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综述
磁共振T2-FLAIR错配征在预测较低级别胶质瘤分子分型中的研究进展
王瀚苇 曾琳岚 陈立朝 王舒楠

Cite this article as: Wang HW, Zeng LL, Chen LZ, et al. Research progress of T2-FLAIR mismatch sign in predicting molecular typing of lower-grade glioma[J]. Chin J Magn Reson Imaging, 2022, 13(9): 136-138, 143.本文引用格式:王瀚苇, 曾琳岚, 陈立朝, 等. 磁共振T2-FLAIR错配征在预测较低级别胶质瘤分子分型中的研究进展[J]. 磁共振成像, 2022, 13(9): 136-138, 143. DOI:10.12015/issn.1674-8034.2022.09.032.


[摘要] T2—液体衰减反转恢复(fluid attenuated inversion recovery, FLAIR)序列错配征是常规MRI中易于识别的影像学征象,表现为胶质瘤瘤体在T2WI序列上呈均匀高信号,且能被FLAIR序列部分抑制。大量研究表明,该征象能有效预测较低级别胶质瘤的分子分型,尤其是对预测异柠檬酸脱氢酶(isocitrate dehydrogenase, IDH)突变伴1p/19q未联合缺失型较低级别胶质瘤具有较高的特异性。T2-FLAIR错配征因其无创性、高特异性在未来的临床应用中具有巨大的潜力。本文就T2-FLAIR错配征的定义、病理—影像相关机制以及该征象的临床应用进行综述。
[Abstract] T2-fluid attenuated inversion recovery (FLAIR) mismatch sign is an easily recognized imaging sign in conventional magnetic resonance imaging, which is characterized by homogenous hyperintensity of the glioma on T2WI and can be suppressed by FLAIR. A large number of studies have shown that this sign can effectively predict the molecular typing of lower–grade gliomas, especially for the prediction of isocitrate dehydrogenase (IDH) mutation and 1p/19q non-codeletion. T2-FLAIR mismatch sign has great potential in future clinical application due to its noninvasive and high specificity. In this paper, we review the definition of T2-FLAIR mismatch sign, pathological-image mechanism, and clinical application.
[关键词] 磁共振成像;T2-FLAIR错配征;较低级别胶质瘤;分子分型
[Keywords] magnetic resonance imaging;T2-FLAIR mismatch sign;lower-grade gliomas;molecular typing

王瀚苇 1, 2   曾琳岚 1, 2   陈立朝 3   王舒楠 1, 2*  

1 陆军军医大学大坪医院放射科,重庆 400042

2 重庆市影像学与核医学临床研究中心,重庆 400042

3 陆军军医大学大坪医院神经外科,重庆 400042

*王舒楠,E-mail:wangshunan@tmmu.edu.cn

作者利益冲突声明:全体作者均声明无利益冲突。


基金项目: 国家自然科学基金 81701661 重庆市影像医学与核医学临床研究中心科技计划项目 CSTC2015YFPT-gcjsyjzx0175
收稿日期:2021-12-26
接受日期:2022-09-06
中图分类号:R445.2  R730.264 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.09.032
本文引用格式:王瀚苇, 曾琳岚, 陈立朝, 等. 磁共振T2-FLAIR错配征在预测较低级别胶质瘤分子分型中的研究进展[J]. 磁共振成像, 2022, 13(9): 136-138, 143. DOI:10.12015/issn.1674-8034.2022.09.032

