Probiotics for the Treatment of Overweight and Obesity in Humans—A Review of Clinical Trials
Abstract
:1. Introduction
2. Methods
2.1. Data Sources and Searches
2.2. Eligibility Criteria
2.3. Quality Assessment
3. Results
3.1. Search Results
3.2. Risk of Bias Assessment
4. Obesity
4.1. The Role of Gut Microbiota in Obesity
4.2. The Impact on Energy Homeostasis
4.3. The Impact on Inflammatory Processes
4.4. The Role of Probiotics in the Treatment and Prevention of Obesity
5. Review of Clinical Studies Using Probiotics in Obesity
5.1. The Effect of Probiotic Supplementation in Pregnant Women on Body Weight
5.2. The Effect of Probiotic Supplementation in Infants in the Prevention of Overweight or Obesity
5.3. The Effect of Probiotic Supplementation in Children on Body Weight
5.4. The Effect of Probiotic Supplementation in Adults on Body Weight
5.5. The Effect of Heat Killed Probiotics on Body Weight
5.6. The Effect of Probiotic Supplementation on Weight Gain
6. Meta-Analyses
7. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Short-Chain Fatty Acid (SCFA) | Receptors | Properties |
---|---|---|
Acetic acid | GPR 41, GPR43 | Stimulates the secretion of intestinal hormones PYY and GLP-1—appetite reduction Increased production of leptin Precursors for cholesterol and fat acids synthesis |
Propionic acid | GPR 41, GPR43 | Stimulates the secretion of intestinal hormones PYY and GLP-1—appetite reduction Inhibition of fat accumulation in adipocytes Increased production of leptin Substrate of gluconeogenesis |
Butyric acid | GPR 41, GPR43, GPR109A | Differentiation of Treg-cell Decrease the production of IL-12 Increase the production of IL-10 Stimulation of fat storage in adipose tissue Promotes intestinal epithelial integrity Increase in the oxidation of fatty acids Stimulating production of mucin |
Author | Study Design | Duration of Intervention | Intervention | Sample (Age) | Control/Placebo Groups | Clinical Outcome (vs. Control/Placebo Group) | Reference |
---|---|---|---|---|---|---|---|
Ilmonen et al. | Randomized placebo-controlled trial | From the first trimester, pregnancy up to 6 months after delivery | L. rhamnosus GG, B. lactis ( CFU) 1 capsule per day | 256 pregnant women; 85 diet/probiotics; 86 diet/placebo; 85 control/placebo (25–35 years) | 1 capsule containing microcrystalline cellulose and dextrose per day/without diet | ↓WC (p < 0.001) | [75] |
Luoto et al. | Randomized, double-blind, placebo-controlled trial | From the first trimester to the end of breastfeeding | L. rhamnosus GG, B. lactis ( CFU) 1 capsule per day | 256 pregnant women; 85 diet/probiotics; 86; diet/placebo; 85 control/placebo | 1 capsule containing microcrystalline cellulose and dextrose per day/without diet | Reduction in gestational diabetes (GDM) (13% diet/probiotics; 36% diet/placebo; 34% control/placebo) (p < 0.003) | [76] |
Lindsay et al. | Randomized, double-blind, placebo-controlled trial | 4 weeks | L. salivarius UCC118 ( CFU) 1 capsule per day | 138 women in the first trimester of pregnancy; 63 probiotic group; 75 placebo group (>18 years) | 1 capsule per day | No effect | [77] |
Asemi et al. | Randomized single-blinded controlled trial | 9 weeks | 200 g of yogurt containing L. acidophilus LA5 and B. animalis BB12 ( CFU/g) per day | 67 women in the third trimester of pregnancy; 33 probiotic group; 37 placebo group (18–30 years) | 200 g of conventional yoghurt per day | No effect | [78] |
