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Application of response surface methodology for the co-optimization of extraction and probiotication of phenolic compounds from pomegranate fruit peels (Punica granatum L.)

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Abstract

Currently, the synergistic interactions between plant polyphenols and probiotic bacteria are gaining interest with diverse perspectives of applications of both functional ingredients. This study aims to explore and optimize the interaction between pomegranate peel polyphenols and the probiotic strain Lactobacillus rhamnosus ATCC 53103, throughout the co-optimization of the extraction/probiotication techniques. In this context, the response surface methodology (RSM) was applied to find the suitable extraction conditions to obtain phenolic extracts exhibiting a synergistic interaction when fermented with the probiotic strain. A ß-Cyclodextrin ultrasound-assisted extraction technique has been applied for pomegranate polyphenols extraction, followed by the probiotic fermentation of extracts. Results of RSM indicate that for all chosen design responses, the experimental values are in good agreement with the predicted one, with R squared values above 0.8 for all prediction models. Using optimal conditions predicted by the desirability function, it has been found that after probiotication of optimized phenolic extracts, the growth of probiotic strain at presence of polyphenols was possible. Moreover, a significant (p < 0.05) improvement of in vitro antioxidant activity of probioticated extracts was confirmed (an increase on in vitro free radical scavenging activity up to 51.37%). Results of this study, demonstrate for the first time, the feasibility of RSM approach to perform simultaneously the optimization of extraction and probiotication processes of phenolic compounds with the perspective to develop a new bioprocess aiming to produce functional food ingredient or novel nutraceutical products containing both bioactive polyphenols and beneficial probiotic bacteria.

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Abbreviations

ABTS:

2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt

DPPH:

2,2-Di(4-tert-octylphenyl)-1-picrylhydrazyl

TPC:

Total phenolic content

RSM:

Response surface methodology

DOD:

D-optimal design of experiments

GAE/mL:

Gallic acid equivalent per milliliter

OD:

Optical density

ß-CD:

ß-Cyclodextrin

ANOVA:

Analysis of variance

R 2 :

Coefficient of determination R squared

Adj R 2 :

Adjusted R squared

Pred R 2 :

Predicted R squared

r :

Coefficient of Pearson correlation

df:

Degrees of freedom

ABTS RSA:

ABTS radical scavenging activity

DPPH RSA:

DPPH radical scavenging activity

CFU:

Colony forming units

References

  1. C. Galanakis, Food Waste Valorization Opportunities for Different Food Industries. In The Interaction of Food Industry and Environment (Elsevier, New York, 2020), pp. 341–422

    Google Scholar 

  2. N. Jiménez-Moreno et al., Valorization of selected fruit and vegetable wastes as bioactive compounds: Opportunities and challenges. Crit. Rev. Environ. Sci. Technol. 50(20), 2061–2108 (2020)

    Article  Google Scholar 

  3. J. Villacís-Chiriboga et al., Valorization of byproducts from tropical fruits: extraction methodologies, applications, environmental, and economic assessment: a review (Part 1: general overview of the byproducts, traditional biorefinery practices, and possible applications). Comprehensive Reviews in Food Science and Food Safety 19(2), 405–447 (2020)

    Article  PubMed  Google Scholar 

  4. P. Negi, G. Jayaprakasha, B. Jena, Antioxidant and antimutagenic activities of pomegranate peel extracts. Food Chem. 80(3), 393–397 (2003)

    Article  CAS  Google Scholar 

  5. T. Ismail, P. Sestili, S. Akhtar, Pomegranate peel and fruit extracts: a review of potential anti-inflammatory and anti-infective effects. J. Ethnopharmacol. 143(2), 397–405 (2012)

    Article  CAS  PubMed  Google Scholar 

  6. N. Panth, B. Manandhar, K.R. Paudel, Anticancer activity of Punica granatum (pomegranate): a review. Phytother. Res. 31(4), 568–578 (2017)

