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综述
多模态MRI在肝内肿块型胆管细胞癌诊疗中的研究进展
陈爽 张红梅

Cite this article as: Chen S, Zhang HM. Research progress of multimodality MRI in the diagnosis and treatment of intrahepatic mass-forming cholangiocarcinoma[J]. Chin J Magn Reson Imaging, 2022, 13(5): 158-161.本文引用格式:陈爽, 张红梅. 多模态MRI在肝内肿块型胆管细胞癌诊疗中的研究进展[J]. 磁共振成像, 2022, 13(5): 158-161. DOI:10.12015/issn.1674-8034.2022.05.034.


[摘要] 肝内胆管细胞癌(intrahepatic cholangiocarcinoma,ICC)是仅次于肝细胞癌的肝脏原发恶性肿瘤,近几年发病率逐渐增加。根据大体形态和生长方式,可将ICC分为肿块型、胆管内生长型和沿胆管浸润型,其中以肝内肿块型胆管细胞癌(intrahepatic mass-forming cholangiocarcinoma,IMCC)最常见。由于治疗方式和预后表现有别于其他肝脏恶性肿瘤,因此,较早且较准确的诊断对选择最佳的治疗具有重要意义。MRI目前是治疗前对ICC进行诊断、分期和预后评估的首选影像检查方法。尤其是多模态MRI技术,可以综合各模态的优点,反映肿瘤组织微观结构的改变,有助于肿瘤的定性诊断及肿瘤微环境的评估,从而间接反映肿瘤的恶性程度、浸润范围等与预后相关的一系列特征。常用的多模态MRI技术包括扩散加权成像、动态对比增强磁共振成像等。现对多模态MRI的不同技术及其在ICC的研究进展进行综述。
[Abstract] Intrahepatic cholangiocarcinoma (ICC) is the primary malignant tumor of liver, second only to hepatocellular carcinoma (HCC), and its incidence increases gradually in recent years. ICC can be divided into mass-forming, periductal-infiltrating, and intraductal-growing patterns according to their gross morphology and growth pattern and intrahepatic mass-forming cholangiocarcinoma is most common. As the treatment and prognosis are different from other liver malignancies, early and accurate diagnosis is of great significance for optimal treatment. MRI is currently the preferred imaging method for diagnosis, staging, and prognosis of ICC before treatment. In particular, multimodal MRI technology can reflect the changes of tumor tissue microstructure by integrating the advantages of various modes, which is helpful for the qualitative diagnosis of tumor and the evaluation of tumor microenvironment, thus indirectly reflecting a series of prognostic characteristics such as the degree of malignancy and the scope of invasion of tumor. The commonly used multimodal MRI techniques including diffusion-weighted imaging, dynamic contrast enhanced magnetic resonance imaging. In this article, the different techniques of multimodal MRI and their research progress in ICC are reviewed.
[关键词] 多模态磁共振成像;扩散加权成像;动态对比增强磁共振成像;肝内肿块型胆管细胞癌;诊断;预后
[Keywords] multimodal magnetic resonance imaging;diffusion weighted imaging;dynamic contrast enhanced magnetic resonance imaging;intrahepatic mass-forming cholangiocarcinoma;diagnosis;prognosis

陈爽    张红梅 *  

国家癌症中心/国家肿瘤临床医学研究中心/中国医学科学院北京协和医学院肿瘤医院影像诊断科,北京 100021

张红梅,E-mail:13581968865@163.com

作者利益冲突声明:全部作者均声明无利益冲突。


收稿日期:2021-09-21
接受日期:2022-04-11
中图分类号:R445.2  R735.8 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.05.034
本文引用格式:陈爽, 张红梅. 多模态MRI在肝内肿块型胆管细胞癌诊疗中的研究进展[J]. 磁共振成像, 2022, 13(5): 158-161. DOI:10.12015/issn.1674-8034.2022.05.034

