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综述
磁共振影像生物标志物预测肝细胞癌术后复发风险的研究进展
于长江 朱绍成

Cite this article as: Yu CJ, Zhu SC. Research progress on magnetic resonance imaging biomarkers in predicting the risk of postoperative recurrence with hepatocellular carcinoma[J]. Chin J Magn Reson Imaging, 2022, 13(5): 154-157.本文引用格式:于长江, 朱绍成. 磁共振影像生物标志物预测肝细胞癌术后复发风险的研究进展[J]. 磁共振成像, 2022, 13(5): 154-157. DOI:10.12015/issn.1674-8034.2022.05.033.


[摘要] MRI可以预测肝细胞癌的预后,近年来功能MRI和肝胆特异性对比剂的应用推广以及影像组学的发展,使得MRI预测肝细胞癌预后及复发风险评估这一研究领域进一步深化,并探索出部分影像生物标志物。本文对此类磁共振影像生物标志物的定义、特征、潜在发生机制及临床关联进行综述,旨在提高对MRI评估肝细胞癌术后复发价值的认识,更好地辅助科研和指导临床实践。
[Abstract] Magnetic resonance imaging can predict prognosis of hepatocellular carcinoma. In recent years, the application and promotion of functional magnetic resonance imaging and hepatobiliary specific contrast agents as well as the development of imaging omics have further deepened the research field of prediction of prognosis and recurrence risk assessment of hepatocellular carcinoma by magnetic resonance imaging. Besides, some imaging biomarkers have been explored. In this paper, the definition, characteristics, potential mechanisms and clinical relevance of magnetic resonance imaging biomarkers were reviewed. It aims to improve the understanding of the evaluation value of postoperative recurrence of hepatocellular carcinoma by magnetic resonance imaging, and to better assist scientific research and guide clinical practice.
[关键词] 肝细胞癌;磁共振成像;影像生物标志物;术后复发;预后;风险预测
[Keywords] hepatocellular carcinoma;magnetic resonance imaging;imaging biomarker;postoperative recurrence;prognosis;risk prediction

于长江 1, 2   朱绍成 1, 2*  

1 郑州大学人民医院医学影像科,郑州 450003

2 河南省人民医院医学影像科,郑州 450003

朱绍成,E-mail:zsc2686@163.com

作者利益冲突声明:全体作者均声明无利益冲突。


基金项目: 河南省重点研发与推广专项(科技攻关) 212102310729
收稿日期:2021-12-30
接受日期:2022-04-11
中图分类号:R445.2  R735.7 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.05.033
本文引用格式:于长江, 朱绍成. 磁共振影像生物标志物预测肝细胞癌术后复发风险的研究进展[J]. 磁共振成像, 2022, 13(5): 154-157. DOI:10.12015/issn.1674-8034.2022.05.033.

       肝细胞癌(hepatocellular carcinoma,HCC)是全球第六大最常见的癌症[1],是全世界癌症死亡的第三大原因,也是肝脏原发性恶性肿瘤发病率之首[2]。HCC起病隐匿,病情进展迅速,且治疗后复发率高。其诊断主要基于临床表现、影像学特征、实验室肿瘤生化指标及病理,因其特定的高危人群和典型的影像学征象,是少数仅通过医学影像诊断即可定性的恶性肿瘤[3]。医学影像作为非侵入性成像技术,不仅可用于HCC的诊断,亦可通过评估肿瘤特征即影像生物标志物预测HCC预后及潜在复发风险,对临床治疗中的疾病监测提供信息支持。MRI以其多参数、多序列、多方位的特点和软组织分辨率高的优势,在肝脏病变的评估中起到不可替代的作用[4],近年来随着功能MRI技术和肝胆特异性对比剂的应用,为HCC的诊断及预后复发风险评估提供了更多方法和可能[5]

       广义上,HCC的复发风险评估涉及多个复杂的系统和学科[6],仅医学影像就包括不同的成像技术、扫描部位及相应征象,本文仅对磁共振影像生物标志物预测HCC术后复发风险的研究进展进行综述。

