Skip to main content
Top
Published in: Arthritis Research & Therapy 1/2019

Open Access 01-12-2019 | Vaccination | Research article

Impact of synthetic and biological immunomodulatory therapy on the duration of 17DD yellow fever vaccine-induced immunity in rheumatoid arthritis

Authors: Clarissa de Castro Ferreira, Ana Carolina Campi-Azevedo, Vanessa Peruhype-Magalhāes, Jordana Grazziela Coelho-dos-Reis, Lis Ribeiro do Valle Antonelli, Karen Torres, Larissa Chaves Freire, Ismael Artur da Costa-Rocha, Ana Cristina Vanderley Oliveira, Maria de Lourdes de Sousa Maia, Sheila Maria Barbosa de Lima, Carla Magda Domingues, Andréa Teixeira-Carvalho, Olindo Assis Martins-Filho, Lícia Maria Henrique da Mota, on behalf of the Collaborative Group for Studies of Yellow Fever Vaccine

Published in: Arthritis Research & Therapy | Issue 1/2019

Login to get access

Abstract

Background

The 17DD-yellow fever (YF) vaccine induces a long-lasting protective immunity, resulting from humoral and cellular immunological memory. The treatment of rheumatoid arthritis (RA) patients with disease-modifying anti-rheumatic drugs (DMARD) may affect pre-existing 17DD-vaccine protective immunity and increase the risk of acquiring YF infection. Our goal was to determine whether DMARD would affect the duration of YF-specific protective immunity in RA patients.

Methods

A total of 122 RA patients, previously immunized with the 17DD-YF vaccine (1–5, 5–9, and ≥ 10 years) and currently under DMARD therapy, were enrolled in the present investigation. Immunomodulatory therapy encompasses the use of conventional synthetic DMARD alone (csDMARD) or combines with biological DMARD (cs+bDMARD). A total of 226 healthy subjects were recruited as a control group (CONT). Neutralizing antibody responses were measured by a plaque-reduction neutralization test (PRNT), and cellular immunity was evaluated by an in vitro 17DD-YF-specific peripheral blood lymphoproliferative assay.

Results

The data demonstrated that csDMARD therapy did not affect the duration of protective immunity induced by the 17DD-YF vaccine compared to that of CONT, as both presented a significant time-dependent decline at 10 years after vaccination. Conversely, cs+bDMARD therapy induced a premature depletion in the main determinants of the vaccine protective response, with diminished PRNT seropositivity levels between 5 and 9 years and impaired effector memory in CD8+ T cells as early as 1–5 years after 17DD-YF vaccination.

Conclusions

These findings could support changing the vaccination schedule of this population, with the possibility of a planned booster dose upon the suspension of bDMARD in cases where this is allowed, even before 10 years following 17DD-YF vaccination. The benefit of a planned booster dose should be evaluated in further studies.

