Plant-Based Dietary Fibers and Polysaccharides as Modulators of Gut Microbiota in Intestinal and Lung Inflammation: Current State and Challenges
Abstract
:1. Introduction
2. Plant Dietary Fibers and Polysaccharides against Gut and Lung Inflammation
2.1. Different Plant Dietary Fibers and Polysaccharides Shape Gut Microbiota and Affect SCFA Production Differently
2.2. Plant Dietary Fibers and Polysaccharides Alter the Intestinal Barrier in Both Gut Inflammation and Lung Inflammation
2.3. Plant-Dietary-Fiber and Polysaccharide Supplementation in Gut and Lung Inflammation in Human Adults (Clinical Studies) and Adult Mice (Preclinical Studies)
2.4. Plant-Dietary-Fiber and Polysaccharide Supplementation in Maternal Rodent Models
2.5. Sex Differences in Lung Anti-Inflammatory Effect of Plant DFs and Polysaccharides
2.6. Combination of Plant Polysaccharides with Other Phytochemicals
2.7. Mechanisms of Polysaccharides and Dietary Fibers in Reducing Intestinal and Lung Inflammation
3. Issues and Challenges
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Gut Microbiota | Lung Microbiota | ||
---|---|---|---|
IBD | ↓ Bifidobacterium longum, ↓ Eubacterium rectale, ↓ Faecalibacterium prausnitzii, ↓ Roseburia intestinalis, ↑ Bacteroides, ↑ Ruminococcus torques, ↑ Ruminococcus, ↓ Christensenellaceae, ↓ Coriobacteriaceae, ↓ Clostridium leptum, ↑ Actinomyces spp., ↑ Veillonella spp., ↑ Escherichia coli, ↓ Eubacterium rectum, ↓ Akkermansia muciniphila | — | [16] |
COPD | Streptococcus parasanguinis_B and Streptococcus salivarius, Streptococcus vestibularis, Streptococcus sp000187445, Lachnospiraceae | ↓ Veillonella, ↑ Actinomyces, ↑ Actinobacillus, ↑ Megasphaera, ↑ Selenomonas, ↑ Corynebacterium, ↑ Streptococcus pneumoniae, ↑ Gemella morbillorum, ↑ Prevotella histicola, ↑ Streptococcus gordonii | [17,18] |
Asthma | ↑ Haemophilus, ↑ Streptococcus, ↑ Moraxella, ↑ Lactobacillus | ↑ Haemophilus spp., ↑ Moraxella catarrhalis, ↑ Streptococcus spp., Tropheryma | [19] |
Cystic fibrosis | ↑ Escherichia, ↑ Shigella, ↑ Enterobacter, ↑ Clostridium, ↑ Veillonella, ↑ Enterococcus, ↑ Staphylococcus, ↓ Lachnospiraceae, ↓ Ruminococcu, ↓ Roseburia, ↓ Faecalibacterium, ↓ Eubacterium, ↓ Prevotella, ↓ Eggerthella, ↓ Alistipes | Pseudomonas aeruginosa, Staphylococcus aureus, H. influenzae, Burkholderia cepacia, Actinobacteria, Proteobacteria | [19,20] |
Natural Source | Model | Effects on Inflammation Related Biomarkers | Intestinal Microbiota Modulation | References |
---|---|---|---|---|
Buckwheat | TNBS-induced colitis | ↓ IL-6, IL-1β, and TNF-α | ↑ F/B ratio, ↑ Oscillospiraceae, ↑ Oscillibacter, ↑ SCFAs | [21] |
Rosa roxburghii Tratt polysaccharide | HFD-induced colitis | ↓ TNF-α, IL-6 and IL-1β, ↑ tight junction proteins | ↓ Desulfovibrionaceae, ↓ Enterobacteriaceae, ↑ Muribaculaceae, ↑ Bacteroidaceae | [22] |
Rubus chingii Hu unripe fruit polysaccharide | HFD-induced colitis | ↓ IL-6, ↓ IL-1β, ↓ TNF-α | ↑ gut microbial diversity, ↓ Erysipelatoclostridium, ↓ Negativibacillus | [23] |
Cyclocarya paliurus polysaccharide | DSS-induced colitis | ↑ IL-10, ↓ IL-1β, ↓ TNF-α | ↓ Akkermansia, ↓ Sutterella, ↓ AF12, ↓ Clostridiaceae_Clostridium, ↓ Helicobacter, ↓ Prevotella, ↑ Lactobacillus, ↑ Coprococcus | [24] |
Smilax china L. polysaccharide | DSS-induced colitis | ↓ TNF-α, ↓ IL-6, ↓ IL-1β, ↑ IL-10 | ↑ Lachnospiraceae, ↑ Muribaculaceae, ↑ Blautia, ↑ Mucispirillum, ↓ Akkermansiaceae, ↓ Deferribacteraceae, ↓ Oscillibacter | [25] |