1 肿瘤大小及数量

       因MRI断层扫描的特性及图像良好的软组织对比度,肿瘤的大小和病灶数量是最易获取的影像参数,是评估HCC术后预后及早期复发风险的影像生物标志物。肿瘤大小和数量与肿瘤负荷、微血管浸润(microvascular invasion,MVI)及肿瘤分期、分级直接相关[7, 8, 9, 10],较大的瘤体及多灶性肿瘤预示较高的早期复发风险和不良预后可能。HCC为实体肿瘤,多呈膨胀性块状生长,对其大小的描述,临床中多采用轴位图像瘤体最大直径表示。亦可通过后处理及图像分割软件,手动或程序自动勾画感兴趣区域(region of interest,ROI),对肿瘤大小进行二维或三维分析,计算得出瘤体最大截面积、体积及体表面积等参数。相对于轴位图像瘤体最大直径的一维评估,三维评估被证明能更准确地评估肿瘤负荷[11]。对于同一肿瘤的大小描述,因扫描序列及期相的差异、肿瘤边界情况的异质性及人工测量的随机误差可得出不同的结果。美国放射学院发布的2018版肝脏影像报告和数据系统(Liver Imaging Reporting and Data System,LI-RADS)推荐使用除增强扫描动脉期及DWI序列之外的肿瘤边界显示清楚的期相和序列测量,并且测量范围应包含肿瘤的包膜。对此解释为动脉期及DWI序列上测量结果可存在较大误差,例如动脉晚期HCC强化的程度常高于动脉早期,部分HCC可表现为仅在动脉晚期高强化,以上强化特点对肿瘤边界判定的影响可能造成动脉期内部的测量差异;动脉期测量的结果可能包含观察目标瘤体及周围同期强化的组织而被高估;DWI序列图像的形变及磁化率伪影等。Jeon等[8]因肝胆特异性对比剂钆塞酸二钠增强中肝胆期图像(hepatobiliary phase,HBP)可提供HCC瘤体与周围正常肝功能组织鲜明的信号对比,认为HBP图像可能是获得肝脏肿瘤体积等参数的最合适阶段,进而描述肿瘤的大小。并指出HCC为单个瘤体时,HBP图像评估提示肿瘤体积是HCC术后复发和总生存期(overall survival,OS)的显著预测因素。肿瘤体积预测无复发生存期(recurrence-free survival,RFS)的最佳截断点为4.0 mL, 瘤体体积大于4.0 mL时OS和RFS显著下降,提示HCC术后复发高风险。

       HCC在MRI影像上多表现为肝内单个孤立瘤体或2~3个大小不等的孤立瘤体,部分空间位置邻近的瘤体可随着肿瘤不间断的恶性生长发生融合,从而分界不清,瘤体周围可伴有卫星结节及异常信号影。少数表现为弥漫性的小肿瘤结节灶散在分布于肝内,即HCC Eggel's大体形态学分类中的弥漫型。文献中HCC肿瘤数量的分类方法众多,为了便于影像诊断的描述和临床实践中的应用,通常将其简化,分类为单发肿瘤或多发肿瘤。病理学上,HCC的多灶性及主瘤体周围卫星结节的存在提示肿瘤较高的侵袭性和浸润播散可能[7,9, 10,12, 13, 14],多为肝内转移的结果。研究表明相较于单发肿瘤,多灶性肿瘤或主要瘤体伴周围卫星结节的HCC患者治疗后复发风险更高[12],归因于更具侵袭性的肿瘤生物学行为及相应更高难度的治疗措施。

