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临床研究
肿块型肝内胆管细胞癌的MRI增强特征与相关病理及预后
魏友平 张顺 宋美娜 吴巍 张立洪

WEI Y P, ZHANG S, SONG M N, et al. MRI enhanced features, pathology and prognosis of intrahepatic mass-forming cholangiocarcinoma[J]. Chin J Magn Reson Imaging, 2023, 14(8): 68-72.引用本文:魏友平, 张顺, 宋美娜, 等. 肿块型肝内胆管细胞癌的MRI增强特征与相关病理及预后[J]. 磁共振成像, 2023, 14(8): 68-72. DOI:10.12015/issn.1674-8034.2023.08.011.


[摘要] 目的 探讨肿块型肝内胆管细胞癌(intrahepatic cholangiocarcinoma, ICC)MRI增强特征与相关病理及预后间的关系。材料与方法 回顾性分析2008年1月至2020年6月中国医科大学航空总医院收治的肿块型ICC患者病例69例,其中男62例,女7例。根据肿块型ICC MRI强化方式不同分为3组:渐进强化组25例,周边强化组24例,富血供组20例。分析3组MRI表现及其病理特点,并比较三组生存率方面的差异。结果 肿块型ICC MRI强化程度与肿瘤细胞、纤维组织以及其他组织,如黏液、组织坏死等所构成比例不同有关。所有患者中位生存时间为35.9个月(95% CI:17.4~54.6),1年总生存率为75.9%,3年总生存率为46.7%,5年总生存率为23.4%。渐进强化组患者1、3和5年生存率分别为75.0%、41.3%和20.6%,周边强化组患者1、3和5年生存率分别为71.8%、47.9%和18.0%,富血供组患者1、3和5年生存率分别为83.3%、51.3%和32.1%;组间Log-rank检验结果显示三组患者间生存率无显著差异(χ2=1.117,P=0.572);三组间1年生存率无显著差异(F=0.50,P=0.616),3年生存率亦无显著差异(F=0.632,P=0.725),5年生存率有显著差异(F=5.93,P=0.007),富血供组优于渐进强化组(P=0.013)和周边强化组(P=0.001)。结论 肿块型ICC的MRI不同增强方式有其相应的病理基础;不同强化方式与预后间可能有相关性,富血供型ICC可能在5年生存率方面更有优势。
[Abstract] Objective To explore the relationship between MRI enhanced features, pathological basis and prognosis of intrahepatic mass-forming cholangiocarcinoma (IMCC).Materials and Methods The data of intrahepatic cholangiocarcinoma (ICC) patients admitted to Aviation General Hospital of China Medical University from January 2008 to June 2020 were retrospectively analyzed. A total of 69 cases of IMCC were included in the study including 62 males and 7 females. According to the different MRI enhancement methods of IMCC, they were divided into 3 groups: progressive enhancement group (25 cases), peripheral enhancement group (24 cases) and rich blood supply group (20 cases). The MRI findings and pathological characteristics of the three groups were analyzed, and the survival rate of the three groups was compared.Results The enhancement degree of MRI was related to the proportion of tumor cells, fibrous tissues, and other tissues ( such as mucus and tissue necrosis). The median survival time of all patients was 35.9 months (95% CI: 17.4-54.6), the 1-year cumulative survival rate was 75.9%, the 3-year cumulative survival rate was 46.7%, and the 5-year cumulative survival rate was 23.4%. The 1-year, 3-year, and 5-year survival rates of patients in progressive enhancement group were 75.0%, 41.3%, and 20.6%, those in peripheral enhancement group were 71.8%, 47.9%, and 18.0%, and those in rich blood supply group were 83.3%, 51.3%, and 32.1%, respectively. Log rank test showed that there was no significant difference in survival rate among the three groups (χ2=1.117, P=0.572). There was no significant difference in 1-year survival rate among the three groups (F=0.50, P=0.616), and no significant difference in 3-year survival rate (F=0.632, P=0.725). There was a significant difference in 5-year survival rate (F=5.93, P=0.007). The rich blood supply group was superior to the progressive reinforcement group (P=0.013) and the peripheral reinforcement group (P=0.001).Conclusions Different enhancement modes of MRI in IMCC have their corresponding pathological basis. There may be a correlation between different reinforcement methods and prognosis, and blood supply rich ICC may have an advantage in 5-year survival rate.
[关键词] 肝脏肿瘤;肝内胆管细胞癌;病理;预后;磁共振成像
[Keywords] liver tumor;intrahepatic cholangiocarcinoma;pathology;prognosis;magnetic resonance imaging

