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Article(id=1198558266251903245, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198558265329152414, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2283.2023.0529, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1667404800000, receivedDateStr=2022-11-03, revisedDate=null, revisedDateStr=null, acceptedDate=1673452800000, acceptedDateStr=2023-01-12, onlineDate=1763688158809, onlineDateStr=2025-11-21, pubDate=1722096000000, pubDateStr=2024-07-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1763688158809, onlineIssueDateStr=2025-11-21, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1763688158809, creator=13701087609, updateTime=1763688158809, updator=13701087609, issue=Issue{id=1198558265329152414, tenantId=1146029695717560320, journalId=1189873630562394117, year='2024', volume='49', issue='7', pageStart='733', pageEnd='854', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1763688158589, creator=13701087609, updateTime=1763689196450, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1198562618517581944, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198558265329152414, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1198562618517581945, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198558265329152414, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=747, endPage=753, ext={EN=ArticleExt(id=1198558266490978574, articleId=1198558266251903245, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Clinical prognosis analysis of gastric signet ring cell carcinoma with different pathological subtypes, columnId=1190310109000602400, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Clinical Research, runingTitle=null, highlight=null, articleAbstract=

Objective To explore the clinicopathological characteristics, prognosis and influencing factors of different pathological subtypes of gastric signet ring cell carcinoma (GSRC). Methods A retrospective analysis was performed on the clinical data of 232 patients with GSRC collected from January 2016 to December 2018 in Lanzhou University Second Hospital. According to the WHO classification criteria for GSRC, the patients were divided into pure gastric signet-ring cell carcinoma (pGSRC, n=36) and mixed gastric signet-ring cell carcinoma (mGSRC, n=196). The follow-up as of September 30, 2022, the survival analysis was done using Kaplan-Meier method, the univariate and multivariate Cox regression were performed to analyze the risk factors affecting the prognosis of GSRC patients. Results The median survival time of pGSRC and mGSRC patients was 41.0(6.0-70.0) months and 24.0(2.0-74.0) months, respectively. Kaplan-Meier analysis showed that combination with diabetes, anemia, tumor diameter, nerve invasion, lymphovascular invasion, T stage, N stage, GSRC pathological subtype, CA125 and tumor diameter could affect the overall survival (OS) of patients with GSRC after radical gastrectomy (P<0.05), but Her-2, whether adjuvant chemotherapy or not and others elements had no significant effect on OS of GSRC patients after radical gastrectomy (P>0.05). Univariate Cox regression analysis showed that the combination with diabetes (P=0.031), anemia (P=0.028), tumor diameter >5 cm (P=0.009), nerve invasion (P=0.002), lymphovascular invasion (P=0.002), mGSRC pathological type (P=0.039), T2-T4 stage (P=0.001), N1-N4 stage (P=0.004), pTNM stage Ⅲ (P=0.044), the number of lymph node metastasis >30 (P=0.044) and CA125 positive (P=0.009) were related to the prognosis of patients with GSRC after radical gastrectomy. Multivariate Cox regression analysis showed that mGSRC pathological type (P=0.035), T2-T4 stage (P=0.003), CA125 positive (P=0.010) were independent risk factors for poor prognosis of patients with GSRC after radical gastrectomy. Conclusion Compared with pGSRC, patients with mGSRC at diagnosis have higher pTNM stages, more aggressive, and shorter median survival time. mGSRC pathological type, T2-T4 stage, and CA125 positive were all independent factors affecting the prognosis of patients with GSRC.

, correspAuthors=Xiao Chen, authorNote=null, correspAuthorsNote=
E-mail:
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目的 探讨不同病理亚型胃印戒细胞癌(GSRC)患者的临床病理特征、预后及其影响因素。方法 回顾性收集2016年1月-2018年12月兰州大学第二医院收治的经病理确诊的232例GSRC患者的临床资料。按照WHO诊断标准进行分类，其中胃纯印戒细胞癌(pGSRC)36例，胃混合印戒细胞癌(mGSRC)196例，随访截至2022年9月30日。应用Kaplan-Meier法进行生存分析，单因素及多因素Cox回归分析影响GSRC患者预后的危险因素。结果 pGSRC和mGSRC患者中位生存时间分别为41.0(6.0~70.0)个月、24.0(2.0~74.0)个月。Kaplan-Meier生存分析显示，合并糖尿病、合并贫血、神经侵犯、脉管侵犯、T分期、N分期、GSRC病理类型、CA125和肿瘤直径可影响GSRC患者根治术后总生存期(OS)(P<0.05)，而Her-2、是否接受化疗等对GSRC患者根治术后OS无明显影响(P>0.05)。单因素Cox回归分析显示，合并糖尿病(P=0.031)、合并贫血(P=0.028)、肿瘤直径>5 cm(P=0.009)、神经侵犯(P=0.002)、脉管侵犯(P=0.002)、病理类型为mGSRC(P=0.039)、T2-T4分期(P=0.001)、N1-N4分期(P=0.004)、pTNM Ⅲ期(P=0.044)、淋巴结清扫数目>30个(P=0.044)和CA125阳性(P=0.009)是GSRC患者根治术后预后的影响因素。多因素Cox回归分析显示，mGSRC病理类型(P=0.035)、T2-T4分期(P=0.003)和CA125阳性(P=0.010)是GSRC患者根治术后预后不良的独立危险因素。结论 与pGSRC相比，mGSRC在确诊时pTNM分期较高，侵袭性较强，中位生存时间较短。mGSRC病理类型、T2-T4分期和CA125阳性是GSRC患者预后不良的独立危险因素。

