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Quercetin extracted from Sophora japonica flower improves growth performance, nutrient digestibility, cecal microbiota, organ indexes, and breast quality in broiler chicks

  • Dang, De Xin (Department of Animal Resource and Science, Dankook University) ;
  • Cho, Sungbo (School of Mongolian Medicine, Inner Mongolia University for Nationalities) ;
  • Wang, Huan (Department of Animal Resource and Science, Dankook University) ;
  • Seok, Woo Jeong (Department of Animal Resource and Science, Dankook University) ;
  • Ha, Jung Heun (Department of Food Science and Nutrition, Dankook University) ;
  • Kim, In Ho (Department of Animal Resource and Science, Dankook University)
  • Received : 2021.07.23
  • Accepted : 2021.11.29
  • Published : 2022.04.01

Abstract

Objective: The objective of this study was to evaluate the effects of supplementing quercetin extracted from Sophora japonica flower (QS) to the diet of broiler chicks on their growth performance, apparent nutrient digestibility, cecal microbiota, serum lipid profiles, relative organ weight, and breast muscle quality. Methods: A total of 1,088 1-day-old broiler chicks (mixed sex) were randomly assigned to four groups based on the initial body weight (43.00±0.29 g). The experimental period was 35 days (starter, days 0 to 7; grower, days 7 to 21; finisher, days 21 to 35). There were 17 replicate cages per treatment and 16 birds per cage. Dietary treatments consisted of birds receiving basal diet without quercetin as the control group and treatment groups consisted of birds fed basal diet supplemented with 0.2, 0.4, or 0.6 g/kg QS. Results: With the increase of the QS dosage, body weight gain during days 0 to 7 (p = 0.021), 7 to 21 (p = 0.010), and 1 to 35 (p = 0.045), feed intake during days 0 to 7 (p = 0.037) and 1 to 35 (p = 0.025), apparent dry matter digestibility (p = 0.008), apparent energy retention (p = 0.004), cecal lactic acid bacteria counts (p = 0.023), the relative weight of breast muscle (p = 0.014), pH value from breast muscle (p<0.001), and the water holding capacity of breast muscle (p = 0.012) increased linearly, whereas the drip loss from breast muscle (p = 0.001) decreased linearly. Conclusion: The addition of QS in the diet of broiler chicks had positive effects on the breast muscle yield and breast muscle quality, and improved the dry matter digestibility and energy retention by increasing cecal beneficial bacteria counts, thus improving growth performance.

Keywords

References

  1. Gonzalez-Gallego J, Garcia-Mediavilla MV, Sanchez-Campos S, Tunon MJ. Fruit polyphenols, immunity and inflammation. Br J Nutr 2010;104:S15-27. https://doi.org/10.1017/S0007114510003910
  2. Georgiev V, Ananga A, Tsolova V. Recent advances and uses of grape flavonoids as nutraceuticals. Nutrients 2014;6:391-415. https://doi.org/10.3390/nu6010391
  3. Oboh G, Ademosun AO, Ogunsuyi OB. Quercetin and its role in chronic diseases. In: Gupta S, Prasad S, Aggarwal B, editors. Drug discovery from mother nature. Springer-Cham; 2016. p. 377-87. https://doi.org/10.1007/978-3-319-41342-6_17
  4. 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
  5. Sun HY, Kim YM, Kim IH. Evaluation of Achyranthes japonica Nakai extract on growth performance, nutrient utilization, cecal microbiota, excreta noxious gas emission, and meat quality in broilers fed corn-wheat-soybean meal diet. Poult Sci 2020;99:5728-35. https://doi.org/10.1016/j.psj.2020.07.023
