常规MRI与弥散加权成像测量的肿瘤容积对直肠癌TN分期的诊断价值

胡友强，陈晨，陈勇，解超莲，李勇，曾南林，陈天武，张小明

常规MRI与弥散加权成像测量的肿瘤容积对直肠癌TN分期的诊断价值

胡友强，陈晨，陈勇，解超莲，李勇，曾南林，陈天武，张小明*

目的探讨常规MRI与弥散加权成像(DWI)测量的肿瘤容积对直肠癌TN分期的诊断价值。材料与方法对经肠镜确诊的74例直肠癌患者行盆腔3.0 T MRI检查。分析MRI对直肠癌术前TN分期的准确性，用Kappa检验评价MRI术前TN分期与病理分期的一致性。用单因素方差分析评价DWI (b=1000 s/mm2) 测量的肿瘤容积与病理TN分期的相关性。结果MRI诊断直肠癌T、N分期的准确率分别为87.8% (66/74)、66.2% (49/74)；病理学和MRI对T分期诊断有较好的一致性(Kappa=0.78，P=0.000)、对N分期诊断一致性较差(Kappa=0.33，P=0.000)。在DWI上测量肿瘤容积≤T2期、T3期、T4期分别为 (4145.13±718.00) mm3、(14939.73±3591.38) mm3、(22714.76±4251.71) mm3；N0期、N1期、N2期分别为(14367.15±6425.83) mm3、(17967.69±5259.88) mm3、(19464.00±3588.77) mm3。DWI测肿瘤容积越大直肠癌T分期越高，差异有统计学意义 (F=75.189，P=0.000)；肿瘤容积与直肠癌不同N分期间差异有统计学意义(F=3.545，P=0.034)。结论MRI评价直肠癌T分期准确率较高，对N分期也有一定诊断价值。MR肿瘤容积测量对直肠癌TN分期有重要参考价值。

直肠肿瘤；腺癌；磁共振成像；弥散加权成像；肿瘤容积；分期

结直肠癌是常见的恶性肿瘤之一，发病率在所有肿瘤中占第三位，其中直肠癌占50%～70%[1]。目前，直肠癌的主要治疗手段为外科手术治疗结合相应阶段的辅助放化疗，而手术治疗仍是其主要治疗方法，全直肠系膜切除术(total mesorectal excision，TME)成为直肠癌外科手术的金标准[2]。直肠癌术前分期是选择治疗方案的必要条件，在直肠癌术前评估的基础上，不同分期可选择相应的治疗方案，因此准确的术前分期对选择治疗方式、判断预后情况都有一定的指导意义[3]。目前，临床上用于诊断直肠癌的主要方法包括结直肠镜、钡剂灌肠、CT 、MRI。虽然结直肠镜、钡灌肠能确诊直肠癌，但是这些腔内技术无法观察肿瘤大小、浸润范围及淋巴结转移。与CT相比，MRI无放射线辐射、有卓越的软组织分辨率、可提供功能成像及进行多平面成像，尤其是薄层高分辨率 MRI的应用，它能更好地显示直肠肠壁的各层结构和直肠系膜筋膜，分期准确性较高[4-5]。MRI也能评价新辅助化疗疗效及诊断局部肿瘤复发情况[6-7]，有文献报道，在MR图像上测量直肠癌容积可较好地评价直肠癌新辅助化疗(neoadjuvant chemotherapy，NACT) 及后续化疗反应情况[8-9]。但有关肿瘤容积与直肠癌T分期相关性的研究尚未见报道。笔者通过常规磁共振成像序列对直肠癌进行术前TN分期的同时，进一步研究DWI测量的肿瘤容积与直肠癌TN分期的相关性，为临床医师提供更多治疗依据。

1 材料与方法

1.1 一般资料

本研究获得川北医学院附属医院伦理委员会批准，所有病例均签署知情同意书。2014年9月至2016年2月期间在我院收治74例未行术前放化疗且经肠镜确诊的直肠腺癌患者行盆腔3.0 T MRI检查。入组标准：MRI检查前经肠镜确诊为直肠腺癌；MRI检查前未行放化疗；检查后1周内行TME并成功获得病理TN分期结果；有完整MRI资料且图像清晰可辨；无MRI禁忌证(如心脏起搏器、神经刺激器、动脉瘤夹、胰岛素泵、人工耳蜗等)。74例有完整影像及临床资料患者入选本组实验，其中男48例，女26例，年龄38～84岁，平均为61.5岁。

