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Article(id=1307013212096983543, tenantId=1146029695717560320, journalId=1306274286668972124, issueId=1307013104081068276, articleNumber=null, orderNo=null, doi=10.11843/j.issn.0366-6964.2026.02.043, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1745942400000, receivedDateStr=2025-04-30, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1789545832894, onlineDateStr=2026-09-16, pubDate=1771776000000, pubDateStr=2026-02-23, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1789545832894, onlineIssueDateStr=2026-09-16, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1789545832894, creator=13701087609, updateTime=1789545832894, updator=13701087609, issue=Issue{id=1307013104081068276, tenantId=1146029695717560320, journalId=1306274286668972124, year='2026', volume='57', issue='2', pageStart='569', pageEnd='1176', issueExtLink='null', onlineDate='null', pubDate='1771776000000', pubDateStr='2026-02-23', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1789545807142, creator='13701087609', updateTime=1789609910854, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1307281975350419753, tenantId=1146029695717560320, journalId=1306274286668972124, issueId=1307013104081068276, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1307281975350419754, tenantId=1146029695717560320, journalId=1306274286668972124, issueId=1307013104081068276, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=1099, endPage=1109, ext={EN=ArticleExt(id=1307013212323475960, articleId=1307013212096983543, tenantId=1146029695717560320, journalId=1306274286668972124, language=EN, title=Preventive Effects of Aspirin Eugenol Ester on Oxidative Stress and Inflammatory Response in the Ovaries of Hens with Fatty Liver Hemorrhagic Syndrome, columnId=1307007406035198078, journalTitle=Acta Veterinaria et Zootechnica Sinica, columnName=BASIC VETERINARY MEDICINE, runingTitle=null, highlight=null, articleAbstract=

This study aimed to investigate preventive effects of aspirin eugenol ester （AEE） on oxidative stress and inflammatory response in the ovaries of hens with fatty liver hemorrhagic syndrome （FLHS）. A total of sixty-five 160-day-old Hy-Line Brown laying hens were randomly assigned to five groups， each containing 13 hens. The control group （Control） was fed a basal diet， while the model group （high-energy low-protein diet， HELP） and low-， medium-， and high-dose AEE treatment groups （AEE-L， AEE-M， AEE-H） were all fed a high-energy low-protein diet supplemented with 0， 25， 50， and 100 mg·kg-1 aspirin eugenol ester， respectively. The results showed that， compared with the control group， the ovaries of laying hens in the HELP group exhibited distinct lipid vacuoles of varying sizes. In contrast， the number of lipid vacuoles in the ovarian tissue was significantly reduced in the AEE-treated groups compared with the HELP group. Compared with the control group， the activities of SOD， GSH， and CAT in the ovaries of hens in the HELP group were significantly decreased， while the level of MDA was significantly increased （P<0.05）. In contrast， AEE treatment groups demonstrated significantly enhanced SOD， CAT， and GSH activities and reduced MDA levels and significantly upregulated SOD and CAT mRNA transcription compared with the HELP group （P<0.05）. Compared with the Control group， the expression levels of antioxidant-related genes and proteins Nrf2， NQO1， and HO-1 were significantly decreased in the ovaries of hens in the HELP group， while the expression of Keap1 was significantly increased （P<0.05）. In contrast， the AEE-treated groups showed significantly increased expression of Nrf2， NQO1， and HO-1 and decreased expression of Keap1 compared with the HELP group （P<0.05）. Compared with the control group， the mRNA transcription levels of inflammatory cytokines IL-1β， IL-6， and TNF-α were significantly increased in the ovaries of hens in the HELP group. In addition， the expression levels of inflammation-related genes and proteins-including TLR4， NF-κB， and p-p65 were also significantly elevated （P<0.05）. In contrast， AEE treatment groups exhibited significantly reduced expression of IL-1β， IL-6， TNF-α， TLR4 and NF-κB genes， along with significantly decreased p-p65 protein expression compared to the HELP group （P<0.05）. In summary， fatty liver hemorrhagic syndrome in laying hens can induce ovarian oxidative stress and inflammatory responses. Supplementation with varying doses of AEE demonstrated preventive effects against ovarian damage in laying hens with fatty liver hemorrhagic syndrome.

