Solid State Bioconversion for Producing Common Bean (Phaseolus vulgaris L.) Functional Flour with High Antioxidant Activity and Antihypertensive Potential

Abstract

The main objective of this investigation was to study the time effect during solid state bioconversion (SSB) on total phenolics content (TPC) and antioxidant activity (AoxA) of common beans to improve antihypertensive functionality. Cooked cotyledons of dehulled common beans were inoculated with a suspension of R. oligosporus NRRL 2710 (1 × 106 spores/mL), and incubated at 35for times of 24, 36, 48, 60, 72, 84, 96 and 108 h (after 108 h the cotyledons showed off odor). Flours from bioprocessed dehulled common bean from each incubation time were blended with their corresponding milled seed coats. The best time for producing bioprocessed common bean (added with seed coats) functional flour with the highest AoxA (ORAC value = 17,468 μmol Trolox equivalents (TE)/100 gsample, dw; ABTS value = 13,505 μmol TE/100 gsample, dw) was 108 h. The SSB process substantially increased TPC and total hydrophilic AoxA and antihypertensive potential of common beans in 2.24, 2.45 - 2.73 and 6769 times, respectively. Proteins hydrolyzates from unprocessed whole and bioprocessed (108 h) common beans had IC50 [concentration needed to inhibit 50% the activity of angiotensin converting enzyme (ACE)] of 79.2 and 0.0117 μg/mL, respectively. The SSB is an efective strategy to improve the TPC of common beans for enhanced functionality with improved antioxidant activity and antihypertensive potential.

Share and Cite:

M. Guzmán-Uriarte, L. Sánchez-Magaña, G. Angulo-Meza, E. Cuevas-Rodríguez, R. Gutiérrez-Dorado, S. Mora-Rochín, J. Milán-Carrillo, A. Valdez-Ortiz and C. Reyes-Moreno, "Solid State Bioconversion for Producing Common Bean (Phaseolus vulgaris L.) Functional Flour with High Antioxidant Activity and Antihypertensive Potential," Food and Nutrition Sciences, Vol. 4 No. 4, 2013, pp. 480-490. doi: 10.4236/fns.2013.44061.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] K. Sowndharajan, P. Siddhuraju and S. Manian, “In Vitro Evaluation of the Antioxidant Activities in the Differentially Processed Seeds from Underutilized Legume, Bauhinia Vahilii Wight and Arn,” Food Science and Bio technology, Vol. 19, No. 2, 2010, pp. 503-509. doi:10.1007/s10068-010-0070-6
[2] W. Wiczkowski and M. K. Piskula, “Food Flavonoids,” Polish Journal of Food Nutrition Science, Vol. 13, 2004, pp. 101-114.
[3] V. Cheynier, “Polyphenols in Foods Are More Complex than Often Thought,” American Journal of Clinical Nutrition, Vol. 81, No. 1, 2005, pp. 223-229.
[4] R. Pilarski, H. Zielinski, D. Ciesiolka and K. Gulewicz, “Antioxidant Activity of Ethanolic and Aqueous Extracts of Uncaria tomentosa (Willd.) DC,” Journal of Ethno pharmacology, Vol. 104, No. 1-2, 2006, pp. 18-23. doi:10.1016/j.jep.2005.08.046
[5] A. Romani, P. Vignolini, C. Galardi, N. Mulinacci, S. Be nedettelli and D. HeimLer, “Germplasm Characterization by Zolfino Landraces (Phaseolus vulgaris L.) by Flavonoid Content,” Journal of Agricultural and Food Chemistry, Vol. 52, No. 12, 2004, pp. 3838-3842. doi:10.1021/jf0307402
[6] T. Madhujith and F. Shahidi, “Antioxidant Potential of Pea Beans (Phaseolus vulgaris L.)”, Journal of Food Science, Vol. 70, No. 1, 2005, pp. 85-90. doi:10.1111/j.1365-2621.2005.tb09071.x
[7] B. D. Oomah, A. Cardador-Martinez and G. Loarca-Pina, “Phenolics and Antioxidative Activities in Common Beans (Phaseolus vulgaris L),” Journal of the Science and Food Agriculture, Vol. 85, No. 6, 2005, pp. 935-942. doi:10.1002/jsfa.2019
[8] L. Bazzano, J. He, L.G. Ogden, C. Loria, S. Vupputuri, L. Myers and P. K. Whelton, “Legume Consumption and Risk of Coronary Heart Disease in US Men and Women,” Archives of Internal Medicine, Vol. 161, No. 21, 2001, pp. 2573-2578. doi:10.1001/archinte.161.21.2573
[9] X. Aparicio-Fernández, T. García-Gasca, G. G. Yousef, M. A. Lila, E. G. de Mejía and G. Loarca-Pina, “Chemo preventive Activity of Polyphenolics from Black Jamada Bean (Phaseolus vulgaris L.) on HeLa and HaCaT Cells,” Journal of Agricultural and Food Chemistry, Vol. 54, No. 6, 2006, pp. 2116-2122. doi:10.1021/jf052974m
[10] R. Reynoso-Camacho, M. C. Ríos-Ugalde, I. Torres-Pa checo, J. A. Acosta-Gallegos, A. C. Palomino-Salinas, M. Ramos-Gómez, E. González-Jasso and S. H. Guzmán Maldonado, “El Consumo de Frijol Común (Phaseolus vulgaris L) y su Efecto Sobre el Cáncer de Colon en Ratas Sprague-Dauley,” Agricultura Técnica de México, Vol. 33, 2007, pp. 43-52.