2 肿瘤边缘及包膜情况

       作为正常肝实质与HCC的交界处,瘤体的边缘情况常用来评判肿瘤的恶性程度和预测肿瘤的生物学行为,进而影响临床治疗术式的制订与术区范围规划[15],是MRI评估HCC术后早期复发和预后[10,16]的重要一环。MRI对肿瘤边缘不光滑定义为各序列和期相中肿瘤边界不整或与周围组织分界欠清,瘤体呈分叶状,局部见凸起或出芽,常预示瘤周组织受侵或发生MVI[7,17],进而提示潜在的早期复发风险及预后不良[18]。Lee等[19]研究表明非光滑肿瘤边缘在预测MVI方面的准确率为69% (136/197)。在钆塞酸二钠增强肝胆特异期,因HCC瘤体与周围正常肝组织有较高的信号对比度,可以更清晰地显示肿瘤的边界情况。

       组织学上,HCC假包膜是瘤体在膨胀性生长的过程中对周边解剖结构的压迫和刺激而反应性生成的膜状结缔组织,由周围肝组织增生的胶原纤维外层和内层新生的薄壁小血管、门静脉分支血管构成。相较于肝硬化再生结节的包膜结构,HCC假包膜更厚,在MRI上显示更清晰,犹如一道隔离墙阻止了HCC向四周的浸润生长。MRI影像中,HCC假包膜在T1加权图像呈线样低信号,完整或部分包绕瘤体,增强扫描主要在门脉期和延迟期强化,呈高信号环形结构。若假包膜在动脉期显著强化,常提示新生微血管明显且血管管壁薄弱,结构欠完整,肿瘤易突破血管进入血液循环,造成周围肝组织的局部浸润和远处转移,MVI危险度提高,早期复发风险增大。多数学者认为HCC完整的假包膜是良好预后的保护性因素,不完整假包膜及无假包膜的HCC早期复发风险显著增高[9, 10,17,20, 21],造成不良预后;并指出包膜的完整程度与早期复发风险呈负相关,这被解释为假包膜的天然屏障作用利于各治疗术式的开展,以期达成预计治疗效果。例如肝动脉化疗栓塞术(transcatheter arterial chemoembolization,TACE)中,HCC假包膜可阻止化疗药物和碘油从肿瘤组织中流出,利于化疗药物和碘油的瘤内沉积,预示更好的疗效及预后。

3 肿瘤位置及大血管浸润

       相较于MRI中HCC的形态学影像生物标志物,HCC在肝内发生发展的空间位置及周边脉管结构关系也对HCC的早期复发起到警示作用。当HCC位于肝脏浅表部位或肝包膜下时,因HCC的直接侵袭行为导致腹腔及邻近组织器官转移风险增大。鉴于HCC多存在于肝炎、肝硬化背景下,肝组织硬度及脆性增加,肝脏浅表部位或肝包膜下的HCC发生自发性破裂出血的可能性增加,亦使得癌细胞肝外扩散转移概率上升,对预后造成不利影响。在MRI临床实践中应充分评估HCC边界与肝缘的距离及肝内位置情况。Kang等[22]研究显示门静脉周围HCC的不良预后及早期复发风险较高,对此可解释为HCC大血管浸润较易侵犯门静脉系统而非肝静脉和肝固有动脉这一独特肿瘤生物学行为。另因门静脉主干及分支位于第一肝门区,其周围解剖结构复杂,脉管系统发达,在此位置生长的HCC治疗措施和方法更加局限,手术难度大,术中操作易造成肿瘤细胞的周围转移及血行播散,导致潜在的HCC异位复发风险。

       HCC的血管侵犯及MVI反映出肿瘤的高度侵袭性,是术后复发及不良预后的独立预测因子,此观点已取得业界的普遍认可并有大量文献资料的支持。MVI指在显微镜下由内皮细胞衬覆的微小血管腔内发现肿瘤细胞的巢团,作为一病理学的微观概念,当前的影像技术手段无法将其在MRI上直接显示,继而无法通过图像直观评估。但MRI可清晰显示肉眼可见的血管浸润癌栓,以门静脉瘤栓(portal vein tumor thrombus,PVTT)最常见,表现为门静脉内团片状软组织信号影,增强扫描可见强化,有时可见癌栓内的滋养动脉显影,门静脉期呈充盈缺损改变。大血管癌栓是HCC肝内转移的常见形式,作为前哨可进一步引起肝内乃至肝外的广泛癌细胞转移。大血管浸润及癌栓的存在常提示肿瘤进展和较差的分期,是影响预后的关键因素[9, 10,22],是评估HCC早期复发风险的重要影像生物标志物。

