Compuestos bioactivos en quesos: biosíntesis, actividad biológica y contribución de las bacterias ácido lácticas
DOI:
https://doi.org/10.15517/am.v34i2.51432Palabras clave:
ácido gamma-aminobutírico, aminas biogénicas, bacteriocinas, cultivo iniciador, alimentos funcionalesResumen
Introducción. A partir de 1990 se ha observado un incremento en la tasa de enfermedades asociadas con dietas poco saludables y estilos de vida sedentaria, cuya atención supone un reto para los sistemas de salud. Lo anterior, ha despertado el interés por los alimentos funcionales, es decir, aquellos que además de proporcionar macro y micronutrientes, aporten sustancias que poseen efecto fisiológico en el organismo, lo que se traduce en la mejora de la salud de quien lo ingiere. De manera genérica a estos compuestos se les conoce como bioactivos. Objetivo. Revisar las principales sustancias bioactivas reportadas en quesos, el papel de los microorganismos en la producción de las mismas y las rutas de biosíntesis de los principales compuestos. Desarrollo. La leche y sus derivados son productos alimenticios consumidos alrededor del mundo y presentan un incremento constante en su producción y consumo. Esta tendencia de mercado es debida a su sabor y aporte nutrimental. Uno de los derivados lácteos con mayor demanda en el mundo son los quesos. Son una fuente de sustancias como péptidos, ácidos grasos, vitaminas, bacteriocinas, ácidos orgánicos, ácido gamma aminobutírico, etc., todas con importante actividad biológica. Conclusión. La presencia, cantidad y disponibilidad de los compuestos bioactivos presentes en los quesos difiere, como resultado del tipo de leche empleada para su elaboración, el tipo de microorganismo empleado, ya sea como cultivo iniciador o secundario, así también como el proceso tecnológico empleado.
Descargas
Citas
Bae, H. C., Nam, J. H., Renchinkhand, G., Choi, S. -H., & Nam, M. S. (2020). Physicochemical changes during 4 weeks ripening of Camembert cheeses salted with four types of salts. Applied Biological Chemistry, 63, Article 66. https://doi.org/10.1186/s13765-020-00539-5
Bactibase. (n.d.). A database dedicated to bacteriocins. Retrieved March 17th 2022 from http://bactibase.hammamilab.org/about.php
Baptista, R. C., Horita, C. N., & Sant’Ana, A. S. (2020). Natural products with preservative properties for enhancing the microbiological safety and extending the shelf-life of seafood: A review. Food Research International, 127, Article 108762. https://doi.org/10.1016/j.foodres.2019.108762
Barbieri, F., Montanari, C., Gardini, F., & Tabanelli, G. (2019). Biogenic amine production by lactic acid bacteria: A review. Foods, 8(1), Article 17. https://doi.org/10.3390/foods8010017
Benkerroum, N. (2016). Biogenic amines in dairy products: origin, incidence, and control means. Comprehensive Reviews in Food Science and Food Safety, 15(4), 801–826. https://doi.org/10.1111/1541-4337.12212
Briguglio, M., Dell’Osso, B., Panzica, G., Malgaroli, A., Banfi, G., Zanaboni Dina, C. Z., Galentino, R., & Porta, M. (2018). Dietary neurotransmitters: A narrative review on current knowledge. Nutrients, 10(5), Article 591. https://doi.org/10.3390/nu10050591
Bulat, T., & Topcu, A. (2020). Oxidation-reduction potential of UF white cheese: Impact on organic acids, volatile compounds and sensorial properties. LWT-Food Science and Technology, 131, Article 109770. https://doi.org/10.1016/j.lwt.2020.109770