, authors=Wenbo GE, Kai YAN, Yajun YANG, Xiwang LIU, Xiao XU, Shihong LI, Lixia BAI, Zhe QIN, Zhun LI, Jianyong LI, authorsList=Wenbo GE, Kai YAN, Yajun YANG, Xiwang LIU, Xiao XU, Shihong LI, Lixia BAI, Zhe QIN, Zhun LI, Jianyong LI, authorCompany=null, correspAuthors=Jianyong LI, authorNote=null, correspAuthorsNote=
LI Jianyong， E-mail：
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旨在探讨阿司匹林丁香酚酯（aspirin eugenol ester，AEE）对脂肪肝出血综合征（fatty liver hemorrhagic syndrome，FLHS）蛋鸡卵巢氧化应激和炎症反应的预防作用。选取65羽健康的160日龄海兰褐蛋鸡，随机分为5组，每组13羽。空白对照组（Control）饲喂基础日粮；模型组（high-energy low-protein diet，HELP）和低、中、高剂量AEE给药组（AEE-L、AEE-M、AEE-H）均饲喂高能低蛋白日粮，并根据蛋鸡体重，分别在高能低蛋白日粮中添加0、25、50、100 mg∙kg-1阿司匹林丁香酚酯。结果显示，相较于Control组，HELP组蛋鸡卵巢有明显的大小不等的脂肪空泡；相较于HELP组，AEE组卵巢组织脂肪空泡数量显著减少。相较于Control组，HELP组蛋鸡卵巢中超氧化物歧化酶（superoxide dismutase，SOD）、谷胱甘肽过氧化物酶（glutathione peroxidase，GSH）、过氧化氢酶（catalase，CAT）活性显著降低，丙二醛（malondialdehyde，MDA）水平显著升高（P<0.05）；相较于HELP组，不同剂量AEE组SOD、CAT、GSH活性显著增加，MDA水平显著减少（P<0.05），SOD和CAT mRNA转录显著升高（P<0.05）。相较于Control组，HELP组蛋鸡卵巢中抗氧化相关基因和蛋白，如核因子E2相关因子2（nuclear factor erythroid-2-related factor 2，Nrf2）、醌氧化还原酶1（NADPH：Quinone Oxidoreductase1，NQO1）、血红素加氧酶1（heme oxygenase-1，HO-1）表达显著降低，kelch样ECH关联蛋白1（kelch-like ECH-associated protein 1，Keap1）表达显著升高（P<0.05）；相较于HELP组，不同剂量AEE组Nrf2、NQO1、HO-1基因和蛋白表达显著升高，Keap1表达显著降低（P<0.05）。相较于Control组，HELP组蛋鸡卵巢中炎性因子白细胞介素1β（interleukin-1β，IL-1β）、白细胞介素6（interleukin-6，IL-6）、肿瘤坏死因子α（tumor necrosis factor-α，TNF-α）mRNA转录显著升高，炎症相关基因和蛋白（toll-like receptor 4，TLR4）、核因子κB（nuclear factor kappa B，NF-κB）、磷酸化p65（phosphorylated p65，p-p65）表达显著增加（P<0.05）；相较于HELP组，不同剂量AEE组IL-1β、IL-6、TNF-α、TLR4、NF-κB基因转录显著减少，p-p65蛋白表达显著降低（P<0.05）。综上，蛋鸡脂肪肝出血综合征可导致卵巢发生氧化应激和炎症反应；高能低蛋白日粮中添加不同剂量AEE对脂肪肝出血综合征蛋鸡卵巢损伤均有一定的预防效果。

, authors=葛闻博, 言凯, 杨亚军, 刘希望, 许笑, 李世宏, 白莉霞, 秦哲, 李准, 李剑勇, authorsList=葛闻博, 言凯, 杨亚军, 刘希望, 许笑, 李世宏, 白莉霞, 秦哲, 李准, 李剑勇, authorCompany=null, correspAuthors=李剑勇, authorNote=

葛闻博，主要从事药理毒理学研究，E-mail： ；Tel： 0931-2117168

, correspAuthorsNote=
李剑勇，主要从事药理毒理学研究，E-mail：
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葛闻博，主要从事药理毒理学研究，E-mail： ；Tel： 0931-2117168

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葛闻博，主要从事药理毒理学研究，E-mail： ；Tel： 0931-2117168

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doi=null, pmid=null, pmcid=null, year=null, volume=null, issue=null, pageStart=null, pageEnd=null, url=null, language=null, rfNumber=[36], rfOrder=40, authorNames=null, journalName=null, refType=null, unstructuredReference=LIEW F Y，XU D，BRINT E K，et al.Negative regulation of toll-like receptor-mediated immune responses［J］.Nat Rev Immunol，2005，5（6）：446-458., articleTitle=null, refAbstract=null), Reference(id=1307282419279745734, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, doi=null, pmid=null, pmcid=null, year=null, volume=null, issue=null, pageStart=null, pageEnd=null, url=null, language=null, rfNumber=[37], rfOrder=41, authorNames=null, journalName=null, refType=null, unstructuredReference=LI J W，LI L，WANG S，et al.Resveratrol alleviates inflammatory responses and oxidative stress in rat kidney ischemia-reperfusion injury and H2O2-induced NRK-52E cells via the Nrf2/TLR4/NF-κB pathway［J］.Cell Physiol Biochem，2018，45（4）：1677-1689., articleTitle=null, refAbstract=null), Reference(id=1307282419355243207, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, doi=null, pmid=null, pmcid=null, year=null, volume=null, issue=null, pageStart=null, pageEnd=null, url=null, language=null, rfNumber=[38], rfOrder=42, authorNames=null, journalName=null, refType=null, unstructuredReference=HU B，WEI H J，SONG Y H，et al.NF-κB and Keap1 interaction represses Nrf2-mediated antioxidant response in rabbit hemorrhagic disease virus infection［J］.J Virol，2020，94（10）：e00016-20., articleTitle=null, refAbstract=null)], funds=[Fund(id=1307282411763552921, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, awardId=25ZDNA003, language=CN, fundingSource=甘肃省科技计划资助(25ZDNA003), fundOrder=null, country=null), Fund(id=1307282411839050394, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, awardId=25JRRA456, language=CN, 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A. Control； B. HELP； C. AEE-L； D. AEE-M； E. AEE-H； F. The relative counts of fat droplets； The red arrows indicate lipid droplet vacuoles. The same lowercase letters indicate no significant difference（P>0.05），different lowercase letters indicate significant difference（P<0.05）. The same as below

, figureFileSmall=zeKdcSNkkBwbkIkcq2w6Fw==, figureFileBig=k1z6wy0tWliyMGlNTFzIxg==, tableContent=null), ArticleFig(id=1307282410559787662, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=CN, label=图1, caption=卵巢组织切片HE染色（图A~E中，标尺=20 μm）

A. 对照组；B. 模型组；C. AEE低剂量组；D. AEE中剂量组；E. AEE高剂量组；F. 脂肪滴相对数量；红色箭头代表脂滴空泡。相同小写字母表示差异不显著（P>0.05），不同小写字母表示差异显著（P<0.05）。下同

, figureFileSmall=zeKdcSNkkBwbkIkcq2w6Fw==, figureFileBig=k1z6wy0tWliyMGlNTFzIxg==, tableContent=null), ArticleFig(id=1307282410723365519, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=EN, label=Fig.2, caption=Effects of AEE on ovary antioxidant indicators

