Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Potential crosstalk of oxidative stress and immune response in poultry through phytochemicals - A review

  • Lee, M.T. (Department of Animal Science, National Chung Hsing University) ;
  • Lin, W.C. (Department of Animal Science, National Chung Hsing University) ;
  • Lee, T.T. (Department of Animal Science, National Chung Hsing University)
  • Received : 2018.07.21
  • Accepted : 2018.09.28
  • Published : 2019.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Phytochemicals which exist in various plants and fungi are non-nutritive compounds that exert numerous beneficial bioactive actions for animals. In recent years following the restriction of antibiotics, phytochemicals have been regarded as a primal selection when dealing with the challenges during the producing process in the poultry industry. The selected fast-growing broiler breed was more fragile when confronting the stressors in their growing environments. The disruption of oxidative balance that impairs the production performance in birds may somehow be linked to the immune system since oxidative stress and inflammatory damage are multi-stage processes. This review firstly discusses the individual influence of oxidative stress and inflammation on the poultry industry. Next, studies related to the application of phytochemicals or botanical compounds with the significance of their antioxidant and immunomodulatory abilities are reviewed. Furthermore, we bring up nuclear factor (erythroid-derived 2)-like 2 (Nrf2) and nuclear factor kappa B ($NF-{\kappa}B$) for they are respectively the key transcription factors involved in oxidative stress and inflammation for elucidating the underlying signal transduction pathways. Finally, by the discussion about several reports using phytochemicals to regulate these transcription factors leading to the improvement of oxidative status, heme oxygenase-1 gene is found crucial for Nrf2-mediated $NF-{\kappa}B$ inhibition.

Keywords

References

  1. Kamboh AA, Khan MA, Kaka U, et al. Effect of dietary supplementation of phytochemicals on immunity and haematology of growing broiler chickens. Ital J Anim Sci 2018;17:1038-43. https://doi.org/10.1080/1828051X.2018.1438854
  2. Lee MT, Lin WC, Yu B, Lee TT. Antioxidant capacity of phytochemicals and their potential effects on oxidative status in animals - A review. Asian-Australas J Anim Sci 2017;30:299-308. https://doi.org/10.5713/ajas.16.0438
  3. Unekwu HR, Audu JA, Makun MH, Chidi EE. Phytochemical screening and antioxidant activity of methanolic extract of selected wild edible Nigerian mushrooms. Asian Pac J Trop Dis 2014;4(Suppl 1):S153-S7. https://doi.org/10.1016/S2222-1808(14)60431-X
  4. Wandati TW, Kenji GM, Onguso JM. Phytochemicals in edible wild mushrooms from selected areas in Kenya. J Food Res 2013;2:137-44. https://doi.org/10.5539/jfr.v2n3p137
  5. Barbieri R, Coppo E, Marchese A, et al. Phytochemicals for human disease: An update on plant-derived compounds antibacterial activity. Microbiol Res 2017;196:44-68. https://doi.org/10.1016/j.micres.2016.12.003
  6. Sahin K, Orhan C, Smith MO, Sahin N. Molecular targets of dietary phytochemicals for the alleviation of heat stress in poultry. Worlds Poult Sci J 2013;69:113-24. https://doi.org/10.1017/S004393391300010X
  7. Valenzuela-Grijalva NV, Pinelli-Saavedra A, Muhlia-Almazan A, Dominguez-Diaz D, Gonzalez-Rios H. Dietary inclusion effects of phytochemicals as growth promoters in animal production. J Anim Sci Technol 2017;59:8. https://doi.org/10.1186/s40781-017-0133-9
  8. Broom LJ, Kogut MH. Inflammation: friend or foe for animal production? Poult Sci 2018;97:510-4. https://doi.org/10.3382/ps/pex314