魏友平 1   张顺 1   宋美娜 1   吴巍 2   张立洪 2*  

1 中国医科大学航空总医院影像科,北京 100012

2 扬州大学附属医院肝胆外科,扬州 225012

通信作者:张立洪,E-mail:zhanglh@yzu.edu.cn

作者贡献声明:张立洪设计本研究的方案,对稿件重要的智力内容进行了修改;魏友平起草和撰写稿件,获取、分析或解释本研究的数据;张顺、吴巍、宋美娜获取、分析或解释本研究的数据,对稿件重要的智力内容进行了修改;吴巍获得国家自然科学基金项目支持;全体作者都同意发表最后的修改稿,同意对本研究的所有方面负责,确保本研究的准确性和诚信。


基金项目: 国家自然科学基金 82001964
收稿日期:2022-10-17
接受日期:2023-07-27
中图分类号:R445.2  R735.8 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.08.011
引用本文:魏友平, 张顺, 宋美娜, 等. 肿块型肝内胆管细胞癌的MRI增强特征与相关病理及预后[J]. 磁共振成像, 2023, 14(8): 68-72. DOI:10.12015/issn.1674-8034.2023.08.011.

0 前言

       肝内胆管细胞癌(intrahepatic cholangiocarcinoma, ICC)是排名第二位的肝脏原发性恶性肿瘤,约占10%~20%,近年发病率有持续性上升趋势[1, 2]。我国是ICC的高发地区,其中肝内胆管结石和病毒性肝炎是ICC的主要危险因素[2]。日本肝癌研究会根据形态学将其分为肿块型、管周浸润型、管内生长型,以及混合型,其中绝大多数为肿块型[3, 4]

       ICC早期症状无特异性,大部分患者就诊时已处于中晚期。以往ICC的治疗主要是以手术为主的综合治疗[5, 6]。近年来随着免疫以及分子靶向药物的问世,ICC的治疗方式也发生了改变[7, 8, 9]。尽管如此,ICC的预后仍不佳,5年累积生存率仅为7%~20%[10, 11]。因而,早期准确诊断及治疗非常重要。增强MRI检查是诊断ICC重要手段之一;肿块型ICC可有多种强化方式,动脉期大面积明显强化的肿块型ICC相对较少见且误诊率高[12],因此对其认识有待加强。有研究发现,肿块型ICC影像学表现多样化与病理基础是相关的,且不同的影像学表现其预后可能也不同[13, 14]。但现有的研究多集中在影像学与病理,或影像学与预后两者的关系方面,而MRI不同的强化表现同时与病理基础及其预后三方面的研究未见报道。为了解肿块型ICC在磁共振上不同影像特征与病理的关系,以及对预后的影响,本研究拟采用回顾性分析的方法对肿块型ICC在磁共振上不同的强化方式与病理及临床预后三者间进行分析,现报道如下。

1 材料与方法

1.1 一般资料

       本回顾性研究遵守《赫尔辛基宣言》,并经中国医科大学航空总医院伦理委员会批准,免除受试者知情同意,批准文号:HK2022-37。纳入标准:(1)标本经术后病理证实;(2)完成增强MRI检查;(3)病理及影像符合肿块型ICC;(4)AJCC第八版TNM分期为Ⅰ、Ⅱ及Ⅲ期,且能手术切除。排除标准:(1)合并有其他恶性肿瘤;(2)图像质量不佳不能用于分析;(3)资料不全;(4)失访。回顾性分析2008年1月至2020年6月我院收治的ICC患者的病例资料92例,其中18例失访,2例合并有其他恶性肿瘤,3例资料不全,最终有69例肿块型ICC纳入研究。男62例,女7例;年龄35~82(57.1±13.4)岁。根据肿块型ICC MRI强化方式不同,分为3组,渐进强化组25例,周边强化组24例,富血供组20例。

