Relationship between Wine Consumption, Diet and Microbiome Modulation in Alzheimer’s Disease
Abstract
:1. Introduction
2. Lifestyle and Dietary Patterns and Alzheimer’s Disease
2.1. Diet
2.2. Alcohol
2.3. Wine
3. Oral and Gut Microbiota in Alzheimer’s Disease
Study | Design, Aims and Details | Digestive Tract Compartment | Key Findings |
---|---|---|---|
Exploring the association between AD, Oral Health, Microbial Endocrinology and Nutrition [104] | Scientific literature review | Oral | Healthy diet based interventions together with improved life style/behavioral changes may reduce and/or delay the incidence of AD. |
The Microbiome and Disease: Reviewing the Links between the Oral Microbiome, Aging, and Alzheimer’s Disease [31] | Scientific literature review | Oral | Epidemiological and experimental evidence links oral bacteria found in brains and oral bacteria and tumor necrosis factor in blood in AD. Combining human genetic factors with microbiome composition greatly improves the predictive capacity for assessing disease risk. |
The Possible Causal Link of Periodontitis to Neuropsychiatric Disorders: More Than Psychosocial Mechanisms [105] | Scientific literature review | Oral | Periodontal bacteria/bacterial molecules can directly invade the brain either through the blood stream or via cranial nerves. In periodontitis, a periodontal pocket is filled with periodontal bacteria/bacterial molecules that form biofilms. Oral bacteria are capable of invading an intact pocket epithelium, and gain access to the circulation. |
Oral microbiota and AD: Do all roads lead to Rome? [81] | Scientific literature review | Oral | Oral microbiota produces inflammatory mediators able to migrate into the bloodstream and affect distant tissues and organs, thus representing a source of neuro-inflammation. |
Association between chronic periodontitis and the risk of AD: a retrospective, population-based, matched-cohort study [106] | Retrospective matched-cohort study: 9291 patients diagnosed with chronic periodontitis (1997–2004) | Oral | 10-year chronic periodontitis exposure was associated with a 1.707-fold increase in the risk of developing AD. |
Periodontitis and Cognitive Decline in Alzheimer’s Disease [107] | Six month observational cohort study (n = 60 participants with mild to moderate AD). To determine if periodontitis in AD is associated with both increased dementia severity and cognitive decline. | Oral | Periodontitis is associated with an increased systemic pro inflammatory state, and increase in cognitive decline in AD, independent to baseline cognitive state, which may be mediated through effects on systemic inflammation. |
Chronic P. gingivalis infection accelerates the occurrence of age-related granules in APOE−/− mice brains [85] | Age-related granules in the apolipoprotein E gene knockout (APOE−/−) B6 background mice brains following chronic gingival infection with P.gingivalis for 24 weeks. | Oral | Periodontal bacterial infection results in injury of the hippocampus, thereby increasing blood-brain barrier permeability to toxic vascular components. Early appearance of age-related granules in APOE−/− mice following inflammation-mediated tissue injury, accompanied by loss of cerebral blood-brain barrier integrity |
Determining the presence of periodontopathic virulence factors in short-term postmortem Alzheimer’s disease brain tissue [84] | Postmortem study, identifying the major periodontal disease bacteria components in brain tissue from 12 h postmostem delay (n = 10 AD cases for tissue from brains and 10 non-AD-related control with similar or greater postmortem interval). | Oral | LPS from periodontal bacteria can access the AD brain during life as labeling in the corresponding controls, with equivalent/longer postmortem interval. Demonstration of a known chronic oral-pathogen-related virulence factor reaching the human brains suggests and inflammatory role in the existing AD pathology |
Porphyromonas gingivalis in Alzheimer’s disease brains: Evidence for disease causation and treatment with small-molecule inhibitors [32] | Postmortem study, identifying P. gingivalis DNA and gingipains, toxic proteases in AD brains | Oral | Immunohistochemical analyses using tissue microarrays showed that gingipain immunoreactivity in AD brains and that gingipain immunoreactivity significantly correlates with tau and ubiquitin loads and AD diagnosis. Using quantitative Polymerase Chain Reaction, the authors identified P. gingivalis DNA in the AD brains which were lysine gingipain-positive |
