Comparative Analysis of Lactulose and Fructooligosaccharide on Growth Kinetics, Fermentation, and Antioxidant Activity of Common Probiotics — Oak Academic Publishing
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Comparative Analysis of Lactulose and Fructooligosaccharide on Growth Kinetics, Fermentation, and Antioxidant Activity of Common Probiotics
Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA, USA
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Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA, USA
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Animal Science Department, California Polytechnic State University, San Luis Obispo, CA, USA
1 Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA, USA
2 Biological Sciences Department, California Polytechnic State University, San Luis Obispo, CA, USA
3 Animal Science Department, California Polytechnic State University, San Luis Obispo, CA, USA
Prebiotics are non-digestible oligosaccharides that selectively stimulate the growth of beneficial bacteria in the human gut. Fructooligosaccharide (FOS) is a common prebiotic found in food products and infant formula. Lactulose is primarily used as a pharmaceutical ingredient but also shows potential prebiotic activities. Our objectives were to determine and compare the effects of FOS and lactulose on: 1) growth kinetics of common probiotics in aerobic condition; 2) pH and titratable acidity after fermentation; and 3) antioxidant capacity of the probiotics. Ten probiotic and two non-probiotic strains, representing genera Lactobacillus , Bifidobacterium , Bacillus , and Escherichia were assembled. Media used for prebiotics experiment were modified to contain 2% FOS or lactulose as the sole or main carbohydrate source. All experiments were done in triplicate. In aerobic condition, most strains cultured with FOS or lactulose did not grow optimally compared to dextrose (a non-prebiotic), while all four Bifidobacterium spp. showed little growth regardless of the carbohydrate source. In anaerobic condition, lactulose and FOS fermentation of Bifidobacterium spp. yielded similar pH ( p = 0.2723), but percent lactic acid, as determined by titratable acidity, was higher after lactulose fermentation ( p = 0.0004). The non-probiotic strains were able to utilize both FOS and lactulose, but displayed weaker acid production and higher pH (p Bifidobacterium spp. ( p = 0.0002) and Lactobacillus spp. ( p = 0.0447), but not probiotic E. coli and Bacillus spp. ( p = 0.2599) or non-probiotics ( p = 0.8816). In conclusion, lactulose supported growth activities of probiotics to a similar extent as FOS. Lactulose also stimulated higher acid production for Bifidobacterium spp. than FOS in anaerobic condition, thus it might be considered for incorporation into functional food products containing bifidobacteria.
Ley, R.E., Hamady, M., Lozupone, C., Turnbaugh, P.J., Ramey, R.R., Bircher, J.S., Schlegel, M.L., Tucker, T.A., Schrenzel, M.D. and Knight, R. (2008) Evolution of Mammals and Their Gut Microbes. Science, 320, 1647-1651. https://doi.org/10.1126/science.1155725
Ishibashi, N., Yaeshima, T. and Hayasawa, H. (1997) Bifidobacteria: Their Significance in Human Intestinal Health. Malaysian Journal of Nutrition, 3, 149-159.
Maynard, C.L., Elson, C.O., Hatton, R.D. and Weaver, C.T. (2012) Reciprocal Interactions of the Intestinal Microbiota and Immune System. Nature, 489, 231-241. https://doi.org/10.1038/nature11551
Gibson, G.R., Scott, K.P., Rastall, R.A., Tuohy, K.M., Hotchkiss, A., Dubert-Ferrandon, A., Gareau, M., Murphy, E.F., Saulnier, D., Loh, G. and Macfarlane, S. (2010) Dietary Prebiotics: Current Status and New Definition. Food Science and Technology Bulletin: Functional Foods, 7, 1-19. https://doi.org/10.1616/1476-2137.15880
Jeurink, P.V., van Esch, B.C., Rijnierse, A., Garssen, J. and Knippels, L.M. (2013) Mechanisms Underlying Immune Effects of Dietary Oligosaccharides. The American Journal of Clinical Nutrition, 98, 572S-577S. https://doi.org/10.3945/ajcn.112.038596
Spiegel, J.E., Rose, R., Karabell, P., Frankos, V.H. and Schmitt, D.F. (1994) Safety and Benefits of Fructooligosaccharides as Food Ingredients. Food Technology, 48, 85-89.
