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临床研究
T2* mapping功能磁共振成像定量评估糖尿病性黄斑水肿视网膜出血的价值
王叶红 邵举薇 李磊 李建波 张利伟 熊煜欣 杨莹 杨梦维 苏伟

Cite this article as: Wang YH, Shao JW, Li L, et al. Value of T2* mapping MRI in quantitative assessment of diabetic macular edema with retinal hemorrhage[J]. Chin J Magn Reson Imaging, 2022, 13(11): 66-70, 81.本文引用格式:王叶红, 邵举薇, 李磊, 等. T2* mapping功能磁共振成像定量评估糖尿病性黄斑水肿视网膜出血的价值[J]. 磁共振成像, 2022, 13(11): 66-70, 81. DOI:10.12015/issn.1674-8034.2022.11.012.


[摘要] 目的 探讨T2* mapping功能MRI技术定量分析糖尿病性黄斑水肿(diabetic macular edema, DME)的可行性及其价值。材料与方法 前瞻性纳入2020年10月至2021年12月于云南大学附属医院诊断为DME的患者30人(36只眼)作为病例组,其中合并视网膜出血组26只眼,不合并视网膜出血组10只眼。选择20名(39只眼)健康志愿者作为对照组。对两组行磁共振检查,包括眼眶轴位、冠状位T2WI、矢状位T1WI、轴位T2* mapping扫描。在视网膜上6个区域[视盘区、黄斑区、外直肌眼环附着点(颞侧)、内直肌眼环附着点(鼻侧)、视盘区与颞侧的中点(颞中)、视盘区与鼻侧的中点(鼻中)]及对应视网膜前方6个区域选取感兴趣区(region of interest, ROI),大小为1 mm2。各组不同区域T2*值采用Kruskal-Wallis检验,如差异有统计学意义,再使用最小显著差异(least significant difference, LSD)t检验进行组间比较。使用组内/组间相关系数(intra- /inter- class correlation coefficient, ICC)分析观察者内及观察者间的一致性。结果 合并视网膜出血组与对照组比较视网膜区(视盘区、黄斑区、颞侧、鼻侧、颞中、鼻中)、视网膜前区(黄斑区、颞侧、鼻侧、颞中、鼻中)T2*值差异具有统计学意义(P<0.05);合并视网膜出血组与不合并视网膜出血组比较视网膜区(视盘区、黄斑区、颞中、鼻中)、视网膜前区(黄斑区、颞侧、鼻侧、颞中)T2*值差异具有统计学意义(P<0.05);不合并视网膜出血组与对照组比较视网膜区(视盘区、颞侧)T2*值差异具有统计学意义(P<0.05)。结论 磁共振T2* mapping技术可以敏感且定量地反映DME视网膜出血情况,在DME的诊断、疾病监测及治疗疗效判断方面具有重要临床价值。
[Abstract] Objective To investigate the value and feasibility of T2* mapping MRI in evaluating diabetic macular edema (DME).Materials and Methods Thirty patients (36 eyes) with DME (patient group) in the Affiliated Hospital of Yunnan University from October 2020 to December 2021 were prospectively enrolled,including a group of 26 eyes with retinal hemorrhage and a group of 10 eyes without retinal hemorrhage. Twenty healthy volunteers (39 eyes) were collected as the control group. Axial T2WI, coronal T2WI, sagittal T1WI and axial T2* mapping MRI were performed between the two groups. Six regions of interest (ROIs) were drawn at the retina region: optic disc sector, macula sector, the attachment point of lateral rectus muscle eye ring (temporal side), the attachment point of medial rectus muscle eye ring (nasal side), the midpoint of optic disc sector and temporal side (MOT), the midpoint of optic disc sector and nasal side (MON) and 6 ROIs were drawn in front of the retina (ROI size 1 mm2). Statistical analyses among multiple groups were conducted using one-way analysis of variance and the Kruskal-Wallis test.Results The T2* value of the retina region (optic disc sector, macula sector, temporal side, nasal side, MON, MOT) and those in front of the retina (macula sector, temporal side, nasal side, MON, MOT) was statistically significant between the retinal hemorrhage group and the control group (P<0.05). The T2* value of the retina region (optic disc sector, macula sector, MON, MOT) and those in front of the retina (macula sector, temporal side, nasal side, MOT) was statistically significant between the retinal hemorrhage group and the group without retinal hemorrhage (P<0.05). The T2* value of the retina region (optic disc sector, temporal side) was statistically significant between the group without retinal hemorrhage and the control group (P<0.05).Conclusions T2* mapping MRI can sensitively and quantitatively assess the retinal hemorrhage of DME, and has a high value in diagnosis, monitoring progression and therapeutic effect of DME.
[关键词] 糖尿病性黄斑水肿;视网膜出血;磁共振成像;功能磁共振成像;T2* mapping;定量评估
[Keywords] diabetic macular edema;retinal hemorrhage;magnetic resonance imaging;functional magnetic resonance imaging;T2* mapping;quantitative assessment

