Enhancing impact of dietary nano formulated quercetin on laying performance: egg quality, oxidative stability of stored eggs, intestinal immune and antioxidants related genes expression.
Antioxidant
Egg quality
Laying performance
Lipid peroxidation
Quercetin nano formulated
Storage
Journal
BMC veterinary research
ISSN: 1746-6148
Titre abrégé: BMC Vet Res
Pays: England
ID NLM: 101249759
Informations de publication
Date de publication:
29 Oct 2024
29 Oct 2024
Historique:
received:
18
04
2024
accepted:
10
10
2024
medline:
30
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
Nutritional interventions with natural antioxidants can provide a pragmatic solution for modifying hens' performance and maintaining oxidative stability of eggs during storage. Quercetin is the most abundant flavonoids with potent antioxidant and immune stimulant activities. The concept of incorporating of quercetin, as potent antioxidant and immunostimulant, into effective nano-carriers (QNPs) has promoted their bioavailability and stability thus, their effectiveness for the first time were assessed on laying hens' performance and immunity, eggs quality during storage. Four hundred 12-weeks-old Hy-line brown laying hens were distributed to four experimental groups: control group fed basal diets, and other 3 groups fed basal diets fortified with 100, 200 and 300 mg/kg QNPs for 60 weeks. Laying performance and quality of laid eggs were improved as expressed by elevated laying rate, egg mass %, eggs weight and yolk weight in QNPs200 and 300. Fortification of QNPs300 remarkably decreased layers serum total cholesterol concurrently with decreased egg yolk saturated fatty acids and cholesterol while increased polyunsaturated fatty acids. Over- 45 days storage period, QNPs enhanced phospholipids, total phenolics and flavonoids, total antioxidant activity (T-AOC) simultaneous with decreased MDA content in eggs. Furthermore, enhanced immune response was detected in both in serum and intestine of QNPs fed hens as reflected by higher lysozymes activity, IgM, IgG and phagocytic index and demotion of NO together with AvBD 6-12, IL-10, IgM and ATg 5-7-12 upregulation and downregulation of IL-1β and TNF-α especially at QNPs200 and 300. Intestinal redox balance was modified via decreasing H QNPs supplementation provides a new nutritional strategy towards increasing hen performance, fortification of eggs with natural antioxidants that prevents egg quality deterioration during storage.
Sections du résumé
BACKGROUND
BACKGROUND
Nutritional interventions with natural antioxidants can provide a pragmatic solution for modifying hens' performance and maintaining oxidative stability of eggs during storage. Quercetin is the most abundant flavonoids with potent antioxidant and immune stimulant activities. The concept of incorporating of quercetin, as potent antioxidant and immunostimulant, into effective nano-carriers (QNPs) has promoted their bioavailability and stability thus, their effectiveness for the first time were assessed on laying hens' performance and immunity, eggs quality during storage. Four hundred 12-weeks-old Hy-line brown laying hens were distributed to four experimental groups: control group fed basal diets, and other 3 groups fed basal diets fortified with 100, 200 and 300 mg/kg QNPs for 60 weeks.
RESULTS
RESULTS
Laying performance and quality of laid eggs were improved as expressed by elevated laying rate, egg mass %, eggs weight and yolk weight in QNPs200 and 300. Fortification of QNPs300 remarkably decreased layers serum total cholesterol concurrently with decreased egg yolk saturated fatty acids and cholesterol while increased polyunsaturated fatty acids. Over- 45 days storage period, QNPs enhanced phospholipids, total phenolics and flavonoids, total antioxidant activity (T-AOC) simultaneous with decreased MDA content in eggs. Furthermore, enhanced immune response was detected in both in serum and intestine of QNPs fed hens as reflected by higher lysozymes activity, IgM, IgG and phagocytic index and demotion of NO together with AvBD 6-12, IL-10, IgM and ATg 5-7-12 upregulation and downregulation of IL-1β and TNF-α especially at QNPs200 and 300. Intestinal redox balance was modified via decreasing H
CONCLUSIONS
CONCLUSIONS
QNPs supplementation provides a new nutritional strategy towards increasing hen performance, fortification of eggs with natural antioxidants that prevents egg quality deterioration during storage.
Identifiants
pubmed: 39472914
doi: 10.1186/s12917-024-04327-x
pii: 10.1186/s12917-024-04327-x
doi:
Substances chimiques
Quercetin
9IKM0I5T1E
Antioxidants
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
494Informations de copyright
© 2024. The Author(s).
