Abstract
The study aimed to determine the antioxidant activities and phenolic compounds of Bambangan (Mangifera pajang), a type of wild fruit belongs to the family of Anacardiaceae during fermentation at room (28 °C) and elevated temperature (35 °C). The antioxidant capacity was estimated based on 2,2-diphenyl-1-picyrlhydrazyl (DPPH) scavenging activity, ferric-ion-reducing power (FRAP), 2,2´-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) radical cation assay and oxygen-radical absorbing capacity (ORAC). A reversed phase high performance liquid chromatography (HPLC) was used to identify the phenolic compounds. Samples of bambangan fermented at 35 °C achieved the highest FRAP (141.42 mM Fe(II)/g extract) and ABTS values (5.00 mmol TE/g) within the first six days as compared to the samples fermented at room temperature (28 °C), which required 10 days to achieve the highest FRAP and ABTS values. No significant difference was found (p > 0.05) on the antioxidant activity of the samples that were kept at prolonged fermentation and storage. The total phenolic content (TPC) increased throughout the fermentation with the highest value of 44.69 \(\pm\) 0.01 mg GAE/g. Gallic acid, chlorogenic acid, vanillin, \(\rho\)-coumaric acid and rutin are the major phenolic compounds identified in the fermented product. The results suggested that the antioxidant capacity of bambangan is affected by the fermentation temperature and the fermented product could be a source of antioxidants.

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Abbreviations
- DPPH:
-
2,2-Diphenyl-2-picrylhydrazyl
- TPTZ:
-
2,4,6-Tripyridyl-s- triazine
- AAPH:
-
2,2’-Azobis(2-amidinopropane) dihydrochloride
- Trolox:
-
2,5,7,8-Tetramethychroman-2-carboxylic acid
- BHA:
-
Butylated hydroxy anisole
- EC50 :
-
Effective concentration providing 50% radical scavenging activity
- RSA:
-
Radical scavenging activity
- ORAC:
-
Oxygen-radical absorbing capacity
- HPLC:
-
High performance liquid chromatography
- DAD:
-
Diode array detector
- UV:
-
Ultraviolet
- DW:
-
Dry weight
- GAE:
-
Gallic acid equivalent
- SPSS:
-
Statistical Package for Social Science
- ANOVA:
-
One-way analysis of variance
- SD:
-
Standard deviation
References
Adwas AA, Elsayed ASI, Azab AE, Quwaydir FA (2019) Oxidative stress and antioxidant mechanisms in human body. J Appl Biotechnol Bioeng 6(1):43–47
Alexandraki V, Georgalaki M, Papadimitriou K, Anastasiou R, Zoumpopoulou G, Chatzipavlidis I et al (2014) Determination of triterpenic acids in natural and alkaline-treated Greek table olives throughout the fermentation process. LWT Food Sci Technol 58(2):609–613
Bhanja Dey T, Chakraborty S, Jain KK, Sharma A, Kuhad RC (2016) Antioxidant phenolics and their microbial production by submerged and solid-state fermentation process: A review. Trends Food Sci Technol 53:60–74
Bock C, Ternes W (2010) The phenolic acids from bacterial degradation of the mangiferin aglycone are quantified in the feces of pigs after oral ingestion of an extract of Cyclopia genistoides (honeybush tea). Nutr Res 30(5):348–357
Bravo-Ferrada BM, Hollmann A, Brizuela NL, Hens DV, Tymczyszyn E, Semorile L (2016) Growth and consumption of l-malic acid in wine-like medium by acclimated and non-acclimated cultures of Patagonian Oenococcus oeni strains. Folia Microbiol 61(5):365–373
Cecchi L, Migliorini M, Cherubini C, Giusti M, Zanoni B, Innocenti M, Mulinacci N (2013) Phenolic profiles, oil amount and sugar content during olive ripening of three typical Tuscan cultivars to detect the best harvesting time for oil production. Food Res Intern 54(2):1876–1884
Chen C, Zhang Y, Gao Y, Xu Q, Ju X, Wang L (2016) Identification and anti-tumour activities of phenolic compounds isolated from defatted adlay (Coix lachryma-jobi L. var. ma-yuen Stapf) seed meal. J Funct Foods 26:394–405
Choo KY, Kho C, Ong YY, Thoo YY, Lim RLH, Tan CP, Ho CW (2018) Studies on the storage stability of fermented red dragon fruit (Hylocereus polyrhizus) drink. Food Sci Biotechnol 27:1411–1417