A. SOD content；B. GSH content；C. CAT content；D. MDA content

, figureFileSmall=x/14bGES8le3PVkwJeJqxQ==, figureFileBig=EakDRUqEWNLtqQ0pHwWsPg==, tableContent=null), ArticleFig(id=1307282410803057296, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=CN, label=图2, caption=AEE对卵巢组织抗氧化指标的影响

A. SOD含量；B. GSH含量；C. CAT含量；D. MDA含量

, figureFileSmall=x/14bGES8le3PVkwJeJqxQ==, figureFileBig=EakDRUqEWNLtqQ0pHwWsPg==, tableContent=null), ArticleFig(id=1307282410912109201, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=EN, label=Fig.3, caption=Effects of AEE on ovary antioxidant gene and protein expression

A. The relative transcription of Nrf2 mRNA；B. The relative transcription of Keap1 mRNA；C. The relative transcription of NQO1 mRNA；D. The relative transcription of HO-1 mRNA；E. The relative transcription of SOD mRNA；F. The relative transcription of CAT mRNA；G. The result of Western blot；H. The relative expression of Nrf2 protein；I. The relative expression of Keap1 protein；J. The relative expression of NQO1 protein；K. The relative expression of HO-1 protein

, figureFileSmall=apLv7M8JZs7E5ixNYmrHWg==, figureFileBig=Lm0hZqdngo33x0+b2tuwcw==, tableContent=null), ArticleFig(id=1307282411004383890, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=CN, label=图3, caption=AEE对卵巢组织抗氧化基因和蛋白表达的影响

A. Nrf2 mRNA相对转录量；B. Keap1 mRNA相对转录量；C. NQO1 mRNA相对转录量；D. HO-1 mRNA相对转录量；E. SOD mRMA相对转录量；F. CAT mRNA相对转录量；G. Western blot结果；H. Nrf2蛋白相对表达量；I. Keap蛋白相对表达量；J. NQO1蛋白相对表达量；K. HO-1蛋白相对表达量

, figureFileSmall=apLv7M8JZs7E5ixNYmrHWg==, figureFileBig=Lm0hZqdngo33x0+b2tuwcw==, tableContent=null), ArticleFig(id=1307282411079881363, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=EN, label=Fig.4, caption=Effects of AEE on ovary inflammation gene and protein expression

A. The relative transcription of TLR4 mRNA；B. The relative transcription of NF-κB mRNA；C. The relative transcription of IL-1β mRNA；D. The relative transcription of IL-6 mRNA；E. The relative transcription of TNF-α mRNA；F. The result of Western blot；G. The relative expression of p-p65 protein

, figureFileSmall=Q605KsoO7Wde8/USCCaUoQ==, figureFileBig=OcDXVYqgBBr5YE2BWzWl2g==, tableContent=null), ArticleFig(id=1307282411193127572, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=CN, label=图4, caption=AEE对卵巢组织炎症基因和蛋白表达的影响

A. TLR4 mRNA相对转录量；B. NF-κB mRNA相对转录量；C. IL-1β mRNA相对转录量；D. IL-6 mRNA相对转录量；E. TNF-α mRMA相对转录量；F. Western blot结果；G. p-p65蛋白相对表达量

, figureFileSmall=Q605KsoO7Wde8/USCCaUoQ==, figureFileBig=OcDXVYqgBBr5YE2BWzWl2g==, tableContent=null), ArticleFig(id=1307282411285402261, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=EN, label=Table 1, caption=

Composition and nutrient levels of basal and high-energy low-protein diet （air-dry basis）

, figureFileSmall=null, figureFileBig=null, tableContent=
项目 Items含量 Content
基础日粮 Basic diet高能低蛋白日粮 High-energy low-protein diet
原料 Ingredients
玉米 Corn64.0070.00
豆粕 Soybean meal26.0015.78
豆油 Soybean oil4.22
钙 Calcium8.008.00
预混料* Premix*2.002.00
合计 Total100.00100.00
营养水平 Nutrient level
代谢能 ME/（kJ∙kg-1）11 248.6413 212.22
粗蛋白质 CP15.5012.30
有效磷 AP0.530.51
精氨酸 Arg1.030.74
蛋氨酸 Met0.370.32
缬氨酸 Val0.770.58
蛋氨酸+半胱氨酸 Met+Cys0.670.56
), ArticleFig(id=1307282411365094038, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=CN, label=表1, caption=

基础饲粮组成及营养水平（风干基础） (%)

, figureFileSmall=null, figureFileBig=null, tableContent=
项目 Items含量 Content
基础日粮 Basic diet高能低蛋白日粮 High-energy low-protein diet
原料 Ingredients
玉米 Corn64.0070.00
豆粕 Soybean meal26.0015.78
豆油 Soybean oil4.22
钙 Calcium8.008.00
预混料* Premix*2.002.00
合计 Total100.00100.00
营养水平 Nutrient level
代谢能 ME/（kJ∙kg-1）11 248.6413 212.22
粗蛋白质 CP15.5012.30
有效磷 AP0.530.51
精氨酸 Arg1.030.74
蛋氨酸 Met0.370.32
缬氨酸 Val0.770.58
蛋氨酸+半胱氨酸 Met+Cys0.670.56
), ArticleFig(id=1307282411474145943, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=EN, label=Table 2, caption=

Real-time fluorescent quantitative PCR amplification primers

, figureFileSmall=null, figureFileBig=null, tableContent=

基因名称

Gene name

引物序列（5′→3′）

Primer sequences

登录号

Accession No.

