Effect of Short-Term Dietary Intervention and Probiotic Mix Supplementation on the Gut Microbiota of Elderly Obese Women

Raffaella Cancello, Silvia Turroni, Simone Rampelli, Stefania Cattaldo, Marco Candela, Laila Cattani, Stefania Mai, Roberta Vietti, Massimo Scacchi, Patrizia Brigidi, Cecilia Invitti, Raffaella Cancello, Silvia Turroni, Simone Rampelli, Stefania Cattaldo, Marco Candela, Laila Cattani, Stefania Mai, Roberta Vietti, Massimo Scacchi, Patrizia Brigidi, Cecilia Invitti

Abstract

Accumulating literature is providing evidence that the gut microbiota is involved in metabolic disorders, but the question of how to effectively modulate it to restore homeostasis, especially in the elderly, is still under debate. In this study, we profiled the intestinal microbiota of 20 elderly obese women (EO) at the baseline (T0), after 15 days of hypocaloric Mediterranean diet administered as part of a nutritional-metabolic rehabilitation program for obesity (T1), and after a further 15 days of the same diet supplemented with a probiotic mix (T2). Fecal samples were characterized by Illumina MiSeq sequencing of the 16S rRNA gene. The EO microbiota showed the typical alterations found in obesity, namely, an increase in potential pro-inflammatory components (i.e., Collinsella) and a decrease in health-promoting, short-chain fatty acid producers (i.e., Lachnospiraceae and Ruminococcaceae members), with a tendency to reduced biodiversity. After 15 days of the rehabilitation program, weight decreased by (2.7 ± 1.5)% and the gut microbiota dysbiosis was partially reversed, with a decline of Collinsella and an increase in leanness-related taxa. During the next 15 days of diet and probiotics, weight dropped further by (1.2 ± 1.1)%, markers of oxidative stress improved, and Akkermansia, a mucin degrader with beneficial effects on host metabolism, increased significantly. These findings support the relevant role of a correct dietetic approach, even in the short term, to modulate the EO gut microbiota towards a metabolic health-related configuration, counteracting the increased risk of morbidity in these patients.

Keywords: Mediterranean diet; elderly; gut microbiota; obesity; probiotics.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The gut microbiota of obese elderly women segregates from that of healthy elders. (A) Box plots showing the distribution of alpha diversity values, according to the inverse Simpson index, in elderly subjects with class I (OB1), class II (OB2) and class III (OB3) obesity, as compared to healthy non-obese controls (EC). Samples are identified with gray dots within boxes. A significantly reduced biodiversity was observed in OB2 patients compared to EC (p = 0.03, Wilcoxon test). (B) PCoA plot of inter-sample diversity, based on Bray–Curtis distances between the genus-level microbial profiles. A significant separation between obese elderly patients and EC was found (p = 1 × 10−5, permutation test with pseudo-F ratios). Samples are identified with colored dots as in A. Ellipses include 99% confidence area based on the standard error of the weighted average of sample coordinates (lilac, elderly obese patients; green, EC).
Figure 2
Figure 2
Genus-level compositional differences in the gut microbiota of obese vs. healthy elders. Box plots showing the distribution of the relative abundance values of discriminant genera between obese (EO) and non-obese healthy elders (EC). Samples from EO patients with class I (OB1, pink), class II (OB2, red) and class III (OB3, brown) obesity are identified with colored dots within boxes. p ≤ 0.05, Wilcoxon test.
Figure 3
Figure 3
Diet and probiotic mix supplementation improve oxidative stress and stool consistency, and reduce fecal calprotectin levels in elderly obese women. (A) Circulating levels of reduced (GSH) and oxidized (GSSG) glutathione, (B) GSH/GSSG ratio, (C) stool consistency by Bristol stool scale (BSS) ranging from type 1 to type 7, where types 1–2 indicate constipation, types 3–4 ideal stools and types 5–7 diarrhea and urgency, and (D) fecal calprotectin concentrations in elderly obese patients before intervention (T0), after two weeks of hypocaloric balanced Mediterranean diet (T1) and after two additional weeks of diet with probiotic mixture supplementation (T2). Data are expressed as mean ± SD. * p < 0.05; ** p < 0.0001, ANOVA.
Figure 4
Figure 4
Diet and probiotic mix supplementation impact on the gut microbiota diversity of elderly obese women. (A) Alpha diversity values, according to the inverse Simpson index, in elders with class I (OB1), class II (OB2) and class III (OB3) obesity, before intervention (T0), after two weeks of hypocaloric balanced Mediterranean diet (T1) and after two additional weeks of diet with probiotic mixture supplementation (T2). On the right, as a control, the biodiversity of the gut microbiota of healthy non-obese elders (EC). Within each group (OB1 to OB3 and EC), samples are colored by subject. The black line within each series indicates the median value. A significantly increased biodiversity was observed in OB2 patients at T1 compared to the baseline (p = 0.04; Wilcoxon test). (B) PCoA plot based on Bray–Curtis distances between the genus-level microbiota profiles of EO patients at the baseline (pink), T1 (light yellow) and T2 (yellow). Ellipses include 99% confidence area based on the standard error of the weighted average of sample coordinates. No significant segregation was found (p > 0.05, permutation test with pseudo-F ratios).
Figure 5
Figure 5
Diet and probiotic mix supplementation counteract the obesity-related dysbiotic features of the gut microbiota in elderly obese women. (A) Box plots showing the distribution of the relative abundance values of significantly altered bacterial genera over the course of the intervention (p ≤ 0.05, Wilcoxon test). For Oscillospira and Faecalibacterium, only trends were observed (p ≤ 0.08). T0, before intervention; T1, after two weeks of hypocaloric balanced Mediterranean diet; T2, after two additional weeks of diet with probiotic mixture supplementation. Samples are identified with colored dots within boxes, based on the obesity grade as assessed at T0 and T2 (pink, class I obesity—OB1; red, class II obesity—OB2; brown, class III obesity—OB3). EC, healthy non-obese elderly. *, unclassified OTU reported at higher taxonomic level. (B) Relative abundance dynamics for the genera of panel A. Changes in mean values (±SD) are shown by obesity grade (same color code as in A). The dotted line indicates the mean value in the control population (i.e., EC).

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