{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,16]],"date-time":"2026-07-16T05:03:18Z","timestamp":1784178198302,"version":"3.55.0"},"reference-count":47,"publisher":"MDPI AG","issue":"14","license":[{"start":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T00:00:00Z","timestamp":1783641600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004761","name":"The Natural Science Foundation of Henan Province","doi-asserted-by":"crossref","award":["no.212300410136"],"award-info":[{"award-number":["no.212300410136"]}],"id":[{"id":"10.13039\/501100004761","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Fructus Ligustri Lucidi (FLL) is a traditional tonic Chinese medicine with a long history of application due to its various pharmacological effects, but there are fewer studies on the use of FLL to alleviate fatty liver in animals. The objective of the current study was to assess the influence of FLL fermentation products on fatty liver hemorrhagic syndrome in hens during the late stages of egg production. The study involved 288 Hy-Line Brown laying hens, aged 500 days, which were randomly allocated into 4 groups, with each group having 6 replicates of 12 chickens. Hens were fed a basal diet (control group, group \u0399), a high-energy diet (model group, group II) and a high-energy diet supplemented with 0.05% and 0.1% FLL fermentation product (groups III and IV). The duration of the pre-experiment was 1 week, and the trial period was 12 weeks. The results showed that the addition of FLL fermentation product to high-energy diets significantly increased egg weight and reduced eggshell breakage rate. High-energy diet supplementation with FLL fermentation product increased serum T-AOC and T-SOD activity (p &lt; 0.05), and reduced serum MDA content (p &lt; 0.05). As more FLL fermentation product was added, there was a notable reduction in lipid droplets in liver tissues, alleviation of symptoms of steatosis, and suppression of mRNA expression levels of lipid synthesis genes ACC, FAS, and SCD in the liver (p &lt; 0.001). Transcription factors such as NR1H3 (p &lt; 0.01), LPK (p &lt; 0.001), and SREBF1 (p &lt; 0.05) were differentially down-regulated, significantly reducing MTTP gene expression (p &lt; 0.001). It can be concluded that the addition of 0.1% FLL fermentation product can enhance the productivity of laying hens during their late laying phase, increase the antioxidant capacity, inhibit the mRNA expression level of genes related to fat synthesis in the liver, reduce the accumulation of fat, and alleviate the fatty liver of laying hens caused by the high-energy diet.<\/jats:p>","DOI":"10.3390\/ani16142147","type":"journal-article","created":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T13:16:28Z","timestamp":1783689388000},"page":"2147","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Protective Effects of Fructus Ligustri Lucidi Fermentation on Fatty Liver Hemorrhagic Syndrome in Laying Hens"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6696-7703","authenticated-orcid":false,"given":"Xiaoli","family":"Li","sequence":"first","affiliation":[{"name":"College of Animal Science and Technology, Henan University of Science and Technology, No. 263 Kaiyuan Road, Luoyang 471000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-4520-4780","authenticated-orcid":false,"given":"Songchen","family":"Yuan","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Henan University of Science and Technology, No. 263 Kaiyuan Road, Luoyang 471000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xixi","family":"Li","sequence":"additional","affiliation":[{"name":"Henan Egdoo Technology Group Co., Ltd., No. 221 Lianhua Street, Zhengzhou 450001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaowei","family":"Ding","sequence":"additional","affiliation":[{"name":"Henan Egdoo Technology Group Co., Ltd., No. 221 Lianhua Street, Zhengzhou 450001, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wanling","family":"He","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Henan University of Science and Technology, No. 263 Kaiyuan Road, Luoyang 471000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3559","DOI":"10.3382\/ps\/pex163","article-title":"Abnormal histopathology, fat percent and hepatic apolipoprotein A I and apolipoprotein B100 mRNA expression in fatty liver hemorrhagic syndrome and their improvement by soybean lecithin","volume":"96","author":"Song","year":"2017","journal-title":"Poult. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1016\/j.psj.2019.10.009","article-title":"The protective effects of resveratrol on antioxidant function and the mRNA expression of inflammatory cytokines in the ovaries of hens with fatty liver hemorrhagic syndrome","volume":"99","author":"Xing","year":"2020","journal-title":"Poult. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1080\/03079457.2018.1538550","article-title":"Fatty liver haemorrhagic syndrome occurrence in laying hens: Impact of production system","volume":"48","author":"Shini","year":"2019","journal-title":"Avian Pathol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1232","DOI":"10.3923\/ijps.2008.1232.1236","article-title":"Effect of different dietary energy Sources on Induction of fatty liver-hemorrhagic syndrome in laying hens","volume":"7","author":"Zhang","year":"2008","journal-title":"Int. J. Poult. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Chen, B., Wang, L., Li, L., Zhu, R., Liu, H., Liu, C., Ma, R., Jia, Q., Zhao, D., and Niu, J. (2017). Fructus Ligustri Lucidi in Osteoporosis: A Review of its Pharmacology, Phytochemistry, Pharmacokinetics and Safety. Molecules, 22.","DOI":"10.3390\/molecules22091469"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"115789","DOI":"10.1016\/j.jep.2022.115789","article-title":"Ligustri Lucidi Fructus, a traditional Chinese Medicine: Comprehensive review of botany, traditional uses, chemical composition, pharmacology, and toxicity","volume":"301","author":"Cao","year":"2023","journal-title":"J. Ethnopharmacol."},{"key":"ref_7","first-page":"4494","article-title":"Effects of Dietary Oleanolic Acid on Performance, Serum Biochemical Indices and Antioxidant Function of Laying Hens with Fatty Liver Hemorrhagic Syndrome Induced by High-Energy and Low-Protein Die","volume":"37","author":"Wu","year":"2025","journal-title":"Chin. J. Anim. Nutr."},{"key":"ref_8","unstructured":"NRC (1994). Nutrient Requirements of Poultry, National Academy Press."},{"key":"ref_9","unstructured":"Wen, J., Cai, H.Y., Guo, Y.M., Qi, G.H., Chen, J.L., Zhang, G.Z., Liu, G.H., Xiong, B.H., Su, J.S., and Ji, C. (2004). Feeding Standard of Chicken, Ministry of Agriculture of the People\u2019s Republic of China."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and 2\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2509","DOI":"10.3382\/ps\/pey596","article-title":"Interactions between the cecal microbiota and non-alcoholic steatohepatitis using laying hens as the model","volume":"98","author":"Hamid","year":"2019","journal-title":"Poult. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1637\/10382-092312-Case.1","article-title":"Causes of mortality in backyard chickens in northern California: 2007\u20132011","volume":"57","author":"Mete","year":"2013","journal-title":"Avian Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"skad045","DOI":"10.1093\/jas\/skad045","article-title":"Alleviation effect of conjugated linoleic acid on estradiol benzoate induced fatty liver hemorrhage syndrome in Hy-line male chickens","volume":"101","author":"Wang","year":"2023","journal-title":"J. Anim. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2489","DOI":"10.1007\/s11259-024-10420-1","article-title":"Development of fatty liver disease model using high cholesterol and low choline diet in white leghorn chickens","volume":"48","author":"Yadav","year":"2024","journal-title":"Vet. Res. Commun."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"103785","DOI":"10.1016\/j.psj.2024.103785","article-title":"Quantitative lipidomics reveals the changes of lipids and antioxidant capacity in egg yolk from laying hens with fatty liver hemorrhagic syndrome","volume":"103","author":"Guo","year":"2024","journal-title":"Poult. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Wang, N., Li, W., Ouyang, G., Li, H., Yang, J., and Wu, G. (2025). Goose Deoxycholic Acid Ameliorates Liver Injury in Laying Hens with Fatty Liver Hemorrhage Syndrome by Inhibiting the Inflammatory Response. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26010429"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Lv, Z., Xing, K., Li, G., Liu, D., and Guo, Y. (2018). Dietary genistein alleviates lipid metabolism disorder and inflammatory response in laying hens with fatty liver syndrome. Front. Physiol., 9.","DOI":"10.3389\/fphys.2018.01493"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"102085","DOI":"10.1016\/j.psj.2022.102085","article-title":"Heat stress in broilers of liver injury effects of heat stress on oxidative stress and autophagy in liver of broilers","volume":"101","author":"Tang","year":"2022","journal-title":"Poult. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"668","DOI":"10.2460\/javma.2004.224.668","article-title":"Lipoprotein-mediated transport of dietary and synthesized lipids and lipid abnormalities of dogs and cats","volume":"224","author":"Bauer","year":"2004","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1016\/j.psj.2020.11.036","article-title":"Protective effect of the new prepared Atractylodes macrocephala Koidz polysaccharide on fatty liver hemorrhagic syndrome in laying hens","volume":"100","author":"Miao","year":"2021","journal-title":"Poult. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1089\/ars.2018.7544","article-title":"Peroxiredoxin 6 Confers protection against nonalcoholic fatty liver disease through maintaining Mitochondrial function","volume":"31","author":"Lee","year":"2019","journal-title":"Antioxid. Redox Signal."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1159\/000485089","article-title":"Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species","volume":"44","author":"He","year":"2017","journal-title":"Cell. Physiol. Biochem."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Zhang, Y., Liu, Z., Liu, R., Wang, J., Zheng, M., and Li, Q. (2018). Alteration of hepatic gene expression along with the inherited phenotype of acquired fatty liver in chicken. Genes, 9.","DOI":"10.3390\/genes9040199"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Luan, R., Zhao, P., Zhang, X., Li, Q., Chen, X., and Wang, L. (2023). Pharmacodynamics, Pharmacokinetics, and Kidney Distribution of Raw and Wine-Steamed Ligustri Lucidi Fructus Extracts in Diabetic Nephropathy Rats. Molecules, 28.","DOI":"10.3390\/molecules28020791"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"102350","DOI":"10.1016\/j.psj.2022.102350","article-title":"Effects of Astragalus, Epimedium, and Fructus Ligustri Lucidi extractive on antioxidant capacity, production performance, and immune mechanism of breeding pigeons under stress","volume":"102","author":"Zhang","year":"2023","journal-title":"Poult. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1002\/ptr.2603","article-title":"Antidiabetic and antioxidant effects of oleanolic acid from Ligustrum lucidum Ait in alloxan-induced diabetic rats","volume":"23","author":"Gao","year":"2009","journal-title":"Phytother. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.jep.2006.11.004","article-title":"Protective effects of Ligustrum lucidum fruit extract on acute butylated hydroxytoluene-induced oxidative stress in rats","volume":"111","author":"Lin","year":"2007","journal-title":"J. Ethnopharmacol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"11245","DOI":"10.1073\/pnas.0404297101","article-title":"Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver","volume":"101","author":"Chen","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"7281","DOI":"10.1073\/pnas.0401516101","article-title":"Deficiency of carbohydrate response element-binding protein (ChREBP) reduces lipogenesis as well as glycolysis","volume":"101","author":"Lizuka","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1093\/jn\/121.6.900","article-title":"Porcine fatty acid synthase: Cloning of a complementary DNA, tissue distribution of its mRNA and suppression of expression by somatotropin and dietary protein","volume":"121","author":"Mildner","year":"1991","journal-title":"J. Nutr."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S1388-1981(01)00142-1","article-title":"The age-related differences in obese and fatty acid synthase gene expression in white adipose tissue of rat","volume":"1533","author":"Nogalska","year":"2001","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"16401","DOI":"10.1016\/j.heliyon.2023.e16401","article-title":"Taurine alleviated hepatic steatosis in oleic acid-treated-HepG2 cells and rats fed a high-fat diet","volume":"9","author":"Song","year":"2023","journal-title":"Heliyon"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/j.cmet.2017.07.009","article-title":"Acetyl CoA Carboxylase Inhibition Reduces Hepatic Steatosis but Elevates Plasma Triglycerides in Mice and Humans: A Bedside to Bench Investigation","volume":"26","author":"Kim","year":"2017","journal-title":"Cell Metab."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1146\/annurev.nutr.27.061406.093618","article-title":"ChREBP, a transcriptional regulator of glucose and lipid metabolism","volume":"27","author":"Postic","year":"2007","journal-title":"Annu. Rev. Nutr."