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Article(id=1208862372844933545, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208862365714616539, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2021.09.03, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1616342400000, receivedDateStr=2021-03-22, revisedDate=1623945600000, revisedDateStr=2021-06-18, acceptedDate=null, acceptedDateStr=null, onlineDate=1766144849263, onlineDateStr=2025-12-19, pubDate=1632758400000, pubDateStr=2021-09-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1766144849263, onlineIssueDateStr=2025-12-19, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1766144849263, creator=13701087609, updateTime=1766144849263, updator=13701087609, issue=Issue{id=1208862365714616539, tenantId=1146029695717560320, journalId=1189873630562394117, year='2021', volume='46', issue='9', pageStart='849', pageEnd='953', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1766144847562, creator=13701087609, updateTime=1766144914151, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1208862645055254758, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208862365714616539, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1208862645055254759, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208862365714616539, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=860, endPage=864, ext={EN=ArticleExt(id=1208862373948035518, articleId=1208862372844933545, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Research progress of intestinal flora and hepatic encephalopathy, columnId=1208862370294788358, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Special Issues on Intestinal Flora and Disease Progression, runingTitle=null, highlight=null, articleAbstract=

Hepatic encephalopathy (HE) is a common clinical end-stage liver disease complicated with a complex neuropsychiatric syndrome, the occurrence of HE often suggests a poor outcome in patients with liver disease. The pathological mechanism involved in HE is complex, and the exact mechanism remains unclear. In recent years, with the continuous in-depth studies on the intestinal flora of patients with cirrhosis, the correlation between intestinal flora changes and HE occurrence has become the focus of attention. At present, the treatment of HE by regulating intestinal flora imbalance has achieved certain efficacy.Therefore, the relationship between intestinal flora and HE, as well as the treatment measures for HE are reviewed, aiming to provide new ideas for further exploring the pathogenesis of HE and new theoretical basis for clinical treatment of HE.

, correspAuthors=Hui-Fang Huang, authorNote=null, correspAuthorsNote=
*E-mail:
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肝性脑病(HE)是临床上终末期肝病并发的一种常见的、复杂的神经精神综合征。HE的出现往往提示肝病患者结局较差。HE涉及的病理机制复杂，确切的机制尚不明确。近年来，随着对肝硬化患者肠道菌群的深入研究，肠道菌群改变与HE发生的相关性已成为临床关注的焦点。目前通过调节肠道菌群治疗HE已取得一定疗效。该文就肠道菌群与HE的关系，以及采用微生态制剂、乳果糖、抗生素、菌群移植等治疗HE的研究进展进行综述，旨在为进一步探索HE的发病机制提供新思路，为临床治疗HE提供新的理论依据。

, correspAuthors=黄会芳, authorNote=null, correspAuthorsNote=
黄会芳，E-mail：
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李变玲，研究生，主要从事慢性肝病诊治方面的研究

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李变玲，研究生，主要从事慢性肝病诊治方面的研究

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李变玲，研究生，主要从事慢性肝病诊治方面的研究

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journalId=1189873630562394117, articleId=1208862372844933545, language=CN, orderNo=1, keyword=肝性脑病), Keyword(id=1208862377001489017, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208862372844933545, language=CN, orderNo=2, keyword=肠道菌群), Keyword(id=1208862378175894139, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208862372844933545, language=CN, orderNo=3, keyword=研究进展)], refs=[Reference(id=1208862378268168834, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208862372844933545, doi=null, pmid=null, pmcid=null, year=2020, volume=25, issue=2, pageStart=116, pageEnd=120, url=null, language=null, rfNumber=[1], rfOrder=0, authorNames=Li MY, Zhou XQ, journalName=Chin J Gastroenterol, refType=null, unstructuredReference=Li MY, Zhou XQ. 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肠道菌群与肝性脑病的关系及其治疗措施研究进展
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李变玲 1 , 黄会芳 2, * , 王晓阳 1 , 严微 1
解放军医学杂志 | 肠道菌群与疾病的关系研究进展专题 2021,46(9): 860-864
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解放军医学杂志 | 肠道菌群与疾病的关系研究进展专题 2021, 46(9): 860-864
肠道菌群与肝性脑病的关系及其治疗措施研究进展
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李变玲1, 黄会芳2, * , 王晓阳1, 严微1
作者信息
  • 1山西医科大学第一临床医学院，太原 030001
  • 2山西医科大学第一医院消化内科，太原 030001

