Extracción de compuestos fenólicos de subproductos agroindustriales por fermentación fúngica con uso potencial como aditivos para carne y productos cárnicos. Revisión


  • Rey David Vargas Sánchez Universidad Autónoma de Sinaloa (UAS). Facultad de Medicina Veterinaria y Zootecnia. https://orcid.org/0000-0002-8537-1155
  • Brisa del Mar Torres Martínez Coordinación de Tecnología de Alimentos de Origen Animal, Centro de Investigación en Alimentación y Desarrollo, A.C. Hermosillo, Sonora, CP 83304, México. https://orcid.org/0000-0003-0354-9982
  • Gastón Ramón Torrescano Urrutia Coordinación de Tecnología de Alimentos de Origen Animal, Centro de Investigación en Alimentación y Desarrollo, A.C. Hermosillo, Sonora, CP 83304, México. https://orcid.org/0000-0003-1117-501X
  • Armida Sánchez Escalante Coordinación de Tecnología de Alimentos de Origen Animal, Centro de Investigación en Alimentación y Desarrollo, A.C. Hermosillo, Sonora, CP 83304, México. https://orcid.org/0000-0002-5966-5512
  • Martín Esqueda Coordinación de Tecnología de Alimentos de Origen Vegetal, Centro de Investigación en Alimentación y Desarrollo, A.C. Hermosillo, Sonora, CP 83304, México. https://orcid.org/0000-0003-0132-1810



Palabras clave:

hongos, Fermentación, Extracción de compuestos, Aditivos alimentarios


El presente manuscrito revisa los hallazgos de diferentes estudios de investigación que evalúan el uso de la fermentación con hongos en cultivo sumergido (SCF) y sólido (SSF) con residuos agroindustriales como sustratos para mejorar la producción de polifenoles y su posible uso como aditivos alimentarios. Algunos residuos agroindustriales (pulpas, cáscaras y semillas) son una fuente importante de compuestos como ácidos fenólicos (p-cumárico, p-hidroxibenzoico, clorogénico, cinámico, ferúlico, gálico, gentísico, protocatecuico, rosmarínico, salicílico, siríngico, y vanílico) y flavonoides (apigenina, crisina, (+)-catequina, kaempferol, miricetina, quercetina, rutina, hesperetina, y naringina). Además, la utilización de estos residuos como sustratos en SMF y SSF mejora la producción de polifenoles, mejora la función biológica al incrementar la actividad antioxidante y antimicrobiana, y proporciona una alternativa potencial al uso de antioxidantes sintéticos en la industria de la carne y productos cárnicos.

Biografía del autor/a

Rey David Vargas Sánchez, Universidad Autónoma de Sinaloa (UAS). Facultad de Medicina Veterinaria y Zootecnia.

Estudiante de posdoctorado


Aziz, M. and Karboune, S. 2018. Natural antimicrobial/antioxidant agents in meat and poultry products as well as fruits and vegetables: a review. Critical Reviews in Food Science and Nutrition. 58: 486-511.
Azmir, J., Zaidul, I.S.M., Rahman, M.M., Sharif, K.M., Mohamed, A., Sahena, F., Jahurul, M.H.A. and Omar, A.K.M. 2013. Techniques for extraction of bioactive compounds from plant materials: A review. Journal of Food Engineering. 117: 426-436.
Balasuriya, N. and Rupasinghe, H.V. 2012. Antihypertensive properties of flavonoid-rich apple peel extract. Food Chemistry. 135: 2320-2325.
Bekhit, A.E.D., Geesink, G.H., Ilian, M.A., Morton, J.D., Sedcole, J.R. and Bickerstaffe, R. 2004. Pro-oxidant activities of carnosine, rutin and quercetin in a beef model system and their effects on the metmyoglobin-reducing activity. European Food Research and Technology. 218: 507-514.
