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临床研究
MR集成序列在皮肌炎/多发性肌炎诊断及其活动性定量评估中的应用
王玉琪 田兆荣 张莉萍 田博 倪亚博 王志军

WANG Y Q, TIAN Z R, ZHANG L P, et al. Application of magnetic resonance image compilation in the diagnosis of dermatomyositis/polymyositis and quantitative assessment of activity[J]. Chin J Magn Reson Imaging, 2023, 14(9): 92-96, 99.引用本文:王玉琪, 田兆荣, 张莉萍, 等. MR集成序列在皮肌炎/多发性肌炎诊断及其活动性定量评估中的应用[J]. 磁共振成像, 2023, 14(9): 92-96, 99. DOI:10.12015/issn.1674-8034.2023.09.016.


[摘要] 目的 探讨MR集成(magnetic resonance image compilation, MAGiC)序列的定量参数对皮肌炎(dermatomyositis, DM)/多发性肌炎(polymyositis, PM)活动性的诊断价值,分析定量参数与临床指标的相关性。材料与方法 回顾性收集宁夏医科大学总医院68例经临床及病理证实为DM/PM患者的影像资料及临床资料,并根据肌电图及肌炎疾病活动性评价工具分为活动组(28例)及非活动组(40例)。另收集年龄、性别及体质量指数(body mass index, BMI)与病例组相匹配的正常志愿者24例。采用SIGNA Architect 3.0 T MRI扫描仪对所有受试者行双大腿轴位MAGiC序列及常规T1WI、T2WI、T2Flex序列扫描。由两名放射科医生于MAGiC序列上分别测量两次大腿三个肌群的T2值及T1值,采用单因素方差分析或Kruskal-Wallis H检验比较不同组T2值及T1值的差异。绘制受试者工作特征(receiver operating characteristic, ROC)曲线并计算曲线下面积(area under the curve, AUC)分析T2值对DM及其活动性的诊断效能。采用Spearman相关性分析DM/PM患者定量参数与肌酸激酶(creatine kinase, CK)值的相关性。结果 (1)DM/PM活动组中前外侧肌群、内侧肌群及后侧肌群肌肉的T2值均分别高于非活动组、对照组相应三组肌群肌肉的T2值(F值分别为48.17、94.60、79.11,P均<0.05)。活动组前外侧肌群的T1值高于非活动组的T1值,高于对照组的T1值(F=16.13,P<0.05);内侧肌群及后侧肌群差异无统计学意义(P>0.05)。(2)病例组与对照组三组肌群T2值的AUC为0.939;约登指数、敏感度和特异度分别为0.726、81.5%、91.0%。活动期与非活动期肌肉T2值的AUC为0.722,约登指数、敏感度和特异度分别为0.389、57.1%和81.8%。(3)后侧肌群的T2值与CK呈显著正相关(r=0.48,P<0.05)。结论 MAGiC定量图谱技术的T2值能定量分析DM/PM患者的肌肉受累情况,与临床指标CK高度相关。
[Abstract] Objective To investigate the quantitative parameters of MR compilation on dermatomyositis (DM) / polymyositis (PM) the diagnostic value of activity, and the correlation between quantitative parameters and clinical indicators was analyzed.Materials and Methods The imaging data and clinical data of 68 patients with DM/PM confirmed by clinical and pathological methods in General Hospital of Ningxia Medical University were retrospectively collected, and the case group was divided into an active group (28 cases) and an inactive group (40 cases) according to the electromyogram and myositis disease activity tool. Another 24 normal volunteers matching the age, gender and body mass index (BMI) of the case group were also collected. SIGNA Architect 3.0 T MRI scanner was used to perform MAGiC sequence and conventional T1WI, T2WI and T2Flex sequence scanning on both thighs. The T2 and T1 values of the three thigh muscle groups were measured twice by two radiologists on the MAGiC sequence. One-way analysis of variance or Kruskal-Wallis H-test was used to compare the T2 and T1 values of different groups. Receiver operating characteristic (ROC) curves were plotted and the area under the curve (AUC) was calculated to analyze the diagnostic efficacy of T2 values for DM and its activity. Spearman correlation was used to analyze the correlation between DM/PM quantitative parameters and creatine kinase (CK) value.Results (1) The T2 values of anterolateral, medial and posterior muscles in DM/PM active group were higher than those in inactive group and control group (F values were 48.17, 94.60, 79.11, P<0.05). The T1 value of the active group was higher than that of the inactive group and higher than that of the control group (F=16.13, P<0.05). There was no significant difference between medial muscle group and posterior muscle group (P>0.05). (2) The AUC value of T2 value of muscle groups in case group and control group was 0.939; the Youden index, sensitivity and specificity were 0.726, 81.5% and 91.0%, respectively. The AUC value of active and inactive muscle T2 values was 0.722, and the Youden index, sensitivity and specificity were 0.389, 57.1% and 81.8%, respectively. (3) The T2 value of the posterior muscle group was significantly positively correlated with CK (r=0.48, P<0.05).Conclusions T2 value of MAGiC quantitative mapping technique can quantitatively analyze muscle involvement in DM/PM patients, which is highly correlated with clinical indicators of CK.
[关键词] 皮肌炎/多发性肌炎;磁共振成像;影像指标;临床指标;活动性
[Keywords] dermatomyositis/polymyositis;magnetic resonance imaging;image index;clinical index;activity

