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临床研究
钆塞酸二钠增强MRI的影像特征和肝胆期直方图参数对肝细胞癌经动脉化疗栓塞术应答反应的预测价值
滕飞 任继鹏 闫瑞芳 蔡明溪 韩东明

Cite this article as: Teng F, Ren JP, Yan RF, et al. Predictive value of Gd-EOB-DTPA enhanced MRI features and hepatobiliary phase histogram parameters in response to transarterial chemoembolization for hepatocellular carcinoma[J]. Chin J Magn Reson Imaging, 2022, 13(11): 71-75.本文引用格式:滕飞, 任继鹏, 闫瑞芳, 等. 钆塞酸二钠增强MRI的影像特征和肝胆期直方图参数对肝细胞癌经动脉化疗栓塞术应答反应的预测价值[J]. 磁共振成像, 2022, 13(11): 71-75. DOI:10.12015/issn.1674-8034.2022.11.013.


[摘要] 目的 探讨钆塞酸二钠(gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid, Gd-EOB-DTPA)增强MRI的影像特征和肝胆期直方图参数对肝细胞癌(hepatocellular carcinoma, HCC)患者经动脉化疗栓塞术(transarterial chemonembolization, TACE)治疗应答反应的预测价值。材料与方法 前瞻性招募2020年6月至2021年6月在新乡医学院第一附属医院初诊的54例HCC患者,评估病灶的影像学特征,并提取肝胆期病灶的直方图均值、变异度、峰度、偏度、第10百分位、第90百分位、熵、最大值、最小值及中值等参数。根据改良实体瘤疗效评价标准(modified Response Evaluation Criteria in Solid Tumors, mRECIST),分析影像学特征和肝胆期直方图参数在TACE术后不同应答组中的差异,应用logistic回归分析和受试者工作特征(receive operating characteristic, ROC)曲线分析有统计学意义的参数对应答反应的预测价值。结果 应答组28例,非应答组26例。不完整的包膜、动脉期瘤周强化、肝胆期瘤周低信号的发生率在非应答组明显高于应答组(P均<0.05)。均值、变异度、第10百分位、中值非应答组明显高于应答组(P<0.05)。Logistic回归分析显示,动脉期瘤周强化、肝胆期瘤周低信号和变异度是应答反应独立影响因素(P均<0.05)。ROC曲线分析显示,综合参数预测应答反应的曲线下面积、敏感度、特异度分别为0.904(95% CI:0.816~0.992)、80.8%、96.4%。结论 动脉期瘤周强化、肝胆期瘤周低信号和变异度是TACE术后应答反应的独立预测因素,且定性指标与定量参数综合的预测模型有好的预测效能,为HCC患者的精准治疗提供帮助。
[Abstract] Objective To evaluate the value of Gd-EOB-DTPA enhanced MRI and hepatobiliary tumor histogram parameters in predicting the response to transarterial chemoembolization (TACE) in patients with hepatocellular carcinoma.Materials and Methods Fifty-four patients with newly diagnosed HCC treated in the First Affiliated Hospital of Xinxiang Medical College from June 2020 to June 2021 were collected. The imaging features of the lesions were evaluated, and the histogram mean, variation, kurtosis, skewness, 10th percentile (Perc10%), 90th percentile (Perc90%), entropy, maximum, minimum and median values of hepatobiliary lesions were extracted. According to modified Response Evaluation Criteria in Solid Tumors (mRECIST), the differences of imaging features and histogram parameters in different response groups after TACE were analyzed. Logistic regression and receiver operating characteristic (ROC) curves were used to analyze the predictive value of meaningful parameters for response.Results There were 28 cases in response group and 26 cases in non-response group. The incidences of incomplete capsule, arterial phase peritumoral enhancement and hepatobiliary peritumoral hypointensity in the non-response group were significantly higher than those in the response group (P<0.05). The mean value, degree of variability, Perc10% and median response group were significantly higher than those in the non-response group. Logistic regression analysis showed that peritumoral enhancement in arterial phase, low signal intensity and degree of variation in hepatobiliary phase were independent influencing factors of response (P<0.05). The area under the ROC curve, sensitivity and specificity of the combined parameters were 0.904 (95% CI: 0.816-0.992), 80.8% and 96.4%, respectively.Conclusions Periarterial tumor enhancement, perihepatobiliary tumor hypointense and variation are independent predictors of response after TACE, and the predictive model combining qualitative indicators and quantitative parameters has good predictive efficacy, which helps in the precision treatment of HCC patients.
[关键词] 肝细胞癌;化疗栓塞;应答反应;肝胆期;钆塞酸二钠;直方图;磁共振成像
[Keywords] hepatocellular carcinoma;chemoembolization;response reaction;hepatobiliary phase;Gd-EOB-DTPA;histograms;magnetic resonance imaging

