Adequate tetanus but poor diphtheria and pertussis response to a Tdap booster in adolescents with juvenile systemic lupus erythematosus

Abstract

Background

Reports on vaccine responses in immunocompromised patients, such as juvenile systemic lupus erythematosus (jSLE), have shown highly variable results.

Objective

To compare the immune response and safety after a Tdap booster in 26 jSLE patients and 26 matched healthy adolescents.

Methodology: Adverse events and disease activity were evaluated. Lymphocyte immunophenotyping was performed by flow cytometry. Tetanus, diphtheria and pertussis toxin antibodies were assessed by ELISA; whole blood was stimulated with whole cell pertussis and supernatants were assessed for cytokines by xMAP.

Results

Both groups showed a similar frequency of adverse events. There was no evidence of disease reactivation after Tdap booster in the jSLE cohort. Both groups showed a significant increase in antibody titers for all three antigens on D14 and D28 (p < 0.001). jSLE patients had a significantly lower increase in diphtheria titers than the control group (p = 0.007). jSLE patients had a distinct titer increase of tetanus and pertussis antibodies when compared to controls (p = 0.004 and p < 0.001, respectively). There was a lower frequency of pertussis seroconversion in the jSLE group on D14 (p = 0.009), D28 (p = 0.023), D12m (p = 0.015) and D24m (p = 0.004). Cellular immune response to Bordetella pertussis showed significantly lower levels of IFNγ (p < 0.001) and higher levels of IL10, IL12, IL21 and TNFα in jSLE patients than controls.

Conclusions

jSLE patients had good response to Tdap booster dose for the tetanus antigen, but not for diphtheria and pertussis. This vaccine was safe in relation to adverse events and absence of disease reactivation.

Keywords

Juvenile systemic lupus erythematosus vaccine vaccine against diphtheria tetanus and acellular pertussis Tdap immunogenicity adolescents

Get full access to this article

View all access options for this article.

References

Silva

Aikawa

Bonfa

Vaccinations in juvenile chronic inflammatory diseases: an update. Nat Rev Rheumatol 2013; 9: 532–543.

Groot

Heijstek

Wulffraat

NM.

Vaccinations in paediatric rheumatology: an update on current developments. Curr Rheumatol Rep 2015; 17: 46–65.

Klein-Gitelman

Lane

JC.

Textbook of pediatric rheumatology. 7th ed. Philadelphia: Elsevier Saunders, 2016, p.285.

American Academy of Pediatrics. Tetanus. In: Kimberlin DW, Brady MT, Jackson MA and Long SS (eds) Red book: 2018 report of the committee on infectious diseases. Itasca, IL: American Academy of Pediatrics, 2018, pp.793–798.

Hochberg

MC.

Updating the American college of rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997; 40: 1725.

Petri

Orbai

Alarcon

, et al. Derivation and validation of the systemic lupus international collaborating clinics classification criteria for systemic lupus erythematosus. Arthr Rheum 2012; 64: 2677–2686.

Gladman

Ibañez

Urowitz

MB.

Systemic lupus erythematosus disease activity index 2000. J Rheumatol 2002; 29: 288–289.

Kristiansen

Aggerbeck

Heron

Improved ELISA for determination of anti-diphtheria and/or anti-tetanus antitoxin antibodies in sera. Apmis 1997; 105: 843–853.

Borrow

Balmer

Roper

MH.

The immunological basis for immunization series. Module 3: Tetanus. Geneva: World Health Organization, 2006, pp.1–52.

10.

Scheifele

Ochnio

JJ.

The immunological basis for immunization series. Module 2: Diphtheria. Geneva: World Health Organization, 2009, pp.1–28.

11.

Guiso

Berbers

Fry

Riffelmann

Wirsing von König

; EU Pertstrain group. What to do and what not to do in serological diagnosis of pertussis: recommendations from EU reference laboratories. Eur J Clin Microbiol Infect Dis 2011; 30: 307–312.

12.

Gröndahl-Yli-Hannuksela

Kauko

Van Der Meeren

Mertsola

Pertussis specific cell-mediated immune responses ten years after acellular pertussis booster vaccination in young adults. Vaccine 2016; 34: 341–349.

13.

Moir

Fauci

AS.

B cells in HIV infection and disease. Nat Rev Immunol 2009; 9: 235–245.

14.

Thierry-Carstensen

Jordan

Uhlving

, et al. A randomised, double-blind, non-inferiority clinical trial on the safety and immunogenicity of a tetanus, diphtheria and monocomponent acellular pertussis (TdaP) vaccine in comparison to a tetanus and diphtheria (Td) vaccine when given as booster vaccinations to healthy adults. Vaccine 2012; 30: 5464–5471.

