Functional Properties of Chlorella vulgaris, Colostrum, and Bifidobacteria, and Their Potential for Application in Functional Foods
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microorganisms
2.2. Colostrum
2.3. Immunomodulation Assay
2.4. Cytotoxic Effect
2.5. Prebiotic Assay
2.6. Animal Model and Study Design
2.7. Biochemical Analysis
2.8. Statistical Analysis
3. Results and Discussion
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Camacho, F.; Macedo, A.; Malcata, F. Potential Industrial Applications and Commercialization of Microalgae in the Functional Food and Feed Industries: A Short Review. Mar. Drugs 2019, 17, 312. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Safi, C.; Zebib, B.; Merah, O.; Pontalier, P.-Y.; Vaca-Garcia, C. Morphology, composition, production, processing and applications of Chlorella vulgaris: A review. Renew. Sustain. Energy Rev. 2014, 35, 265–278. [Google Scholar] [CrossRef] [Green Version]
- Lai, Y.-C.; Chang, C.-H.; Chen, C.-Y.; Chang, J.-S.; Ng, I.-S. Towards protein production and application by using Chlorella species as circular economy. Bioresour. Technol. 2019, 289, 121625. [Google Scholar] [CrossRef]
- Vigani, M.; Parisi, C.; Rodríguez-Cerezo, E.; Barbosa, M.J.; Sijtsma, L.; Ploeg, M.; Enzing, C. Food and feed products from micro-algae: Market opportunities and challenges for the EU. Trends Food Sci. Technol. 2015, 42, 81–92. [Google Scholar] [CrossRef]
- Shibata, S.; Oda, K.; Onodera-Masuoka, N.; Matsubara, S.; Kikuchi-Hayakawa, H.; Ishikawa, F.; Iwabuchi, A.; Sansawa, H. Hypocholesterolemic Effect of Indigestible Fraction of Chlorella regularis in Cholesterol-Fed Rats. J. Nutr. Sci. Vitaminol. 2001, 47, 373–377. [Google Scholar] [CrossRef] [PubMed]
- Niccolai, A.; Zittelli, G.C.; Rodolfi, L.; Biondi, N.; Tredici, M.R. Microalgae of interest as food source: Biochemical composition and digestibility. Algal Res. 2019, 42, 101617. [Google Scholar] [CrossRef]
- Gupta, C. Prebiotic Efficiency of Blue Green Algae on Probiotics Microorganisms. J. Microbiol. Exp. 2017, 4, 1–4. [Google Scholar] [CrossRef] [Green Version]
- Lee, H.S.; Park, H.J.; Kim, M.K. Effect of Chlorella vulgaris on lipid metabolism in Wistar rats fed high fat diet. Nutr. Res. Pr. 2008, 2, 204–210. [Google Scholar] [CrossRef]
- Torres-Tiji, Y.; Fields, F.J.; Mayfield, S.P. Microalgae as a future food source. Biotechnol. Adv. 2020, 41, 107536. [Google Scholar] [CrossRef]
- Cantú-Bernal, S.; Domínguez-Gámez, M.; Medina-Peraza, I.; Aros-Uzarraga, E.; Ontiveros, N.; Flores-Mendoza, L.; Gomez-Flores, R.; Tamez-Guerra, P.; González-Ochoa, G. Enhanced Viability and Anti-rotavirus Effect of Bifidobacterium longum and Lactobacillus plantarum in Combination With Chlorella sorokiniana in a Dairy Product. Front. Microbiol. 2020, 11, 875. [Google Scholar] [CrossRef]