Références
Meligy AM, Abd El-Hamid MI, Yonis AE, Elhaddad GY, Abdel-Raheem SM, El-Ghareeb WR, Mohamed MH, Ismail H, Ibrahim D. Liposomal encapsulated oregano, cinnamon, and clove oils enhanced the performance, bacterial metabolites antioxidant potential, and intestinal microbiota of broiler chickens. Poult Sci. 2023;102(6):102683.
pubmed: 37120892
pmcid: 10173274
doi: 10.1016/j.psj.2023.102683
Nii T, Bungo T, Isobe N, Yoshimura Y. Intestinal inflammation induced by dextran sodium sulphate causes liver inflammation and lipid metabolism disfunction in laying hens. Poult Sci. 2020;99(3):1663–77.
pubmed: 32111331
pmcid: 7587789
doi: 10.1016/j.psj.2019.11.028
Al-Khalaifah, Hanan S, Sara E Shahin, Anaam E Omar, Haiam A Mohammed, Hala I Mahmoud, and Doaa Ibrahim. "Effects of graded levels of microbial fermented or enzymatically treated dried brewer’s grains on growth, digestive and nutrient transporter genes expression and cost effectiveness in broiler chickens." BMC veterinary research 2020;16:1–15.
Li Y, Zhang Q, Feng Y, Yan S, Shi B, Guo X, Zhao Y, Guo Y. Dietary Chitosan Supplementation Improved Egg production and antioxidative function in laying breeders. Animals. 2022;12(10):1225.
pubmed: 35625071
pmcid: 9137984
doi: 10.3390/ani12101225
Ibrahim D, Moustafa A, Shahin SE, Sherief WRIA, Abdallah K, Farag MFM, Nassan MA, Ibrahim SM. Impact of fermented or enzymatically fermented dried Olive Pomace on Growth, expression of Digestive enzyme and glucose transporter genes, Oxidative Stability of Frozen Meat, and economic efficiency of broiler chickens. Front Veterinary Sci 2021;8:644325.
El-Ghareeb WR, Kishawy AT, Anter RG, Aboelabbas Gouda A, Abdelaziz WS, Alhawas B, Meligy AM, Abdel-Raheem SM, Ismail H, Ibrahim D: Novel antioxidant insights of myricetin on the performance of broiler chickens and alleviating experimental infection with Eimeria spp.: Crosstalk between oxidative stress and inflammation. Antioxidants 2023;12(5):1026.
doi: 10.3390/vetsci10010055
Ding X, Cai C, Jia R, Bai S, Zeng Q, Mao X, Xu S, Zhang K, Wang J. Dietary resveratrol improved production performance, egg quality, and intestinal health of laying hens under oxidative stress. Poult Sci. 2022;101(6):101886.
pubmed: 35526444
pmcid: 9092510
doi: 10.1016/j.psj.2022.101886
Gu Y, Chen Y, Jin R, Wang C, Wen C, Zhou Y. A comparison of intestinal integrity, digestive function, and egg quality in laying hens with different ages. Poult Sci. 2021;100(3):100949.
pubmed: 33652523
pmcid: 7936206
doi: 10.1016/j.psj.2020.12.046
Lesnierowski G, Stangierski J. What’s new in chicken egg research and technology for human health promotion?-A review. Trends Food Sci Technol. 2018;71:46–51.
doi: 10.1016/j.tifs.2017.10.022
Nimalaratne C, Schieber A, Wu J. Effects of storage and cooking on the antioxidant capacity of laying hen eggs. Food Chem. 2016;194:111–6.
pubmed: 26471533
doi: 10.1016/j.foodchem.2015.07.116
Kovacs-Nolan J, Phillips M, Mine Y. Advances in the value of eggs and egg components for human health. J Agric Food Chem. 2005;53(22):8421–31.
pubmed: 16248532
doi: 10.1021/jf050964f
Zhao Y-Y, Xiong Y, Curtis JM. Measurement of phospholipids by hydrophilic interaction liquid chromatography coupled to tandem mass spectrometry: the determination of choline containing compounds in foods. J Chromatogr A. 2011;1218(32):5470–9.
pubmed: 21737084
doi: 10.1016/j.chroma.2011.06.025
Herron KL, Fernandez ML. Are the current dietary guidelines regarding egg consumption appropriate? J Nutr. 2004;134(1):187–90.
