DOI QR코드

DOI QR Code

Effect of green tea supplementation on probiotic potential, physico-chemical, and functional properties of yogurt

요구르트의 프로바이오틱 활성과 물리화학적 및 기능적 특성에 대한 녹차 추출물의 영향

  • Lim, Eun-Seo (Department of Food Science & Nutrition, Tongmyong University)
  • 임은서 (동명대학교 식품영양학과)
  • Received : 2017.06.02
  • Accepted : 2017.06.26
  • Published : 2017.06.30

Abstract

The aim of this study was to evaluate the effect of green tea extract on probiotic potential, physico-chemical and functional properties of yogurt fermented with Lactobacillus acidophilus D11 or Lactobacillus fermentum D37 strains isolated from Doenjang. Probiotic activities such as the resistance to artificial digestive juices and the ability to adhere to epithelial cells were slightly higher in yogurt supplemented with green tea extract than in plain yogurt, which may be attributed to the increase in the number of lactic acid bacteria (LAB) by green tea extract supplementation. Furthermore, the microbiological and physico-chemical properties such as the number of LAB, organic acid production and viscosity were significantly (P<0.05) increased in yogurt added green tea extract compared to plain yogurt fermented with L. acidophilus D11. However, the green tea extract did not significantly (P>0.05) affect these properties of yogurt fermented with L. fermentum D37 strain. Meanwhile, the antibacterial activities against Escherichia coli O157 ATCC 43889, Salmonella enteritidis ATCC 13076, and Salmonella typhimurium KCTC 2514 and antioxidant activities including total phenol content, radical scavenging ability, and ferric-reducing antioxidant power were significantly higher in plain yogurt fermented with L. fermentum D37 than with L. acidophilus D11. The antibacterial and antioxidant activities of the yogurt were significantly (P<0.05) increased in proportion to the concentration of green tea extract added to plain yogurt. Consequently, green tea yogurt fermented with L. acidophilus D11 or L. fermentum D37 was considered to be a useful functional food that can inhibit the growth of pathogenic bacteria and scavenge the free radicals from the body cells.

본 연구에서는 된장으로부터 분리된 Lactobacillus acidophilus D11 또는 Lactobacillus fermentum D37 균주로 발효시킨 요구르트의 프로바이오틱로서의 가능성, 물리 화학적 및 기능적 특성에 대한 녹차 추출물의 영향을 조사하였다. 인공 소화액에 대한 저항성과 상피 세포에 대한 부착력과 같은 프로바이오틱활성은 플레인 요구르트보다 녹차 추출물을 첨가한 요구르트에서 다소 높게 나타났는데, 이는 유산균의 수의 증가에 기인하는 것으로 추정되었다. L. acidophilus D11로 발효시킨 플레인 요구르트에 녹차 추출물을 첨가한 경우 유산균수, 유기산 함량 및 점도와 같은 요구르트의 물리 화학적 특성도 유의하게 (P<0.05) 증가하였다. 하지만 녹차 추출물은 L. fermentum D37 균주 발효시킨 요구르트의 물리 화학적 특성에는 유의한 영향을 미치지 않았다 (P>0.05). 한편, Escherichia coli O157 ATCC 43889, Salmonella enteritidis ATCC 13076 및 Salmonella typhimurium KCTC 2514에 대한 항균 활성 및 총 페놀 함량, 라디칼 소거능 및 철 환원력과 같은 항산화 활성은 L. acidophilus D11 보다는 L. fermentum D37로 발효시킨 플레인 요구르트에서 현저히 높았다. 게다가 요구르트의 항균 및 항산화 활성은 녹차 추출물의 농도에 비례하여 유의적으로 증가하였다(P<0.05). 결론적으로, L. acidophilus D11 또는 L. fermentum D37로 발효시킨 녹차 요구르트는 병원성 세균의 성장을 억제하고 체세포 내에 생성된 자유 라디칼을 제거 할 수 있는 유용한 기능성 식품으로 이용할 수 있는 것으로 판단되었다.