- Sylwia, Ś.; Elżbieta, K. Algae Chlorella vulgaris as a factor conditioning the survival of Lactobacillus spp. in adverse environmental conditions. LWT 2020, 133, 109936. [Google Scholar] [CrossRef]
- FAO/WHO. Guidelines for the evaluation of probiotics in food. In Proceedings of the Joint FAO/WHO Working Group Report on Drafting Guide-Lines for the Evaluation of Probiotics in Food, London, ON, Canada, 30 April–1 May 2002. [Google Scholar]
- Rajoka, M.S.R.; Mehwish, H.M.; Siddiq, M.; Haobin, Z.; Zhu, J.; Yan, L.; Shao, D.; Xu, X.; Shi, J. Identification, characterization, and probiotic potential of Lactobacillus rhamnosus isolated from human milk. LWT 2017, 84, 271–280. [Google Scholar] [CrossRef]
- Boricha, A.A.; Shekh, S.L.; Pithva, S.P.; Ambalam, P.S.; Vyas, B.R.M. In vitro evaluation of probiotic properties of Lactobacillus species of food and human origin. LWT 2019, 106, 201–208. [Google Scholar] [CrossRef]
- Beheshtipour, H.; Mortazavian, A.M.; Haratian, P.; Khosravi-Darani, K. Effects of Chlorella vulgaris and Arthrospira platensis addition on viability of probiotic bacteria in yogurt and its biochemical properties. Eur. Food Res. Technol. 2012, 235, 719–728. [Google Scholar] [CrossRef]
- Ruiz, P.; Barragán, I.; Seseña, S.; Palop, M.L. Functional properties and safety assessment of lactic acid bacteria isolated from goat colostrum for application in food fermentations. Int. J. Dairy Technol. 2016, 69, 559–568. [Google Scholar] [CrossRef]
- Silva, E.G.D.S.O.; Rangel, A.H.D.N.; Mürmam, L.; Bezerra, M.D.F.; De Oliveira, J.P.F. Bovine colostrum: Benefits of its use in human food. Food Sci. Technol. 2019, 39, 355–362. [Google Scholar] [CrossRef] [Green Version]
- Urakami, H.; Saeki, M.; Watanabe, Y.; Kawamura, R.; Nishizawa, S.; Suzuki, Y.; Watanabe, A.; Ajisaka, K. Isolation and assessment of acidic and neutral oligosaccharides from goat milk and bovine colostrum for use as ingredients of infant formulae. Int. Dairy J. 2018, 83, 1–9. [Google Scholar] [CrossRef]
- Bagwe, S.; Tharappel, L.J.; Kaur, G.; Buttar, H.S. Bovine colostrum: An emerging nutraceutical. J. Complement. Integr. Med. 2015, 12, 175–185. [Google Scholar] [CrossRef]
- Hyrslova, I.; Krausova, G.; Bartova, J.; Kolesar, L.; Curda, L. Goat and Bovine Colostrum as a Basis for New Probiotic Functional Foods and Dietary Supplements. J. Microb. Biochem. Technol. 2016, 8, 56–59. [Google Scholar] [CrossRef] [Green Version]
- Hyrslova, I.; Krausova, G.; Michlova, T.; Kana, A.; Curda, L. Fermentation Ability of Bovine Colostrum by Different Probiotic Strains. Fermentation 2020, 6, 93. [Google Scholar] [CrossRef]