  9. Surai PF. Antioxidant systems in poultry biology: superoxide dismutase. J Anim Res Nutr 2015;1:8.
  10. Gessner DK, Ringseis R, Eder K. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. J Anim Physiol Anim Nutr 2017;101:605-28. https://doi.org/10.1111/jpn.12579
  11. Huang CM, Lee TT. Immunomodulatory effects of phytogenics in chickens and pigs - a review. Asian-Australas J Anim Sci 2018;31:617-27. https://doi.org/10.5713/ajas.17.0657
  12. Castellani P, Balza E, Rubartelli A. Inflammation, DAMPs, tumor development, and progression: a vicious circle orchestrated by redox signaling. Antioxid Redox Signal 2014;20:1086-97. https://doi.org/10.1089/ars.2012.5164
  13. Li J, Lan T, Zhang C, et al. Reciprocal activation between IL-6/STAT3 and NOX4/Akt signalings promotes proliferation and survival of non-small cell lung cancer cells. Oncotarget 2015;6:1031-48. https://doi.org/10.18632/oncotarget.2671
  14. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 2014;20:1126-67. https://doi.org/10.1089/ars.2012.5149
  15. Wu Y, Lu J, Antony S, et al. Activation of TLR4 is required for the synergistic induction of dual oxidase 2 and dual oxidase A2 by IFN-${\gamma}$ and lipopolysaccharide in human pancreatic cancer cell lines. J Immunol 2013;190:1859-72. https://doi.org/10.4049/jimmunol.1201725
  16. Calabrese V, Cornelius C, Mancuso C, et al. Cellular stress response: A novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem Res 2008;33:2444-71. https://doi.org/10.1007/s11064-008-9775-9
  17. Latchman DS. Transcription factors: an overview. Int J Biochem Cell Biol 1997;29:1305-12. https://doi.org/10.1016/S1357-2725(97)00085-X
  18. Haddad JJ. Science review: Redox and oxygen-sensitive transcription factors in the regulation of oxidant-mediated lung injury: role for nuclear $factor-{\kappa}B$. Crit Care 2002;6:481-90. https://doi.org/10.1186/cc1839
  19. Lee MT, Lin WC, Wang SY, et al. Evaluation of potential antioxidant and anti-inflammatory effects of Antrodia cinnamomea powder and the underlying molecular mechanisms via Nrf2-and $NF-{\kappa}B$-dominated pathways in broiler chickens. Poult Sci 2018;97:2419-34. https://doi.org/10.3382/ps/pey076
  20. Selye H. A syndrome produced by diverse nocuous agents. Nature 1936;138:32. https://doi.org/10.1038/138032a0
  21. Koolhaas JM, Bartolomucci A, Buwalda B, et al. Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev 2011;35:1291-301. https://doi.org/10.1016/j.neubiorev.2011.02.003
  22. Surai PF, Fisinin VI. Vitagenes in poultry production: Part 3. Vitagene concept development. World's Poult Sci J 2016;72:793-804. https://doi.org/10.1017/S0043933916000751
  23. Mruk DD, Silvestrini B, Mo MY, Cheng CY. Antioxidant superoxide dismutase - a review: its function, regulation in the testis, and role in male fertility. Contraception 2002;65:305-11. https://doi.org/10.1016/S0010-7824(01)00320-1
  24. Deeb N, Cahaner A. Genotype-by-environment interaction with broiler genotypes differing in growth rate. 3. Growth rate and water consumption of broiler progeny from weight-selected versus nonselected parents under normal and high ambient temperatures. Poult Sci 2002;81:293-301. https://doi.org/10.1093/ps/81.3.293
  25. Lara LJ, Rostagno MH. Impact of heat stress on poultry production. Animals (Basel) 2013;3:356-69. https://doi.org/10.3390/ani3020356
  26. Yahav S, Straschnow A, Luger D, et al. Ventilation, sensible heat loss, broiler energy, and water balance under harsh environmental conditions. Poult Sci 2004;83:253-8. https://doi.org/10.1093/ps/83.2.253
  27. Ismail IB, Al-Busadah KA, El-Bahr SM. Oxidative stress biomarkers and biochemical profile in broilers chicken fed zinc bacitracin and ascorbic acid under hot climate. Am J Biochem Mol Biol 2013;3:202-14. https://doi.org/10.3923/ajbmb.2013.202.214
