Prebiotic Activity of Plants from Cucurbitaceae Family and In Vitro Fermentation by Gut Microbiota
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Published
31 August 2024
Keywords:
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fecal samples, freeze-dried, gas production, gut microbiota
Abstract
This study aims to examine the effect of Freeze-Dried Pumpkin Powder (FDPP), Freeze-Dried Winter Melon Powder (FDWMP), Freeze-Dried Rock Melon Powder (FDRMP), inulin, and D glucose on prebiotic activity score by in vitro fermentation. We also elucidate the changes in bacterial populations through batch culture fermentation using fecal samples from 5 healthy volunteers and In vitro fecal fermentation using batch culture and analyses of Short-Chain Fatty Acids (SCFAs). The growth of Bifidobacterium has significantly increased from 0 (8.90±0.05 log10 cells/mL) and 72h (8.83±0.14 log10 cells/mL) for D glucose and FDWMP (8.75±0.07 log10 cells/mL (0h) and 8.87±0.12 log10 cells/mL (72h)). However, the increase in population was not significant for inulin (9.15±0.06 log10 cells/mL), FDPP (9.04±0.12 log10 cells/mL), and FDRMP (8.67±0.08 log10 cells/mL). The number of Lactobacili significantly increased at 6h for FDPP (9.11±0.07 log10 cells/mL) and 24h for FDWMP (8.88±0.07 log10 cells/mL) and FDRMP (8.80±0.09 log10 cells/mL). Acetic acid was detected in all samples, and the concentration increased in all vessels at any given time except for the FDWMP fermentation, which decreased after 0h and increased after 6h. Overall, FDWMP has increased the probiotic growth of L. plantarum TISTR 1465 and exhibit the highest prebiotic index. As a result, it is suggested that the FDWMP be potentially used as a healthy raw material in developing varieties of functional prebiotic food products.
References
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Ariestanti CA, Seechamnanturakit V, Harmayani E, Wichienchot S 2019. Optimization on production of konjac oligo-glucomannan and their effect on the gut microbiota. Food Sci & Nutri 7(2):788−796. https://doi.org/10.1002/fsn3.927
Bergantin C, Maietti A, Tedeschi P, Font G, Manyes L, Marchetti N. 2018. HPLC-UV/Vis-APCI-MS/MS determination of major carotenoids and their bioaccessibility from Delica (Cucurbita maxima) and Violina (Cucurbita moschata) pumpkins as food traceability markers. Molecules 23(11):2791. https://doi.org/10.3390/molecules23112791
Borges JM, Lucarini M, Durazzo A. 2023. Effect of freezing and freeze-drying on bioactive compounds and antioxidant activity of carnauba pulp (Copernicia prunifera (Mill.) HE Moore). MOJ Food Process Technols 11(2):78−82. https://doi.org/10.15406/mojfpt.2023.11.00284
Bhatta S, Stevanovic Janezic T, Ratti C. 2020. Freeze-drying of plant-based foods. Foods 9(1):87. https://doi.org/ 10.3390/foods9010087
Dávila I, Gullón B, Alonso JL, Labidi J, Gullón P. 2019. Vine shoots as new source for the manufacture of prebiotic oligosaccharides. Carbohydr Polym 207:34–43. doi:10.1016/j.carbpol.2018.11.065. https://doi.org/10.1016/j.carbpol.2018.11.065