Kato, K., Mizuno, S., Umesaki, Y., Ishii, Y., Sugitani, M., Imaoka, A., Otsuka, M., Hasunuma, O., Kurihara, R., Iwasaki, A. and Arakawa, Y. (2004) Randomized Placebo-Controlled Trial Assessing the Effect of Bifidobacteria-Fermented Milk on Active Ulcerative Colitis. Alimentary Pharmacology & Therapeutics, 20, 1133-1141. https://doi.org/10.1111/j.1365-2036.2004.02268.x
Ulluwishewa, D., Anderson, R.C., McNabb, W.C., Moughan, P.J., Wells, J.M. and Roy, N.C. (2011) Regulation of Tight Junction Permeability by Intestinal Bacteria and Dietary Components. The Journal of Nutrition, 141, 769-776. https://doi.org/10.3945/jn.110.135657
Zhang, F., Yung, K.K.L., Chung, S.S.M. and Yeung, C.K. (2017) Supplementation of Fructooligosaccharide Mildly Improves the Iron Status of Anemic Rats Fed a Low-Iron Diet. Food and Nutrition Sciences, 8, 294-304. https://doi.org/10.4236/fns.2017.82019
Ito, M., Sawada, H., Ohishi, K., Yoshida, Y., Yokoi, W., Watanabe, T. and Yokokura, T. (2001) Suppressive Effects of Bifidobacteria on Lipid Peroxidation in the Colonic Mucosa of Iron-Overloaded Mice. Journal of Dairy Science, 84, 1583-1589. https://doi.org/10.3168/jds.S0022-0302(01)74591-2
Şengül, N., Işık, S., Aslım, B., Uçar, G. and Demirbağ, A.E. (2011) The Effect of Exopolysaccharide-Producing Probiotic Strains on Gut Oxidative Damage in Experimental Colitis. Digestive Diseases and Sciences, 56, 707-714. https://doi.org/10.1007/s10620-010-1362-7
Federico, A., Morgillo, F., Tuccillo, C., Ciardiello, F. and Loguercio, C. (2007) Chronic Inflammation and Oxidative Stress in Human Carcinogenesis. International Journal of Cancer, 121, 2381-2386. https://doi.org/10.1002/ijc.23192
Fox, P.F. and McSweeney, P.L.H. (1998) Dairy Chemistry and Biochemistry.
Fadden, K. and Owen, R.W. (1992) Faecal Steroids and Colorectal Cancer: The Effect of Lactulose on Faecal Bacterial Metabolism in a Continuous Culture Model of the Large Intestine. European Journal of Cancer Prevention, 1, 113-128. https://doi.org/10.1097/00008469-199202000-00004
Nagendra, R. and Rao, S.V. (1992) Effect of Incorporation of Lactulose in Infant Formulas on the Intestinal Bifidobacteria! Flora in Rats. International Journal of Food Sciences and Nutrition, 43, 169-173. https://doi.org/10.3109/09637489209028369
Terada, A., Hara, H., Kataoka, M. and Mitsuoka, T. (1992) Effect of Lactulose on the Composition and Metabolic Activity of the Human Faecal Flora. Microbial Ecology in Health and Disease, 5, 43-50. https://doi.org/10.3109/08910609209141303
Crittenden, R.G. and Playne, M.J. (1996) Production, Properties and Applications of Food-Grade Oligosaccharides. Trends in Food Science & Technology, 7, 353-361. https://doi.org/10.1016/S0924-2244(96)10038-8
Playne, M.J. and Crittenden, R.G. (2009) Galacto-Oligosaccharides and Other Products Derived from Lactose. Advanced Dairy Chemistry, 3, 121-202.
Gorski, D. (1997) Ingredient Forecast Product Development for World Markets. Dairy Foods, 98, 60-62.
