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Article(id=1203002059831337075, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1203002056400396334, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2023.06.0708, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1655395200000, receivedDateStr=2022-06-17, revisedDate=null, revisedDateStr=null, acceptedDate=1657900800000, acceptedDateStr=2022-07-16, onlineDate=1764747641761, onlineDateStr=2025-12-03, pubDate=1687881600000, pubDateStr=2023-06-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1764747641761, onlineIssueDateStr=2025-12-03, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1764747641761, creator=13701087609, updateTime=1764747641761, updator=13701087609, issue=Issue{id=1203002056400396334, tenantId=1146029695717560320, journalId=1189873630562394117, year='2023', volume='48', issue='6', pageStart='627', pageEnd='748', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1764747640943, creator=13701087609, updateTime=1764747714497, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1203002364979540735, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1203002056400396334, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1203002364979540736, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1203002056400396334, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=708, endPage=714, ext={EN=ArticleExt(id=1203002060225601671, articleId=1203002059831337075, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Value of tumor growth pattern and tumor budding on judgment of patient’s prognosis with stageⅠ-Ⅲ colorectal cancer, columnId=1190310109000602400, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Clinical Research, runingTitle=null, highlight=null, articleAbstract=

Objective To analyze the value of tumor growth pattern (TGP) and tumor budding (TB) on judgment of the prognosis of patients with stage Ⅰ-Ⅲ colorectal cancer. Methods The clinical data of 152 patients with stage Ⅰ-Ⅲ colorectal cancer, admitted and undergone radical operation from December 2012 to June 2020 in Hainan Hospital of Chinese PLA General Hospital, were collected and retrospectively analyzed. TGP and TB were interpreted with HE staining and patients were divided into TGP-A (dilatant growth type and intermediate type) or B (invasive growth type), TB-low or TB-high subgroups. The differences of clinicopathological features among these subgroups were analyzed; Kaplan-Meier analysis was performed to analyze the disease-free survival (DFS) and overall survival (OS) of these subgroups. Finally, Cox proportional risk model was used to analyze the risk factors influencing prognosis of colorectal cancer patients. Results Statistical differences of tumor differentiation degree and N stage existed in TGP-A or TGP-B, TB-low or TB-high subgroups (P<0.01); in addition, the characteristics were more obvious of high CEA level (P=0.03), T3+T4 stage (P<0.01) and TNM Ⅲ stage (P<0.01) in TGP-B groups. Between TGP-A and TGP-B subgroups, and between TB-low and TB-high subgroups, the statistical significantly difference existed in DFS (TGP: Log-rank=10.06, P<0.01; TB: Log-rank=6.62, P=0.01) and OS (TGP: Log-rank=6.53, P=0.01; TB: Log-rank=4.90, P=0.03). TGP was an independent risk factor for both DFS (HR=2.95, 95%CI 1.54-5.63, P<0.01) and OS (HR=2.37, 95%CI 1.14-4.94, P=0.02). Conclusion Both TGP and TB were more reliable prognostic markers for patients with stage Ⅰ-Ⅲ colorectal cancer, the ones presented TGP with infiltrative pattern or TB ≥10/0.785 mm2 would have poor prognosis.

, correspAuthors=Bing Yan, authorNote=null, correspAuthorsNote=
* E-mail:
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目的 分析肿瘤生长形式（TGP）和肿瘤出芽（TB）对Ⅰ－Ⅲ期结直肠癌患者预后的判断价值。方法 回顾性收集2012年12月－2020年6月于解放军总医院海南医院行根治手术的152例Ⅰ－Ⅲ期结直肠癌患者。通过HE染色判读TGP和TB，并将患者分为TGP-A组（扩张性生长型和中间型）与TGP-B组（侵袭性生长型）或TB低组与TB高组，分析各亚组临床参数的差异，采用Kaplan-Meier法分析TGP-A组与TGP-B组、TB低组与TB高组的无病生存期（DFS）、总生存期（OS）；采用Cox比例风险模型分析影响结直肠癌患者预后的危险因素。结果 不同肿瘤分化程度、合并N分期在不同TGP、TB亚组中存在统计学差异（P<0.01）；此外，CEA值升高（P=0.03）、T3+T4期（P<0.01）、TNM Ⅲ期（P<0.01）等特征在TGP-B组更明显。TGP-A组与TGP-B组、TB低组与TB高组结直肠癌患者的DFS（TGP：Log-rank=10.06，P<0.01；TB：Log-rank=6.62，P=0.01）、OS（TGP：Log-rank=6.53，P=0.01；TB：Log-rank=4.90，P=0.03）存在统计学差异。TGP是结直肠癌患者DFS（HR=2.95，95%CI 1.54～5.63，P<0.01）和OS（HR=2.37，95%CI 1.14～4.94，P=0.02）的独立危险因素。结论 TGP、TB是Ⅰ－Ⅲ期结直肠癌患者较为可靠的预后标志物，TGP表现为侵袭性生长型或TB≥10个/0.785 mm2的患者预后较差。

