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Soliz-Rueda JR, Cuesta-Marti C, O'Mahony SM, Clarke G, Schellekens H, Muguerza B. Gut microbiota and eating behaviour in circadian syndrome. Trends Endocrinol Metab 2025; 36:15-28. [PMID: 39095231 DOI: 10.1016/j.tem.2024.07.008] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/20/2024] [Revised: 07/04/2024] [Accepted: 07/12/2024] [Indexed: 08/04/2024]
Abstract
Eating behaviour and circadian rhythms are closely related. The type, timing, and quantity of food consumed, and host circadian rhythms, directly influence the intestinal microbiota, which in turn impacts host circadian rhythms and regulates food intake beyond homeostatic eating. This Opinion discusses the impact of food intake and circadian disruptions induced by an obesogenic environment on gut-brain axis signalling. We also explore potential mechanisms underlying the effects of altered gut microbiota on food intake behaviour and circadian rhythmicity. Understanding the crosstalk between gut microbiota, circadian rhythms, and unhealthy eating behaviour is crucial to addressing the obesity epidemic, which remains one of the biggest societal challenges of our time.
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Affiliation(s)
- Jorge R Soliz-Rueda
- Nutrigenomics Research Group, Department of Biochemistry and Biotechnology, Universitat Rovira I Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain; Center of Environmental, Food and Toxicological Technology (TecnATox), Tarragona, Spain
| | - Cristina Cuesta-Marti
- Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland; APC Microbiome Ireland, Cork, Ireland
| | - Siobhain M O'Mahony
- Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland; APC Microbiome Ireland, Cork, Ireland
| | - Gerard Clarke
- APC Microbiome Ireland, Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, Cork, Ireland
| | - Harriët Schellekens
- Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland; APC Microbiome Ireland, Cork, Ireland.
| | - Begoña Muguerza
- Nutrigenomics Research Group, Department of Biochemistry and Biotechnology, Universitat Rovira I Virgili, Reus, Spain; Institut d'Investigació Sanitària Pere Virgili (IISPV), Reus, Spain; Center of Environmental, Food and Toxicological Technology (TecnATox), Tarragona, Spain
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Caprara GL, von Ameln Lovison O, Martins AF, Bernardi JR, Goldani MZ. Characterization of newborn gut microbiota according to the pre-gestational maternal nutritional status and delivery mode. Arch Gynecol Obstet 2024; 310:2889-2898. [PMID: 39387928 DOI: 10.1007/s00404-024-07772-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/17/2023] [Accepted: 10/05/2024] [Indexed: 10/15/2024]
Abstract
PURPOSE The aim of this study is to characterize the composition of the newborn gut microbiota based on the maternal pre-pregnancy nutritional status and the delivery mode. METHODS A biological sample was collected from the anal mucosa of the newborns between 24 and 48 h after delivery, as it was not possible to collect a meconium sample at that time. A general data collection questionnaire was administered. The microbiome of the samples was analyzed by next-generation sequencing of the hypervariable regions v3-v4 of the 16S gene. Alpha diversity analyses were performed using the Observed Richness and Shannon diversity index metrics and Beta diversity analyses were conducted using Nonmetric multidimensional scaling with Weighted Unifrac, Differential abundance analysis was performed using a Negative Binomial Wald Test with maximum likelihood estimation for coefficients of Generalized Linear Models. RESULTS Newborns of obese mothers exhibited lower alpha diversity compared to newborns of mothers with adequate BMI (body mass index). We observed variation in the composition of the microbial community in newborn stool samples, both from mothers with overweight/obesity and those with adequate pre-pregnancy BMI. We observed a visible correlation between the mode of delivery and the newborn's microbiota. We found variation in the overall composition of the microbial community in the stools of newborns, regardless of the delivery mode. CONCLUSIONS The results of our study demonstrate differences in the microbiota of neonates born via cesarean section compared to those born vaginally as well as differences in newborns of mothers with overweight/obesity compared to those with an adequate pre-pregnancy BMI.
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Affiliation(s)
- Gabriele Luiza Caprara
- Programa de Pós-Graduação Em Saúde da Criança E Do Adolescente, Faculdade de Medicina, Universidade Federal Do Rio Grande Do Sul, Porto Alegre, RS, Brazil.
| | - Otávio von Ameln Lovison
- Laboratório de Pesquisa Em Resistência Bacteriana (LABRESIS), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Núcleo de Bioinformática (Bioinformatics Core), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Programa de Pós-Graduação Em Ciências Farmacêuticas, Universidade Federal Do Rio Grande Do Sul, Porto Alegre, RS, Brazil
| | - Andreza Francisco Martins
- Laboratório de Pesquisa Em Resistência Bacteriana (LABRESIS), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Núcleo de Bioinformática (Bioinformatics Core), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Programa de Pós-Graduação Em Ciências Farmacêuticas, Universidade Federal Do Rio Grande Do Sul, Porto Alegre, RS, Brazil
| | - Juliana Rombaldi Bernardi
- Programa de Pós-Graduação Em Saúde da Criança E Do Adolescente, Faculdade de Medicina, Universidade Federal Do Rio Grande Do Sul, Porto Alegre, RS, Brazil
- Programa de Pós-Graduação Em Alimentação, Nutrição E Saúde, Universidade Federal Do Rio Grande Do Sul, Porto Alegre, RS, Brazil
| | - Marcelo Zubaran Goldani
- Programa de Pós-Graduação Em Saúde da Criança E Do Adolescente, Faculdade de Medicina, Universidade Federal Do Rio Grande Do Sul, Porto Alegre, RS, Brazil
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Almahmoud E, Alkazemi DUZ, Al-Qabandi W. Growth Stunting and Nutritional Deficiencies among Children and Adolescents with Celiac Disease in Kuwait: A Case-Control Study. CHILDREN (BASEL, SWITZERLAND) 2024; 11:1042. [PMID: 39334575 PMCID: PMC11429790 DOI: 10.3390/children11091042] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/27/2024] [Revised: 08/14/2024] [Accepted: 08/26/2024] [Indexed: 09/30/2024]
Abstract
BACKGROUND/OBJECTIVES This study aimed to assess the nutritional status of children and adolescents with celiac disease (CD) in Kuwait and investigate the nutritional deficiencies and sociodemographic factors associated with growth stunting in this population. METHODS This case-control study included 77 CD patients aged 3-18 years diagnosed with CD using IgA anti-tissue transglutaminase and duodenal biopsy and 33 healthy controls. Nutritional status was evaluated based on demographic and clinical characteristics, anthropometric measurements, and biochemical parameters. Univariate and multivariate logistic regression models were used to determine the association between CD and growth stunting. RESULTS Approximately one-third (31%) of children with CD had stunted growth, 20.8% had a low body mass index for their age, and 5.2% had both growth stunting and wasting. Children with CD had higher odds of iron-deficiency anemia, vitamin D deficiency, anemia, and lower socioeconomic status. They were also younger and had decreased serum levels of vitamin D compared to the controls. These factors were all significantly associated with an increased risk of CD, collectively explaining over 50% of the risk. For growth stunting, lower education status among mothers, family income, and serum ferritin were identified as risk factors. CONCLUSIONS A significant proportion of children and adolescents with CD had malnutrition, overt deficiencies, and impaired growth despite coherence with a gluten-free diet. RECOMMENDATION Routine monitoring and targeted nutritional interventions are recommended for children and adolescents with CD to address malnutrition and growth stunting. Addressing socioeconomic disparities and enhancing maternal education may also help mitigate the risk factors.
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Affiliation(s)
- Esraa Almahmoud
- Department of Food Science and Nutrition, College of Life Sciences, Kuwait University, P.O. Box 17438, Al-Shadadiya 72455, Kuwait
| | - Dalal Usamah Zaid Alkazemi
- Department of Food Science and Nutrition, College of Life Sciences, Kuwait University, P.O. Box 17438, Al-Shadadiya 72455, Kuwait
| | - Wafaa Al-Qabandi
- Department of Pediatrics, Faculty of Medicine, Kuwait University, P.O. Box 24923, Jabriya 90805, Kuwait
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Caprara GL, von Ameln Lovison O, Martins AF, Bernardi JR, Goldani MZ. Gut microbiota transfer evidence from mother to newborn. Eur J Pediatr 2024; 183:749-757. [PMID: 37987847 DOI: 10.1007/s00431-023-05341-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/16/2023] [Revised: 11/10/2023] [Accepted: 11/16/2023] [Indexed: 11/22/2023]
Abstract
Early life microbiota is a risk factor for future diseases. The main purpose of this study was to investigate the transfer of gut microbiota from mother to newborn. A biological sample was collected from the anal mucosa of the pregnant women before delivery and from the newborns between 24 and 48 h after delivery, as it was not possible to collect a meconium sample at that time. The microbiome of the samples was analyzed by sequencing the hypervariable regions V3-V4 of the 16S gene. To determine the likelihood of microbiota transfer from mother to newborn and examine the relationship with the mode of delivery, we utilized Fisher's exact test and odds ratio. A weighted transfer ratio was employed as a comprehensive measure of transfer. A total of 5767 ASVs were identified in newborn samples (n = 30) and 7253 in maternal samples (n = 30). In the analysis of transfer correlated with the mode of delivery, we observed significant ASVs (p < 0.05). Vaginal delivery showed a positive probability of transfer (OR = 2.184 and WTR = 1.852). We found a negative correlation (OR < 1) between the abundance of maternal ASVs and the likelihood of microbiota transfer to the newborn in both delivery modes. The relationship was inversely proportional for both cesarean section (log10 = - 0.2229) and vaginal delivery (log10 = - 0.1083), with statistical significance observed only for cesarean section (p = 0.0083). Conclusion: In our sample, the maternal gut microbiome was found to be associated with the infant gut microbiome, indicating evidence of ASV-specific transfer from the maternal microbiome to newborns. What is Known: • There is a relationship of early-life microbiota composition with future health outcomes. What is New: • This was the first study to evaluate maternal gut microbiota transfer to newborns in Brazil.
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Affiliation(s)
- Gabriele Luiza Caprara
- Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil.
| | - Otávio von Ameln Lovison
- Laboratório de Pesquisa em Resistência Bacteriana (LABRESIS), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Núcleo de Bioinformática (Bioinformatics Core), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
| | - Andreza Francisco Martins
- Laboratório de Pesquisa em Resistência Bacteriana (LABRESIS), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Núcleo de Bioinformática (Bioinformatics Core), Hospital de Clínicas de Porto Alegre, Porto Alegre, RS, Brazil
- Programa de Pós-Graduação em Ciências Farmacêuticas, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
| | - Juliana Rombaldi Bernardi
- Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
| | - Marcelo Zubaran Goldani
- Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
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Kang T, Ree J, Park JW, Choe H, Park YI. Anti-Obesity Effects of SPY Fermented with Lactobacillus rhamnosus BST-L.601 via Suppression of Adipogenesis and Lipogenesis in High-Fat Diet-Induced Obese Mice. Foods 2023; 12:foods12112202. [PMID: 37297447 DOI: 10.3390/foods12112202] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/17/2023] [Revised: 05/19/2023] [Accepted: 05/27/2023] [Indexed: 06/12/2023] Open
Abstract
In this research, the potential anti-obesity efficacy of Lactobacillus rhamnosus BST-L.601 and its fermented product (named SPY) with mashed sweet potato paste were investigated using 3T3-L1 preadipocytes and high-fat diet (HD)-induced obese mice. SPY (0-0.5 mg/mL) dose-dependently and significantly reduced lipid accumulation and TG content and the expression of adipogenic markers (C/EBPα, PPAR-γ, and aP2) and fatty acid synthetic pathway proteins (ACC and FAS) in 3T3-L1 adipocytes, demonstrating that SPY suppresses adipocyte differentiation and lipogenesis. Oral administration of SPY (4 × 107 CFU/kg body weight) to HD-induced obese mice for 12 weeks significantly reduced the body and liver weight, the size of adipocytes, and the weight of epididymal, visceral, and subcutaneous fat tissues. SPY was more effective in decreasing body weight gain in HD mice than in treatment with BST-L.601 alone. Administration of SPY or BST-L.601 also reduced the serum level of total cholesterol and LDL cholesterol and leptin secretion at a similar level. These results revealed that both SPY and BST-L.601 effectively suppress HD-induced adipogenesis and lipogenesis, suggesting that these materials would be useful in the functional foods industry to ameliorate and/or prevent obesity.
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Affiliation(s)
- Taewook Kang
- Department of Biotechnology, Graduate School, The Catholic University of Korea, Bucheon 14662, Republic of Korea
- Biostream Co., Ltd., Suwon 10442, Republic of Korea
| | - Jin Ree
- Department of Biotechnology, Graduate School, The Catholic University of Korea, Bucheon 14662, Republic of Korea
- Biostream Co., Ltd., Suwon 10442, Republic of Korea
| | | | - Hyewon Choe
- Biostream Co., Ltd., Suwon 10442, Republic of Korea
- Graduate School of Genetics and Biotechnology, Kyung Hee University, Yongin 17104, Republic of Korea
| | - Yong Il Park
- Department of Biotechnology, Graduate School, The Catholic University of Korea, Bucheon 14662, Republic of Korea
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Oraphruek P, Chusak C, Ngamukote S, Sawaswong V, Chanchaem P, Payungporn S, Suantawee T, Adisakwattana S. Effect of a Multispecies Synbiotic Supplementation on Body Composition, Antioxidant Status, and Gut Microbiomes in Overweight and Obese Subjects: A Randomized, Double-Blind, Placebo-Controlled Study. Nutrients 2023; 15:nu15081863. [PMID: 37111082 PMCID: PMC10141052 DOI: 10.3390/nu15081863] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/27/2023] [Revised: 04/05/2023] [Accepted: 04/11/2023] [Indexed: 04/29/2023] Open
Abstract
Studies investigating the effect of multispecies synbiotic supplementation in obesity management are limited. The current study was performed to evaluate the effects of multispecies probiotics mixed with fructooligosaccharides on body composition, antioxidant status, and gut microbiome composition in overweight and obese individuals. We employed a randomized, double-blind, placebo-controlled trial design, in which 63 individuals aged 18-45 years were assigned to receive either a synbiotic supplement or placebo for 12 weeks. The synbiotic group consumed a daily dose of 37 × 109 colony-forming units (CFU) of a unique blend of seven different probiotics, along with 2 g of fructooligosaccharides, while the placebo group consumed 2 g of maltodextrin daily. Assessments were performed at baseline, week 6, and the end of the study. The results of the study indicated that synbiotic supplementation resulted in a significant reduction in waist circumference and body fat percentage compared to the baseline measurements, as observed at 12 weeks. At the end of the study, there were no significant differences observed in body weight, BMI, waist circumference, or percentage of body fat between the synbiotic group and the placebo group. An analysis of plasma antioxidant capacity revealed that synbiotic supplementation caused a significant increase in Trolox equivalent antioxidant capacity (TEAC) and a concomitant decrease in malondialdehyde (MDA) in the test group when compared to the placebo. For the gut microbiota analysis, synbiotic supplementation significantly decreased Firmicutes abundance and the Firmicutes/Bacteroidetes (F/B) ratio at week 12 as compared to the placebo group. Nevertheless, the synbiotic group did not exhibit any substantial alterations in other biochemical blood parameters compared to the placebo group. These findings suggest that multispecies synbiotic supplementation could be a beneficial strategy to improve body composition, antioxidant status, and gut microbiome composition in overweight and obese subjects.