Microbiota and Aging. A Review and Commentary [108] | Scientific literature review | Oral and Intestinal | Oral microbiota is especially important because of the opportunities for access to the brain through the olfactory nerve at the roof of the nose or through the abundant innervations of the oral cavity by the trigeminal and other cranial nerves. Communication in the gut-brain-axis is regulated by many intermediaries including diverse metabolites of the microbiota. Microbial changes have been observed in several geriatric diseases, like AD. Individuals with high frailty scores had a significant reduction on lactobacilli species when compared to non-frail individuals suggesting potential mechanisms by which the microbiota promote human health span and aging. |
Secretory products of the human GI tract microbiome and their potential impact on Alzheimer’s disease (AD): detection of lipopolysaccharide (LPS) in AD hippocampus [93] | Scientific literature review | Intestinal | Presence of gastrointestinal tract microbiome-derived lipopolysaccharide (LPS) in brain lysates from the hippocampus and superior temporal lobe neocortex of AD brains. Presence of bacterial LPS hippocampal cases exhibited up to a 26-fold increase in LPS over age-matched controls. |
Gut Microbiota and Their Neuroinflammatory Implications in Alzheimer’s Disease [109] | Scientific literature review | Intestinal | Impact of the microbiota of elderly people and the neuro-inflammatory roles they may have in AD, by different mechanisms: (1) role of the intestinal microbiota in homeostatic communication between the microbiota–gut–brain axis; (2) mechanisms of signal dysfunction; and (3) impact of signal dysfunction induced by the microbiota on AD |
Microbiota modulation counteracts Alzheimer’s disease progression influencing neuronal proteolysis and gut hormones plasma levels [110] | Triple-transgenic mouse model of AD (3xTg-AD) mice in the early stage of AD were treated with a probiotic formulation, thereby affecting the composition of gut microbiota and its metabolites | Intestinal | Treated mice with a probiotic formulation showed partial restoration of two impaired neuronal proteolytic pathways (the ubiquitin proteasome system and autophagy). Their cognitive decline was decreased compared with controls, due to a reduction in brain damage and reduced accumulation of amyloid beta aggregates. Modulation of the microbiota induces positive effects on neuronal pathways that are able to slow down the progression of AD |
Transferring the blues: depression-associated gut microbiota induces neuro-behavioral changes in the rat [89] | Thirty four patients with major depression and thirty three matched healthy controls were evaluated for the study of changes in gut microbiota, including fecal microbiota transplantation from depressed patients to microbiota-depleted rats | Intestinal | Fecal microbiota transplantation from depressed patients to microbiota-depleted rats can induce behavioral and physiological features characteristic of depression in the recipient animals, including anhedonia and anxiety-like behaviors, as well as alterations in tryptophan metabolism. |
Microbiome-metabolome signatures in mice genetically prone to develop dementia, fed a normal or fatty diet [90] | To identify gut microbiota-metabolomics signatures preceding dementia in genetically prone (3xTg-AD) mice | Intestinal | 3xtg mice showed brain hypometabolism typical of pre-demented stage and lacked the physiological bacterial diversity between caecum and colon seen in controls. Cluster analyses revealed distinct profiles of microbiota, and serum and fecal metabolome across groups. Elevation in Firmicutes-to-Bacteroidetes abundance, and exclusive presence of Turicibacteraceae, Christensenellaceae, Anaeroplasmataceae and Ruminococcaceae, and lack of Bifidobacteriaceae, were also observed. Metabolome analysis revealed a deficiency in unsaturated fatty acids and choline, and an overabundance in ketone bodies, lactate, amino acids, trimethylamine and trimethylamine N-oxide in 3xTg-AD mice. These metabolic alterations were correlated with high prevalence of Enterococcaceae, Staphylococcus, Roseburia, Coprobacillus and Dorea, and low prevalence of Bifidobacterium, which, in turn, related to cognitive impairment and cerebral hypometabolism |
