Sains Malaysiana 45(9)(2016): 1289–1297

Lactobacillus fermentum LAB 9-Fermented Soymilk with Enriched Isoflavones and Antioxidants Improved Memory In vivo

(Susu Soya Difermentasi oleh Lactobacillus fermentum LAB 9 yang Kaya dengan Isoflavon

dan Antioksida Memperbaiki Daya Ingatan secara In vivo)

 

E.F. MOHAMAD FAKRI1,2, S.M. LIM1,2, N.H. MUSA1,2,4, M. HAZIZUL HASAN1,3, A. ADAM1,3

& K. RAMASAMY1,2*

 

1Faculty of Pharmacy, Universiti Teknologi MARA, 42300 Bandar Puncak Alam, Selangor Darul Ehsan, Malaysia

 

2Collaborative Drug Discovery Research (CDDR) Group, Pharmaceutical and Life Science, Community of Research, Universiti Teknologi MARA, 40450 Shah Alam, Selangor Darul Ehsan

Malaysia

 

3Research on Affinity, Safety and Efficacy Studies (OASES), Pharmaceutical and Life Sciences Community of Research, Universiti Teknologi MARA, 40450 Shah Alam, Selangor Darul Ehsan

Malaysia

 

4Faculty of Applied Sciences, Universiti Teknologi MARA, Tapah Campus, Tapah Road

35400 Tapah, Perak Darul Redzuan, Malaysia

 

Diserahkan: 3 Januari 2016/Diterima: 3 Mei 2016

 

ABSTRACT

This study examined lactic acid bacteria (LAB)-fermented soymilk for their ability in hydrolyzing glucosides to aglycones and corresponding antioxidant capacity and memory enhancing effect. Twelve LAB isolated from Malaysian fermented food and milk products were incubated in commercially available soymilk for 48 h. Generally, soymilk supported LAB growth and significantly increased (p<0.05) conversion to bioactive aglycone by 2.1-6.5 fold when compared to unfermented soymilk. Lactobacillus fermentum LAB 9- fermented soymilk, in particular, was presented with increased total phenolic content (+10%) as opposed to unfermented soymilk. Lactobacilli (LAB 10-12)- and pediococci (LAB 5)-fermented soymilk elicited maximal DPPH radical-scavenging activity. LAB 1, 7, 8, 9 and 12 exhibited significantly higher (p<0.05) ferrous ion chelating activity when compared to control. Interestingly, LAB 9 had significantly improved memory deficit (p<0.05) in LPS-challenged mice. LAB-enriched nutritional value of soymilk could be useful against oxidative stress and memory deficit.

 

Keywords: Antioxidant; bioactive isoflavones; lactic acid bacteria; memory enhancing; soymilk

 

 

ABSTRAK

Kajian ini bertujuan menguji kebolehan susu soya yang difermentasi oleh bakteria laktik asid (LAB) dalam menghirolisiskan glukosida kepada aglikon dan potensi daripada segi antioksida serta peningkatan ingatan. Dua belas LAB yang dipencil daripada makanan Malaysia yang telah difermentasi telah dieram dalam susu soya komersial selama 48 jam. Secara amnya, susu soya menyokong pertumbuhan LAB dan meningkatkan secara signifikan (p<0.05) penukaran glukosida kepada aglikon bioaktif 2.1-6.5 kali ganda apabila dibandingkan dengan susu soya yang tidak difermentasi. Lactobacillus fermentum LAB 9, terutamanya, menunjukkan peningkatan jumlah kandungan fenol (+10%) berbanding dengan susu soya yang tidak difermentasi. Susu soya yang difermentasi oleh Lactobacilli (LAB 10-12)- dan pediococci (LAB 5) menunjukkan aktiviti DPPH radikal skaven yang maksimum. LAB 1, 7, 8, 9 dan 12 mempunyai aktiviti pengkelatan ferus ion yang tinggi secara signifikan (p<0.05) berbanding dengan kawalan. LAB 9 juga memperbaiki defisit daya ingatan mencit yang terdedah kepada LPS secara signifikan (p<0.05). Nilai nutrisi susu soya yang diperkayakan oleh LAB mungkin berguna terhadap tegasan pengoksidaan dan defisit ingatan.