, correspAuthors=陈晓, authorNote=null, correspAuthorsNote=
陈晓，E-mail：
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沈亦敏，硕士研究生，主要从事消化系统肿瘤发病机制方面的研究

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沈亦敏，硕士研究生，主要从事消化系统肿瘤发病机制方面的研究

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沈亦敏，硕士研究生，主要从事消化系统肿瘤发病机制方面的研究

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J Surg Oncol, 2014, 109(2): 61-66., articleTitle=HER2 in resected gastric cancer: Is there prognostic value?, refAbstract=null)], funds=[Fund(id=1198589377245971059, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, awardId=21JR7RA424, language=EN, fundingSource=Gansu Provincial Youth Science and Technology Fund(21JR7RA424), fundOrder=null, country=null), Fund(id=1198589377350828663, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, awardId=21JR7RA424, language=CN, fundingSource=甘肃省青年科技基金项目(21JR7RA424), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1198589370161791349, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, xref=1, ext=[AuthorCompanyExt(id=1198589370165985654, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, companyId=1198589370161791349, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1The Second School of Clinical Medicine, Lanzhou University, Lanzhou, Gansu 730013, China), AuthorCompanyExt(id=1198589370174374263, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, companyId=1198589370161791349, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1兰州大学第二临床医学院，甘肃兰州 730013)]), AuthorCompany(id=1198589370262454654, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, xref=2, ext=[AuthorCompanyExt(id=1198589370270843263, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, companyId=1198589370262454654, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Department of General Surgery, Lanzhou University Second Hospital, Lanzhou, Gansu 730030, China), AuthorCompanyExt(id=1198589370275037569, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, companyId=1198589370262454654, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2兰州大学第二医院普通外科，甘肃兰州 730030)])], figs=[ArticleFig(id=1198589375551472216, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, language=EN, label=Fig.1, caption=Kaplan-Meier survival analysis of GSRC patients after radical gastrectomy, figureFileSmall=LNGdphtSHSTjpUkpY+DQxw==, figureFileBig=IwHn0evuF52WQv5IbcLgpg==, tableContent=null), ArticleFig(id=1198589375635358300, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, language=CN, label=图1, caption=GSRC患者胃癌根治术后Kaplan-Meier生存分析

GSRC. 胃印戒细胞癌；pGSRC. 胃纯印戒细胞癌；CA125. 糖蛋白抗原125；Her-2. 人表皮生长因子受体2

, figureFileSmall=LNGdphtSHSTjpUkpY+DQxw==, figureFileBig=IwHn0evuF52WQv5IbcLgpg==, tableContent=null), ArticleFig(id=1198589375769576033, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, language=EN, label=Tab.1, caption=

