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Valorization of spinach roots for recovery of phenolic compounds by ultrasound-assisted extraction: characterization, optimization, and bioaccessibility

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Abstract

In this study, the total phenolic content (TPC), the total flavonoid content (TFC), antioxidant activity (TAA), phenolic compounds composition with liquid chromatography–tandem mass spectrometry (LC–MS/MS), and mineral compounds composition with inductively coupled plasma mass spectrometry (ICP-MS) of spinach roots were determined. In addition, the aim of the study was to obtain bioactive components from spinach roots by ultrasound-assisted extraction method. Ultrasound-assisted extraction was performed with a probe-type ultrasonic homogenizer, and extraction variables were determined as amplitude (25–55%), temperature (10–30 °C), time (3–5 min), and ethanol concentration (20–60%). The process conditions were optimized using the response surface method and a central composite design. The effects of extraction variables on the TPC, TFC, and TAA of spinach roots were investigated in the optimization process. The maximum amount of phenolic compound, flavonoid compound, and antioxidant activity were determined as 5579.51 mg GAE kg−1 LW, 1824.34 mg CE kg−1 LW, and 20.79 mmol TE kg−1 LW under the optimum extraction conditions of time (3 min), temperature (10 °C), amplitude (55%), and ethanol concentration (20%). The predictive capabilities of the proposed quadratic polynomial models were found to be sufficient as the experimental and predicted data were consistent with each other. The ultrasound-assisted extraction improved the bioaccessibility of phenolic compounds spinach roots in the stomach. The ultrasound-assisted extraction can be considered as an efficient, green, and practical technique for recovering bioactive components from spinach roots.

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Data availability

The data were obtained during Research Projects supported by Trakya University (TUBAP, Grant No. 2021/102). The authors declare that the data supporting the findings of this study are available within the article files, and if necessary, the data files can be presented by the corresponding author.

References

  1. De Laurentiis V, Corrado S, Sala S (2018) Quantifying household waste of fresh fruit and vegetables in the EU. Waste Manag 77:238–251

    Article  PubMed  Google Scholar 

  2. Dos Santos SF, Cardoso RDCV, Borges ÍMP, e Almeida AC, Andrade ES, Ferreira IO, do Carmo Ramos L (2020) Post-harvest losses of fruits and vegetables in supply centers in Salvador, Brazil: analysis of determinants, volumes and reduction strategies. Waste Manag 101:161–170

  3. Nanda S, Reddy SN, Hunter HN, Dalai AK, Kozinski JA (2015) Supercritical water gasification of fructose as a model compound for waste fruits and vegetables. J Supercrit Fluids 104:112–121

    Article  CAS  Google Scholar 

  4. Raak N, Symmank C, Zahn S, Aschemann-Witzel J, Rohm H (2017) Processing-and product-related causes for food waste and implications for the food supply chain. Waste Manag 61:461–472

    Article  PubMed  Google Scholar 

  5. Díaz AI, Laca A, Laca A, Díaz M (2017) Treatment of supermarket vegetable wastes to be used as alternative substrates in bioprocesses. Waste Manag 67:59–66

    Article  PubMed  Google Scholar 

  6. Jiménez-Moreno N, Esparza I, Bimbela F, Gandía LM, Ancín-Azpilicueta C (2020) Valorization of selected fruit and vegetable wastes as bioactive compounds: opportunities and challenges. Crit Rev Environ Sci Technol 50(20):2061–2108

    Article  Google Scholar 

  7. De Corato U (2019) The market of the minimally processed fresh produce needs of safer strategies for improving shelf life and quality: a critical overview of the traditional technologies. Open Access J Agric Res 4(1):23

    Google Scholar 

  8. Ragaert P, Verbeke W, Devlieghere F, Debevere J (2004) Consumer perception and choice of minimally processed vegetables and packaged fruits. Food Qual Prefer 15(3):259–270

    Article  Google Scholar 

  9. Saini RK, Ko EY, Keum Y-S (2017) Minimally processed ready-to-eat baby-leaf vegetables: Production, processing, storage, microbial safety, and nutritional potential. Food Rev Intl 33(6):644–663

    Article  CAS  Google Scholar 

  10. El-Sayed SM (2020) Use of spinach powder as functional ingredient in the manufacture of UF-Soft cheese. Heliyon 6(1):e03278

    Article  PubMed  PubMed Central  Google Scholar 

  11. Derrien M, Aghabararnejad M, Gosselin A, Desjardins Y, Angers P, Boumghar Y (2018) Optimization of supercritical carbon dioxide extraction of lutein and chlorophyll from spinach by-products using response surface methodology. LWT 93:79–87

