The Impact of the Gut Microbiota on Humoral Immunity to Pathogens and Vaccination in Early Infancy

Nguyen, Quoc‐Hung; Himes, Jonathon E.; Martinez, David R.; Permar, Sallie R.

doi:10.1371/journal.ppat.1005997

Cited by 55 publications

(54 citation statements)

References 36 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Recently, a number of studies have demonstrated an association between the immune system and gut microbiota [20,[32][33][34][35][36][37]. Early infancy is considered as an ideal window for gut microbial colonization [18,38]. Our previous study has validated the benefits of transplanting sow fecal microbiota to newborn piglets [20].…”

Section: Discussionmentioning

confidence: 76%

Early-Life Intervention Using Fecal Microbiota Combined with Probiotics Promotes Gut Microbiota Maturation, Regulates Immune System Development, and Alleviates Weaning Stress in Piglets

Xiang

Pan

et al. 2020

IJMS

View full text Add to dashboard Cite

Previous studies have suggested that immune system development and weaning stress are closely related to the maturation of gut microbiota. The early-life period is a "window of opportunity" for microbial colonization, which potentially has a critical impact on the development of the immune system. Fecal microbiota transplantation (FMT) and probiotics are often used to regulate gut microbial colonization. This study aims to test whether early intervention with FMT using fecal microbiota from gestation sows combined with Clostridium butyricum and Saccharomyces boulardii (FMT-CS) administration could promote the maturation of gut microbiota and development of immune system in piglets. Piglets were assigned to control (n = 84) and FMT-CS treatment (n = 106), which were treated with placebo and bacterial suspension during the first three days after birth, respectively. By 16S rRNA gene sequencing, we found that FMT-CS increased the α-diversity and reduced the unweighted UniFrac distances of the OTU community. Besides, FMT-CS increased the relative abundance of beneficial bacteria, while decreasing that of opportunistic pathogens. FMT-CS also enhanced the relative abundance of genes related to cofactors and vitamin, energy, and amino acid metabolisms during the early-life period. ELISA analysis revealed that FMT-CS gave rise to the plasma concentrations of IL-23, IL-17, and IL-22, as well as the plasma levels of anti-M.hyo and anti-PCV2 antibodies. Furthermore, the FMT-CS-treated piglets showed decreases in inflammation levels and oxidative stress injury, and improvement of intestinal barrier function after weaning as well. Taken together, our results suggest that early-life intervention with FMT-CS could promote the development of innate and adaptive immune system and vaccine efficacy, and subsequently alleviate weaning stress through promoting the maturation of gut microbiota in piglets.

show abstract

Section: Discussionmentioning

confidence: 76%

Early-Life Intervention Using Fecal Microbiota Combined with Probiotics Promotes Gut Microbiota Maturation, Regulates Immune System Development, and Alleviates Weaning Stress in Piglets

Xiang

Pan

et al. 2020

IJMS

View full text Add to dashboard Cite

show abstract

“…Several studies have suggested that early postnatal birth is a critical window for gut microbiota manipulation to optimise the gut health and immunity (Nguyen et al, 2016;Torow and Hornef, 2017). Faecal microbiota transplantation involves administration of the whole commensal microbial community from healthy donor stool into the recipient's intestinal tract to normalise or modify intestinal microbiota composition and function and has now become widely accepted as a highly successful rescue treatment for recurrent infections (i.e.…”

Section: Discussionmentioning

confidence: 99%

Early intervention with faecal microbiota transplantation: an effective means to improve growth performance and the intestinal development of suckling piglets