滕飞    任继鹏    闫瑞芳    蔡明溪    韩东明 *  

新乡医学院第一附属医院磁共振科,新乡 453100

韩东明,E-mail:625492590@qq.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: 北京康盟慈善基金会医学科研发展基金项目 B21145AN
收稿日期:2022-07-08
接受日期:2022-10-08
中图分类号:R445.2  R735.7 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.11.013
本文引用格式:滕飞, 任继鹏, 闫瑞芳, 等. 钆塞酸二钠增强MRI的影像特征和肝胆期直方图参数对肝细胞癌经动脉化疗栓塞术应答反应的预测价值[J]. 磁共振成像, 2022, 13(11): 71-75. DOI:10.12015/issn.1674-8034.2022.11.013

       肝细胞癌(hepatocellular carcinoma, HCC)是全球第六大常见癌症和第三大癌症相关死亡原因[1]。最近的国际指南建议将经动脉化疗栓塞术(transarterial chemonembolization, TACE)作为中期HCC的标准治疗方案[2, 3]。但是不同个体TACE治疗的疗效差异很大,因此,识别能够早期预测TACE术后治疗反应的因素对HCC的个体治疗具有关键意义[4]。目前已有动态对比增强MRI(dynamic contrast-enhanced MRI, DCE-MRI)、表观扩散系数(apparent diffusion coefficient, ADC)等相关研究,但参数都相对单一,难以评价其病变恶性程度及预后[5]。钆塞酸二钠(gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid, Gd-EOB-DTPA)增强MRI影像学特征可以提供形态学表现,且肝胆期更能提供肝细胞功能相关信息;直方图分析可定量分析图像包含的微观病理生理学信息,有助于疾病治疗反应预测及预后评价。近期的研究显示,Gd-EOB-DTPA增强MRI定性指标可以术前预测HCC肝切除术后早期复发[6];另一项初步研究也表明直方图参数可作为检测TACE术后复发的生物学标志物[7]。然而定性指标与定量参数的组合是否能提供更好的预测性能还未完全清楚。本研究探讨Gd-EOB-DTPA增强MRI影像特征和肝胆期直方图参数对TACE术后应答反应的预测价值。

1 材料与方法

1.1 临床资料

       本研究经新乡医学院第一附属医院伦理委员会批准(批准文号:2020025),全体受试者均签署了知情同意书。前瞻性纳入2020年6月至2021年6月在新乡医学院第一附属医院初诊的54例HCC患者。入组标准:(1)肝脏病灶经穿刺病理证实为HCC;(2)病灶呈单结节型或巨块型,未见门静脉系统瘤栓及其他部位转移;(3)术前行Gd-EOB-DTPA增强MRI检查;(4)MRI检查后1周内进行TACE手术;(5)术后定期随访。排除标准:(1)患者配合不佳,有运动伪影;(2)临床资料不全;(3)术前接受其他抗肿瘤治疗。最后纳入患者54例,其中男26例,女28例。

1.2 检查方法

       采用美国GE Discovery 750 3.0 T MRI扫描仪。常规腹部扫描序列包括横轴位T1WI双回波序列和横轴位T2WI脂肪抑制序列;增强扫描序列采用屏气肝脏快速容积(liver acceleration volume acquisition, LAVA)成像。各序列扫描参数:重复时间4.3 ms,回波时间1.6 ms,扫描视野360 mm×324 mm,矩阵260×210,层厚4.0 mm,层间距0 mm,翻转角14°;增强扫描时,高压注射器经手背静脉以2.0 mL/s的流速注射Gd-EOB-DTPA(显爱,南京正大天晴制药,中国),剂量0.1 mL/kg,注射完毕后以同样速率推注20 mL生理盐水。在注射对比剂后15~20 s、60 s、3 min和20 min分别采集增强扫描动脉期、门静脉期、过渡期和肝胆特异期图像。

