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综述
磁共振弹性成像在腹盆部肿瘤中的研究进展
张潇月 王效春

Cite this article as ZHANG X Y, WANG X C. Research progress of magnetic resonance elastography in abdominal and pelvic cancer[J]. Chin J Magn Reson Imaging, 2024, 15(5): 216-221.本文引用格式张潇月, 王效春. 磁共振弹性成像在腹盆部肿瘤中的研究进展[J]. 磁共振成像, 2024, 15(5): 216-221. DOI:10.12015/issn.1674-8034.2024.05.035.


[摘要] 肿瘤力学特性与肿瘤侵袭、进展密切相关,准确评估肿瘤组织硬度对于肿瘤的检测、鉴别诊断、诊疗规划及预后评估具有重要意义。磁共振弹性成像(magnetic resonance elastography, MRE)能量化组织力学特性,无创定量评估组织硬度,进而间接反映组织纤维化程度。本文将对MRE的基本原理、技术发展及其在腹盆部肿瘤中应用的研究现状进行综述,旨在为未来的研究提供新思路,推进MRE的不断成熟,辅助指导临床精准诊疗。
[Abstract] The mechanical properties of tumors are closely associated with tumor invasion and progression, and the accurate assessment of tumor tissue stiffness holds significant importance in tumor detection, treatment planning, and prognosis evaluation. Magnetic resonance elastography (MRE) enables the quantification of tissue mechanical properties, noninvasive and quantitative evaluation of tissue stiffness, as well as indirect reflection of the extent of tissue fibrosis. This article provides a review on the fundamental principles, technical advancements, and research status of MRE in abdominal and pelvic tumors with an aim to offer novel insights for future investigations while promoting the continuous maturation of MRE technology to aid in guiding clinical precision diagnosis and treatment.
[关键词] 肝脏;胰腺;前列腺;肾脏;肿瘤;磁共振弹性成像
[Keywords] liver;pancreas;prostate;kidney;neoplasms;magnetic resonance elastography

张潇月 1   王效春 2*  

1 山西医科大学医学影像学院,太原 030001

2 山西医科大学第一医院影像科,太原 030001

通信作者:王效春,E-mail:2010xiaochun@163.com

作者贡献声明::王效春拟定本综述的写作思路,指导撰写稿件,对稿件重要的内容进行了修改,获得了国家自然科学基金、山西省“四个一批”科技兴医创新计划项目重大科技攻关专项、中华国际医学交流基金会2023 sky影像科研基金资助;张潇月起草和撰写稿件,获取、分析并解释本综述的参考文献;全体作者都同意最后的修改稿发表,都同意对本研究的所有方面负责,确保本综述的准确性和诚信。


基金项目: 国家自然科学基金项目 81971592 山西省“四个一批”科技兴医创新计划项目重大科技攻关专项 2023XM011 中华国际医学交流基金会2023 sky影像科研基金项目 z-2014-07-2301
收稿日期:2024-01-25
接受日期:2024-04-17
中图分类号:R445.2  R735  R737 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2024.05.035
本文引用格式张潇月, 王效春. 磁共振弹性成像在腹盆部肿瘤中的研究进展[J]. 磁共振成像, 2024, 15(5): 216-221. DOI:10.12015/issn.1674-8034.2024.05.035.

0 引言

       组织机械特性会随生理和病理过程发生显著变化,也是疾病进展的关键组成部分。肿瘤组织硬度增加与其生长、代谢、侵袭和转移密切相关[1]。触诊能直接感知组织硬度,但多用于表浅病变,且不可避免受到操作者经验和敏感程度影响,限制了诊断的应用范围和准确性[2]。超声弹性成像(ultrasound elastography, USE)由于成本较低、用途广泛等优点受到关注,但同时具有阴影、杂波伪影、信号衰减、操作者依赖性等局限性[3]

       MRE是一种非侵入性“触诊”技术,具有较触诊与USE更强的客观性和更好的可重复性,能扩展触诊的深度与广度。MRE最早于1995年被Muthupillai等报告,其通过机械剪切波应力作用所致的空间映射和定量位移,直接量化组织内部的力学特性[4],为定量分析病理组织生物学信息提供有力依据。目前,MRE逐渐应用于腹盆部肿瘤相关研究,在疾病检测、鉴别诊断、预后评估中具有重要价值,但对于此方面的综合分析和全面评估较为有限。因此,本文就MRE的基本原理及其在腹盆部肿瘤的研究现状进行综述,探讨其潜在临床应用价值,以对相关疾病的进一步研究提供参考。

