Identification of an oral microbiota signature associated with an impaired orosensory perception of lipids in insulin-resistant patients

Philippe Besnard,Xavier Collet,Rémy Burcelin,Jeffrey E Christensen,Isabelle Simoneau-Robin,Bruno Verges,Arnaud Bernard

doi:10.1007/s00592-020-01567-9

Abstract

AimsType 2 diabetes leads to multiple sensory dysfunctions affecting notably the gustatory sensitivity. Although this sensory defect, by impacting food choices, might lead to unhealthy eating behavior, underlying mechanisms remains poorly studied. We have recently reported that the composition of microbiota in contact with circumvallate gustatory papillae might affect the orosensory perception of lipids in lean and normoglycemic obese subjects. This finding has prompted us to explore whether such a phenomenon also occurs in diabetic obese patients.MethodsThe composition of microbiota surrounding the circumvallate papillae was analyzed in combination with the linoleic acid perception thresholds in male insulin-resistant patients and weight-matched healthy controls. Two complementary comparisons were performed: (1) controls vs diabetic and (2) diabetic low-lipid tasters versus diabetic high-lipid tasters.ResultsDespite subtle modifications in the oral microbiota composition, comparison of orosensory lipid perception in controls and diabetic subjects did not lead to discriminating data due to the large inter-individual variability of linoleic acid perception thresholds. In contrast, specific bacterial signatures were found by comparing diabetic low- and high-lipid tasters leading to differential molecular pathways. Surprisingly, a lower fatty taste perception was mainly found in patients treated with metformin and/or statins, suggesting a possible side effect of these antidiabetic and/or hypolipidemic drugs on taste acuity.ConclusionsCollectively, these data show that the diabetic patients with defective fatty taste detection are characterized by a specific microbiota metabolism at the circumvallate papillae levels, this occurrence seeming amplified by drugs commonly used to counteract the damaging metabolic effects of T2D.Trial registration for original previous studies: ClinicalTrials.gov #NCT02028975

Highlights

The prevalence of type 2 diabetes (T2D) has increased dramatically in the past decades becoming a major health issue worldwide
Consistent with previous studies [16, 17], we observed a large inter-individual variability in linoleic acid (LA) perception thresholds that led to a lack of significant difference between obese C and D patients (Fig. 2a)
A similar inter-individual heterogeneity of LA perception threshold was found in D patients and in weight-matched controls suggesting that insulin resistance, as such, does not play a major role in the modulation of fatty taste sensitivity

Summary

Introduction

The prevalence of type 2 diabetes (T2D) has increased dramatically in the past decades becoming a major health issue worldwide This obesity-related disease is associated with metabolic disorders at the origin of serious long-term health problems (heart disease, stroke, hypertension, eye and kidney damages, neuro-degeneration), mainly due to vascular and nerve impairments. Since sweet and salt tastes are strong contributors of hedonic value of foods, this gustatory blunting might lead to eating behavior changes in order to reach the expected food reward Consistent with this assumption, cravings for sugar-rich foods were more common in patients with T2DM than in age-, sex- and BMI-matched controls, this phenomenon being tightly related to a poor glycemic control [8]

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Conclusion