15.

Halperin

McNeil

Langley

, et al. Tolerability and antibody response in adolescents and adults revaccinated with tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis vaccine adsorbed (tdap) 4-5 years after a previous dose. Vaccine 2011; 29: 8459–8465.

16.

Pichichero

Rennels

Edwards

, et al. Combined tetanus, diphtheria, and 5-component pertussis vaccine for use in adolescents and adults. Jama 2005; 293: 3003–3011.

17.

Sandora

Pfoh

Lee

GM.

Adverse events after administration of tetanus- diphtheria-acellular pertussis vaccine to healthcare workers. Infect Control Hosp Epidemiol 2009; 30: 389–391.

18.

Blatter

Friedland

Weston

Howe

Immunogenicity and safety of a tetanus toxoid, reduced diphtheria toxoid and three-component acellular pertussis vaccine in adults 19-64 years of age. Vaccine 2009; 27: 765–772.

19.

Aikawa

Campos

LMA

Silva

, et al. Glucocorticoid: major factor for reduced immunogenicity of 2009 influenza A (H1N1) vaccine in patients with juvenile autoimmune rheumatic disease. J Rheumatol 2012; 39: 167–173.

20.

Barbosa

CMPL

Terreri

MTRA

Rosario

Moraes-Pinto

Silva

CAA

Hilario

MOE.

Immune response and tolerability of varicela vaccine in children and adolescents with systemic lupus erythematosus previously expose to varicela-zoster virus. Clin Exp Rheumatol 2012; 30: 791–798.

21.

Miyamoto

Ono

Barbosa

CPL

, et al. Vaccine antibodies and T- and B-cell interaction in juvenile systemic lupus erythematosus. Lupus 2011; 20: 736–744.

22.

Spina

Gouvea

Succi

RCM

, et al. Immune response to a Tdap booster in vertically HIV-infected adolescents. Vaccine 2018; 36: 5609–5616.

23.

Schmitt

Bentebibel

Ueno

Phenotype and functions of memory TFH cells in human blood. Trends Immunol 2014; 35: 436–442.

24.

Le Coz

Joublin

Pasquali

J-L

Korganow

A-S

Dumortier

Monneaux

Circulating TFH subset distribution is strongly affected in lupus patients with an active disease. PLoS ONE 2013; 8: e75319.

25.

Mesquita

Cruvinel

Resende

, et al. Follicular helper T cell in immunity and autoimmunity. Braz J Med Biol Res 2016; 49: e5209.

26.

Tangye

Brink

Deenick

EK.

The good, the bad and the ugly - TFH cells in human health and disease. Nat Rev Immunol 2013; 13: 412–426.

27.

BRASIL. Ministério da Saúde. Situação epidemiológica dados. Difteria, https://saude.gov.br/saude-de-a-z/difteria (2020, accessed 29 August 2020).

28.

Heijstek

Gageldonk

PGM

Berbers

GAM

Wulffraat

NM.

Differences in persistence of measles, mumps, rubella, diphtheria and tetanus antibodies between children with rheumatic disease and healthy controls: a retrospective cross-sectional study. Ann Rheum Dis 2012; 71: 948–954.

29.

Kashef

Ghazizadeh

Derakhshan

Farjadian

Alyasin

Antigen-specific antibody response inJuvenile-Onset SLE patients following routine immunization with tetanus toxoid. Iran J Immunol 2008; 5: 181–184.

30.

Higgs

Higgins

Ross

Mills

KH.

Immunity to the respiratory pathogen. Bordetella pertussis. Mucosal Immunol 2012; 5: 485–500.

31.

Ross

Sutton

Higgins

, et al. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS Pathog 2013; 9: e1003264.

32.

Cavalcanti

Santos

Mesquita

Duarte

Lucena-Silva

Cytokine profile in childhood-onset systemic lupus erythematosus: a cross-sectional and longitudinal study. Braz J Med Biol Res 2017; 50: e5738. 3

33.

Wang

Zhao

, et al. Increased interleukin 21 and follicular helper T-like cells and reduced interleukin 10+ B cells in patients with new-onset systemic lupus erythematosus. J Rheumatol 2014; 41: 1781–1792.

34.

Krasselt

Baerwald

Seifert

Insufficient vaccination rates in patients with systemic lupus erythematosus in a German outpatient clinic. Z Rheumatol 2018; 77: 727.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.11 MB