Keywords

References

  1. Almajano, M.P., Carbo, R., Jimenez, J.A.L. 2008. Antioxidant and antimicrobial activities of tea infusions. Food Chem. 108, 55-63. https://doi.org/10.1016/j.foodchem.2007.10.040
  2. Amirdivani, S. and Baba, A.S. 2011. Changes in yogurt fermentation characteristics, and antioxidant potential and in vitro inhibition of angiotensin-1 converting enzyme upon the inclusion of peppermint, dill and basil. LWT-Food Sci. Technol. 44, 1458-1464. https://doi.org/10.1016/j.lwt.2011.01.019
  3. Amirdivani, S. and Baba, A.S. 2015. Changes in yogurt fermentation characteristics, and antioxidant potential and in vitro inhibition of angiotensin-1 converting enzyme upon the inclusion of peppermint, dill and basil. LWT-Food Sci. Technol. 44, 1458-1464.
  4. Apostolidis, E., Kwon, Y.I., and Shetty, K. 2007. Inhibitory potential of herb, fruit, and fungal-enriched cheese against key enzymes linked to type 2 diabetes and hypertension. Inno. Food Sci. Emerg. Technol. 8, 46-54. https://doi.org/10.1016/j.ifset.2006.06.001
  5. Arts, M.J., Haenen, G.R., Wilms, L.C., Beetstra, S.A., Heijnen, C.G., Voss, H.P., and Bast, A.J. 2002. Interactions between flavonoids and proteins: effect on the total antioxidant capacity. J. Agr. Food Chem. 50, 1184-1187. https://doi.org/10.1021/jf010855a
  6. Aryana, K.J. 2003. Folic acid fortified fat free plain set yogurts. Int. J. Dairy Technol. 56, 219-222. https://doi.org/10.1046/j.1471-0307.2003.00105.x
  7. Avall-Jaaskelainen, S. and Palva, A. 2005. Lactobacillus surface layers and their applications. FEMS Microbiol. Rev. 29, 511-529.
  8. Azizkhani, M. and Tooryan, F. 2016. Antimicrobial activities of probiotic yogurt flavored with pepperment, basil, and Zataria against Escherichia coli and Listeria monocytogenes. J. Food Qual. Hazard. Control 3, 79-86.
  9. Baba, A.S., Najarian, A., Shori, A.B., Lit, K., and Keng, G.A. 2014. In vitro inhibition of key enzymes related to diabetes and hypertension in Lycium barbarum-yogurt. Arabian J. Sci. Eng. 39, 5355-5362. https://doi.org/10.1007/s13369-014-1127-2
  10. Bazzaz, B.S.F., Sarabandi, S., Khameneh, B., and Hosseinzadeh, H. 2016. Effect of catechins, green tea extract and methylxanthines in combination with gentamicin against Staphylococcus aureus and Pseudomonas aeruginosa. J. Pharmaco. 19, 312-318. https://doi.org/10.3831/KPI.2016.19.032
  11. Billard, I., Mekki, S., Ouadi, A., and Gaillard, C. 2007. TTA solvation kinetics in the ionic liquid Bumim Tf2N. Comp. Rendus. Chimie. 10, 1117-1121. https://doi.org/10.1016/j.crci.2007.04.007
  12. Blum, U. 1998. Effects of microbial utilization of phenolic acids and their phenolic acid breakdown products on allelpathic interactions. J. Chem. Ecol. 24, 685-708. https://doi.org/10.1023/A:1022394203540
  13. Chan, EWC., Soh, E.Y., Tie, P.P., and Law, Y.P. 2011. Antioxidant and antibacterial properties of green, black, and herbal teas of Camellia sinensis. Pharmaco. Res. 3, 266-272. https://doi.org/10.4103/0974-8490.89748
  14. Cinbas, A. and Yazici, F. 2008. Effect of the addition of blueberries on selected physicochemical and sensory properties of yoghurt. J. Food Technol. Biotechnol. 46, 434-441.
