The role of the gut microbiota on the metabolic status of obese children

Abstract

Background: The term "metabolically healthy obese (MHO)" denotes a hale and salutary status, yet this connotation has not been validated in children, and may, in fact, be a misnomer. As pertains to obesity, the gut microbiota has garnered attention as conceivably a nosogenic or, on the other hand, protective participator.

Objective: This study explored the characteristics of the fecal microbiota of obese Chinese children and adolescents of disparate metabolic statuses, and the associations between their gut microbiota and circulating proinflammatory factors, such as IL-6, TNF-α, lipopolysaccharide-binding protein (LBP), and a cytokine up-regulator and mediator, leptin.

Results: Based on weight and metabolic status, the 86 Chinese children (ages 5-15 years) were divided into three groups: metabolically healthy obese (MHO, n = 42), metabolic unhealthy obese (MUO, n = 23), and healthy normal weight controls (Con, n = 21). In the MUO subjects, the phylum Tenericutes, as well as the alpha and beta diversity, were significantly reduced compared with the controls. Furthermore, Phylum Synergistetes and genus Bacteroides were more prevalent in the MHO population compared with controls. For the MHO group, Spearman's correlation analysis revealed that serum IL-6 positively correlated with genus Paraprevotella, LBP was positively correlated with genus Roseburia and Faecalibacterium, and negatively correlated with genus Lactobacillus, and leptin correlated positively with genus Phascolarctobacterium and negatively with genus Dialister (all p < 0.05).

Conclusion: Although there are distinct differences in the characteristic gut microbiota of the MUO population versus MHO, dysbiosis of gut microsystem is already extant in the MHO cohort. The abundance of some metabolism-related bacteria associates with the degree of circulating inflammatory compounds, suggesting that dysbiosis of gut microbiota, present in the MHO children, conceivably serves as a compensatory or remedial response to a surfeit of nutrients.

Keywords: 16s rRNA; Children; Gut microbiota; Metabolically healthy obese.

Fig. 1

Bar chart representing Mann–Whitney U-test results on operational taxonomic units (OTUs) grouped in phyla (a, c, e) and in genus (b, d, f) of the different metabolic status groups. Each column in the plot represents a group, and each color in the column represents the percentage of relative abundance for each OTU. MUO metabolic unhealthy obese, MHO metabolically healthy obese, Con controls

Fig. 2

Characterization of alpha- and beta-diversity of the gut microbiota in Con, MUO and MHO groups. The y-axes show the Shannon index (a, c) and Chao1 richness index (b, d). The x-axes show the phenotypic categories. Additional data are in Additional file 1: Table S2. Principal coordinates analysis (PCoA) plot of Con and MHO children and MUO subjects (e). The plots show the first two principal coordinates (axes) for PCoA using Bray–Curtis Distance method. MUO metabolic unhealthy obese, MHO metabolically healthy obese, Con controls

Fig. 3

Differential biomarkers associated with different metabolic status. A linear discriminant effect size (LeFse) analysis have been performed (α value = 0.05, logarithmic LDA score threshold = 2.0). MUO metabolic unhealthy obese, MHO metabolically healthy obese, Con controls

Fig. 4

KEGGs biomarkers associated with the three metabolic statuses. MUO metabolic unhealthy obese, MHO metabolically healthy obese, Con controls