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临床研究
T2 mapping预测直肠癌脉管侵犯的初步研究
李茜玮 刘爱连 陈安良 董宛 沈智威 宋清伟

Cite this article as: Li XW, Liu AL, Chen AL, et al. Preliminary study on the value of T2 mapping in predicting lymphovascular invasion of rectal cancer[J]. Chin J Magn Reson Imaging, 2022, 13(6): 23-27.本文引用格式:李茜玮, 刘爱连, 陈安良, 等. T2 mapping预测直肠癌脉管侵犯的初步研究[J]. 磁共振成像, 2022, 13(6): 23-27. DOI:10.12015/issn.1674-8034.2022.06.005.


[摘要] 目的 探讨T2 mapping定量参数预测直肠癌脉管侵犯(lymphovascular invasion,LVI)的价值。材料与方法 回顾性分析2019年10月至2021年11月于大连医科大学附属第一医院行3.0 T MRI扫描的34例直肠癌患者资料,分为LVI组(A组) 13例与非LVI组(B组) 21例。扫描序列包括T1WI、T2WI、扩散加权成像及T2 mapping等。结合以上序列图像定位病灶,并由2名观察者于T2 mapping图像显示肠壁最厚层面放置三个感兴趣区(region of interest,ROI)测量T2值。采用Bland-Altman曲线检验2名观察者测量值的一致性。根据数据符合正态性分布与否,采用独立样本t检验或Mann-Whitney U检验比较两组T2值的差异。结果 2名观察者测量的T2值一致性良好,表现为Bland-Altman图中的点均匀分布在+1.96至-1.96倍标准线差内。A组和B组的T2值分别为(77.15±6.95) ms、(87.06±7.55) ms,A组低于B组,差异具有统计学意义(P<0.05);T2值预测直肠癌LVI的曲线下面积、阈值、敏感度及特异度分别为0.861、83.19 ms、84.62%及76.19%。结论 T2 mapping在预测LVI方面具有较好的价值。
[Abstract] Objective To investigate the value of T2 mapping quantitative parameters in predicting lymphovascular invasion (LVI) and non-LVI of rectal cancer.Materials and methods A retrospective analysis of 34 cases with rectal cancer who underwent 3.0 T MRI scans in the First Affiliated Hospital of Dalian Medical University from October 2019 to November 2021 was divided into a LVI group (group A) of 13 cases and a non-LVI group (group B) of 21 cases. Scanning sequences include T1WI, T2WI, diffusion weighted imaging (DWI), and T2 mapping. Combined with the above sequence images, the lesions were located, and two observers placed three region of interest (ROIs) to measure the T2 value on the largest slice of the lesion displayed on the T2 mapping image. A Bland-Altman curve was used to test the agreement of the 2 observers' measurements. According to whether the data conformed to the normal distribution or not, independent samples t-test or Mann-Whitney U test was used to compare the difference of T2 value between rectal cancer group A and group B.Results T2 mapping parameters measured by the two observers were in consistent, and most of the scattered points in the Bland-Altman graph were evenly distributed between the +1.96 and -1.96 standard lines. The T2 values ​​of group A and group B were (77.15±6.95) ms and (87.06±7.55) ms, respectively. Group A was lower than group B, and the difference was statistically significant (P<0.05); the area under the curve (AUC), threshold, sensitivity and specificity of T2 value in predicting LVI were 0.861, 83.19 ms, 84.62% and 76.19%, respectively.Conclusions T2 mapping has high value in predicting LVI of rectal cancer.
[关键词] 直肠癌;脉管侵犯;磁共振成像;T2 mapping成像;预测;鉴别;定量
[Keywords] rectal cancer;lymphovascular invasion;magnetic resonance imaging;T2 mapping;prediction;distinguish;quantification

李茜玮 1, 2   刘爱连 1, 2*   陈安良 1, 2   董宛 1, 2   沈智威 3   宋清伟 1, 2  

1 大连医科大学附属第一医院放射科,大连 116011

2 大连市医学影像人工智能工程技术研究中心,大连 116011

3 飞利浦医疗临床科学部,北京 100016

刘爱连,E-mail:cjr.liuailian@vip.163.com

作者利益冲突声明:全体作者均声明无利益冲突。


收稿日期:2022-02-21
接受日期:2022-05-27
中图分类号:R445.2  R735.37 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.06.005
本文引用格式:李茜玮, 刘爱连, 陈安良, 等. T2 mapping预测直肠癌脉管侵犯的初步研究[J]. 磁共振成像, 2022, 13(6): 23-27. DOI:10.12015/issn.1674-8034.2022.06.005

