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临床研究
磁共振扩散加权成像定量评估克罗恩病活动性的临床应用价值
程静云 查云飞 刘昌盛 李玉爽 杨仁杰

Cite this article as: Cheng JY, Zha YF, Liu CS, et al. The clinical application value of DWI in quantitative evaluation of Crohn′s disease lesions[J]. Chin J Magn Reson Imaging, 2022, 13(1): 48-53.本文引用格式:程静云, 查云飞, 刘昌盛, 等. 磁共振扩散加权成像定量评估克罗恩病活动性的临床应用价值[J]. 磁共振成像, 2022, 13(1): 48-53. DOI:10.12015/issn.1674-8034.2022.01.010.


[摘要] 目的 探讨磁共振扩散加权成像(diffusion weighted imaging,DWI)定量评估肠道克罗恩病(Crohn′s disease,CD)病变的活动性的价值。材料与方法 回顾性分析了51例确诊为CD的患者,患者均在2周时间内进行磁共振小肠成像(magnetic resonance enterography,MRE)、DWI及小肠镜检查。根据CD简化内镜活动性评分(simplified endoscopic activity score for Crohn′s disease,SES-CD)将病变肠段分为缓解组(0~2)、轻微活动组(3~6)及中重度活动组(>6)。观察MRE及DWI表现,计算磁共振活动指数(magnetic resonance index of activity,MaRIA)及测量表观扩散系数(apparent diffusion coefficient,ADC)。采用Kruskal-Wallis秩和检验比较不同活动组间MaRIA及ADC值的差异性,采用ROC曲线分析MaRIA及ADC值区分不同活动期病变的诊断效能,MaRIA及ADC值与SES-CD的相关性采用Spearman相关分析。结果 共127个肠段纳入研究,缓解组15段,轻微活动组45段,中重度活动组67段,SES-CD评分为1.0~11.0。不同组间MaRIA及ADC值差异均有统计学意义(P均小于0.01)。MaRIA及ADC值与SES-CD的相关性分别为0.793 (P<0.01)和-0.742 (P<0.01)。ROC曲线分析发现,当MaRIA为9.1,ADC值为-1.585×10-3 mm2/s时,区分缓解组与活动组的曲线下面积最大分别为0.962 (P<0.01)及0.957 (P<0.01);当MaRIA为11.1,ADC值为-1.345×10-3 mm2/s时,区分缓解-轻微活动组与中重活动组的曲线下面积最大分别为0.942 (P<0.01)及0.920 (P<0.01)。结论 DWI可定量准确区分CD不同活动期病灶。
[Abstract] Objective To explore the value of magnetic resonance diffusion weighted imaging (DWI) to quantitatively assess the activity of intestinal Crohn's disease (CD) lesions.Materials and Methods: A total of 51 patients diagnosed with CD were retrospectively analyzed, all of those were underwent magnetic resonance enterography (MRE), DWI and enteroscopy within 2 weeks. The lesions of bowel segments were graded as inactive (0-2), mild (3-6), and moderate-severe group (>6) based on simplified endoscopic activity score for Crohn′s disease (SES-CD).To observe the performance of MRE and DWI, and calculate the magnetic resonance index of activity (MaRIA) and the apparent diffusion coefficient (ADC) value of the lesions. The Kruskal-Wallis rank sum test was applied to compare the differences in MaRIA and ADC values among different activity groups, and the receiver operating characteristic (ROC) curve was used to analyze the diagnostic efficiency of MaRIA and ADC values to distinguish different active lesions. Spearman analysis was used to evaluate the correlation between SES-CD and MaRIA, ADC values.Results A total of 127 intestinal segments were included in the study. There were 15 inactive, 45 mild, and 67 moderate-severe. The SES-CD score ranged from 1.0 to 11.0. There were significant differences in MaRIA and ADC values among different groups (P<0.01). The correlations between SES-CD and MaRIA, ADC values were 0.793 (P<0.01) and -0.742 (P<0.01), respectively. ROC curve analysis found that when the MaRIA was the threshold at 9.1 and the ADC value was the threshold at -1.585×10-3 mm2/s, the maximum of area under the curves (AUCs) to distinguish the inactive from the active were 0.962 (P<0.01) and 0.957 (P<0.01), respectively. When the MaRIA was the threshold at 11.1 and the ADC value was the threshold at -1.345×10-3 mm2/s, the maximum of AUCs to distinguish the inactive-mild from the moderate-severe were 0.942 (P<0.01) and 0.920 (P<0.01), respectively.Conclusions DWI can quantitatively and accurately distinguish the lesions in different active stages of CD.
[关键词] 克罗恩病;磁共振成像;扩散加权成像;活动性评分
[Keywords] Crohn's disease;magnetic resonance imaging;diffusion weighted imaging;activity score

