Enhanced Bioactivity and Anti-microbial Properties of Lactobacillus plantarum Fermented Purple Onion (Allium cepa L.) Extracts Against Selected Poultry Microbes

Al-Yousef HM, Ahmed AF, Al-Shabib NA, Laeeq S, Khan RA, Rehman MT, Alsalme A, Al-Ajmi MF, Khan MS & Husain FM. 2017. Onion peel ethyl acetate fraction and its derived constituent quercetin 4′-O-β-D glucopyranoside attenuate quorum sensing regulated virulence and biofilm formation. Frontiers in Microbiology, 8: 1675. DOI: 10.3389/fmicb.2017.01675

Aujoulat F, Lebreton F, Romano S, Delage M, Marchandin H, Brabet M, Bricard F, Godreuil S, Parer S & Jumas-Bilak E. 2011. Comparative diffusion assay to assess the efficacy of topical antimicrobial agents against Pseudomonas aeruginosa in burns care. Annals of Clinical Microbiology and Antimicrobials, 10: 27. DOI: 10.1186/1476-0711-10-27

Brizuela N, Tymczyszyn EE, Semorile LC, La Hens DV, Delfederico L, Hollmann A & Bravo-Ferrada BJ. 2019. Lactobacillus plantarum as a malolactic starter culture in winemaking: A new (old) player? European Journal of Biotechnology, 38: 10-18. DOI: 10.1016/j.ejbt.2018.12.002

Casella S, Leonardi M, Melai B, Fratini F & Pistelli L. 2013. The role of diallyl sulfides and dipropyl sulfides in the in vitro antimicrobial activity of the essential oil of garlic, Allium sativum L., and leek, Allium porrum L. Phytotherapy Research, 27: 380-383. DOI: 10.1002/ptr.4725

Dec M, Puchalski A, Urban-Chmiel R & Wernicki A. 2014. Screening of Lactobacillus strains of domestic goose origin against bacterial poultry pathogens for use as probiotics. Poultry Science, 93: 2464-2472. DOI: 10.3382/ps.2014-04025

Di Cagno R, Coda R, De Angelis M & Gobbetti M. 2013. Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiology, 33: 1-10. DOI: 10.1016/j.fm.2012.09.003

Ding SC. Virology: Principles and Applications. The Yale Journal of Biology and Medicine, 2008; Sep;81(3):155–6. Epub 2008 Sep. PMCID: PMC2553660

Elmowalid GA, Abd El-Hamid MI, Abd El-Wahab AM, Atta M, Abd El-Naser G & Attia AM. 2019. Garlic and ginger extracts modulated broiler chicks innate immune responses and enhanced multidrug resistant Escherichia coli O78 clearance. Comparative immunology, microbiology and infectious diseases, 66: 101334. DOI: 10.1016/j.cimid.2019.101334

Fadare OS, Singh V, Enabulele OI, Shittu OH & Pradhan D. 2022. In vitro evaluation of the synbiotic effect of probiotic Lactobacillus strains and garlic extract against Salmonella species. LWT - Food Science and Technology, 153: 112439. DOI: 10.1016/j.lwt.2021.112439

Filocamo A, Nueno-Palop C, Bisignano C, Mandalari G & Narbad A. 2012. Effect of garlic powder on the growth of commensal bacteria from the gastrointestinal tract. Phytotherapy Research, 19: 707-711. DOI: 10.1016/j.phymed.2012.02.018

Georgieva R, Yocheva L, Tserovska L, Zhelezova G, Stefanova N, Atanasova A, Danguleva A, Ivanova G, Karapetkov N, Rumyan N & Karaivanova E. 2015. Antimicrobial activity and antibiotic susceptibility of Lactobacillus and Bifidobacterium spp. intended for use as starter and probiotic cultures. Biotechnology and Biotechnological Equipment, 29: 84-91. DOI: 10.1080/13102818.2014.987450