[11] A. Valdez-Ortiz, C. I. Fuentes-Gutiérrez, L. J. Germán Báez, R. Gutiérrez-Dorado and S. Medina-Godoy, “Protein Hydrolysates Obtained from Azufrado (Sulphur Yel low) Beans (Phaseolus vulgaris): Nutritional, ACE-Inhibitory and Antioxidative Characterization,” Food Science and Technology, Vol. 46, 2012, pp. 91-96.
[12] A. Moure, H. Domínguez and J. C. Parajo, “Antioxidant Properties and Ultrafiltration-Recovered Soy Protein Fractions from Industrial Effluents and Their Hydrolysates,” Process Biochemistry, Vol. 41, No. 2, 2006, pp. 447-452. doi:10.1016/j.procbio.2005.07.014
[13] A. J. Hernández-álvarez, G. Dávila-Ort?z, C. Jiménez Martínez and C. Jacinto-Hernández, “Isolation and Characterization of Bioactive Peptides from Seed of Bean (Phaseolus vulgaris var. Jamapa),” Food Science and Food Biotechnology in Developing Countries, Vol. 19, 2008, pp. 505-509.
[14] W. Wang and E. G. de Mejia, “A New Frontier in Soy Bioactive Peptides That May Prevent Age-Related Chronic Diseases,” Comprehensive Reviews in Food Sci ence and Food Safety, Vol. 4, No. 4, 2005, pp. 63-78. doi:10.1111/j.1541-4337.2005.tb00075.x
[15] Y. H. Pyo and T. C. Lee, “The Potential Antioxidant Capacity and Angiotensin-I Converting Enzyme Inhibitory Activity of Monascus-Fermented Soybean Extracts: Eva luation of Monascus-Fermented Soybean Extracts as Multifunctional Food Additives,” Journal of Food Science, Vol. 72, No. 3, 2007, pp. S218-S223. doi:10.1111/j.1750-3841.2007.00312.x
[16] U. Holker and J. Lenz, “Solid-State Fermentation—Are There Any Biotechnological Advantages?” Current Opinion in Microbiology, Vol. 8, No. 3, 2005, pp. 301-306. doi:10.1016/j.mib.2005.04.006
[17] A. Sharma and N. Khetarpaul, “Effect of Fermentation on Phytic Acid Content and in Vitro Digestibility of Starch and Protein of Rice-Black Gram Dhal-Wheat Blends,” Journal of Food Science and Technology, Vol. 34, 1997, pp. 20-30.