Cheng

Wei

Wang

et al. 2019

Animal

View full text Add to dashboard Cite

Recent studies indicate that early postnatal period is a critical window for gut microbiota manipulation to optimise the immunity and body growth. This study investigated the effects of maternal faecal microbiota orally administered to neonatal piglets after birth on growth performance, selected microbial populations, intestinal permeability and the development of intestinal mucosal immune system. In total, 12 litters of crossbred newborn piglets were selected in this study. Litter size was standardised to 10 piglets. On day 1, 10 piglets in each litter were randomly allotted to the faecal microbiota transplantation (FMT) and control groups. Piglets in the FMT group were orally administrated with 2ml faecal suspension of their nursing sow per day from the age of 1 to 3 days; piglets in the control group were treated with the same dose of a placebo (0.1M potassium phosphate buffer containing 10% glycerol (vol/vol)) inoculant. The experiment lasted 21 days. On days 7, 14 and 21, plasma and faecal samples were collected for the analysis of growth-related hormones and cytokines in plasma and lipocalin-2, secretory immunoglobulin A (sIgA), selected microbiota and short-chain fatty acids (SCFAs) in faeces. Faecal microbiota transplantation increased the average daily gain of piglets during week 3 and the whole experiment period. Compared with the control group, the FMT group had increased concentrations of plasma growth hormone and IGF-1 on days 14 and 21. Faecal microbiota transplantation also reduced the incidence of diarrhoea during weeks 1 and 3 and plasma concentrations of zonulin, endotoxin and diamine oxidase activities in piglets on days 7 and 14. The populations of Lactobacillus spp. and Faecalibacterium prausnitzii and the concentrations of faecal and plasma acetate, butyrate and total SCFAs in FMT group were higher than those in the control group on day 21. Moreover, the FMT piglets have higher concentrations of plasma transforming growth factor-β and immunoglobulin G, and faecal sIgA than the control piglets on day 21. These findings indicate that early intervention with maternal faecal microbiota improves growth performance, decreases intestinal permeability, stimulates sIgA secretion, and modulates gut microbiota composition and metabolism in suckling piglets.

show abstract

“…In addition, clinical trials consistently show lower immunogenicity for vaccines in developing world populations, including the BCG vaccine and those against poliomyelitis and rotavirus . Although many factors, such as genetics, prior Ag exposure, and maternal vaccination, can influence vaccine immunogenicity, several lines of evidence now suggest that the microbiota is also a significant factor . In this review, we summarize the evidence that the gut microbiota can influence vaccine responses and discuss potential mechanisms through which this can occur (Fig.…”

Section: Introductionmentioning

confidence: 99%

The potential of the microbiota to influence vaccine responses

Lynn

Pulendran

2017

Journal of Leukocyte Biology

View full text Add to dashboard Cite

After clean water, vaccines are the primary public health intervention providing protection against serious infectious diseases. Antigen-specific antibody-mediated responses play a critical role in the protection conferred by vaccination; however these responses are highly variable among individuals. In addition, vaccine immunogenicity is frequently impaired in developing world populations, for reasons that are poorly understood. Although the factors that are associated with interindividual variation in vaccine responses are likely manifold, emerging evidence from mouse models and studies in human populations now suggests that the gut microbiome plays a key role in shaping systemic immune responses to both orally and parenterally administered vaccines. Herein, we review the evidence to date that the microbiota can influence vaccine responses and discuss the potential mechanisms through which these effects may be mediated. In addition, we highlight the gaps in this evidence and suggest future directions for research.

show abstract

The Impact of the Gut Microbiota on Humoral Immunity to Pathogens and Vaccination in Early Infancy

Cited by 55 publications

References 36 publications

Early-Life Intervention Using Fecal Microbiota Combined with Probiotics Promotes Gut Microbiota Maturation, Regulates Immune System Development, and Alleviates Weaning Stress in Piglets

Early-Life Intervention Using Fecal Microbiota Combined with Probiotics Promotes Gut Microbiota Maturation, Regulates Immune System Development, and Alleviates Weaning Stress in Piglets

Early intervention with faecal microbiota transplantation: an effective means to improve growth performance and the intestinal development of suckling piglets

The potential of the microbiota to influence vaccine responses

Contact Info

Product

Resources

About