王叶红 1   邵举薇 1   李磊 1   李建波 1   张利伟 2   熊煜欣 3   杨莹 3   杨梦维 1   苏伟 1*  

1 云南大学附属医院放射科,昆明 650021

2 云南大学附属医院眼科,昆明 650021

3 云南大学附属医院内分泌科,昆明 650021

苏伟,E-mail:13619634911@163.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: 2020中华国际医学交流基金会影像科研基金 Z-2014-07-2003-12
收稿日期:2022-06-09
接受日期:2022-11-04
中图分类号:R445.2  R781.64  R774 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.11.012
本文引用格式:王叶红, 邵举薇, 李磊, 等. T2* mapping功能磁共振成像定量评估糖尿病性黄斑水肿视网膜出血的价值[J]. 磁共振成像, 2022, 13(11): 66-70, 81. DOI:10.12015/issn.1674-8034.2022.11.012

       糖尿病性黄斑水肿(diabetic macular edema, DME)是指血脂、血糖等代谢异常造成血-视网膜屏障破坏,渗漏的液体在视网膜黄斑区积聚,引起视力下降并最终造成失明的疾病[1],是糖尿病性视网膜病变(diabetic retinopathy, DR)最常见的并发症之一。根据DR是否出现血管病变和新生血管,将其分非增殖期DR和增殖期DR[2]。增殖期DR是以视网膜病理性新生血管和纤维血管增殖膜形成为特征的晚期DR,病理性新生血管渗漏的液体在黄斑区视网膜内积聚可造成视力受损,其渗出的血液和/或纤维血管增殖膜牵拉,会造成视网膜脱离而严重影响视力[3, 4]。目前DME眼底出血的临床检查方法主要有彩色眼底照相和超广角成像,但二者均属于结构性评估,目前临床缺乏功能性定量评估手段。而T2* mapping能非侵入性地可视化、量化组织成分(如水肿、出血),反映组织生化成分及微结构改变,目前已被广泛应用于心脏疾病的临床研究[5, 6, 7],并逐渐扩展至肝脏、胰腺、肾脏、前列腺、下肢、软骨及卵巢等[8, 9, 10, 11, 12, 13, 14, 15, 16]部位,但尚未用于评估眼部疾病。本研究旨在探讨T2* mapping功能MRI技术定量分析DME伴眼底出血的可行性及其价值。

1 材料与方法

1.1 研究对象

       前瞻性招募2020年10月至2021年12月在云南大学附属医院就诊且临床诊断为DME患者30例为病例组,根据是否合并视网膜出血分为合并视网膜出血组、不合并视网膜出血组。另选择20名年龄、性别与病例组相匹配的健康志愿者作为对照组,招募志愿者为医院职工及其家属。本研究遵守《赫尔辛基宣言》,并经云南大学附属医院伦理委员会审核同意(编号:2020147),所有受检者均签署了知情同意书。

1.2 纳排标准

       病例组纳入标准:(1)经内分泌科检查确诊为2型糖尿病患者;(2)经临床光学相干断层扫描(optical coherence tomography, OCT)、眼底荧光素血管造影等检查确诊为DME的患者,视网膜出血患者为广泛眼底出血。病例组排除标准:(1)既往有玻璃体内药物注射、除激光治疗外的眼科手术史;(2)患有其他眼底疾病或眼部肿瘤等眼病者;(3)磁共振检查禁忌证,如人工耳蜗植入和幽闭恐惧症患者;(4)影像质量未达到评估要求。

