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临床研究
IDEAL-IQ序列在冈上肌腱损伤后肩袖肌群脂肪浸润定量评估中的应用
徐奋玲 田兆荣 田博 龚瑞 马芳芳 胡靖波 王志军

Cite this article as: XU F L, TIAN Z R, TIAN B, et al. Application of the IDEAL-IQ sequence in the quantitative evaluation of fat infiltration in the rotator cuff muscle group after supraspinatus tendon injury[J]. Chin J Magn Reson Imaging, 2024, 15(10): 115-122.本文引用格式:徐奋玲, 田兆荣, 田博, 等. IDEAL-IQ序列在冈上肌腱损伤后肩袖肌群脂肪浸润定量评估中的应用[J]. 磁共振成像, 2024, 15(10): 115-122. DOI:10.12015/issn.1674-8034.2024.10.020.


[摘要] 目的 采用非对称采集与迭代最小二乘估算法迭代水脂分离(iteraterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation, IDEAL-IQ)方法定量评估冈上肌腱损伤的严重程度与肩袖肌群脂肪浸润程度及受试者特征之间的关系。材料与方法 回顾性分析2022年8月至2024年6月本院经肩关节镜证实的33例冈上肌腱部分撕裂患者及89例完全撕裂患者,均进行了常规MRI扫描及IDEAL-IQ序列扫描。由两名放射科医生分别对所有受试者的MRI图像进行独立评估,根据常规MRI图像的冈上肌腱损伤表现,将完全撕裂组的冈上肌腱按照Patte分型分为Patte 1型(Ⅱ级)、Patte 2型(Ⅲ级)、Patte 3型(Ⅳ级),将部分撕裂组定义为Ⅰ级。同时在斜矢状位上进行Goutallier分级及Thomazeau萎缩分级,并通过GE ADW 4.7工作站后处理软件在IDEAL-IQ序列生成的脂肪分数图像上测量冈上肌、冈下肌、肩胛下肌及小圆肌脂肪分数(fat fraction, FF)。用组内相关系数(intra-class correlation coefficient, ICC)及Kappa一致性检验评估观察者间及观察者内的一致性。采用Kruskal-Wallis H检验、单因素ANOVA检验分析FF值在不同分组之间的差异,组间两两比较用Bonferroni检验。采用Pearson相关性分析肩袖肌肉FF值与年龄、症状持续时间的相关性(相关系数r),Spearman相关性分析冈上肌腱损伤分级与肩袖肌群FF值、Goutallier分级及Thomazeau萎缩分级之间的相关性(相关系数rs)。结果 (1)冈上肌、冈下肌、肩胛下肌的FF值在冈上肌腱损伤Ⅳ级中显著高于Ⅲ级,高于Ⅱ级和Ⅰ级,差异有统计学意义(P值分别为<0.001、<0.001、0.005);小圆肌的FF值在不同分级之间差异无统计学意义(P=0.073)。组内比较Ⅰ级和Ⅱ级的冈上肌、冈下肌、肩胛下肌、小圆肌FF值差异无统计学意义(P值分别为0.026、0.102);Ⅲ级和Ⅳ级的FF值差异有统计学意义(P<0.001)。(2)冈上肌、冈下肌、小圆肌的FF值与年龄呈中等相关(r值分别为0.381、0.339、0.349,P均<0.001),肩胛下肌的FF值与年龄呈弱相关(r=0.216,P=0.017);冈上肌、冈下肌、肩胛下肌FF值与症状持续时间呈中等程度相关(r分别为0.442、0.412、0.314,P均<0.001),小圆肌的FF值与症状持续时间呈弱相关(r=0.277,P=0.002);冈上肌腱损伤程度与冈上肌FF值呈显著相关(rs=0.740,P<0.001),与冈下肌的FF值呈强相关性(rs=0.596,P<0.001),与肩胛下肌、小圆肌的FF值呈弱相关(rs分别为0.257、0.212,P值分别为0.004、0.019);冈上肌损伤程度分级与Goutallier分级、Thomazeau分级之间呈显著正相关(rs分别为0.757、0.737,P均<0.001),且冈上肌FF值在Goutallier和Thomazeau的分级中差异具有统计学意义(P均<0.001)。结论 3.0 T MR IDEAL-IQ序列能量化和客观评估肩袖肌群脂肪浸润程度,肩袖肌群脂肪浸润程度与冈上肌腱损伤分级呈正相关,与年龄、症状持续时间呈正相关。
[Abstract] Objective The study utilized the iteraterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation (IDEAL-IQ) method to quantitatively evaluate the relationship between the severity of supraspinatus tendon injuries and the degree of fat infiltration of the rotator cuff muscle group and subject characteristics.Materials and Methods A retrospective collection of 33 patients with partial supraspinatus tendon tears and 89 patients with complete tears confirmed by shoulder arthroscopy in our hospital from August 2022 to June 2024 was conducted. Conventional MRI and IDEAL-IQ sequence scans were performed. Two radiologists independently evaluated the MRI images of all subjects. Based on the supraspinatus tendon injury performance on conventional MRI images, the supraspinatus tendon in the fully tear group was divided into Patte 1 (Grade Ⅱ), Patte 2 (Grade Ⅲ), and Patte 3 (Grade Ⅳ) according to the Patte classification. The partial tear group was defined as Grade I. At the same time, the Goutallier score and Thomazeau atrophy grading were performed on the oblique sagittal plane. Fat fraction (FF) of supraspinatus muscle, infraspinatus muscle, subscapularis muscle and teres minor muscle were measured on the fat fraction image generated by IDEAL-IQ sequence using GE ADW 4.7 workstation post-processing software. Intra-observer and intra-observer consistency were evaluated by intra-class correlation coefficient (ICC) and Kappa consistency test. Kruskal-Wallis H test and One-Way ANOVA test