Impact of Diet on Gut Microbiota Composition and Microbiota-Associated Functions in Heart Failure: A Systematic Review of In Vivo Animal Studies
Abstract
:1. Introduction
2. Methods
2.1. Inclusion Criteria
2.2. Data Sources and Search Strategy
2.3. Study Selection
2.4. Data Extraction and Reporting
2.5. Quality Assessment
3. Results
3.1. Study Selection
3.2. Study Characteristics
3.3. Results
3.3.1. Impact of Diet Rich in Fiber on Gut Microbiota Composition and Functions in HF
3.3.2. Impact of Choline Diet on Gut Microbiota Composition and Functions in HF
3.3.3. Impact of Western/Obesogenic Diet on Gut Microbiota Composition and Functions in HF
3.3.4. Impact of Polyphenols on Gut Microbiota Composition and Functions in HF
3.4. Quality Assessment
4. Discussion
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Population | Animals or Humans |
---|---|
Intervention | Diet interventions (dietary factors or dietary patterns or prebiotic intake) |
Comparator | Any comparator |
Gut microbial outcomes | Differences in alpha diversity (Chao1 index, Shannon diversity index, Simpson diversity index) and beta diversity of fecal microbiota at the end of the intervention |
Differences in abundance of bacterial taxa | |
Differences in fecal SCFAs, muc-2 gene expression, TMAO levels, indole levels, phenol indoxyl sulfate, indole acetic acid levels, LPS levels | |
Heart failure outcomes | Blood pressure (in mmHg) Cardiac hypertrophy (in mm) Ventricular thickness (in mm) Left ventricular ejection fraction (%) BNP (in pg/mL) Interstitial fibrosis (%) Cardiac remodeling |
Study design | All types |
First Author, Year of Publication, Country | Animal Type | Sample | Dietary Intervention Type | Duration of Dietary Intervention | Methods of Characterization of Microbiota and/or Metabolites | Changes in Gut Microbiota (Compared with Control Groups) | Effects on Microbiota-Associated Functions (Compared with Control Group) | Effects on Heart Failure Outcomes |
---|---|---|---|---|---|---|---|---|
Fiber diet | ||||||||
Jama, 2020, Australia [35] | C57BL/6 male mice 1 | N = 48 7–8 mice/group 2 groups DCM mice WT mice | 3 interventions High-RS diet (High-fiber SF11-025, Specialty Feeds) Control diet with acetate supplementation (magnesium acetate, Sigma-Aldrich, 200 mM in drinking water) Control chow diet | 7 weeks | 16S rRNA amplicon sequencing | Irrespective of mice type: ● significant compositional variations in high-RS diet vs. control diet ● ↑ Bacteriodetes and Bacteriodales abundance in mice following high-RS diet vs. control diet | Significant expansion of splenic T regulatory (Treg) cells in DCM mice fed a high-RS diet (p = 0.009) vs. WT mice. and a non-significant increase compared to DCM mice on the control diet (p = 0.05) | In high-RS diet or acetate supplementation vs. control diet, in DCM mice, no significant improvements in: ● cardiac hypertrophy ● cardiac remodeling ● systolic and diastolic pressure |
Zhang, 2020, China [36] | Healthy specific-pathogen-free C57BL/6J male mice2 | N = 18 6/group | Control diet HFD HFD + oral Lycium barbarum polysaccharide 100 mg/kg once a day (HFPD) | 2 months | 16S rRNA amplicon sequencing | ● ↑ Bacteroides, Muribaculum, Alistipes, Parasuterella, and Alloprevotella abundance in control group vs. HFD diet groups. ● ↑ Lactobacillus, Bifidobacterium, Enterococcus, Lactococcus, Romboutsia in the HFD group vs. control group ● ↑ Gordonibacter, Parabacteroides, Anaerostipes, Blautia, Hungatella, Marvin bryantia abundance in the HFPD group vs. other groups. | ● ↑ the indole derivatives (indole-3-acrylic acid, methyl indole-3-acetate, and DI-indole-3-lactic acid) in HFPD vs. HFD group ● ↑ intestinal permeability in the HFD fed mice vs. control ● ↓ intestinal permeability in HFPD group | ● In the HFD group, depressed left ventricular systolic function and abnormal diastolic relaxation ● In the HFD group vs. the control and HFPD groups, ↑ cardiac remodeling (↑ LVPWd, LVPWs LVAWd,…, LVAWs, and ↓ LVIDd, LVIDs, LVEDd, LVEDs, EF, and FS) |
