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局部进展期直肠癌新辅助放化疗后肿瘤退缩分级:MRI与病理对照研究
董龙春 李一鸣 孙超 包翠萍 杨筠 张明庆 杨正多 钟进

Cite this article as: Dong LC, Li YM, Sun C, et al. Tumor regression grade after neoadjuvant chemoradiotherapy for locally advanced rectal cancer: MRI and pathological control study[J]. Chin J Magn Reson Imaging, 2022, 13(9): 91-94, 103.本文引用格式:董龙春, 李一鸣, 孙超, 等. 局部进展期直肠癌新辅助放化疗后肿瘤退缩分级:MRI与病理对照研究[J]. 磁共振成像, 2022, 13(9): 91-94, 103. DOI:10.12015/issn.1674-8034.2022.09.017.


[摘要] 目的 探讨磁共振肿瘤退缩分级(magnetic resonance tumor regression grade, mrTRG)的诊断效能及影响因素。材料与方法 本研究回顾性分析2017年10月至2021年6月期间天津市人民医院肛肠诊疗中心收治的局部进展期中低位直肠癌患者病例129例。所有病例均行常规长程同步放化疗加根治性手术治疗,分别于同步放化疗前1周及结束后4周进行MRI扫描。以病理肿瘤退缩分级(pathologic tumor regression grade, pTRG)作为金标准,采用Kappa检验分析mrTRG的诊断效能。采用分层分析,评估不同MR因素[扩散加权成像(diffusion-weighted imaging, DWI)、T分期、T2WI高信号、直肠系膜筋膜(mesorectal fascia, MRF)侵犯阳性(MRF+)、壁外血管侵犯(extramural vascular invasion, EMVI)阳性(EMVI+)]对mrTRG诊断效能的影响。结果 单独采用T2WI进行评估,mrTRG 1~2级57例,3~5级72例。采用T2WI联合DWI进行评估,mrTRG 1~2级70例,3~5级59例。病理结果显示,pTRG 0~1级66例,2~3级63例。mrTRG与pTRG间一致性中等(单纯T2WI:Kappa=0.602,P<0.001;T2WI+DWI:Kappa=0.693,P<0.001)。与单纯T2WI相比,T2WI联合DWI提高了mrTRG的敏感度(86.4% vs. 82.9%)、特异度(83.9% vs. 77.1%)、阴性预测值(89.7% vs. 79.4%)、约登指数(70.3% vs. 60.0%)、总符合率(84.9% vs. 80.2%)。T分期高、T2WI高信号、MRF+、EMVI+使mrTRG的敏感度、特异度、阳性预测值、阴性预测值、约登指数、总符合率不同程度减低(T2WI高信号对mrTRG的敏感度影响除外)。结论 T2WI联合DWI能够提高mrTRG的诊断效能,新辅助放化疗前T分期高、T2WI高信号、MRF+、EMVI+会降低mrTRG评估的准确性。
[Abstract] Objective To investigate the diagnostic efficacy of magnetic resonance tumor regression grade (mrTRG) and affecting factors.Materials and Methods A retrospective study was conducted in 129 cases with locally advanced low rectal cancer admitted to the Anorectal Disease Diagnosis and Treatment Center of Tianjin Union Medical Center from October 2017 to June 2021. All patients received conventional long-term concurrent chemoradiotherapy and radical surgery. MRI scans were performed 1 week before and 4 weeks after the end of concurrent chemoradiotherapy. Using pathologic tumor regression grade (pTRG) as the gold standard, Kappa test was used to analyze the diagnostic efficacy of mrTRG. The effects of different MR factors [diffusion-weighted imaging (DWI), T staging, high signal intensity on T2WI, mesorectal fascia invasion positive (MRF+), extramural vascular invasion positive (EMVI+)] on the diagnostic efficacy of mrTRG were evaluated by stratified analysis.Results Using T2WI alone, 57 cases were mrTRG 1-2 and 72 cases were mrTRG 3-5. Using T2WI combined with DWI, 70 cases were mrTRG 1-2 and 59 cases were mrTRG 3-5. The pathological results showed that 66 cases were pTRG 0-1 and 63 cases were pTRG 2-3. mrTRG was moderately consistent with pTRG (T2WI alone: Kappa=0.602, P<0.001; T2WI+DWI: Kappa=0.693, P<0.001). Compared with T2WI, T2WI combined with DWI increased the sensitivity (86.4% vs. 82.9%), specificity (83.9% vs. 77.1%), negative predictive value (89.7% vs. 79.4%), Jorden index (70.3% vs. 60.0%) and total coincidence rate (84.9% vs. 80.2%) of mrTRG. High T stage, T2WI high signal intensity, MRF+ and EMVI+ reduced the sensitivity, specificity, positive predictive value, negative predictive value, Jordon index and total coincidence rate of mrTRG in varying degrees (except the effect of high T2WI signal on mrTRG sensitivity).Conclusions T2WI combined with DWI can improve the diagnostic efficiency of mrTRG. High T stage, T2WI high signal intensity, MRF+, EMVI+ before neoadjuvant chemoradiotherapy will reduce the accuracy of mrTRG assessment.
[关键词] 直肠癌;新辅助放化疗;肿瘤退缩分级;磁共振成像;弥散加权成像
[Keywords] rectal cancer;neoadjuvant chemoradiotherapy;tumor regression grade;magnetic resonance imaging;diffusion-weighted imaging

