Effects of probiotics on the lipid profile: systematic review

Gadelha, Carlos Jorge Maciel Uchoa; Bezerra, Alane Nogueira

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Jornal Vascular Brasileiro

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REVIEW ARTICLE • J. Vasc. Bras. 18 • 2019 • https://doi.org/10.1590/1677-5449.180124 copy

Effects of probiotics on the lipid profile: systematic review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Alterations in the intestinal microbiota can modulate mechanisms involving risk factors for cardiovascular diseases, including dyslipidemias The objective was to review the effects of probiotic supplementation on the prevention and treatment of changes to the lipid profile. The searches were run on the PubMed database, using the descriptors “probiotics and lipid profile” and “probiotics and dyslipidemia,” with publication dates restricted to 2013 to 2018. Supplementation with probiotics significantly reduced total cholesterol, LDL-c, and triglycerides and increased HDL-c. Some benefits were observed on anthropometric variables, glycemic control, oxidative stress, inflammation, and immune system. The present study suggests that probiotic supplementation should be indicated as adjunctive treatment for dyslipidemias. Further studies should be developed to clarify long-term effects, as well as the influence of probiotics in combination with drug therapy.

Keywords:
dyslipidemias; hypercholesterolemia; probiotics

Authors/Type of study	Description of samples	Objectives	Results	Limitations	Conclusions
Ahn et al. (2015)¹²12 Ahn HY, Kim M, Chae JS, et al. Supplementation with two probiotic strains, Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032, reduces fasting triglycerides and enhances apolipoprotein AV levels in non-diabetic subjects with hypertriglyceridemia. Atherosclerosis. 2015;241(2):649-56. http://dx.doi.org/10.1016/j.atherosclerosis.2015.06.030. PMid:26117402. http://dx.doi.org/10.1016/j.atherosclero... /Clinical trial.	121 non-diabetic people with hypertriglyceridemia.	To investigate the effects of supplementation with two strains, Lactobacillus curvatus HY7601 and L. plantarum KY1052, on capacity for reduction of TG in non-diabetics with borderline and moderate hypertriglyceridemia.	Between the groups, there was a 18.3% reduction in TG and a 15.6% reduction in LDL particle size and a 21.1% increase in apo A-V (p<0.05). TG and apo A-V values were inversely correlated.	Short duration, small sample, no control of diet, and no analysis of the IM.	The authors concluded that supplementation with these strains reduced serum TG levels, and the greatest effect was observed in subjects with higher levels.
	Intervention period: 12 weeks.
	IG: 2 grams of powder containing Lactobacillus curvatus HY7601 and L. plantarum KY1052, 0.5 x 10¹⁰ CFU of each.
	PG: 2 grams of powder, with no microorganisms
Bernini et al. (2016)¹³13 Bernini LJ, Simão ANC, Alfieri DF, et al. Beneficial effects of Bifidobacterium lactis on lipid profile and cytokines in patients with metabolic syndrome: a randomized trial. Effects of probiotics on metabolic syndrome. Nutrition. 2016;32(6):716-9. http://dx.doi.org/10.1016/j.nut.2015.11.001. PMid:27126957. http://dx.doi.org/10.1016/j.nut.2015.11.... /Clinical trial.	51 people with metabolic syndrome aged from 18 to 60 years.	To assess the influence of milk fermented with Bifidobacterium lactis HN019 on the lipid profile, glycemic control, and inflammatory profile of patients with metabolic syndrome.	Significant reductions were observed in TC (p=0.009) and LDL-c (p=0.008).	Short duration, small sample, and no analysis of the IM.	The data showed potential effects of Bifidobacterium lactis HN019 on reduction of lipids in the blood.
	Intervention period: 45 days.
	IG: 26 subjects, consumed milk fermented with 2.72 x 10^¹⁰10 Coppola MM, Gil-Turnes C. Probióticos e resposta imune. Cienc Rural. 2004;34(4):1297-303. http://dx.doi.org/10.1590/S0103-84782004000400056. http://dx.doi.org/10.1590/S0103-84782004... CFU of Bifidobacterium lactis HN019.