Callaway et al. | Prospective double-blind RCT | From 20 weeks gestation to delivery | L. rhamnosus, B. animalis subspecies lactis ( CFU) per day | 211 obese and overweight women; 207 probiotic; 204 placebo (>18 years) | 1 capsule containing microcrystalline cellulose and dextrose per day | No effect | [79] |
Karlsson Videhult et al. | Randomized, double-blind, placebo-controlled trial | From 4 to 13 months of age | Cereals containing of L. paracasei ssp. paracasei—LF19 ( CFU) per day | 120 children; 58 probiotic group; 62 placebo group (8–9 years) | Cereals without LF19 | Effect on anthropometric parameters (p < 0.05) | [80] |
Karlsson Videhult et al. | Randomized, double-blind, placebo-controlled trial | From 4 to 13 months of age | Cereals containing of L. paracasei ssp. paracasei—LF19 ( CFU) per day | 120 children; 58 intervention group; 62 placebo group (8–9 years) | Cereals without LF19 | No effect | [81] |
Luoto et al. | Randomized, double-blind, prospective follow-up | Mothers 4 weeks before delivery; infants for 6 months after birth | L. rhamnosus GG ( CFU) 1 capsule per day | 113 Mother-child; 54 probiotic group; 59 placebo group | 1 capsule containing microcrystalline cellulose per day | Probiotic administration may reduce weight gain, especially up to 4 years of age (p = 0.08) | [82] |
Ipar et al. | Open-label, randomized, controlled trial | 4 weeks | L. acidophilus, L. rhamnosus, B. bifidum, B. longum (each 4.3 × CFU), E. faecium (8.2 × CFU), FOS 625mg, lactulose 400 mg, vit. A 6 mg, B1 1.8 mg, B2 1.6 mg, B6 2.4 mg, E 30 mg, C 75 mg 1 sachet per day | 117 children with primary obesity; 77 intervention group + calorie reduction + physical activity; 40 calorie reduction + physical activity (5–17 years) | Calorie reduction + physical activity | ↓BMI (p < 0.05); ↓ HC and WC (p < 0.05) | [83] |
Nagata et al. | Open-label prospective | 6 months | 1 bottle of fermented milk contained L. casei Shirota (4 × ) per day | 12 obese children; 22 healthy non-obese children | Diet + physical activity | ↓ weight (p < 0.05) | [84] |
Sanchis-Chorda et al. | Open-label prospective | 13 weeks | B. pseudocatenulatum CECT 7765 ( CFU) 1 capsule per day | 48 obese children with insulin resistance; 24 probiotic + diet; 24 diet (10–15 years) | 1 capsule per day | Improved lipid profile (p = 0.035), inflammatory markers (p = 0.026) and ↓ BMI (p = 0.001) | [85] |
Safavi et al. | Randomized triple-blinded controlled trial | 8 weeks | L. casei, L. rhamnosus, S. thermophilus, B. breve, L. acidophilus, B. longum and L. bulgaricus (Each 2 × CFU), vit. E, A, C per day | 56 obese children and adolescents; 29 intervention group; 27 placebo (6–18 years) | 1 capsule containing maltodextrin per day | ↓ BMI (p = 0.002), ↓ WC (p = 0.001) | [86] |
Kelishadi et al. | Triple-blinded controlled RTC | 8 weeks | L. casei, L. rhamnosus, S. thermophilus, B. breve, L. acidophilus, B. longum and L. bulgaricus (Each 2 × CFU), vit. E, A, C per day | 56 obese children and adolescents; 29 probiotic; 27 placebo (6–18 years) | 1 capsule containing maltodextrin per day | ↓ BMI (p = 0.002) | [87] |
Vajro et al. | Double-blind placebo-controlled pilot study | 8 weeks | L. rhamnosus GG (12 billion CFU/day) | 20 obese children with persisting hypertransaminasemia and ultrasonographic bright liver; 10 probiotic; 10 placebo (10–13 years) | Placebo | No effect | [88] |