were used to analyze the differences of FF values among different groups, and Bonferroni test was utilized for pairwise comparison between groups. Pearson correlation was used to analyze the correlation between rotator cuff muscle FF value and age and duration of symptoms (the correlation coefficient is r). Spearman correlation was used to analyze the correlation between supraspinatus tendon injury grade and rotator cuff muscle FF value, Goutallier grade and Thomazeau atrophy grade (the correlation coefficient is rs).Results (1) The FF values of the supraspinatus muscle, infraspinatus muscle, and subscapular muscle were significantly higher in Grade Ⅳ than those of the same muscles in Grade Ⅲ, Grade Ⅱ and Grade Ⅰ, with statistical significance (P<0.001, <0.001, 0.005, respectively). There was no significant difference in the FF value of the teres minor muscle among different grades (P=0.073). Results of intra-group comparision suggested that there was no significant difference in the FF values of the supraspinatus muscle, infraspinatus muscle, subscapularis muscle, and teres minor between Grade Ⅰ and Grade Ⅱ (P=0.026, 0.102). There was a significant difference in the FF value between Grade Ⅲ and Grade Ⅳ (P<0.001). (2) The FF values of supraspinatus, infraspinatus, subscapularis and teres minor were moderately correlated with age (with r values of 0.381, 0.339, 0.349, respectively, all P<0.001), while FF values of subscapular muscle were weakly correlated with age (r=0.216, P=0.017). The FF values of supraspinatus, infraspinatus, subscapularis were moderately correlated with the duration of symptoms(with r values of 0.442, 0.412, 0.314, respectively, all P<0.001), while FF values of teres minor were weakly correlated with symptom duration (r=0.277, P=0.002). The degree of injury of the supraspinatus tendon was significantly correlated with the FF value of the supraspinatus muscle (rs=0.740, P<0.001), was strongly correlated with the FF value of the infraspinatus muscle (rs=0.596, P<0.001), and was weakly correlated with the FF values of the subscapularis muscle and the teres minor muscle (with rs value of 0.257, 0.212, P=0.004, 0.019). There was a positive correlation between the degree of supraspinatus injury grade and Goutallier grade and Thomazeau grade (with rs value of 0.757, 0.737, all P<0.001). The FF value of supraspinatus muscle was significantly different in Goutallier grade and Thomazeau grade (all P<0.001).Conclusions 3.0 T MR IDEAL-IQ sequence could objectively assessed the degree of rotator cuff injury, and the quantified FF was positively correlated with supraspinatus injury grade, and associated with age and duration of symptoms.
[关键词] 冈上肌腱;Patte分型;Goutallier分级;肩袖肌群;脂肪定量;IDEAL-IQ;脂肪分数;磁共振成像
[Keywords] supraspinatus;Patte classification;Goutallier grade;rotator cuff muscles;fat quantification;IDEAL-IQ;fat fraction;magnetic resonance imaging

徐奋玲 1   田兆荣 2   田博 2   龚瑞 2   马芳芳 1   胡靖波 1   王志军 2*  

1 宁夏医科大学第一临床医学院,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;徐奋玲起草和撰写稿件,获取、分析和解释本研究的数据;田兆荣、田博、龚瑞、马芳芳、胡靖波获取、分析或解释本研究的数据,对稿件重要内容进行了修改;王志军、田兆荣获得了宁夏回族自治区重点研发计划项目基金资助;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项目 2021BEG03033 宁夏回族自治区重点研发计划项目 2023BEG03003
收稿日期:2024-04-16
接受日期:2024-09-10
中图分类号:R445.2  R686 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2024.10.020
本文引用格式:徐奋玲, 田兆荣, 田博, 等. IDEAL-IQ序列在冈上肌腱损伤后肩袖肌群脂肪浸润定量评估中的应用[J]. 磁共振成像, 2024, 15(10): 115-122. DOI:10.12015/issn.1674-8034.2024.10.020.