- Palacios, T.; Coulson, S.; Butt, H.; Vitetta, L. The gastrointestinal microbiota and multi-strain probiotic therapy: In children and adolescent obesity. Adv. Integr. Med. 2014, 1, 2–8. [Google Scholar] [CrossRef]
- Vlachová, M.; Heczková, M.; Jirsa, M.; Poledne, R.; Kovar, J. The Response of Hepatic Transcriptome to Dietary Cholesterol in Prague Hereditary Hypercholesterolemic (PHHC) Rat. Physiol. Res. 2014, 63, S429–S437. [Google Scholar] [CrossRef]
- Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65, 55–63. [Google Scholar] [CrossRef]
- Caleffi-Marchesini, E.; Krausová, G.; Hyršlová, I.; Paredes, L.L.R.; dos Santos, M.M.; Sassaki, G.L.; Gonçalves, R.A.C.; de Oliveira, A.J.B. Isolation and prebiotic activity of inulin-type fructan extracted from Pfaffia glomerata (Spreng) Pedersen roots. Int. J. Biol. Macromol. 2015, 80, 392–399. [Google Scholar] [CrossRef] [Green Version]
- Gazi, I.; Tsimihodimos, V.; Filippatos, T.; Bairaktari, E.; Tselepis, A.D.; Elisaf, M. Concentration and relative distribution of low-density lipoprotein subfractions in patients with metabolic syndrome defined according to the National Cholesterol Education Program criteria. Metabol 2006, 55, 885–891. [Google Scholar] [CrossRef] [PubMed]
- Raposo, M.F.D.J.; De Morais, A.M.B.; De Morais, R.M.S.C. Marine Polysaccharides from Algae with Potential Biomedical Applications. Mar. Drugs 2015, 13, 2967–3028. [Google Scholar] [CrossRef]
- Ścieszka, S.; Klewicka, E. Influence of the Microalga Chlorella vulgaris on the Growth and Metabolic Activity of Lactobacillus spp. Bacteria. Foods 2020, 9, 959. [Google Scholar] [CrossRef]
- Lordan, S.; Ross, R.P.; Stanton, C. Marine Bioactives as Functional Food Ingredients: Potential to Reduce the Incidence of Chronic Diseases. Mar. Drugs 2011, 9, 1056–1100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suárez, E.R.; Kralovec, J.A.; Noseda, M.D.; Ewart, H.S.; Barrow, C.J.; Lumsden, M.D.; Grindley, T.B. Isolation, characterization and structural determination of a unique type of arabinogalactan from an immunostimulatory extract of Chlorella pyrenoidosa. Carbohydr. Res. 2005, 340, 1489–1498. [Google Scholar] [CrossRef] [PubMed]
- Ewart, H.S.; Bloch, O.; Girouard, G.S.; Kralovec, J.; Barrow, C.J.; Ben-Yehudah, G.; Suárez, E.R.; Rapoport, M.J. Stimulation of cytokine production in human peripheral blood mononuclear cells by an aqueous Chlorella extract. Planta Med. 2007, 73, 762–768. [Google Scholar] [CrossRef] [Green Version]
- An, H.J.; Rim, H.K.; Lee, J.H.; Seo, M.J.; Hong, J.W.; Kim, N.H.; Kim, H.M. Effect of Chlorella Vulgaris on Im-Mune-Enhancement and Cytokine Production In Vivo and In Vitro. Food Sci. Biotechnol. 2008, 17, 953–958. [Google Scholar]
- Sibi, G.; Rabina, S. Inhibition of Pro-inflammatory mediators and cytokines by Chlorella Vulgaris extracts. Pharmacogn. Res. 2016, 8, 118. [Google Scholar] [CrossRef] [Green Version]
