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综述
MRI评估结直肠癌肝转移瘤化疗疗效的研究进展
李彦瑶 贺业新

Cite this article as: LI Y Y, HE Y X. Progress of MRI in assessing the efficacy of chemotherapy for colorectal liver metastases[J]. Chin J Magn Reson Imaging, 2023, 14(11): 183-187.本文引用格式:李彦瑶, 贺业新. MRI评估结直肠癌肝转移瘤化疗疗效的研究进展[J]. 磁共振成像, 2023, 14(11): 183-187. DOI:10.12015/issn.1674-8034.2023.11.031.


[摘要] 结直肠癌(colorectal cancer, CRC)是世界上第三位最常见的恶性肿瘤,也是导致癌症相关死亡的主要原因。肝转移是CRC最常见的远处转移,与不良预后密切相关。早期精准预测疗效对患者的预后至关重要。近年来,出现了一些基于MRI评估疗效的方法,包括功能MRI(functional magnetic resonance imaging, fMRI)和基于MRI的影像组学等。本文就各种MRI技术在结直肠癌肝转移瘤(colorectal liver metastasis, CRLM)疗效评估中的优劣进行综述,同时叙述了生物标志物在评估CRLM患者预后方面的应用,为临床制订个体化治疗方案提供可靠依据,为科研工作提供新的思路。
[Abstract] Colorectal cancer (CRC) is the third most common malignancy in the world and the leading cause of cancer-related deaths. Liver metastasis is the most common distant metastasis of CRC, which is closely related to poor prognosis. Early and accurate prediction of curative effect is very important for the prognosis of patients. In recent years, there have been some MRI-based methods to evaluate the efficacy, including functional magnetic resonance imaging (fMRI), MRI-based imagomics and so on. This article reviews the advantages and disadvantages of the efficacy evaluation methods for colorectal liver metastasis (CRLM), and describes the application of biomarkers in evaluating the prognosis of CRLM patients, provides a reliable basis for clinical individualized treatment, and provides new ideas for scientific research.
[关键词] 结直肠癌肝转移瘤;生物标志物;化疗疗效;磁共振成像;功能磁共振成像;影像组学
[Keywords] colorectal liver metastasis;biomarkers;chemotherapeutic efficacy;magnetic resonance imaging;functional magnetic resonance imaging;radiomics

李彦瑶 1   贺业新 2*  

1 山西医科大学医学影像学院,太原 030001

2 山西医科大学第五临床学院/山西省人民医院磁共振室,太原 030012

通信作者:贺业新,E-mail:heyexinty2000@sina.com

作者贡献声明:贺业新、李彦瑶均参与文章的构思和设计,起草论文或参与论文重要内容的修改;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。


收稿日期:2023-06-24
接受日期:2023-10-27
中图分类号:R445.2  R735.37 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.11.031
本文引用格式:李彦瑶, 贺业新. MRI评估结直肠癌肝转移瘤化疗疗效的研究进展[J]. 磁共振成像, 2023, 14(11): 183-187. DOI:10.12015/issn.1674-8034.2023.11.031.

0 前言

       结直肠癌(colorectal cancer, CRC)是世界上第三位最常见的恶性肿瘤,也是导致癌症相关死亡的主要原因[1]。肝转移是CRC最常见的远处转移,与不良预后密切相关。结直肠癌肝转移瘤(colorectal liver metastasis, CRLM)根治性切除是改善患者预后的首选治疗方法。然而,只有不足20%的患者适合进行直接手术切除;对于其他患者,全身化疗是首选的治疗方法[2, 3, 4, 5]。全身化疗有助于最初不可切除病灶的切除,有助于降低肝脏转移瘤切除后复发的风险,并提高不可切除肝转移瘤患者的生存率[6, 7, 8]。但是,化疗会对肝脏产生多种副作用,这些副作用与复发率和死亡率相关[9, 10, 11]。因此,考虑到化疗的肝毒性,早期评估化疗反应对制订个体化治疗方案及减少肝损伤具有重要意义。