0 引言

       肩袖由冈上肌、冈下肌、肩胛下肌以及小圆肌组成,相互作用成为肱骨头的主要动态稳定器。任何不对称的张力均会导致盂肱关节剪切力的改变,使肱骨头从关节盂旋转中心移位,从而导致其他拮抗肌无力和萎缩[1]。冈上肌作为肩部力量集中的交叉点,因其独特的解剖结构特点以及承受的机械应力使其成为肩袖中最易损伤的肌腱,约占肩袖损伤的85%以上[2]。常因撕裂而改变肩袖内部固有的力偶平衡,严重影响肩关节稳定性,从而导致周围其他组织变性。有研究表明肌腱撕裂晚期肌肉会出现脂肪浸润和萎缩,导致肌腱修复后再撕裂的概率明显增加。另外,临床普遍认为年龄、性别、肥胖等非损伤因素也与脂肪浸润密切相关,认为其会影响肌肉形态和质量,并有研究观察到与年龄相关的肌肉力量下降,随着年龄的增长,异位脂肪组织会浸润萎缩的骨骼肌[3]。而且肩袖撕裂大小、年龄、病程等诸多因素均能对肩袖损伤患者的预后造成负面影响。因此,术前对肌肉脂肪浸润程度的准确评估成为了临床关注热点。目前对肩袖肌肉脂肪变性程度的报道多为半定量Goutallier分级,以及定量磁共振波谱、T1 mapping及T2 mapping成像等[4, 5]。半定量Goutallier分级是术前评价肩袖肌肉质量最常用的方法,最初用于在CT上对肩袖肌肉的脂肪变性进行分级,从0级(肌肉内无脂肪)到4级(肌肉内超过50%的脂肪)的5个不同等级。这种类似的分级方法目前被广泛应用于MRI图像,通过常规的T1WI图像进行视觉评估,较为快速和便捷,但其具有较强的主观性[6],多依赖于观察者的经验,重复性差。其他众多定量分析所采用的测量方法及成像技术各不相同,缺乏统一标准,因此得到的研究结果亦不尽相同,且部分技术对扫描条件及扫描时长也具有较高的要求[7]

       IDEAL-IQ作为近年来兴起的脂肪定量技术,单次扫描即可生成水像、脂像、同相位及反相位、脂肪分数(Fat Fraction, FF)图及R2*图6种不同对比度的图像,优化了脂-水分离并且大大缩短扫描时间[8]。目前IDEAL-IQ多用于评估脂肪肝、骨质疏松及椎旁肌肉脂肪含量[9, 10],也有研究用于预测肌肉脂肪变性对肌腱修复后再撕裂概率的影响[11],以及肌腱炎、部分撕裂、完全撕裂时肩袖肌群脂肪浸润程度,但并未有文献针对冈上肌腱完全撕裂不同回缩程度下的肩袖肌群脂肪含量变化进行评估。故本研究通过磁共振IDEAL-IQ技术定量评估肩袖肌肉群脂肪浸润程度,并探讨其与受试者冈上肌肌腱损伤程度分级、年龄、症状持续时间以及冈上肌萎缩程度及半定量脂肪浸润分级之间的关系,以期为临床诊疗及预后提供客观参考依据。