Comparison of the clinicopathological characteristics between two groups of GSRC patients [n(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理特征pGSRC组(n=36)mGSRC组(n=196)χ2/ZP
性别4.8590.039
男21(58.3)149(76.0)
女15(41.7)47(24.0)
年龄(岁)2.1830.151
<5523(63.9)99(50.5)
≥5513(36.1)97(49.5)
合并高血压12(33.3)61(31.1)0.0690.846
合并糖尿病9(25.0)53(27.0)0.0651.000
合并贫血6(16.7)44(22.4)0.6010.515
肿瘤部位1.0640.587
上部4(11.1)35(17.9)
中部4(11.1)23(11.7)
下部28(77.8)138(70.4)
肿瘤直径(cm)9.8590.007
≤212(33.3)26(13.3)
2~516(44.4)94(48.0)
>58(22.2)76(38.8)
神经侵犯2.8580.099
是17(47.2)122(62.2)
否19(52.8)74(37.8)
脉管侵犯1.0890.331
是22(61.1)137(69.9)
否14(38.9)59(30.1)
T分期1.9150.173
T110(27.8)35(17.9)
T2-T426(72.2)161(82.1)
N分期4.0050.058
N018(50.0)64(32.7)
N1-N418(50.0)132(67.3)
pTNM分期11.9610.003
Ⅰ18(50.0)48(24.5)
Ⅱ9(25.0)44(22.4)
Ⅲ9(25.0)104(53.1)
淋巴结清扫数目(个)3.2470.197
1~1511(30.6)38(19.4)
15~3022(61.1)125(63.8)
>303(8.3)33(16.8)
CA1990.0001.000
阴性32(88.9)174(88.8)
阳性4(11.1)25(11.2)
CA1251.9370.242
阴性32(88.9)186(94.9)
阳性4(11.1)10(5.1)
Her-20.0091.000
阴性26(72.2)140(71.4)
阳性10(27.8)56(28.6)
BMI(kg/m2)2.4320.296
<18.52(5.6)30(15.3)
18.5~23.925(69.4)122(62.2)
>23.99(25.0)44(22.4)
接受化疗26(72.2)158(80.6)1.3050.266
), ArticleFig(id=1198589375866045028, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, language=CN, label=表1, caption=

两组GSRC患者临床病理特征比较[例(%)]

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理特征pGSRC组(n=36)mGSRC组(n=196)χ2/ZP
性别4.8590.039
男21(58.3)149(76.0)
女15(41.7)47(24.0)
年龄(岁)2.1830.151
<5523(63.9)99(50.5)
≥5513(36.1)97(49.5)
合并高血压12(33.3)61(31.1)0.0690.846
合并糖尿病9(25.0)53(27.0)0.0651.000
合并贫血6(16.7)44(22.4)0.6010.515
肿瘤部位1.0640.587
上部4(11.1)35(17.9)
中部4(11.1)23(11.7)
下部28(77.8)138(70.4)
肿瘤直径(cm)9.8590.007
≤212(33.3)26(13.3)
2~516(44.4)94(48.0)
>58(22.2)76(38.8)
神经侵犯2.8580.099
是17(47.2)122(62.2)
否19(52.8)74(37.8)
脉管侵犯1.0890.331
是22(61.1)137(69.9)
否14(38.9)59(30.1)
T分期1.9150.173
T110(27.8)35(17.9)
T2-T426(72.2)161(82.1)
N分期4.0050.058
N018(50.0)64(32.7)
N1-N418(50.0)132(67.3)
pTNM分期11.9610.003
Ⅰ18(50.0)48(24.5)
Ⅱ9(25.0)44(22.4)
Ⅲ9(25.0)104(53.1)
淋巴结清扫数目(个)3.2470.197
1~1511(30.6)38(19.4)
15~3022(61.1)125(63.8)
>303(8.3)33(16.8)
CA1990.0001.000
阴性32(88.9)174(88.8)
阳性4(11.1)25(11.2)
CA1251.9370.242
阴性32(88.9)186(94.9)
阳性4(11.1)10(5.1)
Her-20.0091.000
阴性26(72.2)140(71.4)
阳性10(27.8)56(28.6)
BMI(kg/m2)2.4320.296
<18.52(5.6)30(15.3)
18.5~23.925(69.4)122(62.2)
>23.99(25.0)44(22.4)
接受化疗26(72.2)158(80.6)1.3050.266
), ArticleFig(id=1198589375975096935, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, language=EN, label=Tab.2, caption=

Analysis of factors affecting the prognosis of GSRC patients after radical operation (n=232)

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理特征单因素分析多因素分析
HR95%CIPHR95%CIP
性别
男参照--
女1.1160.800~1.5580.517
年龄(岁)
<55参照--
≥551.0100.745~1.3710.947
合并高血压
无参照--
有0.8640.629~1.1890.371
合并糖尿病0.7100.509~0.9910.044
无参照--
有0.6940.498~0.9670.031
合并贫血
无参照--
有0.6730.472~0.9580.028
肿瘤部位
上部参照--
中部0.9500.541~1.6650.857
下部0.8570.470~1.0610.094
肿瘤直径(cm)
≤2参照--
2~51.4470.909~2.3030.119
>51.8861.170~3.0410.009
神经侵犯
无参照--
有0.6010.436~0.8290.002
脉管侵犯
无参照--
有0.5710.404~0.8070.002
病理类型1.6271.034~2.5600.035
pGSRC参照--
mGSRC1.6061.025~2.5160.039
T分期1.9461.255~3.0180.003
T1参照--
T2-T42.1561.396~3.3290.001
N分期
N0参照--
N1-N41.6241.169~2.2560.004
pTNM分期
Ⅰ参照--
Ⅱ0.7140.469~1.0870.116
Ⅲ0.7000.494~0.9900.044
淋巴结清扫数目(个)
1~15参照--
15~300.7140.469~1.0870.116
>300.7000.494~0.9900.044
CA199
阴性参照--
阳性1.5300.967~2.4220.069
CA1252.1441.200~3.8310.010
阴性参照--
阳性2.1421.212~3.7870.009
Her-2
阴性参照--
阳性0.8390.597~1.1780.310
BMI
<18.5参照--
18.5~23.90.9660.615~1.5190.966
>23.91.0700.642~1.7830.796
接受化疗
无参照--
有1.2140.845~1.7430.294
), ArticleFig(id=1198589376105120363, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198558266251903245, language=CN, label=表2, caption=

