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临床研究
T2 mapping联合mDixon-Quant多参数成像定量评估子宫内膜癌微卫星不稳定状态的研究
马长军 田士峰 陈丽华 宋庆玲 宋清伟 林良杰 刘爱连

Cite this article as: Ma CJ, Tian SF, Chen LH, et al. Quantitative assessment of microsatellite instability in endometrial cancer by T2 mapping combined with mDixon-Quant multiparameter imaging[J]. Chin J Magn Reson Imaging, 2022, 13(8): 48-54.本文引用格式:马长军, 田士峰, 陈丽华, 等. T2 mapping联合mDixon-Quant多参数成像定量评估子宫内膜癌微卫星不稳定状态的研究[J]. 磁共振成像, 2022, 13(8): 48-54. DOI:10.12015/issn.1674-8034.2022.08.009.


[摘要] 目的 探讨T2定量成像(T2 mapping)联合魔镜成像(mDixon-Quant)的多参数成像定量评估子宫内膜癌(endometrial cancer, EC)微卫星不稳定状态(microsatellite instability, MSI)中的应用价值。材料与方法 回顾性分析大连医科大学附属第一医院2019年6月至2021年9月经病理证实的34例EC患者的影像资料。所有患者术前两周均行3.0 T MRI检查,扫描序列包括T1WI、T2WI、T2 mapping、mDixon-Quant等。由两位观察者采用独立盲法测量病灶T2 mapping序列的T2值及mDixon-Quant序列的脂肪分数(fat fraction, FF)值、R2*值、T2*值。采用组内相关系数(intra-class correlation coefficient, ICC)评估两位观察者测量结果的一致性,采用独立样本t检验或Mann-Whitney U检验比较各参数值的差异,采用受试者工作特征(receiver operating characteristic, ROC)曲线评估参数预测EC MSI状态的效能。采用Delong检验比较各曲线下面积(area under the curve, AUC)间的差异性。结果 两位观察者测量值的一致性均很好(ICC>0.75);MSI组的R2*值及T2值均高于微卫星稳定(microsatellite stabilization, MSS)组,MSI组的T2*值低于MSS组,差异均具有统计学意义(P<0.05);R2*值、T2*值、T2值及联合参数评估EC的MSI状态的AUC值分别为0.773、0.761、0.780、0.939;Delong检验结果显示各单一参数评估EC MSI状态的AUC间差异无统计学意义(P>0.05);联合参数评估EC MSI状态的AUC与单一参数评估EC MSI状态的AUC间差异有统计学意义(P<0.05)。结论 mDixon-Quant及T2 mapping多参数成像均能定量地评估EC MSI状态,两者联合可明显提升预测的效能,具有很好的临床应用前景。
[Abstract] Objective To explore the application value of T2 mapping combined with mDixon-Quant multiparameter imaging in quantitative assessment of microsatellite instability (MSI) in endometrial cancer (EC).Materials and Methods The imaging data of 34 EC patients who were pathologically confirmed in our hospital from June 2019 to September 2021 were retrospectively analyzed. All patients underwent 3.0 T magnetic resonance imaging examination two weeks before surgery, and the scanning sequence included T1WI, T2WI, T2 mapping, mDixon-Quant, etc. Two observers independently and blindly measured the T2 value of the lesion T2 mapping sequence and the fat fraction (FF) value, R2* value and T2* value of the mDixon-Quant sequence. The intra-class correlation coefficient (ICC) was used to evaluate the consistency of the measurement results between the two observers, and the independent samples t-test or Mann-Whitney U test was used to compare the differences of each parameter value. The efficacy of parameters to predict EC MSI status was assessed using receiver operating characteristic (ROC) curves. The Delong test was used to compare the differences among the area under the curves (AUCs).Results The agreement between the two observers' measurements was good (ICC>0.75). The R2* value and T2 value of the MSI group were higher than those of the microsatellite stabilization (MSS) group, and the T2* value of the MSI group was lower than that of the MSS group, and the differences were statistically significant (P<0.05). The AUC values of R2* value, T2* value, T2 value and the combined parameters for evaluating the MSI status of EC were 0.773, 0.761, 0.780 and 0.939, respectively; the results of Delong test showed that there was no significant difference in the AUC of each single parameter for evaluating the MSI status of EC (P>0.05). There is a statistically significant difference between the AUC of the combined parameter to assess the EC MSI status and the AUC of the single parameter to assess the EC MSI status (P<0.05).Conclusions Both mDixon-Quant and T2 mapping multi-parameter imaging can quantitatively evaluate EC MSI status. The combination of the two can significantly improve the prediction performance and has a good clinical application prospect.
[关键词] 子宫内膜癌;微卫星不稳定;T2定量成像;魔镜成像;磁共振成像
[Keywords] endometrial cancer;microsatellite instability;T2 mapping;mDixon-Quant;magnetic resonance imaging

