DOI QR코드

DOI QR Code

Efficacy of dietary propolis and its nanoparticles on immune-response, stress indicators, and prevention of Pseudomonas aeruginosa infection in Oreochromis niloticus

  • Fatma M. M. Korni (Department of Fish Diseases and Management, Faculty of Veterinary Medicine, Beni-Suef University) ;
  • Asmaa N. Mohammed (Department of Hygiene, Zoonoses and Epidemiology, Faculty of Veterinary Medicine, Beni-Suef University) ;
  • Usama K. Moawad (Department of Histology and Cytology, Faculty of Veterinary Medicine, Beni-Suef University) ;
  • Nour El-Houda y. Hassan (Department of Forensic medicine and toxicology, Faculty of Veterinary Medicine, Beni-Suef University) ;
  • Ahmed Farghali (Departement of Materials Science and Nanotechnology, Faculty of Postgraduate Studies for Advanced Sciences, Beni-Suef University) ;
  • Rehab K. Mahmoud (Department of Chemistry, Faculty of Science, Beni-Suef University)
  • Received : 2023.01.15
  • Accepted : 2023.04.08
  • Published : 2023.06.30

Abstract

Nanotechnology seeks to improve material effectiveness to have a greater impact on medicine. The current study was performed to determine how effective dietary propolis (PR) and propolis nanoparticles (PR-NPs) were at improving immune and anti-oxidant status, lowering cortisol levels as stress indicators, and preventing Pseudomonas aeruginosa infection in O. niloticus. Histopathology was carried out. Fish (N = 516, 25 ± 2g) were fed basal diets supplemented with 1 gm PR/kg, 2 gm PR/kg, 1 gm PR-NPs/kg, 2 gm PR-NPs/kg feed and control diet for 28 days. When compared to the control, interlukin-1, IgM, complement 5, and levels of lysozyme were dramatically higher in PR and PR-NPs fed-groups. Antioxidant enzymes and glutathione levels were higher in fish fed PR and PR-NPs, but malondialdehyde levels were lower. Cortisol levels decreased in feeding groups compared to the control. When compared to O. niloticus group fed 1 gm PR/kg and the positive control, propolis nanoparticles successfully prevented P. aeruginosa infection and the mortality rate was zero. When compared to the negative control, the positive control group's histopathological findings revealed severe histopathological changes. In low and high groups fed PR-NPS, normal structures were observed as well as high concentrations of PR after being injected with P. aeruginosa. The group that was fed low concentrations of PR after being injected with P. aeruginosa showed only minor histopathological changes. Conclusion: Dietary supplementation of PR or PR-NPs may have a beneficial effect on aquaculture, with PR-NPs having a superior effect.

Keywords

References

  1. Abdel mageid A. D.; Adel A. Shaheen; Nahed Sh. Gad, Rania M. Zahem, 2020. Ameliorative effect of propolis and nanopropolis supplementation against oxidative stress induced by Microcystis aeruginosa in Oreochromis niloticus. Egyptian Journal of Aquatic Biology & Fisheries. 24(1): 573-582. https://doi.org/10.21608/ejabf.2020.76547
  2. Abdelmagid AD, Said AM, Gawad EAA, Shalaby SA, Dawood MAO, 2022. Propolis nanoparticles relieved the impacts of glyphosate-induced oxidative stress and immunosuppression in Nile tilapia. Environ Sci Pollut Res Int. 2022 Mar; 29(13): 19778-19789. doi: 10.1007/s11356-021-17201-2. Epub 2021 Oct 31. PMID: 34718976.
  3. Abdelmagid, A. Shaheen, N. Gad andR. Zahem. 2019. Biochemical and histopathological effect of propolis and nanopropolis supplementation on alleviating dietary Microcystis aeruginosa toxicity on Nile tilapia, Oreochromis niloticus. Benha Veterinary Medical Journal, 36(2): 150-160. https://doi.org/10.21608/bvmj.2019.14704.1045
  4. Abd-El-Rhman, A. M. M. Antagonism of Aeromonas hydrophila by propolis and its effect on the performance of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol., 27(3): 454-459 (2009). doi:10.1016/j.fsi.2009.06.015.
