Dairy Lactic Acid Bacteria and Their Potential Function in Dietetics: The Food–Gut-Health Axis
Abstract
:1. Introduction
2. Definitions and Some Characteristics of LABs
3. Importance of LABs in Dairy Foods in Terms of Health
4. Involvement of Dairy LABs in the Modulation of Non-Communicable Diseases (NCDs)
4.1. Obesity
4.2. Cardiovascular Diseases
4.3. Diabetes Mellitus
4.4. Cancer
4.5. Inflammatory Bowel Diseases (IBD)
5. Conclusions
Author Contributions
Funding
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
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LAB | Family | Genus | Gram −/+ | Growth Conditions | Type of Lactic Acid | ||
---|---|---|---|---|---|---|---|
Heat-Stable (45 °C) | Salt-Tolerant (18% NaCl) | Acid-Resistant (pH 4.4) | |||||
Dairy | |||||||
Lactobacillaceae | Lactobacillus | + | Changeable | - | Changeable | D, L, DL | |
Pediococcus | + | Changeable | - | + | L, DL | ||
Streptococcaceae | Streptococcus | + | Changeable | - | - | L | |
Lactococcus | + | - | - | Changeable | L | ||
Propionibacteriaceae | Propionibacterium | + | - | - | - | ||
Enterococcaceae | Enterococcus | + | + | - | + | L | |
Leuconostocaecae | Leuconostoc | + | - | - | Changeable | D | |
Nondairy | |||||||
Aerococcaceae | Aerococcus | + | - | - | - | L | |
Carnobacteriaceae | Carnobacterium | + | - | - | NA | L | |
Enterococcaceae | Tetragenococcus | + | - | + | Changeable | L | |
Enterococcaceae | Vagococcus | + | - | - | NA | L | |
Fructobacillus | + | NA | - | NA | D | ||
Leuconostocaecae | Oenococcus | + | - | - | Changeable | D | |
Weissella | + | - | - | Changeable | D, L |
Dairy Products | Isolated Probiotic Strains | Their Bioactivities and Stability Issues | Reference(s) |
---|---|---|---|
Kalarei, a traditional fermented cheese product | Pediococcus acidilactici SMVDUDB2 | * An 80% survival rate at low pH (2.0 and 3.0) and high bile salt concentration (0.3 and 0.5%) * High hydrophobicity affinity (33.3%) with ethyl acetate * Autoaggregation (77.68 ± 0.68%) and coaggregation (73.57 ± 0.47%) with Staphylococcus aureus (MTCC 3160) * Antibacterial activity against Bacillus subtilis (MTCC 121), Mycobacterium smegmatis (MTCC 994), Staphylococcus aureus (MTCC 3160), Proteus vulgaris (MTCC 426), Escherichia coli (MTCC 1652), and Lactocaseibacillus rhamnosus (MTCC 1408) | [37] |
Ezine cheese (a Turkish cheese) | Enterococcus lactis PMD74 | * The strain showed autoaggregative (41%) and coaggregative properties along with high viability at acidic pH (3.0) and in the presence of pepsin, pancreatin, and bile salts (0.3% and 0.5%). * The strain PMD74 inhibited the growth of a number of Gram-positive bacteria (Listeria monocytogenes, Lactobacillus sake, Staphylococcus aureus, and Enterococcus faecalis). | [36] |
Tulum cheese (a Turkish cheese) | Seven Limosilactobacillus fermentum strains | * Limosilactobacillus fermentum LP3 and LP4 were able to tolerate acidic pH (2.5) and 1% bile salt. * Although all strains had similar enzymatic activity and antibiotic resistance patterns, the highest antagonistic effect belonged to LP3, LP4, and LP6 and the highest cholesterol assimilation belonged to LP3 and LP4, respectively. | [39] |
Probiotic yogurt | Lactobacillus acidophilus, Bifidobacterium bifidum, Lactiplantibacillus plantarum, Lacticaseibacillus casei | * A combination of Lactobacillus acidophilus and Bifidobacterium bifidum survived at pH 1.5 during an incubation period of 1.5 h and also showed good survivability at 0.3% bile salt concentration. * At pH 2.0, 3.0, and 4.0, the survivability rate for Lactobacillus acidophilus and Bifidobacterium bifidum was 54, 66, and 64%, respectively. | [40] |
Yogurt | Streptococcus thermophilus BGKMJ1-36 and Lactobacillus bulgaricus BGVLJ1-21 | * Both strains grew at 37 and 45 °C in GM17 broth, while they did not grow in GM17 broth with 2% NaCl. * Both strains showed antimicrobial activity toward Listeria monocytogenes, while the BGKMJ1-36 strain produced EPS. * The colonies of BGKMJ1-36 and BGVLJ1-21 strains that successfully survived transit of the yogurt via simulated gastrointestinal tract conditions have been examined for adhesion to intestinal epithelial Caco-2 cells. | [41] |