    Article  CAS  Google Scholar 

  12. Mola ID, Ottaiano L, Cozzolino E, Sabatino L, Sifola MI, Mormile P, El-Nakhel C, Rouphael Y, Mori M (2021) Optical characteristics of greenhouse plastic films affect yield and some quality traits of spinach (Spinacia oleracea L.) subjected to different nitrogen doses. Horticulturae 7(7):200

  13. Howard L, Pandjaitan N (2008) Pressurized liquid extraction of flavonoids from spinach. J Food Sci 73(3):C151–C157

    Article  CAS  PubMed  Google Scholar 

  14. Anticona M, Blesa J, Lopez-Malo D, Frigola A, Esteve MJ (2021) Effects of ultrasound-assisted extraction on physicochemical properties, bioactive compounds, and antioxidant capacity for the valorization of hybrid Mandarin peels. Food Biosci 42:101185

    Article  CAS  Google Scholar 

  15. Vinatoru M, Mason T, Calinescu I (2017) Ultrasonically assisted extraction (UAE) and microwave assisted extraction (MAE) of functional compounds from plant materials. TrAC Trends Anal Chem 97:159–178

    Article  CAS  Google Scholar 

  16. Chemat F, Khan MK (2011) Applications of ultrasound in food technology: processing, preservation and extraction. Ultrason Sonochem 18(4):813–835

    Article  CAS  PubMed  Google Scholar 

  17. Chemat F, Rombaut N, Sicaire A-G, Meullemiestre A, Fabiano-Tixier A-S, Abert-Vian M (2017) Ultrasound assisted extraction of food and natural products. Mechanisms, techniques, combinations, protocols and applications. A review. Ultrasonics Sonochem 34:540–560

    Article  CAS  Google Scholar 

  18. Shekarchizadeh H, Kadivar M, Ghaziaskar HS, Rezayat M (2009) Optimization of enzymatic synthesis of cocoa butter analog from camel hump fat in supercritical carbon dioxide by response surface method (RSM). J Supercrit Fluids 49(2):209–215

    Article  CAS  Google Scholar 

  19. Espada-Bellido E, Ferreiro-González M, Carrera C, Palma M, Barroso CG, Barbero GF (2017) Optimization of the ultrasound-assisted extraction of anthocyanins and total phenolic compounds in mulberry (Morus nigra) pulp. Food Chem 219:23–32

    Article  CAS  PubMed  Google Scholar 

  20. He B, Zhang L-L, Yue X-Y, Liang J, Jiang J, Gao X-L, Yue P-X (2016) Optimization of ultrasound-assisted extraction of phenolic compounds and anthocyanins from blueberry (Vaccinium ashei) wine pomace. Food Chem 204:70–76

    Article  CAS  PubMed  Google Scholar 

  21. Milella RA, Basile T, Alba V, Gasparro M, Giannandrea MA, Debiase G, Genghi R, Antonacci D (2019) Optimized ultrasonic-assisted extraction of phenolic antioxidants from grape (Vitis vinifera L.) skin using response surface methodology. J Food Sci Technol 56(10):4417–4428

  22. Bayram NE, Canli D, Gercek YC, Bayram S, Celik S, Güzel F, Morgil H, Oz GC (2020) Macronutrient and micronutrient levels and phenolic compound characteristics of monofloral honey samples. J Food Nutr Res 59(4):1

    Google Scholar 

  23. Shahidi F, Chavan U, Naczk M, Amarowicz R (2001) Nutrient distribution and phenolic antioxidants in air-classified fractions of beach pea (Lathyrus maritimus L.). J Agric Food Chemi 49(2):926–933

  24. Wannes WA, Mhamdi B, Sriti J, Jemia MB, Ouchikh O, Hamdaoui G, Kchouk ME, Marzouk B (2010) Antioxidant activities of the essential oils and methanol extracts from myrtle (Myrtus communis var. italica L.) leaf, stem and flower. Food Chem Toxicol 48(5):1362–1370

  25. 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 Radical Biol Med 26(9–10):1231–1237

    Article  CAS  Google Scholar 

  26. Tiwari BK, Patras A, Brunton N, Cullen PJ, O’donnell CP (2010) Effect of ultrasound processing on anthocyanins and color of red grape juice. Ultrasonics Sonochem 17(3):598–604

  27. McDougall G, Fyffe S, Dobson P, Stewart D (2005) Anthocyanins from red wine—their stability under simulated gastrointestinal digestion. Phytochemistry 66(21):2540–2548