	PG: no intervention.
Cavallini et al. (2016)¹⁴14 Cavallini DC, Manzoni MS, Bedani R, et al. Probiotic soy product supplemented with isoflavones improves the lipid profile of moderately hypercholesterolemic Men: a randomized controlled trial. Nutrients. 2016;8(1):52. http://dx.doi.org/10.3390/nu8010052. PMid:26797632. http://dx.doi.org/10.3390/nu8010052... /Clinical trial.	49 hypercholesterolemic males aged 45 to 48 years.	To investigate the influence of a soy product fermented with Enterococcus faecium CRL 183 and Lactobacillus helveticus 416 plus isoflavones.	Only subjects in G1 exhibited a significant reduction in TC. When compared with G2, the result at the end of the study was reduction in LDL-c (p<0.05) in both treatment groups, from days 30 to 42, and also in the TC/HDL ratio.	Short duration, small sample, and no analysis of the IM.	Regular consumption of the probiotics Enterococcus faecium CRL 183 and Lactobacillus helveticus 416 contributed to a reduction in markers of cardiovascular risk in hypercholesterolemic men, with improved lipid profile and reduced oxidation of LDL particles.
	Intervention period: 42 days.
	G1: 200 mL of soy product fermented with the probiotic Enterococcus faecium CRL 183 and Lactobacillus helveticus 416, supplemented with isoflavone.
	G2: 200 mL unfermented soy product.
Childs et al. (2014)¹⁵15 Childs CE, Röytiö H, Alhoniemi E, et al. Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study. Br J Nutr. 2014;111(11):1945-56. http://dx.doi.org/10.1017/S0007114513004261. PMid:24661576. http://dx.doi.org/10.1017/S0007114513004... /Clinical trial.	43 healthy subjects, aged from 25 to 65 years.	To investigate the effects of xylo-oligosaccharide and Bifidobacterium animalis BI–07 on the IM and on immune function.	Higher HDL levels were observed in subjects given xylo-oligosaccharide, with no difference in the other plasma lipid levels tested.	Short duration and small sample.	The data indicate potential benefits of the xylo-oligosaccharide and Bifidobacterium animalis BI–07 on the capacity to increase HDL.
	Four different treatments were tested (G1: maltodextrin; G2: Bifidobacterium animalis BI–07, 10⁹ CFU; G3: xylo-oligosaccharide, 8 g/d; G4: Bifidobacterium animalis BI–07, 10⁹ CFU + xylo-oligosaccharide, 8 g/d).
	Intervention period: 21 days, followed by 28 days’ washout.
Dong et al. (2013)¹⁶16 Dong H, Rowland I, Thomas LV, Yaqoob P. Immunomodulatory effects of a probiotic drink containing Lactobacillus casei Shirota in healthy older volunteers. Eur J Nutr. 2013;52(8):1853-63. http://dx.doi.org/10.1007/s00394-012-0487-1. PMid:23307112. http://dx.doi.org/10.1007/s00394-012-048... /Clinical trial.	30 healthy volunteers aged 55 to 74 years.	To test probiotics on the immune systems of people with immunosenescence.	The data indicated that there was no significant reduction in TC or TG..	Short duration, small sample, lack of data on the lipid profile, and no analysis of the IM.	Consumption of the probiotic Lactobacillus casei Shirota did not have a significant effect on the lipid profile.
	Intervention period: 4 weeks.
	IG: Lactobacillus casei shirota with 1.3 x 10¹⁰ CFU/day.
	PG: skimmed milk without the probiotic.
Dönmez et al. (2014)¹⁷17 Dönmez N, Kısadere İ, Balaban C, Kadiralieva N. Effects of traditional homemade koumiss on some hematological and biochemical characteristics in sedentary men exposed to exercise. Biotech Histochem. 2014;89(8):558-63. http://dx.doi.org/10.3109/10520295.2014.915428. PMid:24893332. http://dx.doi.org/10.3109/10520295.2014.... /Clinical trial.	18 sedentary males with a mean age of 33.66 years.	To investigate the effects of koumiss as a probiotic, in combination with physical exercise, on hematological and biochemical variables in sedentary people	TC and TG tended to reduce in all groups, but only in G2 at day 15. HDL increased in all groups, and the greatest effect was observed in G2	Short duration, small sample, and no analysis of the IM.	The findings suggest that koumiss plus physical exercise provoked an increase in HDL.