1.2 检查方法及分析

       所有患者MRI扫描均采用Siemens Novus 1.5 T或SIEMENS SKYRA 3.0 T超导MRI系统,采用8通道或18通道相控阵表面线圈,常规扫描T1WI、T2WI及DWI序列,动态增强序列使用3D-梯度回波容积插值屏息系列(3D-VIBE)扫描,相关技术参数见表1。用高压注射器(山东威高集团有限公司,MRI-ME 60/110)按照2.5~3.0 mL/s的速率,0.2 mmol/kg的剂量注射Gd-DTPA对比剂,进行3期增强扫描。采集25 s动脉期、60 s门脉期、190 s平衡期的图像。

       所有扫描后的图像均由两名工作10年以上的副高职称医师判读,意见不一致时经讨论后达成一致意见。根据肿瘤不同的强化方式,分为3种强化类型:动脉期肿瘤周边出现轻度强化,中央强化不明显,随着时间延迟中央开始强化并逐渐加强,呈整体渐进性高强化,为渐进强化组;动脉期整个肿块明显高强化,而后强化减退,为富血供组;肿块周边不规则高强化,而中央始终无明显强化,为周边强化组。

表1  MRI扫描技术参数
Tab. 1  Technical parameters of MRI scanning

1.3 治疗方法

       所有患者均接受根治性肿瘤切除,包括腹腔淋巴结清扫,术后辅助化疗未采取统一方案。

1.4 病理分析

       肿瘤标本获取后,经标本固定、石蜡包埋和石蜡切片等过程,充分取材,HE染色,由1名具有10年以上丰富工作经验的副高职称的病理医师阅片,观察成活肿瘤细胞、纤维间质、凝固性坏死并对肿瘤细胞分化程度进行分级。

1.5 随访方法

       所有患者均采用电话随访,随访截止时间为2021年12月31日。平均随访时间为52(18~90)个月。事件终点:总体生存时间以患者死亡或随访截止日期为事件终点。

1.6 统计学分析

       应用SPSS 26.0统计软件进行分析,计量资料以均数±标准差(x¯±s)表示,采用t检验,计数资料比较采用χ2检验,生存率计算采用寿命表法,生存曲线采用Kaplan-Meier法绘制,组间比较采用Log-rank检验,率的比较采用ANOVA,组间两两比较用Bonferroni法。P<0.05为差异有统计学意义。

2 结果

2.1 一般临床资料

       三组患者在性别、年龄、合并HBV或HCV感染、肿瘤大小、TNM分期及淋巴结转移等方面差异均无统计学意义(P>0),其中术后辅助化疗未采取统一方案(表2)。

表2  69例肿块型肝内胆管细胞癌患者一般临床资料
Tab. 2  Clinical data of patients with intrahepatic mass-forming cholangiocarcinoma of 69 general

2.2 肿块型ICC强化方式及其病理基础

       所有69例患者术前MRI均给出了ICC的诊断,并根据肿瘤不同的强化方式,分为3组:(1)渐进强化组(25例),其病理表现为大量的恶性肿瘤细胞和少许纤维组织位于肿瘤的外周,而肿瘤中央区肿瘤细胞比较少,主要是纤维组织。肿瘤细胞是肿瘤早期强化的病理基础,而纤维组织会导致延迟强化,这是因为对比剂进入纤维组织中相对缓慢,但存留时间较长(图1)。(2)富血供组(20例),病理上可见大量的肿瘤细胞和少量的纤维组织(图2)。(3)周边强化组(24例),病理上中央无强化区由坏死组织和肿瘤细胞分泌的黏液等构成(图3)。

