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Bifidobacteria in Hypercholesterolemia
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This entry is adapted from the peer-reviewed paper 10.3390/microorganisms9040836

Strains belonging to the genera Bifidobacterium and Lactobacillus are able to reduce skin disorders. They play an important role in modulating the cutaneous immune response and are able to promote the differentiation of normal human keratocytes inducing a high expression of differentiation markers. Moreover, some strains showed the ability to assimilate cholesterol and to produce shorty chain fatty acid, reducing the total cholesterol levels. 

Bidifobacterium longum Bidifobacterium bifidum dermatitis syndrome eczema cholesterol SCFAs BDNF gut microbiota skin microbiota COVID-19

1. Introduction

Bifidobacteria colonize the human gastrointestinal tract early on in life, their interaction with the host starting soon after birth. The health benefits are strain specific and could be due to the produced polysaccharides. The consumption of probiotics may prevent obesity, irritable bowel syndrome, eczema or atopic dermatitis, and asthma. Non-replicative strains of Bifidobacterium longum (NCC3001 and NCC2705) promote the differentiation of normal human epidermal keratinocytes (NHEKs), inducing a high expression of differentiation markers (keratin —KRT1—, and transglutaminase —TGM1—) and pro-regeneration markers (cathepsins), including β-defensin-1, which plays an important role in modulating the cutaneous immune response. Strains belonging to the genera Bifidobacterium and Lactobacillus can increase tight-junction proteins in NHEKs and enhance barrier function. Bifidobacteria and lactobacilli may be used as prophylactic or therapeutic agents towards enteric pathogens, antibiotic-associated diarrhea, lactose intolerance, ulcerative colitis, irritable bowel syndrome, colorectal cancer, cholesterol reduction, and control of obesity and metabolic disorders. Bifidobacterium bifidum showed an in vitro capability of lowering cholesterol levels thanks to its absorption into the bacterial membrane. Several strains of the species Lactobacillus acidophilus, L. delbrueckii subsp. bulgaricus, L. casei, and L. gasseri led to a reduced amount of serum cholesterol due to their ability to assimilate cholesterol (in vitro). Lactococcus lactis KF147 and Lactobacillus plantarum Lp81 have also been shown to reduce cholesterol levels by 12%. Clarifying the specific health mechanisms of Bifidobacterium and Lactobacillus strains in preventing high-cost pathologies could be useful for delineating effective guidelines for the treatment of infants and adults.

