基于MRI测量小腿软组织厚度对原发性下肢淋巴水肿分期的研究

刘梦珂; 李兴鹏; 张妍; 郝琪; 孙小丽; 李滨; 王仁贵

doi:10.15953/j.ctta.2022.100

基于MRI测量小腿软组织厚度对原发性下肢淋巴水肿分期的研究

doi: 10.15953/j.ctta.2022.100

刘梦珂^1a,,
李兴鹏^1a,
张妍^1a,
郝琪²,
孙小丽^1a,
李滨^1b, ,,
王仁贵^1a, ,

1.
放射科；首都医科大学附属北京世纪坛医院
2.
磁共振室，北京100038 首都医科大学附属北京世纪坛医院
2.
北京大学第九临床医学院放射科, 北京100038

基金项目: 国家自然科学基金面上项目（基于多模态影像和遗传基因筛查对原发性淋巴水肿临床分期和分级精准评价的人工智能分析（61876216））；北京市医管局“培育计划”（基于MR mDixon序列的淋巴水肿肢体体积及脂肪含量测量的临床应用研究（PX2020030））；北京世纪坛医院淋巴外科开放课题专项基金（肢体淋巴水肿体积指数的可行性研究（2019-LB04））。

详细信息

作者简介:
刘梦珂：女，首都医科大学附属北京世纪坛医院博士研究生，主要从事淋巴系统疾病的影像学诊断，E-mail：805587047@qq.com

李滨：男，首都医科大学附属北京世纪坛医院磁共振室主治医师，主要从事淋巴系统疾病的影像学诊断，E-mail：libin2434@bjsjth.cn

王仁贵：男，首都医科大学附属北京世纪坛医院放射科主任医师，主要从事弥漫性肺疾病及淋巴系统疾病的影像学诊断，E-mail：wangrg@bjsjth.cn

通讯作者:
李滨✉，男，首都医科大学附属北京世纪坛医院磁共振室主治医师，主要从事淋巴系统疾病的影像学诊断，E-mail：libin2434@bjsjth.cn

王仁贵✉，男，首都医科大学附属北京世纪坛医院放射科主任医师、博士生导师，主要从事胸部影像学及淋巴系统疾病的影像学诊断，E-mail：wangrg@bjsjth.cn

中图分类号: R 816；R 322.2+7
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出版历程
- 收稿日期: 2022-05-26
- 修回日期: 2022-07-01
- 录用日期: 2022-07-06
- 网络出版日期: 2022-07-13
- 刊出日期: 2022-08-01

Study on the Staging of Primary Lower Extremity Lymphedema Based on Calf Soft-tissue Thickness Measurement by MRI

LIU Mengke^{1a
,},
LI Xingpeng^1a,
ZHANG Yan^1a,
HAO Qi²,
SUN Xiaoli^1a,
LI Bin^{1b
, ,},
WANG Rengui^{1a
, ,}

1.
Capital Medical University, Beijing 100038, China Department of Radiology
2.
Capital Medical University, Beijing 100038, China Department of MR, Affiliated Beijing Shijitan Hospital
2.
Department of Radiology, The Ninth Clinical Medical College of Peking University, Beijing 100038,China