图1  IDEAL-IQ序列脂肪分数图。1A:IDEAL-IQ序列脂肪分数图;1B:IDEAL-IQ序列脂肪分数伪彩图。
图2  冈上肌损伤程度分级。2A:冈上肌腱部分撕裂;2B:冈上肌完全撕裂并回缩,残端靠近肱骨大结节肌腱附着处(Patte 1);2C:冈上肌完全撕裂并回缩,残端位于肱骨头顶端与关节盂水平之间(Patte 2);2D:冈上肌完全撕裂并回缩,残端位于关节盂水平内侧(Patte 3)。
图3  利用肩关节斜矢状位T1WI序列行冈上肌脂肪浸润评估(Goutallier分级)。3A:冈上肌脂肪浸润0级,脂肪含量=0;3B:冈上肌脂肪浸润1级,肌肉内可见少许线状、条纹状脂肪信号;3C:冈上肌脂肪浸润2级,肉内少量羽毛状脂肪信号;3D:冈上肌脂肪浸润3级,脂肪信号与肌肉信号基本等量;3E:冈上肌脂肪浸润4级,脂肪信号多于肌肉信号。
图4  Thomazeau萎缩分级,肩关节斜矢状位图像上肩胛骨的结构显示为“Y”字形时,冈上肌横截面与冈上窝横截面占位比。蓝线代表冈上肌横截面,黄线代表冈上窝横截面。IDEAL-IQ:非对称采集与迭代最小二乘估算法迭代水脂分离。
Fig. 1  Fat fraction image of the IDEAL-IQ sequence. 1A: The map of fat fraction of IDEAL-IQ sequence; 1B: The pseudo-color map of fat fraction of IDEAL-IQ sequence.
Fig. 2  Degree grade of supraspinatus injury. 2A: The supraspinatus tendon is partially tear; 2B: Supraspinatus muscle is completely tear and retracted, and the stump is close to the attachment of the greater tuberosity of the humerus (Patte 1); 2C: The supraspinatus is completely tear and retracted, and the stump is located between the top of the humeral head and the level of the glenoid (Patte 2); 2D:The supraspinatus is completely tear and retracted, and the stump is located medial to the level of the glenoid (Patte 3).
Fig. 3  Fat infiltration of the supraspinatus muscle is assessed using the T1WI sequence in the oblique sagittal position of the shoulder. 3A: Fat infiltration of the supraspinatus muscle is Grade 0; 3B: Fat infiltration of the supraspinatus muscle is Grade 1, a few linear and stripe-like fat signals can be seen in the muscle; 3C: Fat infiltration of the supraspinatus muscle is Grade 2, a small amount of feather-like fat signal in the muscle; 3D: Fat infiltration of the supraspinatus muscle is Grade 3, fat signal basically the same amount as muscle signal; 3E: Fat infiltration of the supraspinatus muscle is Grade 4, fat signal is more than muscle signal.
Fig. 4  Thomazeau atrophy classification, when the structure of the scapula appears as a “Y” shape on the oblique sagittal image of the shoulder joint, the ratio of the cross-section of the supraspinatus muscle to the cross-section of the supraspinatus fossa. The blue line represents the cross-section of the supraspinatus muscle, and the yellow line represents the cross-section of the supraspinatus fossa. IDEAL-IQ:iteraterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation.
图5  不同肩袖肌肉脂肪分数(FF)在冈上肌腱损伤同一分级中的结果比较。n.s.表示该组间差异无统计学意义,*表示P<0.01;**表示P<0.001。Ⅰ级:部分撕裂;Ⅱ级:Patte分型1型;Ⅲ级:Patte分型2型;Ⅳ级:Patte分型3型。
Fig. 5  Comparison of results of different rotator cuff muscle fat fraction (FF) in the same grade of supraspinatus injury. n.s. indicates no statistical significant difference between this group. * indicates P<0.01; ** indicates P<0.001. Grade Ⅰ: Supraspinatus partial tear; Grade Ⅱ: Patte type 1; Grade Ⅲ: Patte type 2; Grade Ⅳ: Patte type 3.
图6  肩袖肌群脂肪分数(FF)值与冈上肌腱损伤分级相关性散点图。Ⅰ级:部分撕裂;Ⅱ级:Patte分型1型;Ⅲ级:Patte分型2型;Ⅳ级:Patte分型3型。
Fig. 6  Scatter plot of the correlation between rotator cuff muscle fat fraction (FF) values and supraspinatus injury grade. Grade Ⅰ: Supraspinatus partial tear; Grade Ⅱ: Patte type 1; Grade Ⅲ: Patte type 2; Grade Ⅳ: Patte type 3.

1 材料与方法

1.1 研究对象

       本研究遵循《赫尔辛基宣言》,经宁夏医科大学总医院伦理委员会批准(批准文号:2020-657),免除受试者知情同意书。回顾性收集2022年8月至2024年6月宁夏医科大学总医院肩袖撕裂患者122例。纳入标准:(1)所有冈上肌腱撕裂病例均经关节镜确诊;(2)完成所有常规MRI扫描及IDEAL-IQ序列扫描。排除标准:(1)患有风湿病、糖尿病及其他相关性系统疾病者;(2)肥胖患者[身体质量指数(body mass index, BMI)≥30 kg/m2];(3)上肢骨折及肿瘤病史。