de Andrade RMS, Silva S, Costa CM, Veiga M, Costa E, Ferreira MSL, Pintado ME. 2020. Potential prebiotic effect of fruit and vegetable byproducts flour using in vitro gastrointestinal digestion. Food Res Int 137: 109354. https://doi.org/10.1016/j.foodres.2020.109354
Do, TVT, Fan L. 2019. Probiotic Viability, Qualitative Characteristics, and Sensory Acceptability of Vegetable Juice Mixture Fermented with Lactobacillus Strains. Food and Nutrition Sciences 10(04):412–427. doi:10.4236/fns.2019.104031. https://doi.org/10.4236/fns.2019.104031
Duan X, Yang X, Ren G, Pang Y, Liu L, Liu Y. 2016. Technical aspects in freeze-drying of foods. Dry Technol 34(11):1271–1285. https://doi.org/10.1080/07373937.2015.1099545
Frank DN, Pace NR. 2008. Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 24(1):4–10. http://doi.org/10.1097/MOG.0b013e3282f2b0e8
Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T et al. 2013. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446−450. http://doi.org/10.1038/nature12721
Ghoddusi HB, Grandison MA, Grandison AS, Tuohy KM. 2007. In vitro study on gas generation and prebiotic effects of some carbohydrates and their mixtures. Anaerobe 13(5−6):193−199. http://doi.org/10.1016/j.anaerobe.2007.06.002
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S et al. 2014. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506−514. https://doi.org/10.1038/nrgastro.2014.66
Islam MT, Quispe C, El-Kersh DM, Shill MC, Bhardwaj K, Bhardwaj P, Cho WC. 2021. A literature-based update on Benincasa hispida (Thunb.) Cogn.: traditional uses, nutraceutical, and phytopharmacological profiles. Oxidative Medicine and Cellular Longevity Vol 2021, Article ID 6349041. https://doi.org/10.1155/2021/6349041
Karam MC, Petit J, Zimmer D, Djantou EB, Scher J. 2016. Effects of drying and grinding in production of fruit and vegetable powders: A review. J. Food Eng 188:32–49. https://doi.org/10.1016/j.jfoodeng.2016.05.001
Kiharason JW, Isutsa DK, Ngoda PN. 2017. Effect of drying method on nutrient integrity of selected components of pumpkin (Cucurbita moschata Duch.) fruit flour. ARPN J of Agric and Biol Sci 12(3):110−116.
Kittibunchakul S, Temviriyanukul P, Chaikham P, Kemsawasd V. 2023. Effects of freeze drying and convective hot-air drying on predominant bioactive compounds, antioxidant potential and safe consumption of maoberry fruits. LWT 184:114992. https://doi.org/10.1016/j.lwt.2023.114992
Liu Z, Lin X, Huang G, Zhang W, Rao P, Ni L. 2014. Prebiotic effects of almonds and almond skins on intestinal microbiota in healthy adult humans. Anaerobe, 26:1–6. https://doi.org/10.1016/j.anaerobe.2013.11.007
Men X, Choi SI, Han X, Kwon HY, Jang GW, Choi YE, Lee OH. 2021. Physicochemical, nutritional and functional properties of Cucurbita moschata. Food Sci and Biotechnol 30:171−183. https://doi.org/10.1007/s10068-020-00835-2
Mohammad NA, Anwar F, Mehmood T, Hamid AA, Muhammad K, Saari, N. 2019. Phenolic compounds, tocochromanols profile and antioxidant properties of winter melon [Benincasa hispida (Thunb.) Cogn.] seed oils. J Food Meas Charact 13:940−948. https://doi.org/10.1007/s11694-018-0008-x
Ng YV, Tengku Ismail TA, Wan Ishak WR. 2020. Effect of overripe banana in developing high dietary fibre and low glycaemic index cookie. Br Food J 122(10):3165−3177. https://doi.org/10.1108/BFJ-12-2019-0934
