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Effect of mulberry leaf extract fortification and probiotic fermentation on the bioactivities of cottage cheese

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Abstract

This study aims to enhance the bioactive property of cottage cheese by incorporating mulberry leaf extract (MLE) and applying probiotic fermentation. The MLE was produced via ultrasound-assisted water extraction (UW), pectinase-pretreated ultrasound-assisted water extraction (PUW) and cellulase-pretreated ultrasound-assisted water extraction. The MLE with the highest DPPH, FRAP, α-amylase inhibition (AI) and albumin denaturation inhibition (ADI) activities was selected to incorporate into the cheese. Lastly, the cheese was fermented with Lactobacillus plantarum TAR4. Results obtained reveal that UW and PUW produced MLE with the best bioactivities. Total phenolics, flavonoids, DPPH, FRAP, AI and ADI activities of the cottage cheeses were significantly enhanced with the fortification of MLE. Fermentation with L. plantarum TAR4 further enhanced the DPPH, FRAP, AI and ADI activities of the cheeses. Results of in-vitro digestion proved that the bioactivities exhibited by the cheeses did not diminished after digestion. Among the cheeses, fermented cheese fortified with MLE produced via UW (UW-LAB) showed the best bioactivity. After digestion, UW-LAB cheese exhibited 2.09 ± 0.12 mg g1 of FRAP, 74.77 ± 1.90% of DPPH, 64.91 ± 1.16% of AI and 38.83 ± 2.50% of ADI activities. This study recommends that combined MLE fortification with L. plantarum TAR4 fermentation was the best approach to improve nutrition value of cottage cheese.

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Data of this study are available from the corresponding author upon request.

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References

  1. E. Pappa, I. Kandarakis, H. Mallatou, Effect of different types of milks and cultures on the rheological characteristics of Teleme cheese. J. Food Eng 79(1), 143–149 (2007)

    Google Scholar 

  2. B. Walther, A. Schmid, R. Sieber, K. Wehrmüller, Cheese in nutrition and health. Dairy Sci. Technol. 88(4–5), 389–405 (2008)

    CAS  Google Scholar 

  3. R. Foster, Cheese: Types, Nutrition and Consumption, 1st edn. (Nova Science Publishers, Hauppauge, 2011), pp. 269–270

    Google Scholar 

  4. P. Solhi, S. Azadmard-Damirchi, J. Hesari, H. Hamishehkar, Effect of fortification with asparagus powder on the qualitative properties of processed cheese. Int. J. Dairy Technol. 73(1), 226–233 (2019)

    Google Scholar 

  5. K. Kim, J. Hwang, S. Eum, H. Paik, Physiochemical analysis, antioxidant effects, and sensory characteristics of quark cheese supplemented with ginseng extract. Food Sci. Anim. Resour. 39(2), 324–331 (2019)

    PubMed  PubMed Central  Google Scholar 

  6. H. Himed-Idir, K. Mouhoubi, E. Siar, H. Boudries, H. Mansouri, N. Adjeroud, K. Madani, L. Boulekbache-Makhlouf, Effect of rosemary (Rosmarinus officinalis L.) supplementation on fresh cheese: physicochemical properties, antioxidant potential, and sensory attributes. J. Food Process Presv. 45(1), e15057 (2020)

    Google Scholar 

  7. D.F. Hasneen, N.L. Zaki, M.S. Abbas, A.S. Soliman, I.S. Ashoush, A.E. Fayed, Comparative evaluation of some herbs and their suitability for skimmed milk yoghurt and cast Kariesh cheese fortification as functional foods. Ann. Agric. Sci. 65, 6–12 (2020)

    Google Scholar 

  8. S. Srivastava, R. Kapoor, A. Thathola, R. Srivastava, Nutritional quality of leaves of some genotypes of mulberry (Morus alba). Int. J. Food Sci. Nutr. 57(5–6), 305–313 (2006)