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Affiliation(s)
- Piyarat Oraphruek
- Phytochemical and Functional Food Research Unit for Clinical Nutrition, Department of Nutrition and Dietetics, Faculty of Allied Health Sciences, Chulalongkorn University, Bangkok 10330, Thailand
| | - Charoonsri Chusak
- Phytochemical and Functional Food Research Unit for Clinical Nutrition, Department of Nutrition and Dietetics, Faculty of Allied Health Sciences, Chulalongkorn University, Bangkok 10330, Thailand
| | - Sathaporn Ngamukote
- Phytochemical and Functional Food Research Unit for Clinical Nutrition, Department of Nutrition and Dietetics, Faculty of Allied Health Sciences, Chulalongkorn University, Bangkok 10330, Thailand
| | - Vorthon Sawaswong
- Center of Excellence in Systems Microbiology, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand
| | - Prangwalai Chanchaem
- Center of Excellence in Systems Microbiology, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand
| | - Sunchai Payungporn
- Center of Excellence in Systems Microbiology, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand
- Department of Biochemistry, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand
| | - Tanyawan Suantawee
- Phytochemical and Functional Food Research Unit for Clinical Nutrition, Department of Nutrition and Dietetics, Faculty of Allied Health Sciences, Chulalongkorn University, Bangkok 10330, Thailand
| | - Sirichai Adisakwattana
- Phytochemical and Functional Food Research Unit for Clinical Nutrition, Department of Nutrition and Dietetics, Faculty of Allied Health Sciences, Chulalongkorn University, Bangkok 10330, Thailand
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Thriene K, Michels KB. Human Gut Microbiota Plasticity throughout the Life Course. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2023; 20:1463. [PMID: 36674218 PMCID: PMC9860808 DOI: 10.3390/ijerph20021463] [Citation(s) in RCA: 14] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/01/2022] [Revised: 01/06/2023] [Accepted: 01/09/2023] [Indexed: 06/02/2023]
Abstract
The role of the gut microbiota in human health and disease has garnered heightened attention over the past decade. A thorough understanding of microbial variation over the life course and possible ways to influence and optimize the microbial pattern is essential to capitalize on the microbiota's potential to influence human health. Here, we review our current understanding of the concept of plasticity of the human gut microbiota throughout the life course. Characterization of the plasticity of the microbiota has emerged through recent research and suggests that the plasticity in the microbiota signature is largest at birth when the microbial colonization of the gut is initiated and mode of birth imprints its mark, then decreases postnatally continuously and becomes less malleable and largely stabilized with advancing age. This continuing loss of plasticity has important implication for the impact of the exposome on the microbiota and health throughout the life course and the identification of susceptible 'windows of opportunity' and methods for interventions.
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Affiliation(s)
- Kerstin Thriene
- Institute for Prevention and Cancer Epidemiology, Faculty of Medicine and Medical Center, University of Freiburg, 79110 Freiburg, Germany
| | - Karin B. Michels
- Institute for Prevention and Cancer Epidemiology, Faculty of Medicine and Medical Center, University of Freiburg, 79110 Freiburg, Germany
- Department of Epidemiology, Fielding School of Public Health, University of California, Los Angeles, CA 90095, USA
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8
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Li J, Lv JL, Cao XY, Zhang HP, Tan YJ, Chu T, Zhao LL, Liu Z, Ren YS. Gut microbiota dysbiosis as an inflammaging condition that regulates obesity-related retinopathy and nephropathy. Front Microbiol 2022; 13:1040846. [PMID: 36406423 PMCID: PMC9666733 DOI: 10.3389/fmicb.2022.1040846] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/09/2022] [Accepted: 10/17/2022] [Indexed: 01/21/2023] Open
Abstract
Diabetes-specific microvascular disease is a leading cause of blindness, renal failure and nerve damage. Epidemiological data demonstrated that the high morbidity of T2DM occurs as a result of obesity and gradually develops into serious complications. To date, the mechanisms that underlie this observation are still ill-defined. In view of the effect of obesity on the gut microflora, Leprdb/db mice underwent antibiotic treatment and microbiota transplants to modify the gut microbiome to investigate whether microbes are involved in the development of diabetic nephropathy (DN) and/or diabetic retinopathy (DR). The mouse feces were collected for bacterial 16S ribosomal RNA gene sequencing. Cytokines including TNF-α, TGF-β1, IFN-γ, IL-1β, IL-6, IL-17A, IL-10, and VEGFA were detected by enzyme-linked immunosorbent assay (ELISA), flow cytometry, real-time PCR and immunofluorescent assay. Eyes and kidney were collected for histopathological assay. Intestinal permeability was also detected using Evans Blue. The results showed that obesity influenced metabolic variables (including fast/fed glucose, insulin, and triglyceride), retinopathy and nephropathy, and the gut microbiota. Obesity mainly reduced the ratio of Bacteroidetes/Firmicutes and influenced relative abundance of Proteobacteria, Actinobacteria, and Spirochetes. Obesity also increased intestinal permeability, metabolic endotoxemia, cytokines, and VEGFA. Microbiota transplants confirm that obesity aggravates retinopathy and nephropathy through the gut microbiota. These findings suggest that obesity exacerbates retinopathy and nephropathy by inducing gut microbiota dysbiosis, which further enhanced intestinal permeability and chronic low-grade inflammation.
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Affiliation(s)
- Jie Li
- Yantai Key Laboratory of Pharmacology of Traditional Chinese Medicine in Tumor Metabolism, Binzhou Medical University, Yantai, China
| | - Jun-lin Lv
- Yantai Key Laboratory of Pharmacology of Traditional Chinese Medicine in Tumor Metabolism, Binzhou Medical University, Yantai, China
| | - Xin-yue Cao
- Yantai Key Laboratory of Pharmacology of Traditional Chinese Medicine in Tumor Metabolism, Binzhou Medical University, Yantai, China
| | - Hai-ping Zhang
- Endocrine and Metabolic Diseases Hospital of Shandong First Medical University, Jinan, China
| | - Yu-jun Tan
- Yantai Key Laboratory of Pharmacology of Traditional Chinese Medicine in Tumor Metabolism, Binzhou Medical University, Yantai, China
| | - Ting Chu
- School of Life Sciences, Jiangsu Normal University, Xuzhou, China
| | - Li-li Zhao
- State Key Laboratory of Generic Manufacture Technology of Chinese Traditional Medicine, Lunan Pharmaceutical Group Co., Ltd., Linyi, China
| | - Zhong Liu
- State Key Laboratory of Generic Manufacture Technology of Chinese Traditional Medicine, Lunan Pharmaceutical Group Co., Ltd., Linyi, China,*Correspondence: Zhong Liu,
| | - Yu-shan Ren
- Yantai Key Laboratory of Pharmacology of Traditional Chinese Medicine in Tumor Metabolism, Binzhou Medical University, Yantai, China,Yu-shan Ren,
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9
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Shehata AM, Paswan VK, Attia YA, Abougabal MS, Khamis T, Alqosaibi AI, Alnamshan MM, Elmazoudy R, Abaza MA, Salama EAA, El-Saadony MT, Saad AM, Abdel-Moneim AME. In ovo Inoculation of Bacillus subtilis and Raffinose Affects Growth Performance, Cecal Microbiota, Volatile Fatty Acid, Ileal Morphology and Gene Expression, and Sustainability of Broiler Chickens ( Gallus gallus). Front Nutr 2022; 9:903847. [PMID: 35711554 PMCID: PMC9194610 DOI: 10.3389/fnut.2022.903847] [Citation(s) in RCA: 23] [Impact Index Per Article: 7.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/24/2022] [Accepted: 05/04/2022] [Indexed: 11/13/2022] Open
Abstract
Banning antibiotic growth promoters has negatively impacted poultry production and sustainability, which led to exploring efficient alternatives such as probiotics, probiotics, and synbiotics. Effect of in ovo injection of Bacillus subtilis, raffinose, and their synbiotics on growth performance, cecal microbial population and volatile fatty acid concentration, ileal histomorphology, and ileal gene expression was investigated in broilers (Gallus gallus) raised for 21 days. On 300 h of incubation, a total of 1,500 embryonated eggs were equally allotted into 10 groups. The first was non-injected (NC) and the remaining in ovo injected with sterile distilled water (PC), B. subtilis 4 × 105 and 4 × 106 CFU (BS1 and BS2), Raffinose 2 and 3 mg (R1 and R2), B. subtilis 4 × 105 CFU + raffinose 2 mg (BS1R1), B. subtilis 4 × 105 CFU + raffinose 3 mg (BS1R2), B. subtilis 4 × 106 CFU + raffinose 2 mg (BS2R1), and B. subtilis 4 × 106 CFU + raffinose 3 mg (BS2R2). At hatch, 60 chicks from each group were randomly chosen, divided into groups of 6 replicates (10 birds/replicate), and fed with a corn–soybean-based diet. In ovo inoculation of B. subtilis and raffinose alone or combinations significantly improved body weight, feed intake, and feed conversion ratio of 21-day-old broilers compared to NC. Cecal concentrations of butyric, pentanoic, propionic, and isobutyric acids were significantly elevated in R1, R2, BS2R1, and BS2R2, whereas isovaleric and acetic acids were significantly increased in R1 and BS2R1 compared to NC. Cecal microbial population was significantly altered in treated groups. Ileal villus height was increased (p < 0.001) in BS1, R2, and BS2R2 compared to NC. The mRNA expression of mucin-2 was upregulated (p < 0.05) in synbiotic groups except for BS1R1. Vascular endothelial growth factor (VEGF) expression was increased (p < 0.05) in BS2, R1, BS1R1, and BS1R2 compared to NC. SGLT-1 expression was upregulated (p < 0.05) in all treated birds except those of R1 group compared to NC. The mRNA expressions of interleukin (IL)-2 and toll-like receptor (TLR)-4 were downregulated (p < 0.05) in BS2 and R1 for IL-2 and BS1R1 and BS2R2 for TLR-4. It was concluded that in ovo B. subtilis, raffinose, and synbiotics positively affected growth performance, cecal microbiota, gut health, immune responses, and thus the sustainability of production in 21-day-old broilers.
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Affiliation(s)
- Abdelrazeq M Shehata
- Department of Animal Production, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt.,Department of Dairy Science and Food Technology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, India
| | - Vinod K Paswan
- Department of Dairy Science and Food Technology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, India
| | - Youssef A Attia
- Department of Animal and Poultry Production, Faculty of Agriculture, Damanhour University, Damanhour, Egypt.,Sustainable Agriculture Research Group, Department of Agriculture, Faculty of Environmental Sciences, King Abdulaziz University, Jeddah, Saudi Arabia
| | - Mohammed Sh Abougabal
- Department of Animal Production, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt
| | - Tarek Khamis
- Department of Pharmacology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt.,Laboratory of Biotechnology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt
| | - Amany I Alqosaibi
- Biology Department, College of Science, Imam Abdulrahman Bin Faisal University, Dammam, Saudi Arabia
| | - Mashael M Alnamshan
- Biology Department, College of Science, Imam Abdulrahman Bin Faisal University, Dammam, Saudi Arabia
| | - Reda Elmazoudy
- Biology Department, College of Science, Imam Abdulrahman Bin Faisal University, Dammam, Saudi Arabia
| | - Mohamed A Abaza
- Avian and Rabbit Diseases Department, Faculty of Veterinary Medicine, Benha University, Banha, Egypt
| | - Ehab A A Salama
- Agricultural Botany Department, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria, Egypt
| | - Mohamed T El-Saadony
- Department of Agricultural Microbiology, Faculty of Agriculture, Zagazig University, Zagazig, Egypt
| | - Ahmed M Saad
- Biochemistry Department, Faculty of Agriculture, Zagazig University, Zagazig, Egypt
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10
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Zou L. Pivotal Dominant Bacteria Ratio and Metabolites Related to Healthy Body Index Revealed by Intestinal Microbiome and Metabolomics. Indian J Microbiol 2022; 62:130-141. [PMID: 35068612 PMCID: PMC8758854 DOI: 10.1007/s12088-021-00989-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/07/2021] [Accepted: 10/18/2021] [Indexed: 11/24/2022] Open
Abstract
Various body indexes, especially body fat percentage (BFP), are widely used as effective indicators to measure our health. BFP is used in medicine to assess obesity, which is a body fat mass disorder accompanied with changes of the gut microbiota. However, the relationship between BFP and the gut microbiota has not been studied so far. To address this problem, we examined how gut microbiota and metabolome associated with body indices in healthy people. Microbial and metabolomics data based on 16S rDNA sequencing and LC-MS were obtained from stool samples of 20 healthy adults. Bioinformatics analysis was performed to explore the correlations between the body indices and gut microbial characteristics. Significantly different microbes were further validated via qPCR. Differential characteristics were filtered by building machine learning models to predict body status. Our data showed that abundance of Prevotella and the Prevotella/Bacteroides (P/B) ratio in the gut were markedly higher in high-BFP individuals than in low-BFP individuals. Microbial and metabolomics data consistently suggested significant differences in fatty acid metabolism in stool samples from the two groups. The P/B ratio and fatty acids are discriminative for people with different index levels by cross validation tests with machine learning models. These results suggest using Prevotella and fecal fatty acids as predictors may offer an alternative method for evaluating health status or weight loss. SUPPLEMENTARY INFORMATION The online version contains supplementary material available at 10.1007/s12088-021-00989-5.