Brettonnet, A., Hewavitarana, A., DeJong, S. and Lanari, M.C. 2010. Phenolic acids composition and antioxidant activity of canola extracts in cooked beef, chicken, and pork. Food Chemistry. 121: 927-933.
Castañeda-Casasola, C., Arana-Cuenca, A., Favela-Torres, E., Anducho-Reyes, M.A., González, A.E. and Téllez-Jurado, A. 2018. Xylanase enzymes production by Aspergillus fumigatus in solid state fermentation and submerge fermentation. Revista Mexicana de Ingeniería Química. 17: 47-61.
Chandra, P. and Arora, D.S. 2016. Production of antioxidant bioactive phenolic compounds by solid-state fermentation on agro-residues using various fungi isolated from soil. Asian Journal of Biotechnology. 8: 8-15.
Choi, J.W., Ra, K.S., Kim, S.Y., Yoon, T.J., Yu, K.W., Shin, K.S., Lee, S.P. and Suh, H.J. 2010. Enhancement of anti-complementary and radical scavenging activities in the submerged culture of Cordyceps sinensis by addition of citrus peel. Bioresource Technology. 101: 6028-6034.
Comisión del Codex Alimentarius, Normas internacionales de los alimentos; Norma general para los aditivos alimentarios [Accesses 2 march 2020] 2017. Available in: http://www.fao.org/gsfaonline/docs/CXS_192s.pdf. (Fecha de consulta, Septiembre de 2019).
Cushnie, T.P.T. and Lamb, A.J. 2005. Antimicrobial activity of flavonoids. International Journal of Antimicrobial Agents. 26: 343-356.
Das, R.K., Brar, S.K. and Verma, M. 2015. A fermentative approach towards optimizing directed biosynthesis of fumaric acid by Rhizopus oryzae 1526 utilizing apple industry waste biomass. Fungal Biology. 119: 1279-1290.
De Oliveira, C.E.V., Stamford, T.L.M., Neto, N.J.G. and de Souza, E.L. 2010. Inhibition of Staphylococcus aureus in broth and meat broth using synergies of phenolics and organic acids. International Journal of Food Microbiology. 137: 312-316.
Dey, T.B., Chakraborty, S., Jain, K.K., Sharma, A. and Kuhad, R.C. 2016. Antioxidant phenolics and their microbial production by submerged and solid-state fermentation process: A review. Trends in Food Science & Technology. 53: 60-74.
Dong, J.W., Cai, L., Xiong, J., Chen, X.H., Wang, W.Y., Shen, N., Liu, B.L. and Ding, Z.T. 2015. Improving the antioxidant and antibacterial activities of fermented Bletilla striata with Fusarium avenaceum and Fusarium oxysporum. Process Biochemistry. 50: 8-13.
Dulf, F.V., Vodnar, D.C. and Socaciu, C. 2016. Effects of solid-state fermentation with two filamentous fungi on the total phenolic contents, flavonoids, antioxidant activities and lipid fractions of plum fruit (Prunus domestica L.) by-products. Food Chemistry. 209: 27-36.
Eom, S.H., Lee, D.S., Kang, Y.M., Son, K.T., Jeon, Y.J. and Kim, Y.M. 2013. Application of yeast Candida utilis to ferment Eisenia bicyclis for enhanced antibacterial effect. Applied Biochemistry and Biotechnology. 171: 569-582.
European Commission (EC), Guidance document describing the food categories in Part E of Annex II to Regulation (EC) No 1333/2008 on Food Additives [Accesses 2 march 2020] 2014. Available in: https://ec.europa.eu/food/sites/food/files/safety/docs/fs_food-improvement-agents_guidance_1333-2008_annex2.pdf
Faustman, C., Sun, Q., Mancini, R. and Suman, S.P. 2010. Myoglobin and lipid oxidation interactions: Mechanistic bases and control. Meat science. 86: 86-94.