       肝内胆管细胞癌(intrahepatic cholangiocarcinoma,ICC)起源于第二级胆管到近端胆管的上皮细胞,是仅次于肝细胞癌(hepatocellular carcinoma,HCC)的第二大原发性肝内恶性肿瘤,ICC的发病率在泰国、韩国和中国等东方国家最高,但其发病率和死亡率在全球范围内都在增加[1, 2]。日本肝癌研究组根据形态学特征将ICC分为肿块型、管周浸润型和管内生长型[3],三者的病因、危险因素、预后、临床和治疗管理各不相同,其中以肝内肿块型胆管细胞癌(intrahepatic mass-forming cholangiocarcinoma,IMCC)最常见,约占ICC的78%[4]。目前认为,将肿瘤完整地切除是患者获得长期生存的唯一治疗方式[5]。但由于ICC在早期缺乏典型的临床症状,大多数患者在发现时已经处于中晚期,只有不到三分之一的患者符合手术标准,而且术后复发率为50%~70%,五年生存率仅约4%~35%[6, 7]。因此,准确诊断及治疗前评估对于制订个体化的治疗方案、提高患者总体疗效与生存期至关重要[8]。MRI具有软组织分辨率高、无辐射、多参数成像等特点,由于其高敏感性和特异性,成为ICC诊断、分期和预后评估的首选无创检查方法[9]。多模态MRI技术包括动态对比增强磁共振成像(dynamic contrast enhanced magnetic resonance imaging,DCE-MRI)、扩散加权成像(diffusion weighted imaging,DWI)等,联合两种或两种以上MRI参数可以在时间、空间分辨率上优势互补,既可显示肿瘤解剖形态学特征,又能够反映肿瘤组织微观结构的改变,有助于肿瘤的定性诊断及微环境的评估,从而反映出与肿瘤的恶性程度、浸润范围等与预后相关的一系列特征[10]。本文就多模态MRI在IMCC诊断与预后评估中的研究进展进行综述,以期为临床诊疗决策提供影像学依据。

1 直接MR征象

       IMCC通常起源于肝内小胆管上皮细胞,呈浸润型生长,肿瘤的边缘由致密的癌细胞组成,中心为排列稀疏的癌细胞和丰富的纤维间质成分[3]。肿瘤纤维间质中含有丰富的表达α-平滑肌肌动蛋白的成纤维细胞,也称肿瘤相关成纤维细胞(cancer-associated fibroblasts,CAFs)。CAFs通过分泌生长因子、多种趋化因子以及小分子代谢物,从而促进肿瘤细胞增殖、迁移、侵袭与血管生成[11]。CAFs中α-平滑肌肌动蛋白的阳性表达预示肝内胆管癌患者预后不良,并与淋巴结转移呈正相关[12]。在MRI图像上肿瘤边缘模糊,T1加权像呈低信号,T2加权像多表现为中高信号伴中心低信号,提示内部含纤维成分[13]。其他常见的非特异性表现还包括胆管扩张、肝被膜皱缩、血管侵犯、肝段萎缩、卫星结节和淋巴结转移等[14]。Mao等[15]认为肝内胆管扩张可作为评价肿瘤是否侵犯Glisson鞘的独立预测因子。沿Glisson鞘浸润为ICC最常见的转移方式之一。肿瘤内部丰富的纤维间质成分牵拉邻近的肝组织可表现为肝被膜皱缩,当肿瘤侵犯邻近血管引起肝组织供血障碍时,可导致局部肝叶或肝段的萎缩[13]。相对于HCC来说,血管侵犯在ICC中并不常见。最近的一项荟萃分析表明,ICC是继HCC和混合性HCC之后第三常见的静脉内瘤栓产生的原因[16]。肿瘤侵犯肝被膜或周围门静脉分支小血管可引起肿瘤在肝内的播散,形成卫星结节及肝内转移灶,位于肿瘤边缘的多发卫星结节与肿瘤相互融合,可形成最常见的分叶样外观。淋巴结转移是ICC最显著的恶性特征之一,术前诊断淋巴结转移的主要依据短径大于1 cm、内部坏死和形态不规则来诊断是否存在淋巴结转移[14]。MRI可清晰显示肿瘤的范围与子灶的数目、分布等信息,为临床诊疗提供依据[10]

2 DWI

       DWI是一种检测活体组织细胞内外水分子扩散能力的无创检查技术,反映了病变的细胞结构和细胞膜的完整性,并能对体内各个器官系统的病变进行诊断以及鉴别诊断。b值(s/mm2)表示图像的扩散加权,称为扩散敏感因子。低b值图像对组织灌注更敏感,而高b值图像对受限的布朗运动更敏感[17]。近年来,DWI已被广泛应用于肝肿瘤的检测、诊断、分级和治疗反应评估[18]。DWI信号强度的保留或丢失的程度可通过“单指数模型”量化为表观扩散系数(apparent diffusion coefficient,ADC)[18]。通常情况下,肿瘤组织细胞丰富,细胞外空间较小,扩散常受到限制,通常在DWI图表现为高信号,ADC图呈低信号[19]。约25%~75%的ICC患者可在DWI上观察到“靶征”[20, 21],即边缘为高信号,代表了血供丰富、细胞密集的肿瘤成分,中心显示为低信号的纤维和坏死成分。研究者认为,这种在DWI上所呈现出的“靶征”征象,可以作为IMCC与肝脏其他肿瘤的重要鉴别点之一[20,22, 23]

