Biochemical and physical investigations on detoxification of ginkgo kernel juice using probiotic fermentation with macroporous resin addition
Yuyu Sun, Jiaying Zhao, Sivakumar Manickam, Jingyang He, Dandan Li, Yongbin Han, Xiaosan Jiang, Yang Tao
Biochemical and physical investigations on detoxification of ginkgo kernel juice using probiotic fermentation with macroporous resin addition
The toxicity of ginkgo kernel is a global concern, restricting its consumption as a medicinal food. This study focuses on eliminating the toxic components, specifically ginkgolic acid, from ginkgo kernel juice. The approach used was probiotic fermentation with autochthonous lactic acid bacteria combined with macroporous resin. Compared to using lactic acid fermentation alone, adding macroporous resin during probiotic fermentation significantly enhanced the removal of toxic ginkgolic acid and 4'- O-methylpyridoxine from ginkgo kernel juice. After 48 h of fermentation with macroporous resin, the contents of ginkgolic acid and 4'- O-methylpyridoxine decreased by more than 69% and 61%, respectively. Interestingly, the adsorption of microbial growth inhibitors, such as ginkgolic acid, 4'- O-methylpyridoxine, and phenolics, by the resin did not hinder the growth of lactic acid bacteria or their metabolic activities involving organic acids and monosaccharides. The study further confirmed that microbial adsorption was the primary reason for removing ginkgolic acid during probiotic fermentation. Also, the adsorption mechanism of ginkgolic acid during probiotic fermentation with macroporous resin was explored. From a mass transfer perspective, incorporating macroporous resin during the probiotic fermentation of ginkgo kernel juice reduced the mass transfer resistance for surface diffusion. Consequently, this lowered the contribution of surface diffusion to the overall diffusion process and facilitated the efficient removal of toxic ginkgolic acid. This work can help to understand the physical mechanism regarding detoxification of ginkgo kernel juice by probiotic fermentation, and offer potential strategies to enhance the safety of ginkgo kernel products.
Ginkgo kernel / Probiotic fermentation / Ginkgolic acid / Adsorption / Mass transfer
[1] |
Major RT. The Ginkgo, the most ancient living tree: The resistance of Ginkgo biloba L. to pests accounts in part for the longevity of this species Science. 1967, 157, 1270-73
CrossRef
Google scholar
|
[2] |
van Beek TA. Ginkgolides and bilobalide: Their physical, chromatographic and spectroscopic properties Bioorganic & Medicinal Chemistry. 2005, 13 17 5001-12
CrossRef
Google scholar
|
[3] |
Zhou G, Yao X, Tang Y, Qian D, Su S, et al. An optimized ultrasound-assisted extraction and simultaneous quantification of 26 characteristic components with four structure types in functional foods from ginkgo seeds Food Chemistry. 2014, 15 1 177-85
CrossRef
Google scholar
|
[4] |
Boateng ID, Zhang W, Li Y, Saalia FK, Yang X. Non-thermal pretreatment affects Ginkgo biloba L. seed's product qualities, sensory, and physicochemical properties Journal of Food Science. 2021, 12, 94-111
CrossRef
Google scholar
|
[5] |
Wang H, Shi M, Cao F, Su E. Ginkgo biloba seed exocarp: A waste resource with abundant active substances and other components for potential applications Food Research International. 2022, 160, 111637
CrossRef
Google scholar
|
[6] |