2.  Bifidobacteria and Their Role in Hypercholesterolemia

Among the microorganisms with claimed probiotic properties are several strains belonging to the genera Bifidobacterium and Lactobacillus. The healthy claims are strain specific and cannot be arbitrarily extended to other strains even if they belong to the same species [1][2][3]. The strain-specific claims are the results of well-designed double-blinded and placebo-controlled studies [1][2]. Moreover, the health effects can be due to produced metabolites, such as short-chain fatty acids (SCFAs) or exopolysaccharides [4][5][6][7], which can also exert different effects with respect those of the produced strain [8].
The genera Bifidobacterium and Lactobacillus are considered as very promising for the prevention of total cholesterol (TC) regulation, also in pharmaceutical approaches. A large number of in vitro and in vivo studies have shown that probiotics do have hypolipidemic effects [9].
Bifidiobacterium and Lactobacillus have therefore triggered great interest amongst researchers for the treatment of cardiovascular disease. Animal models have demonstrated that these strains are able to reduce hepatic cholesterol levels, improve the adsorption of nutrients, and increase the production of short-chain fatty acids (SCFAs) [6]. SCFAs are produced mainly by Bifidobacterium, Bacteroides, Clostriudium, Provotella, and Ruminococcus and are implicated in sympathetic system activation and the maintenance of lymphocyte influx to the gut epithelium. A reduction in acetate levels is involved in hypertension in sleep apnea. Propionate administration leads to a reduction of systolic and diastolic blood pressure. Instead, butyrate administration ameliorates vascular function. Moreover, SCFAs can activate G-protein coupled receptors (Gpr41, Gpr43, Gpr109a, and Olfr78), regulating renin secretion and blood pressure [4][7]. In vivo studies have demonstrated that the supplementation of acetate, butyrate, and propionate in rats/Syrian hamsters administered high levels of dietary cholesterol led to a decrease in CT levels and the LDL-C/HDL-C ratio and an increase in the fecal excretion of Bas, such as CA, CDCA, LCA, and DCA [6].
Moreover, they can modulate the peripheral expression of the bdnf gene in zebrafish [10]. A rat model demonstrated that Bifidobacterium longum BB536 significantly reduced total cholesterol, low-density lipoprotein cholesterol, high-density lipoprotein cholesterol, very low-density lipoprotein cholesterol, and atherosclerotic index levels as well as liver lipid deposition, adipocyte size, and positively affected liver and kidney function [11].
In 2009, an Italian research group studied the activity of Lactobacillus plantarum and Lactobacillus paracasei, isolated from Castelmagno D.O.P. cheese, in lowering cholesterol in vitro (without presence of bile) [12]. Another study confirmed the cholesterol-lowering effects of L. plantarum studied in rats [13]. In 1985, Gilliland et al. noted that cholesterol could be assimilated by Lactobacillus acidophilus. The study demonstrated that Lactobacillus acidophilus RP 32 significantly inhibited the increase of serum cholesterol in pigs, and the researchers hypothesized a direct action of the microorganism on the molecule [14]. Another in vitro study in 2000 confirmed this hypothesis [15]. In 2018, an article [16] was published that highlighted a decrease in circulating cholesterol in a murine model treated with Lactobacillus rhamnosus BFE5264 isolated from Maasai fermented milk. This discovery could at least partly explain the results of a 1975 group-control study in which Mann et al. (treatment group fed with typical Maasai fermented milk with additional fat and a second control group with milk and placebo) noted that there was no difference in the total cholesterol of each of the groups, assuming an intrinsic factor in milk helps the body to break down exogenous cholesterol [17].
However, there is some controversy in human clinical studies about the lipid-lowering effect of probiotics. Some research has argued against this role [9]. A recent metanalysis by Wang et al. (2018) compared 32 studies with 1971 participants and showed that there is a decrease in total cholesterol when lactobacilli and bifidobacteria are used as dietary supplements in various foods. This overall reduction in the sum of all studies was found to be on average −13.27 mg/dL, 95% CI (−16.74; −9.80), p < 0.05 [9]. Further studies should be performed to evaluate how bifidobacterial and SCFA production can modulate TC levels and vascular disease progression. Table 1 shows the main clinical and experimental studies on atopic dermatitis and hypercholesterolemia recently performed on bifidobacteria alone and in combination with lactobacilli.

3. Bifidobacteria and Their Therapeutic Potential in Eczema

The genus Bifidobacterium has been shown to be reduced in the gut microbiota of infants, children, and young adults with eczema. Skin disorders are related to a defect in the barrier beyond the skin and the intestinal mucosa, where gut microbiota contribute to the maintenance of intestinal permeability. On the contrary, the gut barrier breakdown leads to an intestinal permeability increase and a consequent bacterial and endotoxin (lipopolysaccharide, LPS) translocation into the systemic circulation, leading to immune disorders [18]. A reduction of plasmatic LPS levels was observed in patients treated with Bifidobacterium breve BR03 in combination with Lactobacillus salivarius LS01 [19]. Evidence indicates that strains belonging to the genus Bifibobacterium and Lactobacillus have immunomodulatory effects, stimulating T helper 1 (Th1) cytokines and suppressing the T helper 2 (Th2) response, which is increased in chronic eczema. In particular, the production of IL-10 and TGF-beta (tumor growth factor) is stimulated [20]. Moreover, strains belonging to the species Bifidobacterium longum are able to promote the production of antimicrobial peptides in keratinocytes and to produce metabolites, such as lipids, which can help skin commensals avoid pathogenic strains’ colonization [21]. The development of allergic diseases in children seems to be related to a defect in the early stimulation of Th1 cells. Eczema is considered a multifactorial disease, associated with epigenetic, genetic, developmental, and environmental factors. Studies have demonstrated that infants suffering from eczema show less gut colonization by strains belonging to the genus Bifidobacterium and Lactobacillus, with a prevalence in skin microbiota of strains belonging to Clostridium spp. and Staphylococcus spp. as compared to healthy children [22][19][23]. Strains belonging to the genus Bifidobacterium and Lactobacillus are able to interact with the immune system, modulating Th1 cytokine production and the Th2 response. They also show an ability to regulate regulatory T cells (Tregs), diminishing the inflammatory pathway; in particular, they are able to decrease immune globulin E (IgE), interferon-gamma, and eosinophilia [24][25][26][27]. Bifidobacteria adolescentis treatments reduced ear and skin thickness and suppressed eosinophils and mast cell infiltration. Th1- and Th2-type responses were regulated and the Tregs population was promoted in the spleen by B. adolescentis treatments. The strains Bifidobacterium adolescentis Ad1, B. adolescentis Ad2, B. adolescentis Ad3, B. adolescentis Ad4, B. adolescentis Ad5, and B. adolescentis Ad6 led to an increase in the relative abundance of the genus Lactobacillus and to a decrease in the relative abundance of the genera Dorea and Pediococcus. Moreover, the strains B. adolescentis Ad1, B. adolescentis Ad3, and B. adolescentis Ad6 decreased ear thickness; and the strains B. adolescentis Ad1 and B. adolescentis Ad3 alleviated AD clinical symptoms. The strains B. adolescentis Ad1, B. adolescentis Ad4, B. adolescentis Ad5, and B. adolescentis Ad6 significantly reduced serum immune globulin E (IgE) levels and IL-4 levels [28].