- Taylor, P.; Colman, L.; Bajoon, J. The search for plants with anticancer activity: Pitfalls at the early stages. J. Ethnopharmacol. 2014, 158, 246–254. [Google Scholar] [CrossRef] [PubMed]
- Houdkova, M.; Albarico, G.; Doskocil, I.; Tauchen, J.; Urbanova, K.; Tulin, E.E.; Kokoska, L. Vapors of Volatile Plant-Derived Products Significantly Affect the Results of Antimicrobial, Antioxidative and Cytotoxicity Microplate-Based Assays. Molecules 2020, 25, 6004. [Google Scholar] [CrossRef]
- Houdkova, M.; Urbanova, K.; Doskocil, I.; Soon, J.W.; Foliga, T.; Novy, P.; Kokoska, L. Anti-staphylococcal activity, cytotoxicity, and chemical composition of hexane extracts from arils and seeds of two Samoan Myristica spp. South. Afr. J. Bot. 2021, 139, 1–5. [Google Scholar] [CrossRef]
- Tauchen, J.; Doskocil, I.; Caffi, C.; Lulekal, E.; Marsik, P.; Havlik, J.; Van Damme, P.; Kokoska, L. In vitro antioxidant and anti-proliferative activity of Ethiopian medicinal plant extracts. Ind. Crop. Prod. 2015, 74, 671–679. [Google Scholar] [CrossRef]
- Zhang, J.; Liu, L.; Chen, F. Production and characterization of exopolysaccharides from Chlorella zofingiensis and Chlorella vulgaris with anti-colorectal cancer activity. Int. J. Biol. Macromol. 2019, 134, 976–983. [Google Scholar] [CrossRef]
- Gómez-Zorita, S.; González-Arceo, M.; Trepiana, J.; Eseberri, I.; Fernández-Quintela, A.; Milton-Laskibar, I.; Aguirre, L.; González, M.; Portillo, M.P. Anti-Obesity Effects of Macroalgae. Nutrients 2020, 12, 2378. [Google Scholar] [CrossRef]
- Panahi, Y.; Darvishi, B.; Jowzi, N.; Beiraghdar, F.; Sahebkar, A. Chlorella vulgaris: A multifunctional dietary supplement with diverse medicinal properties. Curr. Pharm. Des. 2016, 22, 164–173. [Google Scholar] [CrossRef] [PubMed]
- Shibata, S.; Hayakawa, K.; Egashira, Y.; Sanada, H. Hypocholesterolemic mechanism of Chlorella: Chlorella and its indigestible fraction enhance hepatic cholesterol catabolism through up-regulation of cholesterol 7alpha-hydroxylase in rats. Biosci. Biotechnol. Biochem. 2007, 71, 916–925. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chovančíková, M.; Šimek, V. Effects of high-fat and Chlorella vulgaris feeding on changes in lipid metabolism in mice. Biol. Bratisl. 2001, 56, 661–666. [Google Scholar]
- Ryu, N.H.; Lim, Y.; Park, J.E.; Kim, J.; Kim, J.Y.; Kwon, S.W.; Kwon, O. Impact of daily Chlorella consumption on serum lipid and carotenoid profiles in mildly hypercholesterolemic adults: A double-blinded, randomized, placebo-controlled study. Nutr. J. 2014, 13, 57. [Google Scholar] [CrossRef] [Green Version]