Ghoke S, Sood R, Kumar N, Pateriya A, Bhatia S, Mishra A, Dixit R, Singh V, Desai D & Kulkarni D. 2018. Evaluation of antiviral activity of Ocimum sanctum and Acacia arabica leaves extracts against H9N2 virus using embryonated chicken egg model. BMC Complementary Medicine and Therapies, 18: 1-10. DOI: 10.1186/s12906-018-2238-1

Hai PV, Van HT, Van Chao N, Khuong ND, Le TT, Dung HT & Hung PHS. 2019. Antimicrobial activity of chives and ginger extract on Escherichia coli and Salmonella spp. isolated from broiler chickens. Hue University Journal of Science: Agriculture and Rural Development, Dec 4; 128(3B): 105-11. DOI: 10.26459/hueuni-jard.v128i3B.5310

Hai PV, Phuong HTA, Hung PHS, Na TT, Lai NH, Khuong NDT, Liem TN & Hoa NX. 2024. Selection of Lactobacillus strains from native chicken feces for the fermentation of purple onion (Allium cepa L.) as an antibiotic alternative against Salmonella spp. in chickens. Open Veterinary Journal, 14(12): 3525-3538. DOI: 10.5455/OVJ.2024.v14.i12.35

Han J, Lawson L, Han G & Han P. 1995. Spectrophotometric method for quantitative determination of allicin and total garlic thiosulfinates. Analytical Biochemistry, 225: 157-160. DOI: 10.1006/abio.1995.1124

Kim S, Park SL, Lee S, Lee SY, Ko S &Yoo M. 2016. UPLC/ESI-MS/MS analysis of compositional changes for organosulfur compounds in garlic (Allium sativum L.) during fermentation. Food Chemistry, 211: 555-559. DOI: 10.1016/j.foodchem.2016.05.102

Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, Goossens H & Laxminarayan R. 2018. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proceedings of the National Academy of Sciences, 115: E3463-E3470. DOI:10.1073/pnas.1717295115

Kothari D, Lee WD, Niu KM & Kim SK. 2019. The genus Allium as poultry feed additive: A review. Animals, 9: 1032. DOI: 10.3390/ani9121032

Kyung KH. 2012. Antimicrobial properties of Allium species. Current Opinion in Biotechnology, 23: 142–147. DOI: 10.1016/j.copbio.2011.08.004

Lee CF, Han CK & Tsau JL. 2004. In vitro inhibitory activity of Chinese leek extract against Campylobacter species. International Journal of Food Microbiology, 94: 169–174. DOI: 10.1016/j.ijfoodmicro.2004.01.009

Lee S, Oh DG, Singh D, Lee JS, Lee S & Lee CH. 2020. Exploring the metabolomic diversity of plant species across spatial (leaf and stem) components and phylogenic groups. BMC Plant Biology, 20: 1–10. DOI: 10.1186/s12870-019-2231-y

Lee YG, Cho JY, Kim YM & Moon JH. 2016. Change in flavonoid composition and antioxidative activity during fermentation of onion (Allium cepa L.) by Leuconostoc mesenteroides with different salt concentrations. Journal of Food Science, 81. DOI: 10.1111/1750-3841.13329

Martino ME, Bayjanov JR, Caffrey BE, Wels M, Joncour P, Hughes S, Gillet B, Kleerebezem M, van Hijum SAFT & Leulier F. 2016. Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats. Environmental Microbiology, 18: 4974–4989. DOI: 10.1111/1462-2920.13455

Millet A, Lamy E, Jonas D, Stintzing F, Mersch-Sundermann V & Merfort I. 2012. Fermentation enhances the biological activity of Allium cepa bulb extracts. Journal of Agricultural and Food Chemistry, 60(9): 2148–2156. DOI: 10.1021/jf2041643