马长军 1, 2   田士峰 1, 2   陈丽华 1, 2   宋庆玲 1, 2   宋清伟 1, 2   林良杰 3   刘爱连 1, 2*  

1 大连医科大学附属第一医院放射科,大连 116011

2 大连市医学影像人工智能工程技术研究中心,大连 116011

3 飞利浦(中国)投资有限公司,上海 200040

刘爱连,E-mail:cjr.liuailian@vip.163.com

作者利益冲突声明:全部作者均声明无利益冲突。


收稿日期:2022-03-22
接受日期:2022-08-05
中图分类号:R445.2  R737.33 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.08.009
本文引用格式:马长军, 田士峰, 陈丽华, 等. T2 mapping联合mDixon-Quant多参数成像定量评估子宫内膜癌微卫星不稳定状态的研究[J]. 磁共振成像, 2022, 13(8): 48-54. DOI:10.12015/issn.1674-8034.2022.08.009

       子宫内膜癌(endometrial cancer, EC)是女性生殖系统常见的恶性肿瘤,在发达国家位居首位,并且呈年轻化趋势[1]。导致EC发生的危险因素有很多,如代谢异常、初潮早、携带子宫内膜癌遗传的易感基因[2]等。微卫星不稳定(microsatellite instability, MSI)是因错配修复(mismatch repair, MMR)基因缺陷而导致错配碱基不能被纠正,引起基因突变累积,最终导致肿瘤的发生[3, 4],这些基因的突变会引起遗传性非息肉病性结直肠癌、林奇综合征(Lynch syndrome, LS)、EC[5]等。同时评估MSI状态在EC的治疗[6]及预后评估[7]方面也有一定的价值,如在MSI的EC患者中程序性死亡受体(programmed death 1, PD-1)及程序性死亡受体配体(programmed cell death-ligand, PD-L1)高表达[8, 9],二者可以抑制T细胞的增殖、分化,使T细胞功能失活,对肿瘤细胞的抑制作用减弱。PD-1/PD-L1抑制剂可以恢复T细胞对肿瘤细胞的抑制作用[10],可以对MSI的EC患者进行靶向治疗。有研究[11]也报道了PD-1/PD-L1抑制剂对MSI状态EC的疗效高于MSS者,故检测EC患者MSI状态可以筛查LS及评估肿瘤疗效与预后等,可为EC患者个性化精准治疗提供合理依据。

       T2定量成像(T2 mapping)作为一种定量的MRI技术,可提供水和胶原纤维的含量和组成的量化信息[12],已应用于心脏、神经和骨关节的定量评估。魔镜成像(mDixon-Quant)序列是一种水脂分离定量技术[13, 14],利用水质子和脂肪质子进动频率差,通过调节回波时间做多次采集,一次屏气采集6个回波,结合7个峰值脂肪模型和T2*校正,得到脂肪分数图(fat fraction, FF)、R2*图、T2*图。mDixon-Quant技术已经应用于定量评估脂肪含量的相关研究中,如肝脏脂肪含量的定量研究[15]、腰椎椎体脂肪含量的研究[16]等。据我们所知,之前没有报道使用mDixon-Quant和T2 mapping定量参数来评估EC MSI状态。本研究拟基于T2 mapping与mDixon-Quant多参数成像,从分子层面对EC MSI状态进行评估。