Food and Drug Administration (FDA), Overview of food ingredients, additives & colors [Accesses 2 march 2020] 2004. Available in: https://www.fda.gov/food/food-ingredients-packaging/overview-food-ingredients-additives-colors
Food and Drug Administration (FDA), Microbiological considerations for antimicrobial food additive submissions [Accesses 2 march 2020] 2008. Available in: https://www.fda.gov/media/83078/download
Food and Agriculture Organization of the United Nations (FAO), The future of food and agriculture, trends and challenges [Accesses 2 march 2020] 2017. Available in: http://www.fao.org/3/a-i6583e.pdf
Food and Agriculture Organization of the United Nations (FAO), Codex alimentarius, norma general para los aditivos alimentarios [Accesses 2 march 2020] 2018. Available: http://www.fao.org/gsfaonline/docs/CXS_192s.pdf
Hammad, H.H.M., Jin, G., Ma, M., Khalifa, I., Shukat, R., Elkhedir, A.E., Zeng, Q. and Noman, A.E. 2020. Comparative characterization of proximate nutritional compositions, microbial quality, and safety of camel meat in relation to mutton, beef, and chicken. LWT-Food Science and Technology. 118: 108714.
He, Y. and Shahidi, F. 1997. Antioxidant activity of green tea and its catechins in a fish meat model system. Journal of Agricultural and Food Chemistry. 45: 4262-4266.
Hernández-Carlos, B., Santos-Sánchez, N.F., Salas-Coronado, R., Villanueva-Cañongo, C. and Guadarrama-Mendoza, P.C. 2019. Antioxidant Compounds from Agro-Industrial Residue. In Antioxidants. IntechOpen (Ed). DOI: 10.5772/intechopen.85184.
Hölker, U., Höfer, M. and Lenz, J. (2004). Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Applied Microbiology and Biotechnology. 64: 175-186.
Huang, W., Niu, H., Li, Z., Lin, W., Gong, G. and Wang, W. 2007. Effect of ellagitannin acyl hydrolase, xylanase and cellulase on ellagic acid production from cups extract of valonia acorns. Process Biochemistry. 42: 1291-1295.
Huang, Y.C., Chen, Y.F., Chen, C.Y., Chen, W.L., Ciou, Y.P., Liu, W.H. and Yang, C.H. 2011. Production of ferulic acid from lignocellulolytic agricultural biomass by Thermobifida fusca thermostable esterase produced in Yarrowia lipolytica transformant. Bioresource Technology. 102: 8117-8122.
Jiang, J. and Xiong, Y.L. 2016. Natural antioxidants as food and feed additives to promote health benefits and quality of meat products: A review. Meat Science. 120: 107-117.
Karastogiannidou, C. 1999. Effects of onion quercetin on oxidative stability of cook‐chill chicken in vacuum‐sealed containers. Journal of Food Science. 64: 978-981.
Łata, B., Trampczynska, A. and Paczesna, J. 2009. Cultivar variation in apple peel and whole fruit phenolic composition. Scientia Horticulturae. 121: 176-181.
Lokeshwari, N. and Reddy, S. 2010. Microbiological production of gallic acid by a mutant strain of Aspergillus oryzae using cashew husk. Pharmacophore. 1: 112-122.
Ma, T.W., Lai, Y. and Yang, F.C. 2014. Enhanced production of triterpenoid in submerged cultures of Antrodia cinnamomea with the addition of citrus peel extract. Bioprocess and Biosystems Engineering. 37: 2251-2261.
Machado, E.M., Rodriguez-Jasso, R.M., Teixeira, J.A. and Mussatto, S.I. 2012. Growth of fungal strains on coffee industry residues with removal of polyphenolic compounds. Biochemical Engineering Journal. 60: 87-90.
Maqsood, S., Abushelaibi, A., Manheem, K., Al Rashedi, A. and Kadim, I.T. 2015. Lipid oxidation, protein degradation, microbial and sensorial quality of camel meat as influenced by phenolic compounds. LWT-Food Science and Technology. 63: 953-959.