, correspAuthors=颜兵, authorNote=null, correspAuthorsNote=
颜兵，E-mail：
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吴勇金，主治医师，主要从事胃肠道疾病手术治疗与预后相关指标方面的研究

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吴勇金，主治医师，主要从事胃肠道疾病手术治疗与预后相关指标方面的研究

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吴勇金，主治医师，主要从事胃肠道疾病手术治疗与预后相关指标方面的研究

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Nat Med, 2015, 21（11）: 1350-1356., articleTitle=The consensus molecular subtypes of colorectal cancer, refAbstract=null)], funds=[Fund(id=1203008551330472865, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, awardId=823MS164, language=EN, fundingSource=Natural Science Foundation of Hainan Province(823MS164), fundOrder=null, country=null), Fund(id=1203008551414358949, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, awardId=823MS164, language=CN, fundingSource=海南省自然科学基金(823MS164), fundOrder=null, country=null), Fund(id=1203008551485662120, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, awardId=2018YW06, language=EN, fundingSource=Medical and Health Technology Innovation Project of Sanya(2018YW06), fundOrder=null, country=null), Fund(id=1203008551598908331, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, awardId=2018YW06, language=CN, fundingSource=三亚市医疗卫生科技创新项目(2018YW06), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1203008547568182007, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, xref=1, ext=[AuthorCompanyExt(id=1203008547580764921, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, companyId=1203008547568182007, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1Department of General Surgery Unit 2, Sanya Central Hospital (Hainan Third People’s Hospital), Sanya, Hainan 572000, China), AuthorCompanyExt(id=1203008547589153533, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, companyId=1203008547568182007, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1三亚中心医院（海南省第三人民医院）普通外科二病区，海南三亚 572000)]), AuthorCompany(id=1203008547689816833, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, xref=2, ext=[AuthorCompanyExt(id=1203008547698205440, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, companyId=1203008547689816833, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Department of Oncology, Hainan Hospital of Chinese PLA General Hospital, Sanya, Hainan 572000, China), AuthorCompanyExt(id=1203008547706594049, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, companyId=1203008547689816833, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2解放军总医院海南医院肿瘤科，海南三亚 572000)])], figs=[ArticleFig(id=1203008550260925295, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=EN, label=Fig.1, caption=Typical pictures of TGP and TB in HE stained slides（×200）, figureFileSmall=zk47vfhDq9junpIHi4pY3w==, figureFileBig=PhTI768SbLmTmYQoSRKJcg==, tableContent=null), ArticleFig(id=1203008550344811379, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=CN, label=图1, caption=TGP、TB典型HE染色图（×200）

TGP. 肿瘤生长形式；TB. 肿瘤出芽；A. TGP扩张性生长型；B. TGP中间型；C. TGP侵袭性生长型；D. TB（低组），黑色箭头示TB

, figureFileSmall=zk47vfhDq9junpIHi4pY3w==, figureFileBig=PhTI768SbLmTmYQoSRKJcg==, tableContent=null), ArticleFig(id=1203008550449668984, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=EN, label=Fig.2, caption=Kaplan-Meier survival curve of different TGP and TB colorectal cancer patients, figureFileSmall=2bcekLbkcPzYsxro5vpB8g==, figureFileBig=4mscAGiu6hxGa9lmuXAN5Q==, tableContent=null), ArticleFig(id=1203008550537749372, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=CN, label=图2, caption=不同TGP与TB结直肠癌患者的Kaplan-Meier生存曲线

DFS. 无病生存期；OS. 总生存期；TGP. 肿瘤生长形式；TB. 肿瘤出芽

, figureFileSmall=2bcekLbkcPzYsxro5vpB8g==, figureFileBig=4mscAGiu6hxGa9lmuXAN5Q==, tableContent=null), ArticleFig(id=1203008550642606976, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=EN, label=Tab.1, caption=

Comparison of clinicopathological parameters in different TGP and TB colorectal cancer patients [n（%）]