    • 李变玲，研究生，主要从事慢性肝病诊治方面的研究

通讯作者:

黄会芳，E-mail：
Research progress of intestinal flora and hepatic encephalopathy
Bian-Ling Li1, Hui-Fang Huang2, * , Xiao-Yang Wang1, Wei Yan1
Affiliations
  • 1the First Clinical Medical College of Shanxi Medical University, Taiyuan 030001, China
  • 2Department of Gastroenterology, the First Hospital of Shanxi Medical University, Taiyuan 030001, China
出版时间: 2021-09-28 doi: 10.11855/j.issn.0577-7402.2021.09.03
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摘要
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肝性脑病(HE)是临床上终末期肝病并发的一种常见的、复杂的神经精神综合征。HE的出现往往提示肝病患者结局较差。HE涉及的病理机制复杂，确切的机制尚不明确。近年来，随着对肝硬化患者肠道菌群的深入研究，肠道菌群改变与HE发生的相关性已成为临床关注的焦点。目前通过调节肠道菌群治疗HE已取得一定疗效。该文就肠道菌群与HE的关系，以及采用微生态制剂、乳果糖、抗生素、菌群移植等治疗HE的研究进展进行综述，旨在为进一步探索HE的发病机制提供新思路，为临床治疗HE提供新的理论依据。

肝性脑病  /  肠道菌群  /  研究进展

Hepatic encephalopathy (HE) is a common clinical end-stage liver disease complicated with a complex neuropsychiatric syndrome, the occurrence of HE often suggests a poor outcome in patients with liver disease. The pathological mechanism involved in HE is complex, and the exact mechanism remains unclear. In recent years, with the continuous in-depth studies on the intestinal flora of patients with cirrhosis, the correlation between intestinal flora changes and HE occurrence has become the focus of attention. At present, the treatment of HE by regulating intestinal flora imbalance has achieved certain efficacy.Therefore, the relationship between intestinal flora and HE, as well as the treatment measures for HE are reviewed, aiming to provide new ideas for further exploring the pathogenesis of HE and new theoretical basis for clinical treatment of HE.

