Effect of a synbiotic on the response to seasonal influenza vaccination is strongly influenced by degree of immunosenescence

A. Przemska-Kosicka, C. E. Childs, S. Enani, C. Maidens, Honglin Dong, I. Bin Dayel, K. Tuohy, S. Todd, M. A. Gosney, P. Yaqoob

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Abstract

Background: Ageing increases risk of respiratory infections and impairs the response to influenza vaccination. Pre- and probiotics offer an opportunity to modulate anti-viral defenses and the response to vaccination via alteration of the gut microbiota. This study investigated the effect of a novel probiotic, Bifidobacterium longum bv. infantis CCUG 52,486, combined with a prebiotic, gluco-oligosaccharide (B. longum + Gl-OS), on the response to seasonal influenza vaccination in young and older subjects in a double-blind, randomized controlled trial, taking into account the influence of immunosenescence markers at baseline. Results: Vaccination resulted in a significant increase in total antibody titres, vaccine-specific IgA, IgM and IgG and seroprotection to all three subunits of the vaccine in both young and older subjects, and in general, the increases in young subjects were greater. There was little effect of the synbiotic, although it tended to reduce seroconversion to the Brisbane subunit of the vaccine and the vaccine-specific IgG response in older subjects. Immunological characterization revealed that older subjects randomized to the synbiotic had a significantly higher number of senescent (CD28−CD57+) helper T cells at baseline compared with those randomized to the placebo, and they also had significantly higher plasma levels of anti-CMV IgG and a greater tendency for CMV seropositivity. Moreover, higher numbers of CD28−CD57+ helper T cells were associated with failure to seroconvert to Brisbane, strongly suggesting that the subjects randomized to the synbiotic were already at a significant disadvantage in terms of likely ability to respond to the vaccine compared with those randomized to the placebo. Conclusions: Ageing was associated with marked impairment of the antibody response to influenza vaccination in older subjects and the synbiotic failed to reverse this impairment. However, the older subjects randomized to the synbiotic were at a significant disadvantage due to a greater degree of immunosenscence at baseline compared with those randomized to the placebo. Thus, baseline differences in immunosenescence between the randomized groups are likely to have influenced the outcome of the intervention, highlighting the need for detailed immunological characterization of subjects prior to interventions.
Original languageEnglish
JournalImmunity and Ageing
Volume13
Issue number6
DOIs
Publication statusPublished - 15 Mar 2016

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Synbiotics
Human Influenza
Vaccination
Prebiotics
Subunit Vaccines
Vaccines
Probiotics
Helper-Inducer T-Lymphocytes
Placebos
Bifidobacterium
Oligosaccharides
Respiratory Tract Infections
Immunoglobulin A
Antibody Formation
Immunoglobulin M
Randomized Controlled Trials
Immunoglobulin G
Immunosenescence
Antibodies

Bibliographical note

Open Access This article is distributed under the terms of the Creative Commons Attribution
4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Keywords

  • Ageing
  • Influenza
  • Prebiotic
  • Probiotic
  • Vaccination

Cite this

Effect of a synbiotic on the response to seasonal influenza vaccination is strongly influenced by degree of immunosenescence. / Przemska-Kosicka, A.; Childs, C. E.; Enani, S.; Maidens, C.; Dong, Honglin; Bin Dayel, I.; Tuohy, K.; Todd, S.; Gosney, M. A.; Yaqoob, P.

In: Immunity and Ageing, Vol. 13, No. 6, 15.03.2016.

Research output: Contribution to journalArticle

Przemska-Kosicka, A, Childs, CE, Enani, S, Maidens, C, Dong, H, Bin Dayel, I, Tuohy, K, Todd, S, Gosney, MA & Yaqoob, P 2016, 'Effect of a synbiotic on the response to seasonal influenza vaccination is strongly influenced by degree of immunosenescence' Immunity and Ageing, vol. 13, no. 6. https://doi.org/10.1186/s12979-016-0061-4
Przemska-Kosicka, A. ; Childs, C. E. ; Enani, S. ; Maidens, C. ; Dong, Honglin ; Bin Dayel, I. ; Tuohy, K. ; Todd, S. ; Gosney, M. A. ; Yaqoob, P. / Effect of a synbiotic on the response to seasonal influenza vaccination is strongly influenced by degree of immunosenescence. In: Immunity and Ageing. 2016 ; Vol. 13, No. 6.
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T1 - Effect of a synbiotic on the response to seasonal influenza vaccination is strongly influenced by degree of immunosenescence

AU - Przemska-Kosicka, A.

