Propiedades inmunomoduladoras y antivibrio de extractos de plantas para manejar la salud del camarón Penaeus vannamei
DOI:
https://doi.org/10.33936/at.v4i2.4776Keywords:
Plantas GRAS , Sistema Inmune de camarón , Detección de cuorum , Acuicultura de camarón , VibriosisAbstract
RESUMEN | Las vibriosis son enfermedades multifactoriales que causan pérdidas económicas en la industria camaronera. Como parte de un enfoque ecológico para su control, extractos acuosos de plantas generalmente reconocidas como seguras (GRAS): Allium sativum (290000 µg mL-1), Camellia sinensis (40000 µg mL-1), Morinda citrifolia (250000 µg mL-1) y Origanum vulgare (50 000 µg mL-1), fueron evaluados por sus propiedades antibacterianas, antioxidantes e inmunoestimulantes. Se inició el estudio evaluando las propiedades microbicidas de los extractos contra Vibrio spp. patógenos del camarón, así como sus características antioxidantes. Posteriormente, se encontró la concentración inhibitoria mínima y la concentración bactericida mínima (MBC) para determinar concentraciones subletales como parte de una estrategia antivirulencia. Los extractos mantuvieron la capacidad de interrumpir la bioluminiscencia y/o la formación de biopelículas en un amplio rango de dilución por debajo del MBC (alrededor de 10 a 50 veces el MBC); 1450 a 145 µg mL-1 para A. sativum, 2000 a 200 µg mL-1 para C. sinensis, 12500 a 1250 µg mL-1 para M. citrifolia y 2500 a 250 µg mL-1 para O. vulgare. Todos los extractos de plantas exhibieron características antioxidantes, modulando de manera diferencial la generación de superóxido según el extracto de la planta, sin afectar significativamente las tasas de generación de superóxido, a las concentraciones más bajas ensayadas. Los resultados más consistentes se obtuvieron del ensayo realizado con extracto de A. sativum, el cual exhibió poderosas propiedades para eliminar el superóxido de los hemocitos no estimulados en concentraciones que oscilaron entre 14500 y 1,45 µg mL-1. En estanques de tierra experimentales (400 m2, cuatro repeticiones por tratamiento), los camarones tratados con extractos de plantas añadidos
al alimento en concentraciones inmunomoduladoras (A. sativum: 36 µg por g, M. citrifolia: 36 µg por g) exhibieron una melanosis reducida. Además, los camarones tratados con A. sativum tuvieron el mayor tamaño a la cosecha. Estos resultados indican que los extractos acuosos de A. sativum, C. sinensis, O. vulgare y M. citrifolia pueden promover la salud de los camarones debido a sus propiedades antioxidantes, inmunomoduladoras y antimicrobianas.
Downloads
References
Adineh, H., Harsij, M., Jafaryan, H., & Asadi, M. (2020). The effects of microencapsulated garlic (Allium sativum) extract on growth performance, body composition, immune response and antioxidant status of rainbow trout (Oncorhynchus mykiss) juveniles. Journal of Applied Animal Research, 48(1):372-378. https://doi.org/10.1080/09712119.2020.1808473.
AftabUddin, S., Siddique, M. A. M., Romkey, S. S., & Shelton, W. L. (2017). Antibacterial function of herbal extracts on growth, survival and immunoprotection in the black tiger shrimp Penaeus monodon. Fish & Shellfish Immunology, 65:52-58. https://doi.org/10.1016/j.fsi.2017.03.050.
Akinbowale, O. l., Peng, H., & Barton, M. d. (2007). Diversity of tetracycline resistance genes in bacteria from aquaculture sources in Australia. Journal of Applied Microbiology, 103(5):2016-2025. https://doi.org/10.1111/j.1365-2672.2007.03445.x.
Arvaniti, O. S., Samaras, Y., Gatidou, G., Thomaidis, N. S., & Stasinakis, A. S. (2019). Review on fresh and dried figs: Chemical analysis and occurrence of phytochemical compounds, antioxidant capacity and health effects. Food Research International, 119,: 244-267. https://doi.org/10.1016/j.foodres.2019.01.055
Asimi, O., & Sahu, N. (2013). Herbs/spices as feed additive in aquaculture. Scientific Journal of Pure and Applied Sciences, 2:284-292. doi: 10.14196/sjpas.v2i8.868.
