Efecto de prebióticos y probióticos en la expresión y actividad de fenoloxidasa en camarones Penaeus: Meta-análisis

Main Article Content

Yailén de la Caridad Valdes Vaillant
https://orcid.org/0000-0001-7709-6192
Juliet Mejías Palmero
https://orcid.org/0000-0002-4388-5254
Yulaine Corrales Barrios
https://orcid.org/0000-0003-4757-1911
Marileyxis Regla López Rodríguez
https://orcid.org/0000-0001-6967-0596
Taimy Hernández Sariego
https://orcid.org/0000-0002-9638-2765
Amilcar Arenal Cruz
https://orcid.org/0000-0003-2912-9871
Peter Bossier
https://orcid.org/0000-0002-6165-9111

Resumen

Contexto: Los inmunoestimulantes estimulan la respuesta inmune y el crecimiento, incrementan la resistencia al estrés y a las enfermedades enacuicultura. A veces se encuentran resultados contradictorios que brindan confusión acerca del empleo de ellos, por lo que se planteó como problema: ¿Pudiera la literatura científica relacionada con prebióticos y probióticos, donde se evalúen los indicadores del sistema inmune del camarón, servir como base para la toma de decisiones en empleo de inmunoestimulantes en la camaronicultura?


Objetivo: Evaluar la influencia de prebióticos y probióticos en la expresión y actividad fenoloxidasa de camarones Penaeus, mediante un meta-análisis que permita la toma de decisiones para su empleo en la camaronicultura.


Métodos: Se realizaron búsquedas en Pubmed, Science Direct, Scopusdesde el 2008 hasta el 2019 sobre la influencia de inmunoestimulantes en la actividad fenoloxidasa y expresión de genes. El análisis estadístico se realizó con el programa Jasp Metaanalysis Versión 0.9.2. a un 95% de confianza.


Resultados: Se obtuvieron 262 artículos científicos sobre evaluación de prebióticos y probióticos en camarones Penaeus. De estos, 61 cumplieron los criterios de inclusión para la respuesta inmunológica: 51evaluaronla actividad de fenoloxidasa y 11 la profenoloxidasa. Tanto los prebióticos como los probióticos estimulan la enzima y la proenzima; los extractos de plantas fueron los que más modificaron esta actividad y los Bacillus fue el género que más estimuló.


Conclusiones: La literatura científica relacionada con fenoloxidasa en camarones Penaeus indican que se deben evaluar con cuidado, debido al diseño experimental y la forma que expresan los resultados.

Article Details

Cómo citar
Valdes Vaillant, Y., Mejías Palmero, J., Corrales Barrios, Y., López Rodríguez, M., Hernández Sariego, T., Arenal Cruz, A., & Bossier, P. (2020). Efecto de prebióticos y probióticos en la expresión y actividad de fenoloxidasa en camarones Penaeus: Meta-análisis. Agrisost, 26(3), 1-16. Recuperado a partir de https://revistas.reduc.edu.cu/index.php/agrisost/article/view/e3279
Sección
Revisión sistemática y metaanálisis

Citas

Ajadi, A., Sabri, M., Dauda, A. B., Ina-Salwany, M., & Hasliza, A. (2016). Immunoprophylaxis: A better alternative protective measure against shrimp vibriosis–a review. PJSSR, 2(2), 58-69. Recuperado el 10 de diciembre se 2019, de: https://www.researchgate.net/profile/Akeem_Dauda/publication/304134799_PJSRR_2016_22_58-69_Immunoprophylaxis_A_Better_Alternative_Protective_Measure_against_Shrimp_Vibriosis_-A_Review/links/57679af508aeb4b998098ae8.pdf
Anas, A., Lowman, D. W., Williams, D. L., Millen, S., Pai, S. S., Sajeevan, T. P., . . . Singh, I.S.B. (2009). Alkali insoluble glucan extracted from Acremonium diospyri is a more potent immunostimulant in the Indian White Shrimp, Fenneropenaeus indicus than alkali soluble glucan. Aquaculture Research, 40(11), 1320-1327, doi: https://doi.org/10.1111/j.1365-2109.2009.02231.x
Arenal, A., Pimentel, R., Pimentel, E., Martín, L., Santiesteban, D., Franco, R., & Aleström, P. (2008). Growth enhancement of shrimp (Litopenaeus schmitti) after transfer of tilapia growth hormone gene. Biotechnology letters, 30(5), 845-851, doi: https://doi.org/10.1007/s10529-008-9636-2