1 材料与方法

1.1 研究对象

       本研究经大连医科大学附属第一医院伦理委员会批准,免除知情同意,批文号:PJ-KS-KY-2021-99(X)。回顾性分析2019年6月至2021年9月在大连医科大学附属第一医院因临床怀疑子宫疾病行子宫MRI检查的299例患者资料。纳入标准:(1)经手术后病理证实为EC,并且有完整、翔实的临床病理资料,根据MMR蛋白(MLH-1、MSH-2、MSH-6、PMS-2)的表达缺失情况,本研究分为MSI组与MSS组,其中四种MMR蛋白均表达被定义为MSS状态,至少有一种MMR蛋白不表达被定义为MSI状态[17];(2)术前两周内行盆腔3.0 T MRI检查,扫描序列包括mDixon-Quant、T2 mapping,且图像质量良好;(3)检查前未接受其他治疗或处置。排除标准:(1)患者免疫组化指标中无MMR蛋白表达情况;(2)图像伪影大或病灶显示不清影响诊断与数据测量;(3)扫描序列中不包括mDixon-Quant序列或T2 mapping序列。最终MSI组纳入12例患者,MSS组纳入22例。

1.2 扫描方法及参数

       采用Philips Ingenia 3.0 T CX磁共振扫描仪(Philips Healthcare,Best,the Netherlands)进行扫描,使用32通道线圈。检查前嘱咐患者排空膀胱和肠管,禁食水4 h。同时训练患者呼吸,以免检查过程中出现大的呼吸运动伪影影响图像质量。有节育环者检查前1 d取出,患者取仰卧位,足先进,扫描序列包括轴位2D-T2WI、矢状位2D-T2WI、扩散加权成像(diffusion weighted imaging, DWI)(b=0、800 s/mm2)、mDixon-Quant及T2 mapping序列,具体参数如表1所示。

表1  MRI序列扫描参数
Tab. 1  MRI scan parameters of each sequence

1.3 图像分析和数据测量

       图像的分析和数据的测量由两位放射科医生(分别具有7年、2年子宫MRI读片经验)在对患者病理信息未知的情况下独立进行。把mDixon-Quant序列和T2 mapping序列的图像传输到ISP(Intellispace Portal, Philips Healthcare)7.0工作站,分别生成mDixon-Quant序列的FF图、R2*图、T2*图及T2 mapping序列的T2图(图1图2);以T2WI图像为参考,选择肿瘤最大径所在层面,在肿瘤实质区域逐点手动勾画两个感兴趣区(region of interest, ROI),ROI覆盖范围尽可能大(ROI大小大于肿瘤实质的1/3),避开坏死、囊变、出血区,并适当避开肿瘤边缘,避免部分容积效应。勾画的ROI会自动复制到功能参数图上(FF图、R2*图、T2*图、T2图),然后记录每个参数的平均值做进一步的研究。

