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临床研究
3.0 T动态对比增强MRI联合扩散加权成像在鉴别唾液腺多形性腺瘤和基底细胞腺瘤中的诊断价值
李森 邵硕 闫小凡 吴建伟 赵晓萌 郑宁

Cite this article as: LI S, SHAO S, YAN X F, et al. The diagnostic value of 3.0 T DCE-MRI combined with DWI in differentiating pleomorphic adenoma and basal cell adenoma of salivary gland[J]. Chin J Magn Reson Imaging, 2023, 14(4): 34-40.本文引用格式:李森, 邵硕, 闫小凡, 等. 3.0 T动态对比增强MRI联合扩散加权成像在鉴别唾液腺多形性腺瘤和基底细胞腺瘤中的诊断价值[J]. 磁共振成像, 2023, 14(4): 34-40. DOI:10.12015/issn.1674-8034.2023.04.007.


[摘要] 目的 探讨动态对比增强MRI(dynamic contrast-enhanced MRI, DCE-MRI)联合扩散加权成像(diffusion weighted imaging, DWI)鉴别唾液腺多形性腺瘤(pleomorphic adenoma, PA)和基底细胞腺瘤(basal cell adenoma, BCA)的价值。材料与方法 回顾性分析2018年12月至2022年8月济宁市第一人民医院经病理证实的唾液腺肿瘤患者病例55例,其中PA 38例,BCA 17例,从影像归档和通信系统收集所有患者的MRI影像资料,对比分析两肿瘤的时间-信号强度曲线(time intensity curve, TIC)类型、定量参数[转运常数(volume transfer constant, Ktrans)、渗出速率常数(the rate constant, Kep)、血管外细胞外容积分数(fractional volume of the extravascular-extracellular space, Ve)、血浆分数(plasma fraction, Vp)]、表观扩散系数(apparent diffusion coefficient, ADC)值。通过受试者工作特征(receiver operating characteristic, ROC)曲线评估DCE-MRI联合DWI对PA和BCA的鉴别能力。结果 PA的平均ADC值为(1.74±0.36)×10-3 mm2/s,高于BCA[(1.32±0.13)×10-3 mm2/s],差异有统计学意义(P<0.05)。17例BCA的TIC中B型5例、C型11例,38例PA 的TIC中A型27例、C型10例。DCE-MRI定量参数中,PA的Kep值小于BCA,而Ve值大于BCA,P均<0.05。PA和BCA的组间Ktrans和Vp值差异无统计学意义。ADC值、TIC、Kep值和Ve值的曲线下面积(area under the curve, AUC)值分别为0.875、0.808、0.822和0.747,多参数联合的AUC值为0.895~0.952。结论 TIC、Kep值、Ve值、ADC值均有助于鉴别唾液腺BCA与PA,多参数联合进一步提高了其诊断效能。
[Abstract] Objective To investigate the value of dynamic contrast-enhanced MRI (DCE-MRI) combined with diffusion-weighted imaging (DWI) in the differential diagnosis of salivary gland pleomorphic adenoma (PA) and basal cell adenoma (BCA).Materials and Methods Retrospective analysis of 55 cases with salivary gland tumors confirmed by pathology in Jining First People 's Hospital from December 2018 to August 2022, including 38 cases of PA and 17 cases of BCA. MRI data of all patients were collected and analyzed from picture archiving and communication system. The PA and BCA were compared and analyzed in time intensity curve (TIC) types, quantitative parameters [volume transfer constant (Ktrans), the rate constant (Kep), fractional volume of the extravascular-extracellular space (Ve), plasma fraction (Vp)] and apparent diffusion coefficient (ADC) value. Rreceiver operating characteristic (ROC) curve was used to evaluate the efficiency of DCE-MRI combined with DWI in distinguishing PA and BCA.Results The mean ADC value of PA [(1.74±0.36)×10-3 mm2/s] was higher than that of BCA [(1.32±0.13)×10-3 mm2/s], and the difference was statistically significant (P<0.05). There were 5 cases of type B and 11 cases of type C in TIC of 17 cases of BCA, and 27 cases of type A, 10 cases of type C in 38 cases of PA. The Kep value of PA was lower than that of BCA and the Ve value of PA was higher than that of BCA (P<0.05 ) in the quantitative parameters of DCE-MRI. There was no significant difference in Ktrans and Vp values between PA and BCA groups. The area under the curve (AUC) of ADC, TIC, Kep and Ve were 0.875, 0.808, 0.822 and 0.747, respectively. And the AUC of multi-parameter combination was 0.895-0.952.Conclusions TIC, Kep, Ve and ADC are all helpful to differentiate BCA and PA in salivary gland, and the combination of multiple parameters further improves its diagnostic efficiency.
[关键词] 唾液腺肿瘤;多形性腺瘤;基底细胞腺瘤;动态对比增强;磁共振成像;扩散加权成像;定量参数
[Keywords] salivary gland tumors;pleomorphic adenoma;basal cell adenoma;dynamic contrast-enhanced;magnetic resonance imagining;diffusion weighted imaging;quantitative parameter

