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Article(id=1199337300208484764, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199337298941804946, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2625.2023.0330, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1671465600000, receivedDateStr=2022-12-20, revisedDate=null, revisedDateStr=null, acceptedDate=1677945600000, acceptedDateStr=2023-03-05, onlineDate=1763873894979, onlineDateStr=2025-11-23, pubDate=1706371200000, pubDateStr=2024-01-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1763873894979, onlineIssueDateStr=2025-11-23, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1763873894979, creator=13701087609, updateTime=1763873894979, updator=13701087609, issue=Issue{id=1199337298941804946, tenantId=1146029695717560320, journalId=1189873630562394117, year='2024', volume='49', issue='1', pageStart='1', pageEnd='120', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1763873894677, creator=13701087609, updateTime=1763874094669, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1199338137823572576, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199337298941804946, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1199338137823572577, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199337298941804946, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=23, endPage=30, ext={EN=ArticleExt(id=1199337300929905063, articleId=1199337300208484764, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Clinical characteristics and prognostic factors of young patients with sporadic rectal cancer liver metastasis, columnId=1199337300007158168, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Special Issue on Rectal Cancer Surgery and Perioperative Treatment Strategies, runingTitle=null, highlight=null, articleAbstract=

Objective To identify the clinical characteristics and prognostic factors of young patients with sporadic rectal cancer liver metastasis (RCLM). Methods The clinical data of young RCLM patients at 45 years or under (n=40, as younger patient group) in Peking University First Hospital from January 2016 to January 2021 were reviewed, meanwhile, elder RCLM patient group were comprised of 82 patients older than 45-year-old in a 1:2 ratio. Proportions of categorical variables were compared between young patients and old patients. The clinicopathologic parameters were analyzed with univariate and multivariate Cox regression models and Kaplan-Meier method for demonstrating survival differences between the maximum diameter of liver metastasis and local therapy. Results One hundred and twenty-two RCLM patients were identified, the 1-, 3- and 5-year survival rates of young patient group were 97.5%, 47.5%, 15.0%, those of elder patient group were 84.1%, 26.8%, 9.8%, respectively. The differences in BMI (P=0.008), primary tumor with obstruction and bleeding (P=0.006), synchronous rectal cancer liver metastases (P=0.005), the maximum diameter of liver metastasis >3 cm (P=0.019) were statistically significant between the two groups. And univariate and multivariate analyses showed that age (P=0.003), N stage (P=0.007), local therapy for liver metastases (P=0.047) and the maximum diameter of liver metastasis (P=0.030) were independent risk factors for influencing the prognosis of RCLM patients; curative resection or not of primary tumor (P=0.035) and the maximum diameter of liver metastasis (P=0.041) were independent risk factors for influencing the prognosis of young RCLM patients. Kaplan-Maier curve demonstrated survival differences between the maximum diameter of liver metastasis and local therapy for liver metastasis in RCLM patients (log-rank P=0.000). Conclusions Although with later staging of initial tumor station, young RCLM patients may obtain better survival benefit compared with old patients. Higher degree of lymph node metastasis, local therapy for liver metastases and the maximum diameter of liver metastasis >3 cm indicates poor prognosis in RCLM patients, and without curative resection of primary tumor and maximum diameter of liver metastasis are also considered as the independent poor prognostic factors of young RCLM patients. Local therapy for liver metastases appears to play an important role in the treatment strategy of RCLM patients.

, correspAuthors=Zhan-Bing Liu, authorNote=null, correspAuthorsNote=
E-mail:
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目的 探讨散发性青年直肠癌肝转移(RCLM)患者的临床特点及其预后影响因素。方法 回顾性分析2016年1月-2021年1月北京大学第一医院收治的青年RCLM患者(发病年龄≤45岁)的临床病理资料(设为青年组，n=40)，并按照1∶2的比例纳入中老年RCLM患者(发病年龄>45岁，设为中老年组，n=82)。比较两组临床病理因素的差异性，采用单因素及多因素Cox回归分析影响RCLM及青年RCLM患者预后的危险因素，结合Kaplan-Meier生存曲线分析肝转移瘤直径与局部治疗之间的预后关系。结果 共纳入RCLM患者122例，青年组1、3、5年生存率分别为97.5%、47.5%、15.0%，中老年组1、3、5生存率分别为84.1%、26.8%、9.8%。两组BMI(P=0.008)、原发肿瘤存在并发症情况(P=0.006)、肝转移发生时限中同时性肝转移(P=0.005)、肝转移瘤最大直径>3 cm(P=0.019)差异有统计学意义。单因素及多因素Cox回归分析显示，年龄(P=0.003)、原发肿瘤N分期(P=0.007)、肝转移瘤局部治疗(P=0.047)和肝转移瘤最大直径(P=0.030)是影响RCLM患者预后的独立危险因素，原发肿瘤是否根治性切除(P=0.035)和肝转移瘤最大直径(P=0.041)是影响青年RCLM患者预后的独立危险因素。肝转移瘤最大直径与肝转移瘤局部治疗组间生存期差异有统计学意义(log-rank P=0.000)。结论 青年RCLM患者肿瘤初始分期较晚，但生存预后优于中老年RCLM患者。淋巴结转移程度高、肝转移瘤未经局部治疗以及肝转移瘤最大直径>3 cm提示RCLM患者预后不良。原发肿瘤根治性切除及肝转移瘤最大直径是影响青年RCLM患者预后的独立危险因素，肝转移瘤局部治疗在RLCM患者治疗策略中起重要作用。

, correspAuthors=刘占兵, authorNote=null, correspAuthorsNote=
刘占兵，E-mail：
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关宇，博士研究生，主治医师，主要从事胃肠、肝胆良恶性疾病外科治疗方面的研究

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关宇，博士研究生，主治医师，主要从事胃肠、肝胆良恶性疾病外科治疗方面的研究