    Article  PubMed  Google Scholar 

  7. E.L. de Souza et al., Potential interactions among phenolic compounds and probiotics for mutual boosting of their health-promoting properties and food functionalities—a review. Crit. Rev. Food Sci. Nutr. 59(10), 1645–1659 (2019)

    Article  PubMed  Google Scholar 

  8. A. Banerjee, P. Dhar, Amalgamation of polyphenols and probiotics induce health promotion. Crit. Rev. Food Sci. Nutr. 59(18), 2903–2926 (2019)

    Article  CAS  PubMed  Google Scholar 

  9. Y. Liu et al., Increasing antiradical activity of polyphenols from lotus seed epicarp by probiotic bacteria bioconversion. Molecules 23(10), 2667 (2018)

    Article  PubMed Central  Google Scholar 

  10. S. Li et al., Increasing antioxidant activity of procyanidin extracts from the pericarp of Litchi chinensis processing waste by two probiotic bacteria bioconversions. J. Agric. Food Chem. 61(10), 2506–2512 (2013)

    Article  CAS  PubMed  Google Scholar 

  11. A.M.L. de Lacey et al., Biotransformation and resulting biological properties of green tea polyphenols produced by probiotic bacteria. LWT Food Sci. Technol. 58(2), 633–638 (2014)

    Article  Google Scholar 

  12. H. Rupasinghe, I. Parmar, S.V. Neir, Biotransformation of cranberry proanthocyanidins to probiotic metabolites by Lactobacillus rhamnosus enhances their anticancer activity in HepG2 cells in vitro. Oxidat. Med. Cell. Longevity (2019)

  13. V. Sorrenti et al., Beneficial effects of pomegranate peel extract and probiotics on pre-adipocyte differentiation. Front. Microbiol. 10, 660 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  14. A. Cozzolino et al., Preliminary evaluation of the safety and probiotic potential of Akkermansia muciniphila DSM 22959 in comparison with Lactobacillus rhamnosus GG. Microorganisms 8(2), 189 (2020)

    Article  CAS  PubMed Central  Google Scholar 

  15. M. Giovanni, Response surface methodology and product optimization. Food Technol. (1983).

  16. R. Tabaraki, E. Heidarizadi, A. Benvidi, Optimization of ultrasonic-assisted extraction of pomegranate (Punica granatum L.) peel antioxidants by response surface methodology. Separ. Purif. Technol. 98, 16–23 (2012)

    Article  CAS  Google Scholar 

  17. V.L. Singleton, J.A. Rossi, Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16(3), 144–158 (1965)

    CAS  Google Scholar 

  18. F. Saci et al., Changes in anticholinesterase, antioxidant activities and related bioactive compounds of carob pulp (Ceratonia siliqua L.) during ripening stages. J Food Measur. Charact. 14(2), 937–945 (2020)

    Article  Google Scholar 

  19. P. Molyneux, The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J. sci. technol 26(2), 211–219 (2004)

    CAS  Google Scholar 

  20. R. Re et al., Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 26(9–10), 1231–1237 (1999)

    Article  CAS  Google Scholar 

  21. M. Singh et al., Influence of the solvents on the extraction of major phenolic compounds (punicalagin, ellagic acid and gallic acid) and their antioxidant activities in pomegranate aril. J. Food Sci. Technol. 51(9), 2070–2077 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. S. Ben-Ali et al., Optimization of extraction process and chemical characterization of pomegranate peel extract. Chem. Pap. 72(8), 2087–2100 (2018)

    Article  CAS  Google Scholar 

  23. Wang, Z., et al., Extract of phenolics from pomegranate peels. Open Food Sci. J. 5(1), 2011.

  24. H. Saad et al., Characterization of pomegranate peels tannin extractives. Ind. Crops Prod. 40, 239–246 (2012)

    Article  CAS  Google Scholar 

  25. A.C. Diamanti et al., Green extraction of polyphenols from whole pomegranate fruit using cyclodextrins. Food Chem. 214, 61–66 (2017)

    Article  CAS  PubMed  Google Scholar 

  26. R. Cai et al., Cyclodextrin-assisted extraction of phenolic compounds: current research and future prospects. Trends Food Sci. Technol. 79, 19–27 (2018)