Vlasov, 2020, Russia [37] | Female adult rats | N = 30 n = 10 female rats/group 3 groups - HF female rats - control healthy - control group HF female rats | Pre-treatment with prebiotic complex (fermented wheat bran and inactivated Saccharomyces cerevisiae culture) Control | 7 days | Not specified | HF rats vs. controls ● ↑ Prevotella spp., Fusobacterium spp., Kingella spp., Enterococcus spp., Clostridium spp., and Lactobacillus spp. abundance ● ↓ Bifidobacterium spp., Propionibacterium spp., and Eubacterium spp. abundance HF rats pretreated with prebiotic complex vs. HF rats ● ↓ Pretovella spp., Fusobacterium spp., Helicobacter pylori, Lactobacillus spp., Enterococcus spp., Actinomyces abundance ● ↑Bifidobacterium spp., Propionibacterium spp., and Eubacterium spp. abundance | HF rats vs. controls ● ↑ endotoxemia LPS levels (p = 0.03) HF pretreated with prebiotic complex vs. HF rats ● ↓ endotoxemia LPS levels (p = 0.02) | |
Marques, 2017, Australia [38] | C57Bl/6 male mice 3 (hypertension induced by treatment with uni- nephrectomy and implantation of deoxycorticosteroid acetate or sham pellets) | N = 64 n= 6–15 mice/group 6 groups - sham + control -DOCA + control -DOCA + fiber -DOCA + acetate - sham + fiber -sham + acetate | Control High-fiber diet (72,7% fiber) SCFA supplementation (200 mmol/L magnesium acetate) | 6 weeks | 16S rRNA amplicon sequencing | ● Significant compositional variations in mice fed a control diet vs. high-fiber diet (in both sham and DOCA groups) ● ↑ acetate-producing bacteria in mice fed with high-fiber diet ● ↓ Firmicutes to Bacteroidetes ratio (F/B) in mice fed with high-fiber diet or acetate ● ↑ levels of Bacteroides acidifaciens spp. in mice fed a high-fiber diet or acetate vs. mice fed the control chow | In high-fiber diet and acetate supplementation groups: ● ↓ systolic blood pressure ● ↓ cardiac hypertrophy ● ↓ left ventricular wall thickness ● ↓ left ventricular chamber dilatation In mice fed with acetate supplementation: ● ↓ renal fibrosis | |
Choline diet | ||||||||
Organ, 2016, USA [39] | C57BL6/J male mice 4 (cardiac pressure overload and HF were induced using transverse aortic constriction TAC surgery) | N = 36 n = 10–12 mice/group | Control diet (TD.130104) Diet containing 0.12% TMAO added to the standard rodent chow (TD.07865) Diet containing 1.2% choline added to the standard rodent chow (TD.09041) | 15 weeks | Stable isotope dilution LC/MS/MS for quantification of the total choline, TMA, TMAO, and betaine levels | ● ↑ TMAO levels in mice fed either TMAO or choline vs. mice fed a control diet ● ↑ plasma betaine levels in the mice fed TMAO vs. mice fed a control diet | In mice fed either TMAO or choline vs. mice fed a control diet: ● ↓ cardiac function ● ↑ left ventricular end-systolic diameter and end-diastolic diameter ● ↓ IVSd ● ↓ left ventricular ejection fraction.supplemented diet: ● ↑ heart weight and ↑ left atrial weight ● ↑ lung weight /tibia length ● ↑ BNP levels ● ↑ interstitial and perivascular fibrosis | |
Organ, 2020, USA [40] | C57BL/6 male mice 4 (cardiac pressure overload and HF were induced using transverse aortic constriction TAC surgery) | N= 121 N= 19–35 mice/group | Control diet Diet supplemented with 0.12% TMAO (Subgroup withdrawal of dietary TMAO at 6 weeks after TAC surgery) Diet supplemented with 1% choline Diet containing 1% choline + 0.06% iodomethylcholine (choline TMA lyase inhibitor) | 20 weeks | Nexera ultra-high-performance liquid chromatography system for quantification of plasma TMAO levels | ● ↑ plasma TMAO in mice fed with TMAO supplemented diet; withdrawal of dietary TMAO significantly reduced plasma levels, but they remained elevated compared with control diet ● ↑ circulating TMAO in choline group; TMAO remained at control levels in choline + iodomethylcholine group | In the TMAO group compared with control: ● ↑ adverse cardiac remodeling (↑ LVESD, ↑ LVEDD) (adverse cardiac remodeling was attenuated when TMAO was withdrawn) ● ↑ BNP levels (TAMO withdrawal led to reduced circulating BNP) ↑ heart weight (no significant reduction after TMAO withdrawal) ● no difference in cardiac fibrosis but ↑ levels of profibrotic genes ↑TGFβ, ↓COL1A1, ↓TIMP2 after TMAO withdrawn ● ↑ renal fibrosis (no significant difference after TMAO withdrawal) Choline diet vs. control and choline diet + iodomethylcholine: ● ↑ adverse cardiac remodeling (↓LVFS) ● ↑ BNP levels ● no significant changes in heart weight ●↑ levels of cardiac profibrotic genes (↑TGFβ, ↑ MMPs) ● ↑ renal fibrosis | |