Chinese yam polysaccharide | LPS-stimulated co-culture of Caco-2/Raw264.7 cells | ↓ NO, ↓ IL-1β, ↓ TNF-α | ↑ Bifidobacterium, ↑ Megasphaera. | [26] |
Fuzhuan brick tea polysaccharide | DSS-induced colitis | ↓ IL-6, ↓ IL-1β, ↓ IFN-γ, ↓ TNF-α, ↑ tight junction proteins (Occludin, Claudin-1, and ZO-1), ↑ intestinal barrier function | ↑ Bacteroides, ↑ Parasutterella, ↑ Collinsella | [27] |
Fuc-S (a sulfated α-L-Fucooligosaccharide) | DSS-induced colitis | ↓ TNF-α, ↓ IL-1β, ↓ IL-6, ↓ IL-17A | ↓ F/B ratio, ↑ Akkermansia, ↑ Prevotellaceae_UCG_001, ↓ Eubacterium xylanophilum, ↓ Intestinimonas, ↓ Ruminococcaceae UCG-014, ↓ Oscillibacter | [28] |
Polysaccharide conjugates derived from dried fresh tea leaves, green tea, and black tea | DSS-induced colitis | ↓ IL-6, ↓ IFN-γ, ↓ IL-1β, ↓ TNF-α, ↑ IL-10 | ↑ Bacteroides, ↑ Muribaculaceae, ↓ Helicobacter, ↓ Enterococcus | [29] |
Pectin with various esterification degrees | DSS-induced colitis | — | ↑ Lactobacillus, ↑ Bifidobacterium | [30] |
Rosa roxburghii Tratt | HFD-induced intestinal barrier dysfunction and inflammation | ↓ TNF-α, ↓IL-6, ↓IL-1β; ↑ tight junction proteins (ZO-1, claudin-1, and occludin); ↓ intestinal permeability; ↓ colonic oxidative stress | ↓ F/B ratio, ↑ Ruminococcaceae, ↑ Muribaculaceae, ↑ Akkermansiaceae | [22] |
Dendrobium fimbriatum Hook | DSS-induced colitis | ↓ IL-1β, ↓ IL-6, ↓ IL-17A, ↓ IL-17F, ↓ IL-21, ↓ IL-23, ↑ IL-5, ↑ IL-10, ↑ IL-22, ↑ IFN-γ, ↑ TNF-α, ↑ TGFβ | ↑ Romboutsia, ↑ Lactobacillus, ↑ Odoribacter, ↓ Parasutterella, ↓ Burkholderia-Caballeronia-Paraburkholderia, ↓ Acinetobacter | [31] |
Pectin | LPS-induced inflammation in piglets | ↓ TNF-α, ↑ IL-10 | ↓ Helicobacter, ↑ Olsenella, ↑ Bacteroides, ↑ Proteus, ↑ Eubacterium | [32] |
Rehmannia glutinosa polysaccharide | DSS-induced colitis | ↑tight junction proteins, ↓ IL-10, ↓ IL-6, ↓ TNF-α, ↑ IL-10 | ↓ Bacteroidaceae, ↑ Lactobacillus, ↑ Alistipes, ↑ Lachnospiraceae_NK4A13 | [33] |
Polygonatum sibiricum polysaccharide | Aged mouse model | ↓ IL-23, ↓ IL-6, ↓ IL-1β, ↓ TNFα, ↓ IL-17, ↓ IL-12, ↓ IL-6, ↑ IL4, ↑ IL-10 | ↑ Bifidobacterium, ↑ Lactobacillus, ↓ Escherichia coli | [34] |
Rhinacanthus nasutus and okra | AA-induced colitis | ↓ IL1β, ↓ IL-2, ↓ IL-6, ↑ IL-10 | ↑ Muribaculaceae, ↓ Bacteroidaceae, ↓ Tannerellaceae | [35] |
Houttuynia cordata polysaccharides | DSS-induced colitis | ↓ TNF-α, ↓ IL-1β, ↓ IL-6 | ↑ Firmicutes, ↑ Bacteroides, ↓ Proteobacteria | [36] |
Lonicera japonica Thunb | DSS-induced colitis | ↑ IL-2, ↑ TNF-α, ↑ IFN-γ | ↑ Bifidobacterium, ↑ Lactobacilli, ↓ Escherichia coli, ↓ Enterococcus | [37] |
Crataegus pinnatifida | DSS-induced colitis | ↓ IL-1β, ↓ IL-6, ↓ TNF-α | ↑ Alistipes, ↑ Odoribacter | [38] |
Morinda citrifolia L. | DSS-induced colitis | ↓ TNF-α, ↓ IL-17 | ↑ Dubosiella, ↑ Muribaculaceae, ↑ Ruminococcaceae_UGG-014, ↑ Ruminococcus_1, ↓ Bilophila, ↓ Campylobacter, ↓ Escherichia-Shigella, ↓ Ochrobactrum, ↓ Vibrio | [39] |
Scutellaria baicalensis Georgi. | DSS-induced colitis | ↓IL-6, ↓IL-1β, ↓TNF-α | ↑ Bifidobacterium, ↑ Firmicutes, ↑ Lactobacillus, ↑ Roseburia | [40] |
Polysaccharide Intervention | Disease | Anti-Inflammatory Outcomes in Lungs | Effects on Intestinal Microflora | Reference |
---|---|---|---|---|