  6. Rupasinghe HP, Ronalds CM, Rathgeber B, Robinson RA. Absorption and tissue distribution of dietary quercetin and quercetin glycosides of apple skin in broiler chickens. J Sci Food Agric 2010;90:1172-8. https://doi.org/10.1002/jsfa.3944
  7. Boots AW, Drent M, de Boer VCJ, Bast A, Haenen GRMM. Quercetin reduces markers of oxidative stress and inflammation in sarcoidosis. Clin Nutr 2011;30:506-12. https://doi.org/10.1016/j.clnu.2011.01.010
  8. Liu HN, Liu Y, Hu LL, et al. Effects of dietary supplementation of quercetin on performance, egg quality, cecal microflora populations, and antioxidant status in laying hens. Poult Sci 2014;93:347-53. https://doi.org/10.3382/ps.2013-03225
  9. Ognik K, Cholewinska E, Czech A. The effect of adding hesperidin, diosmin, quercetin and resveratrol extracts to feed for turkey hens on selected immunological and biochemical blood indices. Ann Anim Sci 2016;16:1101-14. https://doi.org/10.1515/aoas-2016-0035
  10. Hong Z, Piao M. Effect of quercetin monoglycosides on oxidative stress and gut microbiota diversity in mice with dextran sodium sulphate-induced colitis. BioMed Res Int 2018;2018:8343052. https://doi.org/10.1155/2018/8343052
  11. Hager-Theodorides AL, Goliomytis M, Delis S, Deligeorgis S. Effects of dietary supplementation with quercetin on broiler immunological characteristics. Anim Feed Sci Technol 2014; 198:224-30. https://doi.org/10.1016/j.anifeedsci.2014.09.021
  12. Goliomytis M, Tsoureki D, Simitzis PE, Charismiadou MA, Hager-Theodorides AL, Deligeorgis SG. The effects of quercetin dietary supplementation on broiler growth performance, meat quality, and oxidative stability. Poult Sci 2014;93:1957-62. https://doi.org/10.3382/ps.2013-03585
  13. Van Krimpen MM, Torki M, Schokker D, et al. Effect of nutritional interventions with quercetin, oat hulls, β-glucans, lysozyme, and fish oil on immune competence related parameters of adult broiler. Wageningen Livest Res Rep 2016;977:50. https://doi.org/10.18174/390435
  14. Torki M, Schokker D, Duijster-Lensing M, van Krimpen MM. Effect of nutritional interventions with quercetin, oat hulls, β-glucans, lysozyme and fish oil on performance and health status related parameters of broilers chickens. Br Poult Sci 2018;59:579-90. https://doi.org/10.1080/00071668.2018.1496402
  15. Parmar AB, Patel VR, Usadadia SV, Chaudhary LM, Prajapati DR, Londhe AS. Influence of dietary inclusion of oil and Quercetin supplementation on carcass characters and meat quality attributes of broiler chickens. Int J Livest Res 2019;9:93-103. https://doi.org/10.5455/ijlr.20190629072333
  16. Yang JX, Maria TC, Zhou B, et al. Quercetin improves immune function in Arbor Acre broilers through activation of NF-κB signaling pathway. Poult Sci 2020;99:906-13. https://doi.org/10.1016/j.psj.2019.12.021
  17. Zhang S, Kim IH. Effect of quercetin (flavonoid) supplementation on growth performance, meat stability, and immunological response in broiler chickens. Livest Sci 2020;242:104286. https://doi.org/10.1016/j.livsci.2020.104286
  18. Abid AR, Areaaer AH, Hussein MA, Gatea SM, Al-Nuaimi AJ. impact of different levels of quercetin on productive performance of broiler chicken (Ross-308). AIP Conf Proc 2020;2290:020046. https://doi.org/10.1063/5.0028377
  19. Sohaib M, Butt MS, Shabbir MA, Shahid M. Lipid stability, antioxidant potential and fatty acid composition of broilers breast meat as influenced by quercetin in combination with α-tocopherol enriched diets. Lipids Health Dis 2015;14:61. https://doi.org/10.1186/s12944-015-0058-6
  20. National Research Council. Nutrient requirements of poultry. 9th ed. Washington, DC, USA: National Academy Press; 1994.
