Gut microbial dysbiosis is associated with allergen-specific IgE responses in young children with airway allergies

Abstract

Background There is increasing evidence linking alterations of the gut microbial composition during early infancy to the development of atopic diseases and asthma. However, few studies have addressed the association of dysbiotic gut microbiota with allergic reactions through evaluation of feces in young children with allergic airway diseases. Methods We sought to evaluate relationships among gut microbiota, total fecal immunoglobulin E (IgE) levels, serum allergic sensitization, and their relevance to childhood allergic rhinitis and asthma. Microbial composition and diversity were analyzed with Illumina-based 16S rRNA gene sequencing of 89 stool samples collected from children with asthma (n = 35) and allergic rhinitis (n = 28), and from healthy controls (n = 26). Data analysis was performed using Quantitative Insights into Microbial Ecology (QIIME) software. Results A significantly lower abundance of organisms of the phylum Firmicutes were found in children with asthma and allergic rhinitis than in the healthy controls. Relatively lower Chao1 and Shannon indices were also found in children with allergic airway diseases but without any significant difference. Total fecal IgE levels in early childhood were strongly correlated with serum D. pteronyssinus - and D. farinae -specific IgE but not with food-specific IgE levels. In comparison with healthy controls, the genus Dorea was less abundant and negatively correlated with total fecal IgE levels in children with rhinitis, whereas the genus Clostridium was abundant and positively correlated with fecal IgE levels in children with asthma. Conclusions An interaction between particular subsets of gut microbial dysbiosis and IgE-mediated responses to allergens may contribute to the susceptibility to allergic rhinitis and asthma in early childhood.

Gut Microbiome and Serum Metabolome Analyses Identify Unsaturated Fatty Acids and Butanoate Metabolism Induced by Gut Microbiota in Patients With Chronic Spontaneous Urticaria

“…Both the ACE and Shannon indices reflected a reduction in the bacterial diversity and richness in CSU patients, which is highly consistent with other allergic diseases (Bisgaard et al, 2011). At the phylum level, when compared with healthy controls, there was a relative reduced abundance of Bacteroidetes and Firmicutes in CSU patients, which is partly in agreement with the airway allergies in young children (Chiu et al, 2019). At the genus level, members of the Bacteroides, Faecalibacterium, Bifidobacterium, Lactobacillus, and unidentified Ruminococcaceae were relatively lower and members of unidentified Enterobacteriaceae were relatively increased compared to healthy controls, which is partly consistent with previous studies about CU or allergic diseases (Sjogren et al, 2009;Johansson et al, 2011;Candela et al, 2012;Nabizadeh et al, 2017;Rezazadeh et al, 2018;Chiu et al, 2019).…”

“…At the phylum level, when compared with healthy controls, there was a relative reduced abundance of Bacteroidetes and Firmicutes in CSU patients, which is partly in agreement with the airway allergies in young children (Chiu et al, 2019). At the genus level, members of the Bacteroides, Faecalibacterium, Bifidobacterium, Lactobacillus, and unidentified Ruminococcaceae were relatively lower and members of unidentified Enterobacteriaceae were relatively increased compared to healthy controls, which is partly consistent with previous studies about CU or allergic diseases (Sjogren et al, 2009;Johansson et al, 2011;Candela et al, 2012;Nabizadeh et al, 2017;Rezazadeh et al, 2018;Chiu et al, 2019). For example, Nabizadeh et al (2017) and Rezazadeh et al (2018) reported a depletion in the relative amounts of Faecalibacterium prausnitzii, Clostridia, Akkermansia muciniphila, Bifidobacterium, and Lactobacillus in CU patients.…”

“…Recent evidence revealed that the abundance of butyrate was decreased in children with asthma and was negatively correlated with serum IgE levels. This suggests that the dysregulation of the intestinal epithelial barrier due to reduced butyrate secretion may be related to allergen uptake and immunological responses in allergic asthma (Chiu et al, 2019). We detected a decrease in the serum levels of glutamate and succinic acid in CSU patients which both belong to butanoate metabolism.…”

The role of gut microbiota in atopic asthma and allergy, implications in the understanding of disease pathogenesis

“…It was hypothesized that commensal‐driven signals limit isotype switching to IgE and direct it towards IgA and reduce levels of circulating basophils which in turn alleviates lung inflammation . A recent study revealed that antigens contributing to childhood airway diseases were associated with alterations in the composition of gut microbiota and elevated levels of faecal IgE . Another study showed that early exposure to intestinal microbiota reduces the levels of invariant natural killer T (iNKT) cells which produce IL‐4 and IL‐13 that accumulate in the lungs of GF mice and promote isotype switching to IgE .…”

“…4,29 A recent study revealed that antigens contributing to childhood airway diseases were associated with alterations in the composition of gut microbiota and elevated levels of faecal IgE. 33 Another study showed that early exposure to intestinal microbiota reduces the levels of invariant natural killer T (iNKT) cells which produce IL-4 and IL-13 that accumulate in the lungs of GF mice and promote isotype switching to IgE. 34 An increase in iNKT cells caused by microbial deficiency leads to increased susceptibility to asthma (Figures 1 and 2).…”