李森 1   邵硕 2   闫小凡 1   吴建伟 3   赵晓萌 3   郑宁 2*  

1 山东第一医科大学(山东省医学科学院),济南 250000

2 济宁市第一人民医院磁共振室,济宁 272000

3 济宁医学院临床医学院,济宁 272013

通信作者:郑宁,E-mail:zhengning_369@163.com

作者贡献声明:郑宁设计本研究的方案,对稿件重要的智力内容进行了修改,获得了济宁市重点研发计划项目基金的资助;李森起草和撰写稿件,获取、分析或解释本研究的数据;邵硕、闫小凡、吴建伟、赵晓萌获取、分析或解释本研究的数据,对稿件重要的智力内容进行了修改;全体作者都同意发表最后的修改稿,同意对本研究的所有方面负责,确保本研究的准确性和诚信。


基金项目: 济宁市重点研发计划项目 2021YXNS022
收稿日期:2022-11-25
接受日期:2023-04-11
中图分类号:R445.2  R739.87 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.04.007
本文引用格式:李森, 邵硕, 闫小凡, 等. 3.0 T动态对比增强MRI联合扩散加权成像在鉴别唾液腺多形性腺瘤和基底细胞腺瘤中的诊断价值[J]. 磁共振成像, 2023, 14(4): 34-40. DOI:10.12015/issn.1674-8034.2023.04.007.

0 前言

       多形性腺瘤(pleomorphic adenoma, PA)约占唾液腺肿瘤的三分之二,是发病率最高的唾液腺肿瘤,好发于中青年女性[1],其组织学上由唾液腺组织、软骨样组织及黏液等构成[2]。基底细胞腺瘤(basal cell adenoma, BCA)是第三常见的良性唾液腺肿瘤,女性较男性多见[3],其主要由基底样细胞构成,但不含黏液软骨样间质,在病理学上根据不同生长模式分为梁状型、实体型、管状型和膜性型四种亚型,以梁状型和管状型多见[4, 5]。PA有复发、恶变倾向,临床多选择根治性切除术[6];而BCA预后较PA好,术后不易复发,临床上仅需选择部分腺叶切除术或单纯瘤体切除术即可[7],因此术前准确定性PA和BCA对临床手术方案的制订具有指导意义。基于MRI影像学表现(如病变形态、大小、边缘、信号特点、有无囊变及强化方式等)鉴别PA和BCA在实际工作中易受医师主观判断及经验影响受到限制[8]。细针穿刺活检细胞学检查不能获得全部肿瘤信息且有一定的假阴性率(4%~7%),有时并不能提供决定性结果,且细针穿刺属于有创检查[9, 10]。扩散加权成像(diffusion weighted imaging, DWI)是一种应用广泛的无创功能成像技术,动态对比增强MRI(dynamic contrast-enhanced MRI, DCE-MRI)可以反映肿瘤的血管分布,能通过定量分析参数提供通透性相关和肿瘤灌注方面信息[11]。国内外已有应用DCE-MRI、DWI、影像组学等方法用于鉴别唾液腺良恶性肿瘤的研究,本研究应用DCE-MRI定量参数联合DWI鉴别PA和BCA,在国内外文献中鲜有报道[12, 13]