Lise et al. (2019) [22] reported a clinical case regarding a female 18-month-old child who showed xerosis, Dennie–Morgan double fold, and areas of erythema and lichenification in the antecubital fossae, abdomen, and legs. The scoring atopic dermatitis index (SCORAD) was 60.15, body surface area (BSA) was 60%, family dermatology life quality index (FDLQI) was 18, and IgE was 140 kU/L (normal value: <60 kU/L). The young patient was treated with a mixture of Bifidobacterium lactis HN019, Lactobacillus acidophilus NCFM, Lactobacillus rhamnosus HN001, and Lactobacillus paracasei LPC37 once a day after a bath for two weeks. After treatment, all parameters improved: the SCORAD was 4.95 and BSA 0% while the FDLQI was 8.

Moreover, it has been demonstrated that non-replicative Bifidobacterium longum NCC2705 and Bifidobacterium longum NCC3001 (heat treated), Bifidobacterium longum BL/81, and sonicated Bifidobacterium longum BL/84 cells promote differentiation markers (keratin KRT1, KRT10, and transglutaminase TGM1) of human keratinocytes (NHEKs) during pre-confluent and confluent stadiums. Moreover, the expression of antimicrobial peptides, such as beta-defensin-1 and BDEF, as well as the molecules involved in wound healing, such as cathepsins B, D, and H, was significantly elevated in post-confluent NHEKs after treatment with Bifidobacterium longum non-replicative strains and extracts. These results were confirmed by the levels of mRNA transcripts. The mechanism could be related to the ability to increase intracellular calcium levels, inducing a calcium influx from the extracellular medium [29]. One other mechanism proposed in recent literature is an increased expression of brain-derived neurotrophic factor (BDNF) starting from butyrate, which is one of the main SCFAs derived from oligosaccharides, such as fructooligosaccharides (FOSs) and galactolygosaccharides (GOSs), through metabolism by bifidobacteria [30][31][32][33]. Thus, for example, Bifidobacterium longum BL986 orally administered in mice led to an increase in the mRNA expression of BDNF and caused a decrease in glutathione-disulfide reductase (Gsr), superoxide dismutase (Sod), catalase (Cat), tumour necrosis factor (Tnf), Il-6, and Il-1b expression in peripheral tissue [34]. The suppression of Il-1b due to Bifidobacterium breve B-3 metabolic activity increased cathepsin L-like protease activity, reducing the incidence of atopic eczema [35][36][37][38]. Future studies are needed to further evaluate how live or killed bifidobacteria can be used in topic formulations to ameliorate the progression of atopic dermatitis symptoms thanks to a restored balance between friend and foe strains.

Table 1. Main clinical and experimental studies and principal strain-specific effects of bifidobacteria, used alone and in combination with lactobacilli, on hypercholesterolemia and atopic dermatitis.

