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1
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Moore M, Whittington HD, Knickmeyer R, Azcarate-Peril MA, Bruno-Bárcena JM. Non-stochastic reassembly of a metabolically cohesive gut consortium shaped by N-acetyl-lactosamine-enriched fibers. Gut Microbes 2025; 17:2440120. [PMID: 39695352 DOI: 10.1080/19490976.2024.2440120] [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: 04/30/2024] [Revised: 10/15/2024] [Accepted: 12/04/2024] [Indexed: 12/20/2024] Open
Abstract
Diet is one of the main factors shaping the human microbiome, yet our understanding of how specific dietary components influence microbial consortia assembly and subsequent stability in response to press disturbances - such as increasing resource availability (feeding rate) - is still incomplete. This study explores the reproducible re-assembly, metabolic interplay, and compositional stability within microbial consortia derived from pooled stool samples of three healthy infants. Using a single-step packed-bed reactor (PBR) system, we assessed the reassembly and metabolic output of consortia exposed to lactose, glucose, galacto-oligosaccharides (GOS), and humanized GOS (hGOS). Our findings reveal that complex carbohydrates, especially those containing low inclusion (~1.25 gL-1) components present in human milk, such as N-acetyl-lactosamine (LacNAc), promote taxonomic, and metabolic stability under varying feeding rates, as shown by diversity metrics and network analysis. Targeted metabolomics highlighted distinct metabolic responses to different carbohydrates: GOS was linked to increased lactate, lactose to propionate, sucrose to butyrate, and CO2, and the introduction of bile salts with GOS or hGOS resulted in butyrate reduction and increased hydrogen production. This study validates the use of single-step PBRs for reliably studying microbial consortium stability and functionality in response to nutritional press disturbances, offering insights into the dietary modulation of microbial consortia and their ecological dynamics.
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Affiliation(s)
- Madison Moore
- Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, USA
| | - Hunter D Whittington
- Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, USA
| | - Rebecca Knickmeyer
- Department of Psychiatry, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
| | - M Andrea Azcarate-Peril
- Department of Medicine, Division of Gastroenterology and Hepatology, and UNC Microbiome Core, Center for Gastrointestinal Biology and Disease (CGIBD), School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
| | - Jose M Bruno-Bárcena
- Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, USA
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2
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Clementino JR, de Oliveira LIG, Salgaço MK, de Oliveira FL, Mesa V, Tavares JF, Silva-Pereira L, Raimundo BVB, Oliveira KC, Medeiros AI, Silva FA, Sivieri K, Magnani M. β-Glucan Alone or Combined with Lactobacillus acidophilus Positively Influences the Bacterial Diversity and Metabolites in the Colonic Microbiota of Type II Diabetic Patients. Probiotics Antimicrob Proteins 2025:10.1007/s12602-025-10491-9. [PMID: 40011383 DOI: 10.1007/s12602-025-10491-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 02/14/2025] [Indexed: 02/28/2025]
Abstract
β-Glucan is a fermentable polysaccharide with prebiotic properties that has been shown to improve metabolic indicators. This study evaluated the effects of spent brewer's yeast β-glucan (BGL) and Lactobacillus acidophilus LA-5 (106 CFU/g) (LA5) alone and in combination (LA5-BGL) on the composition of the fecal microbiome of adults with type 2 diabetes mellitus (T2DM) using the Human Gut Microbial Ecosystem Simulator (SHIME®). Short-chain fatty acids (SCFAs), ammonium ions, and cytokines (IL-6 and IL-10) were measured. BGL, LA5, and LA5-BGL increased (p < 0.05) the richness and diversity of microbial communities in the gut microbiome of individuals with T2DM. All treatments increased (p < 0.05) the abundance of Bacteroides, Alistipes, Lactobacillus, Subdoligranulum, and Acidaminococcus, along with increased (p < 0.05) production of SCFAs and anti-inflammatory cytokine (IL-10) compared to the control group. BGL treatments showed a greater increase in microbial diversity, SCFAs levels (butyric, propionic, and acetic acid), and the anti-inflammatory cytokine (IL-10). LA5 showed the highest decrease in ammonium ion levels. Results indicate that BGL may have a prebiotic and immunomodulatory effect on the fecal microbial community and metabolic indicators in adults with type 2 diabetes mellitus (T2DM). Findings underscore the role of BGL as a prebiotic food.
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Affiliation(s)
| | | | | | | | - Victoria Mesa
- School of Nutrition and Dietetics, Universidad de Antioquia, Medellín, Colombia
- Faculty of Pharmacy, Université Paris Cité, Paris, France
| | - Josean Fechine Tavares
- Department of Pharmaceutical Sciences, Health Science Center, Federal University of Paraíba, João Pessoa, Brazil
| | - Ludmilla Silva-Pereira
- Department of Biological Sciences, São Paulo State University, Araraquara, São Paulo, Brazil
| | | | - Karen Cristina Oliveira
- Department of Biological Sciences, São Paulo State University, Araraquara, São Paulo, Brazil
| | - Alexandra Ivo Medeiros
- Department of Biological Sciences, São Paulo State University, Araraquara, São Paulo, Brazil
| | - Francyeli Araújo Silva
- Laboratory of Microbial Processes in Foods, Federal University of Paraíba, João Pessoa, Brazil
| | - Katia Sivieri
- Department of Food and Nutrition, São Paulo State University, Araraquara, Brazil
| | - Marciane Magnani
- Laboratory of Microbial Processes in Foods, Federal University of Paraíba, João Pessoa, Brazil.
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3
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François AC, Cesarini C, Taminiau B, Renaud B, Kruse CJ, Boemer F, van Loon G, Palmers K, Daube G, Wouters CP, Lecoq L, Gustin P, Votion DM. Unravelling Faecal Microbiota Variations in Equine Atypical Myopathy: Correlation with Blood Markers and Contribution of Microbiome. Animals (Basel) 2025; 15:354. [PMID: 39943124 PMCID: PMC11815872 DOI: 10.3390/ani15030354] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/18/2024] [Revised: 01/15/2025] [Accepted: 01/18/2025] [Indexed: 02/16/2025] Open
Abstract
Hypoglycin A and methylenecyclopropylglycine are protoxins responsible for atypical myopathy in equids. These protoxins are converted into toxins that inhibit fatty acid β-oxidation, leading to blood accumulation of acylcarnitines and toxin conjugates, such as methylenecyclopropylacetyl-carnitine. The enzymes involved in this activation are also present in some prokaryotic cells, raising questions about the potential role of intestinal microbiota in the development of intoxication. Differences have been noted between the faecal microbiota of cograzers and atypical myopathy-affected horses. However, recent blood acylcarnitines profiling revealed subclinical cases among cograzers, challenging their status as a control group. This study investigates the faecal microbiota of horses clinically affected by atypical myopathy, their cograzers, and a control group of toxin-free horses while analysing correlations between microbiota composition and blood parameters. Faecal samples were analysed using 16S amplicon sequencing, revealing significant differences in α-diversity, evenness, and β-diversity. Notable differences were found between several genera, especially Clostridia_ge, Bacteria_ge, Firmicutes_ge, Fibrobacter, and NK4A214_group. Blood levels of methylenecyclopropylacetyl-carnitine and C14:1 correlated with variations in faecal microbial composition. The theoretical presence of enzymes in bacterial populations was also investigated. These results underscore the critical need to investigate the potential role of intestinal microbiota in this poisoning and may provide insights for developing prevention and treatment strategies.
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Affiliation(s)
- Anne-Christine François
- Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (B.R.); (P.G.); (D.-M.V.)
| | - Carla Cesarini
- Equine Clinical Department, Faculty of Veterinary Medicine, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (C.C.); (L.L.)
| | - Bernard Taminiau
- Department of Food Sciences–Microbiology, Faculty of Veterinary Medicine, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (B.T.); (G.D.)
| | - Benoît Renaud
- Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (B.R.); (P.G.); (D.-M.V.)
| | - Caroline-Julia Kruse
- Department of Functional Sciences, Faculty of Veterinary Medicine, Physiology and Sport Medicine, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium;
| | - François Boemer
- Biochemical Genetics Laboratory, CHU, University of Liège, 4000 Liège, Belgium;
| | - Gunther van Loon
- Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium;
| | | | - Georges Daube
- Department of Food Sciences–Microbiology, Faculty of Veterinary Medicine, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (B.T.); (G.D.)
| | - Clovis P. Wouters
- Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (B.R.); (P.G.); (D.-M.V.)
| | - Laureline Lecoq
- Equine Clinical Department, Faculty of Veterinary Medicine, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (C.C.); (L.L.)
| | - Pascal Gustin
- Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (B.R.); (P.G.); (D.-M.V.)
| | - Dominique-Marie Votion
- Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liège, 4000 Liège, Belgium; (B.R.); (P.G.); (D.-M.V.)
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4
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Bao X, Wu J. Natural anti-adhesive components against pathogenic bacterial adhesion and infection in gastrointestinal tract: case studies of Helicobacter pylori, Salmonella enterica, Clostridium difficile, and diarrheagenic Escherichia coli. Crit Rev Food Sci Nutr 2024:1-46. [PMID: 39666022 DOI: 10.1080/10408398.2024.2436139] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2024]
Abstract
Antimicrobial resistance (AMR) poses a global public health concern. Recognizing the critical role of bacterial adhesion in pathogenesis of infection, anti-adhesive therapy emerges as a promising approach to impede initial bacterial attachment, thus preventing pathogenic colonization and infection. Natural anti-adhesive agents derived from food sources are generally safe and have the potential to inhibit the emergence of resistant bacteria. This comprehensive review explored diverse natural dietary components exhibiting anti-adhesive activities against several model enteric pathogens, including Helicobacter pylori, Salmonella enterica, Clostridium difficile, and three key diarrheagenic Escherichia coli (i.e., enterotoxigenic E. coli, enteropathogenic E. coli, and enterohemorrhagic E. coli). Investigating various anti-adhesive products will advance our understanding of current research of the field and inspire further development of these agents as potential nutraceuticals or adjuvants to improve the efficacy of conventional antibiotics.
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Affiliation(s)
- Xiaoyu Bao
- Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
| | - Jianping Wu
- Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
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5
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Garcia Mendez DF, Egan S, Wist J, Holmes E, Sanabria J. Meta-analysis of the Microbial Diversity Cultured in Bioreactors Simulating the Gut Microbiome. MICROBIAL ECOLOGY 2024; 87:57. [PMID: 38587527 PMCID: PMC11001690 DOI: 10.1007/s00248-024-02369-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/07/2023] [Accepted: 03/25/2024] [Indexed: 04/09/2024]
Abstract
Understanding the intricate ecological interactions within the gut microbiome and unravelling its impact on human health is a challenging task. Bioreactors are valuable tools that have contributed to our understanding of gut microbial ecology. However, there is a lack of studies describing and comparing the microbial diversity cultivated in these models. This knowledge is crucial for refining current models to reflect the gastrointestinal microbiome accurately. In this study, we analysed the microbial diversity of 1512 samples from 18 studies available in public repositories that employed cultures performed in batches and various bioreactor models to cultivate faecal microbiota. Community structure comparison between samples using t-distributed stochastic neighbour embedding and the Hellinger distance revealed a high variation between projects. The main driver of these differences was the inter-individual variation between the donor faecal inocula. Moreover, there was no overlap in the structure of the microbial communities between studies using the same bioreactor platform. In addition, α-diversity analysis using Hill numbers showed that highly complex bioreactors did not exhibit higher diversities than simpler designs. However, analyses of five projects in which the samples from the faecal inoculum were also provided revealed an amplicon sequence variants enrichment in bioreactors compared to the inoculum. Finally, a comparative analysis of the taxonomy of the families detected in the projects and the GMRepo database revealed bacterial families exclusively found in the bioreactor models. These findings highlight the potential of bioreactors to enrich low-abundance microorganisms from faecal samples, contributing to uncovering the gut microbial "dark matter".
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Affiliation(s)
- David Felipe Garcia Mendez
- Australian National Phenome Centre and Centre for Computational and Systems Medicine, Health Futures Institute, Murdoch University, Harry Perkins Building, Perth, WA, 6150, Australia
| | - Siobhon Egan
- Australian National Phenome Centre and Centre for Computational and Systems Medicine, Health Futures Institute, Murdoch University, Harry Perkins Building, Perth, WA, 6150, Australia
| | - Julien Wist
- Australian National Phenome Centre and Centre for Computational and Systems Medicine, Health Futures Institute, Murdoch University, Harry Perkins Building, Perth, WA, 6150, Australia
- Chemistry Department, Universidad del Valle - Sede Meléndez, 76001, Cali, Colombia
| | - Elaine Holmes
- Australian National Phenome Centre and Centre for Computational and Systems Medicine, Health Futures Institute, Murdoch University, Harry Perkins Building, Perth, WA, 6150, Australia
| | - Janeth Sanabria
- Australian National Phenome Centre and Centre for Computational and Systems Medicine, Health Futures Institute, Murdoch University, Harry Perkins Building, Perth, WA, 6150, Australia.
- Environmental Microbiology and Biotechnology Laboratory, Engineering School of Environmental & Natural Resources, Engineering Faculty, Universidad del Valle - Sede Meléndez, 76001, Cali, Colombia.
