Table 2.
Reference | Year | Location | Design | Participants, Age, Nr. Treated/ Nr. Controls | Probiotic Source | Probiotic Dose, CFU | Study Period (wk/d) |
Glycemia | Insulin | Lipid Metabolism | Incretins |
---|---|---|---|---|---|---|---|---|---|---|---|
[135] | 2002 | Poland | RD, DB, CT | Healthy participants 35–45 y 18/18 |
rose-hip drink |
L. plantarum 299v, 5 × 107 CFU/mL |
6 wk | =FG | =I | =TC, LDL-C, HDL-C, TG, lipoprotein(a) | S↓ leptin |
[136] | 2006 | Australia | DB, PC, parallel design trial, single centre | Healthy volunteers 30–75 y 23/21 |
capsule |
L. fermentum, 2 × 109 CFU |
10 wk | =FG | - | =LDL-C, TC, HDL-C, TGL | - |
[137] | 2009 | Finland | RD, prospective, parallel-group | Pregnant women 29.7/30.1/30.2 y 85/86/85 |
capsule |
L. rhamnosus GG, ATCC 53 103, B. lactis Bb12, 1010 CFU/d each |
4 wk | S↓ FG, =HbA1c |
S↓ I, HOMA, S↑ QUICKI |
- | - |
[138] | 2010 | Denmark | RD, PC, DB | T2DM/non-diabetic 48–66 y 24/24 |
capsule |
L. acidophilus NCFM, 1 g; about 1010 CFU |
4 wk | - | =QUICKI | - | - |
[139] | 2012 | Iran | DB, RD, CT | T2DM 30–60 y 32/32 |
yogurt |
L. acidophilus La5, 7.23 × 106–1.85 × 106 CFU/g B. lactis Bb12, 6.04 × 106 CFU/g–1.79 × 106 CFU/g |
6 wk | S↓ FG, HbA1c | =I | - | - |
[140] | 2012 | Brazil | DB, PC, RD | Healthy participants 50–65 y 10/10 |
shake |
L. acidophillus, 4 × 108 CFU/100 mL B. bifidum 4 ×108 CFU/100 mL 1 g/100 mL FOS |
30 d | S↓ FG | - | S↑ HDL-C =TC, TG |
- |
[141] | 2012 | Canada | DB, PC, multi-center study | Healthy hypercholester-olemic human subjects 20–75 y 67/64 |
capsule |
L. reuteri NCIMB 30242, 2.9 × 10⁹ CFU |
9 wk | =FG | - | - | - |
[142] | 2012 | Denmark | DB, PC, RD | Ob adolescents 12–15 y 27/23 |
capsule |
L. salivarius Ls-33 ATCC SD5208, 1010 CFU |
12 wk | =FG | =I, HOMA-IR | =TC, HDL-C, LDL-C, TG | - |
[143] | 2013 | Iran | RD, DB, PC, CT | T2DM 35–70 y 27/27 |
capsule |
L. acidophilus, 2 × 109 CFU L. casei, 7 × 109 CFU L. rhamnosus, 1.5 × 109 CFU L. bulgaricus, 2 × 108 CFU B. breve, 2 × 1010 CFU B. longum, 7 × 109 CFU S. thermophiles, 1.5 ×109 CFU 100 mg FOS |
8 wk | S↓ FG | S↑ I, HOMA-IR | S↑ LDL-C | - |
[144] | 2013 | Iran | RD, DB, CT | Patients with NASH 18–75 y 34/36 |
tablet |
L. acidophilus, 1 × 108 CFU L. casei, 5 × 108 CFU L. rhamnosus, 7.5 × 107 CFU L. bulgaricus, 1.5 × 108 CFU B. breve, 5 × 107 CFU B. longum, 2.5 × 107 CFU S. thermophilus, 5 × 107 CFU 350 mg FOS |
24 wk | S↓ FG | - | S↓ TC, TG |
- |