IL-1βF： ACTGGGCATCAAGGGCTANM_204524.2
R： GGTAGAAGATGAAGCGGGTC
IL-6F： AGGACGAGATGTGCAAGAAGTNM_204628.2
R： TTGGGCAGGTTGAGGTTGTT
TNF-αF： GCCCTTCCTGTAACCAGATGNM_204267.2
R： ACACGACAGCCAAGTCAACG
NF-κBF： TCAACGCAGGACCTAAAGACATNM_205134
R： GCAGATAGCCAAGTTCAGGATG
TLR4F： GGATCTTTCAAGGTGCCACAKP410249.1
R： CAAGTGTCCGATGGGTAGGT
SOD1F： GGTGCTCACTTTAATCCTGNM_205064.2
R： CTACTTCTGCCACTCCTCC
CATF： TGCAAGGCGAAAGTGTTTGANM_001031215.2
R： CCCACAAGATCCCAGTTACCT
Nrf2F： ATCACCTCTTCTGCACCGAANM_205117.2
R： GCTTTCTCCCGCTCTTTCTG
HO-1F： CTTCGCACAAGGAGTGTTAACNM_205344.2
R： CATCCTGCTTGTCCTCTCAC
Keap1F： TGCCCCTGTGGTCAAAGTGMN416132.1
R： GGTTCGGTTACCGTCCTGC
NQO1F： CGCACCCTGAGAAAACCTCTNM_001277620.2
R： TTCTTGAGGGGTCCGGTGAT
β-actinF： AGCGAACGCCCCCAAAGTTCTNM_205518
R： AGCTGGGCTGTTGCCTTCACA
), ArticleFig(id=1307282411553837720, tenantId=1146029695717560320, journalId=1306274286668972124, articleId=1307013212096983543, language=CN, label=表2, caption=

荧光定量PCR扩增引物

, figureFileSmall=null, figureFileBig=null, tableContent=

基因名称

Gene name

引物序列（5′→3′）

Primer sequences

登录号

Accession No.

IL-1βF： ACTGGGCATCAAGGGCTANM_204524.2
R： GGTAGAAGATGAAGCGGGTC
IL-6F： AGGACGAGATGTGCAAGAAGTNM_204628.2
R： TTGGGCAGGTTGAGGTTGTT
TNF-αF： GCCCTTCCTGTAACCAGATGNM_204267.2
R： ACACGACAGCCAAGTCAACG
NF-κBF： TCAACGCAGGACCTAAAGACATNM_205134
R： GCAGATAGCCAAGTTCAGGATG
TLR4F： GGATCTTTCAAGGTGCCACAKP410249.1
R： CAAGTGTCCGATGGGTAGGT
SOD1F： GGTGCTCACTTTAATCCTGNM_205064.2
R： CTACTTCTGCCACTCCTCC
CATF： TGCAAGGCGAAAGTGTTTGANM_001031215.2
R： CCCACAAGATCCCAGTTACCT
Nrf2F： ATCACCTCTTCTGCACCGAANM_205117.2
R： GCTTTCTCCCGCTCTTTCTG
HO-1F： CTTCGCACAAGGAGTGTTAACNM_205344.2
R： CATCCTGCTTGTCCTCTCAC
Keap1F： TGCCCCTGTGGTCAAAGTGMN416132.1
R： GGTTCGGTTACCGTCCTGC
NQO1F： CGCACCCTGAGAAAACCTCTNM_001277620.2
R： TTCTTGAGGGGTCCGGTGAT
β-actinF： AGCGAACGCCCCCAAAGTTCTNM_205518
R： AGCTGGGCTGTTGCCTTCACA
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阿司匹林丁香酚酯对脂肪肝出血综合征蛋鸡卵巢氧化应激和炎症反应预防作用
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葛闻博 , 言凯 , 杨亚军 , 刘希望 , 许笑 , 李世宏 , 白莉霞 , 秦哲 , 李准 , 李剑勇
畜牧兽医学报 | 基础兽医 2026,57(2): 1099-1109
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畜牧兽医学报 |基础兽医 2026 , 57 (2) : 1099 -1109
阿司匹林丁香酚酯对脂肪肝出血综合征蛋鸡卵巢氧化应激和炎症反应预防作用
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葛闻博 , 言凯, 杨亚军, 刘希望, 许笑, 李世宏, 白莉霞, 秦哲, 李准, 李剑勇
作者信息
  • 中国农业科学院兰州畜牧与兽药研究所 农业农村部兽用药物创制重点实验室/甘肃省新兽药工程重点实验室，兰州 730050
通讯作者:
李剑勇，主要从事药理毒理学研究，E-mail：
作者简介:

葛闻博，主要从事药理毒理学研究，E-mail： ；Tel： 0931-2117168

Preventive Effects of Aspirin Eugenol Ester on Oxidative Stress and Inflammatory Response in the Ovaries of Hens with Fatty Liver Hemorrhagic Syndrome
Wenbo GE , Kai YAN, Yajun YANG, Xiwang LIU, Xiao XU, Shihong LI, Lixia BAI, Zhe QIN, Zhun LI, Jianyong LI
Affiliations
  • Key Laboratory of New Animal Drug Project of Gansu Province，Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs，Lanzhou Institute of Husbandry and Pharmaceutical Sciences，Chinese Academy of Agricultural Sciences，Lanzhou 730050，China
    • Corresponding Author:
    LI Jianyong， E-mail：
出版时间: 2026-02-23 doi: 10.11843/j.issn.0366-6964.2026.02.043
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摘要
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旨在探讨阿司匹林丁香酚酯（aspirin eugenol ester，AEE）对脂肪肝出血综合征（fatty liver hemorrhagic syndrome，FLHS）蛋鸡卵巢氧化应激和炎症反应的预防作用。选取65羽健康的160日龄海兰褐蛋鸡，随机分为5组，每组13羽。空白对照组（Control）饲喂基础日粮；模型组（high-energy low-protein diet，HELP）和低、中、高剂量AEE给药组（AEE-L、AEE-M、AEE-H）均饲喂高能低蛋白日粮，并根据蛋鸡体重，分别在高能低蛋白日粮中添加0、25、50、100 mg∙kg-1阿司匹林丁香酚酯。结果显示，相较于Control组，HELP组蛋鸡卵巢有明显的大小不等的脂肪空泡；相较于HELP组，AEE组卵巢组织脂肪空泡数量显著减少。相较于Control组，HELP组蛋鸡卵巢中超氧化物歧化酶（superoxide dismutase，SOD）、谷胱甘肽过氧化物酶（glutathione peroxidase，GSH）、过氧化氢酶（catalase，CAT）活性显著降低，丙二醛（malondialdehyde，MDA）水平显著升高（P<0.05）；相较于HELP组，不同剂量AEE组SOD、CAT、GSH活性显著增加，MDA水平显著减少（P<0.05），SOD和CAT mRNA转录显著升高（P<0.05）。相较于Control组，HELP组蛋鸡卵巢中抗氧化相关基因和蛋白，如核因子E2相关因子2（nuclear factor erythroid-2-related factor 2，Nrf2）、醌氧化还原酶1（NADPH：Quinone Oxidoreductase1，NQO1）、血红素加氧酶1（heme oxygenase-1，HO-1）表达显著降低，kelch样ECH关联蛋白1（kelch-like ECH-associated protein 1，Keap1）表达显著升高（P<0.05）；相较于HELP组，不同剂量AEE组Nrf2、NQO1、HO-1基因和蛋白表达显著升高，Keap1表达显著降低（P<0.05）。相较于Control组，HELP组蛋鸡卵巢中炎性因子白细胞介素1β（interleukin-1β，IL-1β）、白细胞介素6（interleukin-6，IL-6）、肿瘤坏死因子α（tumor necrosis factor-α，TNF-α）mRNA转录显著升高，炎症相关基因和蛋白（toll-like receptor 4，TLR4）、核因子κB（nuclear factor kappa B，NF-κB）、磷酸化p65（phosphorylated p65，p-p65）表达显著增加（P<0.05）；相较于HELP组，不同剂量AEE组IL-1β、IL-6、TNF-α、TLR4、NF-κB基因转录显著减少，p-p65蛋白表达显著降低（P<0.05）。综上，蛋鸡脂肪肝出血综合征可导致卵巢发生氧化应激和炎症反应；高能低蛋白日粮中添加不同剂量AEE对脂肪肝出血综合征蛋鸡卵巢损伤均有一定的预防效果。

阿司匹林丁香酚酯  /  蛋鸡脂肪肝出血综合征  /  卵巢  /  氧化应激  /  炎症

This study aimed to investigate preventive effects of aspirin eugenol ester （AEE） on oxidative stress and inflammatory response in the ovaries of hens with fatty liver hemorrhagic syndrome （FLHS）. A total of sixty-five 160-day-old Hy-Line Brown laying hens were randomly assigned to five groups， each containing 13 hens. The control group （Control） was fed a basal diet， while the model group （high-energy low-protein diet， HELP） and low-， medium-， and high-dose AEE treatment groups （AEE-L， AEE-M， AEE-H） were all fed a high-energy low-protein diet supplemented with 0， 25， 50， and 100 mg·kg-1 aspirin eugenol ester， respectively. The results showed that， compared with the control group， the ovaries of laying hens in the HELP group exhibited distinct lipid vacuoles of varying sizes. In contrast， the number of lipid vacuoles in the ovarian tissue was significantly reduced in the AEE-treated groups compared with the HELP group. Compared with the control group， the activities of SOD， GSH， and CAT in the ovaries of hens in the HELP group were significantly decreased， while the level of MDA was significantly increased （P<0.05）. In contrast， AEE treatment groups demonstrated significantly enhanced SOD， CAT， and GSH activities and reduced MDA levels and significantly upregulated SOD and CAT mRNA transcription compared with the HELP group （P<0.05）. Compared with the Control group， the expression levels of antioxidant-related genes and proteins Nrf2， NQO1， and HO-1 were significantly decreased in the ovaries of hens in the HELP group， while the expression of Keap1 was significantly increased （P<0.05）. In contrast， the AEE-treated groups showed significantly increased expression of Nrf2， NQO1， and HO-1 and decreased expression of Keap1 compared with the HELP group （P<0.05）. Compared with the control group， the mRNA transcription levels of inflammatory cytokines IL-1β， IL-6， and TNF-α were significantly increased in the ovaries of hens in the HELP group. In addition， the expression levels of inflammation-related genes and proteins-including TLR4， NF-κB， and p-p65 were also significantly elevated （P<0.05）. In contrast， AEE treatment groups exhibited significantly reduced expression of IL-1β， IL-6， TNF-α， TLR4 and NF-κB genes， along with significantly decreased p-p65 protein expression compared to the HELP group （P<0.05）. In summary， fatty liver hemorrhagic syndrome in laying hens can induce ovarian oxidative stress and inflammatory responses. Supplementation with varying doses of AEE demonstrated preventive effects against ovarian damage in laying hens with fatty liver hemorrhagic syndrome.