Trial registration

RBR-946bv5. Date of registration: March 05, 2018. Retrospectively registered
Literature
2.
go back to reference Spindler A, Bellomio V, Berman A, Lucero E, Baigorria M, Paz S, et al. Prevalence of rheumatoid arthritis in Tucuman. Argentina J Rheumatol. 2002;29:1166–70.PubMed Spindler A, Bellomio V, Berman A, Lucero E, Baigorria M, Paz S, et al. Prevalence of rheumatoid arthritis in Tucuman. Argentina J Rheumatol. 2002;29:1166–70.PubMed
3.
go back to reference Pelaez-Ballestas I, Sanin LH, Moreno-Montoya J, Alvarez-Nemegyei J, Burgos-Vargas R, Garza-Elizondo M, et al. Epidemiology of the rheumatic diseases in Mexico. A study of 5 regions based on the COPCORD methodology. J Rheumatol Suppl. 2011;86:3–8.CrossRef Pelaez-Ballestas I, Sanin LH, Moreno-Montoya J, Alvarez-Nemegyei J, Burgos-Vargas R, Garza-Elizondo M, et al. Epidemiology of the rheumatic diseases in Mexico. A study of 5 regions based on the COPCORD methodology. J Rheumatol Suppl. 2011;86:3–8.CrossRef
4.
go back to reference Marques-Neto JF, Gonçalves ET, Langen LFOB, Cunha MFL, Radominski S, Oliveira SM, et al. Multicentric study of the prevalence of adult rheumatoid arthritis in Brazilian population samples. Rev Bras Reumatol. 1993;33:169–73. Marques-Neto JF, Gonçalves ET, Langen LFOB, Cunha MFL, Radominski S, Oliveira SM, et al. Multicentric study of the prevalence of adult rheumatoid arthritis in Brazilian population samples. Rev Bras Reumatol. 1993;33:169–73.
5.
go back to reference Senna ER, De Barros AL, Silva EO, Costa IF, Pereira LV, Ciconelli RM, et al. Prevalence of rheumatic diseases in Brazil: a study using the COPCORD approach. J Rheumatol. 2004;31:594–7.PubMed Senna ER, De Barros AL, Silva EO, Costa IF, Pereira LV, Ciconelli RM, et al. Prevalence of rheumatic diseases in Brazil: a study using the COPCORD approach. J Rheumatol. 2004;31:594–7.PubMed
6.
go back to reference Meroni PL, Zavaglia D, Girmenia C. Vaccinations in adults with rheumatoid arthritis in an era of new disease-modifying anti-rheumatic drugs. Clin Exp Rheumatol. 2017;36:317-28. Meroni PL, Zavaglia D, Girmenia C. Vaccinations in adults with rheumatoid arthritis in an era of new disease-modifying anti-rheumatic drugs. Clin Exp Rheumatol. 2017;36:317-28.
7.
go back to reference Muniz LF, Silva CR, Costa TF, da Mota LM. Vaccination in patients from Brasilia cohort with early rheumatoid arthritis. Rev Bras Reumatol. 2014;54:349–55.CrossRef Muniz LF, Silva CR, Costa TF, da Mota LM. Vaccination in patients from Brasilia cohort with early rheumatoid arthritis. Rev Bras Reumatol. 2014;54:349–55.CrossRef
8.
go back to reference Friedman MA, Winthrop KL. Vaccines and disease-modifying antirheumatic drugs: practical implications for the rheumatologist. Rheum Dis Clin N Am. 2017;43:1–13.CrossRef Friedman MA, Winthrop KL. Vaccines and disease-modifying antirheumatic drugs: practical implications for the rheumatologist. Rheum Dis Clin N Am. 2017;43:1–13.CrossRef
9.
go back to reference Goldani LZ. Yellow fever outbreak in Brazil, 2017. Braz J Infect Dis. 2017;21:123–4.CrossRef Goldani LZ. Yellow fever outbreak in Brazil, 2017. Braz J Infect Dis. 2017;21:123–4.CrossRef
10.
go back to reference Ortiz-Martinez Y, Patino-Barbosa AM, Rodriguez-Morales AJ. Yellow fever in the Americas: the growing concern about new epidemics. F1000Res. 2017;6:398.CrossRef Ortiz-Martinez Y, Patino-Barbosa AM, Rodriguez-Morales AJ. Yellow fever in the Americas: the growing concern about new epidemics. F1000Res. 2017;6:398.CrossRef
11.
go back to reference Simoes M, Camacho LA, Yamamura AM, Miranda EH, Cajaraville AC, Silva-Freire M. Evaluation of accuracy and reliability of the plaque reduction neutralization test (micro-PRNT) in detection of yellow fever virus antibodies. Biologicals. 2012;40:399–404.CrossRef Simoes M, Camacho LA, Yamamura AM, Miranda EH, Cajaraville AC, Silva-Freire M. Evaluation of accuracy and reliability of the plaque reduction neutralization test (micro-PRNT) in detection of yellow fever virus antibodies. Biologicals. 2012;40:399–404.CrossRef
13.