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关宇，博士研究生，主治医师，主要从事胃肠、肝胆良恶性疾病外科治疗方面的研究

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Front Oncol, 2021, 11: 719638., articleTitle=Development and validation of a predictive scoring system for colorectal cancer patients with liver metastasis: a population-based study, refAbstract=null), Reference(id=1199376222166811156, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, doi=null, pmid=null, pmcid=null, year=2019, volume=29, issue=null, pageStart=102, pageEnd=106, url=null, language=null, rfNumber=[24], rfOrder=23, authorNames=Afshari K, Chabok A, Naredi P, journalName=Surg Oncol, refType=null, unstructuredReference=Afshari K, Chabok A, Naredi P, et al. Prognostic factors for survival in stage IV rectal cancer: a Swedish nationwide case-control study[J]. Surg Oncol, 2019, 29: 102-106., articleTitle=Prognostic factors for survival in stage IV rectal cancer: a Swedish nationwide case-control study, refAbstract=null), Reference(id=1199376222259085846, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, doi=null, pmid=null, pmcid=null, year=2021, volume=47, issue=9, pageStart=2377, pageEnd=2383, url=null, language=null, rfNumber=[25], rfOrder=24, authorNames=Mariathasan AB, Boye K, Dueland S, journalName=Eur J Surg Oncol, refType=null, unstructuredReference=Mariathasan AB, Boye K, Dueland S, et al. Metastases in locally advanced rectal cancer undergoing curatively intended treatment[J]. Eur J Surg Oncol, 2021, 47(9): 2377-2383., articleTitle=Metastases in locally advanced rectal cancer undergoing curatively intended treatment, refAbstract=null), Reference(id=1199376222355554839, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, doi=null, pmid=null, pmcid=null, year=2022, volume=11, issue=1, pageStart=171, pageEnd=180, url=null, language=null, rfNumber=[26], rfOrder=25, authorNames=Chen J, Chen H, Zhao F, journalName=Transl Cancer Res, refType=null, unstructuredReference=Chen J, Chen H, Zhao F, et al. Survival outcomes in unresectable metastatic rectal cancer patients after both primary site resection and chemoradiotherapy: a SEER-based observational study[J]. Transl Cancer Res, 2022, 11(1): 171-180., articleTitle=Survival outcomes in unresectable metastatic rectal cancer patients after both primary site resection and chemoradiotherapy: a SEER-based observational study, refAbstract=null)], funds=[Fund(id=1199376219725726162, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, awardId=81902384, language=EN, fundingSource=National Natural Science Foundation of China(81902384), fundOrder=null, country=null), Fund(id=1199376219830583765, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, awardId=81902384, language=CN, fundingSource=国家自然科学基金(81902384), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1199376214495428835, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, xref=null, ext=[AuthorCompanyExt(id=1199376214503817443, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, companyId=1199376214495428835, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Department of General Surgery, Peking University First Hospital, Beijing 100034, China), AuthorCompanyExt(id=1199376214512206052, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, companyId=1199376214495428835, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=北京大学第一医院普通外科，北京 100034)])], figs=[ArticleFig(id=1199376218505183651, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=EN, label=Fig.1, caption=Survival curve analyzing the predictive factor of RCLM patients, figureFileSmall=5wzOEinASV41icLrKm5kCQ==, figureFileBig=XTC3wy0WEzUyh4oRaO3aAg==, tableContent=null), ArticleFig(id=1199376218589069735, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=CN, label=图1, caption=RCLM患者预后因素生存曲线分析

RCLM. 直肠癌肝转移

, figureFileSmall=5wzOEinASV41icLrKm5kCQ==, figureFileBig=XTC3wy0WEzUyh4oRaO3aAg==, tableContent=null), ArticleFig(id=1199376218698121643, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=EN, label=Fig.2, caption=Survival curve analyzing the predictive factor of young RCLM patients, figureFileSmall=qJogqQehx6Zalkzumn99cg==, figureFileBig=XRWzHkP0ca1tTNyuxMC4ww==, tableContent=null), ArticleFig(id=1199376218790396336, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=CN, label=图2, caption=青年RCLM患者预后因素生存曲线分析

RCLM. 直肠癌肝转移

, figureFileSmall=qJogqQehx6Zalkzumn99cg==, figureFileBig=XRWzHkP0ca1tTNyuxMC4ww==, tableContent=null), ArticleFig(id=1199376218903642546, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=EN, label=Fig.3, caption=Survival curve analyzing the relationship between the maximum diameter of liver metastasis and local therapy in RCLM patients, figureFileSmall=d9hPqGoPCndfszGcrbBwNw==, figureFileBig=T5g3HXGK5TxK4HGHOumkLQ==, tableContent=null), ArticleFig(id=1199376218991722934, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=CN, label=图3, caption=RCLM患者肝转移瘤最大直径与局部治疗关系的生存曲线

RCLM. 直肠癌肝转移

, figureFileSmall=d9hPqGoPCndfszGcrbBwNw==, figureFileBig=T5g3HXGK5TxK4HGHOumkLQ==, tableContent=null), ArticleFig(id=1199376219079803322, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=EN, label=Tab.1, caption=

Comparison of clinicopathologic characteristics between two groups of RCLM patients [n(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
指标

青年组
(n=40)

中老年组
(n=82)