Famouri et al. | Randomized triple-blind placebo-controlled trial | 12 weeks | L. acidophilus ATCC B3208 (3 × CFU), B. lactis DSMZ 32269 (6 × CFU), B. bifidum ATCC SD6576, L. rhamnosus DSMZ 21690 (each 2 × CFU) 1 capsule per day | 64 obese children and adults with NAFLD; 32 probiotics group; 32 placebo group (10–18 years) | 1 capsule per day | Improvement of lipid profile (p < 0.001) and NAFLD (p < 0.05); ↓ plasma liver enzymes (p = 0.02); No effect on BMI and body weight | [89] |
Alisi et al. | Parallel double-blind RCT | 4 months | Age < 10 year 1 sachet per day of VSL#3, age > 10 year 2 sachets of VSL#3 | 44 children with NAFLD; 22 probiotic group; 22 placebo group (9–12 years) | Age < 10 year 1 sachet per day, age > 10 year 2 sachets of VSL#3 | ↓ BMI (p = 0.001); ↑ GLP-1 (p = 0.001) | [90] |
Gobel et al. | Randomized double-blind placebo-controlled trial | 12 weeks | L. salivarius LS 33 ( CFU) 1 capsule per day | 50 obese adolescents; 27 probiotic; 23 placebo (12–15 years) | 1 capsule containing cellulose, silicon dioxide and rice-maltodextrin per day | No effect | [91] |
Kadooka et al. | Multi-centre, double-blind, parallel group RCT | 12 weeks | 200 g of fermented milk containing L. gasseri SBT2055 ( CFU/g) per day) | 87 obese adults; 43 probiotic group, 44 placebo group (33–63 years) | 200 g of fermented milk without probiotic per day | ↓ Weight, BMI, HC and WC (p = 0.01) | [92] |
Kadooka et al. | Multi-centre, double-blind, parallel group RCT | 12 weeks | 200 g of fermented milk containing L. gasseri SBT2055 ( or CFU/g) per day | 210 obese adults; 69 high dose probiotic, 71 low dose probiotic, 70 placebo (35–60 years) | 200 g of fermented milk without probiotic per day | ↓BMI, HC, WC and body fat mass (p = 0.01) | [93] |
Jung et al. | Randomized, double-blind, placebo-controlled trial | 12 weeks | L. gasseri BNR17 ( CFU) 6 capsules per day | 57 overweight or obese adults; 28 probiotic group; 29 placebo group (19–60 years) | 6 capsules containing trehalose, skim milk, and fructooligosaccharide per day | ↓ WC and HC (p = 0.015); ↓ body weight (p = 0.008) | [94] |
Kim et al. | Randomized, double-blind, placebo-controlled trial | 12 weeks | L. gasseri BNR17 ( CFU) 2 capsuls per day | 90 overweight or obese adults; 30 high dose probiotic; 30 low dose probiotic; 30 placebo (20–75 years) | 2 capsule containing maltodextrin, crystalline cellulose, and magnesium stearate per day | High and low probiotic doses reduce body weight and waist circumferences (p < 0.05); A high dose of probiotic reduces visceral adipose tissue (p < 0.05) | [95] |
Takahashi et al. | Multicenter, randomized, double-blind, placebo-controlled intervention trial | 12 weeks | 100g of fermented milk containing B. animalis ssp. lactis GCL2505 (8 × CFU) per day | 137 overweight and obese adults; 69 probiotic; 68 placebo (20–65 years) | 100 g of fermented milk without probiotic | ↓ visceral fat (p = 0.05) | [96] |
Omar et al. | Randomized double-blind placebo-controlled trial | 43 days | 100 g of yogurt containing L. amylovorus (1.39 × CFU) or 100 g of yogurt containing L. fermentum (1.08 × CFU) per day | 28 overweight and obese adults; 14 probiotic LA; 12 probiotic LF; 12 placebo (16–60 years) | 100 g of control yogurt per day | No effect | [97] |
Kim et al. | Randomized, double-blind, placebo-controlled trial | 12 weeks | 2 g of powder containing L. plantarum KY1032 and L. curvatus (2.5 × CFU) twice a day | 65 overweight adults; 32 probiotic; 34 placebo (25–75 years) | 2 g of powder without probiotic twice a day | ↓ body weight (p < 0.05) | [98] |