go back to reference Campi-Azevedo AC, Costa-Pereira C, Antonelli LR, Fonseca CT, Teixeira-Carvalho A, Villela-Rezende G, et al. Booster dose after 10 years is recommended following 17DD-YF primary vaccination. Hum Vaccin Immunother. 2016;12:491–502.CrossRef Campi-Azevedo AC, Costa-Pereira C, Antonelli LR, Fonseca CT, Teixeira-Carvalho A, Villela-Rezende G, et al. Booster dose after 10 years is recommended following 17DD-YF primary vaccination. Hum Vaccin Immunother. 2016;12:491–502.CrossRef
14.
go back to reference Luiza-Silva M, Campi-Azevedo AC, Batista MA, Martins MA, Avelar RS, Silveira- Lemos D, et al. Cytokine signatures of innate and adaptive immunity in 17DD yellow fever vaccinated children and its association with the level of neutralizing antibody. J Infect Dis. 2011;204:873–83.CrossRef Luiza-Silva M, Campi-Azevedo AC, Batista MA, Martins MA, Avelar RS, Silveira- Lemos D, et al. Cytokine signatures of innate and adaptive immunity in 17DD yellow fever vaccinated children and its association with the level of neutralizing antibody. J Infect Dis. 2011;204:873–83.CrossRef
17.
go back to reference Mason RA, Tauraso NM, Spertzel RO, Ginn RK. Yellow fever vaccine: direct challenge of monkeys given graded doses of 17D vaccine. Appl Microbiol. 1973;25:539–44.PubMedPubMedCentral Mason RA, Tauraso NM, Spertzel RO, Ginn RK. Yellow fever vaccine: direct challenge of monkeys given graded doses of 17D vaccine. Appl Microbiol. 1973;25:539–44.PubMedPubMedCentral
18.
go back to reference Julander JG, Trent DW, Monath TP. Immune correlates of protection against yellow fever determined by passive immunization and challenge in the hamster model. Vaccine. 2011;29:6008–16.CrossRef Julander JG, Trent DW, Monath TP. Immune correlates of protection against yellow fever determined by passive immunization and challenge in the hamster model. Vaccine. 2011;29:6008–16.CrossRef
19.
go back to reference Camacho LA, Freire MS, Leal ML, Aguiar SG, Nascimento JP, Iguchi T, et al. Immunogenicity of WHO-17D and brazilian 17DD yellow fever vaccines: a randomized trial. Rev Saude Publica. 2004;38:671–8.CrossRef Camacho LA, Freire MS, Leal ML, Aguiar SG, Nascimento JP, Iguchi T, et al. Immunogenicity of WHO-17D and brazilian 17DD yellow fever vaccines: a randomized trial. Rev Saude Publica. 2004;38:671–8.CrossRef
20.
go back to reference Niedrig M, Lademann M, Emmerich P, Lafrenz M. Assessment of IgG antibodies against yellow fever virus after vaccination with 17D by different assays: neutralization test, haemagglutination inhibition test, immunofluorescence assay and ELISA. Tropical Med Int Health. 1999;4:867–71.CrossRef Niedrig M, Lademann M, Emmerich P, Lafrenz M. Assessment of IgG antibodies against yellow fever virus after vaccination with 17D by different assays: neutralization test, haemagglutination inhibition test, immunofluorescence assay and ELISA. Tropical Med Int Health. 1999;4:867–71.CrossRef
21.
go back to reference Collaborative Group for Studies on Yellow Fever Vaccines. Duration of post-vaccination immunity against yellow fever in adults. Vaccine. 2014;32:4977–84.CrossRef Collaborative Group for Studies on Yellow Fever Vaccines. Duration of post-vaccination immunity against yellow fever in adults. Vaccine. 2014;32:4977–84.CrossRef
22.
go back to reference Miller JD, van der Most RG, Akondy RS, Glidewell JT, Albott S, Masopust D, et al. Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity. 2008;28:710–22.CrossRef Miller JD, van der Most RG, Akondy RS, Glidewell JT, Albott S, Masopust D, et al. Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity. 2008;28:710–22.CrossRef
23.
go back to reference Akondy RS, Monson ND, Miller JD, Edupuganti S, Teuwen D, Wu H, et al. The yellow fever virus vaccine induces a broad and polyfunctional human memory CD8+ T cell response. J Immunol. 2009;183:7919–30.CrossRef Akondy RS, Monson ND, Miller JD, Edupuganti S, Teuwen D, Wu H, et al. The yellow fever virus vaccine induces a broad and polyfunctional human memory CD8+ T cell response. J Immunol. 2009;183:7919–30.CrossRef
24.
go back to reference Blom K, Braun M, Ivarsson MA, Gonzalez VD, Falconer K, Moll M, et al. Temporal dynamics of the primary human T cell response to yellow fever virus 17D as it matures from an effector- to a memory-type response. J Immunol. 2013;190:2150–8.CrossRef Blom K, Braun M, Ivarsson MA, Gonzalez VD, Falconer K, Moll M, et al. Temporal dynamics of the primary human T cell response to yellow fever virus 17D as it matures from an effector- to a memory-type response. J Immunol. 2013;190:2150–8.CrossRef