P
性别0.241
男23(57.5)56(68.3)
女17(42.5)26(31.7)
BMI(kg/m2)0.008
≤2625(62.5)69(84.1)
>2615(37.5)13(15.9)
CEA(ng/ml)0.822
≤513(32.5)25(30.5)
>527(67.5)57(69.5)
CA19-9(ng/ml)0.199
≤4017(42.5)45(54.9)
>4023(57.5)37(45.1)
初始白蛋白(g/L)0.121
≤3815(37.5)43(52.4)
>3825(62.5)39(47.6)
原发肿瘤T分期a-
T1+T2013(15.9)
T3+T440(100.0)69(84.1)
原发肿瘤N分期a0.240
N07(17.5)11(13.4)
N114(35.0)42(51.2)
N219(47.5)29(35.4)
原发肿瘤并发症b0.006
是33(82.5)47(57.3)
否7(17.5)35(42.7)
原发肿瘤是否切除0.824
是30(75.0)63(76.8)
否10(25.0)19(23.2)
肝转移发生时限0.005
同时性31(77.5)42(51.2)
异时性9(22.5)40(48.8)
肝转移瘤分布情况0.118
单侧半肝14(35.0)41(50.0)
双侧半肝26(65.0)41(50.0)
肝转移瘤最大直径(cm)0.019
≤319(47.5)57(69.5)
>321(52.5)25(30.5)
肝转移瘤数目(个)0.431
≤516(40.0)39(47.6)
>524(60.0)43(52.4)
肝转移瘤局部治疗c0.818
是15(37.5)29(35.4)
否25(62.5)53(64.6)
肝外转移情况d0.416
是14(35.0)35(42.7)
否26(65.0)47(57.3)
化疗周期数e0.157
≤1020(50.0)52(63.4)
>1020(50.0)30(36.6)
靶向治疗f0.069
是20(50.0)27(32.9)
否20(50.0)55(67.1)
肿瘤分化程度0.818
高分化/高-中分化/中分化25(62.5)53(64.6)
中低分化/低分化15(37.5)29(35.4)
肿瘤ras、raf基因状态0.054
未突变27(67.5)68(82.9)
突变13(32.5)14(17.1)
), ArticleFig(id=1199376219176272317, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=CN, label=表1, caption=

两组RCLM患者临床病理资料比较[例(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
指标

青年组
(n=40)

中老年组
(n=82)

P
性别0.241
男23(57.5)56(68.3)
女17(42.5)26(31.7)
BMI(kg/m2)0.008
≤2625(62.5)69(84.1)
>2615(37.5)13(15.9)
CEA(ng/ml)0.822
≤513(32.5)25(30.5)
>527(67.5)57(69.5)
CA19-9(ng/ml)0.199
≤4017(42.5)45(54.9)
>4023(57.5)37(45.1)
初始白蛋白(g/L)0.121
≤3815(37.5)43(52.4)
>3825(62.5)39(47.6)
原发肿瘤T分期a-
T1+T2013(15.9)
T3+T440(100.0)69(84.1)
原发肿瘤N分期a0.240
N07(17.5)11(13.4)
N114(35.0)42(51.2)
N219(47.5)29(35.4)
原发肿瘤并发症b0.006
是33(82.5)47(57.3)
否7(17.5)35(42.7)
原发肿瘤是否切除0.824
是30(75.0)63(76.8)
否10(25.0)19(23.2)
肝转移发生时限0.005
同时性31(77.5)42(51.2)
异时性9(22.5)40(48.8)
肝转移瘤分布情况0.118
单侧半肝14(35.0)41(50.0)
双侧半肝26(65.0)41(50.0)
肝转移瘤最大直径(cm)0.019
≤319(47.5)57(69.5)
>321(52.5)25(30.5)
肝转移瘤数目(个)0.431
≤516(40.0)39(47.6)
>524(60.0)43(52.4)
肝转移瘤局部治疗c0.818
是15(37.5)29(35.4)
否25(62.5)53(64.6)
肝外转移情况d0.416
是14(35.0)35(42.7)
否26(65.0)47(57.3)
化疗周期数e0.157
≤1020(50.0)52(63.4)
>1020(50.0)30(36.6)
靶向治疗f0.069
是20(50.0)27(32.9)
否20(50.0)55(67.1)
肿瘤分化程度0.818
高分化/高-中分化/中分化25(62.5)53(64.6)
中低分化/低分化15(37.5)29(35.4)
肿瘤ras、raf基因状态0.054
未突变27(67.5)68(82.9)
突变13(32.5)14(17.1)
), ArticleFig(id=1199376219255964097, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=EN, label=Tab.2, caption=

Univariate and multivariate Cox analysis of factors affecting OS in RCLM patients

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理因素(对照参数)单因素回归分析多因素回归分析
HR(95%CI)PHR(95%CI)P
年龄(≤45岁 vs. >45岁)1.573(1.011~2.447)0.0452.002(1.257~3.188)0.003
BMI(≤26 kg/m2 vs. >26 kg/m2)1.339(0.831~2.158)0.230
初始白蛋白(≤38 g/L vs. >38 g/L)1.166(0.772~1.761)0.465
CEA(≤5 ng/ml vs. >5 ng/ml)1.553(0.976~2.469)0.063
CA19-9(≤40 ng/ml vs. >40 ng/ml)1.448(0.960~2.186)0.078
原发肿瘤并发症(是 vs. 否)0.775(0.509~1.180)0.234
原发肿瘤根治切除(是 vs. 否)0.360(0.220~0.589)0.0000.731(0.414~1.290)0.279
原发肿瘤T分期(T1+T2 vs. T3+T4)1.770(0.851~3.683)0.126
原发肿瘤N分期(N0 vs. N1 vs. N2)1.542(1.150~2.067)0.0041.579(1.134~2.198)0.007
肝转移瘤分布情况(单侧 vs. 双侧)1.176(0.778~1.777)0.442
肝转移发生时限(同时性 vs. 异时性)1.104(0.726~1.680)0.643
肝外转移情况(是 vs. 否)1.457(0.955~2.223)0.080
分化程度(高分化/高-中分化/中分化 vs. 中低分化/低分化)1.357(0.877~2.099)0.171
肝转移瘤局部治疗(是 vs. 否)0.534(0.341~0.834)0.0060.598(0.361~0.992)0.047
肝转移瘤数目(≤5个vs. >5个)1.838(1.202~2.812)0.0051.368(0.839~2.230)0.209
肝转移瘤最大直径(≤3 cm vs. >3 cm)1.595(1.043~2.440)0.0311.723(1.054~2.817)0.030
化疗周期数(≤10 vs. >10)0.496(0.320~0.767)0.0020.671(0.414~1.088)0.106
靶向治疗(是 vs. 否)0.701(0.453~1.086)0.111
肿瘤ras、raf基因状态(未突变 vs. 突变)0.809(0.477~1.372)0.432
), ArticleFig(id=1199376219331461573, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=CN, label=表2, caption=