Bai, N., Zhang, W., Mai, K., Wang, X., Xu, W., & Ma, H. (2010). Effects of discontinuous administration of β-glucan and glycyrrhizin on the growth and immunity of white shrimp Litopenaeus vannamei. Aquaculture, 306(1-4), 218-224, doi: https://doi.org/10.1016/j.aquaculture.2010.06.017
Bernal, M. G., Marrero, R. M., Campa-Córdova, Á. I., & Mazón-Suástegui, J. M. (2017). Probiotic effect of Streptomyces strains alone or in combination with Bacillus and Lactobacillus in juveniles of the white shrimp Litopenaeus vannamei. Aquaculture international, 25(2), 927-939. doi: https://doi.org/10.1007/s10499-016-0085-y
Bolivar, N. C., Legarda, E. C., Seiffert, W. Q., Andreatta, E. R., & Vieira, F. d. N. (2018). Combining a probiotic with organic salts presents synergistic in vitro inhibition against aquaculture bacterial pathogens. Brazilian Archives of Biology and Technology, 61, doi: https://doi.org/10.1590/1678-4324-2018160694
Braga, A., Lopes, D., Magalhães, V., Klosterhoff, M. C., Romano, L. A., Poersch, L. H., & Wasielesky, W. (2018). Hemocytic melanization in shrimp spermatophores. Aquaculture, 486, 64-67, doi: https://doi.org/10.1016/j.aquaculture.2017.12.018
Bui, H.T.D., Khosravi, S., Lee, C., Kim, M.-G., Lim, S.-J., Shin, C.-H., . . . Lee, K.-J. (2017). Supplemental Effects of AAMC, an Anionic Alkali Mineral Complex, in Diets for Pacific White Shrimp (Litopenaeus vannamei). The Israeli Journal of Aquaculture -Bamidgeh, 69. Recuperado el 10 de diciembre se 2019, de: http://hdl.handle.net/10524/57039
Chandran, M. N., Iyapparaj, P., Moovendhan, S., Ramasubburayan, R., Prakash, S., Immanuel, G., & Palavesam, A. (2014). Influence of probiotic bacterium Bacillus cereus isolated from the gut of wild shrimp Penaeus monodon in turn as a potent growth promoter and immune enhancer in P. monodon. Fish & shellfish immunology, 36(1), 38-45, doi: https://doi.org/10.1016/j.fsi.2013.10.004
Chandran, M. N., Suganya, A. M., Immanuel, G., & Palavesam, A. (2017). Immunomodulatory and Growth-Promoting Potential of Lowcost Probiotic Product in Penaeus monodon Culture System. Croatian journal of fisheries,75(2), 58-66, doi: https://doi.org/10.1515/cjf-2017-0009
Chang, Y.-H., Kumar, R., Ng, T. H., & Wang, H.-C. (2018). What vaccination studies tell us about immunological memory within the innate immune system of cultured shrimp and crayfish. Developmental & Comparative Immunology, 80, 53-66, doi: https://doi.org/10.1016/j.dci.2017.03.003
Chen, Y.-Y., Chen, J.-C., Kuo, Y.-H., Lin, Y.-C., Chang, Y.-H., Gong, H.-Y., & Huang, C.-L. (2016). Lipopolysaccharide and β-1, 3-glucan-binding protein (LGBP) bind to seaweed polysaccharides and activate the prophenoloxidase system in white shrimp Litopenaeus vannamei. Developmental & Comparative Immunology, 55, 144-151, doi: https://doi.org/10.1016/j.dci.2015.10.023
Chomwong, S., Charoensapsri, W., Amparyup, P., & Tassanakajon, A. (2018). Two host gut-derived lactic acid bacteria activate the proPO system and increase resistance to an AHPND-causing strain of Vibrio parahaemolyticus in the shrimp Litopenaeus vannamei. Developmental & Comparative Immunology, 89, 54-65, doi: https://doi.org/10.1016/j.dci.2018.08.002
Dawood, M. A., Koshio, S., & Esteban, M. Á. (2018). Beneficial roles of feed additives as immunostimulants in aquaculture: a review. Reviews in Aquaculture, 10(4), 950-974, doi: https://doi.org/10.1111/raq.12209
De, D., Ananda Raja, R., Ghoshal, T. K., Mukherjee, S., & Vijayan, K. K. (2018). Evaluation of growth, feed utilization efficiency and immune parameters in tiger shrimp (Penaeus monodon) fed diets supplemented with or diet fermented with gut bacterium Bacillus sp. DDKRC1. isolated from gut of Asian seabass (Lates calcarifer). Aquaculture Research, 49(6), 2147-2155, doi: https://doi.org/10.1111/are.13669