    Article  CAS  PubMed  Google Scholar 

  28. Bhattacharjee S, Dasgupta P, Paul AR, Ghosal S, Padhi KK, Pandey LP (1998) Mineral element composition of spinach. J Sci Food Agric 77(4):456–458

    Article  CAS  Google Scholar 

  29. Acosta-Estrada BA, Gutiérrez-Uribe JA, Serna-Saldívar SO (2014) Bound phenolics in foods, a review. Food Chem 152:46–55

    Article  CAS  PubMed  Google Scholar 

  30. Bunea A, Andjelkovic M, Socaciu C, Bobis O, Neacsu M, Verhé R, Van Camp J (2008) Total and individual carotenoids and phenolic acids content in fresh, refrigerated and processed spinach (Spinacia oleracea L.). Food Chem 108(2):649–656

  31. Zhou K, Yu L (2006) Total phenolic contents and antioxidant properties of commonly consumed vegetables grown in Colorado. LWT Food Sci Technol 39(10):1155–1162

    Article  CAS  Google Scholar 

  32. Jaime L, Vázquez E, Fornari T, López‐Hazas MDC, García‐Risco MR, Santoyo S, Reglero G (2015) Extraction of functional ingredients from spinach (Spinacia oleracea L.) using liquid solvent and supercritical CO2 extraction. J Sci Food Agric 95(4):722–729

  33. Yosefi Z, Tabaraki R, Gharneh HA, Mehrabi A (2010) Variation in antioxidant activity, total phenolics, and nitrate in spinach. Int J Veg Sci 16(3):233–242

    Article  Google Scholar 

  34. Tan SF, Masoumi HRF, Karjiban RA, Stanslas J, Kirby BP, Basri M, Basri HB (2016) Ultrasonic emulsification of parenteral valproic acid-loaded nanoemulsion with response surface methodology and evaluation of its stability. Ultrason Sonochem 29:299–308

    Article  CAS  PubMed  Google Scholar 

  35. Islam Shishir MR, Taip FS, Aziz NA, Talib RA, Hossain Sarker MS (2016) Optimization of spray drying parameters for pink guava powder using RSM. Food Sci Biotechnol 25:461–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Fumic B, Jug M, Koncic MZ (2019) Optimization of ultrasound-assisted extraction of phenolic antioxidants from lotus corniculatus. Croat Chem Acta 92(3):1H-1H

    Article  Google Scholar 

  37. Shehata MG, Abd El Aziz NM, Youssef MM, El-Sohaimy SA (2021) Optimization conditions of ultrasound-assisted extraction of phenolic compounds from orange peels using response surface methodology. J Food Process Preserv 45(10):e15870

    Article  CAS  Google Scholar 

  38. d’Alessandro LG, Kriaa K, Nikov I, Dimitrov K (2012) Ultrasound assisted extraction of polyphenols from black chokeberry. Sep Purif Technol 93:42–47

    Article  Google Scholar 

  39. Milić A, Daničić T, Tepić Horecki A, Šumić Z, Teslić N, Bursać Kovačević D, Putnik P, Pavlić B (2022) Sustainable extractions for maximizing content of antioxidant phytochemicals from black and red currants. Foods 11(3):325

    Article  PubMed  PubMed Central  Google Scholar 

  40. Doulabi M, Golmakani MT, Ansari S (2020) Evaluation and optimization of microwave-assisted extraction of bioactive compounds from eggplant peel by-product. J Food Process Preserv 44(11):e14853

    Article  CAS  Google Scholar 

  41. Dahmoune F, Nayak B, Moussi K, Remini H, Madani K (2015) Optimization of microwave-assisted extraction of polyphenols from Myrtus communis L. leaves. Food Chem 166:585–595

    Article  CAS  PubMed  Google Scholar 

  42. Lim KJA, Cabajar AA, Lobarbio CFY, Taboada EB, Lacks DJ (2019) Extraction of bioactive compounds from mango (Mangifera indica L. var. Carabao) seed kernel with ethanol–water binary solvent systems. J Food Sci Technol 56:2536–2544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Medina-Torres N, Ayora-Talavera T, Espinosa-Andrews H, Sánchez-Contreras A, Pacheco N (2017) Ultrasound assisted extraction for the recovery of phenolic compounds from vegetable sources. Agronomy 7(3):47

    Article  CAS  Google Scholar 

  44. Ilaiyaraja N, Likhith K, Babu GS, Khanum F (2015) Optimisation of extraction of bioactive compounds from Feronia limonia (wood apple) fruit using response surface methodology (RSM). Food Chem 173:348–354