GSRC患者根治术后预后影响因素分析(n=232)

, figureFileSmall=null, figureFileBig=null, tableContent=
临床病理特征单因素分析多因素分析
HR95%CIPHR95%CIP
性别
男参照--
女1.1160.800~1.5580.517
年龄(岁)
<55参照--
≥551.0100.745~1.3710.947
合并高血压
无参照--
有0.8640.629~1.1890.371
合并糖尿病0.7100.509~0.9910.044
无参照--
有0.6940.498~0.9670.031
合并贫血
无参照--
有0.6730.472~0.9580.028
肿瘤部位
上部参照--
中部0.9500.541~1.6650.857
下部0.8570.470~1.0610.094
肿瘤直径(cm)
≤2参照--
2~51.4470.909~2.3030.119
>51.8861.170~3.0410.009
神经侵犯
无参照--
有0.6010.436~0.8290.002
脉管侵犯
无参照--
有0.5710.404~0.8070.002
病理类型1.6271.034~2.5600.035
pGSRC参照--
mGSRC1.6061.025~2.5160.039
T分期1.9461.255~3.0180.003
T1参照--
T2-T42.1561.396~3.3290.001
N分期
N0参照--
N1-N41.6241.169~2.2560.004
pTNM分期
Ⅰ参照--
Ⅱ0.7140.469~1.0870.116
Ⅲ0.7000.494~0.9900.044
淋巴结清扫数目(个)
1~15参照--
15~300.7140.469~1.0870.116
>300.7000.494~0.9900.044
CA199
阴性参照--
阳性1.5300.967~2.4220.069
CA1252.1441.200~3.8310.010
阴性参照--
阳性2.1421.212~3.7870.009
Her-2
阴性参照--
阳性0.8390.597~1.1780.310
BMI
<18.5参照--
18.5~23.90.9660.615~1.5190.966
>23.91.0700.642~1.7830.796
接受化疗
无参照--
有1.2140.845~1.7430.294
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不同病理亚型胃印戒细胞癌的临床预后分析
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沈亦敏 1 , 李元元 1 , 王舟 1 , 徐伟 1 , 李金洲 1 , 穆彦熹 1 , 姚亚龙 1 , 汪文杰 2 , 陈晓 2, *
解放军医学杂志 | 临床研究 2024,49(7): 747-753
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解放军医学杂志 | 临床研究 2024, 49(7): 747-753
不同病理亚型胃印戒细胞癌的临床预后分析
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沈亦敏1, 李元元1, 王舟1, 徐伟1, 李金洲1, 穆彦熹1, 姚亚龙1, 汪文杰2, 陈晓2, *
作者信息
  • 1兰州大学第二临床医学院，甘肃兰州 730013
  • 2兰州大学第二医院普通外科，甘肃兰州 730030

    • 沈亦敏，硕士研究生，主要从事消化系统肿瘤发病机制方面的研究

通讯作者:

陈晓，E-mail：
Clinical prognosis analysis of gastric signet ring cell carcinoma with different pathological subtypes
Yi-Min Shen1, Yuan-Yuan Li1, Zhou Wang1, Wei Xu1, Jin-Zhou Li1, Yan-Xi Mu1, Ya-Long Yao1, Wen-Jie Wang2, Xiao Chen2, *
Affiliations
  • 1The Second School of Clinical Medicine, Lanzhou University, Lanzhou, Gansu 730013, China
  • 2Department of General Surgery, Lanzhou University Second Hospital, Lanzhou, Gansu 730030, China
出版时间: 2024-07-28 doi: 10.11855/j.issn.0577-7402.2283.2023.0529
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摘要
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目的 探讨不同病理亚型胃印戒细胞癌(GSRC)患者的临床病理特征、预后及其影响因素。方法 回顾性收集2016年1月-2018年12月兰州大学第二医院收治的经病理确诊的232例GSRC患者的临床资料。按照WHO诊断标准进行分类，其中胃纯印戒细胞癌(pGSRC)36例，胃混合印戒细胞癌(mGSRC)196例，随访截至2022年9月30日。应用Kaplan-Meier法进行生存分析，单因素及多因素Cox回归分析影响GSRC患者预后的危险因素。结果 pGSRC和mGSRC患者中位生存时间分别为41.0(6.0~70.0)个月、24.0(2.0~74.0)个月。Kaplan-Meier生存分析显示，合并糖尿病、合并贫血、神经侵犯、脉管侵犯、T分期、N分期、GSRC病理类型、CA125和肿瘤直径可影响GSRC患者根治术后总生存期(OS)(P<0.05)，而Her-2、是否接受化疗等对GSRC患者根治术后OS无明显影响(P>0.05)。单因素Cox回归分析显示，合并糖尿病(P=0.031)、合并贫血(P=0.028)、肿瘤直径>5 cm(P=0.009)、神经侵犯(P=0.002)、脉管侵犯(P=0.002)、病理类型为mGSRC(P=0.039)、T2-T4分期(P=0.001)、N1-N4分期(P=0.004)、pTNM Ⅲ期(P=0.044)、淋巴结清扫数目>30个(P=0.044)和CA125阳性(P=0.009)是GSRC患者根治术后预后的影响因素。多因素Cox回归分析显示，mGSRC病理类型(P=0.035)、T2-T4分期(P=0.003)和CA125阳性(P=0.010)是GSRC患者根治术后预后不良的独立危险因素。结论 与pGSRC相比，mGSRC在确诊时pTNM分期较高，侵袭性较强，中位生存时间较短。mGSRC病理类型、T2-T4分期和CA125阳性是GSRC患者预后不良的独立危险因素。

印戒细胞癌  /  胃纯印戒细胞癌  /  胃混合印戒细胞癌  /  预后

Objective To explore the clinicopathological characteristics, prognosis and influencing factors of different pathological subtypes of gastric signet ring cell carcinoma (GSRC). Methods A retrospective analysis was performed on the clinical data of 232 patients with GSRC collected from January 2016 to December 2018 in Lanzhou University Second Hospital. According to the WHO classification criteria for GSRC, the patients were divided into pure gastric signet-ring cell carcinoma (pGSRC, n=36) and mixed gastric signet-ring cell carcinoma (mGSRC, n=196). The follow-up as of September 30, 2022, the survival analysis was done using Kaplan-Meier method, the univariate and multivariate Cox regression were performed to analyze the risk factors affecting the prognosis of GSRC patients. Results The median survival time of pGSRC and mGSRC patients was 41.0(6.0-70.0) months and 24.0(2.0-74.0) months, respectively. Kaplan-Meier analysis showed that combination with diabetes, anemia, tumor diameter, nerve invasion, lymphovascular invasion, T stage, N stage, GSRC pathological subtype, CA125 and tumor diameter could affect the overall survival (OS) of patients with GSRC after radical gastrectomy (P<0.05), but Her-2, whether adjuvant chemotherapy or not and others elements had no significant effect on OS of GSRC patients after radical gastrectomy (P>0.05). Univariate Cox regression analysis showed that the combination with diabetes (P=0.031), anemia (P=0.028), tumor diameter >5 cm (P=0.009), nerve invasion (P=0.002), lymphovascular invasion (P=0.002), mGSRC pathological type (P=0.039), T2-T4 stage (P=0.001), N1-N4 stage (P=0.004), pTNM stage Ⅲ (P=0.044), the number of lymph node metastasis >30 (P=0.044) and CA125 positive (P=0.009) were related to the prognosis of patients with GSRC after radical gastrectomy. Multivariate Cox regression analysis showed that mGSRC pathological type (P=0.035), T2-T4 stage (P=0.003), CA125 positive (P=0.010) were independent risk factors for poor prognosis of patients with GSRC after radical gastrectomy. Conclusion Compared with pGSRC, patients with mGSRC at diagnosis have higher pTNM stages, more aggressive, and shorter median survival time. mGSRC pathological type, T2-T4 stage, and CA125 positive were all independent factors affecting the prognosis of patients with GSRC.