程静云    查云飞 *   刘昌盛    李玉爽    杨仁杰   

武汉大学人民医院放射科,武汉 430060

查云飞,E-mail:zhayunfei999@126.com

全部作者均声明无利益冲突。


收稿日期:2021-07-16
接受日期:2021-11-26
中图分类号:R445.2  R574.5 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.01.010
本文引用格式:程静云, 查云飞, 刘昌盛, 等. 磁共振扩散加权成像定量评估克罗恩病活动性的临床应用价值[J]. 磁共振成像, 2022, 13(1): 48-53. DOI:10.12015/issn.1674-8034.2022.01.010

       克罗恩病(Crohn′s disease,CD)是一种可累及整个胃肠道的慢性非特异性肠道疾病,该病具有透壁特性,且缓解与复发交替,约40%的患者最终发展为肠腔狭窄或肠瘘,严重损害了患者生活质量[1, 2]。CD患者病变的严重程度、活动性、病变范围随着时间推移而不断变化。定期随访检查并准确评估CD活动性对于指导临床治疗,控制CD病变进展,提高患者生活质量至关重要[2]。目前,尽管内镜检查是评估CD活动性的金标准[1],但内镜具有侵袭性,无法通过狭窄肠段,不能观察肠腔外病灶等缺点[2],限制了其在CD患者长期随访检查中的应用。而CT及MR小肠成像无侵袭性,患者舒适度良好,可准确客观显示肠腔内外病灶及并发症,已广泛用于CD患者随访检查。

       与CT相比,磁共振小肠成像(magnetic resonance enterography,MRE)具有无电离辐射,软组织分辨率高,多参数成像等优势,尤其适用于年轻CD患者的随访检查[3, 4, 5]。研究表明,基于MRE而形成的磁共振活动指数(magnetic resonance index of activity,MaRIA)与CD内镜严重指数(Crohn′s disease endoscopic index of severity,CDEIS)高度相关,可准确评估CD患者药物疗效[5, 6, 7, 8]。然而,MaRIA计算烦琐,尚未能广泛用于临床。扩散加权成像(diffusion weighted imaging,DWI)可无创性评估组织内水分子自由扩散运动。研究表明,随着CD病变活动性加重,肠壁黏膜水分子明显扩散受限,表观扩散系数(apparent diffusion coeffecient,ADC)值相应降低[9, 10, 11, 12, 13]。ADC值的测量相对简单,对于肾功能不全的患者及儿童患者,DWI将是一种可替代钆剂增强的有效检查方法[12,14]。尽管DWI已用于评估CD病变活动性,但目前ADC值区分不同活动期病变的阈值仍未统一标准。笔者对CD患者进行回顾性分析,以CD简化内镜活动性评分为参考标准,探讨DWI在定量评估CD病变活动性中的临床应用价值。

1 资料与方法

1.1 研究对象

       本研究经武汉大学人民医院伦理委员会批准,免除受试者知情同意,批准文号:WDRY2021-KS041。回顾性分析了本院2018年9月至2020年12月符合以下标准的患者。纳入标准:(1)经小肠镜、病理、临床表现、影像学检查、实验室检查等综合诊断为CD[1];(2)小肠镜检查与MRE及DWI检查间隔时间小于或等于2周;(3)肠道充盈良好,伪影较小,不影响病变诊断及评估。排除标准:(1)在小肠镜及MR检查前行肠切除术的患者;(2)内镜资料不完整者。CD患者临床活动性评分采用Harvey-Bradshaw指数(Harvey-Bradshaw index,HBI),并检测血沉(erythrocyte sedimentation rate,ESR)及C-反应蛋白(C-reactive protein,CRP)水平。

