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
|