  5. Acar U., (2018). Effects of diet supplemented with ethanolic extract of propolis on growth performance, hematological and serum biochemical parameters and disease resistance of Mozambique tilapia (Oreochromis mossambicus) against Streptococcus iniae. Aquaculture, 495, 339-344. https://doi.org/10.1016/j.aquaculture.2018.06.007
  6. Afrouzan H, Amirinia C, Mirhadi SA, Ebadollahi A, Vaseji N, Tahmasbi G., 2012. Evaluation of antimicrobial activity of propolis and nanopropolis against Staphylococcus aureus and Candida albicans. Afr J Microbiol Res. 6: 421-425. https://doi.org/10.5897/AJMR11.1183
  7. Aldemir, O. S., Z. Selamoglu, M. F. Gulhan, O. Cakir, I. Ozdemir, S. D. Dastan, and H. Dogan. Role of propolis on oxidative stress in various tissues of fish. Fresenius Envir. Bull., 23(12C): 3547-3551 (2014).
  8. Amend, D. F., 1981. Potency testing of fish vaccines. International symposium on fish Biologics: Serodiagnostics and Vaccines. Developmental biology. 49, 447-454. Aquaculture, 310, 395-400.
  9. Atle Foss, Albert K. Imsland, Bjorn Roth, Edward Schram, Sigurd O. Stefansson, 2009. Effects of chronic and periodic exposure to ammonia on growth and blood physiology in juvenile turbot (Scophthalmus maximus). Aquaculture, 296 (1-2) 45-50,ISSN 0044 8486,https://doi.org/10.1016/j.Aquaculture. 2009.07.013.
  10. Bankova, V. S., Castro, S. L., Marcucci, M. C., 2000. "Propolis: recent advances in chemistry and plant origin," Apidologie, 31(1): 3-15. https://doi.org/10.1051/apido:2000102
  11. Banskota, A.H., Tezuka, Y., Adnyana, I.K., Ishii, E., Midorikawa, K., Matsushige, K., Kadota, S. 2001. Hepatoprotective and anti-Helicobacter pyloriactivities of constituents from Brazilian propolis. Phytomedicine 8(1): 16-23. https://doi.org/10.1078/0944-7113-00004
  12. Beutler E., Duron O., Kelly M. B., 1963. Effects of ammonia stress, dietary linseed oil and Edwardsiella ictaluri challenge on juvenile darkbarbel catfish Pelteobagrus vachelli. J lab Clin. Med., 61,882.
  13. Carrasco, G.A., & Van de Kar, L.D. (2003). Neuroendocrine pharmacology of stress. European Journal of Pharmacology, 3: 272-364.
  14. De Aguiar, S.C., Zeoula, L.M., Franco, S.L. 2013. Antimicrobial activity of Brazilian propolis extracts against rumen bacteria in vitro. World J Microbiol Biotechnol 29: 1951-1959. https://doi.org/10.1007/s11274-013-1361
  15. El-Gendy, M., Gouda, A., and Shehab El-Din, M. 2015. Effect of zeolite on feeding rates and growth performance for Nile tilapia (Oreochromis niloticus). International Journal of Scientific Essa, M.M., Subramanian, P., 2006. Pongamia pinnata modulates oxidant antioxidant imbalance during hyperammonemic rats. Fund. Clin. Pharm., 3: 299-303. search in Agricultural Sciences, 2: 18-24.