  15. Corr, S.C., Hill, C., and Gahan, C.G. 2009. Understanding the mechanisms by which probiotics inhibit gastrointestinal pathogens. Adv. Food Nutr. Res. 56, 1-15.
  16. Curk, M.C., Hubert, J.C., and Bringel, F. 1996. Lactobacillus paraplantarum sp. Now, a new species related to Lactobacillus plantarum. Int. J. System. Bacteriol. 46, 595-598. https://doi.org/10.1099/00207713-46-2-595
  17. Damin, M.R., Alcantara, M.R., Nunes, A.P., and Oliveira, M.N. 2009. Effects of milk supplementation with skim milk powder whey protein concentration and sodium caseinate on acidification kinetics, rheological properties and structure of nonfat stirred yogurt. LWT-Food Sci. Technol. 17, 1744-1750.
  18. Dave, R.I. and Shah, N.P. 1998. Ingredient supplementation effects on viability of probiotic bacteria in yogurt. J. Dairy Sci. 81, 2804-2816. https://doi.org/10.3168/jds.S0022-0302(98)75839-4
  19. Eissa, E.A., Mohamed, Ahamed, I.A., Yagoub, A.E., and Babiker, E.E. 2010. Physico-chemical, microbiological and sensory characteristics of yoghurt produced from goat milk. Livestock Res. Rural Develop. 22, 247-253.
  20. Farvin, S., Baron, C., Nina, S.K., and Jacobsen, C. 2010. Antioxidant activity of yoghurt peptides: par 1-in vitro assays and evaluation in omega-3 enriched milk. Food Chem. 123, 1081-1089. https://doi.org/10.1016/j.foodchem.2010.05.067
  21. Gemenchu, T. 2015. Review on lactic acid bacteria function in milk fermentation and preservation. Afr. J. Food Sci. 9, 170-175. https://doi.org/10.5897/AJFS2015.1276
  22. Huang, Y. and Adams, M.C. 2004. In vitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy propionibacteria. Int. J. Food Microbiol. 91, 253-260. https://doi.org/10.1016/j.ijfoodmicro.2003.07.001
  23. Jack, R.W., Tagg, J.R., and Ray, B. 1995. Bacteriocins of Grampositive bacteria. Microbiol. Rev. 59, 171-200.
  24. Jaziri, I., Slama, M.B., Mhadhbi, H., Urdaci, M.C., and Hamdi, M. 2009. Effect of green and black teas (Camellia sinensis L.) on the characteristic microflora of yogurt during fermentation and refrigerated storage. Food Chem. 112, 614-620. https://doi.org/10.1016/j.foodchem.2008.06.017
  25. Joung, J.Y., Lee, J.Y., Ha, Y.S., Shin, Y.K., Kim, Y.H., Kim, S.H., and Oh, N.S. 2016. Enhanced microbial, functional and sensory properties of herbal yogurt fermented with Korean traditional plant extracts. Kor. J. Food Sci. 36, 90-99. https://doi.org/10.5851/kosfa.2016.36.1.90
  26. Jung, D.W., Nam, E.S., and Park, S.I. 2005. Effect of green tea powder on growth of lactic culture. Korean J. Food Nutr. 18, 325-333.
  27. Jung, D.W. and Park, S.I. 2005. Preparation of drinkable yoghurt added with green tea powder. Korean J. Food Nutr. 18, 349-356.
  28. Kankainen, M., Paulin, L., Tynkkynen, S., Von Ossowski, I., Reunanen, J., and Partanen, P. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pilli containing a humanmucus binding protein. Natl. Acad. Sci. 106, 17193-17198. https://doi.org/10.1073/pnas.0908876106
  29. Korhonen, H. 2009. Milk derived bioactive peptides: from science to applications. J. Funct. Food 1, 177-187. https://doi.org/10.1016/j.jff.2009.01.007
  30. Kumar, R., Bhagat, S.K., Kumar, V., and Nirmala, A. 2013. Antioxidant activity and cytotoxic analysis of seed extract of Punical Granatum. Asian J. Biochem. Pharm. 3, 225-236.