王玉琪 1   田兆荣 2   张莉萍 2   田博 2   倪亚博 1   王志军 2*  

1 宁夏医科大学临床医学院,银川 750001

2 宁夏医科大学总医院放射科,银川 750001

通信作者:王志军,E-mail:wangzhijun2056@163.com

作者贡献声明:王志军设计本研究的方案,对稿件重要内容进行了修改;王玉琪起草和撰写稿件,获取、分析或解释本研究的数据;田兆荣、张莉萍、田博、倪亚博获取、分析或解释本研究的数据,对稿件重要内容进行了修改;田兆荣获得了宁夏回族自治区重点研发计划基金项目资助;全体作者都同意发表最后的修改稿,同意对本研究的所有方面负责,确保本研究的准确性和诚信。


基金项目: 宁夏回族自治区重点研发计划 2021BEG03033,2023BEG03003
收稿日期:2023-04-06
接受日期:2023-08-04
中图分类号:R445.2  R593.26 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.09.016
引用本文:王玉琪, 田兆荣, 张莉萍, 等. MR集成序列在皮肌炎/多发性肌炎诊断及其活动性定量评估中的应用[J]. 磁共振成像, 2023, 14(9): 92-96, 99. DOI:10.12015/issn.1674-8034.2023.09.016.

0 前言

       特发性炎性肌病(idiopathic inflammatory myopathies, IIM)是一组以自身免疫介导的骨骼肌慢性炎性疾病,以对称性进行性肌无力为特征[1],全球每年每百万人中有5~10例新发病例[2],女性较男性多发。其中,以皮肌炎(dermatomyositis, DM)/多发性肌炎(polymyositis, PM)最为常见,并且DM/PM具有极高的致残率和复发率[3, 4, 5],尤其是活动期的患者常有近端肌无力、肌压痛的表现,若不及时治疗将会出现呼吸困难及心脏损害的后果,给患者造成功能限制、残疾和生活质量下降的严重危害[6]。因此,如何尽早精准地判断活动期,对于患者治疗及预后至关重要。目前对于DM/PM活动期的诊断,肌电图及肌肉活检为“金标准”,由于股四头肌活检易操作,常作为首选部位。但是,临床工作中由于患者个体性差异,病变也可位于其他肌肉,或者某些肌肉改变以散在形式,斑片状分布在各个肌肉,导致活检结果出现假阳性,假阳性率为10%~30%[7],并且两者均为有创检查,重复性较低,影响诊断和治疗[8, 9, 10]