影响RCLM患者OS的单因素及多因素Cox回归分析

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理因素(对照参数)单因素回归分析多因素回归分析
HR(95%CI)PHR(95%CI)P
年龄(≤45岁 vs. >45岁)1.573(1.011~2.447)0.0452.002(1.257~3.188)0.003
BMI(≤26 kg/m2 vs. >26 kg/m2)1.339(0.831~2.158)0.230
初始白蛋白(≤38 g/L vs. >38 g/L)1.166(0.772~1.761)0.465
CEA(≤5 ng/ml vs. >5 ng/ml)1.553(0.976~2.469)0.063
CA19-9(≤40 ng/ml vs. >40 ng/ml)1.448(0.960~2.186)0.078
原发肿瘤并发症(是 vs. 否)0.775(0.509~1.180)0.234
原发肿瘤根治切除(是 vs. 否)0.360(0.220~0.589)0.0000.731(0.414~1.290)0.279
原发肿瘤T分期(T1+T2 vs. T3+T4)1.770(0.851~3.683)0.126
原发肿瘤N分期(N0 vs. N1 vs. N2)1.542(1.150~2.067)0.0041.579(1.134~2.198)0.007
肝转移瘤分布情况(单侧 vs. 双侧)1.176(0.778~1.777)0.442
肝转移发生时限(同时性 vs. 异时性)1.104(0.726~1.680)0.643
肝外转移情况(是 vs. 否)1.457(0.955~2.223)0.080
分化程度(高分化/高-中分化/中分化 vs. 中低分化/低分化)1.357(0.877~2.099)0.171
肝转移瘤局部治疗(是 vs. 否)0.534(0.341~0.834)0.0060.598(0.361~0.992)0.047
肝转移瘤数目(≤5个vs. >5个)1.838(1.202~2.812)0.0051.368(0.839~2.230)0.209
肝转移瘤最大直径(≤3 cm vs. >3 cm)1.595(1.043~2.440)0.0311.723(1.054~2.817)0.030
化疗周期数(≤10 vs. >10)0.496(0.320~0.767)0.0020.671(0.414~1.088)0.106
靶向治疗(是 vs. 否)0.701(0.453~1.086)0.111
肿瘤ras、raf基因状态(未突变 vs. 突变)0.809(0.477~1.372)0.432
), ArticleFig(id=1199376219436319176, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=EN, label=Tab.3, caption=

Univariate and multivariate analysis of factors affecting OS in young RCLM patients

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理因素(对照参数)单因素回归分析多因素回归分析
HR(95%CI)PHR(95%CI)P
BMI(≤26 kg/m2 vs. >26 kg/m2)1.441(0.673~3.087)0.347
白蛋白(≤38 g/L vs. >38 g/L)1.294(0.609~2.753)0.503
CEA(≤5 ng/ml vs. >5 ng/ml)1.781(0.759~4.180)0.185
CA19-9(≤40 ng/ml vs. >40 ng/ml)2.696(1.237~5.874)0.0131.320(0.534~3.260)0.547
原发肿瘤并发症(是 vs. 否)0.538(0.227~1.272)0.158
原发肿瘤根治切除(是 vs. 否)0.153(0.055~0.421)0.0000.277(0.084~0.911)0.035
原发肿瘤N分期(N0 vs. N1 vs. N2)1.975(1.162~3.354)0.0121.756(0.968~3.185)0.064
肝转移瘤分布情况(单侧 vs. 双侧)1.426(0.645~3.155)0.380
肝转移发生时限(同时性 vs. 异时性)1.084(0.478~2.458)0.846
肝外转移情况(是 vs. 否)2.114(1.173~4.593)0.0491.197(0.467~3.096)0.708
分化程度(高分化/高-中分化/中分化 vs. 中低分化/低分化)1.847(0.854~3.995)0.119
肝转移瘤局部治疗(是 vs. 否)0.723(0.328~1.594)0.422
肝转移瘤数目(≤5个vs. >5个)1.948(0.893~4.247)0.094
肝转移瘤最大直径(≤3 cm vs. >3 cm)2.343(1.094~5.017)0.0282.616(1.041~6.573)0.041
化疗周期数(≤10 vs. >10)0.448(0.204~0.984)0.0460.871(0.305~2.487)0.797
靶向治疗(是 vs. 否)1.279(0.608~2.690)0.516
肿瘤ras、raf基因状态(未突变 vs. 突变)1.177(0.498~2.783)0.711
), ArticleFig(id=1199376219532788173, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199337300208484764, language=CN, label=表3, caption=