       对照组纳入标准:(1)无糖尿病、高血压、眼底疾病病史;(2)血压测量、糖化血红蛋白检测、眼底照相检查结果正常。对照组排除标准:(1)磁共振检查禁忌证,如人工耳蜗植入和幽闭恐惧症患者;(2)影像质量未达到评估要求。

1.3 磁共振检查方法

       磁共振数据采集采用3.0 T(PHILIPS Ingenia)磁共振仪及32通道头线圈。扫描序列包括眼眶轴位、冠状位T2WI、矢状位T1WI、轴位T2* mapping扫描,其中轴位T2WI采用压脂序列,轴位T2* mapping添加饱和带进行扫描。取仰卧位、头先进,使用海绵垫固定头部,双眼外压小米袋帮助固定眼球位置,参照心脏磁共振扫描方式连接心脏电极片。扫描前告知受检者扫描过程中的注意事项,保持双眼正视正前方,然后轻轻闭合,保持放松。扫描过程中,要求患者保持眼球不旋转。扫描图像尽量保证视神经、内直肌、外直肌、晶状体在同一层面,剔除影像质量未达到评估要求者。磁共振扫描主要参数见表1

表1  磁共振扫描序列及主要参数
Tab. 1  The main imaging parameters of magnetic resonance imaging sequence

1.4 图像后处理和图像分析

       将图像传入3.0 T磁共振(PHILIPS Ingenia)后处理工作站,由两名具有5年以上经验的头颈部影像诊断医生(均为副主任医师)独立测量,取平均值。参照Ma等[17]和许庆刚等[18]研究中感兴趣区(region of interest, ROI)的勾画方法,结合本研究具体情况制订ROI勾画标准:在视网膜区勾画6个ROI,包括视盘区、黄斑区、外直肌眼环附着点(颞侧)、内直径眼环附着点(鼻侧)、视盘区与颞侧中点(颞中)、视盘区与鼻侧中点(鼻中),接着在紧邻视网膜区前方勾画6个ROI,最后将所有ROI复制到功能图测值。ROI具体勾画及T2* mapping功能伪彩图见图1。

图1  感兴趣区(ROI)具体勾画及T2* mapping功能测值示意图。1A、1B、1C分别为T2WI压脂序列、T2* mapping功能图、T2* mapping伪彩图。黄色圆圈代表视网膜区;红色圆圈代表视网膜前区;a:鼻侧;b:视盘区;c:黄斑区;d:颞侧;e:鼻中;f:颞中。
Fig. 1  Detailed delineation of the region of interest (ROI) and schematic diagram of T2* mapping function measurement. 1A, 1B, 1C are respectively fat-saturated T2 weighted imaging, T2* mapping function diagram, and T2* mapping color map. The yellow circle represents the retina region and the red circle represents the ante-retina region. a: nasal side; b: optic disc sector; c: macula sector; d: temporal side; e: the midpoint of optic disc sector and nasal side (MON); f: the midpoint of optic disc sector and temporal side (MOT).

1.5 统计学分析

       统计学分析采用IBM SPSS 25.0统计软件。定量资料符合正态分布,采用均数±标准差(x¯±s)表示;采用Fisher确切概率法比较性别差异;多组比较采用单因素方差分析或Kruskal-Wallis检验。Kruskal-Wallis检验时,如差异有统计学意义,再使用最小显著差异(least significant difference, LSD)t检验两两比较。使用组内/组间相关系数(intra- /inter -class correlation coefficient, ICC)分析观察者内及观察者间的一致性。以P<0.05为差异有统计学意义。

2 结果

2.1 临床一般资料

       根据纳排标准,病例组共纳入DME患者30例(36只眼),其中:合并视网膜出血组22例(26只眼),男14例,女8例,年龄(54.96±6.79)岁;不合并视网膜出血组8例(10只眼)男6例,女2例,年龄(50.10±9.95)岁。对照组纳入20例(39只眼),其中:男13例,女7例,年龄(50.90±8.05)岁。合并视网膜出血组、不合并视网膜出血组、对照组的性别(χ2=0.363)、年龄(F=2.191)差异均无统计学意义(P>0.05)。