1.2 MRI检查技术

使用美国GE公司的DV 750 3.0 T超导性磁共振成像扫描仪，32通道相控阵表面线圈。患者采用足先进方式，对所有患者行常规MRI及多b值DWI检查。所有患者检查前均未做清洁胃肠道准备。检查前15～20 min肌内注射山莨菪碱注射液 (654-2) 20 mg，以减少肠蠕动。行TSE T1WI横断面、TSE T2WI横断面、T2WI SPAIR横断面 (FOV 360 mm ×360 mm，矩阵：384×384，层厚6 mm)。TSE T2WI矢状面 (FOV 160 mm×160 mm，矩阵384×384，层厚4 mm)；小FOV T2WI横断面(FOV 240 mm×240 mm，矩阵360×224，层厚4 mm)；DWI横断面(FOV 380 mm×380 mm，矩阵160×192，层厚4 mm，b=0、100、300、500、800、1000、1500 s/mm2)。

1.3 图像分析及统计分析

根据美国癌症联合会(AJCC)直肠癌TNM分期系统标准[10]，T分期标准：T1肿瘤侵及黏膜及黏膜下层；T2肿瘤侵及肠壁固有肌层；T3肿瘤侵及肌层穿入浆膜下，或侵及无腹膜覆盖的肠旁组织；T4肿瘤穿透腹膜脏层或者直接侵犯或粘连于周围器官或结构。N分期标准：N0无淋巴结转移； N1有1～3枚淋巴结转移；N2有4枚以上淋巴结转移。由于T1与T2期直肠癌在MRI上难以分辨， 临床治疗方法也相似， 因此本研究将两期合并为≤T2期进行研究。

由2名有5年以上MRI诊断经验的医师对盆腔MR图像进行分析判断，并作出TN分期，分析的图像资料包括T1WI、T2WI、DWI。对有异议的结果则由2名医师讨论取得一致意见后作为最终结果。2名医师除已知肠镜确诊为直肠腺癌外，未知病变大小、位置及术后病理结果等其他信息。常规序列中若淋巴结短径≥0.6 cm、形态不规整则视为转移[11]；高b值DWI 上为明显高信号，且形态不规整则视为转移淋巴结。在轴面DWI (b=1000 s/mm2)上，2名MRI医师勾画出不规则的肿瘤感兴趣区面积，然后与层厚(0.4 cm)相乘，如此逐层测量，最后相加得出肿瘤容积。直到2名医师测量值相差10%以内，则计算平均值作为最终结果。

表1 直肠癌MRI T分期与病理T分期结果对照Tab. 1 The comparison between pathologic and MRI tumor T staging

表2 直肠癌MRI N分期与病理N分期结果对照Tab. 2 The comparison between pathologic and MRI tumor N staging

表3 直肠癌不同T分期的DWI肿瘤容积比较Tab. 3 The comparison of diffusion-weighted MR tumor volumetry between pathologic T stage

表4 直肠癌不同N分期的DWI肿瘤容积比较Tab. 4 The comparison of diffusion-weighted MR tumor volumetry between pathologic N stage

1.4 统计学方法

运用SPSS 17.0软件进行数据分析。2名观察者之间的一致性及MRI TN分期与病理TN分期的一致性采用Kappa检验，Kappa≤0.40时，表明一致性较差；0.40＜Kappa≤0.60时，表明中度一致；0.60＜Kappa≤0.80时，表明有较高一致性；Kappa＞0.80时，表明有很好的一致性。应用单因素方差分析评价肿瘤容积与直肠癌T分期、N分期的相关性。P＜0.05认为差异有统计学意义。

2 结果

2.1 病理结果

74例患者MRI检查后2周内均完成手术，术中切除原发肿瘤，远切缘术中冰冻及病理切片报告均为阴性。病理T分期：≤T2期8例、T3期49例、T4期17例；N0期52例，N1期16例，N2期6例。