1.2 仪器与扫描参数

       所有被检者均采用GE SIGNA Architect 3.0 T扫描仪(SIGNA™ Architect 3.0T, 美国通用电气医疗公司,芝加哥,美国)和16通道肩关节专用线圈进行检查,患者取仰卧位,头先进,患侧尽量靠近主磁场中心,肩部放松,患肢自然放置身侧,掌心朝上,使用沙袋固定线圈及肩关节以减少运动伪影。行肩关节常规轴位[T2WI脂肪抑制(fat saturation, FS)序列、T1WI序列]、斜冠状位(T2WI FS序列)、斜矢状位[质子密度加权成像(proton density weighted imaging, PDWI)FS序列、T1WI序列]和斜矢状位IDEAL-IQ序列扫描。横断位扫描层面与关节盂垂直,扫描范围从肩锁关节至关节盂下缘。冠状面扫描层面与冈上肌腱平行。矢状面扫描层面与冈上肌腱垂直,扫描范围包括肱骨头和整个冈上肌。具体扫描参数如表1所示。

表1  肩关节MRI扫描序列及相关参数
Tab.1  Shoulder MR into the scanning sequence and related parameters

1.3 图像后处理

       由两名放射科医师(分别具有5、10年以上骨肌系统诊断经验的主治、副主任医师)在掌握冈上肌腱损伤Patte分型、脂肪浸润半定量Goutallier分级以及Thomazeau萎缩分级的情况下,对所有研究对象的肩关节常规MRI独立进行评估,当两者意见不一致时,共同商量决定。并将扫描完成的IDEAL-IQ序列上传至GE ADW 4.7工作站后处理,参照以往研究[12],在斜矢状位图像上肩胛骨的结构显示为“Y”字形时,以该层面作为研究层面,根据肌肉的轮廓于IDEAL-IQ序列生成的脂肪分数图像(图1)上勾画冈上肌、冈下肌、肩胛下肌及小圆肌的感兴趣区,尽量根据肌肉的外侧边缘勾画ROI,避开周围其他组织,自动生成各肌肉的FF值(注意在肌肉萎缩时,肌肉周围的脂肪组织被排除在ROI之外)。在反相位图像上沿冈上肌及冈上窝边缘绘制ROI,得到横截面积,两者的比值即为肌肉占位比。间隔至少两周后重复测量数据,最终的结果为两名医师4次测量结果的平均值。

1.3.1 肌腱回缩Patte分型

       使用斜冠状位T2WI FS图像,根据Patte分型[13]对冈上肌腱回缩进行评价。Patte 1型,冈上肌腱残端靠近肱骨大结节肌腱附着处;Patte 2型,残端位于肱骨头顶端与关节盂水平之间;Patte 3型,残端位于关节盂水平内侧,如图2所示。

1.3.2 半定量脂肪浸润Goutallier分级

       根据FUCHS等[14]改进的Goutallier分级法[15],评估冈上肌脂肪浸润的程度:0级为正常的肌肉,脂肪含量=0;1级为肌肉内可见少许线状、条纹状脂肪信号,脂肪含量<10%;2级为肌肉内少量羽毛状脂肪信号,脂肪含量<肌肉含量;3级为脂肪信号与肌肉信号基本等量,脂肪含量=肌肉含量;4级为脂肪信号多于肌肉信号,脂肪含量>肌肉含量。两位观察者意见不同时经协商达成一致,如图3所示。

1.3.3 Thomazeau萎缩分级

       冈上肌萎缩评估根据THOMAZEAU等[16]的方法,用占位比(R)对冈上肌萎缩进行分级。在斜矢状位“Y”字形截面上,用冈上肌面积除以冈上窝面积,测量占位比(R)(图4)。共分为3个等级:1级=正常或轻度肌萎缩(1.0>R≥0.6),2级=中度肌萎缩(0.6>R≥0.4),3级=重度肌萎缩(R<0.4)。

1.4 统计学分析

       采用SPSS 21.0软件(SPSS Inc, Chicago, IL, USA)、GraphPad Prism 8.0软件(Prism, 8.0.2.263, USA)进行统计学分析,观察者间和观察者内测量FF值的可重复性用组内相关系数(intra-class correlation coefficient, ICC)进行评估,ICC<0.5为一致性较差,0.5≤ICC<0.7为一致性中等,ICC≥0.7为一致性较好。两观察者对Goutallier评分及Thomazeau萎缩分级之间的一致性采用Kappa检验。利用Shapiro-Wilk检验对所有定量值进行正态性检验,符合正态分布的计量资料用(x¯±s)表示,采用独立样本t检验、单因素ANOVA检验;偏态分布的数据用M(Q1,Q3)表示,采用Kruskal-Wallis H检验,组间两两比较用Bonferroni检验。使用Pearson相关性分析评价肩袖肌肉FF值与年龄、症状持续时间的相关性(相关系数r);Spearman相关性评价冈上肌腱损伤分级与肩袖肌群FF值、Goutallier评分及Thomazeau萎缩分级之间的相关性(相关系数rs)。相关系数r≥0.7被认为显著相关;0.5≤r<0.7为强相关;0.3≤r<0.5为中等程度相关;r<0.3为弱相关[17]P<0.05为差异有统计学意义。