    CAS  PubMed  Google Scholar 

  9. D. Yigit, F. Akar, E. Baydas, M. Buyukyildiz, Elemental composition of various mulberry species. Asian J. Chem. 22(5), 3554–3560 (2010)

    CAS  Google Scholar 

  10. S. Shahana, A. Nikalje, Phytochemistry and bioactivity of Morus alba (Mulberry) plant: a comprehensive review. Asian J Pharm Pharmacol. 5(2), 207–217 (2019)

    CAS  Google Scholar 

  11. E. Chan, R. Lye, S. Wong, Phytochemistry, pharmacology, and clinical trials of Morus alba. Chin. J Nat. Med. 14(1), 0017–0030 (2016)

    CAS  Google Scholar 

  12. Y. Liu, X. Li, C. **e, X. Luo, Y. Bao, B. Wu, Y. Hu, Z. Zhong, C. Liu, M. Li, Prevention effects and possible molecular mechanism of mulberry leaf extract and its formulation on rats with insulin-insensitivity. PLoS ONE 11(4), e0152728 (2016)

    PubMed  PubMed Central  Google Scholar 

  13. J. Huang, Y. Wang, C. Ying, L. Liu, Z. Lou, Effects of mulberry leaf on experimental hyperlipidemia rats induced by high-fat diet. Exp. Ther. Med. 16, 547–556 (2018)

    PubMed  PubMed Central  Google Scholar 

  14. S. Fathy, A. Singab, S. Agwa, D. Abd El Hamid, F. Zahra, S. Abd El Moneim, The antiproliferative effect of mulberry (Morus alba L.) plant on hepatocarcinoma cell line HepG2. Egypt. J. Med. Hum. Genet 14(4), 375–382 (2013)

    Google Scholar 

  15. H. Lim, S. Lee, S. Kim, S. Yang, Y. Lim, Anti-inflammatory and antiobesity effects of mulberry leaf and fruit extract on high fat diet-induced obesity. Exp. Biol. Med. 238(10), 1160–1169 (2013)

    Google Scholar 

  16. G. Kim, H. Jang, Flavonol content in the water extract of the mulberry (Morus alba L.) leaf and their antioxidant capacities. J. Food Sci. 76(6), C869–C873 (2011)

    CAS  PubMed  Google Scholar 

  17. Y. Wang, D. Shurtleff, Probiotics: What you need to know. (Nccih.nih.gov., 2019) https://www.nccih.nih.gov/health/probiotics-what-you-need-to-know. Accessed 17 January 2021.

  18. C. Shortt, The probiotic century: historical and current perspectives. Trends Food Sci. Technol. 10(12), 411–417 (1999)

    CAS  Google Scholar 

  19. S. Gupta, N. Abu-Ghannam, Probiotic fermentation of plant-based products: Possibilities and opportunities. Crit Rev Food Sci Nutr. 52(2), 183–199 (2012)

    CAS  PubMed  Google Scholar 

  20. E. Pessione, S. Cirrincione, Bioactive molecules released in food by lactic acid bacteria: Encrypted peptides and biogenic amines. Front. Microbiol. 7, 876 (2016). https://doi.org/10.3389/fmicb.2016.00876

    Article  PubMed  PubMed Central  Google Scholar 

  21. R. Perez, T. Zendo, K. Sonomoto, Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microb. Cell Fact. 13(Suppl 1), S3 (2014)

    PubMed  PubMed Central  Google Scholar 

  22. K. Peng, M. Koubaa, O. Bals, E. Vorobiev, Recent insights in the impact of emerging technologies on lactic acid bacteria: a review. Food Res. Int. 137, 109544 (2020)

    CAS  PubMed  Google Scholar 

  23. P. Wen, T. Hu, R. Linhardt, S. Liao, H. Wu, Y. Zou, Mulberry: a review of bioactive compounds and advanced processing technology. Trends Food Sci. Technol. 83, 138–158 (2019)

