Effects of Synbiotic Supplement on Human Gut Microbiota, Body Composition and Weight Loss in Obesity

Nutrients - Tập 12 Số 1 - Trang 222
И. Н. Сергеев1, Thamer Aljutaily1, Gemma Walton2, Eduardo Huarte1
1Department of Health and Nutritional Sciences, South Dakota State University, Brookings, SD 57007, USA
2Department of Food and Nutritional Sciences, University of Reading, Reading RG6 6AP, UK

Tóm tắt

Targeting gut microbiota with synbiotics (probiotic supplements containing prebiotic components) is emerging as a promising intervention in the comprehensive nutritional approach to reducing obesity. Weight loss resulting from low-carbohydrate high-protein diets can be significant but has also been linked to potentially negative health effects due to increased bacterial fermentation of undigested protein within the colon and subsequent changes in gut microbiota composition. Correcting obesity-induced disruption of gut microbiota with synbiotics can be more effective than supplementation with probiotics alone because prebiotic components of synbiotics support the growth and survival of positive bacteria therein. The purpose of this placebo-controlled intervention clinical trial was to evaluate the effects of a synbiotic supplement on the composition, richness and diversity of gut microbiota and associations of microbial species with body composition parameters and biomarkers of obesity in human subjects participating in a weight loss program. The probiotic component of the synbiotic used in the study contained Lactobacillus acidophilus, Bifidobacterium lactis, Bifidobacterium longum, and Bifidobacterium bifidum and the prebiotic component was a galactooligosaccharide mixture. The results showed no statistically significant differences in body composition (body mass, BMI, body fat mass, body fat percentage, body lean mass, and bone mineral content) between the placebo and synbiotic groups at the end of the clinical trial (3-month intervention, 20 human subjects participating in weight loss intervention based on a low-carbohydrate, high-protein, reduced energy diet). Synbiotic supplementation increased the abundance of gut bacteria associated with positive health effects, especially Bifidobacterium and Lactobacillus, and it also appeared to increase the gut microbiota richness. A decreasing trend in the gut microbiota diversity in the placebo and synbiotic groups was observed at the end of trial, which may imply the effect of the high-protein low-carbohydrate diet used in the weight loss program. Regression analysis performed to correlate abundance of species following supplementation with body composition parameters and biomarkers of obesity found an association between a decrease over time in blood glucose and an increase in Lactobacillus abundance, particularly in the synbiotic group. However, the decrease over time in body mass, BMI, waist circumstance, and body fat mass was associated with a decrease in Bifidobacterium abundance. The results obtained support the conclusion that synbiotic supplement used in this clinical trial modulates human gut microbiota by increasing abundance of potentially beneficial microbial species.

Từ khóa


Tài liệu tham khảo

Sergeev, 2016, Vitamin D—Cellular Ca2+ link to obesity and diabetes, J. Steroid Biochem. Mol. Biol., 164, 326, 10.1016/j.jsbmb.2015.11.008

Bouter, 2017, Role of the gut microbiome in the pathogenesis of obesity and obesity-related metabolic dysfunction, Gastroenterology, 152, 1671, 10.1053/j.gastro.2016.12.048

Dao, 2018, Gut microbiota and obesity: Concepts relevant to clinical care, Eur. J. Int. Med., 48, 18, 10.1016/j.ejim.2017.10.005

Isolauri, 2017, Microbiota and Obesity, Nestle Nutr. Inst. Workshop Ser., 88, 95, 10.1159/000455217

Rowland, 2018, Gut microbiota functions: Metabolism of nutrients and other food components, Eur. J. Nutr., 57, 1, 10.1007/s00394-017-1445-8

Boulange, 2016, Impact of the gut microbiota on inflammation, obesity, and metabolic disease, Genome Med., 8, 42, 10.1186/s13073-016-0303-2

Brahe, 2016, Can We Prevent Obesity-Related Metabolic Diseases by Dietary Modulation of the Gut Microbiota?, Adv. Nutr., 7, 90, 10.3945/an.115.010587

Heiss, 2018, Gut Microbiota-Dependent Modulation of Energy Metabolism, J. Innate Immun., 10, 163, 10.1159/000481519

Russell, 2011, High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health, Am. J. Clin. Nutr., 93, 1062, 10.3945/ajcn.110.002188

Brinkworth, 2009, Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations, Br. J. Nutr., 101, 1493, 10.1017/S0007114508094658

Duncan, 2007, Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces, Appl. Environ. Microbiol., 73, 1073, 10.1128/AEM.02340-06