2.2 直肠癌MRI TN分期与术后病理TN分期结果比较

2名医师对直肠癌T分期结果一致性为Kappa=0.82 (P＜0.001)。直肠癌T分期MRI的诊断准确率为87.8%(66/74)，过高分期5例，2例T2期误诊为T3期，3例T3期误诊为T4期，过低分期4例均为T4期误诊为T3期。病理学和MRI对直肠癌T分期诊断二者一致性较好(表1)。2名医师对直肠癌N分期结果一致性为Kappa=0.79 (P＜0.001)。N分期的诊断准确率为66.2% (49/74)，过高分期17例，其中有7例N0期误诊为N2期，5例N0期误诊为N1期，5例N2期误诊为N1期，过低分期8例，6例N1期误诊为N0期，1例N2期误诊为N0期，1例N2期期误诊为N1期。病理学和MRI对N分期诊断一致性较差(表2)。典型MR图像见图1～4。

2.3 DWI直肠癌容积与术后T、N分期的相关性

2名医师在DWI上测量的肿瘤容积的结果一致性为Kappa=0.78(P＜0.001)。在DWI上所测量的≤T2期、T3期、T4期肿瘤容积分别为(4145.13±718.00) mm3、(14939.73±3591.38) mm3、(22714.76±4251.71) mm3；N0期、N1期、N2期肿瘤容积分别为(14367.15±6425.83) mm3、(17967.69± 5259.88) mm3、(19464.00±3588.77) mm3。直肠癌DWI测量肿瘤容积越大其T分期越高，差异有显著统计学意义(P=0.000)(表3)。不同N分期与肿瘤容积间差异有统计学意义(P=0.034)(表4)。典型MR图像见图5。

3 讨论

MRI是目前结直肠癌分期的重要检查方法，在对肿瘤定位、判断肿瘤浸润深度、决定切除范围方面，准确度较高[12]。相关研究结果提示，应用相控阵线圈高分辨MRI显示直肠癌T分期总的诊断准确率分别为85.7%(36/42)和89.5%(85/95)[13-14]，与本研究综合常规MRI及DWI显示T分期总体准确率87.8%(66/74)基本一致。本研究中T2期误诊为T3期主要MRI表现为肿瘤周围脂肪间隙欠清晰，可见条索状长T2异常信号影。有报道表明判断直肠癌T分期最主要的困难在于T2期与T3期的鉴别，由于肿瘤周围纤维化、炎症、感染或血管病变会对T2、T3期的诊断造成影响[15-16]。T3期误诊为T4期主要MRI表现为肿瘤周围脂肪间隙不清，其内可见片状异常信号影并与临近盆壁及肌肉分界不清。分析原因多为感染、炎症范围较大致肠壁与周围结构产生类似肿瘤浸润征象。T3期误诊为T4期MRI表现为肿瘤浸润范围较广，与邻近充盈欠佳的膀胱壁或肛提肌分界不清，似有受侵。但病理结果显示均未侵及邻近器官，可能因肿瘤生长，推挤压迫邻近组织，使局部分界不清。MRI对临界期肿瘤的T分期的诊断存在一定的难度，而在实际工作中， 联合观察轴位、矢状位、冠状位图像对于减少直肠癌分期错误有一定的帮助[15]。

图1 A为T2期直肠腺癌轴面DWI，显示后壁不均匀增厚，外缘光整，周围脂肪间隙尚清；B为同一患者不同层面轴面T2WI图2 A为T3期直肠腺癌轴位DWI，显示右前壁明显不均匀增厚，肿瘤累及肌层及周围脂肪组织，外缘部分呈结节状隆起；B为同一患者轴面T2WI图3 A为T4期直肠腺癌轴面DWI，显示肠壁广泛增厚，穿透腹膜脏层，脂肪间隙不清，周围见结节状、条片状高信号影，并累及双侧盆壁筋膜，B为同一患者不同层面轴面T2WI图4 A为直肠腺癌轴面DWI，显示直肠右后方1枚肿大淋巴结, 边界清，DWI上明显高信号，病理学显示淋巴结为增生性反应，B为同一患者不同层面轴面T2WI图5 患者男，61岁，病理证实为T3期直肠腺癌，A～D为DWI (b=1000 s/mm2)，显示沿肿瘤边缘手动勾画肿瘤面积，最后计算出肿瘤容积Fig. 1 A is axial DWI of a patient with T2 staging of rectal adenocarcinoma. It displays the back wall is thick and the edges became smooth and clear (arrow represents the location of rectal adenocarcinoma). B is axial T2WI of the same patient with 1A.Fig. 2 A is axial DWI of a patient with T3 staging of rectal adenocarcinoma. It displays the right front wall is obvious uneven thicking (arrow represents the location of rectal adenocarcinoma). B is axial T2WI of the same patient with 2A.Fig. 3 A is axial DWI of a patient with T4 staging of rectal adenocarcinoma. It displays the rectal wall is extensive thicking (arrow represents the location of rectal adenocarcinoma). B is axial T2WI of the same patient with 3A.Fig. 4 A is axial DWI of a patient with rectal adenocarcinoma. It displays a pelvic lymph node with high signal behind the rectum,but pathology shows that lymph nodes are proliferative (arrow represents the location of lymph node). B is axial T2WI of the same patient with A.Fig. 5 A 61-year-old male patient, and the pathology conf i rmed the stage is T3. A—D: Tumor area is manually drawn along margin of tumor, and value of this area on axial DWI (b=1000 s/mm2), then calculate the tumor volume.