Carafa, I., Stocco, G., Nardin, T., Larcher, R., Bittante, G., Tuohy, K., & Franciosi, E. (2019). Production of naturally γ-aminobutyric acid-enriched cheese using the dairy strains Streptococcus thermophilus 84C and Lactobacillus brevis DSM 32386. Frontiers in Microbiology, 10, Article 93. https://doi.org/10.3389/fmicb.2019.00093
Crevier, B., Bélanger, G., Vuillemard, J. -C., & St-Gelais, D. (2017). Production of cottage cheese fortified with vitamin D. Journal of Dairy Science, 100(7), 5212–5216. https://doi.org/10.3168/jds.2016-12308
Diana, M., Rafecas, M., Arco, C., & Quílez, J. (2014). Free amino acid profile of Spanish artisanal cheeses: Importance of gamma-aminobutyric acid (GABA) and ornithine content. Journal of Food Composition and Analysis, 35(2), 94–100. https://doi.org/10.1016/j.jfca.2014.06.007
Di Bonito, P., Pacifico, L., Licenziati, M. R., Maffeis, C., Morandi, A., Manco, M., del Giudice, E. M., Di Sessa, A., Campana, G., Moio, N., Baroni, M. G., Chiesa, C., De Simone, G., & Valerio, G. (2020). Elevated blood pressure, cardiometabolic risk and target organ damage in youth with overweight and obesity. Nutrition, Metabolism and Cardiovascular Diseases, 30(10), 1840–1847. https://doi.org/10.1016/j.numecd.2020.05.024
Fiore, M., Cristaldi, A., Okatyeva, V., Lo Bianco, S., Oliveri Conti, G., Zuccarello, P., Copat, C., Caltabiano, R., Cannizzaro, M., & Ferrante, M. (2020). Dietary habits and thyroid cancer risk: a hospital-based case–control study in Sicily (South Italy). Food and Chemical Toxicology, 146, Article 111778. https://doi.org/10.1016/j.fct.2020.111778
Fox, P. F., Cogan, T. M., & Guinee, T. P. (2017). Factors that affect the quality of cheese. In P. L. H. McSweeney, P. F. Fox, P. D. Cotter, & D. W. Everett (Eds.), Cheese (Chapter 25, 4th ed., pp. 617–641). Academic Press. https://doi.org/10.1016/B978-0-12-417012-4.00025-9
García-Burgos, M., Moreno-Fernández, J., Alférez, M. J. M., Díaz-Castro, J., & López-Aliaga, I. (2020). New perspectives in fermented dairy products and their health relevance. Journal of Functional Foods, 72, Article 104059. https://doi.org/10.1016/j.jff.2020.104059
Gatzias, I. S., Karabagias, I. K., Kontominas, M. G., & Badeka, A. V. (2020). Geographical differentiation of feta cheese from northern Greece based on physicochemical parameters, volatile compounds and fatty acids. LWT-Food Science and Technology, 131, Article 109615. https://doi.org/10.1016/j.lwt.2020.109615
Gonzalez-Gonzalez, C. R., Machado, J., Correia, S., McCartney, A. L., Stephen Elmore, J., & Jauregi, P. (2019). Highly proteolytic bacteria from semi-ripened Chiapas cheese elicit angiotensin-I converting enzyme inhibition and antioxidant activity. LWT-Food Science and Technology, 111, 449–456. https://doi.org/10.1016/j.lwt.2019.05.039
Hernández-Lara, A. H., Almazán-Urbina, F. E., Santiago-Torres, M., & Rangel-Cruz, E. (2020). Intragastric balloon placement in the treatment of overweight and obesity: Experience at a Mexican referral center. Revista de Gastroenterología de México, 85(4), 410–415. https://doi.org/10.1016/j.rgmx.2019.10.007
Higurashi, S., Ogawa, A., Nara, T. Y., Kato, K., & Kadooka, Y. (2016). Cheese consumption prevents fat accumulation in the liver and improves serum lipid parameters in rats fed a high-fat diet. Dairy Science and Technology, 96, 539–549. https://doi.org/10.1007/s13594-016-0288-z
