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临床研究
集成MRI联合三维动脉自旋标记成像鉴别胶质瘤复发和假性进展的初步研究
吕瑞瑞 杨治花 葛鑫 王明磊 黄雪莹 刘珊 马文富 王晓东

Cite this article as: Lü RR, Yang ZH, Ge X, et al. Preliminary study of synthetic MRI combined with three-dimensional arterial spin labeling imaging in differentiating recurrence and pseudoprogression of glioma[J]. Chin J Magn Reson Imaging, 2022, 13(8): 19-23, 35.本文引用格式:吕瑞瑞, 杨治花, 葛鑫, 等. 集成MRI联合三维动脉自旋标记成像鉴别胶质瘤复发和假性进展的初步研究[J]. 磁共振成像, 2022, 13(8): 19-23, 35. DOI:10.12015/issn.1674-8034.2022.08.004.


[摘要] 目的 探讨集成MRI(synthetic magnetic resonance imaging, syMRI)联合三维动脉自旋标记成像(three dimension arterial spin labeling, 3D-ASL)在鉴别胶质瘤复发和假性进展中的应用价值。材料与方法 回顾性分析2020年7月至2022年3月于宁夏医科大学总医院手术病理证实为高级别胶质瘤并术后辅以放化疗后出现异常强化灶患者病例38例。将入组病例按修订版脑胶质瘤治疗反应评估标准分为复发组(22例)和假性进展组(16例)。所有患者均行3D-ASL及syMRI序列扫描。测量异常强化区脑血流量(cerebral blood flow, CBF)及增强后T1值(T1-Gd)、T2值(T2-Gd)。采用独立样本t检验或Mann-Whitney U检验比较复发组和假性进展组各参数的差异,对差异具有统计学意义的参数绘制受试者工作特征(receiver operating characteristic, ROC)曲线,分析评价各参数及其联合诊断的效能。结果 复发组T1-Gd低于假性进展组T1-Gd,差异有统计学意义(P<0.001),T2-Gd两组间差异无统计学意义(P>0.05),复发组CBF值高于假性进展组,差异有统计学意义(P<0.001)。ROC曲线分析结果显示,T1-Gd、CBF值ROC曲线下面积(area under the curve, AUC)分别为0.882、0.916, T1-Gd联合CBF值的AUC为0.951。结论 syMRI联合3D-ASL有助于无创鉴别脑胶质瘤复发和假性进展,且诊断效能优于单一MR参数。
[Abstract] Objective To evaluate the value of synthetic MRI (synthetic MRI, syMRI) combined with three-dimensional arterial spin labeling imaging (3D-ASL) in differentiating recurrence and pseudoprogression of glioma.Materials and Methods Thirty-eight patient cases with surgical pathologically confirmed glioma and abnormal enhancing foci after postoperative adjuvant radiotherapy at the General Hospital of Ningxia Medical University from July 2020 to March 2022 were collected. The enrolled cases were divided into recurrence group (22 cases) and pseudoprogression group (16 cases) according to the Modified Criteria for Radiographic Response Assessment in Glioblastoma (mRANO). All patients underwent 3D-ASL and syMRI serial scans. The cerebral blood flow (CBF) value of abnormal enhancement area and post-enhancement T1 value (T1-Gd) and T2 value (T2-Gd) were measured. Independent sample t test or Mann-Whitney U test was used to compare the differences of parameters between recurrence and pseudoprogression group. Receiver operating characteristic (ROC) curve was used to analyze the diagnostic efficacy of T1-Gd, CBF and the combination.Results T1-Gd in recurrence group was lower than T1-Gd in pseudoprogression group, and the difference was statistically significant (P<0.001). The difference between the two groups in T2-Gd was not statistically significant (P>0.05). The CBF value in recurrence group was higher than that in pseudoprogression group, and the difference was statistically significant (P<0.001). The results of ROC curve analysis showed the area under the curve (AUC) was 0.882 and 0.916 for T1-Gd and CBF values, and the AUC was 0.951 for T1-Gd combined with CBF values.Conclusions Synthetic MRI combined with 3D-ASL is helpful to non-invasively distinguish the recurrence and pseudoprogression of glioma, and its diagnostic efficiency is better than that of single MR parameter.
[关键词] 胶质瘤;复发;假性进展;集成磁共振成像;三维动脉自旋标记成像;诊断
[Keywords] glioma;recurrence;pseudoprogression;synthetic magnetic resonance imaging;three-dimensional arterial spin labeling imaging;diagnosis