  16. Elgohary, J., Abd Elatief, N. G. F., Alaa E. E., Mahmoud A. M., 2020. Pathological, bacteriological and seasonal prevalence of Aeromonas hydrophila, vibrio vulnificus, Proteus vulgaris and Pseudomonas aeruginosa; infecting Oreochromis niloticus in some Egyptian fish farms Islam. Egyptian Journal of Aquatic Biology & Fisheries 24(5): 467-482. https://doi.org/10.21608/ejabf.2020.108585
  17. El-Sayed, A.F.M., 2006. Tilapia culture. CABI. 
  18. Engler, P., Pierre Caillis, Samue Voller, Laura Labrie, 2018. Dietary Supplementation of a Mixture of Saponin-Rich Plants to Reduce Ammonia-Nitrogen Excretion in Juvenile Nile Tilapia (Oreochromis niloticus). Sustainable Food Production. 2: 6-12. https://doi.org/10.18052/www.scipress.com/SFP.2.6
  19. Enis M. Yonar , Serpil Mise Yonar, Sibel Silici., 2011. Protective effect of propolis against oxidative stress and immunosuppression induced by oxytetracycline in rainbow trout (Oncorhynchus mykiss, W.). Fish Shellfish Immunol. Aug;31(2):318-25. doi: 10.1016/j.fsi.2011.05.019. Epub 2011 May 30.
  20. FAO 2009. The State of World Fisheries and Aquaculture 2008. FAO, Rome.
  21. Fatoni A., 2008. Effect of propolis Trigona spp. Bukittinggi against several bacterial the small intestine of cattle and searches active component. Bogor (Indonesia): Bogor Agricultural University.
  22. Ferreira, D., H. C. Rocha, L. C. Kreutz, V. L. Loro, A. Marqueze, G. Koakoski, J. G. S. da Rosa, D. Gusso, T. A. Oliveira, M. S. de Abreu, and L. J. G. Barcellos. Bee products prevent agrichemical-induced oxidative damage in fish. PLoS One, 8(10): 11 (2013). doi:10.1371/journal. pone.0074499.
  23. Funakoshi-Tago M, Okamoto K, Izumi R, Tago K, Yanagisawa K, Narukawa Y, Kiuchi F, Kasahara T, Tamura H. 2015. Antiinflammatory activity of flavonoids in Nepalese propolis is attributed to inhibition of the IL-33 signaling pathway. Int Immunopharmacol. 25: 189-198. https://doi.org/10.1016/j.intimp.2015.01.012
  24. GAFRD (General Authority for Fish Resources Development) 2012. Fish statistics year book. Egyptian Ministry of Agriculture. 89 pp.
  25. Ghanawi, J., Roy, L., Davis, D.A., Saoud I.P., 2011. Effects of dietary lipid levels on growth performance of marbled spinefoot rabbitfish Siganus rivulatus https://doi.org/10.1016/j.aquaculture.2010.11.012
  26. Gul Baykalir B, Tatli Seven P, Gur S, Seven I., 2016. The effects of propolis on sperm quality, reproductive organs and testicular antioxidant status of male rats treated with cyclosporine-A. Anim Reprod. 13: 105-111. https://doi.org/10.21451/1984-3143-AR736
  27. Guo Honghui, Lin Wang, Hou Jie, Wang Lingkai, Zhang Dandan, Wu Xueyang, Li Li, Li Dapeng , 2018.The Protective Roles of Dietary Selenium Yeast and Tea Polyphenols on Growth Performance and Ammonia Tolerance of Juvenile Wuchang Bream (Megalobrama amblycephala). Frontiers in Physiology. 9: 1371.
  28. Kitabchi, A.E. (1967) Ascorbic acid in steroidogenesis. Nature, 215: 1385-1386. https://doi.org/10.1038/2151385a0
  29. Hasan, A.E.Z.; Artika, I.M.; Fahri, V.R.; Sari, N. 2012. Application of nanoparticle technology for medicine preparate (Antibiotic base on natural product, Propolis Trigona spp.). Chem. Prog. 5: 1-7.
  30. Huang S., Ling Wang , Lianmeng Liu, Yuxuan Hou, Lu Li., 2015. Nanotechnology in agriculture, livestock, and aquaculture in China. A review. Agron. Sustain. Dev. 35: 369-400 DOI 10.1007/s13593-014-0274-x.