1 MRE理论基础及技术发展

1.1 病理基础

       机械特性变化是肿瘤治疗反应和恶性行为的重要驱动因素。由于纤维化,肿瘤细胞外基质(extracellular matrix, ECM)硬度高于正常组织[5],而基质金属蛋白酶作用下的基质降解,会导致基质重构,增加肿瘤组织流动性,二者均与肿瘤侵袭性密切相关[6]。硬度和压力升高是肿瘤微环境的物理特征,其主要成分是间质液压力(interstitial fluid pressure, IFP)。升高的IFP为侵袭和转移提供条件,也是药物递送的物理屏障[1]。与IFP不同,固体应力包含在ECM和细胞弹性成分中,随肿瘤和基质细胞的增殖而传递,其在大多数健康组织中可忽略不计,但在肿瘤级联的组织、细胞、分子等不同水平上都起着关键调节作用,是肿瘤生长的标志物[5, 7]

1.2 基本原理与技术发展

       MRE成像主要步骤包括:(1)利用外部机械振动器在组织中产生可传播的剪切波;(2)通过与机械振动频率相似的梯度脉冲序列,获取对组织位移敏感的相位图像;(3)使用反演算法从位移数据得到组织的机械特性或弹性图[8]。MRE最常用的结果参数是给定频率下的复合剪切模量G*,其实部G'和虚部G″分别量化为储能模量和损耗模量,代表组织的弹性和黏性行为;剪切模量幅值|G*|常被描述为刚度或剪切刚度[2, 9]

       MRE的出现使量化力学特性成为可能,但复杂的机械设备、高昂的检查费用及较长的扫描时间均在一定程度上限制其临床应用。此外,剪切波振幅在穿透组织时会快速衰减,衰减程度与频率正相关,而频率的降低会影响空间分辨率,难以分辨出小病灶[10, 11]。由于腹盆部器官位置、形态及毗邻的特殊性,准确且可重复的刚度测量是MRE规范应用的又一大挑战。

       为产生具有足够空间分辨率的剪切波,研究人员开发了经尿道、直肠和会阴等多种剪切波激励设备。此外,有研究[12]表明3D-MRE可对波场数据进行3D分析,在评估组织硬度方面具有高度可重复性。但3D-MRE扫描时间长,技术要求较高,故普及率不高。基于3D多频MRE的断层弹性成像可提供更高的空间分辨率,用于检测小病变。除硬度外,断层弹性成像可通过损耗角φ来表征组织流动性[13]。流动性是从MRE同一数据集获得的独立于硬度的力学参数,较单独的硬度对比度更优,且可作为监测和预测侵袭性和转移潜力的预后标志物[6]

       此外,研究人员进一步提出虚拟磁共振弹性成像(virtual MRE, vMRE),vMRE基于组织弹性和水扩散间的显著相关性,通过体素内不相干运动(intravoxel incoherent motion, IVIM)引起的相位分布和IVIM效应,生成虚拟IVIM弹性图像,产生依赖于振动频率或振幅组合的弹性驱动的对比[10, 14],进而定量评估组织硬度。因而,vMRE的最大优势是具有不受MRE硬件能力限制的虚拟振动频率和振幅范围。

2 MRE在腹盆部肿瘤的应用

2.1 肝脏

       肝脏是MRE应用最成熟的器官,已广泛应用于肝脏纤维化,成为慢性肝病的主要诊断工具。近年来部分研究表明MRE在肝肿瘤评估方面也显示出一定优势。

2.1.1 预测HCC发生

       肝纤维化是肝细胞癌(hepatocellular carcinoma, HCC)发生的关键危险因素,对HCC发展具有良好的预测性,已是共识,而作为可间接量化肝纤维化程度的MRE技术在此方面的价值也得到进展和应用。MOTOSUGI等[15]发现HCC患者MRE的肝硬度测量值(liver stiffness measurement, LSM)显著高于非HCC患者(5.0 kPa vs. 3.9 kPa),可能是HCC发展的重要预测因素。随后,HIGUCHI等[16]发现HCC发生风险随LSM的增加而增加,呈剂量依赖性。但肝纤维化后HCC的发生是长期事件,单点测量LSM不能准确分层风险,ICHIKAWA等[17]指出持续高LSM是HCC发生的更大风险因素,通过MRE纵向监测LSM有助于分层慢性肝病患者发生HCC的风险,可能是一种更有价值的评价方式。