  28. Zhang ZW, Wang QH, Zhang JL, et al. Effects of oxidative stress on immunosuppresion induced by selenium deficiency in chickens. Biol Trace Elem Res 2012;149:352-61. https://doi.org/10.1007/s12011-012-9439-0
  29. Nie CX, Zhang WJ, Wang YG, et al. Tissue lipid metabolism and hepatic metabolomic profiling in response to supplementation of fermented cottonseed meal in the diets of broiler chickens. J Zhejiang Univ Sci B 2015;16:447-55. https://doi.org/10.1631/jzus.B1400255
  30. Sihvo HK, Immonen K, Puolanne E. Myodegeneration with fibrosis and regeneration in the pectoralis major muscle of broilers. Vet Pathol 2014;51:619-23. https://doi.org/10.1177/0300985813497488
  31. Hou DX, Luo D, Tanigawa S, et al. Prodelphinidin B-4 3'-Ogallate, a tea polyphenol, is involved in the inhibition of COX-2 and iNOS via the downregulation of TAK1-$NF-{\kappa}B$ pathway. Biochem Pharmacol 2007;74:742-51. https://doi.org/10.1016/j.bcp.2007.06.006
  32. Lee Y, Lee S, Gadde UD, Oh S, Lillehoj HS. Relievable effect of dietary Allium hookeri on LPS induced intestinal inflammation response in young broiler chickens. J Immunol 2017;198:(1 Supplement)226.3.
  33. Jiang Z, Schatzmayr G, Mohnl M, Applegate TJ. Net effect of an acute phase response-Partial alleviation with probiotic supplementation. Poult Sci 2010;89:28-33. https://doi.org/10.3382/ps.2009-00464
  34. Aziza A, Awadin W. Impact of dietary supplementation of whole flaxseed and flaxseed meal to infected broiler chickens with Eimeria tenella. Asian J Anim Vet Adv 2018;13:166-74. https://doi.org/10.3923/ajava.2018.166.174
  35. Humphrey BD, Klasing KC. Modulation of nutrient metabolism and homeostasis by the immune system. World's Poult Sci J 2004;60:90-100. https://doi.org/10.1079/WPS20037
  36. Ahmed SM, Luo L, Namani A, Wang XJ, Tang X. Nrf2 signaling pathway: pivotal roles in inflammation. Biochim Biophys Acta Mol Basis Dis 2017;1863:585-97. https://doi.org/10.1016/j.bbadis.2016.11.005
  37. Cheng G, Zhao Y, Li Y, et al. Forsythiaside attenuates lipopolysaccharide- induced inflammatory responses in the bursa of Fabricius of chickens by downregulating the $NF-{\kappa}B$ signaling pathway. Exp Ther Med 2014;7:179-84. https://doi.org/10.3892/etm.2013.1378
  38. Fontana AR, Antoniolli A, Bottini R. Grape pomace as a sustainable source of bioactive compounds: extraction, characterization, and biotechnological applications of phenolics. J Agric Food Chem 2013;61:8987-9003. https://doi.org/10.1021/jf402586f
  39. Ebrahimzadeh SK, Navidshad B, Farhoomandl P, Mirzaei Aghjehgheshlagh F. Effects of grape pomace and vitamin E on performance, antioxidant status, immune response, gut morphology and histopathological responses in broiler chickens. S Afr J Anim Sci 2018;48:324-36. https://doi.org/10.4314/sajas.v48i2.13
  40. Iqbal Z, Kamran Z, Sultan JI, et al. Replacement effect of vitamin E with grape polyphenols on antioxidant status, immune, and organs histopathological responses in broilers from 1- to 35-d age. J Appl Poult Res 2015;24:127-34. https://doi.org/10.3382/japr/pfv009
  41. Brenes A, Viveros A, Goni I, et al. Effect of grape pomace concentrate and vitamin E on digestibility of polyphenols and antioxidant activity in chickens. Poult Sci 2008;87:307-16. https://doi.org/10.3382/ps.2007-00297
  42. Yarru LP, Settivari RS, Gowda NK, et al. Effects of turmeric (Curcuma longa) on the expression of hepatic genes associated with biotransformation, antioxidant, and immune systems in broiler chicks fed aflatoxin. Poult Sci 2009;88:2620-7. https://doi.org/10.3382/ps.2009-00204