       传统上,使用实体瘤临床疗效评价标准(Response Evaluation Criteria in Solid Tumor, RECIST)来评估肿瘤对化疗的反应[7, 12],它是通过在影像图像上观察并测量肿瘤的数量和大小变化,结合临床肿瘤标志物水平来评估化疗反应,然而,仅仅依靠肿瘤数量和大小的变化来确定化疗反应可能不够准确,因为微环境中的功能变化发生在肿瘤体积变化之前[13, 14, 15]。后来,RUBBIA-BRANDT等[16]首次引入了关于CRLM的肿瘤退缩分级(tumor regression grade, TRG)系统,在组织学的基础上,主要依据镜下残余肿瘤细胞和纤维化的比例进行分级,以评估CRLM患者对不同类型新辅助化疗方案的组织学反应程度。TRG基于组织学基础比RECIST能更准确地反映化疗效果,然而TRG是一种侵入性的评估方法,会对患者产生创伤。近年来,出现了一些基于MRI的非侵入性半定量及定量评估化疗反应方法,包括常规MRI、功能MRI(functional magnetic resonance imaging, fMRI)、影像组学及生物标志物等,它们解决了上面两种方法的不足,可以为临床医生提供更早期的预测信息及更简便的预测方法,也避免了对患者的损伤,但是这些方法获得影像图像后还需要通过后处理才能得到结果,且研究还不太成熟,所以目前还未广泛应用于临床。本文就不同MRI技术预测CRLM化疗反应方法的研究现状进行综述,对已有方法的优劣进行整合并提出自己的观点,希望通过本综述给临床医生制订个体化治疗方案提供可靠依据,给研究者们提供新的研究思路。

1 常规MRI

       常规MRI中常用的评估CRLM化疗疗效的方法有RECIST和钆塞酸二钠(gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid, Gd-EOB-DTPA)增强MRI。RECIST是基于肿瘤数量和大小的变化,从放射学角度评估肿瘤的化疗反应。然而,肿瘤数量和大小的变化受化疗方案等多种因素的影响,因此可以通过测量Gd-EOB-DTPA增强前后肿瘤的信号强度变化来评估化疗反应。

       Gd-EOB-DTPA是一种肝细胞特异性对比剂,在人体内约50%被肝细胞摄取并通过胆道系统排泄[12, 17, 18]。在注射对比剂后约15-20 min,胆道显影进入肝胆特异期(hepatobiliary phase, HBP),此期提供了极好的肝脏对比度,提高了病灶的检出率[19, 20, 21]。Gd-EOB-DTPA增强MRI正越来越多地被用于CRLM的诊断、手术计划制订和化疗后评估[22]。CRLM对化疗的病理反应主要表现为过度纤维化,纤维化区域或坏死区域在增强MRI中可能表现为延迟增强或缓慢消退[8]。通过测量延迟成像的肿瘤信号强度来反映化疗后的肿瘤纤维化或坏死,以评估化疗反应。MUADDI等[23]研究认为使用Gd-EOB-DTPA增强MRI是评估化疗后CRLM的首选成像方式。HOSSEINI-NIK等[8]基于Gd-EOB-DTPA增强MRI测量了肿瘤的标准化相对增强和相对信号强度差,结果表明病理完全缓解组的相对信号强度差显著低于非完全缓解组,敏感度为70%,特异度为83%。WANG等[21]研究表明,Gd-EOB-DTPA增强MRI中肝胆期边缘增强和目标病灶中心部分与目标病变周围正常肝实质的平均信号强度值的比值较低时,组合模型受试者工作特征曲线下面积(area under the curve, AUC)为0.712,转移病灶显示出对化疗的良好反应,是早期评估CRLM患者化疗反应的有用指标。综上所述,Gd-EOB-DTPA作为一种具有细胞外和肝细胞特异性的对比剂,对小病灶的检出率高,通过对肝胆特异期病灶信号强度的测量,在CRLM的诊断及评估术前化疗反应方面具有良好的应用前景。另外,有研究表明[24],化疗会导致肝脏脂肪变性增加,是否可以通过在同反相位上测量化疗前后病灶的脂肪分数变化来评估化疗反应,可能作为今后的一个研究方向。