2 结果

2.1 一般资料

       最终纳入患者122例,男性56例,女性66例,年龄25~70(54.80±4.46)岁,男性(54.31±1.50)岁,女性(55.19±5.85)岁,患者病程最短2周,最长10年。根据冈上肌损伤结果,分为肌腱部分撕裂组33例,完全撕裂组(Patte 1型)30例,完全撕裂组(Patte 2型)29例,完全撕裂组(Patte 3型)30例。

2.2 观察者测量参数的一致性检验

       观察者间及观察者内部测量肩袖肌肉FF值的一致性较好,如表2所示。两位观察者对冈上肌Goutallier和Thomazeau分级的主观评分一致性较好,如表3所示。

表2  观察者测量肩袖肌肉FF值的一致性检验ICC(95% CI
Tab. 2  Observer consistency test of rotator cuff muscle FF measurements ICC (95% CI)
表3  观察者对冈上肌半定量评分分值分布和一致性分析
Tab. 3  Distribution and consistency analysis of semi-quantitative scores of supraspinatus muscle

2.3 冈上肌腱不同程度撕裂时其他肩袖肌腱损伤程度比较

       随着冈上肌腱损伤程度加重,冈下肌、肩胛下肌、小圆肌的撕裂概率逐渐增加,如表4所示。

表4  冈上肌腱不同程度撕裂时其他肩袖肌腱损伤程度比较
Tab. 4  Comparison of the degree of injury to other rotator cuff tendons when the supraspinatus tendon is torn to varying degrees.

2.4 IDEAL-IQ序列肩袖肌肉脂肪分数在冈上肌损伤不同分级中的比较

       Ⅰ级、Ⅱ级、Ⅲ级、Ⅳ级冈上肌不同损伤分级的各肩袖肌群FF值比较结果显示:(1)冈上肌FF值的总体差异有统计学意义(P<0.001);组内两两比较,Ⅲ级和Ⅰ级、Ⅲ级和Ⅱ级、Ⅳ级和Ⅰ级、Ⅳ级和Ⅱ级组间的FF值差异有统计学意义(P均<0.001)。(2)冈下肌FF值的总体差异有统计学意义(P<0.001)。组内两两比较,Ⅱ级和Ⅲ级、Ⅲ级和Ⅳ级组间的FF值差异有统计学意义(P值分别为0.002,0.010)。Ⅳ级和Ⅰ级、Ⅳ级和Ⅱ级组间的FF值差异有统计学意义(P均<0.001)。(3)肩胛下肌FF值的总体差异有统计学意义(P=0.005)。组内两两比较,Ⅲ级和Ⅱ级、Ⅳ级和Ⅱ级组间的FF值差异有统计学意义(P值分别为0.042,0.012)。(4)小圆肌的FF值差异无统计学意义(P=0.073),具体结果见表5

表5  冈上肌不同损伤分级的肩袖肌群FF值比较
Tab. 5  Comparison of FF values of rotator cuff muscles in different injury grades of supraspinatus muscle

2.5 IDEAL-IQ序列不同肩袖肌肉脂肪分数在冈上肌腱损伤同一分级中的比较

       IDEAL-IQ序列不同肩袖肌肉脂肪分数在肩袖损伤同一分级中比较结果显示,Ⅰ级和Ⅱ级中肩袖肌肉FF值差异无统计学意义,P值分别为0.026,0.102;Ⅲ级和Ⅳ级中肩袖肌肉FF值差异具有统计学意义(图5)。

2.6 肩袖肌肉FF值与冈上肌腱损伤分级、症状持续时间、年龄的相关性

       经Spearman相关性分析,冈上肌、冈下肌的FF值与冈上肌损伤分级呈显著强相关,(rs分别为0.740,0.596,P<0.001),肩胛下肌、小圆肌的FF值与冈上肌腱损伤分级呈弱相关(rs分别为0.257,0.212,P值分别为0.004,0.019),如图6所示。

       经Pearson相关性分析,冈上肌、冈下肌、肩胛下肌FF值与症状持续时间呈中等程度相关(r分别为0.442,0.412,0.314,P均<0.001),小圆肌的FF值与症状持续时间呈弱相关(r=0.277,P=0.002)。