  31. Iglewski, B.H.; Liu, P.V. and Kabat, D. (1977). Mechanism of action of Pseudomonas aeruginosa exotoxin Aiadenosine diphosphate-ribosylation of mammalian elongation factor 2 in vitro and in vivo. Infection and immunity. 15(1): 138-144. https://doi.org/10.1128/iai.15.1.138-144.1977
  32. Jesus Alberto de la Cruz-Cervantes, Flaviano Benavides-Gonzalez, Jesus Genaro Sanchez-Martinez, Maria de la Luz Vazquez-Sauceda, Antonio Joel Ruiz-Uribe, 2018. Propolis in Aquaculture: A Review of Its Potential, Reviews in Fisheries Science & Aquaculture, 26:3, 337-349, DOI: 10.1080/23308249.2018.1424798.
  33. Kanbur, M., Eraslan, G. & Silici, S., 2009. Antioxidant effect of propolis against exposure to propetamphosin rats. Ecotox Environ Safe, 72: 909-915. https://doi.org/10.1016/j.ecoenv.2007.12.018
  34. Koracevic, D., Koracevic, G., Djordjevic, V., Andrejevic, S., Cosic, V., 2001. Method for the measurement of antioxidant activity in human fluids, J. Clin. Pathol. 54(5): 356-361. https://doi.org/10.1136/jcp.54.5.356
  35. Kumar, K. M.; Mandal, B. K.; Kumar, K. S.; Reddy, P. S.; Sreedhar, B., 2013. Biobased green method to synthesise palladium and iron nanoparticles using Terminalia chebula aqueous extract. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 102: 128-133. https://doi.org/10.1016/j.saa.2012.10.015
  36. Lemarie G, Dosdat A, Coves D, Dutto G, Gasset G, Person-Le Ruyet J., 2004. Effect of chronic ammonia exposure on growth of European seabass (Dicentrarchus labrax) juveniles. Aquaculture; 229: 479e91.
  37. Lia,M. , Na Yua, Jian G. Qinc, Erchao Lia, Zhenyu Dua, Liqiao Chena, 2014.
  38. Li M, Yu N, Qin JG, Li E, Du Z, Chen L. Effects of ammonia stress, dietary linseed oil and Edwardsiella ictaluri challenge on juvenile darkbarbel catfish Pelteobagrus vachelli. Fish Shellfish Immunol. 2014 May; 38(1): 158-65. doi: 10.1016/j.fsi.2014.03.015. Epub 2014 Mar 19. PMID: 24657724.
  39. Liu, L., Gao, Z.Y., Su, X.P., Chen, X., Jiang, L., Yao, J.M. 2015. ACS Sustainable Chemistry & Engineering 3, 432. https://doi.org/10.1021/sc500848m
  40. Lowther, A., 2005. Highlights from the FAO database on aquaculture production statistics. FAO Aquaculture Newsletter, 33: 22-24.
  41. Magdy, I.; El-Hady, M.; Ahmed, H.; Elmeadawy, S. & Kenwy, A. (2014). A contribution on Pseudomonas aeruginosa infection in African catfish (Clarias gariepinus). Res. J. Phar. Biol. Chem. Sci., 5(5): 575-588.
  42. Mahmoud, R., Kotp, A. A., El-Ela, F. I. A., Farghali, A. A., Moaty, S. A., Zahran, H. Y., & Amin, R. (2021). Green synthesis of Iron Nanoparticles of Clove and Green Coffee origin with an in vivo Hepatoprotective Investigation. Journal of Environmental Chemical Engineering, 106320.
  43. Marcaida G, Felipo V, Hermenegildo C, Minana MD, Grisolia S., 1992. Acute ammonia toxicity is mediated by NMDA type of glutamate receptors. FEBS Lett. 296:67e8.