	Intervention period: 15 days.
	G1: koumiss;
	G2: koumiss plus physical exercise.
	G3:physical exercise.
	Main probiotics used to ferment koumiss: L. delbrueckii subsp. Bulgaricus, L. salivarus, L. buchneri, L. plantarum, L. casei, L. helveticus, and L. fermentum.
Fuentes et al. (2013)¹⁸18 Fuentes MC, Lajo T, Carrión JM, Cuñé J. Cholesterol-lowering efficacy of Lactobacillus plantarum CECT 7527, 7528 and 7529 in hypercholesterolaemic adults. Br J Nutr. 2013;109(10):1866-72. http://dx.doi.org/10.1017/S000711451200373X. PMid:23017585. http://dx.doi.org/10.1017/S0007114512003... /Clinical trial.	60 hypercholesterolemic subjects, aged 18 to 65 years.	To evaluate the effects of the AB-LIFE® formula on concentrations of lipids and on other parameters related to cardiovascular risk in hypercholesterolemic subjects.	The intervention significantly reduced TC and caused a trend to reduction of LDL-c and OX-LDL, compared with the PG. In the IG, there were significant (p<0.05) reductions in TC, LDL-C, LDL-C:HDL-C ratio, and OX-LDL (13.6%, 14.7%, 19.7%, and 13.6%, respectively), in relation to baseline. The increase in HDL-C (p<0.05) was only observed in the IG.	Short duration, small sample, and no analysis of the IM.	Supplementation with Lactobacillus plantarum CECT (7527, 7528, and 7529) made a significant contribution to reducing serum cholesterol in hypercholesterolemic patients, exhibiting better effects in those with higher cholesterol levels.
	BMI: 19-30 kg/m².
	Intervention period: 12 weeks.
	IG: 1 capsule of Lactobacillus plantarum CECT (7527, 7528 and 7529) containing a 1.2 x 10⁹ CFU dose.
	PG: 1 capsule containing no bacteria.
Gomes et al. (2017)¹⁹19 Gomes AC, Sousa RGM, Botelho PB, Gomes TLN, Prada PO, Mota JF. The additional effects of a probiotic mix on abdominal adiposity and antioxidant Status: a double‐blind, randomized trial. Obesity (Silver Spring). 2017;25(1):30-8. http://dx.doi.org/10.1002/oby.21671. PMid:28008750. http://dx.doi.org/10.1002/oby.21671... /Clinical trial.	43 women, aged 20 to 59 years, with BMI in the range 24-40 kg/m².	To investigate whether a mix of probiotics has additional effects, when compared with a dietary intervention alone, on body composition, lipid profile, endotoxemia, inflammation, and antioxidant and anti-inflammatory profiles.	There was no difference between groups in LDL-c, just a reduction in results for polyunsaturated fatty acids (PG= -5.65% vs. IG = - 18.63%, at p<0.04).	Short duration, small sample, and no analysis of the IM.	Supplementation with the mixture of probiotics had an additional effect when compared with the group with only a dietary intervention.
	Intervention period: 8 weeks.
	IG: dietary intervention plus mixture of Lactobacillus acidophiluse, L. casei; Lactococcus lactis; Bifidobacterium bifidum and lactis, at a dosage of 2 × 10¹⁰.
	PG: Dietary intervention only.