Pear extract | Preclinical asthma mouse model and randomized, double-blind clinical studies | ↓ pro-inflammatory cytokines, including IgE, IL-4, IL-5, and IL-13 | ↑ Bifidobacterium and Eubacterium | [41] |
Inulin (10%) | OVA- and Al (OH)3-induced asthma in SD rats | Attenuation of the asthmatic inflammatory response in the offspring | ↑ SCFA-producing bacteria (mainly Bifidobacterium) in maternal intestinal microflora; alteration in intestinal microflora composition of offspring | [42] |
Astragalus membranaceus polysaccharide (25, 50, and 100 mg/kg) | Bleomycin-induced pulmonary fibrosis | ↓ damage and collagen deposition in lung tissue; ↓ inflammatory cytokines TNF-α, IL-6, and IL-1β levels; ↓ apoptosis | Restoration of gut microbiota homeostasis; ↑ Lactobacillus and Akkermansia; ↓ Lachnoclostridium, Clostridium, and Erysipelatoclostridium | [43] |
Houttuynia cordata polysaccharides (80 mg/kg) and flavonoids (100 mg/kg) either alone or in combination | Influenza virus H1N1-infected mice | Combined therapy showed more potent effect than monotherapy; inhibition of inflammatory-cell infiltration and production of chemokines or pro-inflammatory cytokines such as MCP-1, IL-8, TNF-α, IL-6, and IL-1 β; | Restoration of microflora composition, ↑ Bacteroidetes-to-Firmicutes (B/F) ratio | [44] |
Cellulose-rich diet (30%) | OVA- and Al(OH)3-induced asthma in C57BL/6J mice | ↓ inflammatory cell infiltration around the bronchus and blood vessels; normalization of airway epithelial structure; ↓IL-4; ↓IgE | ↑Peptostreptococcaceae | [45] |
Houttuynia cordata polysaccharides (40 mg/kg) | H1N1-induced pneumonia in antibiotic-treated BALB/c mice (termed BALB/c-ABX mice) | Significant amelioration of inflammation in lungs of BALB/c mice | Attenuation of pathological change in intestine; ↓ Bacteroidetes at phylum level; ↓ Bacteroides and ↑ f_Lachnoospiraceae at genus level, ↑ gut microbial diversity; ↑ acetate | [46] |
Astragalus polysaccharides | Lipopolysaccharide-induced inflammatory lung injury | Alleviation of histopathological abnormalities in lung tissues; ↓ neutrophils infiltration; inhibition of LPS-induced lung inflammation | Change in colonic microbiota composition; ↑ short-chain fatty acid (SCFA)-producing genera such as Oscillospira, Akkermansia, and Coprococcus | [47] |
Platycodon grandiflorus polysaccharide (75, 150, and 300 mg/kg) and platycodin D alone and together | Chronic bronchitis in SD rats induced via smoking | Improvement in histopathological abnormalities; ↓ excess mucus secretion; improved immunological imbalance in lungs of CB model rat | — | [48] |
Ephedra sinica polysaccharide | PM- and OVA-induced asthma in mice | ↓ eosinophils in BALF; ↓ serum Ig-E, IL-6, TNF-α, and IL-1β; ↓ airway inflammation | ↑ Bacteroides, Lactobacillus, Prevotella, Butyricicoccus, and Paraprevotella; ↓ Enterococcus and Ruminococcus; ↑ acetic acid, propionic acid, butyric acid, isobutyric acid, valeric acid, isovaleric acid, and isohexanic acid | [49] |
Polysaccharides from Tetrastigma hemsleyanum Diels et Gilg | LPS-induced ARDS in Balb/c mice | ↓ IL-6, ↓ TNF-α, inhibition of pulmonary inflammation via TLR2/TLR4 pathway | — | [50] |
Polysaccharide-rich ethanol precipitate fraction of black tea | Particulate matter (PM)-induced lung injury in BALB/c mice | ↓ oxidative stress and inflammation in the lungs; ↓ IL-6, CXCL1, CXCL15, and MDA | ↑ Lachnospiraceae, ↓ Lactobacillaceae | [51] |