摘要

摘要: 目的：探讨基于MRI测量小腿软组织厚度对评估原发性下肢淋巴水肿（PLEL）分期的价值。方法：回顾性收集确诊为PLEL患者90例的临床及MR影像资料，所有患者均行双侧下肢MR检查。采用短时反转恢复序列（STIR）序列测量双侧小腿软组织总厚度（T）、肌骨厚度（M）和皮下软组织厚度（S），分别计算双侧小腿T及S的差值（DT、DS）。参考2020年国际淋巴协会及淋巴外科下肢淋巴水肿的临床分期标准将患者分为Ⅰ、Ⅱ、Ⅲ 期。使用单因素方差分析比较不同临床分期之间的小腿软组织厚度，使用Spearman相关分析小腿软组织厚度与临床分期的相关性，使用ROC曲线确定小腿软组织厚度对临床分期的鉴别效能。结果：3期之间T、S、DT及DS差异均有统计学意义，而M不存在统计学差异；各分期间两两比较，T、S、DT及DS在Ⅰ期与Ⅱ期及Ⅰ期与 Ⅲ 期之间比较均具有统计学差异，而在Ⅱ期与 Ⅲ 期比较无统计学差异。DT（r=0.750）与DS（r=0.772）与临床分期的相关性明显大于T（r=0.669）及S（r=0.734），DS与临床分期相关性最高；M与临床分期无明显相关关系。ROC曲线显示各参数鉴别Ⅰ期与Ⅱ期的AUC值大于鉴别Ⅱ期与 Ⅲ 期的AUC值，所有参数中DS（AUC=0.945）鉴别Ⅰ期与Ⅱ期的曲线下面积（AUC）最高。结论：MRI小腿软组织厚度测量可以作为单侧PLEL临床分期的定量辅助方法，对于单侧PLEL患者，我们推荐DS作为鉴别Ⅰ期与Ⅱ期淋巴水肿的最佳厚度指标。
- MRI /
- 淋巴水肿 /
- 原发性 /
- 下肢 /
- 分期
Abstract: Objective: To investigate the value of MRI-based measurement of calf soft-tissue thickness in assessing the clinical staging of primary lower extremity lymphedema (PLEL). Methods: The clinical and MR imaging data of 90 patients diagnosed with PLEL in our hospital were retrospectively collected, and all patients underwent bilateral lower limb MR examinations. Short Time Inversion Recovery (STIR) sequence was used to measure the total soft tissue thickness (T), musculoskeletal thickness (M) and subcutaneous soft tissue thickness (S) of bilateral lower legs, and the difference between T and S of bilateral lower legs (DT, DS) was calculated respectively. Patients were classified into stages Ⅰ, Ⅱ and Ⅲ with reference to the clinical staging criteria of the International Lymphatic Association 2020 and our lymphatic surgery department for lower limb lymphedema, excluding stage 0. One-way ANOVA was used to compare calf soft tissue thickness among different clinical stages, Spearman correlation was used to analyze the correlation between calf soft tissue thickness and clinical stage, and ROC curves were used to evaluate the efficacy of calf soft tissue thickness in discriminating clinical stage. Results: The differences among T, S, DT and DS of the three stages were statistically significant, while there was no statistical difference among M; when comparing two by two in each subperiod, T, S, DT and DS were statistically different between stage Ⅰ and Ⅱ and stage Ⅰ and Ⅲ, while there was no statistical difference between stage II and III. The correlation between DT (r=0.750) and DS (r=0.772) and clinical stage was significantly greater than that between T (r=0.669) and S (r=0.734), with DS showing the highest correlation with clinical stage; there was no significant correlation between M and clinical stage. ROC curves showed that the AUC values for each parameter to identify stage Ⅰ and Ⅱ were greater than those to identify stage Ⅱ and Ⅲ. The AUC value of DS (AUC=0.945) demonstrated the highest area under the curve (AUC) among all parameters to identify stage Ⅰ and stage Ⅱ. Conclusion: MRI soft-tissue thickness measurement of calf can be used as a quantitative adjunct in the clinical staging of unilateral PLEL, and for patients with unilateral PLEL, we recommend DS as the best thickness index to differentiate stage Ⅰ from Ⅱ lymphedema.
- MRI /
- lymphedema /
- primary /
- lower extremity /
- stage

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图 1 小腿软组织总厚度（T）、肌肉厚度（M）和皮下组织厚度（S）的测量方法

在小腿轴面STIR图像上，通过小腿上1/3及下1/3层面正中位置（虚线）画一条水平线，测量两层面软组织的厚度。这些线分别与小腿的内侧（a）和外侧（d）皮肤、内侧（b）和外侧（c）浅筋膜相交，（a）与（d）之间的距离表示T的值；（b）与（c）之间的距离表示M的值。S为T减M。健侧小腿的T、M和T的测量方法同患侧小腿。

Figure 1. Total soft tissue thickness (T), muscle thickness (M) and subcutaneous tissue thickness (S) of calf were measured

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图 2 STIR图像显示不同临床分期皮下软组织厚度的变化

（a）女，14岁，右下肢原发性下肢淋巴水肿1年余（箭头）（Ⅰ期）；（b）男，12岁，左下肢原发性下肢淋巴水肿4年（箭头）（Ⅱ期）；（c）女，74岁，右下肢原发性下肢淋巴水肿8年（箭头）（Ⅲ 期）。

Figure 2. STIR images show changes in subcutaneous soft tissue thickness at different clinical stages

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图 3 ROC曲线显示患侧小腿的T、S、DT以及DS进行下肢淋巴水肿分期的效能

（a）Ⅰ期与Ⅱ期比较；（b）Ⅱ期与 Ⅲ期比较。T：总厚度；S：皮下软组织厚度；DT：患侧与健侧总厚度差值；DS：患侧与健侧皮下软组织厚度差值。

Figure 3. ROC curve showed the effectiveness of T, S, DT and DS of the affected leg in staging lymphedema of the lower limb