Cvetković BR, Pezo LL, Tasić T, Šarić L, Kevrešan Ž, Mastilović J (2015) The optimisation of traditional fermentation process of white cabbage (in relation to biogenic amines and polyamines content and microbiological profile). Food Chem 168:471–477
Deʇirmencioʇlu N, Gürbüz O, Herken EN, Yildiz AY (2016) The impact of drying techniques on phenolic compound, total phenolic content and antioxidant capacity of oat flour tarhana. Food Chem 194:587–594
Filannino P, Bai Y, Di Cagno R, Gobbetti M, Gänzle MG (2015) Metabolism of phenolic compounds by Lactobacillus spp. during fermentation of cherry juice and broccoli puree. Food Microbiol 46:272–279
Fritsch C, Heinrich V, Vogel RF, Toelstede S (2016) Phenolic acid degradation potential and growth behavior of lactic acid bacteria in sunflower substrates. Food Microbiol 57:178–186
Gagné MJ, Barrette J, Savard T, Brassard J (2015) Evaluation of survival of murine norovirus-1 during sauerkraut fermentation and storage under standard and low-sodium conditions. Food Microbiol 52:119–123
Gao H, Wen JJ, Hu JL, Nie QX, Chen HH, Nie SP, Xiong T, Xie MY (2019) Momordica charantia juice with Lactobacillus plantarum fermentation: chemical composition, antioxidant properties and aroma profile. Food Biosci 29:62–72
Hassan FA, Ismail A, Abdulhamid A, Azlan A (2011) Identification and quantification of phenolic compounds in bambangan (Mangifera pajang Kort.) peels and their free radical scavenging activity. J Agric Food Chem 59(17):9102–9111
Hoyos-Arbeláez J, Vázquez M, Contreras-Calderón J (2017) Electrochemical methods as a tool for determining the antioxidant capacity of food and beverages: a review. Food Chem 221:1371–1381
Hur SJ, Lee SY, Kim YC, Choi I, Kim GB (2014) Effect of fermentation on the antioxidant activity in plant-based foods. Food Chem 160:346–356
Jahurul MHA, Leykey B, Sharifudin MS et al (2018) Optimization of fat yield of bambangan (Mangifera pajang) kernel using response surface methodology and its antioxidant activities. Food Measure 12:1427–1438
Jaiswal AK, Abu-Ghannam N (2013) Kinetic studies for the preparation of probiotic cabbage juice: Impact on phytochemicals and bioactivity. Ind Crops Prod 50:212–218
Jutiviboonsuk A, Leeprechanon W (2019) Stability of Mangiferin in lotion and its Antioxidant Activity. Key Eng Mater 819:79–84
Kaur B, Chakraborty D, Kumar B (2013) Phenolic Biotransformations during conversion of ferulic acid to vanillin by lactic acid bacteria. Biomed Res Int 2013:e590359
Khurana RK, Bansal AK, Beg S, Burrow AJ, Katare OP, Singh KK, Singh B (2017) Enhancing biopharmaceutical attributes of phospholipid complex-loaded nanostructured lipidic carriers of mangiferin: systematic development, characterization and evaluation. Int J of Pharm 518(1-2):289–306
Kiai H, Hafidi A (2014) Chemical composition changes in four green olive cultivars during spontaneous fermentation. LWT - Food Sci Technol 57(2):663–670
Kitaoka N, Nomura T, Ogita S, Kato Y (2021) Bioproduction of 4-vinylphenol and 4-vinylguaiacol β-primeverosides using transformed bamboo cells expressing bacterial phenolic acid decarboxylase. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-021-03522-y
Knockaert D, Raes K, Struijs K, Wille C, Van Camp J (2014) Influence of microbial conversion and change in pH on iron-gallic acid complexation during lactobacillus fermentation. LWT Food Sci Technol 55(1):335–340
Kong KW, Khoo HE, Prasad NK, Chew LY, Amin I (2013) Total phenolics and antioxidant activities of pouteria campechiana fruit parts. Sains Malaysiana 42(2):123–127
Kumar N, Pruthi V (2014) Potential applications of ferulic acid from natural sources. Biotechnol Rep 4(1):86–93
Li T, Jiang T, Liu N, Wu C, Xu H, Lei H (2021) Biotransformation of phenolic profiles and improvement of antioxidant capacities in jujube juice by select lactic acid bacteria. Food Chem 339(1):127859