[145] | 2013 | Korea | single center, RD, DB, PC, CT | Ob volunteers 19–60 y 31/31 |
capsule |
L. gasseri BNR17, 1010 CFU 25% FOS |
12 wk | =FG, HbA1c | =I | =TC, TG, LDL-C, HDL-C, | - |
[146] | 2013 | Russian Federation | RD, DB, PC, parallel pilot study | Patients with metabolic syndrome 30–69 y 25/15 |
cheese |
L. plantarum TENSIA, 1.5 × 1011 CFU/g |
3 wk | =FG | - | =TC, LDL-C, HDL-C, TG | - |
[147] | 2013 | Iran | RD, SB, CT | Pregnant women 37/33 18–30 y |
yogurt |
L. acidophilus LA5, B. animalis BB12, 1 × 10⁷ CFU |
9 wk | =FG | S↓ I, HOMA |
- | - |
[148] | 2014 | Iran | RD, DB, cross-over CT | T2DM 35–70 y 62/62 |
package |
L. sporogenes, 27 × 107 CFU 1.08 g inulin |
6 wk | =FG | S↓ I =HOMA-IR |
=CT, LDL-C, TG, HDL-C | - |
[149] | 2014 | Iran | RD, DB, CT | T2DM ov/ob obese 53.00 ± 5.9/ 49.00 ± 7.08 y 22/22 |
yogurt |
B. lactis Bb12, L. acidophilus strain La5, 3.7 × 106 CFU/g |
8 wk | S↓ HbA1c =FG |
- | - | - |
[150] | 2014 | Ireland | PC, DB, RD | Ob pregnant women, 31.4 ± 5.0/31.0 ± 5.2 y 63/75 |
capsule |
L. salivarius UCC118, 109 CFU |
4 wk | =FG | =I, HOMA-IR | =TC, HDL-C, LDL-C, TG | - |
[151] | 2014 | Australia | RD, DB, parallel study | Ov >55 y 40/37/39/40 |
Yogurt/ capsule |
L. acidophilus La5, B. lactis Bb12, 3 × 109 CFU/d |
6 wk | S↑ FG =HbA1c |
S↑ HOMA-IR =I |
- | - |
[152] | 2014 | India | RD, CT, DB |
Ov/ob healthy adults 40–60 y 15/15/15/15 |
capsule |
B. longum, B. infantis, B. breve, L. acidophilus, L. paracasei, L. bulgaricus, L. plantarum, S. thermophilus. 112.5 × 109 CFU/capsule |
6 wk | S↓ FG | S↓ I, HOMA-IR | S↓ TC, TG, LDL-C, VLDL-C S↑ HDL-C |
- |
[153] | 2014 | Japan | SB, PC, within-subject, repeated-measure intervention trial | Adults with hypertriacylglycerolemia, 51.1 ± 6.6 y 10/10 |
fermented mil |
L. gasseri SBT2055 (LG2055), 5 × 1010 CFU/100 g |
4 wk | S↑ HbA1c =FG |
=I | S↓ NEFA =TG, Apo B-48, TC, LDL-C, HDL-C |
- |
[154] | 2014 | Iran | RD, DB, PC, CT | NAFLD >18 y 26/26 |
capsule |
L. casei, L. rhamnosus, S. thermophilus, B. breve, L. acidophilus, B. longum, L. bulgaricus 2 × 108 CFU 250 mg FOS |
28 wk | S↓ FG | S↓ I, HOMA-IR | - | - |
[155] | 2014 | Iran | RD, DB, PC pilot study | Patients with MS >18 y 19/19 |
capsule |
L. casei, L. rhamnosus, S. thermophilus, B. breve, L. acidophilus, B. longum, L. bulgaricus 2 × 108 CFU 250 mg FOS |
28 wk | S↓ FG |
S↓ I, HOMA-IR S↑ QUICKI |
=LDL-C S↓ TG, CT S↑ HDL |
- |
[156] | 2014 | Iran | RD, PC, CT | Pregnant women 18–35 y 26/26 |
food |
L. sporogenes, 1 × 107 CFU 0.04 g inulin |