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Affiliation(s)
- Lingyun Zou
- Sichuan EYE Hospital, Aier EYE Hospital Group, No. 153, Tianfu Fourth Street, High-tech Zone, Chengdu, 610047 China
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11
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Bhuta R, DeNardo B, Wang J, Atoyan J, Zhang Y, Nelson D, Shapiro J. Durable changes in the gut microbiome in survivors of childhood acute lymphoblastic leukemia. Pediatr Blood Cancer 2021; 68:e29308. [PMID: 34467651 DOI: 10.1002/pbc.29308] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/11/2021] [Revised: 07/13/2021] [Accepted: 07/14/2021] [Indexed: 11/06/2022]
Abstract
There are limiteddata on long-term changes in the gut microbiome after acute lymphoblastic leukemia (ALL) therapy. We compared the gut microbial composition in stool samples of nine survivors of childhood ALL with 10 healthy sibling controls using 16S rRNA gene sequencing. Analysis of beta diversity within family units demonstrated a significant difference in bacterial strains between patients and healthy siblings. A significant difference in alpha diversity between patients and their healthy siblings was noted using Pielou's evenness. The composition of the gut microbiome differs between pediatric ALL survivors and healthy sibling controls for years after completion of therapy.
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Affiliation(s)
- Roma Bhuta
- Division of Pediatric Hematology-Oncology, Hasbro Children's Hospital, The Warren Alpert Medical School of Brown University, Providence, Rhode Island, USA
| | - Bradley DeNardo
- Division of Pediatric Hematology-Oncology, Hasbro Children's Hospital, The Warren Alpert Medical School of Brown University, Providence, Rhode Island, USA
| | - Jing Wang
- Department of Cell and Molecular Biology, University of Rhode Island, Kingston, Rhode Island, USA
| | - Janet Atoyan
- Rhode Island Genomics and Sequencing Center, University of Rhode Island, Kingston, Rhode Island, USA
| | - Ying Zhang
- Department of Cell and Molecular Biology, University of Rhode Island, Kingston, Rhode Island, USA
| | - David Nelson
- Department of Cell and Molecular Biology, University of Rhode Island, Kingston, Rhode Island, USA
| | - Jason Shapiro
- Division of Pediatric Gastroenterology, Hasbro Children's Hospital, Nutrition and Liver Diseases, The Warren Alpert Medical School of Brown University, Providence, Rhode Island, USA
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12
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Nour MA, El-Hindawy MM, Abou-Kassem DE, Ashour EA, Abd El-Hack ME, Mahgoub S, Aboelenin SM, Soliman MM, El-Tarabily KA, Abdel-Moneim AME. Productive performance, fertility and hatchability, blood indices and gut microbial load in laying quails as affected by two types of probiotic bacteria. Saudi J Biol Sci 2021; 28:6544-6555. [PMID: 34764770 PMCID: PMC8568992 DOI: 10.1016/j.sjbs.2021.07.030] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/23/2021] [Revised: 06/16/2021] [Accepted: 07/06/2021] [Indexed: 01/23/2023] Open
Abstract
This study investigated two kinds of probiotic bacteria (Bacillus toyonensis, B1 and Bifidobacterium bifidum, B2) on laying Japanese quail’s performance, egg quality, fertility and hatchability, blood biochemical characteristics and microbiological parameters. A total of 270 mature quails (180 females and 90 males) were distributed into ten groups in a completely randomized design at eight weeks of age. The experimental groups were as follows: T1: basal diet only (control); T2-T5, basal diet plus 0.05, 0.075, 0.10 and 0.125% B1, respectively; T6: basal diet plus 0.10% B2; T7-T10: basal diet plus 0.05, 0.075, 0.10 and 0.125% B1 plus 0.05% B2, respectively. Results revealed that egg number (EN) and egg weight (EW) were gradually increased (P < 0.01) as the levels of both probiotic types increased. The feed conversion ratio (FCR) was significantly (P < 0.05) better within the total experimental period (8–20 weeks) due to B1 alone or/with B2 supplementation. Values of yolk percentage (Y%) were statistically (P < 0.01) higher only at 8–20 weeks of age and T10 recorded the highest value. By increasing the level of probiotics, fertility and hatchability percentages (F% and H%) were gradually increased (P < 0.01 and P < 0.05). Creatinine (CR) level was statistically reduced in birds fed T4 diet. Also, urea-N and aspartate aminotransferase (AST) levels were reduced in treated birds. The opposite was found regarding alkaline phosphatase (ALP). Conclusively, using B1 and B2 enhanced the productive performance, some egg quality traits, fertility and hatchability, digestive enzyme activities, and reduced the harmful bacteria in the gut of laying Japanese quail. Our findings could recommend to apply T4 (basal diet + 0.10 % B1), T6 (basal diet + 0.10% B2) and T9 (basal diet + 0.10% B1 + 0.05% B2) levels for the best results.
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Affiliation(s)
- Mohamed A Nour
- Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt
| | - Mohamed M El-Hindawy
- Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt
| | - Diaa E Abou-Kassem
- Animal and Poultry Production Department, Faculty of Technology and Development, Zagazig University, Zagazig 44511, Egypt
| | - Elwy A Ashour
- Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt
| | - Mohamed E Abd El-Hack
- Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt
| | - Samir Mahgoub
- Agricultural Microbiology Department, Faculty of Agriculture, Zagazig University, Zagazig 44111, Egypt
| | - Salama M Aboelenin
- Biology Department, Turabah University College, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia
| | - Mohamed M Soliman
- Clinical Laboratory Sciences Department, Turabah University College, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia
| | - Khaled A El-Tarabily
- Department of Biology, College of Science, United Arab Emirates University, 15551 Al-Ain, United Arab Emirates.,Harry Butler Institute, Murdoch University, Murdoch, 6150, Western Australia, Australia
| | - Abdel-Moneim E Abdel-Moneim
- Biological Application Department, Nuclear Research Center, Atomic Energy Authority, Abou-Zabael 13759, Egypt
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13
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Gao F, Fang Z, Lu W. Regulation divergences of Lactobacillus fermentum PCC and Lactobacillus paracasei 431 on penicillin-induced upper respiratory tract microbial dysbiosis in BALB/c mice. Food Funct 2021; 12:11913-11925. [PMID: 34739535 DOI: 10.1039/d0fo02981e] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Antibiotic-induced host health imbalance during upper respiratory tract infection (URTI) treatment is an emerging issue. Studies have confirmed that Lactobacillus casei 431 and Lactobacillus fermentum PCC alleviate gut microbiome dysbiosis and improve immune response. However, their effect on the upper respiratory tract (URT) microbial structure and the correlation between the URT microbiota and immunological indicators remain unclear. To evaluate the effects of Lactobacillus strains on restoring penicillin-induced imbalance in the URT microbiome and on immune response, Lactobacillus fermentum PCC and Lactobacillus casei 431 were individually administered to penicillin-pretreated mice, and their effects were assessed. The results revealed that L. casei 431 and L. fermentum PCC could regulate the systemic immune response imbalance, but the regulation direction of L. fermentum PCC was closer to that of the control group. Moreover, the Lactobacillus strains could restore penicillin-induced URT dysbacteriosis in the microbial community structure, but no significant change in alpha diversity was observed. The key bacterial taxa modulated by L. casei 431 were Faecalibaculum, Lactococcus, and Ralstonia. L. fermentum PCC enhanced biofilms and facultatively anaerobic bacteria. Different regulation pathways were observed in the two strains, and RDA revealed that both L. casei 431 and L. fermentum PCC groups were correlated with IL-17 and IL-1α, while the L. casei 431 group was also correlated with IL-6. In conclusion, L. casei 431 and L. fermentum PCC could beneficially and differentially ameliorate penicillin-induced imbalance in the URT microbial composition structure and functional metabolic pathways and modulate immune response, reflecting strain-specific regulation.
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Affiliation(s)
- Feng Gao
- State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China. .,School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Zhifeng Fang
- State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China. .,School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China
| | - Wenwei Lu
- State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China. .,School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China.,National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, Jiangsu 214122, China.,(Yangzhou) Institute of Food Biotechnology, Jiangnan University, Yangzhou 225004, China
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14
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Stanislawski MA, Frank DN, Borengasser SJ, Ostendorf DM, Ir D, Jambal P, Bing K, Wayland L, Siebert JC, Bessesen DH, MacLean PS, Melanson EL, Catenacci VA. The Gut Microbiota during a Behavioral Weight Loss Intervention. Nutrients 2021; 13:3248. [PMID: 34579125 PMCID: PMC8471894 DOI: 10.3390/nu13093248] [Citation(s) in RCA: 28] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/31/2021] [Revised: 09/13/2021] [Accepted: 09/14/2021] [Indexed: 12/14/2022] Open
Abstract
Altered gut microbiota has been linked to obesity and may influence weight loss. We are conducting an ongoing weight loss trial, comparing daily caloric restriction (DCR) to intermittent fasting (IMF) in adults who are overweight or obese. We report here an ancillary study of the gut microbiota and selected obesity-related parameters at the baseline and after the first three months of interventions. During this time, participants experienced significant improvements in clinical health measures, along with altered composition and diversity of fecal microbiota. We observed significant associations between the gut microbiota features and clinical measures, including weight and waist circumference, as well as changes in these clinical measures over time. Analysis by intervention group found between-group differences in the relative abundance of Akkermansia in response to the interventions. Our results provide insight into the impact of baseline gut microbiota on weight loss responsiveness as well as the early effects of DCR and IMF on gut microbiota.
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Affiliation(s)
- Maggie A. Stanislawski
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Daniel N. Frank
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Sarah J. Borengasser
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Danielle M. Ostendorf
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Diana Ir
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Purevsuren Jambal
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Kristen Bing
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Liza Wayland
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Janet C. Siebert
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Daniel H. Bessesen
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Paul S. MacLean
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
| | - Edward L. Melanson
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
- Eastern Colorado Veterans Affairs Geriatric Research, Education and Clinical Center, Denver, CO 80045, USA
| | - Victoria A. Catenacci
- School of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA; (D.N.F.); (S.J.B.); (D.M.O.); (D.I.); (P.J.); (K.B.); (L.W.); (J.C.S.); (D.H.B.); (P.S.M.); (E.L.M.); (V.A.C.)
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15
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Wu H, Chiou J. Potential Benefits of Probiotics and Prebiotics for Coronary Heart Disease and Stroke. Nutrients 2021; 13:2878. [PMID: 34445037 PMCID: PMC8401746 DOI: 10.3390/nu13082878] [Citation(s) in RCA: 64] [Impact Index Per Article: 16.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/30/2021] [Revised: 08/18/2021] [Accepted: 08/19/2021] [Indexed: 12/16/2022] Open
Abstract
Among cardiovascular diseases (CVDs), a major cause of morbidity and mortality worldwide, coronary heart disease and stroke are the most well-known and extensively studied. The onset and progression of CVD is associated with multiple risk factors, among which, gut microbiota has received much attention in the past two decades. Gut microbiota, the microbial community colonizing in the gut, plays a prominent role in human health. In particular, gut dysbiosis is directly related to many acute or chronic dysfunctions of the cardiovascular system (CVS) in the host. Earlier studies have demonstrated that the pathogenesis of CVD is strongly linked to intestinal microbiota imbalance and inflammatory responses. Probiotics and prebiotics conferring various health benefits on the host are emerging as promising therapeutic interventions for many diseases. These two types of food supplements have the potential to alleviate the risks of CVD through improving the levels of several cardiovascular markers, such as total and low-density lipoprotein (LDL) cholesterol, high sensitivity C-reactive protein (hs-CRP), and certain cytokines involved in the inflammatory response. In this review, we focus mainly on the preventive effects of probiotics and prebiotics on CVD via rebalancing the structural and functional changes in gut microbiota and maintaining immune homeostasis.
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Affiliation(s)
- Haicui Wu
- Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China;
- Research Institute for Future Food, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China
| | - Jiachi Chiou
- Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China;
- Research Institute for Future Food, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China
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16
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Beam A, Clinger E, Hao L. Effect of Diet and Dietary Components on the Composition of the Gut Microbiota. Nutrients 2021; 13:2795. [PMID: 34444955 PMCID: PMC8398149 DOI: 10.3390/nu13082795] [Citation(s) in RCA: 286] [Impact Index Per Article: 71.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2021] [Revised: 08/06/2021] [Accepted: 08/11/2021] [Indexed: 12/18/2022] Open
Abstract
Diet and dietary components have profound effects on the composition of the gut microbiota and are among the most important contributors to the alteration in bacterial flora. This review examines the effects the "Western", "plant-based", "high-fat", "medical ketogenic", and "Mediterranean" diets have on the composition of the gut microbiota in both mice and human subjects. We show that specific dietary components that are commonly found in the "plant-based" and "Mediterranean" diet play a role in shifting the microbial composition. This review further evaluates the bacterial metabolites that are associated with diet, and their role in systemic inflammation and metabolic endotoxemia. Furthermore, the associations between diet/dietary components and altering bacterial composition, may lead to potential therapeutic targets for type II diabetes, obesity, and inflammatory diseases.
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Affiliation(s)
- Ashley Beam
- Department of Food and Nutrition, Indiana University of Pennsylvania, Indiana, PA 15705, USA; (A.B.); (E.C.)
| | - Elizabeth Clinger
- Department of Food and Nutrition, Indiana University of Pennsylvania, Indiana, PA 15705, USA; (A.B.); (E.C.)
- Nutrition with Elizabeth, LLC, Brookville, PA 15825, USA
| | - Lei Hao
- Department of Food and Nutrition, Indiana University of Pennsylvania, Indiana, PA 15705, USA; (A.B.); (E.C.)