[18] E. Berghofer, B. Grzeskowiak, N. Mundigler, W. B. Sen tall and J. Walcak, “Antioxidative Properties of Faba Bean, Soybean and Oat Tempeh,” International Journal of Food Science and Nutrition, Vol. 49, No. 1, 1998, pp. 45-54. doi:10.3109/09637489809086403
[19] H. Han and B. K. Baik, “Antioxidant Activity and Phenolic Content of Lentils (Lens culinaris), Chickpeas (Cicerarietinum L.), Peas (Pisum sativum L.) and Soybeans (Glycine max), and Their Quantitative Changes during Processing,” International Journal of Food Science and Technology, Vol. 43, 2008, pp. 1971-1978. doi:10.1111/j.1365-2621.2008.01800.x
[20] M. Reyes-Bastidas, E. Z. Reyes-Fernández, J. López-Cer vantes, J. Milán-Carrillo, G. F. Loarca-Pila and C. Reyes Moreno, “Physicochemical, Nutritional and Antioxidant Activity Properties of Tempeh from Common Beans (Phaseolus vulgaris L),” Food Science and Technology International, Vol. 16, No. 5, 2010, pp. 427-434. doi:10.1177/1082013210367559
[21] D. Maiti and M. Majumdar, “Impact of Bioprocessing on Phenolic Content and Antioxidant Activity of Two Edible Seeds to Improve Hypoglycemic Functionality,” Journal of Natural Pharmaceuticals, Vol. 3, 2012, pp. 31-36
[22] C. Chen-Tien, H. Cheng-Kuang, C. Su-Tze, C. Ya-Chen, H. Feng-Sheng and C. Yun-Chin, “Effect of Fermentation Time on the Antioxidant Activities of Tempeh Prepared from Fermented Soybean Using Rhizopus oligosporus,” International Journal of Food Science and Technology, Vol. 44, No. 4, 2009, pp. 799-806. doi:10.1111/j.1365-2621.2009.01907.x
[23] C. Chaivasut, T. Kumar, P. Tipduangta and W. Rungsee vijitprapa, “Isoflavone Content and Antioxidant Activity of Thai Fermented Soybean and Its Capsule Formulation,” African Journal of Biotechnology, Vol. 9, 2010, pp. 4120-4126.
[24] B. P. Sousa and R. T. P. Correia, “Phenolic Content, An tioxidant Activity and Antiamylolytic Activity of Extracts Obtained from Bioprocessed Pineapple and Guava Wastes,” Brazilian Journal of Chemical Engineering, Vol. 29, 2012, pp. 25-30
[25] C. Reyes-Moreno, E. O. Cuevas-Rodríguez, J. Milán-Car rillo, O. G. Cárdenas-Valenzuela and J. Barrón-Hoyos, “Solid State Fermentation Process for Producing Chick pea (Cicer arietinum L) Tempe Flour. Physicochemical and Nutritional Characteristics of the Product,” Journal of the Science of Food and Agriculture, Vol. 84, No. 3, 2004, pp. 271-278. doi:10.1002/jsfa.1637
[26] V. Dewanto, X. Wu and R. H. Liu, “Processed Sweet Corn Has Higher Antioxidant Activity,” Journal of Agricultural and Food Chemistry, Vol. 50, No. 17, 2002, pp. 4959-4964. doi:10.1021/jf0255937
[27] K. K. Adom and R. H. Liu, “Antioxidant Activity of Grains,” Journal of Agricultural and Food Chemistry, Vol. 50, No. 21, 2002, pp. 6182-6187. doi:10.1021/jf0205099
[28] S. Mora-Rochín, J. A. Gutiérrez-Uribe, S. O. Serna-Sal divar, P. Sánchez-Pena, C. Reyes-Moreno and J. Milán Carrillo, “Phenolic Content and Antioxidant Activity of Tortillas Produced from Pigmented Maize Processed by Conventional Nixtamalization or Extrusion Cooking,” Journal of Cereal Science, Vol. 52, No. 3, 2010, pp. 502 508. doi:10.1016/j.jcs.2010.08.010
[29] V. L. Singleton, R. Orthofer and R. M. Lamuela-Raventos, “Analysis of Total Phenols and Other Oxidation Substrates and Antioxidants by Means of Folin-Ciocalteu Reagent,” Methods in Enzymology, Vol. 299, 1999, pp. 152-178. doi:10.1016/S0076-6879(99)99017-1
[30] G. Cao, H. M. Alessio and R. Culter, “Oxygen-Radical Absorbance Capacity Assays for Antioxidants,” Free Radical Biology and Medicine, Vol. 14, No. 3, 1993, pp. 303-311. doi:10.1016/0891-5849(93)90027-R
[31] B. Ou, M. Hampsch-Woodill and R. L. Prior, “Development and Validation of an Improved Oxygen Radical Absorbance Capacity Assay Using Fluorescein as the Fluorescent Probe,” Journal of Agricultural and Food Chem istry, Vol. 49, No. 10, 2001, pp. 4619-4626. doi:10.1021/jf010586o
[32] R. Re, N. Pellegrini, A. Proteggente, A. Pannala, M. Yang and C. Rice-Evans, “Antioxidant Activity Applying an Improved ABTS Radical Cation Decolorization Assay,” Free Radical Biology and Medicine, Vol. 26, No. 9-10, 1999, pp. 1231-1237. doi:10.1016/S0891-5849(98)00315-3
[33] L. M. Humiski and R. E. Aluko, “Physicochemical and Bitterness Properties of Enzymatic Pea Protein Hydrolysates,” Journal of Food Science, Vol. 72, 2007, pp. 605 611. doi:10.1111/j.1750-3841.2007.00475.x
[34] J. Adler-Nissen, “Enzymatic Hydrolysis of Food Proteins,” Elsevier Applied Science Publication, New York, 1986.