Hossain, S., Khetra, Y., Ganguly, S., Kumar, R., & Sabikhi, L. (2020). Effect of heat treatment on plasmin activity and bio-functional attributes of Cheddar cheese. LWT-Food Science and Technology, 120, Article 108924. https://doi.org/10.1016/j.lwt.2019.108924
Ianni, A., Bennato, F., Martino, C., Grotta, L., & Martino, G. (2020). Volatile flavor compounds in cheese as affected by ruminant diet. Molecules, 25(3), Article 461. https://doi.org/10.3390/molecules25030461
Jeon Park, S., Hyun Kim, D., Jee Kang, H., Shin, M., Yang, S. -Y., Yang, J., & Hoon Jung, Y. (2021). Enhanced production of γ-aminobutyric acid (GABA) using Lactobacillus plantarum EJ2014 with simple medium composition. LWT-Food Science and Technology, 137, Article 110443. https://doi.org/10.1016/j.lwt.2020.110443
Johnson, M. E. (2017). A 100-year review: Cheese production and quality. Journal of Dairy Science, 100(12), 9952–9965. https:/doi.org/10.3168/jds.2017-12979
Juan, B., Zamora, A., Quevedo, J. M., & Trujillo, A. -J. (2016). Proteolysis of cheese made from goat milk treated by ultra high pressure homogenisation. LWT-Food Science and Technology, 69, 17–23. https://doi.org/10.1016/j.lwt.2015.12.013
Kumariya, R., Kumari Garsa, A., Rajput, Y. S., Sood, S. K., Akhtar, N., & Patel, S. (2019). Bacteriocins: Classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microbial Pathogenesis, 128, 171–177. https:/doi.org/10.1016/j.micpath.2019.01.002
López-Expósito, I., Miralles, B., Amigo, L., & Hernández-Ledesma, B. (2017). Health effects of cheese components with a focus on bioactive peptides. In J. Frías, C. Martinez-Villaluenga, & E. Peñas (Eds.), Fermented foods in health and disease prevention (Chapter 11, pp. 239–273). Academic Press. https://doi.org/10.1016/B978-0-12-802309-9.00011-X
Lordan, R., Walsh, A., Crispie, F., Finnegan, L., Demuru, M., Tsoupras, A., Cotter, P. D., & Zabetakis, I. (2019). Caprine milk fermentation enhances the antithrombotic properties of cheese polar lipids. Journal of Functional Foods, 61, Article 103507. https://doi.org/10.1016/j.jff.2019.103507
Majid, S. (2016). Bioactive components in milk and dairy products. Sweish University of Agricultural Sciences.
Maqsood, S., Adiamo, O., Ahmad, M., & Mudgil, P. (2020). Bioactive compounds from date fruit and seed as potential nutraceutical and functional food ingredients. Food Chemistry, 308, Article 125522. https://doi.org/10.1016/j.foodchem.2019.125522
Møller, C. O. de A., Ücok, E. F., & Rattray, F. P. (2020). Histamine forming behaviour of bacterial isolates from aged cheese. Food Research International, 128, Article 108719. https://doi.org/10.1016/j.foodres.2019.108719
Moradi, M., Khalid Omer, A., Razavi, R., Valipour, S., & Guimarães, J. T. (2021). The relationship between milk somatic cell count and cheese production, quality and safety: A review. International Dairy Journal, 113, Article 104884. https://doi.org/10.1016/j.idairyj.2020.104884
Munir, M., Nadeem, M., Mahmood Qureshi, T., Gamlath, C. J., Martin, G. J. O., Hemar, Y., & Ashokkumar, M. (2020). Effect of sonication, microwaves and high-pressure processing on ACE-inhibitory activity and antioxidant potential of Cheddar cheese during ripening. Ultrasonics Sonochemistry, 67, Article 105140. https://doi.org/10.1016/j.ultsonch.2020.105140
Nájera, A. I., Bustamante, M. A., Albisu, M., Valdivielso, I., Amores, G., Mandaluniz, N., Arranz, J., Barron, L. J. R., & de Renobales, M. (2017). Fatty acids, vitamins and cholesterol content, and sensory properties of cheese made with milk from sheep fed rapeseed oilcake. Journal of Dairy Science, 100(9), 6962–6971. https://doi.org/10.3168/jds.2017-12588