, figureFileSmall=null, figureFileBig=null, tableContent=
项目TGPTB
TGP-A组（n=84）TGP-B组（n=68）χ2PTB低组（n=127）TB高组（n=25）χ2P
性别  0.710.50  3.910.07
 男50（59.5）45（66.2）  75（59.1）20（80.0）
 女34（40.5）23（33.8）  52（40.9）5（20.0）
年龄（岁）  0.270.63  0.130.83
 ≥6048（57.1）36（52.9）  71（55.9）13（52.0）
 <6036（42.9）32（47.1）  56（44.1）12（48.0）
肿瘤位置  2.860.13  0.220.80
 右侧16（19.0）21（30.9）  30（23.6）7（28.0）
 左侧68（81.0）47（69.1）  97（76.4）18（72.0）
肿瘤分化程度  12.08<0.01  13.07<0.01
 高中分化75（89.3）45（66.2）  107（84.3）13（52.0）
 低分化9（10.7）23（33.8）  20（15.7）12（48.0）
CEA值a  4.720.03  4.230.06
 正常60（73.2）34（55.7）  82（69.5）12（48.0）
 升高22（26.8）27（44.3）  36（30.5）13（52.0）
合并T分期 15.97<0.01  3.560.07
 T1+T229（34.5）5（7.4）  32（25.2）2（8.0）
 T3+T455（65.5）63（92.6）  95（74.8）23（92.0）
合并N分期  25.59<0.01  7.530.01
 N066（78.6）26（38.2）  83（65.4）9（36.0）
 N1+N218（21.4）42（61.8）  44（34.6）16（64.0）
TNM分期  23.44<0.01  5.390.06
 Ⅰ23（27.4）3（4.4）  24（18.9）2（8.0）
 Ⅱ41（48.8）26（38.2）  59（46.5）8（32.0）
 Ⅲ20（23.8）39（57.4）  44（34.6）15（60.0）  
), ArticleFig(id=1203008550726493060, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=CN, label=表1, caption=

不同TGP与TB结直肠癌患者临床病理参数比较[例（%）]

, figureFileSmall=null, figureFileBig=null, tableContent=
项目TGPTB
TGP-A组（n=84）TGP-B组（n=68）χ2PTB低组（n=127）TB高组（n=25）χ2P
性别  0.710.50  3.910.07
 男50（59.5）45（66.2）  75（59.1）20（80.0）
 女34（40.5）23（33.8）  52（40.9）5（20.0）
年龄（岁）  0.270.63  0.130.83
 ≥6048（57.1）36（52.9）  71（55.9）13（52.0）
 <6036（42.9）32（47.1）  56（44.1）12（48.0）
肿瘤位置  2.860.13  0.220.80
 右侧16（19.0）21（30.9）  30（23.6）7（28.0）
 左侧68（81.0）47（69.1）  97（76.4）18（72.0）
肿瘤分化程度  12.08<0.01  13.07<0.01
 高中分化75（89.3）45（66.2）  107（84.3）13（52.0）
 低分化9（10.7）23（33.8）  20（15.7）12（48.0）
CEA值a  4.720.03  4.230.06
 正常60（73.2）34（55.7）  82（69.5）12（48.0）
 升高22（26.8）27（44.3）  36（30.5）13（52.0）
合并T分期 15.97<0.01  3.560.07
 T1+T229（34.5）5（7.4）  32（25.2）2（8.0）
 T3+T455（65.5）63（92.6）  95（74.8）23（92.0）
合并N分期  25.59<0.01  7.530.01
 N066（78.6）26（38.2）  83（65.4）9（36.0）
 N1+N218（21.4）42（61.8）  44（34.6）16（64.0）
TNM分期  23.44<0.01  5.390.06
 Ⅰ23（27.4）3（4.4）  24（18.9）2（8.0）
 Ⅱ41（48.8）26（38.2）  59（46.5）8（32.0）
 Ⅲ20（23.8）39（57.4）  44（34.6）15（60.0）  
), ArticleFig(id=1203008550818767752, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=EN, label=Tab.2, caption=

Univariate analyses of the influence factors for DFS and OS for colorectal cancer patients after surgery

