Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilers

Salmonellosis, a gastrointestinal disease, continues to be one of the major public health concerns worldwide. Poultry meat and eggs are recognized as the major source of Salmonella food poisoning in humans. Our study evaluated the protective efficacy of mannose-conjugated chitosan-nanoparticle (mChi...

Full description

Saved in:
Bibliographic Details
Main Authors: Raksha Suresh, Shekoni Olaitan Comfort, Sara Dolatyabi, Jennifer Schrock, Mithilesh Singh, Gourapura J. Renukaradhya
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-02-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1509990/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832086987664785408
author Raksha Suresh
Shekoni Olaitan Comfort
Sara Dolatyabi
Jennifer Schrock
Mithilesh Singh
Gourapura J. Renukaradhya
author_facet Raksha Suresh
Shekoni Olaitan Comfort
Sara Dolatyabi
Jennifer Schrock
Mithilesh Singh
Gourapura J. Renukaradhya
author_sort Raksha Suresh
collection DOAJ
description Salmonellosis, a gastrointestinal disease, continues to be one of the major public health concerns worldwide. Poultry meat and eggs are recognized as the major source of Salmonella food poisoning in humans. Our study evaluated the protective efficacy of mannose-conjugated chitosan-nanoparticle (mChitosan-NP)-based subunit vaccine, consisting of immunogenic outer membrane proteins and flagella of Salmonella Enteritidis [mChitosan (OMP+FLA)/FLA-NP], coadministered orally with potent mucosal adjuvants to reduce the colonization of S. Enteritidis in the intestines of broiler chickens. We evaluated the adjuvant effects of three different doses of two well-known mucosal adjuvants, c-di-GMP (stimulator of interferon gene agonist) and whole cell lysate (WCL) of Mycobacterium smegmatis, to improve the efficacy of mChitosan (OMP+FLA)/FLA-NP vaccine. Our data reaffirmed the potent adjuvanticity of both of these adjuvants and identified their optimal dose when entrapped in mChitosan-NP to potentiate the immunogenicity and efficacy of orally delivered mChitosan (OMP+FLA)/FLA-NP vaccine. The physical characteristics of mChitosan (OMP+FLA)/FLA-NP, mChitosan-GMP/FLA-NP, and mChitosan-WCL/FLA-NP formulations revealed a high positive charge (Zeta potential +20–25 mV), size 235–260 nm, and polydispersity index 0.35–0.52, which are conducive for oral delivery. The efficacy in chickens that received oral administration with a combination of the vaccine-adjuvant formulations was evaluated by challenging with Salmonella Enteritidis. Our data showed that mChitosan (OMP+FLA)/FLA-NP WCL at 10 µg/dose formulation consistently reduced the S. Enteritidis load by over 0.5 log10 comparable to a commercial live vaccine at post-challenge days 4 and 10. Immunologically, we observed enhanced systemic and mucosal antibody and cellular (B cells and T-helper cells) immune responses as well as upregulation of expression of immune cytokine genes IFN-γ, TGF-β, and IL-17 in the cecal tonsils of adjuvanted mChitosan-NP Salmonella-subunit-vaccinated birds. Overall, particularly the mucosal adjuvant WCL consistently enhanced the efficacy of mChitosan (OMP+FLA)/FLA-NP vaccine by inducing effective immune responses.
format Article
id doaj-art-e38807109e544c0a86331de67473c8bf
institution Kabale University
issn 1664-3224
language English
