Effect of in vitro gastrointestinal digestion on the release of phytochemicals from nanche (Byrsonima crassifolia L.) fruit
Keywords:
Antioxidant capacity, Byrsonima crassifolia, phenolic compounds, phytochemicals.Abstract
The nanche fruit (Byrsonima crassifolia L.) represents an important nutritional source due to its high content of fiber, vitamins and minerals, as well as phytochemicals with biological activity. The objective of this investigation was to evaluate the release of phytochemicals during gastrointestinal digestion using an in vitro digestion model that simulates chemical and biological conditions, and to study changes in antioxidant activity during the digestion process. The results of the research showed that the fruits of the UAA1 selection showed the highest content of total soluble phenols in the chemical extraction (35 mg EAG/g) as well as in the gastric (11.02 mg EAG/g) and intestinal (8.9 mg GAE/g) stages. The transition from the acid environment to alkaline conditions caused a decrease in the amount of hydrolysable polyphenols. As for total flavonoids, these increased when passing to the intestinal phase. The stability of phenolic compounds to pH changes in the different stages of digestion affected their bioavailability, even though about 35 to 45% of the total phenol content was released in the gastric stage, these compounds decreased when passing to the intestinal stage. The changes in antioxidant activity during in vitro digestion correlated with changes in flavonoid concentration as well as pH. The fruits of the UAA1 selection showed the highest antioxidant capacity both gastric and intestinal levels. For the ABTS test, the fruits of the UAA1 selection presented a higher antioxidant capacity in the gastric stage (561 mmol ET/g). Regarding the intestinal stage, the UAA1 selection showed higher antioxidant capacity in the DPPH (763 mmol ET/g) and FRAP (1326 mmol ET/g) assays. The chemical extract of the UAA1 selection showed an antioxidant activity measured with the FRAP assay of 1442 mmol TE/g of nanche on a dry basis. The antioxidant activity measured at the end of the digestion procedure was 1326 mmol TE/g of butter on a dry basis, corresponding to 91% of the total antioxidant activity in the chemical extract. In conclusion, due to their intrinsic characteristics, the nanche fruits of the UAA1 selection could be used to obtain phytochemicals with applications in the development of functional foods.
References
1. Palafox‐Carlos, H., Ayala‐Zavala, J.F and González‐Aguilar, G.A. (2011). The Role of Dietary Fiber in the Bioaccessibility and Bioavailability of Fruit and Vegetable Antioxidants. Journal of Food Science, 76(1):R6-R15. https://doi.org/10.1111/j.1750-3841.2010.01957.x
2. De La Rosa, L.A., E. Álvarez-Parrilla y G. González-Aguilar. (2010). Fruit and Vegetable Phytochemicals: Chemistry, Nutritional Value and Stability. Wiley-Blackwell, 367.
3. CONABIO. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. 2020. Catálogo de autoridades taxonómicas de especies de flora y fauna con distribución en México. Base de datos SNIB-CONABIO Internet: https://www.snib.mx/descargasSNIBmx/SNIBTaxonomia_20220504_162249.zip (Accessed September 20, 2020)
4. Pires, F. C. S., Silva, A. P. de S. e, Salazar, M. de los A. R., Costa, W. A. da, Costa, H. S. C. da, Lopes, A. S.,Carvalho Junior, R. N. de. (2019). Determination of process parameters and bioactive properties of the murici pulp (Byrsonima crassifolia) extracts obtained by supercritical extraction. The Journal of Supercritical Fluids, 146, 128–135. https://doi.org/10.1016/j.supflu.2019.01.014
5. Rodrigues, S. M., Moura, E. F., Ramos, G. K., Oliveira, M. S. (2016). Genetic variability analysis of Byrsonima crassifolia germplasm collected in Pará state using ISSR markers. Genetics and Molecular Research, 15(4). https://doi.org/10.4238/gmr15048887
6. Mariutti, L. R. B., Rodrigues, E and Mercadante, A. Z. (2013). Carotenoids from Byrsonima crassifolia: Identification, quantification and in vitro scavenging capacity against peroxyl radicals. Journal of Food Composition and Analysis, 31(1), 155–160.
https://doi.org/10.1016/j.jfca.2013.05.005
7. López, E., Navarro, A., Manchón, N and Herrera, J. (2014). Componentes funcionales en Nanche (Byrsonima crassifolia (L) Kunth). Ciencias Agropecuarias, Handbook, ed. ECORFAN, Valle de Santiago, Guanajuato, 6-22.
