J Obes Metab Syndr 2019; 28(4): 216-224
Published online December 30, 2019 https://doi.org/10.7570/jomes.2019.28.4.216
Copyright © Korean Society for the Study of Obesity.
1Department of Food Science and Nutrition, Pusan National University, Busan; 2Department of Food and Nutrition, Changwon National University, Changwon, Korea
Department of Food and Nutrition, Changwon National University, 20 Changwondaehak-ro, Uichang-gu, Changwon 51140, Korea
Tel: +82-55-213-3517 Fax: +82-55-281-7480 E-mail: email@example.com
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Obesity is abnormal or excessive fat accumulation that is associated with progression of metabolic diseases including type 2 diabetes mellitus, cardiovascular disease, nonalcoholic fatty liver disease, and cancer. Gut microbiota (GM) have received much attention as essential factors in development and progression of obesity. The diversity, composition, and metabolic activity of GM are closely associated with nutrient intake and dietary pattern. Scientific evidence supports the idea that dietary pattern directly changes the GM profile; therefore, diet is a crucial component related to interactions between GM and obesity progression. A literature review showed that dietary factors such as probiotics, prebiotics, fat, fatty acids, and fiber dramatically alter the GM profile related to obesity. Furthermore, different dietary patterns result in different GM composition and activity that can contribute to amelioration of obesity.
Keywords: Diet, Prebiotics, Probiotics, Gastrointestinal microbiome, Obesity
Overweight and obesity have nearly tripled in the population since 1975. According to the World Health Organization (WHO), over 1.9 billion adults were considered overweight in 2014, representing 39% of the world’s population. Over 340 million children and adolescents aged 5–19 years were also overweight or obese in 2016. Finkelstein et al.1 estimated an increase of 3.3 billion people with a body mass index (BMI) ≥25.0 kg/m2, corresponding to 57.8% of the adults worldwide by 2030. Obesity is described as an accumulation of excessive fat mass concomitant with low-grade chronic systemic inflammation.2 Obesity has commonly been associated with development of other metabolic disorders such as type 2 diabetes mellitus (T2DM), cardiovascular disease (CVD), and some types of cancer.3,4
The gastrointestinal tract contains at least 1014 bacteria, with the most abundant numbers in the large intestine.5 The number of genes in the intestinal microbiome is 150- to 500-fold greater than in human DNA.6 The collected gut microbiota (GM) are described as a “forgotten organ” that is sensitive to dietary, environmental, and host factors with function complicatedly intertwined with host metabolism.7 Both endogenous and exogeneous factors such as autoimmune disease, chronic disease, medications, antibiotics, smoking, stress level, and diet affect the diversity and composition of GM. Each individual has a unique GM composition and profile that may affect nutrient metabolism. Recent evidence has suggested that GM is a contributing factor in the progression of obesity.6,8,9 The GM is capable of modulating host metabolism through energy balance, chronic low-grade inflammation, and intestinal barrier function.6 Furthermore, the composition and diversity of GM are different between healthy weight and obese individuals.8 Therefore, the main objective of this review is to discuss whether GM altered by probiotics, prebiotics, and specific diet composition can contribute to amelioration of obesity (Fig. 1).
Obesity is a multifactorial, chronic disorder associated with other metabolic diseases. Recently, GM has received attention as a metabolic factor that affects the interactions between exogeneous factors and host metabolism. The GM is known to affect host metabolism by modulating energy balance, chronic-low grade inflammation, and gut barrier function.10 Modulation of these factors is highly associated with obesity; therefore, the GM is considered an environmental regulator of obesity. Several mechanisms of obesity and GM interactions have been suggested. The GM is comprised of a dynamic population of microorganisms including bacteria, archaea, fungi, and viruses. The dominant bacterial species in human GM are
Development of obesity also has been linked to abnormal energy intake and expenditure.21 Increasing evidence suggests that energy balance (energy intake and expenditure) is highly intertwined and modulated by GM.22 GM can regulate energy intake and appetite by production of short-chain fatty acids (SCFAs) of nondigestible polysaccharides.23 The SCFAs, such as acetate, butyrate, and propionate, produced by bacterial fermentation act as substrates of energy as well as modulators of satiety and food consumption when they combine with G-protein coupled receptor 41 (GPR41) and GPR43 in intestinal epithelial cells.24,25 The SCFAs also stimulate secretion of peptide YY (PYY) and glucagon-like peptide-1 (GLP-1), which can suppress intestinal mobility transit allowing higher uptake of nutrients.23,25
Many environmental factors such as diet, energy intake, and exercise can dramatically influence GM.26,27 Specific foods and diets can influence the abundance of different bacteria in the GM, which can affect host health. Probiotics can increase GM diversity and SCFA production and reduce T2DM and CVD. Several suggested mechanisms linking microbiota to weight changes include an increased capacity of some bacteria to extract energy, improved transfer of calories from food to host, and changes in host absorption metabolism.