publishDate 2025-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj-art-e38807109e544c0a86331de67473c8bf2025-02-06T09:01:34ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-02-011610.3389/fimmu.2025.15099901509990Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilersRaksha SureshShekoni Olaitan ComfortSara DolatyabiJennifer SchrockMithilesh SinghGourapura J. RenukaradhyaSalmonellosis, a gastrointestinal disease, continues to be one of the major public health concerns worldwide. Poultry meat and eggs are recognized as the major source of Salmonella food poisoning in humans. Our study evaluated the protective efficacy of mannose-conjugated chitosan-nanoparticle (mChitosan-NP)-based subunit vaccine, consisting of immunogenic outer membrane proteins and flagella of Salmonella Enteritidis [mChitosan (OMP+FLA)/FLA-NP], coadministered orally with potent mucosal adjuvants to reduce the colonization of S. Enteritidis in the intestines of broiler chickens. We evaluated the adjuvant effects of three different doses of two well-known mucosal adjuvants, c-di-GMP (stimulator of interferon gene agonist) and whole cell lysate (WCL) of Mycobacterium smegmatis, to improve the efficacy of mChitosan (OMP+FLA)/FLA-NP vaccine. Our data reaffirmed the potent adjuvanticity of both of these adjuvants and identified their optimal dose when entrapped in mChitosan-NP to potentiate the immunogenicity and efficacy of orally delivered mChitosan (OMP+FLA)/FLA-NP vaccine. The physical characteristics of mChitosan (OMP+FLA)/FLA-NP, mChitosan-GMP/FLA-NP, and mChitosan-WCL/FLA-NP formulations revealed a high positive charge (Zeta potential +20–25 mV), size 235–260 nm, and polydispersity index 0.35–0.52, which are conducive for oral delivery. The efficacy in chickens that received oral administration with a combination of the vaccine-adjuvant formulations was evaluated by challenging with Salmonella Enteritidis. Our data showed that mChitosan (OMP+FLA)/FLA-NP WCL at 10 µg/dose formulation consistently reduced the S. Enteritidis load by over 0.5 log10 comparable to a commercial live vaccine at post-challenge days 4 and 10. Immunologically, we observed enhanced systemic and mucosal antibody and cellular (B cells and T-helper cells) immune responses as well as upregulation of expression of immune cytokine genes IFN-γ, TGF-β, and IL-17 in the cecal tonsils of adjuvanted mChitosan-NP Salmonella-subunit-vaccinated birds. Overall, particularly the mucosal adjuvant WCL consistently enhanced the efficacy of mChitosan (OMP+FLA)/FLA-NP vaccine by inducing effective immune responses.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1509990/fullSalmonella Enteritidisbroiler chickensadjuvantsoral vaccinemucosal immunity
spellingShingle Raksha Suresh
Shekoni Olaitan Comfort
Sara Dolatyabi
Jennifer Schrock
Mithilesh Singh
Gourapura J. Renukaradhya
Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilers
Frontiers in Immunology
Salmonella Enteritidis
broiler chickens
adjuvants
oral vaccine
mucosal immunity
title Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilers
title_full Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilers
title_fullStr Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilers
title_full_unstemmed Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilers
title_short Evaluation of mucosal adjuvants to chitosan-nanoparticle-based oral subunit vaccine for controlling salmonellosis in broilers
title_sort evaluation of mucosal adjuvants to chitosan nanoparticle based oral subunit vaccine for controlling salmonellosis in broilers
topic Salmonella Enteritidis
broiler chickens
adjuvants
oral vaccine
mucosal immunity
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1509990/full
work_keys_str_mv AT rakshasuresh evaluationofmucosaladjuvantstochitosannanoparticlebasedoralsubunitvaccineforcontrollingsalmonellosisinbroilers
AT shekoniolaitancomfort evaluationofmucosaladjuvantstochitosannanoparticlebasedoralsubunitvaccineforcontrollingsalmonellosisinbroilers
AT saradolatyabi evaluationofmucosaladjuvantstochitosannanoparticlebasedoralsubunitvaccineforcontrollingsalmonellosisinbroilers
AT jenniferschrock evaluationofmucosaladjuvantstochitosannanoparticlebasedoralsubunitvaccineforcontrollingsalmonellosisinbroilers
AT mithileshsingh evaluationofmucosaladjuvantstochitosannanoparticlebasedoralsubunitvaccineforcontrollingsalmonellosisinbroilers
AT gourapurajrenukaradhya evaluationofmucosaladjuvantstochitosannanoparticlebasedoralsubunitvaccineforcontrollingsalmonellosisinbroilers