MRI诊断淋巴结转移的符合率差别较大，但大多数文献报道其诊断符合率为50%～70%[17]，与本研究结果基本一致。本研究过高分期病例MRI上显示直肠周围、肠系膜间多发淋巴结肿大影，DWI上呈高信号，但边缘较规则，多数淋巴直径大于1.0 cm。但病理学显示淋巴结反应性增生，不含有肿瘤细胞，原因可能是直肠癌导致淋巴结炎性增大。Brown等[18]报道，在同一直肠癌标本中转移性淋巴结与炎性增大淋巴结经常难以区分。误诊为N0期的7例患者中有6例MRI上未发现淋巴结影，仅1例患者病变肠旁可见小淋巴结显示，直径小于0.5 cm，信号较均匀。但病理结果显示淋巴结内有肿瘤细胞。Monig等[19]通过132枚转移淋巴结研究发现，53%转移淋巴结直径小于0.5 cm，应用0.5 cm 作为鉴别良、恶性淋巴结的阈值仅仅具有中等度的敏感性和特异性。事实上，较小的转移淋巴结非常普遍，有研究发现在MRI上小于0.5 cm的淋巴结15%属于转移淋巴结，没有淋巴结大小的限制可以排除转移淋巴结[16]。因此，基于淋巴结大小的标准，MRI对直肠癌术前淋巴结淋巴结转移的诊断准确性较低[19-22]。结合本组病例术中所见发现，多发小淋巴结位于与肠壁融合的区域，MRI上难以辨别。通过形态学观察鉴别转移淋巴结因主观性太大，不同观察者间差异较大导致可靠性低，而利用超微型超顺磁性氧化铁颗粒(USPIO)增强扫描，则可提高转移淋巴结检出的特异性[23]。但国内USPIO尚用于实验阶段。

直肠癌的研究表明DWI可以提高病变的检出，在T2WI的基础上运用DWI对直肠癌的诊断敏感性从82%～84%提高到93%～95%[24]。Curvo-Semedo等[25]报道，应用DWI和T2WI测量的肿瘤容积有较好的一致性，但在DWI上测量的容积较T2WI测量值稍小，鉴于DWI应用越来越广泛，可能成为制定放疗计划和GTV勾画的重要参考[26]。而在高b值的DWI上，直肠癌呈高信号，病变显示较好，故本研究选择b值为1000 s/mm2DWI图像测量肿瘤容积。相关文献报道，通过MR肿瘤容积测量区别直肠癌新辅助化疗反应好坏与组织病理学对比一致性达68%～78%[8-9，27]，表明 MRI肿瘤容积测量是评价直肠癌术前NACT及后续化疗的较好方法。但目前对于测量肿瘤容积与直肠癌T分期相关性的研究尚未见报道。笔者发现直肠癌DWI上测量容积越大其T分期越高，其原因可能是随肿瘤容积的增大，浸润直肠壁的深度随之增加，故T分期越高。因此在观察肿瘤浸润深度显示欠清或不确切时，可通过测量肿瘤容积，对直肠癌进行T分期诊断。对于直肠癌N分期的MRI研究，多集中在淋巴结大小、形态、DWI信号、强化程度及ADC值等方面，本研究通过测量直肠癌原发肿块大小，探讨其与N分期的相关性，期望为临床治疗提供更多依据。研究发现DWI上测量肿瘤容积越大，其N分期越高。其发生机制可能是，原发肿瘤体积越大，血供越丰富，肿瘤细胞通过直接浸润淋巴管或经细胞外间隙渗入淋巴管而发生淋巴结转移的数量也越多[28]。多个研究表明，口咽癌、舌癌、食管鳞状上皮细胞癌在CT或MRI上测量肿瘤容积大小可以帮助预测淋巴结转移[29-31]，与本研究在直肠癌上基本一致。肿瘤容积大小对直肠癌TN分期的诊断可以作出良好的补充。