       MRI检查作为研究肌病患者疾病状态的重要非侵入性工具,2017年被欧洲抗风湿病联盟(European League Against Rheumatism, EULAR)和美国风湿病学会(American College of Rheumatology, ACR)纳入到DM/PM的诊断标准[7]。MRI具有软组织分辨率高、多参数、多序列的优势,可以清晰地显示双大腿解剖结构、肌肉病理改变和程度,已有研究证明MRI检查对DM/PM诊断具有很高的临床价值[11, 12, 13, 14]。而常规MRI检查仅凭主观判断信号高低定性病变,缺乏量化方法[15]。近年来新出现的MR集成(magnetic resonance image compilation, MAGiC)序列是一种新型的定量技术,可以经过一次扫描调整重复时间(repetition time, TR)及回波时间(echo time, TE)重建出不同的对比图像和定量图像,如T1 mapping、T2 mapping、PD mapping等,获得特定的弛豫值(T1、T2、PD、R1及R2值)可定量分析损伤组织中各种成分含量改变,对组织成分进行定量评估[16],从分子影像学的角度可视化炎性肌病的活动性。目前,MAGiC序列较多应用于前列腺、乳房、宫颈、直肠和脊柱方面[17, 18, 19, 20, 21, 22, 23],但目前很少有MAGiC技术在DM/PM中应用及对其活动性定量诊断的相关报道,RAN等[24]的研究反映T2值与受影响肌肉有关,T2值与激酶CK缺乏统计学上的相关性,但由于病例量较少,缺乏一定客观性。因此,本研究旨在探讨MAGiC序列对DM/PM的诊断价值及对其活动性的定量评估,并分析定量参数与临床指标的相关性。

1 材料与方法

1.1 研究对象

       回顾性分析宁夏医科大学总医院经临床及病理证实为DM/PM并接受双大腿MRI检查的患者病例68例(病例组),纳入标准:(1)经临床判断或病理确诊为DM/PM;(2)根据肌电图及肌炎疾病活动性评价工具[25],确定疾病处于活动期或非活动期(将病例组分为活动组和非活动组2个亚组);(3)年龄18~75岁;(4)患者有完整的影像学及临床信息资料。排除标准:(1)患者合并系统性红斑狼疮等其他免疫疾病;(2)合并有严重的高血压、糖尿病等慢性病。同时选择本院同期进行常规T1WI、T2WI、T2Flex序列及MAGiC序列扫描的年龄、性别及体质量指数(body mass index, BMI)与病例组相匹配的正常志愿者(对照组),纳入标准:(1)年龄在18~75岁之间;(2)无其他免疫系统疾病。本研究遵守《赫尔辛基宣言》,通过宁夏医科大学总医院伦理委员会批准,免除受试者知情同意,批准文号:2020-657。

1.2 临床资料

       收集受试者一般资料:性别(男/女)、年龄(岁)、BMI(kg/m2)、病程(月)、皮肤表现(Gottron征、斑丘疹)、全身症状(发热、乏力、体质量减轻);实验室资料:血清肌酶学[肌酸激酶(creatine kinase, CK)、乳酸脱氢酶(lactate dehydrogenase, LDH)、丙氨酸氨基转移酶(alanine aminotransferase, ALT)、天冬氨酸氨基转移酶(aspartate aminotransferase, AST)]、白细胞介素IL-6、抗体(抗MDA5IgG、抗RO-52IgG、抗Jo-1)。