High-cellulose (20%) or high-pectin diet (20) | Cigarette-smoke (CS)-exposed C57BL/6 mouse emphysema model | ↓ Alveolar destruction and inflammation in BALF; ↓ macrophages and neutrophils in BALF; ↓ mRNA expression of IFN-γ, IL-1β, IL-6, IL-8, IL-18, TNF-α, TGF-β | ↑ SCFAs, bile acids, sphingolipids; ↑ Bacteroidetes; ↓ Lactobacillaceae; ↓ Defluviitaleaceae; ↓ Oscillospiraceae | [52] |
Cellulose- or pectin-enriched diet | Ozone-induced airway hyperresponsiveness in C57BL/6 mice | ↓ ozone-induced AHR, neutrophilic airway inflammation, and airway injury in female but not male mice; cellulose-based diets ameliorated ozone-induced airway hyperresponsiveness in male but not female mice | ↓ Firmicutes, ↑ Proteobacteria and Verrucomicrobia in pectin-fed mice; ↑ Proteus and Lactobacillus, and ↓ Parabacteroides, Clostridiales, and Lachnospiraceae in pectin- versus cellulose-fed mice | [53] |
Houttuynia cordata polysaccharides | H1N1-induced acute lung injury in C57BL/6 mice | Restoration of Th17/Treg cells balance in the lung, ↓ CCL20 expression | Restoration of Th17/Treg-cell balance of gut mucosa-associated lymphoid tissue (GALT) | [54] |
Lycium barbarum polysaccharide | Asthma (OVA-induced mouse model) | ↓ lung injury; ↓ TNF, IL-4, IL-6, MCP-1, and IL-17A in plasma and BALF | ↑ Lactobacillus and Bifidobacterium; ↓ Firmicutes, Actinobacteria, Alistipes, and Clostridiales | [55] |
Soluble fiber (inulin 12 g/day), soluble fiber + probiotic (inulin 12 g/day + multi-strain probiotic >25 billion CFU) | Randomized, double-blind, three-way cross-over trial involving asthmatic patients | No differences between groups in asthma control or airway inflammation | No differences between groups in SCFA levels | [56] |
Houttuynia cordata polysaccharide (40 mg/kg/day) | H1N1 virus-infected mice | ↓ lung inflammation via inhibition of TLR signaling pathway, and IL-1β production and promotion of IL-10 production | ↓ intestinal barrier damage; ↑ ZO-1 expression; ↓ relative abundance of pathogenic bacterial genera Vibrio and Bacillus | [57] |
Houttuynia cordata polysaccharide (20 mg/kg; 40 mg/kg) | Influenza A virus (IAV) H1N1-mediated pneumonia in BALB/c mice | Amelioration of pulmonary injury; inhibition of TNF-α, IL-6, IFN-α, RANTES, MCP-1, MIP-1α; and IP-10 production | ↓ intestinal goblet cells; ↑ intestinal physical and immune barrier; ↑ tight junction protein (ZO-1) in intestine | [58] |
Pectin (30%) | Asthma (ozone-exposed mice) | ↓ ozone-induced airway hyperresponsiveness | ↑ serum short-chain fatty acids | [59] |
GOS (1 or 2.5 w/w%) alone or with budesonide | HDM-induced asthma in BALB/c mice | Budesonide or GOS: ↓ eosinophils in BALF GOS + budesonide: ↓ CCL17, CCL22, and IL-33 protein levels; ↓ allergic inflammatory response | — | [60] |
Soluble-fiber meal containing probiotic yoghurt; inulin (3.5 g); and the probiotics Lactobacillus acidophilus, Bifidobacterium lactis, and Lactobacillus rhamnosus | Human subjects with stable asthma | Airway inflammation biomarkers, including sputum total cell count, neutrophils, macrophages, lymphocytes, sputum IL-8, and eNO, significantly decreased; no decrease in airway eosinophils | — | [61] |
Soluble pectin/insoluble cellulose (4%) | Asthma (female BALB/c mice; OVA induction) | ↓ eosinophil inflammation, ↓ frequency of allergic symptoms, ↓ BALF and NALF total cells and eosinophils, ↓ IL-4 in BALF, ↑ IFN-γ and IL-10 in BALF | ↑ Bifidobacteria | [62] |
