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技术研究
多次激发平面回波扩散加权成像在颅底成像中的应用
罗贺丹 张浩南 胡帅 卢绪论 王楠 苗延巍 刘爱连 林良杰 宋清伟

Cite this article as: Luo HD, Zhang HN, Hu S, et al. Application of multi-shot echo planar imaging diffusion weighted imaging in the skull base[J]. Chin J Magn Reson Imaging, 2022, 13(9): 75-80.本文引用格式:罗贺丹, 张浩南, 胡帅, 等. 多次激发平面回波扩散加权成像在颅底成像中的应用[J]. 磁共振成像, 2022, 13(9): 75-80. DOI:10.12015/issn.1674-8034.2022.09.014.


[摘要] 目的 探讨不同激发次数和图像空间采样重建算法(image reconstruction using image-space sampling, IRIS)对颅底多次激发平面回波扩散加权成像(multi-shot echo planar imaging diffusion weighted imaging, MS-EPI DWI)图像质量的影响。材料与方法 招募健康志愿者49例,年龄(42.00±19.39)岁,所有受试者均行常规单激发平面回波扩散加权成像(single-shot echo planar imaging diffusion weighted imaging, SS-EPI DWI)序列和基于IRIS的MS-EPI DWI序列(激发次数分别为8、6、4、2)。测量计算两侧小脑和脑干脑桥的表观扩散系数(apparent diffusion coefficient, ADC)、信噪比(signal to noise ratio, SNR)、对比噪声比(contrast to noise ratio, CNR)。两位观察者采用五分评分法对图像质量进行评价。采用Kappa检验评价两位观察者评分的一致性。使用Friedman检验MS-EPI DWI序列不同激发次数ADC、SNR、CNR及主观评分与SS-EPI DWI序列的差异性。若差异具有统计学意义,进行后续多重比较并对P值做Bonferroni校正。结果 两位观察者主观评分一致性良好(Kappa=0.795、0.871、0.782、0.880、0.847)。MS-EPI DWI序列不同激发次数间比较,两侧小脑ADC差异无统计学意义(P>0.05),其余数据差异均有统计学意义(P<0.05)。与SS-EPI DWI序列相比,当激发次数为8时,MS-EPI DWI序列左脑桥脑干处ADC小于SS-EPI DWI序列(P<0.05);当激发次数为4、2时两侧脑桥脑干ADC小于SS-EPI DWI序列(P<0.05);当激发次数为8、6、2时,MS-EPI DWI序列两侧小脑和脑桥脑干SNR、CNR及主观评分均大于SS-EPI DWI序列;其中当激发次数为6时,左侧小脑和脑桥脑干SNR、CNR和右侧小脑SNR、CNR,右侧脑桥脑干SNR及主观评分较SS-EPI DWI序列差异均有统计学意义(P<0.05)。结论 与SS-EPI DWI序列相比,基于IRIS的MS-EPI DWI序列具有SNR较高、几何畸变小等优势。对于颅底部成像,临床推荐使用MS-EPI DWI序列激发次数为6次。
[Abstract] Objective To explore the performance of image reconstruction using image-space sampling (IRIS)-based multi-shot echo planar imaging diffusion weighted imaging (MS-EPI DWI) for the skull base region.Materials and Methods Forty-nine volunteerss were recruited, with an average age of (42.00±19.39) years old. All subjects underwent conventional single-shot echo planar imaging diffusion weighted imaging (SS-EPI DWI) and IRIS-based multiple-shot diffusion-weighted imaging (8, 6, 4, and 2 shots, respectively). The apparent diffusion coefficient (ADC) values, signal to noise ratio (SNR) and contrast to noise ratio (CNR) of bilateral cerebellum, brainstem and pons were measured or calculated. A five-point scoring method was used by two observers to subjectively evaluate the image quality. The Kappa test was adopted to evaluate the consistency of the scores by the two observers. The differences of ADC, SNR, CNR and subjective scores among MS-EPI DWI with different number of shots and SS-EPI DWI were analyzed using Friedman test. If the differences were statistically significant, subsequent multiple comparisons were performed with Bonferroni correction for P values.Results The scores by the two observers were in good agreement (Kappa=0.795, 0.871, 0.782, 0.880, 0.847). Compared with different shot times of MS-EPI DWI, there was no significant difference in ADC between the two sides of the cerebellum, and there was statistical difference in the rest of the data (P<0.05). Compared with the SS-EPI DWI sequence, when the number of shots was 8, the ADC in the left brainstem and pons was smaller than that in the SS-EPI DWI (P<0.05), and when the number of shots was 4 and 2, the ADC in the bilateral brainstem and pons was smaller than that in the SS-EPI DWI (P<0.05). When the number of shots was 8, 6, and 2, the SNR, CNR and subjective scores of both sides of the cerebellum and pons and brain stem of MS-EPI DWI were higher than those of SS-EPI DWI. When the number of shots was 6, the SNR and CNR of the left cerebellum and pontine stem, the SNR and CNR of the right cerebellum, the SNR of the right pontine stem and subjective scores were significantly different from those of SS-EPI DWI (P<0.05).Conclusions Compared with SS-EPI DWI, MS-EPI DWI based on IRIS that showed higher SNR and lower geometric distortion compared with SS-EPI DWI. MS-EPI DWI shots 6 is recommended for clinical skull base between imaging time and image quality.
[关键词] 颅底;扩散加权成像;空间采样的图像重建;磁共振成像;激发次数;多次激发平面回波成像
[Keywords] skull base;diffusion weighted imaging;image reconstruction using image-space sampling;magnetic resonance imaging;number of shots;multi-shot echo planar imaging

