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调查研究
体素内不相干运动扩散加权成像在前列腺癌鉴别诊断及Gleason分级中应用的Meta分析
郭定波 曾国飞 杨华 李雪娇 欧芳元

Cite this article as: Guo DB, Zeng GF, Yang H, et al. Intravoxel incoherent motion diffusion-weighted imaging for assessment of the differential diagnosis and Gleason grade in prostate cancer: a Meta-analysis[J]. Chin J Magn Reson Imaging, 2022, 13(2): 69-74.本文引用格式:郭定波, 曾国飞, 杨华, 等. 体素内不相干运动扩散加权成像在前列腺癌鉴别诊断及Gleason分级中应用的Meta分析[J]. 磁共振成像, 2022, 13(2): 69-74. DOI:10.12015/issn.1674-8034.2022.02.014.


[摘要] 目的 采用Meta分析方法综合探讨体素内不相干运动(intravoxel incoherent motion,IVIM)扩散加权成像(diffusion-weighted imaging,DWI)的各参数,包括表观扩散系数(apparent diffusion coefficients,ADC)、真性扩散系数(true diffusion coefficient,D)、灌注相关假性扩散系数(perfusion-related pseudo-diffusion coefficient,D*)和灌注分数(perfusion fraction,f)在前列腺癌(prostate cancer,PCa)鉴别诊断和Gleason分级中的价值。材料与方法 于Embase、PubMed、Medline和Cochrane Library数据库检索自建库至2021年8月应用IVIM DWI对PCa进行鉴别诊断和Gleason分级的相关文献。采用Stata 15.0软件进行Meta分析,连续性变量资料采用加权均数差(weighted mean difference,WMD)及其95% CI作为统计效应量,并绘制森林图。通过亚组分析来讨论研究异质性,并评估发表偏倚。结果 共纳入文献13篇,涉及504例患者和821个感兴趣区(regions of interest,ROI)。合并结果显示:与健康外周带组织(peripheral zone,PZ)比较,PCa的ADC、D与f值均明显减低{WMD=-0.82 [95% CI (-1.01~-0.64)],Z=8.69,P<0.0001;WMD=-0.54 [95% CI (-0.78~-0.29)],Z=4.34,P<0.0001;WMD=-6.91 [95% CI (-12.12~-1.70)],Z=2.60,P<0.0001}。与ADC值比较,PCa组织中D值明显减低{WMD=-0.20 [95% CI (-0.38~-0.03)],Z=2.26,P=0.02}。与低级别(low-grade,LG) PCa组比较,中/高级别(intermediate/high-grade,HG) PCa组ADC值和D值均明显减低{WMD=-0.24 [95% CI (-0.30~-0.19)],Z=8.06,P<0.001;WMD=-0.25 [95% CI (-0.33~-0.17)],Z=5.99,P<0.001}。结论 IVIM参数适用于PCa的鉴别诊断,D值可能比ADC值在PCa灶上的表征价值更大。另外,ADC值与D值可进一步区分LG和HG前列腺癌。
[Abstract] Objective To explore the value of parameters of intravoxel incoherent motion (IVIM) diffusion-weighted imaging (DWI), including apparent diffusion coefficient (ADC), true diffusion coefficient (D), pseudo-diffusion coefficient (D*) and perfusion fraction (f) in the differential diagnosis and Gleason grade of prostate cancer (PCa).Materials and Methods A literature search on Embase, Medline, PubMed and Cochrane Library was performed to identify all the relevant studies characterizing differential diagnosis and Gleason grade of PCa by IVIM DWI published until August 2021. Stata 15.0 software was used for statistics analysis, for continuous variables, weighted mean difference (WMD) with corresponding 95% confidence interval (95% CI) was used as the statistical effect size, and forest maps were drawn. In addition, subgroup analysis was conducted to assess for heterogeneity, and risk of bias was assessed by Begg's test.Results A total of 13 articles were included, involving 504 patients and 821 ROIs. The pooled results of IVIM parameters for differentiating between PCa and healthy peripheral zone (PZ) showed that ADC, D and f values were significantly lower in regions of PCa compared to those of regions of PZ {WMD=-0.82 [95% CI (-1.01--0.64)], Z=8.69, P<0.0001; WMD=-0.54 [95% CI (-0.78--0.29)], Z=4.34, P<0.0001; WMD=-6.91 [95% CI (-12.12--1.70)], Z=2.60, P<0.0001}. In addition, D was significantly lower than ADC in the regions of PCa {WMD=-0.20 [95% CI (-0.38--0.03)], Z=2.26, P=0.02}. Compared with the low-grade (LG) PCa group, the pooled results showed that ADC value and D value in intermediate/high-grade (HG) PCa were significantly decreased {WMD=-0.24 [95% CI (-0.30--0.19)], Z=8.06, P<0.001; WMD=-0.25 [95% CI (-0.33--0.17)], Z=5.99, P<0.001}.Conclusions IVIM parameters are suitable for the differential diagnosis of PCa, and the D value may be more valuable than the ADC value in the characterization of PCa lesions. In addition, ADC value and D value can further distinguish LG and HG prostate cancer.
[关键词] 前列腺癌;体素内不相干运动;扩散加权成像;Gleason分级;鉴别诊断
[Keywords] prostate cancer;intravoxel incoherent motion;diffusion-weighted imaging;Gleason grade;differential diagnosis

