Abstract
Lactobacillus plantarum was encapsulated by slowly digestible hydrolyzed heat-moisture-treated (hydrolyzed-HMT) black waxy rice and applied in yoghurt. Incorporating these microcapsules in yoghurt resulted in higher viability of Lactobacillus bulgaricus C49 and Streptococcus thermophilus C44, especially in prolonged storage. The viability of L. bulgaricus and S. thermophilus (7.98 and 8.28 Log CFU/g) in synbiotic yoghurt was higher than in the control (7.81 and 7.96 Log CFU/g). Thirty-two aromatic compounds were detected and classified into 4 groups: alcohols, carbonyls, organic acids, and sulfur. Synbiotic yoghurt produced higher carbonyl compounds, particularly acetaldehyde and diacetyl. On the other hand, higher organic acid especially hexanoic, dodecanoic, acetic, butanoic, and pentanoic acids was observed at the end of fermentation but did not differ from control after storage. Ethanol was also higher in the synbiotic yoghurt due to the breakdown of glucose from starch and acetaldehyde by lactic acid bacteria. Weak correlation was found concerning sulfur compounds. Rice starch granules were aggregated and still retained its hexagonal shape, indicating high resistance to acid fermentation during 28 days of storage. The resistant starch coating from rice could provide a good prebiotic ingredient and allow the design of synbiotic yoghurt with enhanced aroma.
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Al-Attabi, Z., D’Arcy, B. R., & Deeth, H. C. (2014). Volatile sulfur compounds in pasteurised and UHT milk during storage. Dairy Science & Technology, 94(3), 241–253. https://doi.org/10.1007/s13594-013-0157-y.
Avila-Reyes, S. V., Garcia-Suarez, F. J., Jiménez, M. T., Martín-Gonzalez, M. F. S., & Bello-Perez, L. A. (2014). Protection of L. rhamnosus by spray-drying using two prebiotics colloids to enhance the viability. Carbohydrate Polymers, 102, 423–430. https://doi.org/10.1016/j.carbpol.2013.11.033.
Ardö, Y. (2006). Flavour formation by amino acid catabolism. Biotechnology Advances, 24(2), 238–242. https://doi.org/10.1016/j.biotechadv.2005.11.005.
Aryana, k. J., & McGrew, P. (2007). Quality attributes of yogurt with Lactobacillus casei and various prebiotics. LWT - Food Science and Technology, 40(10), 1808–1814. https://doi.org/10.1016/j.lwt.2007.01.008.
Beards, E., Tuohy, K., & Gibson, G. (2010). Bacterial, SCFA and gas profiles of a range of food ingredients following in vitro fermentation by human colonic microbiota. Anaerobe, 16(4), 420–425. https://doi.org/10.1016/j.anaerobe.2010.05.006.
Beshkova, D., Simova, E., Frengova, G., & Simov, Z. (1998). Production of flavour compounds by yogurt starter cultures. Journal of Industrial Microbiology & Biotechnology, 20(3-4), 180–186. https://doi.org/10.1038/sj.jim.2900504.
Chaves, A. C. S. D., Fernandez, M., Lerayer, A. L. S., Mierau, I., Kleerebezem, M., & Hugenholtz, J. (2002). Metabolic engineering of acetaldehyde production by Streptococcus thermophilus. Applied and Environmental Microbiology, 68(11), 5656–5662. https://doi.org/10.1128/AEM.68.11.5656-5662.2002.
Cheng, H. (2010). Volatile flavor compounds in yoghurt: a review. Critical Reviews in Food Science and Nutrition, 50(10), 938–950. https://doi.org/10.1080/10408390903044081.
Coghetto, C. C., Brinques, G. B., & Ayub, M. A. Z. (2016). Probiotics production and alternative encapsulation methodologies to improve their viabilities under adverse environmental conditions. International Journal of Food Sciences and Nutrition, 67(8), 929–943. https://doi.org/10.1080/09637486.2016.1211995.
Cogan, T. M., Fitzgerald, R. J., & Doonan, S. (1984). Acetolactate synthase of Leuconostoc lactis and its regulation of acetoin production. Journal of Dairy Research, 51(04), 597–604. https://doi.org/10.1017/S002202990003291X.