signet ring cell carcinoma  /  pure gastric signet-ring cell carcinoma  /  mixed gastric signet-ring cell carcinoma  /  prognosis
沈亦敏, 李元元, 王舟, 徐伟, 李金洲, 穆彦熹, 姚亚龙, 汪文杰, 陈晓. 不同病理亚型胃印戒细胞癌的临床预后分析. 解放军医学杂志, 2024 , 49 (7) : 747 -753 . DOI: 10.11855/j.issn.0577-7402.2283.2023.0529
Yi-Min Shen, Yuan-Yuan Li, Zhou Wang, Wei Xu, Jin-Zhou Li, Yan-Xi Mu, Ya-Long Yao, Wen-Jie Wang, Xiao Chen. Clinical prognosis analysis of gastric signet ring cell carcinoma with different pathological subtypes[J]. Medical Journal of Chinese People’s Liberation Army, 2024 , 49 (7) : 747 -753 . DOI: 10.11855/j.issn.0577-7402.2283.2023.0529
正文
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胃癌是全球第五大常见肿瘤，居全球癌症相关死亡原因第3位，也是我国最常见的消化道肿瘤[1]。按组织病理学分类，胃癌大多数为胃腺癌。胃腺癌细胞在组织学上分为分化型与未分化型，前者包括乳头状腺癌和管状腺癌，后者包括低分化腺癌和印戒细胞癌[2]。印戒细胞癌占原发性胃癌的3.4%~39.0%，其特征为肿瘤细胞质内黏蛋白将细胞核推向外周，是高度恶性低分化癌[3]。近年来尽管如幽门螺杆菌感染治疗方法和内镜等技术的发展[4]，使得胃癌总体发病率有所下降，但有研究显示，胃印戒细胞癌(gastric signet ring cell carcinoma，GSRC)在亚洲国家、欧洲国家和美国的发病率却逐渐上升[5]。GSRC患者的预后目前仍存在争议，有学者认为，与腺癌相比，GSRC分化程度低、侵袭性强，容易发生转移，恶性程度高，且对放化疗反应不佳[6-7]，但也有学者持不同意见[8]，因此，探究印戒细胞癌的病理亚型对胃癌诊治具有重要临床价值。根据WHO诊断标准对GSRC进行分类[9]，将印戒细胞占比相对较高(>50%)的病例定义为胃纯印戒细胞癌(pure gastric signet ring cell carcinoma，pGSRC)，将印戒细胞占比相对较低(10%~50%)的病例定义为胃混合印戒细胞癌(mixed gastric signet ring cell carcinoma，mGSRC)[10]。目前关于pGSRC与mGSRC的研究报道鲜少。因此，本研究回顾性分析不同病理亚型GSRC的临床特征和预后，以期加深对GSRC的认识。
1 资料与方法
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1.1 研究对象
以“胃恶性肿瘤”和“印戒细胞癌”为关键词，检索兰州大学第二医院病案系统，收集2016年1月-2018年12月经病理确诊的232例GSRC患者的临床资料进行回顾性分析。纳入标准：(1)行根治性手术治疗；(2)病理诊断为mGSRC或pGSRC。排除标准：(1)术后发生并发症导致生存时间<30 d；(2)有其他恶性肿瘤病史；(3)有远处转移或其他部位来源的肿瘤侵袭；(4)随访资料缺失。根据病理诊断结果将患者分为mGSRC组(n=196)与pGSRC组(n=36)。
1.2 资料收集
收集患者的年龄、性别、既往疾病史、术前血清糖蛋白抗原199(carbohydrate antigen 199，CA199)、CA125、病理类型、脉管侵犯、神经侵犯、肿瘤部位、肿瘤直径、治疗方式、T分期、N分期、淋巴结清扫数目、人表皮生长因子受体2(human epidermal growth factor receptor 2，Her-2)、首诊症状等临床资料。关于胃癌肿瘤部位，上部包括食管胃结合部、贲门和胃底，中部指胃体部，下部指胃窦、幽门部。病理学TNM分期参考第8版国际抗癌联盟(Union for International Cancer Control，UICC)及美国癌症联合委员会(American Joint Committee on Cancer，AJCC)胃腺癌分级系统[11]。本研究获兰州大学第二医院伦理委员会审批(2022A-214)。
1.3 术后随访
采用门诊复查、电话和病例资料查询等方式进行随访，以死亡日期或随访截止时间(2022年9月30日)为截止日期，随访内容包括临床、实验室检查结果，化疗情况及生存状态。
1.4 GSRC患者胃癌根治术后生存分析