[35] M. Miguel, M. A. Aleixandre, M. Ramos and R. López Fandino, “Effect of Simulated Gastrointestinal Digestion on the Antihypertensive Properties of ACE-Inhibitory Peptides Derived from Ovalbumin,” Journal of Agricultural and Food Chemistry, Vol. 54, No. 3, 2006, pp. 726 731. doi:10.1021/jf051101p
[36] H. J. Motulsky and A. Christopoulos, “Fitting Models to Biological Data Using Linear and Nonlinear Regression,” A Practical Guide to Curve Fitting, GraphPad Software Inc., San Diego, 2003.
[37] AOAC, “Association of Official Analytical Chemists,” 16th Edition, Official Methods of Analysis, Association of Official Analytical Chemists, Washington DC, 1999.
[38] American Association of Cereal Chemists, “Approved Methods of the American Association of Cereal Chem ists,” AACC, St. Paul, 2000.
[39] R. A. Anderson, H. F. Conway, V. F. Pfeifer and E. Grif fin, “Gelatinization of Corn Grits by Roll and Extrusion Cooking,” Cereal Science Today, Vol. 14, 1969, pp. 4-7, 11-12.
[40] R. Mora-Escobedo, O. Paredes-López and G. F. Gutiér rez-López, “Effect of Germination on the Rheological and Functional Properties of Amaranth Seeds,” Lebensmmitel Wissenschaft und-Technologie, Vol. 24, 1994, pp. 241-246.
[41] D. A. Vattem and K. Shetty, “Solid-State Production of Phenolic Antioxidants from Cranberry Pomace by Rhizopus oligosporus,” Food Biotechnology, Vol. 16, No. 3, 2002, pp. 189-210. doi:10.1081/FBT-120016667
[42] R. Randhir, D. Vattem and K. Shetty, “Solid-State Bio conversion of Faba Bean by Rhizopus oligosporus for Enrichment of Phenolic Antioxidants and L-DOPA,” Innovative Food Science and Emerging Technologies, Vol. 5, No. 2, 2004, pp. 235-244. doi:10.1016/j.ifset.2004.01.003
[43] C. H. Lin, Y. T. Wei and C. C. Chou, “Enhanced Anti oxidative Activity of Soybean Koji Prepared with Various Filamentous Fungi,” Food Microbiology, Vol. 23, No. 7, 2006, pp. 628-633. doi:10.1016/j.fm.2005.12.004
[44] M. Naczk and F. Shahidi, “Phenolics in Cereals, Fruits and Vegetables: Occurrence, Extraction and Analysis,” Journal of Pharmaceutical and Biomedical Analysis, Vol. 41, No. 5, 2006, pp. 1523-1542. doi:10.1016/j.jpba.2006.04.002
[45] A. Segev, H. Badani, Y. Kapulnik, I. Shomer, M. Oren Shamir and S. Galili, “Determination of Polyphenols, Fla vonoids, and Antioxidant Capacity in Colored Chickpea (Cicer arietinum L.),” Journal of Food Science, Vol. 75, No. 2, 2010, pp. S115-S119. doi:10.1111/j.1750-3841.2009.01477.x
[46] Y. Yao, W. Sang, M. Zhou and G. Ren, “Antioxidant and α-Glucosidase Inhibition of Colored Grains in China,” Journal of Agricultural and Food Chemistry, Vol. 58, No. 2, 2010, pp. 770-774. doi:10.1021/jf903234c
[47] Y. Yao, X. Cheng, L. Wang, S. Wang and G. Ren, “Bio logical Potential of Sixteen Legumes in China,” International Journal of Molecular Science, Vol. 12, No. 10, 2011, pp. 7048-7058. doi:10.3390/ijms12107048
[48] M. J. Heiras-Palazuelos, M. Ochoa-Lugo, S. Mora-Ro chin, R. Gutiérrez-Dorado, J. Milan-Carrillo, J. A. Garzón Tiznado and C. Reyes-Moreno, “Technological Properties, Antioxidant Activity and Total Phenolic and Flavonoid Content of Pigmented Chickpea (Cicerarietinum L) Cultivars,” International Journal of Food Science and Nutri tion, Vol. 64, No. 1, 2012, pp. 69-76. doi:10.3109/09637486.2012.694854
[49] R. Randhir and K. Shetty, “Mung Beans Processed by Solid-State Bioconversion Improves Phenolic Content and Functionality Relevant for Diabetes and Ulcer Management,” Innovative Food Science and Emerging Technologies, Vol. 8, No. 2, 2007, pp. 197-204. doi:10.1016/j.ifset.2006.10.003
[50] J. G. Torruco-Uco, L. A. Chel-Guerrero, A. Martínez Ayala, G. Dávila-Ortíz and D. A. Betancur-Ancona, “Angiotensin-I Converting Enzyme Inhibitory and Antioxidant Activities of Protein Hydrolysates from Phaseolus lunatus and Phaseolus vulgaris Seeds,” Food Science and Technology, Vol. 42, No. 10, 2009, pp. 1597-1604.
