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临床研究
3D酰胺质子转移成像与体素内不相干运动成像对前列腺癌的诊断价值研究
侯国瑞 王晨 李磊磊 林港 李奕均 郑建民

Cite this article as: HOU G R, WANG C, LI L L, et al. Comparison of 3D amide proton transfer imaging and intravoxel incoherent motion imaging in the diagnosis of prostate cancer[J]. Chin J Magn Reson Imaging, 2023, 14(5): 139-144.本文引用格式:侯国瑞, 王晨, 李磊磊, 等. 3D酰胺质子转移成像与体素内不相干运动成像对前列腺癌的诊断价值研究[J]. 磁共振成像, 2023, 14(5): 139-144. DOI:10.12015/issn.1674-8034.2023.05.024.


[摘要] 目的 探讨3D酰胺质子转移成像(amide proton transfer, APT)与体素内不相干运动(intravoxel incoherent motion, IVIM)成像对前列腺癌(prostate cancer, PCa)诊断以及评估PCa危险度的价值。材料与方法 回顾性分析2022年4月至2022年11月本院51例前列腺疾病患者病例资料,根据患者病理穿刺或者手术结果分为良性前列腺增生(benign prostatic hyperplasia, BPH)组27例和PCa组24例,依照Gleason评分(Gleason score, GS)结果把PCa组分为低危组(≤6分)6例和高危组(≥7分)18例。所有患者在术前行3.0 T MRI前列腺检查,扫描序列包括T2WI、APT、IVIM、扩散加权成像(diffusion-weighted imaging, DWI)等,在APT和IVIM参数图像上勾画感兴趣区,测量病灶的APT值、真实扩散系数(D)、伪扩散系数(D*)、灌注分数(f)以及表观扩散系数(apparent diffusion coefficient, ADC)。使用独立样本t检验比较BPH组和PCa组、PCa低危组与高危组间各参数差异,用受试者工作特征(receiver operating characteristic, ROC)曲线评估各参数的诊断效能。应用Spearman相关性分析法分析上述各参数与GS的相关性。结果 BPH组的D值和ADC值显著高于PCa组,APT值显著低于PCa组,差异均有统计学意义(P<0.05),D*值和f值在两组间差异无统计学意义(P>0.05)。PCa低危组的D值和ADC值显著高于PCa高危组,APT值显著低于PCa高危组,差异均有统计学意义(P<0.05)。ROC分析示ADC与D值鉴别诊断BPH与PCa的特异度高于APT值,而APT和D值鉴别诊断的敏感度高于ADC值。Spearman相关分析显示PCa病灶ADC值、D值与GS呈显著负相关(r=-0.691、-0.624,P<0.001);APT值与GS呈显著正相关(P=0.026,r=0.455),D*值和f值与GS无相关性(P>0.05)。结论 APT和IVIM成像对PCa鉴别诊断具有一定价值,APT值和IVIM的D值可为PCa的病理分级提供帮助,且D值的价值更高。
[Abstract] Objective To investigate the value of 3D amide proton transfer (APT) imaging and intravoxel incoherent motion (IVIM) imaging in the diagnosis and risk assessment of prostate cancer (PCa).Materials and Methods A total of 51 patients with prostate disease in our hospital from April 2022 to November 2022 were prospectively included and divided into 27 patients in the benign prostatic hyperplasia (BPH) group and 24 patients in the PCa group according to pathological puncture or surgical results. According to Gleason score (GS), PCa group was divided into low-risk group (≤6) with 6 cases and high-risk group (≥7) with 18 cases. All patients underwent 3.0 T MRI prostatic examination before surgery. The scans included APT, IVIM, diffusion-weighted imaging (DWI) and other sequences. The areas of interest were delineated on the APT and IVIM parameter images, and the APT value, true diffusion coefficient (D), pseudo diffusion coefficient (D*), perfusion fraction (f) and ADC value of the lesions were measured. Independent sample t test was used to compare the differences of various parameters between BPH group and PCa group, and between PCa high-risk group and low-risk group. Receiver operating characteristic (ROC) curve was used to assess the diagnostic efficiency of each parameter. Spearman correlation analysis was used to analyze the correlation between the parameters and GS.Results The D value and ADC value of BPH group were observably higher than that of PCa group, while the APT value was observably lower than that of PCa group, with statistical significance (P<0.05). There was no statistical difference in D* and f values between the two groups. D value and ADC value in PCa low-risk group were significantly higher than those in PCa high-risk group, and APT value was significantly lower than those in PCa high-risk group, with statistical significance (P<0.05). ROC curve analysis showed that the diagnostic specificity of ADC and D values was higher than APT values, while the diagnostic sensitivity of APT and D values was higher than ADC values. Spearman correlation analysis displayed that the ADC value and D value of PCa lesions were significantly negatively correlated with GS (r=-0.691, -0.624; P<0.001); APT value was significantly positively correlated with GS (r=0.455, P=0.026), while D* value and f value were not correlated with GS (P>0.05).Conclusions APT and IVIM imaging have certain value in the differential diagnosis of PCa, APT and IVIM D value can provide help for the pathological grading of PCa, and D value is higher.
[关键词] 前列腺癌;病理分级;Gleason 评分;磁共振成像;酰胺质子转移成像;体素内不相干运动;鉴别诊断
[Keywords] prostate cancer;pathological grade;Gleason score;magnetic resonance imaging;amide proton transfer imaging;intravoxel incoherent motion;differential diagnosis