Costabile, A., Walton, G. E., Tzortzis, G., Vulevic, J., Charalampopoulos, D., & Gibson, G. R. (2015). Effects of orange juice formulation on prebiotic functionality using an in vitro colonic model system. PLoS One, 10(3), e0121955. https://doi.org/10.1371/journal.pone.0121955.
Crittenden, R., Karppinen, S., Ojanen, S., Tenkanen, M., Fagerström, R., Mättö, J., Saarela, M., Sandholm, T. M., & Poutanen, K. (2002). In vitro fermentation of cereal dietary fiber carbohydrates by probiotic and intestinal bacteria. Journal of the Science of Food and Agriculture, 82(8), 781–789. https://doi.org/10.1002/jsfa.1095.
Cummings, J. H., Macfarlane, G. T., & Englyst, H. N. (2001). Prebiotic digestion and fermentation. American Journal of Clinical Nutrition, 73(2 Suppl), 415S–420S.
Curic, M., Lauridsen, B. S., Renaulp, P., & Nilsson, D. (1999). A general method for selection of α-acetolactate decarboxylase-deficient Lactococcus lactis mutants to improve diacetyl formation. Applied and Environmental Microbiology, 65(3), 1202–1206.
Curioni, P. M. G., & Bosset, J. O. (2002). Key odorants in various cheese types as determined by gas chromatography-olfactometry. International Dairy Journal, 12(12), 959–984. https://doi.org/10.1016/S0958-6946(02)00124-3.
Damin, M. R., Minowa, E., Alcantara, M. R., & Oliveira, M. N. (2008). Effect of cold storage on culture viability and some rheological properties of fermented milk prepared with yoghurt probiotic bacteria. Journal of Texture Studies, 39(1), 40–55. https://doi.org/10.1111/j.1745-4603.2007.00129.x.
Daims, H., Brühl, A., Amann, R., Schleifer, K. H., & Wagner, M. (1999). The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Systematic and Applied Microbiology, 22(3), 434–444. https://doi.org/10.1016/S0723-2020(99)80053-8.
Dave, R. I., & Shah, N. P. (1997). Viability of yoghurt and probiotic bacteria in yoghurts made from commercial starter cultures. International Dairy Journal, 7(1), 31–41. https://doi.org/10.1016/S0958-6946(96)00046-5.
De Araújo Etchepare, M., Raddatz, G. C., de Moraes Flores, E. M., Zepka, L. Q., Jacob-Lopes, E., Barin, J. S., Grosso, C. R. F., & de Menezes, C. R. (2016). Effect of resistant starch and chitosan on survival of Lactobacillus acidophilus microencapsulated with sodium alginate. LWT - Food Science and Technology, 65, 511–517. https://doi.org/10.1016/j.lwt.2015.08.039.
Desai, A. R., Powell, I. B., & Shah, N. P. (2004). Survival and activity of probiotic Lactobacilli in skim milk containing prebiotics. Journal of Food Science, 69, 57–60.
Dongowski, E., Jacobasch, G., & Schmiedl, D. (2005). Structural stability and prebiotic properties of resistant starch type 3 increase bile acid turnover and lower secondary bile acid formation. Journal of Agricultural and Food Chemistry, 53(23), 9257–9267. https://doi.org/10.1021/jf0507792.
Fakhravar, S., Najafpour, G., Heris, S. Z., Izadi, M., & Fakhravar, A. (2012). Fermentative lactic acid from deproteinized whey using Lactobacillus bulgaricus in batch culture. World Applied Sciences Journal, 17(9), 1083–1086.
Franks, A. H., Harmsen, H. J., Raangs, G. C., Jansen, G. J., Schut, F., & Welling, G. W. (1998). Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group specific 16S RNAtargeted oligonucleotide probes. Applied and Environmental Microbiology, 64(9), 3336–3345.