Iranian traditional yogurts | 12 LAB isolates from two genera (Pediococcus; 6 P. acidilacticii isolates and Lactobacillus; 2 Lactiplantibacillus plantarum, 2 Levilactobacillus brevis, 1 Limosilactobacillus fermentum and 1 Lactobacillus kefiri isolates). | * Limosilactobacillus fermentum 27 had the highest acid tolerance, while Levilactobacillus brevis 25 had the highest bile salt tolerance. * Pediococcus acidilactici 23 showed a lower acid tolerance as well as Levilactobacillus Brevis 86 exhibited a lower bile salt tolerance than others. | [35] |
Local dairy (cow milk, buffalo milk, cheese, and yogurt) | Lactobacillus alimentarius, Lactobacillus sake, and Lactobacillus collinoides | * The Lactobacillus strains inhibited pathogens’ growth. * All three isolates showed moderate activity apart from Lactobacillus collinoides and Lactobacillus alimentarius, which had relatively strong activity against Pseudomonas aeruginosa and Bacillus subtilis. | [42] |
30 dairy samples (household milk and curd) | 12 Lactobacillus isolates (LBS 1-LBS 12) | * Eight isolates (LBS 1-6, 8 and 11) were bile resistant (survival >50% at 0.3% bile salt w/v) and five isolates (LBS 1, 2, 5, 6 and 11) were resistant at acidic pH (survival >50% at pH 3). * All isolates inhibited the growth of Staphylococcus aureus. * LBS 2 also inhibited the growth of Escherichia coli and Salmonella typhimurium. * Isolate LBS 2 was resistant to five antibiotics as well as Lactocaseibacillus rhamnosus LBS2 successfully adhered to rat epithelial cells in in vitro conditions. | [43] |
Traditional Greek dairy products (Feta, Kasseri, Xynotyri, Graviera, Formaela, Galotyri, and Kefalotyri cheeses as well as yogurt and milk) | 25 LAB strains | * Only Streptococcus thermophilus ACA-DC 26 (Greek yogurt isolate) had antimicrobial activity (against Streptococcus mutans LMG 14558T). * Two Lactiplantibacillus plantarum strains (ACA-DC 2640 and ACA-DC 4039) showed the highest adhesion according to a collagen-based microplate assay and by using HΤ-29 and Caco-2 cells. * Milk cell-free supernatants of Lactiplantibacillus plantarum ACA-DC 2640 and ACA-DC 4039 showed strong angiotensin I-converting enzyme inhibition. * Lactiplantibacillus plantarum ACA-DC 2640, Streptococcus thermophilus ACA-DC 26, and ACA-DC 170 had anti-inflammatory activity. | [44] |
Tibetan kefir | Lactobacillus kefiranofaciens XL10 | * XL10 survived 3-h incubation at pH 3.5 and exhibited cell surface hydrophobicity of ~79.9% and autoaggregation of ~27.8%. * XL10 successfully adhered to the mucous tissue and colonized the ileum of the mice. * XL10 modulated gut microbiota by increasing the Bifidobacteriaceae family and decreasing in Proteobacteria phyla. | [45] |
Mongolian fermented koumiss | Lactobacillus helveticus NS8 | * Although NS8 exhibited a moderate survival ability in the gastrointestinal tract environment in vitro, an excellent adhesion ability to human intestinal cells and significant autoaggregation and cell-surface hydrophobicity were reported. * NS8 was able to decline the proinflammatory effects of lipopolysaccharide by inducing higher levels of IL-10. | [38] |
References | Health Effect | Study Design | Intervention | Intervention Duration | Dairy Product Type | Milk Heat Treatment | LAB Species | Main Results |
---|---|---|---|---|---|---|---|---|
ANIMAL MODELS, IN VITRO AND IN VIVO STUDIES | ||||||||
[58] | Cardiometabolic markers and intestinal microbiota | 8-weeks-old C57BL/6J wild-type (WT) and atherosclerotic (LRKO) male mice | HFD/high-sucrose diet [66% kcal lipids, 22% kcal carbohydrates (100% sucrose), 12% kcal proteins]. Protein sources groups: 1. 100% non-dairy protein (NDP) 2. 50% of the NDP energy replaced by milk protein (MP) 3. Lactobacillus helveticus fermented milk protein (FMP) 4. Greek-style yogurt protein (YP) | 12 weeks (WT mice) 24 weeks (LRKO mice) | Yogurt and fermented milk | 90 °C |
|
|
[121] | Dextran sulfate sodium-induced colitis and intestinal microbiota | 8-weeks-old specific-pathogen-free BALB/c female mice | 1. Interventional colitis group (DSS-YC group) was administered 200 μL/d per mouse of the YC mixture (~5 × 109 cfu) intragastrically. 2. The control colitis group (DSS group) received saline intragastrically as a vehicle. 3. Healthy control group received normal drinking water ad libitum (without DSS) | 8 days | Yogurt culture (YC) bacteria | Not applied |