Ling JKU, Chan YS, Nandong J (2020) Extraction of antioxidant compounds from the wastes of Mangifera pajang fruit: a comparative study using aqueous ethanol and deep eutectic solvent. SN Appl Sci 2(8):1365
Liu S, Chang X, Liu X, Shen Z (2016) Effects of pretreatments on anthocyanin composition, phenolics contents and antioxidant capacities during fermentation of hawthorn (Crataegus pinnatifida) drink. Food Chem 212:87–95
Liu A, Li X, Pu B, Ao X, Zhou K, He L, Chen S, Liu S (2017) Use of psychrotolerant lactic acid bacteria (Lactobacillus spp. and Leuconostoc spp.) isolated from chinese traditional paocai for the quality improvement of paocai products. J Agric Food Chem 65(12):2580–2587
Liu Z, Ren Z, Zhang J, Chuang C-C, Kandaswamy E, Zhou T, Zuo L (2018) Role of ROS and nutritional antioxidants in human diseases. Front Physiol 9:477
Mantzourani I, Kazakos S, Terpou A, Alexopoulos A, Bezirtzoglou E, Bekatorou A, Plessas S (2018a) potential of the probiotic Lactobacillus plantarum ATCC 14917 strain to produce functional fermented pomegranate juice. Foods 8(1):4
Mantzourani I, Kazakos S, Terpou A, Mallouchos A, Kimbaris A, Alexopoulos A, Bezirtzoglou E, Plessas S (2018b) Assessment of volatile compounds evolution, antioxidant activity, and total phenolics content during cold storage of pomegranate beverage fermented by Lactobacillus paracasei K5. Fermentation 4(4):95
Mirfat AHS, Salma I, Razali M (2016) Natural antioxidant properties of selected wild Mangifera species in Malaysia. J Trop Agric Food Sci 44(1):63–72
Molaveisi M, Beigbabaei A, Akbari E, Noghabi MS, Mohamadi M (2019) Kinetics of temperature effect on antioxidant activity, phenolic compounds and color of Iranian jujube honey. Heliyon 5(1):e01129
Nemec MJ, Kim H, Marciante AB, Barnes RC, Hendrick ED, Bisson WH et al (2017) Polyphenolics from mango (Mangifera indica L.) suppress breast cancer ductal carcinoma in situ proliferation through activation of AMPK pathway and suppression of mTOR in athymic nude mice. J Nutr Biochem 41:12–19
Ng SY, Koon SS, Padam BS, Chye FY (2015) Evaluation of probiotic potential of lactic acid bacteria isolated from traditional Malaysian fermented Bambangan (Mangifera pajang). CYTA J Food 13(4):563–572
Nile SH, Nile AS, Keum YS (2017) Total phenolics, antioxidant, antitumor, and enzyme inhibitory activity of Indian medicinal and aromatic plants extracted with different extraction methods. Biotech 7(1):76
Okcu G, Ayhan K, Gunes Altuntas E, Vural N, Poyrazoglu ES (2016) Determination of phenolic acid decarboxylase produced by lactic acid bacteria isolated from shalgam (şalgam) juice using green analytical chemistry method. LWT Food Sci Technol 66:615–621
Padh H, Parmar S, Patel B (2017) Stability indicating HPTLC method for estimation of mangiferin in bulk and dosage form. Int J Pharma Bio Sci 7(3):71–77
Pang Y, Ahmed S, Xu Y, Beta T, Zhu Z, Shao Y, Bao J (2018) Bound phenolic compounds and antioxidant properties of whole grain and bran of white, red and black rice. Food Chem 240:212–221
Pérez-Martín F, Seseña S, Izquierdo PM, Palop ML (2013) Esterase activity of lactic acid bacteria isolated from malolactic fermentation of red wines. Int J Food Microbiol 163(2–3):153–158
Pinsirodom P, Taprap R, Parinyapatthanaboot T (2018) Antioxidant activity and phenolic acid composition in different parts of selected cultivars of mangoes in Thailand. Int Food Res J 25(4):1435–1443
Qu F, Zeng W, Tong X, Feng W, Chen Y, Ni D (2020) The new insight into the influence of fermentation temperature on quality and bioactivities of black tea. LWT 117:108646
Queiroz Santos VA, Nascimento CG, Schmidt CAP, Mantovani D, Dekker RFH, da Cunha MAA (2018) Solid-state fermentation of soybean okara : Isoflavones biotransformation, antioxidant activity and enhancement of nutritional quality. LW 92:509515
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26(9–10):1231–1237
Rochín-Medina JJ, Ramírez K, Rangel-Peraza JG et al (2018) Increase of content and bioactivity of total phenolic compounds from spent coffee grounds through solid state fermentation by Bacillus clausii. J Food Sci Technol 55:915–923