       部分研究为MRE成为HCC病理或分子特征的预测因子奠定基础。李宗泰等[18]纳入47例HCC患者,发现MRE鉴别低分化与中高分化HCC的曲线下面积(area under the curve, AUC)为0.869,且中高分化HCC的肿瘤硬度(tumor stiffness, TS)显著低于低分化HCC(7.40 kPa vs. 11.98 kPa),但结果与先前研究[19]相反,这可能与肿瘤坏死的比例相关。Ki-67高水平与HCC高侵袭性密切相关,而MRE对深度学习联合影像组学预测Ki-67表达的模型具有良好附加价值,AUC达0.90,独立测试队列的AUC为0.83[20]

2.1.2 鉴别良/恶性肝脏局灶性病变

       国内外研究[21, 22]均表明恶性肝脏局灶性病变(focal liver lesion, FLL)刚度明显高于良性,且临界值相近(5.00 kPa[21] vs. 5.09 kPa[22]),但上述研究中良性FLL与正常肝组织弹性值的比较结果截然相反,可能与测量方法及样本量等多种因素相关,如感兴趣区域(region of interest, ROI)[23]、应力[24]、机械频率[25]。HENNEDIGE等[26]发现MRE鉴别良恶性FLL的AUC优于扩散加权成像(diffusion weighted imaging, DWI)(0.986 vs. 0.82)。而GARTEISER等[27]发现,尽管恶性FLL的|G*|和G″均高于良性[(3.38±0.26)kPa vs.(2.41±0.15)kPa和(2.25±0.26)kPa vs.(1.05±0.13)kPa],但G″的AUC明显大于|G*|,达0.774,提示肿瘤流动性在鉴别良恶性肿瘤方面具有重要价值。随后,SHAHRYARI等[28]引入断层弹性成像,以c和φ作为黏弹性参数,在区分良恶性病变方面展现出基于硬度的高敏感度(94%)和基于流动性的高特异度(92%),且与c相比,φ具有更高的AUC,为0.95。王矜涵等[29]用vMRE技术对224例FLL患者评估也发现,恶性FLL的硬度明显高于良性(Z=-12.309),vMRE鉴别良恶性FLL的敏感度为92.2%,特异度为96.7%,AUC为0.981,但恶性病变之间尚不能完全区分,可能与病变的异质成分相关。因而,组织流动性与硬度相结合的固液组织特性,可能为表征FLL提供新的无创定量成像标志物。

2.1.3 预后预测

       肝切除术(hepatic resection, HR)是肝恶性肿瘤最有效的治疗方法,但复发及术后并发症是患者长期生存的主要威胁。若患者不适应HR,可据病程选择肝动脉化疗栓塞术(transcatheter arterial chemoembolization, TACE)、射频消融术(radiofrequency ablation, RFA)、放射治疗、免疫治疗、靶向治疗等非手术治疗。因此,术后不良结局的风险评估对患者管理方案的选择至关重要。

       肝纤维化与HCC术后复发显著相关。一项Mate分析[30]显示术前LSM与术后结局相关性良好,是HCC复发的潜在生物标志物。CHO等[31]指出治疗前高LSM(界值5.5 kPa)是HCC患者完全缓解后早期复发的独立风险因素;亚组中,TACE组的LSM界值(6.0 kPa)高于HR/RFA组(4.5 kPa),意味着接受TACE的晚期患者较多,LSM基础值较高。ZHANG等[32]还探讨了MRE诊断乙肝病毒/乙型肝炎病毒相关HCC晚期复发的价值,多变量分析显示LSM是晚期复发的唯一独立预测因子,在术前和术后模型中均具有高特异度(90.0%),AUC为0.860。但先前的研究[33]显示血管浸润和TS是早期复发风险因素,TS每增加1 kPa,复发风险增加16.3%,LSM则与复发无显著相关性(P=0.699)。PARK等[34]测量95例HCC患者整个肿瘤(whole tumor, WT)和剔除坏死区后肿瘤实质部分(solid portion, SP)的TS,发现TS-SP与无复发生存期正相关,而TS-WT与RFS负相关,这看似矛盾的结果可能由于TS与肿瘤坏死显著相关,高级别HCC坏死面积更大,硬度较低。因此,TS-SP可能比TS-WT更好地代表HCC的生物学侵袭性。

       在预测术后并发症方面,有研究[35]报告,术前LSM与总体术后并发症显著相关,优势比为1.78。HUI等[36]在治疗前对HCC患者的肿瘤和非肿瘤区域进行MRE评估,发现与治疗方式无关,非肿瘤区域LSM能独立预测相关并发症,如腹水、静脉曲张出血等,风险比为1.384,特别是局部/全身治疗组中,TS≥5.7 kPa+非肿瘤硬度≥3.7 kPa的患者相关并发症发生风险明显增加(86.7%和40.0%)。肝切除术后肝功能衰竭(posthepatectomy liver failure, PHLF)是主要并发症之一,HR后残肝再生能力不足可导致PHLF。既往研究[37]证明,LSM是预测PHLF的有效生物标志物,AUC=0.740。ZHANG等[38]以再生指数(regeneration index, RI)作为肝再生能力的评价指标,发现LSM越低,RI越高,LSM预测RI的AUC达0.882。CHO等[39]纳入多种独立危险因素(高LSM、低血清白蛋白、切除肝段≥3个等)开发基于LSM的预测模型,其预测PHLF的AUC为0.877,对B和C级PHLF预测性能更佳,AUC达0.923。

