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Lactic acid fermentation of Amla-Indian gooseberry blend: enhancing antioxidants and developing a novel bio-intervention

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Abstract

Indian gooseberry, Amla, is a highly nutritious fruit and one of the richest sources of vitamin C. However, due to its high acidity and astringent taste, it is not suitable for direct consumption. In this study, a blend of amla, guava, and ginger was evaluated as a fermentable substrate by lactic acid bacterial (LAB) fermentation, to improve the quality and stability of this low-pH fruit and to develop a fermented non-dairy beverage. The study results showed that the amla blend was an excellent matrix for LAB growth, with more than 9.38 log10 CFU/mL of viable counts at the end of fermentation. LAB fermentation dramatically increased the total phenolic content, flavonoid content, and antioxidant capacities based on DPPH and FRAP methods. The stability of the fermented amla beverage (FAB) was investigated after storage at 4 °C for 90 days, and there was a healthy bacterial population of 7.43 log10 CFU/mL. The FAB also showed potential as a bio-intervention with enhanced antioxidants, polyphenols, and flavonoids with anti-proliferative activity. Inhibition of the growth of Caco-2 and MOLT 4 cancerous cell lines was observed in a dosage and time-reliant manner, respectively, with considerably high inhibition at 10,000 μg/mL and at 120 min, respectively. This way, lactic acid fermentation can be considered an appropriate tool for developing an amla-based novel bio-intervention with enhanced antioxidants, polyphenols, and flavonoids with anti-proliferative activity and antagonistic efficacy against recurring foodborne pathogens in this post-antibiotic era.

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Data availability

The data that support the findings of this study are not openly available and are available from the corresponding author upon reasonable request.

Code availability

Not applicable.

Abbreviations

LAB:

Lactic acid bacteria

FAB:

Fermented amla beverage

NFAB:

Non-fermented amla beverage

TPC:

Total phenolic content

TFC:

Total flavonoid content

%SA:

%Scavenging activity

FRAP:

Ferric Reduction Antioxidant Power

MOLT-4 cell line:

Human T-lymphoblast; acute lymphoblastic leukemia

CaCo2:

Colorectal carcinoma cells

References

  1. L. Vandenberghe et al., The potential of probiotics: a review. Food Technol. Biotechnol. 48(4), 413–434 (2010)

    Google Scholar 

  2. K.Y. Yoon, E.E. Woodams, Y.D. Hang, Production of probiotic cabbage juice by lactic acid bacteria. Bioresour. Technol. 97(12), 1427–1430 (2006)

    Article  CAS  PubMed  Google Scholar 

  3. R. Modi, I. Kaur, P. Sahota, Lactic acid bacteria as an adjunct starter culture in the development of metabiotic functional black pearl grapes beverage. Environ. Conserv. J. 23(3), 71–80 (2022)

    Article  CAS  Google Scholar 

  4. J. Szutowska, Functional properties of lactic acid bacteria in fermented fruit and vegetable juices: a systematic literature review. Eur. Food Res. Technol. 246(3), 357–372 (2020)

    Article  CAS  Google Scholar 

  5. P. Filannino et al., Exploitation of the health-promoting and sensory properties of organic pomegranate (Punica granatum L.) juice through lactic acid fermentation. Int. J. Food Microbiol. 163(2–3), 184–92 (2013)

    Article  CAS  PubMed  Google Scholar 

  6. M.S. Baliga, J.J. Dsouza, Amla (Emblica officinalis Gaertn), a wonder berry in the treatment and prevention of cancer. Eur. J. Cancer Prev. 20(3), 225–239 (2011)

    Article  CAS  PubMed  Google Scholar 

  7. B.C. Variya, A.K. Bakrania, S.S. Patel, Emblica officinalis (Amla): a review for its phytochemistry, ethnomedicinal uses and medicinal potentials with respect to molecular mechanisms. Pharmacol. Res. 111, 180–200 (2016)

    Article  CAS  PubMed  Google Scholar 

  8. S. Rezac et al., Fermented foods as a dietary source of live organisms. Front. Microbiol. 9, 1785 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  9. G. Pandove, P. Sahota, N. Gupta, Development of low alcoholic naturally carbonated fermented debittered beverage from grapefruit (Citrus paradisi). J. Appl. Nat. Sci. 8, 1649–1653 (2016)