1.3 图像分析及参数提取

       所有术前MRI图像均传输至医学影像存档与通信系统(picture archiving and communication systems, PACS),由2名分别具有5年和15年腹部MRI影像诊断经验的主治医师及副主任医师进行评估,分析的特征包含:(1)肿瘤形态;(2)瘤内出血;(3)包膜;(4)壁结节;(5)非边缘洗褪;(6)动脉期瘤内血管;(7)动脉期瘤周强化;(8)肝胆期瘤周低信号。

       采用3D Slicer(版本4.11.2,https://download.slicer.org/)软件,进行直方图参数提取。将肝胆期图像导入3D Slicer软件中,选取肿瘤最大层面,沿肿瘤边缘手动勾画感兴趣区(region of interest, ROI)(图1),并用Radiomics插件提取肿瘤的均值(mean)、变异度(variance)、峰度(skewnsss)、偏度(kurrosis)、第10百分位(Perc10%)、第90百分位(Perc90%)、熵(entropy)、最大值(maximum)、最小值(minimum)、中值(median)等直方图参数。

图1  Gd-EOB-DTPA增强MRI肝胆期肿瘤感兴趣区勾画示意图。
图2  非应答组典型影像特征。动脉期瘤周强化(箭),变异度为2234.5(2A);肝胆期瘤周低信号(箭),变异度为2548.9(2B)。
图3  综合预测肝细胞癌经动脉化疗栓塞术后应答反应的受试者工作特征曲线。
Fig. 1  Gd-EOB-DTPA enhanced MRI hepatobiliary stage tumor schematic sketch of the area of interest.
Fig. 2  The typical imaging features of the non-responder group. 2A shows peritumoral enhancement (arrow) in the arterial stage, with a degree of variability of 2234.5. 2B shows peritumoral tumor in the hepatobiliary stage low signal (arrow) with a variability of 2548.9.
Fig. 3  The receive operating characteristic curve for predicting the response of hepatocellular carcinoma after transcatheter arterial chemoembolization.

1.4 术后随访

       TACE术后随访3~6个月。每3个月行腹部MRI或CT增强及实验室检查。根据改良后实体瘤疗效评价标准(modified Response Evaluation Criteria in Solid Tumors, mRECIST)对治疗后肿瘤疗效情况进行分组[6]。将患者分为应答组[28例,完全缓解(complete remission, CR)+部分缓解(partial remission, PR)]及非应答组[26例,病情稳定(srable disease, SD)+疾病进展(progressive disease, PD)]。

1.5 统计学分析

       使用SPSS 25.0软件对数据进行分析。当两组数据均符合正态分布时,计量资料以均数±标准差(x¯±s)表示,否则计量资料以中位数(四分位数间距)表示,计数资料以例数表示。对不同组的一般临床资料及影像特征采用χ2检验,肝胆期直方图参数采用Mann-Whitney U检验,比较各组间参数的差异。采用组内相关系数(intra-class correlation coefficient, ICC)评价2名医师测量结果的一致性。采用线性回归及偏相关检验和排除共线性问题。采用单因素和多因素logistic回归分析确定TACE术后应答反应的独立影响因素。根据logistic回归分析结果选取差异有统计学意义的参数建立综合预测模型。采用受试者工作特征(receiver operating characteristic, ROC)曲线分析,评价综合预测效能。根据最大约登指数确定最佳的诊断阈值,获得曲线下面积(area under the curve, AUC)、敏感度、特异度。

2 结果

2.1 患者一般临床资料比较

       54例患者中,应答组28例(51.9%),非应答组26例(48.1%)。患者的性别、肝硬化、甲胎蛋白(alpha-fetoprotein, AFP)、谷草转氨酶(aspartate aminotransferase, AST)、血清总胆红素(total bilirubin, TBIL)的差异无统计学意义(P均>0.05)。而非应答组患者的肿瘤直径高于应答组,差异有统计学意义(P<0.05)(表1)。

表1  各组患者术前一般临床资料分析结果 例
Tab. 1  Analysis of preoperative general clinical data in different groups Unit: Case

2.2 应答组和非应答组的影像特征和肝胆期直方图参数比较

       非应答组不完整包膜、动脉期瘤周强化和肝胆期瘤周低信号的发生率明显高于应答组(P均<0.05);而肿瘤形态、瘤内出血、壁结节、非边缘洗褪、动脉期瘤内血管在两组间差异无统计学意义(P均>0.05)。非应答组和应答组直方图参数中均值、变异度、第10百分位和中值差异有统计学意义(P均<0.05)。而峰度、偏度、第90百分位、熵、最大值及最小值差异无统计学意义(P均>0.05)(表2表3图2)。