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6
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Dixit Y, Kanojiya K, Bhingardeve N, Ahire JJ, Saroj D. In Vitro Human Gastrointestinal Tract Simulation Systems: A Panoramic Review. Probiotics Antimicrob Proteins 2024; 16:501-518. [PMID: 36988898 DOI: 10.1007/s12602-023-10052-y] [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] [Accepted: 03/02/2023] [Indexed: 03/30/2023]
Abstract
Simulated human gastrointestinal (GI) tract systems are important for their applications in the fields of probiotics, nutrition and health. To date, various in vitro gut systems have been available to study GI tract dynamics and its association with health. In contrast to in vivo investigations, which are constrained by ethical considerations, in vitro models have several benefits despite the challenges involved in mimicking the GI environment. These in vitro models can be used for a range of research, from simple to dynamic, with one compartment to several compartments. In this review, we present a panoramic development of in vitro GI models for the first time through an evolutionary timeline. We tried to provide insight on designing an in vitro gut model, especially for novices. Latest developments and scope for improvement based on the limitations of the existing models were highlighted. In conclusion, designing an in vitro GI model suitable for a particular application is a multifaceted task. The bio-mimicking of the GI tract specific to geometrical, anatomical and mechanical features remains a challenge for the development of effective in vitro GI models. Advances in computer technology, artificial intelligence and nanotechnology are going to be revolutionary for further development. Besides this, in silico high-throughput technologies and miniaturisation are key players in the success of making in vitro modelling cost-effective and reducing the burden of in vivo studies.
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Affiliation(s)
- Yogini Dixit
- Advanced Enzyme Technologies Ltd., 5th Floor, A-Wing, Sun Magnetica, Louiswadi, Maharashtra, Thane West, India
| | - Khushboo Kanojiya
- Advanced Enzyme Technologies Ltd., 5th Floor, A-Wing, Sun Magnetica, Louiswadi, Maharashtra, Thane West, India
| | - Namrata Bhingardeve
- Advanced Enzyme Technologies Ltd., 5th Floor, A-Wing, Sun Magnetica, Louiswadi, Maharashtra, Thane West, India
| | - Jayesh J Ahire
- Advanced Enzyme Technologies Ltd., 5th Floor, A-Wing, Sun Magnetica, Louiswadi, Maharashtra, Thane West, India.
| | - Dina Saroj
- Advanced Enzyme Technologies Ltd., 5th Floor, A-Wing, Sun Magnetica, Louiswadi, Maharashtra, Thane West, India
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7
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Vasquez S, Angeli MAC, Polo A, Costantini A, Petrelli M, Avancini E, Di Cagno R, Gobbetti M, Gaiardo A, Valt M, Lugli P, Petti L. In vitro gastrointestinal gas monitoring with carbon nanotube sensors. Sci Rep 2024; 14:825. [PMID: 38191903 PMCID: PMC10774382 DOI: 10.1038/s41598-023-50134-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: 09/05/2023] [Accepted: 12/15/2023] [Indexed: 01/10/2024] Open
Abstract
In vitro simulators of the human gastrointestinal (GI) tract are remarkable technological platforms for studying the impact of food on the gut microbiota, enabling continuous and real-time monitoring of key biomarkers. However, comprehensive real-time monitoring of gaseous biomarkers in these systems is required with a cost-effective approach, which has been challenging to perform experimentally to date. In this work, we demonstrate the integration and in-line use of carbon nanotube (CNT)-based chemiresitive gas sensors coated with a thin polydimethylsiloxane (PDMS) membrane for the continuous monitoring of gases within the Simulator of the Human Microbial Ecosystem (SHIME). The findings demonstrate the ability of the gas sensor to continuously monitor the different phases of gas production in this harsh, anaerobic, highly humid, and acidic environment for a long exposure time (16 h) without saturation. This establishes our sensor platform as an effective tool for real-time monitoring of gaseous biomarkers in in vitro systems like SHIME.
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Affiliation(s)
- Sahira Vasquez
- Sensing Technologies Laboratory (STL), Faculty of Engineering, Free University of Bozen-Bolzano, 39100, Bolzano, Italy.
| | - Martina Aurora Costa Angeli
- Sensing Technologies Laboratory (STL), Faculty of Engineering, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Andrea Polo
- Micro4Food Lab, Faculty of Agricultural, Food, and Environmental Sciences, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Alice Costantini
- Micro4Food Lab, Faculty of Agricultural, Food, and Environmental Sciences, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Mattia Petrelli
- Sensing Technologies Laboratory (STL), Faculty of Engineering, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Enrico Avancini
- Sensing Technologies Laboratory (STL), Faculty of Engineering, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Raffaella Di Cagno
- Micro4Food Lab, Faculty of Agricultural, Food, and Environmental Sciences, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Marco Gobbetti
- Micro4Food Lab, Faculty of Agricultural, Food, and Environmental Sciences, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Andrea Gaiardo
- Micro Nano Facility, Bruno Kessler Foundation, 38123, Trento, Italy
| | - Matteo Valt
- Micro Nano Facility, Bruno Kessler Foundation, 38123, Trento, Italy
| | - Paolo Lugli
- Sensing Technologies Laboratory (STL), Faculty of Engineering, Free University of Bozen-Bolzano, 39100, Bolzano, Italy
| | - Luisa Petti
- Sensing Technologies Laboratory (STL), Faculty of Engineering, Free University of Bozen-Bolzano, 39100, Bolzano, Italy.
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8
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Rosés C, Garcia-Ibañez P, Agudelo A, Viadel B, Tomás-Cobos L, Gallego E, Carvajal M, Milagro FI, Barceló A. Effects of Glucosinolate-Enriched Red Radish ( Raphanus sativus) on In Vitro Models of Intestinal Microbiota and Metabolic Syndrome-Related Functionalities. ACS OMEGA 2023; 8:23373-23388. [PMID: 37426251 PMCID: PMC10324062 DOI: 10.1021/acsomega.2c08128] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 12/22/2022] [Accepted: 04/25/2023] [Indexed: 07/11/2023]
Abstract
The gut microbiota profile is determined by diet composition, and therefore this interaction is crucial for promoting specific bacterial growth and enhancing the health status. Red radish (Raphanus sativusL.) contains several secondary plant metabolites that can exert a protective effect on human health. Recent studies have shown that radish leaves have a higher content of major nutrients, minerals, and fiber than roots, and they have garnered attention as a healthy food or supplement. Therefore, the consumption of the whole plant should be considered, as its nutritional value may be of greater interest. The aim of this work is to evaluate the effects of glucosinolate (GSL)-enriched radish with elicitors on the intestinal microbiota and metabolic syndrome-related functionalities by using an in vitro dynamic gastrointestinal system and several cellular models developed to study the GSL impact on different health indicators such as blood pressure, cholesterol metabolism, insulin resistance, adipogenesis, and reactive oxygen species (ROS). The treatment with red radish had an influence on short-chain fatty acids (SCFA) production, especially on acetic and propionic acid and many butyrate-producing bacteria, suggesting that consumption of the entire red radish plant (leaves and roots) could modify the human gut microbiota profile toward a healthier one. The evaluation of the metabolic syndrome-related functionalities showed a significant decrease in the gene expression of endothelin, interleukin IL-6, and cholesterol transporter-associated biomarkers (ABCA1 and ABCG5), suggesting an improvement of three risk factors associated with metabolic syndrome. The results support the idea that the use of elicitors on red radish crops and its further consumption (the entire plant) may contribute to improving the general health status and gut microbiota profile.
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Affiliation(s)
- Carles Rosés
- Servei
de Genòmica, Universitat Autònoma
de Barcelona, 08193 Bellaterra, Cerdanyola
del Vallés, Spain
| | - Paula Garcia-Ibañez
- Aquaporins
Group, Centro de Edafología y Biología
Aplicada del Segura, CEBAS-CSIC, Campus Universitario de Espinardo - 25, E-30100 Murcia, Spain
- Phytochemistry
and Healthy Foods Lab, Department of Food Science Technology, Centro de Edafología y Biología Aplicada
del Segura, CEBAS-CSIC, Campus de Espinardo-25, E-30100 Murcia, Spain
| | - Agatha Agudelo
- Sakata
Seed Ibérica S.L., Pl, Poeta Vicente Gaos, 6 bajo, Valencia 46021, Spain
- Universidad
Politécnica de Valencia, UPV, Camino de Vera s/n, Valencia 46022, Spain
| | - Blanca Viadel
- AINIA,
Technology Centre, C/
Benjamin Franklin 5-11, Parque Tecnológico de Valencia, 46980 Paterna, Valenca, Spain
| | - Lidia Tomás-Cobos
- AINIA,
Technology Centre, C/
Benjamin Franklin 5-11, Parque Tecnológico de Valencia, 46980 Paterna, Valenca, Spain
| | - Elisa Gallego
- AINIA,
Technology Centre, C/
Benjamin Franklin 5-11, Parque Tecnológico de Valencia, 46980 Paterna, Valenca, Spain
| | - Micaela Carvajal
- Aquaporins
Group, Centro de Edafología y Biología
Aplicada del Segura, CEBAS-CSIC, Campus Universitario de Espinardo - 25, E-30100 Murcia, Spain
- Phytochemistry
and Healthy Foods Lab, Department of Food Science Technology, Centro de Edafología y Biología Aplicada
del Segura, CEBAS-CSIC, Campus de Espinardo-25, E-30100 Murcia, Spain
| | - Fermín I. Milagro
- Center for
Nutrition Research, Department of Nutrition, Food Sciences and Physiology, University of Navarra, 31008 Pamplona, Spain
- Navarra
Institute for Health Research (IdISNA), 31008 Pamplona, Spain
- Centro
de Investigación Biomédica en Red de la Fisiopatología
de la Obesidad y Nutrición (CIBERobn), Instituto de la Salud Carlos III, 289029 Madrid, Spain
| | - Anna Barceló
- Servei
de Genòmica, Universitat Autònoma
de Barcelona, 08193 Bellaterra, Cerdanyola
del Vallés, Spain
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9
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Lesmes U. In vitro digestion models for the design of safe and nutritious foods. ADVANCES IN FOOD AND NUTRITION RESEARCH 2023; 104:179-203. [PMID: 37236731 DOI: 10.1016/bs.afnr.2022.10.006] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/28/2023]
Abstract
Responsible development of future foods requires in depth understanding of food digestion in the human body based on robust research models, ranging from in vitro models to randomized controlled human trials. This chapter overviews fundamental aspects of food digestion, namely bioaccessibility and bioavailability, and models mirroring gastric, intestinal, and colonic conditions. Second, the chapter demonstrates the potential of in vitro digestion models to help screen adverse effects of food additives, such as Titanium dioxide or carrageenan, or underpin the determinants of macro- and micronutrient digestion in different strata of the population, for example digestion of emulsions. Such efforts support rationalized design of functional foods, such as infant formulae, cheese, cereals and biscuits which are validated in vivo or in randomized controlled trials.
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Affiliation(s)
- Uri Lesmes
- Faculty of Biotechnology and Food Engineering, Technion, Israel.
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10
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García Mendez D, Sanabria J, Wist J, Holmes E. Effect of Operational Parameters on the Cultivation of the Gut Microbiome in Continuous Bioreactors Inoculated with Feces: A Systematic Review. JOURNAL OF AGRICULTURAL AND FOOD CHEMISTRY 2023; 71:6213-6225. [PMID: 37070710 PMCID: PMC10143624 DOI: 10.1021/acs.jafc.2c08146] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/20/2022] [Revised: 01/27/2023] [Accepted: 01/27/2023] [Indexed: 05/03/2023]
Abstract
Since the early 1980s, multiple researchers have contributed to the development of in vitro models of the human gastrointestinal system for the mechanistic interrogation of the gut microbiome ecology. Using a bioreactor for simulating all the features and conditions of the gastrointestinal system is a massive challenge. Some conditions, such as temperature and pH, are readily controlled, but a more challenging feature to simulate is that both may vary in different regions of the gastrointestinal tract. Promising solutions have been developed for simulating other functionalities, such as dialysis capabilities, peristaltic movements, and biofilm growth. This research field is under constant development, and further efforts are needed to drive these models closer to in vivo conditions, thereby increasing their usefulness for studying the gut microbiome impact on human health. Therefore, understanding the influence of key operational parameters is fundamental for the refinement of the current bioreactors and for guiding the development of more complex models. In this review, we performed a systematic search for operational parameters in 229 papers that used continuous bioreactors seeded with human feces. Despite the reporting of operational parameters for the various bioreactor models being variable, as a result of a lack of standardization, the impact of specific operational parameters on gut microbial ecology is discussed, highlighting the advantages and limitations of the current bioreactor systems.