- Department of Nursing and Allied Health Professions, Indiana University of Pennsylvania, Indiana, PA 15705, USA
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17
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Effect of graded levels of dietary Bacillus toyonensis and Bifidobacterium bifidum supplementation on growth, carcass traits and ileal histomorphometry and microbiota of growing quails. Saudi J Biol Sci 2021; 28:4532-4541. [PMID: 34354439 PMCID: PMC8325023 DOI: 10.1016/j.sjbs.2021.04.054] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2021] [Revised: 04/14/2021] [Accepted: 04/18/2021] [Indexed: 11/30/2022] Open
Abstract
This experiment investigated the role of graded dietary levels of two probiotic strains (Bacillus toyonensis; BT and Bifidobacterium bifidum; BB) on the growth rate, carcass traits, physiological and histological aspects of growing Japanese quail. One thousand and three hundred sixty one-day-old un-sexed Japanese quail chicks were distributed randomly into ten groups. The 1st group served as a control and fed the basal diet without supplement while the 2nd, 3rd, 4th and 5th groups received the control diet supplemented with 0.05, 0.075, 0.10 and 0.125% BT, respectively. The 6th group fed the control diet plus 0.10% BB while the remaining groups (7th to 10th) received the basal diet incorporated with the previous levels of BT rich with 0.05% BB. Dietary supplementation of BT and/or BB increased body weight and gain; however, feed intake and feed conversion were not affected. Amylase activity was significantly elevated in 5th, 7th and 9th groups, while lipase activity was improved in all treatment groups except 3rd and 6th groups. Results obtained concluded that dietary supplementation of BT with or without BB is useful for performance, digestive enzyme activities, blood cholesterols, antioxidant status and ileal histomorphometry and microbiota of growing Japanese quail.
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18
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Djekkoun N, Lalau JD, Bach V, Depeint F, Khorsi-Cauet H. Chronic oral exposure to pesticides and their consequences on metabolic regulation: role of the microbiota. Eur J Nutr 2021; 60:4131-4149. [PMID: 33837455 DOI: 10.1007/s00394-021-02548-6] [Citation(s) in RCA: 11] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/16/2020] [Accepted: 03/22/2021] [Indexed: 12/17/2022]
Abstract
Pesticides have long been used in agriculture and household treatments. Pesticide residues can be found in biological samples for both the agriculture workers through direct exposure but also to the general population by indirect exposure. There is also evidence of pesticide contamination in utero and trans-generational impacts. Whilst acute exposure to pesticides has long been associated with endocrine perturbations, chronic exposure with low doses also increases the prevalence of metabolic disorders such as obesity or type 2 diabetes. Dysmetabolism is a low-grade inflammation disorder and as such the microbiota plays a role in its etiology. It is therefore important to fully understand the role of microbiota on the genesis of subsequent health effects. The digestive tract and mostly microbiota are the first organs of contact after oral exposure. The objective of this review is thus to better understand mechanisms that link pesticide exposure, dysmetabolism and microbiota. One of the key outcomes on the microbiota is the reduced Bacteroidetes and increased Firmicutes phyla, reflecting both pesticide exposure and risk factors of dysmetabolism. Other bacterial genders and metabolic activities are also involved. As for most pathologies impacting microbiota (including inflammatory disorders), the role of prebiotics can be suggested as a prevention strategy and some preliminary evidence reinforces this axis.
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Affiliation(s)
- Narimane Djekkoun
- PeriTox UMR_I 01 Laboratory, University Center for Health Research, CURS-UPJV, Picardy Jules Verne University, 80054, Amiens cedex 1, France
| | - Jean-Daniel Lalau
- PeriTox UMR_I 01 Laboratory, University Center for Health Research, CURS-UPJV, Picardy Jules Verne University, 80054, Amiens cedex 1, France.,Service Endocrinologie, Diabétologie, Nutrition, CHU Amiens Picardie, Site Nord, 80054, Amiens cedex 1, France
| | - Véronique Bach
- PeriTox UMR_I 01 Laboratory, University Center for Health Research, CURS-UPJV, Picardy Jules Verne University, 80054, Amiens cedex 1, France
| | - Flore Depeint
- Unité Transformations & Agroressources ULR7519, Institut Polytechnique UniLaSalle-Université d'Artois, 60026, Beauvais, France
| | - Hafida Khorsi-Cauet
- PeriTox UMR_I 01 Laboratory, University Center for Health Research, CURS-UPJV, Picardy Jules Verne University, 80054, Amiens cedex 1, France.
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19
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El-Mallah CA, Beyh YS, Obeid OA. Iron Fortification and Supplementation: Fighting Anemia of Chronic Diseases or Fueling Obesity? Curr Dev Nutr 2021; 5:nzab032. [PMID: 33959691 PMCID: PMC8085477 DOI: 10.1093/cdn/nzab032] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/06/2020] [Revised: 01/07/2021] [Accepted: 03/31/2021] [Indexed: 12/13/2022] Open
Abstract
The significant worldwide increase in obesity has become a major health problem. Excess adiposity has been extensively linked to inflammation. Recently, studies have shown that dietary intake and microbiota dysbiosis can affect the health of the gut and lead to low-grade systemic inflammation, worsening the state of obesity and further exacerbating inflammation. The latter is shown to decrease iron status and potentially increase the risk of anemia by inhibiting iron absorption. Hence, anemia of obesity is independent of iron intake and does not properly respond to increased iron ingestion. Therefore, countries with a high rate of obesity should assess the health impact of fortification and supplementation with iron due to their potential drawbacks. This review tries to elucidate the relation between inflammation and iron status to better understand the etiology of anemia of obesity and chronic diseases and wisely design any dietary or medical interventions for the management of anemia and/or obesity.
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Affiliation(s)
- Carla A El-Mallah
- Department of Nutrition and Food Science, Faculty of Agricultural and Food Sciences, American University of Beirut, Beirut, Lebanon
| | - Yara S Beyh
- Nutrition and Health Sciences, Laney Graduate School, Emory University, Atlanta, GA, USA
| | - Omar A Obeid
- Department of Nutrition and Food Science, Faculty of Agricultural and Food Sciences, American University of Beirut, Beirut, Lebanon
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20
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Huang J, Huang J, Yin T, Lv H, Zhang P, Li H. Enterococcus faecium R0026 Combined with Bacillus subtilis R0179 Prevent Obesity-Associated Hyperlipidemia and Modulate Gut Microbiota in C57BL/6 Mice. J Microbiol Biotechnol 2021; 31:181-188. [PMID: 33144552 PMCID: PMC9706029 DOI: 10.4014/jmb.2009.09005] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/04/2020] [Revised: 10/13/2020] [Accepted: 10/18/2020] [Indexed: 01/09/2023]
Abstract
Bacillus subtilis and Enterococcus faecium are commonly used probiotics. This study aimed to identify the effect of live combined Bacillus subtilis R0179 and Enterococcus faecium R0026 (LCBE) on obesityassociated hyperlipidemia and gut microbiota in C57BL/6 mice. Forty male C57BL/6 mice were divided into four groups: normal group (N group), model group (M group), low-dose group (L group), and high-dose group (H group). Mice were gavaged with LCBE at 0.023 g/mice/day (L group) or 0.23 g/mice/day (H group) and fed with a high-fat diet for 8 weeks. In vitro E. faecium R0026 showed an ability to lower the low-concentration of cholesterol by 46%, and the ability to lower the highconcentration of cholesterol by 58%. LCBE significantly reduced the body weight gain, Lee index, brown fat index and body mass index of mice on a high-fat diet. Moreover, LCBE markedly improved serum lipids (including serum triglyceride, total cholesterol, low-density lipoprotein and highdensity lipoprotein) while also significantly reducing liver total cholesterol. Serum lipopolysaccharide and total bile acid in L and H groups decreased significantly compared with M group. PCR-DGGE analysis showed that the composition of gut microbiota in the treatment groups was improved. Akkermansia muciniphila was found in H group. The PCA result indicated a similar gut microbiota structure between LCBE treatment groups and normal group while the number of bands and Shannon diversity index increased significantly in the LCBE treatment groups. Finally, qPCR showed Bifidobacterium spp. increased significantly in H group compared with M group, LCBE alleviated liver steatosis and improved brown adipose tissue index.
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Affiliation(s)
- Jinli Huang
- Department of Microecology, College of Basic Medical Sciences, Dalian Medical University, Dalian 6044, P.R. China
| | - Juan Huang
- Department of Microecology, College of Basic Medical Sciences, Dalian Medical University, Dalian 6044, P.R. China
| | - Tianyi Yin
- First Affiliated Hospital of Dalian Medical University, Dalian, P.R. China
| | - Huiyun Lv
- First Affiliated Hospital of Dalian Medical University, Dalian, P.R. China
| | - Pengyu Zhang
- Department of Microecology, College of Basic Medical Sciences, Dalian Medical University, Dalian 6044, P.R. China
| | - Huajun Li
- Department of Microecology, College of Basic Medical Sciences, Dalian Medical University, Dalian 6044, P.R. China,Corresponding author Phone: +86-411 86110305 Fax: +86-411-86110282 E-mail:
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21
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Jobira B, Frank DN, Silveira LJ, Pyle L, Kelsey MM, Garcia-Reyes Y, Robertson CE, Ir D, Nadeau KJ, Cree-Green M. Hepatic steatosis relates to gastrointestinal microbiota changes in obese girls with polycystic ovary syndrome. PLoS One 2021; 16:e0245219. [PMID: 33465100 PMCID: PMC7815089 DOI: 10.1371/journal.pone.0245219] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/31/2020] [Accepted: 12/23/2020] [Indexed: 02/06/2023] Open
Abstract
Objective Hepatic steatosis (HS) is common in adolescents with obesity and polycystic ovary syndrome (PCOS). Gut microbiota are altered in adults with obesity, HS, and PCOS, which may worsen metabolic outcomes, but similar data is lacking in youth. Methods Thirty-four adolescents with PCOS and obesity underwent stool and fasting blood collection, oral glucose tolerance testing, and MRI for hepatic fat fraction (HFF). Fecal bacteria were profiled by high-throughput 16S rRNA gene sequencing. Results 50% had HS (N = 17, age 16.2±1.5 years, BMI 38±7 kg/m2, HFF 9.8[6.5, 20.7]%) and 50% did not (N = 17, age 15.8±2.2 years, BMI 35±4 kg/m2, HFF 3.8[2.6, 4.4]%). The groups showed no difference in bacterial α-diversity (richness p = 0.202; evenness p = 0.087; and diversity p = 0.069) or global difference in microbiota (β-diversity). Those with HS had lower % relative abundance (%RA) of Bacteroidetes (p = 0.013), Bacteroidaceae (p = 0.009), Porphyromonadaceae (p = 0.011), and Ruminococcaceae (p = 0.008), and higher Firmicutes:Bacteroidetes (F:B) ratio (47.8% vs. 4.3%, p = 0.018) and Streptococcaceae (p = 0.034). Bacterial taxa including phyla F:B ratio, Bacteroidetes, and family Bacteroidaceae, Ruminococcaceae and Porphyromonadaceae correlated with metabolic markers. Conclusions Obese adolescents with PCOS and HS have differences in composition of gut microbiota, which correlate with metabolic markers, suggesting a modifying role of gut microbiota in HS and PCOS.
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Affiliation(s)
- Beza Jobira
- Department of Pediatrics, Division of Pediatric Endocrinology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
- Department of Medicine, Division of Infectious Diseases, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
| | - Daniel N. Frank
- Department of Medicine, Division of Infectious Diseases, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
| | - Lori J. Silveira
- Department of Pediatrics, Division of Pediatric Endocrinology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
- Department of Biostatistics and Informatics, Colorado School of Public Health, Aurora, Colorado, United States of America
| | - Laura Pyle
- Department of Pediatrics, Division of Pediatric Endocrinology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
- Department of Biostatistics and Informatics, Colorado School of Public Health, Aurora, Colorado, United States of America
| | - Megan M. Kelsey
- Department of Pediatrics, Division of Pediatric Endocrinology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
- Center for Women’s Health Research, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
| | - Yesenia Garcia-Reyes
- Department of Pediatrics, Division of Pediatric Endocrinology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
| | - Charles E. Robertson
- Department of Medicine, Division of Infectious Diseases, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
| | - Diana Ir
- Department of Medicine, Division of Infectious Diseases, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
| | - Kristen J. Nadeau
- Department of Pediatrics, Division of Pediatric Endocrinology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
- Center for Women’s Health Research, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
| | - Melanie Cree-Green
- Department of Pediatrics, Division of Pediatric Endocrinology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
- Center for Women’s Health Research, University of Colorado Anschutz Medical Campus, Aurora, Colorado, United States of America
- * E-mail:
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22
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Schellekens H, Torres-Fuentes C, van de Wouw M, Long-Smith CM, Mitchell A, Strain C, Berding K, Bastiaanssen TFS, Rea K, Golubeva AV, Arboleya S, Verpaalen M, Pusceddu MM, Murphy A, Fouhy F, Murphy K, Ross P, Roy BL, Stanton C, Dinan TG, Cryan JF. Bifidobacterium longum counters the effects of obesity: Partial successful translation from rodent to human. EBioMedicine 2020; 63:103176. [PMID: 33349590 PMCID: PMC7838052 DOI: 10.1016/j.ebiom.2020.103176] [Citation(s) in RCA: 68] [Impact Index Per Article: 13.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/06/2020] [Revised: 10/13/2020] [Accepted: 12/03/2020] [Indexed: 02/07/2023] Open
Abstract
Background The human gut microbiota has emerged as a key factor in the development of obesity. Certain probiotic strains have shown anti-obesity effects. The objective of this study was to investigate whether Bifidobacterium longum APC1472 has anti-obesity effects in high-fat diet (HFD)-induced obese mice and whether B. longum APC1472 supplementation reduces body-mass index (BMI) in healthy overweight/obese individuals as the primary outcome. B. longum APC1472 effects on waist-to-hip ratio (W/H ratio) and on obesity-associated plasma biomarkers were analysed as secondary outcomes. Methods B. longum APC1472 was administered to HFD-fed C57BL/6 mice in drinking water for 16 weeks. In the human intervention trial, participants received B. longum APC1472 or placebo supplementation for 12 weeks, during which primary and secondary outcomes were measured at the beginning and end of the intervention. Findings B. longum APC1472 supplementation was associated with decreased bodyweight, fat depots accumulation and increased glucose tolerance in HFD-fed mice. While, in healthy overweight/obese adults, the supplementation of B. longum APC1472 strain did not change primary outcomes of BMI (0.03, 95% CI [-0.4, 0.3]) or W/H ratio (0.003, 95% CI [-0.01, 0.01]), a positive effect on the secondary outcome of fasting blood glucose levels was found (-0.299, 95% CI [-0.44, -0.09]). Interpretation This study shows a positive translational effect of B. longum APC1472 on fasting blood glucose from a preclinical mouse model of obesity to a human intervention study in otherwise healthy overweight and obese individuals. This highlights the promising potential of B. longum APC1472 to be developed as a valuable supplement in reducing specific markers of obesity. Funding This research was funded in part by Science Foundation Ireland in the form of a Research Centre grant (SFI/12/RC/2273) to APC Microbiome Ireland and by a research grant from Cremo S.A.