       随着2021年WHO中枢神经系统肿瘤分类标准的更新,在传统组织学诊断的基础上,分子特征为胶质瘤精准诊断提供更多有价值的线索,同时对指导治疗及评估预后具有重要意义[1]。2级与3级胶质瘤被称为较低级别胶质瘤(lower-grade gliomas, LGG),其生物学特性与4级胶质瘤存在差异[2]。有研究表明,不同分子分型LGG之间预后差异显著[3, 4]。术前预测LGG的分子分型对临床治疗方案的制订具有指导价值。T2—液体衰减反转恢复(fluid attenuated inversion recovery, FLAIR)序列错配征(T2-FLAIR mismatch sign)是一种在常规MRI中易于识别的影像学征象,表现为胶质瘤瘤体在T2WI序列上呈均匀高信号,且能被FLAIR序列部分抑制。大量文献报道,该征象对预测异柠檬酸脱氢酶(isocitrate dehydrogenase, IDH)突变伴染色体臂1p和19q(1p/19q)未联合缺失型(IDH mutant and 1p/19q non-codeleted, IDHmt/non-codel)LGG具有较高的特异性[5, 6, 7, 8],但其敏感性欠佳并且存在一些假阳性以及演变的情况[9, 10, 11, 12]。此外,不少研究者利用T2-FLAIR错配征结合功能MRI技术以提高诊断IDHmt/non-codel LGG的效能[13, 14, 15]。本文结合近年来相关文献,对磁共振T2-FLAIR错配征在预测IDHmt/non-codel LGG中的研究和发展现状予以综述。

1 T2-FLAIR错配征的定义

       IDH基因与1p/19q是胶质瘤常见的生物学标志物,如何利用影像学特征预测上述两种生物学标志物状态是近年来的研究热点。在2017年,Patel等[5]首次提出T2-FLAIR错配征是一种可以同时预测IDH以及1p/19q状态的影像学征象。该征象在常规MRI上表现为肿瘤瘤体在T2WI序列上呈完全或接近完全均匀的高信号,相应部分在FLAIR序列上抑制呈相对低信号,外周可见高信号环[5]图1)。类似于T2-FLAIR错配征的影像学表现可以追溯至2011年,一项对原浆型星形细胞瘤MRI特征的研究发现,该类型胶质瘤瘤体在T2WI序列上表现为接近脑脊液的高信号,相应区域信号大部分在FLAIR序列上明显抑制[16]。在2007年WHO中枢神经系统肿瘤分类标准中,原浆型星形细胞瘤曾被定义为星形细胞瘤的一种少见亚型,属于WHO Ⅱ级[17]。当时,该征象与分子分型的关系不明确,直至2017年,Patel等[5]明确定义该征象并指出T2-FLAIR错配征对预测IDHmt/non-codel LGG具有高特异度(100%)。相比其他定量影像学参数而言,T2-FLAIR错配征在常规MRI中易于识别,并作为一种无创性预测IDHmt/non-codel LGG的影像征象,受到许多研究者的关注。

图1  1 例IDHmt/non-codel LGG患者的T2-FLAIR错配征。1A:T2WI 显示瘤体呈均匀高信号;1B:FLAIR显示瘤体呈相对低信号,外周可见高信号环。IDHmt/non-codel LGG:异柠檬酸脱氢酶突变伴染色体臂1p 和19q未联合缺失型较低级别胶质瘤;T2-FLAIR:T2 液体衰减反转恢复。

2 T2-FLAIR错配征的病理—影像相关机制

       目前,T2-FLAIR错配征的病理—影像相关机制尚不明确。对单一病变不同部位多次取材进行病理学研究显示,T2-FLAIR错配征区域具有微囊变成分,无T2-FLAIR错配征区域几乎没有微囊变成分[18],这表明T2-FLAIR错配征可能与病理学上微囊变有关[9,18, 19]。Yamashita等[20]初步验证了T2-FLAIR错配征与微囊变的相关性,并且发现细胞间隙增大也与T2-FLAIR错配征有关。进一步对LGG基因表达谱和蛋白质组学分析发现,哺乳动物雷帕霉素靶蛋白(mammalian target of rapamycin, mTOR)信号通路基因表达和蛋白质水平在具有T2-FLAIR错配征的患者中增加,而酪氨酸激酶受体2(erbB-2)水平降低[5]。随后的研究表明,mTOR相关基因过表达与IDHmt/non-codel LGG中的T2-FLAIR错配征有关,但其相互作用机制不明确[20]。因此,T2-FLAIR错配征相关病理生理机制有待深入研究。