1 材料与方法

1.1 研究对象

       回顾性分析2018年12月至2022年8月济宁市第一人民医院唾液腺肿瘤患者病例55例,所有患者均经术后病理证实,其中PA 38例(腮腺30例,下颌下腺8例),BCA 17例(腮腺16例,下颌下腺1例)。纳入标准:(1)术前均行常规 MRI、DWI以及DCE-MRI检查,并由同一台MRI机器采用相同参数扫描;(2)检查前未经细针穿刺抽吸细胞学检查等有创检查及治疗;(3)肿瘤内具有足够的非囊变、坏死区域;(4)所有肿瘤均经病理证实为PA和BCA。排除标准:(1)图像存在明显的运动伪影或图像变形,影响数据采集;(2)病灶实性部分感兴趣区(region of interset, ROI)范围<0.3 cm2,难以精准勾画病灶实性部分。本研究遵守《赫尔辛基宣言》,并经济宁市第一人民医院伦理委员会批准[批准文号:2022伦审研第(110)号],免除受试者知情同意。

1.2 仪器与方法

       采用荷兰Philips Ingenia 3.0 T MR扫描仪,多通道头颈部专用线圈。(1)常规平扫MRI序列:T1WI轴状位(TE 6.9,TR 508),T1WI冠状位(TE 12,TR 494),T2WI轴状位(TE 85,TR 2064),T2WI冠状位(TE 62,TR 2317)。(2)DWI序列:TR 3386 ms,TE 64 ms,b值为0、800 s/mm2,FOV 200 mm×200 mm。(3)DCE-MRI序列:TR 16 ms,TE 3.4 ms,FOV 240 mm×180 mm,矩阵192×144,采用Gd-DTPA经肘静脉注射,剂量0.2 mmol/kg,注射流率2.5 mL/s,并加注20 mL生理盐水。共15个动态时相,扫描时间447 s。

1.3 图像后处理

1.3.1 DWI

       首先,将所有患者的DWI原始图像传至Philips后处理软件高级扩散分析,由两名影像科医生分别进行测量,软件将自动获得表观扩散系数(apparent diffusion coefficient, ADC)图,选取DWI(b=800)图像,手动勾画ROI,在肿瘤最大层面选取肿瘤实性成分,对比T2WI及DCE-MRI避开肿瘤囊变、出血区域,获取ADC值,测量三次取平均值。

1.3.2 DCE-MRI

       将已获取全部患者的DCE-MRI原始图像并传至Philips MR permeability软件,后处理软件自动生成时间-信号强度曲线(time intensity curve, TIC),TIC的分型采用YABUUCHL等[14]提出的4个类型,具体为:达峰时间>120 s定义为 A型;达峰时间≤120 s、流出率≥30%定义为 B型;达峰时间≤120 s、流出率<30%定义为C型;病变无强化或囊性病变定义为D型。DCE-MRI定量分析选取pre35原始图像作为参考底图,选取肿瘤侧颈内动脉,手动勾画ROI获取动脉输入函数,对比常规MRI平片手动勾画ROI,因部分容积效应勾画时避开肿瘤边缘,软件自动生成转运常数(volume transfer constant, Ktrans)、渗出速率常数(the rate constant, Kep)、血管外细胞外容积分数(fractional volume of the extravascular-extracellular space, Ve)、血浆分数(plasma fraction, Vp)伪彩图及其数值,测量三次取平均值。