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Affiliation(s)
- Harriët Schellekens
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland.
| | | | | | | | - Avery Mitchell
- Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
| | - Conall Strain
- Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
| | - Kirsten Berding
- APC Microbiome Ireland, University College Cork, Cork, Ireland
| | - Thomaz F S Bastiaanssen
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland
| | - Kieran Rea
- APC Microbiome Ireland, University College Cork, Cork, Ireland
| | - Anna V Golubeva
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland
| | - Silvia Arboleya
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
| | - Mathieu Verpaalen
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland
| | | | - Amy Murphy
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
| | - Fiona Fouhy
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
| | - Kiera Murphy
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
| | - Paul Ross
- APC Microbiome Ireland, University College Cork, Cork, Ireland; College of Science Engineering & Food Science, University College Cork, Cork, Ireland
| | | | - Catherine Stanton
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
| | - Timothy G Dinan
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Dept of Psychiatry and Behavioural Neuroscience, University College Cork, Cork, Ireland
| | - John F Cryan
- APC Microbiome Ireland, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland
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23
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Selber-Hnatiw S, Sultana T, Tse W, Abdollahi N, Abdullah S, Al Rahbani J, Alazar D, Alrumhein NJ, Aprikian S, Arshad R, Azuelos JD, Bernadotte D, Beswick N, Chazbey H, Church K, Ciubotaru E, D'Amato L, Del Corpo T, Deng J, Di Giulio BL, Diveeva D, Elahie E, Frank JGM, Furze E, Garner R, Gibbs V, Goldberg-Hall R, Goldman CJ, Goltsios FF, Gorjipour K, Grant T, Greco B, Guliyev N, Habrich A, Hyland H, Ibrahim N, Iozzo T, Jawaheer-Fenaoui A, Jaworski JJ, Jhajj MK, Jones J, Joyette R, Kaudeer S, Kelley S, Kiani S, Koayes M, Kpata AJAAL, Maingot S, Martin S, Mathers K, McCullogh S, McNamara K, Mendonca J, Mohammad K, Momtaz SA, Navaratnarajah T, Nguyen-Duong K, Omran M, Ortiz A, Patel A, Paul-Cole K, Plaisir PA, Porras Marroquin JA, Prevost A, Quach A, Rafal AJ, Ramsarun R, Rhnima S, Rili L, Safir N, Samson E, Sandiford RR, Secondi S, Shahid S, Shahroozi M, Sidibé F, Smith M, Sreng Flores AM, Suarez Ybarra A, Sénéchal R, Taifour T, Tang L, Trapid A, Tremblay Potvin M, Wainberg J, Wang DN, Weissenberg M, White A, Wilkinson G, Williams B, Wilson JR, Zoppi J, Zouboulakis K, Gamberi C. Metabolic networks of the human gut microbiota. MICROBIOLOGY-SGM 2020; 166:96-119. [PMID: 31799915 DOI: 10.1099/mic.0.000853] [Citation(s) in RCA: 21] [Impact Index Per Article: 4.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
Abstract
The human gut microbiota controls factors that relate to human metabolism with a reach far greater than originally expected. Microbial communities and human (or animal) hosts entertain reciprocal exchanges between various inputs that are largely controlled by the host via its genetic make-up, nutrition and lifestyle. The composition of these microbial communities is fundamental to supply metabolic capabilities beyond those encoded in the host genome, and contributes to hormone and cellular signalling that support the dynamic adaptation to changes in food availability, environment and organismal development. Poor functional exchange between the microbial communities and their human host is associated with dysbiosis, metabolic dysfunction and disease. This review examines the biology of the dynamic relationship between the reciprocal metabolic state of the microbiota-host entity in balance with its environment (i.e. in healthy states), the enzymatic and metabolic changes associated with its imbalance in three well-studied diseases states such as obesity, diabetes and atherosclerosis, and the effects of bariatric surgery and exercise.
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Affiliation(s)
- Susannah Selber-Hnatiw
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Tarin Sultana
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - W Tse
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Niki Abdollahi
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Sheyar Abdullah
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Jalal Al Rahbani
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Diala Alazar
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Nekoula Jean Alrumhein
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Saro Aprikian
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Rimsha Arshad
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Jean-Daniel Azuelos
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Daphney Bernadotte
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Natalie Beswick
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Hana Chazbey
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Kelsey Church
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Emaly Ciubotaru
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Lora D'Amato
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Tavia Del Corpo
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Jasmine Deng
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Briana Laura Di Giulio
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Diana Diveeva
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Elias Elahie
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - James Gordon Marcel Frank
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Emma Furze
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Rebecca Garner
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Vanessa Gibbs
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Rachel Goldberg-Hall
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Chaim Jacob Goldman
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Fani-Fay Goltsios
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Kevin Gorjipour
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Taylor Grant
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Brittany Greco
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Nadir Guliyev
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Andrew Habrich
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Hillary Hyland
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Nabila Ibrahim
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Tania Iozzo
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Anastasia Jawaheer-Fenaoui
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Julia Jane Jaworski
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Maneet Kaur Jhajj
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Jermaine Jones
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Rodney Joyette
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Samad Kaudeer
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Shawn Kelley
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Shayesteh Kiani
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Marylin Koayes
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | | | - Shannon Maingot
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Sara Martin
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Kelly Mathers
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Sean McCullogh
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Kelly McNamara
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - James Mendonca
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Karamat Mohammad
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Sharara Arezo Momtaz
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Thiban Navaratnarajah
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Kathy Nguyen-Duong
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Mustafa Omran
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Angela Ortiz
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Anjali Patel
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Kahlila Paul-Cole
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Paul-Arthur Plaisir
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | | | - Ashlee Prevost
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Angela Quach
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Aries John Rafal
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Rewaparsad Ramsarun
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Sami Rhnima
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Lydia Rili
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Naomi Safir
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Eugenie Samson
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Rebecca Rose Sandiford
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Stefano Secondi
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Stephanie Shahid
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Mojdeh Shahroozi
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Fily Sidibé
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Megan Smith
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Alina Maria Sreng Flores
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Anabel Suarez Ybarra
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Rebecca Sénéchal
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Tarek Taifour
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Lawrence Tang
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Adam Trapid
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Maxim Tremblay Potvin
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Justin Wainberg
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Dani Ni Wang
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Mischa Weissenberg
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Allison White
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Gabrielle Wilkinson
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Brittany Williams
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Joshua Roth Wilson
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Johanna Zoppi
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Katerina Zouboulakis
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
| | - Chiara Gamberi
- Biology Department, Concordia University, 7141 Sherbrooke St W, SP-375-09 Montreal, Quebec, H4B 1R6, Canada
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Gierse LC, Meene A, Schultz D, Schwaiger T, Karte C, Schröder C, Wang H, Wünsche C, Methling K, Kreikemeyer B, Fuchs S, Bernhardt J, Becher D, Lalk M, Study Group K, Urich T, Riedel K. A Multi-Omics Protocol for Swine Feces to Elucidate Longitudinal Dynamics in Microbiome Structure and Function. Microorganisms 2020; 8:microorganisms8121887. [PMID: 33260576 PMCID: PMC7760263 DOI: 10.3390/microorganisms8121887] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/04/2020] [Revised: 11/03/2020] [Accepted: 11/27/2020] [Indexed: 12/19/2022] Open
Abstract
Swine are regarded as promising biomedical models, but the dynamics of their gastrointestinal microbiome have been much less investigated than that of humans or mice. The aim of this study was to establish an integrated multi-omics protocol to investigate the fecal microbiome of healthy swine. To this end, a preparation and analysis protocol including integrated sample preparation for meta-omics analyses of deep-frozen feces was developed. Subsequent data integration linked microbiome composition with function, and metabolic activity with protein inventories, i.e., 16S rRNA data and expressed proteins, and identified proteins with corresponding metabolites. 16S rRNA gene amplicon and metaproteomics analyses revealed a fecal microbiome dominated by Prevotellaceae, Lactobacillaceae, Lachnospiraceae, Ruminococcaceae and Clostridiaceae. Similar microbiome compositions in feces and colon, but not ileum samples, were observed, showing that feces can serve as minimal-invasive proxy for porcine colon microbiomes. Longitudinal dynamics in composition, e.g., temporal decreased abundance of Lactobacillaceae and Streptococcaceae during the experiment, were not reflected in microbiome function. Instead, metaproteomics and metabolomics showed a rather stable functional state, as evident from short-chain fatty acids (SCFA) profiles and associated metaproteome functions, pointing towards functional redundancy among microbiome constituents. In conclusion, our pipeline generates congruent data from different omics approaches on the taxonomy and functionality of the intestinal microbiome of swine.
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Affiliation(s)
- Laurin Christopher Gierse
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
| | - Alexander Meene
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
| | - Daniel Schultz
- Institute of Biochemistry, University of Greifswald, Felix-Hausdorff-Str. 4, 17489 Greifswald, Germany; (D.S.); (K.M.); (M.L.)
| | - Theresa Schwaiger
- Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Südufer 10, 17493 Greifswald, Germany; (T.S.); (C.K.); (C.S.)
| | - Claudia Karte
- Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Südufer 10, 17493 Greifswald, Germany; (T.S.); (C.K.); (C.S.)
| | - Charlotte Schröder
- Friedrich-Loeffler-Institut, Greifswald-Insel Riems, Südufer 10, 17493 Greifswald, Germany; (T.S.); (C.K.); (C.S.)
| | - Haitao Wang
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
| | - Christine Wünsche
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
| | - Karen Methling
- Institute of Biochemistry, University of Greifswald, Felix-Hausdorff-Str. 4, 17489 Greifswald, Germany; (D.S.); (K.M.); (M.L.)
| | - Bernd Kreikemeyer
- Institute for Medical Microbiology, Virology and Hygiene, Rostock University Medical Centre, Schillingallee 70, 18055 Rostock, Germany;
| | - Stephan Fuchs
- Division of Nosocomial Pathogens and Antibiotic Resistance, Robert Koch Institute Wernigerode, Burgstraße 37, 38855 Wernigerode, Germany;
| | - Jörg Bernhardt
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
| | - Dörte Becher
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
| | - Michael Lalk
- Institute of Biochemistry, University of Greifswald, Felix-Hausdorff-Str. 4, 17489 Greifswald, Germany; (D.S.); (K.M.); (M.L.)
| | | | - Tim Urich
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
- Correspondence: (T.U.); (K.R.); Tel.: +49-3834-420-5904 (T.U.); +49-3834-420-5900 (K.R.)
| | - Katharina Riedel
- Institute of Microbiology, University of Greifswald, Felix-Hausdorff-Str. 8, 17489 Greifswald, Germany; (L.C.G.); (A.M.); (H.W.); (C.W.); (J.B.); (D.B.)
- Correspondence: (T.U.); (K.R.); Tel.: +49-3834-420-5904 (T.U.); +49-3834-420-5900 (K.R.)
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Bhuta R, Nieder M, Jubelirer T, Ladas EJ. The Gut Microbiome and Pediatric Cancer: Current Research and Gaps in Knowledge. J Natl Cancer Inst Monogr 2020; 2019:169-173. [PMID: 31532533 DOI: 10.1093/jncimonographs/lgz026] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/28/2019] [Revised: 07/05/2019] [Accepted: 07/08/2019] [Indexed: 12/12/2022] Open
Abstract
The human microbiome consists of trillions of microbial cells that interact with one another and the human host to play a clinically significant role in health and disease. Gut microbial changes have been identified in cancer pathogenesis, at disease diagnosis, during therapy, and even long after completion of treatment. Alterations in the gut microbiome have been linked to treatment-related toxicity and potential long-term morbidity and mortality in children with cancer. Such alterations are plausible given immune modulation due to disease as well as exposure to cytotoxic chemotherapy, infections, and antibiotics. The following review presents our current scientific understanding on the role of the gut microbiome in pediatric cancer, identifies gaps in knowledge, and suggests future research goals.
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Affiliation(s)
- Roma Bhuta
- Division of Pediatric Hematology-Oncology, Hasbro Children's Hospital, The Warren Alpert Medical School of Brown University, Providence, RI
| | - Michael Nieder
- Blood and Marrow Transplant and Cellular Immunotherapy, Moffitt Cancer Center, University of South Florida College of Medicine, Tampa, FL
| | - Tracey Jubelirer
- Division of Oncology, The Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine, Philadelphia, PA
| | - Elena J Ladas
- Division of Hematology/Oncology/Stem Cell Transplant in the Department of Pediatrics (in Epidemiology and in the Institute of Human Nutrition) at the, Columbia University Medical Center, New York, NY
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26
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Abou-Kassem DE, Elsadek MF, Abdel-Moneim AE, Mahgoub SA, Elaraby GM, Taha AE, Elshafie MM, Alkhawtani DM, Abd El-Hack ME, Ashour EA. Growth, carcass characteristics, meat quality, and microbial aspects of growing quail fed diets enriched with two different types of probiotics (Bacillus toyonensis and Bifidobacterium bifidum). Poult Sci 2020; 100:84-93. [PMID: 33357710 PMCID: PMC7772674 DOI: 10.1016/j.psj.2020.04.019] [Citation(s) in RCA: 33] [Impact Index Per Article: 6.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/05/2019] [Revised: 04/07/2020] [Accepted: 04/12/2020] [Indexed: 12/23/2022] Open
Abstract
The present investigation aimed to explore the impact of dietary graded levels of 2 types of probiotic bacteria (Bacillus toyonensis [BT] and Bifidobacterium bifidum [BB]) on growth, carcass traits, meat quality, and bacteriology of growing Japanese quail reared under the cage system. One thousand three hundred sixty Japanese quail day-old chicks were randomly divided into 10 groups (8 replicates each). Birds were fed a basal diet (control, T1) and the basal diet plus 0.05, 0.075, 0.10, and 0.125% BT (T2, T3, T4, and T5, respectively), 0.10% BB (T6), and the same previous doses of BT plus 0.05% BB (T7, T8, T9, and T10, respectively). Results showed a significant (P < 0.001) increase in final BW and weight gain because of probiotic supplementation (except T2 for weight gain). Both feed intake and feed conversion ratio did not differ during the overall experimental period (1–42 D of age) except feed intake that was reduced in T2 and increased in T5 and T9 groups. All carcass traits studied were significantly (P < 0.01) affected by probiotics, and the combination between BT and BB in group T8 increased all studied parameters as compared with the other treatment groups. The quail meat color of redness a∗ and L∗ values, thiobarbituric content, cooking loss, proteolysis, and total coliform were decreased (P < 0.001) by probiotic treatment. In general, supplementing BT, BB, or their combination to the basal diet delayed the proliferation of pathogenic bacteria in the diet and intestine. Using BT and BB as feed supplements enhanced growth performance and meat quality of quails as well as diminished pathogenic bacteria proliferation in their diet and intestine. As per our results, we can recommend the application of T5 and T8 to T10 levels for the best performance, carcass traits, and meat quality of growing quails.