董龙春 1   李一鸣 1   孙超 1   包翠萍 1   杨筠 1   张明庆 2   杨正多 3   钟进 1*  

1 天津市人民医院影像科,天津 300010

2 天津市人民医院肛肠外科,天津 300010

3 天津市人民医院病理科,天津 300010

*钟进,E-mail:zhongjin20@sina.com

作者利益冲突声明:全体作者均声明无利益冲突。


基金项目: 天津市卫生健康委员会科技人才培育项目 KJ20124 天津市人民医院院级课题 2017YJ015,2018YJ007
收稿日期:2022-05-20
接受日期:2022-08-23
中图分类号:R445.2  R735.37 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.09.017
本文引用格式:董龙春, 李一鸣, 孙超, 等. 局部进展期直肠癌新辅助放化疗后肿瘤退缩分级:MRI与病理对照研究[J]. 磁共振成像, 2022, 13(9): 91-94, 103. DOI:10.12015/issn.1674-8034.2022.09.017

       近年来,直肠癌的发病率和死亡率均呈持续上升趋势,近一半的直肠癌患者确诊时已为局部进展期[1]。对于局部进展期直肠癌(locally advanced rectal cancer, LARC)患者,新辅助放化疗(neoadjuvant chemoradiotherapy, nCRT)联合全直肠系膜切除术已成为临床标准治疗策略。大量研究证实,nCRT可以增加保肛几率、提高R0切除率、降低局部复发率、延长无病生存期和总生存期[2, 3, 4, 5, 6]。而nCRT后准确的疗效评估直接决定了患者的后续治疗方案。NCCN指南[7]推荐高分辨MRI应作为直肠癌评估的主要检查手段,应常规用于直肠癌nCRT的疗效评估中。参考病理肿瘤退缩分级(pathologic tumor regression grade, pTRG)原则,Patel等[8]基于MRI上瘤床区域纤维化和残余存活肿瘤之间的比例,建立了MR肿瘤退缩分级(magnetic resonance tumour regression grade, mrTRG)系统,用以评估直肠癌nCRT疗效。当前,mrTRG越来越广泛地被应用于直肠癌nCRT后疗效量化评估中,尤其是对mrTRG 1级(代表病理完全缓解)的准确识别已成为近些年研究的热点。但这是一种基于T2加权成像(T2 weighted imaging, T2WI)的传统形态学评估方法,具有较强的主观性,易受到瘤床复杂病理变化(炎性反应、纤维化、黏液变性、水肿)的影响,导致特异性、可重复性不高[9]

       目前国际上针对该评分系统诊断效能的研究较少,研究结果不甚统一。肿瘤T分期、黏液成分(T2WI高信号)、直肠系膜筋膜(mesorectal fascia, MRF)状态、壁外血管侵犯(extramural vascular invasion, EMVI)是直肠癌术前MR评估的常用指标。这些MR指标对mrTRG有何影响,联合DWI能否提升mrTRG的诊断效能尚不清楚。因此,本研究旨在探讨mrTRG的诊断效能及影响因素。

1 材料与方法

1.1 研究对象

       本研究经过天津市人民医院学术伦理委员会批准,免除受试者知情同意,批准文号:2022B15。回顾性分析2017年10月至2021年6月期间天津市人民医院肛肠诊疗中心收治的局部进展期中低位直肠癌患者病例129例。病例纳入标准:(1)距肛门10 cm以内、经病理确诊的直肠腺癌;(2)术前MRI评估为局部进展期直肠癌(cT3~4和/或cN+);(3)完成常规长程新辅助同步放化疗;(4)心、肝、肾功能及凝血功能正常;(5)放化疗完成后接受根治性手术。病例排除标准:(1)MR图像存在较为严重伪影;(2)治疗前及治疗过程中影像学检查发现肝、肺等远处转移。

1.2 nCRT方案

       129例患者均行常规长程同步放化疗。采用三维适形放疗技术,照射野包括肿瘤或瘤床及其周围2~5 cm的安全边缘、直肠系膜区、髂内和闭孔血管淋巴引流区和骶前区。T4期肿瘤侵犯前方结构时(男性前列腺或女性阴道)需照射髂外血管淋巴引流区。照射剂量DT 45.0~50.4 Gy,单次剂量1.8~2.0 Gy,共25~28次。放疗期间同步进行化疗,化疗方案为口服卡培他滨825 mg/m2,每天两次。放疗结束后6~12周行根治性手术。