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Affiliation(s)
- David
Felipe García Mendez
- Australian
National Phenome Centre and Computational and Systems Medicine, Health
Futures Institute, Murdoch University, Harry Perkins Building, Perth, Australia WA6150
| | - Janeth Sanabria
- Australian
National Phenome Centre and Computational and Systems Medicine, Health
Futures Institute, Murdoch University, Harry Perkins Building, Perth, Australia WA6150
- Environmental
Microbiology and Biotechnology Laboratory, Engineering School of Environmental
& Natural Resources, Engineering Faculty, Universidad del Valle—Sede Meléndez, Cali, Colombia 76001
| | - Julien Wist
- Australian
National Phenome Centre and Computational and Systems Medicine, Health
Futures Institute, Murdoch University, Harry Perkins Building, Perth, Australia WA6150
- Chemistry
Department, Universidad del Valle, 76001, Cali, Colombia
| | - Elaine Holmes
- Australian
National Phenome Centre and Computational and Systems Medicine, Health
Futures Institute, Murdoch University, Harry Perkins Building, Perth, Australia WA6150
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11
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Guo Z, Yang Y, Wu Q, Liu M, Zhou L, Zhang L, Dong D. New insights into the characteristic skin microorganisms in different grades of acne and different acne sites. Front Microbiol 2023; 14:1167923. [PMID: 37180251 PMCID: PMC10172595 DOI: 10.3389/fmicb.2023.1167923] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/17/2023] [Accepted: 04/05/2023] [Indexed: 05/16/2023] Open
Abstract
Background The increasing maturity of sequencing technology provides a convenient approach to studying the role of skin microorganisms in acne pathogenesis. However, there are still too few studies about the skin microbiota of Asian acne patients, especially a lack of detailed analysis of the characteristics of the skin microbiota in the different acne sites. Methods In this study, a total of 34 college students were recruited and divided into the health, mild acne, and severe acne groups. The bacterial and fungal flora of samples were separately detected by 16S and 18S rRNA gene sequencing. The biomarkers of different acne grades and different acne sites [forehead, cheek, chin, torso (including chest and back)] were excavated. Results and Discussion Our results indicated that there was no significant difference in species diversity between groups. The genera like Propionibacterium, Staphylococcus, Corynebacterium, and Malassezia, which have a relatively high abundance in the skin microbiota and were reported as the most acne-associated microbes, were no obvious differences between groups. On the contrary, the abundance of less reported Gram-negative bacteria (Pseudomonas, Ralstonia, and Pseudidiomarina) and Candida has a significant alteration. Compared with the health group and the mild group, in the severe group, the abundance of Pseudomonas and Ralstonia sharply reduced while that of Pseudidiomarina and Candida remarkably raised. Moreover, different acne sites have different numbers and types of biomarkers. Among the four acne sites, the cheek has the greatest number of biomarkers including Pseudomonas, Ralstonia, Pseudidiomarina, Malassezia, Saccharomyces, and Candida, while no biomarker was observed for the forehead. The network analysis indicated that there might be a competitive relationship between Pseudomonas and Propionibacterium. This study would provide a new insight and theoretical basis for precise and personalized acne microbial therapy.
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Affiliation(s)
- Zitao Guo
- National Engineering Research Center of Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi, China
- Jiangsu Provincial Research Center for Bioactive Product Processing Technology, Jiangnan University, Wuxi, China
| | - Yuliang Yang
- National Engineering Research Center of Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi, China
- Jiangsu Provincial Research Center for Bioactive Product Processing Technology, Jiangnan University, Wuxi, China
| | - Qianjie Wu
- Wuxi Medical College, Jiangnan University, Wuxi, China
| | - Meng Liu
- Wuxi Medical College, Jiangnan University, Wuxi, China
| | - Leyuan Zhou
- Department of Radiation Oncology, Dushu Lake Hospital Affiliated to Soochow University, Suzhou, China
| | - Liang Zhang
- National Engineering Research Center of Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi, China
- Jiangsu Provincial Research Center for Bioactive Product Processing Technology, Jiangnan University, Wuxi, China
- *Correspondence: Liang Zhang,
| | - Dake Dong
- Department of Dermatology, Affiliated Hospital of Jiangnan University, Wuxi, China
- Dake Dong,
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12
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Functional Fermented Milk with Fruit Pulp Modulates the In Vitro Intestinal Microbiota. Foods 2022; 11:foods11244113. [PMID: 36553855 PMCID: PMC9778618 DOI: 10.3390/foods11244113] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/13/2022] [Revised: 12/14/2022] [Accepted: 12/15/2022] [Indexed: 12/23/2022] Open
Abstract
The effect of putative probiotic fermented milk (FM) with buriti pulp (FMB) or passion fruit pulp (FMPF) or without fruit pulp (FMC) on the microbiota of healthy humans was evaluated. FM formulations were administered into a simulator of the human intestinal microbial ecosystem (SHIME®) to evaluate the viability of lactic acid bacteria (LAB), microbiota composition, presence of short-chain fatty acids (SCFA), and ammonium ions. The probiotic LAB viability in FM was affected by the addition of the fruit pulp. Phocaeicola was dominant in the FMPF and FMB samples; Bifidobacterium was related to FM formulations, while Alistipes was associated with FMPF and FMB, and Lactobacillus and Lacticaseibacillus were predominant in FMC. Trabulsiella was the central element in the FMC, while Mediterraneibacter was the central one in the FMPF and FMB networks. The FM formulations increased the acetic acid, and a remarkably high amount of propionic and butyric acids were detected in the FMB treatment. All FM formulations decreased the ammonium ions compared to the control; FMPF samples stood out for having lower amounts of ammonia. The probiotic FM with fruit pulp boosted the beneficial effects on the intestinal microbiota of healthy humans in addition to increasing SCFA in SHIME® and decreasing ammonium ions, which could be related to the presence of bioactive compounds.
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13
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Risso D, Kaczmarczyk M, Laurie I, Mah E, Blonquist TM, Derrig L, Karnik K. Moderate intakes of soluble corn fibre or inulin do not cause gastrointestinal discomfort and are well tolerated in healthy children. Int J Food Sci Nutr 2022; 73:1104-1115. [PMID: 36245250 DOI: 10.1080/09637486.2022.2133098] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/24/2022]
Abstract
We investigated the gastrointestinal (GI) tolerance of soluble corn fibre (SCF) compared with inulin in children 3-9 years old. SCF (3-8 g/d for 10d) was tolerated as well as inulin: no differences were identified in stool frequency and consistency, proportion of subjects with at least one loose stool or reporting symptoms during bowel movement. Compared to inulin, 6 g/d of SCF lowered gas severity in children aged 3-5 years old. No differences were noted for alpha and beta diversity, relative abundance of Bacteroidota, Firmicutes, Ruminococcaceae, or the Firmicutes to Bacteroidota ratio. Relative abundance of some specific strains (i.e. Anaerostipes, Bifidobacterium, Fusicatenibacter, Parabacteroides) varied depending on the fibre type and dose level. Fortification at a level of 6-8 g/d of SCF and/or inulin could help addressing the fibre gap without any GI discomfort.
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Affiliation(s)
| | | | | | - Eunice Mah
- Biofortis Research, Inc., Addison, IL, USA
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14
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Effects of Marine Bioactive Compounds on Gut Ecology Based on In Vitro Digestion and Colonic Fermentation Models. Nutrients 2022; 14:nu14163307. [PMID: 36014813 PMCID: PMC9412687 DOI: 10.3390/nu14163307] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/08/2022] [Revised: 07/30/2022] [Accepted: 08/08/2022] [Indexed: 11/30/2022] Open
Abstract
Digestion and the absorption of food compounds are necessary steps before nutrients can exert a role in human health. The absorption and utilization of nutrients in the diet is an extremely complex dynamic process. Accurately grasping the digestion and absorption mechanisms of different nutrients or bioactive compounds can provide a better understanding regarding the relationship between health and nutrition. Several in vitro models for simulating human gastrointestinal digestion and colonic fermentation have been established to obtain more accurate data for further understanding of the metabolism of dietary components. Marine media is rich in a wide variety of nutrients that are essential for humans and is gaining increased attention as a research topic. This review summarizes some of the most explored in vitro digestion and colonic fermentation models. It also summarizes the research progress on the digestion and absorption of nutrients and bioactive compounds from marine substrates when subjected to these in vitro models. Additionally, an overview of the changes imparted by the digestion process on these bioactive compounds is provided, in order to support those marine resources that can be utilized for developing new healthy foods.
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15
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Effect of cinnamon on starch hydrolysis of rice pudding: comparing static and dynamic in vitro digestion models. Food Res Int 2022; 161:111813. [DOI: 10.1016/j.foodres.2022.111813] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/21/2022] [Revised: 07/31/2022] [Accepted: 08/18/2022] [Indexed: 11/19/2022]
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16
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Gościniak A, Eder P, Walkowiak J, Cielecka-Piontek J. Artificial Gastrointestinal Models for Nutraceuticals Research—Achievements and Challenges: A Practical Review. Nutrients 2022; 14:nu14132560. [PMID: 35807741 PMCID: PMC9268564 DOI: 10.3390/nu14132560] [Citation(s) in RCA: 15] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/04/2022] [Revised: 06/09/2022] [Accepted: 06/16/2022] [Indexed: 11/16/2022] Open
Abstract
Imitating the human digestive system as closely as possible is the goal of modern science. The main reason is to find an alternative to expensive, risky and time-consuming clinical trials. Of particular interest are models that simulate the gut microbiome. This paper aims to characterize the human gut microbiome, highlight the importance of its contribution to disease, and present in vitro models that allow studying the microbiome outside the human body but under near-natural conditions. A review of studies using models SHIME, SIMGI, TIM-2, ECSIM, EnteroMix, and PolyfermS will provide an overview of the options available and the choice of a model that suits the researcher’s expectations with advantages and disadvantages.
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Affiliation(s)
- Anna Gościniak
- Department of Pharmacognosy, Poznan University of Medical Sciences, Rokietnicka 3, 60-806 Poznan, Poland;
| | - Piotr Eder
- Department of Gastroenterology, Dietetics and Internal Diseases, Poznan University of Medical Sciences, Przybyszewskiego 49, 60-355 Poznan, Poland;
| | - Jarosław Walkowiak
- Department of Pediatric Gastroenterology and Metabolic Diseases, Poznan University of Medical Sciences, Szpitalna 27/33, 60-572 Poznan, Poland;
| | - Judyta Cielecka-Piontek
- Department of Pharmacognosy, Poznan University of Medical Sciences, Rokietnicka 3, 60-806 Poznan, Poland;
- Correspondence:
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17
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Rastall RA, Diez-Municio M, Forssten SD, Hamaker B, Meynier A, Moreno FJ, Respondek F, Stah B, Venema K, Wiese M. Structure and function of non-digestible carbohydrates in the gut microbiome. Benef Microbes 2022; 13:95-168. [PMID: 35729770 DOI: 10.3920/bm2021.0090] [Citation(s) in RCA: 40] [Impact Index Per Article: 13.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Together with proteins and fats, carbohydrates are one of the macronutrients in the human diet. Digestible carbohydrates, such as starch, starch-based products, sucrose, lactose, glucose and some sugar alcohols and unusual (and fairly rare) α-linked glucans, directly provide us with energy while other carbohydrates including high molecular weight polysaccharides, mainly from plant cell walls, provide us with dietary fibre. Carbohydrates which are efficiently digested in the small intestine are not available in appreciable quantities to act as substrates for gut bacteria. Some oligo- and polysaccharides, many of which are also dietary fibres, are resistant to digestion in the small intestines and enter the colon where they provide substrates for the complex bacterial ecosystem that resides there. This review will focus on these non-digestible carbohydrates (NDC) and examine their impact on the gut microbiota and their physiological impact. Of particular focus will be the potential of non-digestible carbohydrates to act as prebiotics, but the review will also evaluate direct effects of NDC on human cells and systems.
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Affiliation(s)
- R A Rastall
- Department of Food and Nutritional Sciences, The University of Reading, P.O. Box 226, Whiteknights, Reading, RG6 6AP, United Kingdom
| | - M Diez-Municio
- Instituto de Investigación en Ciencias de la Alimentación, CIAL (CSIC-UAM), CEI (UAM+CSIC), Nicolás Cabrera 9, 28049 Madrid, Spain
| | - S D Forssten
- IFF Health & Biosciences, Sokeritehtaantie 20, 02460 Kantvik, Finland
| | - B Hamaker
- Whistler Center for Carbohydrate Research, Department of Food Science, Purdue University, 745 Agriculture Mall Drive, West Lafayette, IN 47907-2009, USA
| | - A Meynier
- Nutrition Research, Mondelez France R&D SAS, 6 rue René Razel, 91400 Saclay, France
| | - F Javier Moreno
- Instituto de Investigación en Ciencias de la Alimentación, CIAL (CSIC-UAM), CEI (UAM+CSIC), Nicolás Cabrera 9, 28049 Madrid, Spain
| | - F Respondek
- Tereos, Zoning Industriel Portuaire, 67390 Marckolsheim, France
| | - B Stah
- Human Milk Research & Analytical Science, Danone Nutricia Research, Uppsalalaan 12, 3584 CT Utrecht, the Netherlands.,Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Faculty of Science, Utrecht University, Universiteitsweg 99, 3584 CG Utrecht, the Netherlands
| | - K Venema
- Centre for Healthy Eating & Food Innovation (HEFI), Maastricht University - campus Venlo, St. Jansweg 20, 5928 RC Venlo, the Netherlands
| | - M Wiese
- Department of Microbiology and Systems Biology, TNO, Utrechtseweg 48, 3704 HE, Zeist, the Netherlands
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18
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Barros de Medeiros VP, Salgaço MK, Pimentel TC, Rodrigues da Silva TC, Sartoratto A, Lima MDS, Sassi CFDC, Mesa V, Magnani M, Sivieri K. Spirulina platensis biomass enhances the proliferation rate of Lactobacillus acidophilus 5 (La-5) and combined with La-5 impact the gut microbiota of medium-age healthy individuals through an in vitro gut microbiome model. Food Res Int 2022; 154:110880. [PMID: 35337549 DOI: 10.1016/j.foodres.2021.110880] [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: 10/06/2021] [Revised: 12/03/2021] [Accepted: 12/04/2021] [Indexed: 11/16/2022]
Abstract
This study first evaluated the stimulatory effect of S. platensis biomass on the growth of L. acidophilus and the metabolic activity during fermentation (37 °C, 72 h) in a culture medium. The results demonstrated a higher impact of S. platensis biomass than fructooligosaccharide (FOS), an established prebiotic. Higher L. acidophilus proliferation rates and metabolic activity were observed (lower pH values and higher concentrations of acetic, lactic, and propionic acids) in the presence of S. platensis. Then, we evaluated the effects of the S. platensis biomass (1.5 g, twice a day, 5 days) in association with L. acidophilus (106 CFU/g) on the gut microbiota composition of medium-age healthy individuals through the Simulator of Human Intestinal Microbial Ecosystem (SHIME®) and measurement of metabolites. L. acidophilus (La5) and L. acidophilus + S. platensis (Spi-La5) could positively modulate the intestinal microbiota. The administration of La5 resulted in increases in Bacteroides, Megasphaera, Lactobacillus, and Parabacteroides genus abundance, with a consequent decrease in ammonium ions. The administration of Spi-La5 increased the abundance of the genus Erysipelatoclostridium, Roseburia, Enterococcus, Bifidobacterium, Coriobacteriaceae UCG-003, Enterobacter, and Paraclostridium. The results demonstrate that the intestinal microbiota was differently modified by administrating La5 and Spi-La5 and indicate the latter as an alternative for microbiota positive modulation in healthy individuals.