1.3 检查方法

       采用SIGNA Architect 3.0 T MRI扫描仪,行双大腿常规T1WI、T2WI、T2Flex序列及MAGiC序列扫描,患者取仰卧位,16通道躯干线圈覆盖双腿,双手放置于身侧。扫描范围:自髂前上棘至腘窝水平。扫描参数如下:(1)常规轴位T1WI序列,TR 637 ms,TE 20 ms,矩阵320×256,视野380 mm×380 mm,层厚7 mm,层间隔1 mm,扫描时间51 s;(2)轴位T2WI序列,TR 3000 ms,TE 63 ms,矩阵320×256,视野380 mm×380 mm,层厚7 mm,层间隔1 mm,扫描时间1 min 3 s;(3)轴位T2 Flex序列,TR 3000 ms,TE 85 ms,矩阵320×256,视野380 mm×380 mm,层厚7 mm,层间隔1 mm,扫描时间3 min;(4)轴位MAGiC序列,TR 4000 ms,TE 13.2 ms,矩阵320×256;视野380 mm×380 mm,层厚7 mm,层间隔1 mm,扫描时间4 min 32 s。

1.4 图像后处理

       扫描完成后由2名具有10年以上骨肌系统疾病诊断经验的放射科主治医师,采用双盲法独立阅片,利用主机MAGiC软件包进行图像后处理,生成T1 mapping、T2 mapping两组定量图谱。在生成的图像上测量大腿肌肉T1、T2值,在MAGiC序列生成的T2WI轴位图像上将双大腿肌肉分为大腿前外侧肌群(阔筋膜张肌、缝匠肌、股四头肌),内侧肌群(大收肌、长收肌、股薄肌)及后侧肌群(半膜肌、半腱肌、股二头肌)。手工绘制ROI,测量12块肌肉的T1值、T2值,绘制ROI时应沿着肌肉边缘,避开皮下脂肪、筋膜及其他组织(图1)。ROI的绘制及测量分别由上述2名放射科医师独立完成,分别测量两次,最终分析数据为2名医师4次测量结果的平均值。

图1  大腿绘制ROI示意图。
Fig. 1  Thigh drawing region of interest.

1.5 统计学分析

       采用SPSS 21.0对所有数据进行统计分析,利用Kolmogorov-Smirnov检验对所有计量资料进行正态性检验,符合正态分布的数据用(x¯±s)表示,不符合正态分布的用MQ1,Q3)表示。以组内相关系数(intra-class correlation coefficient, ICC)评估观察者间和观察者内测量T1和T2值的可重复性,ICC>0.75表明一致性良好。采用单因素方差分析或Kruskal-Wallis H检验比较不同组T2及T1值差异,对差异有统计学意义的参数绘制受试者工作特征(receiver operating characteristic, ROC)曲线,评估大腿肌肉T1、T2值诊断效能。采用Spearman和Pearson相关性分析评估DM/PM患者大腿肌肉的平均T2值与血清CK之间的相关性。P<0.05为差异有统计学意义。

2 结果

2.1 一般资料

       纳入病例组68例,其中男24例,女44例,年龄20.0~74.0(47.9±15.0)岁,CK值20.00~6227.20(927.99±1973.71)U/L;对照组24例,其中男10例,女14例,年龄20.0~65.0(49.1±17.0)岁,CK值26.40~827.80(287.49±312.25)U/L。两组间的年龄、性别、BMI差异无统计学意义(P>0.05)(表1)。

表1  一般资料比较
Tab. 1  General data comparison

2.2 观察者的一致性

       两位观察者两次测量大腿肌肉三组肌群T1、T2值一致性分析发现,前外侧肌群的ICC值较高,其次是后侧肌群,最后是内侧肌群,所有ICC值均>0.75,P均<0.001。

2.3 病例组与对照组定量参数值比较

       DM/PM患者活动组的前外侧肌群、内侧肌群及后侧肌群T2值均分别高于非活动组、对照组相应三组肌群的T2值(F值分别为48.17、94.60、79.11),差异有统计学意义(P<0.05);DM/PM患者活动组的前外侧肌群的T1值高于非活动组、对照组(F为16.13),差异有统计学意义(P<0.05);DM/PM患者活动组的内侧肌群及后侧肌群T1值与非活动组及对照组T1值(F值分别为17.45、6.99),差异无统计学意义(P>0.05)(表2图2)。