Salgado JM, Rodríguez-Solana R, Curiel JA, de las Rivas B, Muñoz R, Domínguez JM (2012) Production of vinyl derivatives from alkaline hydrolysates of corn cobs by recombinant Escherichia coli containing the phenolic acid decarboxylase from Lactobacillus plantarum CECT 748T. Bioresour Technol 117:274–285
Sarwar S, Anwar F, Raziq S, Nadeem M, Zreen Z, Cecil F (2012) Antioxidant characteristics of different solvent extracts from almond (Prunus dulcis L.) shell. J Med Plants Res 6:3311–3316
Schaich KM, Tian X, Xie J (2015) Hurdles and pitfalls in measuring antioxidant efficacy: a critical evaluation of ABTS, DPPH, and ORAC assays. J Funct Foods 14:111–125
Shalaby E, Shanab SMM (2013) Antioxidant compounds, assays of determination and mode of action. Afr J Pharma Phamacol 7(10):528–539
Shao P, Zhang J, Fang Z, Sun P (2014) Complexing of chlorogenic acid with β-cyclodextrins: Inclusion effects, antioxidative properties and potential application in grape juice. Food Hydrocoll 41:132–139
Shin HS, Satsu H, Bae MJ, Zhao Z, Ogiwara H, Totsuka M, Shimizu M (2015) Anti-inflammatory effect of chlorogenic acid on the IL-8 production in Caco-2 cells and the dextran sulphate sodium-induced colitis symptoms in C57BL/6 mice. Food Chem 168:167–175
Tabaszewska M, Gabor A, Jaworska G, Drożdż I (2018) Effect of fermentation and storage on the nutritional value and contents of biologically—active compounds in lacto-fermented white asparagus (Asparagus officinalis L.). LWT 92:67–72
Wang CY, Wu SJ, Shyu YT (2014) Antioxidant properties of certain cereals as affected by food-grade bacteria fermentation. J Biosci Bioeng 117(4):449–456
Wang Y, He L, Xing Y, Zhou W, Pian R, Yang F, Chen X, Zhang Q (2019) Bacterial diversity and fermentation quality of Moringa oleifera leaves silage prepared with lactic acid bacteria inoculants and stored at different temperatures. Bioresour Technol 284:349–358
Wiczkowski W, Szawara-Nowak D, Topolska J (2015) Changes in the content and composition of anthocyanins in red cabbage and its antioxidant capacity during fermentation, storage and stewing. Food Chem 167:115–123
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 Microbiol 33(2):185–196
Xiao Y, Wang L, Rui X, Li W, Chen X, Jiang M, Dong M (2015) Enhancement of the antioxidant capacity of soy whey by fermentation with Lactobacillus plantarum B1–6. J Funct Foods 12:33–44
Xu D, Li Y, Meng X, Zhou T, Zhou Y, Zheng J, Zhang J (2017) Natural antioxidants in foods and medicinal plants: extraction, assessment and resources. Int J Mol Sci 18(1):96
Yang W, Tang H, Ni J, Wu Q, Hua D, Tao F, Xu P, Janssen PJ (2013) Characterization of two streptomyces enzymes that convert ferulic acid to vanillin. PLoS ONE 8(6):e67339
Yao J, Guo GS, Ren GH, Liu YH (2014) Production, characterization and applications of tannase. J Mol Catal B Enzym 101:137–147
Zou B, Wu J, Yu Y et al (2017) Evolution of the antioxidant capacity and phenolic contents of persimmon during fermentation. Food Sci Biotechnol 26:563–571
Acknowledgements
This work was financial supported by Seaweed Research Unit, Universiti Malaysia Sabah (Project Number: GPRL 006). The authors also gratefully acknowledge Mr. Chin from Penampang, Kota Kinabalu, Sabah, for providing samples of fermented bambangan used in the study.
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STC carried out the experiments, analyzed data and preparing the draft; BSP analyzed data and corrected the draft; FYC supervised the work and edited the manuscript.
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Chan, S.T., Padam, B.S. & Chye, F.Y. Effect of fermentation on the antioxidant properties and phenolic compounds of Bambangan (Mangifera pajang) fruit. J Food Sci Technol 60, 303–314 (2023). https://doi.org/10.1007/s13197-022-05615-w
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DOI: https://doi.org/10.1007/s13197-022-05615-w