Declarador, R. S., Serrano Jr, A. E., & Corre Jr, V. L. (2014). Ulvan extract acts as immunostimulant against white spot syndrome virus (WSSV) in juvenile black tiger shrimp Penaeus monodon. Aquaculture, Aquarium, Conservation & Legislation, 7(3), 153-161. Recuperado el 9 de diciembre se 2019, de: http://www.bioflux.com.ro/docs/2014.153-161.pdf
Dineshkumar, M., Kannappan, S., & Sivakumar, K. (2017). Effect of mangrove plant (Sesuvium portulacastrum) extract against Vibrio harveyi during shrimp larviculture. Journal of Environmental Biology, 38(1), 47-53, doi: https://doi.org/10.5958/2349-2104.2015.00011.X
Duan, Y., Wang, Y., Zhang, J., Sun, Y., & Wang, J. (2018). Dietary effects of succinic acid on the growth, digestive enzymes, immune response and resistance to ammonia stress of Litopenaeus vannamei. Fish & shellfish immunology, 78, 10-17, doi: https://doi.org/10.1016/j.fsi.2018.04.008
FAO. (2018). The State of World Fisheries and Aquaculture 2018 - Meeting the sustainable development goals. Recuperado el 6 de septiembre de 2019, de: https://ec.europa.eu/knowledge4policy/publication/state-world-fisheries-aquaculture-2018_en
Franco, R., Arenal, A., Martín, L., Martinez, Y., Santiesteban, D., Sotolongo, J., . . . Bossier, P. (2016). Psychrobacter sp. 17-1 enhances growth and survival in early postlarvae of white shrimp, Penaeus vannamei Boone, 1931 (Decapoda, Penaeidae). Crustaceana, 89(13), 1467-1484, doi: https://dx.doi.org/10.1163/15685403-00003595
Franco, R., Martín, L., Arenal, A., Santiesteban, D., Sotolongo, J., Cabrera, H., . . . Castillo, N. M. (2017). Evaluation of two probiotics used during farm production of white shrimp Litopenaeus vannamei (Crustacea: Decapoda). Aquaculture Research, 48(4), 1936-1950. doi: https://doi.org/10.1111/are.13031
Fu, L.-L., Shuai, J.-B., Xu, Z.-R., Li, J.-R., & Li, W.-F. (2010). Immune responses of Fenneropenaeus chinensis against white spot syndrome virus after oral delivery of VP28 using Bacillus subtilis as vehicles. Fish & shellfish immunology, 28(1), 49-55, doi: https://doi.org/10.1016/j.fsi.2009.09.016
Ge, H., Li, J., Chen, P., Chang, Z., Shen, M., & Zhao, F. (2017). Cultivation of green algae Platymonas helgolandica in rearing water enhances the growth performance and resistance of Litopenaeus vannamei against Vibrio parahaemolyticus infection. Aquaculture international, 25(3), 1279-1290, doi: https://doi.org/10.1007/s10499-017-0113-6
Harikrishnan, R., Balasundaram, C., Jawahar, S., & Heo, M.-S. (2011). Solanum nigrum enhancement of the immune response and disease resistance of tiger shrimp, Penaeus monodon against Vibrio harveyi. Aquaculture, 318(1-2), 67-73, doi: https://doi.org/10.1016/j.aquaculture.2011.05.024
He, W., Rahimnejad, S., Wang, L., Song, K., Lu, K., & Zhang, C. (2017). Effects of organic acids and essential oils blend on growth, gut microbiota, immune response and disease resistance of Pacific white shrimp (Litopenaeus vannamei) against Vibrio parahaemolyticus. Fish & shellfish immunology, 70, 164-173, doi: https://doi.org/10.1016/j.fsi.2017.09.007
Higgins, J. P. T., & Thompson, S. G. (2002). Quantifying heterogeneity in a meta‐analysis. Statistics in medicine, 21(11), 1539-1558, doi: https://doi.org/10.1002/sim.1186
Hsieh, T.-J., Wang, J.-C., Hu, C.-Y., Li, C.-T., Kuo, C.-M., & Hsieh, S.-L. (2008). Effects of rutin from Toona sinensis on the immune and physiological responses of white shrimp (Litopenaeus vannamei) under Vibrio alginolyticus challenge. Fish & shellfish immunology, 25(5), 581-588, doi: https://doi.org/10.1016/j.fsi.2008.07.014
Hu, X., Yang, H. L., Yan, Y.Y., Zhang, C. X., Ye, J.d., Lu, K. L., . . . Sun, Y. Z. (2019). Effects of fructooligosaccharide on growth, immunity and intestinal microbiota of shrimp (Litopenaeus vannamei) fed diets with fish meal partially replaced by soybean meal. Aquaculture Nutrition, 25(1), 194-204, doi: https://doi.org/10.1111/anu.12843