图2  大腿各肌肉活动期磁共振集成序列定量参数T2值柱状图。
Fig. 2  Histogram of T2 values of quantitative parameters of magnetic resonance image compilation sequence of thigh muscles.
表2  病例组与对照组MRI定量参数比较
Tab. 2  Comparison of quantitative MRI parameters between case group and control group

2.4 MAGiC序列定量参数对DM/PM的诊断价值

       病例组大腿肌肉T2值的ROC曲线诊断价值较高,AUC为0.939,约登指数、敏感度和特异度分别为0.726、81.5%、91.0%,差异有统计学意义(P<0.05)(图3)。T1值诊断DM/PM的AUC差异无统计学意义(P>0.05)。

图3  MRI定量参数T2值对皮肌炎/多发性肌炎及其活动性的诊断ROC曲线。
图4  后组肌群MRI定量参数T2值与肌酸激酶(CK)的相关性分析散点图。
Fig. 3  Diagnostic ROC curve of dermatomyositis/polymyositis and its activity induced by T2 value of MRI quantitative parameter.
Fig. 4  Scatter plot of correlation between T2 value of quantitative parameter of hemiembrane MRI and creatine kinase.

2.5 MAGiC序列定量参数对DM/PM活动性的诊断效能

       活动组大腿肌肉T2值的ROC曲线诊断价值中等,AUC为0.722,约登指数、敏感度和特异度分别为0.389、57.1%和81.8%,差异有统计学意义(P<0.05)(图3)。T1值诊断DM/PM活动期的AUC差异无统计学意义(P>0.05)。

2.6 MAGiC序列定量参数与临床指标的相关性

       经Spearman相关性分析发现,活动组与非活动组大腿肌肉的T2值与CK呈正相关(图4),相关系数为0.48(P<0.05)。

3 讨论

       DM/PM活动期作为病理演变中的重要过程,早期诊断不仅有利于治疗,减少激素造成的骨损伤,还能减少呼吸困难及心脏损害导致的死亡[26]。MAGiC序列为通过一次扫描重建多组定量图像进而实现疾病定量诊断的新技术,近年来成为国内外的研究热点,本研究参照RAN等[24]的研究方法,观察CK和LDH标志物变化,在国内首次测量DM/PM活动期患者MAGiC序列中大腿肌肉的T1、T2值,并与临床指标相结合,结果发现活动组T2值明显高于非活动组及对照组,对DM/PM及其活动性具有较高的诊断价值,并且T2值与CK存在较高相关性,因此可作为反映DM/PM活动期的有效量化参数。

3.1 DM/PM患者大腿肌肉定量参数变化的原因分析

       本研究结果显示,DM/PM患者大腿肌肉水肿程度具有显著的分布特征,病例组大腿前外侧肌群的T2值显著高于后组肌群及内组肌群,前外侧肌群肌肉水肿最严重,与ZHENG等[27]研究结果相同。这可能是因为前外侧肌群为股四头肌,是人体最大、最有力的肌肉之一,其肌纤维除了股中间肌平行排列外,其余三块均为羽状排列,羽状肌的特点为肌纤维排列像羽毛的走向,斜向走行汇聚于肌腹中央的肌腱,肌纤维排列密度大,其收缩的力量大于平行肌,肌肉内部产生的乳酸菌堆积量大于平行肌,更易导致炎细胞浸润肌束膜,细胞间液增多,形成水肿[28],此时,T2弛豫时间延长,T2值增高,这种弛豫时间的差异反映了T2值对水含量非常敏感;另一方面与外侧肌群的股四头肌走行及工作机制有关,股直肌起自髂前下棘,股中肌起自股骨体前面,股外侧肌起自股骨粗线外侧唇,股内侧肌起自股骨粗线内侧唇,四块肌肉联合在一起产生肌力,并作为一个整体通过髌腱及髌韧带附着在胫骨粗隆上,其主要生理作用为控制髋关节和膝关节的屈伸[29, 30],在跑步、跨步等活动中会受到较大的压力。当外侧肌群承受过大的压力时,会导致外侧肌群神经组织受损,从而引起水肿。此外,与股四头肌其他部分不同,外侧肌群很少有交叉支配,这也可能是其易受损的原因之一。因此DM/PM活动期以外侧肌群受累最为明显。