Roberfroid, M.B., Van Loo, J.A. and Gibson, G.R. (1998) The Bifidogenic Nature of Chicory Inulin and Its Hydrolysis Products. The Journal of Nutrition, 128, 11-19. https://doi.org/10.1093/jn/128.1.11
Rao, V.A. (2001) The Prebiotic Properties of Oligofructose at Low Intake Levels. Nutrition Research, 21, 843-848. https://doi.org/10.1016/S0271-5317(01)00284-6
Duar, R.M., Ang, P.T., Hoffman, M., Wehling, R., Hutkins, R. and Schlegel, V. (2015) Processing Effects on Four Prebiotic Carbohydrates Supplemented in an Extruded Cereal and a Low pH Drink. Cogent Food & Agriculture, 1, Article ID: 1013782. https://doi.org/10.1080/23311932.2015.1013782
Vega, R. and Zuniga-Hansen, M.E. (2015) The Effect of Processing Conditions on the Stability of Fructooligosaccharides in Acidic Food Products. Food Chemistry, 173, 784-789. https://doi.org/10.1016/j.foodchem.2014.10.119
Ukena, S.N., Singh, A., Dringenberg, U., Engelhardt, R., Seidler, U., Hansen, W., Bleich, A., Bruder, D., Franzke, A. and Rogler, G. (2007) Probiotic Escherichia coli Nissle 1917 Inhibits Leaky Gut by Enhancing Mucosal Integrity. PLoS ONE, 2, e1308. https://doi.org/10.1371/journal.pone.0001308
Henker, J., Laass, M., Blokhin, B.M., Bolbot, Y.K., Maydannik, V.G., Elze, M., Wolff, C. and Schulze, J. (2007) The Probiotic Escherichia coli Strain Nissle 1917 (EcN) Stops Acute Diarrhoea in Infants and Toddlers. European Journal of Pediatrics, 166, 311-318. https://doi.org/10.1007/s00431-007-0419-x
Watson, D., O’Connell Motherway, M., Schoterman, M.H.C., Neerven, R.J., Nauta, A. and Sinderen, D. (2013) Selective Carbohydrate Utilization by Lactobacilli and Bifidobacteria. Journal of Applied Microbiology, 114, 1132-1146. https://doi.org/10.1111/jam.12105
Kaplan, H. and Hutkins, R.W. (2000) Fermentation of Fructooligosaccharides by Lactic Acid Bacteria and Bifidobacteria. Applied and Environmental Microbiology, 66, 2682-2684. https://doi.org/10.1128/AEM.66.6.2682-2684.2000
Shigwedha, N., Hiwilepo-Van Hal, P., Jia, L., Sichel, L. and Zhang, S. (2016) Prebiotics: Metabolism and Symbiotic Synergy with Probiotics in Promoting Health. In: Rao, V. and Rao, L.G., Eds., Probiotics and Prebiotics in Human Nutrition and Health, InTech, London, Chapter 3.
De Vries, W. and Stouthamer, A.H. (1969) Factors Determining the Degree of Anaerobiosis of Bifidobacterium Strains. Archivfür Mikrobiologie, 65, 275-287.
Scaldaferri, F., Gerardi, V., Lopetuso, L.R., Del Zompo, F., Mangiola, F., Boškoski, I., Bruno, G., Petito, V., Laterza, L., Cammarota, G. and Gaetani, E. (2013) Gut Microbial Flora, Prebiotics, and Probiotics in IBD: Their Current Usage and Utility. BioMed Research International, 2013, Article ID: 435268.