       经Pearson相关性分析,冈上肌、冈下肌、小圆肌的FF值与年龄呈中等相关(r值分别为0.381,0.339,0.349,P均<0.001),肩胛下肌的FF值与年龄呈弱相关(r=0.216,P=0.017)。

       经Spearman相关性分析,冈上肌损伤程度分级与Goutallier分级、Thomazeau分级之间呈显著正相关(rs分别为0.757,0.737,P均<0.001)。

2.7 冈上肌FF值与半定量Goutallier分级、Thomazeau分级的比较

       根据Goutallier分级,将病例分为5级,随着分级增高,冈上肌FF值增加。冈上肌FF值在5级中总体比较差异有统计学意义(P<0.001);冈上肌Goutallier 0级、1级分别与3级、4级比较,2级与4级比较,差异均有统计学意义,(P均<0.001),Goutallier 0级与2级、2级与3级、3级与4级比较,差异有统计学意义(P值分别为0.005,0.019,0.012),如表6所示。

       根据Thomazeau分级,将冈上肌萎缩程度分为3级,FF值随着分级的增加逐渐增高,冈上肌FF值在3级中总体比较差异有统计学意义(P<0.001),组内两两比较差异有统计学意义(P均<0.001),如表6所示。

表6  冈上肌FF值与半定量分级之间的比较
Tab. 6  Comparison between the FF values of the supraspinatus muscle and the semi-quantitative grading

3 讨论

       本研究采用IDEAL-IQ定量参数对冈上肌损伤患者的肩袖肌群脂肪浸润程度进行定量分析,结果显示随着冈上肌腱损伤程度加重,肩袖肌肉脂肪浸润程度逐渐加重,以冈上肌、冈下肌脂肪浸润为著,且冈上肌腱损伤程度与冈上肌FF值呈显著相关,与冈下肌的FF值呈强相关性,与肩胛下肌、小圆肌的FF值呈弱相关。另外肩袖肌肉FF值与年龄、症状持续时间呈正相关。

3.1 Goutallier分级与IDEAL-IQ脂肪定量技术

       目前临床应用相对广泛的脂肪浸润分级评分主要是Goutallier评分法,该分级将肩袖肌肉的脂肪浸润情况与肌肉的本身比例分为5个等级,但是该分级主要依据观察者的主观性判断,重复性较差,具有一定局限性,并不能准确地实现脂肪定量[18, 19]。本研究也显示在2个具有丰富骨肌系统影像诊断经验的观察者之间,对半定量评分的一致性并非很高(Kappa=0.653),而基于IDEAL-IQ技术的脂肪变性定量评估显示,在不同观察者间,具有很高的一致性(ICC>0.85),在克服了传统水脂分离技术对主磁场均匀度依赖性的基础上,提高了脂肪定量的准确性及可重复性。一般来说,随着肩袖肌撕裂的进展,冈上肌脂肪变性及萎缩程度增加,其中最严重的变性发生在巨大的撕裂,如以前的报道[20, 21, 22]。本研究还发现,IDEAL-IQ的FF值、Goutallier分级以及Thomazeau萎缩分级与冈上肌损伤分级之间高度相关,差异具有统计学意义。