       定量参数ADC值可以作为IMCC鉴别诊断与预后评估的指标之一。由于肿瘤组织细胞密集,水分子的扩散受限,ADC值降低,既往有文献报道,IMCC的ADC值越低,肿瘤的分化程度越低,患者预后较差[24]。Yamada等[25]测定26例IMCC患者的ADC值,选取中位数1.5×10-3 mm2/s作为分界值将患者分为两组,术前低ADC值组的患者三年生存率明显短于高ADC值组患者。但也有相反的观点[26]。如前所述,肿瘤内部纤维成分在促进ICC侵袭、转移以及治疗抵抗中起到一定的促进作用[27]。而与肿瘤组织相比,纤维组织内的水分子运动空间相对较大,扩散受限程度相对较小,因此ADC值偏高。Lee等[26]通过对91例ICC患者回顾性分析发现,肿瘤的ADC值越高,内部纤维成分越丰富,肿瘤的分期相对较晚,淋巴结转移几率增高,从而导致患者预后较差。Zhou等[28]认为,ADC值的升高除了与肿瘤内部纤维成分丰富有关外,肿瘤中心发生液化坏死也起到一定的作用。而肿瘤内部坏死成分被认为与较差的预后有关[29],原因可能为坏死细胞释放的细胞内容物,可作为促炎症和促肿瘤细胞因子发挥作用。同时,还有研究发现,较高的ADC值与肿瘤的微血管侵犯(microvascular invasion,MVI)呈正相关[28]。以上的研究表明,DWI的图像特征和ADC值的大小均可作为IMCC患者的潜在预后评估方法应用于临床,指导临床医师选择最佳的治疗方式。

       目前DWI在肝脏应用中仍然存在一些问题,如随b值的升高,图像质量下降明显,对解剖结构的观察造成一定的障碍[17]。腹部DWI容易受到患者呼吸伪影的影响,部分病灶边界模糊。对于ADC值的测量来说,感兴趣区的勾画方式、序列扫描时b值的选择在国内外的研究中均未形成标准的规范,均可影响ADC值大小。ADC值的大小还受到许多生理因素的影响,诸如血液流动,以及呼吸、心跳等。但随着MRI技术的不断进步和发展,DWI图像质量会得到进一步的提高,在今后的研究中,我们将探索更加精确的测量方法,以期将ADC值作为可靠的预测变量应用于临床工作中。

3 DCE-MRI

       肝脏增强MR扫描通常包括动脉期、门静脉期和延迟期,在注射对比剂后的20~25 s、70~90 s和180 s处获得[30]。目前临床常规应用的主要有钆喷替酸葡甲胺(Gd-DTPA)、钆特酸葡胺(Gd-DOTA)等含钆细胞外对比剂,通常为亲水性螯合物,经静脉给药后能快速分布到全身血管系统,以被动分布机制聚集在血管间隙和细胞外血管外间隙,最终几乎全部通过肾脏排泄[31]。IMCC多由边缘血供丰富的肿瘤细胞及中心低血供的纤维间质成分组成,其最常见的强化模式为动脉期边缘强化,门脉期及延迟期强化逐渐向中心填充[13]。这种典型的强化模式可较准确地与HCC或混合型肝癌进行鉴别[32, 33]。IMCC其他较少见的强化模式包括“稳定型强化”(动脉期及延迟期均呈高强化)、“快进快出型强化”(动脉期对比剂摄取明显,延迟期对比剂洗脱)和“弥漫低强化”(动脉期和延迟期均呈低信号)[14,34]

       在探索不同强化模式出现的原因过程中,Xu等[35]认为IMCC动脉期明显强化与存在慢性肝病及肝硬化背景有关。他们发现,在肝硬化或肝硬化前期的背景下,动脉的细小分支、胆道周围血管丛增加,这种血管结构的改变使得病变肝动脉供血增加,因此在增强扫描的动脉期,IMCC呈现出明显的强化模式。此外,还有学者研究认为[36, 37]肿瘤的大小也是影响强化方式出现差异的潜在因素。较小(<3 cm)的肿瘤,由于内部纤维化发育不良,主要成分以肿瘤细胞为主,因此以“稳定型强化”最常见[38, 39];而较大(≥3 cm)的肿瘤生长迅速,内部新生血管发育不良,导致肿瘤中心血供减少,低氧环境促进内部纤维间质成分的产生,这种改变使得“渐进性强化”模式最常见[9]。强化模式的不同可能影响患者预后。Min等[40]及Teraoku等[41]研究发现,与动脉期弥漫高强化相比,低强化及环形强化的患者预后更差。作者认为,相对于动脉期高强化的富血供病变,后两种强化模式的肿瘤内部纤维及坏死成分更多,肿瘤的分化程度更低,生存期缩短。然而目前的研究以单中心、回顾性研究为主,且大部分研究受到患者数量的限制缺乏外部验证组,因此需要更多的研究来验证不同强化方式对患者的预后影响,并进一步解释影像学特征与临床结果之间的关系。