Marković, Z., Milenković, D., Đorović, J., Marković, J.M.D., Stepanić, V., Lučić, B. and Amić, D. 2012. PM6 and DFT study of free radical scavenging activity of morin. Food Chemistry. 134: 1754-1760
Moulehi, I., Bourgou, S., Ourghemmi, I. and Tounsi, M.S. 2012. Variety and ripening impact on phenolic composition and antioxidant activity of mandarin (Citrus reticulate Blanco) and bitter orange (Citrus aurantium L.) seeds extracts. Industrial Crops and Products. 39: 74-80.
Norma Oficial Mexicana NOM-122-SSA1-1994 (NOM), Bienes y servicios. Productos de la carne. Productos cárnicos curados y cocidos, y curados emulsionados y cocidos. Especificaciones sanitarias [Accesses 2 march 2020] 1994. Available in: http://www.salud.gob.mx/unidades/cdi/nom/122ssa14.html
Norma Oficial Mexicana NOM-251-SSA1-2009 (NOM). Prácticas de higiene para el procesamiento de alimentos, bebidas o suplementos alimenticios [Accesses 2 march 2020] 2009. Available in: http://www.dof.gob.mx/normasOficiales/3980/salud/salud.htm
Norma Oficial Mexicana NOM-213-SSA1-2002 (NOM), Productos y servicios. Productos cárnicos procesados. Especificaciones sanitarias. Métodos de prueba [Accesses 2 march 2020] 2002. Available in: http://www.salud.gob.mx/unidades/cdi/nom/213ssa102.html
Onyeneho, S.N. and Hettiarachchy, N S. 1993. Antioxidant activity, fatty acids and phenolic acids compositions of potato peels. Journal of the Science of Food and Agriculture. 62: 345-350.
OrphAnides, A., GOulAs, V. and GekAs, V. 2013. Effect of drying method on the phenolic content and antioxidant capacity of spearmint. Czech Journal of Food Sciences. 31: 509-513.
Pandey, A. 2003. Solid-state fermentation. Biochemical Engineering Journal. 13: 81-84.
Papaspyridi, L.M., Aligiannis, N., Topakas, E., Christakopoulos, P., Skaltsounis, A.L. and Fokialakis, N. 2012. Submerged fermentation of the edible mushroom Pleurotus ostreatus in a batch stirred tank bioreactor as a promising alternative for the effective production of bioactive metabolites. Molecules. 17: 2714-2724.
Peanparkdee, M. and Iwamoto, S. 2019. Bioactive compounds from by-products of rice cultivation and rice processing: Extraction and application in the food and pharmaceutical industries. Trends in Food Science & Technology. 86: 109-117.
Pinelo, M., Tress, A.G., Pedersen, M., Arnous, A. and Meyer, A.S. 2007. Effect of cellulases, solvent type and particle size distribution on the extraction of chlorogenic acid and other phenols from spent coffee grounds. American Journal of Food and Technology. 2: 641-651.
Poljsak, B., Šuput, D. and Milisav, I. 2013. Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxidative medicine and Cellular Longevity. 1: 1-11.
Pronyk, C. and Mazza, G. 2009. Design and scale-up of pressurized fluid extractors for food and bioproducts. Journal of Food Engineering. 95: 215-226.
Ramírez-Rojo, M.I., Vargas-Sánchez, R.D., del Mar Torres-Martínez, B., Torrescano-Urrutia, G.R. and Sánchez-Escalante, A. 2018. Extractos de hojas de plantas para conservar la calidad de la carne y los productos cárnicos frescos. Revisión. Biotecnia. 20: 155-164.
Ravichandran, M., Hettiarachchy, N.S., Ganesh, V., Ricke, S.C. and Singh, S. 2011. Enhancement of antimicrobial activities of naturally occurring phenolic compounds by nanoscale delivery against Listeria monocytogenes, Escherichia coli O157: H7 and Salmonella Typhimurium in broth and chicken meat system. Journal of Food Safety. 31: 462-471.