  21. Official methods of analysis of AOAC International. 17th ed. Washington, DC, USA: AOAC International; 2000.
  22. Parmar AB, Patel VR, Dangar NS. Efficiency of dietary supplementation of flavonoid (Quercetin), vegetable oil and its combination on growth traits and feed conversion in broilers. J Anim Res 2020;10:557-62. https://doi.org/10.30954/2277-940X.04.2020.12
  23. 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. https://doi.org/10.1016/j.anifeedsci.2019.03.005
  24. Wang S, Yao J, Zhou B, et al. Bacteriostatic effect of quercetin as an antibiotic alternative in vivo and its antibacterial mechanism in vitro. J Food Prot 2018;81:68-78. https://doi.org/10.4315/0362-028X.JFP-17-214
  25. Abolfathi ME, Tabeidian SA, Shahraki ADF, Tabatabaei SN, Habibian M. Comparative effects of n-hexane and methanol extracts of elecampane (Inula helenium L.) rhizome on growth performance, carcass traits, feed digestibility, intestinal antioxidant status and ileal microbiota in broiler chickens. Archiv Anim Nutr 2019;73:88-110. https://doi.org/10.1080/1745039X.2019.1581027
  26. Dos Santos AS, de Albuquerque TMR, de Brito Alves JL, de Souza EL. Effects of quercetin and resveratrol on in vitro properties related to the functionality of potentially probiotic lactobacillus strains. Front Microbiol 2019;10:2229. https://doi.org/10.3389/fmicb.2019.02229
  27. Deepika G, Rastall RA, Charalampopoulos D. Effect of food models and low-temperature storage on the adhesion of Lactobacillus rhamnosus GG to Caco-2 cells. J Agric Food Chem 2011;59:8661-6. https://doi.org/10.1021/jf2018287
  28. Cardona F, Andres-Lacueva C, Tulipani S, Tinahones FJ, Queipo-Ortuno MI. Benefits of polyphenols on gut microbiota and implications in human health. J Nutr Biochem 2013;24:1415-22. https://doi.org/10.1016/j.jnutbio.2013.05.001
  29. Etxeberria U, Arias N, Boque N, et al. Reshaping faecal gut microbiota composition by the intake of trans-resveratrol and quercetin in high-fat sucrose diet-fed rats. J Nutr Biochem 2015;26:651-60. https://doi.org/10.1016/j.jnutbio.2015.01.002
  30. Gonzales GB, Camp JV, Smagghe G, Raes K, Mackie A. Flavonoid-gastrointestinal mucus interaction and its potential role in regulating flavonoid bioavailability and mucosal biophysical properties. Food Res Int 2016;88:342-7. https://doi.org/10.1016/j.foodres.2015.12.023
  31. Porras D, Nistal E, Martinez-Florez S, et al. Protective effect of quercetin on high-fat diet-induced non-alcoholic fatty liver disease in mice is mediated by modulating intestinal microbiota imbalance and related gut-liver axis activation. Free Radic Biol Med 2017;102:188-202. https://doi.org/10.1016/j.freeradbiomed.2016.11.037
  32. Zhao L, Zhang Q, Ma W, Tian F, Shen H, Zhou M. A combination of quercetin and resveratrol reduces obesity in highfat diet-fed rats by modulation of gut microbiota. Food Funct 2017;8:4644-56. https://doi.org/10.1039/C7FO01383C
  33. Yang JX, Chaudhry MT, Yao JY, et al. Effects of phyto-oestrogen quercetin on productive performance, hormones, reproductive organs and apoptotic genes in laying hens. J Anim Physiol Anim Nutr 2018;102:505-13. https://doi.org/10.1111/jpn.12778
  34. Dong Y, Lei J, Zhang B. Effects of dietary quercetin on the antioxidative status and cecal microbiota in broiler chickens fed with oxidized oil. Poult Sci 2020;99:4892-903. https://doi.org/10.1016/j.psj.2020.06.028
  35. Musa HH, Chen GH, Cheng JH, Li BC, Mekki DM. Study on carcass characteristics of chicken breeds raised under the intensive condition. Int J Poult Sci 2006;5:530-3. https://doi.org/10.3923/ijps.2006.530.533
  36. Peng J, Li Q, Li K, et al. Quercetin improves glucose and lipid metabolism of diabetic rats: involvement of akt signaling and SIRT1. J Diabetes Res 2017;2017:Article ID 3417306. https://doi.org/10.1155/2017/3417306
  37. Rocca C, Albano L, Granieri MC, et al. Novel anti-obesity quercetin-derived Q2 prevents metabolic disorders in rats fed with high-fat diet. Vascul Pharmacol 2018;103-5:58. https://doi.org/10.1016/j.vph.2017.12.030
  38. Wang M, Xiao FL, Mao YJ, Ying LL, Zhou B, Li Y. Quercetin decreases the triglyceride content through the PPAR signalling pathway in primary hepatocytes of broiler chickens. Biotechnol Biotechnol Equip 2019;33:1000-10. https://doi.org/10.1080/13102818.2019.1635528
  39. Wang M, Wang B, Wang S, et al. Effect of quercetin on lipids metabolism through modulating the gut microbial and AMPK/PPAR signaling pathway in broilers. Front Cell Dev Biol 2021;9:616219. https://doi.org/10.3389/fcell.2021.616219
  40. Ouyang WW, Li Y, Zhao W, Wang M, Jin F. Effect of quercetin on cAMP signaling pathway in chicken adipocytes. Scientia Agricultura Sinica 2013;46:2769-76.