       近几年,肝细胞特异性对比剂钆塞酸二钠(gadoxetic acid,Gd-EOB-DTPA)在临床诊断中的应用范围逐渐增加[42],这是一种新型T1顺磁性对比剂,通过将亲脂性乙氧基苄基与Gd-DTPA结合,50%的对比剂会通过有机阴离子转运体存在于肝血窦的肝脏细胞膜上,在注射对比剂1~2 min后开始被肝细胞吸收,之后再经过肝细胞膜上的多耐药相关蛋2排泄入胆道,这一时期被称为肝胆特异性期或肝胆期[43]。肝胆期图像通常在静脉注射对比剂后10~20 min时获得,肝脏纤维化或肝硬化的患者因肝细胞的摄取功能减弱应适当延长成像时间[44]。其余的50%对比剂仍通过肾脏排出[45],这种双重清除途径可以在肝肾功能受损时相互补偿,从而保证更高的安全性。在肝胆期,周围正常肝细胞摄取对比剂呈高信号,多数肿瘤组织由于正常肝细胞含量减少或缺乏呈相对低信号[46]。相对于细胞外对比剂来说,肝胆期更易发现位于肿瘤周围较小的卫星病灶或肝内隐匿的转移灶[13],有助于治疗策略的制订和预后预测。由于IMCC肿瘤内含丰富的纤维间质成分,细胞外间隙增大,对比剂潴留在纤维间质内引起排泄延迟,因此,约42%~56%的IMCC在肝胆期可见中心相对等或稍高信号[37,7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48],这种征象被称为肝胆期“靶征”。肝胆期“靶征”同样可作为IMCC与HCC的重要鉴别点之一[33,49, 50]。研究认为存在肝胆期“靶征”的IMCC患者预后较差,无复发生存期和总生存期均显著低于无此征象的患者,五年复发率分别为65%和24%,五年生存率为53%和87%[48]。Asayama等[51]在关于动态多期增强CT的研究中得出相似的结论,他们认为在延迟期强化范围大的患者(>2/3)预后要差于强化范围小的患者(≤2/3),一年、三年和五年生存率分别为66.1%、13.8%、0%及83.3%、57.6%和48.0%。然而也有研究得出与此相反的结果[37]。Kang等[37]对50例患者回顾性分析发现,肝胆期“靶征”意味着更好的肿瘤分化和更少的淋巴结转移。由此可见,影像与病理的精确对照将有助于解释IMCC肝胆期“靶征”的真正形成原因,这也将成为我们在今后研究中期待解决的问题。既往的研究显示,注射Gd-EOB-DTPA对比剂在动脉期扫描时易产生伪影[52],且由于扫描时间较长、价格较昂贵等原因,对于一些体弱、呼气控制较差的患者成像效果不佳,一定程度上限制了其在临床上的应用。

       通过DCE-MRI计算出的定量参数,可以反映肿瘤内部血管生成的情况以及肿瘤血流动力学和细胞代谢等特征,包括对比剂从血管到组织间的渗透率(Ktrans)、细胞外间隙容积(Ve)、血管内容积(VP)、细胞外间隙容积与血管内容积比(Kep)以及浓度曲线下面积AUC90、AUC180等[53],但在IMCC中的研究尚少见报道。Jarnagin等[54]发现,Kep和Ktrans在肝动脉灌注化疗前的基线值与化疗后差值(-DeltaKep和-DeltaKtrans)和患者的生存期呈负相关,差值越大,生存期越短。另有研究报道[54, 55],化疗前更高的基线AUC90和AUC180与较长的生存期相关。以上结果提示我们,DCE-MRI的定量参数在评估不可切除IMCC的化疗反应中存在潜在的应用价值,但在可切除IMCC的术前诊断、预后预测中还未见报道。此外,目前DCE-MRI定量分析技术没有统一的标准、扫描设备与扫描参数,药代动力学模型的选择也不尽相同,导致研究结果可能存在差异,这有待进一步探索和研究。

       以上关于IMCC诊断及预后的分析主要集中于DWI及DCE-MRI,其他多模态MRI序列如磁共振弹性成像、扩散峰度成像、扩散张量成像等在IMCC中的应用价值还未见探索。

       综上所述,多模态MRI由于可以提供肿瘤形态学特征、强化特征,以及一系列定量参数特征,可以为IMCC的诊疗提供重要的参考依据,同时评估患者预后。随着影像技术的不断发展、多中心合作的不断深入,在今后的工作中,探索更多新型功能影像技术,以及结合人工智能及影像组学技术,多模态MRI将会在IMCC的准确诊断、预后预测、疗效评估等方面发挥更重要的意义。

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