       直肠癌在我国发病率逐年增高,是降低我国居民生活质量的恶性肿瘤之一[1, 2]。直肠癌脉管侵犯(lymphovascular invasion,LVI)为血管和(或)淋巴管侵犯,是直肠癌早期侵袭性的表现,为直肠癌患者预后的独立危险因素之一[3]。临床诊断直肠癌LVI的金标准为术后病理检查,但其为一项有创性检查[4],且会因病理取材部位不同而影响病理结果的准确性。因此寻找术前无创且准确预测LVI的方法,对于临床指导直肠癌患者具有参考意义。

       MRI是一种无创性检查直肠癌的必要手段[5]。近年来,高分辨MRI通过形态学征象可用于评估管径较大的LVI,但对于诊断部分早期直肠癌患者管径较小的LVI及肿瘤分期敏感度低[6, 7]。T2 mapping作为一种MRI定量成像技术,能够对组织水分和胶原纤维含量及组成进行量化来对疾病进行评估[5]。既往研究发现,T2 mapping技术对于鉴别直肠管状腺癌及非管状腺癌、非黏液性直肠癌周围淋巴结的良恶性均具有较好的价值,能很好地反映病灶自由水的含量[8, 9]。但尚无学者利用T2 mapping技术定量预测直肠癌LVI的价值。本研究旨在利用T2 mapping技术来预测直肠癌LVI,以期为诊断直肠癌LVI提供一定分子层面信息。

1 材料与方法

1.1 患者资料

       本研究经过大连医科大学附属第一医院医学伦理委员会批准,免除受试者知情同意,批准文号:PJ-KS-KY-2019-49。回顾性分析2019年10月至2021年11月大连医科大学附属第一医院因临床诊断为直肠癌行3.0 T MRI检查(包括T2 mapping序列)的患者资料。入组标准:(1)术后病理结果证实为直肠癌,包括管状腺癌29例,黏液腺癌1例,混合性癌(同时包含任意两种及两种以上病理类型) 4例;(2)患者MRI检查前均未行手术及相关放化疗、免疫治疗、靶向治疗。排除标准:(1)病灶过小(最大径小于3 mm),难以勾画感兴趣区(region of interest,ROI);(2)临床或病理资料不完整;(3)合并直肠其他疾病。最终入组患者共34例,根据病理结果将入组患者分为LVI组(A组)与非LVI组(B组)。最终入组:A组13例,男7例,女6例,年龄27~83 (61.69±16.05)岁;B组21例,男17例,女4例,年龄37~74 (62.76±10.14)岁。

1.2 检查设备及方法

       所有入组患者均行盆腔3.0 T MRI扫描(IngeniaCX,Philips,Holand),扫描前嘱患者排空肠管,禁食水4~6 h。训练患者呼吸,避免扫描过程中产生较大伪影降低图像质量。采用32通道腹部扫描线圈。扫描时采取仰卧位,两侧髂前上棘连线与扫描床中心垂直。扫描序列包括T2 mapping、扩散加权成像(diffusion weighted imaging,DWI)及常规T1WI、T2WI序列,具体扫描参数可见表1

表1  扫描序列参数
Tab. 1  Scan sequence parameters

1.3 临床及病理资料

       记录患者的临床及病理资料:排便习惯改变、便血、腹部包块、CA-199、癌胚抗原(carcinoma embryonic antigen,CEA)、分化程度、生长方式、病理类型、神经侵犯、肿瘤沉积、T分期、N分期及M分期。

1.4 图像处理与数据测量

       将T2 mapping图像传至ISP (IntelliSpacePortall,Philips Healthcare)工作站,以DWI图像作为参考,寻找DWI (b=1200 mm2/s)为高信号的肠壁最厚层面,避开囊变、出血及肠气区,由2名观察者(1年、7年以上MRI读片经验)在未知病理的情况下分别放置3个ROI进行病灶勾画,并将各ROI对应到T2 mapping图像中,取3个ROI的平均T2值进行后续分析(图12)。