侯国瑞    王晨    李磊磊    林港    李奕均    郑建民 *  

空军军医大学西京医院放射诊断科,西安 710032

通信作者:郑建民,jmzheng1986@126.com

作者贡献声明:郑建民设计本研究的方案,对稿件重要的内容进行了修改;侯国瑞起草和撰写稿件,获取、分析或解释本研究的数据;王晨、李磊磊、林港、李奕均获取、分析或解释本研究的数据,对稿件重要的内容进行了修改;全部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。


收稿日期:2022-12-19
接受日期:2023-05-06
中图分类号:R445.2  R737.25 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.05.024
本文引用格式:侯国瑞, 王晨, 李磊磊, 等. 3D酰胺质子转移成像与体素内不相干运动成像对前列腺癌的诊断价值研究[J]. 磁共振成像, 2023, 14(5): 139-144. DOI:10.12015/issn.1674-8034.2023.05.024.

0 前言

       前列腺癌(prostate cancer, PCa)是男性死亡率仅次于肺癌的恶性疾病[1],也是我国中老年男性较为常见的恶性疾病之一,近年来其发患者群趋于年轻化,且发病率不断增加[2],严重危害男性生命健康,因此对PCa的预防与早期诊断显得尤为重要。前列腺病理穿刺活检是目前诊断PCa的金标准[3],但它是有创性的,会给患者带来痛苦,且容易引发出血、感染等并发症,因此需另寻求一种无创的PCa检查方法。MRI作为一种非侵入性的无创检查,是诊断前列腺良恶性疾病的重要辅助检查之一。近年来,随着MRI技术的飞速发展,3D酰胺质子转移(amide proton transfer, APT)成像和体素内不相干运动(intravoxel incoherent motion, IVIM)成像逐渐被用于前列腺相关疾病的鉴别诊断研究[4]

       APT技术主要用于检测细胞内游离蛋白质及多肽含量,间接反映活体细胞内部游离蛋白质及多肽含量,进而呈现活体细胞内部的代谢情况和生理病理信息[5]。IVIM主要用于测量体素内分子扩散程度,以及反映局部组织血液微循环灌注信息。既往研究表明,APT或IVIM技术对前列腺疾病均有一定的诊断价值[6, 7],但既往APT采用的是2D技术,一次成像只能采集一个病变层面,如对整个前列腺组织进行成像,需进行多次成像,扫描时间很长,故其在前列腺的应用较少。同时IVIM的成像时间也相对较长,因此鲜有关于APT和IVIM技术对PCa诊断价值的对比研究。而3D-APT技术一次成像便可对前列腺组织进行多层面成像,大大缩短了扫描时间,本研究借助3D-APT技术,对比分析APT和IVIM技术对PCa的诊断价值,并分析其与Gleason评分(Gleason score, GS)的相关性。