pubmed: 14704316
doi: 10.1093/jn/134.1.187
Nimalaratne C, Wu J. Hen egg as an antioxidant food commodity: a review. Nutrients. 2015;7(10):8274–93.
pubmed: 26404361
pmcid: 4632414
doi: 10.3390/nu7105394
Kamboh A, Leghari R, Khan M, Kaka U, Naseer M, Sazili A, Malhi K. Flavonoids supplementation-An ideal approach to improve quality of poultry products. Worlds Poult Sci J. 2019;75(1):115–26.
doi: 10.1017/S0043933918000703
Gladine C, Morand C, Rock E, Bauchart D, Durand D. Plant extracts rich in polyphenols (PERP) are efficient antioxidants to prevent lipoperoxidation in plasma lipids from animals fed n – 3 PUFA supplemented diets. Anim Feed Sci Technol. 2007;136(3–4):281–96.
doi: 10.1016/j.anifeedsci.2006.09.003
Aluani D, Tzankova V, Kondeva-Burdina M, Yordanov Y, Nikolova E, Odzhakov F, Apostolov A, Markova T, Yoncheva K. Еvaluation of biocompatibility and antioxidant efficiency of chitosan-alginate nanoparticles loaded with quercetin. Int J Biol Macromol. 2017;103:771–82.
pubmed: 28536020
doi: 10.1016/j.ijbiomac.2017.05.062
Saeed M, Naveed M, Arain M, Arif M, Abd El-Hack M, Alagawany M, Siyal F, Soomro R, Sun C. Quercetin: Nutritional and beneficial effects in poultry. Worlds Poult Sci J. 2017;73(2):355–64.
doi: 10.1017/S004393391700023X
Xu Dong XD, Hu MengJiao HM, Wang YanQiu WY. Cui YuanLu CY: Antioxidant activities of quercetin and its complexes for medicinal application. 2019.
Zhang Y, Ahmad KA, Khan FU, Yan S, Ihsan AU, Ding Q. Chitosan oligosaccharides prevent doxorubicin-induced oxidative stress and cardiac apoptosis through activating p38 and JNK MAPK mediated Nrf2/ARE pathway. Chem Biol Interact. 2019;305:54–65.
pubmed: 30928397
doi: 10.1016/j.cbi.2019.03.027
Ryter SW, Choi AM. Therapeutic applications of carbon monoxide in lung disease. Curr Opin Pharmacol. 2006;6(3):257–62.
pubmed: 16580257
doi: 10.1016/j.coph.2006.03.002
Khater SI, Lotfy MM, Alandiyjany MN, Alqahtani LS, Zaglool AW, Althobaiti F, Ismail TA, Soliman MM, Saad S, Ibrahim D. Therapeutic potential of Quercetin Loaded nanoparticles: Novel insights in alleviating colitis in an experimental DSS Induced Colitis Model. Biomedicines. 2022;10(7):1654.
pubmed: 35884960
pmcid: 9313390
doi: 10.3390/biomedicines10071654
Lu Z, He X, Ma B, Zhang L, Li J, Jiang Y, Zhou G, Gao F. Dietary taurine supplementation improves breast meat quality in chronic heat-stressed broilers via activating the Nrf2 pathway and protecting mitochondria from oxidative attack. J Sci Food Agric. 2019;99(3):1066–72.
pubmed: 30014460
doi: 10.1002/jsfa.9273
Forney LA, Lenard NR, Stewart LK, Henagan TM. Dietary quercetin attenuates adipose tissue expansion and inflammation and alters adipocyte morphology in a tissue-specific manner. Int J Mol Sci. 2018;19(3):895.
pubmed: 29562620
pmcid: 5877756
doi: 10.3390/ijms19030895
Ahmed OA, Azhar AS, Tarkhan MM, Balamash KS, El-Bassossy HM. Antiglycation activities and common mechanisms mediating vasculoprotective effect of quercetin and chrysin in metabolic syndrome. Evid Based Complement Alternat Med 2020, 2020.