4 动脉期瘤周强化

       动脉期瘤周强化指HCC瘤体之外,在瘤体周围MRI增强扫描动脉期呈斑片状或絮状强化,在LI-RADS中被称为晕样强化(corona enhancement),并将期相限定和补充为动脉晚期和门静脉早期,是支持恶性肿瘤诊断的次要征象之一。目前发生机制尚未完全明确,部分学者解释为HCC瘤体周围肝组织门静脉的微小分支发生MVI[7,9, 10,12,17,20],侵袭的微瘤栓阻塞血管,造成瘤周门静脉血流量减低,促使瘤周小动脉代偿性增生。动脉期瘤周强化反映出瘤体周围血流动力学的改变即瘤周血流高灌注状态,常提示HCC不良进展和高侵袭性。通常会进一步导致肝内转移,表现为瘤周门静脉引流区内卫星结节的生长。Wei等[14]研究表明,动脉期瘤周强化阳性的HCC较阴性肿瘤分化更差,并得到了相关研究的支持[23]。Wang等[21]为了排除肝纤维化或肝硬化对肿瘤周围组织强化程度的影响,采用动脉期瘤周强化与周围正常肝组织信号的比值,通过量化信号强度的方式,论证了动脉期瘤周强化是预测HCC术后早期复发的影像生物标志物并进一步细化了风险分层。

5 肝胆特异期瘤周低信号

       肝胆特异期是使用肝胆特异性MRI对比剂钆塞酸二钠增强扫描所取得的独特期相,因其肝胆特异性,能够清晰区别正常肝组织与异常病灶,显著提高肝脏小病灶的检出率,为病灶的鉴别诊断及周边肝组织状态评价提供必要的功能学信息[24]。对于HCC,尤其是早期HCC的影像学诊断、定性及分型,肝胆特异期起到重要的循证医学支撑[25],并在HCC治疗全程中的病情监测、疗效评估及复发风险预测等方向展现出巨大的潜力。

       MRI肝胆特异期中,因正常肝细胞对钆塞酸二钠高达50%的摄取率而呈现强化,显示为均质的高信号。当HCC瘤体周围出现片状、晕状或不规则状的低信号影,通常意味着瘤体周围肝细胞的功能改变。有学者解释其机制可能为HCC局部浸润瘤周肝组织及微小血管引起血流动力学的变化,导致肝细胞缺氧受损和代谢异常,进而影响有机阴离子转运多肽8在肝细胞表面的正常表达,使得瘤周肝细胞对钆塞酸二钠的摄取降低[17],显示为肝胆特异期瘤周低信号。这一影像生物标志物在多数研究中已被证明可以预测HCC的MVI存在[10,12,14,16,26, 27],是HCC早期复发的危险因素。

6 磁共振扩散加权成像显著高信号及衍生

       磁共振扩散加权成像(diffusion weighted imaging,DWI)是一种描述体内组织水分子扩散运动的功能MRI技术。大多数HCC在高b值DWI上表现为高信号,提示水分子扩散受限,反映出HCC瘤内细胞密度增高的特征。基于DWI技术,利用单指数模型计算出表观扩散系数(apparent diffusion coefficient,ADC)及多b值双指数模型体素内不相干运动扩散加权成像(intravoxel incoherent motion diffusion weighted imaging,IVIM-DWI),可以减少或消除例如T2穿透效应等干扰因素并定量描述水分子扩散受限的程度。有研究表明ADC值是术前预测HCC发生MVI的重要风险因子[9,17,28, 29],ADC值和IVIM-DWI参数均与HCC组织学分级显著相关[30]。这被解释为相较于未发生MVI且恶性程度较低的高分化HCC,发生MVI的HCC具有更强的侵袭性,组织学上分化程度较低,多具有更高的细胞密度和更显著的细胞异型性使得瘤内水分子的扩散更加受限,DWI显示为更高的信号及更低的ADC值,预示着更高复发风险[31]