Ming T, Han J, Li Y, Lu C, Qiu D, Li Y, Zhou J & Su X. 2018. A metabolomics and proteomics study of the Lactobacillus plantarum in the grass carp fermentation. BMC Microbiology, 18: 1–13. DOI: 10.1021/jf2041643

Nhung NT, Chansiripornchai N & Carrique-Mas JJ. 2017. Antimicrobial resistance in bacterial poultry pathogens: A review. Frontiers in Veterinary Science, 4: 126. DOI: 10.3389/fvets.2017.00126

Osman KM, Kappell AD, Elhadidy M, ElMougy F, El-Ghany WAA, Orabi A, Mubarak AS, Dawoud TM, Hemeg HA & Moussa IM. 2018. Poultry hatcheries as potential reservoirs for antimicrobial-resistant Escherichia coli: A risk to public health and food safety. Scientific Reports, 8(1): 5859. DOI: 10.1038/s41598-018-23962-7

Othman NB, Roblain D, Chammen N, Thonart P, Hamdi M. 2009. Antioxidant phenolic compounds loss during the fermentation of Chétoui olives. Food Chemistry, 116: 662–669. DOI: 10.1016/j.foodchem.2009.02.084

Pan M, Wu Q, Tao X, Wan C, Shah NP & Wei HJ. 2015. Fermentation of Allium Chinese bulbs with Lactobacillus plantarum ZDY 2013 shows enhanced bifunctionalities, and nutritional and chemical properties. Journal of Food Science, 80: M2272–M2278. DOI: 10.1111/1750-3841.12994

Park DH, Kothari D, Niu KM, Han SG, Yoon JE, Lee HG & Kim SK. 2019. Effect of fermented medicinal plants as dietary additives on food preference and fecal microbial quality in dogs. Animals, 9: 690. DOI: 10.3390/ani9090690

Putnik P, Gabrić D, Roohinejad S, Barba FJ, Granato D, Mallikarjunan K, Lorenzo JM & Kovačević DB. 2019. An overview of organosulfur compounds from Allium spp.: From processing and preservation to evaluation of their bioavailability, antimicrobial, and anti-inflammatory properties. Food Chemistry, 276: 680–691. DOI: 10.1016/j.foodchem.2018.10.068

Rahman K & Billington D. 2000. Dietary supplementation with aged garlic extract inhibits ADP-induced platelet aggregation in humans. Journal of Nutrition, 130: 2662–2665. DOI: 10.1093/jn/130.11.2662

Reuben RC, Roy PC, Sarkar SL, Alam RU & Jahid IK. 2019. Isolation, characterization, and assessment of lactic acid bacteria toward their selection as poultry probiotics. BMC Microbiology, 19: 1–20. DOI: 10.1186/s12866-019-1626-0

Rhee SJ, Lee JE & Lee CH. 2011. Importance of lactic acid bacteria in Asian fermented foods. Microbial Cell Factories, 10: S5. DOI:10.1186/1475-2859-10-S1-S5

Salem W, El-Hamed DMS, Sayed W & Elamary R. 2017. Alterations in virulence and antibiotic-resistant genes of multidrug-resistant Salmonella serovars isolated from poultry: The bactericidal efficacy of Allium sativum. Microbial Pathogenesis, 108: 91–100. DOI: 10.1016/j.micpath.2017.05.008

Shokryazdan P, Kalavathy R, Sieo C, Alitheen N, Liang J, Jahromi M & Ho Y. 2014. Isolation and characterization of Lactobacillus strains as potential probiotics for chickens. Pertanika Journal of Tropical Agricultural Science, 37: 141-157.

Suh DH, Jung ES, Park HM, Kim SH, Lee S, Jo YH, Lee MK, Jung G, Do SG & Lee CH. 2016. Comparison of metabolites variation and anti-obesity effects of fermented versus nonfermented mixtures of Cudrania tricuspidata, Lonicera caerulea, and soybean according to fermentation in vitro and in vivo. PLoS One, 11: e0149022. DOI: 10.1371/journal.pone.0149022.