1.2 MR检查方法

       检查前准备:患者于检查前1天进食流质或半流质饮食,于当晚或第二天清晨冲服聚乙二醇电解质溶液清洁肠道。检查前约1 h分5~6次匀速口服2.5%等渗甘露醇溶液1500~2000 mL充盈肠道,每次口服量约300 mL。扫描前10 min肌注盐酸消旋山莨菪碱(杭州民生药业有限公司,1 mL∶10 mg) 10 mg抑制肠道蠕动,有青光眼、前列腺增生等禁忌证者除外。

       检查设备及方案:采用GE Discovery 750w 3.0 T超导磁共振及16通道体部相控阵线圈扫描。采取仰卧位扫描。扫描前训练患者呼吸。常规MRE序列行冠状位及轴位屏气扫描,扫描序列及参数如下:(1)单次激发快速自旋回波序列(SS-FSE) T2WI:冠状位或轴位,TR min,TE 68 ms,层厚4 mm,层间距0.3 mm,矩阵288×288,翻转角90°,激励次数0.5。(2)平衡式稳态自由进动序列(FIESTA):冠状位脂肪抑制,TR 4.2 ms,TE 1.5 ms,层厚4 mm,层间距0.3 mm,矩阵256×288,翻转角45°,激励次数1.0。磁共振动态增强扫描采用高压注射器以2.0 mL/s流速注射钆对比剂(钆喷酸葡胺,商品名Magnevist;北京北陆制药有限公司) 0.2 mL/kg (10 g∶4.69 g),分别在注射对比剂前及注射后30、60、90、180 s行冠状位多期扫描。扫描序列为肝脏容积加速采集序列(liver acquisition with volume acceleration,LAVA),TR 4.9 ms,TE 2.4 ms,层厚5.0 mm,层间距0,矩阵256×160,翻转角12°,激励次数0.75。DWI扫描在自由呼吸模式下进行,采用呼吸门控单次激发自旋回波平面成像序列行轴位扫描,b值为0、800、1000 s/mm2,TR 7000 ms,TE 58 ms,层厚5 mm,层间距为1 mm,矩阵288×288,翻转角90°,激励次数4。

1.3 内镜检查及评估

       患者于检查前一晚口服2000 mL聚乙二醇电解质溶液清洁肠道。由1名具有10年以上肠镜经验的内镜医师采用单气囊电子小肠镜(SIF-Q260 Olympus,日本)在异丙酚(Fresenius Kabi Austria GmbH,奥地利)麻醉下进行检查。分别经口进镜至空肠距幽门约350 cm和经肛进镜至回盲瓣约150 cm行小肠镜检查,病变处均多点取活检。

       由1名具有5年以上消化内镜阅片经验的医生根据CD简化内镜活动性评分(simplified endoscopic activity score for Crohn′s disease,SES-CD)对每个肠段最严重处进行评估。评估内容包括:溃疡大小、面积、病变范围、肠段是否存在狭窄及程度[15],小肠及结肠共分为7段,分别为空肠、近段回肠、末端回肠(距回盲瓣约10 cm的回肠)、盲肠及升结肠、横结肠、降结肠及乙状结肠、直肠。近段回肠为除末端回肠之外的回肠部分[3]。每个肠段根据SES-CD被分为缓解组(0~2)、轻微活动组(3~6)及中重度活动组(>6)。

1.4 MR图像评估

       将MR小肠成像数据上传至GE AW4.4工作站进行测量。在肠腔充盈良好的条件下,将肠壁增厚(>3 mm)或异常高强化的肠管定义为病变肠段[16]。MR肠管分段同上文内镜肠管分段。由2名分别具有5年及15年MR肠道阅片经验的影像医师进行评估,评估内容包括:肠壁厚度,肠壁溃疡(增厚肠段黏膜表面的凹陷),肠壁水肿,相对强化程度(relative contrast enhancement,RCE),MR活动性指数(magnetic resonance index of activity,MaRIA)及ADC值,评估项目出现分歧较大时,经讨论后达成一致。