aspirin eugenol ester  /  fatty liver hemorrhagic syndrome in laying hens  /  ovary  /  oxidative stress  /  inflammation
葛闻博, 言凯, 杨亚军, 刘希望, 许笑, 李世宏, 白莉霞, 秦哲, 李准, 李剑勇. 阿司匹林丁香酚酯对脂肪肝出血综合征蛋鸡卵巢氧化应激和炎症反应预防作用. 畜牧兽医学报, 2026 , 57 (2) : 1099 -1109 . DOI: 10.11843/j.issn.0366-6964.2026.02.043
Wenbo GE, Kai YAN, Yajun YANG, Xiwang LIU, Xiao XU, Shihong LI, Lixia BAI, Zhe QIN, Zhun LI, Jianyong LI. Preventive Effects of Aspirin Eugenol Ester on Oxidative Stress and Inflammatory Response in the Ovaries of Hens with Fatty Liver Hemorrhagic Syndrome[J]. Acta Veterinaria et Zootechnica Sinica, 2026 , 57 (2) : 1099 -1109 . DOI: 10.11843/j.issn.0366-6964.2026.02.043
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蛋鸡脂肪肝出血综合征（FLHS）是笼养高产蛋鸡常见的营养代谢性疾病，其可由环境、遗传、激素、营养等因素诱发［1⁃2］。蛋鸡FLHS是一种多系统疾病综合征，可导致肝、卵巢、肾和肠道出血及脂质沉积，甚至引起蛋鸡死亡［3⁃4］。代谢紊乱、氧化应激和炎症反应可能是脂肪肝疾病的相关机制［4⁃5］。蛋鸡FLHS最显著的特征是产蛋率骤降和产蛋高峰期严重缩短，给蛋鸡养殖业造成巨大的经济损失［6］。研究表明，蛋鸡FLHS还会引发卵泡闭锁、卵巢氧化应激和炎症反应［5， 7⁃8］。卵巢是促进蛋鸡排卵产蛋的主要器官，其功能障碍会导致产蛋量和蛋品质显著下降［9⁃10］。因此，改善卵巢功能对维持蛋鸡生产性能具有积极意义。
当机体受到各种有害刺激时，活性氧（reactive oxygen species， ROS）和活性氮（reactive nitrogen species， RNS）生成增加，导致体内动态氧化还原平衡被破坏，这种失衡进而促进动脉粥样硬化、糖尿病、脂肪肝出血综合征等多种疾病的病理生理过程［11⁃13］。肝脏脂质合成与分泌的平衡是调控蛋鸡肝脏及肝外脂肪沉积的关键［14］。蛋鸡FLHS发生过程，脂肪沉积肝细胞内，尤其是含有大量易被氧化的脂肪酸，会生成大量ROS引起脂质过氧化反应［15］。肝细胞内产生的ROS可导致溶酶体释放，进而激活核因子κB（NF-κB）炎症通路，促进IL-1β、IL-6、TNF-α等炎症因子的转录，最终触发炎症反应［16］。
阿司匹林丁香酚酯（AEE）是利用结构拼合的孪药原理将阿司匹林与丁香酚进行酯化修饰而合成的一种新型药用化合物［17］；其具有抗氧化、抗炎、抗凋亡、降血脂等多种药理活性［18⁃20］。SOD、GSH、CAT作为三种重要的内源性自由基清除剂，在维持机体氧化与抗氧化平衡，保护细胞免受氧化损伤发挥关键作用。MDA是脂质过氧化产物，也是公认的氧化应激和抗氧化的标志物［21］。研究表明，阿司匹林通过提高SOD、GSH、CAT活性和降低MDA水平，改善脱氢表雄酮诱导的多囊卵巢综合征大鼠卵巢代谢［22］。AEE可改善蛋鸡FLHS的生产性能，并且显著提高FLHS蛋鸡肝脏的抗氧化能力。基于AEE的研究成果，推测AEE可能对FLHS蛋鸡卵巢氧化应激和炎症反应具有一定的调控作用。因此，本试验通过高能低蛋白日粮诱导蛋鸡FLHS的发生，研究在饲料中添加AEE颗粒剂对蛋鸡卵巢抗氧化能力及炎症反应的影响，旨在为将AEE开发成防治蛋鸡FLHS创新药物提供理论依据。
1　材料与方法
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1.1　试验材料
阿司匹林丁香酚酯（AEE）颗粒剂（含量99.8%，由中国农业科学院兰州畜牧与兽药研究所自制）；海兰褐蛋鸡（甘肃省兰州市皋兰吉祥村养殖场）；超氧化物歧化酶（SOD）、过氧化氢酶（CAT）、谷胱甘肽过氧化物酶（GSH）和丙二醛（MDA）ELISA检测试剂盒（上海酶联）；TRIzol Reagent和10%中性福尔马林（索莱宝）；PrimeScript RT Master Mix和TB Green Premix Ex Taq（宝生物工程）；BCA检测试剂盒和增强型ECL发光液（塞维尔）；一抗Anti-Nrf2、Anti-Keap1、Anti-NQO1、Anti-HO-1和Anti-β-actin（武汉三鹰）；一抗Anti-p-p65、Anti-p65（艾比玛特）；二抗HRP标记的山羊抗兔IgG（武汉三鹰）。
1.2　试验分组与饲养管理
选取65羽健康的160日龄海兰褐蛋鸡，随机分为5组，每组13羽。空白对照组（Control）饲喂基础日粮；模型组（HELP）和低、中、高剂量AEE给药组（AEE-L、AEE-M、AEE-H）均饲喂高能低蛋白日粮，根据体表面积换算，分别在高能低蛋白日粮中添加0、25、50、100 mg∙kg-1阿司匹林丁香酚酯颗粒剂。参照NRC（1994）蛋鸡营养需求及课题组前期研究配制基础日粮和高能低蛋白日粮［23］，基础日粮和高能低蛋白日粮组成及营养水平见表1。自由采食、饮水，每天给予光照16 h，按正常免疫程序免疫接种，预饲期7 d，试验期90 d。
1.3　检测指标和方法
1.3.1　卵巢组织采集