       综上,HCC是一种异质性肿瘤,MRE表征的组织力学特性将肿瘤病理变化与侵袭性相联系,为更好管理患者提供新的生物标记物。但图像处理方式、磁场强度、扫描序列设置、刺激频率、ROI等的差异仍可能是影响最终结论的重要因素,因而更具信服力的结果需要大样本的数据验证以统一规范化扫描设置。

2.2 胰腺

       由于胰腺良恶性疾病临床症状和影像特征重叠,且胰腺位于腹膜后,活检及剖腹探查风险较大,胰腺癌的早期诊断具有高度挑战性。而胰腺导管腺癌(pancreatic duct adenocarcinoma, PDAC)具有促纤维组织增生反应的特征[40],因此,能够无创评估力学性质的MRE显得尤为重要。

       SHI等[41]将MRE与糖类抗原199(carbohydrate antigen 199, CA19-9)鉴别胰腺良恶性肿块的性能进行比较,发现刚度比的诊断性能优于硬度和CA199,AUC达0.912,特别是鉴别PDAC和肿块型胰腺炎。LIU等[42]进一步证明,较胰腺良性肿块,PDAC具有更高的硬度、刚度比及CA199,三者组合诊断的AUC达0.975 8,提高了诊断准确性;研究还发现,不同于良性肿块,胰腺实质硬度与PDAC硬度正相关。自身免疫性胰腺炎(autoimmune pancreatitis, AIP)具有与PDAC相似的肿瘤样肿胀和继发性梗阻,但ZHU等[43]发现胰腺实质流动性不受继发性梗阻影响,即流动性可区分恶性与非恶性继发性梗阻,是PDAC较硬度更具特异性的特征;该研究对208例患者进行断层弹性成像,发现AIP的硬度和流动性显著低于PDAC,高于健康胰腺,二者鉴别PDAC与AIP的AUC为0.906和0.872。在预测PDCA病理分级和预后的研究中,MRE也显示出较好的价值[44]

       综上,MRE可作为有效的定量成像标记用于胰腺疾病的鉴别诊断及肿瘤侵袭性的预测。但剪切波在胰腺中传播模式复杂,MRE在胰腺应用的最大挑战可能是剪切波的有效传导及高分辨率图像的获得,而3D-MRE、断层弹性成像技术的发展为准确评估胰腺疾病提供了可靠的方法。

2.3 前列腺

       前列腺癌(prostate cancer, PCa)诊断的“金标准”是系统穿刺活检,采用的是非靶向、系统间隔的采样方式,会导致漏诊及过高或过低的错误分类。因而,PCa诊断更倾向于基于成像的靶向活检方法。

       REITER等[45]用500 Hz MRE评估14例PCa切除标本的节段黏弹性,结果显示癌性与良性节段的G'平均值为10.84 kPa和5.44 kPa,且G'诊断的AUC高于|G*|和G″,为0.81,表明MRE有诊断PCa的潜力。LI等[46]发现,PCa的c(3.4 m/s)和φ(1.3 rad)显著高于良性前列腺病变(2.6 m/s,1.0 rad)和健康对照者(healthy controls, HCs)(2.2 m/s,0.8 rad),且c+φ(AUC=0.95)显著改善了前列腺成像报告和数据系统2.1版评分(AUC=0.85)的诊断性能,亚组中鉴别移行带(central zone, CZ)PCa与前列腺增生(benign prostatic hyperplasia, BPH)、外周带(peripheral zone, PZ)PCa与前列腺炎的AUC为0.91和0.94;该研究还揭示了在HCs中,CZ的刚度和流动性具有年龄依赖性,而PZ没有。淋巴结转移是PCa预后的重要预测因素,HU等[47]用基于MRE的PCa硬度术前预测淋巴结转移显示出良好性能,AUC达0.982。由于前列腺的异质性,适当的组织分割至关重要。ALDOJ等[48]用MRE和密集U-net分割对前列腺不同区域的黏弹性进行全自动定量分析,纳入40例BPH或PCa患者的6组数据(T2WI、DWI、表观扩散系数、MRE幅度、c和φ)训练U-net网络,发现基于MRE幅度图的分割能力更可靠,在整个前列腺、CZ和PZ的Dice系数分别达0.93±0.04、0.95±0.03、0.77±0.05。