- Sansawa, H.; Takahashi, M.; Tsuchikura, S.; Endo, H. Effect of chlorella and its fractions on blood pressure, cerebral stroke lesions, and life-span in stroke-prone spontaneously hypertensive rats. J. Nutr. Sci. Vitaminol. 2006, 52, 457–466. [Google Scholar] [CrossRef] [Green Version]
- Cherng, J.-Y.; Shih, M.-F. Improving glycogenesis in Streptozocin (STZ) diabetic mice after administration of green algae Chlorella. Life Sci. 2006, 78, 1181–1186. [Google Scholar] [CrossRef] [PubMed]
- Ishimwe, N.; Daliri, E.B.; Lee, B.H.; Fang, F.; Du, G. The perspective on cholesterol-lowering mechanisms of probiotics. Mol. Nutr. Food Res. 2015, 59, 94–105. [Google Scholar] [CrossRef]
- Pavlović, N.; Stankov, K.; Mikov, M. Probiotics—Interactions with Bile Acids and Impact on Cholesterol Metabolism. Appl. Biochem. Biotechnol. 2012, 168, 1880–1895. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Jung, W.S.; Choi, N.-J.; Kim, D.-O.; Shin, D.-H.; Kim, Y.J. Health-promoting effects of bovine colostrum in Type 2 diabetic patients can reduce blood glucose, cholesterol, triglyceride and ketones. J. Nutr. Biochem. 2009, 20, 298–303. [Google Scholar] [CrossRef] [PubMed]
Tested Strains | Concentration of Acids (mg/L)/pH | Control (WCH Broth) | BS + Chlorella 1% (w/v) | BS + Chlorella 3% (w/v) |
---|---|---|---|---|
CCDM 93 | Lactic acid | 218 ± 10 A | 862 ± 40 B | 1422 ± 70 C |
Acetic acid | 1388 ± 70 A | 1526 ± 20 B | 1953 ± 100 C | |
pH | 4.47 ± 0.03 A | 4.80 ± 0.03 C | 4.64 ± 0.03 B | |
BB-12 | Lactic acid | 170 ± 10 A | 865 ± 40 B | 1455 ± 70 C |
Acetic acid | 1349 ± 65 A | 1522 ± 80 B | 2007 ± 100 C | |
pH | 4.47 ± 0.03 A | 4.80 ± 0.00 C | 4.65 ± 0.00 B | |
CCDM 486 | Lactic acid | 158 ± 10 A | 208 ± 10 B | 753 ± 35 C |
Acetic acid | 1268 ± 60 B | 606 ± 30 A | 1271 ± 65 B | |
pH | 4.57 ± 0.01 B | 5.37 ± 0.01 C | 4.44 ± 0.00 A | |
CCDM 562 | Lactic acid | 378 ± 20 A | 908 ± 45 B | 1507 ± 75 C |
Acetic acid | 1514 ± 75 A | 1720 ± 85 B | 2120 ± 105 C | |
pH | 4.39 ± 0.03 A | 4.71 ± 0.00 C | 4.60 ± 0.00 B |
Cytokine Levels (pg/mL) | |||||
---|---|---|---|---|---|
Chlorella Concentration | TNF-α | IL-17 | IL-6 | IL-4 | IFN-γ |
1% (w/v) | 15.4 ± 9.1 B | 0.7 ± 0.3 A | 143.6 ± 96.8 B | 2.7 ± 0.0 A | 0.7 ± 0.3 A |
3% (w/v) | 1.3 ± 0.7 A | 0.9 ± 1.0 A | 37.9 ± 11.8 A | 3.2 ± 0.4 B | 1.0 ± 0.5 A |
0% (Control) | 0.0 ± 0.7 A | 2.0 ± 0.0 B | 7.3 ± 2.9 A | 4.9 ± 1.3 B | 3.5 ± 1.1 B |
Tested Parameters | Times | Group of Rats | |||
---|---|---|---|---|---|
GI (control) | GII | GIII | GIV | ||
TAG aorta (μmol/g) | week 4 | 0.5 ± 0.1 A | 0.9 ± 0.3 AB | 1.1 ± 0.0 B | 1.3 ± 0.2 B |
week 8 | 1.4 ± 0.2 AB | 1.6 ± 0.4 B | 1.6 ± 0.4 B | 0.9 ± 0.3 A | |
TAG serum (mmol/L) | week 4 | 2.9 ± 0.8 AB | 2.6 ± 0.5 A | 3.9 ± 0.6 B | 2.5 ± 0.5 A |
week 8 | 2.3 ± 0.6 B | 2.1 ± 0.2 B | 1.6 ± 0.5 A | 1.6 ± 0.4 A |
