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The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients

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A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Advances in Metabolomics".

Deadline for manuscript submissions: closed (10 February 2023) | Viewed by 34422

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Dr. Karolina Skonieczna-Żydecka

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Department of Biochemical Sciences, Pomeranian Medical University in Szczecin, 24 Broniewskiego Street, 71-460 Szczecin, Poland
Interests: microbiota; gut–brain axis
Special Issues, Collections and Topics in MDPI journals

Dr. Igor Loniewski

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Department of Biochemistry and Human Nutrition, Pomeranian Medical University in Szczecin, Broniewskiego Str. 24, 71-460 Szczecin, Poland
Interests: obesity; Probiotics; metabolic profile

Special Issue Information

Dear Colleagues,

The value of the global probiotics market was around USD 49 billion in 2019 and is projected to reach USD 95 billion by 2027, exhibiting an annual growth rate of 7.9%. However, despite the popularity of this group of products, their mechanism of action is relatively poorly understood, especially in the context of cause-and-effect relationships.

Probiotics are used primarily to replenish the deficiency of microorganisms in the gut, which can cause specific diseases. An example of such an approach is the concept of the prophylactic introduction of probiotics during antibiotic therapy, which damages the intestinal microbiota. In addition, probiotic strains are administered to patients due to their antagonistic properties against pathogenic bacteria or microorganisms that may be responsible for a given disease. Finally, probiotic bacteria are also used to supplement the metabolites that bacterial strains produce. The latter use is of particular interest in studies evaluating the efficacy of the psychobiotic intervention.

Psychobiotics, i.e., probiotics that support mental health, are currently of great interest to researchers, doctors and people with mental disorders or those exposed to stress. Alterations in the secretion of microbiota-derived metabolites have been described in patients with neuropsychiatric diseases. For example, in patients with major depressive disorder (MDD), a lower abundance of bacteria involved in short-chain fatty acids (SCFAs) production has been described. Moreover, microbial alterations that result in increased putrefaction have been implicated in the pathogenesis of autism spectrum disorders. Selected psychobiotic strains affect the activity of the vagus nerve. If administered for a sufficiently long time, they can change the expression of gamma-aminobutyric acid (GABA) receptors, which has been related to the pathogenesis of anxiety-depressive disorders. Moreover, numerous experimental and clinical studies have shown that some probiotics can lower cortisol levels in humans. It follows that they are also indirectly involved in the regulation of the hypothalamic–pituitary–adrenal (HPA) axis.

In this special issue of Metabolites, reviews and original research articles covering the latest developments in studying the effects of probiotics and their metabolites on the central nervous system (CNS), specifically relationships between the microbiota, its metabolites and mental health. We hope that our Special Issue will contribute to deepening the knowledge on the use of probiotics in mental disorders and provide the basis for creating new therapeutic standards.

Dr. Karolina Skonieczna-Żydecka
Dr. Igor Loniewski
Guest Editors

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Keywords

microbiota
metabolome
probiotics
psychobiotics
psychiatric diseases
mental health

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Published Papers (9 papers)

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Research

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14 pages, 940 KiB

Open AccessArticle

Independent and Combined Effects of Probiotics and Prebiotics as Supplements or Food-Rich Diets on a Propionic-Acid-Induced Rodent Model of Autism Spectrum Disorder

by Sana Razhan M. Alsubaiei, Hanan A. Alfawaz, Abdullah Yaseen Almubarak, Nouf Ahmed Alabdali, Abir Ben Bacha and Afaf El-Ansary

Metabolites 2023, 13(1), 50; https://doi.org/10.3390/metabo13010050 - 29 Dec 2022