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Affiliation(s)
- D E Abou-Kassem
- Animal and Poultry Production Department, Faculty of Technology and Development, Zagazig University, Zagazig, Egypt
| | - M F Elsadek
- Department of Community Health Sciences, College of Applied Medical Sciences, King Saud University, Saudi Arabia; Nutrition and Food Science Department, Helwan University, Helwan, Egypt.
| | - A E Abdel-Moneim
- Biological Application Department, Nuclear Research Center, Atomic Energy Authority, Abu-Zaabal 13759, Egypt
| | - S A Mahgoub
- Department of Microbiology, Faculty of Agriculture, Zagazig University, Zagazig 44111, Egypt
| | - G M Elaraby
- Food Science Department, Faculty of Agriculture, Zagazig University, Zagazig, Egypt
| | - A E Taha
- Department of Animal Husbandry and Animal Wealth Development, Faculty of Veterinary Medicine, Alexandria University, Rasheed, Edfina 22758, Egypt
| | - M M Elshafie
- Department of Community Health Sciences, College of Applied Medical Sciences, King Saud University, Saudi Arabia
| | - D M Alkhawtani
- Department of Community Health Sciences, College of Applied Medical Sciences, King Saud University, Saudi Arabia
| | - M E Abd El-Hack
- Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt.
| | - E A Ashour
- Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt
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Microbial dysbiosis-induced obesity: role of gut microbiota in homoeostasis of energy metabolism. Br J Nutr 2020; 123:1127-1137. [PMID: 32008579 DOI: 10.1017/s0007114520000380] [Citation(s) in RCA: 223] [Impact Index Per Article: 44.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/04/2023]
Abstract
The global obesity epidemic has necessitated the search for better intervention strategies including the exploitation of the health benefits of some gut microbiota and their metabolic products. Therefore, we examined the gut microbial composition and mechanisms of interaction with the host in relation to homoeostatic energy metabolism and pathophysiology of dysbiosis-induced metabolic inflammation and obesity. We also discussed the eubiotic, health-promoting effects of probiotics and prebiotics as well as epigenetic modifications associated with gut microbial dysbiosis and risk of obesity. High-fat/carbohydrate diet programmes the gut microbiota to one predominated by Firmicutes (Clostridium), Prevotella and Methanobrevibacter but deficient in beneficial genera/species such as Bacteroides, Bifidobacterium, Lactobacillus and Akkermansia. Altered gut microbiota is associated with decreased expression of SCFA that maintain intestinal epithelial barrier integrity, reduce bacterial translocation and inflammation and increase expression of hunger-suppressing hormones. Reduced amounts of beneficial micro-organisms also inhibit fasting-induced adipocyte factor expression leading to dyslipidaemia. A low-grade chronic inflammation (metabolic endotoxaemia) ensues which culminates in obesity and its co-morbidities. The synergy of high-fat diet and dysbiotic gut microbiota initiates a recipe that epigenetically programmes the host for increased adiposity and poor glycaemic control. Interestingly, these obesogenic mechanistic pathways that are transmittable from one generation to another can be modulated through the administration of probiotics, prebiotics and synbiotics. Though the influence of gut microbiota on the risk of obesity and several intervention strategies have been extensively demonstrated in animal models, application in humans still requires further robust investigation.
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28
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Miranda VPN, dos Santos Amorim PR, Bastos RR, de Faria ER, de Castro Moreira ME, do Carmo Castro Franceschini S, do Carmo Gouveia Peluzio M, de Luces Fortes Ferreira CL, Priore SE. Abundance of Gut Microbiota, Concentration of Short-Chain Fatty Acids, and Inflammatory Markers Associated with Elevated Body Fat, Overweight, and Obesity in Female Adolescents. Mediators Inflamm 2019; 2019:7346863. [PMID: 31933541 PMCID: PMC6942879 DOI: 10.1155/2019/7346863] [Citation(s) in RCA: 23] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/16/2019] [Revised: 10/02/2019] [Accepted: 10/16/2019] [Indexed: 02/07/2023] Open
Abstract
BACKGROUND AND AIMS Overweight is ever more prevalent in the pediatric population, and this cardiometabolic factor can be associated with inflammatory markers, gut microbiota composition, and short-chain fatty acid (SCFA) concentrations. The aim of this study is to evaluate to what extent the abundance of gut microbiota phyla, SCFA concentrations, and inflammatory markers are associated with elevated body fat percentage (BF%), overweight, and obesity in female adolescents. METHODS An experimental and comparative study was conducted with 96 girls 14 to 19 years old. They were divided into 3 groups: G1-eutrophic (EUT) and adequate BF%; G2-EUT and high BF%; and G3-overweight (OW) or obese (OB) and high BF%. Waist circumference (WC), waist to height ratio (WtHR), and neck circumference (NC) were analyzed as indicators of central visceral adiposity. The BF% was evaluated by DEXA equipment. A food frequency questionnaire was used to evaluate the main types of food consumed in a week. The abundance of the Firmicutes, Bacteroidetes, and Proteobacteria phyla was measured by real-time polymerase chain reaction (RT-qPCR), and the SFCA concentrations (acetic, butyric, and propionic) were determined by high-performance liquid chromatography (HPLC). The inflammatory markers leptin, tumor necrosis factor-alpha, interleukin-6, and high-sensitivity C-reactive protein (hs-CRP) were assessed. RESULTS Female adolescents in groups G2 and G3 had greater central visceral adiposity and leptin concentration than those in group G1. No association was found between gut microbiota phyla abundance and SFCA concentrations in any of the groups. WC and frequency of consumption of oily and fatty foods were associated with Firmicutes abundance and SFCA concentrations. Girls with high WC also had the greatest leptin (p < 0.001) and hs-CRP (p = 0.035) concentrations. CONCLUSIONS Inflammatory markers showed association with increased BMI and high BF% in female adolescents. The abundance of Firmicutes was associated with WC and NC, but not with BMI classification or BF%. Specifically, WC and the consumption of oils and fats showed correlation with SCFA concentrations. Different anthropometric indicators, such as NC and WC, should be incorporated into the clinical evaluation of the nutritional status of individuals in the adolescent population.
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Affiliation(s)
- Valter Paulo Neves Miranda
- Department of Nutrition and Health and Department of Physical Education, Universidade Federal de Viçosa, Minas Gerais CEP 36570-900, Brazil
| | | | - Ronaldo Rocha Bastos
- Department of Statistics-ICE, Universidade Federal de Juiz de Fora, Juiz de Fora MG, Brazil CEP 36036-330
| | - Eliane Rodrigues de Faria
- Department of Nutrition, Universidade Federal de Juiz de Fora, Juiz de Fora, MG, Brazil CEP 36036-900
| | | | | | | | | | - Silvia Eloiza Priore
- Department of Nutrition and Health, Universidade Federal de Viçosa, Minas Gerais CEP 36570-900, Brazil
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Steatosis and gut microbiota dysbiosis induced by high-fat diet are reversed by 1-week chow diet administration. Nutr Res 2019; 71:72-88. [PMID: 31757631 DOI: 10.1016/j.nutres.2019.09.004] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/24/2019] [Revised: 08/26/2019] [Accepted: 09/13/2019] [Indexed: 12/12/2022]
Abstract
Many studies have recently shown that diet and its impact on gut microbiota are closely related to obesity and metabolic diseases including nonalcoholic fatty liver disease. Gut microbiota may be an important intermediate link, causing gastrointestinal and metabolic diseases under the influence of changes in diet and genetic predisposition. The aim of this study was to assess the reversibility of liver phenotype in parallel with exploring the resilience of the mice gut microbiota by switching high-fat diet (HFD) to chow diet (CD). Mice were fed an HF for 8 weeks. A part of the mice was euthanized, whereas the rest were then fed a CD. These mice were euthanized after 3 and 7 days of feeding with CD, respectively. Gut microbiota composition, serum parameters, and liver morphology were assessed. Eight weeks of HFD treatment induced marked liver steatosis in mice with a perturbed microbiome. Interestingly, only 7 days of CD was enough to recover the liver to a normal status, whereas the microbiome was accordingly reshaped to a close to initial pattern. The abundance of some of the bacteria including Prevotella, Parabacteroides, Lactobacillus, and Allobaculum was reversible upon diet change from HFD to CD. This suggests that microbiome modifications contribute to the metabolic effects of HFD feeding and that restoration of a normal microbiota may lead to improvement of the liver phenotype. In conclusion, we found that steatosis and gut microbiota dysbiosis induced by 8 weeks of high-fat diet can be reversed by 1 week of chow diet administration, and we identified gut bacteria associated with the metabolic phenotype.
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30
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Koopman N, Molinaro A, Nieuwdorp M, Holleboom AG. Review article: can bugs be drugs? The potential of probiotics and prebiotics as treatment for non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2019; 50:628-639. [PMID: 31373710 DOI: 10.1111/apt.15416] [Citation(s) in RCA: 41] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/20/2019] [Revised: 05/06/2019] [Accepted: 06/23/2019] [Indexed: 12/11/2022]
Abstract
BACKGROUND Non-alcoholic fatty liver disease (NAFLD) has become the most common chronic liver condition. A major current research effort is ongoing to find potential strategies to treat NAFLD-non-alcoholic steatohepatitis (NASH), with special attention to the gut microbiota. Multiple animal studies and pilot clinical trials are assessing different gut microbiota modulating strategies such as faecal microbiota transplantation, antibiotics, probiotics, prebiotics and synbiotics. AIM To review the role of microbiota in NAFLD-NASH and determine whether pro- and prebiotics have potential as treatment METHODS: Information was obtained from critically reviewing literature on PubMed on targeting the gut microbiota in NAFLD. Search terms included NAFLD, NASH, non-alcoholic fatty liver disease, steatohepatitis; combined with microbiome, microbiota, gut bacteria, probiotics and prebiotics. RESULTS Animal studies and the first emerging studies in humans show promising results for both the common probiotics Lactobacillus, Bifidobacterium and Streptococci as for short chain fatty acid (SCFA) butyrate-producing bacteria. Also, prebiotics have positive effects on different mechanisms underlying NAFLD-NASH. CONCLUSIONS The most promising strategies thus far developed to alter the microbiome in NAFLD-NASH are probiotics and prebiotics. However, pre- and probiotic treatment of NAFLD-NASH is relatively new and still under development. Actual understanding of the involved mechanisms is lacking and changes in the intestinal microbiota composition after treatment are rarely measured. Furthermore, large clinical trials with comparative endpoints are unavailable. Personalised treatment based on metagenomics gut microbiota analysis will probably be part of the future diagnosis and treatment of NAFLD-NASH.
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Affiliation(s)
- Nienke Koopman
- Department of Molecular Biology and Microbial Food Safety, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands
| | - Antonio Molinaro
- Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
| | - Max Nieuwdorp
- Vascular Medicine, Amsterdam University Medical Center, Amsterdam, The Netherlands
| | - Adriaan G Holleboom
- Vascular Medicine, Amsterdam University Medical Center, Amsterdam, The Netherlands
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31
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Carson TL, Little RB, Townsend S. Preliminary feasibility for recruiting and retaining black and white females to provide fecal samples for longitudinal research. Gut Pathog 2019; 11:43. [PMID: 31462930 PMCID: PMC6710875 DOI: 10.1186/s13099-019-0324-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/04/2019] [Accepted: 08/14/2019] [Indexed: 11/24/2022] Open
Abstract
As the associations between the gut microbiota and numerous health outcomes become more evident, it is important to conduct longitudinal microbiome research to advance the field beyond the identification of associations. It is also necessary to include individuals who have historically been underrepresented in biomedical research in longitudinal microbiome studies to better understand and eliminate racial/ethnic health disparities. This paper describes our experiences in recruiting and retaining participants for an ongoing, longitudinal microbiome study for which the main results will be reported at a later time. This article provides preliminary evidence of the feasibility of recruiting and retaining a racially diverse sample of females (97% completion for invited participants) for longitudinal microbiome research.
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Affiliation(s)
- Tiffany L Carson
- 1Division of Preventive Medicine, Department of Medicine, School of Medicine, University of Alabama at Birmingham, 1720 2nd Avenue South MT 639, Birmingham, AL 35294-4410 USA.,2Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham, AL USA
| | - Rebecca B Little
- 3Division of Preventive Medicine, Department of Medicine, School of Medicine, University of Alabama at Birmingham, 1720 2nd Avenue South MT 518K, Birmingham, AL 35294-4410 USA
| | - Sh'Nese Townsend
- 4Division of Preventive Medicine, Department of Medicine, School of Medicine, University of Alabama at Birmingham, 1720 2nd Avenue South MT 518E, Birmingham, AL 35294-4410 USA
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32
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The Short-Chain Fatty Acid Acetate in Body Weight Control and Insulin Sensitivity. Nutrients 2019; 11:nu11081943. [PMID: 31426593 PMCID: PMC6723943 DOI: 10.3390/nu11081943] [Citation(s) in RCA: 348] [Impact Index Per Article: 58.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/08/2019] [Revised: 08/08/2019] [Accepted: 08/15/2019] [Indexed: 02/06/2023] Open
Abstract
The interplay of gut microbiota, host metabolism, and metabolic health has gained increased attention. Gut microbiota may play a regulatory role in gastrointestinal health, substrate metabolism, and peripheral tissues including adipose tissue, skeletal muscle, liver, and pancreas via its metabolites short-chain fatty acids (SCFA). Animal and human data demonstrated that, in particular, acetate beneficially affects host energy and substrate metabolism via secretion of the gut hormones like glucagon-like peptide-1 and peptide YY, which, thereby, affects appetite, via a reduction in whole-body lipolysis, systemic pro-inflammatory cytokine levels, and via an increase in energy expenditure and fat oxidation. Thus, potential therapies to increase gut microbial fermentation and acetate production have been under vigorous scientific scrutiny. In this review, the relevance of the colonically and systemically most abundant SCFA acetate and its effects on the previously mentioned tissues will be discussed in relation to body weight control and glucose homeostasis. We discuss in detail the differential effects of oral acetate administration (vinegar intake), colonic acetate infusions, acetogenic fiber, and acetogenic probiotic administrations as approaches to combat obesity and comorbidities. Notably, human data are scarce, which highlights the necessity for further human research to investigate acetate’s role in host physiology, metabolic, and cardiovascular health.
