FNS  Vol.12 No.7 , July 2021
Effect of Flaxseed on Bile Tolerances of Lactobacillus acidophilus, Lactobacillus bulgaricus, and Streptococcus thermophilus
Abstract: Consumption of flaxseed provides health benefits. Bile tolerance allows survival of probiotics in the intestinal tract. The objective was to determine whether or not flaxseed enhances bile tolerance of Lactobacillus acidophilus (L. acidophilus) LA-K, Lactobacillus delbruekii ssp. bulgaricus (L. bulgaricus) LB-12, and Streptococcus salivarius ssp. thermophilus (S. thermophilus) ST-M5. Control and experimental (62 g flaxseed/L) broths containing 0.3% oxgall were prepared for each culture, sterilized, cooled, inoculated, and plated for 8 h. Growth of each microorganism in both the control and experimental broths was evaluated by the slope of the regression line of its log count versus time after inoculation. Flaxseed significantly enhanced growth of L. acidophilus but not L. bulgaricus and S. thermophilus over 8 h compared to its corresponding control. Therefore, flaxseed improved the bile tolerance of L. acidophilus but not of S. thermophilus and L. bulgaricus.
Cite this paper: Theegala, M. , Arévalo, R. , Viana, V. , Olson, D. and Aryana, K. (2021) Effect of Flaxseed on Bile Tolerances of Lactobacillus acidophilus, Lactobacillus bulgaricus, and Streptococcus thermophilus. Food and Nutrition Sciences, 12, 670-680. doi: 10.4236/fns.2021.127050.

[1]   Berglund, D.R. (2002) Flax: New Uses and Demands. In: Janick, J. and Whipkey, A., Eds., Trends in New Crops and New Uses, ASHS Press, Alexandria, 358-360.

[2]   Herchi, W., Arráez-Román, D., Boukhchina, S., Kallel, H., Segura-Carretero, A. and Fernández-Gutierrez, A. (2012) A Review of the Methods Used in the Determination of Flaxseed Components. African Journal of Biotechnology, 11, 724-731.

[3]   Tavarini, S., De Leo, M., Matteo, R., Lazzeri, L., Braca, A. and Angelini, A. (2021) Flaxseed and Camelina Meals as Potential Sources of Health-Beneficial Compounds. Plants, 10, 156.

[4]   Zhang, W., Wang, X.B., Liu, Y., Tian, H.M., Flickinger, B., Empie, M.W. and Sun, S.Z. (2008) Dietary Flaxseed Lignan Extract Lowers Plasma Cholesterol and Glucose Concentrations in Hypercholesterolaemic Subjects. British Journal of Nutrition, 99, 1301-1309.

[5]   Johnsson, P., Kamal-Eldin, A., Lundgren, L.N. and Åman, P. (2000) HPLC Method for Analysis of Secoisolariciresinol Diglucoside in Flaxseeds. Journal of Agricultural and Food Chemistry, 48, 5216-5219.

[6]   Westcott, N.D. and Muir, A.D. (1998) Process for Extracting Lignans from Flaxseed. Agriculture and Agri-Food Canada, Assignee. US Patent Number 5,705,618.

[7]   Dixon, R.A. (2004) Phytoestrogens. Annual Review of Plant Biology, 55, 225-261.

[8]   Cunnane, S.C., Ganguli, S., Menard, C., Liede, A.C., Hamadeh, M.J., Chen, Z.-Y., Wolever, T.M.S. and Jenkins, D.J.A. (1993) High-Linolenic Acid Flaxseed (Linum usitatissimum): Some Nutritional Properties in Humans. British Journal of Nutrition, 69, 443-453.

[9]   Pan, A., Sun, J., Chen, Y., Ye, X., Li, H., Yu, Z., Wang, Y., Gu, W., Zhang, X., Chen, X., Demark-Wahnefried, W., Liu, Y. and Lin, X. (2007) Effects of a Flaxseed-Derived Lignan Supplement in Type 2 Diabetic Patients: A Randomized, Double-Blind, Cross-Over Trial. PLoS ONE, 2, e1148.