3.2 MAGiC序列定量参数对DM/PM及活动性的诊断价值

       MAGiC序列中的T2 mapping,是一种能定量分析损伤组织中各种成分含量改变的MRI新技术,其工作原理为多回波自旋回波序列,信号经过工作站处理,形成伪彩图,通过测量ROI的T2值,对组织成分进行定量评估[31],反映骨骼肌的炎症细胞浸润,并检测肌肉水肿的程度,用于测量与生理或病理大分子环境变化相关的水结合改变[32]。本研究证明,DM/PM患者活动期、非活动期和对照组肌肉的T2值存在显著性差异。患者MAGiC序列T2值的ROC曲线显示,T2值可实现对DM/PM及其活动性的诊断,具有较高的诊断价值,与RAN等[33]的研究结果类似,而T1值差异无统计学意义,表明T1值在反应组织水肿方面可能不如T2值敏感。水肿与DM/PM患者的疾病活动期相关[34, 35],其经典病例的组织病理学表现为伴有表皮萎缩的细微空泡界面改变、轻度毛细血管扩张和血管周围淋巴细胞稀疏充盈,这种病理状态可能会增加肌膜的通透性,导致细胞内自由水增加。肌肉组织自由水含量增加对T2弛豫时间有明显的影响,毛细血管扩张和血管水肿的严重程度反映了DM/PM的活动性,T2值对液体异常敏感,而T1值常用于观察解剖结构,所以在DM/PM活动期时T2值明显升高。综上,通过MAGiC序列定量图谱T2 mapping能够实现对DM/PM患者活动期的诊断,尤其是T2值可以作为DM/PM炎性诊断及肌肉活动期的影像学标志物,对其早期治疗及用药预后有一定的辅助价值。

3.3 MAGiC序列定量参数与临床指标的相关性

       本研究显示,DM/PM患者的CK值与大腿肌肉T2值之间在统计学上存在一定的正相关。血清CK催化肌酸转化为磷酸肌酸,血清CK水平升高被认为是标志肌肉损伤的实验室指标。由于炎性细胞浸润以肌内膜为主,血清CK升高水平与肌细胞破坏程度一致,肌细胞破坏明显,CK释放入血,导致CK显著升高[36]。T2值反映肌肉炎性细胞浸润导致的水肿程度,因此,T2值与血清CK存在相关性。临床上,由于肌损伤酶的相对特异性,CK是DM/PM患者建立诊断和预后的主要生物标志物,且有较高的敏感度,经常被用来检测疾病进展和对治疗的反应,但实验室标准值存在差异、假阳性率高、特异性低等的缺点,而MRI检查具有一次扫描可全面分析肌肉水肿程度及病情演变、可提供更多定量参数、精准分析评估疾病活动性的优势,MAGiC序列中的定量参数T2值能直观精准评估DM/PM肌肉的水肿程度,不受外界环境的影响。因此,T2值可作为检测DM/PM疾病活动期的影像学标志物。

3.4 本研究的局限性

       本研究存在一定的局限性:(1)样本量较少,未来可纳入更多活动期DM病例进行大样本量DM活动期的进一步研究;(2)未对MAGiC序列中的其他定量图谱进行研究,后期将会逐一研究分析,以验证MAGiC定量图谱技术作为治疗检测工具的有效性。

4 结论

       综上所述,MAGiC序列的T2值是反映DM/PM及其活动期的有效的量化参数,能够为临床对DM/PM的诊断提供量化的客观依据。

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