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因素DFSOS
HR（95%CI）PHR（95%CI）P
性别
 男 1 1
 女0.88（0.46～1.68）0.690.64（0.30～1.38）0.26
年龄（岁）
 ≥60 1 1
 <600.80（0.42～1.50）0.490.56（0.27～1.17）0.12
肿瘤位置
 右侧 1 1
 左侧0.63（0.28～1.42）0.270.68（0.28～1.65）0.40
肿瘤分化程度
 高中分化 1 1
 低分化2.06（1.05～4.05）0.042.36（1.14～4.90）0.02
CEA值a
 正常 1 1
 升高2.15（1.14～4.03）0.022.45（1.22～4.92）0.01
合并T分期
 T1+T2 1 1
 T3+T44.58（1.41～14.88）0.015.44（1.30～22.79）0.02
合并N分期
 N0 1 1
 N1+N22.14（1.15～3.99）0.021.61（0.81～3.23）0.18
TNM分期
 Ⅰ 1 1
 Ⅱ3.96（0.91～17.13）0.076.92（0.91～52.45）0.06
 Ⅲ6.64（1.55～28.38）0.019.88（1.31～74.62）0.03
术后辅助治疗
 接受 1 1
 未接受或不详1.66（0.88～3.15）0.121.32（0.65～2.68）0.44
TGP
 A 1 1
 B2.70（1.42～5.13）<0.012.46（1.20～5.04）0.01
TB
 低组 1 1
 高组2.41（1.20～4.84）0.012.33（1.08～5.03）0.03
), ArticleFig(id=1203008550919431053, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=CN, label=表2, caption=

结直肠癌患者术后DFS和OS影响因素的单因素分析

, figureFileSmall=null, figureFileBig=null, tableContent=
因素DFSOS
HR（95%CI）PHR（95%CI）P
性别
 男 1 1
 女0.88（0.46～1.68）0.690.64（0.30～1.38）0.26
年龄（岁）
 ≥60 1 1
 <600.80（0.42～1.50）0.490.56（0.27～1.17）0.12
肿瘤位置
 右侧 1 1
 左侧0.63（0.28～1.42）0.270.68（0.28～1.65）0.40
肿瘤分化程度
 高中分化 1 1
 低分化2.06（1.05～4.05）0.042.36（1.14～4.90）0.02
CEA值a
 正常 1 1
 升高2.15（1.14～4.03）0.022.45（1.22～4.92）0.01
合并T分期
 T1+T2 1 1
 T3+T44.58（1.41～14.88）0.015.44（1.30～22.79）0.02
合并N分期
 N0 1 1
 N1+N22.14（1.15～3.99）0.021.61（0.81～3.23）0.18
TNM分期
 Ⅰ 1 1
 Ⅱ3.96（0.91～17.13）0.076.92（0.91～52.45）0.06
 Ⅲ6.64（1.55～28.38）0.019.88（1.31～74.62）0.03
术后辅助治疗
 接受 1 1
 未接受或不详1.66（0.88～3.15）0.121.32（0.65～2.68）0.44
TGP
 A 1 1
 B2.70（1.42～5.13）<0.012.46（1.20～5.04）0.01
TB
 低组 1 1
 高组2.41（1.20～4.84）0.012.33（1.08～5.03）0.03
), ArticleFig(id=1203008551041065878, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=EN, label=Tab.3, caption=

Multivariate analyses of prognostic factors in patients with colorectal cancer after surgery

, figureFileSmall=null, figureFileBig=null, tableContent=
因素DFSOS
HR（95%CI）PHR（95%CI）P
TGP A 1 1
TGP B2.95（1.54～5.63）<0.012.37（1.14～4.94）0.02
), ArticleFig(id=1203008551145923481, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1203002059831337075, language=CN, label=表3, caption=

结直肠癌患者术后预后影响因素的多因素分析

, figureFileSmall=null, figureFileBig=null, tableContent=
因素DFSOS
HR（95%CI）PHR（95%CI）P
TGP A 1 1
TGP B2.95（1.54～5.63）<0.012.37（1.14～4.94）0.02
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肿瘤生长形式和肿瘤出芽对Ⅰ－Ⅲ期结直肠癌患者预后的判断价值
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吴勇金 1 , 薛天慧 2 , 颜兵 2, *
解放军医学杂志 | 临床研究 2023,48(6): 708-714
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解放军医学杂志 | 临床研究 2023, 48(6): 708-714
肿瘤生长形式和肿瘤出芽对Ⅰ－Ⅲ期结直肠癌患者预后的判断价值
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吴勇金1, 薛天慧2, 颜兵2, *
作者信息
  • 1三亚中心医院（海南省第三人民医院）普通外科二病区，海南三亚 572000
  • 2解放军总医院海南医院肿瘤科，海南三亚 572000

    • 吴勇金，主治医师，主要从事胃肠道疾病手术治疗与预后相关指标方面的研究

通讯作者:

颜兵，E-mail：
Value of tumor growth pattern and tumor budding on judgment of patient’s prognosis with stageⅠ-Ⅲ colorectal cancer
Yong-Jin Wu1, Tian-Hui Xue2, Bing Yan2, *
Affiliations
  • 1Department of General Surgery Unit 2, Sanya Central Hospital (Hainan Third People’s Hospital), Sanya, Hainan 572000, China
  • 2Department of Oncology, Hainan Hospital of Chinese PLA General Hospital, Sanya, Hainan 572000, China
出版时间: 2023-06-28 doi: 10.11855/j.issn.0577-7402.2023.06.0708
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摘要
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目的 分析肿瘤生长形式（TGP）和肿瘤出芽（TB）对Ⅰ－Ⅲ期结直肠癌患者预后的判断价值。方法 回顾性收集2012年12月－2020年6月于解放军总医院海南医院行根治手术的152例Ⅰ－Ⅲ期结直肠癌患者。通过HE染色判读TGP和TB，并将患者分为TGP-A组（扩张性生长型和中间型）与TGP-B组（侵袭性生长型）或TB低组与TB高组，分析各亚组临床参数的差异，采用Kaplan-Meier法分析TGP-A组与TGP-B组、TB低组与TB高组的无病生存期（DFS）、总生存期（OS）；采用Cox比例风险模型分析影响结直肠癌患者预后的危险因素。结果 不同肿瘤分化程度、合并N分期在不同TGP、TB亚组中存在统计学差异（P<0.01）；此外，CEA值升高（P=0.03）、T3+T4期（P<0.01）、TNM Ⅲ期（P<0.01）等特征在TGP-B组更明显。TGP-A组与TGP-B组、TB低组与TB高组结直肠癌患者的DFS（TGP：Log-rank=10.06，P<0.01；TB：Log-rank=6.62，P=0.01）、OS（TGP：Log-rank=6.53，P=0.01；TB：Log-rank=4.90，P=0.03）存在统计学差异。TGP是结直肠癌患者DFS（HR=2.95，95%CI 1.54～5.63，P<0.01）和OS（HR=2.37，95%CI 1.14～4.94，P=0.02）的独立危险因素。结论 TGP、TB是Ⅰ－Ⅲ期结直肠癌患者较为可靠的预后标志物，TGP表现为侵袭性生长型或TB≥10个/0.785 mm2的患者预后较差。

结直肠癌  /  肿瘤生长形式  /  肿瘤出芽  /  无病生存期  /  总生存期

Objective To analyze the value of tumor growth pattern (TGP) and tumor budding (TB) on judgment of the prognosis of patients with stage Ⅰ-Ⅲ colorectal cancer. Methods The clinical data of 152 patients with stage Ⅰ-Ⅲ colorectal cancer, admitted and undergone radical operation from December 2012 to June 2020 in Hainan Hospital of Chinese PLA General Hospital, were collected and retrospectively analyzed. TGP and TB were interpreted with HE staining and patients were divided into TGP-A (dilatant growth type and intermediate type) or B (invasive growth type), TB-low or TB-high subgroups. The differences of clinicopathological features among these subgroups were analyzed; Kaplan-Meier analysis was performed to analyze the disease-free survival (DFS) and overall survival (OS) of these subgroups. Finally, Cox proportional risk model was used to analyze the risk factors influencing prognosis of colorectal cancer patients. Results Statistical differences of tumor differentiation degree and N stage existed in TGP-A or TGP-B, TB-low or TB-high subgroups (P<0.01); in addition, the characteristics were more obvious of high CEA level (P=0.03), T3+T4 stage (P<0.01) and TNM Ⅲ stage (P<0.01) in TGP-B groups. Between TGP-A and TGP-B subgroups, and between TB-low and TB-high subgroups, the statistical significantly difference existed in DFS (TGP: Log-rank=10.06, P<0.01; TB: Log-rank=6.62, P=0.01) and OS (TGP: Log-rank=6.53, P=0.01; TB: Log-rank=4.90, P=0.03). TGP was an independent risk factor for both DFS (HR=2.95, 95%CI 1.54-5.63, P<0.01) and OS (HR=2.37, 95%CI 1.14-4.94, P=0.02). Conclusion Both TGP and TB were more reliable prognostic markers for patients with stage Ⅰ-Ⅲ colorectal cancer, the ones presented TGP with infiltrative pattern or TB ≥10/0.785 mm2 would have poor prognosis.

