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综述
踝关节软骨损伤的功能磁共振成像研究进展
高艺洋 李相生

Cite this article as: Gao YY, Li XS. The latest research progress of functional MRI in traumatic cartilage injury of ankle joint[J]. Chin J Magn Reson Imaging, 2022, 13(9): 167-170.本文引用格式:高艺洋, 李相生. 踝关节软骨损伤的功能磁共振成像研究进展[J]. 磁共振成像, 2022, 13(9): 167-170. DOI:10.12015/issn.1674-8034.2022.09.040.


[摘要] 踝关节外伤后常引起关节软骨早期损伤,若关节软骨损伤没有得到早期诊断,可能会导致病情进一步恶化,诱发患者活动功能下降或障碍。目前,运用常规MRI扫描容易漏诊软骨损伤,并且很难定量评估软骨损伤程度,功能MRI(functional MRI, fMRI)可以反映关节软骨的病理生理学异常,在踝关节软骨损伤的早期诊断、严重程度分级等方面有较好的应用前景。为此,本文就踝关节软骨fMRI技术的临床应用最新进展进行综述,以拓宽fMRI在踝关节软骨早期诊断、疗效预测中的应用范围。
[Abstract] Ankle trauma often causes early injury of articular cartilage. If the articular cartilage injury is not diagnosed early, it may lead to further deterioration of the condition and induce a decrease or impairment of the patient's mobility. At present, it is easy to miss the diagnosis of cartilage injury by conventional MRI scanning, and it is difficult to quantitatively evaluate the degree of cartilage injury. However, functional MRI (fMRI) can reflect the pathophysiological abnormalities of articular cartilage, and it has a high application prospect in early diagnosis and severity grading of ankle cartilage injury. To address this issue, this paper reviews the latest advances in the clinical application of fMRI techniques of ankle cartilage, in order to broaden the application scope of fMRI in early diagnosis and curative effect prediction of ankle cartilage.
[关键词] 踝关节;关节软骨;损伤;功能磁共振成像;T1ρ成像;扩散张量成像;T1-mapping;延迟钆增强磁共振软骨成像;早期诊断
[Keywords] ankle joint;articular cartilage;trauma;functional magnetic resonance imaging;T1ρ imaging;diffusion tensor imaging;T1-mapping;delayed gadolinium-enhanced magnetic resonance imaging of cartilage;early diagnosis

高艺洋    李相生 *  

中国人民解放军空军特色医学中心医学影像科,北京 100142

*李相生,E-mail:lxsheng500@163.com

作者利益冲突声明:全部作者均声明无利益冲突。


收稿日期:2022-04-12
接受日期:2022-09-01
中图分类号:R445.2  R684 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.09.040
本文引用格式:高艺洋, 李相生. 踝关节软骨损伤的功能磁共振成像研究进展[J]. 磁共振成像, 2022, 13(9): 167-170. DOI:10.12015/issn.1674-8034.2022.09.040

       踝关节软骨损伤是足踝部常见的外伤性疾病之一,其病因多来源于外伤或缺血等因素。由于缺乏滋养血管,关节软骨的自身修复能力较弱,一旦发生损伤,关节软骨损伤很难完全修复,因此关节软骨的早期诊断和尽早治疗尤为重要。目前,MRI是临床上最常用的成像技术,可以显示软骨损伤的部位和范围。近年来,多种功能MRI(functional MRI, fMRI)技术开始应用于关节软骨成像,包括:T1ρ成像、扩散张量成像(diffusion tensor imaging,DTI)、T1-mapping、T2-mapping、T2*-mapping、延迟钆增强磁共振软骨成像(delayed gadolinium-enhanced magnetic resonance imaging of cartilage, dGEMRIC)等,在关节软骨早期诊断和病情监测中有较大的潜在价值。因此,本文就fMRI在踝关节软骨早期诊断的最新应用研究进展作一综述。

1 踝关节软骨损伤的病理生理学机制

       关节软骨主要由软骨细胞和软骨基质构成,软骨基质主要由葡胺聚糖和核心蛋白组成的蛋白多糖、胶原原纤维和水组成,软骨基质中的蛋白多糖主要由硫酸软骨素和透明质酸组成[1, 2, 3],这些结构复合体相互连接赋予了透明软骨特殊的生物力学特性,具有一定弹性,可以使关节软骨缓冲相连骨在运动时的震动和冲击[4],可以减少关节之间摩擦,从而减少关节面的损伤。目前,关节软骨的损伤机制还未完全明确,研究[5]表明,外伤是关节软骨损伤最常见的病因,但是其他非外伤原因也可以导致踝关节软骨损伤,例如:慢性踝关节不稳定、血管及滑膜损伤、微创伤、韧带松弛、自发坏死、激素失调、先天性因素或遗传因素、激素和酗酒等。