25.
go back to reference Martins MA, Silva ML, Marciano AP, Peruhype-Magalhaes V, Eloi-Santos SM, Ribeiro JG, et al. Activation/modulation of adaptive immunity emerges simultaneously after 17DD yellow fever first-time vaccination: is this the key to prevent severe adverse reactions following immunization? Clin Exp Immunol. 2007;148:90–100.CrossRef Martins MA, Silva ML, Marciano AP, Peruhype-Magalhaes V, Eloi-Santos SM, Ribeiro JG, et al. Activation/modulation of adaptive immunity emerges simultaneously after 17DD yellow fever first-time vaccination: is this the key to prevent severe adverse reactions following immunization? Clin Exp Immunol. 2007;148:90–100.CrossRef
26.
go back to reference Neves PC, Matos DC, Marcovistz R, Galler R. TLR expression and NK cell activation after human yellow fever vaccination. Vaccine. 2009;27:5543–9.CrossRef Neves PC, Matos DC, Marcovistz R, Galler R. TLR expression and NK cell activation after human yellow fever vaccination. Vaccine. 2009;27:5543–9.CrossRef
27.
go back to reference Silva ML, Espirito-Santo LR, Martins MA, Silveira-Lemos D, Peruhype-Magalhaes V, Caminha RC, et al. Characterization of main cytokine sources from the innate and adaptive immune responses following primary 17DD yellow fever vaccination in adults. Vaccine. 2011;29:583–92.CrossRef Silva ML, Espirito-Santo LR, Martins MA, Silveira-Lemos D, Peruhype-Magalhaes V, Caminha RC, et al. Characterization of main cytokine sources from the innate and adaptive immune responses following primary 17DD yellow fever vaccination in adults. Vaccine. 2011;29:583–92.CrossRef
28.
go back to reference Silva ML, Espirito-Santo LR, Martins MA, Silveira-Lemos D, Peruhype-Magalhaes V, Caminha RC, et al. Clinical and immunological insights on severe, adverse neurotropic and viscerotropic disease following 17D yellow fever vaccination. Clin Vaccine Immunol. 2010;17:118–26.CrossRef Silva ML, Espirito-Santo LR, Martins MA, Silveira-Lemos D, Peruhype-Magalhaes V, Caminha RC, et al. Clinical and immunological insights on severe, adverse neurotropic and viscerotropic disease following 17D yellow fever vaccination. Clin Vaccine Immunol. 2010;17:118–26.CrossRef
30.
go back to reference Rubin LG, Levin MJ, Ljungman P, Davies EG, Avery R, Tomblyn M, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014;58:309–18.CrossRef Rubin LG, Levin MJ, Ljungman P, Davies EG, Avery R, Tomblyn M, et al. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis. 2014;58:309–18.CrossRef
31.
go back to reference Gabay C, Bel M, Combescure C, Ribi C, Meier S, Posfay-Barbe K, et al. Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum. 2011;6:1486–96.CrossRef Gabay C, Bel M, Combescure C, Ribi C, Meier S, Posfay-Barbe K, et al. Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum. 2011;6:1486–96.CrossRef
32.
go back to reference McMahan ZH, Bingham CO 3rd. Effects of biological and non-biological immunomodulatory therapies on the immunogenicity of vaccines in patients with rheumatic diseases. Arthritis Res Ther. 2014;16:506.CrossRef McMahan ZH, Bingham CO 3rd. Effects of biological and non-biological immunomodulatory therapies on the immunogenicity of vaccines in patients with rheumatic diseases. Arthritis Res Ther. 2014;16:506.CrossRef
Metadata
Title
Impact of synthetic and biological immunomodulatory therapy on the duration of 17DD yellow fever vaccine-induced immunity in rheumatoid arthritis
Authors
Clarissa de Castro Ferreira
Ana Carolina Campi-Azevedo
Vanessa Peruhype-Magalhāes
Jordana Grazziela Coelho-dos-Reis
Lis Ribeiro do Valle Antonelli
Karen Torres
Larissa Chaves Freire
Ismael Artur da Costa-Rocha
Ana Cristina Vanderley Oliveira
Maria de Lourdes de Sousa Maia
Sheila Maria Barbosa de Lima
Carla Magda Domingues
Andréa Teixeira-Carvalho
Olindo Assis Martins-Filho
Lícia Maria Henrique da Mota
on behalf of the Collaborative Group for Studies of Yellow Fever Vaccine
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2019
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-019-1854-6

Other articles of this Issue 1/2019

Arthritis Research & Therapy 1/2019 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine