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A narrative review of relationship between gut microbiota and neuropsychiatric disorders: mechanisms and clinical application of probiotics and prebiotics.
The gut microbiota is a kind of fixed-value bacteria in the human intestine, characterized by a large quantity, a wide variety and interdependence with each other and with the host. The gut microbiota is considered to be an important link in maintaining health and pathogenic mechanism of many diseases. The gut microbiota affects the central nervous system under the action of the microbe-gut-brain axis through nerve, immune, endocrine and metabolic pathways. The gut microbiota not only regulates the gastrointestinal tract but plays a vital role in the development and function of the brain. More and more studies believe that normal gut microbiota is essential for the development of the central nervous system and emotional regulation. The imbalance of the gut microbiota can affect some neuropsychiatric diseases. Probiotics and prebiotics are active microorganisms beneficial to the human body and can regulate the microecological balance of the human intestinal tract. Current research shows that probiotics and prebiotics have a good preventive effect on Alzheimer's disease, Parkinson's disease, depression, autism spectrum disorders and other neurological and mental diseases. Based on this, we review the relevant research on the pathogenesis of probiotics and prebiotics and neuropsychiatric diseases, in an attempt to providing new ideas for exploring the treatment and prevention of neuropsychiatric diseases.
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Gingerol-Enriched Ginger Extract Effects on Anxiety-like Behavior in a Neuropathic Pain Model via Colonic Microbiome-Neuroimmune Modulation.
Growing evidence has revealed that gut dysbiosis is associated with the development of anxio-depressive disorders through mechanisms that involve neuroimmune signaling, neurotransmitter changes, and neuroplasticity in the brain. This study investigated the effects of gingerol-enriched ginger (GEG) on specifically anxiety-related neuroinflammation-, neuroimmunity-, neuroplasticity-, neurotransmission-, and neurotoxicity-associated genes in different brain regions, as well as on alterations linked to colonic microflora-driven dysbiosis, in the spinal nerve ligation (SNL) rat model of neuropathic pain (NP). Twenty-seven male rats were assigned to 3 groups: sham, SNL, and SNL-treated with GEG at 200 mg/kg body weight (SNL+200GEG) via oral gavage for 5 weeks. Anxiety-like behavior was assessed on the elevated plus maze (EPM). mRNA expression was assessed by qRT-PCR using respective primers. Correlation between behavioral parameters and colonic microbiome composition was analyzed using the Spearman rank correlation. The SNL+200GEG group demonstrated decreased anxiety-like behavior in the SNL model. Compared to the SNL group, the SNL+200GEG group had increased mRNA expression of NRF2 (amygdala: left), LXRα (amygdala: both sides), and CX3CR1 (amygdala: both sides, hippocampus: right). GEG modulated neuroplasticity as shown by increased gene expression of PGK1 (amygdala: right, hippocampus: both sides), MEK1 (frontal cortex: both sides), LDHA (frontal cortex: both sides), GPM6A (frontal cortex: both sides, amygdala: right, hippocampus: right, and hypothalamus), and GLUT1 (amygdala: right) as well by decreased gene expression of HIF1α (in all brain regions except for the hypothalamus). GEG modulated neurotransmission via clearance of excessive glutamate release as suggested by increased gene expression of SLC1A3 (frontal cortex: both sides, hippocampus: right) and via augmenting mGluR5 signaling as shown by increased gene expression of GRM5 (hippocampus: both sides, hypothalamus) as well as downregulation of KMO, HAAO, GRIN2B, and GRIN2C influencing downstream serotonergic neurotransmission and NMDA receptor-mediated glutamatergic pathways in different brain regions. GEG further alleviated neurotoxicity through downregulated gene expression of SIRT1, KMO, IDO1, and HAAO in different brain regions. Moreover, the increased relative abundance of Bilophila spp., accompanied by decreased time spent in the EPM open arms, suggests that increased Bilophila abundance increases anxiety-like behavior. GEG supplementation mitigated anxiety-like behavior in male rats with NP, at least in part, by reducing SNL-induced inflammatory sequelae-related mRNA gene expression in different brain regions. In addition, there is a positive correlation between the abundance of Bilophila wadsworthia and the degree of anxiety-like behavior.