2.2 各组T2*值结果

       合并视网膜出血组、不合并视网膜底出血组和对照组T2*值比较(表2):视网膜区(视盘区、黄斑区、颞侧、鼻侧、颞中、鼻中)、视网膜前区(黄斑区、颞侧、鼻侧、颞中、鼻中)差异具有统计学意义(P<0.05)。观察者内及观察者间具有良好的一致性[ICC(组内)=0.971、ICC(组间)=0.962]。

       组间多重比较显示(表3图2):合并视网膜出血组与不合并视网膜出血组比较视网膜区(视盘区、黄斑区、颞中、鼻中)、视网膜前区(黄斑区、颞侧、鼻侧、颞中)T2*值差异具有统计学意义(P<0.05);合并视网膜出血组与对照组比较视网膜区(视盘区、黄斑区、颞侧、鼻侧、颞中、鼻中)、视网膜前区(黄斑区、颞侧、鼻侧、颞中、鼻中)T2*值差异具有统计学意义(P<0.05);不合并视网膜出血组与对照组比较视网膜区(视盘区、颞侧)T2*值差异具有统计学意义(P<0.05)。

图2  三组视网膜区、视网膜前区的T2*值柱状图。*P<0.05。
Fig. 2  The T2* values among the three groups in retina region and ante-retina region. *: P<0.05.
表2  三组视网膜区、视网膜前区T2*值比较
Tab. 2  Comparison of T2* values among the three groups in the retina region and the ante-retina region
表3  T2*值组间多重比较
Tab. 3  Multiple comparison of T2* values among the three groups

2.3 眼底照相

       对照组与合并视网膜出血组眼底照相结果比较(图3):对照组眼底正常,合并视网膜出血组眼底出血较明显。本研究中DME合并视网膜出血组患者视网膜出血均类似图3B所示,出血呈散在斑片状,而非仅仅黄斑区出血,故本研究选取多个ROI进行测值,意图对出血的判读更加准确、可靠。

图3  对照组与合并视网膜出血组彩色眼底照相。3A:对照组眼底照相,可见后极部网膜平伏,血管走行正常,未见明显出血、渗出,视乳头圆,边界清;3B:合并视网膜出血组眼底照相,可见后极部网膜平伏,黄斑血管弓处点片状渗出,散在微血管瘤,斑片状出血,视乳头圆,边界清。
Fig. 3  Fundus photography in the control group and the group with fundus hemorrhage. 3A: In the control group, the retina at the posterior pole is flat, the blood vessels run normally, no obvious bleeding or exudation is found, the optic papilla is round and the boundary is clear; 3B: Fundus photography in the group with fundus hemorrhage shows that the posterior pole omentum is flat and the macular vascular arch exuded in patches, scattered microangiopathy, patchy hemorrhage, the optic papilla is round with a clear boundary.

3 讨论

       磁共振T2* mapping技术目前较多应用于心脏疾病的研究,目前国内外尚未有学者将其应用于眼部疾病。本研究首次使用T2* mapping技术对DME合并视网膜出血组、不合并视网膜出血组和对照组进行研究,结果显示合并视网膜出血组在视网膜区(视盘区、黄斑区、颞中、鼻中)、视网膜前区(黄斑区、颞侧、鼻侧、颞中)T2*值明显低于对照组(P<0.05);不合并视网膜出血组在视网膜区(视盘区、颞侧)T2*值明显低于对照组(P<0.05)。本研究首次提出T2* mapping技术在一定程度上可以定量评估DME合并视网膜出血,且早于眼底照相检查。该技术观察范围广泛且可定量,在眼部疾病早诊断、早治疗及监测疗效方面可提供重要临床价值。

3.1 T2* mapping技术的原理与优势

       视网膜出血的精准评估对临床眼部疾病的早期诊断、早期治疗及监测疗效具有至关重要的指导意义。眼底照相、超广角眼底成像是临床中最常用的视网膜出血检查方法,但其仅用于观察眼底组织结构,且不能进行定量评估,诊断结果依赖医生的专业技能水平。虽然目前眼底照相联合AI技术在眼底疾病中应用广泛,但其主要通过测量出血面积来反映视网膜出血变化[19, 20, 21],对于出血量的判断不够精准,且无法对眼底照相未显示出血者进行评估。而磁共振T2* mapping技术能弥补前述眼底照相、超广角成像及AI的缺陷,体现其在视网膜出血判断方面的优势。目前,AI技术逐渐发展为DR的初筛手段[22, 23],若AI与T2* mapping技术联合,未来有望进一步提高眼底疾病的早期筛查。