8. Alamed, J., Chaiyasit, W., McClements, D. J. and Decker, E. A. (2009). Relationships between free radical scavenging and antioxidant activity in foods. Journal of Agricultural and Food Chemistry, 57(7), 2969-2976. https://doi.org/10.1021/jf803436c
9. Saura-Calixto, F., Serrano, J., Goñi, I. (2007). Intake and bioaccessibility of total polyphenols in a whole diet. Food Chemistry. 101, 492-501. https://doi.org/10.1016/j.foodchem.2006.02.006
10. Bohn, T. (2014). Dietary factors affecting polyphenol bioavailability. Nutrition Reviews. 72, 429–452. https://doi.org/10.1111/nure.12114
11. Manach, C., G. Williamson, C. Morand, A. Scalbert and C. Rémésy. (2005). Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. The American Journal of Clinical Nutrition, 81(1):230S-242S. https://doi.org/10.1093/ajcn/81.1.230S
12. Crozier, A., Jaganath, I., B, Clifford, M., N. (2009). Dietary phenolics: chemistry, bioavailability and effects on health. Natural Product Reports, 26, 1001–1043. https://doi.org/10.1039/b802662a
13. Bouayed, J., Deußer, H., Hoffmann, L. and Bohn, T. (2012). Bioaccessible and dialysable polyphenols in selected apple varieties following in vitro digestion vs. their native patterns. Food Chemistry, 131(4), 1466-1472. https://doi.org/10.1016/j.foodchem.2011.10.030
14. Saura-Calixto, F., Garcia-Alonso, A., Goni, I., Bravo, L. (2000). In vitro determination of the indigestible fraction in foods: An alternative to dietary fiber analysis. Journal of Agricultural and Food Chemistry. 48, 3342–3347. https://doi.org/10.1021/jf0000373
15. Blancas-Benitez, F.J.; Pérez-Jiménez, J.; Montalvo-González, E.; González-Aguilar, G.A.; Sáyago-Ayerdi, S.G. (2018). In vitro evaluation of the kinetics of the release of phenolic compounds from guava (Psidium guajava L.) fruit. J. Funct. Foods, 43, 139–145.
16. Pérez-Jiménez, J., Arranz, S., Tabernero, M., Díaz-Rubio, M.E., Serrano, J., Goñi, I., Saura-Calixto, F. (2008). Updated methodology to determine antioxidant capacity in plant foods, oils and beverages: Extraction, measurement and expression of results. Food Research. 41, 274–285. https://doi.org/10.1016/j.foodres.2007.12.004
17. Hartzfeld, P.W., Forkner, R., Hunter, M.D., and Hagerman, A.E. (2002). Determination of hydrolyzable tannins (gallotannins and ellagitannins) after reaction with potassium iodate. Journal of Agricultural and Food Chemistry, 50(7):1785-1790. https://doi.org/10.1021/jf0111155
18. Montreau, F. (1972). Sur le dosage des composés phénoliques totaux dans les vins par la méthode Folin-Ciocalteau. Connais Vigne Vin, 24, 397-404.
19. Oomah, B.D., Cardador-Martínez, A. and Loarca-Piña, G. (2005), Phenolics and antioxidative activities in common beans (Phaseolus vulgaris L). Journal of the Science of Food and Agriculture. 85: 935-942. https://doi.org/10.1002/jsfa.2019
20. Benzie, I and Strain, J. (1996). The Ferric Reducing Ability of Plasma (FRAP) as a measure of Antioxidant Power. The FRAP Assay. Analytical Biochemistry. 239, 70-76. https://doi.org/10.1006/abio.1996.0292
21. Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26(9–10), 1231–1237. https://doi.org/10.1016/s0891-5849(98)00315-3
22. Brand-Williams, W., Cuvelier, M. E., and Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT - Food Science and Technology, 28(1), 25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
23. Tagliazucchi, D., Verzelloni, E., Bertolini, D. and Conte, A. (2010). In vitro bioaccessibility and antioxidant activity of grape polyphenols. Food Chemistry 120(2):599-606. https://doi.org/10.1016/j.foodchem.2009.10.030
24. Rodríguez-Roque, M. J., Rojas-Graü, M. A., Elez-Martínez, P., Martín-Belloso, O. (2013). Soymilk phenolic compounds, isoflavones and antioxidant activity as affected by in vitro gastrointestinal digestion. Food chemistry, 136(1), 206-212. https://doi.org/10.1016/j.foodchem.2012.07.115
25. Lafay, S and Gil-Izquierdo, A. (2008). Bioavailability of phenolic acids. Phytochemistry Reviews. 7(2):301-311. https://doi.org/10.1007/s11101-007-9077-x
26. Paull, R. E. (1997). Postharvest physiology and storage of tropical and subtropical fruits. In S. K. Mitra (Ed.). Pineapple (pp.123-143). New York: CAB INTERNATIONAL.