罗贺丹 1   张浩南 1   胡帅 1   卢绪论 1   王楠 1   苗延巍 1   刘爱连 1   林良杰 2   宋清伟 1*  

1 大连医科大学附属第一医院放射科,大连 116000

2 飞利浦(中国)投资有限公司,上海 200072

*宋清伟,E-mail:songqw1964@163.com

作者利益冲突声明:全部作者均声明无利益冲突。


基金项目: 辽宁省教育厅基金项目 LJKZ0856 横向课题基金项目 2021HZ006
收稿日期:2022-06-13
接受日期:2022-08-19
中图分类号:R445.2  R741 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.09.014
本文引用格式:罗贺丹, 张浩南, 胡帅, 等. 多次激发平面回波扩散加权成像在颅底成像中的应用[J]. 磁共振成像, 2022, 13(9): 75-80. DOI:10.12015/issn.1674-8034.2022.09.014

       扩散加权成像(diffusion weighted imaging, DWI)能够无创地将水分子的扩散特性量化为表观扩散系数(apparent diffusion coefficient, ADC),在评估颅脑病变方面有非常重要的应用价值[1, 2, 3]。常规DWI采用单次激发平面回波成像(single shot-echo planar imaging, SS-EPI)技术,可以检测急性脑梗塞、肿瘤、炎症等多种病变[4, 5, 6]。然而,传统SS-EPI DWI沿相位编码方向额外的相位累积会导致图像几何失真,尤其在颅底岩骨周围、额窦、颞叶、脑桥脑干等组织交界处,受磁场不均匀的影响,几何畸变更加明显。另外,由于相对较长的读出时间,使信号衰减而容易出现模糊伪影,影响颅底部病变的检出[7, 8, 9]。多次激发平面回波扩散加权成像(multi-shot echo planar imaging diffusion weighted imaging, MS-EPI DWI)通过激发次数的增加提高了图像分辨率,并减少了几何失真,对病变更加敏感。目前MS-EPI DWI已在神经系统、乳腺、盆腔等部位的应用中取得了较好的效果[10, 11, 12],并对头颈部鳞状细胞癌的结节转移[13]、中耳胆脂瘤等病变具有较高敏感度[14]。然而,MS-EPI DWI序列受到扫描设备硬件和软件的制约扫描时间比较长[11],无法配合的老人、小孩和危重患者难以耐受长时间检查,临床应用受限,国外主要集中于单一MS-EPI DWI和单激发平面回波扩散加权成像(single-shot echo planar imaging diffusion weighted imaging, SS-EPI DWI)的对比研究,而并未对MS-EPI DWI的不同激发次数进行比较研究。因此,本研究通过对SS-EPI DWI和不同激发次数(8、6、4、2)的MS-EPI DWI图像进行主观评分和客观评估,拟探讨MS-EPI DWI对颅底区域DWI图像质量的影响,并寻找适用于临床最佳的激发次数,有效缩短MS-EPI DWI扫描时间,提高检查成功率。