Fritzen-Freire, C. B., Prudêncio, E. S., Pinto, S. S., Muñoz, I. B., & Amboni, R. D. M. C. (2013). Effect of microencapsulation on survival of Bifidobacterium BB-12 exposed to simulated gastrointestinal conditions and heat treatments. LWT - Food Science and Technology, 50(1), 39–44. https://doi.org/10.1016/j.lwt.2012.07.037.
Gaggia, F., Mattarelli, P., & Biavati, B. (2010). Probiotics and prebiotics in animal feeding for safe food production. International Journal of Food Microbiology, 141(Suppl 1), S15–S28. https://doi.org/10.1016/j.ijfoodmicro.2010.02.031.
Gibson, G. R., & Roberfroid, M. D. (1995). Dietary modulation of the human colonic microbiota – Introducing the concept of prebiotics. Journal of Nutrition, 125(6), 1401–1412.
Grimaldi, R., Swann, J. R., Vulevic, J., Gibson, G. R., & Costabile, A. (2016). Fermentation properties and potential prebiotic activity of Bimuno® galacto-oligosaccharide (65% galacto-oligosaccharide content) on in vitro gut microbiota parameters. British Journal of Nutrition, 116(3), 480–486. https://doi.org/10.1017/S0007114516002269.
Gustaw, W., Kordowska-Wiater, M., & Kozioł, J. (2011). The influence of selected prebiotics on the growth of lactic acid bacteria for bio-yoghurt production. Acta Scientiarum Polonorum Technologia Alimentaria, 10(4), 455–466.
Hidalgo, M., Oruna-Concha, M. J., Kolida, S., Walton, G. E., Kallithraka, S., Spencer, J. P., & de Pascual-Teresa, S. (2012). Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. Journal of Agricultural and Food Chemistry, 60, 3882−3890.
ISO/IDF (2009). ISO-PDTS11869/IDF-DRM150 Fermented Milks: Determination of titratable acidity—potentiometric method. International standard; ISO 14673–2International Organization for Standardization, Geneva.
Kailasapathy, K. (2006). Survival of free and encapsulated probiotic bacteria and their effect on the sensory properties of yoghurt. LWT - Food Science and Technology, 39(10), 1221–1227. https://doi.org/10.1016/j.lwt.2005.07.013.
Kailasapathy, K., & Supriadi, D. (1996). Effect of whey protein concentrate on the survival of Lactobacillus acidophilus in lactose hydrolyzed yoghurt during. Milchwissenschaft, 51, 566–569.
Le Leu, R. K., Brown, I. L., Hu, Y., Bird, A. R., Jackson, M., Esterman, A., & Young, G. P. (2005). A Synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged cells in rat colon. Journal of Nutrition, 135(5), 996–1001. https://doi.org/10.1093/jn/135.5.996.
Macfarlane, G. T., Steed, H., & Macfarlane, S. (2008). Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. Journal of Applied Microbiology, 104(2), 305–344. https://doi.org/10.1111/j.1365-2672.2007.03520.x.
Maconi, E., Griffini, A., Cavazzoni, V., & Aragozzini, F. (1988). Reduction of acetaldehyde to ethanol by some micro-organisms and its stereospecificity. Biochemical Journal, 250(3), 929–932. https://doi.org/10.1042/bj2500929.
Mani-López, E., Palou, E., & López-malo, A. (2014). Probiotic viability and storage stability of yoghurts and fermented milks prepared with several mixtures of lactic acid bacteria. Journal of Dairy Science, 97(5), 2578–2590. https://doi.org/10.3168/jds.2013-7551.
Massot-Cladera, M., Costabile, A., Childs, C. E., Yaqoob, P., Franch, A., Castell, M., & Pérez-Cano, F. J. (2015). Prebiotic effects of cocoa fibre on rats. Journal of Functional Foods, 19, 341–352. https://doi.org/10.1016/j.jff.2015.09.021.
Miao, M., Jiang, B., & Zhang, T. (2009). Effect of pullulanase debranching and recrystallization on structure and digestibility of waxy maize starch. Carbohydrate Polymers, 76(2), 214–221. https://doi.org/10.1016/j.carbpol.2008.10.007.