 

Kata kunci: Antioksida; bakteria asid laktik; isoflavon; peningkatan ingatan; susu soya

RUJUKAN

Ahire, J.J., Mokashe, N.U., Patil, H.J. & Chaudhari, B.L. 2013. Antioxidative potential of folate producing probiotic Lactobacillus helveticus CD6. Journal of Food Science and Technology 50(1): 26-34.

Ahmad, A., Ramasamy, K., Jaafar, S.M., Majeed, A.B. & Mani, V. 2014. Total isoflavones from soybean and tempeh reversed scopolamine-induced amnesia, improved cholinergic activities and reduced neuroinflammation in brain. Food and Chemical Toxicology 65: 120-128.

de Moreno de LeBlanc, A., Del Carmen, S., Chatel, J.M., Miyoshi, A., Azevedo, V., Langella, P., Bermúdez-Humarán, L.G. & LeBlanc, J.G. 2015. Current review of genetically modified lactic acid bacteria for the prevention and treatment of colitis using murine models. Gastroenterology Research and Practice 2015: Article ID. 146972.

Ding, W.K. & Shah, N.P. 2010. Enhancing the biotransformation of isoflavones in soymilk supplemented with lactose using probiotic bacteria during extended fermentation. Journal of Food Science 75(3): M140-M149.

Donkor, O.N. & Shah, N.P. 2008. Production of beta-glucosidase and hydrolysis of isoflavone phytoestrogens by Lactobacillus acidophilus, Bifidobacterium lactis and Lactobacillus casei in soymilk. Journal of Food Science 73(1): M15-M20.

FAO 2002. Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live Lactic Acid Bacteria. Joint Food and Agricultural Organization of the United Nations and World Health Organization Expert Consultation Report, Cordoba, Argentina, 2001.

Food and Drug Administration. 1999. FDA survey of imported fresh produce. http://vm.cfsan.fda.gov/~dms/prodsurv.html. Accessed on 28 July 2015.

Izumi, T., Piskula, M.K., Osawa, S., Obata, A., Tobe, K., Saito, M., Kataoka, S., Kubota, Y. & Kikuchi, M. 2000. Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. The Journal of Nutrition 130(7): 1695-1699.

Kim, J.H., Choi, J.M., Lee, S. & Cho, E.J. 2012. Protective effects of purple sweet potato added to Bacillus subtilis-fermented soymilk against amyloid beta-induced memory impairment. Journal of Agricultural Science 4(4): 223-232.

King, R.A. & Bignell, C.M. 2000. Concentrations of isoflavone phytoestrgens and their glucosides in Australian soya beans and soya foods. Australian Journal of Nutrition and Dietetics 57: 70-78.

Kullisaar, T., Zilmer, M., Mikelsaar, M., Vihalemm, T., Annuk, H., Kairane, C. & Kilk, A. 2002. Two antioxidative lactobacilli strains as promising probiotics. International Journal of Food Microbiology 72(3): 215-224.

Le, K., Chiu, F. & Ng, K. 2007. Identification and quantification of antioxidants in Fructus lycii. Food Chemistry 105(1): 353-363.

Lee, J., Hwang, K.T., Chung, M.Y., Cho, D.H. & Park, C.S. 2005. Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect. Journal of Food Science 70(8): m388-m391.

Liu, C.F., Tseng, K.C., Chiang, S.S., Lee, B.H., Hsu, W.H. & Pan, T.M. 2011. Immunomodulatory and antioxidant potential of Lactobacillus exopolysaccharides. Journal of the Science of Food and Agriculture 91(12): 2284-2291.

Liu, C.F. & Pan, T.M. 2010. In vitro effects of lactic acid bacteria on cancer cell viability and antioxidant activity. Journal of Food and Drug Analysis 18(2): 77-86.

Marazza, J.A., Nazareno, M.A., de Giori, G.S. & Garro, M.S. 2012. Enhancement of the antioxidant capacity of soymilk by fermentation with Lactobacillus rhamnosus. Journal of Functional Foods 4(3): 594-601.

Marazza, J.A., Garro, M.S. & de Giori, G.S. 2009. Aglycone production by Lactobacillus rhamnosus CRL981 during soymilk fermentation. Food Microbiology 26(3): 333-339.

McCue, P.P. & Shetty, K. 2005. Phenolic antioxidant mobilization during yogurt production from soymilk using Kefir cultures. Process Biochemistry 40(5): 1791-1797.