影响青年RCLM患者OS的单因素及多因素COX回归分析

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理因素(对照参数)单因素回归分析多因素回归分析
HR(95%CI)PHR(95%CI)P
BMI(≤26 kg/m2 vs. >26 kg/m2)1.441(0.673~3.087)0.347
白蛋白(≤38 g/L vs. >38 g/L)1.294(0.609~2.753)0.503
CEA(≤5 ng/ml vs. >5 ng/ml)1.781(0.759~4.180)0.185
CA19-9(≤40 ng/ml vs. >40 ng/ml)2.696(1.237~5.874)0.0131.320(0.534~3.260)0.547
原发肿瘤并发症(是 vs. 否)0.538(0.227~1.272)0.158
原发肿瘤根治切除(是 vs. 否)0.153(0.055~0.421)0.0000.277(0.084~0.911)0.035
原发肿瘤N分期(N0 vs. N1 vs. N2)1.975(1.162~3.354)0.0121.756(0.968~3.185)0.064
肝转移瘤分布情况(单侧 vs. 双侧)1.426(0.645~3.155)0.380
肝转移发生时限(同时性 vs. 异时性)1.084(0.478~2.458)0.846
肝外转移情况(是 vs. 否)2.114(1.173~4.593)0.0491.197(0.467~3.096)0.708
分化程度(高分化/高-中分化/中分化 vs. 中低分化/低分化)1.847(0.854~3.995)0.119
肝转移瘤局部治疗(是 vs. 否)0.723(0.328~1.594)0.422
肝转移瘤数目(≤5个vs. >5个)1.948(0.893~4.247)0.094
肝转移瘤最大直径(≤3 cm vs. >3 cm)2.343(1.094~5.017)0.0282.616(1.041~6.573)0.041
化疗周期数(≤10 vs. >10)0.448(0.204~0.984)0.0460.871(0.305~2.487)0.797
靶向治疗(是 vs. 否)1.279(0.608~2.690)0.516
肿瘤ras、raf基因状态(未突变 vs. 突变)1.177(0.498~2.783)0.711
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散发性青年直肠癌肝转移患者临床特点及其预后影响因素
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关宇 , 杨磊 , 蒋世濡 , 窦伟冬 , 王金贵 , 陈善稳 , 刘占兵 * , 武颖超
解放军医学杂志 | 直肠癌手术及围手术期治疗策略专题 2024,49(1): 23-30
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解放军医学杂志 | 直肠癌手术及围手术期治疗策略专题 2024, 49(1): 23-30
散发性青年直肠癌肝转移患者临床特点及其预后影响因素
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关宇, 杨磊, 蒋世濡, 窦伟冬, 王金贵, 陈善稳, 刘占兵* , 武颖超
作者信息
  • 北京大学第一医院普通外科，北京 100034

    • 关宇，博士研究生，主治医师，主要从事胃肠、肝胆良恶性疾病外科治疗方面的研究

通讯作者:

刘占兵，E-mail：
Clinical characteristics and prognostic factors of young patients with sporadic rectal cancer liver metastasis
Yu Guan, Lei Yang, Shi-Ru Jiang, Wei-Dong Dou, Jin-Gui Wang, Shan-Wen Chen, Zhan-Bing Liu* , Ying-Chao Wu
Affiliations
  • Department of General Surgery, Peking University First Hospital, Beijing 100034, China
出版时间: 2024-01-28 doi: 10.11855/j.issn.0577-7402.2625.2023.0330
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摘要
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目的 探讨散发性青年直肠癌肝转移(RCLM)患者的临床特点及其预后影响因素。方法 回顾性分析2016年1月-2021年1月北京大学第一医院收治的青年RCLM患者(发病年龄≤45岁)的临床病理资料(设为青年组，n=40)，并按照1∶2的比例纳入中老年RCLM患者(发病年龄>45岁，设为中老年组，n=82)。比较两组临床病理因素的差异性，采用单因素及多因素Cox回归分析影响RCLM及青年RCLM患者预后的危险因素，结合Kaplan-Meier生存曲线分析肝转移瘤直径与局部治疗之间的预后关系。结果 共纳入RCLM患者122例，青年组1、3、5年生存率分别为97.5%、47.5%、15.0%，中老年组1、3、5生存率分别为84.1%、26.8%、9.8%。两组BMI(P=0.008)、原发肿瘤存在并发症情况(P=0.006)、肝转移发生时限中同时性肝转移(P=0.005)、肝转移瘤最大直径>3 cm(P=0.019)差异有统计学意义。单因素及多因素Cox回归分析显示，年龄(P=0.003)、原发肿瘤N分期(P=0.007)、肝转移瘤局部治疗(P=0.047)和肝转移瘤最大直径(P=0.030)是影响RCLM患者预后的独立危险因素，原发肿瘤是否根治性切除(P=0.035)和肝转移瘤最大直径(P=0.041)是影响青年RCLM患者预后的独立危险因素。肝转移瘤最大直径与肝转移瘤局部治疗组间生存期差异有统计学意义(log-rank P=0.000)。结论 青年RCLM患者肿瘤初始分期较晚，但生存预后优于中老年RCLM患者。淋巴结转移程度高、肝转移瘤未经局部治疗以及肝转移瘤最大直径>3 cm提示RCLM患者预后不良。原发肿瘤根治性切除及肝转移瘤最大直径是影响青年RCLM患者预后的独立危险因素，肝转移瘤局部治疗在RLCM患者治疗策略中起重要作用。

直肠癌肝转移  /  青年患者  /  预后因素

Objective To identify the clinical characteristics and prognostic factors of young patients with sporadic rectal cancer liver metastasis (RCLM). Methods The clinical data of young RCLM patients at 45 years or under (n=40, as younger patient group) in Peking University First Hospital from January 2016 to January 2021 were reviewed, meanwhile, elder RCLM patient group were comprised of 82 patients older than 45-year-old in a 1:2 ratio. Proportions of categorical variables were compared between young patients and old patients. The clinicopathologic parameters were analyzed with univariate and multivariate Cox regression models and Kaplan-Meier method for demonstrating survival differences between the maximum diameter of liver metastasis and local therapy. Results One hundred and twenty-two RCLM patients were identified, the 1-, 3- and 5-year survival rates of young patient group were 97.5%, 47.5%, 15.0%, those of elder patient group were 84.1%, 26.8%, 9.8%, respectively. The differences in BMI (P=0.008), primary tumor with obstruction and bleeding (P=0.006), synchronous rectal cancer liver metastases (P=0.005), the maximum diameter of liver metastasis >3 cm (P=0.019) were statistically significant between the two groups. And univariate and multivariate analyses showed that age (P=0.003), N stage (P=0.007), local therapy for liver metastases (P=0.047) and the maximum diameter of liver metastasis (P=0.030) were independent risk factors for influencing the prognosis of RCLM patients; curative resection or not of primary tumor (P=0.035) and the maximum diameter of liver metastasis (P=0.041) were independent risk factors for influencing the prognosis of young RCLM patients. Kaplan-Maier curve demonstrated survival differences between the maximum diameter of liver metastasis and local therapy for liver metastasis in RCLM patients (log-rank P=0.000). Conclusions Although with later staging of initial tumor station, young RCLM patients may obtain better survival benefit compared with old patients. Higher degree of lymph node metastasis, local therapy for liver metastases and the maximum diameter of liver metastasis >3 cm indicates poor prognosis in RCLM patients, and without curative resection of primary tumor and maximum diameter of liver metastasis are also considered as the independent poor prognostic factors of young RCLM patients. Local therapy for liver metastases appears to play an important role in the treatment strategy of RCLM patients.