Xu D, Hu M-J, Wang Y-Q, Cui Y-L. Antioxidant activities of quercetin and its complexes for medicinal application. Molecules. 2019;24(6):1123.
pubmed: 30901869
pmcid: 6470739
doi: 10.3390/molecules24061123
Zhang Y, Yang Y, Tang K, Hu X, Zou G. Physicochemical characterization and antioxidant activity of quercetin-loaded chitosan nanoparticles. J Appl Polym Sci. 2008;107(2):891–7.
doi: 10.1002/app.26402
Hu B, Pan C, Sun Y, Hou Z, Ye H, Hu B, Zeng X. Optimization of fabrication parameters to produce chitosan – tripolyphosphate nanoparticles for delivery of tea catechins. J Agric Food Chem. 2008;56(16):7451–8.
pubmed: 18627163
doi: 10.1021/jf801111c
Shah S, Pal A, Kaushik V, Devi S. Preparation and characterization of venlafaxine hydrochloride-loaded chitosan nanoparticles and in vitro release of drug. J Appl Polym Sci. 2009;112(5):2876–87.
doi: 10.1002/app.29807
mHy-Line. Hy-line variety W-36 commercial management guide 2016. In.: Hy-Line International West Des Moines (IA); 2016.
AOAC. Official methods of analysis of AOAC International, Association of Official Analytical Chemists 2012.
Reddy P, Reddy V, Reddy C, Rao P. Egg weight, shape index and hatachability in Khaki Campbell duck eggs. Indian J Poult Sci 1979;14(1):26–31.
Romanoff AL, Romanoff AJ. The avian egg. John Wiley and Sons Inc New York, NY, USA 1949.
Haugh R. The Haugh unit for measuring egg quality. United States Egg Poult Magazine. 1937;43:552–5.
AOAC. Official methods of analysis of AOAC International; 2012.
Washburn K, Nix D. A rapid technique for extraction of yolk cholesterol. Poult Sci. 1974;53(3):1118–22.
pubmed: 4858295
doi: 10.3382/ps.0531118
Stahl E: thin layer chromatography A laboratory and Book publisged by springes verloag, editor. Berlin, Heidelberg, New york 1967.
Palacios LE, Wang T. Egg-yolk lipid fractionation and lecithin characterization. J Am Oil Chem Soc. 2005;82:571–8.
doi: 10.1007/s11746-005-1111-4
Restuccia D, Spizzirri UG, Puoci F, Cirillo G, Vinci G, Picci N. Determination of phospholipids in food samples. Food Reviews Int. 2012;28(1):1–46.
doi: 10.1080/87559129.2011.563398
Senevirathne M, Kim S-H, Siriwardhana N, Ha J-H, Lee K-W, Jeon Y-J. Antioxidant potential of ecklonia cavaon reactive oxygen species scavenging, metal chelating, reducing power and lipid peroxidation inhibition. Food Sci Technol Int. 2006;12(1):27–38.
doi: 10.1177/1082013206062422
Meda A, Lamien CE, Romito M, Millogo J, Nacoulma OG. Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan Honey, as well as their radical scavenging activity. Food Chem. 2005;91(3):571–7.
doi: 10.1016/j.foodchem.2004.10.006
Draper HH, Hadley M. [43] Malondialdehyde determination as index of lipid peroxidation. In: Packer L, Glazer Alexander N, edn. Methods in enzymology. Elsevier; 1990;186:1–855.
Bos H, de Souza W. Phagocytosis of yeast: a method for concurrent quantification of binding and internalization using differential interference contrast microscopy. J Immunol Methods. 2000;238(1–2):29–43.
pubmed: 10758233
doi: 10.1016/S0022-1759(00)00132-0
Ahn D, Olson D, Jo C, Love J, Jin S. Volatiles production and lipid oxidation in irradiated cooked sausage as related to packaging and storage. J Food Sci. 1999;64(2):226–9.
doi: 10.1111/j.1365-2621.1999.tb15870.x
Loreto F, Velikova V. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol. 2001;127(4):1781–7.
pubmed: 11743121
pmcid: 133581
doi: 10.1104/pp.010497
LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2’, 7’-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol. 1992;5(2):227–31.
pubmed: 1322737
doi: 10.1021/tx00026a012
Livak KJ. TD Schmittgen 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2 – ∆∆CT method. Methods 25 4 402–8.