7 其他可能的影像生物标志物

       除上述被众多学者广泛描述的可评估HCC复发风险的MRI生物标志物外,尚有部分发现可能对其有帮助,但因较少的报道量及较低的重复试验阳性率,临床价值尚不确定,仍需进一步的探索。有研究[32, 33]显示,LI-RADS分类(LR-4/5 vs. LR-M)是评估HCC术后预后的独立因素,并称LR-M型HCC的预后可能比LR-5/4型差。预示着病理组织学分级及临床肿瘤分级之外,基于影像学的分级也可对HCC的治疗及预后风险分层起到指导作用[34]。部分影像学特征被认为与HCC患者更好的预后及较低的复发风险相关,如瘤内脂肪成分存在和肝胆特异期瘤体呈等、高信号[10],并归因于此类表现多见于分化良好的HCC,恶性程度低,治疗效果好。

8 影像组学

       影像组学作为一种新兴的跨学科影像分析方法,通过多种数据挖掘算法,高吞吐量地从医学影像中提取高维定量图像特征,发掘隐藏在视觉灰度图像中的数字信息进行分析处理,结合人工智能及机器学习手段对疾病的诊疗提供数据支持,具有稳定性高、重复性好、快速高效且不受个人意志主观干扰的特点,近年来在HCC的复发风险评估研究中广泛应用[35]。Wei等[36]通过影像组学深度学习的方法,提出相较于CT,MRI组学对HCC的MVI及复发风险评估表现更加优异,并因MRI肝胆特异性对比剂在HCC诊疗中的广泛应用,可提供更多的细节参数、更准确的预测效果。部分学者[29,37, 38]基于MRI组学特征结合实验室指标及临床参数,经统计整理后构建联合评估模型对HCC术后患者的预后及早期复发风险进行预测并取得可喜的结果。Zhao等[39]学者在此基础上进一步深化研究,对HCC进行了术前复发风险分层。

       众多优势使得影像组学成为预测HCC患者预后及早期复发风险的可靠影像生物标志物[5,16,20,40],近些年来也一直是业内研究的热点领域,但现有条件下,其临床应用还存在一定的挑战和局限性。目前学术界尚无有关影像组学信息特征提取、图像分割和采集、人工智能分析、统计策略及建模的统一方法与标准,再因不同影像设备机械参数的差异及调教设置不同,所获图像质量参差不齐,造成影像组学的研究成果在临床中应用与推广困难,是未来亟待解决的问题,亦是未来研究的方向。

9 总结与展望

       近年来,随着医学影像学的发展与深入研究,MRI不仅活跃在HCC的诊断与鉴别诊断舞台上,在HCC的预后评估及复发风险分层方面也颇有建树。特别是功能MRI的推广与肝胆特异性对比剂的应用[41],外加组学及人工智能的加持,取得了大量影像学参数并探索出有关HCC预后及复发风险的影像生物标志物。通过无创性的评估,缓解了病理诊断侵入性操作的风险及患者心理负担。这些标志物可术前评估HCC患者预后及复发可能性,结合其他专业指征从而指导临床合理制订治疗方案及后期随访计划[42]。通过评估,这些患者可能被考虑进行更高疗效的手术,如扩大射频消融范围,或将非解剖性肝切除术升格为解剖性肝切除术等方式来减少不良预后的发生[26, 27],或在不影响预后的情况下缩小手术范围及创面,更好地保全器官结构及功能。值得一提的是,这些影像生物标志物虽有易于观察、操作简单、识别方便的优势,但单独使用的诊断效能较差。在实践应用过程中,应将诸影像生物标志物整体评估,联合诊断,综合考虑,结合患者实际情况进行个体化诊疗[43]。相信未来随着技术的进步与研究的深入,会提出更明细的量化标准及规范指南。

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