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33
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Erliana UD, Fly AD. The Function and Alteration of Immunological Properties in Human Milk of Obese Mothers. Nutrients 2019; 11:nu11061284. [PMID: 31174304 PMCID: PMC6627488 DOI: 10.3390/nu11061284] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/29/2019] [Revised: 05/28/2019] [Accepted: 06/01/2019] [Indexed: 01/08/2023] Open
Abstract
Maternal obesity is associated with metabolic changes in mothers and higher risk of obesity in the offspring. Obesity in breastfeeding mothers appears to influence human milk production as well as the quality of human milk. Maternal obesity is associated with alteration of immunological factors concentrations in the human milk, such as C-reactive protein (CRP), leptin, IL-6, insulin, TNF-Alpha, ghrelin, adiponectin, and obestatin. Human milk is considered a first choice for infant nutrition due to the complete profile of macro nutrients, micro nutrients, and immunological properties. It is essential to understand how maternal obesity influences immunological properties of human milk because alterations could impact the nutrition status and health of the infant. This review summarizes the literature regarding the impact of maternal obesity on the concentration of particular immunological properties in the human milk.
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Affiliation(s)
- Ummu D Erliana
- Indiana University Bloomington School of Public Health, Bloomington, IN 47405, USA.
| | - Alyce D Fly
- Indiana University Bloomington School of Public Health, Bloomington, IN 47405, USA.
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34
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Wang X, Pan Q, Ma F, Li P, Xu B, Chen C. Amelioration of Growth Performance, Lipid Accumulation, and Intestinal Health in Mice by a Cooked Mixture of Lean Meat and Resistant Starch. Mol Nutr Food Res 2019; 63:e1801364. [DOI: 10.1002/mnfr.201801364] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/14/2018] [Revised: 02/18/2019] [Indexed: 12/21/2022]
Affiliation(s)
- Xi‐xi Wang
- School of Food and Biological EngineeringHefei University of Technology Hefei 230009 Anhui P. R. China
- Engineering Research Center of Bioprocess from Ministry of EducationHefei University of Technology Hefei 230009 Anhui P. R. China
| | - Qiong Pan
- School of Food and Biological EngineeringHefei University of Technology Hefei 230009 Anhui P. R. China
- Engineering Research Center of Bioprocess from Ministry of EducationHefei University of Technology Hefei 230009 Anhui P. R. China
| | - Fei Ma
- School of Food and Biological EngineeringHefei University of Technology Hefei 230009 Anhui P. R. China
- Engineering Research Center of Bioprocess from Ministry of EducationHefei University of Technology Hefei 230009 Anhui P. R. China
| | - Pei‐jun Li
- School of Food and Biological EngineeringHefei University of Technology Hefei 230009 Anhui P. R. China
- Engineering Research Center of Bioprocess from Ministry of EducationHefei University of Technology Hefei 230009 Anhui P. R. China
- Key Laboratory on Deep Processing of Agricultural Products for Anhui Province Hefei 230009 Anhui P. R. China
| | - Bao‐cai Xu
- School of Food and Biological EngineeringHefei University of Technology Hefei 230009 Anhui P. R. China
- Engineering Research Center of Bioprocess from Ministry of EducationHefei University of Technology Hefei 230009 Anhui P. R. China
- Key Laboratory on Deep Processing of Agricultural Products for Anhui Province Hefei 230009 Anhui P. R. China
| | - Cong‐gui Chen
- School of Food and Biological EngineeringHefei University of Technology Hefei 230009 Anhui P. R. China
- Engineering Research Center of Bioprocess from Ministry of EducationHefei University of Technology Hefei 230009 Anhui P. R. China
- Key Laboratory on Deep Processing of Agricultural Products for Anhui Province Hefei 230009 Anhui P. R. China
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Maghsoodi N, Shaw N, Cross GF, Alaghband-Zadeh J, Wierzbicki AS, Pinkney J, Millward A, Vincent RP. Bile acid metabolism is altered in those with insulin resistance after gestational diabetes mellitus. Clin Biochem 2019; 64:12-17. [DOI: 10.1016/j.clinbiochem.2018.11.016] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/02/2018] [Revised: 11/02/2018] [Accepted: 11/29/2018] [Indexed: 12/28/2022]
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Ye S, Bhattacharjee M, Siemann E. Thermal Tolerance in Green Hydra: Identifying the Roles of Algal Endosymbionts and Hosts in a Freshwater Holobiont Under Stress. MICROBIAL ECOLOGY 2019; 77:537-545. [PMID: 30613848 DOI: 10.1007/s00248-018-01315-1] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/29/2018] [Accepted: 12/25/2018] [Indexed: 05/23/2023]
Abstract
It has been proposed that holobionts (host-symbiont units) could swap endosymbionts, rapidly alter the hologenome (host plus symbiont genome), and increase their stress tolerance. However, experimental tests of individual and combined contributions of hosts and endosymbionts to holobiont stress tolerance are needed to test this hypothesis. Here, we used six green hydra (Hydra viridissima) strains to tease apart host (hydra) and symbiont (algae) contributions to thermal tolerance. Heat shock experiments with (1) hydra with their original symbionts, (2) aposymbiotic hydra (algae removed), (3) novel associations (a single hydra strain hosting different algae individually), and (4) control hydra (aposymbiotic hydra re-associated with their original algae) showed high variation in thermal tolerance in each group. Relative tolerances of strains were the same within original, aposymbiotic, and control treatments, but reversed in the novel associations group. Aposymbiotic hydra had similar or higher thermal tolerance than hydra with algal symbionts. Selection on the holobiont appears to be stronger than on either partner alone, suggesting endosymbiosis could become an evolutionary trap under climate change. Our results suggest that green hydra thermal tolerance is strongly determined by the host, with a smaller, non-positive role for the algal symbiont. Once temperatures exceed host tolerance limits, swapping symbionts is unlikely to allow these holobionts to persist. Rather, increases in host tolerance through in situ adaptation or migration of pre-adapted host strains appear more likely to increase local thermal tolerance. Overall, our results indicate green hydra is a valuable system for studying aquatic endosymbiosis under changing environmental conditions, and demonstrate how the host and the endosymbiont contribute to holobiont stress tolerance.
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Affiliation(s)
- Siao Ye
- Department of Biosciences, Rice University, 6100 S. Main St., Houston, TX, 77005, USA.
| | | | - Evan Siemann
- Department of Biosciences, Rice University, 6100 S. Main St., Houston, TX, 77005, USA
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Pimentel LL, Fontes AL, Salsinha AS, Cardoso BB, Gomes AM, Rodríguez-Alcalá LM. Microbiological In Vivo Production of CLNA as a Tool in the Regulation of Host Microbiota in Obesity Control. STUDIES IN NATURAL PRODUCTS CHEMISTRY 2019:369-394. [DOI: 10.1016/b978-0-444-64183-0.00010-5] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/05/2025]
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Johny TK, Saidumohamed BE, Sasidharan RS, Bhat SG. Inferences of gut bacterial diversity from next-generation sequencing of 16S rDNA in deep sea blind ray - Benthobatis moresbyi. ACTA ACUST UNITED AC 2018. [DOI: 10.1016/j.egg.2018.07.001] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/17/2022]
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Carson TL, Wang F, Cui X, Jackson BE, Van Der Pol WJ, Lefkowitz EJ, Morrow C, Baskin ML. Associations Between Race, Perceived Psychological Stress, and the Gut Microbiota in a Sample of Generally Healthy Black and White Women: A Pilot Study on the Role of Race and Perceived Psychological Stress. Psychosom Med 2018; 80:640-648. [PMID: 29901485 PMCID: PMC6113071 DOI: 10.1097/psy.0000000000000614] [Citation(s) in RCA: 39] [Impact Index Per Article: 5.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/12/2022]
Abstract
OBJECTIVE Racial health disparities persist among black and white women for colorectal cancer. Understanding racial differences in the gut microbiota and related covariates (e.g., stress) may yield new insight into unexplained colorectal cancer disparities. METHODS Healthy non-Hispanic black or white women (age ≥19 years) provided survey data, anthropometrics, and stool samples. Fecal DNA was collected and isolated from a wipe. Polymerase chain reaction was used to amplify the V4 region of the 16SrRNA gene and 250 bases were sequenced using the MiSeq platform. Microbiome data were analyzed using QIIME. Operational taxonomic unit data were log transformed and normalized. Analyses were conducted using linear models in R Package "limma." RESULTS Fecal samples were analyzed for 80 women (M (SD) age = 39.9 (14.0) years, 47 black, 33 white). Blacks had greater average body mass index (33.3 versus 27.5 kg/m, p < .01) and waist circumference (98.3 versus 86.6 cm, p = .003) than whites. Whites reported more stressful life events (p = .026) and greater distress (p = .052) than blacks. Final models accounted for these differences. There were no significant differences in dietary variables. Unadjusted comparisons revealed no racial differences in alpha diversity. Racial differences were observed in beta diversity and abundance of top 10 operational taxonomic units. Blacks had higher abundances than whites of Faecalibacterium (p = .034) and Bacteroides (p = .038). Stress was associated with abundances of Bifidobacterium. The association between race and Bacteroides (logFC = 1.72, 0 = 0.020) persisted in fully adjusted models. CONCLUSIONS Racial differences in the gut microbiota were observed including higher Bacteroides among blacks. Efforts to cultivate an "ideal" gut microbiota may help reduce colorectal cancer risk.
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Affiliation(s)
- Tiffany L. Carson
- Division of Preventive Medicine, Department of Medicine, School of Medicine, University of Alabama at Birmingham; Birmingham, AL
- Comprehensive Cancer Center, University of Alabama at Birmingham
| | - Fuchenchu Wang
- Department of Biostatistics, School of Public Health, University of Alabama at Birmingham; Birmingham, AL
| | - Xiangqin Cui
- Department of Biostatistics, School of Public Health, University of Alabama at Birmingham; Birmingham, AL
| | - Bradford E. Jackson
- Center for Outcomes Research, JPS Health Network; Fort Worth, TX
- Department of Biostatistics and Epidemiology; UNT Health Science Center, School of Public Health; Fort Worth, TX
| | | | - Elliot J. Lefkowitz
- Center for Clinical and Translational Sciences, University of Alabama at Birmingham
- Department of Microbiology, University of Alabama at Birmingham; Birmingham, AL
| | - Casey Morrow
- Department of Cell, Developmental and Integrative Biology, University of Alabama at Birmingham; Birmingham, AL
| | - Monica L. Baskin
- Division of Preventive Medicine, Department of Medicine, School of Medicine, University of Alabama at Birmingham; Birmingham, AL
- Comprehensive Cancer Center, University of Alabama at Birmingham
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The short-term impact of probiotic consumption on the oral cavity microbiome. Sci Rep 2018; 8:10476. [PMID: 29992994 PMCID: PMC6041349 DOI: 10.1038/s41598-018-28491-x] [Citation(s) in RCA: 35] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/08/2018] [Accepted: 06/22/2018] [Indexed: 12/26/2022] Open
Abstract
The dysbiosis of the oral microbiome is associated with both localized and systemic diseases. Modulating the resident microbial communities by the dietary consumption of probiotics has become an appealing means to promote host health by either restoring host-microbe balance or preventing dysbiosis. Most probiotics strategies target the intestinal microbiome, but little is known about their impact on the oral microbiome. We analyzed here the saliva microbiome from 21 volunteers, longitudinally collected before, during, and after consumption of a commercial probiotic and a standard yoghurt using 16S amplicon sequencing. The alpha diversity of the saliva microbiome had a statistically significant increase (P-value = 0.0011) in one of the groups that consumed the probiotic. The overall structure of the microbiome was however not significantly impacted by the probiotic, although oligotyping analysis revealed that both Streptococci and Lactobacilli present in the probiotic product persisted in the saliva microbiome. In contrast, non-probiotic yoghurt consumption had a lesser impact on the overall diversity and Lactobacillus and Streptococcus persistence. Our results suggest that consumption of commercial probiotics in healthy subjects increase the overall diversity of the oral cavity microbiome in the short term, but such dietary interventions are not able to substantially modify the structure of the microbiome.
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de Almeida CV, Taddei A, Amedei A. The controversial role of Enterococcus faecalis in colorectal cancer. Therap Adv Gastroenterol 2018; 11:1756284818783606. [PMID: 30013618 PMCID: PMC6044108 DOI: 10.1177/1756284818783606] [Citation(s) in RCA: 102] [Impact Index Per Article: 14.6] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/02/2018] [Accepted: 05/17/2018] [Indexed: 02/04/2023] Open
Abstract
Colorectal cancer (CRC) is a complex and widespread disease, currently ranked as the third most frequent cancer worldwide. It is well known that the gut microbiota has an essential role in the initiation and promotion of different cancer types, particularly gastrointestinal tumors. In fact, bacteria can trigger chronic inflammation of the gastric mucosal, which can induce irreversible changes to intestinal epithelial cells, thus predisposing individuals to cancer. Some bacterial strains, such as Helicobacter pylori, Streptococcus bovis, Bacteroides fragilis, Clostridium septicum and Fusobacterium spp. have a well established role in CRC development. However, the role of Enterococcus faecalis still remains controversial. While part of the literature suggests a harmful role, other papers reported E. faecalis as an important probiotic microorganism, with great applicability in food products. In this review we have examined the vast majority of published data about E. faecalis either in CRC development or concerning its protective role. Our analysis should provide some answers regarding the controversial role of E. faecalis in CRC.