Zhang L, Zhong G, Gu W, Yin N, Chen L, Shi S. Dietary supplementation with daidzein and Chinese herbs, independently and combined, improves laying performance, egg quality and plasma hormone levels of post-peak laying hens. Poult Sci. 2021;100(6):101115.
pubmed: 33975040
pmcid: 8131741
doi: 10.1016/j.psj.2021.101115
Abdel-Latif MA, Elbestawy AR, El-Far AH, Noreldin AE, Emam M, Baty RS, Albadrani GM, Abdel-Daim MM. Abd El-Hamid HS: Quercetin dietary supplementation advances growth performance, gut microbiota, and intestinal mrna expression genes in broiler chickens. Animals. 2021;11(8):2302.
pubmed: 34438756
pmcid: 8388376
doi: 10.3390/ani11082302
Liu H, Liu Y, Hu L, Suo Y, Zhang L, Jin F, Feng X, Teng N, Li Y. Effects of dietary supplementation of quercetin on performance, egg quality, cecal microflora populations, and antioxidant status in laying hens. Poult Sci. 2014;93(2):347–53.
pubmed: 24570456
doi: 10.3382/ps.2013-03225
Liu J, Fu Y, Zhou S, Zhao P, Zhao J, Yang Q, Wu H, Ding M, Li Y. Comparison of the effect of quercetin and daidzein on production performance, anti-oxidation, hormones, and cecal microflora in laying hens during the late laying period. Poult Sci. 2023;102(6):102674.
pubmed: 37104906
pmcid: 10160590
doi: 10.1016/j.psj.2023.102674
Amevor FK, Cui Z, Ning Z, Du X, Jin N, Shu G, Deng X, Zhu Q, Tian Y, Li D. Synergistic effects of quercetin and vitamin E on egg production, egg quality, and immunity in aging breeder hens. Poult Sci. 2021;100(12):101481.
pubmed: 34717121
pmcid: 8564671
doi: 10.1016/j.psj.2021.101481
Santini SE, Basini G, Bussolati S, Grasselli F. The phytoestrogen quercetin impairs steroidogenesis and angiogenesis in swine granulosa cells in vitro. Journal of biomedicine & biotechnology 2009, 2009:419891.
Wei Y, Liu Y, Li G, Guo Y, Zhang B. Effects of quercetin and genistein on egg quality, lipid profiles, and immunity in laying hens. J Sci Food Agric. 2024;104(1):207–14.
pubmed: 37552763
doi: 10.1002/jsfa.12910
Liu Y, Li Y, Liu H-N, Suo Y-L, Hu L-L, Feng X-A, Zhang L, Jin F. Effect of quercetin on performance and egg quality during the late laying period of hens. Br Poult Sci. 2013;54(4):510–4.
pubmed: 23906219
doi: 10.1080/00071668.2013.799758
Wang J, Omana DA, Wu J. Effect of shell eggs storage on ovomucin extraction. Food Bioprocess Technol. 2012;5:2280–4.
doi: 10.1007/s11947-011-0558-y
Obianwuna UE, Oleforuh-Okoleh VU, Wang J, Zhang H-J, Qi G-H, Qiu K, Wu S-G. Potential implications of natural antioxidants of plant origin on oxidative stability of chicken albumen during storage: a review. Antioxidants. 2022;11(4):630.
pubmed: 35453315
pmcid: 9027279
doi: 10.3390/antiox11040630
Lee J, Seo HG, Lee C-H. Effects of lotus (Nelumbo nucifera) leaf hot water extracts on the quality and stability of eggs using ultrasonication treatment during storage. Food Sci Anim Resour. 2020;40(6):1044.
pubmed: 33305287
pmcid: 7713773
doi: 10.5851/kosfa.2020.e81
Wang J, Jia R, Celi P, Ding X, Bai S, Zeng Q, Mao X, Xu S, Zhang K. Green tea polyphenol epigallocatechin-3-gallate improves the antioxidant capacity of eggs. Food Funct. 2020;11(1):534–43.
pubmed: 31845690
doi: 10.1039/C9FO02157D
Goliomytis M, Orfanou H, Petrou E, Charismiadou M, Simitzis P, Deligeorgis S. Effect of hesperidin dietary supplementation on hen performance, egg quality and yolk oxidative stability. Br Poult Sci. 2014;55(1):98–104.
pubmed: 24397432
doi: 10.1080/00071668.2013.870328
Aritanoga M, Effendi C, Herawati L. Kopi Arabika-Gayo Menurunkan MDA Dan Meningkatkan SOD Setelah Latihan Fisik Akut Submaksimal pada Pria Sedenter. Jurnal Sumberdaya Hayati. 2019;5(2):58–63.
doi: 10.29244/jsdh.5.2.58-63
Sameh S, Al-Sayed E, Labib RM, Singab AN. Genus Spondias: A phytochemical and pharmacological review. Evid Based Complement Alternat Med 2018, 2018.
