deltoid muscle at inclusion and 6 weeks (two doses).

Evaluation of discontinuation of the use of methotrexate (MTX) for 2 weeks after each vaccine dose in ARD patients: patients using MTX at a stable dose for at least 12 weeks, prednisone maximum dose of 5 mg/day, in association or not with other drugs except rituximab will be consecutively evaluated at outpatient clinics regarding disease activity. Those considered to be at stable disease (at remission or low disease activity according to specific standardized disease activity indexes) will be randomized (1:1) into two arms: one that will withhold MTX for 2 weeks after each vaccine dose (MTX-withhold) and other that will maintain stable therapy (MTX-maintain).

Evaluation of discontinuation of the use of mycophenolate mofetil (MMF) for one week after each vaccine dose in ARD patients: patients using MMF at a stable dose for at least 12 weeks, prednisone maximum dose of 7.5 mg/day, not associated with other immunosuppressive therapy, will be consecutively evaluated at outpatient clinics regarding disease activity. Those considered to be at stable disease (at remission or low disease activity according to specific standardized disease activity indexes) will be randomized (1:1) into two arms: one that will withhold MMF for 2 weeks after each vaccine dose (MMF-withhold) and other that will maintain stable therapy (MMF-maintain).

Patients with ARDs who received the placebo at study entry (P2). ARD patients will be randomly assigned in a 1:1 ratio, with the use of an automated Web and telephone system, to one of two subgroups: P1, patients allocated to receive vaccine right after randomization (at D0 and D42), and P2, patients allocated to receive placebo at D0 and D42. Subsequently, blindness will be broken at D84 and P2 patients will receive vaccine doses at the D84 and D126.

MTX dose will be held stable after the two vaccine doses for comparison of vaccine immunogenicity and disease activity with the MTX-withhold group.

MMF dose will be held stable after the two vaccine doses for comparison of vaccine immunogenicity and disease activity with the MMF-withhold group.

Subproject A: Disease safety (flare) in ARD patients immunized with RZV in comparison to non-vaccinated ARD patients (placebo group)

Flare will be defined as a new flare or worsening of previous disease activity according to established scores for each ARD or the change of therapy. Disease activity will be evaluated in ARD patients according to specific standardized disease activity indexes: RA (DAS28 - Disease Activity Score 28, RA-CDAI - Rheumatoid Arthritis Clinical Disease Activity Index), SLE (SLEDAI2K - Systemic Lupus Erythematosus Disease Activity Index 2000), pSS (ESSDAI- EULAR Sjögren's Syndrome Disease Activity Index), IIM (MMT - Manual Muscle Test), AxS (ASDAS - Ankylosing Spondylitis Disease Activity Score), and vasculitis (Birmingham Vasculitis Activity Score).

Humoral immunogenicity will be assessed through serum anti-gE antibody concentrations analysis (ELISA) of blood samples collected from participants at pre-vaccination, 6 weeks, and one-year after the second dose of RZV. The frequencies of gE-specific CD4[2+] T cells (CD4+ T-cells expressing at least 2 activation markers of the 4 markers assessed: interferon-γ, interleukin 2, tumor necrosis factor-α, and CD40 ligand) will be measured after in vitro stimulation with a pool of peptides covering the gE ectodomain, by intracellular cytokine staining and detection by flow cytometry, in a convenience sample (20% of total research participants).

Humoral immunogenicity will be assessed through serum anti-gE antibody concentrations analysis (ELISA) of blood samples collected from participants at pre-vaccination, 6 weeks, and one-year after the second dose of RZV. The frequencies of gE-specific CD4[2+] T cells (CD4+ T-cells expressing at least 2 activation markers of the 4 markers assessed: interferon-γ, interleukin 2, tumor necrosis factor-α, and CD40 ligand) will be measured after in vitro stimulation with a pool of peptides covering the gE ectodomain, by intracellular cytokine staining and detection by flow cytometry, in a convenience sample (20% of total research participants).

Subproject A: Incidence of vaccine adverse events [safety and tolerability] in ARD patients immunized with RZV in comparison to non-vaccinated ARD patients (placebo group) and non-immunosupressed controls (control group)

A standardized diary card of AEs for recording of solicited local and systemic manifestations will be systematically provided to all patients and healthy controls collected for 7 days post each vaccination. Unsolicited AEs will be recorded within 6 weeks post each vaccination. Serious AEs (SAEs) and adverse events of special interest (AESIs) [potential immune mediated disorder (pIMDs)] will be evaluated throughout the entire study duration.

Subproject A: Humoral immunogenicity of the RZV in ARD patients in comparison to non-immunosupressed control group

Humoral immunogenicity will be assessed through serum anti-gE antibody concentrations analysis (ELISA) of blood samples collected from participants at pre-vaccination, 6 weeks, and one-year after the second dose of RZV. The frequencies of gE-specific CD4[2+] T cells (CD4+ T-cells expressing at least 2 activation markers of the 4 markers assessed: interferon-γ, interleukin 2, tumor necrosis factor-α, and CD40 ligand) will be measured after in vitro stimulation with a pool of peptides covering the gE ectodomain, by intracellular cytokine staining and detection by flow cytometry, in a convenience sample (20% of total research participants).

Subproject A: Incident cases of HZ after RZV vaccination in ARD patients and in the non-immunosupressed control group

A suspected case of HZ will be defined as (1) a new unilateral, dermatomal, rash with pain (broadly defined to include allodynia, pruritus, or other abnormal sensations) without any alternative diagnosis or (2A) or a vesicular rash suggestive of varicella zoster virus infection regardless of the distribution, and no alternative diagnosis; without any alternative diagnosis. For each suspected case, the rash will be photographed and samples will be collected from three lesions to confirm the diagnosis of HZ by real-time polymerase-chain reaction (PCR) assay. If the PCR results were indeterminate or if samples were not available, the final diagnosis will be determined by unanimous agreement among the five members of an ascertainment committee, which includes a dermatologist.

Inclusion Criteria: All subjects will be adults (≥18 years-old). ARD patients will be selected from patients regularly followed up at the Outpatient Rheumatology Clinics of the Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brazil, according to the specific classification criteria: RA (Aletaha et al., 2010), SLE (Petri et al., 2012), pSS (Vitali et al., 2002), SSc (van den Hoogen et al., 2013), IIM (Lundberg et al., 2017), axial spondyloarthritis (axSpA) (Rudwaleit et al., 2009), PsA (Tillett et al., 2012) and granulomatosis with polyangiitis (Leavitt et al., 1990). Patients must be under current use of cyclophosphamide, mycophenolate mofetil, azathioprine, cyclosporin, tacrolimus, leflunomide, glucocorticoids, methotrexate, biologic therapy or JAKi with or without csDMARDs for at least one month prior to study inclusion. Exclusion Criteria: history of any reaction or hypersensitivity to any component of the vaccine; previous HZ vaccination; any occurrence of Guillain-Barré syndrome; hospitalization, acute infectious disease or fever at the time of vaccination; pregnancy or lactation at the time of vaccination; history of HZ within the 12 months preceding the first dose of study vaccine; people living with HIV/AIDS (PLWHA).

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