Distinctive microbiomes and metabolites linked with weight loss after gastric bypass, but not gastric banding - PubMed (original) (raw)

Distinctive microbiomes and metabolites linked with weight loss after gastric bypass, but not gastric banding

Zehra Esra Ilhan et al. ISME J. 2017 Sep.

Abstract

Roux-en-Y gastric bypass (RYGB) and laparoscopic adjustable gastric banding (LAGB) are anatomically different bariatric operations. RYGB achieves greater weight loss compared with LAGB. Changes in the gut microbiome have been documented after RYGB, but not LAGB, and the microbial contribution to sustainable surgical weight loss warrants further evaluation. We hypothesized that RYGB imposes greater changes on the microbiota and its metabolism than LAGB, and that the altered microbiota may contribute to greater weight loss. Using multi-omic approaches, we analyzed fecal microbial community structure and metabolites of pre-bariatric surgery morbidly obese (PreB-Ob), normal weight (NW), post-RYGB, and post-LAGB participants. RYGB microbiomes were significantly different from those from NW, LAGB and PreB-Ob. Microbiome differences between RYGB and PreB-Ob populations were mirrored in their metabolomes. Diversity was higher in RYGB compared with LAGB, possibly because of an increase in the abundance of facultative anaerobic, bile-tolerant and acid-sensible microorganisms in the former. Possibly because of lower gastric acid exposure, phylotypes from the oral cavity, such as Escherichia, Veillonella and Streptococcus, were in greater abundance in the RYGB group, and their abundances positively correlated with percent excess weight loss. Many of these post-RYGB microorganisms are capable of amino-acid fermentation. Amino-acid and carbohydrate fermentation products-isovalerate, isobutyrate, butyrate and propionate-were prevalent in RYGB participants, but not in LAGB participants. RYGB resulted in greater alteration of the gut microbiome and metabolome than LAGB, and RYGB group exhibited unique microbiome composed of many amino-acid fermenters, compared with nonsurgical controls.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1

Figure 1

Subject’s BMI, %EWL and average daily calorie intake. (a) BMI distribution of the participants that participated in this study. Empty circles represent BMI at the time of sampling and full circles represent recorded BMI before surgeries retrospectively. The horizontal dashed lines indicate the BMI-based weight categories according to National Institutes of Health guidelines (nhlbi.nih.gov). (b) %EWL for the RYGB and LAGB groups. The RYGB group had significantly higher % EWL than the LAGB participants. (c) Median calorie intake per experimental group. *Denotes Mann–Whitney _U_-test P<0.05.

Figure 2

Figure 2

Microbial community structure after RYGB and LAGB surgeries compared with NW and PreB-Ob controls. (a) Unweighted Unifrac distances between the samples visualized using principal coordinate analysis showed two distinctive clusters: RYGB and PreB-Ob. (b) Pairwise comparison of median unweighted Unifrac distances between the groups. (c) Class-level phylotypes on principal coordinates show the taxa that are responsible for clustering of RYGB participants. (d) Relative abundance of the four main class-level phylotypes that separated the RYGB group from NW, LAGB and PreB-Ob groups. (e) Principal component analysis (PCA) of fecal metabolites. (f) Spearman’s rho correlations between Gammaproteobacteria, Fusobacteriia, Flavobacteriia and Bacilli and fecal metabolites.

Figure 3

Figure 3

Within-community variation and alpha diversity indexes reveal differences in the community structure. (a) Within-group Unweighted Unifrac distance was the smallest for the RYGB group. Alpha diversity parameters: (b) PD whole tree and (c) equitability indexes for diversity and evenness.

Figure 4

Figure 4

Significantly abundant genera in the RYGB participants compared with the other groups. * and ** denote P<0.01 and P<0.05, respectively, of Mann–Whitney _U-_test adjusted results.

Figure 5

Figure 5

Fecal fermentation products and substrates. (a) The most abundant fermentation products: acetate, propionate and butyrate showed different distribution among the groups. (b) Ratios of butyrate-to-acetate and propionate-to-acetate were greatest in the RYGB group compared with NW, LAGB and PreB-Ob groups. (c) Isobutyrate and isovalerate, which are fermentation products of BCAAs (isoleucine and valine), were at greater abundance in the RYGB group compared with the other groups. (d) BCAAs: valine, leucine and isoleucine concentrations did not significantly vary among the groups. (e) PICRUSt predicted relative abundance of the genes involved in the consumption and production of BCFAs. (f) Illustration of conversion of carbohydrates and proteins into short chain and branched chain fatty acids by significantly abundant taxa in RYGB participants. * and ** denote Mann–Whitney _U_-test _P_adj value <0.05 and <0.01, respectively.

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