图1  男,52岁,肝内胆管细胞癌(ICC)渐进强化病例,术后存活2年6个月。肝脏左叶病灶T2WI呈低、稍高信号,T1WI呈低信号(1A、1B),增强后动脉期病灶轻度不均匀强(1C),静脉期及平衡期进一步不均匀强化(1D、1E)。病理图(HE ×100)示纤维化背景中可见腺癌浸润(1F)。
Fig. 1  Male, 52 years old, intrahepatic cholangiocarcinoma (ICC) progressive enhancement, survive for 2 years and 6 months after surgery. Liver lesion in the left lobe shows low or slightly high signal on T2WI, low signal on T1WI (1A, 1B), mild uneven enhancement in the arterial phase after enhancement (1C), and further uneven enhancement in the venous and equilibrium phases (1D, 1E). Pathological examination (HE ×100) shows that adenocarcinoma infiltration can be seen in the fibrotic background (1F).
图2  女,63岁,肝内胆管细胞癌(ICC)富血供病例,术后存活5年4个月。肝脏右叶病灶T2WI呈高信号,T1WI呈低信号(2A、2B),增强后动脉期病灶明显强化(2C),静脉期及平衡期显示病灶强化逐渐减退(2D、2E)。病理图(HE ×100)示癌细胞成巢状、条索状排列,细胞异型明显,胞浆嗜酸(2F)。
Fig. 2  Female, 63 years old, intrahepatic cholangiocarcinoma (ICC) abundant blood supply, survive for 5 years and 4 months after surgery. The lesion in the right lobe of the liver shows high signal on T2WI and low signal on T1WI (2A, 2B). After enhancement, the lesion shows significant enhancement in the arterial phase (2C), and gradually decreased enhancement in the venous and equilibrium phases (2D, 2E). Pathological examination (HE ×100) shows that the cancer cells are arranged in a nest like and strip like manner, with obvious cell abnormalities and eosinophilic cytoplasm (2F).
图3  男,65岁,肝内胆管细胞癌(ICC)周边强化病例,术后存活3年5个月。肝脏内病灶T2WI呈高信号,T1WI呈低信号(3A、3B),动脉期增强后边缘轻度强化,中央未见强化(3C),静脉期及平衡期仍显示周边强化,而中央区始终未强化(3D、3E)。病理图(HE ×100)示坏死背景中可见残存肿瘤细胞核(3F)。
Fig. 3  Male, 65 years old, intrahepatic cholangiocarcinoma (ICC) peripheral enhancement, survive for 3 years and 5 months after surgery. The lesions in the liver shows high signal intensity on T2WI and low signal intensity on T1WI (3A, 3B), with slight enhancement at the edge after arterial phase enhancement, but no enhancement at the center (3C), peripheral enhancement is still shown in the venous phase and balance phase, while the central area remained unreinforced (3D, 3E). Pathological examination (HE ×100) shows that residual tumor nuclei can be seen in the background of necrosis (3F).

2.3 生存分析结果

       生存分析显示,69例患者中位生存时间为35.9个月(95% CI:17.4~54.6),1年累积生存率为75.9%,3年累积生存率为46.7%,5年累积生存率为23.4%(图4)。渐进强化组患者1、3和5年生存率分别为75.0%、41.3%和20.6%,周边强化组患者1、3和5年生存率分别为71.8%、47.9%和18.0%,富血供组患者1、3和5年生存率分别为83.3%、51.3%和32.1%;组间Log-rank检验结果显示三组患者间总的生存曲线未见显著差异(χ2=1.117,P=0.572)(图5);三组间:1年生存率无显著差异(F=0.50,P=0.616),3年生存率亦无显著差异(F=0.632,P=0.725),5年生存率有显著差异(F=5.93,P=0.007),富血供组优于渐进强化组(P=0.013)和周边强化组(P=0.001),渐进强化组和周边强化组无显著差异(P=0.538)。

图4  肿块型肝内胆管细胞癌患者的总体生存曲线。
图5  不同分组的肿块型肝内胆管细胞癌患者的生存曲线。
Fig. 4  Overall survival curve of patients with intrahepatic mass-forming cholangiocarcinoma.
Fig. 5  Survival curves of patients with intrahepatic mass-forming cholangiocarcinoma in different groups.

