Influence of Fermentation with Different Lactic Acid Bacteria and in Vitro Digestion on the Biotransformation of Phenolic Compounds in Fermented Pomegranate Juices

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 31, 2017, Pages 6488-6496

  Valero Cases, Estefanía ^a   Nuncio Jáuregui, Nallely ^a   Frutos, María José ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

antioxidant capacity; Bifidobacterium; bioactive compounds; Lactobacillus; probiotic

Indexed keywords

ANTIOXIDANTS; BACTERIA; BIOCONVERSION; FERMENTATION; FLAVONOIDS; FRUIT JUICES; LABORATORIES; LACTIC ACID; ORGANIC COMPOUNDS;

ANTIOXIDANT CAPACITY; BIFIDOBACTERIUM; BIOACTIVE COMPOUNDS; LACTOBACILLUS; PROBIOTICS;

PHENOLS;

PHENOL DERIVATIVE;

ANALYSIS; BIOLOGICAL MODEL; BIOTRANSFORMATION; CHEMISTRY; DIGESTION; FERMENTATION; FRUIT AND VEGETABLE JUICE; GASTROINTESTINAL TRACT; HUMAN; INTESTINE FLORA; LACTOBACILLUS; LYTHRACEAE; METABOLISM; MICROBIOLOGY;

BIOTRANSFORMATION; DIGESTION; FERMENTATION; FRUIT AND VEGETABLE JUICES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; LACTOBACILLUS; MODELS, BIOLOGICAL; PHENOLS; PUNICACEAE;

EID: 85024875776     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b04854     Document Type: Article

References (44)