2 fMRI

2.1 扩散加权成像

       扩散加权成像diffusion weighted imaging, DWI是通过检测活体组织中水分子的扩散运动来反映组织微观结构的变化。通过DWI获得的表观扩散系数(apparent diffusion coefficient, ADC)用于描述水分子的扩散运动速度,它与分子黏度、主动转运机制、微血管循环、膜通透性以及细胞结构密切相关[5, 24]。研究表明,ADC值在多种恶性肿瘤中都可以作为预测化疗反应的良好指标[7, 25, 26, 27]。有效化疗后,早期就能发现病变的ADC值增高[25]。BORASCHI等[6]将CRLM新辅助化疗前和后的ADC值(preADC和postADC)及其差值(ΔADC)与组织学TRG相关联,表明postADC、ΔADC和TRG分级具有一致性,可作为评估CRLM患者术前化疗后肿瘤治疗反应的可靠指标。ZHU等[4]将RECIST标准与平均ADC值在预测接受贝伐单抗治疗的CRLM患者的预后价值方面进行比较,发现治疗后平均ADC值能准确反映治疗效果和预测生存期(AUC为0.793),优于RECIST标准。另有研究表明,治疗前ADC直方图分析也可以作为恶性肿瘤患者放化疗反应的有用预测指标[28, 29]。LIANG等[30]研究表明,ADC直方图参数的平均值和百分位数在反应组中显著降低,可以用于识别对化疗反应良好的患者,其中第99百分位数在预测化疗反应方面具有最高的诊断性能,AUC为0.82,敏感度为93.3%。综上,ADC值作为一种无创性的指标,可以反映肿瘤接受化疗后早期的结构及功能变化信息,早于肿瘤大小的变化,而早期预测治疗反应有助于优化治疗方案以保证患者最好的疗效,因此它与组织学TRG分级和仅基于大小变化的RECIST标准相比,在评估化疗反应和准确预测生存方面显示出巨大的潜力。但由于ADC值仅反映水分子的自由扩散程度,而组织的微循环灌注会影响信号强度的变化,使测得的ADC值不够准确,因此,学者们提出了基于双指数模型的DWI,用来弥补这一不足。

2.2 体素内不相干运动成像和扩散峰度成像

       体素内不相干运动(intravoxel incoherent motion, IVIM)成像使用双指数模型区分水分子的扩散和组织的微循环灌注并获得参数,包括扩散参数(真扩散系数D)和灌注参数(假扩散系数D*、灌注分数f)[31]。D值反映了水分子的纯扩散运动,D*值反映了毛细血管网中微循环灌注的相关扩散运动,f值反映了微循环灌注相关扩散占总扩散的比例。一些研究[32, 33]表明,IVIM成像的功能参数在反映CRLM的病理特征及其化疗反应方面具有重要意义。WU等[15]研究表明,f值和D值可以有效评估CRLM患者的治疗效果,有效治疗后,f值显著降低,D值显著升高,AUC分别为0.797、0.722;治疗前f值有助于预测患者的治疗反应。CHIARADIA等[32]认为D值和ADC值与化疗后肿瘤坏死程度相关。ZHANG等[5]研究表明有效治疗后D值增加(AUC为0.832),可作为反映CRLM有效治疗的指标。扩散峰度成像(diffffusion kurtosis imaging, DKI)可以反映生物组织中水分子的非高斯扩散特性,可以提供具有高b值的组织异质性和其他微观结构信息[34]。DKI的参数较多,腹部研究常用的参数是平均扩散峰度(mean kurtosis, MK)和平均扩散率(mean diffusion, MD),MK是组织沿空间各方向扩散峰度的平均值,MD是经过非高斯水扩散校正过的ADC值[35]。DKI在描述组织微观结构方面优于DWI,逐渐用于腹部疾病的研究[36, 37]。ZHANG等[5]研究发现治疗前高MK值(AUC为0.787)和低MD(AUC为0.819)值与CRLM的良好治疗反应相关,这表明DKI参数在预测CRLM的化疗反应方面可能具有重要价值。IVIM和DKI都是以水分子运动非高斯分布为理论基础,在显示组织微循环灌注方面优于传统的DWI,DKI可以量化水分子偏离高斯分布的程度,它们能更准确和真实地反映肿瘤内部的病理生理变化。越来越多的研究将IVIM应用于肝脏肿瘤的研究,但在预测化疗疗效方面的研究较少,关于DKI的研究目前主要还是应用于神经系统,因此,IVIM和DKI在预测肝脏转移瘤化疗疗效方面的价值有待进一步挖掘。