图1  男,61岁,直肠癌脉管侵犯。1A、1B:DWI (1A)及T2 mapping (1B)示直肠癌病灶,DWI表现为直肠左侧壁突向腔内不规则高信号肿块,T2 mapping表现为左侧壁突向腔内不规则稍高信号肿块,DWI及T2 mapping图像可见三个ROI,T2 mapping图像测得三个ROI的T2值分别为68.97 ms、64.28 ms及65.34 ms,三个ROI的平均T2值为66.20 ms。1C:镜下显示脉管侵犯(箭;HE ×200)。
图2  男,67岁,直肠癌脉管非侵犯。2A、2B:DWI (2A)及T2 mapping (2B)示直肠癌病灶,DWI表现为环壁高信号,T2 mapping表现为环壁等低信号,DWI及T2 mapping图像可见三个ROI,T2 mapping测得三个ROI的T2值分别为74.36 ms、77.97 ms及79.76 ms,三个ROI的平均T2值为77.36 ms。2C:镜下显示脉管未侵犯(箭;HE ×200)。注:DWI:扩散加权成像;ROI:感兴趣区。
Fig. 1  A 61-year-old man with lymphovascular invasion of rectal cancer. 1A, 1B: DWI (1A) and T2 mapping (1B) showed rectal cancer lesions. DWI showed an irregular high-intensity mass protruding from the left rectal wall into the cavity, and T2 mapping showed an irregular slightly high-intensity mass protruding from the left wall into the cavity. DWI and T2 mapping images showed three ROIs. The T2 values of the three ROIs were 68.97 ms, 64.28 ms, and 65.34 ms, respectively, and the average T2 value of the three ROIs was 66.20 ms. 1C: Microscopically showing lymphovascular invasion (arrows, HE ×200).
Fig. 2  A 67-year-old man with non-lymphovascular invasion rectal cancer vessels. 2A, 2B: DWI (2A) and T2 mapping (2B) showed rectal cancer lesions. DWI showed high signal in the ring wall, DWI showed low signal in the ring wall. DWI and T2 mapping images showed three ROIs. The T2 values of the three ROIs measured by T2 mapping were 74.36 ms, 77.97 ms, and 79.76 ms, respectively, and the average T2 value of the three ROIs was 77.36 ms. 2C: Microscopically showing non-lymphovascular invasion (arrows, HE ×200). Note: DWI: diffusion weighted imaging; ROI: region of interest.

1.5 统计学分析

       使用SPSS 23.0及MedCalc 18.2.1进行统计学分析。采用Bland-Altman图评估2名观察者T2值测量的一致性,比较散点在1.96倍标准差线内分布情况,若大部分散点均匀分布在+1.96 SD至-1.96 SD线内则代表一致性好。若一致性良好采取两者T2值的平均值进行后续分析,采用Shapiro-Wilk检验数据的正态性,符合正态性分布的数据,使用独立样本t检验,表示为均值±标准差;非正态性分布的数据,使用Mann-Whitney U检验,表示为中位数(25%分位数,75%分位数)。采用ROC曲线分析T2值预测直肠癌LVI的效能,并记录T2值鉴别两组的AUC值、敏感度、特异度及阈值。采用Fisher确切概率法分析与预测直肠癌LVI相关临床及病理因素。

2 结果

2.1 临床一般资料

       A组及B组的临床病理资料见表2。研究结果发现:A组发生神经侵犯概率高于B组,两组差异具有统计学意义(P<0.01);余临床与病理学资料对于区分两组差异无统计学意义。

表2  直肠癌脉管侵犯组与非侵犯组临床一般资料分析
Tab. 2  Analysis of general clinical data of rectal cancer lymphovascular invasion group and non-lymphovascular invasion group

2.2 观察者间测量值一致性分析

       A组及B组两组数据均符合正态分布。两名观察者对A组及B组测量值的一致性良好,表现为Bland-Altman曲线图中的散点均匀分布在+1.96SD与-1.96SD线之间(图3)。

图3  Bland-Altman图评价2名医师T2测量值的一致性。
Fig. 3  Bland-Altman plot to evaluate the consistency of T2 measurements between two physicians.

2.3 两组T2值的差异性分析及诊断效能

       两组T2值的差异性分析方法可见图45。A组T2值为(77.15±6.95) ms,B组T2值为(87.06±7.55) ms,A组小于B组,差异具有统计学意义[P<0.05,t=-3.826,95% CI:(-15.180,-4.632)] (图4)。T2值预测A组与B组AUC值为0.861,敏感度、特异度及阈值分别为84.62%、76.19%及83.19 ms(图5)。

图4  T2 mapping预测直肠癌脉管侵犯组(A组)与非侵犯组(B组)的箱式图。
Fig. 4  Box plot of T2 mapping predicting rectal cancer lymphovascular invasion group (group A) and non-lymphovascular invasion group (group B).
图5  T2值预测直肠癌脉管侵犯ROC曲线图。
Fig 5  ROC curve of T2 value predicting lymphovascular invasion of rectal cancer.