Huang, X., Zhou, H., & Zhang, H. (2006). The effect of Sargassum fusiforme polysaccharide extracts on vibriosis resistance and immune activity of the shrimp, Fenneropenaeus chinensis. Fish & shellfish immunology, 20(5), 750-757, doi: https://doi.org/10.1016/j.fsi.2005.09.008
Huynh, T. G., Cheng, A.-C., Chi, C.-C., Chiu, K.-H., & Liu, C.-H. (2018). A synbiotic improves the immunity of white shrimp, Litopenaeus vannamei: Metabolomic analysis reveal compelling evidence. Fish & shellfish immunology, 79, 284-293, doi: https://doi.org/10.1016/j.fsi.2018.05.031
Huynh, T. G., Hu, S. Y., Chiu, C. S., Truong, Q. P., & Liu, C. H. (2019). Bacterial population in intestines of white shrimp, Litopenaeus vannamei fed a synbiotic containing Lactobacillus plantarum and galactooligosaccharide. Aquaculture Research, 50(3), 807-817, doi: https://doi.org/10.1111/are.13951
Immanuel, G., Sivagnanavelmurugan, M., Marudhupandi, T., Radhakrishnan, S., & Palavesam, A. (2012). The effect of fucoidan from brown seaweed Sargassum wightii on WSSV resistance and immune activity in shrimp Penaeus monodon (Fab). Fish & shellfish immunology, 32(4), 551-564, doi: https://doi.org/10.1016/j.fsi.2012.01.003
Kitikiew, S., Chen, J.-C., Putra, D. F., Lin, Y.-C., Yeh, S.-T., & Liou, C.-H. (2013). Fucoidan effectively provokes the innate immunity of white shrimp Litopenaeus vannamei and its resistance against experimental Vibrio alginolyticus infection. Fish & shellfish immunology, 34(1), 280-290, doi: https://doi.org/10.1016/j.fsi.2012.11.016
Lamela, R. E., Quintana, Y. C., Silveira Coffigny, R., Martínez, M., & Herrate, N. 2008). Effects of formalin on total haemocytes count and histopathological changes in the shrimp Litopenaeus schmitti (Pérez‐Farfante & Kensley 1997). Aquaculture Research, 39(12), 1316-1321, doi: https://doi.org/10.1111/j.1365-2109.2008.01997.x
Lara-Fiallos, M., Lara-Gordillo, P., Julián-Ricardo, M. C., Pérez-Martínez, A., & Benítes-Cortés, I. (2017). Avances en la producción de inulina. Tecnología Química, 37(2), 352-366. Recuperado el 8 de septiembre de 2019, de: http://scielo.sld.cu/pdf/rtq/v37n2/rtq16217.pdf
Laranja, J. L. Q., Amar, E. C., Ludevese-Pascual, G. L., Niu, Y., Geaga, M. J., De Schryver, P., & Bossier, P. (2017). A probiotic Bacillus strain containing amorphous poly-beta-hydroxybutyrate (PHB) stimulates the innate immune response of Penaeus monodon postlarvae. Fish & shellfish immunology, 68, 202-210, doi: https://doi.org/10.1016/j.fsi.2017.07.023
Li, J., Tan, B., Mai, K., Ai, Q., Zhang, W., Liufu, Z., & Xu, W. (2008). Immune responses and resistance against Vibrio parahaemolyticus induced by probiotic bacterium Arthrobacter XE‐7 in Pacific white shrimp, Litopenaeus vannamei. Journal of the World Aquaculture Society, 39(4), 477-489, doi: https://doi.org/10.1111/j.1749-7345.2008.00188.x
Li, Y. D., Jiang, S. G., Huang, J. H., Ma, Z. H., & Zhou, F. L. (2016). Growth and survival variations of Penaeus monodon from six breeding families. International Journal of Aquaculture, 5, 1-9 doi: https://doi.org/10.5376/ija.2015.05.0039
Li, Y., Liu, H., Dai, X., Li, J., & Ding, F. (2018). Effects of dietary inulin and mannan oligosaccharide on immune related genes expression and disease resistance of Pacific white shrimp, Litopenaeus vannamei. Fish & shellfish immunology, 76, 78-92, doi: https://doi.org/10.1016/j.fsi.2018.02.034
Liu, H., Li, Z., Tan, B., Lao, Y., Duan, Z., Sun, W., & Dong, X. (2014). Isolation of a putative probiotic strain S12 and its effect on growth performance, non-specific immunity and disease-resistance of white shrimp, Litopenaeus vannamei. Fish & shellfish immunology, 41(2), 300-307, doi: https://doi.org/10.1016/j.fsi.2014.08.028