  31. Lavermicocca, P. 2006. Highlights on new food research. Digest. Liver. Dis. 38, S295-S299. https://doi.org/10.1016/S1590-8658(07)60014-0
  32. Lee, H.C., Jenner, A.M., Low, C.S., and Lee, Y.K. 2006. Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota. Res. Microbiol. 157, 876-884. https://doi.org/10.1016/j.resmic.2006.07.004
  33. Lejeune, J.T. and Rajala-Schultz, P.J. 2009. Unpasturized milk : a continued public health threat. Food Safety 48, 93-100.
  34. Lim, S.M. 2014. Heterocyclic amines removal by binding ability of lactic acid bacteria isolated from soybean paste. Korean J. Microbiol. 50, 73-83. https://doi.org/10.7845/kjm.2014.4011
  35. Lim, S.M., Lee, G.J., Park, S.M., Ahn, D.H., and Im, D.S. 2006. Characterization of Lactobacillus cellobiosus D37 isolated from soybean paste as a probiotic with anti-cancer and antimicrobial properties. Food Sci. Biotechnol. 5, 792-798.
  36. Lin, M.Y. and Yen, C.L. 1999. Antioxidative ability of lactic acid bacteria. J. Agric. Food Chem. 47, 1460-1466. https://doi.org/10.1021/jf981149l
  37. Lopez de Lacey, A.M., Perez-Santin, E., Lopez-Caballero, M.E., and Montero, P. 2014. Survival and metabolic activity of probiotic bacteria in green tea. LWT-Food Sci. Technol. 55, 314-322. https://doi.org/10.1016/j.lwt.2013.08.021
  38. Lu, M., Shiau, Y., Wong, J., Lin, R., Kravis, H., Blackmon, T., Pakzad, T., Jen, T., Cheng, A., Chang, J., et al. 2013. Milk spoilage: methods and practices of detecting milk quality. Food Nutr. Sci. 4, 113-123.
  39. Marcinakova, M., Klingberg, T.D., Laukova, A., and Budde, B.B. 2010. The effect of pH, bile and calcium on the adhesion ability of probiotic enterococci of animal origin to the porcine jejunal epithelial cell line IPEC-J2. Anaerobe 16, 120-124. https://doi.org/10.1016/j.anaerobe.2009.05.001
  40. Marhamatizadeh, M.H., Ehsandoost, E., and Gholami, P. 2013. The influence of green tea (Camellia sinensis L.) extract on characteristic of probiotic bacteria in milk and yoghurt during fermentation and refrigerated storage. Int. J. Farm Alli. Sci. 2, 599-606.
  41. Michael, M., Phebus, R.K., and Schmidt, K.A. 2010. Impact of a plant extract on the viability of Lactobacillus delbrueckii spp. bulgaricus and Streptococcus thermophilus in a non-fat yogurt. Int, Dairy J. 20, 665-672. https://doi.org/10.1016/j.idairyj.2010.03.005
  42. Michalczyk, M. and Zawislak, A. 2008. The effect of tea infusions on the proliferation of selected bacteria important for the human intestinal tract. Acta. Sci. Pol. Technol. Aliment. 7, 59-65.
  43. Muniandy, P., Shori, A.B., and Baba, A.S. 2016. Influence of green, white and black tea addition on the antioxidant activity of probiotic yogurt during refrigerated storage. Food Pack Shelf Life 8, 1-8. https://doi.org/10.1016/j.fpsl.2016.02.002
  44. Muniandy, P., Shori, A.B., and Baba, A.S. 2017. Comparison of the effect of green, white and black tea on Streptococcus thermophilus and Lactobacillus spp. in yogurt during refrigerated storage. J. Asso. Arab. Uni. Basic Appl. Sci. 22, 26-30.