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Affiliation(s)
| | - Mateus Kawata Salgaço
- School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil
| | | | | | - Adilson Sartoratto
- Pluridisciplinary Center for Chemical, Biological and Agricultural Research (CPQBA), UNICAMP, Brazil
| | - Marcos Dos Santos Lima
- Departament of Food Technology, Federal Institute of Sertão Pernambucano, Pernambuco, Brazil
| | | | - Victoria Mesa
- Food and Human Nutrition Research Group, University of Antioquia, Medellín, Colombia
| | - Marciane Magnani
- Department of Food Engineering, Center of Technology, Federal University of Paraíba, PB, Brazil.
| | - Katia Sivieri
- School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil
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19
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Gaisawat MB, Lopez-Escalera S, MacPherson CW, Iskandar MM, Tompkins TA, Kubow S. Probiotics Exhibit Strain-Specific Protective Effects in T84 Cells Challenged With Clostridioides difficile-Infected Fecal Water. Front Microbiol 2022; 12:698638. [PMID: 35154018 PMCID: PMC8826048 DOI: 10.3389/fmicb.2021.698638] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/21/2021] [Accepted: 12/17/2021] [Indexed: 12/22/2022] Open
Abstract
Clostridioides difficile infection (CDI) is frequently associated with intestinal injury and mucosal barrier dysfunction, leading to an inflammatory response involving neutrophil localization and upregulation of pro-inflammatory cytokines. The severity of clinical manifestations is associated with the extent of the immune response, which requires mitigation for better clinical management. Probiotics could play a protective role in this disorder due to their immunomodulatory ability in gastrointestinal disorders. We assessed five single-strain and three multi-strain probiotics for their ability to modulate CDI fecal water (FW)-induced effects on T84 cells. The CDI-FW significantly (p < 0.05) decreased T84 cell viability. The CDI-FW-exposed cells also exhibited increased pro-inflammatory cytokine production as characterized by interleukin (IL)-8, C-X-C motif chemokine 5, macrophage inhibitory factor (MIF), IL-32, and tumor necrosis factor (TNF) ligand superfamily member 8. Probiotics were associated with strain-specific attenuation of the CDI-FW mediated effects, whereby Saccharomyces boulardii CNCM I-1079 and Lacticaseibacillus rhamnosus R0011 were most effective in reducing pro-inflammatory cytokine production and in increasing T84 cell viability. ProtecFlor™, Lactobacillus helveticus R0052, and Bifidobacterium longum R0175 showed moderate effectiveness, and L. rhamnosus GG R0343 along with the two other multi-strain combinations were the least effective. Overall, the findings showed that probiotic strains possess the capability to modulate the CDI-mediated inflammatory response in the gut lumen.
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Affiliation(s)
| | | | - Chad W MacPherson
- Rosell Institute for Microbiome and Probiotics, Montréal, QC, Canada
| | | | - Thomas A Tompkins
- Rosell Institute for Microbiome and Probiotics, Montréal, QC, Canada
| | - Stan Kubow
- School of Human Nutrition, McGill University, Montréal, QC, Canada
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20
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García MA, Varum F, Al-Gousous J, Hofmann M, Page S, Langguth P. In Vitro Methodologies for Evaluating Colon-Targeted Pharmaceutical Products and Industry Perspectives for Their Applications. Pharmaceutics 2022; 14:pharmaceutics14020291. [PMID: 35214024 PMCID: PMC8876830 DOI: 10.3390/pharmaceutics14020291] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/29/2021] [Revised: 01/22/2022] [Accepted: 01/24/2022] [Indexed: 02/04/2023] Open
Abstract
Several locally acting colon-targeted products to treat colonic diseases have been recently developed and marketed, taking advantage of gastrointestinal physiology to target delivery. Main mechanisms involve pH-dependent, time-controlled and/or enzymatic-triggered release. With site of action located before systemic circulation and troublesome colonic sampling, there is room for the introduction of meaningful in vitro methods for development, quality control (QC) and regulatory applications of these formulations. A one-size-fits-all method seems unrealistic, as the selection of experimental conditions should resemble the physiological features exploited to trigger the release. This article reviews the state of the art for bio-predictive dissolution testing of colon-targeted products. Compendial methods overlook physiological aspects, such as buffer molarity and fluid composition. These are critical for pH-dependent products and time-controlled systems containing ionizable drugs. Moreover, meaningful methods for enzymatic-triggered products including either bacteria or enzymes are completely ignored by pharmacopeias. Bio-predictive testing may accelerate the development of successful products, although this may require complex methodologies. However, for high-throughput routine testing (e.g., QC), simplified methods can be used where balance is struck between simplicity, robustness and transferability on one side and bio-predictivity on the other. Ultimately, bio-predictive methods can occupy a special niche in terms of supplementing plasma concentration data for regulatory approval.
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Affiliation(s)
- Mauricio A. García
- Department of Biopharmaceutics and Pharmaceutical Technology, Johannes Gutenberg University Mainz, 55099 Mainz, Germany; (M.A.G.); (J.A.-G.)
| | - Felipe Varum
- Pharmaceutical Research and Development, F. Hoffmann-La Roche Ltd., 4070 Basel, Switzerland; (F.V.); (M.H.); (S.P.)
| | - Jozef Al-Gousous
- Department of Biopharmaceutics and Pharmaceutical Technology, Johannes Gutenberg University Mainz, 55099 Mainz, Germany; (M.A.G.); (J.A.-G.)
- Department of Pharmaceutical Sciences, University of Michigan, 428 Church Street, Ann Arbor, MI 48109, USA
| | - Michael Hofmann
- Pharmaceutical Research and Development, F. Hoffmann-La Roche Ltd., 4070 Basel, Switzerland; (F.V.); (M.H.); (S.P.)
| | - Susanne Page
- Pharmaceutical Research and Development, F. Hoffmann-La Roche Ltd., 4070 Basel, Switzerland; (F.V.); (M.H.); (S.P.)
| | - Peter Langguth
- Department of Biopharmaceutics and Pharmaceutical Technology, Johannes Gutenberg University Mainz, 55099 Mainz, Germany; (M.A.G.); (J.A.-G.)
- Correspondence:
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21
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Hernalsteens S, Huang S, Cong HH, Chen XD. The final fate of food: On the establishment of in vitro colon models. Food Res Int 2021; 150:110743. [PMID: 34865762 DOI: 10.1016/j.foodres.2021.110743] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/04/2021] [Revised: 09/24/2021] [Accepted: 10/06/2021] [Indexed: 02/07/2023]
Abstract
The search for life/health quality has driven the search for a better understanding of food components on the overall individual health, which turns to be intrinsically related to the digestive system. In vitro digestion models are considered an alternative for the in vivo studies for a variety of practical reasons, but further research is still needed concerning the colon model establishment. An effective in vitro colon model should consider all unit operations and transport phenomena, together with chemical and biochemical reactions, material handling and reactor design. Due to the different techniques and dependence on the donor microbiota, it is difficult to obtain a standard protocol with results reproductible in time and space. Furthermore, the colon model should be fed with a representative substrate, thus what happens in upper digestion tract and absorption prior to colon is also of crucial importance. Essentially, there are two ways to think about how to achieve a good and useful in vitro colon model: a complex biomimetic system that provides results comparable with the in vivo studies or a simple system, that despite the fact it could not give physiologically relevant data, it is sufficient to understand the fate of some specific components.
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Affiliation(s)
- Saartje Hernalsteens
- College of Chemistry, Chemical Engineering and Materials Science - Soochow University, China.
| | | | - Hai Hua Cong
- College of Food Science and Engineering - Dalian Ocean University, China
| | - Xiao Dong Chen
- College of Chemistry, Chemical Engineering and Materials Science - Soochow University, China.
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22
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O'Farrell C, Stamatopoulos K, Simmons M, Batchelor H. In vitro models to evaluate ingestible devices: Present status and current trends. Adv Drug Deliv Rev 2021; 178:113924. [PMID: 34390774 DOI: 10.1016/j.addr.2021.113924] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2021] [Revised: 08/03/2021] [Accepted: 08/09/2021] [Indexed: 12/14/2022]
Abstract
Orally ingestible medical devices offer significant opportunity in the diagnosis and treatment of gastrointestinal conditions. Their development necessitates the use of models that simulate the gastrointestinal environment on both a macro and micro scale. An evolution in scientific technology has enabled a wide range of in vitro, ex vivo and in vivo models to be developed that replicate the gastrointestinal tract. This review describes the landscape of the existing range of in vitro tools that are available to characterize ingestible devices. Models are presented with details on their benefits and limitations with regards to the evaluation of ingestible devices and examples of their use in the evaluation of such devices is presented where available. The multitude of models available provides a suite of tools that can be used in the evaluation of ingestible devices that should be selected on the functionality of the device and the mechanism of its function.
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Affiliation(s)
- Connor O'Farrell
- School of Chemical Engineering, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
| | - Konstantinos Stamatopoulos
- School of Chemical Engineering, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK; Biopharmaceutics, Pharmaceutical Development, PDS, MST, RD Platform Technology & Science, GSK, David Jack Centre, Park Road, Ware, Hertfordshire SG12 0DP, UK
| | - Mark Simmons
- School of Chemical Engineering, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
| | - Hannah Batchelor
- Strathclyde Institute of Pharmacy and Biomedical Sciences, 161 Cathedral Street, Glasgow G4 0RE, UK.
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23
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Consistent Prebiotic Effects of Carrot RG-I on the Gut Microbiota of Four Human Adult Donors in the SHIME ® Model despite Baseline Individual Variability. Microorganisms 2021; 9:microorganisms9102142. [PMID: 34683463 PMCID: PMC8538933 DOI: 10.3390/microorganisms9102142] [Citation(s) in RCA: 13] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/05/2021] [Revised: 10/09/2021] [Accepted: 10/10/2021] [Indexed: 12/13/2022] Open
Abstract
The human gut microbiome is currently recognized to play a vital role in human biology and development, with diet as a major modulator. Therefore, novel indigestible polysaccharides that confer a health benefit upon their fermentation by the microbiome are under investigation. Based on the recently demonstrated prebiotic potential of a carrot-derived pectin extract enriched for rhamnogalacturonan I (cRG-I), the current study aimed to assess the impact of cRG-I upon repeated administration using the M-SHIME technology (3 weeks at 3g cRG-I/d). Consistent effects across four simulated adult donors included enhanced levels of acetate (+21.1 mM), propionate (+17.6 mM), and to a lesser extent butyrate (+4.1 mM), coinciding with a marked increase of OTUs related to Bacteroides dorei and Prevotella species with versatile enzymatic potential likely allowing them to serve as primary degraders of cRG-I. These Bacteroidetes members are able to produce succinate, explaining the consistent increase of an OTU related to the succinate-converting Phascolarctobacterium faecium (+0.47 log10(cells/mL)). While the Bifidobacteriaceae family remained unaffected, a specific OTU related to Bifidobacterium longum increased significantly upon cRG-I treatment (+1.32 log10(cells/mL)). Additional monoculture experiments suggested that Bifidobacterium species are unable to ferment cRG-I structures as such and that B. longum probably feeds on arabinan and galactan side chains of cRG-I, released by aforementioned Bacteroidetes members. Overall, this study confirms the prebiotic potential of cRG-I and additionally highlights the marked consistency of the microbial changes observed across simulated subjects, suggesting the involvement of a specialized consortium in cRG-I fermentation by the human gut microbiome.