De Lorenzo et al. | Randomized, double-blinded controlled trial | 3 weeks | S. thermophilus SGSt01, B. animalis subsp. Lactis SGB06, S. thermophiles, B. bifidum SGB02, L. delbrueckii spp. Bulgaricus DSM 20081, L. lactis subsp. Lactis SGLc01, L. acidophilus SGL11, L. plantarum SGL07, L. reuteri SGL01 (1.5 × CFU) 1 sachet per day | 48 women with normal weight, overweight or obesity; 24 probiotics; 24 placebo (20–65 years) | 1 sachet containing maltodextrin from corn and silica per day | ↓ BMI, and fat mass (p < 0.05) | [99] |
Szulińska et al. | Randomized, double-blind, placebo-controlled trial | 12 weeks | 2 g of powder containing B. bifidum W23, B. lactis W51, B. lactis W52, L. acidophilus W37, L. brevis W63, L. casei W56, L. salivarius W24, L. lactis W19, and L. lactis W58 (High dose CFU or low dose 2.5 × CFU per day divided in two equal doses) | 71 obese women; 23 high dose probiotic; 24 low dose probiotic; 24 placebo (45–70 years) | 2 g of powder containing only the excipients, i.e., maize starch and maltodextrins | Improving lipid profile and glucose metabolism (p < 0.05); ↓ visceral fat, waist circumference (p < 0.05); High probiotic doses ↓ LPS levels (p < 0.05) | [100] |
Minami et al. | Randomized, double-blind, parallel-group comparative trial | 12 weeks | B. breve B-3 (5 × CFU, 3 capsules per day) | 44 overweight adults with diabetes; 19 probiotic group; 25 placebo group (40–69 years) | 3 capsules per day containing maize starch | Improving liver function (p < 0.05); Reduction of metabolic disorders (p < 0.05); Reduction of fat mass (p < 0.05) | [101] |
Minami et al. | Randomized, double-blind, placebo-controlled trial | 12 weeks | B. breve B-3 (2 × CFU) 2 capsuls per day | 80 healthy pre-obese adults; 40 probiotics; 40 placebo (20–64 years) | 2 capsules per day containing corn starch | ↓ body fat (p < 0.05); No effect on lipid profile | [102] |
Ivey et al. | Randomized double-blinded parallel study | 6 weeks | Both the probiotic yogurt and the probiotic capsule contained L. acidophilus La5, B. animalis subsp. lactis Bb12 (3 × CFU per day) | 156 overweight men and women; 40 probiotic yoghurt + probiotic capsules; 37 probiotic yoghurt + placebo capsules; 39 control milk + probiotic capsules; 40 control milk + placebo capsules (over 55 years) | Control milk | No effect | [103] |
Sanchez et al. | Randomized, double-blind, placebo-controlled trial | 12 weeks | L. rhamnosus CGMCC1.3724 (3.24 × CFU) + 90 g inulin and 210 g FOS, 2 capsules per day | 125 obese adults; 62 intervention group, 63 placebo group (18-55 years) | 2 capsules containing maltodextrin and magnesium stearate per day | ↓ weight (p = 0.02); ↓ appetite (p = 0.02) | [104] |
Mohammadi-Sartang et al. | Randomized double-blinded controlled trial | 10 weeks | 250 g of fortified yogurt (FSY) with whey protein, calcium, vit. D, fiber and probiotic (S. thermophiles, L. bulgaricus and at least B. lactis Bb-12) 250 g twice a day | 87 obese adults with metabolic syndrome; 44 fortified yogurt + diet; 43 low-fat conventional yogurt + diet (20–65 years) | 250 g of low fat plain yogurt with St. thermophiles and L. bulgaricus (LFY) twice a day | ↓ body fat mass (p < 0.05); ↓ WC (p < 0.05), ↓ TG ↓ HOMAR-IR value (p < 0.05); ↑HDL (p < 0.05) | [105] |