Ahlemeyer B, Krieglstein J. Neuroprotective effects of Ginkgo biloba extract Cellular and Molecular Life Sciences CMLS. 2003, 60, 1779-92
CrossRef
Google scholar
|
[7] |
Jang HS, Roh SY, Jeong EH, Kim BS, Sunwoo MK. Ginkgotoxin Induced Seizure Caused by Vitamin B6 Deficiency Journal of Epilepsy Research. 2015, 5 2 104-6
CrossRef
Google scholar
|
[8] |
Kobayashi D, Yoshimura T, Johno A, Sasaki K, Wada K. Toxicity of 4'- O-methylpyridoxine-5'-glucoside in Ginkgo biloba seeds Food Chemistry. 2011, 126 3 1198-202
CrossRef
Google scholar
|
[9] |
Fan GJ, Wang X, Wu CE, Pan HM, Yang JT, et al. Effect of heating on the content and composition of ginkgolic acids in ginkgo seeds Quality Assurance and Safety of Crops & Foods. 2017, 9 2 195-99
CrossRef
Google scholar
|
[10] |
Lim HB, Kim DH. Effects of roasting conditions on physicochemical properties and antioxidant activities in Ginkgo bilobaseeds Food Science and Biotechnology. 2018, 27 4 1057-66
CrossRef
Google scholar
|
[11] |
Liu J, Chen J, Ye S, Ding Y, Guo S, et al. Inhibitory action of ginkgolic acid against pathogenic fungi and characterisation of its inhibitory activities on Nigrospora oryzae Folia Horticulturae. 2023, 35, 49-59
CrossRef
Google scholar
|
[12] |
Wang Y, Tao Y, Zhang X, Shao S, Han Y, et al. Metabolic profile of ginkgo kernel juice fermented with lactic aicd bacteria: A potential way to degrade ginkgolic acids and enrich terpene lactones and phenolics Process Biochemistry. 2019, 76, 25-33
CrossRef
Google scholar
|
[13] |
Hathout AS, Aly SE. Biological detoxification of mycotoxins: a review Annals of Microbiology. 2014, 64 3 905-19
CrossRef
Google scholar
|
[14] |
Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P. The biosynthesis and functionality of the cell-wall of lactic acid bacteria Antonie van Leeuwenhoek. 1999, 76, 159-84
CrossRef
Google scholar
|
[15] |
Bueno DJ, Casale CH, Pizzolitto RP, Salvano MA, Oliver G. Physical adsorption of aflatoxin B 1 by lactic acid bacteria and Saccharomyces cerevisiae: A theoretical model Journal of Food Protection. 2007, 70, 2148-54
CrossRef
Google scholar
|
[16] |
Ge N, Xu J, Peng B, Pan S. Adsorption mechanism of tenuazonic acid using inactivated lactic acid bacteria Food Control. 2017, 82, 274-82
CrossRef
Google scholar
|
[17] |
Zhang W, Zou M, Wu R, Jiang H, Cao F, et al. Efficient removal of ginkgotoxin from Ginkgo bilob a seed powder by combining endogenous enzymatic hydrolysis with resin adsorption Journal of the Science of Food and Agriculture. 2021, 101, 1589-97
CrossRef
Google scholar
|
[18] |
Kou Z, Wang C. Preparation of polyhydroxyl adsorbent and its application in the removal of Ginkgolic acids Industrial Crops and Products. 2022, 184, 114998
CrossRef
Google scholar
|
[19] |
Estevinho L, Paula AP, Moreira L, Dias LG, Pereira E. Antioxidant and antimicrobial effects of phenolic compounds extracts of Northeast Portugal honey Food and Chemical Toxicology. 2008, 46, 3774-79
CrossRef
Google scholar
|
[20] |
Li S, Tao Y, Li D, Wen G, Zhou J, et al. Fermentation of blueberry juices using autochthonous lactic acid bacteria isolated from fruit environment: Fermentation characteristics and evolution of phenolic profiles Chemosphere. 2021, 276 1 130090
CrossRef
Google scholar
|
[21] |
Wu Y, Han Y, Tao Y, Fan S, Chu D, et al. Ultrasound assisted adsorption and desorption of blueberry anthocyanins using macroporous resins Ultrasonics Sonochemistry. 2018, 48, 311-20
CrossRef