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Duque ALRF, Demarqui FM, Santoni MM, Zanelli CF, Adorno MAT, Milenkovic D, Mesa V, Sivieri K. Effect of probiotic, prebiotic, and synbiotic on the gut microbiota of autistic children using an in vitro gut microbiome model. Food Res Int 2021; 149:110657. [PMID: 34600659 DOI: 10.1016/j.foodres.2021.110657] [Citation(s) in RCA: 21] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/05/2021] [Revised: 08/11/2021] [Accepted: 08/17/2021] [Indexed: 12/29/2022]
Abstract
Imbalances in gut microbiota composition occur in individuals with autism spectrum disorder (ASD). The administration of probiotics, prebiotics, and synbiotics is emerging as a potential and promising strategy for regulating the gut microbiota and improving ASD-related symptoms. We first investigated the survival of the probiotics Limosilactobacillus (L.) reuteri and Bifidobacterium (B.) longum alone, mixed and combined with a galacto-oligosaccharide (GOS) under simulated gastrointestinal conditions. Next, we evaluated the impact of probiotics (L. reuteri + B. longum), prebiotic (GOS), and synbiotic (L. reuteri + B. longum + GOS) on gut microbiota composition and metabolism of children with ASD using an in vitro fermentation model (SHIME®). The combination of L. reuteri, B. longum, and GOS showed elevated gastrointestinal resistance. The probiotic, prebiotic, and synbiotic treatments resulted in a positive modulation of the gut microbiota and metabolic activity of children with ASD. More specifically, the probiotic treatment increased the relative abundance of Lactobacillus, while the prebiotic treatment increased the relative abundance of Bifidobacterium and decreased the relative abundance of Lachnoclostridium. Changes in microbial metabolism were associated with increased short-chain fatty acid concentrations and reduced ammonium levels, particularly in the prebiotic and synbiotic treatments.
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Affiliation(s)
- Ana Luiza Rocha Faria Duque
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil
| | - Fernanda Manaia Demarqui
- Department of Biological Sciences, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil
| | - Mariana Marchi Santoni
- Department of Biological Sciences, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil
| | - Cleslei Fernando Zanelli
- Department of Biological Sciences, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil
| | - Maria Angela Tallarico Adorno
- Department of Hydraulics and Sanitation, School of Engineering of São Carlos, University of São Paulo (USP), São Carlos, Brazil
| | - Dragan Milenkovic
- Department of Internal Medicine, UC Davis School of Medicine, University of California, Davis, United States; INRAE, UNH, Université Clermont Auvergne, St Genes Champanelle, France
| | - Victoria Mesa
- Faculty of Pharmacy, Paris University, Paris, France; Food and Human Nutrition Research Group, University of Antioquia, Medellín, Colombia
| | - Katia Sivieri
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil.
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Griggs JL, Thomas DJ, Fry R, Bradham KD. Improving the predictive value of bioaccessibility assays and their use to provide mechanistic insights into bioavailability for toxic metals/metalloids - A research prospectus. JOURNAL OF TOXICOLOGY AND ENVIRONMENTAL HEALTH. PART B, CRITICAL REVIEWS 2021; 24:307-324. [PMID: 34092204 PMCID: PMC8390437 DOI: 10.1080/10937404.2021.1934764] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/25/2023]
Abstract
Widespread contamination of soil, dust, and food with toxic metal(loid)s pose a significant public health concern. Only a portion of orally ingested metal(loid) contaminants are bioavailable, which is defined as the fraction of ingested metal(loid)s absorbed across the gastrointestinal barrier and into systemic circulation. Bioaccessibility tools are a class of in vitro assays used as a surrogate to estimate risk of oral exposure and bioavailability. Although development and use of bioaccessibility tools have contributed to our understanding of the factors influencing oral bioavailability of metal(loid)s, some of these assays may lack data that support their use in decisions concerning adverse health risks and soil remediation. This review discusses the factors known to influence bioaccessibility of metal(loid) contaminants and evaluates experimental approaches and key findings of SW-846 Test Method 1340, Unified BARGE Method, Simulated Human Intestinal Microbial Ecosystem, Solubility Bioaccessibility Research Consortium assay, In Vitro Gastrointestinal model, TNO-Gastrointestinal Model, and Dutch National Institute for Public Health and the Environment bioaccessibility models which are used to assess oral absolute bioavailability and relative bioavailability in solid matrices. The aim of this review was to identify emerging knowledge gaps and research needs with an emphasis on research required to evaluate these models on (1) standardization of assay techniques and methodology, and (2) use of common criteria for assessing the performance of bioaccessibility models.
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Affiliation(s)
- Jennifer L Griggs
- Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
| | - David J Thomas
- Chemical Characterization and Exposure Division, Center for Computational Toxicology & Exposure, Office of Research and Development, U.S. Environmental Protection Agency, Research Triangle Park, NC, USA
| | - Rebecca Fry
- Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
| | - Karen D Bradham
- Watershed and Ecosystem Characterization Division, Center for Environmental Measurement and Modelling, Office of Research and Development, U.S. Environmental Protection Agency, Research Triangle Park, NC, USA
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Influence of Cultivation pH on Composition, Diversity, and Metabolic Production in an In Vitro Human Intestinal Microbiota. FERMENTATION-BASEL 2021. [DOI: 10.3390/fermentation7030156] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/07/2023]
Abstract
Fecal microbiota transplantation, an alternative treatment method for gastrointestinal diseases, has a high recovery rate, but comes with disadvantages, such as high donor requirements and the low storability of stool. A solution to overcome these problems is the cultivation of an in vitro microbiota. However, the influence of cultivation conditions on the pH are yet unknown. In this study, the influence of the cultivation pH (6.0–7.0) on the system’s behavior and characteristics, including cell count, metabolism, and microbial composition, was investigated. With an increasing cultivation pH, an increase in cell count, total amount of SCFAs, acetate, propionate, and the abundance of Bacteroidetes and Verrucomicrobia were observed. For the concentration of butyrate and the abundance of Actinobacteria and Firmicutes, a decrease with increasing pH was determined. For the concentration of isovalerate, the abundance of Proteobacteria and diversity (richness and Shannon effective), no effect of the pH was observed. Health-promoting genera were more abundant at lower pH levels. When cultivating an in vitro microbiota, all investigated pH values created a diverse and stable system. Ultimately, therefore, the choice of pH creates significant differences in the established in vitro microbiota, but no clear recommendations for a special value can be made.
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Lee S, Jo K, Jeong HG, Choi YS, Yong HI, Jung S. Understanding protein digestion in infants and the elderly: Current in vitro digestion models. Crit Rev Food Sci Nutr 2021; 63:975-992. [PMID: 34346822 DOI: 10.1080/10408398.2021.1957765] [Citation(s) in RCA: 25] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/20/2022]
Abstract
The last decades have witnessed a surge of interest in the fate of dietary proteins during gastrointestinal (GI) digestion. Although several in vitro digestion models are available as alternatives to clinical experiments, most of them focus on the digestive conditions of healthy young adults. This study investigates the static/dynamic models used to simulate digestion in infants and the elderly and considers the related in vivo conditions. The in vitro digestive protocols targeting these two groups are summarized, and the challenges associated with the further development of in vitro digestion models are discussed. Static models rely on several factors (e.g., enzyme concentration, pH, reaction time, and rotation speed) to differentiate digestive conditions depending on age. Dynamic models can more accurately simulate the complex digestion process and allow the inclusion of further parameters (sequential secretion of digestive fluids, gradual changes in pH, peristaltic mixing, GI emptying, and the inoculation of luminal microbiota). In the case of infants, age or growth stage clarification and the differentiation of digestive protocols between full-term and preterm infants are required, whereas protocols dealing with various health statuses are required in the case of the elderly, as this group is prone to oral cavity and GI function deterioration.
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Affiliation(s)
- Seonmin Lee
- Division of Animal and Dairy Science, Chungnam National University, Daejeon, Republic of Korea
| | - Kyung Jo
- Division of Animal and Dairy Science, Chungnam National University, Daejeon, Republic of Korea
| | - Hyun Gyung Jeong
- Division of Animal and Dairy Science, Chungnam National University, Daejeon, Republic of Korea
| | - Yun-Sang Choi
- Research Group of Food Processing, Korea Food Research Institute, Wanju, Republic of Korea
| | - Hae In Yong
- Research Group of Food Processing, Korea Food Research Institute, Wanju, Republic of Korea
| | - Samooel Jung
- Division of Animal and Dairy Science, Chungnam National University, Daejeon, Republic of Korea
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Vigsnaes LK, Ghyselinck J, Van den Abbeele P, McConnell B, Moens F, Marzorati M, Bajic D. 2'FL and LNnT Exert Antipathogenic Effects against C. difficile ATCC 9689 In Vitro, Coinciding with Increased Levels of Bifidobacteriaceae and/or Secondary Bile Acids. Pathogens 2021; 10:927. [PMID: 34451391 PMCID: PMC8402123 DOI: 10.3390/pathogens10080927] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/16/2021] [Revised: 07/19/2021] [Accepted: 07/20/2021] [Indexed: 12/13/2022] Open
Abstract
Clostridioides difficile (formerly Clostridium difficile) infection (CDI) is one of the most common hospital-acquired infections, which is often triggered by a dysbiosed indigenous gut microbiota (e.g., upon antibiotic therapy). Symptoms can be as severe as life-threatening colitis. The current study assessed the antipathogenic potential of human milk oligosaccharides (HMOs), i.e., 2'-O-fucosyllactose (2'FL), lacto-N-neotetraose (LNnT), and a combination thereof (MIX), against C. difficile ATCC 9689 using in vitro gut models that allowed the evaluation of both direct and, upon microbiota modulation, indirect effects. During a first 48 h fecal batch study, dysbiosis and CDI were induced by dilution of the fecal inoculum. For each of the three donors tested, C. difficile levels strongly decreased (with >4 log CFU/mL) upon treatment with 2'FL, LNnT and MIX versus untreated blanks, coinciding with increased acetate/Bifidobacteriaceae levels. Interindividual differences among donors at an intermediate time point suggested that the antimicrobial effect was microbiota-mediated rather than being a direct effect of the HMOs. During a subsequent 11 week study with the PathogutTM model (specific application of the Simulator of the Human Intestinal Microbial Ecosystem (SHIME®)), dysbiosis and CDI were induced by clindamycin (CLI) treatment. Vancomycin (VNC) treatment cured CDI, but the further dysbiosis of the indigenous microbiota likely contributed to CDI recurrence. Upon co-supplementation with VNC, both 2'FL and MIX boosted microbial activity (acetate and to lesser extent propionate/butyrate). Moreover, 2'FL avoided CDI recurrence, potentially because of increased secondary bile acid production. Overall, while not elucidating the exact antipathogenic mechanisms-of-action, the current study highlights the potential of HMOs to combat CDI recurrence, help the gut microbial community recover after antibiotic treatment, and hence counteract the adverse effects of antibiotic therapies.
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Affiliation(s)
- Louise Kristine Vigsnaes
- Glycom A/S—DSM Nutritional Products Ltd., Kogle Allé 4, DK-2970 Hørsholm, Denmark; (L.K.V.); (B.M.)
- Department of Technology, Faculty of Health, University College Copenhagen, DK-2200 Copenhagen, Denmark
| | | | - Pieter Van den Abbeele
- ProDigest, 9052 Ghent, Belgium; (J.G.); (F.M.); (M.M.)
- Cryptobiotix, 9052 Ghent, Belgium;
| | - Bruce McConnell
- Glycom A/S—DSM Nutritional Products Ltd., Kogle Allé 4, DK-2970 Hørsholm, Denmark; (L.K.V.); (B.M.)
| | | | - Massimo Marzorati
- ProDigest, 9052 Ghent, Belgium; (J.G.); (F.M.); (M.M.)
- Center of Microbial Ecology and Technology (CMET), Ghent University, 9000 Ghent, Belgium
| | - Danica Bajic
- Glycom A/S—DSM Nutritional Products Ltd., Kogle Allé 4, DK-2970 Hørsholm, Denmark; (L.K.V.); (B.M.)
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Machado Ribeiro TR, Salgaço MK, Adorno MAT, da Silva MA, Piazza RMF, Sivieri K, Moreira CG. Human microbiota modulation via QseC sensor kinase mediated in the Escherichia coli O104:H4 outbreak strain infection in microbiome model. BMC Microbiol 2021; 21:163. [PMID: 34078285 PMCID: PMC8170955 DOI: 10.1186/s12866-021-02220-3] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/11/2020] [Accepted: 05/06/2021] [Indexed: 01/01/2023] Open
Abstract
Background The intestinal microbiota plays a crucial role in human health, adjusting its composition and the microbial metabolites protects the gut against invading microorganisms. Enteroaggregative E. coli (EAEC) is an important diarrheagenic pathogen, which may cause acute or persistent diarrhea (≥14 days). The outbreak strain has the potent Shiga toxin, forms a dense biofilm and communicate via QseBC two-component system regulating the expression of many important virulence factors. Results Herein, we investigated the QseC histidine sensor kinase role in the microbiota shift during O104:H4 C227–11 infection in the colonic model SHIME® (Simulator of the Human Intestinal Microbial Ecosystem) and in vivo mice model. The microbiota imbalance caused by C227–11 infection affected ỿ-Proteobacteria and Lactobacillus spp. predominance, with direct alteration in intestinal metabolites driven by microbiota change, such as Short-chain fatty acids (SCFA). However, in the absence of QseC sensor kinase, the microbiota recovery was delayed on day 3 p.i., with change in the intestinal production of SCFA, like an increase in acetate production. The higher predominance of Lactobacillus spp. in the microbiota and significant augmented qseC gene expression levels were also observed during C227–11 mice infection upon intestinal depletion. Novel insights during pathogenic bacteria infection with the intestinal microbiota were observed. The QseC kinase sensor seems to have a role in the microbiota shift during the infectious process by Shiga toxin-producing EAEC C227–11. Conclusions The QseC role in C227–11 infection helps to unravel the intestine microbiota modulation and its metabolites during SHIME® and in vivo models, besides they contribute to elucidate bacterial intestinal pathogenesis and the microbiota relationships. Supplementary Information The online version contains supplementary material available at 10.1186/s12866-021-02220-3.