Swapna LA, Pradeep K, Reddy P, Deepak K, Goyal S. Antioxidants and their implication in oral health and general health. Int J Case Rep Imag. 2014;5:258–63.
doi: 10.5348/ijcri-201555-RA-10010
Vlaicu PA, Panaite TD, Turcu RP. Enriching laying hens eggs by feeding diets with different fatty acid composition and antioxidants. Sci Rep. 2021;11(1):20707.
pubmed: 34667227
pmcid: 8526598
doi: 10.1038/s41598-021-00343-1
Gangadoo S, Stanley D, Hughes RJ, Moore RJ, Chapman J. Nanoparticles in feed: Progress and prospects in poultry research. Trends Food Sci Technol. 2016;58:115–26.
doi: 10.1016/j.tifs.2016.10.013
Liang K, Zu H, Wang X. Effect of storage on n-3 PUFA-enriched eggs. CyTA-Journal Food. 2020;18(1):102–7.
doi: 10.1080/19476337.2020.1713896
Li J, Zhou D, Li H, Luo Q, Wang X, Qin J, Xu Y, Lu Q, Tian X. Effect of purple corn extract on performance, antioxidant activity, egg quality, egg amino acid, and fatty acid profiles of laying hen. Front Veterinary Sci. 2023;9:1083842.
doi: 10.3389/fvets.2022.1083842
Shahid MS, Zhou S, Nie W, Wang L, Lv H, Yuan J. Phytogenic antioxidants prolong n-3 fatty acid-enriched Eggs’ Shelf Life by activating the Nrf-2 pathway through phosphorylation of MAPK. Foods. 2022;11(20):3158.
pubmed: 37430907
pmcid: 9601970
doi: 10.3390/foods11203158
Matumoto-Pintro PT, Murakami AE, Vital ACP, Croge C, da Silva DF, Ospina-Roja IC, Guerra AFQG. Effects of storage time and temperature on lipid oxidation of egg powders enriched with natural antioxidants. Food Chem. 2017;228:463–8.
pubmed: 28317750
doi: 10.1016/j.foodchem.2017.02.044
Gonçalves ACS, Murgas LDS, Rosa PV, Navarro RD, Costa, DVd. Teixeira EdA: Desempenho produtivo de tambacus alimentados com dietas suplementadas com vitamina E. Pesqui Agropecu Bras. 2010;45:1005–11.
doi: 10.1590/S0100-204X2010000900010
Baldissera MD, Souza CF, Parmeggiani B, Vendrusculo RG, Ribeiro LC, Muenchen DK, Zeppenfeld CC, Meinhart AD, Wagner R, Zanella R. Protective effects of diet containing rutin against trichlorfon-induced muscle bioenergetics disruption and impairment on fatty acid profile of silver catfish Rhamdia quelen. Ecotoxicol Environ Saf. 2020;205:111127.
pubmed: 32846293
doi: 10.1016/j.ecoenv.2020.111127
Wang G, Wang J-J, Chen X-L, Du L, Li F. Quercetin-loaded freeze-dried nanomicelles: improving absorption and anti-glioma efficiency in vitro and in vivo. J Control Release. 2016;235:276–90.
pubmed: 27242199
doi: 10.1016/j.jconrel.2016.05.045
Zhang B, Wang Z, Huang C, Wang D, Chang D, Shi X, Chen Y, Chen H. Positive effects of Mulberry leaf extract on egg quality, lipid metabolism, serum biochemistry, and antioxidant indices of laying hens. Front Veterinary Sci. 2022;9:1005643.
doi: 10.3389/fvets.2022.1005643
Yenice G, Kaynar Ö, Hayırlı A, Kaya A. Comparison of the effects of dietary supplementation of flavonoids on laying hen performance, egg quality and egg nutrient profile. 2017.