Cited by 8 | Viewed by 3648

Abstract

The link between nutrition and autism spectrum disorder (ASD) as a neurodevelopmental condition, which is clinically presented as significant delays or deviations in interaction and communication, has provided a fresh point of view and signals that nutrition may play a role in the etiology of ASD, as well as playing an effective role in treatment by improving symptoms. In this study, 36 male albino rat pups were used. They were randomly divided into five groups. The control group was fed only a standard diet and water for the 30 days of the experiment. The second group, which served as a propionic acid (PPA)-induced rodent model of ASD, received orally administered PPA (250 mg/kg body weight (BW)) for 3 days, followed by feeding with a standard diet until the end of the experiment. The three other groups were given PPA (250 mg/kg body weight (BW)) for 3 days and then fed a standard diet and orally administered yogurt (3 mL/kg BW/day), artichokes (400 mL/kg BW/day), and a combination of Lacticaseibacillus rhamnosus GG at 0.2 mL daily (1 × 10⁹ CFU; as the probiotic of yogurt) and luteolin (50 mg/kg BW/day; as the major antioxidant and anti-inflammatory ingredient of artichokes) for 27 days. Biochemical markers, including gamma-aminobutyric acid (GABA), reduced glutathione (GSH), glutathione peroxidase (GPx1), tumor necrosis factor-alpha (TNF-α), interleukin-6 (IL-6), and interleukin-10 (IL-10), were measured in brain homogenates in all groups. The data showed that while PPA demonstrated oxidative stress and neuroinflammation in the treated rats, yogurt, Lacticaseibacillus rhamnosus GG as a probiotic, and luteolin as a prebiotic ingredient in artichokes were effective in alleviating the biochemical features of ASD. In conclusion, nutritional supplementation seems to be a promising intervention strategy for ASD. A combined dietary approach using pro- and prebiotics resulted in significant amelioration of most of the measured variables, suggesting that multiple interventions might be more relevant for the improvement of biochemical autistic features, as well as psychological traits. Prospective controlled trials are needed before recommendations can be made regarding the ideal ASD diet. Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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12 pages, 2961 KiB

Open AccessArticle

Probiotic Ameliorating Effects of Altered GABA/Glutamate Signaling in a Rodent Model of Autism

by Rawan M. Bin-Khattaf, Mona A. Alonazi, Abeer M. Al-Dbass, Ahmad T. Almnaizel, Hisham S. Aloudah, Dina A. Soliman and Afaf K. El-Ansary

Metabolites 2022, 12(8), 720; https://doi.org/10.3390/metabo12080720 - 4 Aug 2022

Cited by 14 | Viewed by 3777

Abstract

Autism spectrum disorders (ASDs) comprise a heterogeneous group of pathological conditions, mainly of genetic origin, characterized by stereotyped behavior, such as marked impairment in verbal and nonverbal communication, social skills, and cognition. Excitatory/inhibitory (E/I) imbalances have been recorded as an etiological mechanism of ASD. Furthermore, GABA, the main inhibitory neurotransmitter in adult life, is known to be much lower in both patients and rodent models of ASD. We propose correcting GABA signaling as a therapeutic strategy for ASD. In this study, 40 young male western Albino rats, 3–4 weeks in age, weighing about 60–70 g, were used. The animals were randomly assigned into six experimental groups, each including eight rats. Group I served as the control group and was orally administered phosphate-buffered saline. Groups II and III served as rodent models of ASD and were orally administered a neurotoxic dose of propionic acid (PPA). The rats in the three therapeutic groups (IV, V, and IV) received the same doses of PPA, followed by 0.2 g/kg body weight of pure Bifidobacterium infantis, a probiotic mixture of ProtexinR, and pure Lactobacillus bulgaricus, respectively, for 3 weeks. Selected variables related to oxidative stress, glutamate excitotoxicity, and gut bacteria were measured in the six groups. Both pure and mixed Lactobacillus and Bifidobacterium were effective in ameliorating glutamate excitotoxicity as an autistic feature developed in the PPA-induced rodent model. Their therapeutic effects mostly involved the correction of oxidative stress, restoration of depleted GABA, and up-regulation of GABA receptor gene expression. Pure Bifidobacterium was the most effective, followed by the mixture of probiotics and finally lactobacillus. In conclusion, Bifidobacteria and lactobacilli can be used independently or in combination as psychobiotics to ameliorate oxidative stress and glutamate excitotoxicity as two confirmed etiological mechanisms through the gut–brain axis. Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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13 pages, 1239 KiB

Open AccessArticle

Vitamin D Status in Children with Autism Spectrum Disorders: Determinants and Effects of the Response to Probiotic Supplementation

by Letizia Guiducci, Cristina Vassalle, Margherita Prosperi, Elisa Santocchi, Maria Aurora Morales, Filippo Muratori and Sara Calderoni