  41. Ying L, Chaudhry MT, Xiao F, et al. The effects and mechanism of quercetin dietary supplementation in streptozotocin-induced hyperglycemic arbor acre broilers. Oxid Med Cell Longev 2020;2020:9585047. https://doi.org/10.1155/2020/9585047
  42. Panchal SK, Poudyal H, Brown L. Quercetin ameliorates cardiovascular, hepatic, and metabolic changes in diet-induced metabolic syndrome in rats. J Nutr 2012;142:1026-32. https://doi.org/10.3945/jn.111.157263
  43. Kim CS, Kwon Y, Choe SY, et al. Quercetin reduces obesity-induced hepatosteatosis by enhancing mitochondrial oxidative metabolism via heme oxygenase-1. Nutr Metab 2015;12:33. https://doi.org/10.1186/s12986-015-0030-5
  44. Zhou Y, Mao S, Zhou M. Effect of the flavonoid baicalein as a feed additive on the growth performance, immunity, and antioxidant capacity of broiler chickens. Poult Sci 2019;98:2790-9. https://doi.org/10.3382/ps/pez071
  45. Liu X, Yoon SB, Kim IH. Growth performance, nutrient digestibility, blood profiles, excreta microbial counts, meat quality and organ weight on broilers fed with de-oiled lecithin emulsifier. Animals 2020;10:478. https://doi.org/10.3390/ani10030478
  46. Yugarani T, Tan BKH, Teh M, Das NP. Effects of polyphenolic natural products on the lipid profiles of rats fed high fat diets. Lipids 1992;27:181-6. https://doi.org/10.1007/BF02536175
  47. Egert S, Boesch-Saadatmandi C, Wolffram S, Rimbach G, Muller MJ. Serum lipid and blood pressure responses to quercetin vary in overweight patients by apolipoprotein E genotype. J Nutr 2010;140:278-84. https://doi.org/10.3945/jn.109.117655
  48. Simitzis P, Spanou D, Glastra N, Goliomytis M. Impact of dietary quercetin on laying hen performance, egg quality and yolk oxidative stability. Anim Feed Sci Technol 2018;239:27-32. https://doi.org/10.1016/j.anifeedsci.2018.03.004
  49. Jung CH, Cho I, Ahn J, Jeon TI, Ha TY. Quercetin reduces high-fat diet-induced fat accumulation in the liver by regulating lipid metabolism genes. Phytother Res 2013;27:139-43. https://doi.org/10.1002/ptr.4687
  50. Santoso U, Kususiyan K, Suharyanto S. The effect of Sauropus androgynus leaves extract plus turmeric powder on fat deposition, carcass quality and blood profile in broilers fed low protein diets. J Indones Trop Anim Agric 2015;40:121-30. https://doi.org/10.14710/jitaa.40.2.121-130
  51. Payne RL, Bidner TD, Southern LL, McMillin KW. Dietary effects of soy isoflavones on growth and carcass traits of commercial broilers. Poult Sci 2001;80:1201-7. https://doi.org/10.1093/ps/80.8.1201
  52. Chan ST, Chuang CH, Lin YC, Liao JW, Lii CK, Yeh SL. Quercetin enhances the antitumor effect of trichostatin A and suppresses muscle wasting in tumor-bearing mice. Food Funct 2018;9:871-9. https://doi.org/10.1039/C7FO01444A
  53. Kamboh AA, Zhu WY. Effect of increasing levels of bioflavonoids in broiler feed on plasma anti-oxidative potential, lipid metabolites, and fatty acid composition of meat. Poult Sci 2013;92:454-61. https://doi.org/10.3382/ps.2012-02584