吕瑞瑞 1   杨治花 2   葛鑫 1   王明磊 3   黄雪莹 3   刘珊 3   马文富 1   王晓东 3*  

1 宁夏医科大学临床医学院,银川 750004

2 宁夏医科大学总医院肿瘤医院放疗科,银川 750004

3 宁夏医科大学总医院放射科,银川 750004

王晓东,E-mail:xdw80@yeah.net

作者利益冲突声明:全体作者均声明无利益冲突。


基金项目: 宁夏回族自治区自然科学基金 2022AAC03487 宁夏回族自治区科技重点研究计划 2019BEG03037
收稿日期:2022-05-13
接受日期:2022-08-05
中图分类号:R445.2  R730.264 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.08.004
本文引用格式:吕瑞瑞, 杨治花, 葛鑫, 等. 集成MRI联合三维动脉自旋标记成像鉴别胶质瘤复发和假性进展的初步研究[J]. 磁共振成像, 2022, 13(8): 19-23, 35. DOI:10.12015/issn.1674-8034.2022.08.004

       胶质瘤是中枢神经系统最常见的原发恶性肿瘤,复发和死亡率高,研究发现胶质母细胞瘤的平均生存时间仅12~14个月[1],预后差。目前治疗方式是最大范围手术切除、术后辅以放化疗[2],同步放化疗完成后,MRI检查出现异常强化灶,可能是复发或假性进展,两者影像学表现相似加之出现异常强化灶时间窗相似,在临床诊疗过程中误诊率很高,这依然是国内、外研究的难题[3],两者治疗方案和预后完全不同,因此早期无创准确鉴别非常必要[4]。集成MRI(synthetic magnetic resonance imaging, syMRI)采用多动态多回波(multi-dynamic multi-echo, MDME)采集方式,一次扫描获得多种对比度图像,还可以获得具有组织弛豫特性的T1、T2值,在特定场强下不易受扫描设备和参数影响,能从微观角度反映组织病理生理特征[5],已广泛应用于神经系统[6]、乳腺[7]、心脏[8]、前列腺[9]、骨骼系统[10]等部位。三维动脉自旋标记成像(three dimension arterial spin labeling, 3D-ASL)使用射频反转脉冲对自身动脉血液进行磁性标记,不受血脑屏障限制,能够定量评估脑肿瘤血流灌注情况[11]。传统MRI根据形态学进行诊断,不能量化评估病灶,导致鉴别困难,syMRI可以对病灶进行定量分析,本研究拟采用syMRI联合3D-ASL定量分析胶质瘤复发和假性进展的差异,为两者的鉴别诊断提供新的思路。

1 材料与方法

1.1 一般资料

       回顾性分析自2020年7月至2022年3月于我院行脑胶质瘤全切术,术后辅以放化疗的患者病例。纳入标准:(1)术后病理为高级别胶质瘤;(2)术后未见残留肿瘤病灶;(3)放化疗后定期MRI随访临床症状加重且出现新发强化灶;(4)接受常规MRI、3D-ASL和syMRI检查者。排除标准:(1)临床或病理资料不完善者;(2)患者状态欠佳等导致图像伪影重不能分析者。本研究经宁夏医科大学总医院科研伦理委员会批准(批准文号:KYLL-2022-0298),免除受试者知情同意。

1.2 仪器与方法

       扫描设备为3.0 T磁共振扫描仪(Signa Architect;GE Healthcare, USA)及48通道头颈联合科研线圈。所有患者先接受3D-ASL及syMRI扫描,syMRI增强前后各扫描一次。syMRI扫描参数:TR 4214 ms, TE 21.6 ms,矩阵256×256,视野24 cm×24 cm,平均激发次数1,层数20,层厚5 mm,层间隔1 mm,扫描时长3 min 39 s; 3D-ASL采集方式为3D螺旋快速自旋回波成像,扫描参数:TR 4854 ms,TE 53.5 ms,点数×螺旋臂512×6,视野24 cm×24 cm,带宽±62.5 kHz,层数36,层厚4 mm,激励次数3,标记后延迟时间2025 ms,扫描时长3 min 22 s。采用专用高压注射器,肘静脉团注钆双胺(GE,美国),剂量为0.2 mL/kg,注射速率为3.0 mL/s,再以同样速率注射生理盐水20 mL,行syMRI扫描,参数同前。