图1  66岁中分化子宫内膜样腺癌患者,微卫星不稳定状态。1A:轴位T2WI示子宫体积增大,见宫腔内稍高信号肿块;1B:脂肪分数(FF)图,FF值为2.06%;1C:R2*图,R2*值为30.195 Hz;1D:T2*图,T2*值为48.325 ms;1E:T2 mapping序列的T2图,T2值为107.1 ms;1F~1I:错配修复(MMR)蛋白表达情况(免疫组化图片,×200),1F为MSH6表达、1G为MSH2表达、1H为PMS缺失、1I为MLH1表达。
Fig. 1  A 66-year-old patient with moderately differentiated endometrioid adenocarcinoma, microsatellite instability status. 1A: Axial T2WI showing enlarged uterus with slightly high signal mass in the uterine cavity; 1B: Fat fraction (FF) map, FF value is 2.06%; 1C: R2* map, R2* value is 30.195 Hz; 1D: T2* map, T2* value is 48.325 ms; 1E: T2 map, T2 value is 107.1 ms; 1F – 1I: Mismatch repair protein expression (immunohistochemistry, ×200), where 1F is MSH6 expression, 1G is MSH2 expression, 1H is PMS deletion, and 1I is MLH1 expression.
图2  51岁高分化子宫内膜癌患者,微卫星稳定状态。2A:轴位T2WI示子宫体积增大,见宫腔内稍高信号肿块;2B:脂肪分数(FF)图,FF值为1.435%;2C:R2*图,R2*值为18.3 Hz;2D:T2*图,T2*值为59.18 ms;2E:T2 mapping序列的T2图,T2值为82.265 ms;2F~2I:错配修复(MMR)蛋白表达情况(免疫组化图片,×200),其中2F为MSH6表达、2G为MSH2表达、2H为PMS表达、2I为MLH1表达。
Fig. 2  A 51-year-old patient with well-differentiated endometrial cancer, microsatellite stabilization status. 2A: Axial T2WI showing enlarged uterus, a slightly high signal mass in the uterine cavity; 2B: Fat fraction (FF) map, FF value is 1.435%; 2C: R2* map, R2* value is 18.3 Hz; 2D: T2* map, T2* value is 59.18 ms; 2E: T2map, T2 value is 82.265 ms; 2F–2I: Mismatch repair protein expression (immunohistochemistry, ×200), where 2F is MSH6 expression, 2G is MSH2 expression, 2H is PMS expression, and 2I is MLH1 expression.

1.4 统计学方法

       使用SPSS 22.0软件(Chicago, IL, USA)及MedCalc 15.2.2 软件(MedCalc Software, Ostend, Belgium)进行统计学分析。使用组内相关系数(intra-class correlation coefficient, ICC)比较两位观察者对两组患者mDixon-Quant序列参数和T2 mapping序列参数测量值间的一致性,ICC>0.75为一致性良好,采用两位观察者测量数据的平均值进行后续的分析。两种序列参数值采用Kolmogorov-Smirnov检验各数据是否符合正态分布,符合正态分布的数据用均值±标准差的形式表示,并进行独立样本t检验;不符合正态分布的数据采用中位数(25%分位数,75%分位数)来表示,并进行Mann-Whitney U检验。两组患者一般临床病理资料以例数或率(%)表示,组间比较采用卡方检验或者Fisher确切概率法。采用受试者工作特征(receiver operating characteristic, ROC)曲线评估差异有统计学意义的参数在评估EC MSI状态的效能,计算曲线下面积(area under the curve, AUC),并根据最大约登指数确定其阈值、敏感度和特异度。采用二元logistic回归计算差异有统计学意义的参数联合评估EC MSI状态的预测值。采用Delong检验比较各AUC间的差异性。P<0.05为差异具有统计学意义。

2 结果

2.1 临床一般资料

       纳入本研究的34例EC患者中,MSI组12例,阳性率为35.29%。两组病例在年龄、病理分化等级、国际妇产科联盟(International Federation of Gynecology and Obstetrics, FIGO)分期、肌层浸润深度、绝经前后、有无阴道不规则流血间差异均无统计意义(P>0.05),如表2所示。

表2  MSI组与MSS组患者一般临床资料的比较
Tab. 2  Comparison of general clinical data of patients in MSI group and MSS group

2.2 两位观察者测量结果的一致性

       两位观察者对mDixon-Quant序列的FF值、R2*值、T2*值及T2 mapping序列的T2值测量结果的一致性良好,ICC均>0.75,如表3所示。

表3  两位观察者测量结果的一致性
Tab. 3  Agreement between two observers' measurements

2.3 两组病例间参数差异

       MSI组的R2*值及T2值均高于MSS组,差异均具有统计学意义(P<0.05);MSI组的T2*值低于MSS组,差异具有统计学意义(P<0.05);MSI组的FF值低于MSS组,差异无统计学意义(P>0.05)(表4图3)。