Ojo A, Abiodun OA, Odedeji JO, Akintoyese OA. 2014. Effects of Drying Methods on Proximate and Physico-chemical Properties of Fufu Flour Fortified with Soybean. Br J Appl Sci Technol 4(14):2079−2089. http://doi.org/10.9734/bjast/2014/8984
Promjiam P, Siripongvutikorn S, Wichienchot S. 2017. Functional properties of curry paste in relation to digestibility and fermentation by gut microbiota. Int J of Food Properties 20:3204–3214. http://doi.org/10.1080/10942912.2017.1282515
Ríos-Covian D, Ruas-Madiedo P, Margolles A, Gueimonde M, De los Reyes-Gavilán CG, Salazar N. 2016. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol 7:1−9. http://doi.org/10.3389/fmicb.2016.00185
Siti Mahirah Y, Rabeta MS, Antora RA. 2018. Effects of different drying methods on the proximate composition and antioxidant activities of ocimum basilicum leaves. Food Res 2:421–428. http://doi.org/10.26656/fr.2017.2(5).083
Sommer F, Bäckhed F. 2013. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 11:227−238. http://doi.org/10.1038/nrmicro2974
Sreenivas KM, Lele SS. 2013. Prebiotic activity of gourd family vegetable fibers using in vitro fermentation. Food Biosci 1:26−30. http://doi.org/10.1016/j.fbio.2013.01.002
Tomas-Barberan FA, Selma MV, Espín JC. 2016. Interactions of gut microbiota with dietary polyphenols and consequences to human health. In Current opinion in clinical nutrition and metabolic care. 19(6):471–476. https://doi.org/10.1097/MCO.0000000000000314
Thursby E, Juge N. 2017. Introduction to the human gut microbiota. Biochem J 474: 1823–1836. http://doi.org/10.1042/BCJ20160510
Wang A, Lin J, Zhong Q. 2020. Probiotic Powders Prepared by Mixing Suspension of Lactobacillus salivarius NRRL B-30514 and Spray-Dried Lactose: Physical and Microbiological Properties. Food Res Int 127:108706. http://doi.org/10.1016/j.foodres.2019.108706
Wang M, Wichienchot S, He X, Fu X, Huang Q, Zhang B. 2019. In vitro colonic fermentation of dietary fibers: Fermentation rate, short-chain fatty acid production and changes in microbiota. Trends Food Sci Technol 88:1−9. http://doi.org/10.1016/j.tifs.2019.03.005
Ying WS, Dian NLHM, Wasoh H, Ming LO. 2018. Formulation of a low glycaemic binder fortified with palm Vitamin E (tocotrienol-rich fraction) for functional granola bars. J Oil Palm Res 30:591−601. http://doi.org/10.21894/jopr.2018.0049
Zhou L, Wang W, Huang J, Ding Y, Pan Z, Zhao Y, Zhang R, Hu B, Zeng X. 2016. In vitro extraction and fermentation of polyphenols from grape seeds (Vitis vinifera) by human intestinal microbiota. Food Funct 7:1959−1967. http://doi.org/10.1039/c6fo00032k
Ahire ED, Sharma N, Gupta PC, Khairnar S, Surana K, Ahire B, Kshirsagar S. 2022. Developing formulations of prebiotics and probiotics. Prebio and Probio in Disease Reg and Manage 271−290.
Alfilasari N, Sirivongpaisal P, Wichienchot S. 2021. Gut health function of instant dehydrated rice sticks substituted with resistant starch types 2 and 4. Curr Microbiol 78(8):3010−3019. http://doi.org/10.1007/s00284-021-02564-z
[AOAC] Association of Official Analytical Chemists. 2020. Official Methods of Analysis of AOAC International - 20th Edition. Maryland (USA): AOAC International.