Neofytou, M. C., Miltiadou, D., Sfakianaki, E., Constantinou, C., Symeou, S., Sparaggis, D., Hager-Theodorides, A. L., & Tzamaloukas, O. (2020). The use of ensiled olive cake in the diets of Friesian cows increases beneficial fatty acids in milk and Halloumi cheese and alters the expression of SREBF1 in adipose tissue. Journal of Dairy Science, 103(10), 8998–9011. https://doi.org/10.3168/jds.2020-18235
Ortakci, F., Broadbent, J. R., Oberg C. J., & McMahon, D. J. (2015). Growth and gas formation by Lactobacillus wasatchensis, a novel obligatory heterofermentative nonstarter lactic acid bacterium, in Cheddar-style cheese made using a Streptococcus thermophilus starter. Journal of Dairy Science, 98(11), 7473–7482. https://doi.org/10.3168/jds.2015-9556
Pardini Gontijo, M. T., de Sousa Silva, J., Pereira Vidigal, P. M., & Prado Martin, J. G. (2020). Phylogenetic distribution of the bacteriocin repertoire of lactic acid bacteria species associated with artisanal cheese. Food Research International, 128, Article 108783. https://doi.org/10.1016/j.foodres.2019.108783
Park, Y. W., & Nam, M. S. (2015). Bioactive peptides in milk and dairy products: A Review. Korean Journal for Food Science of Animal Resources, 35(6), 831–840. https://doi.org/10.5851/kosfa.2015.35.6.831
Paucar-Menacho, L. M., Martínez-Villaluenga, C., Dueñas, M., Frias, J., & Peñas, E. (2017). Optimization of germination time and temperature to maximize the content of bioactive compounds and the antioxidant activity of purple corn (Zea mays L.) by response surface methodology. LWT-Food Science and Technology, 76(PartB), 236–244. https://doi.org/10.1016/j.lwt.2016.07.064
Pedersen, T. B., Vogensen, F. K., & Ardö, Y. (2016). Effect of heterofermentative lactic acid bacteria of DL-starters in initial ripening of semi-hard cheese. International Dairy Journal, 57, 72–79. https://doi.org/10.1016/j.idairyj.2016.02.041
Pisanu, S., Pagnozzi, D., Pes, M., Pirisi, A., Roggio, T., Uzzau, S., & Addis, M. F. (2015). Differences in the peptide profile of raw and pasteurised ovine milk cheese and implications for its bioactive potential. International Dairy Journal, 42, 26–33. https://doi.org/10.1016/j.idairyj.2014.10.007
Redruello, B., Szwengiel, A., Ladero, V., del Rio, B., & Alvarez, M. A. (2020). Identification of technological/metabolic/environmental profiles of cheeses with high GABA contents. LWT-Food Science and Technology, 130, Article 109603. https://doi.org/10.1016/j.lwt.2020.109603
Rojo Álvaro, J., Bermejo Fraile, B., Menéndez Torre, E., Ardanaz, E., Guevara, M., & Anda Apiñániz, E. (2017). Increased incidence of thyroid cancer in Navarra (Spain). Evolution and clinical characteristics, 1986-2010. Endocrinología, Diabetes y Nutrición, 64(6), 303–309. https://doi.org/10.1016/j.endinu.2017.02.013
Rolim, F. R. L., Freitas Neto, O. C., Oliveira, M. E. G., Oliveira, C. J. B., & Queiroga, R. C. R. E. (2020). Cheeses as food matrixes for probiotics: In vitro and in vivo tests. Trends in Food Science and Technology, 100, 138–154. https://doi.org/10.1016/j.tifs.2020.04.008
Saidi, V., Sheikh-Zeinoddin, M., Kobarfard, F., & Soleimanian-Zad, S. (2020). Bioactive characteristics of a semi-hard non-starter culture cheese made from raw or pasteurized sheep’s milk. 3 Biotech, 10, Article 85. https://doi.org/10.1007/s13205-020-2075-z
