To evaluate the Effects of Lactic Acid Bacteria Fermented Lemon Juice from Limon and Eureka Varieties of Taiwan on Anti-pathogenic Bacteria and Anti-allergy

Cheng-Chih Tsai^1, , Li-Yun Lin¹, Tzu-Min Lai¹ and Lan-Chun Chou¹

¹Department of Food Science and Technology, HungKuang University, Taichung 43302, Taiwan

Cite this paper:
Cheng-Chih Tsai, Li-Yun Lin, Tzu-Min Lai and Lan-Chun Chou. To evaluate the Effects of Lactic Acid Bacteria Fermented Lemon Juice from Limon and Eureka Varieties of Taiwan on Anti-pathogenic Bacteria and Anti-allergy. Journal of Food and Nutrition Research. 2021; 9(7):382-388. doi: 10.12691/jfnr-9-7-9

Abstract

Lemon juice contains many bioactive compounds that have potential health benefits. In this study, two different lactic acid bacteria (LAB) strains were used as starter cultures, change in pH, viable cell count during fermentation and antimicrobial, immune boosting, anti-allergy properties were monitored. LAB strains were able to grow in the juice and their viable cell reached to 8.0 log CFU/mL after 72 h at 30°C. Fermentation of lemon juice with LAB had a 2+ inhibitory ability against Vibrio parahaemolyticus and 3+ inhibitory ability against uropathogenic Escherichia coli. The inhibitory action of lactic acid fermentation against the pathogens may be due to the accumulation of main primary metabolites and pH changed during the fermentation. In the adhesion assay, PL LP10069 and TL PM229 exhibited stronger adherence to the Caco-2 cell line. With the anti-allergy test, the expression of anti-allergy cytokine of lemon juice fermentation in PBMC cell lines. The result indicated the significant enhanced to IL-12 by 1% NE PM229. The conclusion showed that fermentation of Lemon juice by probiotic bacteria not only increase antibacterial and anti-allergy effects but also enhance health benefit.

Keywords:
lemon lactic acid bacteria antimicrobial anti-allergy

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References:

[1]	Harima-Mizusawa, N., Iino, T., Onodera-Masuoka, N., Kato-Nagaoka, N., Kiyoshima-Shibata, J., Gomi, A. et al. “Beneficial effects of citrus juice fermented with Lactobacillus plantarum YIT 0132 on Japanese cedar pollinosis,” Bioscience of Microbiota, Food and Health, 33 (4). 147-155. Jun. 2014.
[2]	Mahmoud Barakat, S.M., Yamazaki, K., Miyashita, K., Shin, I.S., Chang D.S., and Suzuki, T. “Bacterial microflora of carp (Cyprinus carpio) and its shelf-life extension by essential oil compounds,” Food Microbiology, 21 (6). 657-666. Dec. 2004.
[3]	Fernández-López, J., Zhi, N., Aleson-Carbonell, L., Pérez-Alvarez, J.A., and Kuri, V. “Antioxidant and antibacterial activities of natural extracts: application in beef meatballs,” Meat Science, 69 (3). 371-380. Mar. 2005.
[4]	Alakomi, H.L., Skyttä, E., Saarela, M., Mattila-Sandholm, T., Latva-Kala, K., and Helander, I.M. “Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane,” Applied and Environmental Microbiology, 66 (5). 2001-2005. May 2001.
[5]	Bernardes, T.F., Reis, R.A., and Amaral, R.C.D. “Chemical and microbiological changes and aerobic stability of marandu grass silages after silo opening,” Revista Brasileira de Zootecnia, 38 (1). 1-8. Jan. 2009.
[6]	Bruno, M.E.C., and Montville, T.J. “Common mechanistic action of bacteriocins from lactic acid bacteria,” Applied and Environmental Microbiology, 59 (9). 3003-3010. Sep. 1993.
[7]	Zacharofa, M.P., and Lovittb, R.W. “Bacteriocins produced by lactic acid bacteria a review article,” APCBEE Procedia, 2. 50-56. 2012.
[8]	Jay, J.M. “Antimicrobial properties of diacetyl,” Applied and Environmental Microbiology, 44 (3): 525-532. Sep. 1982.
[9]	Hessle, C., Andersson, B., Wold, A.E. “Gram-positive bacteria are potent inducers of monocytic interleukin-12 (IL-12) while gram-negative bacteria preferentially stimulate IL-10 production,” Infection and Immunity, 68 (6). 3581-3586. Jun. 2000.
[10]	Chen, J., Fujino, Y., and Takahashi, T. “Experimental uveitis induced by intravitreal or intravenous lipoteichoic acid in rabbits,” Japanese Journal of Ophthalmology, 43 (5). 368-374. Sep-Oct. 1999.
[11]	LeBlanc, J.G., Matar, C., Valdez, J.C., LeBlanc, J., and Perdigon, G. “Immunomodulating effects of peptidic fractions issued from milk fermented with Lactobacillus helveticus,” Journal of Dairy Science, 85 (11). 2733-2742. Nov. 2002.
[12]	Wei, D., Ci, X., Chu, X., Wei, M., Hua, S., and Deng, X. “Hesperidin suppresses ovalbumin-induced airway inflammation in a mouse allergic asthma model,” Inflammation, 35 (1) 114-121. Feb. 2012.
[13]	Tsai, C.C., Lai, T.M., Lin, P.P., and Hsieh, Y.M. “Evaluation of lactic acid bacteria isolated from fermented plant products for antagonistic activity against urinary tract pathogen Staphylococcus saprophyticus,” Probiotics and Antimicrobial Proteins, 10 (2). 210-217. Jun. 2018.
[14]	Chapman, C.M.C., Gibson, G.R., Todd, S., and Rowland, I. “Comparative in vitro inhibition of urinary tract pathogens by single- and multi-strain probiotics,” European Journal of Nutrition, 52 (6) 1669-1677. Sep. 2013.
[15]	Tsai, C.C., Hsih, H.Y., Huang, L.F., Lin, C.C., and Tsen, H.Y. “Antagonistic activity against Helicobacter pylori infection in vitro by a strain of Enterococcus faecium TM39,” International Journal of Food Microbiology, 96 (1). 1-12. Oct. 2004.
[16]	Villanova, PA. “Performance standards for antimicrobial disk susceptibility tests,” 6th ed. National Committee for Clinical Laboratory Standard; M2-A6. 1998.
[17]	Prescott, S.L., Dunstan, J.A., Hale, J., Breckler, L., Lehmann, H., Weston, S., and Richmond, P. “Clinical effects of probiotics are associated with increased interferon-gamma responses in very young children with atopic dermatitis,” Clinical & Experimental Allergy, 35 (12), 1557-1564. Dec. 2005.
[18]	Islam, M.K., Hasan, M.S., Mamun, M.A.A., Kudrat-E-Zahan, M., and Al-Bari, M.A.A. “Lemon juice synergistically preserved with lactobacilli ameliorates inflammation in Shigellosis mice,” Advances in Pharmacology and Pharmacy, 3 (1) 11-21. Feb. 2015.
[19]	Bernet-Camard, M.F., Liévin, V., Neeser, J.R., Servin, A.L., and Hudault, S. “The human Lactobacillus acidophilus strain LA1 secretes a nonbacteriocin antibacterial substance(s) active in vitro and in vivo,” Applied and Environmental Microbiology, 63 (7). 2747-2753. Jul. 1997.
[20]	Annuk, H., Shchepetova, J., Kullisaar, T., Songisepp, E., Zilmer, M., and Mikelsaar, M. “Characterization of intestinal lactobacilli as putative probiotic candidates,” Journal of Applied Microbiology, 94 (3). 403-412. 2003.
[21]	Gopal, P.K., Prasad, J., Smart, J., and Gill, HS. “In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli,” International Journal of Food Microbiology, 67 (3). 207-216. Aug. 2001.
[22]	Campana, R., van Hemert, S., and Baffone, W. “Strain-specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion,” Gut Pathogens, 9. 12. Mar. 2017.
[23]	Konieczna, C., Słodziński, M., and Schmidt, M.T. “Exopolysaccharides produced by Lactobacillus rhamnosus KL 53A and Lactobacillus casei Fyos affect their adhesion to enterocytes,” Polish Journal of Microbiology, 67 (3). 273-281. 2018.
[24]	Falah, F., Vasiee, A., Behbahani, B.A., Yazdi, F.T., Moradi, S., Mortazavi, S.A., and Roshanak, S. “Evaluation of adherence and anti-infective properties of probiotic Lactobacillus fermentum strain 4-17 against Escherichia coli causing urinary tract infection in humans,” Microbial Pathogenesis, 131. 246-253. Jun.2019.
[25]	Fina Martin, J., Palomino, M.M., Cutine, A.M., Modenutti, C.P., Fernández Do Porto, D.A., Allievi, M.C., Zanini, S.H., Mariño, K.V., Barquero, A.A., and Ruzal, S.M. “Exploring lectin-like activity of the S-layer protein of Lactobacillus acidophilus ATCC 4356,” Applied Microbiology and Biotechnology, 103 (12). 4839-4857. Jun. 2019.
[26]	Dimitrov, Z., Gotova, I., and Chorbadjiyska, E. “In vitro characterization of the adhesive factors of selected probiotics to Caco-2 epithelium cell line,” Biotechnology & Biotechnological Equipment, 28 (6) 1079-1083. Nov. 2014.
[27]	Leung, D.Y. “Atopic dermatitis: the skin as a window into the pathogenesis of chronic allergic diseases,” Journal of Allergy and Clinical Immunology. 96 (3). 302-318. Sep. 1995.
[28]	Cross, M.L., Stevenson, L.M., and Gill, H.S. “Anti-allergy properties of fermented foods: an important immunoregulatory mechanism of lactic acid bacteria?” International Immunopharmacology, 1 (5). 891-901. May 2001.
[29]	Isolauri, E., Sütas, Y., Kankaanpää, P., Arvilommi, H., and Salminen, S. “Probiotics: effects on immunity,” The American Journal of Clinical Nutrition, 73 (2). 444-450. 2001.
[30]	Foligne, B., Nutten, S., Grangette, C., Dennin, V., Goudercourt, D., Poiret, S. et al. “Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria,” World Journal of Gastroenterology, 13 (2). 236-243. Jan. 2007.
[31]	Guasti, L., Marino, F., Cosentino, M., Maroni, L., Maresca, A.M., Colombo, F. et al. “Cytokine production from peripheral blood mononuclear cells and polymorphonuclear leukocytes in patients studied for suspected obstructive sleep apnea,” Sleep and Breathing, 15 (1). 3-11. Jan. 2011.
[32]	Miettinen, M., Matikainen, S., Vuopio-Varkila, J., Pirhonen, J., Varkila, K., Kurimoto, M., and Julkunen, I. “Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells,” Infection and Immunity, 66 (12). 6058-6062. Dec. 1998.
[33]	Kekkonen, R.A., Kajasto, E., Miettinen, M., Veckman, V., Korpela, R., and Julkunen, I. “Probiotic Leuconostoc mesenteroides ssp. cremoris and Streptococcus thermophiles induce IL-12 and IFN-gamma production,” World Journal of Gastroenterology, 14 (8). 1192-1203. Feb. 2008.