Li P, Gao M, Fu J, Yan S, Liu Y, Mahmood T, Lv Z, Guo Y. Dietary soya saponin improves the lipid metabolism and intestinal health of laying hens. Poult Sci. 2022;101(4):101663.
pubmed: 35172236
doi: 10.1016/j.psj.2021.101663
Li M-Y, Chen J-H, Chen C, Kang Y-N. Association between egg consumption and cholesterol concentration: a systematic review and meta-analysis of randomized controlled trials. Nutrients. 2020;12(7):1995.
pubmed: 32635569
pmcid: 7400894
doi: 10.3390/nu12071995
Ding X, Mu Y, Zhang K, Wang J, Bai S, Zeng Q, Peng H. Vitamin E improves antioxidant status but not lipid metabolism in laying hens fed a aged corn-containing diet. Anim Bioscience. 2021;34(2):276.
doi: 10.5713/ajas.19.0934
Wang M, Wang B, Wang S, Lu H, Wu H, Ding M, Ying L, Mao Y, Li Y. Effect of quercetin on lipids metabolism through modulating the gut microbial and AMPK/PPAR signaling pathway in broilers. Front Cell Dev Biology. 2021;9:616219.
doi: 10.3389/fcell.2021.616219
Zhao L, Zhang X, Cao F, Sun D, Wang T, Wang G. Effect of dietary supplementation with fermented Ginkgo-leaves on performance, egg quality, lipid metabolism and egg-yolk fatty acids composition in laying hens. Livest Sci. 2013;155(1):77–85.
doi: 10.1016/j.livsci.2013.03.024
Rasouli E, Jahanian R. Comparative effects of genistein and antibiotics on performance, meat oxidative stability, jejunal morphology, and ileal microbial community in broiler chicks. Anim Feed Sci Technol. 2019;256:114153.
doi: 10.1016/j.anifeedsci.2019.03.005
Chowdhury S, Mandal GP, Patra AK, Kumar P, Samanta I, Pradhan S, Samanta AK. Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Anim Feed Sci Technol. 2018;236:39–47.
doi: 10.1016/j.anifeedsci.2017.12.003
SATOH T, GOTO M, IGARASHI K. Effects of protein isolates from radish and spinach leaves on serum lipids levels in rats. J Nutri Sci Vitaminol. 1993;39(6):627–33.
doi: 10.3177/jnsv.39.627
Eseberri I, Miranda J, Lasa A, Churruca I, Portillo MP. Doses of quercetin in the range of serum concentrations exert delipidating effects in 3T3-L1 preadipocytes by acting on different stages of adipogenesis, but not in mature adipocytes. Oxid Med Cell Longev 2015, 2015.
Gentile D, Fornai M, Pellegrini C, Colucci R, Blandizzi C, Antonioli L. Dietary flavonoids as a potential intervention to improve redox balance in obesity and related co-morbidities: a review. Nutr Res Rev. 2018;31(2):239–47.
pubmed: 29871706
doi: 10.1017/S0954422418000082
Feng J, Li Z, Ma H, Yue Y, Hao K, Li J, Xiang Y, Min Y. Quercetin alleviates intestinal inflammation and improves intestinal functions via modulating gut microbiota composition in LPS-challenged laying hens. Poult Sci. 2023;102(3):102433.
pubmed: 36587451
doi: 10.1016/j.psj.2022.102433
Abdel-Latif MA, El-Far AH, Elbestawy AR, Ghanem R, Mousa SA, Abd El-Hamid HS. Exogenous dietary lysozyme improves the growth performance and gut microbiota in broiler chickens targeting the antioxidant and non-specific immunity mRNA expression. PLoS ONE. 2017;12(10):e0185153.
pubmed: 29059196
pmcid: 5653193
doi: 10.1371/journal.pone.0185153
İskender H, Yenice G, Dokumacioglu E, Kaynar O, Hayirli A, Kaya A. The effects of dietary flavonoid supplementation on the antioxidant status of laying hens. Brazilian J Poult Sci. 2016;18:663–8.
doi: 10.1590/1806-9061-2016-0356
Zhou N, Tian Y, Liu W, Tu B, Xu W, Gu T, Zou K, Lu L. Protective effects of resveratrol and apigenin dietary supplementation on serum antioxidative parameters and mRNAs expression in the small intestines of diquat-challenged pullets. Front Veterinary Sci. 2022;9:850769.
doi: 10.3389/fvets.2022.850769
Baksi R, Singh DP, Borse SP, Rana R, Sharma V, Nivsarkar M. In vitro and in vivo anticancer efficacy potential of Quercetin loaded polymeric nanoparticles. Biomed Pharmacother. 2018;106:1513–26.
pubmed: 30119227
doi: 10.1016/j.biopha.2018.07.106
Jiang N, Li Y, Shu T, Wang J. Cytokines and inflammation in adipogenesis: an updated review. Front Med. 2019;13:314–29.