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Affiliation(s)
- Tamara Renata Machado Ribeiro
- Department of Biological Sciences, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP, Brazil
| | - Mateus Kawata Salgaço
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP, Brazil
| | - Maria Angela Tallarico Adorno
- Department of Hydraulics and Sanitation, School of Engineering of São Carlos, University of São Paulo (USP), São Carlos, SP, Brazil
| | | | | | - Katia Sivieri
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP, Brazil
| | - Cristiano Gallina Moreira
- Department of Biological Sciences, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP, Brazil.
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30
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Roupar D, Berni P, Martins JT, Caetano AC, Teixeira JA, Nobre C. Bioengineering approaches to simulate human colon microbiome ecosystem. Trends Food Sci Technol 2021. [DOI: 10.1016/j.tifs.2021.04.035] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/14/2022]
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31
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Oliveira AS, Niro CM, Bresolin JD, Soares VF, Ferreira MD, Sivieri K, Azeredo HM. Dehydrated strawberries for probiotic delivery: Influence of dehydration and probiotic incorporation methods. Lebensm Wiss Technol 2021. [DOI: 10.1016/j.lwt.2021.111105] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
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Blanco-Morales V, Garcia-Llatas G, Yebra MJ, Sentandreu V, Alegría A. In vitro colonic fermentation of a plant sterol-enriched beverage in a dynamic-colonic gastrointestinal digester. Lebensm Wiss Technol 2021. [DOI: 10.1016/j.lwt.2021.111273] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023]
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Salgaço MK, Perina NP, Tomé TM, Mosquera EMB, Lazarini T, Sartoratto A, Sivieri K. Probiotic infant cereal improves children's gut microbiota: Insights using the Simulator of Human Intestinal Microbial Ecosystem (SHIME®). Food Res Int 2021; 143:110292. [PMID: 33992391 DOI: 10.1016/j.foodres.2021.110292] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/22/2020] [Revised: 02/27/2021] [Accepted: 02/27/2021] [Indexed: 02/08/2023]
Abstract
Infant́s gut microbiota can be modulated by many factors, including mode of delivery, feeding regime, maternal diet/weight and probiotic and prebiotic consumption. The gut microbiota in dysbiosis has been associated with innumerous diseases. In this sense, early childhood intestinal microbiome modulation can be a strategy for disease prevention. This study had the purpose to evaluate the effect of an infant cereal with probiotic (Bifidobacterium animalis ssp. lactis BB-12®) on infant́s intestinal microbiota using SHIME®, which simulates human gastrointestinal conditions. The ascending colon was inoculated with fecal microbiota from three children (2-3 years old). NH4+, short chain fatty acids (SCFASs) and microbiota composition were determined by selective ion electrode, GC/MS and 16S sequencing, respectively. After treatment, butyric acid production increased (p < 0.05) 52% and a decrease in NH4+ production was observed (p < 0.01). The treatment stimulated an increase (p < 0.01) of Lactobacillaceae families, more precisely L. gasseri and L. kefiri. L. gasseri has been associated with the prevention of allergic rhinitis in children and L. kefiri in the prevention of obesity. Thus, infant cereal with BB-12® is able to stimulate the growth of L. gasseri and L. kefiri in a beneficial way, reducing NH4+ and increasing the production of SCFAs, especially butyric acid, in SHIME®.
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Affiliation(s)
- Mateus Kawata Salgaço
- Department of Food and Nutrition, School of Pharmaceutical Science, São Paulo State University-UNESP, Araraquara, São Paulo, Brazil
| | - Natália Partis Perina
- Medical, Scientific and Regulatory Affairs - Nestlé Nutrition/Nestlé Brazil Ltda, São Paulo, Brazil
| | - Thaís Moreno Tomé
- Medical, Scientific and Regulatory Affairs - Nestlé Nutrition/Nestlé Brazil Ltda, São Paulo, Brazil
| | | | - Tamara Lazarini
- Medical, Scientific and Regulatory Affairs - Nestlé Nutrition/Nestlé Brazil Ltda, São Paulo, Brazil
| | | | - Katia Sivieri
- Department of Food and Nutrition, School of Pharmaceutical Science, São Paulo State University-UNESP, Araraquara, São Paulo, Brazil.
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Haindl R, Engel J, Kulozik U. Establishment of an In Vitro System of the Human Intestinal Microbiota: Effect of Cultivation Conditions and Influence of Three Donor Stool Samples. Microorganisms 2021; 9:1049. [PMID: 34068085 PMCID: PMC8152740 DOI: 10.3390/microorganisms9051049] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/06/2021] [Revised: 05/07/2021] [Accepted: 05/08/2021] [Indexed: 11/16/2022] Open
Abstract
Fecal microbiota transplantation (FMT) is an alternative method for the treatment of gastrointestinal diseases with a high recovery rate. Disadvantages are ethical concerns, high donor requirements and the low storability of stool samples. The cultivation of an in vitro microbiota in a continuous bioreactor was established as an alternative to FMT to overcome these problems. In this study, the influence of the system parameters and donor stool characteristics was investigated. Each continuous colonic fermentation system was inoculated with feces from three different donors until a stable state was established. The influence of the fermentation conditions on the system's behavior regarding cell count, metabolic activity, short-chain fatty acid profile and microbiota composition as well as richness and diversity was assessed. Cultivation conditions were found to affect the microbial system: the number of cells and the production of short-chain fatty acids increased. The abundance of Actinobacteria and Firmicutes decreased, Bacteroidetes increased, while Proteobacteria and Verrucomicrobia remained largely unaffected. Diversity in the in vitro system decreased, but richness was unaffected. The cultivation of stool from different donors revealed that the performance of the created in vitro system was similar and comparable, but unique characteristics of the composition of the original stool remained.
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Affiliation(s)
- Regina Haindl
- Chair of Food and Bioprocess Engineering, ZIEL—Institute for Food & Health, Technical University of Munich, Weihenstephaner Berg 1, 85354 Freising, Germany; (J.E.); (U.K.)
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Garcia-Ibañez P, Roses C, Agudelo A, Milagro FI, Barceló AM, Viadel B, Nieto JA, Moreno DA, Carvajal M. The Influence of Red Cabbage Extract Nanoencapsulated with Brassica Plasma Membrane Vesicles on the Gut Microbiome of Obese Volunteers. Foods 2021; 10:foods10051038. [PMID: 34068672 PMCID: PMC8151636 DOI: 10.3390/foods10051038] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/23/2021] [Revised: 04/30/2021] [Accepted: 05/07/2021] [Indexed: 12/28/2022] Open
Abstract
The aim of the study was to evaluate the influence of the red cabbage extracts on the bioaccessibility of their isothiocyanates, and their effect on the intestinal microbiota using a dynamic model of human digestion treated with the gut microbiome of obese adults. The elicitation of red cabbage plants with methyl jasmonate (MeJA) duplicated the content of glucosinolates (GSLs) in the plant organs used for elaborating the encapsulated formula. The use of plasma membrane vesicles, according to a proper methodology and technology, showed a high retention of sulforaphane (SFN) and indol-3-carbinol (I3C) over the course of the 14-day digestion study. The microbiome was scarcely affected by the treatments in terms of microbiota composition or the Bacteroidetes/Firmicutes ratio, but a 3 to 4-fold increase was observed in the production of butyric acid with the encapsulated extract treatment. Based on our pilot red cabbage extract study, the consumption of this extract, mainly encapsulated, may play a potential role in the management of obesity in adults.
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Affiliation(s)
- Paula Garcia-Ibañez
- Aquaporins Group, Centro de Edafología y Biología Aplicada del Segura, CEBAS-CSIC, Campus Universitario de Espinardo-25, E-30100 Murcia, Spain; (P.G.-I.); (M.C.)
- Phytochemistry and Healthy Foods Lab, Department of Food Science Technology, Centro de Edafología y Biología Aplicada del Segura, CEBAS-CSIC, Campus de Espinardo-25, E-30100 Murcia, Spain
| | - Carles Roses
- Servei de Genòmica I Bioinformàtica, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain; (C.R.); (A.M.B.)
| | - Agatha Agudelo
- Sakata Seed Ibérica S.L., Pl. Poeta Vicente Gaos, 6 Bajo, 46021 Valencia, Spain;
- Biotechnology Department, Universidad Politécnica de Valencia, UPV, Camino de Vera s/n, 46022 Valencia, Spain
| | - Fermin I. Milagro
- Center for Nutrition Research, Department of Nutrition, Food Sciences and Physiology, University of Navarra, 31008 Pamplona, Spain;
- Navarra Institute for Health Research (IdISNA), 31008 Pamplona, Spain
- Centro de Investigación Biomédica en Red de la Fisiopatología de la Obesidad y Nutrición (CIBERobn), Instituto de la Salud Carlos III, 289029 Madrid, Spain
| | - Ana M. Barceló
- Servei de Genòmica I Bioinformàtica, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain; (C.R.); (A.M.B.)
| | - Blanca Viadel
- AINIA, Technology Centre, C/Benjamin Franklin 5-11, Parque Tecnológico de Valencia, 46980 Paterna, Valencia, Spain; (B.V.); (J.A.N.)
| | - Juan Antonio Nieto
- AINIA, Technology Centre, C/Benjamin Franklin 5-11, Parque Tecnológico de Valencia, 46980 Paterna, Valencia, Spain; (B.V.); (J.A.N.)
| | - Diego A. Moreno
- Phytochemistry and Healthy Foods Lab, Department of Food Science Technology, Centro de Edafología y Biología Aplicada del Segura, CEBAS-CSIC, Campus de Espinardo-25, E-30100 Murcia, Spain
- Correspondence:
| | - Micaela Carvajal
- Aquaporins Group, Centro de Edafología y Biología Aplicada del Segura, CEBAS-CSIC, Campus Universitario de Espinardo-25, E-30100 Murcia, Spain; (P.G.-I.); (M.C.)
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Fernández-Jalao I, Balderas C, Calvo MV, Fontecha J, Sánchez-Moreno C, De Ancos B. Impact of High-Pressure Processed Onion on Colonic Metabolism Using a Dynamic Gastrointestinal Digestion Simulator. Metabolites 2021; 11:metabo11050262. [PMID: 33922352 PMCID: PMC8145356 DOI: 10.3390/metabo11050262] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2021] [Revised: 04/19/2021] [Accepted: 04/20/2021] [Indexed: 02/07/2023] Open
Abstract
Onions are the main dietary source of flavonols that have been associated with important health-promoting properties. Onion treated by high-pressure processing (HPP-treated onion) was subjected to a dynamic gastrointestinal digestion and colon fermentation simulator (DGID-CF) to study the effect on the gut microbiota metabolism in the three colon regions (ascending—AC, transverse—TC, and descending—DC) by means of chronic feeding with 27 g/day for 14 days. HPP-treated onion presented a high content of the flavonols quercetin-3,4’-diglucoside and quercetin-4’-glucoside, and a large percentage of them reached the AC without change. TC and DC progressively increased the total phenolic metabolites 2.5 times respective to day 2, mainly 3-hydroxyphenylacetic, 4-hydroxyphenylacetic, 3-(4-hydroxyphenyl)-propionic, and 3,4-dihydroxyphenylpropionic acids. In addition, the chronic feeding increased the beneficial colon bacteria Bifidobacterium spp. and Lactobacillus spp. and the production of total SCFAs (acetic, propionic, and butyric acids) 9 times (AC), 2.2 times (TC), and 4.4 times (DC) respective to day 1. A multivariate analysis (principal component analysis, PCA) showed a clear separation between the three colon regions based on their phenolic composition (precursors and metabolites). These results showed that HPP-treated onion modulated the human gut microbiota’s metabolism and the DGID-CF is a good system to study these changes.
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Affiliation(s)
- Irene Fernández-Jalao
- Department of Characterization, Quality and Safety, Institute of Food Science, Technology and Nutrition (ICTAN-CSIC), 28040 Madrid, Spain; (I.F.-J.); (C.B.); (C.S.-M.)
| | - Claudia Balderas
- Department of Characterization, Quality and Safety, Institute of Food Science, Technology and Nutrition (ICTAN-CSIC), 28040 Madrid, Spain; (I.F.-J.); (C.B.); (C.S.-M.)
| | - María V. Calvo
- Department of Bioactivity and Food Analysis, Institute of Food Science Research (CIAL, CSIC-UAM), 28049 Madrid, Spain; (M.V.C.); (J.F.)
| | - Javier Fontecha
- Department of Bioactivity and Food Analysis, Institute of Food Science Research (CIAL, CSIC-UAM), 28049 Madrid, Spain; (M.V.C.); (J.F.)
| | - Concepción Sánchez-Moreno
- Department of Characterization, Quality and Safety, Institute of Food Science, Technology and Nutrition (ICTAN-CSIC), 28040 Madrid, Spain; (I.F.-J.); (C.B.); (C.S.-M.)
| | - Begoña De Ancos
- Department of Characterization, Quality and Safety, Institute of Food Science, Technology and Nutrition (ICTAN-CSIC), 28040 Madrid, Spain; (I.F.-J.); (C.B.); (C.S.-M.)