1. Lewandowska, U.; Szewczyk, K.; Hrabec, E.; Janecka, A.; Gorlach, S. Overview of metabolism and bioavailability enhancement of polyphenols J. Agric. Food Chem. 2013, 61, 12183-12199 10.1021/jf404439b
2. Etxeberria, U.; Fernandez-Quintela, A.; Milagro, F. I.; Aguirre, L.; Martinez, J. A.; Portillo, M. P. Impact of polyphenols and polyphenol-rich dietary sources on gut microbiota composition J. Agric. Food Chem. 2013, 61, 9517-9533 10.1021/jf402506c
3. Fernandez-Garcia, E.; Carvajal-Lerida, I.; Perez-Galvez, A. In vitro bioaccessibility assessment as a prediction tool of nutritional efficiency Nutr. Res. (N. Y., NY, U. S.) 2009, 29, 751-760 10.1016/j.nutres.2009.09.016
4. Chandrasekara, A.; Shahidi, F. Bioaccessibility and antioxidant potential of millet grain phenolics as affected by simulated in vitro digestion and microbial fermentation J. Funct. Foods 2012, 4, 226-237 10.1016/j.jff.2011.11.001
5. Mosele, J. I.; Macià, A.; Romero, M.-P.; Motilva, M.-J.; Rubió, L. Application of in vitro gastrointestinal digestion and colonic fermentation models to pomegranate products (juice, pulp and peel extract) to study the stability and catabolism of phenolic compounds J. Funct. Foods 2015, 14, 529-540 10.1016/j.jff.2015.02.026
6. Moco, S.; Martin, F. P.; Rezzi, S. Metabolomics view on gut microbiome modulation by polyphenol-rich foods J. Proteome Res. 2012, 11, 4781-4790 10.1021/pr300581s
7. Pandareesh, M. D.; Mythri, R. B.; Srinivas Bharath, M. M. Bioavailability of dietary polyphenols: factors contributing to their clinical application in CNS diseases Neurochem. Int. 2015, 89, 198-208 10.1016/j.neuint.2015.07.003
8. Viuda-Martos, M.; Fernández-López, J.; Pérez-álvarez, J. A. Pomegranate and its many functional components as related to human health: a review Compr. Rev. Food Sci. Food Saf. 2010, 9, 635-654 10.1111/j.1541-4337.2010.00131.x
9. Gomez-Caravaca, A. M.; Verardo, V.; Toselli, M.; Segura-Carretero, A.; Fernandez-Gutierrez, A.; Caboni, M. F. Determination of the major phenolic compounds in pomegranate juices by HPLC-DAD-ESI-MS J. Agric. Food Chem. 2013, 61, 5328-5337 10.1021/jf400684n
10. Tomas-Barberan, F. A.; Garcia-Villalba, R.; Gonzalez-Sarrias, A.; Selma, M. V.; Espin, J. C. Ellagic acid metabolism by human gut microbiota: consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status J. Agric. Food Chem. 2014, 62, 6535-6538 10.1021/jf5024615
11. Cueva, C.; Moreno-Arribas, M. V.; Martin-Alvarez, P. J.; Bills, G.; Vicente, M. F.; Basilio, A.; Rivas, C. L.; Requena, T.; Rodriguez, J. M.; Bartolome, B. Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria Res. Microbiol. 2010, 161, 372-382 10.1016/j.resmic.2010.04.006
12. Filannino, P.; Bai, Y.; Di Cagno, R.; Gobbetti, M.; Ganzle, M. G. Metabolism of phenolic compounds by Lactobacillus spp. during fermentation of cherry juice and broccoli puree Food Microbiol. 2015, 46, 272-279 10.1016/j.fm.2014.08.018
13. Filannino, P.; Azzi, L.; Cavoski, I.; Vincentini, O.; Rizzello, C. G.; Gobbetti, M.; Di Cagno, R. Exploitation of the health-promoting and sensory properties of organic pomegranate (Punica granatum L.) juice through lactic acid fermentation Int. J. Food Microbiol. 2013, 163, 184-192 10.1016/j.ijfoodmicro.2013.03.002
14. Svensson, L.; Sekwati-Monang, B.; Lutz, D. L.; Schieber, A.; Ganzle, M. G. Phenolic acids and flavonoids in nonfermented and fermented red sorghum (Sorghum bicolor (L.) Moench J. Agric. Food Chem. 2010, 58, 9214-9220 10.1021/jf101504v
15. FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food; FAO/WHO: London, ON, Canada, 2002.
16. Mishra, V.; Shah, C.; Mokashe, N.; Chavan, R.; Yadav, H.; Prajapati, J. Probiotics as potential antioxidants: a systematic review J. Agric. Food Chem. 2015, 63, 3615-3626 10.1021/jf506326t
17. Valero-Cases, E.; Frutos, M. J. Effect of different types of encapsulation on the survival of Lactobacillus plantarum during storage with inulin and in vitro digestion LWT-Food Sci. Technol. 2015, 64, 824-828 10.1016/j.lwt.2015.06.049
18. Nuncio-Jáuregui, N.; Nowicka, P.; Munera-Picazo, S.; Hernández, F.; Carbonell-Barrachina, á. A.; Wojdyło, A. Identification and quantification of major derivatives of ellagic acid and antioxidant properties of thinning and ripe Spanish pomegranates J. Funct. Foods 2015, 12, 354-364 10.1016/j.jff.2014.11.007
19. Robles-Sánchez, R. M.; Rojas-Graü, M. A.; Odriozola-Serrano, I.; González-Aguilar, G. A.; Martín-Belloso, O. Effect of minimal processing on bioactive compounds and antioxidant activity of fresh-cut 'Kent' mango (Mangifera indica L.) Postharvest Biol. Technol. 2009, 51, 384-390 10.1016/j.postharvbio.2008.09.003
20. Alberto, M. R.; Gómez-Cordovés, C.; Manca de Nadra, M. Metabolism of gallic acid and catechin by Lactobacillus hilgardii from wine J. Agric. Food Chem. 2004, 52, 6465-6469 10.1021/jf049239f
21. Gullon, B.; Pintado, M. E.; Fernández-López, J.; Pérez-álvarez, J. A.; Viuda-Martos, M. In vitro gastrointestinal digestion of pomegranate peel (Punica granatum) flour obtained from co-products: changes in the antioxidant potential and bioactive compounds stability J. Funct. Foods 2015, 19, 617-628 10.1016/j.jff.2015.09.056