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1002\/jcp.29890","article-title":"Carbohydrate response element-binding protein regulates lipid metabolism via mTOR complex1 in diabetic nephropathy","volume":"236","author":"Chen","year":"2021","journal-title":"J. Cell. Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1515\/znc-2015-4161","article-title":"Preventive effect of total glycosides from Ligustri Lucidi Fructus against nonalcoholic fatty liver in mice","volume":"70","author":"Yang","year":"2015","journal-title":"Z. Naturforschung C"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"10964","DOI":"10.1021\/acs.jafc.8b03372","article-title":"Oleanolic Acid Inhibits Liver X Receptor Alpha and Pregnane X Receptor to Attenuate Ligand-Induced Lipogenesis","volume":"66","author":"Lin","year":"2018","journal-title":"J. Agr. Food Chem."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"111137","DOI":"10.1016\/j.biopha.2020.111137","article-title":"Salidroside simultaneously reduces de novo lipogenesis and cholesterol biosynthesis to attenuate atherosclerosis in mice","volume":"134","author":"Song","year":"2021","journal-title":"Biomed. Pharmacother."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.3382\/ps.2012-02800","article-title":"Changes of blood parameters associated with bone remodeling following experimentally induced fatty liver disorder in laying hens","volume":"92","author":"Jiang","year":"2013","journal-title":"Poult. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1479","DOI":"10.3382\/ps.0721479","article-title":"Fatty liver hemorrhagic syndrome in hens overfed a purified diet. Selected enzyme activities and liver histology in relation to liver hemorrhage and reproductive performance","volume":"72","author":"Walzem","year":"1993","journal-title":"Poult. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.theriogenology.2021.11.019","article-title":"Dietary mulberry-leaf flavonoids improve the eggshell quality of aged breeder hens","volume":"179","author":"Huang","year":"2022","journal-title":"Theriogenology"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"4598","DOI":"10.1016\/j.psj.2020.05.032","article-title":"The effect of total flavonoids of Epimedium on granulosa cell development in laying hens","volume":"99","author":"Guo","year":"2020","journal-title":"Poult. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1186\/s40168-025-02083-0","article-title":"Lactiplantibacillus plantarum FRT4 protects against fatty liver hemorrhage syndrome: Regulating gut microbiota and FoxO\/TLR-4\/NF-\u03baB signaling pathway in laying hens","volume":"13","author":"Li","year":"2025","journal-title":"Microbiome"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"155291","DOI":"10.1016\/j.phymed.2023.155291","article-title":"Aqueous extract of fermented Eucommia ulmoides leaves alleviates hyperlipidemia by maintaining gut homeostasis and modulating metabolism in high-fat diet fed rats","volume":"128","author":"Duan","year":"2024","journal-title":"Phytomedicine"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"144463","DOI":"10.1016\/j.foodchem.2025.144463","article-title":"Enhanced bioactivity of honeysuckle-Cassia seeds extracts through Lactobacillus acidophilus and Bacillus subtilis co-fermentation: Impact on alcoholic liver disease and gut microbiota","volume":"486","author":"Zhou","year":"2025","journal-title":"Food Chem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"105422","DOI":"10.1016\/j.jff.2023.105422","article-title":"Bioactive peptides derived from fermented foods: Preparation and biological activities","volume":"101","author":"Guo","year":"2023","journal-title":"J. Funct. Foods"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/s40104-025-01178-w","article-title":"Herbal extract fermented with inherent microbiota improves intestinal health by exerting antioxidant and anti-inflammatory effects in vitro and in vivo","volume":"16","author":"Heckmann","year":"2025","journal-title":"J. Anim. Sci. Biotechnol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/14\/2147\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,16]],"date-time":"2026-07-16T04:13:36Z","timestamp":1784175216000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/16\/14\/2147"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,10]]},"references-count":47,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2026,7]]}},"alternative-id":["ani16142147"],"URL":"https:\/\/doi.org\/10.3390\/ani16142147","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,10]]}}}