3 影像组学与生物标志物

       影像组学是从医学影像图像中高通量获取定量图像特征并将其转换为可挖掘数据以进行分析的一种非侵入性影像学分析工具,用于包括CRLM在内的各种肿瘤的疾病分期、组织学分级、治疗反应和生存预测[38, 39, 40, 41]。MA等[42]构建了基于MRI影像组学和临床参数的预测模型评估CRLM患者的化疗反应,结果表明包含影像组学评分、糖类抗原199和临床分期的影像组学临床诺模图(AUC为0.809)比基于MRI的影像组学模型在预测CRLM患者的化疗反应方面更有效,该影像组学临床诺模图可以有效区分治疗有反应组患者和无反应组患者。申洋等[43]通过分析同时性CRLM患者的T2WI、DWI及增强门脉期图像,提取影像组学特征来预测化疗疗效,结果表明单独MRI序列中DWI预测效能好(AUC为0.649),而结合三个序列的影像组学预测效能更好(AUC为0.739)。影像组学虽然更能反映放射影像中病灶的细微结构变化,但由于绘制感兴趣区和图像分割的方法以及数据集大小的变化等影响,其也存在不稳定性。随着深度学习的应用,它在识别和分割小病灶方面优于影像组学,因此,可以将影像组学与深度学习相结合,来提高预测准确性。目前报道的影像组学研究大多基于CT图像,基于MRI图像的影像组学还需要今后进一步研究。

       随着对CRLM研究的深入,越来越多的相关生物标志物被揭示,包括肿瘤标志物和基因标志物[44, 45]。ALI GÜLTEKIN等[46]首次研究了用ADC值确定CRLM患者的KRAS基因突变状态,发现与野生型相比KRAS基因突变型的CRLM患者ADC值显著降低。GRANATA等[47]认为DKI参数MK和MD可以用来检测CRLM患者的KRAS基因突变,MK的敏感度为72%,特异度为85%,MD的敏感度为84%,特异度为73%。也有研究[48]认为可以用影像组学来预测基因突变,但大多都基于CT影像特征,基于MRI影像特征的研究较少。KRAS和BRAF等基因突变与CRLM患者的临床预后不良相关[49, 50, 51, 52]。TOSI等[49]研究发现,KRAS基因突变与CRLM全肝切除术患者的总生存期和无复发生存期呈负相关,BRAF基因突变与总生存期呈负相关。综上所述,MRI参数及影像组学可以预测CRLM患者的基因突变类型,而基因突变类型又与预后紧密相关。我们猜测基因突变类型可能与化疗反应也存在一定的相关性。因此,未来可以用基于MRI的影像组学或MRI与基因标志物结合来预测CRLM患者的化疗疗效。另有研究[53, 54, 55, 56]表明,肿瘤标志物如循环肿瘤DNA可以预测CRLM患者的化疗疗效,目前还没有把肿瘤标志物与MRI结合来预测疗效的相关研究,可以作为今后的一个研究方向。

4 小结与展望

       与RECIST相比,Gd-EOB-DTPA增强MRI可以反映肿瘤内部的纤维化及坏死程度,与TRG分级相比,fMRI和基于MRI的影像组学可以无创性地评估化疗疗效,避免了患者的损伤。DWI基于高斯分布反映水分子的自由扩散程度,获得的ADC值可以反映组织的微观结构,但由于受化疗药物种类等多种因素的影响并不准确。因此出现了基于非高斯分布的IVIM和DKI,它们在DWI的基础上考虑了组织微循环灌注的影响,能够更准确地反映组织的细微结构变化,在预测CRLM患者化疗疗效方面更准确,但它们获得影像图像后还需要通过后处理才能得到数据,所以还没有广泛应用于临床。影像组学作为一种非侵入性的方法,在评估疗效方面有重要的应用价值,但目前的研究都是单中心的回顾性研究,样本量较少,且基于MRI的影像组学研究较少。生物标志物作为近年来的研究热点,大多用来预测CRLM患者的生存期,还没有将它与MRI联合预测疗效的相关研究。在大数据时代背景下,随着各种技术的发展,期望研究者们可以开发出一体化全自动的图像处理分析软件增加研究的可重复性,并将影像组学、生物标志物和MRI相结合,进一步探索更精确的适合广泛应用于临床的预测疗效的方法,为临床的诊疗工作提供更早期、更可靠的理论依据。

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