Razak, D.L.A., Rashid, N.Y.A., Jamaluddin, A., Sharifudin, S.A., Kahar, A.A. and Long, K. 2017. Cosmeceutical potentials and bioactive compounds of rice bran fermented with single and mix culture of Aspergillus oryzae and Rhizopus oryzae. Journal of the Saudi Society of Agricultural Sciences. 16: 127-134.
Rico, X., Gullón, B., Alonso, J.L. and Yáñez, R. 2020. Recovery of high value-added compounds from pineapple, melon, watermelon, and pumpkin processing by-products: an overview. Food Research International. 109086.
Rodríguez-Carpena, J.G., Morcuende, D., Andrade, M.J., Kylli, P. and Estévez, M. 2011. Avocado (Persea americana Mill.) phenolics, in vitro antioxidant and antimicrobial activities, and inhibition of lipid and protein oxidation in porcine patties. Journal of Agricultural and Food Chemistry. 59: 5625-5635.
Rodríguez Vaquero, M.J., Aredes Fernandez, P.A., Manca de Nadra, M.C. and Strasser de Saad, A.M. 2010. Phenolic compound combinations on Escherichia coli viability in a meat system. Journal of Agricultural and Food Chemistry. 58: 6048-6052.
Rodríguez Vaquero, M.J., Aredes Fernández, P.A., de Nadra, M. and Cristina, M. 2011. Effect of phenolic compound mixtures on the viability of Listeria monocytogenes in meat model. Food Technology and Biotechnology. 49: 83-88.
Sadh, P.K., Chawla, P. and Duhan, J.S. 2018. Fermentation approach on phenolic, antioxidants and functional properties of peanut press cake. Food Bioscience. 22: 113-120.
Santana-Méridas, O., González-Coloma, A. and Sánchez-Vioque, R. 2012. Agricultural residues as a source of bioactive natural products. Phytochemistry Reviews. 11: 447-466.
Seth, M. and Chand, S. 2000. Biosynthesis of tannase and hydrolysis of tannins to gallic acid by Aspergillus awamori-optimisation of process parameters. Process Biochemistry. 36: 39-44.
Shahidi, F., Wanasundara, P.K.J.P.D. and Hong, C. 1992. Antioxidant activity of phenolic compounds in meat model systems. In: Phenolic Compounds in Foods and Their Effects on Health. Ho, C.-T., Lee, C.Y. and Huang, M.-T. (Eds.). ACS Symposium Series 506, American Chemical Society, Washington, DC. pp. 214-222.
Shahidi, F., Yang, Z. and Saleemi, Z.O. 1993. Stabilization of meat lipids with flavonoids and flavonoid‐related compounds. Journal of Food Lipids. 1: 69-78.
Shin, H.Y., Kim, S.M., Lee, J.H. and Lim, S.T. 2019. Solid-state fermentation of black rice bran with Aspergillus awamori and Aspergillus oryzae: effects on phenolic acid composition and antioxidant activity of bran extracts. Food Chemistry. 272: 235-241.
Sousa, B.A. and Correia, R.T.P. 2012. Phenolic content, antioxidant activity and antiamylolytic activity of extracts obtained from bioprocessed pineapple and guava wastes. Brazilian Journal of Chemical Engineering. 29: 25-30.
Spigno, G., Tramelli, L. and De Faveri, D.M. 2007. Effects of extraction time, temperature and solvent on concentration and antioxidant activity of grape marc phenolics. Journal of Food Engineering. 81: 200-208.
Sova, M. 2012. Antioxidant and Antimicrobial Activities of Cinnamic Acid Derivatives. Mini-Reviews in Medicinal Chemistry. 12: 749-767.