Reduction of Alzheimer’s disease Beta-amyloid pathology in the absence of gut microbiota [111] | Preclinical study: conventionally-raised transgenic APPPS1 mice aged 8-months | Intestinal | In the intestine of conventionally-raised transgenic APPPS1 mice aged 8-months, there is a significant reduction in bacteria belonging to the phyla Firmicutes and Actinobacteria with respect to an increase of Bacteroidetes and Tenericutes, supporting evidence of the role of amyloid and related bacterial accumulation in the pathogenesis of cognitive damage. |
Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly [94] | Cognitively impaired patients with (n = 40, Amy+) and with no brain amyloidosis (n = 33, Amy-) and also in a group of controls (n = 10, no brain amyloidosis and no cognitive impairment). Studying the association of brain amyloidosis with gut microbiota taxa with pro- and anti-inflammatory activity | Intestinal | Clinical evidence of gut microbiota bacteria alterations in patients with brain amyloidosis. Abundance of the pro-inflammatory genus Escherichia/Shigella was significantly increased in Amyþ compared with Amy patients. Significant reduction in E. rectale (butyrate producer with key protective roles against inflammation) abundance in Amyþ compared with Amy_ subjects. Cognitive impairment is associated with a reduction in certain anti-inflammatory bacteria belonging to the phyla Firmicutes and Bacteroidetes compared to an increase of other pro-inflammatory bacteria of phylum Proteobacteria. |
Gut microbiota is altered in patients with Alzheimer’s disease [112] | Fecal samples from 43 AD patients and 43 age- and gender-matched cognitively normal controls were evaluated by sequencing techniques to ascertain if the composition of gut microbiota was different between the two groups | Intestinal | Several bacteria taxa in AD patients were different from those in controls at taxonomic levels, such as Bacteroides, Actinobacteria, Ruminococcus, Lachnospiraceae, and Selenomonadales. These findings suggest that gut microbiota is altered in AD patients and may be involved in the pathogenesis of AD. |
Alzheimer’s disease microbiome is associated with dysregulation of the anti-inflammatory P-glycoprotein pathway [96] | Prospective study (n = 108 nursing home elders, 5 months), metagenomic sequencing and in vitro T84 intestinal epithelial cell functional assays | Intestinal | Clinical parameters as well as numerous microbial taxa and functional genes act as predictors of AD dementia in comparison to elders without dementia. Less abundance of butyrate-producing species: Butyrivibrio (B. hungatei and B. proteoclasticus), Eubacterium (E. eigens, E. hallii and E. rectale) and Clostridium sp. SY8519, R.hominis and F.prausnitzzi in AD patients, as well as greater abundance of O. splanchnicus, Odoribacter sp., K. pneumoniae, B. fragilis, and E. lenta and Desulfovibrio genus (D. fairfieldensis). |
4. Microbiome Modulation by Diet/Wine Polyphenols and Alzheimer’s Disease
4.1. Oral Microbiota Modulation by Wine Polyphenols and Alzheimer’s Disease
4.2. Intestinal Microbiota Modulation by Wine Polyphenols and Alzheimer’s Disease
5. Conclusions and Future Directions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
AD | Alzheimer’s disease |
Aβ | Amyloid-β |
BBB | Blood-Brain Barrier |
CI | Confidence Interval |
APOE | Apolipoprotein E |
DASH | Dietary Approaches to Stop Hypertension |
LPS | lipopolysaccharide |
MD | Mediterranean diet |
MIND | Mediterranean–DASH Intervention for Neurodegenerative Delay |
RR | Relative Risk |
SCFA | Short-Chain Fatty Acids |
3xTg-AD | Triple-transgenic mouse model of AD |
WHO | World Health Organization |
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Moreno-Arribas, M.V.; Bartolomé, B.; Peñalvo, J.L.; Pérez-Matute, P.; Motilva, M.J. Relationship between Wine Consumption, Diet and Microbiome Modulation in Alzheimer’s Disease. Nutrients 2020, 12, 3082. https://doi.org/10.3390/nu12103082
Moreno-Arribas MV, Bartolomé B, Peñalvo JL, Pérez-Matute P, Motilva MJ. Relationship between Wine Consumption, Diet and Microbiome Modulation in Alzheimer’s Disease. Nutrients. 2020; 12(10):3082. https://doi.org/10.3390/nu12103082
Chicago/Turabian StyleMoreno-Arribas, M. Victoria, Begoña Bartolomé, José L. Peñalvo, Patricia Pérez-Matute, and Maria José Motilva. 2020. "Relationship between Wine Consumption, Diet and Microbiome Modulation in Alzheimer’s Disease" Nutrients 12, no. 10: 3082. https://doi.org/10.3390/nu12103082