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Critical windows of early-life microbiota disruption on behaviour, neuroimmune function, and neurodevelopment.
Numerous studies have emphasised the importance of the gut microbiota during early life and its role in modulating neurodevelopment and behaviour. Epidemiological studies have shown that early-life antibiotic exposure can increase an individual's risk of developing immune and metabolic diseases. Moreover, preclinical studies have shown that long-term antibiotic-induced microbial disruption in early life can have enduring effects on physiology, brain function and behaviour. However, these studies have not investigated the impact of targeted antibiotic-induced microbiota depletion during critical developmental windows and how this may be related to neurodevelopmental outcomes. Here, we addressed this gap by administering a broad-spectrum oral antibiotic cocktail (ampicillin, gentamicin, vancomycin, and imipenem) to mice during one of three putative critical windows: the postnatal (PN; P2-9), pre-weaning (PreWean; P12-18), or post-weaning (Wean; P21-27) developmental periods and assessed the effects on physiology and behaviour in later life. Our results demonstrate that targeted microbiota disruption during early life has enduring effects into adolescence on the structure and function of the caecal microbiome, especially for antibiotic exposure during the weaning period. Further, we show that microbial disruption in early life selectively alters circulating immune cells and modifies neurophysiology in adolescence, including altered myelin-related gene expression in the prefrontal cortex and altered microglial morphology in the basolateral amygdala. We also observed sex and time-dependent effects of microbiota depletion on anxiety-related behavioural outcomes in adolescence and adulthood. Antibiotic-induced microbial disruption had limited and subtle effects on social behaviour and did not have any significant effects on depressive-like behaviour, short-term working, or recognition memory. Overall, this study highlights the importance of the gut microbiota during critical windows of development and the subtle but long-term effects that microbiota-targeted perturbations can have on brain physiology and behaviour.
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Serum short-chain fatty acids and its correlation with motor and non-motor symptoms in Parkinson's disease patients.
BACKGROUND: Parkinson's disease (PD) is associated with enteric nervous system dysfunction and gut microbiota dysbiosis. Short-chain fatty acids (SCFAs), derived from gut microbiota, are supposed to anticipate PD pathogenesis via the pathway of spinal cord and vagal nerve or the circulatory system. However, the serum concentration of SCFAs in PD patients is poorly known. This study aims to investigate the exact level of SCFAs in PD patients and its correlation with Parkinson's symptoms. METHODS: 50 PD patients and 50 healthy controls were recruited, and their demographic and clinical characteristics were collected. The serum concentration of SCFAs was detected using a gas chromatography-mass spectrometer. SCFAs were compared between PD and control groups. The correlation between serum SCFAs and Parkinson's symptoms and the potential effects of medications on the serum SCFAs was analyzed. RESULTS: Serum propionic acid, butyric acid and caproic acid were lower, while heptanoic acid was higher in PD patients than in control subjects. However, only the serum level of propionic acid was correlated with Unified Parkinson's Disease Rating Scale (UPDRs) part III score (R = -0.365, P = 0.009), Mini-mental State Examination (MMSE) score (R = -0.416, P = 0.003), and Hamilton Depression Scale (HAMD) score (R = 0.306, P = 0.03). There was no correlation between other serum SCFAs and motor complications. The use of trihexyphenidyl or tizanidine increased the serum concentration of propionic acid. CONCLUSIONS: Serum SCFAs are altered in PD patients, and the decrease of serum propionic acid level is correlated with motor symptoms, cognitive ability and non-depressed state. Thus, the gut microbial-derived SCFAs potentially affect Parkinson's symptoms through the blood circulation. Propionic acid supplementation might ameliorate motor and non-motor symptoms of PD patients, although clinical trials are needed to test this hypothesis.
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Early life stress in mice alters gut microbiota independent of maternal microbiota inheritance.