       Zhao等[21]认为肿瘤细胞内含较多的自由水是造成IDHmt/non-codel LGG出现T2-FLAIR错配征的原因。扩散加权成像(diffusion weighted imaging, DWI)是无创性反映组织中水分子的微观扩散状态的功能成像方法,利用表观扩散系数(apparent diffusion coefficient, ADC)能够定量评估组织内游离水分子的扩散速率,组织内细胞越密集,水分子扩散受限,ADC值越低。研究发现,T2-FLAIR错配征阳性肿瘤比阴性肿瘤有更高的平均ADC值[22]。同时,T2-FLAIR错配征在FLAIR上表现为边缘高信号环以及与中心相对低信号的区域具有不同的ADC值,中心低信号区域的ADC值高于外周高信号环,这种差异间接反映了肿瘤细胞内部可能含有较多水分子,同时肿瘤细胞与肿瘤微环境间存在差异[19,23]。此外,Kinoshita等[24]提出一种观点,不同分子分型的LGG在MRI上表现出不同的弛豫时间,其中IDHmt/non-codel LGG在MRI上具有长T1长T2弛豫时间特征,T2-FLAIR错配征恰好反映出这种独特的弛豫时间,不同的图像采集参数可能会影响T2-FLAIR错配征的显示。在未来研究中有必要使用规范化的MRI扫描场强以及参数,以提高T2-FLAIR错配征的识别性,指导临床应用。

3 T2-FLAIR错配征的临床应用

3.1 T2-FLAIR错配征的诊断效能

       Patel等[5]在训练组与测试组中采用T2-FLAIR错配征预测IDHmt/non-codel LGG显示,两组均具有高诊断特异度(100%),但敏感度较低(分别为22%、45%)。Lasocki等[6]利用肿瘤内T2-FLAIR错配征存在面积的比例不同进行分层研究,结果显示T2-FLAIR错配征存在>50%的面积时预测1p/19q未联合缺失特异度高。随后Broen等[7]证实,T2-FLAIR错配征可作为预测IDHmt/non-codel LGG高特异度(100%)的影像学征象。总的来说,T2-FLAIR错配征对IDHmt/non-codel LGG的诊断效能佳,其特异度、敏感度、阳性预测值及阴性预测值大约为90.7%~100%、22%~58.7%、91.7%~100%、54%~76%[5, 6, 7,25]。有研究者提出T2-FLAIR错配征的特异性高是建立在严格的定义标准上,尤其是肿瘤内须具有完全或接近完全均匀的同质T2高信号以及FLAIR高信号环才能够被定义为T2-FLAIR错配征[7,26]。但是,由于胶质瘤的异质性造成MRI各序列上信号多变,如此严格的诊断标准是造成T2-FLAIR错配征敏感性较低的重要因素,T2-FLAIR错配征在临床的广泛应用受到一定程度的限制。当下,对T2-FLAIR错配征的认识仍存在不足。对此,Throckmorton等[9]提出无论T2WI信号是否为均质高信号,只要相应T2WI高信号区域在FLAIR能抑制,即部分T2-FLAIR错配征,也可作为IDHmt/non-codel LGG的影像学标志物,当纳入部分T2-FLAIR错配征作为诊断标准时,T2-FLAIR错配征的诊断敏感度提高了30%,特异度没有因此受到影响。不少研究支持Throckmorton等的观点,认为部分T2-FLAIR错配征可用于预测LGG的分子分型[27, 28]。如何提高T2-FLAIR错配征的敏感性值得进一步探讨。

3.2 T2-FLAIR错配征假阳性与演变

       尽管T2-FLAIR错配征在预测IDHmt/non-codel LGG方面具有高度特异性,但也存在一些假阳性的情况。特别是儿童患者,例如,毛细胞星形细胞瘤、异位灰质、H3 K27M突变型弥漫性中线胶质瘤及含有MYB重排的星形细胞瘤中发现T2-FLAIR错配征[10]。在成人患者中发现IDH突变伴1p/19q联合缺失型少突胶质细胞瘤[10, 11, 12,18]和胶质母细胞瘤[9,12]也可表征T2-FLAIR错配征。有学者认为,T2-FLAIR错配征出现在不含钙化成分的胚胎发育不良性神经上皮肿瘤[29]及弥漫性内生性脑桥胶质瘤[30]中,这一征象并非IDHmt/non-codel LGG的独特表现。但总的来说,T2-FLAIR错配征对成人型IDHmt/non-codel LGG具有较高的特异性。