郭定波    曾国飞    杨华    李雪娇    欧芳元 *  

重庆市中医院放射科,重庆 400021

欧芳元,E-mail:ofy0705@126.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: 重庆市自然科学基金项目 cstc2020jcyj-msxmX0751 重庆市科卫联合医学科研项目 2019QNXM010
收稿日期:2021-10-09
接受日期:2021-12-31
中图分类号:R445.2  R737.25 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.02.014
本文引用格式:郭定波, 曾国飞, 杨华, 等. 体素内不相干运动扩散加权成像在前列腺癌鉴别诊断及Gleason分级中应用的Meta分析[J]. 磁共振成像, 2022, 13(2): 69-74. DOI:10.12015/issn.1674-8034.2022.02.014

       前列腺癌(prostate cancer,PCa)是老年男性泌尿生殖系统最常见的恶性肿瘤之一,近年来其发病率和病死率有持续上升的趋势[1]。Gleason分级是判断PCa生物学活性和侵袭性的重要因素,并可作为PCa预后的主要病理预测指标,指导疾病管理和治疗策略[2]。PCa的术前确诊仍需依靠穿刺活检并获得Gleason评分(Gleason score,GS),而有创性活检的检出率约为62.2%[3]。因此,应用准确可靠的无创技术对PCa的术前诊断和评估至关重要。扩散加权成像(diffusion-weighted imaging,DWI)利用组织间水分子扩散差异,显示出改进PCa检测的潜能,但经单指数模型DWI计算所得的表观扩散系数(apparent diffusion coefficients,ADC)不同程度混有微循环灌注成分,不能代表体素内的真实水分子扩散,而体素内不相干运动(intravoxel incoherent motion,IVIM)-DWI通过多b值拟合可更精确地反映水分子的信号衰减情况,将真性扩散系数(true diffusion coefficient,D)和灌注相关假性扩散系数(perfusion-related pseudo-diffusion coefficient,D*)区分开来,并获得反映肿瘤微循环的灌注分数(perfusion fraction,f)[4, 5]。本文采用Meta分析方法旨在评估IVIM各参数在PCa鉴别诊断和Gleason分级中应用的价值。

1 材料与方法

1.1 文献检索

       于PubMed、Embase、Medline和Cochrane Library数据库检索建库至2021年8月应用IVIM 各参数对PCa进行鉴别诊断和Gleason分级评估的相关英文文献。检索词为:“DWI”“diffusion weighted imaging”“ADC”“apparent diffusion coefficient”“IVIM”“intravoxel incoherent motion”“prostate carcinoma”“prostate”、“cancer”“neoplasm”和“tumor”。由两名研究者独立检索文献,不一致时经协商确定。为尽可能覆盖相关文献,采用主题词与自由词结合的检索方法,并对纳入研究的参考文献进行再次检索。

1.2 纳入标准

       纳入标准:(1)公开发表的关于IVIM各参数用于区分PCa与健康外周带(peripheral zone,PZ)组织和/或低级别(low-grade,LG) PCa与中/高级别(intermediate/high-grade,HG) PCa的前瞻性或回顾性英文研究;(2)可提取到至少包含D、D*、f的均值和标准差数据;(3)以病理学和/或临床长期随访结果为诊断“金标准”;(4)相同主题文献补充数据后重新发表的研究,采用最新研究数据;(5)对照组的感兴趣区(regions of interest,ROI)为健康PZ组织。本研究经重庆市中医院伦理委员会审批,免除受试者知情同意,批准文号:2020-ky-51。

1.3 文献质量评价和数据

       采用诊断准确性试验质量评价工具2 (quality assessment of diagnostic accuracy studies 2,QUADAS-2)对纳入研究进行分级评估,评价文献质量及发生偏倚的可能性,并作出“是”(低度偏倚或适用性好)、“否”(高度偏倚或适用性差)或“不清楚”(缺乏相关信息或偏倚情况不确定)的判断[6]。并提取纳入各项研究的基本特征、PCa灶和健康外周带组织的IVIM各参数值、LG PCa和HG PCa的IVIM各参数值等。