Google scholar
|
[22] |
Balestra GM, Misaghi IJ. Increasing the efficiency of the plate counting method for estimating bacterial diversity Journal of Microbiological Methods. 1997, 30 2 111-17
CrossRef
Google scholar
|
[23] |
Wu Y, Li S, Tao Y, Li D, Han Y, et al. Fermentation of blueberry and blackberry juices using Lactobacillus plantarum, Streptococcus thermophilus and Bifidobacterium bifidum: Growth of probiotics, metabolism of phenolics, antioxidant capacity in vitro and sensory evaluation Food Chemistry. 2021, 348, 129083
CrossRef
Google scholar
|
[24] |
Gong W, Zhao X, Manickam S, Liu X, Li D, et al. Impact of cell wall adsorption behaviours on phenolic stability under air drying of blackberry with and without contact ultrasound assistance Food Hydrocolloids. 2023, 137 1 108312
CrossRef
Google scholar
|
[25] |
Zou M, Zhang W, Wu R, Jiang H, Cao F, et al. Removal of ginkgotoxin from the Ginkgo biloba seeds powder by adopting membrane separation technology Journal of Cleaner Production. 2021, 280, 124452
CrossRef
Google scholar
|
[26] |
Wu Y, Han Y, Tao Y, Li D, Xie G, et al. In vitro gastrointestinal digestion and fecal fermentation reveal the effect of different encapsulation materials on the release, degradation and modulation of gut microbiota of blueberry anthocyanin extract Food Research International. 2020, 132, 109098
CrossRef
Google scholar
|
[27] |
Tao Y, Wu P, Dai Y, Luo X, Manickam S, et al. Bridge between mass transfer behavior and properties of bubbles under two-stage ultrasound-assisted physisorption of polyphenols using macroporous resin Chemical Engineering Journal. 2022, 436 1 135158
CrossRef
Google scholar
|
[28] |
Franco DSP, Vieillard J, Salau NPG, Dotto GL. Interpretations on the mechanism of In(III) adsorption onto chitosan and chitin: A mass transfer model approach Journal of Molecular Liquids. 2020, 304, 112758
CrossRef
Google scholar
|
[29] |
Leyva-Ramos R, Geankoplis CJ. Model simulation and analysis of surface diffusion of liquids in porous solids Chemical Engineering Science. 1985, 40, 799-807
CrossRef
Google scholar
|
[30] |
Ocampo-Perez R, Leyva-Ramos R, Alonso-Davila P, Rivera-Utrilla J, Sánchez-Polo M. Modeling adsorption rate of pyridine onto granular activated carbon Chemical Engineering Journal. 2010, 165, 133-41
CrossRef
Google scholar
|
[31] |
Leyva-Ramos R, Ocampo-Perez R, Mendoza-Barron J. External mass transfer and hindered diffusion of organic compounds in the adsorption on activated carbon cloth Chemical Engineering Journal. 2012, 183, 141-51
CrossRef
Google scholar
|
[32] |
Podstawczyk D, Witek-Krowiak A. Novel nanoparticles modified composite eco-adsorbents—a deep insight into kinetics modelling using numerical surface diffusion and artificial neural network models Chemical Engineering Research and Design. 2016, 109, 1-17
CrossRef
Google scholar
|
[33] |
Pauletto PS, Moreno-Pérez J, Hernández-Hernández LE, Bonilla-Petriciolet A, Dotto GL, et al. Novel biochar and hydrochar for the adsorption of 2-nitrophenol from aqueous solutions: An approach using the PVSDM model Chemosphere. 2021, 269, 128748
CrossRef
Google scholar
|
[34] |
Fröhlich AC, Ocampo-Pérez R, Diaz-Blancas V, Salau NPG, Dotto GL. Three dimensional mass transfer modeling of ibuprofen adsorption on activated carbon prepared by sonication Chemical Engineering Journal. 2018, 341, 65-74
CrossRef
Google scholar
|
[35] |