  43. Gowda NKS, Ledoux DR, Rottinghaus GE, Bermudez AJ, Chen YC. Antioxidant efficacy of curcuminoids from turmeric (Curcuma longa L.) powder in broiler chickens fed diets containing aflatoxin B1. Br J Nutr 2009;102:1629-34. https://doi.org/10.1017/S0007114509990869
  44. Gowda NKS, Ledoux DR, Rottinghaus GE, Bermudez AJ, Chen YC. Efficacy of Turmeric (Curcuma longa), containing a known level of curcumin, and a hydrated sodium calcium aluminosilicate to ameliorate the adverse effects of aflatoxin in broiler chicks. Poult Sci 2008;87:1125-30. https://doi.org/10.3382/ps.2007-00313
  45. Rajput N, Naeem M, Ali S, et al. The effect of dietary supplementation with the natural carotenoids curcumin and lutein on broiler pigmentation and immunity. Poult Sci 2013;92:1177-85. https://doi.org/10.3382/ps.2012-02853
  46. Ribeiro B, Valentao P, Baptista P, Seabra RM, Andrade PB. Phenolic compounds, organic acids profiles and antioxidative properties of beefsteak fungus (Fistulina hepatica). Food Chem Toxicol 2007;45:1805-13. https://doi.org/10.1016/j.fct.2007.03.015
  47. Kozarski M, Klaus A, Jakovljevic D, et al. Antioxidants of edible mushrooms. Molecules 2015;20:19489-525. https://doi.org/10.3390/molecules201019489
  48. Yang JH, Lin HC, Mau JL. Antioxidant properties of several commercial mushrooms. Food Chem 2002;77:229-35. https://doi.org/10.1016/S0308-8146(01)00342-9
  49. Valentao, P, Lopes G, Valente M, et al. Quantitation of nine organic acids in wild mushrooms. J Agric Food Chem 2005;53:3626-30. https://doi.org/10.1021/jf040465z
  50. Yildiz O, Can Z, Laghari AQ, Sahin H, Malkoc M. Wild edible mushrooms as a natural source of phenolics and antioxidants. J Food Chem 2015;39:148-54.
  51. Lee TT, Ciou JY, Chiang CJ, Chao YP, Yu B. Effect of Pleurotus eryngii stalk residue on the oxidative status and meat quality of broiler chickens. J Agric Food Chem 2012;60:11157-63. https://doi.org/10.1021/jf302740h
  52. Li S, Shah NP. Effects of various heat treatments on phenolic profiles and antioxidant activities of Pleurotus eryngii extracts. J Food Sci 2013;78:1122-9. https://doi.org/10.1111/1750-3841.12189
  53. Zhang A, Li X, Xing C, Yang J, Sun P. Antioxidant activity of polysaccharide extracted from Pleurotus eryngii using response surface methodology. Int J Biol Macromol 2014;65:28-32. https://doi.org/10.1016/j.ijbiomac.2014.01.013
  54. Vargas-Sancheza RD, Torrescano-Urrutiab GR, Ibarra-Ariasc FJ, et al. Effect of dietary supplementation with Pleurotus ostreatus on growth performance and meat quality of Japanese quail. Livest Sci 2018;207:117-25. https://doi.org/10.1016/j.livsci.2017.11.015
  55. Chen J, Mao D, Yong Y, et al. Hepatoprotective and hypolipidemic effects of water-soluble polysaccharidic extract of Pleurotus eryngii. Food Chem 2012;130:687-94. https://doi.org/10.1016/j.foodchem.2011.07.110
  56. Jeong YT, Jeong SC, Gu YA, Islam R, Song CH. Antitumor and immunomodulating activities of endo-biopolymers otained from a submerged culture of Pleurotus eryngii. Food Sci Biotechnol 2010;19:399-404. https://doi.org/10.1007/s10068-010-0056-4
  57. Guo FC, Kwakkel RP, Williams BA, et al. Effects of mushroom and herb polysaccharides on cellular and humoral immune responses of Eimeria tenella infected chickens. Poult Sci 2004;83:1124-32. https://doi.org/10.1093/ps/83.7.1124
  58. Li X, Jiao LL, Zhang X, et al. Anti-tumor and immunomodulating activities of proteoglycans from mycelium of Phellinus nigricans and culture medium. Int Immunopharmacol 2008;8:909-15. https://doi.org/10.1016/j.intimp.2008.02.008
  59. Ullah MI, Akhtar M, Iqbal Z, Muhammad F. Immunotherapeutic activities of mushroom derived polysaccharides in chicken. Int J Agric Biol 2014;16:269-76.