Saidi, V., Sheikh-Zeinoddin, M., Kobarfard, F., Soleimanian-Zad, S., & Sedaghat Doost, A. (2020). Profiling of bioactive metabolites during the ripening of a semi-hard non-starter culture cheese to detect functional dietary neurotransmitters. Biocatalysis and Agricultural Biotechnology, 28, Article 101734. https://doi.org/10.1016/j.bcab.2020.101734
Sampaio Rigueira Ubaldo, J. C., Fernandes Carvalho, A., Moraes Fonseca, L., & Abreu Glória, M. B. (2015). Bioactive amines in Mozzarella cheese from milk with varying somatic cell counts. Food Chemistry, 178, 229–235. https://doi.org/10.1016/j.foodchem.2015.01.084
Şanlı, T., & Şenel, E. (2015). Formation of biogenic amines in cheese. In V. Preedy (Ed.), Processing and impact on active components in food (pp. 223–230). Academic Press. https://doi.org/10.1016/B978-0-12-404699-3.00027-5
Şanlier, N., Başar Gökcen, B., & Ceyhun Sezgin, A. (2019). Health benefits of fermented foods. Critical Reviews in Food Science and Nutrition, 59(3), 506–527. https://doi.org/10.1080/10408398.2017.1383355
Santiago-López, L., Aguilar-Toalá, J. E., Hernández-Mendoza, A., Vallejo-Cordoba, B., Liceaga, A. M., & González-Córdova, A. F. (2018). Invited review: Bioactive compounds produced during cheese ripening and health effects associated with aged cheese consumption. Journal of Dairy Science, 101(5), 3742–3757. https://doi.org/10.3168/jds.2017-13465
Santos, E., Marques, G., & Lino-Neto, T. (2020). Phaseolus vulgaris L. as a functional food for aging protection. In V. R. Preedy, & V. B. Patel (Eds.), Aging. Oxidative stress and dietary antioxidants (Chapter 29, 2nd ed., pp. 289–295). Academic Press. https://doi.org/10.1016/B978-0-12-818698-5.00029-8
Santos-Espinosa, A., Beltrán-Barrientos, L. M., Reyes-Díaz, R., Mazorra-Manzano, M. Á., Hernández-Mendoza, A., González-Aguilar, G. A., Sáyago-Ayerdi, S. G., Vallejo-Cordoba, B., & González-Córdova, A. F. (2020). Gamma-aminobutyric acid (GABA) production in milk fermented by specific wild lactic acid bacteria strains isolated from artisanal Mexican cheeses. Annals of Microbiology, 70, Article 12. https://doi.org/10.1186/s13213-020-01542-3
Santos-Espinosa, A., Manzanarez-Quin, C. G., Reyes-Díaz, R., Hernández-Mendoza, A., Vallejo-Cordoba, B., & González-Córdova, A. F. (2018). Ácido γ-Aminobutírico (GABA) producido por bacterias ácido lácticas en alimentos fermentados. Interciencia, 43(3), 175–181. https://bit.ly/3YXqF2N
Schettino-Bermúdez, B., Vega y León, S., Gutierrez-Tolentino, R., Pérez-González, J. J., Escobar, A., Gonzalez-Ronquillo, M., & Vargas-Bello-Pérez, E. (2020). Effect of dietary inclusion of chia seed (Salvia hispanica L.) on goat cheese fatty acid profile and conjugated linoleic acid isomers. International Dairy Journal, 105, Article 104664. https://doi.org/10.1016/j.idairyj.2020.104664
Soltani, S., Hammami, R., Cotter, P. D., Rebuffat, S., Said, L. B., Gaudreau, H., Bédard, F., Biron, E., Drider, D., & Fliss, I. (2021). Bacteriocins as a new generation of antimicrobials: toxicity aspects and regulations. FEMS Microbiology Reviews, 45(1), Article fuaa039. https://doi.org/10.1093/femsre/fuaa039
Summer, A., Formaggioni, P., Franceschi, P., Di Frangia, F., Righi, F., & Malacarne, M. (2017). Cheese as functional food: The example of Parmigiano Reggiano and Grana Padano. Food Technology and Biotechnology, 55(3), 277-289. https://doi.org/10.17113/ftb.55.03.17.5233