Suresh G, Das RK, Kaur Brar S, Rouissi T, Avalos Ramirez A, Chorfi Y & Godbout S. 2018. Alternatives to antibiotics in poultry feed: molecular perspectives. Critical Reviews in Microbiology, 44: 318–335. DOI: 10.1080/1040841X.2017.1373062

Torino MI, Limón RI, Martínez-Villaluenga C, Mäkinen S, Pihlanto A, Vidal-Valverde C & Frias J. 2013. Antioxidant and antihypertensive properties of liquid and solid-state fermented lentils. Food Chemistry, 136: 1030–1037. DOI: 10.1016/j.foodchem.2012.09.015

Torres S, Verón H, Contreras L & Isla MI. 2020. An overview of plant-autochthonous microorganisms and fermented vegetable foods. Food Science and Human Wellness, 9: 112–123. DOI: 10.1016/j.fshw.2020.02.006

Wang S, Peng Q, Jia H, Zeng X, Zhu J, Hou C, Liu X, Yang F & Qiao S. 2017. Prevention of Escherichia coli infection in broiler chickens with Lactobacillus plantarum B1. Poultry Science, 96: 2576–2586. DOI: 10.3382/ps/pex061

Wouters D, Bernaert N, Conjaerts W, Van Droogenbroeck B, De Loose M & De Vuyst L. 2013. Species diversity, community dynamics, and metabolite kinetics of spontaneous leek fermentations. Food Microbiology, 33: 185–196. DOI: 10.1016/j.fm.2012.09.016

Xiang H, Sun-Waterhouse D, Waterhouse GI, Cui C, Ruan Z. 2019. Fermentation-enabled wellness foods: A fresh perspective. Food Science and Human Wellness, 8: 203–243. DOI: 10.1016/j.fshw.2019.08.003

Yabuki Y, Mukaida Y, Saito Y, Oshima K, Takahashi T, Muroi E, Hashimoto K & Uda Y. 2010. Characterization of volatile sulfur-containing compounds generated in crushed leaves of Chinese chive (Allium tuberosum Rottler). Food Chemistry, 120: 343–348. DOI: 10.1016/j.jksus.2022.101971

Yadav S, Trivedi NA & Bhatt JD. 2015. Antimicrobial activity of fresh garlic juice: An in vitro study. Ancient Science of Life, 36: 203–207. DOI: 10.4103/0974-8520.175548

Yang F, Chen C, Ni D, Yang Y, Tian J, Li Y, Chen S, Ye X & Wang L. 2023. Effects of fermentation on bioactivity and the composition of polyphenols contained in polyphenol-rich foods: A review. Foods, 12: 3315. DOI: 10.3390/foods12173315

Yang J, Ji Y, Park H, Lee J, Park S, Yeo S, Shin H & Holzapfel WH. 2014. Selection of functional lactic acid bacteria as starter cultures for the fermentation of Korean leek (Allium tuberosum Rottler ex Sprengel). International Journal of Food Microbiology, 191: 164–171. DOI: 10.1016/j.ijfoodmicro.2014.09.016

Ye JH, Huang LY, Terefe NS & Augustin MA. 2019. Fermentation-based biotransformation of glucosinolates, phenolics, and sugars in retorted broccoli puree by lactic acid bacteria. Food Chemistry, 286: 616–623. DOI: 10.1016/j.foodchem.2019.02.030

Ye M, Yue T & Yuan Y. 2014. Changes in the profile of volatile compounds and amino acids during cider fermentation using dessert variety of apples. European Food Research and Technology, 239: 67–77. DOI: 10.1007/s00217-014-2204-1 · 

Yu Y, Xu Y, Li L, Chen S, An K, Yu Y & Xu ZL. 2023. Isolation of lactic acid bacteria from Chinese pickle and evaluation of fermentation characteristics. LWT, 180: 114627. DOI:10.2139/ssrn.4285445