使用Kaplan-Meier法进行生存分析，生存率差异的比较采用log-rank检验。
1.5 GSRC患者根治术后预后影响因素分析
采用单因素和多因素Cox比例风险模型分析GSRC患者根治术后预后的影响因素。
1.6 统计学处理
采用SPSS 26.0软件进行统计分析，GraphPad Prism 9.0软件制图。计数资料以例(%)表示，连续变量转换为分类变量，两组间比较采用χ2检验或Fisher精确概率检验。P<0.05为差异有统计学意义。
2 结果
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2.1 两组临床病理特征比较
共检索到253例患者，排除有其他恶性肿瘤3例，有远处转移5例，发生严重并发症致生存时间<30 d 3例，以及随访资料缺失10例，最终纳入232例。
232例中，男170例(73.3%)，女62例(26.7%)，男女比例2.74∶1，发病中位年龄为54(23~84)岁，中位生存时间为26.5(2.0~74.0)个月。pGSRC患者36例(15.5%，36/232)，男21例(58.3%，21/36)；发病年龄≥55岁者占36.1%(13/36)，肿瘤原发部位为下部者占77.8%(28/36)。mGSRC患者196例(84.5%，196/232)，男149例(76.0%，149/196)，发病年龄≥55岁者占49.5%(97/196)，肿瘤原发部位为下部者占70.4%(138/196)。
232例中，以腹痛为首诊症状占比最高，为58.6%(136/232)，其次为吞咽不适(13.4%，31/232)、腹部不适(9.9%，23/232)、黑便(8.6%，20/232)、恶心(3.9%，9/232)、纳差乏力(3.4%，8/232)、便血(2.2%，5/232)等。
两组性别、肿瘤直径和pTNM分期差异有统计学意义(P<0.05)，但年龄、合并高血压、合并糖尿病、合并贫血、肿瘤部位、神经侵犯、脉管侵犯、T分期、N分期、淋巴结清扫数目，术前CA125、CA199、BMI、Her-2及是否接受化疗等差异均无统计学意义(P>0.05，表1)。
2.2 GSRC患者胃癌根治术后生存分析
Kaplan-Meier生存分析显示，pGSRC患者的存活率高于mGSRC患者(50.0% vs. 48.0%，P=0.034)，pGSRC、mGSRC患者的中位生存时间分别为41.0(6.0~70.0)个月、24.0(2.0~74.0)个月。合并糖尿病、合并贫血、神经侵犯、脉管侵犯、T分期、N分期、GSRC病理类型、CA125和肿瘤直径影响GSRC患者根治术后总生存期(overall survival，OS) (P<0.05)，而Her-2、是否接受化疗等对GSRC患者根治术后OS无明显影响(P>0.05，图1)。
2.3 GSRC患者胃癌根治术后预后影响因素分析
单因素Cox回归分析结果显示，合并糖尿病(P=0.031)、合并贫血(P=0.028)、肿瘤直径>5 cm(P=0.009)、神经侵犯(P=0.002)、脉管侵犯(P=0.002)、病理类型为mGSRC(P=0.039)、T2-T4分期(P=0.001)、N1-N4分期(P=0.004)、pTNM Ⅲ期(P=0.044)、淋巴结清扫数目>30个(P=0.044)和CA125阳性(P=0.009)是GSRC患者根治术后预后的影响因素；而Her-2、是否接受化疗等对GSRC患者根治术后预后无明显影响(P>0.05，表2)。
将单因素分析中有统计学差异的因素纳入多因素Cox比例风险模型，结果显示，合并糖尿病(P=0.044)是GSRC患者根治术后预后的保护因素，mGSRC病理类型(P=0.035)、T2-T4分期(P=0.003)和CA125阳性(P=0.010)是GSRC患者根治术后预后不良的独立危险因素(表2)。
3 讨论
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胃癌是全球最常见的消化系统肿瘤之一，以东亚国家发病率最高[3]。GSRC作为一种独特的胃癌类型，在胃癌中的比例不断上升[12]。GSRC依据组织学分型被划分为低分化肿瘤，通常发现时已是晚期[8]。所有分期GSRC患者5年生存率仅51%，而中分化和高分化肿瘤患者5年生存率为76%[13]，因此GSRC患者的预后更差[8,14]。根据WHO诊断标准中的GSRC分类[9]，本研究对232例GSRC患者(36例pGSRC和196例mGSRC)进行深入分析，结果显示，pGSRC和mGSRC患者多为中青年男性，肿瘤部位多位于下部，肿瘤直径多>2 cm。与pGSRC患者相比mGSRC患者中肿瘤直径>2 cm者、神经侵犯者及淋巴结转移数目>15个者占比均较高，这可能与mGSRC患者预后不良有关。GSRC患者发病隐匿，首发症状多为腹痛、吞咽不适和腹部不适，症状无特异性。大部分患者确诊时已是pTNM分期Ⅱ期及以上，尤其是mGSRC更为显著(Ⅱ期和Ⅲ期各占22.4%和53.1%)，提示尽早进行胃镜检查对GSRC的诊断及预后极为重要。