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表 1 2020年国际淋巴协会肢体淋巴水肿临床分期标准

Table 1. Clinical staging criteria for limb lymphedema by the International Lymphatic Society 2020

分期	临床表现
0期	亚临床状态，淋巴系统受损，组织液或成分发生微小变化，但肿胀不明显。可在水肿发生（I～Ⅲ 期）之前存在数月或数年。
Ⅰ期	水肿部位柔软，按压可凹陷，无皮肤纤维化，抬高患肢后肿胀可缓解，又称可逆性水肿。
Ⅱ期	抬高患肢肿胀消退不明显，后期由于皮下脂肪过多和纤维化，水肿可呈非凹陷性。
Ⅲ 期	水肿不可凹陷，病变肢体皮肤改变如脂肪沉积，色素沉着、棘皮病、疣状增生，呈现淋巴象皮肿。

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表 2 不同分期的原发性下肢淋巴水肿的临床资料

Table 2. Clinical data of patients with primary lymphedema of the lower extremity at different clinical stages

项目		分期临床资料
项目		Ⅰ（n=33）	Ⅱ（n=44）	Ⅲ（n=13）
年龄/岁^*		20.00±19.00	35.50±27.00	29.50±29.00
病程/年^*		2.00±9.40	9.00±21.25	9.00±15.00
性别/n（%）^a	女	21（63.64）	26（59.09）	7（53.84）
性别/n（%）^a	男	12（36.36）	18（40.91）	6（46.16）
注：*-数据采用中位数±四分位间距表示；a-计数资料采用频数（构成比）表示。

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表 3 原发性下肢淋巴水肿患者不同临床分期小腿软组织厚度比较

Table 3. Comparison of calf soft tissue thickness in patients with primary lymphedema of the lower extremity at different clinical stages

参数	分期			统计检验
参数	Ⅰ（n=33）	Ⅱ（n=44）	Ⅲ（n=13）	F/χ	P
T/cm	10.66±0.91^a,b	13.04±1.89^a	14.53±2.67^b	28.821	<0.001
M/cm	8.08±0.77	8.42±1.30	8.24±0.87	0.944	0.393
S/cm	2.58±0.69^a,b	4.62±1.39^a	6.29±2.47^b	37.970	<0.001
DT/cm	0.95±0.80^1,a,b	3.50±1.62^a	4.94±2.55^b	52.231¹	<0.001
DS/cm	1.00±0.65^a,b	3.18±1.34^a	3.40±3.00^1,b	54.861¹	<0.001
注：1-数据采用（中位数±四分位数间距）表示，组间比较采用非参数检验；余数据采用均数±标准差表示，组间　　　比较采用单因素方差分析。a-Ⅰ期与Ⅱ期比较，P<0.05；b-Ⅰ期与 Ⅲ 期比较，P<0.05。

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表 4 原发性下肢淋巴水肿患者小腿软组织厚度鉴别Ⅰ期及Ⅱ期的ROC曲线分析

Table 4. ROC curve analysis of stage Ⅰ and Ⅱ differentiation of leg soft tissue thickness in patients with primary lower extremity lymphedema

参数	AUC	95% CI	P	Youden指数	临界值/cm	敏感性/%	特异性/%
T	0.882	0.788～0.944	<0.0001	0.6515	11.55	77.27	87.88
S	0.916	0.830～0.967	<0.0001	0.7121	3.55	77.27	93.94
DT	0.935	0.855～0.979	<0.0001	0.8106	1.65	93.18	87.88
DS	0.945	0.869～0.984	<0.0001	0.7879	1.60	90.91	87.88

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表 5 原发性下肢淋巴水肿患者小腿软组织厚度鉴别Ⅱ期及 Ⅲ 期的ROC曲线分析

Table 5. ROC curve analysis of leg soft tissue thickness in stage Ⅱ and Ⅲ differentiation of primary lymphedema of lower extremities

参数	AUC	95% CI	P	Youden指数	临界值/cm	敏感性/%	特异性/%
T	0.667	0.530～0.786	0.063	0.325	14.90	46.15	86.36
S	0.705	0.570～0.819	0.018	0.362	7.35	38.46	97.73
DT	0.685	0.549～0.802	0.020	0.400	2.95	92.31	47.73
DS	0.717	0.582～0.828	0.007	0.432	2.60	100.00	43.18

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