Stojković, D., Petrović, J., Soković, M., Glamočlija, J., Kukić‐Marković, J. and Petrović, S. 2013. In situ antioxidant and antimicrobial activities of naturally occurring caffeic acid, p‐coumaric acid and rutin, using food systems. Journal of the Science of Food and Agriculture. 93: 3205-3208.
United States Department of Agriculture (USDA), Additives in Meat and Meat Products [Accesses 2 march 2020] 2015. Available in: https://www.fsis.usda.gov/wps/portal/fsis/topics/food-safety-education/get-answers/food-safety-fact-sheets/food-labeling/additives-in-meat-and-poultry-products/additives-in-meat-and-poultry-products
Valdez-Morales, M., Espinosa-Alonso, L.G., Espinoza-Torres, L.C., Delgado-Vargas, F. and Medina-Godoy, S. 2014. Phenolic content and antioxidant and antimutagenic activities in tomato peel, seeds, and byproducts. Journal of Agricultural and Food Chemistry. 62: 5281-5289.
Vattem, D.A. and Shetty, K. 2002. Solid-state production of phenolic antioxidants from cranberry pomace by Rhizopus oligosporus. Food Biotechnology. 16: 189-210.
Vermerris, W. and Nicholson, R. 2008. Families of phenolic compounds and means of classification. In: Phenolic Compound Biochemistry. Springer (ed.), pp 1-34. Switzerland AG.
Wang, S.L., Hsiao, W.J. and Chang, W.T. 2002. Purification and characterization of an antimicrobial chitinase extracellularly produced by Monascus purpureus CCRC31499 in a shrimp and crab shell powder medium. Journal of Agricultural and Food Chemistry. 50: 2249-2255.
Wen, Y.L., Yan, L.P. and Chen, C.S. 2013. Effects of fermentation treatment on antioxidant and antimicrobial activities of four common Chinese herbal medicinal residues by Aspergillus oryzae. Journal of Food and Drug Analysis. 21: 219-226.
Wijngaard, H., Hossain, M.B., Rai, D.K. and Brunton, N. 2012. Techniques to extract bioactive compounds from food by-products of plant origin. Food Research International. 46: 505-513.
Xie, C.Y., Gu, Z.X., You, X., Liu, G., Tan, Y. and Zhang, H. 2010. Screening of edible mushrooms for release of ferulic acid from wheat bran by fermentation. Enzyme and Microbial Technology. 46: 125-128.
Xu, X. and Zhu, J. 2011. Enhanced phenolic antioxidants production in submerged cultures of Inonotus obliquus in a ground corn stover medium. Biochemical Engineering Journal 58: 103-109.
Xu, X.Q., Hu, Y. and Zhu, L.H. 2014. The capability of Inonotus obliquus for lignocellulosic biomass degradation in peanut shell and for simultaneous production of bioactive polysaccharides and polyphenols in submerged fermentation. Journal of the Taiwan Institute of Chemical Engineers. 45: 2851-2858.
Xu, X., Shen, M. and Quan, L. 2015. Stimulatory agents simultaneously improving the production and antioxidant activity of polyphenols from Inonotus obliquus by submerged fermentation. Applied Biochemistry and Biotechnology. 176: 1237-1250.
Yang, F.C. and Liau, C B. 1998. The influence of environmental conditions on polysaccharide formation by Ganoderma lucidum in submerged cultures. Process Biochemistry. 33: 547-553.
Yang, F.C., Ma, T.W. and Chuang, Y.T. 2012. Medium modification to enhance the formation of bioactive metabolites in shake flask cultures of Antrodia cinnamomea by adding citrus peel extract. Bioprocess and Biosystems Engineering. 35: 1251-1258.
Zhu, L. and Xu, X. 2013. Stimulatory effect of different lignocellulosic materials for phenolic compound production and antioxidant activity from Inonotus obliquus in submerged fermentation. Applied Biochemistry and Biotechnology. 169: 2138-2152.