hepatic encephalopathy  /  intestinal flora  /  research progress
李变玲, 黄会芳, 王晓阳, 严微. 肠道菌群与肝性脑病的关系及其治疗措施研究进展. 解放军医学杂志, 2021 , 46 (9) : 860 -864 . DOI: 10.11855/j.issn.0577-7402.2021.09.03
Bian-Ling Li, Hui-Fang Huang, Xiao-Yang Wang, Wei Yan. Research progress of intestinal flora and hepatic encephalopathy[J]. Medical Journal of Chinese People’s Liberation Army, 2021 , 46 (9) : 860 -864 . DOI: 10.11855/j.issn.0577-7402.2021.09.03
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肝性脑病(hepatic encephalopathy，HE)是各种急、慢性肝病患者终末期的急危重症，其发生往往提示预后较差，是导致肝病患者死亡的重要原因。HE涉及的病理机制较为复杂，确切的机制仍不明确。近半个世纪以来，人们一直认为高氨血症是HE发病的最重要机制[1]。但近年来随着微生态学研究的深入，已证实在肠黏膜屏障功能减退及免疫功能障碍的前提下，肠道菌群失调可促进或加剧HE的发展[2]。既往针对HE的治疗，临床多推荐应用乳果糖、利福昔明等降低血氨水平[3]。目前基于肠道菌群失调的治疗在改善HE预后、减轻并发症等方面也发挥了不可或缺的作用[4-6]。本文就HE与肠道菌群的关系，以及对HE的治疗措施进行综述。
1 肠道菌群与HE的关系
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1.1 HE概述
HE是各种急、慢性肝病和(或)门体静脉分流引发的一系列循序性进展的神经精神异常的临床症候群。目前的流行病学数据分析提示，肝硬化是HE的主要病因，30%~45%的肝硬化患者会并发HE[7]。HE患者可进行性地出现一系列以神经认知症状为主的异常变化，从行为的细微变化、运动障碍、睡眠障碍、嗜睡、定向障碍，到最终的深度昏迷。West-Haven HE分级标准将HE分为0~4级。也有专家认为，0级轻微肝性脑病(minimal hepatic encephalopathy，MHE)及1级HE应统称为隐匿性HE；出现不同程度精神异常及神经异常的2~4级HE应统称为显性HE(overt hepatic encephalopathy，OHE)[8]。有研究报道，慢性肝病患者进展为HE者，其1年内生存率小于50%，3年病死率高达75%以上[9]。MHE在肝硬化患者中的发生率为30%~84%[10]。MHE发生率差异大的原因可能是各项研究选取的诊断标准不一，患者年龄、受教育程度、酒精性肝病等影响了智力测验结果，还可能与MHE患者临床症状隐匿、临床医师不够重视有关[11-12]。
1.2 HE患者肠道微生物分布特征
肠道内微生物在各种不利因素的影响下，有利菌群、条件致病菌及有害菌在数量、种类、比例及生物活性等方面发生变化，称为肠道菌群失调，发生率高达2%~3%[13]。Chen等[14]率先使用焦磷酸测序16S rRNA V3区域及实时定量聚合酶链反应(PCR)来鉴定肝硬化患者的粪便微生物群，结果发现与健康人相比，肝硬化患者的粪便微生物多样性发生了明显变化，主要表现为：在门水平上，肝硬化患者拟杆菌门的相对丰度明显降低(47.0% vs. 59.9%，P=0.008)，而变形杆菌及梭杆菌门则高度富集(9.5% vs. 2.8%，2.8% vs. 0.2%，P<0.01)；在科水平上，肝硬化患者的肠杆菌科、巴氏杆菌科、梭菌科也呈现出明显的富集趋势(6.2% vs. 1.2%，1.7% vs. 0.1%，2.7% vs.0.2%，P<0.01)；在属水平上，杆菌属在肝硬化患者中占据了主要优势(7.7% vs. 1.9%，P=0.001)；表明肝硬化患者粪便微生物中潜在致病菌逐渐占据优势，而正常的肠道有益菌明显减少，可能会影响肝硬化患者的预后。