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Affiliation(s)
| | - Antonio Taddei
- Department of Surgery and Translational
Medicine, University of Florence, Florence, Italy
| | - Amedeo Amedei
- Department of Experimental and Clinical
Medicine, University of Florence, Viale Pieraccini, 6, 50139 Florence,
Italy
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The impact of supplementation with dietary fibers on weight loss: A systematic review of randomised controlled trials. ACTA ACUST UNITED AC 2018. [DOI: 10.1016/j.bcdf.2017.07.010] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/24/2022]
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Abstract
The obesity epidemic continues to escalate each year in the United States more than anywhere else in the world. The existing pharmaceutical and other nonsurgical treatments for morbid obesity produce suboptimal physiologic outcomes compared with those of Roux-en-Y gastric bypass (RYGB) surgery. RYGB has been the gold standard of bariatric surgery because the beneficial long-term outcomes, which include sustainable weight loss and type 2 diabetes mellitus (T2DM) resolution, are far superior to those obtained with other bariatric surgeries. However, the current understanding of RYGB's mechanisms of actions remains limited and incomplete. There is an urgent need to understand these mechanisms as gaining this knowledge may lead to the development of innovative and less invasive procedures and/or medical devices, which can mirror the favorable outcomes of RYGB surgery. In this review, we highlight current observations of the metabolic and physiologic events following RYGB, with a particular focus on the role of the anatomical reconfiguration of the gastrointestinal tract after RYGB.
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Affiliation(s)
- Martin L Yarmush
- Center for Engineering in Medicine, Department of Surgery, Massachusetts General Hospital, Harvard Medical School, and Shriners Burn Hospital for Children, Boston, Massachusetts 02114;
| | - Matthew D'Alessandro
- Center for Engineering in Medicine, Department of Surgery, Massachusetts General Hospital, Harvard Medical School, and Shriners Burn Hospital for Children, Boston, Massachusetts 02114;
| | - Nima Saeidi
- Center for Engineering in Medicine, Department of Surgery, Massachusetts General Hospital, Harvard Medical School, and Shriners Burn Hospital for Children, Boston, Massachusetts 02114;
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Daliri EBM, Wei S, Oh DH, Lee BH. The human microbiome and metabolomics: Current concepts and applications. Crit Rev Food Sci Nutr 2018; 57:3565-3576. [PMID: 27767329 DOI: 10.1080/10408398.2016.1220913] [Citation(s) in RCA: 37] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/07/2023]
Abstract
The mammalian gastrointestinal tract has co-developed with a large number of microbes in a symbiotic relationship over millions of years. Recent studies indicate that indigenous bacteria are intimate with the intestine and play essential roles in health and disease. In the quest to maintain a stable niche, these prokaryotes influence multiple host metabolic pathways, resulting from an interactive host-microbiota metabolic signaling and impacting strongly on the metabolic phenotypes of the host. Since dysbiosis of the gut bacteria result in alteration in the levels of certain microbial and host co-metabolites, identifying these markers could enhance early detection of diseases. Also, identification of these metabolic fingerprints could give us clues as to how to manipulate the microbiome to promote health or treat diseases. This review provides an overview of our current knowledge of the microbiome and metablomics, applications and the future perspectives.
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Affiliation(s)
- Eric Banan-Mwine Daliri
- a Department of Food Science and Biotechnology , Kangwon National University , Chuncheon , South Korea
| | - Shuai Wei
- a Department of Food Science and Biotechnology , Kangwon National University , Chuncheon , South Korea
| | - Deog H Oh
- a Department of Food Science and Biotechnology , Kangwon National University , Chuncheon , South Korea
| | - Byong H Lee
- a Department of Food Science and Biotechnology , Kangwon National University , Chuncheon , South Korea.,b Department of Food Science/Agricultural Chemistry , McGill University , Ste.-Anne-de-Bellevue , Quebec , Canada
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Alterations in gut microbiota associated with a cafeteria diet and the physiological consequences in the host. Int J Obes (Lond) 2017; 42:746-754. [PMID: 29167556 DOI: 10.1038/ijo.2017.284] [Citation(s) in RCA: 28] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/09/2017] [Revised: 10/17/2017] [Accepted: 10/30/2017] [Indexed: 12/13/2022]
Abstract
OBJECTIVE Gut microbiota have been described as key factors in the pathophysiology of obesity and different components of metabolic syndrome (MetS). The cafeteria diet (CAF)-fed rat is a preclinical model that reproduces most of the alterations found in human MetS by simulating a palatable human unbalanced diet. Our objective was to assess the effects of CAF on gut microbiota and their associations with different components of MetS in Wistar rats. METHODS Animals were fed a standard diet or CAF for 12 weeks. A partial least square-based methodology was used to reveal associations between gut microbiota, characterized by 16S ribosomal DNA gene sequencing, and biochemical, nutritional and physiological parameters. RESULTS CAF feeding resulted in obesity, dyslipidemia, insulin resistance and hepatic steatosis. These changes were accompanied by a significant decrease in gut bacterial diversity, decreased Firmicutes and an increase in Actinobacteria and Proteobacteria abundances, which were concomitant with increased endotoxemia. Associations of different genera with the intake of lipids and carbohydrates were opposed from those associated with the intake of fiber. Changes in gut microbiota were also associated with the different physiological effects of CAF, mainly increased adiposity and altered levels of plasma leptin and glycerol, consistent with altered adipose tissue metabolism. Also hepatic lipid accretion was associated with changes in microbiota, highlighting the relevance of gut microbiota homeostasis in the adipose-liver axis. CONCLUSIONS Overall, our results suggest that CAF feeding has a profound impact on the gut microbiome and, in turn, that these changes may be associated with important features of MetS.
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Śpiewak K, Majka G, Pilarczyk- Żurek M, Nowak PM, Woźniakiewicz M, Pietrzyk P, Korzeniak T, Stochel-Gaudyn A, Fyderek K, Strus M, Brindell M. Mn 3+ -saturated bovine lactoferrin as a new complex with potential prebiotic activities for dysbiosis treatment and prevention – On the synthesis, chemical characterization and origin of biological activity. J Funct Foods 2017. [DOI: 10.1016/j.jff.2017.09.042] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023] Open
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Belei O, Olariu L, Dobrescu A, Marcovici T, Marginean O. The relationship between non-alcoholic fatty liver disease and small intestinal bacterial overgrowth among overweight and obese children and adolescents. J Pediatr Endocrinol Metab 2017; 30:1161-1168. [PMID: 28988228 DOI: 10.1515/jpem-2017-0252] [Citation(s) in RCA: 29] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/28/2017] [Accepted: 09/04/2017] [Indexed: 12/20/2022]
Abstract
BACKGROUND The increasing rate of obesity and overweight among children has highlighted nonalcoholic fatty liver disease (NAFLD) as the most common cause of chronic pediatric liver diseases. There are many publications supporting the idea that gut microbiota is altered in NAFLD. The aim of this study was to evaluate the prevalence of NAFLD among overweight and obese children with and without small intestinal bacterial overgrowth (SIBO) compared to a control group and to assess if intestinal dysbiosis represents a risk factor for NAFLD. METHODS One hundred and twenty-five overweight and obese children aged 10-18 years and 120 controls matched for age and gender were enrolled. SIBO was assessed by glucose hydrogen breath test (GHBT) in all subjects. NAFLD was assessed in all children using abdominal imaging and laboratory findings. RESULTS Of 125 obese children enrolled, 47 (37.6%) presented intestinal dysbiosis and 78 (62.4%) were SIBO negative. Only four (3.3%) controls were SIBO positive. NAFLD was detected in 28/47 (59.5%) of the SIBO positive obese group, compared to 8/78 (10.2%) of the SIBO negative obese group (p<0.001) and 0/120 (0%) controls (p<0.001). Children from the SIBO positive obese group had higher rates of elevated aminotransferases levels: aspartate aminotransferases (ASAT) (53.1% vs. 6.4%; p<0.001) and alanine aminotransferase (ALAT) (59.5% vs. 7.6%; p<0.001), hypertension (23.4% vs. 5.1%; p=0.002) and metabolic syndrome (44.6% vs. 9%; p=0.002) compared to the SIBO negative obese group. CONCLUSIONS Obese children with SIBO have an increased risk for developing NAFLD. The relationship between intestinal dysbiosis and diet can influence the gut-liver axis.
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Can the gastrointestinal microbiota be modulated by dietary fibre to treat obesity? Ir J Med Sci 2017; 187:393-402. [DOI: 10.1007/s11845-017-1686-9] [Citation(s) in RCA: 17] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/15/2017] [Accepted: 10/03/2017] [Indexed: 12/26/2022]
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Wang L, Hu L, Yan S, Jiang T, Fang S, Wang G, Zhao J, Zhang H, Chen W. Effects of different oligosaccharides at various dosages on the composition of gut microbiota and short-chain fatty acids in mice with constipation. Food Funct 2017; 8:1966-1978. [PMID: 28475191 DOI: 10.1039/c7fo00031f] [Citation(s) in RCA: 114] [Impact Index Per Article: 14.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/20/2022]
Abstract
The aim of this study was to evaluate the effects of three different kinds of oligosaccharides (a fructo-oligosaccharide (FOS) formulation consisting of 95% FOS (FOS95); a galacto-oligosaccharide (GOS) formulation consisting of 90% GOS (GOS90) and an isomalto-oligosaccharide (IMO) formulation consisting of 90% IMO (IMO90)) at dosages of 0.8, 4 g per d per kg bw and 8 g per d per kg bw on the composition and activity of the microbiota in the gut of mice with constipation induced by loperamide. Oligosaccharides were intragastrically administered to specific pathogen-free BALB/c mice once per day for 17 days. Feces were collected during a feeding trial and subjected to 16S rDNA amplicon analysis. Constipation indices, changes in gut microbiota and metabolic activity were measured to evaluate the effects of the oligosaccharides. The results show that oligosaccharides treated constipation by increasing both the water content of the feces and the small intestinal transit rate. The dosage required to treat constipation was different for different oligosaccharides. High-dose GOS90 was the most effective in relieving constipation, followed by medium-dose FOS95 and IMO90. The fecal samples were investigated after the oligosaccharide treatment. All three oligosaccharides increased the ratio of acetic acid and decreased the ratio of propionic and butyric acids in the feces. The increase in the ratio of acetic acid and the concentration of butyric acid were found to have relatively larger effects on constipation. After treatment with oligosaccharides, the gut microbiotas of the mice were dominated by Firmicutes, Bacteroidetes and Actinobacteria. At the genus level, oligosaccharide treatment increased the levels of Lactobacillus and Bifidobacterium and decreased the levels of Odoribacter, Alistipes and Bacteroides. In conclusion, our results demonstrate that oligosaccharides administered as a dietary supplement increase the water content of feces, reduce intestinal transit time, modulate the composition of the gut microbiota and increase the concentration of short-chain fatty acids in the feces of mice with constipation.
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Affiliation(s)
- Linlin Wang
- State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi 214122, P. R. China.
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El Aidy S, Ramsteijn AS, Dini-Andreote F, van Eijk R, Houwing DJ, Salles JF, Olivier JDA. Serotonin Transporter Genotype Modulates the Gut Microbiota Composition in Young Rats, an Effect Augmented by Early Life Stress. Front Cell Neurosci 2017; 11:222. [PMID: 28824378 PMCID: PMC5540888 DOI: 10.3389/fncel.2017.00222] [Citation(s) in RCA: 57] [Impact Index Per Article: 7.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/30/2017] [Accepted: 07/13/2017] [Indexed: 02/01/2023] Open
Abstract
The neurotransmitter serotonin (5-HT) plays a vital regulatory role in both the brain and gut. 5-HT is crucial for regulating mood in the brain as well as gastrointestinal motility and secretion peripherally. Alterations in 5-HT transmission have been linked to pathological symptoms in both intestinal and psychiatric disorders and selective 5-HT transporter (5-HTT) inhibitors, affecting the 5-HT system by blocking the 5-HT transporter (5-HTT) have been successfully used to treat CNS- and intestinal disorders. Humans that carry the short allele of the 5-HTT-linked polymorphic region (5-HTTLPR) are more vulnerable to adverse environmental stressors, in particular early life stress. Although, early life stress has been shown to alter the composition of the gut microbiota, it is not known whether a lower 5-HTT expression is also associated with an altered microbiome composition. To investigate this, male and female wild type (5-HTT+/+), heterozygous (5-HTT+/-), and knockout (5-HTT-/-) 5-HT transporter rats were maternally separated for 6 h a day from postnatal day 2 till 15. On postnatal day 21, fecal samples were collected and the impact of 5-HTT genotype and maternal separation (MS) on the microbiome was analyzed using high-throughput sequencing of the bacterial 16S rRNA gene. MS showed a shift in the ratio between the two main bacterial phyla characterized by a decrease in Bacteroidetes and an increase in Firmicutes. Interestingly, the 5-HTT genotype caused a greater microbal dysbiosis (microbial imbalance) compared with MS. A significant difference in microbiota composition was found segregating 5-HTT-/- apart from 5-HTT+/- and 5-HTT+/+ rats. Moreover, exposure of rats with 5-HTT diminished expression to MS swayed the balance of their microbiota away from homeostasis to 'inflammatory' type microbiota characterized by higher abundance of members of the gut microbiome including Desulfovibrio, Mucispirillum, and Fusobacterium, all of which are previously reported to be associated with a state of intestinal inflammation, including inflammation associated with MS and brain disorders like multiple depressive disorders. Overall, our data show for the first time that altered expression of 5-HTT induces disruptions in male and female rat gut microbes and these 5-HTT genotype-related disruptions are augmented when combined with early life stress.
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Affiliation(s)
- Sahar El Aidy
- Microbial Physiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of GroningenGroningen, Netherlands
| | - Anouschka S Ramsteijn
- Neurobiology, Groningen Institute for Evolutionary Life Sciences, University of GroningenGroningen, Netherlands
| | - Francisco Dini-Andreote
- Microbial Ecology Cluster, Genomics Research in Ecology and Evolution in Nature, Groningen Institute for Evolutionary Life Sciences, University of GroningenGroningen, Netherlands
| | - Roel van Eijk
- Neurobiology, Groningen Institute for Evolutionary Life Sciences, University of GroningenGroningen, Netherlands
| | - Danielle J Houwing
- Neurobiology, Groningen Institute for Evolutionary Life Sciences, University of GroningenGroningen, Netherlands
| | - Joana F Salles
- Microbial Ecology Cluster, Genomics Research in Ecology and Evolution in Nature, Groningen Institute for Evolutionary Life Sciences, University of GroningenGroningen, Netherlands
| | - Jocelien D A Olivier
- Neurobiology, Groningen Institute for Evolutionary Life Sciences, University of GroningenGroningen, Netherlands
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