rectal cancer liver metastasis  /  young patients  /  prognostic factors
关宇, 杨磊, 蒋世濡, 窦伟冬, 王金贵, 陈善稳, 刘占兵, 武颖超. 散发性青年直肠癌肝转移患者临床特点及其预后影响因素. 解放军医学杂志, 2024 , 49 (1) : 23 -30 . DOI: 10.11855/j.issn.0577-7402.2625.2023.0330
Yu Guan, Lei Yang, Shi-Ru Jiang, Wei-Dong Dou, Jin-Gui Wang, Shan-Wen Chen, Zhan-Bing Liu, Ying-Chao Wu. Clinical characteristics and prognostic factors of young patients with sporadic rectal cancer liver metastasis[J]. Medical Journal of Chinese People’s Liberation Army, 2024 , 49 (1) : 23 -30 . DOI: 10.11855/j.issn.0577-7402.2625.2023.0330
正文
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直肠癌是消化系统常见的恶性肿瘤，肝转移是其最常见的远处转移方式，也是引起直肠癌死亡事件的主要原因之一[1-2]。直肠癌肝转移(rectal cancer liver metastasis，RCLM)患者中位生存期为4.5~21.0个月，既往统计显示5年存活率仅为0~3%[3]。直肠癌好发于中老年人群，但随着近年来生活方式、饮食习惯等因素的改变，青年散发性直肠癌患者(发病年龄≤45岁)的发病率逐年上升，且较老年患者更容易发生肝转移，预后较差[4-5]。目前国内外对于青年RCLM的治疗尚无系统研究及统一标准，同时缺乏相应治疗预后的回顾性分析[6]。本研究旨在探讨青年RCLM患者的临床特点及多种临床病理因素对其预后的影响，以期指导其治疗决策的选择。
1 资料与方法
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1.1 研究对象
回顾性分析2016年1月-2021年1月北京大学第一医院普通外科收治的青年RCLM患者[发病年龄≤45岁，设为青年组(n=40)]的临床病理资料，并采用随机生成法按照1∶2的比例纳入中老年RCLM患者[发病年龄>45岁，设为中老年组(n=82)]。纳入标准：(1)肿瘤距离肛门缘≤15 cm，且肠镜检查或手术病理证实为直肠腺癌；(2)病理学或影像学诊断肝转移瘤；(3)随访资料完整。排除标准：(1)失访；(2)围手术期死亡；(3)遗传性结直肠综合征。将RCLM患者分为肝转移瘤最大直径≤3 cm且接受局部治疗(n=24)、肝转移瘤最大直径>3 cm且接受局部治疗(n=20)、肝转移瘤最大直径≤3 cm未接受局部治疗(n=49)以及肝转移瘤最大直径>3 cm未接受局部治疗(n=29) 4个亚组。本研究经过北京大学第一医院伦理委员会审核(2020科研025)。
1.2 资料收集
通过电子病历数据库系统回顾分析患者的一般资料、实验室检查结果及术后病理结果，回顾大宗相关文献选取国内外学者提出的可能与RCLM预后相关的临床病理因素，并结合北京大学第一医院普通外科对于RCLM患者相关外科及综合治疗方面临床实践选取的多项临床病理因素，如表1所示。肿瘤分期使用美国癌症联合会(American Joint Committee on Cancer，AJCC)和国际抗癌联盟(Union for International Cancer Control，UICC) 2017年提出的第8版直肠癌TNM分期定义。记录每例患者原发肿瘤浸润深度(T分期)、淋巴结转移(N分期)等临床病理参数(表1)。末次随访时间为2022年10月31日，总生存期(overall survival，OS)定义为患者确诊直肠癌或直肠癌同时性肝转移时间至患者死亡或末次随访时间间隔。
1.3 指标分析
(1)比较两组临床病理因素的差异；(2)对上述临床病理因素与OS的相关性进行单因素分析，将单因素分析显示有统计学意义的参数纳入多因素Cox回归分析，以确定影响RCLM患者及青年RCLM患者预后的独立危险因素，并分析肝转移瘤直径因素与局部治疗的预后关系。
1.4 统计学处理
采用SPSS 26.0软件进行统计分析；年龄以M(Q1，Q3)表示，计数资料以例(%)表示，连续变量转换为分类变量，组间比较采用χ2检验。临床病理因素与OS的相关性采用log-rank检验，采用多因素Cox回归及Kaplan-Meier生存曲线分析影响RCLM患者及青年RCLM患者预后的独立危险因素，并采用Kaplan-Meier生存曲线分析肝转移瘤直径因素与局部治疗的关系。P<0.05为差异有统计学意义。
2 结果
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2.1 两组临床病理资料比较
122例RCLM患者中男79例(64.8%)，女43例(35.2%)，年龄24~94岁，中位年龄58岁。青年组中男23例(57.5%)，女17例(42.5%)；中老年组中男56例(68.3%)，女26例(31.7%)。末次随访时间为2022年10月31日，总体中位生存期为26.5(OS：1~96)个月，青年组、中老年组中位生存期分别为31(OS：5~96)个月、24(OS：1~84)个月。青年组1、3、5年生存率分别为97.5%、47.5%、15.0%，中老年组1、3、5年生存率分别为84.1%、26.8%、9.8%。