Zarrati et al. | Randomized double-blind placebo-controlled trial | 8 weeks | 200 g of yogurt containing L. acidophilus La5, B. BB12 and L. casei DN001 CFU/g | 75 obese adults; 25 regular yogurt + low calorie diet; 25 probiotic yogurt + low calorie diet; 25 probiotic yogurt without low calorie diet | 200 g of yogurt without probiotics | ↓ body mass and inflammation (p < 0.001) | [106] |
Gomes et al. | Randomized, double-blind, placebo-controlled trial | 8 weeks | L. acidophilus LA-14, L. casei LC-11, L. lactis LL-23, B. bifidum BB-06, B. lactis BL-4 (each CFU) 4 sachets per day + diet | 43 overweight or obese women; 21 probiotics; 22 placebo (20–59 years) | 4 sachets per day of placebo + diet | ↓ abdominal adiposity (p = 0.02) | [107] |
Stenman et al. | Randomized, double-blind, placebo-controlled, multi-center clinical trial | 6 months | B. animalis ssp. lactis 420 ( CFU) with or without 12g of LU per day | 134 overweight or obese adults; 25 probiotic; 36 LU (12 g); 37 probiotic + LU (12 g); 36 placebo (18–65 years) | 1 sachet (12 g) containing microcrystalline cellulose per day | ↓ fat mass and WC (p = 0.02) | [108] |
Karbaschian et al. | Randomized, double-blind, placebo-controlled trial | 4 weeks before surgery and 12 weeks after surgery | L. casei (3.5 × CFU/g), L. rhamnosus (7.5 × CFU/g), S. thermophilus ( CFU/g), B. breve ( CFU/g), L. acidophilus ( CFU/g), B. longum (3.5 × CFU/g), and L. bulgaricus ( CFU/g) and 38.5 mg FOS 1 capsule per day | 46 Obese women; 23 probiotics; 23 placebo (18–60 years) | 1 capsule containing maltodextrin per day | ↓ body weight (p < 0.05) | [109] |
Aller et al. | Randomized, double-blind, parallel-group comparative trial | 3 months | L. bulgaricus and St. thermophilus (500 million of probiotic, 1 tablet per day) | 28 adults with NAFLD; 14 probiotic group; 14 placebo group (39–60 years) | 1 tablet contained 120 mg of starch | Improving glucose metabolism (p < 0.05); Improvement of liver function (p < 0.05); No effect on body weight | [110] |
Miccheli et al. | Parallel-arm, double-blind RCT | 4 months | (112.5 × CFU) - VSL#3 (age < 10 year 1 sachet per day of VSL#3; age > 10 year 2 sachets of VSL#3) + diet + physical activity | 31 children with NAFLD; 15 probiotic group; 16 placebo (9–12 years) | 1 sachet placebo | ↓ BMI (p = 0.045) and liver function (p = 0.026) | [111] |
Javadi et al. | Randomized double-blind placebo-controlled trial | 3 months | B. longum, L. acidophilus (each 2 × CFU per day) | 75 obese adults: 20 probiotic; 19 prebiotic; 17 probiotic + prebiotic; 19 placebo (20–60 years) | Supplementation with probiotic and/or prebiotic improves liver function (p < 0.05); ↓ body mass and BMI (p < 0.05) | [112] | |
Razmpoosh | Randomized, double-blind, placebo-controlled trial | 6 weeks | L. acidophilus (2 × CFU), L. casei, B. longum (each 7 × CFU), L. rhamnosus (1.5 × CFU), L. bulgaricus (2 × CFU), B. breve (3 × CFU), S. thermophilus (1.5 × CFU), 100 mg FOS 2 capsules per day | 60 adults with diabetes; 30 probiotic group, 30 placebo group (30–75 years) | 2 capsules per day containing fructooligosaccharide and magnesium stearate | ↓ fasting glucose (p = 0.001); ↑ HDL (p = 0.002); No effect on anthropometric parameters and insulin levels | [113] |
Madjd et al. | Randomized, single-blind, controlled trial | 12 weeks | 200 g of probiotic yogurt (S. thermophiles, L. bulgaricus, L. acidophilus LA5, B. lactis BB12 - CFU) twice a day | 89 healthy overweight and obese women; 45 probiotic; 44 placebo (18–50 years) | 200 g low-fat yogurt twice a day | No effect | [114] |