Liu, P.-C., Lin, P.-W., Huang, C.-L., Hsu, C.-H., & Chen, J.-C. (2019). Long-term administration of diets containing Gracilaria tenuistipitata extract induce the expression of immune-related genes and increase the immune response and resistance against Vibrio harveyi in white shrimp Litopenaeus vannamei. Gene Reports, 15, 100378, doi: https://doi.org/10.1016/j.genrep.2019.100378
Luna-González, A., Almaraz-Salas, J. C., Fierro-Coronado, J. A., del Carmen Flores-Miranda, M., González-Ocampo, H. A., & Peraza-Gómez, V. (2012). The prebiotic inulin increases the phenoloxidase activity and reduces the prevalence of WSSV in whiteleg shrimp (Litopenaeus vannamei) cultured under laboratory conditions. Aquaculture, 362-363, 28-32, doi: https://doi.org/10.1016/j.aquaculture.2012.07.022
Manilal, A., Sujith, S., Selvin, J., Kiran, G. S., & Shakir, C. (2009). In vivo antiviral activity of polysaccharide from the Indian green alga, Acrosiphonia orientalis (J. Agardh): potential implication in shrimp disease management. World J. Fish Mar. Sci, 1(4), 278-282, Recuperado 15 de noviembre de 2019, de: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.528.4010&rep=rep1&type=pdf
Manoppo, H., Sukenda, S., Djokosetiyanto, D., Sukadi, M. F., & Harris, E. (2010). Nonspecific immune response and resistance of Litopenaeus vannamei fed with nucleotide, β-glucan, and protagen diets. Indonesian Aquaculture Journal, 5(1), 37-44, doi: http://dx.doi.org/10.15578/iaj.5.1.2010.37-44
Martín, L., Castillo, N. M., Arenal, A., Rodríguez, G., Franco, R., Santiesteban, D., . . . Cabrera, H. (2012). Ontogenetic changes of innate immune parameters from eggs to early postlarvae of white shrimp Litopenaeus vannamei (Crustacea: Decapoda). Aquaculture, 358-359, 234-239, doi: https://doi.org/10.1016/j.aquaculture.2012.05.005
Mastan, S. A. (2015). Use of immunostimulants in aquaculture disease management. International Journal of Fisheries and Aquatic Studies, 2(4), 277-280. Recuperado el 6 de octubre de 2019, de: http://www.fisheriesjournal.com/archives/2015/vol2issue4/PartF/2-4-59.pdf
Medina-Beltrán, V., Luna-González, A., Fierro-Coronado, J. A., Campa-Córdova, Á. I., Peraza-Gómez, V., Flores-Miranda, M. del C., & Gutíerrez Rivera, J. N. (2012). Echinacea purpurea and Uncaria tomentosa reduce the prevalence of WSSV in witheleg shrimp (Litopenaeus vannamei) cultured under laboratory conditions. Aquaculture, 358-359, 164-169, doi: https://doi.org/10.1016/j.aquaculture.2012.06.030
Mingmongkolchai, S., & Panbangred, W. (2018). Bacillus probiotics: an alternative to antibiotics for livestock production. Journal of applied microbiology, 124(6), 1334-1346, doi: https://doi.org/10.1111/jam.13690
Niu, J., Xie, S.-W., Fang, H.-H., Xie, J.-J., Guo, T.-Y., Zhang, Y.-M., . . . Liu, Y.-J. (2018). Dietary values of macroalgae Porphyra haitanensis in Litopenaeus vannamei under normal rearing and WSSV challenge conditions: Effect on growth, immune response and intestinal microbiota. Fish & shellfish immunology, 81, 135-149, doi: https://doi.org/10.1016/j.fsi.2018.06.010
Noothuan, N., Amparyup, P., & Tassanakajon, A. (2017). Melanization inhibition protein of Penaeus monodon acts as a negative regulator of the prophenoloxidase-activating system. Developmental & Comparative Immunology, 72, 97-102, doi: https://doi.org/10.1016/j.dci.2017.02.014
Omont, A., Quiroz-Guzman, E., Tovar-Ramirez, D., & Peña-Rodríguez, A. (2018). Effect of diets supplemented with different seaweed extracts on growth performance and digestive enzyme activities of juvenile white shrimp Litopenaeus vannamei. Journal of Applied Phycology, 31 1433-1442, doi: https://doi.org/10.1007/s10811-018-1628-6