Kain, 2019, United Kingdom [41] | Male C57BL/6J mice 5 | n = 3–8 mice/group Young mice Aging mice | Calorie-dense obesogenic diet (OBD) 10% safflower oil Control diet 4% safflower oil diet | 2 months | 6S variable region 4 rRNA gene DNA sequencing and Quantitative Insights Into Microbial Ecology informatics | ● ↑ Allobaculumin genus in young and aging mice fed with OBD versus control diet ● ↑ Actinobacteria in OBD group, irrespective of age ● OBD in aging mice disrupted the composition of the gut microbiome | ● OBD dysregulation of splenic leukocytes with ↓ immune-responsive F4/80 + and CD169 + macrophages in aging mice | OBD in aging dysregulated splenic leukocytes with the expansion of systemic inflammation and the beginning of the incomplete resolution of inflammation in acute HF |
Chen, 2017, China [42] | Male CD1 mice 2 | N = 40 10 mice/group Mice with DMB Mice without DMB (inhibitor of TMA formation) | Western diet (2% total fat, 12.8% saturated fat, and 30% sucrose) Control diet (17% total fat, 0.8% saturated fat, and 0% sucrose) | 8 weeks | Liquid chromatography coupled with triple-quadrupole mass spectrometry | Compared with mice fed a control diet, in mice fed a WD: ● ↑ TMAO levels in mice fed with WD vs. mice fed with control (p < 0.05) | in WD vs. control diet: ↓ cardiac function ● ↓ LVEF ● ↑ LVICT ● ↑ LVIRT ● ↑ MPI DMB prevented WD-induced changes ● ↑ cardiac fibrosis DMB prevented fibrosis ● ↑ pro-inflammatory cytokines (TNFα; IL 1β) DMB determined increase in anti-inflammatory cytokines | |
Wu, 2021, China [43] | BALB/C male mice 1 | N = 60 2 groups HF rats Control rats | Polyphenols from Arctium lappa L. (ALPP) containing 16 phenolic substances Control (saline solution) ALPP1 (50 mg/kg) ALPP2 (150 mg/kg) | 1 month | Gut microbiome: 16S rRNA amplicon sequencing SCFAs levels: Gas chromatography–mass spectrometry | ● ↓ Shannon, ACE, and Chao1 indices in HF group vs. control group, ALPP2, and ALPP2 + HF ● ↓ number of OTUs, ↓ bacterial richness, ↑ Proteobacteria, ↓ Firmicutes in HF group vs. control group, ALPP2, and ALPP2 + HF ● ↓ number of Roseburia, Lactobacillus, Lachnospsiraceae, Prevotellaceae, Ruminococcaceae, Erysipelotrichaceae, in HF group fed with control diet vs. control ● ↑ number of Bilophila, Enterococcus, Erysipeloclostridium, Escherichia and Shigella, in HF group fed with control diet vs. control ● no significant changes in all microbial flora at the genus level (ratio Bacteroidetes/Firmicutes), Firmicutes, Proteobacteria, and Bacteroidetes in control group vs. ALPP2 control and ALPP2 HF group (remission effect) | ● ↑ SCFA levels in the ALPP2 group vs. control group ● ↓ SCFA levels in the HF group vs. control group ● ↑ SCFA levels in the ALPP2 HF group vs. HF group |
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Palombaro, M.; Raoul, P.; Cintoni, M.; Rinninella, E.; Pulcini, G.; Aspromonte, N.; Ianiro, G.; Gasbarrini, A.; Mele, M.C. Impact of Diet on Gut Microbiota Composition and Microbiota-Associated Functions in Heart Failure: A Systematic Review of In Vivo Animal Studies. Metabolites 2022, 12, 1271. https://doi.org/10.3390/metabo12121271
Palombaro M, Raoul P, Cintoni M, Rinninella E, Pulcini G, Aspromonte N, Ianiro G, Gasbarrini A, Mele MC. Impact of Diet on Gut Microbiota Composition and Microbiota-Associated Functions in Heart Failure: A Systematic Review of In Vivo Animal Studies. Metabolites. 2022; 12(12):1271. https://doi.org/10.3390/metabo12121271
Chicago/Turabian StylePalombaro, Marta, Pauline Raoul, Marco Cintoni, Emanuele Rinninella, Gabriele Pulcini, Nadia Aspromonte, Gianluca Ianiro, Antonio Gasbarrini, and Maria Cristina Mele. 2022. "Impact of Diet on Gut Microbiota Composition and Microbiota-Associated Functions in Heart Failure: A Systematic Review of In Vivo Animal Studies" Metabolites 12, no. 12: 1271. https://doi.org/10.3390/metabo12121271
APA StylePalombaro, M., Raoul, P., Cintoni, M., Rinninella, E., Pulcini, G., Aspromonte, N., Ianiro, G., Gasbarrini, A., & Mele, M. C. (2022). Impact of Diet on Gut Microbiota Composition and Microbiota-Associated Functions in Heart Failure: A Systematic Review of In Vivo Animal Studies. Metabolites, 12(12), 1271. https://doi.org/10.3390/metabo12121271