1.3 图像分析及参数测量

       扫描后将DICOM数据传输至GE ADW 4.7对syMRI及3D-ASL数据进行测量分析,由2名分别具有神经影像诊断经验3年、5年的住院医师及主治医师在未知随访结果的情况下,对自动生成的T1 mapping、T2 mapping及脑血流量(cerebral blood flow, CBF)伪彩图进行测量。分析步骤:(1)结合T1WI+C图像避开病灶出血、坏死、囊变区,选取相对容易识别强化区域勾画感兴趣区(region of interest, ROI)进行测量(ROI范围为0.2~0.4 cm2); (2)测量各ROI的CBF值及T1-Gd、T2-Gd,测量3次取平均值。

1.4 分组依据

       采用修订版脑胶质瘤治疗反应评估标准(Modified Criteria for Radiographic Response Assessment in Glioblastoma, mRANO)[12],将病例分为复发组和假性进展组。符合以下条件之一为肿瘤复发:(1)脑组织活检或二次手术组织学检查可见肿瘤细胞;(2)随访期内(≥6个月)术区强化范围增大,周围水肿加重,临床症状加重。符合以下条件之一为假性进展:(1)脑组织活检或二次手术未发现肿瘤细胞;(2)随访期内术区强化范围减小,周围水肿减轻,临床症状减轻。由两名高年资神经影像诊断医师完成,达成一致结果。

1.5 统计学分析

       采用SPSS 26.0和MedCalc 20.0软件进行统计学分析。对符合正态分布及方差齐性的计量资料以(x¯±s)表示,两组间比较采用独立样本t检验,不符合正态分布的资料以MQ1Q3)表示,组间比较采用Mann-Whitney U检验。采用组内相关系数(intraclass correlation coefficient, ICC)评价两名医师测量参数的一致性,ICC>0.75为一致性良好,0.65~0.75为一致性一般,ICC<0.65为一致性差。对差异有统计学意义的参数,采用受试者工作特征(receiver operating characteristic, ROC)曲线及二元logistic回归分析各参数及其联合的诊断效能,计算AUC,确定syMRI参数、CBF值以及联合鉴别诊断的最佳临界值,敏感度和特异度,评估不同参数对复发和假性进展的诊断效能。结果均以双侧P<0.05为差异有统计学意义。

2 结果

2.1 临床资料

       最终收集38例符合纳入排除标准的患者病例(表1),男24例,女14例,根据二次手术病理或MRI增强随访≥6个月(图1、2)进行分组,22例为肿瘤复发(手术病理证实7例);16例为假性进展(手术病理证实3例)。

图1  女,60岁,脑胶质瘤患者。病理:左侧额叶胶质母细胞瘤(WHO 4级),IDH1(+),MGMT(+),1p/19q联合缺失(-)。1A:T1WI增强左侧额叶占位;1B:术后MRI未见肿瘤残留;1C~1F:同步放化疗后复查;1C:随访期内左侧额叶术区出现异常强化灶;1D:经3D-ASL后处理的CBF伪彩图;1E:synthetic MRI增强后T1 mapping;1F:6个月后病灶强化范围明显减小,为假性进展。
图2  男,55岁,脑胶质瘤患者。病理:右侧额叶胶质母细胞瘤(WHO 4级),IDH1(-),MGMT(-),1p/19q联合缺失(-)。2A:T1WI增强右侧额叶占位;2B:术后MRI未见肿瘤残留;2C~2F:同步放化疗后复查;2C:随访期内右侧额叶术区出现异常强化灶;2D:经3D-ASL后处理的CBF伪彩图;2E:synthetic MRI增强后T1 mapping;2F:6个月后病灶强化范围较前增大,为肿瘤复发。IDH1:异柠檬酸脱氢酶1;MGMT:O6-甲基鸟嘌呤-DNA-甲基转移酶;3D-ASL:三维动脉自旋标记;CBF:脑血流量;synthetic MRI:集成磁共振成像。
Fig. 1  Ftemale, 60 years old, glioma patient. Pathology: glioblastoma of left frontal lobe (WHO grade 4), IDH1 (+), MGMT (+), combined deletion of 1p/19q (-). 1A: T1WI enhanced the left frontal lobe space occupying; 1B: No tumor tissue was found after operation on MRI; 1C-1F: The review after simultaneous radiotherapy; 1C: T1WI enhancement scan showed irregular enhancement of the lesion; 1D: CBF pseudo-color map; 1E: T1 mapping after synthetic MRI enhancement; 1F: After 6 months, T1WI enhancement showed that the enhancement range decreased obviously, confirmed as pseudoprogression.
Fig. 2  Male, 55 years old, glioma patient. Pathology: glioblastoma of right frontal lobe (WHO grade 4), IDH1 (-), MGMT (-), combined deletion of 1p/19q (-). 2A: T1WI enhanced the right frontal lobe space occupying; 2B: No tumor tissue was found after operation on MRI; 2C-2F: The review after simultaneous radiotherapy. 2C: T1WI enhancement showed abnormal reinforcing foci in the right parietal area, 2D: CBF pseudo-color map, 2E: T1 mapping after synthetic MRI enhancement, 2F: After 6 months, enhancement of T1WI showed the enhancement range of the lesion was larger than before, confirmed as recurrence.IDH1: isocitrate dehydrogenase 1; MGMT: O6-methylguanine-DNA-methyltransferase; 3D-ASL: three-dimensional arterial spin labeling; CBF: cerebral blood flow.
表1  复发组和假性进展组患者的临床资料
Tab. 1  Clinical data of patients in the recurrence and pseudoprogression groups