3 讨论

       本研究利用T2 mapping成像技术可定量分析组织细胞水含量的特点术前预测直肠癌LVI的价值。研究发现T2值在术前预测直肠癌LVI方面具有很好的潜力,且既往研究示T2 mapping成像虽已用于部分胃肠道疾病的诊断[6, 7],但尚无研究利用将该序列术前预测直肠癌LVI,因此本研究可从分子层面为直肠癌LVI提供一定的诊断信息。

3.1 LVI的概念及临床意义

       LVI指直肠癌细胞存在于邻近淋巴管及血管内[10, 11],美国癌症联合委员会(The American Joint Committee on Cancer,AJCC)在第8版修订中将LVI细化为小脉管侵犯及静脉侵犯,小脉管侵犯指淋巴管及小静脉的侵犯,即在肿瘤灶中发现血管壁或其残留成分;静脉侵犯指肿瘤细胞侵犯血管内皮包绕成分,如红细胞及平滑肌细胞等[12]。有研究表明,直肠癌发生LVI的概率高达94%[10]。目前,LVI被广泛认为是直肠癌的重要转移风险,Compton等[13]已将其与病理评估肿瘤范围、术前CEA水平、切缘阳性、区域淋巴结转移共同列为直肠癌进展的重要特征。LVI的准确诊断有助于对直肠癌患者制订合理的治疗方案[14]。有研究表明,直肠癌LVI患者发生淋巴结转移的风险高于非LVI患者,且患者预后更差[15],并且LVI患者术后复发及发生转移的几率较非LVI患者增高[16]。因此,准确识别直肠癌LVI对于直肠癌早期转移的诊断及治疗具有十分重要的作用。

3.2 T2 mapping预测直肠癌LVI价值评估

       MRI已用于直肠癌LVI临床诊断中,谢玉海等[17]研究发现利用定量参数表观扩散系数(apparent diffusion coefficient,ADC)及动态对比增强磁共振成像(dynamic contrast enhancement magnetic resonance imaging,DCE-MRI)的正性增强积分(positive enhanced intensity,PEI)能有效预测直肠癌LVI。但是DWI的空间分辨率低,病灶边界多显示不清,因此利用DWI序列诊断病变的准确性可存在一定误差;DCE需要注射对比剂,且DCE成像参数缺乏标准化的统一,使得预测直肠癌LVI的价值有限[17, 18]。此外,Li等[19]利用IVIM定量参数评估直肠黏液腺癌壁外静脉侵犯的价值,研究发现虽然D值对于鉴别二者有一定的差异,但诊断效能较低,为0.646。综上,需要寻找精准且简便的评估直肠癌LVI的方法。

       T2 mapping作为一种定量成像技术,具有客观性、良好的稳定性及可重复性等特点,目前已广泛应用于骨关节、心肌、前列腺癌与脑肿瘤方面[20, 21, 22, 23]。T2值作为组织的定量参数之一,通过评估病变组织的横向弛豫时间可反映组织内部的特征。本研究结果示LVI组的T2值显著低于非LVI组。由于T2值反映的是组织内部体素水平上水分子的含量特征[24, 25],因此推测其原因可能为:与非LVI组相比较,LVI组单位体积内肿瘤细胞的数量增加,导致细胞间隙水分子的含量减少;并且由于肿瘤细胞细胞核增大,核浆比失调,致使肿瘤细胞内含水量减少[26]。肿瘤细胞内外水分子的减少均造成LVI组T2值减小。此外,在既往胃肠道相关研究中,Zhang等[8]研究了T2值在鉴别管状腺癌与非管状腺癌方面的价值,发现非管状腺癌的T2值明显低于管状腺癌,诊断效能达到0.999,敏感度及特异度分别达到100%及97%。Ge等[9]研究了T2值对于直肠癌周围淋巴结的定性诊断的价值,发现恶性淋巴结中结合水含量增高,而炎性淋巴结含有更多的游离水,因此恶性淋巴结节的T2值显著低于良性淋巴结。据我们所知,本研究初次探索了T2值预测直肠癌LVI的价值,以期为直肠癌LVI的诊断提供分子层面信息。

3.3 局限性

       本项研究也存在一定的局限性:(1)本研究样本量较少,有待后续扩大样本深入研究;(2)本研究于肿瘤最大层面勾画ROI,未对肿瘤全域进行分析,不能全面反映肿瘤的异质性,后续研究有待逐层勾画病灶ROI进行研究;(3)研究结果示神经侵犯对于鉴别直肠癌LVI具有统计学意义,本研究未验证直肠癌神经侵犯因素对于T2值的影响,有待进一步探索。

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