Sharafedtinov et al. | Randomized, double-blind, placebo-controlled trial | 3 weeks | 50 g cheese with L. plantarum TENSIA per day | 40 obese adults with hypertension; 25 probiotic group; 15 placebo group (30–69 years) | 50 g cheese without probiotic per day | ↓ BMI and morning blood pressure (p = 0.001) | [115] |
Leber et al. | Open label, randomized pilot study | 3 months | 1 bottles (65 mL) containing L. casei Shirota (6.5 × CFU) three times a day | 28 adults with MetS; 13 probiotic; 15 placebo (24–66 years) | 1 bottles (65 mL) of placebo three times a day | No effect | [116] |
Mobini et al. | Randomized double-blind placebo-controlled trial | 12 weeks | Powder containing L. reuteri DSM 17938 low dose ( CFU) or high dose ( CFU) | 44 patients with type 2 diabetes; 15 low dose; 14 high dose; 15 placebo (50–75 years) | Powder without probiotic | No effect | [117] |
Mahadzir et al. | Randomized triple-blind placebo-controlled trial | 4 weeks | L. acidophilus BCMC 12130, L. casei subsp. BCMC 12313, L. lactis BCMC 12451, B. bifidum BCMC 02290, B. longum BCMC 02120 and B. infantis BCMC 02129 (3 × CFU per day) twice a day | 24 overweight adults; 12 probiotics; 12 placebo (18–50 years) | 2 sachets without probiotic | No effect | [118] |
Osterberg et al. | Randomized, double-blind, parallel-group comparative trial | 4 weeks | VLS#3 (4.5 × ) 2 sachets per day | 20 healthy non-obese; 9 probiotic; 11 placebo group (18–30 years) | 2 sachets per day | ↓ body mass (p = 0.023) | [119] |
Pedret et al. | Randomized, parallel, double-blind, placebo-controlled trial | 12 weeks | B. animalis subsp. lactis CECT 8145 ( CFU) 1 capsul per day; heat-killed B. animalis subsp. lactis CECT 8145 ( CFU) 1 capsule per day | 126 abdominally obese adults, 42 probiotic; 44 heat killed from probiotic; 40 placebo group (>18 years) | 1 capsule containing 300 mg of maltodextrose | ↓ BMI and WC (p < 0.05) | [120] |
Higashikawa et al. | Randomized double-blind placebo-controlled trial | 12 weeks | Powder containing living Pediococcus pentosaceus LP28 ( CFU) with dextrin per day; Powder containing heat-kill Pediococcus pentosaceus LP28 ( CFU) with dextrin per day | 62 overweight adults; 21 living LP28; 21 heat-killed LP28; 20 placebo group (20–70 years) | Powder containing dextrin | ↓ body mass (p = 0.004), BMI (p = 0.035), WC (p = 0.009) in group after Heat-killed LP28 | [121] |
Jones et al. | Randomized double-blind placebo-controlled trial | 16 weeks | VLS#3 3 sachets per day | 19 obese adolescents; 8 probiotic; 11 placebo group (12–18 years) | 3 sachets per day | ↑ total adiposity (p = 0.01) | [122] |
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Wiciński, M.; Gębalski, J.; Gołębiewski, J.; Malinowski, B. Probiotics for the Treatment of Overweight and Obesity in Humans—A Review of Clinical Trials. Microorganisms 2020, 8, 1148. https://doi.org/10.3390/microorganisms8081148
Wiciński M, Gębalski J, Gołębiewski J, Malinowski B. Probiotics for the Treatment of Overweight and Obesity in Humans—A Review of Clinical Trials. Microorganisms. 2020; 8(8):1148. https://doi.org/10.3390/microorganisms8081148
Chicago/Turabian StyleWiciński, Michał, Jakub Gębalski, Jakub Gołębiewski, and Bartosz Malinowski. 2020. "Probiotics for the Treatment of Overweight and Obesity in Humans—A Review of Clinical Trials" Microorganisms 8, no. 8: 1148. https://doi.org/10.3390/microorganisms8081148