|
|
[122] | Immunostimulatory effects |
| EPS and bacteria isolated from 3 yogurt varieties fermented with different starter cultures administered to mice at doses of 100 μg/mouse (EPS) and 109 cfu/mouse (bacteria) Yogurt types 1. Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1 and Streptococcus thermophilus OLS3059 (OLL1073R-1 yogurt) 2. Lactobacillus delbrueckii ssp. bulgaricus OLL1245 and Streptococcus thermophilus OLS3059 (yogurt A) 3. Lactobacillus delbrueckii ssp.bulgaricus OLL1256 and Streptococcus thermophilus OLS3295 (yogurt B). | 3 weeks | Yogurt | 90 °C |
|
|
[123] | Colon cancer | BALB/c mice |
| 6 months | Yogurt | Commercial yogurt process |
|
|
[124] | Hyperlipidemia and obesity | Swiss mice |
| 6 weeks | Yak yogurt- a Tibetan dairy product | Not reported |
|
|
[125] | Hypertension | Rabbit lung cultures | Whey proteins were fermented with 34 LAB and their ability to inhibit ACE activity was compared. | 48 h | Whey proteins | 37 °C |
|
|
[126] | Obesity, hyperlipidemia, and inflammation | 6-weeks-old specific- pathogen-free C57BL/6J mice |
| 8 weeks | Yogurt culture bacteria | Not reported |
|
|
[127] | Obesity and hyperlipidemia | 6-weeks-old male Sprague-Dawley rats |
| 8 weeks | Yogurt | 85 °C |
|
|
[128] | Breast cancer | 6-weeks-old female BALB/c mice |
| 50 days | Fermented milk | Sterilized |
|
|
[129] | Breast cancer | 7–8 weeks-old female BALB/c mice |
| 36 days | Fermented milk | Sterilized |
|
|
[130] | Breast cancer | 7–8 weeks-old female BALB/c mice |
| 60 days | Fermented milk | Sterilized |
|
|
[131] | Breast cancer | BALB/c mice |
| 28 days | Fermented milk | Sterilized |
|
|
[132] | ACE inhibitory activity and hypertension | -ACE inhibitory activity-in vitro |
| 28 days | Yogurt | 85 °C | Lactobacillus delbrueckii ssp. bulgaricus Lb1466, Streptococcus thermophilus St1342, Lactobacillus acidophilus L10, Lacticaseibacillus casei and Bifidobacterium lactis B94 |
|
[72] | Obesity and hyperlipidemia | 4-week-old male Sprague-Dawley (SD) rats |
| 4 weeks | Whey beverage | 70 °C |
|
|
[80] | Obesity and hyperlipidemia | 4-week-old male C57BL/6 mice |
| 6 weeks | Kefir culture | 25 °C |
|
|
[83] | Obesity | 4-week-old male C57BL/6J mice and 3T3-L1 preadipocyte cells |
| 4 weeks | Kefir grain | 30 °C | Kefir grain culture |
|
HUMAN STUDIES (RCTs) | ||||||||
[77] | Obesity | 210 Japanese adults with large visceral fat areas (80.2–187.8 cm2) 35–60 years | Fermented milk groups: Containing 107 cfu LG2055/g, 200 g FM/d Containing 106 cfu LG2055/g, 200 g FM/d Containing 0 cfu LG2055/g (control), 200 g FM/d | 12 weeks | Fermented milk | 40 °C |
|
|
[102] | T2DM | 100 obese prediabetic males (BMI ≥ 25), (1-h post-load plasma glucose (PG) levels ≥180 mg/dL) ears |
| 8 weeks | Fermented milk | Not reported | Lacticaseibacillus casei strain Shirota (LcS) |
|
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Ağagündüz, D.; Yılmaz, B.; Şahin, T.Ö.; Güneşliol, B.E.; Ayten, Ş.; Russo, P.; Spano, G.; Rocha, J.M.; Bartkiene, E.; Özogul, F. Dairy Lactic Acid Bacteria and Their Potential Function in Dietetics: The Food–Gut-Health Axis. Foods 2021, 10, 3099. https://doi.org/10.3390/foods10123099
Ağagündüz D, Yılmaz B, Şahin TÖ, Güneşliol BE, Ayten Ş, Russo P, Spano G, Rocha JM, Bartkiene E, Özogul F. Dairy Lactic Acid Bacteria and Their Potential Function in Dietetics: The Food–Gut-Health Axis. Foods. 2021; 10(12):3099. https://doi.org/10.3390/foods10123099
Chicago/Turabian StyleAğagündüz, Duygu, Birsen Yılmaz, Teslime Özge Şahin, Bartu Eren Güneşliol, Şerife Ayten, Pasquale Russo, Giuseppe Spano, João Miguel Rocha, Elena Bartkiene, and Fatih Özogul. 2021. "Dairy Lactic Acid Bacteria and Their Potential Function in Dietetics: The Food–Gut-Health Axis" Foods 10, no. 12: 3099. https://doi.org/10.3390/foods10123099
APA StyleAğagündüz, D., Yılmaz, B., Şahin, T. Ö., Güneşliol, B. E., Ayten, Ş., Russo, P., Spano, G., Rocha, J. M., Bartkiene, E., & Özogul, F. (2021). Dairy Lactic Acid Bacteria and Their Potential Function in Dietetics: The Food–Gut-Health Axis. Foods, 10(12), 3099. https://doi.org/10.3390/foods10123099