9 wk | =FG | S↓ I, HOMA-IR, HOMA-B S↑ QUICKI |
- | - |
[157] | 2014 | Iran | RD, DB, CT | T2DM 35–70 y 26/26/26 |
bread |
L. sporogenes, 1 × 108 CFU 0.07 g inulin |
8 wk | =FG | - | S↓ TG, VLDL-C, TC/HDL-C S↑ HDL-C = TC, LDL-C, HDL-C |
- |
[158] | 2015 | Germany | DB, RD, prospective, longitudinal pilot | Lean/ob participants 40–65 y 11/10 |
capsule |
L. reuteri, 2 × 1010 CFU |
8 wk | =blood glucose levels during OGTT | S↑ QUICKI in lean participants compared with obese | - | S↑ GLP-1, GLP-2 |
[159] | 2015 | Iran | RD, DB, PC, CT | T2DM 35–65 y 30/30 |
fermented milk (kefir) |
L. acidophilus, 3 × 106–25 × 106 L. casei, 2 × 106–15 × 106 B. lactis, 0.5 × 106–8 × 106 |
8 wk | S↓ HbA1c, FG | - | =TG, TC, LDL-C, HDL-C |
- |
[160] | 2015 | India | RD, CP, SB, pilot study | Healthy participants 20–25 y 15/15/15 |
capsule |
L. salivarius UBL S22, 2 × 109 CFU 10 g/d FOS |
6 wk | S↓ FG | S↓ I, HOMA-IR | S↓ TG, CT, LDL-C S↑ HDL-C |
- |
[161] | 2015 | Denmark | CT, DB, RD, PC, two-arm parallel | Young healthy adults 20–45 y 32/32 |
capsule |
L. casei W8, 1010 CFU |
4 wk | =FG | =I | S↓ TG =CT, HDL-C, LDL-C |
=GLP1 |
[162] | 2016 | Iran | RD, DB, PC, CT | GDM, 18–40 y 30/30 |
capsule |
L. acidophilus, 2 × 109 CFU/g L. casei, 2 × 109 CFU/g B. bifidum, 2 × 109 CFU/g |
6 wk | S↓ FG |
S↓ I, HOMA-IR, HOMA-B S↑ QUICKI |
S↓ TG, VLD-C, =TC, HDL-C |
- |
[163] | 2016 | Iran | RD, SB, CT | Ob/ov subjects 18–50 y 44/45 |
yogurt |
L. acidophilus LA5, B. lactis BB12 1 × 107 CFU |
12 wk | S↓ 2-h postprandial glucose, HbA1c =FG |
S↓ HOMA-IR, I | S↓ TC, LDL-C =HDL-C, TG |
- |
[164] | 2016 | Estonia | preliminary, open label study | Clinically healthy volunteers 50–75 y |
capsule |
L. fermentum ME-3 (LFME-3), 6 × 109 CFU |
4 wk | S↓ HbA1c | S↓ HOMA-IR | S↓ LDL-C, oxLDL, TC, TG, TG/HDL-C ratio S↑ HDL-C |
- |
[165] | 2017 | Sweden | RD, PC | T2DM 50–75 y 15/15/16 |
stick pack |
L. reuteri DSM 17938, 108 CFU/day L. reuteri DSM 17938, 1010 CFU/day |
12 wk | =FG =HbA1c |
S↑ QUICKI | =CT, HDL, LDL, TGL | - |
[17] | 2017 | Iran | RD, CT | T2DM, ov, CHD patients 40–85 y 30/30 |
capsule |
L. acidophilus, 2 × 109 L. casei, 2 × 109, B. bifidum, 2 × 109 CFU/g 800 mg inulin |
12 wk | S↓ FG | S↓ I, HOMA-B S↑ QUICKI =HOMA-IR |
S↑ HDL-C =TG, TC, LDL-C, VLDL-C, TC/HDL-C ratio |
- |
[166] | 2017 | Malaysia | RD, DB, parallel-group, CT | T2DM, 30–70 y 68/68 |
sachet |
L. acidophilus, L. casei, L. lactis, B. bifidum, B. longum, B. infantis, 1010 CFU/d each |
12 wk | S↓ HbA1c =FG |