Exposure to early life stress (ELS) is associated with a greater risk of chronic disease development including depression and cardiovascular disease. Altered gut microbiota has been linked to both depression and cardiovascular disease in mice and humans. Rodent models of early life neglect are used to characterize the mechanistic links between early life stress (ELS) and the risk of disease later in life. However, little is understood about ELS exposure and the gut microbiota in the young mice and the influence of the maternal inheritance of the gut microbiota. We used a mouse model of ELS, maternal separation with early weaning (MSEW), and normally reared mice to determine whether the neonate microbiota is altered, and if so, are the differences attributable to changes in dam microbiota that are then transmitted to their offspring. Individual amplicon sequence variants (ASVs) displayed differential abundance in the microbiota of MSEW compared with normally reared pups at postnatal day (PD) 28. Additionally, ELS exposure reduced the alpha diversity and altered microbial community composition at PD28. The composition, levels of alpha diversity, and abundance of individual ASVs in the microbiota of dams were similar from MSEW or normally reared cohorts. Thus, the observed shifts in the abundance of individual bacterial ASVs in the neonates and young pups are likely driven by endogenous effects of MSEW in the offspring host and are not due to inherited differences from the dam. This knowledge suggests that exposure to ELS has a direct effect on microbial factors on the risk of chronic disease development.
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Mind, Mood and Microbiota-Gut-Brain Axis in Psychiatric Disorders.
Psychiatric disorders represent a primary source of disability worldwide, manifesting as disturbances in individuals' cognitive processes, emotional regulation, and behavioral patterns. In the quest to discover novel therapies and expand the boundaries of neuropharmacology, studies from the field have highlighted the gut microbiota's role in modulating these disorders. These alterations may influence the brain's processes through the brain-gut axis, a multifaceted bidirectional system that establishes a connection between the enteric and central nervous systems. Thus, probiotic and prebiotic supplements that are meant to influence overall gut health may play an insightful role in alleviating psychiatric symptoms, such as the cognitive templates of major depressive disorder, anxiety, or schizophrenia. Moreover, the administration of psychotropic drugs has been revealed to induce specific changes in a microbiome's diversity, suggesting their potential utility in combating bacterial infections. This review emphasizes the intricate correlations between psychiatric disorders and the gut microbiota, mentioning the promising approaches in regard to the modulation of probiotic and prebiotic treatments, as well as the antimicrobial effects of psychotropic medication.
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Gut microbiota-derived outer membrane vesicles: under-recognized major players in health and disease?
The role of gut microbiota both in human health and in disease is the subject of intense investigation. The interactions between gut microbiota and the host involve a complex network of metabolic pathways and of biologically active molecules secreted by intestinal bacteria, some of which are packed into nanoparticles known as outer membrane vesicles (OMVs). OMVs can enter the systemic circulation and be delivered to different organs including the brain, eliciting a variety of immunological and metabolic responses. The resulting acute and chronic effects are largely unknown. However, recent studies suggest that OMVs could play a critical role in immune homeostasis and in acute inflammatory reactions. Moreover, the "leaky gut" hypothesis has recently emphasized the role of the brain-gut axis in the pathogenesis of major depressive disorders, pointing to the importance of bacteria and of bacterial products delivered into the circulation in eliciting the low-grade inflammatory response associated with this syndrome. Interestingly, experimental evidence suggests that OMVs can also affect the permeability of the blood-brain barrier. This review also highlights the importance of investigating possible influences of OMVs on the development of the immune system.
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Co-encapsulation of probiotics with functional components: design strategies, synergistic mechanisms, biomedical applications, and challenges for industrialization.
Chronic diseases such as depression, diabetes, inflammatory bowel disease, and colorectal cancer are closely associated with gut microbiota dysbiosis and impaired intestinal barrier function. Probiotic supplementation represents an effective therapeutic approach for modulating gut microecology and alleviating disease symptoms. However, their limited survival rates and colonization efficiency in the gastrointestinal tract compromise their functional efficacy. Co-encapsulation of probiotics with functional components is an effective approach to enhance stability and has gradually become a major focus in current delivery system research. This review summarizes the co-encapsulation strategies of probiotics with functional components, including metabolites, prebiotics, and polyphenols. It also examines the applications of advanced manufacturing technologies such as microfluidics, 3D printing, layer-by-layer encapsulation, and electrospinning/electrospraying in this field. Through functional evaluation methods, including ex vivo gastrointestinal models, in vivo imaging, and metabolic tracking, the advantages of co-encapsulation in improving probiotic survival rates, targeted release capabilities, and functional stability have been demonstrated. Furthermore, this review explores the application potential of co-encapsulation in chronic disease intervention and identifies the challenges that remain in industrial scale-up, safety standardization, and clinical translation. This review aims to provide a scientific foundation for the clinical translation and industrial application of probiotic co-encapsulation technologies.