有研究发现，不同病理亚型和肿瘤直径>2 cm是早期GSRC患者淋巴结转移的独立危险因素[15]。本研究发现，病理亚型与GSRC患者的预后有关，且是GSRC患者预后的独立危险因素，与其他研究结果一致[10]。本研究结果显示，与mGSRC比较，pGSRC患者的死亡风险比降低(HR=1.606，95%CI 1.025~2.516)；生存分析发现，GSRC不同病理亚型与患者术后OS密切相关，病理分型为pGSRC的患者存活率较高(50.0% vs. 48.0%，P=0.034)。Kim等[16]发现，与pGSRC患者比较，mGSRC患者脉管侵犯率较高，且邻近黏膜肠上皮化生较多，这可能是淋巴结转移率较高的原因；此外，该研究还发现pGSRC可能多表现为胃表型，而mGSRC可能与肠道免疫表型更加相关。有研究发现，高度侵袭行为如增殖、凋亡、血管生成、黏蛋白分泌、细胞黏附等，与Ki-67指数、细胞外基质金属蛋白酶诱导剂、血管内皮生长因子表达增加有关，这可能是mGSRC侵袭性较高的原因[17]。也有研究发现，mGSRC经常表现为CpG岛的高甲基化，这可能也是mGSRC侵袭性较高的原因[7]。糖尿病是包括胃癌在内多种癌症的危险因素[18]；一项纳入17项观察性研究的Meta分析显示糖尿病会使胃癌的发生率增高19%[19]，其原因可能是高血糖可直接引起DNA损伤或者通过产生活性氧导致DNA损伤，同时糖尿病患者的高胰岛素血症和胰岛素样生长因子水平升高也可能导致癌症的发生[20]。但本研究中糖尿病是GSRC患者预后的保护因素。同时本研究还发现，血清标志物CA125阳性是GSRC患者预后的独立危险因素，CA125不仅可作为GSRC诊断的标志物，还与肿瘤复发、侵袭和转移有关，且其检测操作简单、成本低和易于推广，可为临床医师制定治疗方案提供参考。
目前，GSRC围手术期的化疗耐药性和实用性，以及术后化疗对GSRC患者的作用仍存在争议。有研究发现，与非GSRC患者相比，术前和术后化疗对GSRC患者(n=899)生存率无明显影响[21]；859例Ⅱ-Ⅲ期GSRC患者术后化疗并未提高生存率[22]。也有研究发现，2815例Ⅳ期GSRC患者术后化疗可延长生存期[23]。本研究发现，是否接受化疗对GSRC患者的预后无明显影响(P=0.286)，这可能与印戒细胞癌对化疗不敏感有关[24]，但仍需进一步探讨。
Her-2属于人表皮类生长因子受体家族，其表达与胃癌患者预后的关系尚不明确。一项多中心研究显示，Her-2阳性胃癌患者的预后明显优于阴性患者[25]。但也有研究显示，Her-2的表达与胃癌根治术患者的预后无关[26]，与本研究结果一致。因此，Her-2与胃癌患者预后的关系仍需深入研究，且可细分到不同胃癌病理类型。笔者建议，在病理报告中应呈现印戒细胞的占比，以为临床医师制定后续治疗方案提供参考。
本研究仍存在一定局限性：为单中心回顾性研究，无法避免回顾性偏倚及随访依从性等造成的偏倚；未纳入血清学指标、饮食习惯、地域和民族等数据，因此仍需进一步研究阐明这些因素与胃印戒细胞癌病理亚型的关系。后续可进行大规模、多中心、前瞻性和队列研究进一步探讨不同化疗方案对GSRC患者的影响。此外，未来可能需要进一步研究不同的胃癌病理亚型的影响，以此指导临床医师为胃癌患者提供个体化的医疗服务。
综上所述，pGSRC与mGSRC患者肿瘤直径、pTNM分期及OS存在明显差异。与pGSRC患者相比，mGSRC患者具有较高的淋巴结转移率、血清CA125阳性率和较强的侵袭性，中位生存时间更短。该结果加深了人们对GSRC的认识，有助于临床医师根据GSRC不同病理分型制定不同的治疗方案。
基金
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  • 甘肃省青年科技基金项目(21JR7RA424)
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2024年第49卷第7期
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doi: 10.11855/j.issn.0577-7402.2283.2023.0529
  • 接收时间：2022-11-03
  • 首发时间：2025-11-21
  • 出版时间：2024-07-28
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  • 收稿日期：2022-11-03
  • 录用日期：2023-01-12
基金
Gansu Provincial Youth Science and Technology Fund(21JR7RA424)
甘肃省青年科技基金项目(21JR7RA424)
作者信息
    1兰州大学第二临床医学院，甘肃兰州 730013
    2兰州大学第二医院普通外科，甘肃兰州 730030

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