  45. Najgebauer-Lejko, D. 2014. Effect of green tea supplementation on the microbiological, antioxidant, and sensory properties of probiotic milks. Dairy Sci. Technol. 94, 327-339. https://doi.org/10.1007/s13594-014-0165-6
  46. Najgebauer-Lejko, D., Sady, M., Grega, T., and Walczycka, M. 2011. The impact of tea supplementation on microflora: pH and antioxidant capacity of yoghurt. Int. Dairy J. 21, 568-574. https://doi.org/10.1016/j.idairyj.2011.03.003
  47. Neffe-Skocinska, K., Jaworska, D., Kolozyn-Krajewska, D., Dolatowski, Z., and Jachacz-Jowko, L. 2015. The effect of LAB as probiotic starter culture and green tea extract addition on dry fermented pork loins quality. BioMed. Res. Int. 2015, 1-9.
  48. Nikjooy, S. and Hashemi, H. 2015. Study the possibility of producing symbiotic yogurt containing Lactobacillus casei and wild thyme extract. Int. J. Agri. Crop. Sci. 8, 61-67.
  49. Ouwehand, A.C. and Salminen, S. 2003. In vitro adhesion assays for probiotics and their in vivo relevance: a review. Microb. Ecol. Health Dis. 15, 175-184. https://doi.org/10.1080/08910600310019886
  50. Ouwehand, A.C., Tuomaola, E.M., Tolkko, S., and Salminen, S. 2001. Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. Int. J. Food Microbiol. 64, 119-126. https://doi.org/10.1016/S0168-1605(00)00440-2
  51. Ozer, B., Kirmachi, H.A., Oztekin, S., Hayaloglu, A., and Atamer, M. 2007. Incorporation of microbial transglutaminase into non-fat yogurt procution. Int. Dairy J. 17, 199-207. https://doi.org/10.1016/j.idairyj.2006.02.007
  52. Ranadheera, C.S., Evans, C.A., Adams, M.C., and Baines, S.K. 2012. In vitro analysis of gastrointestinal tolerance and intestinal cell adhesion of probiotics in goat's milk ice cream and yogurt. Food Res. Int. 49, 619-625. https://doi.org/10.1016/j.foodres.2012.09.007
  53. Rice-Evans, C., Sampson, J., Bramley, P.M., and Holloway, D.E. 1997. Why do we expect carotenoids to be antioxidants in vivo. Free Radical Res. 26, 381-398. https://doi.org/10.3109/10715769709097818
  54. Sanlibaba, P. and Cakmak, G.A. 2016. Exopolysaccharides production by lactic acid bacteria. Appl. Microbiol. 2, 1-5.
  55. Schneider, H., Schwiertz, A., Collins, M.D., and Blaut, M. 1999. Anaerobic transformation of quercetin-3-glucoside by bacteria from the human intestinal tract. Arch. Microbiol. 171, 81-91. https://doi.org/10.1007/s002030050682
  56. Servin, A.L. 2004. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol. Rev. 28, 405-440. https://doi.org/10.1016/j.femsre.2004.01.003
  57. Shah, N.P. 2003. Yogurt: the product and its manufacture. In Caballero, B., Trugo, L.C., and Finglas, P.M. (eds.) (2nd ed.) Encyclopedia Food Sci. Nutr. Vol. 10 Academic Press, London, UK.