[10]   Yari, Z., Cheraghpour, M. and Hekmatdoost, A. (2021a) Flaxseed and/or Hesperidin Supplementation in Metabolic Syndrome: An Open-Labeled Randomized Controlled Trial. European Journal of Nutrition, 60, 287-298.

[11]   Yari, Z., Cheraghpour, M., Alavian, S.M., Hedayati, M., Eini-Zinab, H. and Hekmatdoost, A. (2021b) The Efficacy of Flaxseed and Hesperidin on Non-Alcoholic Fatty Liver Disease: An Open-Labeled Randomized Controlled Trial. European Journal of Clinical Nutrition, 75, 99-111.

[12]   Almehmadi, A., Lightowler, H., Chohan, M. and Clegg, M.E. (2021) The Effect of a Split Portion of Flaxseed on 24-h Blood Glucose Response. European Journal of Nutrition, 60, 1363-1373.

[13]   El Seedy, G.M., El-Shafey, E.S. and Elsherbiny, E.S. (2021) Fortification of Biscuit with Sidr Leaf and Flaxseed Mitigates Immunosuppression and Nephrotoxicity Induced by Cyclosporine A. Journal of Food Biochemistry, 45, e13655.

[14]   Lilly, D.M. and Stillwell, R.H. (1965) Probiotics: Growth-Promoting Factors Produced by Microorganisms. Science, 147, 747-748.

[15]   FAO/WHO (2002) Guidelines for the Evaluation of Probiotics in Food.

[16]   Aryana, K.J. and Olson, D.W. (2017) A 100-Year Review: Yogurt and Other Cultured Dairy Products. Journal of Dairy Science, 100, 9987-10013.

[17]   Uriot, O., Denis, S., Junjua, M., Roussel, Y., Dary-Mourot, A. and Blanquet-Diot, S. (2017) Streptococcus thermophilus: from Yogurt Starter to a New Promising Probiotic Candidate? Journal of Functional Foods, 37, 74-89.

[18]   Wadhai, V.S. and Dhawas, V.K. (2011) Characterization and Study of Lactobacillus bulgaricus as Probiotic Bacteria. Online International Interdisciplinary Research Journal, 1, 55-60.

[19]   Mater, D.D.G., Bretigny, L., Firmesse, O., Flores, M.-J., Mogenet, A., Bresson, J.-L. and Corthier, G. (2005) Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus Survive Gastrointestinal Transit of Healthy Volunteers Consuming Yogurt. FEMS Microbiology Letters, 250, 185-187.

[20]   Elli, M., Callegari, M.L., Ferrari, S., Bessi, E., Cattivelli, D., Soldi, S., Morelli, L., Feuillerat, N.G. and Antoine, J.-M. (2006) Survival of Yogurt Bacteria in the Human Gut. Applied and Environmental Microbiology, 72, 5113-5117.

[21]   Fijan, S. (2014) Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature. International Journal of Environmental Research and Public Health, 11, 4745-4767.

[22]   Sherman, J.M. (1937) The Streptococci. Bacteriological Reviews, 1, 3-97.

[23]   Wheater, D. (1955) The Characteristics of Lactobacillus acidophilus and Lactobacillus bulgaricus, Journal of General Microbiology, 12, 123-132.

[24]   Lankaputhra, W.E.V. and Shah, N.P. (1995) Survival of Lactobacillus acidophilus and Bifidobacterium spp in the Presence of Acid and Bile Salts. Cultured Dairy Products Journal, 30, 2-7.