两组BMI、原发肿瘤并发症、肝转移发生时限、肝转移瘤最大直径差异有统计学意义(P<0.05)，但性别，癌胚抗原(CEA)、糖类抗原19-9(CA19-9)、初始白蛋白水平，原发肿瘤N分期，以及原发肿瘤是否切除等资料比较差异均无统计学意义(P>0.05)。此外，青年组原发肿瘤T分期均为T3-T4期，两组间未进行比较(表1)。
2.2 RCLM患者预后影响因素分析
单因素Cox回归分析结果显示，年龄(P=0.045)、原发肿瘤N分期(P=0.004)、原发肿瘤是否根治性切除(P=0.000)、肝转移瘤是否局部治疗(P=0.006)、肝转移瘤数目(P=0.005)、肝转移瘤最大直径(P=0.031)及化疗周期数(P=0.002)是影响RCLM患者OS的危险因素(表2)。
将上述有统计学意义的因素纳入多因素Cox回归分析，结果显示，年龄(≤45岁 vs. >45岁，P=0.003)、原发肿瘤N分期(N0 vs. N1 vs. N2，P=0.007)、肝转移瘤局部治疗(是 vs. 否，P=0.047)和肝转移瘤最大直径(≤3 cm vs. >3 cm，P=0.030)是影响RCLM患者OS的独立危险因素(表2)。Kaplan-Meier生存曲线如图1所示。
2.3 青年RCLM患者预后影响因素分析
单因素Cox回归分析结果显示，CA19-9(P=0.013)、原发肿瘤N分期(P=0.012)、原发肿瘤是否根治性切除(P=0.000)、肝转移瘤最大直径(P=0.028)、肝外转移情况(P=0.049)及化疗周期数(P=0.046)是影响青年RCLM患者OS的危险因素(表3)。
将上述有统计学意义的因素纳入多因素Cox回归分析，结果显示，原发肿瘤是否根治性切除(是 vs. 否，P=0.035)和肝转移瘤最大直径(≤3 cm vs. >3 cm，P=0.041)是影响青年RCLM患者OS的独立危险因素(表3)。Kaplan-Meier生存曲线如图2所示。
2.4 肝转移瘤最大直径与局部治疗关系的生存分析
Kaplan-Meier生存曲线如图3所示，4个亚组生存期存在差异(log-rank P=0.000)。接受肝转移瘤局部治疗的两个亚组(肝转移瘤最大直径≤3 cm且接受局部治疗、肝转移瘤最大直径>3 cm且接受局部治疗)生存期优于未经过肝转移瘤局部治疗组，而肝转移瘤最大直径>3 cm未接受局部治疗组生存预后最差。
3 讨论
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由于青年直肠癌患者诊断时间延误，其肝转移发生率明显高于老年患者，且初始肿瘤分期较晚，严重影响患者的生存预后[7]。目前青年RCLM患者的治疗策略尚无统一标准，主要有包含肝转移瘤手术切除、介入栓塞、射频消融在内的局部治疗、化疗，以及免疫治疗等方法。因此，探讨青年RCLM患者的临床特点、预后危险因素及选择合适的治疗策略对改善不良预后至关重要[8-9]。
年龄是影响直肠癌患者预后的主要危险因素。Mauri等[10]认为，青年与老年直肠癌患者的临床病理特征存在明显差异。青年直肠癌患者往往表现为疾病进展程度更高、癌细胞分化更差、印戒细胞癌占比更高等特点。Mueller等[11]研究显示，根据肿瘤TNM分期，约51.8%的青年结直肠癌患者(年龄<50岁)发生远处转移，且最常转移至肝脏，肝转移发生率及5年生存期明显优于老年患者，与Ulanja等[12]的研究结果相似。此外，青年结直肠癌患者术后复发时生存预后较老年患者更好[13]。然而，目前关于青年RCLM患者的预后分析鲜少报道。本研究根据美国癌症协会最新结直肠癌筛查建议[14]，将RCLM患者根据年龄分为青年组(发病年龄≤45岁)与中老年组(发病年龄>45岁)，结果显示，年龄是影响RCLM患者预后的独立危险因素，相较老年RCLM患者，青年RCLM患者具有BMI高、身体一般状况可、初始肿瘤T分期晚、原发肿瘤多合并梗阻及出血等并发症、同时性肝转移发生率高、肝转移瘤直径大等特点，但生存预后较好；进一步对青年RCLM患者进行预后影响因素分析，结果显示，原发肿瘤根治性切除是影响预后的主要因素。因此，在临床实践中，应结合青年RCLM患者自身条件情况，积极行原发肿瘤根治性切除，解除原发肿瘤梗阻、出血等情况，可以更为安全有效地采取后续系统治疗，也可能使患者在肿瘤生存期方面获益。青年RCLM患者虽然肿瘤初始分期较晚但总体生存预后较好，针对上述临床发现，目前尚缺乏明确的指南及共识报道，笔者结合相关研究报道，推测可能存在以下几个原因[15-16]：(1)青年直肠癌患者对癌症相关症状不够重视，且结肠镜检查不是青年人群体检的常规检查项目，确诊往往存在延误，因而一经诊断往往处于肿瘤中晚期或局部进展期；(2)青年患者身体素质和营养状况较好，更能耐受复杂手术治疗和长时程的辅助放疗、化疗，甚至免疫治疗；(3)年龄相关的免疫衰老、淋巴细胞功能异常以及系统炎症可能导致老年RCLM患者的预后较差。因此，进一步阐明青年RCHM患者预后良好的机制有助于制定个性化的治疗方案。
淋巴结转移是影响RCLM患者远期预后的独立危险因素[17]。Rees等[18]分析了929例结直肠癌肝转移(colorectal cancer liver metastases，CRLM)肝切除术后病例，发现淋巴结阳性患者癌症特异性生存期明显优于淋巴结阴性患者。Acciuffi等[19]发现，CRLM患者5、10年生存率分别为47%、28%，5、10年无病生存率分别为30%、20%；超过3枚淋巴结阳性的CRLM患者OS和无病生存期明显缩短，且疾病复发率明显增高。相似报道指出，淋巴结分期为N2期的青年CRLM患者较N0期患者预后差[20]。本研究进一步对RCLM患者进行淋巴结转移分期(N0、N1、N2)，结果显示，淋巴结转移明显降低了RCLM患者的总体生存率，且随着淋巴结转移分期越高，总体生存率越低。