Otieno, D.O., Ashton, J.F. & Shah, N.P. 2007. Isoflavone phytoestrogen degradation in fermented soymilk with selected beta-glucosidase producing L. acidophilus strains during storage at different temperatures. International Journal of Food Microbiology 115(1): 79-88.

Pandey, K.B. & Rizvi, S.I. 2009. Current understanding of dietary polyphenols and their role in health and disease. Current Nutrition and Food Science 5(4): 249-263.

Prasad, L.N. & Shah, N.P. 2011. Conversion of isoflavone glycoside to aglycones in soy protein isolate (SPI) using crude enzyme extracted from Bifidobacterium animalis Bb12 and Lactobacillus delbrueckii ssp. bulgaricus ATCC 11842. International Food Research Journal 19(2): 433-439.

Raghavendra, P., Ushakumari, S. & Halami, P. 2011. Phytate-degrading Pediococcus pentosaceus CFR R123 for application in functional foods. Beneficial Microbes 2(1): 57-61.

Ramasamy, K., Abdul Rahman, N.Z., Sieo, C.C., Alitheen, N.J., Abdullah, N. & Ho, Y.W. 2012. Probiotic potential of lactic acid bacteria from fermented Malaysian food or milk products. International Journal of Food Science and Technology 47(10): 2175-2183.

Rekha, C.R. & Vijayalakshmi, G. 2011. Isoflavone phytoestrogens in soymilk fermented with β-glucosidase producing probiotic lactic acid bacteria. International Journal of Food Sciences and Nutrition 62(2): 111-120.

Rekha, C.R. & Vijayalakshmi, G. 2008. Biomolecules and nutritional quality of soymilk fermented with probiotic yeast and bacteria. Applied Biochemistry and Biotechnology 151(2-3): 452-463.

Saide, J.A. & Gilliland, S.E. 2005. Antioxidative activity of lactobacilli measured by oxygen radical absorbance capacity. Journal of Dairy Science 88(4): 1352-1357.

Solioz, M., Mermod, M., Abicht, H.K. & Mancini, S. 2011. Responses of lactic acid bacteria to heavy metal stress. In Stress Responses of Lactic Acid Bacteria, edited by Tsakalidou, E. & Papadimitriou, K. New York: Springer. pp. 163-195.

Song, Y.R., Kim, Y.E., Kim, J.H., Song, N.E., Jeong, D.Y. & Baik, S.H. 2011. Preparation of fermented sugar-soaked black soybean snacks (FSBSS) and characterization of their quality changes. Food Science and Biotechnology 20(6): 1547-1553.

Stratil, P., Klejdus, B. & Kubáň, V. 2007. Determination of phenolic compounds and their antioxidant activity in fruits and cereals. Talanta 71(4): 1741-1751.

Sun, X.D. 2011. Enzymatic hydrolysis of soy proteins and the hydrolysates utilisation. International Journal of Food Science and Technology 46(12): 2447-2459.

Tachakittirungrod, S., Okonogi, S. & Chowwanapoonpohn, S. 2007. Study on antioxidant activity of certain plants in Thailand: mechanism of antioxidant action of guava leaf extract. Food Chemistry 103: 381-388.

Wang, Y.C., Yu, R.C. & Chou, C.C. 2006. Antioxidative activities of soymilk fermented with lactic acid bacteria and bifidobacteria. Food Microbiology 23(2): 128-135.

Wei, Q.K., Chen, T.R. & Chen, J.T. 2007. Using of Lactobacillus and Bifidobacterium to product the isoflavone aglycones in fermented soymilk. International Journal of Food Microbiology 117(1): 120-124.

Yeh, J.Y., Hsieh, L.H., Wu, K.T. & Tsai, C.F. 2011. Antioxidant properties and antioxidant compounds of various extracts from the edible basidiomycete Grifola frondosa (Maitake). Molecules 16(4): 3197-3211.

Zhao, D. & Shah, N.P. 2014. Changes in antioxidant capacity, isoflavone profile, phenolic and vitamin contents in soymilk during extended fermentation. LWT - Food Science and Technology 58(2): 454-462.

 

 

*Pengarang untuk surat-menyurat; email: kalav922@salam.uitm.edu.my