Metabolites 2022, 12(7), 611; https://doi.org/10.3390/metabo12070611 - 1 Jul 2022

Cited by 6 | Viewed by 2910

Abstract

A relationship between the presence of clinical symptoms and gastrointestinal (GI) disturbances associated with nutritional deficiencies, including vitamin D (25(OH)D) deficiency, has been observed in autism spectrum disorder (ASD). The aim was to evaluate 25(OH)D levels according to the annual rhythm cycle, gender, the severity of autism, nutritional or clinical status, inflammatory and metabolic biomarkers, GI symptoms, and the clinical response to probiotic/placebo supplementation in preschooler children with ASD. Eighty-one ASD preschoolers (67 males) were assessed with standardized tools for ASD severity (ADOS score) and GI symptoms (by GI-Index at six-items and at nine-items, the latter defined as the Total GI-Index). The 25(OH)D levels were compared among different ASD subgroups according to metabolic and inflammatory biomarkers (leptin, insulin, resistin, PAI-1, MCP-1, TNF-alfa, and IL-6), gender, and the presence or absence of: (i) GI symptoms, (ii) the response to probiotic supplementation (the improvement of GI symptomatology), (iii) the response to probiotic supplementation (improvement of ASD severity). Only 25% of the ASD children presented an adequate 25(OH)D status (≥30 ng/mL according to the Endocrine Society guidelines). All the 25(OH)D levels falling in the severe deficiency range (<10 ng/mL) were observed in the male subgroup. A significant inverse correlation between 25(OH)D and leptin was observed (R = −0.24, p = 0.037). An inverse correlation was found between 25(OH)D levels and the GI Index 6-Items and Total GI-Index (R = −0.25, p = 0.026; −0.27, = 0.009) and a direct relationship with the probiotic response (R = 0.4, p = 0.05). The monitoring of 25(OH)D levels and the co-administration of 25(OH)D and probiotic supplementation could be considered in ASD from early ages. Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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16 pages, 1100 KiB

Open AccessArticle

Protective Effects of Bee Pollen on Multiple Propionic Acid-Induced Biochemical Autistic Features in a Rat Model

by Hanan A. Alfawaz, Afaf El-Ansary, Laila Al-Ayadhi, Ramesa Shafi Bhat and Wail M. Hassan

Metabolites 2022, 12(7), 571; https://doi.org/10.3390/metabo12070571 - 21 Jun 2022

Cited by 7 | Viewed by 3087

Abstract

Autism spectrum disorders (ASDs) are neurodevelopmental disorders that clinically presented as impaired social interaction, repetitive behaviors, and weakened communication. The use of bee pollen as a supplement rich in amino acids amino acids, vitamins, lipids, and countless bioactive substances may lead to the relief of oxidative stress, neuroinflammation, glutamate excitotoxicity, and impaired neurochemistry as etiological mechanisms autism. Thirty young male Western albino rats were randomly divided as: Group I-control; Group II, in which autism was induced by the oral administration of 250 mg propionic acid/kg body weight/day for three days followed by orally administered saline until the end of experiment and Group III, the bee pollen-treated group, in which the rats were treated with 250 mg/kg body weight of bee pollen for four weeks before autism was induced as described for Group II. Markers related to oxidative stress, apoptosis, inflammation, glutamate excitotoxicity, and neurochemistry were measured in the brain tissue. Our results indicated that while glutathione serotonin, dopamine, gamma-aminobutyric acid (GABA), GABA/Glutamate ratio, and vitamin C were significantly reduced in propionic acid-treated group (p < 0.05), glutamate, IFN-γ, IL-1A, IL-6, caspase-3, and lipid peroxide levels were significantly elevated (p < 0.05). Bee pollen supplementation demonstrates protective potency presented as amelioration of most of the measured variables with significance range between (p < 0.05)–(p < 0.001). Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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14 pages, 1545 KiB

Open AccessArticle

Bee Pollen and Probiotics May Alter Brain Neuropeptide Levels in a Rodent Model of Autism Spectrum Disorders

by Mashael A. Alghamdi, Laila Al-Ayadhi, Wail M. Hassan, Ramesa Shafi Bhat, Mona A. Alonazi and Afaf El-Ansary