1 材料和方法

1.1 研究对象

       本研究遵守《赫尔辛基宣言》,经过空军军医大学西京医院医学伦理审查委员会批准,免除受试者知情同意,批准文号:KY20223060-1。回顾性分析2022年4月至2022年11月间在本院行前列腺3.0 T MRI检查的患者病例资料。纳入标准:(1)MRI检查前未接受手术或放化疗治疗;(2)MRI检查后4周内经前列腺穿刺活检或手术后证实为PCa或良性前列腺增生(benign prostatic hyperplasia, BPH);(3)临床病理资料齐全,MRI图像完整,包含T2WI、T1WI、扩散加权成像(diffusion-weighted imaging, DWI)、IVIM、APT序列的图像。排除标准:(1)病灶小于3 mm,不便于参数测量;(2)MRI图像质量差,影响诊断和参数的测量。按照纳入排除标准,最终选取51例符合条件的患者病例资料作为本研究对象。

1.2 检查方法

       使用Philips 3.0 T MRI扫描仪(Ingenia CX, PHILIPS Healthcare)对患者进行前列腺扫描,采用16通道相控阵体部线圈。嘱咐患者检查前4~6 h禁食禁水,且扫描前排空膀胱,避免肠道蠕动的伪影对图像质量的产生干扰。扫描序列包括T2WI、T1WI、DWI、IVIM、APT,各序列详细参数见表1

表1  各扫描序列参数
Tab. 1  Scanning parameters of each sequence

1.3 图像后处理及参数测量

       APT和DWI图像经Philips后处理工作站IntelliSpace处理,并测量APT值和ADC值。IVIM图像经MRIcroGL(https://www.nitrc.org/projects/mricrogl)和MITK(Medical Imaging Interaction Toolkit, Germany)后处理软件处理后生成IVIM的衍生参数:真实扩散系数(true diffusion coefficient, D)、伪扩散系数(perfusion-related diffusion coefficient, D*)、灌注分数(perfusion fraction, f)。两名前列腺诊断经验丰富的高资历医师(分别为工作5年的主治医师和工作10年的副主任医师)在对患者临床病理信息未知的情况下,根据T2WI和DWI图像的影像征象选择感兴趣区(region of interest, ROI),存在多个病灶时,选择最大的病灶作为ROI进行测量,测量所选点位的APT、ADC、D、D*、f值。两位医师对每个病灶分别测量三次,记录所测平均值作为最后的测量结果。ROI的选择标准:(1)每次所测ROI的面积保持基本一致;(2)ROI尽可能置于病灶的中央区域,避开病灶的边缘;(3)尽量避开出血、囊变及坏死区域。

1.4 病理检查

       所有患者在前列腺MRI检查后四周内行前列腺穿刺活检或前列腺根治性手术治疗,51例患者中,38例经病理穿刺活检证实,13例经术后病例证实,共检出58个病灶。依照病理穿刺或手术结果将患者分为BPH组27例和PCa组24例,并且对PCa组患者的病灶进行Gleason评分。根据Gleason评分将PCa患者分为低危组6例(GS≤6分)和高危组18例(GS≥7分)两个亚组。

1.5 统计学分析

       使用SPSS 27.0(Chicago, IL, USA)和MedCalc20.2(MedCalc Software, Ostend, Belgium)软件对所测数据进行统计分析。两名医师所测数据一致性用组内相关系数(intra-class correlation coefficient, ICC)进行评价,若所测数据一致性良好(ICC>0.75),则取二者所测平均值进行后续分析。使用独立样本t检验分析各组间的APT、ADC、D、D*、f值差异。绘制受试者工作特征(receiver operating characteristic, ROC)曲线评估上述参数的诊断效能,并计算其曲线下面积(area under the curve, AUC)。采用DeLong检验比较各AUC间的差异性。采用Spearman相关性分析方法来分析各参数与GS的相关性。P<0.05为差异具有统计学意义。