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Relationships of sleep disturbance, intestinal microbiota, and postoperative pain in breast cancer patients: a prospective observational study.
PURPOSE: Our study was designed to examine the possible relationship between gut microbiota, sleep disturbances, and acute postoperative pain. METHODS: Using 16S rRNA sequencing, we analyzed preoperative fecal samples from women undergoing breast cancer surgery. Preoperative sleep disturbance was evaluated with the Pittsburgh Sleep Quality Index (PSQI) questionnaire. Peak and average pain at rest and movement were evaluated 24 h after surgery, using a numerical rating scale (NRS). Preoperative symptoms of depression and anxiety were assessed with the Patient Health Questionnaire-9 (PHQ-9) and Generalized Anxiety Disorder-7 (GAD-7), respectively. Inflammation was measured using white blood cell and neutrophil counts, together with platelet-lymphocyte ratio, and neutrophil-lymphocyte ratio. RESULTS: Preoperative sleep disturbance was associated with more severe acute postoperative pain. At the phylum level, women with poor sleep quality had higher relative abundance of Firmicutes (p = 0.021) and lower relative abundance of Bacteroidetes (p = 0.013). At the genus level, women with poor sleep quality harbored higher relative abundance of Acidaminococcus and lower relative abundance of several genera. The genus Alloprevotella was negatively associated with peak pain at movement during the first 24 h (r = - 0.592, p < 0.001). The genus Desulfovibrio was negatively associated with symptoms of anxiety (r = - 0.448, p = 0.006). However, partial correlations suggested that the relationship between Alloprevotella and peak pain at movement during the first 24 h was not statistically significant after controlling for sleep (r = - 0.134, p = 0.443). CONCLUSION: These findings suggest that the changed gut microbiota may be involved in sleep-pain interaction and could be applied as a potential preventive method for postoperative pain. TRIAL REGISTRATION: The present clinical study has been registered on Chinese Clinical Trial Registry ( www.chictr.org.cn ); the clinical trial registration number is ChiCTR1900021730; the date of registration is March 7, 2019.
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The Role of the Gut Microbiota in the Metabolism of Polyphenols as Characterized by Gnotobiotic Mice.
A growing body of experimental data suggests that microbes in the gut influence behavior and can alter brain physiology and neurochemistry. Although promising, researchers are only starting to understand the potential of the gut microbiota for use in neurological disease. Recent evidence demonstrated that gastrointestinal activities are linked to mood disorders such as anxiety, depression, and most recently, cognitive functions in age-related neurodegenerative disorders. Studies from our group and others are uncovering new evidence suggesting that the gut microbiota plays a crucial role in the metabolism and bioavailability of certain dietary compounds and synthetic drugs. Based on this evidence, this review article will discuss the implications of the gut microbiota in mechanisms of bioavailability and biotransformation with an emphasis on dietary polyphenol compounds. This will be followed by a survey of ongoing innovative research identifying the ability of individual gut bacteria to enhance the bioavailability of gut-derived, brain-penetrating, bioactive polyphenol metabolites that ultimately influence mechanisms associated with the promotion of resilience against psychological and cognitive impairment in response to stress. Lastly, current research initiatives aimed at promoting the generation of brain bioactive polyphenol metabolites by specialized gut microbes will be discussed, specifically the use of gnotobiotic mice to develop bioengineered second generation probiotics. We propose that leveraging the gut microbial ecosystem to generate brain targeted bioactive metabolites from dietary polyphenols can attenuate lifestyle risk factors and promote resilience against age-related cognitive decline.