2.2 脑胶质瘤复发组与假性进展组syMRI各参数值及CBF值比较

       脑胶质瘤复发组T1-Gd低于假性进展组,差异有统计学意义(P<0.001),复发组CBF值高于假性进展,差异有统计学意义(P<0.001)。T2-Gd在两组间差异无统计学意义(P>0.05)(表2)。

表2  胶质瘤复发组与假性进展组各参数比较( x ¯ ±s
Tab. 2  Comparison of parameters between the recurrence and pseudoprogression groups (x¯±s)

2.3 脑胶质瘤复发组与假性进展组syMRI参数值及CBF值ROC分析

       T1-Gd、CBF值鉴别脑胶质瘤复发与假性进展的AUC分别为0.882、0.916。CBF值AUC较高,T1-Gd、CBF两者联合时,诊断效能较单参数提高(AUC=0.951)(表3图3)。

图3  T1-Gd、CBF 及其联合的ROC 曲线。T1-Gd:增强后T1 值;CBF:脑血流量;ROC:受试者工作特征。
Fig. 3  ROC curves of T1-Gd, CBF and their combination. T1-Gd: T1 value after enhancement; CBF: cerebral blood flow; ROC: receiver operating characteristic.
表3  T1-Gd、3D-ASL参数及两者联合的ROC曲线分析结果
Tab. 3  T1-Gd, 3D-ASL parameters and their combination ROC curve analysis results

3 讨论

       本研究利用syMRI联合3D-ASL成像技术鉴别胶质瘤复发和假性进展,研究发现两者联合鉴别诊断的效能较好。既往研究示syMRI成像已应用于胶质瘤基因型预测以及瘤周区域增强前后的定量分析[13, 14, 15],但尚未利用该序列行复发和假性进展鉴别的研究,本研究利用syMRI定量反映两者异常强化灶增强后信号差异,联合3D-ASL分别定量显示强化灶的微观结构及血流灌注,为两者鉴别提供影像学依据。

3.1 syMRI参数(T1-Gd)鉴别脑胶质瘤复发和假性进展

       syMRI是一种定量技术,通过单次扫描获得10种对比度图像,还能测定组织的5种绝对量值[16, 17],可以定量增强前后病灶的信号变化,且弛豫时间为组织固有属性,与不同扫描设备或固定场强下的扫描参数无关,克服了传统MRI不同机型扫描导致参数变化大这一缺点,为疾病的定量诊断提供更客观和更稳定的信息[18]。本研究T1-Gd在胶质瘤复发和假性进展中具有差异,复发组T1-Gd更小。其原因可能是在胶质瘤复发时伴有未成熟微血管增多,局部含水量增加,钆剂滞留时间延长,而钆剂是顺磁性物质,可以缩短组织T1弛豫时间[19],因此肿瘤复发T1-Gd值降低更明显。此外,病灶的强化程度与病变组织血供是否丰富以及血脑屏障被破坏的程度有关[20],肿瘤细胞生长侵犯血脑屏障,导致血管通透性增加进而使血液等成分渗到血管外或细胞外间隙,注入钆剂后外漏,因此T1-Gd一定程度量化了血脑屏障的破坏程度[21]。Akbari等[22]利用机器学习的多参数MRI定量分析显示,复发区域T1-Gd序列的对比度摄取增加,可能指示区域血管生成,并与肿瘤浸润区域的血脑屏障受损相关。这与本研究结果相似,本研究发现复发组T1-Gd明显低于假性进展组,可能是由于胶质瘤复发时血供丰富并血脑屏障破坏更严重,T1-Gd值明显下降。