    CAS  Google Scholar 

  24. M. Minekus, M. Alminger, P. Alvito, S. Ballace, T. Bohn, C. Bourlieu, F. Carriere, R. Boutrou, M. Corredig, D. Dupont, C. Dufour, L. Egger, M. Golding, S. Karakaya, B. Kirkhus, S.L. Feunteun, U. Lesmes, A. Macierzanka, A. Mackie, S. Marze, D.J. McClements, O. Menard, I. Recio, C.N. Santos, R. Singh, G.E. Vegarud, M.S.J. Wickham, W. Weitshcies, A. Brodkorb, A standardized static in vitro digestion method suitable for food—an international consensus. Food Funct. 5(6), 1113–1124 (2014)

    CAS  PubMed  Google Scholar 

  25. S.A. Baba, S.A. Malik, Evaluation of antioxidant and antibacterial activity of methanolic extracts of Gentiana kurroo royle. Saudi J. Biol Sci. 21, 493–498 (2014)

    PubMed  PubMed Central  Google Scholar 

  26. M.A. Mir, S.S. Sawhney, M.M.S. Jassal, In-vitro antidiabetic studies of various extracts of Taraxacum officinale. Pharm. Innov. 4(1), 61–66 (2015)

    Google Scholar 

  27. S. Kumari, N. Yasmin, M.R. Hussain, M. Babyselvam, In-vitro anti-inflammatory and anti-arthritic property of Rhizophora mucronate leaves. Int. J. Pharm. Sci. Res. 6, 482–485 (2015)

    CAS  Google Scholar 

  28. L. Wang, Y. Wu, Y. Liu, Z. Wu, Complex enzyme-assisted extraction releases antioxidative phenolic compositions from guava leaves. Molecules 22(10), 1648 (2017)

    PubMed Central  Google Scholar 

  29. K. Rakariyatham, X. Liu, Z. Liu, S. Wu, F. Shahidi, D. Zhou, B. Zhu, Improvement of phenolic contents and antioxidant activities of longan (Dimocarpus longan) peel extracts by enzymatic treatment. Waste Biomass Valorization 11(8), 3987–4002 (2019)

    Google Scholar 

  30. P. Kapasakalidis, R. Rastall, M. Gordon, Effect of a cellulase treatment on extraction of antioxidant phenols from black currant (Ribes nigrum L.) pomace. J. Agric. Food Chem. 57(10), 4342–4351 (2009)

    CAS  PubMed  Google Scholar 

  31. M. Puri, D. Sharma, C. Barrow, Enzyme-assisted extraction of bioactives from plants. Trends Biotechnol. 30(1), 37–44 (2012)

    CAS  PubMed  Google Scholar 

  32. E.W.C. Chan, S.K. Wong, J. Tangah, T. Inoue, H.T. Chan, Phenolic constituents and anticancer properties of Morus alba (White mulberry) leaves. J. Integr. Med. 18, 189–195 (2020)

    PubMed  Google Scholar 

  33. S. Baba, S. Malik, Determination of total phenolic and flavonoid content, antimicrobial and antioxidant activity of a root extract of Arisaema jacquemontii Blume. J. Taibah Univ. Sci. 9(4), 449–454 (2015)

    Google Scholar 

  34. J. Chen, J. Yang, L. Ma, J. Li, N. Shahzad, C.K. Kim, Structural-antioxidant activity relationship of methoxy, phenolic, hydroxyl and carboxylic acid groups of phenolic acids. Sci. Rep. 10, 2611 (2020)

    CAS  PubMed  PubMed Central  Google Scholar 

  35. T. Moussa-Ayoub, S. El-Samahy, L. Kroh, S. Rohn, Identification and quantification of flavonol aglycons in cactus pear (Opuntia ficus indica) fruit using a commercial pectinase and cellulase preparation. Food Chem. 124(3), 1177–1184 (2011)