       综上,MRE可准确区分正常腺体、良性病变和肿瘤组织,在PCa术前诊断、空间定位和临床分期中发挥重要价值。但粘弹性值的年龄依赖性不可忽视,因此,参考值的建立应具化到年龄组和前列腺亚区域,可在一定程度上提高前列腺疾病诊断的特异性和重复性。

2.4 其他

2.4.1 肾脏

       PREZZI等[49]对5例嗜酸细胞瘤和11例肾透明细胞癌(clear-cell renal cell carcinomas, ccRCC)患者评估,发现较T2WI、动态对比增强、DWI,MRE的鉴别能力更强,ccRCC具有比嗜酸细胞瘤更高的c和更低的G″。微血管浸润(microvascular invasion, MVI)是ccRCC预后的重要因素。ZHANG等[50]对T1期ccRCC研究发现,MVI组的平均硬度(5.4±0.6 kPa)与无MVI组(4.1±0.3 kPa)存在显著差异。值得注意的是,肾纤维化是肾病进展的标志,而分级肾缺血的研究[51]表明,伴有肾血流量减少的肾实质萎缩能降低组织硬度,掩盖肾纤维化,这可能导致相关研究结论不一致,因而需要学者们对其进一步完善、验证。

2.4.2 子宫

       OBRZUT等[52]发现,子宫肌瘤硬度随细胞外结缔组织成分占比增加而增加,提示MRE可作为子宫肌瘤的特征性诊断工具。最近,有研究[53]探索了TS在宫颈癌(cervical cancer, CC)分级与病理亚型的术前预测价值,发现低分化CC的TS显著高于高/中分化CC(5.21 kPa vs. 3.47 kPa,P=0.038),且腺癌组TS明显高于鳞癌组(5.27 kPa vs. 3.44 kPa,P=0.042)。此前,ZHANG等[54]同样证实TS可能是子宫内膜癌(endometrial carcinoma, EC)侵袭性的潜在预测因子,发现以3.04 kPa为临界值区分肌层浸润≥50%和肌层浸润<50%的敏感度为100.0%,特异度为77.8%。因此,MRE对CC及EC患者的治疗选择和预后预测具有一定指导意义。

2.4.3 胃肠道

       ECM中胶原蛋白含量是结直肠癌(Colorectal cancer, CRC)进展的重要因素,HU等[55]研究发现胶原体积分数(collagen volume fraction, CVF)与TS正相关(P<0.05),且c在区分高风险和低风险CRC方面具有与CVF相似的诊断准确性,AUC分别为0.82和0.89,因而TS可作为ECM胶原蛋白沉积的定量成像标志物,对预测CRC侵袭性具有补充价值。MRE在肾、子宫及胃肠道肿瘤应用较少,但上述研究展示出其在相关疾病鉴别和术前风险分层的可行性,值得进一步探索。

3 小结

       目前MRE在腹盆部肿瘤的研究仍有很多部位未涉及,如膀胱、脾脏等,但USE在膀胱癌[56, 57]中的探索及MRE对脾脏硬度标准值的研究[58]为MRE相关价值的进一步证实提供生物学基础及可行性证据,将使其在肿瘤领域更广泛的研究得以充分实现。

       MRE作为MRI技术的拓展,可对体内传播的剪切波进行成像,量化组织力学特性,具有很强的可重复性,有望成为新的生物力学肿瘤标志物。但MRE在腹盆部的应用仍存在一些挑战:首先,研究多为小样本临床或临床前研究;其次,MRE需额外配置硬件设备,成本相对较高,且检查时间较长,大规模普及相对困难,且不同腹盆部器官具有独特的解剖位置和生理特性,需要针对性的制动器、序列采集及后处理方式;最后,MRE的扫描序列、参数及设备不同,获得的图像存在一定差异;另外,考虑到组织亚区域的变异性,尽管已有部分研究对不同器官的正常标准值进行探索,但仍缺乏公认的标准。

       因此,MRE的临床应用尚需不断改进成像技术,进行大样本临床研究。同时,确立不同器官正常值的标准共识,是将MRE纳入疾病评估的第一步,也是关键一步。随技术的发展,MRE在腹盆部疾病的应用将有更大潜力,特别是断层弹性成像、vMRE、3D-MRE等新技术的出现,极大提高了MRE临床推广的可能性。

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下一篇 MRI影像组学和深度学习在前列腺癌中的研究进展
  
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