Animal Bioscience

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

DOI QR Code

The effects of plant extracts on lipid metabolism of chickens - A review

  • Xuedong Ding (National Center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Ilias Giannenas (Department of Veterinary Medicine, Aristotle University of Thessaloniki) ;
  • Ioannis Skoufos (Department of Agriculture, University of Ioannina) ;
  • Jing Wang (National Center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Weiyun Zhu (National Center for International Research on Animal Gut Nutrition, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology National Experimental Teaching Demonstration Center of Animal Science, College of Animal Science and Technology, Nanjing Agricultural University)
  • Received : 2022.07.12
  • Accepted : 2022.09.25
  • Published : 2023.05.01
Download PDF
⟨ Previous Next ⟩

Abstract

The fat deposition is an important factor affecting chicken meat quality, which is closely related to lipid metabolism of chickens. Therefore, it is important to regulate the lipid metabolism of chickens to improve the chicken meat quality. Plant extracts have special regulatory effects on animal's growth and health and have been widely used in chicken breeding. Some plant extracts have been reported to have functions of changing the fatty acid composition, reducing abdominal fat percentage, and enhancing the intramuscular fat content of chickens by improving the antioxidant capacity, regulating the expression of genes, enzymes, and signaling pathways related to lipid metabolism, modulating intestinal microbiota, affecting hormones level, and regulating DNA methylation. This paper reviewed the application and mechanism of plant extracts on regulating lipid metabolism of chickens to provide a reference for the further application of plant extracts in chicken breeding.

Keywords

Acknowledgement

This study was supported by the National Key R&D Program of China (2017YFE0135200).

References

  1. Ordaz-Trinidad N, Dorantes-Alvarez L, Salas-Benito J. Patents on phytochemicals: methodologies of extraction, application in food and pharmaceutical industry. Recent Pat Biotechnol 2015;9:158-67. https://doi.org/10.2174/1872208310999160317145333
  2. Righi F, Pitino R, Manuelian CL, et al. Plant feed additives as natural alternatives to the use of synthetic antioxidant vitamins on poultry performances, health, and oxidative status: a review of the literature in the last 20 years. Antioxidants 2021;10:659. https://doi.org/10.3390/antiox10050659
  3. Bosco AD, Mugnai C, Amato MG, Piottoli L, Cartoni A, Castellini C. Effect of slaughtering age in different commercial chicken genotypes reared according to the organic system: 1. Welfare, carcass and meat traits. Ital J Anim Sci 2014;13:3308. https://doi.org/10.4081/ijas.2014.3308
  4. Mahiza MIN, Lokman HI, Ibitoye EB. Fatty acid profile in the breast and thigh muscles of the slow- and fast-growing birds under the same management system. Trop Anim Health Prod 2021;53:409. https://doi.org/10.1007/s11250-021-02777-1
  5. Devatkal SK, Naveena BM, Kotaiah T. Quality, composition, and consumer evaluation of meat from slow-growing broilers relative to commercial broilers. Poult Sci 2019;98:6177-86. https://doi.org/10.3382/ps/pez344
  6. Choct M, Naylor A, Oddy H, Nolan J. Increasing efficiency of lean tissue deposition in broiler chickens. Rural Industries Research and Development Corporation; 2000. RIRDC Publication No 98/123.