Beshiru, A., & Igbinosa, E. O. (2018). Characterization of extracellular virulence properties and biofilm-formation capacity of Vibrio species recovered from ready-to-eat (RTE) shrimps. Microbial Pathogenesis, :93-102. https://doi.org/10.1016/j.micpath.2018.04.015.
Breyer, K. E., Getchell, R. G., Cornwell, E. R., Wooster, G. A., Ketola, H. G., & Bowser, P. R. (2015). Efficacy of an Extract from Garlic, Allium sativum, Against Infection with the Furunculosis Bacterium, Aeromonas salmonicida, in Rainbow Trout, Oncorhynchus mykiss. Journal of the World Aquaculture Society, 46(3):273-282. https://doi.org/10.1111/jwas.12195.
Castex, M., Lemaire, P., Wabete, N., & Chim, L. (2010). Effect of probiotic Pediococcus acidilactici on antioxidant defences and oxidative stress of Litopenaeus stylirostris under Vibrio nigripulchritudo challenge. Fish & Shellfish Immunology, 28(4):622-631. https://doi.org/10.1016/j.fsi.2009.12.024
De Queiroz, Y. S., Antunes, P. B., Vicente, S. J. V., Sampaio, G. R., Shibao, J., Bastos, D. H. M., & Torres, E. A. F. da S. (2014). Bioactive compounds, in vitro antioxidant capacity and Maillard reaction products of raw, boiled, and fried garlic (Allium sativum L.). International Journal of Food Science & Technology, 49(5):1308-1314. https://doi.org/10.1111/ijfs.12428.
Defoirdt, T., Boon, N., & Bossier, P. (2010). Can Bacteria Evolve Resistance to Quorum Sensing Disruption? PLOS Pathogens, 6(7), e1000989. https://doi.org/10.1371/journal.ppat.1000989.
Dixon, M. P. (1968). Organoleptic qualities. International Journal of Food Science & Technology, 3(s1):423-429. https://doi.org/10.1111/j.1365-2621.1968.tb01484.x.
Djordjevic, D., Wiedmann, M., & McLandsborough, L. A. (2002). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied and Environmental Microbiology, 68(6):2950-2958. https://doi.org/10.1128/AEM.68.6.2950-2958.2002.
Done, H. Y., & Halden, R. U. (2015). Reconnaissance of 47 antibiotics and associated microbial risks in seafood sold in the United States. Journal of Hazardous Materials, 282:10-17. https://doi.org/10.1016/j.jhazmat.2014.08.075.
Duan, Y., Zhang, J., Dong, H., Wang, Y., Liu, Q., & Li, H. (2015). Oxidative stress response of the black tiger shrimp Penaeus monodon to Vibrio parahaemolyticus challenge. Fish & Shellfish Immunology, 46(2):354-365. https://doi.org/10.1016/j.fsi.2015.06.032.
Elumalai, P., Kurian, A., Lakshmi, S., Faggio, C., Esteban, M. A., & Ringø, E. (2021). Herbal Immunomodulators in Aquaculture. Reviews in Fisheries Science & Aquaculture, 29(1):33-57. https://doi.org/10.1080/23308249.2020.1779651.
Fakharzadeh, S. M. E., Haghighi, M., Rohani, S., Sharifpour, I., & Hamidi, M. (2020). An in vitro and in vivo study on antimicrobial activity of Origanum vulgare extract and its nano form against Streptococcus iniae in rainbow trout (Oncorhynchus mykiss). Iranian Journal of Fisheries Sciences, 19(5):2454-2463.
García Beltrán, J. M., Silvera, D. G., Ruiz, C. E., Campo, V., Chupani, L., Faggio, C., & Esteban, M. Á. (2020). Effects of dietary Origanum vulgare on gilthead seabream (Sparus aurata L.) immune and antioxidant status. Fish & Shellfish Immunology, 99:452-461. https://doi.org/10.1016/j.fsi.2020.02.040.
Gullian Klanian, M., & Rodríguez, J. (2001). Estudio de las cualidades inmunoestimulantes de bacterias probióticas asociadas al cultivo de Litopenaeus vannamei. Tesis de Pregrado. Escuela Superior Politécnica del Litoral, Guayaquil, Ecuador.
Han, J. E., Tang, K. F. J., Tran, L. H., & Lightner, D. V. (2015). Photorhabdus insect-related (Pir) toxin-like genes in a plasmid of Vibrio parahaemolyticus, the causative agent of acute hepatopancreatic necrosis disease (AHPND) of shrimp. Diseases of Aquatic Organisms, 113(1):33-40. https://doi.org/10.3354/dao02830.