1.4 统计学方法

       使用SPSS 26.0软件进行本研究全部数据的统计分析。采用Shapiro-Wilk法判断数据是否满足正态分布,采用Leneve检验判断方差齐性。正态分布数据采用t检验分析PA和BCA的年龄、ADC值及定量参数的组间差异;非正态分布或非方差齐性数据采用Mann-Whitney U检验。采用卡方检验比较PA和BCA之间性别组成、TIC曲线类型组间差异,通过绘制受试者工作特征(receiver operating characteristic, ROC)曲线分析计算相应曲线下面积(area under the curve, AUC)评价DCE-MRI定量参数及联合ADC模型对PA和BCA的诊断效能,通过最大约登指数(最大约登指数=敏感度+特异度-1)确定诊断阈值,P<0.05表示差异具有统计学意义。组内相关系数(intra-class correlation coefficient, ICC)用来评价两位医师间测得的BCA与PA平均ADC值及DCE-MRI定量参数结果的可重复性。

2 结果

2.1 PA和BCA患者的临床资料与常规影像学表现

       PA和BCA患者的年龄、性别比例差异具有统计学意义(P<0.05)(表1)。常规MRI表现示PA实性部分T1WI多呈等信号,T2WI呈不均匀高信号(图1A1B)。BCA实性成分T1WI呈等信号,T2WI呈稍高信号或稍低信号(图2A2B),大部分PA及BCA周边可见T2WI低信号包膜影,71%(12/17)BCA病灶出现囊变坏死区,呈片状、裂隙状。

图1  女,41岁,右腮腺多形性腺瘤。1A:横断位T1WI示右侧腮腺类圆形等信号影;1B:T2WI呈稍高信号,边界清晰,周围可见线样T2WI低信号包膜影;1C:ADC值为1.51×10-3 mm2;1D:TIC示病变为A型曲线;1E~1F:DCE-MRI定量参数伪彩图示Kep=244.64×10-3/min,Ve=564.66×10-3。ADC为表观扩散系数;TIC为时间-信号强度曲线;DCE-MRI为动态对比增强MRI;Kep为渗出速率常数;Ve为血管外细胞外容积分数。
Fig. 1  Female, 41 years old, right parotid gland tumor. 1A: Transverse T1WI shows round equal signal shadow of right parotid gland; 1B: T2WI shows slightly higher signal, clear boundary, visible line-like T2WI low signal envelope around; 1C: Apparent diffusion coefficient (ADC) value is 1.51×10-3 mm2; 1D: Time intensity curve (TIC) shows type A curve; 1E-1F: Dynamic contrast-enhanced MRI (DCE-MRI) quantitative parameters pseudo-color map shows the rate constant (Kep) is 244.64×10-3/min, fractional volume of the extravascular-extracellular space (Ve) is 564.66×10-3.
图2  女,55岁,左腮腺基底细胞腺瘤。2A:横断位T1WI示左侧腮腺类圆形稍低信号;2B:T2WI呈稍高信号,边界清晰,周围可见线样T2WI低信号包膜影;2C:ADC值为1.39×10-3 mm2;2D:TIC示病变为B型曲线;2E~2F:DCE-MRI定量参数伪彩图示Kep=662.45×10-3/min,Ve=238.44×10-3。ADC为表观扩散系数;TIC为时间-信号强度曲线;DCE-MRI为动态对比增强MRI;Kep为渗出速率常数;Ve为血管外细胞外容积分数。
Fig. 2  Female, 55 years old, left parotid gland tumor. 2A: Transverse T1WI shows round slightly low signal of left parotid gland; 2B: T2WI shows slightly higher signal, clear boundary, visible line-like T2WI low signal envelope around; 2C: Apparent diffusion coefficient (ADC) value is 1.39×10-3 mm2; 2D: Time intensity curve (TIC) shows type B curve; 2E~2F: Dynamic contrast-enhanced MRI (DCE-MRI) quantitative parameters pseudo-color map shows the rate constant (Kep) is 662.45×10-3/min, fractional volume of the extravascular-extracellular space (Ve) is 238.44×10-3.
表1  PA与BCA的临床特征比较
Tab. 1  Comparison of clinical features between PA and BCA