    CAS  Google Scholar 

  10. P. Sahota et al., Evaluation of a BWTK for detection of total coliforms, E. coli and emerging pathogens from drinking water: comparison with standard MPN method. Water Sci. Technol. 62(3), 676–83 (2010)

    Article  CAS  PubMed  Google Scholar 

  11. E. Kim, S.M. Yang, H.Y. Kim, Analysis of cultivable microbial community during Kimchi fermentation using MALDI-TOF MS. Foods 10(5), 1068 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. M.H. Zwietering et al., Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56(6), 1875–1881 (1990)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. C. Aydın, R. Mammadov, Phenolic composition, antioxidant, antibacterial, larvacidal against Culex pipiens, and cytotoxic activities of Hyacinthella lineata steudel extracts. Int. J. Food Prop. 20(10), 2276–2285 (2017)

    Article  Google Scholar 

  14. E. Kwaw et al., Effect of fermentation parameters and their optimization on the phytochemical properties of lactic-acid-fermented mulberry juice. J. Food Meas. Charact. 11(3), 1462–1473 (2017)

    Article  Google Scholar 

  15. B. Suárez et al., Phenolic profiles, antioxidant activity and in vitro antiviral properties of apple pomace. Food Chem. 120(1), 339–342 (2010)

    Article  Google Scholar 

  16. M. Fazaeli, G. Hojjatpanah, Z. Emam-Djomeh, Effects of heating method and conditions on the evaporation rate and quality attributes of black mulberry (Morus nigra) juice concentrate. J. Food Sci. Technol. 50(1), 35–43 (2013)

    Article  PubMed  Google Scholar 

  17. E. Kwaw et al., Effect of lactobacillus strains on phenolic profile, color attributes and antioxidant activities of lactic-acid-fermented mulberry juice. Food Chem. 250, 148–154 (2018)

    Article  CAS  PubMed  Google Scholar 

  18. S. Er, A. Koparal, M. Kivanc, Cytotoxic effects of various lactic acid bacteria on Caco-2 cells. Turk. J. Biol. 39, 23–30 (2015)

    Article  Google Scholar 

  19. M.G.M. Costa et al., Sonicated pineapple juice as substrate for L. casei cultivation for probiotic beverage development: process optimisation and product stability. Food Chem. 139(1), 261–266 (2013)

    Article  CAS  PubMed  Google Scholar 

  20. I. Ferrari Pereira Lima et al., Development of an innovative nutraceutical fermented beverage from herbal mate (Ilex paraguariensis A. St.-Hil.) extract. Int. J. Mol. Sci. 13(1), 788–800 (2012)

    Article  PubMed  Google Scholar 

  21. M. Kieliszek et al., Characteristics of the proteolytic enzymes produced by lactic acid bacteria. Molecules 26(7), 1858 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. S.J. Hur et al., Effect of fermentation on the antioxidant activity in plant-based foods. Food Chem. 160, 346–356 (2014)

    Article  CAS  PubMed  Google Scholar 

  23. C.A. Torres, L.A. Romero, R.I. Diaz, Quality and sensory attributes of apple and quince leathers made without preservatives and with enhanced antioxidant activity. LWT Food Sci. Technol. 62(2), 996–1003 (2015)

    Article  CAS  Google Scholar 

  24. C.-C. Ng et al., Lactic acid bacterial fermentation on the production of functional antioxidant herbal Anoectochilus formosanus Hayata. J. Biosci. Bioeng. 111(3), 289–293 (2011)

    Article  CAS  PubMed  Google Scholar 

  25. S.-C. Chu, C. Chen, Effects of origins and fermentation time on the antioxidant activities of kombucha. Food Chem. 98(3), 502–507 (2006)

    Article  CAS  Google Scholar 

  26. K. Katina et al., Bran fermentation as a means to enhance technological properties and bioactivity of rye. Food Microbiol. 24(2), 175–186 (2007)

    Article  CAS  PubMed  Google Scholar 

  27. E.S. Lago-Vanzela et al., Aging of red wines made from hybrid grape cv. BRS Violeta: effects of accelerated aging conditions on phenolic composition, color and antioxidant activity. Food Res. Int. 56, 182–189 (2014)