Palanikumar, P., Benitta, D. J. D., Lelin, C., Thirumalaikumar, E., Michaelbabu, M., & Citarasu, T. (2018). Effect of Argemone mexicana active principles on inhibiting viral multiplication and stimulating immune system in Pacific white leg shrimp Litopenaeus vannamei against white spot syndrome virus. Fish & shellfish immunology, 75, 243-252, doi: https://doi.org/10.1016/j.fsi.2018.02.011
Panigrahi, A., Sundaram, M., Chakrapani, S., Rajasekar, S., Syama Dayal, J., & Chavali, G. (2019). Effect of carbon and nitrogen ratio (C: N) manipulation on the production performance and immunity of Pacific white shrimp Litopenaeus vannamei (Boone, 1931) in a biofloc‐based rearing system. Aquaculture Research, 50(1), 29-41, doi: https://doi.org/10.1111/are.13857
Parenrengi, A., Tampangallo, B.R., & Tenriulo, A. (2014). Analysis of immune responses on transgenic tiger shrimp (Penaeus monodon) against pathogenic bacterium Vibrio harveyi. Indonesian Aquaculture Journal, 9(1), 23-32, doi: http://dx.doi.org/10.15578/iaj.9.1.2014.23-32
Pham, K.-C., Tran, H. T. T., Van Doan, C., Le, P. H., Van Nguyen, A. T., Nguyen, H. A, . . . Phan, T. -N. (2017). Protection of Penaeus monodon against white spot syndrome by continuous oral administration of a low concentration of Bacillus subtilis spores expressing the VP 28 antigen. Letters in applied microbiology, 64(3), 184-191, doi: https://doi.org/10.1111/lam.12708
Phupet, B., Pitakpornpreecha, T., Baowubon, N., Runsaeng, P., & Utarabhand, P. (2018). Lipopolysaccharide-and β-1, 3-glucan-binding protein from Litopenaeus vannamei: Purification, cloning and contribution in shrimp defense immunity via phenoloxidase activation. Developmental & Comparative Immunology, 81, 167-179, doi: https://doi.org/10.1016/j.dci.2017.11.016
Pourmozaffar, S., Hajimoradloo, A., & Miandare, H.K. (2017). Dietary effect of apple cider vinegar and propionic acid on immune related transcriptional responses and growth performance in white shrimp, Litopenaeus vannamei. Fish & shellfish immunology, 60, 65-71, doi: http://dx.doi.org/10.1016/j.fsi.2016.11.030
Rodríguez-Ramos, T., Espinosa, G., Hernández-López, J., Gollas-Galván, T., Marrero, J., Borrell, Y., . . . Alonso, M. (2008). Effects of Echerichia coli lipopolysaccharides and dissolved ammonia on immune response in southern white shrimp Litopenaeus schmitti. Aquaculture, 274(1), 118-125, doi: http://dx.doi.org/10.1016/j.aquaculture.2007.10.049
Romano, N., Koh, C.-B., & Ng, W.-K. (2015). Dietary microencapsulated organic acids blend enhances growth, phosphorus utilization, immune response, hepatopancreatic integrity and resistance against Vibrio harveyi in white shrimp, Litopenaeus vannamei. Aquaculture, 435, 228-236, doi: https://dx.doi.org/10.1016/j.aquaculture.2014.09.037
Ruan, Y.-H., Kuo, C.-M., Lo, C.-F., Lee, M.-H., Lian, J.-L., & Hsieh, S.-L. (2010). Ferritin administration effectively enhances immunity, physiological responses, and survival of Pacific white shrimp (Litopenaeus vannamei) challenged with white spot syndrome virus. Fish & shellfish immunology, 28(4), 542-548, doi: https://doi.org/10.1016/j.fsi.2009.12.013
Sajeevan, T. P., Lowman, D. W., Williams, D. L., Selven, S., Anas, A., & Rosamma, P. (2009). Marine yeast diet confers better protection than its cell wall component (1‐3)‐β‐d‐glucan as an immunostimulant in Fenneropenaeus indicus. Aquaculture Research, 40(15), 1723-1730, doi: https://doi.org/10.1111/j.1365-2109.2009.02275.x
Sandeepa, G. M., & Ammani, K. (2017). Immunological and Antioxidant Response of Litopenaeus vannamei fed with Lactobacillus species under WSSV challenge. Current Trends in Biotechnology & Pharmacy, 11(1), 43-52. Recuperado el 6 de octubre de 2019, de: http://abap.co.in/sites/default/files/Paper-5_25.pdf
Sapcharoen, P., & Rengpipat, S. (2013). Effects of the probiotic Bacillus subtilis (BP 11 and BS 11) on the growth and survival of Pacific white shrimp, Litopenaeus vannamei. Aquaculture Nutrition, 19(6), 946-954, doi: https://doi.org/10.1111/anu.12040