       ADC值的计算公式为:Sb=S0×exp (-b×ADC)[17],其中S0代表b值为0时的信号强度,Sb为指定b值下的信号强度,ADC为表观扩散系数。ADC值的测量在b值为800 s/mm2的图像上进行,选取病变最突出的切面及相邻上下两个切面,沿着肠壁最亮信号区域的边界手动绘制感兴趣区(region of interest,ROI),计算3个切面ROI的平均值[18]

       MaRIA的计算公式为[6,19]:MaRIA=1.5×肠壁厚度(mm)+0.02×RCE+5×水肿+10×溃疡,其中RCE的计算公式为:RCE=[(SIpost-SIpre)/(SIpre)]×100×(SDnoisepre/SDnoisepost),其中SIpre及SIpost分别代表注射对比剂前后的肠壁信号强度,SDnoisepre及SDnoisepost分别代表注射对比剂前后体部外背景噪声的标准差。SIpost及SDnoisepost的测量在注射对比剂70 s后的LAVA图像上测量。SIpre及SIpost的测量方法为,将图像适当放大,在增厚肠壁内侧画3个相邻的ROI,ROI大小为3~6 mm2,尽量避开肠壁水肿及肠内容物,并计算平均值。SDnoisepre及SDnoisepost的测量方法为,将面积为60~80 mm2的ROI置于体外视野内,注射对比剂前后ROI位置相同。

       由于DWI图像分辨率较低,有15段缓解期及3段轻微活动期病灶在内镜上显示,而在DWI图像上未显示,中重度活动期病变均在内镜及DWI图像显示。最后纳入研究的肠段在内镜及MR图像均被检测到。

1.5 统计分析

       采用SPSS 25.0 (IBM Corp.,Armonk,NY)软件进行统计分析。计量资料经Kolmogorov-Smirnov正态性检验后,符合正态分布的用均数±标准差(x¯±s)表示,偏态分布以中位数(25%,75%)表示。用组内相关系数(intra-class correlation coefficient,ICC)评价2名放射科医师测量肠壁厚度、RCE及ADC的一致性,采用Kappa检验评价两名放射科医师评估各肠段肠是否存在肠壁溃疡、肠壁水肿的一致性。采用单因素差分析(ANOVA)或Kruskal-Wallis检验比较不同活动组间ADC值及MaRIA的差异性。采用ROC分析MaRIA及ADC值区分缓解组与活动组及缓解-轻微活动组与中重度活动组的效能,并计算出相应曲线下面积(areas under the curves,AUCs),采用Delong分析比较MaRIA及ADC值的AUC。采用Spearman相关分析评价ADC值、MaRIA和SES-CD的相关性。P<0.05为差异有统计学意义。

2 结果

2.1 小肠镜结果

       51例患者(男37例,女14例),共127段肠管纳入研究,其中空肠4段,近段回肠32段,末端回肠43段,右半结肠18段,横结肠9段,左半结肠16段,直肠5段。缓解期15段,轻微活动期45段,中重度活动期67段,SES-CD评分为1.0~11.0。有45例患者MR及内镜检查间隔时间小于或等于7天,6例患者检查间隔时间在7至14天。HBI为5.0 (7.0,9.0),CRP为22.0 (12.0,44.0) mg/L,ESR为23.6 (7.2,46.9) mm/h。

2.2 MRI结果

       两名医师评估肠壁厚度、ADC值及RCE的一致性较好,ICC分别为0.93、0.92、0.89,P值均小于0.01;两名医师评估肠壁溃疡及肠壁水肿的一致性好,Kappa值分别为0.83及0.89,P值均小于0.01。

       ADC值、MaRIA与SES-CD呈显著相关,r值分别为-0.742及0.793,P值均小于0.01;ADC值与MaRIA相关性较好,r值为-0.655 (P<0.01)。缓解组ADC值为(-1.90±0.18)×10-3 mm2/s,轻微活动组ADC值为(-1.51±0.23)×10-3 mm2/s,中重度活动组ADC值为(-1.21±0.10)×10-3 mm2/s (图1)。不同组间ADC值差异有统计学意义(F=65.6,P<0.01) (图2)。随着病灶活动性增加,ADC值显著降低,MaRIA显著增加。MaRIA在不同活动组间差异有统计学意义(F=116.6,P<0.01)。两两比较结果,ADC值及MaRIA在不同组间差异有统计学意义,P值均小于0.05。