肝转移瘤直径大小是影响CRLM患者预后的重要因素。Kavlakoglu等[21]报道了2004-2007年单中心的42例肝转移瘤治疗性切除术后CRLM患者，多因素Cox回归分析显示，肝转移瘤最大直径>4 cm是影响CRLM患者预后的独立危险因素，且使CRLM患者死亡的风险增加5.89倍。Ma等[22]发现，CRLM患者肝转移瘤数目>4个及肝转移瘤最大直径>5 cm与预后相关。Cao等[23]回顾性分析了9736例CRLM患者，发现肝转移瘤大小是CRLM预后的独立危险因素，肝转移瘤最大直径>5 cm与术后无复发生存期缩短密切相关。本研究也发现，肝转移瘤最大直径>3 cm明显降低了青年RCLM患者的总体生存率。
对于RCLM可行肝脏局部治疗的患者，目前认为最有效的治疗方法是原发肿瘤根治性切除联合同期或分期肝转移瘤切除。Afshari等[24]回顾性分析了281例RCLM患者，多因素分析显示，肝转移瘤切除是RCLM患者生存期延长的主要因素。Mariathasan等[25]报道，RCLM患者中，接受肝转移瘤切除术者5年生存率为69%，未接受肝转移瘤切除术者5年生存率仅为12%。肝转移瘤不可切除者的中位生存期、2年和5年总体生存率低于肝转移瘤可切除者(37个月 vs. 56个月，68.5% vs. 87.4%，32.9% vs. 48%)，表明肝转移瘤切除术是RCLM患者延长生存期的主要治疗策略[26]。本研究发现，青年RCLM患者行肝脏局部治疗能够明显延长总体生存期。在RCLM同期行原发肿瘤根治切除与肝部分切除术时，直肠与肝脏在解剖学位置上相距较远，手术技术要求较高，手术时间较长，且肝脏手术出血量不可预估，老年患者往往无法耐受同期手术的风险，而青年患者既往身体状况可，往往能够耐受直肠癌根治+肝部分切除术。
本研究针对肝转移瘤直径与局部治疗的关系进行生存分析，结果发现，肝转移瘤最大直径≤3 cm且接受局部治疗、肝转移瘤最大直径>3 cm且接受局部治疗、肝转移瘤最大直径≤3 cm未接受局部治疗以及肝转移瘤最大直径>3 cm未接受局部治疗4个亚组间生存期存在明显差异。接受肝转移瘤局部治疗的两个亚组生存获益明显优于未接受肝转移瘤局部治疗组，由此推断，肝转移瘤局部治疗在RCLM预后中发挥更为重要的作用。肝转移瘤最大直径>3 cm且接受局部治疗组与肝转移瘤最大直径≤3 cm未接受局部治疗组间生存曲线存在交叉，生存期在50个月以内肝转移瘤最大直径>3 cm且接受局部治疗组获得明显生存获益，而后期两组间生存曲线无明显差异。在临床实践过程中，肝外出现转移、肝转移分布情况、身体条件不能耐受肝转移瘤局部治疗等因素使得一部分肝转移瘤直径≤3 cm的患者未接受局部治疗。
然而，青年RCLM患者的预后影响因素及治疗方法选择尚存在诸多不确定性，也缺乏相关指南推荐或循证学证据支持。本研究由于样本量有限、辅助治疗方案不统一、治疗技术及相关药物存在差异、回顾性研究时间跨度较大，研究结果可能存在一定偏差，有待多中心、大样本量的回顾性研究验证相关结果。
综上所述，青年RCLM患者具有BMI高、原发肿瘤初始T分期晚、原发肿瘤合并梗阻及出血等并发症、同时性肝转移以及肝转移瘤直径大等特点。目前，由于青年RCLM患者诊断延误往往导致疾病进展快、肿瘤分期晚，但因其可耐受长周期、多种类的治疗途径，因而预后相对较好。对于RCLM患者，年龄>45岁、原发肿瘤N分期晚、肝转移瘤未经局部治疗以及肝转移瘤最大直径>3 cm提示预后不良。因此针对这类患者应积极提倡采取多学科团队合作综合治疗、个体化治疗手段，积极争取在原发肿瘤根治性切除情况下，综合运用系统治疗联合肝转移瘤局部治疗的策略，为RCLM患者特别是青年RCLM患者提供更多的生存获益。同时也提倡具有高危因素的青年人群能够做到肿瘤的早发现、早治疗。
基金
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  • 国家自然科学基金(81902384)
文献
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2024年第49卷第1期
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doi: 10.11855/j.issn.0577-7402.2625.2023.0330
  • 接收时间：2022-12-20
  • 首发时间：2025-11-23
  • 出版时间：2024-01-28
补充材料
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出版历史
  • 收稿日期：2022-12-20
  • 录用日期：2023-03-05
基金
National Natural Science Foundation of China(81902384)
国家自然科学基金(81902384)
作者信息
    北京大学第一医院普通外科，北京 100034

通讯作者:

刘占兵，E-mail：
参考文献
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https://castjournals.cast.org.cn/joweb/jfjyxzz/CN/10.11855/j.issn.0577-7402.2625.2023.0330
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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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