Mutungi, C., Onyango, C., Doert, T., Paasch, S., Thiele, S., Machill, S., Jaros, D., & Rohm, H. (2011). Long- and short-range structural changes of recrystallised cassava starch subjected to in vitro digestion. Food Hydrocolloids, 25(3), 477–485. https://doi.org/10.1016/j.foodhyd.2010.07.023.
Oliveira, R. P. S., Perego, P., Oliveira, M. N., & Converti, A. (2011). Effect of inulin as prebiotic and synbiotic interactions between probiotics to improve fermented milk firmness. Journal of Food Engineering, 107(1), 36–40. https://doi.org/10.1016/j.jfoodeng.2011.06.005.
Özer, D., Akin, S., & Özar, B. (2005). Effect of inulin and lactulose on survival of Lactobacillus acidophilus LA-5 and Bifidobacterium bifidum BB-02 in acidophilus yoghurt. Food Science and Technology International, 11(1), 19–24. https://doi.org/10.1177/1082013205051275.
Picot, A., & Lacroix, C. (2004). Encapsulation of bifidobacteria in whey protein-based microcapsules and survival in simulated gastrointestinal conditions and in yoghurt. International Dairy Journal, 14(6), 505–515. https://doi.org/10.1016/j.idairyj.2003.10.008.
Paseephol, T., & Sherkat, F. (2009). Probiotic stability of yoghurts containing Jerusalem artichoke inulins during refrigerated storage. Journal of Functional Foods, 1(3), 311–318. https://doi.org/10.1016/j.jff.2009.07.001.
Pitiphunpong, S., & Suwannaporn, P. (2009). Physicochemical properties of KDML 105 rice cultivar from different cultivated locations in Thailand. Journal of the Science of Food and Agriculture, 89(13), 2186–2190. https://doi.org/10.1002/jsfa.3701.
Rodríguez-Cabezas, M. E., Camuesco, D., Arribas, B., Mesa, N. G., Comalada, M., Bailón, E., Sola, M. C., Utrilla, P., Hernández, E. G., Roca, C. P., Gálvez, J., & Zarzuelo, A. (2010). The combination of fructooligosaccharides and resistant starch shows prebiotic additive effects in rats. Clinical Nutrition, 29(6), 832–839. https://doi.org/10.1016/j.clnu.2010.05.005.
Rychlik, M., Sax, M., & Schieberle, P. (2006). On the role of short-chain free fatty acids for the development of a cheese-like off-note in pasteurized yogurt. LWT - Food Science and Technology, 39(5), 521–527. https://doi.org/10.1016/j.lwt.2005.03.014.
Saint-Eve, A., Levy, C., Le Moigne, M., Ducruet, V., & Souchon, I. (2008). Quality changes in yogurt during storage in different packaging materials. Food Chemistry, 110(2), 285–293. https://doi.org/10.1016/j.foodchem.2008.01.070.
Saulnier, D. M. A., Molenaar, D., de Vos, W. M., Gibson, G. R., & Kolida, S. (2007). Identification of prebiotic fructooligosaccharide metabolism in Lactobacillus plantarum WCFS1 through microarrays. Applied and Environment Microbiology, 73(6), 1753–1765. https://doi.org/10.1128/AEM.01151-06.
Suskovic, J., Kos, B., Goreta, J., & Matosic, S. (2001). Role of lactic acid bacteria and Bifidobacteria in synbiotic effect. Food Technology and Biotechnology, 39(3), 227–235.
Scott, K. P., Duncan, S. H., & Flint, H. J. (2008). Dietary fibre and the gut microbiota. Nutrition Foundation Nutrition Bulletin, 33(3), 201–211. https://doi.org/10.1111/j.1467-3010.2008.00706.x.
Settachaimongkon, S., Nout, M. J. R., Antunes Fernandes, E. C., Hettinga, K. A., Vervoort, J. M., van Hooijdonk, T. C. M., Zwietering, M. H., Smid, E. J., & van Valenberg, H. J. F. (2014). Influence of different proteolytic strains of Streptococcus thermophilus in co-culture with Lactobacillus delbrueckii subsp. bulgaricus on the metabolite profile of set-yoghurt. International Journal of Food Microbiology, 177, 29–36. https://doi.org/10.1016/j.ijfoodmicro.2014.02.008.