       国外学者研究[23]发现胶质瘤假性进展及复发有不同的对比剂代谢特点,肿瘤复发时对比剂代谢特征为快速流入—流出型曲线,而假性进展等治疗后反应的对比剂代谢特征为持续流入型曲线。本研究中我们在注射对比剂后约1 min 30 s采集增强后syMRI序列,脑胶质瘤复发伴不成熟微血管生成,血管壁局部缺失,对比剂较假性进展流入更快更多,对比剂缩短T1弛豫时间的作用在复发时更明显,两者对比剂代谢特点不同引起T1-Gd值的差异。

       T2-Gd在两组间差异无统计学意义(P=0.052),其原因可能是:脑胶质瘤浸润性生长方式以及手术、放化疗等治疗后导致术区组织成分复杂,T2-Gd测量可能会受到影响。T2是反映组织游离水的标志物,复发和假性进展均表现为不同程度组织水肿,T2-Gd可能是非特异性的标志。本研究样本量较少,仍需大量样本研究来证实T2-Gd在两组间是否有差异。

3.2 3D-ASL鉴别脑胶质瘤复发和假性进展

       3D-ASL是一种无创灌注技术,利用自身动脉血中水分子进行射频脉冲磁化标记,不依赖于对比剂注射,受敏感性伪影的影响较小[24],且不受血脑屏障的影响,能真实反映组织灌注水平,加之采用螺旋式采集以及螺旋状K空间填充,扫描成像范围广,实现全脑三维容积成像[25]。动态磁敏感对比(dynamic susceptibility contrast, DSC)成像需要注射对比剂作为外源性示踪剂,成像速度较快、灌注参数多,但由于对比剂的注入,易产生磁敏感伪影[26]。胶质瘤手术及放化疗治疗术区脑组织结构改变,DSC成像因局部磁敏感伪影较重,一定程度会影响数据测量。3D-ASL使用快速旋转回波技术与螺旋式读出相结合,可有效降低磁敏感伪影[11]。3D-ASL通过反映血管内皮生长因子的表达情况来定量肿瘤微循环[27]。复发是由于血管内皮生长因子表达增加,继发新血管生成,且新生血管壁不成熟,通透性增加,表现为高灌注;假性进展由于血管源性水肿等炎性反应,缺乏新血管,表现为低灌注[28]。本研究结果显示复发组CBF值高于假性进展组,与先前研究结果[11]一致。

3.3 T1-Gd联合3D-ASL鉴别脑胶质瘤复发和假性进展

       胶质瘤复发和假性进展在常规MRI都表现为放化疗后3~6个月新发强化灶形成[29],加之由于手术、放化疗等治疗方式使术区病理成分复杂,常规MRI难以鉴别肿瘤复发和假性进展[30]。syMRI可以定量显示组织结构的微观信息,本研究结果显示,T1-Gd在两组间有差异。3D-ASL与DSC相比优势是通过使用内源性动脉示踪技术,一定程度降低术区磁敏感伪影使病灶更好地显示。复发和假性进展病理结构复杂,单独使用CBF值评估复发和假性进展存在一定局限性,Pellerin等[26]联合ASL、正电子发射断层-MRI(positron emission tomography combined with magnetic resonance imaging, PET-MRI)进行鉴别胶质瘤复发和假性进展的研究,分别从血流灌注和组织代谢反映强化灶性质,提高了诊断效能。本研究中将CBF值与T1-Gd两者联合,其诊断效能较单一参数有所提高。

3.4 局限性

       本研究的局限性:(1)本研究样本量较少,且大多依据影像学随访结果分组;(2)病灶组织成分复杂,一定程度造成ROI测量存在偏差;(3)本研究中增强后syMRI序列扫描时间是在注入对比剂后约1 min 30 s,这一扫描时间点是否为采集的适合时间点,有待进一步研究;(4)未行3D-ASL及DSC两种不同灌注成像CBF值比较,这为我们今后研究提供了方向。

       综上所述,本研究采用syMRI联合3D-ASL鉴别胶质瘤复发和假性进展,结果说明该方法具有一定的临床应用价值,为两者的鉴别诊断提供了一种有意义的功能成像方法。

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