       此外,T2-FLAIR错配征的演变一定程度提示LGG恶性转化:具有T2-FLAIR错配征的LGG在最大程度安全范围切除后,肿瘤复发为同类型LGG时,复发肿瘤可再次显示T2-FLAIR错配征;而转化为高级别胶质瘤时,T2-FLAIR错配征消失[9]。当复发性胶质瘤患者无法再次进行手术切除时,T2-FLAIR错配征或许可作为无创性检测LGG是否恶性转化的征象。

3.3 T2-FLAIR错配征联合功能MRI

       MRI作为一种无创的检查方法,不仅能在术前提供肿瘤解剖信息,而且能在一定程度反映分子特征[31]。功能MRI技术,如DWI[13]、灌注加权成像(perfusion weighted imaging, PWI)[32, 33, 34]、磁共振波谱(magnetic resonance spectroscopy, MRS)[35, 36]、正电子发射断层扫描/MRI(positron emission computed tomography/MRI, PET/MRI)[37]、多模态MRI参数[38]以及影像组学[39]可揭示胶质瘤不同分子分型上的差异。Batchala等[8]提出了基于T2-FLAIR错配征及影像学特征的两步分类算法预测分子特征,此算法首先利用T2-FLAIR错配征预测IDHmt/non-codel LGG;其次在T2-FLAIR错配征阴性的肿瘤中利用肿瘤位置、纹理特征等进一步对LGG进行分子分型预测,该算法的预测准确率高达86.3%。T2-FLAIR错配征阳性的LGG常表现为较高的ADC值,T2-FLAIR错配征联合ADC值与T2-FLAIR错配征单一诊断IDHmt/non-codel LGG相比敏感度提高8%[13]。T2-FLAIR错配征结合ADC、脑血容量(cerebral blood volume, CBV)直方图参数,不仅能提高诊断不同分子分型的效能,而且这种定量MRI参数有助于减少假阳性的情况[14]。利用T2-FLAIR错配征结合多模态MRI技术,包括DWI、SWI、动态磁敏感对比增强灌注成像,将进一步优化对IDHmt/non-codel LGG的诊断效能[15]。此外,T2-FLAIR错配征联合伦勃朗图像(visually accessible Rembrandt images, VASARI)、临床因素以及多参数影像组学特征可提供一种术前无创性预测LGG分子分型的方法[40]。T2-FLAIR错配征结合多种功能MRI参数时有利于提高对IDHmt/non-codel LGG的诊断效能,并且能够弥补T2-FLAIR错配征敏感性较差的缺陷。

4 总结与展望

       尽管多模态MRI和PET/MRI发展迅速,但常规MRI仍然是临床上诊断胶质瘤不可替代的成像手段之一。T2-FLAIR错配征作为一种无创的、易于识别的以及高度特异性的影像学征象,在LGG分子分型的诊断上具有巨大的潜力。然而,现有研究存在以下几个缺点:(1)大多是回顾性研究,研究样本量小且来源于单中心研究,存在选择偏倚的情况;(2)T2-FLAIR错配征作为一种定性的影像学征象,不同研究者之间因临床经验不同存在识别差异;(3)病理上对T2-FLAIR错配征区域定点取材难以开展。未来T2-FLAIR错配征的研究可从以下几个方面进行:(1)来自多中心、大样本的研究;(2)利用机器学习或深度学习开发肿瘤自动分割方法改善研究者间存在的视觉差异,量化T2-FLAIR错配征的错配程度;(3)深入研究T2-FLAIR错配征的病理生理机制。综上所述,T2-FLAIR错配征在无创性预测LGG分子分型方面具有深远的发展前景。

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