S↓ I =HOMA-IR, QUICKI |
=TC, TG, LDL-C, HDL-C |
- |
[167] | 2017 | Brazil | DB, RD, PC, CT | T2DM 35–60 y 25/25 |
fermented goat milk |
L. acidophilus La-5, B. lactis BB-12, 109 CFU/d each |
6 wk | S↓ FS =HbA1c, FG |
= I, HOMA-IR | S↓ TC, LDL-C =HDL, VLDL, TG. CT/HLD-C ratio |
- |
[9] | 2017 | Saudi Arabia | DB, RD, CT | T2DM 30–60 y 48/46 |
sachet |
B. bifidum W23, B. lactis W52, L. acidophilus W37, L. brevis W63, L. casei W56, L. salivarius W24, Lactococcus lactis W19, Lactococcus lactis W58, 2.5 × 109 CFU/g |
12 wk | =FG | S↓ HOMA-IR = I |
=TG, TC, HDL-C, LDL-C, TC/HDL ratio | - |
[168] | 2017 | Iran | RD, DB, PC, CT | NAFLD patients with normal or low BMI >18 y 25/25 |
capsule |
L. casei, L. rhamnosus, S. thermophilus, B. breve, L. acidophilus, B. longum, L. bulgaricus 2 × 108 CFU |
28 wk | S↓ FG | =HOMA-IR, I, QUICKI | =LDL-C, HDL-C, TC S↓ TG |
- |
[169] | 2018 | Taiwan | DB, RD, PC | T2DM 25–70 y 25/25/24 |
capsule |
ADR-1 (live L. reuteri), 4 × 109 CFU cells of ADR-3 (heat-killed L. reuteri), 2 × 1010 CFU |
24 wk | =fasting blood glucose S↓ HbA1c in liver ADR-1 =HbA1c in heat-killed ADR03, |
=I, HOMA-IR | =LDL-C, free fatty acids S↓ TC in ADR-1 |
- |
[170] | 2018 | Iran | DB, RD, PC, parallel-group, CT | Prediabetes 40/40/40 35–75 y |
powder |
L. acidophilus, B. lactis, B. bifidum, B. longum 1 × 109 CFU/each inulin |
24 wk | S↓ FG, HbA1c | S↓ I, HOMA-IR S↑ QUICKI =HOMA-B |
- | - |
[171] | 2018 | Ukraine | DB, single center RD, CT | T2DM, ov 18–75 y 31/22 |
sachet | 14 alive probiotic strains of L.+ Lactococcus, 6 × 1010 CFU/g B., 1 × 1010 CFU/g, Propionibacterium, 3 × 1010 CFU/g, Acetobacter, 1 × 106 CFU/g |
8 wk | S↓ HbA1c =FG |
S↓ HOMA-IR =I |
- | - |
[172] | 2018 | Iran | RD, DB, PC, CT | T2DM, CHD 45–85 y 30/30 |
capsule |
L. acidophilus, B. bifidum, L. reuteri, L. fermentum 8 × 109 CFU/g |
12 wk | =FG |
S↓ I, HOMA-IR S↑ QUICKI |
S↑ HDL-C =LDL, TC, TG, VLDL-C |
- |
[82] | 2018 | Saudi Arabia | DB, RD, CT | T2DM, 30–60 y 30/31 |
sachet |
B. bifidum W23, B. lactis W52, L. acidophilus W37, L. brevis W63, L. casei W56, L. salivarius W24, Lactococcus lactis W19, Lactococcus lactis W58 2.5 × 109 CFU/g |
24 wk | S↓ FG, | S↓ I, HOMA-IR, | S↓ TC, TG, total/HDL-cholesterol ratio | - |
[173] | 2019 | Iran | parallel-group, RD, CT | T2DM, 20/20 30–50 y |
capsule |
L. casei, 108 CFU/d |
8 wk | S↓ FG =HbA1c |
S↓ I, HOMA-IR | - | - |
[174] | 2019 | Iran | RD, DB, CT | T2DM 30–75 y 34/34 |
capsule |