  44. Ming Li a,b , Na Yu a, Jian G. Qin c , Erchao Li a, Zhenyu Du a , Liqiao Chen a 2014. Fish& shell fish immunology 38;158-165. https://doi.org/10.1016/j.fsi.2014.03.015
  45. Moaty SA, Farghali A, Moussa M, Khaled R, 2017. Remediation of waste water by Co-Fe layered double hydroxide and its catalytic activity. J Taiwan Inst Chem Eng 71: 441-453. https://doi.org/10.1016/j.jtice.2016.12.001
  46. Mohamed S. Hassaan, Ayman G. EL Nagar, Heba S. Salim, Kevin Fitzsimmons, Ehab R. El-Haroun, 2019. Nutritional mitigation of winter thermal stress in Nile tilapia by propolis-extract: Associated indicators of nutritional status, physiological responses and transcriptional response of delta-9-desaturase gene, Aquaculture,Volume 511,2019,734256,ISSN 0044-8486, https://doi.org/10.1016/j.aquaculture.2019.734256.
  47. Mommsen, T.P., Vijayan, M.M., Moon, T.W. (1999). Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Reviews in Fish Biology and Fisheries, 9(3): 862-112.
  48. Nguyen, M., N.H., Thodesen, J. and Gjerde, B., 2007. Genetic improvement of farmed tilapias: composition and genetic parameters of a synthetic base population of Oreochromis niloticus for selective breeding. Aquaculture, 273(1), pp.1-14. https://doi.org/10.1016/j.aquaculture.2007.09.015
  49. Noor El-Deen A.E., Sohad M.D., Azza H.M. H. and Hakim A.S. 2010. Studies on Aeromonas hydrophila in Cultured Oreochromis niloticus at Kafr El Sheikh Governorate, Egypt with Reference to Histopathological Alterations in Some Vital Organs. World Journal of Fish and Marine Sciences 6(3): 233-240.
  50. Ohkawa, H., Ohishi, N., Yagi, K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction, Anal. Biochem. J. 95(2): 351-358. https://doi.org/10.1016/0003-2697(79)90738-3
  51. Olegario LS, Andrade JKS, Andrade GRS, Denadai M, Cavalcanti RL, da Silva MAAP, Narain N., 2019. Chemical characterization of four Brazilian brown propolis: An insight in tracking of its geographical location of production and quality control. Food Res Int. Sep;123,481-502. doi: 10.1016/j.foodres.2019.04.004. Epub 2019 May 13. PMID: 31284998.
  52. Omnia M. A, Nabila M.A., Nadia R.R., 2014. Biochemical effects of propolis and bee pollen in experimentally- induced hyperammonemia in rats. BENHA veterinary medical journal. 27(1): 8-24.
  53. Olczyk, P.; Wisowski, G.; KomosinskaVassev, K.; Stojko J.; Klimek K.; Olczyk, M. and Kozma, E.M. 2013: Propolis modifies collagen types I and III accumulation in the matrix of burnt tissue. Evid. Based Comp. Alternat. Med 2013: 423809.
  54. OZTURK , H., Mert PEKCAN, Meltem SIRELI, Ulvi Reha FIDANCI, 2014. Effects of propolis on in vitro rumen microbial fermentation. Ankara univ Vet Fak Derg, 57: 217-221. https://doi.org/10.1501/Vetfak_0000002428
  55. Pinghui V. Liu (1974): extracellular Toxins of Pseudomonas aeruginosa, Journal of Infectious Diseases, Volume 130,Issue Supplement Pp. S94-S99. https://doi.org/10.1093/infdis/130.Supplement.S94
  56. Prytzyk E, Dantas AP, Salom~ao K, Pereira AS, Bankova VS, De Castro SL, Aquino Neto FR., 2003. Flavonoids and trypanocidal activity of Bulgarian propolis. J Ethnopharmacol. 88: 189-193. https://doi.org/10.1016/S0378-8741(03)00210-1
  57. Quaiyum MA, Jahan R, Jahan N, Akhter T, Sadiqul IM 2014. Effects of Bamboo Charcoal Added Feed on Reduction of Ammonia and Growth of Pangasius hypophthalmus. J Aquac Res Development 5, 269. doi:10.4172/2155-9546.1000269
  58. Quaiyum MA, Jahan R, Jahan N, Akhter T, Sadiqul IM, 2014. Effects of Bamboo Charcoal Added Feed on Reduction of Ammonia and Growth of Pangasius hypophthalmus. J Aquac Res Development 5, 269. doi:10.4172/21559546.1000269.