Ocampo-Pérez R, Rivera-Utrilla J, Gómez-Pacheco C, Sánchez-Polo M, López-Peñalver JJ. Kinetic study of tetracycline adsorption on sludge-derived adsorbents in aqueous phase Chemical Engineering Journal. 2012, 213, 88-96
CrossRef
Google scholar
|
[36] |
Valderrama C, Gamisans X, De las Heras X, Farrán A, Cortina JL. Sorption kinetics of polycyclic aromatic hydrocarbons removal using granular activated carbon: intraparticle diffusion coefficients Journal of Hazardous Materials. 2008, 157, 386-96
CrossRef
Google scholar
|
[37] |
Wilke CR, Chang P. Correlation of diffusion coefficients in dilute solutions AIChE Journal. 1955, 1, 264-70
CrossRef
Google scholar
|
[38] |
Furusawa T, Smith JM. Fluid-particle and intraparticle mass transport rates in slurries Industrial & Engineering Chemistry Fundamentals. 1973, 12, 197-203
CrossRef
Google scholar
|
[39] |
Tao Y, Wu Y, Han Y, Chemat F, Li D, et al. Insight into mass transfer during ultrasound-enhanced adsorption/desorption of blueberry anthocyanins on macroporous resins by numerical simulation considering ultrasonic influence on resin properties Chemical Engineering Journal. 2020, 380 1 122530
CrossRef
Google scholar
|
[40] |
Souza PR, Dotto GL, Salau NPG. Detailed numerical solution of pore volume and surface diffusion model in adsorption systems Chemical Engineering Research and Design. 2017, 122, 298-307
CrossRef
Google scholar
|
[41] |
Xia Y, DeBolt S, Dreyer J, Scott D, Williams MA. Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices Frontiers in Plant Science. 2015, 6, 490
CrossRef
Google scholar
|
[42] |
Liao W, Shen J, Manickam S, Li S, Tao Y, et al. Investigation of blueberry juice fermentation by mixed probiotic strains: Regression modeling, machine learning optimization and comparison with fermentation by single strain in the phenolic and volatile profiles Food Chemistry. 2023, 405, 134982
CrossRef
Google scholar
|
[43] |
Park JJ, Lee WY. Adsorption and desorption characteristics of a phenolic compound from Ecklonia cava on macroporous resin Food Chemistry. 2021, 338, 128150
CrossRef
Google scholar
|
[44] |
Zhou G, Ma J, Tang Y, Wang X, Zhang J, et al. Multi-response optimization of ultrasonic assisted enzymatic extraction followed by macroporous resin purification for maximal recovery of flavonoids and ginkgolides from waste Ginkgo biloba fallen leaves Molecules. 2018, 23, 1029
CrossRef
Google scholar
|
[45] |
Boateng ID. A critical review of ginkgolic acids in Ginkgo biloba leaf extract (EGb): toxicity and technologies to remove ginkgolic acids and their promising bioactivities Food & Function. 2022, 18, 9226-42
CrossRef
Google scholar
|
[46] |
Qian Y, Peng Y, Shang E, Zhao M, Yan L, et al. Metabolic profiling of the hepatotoxicity and nephrotoxicity of Ginkgolic acids in rats using ultra-performance liquid chromatography-high-definition mass spectrometry Chemico-Biological Interactions. 2017, 273, 11-17
CrossRef
Google scholar
|
[47] |
Chinese Association of Integrative Medicine, Chinese Medical Doctor Association, National Clinical Research Center for Chinese Medicine Cardiology, Cardiovascular Disease Working Group, Encephalopathy Disease Working Group, et al. Chinese expert consensus on clinical application of oral Ginkgo biloba preparations (2020) Chinese Journal of Integrative Medicine. 2021, 27 3 163-69
CrossRef
Google scholar
|
[48] |
[49] |
[50] |