图1  男,31岁,克罗恩病中重度活动期患者,SES-CD为7,MaRIA为12。A~E显示末端回肠肠壁增厚(黄箭),T2WI及抑脂图像上(A~C)显示肠壁水肿,呈线状高信号(红箭),增强图像(D与E)显示肠壁明显强化,肠壁水肿未见强化(E红箭),表现为线状低信号。DWI图(F)显示末端回肠肠壁呈高信号。ADC图(G)显示病变ADC值为-1.26×10-3 mm2/s。H为末端回肠图片。
Fig. 1  31-year-old male patient with Crohn's disease in a moderate-severe, with a SES-CD of 7 and MaRIA of 12. A-E show the thickening of the intestinal wall of the terminal ileum (yellow arrow), T2WI and T2WI fat suppression (A-C) show intestinal wall edema, characterizing as linear high signal (red arrow), contrast-enhanced images (D, E) show the intestine the wall is obviously strengthened, and the intestinal wall edema not strengthened characterized as a linear low signal (E red arrow). F shows that the intestinal wall of the terminal ileum is hyperintensive in DWI with the ADC value of -1.26×10-3 mm2/s (G). H is the picture of the terminal ileum.
图2  箱型图显示ADC值在不同活动组间的差异性。
图3  ROC曲线分析显示,(图3A)当MaRIA为9.1,ADC值为-1.585×10-3 mm2/s时(A),区分缓解组与活动组的曲线下面积最大分别为0.962 (P<0.01)及0.957 (P<0.01),Delong分析显示两者曲线下面积无显著差别(Z=0.096,P=0.924)。当MaRIA为11.1时,ADC值为-1.345×10-3 mm2/s时(B),区分缓解-轻微活动组与中重活动组的曲线下面积最大分别为0.942 (P<0.01)及0.920 (P<0.01),Delong分析显示两者曲线下面积差异无统计学意义(Z=0.672,P=0.501)。
Fig. 2  Box plot shows the difference in ADC values among different activity groups.
Fig. 3  ROC curve analysis showed that when the MaRIA was 9.1 and the ADC value was -1.585×10-3 mm2/s (A), the area under the curve to distinguish the inactive from the active was 0.962 (P<0.01) and 0.957 (P<0.01), Delong analysis showed no significant difference in the area under the two curves (Z=0.096, P=0.924). When the MaRIA was 11.1 and the ADC value is -1.345×10-3 mm2/s (B), the area under the curve distinguishing the inactive-mild and the moderate- severe was 0.942 (P<0.01) and 0.920 (P<0.01), Delong analysis showed no significant difference in the area under the two curves (Z=0.672, P=0.501).

2.3 评估CD活动性的效能

       ROC曲线分析发现,当MaRIA为9.1时,区分缓解组与活动组的AUC最大为0.962 (P<0.01),敏感度为100%,特异度为85.9%;当ADC值为-1.585×10-3 mm2/s时,区分缓解组与活动组的AUC最大为0.957 (P<0.01),敏感度为100%,特异度为85.7%。MaRIA及ADC值区分缓解组与活动组的AUC差异无统计学意义(Z=0.096,P=0.924)。当MaRIA为11.1时,区分缓解-轻微活动组与中重活动组的AUC最大为0.942 (P<0.01),敏感度为86.7%,特异度为99.4%;ADC值为-1.345×10-3 mm2/s时,区分缓解-轻微活动组与中重活动组的AUC最大为0.920 (P<0.01),敏感度为85.0%,特异度为92.5%。MaRIA及ADC值区分缓解-轻微活动组与中重活动组的AUC差异无统计学意义(Z=0.672,P=0.501) (图3)。见表1

表1  MaRIA及ADC值区分CD不同活动期病变准确性比较
Tab. 1  Comparison of the accuracy of MaRIA and ADC values in distinguishing CD lesions in different active stages