Hasanpour, S., Salati, A. P., Falahatkar, B., & Azarm, H. M. (2017). Effects of dietary green tea (Camellia sinensis L.) supplementation on growth performance, lipid metabolism, and antioxidant status in a sturgeon hybrid of Sterlet (Huso huso ♂ × Acipenser ruthenus ♀) fed oxidized fish oil. Fish Physiology and Biochemistry, 43(5):1315-1323. https://doi.org/10.1007/s10695-017-0374-z.
Herrera-Calderon, O., Chacaltana-Ramos, L. J., Huayanca-Gutiérrez, I. C., Algarni, M. A., Alqarni, M., & Batiha, G. E.-S. (2021). Chemical Constituents, In Vitro Antioxidant Activity and In Silico Study on NADPH Oxidase of Allium sativum L. (Garlic) Essential Oil. Antioxidants, 10(11):1844. https://doi.org/10.3390/antiox10111844.
Jahanjoo, V., Yahyavi, M., Akrami, R., & Bahri, A. H. (2018). Influence of adding garlic (Allium sativum), ginger (Zingiber officinale), thyme (Thymus vulgaris) and their combination on the growth performance, haemato-immunological parameters and disease resistance to Photobacterium damselae in Sobaity Sea Bream (Sparidentex hasta) Fry. Turkish Journal of Fisheries and Aquatic Sciences, 18(4):633-645. https://doi.org/10.4194/1303-2712-v18_4_15.
Jiang, X.-Y., Liang, J.-Y., Jiang, S.-Y., Zhao, P., Tao, F., Li, J., Li, X.-X., & Zhao, D.-S. (2022). Garlic polysaccharides: A review on their extraction, isolation, structural characteristics, and bioactivities. Carbohydrate Research, 518, 108599. https://doi.org/10.1016/j.carres.2022.108599.
Kakoolaki, S., Akbary, P., Zorriehzahra, M. J., Salehi, H., Sepahdari, A., Afsharnasab, M., Mehrabi, M. R., & Jadgal, S. (2016). Camellia sinensis supplemented diet enhances the innate non-specific responses, haematological parameters, and growth performance in Mugil cephalus against Photobacterium damselae. Fish & Shellfish Immunology, 57: 379-385. https://doi.org/10.1016/j.fsi.2016.08.060.
Kiran, G. S., Lipton, A. N., Priyadharshini, S., Anitha, K., Suárez, L. E. C., Arasu, M. V., Choi, K. C., Selvin, J., & Al-Dhabi, N. A. (2014). Antiadhesive activity of poly-hydroxy butyrate biopolymer from a marine Brevibacterium casei MSI04 against shrimp pathogenic vibrios. Microbial Cell Factories, 13(1):114. https://doi.org/10.1186/s12934-014-0114-3.
Knight, J. A. (2000). Review: Free radicals, antioxidants, and the immune system. Annals of Clinical & Laboratory Science, 30(2):145-158.
Kongchum, P., Chimtong, S., Chareansak, N., & Subprasert, P. (2016). Effect of Green Tea Extract on Vibrio parahaemolyticus Inhibition in Pacific White Shrimp (Litopenaeus vannamei) Postlarvae. Agriculture and Agricultural Science Procedia, 11:117-124. https://doi.org/10.1016/j.aaspro.2016.12.020.
Loo, K.-Y., Letchumanan, V., Law, J. W.-F., Pusparajah, P., Goh, B.-H., Ab Mutalib, N.-S., He, Y.-W., & Lee, L.-H. (2020). Incidence of antibiotic resistance in Vibrio spp. Reviews in Aquaculture, 12(4):2590-2608. https://doi.org/10.1111/raq.12460.
Lu, L., Li, M., Yi, G., Liao, L., Cheng, Q., Zhu, J., Zhang, B., Wang, Y., Chen, Y., & Zeng, M. (2022). Screening strategies for quorum sensing inhibitors in combating bacterial infections. Journal of Pharmaceutical Analysis, 12(1):1-14. https://doi.org/10.1016/j.jpha.2021.03.009.