colorectal cancer  /  tumor growth pattern  /  tumor budding  /  disease free survival  /  overall survival
吴勇金, 薛天慧, 颜兵. 肿瘤生长形式和肿瘤出芽对Ⅰ－Ⅲ期结直肠癌患者预后的判断价值. 解放军医学杂志, 2023 , 48 (6) : 708 -714 . DOI: 10.11855/j.issn.0577-7402.2023.06.0708
Yong-Jin Wu, Tian-Hui Xue, Bing Yan. Value of tumor growth pattern and tumor budding on judgment of patient’s prognosis with stageⅠ-Ⅲ colorectal cancer[J]. Medical Journal of Chinese People’s Liberation Army, 2023 , 48 (6) : 708 -714 . DOI: 10.11855/j.issn.0577-7402.2023.06.0708
正文
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结直肠癌是严重威胁我国人民健康的恶性肿瘤之一，近年来其发病率和死亡率仍无下降趋势[1]。既往临床实践表明，尽管Ⅰ－Ⅲ期结直肠癌可通过手术或手术+化疗的方法获得治愈[2]，但仍有超过50%的患者出现肿瘤复发和转移，其中80%～90%的患者失去了手术治愈的机会[3]。可靠的预后标志物不仅可准确判断患者术后生存时间，且能筛选出复发转移的高危因素，从而指导临床治疗[4-5]，是目前研究的热点之一。既往研究发现，通过苏木精-伊红（hematoxylin and eosin，HE）染色的肿瘤组织病理学切片不仅可提供细胞形态、组织分化程度等信息，还包含肿瘤生长形式（tumor growth pattern，TGP）、肿瘤出芽（tumor budding，TB）、肿瘤间质比（tumor stroma proportion，TSP）等重要预后信息，对临床治疗具有重要的指导意义。研究发现，TGP与结直肠癌患者无病生存期（disease-free survival，DFS）、肿瘤特异性生存期（cancer-specific survival，CSS）等相关[6-7]；TB与结直肠癌患者DFS、复发及死亡等相关[8-9]。然而对于TGP和TB在结直肠癌预后判断中的重要性，目前仅少量研究进行了直接对比。例如，Wang等[10]纳入128例T3N0M0患者进行研究，发现TGP与TB内在相关，但仅TB为预后的独立危险因素；Betge等[11]纳入120例Ⅱ期结直肠癌患者进行研究也得出了类似结论，且发现联合TGP和TB并不能提高预后判断效能。值得注意的是，这些研究样本量均较小且局限于早期患者，对于其他分期患者能否得出同样结论尚不明确。本研究分析了TGP和TB对Ⅰ－Ⅲ期结直肠癌患者的预后判断价值。
1 资料与方法
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1.1 研究对象
回顾性收集2012年12月－2020年6月于解放军总医院海南医院行根治手术的152例结直肠癌Ⅰ－Ⅲ期（根据AJCC第7版）患者。纳入标准：（1）经手术完全切除病灶且病理明确为腺癌；（2）术前检查未发现远处转移；（3）年龄>18岁。排除标准：（1）术前接受任何抗肿瘤方案治疗；（2）术后病理报告缺失TNM任何一项信息；（3）合并其他未治愈的恶性疾病；（4）术后失访。本研究经解放军总医院海南医院伦理委员会批准（301HNFYLL15）。
1.2 资料收集
收集患者的临床病理资料，包括年龄、性别、肿瘤位置、肿瘤分化程度及术前癌胚抗原（carcinoembryonic antigen，CEA）检测值（参考范围0～5 μg/ml，检测方法同文献[12]）等。
1.3 HE染色判读TGP及TB
术后标本处理按照解放军总医院海南医院病理科标准流程进行，取石蜡包埋组织进行切片（厚度4 μm），行HE染色，排除坏死、缺损区域后于肿瘤侵袭性边缘通过HE染色判读TGP、TB，其中侵袭性边缘定义参照文献[13]。根据既往研究和TGP、TB判读结果将患者分为TGP-A组（扩张性生长型和中间型）与TGP-B组（侵袭性生长型）[7]或TB低组与TB高组[9，14]。其中TGP扩张性生长型定义为肿瘤细胞向外挤压式生长且与周围组织有较完整的边界，中间型是指中到大型腺样结构侵入周围组织并且其边界不完整；TGP侵袭性生长型主要指小型腺样结构或肿瘤细胞簇弥散性侵入周围组织而无明显边界[7]。TB的定义和判读参照2016版ITBCC[15]，其中TB低组包括TB1[（0～4）个/0.785 mm2]和TB2[（5～9）个/0.785 mm2]，TB高组仅指TB3（≥10个/0.785 mm2）。所有判读由两位对患者临床信息不知情的病理医师进行，判读不一致时通过协商处理。