    CAS  Google Scholar 

  36. F. Abbes, W. Kchaou, C. Blecker, M. Ongena, G. Lognay, H. Attia, S. Besbes, Effect of processing conditions on phenolic compounds and antioxidant properties of date syrup. Ind Crops Prod. 44, 634–642 (2013)

    CAS  Google Scholar 

  37. J. Kim, B. Choi, M. Jung, J. Wee, K. Chung, O. Kwon, Mulberry leaf water extract ameliorates insulin sensitivity in high fat or high sucrose diet induced overweight rats. J. Korean Soc. Appl Biol. Chem. 54(4), 612–618 (2011)

    CAS  Google Scholar 

  38. T. Anno, K. Tamura, H. Oono, H. Tomi, Maltase, sucrase and alpha-amylase inhibitory activity of Morus leaves extract. Food Preserv. Sci. 30(5), 223–229 (2004)

    Google Scholar 

  39. D. Riche, K. Riche, H. East, E. Barrett, W. May, Impact of mulberry leaf extract on type 2 diabetes (Mul-DM): a randomized, placebo-controlled pilot study. Complement. Ther. Med. 32, 105–108 (2017)

    PubMed  Google Scholar 

  40. M. Lown, R. Fuller, H. Lightowler, A. Fraser, A. Gallagher, B. Stuart, C. Byrne, G. Lewith, Mulberry-extract improves glucose tolerance and decreases insulin concentrations in normoglycaemic adults: results of a randomised double-blind placebo-controlled study. PLoS ONE 12(2), e0172239 (2017)

    PubMed  PubMed Central  Google Scholar 

  41. D. Luo, T. Mu, H. Sun, Profiling of phenolic acids and flavonoids in sweet potato (Ipomoea batatas L.) leaves and evaluation of their anti-oxidant and hypoglycemic activities. Food Biosci. 39, 100801 (2021)

    CAS  Google Scholar 

  42. A.K.P. Reshma, P. Brindha, In vitro anti-inflammatory, antioxidant and nephroprotective studies on leaves of Aegle Marmelos and Ocimum Sanctum. Asian J. Pharm. Clin. Res. 7(4), 121–129 (2014)

    Google Scholar 

  43. P. De, M. Dey, M.J. Mukhophadhyay, The study of antioxidant, membrane stabilization, anti protein-denaturation property and analysis of phytochemicals in three species of tagetes leaf and flower extract. Int. J. Pharmacogn. Phytochem. Res. 9(8), 1159–1165 (2017)

    Google Scholar 

  44. J. Kobus-Cisowska, M. Dziedziński, D. Szymanowska, O. Szczepaniak, S. Byczkiewicz, A. Telichowska, P. Szulc, The effects of Morus alba L. fortification on the quality, functional properties and sensory attributes of bread stored under refrigerated conditions. Sustainability 12(16), 6691 (2020)

    Google Scholar 

  45. M. Tomczyk, M. Miłek, E. Sidor, I. Kapusta, W. Litwińczuk, C. Puchalski, M. Dżugan, The effect of adding the leaves and fruits of Morus alba to rape honey on its antioxidant properties, polyphenolic profile, and amylase activity. Molecules 25(1), 84 (2019)

    PubMed Central  Google Scholar 

  46. K. Katina, K. Liukkonen, A. Kaukovirta-Norja, H. Adlercreutz, S. Heinonen, A. Lampi, J. Pihlava, K. Poutanen, Fermentation-induced changes in the nutritional value of native or germinated rye. J. Cereal Sci. 46(3), 348–355 (2007)

    CAS  Google Scholar 

  47. T. Santos, P. Feitosa, N. Gualberto, N. Narain, L. Santana, Improvement of bioactive compounds content in granadilla (Passiflora ligularis) seeds after solid-state fermentation. Food Sci. Technol. Int. 27(3), 234–241 (2020)