试验结束后，将试验鸡麻醉，通过颈动脉放血安乐死，剖开腹腔并快速取出整个卵巢组织，用预冷的PBS冲洗去除表面的血液。
1.3.2　样品处理及检测
取一部分卵巢组织置于10%中性福尔马林中固定，用于观察卵巢组织病理变化；另一部分卵巢组织立即存于液氮中速冻，之后-80 ℃保存，待用荧光定量PCR和相应试剂盒检测卵巢中超氧化物歧化酶（SOD）、过氧化氢酶（CAT）、谷胱甘肽过氧化物酶（GSH）和丙二醛（MDA）水平、抗氧化和炎症相关基因和蛋白表达。
1.4　组织病理学观察
将蛋鸡卵巢组织固定于10%中性福尔马林中24 h后，取出进行石蜡包埋并使用切片机切成5 μm切片，随后进行HE染色，在光学显微镜下观察卵巢组织的病理变化。
1.5　抗氧化指标检测
将冻存的卵巢组织取出，根据ELISA检测试剂盒说明书测定卵巢组织中SOD、CAT、GSH和MDA水平。
1.6　实施荧光定量PCR检测
为了检测蛋鸡卵巢中炎症相关基因（IL-1β、IL-6、TNF-α、NF-κB、TLR4）和抗氧化相关基因（SOD1、CAT、Nrf2、HO-1、Keap1、NQO1）的相对转录量。将冻存的卵巢组织取出，利用TRIzol法提取组织中的RNA，微量核酸定量仪检测RNA质量合格后，根据TaKaRa反转录试剂盒说明书将RNA反转录成cDNA。利用Primer5.0软件设计引物序列，引物序列见表2。随后按照反应体系加入96孔板后，低速离心。使用荧光定量PCR仪进行RT-qPCR检测，反应条件为95 ℃ 30 s，95 ℃ 5 s后，60 ℃ 30 s，循环40次，72 ℃ 10 s。按照公式2-ΔΔCt 计算目的基因的相对转录量，利用内参基因β-actin进行相对转录量分析，并进行统计学分析。
1.7　Western blot检测
将冻存的卵巢组织放在预冷的RIPA（含1 mmol∙L-1 PMSF）中，在组织匀浆仪上研磨5 min，随后放在4 ℃裂解30 min，在4 ℃以12 000 r∙min-1离心10 min，离心后吸取上清液。接着用BCA蛋白检测试剂盒检测蛋白浓度，根据检测的结果调整蛋白浓度并放置在金属浴中进行高温变性处理。按照等量的蛋白（30 μg）上样量进行SDS-PAGE凝胶电泳，随后在冰浴条件下转印至PVDF膜上，将膜放置在封闭液中，室温摇晃封闭1 h，与目的一抗（1∶1 000稀释）在4 ℃条件下孵育过夜。第二天在室温条件下与二抗羊抗兔IgG-HRP（1∶3 000稀释）进行孵育1 h，最后加入增强型ECL化学发光液，在曝光仪中显示拍照。
1.8　数据分析
数据采用SPSS Statistics 25.0软件进行统计分析，采用单因素方差分析（One-way ANOVA）和多重比较（LSD），分析数据的显著性。所有结果以“x±s”表示，P<0.05表示差异显著，P>0.05表示差异不显著，利用GraphPad Prism 9.1软件进行作图。
2　结果
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2.1　AEE对脂肪肝出血综合征蛋鸡卵巢病变的影响
由图1A~E可知，相较于对照组，模型组蛋鸡卵巢组织有较多的脂滴浸润；相较于模型组，不同剂量AEE组脂肪滴明显减少，其中AEE-H组优于AEE-M和AEE-L组。图1F显示，HELP组脂肪滴数量较对照组显著升高；与HELP组相比，不同剂量AEE组脂肪滴数量显著减少，AEE-H组优于AEE-L和AEE-M组。
2.2　AEE对脂肪肝出血综合征蛋鸡卵巢抗氧化酶活性的影响
由图2A~D可知，和对照组相比，模型组蛋鸡卵巢组织中SOD、CAT、GSH活性显著降低（P<0.05），MDA水平显著增加（P<0.05）；相较于模型组，AEE-L组SOD、CAT、GSH、MDA活性无显著变化（P>0.05），AEE-M和AEE-H组SOD、CAT、GSH活性显著增加（P<0.05），MDA水平显著降低（P<0.05）。
2.3　AEE对脂肪肝出血综合征蛋鸡卵巢抗氧化相关基因和蛋白表达的影响
由图3A~F可知，模型组蛋鸡卵巢组织中Nrf2和NQO1的mRNA转录量显著低于对照组（P<0.05），Keap1的mRNA转录量显著高于对照组（P<0.05），HO-1、SOD、CAT的mRNA转录量与对照组差异不显著（P>0.05）；AEE-L组Nrf2、HO-1、CAT的mRNA转录量与模型组差异不显著（P>0.05），AEE-M和AEE-H组Nrf2、HO-1、CAT的mRNA转录量显著高于模型组（P<0.05），AEE-L、AEE-M、AEE-H组NQO1和SOD的mRNA转录量显著高于模型组（P<0.05），Keap1的mRNA转录量显著低于模型组（P<0.05）。由图3G~K可知，和对照组相比，模型组Nrf2、NQO1、HO-1蛋白表达量显著降低（P<0.05），Keap1蛋白表达量显著升高（P<0.05）；相较于模型组，AEE-L组Nrf2、NQO1、HO-1蛋白表达量差异不显著（P>0.05），AEE-M和AEE-H组Nrf2、NQO1、HO-1蛋白表达量显著升高（P<0.05），AEE-L和AEE-H组Keap1蛋白表达量显著降低（P<0.05）。
2.4　AEE对脂肪肝出血综合征蛋鸡卵巢炎症相关基因和蛋白表达的影响
由图4A~E可知，与对照组相比，模型组蛋鸡卵巢组织中TLR4、NF-κB、IL-1β、IL-6、TNF-α的mRNA转录量显著增加（P<0.05）；与模型组相比，AEE-L、AEE-M、AEE-H组NF-κB和TNF-α的mRNA转录量显著降低（P<0.05），AEE-M、AEE-H组TLR4、IL-1β、IL-6的mRNA转录量显著降低（P<0.05），AEE-L组TLR4、IL-1β、IL-6的mRNA转录量差异不显著（P>0.05）。由图4F和G可知，相较于对照组，模型组p-p65蛋白表达量显著增加（P<0.05）；相较于模型组，AEE-L、AEE-M、AEE-H组p-p65蛋白表达量显著降低（P<0.05）。