Sarangi等[15]研究发现，肝硬化患者肠道菌群中拟杆菌、变形杆菌的丰度增加且存在聚集现象，而厚壁菌门、黏胶球形菌门丰度呈下降趋势，与健康组相比有明显差异。Zhang等[16]研究发现，与对照组相比，在合并与不合并MHE的肝硬化患者中，肠道菌群中的链球菌科、韦荣氏菌科等潜在致病菌有过度富集的趋势；该研究还在肝硬化患者的肠道菌群中检测到唾液链球菌，且合并MHE的肝硬化患者唾液链球菌的丰度明显高于不合并MHE的肝硬化患者，同时唾液链球菌计数与MHE患者的血氨水平呈正相关。
1.3 肠道菌群代谢产物与HE发病机制的关系
近年来大量研究发现，肠道菌群代谢产物(氨、短链脂肪酸、胆汁酸等)通过肠-脑轴双向通路在HE发展中起着至关重要的作用。近一个世纪以来，国内外学者们一致认为血氨水平升高对大脑的不良反应是HE的发病机制。高氨血症主要是由肠道中产脲酶的革兰阴性杆菌或厌氧菌分解胺、氨基酸、嘌呤及尿素所致。Wang等[17]研究发现，MHE患者肠道中的链球菌及韦荣氏球菌增加，且它们的脲酶活性增强，促使高氨血症形成。此外，由于HE患者肝脏功能受损，对门静脉中血氨、内毒素等有毒物质的清除能力下降，在血脑屏障功能减退的情况下，大量氨弥散进入中枢神经系统，与谷氨酸结合生成谷氨酰胺，阻断神经结构之间的传导，影响神经元的正常生理功能；同时，升高的血氨可抑制神经胶质细胞内酶的活性及功能，增加血脑屏障的通透性，进一步形成恶性循环，从而导致异常的神经精神行为[18-20]。
肠道菌群可降解膳食纤维，产生乙酸、丙酸、丁酸等短链脂肪酸(short chain fatty acids，SCFA)[21]，其中丁酸作为结肠细胞的能源物质被局部消耗，而其他被吸收的SCFA排入门静脉，因为丙酸在肝脏中代谢，因此只在外周循环中以低浓度存在，从而使得乙酸成为外周循环中含量最丰富的SCFA，它们可以通过血脑屏障调节大脑发育及神经递质合成，从而影响小胶质细胞的成熟及功能[22-23]。肠道产生的大量SCFA作为游离脂肪酸受体(FFAR)2及FFAR3的激动剂，与同源自由脂肪酸受体结合，从而调节神经元的生理功能[24]。Frost等[25]研究发现，乙酸可以穿过血脑屏障，触发胰高血糖素样肽-1(GLP-1)、肽YY(PYY)和其他肠道激素的产生及释放，从而刺激宿主产生饱腹感以降低食欲。SCFA中的丁酸可上调肠黏膜屏障中紧密连接蛋白的表达，包括claudin-2、occludin、cinglin以及zonula occludens (ZO)-1、ZO-2蛋白，还可促进转录因子与claudin-1启动子之间的联系，增加腺嘌呤核糖核苷酸(AMP)激活的蛋白激酶(AMPK)活性，减少了细菌易位[26]。采用16S rRNA测序技术对小鼠肠道菌群进行研究发现，结肠中能产生大量SCFA的毛螺菌科及瘤胃球菌科呈现富集状态[27]。多不饱和脂肪酸是大脑的重要组成部分，影响大脑的发育和神经传递。多不饱和脂肪酸可调节肠道菌群，而一些乳酸杆菌及双歧杆菌等肠道有益菌也能影响大脑多不饱和脂肪酸的含量，从而影响大脑及行为。在HE发病过程中常存在门静脉高压，从而使肠道长期处于淤血状态，产生SCFA的菌群丰度减少，细胞间的紧密连接受到影响，肠道通透性增加，导致肠道中的致病菌移位及大量代谢产物进入中枢神经系统，诱导神经元凋亡、小胶质细胞功能障碍，最终导致记忆力下降、行为异常及运动障碍[28-29]。Ahluwalia等[30]通过多模式脑磁共振波谱法(MRS)评定肠道内的特定细菌对脑功能星形胶质细胞及神经细胞的影响，发现与健康人及无HE的肝硬化患者相比，合并HE的肝硬化患者葡萄球菌科、肠球菌科、卟啉单胞菌科及乳酸菌科的丰度较高，而螺菌科及瘤胃菌科的丰度较低。但肠道菌群来源的单链脂肪酸与HE发病机制的关系尚需进一步研究。