图3  微卫星不稳定(MSI)组和微卫星稳定(MSS)组子宫内膜癌(EC)各参数小提琴图。3A~3C:MSI组与MSS组EC的R2*值、T2*值及T2值差异均有统计学意义。注:*P<0.05,**P<0.01,***P<0.001。
图4  受试者工作特征曲线分析各参数评估MSI EC状态的效能。
Fig. 3  The violin chart for R2* (3A), T2* (3B), and T2 (3C) values in microsatellite instability (MSI) and microsatellite stabilization (MSS) endometrial cancer (EC). There were significant differences in R2*, T2*, and T2 values between MSI group and MSS group EC. Note: *: P<0.05; **: P<0.01; ***: P<0.001.
Fig. 4  Receiver operating characteristic curve analysis of the efficacy of each parameter to assess EC MSI status.
表4  两组病例各参数比较结果
Tab. 4  Comparison of the parameters of the two groups of patients

2.4 两组病例各参数评估效能比较

       R2*值、T2*值、T2值及mDixon-Quant联合T2 mapping(R2*值+T2*值+T2值)评估EC MSI状态的效能依次为0.773、0.761、0.780、0.939;Delong检验结果显示各单一参数评估EC MSI状态的AUC间差异无统计学意义(P>0.05);mDixon-Quant联合T2 mapping评估EC MSI状态的AUC与单一参数评估EC MSI状态的AUC间差异有统计学意义(P<0.05)(图4表5表6)。

表5  两组病例各参数评估效能比较
Tab. 5  Comparison of the evaluation performance of each parameter between the two groups of cases
表6  各参数评估子宫内膜癌微卫星不稳定状态效能差异的比较
Tab. 6  Comparison of differences in the efficacy of various parameters to assess endometrial cancer microsatellite instability status

3 讨论

3.1 评估EC MSI状态的临床意义和现状

       检测EC患者MSI状态可以筛查LS及评估肿瘤疗效与预后等,如PD-1/PD-L1抑制剂可以对MSI的EC患者进行靶向治疗[10],可为EC患者个性化精准治疗提供合理依据。以往有研究通过影像学手段于术前对胃癌、直肠癌、EC等肿瘤MSI状态进行了预测评估,如Zhang等[18]通过基于T2WI序列的深度学习方法对直肠癌MSI状态进行了评估,其预测效能良好;Bhosale等[19]通过小视野体素内不相干运动(reduced field-of-view intravoxel incoherent motion, rFOV-IVIM)成像序列区分FIGO ⅠA期MSI状态EC与MSS状态EC,发现MSS组EC的表观扩散系数(apparent diffusion coefficient, ADC)值和真扩散系数(D)值高于MSI组EC;也有研究利用扩散张量成像(diffusion tensor imaging, DTI)序列[20]和磁敏感序列[增强梯度回波T2*加权血管成像序列(enhanced T2 star weighted angiography, ESWAN)][21]评估了EC MSI状态。其中IVIM和DTI功能成像技术对水分子的扩散运动可进行更为精确的描述,ESWAN序列对顺磁性和逆磁性等血液代谢产物具有很高的敏感性,可以间接反映肿瘤内新生血管的形成和肿瘤的乏氧状态,且拥有高分辨率、薄层扫描的优势,其较常规MRI序列不仅可获得幅值图以及相位图的信息,并提供多个量化参数,可以对EC MSI状态进行定量评估,然而这几种成像序列信噪比和分辨率不高,易受肠气、呼吸及蠕动伪影等影响,且成像技术要求较高,IVIM成像需要多个高b值,DTI未建立子宫扫描参数及重建技术的统一标准而主要借鉴于神经系统,ESWAN序列处于研究初步阶段,所得到的定量成像参数T2*值及R2*值目前在临床疾病中并没有临床统一的界定值。