1 材料与方法

1.1 一般资料

       前瞻性招募2021年12月至2022年5月在大连医科大学附属第一医院行头部磁共振检查的健康志愿者49例,其中男30例,女19例,年龄13~77(42.00±19.39)岁。纳入标准:(1)无颅脑部手术史;(2)颅脑部无金属植入物。排除标准:(1)MR禁忌证;(2)无法配合MR检查。本研究经大连医科大学附属第一医院伦理委员会批准(审批文号:PJ-KS-KY-2022-169),全体受试者均签署了知情同意书。

1.2 检查方法

       所有受试者均使用Philips Ingenia CX 3.0 T MRI扫描仪(Philips Healthcare,Best,the Netherlands),配备32通道相控阵头部线圈。扫描序列包括常规SS-EPI DWI序列和基于图像空间采样重建算法(image reconstruction using image-space sampling, IRIS)的MS-EPI DWI序列(激发次数分别为8、6、4、2)。扫描同时完成b=0 s/mm2和b=1000 s/mm2的图像重建,ADC 图为自动生成,其他所有参数保持不变,FOV 184 mm×226 mm,分辨率1.6 mm×2.04 mm×6.5 mm,扫描参数见表1

表1  各序列扫描参数
Tab. 1  Scan parameters of each sequence

1.3 数据测量及分析

1.3.1 数据测量

       将扫描所得图像传至ISP(Philips,IntelliSpace Portall Version 9.0)工作站,在b=1000 s/mm2和ADC图像小脑最大层面两侧各划定三个感兴趣区(region of interest, ROI),大小10~20 mm2,分别测量信号值(signal intensity, SI)和ADC值,测量区域为小脑及脑干脑桥左右两侧相同位置的脑实质。在齿状核最大层面两侧各划定两个ROI,ROI大小5~8 mm2,测量齿状核SI和噪声强度(standard deviation, SD)。上述测量均取平均值,计算信噪比(signal to noise ratio, SNR)和对比噪声比(contrast to noise ratio, CNR)。

1.3.2 主观评分

       两位观察者(从事MR工作6年、5年的副主任医师)根据解剖结构细节可见度、图像噪声及几何形变大小以及诊断准确性采用五分评分法对图像质量进行评价(表2[15],3分及3分以上满足诊断要求。

表2  主观评分表
Tab. 2  Subjective score criteria system

1.4 统计学分析

       使用统计软件包SPSS 26.0对数据进行分析。使用Kappa检验两观察者评分的一致性,Kappa≥0.75认为一致性良好。若一致性良好,选择高年资医师主观评分进行后续分析。使用Friedman检验MS-EPI DWI组不同激发次数序列之间两侧小脑、脑干脑桥ADC、SNR、CNR及主观评分差异性。其中P<0.05认为各组之间差异具有统计学意义。若Friedman检验发现存在差异性,进行后续多重比较并对P值做Bonferroni校正。

2 结果

2.1 主观评分一致性检验

       两观察者图像质量主观评分具有良好的一致性(Kappa=0.795、0.871、0.782、0.880、0.847,表3),选择观察者一的主观评分进行后续分析。

表3  两观察者主观评分
Tab. 3  Subjective scores of two observers

2.2 客观评估及主观评分差异性检验

2.2.1 ADC值比较

       基于Friedman检验结果发现,在MS-EPI DWI不同激发次数之间,两侧小脑ADC差异无统计学意义(P>0.05),其余数据差异有统计学意义(P<0.05,表4)。两两比较结果表明,当激发次数为8时,MS-EPI DWI序列左侧脑桥脑干ADC较SS-EPI DWI序列差异有统计学意义(P<0.05),当激发次数为4、2时两侧脑桥脑干ADC较SS-EPI DWI序列差异有统计学意义(P<0.05,表5)。

表4  不同激发次数客观评估以及主观评分的差异性比较(Friedman检验)
Tab. 4  Comparison of objective measurements and subjective evaluation of among DWI with different shots of excitation by Friedman test
表5  不同激发次数客观评估以及主观评分两两比较(P值)
Tab. 5  Pairwise comparison of objective measurement and subjective scores between DWI with different shots of excitation (P value)