  7. Demeure O, Duclos MJ, Bacciu N, et al. Genome-wide interval mapping using SNPs identifies new QTL for growth, body composition and several physiological variables in an F2 intercross between fat and lean chicken lines. Genet Sel Evol 2013;45:36. https://doi.org/10.1186/1297-9686-45-36
  8. 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
  9. Hager-Theodorides AL, Massouras T, Simitzis PE, et al. Hesperidin and naringin improve broiler meat fatty acid profile and modulate the expression of genes involved in fatty acid β-oxidation and antioxidant defense in a dose dependent manner. Foods 2021;10:739. https://doi.org/10.3390/foods10040739
  10. Wan X, Yang Z, Ji H, et al. Effects of lycopene on abdominal fat deposition, serum lipids levels and hepatic lipid metabolismrelated enzymes in broiler chickens. Anim Biosci 2021;34:385-92. https://doi.org/10.5713/ajas.20.0432
  11. Xie Z, Shen G, Wang Y, Wu C. Curcumin supplementation regulates lipid metabolism in broiler chickens. Poult Sci 2019;98:422-9. https://doi.org/10.3382/ps/pey315
  12. Uwineza PA, Waskiewicz A. Recent advances in supercritical fluid extraction of natural bioactive compounds from natural plant materials. Molecules 2020;25:3847. https://doi.org/10.3390/molecules25173847
  13. Lefebvre T, Destandau E, Lesellier E. Selective extraction of bioactive compounds from plants using recent extraction techniques: a review. J Chromatogr A 2021;1635:461770. https://doi.org/10.1016/j.chroma.2020.461770
  14. Lv Z, Xing K, Li G, Liu D, Guo Y. Dietary genistein alleviates lipid metabolism disorder and inflammatory response in laying hens with fatty liver syndrome. Front Physiol 2018;9:1493. https://doi.org/10.3389/fphys.2018.01493
  15. Stochmal A, Simonet AM, Macias FA, Oleszek W. Alfalfa (Medicago sativa L.) flavonoids. 2. tricin and chrysoeriol glycosides from aerial parts. J Agric Food Chem 200;49:5310-4. https://doi.org/10.1021/jf010600x
  16. Ouyang K, Xu M, Jiang Y, Wang W. Effects of alfalfa flavonoids on broiler performance, meat quality, and gene expression. Can J Anim Sci 2016;96:332-41. https://doi.org/10.1139/CJAS-2015-0132
  17. Graham HN. Green tea composition, consumption, and polyphenol chemistry. Prev Med 1992;21:334-50. https://doi.org/10.1016/0091-7435(92)90041-F
  18. Huang J, Zhang Y, Zhou Y, et al. Green tea polyphenols alleviate obesity in broiler chickens through the regulation of lipidmetabolism-related genes and transcription factor expression. J Agric Food Chem 2013;61:8565-72. https://doi.org/10.1021/jf402004x
  19. Shi J, Yu J, Pohorly JE, Kakuda Y. Polyphenolics in grape seeds-biochemistry and functionality. J Med Food 2003;6:291-9. https://doi.org/10.1089/109662003772519831
  20. Farahat MH, Abdallah FM, Ali HA, Hernandez-Santana A. Effect of dietary supplementation of grape seed extract on the growth performance, lipid profile, antioxidant status and immune response of broiler chickens. Animal 2017;11:771-7. https://doi.org/10.1017/S1751731116002251
  21. Gil MI, Tomas-Barberan FA, Hess-Pierce B, Holcroft DM, Kader AA. Antioxidant activity of pomegranate juice and its relationship with phenolic composition and processing. J Agric Food Chem 2000;48:4581-9. https://doi.org/10.1021/jf000404a
  22. Shen M, Xie Z, Jia M, et al. Effect of bamboo leaf extract on antioxidant status and cholesterol metabolism in broiler chickens. Animals 2019;9:699. https://doi.org/10.3390/ani9090699
  23. Shen MM, Zhang LL, Chen YN, et al. Effects of bamboo leaf extract on growth performance, meat quality, and meat oxidative stability in broiler chickens. Poult Sci 2019;98:6787-96. https://doi.org/10.3382/ps/pez404