- Correspondence: ; Tel.: +34-915-492-300
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Vanhoutte I, Vande Ginste J, Verstringe S, Vidal A, De Boevre M, De Saeger S, Audenaert K, De Gelder L. Development of an in vitro gastro-intestinal pig model to screen potential detoxifying agents for the mycotoxin deoxynivalenol. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2021; 38:488-500. [PMID: 33480829 DOI: 10.1080/19440049.2020.1865577] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/22/2022]
Abstract
Deoxynivalenol (DON) is a type B trichothecene mycotoxin with worldwide high incidence in feed which is produced by Fusarium species. Strategies are needed to eliminate its health risk for livestock and to minimise its economic impact on production. In order to assess the efficacy of potential physical, chemical and biological DON detoxifying agents, a good in vitro model is necessary to perform a fast and high-throughput screening of new compounds before in vivo trials are set up. In this paper, an in vitro model was developed to screen potential commercial products for DON degradation and detoxification. Contaminated feed with potential detoxifying agents are first applied to a simulated gastrointestinal tract (GIT) of a pig, after which detoxification is assessed through a robust, inexpensive and readily applicable Lemna minor L. aquatic plant bioassay which enables evaluation of the residual toxicity of possible metabolites formed by DON detoxifying agents. The GIT simulation enables taking matrix and incubation parameters into account as they can affect the binding, removal or degradation of DON. One product could reduce DON in feed in the GIT model for almost 100% after 6 h. DON metabolites were tentatively identified with LC-MS/MS. This GIT simulation coupled to a detoxification bioassay is a valuable model for in vitro screening and assessing compounds for DON detoxification, and could be expanded towards other mycotoxins.
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Affiliation(s)
- Ilse Vanhoutte
- Laboratory of Environmental Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
| | | | | | - Arnau Vidal
- Centre of Excellence in Mycotoxicology and Public Health, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
| | - Marthe De Boevre
- Centre of Excellence in Mycotoxicology and Public Health, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
| | - Sarah De Saeger
- Centre of Excellence in Mycotoxicology and Public Health, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
| | - Kris Audenaert
- Laboratory of Applied Mycology and Phenomics, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
| | - Leen De Gelder
- Laboratory of Environmental Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
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38
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Use of static and dynamic in vitro models to simulate Prato cheese gastrointestinal digestion: Effect of Lactobacillus helveticus LH-B02 addition on peptides bioaccessibility. Lebensm Wiss Technol 2020. [DOI: 10.1016/j.lwt.2020.110229] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/10/2023]
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39
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Roselino MN, Sakamoto IK, Tallarico Adorno MA, Márcia Canaan JM, de Valdez GF, Rossi EA, Sivieri K, Umbelino Cavallini DC. Effect of fermented sausages with probiotic Enterococcus faecium CRL 183 on gut microbiota using dynamic colonic model. Lebensm Wiss Technol 2020. [DOI: 10.1016/j.lwt.2020.109876] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/08/2023]
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Oddi S, Huber P, Rocha Faria Duque AL, Vinderola G, Sivieri K. Breast-milk derived potential probiotics as strategy for the management of childhood obesity. Food Res Int 2020; 137:109673. [PMID: 33233250 DOI: 10.1016/j.foodres.2020.109673] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/21/2020] [Revised: 08/10/2020] [Accepted: 09/06/2020] [Indexed: 12/18/2022]
Abstract
Obesity and overweight, and their concomitant metabolic diseases, emerge as one of the most severe health problems in the world. Prevention and management of obesity are proposed to begin early in childhood, when probiotics may have a role. The Simulator of the Human Intestinal Microbial Ecosystem (SHIME®), in a dynamic validated in vitro system able to simulate the different parts of the gastrointestinal tract, has proven to be useful in analyzing the human intestinal microbial community. L. plantarum 73a and B. animalis subsp. lactis INL1, two strains isolated from breast milk, were assayed in the SHIME® using the fecal microbiota of an obese child. L. plantarum 73a alone or in combination with B. animalis subsp. lactis INL1 demonstrated survival capacity in the SHIME® system. The administration of both strains increased the alpha diversity of the microbiota and reduced the levels of the phylum Proteobacteria. In particular, the genera Escherichia, Shigella, and Clostridium_sensu_stricto_1 were significantly reduced when both strains were administered. The increase of Proteobacteria phylum is generally associated with the microbiota of obese people. Escherichia and Shigellacan be involved in inflammation-dependent adiposity and insulin resistance. L. plantarum73a supplementation reduced ammonia production. L. plantarum 73a alone or in combination with B. animalis subsp. lactis INL1 are potential probiotic candidates for the management of infant obesity.
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Affiliation(s)
- S Oddi
- Instituto de Lactología Industrial (INLAIN, UNL-CONICET), Facultad de Ingeniería Química, Universidad Nacional del Litoral, Santa Fe, Argentina
| | - P Huber
- Laboratorio de Plancton, Instituto Nacional de Limnología (INALI, UNL-CONICET), Universidad Nacional del Litoral, Santa Fe, Argentina
| | - A L Rocha Faria Duque
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara 9 SP 14800-903, Brazil
| | - G Vinderola
- Instituto de Lactología Industrial (INLAIN, UNL-CONICET), Facultad de Ingeniería Química, Universidad Nacional del Litoral, Santa Fe, Argentina.
| | - K Sivieri
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara 9 SP 14800-903, Brazil
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41
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Probiotic low-fat fermented goat milk with passion fruit by-product: In vitro effect on obese individuals' microbiota and on metabolites production. Food Res Int 2020; 136:109453. [PMID: 32846548 DOI: 10.1016/j.foodres.2020.109453] [Citation(s) in RCA: 16] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/30/2019] [Revised: 06/12/2020] [Accepted: 06/14/2020] [Indexed: 12/19/2022]
Abstract
This study aimed to evaluate the impact of a two-week treatment period with probiotic low-fat fermented goat milk by Lactobacillus casei Lc-1, supplemented with passion fruit by-product (1%), on the modulation of gut microbiota from obese individuals using the Simulator of Human Intestinal Microbial Ecosystem (SHIME) system. The effects were carried out through the study of gut microbiota composition, using 16S rRNA next generation sequencing, quantification of short-chain fatty acids (SCFA) and ammonium ions. The microbiota composition changed across three vessels representing the colon regions, because of fermented milk treatment. Fermented goat milk administration caused a reduction of bacteria belonging to genera Prevotella, Megamonas and Succinivibrio, which can produce SCFA, and an increase of Lactobacillus and Bifidobacterium genera in all simulated colon regions. There was no effect on SCFA and on ammonium ions concentration during treatment period. Fermented milk shifted the obese donors' microbiota without changing metabolites production. It happens, possibly, due to a balance in abundances among bacterial genera that can produce or not SCFA, and among bacterial genera with high or low proteolytic activity. Our outcomes help to clarify the effects of the ingestion of a probiotic low-fat fermented goat milk product on colon microbiota composition.
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42
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Lockyer S, Aguirre M, Durrant L, Pot B, Suzuki K. The role of probiotics on the roadmap to a healthy microbiota: a symposium report. GUT MICROBIOME (CAMBRIDGE, ENGLAND) 2020; 1:e2. [PMID: 39296722 PMCID: PMC11406418 DOI: 10.1017/gmb.2020.2] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/16/2020] [Revised: 04/23/2020] [Accepted: 05/01/2020] [Indexed: 09/21/2024]
Abstract
The ninth International Yakult Symposium was held in Ghent, Belgium in April 2018. Keynote lectures were from Professor Wijmenga on using biobanks to understand the relationship between the gut microbiota and health; and Professor Hill on phage-probiotic interactions. Session one included talks from Professor Plӧsch on epigenetic programming by nutritional and environmental factors; Professor Wilmes on the use of "omics" methodologies in microbiome research and Professor Rescigno on the gut vascular barrier. Session two explored the evidence behind Lactobacillus casei Shirota with Dr Nanno explaining the plasticity in immunomodulation that enables the strain to balance immune functions; Dr Macnaughtan outlining its potential therapeutic use in cirrhosis and Professor Nishida detailing effects in subjects under stress. The third session saw Professor Marchesi describing that both the host genes and the gut microbiota can play a role in cancer; Professor Bergheim highlighting crosstalk between the gut and the liver and Professor Cani describing the relationship between the gut microbiota and the endocrine system. The final session explored probiotic mechanisms, with Professor Lebeer dissecting the challenges in conducting mechanistic studies; Professor Wehkamp describing the mucosal defence system and Professor Van de Wiele detailing methods for modelling the gut microbiota in vitro.
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Affiliation(s)
| | | | | | - Bruno Pot
- Yakult Europe B.V., Almere, The Netherlands
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43
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Boling L, Cuevas DA, Grasis JA, Kang HS, Knowles B, Levi K, Maughan H, McNair K, Rojas MI, Sanchez SE, Smurthwaite C, Rohwer F. Dietary prophage inducers and antimicrobials: toward landscaping the human gut microbiome. Gut Microbes 2020; 11:721-734. [PMID: 31931655 PMCID: PMC7524278 DOI: 10.1080/19490976.2019.1701353] [Citation(s) in RCA: 65] [Impact Index Per Article: 13.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/03/2023] Open
Abstract
The approximately 1011 viruses and microbial cells per gram of fecal matter (dry weight) in the large intestine are important to human health. The responses of three common gut bacteria species, and one opportunistic pathogen, to 117 commonly consumed foods, chemical additives, and plant extracts were tested. Many compounds, including Stevia rebaudiana and bee propolis extracts, exhibited species-specific growth inhibition by prophage induction. Overall, these results show that various foods may change the abundances of gut bacteria by modulating temperate phage and suggests a novel path for landscaping the human gut microbiome.
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Affiliation(s)
- Lance Boling
- Department of Biology, San Diego State University, San Diego, CA, USA,CONTACT Lance Boling Department of Biology, San Diego State University, LS301, 5500 Campanile Dr, San Diego, CA92182USA
| | - Daniel A. Cuevas
- Computational Sciences Research Center, San Diego State University, San Diego, CA, USA
| | - Juris A. Grasis
- Department of Biology, San Diego State University, San Diego, CA, USA
| | - Han Suh Kang
- Department of Biology, San Diego State University, San Diego, CA, USA
| | - Ben Knowles
- Department of Biology, San Diego State University, San Diego, CA, USA
| | - Kyle Levi
- Department of Computer Science, San Diego State University, San Diego, CA, USA
| | | | - Katelyn McNair
- Department of Biology, San Diego State University, San Diego, CA, USA,Department of Computer Science, San Diego State University, San Diego, CA, USA
| | | | | | | | - Forest Rohwer
- Department of Biology, San Diego State University, San Diego, CA, USA
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44
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Hao Z, Li L, Ning Z, Zhang X, Mayne J, Cheng K, Walker K, Liu H, Figeys D. Metaproteomics Reveals Growth Phase-Dependent Responses of an In Vitro Gut Microbiota to Metformin. JOURNAL OF THE AMERICAN SOCIETY FOR MASS SPECTROMETRY 2020; 31:1448-1458. [PMID: 32320607 DOI: 10.1021/jasms.0c00054] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 05/20/2023]
Abstract
Metaproteomics has been used in combination with in vitro gut microbiota models to study drug-microbiome interactions. However, it remains unexplored whether the metaproteomics profile of in vitro gut microbiota responds differently to a same stimulus added at different growth phases. In this study, we cultured a human gut microbiota in 96-deep well plates using a previously validated model. Metformin was added during the lag, log, and stationary phases. Microbiome samples, collected at different time points, were analyzed by optical density and function by metaproteomic. The in vitro gut microbiota growth curves, taxonomy, and functional responses were different depending whether metformin was added during the lag, log, or stationary phases. The addition of drugs at the log phase may lead to the greatest decline of bacterial growth. Metaproteomic analysis suggests that the strength of the metformin effect on the gut microbiome functional profile may be ranked as lag phase > log phase > stationary phase. Metformin added at the lag phase may result in a significantly reduced level of the Clostridiales order and an increased level of the Bacteroides genus, which is different from stimulations during the rest of the growth phases. Metformin may also result in alterations of several pathways, including energy production and conversion, lipid transport and metabolism, translation, ribosomal structure, and biogenesis. Our results indicate that the timing for drug stimulation should be considered when studying drug-microbiome interactions in vitro.
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Affiliation(s)
- Zikai Hao
- Beijing Advanced Innovation Centre for Biomedical Engineering, Beihang University, Beijing 100083, China
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
- School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, China
| | - Leyuan Li
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
| | - Zhibin Ning
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
| | - Xu Zhang
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
| | - Janice Mayne
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
| | - Kai Cheng
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
| | - Krystal Walker
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
| | - Hong Liu
- Beijing Advanced Innovation Centre for Biomedical Engineering, Beihang University, Beijing 100083, China
- School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, China
| | - Daniel Figeys
- Beijing Advanced Innovation Centre for Biomedical Engineering, Beihang University, Beijing 100083, China
- Department of Biochemistry, Microbiology and Immunology, Ottawa Institute of Systems Biology, Faculty of Medicine, University of Ottawa, Ottawa K1H 8M5, Canada
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45
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Microplastics as Vectors of Chromium and Lead during Dynamic Simulation of the Human Gastrointestinal Tract. SUSTAINABILITY 2020. [DOI: 10.3390/su12114792] [Citation(s) in RCA: 28] [Impact Index Per Article: 5.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/20/2022]
Abstract
The human body is exposed to the ingestion of microplastics that are often contaminated with other substances, which can be released into our body. In this work, a dynamic in-vitro simulator of the gastrointestinal tract based on a membrane reactor has been used for the first time to study the release, bioaccessibility, and bioavailability of chromium (Cr) and lead (Pb) from polyethylene and polypropylene microplastics previously contaminated in the laboratory. The results showed that 23.11% of the initial Cr and 23.17% of the initial Pb present in microplastics were able to cross the tubular membrane, simulating the intestinal absorption phase. The pH evolution during the gastric phase and the duodenal phase, the interaction mechanisms with physiological fluids, and the properties of the polymers, such as specific surface, porosity, and/or surface degradation, affected the kinetics of release from the microplastics and the behavior of both heavy metals. Cr was released very early in the gastric phase, but also began simultaneously to precipitate quite fast, while Pb was released slower and in less quantity than Cr, and did not precipitate until the beginning of the duodenal phase. This study shows, for the first time, how useful the dynamic gastrointestinal simulator is to study the behavior of microplastics and some problematic heavy metals along the human gastrointestinal tract, and can serve as a reference for future studies focused on the effects of these substances in the human body.