       T2* mapping技术是通过多回波-梯度回波序列同时采集多个回波时间下的幅值信号,通过时间-信号曲线拟合得到T2* mapping伪彩图,从而测得T2*[24]。T2* mapping技术能非侵入性地可视化和量化组织成分(如自由水、脱氧血红蛋白、铁含量等),反映组织生化成分和微结构改变。当组织中自由水含量增加时,T2*值升高,出血引起铁含量减少时,T2*值降低[24, 25, 26, 27, 28, 29]。因此,不论该疾病是否引起结构改变,T2* mapping技术可量化组织成分而客观反映疾病。此外,T2* mapping技术扫描范围包括双侧眼球及眼眶,观察范围广泛,不仅可以观察眼底情况,还能观察眼球其他部位及眼眶整体情况,排除眼眶其他疾病,提高诊断准确率。

3.2 T2*值结果探讨

       本研究DME合并视网膜出血组在视网膜区的T2*值明显低于对照组。而杨超等[8]通过对经血清检查肝脏含铁量增高者进行研究发现,T2*值随着肝脏铁沉积的增加而减低。而心脏铁沉积与T2*值之间的关系已通过多项尸检或动物实验研究得到证实[24,30, 31]。DME视网膜组织水肿会引起T2*值升高,而本研究DME合并眼底出血组在视网膜区的T2*值明显低于对照组,推测在本研究中影响T2*值的主要因素可能为组织出血。视网膜出血造成组织铁含量增加,导致T2*值减低,进一步提示T2* mapping技术可以定量评估DME视网膜出血。考虑到视网膜出血可能部分渗入视网膜前区,在一定程度上影响患者视力,且这部分在眼底照相检查时很难观察到,因此本研究在视网膜前区选取ROI进行研究,结果显示视网膜前区(黄斑区、颞侧、鼻侧、颞中、鼻中)的T2*值明显低于对照组(P<0.05)。因此,本研究结果可在一定程度上提示视网膜区出血向玻璃体渗漏。DME不合并视网膜出血组在视网膜区(视盘区及颞侧)的T2*值明显低于对照组(P<0.05),推测在眼底照相显示出血征象之前,即在发生结构性改变之前,组织成分已发生变化并通过T2*值表现出来。因此可推测T2* mapping技术能早于眼底照相检查发现视网膜出血,可帮助临床早发现及治疗疾病。而本研究中部分ROI比较无意义,推测原因可能与样本量较小有关。

       本研究中采用ROI较多,通过前述研究结果提示视网膜区6个ROI最有助于视网膜出血的诊断,分析原因主要包括:(1)三组在视网膜区的ROI比较均有临床意义,而在视网膜前区仅部分ROI有临床意义;(2)视网膜区ROI主要反映视网膜区出血程度,而视网膜前区ROI主要反映视网膜区出血向玻璃体渗漏情况。

3.3 本研究的创新与不足

       不同于以往的研究,本研究首次将T2* mapping技术应用于眼部疾病,通过量化组织成分客观反映疾病。本研究首次采用视网膜区及视网膜前区勾画12个面积固定圆形ROI进行数据测量,具有以下优点:(1)ROI位置相对固定、面积固定,可减小误差;(2)选取ROI数目较多,考虑到视网膜在磁共振图像上没有明确分界,增加ROI数目以减小误差;(3)先在图像质量更好的结构图中勾画ROI,再粘贴至功能图,可减小测量误差。但本研究尚存在以下局限性:(1)样本量较少,在未来研究中需加大样本量;(2)手动勾画ROI存在一定误差,后续研究中采用其他方法如AI进一步改善;(3)本研究仅研究DME疾病,未来可扩展至其他眼底疾病的研究。

       综上所述,T2* mapping技术不仅能定量评估DME患者视网膜区出血程度,还能定量测量视网膜前区渗漏量,观察范围广泛,比眼底照相检查更早发现眼底出血,在疾病早诊断、早治疗方面提供重要临床价值。T2* mapping技术与AI联合,有望进一步提高眼底疾病的早期筛查率。此外,T2* mapping技术也有望在定量比较DME治疗疗效中发挥重要作用,未来可开展这方面的深入研究。

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