  24. Shehzad A, Wahid F, Lee YS. Curcumin in cancer chemoprevention: molecular targets, pharmacokinetics, bioavailability, and clinical trials. Arch Pharm 2010;343:489-99. https://doi.org/10.1002/ardp.200900319
  25. Jia-li L, De-ming L, Dan W, Hong Z, Xin-rong D, Jian-hua T. Analyses of the contents of total flavonoids and hesperidin in citrus peel. Hunan Agric Sci 2020;11:58-62. https://doi.org/10.16498/j.cnki.hnnykx.2020.011.016
  26. Zuorro A, Fidaleo M, Lavecchia R. Enzyme-assisted lycopene extraction from tomato processing waste. Enzyme Microb Technol 2011;49:567-73. https://doi.org/10.1016/j.enzmictec.2011.04.020
  27. Yusong Z, Cangxue L. Exploitation of sea bucthorn resource and extraction of flavone. Food Res Dev 2005;3:46-7. https://doi.org/10.3969/j.issn.1005-6521.2005.03.016
  28. Ma JS, Chang WH, Liu GH, et al. Effects of flavones of sea buckthorn fruits on growth performance, carcass quality, fat deposition and lipometabolism for broilers. Poult Sci 2015;94:2641-9. https://doi.org/10.3382/ps/pev250
  29. Fernandez C, Lopez-Saez A, Gallego L, de la Fuente JM. Effect of source of betaine on growth performance and carcass traits in lambs. Anim Feed Sci Technol 2000;86:71-82. https://doi.org/10.1016/S0377-8401(00)00150-4
  30. Leng Z, Fu Q, Yang X, Ding L, Wen C, Zhou Y. Increased fatty acid β-oxidation as a possible mechanism for fat-reducing effect of betaine in broilers. Anim Sci J 2016;87:1005-10. https://doi.org/10.1111/asj.12524
  31. Ruiqi F, Guiping Z, Ranran L, Maiqing Z, Jilan C, Jie W. Research on body fat distribution and deposition pattern of beijing-you chickens. Chinese J Anim Nutr 2013;25:1465-72. https://doi.org/10.3969/j.issn.1006-267x
  32. Ghasemi HA, Shivazad M, Mirzapour Rezaei SS, Karimi Torshizi MA. Effect of synbiotic supplementation and dietary fat sources on broiler performance, serum lipids, muscle fatty acid profile and meat quality. Br Poult Sci 2016;57:71-6. https://doi.org/10.1080/00071668.2015.1098766
  33. Zhao GP, Cui HX, Liu RR, Zheng MQ, Chen JL, Wen J. Comparison of breast muscle meat quality in 2 broiler breeds. Poult Sci 2011;90:2355-9. https://doi.org/10.3382/ps.2011-01432
  34. Wiktorowska-Owczarek A, Berezinska M, Nowak JZ. PUFAs: structures, metabolism and functions. Adv Clin Exp Med 2015;24:931-41. https://doi.org/10.17219/acem/31243
  35. Ahmadipour B, Hassanpour H, Khajali F. Evaluation of hepatic lipogenesis and antioxidant status of broiler chickens fed mountain celery. BMC Vet Res 2018;14:234. https://doi.org/10.1186/s12917-018-1561-6
  36. 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
  37. Kamboh AA, Zhu WY. Individual and combined effects of genistein and hesperidin supplementation on meat quality in meat-type broiler chickens. J Sci Food Agric 2013;93:3362-7. https://doi.org/10.1002/jsfa.6185
  38. Zhao JS, Deng W, Liu HW. Effects of chlorogenic acid-enriched extract from Eucommia ulmoides leaf on performance, meat quality, oxidative stability, and fatty acid profile of meat in heat-stressed broilers. Poult Sci 2019;98:3040-9. https://doi.org/10.3382/ps/pez081
  39. Lv Z, Fan H, Song B, Li G, Liu D, Guo Y. Supplementing genistein for breeder hens alters the fatty acid metabolism and growth performance of offsprings by epigenetic modification. Oxid Med Cell Longev 2019;2019:9214209. https://doi.org/10.1155/2019/9214209
  40. Oskoueian E, Ebrahimi M, Abdullah N, Rajion MA, Goh YM. Manipulation of broiler meat fatty acid composition using quercetin. 59th International Congress of Meat Science and Technology; 2013 August, 18-23; Izmir, Turkey.