Settachaimongkon, S., van Valenberg, H. J. F., Gazi, I., Nout, M. J. R., van Hooijdonk, T. C. M., Zwietering, M. H., & Smid, E. J. (2016). Influence of Lactobacillus plantarum WCFS1 on post-acidification, metabolite formation and survival of starter bacteria in set-yoghurt. Food Microbiology, 59, 14–22. https://doi.org/10.1016/j.fm.2016.04.008.
Sidira, M., Santarmaki, V., Kiourtzidis, K., Argyri, A. A., Papadopoulou, O. S., Chorianopoulos, N., Tassou, C., Kaloutsas, S., Galanis, A., & Kourkoutas, Y. (2017). Evaluation of immobilized Lactobacillus plantarum 2035 on whey protein as adjunct probiotic culture in yoghurt production. LWT - Food Science and Technology, 75, 137–146. https://doi.org/10.1016/j.lwt.2016.08.026.
Smid, E. J., & Lacroix, C. (2013). Microbe–microbe interactions in mixed culture food fermentations. Current Opinion in Biotechnology, 24(2), 148–154. https://doi.org/10.1016/j.copbio.2012.11.007.
Subhasree, R. S., Bhakyaraj, R., & Dinesh, B. P. (2013). Evaluation of brown rice and germinated brown rice as an alternative substrate for probiotic food formulation using Lactobacillus spp. isolated from goat milk. International Food Research Journal, 20(5), 2967–2971.
Talwalkar, A., Miller, C. W., Kailasapathy, K., & Nguyen, M. H. (2004). Effect of packaging materials and dissolved oxygen on the survival of probiotic bacteria in yoghurt. International Journal of Food Science and Technology, 39(6), 605–611. https://doi.org/10.1111/j.1365-2621.2004.00820.x.
Walker, A. W., Duncan, S. H., McWilliam Leitch, E. C., Child, M. W., & Flint, H. J. (2005). pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Applied and Environmental Microbiology, 71(7), 3692–3700. https://doi.org/10.1128/AEM.71.7.3692-3700.2005.
Wattananapakasem, I., Costabile, A., & Suwannaporn, P. (2018). Slow digestible colored rice flour as wall material for microencapsulation: Its impacts on gut bacterial population and metabolic activities. Food Research International, 103, 182–191. https://doi.org/10.1016/j.foodres.2017.10.027.
Yüksel, A. K., & Bakırcı, I. (2015). An investigation of the volatile compound profiles of probiotic yoghurts produced using different inulin and demineralised whey powder combinations. Food Science and Biotechnology, 24(3), 807–816. https://doi.org/10.1007/s10068-015-0105-0.
Zhao, R., Sun, J., Torley, P., Wang, D., & Niu, S. (2008). Measurement of particle diameter of lactobacillus acidophilus microcapsule by spray drying and analysis on its microstructure. World Journal of Microbiology and Biotechnology, 24(8), 1349–1354. https://doi.org/10.1007/s11274-007-9615-0.
Zhang, G., & Hamaker, B. R. (2009). Slowly digestible starch: concept, mechanism, and proposed extended glycemic index. Critical Reviews in Food Science and Nutrition, 49(10), 852–867. https://doi.org/10.1080/10408390903372466.
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This study was financially supported by Thailand Research Fund (TRF) through the Royal Golden Jubilee Ph.D. Program (Grant No. PHD/0107/2552) and the Royal Golden Jubilee PhD programme (one-year PhD placement in the UK) co-funded with Newton Fund 2015.
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Wattananapakasem, I., van Valenberg, H.J.F., Fogliano, V. et al. Synbiotic Microencapsulation from Slow Digestible Colored Rice and Its Effect on Yoghurt Quality. Food Bioprocess Technol 11, 1111–1124 (2018). https://doi.org/10.1007/s11947-018-2068-7
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DOI: https://doi.org/10.1007/s11947-018-2068-7