本研究存在一些不足之处，可能使数据统计结果出现偏倚。首先，本研究病例偏少，分期、分组不均；其次，2名医师的经验也会影响TN分期的准确性；最后，虽然肿瘤容积的测量要求2名医师测量值相差10%以内，但仍不能完全反映肿瘤真实容积。

综上所述，常规MRI联合DWI检查能够较准确地诊断直肠癌TN分期，但是对于直肠癌转移淋巴结的鉴别不够准确。DWI肿瘤容积测量对直肠癌TN分期的诊断有良好的参考价值，可协助临床提供较合理的治疗方案。在对直肠癌进行术前分期时，推荐结合测量肿瘤容积大小。

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Value of magnetic resonance imaging combined with diffusionweighted MR tumor volumetry in the diagnosis of TN staging for rectal cancer

HU You-qiang, CHEN Chen, CHEN Yong, XIE Chao-lian, LI Yong, ZENG Nan-lin, CHEN Tian-wu, ZHANG Xiao-ming*
Sichuan Key Laboratory of Medical Imaging and Department of Radiology, Aff i liated Hospital, North Sichuan Medical College, Nanchong 637000, China
*Correspondence to: Zhang XM, E-mail: cjr.zhxm@vip.163.com

Objective:To investigate the value of magnetic resonance imaging (MRI) in the diagnosis of preoperative TN staging for rectal cancer and the correlation between diffusion-weighted MR tumor volumetry and TN staging.Materials and Methods:Between September 2014 and February 2016, 74 patients with histologically proven rectal cancer by the colonoscopic biopsy in our hospital was performed by pelvic 3.0 T MRI. We analyzed the preoperative MRI TN staging of rectal cancer diagnosis accuracy. Concordance between MRI TN staging of tumor and pathologic reporting was assessed by means of theKappastatistic. The correlation between diffusion-weighted MR tumor volumetry and TN staging was analyzed byone-wayanalysis of variance.Results:The accurate rate for T-staging of rectal cancer using MRI was 87.8% (66/74). There was a good correlation between pathologic and MRI tumor staging (Kappa=0.78,P=0.000). The accurate rate for N-staging of rectal cancer using MRI was 66.2% (49/74). There was a poor correlation between pathologic and MRI tumor staging (Kappa=0.33,P=0.000). The tumor volume of rectal cancer at DWI in ≤T2, T3and T4 staging rectal cancer was (4145.13±718.00) mm3, (14939.73±3591.38) mm3and (22714.76±4251.71) mm3. The tumor volume of rectal cancer at DWI in N0, N1 and N2 staging was (14367.15±6425.83) mm3,(17967.69±5259.88) mm3and (19464.00±3588.77) mm3. The greater of the tumor volume, the higher of the T-staging of rectal cancer, and the discrepancies were statistically different (F=75.189,P=0.000). The discrepancies between tumor volume and N-stagings of rectal cancer were statistically different (F=3.545,P=0.034).Conclusions:MRI has a good concordance with pathologic T-staging of rectal cancer, and has a certain clinical value in the N-staging. DWI tumor volumetry contributes a lot to diagnosis of TN-staging of rectal cancer.

Rectal neoplasms; Adenocarcinoma; Magnetic resonance imaging; Diffusion-weighted imaging; Tumor volume; Staging

国家卫生和计划生育委员会公益性行业科研专项基金(编号：201402019)

川北医学院附属医院放射科 医学影像四川省重点实验室，南充 637000

张小明，E-mail：cjr.zhxm@vip.163. com

2016-09-26

接受日期：2017-01-06

R445.2；R735.37

A

10.12015/issn.1674-8034.2017.03.010

胡友强, 陈晨, 陈勇, 等. 常规MRI与弥散加权成像测量的肿瘤容积对直肠癌TN分期的诊断价值. 磁共振成像, 2017, 8(3): 214-219.

Received 26 Sep 2016, Accepted 6 Jan 2017

ACKNOWLEDGMENTSThis article was supported by the National Health and Family Planning Commission public welfare industry research under special funding (No. 201402019).