Prebiotics have been defined by the Food and Agriculture Organization (FAO) of the United Nations and WHO as “non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one or a limited number of bacterial species already established in the colon, and thus improve the host health.”28 As mentioned above, dietary prebiotics have typically been classified as nondigestible fiber that passes undigested through the upper gastrointestinal tract and stimulates and colonizes the growth of beneficial microorganisms.29 Bindels et al.30 reported that prebiotic ingredients include inulin, fructooligosaccharides (FOS), galactooligosaccharides, and human milk oligosaccharides. The prebiotics usually found in fruits and vegetables may lead to various health benefits in the host.31 Among the advantages of prebiotics are promotion of ion and trace element absorption such as that of calcium, iron, and magnesium and immune system regulation by increasing Immunoglobulin A production and modulating cytokine production through mechanisms mediated by microbial metabolic products.29 Prebiotics selectively stimulate the growth of
According to FAO/WHO, probiotics are “live microorganisms which confer a health benefit on the host when administered in adequate amounts.”22 Recent studies have shown that
The effects of
Diet is one of the critical factors in progression of obesity and is profoundly linked to GM composition.51 Nutrient intake and eating habits directly influence the composition, diversity, and metabolism of GM.51,52 Furthermore, the composition and functionality of GM respond quickly to changes in dietary composition. Several studies showed that, within 2 days after the start the dietary intervention, the GM responded and exerted changes in composition.53 Interestingly, a healthy dietary pattern related to GM profiles exerted protective effects against development of diabetes in obese individuals.54 Therefore, a balanced diet is required to maintain the composition and proper function of the GM. Many dietary patterns such as Western diet, vegetarian diet, gluten-free diet, and the Mediterranean diet have been shown to affect the distinct diversity of the GM that may affect host metabolism.52
The Western diet consists of high intake of saturated fats, refined grains, sugar, salt, and high fructose corn syrup and a low intake of fiber. It is highly associated with obesity and metabolic disease. The Western diet promotes inflammation and changes the profile of the GM from healthy to the obese pattern.55 It also has been shown to decrease the total bacteria amount as well as the beneficial
Vegetarian and vegan diets consist of plant-based foods and are rich in dietary fiber, in contrast with the Western diet. Abundant fiber in these diets promotes stable GM profile and increases the presence of lactic acid bacteria.56 Both the vegetarian and vegan diet were shown to lower
The effects of a gluten-free diet on the GM is well known since gluten-related disease is closely associated with GM profile and metabolism.58 The gluten-free diet lowered the abundance of
The Mediterranean diet consists of vegetables, olive oil, and fruits, a moderate intake of poultry, and a low intake of red meat and dairy products. It is well known as one of the healthiest dietary patterns. GM composition in the Mediterranean diet is high in
The prevalence of obesity dramatically increased to 40% according to the data from the 2015 Korea National Health and Nutrition Examination Survey for Korean adults.65 Dietary pattern and lifestyle changed dramatically with the rapid industrialization in Korea over the last several decades. The consumption of Western food and less physical activity increased obesity and metabolic diseases. The traditional Korean dietary pattern is high in consumption of vegetables and fermented foods, with moderate intake of legumes and fish. Compared to the animal-based Western diet, this plantbased diet altered high levels of
The diversity, composition, and metabolic activity of the GM are closely associated with nutrient intake and dietary pattern. Specific dietary factors and dietary patterns alter the GM profiles that can regulate or affect progression of obesity. More studies and longterm trials are needed to understand the effects of dietary pattern on alteration of the GM associated with obesity.
The authors declare no conflict of interest.
Review concept and design: JEY, BK; drafting of the manuscript: BK, HNC; critical revision of the manuscript: JEY.