Tuohy, K.M., Probert, H.M., Smejkal, C.W. and Gibson, G.R. (2003) Using Probiotics and Prebiotics to Improve Gut Health. Drug Discovery Today, 8, 692-700. https://doi.org/10.1016/S1359-6446(03)02746-6
Zuccotti, G.V., Meneghin, F., Raimondi, C., Dilillo, D., Agostoni, C., Riva, E. and Giovannini, M. (2008) Probiotics in Clinical Practice: An Overview. Journal of International Medical Research, 36, 1A-53A. https://doi.org/10.1177/14732300080360S101
Hong, H.A. and Cutting, S.M. (2005) The Use of Bacterial Spore Formers as Probiotics. FEMS Microbiology Reviews, 29, 813-835. https://doi.org/10.1016/j.femsre.2004.12.001
Endres, J., Clewell, A., Jade, K., Farber, T., Hauswirth, J. and Schauss, A. (2009) Safety Assessment of a Proprietary Preparation of a Novel Probiotic, Bacillus coagulans, as a Food Ingredient. Food and Chemical Toxicology, 47, 1231-1238. https://doi.org/10.1016/j.fct.2009.02.018
O’Sullivan, L., Murphy, B., McLoughlin, P., Duggan, P., Lawlor, P.G., Hughes, H. and Gardiner, G.E. (2010) Prebiotics from Marine Macroalgae for Human and Animal Health Applications. Marine Drugs, 8, 2038-2064. https://doi.org/10.3390/md8072038
Wang, X. and Gibson, G. (1993) Effects of the in Vitro Fermentation of Oligofructose and Inulin by Bacteria Growing in the Human Large Intestine. Journal of Applied Bacteriology, 75, 373-380. https://doi.org/10.1111/j.1365-2672.1993.tb02790.x
Schouler, C., Taki, A., Chouikha, I., Moulin-Schouleur, M. and Gilot, P. (2009) A Genomic Island of an Extraintestinal Pathogenic Escherichia coli Strain Enables the Metabolism of Fructooligosaccharides, Which Improves Intestinal Colonization. Journal of Bacteriology, 191, 388-393. https://doi.org/10.1128/JB.01052-08
Ziemer, C.J. and Gibson, G.R. (1998) An Overview of Probiotics, Prebiotics and Synbiotics in the Functional Food Concept: Perspectives and Future Strategies. International Dairy Journal, 8, 473-479. https://doi.org/10.1016/S0958-6946(98)00071-5
Fanaro, S., Chierici, R., Guerrini, P. and Vigi, V. (2003) Intestinal Microflora in Early Infancy: Composition and Development. Acta Paediatrica, 92, 48-55.
Lievin, V., Peiffer, I., Hudault, S., Rochat, F., Brassart, D., Neeser, J.R. and Servin, A.L. (2000) Bifidobacterium Strains from Resident Infant Human Gastrointestinal Microflora Exert Antimicrobial Activity. Gut, 47, 646-652. https://doi.org/10.1136/gut.47.5.646
Rossi, M., Corradini, C., Amaretti, A., Nicolini, M., Pompei, A., Zanoni, S. and Matteuzzi, D. (2005) Fermentation of Fructooligosaccharides and Inulin by Bifidobacteria: A Comparative Study of Pure and Fecal Cultures. Applied and Environmental Microbiology, 71, 6150-6158. https://doi.org/10.1128/AEM.71.10.6150-6158.2005
Valdés-Varela, L., Ruas-Madiedo, P. and Gueimonde, M. (2017) In Vitro Fermentation of Different Fructo-Oligosaccharides by Bifidobacterium Strains for the Selection of Synbiotic Combinations. International Journal of Food Microbiology, 242, 19-23. https://doi.org/10.1016/j.ijfoodmicro.2016.11.011
Langlands, S.J., Hopkins, M.J., Coleman, N. and Cummings, J.H. (2004) Prebiotic Carbohydrates Modify the Mucosa Associated Microflora of the Human Large Bowel. Gut, 53, 1610-1616. https://doi.org/10.1136/gut.2003.037580
Martarelli, D., Verdenelli, M.C., Scuri, S., Cocchioni, M., Silvi, S., Cecchini, C. and Pompei, P. (2011) Effect of a Probiotic Intake on Oxidant and Antioxidant Parameters in Plasma of Athletes during Intense Exercise Training. Current Microbiology, 62, 1689-1696. https://doi.org/10.1007/s00284-011-9915-3
Ejtahed, H.S., Mohtadi-Nia, J., Homayouni-Rad, A., Niafar, M., Asghari-Jafarabadi, M. and Mofid, V. (2012) Probiotic Yogurt Improves Antioxidant Status in Type 2 Diabetic Patients. Nutrition, 28, 539-543. https://doi.org/10.1016/j.nut.2011.08.013
Madhu, A.N., Amrutha, N. and Prapulla, S.G. (2012) Characterization and Antioxidant Property of Probiotic and Synbiotic Yogurts. Probiotics and Antimicrobial Proteins, 4, 90-97. https://doi.org/10.1007/s12602-012-9099-6
Virtanen, T., Pihlanto, A., Akkanen, S. and Korhonen, H. (2007) Development of Antioxidant Activity in Milk Whey during Fermentation with Lactic Acid Bacteria. Journal of Applied Microbiology, 102, 106-115. https://doi.org/10.1111/j.1365-2672.2006.03072.x