Tested Parameters | Time | Group of Rats | |||
---|---|---|---|---|---|
GI (control) | GII | GIII | GIV | ||
VLDL (mg/dL) | week 4 | 88.0 ± 16.8 A | 130.5 ± 22.5 B | 142.0 ± 27.1 B | 118.0 ± 23.4 AB |
week 8 | 153.0 ± 59.8 A | 163.5 ± 21.2 A | 95.0 ± 86.9 A | 91.0 ± 37.3 B | |
IDL-C (mg/dL) | week 4 | 63.0 ± 9.4 AB | 77.5 ± 25.9 A | 49.0 ± 5.2 BC | 43.0 ± 12.3 C |
week 8 | 89.0 ± 22.4 AB | 65.0 ± 15.1 A | 122.0 ± 30.4 B | 160.0 ± 33.7 B | |
IDL-B (mg/dL) | week 4 | 27.0 ± 4.8 A | 50.5 ± 10.4 B | 24.0 ± 5.9 C | 19.0 ± 7.5 C |
week 8 | 35.0 ± 19.9 A | 35.0 ± 11.2 A | 73.0 ± 10.3 B | 78.0 ± 21.4 B | |
IDL-A (mg/dL) | week 4 | 5.0 ± 1.2 A | 12.0 ± 2.5 B | 6.0 ± 1.8 A | 3.0 ± 3.3 A |
week 8 | 13.0 ± 6.05 A | 10.5 ± 3.20 A | 23.0 ± 4.31 B | 29.0 ± 5.54 B | |
HDL (mg/dL) | week 4 | 51.0 ± 6.4 A | 68.0 ± 13.2 B | 67.0 ± 10.9 AB | 78.5 ± 19.1 B |
week 8 | 73.0 ± 12.7 A | 81.5 ± 8.4 AB | 71.0 ± 11.3 A | 92.0 ± 10.6 B |
Tested Parameters | Time | Groups of Rats | |||
---|---|---|---|---|---|
GI (control) | GII | GIII | GIV | ||
Total LDL (mg/dL) | week 4 | 109.0 ± 20.0 A | 140.5 ± 32.0 B | 88.0 ± 15.2 A | 78.5 ± 20.0 A |
week 8 | 182.0 ± 58.1 A | 119.5 ± 28.8 A | 249.0 ± 33.0 B | 303.0 ± 54.6 B | |
TC (mg/dL) | week 4 | 341.0 ± 20.0 AB | 381.0 ± 47.1 A | 295.2 ± 73.0 B | 329.8 ± 27.9 AB |
week 8 | 413.4 ± 106.1 AB | 388.4 ± 32.3 A | 473.9 ± 111.3 B | 500.8 ± 50.9 B | |
ALT (µkat/L) | week 4 | 1.66 ± 0.1 AB | 1.77 ± 0.2 A | 1.73 ± 0.1 A | 1.53 ± 0.1 B |
week 8 | 1.90 ± 0.3 A | 1.65 ± 0.2 AB | 1.48 ± 0.2 B | 1.39 ± 0.2 B | |
AST (µkat/L) | week 4 | 3.88 ± 0.2 A | 4.36 ± 0.5 A | 4.33 ± 0.4 A | 4.14 ± 0.5 A |
week 8 | 4.15 ± 0.4 A | 4.02 ± 0.9 AB | 4.00 ± 0.8 AB | 3.30 ± 0.7 B |
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Hyrslova, I.; Krausova, G.; Smolova, J.; Stankova, B.; Branyik, T.; Malinska, H.; Huttl, M.; Kana, A.; Curda, L.; Doskocil, I. Functional Properties of Chlorella vulgaris, Colostrum, and Bifidobacteria, and Their Potential for Application in Functional Foods. Appl. Sci. 2021, 11, 5264. https://doi.org/10.3390/app11115264
Hyrslova I, Krausova G, Smolova J, Stankova B, Branyik T, Malinska H, Huttl M, Kana A, Curda L, Doskocil I. Functional Properties of Chlorella vulgaris, Colostrum, and Bifidobacteria, and Their Potential for Application in Functional Foods. Applied Sciences. 2021; 11(11):5264. https://doi.org/10.3390/app11115264
Chicago/Turabian StyleHyrslova, Ivana, Gabriela Krausova, Jana Smolova, Barbora Stankova, Tomas Branyik, Hana Malinska, Martina Huttl, Antonin Kana, Ladislav Curda, and Ivo Doskocil. 2021. "Functional Properties of Chlorella vulgaris, Colostrum, and Bifidobacteria, and Their Potential for Application in Functional Foods" Applied Sciences 11, no. 11: 5264. https://doi.org/10.3390/app11115264