  54. Liu Y, Li Y, Liu HN, et al. Effect of quercetin on performance and egg quality during the late laying period of hens. Br Poult Sci 2013;54:510-4. https://doi.org/10.1080/00071668.2013.799758
  55. Svihus B. The gizzard: function, influence of diet structure and effects on nutrient availability. World's Poult Sci J 2011;67:207-24. https://doi.org/10.1017/S0043933911000249
  56. Iftikhar H, Mahmood MS, Arshad MI, Akhtar M, Mahmood F, Rafique A. Immune system dysfunction in broiler chickens experimentally inoculated with fowl adenovirus serotype-4 associated with inclusion body hepatitis hydropericardium syndrome. Turk J Vet Anim Sci 2012;36:223-30. https://doi.org/10.3906/vet-0807-21
  57. Chouliara E, Karatapanis A, Savvaidis IN, Kontominas MG. Combined effect of oregano essential oil and modified atmosphere packaging on shelf-life extension of fresh chicken breast meat, stored at 4℃. Food Microbiol 2007;24:607-17. https://doi.org/10.1016/j.fm.2006.12.005
  58. Nissen PM, Young JF. Creatine monohydrate and glucose supplementation to slow- and fast-growing chickens changes the postmortem pH in pectoralis major. Poult Sci 2006;85:1038-44. https://doi.org/10.1093/ps/85.6.1038
  59. Otto G, Roehe R, Looft H, et al. Drip loss of case-ready meat and of premium cuts and their associations with earlier measured sample drip loss, meat quality and carcass traits in pigs. Meat Sci 2006;72:680-7. https://doi.org/10.1016/j.meatsci.2005.10.001
  60. Luciano G, Monahan FJ, Vasta V, Pennisi P, Bella M, Priolo A. Lipid and colour stability of meat from lambs fed fresh herbage or concentrate. Meat Sci 2009;82:193-9. https://doi.org/10.1016/j.meatsci.2009.01.010
  61. Li Y, Yu C, Li J, Zhang L, Gao F, Zhou G. Effects of dietary energy sources on early postmortem muscle metabolism of finishing pigs. Asia-Australas J Anim Sci 2017;30:1764-72. https://doi.org/10.5713/ajas.17.0090
  62. Jiang ZY, Jiang SQ, Lin YC, Xi PB, Yu DQ, Wu TX. Effects of soybean isoflavone on growth performance, meat quality, and antioxidation in male broilers. Poult Sci 2007;86:1356-62. https://doi.org/10.1093/ps/86.7.1356
  63. Chang Q, Zuo Z, Chow MSS, Ho WKK. Difference in absorption of the two structurally similar flavonoid glycosides, hyperoside and isoquercitrin, in rats. Eur J Pharm Biopharm 2005;59:549-55. https://doi.org/10.1016/j.ejpb.2004.10.004
  64. Kumar D, Tanwar VK. Utilization of clove powder as phyto-preservative for chicken nuggets preparation. J Stored Prod Postharvest Res 2011;2:11-4.
  65. Dang DX, Kim IH. Effects of dietary supplementation of Quillaja saponin on growth performance, nutrient digestibility, fecal gas emissions, and meat quality in finishing pigs. J Appl Anim Res 2020;48:397-401. https://doi.org/10.1080/09712119.2020.1813739
  66. Ngapo TM, Martin JF, Dransfield E. International preferences for pork appearance: I. Consumer choices. Food Qual Prefer 2007;18:26-36. https://doi.org/10.1016/j.foodqual.2005.07.001