2.2.2 SNR、CNR值及主观评分比较

       SNR、CNR及主观评分比较见图1。Friedman检验结果表明,MS-EPI DWI序列不同激发次数之间各部位SNR、CNR差异均有统计学意义(P<0.05,表4)。与SS-EPI DWI序列相比,当激发次数为8、6、2时,MS-EPI DWI序列SNR、CNR及主观评分均大于SS-EPI DWI序列;当激发次数为8时,右侧小脑CNR和右侧脑桥脑干SNR、CNR及主观评分较SS-EPI DWI序列差异有统计学意义(P<0.05,表5);当激发次数为6时,各部位SNR、CNR及主观评分较SS-EPI DWI序列差异均有统计学意义(P<0.05,表5);当激发次数为4时,两侧脑桥脑干CNR较SS-EPI DWI序列差异无统计学意义(P>0.05),其他数据及主观评分差异均有统计学意义(P<0.05,表5);当激发次数为2时,左侧小脑SNR、CNR和右侧小脑CNR,右侧脑桥脑干SNR较SS-EPI DWI序列差异有统计学意义(P<0.05,表5)。

图1  SNR、CNR 值及主观评分比较DWI 序列图。1A~1E:分别为SS-EPIDWI, MS-EPI DWI 8 次激发, MS-EPI DWI 6 次激发, MS-EPI DWI 4 次激发,MS-EPI DWI 2次激发图,1A可见颅底部脑干、颞叶明显的几何畸变,1B、1C几何畸变明显改善,1D、1E改善不显著;1F:在SS-EPI DWI b=1000 s/mm2图像上划取ROI 测量两侧小脑和脑桥脑干SI 值。SNR:信噪比;CNR:对比噪声比;DWI:扩散加权成像;SS-EPI DWI:单次激发平面回波扩散加权成像;MS-EPIDWI:多次激发平面回波扩散加权成像;ROI:感兴趣区;SI:信号值。
Fig. 1  Comparison of SNR with CNR values and subjective scores. 1A-1E are SS-EPI DWI, MS-EPI DWI 8shots, MS-EPI DWI 6shots, MS-EPI DWI 4shots, MS-EPI DWI 2shots. 1A shows the brain stem at the base of the skull, obvious geometric aberrations in the temporal lobe, and the geometric distortions in 1B and 1C were significantly improved. 1D and 1E did not improve significantly. 1F are ROIs drawn on SS-EPI DWI b=1000 s/mm2 image to measure the SI values of the cerebellum and pontine brainstem on both sides. SNR: signal to noise ratio; CNR: contrast to noise ratio; DWI: diffusion weighted imaging; SS-EPI DWI: single-shot echo planar imaging diffusion weighted imaging; MS-EPI DWI: multi-shot echo planar imaging diffusion weighted imaging; ROI: region of interest; SI: signal intensity.

3 讨论

       既往研究表明[16, 17],MS-EPI DWI可以更准确地检测颅底部病灶的形态和位置。然而,随着激发次数的增加,MS-EPI DWI扫描时间显著增加。本研究将MS-EPI DWI应用于颅底扫描,寻找适用于临床最佳的激发次数。结果表明,MS-EPI DWI序列,两侧小脑ADC值差异无统计学意义(P>0.05),脑桥脑干处ADC较常规DWI序列差异有统计学意义(P<0.05);当MS-EPI DWI序列的激发次数为6时,SNR、CNR和主观评分均高于SS-EPI DWI序列,且图像的几何畸变明显减小。本研究的创新性在于将不同激发次数的MS-EPI DWI与传统SS-EPI DWI进行评估与对比,优化适合临床应用的激发次数,以在短时间内获得畸变小、质量高的颅底部DWI图像,具有较好的临床应用前景。