L. acidophilus, 2 × 109 CFU L. casei, 7 × 109 CFU L. rhamnosus, 1.5 × 109 CFU L. bulgaricus, 2 × 108 CFU B. breve, 3 × 1010 CFU B. longum, 7 × 109 CFU S. thermophilus, 1.5 × 109 CFU 100 mg FOS |
6 wk | S↓ FG | =I, HOMA-IR | S↑ HDL-C =TG, TC |
- |
[175] | 2019 | India | RD, DB, CT | T2DM, Ob 18–65 y 39/40 |
capsule |
L. salivarius, L. casei, L. plantarum, L. acidophilus, B. breve, B. coagulans, 30 billion CFU 100 mg FOS |
12 wk | S↓ HbA1c =FG |
=I, HOMA-IR | = TC, TG, HDL-C, LDL-C | - |
[133] | 2019 | Belgium | RD, DB, PC, pilot study | Ob/ov insulin-resistant volunteers 18–70 y 14/13/13 |
sachet | Live/pasteurized Akkermansia municiphila 1010 bacteria/day |
12 wk | =FG, HbA1c | S↑ insulin sensitivity S↓ I |
S↓ TC =LDL-C, TG |
=GLP-1 |
[176] | 2020 | Australia | RD, DB, CT | T2DM BMI ≥ 25 kg/m2 ≥ 18 y 30/30 |
capsule |
L. plantarum, 6 × 109 CFU, L. bulgaricus, 3 × 109 CFU L. gasseri, 18 × 109 CFU B. breve, 7.5 × 109 CFU B. animalis sbsp. lactis, 8 × 109 CFU B. bifidum, 7 × 109 CFU S. thermophiles, 450 × 106 CFU Saccharomyces boulardii, 45 × 106 CFU |
12 wk | S↓ FG, HbA1c (in patients taking probiotics and metformin) |
S↓ HOMA-IR (in patients taking probiotics and metformin) |
- | - |
RD, randomized; DB, double-blind; PC, placebo-controlled; SB, single-blind; CT, clinical trial; T2DM, type 2 diabetes mellitus; Ob, obese; NASH, Nonalcoholic steatohepatitis; Ov, Overweight; NAFLD, Non-alcoholic fatty liver disease; MS, Metabolic syndrome; GDM, gestational diabetes mellitus; CHD, coronary heart disease; L., Lactobacillus; B., Bifidobacterium; S., Streptococcus; CFU, colony-forming units; FOS, fructooligosaccharides; wk, weeks; d, days; FG, fasting glucose fasting blood glucose, fasting plasma glucose, glycemia, fasting blood sugar; HbA1c, Hemoglobin glycated; OGTT, glucose tolerance test; I, serum insulin concentration, insulin concentration, serum insulin level, insulin; HOMA, homeostatic model assessment; HOMA-IR, homeostasis model of assessment-estimated insulin resistance; QUICKI, quantitative insulin sensitivity check index; HOMA-B, homeostasis model assssessment of β-cell dysfunction; TG, triglycerides; VLDL, very-low-density lipoprotein; TC, total cholesterol; HDL-C, high-density lipoprotein; LDL-C, low-density lipoprotein; NEFA, non-esterified fatty acids; Apo B-48, apolipoprotein B-48; oxLDL, oxidatively modified low density lipoprotein; GLP-1, Glucagon-like peptide-1; GLP-2, Glucagon-like peptide-2; =, non significan; S, significant; ↑, increase; ↓, decrease.