1.4 随访及DFS、总生存期（overall survival，OS）定义
通过电话、微信或检索就诊记录等方式进行随访。术后1～3年每3～6个月随访1次，术后3年以上每年随访1次。随访截至2021年3月。
DFS定义为手术至任何部位出现复发、转移或任何原因引起死亡的时间；OS定义为相同起点至任何原因引起死亡的时间。
1.5 观察指标
比较不同TGP、TB结直肠癌患者的临床病理参数。采用Kaplan-Meier法分析不同TGP、TB结直肠癌患者的DFS、OS，采用Log-rank法比较组间差异。采用Cox比例风险模型（向前LR法）分析影响结直肠癌患者预后的危险因素。
1.6 统计学处理
采用SPSS 20.0软件进行统计分析。计数资料以例（%）表示，组间比较采用χ2检验。双侧P<0.05为差异有统计学意义。
2 结果
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2.1 一般资料
共纳入152例结直肠癌Ⅰ－Ⅲ期患者，其中Ⅰ期26例，Ⅱ期67例，Ⅲ期59例；男95例，女57例；平均年龄60.3（24.0～85.0）岁；随访时间48.0（1～91）个月，随访期内共有8例出现复发或转移，32例死亡；无病生存率为73.68%（112/152），总生存率为78.95%（120/152）；其中9例术前未检测CEA。
2.2 不同TGP与TB结直肠癌患者临床病理参数比较
HE染色可见不同形态的肿瘤组织在间质中分布，部分肿瘤组织和间质存在较明显的分界，而部分肿瘤组织已突破分界侵入间质中（图1）。
TGP-A组与TGP-B组、TB低组与TB高组肿瘤分化程度、合并N分期差异均有统计学意义（P<0.01），具体表现为低分化、N1+N2期等特征在TGP-B组或TB高组更常见。此外，CEA值升高（P=0.03）、T3+T4期（P<0.01）、TNM Ⅲ期（P<0.01）等特征在TGP-B组更明显，其他参数在不同TGP、TB亚组中均未见明显差异（表1）。
2.3 不同TGP与TB结直肠癌患者的生存分析
Kaplan-Meier生存曲线分析显示，TGP-B组结肠癌患者的DFS、OS明显短于TGP-A组（DFS：Log-rank=10.06，P<0.01；OS：Log-rank=6.53，P=0.01；图2A、B）；同时，TB高组结肠癌患者的DFS、OS明显短于TB低组（DFS：Log-rank=6.62，P=0.01；OS：Log-rank=4.90，P=0.03；图2C、D）。
2.4 结直肠癌患者术后预后影响因素分析
单因素分析结果显示，肿瘤分化程度、CEA、T1+T2期、TNM Ⅲ期、TGP、TB为结直肠癌患者术后DFS和OS的影响因素（P<0.05）；合并N1+N2期是结直肠癌患者术后DFS的影响因素（P<0.05，表2）。将上述P<0.05的因素纳入多因素Cox比例风险模型，结果显示，仅TGP是结直肠癌患者术后DFS（HR=2.95，95%CI 1.54～5.63，P<0.01）和OS（HR=2.37，95%CI 1.14～4.94，P=0.02）的独立危险因素（表3）。
3 讨论
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既往大量研究显示，TGP、TB对结直肠癌患者的预后判断具有较高价值。例如，Morikawa等[7]纳入1139例Ⅰ－Ⅲ期结直肠癌根治术后患者进行研究，发现TGP表现为侵袭性生长型与更短的CSS、OS相关，TGP的预后判断价值与微卫星、Kirsten大鼠肉瘤病毒癌基因（Kirsten rat sarcoma viral oncogene，KRAS）、鼠类肉瘤病毒癌基因同源物B1（v-raf murine sarcoma viral oncogene homolog B1，BRAF）等具有临床指导意义的分子改变无关。Tokodai等[16]纳入386例Ⅱ－Ⅲ期结直肠癌根治术后患者进行研究，发现TGP为侵袭性生长型提示Ⅱ－Ⅲ期患者具有较高的复发风险。此外，Pinheiro等[17]分析了91例合并肝转移的结直肠癌患者术后标本，发现TGP为侵袭性生长型与更短的DFS相关。对于TB，Oh等[18]纳入4196例Ⅰ－Ⅲ期结直肠癌根治术后患者，通过倾向匹配评分发现TB低组（TB1）与TB高组（TB2+TB3）无生存差异，虽然TB3组无病生存率、总生存率明显低于其他两组，但多因素分析显示TB并不是DFS或OS的独立危险因素；而Lai等[19]纳入135例结肠癌Ⅱ期患者进行分析，发现TB低组患者5年无病生存率明显高于TB高组，且TB是结肠癌患者预后的独立危险因素；Landau等[20]纳入106例Ⅱ期和150例Ⅲ期结肠癌（根据AJCC第8版）患者进行研究，发现TB（TB3）是结肠癌患者预后的独立危险因素，但仅限于Ⅲ期。