3.2 冈上肌腱不同程度损伤后肩袖肌群FF值

       本研究发现,在冈上肌腱损伤Ⅰ级和Ⅱ级中,冈上肌、冈下肌、肩胛下肌及小圆肌的FF值之间差异并无统计学意义,而在Ⅲ级、Ⅳ级中,肩袖肌群FF值具有显著差异,说明冈上肌腱发生损伤后会随着病情的进展肩袖肌群脂肪浸润逐渐增加,与董康康等[23]研究结果基本一致。换言之,冈上肌腱全层撕裂并出现一定程度的回缩可被视为肩袖肌肉脂肪变性增加的危险因素,而肌腱完全撕裂无明显回缩时与部分撕裂的脂肪浸润并无显著性差异。分析原因可能是随着肌腱撕裂程度的不断加重,纤维蛋白结构被完全破坏、具有分化为脂肪细胞的成脂纤维祖细胞(fibro-adipogenic progenitors, FAPS)增多[7, 24],肌纤维分子逐渐被脂肪成分替代,或是已有的脂肪细胞增殖、肌肉周围脂肪细胞浸润。另外,冈上肌腱损伤会引发炎症反应,炎症细胞因子升高、炎症细胞浸润会导其他肩袖肌肉以及关节周围的组织病变的发展。并且炎症细胞迁移到肌腱损伤处造成肌纤维凋亡,肌肉萎缩,甚至随着时间推移,炎症细胞会促使肌源性前提细胞启动脂肪生成途径,使得成熟脂肪细胞浸润游离的肌间纤维和肌内纤维间隙,最终使肌肉细胞减少,脂肪浸润随之增加[25, 26]。其次,本研究发现,随着冈上肌腱损伤程度加重,其他肩袖撕裂概率增加。脂肪浸润主要累及冈上肌、冈下肌,且在Ⅲ级和Ⅳ级中,两者之间FF值差异并无统计学意义。可能是由于冈上肌、冈下肌均由肩胛上神经支配,冈上肌发生严重撕裂时常伴随肩胛上神经的病变,肌肉收缩舒张牵引肩胛上神经病变,导致冈上肌及冈下肌失神经营养严重,肌力丧失,进而引起脂肪沉积[27, 28, 29, 30, 31]。然而,也有研究显示[32, 33, 34],神经病变与肩袖撕裂和脂肪浸润的相关性较低。在我们的研究中,并没有肌电图数据或其他直接的肩胛上神经病变的评估,因此我们的数据并不强烈支持或反驳肩胛上神经病变在肩袖肌脂肪浸润中的作用。另外,生物力学和解剖学研究表明[35],冈下肌作为肩部的外旋肌,并压缩盂肱关节,还可以在肩胛平面中充当肩外展肌和肱骨提举肌,特别是当手臂内旋时。冈下肌由位于肩胛冈正下方的明显横向部分和位于该区域尾部的明显倾斜区域组成,由于其位置和神经支配,冈下肌的横纤维可能与冈上肌的横纤维密切相关。当发生冈上肌撕裂时,冈下肌的这个区域对于肩部外展可能变得更加重要。LAWRENCE等[36]也发现,在孤立性冈上肌腱撕裂的患者中,16.5%有冈下肌退变的证据,冈下肌变性在孤立性冈上肌撕裂的个体中并不罕见,并且与伴随的冈上肌变性最相关。本研究还发现,随着冈上肌腱撕裂程度加重,伴随着冈下肌腱撕裂概率增加。

3.3 肩袖肌群FF值与症状持续时间及年龄的相关性

       另外,本研究通过Pearson相关性分析发现,冈上肌、冈下肌、肩胛下肌FF值与症状持续时间呈中等程度相关,小圆肌的FF值与症状持续时间呈弱相关。与GILBERT等[37]发现的脂肪含量与症状持续时间有较强相关性有差异。分析其中原因可能是由于病史采集时不同职业、不同性别及年龄的患者对疼痛主观感受差异导致症状持续时间产生偏差,因此结果相关性较低。另外,肩袖肌腱撕裂时,有90.8%的病例小圆肌保持完整,并提供一定强度的外旋动力[38],在涉及冈下肌的大的撕裂中,小圆肌常出现进行性代偿性肥大[39, 40],而很少出现萎缩及脂肪浸润,故与症状持续时间呈弱相关。本研究还发现肩袖肌肉的FF值与年龄呈正相关,与KÄLIN等[41]研究结果一致,表明随着年龄增长,肩袖肌肉脂肪浸润会有所增加。而肩胛下肌的FF值与年龄相关性最弱,分析原因可能是由于肩胛下肌在解剖学上由上三分之二的肌腱区域和下三分之一膜性结构组成,肩胛下肌的上、下部分是独立的肌肉单位,由不同的神经支配,大多数肩胛下肌肌腱撕裂始于上缘并逐渐发展到下部,并且该肌肉的脂肪浸润也首先贯穿整个上部,然后才延伸到下部[42, 43],与冈上肌腱和冈下肌腱撕裂的起始和结构不同,这些肌肉中的脂肪浸润进展似乎是均匀地扩散到整个肌肉。因此,肩胛下肌脂肪的浸润性评估应不同于冈上肌和冈下肌。而本研究在进行肩胛下肌脂肪分数测量时,并未考虑肩胛下肌解剖因素及脂肪浸润过程的影响,ROI的绘制包含整个肩胛下肌,测得其中的平均值,因此笔者认为此是肩胛下肌FF值与年龄无显著相关的主要原因。

3.4 本研究局限性

       本研究尚存在一定的局限性:(1)本研究限于肌腱完全撕裂样本较少,拟日后增加样本量对现有的结论进行验证;(2)本研究测量了肩关节斜矢状面“肩胛骨Y视图”脂肪分数值,但本研究中的脂肪分数值是否反映了整个肩袖肌肉的脂肪分数值,我们还需要进一步的研究来评估。

4 结论

       综上所述,3.0 T MRI IDEAL-IQ技术可以量化肩袖肌肉脂肪浸润程度,反映肌腱损伤严重程度并监测疾病进展过程,为临床干预提供客观依据。

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