       当踝关节发生外伤后,关节软骨的生化代谢功能会发生变化。目前,关节软骨损伤的生化代谢机制有多种说法:(1)自由基机制。Zubavlenko等[6]、Chen等[7]认为,自由基会使软骨细胞发生氧化损伤,甚至细胞凋亡,也可氧化损伤蛋白多糖和Ⅱ型胶原,从而使其丧失对软骨细胞的保护支撑功能,软骨细胞和基质成分出现受损,软骨破坏和再生失衡,从而出现软骨损伤。(2)蛋白水解酶家族机制。基质金属蛋白酶-1(matrix metalloproteinase-1, MMP-1)能将所有细胞外基质水解,MMP-1是水解关节软骨Ⅱ型胶原能力最强的蛋白酶,而关节软骨细胞外基质中的主要成分就是Ⅱ型胶原。最近研究[8, 9, 10]表明,关节软骨损伤可导致软骨中的MMP-1含量增加,促使关节软骨损伤进一步加重。

2 常规MRI在踝关节软骨损伤诊断中的应用

       目前,踝关节软骨检查使用的常规MRI序列是T1WI、T2WI和质子加权(proton weighted, PD)成像序列,常规MRI序列图像可以显示骨关节周围肌肉和韧带的损伤,表现为软组织肿胀水肿、不同程度的韧带撕裂、骨髓腔内水肿以及关节腔积液。但是,常规MRI很难诊断关节软骨的早期损伤,尤其关节软骨的微小损伤。近期研究[11, 12, 13, 14]表明,fMRI可以反映关节软骨的生化代谢异常以及病理生理学变化,有望依据关节软骨的生化代谢异常情况来早期诊断软骨损伤以及判断软骨损伤的严重程度,据此指导临床治疗方案设计或预测疗效,避免病变进一步发展,改善软骨损伤患者的预后。

3 多模态fMRI在踝关节软骨早期诊断中的应用

3.1 T1ρ成像

       T1ρ成像即自旋锁定成像,T1ρ弛豫是指在旋转坐标系基础下的自旋晶格时间,当人体内大分子物质与水分子相互结合时,产生能量和质子交换的相互作用,这种作用就会引起T1ρ弛豫。T1ρ值可以反映自由水和结合水的相互作用,根据T1ρ值变化可以检测关节软骨的早期退变及损伤,从而指导临床治疗和疗效预测,避免疾病的进一步发展。有关研究[15, 16, 17]显示,关节软骨退变及损伤程度越严重,T1ρ值越大,在关节软骨损伤后发生形态改变之前,即可早期检测关节软骨基质的异常变化。Baboli等[17]、Wikstrom等[18]利用T1ρ序列对踝关节不稳患者进行研究结果表明,踝关节不稳患者的T1ρ值及变异率较正常人显著增加,利用T1ρ成像可以发现踝关节软骨早期损伤。Taylor等[19]、Rossom等[20]研究表明,日常运动也会影响T1ρ值的高低,晚上比早晨扫描获得的T1ρ值上升了7%,因此,日常运动所造成的关节负荷也会影响T1ρ值。但是,T1ρ成像存在一些技术局限性,如:扫描时间较长、稳定性较差,软骨损伤后T1ρ发生改变的理论机制和影响因素还不完全清楚。

3.2 T1-mapping、T2-mapping和T2*-mapping

       T1-mapping是一种通过计算关节软骨内T1值来量化评估软骨内生化改变的成像技术。Shiguetomi-Medina等[21, 22]研究结果证实,T1值变化与关节软骨内水分子的变化有较高的相关性,而软骨内水分子增多是关节软骨早期损伤的表现之一,通过T1-mapping成像序列,可以在软骨尚未发生形态学改变之前诊断早期损伤。有学者[23, 24, 25]研究结果显示,T1-mapping成像序列显著提高了关节软骨早期损伤的诊断敏感度,但其需要与常规MRI序列联合使用,并且其结果与关节镜检查的结果有一定程度的差异。

       T2-mapping、T2*-mapping成像均采用多层面多回波自旋回波序列,在一个重复时间(repetition time, TR)内采集多个回波时间(echo time, TE)获得影像学数据,最终利用软件计算出病变部位的T2、T2*弛豫时间。T2-mapping序列对关节软骨内的胶原纤维含量及其排列方式、水含量及软骨应力变化等比较敏感[26, 27, 28],可以通过计算T2值来量化评估关节软骨的微观变化,从而实现关节软骨损伤及退变的早期诊断。有研究[29, 30, 31]发现,关节软骨的退变程度与T2值大小呈正相关,即关节软骨退变越严重T2值越大。韩晓兵等[32]研究发现,军人的日常训练对踝关节软骨有一定的影响,军人接受半年左右的体能训练后,胫距关节软骨的平均T2值会高于普通正常青年人,其病理生理学基础为长时间军事训练使得关节软骨内胶原纤维排列顺序及数量发生改变,最终导致自由水增多,促使T2值增加。但T2-mapping成像也有一定技术局限性,例如:扫描时间过长、魔角效应以及对关节软骨早期退变的诊断敏感度较低。