2.2 PA和BCA的DWI衍生的ADC值

       PA与BCA的ADC值分别为(1.74±0.36)×10-3 mm2/s、(1.32±0.13)×10-3 mm2/s,差异具有统计学意义(P<0.05)(图1C2C)。ROC曲线分析显示,当ADC的阈值为1.46×10-3 mm2/s时,其鉴别PA与BCA的敏感度、特异度分别为78%、88%,AUC=0.875(表23图3)。

图3  Kep、Ve、ADC、TIC及它们之间的联合模型对PA和BCA的诊断价值。Kep为渗出速率常数;Ve为血管外细胞外容积分数;ADC为表观扩散系数;TIC为时间-信号强度曲线;ROC为受试者工作特征曲线;PA为多形性腺瘤;BCA为基底细胞腺瘤。
Fig. 3  Diagnostic value of Kep, Ve, ADC, TIC and their combination for PA and BCA. Kep: the rate constant; Ve: fractional volume of the extravascular-extracellular space; ADC: apparent diffusion coefficient; TIC: time intensity curve; ROC: receiver operating characteristic;PA: pleomorphic adenoma; BCA: basal cell adenoma.
表2  DCE-MRI定量参数和DWI参数比较
Tab. 2  Comparison of DCE-MRI quantitative parameters and DWI parameters
表3  Kep、Ve、ADC、TIC及它们的联合模型对PA和BCA的鉴别
Tab. 3  Identification of PA and BCA by Kep, Ve, ADC, TIC and their combination

2.3 PA和BCA的DCE-MRI表现

       PA以A型曲线为主,BCA以C型曲线为主(图1D2D),差异具有统计学意义(P<0.05)。PA和BCA的Kep、Ve值差异具有统计学意义(P<0.05),Ktrans、Vp值差异无统计学意义(P>0.05)(图1E1F2E2F表12)。

2.4 各参数联合对PA和BCA的诊断效能

       各参数两两联合模型中以TIC_Ve的效能最优;四者联合模型TIC_Kep_ADC_Ve的效能在所有联合模型中效能最高(AUC=0.952)。DeLong检验结果表明,除Kep_ADC模型外,大多数两者联合模型较单独模型差异具有统计学意义,四者联合模型较单独模型差异均有统计学意义,而四者联合模型较两者联合模型差异均无统计学意义(P>0.05;表34图3)。

表4  DeLong检验结果
Tab. 4  Results of the DeLong test

2.5 组间一致性

       组间一致性检验结果表明,DCE-MRI、DWI的多参数测量具有较好的一致性(表5)。

表5  DCE-MRI定量、DWI参数的ICC检验
Tab. 5  ICC test of quantitative and DWI parameters of DCE-MRI

3 讨论

       本研究中BCA女性患者发病率明显高于PA,闫小凡等[15]研究发现,BCA对比PA女性较多见,约是男性发病率的2倍,本研究与之相符;刘红生等[16]研究发现PA发病年龄较BCA跨度大,本研究中PA年龄跨度也较BCA大(PA:16~71岁,BCA:34~70),与其结果相符,可能的原因是PA较BCA其发病部位较深,其肿瘤发现时间相对较晚,所以PA发病年龄跨度较大[17]。PA与BCA影像学表现与其病理结构有关,PA组织构成多样,不同成分所含自由水不同,所以T2WI常为不均匀高信号[18, 19];BCA中,T2WI信号强度与细胞间质多少呈负相关,因此实体型与管状型T2WI为较低信号,而梁状型与膜状型为等或稍低信号[20, 21]