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46
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Dufourny S, Everaert N, Lebrun S, Didelez M, Wavreille J, Froidmont E, Rondia P, Delcenserie V. Oxygen as a key parameter in in vitro dynamic and multi-compartment models to improve microbiome studies of the small intestine? Food Res Int 2020; 133:109127. [PMID: 32466899 DOI: 10.1016/j.foodres.2020.109127] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/06/2019] [Revised: 01/10/2020] [Accepted: 02/24/2020] [Indexed: 11/13/2022]
Abstract
In vitro digestion and fermentation models are frequently used for human and animal research purposes. Different dynamic and multi-compartment models exist, but none have been validated with representative microbiota in the distal parts of the small intestine. We recently developed a dynamic and multi-compartment piglet model introducing microbiota in an ileum bioreactor. However, it presented discrepancies compared to in vivo data. Recommendations are available to standardize studies in this field. They target the digestion model but include elements of a fermentation model. But no recommendation is given concerning control of the atmosphere. The gastrointestinal tract is generally associated with anaerobiosis to conduct a good fermentation process. In this study, we attempted to improve the ileal microbiota of the piglet model by testing inoculation: real intestinal content vs feces; the latter being generally used for ethical and economical aspects. Results showed a positive effect of using real intestinal content. Fusobacteriia were less abundant in the model, Bacteroidia were better maintained in the colon. But for the ileum, results showed that anoxic conditions in the ileum bioreactor conditioned the microbial profile probably more than the type of inoculum itself, leading to the general conclusion that in vitro dynamic and multi-compartment models probably have to get oxygenated to improve microbiome studies of the small intestine.
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Affiliation(s)
- S Dufourny
- Animal Nutrition and Sustainability Unit, Production and Sectors Department, Walloon Agricultural Research Centre, Rue de Liroux 8, B-5030 Gembloux, Belgium.
| | - N Everaert
- Precision Livestock and Nutrition Unit, AgroBioChem Department, TERRA Teaching and Research Centre, University of Liège, Passage des Déportés 2, B-5030 Gembloux, Belgium.
| | - S Lebrun
- Food Quality Management, Food Science Department, FARAH, University of Liège, Avenue de Cureghem 10, B-4000 Liège, Belgium.
| | - M Didelez
- Animal Nutrition and Sustainability Unit, Production and Sectors Department, Walloon Agricultural Research Centre, Rue de Liroux 8, B-5030 Gembloux, Belgium.
| | - J Wavreille
- Animal Breeding, Quality Production and Welfare Unit, Production and Sectors Department, Walloon Agricultural Research Centre, Rue de Liroux 8, B-5030 Gembloux, Belgium.
| | - E Froidmont
- Animal Nutrition and Sustainability Unit, Production and Sectors Department, Walloon Agricultural Research Centre, Rue de Liroux 8, B-5030 Gembloux, Belgium.
| | - P Rondia
- Animal Nutrition and Sustainability Unit, Production and Sectors Department, Walloon Agricultural Research Centre, Rue de Liroux 8, B-5030 Gembloux, Belgium.
| | - V Delcenserie
- Food Quality Management, Food Science Department, FARAH, University of Liège, Avenue de Cureghem 10, B-4000 Liège, Belgium.
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47
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Yin N, Cai X, Zheng L, Du H, Wang P, Sun G, Cui Y. In Vitro Assessment of Arsenic Release and Transformation from As(V)-Sorbed Goethite and Jarosite: The Influence of Human Gut Microbiota. ENVIRONMENTAL SCIENCE & TECHNOLOGY 2020; 54:4432-4442. [PMID: 32176848 DOI: 10.1021/acs.est.9b07235] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/10/2023]
Abstract
The importance of arsenic metabolism by gut microbiota has been evidenced in risk characterization from As exposures. In this study, we evaluated the metabolic potency of human gut microbiota toward As(V)-sorbed goethite and jarosite, presenting different behaviors of As release, and the solid-liquid transformation and partitioning. The release of As occurred mainly in the small intestinal phase for jarosite and in the colon phase for goethite, respectively. We found higher degree of As(V) and Fe(III) reduction by human gut microbiota in the colon digests of goethite than jarosite. Speciation analysis using high-performance liquid chromatography coupled with inductively coupled plasma mass spectrometry and X-ray absorption near-edge spectroscopy, revealed that 43.2% and 8.5% of total As was present as As(III) in the liquid and solid phase, respectively, after goethite incubation, whereas almost all generated As(III) was in the colon digests of jarosite. Therefore, As bioaccessibility in human gastrointestinal tract was predominantly contributed to Fe(III) dissolution in jarosite, and to microbial reduction of Fe(III) and As(V) in goethite. It expanded our knowledge on the role of Fe minerals in human health risk assessment associated with soil As exposures.
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Affiliation(s)
- Naiyi Yin
- College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People's Republic of China
- Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People's Republic of China
| | - Xiaolin Cai
- College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People's Republic of China
- Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People's Republic of China
| | - Lirong Zheng
- Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, People's Republic of China
| | - Huili Du
- College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People's Republic of China
- Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People's Republic of China
| | - Pengfei Wang
- College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People's Republic of China
- Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People's Republic of China
| | - Guoxin Sun
- Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People's Republic of China
| | - Yanshan Cui
- College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People's Republic of China
- Research Center for Eco-Environment Sciences, Chinese Academy of Sciences, Beijing 100085, People's Republic of China
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48
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Rodrigues VCDC, Duque ALRF, Fino LDC, Simabuco FM, Sartoratto A, Cabral L, Noronha MF, Sivieri K, Antunes AEC. Modulation of the intestinal microbiota and the metabolites produced by the administration of ice cream and a dietary supplement containing the same probiotics. Br J Nutr 2020; 124:1-12. [PMID: 32138793 DOI: 10.1017/s0007114520000896] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023]
Abstract
The aim of the present work was to compare the capacity to modulate the intestinal microbiota and the production of metabolites after 14 d administration of a commercial dietary supplement and a manufactured ice cream, both containing the same quantity of inulin and the same viable counts of Lactobacillus acidophilus LA-5 and Bifidobacterium animalis BB-12, using the Simulator of the Human Intestinal Microbial Ecosystem (SHIME®) model. Samples of the colonic contents were evaluated microbiologically by real-time quantitative PCR (qRT-PCR) and next-generation sequencing and chemically by the production of SCFA (acetate, propionate and butyrate) and ammonium ions ($\text{NH}_4^ + $). Statistical analyses were carried out for all the variables using the two-way ANOVA followed by the Tukey multiple comparisons test (P < 0·05) for metabolite production, qRT-PCR and the bioinformatics analysis for microbiota diversity. Dietary supplement and ice cream were able to deliver the probiotic L. acidophilus and B. animalis to the simulated colon and modulate the microbiota, increasing beneficial micro-organisms such as Bifidobacterium spp., Bacteroides spp. and Faecalibacterium spp. for dietary supplement administration, and Lactobacillus spp. for ice cream supplementation. However, the ice cream matrix was probably more favourable for the maintenance of the metabolic activity of the probiotics in the SHIME® model, due to the larger amounts of acetate, propionate, butyrate and ammonium ions obtained after 14 d of supplementation. In conclusion, both ways of probiotic supplementation could be efficient, each with its own particularities.
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Affiliation(s)
| | - Ana Luiza Rocha Faria Duque
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP14800-903, Brazil
| | | | | | - Adilson Sartoratto
- Division of Organic and Pharmaceutical Chemistry, Pluridisciplinary Center for Chemical, Biological and Agricultural Research (CPQBA), State University of Campinas, Paulínia, SP13148-218, Brazil
| | - Lucélia Cabral
- Brazilian Biorenewables National Laboratory (LNBR), Brazilian Center for Research in Energy and Materials (CNPEM), Campinas, SP13083-970, Brazil
| | - Melline Fontes Noronha
- Genome Research Division, Research Informatics Core, Research Resource Center, University of Illinois at Chicago, Chicago, IL60612, USA
| | - Katia Sivieri
- Department of Food and Nutrition, School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, SP14800-903, Brazil
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49
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Blanco-Morales V, Garcia-Llatas G, Yebra MJ, Sentandreu V, Lagarda MJ, Alegría A. Impact of a Plant Sterol- and Galactooligosaccharide-Enriched Beverage on Colonic Metabolism and Gut Microbiota Composition Using an In Vitro Dynamic Model. JOURNAL OF AGRICULTURAL AND FOOD CHEMISTRY 2020; 68:1884-1895. [PMID: 31523960 DOI: 10.1021/acs.jafc.9b04796] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 06/10/2023]
Abstract
A beverage enriched with plant sterols (1 g/100 mL) and galactooligosaccharides (1.8 g/100 mL) was subjected to a dynamic gastrointestinal and colonic fermentation process to evaluate the effect on sterol metabolism, organic acid production, and microbiota composition. Production of sterol metabolites (coprostanol, methylcoprostanol, ethylcoprostenol, ethylcoprostanol, and sitostenone) was observed in the transverse colon (TC) and descending colon (DC) vessels in general, from 24 and 48 h, respectively. Microbial activity was assessed through the production of organic acids, mainly acetate in all colon vessels, lactate in the AC, and butyrate and propionate in the TC and DC. A higher diversity in the microbial community was found in the TC and DC, in accordance with a higher sterol metabolism and organic acid production. Although the prebiotic effect of galactooligosaccharides was not detected, changes in microbiota composition (an increase in the Parabacteroides genus and the Synergistaceae and Lachnospiraceae families) indicated an enhancement of sterol metabolism.
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Affiliation(s)
- Virginia Blanco-Morales
- Nutrition and Food Science Area, Faculty of Pharmacy , University of Valencia , Avenida Vicente Andrés Estellés s/n , 46100 Burjassot , Valencia , Spain
| | - Guadalupe Garcia-Llatas
- Nutrition and Food Science Area, Faculty of Pharmacy , University of Valencia , Avenida Vicente Andrés Estellés s/n , 46100 Burjassot , Valencia , Spain
| | - María J Yebra
- Laboratory of Lactic Acid Bacteria and Probiotics, Institute of Agrochemistry and Food Technology (IATA) . Spanish National Research Council (CSIC) , Avenida Agustín Escardino 7 , 46980 Paterna , Valencia , Spain
| | - Vicente Sentandreu
- Genomics Section, Central Service for Experimental Research (SCSIE) , University of Valencia , Carrer del Doctor Moliner 50 , 46100 Burjassot , Valencia , Spain
| | - María Jesús Lagarda
- Nutrition and Food Science Area, Faculty of Pharmacy , University of Valencia , Avenida Vicente Andrés Estellés s/n , 46100 Burjassot , Valencia , Spain
| | - Amparo Alegría
- Nutrition and Food Science Area, Faculty of Pharmacy , University of Valencia , Avenida Vicente Andrés Estellés s/n , 46100 Burjassot , Valencia , Spain
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Yao M, Xie J, Du H, McClements DJ, Xiao H, Li L. Progress in microencapsulation of probiotics: A review. Compr Rev Food Sci Food Saf 2020; 19:857-874. [DOI: 10.1111/1541-4337.12532] [Citation(s) in RCA: 124] [Impact Index Per Article: 24.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/23/2019] [Revised: 11/18/2019] [Accepted: 11/22/2019] [Indexed: 12/14/2022]
Affiliation(s)
- Mingfei Yao
- State Key Laboratory for Diagnosis and Treatment of Infectious DiseasesCollaborative Innovation Center for Diagnosis and Treatment of Infectious DiseasesNatl. Clinical Research Center for Infectious DiseasesThe First Affiliated HospitalCollege of MedicineZhejiang Univ. Hangzhou 310003 China
| | - Jiaojiao Xie
- State Key Laboratory for Diagnosis and Treatment of Infectious DiseasesCollaborative Innovation Center for Diagnosis and Treatment of Infectious DiseasesNatl. Clinical Research Center for Infectious DiseasesThe First Affiliated HospitalCollege of MedicineZhejiang Univ. Hangzhou 310003 China
| | - Hengjun Du
- Dept. of Food ScienceUniv. of Massachusetts Amherst MA 01003 U.S.A
| | | | - Hang Xiao
- Dept. of Food ScienceUniv. of Massachusetts Amherst MA 01003 U.S.A
| | - Lanjuan Li
- State Key Laboratory for Diagnosis and Treatment of Infectious DiseasesCollaborative Innovation Center for Diagnosis and Treatment of Infectious DiseasesNatl. Clinical Research Center for Infectious DiseasesThe First Affiliated HospitalCollege of MedicineZhejiang Univ. Hangzhou 310003 China
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