Blachier, 2018, High-protein diets for weight management: Interactions with the intestinal microbiota and consequences for gut health. A position paper by the my new gut study group, Clin. Nutr., 38, 1012, 10.1016/j.clnu.2018.09.016

Singh, 2017, Influence of diet on the gut microbiome and implications for human health, J. Transl. Med., 15, 73, 10.1186/s12967-017-1175-y

Fuller, 2014, The influence of Mediterranean, carbohydrate and high protein diets on gut microbiota composition in the treatment of obesity and associated inflammatory state, Asia Pac. J. Clin. Nutr., 23, 360

Yao, 2016, Review article: Insights into colonic protein fermentation, its modulation and potential health implications, Aliment. Pharmacol. Ther., 43, 181, 10.1111/apt.13456

Kullamethee, 2019, Modelling the role of microbial p-cresol in colorectal genotoxicity, Gut Microbes, 10, 398, 10.1080/19490976.2018.1534514

Monda, 2017, Exercise Modifies the Gut Microbiota with Positive Health Effects, Oxid. Med. Cell. Longev., 2017, 3831972, 10.1155/2017/3831972

Han, 2017, Dietary Fiber Gap and Host Gut Microbiota, Protein Pept. Lett., 24, 388, 10.2174/0929866524666170220113312

Anhe, 2015, Gut Microbiota Dysbiosis in Obesity-Linked Metabolic Diseases and Prebiotic Potential of Polyphenol-Rich Extracts, Curr. Obes. Rep., 4, 389, 10.1007/s13679-015-0172-9

Martinez, 2017, Western diets, gut dysbiosis, and metabolic diseases: Are they linked?, Gut Microbes, 8, 130, 10.1080/19490976.2016.1270811

Million, 2012, Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals, Microb. Pathog., 53, 100, 10.1016/j.micpath.2012.05.007

Dardmeh, 2016, Potential Nociceptive Regulatory Effect of Probiotic Lactobacillus rhamnosus PB01 (DSM 14870) on Mechanical Sensitivity in Diet-Induced Obesity Model, Pain Res. Manag., 2016, 5080438, 10.1155/2016/5080438

Esmaeilinezhad, 2019, Effect of synbiotic pomegranate juice on glycemic, sex hormone profile and anthropometric indices in PCOS: A randomized, triple blind, controlled trial, Nutr. Metab. Cardiovasc. Dis., 29, 201, 10.1016/j.numecd.2018.07.002

Suzumura, 2019, Effects of oral supplementation with probiotics or synbiotics in overweight and obese adults: A systematic review and meta-analyses of randomized trials, Nutr. Rev., 77, 430, 10.1093/nutrit/nuz001

Vulevic, 2013, A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults, J. Nutr., 143, 324, 10.3945/jn.112.166132

McCormack, 2016, Associations between sedentary time, physical activity, and dual-energy X-ray absorptiometry measures of total body, android, and gynoid fat mass in children, J. Clin. Densitom., 19, 368, 10.1016/j.jocd.2016.03.008

Al-Ghalith, G.A., Montassier, E., Ward, H.N., and Knights, D. (2016). NINJA-OPS: Fast Accurate Marker Gene Alignment Using Concatenated Ribosomes. PLoS Comput. Biol., 12.

Quast, 2013, The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools, Nucleic Acids Res., 41, D590, 10.1093/nar/gks1219

Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nat Methods, 7, 335, 10.1038/nmeth.f.303

Lozupone, 2011, UniFrac: An effective distance metric for microbial community comparison, ISME J., 5, 169, 10.1038/ismej.2010.133

Chiu, 2014, Systematic Analysis of the Association between Gut Flora and Obesity through High-Throughput Sequencing and Bioinformatics Approaches, BioMed Res. Int., 2014, 906168, 10.1155/2014/906168

Mueller, 2016, Metformin Is Associated With Higher Relative Abundance of Mucin-Degrading Akkermansia muciniphila and Several Short-Chain Fatty Acid–Producing Microbiota in the Gut, Diabetes Care, 40, 54

Wang, 2016, Structural modulation of the gut microbiota and the relationship with body weight: Compared evaluation of liraglutide and saxagliptin treatment, Sci. Rep., 6, 33251, 10.1038/srep33251

Zarrati, 2014, Effects of probiotic yogurt on fat distribution and gene expression of proinflammatory factors in peripheral blood mononuclear cells in overweight and obese people with or without weight-loss diet, J. Am. Coll. Nutr., 33, 417, 10.1080/07315724.2013.874937

Canfora, 2017, Supplementation of Diet With Galacto-oligosaccharides Increases Bifidobacteria, but Not Insulin Sensitivity, in Obese Prediabetic Individuals, Gastroenterology, 153, 87, 10.1053/j.gastro.2017.03.051

Azcarate-Peril, M.A., Butz, N., Cadenas, M.B., Koci, M., Ballou, A., Mendoza, M., Ali, R., and Hassan, H. (2018). An Attenuated Salmonella enterica Serovar Typhimurium Strain and Galacto-Oligosaccharides Accelerate Clearance of Salmonella Infections in Poultry through Modifications to the Gut Microbiome. Appl. Environ. Microbiol., 84.