Ariestanti CA, Seechamnanturakit V, Harmayani E, Wichienchot S 2019. Optimization on production of konjac oligo-glucomannan and their effect on the gut microbiota. Food Sci & Nutri 7(2):788−796. https://doi.org/10.1002/fsn3.927
Bergantin C, Maietti A, Tedeschi P, Font G, Manyes L, Marchetti N. 2018. HPLC-UV/Vis-APCI-MS/MS determination of major carotenoids and their bioaccessibility from Delica (Cucurbita maxima) and Violina (Cucurbita moschata) pumpkins as food traceability markers. Molecules 23(11):2791. https://doi.org/10.3390/molecules23112791
Borges JM, Lucarini M, Durazzo A. 2023. Effect of freezing and freeze-drying on bioactive compounds and antioxidant activity of carnauba pulp (Copernicia prunifera (Mill.) HE Moore). MOJ Food Process Technols 11(2):78−82. https://doi.org/10.15406/mojfpt.2023.11.00284
Bhatta S, Stevanovic Janezic T, Ratti C. 2020. Freeze-drying of plant-based foods. Foods 9(1):87. https://doi.org/ 10.3390/foods9010087
Dávila I, Gullón B, Alonso JL, Labidi J, Gullón P. 2019. Vine shoots as new source for the manufacture of prebiotic oligosaccharides. Carbohydr Polym 207:34–43. doi:10.1016/j.carbpol.2018.11.065. https://doi.org/10.1016/j.carbpol.2018.11.065
de Andrade RMS, Silva S, Costa CM, Veiga M, Costa E, Ferreira MSL, Pintado ME. 2020. Potential prebiotic effect of fruit and vegetable byproducts flour using in vitro gastrointestinal digestion. Food Res Int 137: 109354. https://doi.org/10.1016/j.foodres.2020.109354
Do, TVT, Fan L. 2019. Probiotic Viability, Qualitative Characteristics, and Sensory Acceptability of Vegetable Juice Mixture Fermented with Lactobacillus Strains. Food and Nutrition Sciences 10(04):412–427. doi:10.4236/fns.2019.104031. https://doi.org/10.4236/fns.2019.104031
Duan X, Yang X, Ren G, Pang Y, Liu L, Liu Y. 2016. Technical aspects in freeze-drying of foods. Dry Technol 34(11):1271–1285. https://doi.org/10.1080/07373937.2015.1099545
Frank DN, Pace NR. 2008. Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 24(1):4–10. http://doi.org/10.1097/MOG.0b013e3282f2b0e8
Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T et al. 2013. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446−450. http://doi.org/10.1038/nature12721
Ghoddusi HB, Grandison MA, Grandison AS, Tuohy KM. 2007. In vitro study on gas generation and prebiotic effects of some carbohydrates and their mixtures. Anaerobe 13(5−6):193−199. http://doi.org/10.1016/j.anaerobe.2007.06.002
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S et al. 2014. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506−514. https://doi.org/10.1038/nrgastro.2014.66
Islam MT, Quispe C, El-Kersh DM, Shill MC, Bhardwaj K, Bhardwaj P, Cho WC. 2021. A literature-based update on Benincasa hispida (Thunb.) Cogn.: traditional uses, nutraceutical, and phytopharmacological profiles. Oxidative Medicine and Cellular Longevity Vol 2021, Article ID 6349041. https://doi.org/10.1155/2021/6349041
Karam MC, Petit J, Zimmer D, Djantou EB, Scher J. 2016. Effects of drying and grinding in production of fruit and vegetable powders: A review. J. Food Eng 188:32–49. https://doi.org/10.1016/j.jfoodeng.2016.05.001
Kiharason JW, Isutsa DK, Ngoda PN. 2017. Effect of drying method on nutrient integrity of selected components of pumpkin (Cucurbita moschata Duch.) fruit flour. ARPN J of Agric and Biol Sci 12(3):110−116.