pubmed: 30066061
doi: 10.1007/s11684-018-0625-0
Moraes PO, Andretta I, Cardinal KM, Ceron M, Vilella L, Borille R, Frazzon AP, Frazzon J, Santin E, Ribeiro AML. Effect of functional oils on the immune response of broilers challenged with Eimeria spp. Animal. 2019;13(10):2190–8.
pubmed: 30955505
doi: 10.1017/S1751731119000600
Zhao B-C, Lin H-C, Yang D, Ye X, Li Z-G. Disulfide bridges in defensins. Curr Top Med Chem. 2016;16(2):206–19.
doi: 10.2174/1568026615666150701115911
Yang J, Chaudhry M, Yao J, Wang S, Zhou B, Wang M, Han C, You Y, Li Y. Effects of phyto-oestrogen quercetin on productive performance, hormones, reproductive organs and apoptotic genes in laying hens. J Anim Physiol Anim Nutr (Berl). 2018;102(2):505–13.
pubmed: 28986927
doi: 10.1111/jpn.12778
Nunes C, Ferreira E, Freitas V, Almeida L, Barbosa RM, Laranjinha J. Intestinal anti-inflammatory activity of red wine extract: unveiling the mechanisms in colonic epithelial cells. Food Funct. 2013;4(3):373–83.
pubmed: 23233037
doi: 10.1039/C2FO30233K
Abdel-Moneim A-ME, Shehata AM, Alzahrani SO, Shafi ME, Mesalam NM, Taha AE, Swelum AA, Arif M, Fayyaz M, Abd El-Hack ME. The role of polyphenols in poultry nutrition. J Anim Physiol Anim Nutr. 2020;104(6):1851–66.
doi: 10.1111/jpn.13455
Chaudhari N, Talwar P, Parimisetty A, Lefebvre d’Hellencourt C, Ravanan P. A molecular web: endoplasmic reticulum stress, inflammation, and oxidative stress. Front Cell Neurosci. 2014;8:213.
pubmed: 25120434
pmcid: 4114208
doi: 10.3389/fncel.2014.00213
Dridi S, Buyse J, Decuypere E, Taouis M. Potential role of leptin in increase of fatty acid synthase gene expression in chicken liver. Domest Anim Endocrinol. 2005;29(4):646–60.
pubmed: 15941644
doi: 10.1016/j.domaniend.2005.05.002
Kaushik S, Arias E, Kwon H, Lopez NM, Athonvarangkul D, Sahu S, Schwartz GJ, Pessin JE, Singh R. Loss of autophagy in hypothalamic POMC neurons impairs lipolysis. EMBO Rep. 2012;13(3):258–65.
pubmed: 22249165
pmcid: 3323137
doi: 10.1038/embor.2011.260
Rabinowitz JD, White E. Autophagy and metabolism. Science. 2010;330(6009):1344–8.
pubmed: 21127245
pmcid: 3010857
doi: 10.1126/science.1193497
Ward C, Martinez-Lopez N, Otten EG, Carroll B, Maetzel D, Singh R, Sarkar S, Korolchuk VI. Autophagy, lipophagy and lysosomal lipid storage disorders. Biochim et Biophys Acta (BBA)-Molecular Cell Biology Lipids. 2016;1861(4):269–84.
Xiao J, Zhang B, Yin S, Xie S, Huang K, Wang J, Yang W, Liu H, Zhang G, Liu X. Quercetin induces autophagy-associated death in HL-60 cells through CaMKKβ/AMPK/mTOR signal pathway: Quercetin induces autophagic cell death in AML. Acta Biochim Biophys Sin. 2022;54(9):1244.
pubmed: 36148953
pmcid: 9827794
Kim J, Muhammad N, Jhun BH, Yoo J-W. Probiotic delivery systems: a brief overview. J Pharm Invest. 2016;46(4):377–86.
doi: 10.1007/s40005-016-0259-7
Ahmadian E, Eftekhari A, Kavetskyy T, Khosroushahi AY, Turksoy VA, Khalilov R. Effects of quercetin loaded nanostructured lipid carriers on the paraquat-induced toxicity in human lymphocytes. Pestic Biochem Physiol. 2020;167:104586.
pubmed: 32527420
doi: 10.1016/j.pestbp.2020.104586
Council NR. Nutrient requirements of poultry: 1994. National Academies; 1994.