3.1 DWI对PA和BCA的鉴别意义

       DWI及其衍生出来的ADC值与水分子的随机运动有关,ADC值可定量的反映肿瘤细胞密度相关信息[22, 23],现已广泛应用于唾液腺肿瘤的诊断中。本研究中PA的平均ADC值大于BCA的平均ADC值(P<0.05),阈值为1.46×10-3 mm2/s,能较好地对两者进行鉴别诊断,这与程景风等[24]研究结果相符,考虑是因为BCA细胞密集程度较PA高,而PA含有大量的黏液组织间质和软骨样间质,细胞外间隙较BCA大,因此BCA的ADC值低于PA。

3.2 DCE-MRI对PA和BCA的鉴别意义

       DCE-MRI通过注射对比剂可以模拟血流通过肿瘤的血流动力学过程,较病理活检可以无创地获得与肿瘤血管分布和灌注及微循环相关信息[25, 26]。本研究中PA的TIC曲线以A型为主(71%),PA早期强化缓慢与PA内血管较稀疏,含有大量黏液样间质及软骨基质有关,而当PA中以细胞为主时则表现为C型[27]。本研究中BCA的TIC曲线以C型为主,可能与BCA中间质含量较低,廓清较快有关。Ktrans值与单位体积内的血流量、血管通透性及血管表面积有关[28],Kep代表单位时间内由血管外细胞细胞间隙进入血管内的对比剂量,Ktrans和Kep都与血管通透性和灌注有关,反应肿瘤内新生血管程度[29]。本研究中PA和BCA组间Ktrans值差异无统计学意义,说明两者微血管分布、血管通透性差异不大,而PA的Kep值小于BCA,差异有统计学意义,说明对比剂流出血管后BCA有更多的对比剂反流,可能与BCA内缺乏黏液软骨、间质纤维化明显及大量由毛细血管及静脉组成的血管网有关[30, 31],也可能与PA新生血管较少、血流速度低、强化较BCA慢,对比剂易滞留在间质而廓清缓慢有关。Ve代表单位体内血管外细胞间隙的体积,Ktrans、Kep和Ve值三者间存在以下关系:Kep=Ktrans/Ve[32, 33]。PA和BCA都易发生囊变,本研究中BCA的Ve值小于PA,说明BCA的细胞外间隙更小,细胞密集程度较PA高,这可能是因为BCA由含有排列整齐的基底细胞层和基底膜样结构的同形基底细胞样构成,细胞间质内含有大量的内皮血管[34],而PA结构较之稀疏。

3.3 MRI参数联合应用对PA和BCA的鉴别意义

       本研究将定量参数Kep、Ve及TIC、ADC值联合鉴别PA和BCA的准确率为89%,AUC值为0.952,较单独使用各参数具有更高的诊断效能差异。XU等[35]研究发现TIC和Ve的联合应用在区分腮腺肿瘤类型中效能最高(AUC=0.75),其中也包括了鉴别PA和以BCA为主的其他良性肿瘤,在我们的研究中,TIC和Ve的联合应用也表现出了较高的诊断效能(AUC=0.916),与XU等研究不同的是,本研究中Kep、Ve、TIC及ADC值四者的联合应用进一步提高了其诊断效能,这可能是由于多参数的联合应用能够反映出区别两种肿瘤更多的生物学信息。总之,DCE-MRI定量参数、TIC可以反映肿瘤内微血管分布、血管通透性及微循环相关信息,DWI能够评估肿瘤水分子扩散受限的程度,反映肿瘤的异质性[36, 37],将两技术联合使用对PA和BCA进行鉴别诊断,能更全面地反映肿瘤内部信息,对术前诊断有较高的临床价值。

3.4 局限性

       本研究存在以下局限性:(1)本研究样本量较少,诊断准确性可能会被高估,今后将进一步扩充样本量来分析其诊断效能;(2)本研究对PA与BCA进行研究,今后将进一步增加其他类型唾液腺的鉴别诊断;(3)人工勾画ROI有一定主观性,获取的定量参数可能会存在一定的误差。

4 结论

       综上所述,磁共振的参数Kep、Ve、TIC及ADC可以鉴别唾液腺PA和BCA,且多参数的联合应用可以进一步提高诊断效能。

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