  41. 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
  42. Galli GM, Gerbet RR, Griss LG, et al. Combination of herbal components (curcumin, carvacrol, thymol, cinnamaldehyde) in broiler chicken feed: Impacts on response parameters, performance, fatty acid profiles, meat quality and control of coccidia and bacteria. Microb Pathog 2020;139:103916. https://doi.org/10.1016/j.micpath.2019.103916
  43. Ahmed ST, Islam MM, Bostami ABMR, Mun HS, Kim YJ, Yang CJ. Meat composition, fatty acid profile and oxidative stability of meat from broilers supplemented with pomegranate (Punica granatum L.) by-products. Food Chem 2015;188:481-8. https://doi.org/10.1016/j.foodchem.2015.04.140
  44. Ahmed ST, Ko SY, Yang CJ. Improving the nutritional quality and shelf life of broiler meat by feeding diets supplemented with fermented pomegranate (Punica granatum L.) byproducts. Br Poult Sci 2017;58:694-703. https://doi.org/10.1080/00071668.2017.1363870
  45. Kersten S. Physiological regulation of lipoprotein lipase. Biochim Biophys Acta Mol Cell Biol Lipids 2014;1841:919-33. https://doi.org/10.1016/j.bbalip.2014.03.013
  46. Han W, Ze X, Xiong D, Li J, Li J, Zhao C. A mutation in the chicken lipoprotein lipase gene is associated with adipose traits. Anim Prod Sci 2012;52:905-10. https://doi.org/10.1071/AN12021
  47. Griffin HD, Butterwith SC, Goddard C. Contribution of lipoprotein lipase to differences in fatness between broiler and layer-strain chickens. Br Poult Sci 1987;28:197-206. https://doi.org/10.1080/00071668708416953
  48. Sato K, Akiba Y, Chida Y, Takahashi K. Lipoprotein hydrolysis and fat accumulation in chicken adipose tissues are reduced by chronic administration of lipoprotein lipase monoclonal antibodies. Poult Sci 1999;78:1286-91. https://doi.org/10.1093/ps/78.9.1286
  49. Abudilida S, Ting S, Xusheng WU, We J. Developmental Changes of A-FABP, H-FABP and PPAR-γ genes mRNA expression and its correlation with intramuscular fat content in baicheng you chicken. China Poult 2019;41:5-11. https://doi.org/10.16372/j.issn.1004-6364.2019.14.002
  50. Wang Y, Liu W, Hang C, et al. Association of A-FABP gene polymorphism and mRNA expression with intramuscular fat content (IMF) in Baicheng-You chicken. J Anim Physiol Anim Nutr 2019;103:1447-52. https://doi.org/10.1111/jpn.13150
  51. Wang Y, Chen H, Han D, et al. Correlation of the A-FABP gene polymorphism and mRNA expression with intramuscular fat content in three-yellow chicken and hetian-black chicken. Anim Biotechnol 2017;28:37-43. https://doi.org/10.1080/10495398.2016.1194288
  52. Fu RQ, Liu RR, Zhao GP, Zheng MQ, Chen JL, Wen J. Expression profiles of key transcription factors involved in lipid metabolism in Beijing-You chickens. Gene 2014;537:120-5. https://doi.org/10.1016/j.gene.2013.07.109
  53. Cui H, Zheng M, Zhao G, Liu R, Wen J. Identification of differentially expressed genes and pathways for intramuscular fat metabolism between breast and thigh tissues of chickens. BMC Genomics 2018;19:55. https://doi.org/10.1186/s12864-017-4292-3
  54. Hassan FAM, Roushdy EM, Kishawy ATY, Zaglool AW, Tukur HA, Saadeldin IM. Growth performance, antioxidant capacity, lipid-related transcript expression and the economics of broiler chickens fed different levels of rutin. Animals 2019;9:7. https://doi.org/10.3390/ani9010007