  60. Fard SH, Toghyani M, Tabeidian SA. Effect of oyster mushroom wastes on performance, immune responses and intestinal morphology of broiler chickens. Int J Recycl Org Waste Agric 2014;3:141-6. https://doi.org/10.1007/s40093-014-0076-9
  61. Gill BS, Navgeet, Kumar S. Ganoderma lucidum targeting lung cancer signaling: a review. Tumor Biol 2017;39:1010428317707437.
  62. Huang S, Mao J, Ding K, et al. Polysaccharides from Ganoderma lucidum promote cognitive function and neutral progenitor proliferation in mouse model of Alzheimer's disease. Stem Cell Reports 2017;8:84-94. https://doi.org/10.1016/j.stemcr.2016.12.007
  63. Zhang B, Yan L, Li Q, et al. Dynamic succession of substrateassociated bacterial composition and function during Ganoderma lucidum growth. Peer J 2018;6:e4975. https://doi.org/10.7717/peerj.4975
  64. Liu T, Ma Q, Zhao L, et al. Protective effects of sporoderm-broken spores of Ganderma lucidum on growth performance, antioxidant capacity and immune function of broiler chickens exposed to low level of Aflatoxin B1. Toxins (Basel) 2016;8:278. https://doi.org/10.3390/toxins8100278
  65. AL-Zuhariy MTB, Hassan WH. Hepatoprotective and immunostimulatory effect of Ganoderma, Andrographolide and Turmeric against Aflatoxicosis in broiler chickens. Int J Poult Sci 2017;16:281-7. https://doi.org/10.3923/ijps.2017.281.287
  66. Wang L, Piao XL, Kim SW, et al. Effects of Forsythia suspensa extract on growth performance, nutrient digestibility, and antioxidant activities in broiler chickens under high ambient temperature. Poult Sci 2008;87:1287-94. https://doi.org/10.3382/ps.2008-00023
  67. Zeng ZK, Li QY, Piao XS, et al. Forsythia suspensa extract attenuates corticosterone-induced growth inhibition, oxidative injury, and immune depression in broilers. Poult Sci 2014;93:1774-81. https://doi.org/10.3382/ps.2013-03772
  68. Pan L, Zhao PF, Ma XK, et al. Forsythia suspensa extract protects broilers against breast muscle oxidative injury induced by corticosterone mimicked pre-slaughter acute stress. Poult Sci 2018;97:2095-105. https://doi.org/10.3382/ps/pey046
  69. Piao XL, Jang MH, Cui J, Piao X. Lignans from the fruits of Forsythia suspensa. Bioorg Med Chem Lett 2008;18:1980-4. https://doi.org/10.1016/j.bmcl.2008.01.115
  70. Zhang HY, Piao XS, Zhang Q, et al. The effects of Forsythia suspensa extract and berberine on growth performance, immunity, antioxidant activities, and intestinal microbiota in broilers under high stocking density. Poult Sci 2013;92:1981-8. https://doi.org/10.3382/ps.2013-03081
  71. Cheng G, Zhao Y, Li H, et al. Forsythiaside attenuates lipopolysaccharide-induced inflammatory responses in the bursa of Fabricius of chickens by downregulating the $NF-{\kappa}B$ signaling pathway. Exp Ther Med 2014;7:179-84. https://doi.org/10.3892/etm.2013.1378