Schleder, D. D., Da Rosa, J. R., Guimarães, A. M., Ramlov, F., Maraschin, M., Seiffert, W.Q., . . . Andreatta, E.R. (2017). Brown seaweeds as feed additive for white-leg shrimp: effects on thermal stress resistance, midgut microbiology, and immunology. Journal of Applied Phycology, 29(5), 2471-2477, doi: https://doi.org/10.1007/s10811-017-1129-z
Sivasankar, P., John, K.R., George, M.R., Anushalini, S., Kaviarasu, D., & Petchimuthu, M. (2017). Prophylactics in shrimp aquaculture health management: A review. Journal of Entomology and Zoology Studies, 5(4), 1049-1055. Recuperado el 4 de noviembre de 2019, de: http://www.entomoljournal.com/archives/2017/vol5issue4/PartN/5-4-20-100.pdf
Solidum, N. S., Sanares, R. C., Andrino-Felarca, K. G. S., & Corre Jr, V. L. (2016). Immune responses and resistance to vibriosis of juvenile Pacific whiteleg shrimp Penaeus vannamei fed with high dose mannan oligosaccharide and β-glucan. AACL Bioflux, 9(2), 239-249. Recuperado el 4 de noviembre de 2019, de: http://www.bioflux.com.ro/docs/2016.239-249.pdf
Tassanakajon, A., Rimphanitchayakit, V., Visetnan, S., Amparyup, P., Somboonwiwat, K., Charoensapsri, W., & Tang, S. (2018). Shrimp humoral responses against pathogens: antimicrobial peptides and melanization. Developmental & Comparative Immunology, 80, 81-93, doi: https://doi.org/10.1016/j.dci.2017.05.009
Tikito, I., & Souissi, N. (2019). Meta-analysis of Systematic Literature Review Methods. International Journal of Modern Education and Computer Science, 11(2), 17-25, doi: https://doi.org/10.5815/ijmecs.2019.02.03
Toledo, A., Frizzo, L., Signorini, M., Bossier, P., & Arenal, A. (2019). Impact of probiotics on growth performance and shrimp survival: A meta-analysis. Aquaculture, 500, 196-205, doi: https://doi.org/10.1016/j.aquaculture.2018.10.018
Tseng, D.-Y., Ho, P.-L., Huang, S.-Y., Cheng, S.-C., Shiu, Y.-L., Chiu, C.-S., & Liu, C.-H. (2009). Enhancement of immunity and disease resistance in the white shrimp, Litopenaeus vannamei, by the probiotic, Bacillus subtilis E20. Fish & shellfish immunology, 26(2), 339-344, doi: https://doi.org/10.1016/j.fsi.2008.12.003
Van Assen, M. A. L. M., van Aert, R. C. M., & Wicherts, J. M. (2015). Meta-analysis using effect size distributions of only statistically significant studies. Psychological methods, 20(3), 293-309, doi: https://doi.org/10.1037/met0000025
Vaseeharan, B., Ishwarya, R., Malaikozhundan, B., Selvaraj, D., & Chen, J.-C. (2016). Phenoloxidase an Important Constituent in Crustacean Immune System––A Review. J. Fish. Soc. Taiwan, 43(3), 217-227, doi: https://doi.org/10.29822/JFST.201609_43(3).0008
Vaseeharan, B., & Thaya, R. (2014). Medicinal plant derivatives as immunostimulants: an alternative to chemotherapeutics and antibiotics in aquaculture. Aquaculture international, 22(3), 1079-1091, doi: https://doi.org/10.1007/s10499-013-9729-3
Wang, Y., & Gu, Q. (2010). Effect of probiotics on white shrimp (Penaeus vannamei) growth performance and immune response. Marine Biology Research, 6(3), 327-332, doi: https://doi.org/10.1080/17451000903300893
Wang, Z., Sun, B., & Zhu, F. (2018). Epigallocatechin-3-gallate protects Kuruma shrimp Marsupeneaus japonicus from white spot syndrome virus and Vibrio alginolyticus. Fish & shellfish immunology, 78, 1-9, doi: https://doi.org/10.1016/j.fsi.2018.04.021
Wongsasak, U., Chaijamrus, S., Kumkhong, S., & Boonanuntanasarn, S. (2015). Effects of dietary supplementation with β-glucan and synbiotics on immune gene expression and immune parameters under ammonia stress in Pacific white shrimp. Aquaculture, 436, 179-187, doi: https://doi.org/10.1016/j.aquaculture.2014.10.028