2 结果

2.1 BPH组和PCa组患者基本信息

       BPH组患者年龄与PCa组间差异无统计学意义(P>0.05)。BPH组患者前列腺特异性抗原(prostate specific antigen, PSA)值明显低于PCa组(P<0.001)。PCa组中低危组与高危组的GS差异有统计学意义(P<0.001)。详见表2

表2  两组患者临床基本信息
Tab. 2  Basic clinical information of two groups

2.2 各参数一致性检验

       两位医师所测病变ROI的APT、ADC、D、D*、f值一致性检验结果依次为0.952、0.986、0.976、0894、0.863,ICC均>0.75,表明结果一致性良好。

2.3 APT和IVIM参数比较

2.3.1 BPH组和PCa组间APT和IVIM参数比较

       BPH组和PCa组间各参数的独立样本t检验结果显示:BPH组的APT值显著低于PCa组(P<0.001),ADC值和D值显著高于PCa组(P<0.001),但D*值和f值在两组间差异无统计学意义(P>0.05)。详见表3图1、2。

图1  男,68岁,诊断为BPH,病灶如图中箭所指。1A:T2WI图示右侧移行区见类圆形等信号;1B:APT与T2WI融合图,APT值为1.8%;1C:IVIM后处理生成的D图,D值为0.834×10-3 s/mm2;1D:轴位ADC图呈等信号,ADC值为1.08×10-3 s/mm2;1E:轴位DWI图呈等信号;1F:病理大切片图(HE ×200)。
图2  男,72岁,病理诊断为PCa,病灶如箭头所指。2A:T2WI图示右侧外周带见斑片状低信号;2B:APT与T2WI融合图,APT值为3.5%;2C:IVIM后处理生成的D图,D值为0.426×10-3 s/mm2;2D:轴位ADC图呈明显低信号,ADC值为0.67×10-3 s/mm2;2E:轴位DWI图示右侧外周带呈高信号;2F:病理大切片图(HE ×200)。BPH:良性前列腺增生;APT:酰胺质子转移;IVIM:体素内不相干运动;D:真实扩散系数;ADC:表观扩散系数;DWI:扩散加权成像;PCa:前列腺癌。
Fig. 1  A 68-year-old male is diagnosed bengin prostatic hyperplasia (BPH) by pathology, arrows point to BPH lesions. 1A: T2WI shows circular isosignals are seen in the right transitional zone; 1B: APT-T2WI fusion image, APT value is 1.8%; 1C: D image generated by IVIM post-processing, D value is 0.834×10-3 s/mm2; 1D: ADC image shows isointensity, ADC value is 1.08×10-3 s/mm2; 1E: DWI image shows isointensity; 1F: Pathological image (HE ×200).
Fig. 2  A 72-year-old male is diagnosed with prostate cancer (PCa) by pathology, arrows point to PCa lesions. 2A: T2WI shows patchy low signal in the right peripheral zone; 2B: APT-T2WI fusion image, APT value is 3.5%; 2C: D image generated by IVIM post-processing, D value is 0.426×10-3 s/mm2; 2D: ADC image shows low signal, ADC value is 0.67×10-3 s/mm2; 2E: DWI image shows high signal; 2F: Pathological image (HE ×200). APT: amide proton transfer; IVIM: intravoxel incoherent motion; D: true diffusion coefficient; ADC: apparent diffusion coefficient; DWI: diffusion-weighted imaging.
表3  BPH组和PCa组间各参数值比较
Tab. 3  Comparsion of parameters of between BPH group and PCa group

2.3.2 PCa低危组和高危组间APT和IVIM参数比较

       PCa低危组和高危组间APT和IVIM参数独立样本t检验结果显示:低危组ADC值和D值显著高于高危组(P均<0.001),APT值显著低于高危组(P<0.05)。详见表4

表4  低危组和高危组间APT和IVIM参数比较
Tab. 4  Comparsion of parameters of APT and IVIM between low-risk group and high-risk group

2.4 APT和IVIM参数鉴别BPH和PCa的诊断效能比较

       ADC值鉴别BPH和PCa的AUC最大,其次为D值、APT值;ADC值和D值的诊断敏感度均显著高于APT值(P<0.05);APT与D值的诊断特异度均高于ADC值,但差异无统计学意义(P>0.05)。详见表5图3