22. Brand-Williams, W.; Cuvelier, M. E.; Berset, C. Use of a free radical method to evaluate antioxidant activity J. Food Sci. Technol. 1995, 28, 25-30 10.1016/S0023-6438(95)80008-5
23. Benzie, I. F. F.; Strain, J. J. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay Anal. Biochem. 1996, 239, 70-76 10.1006/abio.1996.0292
24. Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay Free Radical Biol. Med. 1999, 26, 1231-1237 10.1016/S0891-5849(98)00315-3
25. Herceg, Z.; Kovacevic, D. B.; Kljusuric, J. G.; Jambrak, A. R.; Zoric, Z.; Dragovic-Uzelac, V. Gas phase plasma impact on phenolic compounds in pomegranate juice Food Chem. 2016, 190, 665-672 10.1016/j.foodchem.2015.05.135
26. Mena, P.; Vegara, S.; Marti, N.; Garcia-Viguera, C.; Saura, D.; Valero, M. Changes on indigenous microbiota, colour, bioactive compounds and antioxidant activity of pasteurised pomegranate juice Food Chem. 2013, 141, 2122-2129 10.1016/j.foodchem.2013.04.118
27. Onsekizoglu, P. Production of high quality clarified pomegranate juice concentrate by membrane processes J. Membr. Sci. 2013, 442, 264-271 10.1016/j.memsci.2013.03.061
28. Bala, I.; Bhardwaj, V.; Hariharan, S.; Kumar, M. N. Analytical methods for assay of ellagic acid and its solubility studies J. Pharm. Biomed. Anal. 2006, 40, 206-210 10.1016/j.jpba.2005.07.006
29. González-Sarrías, A.; García-Villalba, R.; Núñez-Sánchez, M. á.; Tomé-Carneiro, J.; Zafrilla, P.; Mulero, J.; Tomás-Barberán, F. A.; Espín, J. C. Identifying the limits for ellagic acid bioavailability: a crossover pharmacokinetic study in healthy volunteers after consumption of pomegranate extracts J. Funct. Foods 2015, 19, 225-235 10.1016/j.jff.2015.09.019
30. Mousavi, Z. E.; Mousavi, S. M.; Razavi, S. H.; Emam-Djomeh, Z.; Kiani, H. Fermentation of pomegranate juice by probiotic lactic acid bacteria World J. Microbiol. Biotechnol. 2011, 27, 123-128 10.1007/s11274-010-0436-1
31. Bouayed, J.; Deußer, H.; Hoffmann, L.; Bohn, T. Bioaccessible and dialysable polyphenols in selected apple varieties following in vitro digestion vs. their native patterns Food Chem. 2012, 131, 1466-1472 10.1016/j.foodchem.2011.10.030
32. Correa-Betanzo, J.; Allen-Vercoe, E.; McDonald, J.; Schroeter, K.; Corredig, M.; Paliyath, G. Stability and biological activity of wild blueberry (Vaccinium angustifolium) polyphenols during simulated in vitro gastrointestinal digestion Food Chem. 2014, 165, 522-531 10.1016/j.foodchem.2014.05.135
33. Kamiloglu, S.; Capanoglu, E. Investigating the in vitro bioaccessibility of polyphenols in fresh and sun-dried figs (Ficus carica L.) Int. J. Food Sci. Technol. 2013, 48, 2621-2629 10.1111/ijfs.12258
34. Larrosa, M.; Garcia-Conesa, M. T.; Espin, J. C.; Tomas-Barberan, F. A. Ellagitannins, ellagic acid and vascular health Mol. Aspects Med. 2010, 31, 513-539 10.1016/j.mam.2010.09.005
35. Jilani, H.; Cilla, A.; Barberá, R.; Hamdi, M. Biosorption of green and black tea polyphenols into Saccharomyces cerevisiae improves their bioaccessibility J. Funct. Foods 2015, 17, 11-21 10.1016/j.jff.2015.05.006
36. Krook, M. A.; Hagerman, A. E. Stability of polyphenols epigallocatechin gallate and pentagalloyl glucose in a simulated digestive system Food Res. Int. 2012, 49, 112-116 10.1016/j.foodres.2012.08.004
37. Marchese, A.; Coppo, E.; Sobolev, A. P.; Rossi, D.; Mannina, L.; Daglia, M. Influence of in vitro simulated gastroduodenal digestion on the antibacterial activity, metabolic profiling and polyphenols content of green tea (Camellia sinensis) Food Res. Int. 2014, 63, 182-191 10.1016/j.foodres.2014.01.036
38. Huang, H.; Sun, Y.; Lou, S.; Li, H.; Ye, X. In vitro digestion combined with cellular assay to determine the antioxidant activity in Chinese bayberry (Myrica rubra Sieb. et Zucc.) fruits: a comparison with traditional methods Food Chem. 2014, 146, 363-370 10.1016/j.foodchem.2013.09.071
39. Chen, G.-L.; Chen, S.-G.; Zhao, Y.-Y.; Luo, C.-X.; Li, J.; Gao, Y.-Q. Total phenolic contents of 33 fruits and their antioxidant capacities before and after in vitro digestion Ind. Crops Prod. 2014, 57, 150-157 10.1016/j.indcrop.2014.03.018
40. Wootton-Beard, P. C.; Moran, A.; Ryan, L. Stability of the total antioxidant capacity and total polyphenol content of 23 commercially available vegetable juices before and after in vitro digestion measured by FRAP, DPPH, ABTS and Folin-Ciocalteu methods Food Res. Int. 2011, 44, 217-224 10.1016/j.foodres.2010.10.033
41. Huang, D.; Ou, B.; Prior, R. L. The chemistry behind antioxidant capacity assays J. Agric. Food Chem. 2005, 53, 1841-1856 10.1021/jf030723c
42. Braicu, C.; Ladomery, M. R.; Chedea, V. S.; Irimie, A.; Berindan-Neagoe, I. The relationship between the structure and biological actions of green tea catechins Food Chem. 2013, 141, 3282-3289 10.1016/j.foodchem.2013.05.122
43. Argyri, K.; Komaitis, M.; Kapsokefalou, M. Iron decreases the antioxidant capacity of red wine under conditions of in vitro digestion Food Chem. 2006, 96, 281-289 10.1016/j.foodchem.2005.02.035
44. Xia, E. Q.; Deng, G. F.; Guo, Y. J.; Li, H. B. Biological activities of polyphenols from grapes Int. J. Mol. Sci. 2010, 11, 622-646 10.3390/ijms11020622