Wu, C.-C., Chang, Y.-P., Wang, J.-J., Liu, C.-H., Wong, S.-L., Jiang, C.-M., & Hsieh, S.-L. (2015). Dietary administration of Gynura bicolor (Roxb. Willd.) DC water extract enhances immune response and survival rate against Vibrio alginolyticus and white spot syndrome virus in white shrimp Litopeneaus vannamei. Fish & shellfish immunology, 42(1), 25-33. doi: https://doi.org/10.1016/j.fsi.2014.10.016
Yang, Q.-h., Tan, B.-p., Dong, X.-h., Chi, S.-y., & Liu, H.-y. (2015). Effects of different levels of Yucca schidigera extract on the growth and nonspecific immunity of Pacific white shrimp (Litopenaeus vannamei) and on culture water quality. Aquaculture, 439, 39-44, doi: https://doi.org/10.1016/j.aquaculture.2014.11.029
Yeh, M.-S., Lai, C.-Y., Liu, C.-H., Kuo, C.-M., & Cheng, W. (2009). A second proPO present in white shrimp Litopenaeus vannamei and expression of the proPOs during a Vibrio alginolyticus injection, molt stage, and oral sodium alginate ingestion. Fish & shellfish immunology, 26(1), 49-55, doi: https://doi.org/10.1016/j.fsi.2008.10.003
Yeh, S.-T., & Chen, J.-C. (2008). Immunomodulation by carrageenans in the white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Aquaculture, 276(1-4), 22-28, doi: https://doi.org/10.1016/j.aquaculture.2008.01.034
Yeh, S.-T., Li, C.-C., Tsui, W.-C., Lin, Y.-C., & Chen, J.-C. (2010). The protective immunity of white shrimp Litopenaeus vannamei that had been immersed in the hot-water extract of Gracilaria tenuistipitata and subjected to combined stresses of Vibrio alginolyticus injection and temperature change. Fish & shellfish immunology, 29(2), 271-278, doi: https://doi.org/10.1016/j.fsi.2010.04.014
Yeh, S.-T., & Chen, J.-C. (2009). White shrimp Litopenaeus vannamei that received the hot-water extract of Gracilaria tenuistipitata showed earlier recovery in immunity after a Vibrio alginolyticus injection. Fish & shellfish immunology, 26(5), 724-730, doi: https://doi.org/10.1016/j.fsi.2009.02.025
Yogeeswaran, A., Velmurugan, S., Punitha, S. M. J., Babu, M. M., Selvaraj, T., Kumaran, T., & Citarasu, T. (2012). Protection of Penaeus monodon against white spot syndrome virus by inactivated vaccine with herbal immunostimulants. Fish & shellfish immunology, 32(6), 1058-1067, doi: https://doi.org/10.1016/j.fsi.2012.02.029
Yudiati, E., Isnansetyo, A., Murwantoko, M., Ayuningtyas, Triyanto & Handayani, C.R. (2016). Innate immune-stimulating and immune genes up-regulating activities of three types of alginate from Sargassum siliquosum in Pacific white shrimp, Litopenaeus vannamei. Fish & shellfish immunology, 54, 46-53, doi: https://doi.org/10.1016/j.fsi.2016.03.022
Zahra, A., Sukenda, S., & Wahjuningrum, D. (2017). Extract of seaweed Gracilaria verrucosa as immunostimulant to controlling white spot disease in Pacific white shrimp Litopenaeus vannamei. Jurnal Akuakultur Indonesia, 16(2), 174-183, doi: https://doi.org/10.19027/jai.16.2.174-183
Zhang, Q., Tan, B., Mai, K., Zhang, W., Ma, H., Ai, Q., . . . Liufu, Z. (2011). Dietary administration of Bacillus (B. licheniformis and B. subtilis) and isomaltooligosaccharide influences the intestinal microflora, immunological parameters and resistance against Vibrio alginolyticus in shrimp, Penaeus japonicus (Decapoda: Penaeidae). Aquaculture Research, 42(7), 943-952, doi: https://doi.org/10.1111/j.1365-2109.2010.02677.x
Zhu, M., Long, X., & Wu, S. (2018). Effects of dietary trehalose on the growth performance and nonspecific immunity of white shrimps (Litopenaeus vannamei). Fish & shellfish immunology, 78, 127-130, doi: https://doi.org/10.1016/j.fsi.2018.04.035
Zorriehzahra, M. J., Delshad, S. T., Adel, M., Tiwari, R., Karthik, K., Dhama, K., & Lazado, C.C. (2016). Probiotics as beneficial microbes in aquaculture: an update on their multiple modes of action: a review. Veterinary Quarterly, 36(4), 228-241, doi: https://doi.org/10.1080/01652176.2016.1172132