       与T2-mapping序列相比,T2*-mapping序列没有使用180°聚相位脉冲,其TE值比T2-mapping更小,扫描时间更短,图像分辨率更高。因此,T2*-mapping对软骨内胶原蛋白的评价更为敏感,能够更真实反映T2值的大小。有研究[33, 34, 35]使用T2*-mapping对髋关节软骨进行研究,当关节软骨受到损伤时,细胞外基质中的胶原纤维会减少,水分子含量增多,T2值会更高。因此,该成像技术可以更敏感地诊断关节软骨的早期损伤,甚至优于关节镜检查。Morgan等[36, 37]、Weber等[38]使用T2*-mapping对髋关节软骨进行评估的研究发现,T2*-mapping无创、敏感性较高,有望取代关节镜检查方法。Hu等[39]认为,在距骨穹隆和距下关节损伤后,使用T2*-mapping序列可以评估手术后的软骨修复效果,但是,Oei等[40]研究显示T2*-mapping成像参数容易受到魔角效应的影响,魔角效应一般存在于排列高度整齐有序的组织中,而关节软骨中的胶原纤维呈平行排列,当胶原纤维与主磁场呈55°角时会使得T2*弛豫时间增加,最终导致T2*值升高[41];另外,T2*-mapping容易受到磁敏感性伪影的影响。

3.3 dGEMRIC

       dGEMRIC是利用钆对比剂增强成像来评估关节软骨内分子改变,属于一种分子成像技术,可以实现量化评估软骨内蛋白多糖含量变化。当关节软骨出现早期退变时,软骨内蛋白多糖会减少,关节软骨内阴离子明显减少,而顺磁性钆对比剂带有负电荷,可以通过渗透作用进入损伤部位代替蛋白多糖,最终表现为T1值减小[42]。Sigudsson等[43]、Hangaard等[44]研究发现dGEMRIC最好是在注射对比剂之前和2 h后进行一次检查,这样可以使图像更有对比性,并且还发现不同损伤阶段的关节软骨可能对应着不同的dGEMRIC模型,这就意味着dGEMRIC可以对关节软骨损伤程度进行分级。但是,此成像技术需要使用双倍钆对比剂,而研究显示[45, 46, 47]钆对比剂对人体有一定的影响,可能发生肾源性系统性纤维化,这主要在使用钆对比剂后出现严重慢性或急性肾功能衰竭的患者中观察到,因此检查前需要注意患者是否有基础疾病,还需要患者配合关节运动才能使对比剂更好地被吸收。

3.4 DTI

       DTI是通过测量各向异性分数(fractional anisotropy, FA)来量化评估关节软骨内水分子的扩散程度变化,DTI序列与扩散加权成像(diffusion-weighted imaging, DWI)序列成像原理一致,是以水分子布朗运动为基础,FA值越接近于0,组织水分子扩散越不受限。研究发现[48, 49, 50],DWI联合DTI序列可以检出还未出现形态学改变的软骨早期损伤,由于软骨损伤会破坏胶原纤维,影响水分子的异向扩散,最终导致患者的FA值降低。研究显示[51, 52],存在骨软骨早期损伤的患者,FA值明显低于正常人群,其准确性与关节镜检出的早期损伤接近,DTI序列检出关节软骨早期损伤的准确率高达83.6%,说明DTI序列在检测关节软骨早期损伤中具有较高的应用价值。

       综上所述,踝关节受到外伤后,关节软骨层损伤的早期诊断至关重要,直接决定着患者的预后。由于踝关节软骨大多呈不规则形,有一定曲度,普通关节镜很难显示侧面的微小损伤及早期损伤,而fMRI可以量化评价软骨的病理生理学特点和生化代谢情况,可以大大提高关节软骨损伤的检出率和准确性,尤其是在关节软骨还未出现明确的形态变化之前,为尽早治疗和干预提供重要的判断依据。我们相信,随着多模态fMRI技术的不断优化和完善,图像质量会不断提高,对关节软骨的量化评价更敏感、更准确,有望在踝关节软骨损伤的早期诊断、严重程度分级和疗效预测方面发挥更大作用,从而指导临床治疗,改善患者预后。

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