Table
Strain Dosage/Dye Study Design/Subjects Principal Results References
Bifidobacterium animalis subsp. lactis BB-12 1 × 109 CFU/g 1 Infants ↓ Neutral lipids in plasma
↑ Phospholipids		 Kankaanpaa et al. (2002) [39]
Bifidobacterium longum BB536 3 × 107 CFU/mL 3 Rat model ↓ Total cholesterol
↓ Liver lipids deposition
↓ Adipocyte size		 Al-Sheraji et al. (2015) [11]
Bifidobacterium infantis 35624 1 × 1010 CFU/mL 3 Human ↓ C-reactive protein level
↓ TNF-alfa		 Groeger et al. (2013) [40]
Bifidobacterium breve B-3 2 × 109 CFU/mouse 2 Mouse model ↓ IL-1beta
↓ Claudin-1
↓ skin damage
↑ TJs integrity		 Satoh et al. (2015) [37]
Bifidobacterium adolescentis Ad1-6 1 × 109 CFU/0.2 mL Mouse model 4 ↓ IgE
↓ IL-4
↓ AD-simptoms		 Fang et al. (2019) [40]
Bifidobacterium breve BR03
Lactobacillus salivarius LS01		 1x109 CFU/g 5 Human ↓ SCORAD Iemoli et al. (2012) [41]
Bifidobacterium longum CECT 7347
Bifidobacterium lactis CECT 8145
Lactobacillus casei CECT 9104		 1 × 109 CFU/mL 6 Human 7 ↓ AD SCORAD Navarro-López et al. (2018) [42]
Bifidobacterium breve Bbi99
Lactobacillus rhamnosus GG
Lactobacillus rhamnosus LC705
Propionibacterium freudenreichii spp. shermanii JD		 2 × 108 CFU/mL
5 × 109 CFU/mL
5 × 109 CFU/mL
2 × 109 CFU/mL 8		 Infants ↓ AD rates Kukkonen et al. (2007) [36]
Bifidobacterium animalis subspecies lactis CUL34
Bifidobacterium bifidum CUL20
Lactobacillus salivarius CUL61
Lactobacillus paracasei CUL08		 1 × 1010 CFU/mL 9 Infants ↑ AD prevention Allen et al. 2014 [43]
Bifidobacterium lactis HN019
Lactobacillus acidophilus NCFM
Lactobacillus rhamnosus HN001
Lactobacillus paracasei LPC37		 1 × 1010 CFU/mL 9 Infants 10 ↓ SCORAD
↓ BSA
↓ FDLQI		 Lise et al. (1992) [22]
Bifidobacterium breve Bbi99
Lactobacillus rhamnosus GG
Lactobacillus rhamnosus LC705
Propionibacterium freudenreichii spp. shermanii JD		 2 × 108 CFU/mL
5 × 109 CFU/mL
5 × 109 CFU/mL
2 × 1010 CFU/mL 8		 Children 11 ↑ AD prevention Kuitunen et al. (2009) [44]
Bifidobacterium animalis subsp. lactis BB-12
Lactobacillus rhamnosus GG		 1 × 1010 CFU/mL Human adults 12 ↑ AD prevention Rautava et al. 2006 [45]
Bifidobacterium longum BL999
Lactobacillus rhamnosus LPR		 1 × 1010 CFU/mL Human adults 12 ↑ AD prevention Rautava et al. 2012 [46]
Bifidobacterium lactis BB-13
Lactobacillus rhamnosus GG		 1 × 1010 CFU/mL Human adults 12 ↑ AD prevention Huurre et al. (2008) [47]
Bifidobacterium lactis
Lactobacillus rhamnosus		 2 × 1010 CFU/g 6 Children 13 ↓ SCORAD Sistek et al. (2006) [48]
Bifidobacterium breve YIT 12272
Lactococcus lactis YIT 2027
Streptococcus thermophilus YIT 2021		 5–6 × 1010 CFU/100 mL 14 Human adults 12 ↑ Cathepsin L-like activity
↑ Hydration level
↓ Serum phenol
↓ Urine phenol		 Kano et al. (2013) [38]

1 Administration: 73 mL/kg daily for 7.3 months; 2 administration: once a day for 7 weeks; 3 administration: daily for 8 weeks; 4 six-week-old, female, and specific pathogen-free grade C57bl/6 mice; 5 ratio (1:2) twice a day for 12 weeks; 6 ratio (1:1:1) administered for 12 weeks; 7 topical treatment; 8 administration: twice daily 2–4 weeks; 9 total amount administered daily for two weeks; 10 female infants aged 18 months; 11 <5 years Double-lind randomized placebo controlled; 12 Double-blind randomized placebo controlled; 13 1–10 years of age; 14 administered daily for 4 weeks.

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