Metabolites 2022, 12(6), 562; https://doi.org/10.3390/metabo12060562 - 18 Jun 2022

Cited by 11 | Viewed by 3503

Abstract

Neuropeptides play a major role in maintaining normal brain development in children. Dysfunction of some specific neuropeptides can lead to autism spectrum disorders (ASD) in terms of social interaction and repetitive behavior, but the exact underlying etiological mechanisms are still not clear. In this study, we used an animal model of autism to investigate the role of bee pollen and probiotic in maintaining neuropeptide levels in the brain. We measured the Alpha-melanocyte-stimulating hormone (α-MSH), Beta-endorphin (β-End), neurotensin (NT), and substance P (SP) in brain homogenates of six studied groups of rats. Group I served as control, given only PBS for 30 days; Group II as an autistic model treated with 250 mg PPA/kg BW/day for 3 days after being given PBS for 27 days. Groups III-VI were denoted as intervention groups. G-III was treated with bee pollen (BP) 250 mg/kg body weight/day; G-IV with Lactobacillus paracaseii (LB) (109 CFU/mL) suspended in PBS; G-V with 0.2 g/kg body weight/day Protexin^®, a mixture of probiotics (MPB); and G-VI was transplanted with stool from normal animals (FT) for 27 days prior to the induction of PPA neurotoxicity on the last 3 days of study (days 28–30). The obtained data were analyzed through the use of principal component analysis (PCA), discriminant analysis (DA), hierarchical clustering, and receiver operating characteristic (ROC) curves as excellent statistical tools in the field of biomarkers. The obtained data revealed that brain levels of the four measured neuropeptides were significantly reduced in PPA-treated animals compared to healthy control animals. Moreover, the findings demonstrate the ameliorative effects of bee pollen as a prebiotic and of the pure or mixed probiotics. This study proves the protective effects of pre and probiotics against the neurotoxic effects of PPA presented as impaired levels of α-MSH, β-End, NT, and SP. Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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Review

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15 pages, 690 KiB

Open AccessReview

A Review of the Impact of Maternal Prenatal Stress on Offspring Microbiota and Metabolites

by Venkata Yeramilli, Riadh Cheddadi, Juhi Shah, Kyle Brawner and Colin Martin

Metabolites 2023, 13(4), 535; https://doi.org/10.3390/metabo13040535 - 9 Apr 2023

Cited by 13 | Viewed by 2892

Abstract

Maternal prenatal stress exposure affects the development of offspring. We searched for articles in the PubMed database and reviewed the evidence for how prenatal stress alters the composition of the microbiome, the production of microbial-derived metabolites, and regulates microbiome-induced behavioral changes in the offspring. The gut–brain signaling axis has gained considerable attention in recent years and provides insights into the microbial dysfunction in several metabolic disorders. Here, we reviewed evidence from human studies and animal models to discuss how maternal stress can modulate the offspring microbiome. We will discuss how probiotic supplementation has a profound effect on the stress response, the production of short chain fatty acids (SCFAs), and how psychobiotics are emerging as novel therapeutic targets. Finally, we highlight the potential molecular mechanisms by which the effects of stress are transmitted to the offspring and discuss how the mitigation of early-life stress as a risk factor can improve the birth outcomes. Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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20 pages, 2240 KiB

Open AccessReview

Gut Microbiota Dynamics in Relation to Long-COVID-19 Syndrome: Role of Probiotics to Combat Psychiatric Complications

by Maha F. Alenazy, Haya I. Aljohar, Ashwag R. Alruwaili, Maha H. Daghestani, Mona A. Alonazi, Ranyah S. Labban, Afaf K. El-Ansary and Hanan A. Balto

Metabolites 2022, 12(10), 912; https://doi.org/10.3390/metabo12100912 - 27 Sep 2022