Dong Q, Cao J, Wu R, Shi T, Zhang W, et al. Efficient removal of ginkgolic acids from Ginkgo biloba leaves crude extract by using hydrophobic deep eutectic solvents Industrial Crops and Products. 2021, 166, 113462
CrossRef
Google scholar
|
[51] |
Hong SJ, Jang JA, Hwang H, Cho MS. Changes in 4'- O-methylpyridoxine (ginkgotoxin) and antioxidant activity in ginkgo biloba seeds in different cooking conditions Korean Journal of Food Science and Technology. 2017, 49 5 532-37
CrossRef
Google scholar
|
[52] |
Zou M, Zhang W, Dong Q, Tang C, Cao F, et al. Submerged fermentation of Ginkgo biloba seed powder using Eurotium cristatum for the development of ginkgo seeds fermented products Journal of the Science of Food and Agriculture. 2021, 101 5 1782-91
CrossRef
Google scholar
|
[53] |
Leonard W, Zhang P, Ying D, Adhikari B, Fang Z. Fermentation transforms the phenolic profiles and bioactivities of plant-based foods Biotechnology advances. 2021, 49, 107763
CrossRef
Google scholar
|
[54] |
García-Ruiz A, Cueva C, González-Rompinelli EM, Yuste M, Torres M, et al. Antimicrobial phenolic extracts able to inhibit lactic acid bacteria growth and wine malolactic fermentation Food Control. 2012, 28, 212-19
CrossRef
Google scholar
|
[55] |
Gao M, Wang D, Deng L, Liu S, Zhang K, et al. High-crystallinity covalent organic framework synthesized in deep eutectic solvent: Potentially effective adsorbents alternative to macroporous resin for flavonoids Chemistry of Materials. 2021, 33, 8036-51
CrossRef
Google scholar
|
[56] |
Chen HY, Ting Y, Kuo HC, Hsieh CW, Hsu HY, et al. Enzymatic degradation of ginkgolic acids by laccase immobilized on core/shell Fe 3O 4/nylon composite nanoparticles using novel coaxial electrospraying process International Journal of Biological Macromolecules. 2021, 172, 270-80
CrossRef
Google scholar
|
[57] |
Boateng ID, Yang XM, Li YY. Optimization of infrared-drying parameters for Ginkgo biloba L. seed and evaluation of product quality and bioactivity Industrial Crops and Products. 2021, 160, 113108
CrossRef
Google scholar
|
[58] |
Amiri S, Mokarram RR, Khiabani MS, Bari MR, Alizadeh M. Optimization of food-grade medium for co-production of bioactive substances by Lactobacillus acidophilus LA-5 for explaining pharmabiotic mechanisms of probiotic Journal of Food Science and Technology. 2021, 58, 1-12
CrossRef
Google scholar
|
[59] |
Wang WQ, Zhang JL, Yu Q, Zhou JY, Lu ML, et al. Structural and compositional changes of whey protein and blueberry juice fermented using Lactobacillus plantarum or Lactobacillus casei during fermentation RSC Advances. 2021, 11, 26291-302
CrossRef
Google scholar
|
[60] |
Caglar B, Cubuk O, Demir E, Coldur F, Catir M, et al. Characterization of AlFe-pillared Unye bentonite: a study of the surface acidity and catalytic property Journal of Molecular Structure. 2015, 1089, 59-65
CrossRef
Google scholar
|
[61] |
Hernández-Padilla ES, Zárate-Guzmán AI, González-Ortega O, Padilla-Ortega E, Gómez-Durán A, et al. Elucidation of adsorption mechanisms and mass transfer controlling resistances during single and binary adsorption of caffeic and chlorogenic acids Environmental Science and Pollution Research. 2022, 29, 26297-311
CrossRef
Google scholar
|
[62] |
Ocampo-Pérez R, Leyva-Ramos R, Sanchez-Polo M, Rivera-Utrilla J. Role of pore volume and surface diffusion in the adsorption of aromatic compounds on activated carbon Adsorption. 2013, 19, 945-57
CrossRef
Google scholar
|
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