  55. Ouyang WW, Yao LI, Wei Z, Ming Hao W, Fang J. Effect of quercetin on cAMP signaling pathway in chicken adipocytes. Scientia Agricultura Sinica 2013;46:2769-76. https://doi.org/10.3864/j.issn.0578-1752.2013.13.014
  56. 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
  57. Wang M, Mao Y, Wang B, et al. Quercetin improving lipid metabolism by regulating lipid metabolism pathway of ileum mucosa in broilers. Oxid Med Cell Longev 2020;2020:8686248. https://doi.org/10.1155/2020/8686248
  58. Huang J, Zhou Y, Wan B, Wang Q, Wan X. Green tea polyphenols alter lipid metabolism in the livers of broiler chickens through increased phosphorylation of AMP-activated protein kinase. PLoS One 2017;12:e0187061. https://doi.org/10.1371/journal.pone.0187061
  59. Huang JB, Zhang Y, Zhou YB, Wan XC, Zhang JS. Effects of epigallocatechin gallate on lipid metabolism and its underlying molecular mechanism in broiler chickens. J Anim Physiol Anim Nutr 2015;99:719-27. https://doi.org/10.1111/jpn.12276
  60. Gou ZY, Cui XY, Li L, et al. Effects of dietary incorporation of linseed oil with soybean isoflavone on fatty acid profiles and lipid metabolism-related gene expression in breast muscle of chickens. Animal 2020;14:2414-22. https://doi.org/10.1017/S1751731120001020
  61. Ouyang K, Xiong X, Wang W, Hu Y, Zhou P, Liu D. Effects of alfalfa flavones on growth performance and carcass quality of female Chongren chickens. Acta Prataculturae Sinica 2013;22:340-5. https://doi.org/10.11686/cyxb20130440
  62. Cui TT, Xing TY, Chu YK, Li H, Wang N. Genetic and epigenetic regulation of PPARγ during adipogenesis. Hereditas 2017;39:1066-77. https://doi.org/10.16288/j.yczz.17-121
  63. Sun YN, Gao Y, Qiao SP, et al. Epigenetic DNA methylation in the promoters of peroxisome proliferator-activated receptor γ in chicken lines divergently selected for fatness. J Anim Sci 2014;92:48-53. https://doi.org/10.2527/jas.2013-6962
  64. Hu Y, Feng Y, Ding Z, et al. Maternal betaine supplementation decreases hepatic cholesterol deposition in chicken offspring with epigenetic modulation of SREBP2 and CYP7A1 genes. Poult Sci 2020;99:3111-20. https://doi.org/10.1016/j.psj.2019.12.058
  65. Mildner AM, Clarke SD. Porcine fatty acid synthase: cloning of a complementary DNA, tissue distribution of its mRNA and suppression of expression by somatotropin and dietary protein. J Nutr 1991;121:900-7. https://doi.org/10.1093/jn/121.6.900
  66. Zou XT, Lu JJ. Effect of betaine on the regulation of the lipid metabolism in laying hen. Scientia Agricultura Sinica 2002;3:325-330. https://doi.org/10.3321/j.issn:0578-1752.2002.03.018
  67. He S, Zhao S, Dai S, Liu D, Bokhari SG. Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress. Anim Sci J 2015;86:897-903. https://doi.org/10.1111/asj.12372
  68. Xing J, Kang L, Jiang Y. Effect of dietary betaine supplementation on lipogenesis gene expression and CpG methylation of lipoprotein lipase gene in broilers. Mol Biol Rep 2011;38:1975-81. https://doi.org/10.1007/s11033-010-0319-4
  69. Hu Y, Sun Q, Li X, et al. In ovo injection of betaine affects hepatic cholesterol metabolism through epigenetic gene regulation in newly hatched chicks. PLoS One 2015;10:e0122643. https://doi.org/10.1371/journal.pone.0122643