3.1 MS-EPI DWI序列的相关研究及优越性

       DWI序列在常规MRI序列的基础上,x、y、z三个方向施加扩散敏感梯度,将水的扩散特性量化为ADC,从而反映人体内水分子扩散运动情况[18, 19, 20]。Ogawa等[21]证明SS-EPI DWI序列可作为临床评估手术切除颅底侵犯头颈部肿瘤的重要指标。Norri等[22]和Guler等[23]发现SS-EPI DWI提高了筛查部分头颈部病变的敏感性和特异性,例如胆脂瘤、表皮样囊肿、脓肿等。MS-EPI DWI是DWI技术的一项创新,具有图像分辨率高、T2模糊效应少等优势[10]。也有研究者将多激发平面回波扩散张量成像(multi-shot echo planar imaging diffusion tensor imaging, MS-EPI DTI)应用于脊髓可改善线性失真和减小几何畸变,提高诊断准确率[24, 25]。Zhang等[16]和Steinhoff等[17]研究证明MS-EPI DWI可以减少图像失真、噪声水平和信号损失等,图像质量随激发次数增加而提高[16, 17]。本研究MS-EPI DWI采用IRIS在基于运动校正整合到并行采集框架的基础上,运用2D导航应用于MS-EPI DWI,在相位编码方向具有更高的带宽,可以减少几何失真,提高空间分辨率,从而为图像细节提供更高的保真度,提高了图像质量。

3.2 MS-EPI DWI与SS-EPI DWI的比较结果

       Kim等[26]对比了激发次数为2的MS-EPI DWI序列与SS-EPI DWI序列在肝脏部位的图像质量,发现MS-EPI DWI序列的图像噪声和失真更少,肝脏轮廓和病变显示清晰,对病灶显示具有较高的敏感性。Zhang等[27]纳入了75名骶髂关节炎的患者,通过MS-EPI DWI和SS-EPI DWI序列在骶髂关节主观和客观的比较研究,证明MS-EPI DWI序列图像质量明显提高,SNR和CNR均高于SS-EPI DWI序列,可作为骶髂关节MRI的常规扫描序列中使用。本研究通过主、客观评价对颅底部不同激发次数的MS-EPI DWI序列进行研究,两位独立观察者的主观评分kappa值均高于0.75,具有良好的一致性。激发次数为8次比激发次数为6次的图像质量有所下降(不显著),可能是扫描时间加长,带来的运动伪影的概率更大。有研究表明,MS-EPI DWI在相位编码方向上血液和脑脊液搏动可形成伪影[28]。本研究客观评估显示,当激发次数为8时,MS-EPI DWI序列图像的SNR、CNR普遍低于6次,血液和脑脊液搏动伪影较严重,导致噪声增加,数据的组合效果下降,这与既往研究一致。另外,在左侧小脑和脑桥脑干,MS-EPI DWI序列激发次数为2的CNR值大于激发次数为4的CNR,激发次数为4时左脑桥脑干的CNR小于SS-EPI DWI序列,可能是测量的背景齿状核解剖结构造成ROI勾画较小造成的噪声波动;当激发次数从6减少到2时,与SS-EPI DWI序列相比差异具有统计学意义(P<0.05)的部位逐步减少;当激发次数为6时,各部位ADC值与SS-EPI DWI相比差异无统计学意义(P>0.05),SNR、CNR及主观评分均高于SS-EPI DWI序列且差异均有统计学意义(P<0.05),该激发次数的图像质量较SS-EPI DWI序列明显提升;在扫描时间上,相对于激发次数为8的时间缩短了23.8%。本研究表明与SS-EPI DWI序列相比,MS-EPI DWI序列具有更好的整体图像质量,提高了图像清晰度,减少了几何畸变和图像失真,可以提供更多的诊断信息,几何畸变的减少有利于DWI和解剖图像之间更精准地匹配,更清楚地定义解剖边界。也可以为颅底部肿瘤放疗计划的制定和影像组学ROI的勾画提供精准的定位参考。

3.3 本研究的局限性

       MS-EPI DWI在相位编码方向上血液和脑脊液搏动可形成伪影[28],有待后续对此进行研究改进。本研究样本量较小并未对颅底病变受检者进行分组讨论,有待后续扩大样本量进一步研究。

       综上所述,对比传统SS-EPI DWI序列,基于IRIS的MS-EPI DWI技术可显著减少颅底部几何畸变和高信号伪影,对于颅底需要重点观察或怀疑病变时,可应用MS-EPI DWI序列。综合时间和图像质量的平衡,推荐使用激发次数为6的MS-EPI DWI序列行颅底扫描。

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