众所周知，胆汁酸是人体胆汁的主要成分，进入肠道中的初级胆汁酸需在肠道菌群参与下转变为次级胆汁酸[31]，同时，胆汁酸池的组成变化对肠道菌群的分布也有一定影响。胆汁酸也是人体重要的信号分子，进入神经系统中的胆汁酸可以通过法尼类X受体(farnesoid X receptor，FXR)、鞘氨醇-1-磷酸受体(sphingosine-1-phosphate receptor，S1PR)参与HE的病理生理过程[32]。在HE疾病状态下，胆汁酸中的疏水性胆汁酸及其缀合物通过氧化应激导致肝细胞损伤，并跨越血脑屏障，激活FXR，导致神经功能障碍[33-34]。此外，胆汁酸也可通过S1PR2信号通路影响中枢神经元及小胶质细胞的功能，进而促进HE的发生[35]。
2 HE的治疗措施
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2.1 微生态制剂
微生态制剂是基于微生态学原理人工合成的用于调节肠道菌群失调的一类特殊制剂。合理剂量的微生态制剂可以调整宿主肠道微生物的数量及其菌群丰度，调节肠道内菌群的平衡，恢复正常的肠道屏障功能与防御能力。在临床工作中，广泛应用的微生态制剂主要包括以下3类：为肠道提供有益菌的益生菌、提供有益菌生长代谢所需营养物质的益生元以及两者结合的合生元。
益生菌通过活性细菌的直接作用来改善肠道菌群的结构而发挥疗效，是临床实践中应用最多的微生态制剂。益生菌可以通过增加有益菌的丰度及数量恢复肠道菌群平衡。Liu等[36]通过对MHE患者粪便样品进行定量细菌学分析发现，MHE患者的肠道菌群严重紊乱，表现为潜在致病性大肠埃希菌及葡萄球菌大量繁殖，予以益生菌治疗1个月后，这两种过度生长菌群的活菌数量显著减少，降至健康对照组水平，同时产生非脲酶的乳酸杆菌的数量显著增加。Marlicz等[37]研究发现，应用益生菌治疗后，HE患者肠道菌群中的有益菌乳酸杆菌丰度增加，而机会致病菌肠杆菌科的比例有所下降，且血氨水平及OHE的发生率均显著降低。近期Xia等[38]发表的一篇临床随机对照试验通过定量PCR检测了MHE患者粪便菌群的情况，证实益生菌治疗组患者肠道内梭状芽孢杆菌属、双歧杆菌属等有益菌增加，而肠球菌属、肠杆菌科等机会致病菌显著减少，提示益生菌可通过改善肠黏膜的超微结构及通透性来减少细菌易位，进而恢复肠黏膜的屏障能力。Xia等[38]通过对67例乙型肝炎病毒(hepatitis B virus，HBV)引起的肝硬化伴发MHE患者进行研究发现，经过益生菌治疗3个月后，治疗组患者的内毒素水平显著低于对照组[(0.27±0.16) EU/ml vs.(1.38±0.32) EU/ml，P=0.002]，D-乳酸盐水平也低于对照组[(5.38±1.23) mg/ml vs. (25.76±6.14) mg/ml，P=0.014]，表明益生菌可以改善MHE患者肠黏膜的通透性，此外，二胺氧化酶水平明显降低[(1.84±0.46) U/ml vs. (7.35±1.29) U/ml，P<0.001]，表明益生菌可以恢复MHE患者的肠黏膜屏障。国内外大量研究证实，益生菌可以降低HE患者的血氨水平，改善肝功能储备及预后。罗兰等[39]对109例肝硬化MHE患者以枯草杆菌二联活菌肠溶胶囊治疗1个月后发现，益生菌能降低HE患者的血氨水平，改善Child-Pugh评分及终末期肝病模型(model of end-stage liver disease，MELD)评分，延缓HE的进展速度。Cao等[40]开展的meta分析也证实，益生菌可降低MHE患者数字连接试验A(number connection test-A，NCT-A)的评分及血氨水平。Zuo等[41]利用宏基因组学方法对MHE患者进行研究发现，益生菌可降低梭杆菌及链球菌的丰度，有效提高双歧杆菌、乳酸菌、毛螺菌及瘤胃球菌等有益菌的丰度，同时血清内毒素、D-乳酸、血二胺氧化酶水平均下降。
2.2 乳果糖