[25]   Ayyash, M.M., Abdalla, A.K., AlKalbani, N.S., Baig, M.A., Turner, M.S., Liu, S.-Q. and Shah, N.P. (2021) Invited Review: Characterization of New Probiotics from Dairy and Nondairy Products-Insights into Acid Tolerance, Bile Metabolism and Tolerance, and Adhesion Capability. Journal of Dairy Science. (In Press)

[26]   Mihoubi, M., Amellal-Chibane, H., Mekimene, L., Noui, Y. and Halladj, F. (2017) Physicochemical, Microbial, and Sensory Properties of Yogurt Supplemented with Flaxseeds during Fermentation and Refrigerated Storage. Mediterranean Journal of Nutrition and Metabolism, 10, 211-221.

[27]   Mousavi, M., Heshmati, A., Garmakhany, A.D., Vahidinia, A. and Taheri, M. (2019) Optimization of the Viability of Lactobacillus acidophilus and Physico-Chemical, Textural and Sensorial Characteristics of Flaxseed-Enriched Stirred Probiotic Yogurt by Using Response Surface Methodology. LWT-Food Science and Technology, 102, 80-88.

[28]   Pereira, D.I.A. and Gibson, G.R. (2002) Cholesterol Assimilation by Lactic Acid Bacteria and Bifidobacteria Isolated from the Human Gut. Applied and Environmental Microbiology, 68, 4689-4693.

[29]   de Man, J.C., Rogosa, M. and Sharpe, M.E. (1960) A Medium for the Cultivation of Lactobacilli. Journal of Applied Bacteriology, 23, 130-135.

[30]   Terzaghi, B.E. and Sandine, W.E. (1975) Improved Medium for Lactic Streptococci and Their Bacteriophages. Applied Microbiology, 29, 807-813.

[31]   Vargas, L.A., Olson, D.W. and Aryana, K.J. (2015) Whey Protein Isolate Improves Acid and Bile Tolerances of Streptococcus thermophilus ST-M5 and Lactobacillus delbrueckii ssp. bulgaricus LB-12. Journal of Dairy Science, 98, 2215-2221.

[32]   Mena, B. and Aryana, K. (2018) Lactose Enhances Bile Tolerance of Yogurt Culture Bacteria. Journal of Dairy Science, 101, 1957-1959.

[33]   Iltar, R., Asci, A. and Kücükcetin, A. (2012) Viability and in Vitro Properties of Lactobacillus acidophilus Used in Yoghurt as Influenced by Inulin Addition. Milchwissenschaft, 67, 142-146.

[34]   Shi, L.-E., Li, Z.-H., Li, D.-T., Xu, M., Chen, H.-Y., Zhang, Z.-L. and Tang, Z.-X. (2013) Encapsulation of Probiotic Lactobacillus bulgaricus in Alginate-Milk Microspheres and Evaluation of the Survival in Simulated Gastrointestinal Conditions. Journal of Food Engineering, 117, 99-104.

[35]   Muramalla, T. and Aryana, K.J. (2011) Some Low Homogenization Pressures Improve Certain Probiotic Characteristics of Yogurt Culture Bacteria and L. acidophilus LA-K. Journal of Dairy Science, 94, 3725-3738.

[36]   Bialasová, K., Němečková, I., Kyselka, J., Štětina, J., Solichová, K. and Horáčková, S. (2018) Influence of Flaxseed Components on Fermented Dairy Product Properties. Czech Journal of Food Sciences, 36, 51-56.

[37]   Smolová, J., Němečková, I., Klimešová, M., Švandrlík, Z., Bjelková, M., Filip, V. and Kyselka, J. (2017) Flaxseed Varieties: Composition and Influence on the Growth of Probiotic Microorganisms in Milk. Czech Journal of Food Sciences, 35, 18-23.

[38]   Bustamante, M., Villarroel, M., Rubilar, M. and Shene, C. (2015) Lactobacillus acidophilus La-05 Encapsulated by Spray Drying: Effect of Mucilage and Protein from Flaxseed (Linum usitatissimum L.). LWT-Food Science and Technology, 62, 1162-1168.