此外，Trinh等[21]纳入参加LUMC、CAIRO和CAIRO2等临床试验的1320例结肠癌患者（Ⅰ－Ⅳ期）进行事后分析，发现TB高组（定义为≥5个/0.785 mm2）与更差的预后相关，且TB与患者KRAS/BRAF突变状态相关[21]；Ueno等[22]纳入991例经手术治疗的Ⅱ期结肠癌患者，发现TB1、TB2和TB3患者的5年无病生存率分别为90.9%、85.1%和74.4%，差异有统计学意义；Mitrovic等[9]纳入1575例相似分期的结直肠癌患者，随访10年发现，TB低组、TB高组的10年死亡率分别为37%、50%，差异有统计学意义。本研究发现，对于Ⅰ－Ⅲ期结直肠癌患者，TGP、TB均是较为可靠的预后判断标志物，其中TGP-B组、TB高组患者的预后明显劣于TGP-A组、TB低组，具体表现是TGP为侵袭性生长型或TB>10个/0.785 mm2的患者DFS、OS更短，与上述研究结果一致。
值得注意的是，HE染色提供的组织病理学信息可能存在内在联系，不同预后标志物的效能可能不同。因此有学者尝试将TGP、TB联合其他组织病理学结果以进一步提高对患者预后判断的效能。例如，Lee等[23]发现，TB联合低分化簇（poorly-differentiated clusters，PDC）能更好地判断Ⅱ期结直肠癌患者的预后。此外，Eriksen等[24]的研究纳入573例Ⅱ期结直肠癌患者，分析了TB和TSP对患者预后的判断价值，发现仅TSP是结直肠癌患者预后的独立危险因素。然而对于TGP和TB两个指标的对比研究，目前仅见少量报道且均提示仅TB为结直肠癌患者预后的独立危险因素，但这些研究存在样本量小且仅纳入了Ⅱ期患者等局限[10-11]。本研究发现，在Ⅰ－Ⅲ期结直肠癌患者中，尽管TB也具有预后判断价值，但仅TGP为患者预后的独立危险因素。这可能与早期结直肠癌（Ⅰ－ⅡA）患者中TB的判断价值较为有限有关[25]。此外，既往结直肠癌分子亚型（consensus molecular subtypes，CMS）共识将该病分为CMS1、CMS2、CMS3和CMS4等4种亚型，其中CMS4型更多见于Ⅲ－Ⅳ期患者，预后相较其他亚型更差[26]，而TB更多见于CMS4型患者[21]，这也可能在一定程度上限制了TB在Ⅰ－Ⅲ期患者中的预后判断价值。此外，本研究还发现，相较于TB，不同CEA值、合并T分期、TNM分期等参数在不同TGP亚组中存在明显差异，这些因素在一定程度上也提示TGP可能对预后判断更为准确，但仍需进一步验证。
本研究存在一定局限性：（1）为回顾性研究，纳入样本量总体偏少，可能存在一定的混杂因素；（2）尚缺乏微卫星、KRAS、BRAF等分子信息，无法进一步分层分析TGP、TB在不同分子突变状态下对患者预后的判断价值；（3）随访时间短，未能进一步在更长时间内证实TGP、TB对患者预后的判断价值。
综上所述，本研究结果表明，TGP、TB均是Ⅰ－Ⅲ期结直肠癌患者较为可靠的预后标志物，但仅TGP为预后的独立危险因素，TGP-B患者的预后明显劣于TGP-A患者，但该结果仍需进一步扩大样本量进行验证。
基金
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  • 海南省自然科学基金(823MS164)
  • 三亚市医疗卫生科技创新项目(2018YW06)
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2023年第48卷第6期
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doi: 10.11855/j.issn.0577-7402.2023.06.0708
  • 接收时间：2022-06-17
  • 首发时间：2025-12-03
  • 出版时间：2023-06-28
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  • 收稿日期：2022-06-17
  • 录用日期：2022-07-16
基金
Natural Science Foundation of Hainan Province(823MS164)
海南省自然科学基金(823MS164)
Medical and Health Technology Innovation Project of Sanya(2018YW06)
三亚市医疗卫生科技创新项目(2018YW06)
作者信息
    1三亚中心医院（海南省第三人民医院）普通外科二病区，海南三亚 572000
    2解放军总医院海南医院肿瘤科，海南三亚 572000

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2种不同金属材料的力学参数
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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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