  70. Cui X, Li Y, Liu R, et al. Follicle-stimulating hormone increases the intramuscular fat content and expression of lipid biosynthesis genes in chicken breast muscle. J Zhejiang Univ Sci B 2016;17:303-10. https://doi.org/10.1631/jzus.B1500139
  71. Cui X, Cui H, Liu L, et al. Decreased testosterone levels after caponization leads to abdominal fat deposition in chickens. BMC Genomics 2018;19:344. https://doi.org/10.1186/s12864-018-4737-3
  72. Huang HY, Zhao GP, Liu RR, et al. Brain natriuretic peptide stimulates lipid metabolism through its receptor npr1 and the glycerolipid metabolism pathway in chicken adipocytes. Biochemistry 2015;54:6622-30. https://doi.org/10.1021/acs.biochem.5b00714
  73. Kim DH, Lee J, Suh Y, Cressman M, Lee SS, Lee K. Adipogenic and myogenic potentials of chicken embryonic fibroblasts in vitro: combination of fatty acids and insulin induces adipogenesis. Lipids 2020;55:163-71. https://doi.org/10.1002/lipd.12220
  74. Yan J, Yang H, Gan L, Sun C. Adiponectin-impaired adipocyte differentiation negatively regulates fat deposition in chicken. J Anim Physiol Anim Nutr 2014;98:530-7. https://doi.org/10.1111/jpn.12107
  75. Jiang Z, Yang Z, Zhang H, Yao Y, Ma H. Genistein activated adenosine 5'-monophosphate-activated protein kinase-sirtuin1/peroxisome proliferator-activated receptor γ coactivator-1α pathway potentially through adiponectin and estrogen receptor β signaling to suppress fat deposition in broiler chickens. Poult Sci 2021;100:246-55. https://doi.org/10.1016/j.psj.2020.10.013
  76. Wang M, Liu Z, Wang H, Guan J, Hu Q, Wang X. Effects of glucocorticoid and dietary fat level on lipid metabolism of broilers. Chinese J Anim Nutr 2018;30:3772-80. https://doi.org/10.3969/j.issn.1006-267x.2018.09.049
  77. Abobaker H, Hu Y, Hou Z, et al. Dietary betaine supplementation increases adrenal expression of steroidogenic acute regulatory protein and yolk deposition of corticosterone in laying hens. Poult Sci 2017;96:4389-98. https://doi.org/10.3382/ps/pex241
  78. 78.Omer NA, Hu Y, Idriss AA, et al. Dietary betaine improves egg-laying rate in hens through hypomethylation and glucocorticoid receptor-mediated activation of hepatic lipogenesisrelated genes. Poult Sci 2020;99:3121-32. https://doi.org/10.1016/j.psj.2020.01.017
  79. Zhou Y, Chen Z, Lin Q, et al. Nuciferine reduced fat deposition by controlling triglyceride and cholesterol concentration in broiler chickens. Poult Sci 2020;99:7101-8. https://doi.org/10.1016/j.psj.2020.09.013
  80. Xiao Y, Xiang Y, Zhou W, Chen J, Li K, Yang H. Microbial community mapping in intestinal tract of broiler chicken. Poult Sci 2017;96:1387. https://doi.org/10.3382/ps/pew372
  81. Venardou B, O'Doherty JV, Vigors S, et al. Effects of dietary supplementation with a laminarin-rich extract on the growth performance and gastrointestinal health in broilers. Poult Sci 2021;100:101179. https://doi.org/10.1016/j.psj.2021.101179
  82. Long LN, Zhang HH, Wang F, Yin YX, Yang LY, Chen JS. Research Note: Effects of polysaccharide-enriched Acanthopanax senticosus extract on growth performance, immune function, antioxidation, and ileal microbial populations in broiler chickens. Poult Sci 2021;100:101028. https://doi.org/10.1016/j.psj.2021.101028