图3  APT、ADC和D值诊断PCa的ROC曲线。
图4  ADC值、D值、APT值与GS相关性分析。APT:酰胺质子转移;ADC:表观扩散系数;D:真实扩散系数;PCa:前列腺癌;ROC:受试者工作特征;GS:Gleason评分。
Fig. 3  ROC curves of APT, ADC and D values for the diagnosis of PCa.
Fig. 4  Correlation analysis between ADC value, D value, APT value and GS. ROC: receiver operating characteristic; APT: amide proton transfer; ADC: apparent diffusion coefficient; D: true diffusion coefficient; PCa: prostate cancer; GS: Gleason score.
表5  APT和IVIM参数对BHP和PCa的鉴别诊断效能
Tab. 5  Diagnostic performance of APT and IVIM parameters in differentiating BHP and PCa

2.5 APT和IVIM参数与GS相关性分析

       Spearman相关性分析结果显示:ADC值、D值与GS均呈显著负相关(r=-0.691、-0.624,P<0.001);APT值与GS呈显著正相关(r=0.455,P=0.026);而D*值和f值与GS无显著相关性(图4)。

3 讨论

       本研究使用了3D-APT技术和IVIM技术,通过测量图像APT、ADC、D、D*、f值,对比分析两种技术鉴别BPH和PCa的诊断价值,探究两种技术各参数与GS的相关性。本研究是国内首次对这两种技术在PCa方面的诊断价值进行比较,同时创新性使用了3D-APT技术,缩短了扫描时间,同时增加了成像范围。结果显示APT、ADC和D值在BPH组和PCa组间差异有统计学意义(P<0.05),可以为鉴别BPH和PCa提供价值,而D*和f值在BPH组和PCa组间差异无统计学意义(P>0.05),对鉴别BPH和PCa无意义。另外,本研究发现APT值和D值对PCa患者的病理分级也具有一定临床价值。

3.1 APT技术鉴别BPH和PCa的价值

       APT成像是一种基于化学饱和转移发展起来的分子成像技术,可无创检测酰胺质子与水分子之间的交换过程,揭示细胞代谢和病理生理信息[8]。酰胺质子大多存在于游离的蛋白质和多肽中,APT发出一定频率的脉冲对其进行饱和性标记,周围组织中自由水的氢质子与被饱和的酰胺质子进行化学交换,进而使周围组织中自由水的信号也被饱和,自由水的信号因此而降低,通过检测饱和前后自由水信号强度的变化来间接反映组织中酰胺质子的含量和交换率,从而反映出细胞组织蛋白质和多肽等大分子物质代谢信息,在一定程度上反映出组织的病理生理信息。

       已有研究证明APT在胶质瘤[9]、乳腺肿瘤[10]、宫颈癌[11]、直肠肿瘤[12]、膀胱癌[13]、PCa[14]等领域的应用价值。本试验结果显示BPH组的APT值明显低于PCa组,这与既往研究结果一致[15],原因可能是PCa组织内的肿瘤细胞比BPH组织内的细胞代谢水平更加活跃,细胞增殖更迅速,细胞数目增多,细胞内可移动蛋白和多肽增多,蛋白浓度升高进而引起APT值升高。此外有研究表明[16],随着PCa细胞的不断增殖,其产生的一种具有强流动性的蛋白质(雄激素调节的六反式膜蛋白)的浓度也会随之升高,这可能也是引起APT值升高的原因。此外,LAWRENCE等[17]认为随着肿瘤细胞的增殖,前列腺组织中正常的腺体结构会受到破坏,腺体中所含的液体、可移动的蛋白质和多肽含量会减少,这可能会使APT值有所下降,但影响不大。本研究结果中APT技术鉴别BPH和PCa的AUC为0.878,提示其具有较高的诊断效能,因此APT可考虑用于帮助临床鉴别诊断PCa。

