Obese Subjects With Specific Gustatory Papillae Microbiota and Salivary Cues Display an Impairment to Sense Lipids

Philippe Besnard,Laurent Lagrost,Benjamin Lelouvier,Arnaud Bernard,Rémy Burcelin,Jeffrey E Christensen,Florence Servant,Sophie Nicklaus,Patricia Passilly-Degrace,Hélène Brignot,Bruno Verges,Gilles Feron,Jean-Paul Pais De Barros,Xavier Collet,Vincent Blasco-Baque

doi:10.1038/s41598-018-24619-1

Abstract

Some obese subjects overeat lipid-rich foods. The origin of this eating behavior is unknown. We have here tested the hypothesis that these subjects could be characterized by an impaired fatty taste sensitivity linked to a change in the gustatory papillae microbial and salivary environment. The composition of microbiota and saliva surrounding the circumvallate papillae was analyzed in combination with the orosensory lipid detection threshold in normal weight (NW) and obese (O) adults. Microbial architecture was similar to what was known in feces, but with an increased frequency of Proteobacteria. No difference in the orosensory sensitivity to lipids and composition of oral microbiota and saliva was observed between NW and O subjects. By contrast, specific bacterial and salivary signatures were found in lipid non-tasters, irrespectively of BMI. A multivariate approach highlighted that the salivary flow, lysozyme activity, total antioxidant capacity and TM7 bacterial family discriminated between tasters and non-tasters. Subgroup analysis of obese tasters (OT) versus obese non-tasters (ONT) identified specific bacterial metabolic pathways (i.e. phosphotransferase and simple sugar transport systems) as being higher in ONT. Altogether with the identification of a set of significant salivary variables, our study suggests that an “obese tongue” phenotype is associated with decreased orosensory sensitivity to lipids in some obese subjects.

Highlights

The orosensory detection threshold of a fatty acid widely found in foods, microbiota composition in the direct vicinity of circumvallate papillae (CVP), and salivary parameters known to be involved in the oral fat sensitivity were determined in normal weight (NW) (BMI < 25 kg/ m2) and O (BMI ≥ 30 kg/m2) volunteers
obese non-tasters (ONT) were more numerous than NWNT (n = 8 and 4, respectively - Fig. 1), suggesting that obesity increases the susceptibility to be poorly sensitive to oral lipid stimulation
Existence of a sixth taste modality responsible for the oral detection of dietary lipids was supported by a growing number of studies both in rodents and humans[17,28]

Summary

Introduction

An obesity-related dysfunction of the orosensory system responsible for the oral detection and central perception of dietary lipids may be suspected[4] Consistent with this assumption, neuroimaging studies have highlighted the existence of structural remodeling and functional alterations in brain areas (i.e. cortico-mesolimbic system) involved both in food perception and reward processing in some obese subjects[5]. Whether specific features of the microbiota and/or saliva surrounding the CVP contribute to obesity by compromising orosensory sensitivity to lipids remains to be determined In accordance with these observations, we hypothesized that obesity might be characterized in some subjects by an “obese tongue” phenotype leading to a change in sensitivity of their oral fat detection system. Microbiotal, and/or salivary variables were the most discriminant to characterize these subjects, we performed three complementary comparisons on: (i) BMI (NW vs O), (ii) sensitivity of oral fat detection in all subjects (LA taster [T] vs LA non-taster [NT]) and (iii) in obese only (obese taster [OT] vs obese non-taster [ONT])

Methods

Results

Conclusion