27. Agredano-De la Garza, C.S., Balois-Morales, R., Berumen-Varela, G., León-Fernández, A.E., Bautista-Rosales, P.U., López-Guzmán, G.G., Pérez-Ramírez, I.F.(2021). Physicochemical characterization and dietary fiber of 15 Nance (Byrsonima crassifolia L.) fruits selections from Nayarit. Scientia Horticulturae. 289, Article 110460. https://doi.org/10.1016/j.scienta.2021.110460
28. Arranz, S. and Saura-Calixto, F. (2010). Analysis of polyphenols in cereals may be improved performing acidic hydrolysis: a study in wheat flour and wheat bran and cereals of the diet. Journal of Cereal Science, 51, 313-318. https://doi.org/10.1016/j.jcs.2010.01.006
29. García-Gutiérrez, N., Maldonado-Celis, M.E., Rojas-Lopez, M., Loarca-Pina, G.F. and Campos-Vega, R. (2017). The fermented non-digestible fraction of spent coffee grounds induces apoptosis in human colon cancer cells (SW480). Journal of Functional Foods, 30, 237–246. https://doi.org/10.1016/j.jff.2017.01.014
30. Alminger, M., Aura, A. M., Bohn, T., Dufour, C., El, S. N., Gomes, A., Karakaya, S., Martínez-Costa, M. C., McDougall, G. J., Requena, T., Santos, C. N. (2014). In vitro models for studying secondary plant metabolite digestion and bioaccessibility. Comprehensive Reviews in Food Science and Food Safety, 13(4), 413–436. https://doi.org/10.1111/1541-4337.12081
31. Krook, M. A and Hagerman, A. E. (2012). Stability of polyphenols epigallocatechin gallate and pentagalloyl glucose in a simulated digestive system. Food Research International, 49(1), 112-116. https://doi.org/10.1016/j.foodres.2012.08.004
32. Gee J., M, Dupont M., S, Rhodes M., JC, and Johnson I., T. (1998). Quercetin glucosides interact with the intestinal glucose transport pathway. Free Radical Biology and Medicine, 25(1): 19-25. https://doi.org/10.1016/s0891-5849(98)00020-3
33. Crespy, V., Morand, C., Besson, C., Manach, C. (2002). Quercetin, but not Its Glycosides, Is Absorbed from the Rat Stomach. Journal of Agricultural and Food Chemistry. 50(3): 618-621. https://doi.org/10.1021/jf010919h
34. Bily, A. C, L. M. Reid, H. H. Taylor, D. Johnston, C. Malouin, A. J. Burt, B. Bakan, C. Regnault–Roger, K. P. Pauls, J. T. Arnason, and B. J. R. Philogene. (2003). Dehydrodimers of ferulic acid in maize grain pericarp and aleurone: resistance factors to Fusarium graminearum. Phytopathology, 93 (6): 712–719. https://doi.org/10.1094/PHYTO.2003.93.6.712
35. Hur, S.J., B.O. Lim, E.A. Decker and D.J. McClements. (2011). In vitro human digestion models for food applications. Food Chemistry, 125(1):1-12. https://doi.org/10.1016/j.foodchem.2010.08.036
36. Hernández-Maldonado, L.M., Blancas-Benítez, F.J., Zamora-Gasga, V.M., Cárdenas-Castro, A.P., Tovar, J., Sáyago-Ayerdi, S.G. (2019). In vitro Gastrointestinal Digestion and Colonic Fermentation of High Dietary Fiber and Antioxidant-Rich Mango (Mangifera indica L.) “Ataulfo”-Based Fruit Bars. Nutrients, 11, 1564. https://doi.org/10.3390/nu11071564
37. Kosinska-Cagnazzo, A., Diering, S., Prim, D and Andlauer, W. (2015). Identification of bioaccessible and uptaken phenolic compounds from strawberry fruits in in vitro digestion/Caco-2 absorption model. Food chemistry, 170, 288–294. https://doi.org/10.1016/j.foodchem.2014.08.070
38. Masibo, M. and Q. He. (2008). Major Mango Polyphenols and Their Potential Significance to Human Health. Comprehensive Reviews in Food Science and Food Safety. 7(4):309-319. DOI:10.1111/j.1541-4337.2008.00047.x
39. Jovanovic, S.V, Steenken, S., Simic, M. G and Hara, Y. (1998). Antioxidant properties of flavonoids: reduction potentials and electron transfer reactions of flavonoid radicals. In: Rice Evans C, Parker L (eds.): Flavonoids in health and disease. Marcel Dekker, Nueva York, 137-161.
40. Martínez-Flórez, S., J. González-Gallego, J.M. Culebras & Mª J. Tuñón. (2002). Los flavonoides: propiedades y acciones antioxidantes. Nutrición Hospitalaria. XVII. 6: 271-278.
41. Mukai, K., Oka, W., Watanabe, K., Egawa, Y., and Nagaoka, S. (1997). Kinetic study of free-radical-scavenging action of flavonoids in homogeneous and aqueous triton X-100 micellar solutions. Journal of Physical Chemistry A, 101, 3746–3753. https://doi.org/10.1021/jp9706745