乳果糖是一种人工合成的不被小肠吸收的双糖，可通过酸化结肠腔并缩短胃肠道转运时间来有效减少肠道中氨的合成与吸收。长期以来，人们一直认为乳果糖是临床上降低血氨的主要药物。Moratalla等[6]研究发现，乳果糖可以通过控制细菌DNA易位来降低细菌移位水平，提高MHE患者的神经认知评分。Qin等[42]研究证实，接受乳果糖治疗的HE患者终止服用乳果糖后，对其粪便菌群进行分析发现，仅有普拉梭菌属减少，其余菌群成分无显著变化，由此可见，乳果糖的主要功能是改变肠道菌群。Bajaj等[43]研究发现，中途中断乳果糖治疗2、14及30 d后，HE复发患者的肠道菌群丰度发生改变，胆碱代谢紊乱，主要表现为尿氧化三甲胺水平下降，甘氨酸、血清胆碱、二甲基甘氨酸、肌酐水平升高。然而，乳果糖治疗出现的不良反应，包括抽筋、腹泻及胃肠胀气等，导致患者对该治疗的依从性较差，过量服用还可能导致严重的腹泻、电解质紊乱及低血容量，甚至引发HE症状[44]。尽管这些双糖在过去的几年里有很大的用处，但目前对于这一适应证的真正疗效还存在质疑。
2.3 抗生素
利福昔明是一种在利福霉素的结构上增加了吡啶环合成的非氨基糖苷类的衍生物，其吸收率低，很难通过胃肠道进入循环血液，从而可抑制肠道内的机会致病菌过度生长，减少产氨细菌的丰度，进而降低血氨浓度，有利于缓解HE症状。目前指南多推荐利福昔明联合乳果糖治疗HE[3]。Suzuki等[45]通过回顾性研究发现，接受利福昔明治疗4周后，HE患者的血氨水平显著低于治疗前(8.6 μg/L vs. 15.7 μg/L，P<0.01)，且持续时间延长，可见长期应用利福昔明可明显改善HE。Bruyneel等[46]对15例肝硬化复发的HE患者进行研究发现，利福昔明不仅可显著降低复发HE患者的Child-Pugh评分，还可改善其认知能力与客观睡眠结构。目前利福昔明的不良反应尚未明确，仍需临床研究进一步论证。
2.4 菌群移植
近年来，采用菌群移植这一新型的微生物靶向疗法治疗HE已取得初步进展。利用菌群移植可逆转肠道微生态失调，增强肠道黏膜屏障功能[47]。Bajaj等[48]对20例门诊肝硬化复发HE患者的一项随机对照试验发现，与标准治疗组(乳果糖联合利福昔明)相比，菌群移植组HE患者的认知功能明显改善，而住院率、病死率及感染发生率等明显降低，此外，该研究还发现菌群移植增加了肠道有益菌群的丰度。也有研究证实OHE患者应用菌群移植治疗后，其血氨水平、Child-Pugh评分及MELD显著降低[49]。但是目前移植菌群的选择、储存及给药途径等尚未标准化，限制了该靶向治疗方式的临床应用及推广。
3 总结与展望
收起
各种终末期肝病可影响肠道内菌群的比例，进而促进HE的发生发展。肠道内有益菌、机会致病菌丰度及数量的改变，通过直接或间接的作用引发高氨血症及内毒素血症，导致脑细胞的代谢及传导障碍，进而出现中枢神经功能紊乱的症状。作为以肠道菌群为靶点的治疗方式，菌群移植有望成为治疗HE的新手段。在未来的研究中，应通过多基因组学方法系统性地分析肠道菌群功能与HE患者的相互作用，寻找参与HE发生发展的关键性菌群及其功能，并进一步探索肠道菌群失调与HE的具体发病机制，以期为临床治疗HE提供新的理论依据。
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2021年第46卷第9期
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doi: 10.11855/j.issn.0577-7402.2021.09.03
  • 接收时间：2021-03-22
  • 首发时间：2025-12-19
  • 出版时间：2021-09-28
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  • 收稿日期：2021-03-22
  • 修回日期：2021-06-18
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    1山西医科大学第一临床医学院，太原 030001
    2山西医科大学第一医院消化内科，太原 030001

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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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