Ivey et al. (2015)²⁰20 Ivey KL, Hodgson JM, Kerr DA, Thompson PL, Stojceski B, Prince RL. The effect of yoghurt and its probiotics on blood pressure and serum lipid profile: a randomised controlled trial. Nutr Metab Cardiovasc Dis. 2015;25(1):46-51. http://dx.doi.org/10.1016/j.numecd.2014.07.012. PMid:25171898. http://dx.doi.org/10.1016/j.numecd.2014.... /Clinical trial.	156 people with metabolic syndrome and mean age of 67 years.	To determine the effect of Lactobacillus acidophilus La5 and Bifidobacterium animalis, subspecies lactis Bb12, in the form of yoghurt or capsules, on blood pressure and the lipid profile in men and women with metabolic syndrome.	There were no differences in lipid profile markers between groups (p<0.05).	Short duration, small sample, and no analysis of the IM.	The probiotic strains Lactobacillus acidophilus La5 and Bifidobacterium animalis, subspecies lactis Bb12 did not influence changes in lipid profile parameters, probably because baseline cholesterol values were relatively good.
	Intervention period: 6 weeks.
	G1: yoghurt, plus placebo capsule; G2: probiotic capsule plus milk; G3 and G4: placebos.
	Subjects who consumed the probiotic ingested at least 3 x 10⁹ CFU/day.
	Lactobacillus acidophilus La5 and Bifidobacterium animalis, subspecies lactis Bb12 were used.
Kullisaar et al. (2016)²¹21 Kullisaar T, Zilmer K, Salum T, Rehema A, Zilmer M. The use of probiotic L. fermentum ME-3 containing Reg’Activ Cholesterol supplement for 4 weeks has a positive influence on blood lipoprotein profiles and inflammatory cytokines: an open-label preliminary study. Nutr J. 2016;15(1):93. http://dx.doi.org/10.1186/s12937-016-0213-6. PMid:27793203. http://dx.doi.org/10.1186/s12937-016-021... /Clinical trial.	45 healthy volunteers aged 50 to 75 years, with BMI from 24-30 kg/m² and borderline risk factors for cardiovascular disease.	To determine whether the special formulation Reg’active Cholesterol® has a positive effect on the cardiovascular system, lipid and inflammatory profiles, and glycated hemoglobin.	All participants exhibited significant reductions in LDL-c, TC, TG, and OX-LDL (p<0.05) and a tendency to improvements in HDL.	Short duration, no control group, small sample, no dietary control before or after the intervention, no analysis of the IM, and use of a compound formula containing several nutrients.	Consumption of the formula by people with borderline cardiovascular risk values over a 4-week period had a positive effect on reduction of LDL-c, TC, TG and OX-LDL.
	Intervention period: 4 weeks.
	IG: 2 capsules per day containing the probiotic L. fermentum ME-3 (6 x 10⁹ CFU/day), plus other compounds.
Ogawa et al. (2014)²²22 Ogawa A, Kadooka Y, Kato K, Shirouchi B, Sato M. Lactobacillus gasseri SBT2055 reduces postprandial and fasting serum non-esterified fatty acid levels in Japanese hypertriacylglycerolemic subjects. Lipids Health Dis. 2014;13(1):36. http://dx.doi.org/10.1186/1476-511X-13-36. PMid:24548293. http://dx.doi.org/10.1186/1476-511X-13-3... /Clinical trial.	20 people with a mean age of 51.1 years and hypertriglyceridemia.	To examine the effects of the probiotic Lactobacillus gasseri SBT2055 (LG 2055) on postprandial response of blood lipids in Japanese subjects with hypertriglyceridemia.	With relation to fasting parameters, only non-esterified fatty acid levels exhibited a significant reduction (p<0.01). There was no significant difference in TG, TC, HDL, or LDL.	Short duration, small sample, and no analysis of the IM.	Consumption of the probiotic reduced non-esterified fatty acid levels after an oral fat overload and during the post-ingestion period of the probiotic, after 4 weeks consuming the microorganism.
	Intervention period: 4 weeks.
	IG: 5 x 10¹⁰ CFU/day of Lactobacillus gasseri SBT2055 (LG 2055), with a frequency of 2 times a day.