1.4 统计学分析

       采用Stata 15.0软件进行Meta分析,连续性变量数据采用加权均数差(weighted mean difference,WMD)及其95% CI作为统计效应量,并绘制森林图。采用Cochran-Q检验及I2值分析研究间的异质性,I2>50%且P<0.1表示研究存在异质性[7]。若存在明显异质性,则需对异质性来源进行探讨,利用亚组分析排除可能与本研究相关的异质性因素。通过Begg检验评估发表偏倚。

2 结果

2.1 文献检索与质量评价

       按预先制订的标准筛选后,最终纳入13篇文章[8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20],涉及504例患者和821个ROIs (464个PCa ROIs,357个PZ ROIs)。文献筛选流程见图1,基本特征见表1,IVIM关于前列腺癌的特征资料见表2表3。本研究主要从PCa的鉴别诊断和Gleason分级两部分进行讨论。鉴别诊断部分共包含11篇[8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18]文献,其中1篇[15]没有ADC相关数据。Gleason分级部分纳入5篇[16, 17, 18, 19, 20]文献,其中2篇[19, 20]仅有PCa Gleason分级相关数据。依据GS将PCa分为LG (GS≤6)和HG (GS>6)两组。纳入13篇文献的质量均较高,文献质量评价结果见图2

图1  文献筛选流程图。
Fig. 1  Flowchart of literature screening.
图2  文献质量评价图。
Fig. 2  Risk bias assessment for included studies.
表1  纳入研究的基本资料
Tab. 1  The basic data in studies included
表2  IVIM参数鉴别PCa和PZ的特征资料
Tab. 2  The characteristic data of IVIM parameters for PCa and PZ regions
表3  IVIM参数区分LG PCa和HG PCa的特征资料
Tab. 3  The characteristic data of IVIM parameters for LG PCa and HG PCa

2.2 IVIM参数鉴别诊断PCa与PZ组织的合并结果

       与PZ比较,PCa的ADC、D与f值均明显减低{WMD=-0.82 [95% CI (-1.01~-0.64)],Z=8.69,P<0.0001;WMD=-0.54 [95% CI (-0.78~-0.29)],Z=4.34,P<0.0001;WMD=-6.91 [95% CI (-12.12~-1.70)],Z=2.60,P<0.0001};然而,PCa和PZ之间D*值差异无统计学意义{WMD=0.21 [95% CI (-0.56~0.97)],Z=0.53,P=0.60}。此外,与ADC值比较,PCa组织中D值明显减低{WMD=-0.20 [95% CI (-0.38~-0.03)],Z=2.26,P=0.02},见图3

图3  IVIM参数鉴别PCa和PZ的森林图。3A:ADC的森林图;3B:D的森林图;3C:f的森林图;3D:PCa中D值和ADC值差异结果的森林图。注:IVIM:体素内不相干运动;PCa:前列腺癌;PZ:外周带。
Fig. 3  Forest plots of IVIM parameters for PCa and PZ regions. 3A: Forest plot of ADC; 3B: Forest plot of D; 3C: Forest plot of f; 3D: Forest plot showing results of the difference between D and ADC in PCa Note: IVIM: intravoxel incoherent motion; PCa: prostate cancer; PZ: peripheral zone.

2.3 亚组分析结果

       ADC、D和f值合并结果的异质性均较高(I2=96.1%,P<0.01;I2=98.8%,P<0.01;I2=94.1%,P<0.01),因此对可能影响本研究异质性的因素(发表年份,地区,研究类型,磁共振场强大小,b值个数和最大b值)进行亚组分析,结果显示:ADC值中亚洲地区的研究相应异质性水平有所下降(I2=50.1%,P=0.14),PCa的ADC值相较于PZ显著减低{WMD=-0.95 [95% CI (-1.04~-0.85)],Z=19.19,P<0.0001};D值中发表年份≤2015的研究具有低水平异质性(I2=0.0%;P=0.70),PCa的D值相较于PZ显著减低{WMD=-0.41 [95% CI (-0.47~-0.35)],Z=13.44,P<0.001};f值中最大b值<1000的研究对应较低水平的异质性(I2=40.5%,P=0.17),然而PCa的f值减低相较于PZ差异不具有统计学意义{WMD=-2.59 [95% CI (-5.50~0.31)],Z=1.75,P=0.08}。

2.4 发表偏倚分析

       Begg检验结果显示:扩散参数(ADC和D)及灌注参数(D*和f)均未发现明显发表偏倚(P值分别为1.00、0.64、1.00、0.16)。

2.5 IVIM参数区分LG PCa与HG PCa的合并结果

       与LG组比较,HG组ADC值和D值均明显减低{WMD=-0.24 [95% CI (-0.30~-0.19)],Z=8.06,P<0.001;WMD=-0.25 [95% CI (-0.33~-0.17)],Z=5.99,P<0.001},见图4

图4  IVIM参数区分PCa和PZ的森林图。4A:ADC的森林图;4B:D的森林图。注:IVIM:体素内不相干运动;PCa:前列腺癌;PZ:外周带。
Fig. 4  Forest plots of IVIM parameters for HG PCa and LG PCa regions. 4A: Forest plot of ADC; 4B: Forest plot of D Note: IVIM: intravoxel incoherent motion; PCa: prostate cancer; PZ: peripheral zone.