  59. Radwan, R.R., Shaban, E.A., Kenawy, S.A. 2008. Hepatoprotective Efficiency of Combined Administration of Natural Antioxidants (Rutin and Vitamin E) and Cysteine in Hyperthermic Irradiated Rats. Egyptian J. Hospital Medicine, 32: 441-454.
  60. Rattanachaikunsopon, P., Phumkhachorn, P., 2010. Assessment of synergistic efficacy of carvacrol and cymene against Edwardsiella tarda in vitro and in Tilapia (Oreochromis niloticus). African Journal of Microbiology Research. 4: 420-425.
  61. Rossolini G.M., Mantengoli E., 2005. Treatment and control of severe infections caused by multiresistant Pseudomonas aeruginosa, Clinical Microbiology and Infection, 11(4): 17-32, ISSN 1198-743X, https://doi.org/10.1111/j.1469-0691.2005.01161.x.
  62. Sabir A., 2005. The inflammatory response on rat dental pulp following ethanolic extract of propolis (EEP) application. Maj Ked Gigi (Dent J). 38: 77-83. https://doi.org/10.20473/j.djmkg.v38.i2.p77-83
  63. Sahlan M, Dienayati D, Hamdi D, Zahra S, Hermansyah H, Chulasiri M., 2017. Encapsulation process of propolis extract by casein micelle improves sunscreen activity. Makara J Technol. 21: 1-6. https://doi.org/10.7454/mst.v21i1.3072
  64. Santacruz-Reyes AR, Chien Y-H. 2012. The potential of Yucca schidigera extract to reduce the ammonia pollution from shrimp farming. Biores Technol. 113, 311-4. doi: 10.1016/j.biortech.2012.02.132
  65. Segvic-Bubic, T., J. Boban, L. Grubisi c, Z. Trumbic, M. Radman, M. Percic, and R. Coz Rakovac. Effects of propolis enriched diet on growth performance and plasma biochemical parameters of juvenile European sea bass (Dicentrarchus labrax L.) under acute low temperature stress. Aquacult. Nutr., 19(6): 877-885 (2013). doi:10.1111/ anu.12032.
  66. Schmidt, J. O., 1997 "Chemical composition and application," in Bee Products-Properties, Applications, and Apitherapy, A. Mizrahi and Y. Lensky, Eds., pp. 15-26, New York, New York, NY, USA.
  67. Schnitzler P, Neuner A, Nolkemper S, Zundel C, Nowack H, Sensch KH., 2010. Antiviral activity and mode of action of propolis extracts and selected compounds. Phytother Res. 2 Segvic-Bubic, T.; Boban, J.; Grubisic, L.; Trumbi'c, Z.; Radman, M.; Percic, M.; Coz-Rakovac, R. Effects of propolis enriched diet on growth performance and plasma bio-chemical parameters of juvenile European sea bass (Dicentrarchus labrax L.) under acute low temperature stress. Aquac. Nutr. 2013, 19, 877-885. 4: 20-28
  68. Seven I, Tatli Seven P, Silici S., 2011. Effects of dietary Turkish propolis as alternative to antibiotic on growth and laying performances, nutrient digestibility and egg quality in laying hens under heat stress. Rev Med. 162: 186-191.
  69. Seven P. T., Ismail Seven , Selcan Karakus, Seda Iflazoglu Mutlu , Gozde Arkali , Yesim Muge Sahin, Ayben Kilislioglu 2020. Turkish Propolis and Its Nano Form Can Ameliorate the Side Effects of Cisplatin, Which Is a Widely Used Drug in the Treatment of Cancer. Plants, 9: 1075.
