Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers

Abstract

Objective: Obesity alters gut microbiota ecology and associates with low-grade inflammation in humans. Roux-en-Y gastric bypass (RYGB) surgery is one of the most efficient procedures for the treatment of morbid obesity resulting in drastic weight loss and improvement of metabolic and inflammatory status. We analyzed the impact of RYGB on the modifications of gut microbiota and examined links with adaptations associated with this procedure.

Research design and methods: Gut microbiota was profiled from fecal samples by real-time quantitative PCR in 13 lean control subjects and in 30 obese individuals (with seven type 2 diabetics) explored before (M0), 3 months (M3), and 6 months (M6) after RYGB.

Results: Four major findings are highlighted: 1) Bacteroides/Prevotella group was lower in obese subjects than in control subjects at M0 and increased at M3. It was negatively correlated with corpulence, but the correlation depended highly on caloric intake; 2) Escherichia coli species increased at M3 and inversely correlated with fat mass and leptin levels independently of changes in food intake; 3) lactic acid bacteria including Lactobacillus/Leuconostoc/Pediococcus group and Bifidobacterium genus decreased at M3; and 4) Faecalibacterium prausnitzii species was lower in subjects with diabetes and associated negatively with inflammatory markers at M0 and throughout the follow-up after surgery independently of changes in food intake.

Conclusions: These results suggest that components of the dominant gut microbiota rapidly adapt in a starvation-like situation induced by RYGB while the F. prausnitzii species is directly linked to the reduction in low-grade inflammation state in obesity and diabetes independently of calorie intake.

FIG. 1.

Quantifications of fecal microbiota in lean control subjects and obese subjects before (M0) and after surgery (M3 and M6). The qPCR results were plotted as boxes and whiskers graph. The boxes (containing 50% of all values) show the median (horizontal line across the middle of the box) and interquartile range, while the whiskers represent the 10th and 90th percentiles. The extreme data points are indicated as circles. Data not sharing the same letter in parentheses within a horizontal line are significantly different (P < 0.05).

FIG. 2.

Relationship between changes in fecal microbiota composition and clinical parameters in obese patients following RYGB surgery. Real-time qPCR quantifications were used to determine the fecal microbiota composition for the bacterial groups indicated in supplementary Table 6. Clinical parameters included adipocyte cell size, BMI, calorie intake, HOMA-IR, leptin, and orosomucoid. A: Principal component analysis (between class analyses). Bold arrows indicate the marked inverse relationship between changes in E. coli population and leptin serum concentrations. B: Dynamics of E. coli population evolution and leptin concentration during the study. E. coli population levels are expressed as mean ± SEM of the Δlog₁₀ value of normalized data calculated as the log number of targeted bacteria minus the log number of all bacteria. Leptin results were expressed as mean ± SEM of serum concentrations.