    PubMed  Google Scholar 

  48. K. Wang, M. Niu, D. Song, Y. Liu, Y. Wu, J. Zhao, S. Li, B. Lu, Evaluation of biochemical and antioxidant dynamics during the co-fermentation of dehusked barley with Rhizopus oryzae and Lactobacillus plantarum. J. Food Biochem. 44(2), e13106 (2019). https://doi.org/10.1111/jfbc.13106

    Article  PubMed  Google Scholar 

  49. S. Yildirim-Elikoglu, Y. Erdem, Interactions between milk proteins and polyphenols: binding mechanisms, related changes, and the future trends in the dairy industry. Food Rev. Int. 34(7), 665–697 (2017)

    Google Scholar 

  50. M. Mtolo, A. Gerrano, J. Mellem, Effect of simulated gastrointestinal digestion on the phenolic compound content and in vitro antioxidant capacity of processed Cowpea (V. unguiculata) cultivars. CyTA—J. Food 15(3), 391–399 (2017)

    CAS  Google Scholar 

  51. J. Bouayed, L. Hoffmann, T. Bohn, Total phenolics, flavonoids, anthocyanins and antioxidant activity following simulated gastro-intestinal digestion and dialysis of apple varieties: bioaccessibility and potential uptake. Food Chem. 128(1), 14–21 (2011)

    CAS  PubMed  Google Scholar 

  52. G. Gonzales, G. Smagghe, A. Mackie, C. Grootaert, B. Bajka, N. Rigby, K. Raes, J. Van Camp, Use of metabolomics and fluorescence recovery after photobleaching to study the bioavailability and intestinal mucus diffusion of polyphenols from cauliflower waste. J. Funct. Foods 16, 403–413 (2015)

    CAS  Google Scholar 

  53. X. Jiao, B. Li, Q. Zhang, N. Gao, X. Zhang, X. Meng, Effect of in vitro-simulated gastrointestinal digestion on the stability and antioxidant activity of blueberry polyphenols and their cellular antioxidant activity towards HepG2 cells. Int. J. Food Sci. Technol. 53(1), 61–71 (2017)

    Google Scholar 

  54. K. Sharma, E. Ko, A. Assefa, S. Ha, S. Nile, E. Lee, S. Park, Temperature-dependent studies on the total phenolics, flavonoids, antioxidant activities, and sugar content in six onion varieties. J. Food Drug Anal. 23(2), 243–252 (2015)

    CAS  PubMed  Google Scholar 

  55. A. Ali, C. Chong, S. Mah, L. Abdullah, T. Choong, B. Chua, Impact of storage conditions on the stability of predominant phenolic constituents and antioxidant activity of dried piper betle extracts. Molecules 23(2), 484 (2018)

    PubMed Central  Google Scholar 

  56. A. Rashidinejad, E. Birch, D. Everett, Antioxidant activity and recovery of green tea catechins in full-fat cheese following gastrointestinal simulated digestion. J. Food Compos. Anal. 48, 13–24 (2016)

    CAS  Google Scholar 

  57. T. Chukkrit, T. Taweesak, K. Ratchanee, C. Rin, Antioxidant activities and polyphenol compounds in snack products fortified with mulberry leaf powder. RMUTP Res. J. Sci. Technol. 14(2), 57–71 (2020)

    Google Scholar 

  58. S. Lamothe, A. Langlois, L. Bazinet, C. Couillard, M. Britten, Antioxidant activity and nutrient release from polyphenol-enriched cheese in a simulated gastrointestinal environment. Food Funct. 7(3), 1634–1644 (2016)

    CAS  PubMed  Google Scholar 

  59. J. Renata, M. Zvonimira, F. Jadranka, M. Ksenija, K. Snježana, M. Jasna, Improved properties and microbiological safety of novel cottage cheese containing spices. Food Technol. Biotechnol. 53(4), 454–462 (2015)