3　讨论
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蛋鸡FLHS是一种与氧化应激相关的代谢障碍性疾病，可导致蛋鸡产蛋率和蛋品质下降，以及死淘率增加［5，24］。研究表明，外源性雌激素或高能低蛋白日粮（HELP）可诱发蛋鸡FLHS，不仅抑制生产性能，而且导致输卵管和卵巢快速退化［25］。本研究采用高能低蛋白日粮诱导蛋鸡发生脂肪肝出血综合征，该方法是建立蛋鸡FLHS模型的典型方案。本研究发现，与对照组相比，HELP组的产蛋率显著降低，卵巢组织出现脂肪变性这与前人研究结果一致［5，26⁃27］，表明蛋鸡FLHS模型成功建立。本研究进一步证实，AEE颗粒剂能够改善卵巢脂肪变性。
蛋鸡FLHS与氧化应激和炎症密切相关，可导致卵巢功能障碍并引发生殖机能衰退［5，10，28］。研究表明，抗氧化剂能改善蛋鸡产蛋性能与卵巢功能［5，10，29］。本试验结果显示，高能低蛋白饲喂组蛋鸡卵巢中SOD、CAT、GSH活性显著降低，MDA含量显著升高，IL-1β、TNF-α和IL-6的mRNA转录显著升高，表明饲喂高能低蛋白日粮可导致蛋鸡卵巢氧化应激和炎症反应加剧，该结果与Xing等［5］的研究结果一致。前期研究表明，AEE在体内外均具有明显的抗氧化活性和预防炎症相关代谢疾病作用［17，20，30］。AEE通过提高大鼠BRL-3A细胞和肝脏中SOD、GSH、CAT活性并降低MDA含量，从而缓解百草枯诱导的氧化损伤［31］。李剑勇等［32］发现，AEE可降低D-半乳糖诱导的衰老小鼠血清和肝脏MDA水平。本研究中，AEE通过上调SOD、CAT、GSH活性及下调MDA水平来增强卵巢抗氧化能力，以及AEE能显著抑制炎症相关基因的表达，这与前人研究结果［33］类似，表明AEE可有效缓解高能低蛋白日粮导致的蛋鸡卵巢氧化和炎症损伤。
作为抗氧化反应的关键调控因子，Nrf2可通过介导下游抗氧化酶活性抵御氧化应激，在氧化损伤中具有重要作用［16］。正常情况下，Nrf2与Keap1结合，在氧化应激状态时与Keap1解离，进而调控NQO1、HO-1等下游因子的表达［28，34⁃35］。Toll样受体4在炎症反应中起关键作用，其信号激活可触发NF-κB信号通路活化［36］。NF-κB被激活，诱导炎症因子IL-1β、TNF-α和IL-6的表达，这些因子在脂肪肝损伤中发挥关键作用［37⁃38］。研究表明，AEE可通过激活Nrf2信号通路缓解氧化应激并增强抗氧化能力［20］。为此，本研究检测了FLHS蛋鸡卵巢Nrf2通路相关因子的表达。结果显示，AEE显著促进Nrf2、HO-1、NQO1、SOD、CAT mRNA转录和抑制Keap1基因转录，蛋白结果和基因表达结果类似。此外，本研究发现，HELP组蛋鸡卵巢中TLR4基因和p-p65蛋白表达升高，表明NF-κB信号通路被激活。该结果与前人研究FLHS蛋鸡卵巢炎症的结果一致［5，10，33］。以上结果表明AEE可能通过激活Nrf2通路或抑制NF-κB通路提高抗氧化酶活性及抑制炎症基因表达，从而缓解FLHS蛋鸡卵巢氧化损伤和炎症反应。
综上所述，通过饲喂高能低蛋白日粮导致蛋鸡FLHS，引起卵巢损伤；AEE颗粒剂可有效缓解FLHS蛋鸡卵巢损伤。
4　结论
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饲喂HELP日粮会引起蛋鸡FLHS，导致卵巢氧化应激和炎症反应；AEE颗粒剂可显著提高卵巢抗氧化能力和抑制炎症反应。本研究结果为将AEE开发成兽医临床防治蛋鸡FLHS的新型药物奠定基础。
基金
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  • 甘肃省科技计划资助(25ZDNA003)
  • 甘肃省科技计划资助(25JRRA456)
  • 国家自然科学基金青年基金(32402950)
  • 兰州市青年科技人才创新项目(2024-QN-54)
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2026年第57卷第2期
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doi: 10.11843/j.issn.0366-6964.2026.02.043
  • 接收时间：2025-04-30
  • 首发时间：2026-09-16
  • 出版时间：2026-02-23
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  • 收稿日期：2025-04-30
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甘肃省科技计划资助(25ZDNA003)
甘肃省科技计划资助(25JRRA456)
国家自然科学基金青年基金(32402950)
兰州市青年科技人才创新项目(2024-QN-54)
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    中国农业科学院兰州畜牧与兽药研究所 农业农村部兽用药物创制重点实验室/甘肃省新兽药工程重点实验室，兰州 730050

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李剑勇，主要从事药理毒理学研究，E-mail：
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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