表2  各组患者术前影像特征分析结果 例
Tab. 2  Analysis of preoperative imaging features in different groups Unit: Case
表3  各组患者术前肝胆期直方图参数分析结果
Tab. 3  Analysis of preoperative hepatobiliary histogram parameters in different response groups

2.3 应答组和非应答组的logistic回归分析结果

       Logistic回归分析显示,动脉期瘤周强化、肝胆期瘤周低信号和变异度术前预测应答反应的优势比分别为:0.078、0.835和1.043(P均<0.010)(表4)。ROC曲线分析显示,AUC为0.904(95% CI:0.816~0.992),敏感度、特异度分别为80.8%、96.4%,且变异度的约登指数和诊断阈值为0.779、2071.7(图3)。

表4  各组患者术前logistic回归分析结果
Tab. 4  Results of preoperative logistic regression analysis in different response groups

3 讨论

       本研究旨在探究Gd-EOB-DTPA增强MRI影像特征及直方图参数综合预测模型在TACE术后应答反应中的预测价值。我们发现动脉期瘤周强化,肝胆期瘤周低信号和变异度是应答反应的独立预测因素。综合影像特征和直方图参数构建的预测模型对应答反应具有很好的预测能力。

3.1 Gd-EOB-DTPA增强MRI的优点

       在既往的研究中,部分CT和MRI的影像学特征对TACE术后应答反应有预测的价值,但单一的应用其预测效能不高,没有统一的判断标准[8, 9]。本研究中选取来自于文献报道的常见影像特征,增加了临床可操作性和重复性[10, 11]。Gd-EOB-DTPA除具有传统对比剂的动态增强特性外,还具有肝胆特异性期,且在该期病灶与周围肝实质对比度差异更大,不仅病灶更容易识别,还能反映其边缘的病理变化[12, 13, 14]

3.2 Gd-EOB-DTPA增强MRI影像特征及肝胆期直方图参数分析

       本研究发现动脉期瘤周强化及肝胆期瘤周低信号可以对TACE术后应答反应进行预测。Piscaglia等[15]的研究发现动脉期瘤周强化及肝胆期瘤周低信号是由于肿瘤边缘组织受侵犯,造成血流动力学及肝细胞功能改变,与HCC微血管侵犯有关,这些影像特征可能反映了肿瘤的侵袭性生长模式。此外,Kuang等[10]发现在TACE术后瘤周不同程度的强化都与肿瘤的局部进展相关,这是由于肿瘤周边存在丰富的微血管侵犯。侵袭性的肿瘤产生血管内皮生长因子和低氧诱导因子1α,造成基底膜和内皮不完整,进而促进新的微血管网络的形成[16, 17, 18, 19],造成TACE术中药物的分流,不能很好地沉积于病灶内,从而使应答反应有所差异。

       此外,本研究还筛选了肝胆期的直方图特征,这些特征从微观水平反映了肿瘤的异质性,实现了对肿瘤异质性的定量评估[20, 21, 22, 23]。Kuang等[10]发现T2WI及动脉期图像的直方图特征都与常规TACE术后应答反应密切相关,也说明了肿瘤的异质性可用于临床诊断、疗效评估和预后预测[24, 25, 26, 27]。其中非应答组中均值、变异度、第10百分位和中值明显高于应答组。直方图参数中均值、第10百分位及中值主要反映肿瘤细胞密度程度,与肿瘤的侵袭性生长模式有关[28, 29, 30, 31, 32],表明非应答组中病灶较应答组有更大的细胞密度,且有更强的侵袭生长性。变异度反映肿瘤的异质性[33, 34, 35],表明非应答组病灶较应答组有更大的肿瘤异质性,有更高的术后复发可能。

3.3 本研究的局限性

       本研究存在一些局限性:首先,相对较小的样本量,以及人群的选择主要局限于患有乙肝相关HCC,不可避免地带来选择性偏移;其次,本研究未采用外部验证集对构建的预测模型进行进一步验证;再次,影像特征的选取仍然存在主观因素;最后,ROI的选择采取手动勾画,有一定的测量误差。

       综上所述,术前Gd-EOB-DTPA增强MRI影像特征动脉期瘤周强化、肝胆期瘤周低信号及直方图参数变异度是TACE术后应答反应的独立预测因素,且综合的预测模型对应答反应有很好的预测效能。证明了定性指标与定量参数综合预测模型的可行性,不仅增加了临床实用性及客观性,也有助于HCC患者精准制订治疗策略。

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