3.2 T2 mapping评估EC MSI状态的价值

       T2 mapping技术是定量成像技术中的一种,具有客观性及较好的可重复性、稳定性,已广泛应用于关节软骨病变[22, 23]、软组织损伤[24]、心肌病[25]等的研究中,而关于T2 mapping技术应用于EC的研究鲜有报道。本研究基于T2 mapping技术,发现MSI组EC的T2值低于MSS组EC的T2值,可能是因为MSI相关肿瘤通常有更多的淋巴血管浸润性生长以及淋巴细胞浸润肿瘤组织[20,26],局部细胞数目增多,细胞间隙减小,水分子运动受限,自由水含量减低,使得MSI组EC的T2值高于MSS组。

3.3 mDixon-Quant评估EC MSI状态的价值

       mDixon-Quant序列的R2*参数是横向弛豫率,通过不同时间梯度的重聚得到,与组织中的脱氧血红蛋白浓度直接相关[27, 28],其不受TE、B0等影响,可直接反映组织成分的变化。T2*为有效横向弛豫时间,T2*值是R2*[29, 30]的倒数。当血液的代谢产物脱氧血红蛋白、含铁血黄素、正铁血红蛋白等顺磁性物质使磁场不均匀性发生去相位时,T2*值降低,R2*值升高。mDixon-Quant序列已经在EC中得到了初步探索和研究,如鉴别Ⅰ期EC和子宫内膜息肉[31],发现Ⅰ期EC的R2*值高于子宫内膜息肉,且差异具有统计学意义;评估EC免疫组化指标Her-2的表达[32],发现在Her-2阳性表达的EC患者中R2*值高。本研究中MSI组EC的R2*值高于MSS组而T2*值低于MSS组,是由于MSI型肿瘤具有更高的循环内皮祖细胞和血管内皮生长因子(vascular endothelial growth factor, VEGF)水平[33],使其具有更高的微血管密度,但是肿瘤组织新生血管的血管壁较弱且不稳定,使得肿瘤组织出血,血液淤积,血氧利用过度,脱氧血红蛋白、含铁血黄素等顺磁性物质增多[34, 35],与此同时MSI相关肿瘤淋巴细胞浸润,单位体积内细胞密度增高,增加肿瘤组织的耗氧量,使得肿瘤局部脱氧血红蛋白等顺磁性物质增多[27],综合上述原因,最终使得MSI组EC的R2*值高于MSS组EC而T2*值低于MSS组EC。本研究中两种序列联合评估EC MSI状态的效能较R2*值、T2*值、T2值评估EC MSI状态的效能有明显的提升,但是mDixon-Quant与T2 mapping序列各参数间无相关性,提示两种成像序列从不同的角度反映肿瘤的微环境及功能信息,其评估EC MSI状态的作用互相不可代替。

3.4 局限性

       本研究存在一定局限性:(1)病例数较少,有待增加样本量进行更深入的分析,提高统计分析结果的可靠性;(2)研究中选择了肿瘤最大层面来进行数据测量,而没有测量肿瘤全域,这种测量方法可能丢失部分肿瘤的异质性信息,有待于今后进行纹理分析、影像组学等肿瘤全域相关研究;(3)虽然mDixon-Quant序列和T2 mapping序列都是轴位图像,且ROI放置时均选择了两种序列的肿瘤最大层面,但两序列扫描层厚和层间隔不同,ROI放置未能完全匹配,可能导致测量结果存在一定偏差。

       综上所述,T2 mapping联合mDixon-Quant可定量评估EC MSI状态,两者联合可提升预测的效能,mDixon-Quant与T2 mapping序列各参数间无相关性,其评估EC MSI状态的作用互相不可代替,具有很好的临床应用前景。

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