3 讨论

       DWI已被公认为肿瘤的影像生物标记,是肿瘤检测和表征的关键工具[21],可区分肿瘤和非肿瘤组织,甚至可监测和预测治疗反应[22]。从IVIM-DWI数据中确定扩散和灌注信息可提高对肿瘤和正常组织的鉴别能力,有助于对肿瘤组织恶性程度进行分级。近年来,多项研究对不同类型癌症的IVIM-DWI各参数价值进行了探讨[23, 24, 25],在PCa患者中结果不尽相同,尤其是灌注分数f。因此,本文采用Meta分析的方法以探讨IVIM各参数关于PCa研究结果中的不一致性,结果发现IVIM-DWI适用于PCa的鉴别诊断和Gleason分级,参数D值更是具有较大的表征价值和肿瘤分级作用,这是国内首次使用Meta分析对PCa与健康PZ组织进行鉴别诊断与分级评估,通过大样本量数据分析获得更加稳定和可靠的结果。在临床工作中,D值或有望成为无创性筛查PCa和预测PCa侵袭性及预后的有效影像指标。

3.1 PCa鉴别诊断的Meta分析结果

       本研究中,合并结果发现PCa的ADC值、D值均明显低于PZ组织,PCa灶上皮细胞增殖迅速且排列紧密,细胞内水分子的扩散运动显著受限,表现为PCa组织的ADC值、D值降低。与PZ比较,PCa的灌注参数f值减小,而D*值无显著差异。对于D*及f值的研究报道结果不一[12,16],其原因可能与选择的b值范围及最高b值有关。更多的低b值分布有利于D*值对微循环灌注信息表达,但同时易受其他因素的影响,如松弛效应和T2[26],从而导致D*稳定性欠佳。高b值下PCa中f值可能受微循环血流灌注量及血管通透性的双重影响,其减小可能与癌灶中的血管通透性异常有关[27]。此外,本文还比较了PCa的D值与ADC值差异,合并结果发现ADC值显著大于D值,验证了两种不同扩散的存在[16],证明IVIM模型较单指数模型能够更好地拟合信号衰减,剔除灌注成分影响的D值更能真实反映肿瘤组织内的扩散特征[28]

3.2 PCa Gleason分级的Meta分析结果

       Zhang等[29]研究表明IVIM定量参数值可作为术前预测肿瘤复发的潜在生物学标志物,这对未来预后研究有一定指导意义,因为IVIM参数评估PCa预后价值时,需要校正疾病的分期及分级。据此,本文进一步分析了IVIM参数在PCa Gleason分级预测中的价值。合并结果显示HG组的ADC值、D值明显低于LG组,研究结果与Peng等[30]的一致,但Pesapane等[16]发现ADC值能有效鉴别低、高危PCa,但其他IVIM参数并无显著差异,其原因可能是与所设置的b值过低有关。GS越高,ADC值、D值越低,这可能与恶性肿瘤分化程度不同导致的组织结构和细胞密度差异有关[31]。此外,LG组和HG组的ADC值与D值之间并未发现显著差异,这说明ADC值和D值对高、低级别PCa的鉴别能力相当,但有待在未来扩大样本量进一步研究。

3.3 异质性及亚组分析

       我们发现IVIM各参数鉴别PCa与PZ组织时存在较高的异质性。亚组分析结果显示发表年份、地区和最大b值可能是异质性的来源,引起的异质性可能与IVIM扫描参数的设置日趋完善、地区差异以及合理b值的选择有关。Riexinger等[32]推荐理想情况下应该使用不少于16个b值来拟合IVIM信号,同时低b值比高b值更应受到重视。

3.4 局限性

       本Meta分析依然存在一些局限性。首先,研究存在一定异质性;其次,纳入各研究采用不同b值组合方案,b值选择和个数差异会影响结果的可比性,未来研究应集中在b值的最优组合以及确定IVIM参数的最优模型;第三,纳入的部分研究[10, 13]样本量偏小,存在影响结论稳定性的潜在可能。最后,中央带和移行带PCa关于IVIM的研究较少,故未纳入本次Meta分析,日后有待更全面、深入的扩展研究。

       综上所述,IVIM参数适用于PCa的鉴别诊断,D值可能比ADC值在PCa灶上的表征价值更大。另外,ADC值与D值可进一步区分Gleason低级别和中/高级别PCa。

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