Cited by 24 | Viewed by 5340

Abstract

Increasing numbers of patients who recover from COVID-19 report lasting symptoms, such as fatigue, muscle weakness, dementia, and insomnia, known collectively as post-acute COVID syndrome or long COVID. These lasting symptoms have been examined in different studies and found to influence multiple organs, sometimes resulting in life-threating conditions. In this review, these symptoms are discussed in connection to the COVID-19 and long-COVID-19 immune changes, highlighting oral and psychiatric health, as this work focuses on the gut microbiota’s link to long-COVID-19 manifestations in the liver, heart, kidney, brain, and spleen. A model of this is presented to show the biological and clinical implications of gut microbiota in SARS-CoV-2 infection and how they could possibly affect the therapeutic aspects of the disease. Probiotics can support the body’s systems in fighting viral infections. This review focuses on current knowledge about the use of probiotics as adjuvant therapies for COVID-19 patients that might help to prevent long-COVID-19 complications. Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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Other

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13 pages, 826 KiB

Open AccessPerspective

A New Concept of Associations between Gut Microbiota, Immunity and Central Nervous System for the Innovative Treatment of Neurodegenerative Disorders

by Sayuri Yoshikawa, Kurumi Taniguchi, Haruka Sawamura, Yuka Ikeda, Ai Tsuji and Satoru Matsuda

Metabolites 2022, 12(11), 1052; https://doi.org/10.3390/metabo12111052 - 1 Nov 2022

Cited by 18 | Viewed by 4031

Abstract

Nerve cell death accounts for various neurodegenerative disorders, in which altered immunity to the integrated central nervous system (CNS) might have destructive consequences. This undesirable immune response often affects the progressive neurodegenerative diseases such as Alzheimer’s disease, Parkinson’s disease, schizophrenia and/or amyotrophic lateral sclerosis (ALS). It has been shown that commensal gut microbiota could influence the brain and/or several machineries of immune function. In other words, neurodegenerative disorders may be connected to the gut–brain–immune correlational system. The engrams in the brain could retain the information of a certain inflammation in the body which might be involved in the pathogenesis of neurodegenerative disorders. Tactics involving the use of probiotics and/or fecal microbiota transplantation (FMT) are now evolving as the most promising and/or valuable for the modification of the gut–brain–immune axis. More deliberation of this concept and the roles of gut microbiota would lead to the development of stupendous treatments for the prevention of, and/or therapeutics for, various intractable diseases including several neurodegenerative disorders. Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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13 pages, 617 KiB

Open AccessStudy Protocol

“Leaky Gut” as a Keystone of the Connection between Depression and Obstructive Sleep Apnea Syndrome? A Rationale and Study Design

by Oliwia Gawlik-Kotelnicka, Aleksandra Margulska, Agata Gabryelska, Marcin Sochal, Piotr Białasiewicz and Dominik Strzelecki

Metabolites 2022, 12(2), 152; https://doi.org/10.3390/metabo12020152 - 6 Feb 2022

Cited by 5 | Viewed by 3557

Abstract

Obstructive sleep apnea (OSA) and depression are highly comorbid. Immune alterations, oxidative stress or microbiota dysfunction have been proposed as some mechanisms underlying this association. The aim of the proposed study is to assess the severity and profile of OSA and depressive symptoms in the context of serum microbiota metabolites, biomarkers of intestinal permeability, inflammation and oxidative stress in adult patients diagnosed with OSA syndrome. The study population consists of 200 subjects. An apnoea-hypopnoea index ≥ 5/hour is used for the diagnosis. Depressive symptoms are assessed with Beck Depression Inventory. Measured serum markers are: tumour necrosis factor–alpha and interleukin-6 for inflammation, total antioxidant capacity and malondialdehyde concentration for oxidative stress, zonulin, calprotectin, lipopolisaccharide-binding protein and intestinal fatty acids-binding protein for intestinal permeability. All of the above will be measured by enzyme-linked immunosorbent assay (ELISA). Associations between clinical symptoms profile and severity and the above markers levels will be tested. It would be valuable to seek for overlap indicators of depression and OSA to create this endophenotype possible biomarkers and form new prophylactic or therapeutic methods. The results may be useful to establish a subpopulation of patients sensitive to microbiota therapeutic interventions (probiotics, prebiotics, and microbiota transplantation). Full article

(This article belongs to the Special Issue The Effect of Probiotic Supplementation on Gut Microbiota and Their Metabolic Potential in Psychiatric Patients)

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