Clinical trials on the association between prebiotics and obesity
|Study||Study design||Prebiotics intervention||Beneficial effect|
|Edrisi et al. (2018)38||Overweight and obese adults (n=105); randomized control trial (Intervention I and Intervention II)||Energy-restricted diet containing rice bran (intervention I), rice husk powder (intervention II), or a low-calorie diet for 12 weeks||Reduction of body weight, BMI, waist circumference, reduction in inflammatory markers|
|Genta et al. (2009)39||Obese and slightly dyslipidemic premenopausal women (n=35); double-blind, placebo-controlled study||Placebo syrup (tartaric acid 2.5%, carboxymethylcellulose 1.8%, saccharine 2.5%, and glycerine 10%)+healthy hypocaloric diet or yacon syrup (approximately 12.5 g FOS/day)+ healthy hypocaloric diet for 17 weeks||Reduction of body weight, BMI, waist circumference, fasting serum insulin, and HOMA-IR; increased satiety|
|Hume et al. (2017)40||Overweight and obese children aged 7–12 years (n=42); randomized, double-blind, placebo-controlled trial||8 g/day oligofructose-enriched inulin or equicaloric dose of a 3.3 g maltodextrin placebo/day for 16 weeks||Increased satiety, prospective food consumption, and ghrelin; decreased energy intake|
|Nicolucci et al. (2017)41||Overweight and obese children aged 7–12 years (n=42); single-center, double-blind, placebo-controlled trial||8 g/day oligofructose-enriched inulin or equicaloric dose of a 3.3 g maltodextrin placebo/day for 16 weeks||Decreased body weight z-score, percent body fat, and trunk fat; increased |
|Parnell and Reimer (2009)42||Overweight and obese adults (n=39); intervention study||21 g/day oligofructose-enriched diet or equicaloric dose of maltodextrin placebo/day for 12 weeks||Decreased body weight, fat mass, energy intake, postprandial insulin, and ghrelin|
|Reimer et al. (2017)43||Overweight and obese adults (n=39); single-center, placebo-controlled, double-blind, randomized controlled trial||Prebiotic bar (inulin-type fructan with 6 g oligofructose+2 g inulin from chicory root) or control isocaloric bar (100 kcal/bar) for 12 weeks||Decreased hunger; increased |
BMI, body mass index; FOS, fructooligosaccharides; HOMA-IR, homeostasis model assessment of insulin resistance.
Clinical trials on the association between probiotics and obesity
|Study||Study design||Probiotics intervention||Beneficial effect|
|Gomes et al. (2017)44||Obese women aged 20–59 years (n=43); randomized, double-blind, placebo-controlled intervention, clinical trials||Reduction of waist circumference|
|Higashikawa et al. (2016)45||Overweight adults aged 20–70 years (n=62); randomized, double-blind, placebo-controlled clinical trial||1011 CFU/day of living or heat-killed ||Reduction of BMI after heat-killed LP28|
|Kadooka et al. (2010)46||Adults with overweight and obesity (BMI between 24.2 and 30.7 kg/m2, n=87); multicenter, double-blind, randomized, placebo-controlled intervention trial||200 g/day of fermented milk containing ||Reduction of body weight, BMI, and fat areas including abdominal visceral and subcutaneous fat|
|Kim et al. (2018)47||Obese adults aged 20–75 years (n=90); randomized, double-blind, placebo-controlled trial-controlled trial||Low (109 CFU/day) and high (1010 CFU/twice a day) dose of ||Decreased waist circumferences in low dose; decreased visceral adipose tissue in high dose|
|Pedret et al. (2019)48||Abdominally obese randomized, parallel, double-blind, placebo-controlled trial adults (n=126)||1010 CFU/cap/day of ||Reduction in BMI and the ratio of waist circumference/height|
|Sanchis-Chordà et al. (2019)49||Obese adults aged 18–55 years (n=125); randomized, double-blind, placebo-controlled trial||1.62×108 CFU/2 cap/day of ||Reduction in weight|
|Szulińska et al. (2018)50||Obese postmenopausal women aged 45–70 years (n=81); randomized-double-blind, placebo-controlled clinical trial||Probiotic mixture including different ||Reduction in body weight, BMI, and fat mass in both low dose and high dose groups; improvement of lipid profiles in the high dose group|
CFU, colony-forming unit; BMI, body mass index; subsp., subspecies.
The effect of diet on GM associated with obesity
|Diet||Effect on GM associated obesity|
|Western diet: high intake of saturated fat, refined grains, sugars, salt, and high fructose corn syrup and low intake of fiber15,55||Promotes inflammation and changes the GM profile to the obese pattern|
Decrease in total GM amount
Decrease in beneficial
|Vegetarian and vegan diets: plant-based foods and rich in dietary fiber56,57||Increase in the abundance of protective microbiota|
Increase in intestinal barrier protectors (
Decrease in inflammation-inducing lipopolysaccharide producers (
→ prevents obesity
|Gluten-free diet58,59||Decrease in |
|Mediterranean diet: consists of vegetables, olive oil, fruits, a moderate intake of poultry, and a low intake of red meat and dairy products63,64||Increase in |
→ prevents obesity and improves lipid and cholesterol profiles
|Korean traditional diet: high consumption of vegetables and fermented foods, moderate intake of legumes and fish65,66||Increase in |
→ prevents obesity
GM, gut microbiota; sp., species.