3.2 IVIM技术鉴别BPH和PCa的价值

       目前前列腺功能MRI应用最成熟的技术是DWI,ADC值便是在它的单指数模型下经过运算得出的。ADC值能够反映出组织内水分子扩散受限情况,其除了与水分子扩散运动有关,还受组织微循环血液灌注的影响。IVIM正是在此基础上发展起来的,IVIM采用双指数模型,无须对比剂即可同时提供真实水分子扩散受限情况和组织微循环灌注信息[18],通过采用多b值拟合出D、D*和f值。已有研究证明IVIM技术在肝脏[19]、宫颈[20]、乳腺[21]等部位具有良好临床效能。本研究中D值在BPH组与PCa组间差异有统计学意义(P<0.05),这与韩思圆等[22]结果一致。这可能是因为与前列腺增生组织内细胞组织松散排列相比,PCa组织内肿瘤细胞增殖迅速,细胞数目明显增多,细胞密度变大,导致细胞排列更加紧密,细胞间间隙减小,从而导致细胞内外的水分子扩散程度下降,故D值明显降低。但目前关于IVIM衍生参数D*值和f值在PCa与BPH的鉴别诊断中尚无一致结论。例如,LI等[23]研究显示PCa的D*值显著高于BPH组,而f值差异无统计学意义;王睿等[24]研究发现BPH组的f值显著高于PCa组,而D*值在BPH和PCa间差异无统计学意义;王明帅等[25]研究结果则显示PCa与BPH间D*和f值的差异均无统计学意义。本研究发现D*值和f值在PCa与BPH组间无差异。这种不同结果可能是因为PCa组织的异质性,即不同解剖区域、不同分化程度的前列腺的癌组织D*值与f值可能会有差异[26, 27],同时PCa与BPH组织的空间重叠也可能会对结果产生影响。SHINMOTO等[28]认为f值受微血管的血流灌注、腺管内液体流动等多种因素的影响,因此也会导致f值偏离真实水平。此外,关于IVIM中b值的数量、范围选择等缺乏统一标准,这也可能是导致所测结果存在差异的原因。因此ADC值和D值可考虑用于帮助临床鉴别诊断BPH和PCa,而D*和f值对鉴别BPH和PCa无临床价值。

3.3 APT和IVIM对PCa病理分级的价值

       本研究结果显示PCa低危组APT值明显低于高危组,与GUO等[29]研究结果相同,其原因可能是高危组的癌组织比低危组增殖速率更快,癌细胞数目更多,坏死的细胞更多,微血管密度增加,以及细胞核的异性性更大,共同引起组织内可移动的蛋白质和多肽含量升高[30, 31, 32],因此两组间APT值存在显著差异。本研究中PCa低危组D值显著高于高危组,原因可能是随着病变组织恶性程度加重,癌组织排列更加紧密,细胞间隙进一步缩小,水分子扩散进一步受限,故D值降低。研究结果表明APT和IVIM可以为PCa的病理分级的提供价值。

3.4 APT和IVIM与GS的相关性

       GS系统是目前对PCa分级应用最广泛的评分系统[33],GS与PCa危险度呈正相关,GS越高表示癌细胞分化越差,治疗后的疗效往往也越差。本研究依照GS结果把PCa患者划分成低危组和高危组,分析各参数与GS相关性,结果显示ADC和D值与GS呈显著负相关;APT值与GS呈中等程度正相关,与前人研究结果一致[34]。这表明ADC值和D值对评估PCa危险度的有较高的价值,APT值也能对评估PCa危险度提供一定帮助。

3.5 本研究的局限性

       (1)本研究纳入的病例数较少,且将PCa患者仅分为了高低危组,没有划分中危组,后续有待提高样本量进行下一步研究;(2)本研究中一些病理结果是经超声引导下穿刺活检得出的,准确性低于手术切除后的病理结果,可能会影响PCa的分组;(3)勾画ROI时选取了病灶的中心,并未包含全部病灶,可能会忽略部分肿瘤异质信息,后续可考虑利用直方图等方法对全病灶进行分析。

4 结论

       综上所述,3D-APT和IVIM均可提供更多定量参数信息帮助鉴别PCa与BPH,此外APT值和IVIM的D值对PCa患者的病理分级也具有一定临床价值,且D值的临床价值更高。

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