  70. Seven, P. T., 2008. The effects of dietary Turkish propolis and vitamin C on performance, digestibility, egg production and egg quality in laying hens under different environmental temperatures. Asian-Australas. J. Anim. Sci., 21(8): 1164-1170. doi:10.5713/ajas.2008.70605.
  71. Sforcin, J.M., Fernandes, A., Jr., Lopes, C.A., Bankova, V., Funari, S.R., 2000. Seasonal effect on Brazilian propolis antibacterial activity. J. Ethnopharmacol. 73: 243-249. https://doi.org/10.1016/S0378-8741(00)00320-2
  72. Shalaby, M. A., Mohamed k. Khames2 , Adel Fathy1, Amany A. Gharieb1 , Eman A. Abdel-Hamid 2021. The Impact of Zeolite on Ammonia Toxicity, Growth Performance and Physiological Status of the Nile Tilapia (Oreochromius niloticus). Egyptian Journal of Aquatic Biology & Fisheries, 25(1): 643-663. https://doi.org/10.21608/ejabf.2021.148524
  73. Shapour Kakoolaki, Zeliha Selamoglu Talas, Oguz Cakir, Osman Ciftci , Ilknur Ozdemir, 2013. Role of Propolis on Oxidative Stress in Fish Brain. Basic and Clinical neuroscience. 4(2): 153-158.
  74. Shin, K.W., Kim, SH., Kim, JH., 2016. Toxic effects of ammonia exposure on growth performance, hematological parameters, and plasma components in rockfish, Sebastes schlegelii, during thermal stress. Fish Aquatic Sci 19, 44. https://doi.org/10.1186/s41240-016-0044-6
  75. Shokri H, Katiraee F, Fatahinia M, Minooeianhaghighi MH. 2017. Chemical composition and antifungal potential of Iranian propolis against Candida krusei strains. J Apicult Res. 56: 581-587. https://doi.org/10.1080/00218839.2017.1371534
  76. Siddik, M.A.B., Nahar, A., Ahamed, F. and Hossain, M., 2014. Over-wintering growth performance of mixedsex and mono-sex Nile tilapia Oreochromis niloticus in the northeastern Bangladesh. Croatian Journal of Fisheries, 72(2): pp.70-76. https://doi.org/10.14798/72.2.722
  77. Talbot C. and Hole R. 1994. Fish diets and the control of eutrophication resulting from aquaculture. J Applied Ichth 10: 258-270. https://doi.org/10.1111/j.1439-0426.1994.tb00165.x
  78. Tatli Seven P, Yilmaz S, Seven I, Cerci IH, Azman MA, Yilmaz M., 2009. Effects of propolis on selected blood indicators and antioxidant enzyme activities in broilers under heat stress. Acta Vet Brno. 78: 75-83. https://doi.org/10.2754/avb200978010075
  79. Tatli Seven P, Yilmaz S, Seven I, Tuna Kelestemur G., 2012. The effects of propolis in animals exposed oxidative stress. In: Volodymyr L, editor. Oxidative stress: environmental induction and dietary antioxidants. Croatia: InTECH; p. 267-288.
  80. Thomas J, Thanigaivel S, Vijayakumar S, Acharya K, Shinge D, Seelan TSJ, Mukherjee A, Chandrasekaran N., 2014. Pathogenicity of Pseudomonas aeruginosa in Oreochromis mossambicus and treatment using lime oil nanoemulsion. Colloids Surf B: Biointerfaces 116: 372-377. https://doi.org/10.1016/j.colsurfb.2014.01.019
  81. Trenzado CE, Morales AE, Palma JM, Higuer M., 2009. Blood antioxidant defenses and hematological adjustments in crowded/uncrowded rainbow trout (Oncorhynchus mykiss) fed on diets with different levels of antioxidant vitamins and HUFA. Aquaculture. 149: 440e7.
  82. Xu, Y., Luo, L., Chen, B. and Fu, Y.,2009. "Recent development of chemical components in propolis," Frontiers of Biology in China, 4(4): 385-391. https://doi.org/10.1007/s11515-009-0053-2