  58. Shah, N.P. 2007. Functional cultures and health benefits. Int Dairy. J. 17, 1262-1277. https://doi.org/10.1016/j.idairyj.2007.01.014
  59. Shah, N.P. and Ravula, R.R. 2002. Influence of water activity on fermentation, organic acids production and viability of yogurt and probiotic bacteria. Aust. J. Dairy Technol. 55, 127-131. https://doi.org/10.1046/j.1471-0307.2002.00044.x
  60. Shetty, K., Clydesdale, F., and Vattrem, D. 2005. Clonal screening and sprout based bioprocessing of phenolic phytochemicals for functional foods. In Shetty, K., Paliyath, G., Pometto, A., and Levin, R.E. (eds.) Food Biotechnol, p. 603. CRC Taylor & Francis, New York, USA.
  61. Shetty, K., Curtis, O.F., Levin, R.E., Witkowsky, R., and Ang, W. 1995. Prevention of verification associated with in vitro shoot culture of oregano (Origanum vulgare) by Pseudomonas ssp. J. Plant Physiol. 147, 447-451. https://doi.org/10.1016/S0176-1617(11)82181-4
  62. Shewale, R., Sawale, P.D., Khedkar, C.D., and Singh, A. 2014. Selection criteria for probiotics: a review. Int. J. Probiot. Prebiot. 9, 1-6.
  63. Shokryazdan, P., Sieo, C.C., Kalavathy, R., Liang, J.B., Alitheen, N.B., Jahromi, M.F., and Ho, Y.W. 2014. Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. BioMed. Res. Int. 2014, 1-16.
  64. Tabasco, R., Sanchez-Patan, F., Monagas, M., Bartolome, B., Moreno-Arribas, M.V., Pelaez, C., and Requena, T. 2011. Effect of grape polyphenols on lactic acid bacteria and bifidobacteria growth: resistance and metabolism. Food Microbiol. 28, 1345-1352. https://doi.org/10.1016/j.fm.2011.06.005
  65. Tesfay, T., Kebede, A., and Seifu, E. 2013. Quality and safety of cow milk produced and marketed in dire dawa town, eastern Ethiopia. Int. J. Sci. Inn. Tech. 2, 1-5.
  66. Thompson, J.L., Lopetcharat, K., and Drake, M.A. 2007. Preferences for commercial strawberry drinkable yoghurts amon African American, Caucasian, and Hispanic consumers in the United States. J. Dairy Sci. 90, 4974-4987. https://doi.org/10.3168/jds.2007-0313
  67. Unal, G., Karagozlu, C., Kinik, O., Akan, E., and Akalin, A.S. 2016. Influence of supplementation with green and black tea on viscosity and sensory characteristics of drinking yoghurt. Ege. Univ. Ziraat. Fak. Derg. 53, 343-349.
  68. Vinderola, G., Cespedes, M., Mateolli, D., Cardenas, P., Lescano, M., and Aimaretti, N. 2011. Changes in gastric resistance of Lactobacillus casei in flavoured commercial fermented milks during refrigerated storage. Int. J. Dairy Technol. 64, 269-275. https://doi.org/10.1111/j.1471-0307.2010.00659.x
  69. Widyastuti, Y., Rohmatussolihat, A., and Febrisiantosa, A. 2014. The role of lactic acid bacteria in milk fermentation. Food Nutr. Sci. 5, 435-442. https://doi.org/10.4236/fns.2014.54051
  70. Zarate, G., De Ambrosini, V.M., Chaia, A.P., and Gonzalez, A. 2002. Some factors affecting the adherence of probiotic Propionibacterium acidopropionici CRL 1198 to intestinal epithelial cells. Can. J. Microbiol. 48, 449-457. https://doi.org/10.1139/w02-036
  71. Zhu, Q.Y., Hackman, R.M., Ensunsa, J.L., Holt, R.R., and Keen, C.L. 2002. Antioxidative activities of oolong tea. J. Agr. Food Chem. 50, 6929-6934. https://doi.org/10.1021/jf0206163
  72. Zhu, Y., Xiao, L., Shen, D., and Hao, Y. 2010. competition between yogurt probiotics and periodontal pathogens in vitro. Acta. Odontol. Scand 68, 261-268. https://doi.org/10.3109/00016357.2010.492235