Ferrarese, 2018, Probiotics, prebiotics and synbiotics for weight loss and metabolic syndrome in the microbiome era, Eur. Rev. Med. Pharmacol. Sci., 22, 7588

Seganfredo, 2017, Weight-loss interventions and gut microbiota changes in overweight and obese patients: A systematic review, Obes. Rev., 18, 832, 10.1111/obr.12541

Aoki, 2017, A proliferative probiotic Bifidobacterium strain in the gut ameliorates progression of metabolic disorders via microbiota modulation and acetate elevation, Sci. Rep., 7, 43522, 10.1038/srep43522

Jiao, 2019, Blueberry polyphenols extract as a potential prebiotic with anti-obesity effects on C57BL/6 J mice by modulating the gut microbiota, J. Nutr. Biochem., 64, 88, 10.1016/j.jnutbio.2018.07.008

Hu, H.J., Park, S.G., Jang, H.B., Choi, M.K., Park, K.H., Kang, J.H., Park, S.I., Lee, H.J., and Cho, S.H. (2015). Obesity Alters the Microbial Community Profile in Korean Adolescents. PLoS ONE, 10.

Brookheart, R.T., Lewis, W.G., Peipert, J.F., Lewis, A.L., and Allsworth, J.E. (2019). Association between obesity and bacterial vaginosis as assessed by Nugent score. Am. J. Obstet. Gynecol., 220.

Stanislawski, 2019, Gut microbiota phenotypes of obesity, NPJ Biofilms Microbiomes, 5, 18, 10.1038/s41522-019-0091-8

Ott, 2017, Effect of caloric restriction on gut permeability, inflammation markers, and fecal microbiota in obese women, Sci. Rep., 7, 11955, 10.1038/s41598-017-12109-9

Diether, N.E., and Willing, B.P. (2019). Microbial Fermentation of Dietary Protein: An Important Factor in Diet—Microbe—Host Interaction. Microorganisms, 7.

Louis, 2014, The gut microbiota, bacterial metabolites and colorectal cancer, Nat. Rev. Microbiol., 12, 661, 10.1038/nrmicro3344

Dahiya, 2017, Gut Microbiota Modulation and Its Relationship with Obesity Using Prebiotic Fibers and Probiotics: A Review, Front. Microbiol., 8, 563, 10.3389/fmicb.2017.00563

Million, 2012, Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii, Int. J. Obes., 36, 817, 10.1038/ijo.2011.153

Gentile, 2018, The gut microbiota at the intersection of diet and human health, Science, 362, 776, 10.1126/science.aau5812

Cani, 2019, Targeting gut microbiota with a complex mix of dietary fibers improves metabolic diseases, Kidney Int., 95, 14, 10.1016/j.kint.2018.11.012

Shetty, S.A., Marathe, N.P., Lanjekar, V., Ranade, D., and Shouche, Y.S. (2013). Comparative genome analysis of Megasphaera sp. reveals niche specialization and its potential role in the human gut. PLoS ONE, 8.

Korpela, K., Flint, H.J., Johnstone, A.M., Lappi, J., Poutanen, K., Dewulf, E., Delzenne, N., de Vos, W.M., and Salonen, A. (2014). Gut microbiota signatures predict host and microbiota responses to dietary interventions in obese individuals. PLoS ONE, 9.

Mirande, 2010, Dietary fibre degradation and fermentation by two xylanolytic bacteria Bacteroides xylanisolvens XB1A and Roseburia intestinalis XB6B4 from the human intestine, J. Appl. Microbiol., 109, 451, 10.1111/j.1365-2672.2010.04671.x

Aljutaily, 2018, Gut microbiota metabolites for sweetening type I diabetes, Cell. Mol. Immunol., 15, 92, 10.1038/cmi.2017.65

Rafter, 2007, Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients, Am. J. Clin. Nutr., 85, 488, 10.1093/ajcn/85.2.488