Houttuynia cordata Thunb. polysaccharides (40, 80, and 160 mg/kg) | Lipopolysaccharide-induced acute lung injury in Balb/c mice | ↓ pro-inflammatory cytokine (TNF-α, interleukin-6, and interleukin-1β) production | — | [63] |
Citrus pectin-derived acidic oligosaccharides (5%) | Pseudomonas aeruginosa lung infection in BALB/c mice | ↑ M1 macrophage activation, ↑ IL-10 release, ↓ TNF-α release | ↑ Escherichia coli, Allobaculum species, Sutturella wadsworthia, Bacteroides vulgatus, Bifidobacterium species, Clostridium difficile, Clostridium ramosum, Clostridium sphenoides; ↑ production of butyrate and propionate | [64] |
GOS (1%) | HDM-induced asthma in BALB/c mice | ↓ AHR development, ↓ BALF eosinophils, ↓ BALF leukocytes, ↓ CCL5 and IL-13 | — | [65] |
scGOS/lcFOS (in 9:1 ratio) | OVA-induced asthma in female BALB/c and male C57BL/6 | ↓ OVA-induced AHR; no significant change in the concentrations of IFN-γ, IL-4, IL-5, IL-10, IL-12(p70), IL-13, IL-17, and TNF-α in BAL fluid and plasma | — | [66] |
High-fiber diet | HDM-induced asthma in female C57BL/6 and BALB/C mice | ↓ total BALF leukocytes, eosinophils, macrophages, and lymphocytes; ↓ IL-4, -5, -13, −10, and IFN-γ; ↓ airway hyperresponsiveness | ↑ Bacteroidetes; ↓ Firmicutes | [67] |
Apple pectin (30%) | HDM-induced asthma in BALB/c mice | ↓ allergic airway inflammation | Changes in intestinal and lung microbiota; increment in SCFAs; ↑ Bacterioidetes; ↑ Bifidobacteriaceae; ↓ Firmicutes | [68] |
Chitosan oligosaccharides | OVA-induced asthma in mice | ↓ mRNA and protein levels of IL-4, IL-5, IL-13, TNF-α in lung tissue and BALF | — | [69] |
FOS (2.5%) | HDM-induced airway inflammation in male C3H/HeN mice | ↓ BALF eosinophils, ↓ IL-5 | — | [70] |
1% w/w of 9:1 scGOS: lcFOS; 1% w/w of 83% scGOS/lcFOS + 17% pAOS | OVA-induced asthma in male BALB/c mice | ↓ OVA-induced airway inflammation and hyperresponsiveness, ↓ BALF inflammatory cells | — | [71] |
Raffinose (50 g/kg) and GOS (50 g/kg) | Allergic airway eosinophilia (OVA-sensitized brown Norway rats) | ↓ IL-4, ↓ IL-5 | ↑ total anaerobic bacteria in the colon | [72] |
Asian pear pectin (100 µg) | Asthma (OVA-sensitized murine model) | ↓ asthmatic reactions in sensitized mice, ↓ IFN-γ, ↓ IL-5 | — | [73] |
Raffinose (50 g/kg) | Allergic airway eosinophilia (OVA-sensitized brown Norway rats) | ↓ IL-4 and IL-5 mRNA expression, ↓ mucus-producing cells, = IFN-γ mRNA expression | ↑ bifidobacteria | [74] |
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Shen, Y.; Song, M.; Wu, S.; Zhao, H.; Zhang, Y. Plant-Based Dietary Fibers and Polysaccharides as Modulators of Gut Microbiota in Intestinal and Lung Inflammation: Current State and Challenges. Nutrients 2023, 15, 3321. https://doi.org/10.3390/nu15153321
Shen Y, Song M, Wu S, Zhao H, Zhang Y. Plant-Based Dietary Fibers and Polysaccharides as Modulators of Gut Microbiota in Intestinal and Lung Inflammation: Current State and Challenges. Nutrients. 2023; 15(15):3321. https://doi.org/10.3390/nu15153321
Chicago/Turabian StyleShen, Yu, Mingming Song, Shihao Wu, Hongbo Zhao, and Yu Zhang. 2023. "Plant-Based Dietary Fibers and Polysaccharides as Modulators of Gut Microbiota in Intestinal and Lung Inflammation: Current State and Challenges" Nutrients 15, no. 15: 3321. https://doi.org/10.3390/nu15153321