Rajkumar et al. (2014)²³23 Rajkumar H, Mahmood N, Kumar M, Varikuti SR, Challa HR, Myakala SP. Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: a randomized, controlled trial. Mediators Inflamm. 2014;2014:348959. http://dx.doi.org/10.1155/2014/348959. PMid:24795503. http://dx.doi.org/10.1155/2014/348959... /Clinical trial.	60 overweight people aged 40 to 60 years.	To investigate whether probiotics, alone or in combination with omega 3, provoke any improvement in the lipid profile, insulin sensitivity, or inflammatory response in healthy overweight people.	G1: HDL increased by 18.5% (p<0.01), and LDL (p<0.05), TG, and VLDL (p<0.01) values reduced by 7.04%, 5.8%, and 12.98, respectively.	Short duration, small sample, difficult to identify the effect of any specific strain	An increase in HDL and reductions in TG, LDL, and VLDL were observed and the best results were observed in G3.
	Intervention period: 6 weeks.		G2: HDL increased by 23.2% and LDL reduced by 10.7%, TG reduced by 7.78%, and VLDL reduced by 7.78% (p<0.01).
	G1: 112.5 x 10⁹ CFU with: Bifidobacterium longum, Bifidobacterium infantis, Bifidobacterium breve, Lactobacillus acidophilus, Lactobacillus paracasei, Lactobacillus delbrueckii, subspecies bulgaricus, Lactobacillus plantarum, and Streptococcus salivarius subspecies thermophilus.
	G2: omega 3: 1 capsule with 180 mg of EPA and 120 mg of DHA.		G3: TC, TG, LDL, and VLDL reduced and HDL increased by 6.7% (p<0.01).
	G3: probiotics and omega 3.
Ryan et al. (2015)²⁴24 Ryan JJ, Hanes DA, Schafer MB, Mikolai J, Zwickey H. Effect of the probiotic Saccharomyces boulardii on cholesterol and lipoprotein particles in hypercholesterolemic adults: a single-arm, open-label pilot study. J Altern Complement Med. 2015;21(5):288-93. http://dx.doi.org/10.1089/acm.2014.0063. PMid:25893960. http://dx.doi.org/10.1089/acm.2014.0063... /Clinical trial.	11 hypercholesterolemic men, aged 21 to 69 years.	To collect evidence on the effects of the probiotic Saccharomyces boulardii on the lipid profile and other markers in hypercholesterolemic adults.	Compared with baseline, only RLP exhibited a significant reduction (p<0.03). No changes were observed in the other variables studied.	Short duration, small sample, no analysis of the IM, no PG, and no dietary control.	The most promising result was a reduction in RLP-p, after 8 weeks, with therapeutic potential for treating cardiovascular diseases.
	Intervention period: 8 weeks.
	IG: 5.6 x 10¹⁰ CFU/day of Saccharomyces boulardii.
Tonucci et al. (2017)²⁵25 Tonucci LB, Santos KMO, de Oliveira LL, Ribeiro SMR, Martino HSD. Clinical application of probiotics in type 2 diabetes mellitus: A randomized, double-blind, placebo-controlled study. Clin Nutr. 2017;36(1):85-92. http://dx.doi.org/10.1016/j.clnu.2015.11.011. PMid:26732026. http://dx.doi.org/10.1016/j.clnu.2015.11... /Clinical trial.	45 people aged 35 to 60 years with type 2 DM.	To investigate the effects of consumption of fermented goat’s milk containing Lactobacillus acidophilus La-5, Bifidobacterium animalis lactis BB-12, glycemic control, lipid profile, inflammation, oxidative stress, and short-chain fatty acids.	LDL and TG increased in the PG, which indicates a protective effect of the probiotics in the IG. There were significant difference between groups in mean change in TC (p=0.04) and LDL (p=0.03).	Short duration, small sample, and no group that did not consume fermented milk.	Consumption of Lactobacillus acidophilus La-5 and Bifidobacterium animalis lactis BB reduced LDL-c and TC.
	Intervention period: 6 weeks.
	IG: 120 g/day of milk fermented with probiotics (Lactobacillus acidophilus La-5, Bifidobacterium animalis lactis BB-12; 10⁹ CFU of each).
	PG: 120 g/day of conventional fermented milk with Streptococcus thermophilus TA-40.

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[1] Conflicts of interest: No conflicts of interest declared concerning the publication of this article.