3 讨论

       本研究通过回顾性分析肿块型ICC MRI不同的强化方式与其病理及预后间的关系,发现肿块型ICC MRI强化方式主要有三种,分别为渐进强化、周边强化及富血供,不同的强化方式与肿瘤细胞、纤维组织以及其他组织,如黏液、组织坏死等所构成比例不同有关。三组患者1、3和5年总的生存曲线未见显著差异,但富血供组可能在5年生存率方面更具优势。既往的研究多集中在影像学与病理,或影像学与预后两者的关系方面,而本研究则同时对MRI不同的强化方式与病理基础及其预后方面进行了研究。

3.1 MRI强化方式与病理

       本研究表明,肿块型ICC在MRI及其增强扫描上有一定的特点。结合病理特征分析,肿块强化程度跟肿瘤细胞是否丰富有关[15]。富血供型含有丰富的肿瘤细胞及少量的纤维组织,周边强化型是肿块周边有肿瘤细胞,中心为黏液或坏死组织,而逐渐强化型肿块周围肿瘤细胞富集,而中央为纤维组织。这些组织学和生长特征反映在成像中。既往有研究显示,MRI不同显像方式有助于预测肿块型ICC病理分级[16]。MRI作为一种诊断工具,可以同时进行形态学及功能成像,对肝脏病变的描述比CT更充分,因而,对肝脏占位性病变的诊断及鉴别诊断要优于CT[17, 18, 19]

3.2 MRI强化方式与预后

       本研究发现,在肿块型ICC的三种MRI的增强显像模式分组总生存率方面,似乎富血供组的5年生存率要高于另外两组,但统计学方面并没有显著差异,这可能与入组的病例数较少有关。鉴于ICC发病机制和生物学行为的异质性和复杂性,影像学特征的差异可能直接反映不同的生物学行为[20, 21, 22]。事实上,已经有一些研究已发现了肿块型ICC的影像学特征与其预后或临床病理因素之间的关系[12, 23, 24, 25, 26]。MIN等[27]研究发现,富血供型ICC在总体生存和远期复发方面优于其他两型,这与富血供型患者区域淋巴结转移率较低,血管浸润率低,以及较小的肿瘤大小有关。这表明具有不同强化模式的肿块型ICC可能呈现不同的临床特征以及生物学行为,因而可能最终影响患者预后。当然,影像学特征与临床预后之间的关系也并不完全一致[12, 23, 24, 25, 26, 27]

3.3 本研究的局限性

       本文尚存在一定的局限性:首先,本研究为回顾性研究,我们未将全部患者纳入分析,只纳入了具有随访结果的患者,这会导致选择偏倚;其次,本研究为单中心样本,且本研究中纳入分析的每组病例数较少,亦会影响结果分析;最后,本研究在生存分析时未能对影响预后的相关因素,如TNM分期、淋巴结转移情况、肿瘤大小,以及血管侵犯等因素进行分层分析,这些局限性可能对研究结果产生一定的影响。下一步我们将通过前瞻性的观察,联合多家医院,进行大样本的研究,分析肿块型ICC影像学的特点与病理及临床预后间的关系。

4 结论

       本研究首次将肿块型ICC的影像与病理,及临床预后三者间一起研究分析,结果显示,肿块型ICC根据MRI不同的增强方式主要分为富血供型、渐进强化型和周边强化型,不同的强化方式与肿瘤组织中肿瘤细胞、纤维组织及其他组分等构成的病理基础相关;不同强化方式与预后间的关系可能有一定的相关性,富血供型ICC可能在5年生存率方面更有优势。

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