1.3 MRI检查时间及序列

       使用Siemens Skyra 3.0 T MRI扫描仪(西门子,德国)、18通道体部线圈进行MRI检查。所有病例均于同步放化疗前1周及结束后4周进行MRI检查。扫描序列包括常规T1WI(横轴位)、高分辨率T2WI (矢状位、斜轴位、斜冠状位)和DWI(斜轴位,b值0、1000s/mm2)。具体扫描参数见表1

表1  磁共振检查序列及参数

1.4 肿瘤退缩分级

       参考国家卫生健康委员会中国结直肠癌诊疗规范(2020年版),将pTRG分为0~3级[10],参考MERCURY小组的研究将mrTRG分为1~5级[8],具体见表2。mrTRG评分的关键在于识别残余肿瘤,残余肿瘤在T2WI图上表现为中等信号,在DWI图(b=1000 s/mm2)上表现为高信号,而在ADC图上则出现相应的低信号。所有MRI图像均由两名具有5年以上胃肠影像学诊断经验的影像医师进行两次评估。首次评估仅观察高分辨T2WI序列图像,1个月后,观察高分辨T2WI序列联合DWI图评估mrTRG分级。对于意见不一致的病例,由两名观察者相互协商后形成统一的mrTRG分级。

表2  肿瘤退缩分级

1.5 统计学分析

       应用SPSS 22.0软件进行统计学分析。以pTRG作为金标准,采用二分类法(mrTRG 1~2对应pTRG 0~1,代表应答良好;mrTRG 3~5对应pTRG 2~3,代表应答较差)计算mrTRG的敏感度、特异度、阳性预测值、阴性预测值、约登指数、总符合率。采用Kappa检验(二分类法)分析mrTRG与pTRG结果的一致性(Kappa≤0.40表明一致性较差,0.40<Kappa<0.75表明一致性中等,Kappa≥0.75表明一致性较好)。采用分层分析,评估不同因素(DWI、T分期、T2WI高信号、MRF+、EMVI+)对mrTRG评分准确性的影响。P<0.05表示差异具有统计学意义。

2 结果

2.1 患者基本特征

       入组患者年龄为(57.9±10.4)岁。肿瘤长径(5.1±1.5)cm,肿瘤下极与肛缘平均距离(4.9±2.2)cm,其他信息见表3

表3  人口学及影像学一般特征

2.2 mrTRG与pTRG评估结果

       单独采用T2WI序列进行评估,mrTRG 1~2级57例,3~5级72例。采用T2WI联合DWI序列进行评估,mrTRG 1~2级70例,3~5级59例。病理评估结果显示,pTRG 0~1级66例,pTRG 2~3级63例。mrTRG与pTRG间总体一致性中等(单纯T2WI:Kappa=0.602,P<0.001;T2WI+DWI:Kappa=0.693,P<0.001)。与单纯应用T2WI序列相比,T2WI联合DWI提高了mrTRG的敏感度(86.4% vs. 82.9%)、特异度(83.9% vs. 77.1%)、阴性预测值(89.7% vs. 79.4%)、约登指数(70.3% vs. 60.0%)、总符合率(84.9% vs. 80.2%)(图1)。因此,下文中评估不同因素对mrTRG诊断效能的影响选用mrTRG(T2WI+DWI)。

图1  男,62 岁,直肠中分化腺癌。1A~1F 为初诊MR图像,分别为矢状位、斜冠状位和斜轴位T2WI、斜轴位DWI 及ADC图,示直肠下段癌(红箭),MR分期为T3c(MRF-,EMVI-)。1G~1K为新辅助放化疗后复查MR图像,示肿瘤体积明显减小,肿瘤于T2WI 序列主体为低信号(图1G~1I 红箭),代表纤维化,右侧壁局限性T2WI 高信号被认为是黏液变性(图1H、1I 白箭),在没有联合DWI 的情况下mrTRG评分为1 级;图1J、1K示右侧壁9 点位可见局限性弥散受限区域(红箭),提示肿瘤残余可能,因此联合DWI 后mrTRG评分为2 级。术后病理证实pTRG1 级。DWI:扩散加权成像;ADC:表观扩散系数;MRF:直肠系膜筋膜;EMVI:壁外血管侵犯;mrTRG:MR肿瘤退缩分级。

2.3 nCRT前不同因素对mrTRG诊断效能的影响

       分层分析结果显示,mrTRG的敏感度、特异度、阳性预测值、阴性预测值、约登指数、总符合率随着T分期升高而减低。T2WI高信号、MRF+、EMVI+使mrTRG的敏感度、特异度、阳性预测值、阴性预测值、约登指数、总符合率不同程度减低(T2WI高信号对敏感度的影响除外),具体见表4