  83. Yesilbag D, Eren M, Agel H, Kovanlikaya A, Balci F. Effects of dietary rosemary, rosemary volatile oil and vitamin E on broiler performance, meat quality and serum SOD activity. Br Poult Sci 2011;52:472-82. https://doi.org/10.1080/00071668.2011.599026
  84. Wen C, Yan W, Sun C, et al. The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens. ISME J 2019;13:1422-36. https://doi.org/10.1038/s41396-019-0367-2
  85. Indiani C, Rizzardi KF, Castelo PM, Ferraz L, Darrieux M, Parisotto TM. Childhood obesity and firmicutes/bacteroidetes ratio in the gut microbiota: a systematic review. Child Obes 2018;14:501-9. https://doi.org/10.1089/chi.2018.0040
  86. Zhao X, Guo Y, Guo S, Tan J. Effects of Clostridium butyricum and Enterococcus faecium on growth performance, lipid metabolism, and cecal microbiota of broiler chickens. Appl Microbiol Biotechnol 2013;97:6477-88. https://doi.org/10.1007/s00253-013-4970-2
  87. Zhao X, Ding X, Yang Z, Shen Y, Zhang S, Shi S. Effects of Clostridium butyricum on breast muscle lipid metabolism of broilers. Ital J Anim Sci 2018;17:1010-20. https://doi.org/10.1080/1828051X.2018.1453758
  88. Gheorghe A, Lefter NA, Idriceanu L, Ropota M, Habeanu M. Effects of dietary extruded linseed and Lactobacillus acidophilus on growth performance, carcass traits, plasma lipoprotein response, and caecal bacterial populations in broiler chicks. Ital J Anim Sci 2020;19:822-32. https://doi.org/10.1080/1828051X.2020.1801359
  89. Zhang J, Sun Y, Zhao L, et al. SCFAs-Induced GLP-1 secretion links the regulation of gut microbiome on hepatic lipogenesis in chickens. Front Microbiol 2019;10:2176. https://doi.org/10.3389/fmicb.2019.02176
  90. Lin HV, Frassetto A, Kowalik EJ Jr, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One 2012;7:e35240. https://doi.org/10.1371/journal.pone.0035240
  91. Li H, Zhao L, Liu S, Zhang Z, Wang X, Lin H. Propionate inhibits fat deposition via affecting feed intake and modulating gut microbiota in broilers. Poult Sci 2021;100:235-45. https://doi.org/10.1016/j.psj.2020.10.009
  92. Zhao L, Liu S, Zhang Z, et al. Low and high concentrations of butyrate regulate fat accumulation in chicken adipocytes via different mechanisms. Adipocyte 2020;9:120-31. https://doi.org/10.1080/21623945.2020.1738791
  93. Wang J, Chen Y, Hu X, Feng F, Cai L, Chen F. Assessing the effects of ginger extract on polyphenol profiles and the subsequent impact on the fecal microbiota by simulating digestion and fermentation in vitro. Nutrients 2020;12:3194. https://doi.org/10.3390/nu12103194
  94. Chai M, Guo Y, Li Y, Peng Y, Wang Y. Effects of Macleaya cordata extracts instead of antibiotics on growth performance, caecum microbes and tight junction gene expression of yellowfeathered broilers. Acta Microbiologica Sinica 2020;60:1718-28. https://doi.org/10.13343/j.cnki.wsxb.20190531
  95. Chen X, Zhu W, Liu X, Li T, Geng Z, Wan X. The growth performance, meat quality, and gut bacteria of broilers raised with or without antibiotics and green tea powder. J Appl Poult Res 2019;28:712-21. https://doi.org/10.3382/japr/pfz023
  96. Li W, Zhang X, He Z, et al. In vitro and in vivo antioxidant activity of eucalyptus leaf polyphenols extract and its effect on chicken meat quality and cecum microbiota. Food Res Int 2020;136:109302. https://doi.org/10.1016/j.foodres.2020.109302