    Article  CAS  Google Scholar 

  28. Z.E. Mousavi et al., Effect of fermentation of pomegranate juice by Lactobacillus plantarum and Lactobacillus acidophilus on the antioxidant activity and metabolism of sugars, organic acids and phenolic compounds. Food Biotechnol. 27(1), 1–13 (2013)

    Article  CAS  Google Scholar 

  29. G. Pereira-Caro et al., Chronic administration of a microencapsulated probiotic enhances the bioavailability of orange juice flavanones in humans. Free Radic. Biol. Med. 84, 206–214 (2015)

    Article  CAS  PubMed  Google Scholar 

  30. A. Chlebowska-Smigiel et al., The effect of pullulan on the growth and acidifying activity of selected stool microflora of human. Curr. Pharm. Biotechnol. 18(2), 121–126 (2017)

    Article  CAS  PubMed  Google Scholar 

  31. L. Wang et al., Dynamic changes in phenolic compounds, colour and antioxidant activity of mulberry wine during alcoholic fermentation. J. Funct. Foods 18, 254–265 (2015)

    Article  CAS  Google Scholar 

  32. A. Waśko, M. Kieliszek, Z. Targoński, Purification and characterization of a proteinase from the probiotic Lactobacillus rhamnosus OXY. Prep. Biochem. Biotechnol. 42(5), 476–488 (2012)

    Article  PubMed  Google Scholar 

  33. F.O. Adetuyi, T.A. Ibrahim, Effect of fermentation time on the phenolic, flavonoid and vitamin C contents and antioxidant activities of okra (Abelmoschus esculentus) seeds. Niger. Food J. 32(2), 128–137 (2014)

    Article  Google Scholar 

  34. F.A. Silva et al., Phenolic acids and derivatives: studies on the relationship among structure, radical scavenging activity, and physicochemical parameters. J. Agric. Food Chem. 48(6), 2122–2126 (2000)

    Article  CAS  PubMed  Google Scholar 

  35. A.R. Choi et al., Antagonistic activities and probiotic potential of lactic acid bacteria derived from a plant-based fermented food. Front. Microbiol. 9, 1963 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  36. S.S. Choi et al., Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett. Appl. Microbiol. 42(5), 452–458 (2006)

    Article  CAS  PubMed  Google Scholar 

  37. R. Kazimierczak et al., Beetroot (Beta vulgaris L.) and naturally fermented beetroot juices from organic and conventional production: metabolomics, antioxidant levels and anticancer activity. J. Sci. Food Agric. 94(13), 2618–29 (2014)

    Article  CAS  PubMed  Google Scholar 

  38. S.S. Tasdemir, N. Sanlier, An insight into the anticancer effects of fermented foods: a review. J. Funct. Foods 75, 104281 (2020)

    Article  CAS  Google Scholar 

  39. S. Franceschi, C.P. Wild, Meeting the global demands of epidemiologic transition—the indispensable role of cancer prevention. Mol. Oncol. 7(1), 1–13 (2013)

    Article  PubMed  Google Scholar 

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Acknowledgements

RM would like to thank Dr. Mayank Garg, Postdoctoral Researcher, Texas A&M University, College Station, Texas, USA.

Funding

There is no funding agency involved, all the research work is done and supported by the Punjab Agricultural University, Ludhiana, India.

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  1. Ritika Modi

    Present address: Texas A&M University, College Station, TX, USA

Authors and Affiliations

  1. Department of Microbiology, Punjab Agricultural University (PAU), Ludhiana, Punjab, India

    Ritika Modi, ParamPal Sahota & Gulab Pandove

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  1. Ritika Modi
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  2. ParamPal Sahota
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  3. Gulab Pandove
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RM, carried out the research, designed the concept, written the manuscript. PS, designed the concept, reviewed the article and edited. GP, experiment design, reviewed the article and edited.

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Correspondence to Ritika Modi.

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Modi, R., Sahota, P. & Pandove, G. Lactic acid fermentation of Amla-Indian gooseberry blend: enhancing antioxidants and developing a novel bio-intervention. Food Measure 18, 137–149 (2024). https://doi.org/10.1007/s11694-023-02154-6

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  • DOI: https://doi.org/10.1007/s11694-023-02154-6

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