AU - Childs, C. E.

AU - Enani, S.

AU - Maidens, C.

AU - Dong, Honglin

AU - Bin Dayel, I.

AU - Tuohy, K.

AU - Todd, S.

AU - Gosney, M. A.

AU - Yaqoob, P.

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PY - 2016/3/15

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N2 - Background: Ageing increases risk of respiratory infections and impairs the response to influenza vaccination. Pre- and probiotics offer an opportunity to modulate anti-viral defenses and the response to vaccination via alteration of the gut microbiota. This study investigated the effect of a novel probiotic, Bifidobacterium longum bv. infantis CCUG 52,486, combined with a prebiotic, gluco-oligosaccharide (B. longum + Gl-OS), on the response to seasonal influenza vaccination in young and older subjects in a double-blind, randomized controlled trial, taking into account the influence of immunosenescence markers at baseline. Results: Vaccination resulted in a significant increase in total antibody titres, vaccine-specific IgA, IgM and IgG and seroprotection to all three subunits of the vaccine in both young and older subjects, and in general, the increases in young subjects were greater. There was little effect of the synbiotic, although it tended to reduce seroconversion to the Brisbane subunit of the vaccine and the vaccine-specific IgG response in older subjects. Immunological characterization revealed that older subjects randomized to the synbiotic had a significantly higher number of senescent (CD28−CD57+) helper T cells at baseline compared with those randomized to the placebo, and they also had significantly higher plasma levels of anti-CMV IgG and a greater tendency for CMV seropositivity. Moreover, higher numbers of CD28−CD57+ helper T cells were associated with failure to seroconvert to Brisbane, strongly suggesting that the subjects randomized to the synbiotic were already at a significant disadvantage in terms of likely ability to respond to the vaccine compared with those randomized to the placebo. Conclusions: Ageing was associated with marked impairment of the antibody response to influenza vaccination in older subjects and the synbiotic failed to reverse this impairment. However, the older subjects randomized to the synbiotic were at a significant disadvantage due to a greater degree of immunosenscence at baseline compared with those randomized to the placebo. Thus, baseline differences in immunosenescence between the randomized groups are likely to have influenced the outcome of the intervention, highlighting the need for detailed immunological characterization of subjects prior to interventions.

AB - Background: Ageing increases risk of respiratory infections and impairs the response to influenza vaccination. Pre- and probiotics offer an opportunity to modulate anti-viral defenses and the response to vaccination via alteration of the gut microbiota. This study investigated the effect of a novel probiotic, Bifidobacterium longum bv. infantis CCUG 52,486, combined with a prebiotic, gluco-oligosaccharide (B. longum + Gl-OS), on the response to seasonal influenza vaccination in young and older subjects in a double-blind, randomized controlled trial, taking into account the influence of immunosenescence markers at baseline. Results: Vaccination resulted in a significant increase in total antibody titres, vaccine-specific IgA, IgM and IgG and seroprotection to all three subunits of the vaccine in both young and older subjects, and in general, the increases in young subjects were greater. There was little effect of the synbiotic, although it tended to reduce seroconversion to the Brisbane subunit of the vaccine and the vaccine-specific IgG response in older subjects. Immunological characterization revealed that older subjects randomized to the synbiotic had a significantly higher number of senescent (CD28−CD57+) helper T cells at baseline compared with those randomized to the placebo, and they also had significantly higher plasma levels of anti-CMV IgG and a greater tendency for CMV seropositivity. Moreover, higher numbers of CD28−CD57+ helper T cells were associated with failure to seroconvert to Brisbane, strongly suggesting that the subjects randomized to the synbiotic were already at a significant disadvantage in terms of likely ability to respond to the vaccine compared with those randomized to the placebo. Conclusions: Ageing was associated with marked impairment of the antibody response to influenza vaccination in older subjects and the synbiotic failed to reverse this impairment. However, the older subjects randomized to the synbiotic were at a significant disadvantage due to a greater degree of immunosenscence at baseline compared with those randomized to the placebo. Thus, baseline differences in immunosenescence between the randomized groups are likely to have influenced the outcome of the intervention, highlighting the need for detailed immunological characterization of subjects prior to interventions.

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KW - Influenza

KW - Prebiotic

KW - Probiotic

KW - Vaccination

U2 - 10.1186/s12979-016-0061-4

DO - 10.1186/s12979-016-0061-4

M3 - Article

VL - 13

JO - Immunity and Ageing

JF - Immunity and Ageing

SN - 1742-4933

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