表4  不同因素对mrTRG诊断效能的影响

3 讨论

       本研究探讨了不同MR指标(有无DWI、T分期、T2WI高信号、MRF+、EMVI+)对mrTRG评分准确性的影响。研究结果显示,与单纯应用T2WI相比,T2WI联合DWI能够提升mrTRG的诊断效能,DWI应作为常规扫描序列应用于直肠癌nCRT后的疗效评估中。nCRT前T分期高、T2WI高信号、MRF+、EMVI+是mrTRG的干扰因素,会降低评估的准确性。

3.1 DWI提升mrTRG的诊断效能

       直肠癌nCRT后,瘤床区域病理变化复杂,包括炎性反应、纤维化、黏液变性、水肿等,于T2WI图像表现为混杂信号,难以区分,这就决定了基于T2WI的mrTRG评估存在很多不确定性[11]。反应良好的患者中,肿瘤坏死纤维化,主要表现为T2WI序列信号降低,但纤维化内仍可能存在少量肿瘤,常规T2WI序列无法准确分辨。

       DWI能反映组织结构微观水平的变化,能够对残余肿瘤活性进行评估。残余肿瘤在DWI图中表现为高信号,在纤维瘢痕低信号背景中更容易发现。既往大量研究发现DWI可提高mrTRG的观察者间一致性和准确性[12, 13, 14, 15]。而且,通过测量ADC值,能定量评估肿瘤的病理变化,预测直肠癌nCRT的疗效,尤其对病理完全缓解具有较高的预测价值[16, 17, 18, 19, 20]。本研究结果显示,T2WI联合DWI可提高mrTRG与pTRG间的总体一致性。与单纯应用T2WI相比,T2WI联合DWI显著提高了mrTRG的敏感度、特异度、阴性预测值、约登指数、总符合率,与上述研究相符。DWI能够提升mrTRG的诊断效能,推荐作为直肠癌nCRT后MR检查的常规扫描序列。

3.2 nCRT前T分期、T2WI高信号、MRF+、EMVI+对mrTRG的影响

       nCRT前T分期高、黏液成分(T2WI高信号)、MRF+、EMVI+是直肠癌不良预后的危险因素[2,21, 22, 23, 24, 25]。而这些因素对mrTRG的评估是否存在影响还不甚清楚。本研究结果显示,在采用T2WI联合DWI进行图像评估的条件下,T分期高、T2WI高信号、MRF+、EMVI+使mrTRG的准确性降低。且mrTRG的敏感度、特异度、阳性预测值、阴性预测值、约登指数、总符合率随着T分期升高而减低。

       T分期高、MRF+、EMVI+提示肿瘤体积负荷较大、壁外浸润深度大。由于肿瘤本身存在异质性,肿瘤体积越大,往往提示nCRT后出现复杂病理变化的可能性就越大,影像鉴别肿瘤残余的难度随之增加。尤其是nCRT后肿瘤内部及周边出现反应性炎症,尽管联合DWI,亦很难与残余肿瘤鉴别,导致mrTRG准确性下降。如果将残余肿瘤误诊为急性炎症,可能延误患者的治疗。相反,如果将急性炎症误诊为残余肿瘤,可能导致过度治疗。而T2WI高信号代表肿瘤内部含有黏液成分。黏液区域由于T2WI透过效应可在DWI图中可表现为高信号,这时需结合ADC图加以鉴别。残余肿瘤于ADC图表现为低信号,而黏液区域表现为高信号。

3.3 局限性及展望

       本研究存在一定的局限性。首先,肿瘤退缩为动态变化过程,单个时间点的评估无法反映和代表肿瘤的全部变化,采用跟踪扫描的方式或许能够带来更为准确的诊断结果。其次,患者性别、年龄、生活方式、肿瘤病理类型、淋巴结状态、基因类型、是否合并其他疾病等因素均可能会影响肿瘤对放化疗的反应及疗效评估,本研究未进行一一评价。以影像组学和深度学习为代表的人工智能可利用海量影像数据,在肿瘤诊断和疗效评估方面具有广阔应用前景[26, 27, 28, 29, 30, 31]。利用人工智能评价局部进展期直肠癌nCRT后疗效是我们的下一步研究方向。

       综上,本研究结果表明,DWI联合T2WI能够提高mrTRG的诊断效能,而T分期高、T2WI高信号、MRF+、EMVI+使mrTRG的诊断准确性降低,对于这类患者在实际工作中要更为细心、谨慎。研究结论对临床实践具有较高的指导价值,能有效降低因疗效评估不当造成治疗决策失误的发生率。

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