  72. Lee JM, Johnson JA. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 2004;37:139-43.
  73. Nguyen T, Nioi P, Pickett CB. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 2009;284:13291-5. https://doi.org/10.1074/jbc.R900010200
  74. Cardozo LF, Pedruzzi LM, Stenvinkel P, et al. Nutritional strategies to modulate inflammation and oxidative stress pathways via activation of the master antioxidant switch Nrf2. Biochimie 2013;95:1525-33. https://doi.org/10.1016/j.biochi.2013.04.012
  75. Jin W, Wang H, Yan W, et al. Disruption of Nrf2 enhances upregulation of nuclear factor-kappaB activity, proinflammatory cytokines, and intercellular adhesion molecule-1 in the brain after traumatic brain injury. Mediators Inflamm 2008;2008:725174. https://doi.org/10.1155/2008/725174
  76. Jung KA, Kwak MK. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010;15:7266-91. https://doi.org/10.3390/molecules15107266
  77. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in $NF-{\kappa}B$ signaling pathways. Nat Immunol 2011;12:695-708. https://doi.org/10.1038/ni.2065
  78. Gilmore TD. Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 2006;25:6680-4. https://doi.org/10.1038/sj.onc.1209954
  79. Aggarwal BB, Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol 2006;71:1397-421. https://doi.org/10.1016/j.bcp.2006.02.009
  80. Gupta SC, Sundaram C, Reuter S, Aggarwal BB. Inhibiting $NF-{\kappa}B$ activation by small molecules as a therapeutic strategy. Biochim Biophys Acta 2010;1799:775-87. https://doi.org/10.1016/j.bbagrm.2010.05.004
  81. Sahin K, Orhan C, Akdemir F, et al. Resveratrol protects quail hepatocytes against heat stress: modulation of the Nrf2 transcription factor and heat shock proteins. J Anim Physiol Anim Nutr 2012;96:66-74. https://doi.org/10.1111/j.1439-0396.2010.01123.x
  82. Sahin K, Orhan C, Tuzcu Z, Tuzcu M, Sahin N. Curcumin ameloriates heat stress via inhibition of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chem Toxicol 2012;50:4035-41. https://doi.org/10.1016/j.fct.2012.08.029
  83. Fialkow L, Wang Y, Downey GP. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med 2007;42:153-64. https://doi.org/10.1016/j.freeradbiomed.2006.09.030
  84. Li Y, Ma QG, Zhao LH, et al. Protective efficacy of ${\alpha}$-lipoic acid against aflatoxinB1-induced oxidative damage in the liver. Asian-Australas J Anim Sci 2014;27:907-15. https://doi.org/10.5713/ajas.2013.13588
  85. Ali S, Mann DA. Signal transduction via the NF-kappaB pathway: a targeted treatment modality for infection, inflammation and repair. Cell Biochem Funct 2004;22:67-79. https://doi.org/10.1002/cbf.1082
  86. Sahin N, Tuzcu M, Orhan C, et al. The effects of vitamin C and E supplementation on heat shock protein 70 response of ovary and brain in heat-stressed quail. Br Poult Sci 2009;50:259-65. https://doi.org/10.1080/00071660902758981
  87. Sahin K, Orhan C, Akdemir F, et al. Tomato powder supplementation activates Nrf-2 via ERK/Akt signaling pathway and attenuates heat stress-related responses in quails. Anim Feed Sci Technol 2011;165:230-7. https://doi.org/10.1016/j.anifeedsci.2011.03.003
  88. Ben-Dor A, Steiner M, Gheber L, et al. Carotenoids activate the antioxidant response element transcription system. Mol Cancer Ther 2005;4:177-86.