Tofalo, R., Perpetuini, G., Battistelli, N., Pepe, A., Ianni, A., Martino, G., & Suzzi, G. (2019). Accumulation γ-aminobutyric acid and biogenic amines in a traditional raw milk ewe’s cheese. Foods, 8(9), Article 401. https://doi.org/10.3390/foods8090401
Venegas-Ortega, M. G., Flores-Gallegos, A. C., Martínez-Hernández, J. L., Aguilar, C. N. & Nevárez-Moorillón, G. V. (2019). Production of bioactive peptides from lactic acid bacteria: A sustainable approach for healthier foods. Comprehensive Reviews in Food Science and Food Safety, 18(4), 1039–1051. https://doi.org/10.1111/1541-4337.12455
Vrdoljak, M., Mikulec, N., Markov, K., Kalit, S., & Frece, J. (2018). Aromatic compounds of cheese ripening in animal skin: An overview. Journal of Central European Agriculture, 19(2), 318–334. https://doi.org/10.5513/JCEA01/19.2.2154
Walther, B., Guggisberg, D., Schmidt, R. S., Portmann, R., Risse, M. -C., Badertscher, R., & Chollet, M. (2021). Quantitative analysis of menaquinones (vitamin K2) in various types of cheese from Switzerland. International Dairy Journal, 112, Article 104853. https://doi.org/10.1016/j.idairyj.2020.104853
Wang, Y., Wu, J., Lv, M., Shao, Z., Hungwe, M., Wang, J., Bai, X., Xie, J., Wang Y., & Geng, W. (2021). Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry. Frontiers in Bioengeeniring and Biotechnology, 9, Article 612285. https://doi.org/10.3389/fbioe.2021.612285
Wenzel, C., Irmler, S., Bisig, W., Guggisberg, D., Roetschi, A., Portmann, R., Wechsler, D., & Fröhlich-Wyder, M. -T. (2018). The effect of starters with a functional arginine deiminase pathway on cheese ripening and quality. International Dairy Journal, 85, 191–200. https://doi.org/10.1016/j.idairyj.2018.05.008
Xu, N. N., Yang, D. T., Zhang, B. X., Liu, J. X., Ye, J. A., & Ren, D. X. (2020). Influence of intramuscular injection of vitamin B12 in early-lactation dairy cows on Mozzarella cheese quality and vitamin B12 stability. Journal of Dairy Science, 103(11), 9835–9840. https://doi.org/10.3168/jds.2020-18568
Archivos adicionales
Publicado
Cómo citar
Número
Sección
Licencia
Derechos de autor 2023 Joel López-Mendoza, Lourdes Adriano-Anaya, Didiana Gálvez-López, Alfredo Vázquez-Ovando
Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial-SinDerivadas 4.0.
1. Política propuesta para revistas de acceso abierto
Los autores/as que publiquen en esta revista aceptan las siguientes condiciones:
- Los autores/as conservan los derechos morales de autor y ceden a la revista el derecho de la primera publicación, con el trabajo registrado con la licencia de atribución, no comercial y sin obra derivada de Creative Commons, que permite a terceros utilizar lo publicado siempre que mencionen la autoría del trabajo y a la primera publicación en esta revista, no se puede hacer uso de la obra con propósitos comerciales y no se puede utilizar las publicaciones para remezclar, transformar o crear otra obra.
- Los autores/as pueden realizar otros acuerdos contractuales independientes y adicionales para la distribución no exclusiva de la versión del artículo publicado en esta revista (p. ej., incluirlo en un repositorio institucional o publicarlo en un libro) siempre que indiquen claramente que el trabajo se publicó por primera vez en esta revista.
- Se permite y recomienda a los autores/as a publicar su trabajo en Internet (por ejemplo en páginas institucionales o personales) antes y durante el proceso de revisión y publicación, ya que puede conducir a intercambios productivos y a una mayor y más rápida difusión del trabajo publicado (vea The Effect of Open Access).