3 讨论

       本研究结果显示ADC值、MaRIA与SES-CD均呈中等程度相关,ADC值与MaRIA均能准确区分CD病灶缓解组、轻微活动组及中重度活动组,且其准确度差异无统计学意义。两名医生测量ADC值的一致性均较好,结果可信度较高。

3.1 本研究的创新及临床应用价值

       首先,本研究以小肠镜为参考标准,将空肠与近段回肠病变纳入研究,结果更具可靠性。其次,在ADC值的测量方面,我们选取病变最突出的切面及相邻上下两个切面,共三个切面,沿着肠壁最亮信号区域的边界手动绘制ROI,计算三个层面ROI的平均值,可分析更多的像素,重复性及可信度更高[18]。最后,将ADC值区分不同活动期病灶的准确度与MaRIA进行比较,得出其准确度与MaRIA区分缓解组、轻微活动组及中重度活动组的准确度相似,进一步证实ADC值能准确区分CD不同活动期病灶。

       MaRIA的评分项目包括肠壁厚度、RCE及肠壁溃疡和水肿的表现。大量临床研究[3,8,19]证实MaRIA能准确评估CD病变活动性,预测CD患者治疗后反应,且该评分与CDEIS和SES-CD高度相关。但由于其计算烦琐、耗时,尚未用于临床。本研究中,MaRIA区分活动组与缓解组的阈值为9.1,区分中重度活动组的阈值为11.1。而Ordás等[7]研究显示区分活动组与缓解组的临界值为7.0,区分中重度活动组的临界值为11.0。其原因可能为DWI图像分辨率较低,部分缓解期病灶由于未在DWI图像上显示而被排除,导致缓解期肠段相对较少。

       MR-DWI作为唯一无创性评价活体内水分子自由扩散运动的成像方式,与MRE相比,具有成像速度快,无需进行肠道清洁及充盈,无需注射对比剂的优点。对于儿童或肾功能不全的患者,DWI是一种替代钆剂增强的有效检查方法[12,14,20]。本研究发现,ADC值与SES-CD呈显著负相关,区分活动组与缓解组的阈值为-1.585×10-3 mm2/s,AUC最大为0.957;区分中重度活动组的阈值为-1.345×10-3 mm2/s,AUC最大为0.920。最近,Wu等[11]以内镜为参考标准,仅评估末端回肠病变,其区分活动组与缓解组的阈值为-1.60×10-3 mm2/s,缓解组与中重度活动组的平均ADC值分别为-(1.42±0.12)×10-3 mm2/s和-(1.12±0.12)×10-3 mm2/s,其结果与本研究相近,但仍存在细微差别。其可能的原因为,Wu等[11]仅分析末端回肠病变,而本研究分段分析空回肠及结肠病变,样本选择存在差异。另外,扫描仪器、参数设置、ROI选取方式等也会影响结果。目前尚无确切的ADC阈值作为区分不同活动期病变的标准,但大量研究证实ADC值随CD病变活动性加重而显著降低[13,21, 22]

       在b值选取方面,Yoshio等[23]研究发现高b值(1500 s/mm2)背景信号抑制更好,在区分CD活动性病灶的准确度比800 s/mm2更好。但在研究中,我们仍采用腹部最常用的b值(800 s/mm2),因为高b值背景信号抑制强,可能存在漏诊轻微活动期病灶,而导致特异度高,而敏感度很低[24]

3.2 本研究的局限性

       尽管我们做了大量前期工作以提高结果的可靠性,但本研究中仍存在以下不足:首先,因为DWI图像信噪比较低,部分缓解期病灶在图像上未显示,而在内镜及MRE常规图像上显示出来,这部分被我们排除在外,而导致缓解期样本相对不足;其次,由于肠壁较薄,且部分中重度活动期病灶存在肠壁严重水肿,在测量过程中,不可避免地包含了肠腔内容及肠壁水肿成分;最后,本研究属于回顾性研究,在纳入标准上,由于部分确诊为CD的患者存在严重的肠腔狭窄,内镜无法通过,导致内镜资料不完整,而未纳入研究,存在潜在的选择偏倚。

       综上所述,DWI可定量区分CD不同活动期病灶,并具有较高的准确性,ADC值有望成为病变活动性分级的潜在生物标记物。

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