    Article  CAS  Google Scholar 

  27. A. Lakka, S. Lalas, D.P. Makris, Hydroxypropyl-β-cyclodextrin as a green co-solvent in the aqueous extraction of polyphenols from waste orange peels. Beverages 6(3), 50 (2020)

    Article  CAS  Google Scholar 

  28. V. Athanasiadis et al., Methyl β-cyclodextrin as a booster for the extraction for Olea europaea leaf polyphenols with a bio-based deep eutectic solvent. Biomass Convers. Biorefinery 8(2), 345–355 (2018)

    Article  CAS  Google Scholar 

  29. N. El Darra, et al., Comparative study between Ethanolic and β-Cyclodextrin assisted extraction of polyphenols from peach pomace. Int. J. Food Sci. (2018)

  30. A. Floegel et al., Comparison of ABTS/DPPH Assays for the Detection of Antioxidant Capacity in Foods (Wiley Online Library, New York, 2010).

    Google Scholar 

  31. Y. Lee, J. Oh, Y.-S. Jeong, Lactobacillus plantarum-mediated conversion of flavonoid glycosides into flavonols, quercetin, and kaempferol in Cudrania tricuspidata leaves. Food Sci Biotechnol 24(5), 1817–1821 (2015)

    Article  CAS  Google Scholar 

  32. D. Zhao, N.P. Shah, Lactic acid bacterial fermentation modified phenolic composition in tea extracts and enhanced their antioxidant activity and cellular uptake of phenolic compounds following in vitro digestion. J Funct Foods 20, 182–194 (2016)

    Article  CAS  Google Scholar 

  33. C.-L. Chan et al., Polyphenols from selected dietary spices and medicinal herbs differentially affect common food-borne pathogenic bacteria and lactic acid bacteria. Food Control 92, 437–443 (2018)

    Article  CAS  Google Scholar 

  34. D. Hervert-Hernández et al., Stimulatory role of grape pomace polyphenols on Lactobacillus acidophilus growth. Int. J. Food Microbiol. 136(1), 119–122 (2009)

    Article  PubMed  Google Scholar 

  35. R. Pacheco-Ordaz et al., Effect of phenolic compounds on the growth of selected probiotic and pathogenic bacteria. Lett. Appl. Microbiol. 66(1), 25–31 (2018)

    Article  CAS  PubMed  Google Scholar 

  36. S. Raissi, R.-E. Farsani, Statistical process optimization through multi-response surface methodology. World Acad. Sci. Eng. Technol. 51(46), 267–271 (2009)

    Google Scholar 

  37. A. Sood, M. Gupta, Extraction process optimization for bioactive compounds in pomegranate peel. Food Biosci. 12, 100–106 (2015)

    Article  CAS  Google Scholar 

  38. A.I. Andres et al., Optimization of extraction conditions to improve phenolic content and in vitro antioxidant activity in craft brewers’ spent grain using response surface methodology (RSM). Foods 9(10), 1398 (2020)

    Article  CAS  PubMed Central  Google Scholar 

  39. N. Seeram et al., Rapid large scale purification of ellagitannins from pomegranate husk, a by-product of the commercial juice industry. Sep. Purif. Technol. 41(1), 49–55 (2005)

    Article  CAS  Google Scholar 

  40. W.A. Jensen, Response surface methodology: process and product optimization using designed experiments. J. Qual. Technol. 49(2), 186 (2017)

    Article  Google Scholar 

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Acknowledgements

The authors address thanks and gratitude to the Algerian Ministry of Higher Education and Scientific Research and the National Centre for Biotechnology Research for their provided financial and material supports.

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Correspondence to Tarek Moussaoui.

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Moussaoui, T., Khali, M. & Madi, N. Application of response surface methodology for the co-optimization of extraction and probiotication of phenolic compounds from pomegranate fruit peels (Punica granatum L.). Food Measure 15, 3618–3633 (2021). https://doi.org/10.1007/s11694-021-00943-5

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