    Article  CAS  PubMed  Google Scholar 

  45. Tomšik A, Pavlić B, Vladić J, Ramić M, Brindza J, Vidović S (2016) Optimization of ultrasound-assisted extraction of bioactive compounds from wild garlic (Allium ursinum L.). Ultrason Sonochem 29:502–511

    Article  PubMed  Google Scholar 

  46. Chen M, Zhao Y, Yu S (2015) Optimisation of ultrasonic-assisted extraction of phenolic compounds, antioxidants, and anthocyanins from sugar beet molasses. Food Chem 172:543–550

    Article  CAS  PubMed  Google Scholar 

  47. Ivanovic J, Tadic V, Dimitrijevic S, Stamenic M, Petrovic S, Zizovic I (2014) Antioxidant properties of the anthocyanin-containing ultrasonic extract from blackberry cultivar “Čačanska Bestrna.” Ind Crops Prod 53:274–281

    Article  CAS  Google Scholar 

  48. Masuzawa N, Ohdaira E, Ide M (2000) Effects of ultrasonic irradiation on phenolic compounds in wine. Jpn J Appl Phys 39(5S):2978

    Article  CAS  Google Scholar 

  49. Poyraz Ç, Küçükyıldız G, Kırbaşlar Şİ, Ciğeroğlu Z, Şahin S (2021) Valorization of Citrus unshiu biowastes to value-added products: an optimization of ultrasound-assisted extraction method using response surface methodology and particle swarm optimization. Biomass Convers Biorefinery 2021:1–11

  50. Tiwari B, O’donnell C, Patras A, Brunton N, Cullen P (2009) Stability of anthocyanins and ascorbic acid in sonicated strawberry juice during storage. Eur Food Res Technol 228:717–724

  51. Hossain MA, Hossain MS (2021) Optimization of antioxidative phenolic compound extraction from freeze-dried pulp, peel, and seed of Burmese grape (Baccaurea ramiflora Lour.) by response surface methodology. Biomass Convers Biorefinery 2021:1–15

  52. Paini M, Casazza AA, Aliakbarian B, Perego P, Binello A, Cravotto G (2016) Influence of ethanol/water ratio in ultrasound and high-pressure/high-temperature phenolic compound extraction from agri-food waste. Int J Food Sci Technol 51(2):349–358

    Article  CAS  Google Scholar 

  53. Tao Y, Zhang Z, Sun D-W (2014) Kinetic modeling of ultrasound-assisted extraction of phenolic compounds from grape marc: Influence of acoustic energy density and temperature. Ultrason Sonochem 21(4):1461–1469

    Article  CAS  PubMed  Google Scholar 

  54. Gelmez N (2008) Ultrasound assisted and supercritical carbon dioxide extraction of antioxidants from roasted wheat germ. Middle East Technical University

  55. Nguyen L, Le V (2016) Effects of ultrasonic treatment of rumduol mash on the antioxidant level of fruit juice. Int Food Res J 23(6):2335–2340

    CAS  Google Scholar 

  56. Silva E, Rogez H, Larondelle Y (2007) Optimization of extraction of phenolics from Inga edulis leaves using response surface methodology. Sep Purif Technol 55(3):381–387

    Article  CAS  Google Scholar 

  57. Bagheri AR, Arabi M, Ghaedi M, Ostovan A, Wang X, Li J, Chen L (2019) Dummy molecularly imprinted polymers based on a green synthesis strategy for magnetic solid-phase extraction of acrylamide in food samples. Talanta 195:390–400

    Article  CAS  PubMed  Google Scholar 

  58. Kashyap P, Riar CS, Jindal N (2022) Polyphenol bio-accessibility and antioxidant activity of in vitro digested ultrasound-assisted Meghalayan cherry (Prunus nepalensis) pomace extract. Biomass Convers Biorefinery 2022:1–15

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Acknowledgements

This research was supported by Trakya University Office of Scientific Research Projects Coordination (TUBAP, Grant No. 2021/102).

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ID: Formal analysis, investigation, writing—original draft, and writing—review and editing. HO: Formal analysis, investigation, and writing—original draft.

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Correspondence to Irem Damar.

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Ozcan, H., Damar, I. Valorization of spinach roots for recovery of phenolic compounds by ultrasound-assisted extraction: characterization, optimization, and bioaccessibility. Eur Food Res Technol 249, 1899–1913 (2023). https://doi.org/10.1007/s00217-023-04263-4

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