    Google Scholar 

  60. L. Liu, X. Qu, Q. **a, H. Wang, P. Chen, X. Li, L. Wang, W. Yang, Effect of Lactobacillus rhamnosus on the antioxidant activity of Cheddar cheese during ripening and under simulated gastrointestinal digestion. LWT 95, 99–106 (2018)

    CAS  Google Scholar 

  61. O. Ujiroghene, L. Liu, S. Zhang, J. Lu, C. Zhang, X. Pang, J. Lv, Potent α-amylase inhibitory activity of sprouted quinoa-based yoghurt beverages fermented with selected anti-diabetic strains of lactic acid bacteria. RSC Adv. 9(17), 9486–9493 (2019)

    CAS  Google Scholar 

  62. C. Proença, M. Freitas, D. Ribeiro, S. Tomé, E. Oliveira, M. Viegas, A. Araújo, M. Ramos, A. Silva, P. Fernandes, E. Fernandes, Evaluation of a flavonoids library for inhibition of pancreatic α-amylase towards a structure–activity relationship. J. Enzyme Inhib. Med. Chem. 34(1), 577–588 (2019)

    PubMed  PubMed Central  Google Scholar 

  63. A. Yalcin, Emerging therapeutic potential of whey proteins and peptides. Curr. Pharm. Des. 12(13), 1637–1643 (2006)

    CAS  PubMed  Google Scholar 

  64. H. Siow, T. Lim, C. Gan, Development of a workflow for screening and identification of α-amylase inhibitory peptides from food source using an integrated Bioinformatics-phage display approach: Case study—Cumin seed. Food Chem. 214, 67–76 (2017)

    CAS  PubMed  Google Scholar 

  65. M. Alrosan, T. Tan, A. Mat Easa, S. Gammoh, M. Aludatt, Effects of fermentation on the quality, structure, and nonnutritive contents of lentil (Lens culinaris) proteins. J. Food Qual (2021). https://doi.org/10.1155/2021/5556450

    Article  Google Scholar 

  66. C. Zhao, S. Benjakul, J. Eun, Changes in protein compositions and textural properties of the muscle of skate fermented at 10°C. Int. J. Food Prop. 22(1), 173–185 (2019)

    CAS  Google Scholar 

  67. L. Santiago-López, J. Aguilar-Toalá, A. Hernández-Mendoza, B. Vallejo-Cordoba, A. Liceaga, A. González-Córdova, Bioactive compounds produced during cheese ripening and health effects associated with aged cheese consumption. J. Dairy Sci. 101(5), 3742–3757 (2018)

    PubMed  Google Scholar 

  68. L. Amigo, B. Hernández-Ledesma, Current evidence on the bioavailability of food bioactive peptides. Molecules 25(19), 4479 (2020)

    CAS  PubMed Central  Google Scholar 

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Acknowledgements

The authors expressed gratitude to Mr. Booi Chin Hai, laboratory assistant in Department of Bioscience, Faculty of Applied Sciences, Tunku Abdul Rahman University College for his kind assistance in this project.

Funding

This project is supported by teaching activity fund of the Faculty of Applied Science, Tunku Abdul Rahman University College.

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  1. Department of Bioscience, Faculty of Applied Sciences, Tunku Abdul Rahman University College, 53300, Setapak, Kuala Lumpur, Malaysia

    Huei Chin Chew, Pei Ling Tang, **n Yi Tan & Hui Yin Tan

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Contributions

Study conception and design were contributed by PLT. Material preparation, data collection and analysis were performed by XYT. The Lactobacillus plantarum TAR4 strain was isolated by HYT. The first draft of the manuscript was written by HCC and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Pei Ling Tang.

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Chew, H.C., Tang, P.L., Tan, X.Y. et al. Effect of mulberry leaf extract fortification and probiotic fermentation on the bioactivities of cottage cheese. Food Measure 16, 486–499 (2022). https://doi.org/10.1007/s11694-021-01174-4

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