[51] K. X. Zhu, H. M. Zhou and H. F. Qian, “Antioxidant and Free Radical-Scavenging Activities of Wheat Germ Protein Hydrolysates (WGPH) Prepared with Alcalase,” Process Biochemistry, Vol. 41, No. 6, 2006, pp. 1296-1302. doi:10.1016/j.procbio.2005.12.029
[52] C. Silva-Sánchez, A. P. Barba de la Rosa, M. F. León Galván, B. O. de Lumen, A. de León-Rodríguez and E. G. de Mejía, “Bioactive Peptides in Amaranth (Amaranthus hypochondriacus) Seed,” Journal of Agricultural and Food Chemistry, Vol. 56, No. 4, 2008, pp. 1233-1240. doi:10.1021/jf072911z
[53] M. I. Torino, R. I. Limón, C. Martínez-Villaluenga, S. M?kinen, A. Pihlanto, C. Vidal-Valverde and J. Frias, “Antioxidant and Antihypertensive Properties of Liquid and Solid State Fermented Lentils,” Food Chemistry, Vol. 136, No. 2, 2013, pp. 1030-1037. doi:10.1016/j.foodchem.2012.09.015
[54] L. Chel-Guerrero, M. Domínguez-Magana, A. Martínez Ayala, G. Dávila-Ortiz and D. Betancur-Ancona, “Lima Bean (Phaseolus lunatus) Protein Hydrolysates with ACE-I Inhibitory Activity,” Food and Nutrition Sciences, Vol. 3, No. 4, 2012, pp. 511-521. doi:10.4236/fns.2012.34072
[55] O. Paredes-López, J. González-Castaneda and A. Cára bez-Trejo, “Influence of Solid Substrate Fermentation on the Chemical Composition of Chickpea,” Journal of Fermentation Bioengineering, Vol. 71, No. 1, 1991, pp. 58 62. doi:10.1016/0922-338X(91)90304-Y
[56] R. A. Sparringa and J. D. Owens, “Protein Utilization during Soybean Tempe Fermentation,” Journal of Agricultural and Food Chemistry, Vol. 47, No. 10, 1999, pp. 4375-4378. doi:10.1021/jf981279u
[57] S. Hendrich, “Battling Obesity with Resistant Starch,” Food Technology, Vol. 64, No. 3, 2010, pp. 22-30.
[58] W. Shurtleff and A. Aoyagi, “The Book of Tempeh, a Super Soy from Indonesia,” Harper & Row (Colophon Books), New York, 1979.
[59] L. R. Ferguson, C. Tasman-Jones, H. Englyst and P. J. Harris, “Comparative Effects of Three Resistant Starch Preparations on Transit Time and Short-Chain Fatty Acids Production in Rats”, Nutrition Cancer, Vol. 36, No. 2, 2000, pp. 230-237. doi:10.1207/S15327914NC3602_13
[60] J. Hasjim and J. L. Jane, “Production of Resistant Starch by Extrusion Cooking of Acid-Modified Nomal-Maize Starch,” Journal of Food Science, Vol. 74, No. 7, 2009, pp. C556-C562. doi:10.1111/j.1750-3841.2009.01285.x
[61] P. I. Angulo-Bejarano, N. M. Verdugo-Montoya, E. O. Cuevas-Rodríguez, J. Milán-Carrillo, R. Mora-Escobedo, J. A. López-Valenzuela, J. A. Garzón-Tiznado and C. Reyes-Moreno, “Tempeh Flour from Chickpea (Cicerarietinum L). Nutritional and Physicochemical Properties,” Food Chemistry, Vol. 106, No. 1, 2008, pp. 106-112. doi:10.1016/j.foodchem.2007.05.049
[62] USDA, “Antioxidants and Heatlh,” ACES Publications, 2010, p. 4.

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.