  89. Farombi EO, YShrotriya S, Na HK, Kim SH, Surh YJ. Curcumin attenuates dimethylnitrosamine-induced liver injury in rats through Nrf2-mediated induction of heme oxygenase-1. Food Chem Toxicol 2008;46:1279-87. https://doi.org/10.1016/j.fct.2007.09.095
  90. Rubiolo JA, Mithieux G, Vega FV. Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. Eur J Pharmacol 2008;591:66-72. https://doi.org/10.1016/j.ejphar.2008.06.067
  91. Sankar P, Telang AG, Manimaran A. Protective effect of curcumin on cypermethrin-induced oxidative stress in Wistar rats. Exp Toxicol Pathol 2012;64:487-93. https://doi.org/10.1016/j.etp.2010.11.003
  92. Grigorieva MA, Belichko OA, Shabaldin SV, Fisinin VI, Surai PF. Vitagene regulation as a new strategy to fight stresses in poultry production. Agric Biol 2017;52:716-30.
  93. Wardyn JD, Ponsford AH, Sanderson CM. Dissecting molecular cross-talk between Nrf2 and $NF-{\kappa}B$ response pathways. Biochem Soc Trans 2015;43:621-6. https://doi.org/10.1042/BST20150014
  94. de Jonge J, van Trijp HC. The impact of broiler production system practices on consumer perceptions of animal welfare. Poult Sci 2013;92:3080-95. https://doi.org/10.3382/ps.2013-03334

Cited by

  1. Antioxidant capacity of banana peel and its modulation of Nrf2-ARE associated gene expression in broiler chickens vol.18, pp.1, 2019, https://doi.org/10.1080/1828051x.2019.1667884
  2. Antioxidant Defence Systems and Oxidative Stress in Poultry Biology: An Update vol.8, pp.7, 2019, https://doi.org/10.3390/antiox8070235
  3. Nutraceutical Effect of Ganoderma lucidum Fungus on Neonatal Broilers Diet vol.18, pp.12, 2019, https://doi.org/10.3923/ijps.2019.641.647
  4. Algae-Derived Polysaccharides Promote Growth Performance by Improving Antioxidant Capacity and Intestinal Barrier Function in Broiler Chickens vol.7, 2019, https://doi.org/10.3389/fvets.2020.601336
  5. Evaluation of Waste Mushroom Compost as a Feed Supplement and Its Effects on the Fat Metabolism and Antioxidant Capacity of Broilers vol.10, pp.3, 2019, https://doi.org/10.3390/ani10030445
  6. Effects of dietary Antrodia cinnamomea fermented product supplementation on metabolism pathways of antioxidant, inflammatory, and lipid metabolism pathways-a potential crosstalk vol.33, pp.7, 2019, https://doi.org/10.5713/ajas.19.0393
  7. Effects of gallus epidermal growth factor（gEGF）from chicken embryos on growth performance, serum biochemical indices, immune function and intestinal morphology of broilers vol.20, pp.1, 2019, https://doi.org/10.1080/1828051x.2021.1976684
  8. Dietary probiotics as a strategy for improving growth performance, intestinal efficacy, immunity, and antioxidant capacity of white Pekin ducks fed with different levels of CP vol.100, pp.3, 2019, https://doi.org/10.1016/j.psj.2020.11.067
  9. Dietary squalene supplementation alleviates diquat-induced oxidative stress and liver damage of broiler chickens vol.100, pp.3, 2021, https://doi.org/10.1016/j.psj.2020.12.017
  10. Effects of dietary supplementation with Taiwanese tea byproducts and probiotics on growth performance, lipid metabolism, and the immune response in red feather native chickens vol.34, pp.3, 2019, https://doi.org/10.5713/ajas.20.0223
  11. Assessment of Intestinal Immunity and Permeability of Broilers on Partial Replacement Diets of Two-Stage Fermented Soybean Meal by Bacillus velezensis and Lactobacillus brevis ATCC 367 vol.11, pp.8, 2019, https://doi.org/10.3390/ani11082336
  12. Intestinal Microbiota, Anti-Inflammatory, and Anti-Oxidative Status of Broiler Chickens Fed Diets Containing Mushroom Waste Compost By-Products vol.11, pp.9, 2019, https://doi.org/10.3390/ani11092550