Ly, H. T., Pham Nguyen, M. T., Nguyen, T. K. O., Bui, T. P. Q., Ke, X., & Le, V. M. (2020). Phytochemical Analysis and Wound-Healing Activity of Noni (Morinda citrifolia) Leaf Extract. Journal of Herbs, Spices & Medicinal Plants, 26(4):379-393. https://doi.org/10.1080/10496475.2020.1748159.
Marisa Halim, A., Lee, P.-P., Chang, Z.-W., & Chang, C.-C. (2017). The hot-water extract of leaves of noni, Morinda citrifolia, promotes the immunocompetence of giant freshwater prawn, Macrobrachium rosenbergii. Fish & Shellfish Immunology, 64:457-468. https://doi.org/10.1016/j.fsi.2017.03.045.
McFARLAND, J. (1907). The nephelometer: an instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. Journal of the American Medical Association, 49(14):1176-1178. https://doi.org/10.1001/jama.1907.25320140022001f.
Meek, R. W., Vyas, H., & Piddock, L. J. V. (2015). Nonmedical Uses of Antibiotics: Time to Restrict Their Use? PLOS Biology, 13(10):e1002266. https://doi.org/10.1371/journal.pbio.1002266.
Mendonça-Filho, R. R. (2006). Bioactive Phytocompounds: New Approaches in the Phytosciences. En Modern Phytomedicine (pp. 1-24). John Wiley & Sons, Ltd. https://doi.org/10.1002/9783527609987.ch1
Mohammadi, G., Rafiee, G., El Basuini, M. F., Van Doan, H., Ahmed, H. A., Dawood, M. A. O., & Abdel-Latif, H. M. R. (2020). Oregano (Origanum vulgare), St John’s-wort (Hypericum perforatum), and lemon balm (Melissa officinalis) extracts improved the growth rate, antioxidative, and immunological responses in Nile tilapia (Oreochromis niloticus) infected with Aeromonas hydrophila. Aquaculture Reports, 18:100445. https://doi.org/10.1016/j.aqrep.2020.100445.
Mohan, K., Ravichandran, S., Muralisankar, T., Uthayakumar, V., Chandirasekar, R., Seedevi, P., Abirami, R. G., & Rajan, D. K. (2019a). Application of marine-derived polysaccharides as immunostimulants in aquaculture: A review of current knowledge and further perspectives. Fish & Shellfish Immunology, 86:1177-1193. https://doi.org/10.1016/j.fsi.2018.12.072.
Mohan, K., Ravichandran, S., Muralisankar, T., Uthayakumar, V., Chandirasekar, R., Seedevi, P., & Rajan, D. K. (2019b). Potential uses of fungal polysaccharides as immunostimulants in fish and shrimp aquaculture: A review. Aquaculture, 500:250-263. https://doi.org/10.1016/j.aquaculture.2018.10.023.
Morales-Covarrubias, M. S., García-Aguilar, N., Bolan-Mejía, M. D., & Puello-Cruz, A. C. (2016). Evaluation of medicinal plants and colloidal silver efficiency against Vibrio parahaemolyticus infection in Litopenaeus vannamei cultured at low salinity. Diseases of Aquatic Organisms, 122(1):57-65. https://doi.org/10.3354/dao03060.
Mukherjee, S., & Bassler, B. L. (2019). Bacterial quorum sensing in complex and dynamically changing environments. Nature Reviews Microbiology, 17(6):371-382. https://doi.org/10.1038/s41579-019-0186-5
Muñoz, M., Cedeño, R., Rodrı́guez, J., van der Knaap, W. P. W., Mialhe, E., & Bachère, E. (2000). Measurement of reactive oxygen intermediate production in haemocytes of the penaeid shrimp, Penaeus vannamei. Aquaculture, 191(1):89-107. https://doi.org/10.1016/S0044-8486(00)00420-8.
Nelson, S. C., & Elevitch, C. R. (2006). Noni: The Complete Guide for Consumers and Growers. PAR.
Ngo, S. N. T., Williams, D. B., Cobiac, L., & Head, R. J. (2007). Does garlic reduce risk of colorectal cancer? A systematic review. The Journal of Nutrition, 137(10):2264-2269. https://doi.org/10.1093/jn/137.10.2264.
Obeagu, E. (2018). A Review on Free Radicals and Antioxidants. 4:123-133. https://doi.org/10.22192/ijcrms.2018.04.02.019.