Kittibunchakul S, Temviriyanukul P, Chaikham P, Kemsawasd V. 2023. Effects of freeze drying and convective hot-air drying on predominant bioactive compounds, antioxidant potential and safe consumption of maoberry fruits. LWT 184:114992. https://doi.org/10.1016/j.lwt.2023.114992
Liu Z, Lin X, Huang G, Zhang W, Rao P, Ni L. 2014. Prebiotic effects of almonds and almond skins on intestinal microbiota in healthy adult humans. Anaerobe, 26:1–6. https://doi.org/10.1016/j.anaerobe.2013.11.007
Men X, Choi SI, Han X, Kwon HY, Jang GW, Choi YE, Lee OH. 2021. Physicochemical, nutritional and functional properties of Cucurbita moschata. Food Sci and Biotechnol 30:171−183. https://doi.org/10.1007/s10068-020-00835-2
Mohammad NA, Anwar F, Mehmood T, Hamid AA, Muhammad K, Saari, N. 2019. Phenolic compounds, tocochromanols profile and antioxidant properties of winter melon [Benincasa hispida (Thunb.) Cogn.] seed oils. J Food Meas Charact 13:940−948. https://doi.org/10.1007/s11694-018-0008-x
Ng YV, Tengku Ismail TA, Wan Ishak WR. 2020. Effect of overripe banana in developing high dietary fibre and low glycaemic index cookie. Br Food J 122(10):3165−3177. https://doi.org/10.1108/BFJ-12-2019-0934
Ojo A, Abiodun OA, Odedeji JO, Akintoyese OA. 2014. Effects of Drying Methods on Proximate and Physico-chemical Properties of Fufu Flour Fortified with Soybean. Br J Appl Sci Technol 4(14):2079−2089. http://doi.org/10.9734/bjast/2014/8984
Promjiam P, Siripongvutikorn S, Wichienchot S. 2017. Functional properties of curry paste in relation to digestibility and fermentation by gut microbiota. Int J of Food Properties 20:3204–3214. http://doi.org/10.1080/10942912.2017.1282515
Ríos-Covian D, Ruas-Madiedo P, Margolles A, Gueimonde M, De los Reyes-Gavilán CG, Salazar N. 2016. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol 7:1−9. http://doi.org/10.3389/fmicb.2016.00185
Siti Mahirah Y, Rabeta MS, Antora RA. 2018. Effects of different drying methods on the proximate composition and antioxidant activities of ocimum basilicum leaves. Food Res 2:421–428. http://doi.org/10.26656/fr.2017.2(5).083
Sommer F, Bäckhed F. 2013. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 11:227−238. http://doi.org/10.1038/nrmicro2974
Sreenivas KM, Lele SS. 2013. Prebiotic activity of gourd family vegetable fibers using in vitro fermentation. Food Biosci 1:26−30. http://doi.org/10.1016/j.fbio.2013.01.002
Tomas-Barberan FA, Selma MV, Espín JC. 2016. Interactions of gut microbiota with dietary polyphenols and consequences to human health. In Current opinion in clinical nutrition and metabolic care. 19(6):471–476. https://doi.org/10.1097/MCO.0000000000000314
Thursby E, Juge N. 2017. Introduction to the human gut microbiota. Biochem J 474: 1823–1836. http://doi.org/10.1042/BCJ20160510
Wang A, Lin J, Zhong Q. 2020. Probiotic Powders Prepared by Mixing Suspension of Lactobacillus salivarius NRRL B-30514 and Spray-Dried Lactose: Physical and Microbiological Properties. Food Res Int 127:108706. http://doi.org/10.1016/j.foodres.2019.108706
Wang M, Wichienchot S, He X, Fu X, Huang Q, Zhang B. 2019. In vitro colonic fermentation of dietary fibers: Fermentation rate, short-chain fatty acid production and changes in microbiota. Trends Food Sci Technol 88:1−9. http://doi.org/10.1016/j.tifs.2019.03.005
Ying WS, Dian NLHM, Wasoh H, Ming LO. 2018. Formulation of a low glycaemic binder fortified with palm Vitamin E (tocotrienol-rich fraction) for functional granola bars. J Oil Palm Res 30:591−601. http://doi.org/10.21894/jopr.2018.0049
Zhou L, Wang W, Huang J, Ding Y, Pan Z, Zhao Y, Zhang R, Hu B, Zeng X. 2016. In vitro extraction and fermentation of polyphenols from grape seeds (Vitis vinifera) by human intestinal microbiota. Food Funct 7:1959−1967. http://doi.org/10.1039/c6fo00032k
Authors
Ab AzidS. M., WichienchotS., Wan IshakW. R., & SafuanS. (2024). Prebiotic Activity of Plants from Cucurbitaceae Family and In Vitro Fermentation by Gut Microbiota. Jurnal Gizi Dan Pangan, 19(Supp.2), 342-351. https://doi.org/10.25182/jgp.2024.19.Supp.2.342-351
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