Ozdemir, N., Ozgen, Y., Kiralan, M., Bayrak, A., Arslan, N., & Ramadan, M. F. (2018). Effect of different drying methods on the essential oil yield, composition and antioxidant activity of Origanum vulgare L. and Origanum onites L. Journal of Food Measurement and Characterization, 12(2):820-825. https://doi.org/10.1007/s11694-017-9696-x
Palanikumar, P., Wahjuningrum, D., Abinaya, P., Babu, M. M., & Citarasu, T. (2020). Usage of plant natural products for prevention and control of white feces syndrome (WFS) in Pacific whiteleg shrimp Litopenaeus vannamei farming in India. Aquaculture International, 28(1):113-125. https://doi.org/10.1007/s10499-019-00448-5.
Pandy, V., Bonam, S. R., Raya, A. R., & Nadendla, R. R. (2020). Chapter 19—Morinda citrifolia Linn. (Noni) fruit, antioxidant effects, and neuroprotection. En C. R. Martin & V. R. Preedy (Eds.), Oxidative Stress and Dietary Antioxidants in Neurological Diseases (pp. 291-307). Academic Press. https://doi.org/10.1016/B978-0-12-817780-8.00019-0.
Parsek, M. R., & Greenberg, E. P. (2005). Sociomicrobiology: The connections between quorum sensing and biofilms. Trends in Microbiology, 13(1):27-33. https://doi.org/10.1016/j.tim.2004.11.007.
Passos da Silva, D., Schofield, M. C., Parsek, M. R., & Tseng, B. S. (2017). An Update on the Sociomicrobiology of Quorum Sensing in Gram-Negative Biofilm Development. Pathogens, 6(4):51. https://doi.org/10.3390/pathogens6040051.
Phan, A. D. T., Netzel, G., Chhim, P., Netzel, M. E., & Sultanbawa, Y. (2019). Phytochemical Characteristics and Antimicrobial Activity of Australian Grown Garlic (Allium sativum L.) Cultivars. Foods, 8(9):358. https://doi.org/10.3390/foods8090358.
Piyanut Chirawithayaboon, Nontawith Areechon, & Oraporn Meunpol. (s. f.). | Hepatopancreatic antioxidant enzyme activities and disease resistance of Pacific white shrimp (Litopenaeus vannamei) fed diet supplemented with garlic (Allium sativum) extract. Agriculture and Natural Resources, 54(4):377-386. https://li01.tci-thaijo.org/index.php/anres/article/view/247954.
El Productor, E. (06 enero 2020). Prohíben ingreso de camarones de algunos exportadores de Malasia por presencia de antibióticos | Noticias Agropecuarias. https://elproductor.com/2020/01/prohiben-ingreso-de-camarones-de-algunos-exportadores-de-malasia-por-presencia-de-antibioticos/
Rani, R., Arora, S., Kaur, J., & Manhas, R. K. (2018). Phenolic compounds as antioxidants and chemopreventive drugs from Streptomyces cellulosae strain TES17 isolated from rhizosphere of Camellia sinensis. BMC Complementary and Alternative Medicine, 18(1):82. https://doi.org/10.1186/s12906-018-2154-4.
Ravipati, A. S., Zhang, L., Koyyalamudi, S. R., Jeong, S. C., Reddy, N., Bartlett, J., Smith, P. T., Shanmugam, K., Münch, G., Wu, M. J., Satyanarayanan, M., & Vysetti, B. (2012). Antioxidant and anti-inflammatory activities of selected Chinese medicinal plants and their relation with antioxidant content. BMC Complementary and Alternative Medicine, 12:173. https://doi.org/10.1186/1472-6882-12-173.
Reverter, M., Tapissier‐Bontemps, N., Sarter, S., Sasal, P., & Caruso, D. (2021). Moving towards more sustainable aquaculture practices: A meta‐analysis on the potential of plant‐enriched diets to improve fish growth, immunity and disease resistance. Reviews in Aquaculture, 13(1):537-555. https://doi.org/10.1111/raq.12485.
Rivlin, R. S. (2009). Can garlic reduce risk of cancer?123. The American Journal of Clinical Nutrition, 89(1):17-18. https://doi.org/10.3945/ajcn.2008.27181.
SINGH, M., Mallick, A. K., BANERJEE, M., & KUMAR, R. (2016). Loss of outer membrane integrity in Gram-negative bacteria by silver nanoparticles loaded with Camellia sinensis leaf phytochemicals: Plausible mechanism of bacterial cell disintegration. Bulletin of Materials Science, 39(7):1871-1878. https://doi.org/10.1007/s12034-016-1317-5.
Soković, M., Glamočlija, J., Marin, P. D., Brkić, D., & van Griensven, L. J. L. D. (2010). Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model. Molecules (Basel, Switzerland), 15(11):7532-7546. https://doi.org/10.3390/molecules15117532.
Srinivasan, R., Santhakumari, S., & Ravi, A. V. (2017). In vitro antibiofilm efficacy of Piper betle against quorum sensing mediated biofilm formation of luminescent Vibrio harveyi. Microbial Pathogenesis, 110:232-239. https://doi.org/10.1016/j.micpath.2017.07.001.
Stefanakis, M. K., Anastasopoulos, E., Katerinopoulos, H. E., & Makridis, P. (2014). Use of essential oils extracted from three Origanum species for disinfection of cultured rotifers (Brachionus plicatilis). Aquaculture Research, 45(11):1861-1866. https://doi.org/10.1111/are.12137.
Sutton, S. (2011). Measurement of Microbial Cells by Optical Density. Journal of Validation Technology, 4;46-49.
Talpur, A. D., & Ikhwanuddin, M. (2012). Dietary effects of garlic (Allium sativum) on haemato-immunological parameters, survival, growth, and disease resistance against Vibrio harveyi infection in Asian sea bass, Lates calcarifer (Bloch). Aquaculture, 364-365:6-12. https://doi.org/10.1016/j.aquaculture.2012.07.035.
Vandenberghe, J., Verdonck, L., Robles-Arozarena, R., Rivera, G., Bolland, A., Balladares, M., Gomez-Gil, B., Calderon, J., Sorgeloos, P., & Swings, J. (1999). Vibrios associated with Litopenaeus vannamei larvae, postlarvae, broodstock, and hatchery probionts. Applied and Environmental Microbiology, 65(6):2592-2597. https://doi.org/10.1128/AEM.65.6.2592-2597.1999.
Velázquez-Lizárraga, A. E., Juárez-Morales, J. L., Racotta, I. S., Villarreal-Colmenares, H., Valdes-Lopez, O., Luna-González, A., Rodríguez-Jaramillo, C., Estrada, N., & Ascencio, F. (2019). Transcriptomic analysis of Pacific white shrimp (Litopenaeus vannamei, Boone 1931) in response to acute hepatopancreatic necrosis disease caused by Vibrio parahaemolyticus. PLOS ONE, 14(8):e0220993. https://doi.org/10.1371/journal.pone.0220993.
Walker, R. B., & Everette, J. D. (2009). Comparative reaction rates of various antioxidants with ABTS radical cation. Journal of Agricultural and Food Chemistry, 57(4):1156-1161. https://doi.org/10.1021/jf8026765
Wan, Q., Li, N., Du, L., Zhao, R., Yi, M., Xu, Q., & Zhou, Y. (2019). Allium vegetable consumption and health: An umbrella review of meta-analyses of multiple health outcomes. Food Science & Nutrition, 7(8):2451-2470. https://doi.org/10.1002/fsn3.1117.
Wei, L. S., Musa, N., Sengm, C. T., Wee, W., & Shazili, N. a. M. (2008). Antimicrobial properties of tropical plants against 12 pathogenic bacteria isolated from aquatic organisms. African Journal of Biotechnology, 7(13):2275-2278. https://doi.org/10.4314/ajb.v7i13.58974.
Yano, Y., Satomi, M., & Oikawa, H. (2006). Antimicrobial effect of spices and herbs on Vibrio parahaemolyticus. International Journal of Food Microbiology, 111(1):6-11. https://doi.org/10.1016/j.ijfoodmicro.2006.04.031.
Zhao, W., Wang, L., Liu, M., Jiang, K., Qi, C., Yang, G., & Wang, B. (2017). The effects of Vibrio parahaemolyticus on hepatopancreas antioxidant enzyme activity and gene expression of Litopenaeus vannamei. Journal of Fishery Sciences of China 24(6):1261-1270 DOI:10.3724/SP.J.1118.2017.16221.
Published
Issue
Section
License
Copyright (c) 2022 María Gabriela Agurto Rodríguez, MSc, Jennny Antonia Rodríguez León, Ph.D., Cristobal Leonardo Domínguez Borbor, MSc, Cecilia Nelly Tomalá Beltrán, MSc, Rosa María Malave Orrala

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

